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Cutaneous leishmaniasis in Morocco: psychosocial burden and simplified diagnosis
Issam BENNIS
ISBN n° 978-90-5728-583-7 Legal deposit number D/2018/12.293/11 Cover design by Anita Muys (UA media service) Description of cover photo The cover photo shows a 6-month-old facial lesion of cutaneous leishmaniasis in a 7-year-old child living in the northern part of Morocco.
Cutaneous leishmaniasis in Morocco: psychosocial burden and simplified diagnosis Cutane leishmaniase in Marokko: psychosociale belasting en vereenvoudigde diagnose Dissertation submitted for the degree of Doctor of Biomedical Sciences at the University of Antwerp
Issam BENNIS
Promoters: Co-promoters: Prof. Dr. Jean-Claude Dujardin University of Antwerp Institute of Tropical Medicine Antwerp Prof. Dr. Marleen Boelaert Institute of Tropical Medicine Antwerp
Prof. Dr. Vincent De Brouwere Institute of Tropical Medicine Antwerp Prof. Dr. Hamid Sahibi Agricultural and Veterinary Institute Rabat
Antwerp – April 17th, 2018
Individual Doctorate Committee: Chair: Prof. Dr. Luc Kestens University of Antwerp, Antwerp, Belgium Members: Prof. Dr. Louis Maes University of Antwerp, Antwerp, Belgium Prof. Dr. Jean-Claude Dujardin University of Antwerp, Antwerp, Belgium Institute of Tropical Medicine, Antwerp, Belgium Prof. Dr. Marleen Boelaert Institute of Tropical Medicine, Antwerp, Belgium
External Jury Members: Prof. Dr. François Chappuis Geneva University Hospitals, Geneva, Zwitzerland Dr. José Antonio Ruiz Postigo World Health Organisation, Geneva, Zwitzerland
Internal Jury Members: Dr. Edwin Wouters University of Antwerp, Antwerp, Belgium
Table of Contents
Abbreviations
Summary............................................................................................................... 11
Samenvatting ........................................................................................................ 13
CHAPTER 1. General introduction ........................................................................... 15
1. Leishmaniasis, an overview ............................................................................ 17
2. Cutaneous leishmaniasis ................................................................................ 24
2.1 Clinical aspects ......................................................................................... 24
2.2 Diagnosis of cutaneous leishmaniasis ........................................................ 24
2.2.1 Classical methods ............................................................................... 26
2.2.2 Immunological diagnosis .................................................................... 26
2.2.3 Polymerase chain reaction methods ................................................... 27
2.2.4 Identification of Leishmania species ................................................... 28
2.3 Treatment of cutaneous leishmaniasis ...................................................... 28
3. Cutaneous leishmaniasis in Morocco .............................................................. 30
3.1 State of the art of research on CL in Morocco ............................................ 32
3.1.1 Transmission of CL: on host, parasite, and vector ................................ 33
3.1.2 Epidemiological burden ...................................................................... 37
3.1.3 Treatment .......................................................................................... 39
3.1.4 Control strategies ............................................................................... 41
3.2 The CL control policy in Morocco ............................................................... 41
4. Psycho-social burden caused by cutaneous leishmaniasis ................................ 42
5 Thesis outline .................................................................................................. 44
5.1 General objective ..................................................................................... 44
5.2 Specific objectives .................................................................................... 44
5.3 Overview of the thesis, by chapter ............................................................ 45
6. References ..................................................................................................... 50
CHAPTER 2. CONTROL OF CUTANEOUS LEISHMANIASIS CAUSED BY LEISHMANIA
MAJOR IN SOUTHEASTERN MOROCCO .................................................................. 65
CHAPTER 3. Psychosocial impact of scars due to cutaneous leishmaniasis on high
school students in Errachidia province, Morocco ................................................... 85
CHAPTER 4. Social impact of Cutaneous Leishmaniasis in Southeastern Morocco,
A qualitative study. ............................................................................................. 107
CHAPTER 5. Psychosocial burden of localised cutaneous leishmaniasis : a scoping
review. ............................................................................................................... 129
CHAPTER 6. Accuracy of a rapid diagnostic test based on antigen detection for the
diagnosis of cutaneous leishmaniasis in patients with suggestive skin lesions in
Morocco. ............................................................................................................ 157
CHAPTER 7. General discussion ........................................................................... 179
1. Cutaneous leishmaniasis control .................................................................. 181
2. Cutaneous leishmaniasis social representations and psychological suffering . 185
3. Cutaneous leishmaniasis clinical management ............................................. 187
4. Recommendations and conclusion ............................................................... 190
Supporting information ....................................................................................... 201
Acknowledgements ............................................................................................ 247
Abbreviations
ACL Anthroponotic cutaneous leishmaniasis
AIDS Acquired immunodeficiency syndrome
CBI Cutaneous body image
CIMVC Committee of integrated management of vector control
CL Cutaneous leishmaniasis
DALY Disability-Adjusted Life Year
DAT Direct agglutination test
DCL Diffuse cutaneous leishmaniasis DELM
Direction de l’Epidémiologie et de la Lutte contre les Maladies (Directorate of Epidemiology and Disease Control)
DLQI Dermatology life quality index
DNA Deoxyribonucleic acid
ELISA Enzyme-linked immunosorbent assay
EMR Eastern mediterranian region
FGD Focus group discussion
Fig Figure
FR Female respondent from Rissani area
FT Female respondent from Tinejdad area
GBD Global burden of disease
HCP High Commission for Planning
HIV Human immunodeficiency virus
HSP70 Heat shock protein 70
IFAT Immunofluorescence antibody test
IFN Interferon
IPM Institut Pasteur du Maroc
IRS Indoor residual spraying
ITN Insecticide-treated net
ITS1 Internal transcribed spacer
KAP Knowledge, Attitudes, and Practices
L. Leishmania
LAMP Loop-Mediated Isothermal Amplification
LCL Localised cutaneous leishmaniasis
LLIN Long-lasting insecticide-treated net
LMIC Low and middle-income countries
LST Leishmanin Skin Test
MCL Mucocutaneous leishmaniasis
MLEE Multi locus enzyme electrophoresis
MLMT Multilocus microsatellite typing
MoA Ministry of Agriculture
MoH Ministry of Health
MR Male respondent from Rissani area
MT Male respondent from Tinejdad area
NIH National Institute of Hygiene
NNN Novy-MacNeal-Nicolle medium
NPV Negative Predictive Value
NTD Neglected tropical diseases
OR Odds ratio
PCR Polymerase chain reaction
Ph. Phlebotomus
PKDL Post Kala-Azar dermal leishmaniasis
PPV Positive predictive value
QoL Quality of life
RDT Rapid diagnostic test
RFLP Restriction Fragment Length Polymorphism
Se Sensitivity
Sp Specificity
TB Tuberculosis
VL Visceral leishmaniasis
WHO World Health Organisation
YLD Years Lost due to Disability
YLL Years of life lost due to premature mortality
ZCL Zoonotic cutaneous leishmaniasis
11
Summary
Introduction
Cutaneous leishmaniasis (CL) is a neglected tropical disease (NTD) affecting more than one
million persons worldwide. In Morocco, reporting over the past decade on average more than
4000 cases per year, CL is considered a public health problem. CL is mainly poverty-related in
Morocco. The social representations of CL were never explored, though efficient control requires
understanding of people’s perception and community involvement. To fill this gap, and to
facilitate early diagnosis of CL, our research aimed to document the psychosocial burden of CL
in these regions, and to assess a new diagnostic tool for CL that is appropriate for use in remote
endemic areas.
Methods
We first described a major outbreak of CL that took place between 2010 to 2012 in Errachidia
province. We documented the intersectoral response measures including environmental
management and reservoir control. The reservoir of L. major, a rodent, Meriones shawi, was
targeted using strychnine-poisoned wheat baits.
The second part of the thesis documents social representations of CL in Southeastern Morocco,
in both L. major and L. tropica areas. In 2015, we conducted qualitative research in a group of
high school students living in L. major areas to study their perception of CL. Furthermore, we
conducted focus group discussions on CL perception and its psychosocial burden in the adult
population in Errachidia and Tinghir provinces. We related our findings on psychosocial burden
to those in the international literature by conducting a scoping literature review.
The third part of the thesis assessed the accuracy of a new rapid diagnostic test (RDT) of CL in
the real-life conditions of primary health centers. A “phase III” diagnostic accuracy study was
performed in a consecutive series of patients with ulcerative skin lesions not older than four
months and suggestive of CL. We compared the RDT results with a composite reference standard
based on PCR and microscopy.
Results
Between 2004 and 2013, 7099 cases of CL were recorded in Errachidia Province. This outbreak
due to L. major left many adolescents with permanent scar tissue on the face or other exposed
body parts. Almost 20% of 448 high school students reported a CL lesion and 87% said it could
lead to psychological consequences. The indelible CL scars lead to self-stigma and social stigma,
12
and the emergence of adverse psychological effects. Adult participants in the focus groups
considered the impact of CL lesions and scars as important. Young women with CL scars in the
face are stigmatized and may be rejected for marriage in these communities. People usually try
a long list of folk remedies on the active lesions, but none was felt adequate. They expressed a
real demand for better treatment. The scoping review confirmed that localized CL is a source of
pronounced psychological suffering, stigmatization, and reduction of quality of life in several
endemic countries.
In the third part, the RDT showed a sensitivity of 68% [95% CI, 61-74]), a specificity of 94% [95%
CI, 91-97]), a positive predictive value of 95% [95% CI, 92-98] and a negative predictive value of
64% [95% CI, 58-70]. Species typing on a subsample of 87 PCR positives using PCR-RFLP and PCR-
sequencing identified L. tropica (n=40), L. major (n=35) and L. infantum (n=12). Our findings
suggest that this novel RDT for CL is a useful addition to clinical management in Morocco,
especially in isolated localities far from provincial laboratories.
Conclusion
The high number of CL cases and related scars in Morocco should mobilize more public health
attention to sustain preventive measures against vectors and animal reservoirs. The diagnostic
management should be reviewed based on current evidence. We recommend the introduction
of the RDT in all endemic CL areas with difficult geographical access and the psychological
support of people suffering from CL indelible scars.
13
Samenvatting
Introductie
Cutane leishmaniasis (CL) is een verwaarloosde tropische ziekte (NTD) die meer dan een miljoen
mensen over de hele wereld treft. In Marokko, met meer dan 4000 gevallen per jaar, wordt CL
beschouwd als een probleem voor de volksgezondheid. CL is een ziekte die verband houdt met
armoede. De sociale representaties van CL zijn nooit onderzocht in Marokko. We wilden de
psychosociale belasting van CL in deze regio's documenteren, en we hebben een nieuwe test
voor CL-diagnose in afgelegen en endemische CL-gebieden geëvalueerd.
Methoden
We hebben eerst de epidemie van CL beschreven die plaatsvond tussen 2010 en 2012 in de
provincie Errachidia. We bestudeerden de intersectorale bestrijdingsmaatregelen, waaronder
milieubeheer en reservoirbeheer. Het reservoir van L. major, een knaagdier, Meriones shawi,
werd bestreden met lokaas dat behandeld was met strychnine.
Het tweede deel van het proefschrift richtte zich op maatschappelijke dimensies van CL in
Zuidoost-Marokko, zowel in de gebieden van L. major als L. tropica. We deden kwalitatief
onderzoek bij middelbare scholieren die in endemische L. major gebieden woonden. Daarnaast
werden in maart en april 2015 focusgroep discussies gehouden in de provincies Errachidia en
Tinghir met de volwassen bevolking. We hebben ook een literatuuronderzoek uitgevoerd om
onze bevindingen te relateren aan die in de internationale literatuur.
Het derde deel van het proefschrift beoordeelde de nauwkeurigheid van een nieuwe snelle
diagnostische test (RDT) voor CL in de context van negen eerstelijnsgezondheidscentra in vijf
endemische provincies. Een "fase III" studie werd uitgevoerd in een opeenvolgende reeks van
patiënten met ulceratieve huidletsels van minder dan vier maanden. We vergeleken de RDT-
resultaten met een referentiestandaard op basis van PCR en microscopie.
Resultaten
Tussen 2004 en 2013 werden 7099 gevallen van CL geregistreerd in de provincie Errachidia. Deze
epidemie door L. major heeft veel adolescenten met permanent littekenweefsel op het gezicht
of op andere blootgestelde lichaamsdelen opgezadeld. Bijna 20% van de 448 middelbare
scholieren meldde een CL-letsel en 87% zei dat dit psychologische gevolgen zou kunnen hebben.
De permanente CL-littekens leiden tot zelfstigma, sociaal stigma en de andere negatieve
psychologische effecten. Onze focusgroepen met volwassenen beschouwden de impact van CL-
14
laesies en littekens als belangrijk. Jonge vrouwen met CL-littekens in het gezicht worden
gestigmatiseerd en zullen vaak worden afgewezen voor huwelijk in deze gemeenschappen.
Mensen proberen meestal een lange lijst van remedies op de actieve letsels, maar geen daarvan
werd adequaat geacht. Ze drukten een echte vraag uit naar een betere behandeling. De scoping
review bevestigde dat LCL een bron is van psychisch lijden, stigmatisering en vermindering van
levenskwaliteit in andere endemische landen.
In het derde deel toonde de RDT een sensitiviteit van 68% [95% CI, 61-74]), een specificiteit van
94% [95% CI, 91-97]), een positief voorspellende waarde PPV = 95% [95 % CI, 92-98] en een
negatief voorspellende waarde NPV = 64% [95% BI, 58-70]. Species identificatie op een subgroep
van 87 PCR-positieven met PCR-RFLP en PCR-sequentieanalyse toonde L. tropica (n = 40), L.
major (n = 35) en L. infantum (n = 12). Onze studie suggereert dat deze nieuwe RDT voor CL een
nuttige aanvulling is op klinisch management in Marokko, vooral in afgelegen plaatsen ver van
provinciale laboratoria.
Conclusie
Het hoge aantal gevallen van CL in Marokko moet leiden tot meer aandacht voor de
volksgezondheid. Preventieve maatregelen tegen vectoren en dierlijke reservoirs zijn nodig.
Het klinisch beleid moet opnieuw bekeken worden op basis van deze recente resultaten. We
bevelen de introductie van de RDT aan in alle endemische CL-gebieden met een moeilijke
geografische toegang en de psychologische ondersteuning van mensen die lijden aan CL-
onuitwisbare littekens.
Introduction | 15
CHAPTER 1. General introduction
Introduction | 17
1. Leishmaniasis, an overview
Leishmaniases are vector-borne diseases caused by obligate protozoan parasites from the genus
Leishmania (Trypanosomatida: Trypanosomatidae) [1]. They are transmitted to humans through
the bite of a female sand fly. Leishmania parasites are what is called “digenetic,” because they
need two hosts to complete their life cycle. Within the insect vector, they present under the
promastigote form, an extra-cellular form with a flagellum, and in the mammalian host, as the
intracellular amastigote, a form without flagellum. This parasite can lead to a broad spectrum of
diseases, both in humans and animals [2]. Depending on the Leishmania species, the reservoir
of this parasite can be exclusively human, categorizing the disease as an anthroponosis, or,
involve animal reservoirs (rodents, dogs, etc…), categorizing the disease as zoonotic [3].
More than twenty Leishmania species1 are pathogenic for humans [1, 4]. The species
classification within the genus Leishmania has always been a controversial matter, and there is
not yet a definitively accepted taxonomy. Two genera of sand flies are involved in transmission:
Phlebotomus and Lutzomyia, depending on the geographical region. Of the over 800 known
species of sand flies, only 78 transmit Leishmania parasites to humans [1, 5]. Figure 1 gives an
overview of Leishmania species and the sandfly species involved in their transmission in the Old
World (Africa, Asia, Europe) or New World (the Americas).
The history of leishmaniasis can be traced back to 2,500 B.C., as several descriptions of the
disease have been found in ancient writings, and recently molecular techniques confirmed the
presence of the species in the archaeological material [1]. DNA of L. donovani was found in
Egyptian and Nubian mummies dating back 4,000 years [6].
The leishmaniases are now considered as neglected tropical diseases (NTD) by the World Health
Organization (WHO). The word leishmaniasis is often written as a plural noun because several
presentations can clinically be considered as different diseases. In humans, we distinguish three
main clinical forms: visceral, cutaneous and mucocutaneous leishmaniasis. Visceral leishmaniasis
(VL) or kala-azar is a fatal systemic disease that is caused by species of the Leishmania
donovani complex.
1 http://www.who.int/leishmaniasis/resources/who_wer9238/en/
18 | Chapter 1
Introduction | 19
Figure 1. An updated classification of Leishmania (Panel A) and sand fly (Panel B). The source of this diagram is Akhoundi et al. 2016 published in PLoS NTD
under Copyright: © 2016 Akhoundi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
https://doi.org/10.1371/journal.pntd.0004349 [1].
NB: (*) and (+) signs indicate the synonym species name to the original one. No final classification for the underlined species names. Name between quotation
mark means no official name is decided. Old world species are highlighted in blue and New world species are highlighted in red.
20 | Chapter 1
A recent update by the World Health Organisation (WHO)2 indicates that 97 countries and
territories are endemic for leishmaniasis. This list includes 65 countries that are endemic for both
VL and CL, ten countries that are endemic for VL only and 22 countries that are endemic for CL
only. In 2015, 214,201 cases of CL and 23,865 cases of VL were reported to WHO. However,
underreporting is frequent and higher CL incidence may be found at population level [7].
Correcting for this underreporting, the global annual incidence of CL is estimated at 0.6 to 1.0
million cases of CL and 40,000 to 90,000 cases of VL3.
As a metric to estimate the Global Burden of Diseases (GBD), and to compare disease burden
between diseases and countries, health economists use Disability Adjusted Life Years (DALYs).
The total number of DALYs lost due to a disease is calculated as the sum of years of life lost due
to this disease (YLLs) and of years lived with disability (YLDs) 4 see the box.
DALY= YLL+YLD
YLL = N x L1
YLD = I x DW x L2 or YLD = P x DW
N = number of deaths
L1 = standard life expectancy at age of death in years
I = number of incident cases
DW = disability weight
L2 = average duration of the case until remission or death (years)
P = number of prevalent cases
The total number of DALYs per NTD are shown in Table 1 and 2 below, reproduced from the most
recent Global Burden of Disease Report [8].
Table 2 - reproduced from the same publication as above - shows a substantial increase in
prevalent cases of Dengue and CL from 1990 to 2013.
2 http://www.who.int/gho/neglected_diseases/leishmaniasis/en/ accessed in 25 October 2017 3 http://www.who.int/mediacentre/factsheets/fs375/en/ accessed in 25 October 2017 4 http://www.who.int/healthinfo/global_burden_disease/metrics_daly/en/ accessed in 25 October 2017
Introduction | 21
Table 1. Leading causes of DALYs resulting from the NTDs according to the Global Burden of
Diseases Study (GBD) 2013 [8]
SOURCE: Reproduced from Herricks JR, Hotez PJ, Wanga V, Coffeng LE, Haagsma JA, Basáñez M-G, et al. (2017) The global
burden of disease study 2013: What does it mean for the NTDs? PLoS Negl Trop Dis11(8): e0005424.
https://doi.org/10.1371/journal.pntd.0005424 Copyright: © 2017 Herricks et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and
reproduction in any medium, provided the original author and source be credited.
22 | Chapter 1
Table 2. Prevalent cases of NTDs in 2013 and percent change from 1990 to 2013 according to
the Global Burden of Disease Study (GBD) 2013 [8]
SOURCE: Reproduced from Herricks JR, Hotez PJ, Wanga V, Coffeng LE, Haagsma JA, Basáñez M-G, et al. (2017) The global
burden of disease study 2013: What does it mean for the NTDs? PLoS Negl Trop Dis11(8): e0005424.
https://doi.org/10.1371/journal.pntd.0005424 Copyright: © 2017 Herricks et al. This is an open-access article distributed
under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and
reproduction in any medium, provided the original author and source be credited.
Expressed over a population denominator, the global mean age-standardized DALYs for CL was
0.58 per 100 000. The highest level was observed in Afghanistan, 87.03 per 100 000, followed
by Sudan (20.24), Syria (9.15), Yemen (6.25), and Iraq (5.95). Other African countries had a lower
Introduction | 23
burden, Burkina Faso (4.84), Morocco (1.92), Mauritania (1.67), Tunisia (0.66), Libya (0.61), Mali
0.42, Ethiopia (0.28).
However, the use of DALYs to quantify the burden of disease in non-fatal diseases was criticized
[9] and will be discussed more in-depth in chapter 5 of this thesis.
Furthermore, following the resolution adopted at the 60th World Health Assembly in 2007, the
global burden of Leishmaniasis and its control strategies were prioritized for countries where
leishmaniases are considered a public health problem. Two reports published bij WHO in 20165
and 20176 updated the information. WHO Eastern Mediterranean Region (WHO EMR) is the
highest affected region, despite the underreporting bias and the lack of epidemiological
information from some countries (due in general to political instabilities or weak monitoring
system) [7].
The table 3 below, based on the global health observatory7, lists the overall number and the
yearly average of CL cases reported in WHO EMR between 2006 and 2015.
Table 3. Yearly and total CL cases declared in high burden WHO EMR countries between 2006
and 2015
WHO EMR CL high
burden Countries*
Total CL cases declared between
2006 and 2015 (Number of years
declared)
Average annual number of
CL cases
Syria 444,995 (10) 44,499
Afghanistan 276,940 (10) 27,694
Iran 222,229 (12) 18,519
Pakistan 43,393 (09) 4821
Tunisia 44,652 (10) 4465
Morocco 41,651 (10) 4165
Iraq 37,329 (12) 3110
Libya 19,655 (07) 2807
Yemen 27,855 (10) 2785
Saudi Arabia 24,970 (10) 2497
5 http://www.who.int/leishmaniasis/resources/who_wer9122/en/ accessed in 10 april 2018 6 http://www.who.int/leishmaniasis/resources/who_wer9238/en/ accessed in 10 april 2018 7 http://www.who.int/leishmaniasis/resources/REH_38_TABLEAU_S1_S2_Version_finale.pdf
24 | Chapter 1
2. Cutaneous leishmaniasis
2.1 Clinical aspects
Depending on the species involved and the duration of the lesion, the clinical dermatological
manifestations vary from nodule, papule to ulcer associated or not with nodular lymphangitis. In
the Old World, CL is usually caused by L. major, L. tropica, and L. aethiopica. L. infantum, the
agent of VL in children and HIV/co-infected patients in the Mediterranean region, may
occasionally lead to a self-healing cutaneous lesion in adults, but the evolution of the cutaneous
lesion is slower than that observed with L. major and L. tropica infections [10]. L.aethiopica leads
to a more mutilating diffuse form in Ethiopia. In the New World, CL is mainly caused by L.
braziliensis, L. guyanensis, L. peruviana, L. amazonensis. The clinical evolution is most severe in
the mucocutaneous CL that is mutilating and challenging to cure [11].
The incubation period for symptomatic CL ranges from weeks to months, while for mucosal
forms it may occur years after the initial infection. Asymptomatic infection is common and can
be detected by the Montenegro skin test [12].
2.2 Diagnosis of cutaneous leishmaniasis
In endemic CL areas, clinicians make a CL diagnosis based on the suggestive skin lesions and a
history of exposure to sand fly bites. However, the diagnosis of CL can sometimes be challenging
because the lesion mimics both infectious and malignant conditions. The differential diagnosis
of CL contains a long list of diseases as reported in table 4 [13].
Introduction | 25
Table 4. Differential diagnosis of LCL, DCL, and MCL [13]
Differential diagnosis of CL Malignancies that may mimic CL
Infectious
Ecthyma
Furuncle
Carbuncle
Sporotrichosis
North American blastomycosis
Paracocciomycosis
Tuberculosis cutis
Syphilitic gumma
Yaws
Prototheca infection
Condyloma acuminata
Lupus vulgaris
Tuberculoid leprosy
Cutaneous furuncular myiasis
Tungiasis
Other
Xanthoma tuberosum
Sarcoidosis
Pyoderma gangrenosum
Insect bite
Basal cell carcinoma
Squamous cell carcinoma
Lymphoma
Differential diagnosis of diffuse CL
Lepromatous leprosy
Lobomycosis
Lupus vulgaris
Differential diagnosis of mucocutaneous
leishmaniasis
Syphilis
Yaws
Rhinoscleroma
Oral squamous cell carcinoma
Sarcoidosis
Source: M. Z. Handler, P. A. Patel, R. Kapila, Y. Al-Qubati, and R. A. Schwartz, “Cutaneous and mucocutaneous
leishmaniasis: Differential diagnosis, diagnosis, histopathology, and management,” Journal of the American Academy of
Dermatology, vol. 73, no. 6. Dec-2015
26 | Chapter 1
2.2.1 Classical methods
The use of light microscopy to visualize the amastigote form of the parasite after Giemsa
coloration of a tissue smear remains the method of choice for laboratory diagnosis of CL. The
moderate sensitivity of these microscopy readings is a severe limitation in clinical practice and
will be discussed in Chapter 6 of this thesis.
In the literature, the sensitivity of microscopy compared to PCR is variable. For example, in
Pakistan, the sensitivity of microscopy was 60% in areas mainly dominated by L. tropica, L. major,
and L. infantum [14]. In Iran, the sensitivity of microscopy was between 64% and 76%
respectively in areas mainly dominated by L. major, L. tropica, L. infantum [15, 16]. 57% was the
sensitivity found in a recent study from Palestinian districts were both L. major and L. tropica
were found [17]. In Morocco, 69% of microscopy sensitivity was found compared to culture for
L. major, L. tropica and L. infantum strains collected from different areas of endemicity [18].
Another study from Morocco reported a microscopy sensitivity of only 43% [19]. However, the
National Institute of Hygiene in Morocco reached more than 85% of sensitivity and emphasizes
that they have only 8% false positive and false negative microscopy results after a second control
compared to PCR ITS1 [20]. This variability cannot be explained just by the species differences,
but is mainly due to the sampling procedures, the sampling sites targeted in the suspected
lesions [21] and the quality of the microscopy reading and the learner performance (e.g. optical
microscopy versus virtual microscopy) [22].
Parasite culture of tissue samples obtained in biopsy or aspiration can be done in a well-equipped
laboratory. However, there is a risk of culture contamination and the turn-around time, i.e. a
one-week delay before results are available can also be frustrating. Identification of L. major or
L. tropica parasites in blood from CL patients was also attempted. One study from Lebanon
reported the successful detection of Leishmania parasites from whole blood in a culture tube
with Nicole–Novy–McNeal (NNN) in confirmed CL patients [23]. However, no other study
replicated or sustained such finding.
Histological examination is possible, but it depends on the quality of the biopsy and the
experience of the anatomo-pathologist.
2.2.2 Immunological diagnosis
A review published in 2015 [24] listed all known immunological assays for leishmaniasis: Enzyme-
Linked Immunosorbent Assay (ELISA), indirect immunofluorescent-antibody test (IFAT), western
blot, lateral flow assay, and direct agglutination test. However, antibody responses in CL patients
tend to be low in localized forms, which does not encourage the routine use of such
immunological techniques [25, 26]. The antibody detection tests ELISA and IFAT were explored
Introduction | 27
in Iran in a CL endemic area (due to L. major). ELISA showed a sensitivity of 83.6% and 84.7% and
specificity of 62.7% and 54.6%, respectively for detection of total IgG and IgM. The sensitivity
and specificity of IFAT were higher: 91.6% and 81%, respectively [27]. A Direct Agglutination Test
(DAT) based on homologous antigen showed a sensitivity and specificity of 90.5% and 91.8%
respectively in L. aethiopica [28]. However, in LCL patients, antibody levels are generally rather
low, unlike in DCL and VL patients. Therefore, no serologic tool is available for routine LCL
diagnosis [28].
The Leishmanin Skin Test (LST) or Montenegro test detects the delayed-type hypersensitivity
reaction to leishmania antigen with a sensitivity of 86.4% up to 100% [29, 30]. Some researchers
recommended the use of LST as an alternative diagnostic method when there is a clinical doubt
about a cutaneous lesion with no parasites found in direct smear microscopy examination [4].
However, LST remains positive for years after infection and does not allow discriminating a
recent from an old Leishmania infection.
The success of the rK39 rapid diagnostic test for the diagnosis of VL encouraged researchers to
develop a point-of-care test for CL. We report in Chapter 6 of this thesis the clinical evaluation
of such test; the CL Detect™ Rapid Test, which is a membrane-based immunoassay for the
detection of all clinically important Leishmania species that cause CL [24].
2.2.3 Polymerase chain reaction methods
Over the past few decades, several PCR-based methods, including real-time PCR assays, have
been developed for Leishmania detection, quantification, and species identification, improving
the molecular diagnosis of CL [31]. PCR is considered the most sensitive laboratory tool for CL
diagnosis. One study reported that kinetoplast DNA (kDNA) PCR showed the highest sensitivity
(98.7%), followed by the rRNA gene internal transcribed spacer 1 (ITS1) PCR (91.0%) and the
spliced leader mini-exon PCR (53.8%) [32]. Other researchers found that kDNA PCR had a
sensitivity of 90.7%, whereas an ITS1-based PCR had a sensitivity of 70.1% only [33]. A PCR based
on Heat Shock Protein (HSP70) was reported with a moderate to high sensitivity depending on
the performance of laboratories and the Leishmania species studied [34, 35]. Importantly, no
standard single PCR is used by all laboratories. Nowadays, in low and middle-income countries,
the most accessible and less expensive PCR is the one targeting internal transcribed spacers
(ITS1) of the ribosomal DNA locus [31]. Loop-mediated isothermal amplification (LAMP) - also
based on kinetoplast DNA detection- is a simplified PCR method that does not require a
thermocycler. The amplified product is visualized by eye without requiring gels or fluorescence
detection [36].
Quantitative PCR (qPCR) gives information about parasite load, which could be useful in
following up the outcome of treatment. For example, quantitative reverse-transcriptase real-
28 | Chapter 1
time PCR (qRT-PCR) was used to assess the dynamics of parasite clearance in CL patients treated
with miltefosine [37]. Multiplex qPCR was recently shown highly sensitive compared to
Leishmania kinetoplast DNA, and more so than Giemsa-stained smears and parasite culture [38].
2.2.4 Identification of Leishmania species
Multi-locus enzyme electrophoresis (MLEE) has been considered the gold standard for
Leishmania species typing for many years [39, 40]. Different assays for species typing in CL are
reviewed by an article published in 2015 [4]. Restriction Fragment Length Polymorphism analysis
(RFLP) is a PCR-based technique whereby the DNA amplification product is digested with one or
several restriction enzymes (endonucleases) and the restriction fragments are then analyzed by
electrophoresis [4, 41]. Several kinetoplast DNA (kDNA) assays are used in combination with
RFLP analysis. A PCR based on the Heat Shock Protein 70 (HSP70) primers was also used in
combination with RFLP analysis as well as sequencing. Parasite typing based on HSP70
sequencing showed a perfect agreement with MLEE [42]. With the advent of much cheaper
sequencing techniques, this may become in the future the reference standard for parasite
species identification. In contrast to MLEE, PCR based methods can be applied directly to clinical
samples and do not require isolation/culture.
In practice, in CL endemic regions where only one available CL treatment or one CL species
prevails, formal species identification often remains just an academic purpose. However, species
identification is vital in outbreak investigations and in both endemic and non-endemic settings
when travelers present with CL to a clinic.
2.3 Treatment of cutaneous leishmaniasis
The lack of an effective vaccine to prevent CL and the limited therapeutic options available were
highlighted in two Cochrane reviews describing the available interventions for the Old and New
World types [43, 44]. The absence of safe, efficacious and affordable treatment for CL is a matter
for concern in low and middle-income countries (LMIC). The first-line therapy is based on the use
of meglumine antimoniate or sodium stibogluconate. Other treatments are used as a second-
line or for specific categories of patients: liposomal amphotericin B (AmBisome®), paromomycin
(Paromomycin®), and miltefosine (Impavido®)[45]. Physical therapy, like cryotherapy and
thermotherapy, are also used, however without much standardization of dose or technique.
Introduction | 29
A recent update of available treatments for CL localized forms was published as a Cochrane
review and summarized the current evidence as follows [46]. The categories were:
A- Systemic and intralesional antimonials (Meglumine antimoniate and sodium
stibogluconate) The most used drugs and well known for their side effects and resistance
for some CL species.
B- Non-antimonial systemic treatments:
B-1- Oral treatments: Oral antifungal (fluconazole, ketoconazole, itraconazole); Oral
dapsone; Oral allopurinol; Oral antibiotics (metronidazole, cotrimoxazole, rifampicin,
azithromycin); Oral pentoxifylline; Oral miltefosine; Oral zinc sulphate; Oral artesunate.
B-2- Parenteral liposomal amphotericin B.
C- Non-antimonial topical or intralesional therapies:
C-1- Topical antifungals (clotrimazole, miconazole, and ketoconazole); Topical
paromomycin (aminosidine); Topical imiquimod; Topical aminoglycoside ointment
(WR279,396); Topical miltefosine; Topical dapsone; Topical Thio-Ben; Topical 0.045%
pharmaceutical chlorite (DAC N-055).
C-2- Intralesional zinc sulphate; Intralesional hypertonic sodium chloride; Intralesional
interferon-gamma (IFN-γ); Intralesional metronidazole.
D- Physical therapies:
Laser carbon dioxide (CO2); Trichloroacetic acid (TCA); Cryotherapy; Thermotherapy;
Topical photodynamic therapy; Mesotherapy.
E- Methods for promoting healing:
including dressing and antiseptics, are often employed in ulcerative lesions of CL to
accelerate cure, normalize epithelialization, and reduce scarring, especially at cosmetic
sites.
F- Alternative therapies:
Plants and herbal treatments; honey.
30 | Chapter 1
This Cochrane review concluded there is “very low-certainty evidence to support the
effectiveness of itraconazole and paromomycin ointment for localized CL”. The authors
considered it was impossible to conclude on the other interventions because of weak study
design or incomparability of studies [46]. The authors highlighted the absence of evidence on
the prevention of scarring.
3. Cutaneous leishmaniasis in Morocco
In Morocco, chronic skin lesions due to CL are a significant public health problem in some regions
of the country where CL is caused by three species of the Leishmania parasite: L. major, L. tropica,
and, sporadically, L. infantum. Epidemiologically, one distinguishes the L. major transmission
area in the east and southeastern part of Morocco - where the rodent species Meriones shawi is
the primary reservoir - from the L. tropica area that is concentrated in the center of Morocco
and in the northern mountainous regions - where the transmission is from man to man
(anthroponotic) [47]. Sporadic CL cases due to L. infantum occur mainly in the North of the
country, whereas visceral leishmaniasis is endemic in the north and central northern region of
Morocco [48]. Figure 2 shows the distribution of the three Leishmania species as documented
during the past ten years within the map of poverty in Morocco defined by the poverty severity
index as reported by the HCP. This index is known by the World Bank as “the squared poverty
gap index” [49]. This index increases as the gap between the poverty line and the consumption
expenditure of the poor increases. A higher index indicates more pronounced poverty.
Introduction | 31
Figure 2. The geographic distribution of CL causing Leishmania species in Morocco (2003 to 2014) plotted
on the poverty distribution map (based on the poverty severity index 2014 as developed by the Moroccan
high commission of planning (http://rgphencartes.hcp.ma))
Unfortunately, most maps in the literature showing the distribution of CL in Morocco
overestimate the total surface of the endemic areas. Many maps show almost all parts of
Morocco as endemic, except the south and the capital [47]. These flaws are due to technical
limitations of the mapping software used or because of lack of detailed geospatial information
on where cases occur. Other maps give the erroneous impression that cases occur in urban areas.
Before 2013 there were no data about the number of CL cases reported by locality. It was
therefore impossible to map the exact localization of the CL cases, and the case information was
hence linked to the major town in each reporting area like in one recent publication showing the
geographical distribution of ZCL and ACL incidence in Morocco [50].
How many new cases of CL are occurring in Morocco on an annual basis is still an unanswered
question. Two recent reviews documented the CL incidence over the 2004- 2014 period for both
anthroponotic CL (ACL) and zoonotic (ZCL) based on the MoH Data [50, 51]. The Unit of Parasitic
Diseases at the MoH provided epidemiological data on the period 1998 to 2017 (Figure 3),
showing an epidemic peak in 2010 with an expected new peak in 2018. During this 20–year
32 | Chapter 1
period more than 66,000 citizens experienced CL in a total general population in Morocco of
between 27 and 34 million inhabitants8.
Figure 3. Anthroponotic CL (ACL) and Zoonotic CL (CL) human cases reported between 1998 and 2017 in
Morocco (Source of data: Unit of Parasitic Diseases, MoH)
The official number of CL cases reported generates questions about possible underreporting or
overreporting. Are cases diagnosed by private practitioners adequately notified to the official
MoH reporting system? Little is known about this underreporting issue, and there are no
prospective population studies that document the real incidence rate at the population level.
According to Alvar et al., the underreporting factor for Morocco between 2004 and 2008 (period
of the study data analysis) was considered mild with 2.8 to 4.6 for the notification system [7].
According to the Moroccan law, CL is considered since 1996 a notifiable disease of Public Health
importance and should lead to a vector control intervention using insecticides9. Every public
health facility must declare any new CL case to the central epidemiological surveillance unit
within a week after it was diagnosed.
3.1 State of the art of research on CL in Morocco
Several masters and doctoral dissertations in both nursing and medical schools in Morocco have
focused on CL in recent years, some of which have been published in peer review journals. Also,
a growing number of papers on the topic have emerged over the past five years. We tried to
summarize these studies below.
We performed a literature search from the 1950s to the present day in the PubMed database,
combining the keywords "Morocco" and "cutaneous leishmaniasis," excluding the papers on
8 http://www.hcp.ma/ 9 http://www.sgg.gov.ma/BO/fr/1996/bo_4344_fr.pdf
0
1000
2000
3000
4000
5000
6000
7000
19
98
19
99
20
00
20
01
20
02
20
03
20
04
20
05
20
06
20
07
20
08
20
09
20
10
20
11
20
12
20
13
20
14
20
15
20
16
20
17
ZCL ACL
Introduction | 33
visceral leishmaniasis (VL) and the papers that are included further in this Ph.D. thesis. On 15
October 2017, this search led to 85 articles, including 72 Morocco-specific publications. An
additional search on Google scholar based on the names of first authors identified another 22
articles. Out of the 94 Morocco-specific papers (all listed in the references), 60% were published
in the last five years. A timeline showing the evolution of publications on CL in Morocco is
presented in Figure 4. However, of these 94 papers retrieved, 41 were published in non-indexed
journals.
Figure 4. Papers related to cutaneous leishmaniasis in Morocco from 1956 to 31 August 2017
3.1.1 Transmission of CL: on host, parasite, and vector
Out of the 94 papers, 50 (54%) belong to the category ‘transmission of CL; on host, parasite or
vector’. The first cases of the “Oriental Sore“ in Morocco were described by Foley and Vialatte10
in 1914 -cited in Rhajaoui et al. (2004) [52]. The first human case of visceral leishmaniasis in
Morocco was suspected in 1921 in Tanger by Remlinger 11 cited in Rhajaoui et al. [53]. The first
article on CL in Morocco included in our review was published in 1956 [54] during the French
protectorate. The same research team from the Faculty of Montpellier (France) later continued
its work under the supervision of Professor Rioux. Their publications documented the reservoir
and vector of CL in southeastern Morocco. In 1982, Rioux et al. identified L. major in the rodent
species Meriones shawi in Tata province and isolated it thereafter from human cases in south-
eastern Morocco [55]. In 1987, Marty et al. confirmed the presence of L. tropica in a CL lesion of
a Moroccan child admitted to a French hospital after a stay in Tanant (100 km from Marrakech)
[56]. In 1991, a CL case due to L. tropica was reported for the first time in central Morocco [57,
10 Foley, H., & Vialatte, C. (1914). Existence dans le Sud marocain du bouton d’orient à l’état endémique. Bull. Soc. Path. Exot, 7, 114-115. 11 Remlinger P. Un cas de Kala-azar infantile observé au Maroc. Arch Inst Pasteur Afr 1921;1:240–1.
34 | Chapter 1
58]. L. tropica has a very large distribution in Morocco. Several foci and outbreaks were observed
in an area, extending from Agadir-Guelmim in the South via Essaouira and Chichaoua in the West,
Beni Mellal, Azilal, Marrakech in the Centre, Ouarzazate in the East to Taza in the North [59].
The vectors for L. major and L. tropica in Morocco were identified as Phlebotomus papatasi and
Phlebotomus sergenti respectively [57, 60]. At that time, only multilocus enzyme electrophoresis
was available for species identification. Many different zymodemes (a group of parasites with
the same isoenzymes) were identified in Moroccan samples, MON-1 for L. infantum, MON-25 for
L. major and MON-102, MON-107, MON-109, MON-112, MON-113 MON-122, MON-123 for L.
tropica as reported in the map (Figure 5) [61].
Figure 5. Leishmania tropica. Geographical distribution of zymodemes throughout the Moroccan
endemic areas. The source of this map is Pratlong et al. 1991 in Annales de parasitology humaine
comparée under Copyright © Masson, Paris [61]
Introduction | 35
At the end of the 90s, the enzymatic profile MON-102 of L. tropica was identified for the first
time in Taza province by gel electrophoresis [62, 63]. Later, the existence of a canine reservoir of
CL sustaining L. tropica MON-102 and MON-113 was suggested based on the previous work of
Dereure et al. [58]. However, the role of dogs in the transmission of Leishmania species other
than L. infantum was later disputed [64].
In 2015, a comprehensive review of the different rodent species and their epidemiological role
as potential reservoir hosts of zoonotic CL in Morocco was published [65]. In 2017, the same
team reported the presence of L. infantum and L. tropica in rodents caught in Essaouira,
Chichaoua, Al Haouz and Marrakech provinces [66]. Molecular analysis revealed the presence of
Leishmania species in 18 out a total of 197 rodents caught: six Rattus. rattus (out of 80 captured;
7.5%), 11 Mus. musculus (out of 50 captured; 22%), and one Rattus. norvegicus (out of 9
captured; 11%) [66]. However, to identify Leishmania parasites in a mammal host does not
necessarily mean that it is involved in the transmission cycle [64].
In recent years attention has shifted to entomological studies [67–69]. The seasonal fluctuations
of phlebotomine sand fly populations and the correlation between the density of sand flies and
temperature, humidity and rainfall were documented [70–74]. Guilvard et al. documented two
peaks of infectivity of Phlebotomus sergenti, one in August and another in October (9.9%) [57].
Other studies documented the feeding behavior of this sand fly [75, 76]. The relative abundance
of males and females of Ph. sergenti varied according to the trapping method used [77]. Several
studies identified the zymodemes MON-102, MON-107, MON-122 and MON-123 in sand flies
infected by L. tropica. Ajaoud et al. detected L. tropica in human skin samples from CL patients
and female Ph. sergenti in central Morocco, by using nested PCR for amplifying the ITS1-5.8S
rDNA gene [78]. The diversity of parasite zymodemes in those sand flies was not correlated with
parasite diversity in humans in Essaouira, Azilal, Taza where a regional genetic differentiation of
Ph. sergenti exists [77, 78].
Ajaoud et al. corroborated that in the central Moroccan region where L. tropica is dominant, the
most frequent phlebotomine species are Ph. sergenti, Ph. longicuspis, Ph. perniciosis, and Ph.
Sergentomyia [76, 78]. There was higher diversity in Ph. sergenti lineages in Spain compared to
Morocco [79]. Nonetheless, a study in Al Haouz province showed that Ph. sergenti in Morocco
does not have the genetic characteristics of a single species [80]. In the Chichaoua area where
the peak biting rate occurs at twilight with some seasonal variability, there was diversity in the
nocturnal activity [75]. Ph. papatasi and Ph. sergenti were also studied in relation to climatic
factors and CL risk [74]. In Sefrou province continuous sand fly activity was observed during six
months (May–October) for Ph. sergenti, Ph. perniciosus, and Ph. papatasi with two peaks of
transmission, the first peak in July and the second peak in September [81]. Other studies showed
36 | Chapter 1
the coexistence of toscana virus12 with L. tropica specifically in Ph. sergenti [82, 83]. Less common
sandfly species such as Phlebotomus pernicious have been observed [84]. An entomological
investigation in the emerging focus of CL in Chichaoua was published in 2005 [85], followed by
mathematical modeling of epidemic thresholds [86]. Other entomological surveys described the
geographical distribution, current and predicted the distribution of different sand fly vectors of
CL in different endemic-epidemic foci in central and southeastern Morocco [70, 74, 87–92].
Furthermore, unique parasite strains and atypical presentations of CL were documented [93–
99].
In the past five years, molecular studies of Leishmania parasite have gained more interest. Most
of the work was published by the leishmaniasis research teams of the “Institut National
d’Hygiène”, “Institut Pasteur Maroc” (IPM) and the Faculty of Medicine and Pharmacy of
Casablanca, sometimes in collaboration with research units of other Moroccan universities and
European institutions [18, 19, 48, 100–104]. In 2007, the first article using ITS1 primers to confirm
the CL species was reported by Dr. Rhajaoui in collaboration with the Faculty of Medicine in al-
Quds University [105]. In 2009, biopsies from 26 patients were analyzed by PCR using primers
from the small subunit ribosomal gene. This PCR assay had a good specificity (100%) with a higher
sensitivity (84.6%) compared to microscopy (69.2%) and culture (69.2%) [18]. In 2013 a study
using Multilocus Microsatellite Typing (MLMT) has suggested the existence of two different
subpopulations of L. infantum MON1 in Morocco [48]. A study of archived slides collected in the
Chichaoua and Marrakech areas showed that the intra-focal occurrence of genetic variants of L.
tropica documented by MLMT is not due to genetic mutation but is explained by the importation
of pre-existing variants of L. tropica into Morocco [106]. Molecular methods using ITS1 PCR-RFLP
confirmed that L. tropica was the causal agent of CL in Azilal province [100]. An evaluation of this
ITS1 PCR technique showed that the primers 13A and 13B gave the best sensitivity [19]. In
Errachidia, a study based on ITS1 PCR-RFLP confirmed the presence of L. major in most of this
province but also identified L. tropica for the first time [107]. In Sefrou province, an area well
known as a focus of L. tropica transmitted exclusively by Ph. sergenti, the presence of L. infantum
within Ph. longicuspis was confirmed in 2014 by nested PCR (amplifying the ITS-5.8S rDNA gene)
[101]. ITS1 PCR-RFLP confirmed the coexistence of L. tropica and L. infantum in this province in
the same year [104]. With the same technique, the presence of L. tropica was confirmed in
archived microscopic slides collected in Beni Mellal and Fkih Bensaleh [102]. The same technique
was used to confirm the presence of L. tropica as the causative agent of CL in Chichaoua [108].
A molecular investigation of a nation-wide collection of samples will be available soon [103].
12 Toscana virus is an RNA arbovirus (arthropod-borne virus). The virus can be transmitted to humans by the bite of an infected sandfly of the genus Phlebotomus [154].
Introduction | 37
Climate change and its likely effect on the distribution and onset of new epidemic outbreaks of
CL have mainly been studied by research teams from the University of Marrakech in
collaboration with the National Aeronautics and Space Administration (NASA) [72, 87] or INH
[71, 109]. Some of these studies have tried to define the risk factors of anthroponotic CL (L.
tropica and L. infantum) and the link with the microenvironment [110, 111] and human behaviors
[109].
3.1.2 Epidemiological burden
On one hand, the Global Burden of Disease study, as published in the Lancet Infectious Diseases
in 2016 [112] ranks Morocco at the 14th position for CL over the World. On the other hand,
according to the WHO global health observatory, Morocco is ranked the 6th with regard the
yearly CL number of cases in the WHO EMR region (Table 3) and in the 4th among the 12 CL high
burden countries with regard to the incidence rate of 5.62 CL cases/10 000 inhabitants in
endemic areas in 201413.
As discussed above several reviews have been carried out to describe the epidemiological
burden of CL in Morocco. These were often based on routine data collected by the Ministry of
Health [47, 50, 51, 53, 113–115] or data from the HCP [116].
A large number of publications are retrospective surveys, some of them summarised in the
previous sections and others documenting the presence of new epidemic foci of CL as shown in
table 5 [117–128].
13 http://www.who.int/leishmaniasis/resources/who_wer9122/en/ accessed in 10 april 2018
38 | Chapter 1
Table 5. List of the studies reporting Cutaneous Leishmaniasis in Morocco
Year of
publication First author
Province of the
study
Population
sample Confirmation of CL by
1999 Chiheb [117] Taza 132 cases (1995) Microscopy
2008 Qasmi [128] Rabat (Ibn Sina
hospital)
13 children (1995-
2005) Microscopy
2011 Zougaghi [120] Chichaoua 2567 cases (2000-
2006) Microscopy
2013 Er Rami [126] Meknes (Military
Hospital)
49 cases (2005-
2011) Microscopy
2014 Hjira [123] Rabat (Military
hospital)
157 cases (2003-
2012) Histology & Microscopy
2014 Chiheb [118] Casablanca (Ibn
Rochd hospital)
268 cases (1995-
2010) Previous studies
2015 Mezouari [127] Commune
Tamezmoute
23 cases (Nov-Dec
2013) Microscopy
2015 Amarir [119] Settat 553 cases (2007-
2012)
ITS1 PCR-RFLP for 20
microscopic slides
2016 Aasri [121] Sidi Kacem 415 cases (2006-
2014) Microscopy
2016 Aasri [124]
Sidi Kacem,
Kenitra, Sidi
Slimane
439 cases (2006-
2014) Microscopy
2016 El Miri [122] Sidi Kacem,
Ouazzane
1656 cases (1997-
2012)
ITS1 PCR-RFLP for 18
microscopic slides
2017 Alaoui [125] Sidi Kacem (Ain
Dfali commune)
132 cases (2006-
2015) Microscopy
Other epidemiological observational studies based on microscopy and ITS1 PCR-RFLP-based
leishmanial species identification, documented the geographical distribution of the epidemic and
the effect of control measures against reservoir hosts (rodents) [107]. The discovery that more
than one species circulates within a province leads to new questions for control, such as the
identification of L. tropica and L. infantum in Errachidia, Ouarzazate and Zagora provinces where
it was assumed previously they were endemic for L. major species only [107, 129]. Furthermore,
the coexistence of both visceral leishmaniasis and CL in the same areas, as showed in the study
from Taza, raises the question about the real reservoir of L. infantum, L. tropica: is it zoonotic or
anthroponotic? [59].
Introduction | 39
3.1.3 Treatment
The healing potential of plants has been investigated by several recent studies in Moroccan
universities [130–135]. No clinical research to assess novel therapeutic interventions in CL has
been performed in Morocco. A single retrospective case study was recently published showing
the effectiveness of laser in reducing erythematous facial scarring caused by CL in three patients
[136].
Meglumine antimoniate (Glucantime®) is the only free treatment available in the public sector
for all forms of leishmaniasis in Morocco. The dosage and the way of administration (intra-
venous or intralesional) depend on the number, size, and localization of CL lesions. Typically, the
treatment is composed of two injections per week for four weeks. The standard protocol of
leishmaniasis treatment as mentioned in the official MoH manual of leishmaniasis control is
reported in table 6 [137].
Unfortunately, there is no well-defined outcome measurement, that would allow objective
assessment of the success or the failure of this treatment. Usually, after four weeks of treatment,
the ulcer starts healing but almost always leaves a permanent scar. Some CL lesions never come
to the attention of clinicians as patients wait for the spontaneous healing.
Up to now, there are no plans for changing the current therapeutic guidelines for CL in Morocco.
Moreover, current lack of evidence on Glucantime® resistance does not necessarily mean that it
does not exist.
40 | Chapter 1
Table 6. Treatment standard protocol for Leishmaniasis in Morocco
Systematic treatment
Daily intra-muscular injection of
Glucantime* (20 mg of Sb5+/ kg
without exceeding 2 vials
Local treatment
Peri-lesional injections of
Glucatime* (1 to 3 ml per lesion 2
times a week)
Duration
of
treatment
Indication of the
treatment
Duration
of
treatment
Indication of the
treatment
CL with L.
tropica
3 weeks Number of lesions ≥ 5
and/or
Size of lesion ≥ 4 cm
and/or
Periorificial lesion or
peri-articular
and/or
lesions localized in
finger and toe
4 weeks or
more until
complete
cure
Number of lesions < 5
or
Size of lesion <4 cm
CL. with L.
major
2 weeks
Visceral
Leishmaniasis
3 weeks
Nb: Local treatment includes also the use of antiseptics (Eosine®, Betadine®) and antibiotic
ointment (Aureomycine 3%®).
The peri-lesional injection of Glucantime® is done by a syringe with a fine needle (Type insulin
syringe). 1 to 3 ml of Glucantime® per session, 2 times a week until a whole cure reached
generally between 3 to 4 weeks. The quantity injected of Glucantime® depends on the size of
the lesion. For lesions due to L. tropica, the lesion should be covered during the treatment with
an adhesive plaster.
Introduction | 41
3.1.4 Control strategies
Apart from the case study that we will report in this Ph.D. thesis, only three publications
addressing control strategies were found, all published by the same team of Moroccan
investigators. First, they assessed the insecticide susceptibility status of Ph. sergenti and Ph.
papatasi to lambda-cyhalothrin, DDT, and malathion. All Phlebotomus species exposed were
susceptible to all insecticides tested [138]. A second study was done in Oued El Biiaza in Figuig
province in collaboration with the U.S. Army [139]. It showed that rubidium incorporated into
rodent baits could be used to demonstrate the level of blood feeding by sand flies. The
ivermectin-treated rodent bait acts as a systemic insecticide that kills the adult female sand flies
that feed on rodents before the sand flies become infective to vectors and take subsequent
bloodmeals from other hosts [139]. The third study was a field evaluation of alpha-cypermethrin
in indoor residual spraying for leishmaniasis control in the endemic areas in Boulmane and
Taounate provinces. Significant reductions in leishmaniasis incidence and severity rate were
observed when comparing sprayed and unsprayed localities. The residual activity of
alphacypermethrin lasted for ten weeks after spraying [140]. Another field trial published in 2016
focused on the cost-effectiveness of the use of Indoor Residual Spraying (IRS) with a-
cypermethrin, Long-Lasting Insecticide-treated Nets (LLIN) with and without a standard of care
environmental management [141]. IRS with a-cypermethrin and LLIN distribution both reduced
the incidence of CL in Morocco, though IRS was more effective. Indeed, CL incidence and sandfly
abundance were significantly lower in the IRS arm (CL incidence rate ratio was 0.32, 95% CI [0.15–
0.69], p=0.005 and sandfly abundance ratio was 0.39, 95% CI [0.18–0.85], p=0.022) [141].
However, a serious limitation of this study was noticed about the community who refused to use
the bed nets at a significant level. Then, until the end of 2017, none of those interventions were
scaled up. Furthermore, only authorization for research use and not for commercialization of the
insecticides used in those studies was obtained.
3.2 The CL control policy in Morocco
In the 1980s, the Moroccan Ministry of Health (MoH) set up a unit for the management and
control of parasitic diseases to address, amongst others, the CL problem. The main objective of
the CL component of the National Programme for Control of Leishmaniasis is to prevent the
disfiguring scars that are common sequelae of CL lesions. The MoH provides access to CL
diagnosis and treatment free of charge in the public health facilities and does so by standardized
protocols based on available evidence and the World Health Organisation expert advice. The
national guidelines on the control of leishmaniasis, (199714 and 2010) published by the
Directorate of Epidemiology and Disease Control (MoH), consider CL predominantly a self-
healing ailment in immunocompetent persons. Health professionals mostly refer to the most
14 http://sehati.gov.ma/uploads/Guide_des_activites_de_lutte_contre_les_leishmanioses.pdf
42 | Chapter 1
recent edition (2010) of the Leishmaniasis Control Guide which sets out four objectives for the
control of cutaneous leishmaniasis [137]:
- Limit the spread of the parasite in L. tropica foci where humans are the reservoir host;
- Ensure rapid healing of CL lesions
- Avoid disfiguring scars
- Avoid visceralisation in CL due to L. infantum
4. Psycho-social burden caused by cutaneous leishmaniasis
In Latin America, several studies were conducted to assess the psychosocial burden of CL, and
mucocutaneous leishmaniasis (MCL). Most of these researches are based on surveys of
Knowledge, Attitudes, and Practices (KAP). In 1994 Weigel et al. published an article from
Ecuador, where 208 adult persons participated in individual interviews to answer questions
about CL perception. In this study, a gender difference was found. Males were three times more
exposed to this disease, and CL reduced their work opportunities. Furthermore, women
considered CL decreasing their self-esteem [142]. In Brazil, lack of information and
misconceptions about MCL were found in a study of traditional remedies [143]. In North Eastern
Peru, native citizens had a limited knowledge about MCL and CL. Some of them used various
medicinal plants as remedies against leishmaniasis; while others practiced diet restrictions as a
CL treatment [144]. Insufficient knowledge about CL was also the main finding in a study from
Venezuela targeting residents in endemic CL areas [145]. In Paraguay, a KAP survey showed the
need for a better prevention of new cases, better case recognition, better treatment-seeking
behaviors in endemic MCL and CL areas [146]. A study aiming for an in-depth understanding of
the perception of CL was done in Brazil by Reis et al. [147]. They assessed the impact of health
education on the people’s adherence to biomedical explanations about MCL. For example,
“wound” and “mosquito” were the core terms frequently cited by all residents to describe
leishmaniasis [147].
To our knowledge, no study measured the psychosocial burden of CL in Morocco or North Africa,
except one study published about Tunisia in 2016 [148]. Our scoping review (chapter 5) provides
an overview of what has been published so far on the community perception of the localized
form of this disease and compares this with similar work published for mucocutaneous and
diffuse CL forms. In this thesis, we have studied CL stigma with qualitative methods. We provide
a brief definition of the concept of stigma below.
The word “stigma” has its origins in ancient Greece where certain individuals or groups, such as
criminals, burglars, or slaves were tattooed, to deny their membership to the civilized or well-
Introduction | 43
respected communities. Such physical marks defining the difference to others were a source of
devaluation and elicited a range of aggressive behaviors towards the holders of those marks and
sometimes their families.
Goffman was the first to attract attention to the mutual influence between the stigmatized
victim and the stigmatizing persons. He defined stigma as: ‘The phenomenon whereby an
individual with an attribute which is deeply discredited by his/her society is rejected as a result of
the attribute. Stigma is a process by which the reaction of others spoils normal identity’ [149,
150].
Scambler in 1998 defined the concept of stigma in two major categories: 1) felt stigma where
the stigmatized victims develop a fear of perceived discrimination, and 2) enacted stigma as a
clear act of discrimination [151]. Then, Weiss further developed this concept to describe the
social burden of neglected tropical diseases (Figure 6) [152].
Figure 6. Hidden distress model of stigma as reported by Weiss [152]
In our thesis project, we used the conceptual framework of the theory of social representations,
as developed in the 80s’ by Miscovisci [153].
Miscovisci explained that social representations concern the “contents of everyday thinking and
the stock of ideas that gives coherence to our religious beliefs, political ideas and the connections
we create as spontaneously as we breath” [153].
As the stigma concept suffers from a certain lack of clarity, we have opted to document the
psychosocial burden generated by CL in the larger sense. We documented not just the social
burden of any stigmatizing condition, but also the associated concepts of psychological burden
in the “daily-life” contextualized environment.
44 | Chapter 1
5 Thesis outline
5.1 General objective
The overall aim of this thesis was to contribute to the control of CL in Morocco by documenting
the meaning of CL for the exposed population, including the psychosocial burden of CL and by
assessing a new tool for CL diagnosis in remote and endemic CL areas.
5.2 Specific objectives
1. To describe the current epidemiological CL trend and describe the control intervention
against CL reservoir in southeast Morocco.
2. To explore the perception of this disease in the young resident population in southeast
Morocco
3. To evaluate stigmatization associated with CL in the general population of southeast
Morocco
4. To review the concept of stigma, quality of life and psychosocial burden of CL in the
literature
5. To assess the accuracy of a CL rapid diagnostic test in CL patient living in Moroccan endemic
areas.
Introduction | 45
5.3 Overview of the thesis, by chapter
Each specific objective (SO) has resulted in a publication as presented below.
SO1: Epidemiological weight of cutaneous leishmaniasis in Morocco.
See chapter 2
Bennis I., De Brouwere, V, Ameur B., Laamrani El Idrissi A., Chichaoui S., Hamid S., and Boelaert
M. Control of cutaneous leishmaniasis caused by Leishmania major in southeastern Morocco.
Trop Med Int Health 20 (10):1297-1305, 2015
The incidence of cutaneous leishmaniasis (CL) caused by Leishmania major has increased in
Morocco over the last decade, prompting the Ministry of Health to take intersectoral response
measures including vector and reservoir control. This article aimed to describe the CL outbreak
response measures taken in the province of Errachidia, where the reservoir of L. major, a sand
rat (Meriones shawi), was targeted using strychnine-poisoned wheat baits from 2010 to 2012.
We analyzed routine surveillance data and other information using the data of the CL control
programme. We present data on the evolution and the extension of CL in this province as well
as the epidemiological profile of the disease. Between 2004 and 2013, 7099 cases of CL were
recorded in Errachidia Province, gradually affecting all districts. Our results demonstrate that
more women were affected than men and that all age groups were represented. Errachidia
Province was the epicenter of the recent CL outbreak in Morocco. A notable decline in incidence
rates was observed after 2011. The outbreak control measures may have contributed to this
decline, as well as climatic trends or progressing herd immunity.
46 | Chapter 1
SO2: Psychosocial weight of cutaneous leishmaniasis scars in adolescents.
See chapter 3
Bennis I., Thys S., Filali H., De Brouwere, V, Sahibi H., and Boelaert M. Psychosocial impact of
scars due to cutaneous leishmaniasis on high school students in Errachidia province, Morocco.
Infect Dis Poverty. 6 (1):46, 2017
In Morocco, cutaneous leishmaniasis (CL) is usually known to be a slowly healing localized skin
disease, but in some cases, it can lead to mutilating scars. The outbreak of CL due to Leishmania
major in the Errachidia province in southeastern Morocco between 2008 and 2010 left many
adolescents with permanent scar tissue on the face or other exposed body parts. We studied the
psychosocial impact of CL on these young people. In 2015 we conducted a cross-sectional survey
of high-school students living in boarding schools in two CL-endemic areas of Errachidia: Rissani
and Tinejdad. A self-administered questionnaire elicited a response about general knowledge of
CL and related scars. An open-ended question focused on the possible psychosocial effects
associated with these scars. The quantitative data were analyzed with Epi Info™ and the text
data with NVivo software. Almost 20% of 448 respondents reported they had experienced a CL
lesion and 87% said it could or lead to psychological consequences. The text analysis showed
that girls more often than boys expanded on the adverse psychological effects of CL. The
students considered CL as “dangerous,” “serious,” and “deathly,” and said it sometimes led to
extreme suicidal ideations. The burden of CL in this age group is not negligible. The indelible CL
scars lead to self-stigma and social stigma, and the emergence of negative psychological effects
in this age group. While some students accepted their CL scars and related suffering as their
“destiny,” others were eagerly demanding protective measures against CL and treatment for the
scars
Introduction | 47
SO3: Psychosocial weight of cutaneous leishmaniasis in general population.
See chapter 4
Bennis, I., Belaid, L., De Brouwere, V., Filali, H., Sahibi, H., & Boelaert, M. (2017). “The
mosquitoes that destroy your face”. Social impact of Cutaneous Leishmaniasis in Southeastern
Morocco, A qualitative study. PloS One, 12(12), e0189906.
To document the social burden of Cutaneous Leishmaniasis in rural communities in Southeastern
Morocco, between March and April 2015, we conducted qualitative research in communities
exposed to Leishmania major or L. tropica in Errachidia and Tinghir provinces. Twenty-eight
focus groups discussions (FGDs) were realized, with a stratification by gender and tradition of
medicine (users of folk versus professional medicine). Data were analyzed using content analysis.
This rural population most exposed to CL in Morocco lacks access to health care in general and
points out there are other significant public health issues that need to be resolved. Nonetheless,
respondents consider the impact of CL lesions and scars as important and similar to that of burn
scar tissue. Young women with CL scars in the face are stigmatized and will often be rejected for
marriage in these communities. People usually try a long list of folk remedies on the active
lesions, but none was felt adequate. There was a definite demand for better treatment as well
as for treatment of the scars. The social impact of L. major and L. tropica is non-negligible, and
the demand for better treatment should be addressed.
48 | Chapter 1
SO4: Concept of stigma, quality of life and psychosocial burden of CL in the literature.
See chapter 5
Bennis, I., De Brouwere, V., Belrhiti, Z., Sahibi, H., & Boelaert, M. (2018). Psychosocial burden of localized cutaneous Leishmaniasis: a scoping review. BMC public health, 18(1), 358.
Cutaneous Leishmaniasis is a parasitic skin disease, linked to poverty, belonging to the group of
Neglected Tropical Diseases. Depending on the severity, the type of lesions or scars, and the
context, CL can lead to self- and social stigma influencing the quality of life and psychological
well-being of the patient. This dimension is, however, little documented for the most common,
localized type of CL. The population of interest for this review are patients with localized CL (LCL)
or related scars and their entourage. We aimed to describe the current knowledge on the
psychological burden and the stigma related to LCL. We searched the electronic databases
PubMed, Web of Knowledge, PsycINFO, POPLINE, Cochrane Library, Science Direct, Global
Health, and LILACS, for articles written in Arabic, English, French, Dutch, Portuguese, or Spanish,
and published until the end of August 2017. Fifteen papers met our inclusion criteria.
Psychological assessment based on standard scales and qualitative research asserts that LCL is a
source of psychological suffering, stigmatization, and reduction of quality of life. The fact that
the psychosocial burden generated by LCL is time-dependent makes it difficult to measure
adequately.More adequate estimates are needed to document the full burden of this NTD
specific form.
Introduction | 49
SO5: A New rapid diagnostic tool for cutaneous leishmaniasis in Morocco
See chapter 6
Bennis I, Verdonck K, El Khalfaoui N, Riyad M, Fellah H, Van der Auwera G, Sahibi H, Bouhout
S, Dujardin JC, Boelaert M (2018). Accuracy of a rapid diagnostic test based on antigen
detection for the diagnosis of cutaneous leishmaniasis in patients with suggestive skin lesions
in Morocco The American journal of tropical medicine and hygiene.
In Morocco, the diagnosis of cutaneous leishmaniasis (CL) is challenging in remote rural areas.
We evaluated the accuracy of a rapid diagnostic test based on antigen detection (RDT), the CL
Detect Rapid TestTM (Inbios International, Seattle, USA), in this setting. [Registered in
ClinicalTrials.gov as NCT02979002]. We consecutively recruited patients with new skin ulcers in
nine primary health centers. We took a dental broach sample for the RDT and two other tissue
samples by scraping the border and the center of the lesion with a scalpel and smearing it on a
slide. We duplicated each smear by pressing a clean slide against it and processed the slides by
microscopy, ITS1 PCR, and kDNA PCR. In a subsample with positive PCR, Leishmania species was
identified using PCR-RFLP and PCR-sequencing of hsp70 genes. A confirmed CL case was
microscopy and/or PCR positive. We computed sensitivity and specificity of the RDT in
comparison to this reference standard. Between December 2016 until July 2017 we included 219
patients, 50% of them were over 17 years old. The RDT showed a sensitivity of 68% [95% CI, 61-
74]), a specificity of 94% [95% CI, 91-97]), a positive predictive value of 95% [95% CI, 92-98] and
a negative predictive value of 64% [95% CI, 58-70]. Despite its low sensitivity, this novel RDT is a
useful addition to clinical management of CL in Morocco, especially in isolated localities. Positive
lesions can be treated as CL, but if negative, microscopy should be done in a second step. The
sensitivity of the RDT can probably be optimized by improving the sampling procedure.
50 | Chapter 1
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Control of L. major in Morocco | 65
Thesis results
CHAPTER 2. CONTROL OF CUTANEOUS
LEISHMANIASIS CAUSED BY LEISHMANIA
MAJOR IN SOUTHEASTERN MOROCCO
Bennis, I., De Brouwere, V., Ameur, B., El Idrissi Laamrani, A., Chichaoui, S., Hamid,
S., & Boelaert, M. (2015). Control of cutaneous leishmaniasis caused by Leishmania
major in south‐eastern Morocco. Tropical Medicine & International Health, 20(10),
1297-1305
Control of L.major in Morocco | 67
Control of cutaneous leishmaniasis caused by Leishmania major in
Southeastern Morocco
Issam Bennis*, MD, MPH, National School of Public Health, Rabat, Morocco & Institute of
Tropical Medicine, Antwerp, Belgium.
Vincent De Brouwere, MD, MPH, Ph.D.; Professor, Department of Public Health, Institute of
Tropical Medicine, Antwerp, Belgium.
Btissam Ameur, Directorate of Epidemiology and Diseases Control, Ministry of Health, Rabat.
Morocco.
Abderrahmane El Idrissi Laamrani, MD, MPH; Directorate of Epidemiology and Diseases Control,
Ministry of Health, Rabat. Morocco.
Smaine Chichaoui, Ministry of Health, Province of Errachidia, Morocco.
Sahibi Hamid VD, MSc, Ph.D.; Professor, Department of Parasitology, Agronomic and Veterinary
Institute Hassan II, Rabat, Morocco.
Marleen Boelaert, MD, MPH, Ph.D.; Professor, Department of Public Health, Institute of Tropical
Medicine, Antwerp, Belgium.
*corresponding author: [email protected] ; Tel: +212 661 25 99 01
Author Contribution
IB, VDB & MB designed the study. AI, SC & IB designed the intervention. IB & SC implemented
the intervention. SC& IB collected all the data. IB, SH& MB analyzed the data. IB wrote the first
draft of the paper with input from each listed author. VDB, MB, BA significantly contributed to
the writing of different versions of the manuscript. AI & SH commented on drafts of the
manuscript. All authors approved the final manuscript.
68 | Chapter 2
Abstract:
Objective: The incidence of cutaneous leishmaniasis (CL) caused by Leishmania major has
increased in Morocco over the last decade, prompting the Ministry of Health to take inter-
sectoral response measures including vector and reservoir control. The aim of this article is to
describe the CL outbreak response measures taken in the province of Errachidia, where the
reservoir of L. major, a sand rat (Meriones shawi), was targeted using strychnine-poisoned wheat
baits from 2010 to 2012.
Method: We analyzed routine surveillance data and other information using the CL data control
program.
Results: We present data on the evolution and the extension of CL in this province as well as the
epidemiological profile of the disease. Between 2004 and 2013, 7 099 cases of CL were recorded
in Errachidia Province, gradually affecting all districts. Our results demonstrate that more
women were affected than men and that all age groups were represented.
Conclusion: Errachidia Province was the epicenter of the recent CL outbreak in Morocco. A
notable decrease in incidence rates was observed after 2011. The outbreak control measures
may have contributed to this decline, next to climatic trends or progressing herd immunity.
Keywords: Cutaneous leishmaniasis, Zoonoses, Leishmania major, Rodenticide, Morocco.
Control of L.major in Morocco | 69
Introduction:
Leishmaniasis is a disease caused by protozoa of the genus Leishmania, a parasite that infects
many mammals including humans [1] and is transmitted by an insect vector, the phlebotomine
sand fly. The clinical spectrum of leishmaniasis includes cutaneous, mucocutaneous and visceral
disease. While the latter is the most serious and fatal if not treated, cutaneous leishmaniasis (CL)
causes considerable suffering because it can lead to disfiguring scars and social stigma. In North
Africa and the Middle East, CL usually occurs in semi-arid and desert conditions, especially in
Afghanistan, Algeria, Iran, Pakistan, Saudi Arabia, and Syria [2].
In North African countries, CL transmission has been increasing since the 1980s with the
emergence of new foci [3]. Both anthroponotic CL, caused by L. tropica, and zoonotic CL (ZCL),
caused by L. major are widespread [2]. While the former occurs mostly in urban areas, L. major
affects rural populations and is the topic of this paper. In North-African countries, L. major
belongs almost exclusively to the zymodeme Mon 25 [4]. The sand flies Phlebotomus papatasi
or a closely related species is the insect vector [3]. The transmission cycle of L. major is complex
and requires the presence of a rodent reservoir, such as the jird (Meriones spp), the fat sand rat
(Psammomys obesus) or the great gerbil (Rhombomys opimus) [5]. P. obesus transmits L. major
in most foci between Syria and Saudi Arabia in the east and Morocco in the west [6]. However,
in the south of Morocco, M. shawi is the main reservoir [7, 8]. Meriones are granivorous and can
cause important agricultural damage during their periodic population explosions [9]. Moreover,
in Morocco it seems that Shaw’s gerbil has adapted to the peridomestic environment where it
feeds on excreta and detritus, thriving close to garbage pits [8]. The burrows of these rodents
provide optimal sand fly breeding conditions, as the terrestrial larvae of Ph. papatasi thrive in
moist organic matter. The adult sand fly uses the well-insulated rodent burrows as diurnal resting
sites [10, 11]. During spring, emergent sand flies become infected by feeding on infected
reservoir rodents and transmit L. major to other rodents during subsequent feedings. Humans
are an accidental host in this cycle and are usually infected during the sand fly season in
summer/autumn. There is a close temporal association between the abundance of Ph. papatasi
and the incidence of ZCL [12–14]. In Tunisia, the seasonal distribution of human ZCL cases
showed one major peak in December, three months after the second peak of Ph. papatasi
abundance [15].
The first symptoms of ZCL occur 1 to 6 months after the infective sand fly bite and persist until
self-healing. ZCL lesions usually present as multiple ulcerated and often superinfected lesions. A
presumptive diagnosis of CL is based on these clinical symptoms while a parasitological diagnosis
remains the reference standard. It includes microscopic examination of Giemsa-stained biopsy
smears based on the direct identification of amastigote forms with microscopy because more
sophisticated techniques are expensive and rarely available in endemic areas [2, 16].
Spontaneous self-healing often occurs in CL after 2 to 6 months but leaves a scar. Depending on
70 | Chapter 2
the species, this tendency to self-cure usually occurs within approximately 2 to 6 months (e.g., L
major), or 6 to 15 months (e.g., L. tropica) of disease onset [2, 17]. Apart from species, the rate
of spontaneous healing of the lesion depends on factors such as the parasite load, its virulence,
the immune response of the host, the location of the lesion and the presence or absence of a
bacterial infection [14, 18, 19].
ZCL cases usually fluctuate in an epidemic cycle with five- to ten-years intervals [6]. Fluctuating
numbers of cases were attributed either to the cyclic development and loss of herd immunity or
to natural disasters such as floods and famines [20]. There is evidence that the lack of IFN-gamma
allows parasite multiplication and progression from infection to disease. Treatment of non-
healing CL with IFN-gamma resulted in rapid and complete resolution of lesions [21]. However,
the immunopathological and immune-protective mechanisms occurring during CL are difficult to
establish without longitudinal studies accounting for the genetic heterogeneity of human and
parasite populations [22].
The lack of an effective prophylactic vaccine suggests that we still do not fully understand the
factors that regulate the induction and maintenance of anti-Leishmania immunity.
Understanding these factors is critical for the design of effective vaccine and/or vaccination
strategy against leishmaniasis [23].
According to the literature, the most effective way to control L. major is to combine reservoir
and vector control, but the evidence of the effectiveness of this approach is limited to a small
number of case studies [2]. Success stories include the destruction of rodent burrows as resting
and breeding sites for Ph. papatasi between the 1940s and 1980s in the former Soviet Union as
reported in the literature [24, 25]. Measures for controlling Meriones species were developed
initially for agricultural purposes and are mostly based on anticoagulants and zinc phosphide as
rodenticides [26]. Guidelines for Leishmaniasis control published by WHO in 1988 suggested
introducing poisoned bait in burrow entrances to control the foci where Meriones species is the
reservoir host [27].
Since 2008, an unusual increase in CL cases was observed in the province of Errachidia in
Morocco that raised growing concern and frustration in the population and prompted the local
health authorities to take extra control measures. An entomological survey conducted in
Errachidia Province in July 2009 by the National Institute of Hygiene (INH Morocco) had
demonstrated the presence of the species Ph. papatasi [28] as well as the reservoir Meriones
shawi, but rodent control measures in the province had so far only been taken by the Ministry
of Agriculture (MoA) in the framework of crop protection. From 2010 onwards, the local health
authorities in Errachidia added the rodent control component to their ZCL outbreak response
strategy. This paper describes the epidemiological pattern of the recent CL outbreak due to L.
major in Errachidia Province and the results of the control strategy.
Control of L.major in Morocco | 71
Materials and Methods
Study Area
Errachidia Province is located in the Ziz Ghriss Valley in the southeast of Morocco, including the
Saharan areas, plains and highlands at an altitude above 1900 m, and covering a surface of 46
000 km². Errachidia has an arid climate with temperatures between -4 °C and 48 °C, with large
daily and seasonal temperature variations. The annual mean temperature is 21 °C. Rainfall is
scarce and usually occurs between February and March. The annual total precipitation is 134 ±
64 mm [29].
The province consists today of seven urban agglomerations (Errachidia, Erfoud, Goulmima
Tinejdad, Moulay Ali Cherif, Boudnib, and Jorf) and 22 rural districts, with 496 localities (Suppl
1). An administrative reform in 2010 redesigned provincial boundaries and the total population
of the province became 400 422 instead of 564 000 inhabitants. In this analysis, we have
excluded the CL cases recorded in various localities that are no longer part of the province of
Errachidia today.
Intervention
The CL control policy of the Ministry of Health (MoH) in Morocco recommends rodent control as
one of the interventions against ZCL, next to screening and treatment of patients, vector control
and enhancement of environmental sanitation [30]. All these actions should be supported by
health education and intersectoral collaboration. However, in most provinces, local health
authorities lack the resources for rodent control and limit themselves to promoting
environmental hygiene and some limited insecticide spraying around urban and touristic centers.
Contrastingly, the Ministry of Agriculture (MoA) in Morocco actively implements rodent control
in the framework of crop protection. The MoA produces the poisoned bait as the use of
strychnine is strictly regulated and can be handled only by this Ministry. No strychnine is available
in the commercial market. The technical staff of the MoA distributes the poisoned bait to farmers
along with instructions for its use. Surveillance of the rodent population is based on sentinel site
surveillance of the number of active borrows throughout the year.
In Errachidia Province, because of the alarming CL outbreak, the local health authorities of MoH
decided end 2009 to join forces with the MoA workers in an attempt to control the rodent
reservoir. The first joint control campaign with poisoned baits was conducted between early
December 2009 and end of March 2010, and was from the outset inter-sectoral, with a strong
commitment from both MoA and MoH. Technicians from both ministries working in close
72 | Chapter 2
collaboration supervised the community workers who applied the baits in the peridomestic
environment. This was repeated every year thereafter for three consecutive years.
In brief, a squad of 2 to 4 control workers with a supervisor was dispatched to the affected village.
The workers surveyed the full perimeter around the human settlement for rodent burrows up to
the boundary where palm trees or cultivated fields started. Each active rodent hole was treated
as follows. A worker wearing protective gloves and gear deposited six to twelve grains of
strychnine-poisoned wheat about 10 cm inside the burrow using a spoon and the tip of a plastic
bottle, under the supervision of the team leader. Three days later all dead rodents were disposed
of (Figure 1). After 15 to 30 days, the remaining active burrows were counted, and the poisoned-
bait application was repeated up to two times depending on the number of persistent active
burrows. This control operation was repeated for three consecutive years with the same timing.
Figure 1: Poisoned wheat introduced into one burrow (On the left). A colony of
Meriones Shawi rodents killed by this technique in Errachidia Province (On the right)
This intensive campaign was managed as a collaboration between local authorities,
municipalities, MoA and MoH working together in the Committee of Integrated Management of
Vector Control (CIMVC). Additional measures implemented from February 2010 onwards
comprised health education messages to encourage people to use rodenticides at home against
domestic rats and increase individual and community hygiene, including individual protection
Control of L.major in Morocco | 73
measures to avoid insect bites. In addition, complementary measures were introduced by the
CIMVC in the seven urban districts and touristic areas of the province. These were vector control
of mosquitoes using insecticide spraying between May and August and environmental sanitation
around cities and villages involving local communities.
Data collection & analysis
This is a retrospective descriptive study of the ZCL epidemiology in Errachidia Province, dating
back to the initiation of epidemiological surveillance in 1998 and including the intensive control
measures started in 2010. We analyzed routine reports on the control program’s standard
preventive measures, as well as anonymized data from the epidemiological surveillance system
and reports at the provincial and national level. We consulted the central database to crosscheck
the reporting of cases among Errachidia residents diagnosed or reported elsewhere. Information
about laboratory diagnosis was only available for the period after 2008. The database was
analyzed with the approval of the national health authorities in Morocco (MoH, Directorate of
Epidemiology and Diseases Control).
We included only native Moroccan residents in rural and urban areas of Errachidia Province. The
case definition of CL used in this study was the standard MoH definition: any person in an
endemic area with at least one clinically active skin lesion reported as CL by a health professional
[30]. Laboratory confirmation was only sought in the first five cases reported for all newly
affected localities. Confirmation was achieved by direct microscopic examination of tissue
scraping for the detection of amastigote forms. Most of the other cases were clinically diagnosed
by medical staff in health centers or by dermatologists in hospitals, because only one clinical
microbiology laboratory was located in the chief town of the province, far from most of the rural
areas.
We collected data on age, sex, period of diagnosis for each case, which were subsequently
anonymized. Data entry was performed using Microsoft Office Excel 2013 and analyzed by SPSS
Software Version 19.1. Epidemiological curves are presented according to the Gregorian
calendar. We used chi-square tests to compare proportions. Quantum GIS Geographic
Information System (Open Source Geospatial Foundation Project) was used to design and
develop CL distribution maps.
74 | Chapter 2
Results
Since the start of the recording of ZCL cases in the Province of Errachidia in 1998, and up to 2003,
907 cases were reported. Between 2004 and 2013 the total number of cases in the Province
reached 7099, with a peak number of 3483 cases (49%) in 2010 (Figure 2). Almost all cases were
clinically diagnosed by health centers or hospitals, but 237 cases were parasitologically
confirmed (out of a total of 303 smear examinations performed) (Table 1).
Table 1 Cases of cutaneous leishmaniasis in the province of Errachidia between 2004 and 2013
by age group, gender, area of residence, trimester of diagnosis and diagnosis confirmation
Total
Cases %
Age groups* [0–10] 1854 26.1
[11–20] 2038 28.7
[21–30] 971 13.7
[31–40] 782 11.0
[41–50] 634 8.9
[51–60] 471 6.6
>60 348 4.9
Gender Female 4184 58.9
Male 2915 41.1
Area Rural 5940 83.7
Urban 1159 16.3
Diagnosis trimester Fall 3822 53.8
Winter 2453 34.6
Spring 304 4.3
Summer 520 7.3
Diagnosis confirmation†
Clinical 5250 94.6
Laboratory 303 5.4
*One missing data. †Data available from 2009.
Control of L.major in Morocco | 75
Figure 2: Number cases of Zoonotic Cutaneous Leishmaniasis per year in Errachidia Province and other affected Moroccan
Provinces between 2004 and 2013.
The outbreak was first recognized as such in 2007 in the area of Merzouga in the southeast of the province, in Taous district bordering Algeria
(Figure 3), where a total of 94 cases were recorded with an incidence rate (IR) of 2500 cases per 100 000 inhabitants. The following year, the
outbreak spread to the north and west of the province. By 2010 all areas were affected, and the overall incidence rate was 869 per 100 000
inhabitants in that peak year. Incidence rates ranged between 11 and 9382 per 100 000 inhabitants in the rural districts Chorfa M’Daghra and Sidi
Ali respectively.
3500
3000
0 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
YEAR Errachidia district (Annual cases) Other Moroccan districts (Annual cases)
500
1000
1500
2000
2500
76 | Chapter 2
Figure 3: Geographic distribution of Zoonotic Cutaneous Leishmaniasis cases in
Errachidia Province, between 2004 and 2013
Between 2010 and 2012, all affected urban and rural district areas in the province were treated
with poisoned bait, covering approximately 5000 hectares. In these three years, 1287 kg of
strychnine-poisoned wheat was used. The total number of active burrows observed before and
after these operations are provided as additional information (Suppl 2). Initially, the campaign
targeted 322 571 active burrows. Although only 80% to 89% of them could be treated, after the
first round of poisoning in 2010, the number of active burrows decreased by 95%. After the
launch of the campaign, we recorded a steep decrease in the number of CL-affected areas, from
28 areas in 2011 to 17 in 2012 and 5 areas in 2013 (Figure 3).
The overall incidence rate was reduced to 9 per 100 000 inhabitants in 2013 in the affected areas
in the province. However, the city of Errachidia and its neighboring rural areas (Aoufous, Chorfa
M’Daghra, Lkheng), which were not part of the rodent control campaign in 2010, recorded an
increase in the number of CL cases from 54 in 2010 to 84 cases in 2011 (Suppl 3). After the rodent
control intervention was equally applied throughout this area in 2012, the number of annual
cases decreased to 12.
Control of L.major in Morocco | 77
Figure 4: Seasonality pattern of zoonotic CL cases in Errachidia Province showing
cumulative number per month for the period 2004 to 2013, with breakdown by rural
and urban areas
The maximum caseload was recorded in the fall and early winter season (Figure 4). The rural
areas declared 83% of all registered cases. All age groups were affected, and the average age of
cases was 24 ± 18 years. The most affected age group were the [11-20] -year -olds with 28% of
cases, followed by the age group [0-10] -year -olds (26% of cases) (Table 1). Women were more
often affected with 59% of the total number of cases. The female predominance of CL cases was
present in all age groups, except in those older than 60 years (Figure 5).
Figure 5: Sex and age distribution of all cases of Zoonotic Cutaneous Leishmaniasis in
Errachidia Province from 2004 to 2013
78 | Chapter 2
Discussion
Our results describe a succession of yearly CL outbreaks in Errachidia Province, resulting in a total
of 7099 cases between 2004 and 2013, with a peak incidence in 2010. After the launch of an
intensive inter-sectorial campaign in 2010 including for the first-time rodent control to target
the CL reservoir host, we observed a substantial reduction in the incidence rate of CL (from 869
to 9/100 000 inhabitants per year). However, the observed decline in the CL incidence rate in
Errachidia Province could also be due to the natural cycle of the epidemic, with a decline in
incidence when the number of susceptible persons in the human population has become too
low. Climate factors may also play a role in the incidence trend of ZCL [29]. Whereas higher
temperature may positively influence the abundance of the sand fly [31, 32], progressing
desertification and lack of humidity could in turn force the rodent population to move to wetter
areas and lead to decreases in incidence [10, 32]. Our data do not allow to disentangle those
effects. Nevertheless, the systematic application of poisoned bait in the CL affected areas in
Errachidia province has probably contributed to the decrease in CL incidence, as it led to a 95%
reduction in the number of active rodent burrows in treated areas, which was sustained for each
of the three years of the intervention. The effect observed with this strychnine-poisoned bait
intervention was more important than that observed by others with anticoagulants or zinc
phosphide, a 48% and 58% reduction respectively [26]. Another intervention in the valley of
Turkmenia (Turkmenistan, Ex-Soviet Union) in 1941 succeeded in reducing human morbidity
from 70% to 0.4% when chloropicrin bait was used in the burrows of large gerbils [25]. In Iran,
poisoned bait applications led to a less impressive reduction in cases [26, 33]. A recent overview
article about ZCL trends in Morocco confirmed that the peak incidence in the country was
reached in 2010 with 6444 cases, and declined sharply to 2219 cases in 2011 and 740 cases in
2012 [34]. Errachidia Province was the major contributor to this caseload, accounting for 3483
or 54% of the total number of cases in the country in 2010 (Figure 2).
In this Province, the unique feature was the active collaboration of the local MoH leishmaniasis
control program with the MoA in implementing the integrated management of vector control
(IMVC) strategy into the affected areas. The MoH monitored the outcome of the strategy very
closely, apparently with good results. The rodenticide strategy we describe has been used in
Morocco for crop protection for decades and has been used elsewhere for ZCL control. Detailed
knowledge of the animal and vector reservoirs of ZCL in a specific area is essential to use this
chemical method with success. The rationale for rodent control in an integrated ZCL control
strategy is based on the principle of the momentary reduction of the rodent population to reduce
the infected reservoir [35]. If fewer sandflies have an infected blood meal it is expected that less
will accidentally contaminate humans. The timing of the poisoned-bait intervention is essential,
because the transmission from rodent to humans by the sand flies is most intensive in the
summer months (May to September), and food habits of rodents are seasonal.
Control of L.major in Morocco | 79
To be effective, the application of baits should take place from December to March, before the
reproduction season of rodents and before the beginning of the sand fly season. Wheat bait is
chosen because Meriones shawi stores grain reserves in its burrows and survives on it during
winter [36].
The reported incidence of CL was higher among women than men, although men have a higher
exposure level due to their occupations. In contrast, a higher CL incidence in men was found in
a study in Iran [37] and in the Middle East [38]. Other studies from Saudi Arabia supported the
hypothesis that the CL sex ratio is dependent on geographic location and cultural patterns [39,
40].
As men in Errachidia generally perceive CL as non-severe, this may have led to some under-
reporting of cases and the true incidence rate may, therefore, have been higher than what we
report here. Another limitation of our study was that cases were mainly ascertained clinically,
though in each new area affected the first suspect cases were systematically confirmed by
parasitological exam. Further surveillance thereafter was clinical. In addition, the poisoned bait
strategy we describe will not work with P. obesus, as they do not feed on grain in the same way
as Meriones. Finally, we fully acknowledge that the observed reduction in incidence cannot be
directly attributed to the rodent control component, because of the observational nature of our
study, and the fact that the intervention was integrated in a larger package of control
measures. The absence of any control group does not allow establishing a causal effect.
The application of poisoned grains in the peridomestic environment for ZCL control may be
hazardous as there is a lack of clear guidance on the methodology and precautions to take. Even
if no cases of adverse events or fatalities of animals or humans have been reported to date with
the strategy and dose applied, human fatalities have been reported at doses in excess of 5 to 10
mg per weight in the literature [41]. Moreover, questions can be raised about the environmental
impact and sustainability of the strategy. We have no information about the effect of strychnine
on protected species (e.g. Rhombomys opimus, hyraxes), about its efficacy in the longer term, or
about its adverse effects on the ecosystem. There is no clear answer to these questions, and
instead of promoting strychnine-based rodent killing on a large scale in similar contexts, we
conclude that more eco-friendly alternatives for reservoir control are urgently needed. Reservoir
control should include environmental surveillance to monitor the expansion of rodent
populations after the rainy seasons as well as entomological surveillance to predict ZCL
epidemics and target the control measures effectively [10].
80 | Chapter 2
Conclusion
It appears that the intersectoral ZCL control strategy adopted by the Province of Errachidia in
2010 contributed to a quick and major reduction in incidence in the context of the 2004-2013
outbreak. Given there is no vaccine for this disease, more appropriate and less toxic control
measures are desperately needed. Meanwhile, health authorities should be aware of the
rodenticide approach, and use it with caution as a response measure in similar contexts of ZCL
outbreaks.
Acknowledgment
The authors are grateful to Samantha Brunts (Linguapolis, University of Antwerp), who
performed English language editing and offered useful comments.
Competing interests
The authors have no conflict of interest to declare. This manuscript is not submitted elsewhere
for publication.
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Supporting information
Additional supporting information may be found in the online version of this article:
Fig.S1. Maps of the administrative division of districts in Errachidia Province - Kingdom of
Morocco
Table S1. The number of burrows before and after operations to control the density of rodent
Meriones Shawi by subdivision in the Errachidia Province.
Table S2. Distribution of cases and incidence of cutaneous leishmaniasis due to Leishmania major
in Errachidia Province by districts.
Corresponding Author Issam Bennis, National School of Public Health, Lemfedel Cherkaoui
Street, Madinat Al-Irfane, MailBox: 6329, Rabat, Morocco. Tel.: +212 661 25 99 01; Email:
Psychosocial impact of CL scars on students | 85
CHAPTER 3. Psychosocial impact of scars
due to cutaneous leishmaniasis on high
school students in Errachidia province,
Morocco
Bennis, I., Thys, S., Filali, H., De Brouwere, V., Sahibi, H., & Boelaert, M. (2017).
Psychosocial impact of scars due to cutaneous leishmaniasis on high school students
in Errachidia province, Morocco. Infectious diseases of poverty, 6(1), 46.
Psychosocial impact of CL scars on students | 87
Psychosocial impact of scars due to cutaneous leishmaniasis on high school
students in Errachidia province, Morocco
Issam Bennis1,2,3,5*, Séverine Thys2, Hind Filali1, Vincent De Brouwere2, Hamid Sahibi4,
Marleen Boelaert2
*Corresponding author: [email protected]; GSM: 00212661259901
Address : Ecole Nationale de Santé Publique, Rue Lemfedel Cherkaoui, Madinat Al Irfane 10000,
Rabat, Morocco
88 | Chapter 3
Abstract
Background: In Morocco, cutaneous leishmaniasis (CL) is usually known to be a slowly healing
localized skin disease, but in some cases, it can lead to mutilating scars. The outbreak of CL due
to Leishmania major in the Errachidia province in southeastern Morocco between 2008 and 2010
left many adolescents with permanent scar tissue on the face or other exposed body parts. We
studied the psychosocial impact of CL on these young people.
Methods: In 2015 we conducted a cross-sectional survey among high-school students living in
boarding schools in two CL-endemic areas of Errachidia: Rissani and Tinejdad. A self-
administered questionnaire elicited responses about general knowledge of CL and related scars.
An open-ended question focused on the possible psychosocial effects associated with these
scars. The quantitative data were analyzed with Epi Info™ and the text data with NVivo software.
Results: Almost 20% of 448 respondents reported they had experienced a CL lesion and 87% said
it could possibly or definitely lead to psychological consequences. The text analysis showed that
girls more often than boys expanded on the negative psychological effects of CL. The students
considered CL as “dangerous”, “serious”, and “deathly”, and said it sometimes led to extreme
suicidal ideations.
Conclusion: The burden of CL in this age group is not negligible. The indelible CL scars lead to
self-stigma and social stigma, and the emergence of negative psychological effects in this age
group. While some students accepted their CL scars and related suffering as their “destiny”,
others were eagerly demanding treatment to heal the scars and were claiming protective
measures against CL.
Keywords: belief, body image, cutaneous leishmaniasis, Leishmania major, scars, self-concept,
self-stigma, social stigma, students, adolescents, Errachidia, Morocco
Psychosocial impact of CL scars on students | 89
Introduction
Leishmaniasis, a parasitic disease of the genus Leishmania transmitted by a sand-fly vector, is
one of the most neglected diseases in the world, affecting the poorest of the poor [1]. In low-
and middle-income countries, the affected population lives in precarious dwellings within
vulnerable environmental conditions [2].
Cutaneous leishmaniasis (CL), the most frequent clinical presentation, usually presents as a
localized lesion at the site of the sand-fly bite after a lapse of several days to months [2]. The
lesion starts as an erythema that gradually transforms to a papule and later to a nodule. The
nodule then increases in volume and progressively ulcerates [3]. The whole process generally
takes between two and six months [4]. In immunocompetent persons, CL lesions are slowly self-
healing but they often lead to scar tissue [5]. As the sand flies bite most often in the face or other
exposed parts of the body, these disfiguring scars can lead to substantial psychological and social
suffering, and economic losses [6]. Lesions affecting the central area of the face have a higher
impact compared with others [7].
Studies conducted in Afghanistan, Pakistan, Syria, and Iran have demonstrated the serious social
consequences of CL for young women. They may not be able to get married in the future [8–11]
or not be allowed to stay with their partner if they contract CL after marriage [12]. Often, persons
affected by CL during childhood only become aware of their affected body image during
adolescence when the indelible scars become more visible in their own eyes and/or the eyes of
their loved ones [13]. Indeed, the perception of the body, more precisely the self-perceived
beauty of the face, is a major factor influencing self-awareness, especially, but not only, in
women. In contrast, a similar facial scar in a male subject could be considered attractive in some
communities [14].
Interestingly, a recent study quantified the CL burden by estimating the related disability-
adjusted life years lost (DALY) based on physical disfigurement only. The authors of that study
stated that the CL burden calculated in this way did not differ significantly in terms of age in the
same geographic region, probably because this approach does not take into account the social
stigma or the emotional or financial impact of CL [15]. However, as also demonstrated in the
case of lymphatic filariasis, the disabling or disfiguring sequelae of some neglected tropical
diseases can have a substantial impact on mental health [16].
In Morocco, CL is caused by two species, L. major, and L. tropica. The first is a zoonotic disease
with rodents as a reservoir host, the second is anthroponotic [17]. CL due to L. major has recently
led to important epidemics. The Errachidia province in southeastern Morocco has seen an
epidemic peak in most of its districts between 2008 and 2010 [18, 19]. The most affected age
group was those aged between 11 and 20 years, which is rarely studied in the literature.
90 | Chapter 3
Therefore, the aim of this article is to describe the psychosocial impact of CL on adolescents in
Morocco’s L. major-endemic areas.
Method
Conceptual framework
Our concept of stigma is rooted in the framework proposed by Bos et al. [20], which was adapted
from the one developed by Pryor et al. [21] (see Figure 1). Stigma is categorized by these authors
as belonging to one of four types. The public (or social) stigma is at the core of the model and
refers to the social and psychological reactions of society to the person who has the stigmatized
condition [22]. Self-stigma reflects the impact of stigma on the stigmatized person and is partly
internalized through a reduction in self-worth and psychological distress. Stigma by association
reflects the negative reactions to family and friends of stigmatized persons and their attitudes to
this [23]. Then, once the stigma becomes institutionalized within society, the authors define the
fourth category as “structural stigma”, when the ideological systems of society perpetuate the
stigmatized status [21].
Figure 1: Conceptualization of ‘stigma’, based on the framework developed by Bos et
al. (2013) and Pryor et al. (2004)
As stated above, those who internalize stigma often experience a significant loss of self-esteem
[22]. The relationship between self-concept and self-stigma is well documented in psychiatry.
Stigmatized people have negative attitudes towards themselves as a reaction to their condition
[24]. Self-concept should be distinguished from self-awareness and self-esteem. McConnell et
al. [25] state that the awareness about the self is always influenced by the context.
Psychosocial impact of CL scars on students | 91
Over time, the person develops a self-concept, which interacts with self-esteem, self-knowledge,
and self-awareness within the social context. In this article, we use the term self-concept as the
cognitive description of one’s self (self-awareness) added to the opinion about one’s self (self-
esteem).
Study population
In April 2015, we carried out a cross-sectional questionnaire survey among boarding school
students in two areas of the Errachidia province that reported high CL attack rates. The choice
of these two areas was based on the reported incidence of CL cases, as published earlier [18].
One school was located in Tinejdad city with boarding facilities serving the surrounding districts
of the Tinejdad Ferkla area. The second school was located in Rissani city serving the districts of
the Rissani Sfalate area (see Table 1).
The two schools enrolled a total of 3,246 students including 561 boarding students with separate
facilities for the girls and the boys. Henceforward, we will use the codes “FT” or “MT” to identify
respectively the group of girls (F) and boys (M) from the Tinejdad (T) area, and the codes “FR”
and “MR” to identify the respective groups of girls and boys from the Rissani (R) area.
Table 1: Origin of interviewed boarding school students, stratified by gender (n=448)
92 | Chapter 3
Survey questionnaire
The survey was based on a self-administered questionnaire developed to assess the students’
general knowledge about CL. We pre-tested the questionnaire on 10 students from Errachidia
city and found that the time it took to fill out the form was about 10 minutes. In each high school,
the questionnaires were distributed on the same day to all present boarding school students.
The questionnaire was in Arabic (English translation in Additional File 1, original Arabic form in
Additional File 2).
The introductory part consisted of an information sheet and consent section for voluntary
participation in the study, with some administrative information. The questionnaire itself
consisted of 18 closed-ended questions and concluded with one open-ended question about the
perceived psychological effects of CL scars (see Additional file 3).
As a start, the principal investigator (the first author) explained the purpose of the study and the
confidentiality conditions to the students during an extracurricular study session. It was also
stressed that the students were free to refuse to partly or completely answer the questionnaire.
Then, he invited the respondents to select their answers and write a short paragraph for the last
question. Students did not communicate with each other while answering the questions and a
boarding master supervised each group. In the end, students returned the questionnaires to the
investigator one by one (see Additional file 4 for all student responses).
Data analysis
Regarding the 18 closed-ended questions of the survey, the data entry, initial data cleaning, and
descriptive analysis were done using Epi Info™ 7 (CDC Atlanta, USA) software. Three socio-
epidemiological attributes were chosen for the comparative analysis: 1) participant’s gender:
female vs. male; 2) a history of being affected by CL (personal experience with CL): yes or no; and
3) area of residence: Tinejdad or Rissani.
Students’ answers to the open-ended questions required the verbatim transcription in the Arabic
language and then translation into French. The text analysis was performed with NVivo software
version 10 (QSR International Melbourne Australia). The coding followed a deductive approach
based on the conceptual framework (see Figure 1). An inductive analysis was done to extend the
generated codes (see Figure 2) in order to define the factors which influenced the impact of CL
scars on the patient’s psychological state. Five major themes were elucidated: perception of
body image, self-stigma, social stigma, self-concept, and health-seeking behavior. Attributes of
gender, area of residence, and personal CL experience were also used to classify answers in order
to examine relationships within these qualitative data.
Psychosocial impact of CL scars on students | 93
Figure 2: Nodes and codes used in the text analysis (with NVivo 10 software)
Results
From the 454 students present on the day of the survey, 258 boys and 190 girls (448 in total)
participated in the study, while six boys refused. The mean age of the respondents was 18.1
years ± 2.3 for boys and 17.2 years ± 1.6 for girls. Table 1 shows the origin of the students
stratified by gender. All participants were from rural districts that declared CL outbreaks
between 2008 and 2010 [18].
Affliction with and general knowledge about CL
In total, 362 out of 448 respondents (80.8%) said they knew about CL and 60% correctly indicated
that an insect transmits CL to humans. Eighty-eight participants (19.6%) reported having been
personally infected with CL (38 girls, 50 boys) and among the others, 159 knew at least one
person who has been affected by CL. In the group of 88 students that had been personally
infected with CL, 71 remembered the specific year that they were affected. Most cases appeared
between 2008 and 2010.
94 | Chapter 3
When asked if they knew CL by any local name, 181 participants out of 448 replied “Leishmania”.
Twenty wrote a name connected with a “mosquito” and 15 described CL as a boil or a sore such
as the “boil of Ata”. (The Ata is an ethnic group living outside the Errachidia province). Finally,
two respondents noted “azmoulen”, an Amazigh word for “scar”. A minority of 26 students
wrote the name of a non-related skin disease, such as measles, eczema, syphilis, jaundice, or
urticaria.
The majority of respondents (n=356) stated that CL leaves marks and scars on the skin, usually
on the face (n=315). Girls more often than boys pointed out that CL leaves scars and that these
scars are on the face.
Half of the students evoked the existence of medical treatment against CL scars, while one third
quoted traditional remedies such as henna, eucalyptus, saffron, aloe vera, tea, Artemisia, Sahara
grass, among others. Some mentioned food items such as olive oil, lemon, eggs, honey, onion,
and garlic. Others evoked traditional practices such as burning the diseased skin, the use of tar,
acids (bleach, alcohol, bleach water), or urine of animals. In addition, four students referred to
the use of expired drugs (pills blended together or the application in powder form of an outdated
injectable antibiotic) in order to treat CL lesions. However, no one reported any specific
traditional remedy against CL scars.
Almost all respondents (86%, n=384) wrote that CL possibly or definitely has psychological
effects. Table 2 shows that there was no significant difference in response to this question
related to gender or personal experience with CL, although almost twice as many students from
the Rissani area (12.8%) considered there were no psychological consequences than students
from the Tinejdad area (6.6%).
The text analysis of the open-ended question about the possible CL impact is presented below
in three thematic sections: 1) CL severity and body image; 2) CL scars and stigma; and 3) dealing
with scars. A total of 52 boys (20.2%) and 24 girls (12.6%) did not answer the open-ended
question.
Psychosocial impact of CL scars on students | 95
Table 2: Potential psychological effects of CL scars on students, stratified by gender, area of
origin, and personal CL experience (n=422)
a26 missing data bTwo non-respondents to this question cOne non-respondent to this question
CL severity and body image
The students’ perception of the severity of CL can be summarized in three interrelated words:
“dangerous”, “serious”, and “deathly”.
Dangerous: CL is perceived by many as dangerous because of the fear of contagion and the risk
of transmitting CL to relatives: “It will lead to social isolation and the person will live away from
others due to fear of contaminating them.” (MT305). The fear is also given as an explanation of
the rejection by their own relatives: “The person affected is afraid by this disease as there is a
risk it could worsen and not heal. He will be disturbed by its appearance if seen [by others] and
be afraid that his friends and family will become distant from him and reject him for fear of being
affected by the same disease.” (MR081). Another boy wrote: “He will not be able to share meals
with his family.” (MT360).
Serious: One girl wrote: “The affected person will be disgusted to see himself in the mirror.”
(FT186). Another wrote: “Sometimes the affected people end up hating themselves.” (FR044).
Differences according to gender were observed in terms of use of the word “scar”. Many girls
but very few boys thought that CL scars are considerably worse for a woman than for a man.
According to our respondents, girls are more concerned about the effects of CL scars, the
appearance of their face, and the beauty of their body. Three boys reported that men are more
heavily affected by CL, as they lose their masculinity as a result of the disease. One boy evoked
the need for psychological support: “… Also it causes the patient psychological and
dermatological effects over a long period of time, which requires a visit to a psychiatrist.”
(MR121). One girl noted that both sexes suffered equally due to the disease (FR031).
96 | Chapter 3
Deathly: A few respondents thought (erroneously) that CL can have a fatal outcome and wrote
that death is the natural outcome of the disease. Interestingly, others evoked a fatal outcome in
the context of suicidal thoughts, as stated by one boy: “This disease often influences some people
because it leaves scars from the beginning that lead a person to commit suicide.” (MR123). In
addition, four girls cited the terms “depression” and “suicidal ideations” in their answers. One
girl noted: “Cutaneous leishmaniasis influences the psychological state and leads to death.”
(FT289).
CL scars and stigma
The fear of facing others was frequently mentioned by both sexes. “…The affected person cannot
talk about his disease due to fear of being rejected by people,” noted one boy (MR132). “The
person affected cannot show this to his friends because they will not want to sit with him,” said
another boy (MR160). The attitude of friends and family influences the psychological state of the
affected person, as reported by one girl: “She will have depression, a durable fear, and shame.
She does not have the absolute courage to sit with her friends for fear of their mockery.” (FT237).
Additionally, girls noted components of self-stigma such as shame, embarrassment, depression,
and self-contempt. One girl noted: “The affected person is very worried and feels ashamed in the
presence of people. She prohibits herself to go to rallies because of this disease.” (FT 225).
Another wrote: “The sequelae of leishmaniasis negatively influence the condition of the affected
person. A psychological complex will develop, and she will be ashamed to appear in front of
friends because it is a mark of shame and contempt.” (FT265).
The answers show how self-stigma and social stigma are linked. When the scar is formed, people
tend to stare at it and the gaze of others induces social rejection of the affected person. “It affects
me every time I meet my friends. They look at my scar, it diminishes my value in front of people,”
reported a girl who experienced CL (FR009). Consequently, communication barriers emerge:
“The scar is a mark of shame and contempt. The affected person will be unable to cope with
society due to fear of social discrimination and contempt.” (MT413). One girl noted: “She will
become closed off (introverted) and she will not talk to people and she is not going to love looking
at herself because of these scars.” (FT243). The affected person no longer has the same
appearance as before, and she/he is now different from others. The negative behavior of others
leads to a feeling of isolation and difficulty in everyday life: “There is a feeling of isolation and
loneliness, and a lack of stability in daily life because of the negative attitude of society towards
the patient,” wrote one boy (MR120). Another girl wrote: “For a girl when the disease leaves a
mark on the face, for example, the girl will think that is dangerous for her beauty, which will
influence her psychological state. Especially in our traditional society that is absolutely not lenient
towards those who have spots on the face because they think it is hereditary.” (FT194). CL can
lead to ‘social death’ as explained by one girl: “Moroccan society is not merciful and judges
Psychosocial impact of CL scars on students | 97
people’s appearance.” (FT241). Indeed, some participants linked CL scars with diminished
chances of getting married: “Often the scars in affected men and especially in affected women
are a barrier to getting married because the scars are visible, something that is not tolerated by
fiancés.” (FR049). Another girl noted: “Women have more fear on their faces, afraid that the
young man who comes forward to ask for her hand will disappear after having seen these stains.”
(FR001). A girl who previously experienced CL noted that the possibility of not getting married is
a problem only for women: “She will be afraid about her future especially for the wedding.
Meanwhile, in our society, an affected boy remains a man. There is no harm if he has scars.”
(FT202).
In addition, the fear to meet others leads to a lower self-concept: “The girl is ashamed to show
her face; scars can prevent her to leave the house, thereby increasing her psychological suffering”
(FR018). “Why me?” is a question that a person affected by CL often asks: “Why am I the person
who has this disease and carries this mark on the face?” reported a boy previously affected by
CL (MR153).
Dealing with scars
Half of the respondents wrote that treatment for CL scars was available in hospitals from general
practitioners or dermatologists. However, the affected person slowly understands after trying
various treatments that these scars will never disappear: “The psychological state of the affected
person could become worse after receiving treatment because the problem is that scars never
disappear [even after treatment],” noted a boy previously affected by CL (MR116). “The fear and
worry regarding the lack of treatment for this disease is the real problem for a person affected
by it,” added a girl also previously affected by CL (FR011). The ineffectiveness of delayed
treatment was also something stressed upon: “We need prompt treatment for this disease to
avoid any effect on the psychological state of the person affected.” (MR174). In addition, one girl
mentioned the problem of unaffordable treatment (FT224). Nevertheless, a number of
responses included questions about what was indeed, an effective treatment against CL scars.
“Is there a way to heal the scars?” wrote one girl (FR 068). Another girl wrote: “Is there a
treatment for scars? I wish there was a yes answer, there was a cure!” (FT195).
Various coping strategies were described as a solution to deal with the scars, especially among
girls, focusing on ways to hide the scars temporarily: “I am personally affected by this disease. I
suffer from its consequences. The scar on my face has created a big problem in my life. I am
obliged to put cream to try to hide it before going anywhere.” (FR035).
98 | Chapter 3
Alternatively, spiritual factors such as ‘God’s will’ and ‘destiny’ were the third care-seeking
explanations. Two boys and one girl mentioned that God decided who is to be affected by the
disease and who will be healed. One boy also suggested these scars need to be accepted “…After
a while, he will get used to those scars and it will become normal.” (MR096). Contrastingly, other
students asked for direct government intervention: “This disease could leave psychological
trouble in the affected person. That is why the government and the concerned commission must
find a solution for this disease, it’s not the duty of the population,” wrote one boy (MR093).
Another boy noted that the population along with the policymakers should be involved in the
prevention of this dangerous disease (MT355).
Discussion
This study showed that 20% of the boarding school students who were surveyed in this CL-
endemic region of Morocco had been affected by CL in the past and almost all believed there
were potentially psychological implications. CL was found to be relatively well known. Our
findings show that CL and its ensuing scars led to a considerable psychosocial burden in this
adolescent age group. Girls seemed to be more affected than boys, but both genders equally
expressed their concerns and demands for treatment. In this context, adequate dermatological
care was beyond the reach of most of the participants due to the poverty of their families. It
should be noted that in this Moroccan sociocultural context, scarification marks are common in
rural and remote areas in the elderly population and people also contract scars frequently in
agricultural work. Traditional tattoos are considered a sign of beauty, a mark of tribal
identification, or a protection against sin and malicious witchcrafts [26]. However, nowadays this
cultural practice is less commonly accepted by the younger generation living in the same area,
and none of the adolescents referred to it. A large majority of them highlighted the negative
psychological consequences and the stigmatizing effect of CL and its scars.
Students pointed to a large spectrum of negative psychosocial effects, ranging from slight shame
to suicidal thoughts. Social exclusion of CL patients has also been reported elsewhere in the
literature [8]. In its most extreme form, students equated CL with ‘social death’ due to the
visibility of CL scars, which has also been reported by other authors [27–29]. If a CL scar is located
on the face, it is perceived as a barrier to marriage and in this traditional society, this can imply
‘social death’ for women. The participants in this study made comments to this effect
spontaneously, without any trigger related to marriage built into the questionnaire. This
therefore reflected a deep concern in the adolescent age group. The finding is consistent with
previous research reporting that CL scars had a deeper impact for women who remained
unmarried, especially in a society where early marriages for girls are common [12].
Psychosocial impact of CL scars on students | 99
In addition, while several respondents viewed CL scars as a curse, others accepted them within
a spiritual context, which requires praying, asking for forgiveness, and having patience and faith
that God has a treatment for every disease or a plan for it whether it will be treated or not.
The findings in this study illustrate the conceptual model of stigma developed by Pryor and Bos
and colleagues (see Figure 1). In this traditional Moroccan society, the presence of skin lesions
on the face and other exposed body parts leads to public (social) stigma, at least in the
adolescent age group, as the cognitive, affective, and behavioral reactions of people to a skin
lesion affecting the face are negative and lead to social avoidance [30]. Notions of contagion, of
congenitally transmitted infections, and of fatal illness are associated with lesions. In this
context, the presence of a CL scar leads to a depreciation of body image in the affected person,
which is, of course, dependent on age and gender, but female adolescents are highly vulnerable,
as shown in the literature [31, 32]. The ensuing self-devaluation [28, 33] and deterioration of
self-concept [23] leads to self-stigma that is perpetuated due to the protracted nature of the
scars. Hence, the explicit demand for this age group is to treat CL more quickly and effectively.
Our study had some limitations. Firstly, the self-administered questionnaire method inevitably
provides less detailed information than an individual in-depth interview would generate. For
instance, we do not have in-depth explanations for the underlying reasons of shame and
contempt induced by CL, and we see a need to conduct focus group discussions in the future to
better document the social representations of this disease. However, we chose the method of
using a self-administered questionnaire format for ethical reasons, as it would have been difficult
to arrange individual interviews in an anonymous way in this environment of a boarding school.
We wanted to avoid enhancing harassment and mockery among students in such a closed
environment. Secondly, there was a relatively large group of non-respondents to the open-
ended question (n=76). This could be explained for 59 participants by the fact that they did not
know about the disease or any person affected by it. Thirdly, the previous personal CL scar
experience was based only on the self-declaration of the participants and we had no formal
verification of this information.
Conclusion
This is the first study done in Morocco documenting the psychological effects of CL scars in the
adolescent population living in CL-endemic areas. The indelible CL scars lead to self-stigma and
social stigma, and the emergence of negative psychological effects in this age group. Preventing
the avoidable burden of CL and mitigating its dermatological and psychosocial consequences
should be a priority for health authorities. We suggest that the control of CL in the North African
region should be envisaged in an interdisciplinary, multi-sectoral approach, preferably in a
regional framework to prevent as much as possible the avoidable suffering.
100 | Chapter 3
Additional files
Additional files 1: Multilingual abstracts in the five official working languages of the United
Nations. (PDF 763 kb)
Additional files 2: English translation of the self-administered questionnaire. (PDF 327kb)
Additional files 3: Original version of the questionnaire in Arabic (PDF 1639 kb)
Additional files 4: French translation of participants’ responses to the last question in the
questionnaire: Could you write a small paragraph about the probable psychological state of the
person (woman or man) affected by those scars? (PDF 404kb)
Additional files 5: Access database file including full questionnaire and student responses
(ACCDB 1416 kb)
Abbreviations
CL: cutaneous leishmaniasis; FR: female from Rissani area; FT: female from Tinejdad area; MR:
male from Rissani area; MT: male from Tinejdad area
Acknowledgments
We express our gratitude to all boarding school students and their teachers. A special thanks go
to Mr. Chichaoui Smaine from the Delegation of the Ministry of Health in Errachidia province for
his administrative assistance.
Psychosocial impact of CL scars on students | 101
Funding
IB is supported by a doctoral grant from the Belgian Directorate General for Development
Cooperation. The funder had no role in the study design, data collection, and analysis, decision
to publish, or preparation of the paper.
Availability of data
The data sets supporting the conclusions of this article are included in the article and its
additional files.
Authors’ contributions
IB, ST, HF, VDB, HS, and MB drafted the study protocol. IB conducted the data collection. IB, HF,
ST, VDB, and MB analyzed the qualitative part of the data. IB, ST, and MB analyzed the
quantitative data. IB wrote the first draft of the paper and all authors participated in its critical
review. All authors endorse the final version and approve the submission.
Competing interests
All authors declare that they have no competing interests.
Consent for publication
Not applicable.
Ethics approval and consent to participate
Approval for the study was obtained from the representatives of the Ministry of Education and
Ministry of Health in Errachidia province and from the two participating high schools’ education
officials. The study, as part of a social representations project, was approved by the CERB
Biomedical Research and Ethics Committee in Rabat, Morocco, and by the Institutional Review
102 | Chapter 3
Board of the Institute of Tropical Medicine in Antwerp, Belgium. Written informed consent was
obtained from each participant. Students were free to refuse to partly or completely answer the
questionnaire and no names were asked for nor recorded.
Author details
1National School of Public Health, Ministry of Health, Rabat, Morocco. 2Department of Public Health, Institute of Tropical Medicine, Antwerp, Belgium. 3Department of Biomedical Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary
Sciences, University of Antwerp, Belgium. 4Hassan II Institute of Agronomy and Veterinary, Rabat, Morocco. 5Ecole Nationale de Santé Publique, Rue Lemfedel Cherkaoui, Madinat Al Irfane 10000, Rabat,
Morocco.
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Social impact of CL | 107
CHAPTER 4. Social impact of Cutaneous
Leishmaniasis in Southeastern Morocco,
A qualitative study.
Bennis, Issam, Loubna Belaid, Vincent De Brouwere, Hind Filali, Hamid Sahibi, and
Marleen Boelaert. “The mosquitoes that destroy your face”. Social impact of
Cutaneous Leishmaniasis in Southeastern Morocco, A qualitative study." PloS one
12, no. 12 (2017): e0189906.
Social impact of CL | 109
“The mosquitoes that destroy your face”. Social impact of Cutaneous
Leishmaniasis in South-eastern Morocco, a qualitative study.
Issam Bennis1,2,3, Loubna Belaid4, Vincent De Brouwere2, Hind Filali1, Hamid Sahibi5, Marleen
Boelaert2*
Author affiliations:
1 National School of Public Health - Ministry of Health, Rabat, Morocco.
2 Department of Public Health - Institute of Tropical Medicine, Antwerp, Belgium.
3 Department of Biomedical Sciences - Faculty of Pharmaceutical, Biomedical and Veterinary
Sciences- University of Antwerp, Belgium.
4 CRCHUM, École de Santé Publique de l’Université de Montréal, Canada.
5 Agronomy and Veterinary Institute Hassan II-Rabat, Morocco.
* Corresponding author Marleen Boelaert. Email: [email protected]
Keywords: Cutaneous leishmaniasis; Scars; Stigma; Qualitative research; psychosocial burden;
Morocco
Received: September 25, 2017, Accepted: December 4, 2017, Published: December 20, 2017
110 | Chapter 4
Abstract
Objective: To document the psychosocial burden of Cutaneous Leishmaniasis (CL) in rural
communities in Southeastern Morocco.
Method: Between March and April 2015, we conducted qualitative research in communities
exposed to Leishmania major or L. tropica in Errachidia and Tinghir provinces. Twenty-eight
focus groups discussions (FGDs) were realized, with a stratification by gender and tradition of
medicine (users of folk versus professional medicine). Data were analyzed using content analysis.
Results: This rural population most exposed to CL in Morocco lacks access to health care in
general and clearly points out there are other major public health issues that need to be resolved.
Nonetheless, respondents consider the impact of CL lesions and scars as important and similar
to that of burn scar tissue. Young women with CL scars in the face are stigmatized and will often
be rejected for marriage in these communities. People usually try a long list of folk remedies on
the active lesions, but none was felt adequate. There was a clear demand for better treatment
as well as for treatment of the scars.
Conclusions: The psycho-social impact of CL due to L. major and L. tropica is substantial,
especially for young single women with facial scars. These generate social and self-stigma and
diminish their marriage prospects. CL is well known, but not considered as a major health priority
by these poor rural communities in Southeastern Morocco where gender discrimination is still
an issue and access to basic health care is as neglected as CL. Early CL diagnosis and new
treatment options with better skin outcomes are urgently needed.
Social impact of CL | 111
Introduction
Leishmaniasis is a vector-borne disease caused by protozoan species of the genus Leishmania
and transmitted by different sand fly species of the Phlebotomus and Lutzomyia genus. The
disease manifests as one of three main clinical presentations: visceral, cutaneous or
mucocutaneous [1, 2]. Cutaneous Leishmaniasis (CL) is quite common in Morocco and is caused
by the anthroponotically transmitted L. tropica or the zoonotic L. major species [3, 4]. In some
areas, both causal species coexist [5, 6]. CL has led to epidemic outbreaks in Morocco in the past,
the most recent one occurring between 2004 and 2013 in the Southeast of the country with
more than 10,000 recorded cases [7, 8].
Most CL lesions develop on the uncovered parts of the body as those are most exposed to the
sand fly bites [9]. In Moroccan patients, CL lesions are of the “localized” type and start as one or
multiple slowly progressing nodules that subsequently ulcerate. The healing of this skin ulcer
usually leads to substantial scar tissue, which can be quite disfiguring (Figs 1 and 2). CL tends to
be considered as a minor illness when compared to the visceral and mucocutaneous forms of
leishmaniasis that have fatal or severely mutilating outcomes. However, little research has
actually been done about how the affected communities perceive CL, what their explanatory
model is for it, and how they deal with this illness. A number of Knowledge, Attitude, and
Practices (KAP) surveys in different countries and age groups showed a general lack of knowledge
regarding CL symptoms, transmission mode, and reservoir [10–18]. We observed in our previous
work in adolescent youth living in the region affected by the CL epidemic that in this age group
the psychological impact is real and the demand for prevention and care, especially for the repair
of scar tissue was clearly formulated [19]. We wanted to expand this work to the general
population, as a contribution to the formulation of sound control CL policy.
112 | Chapter 4
Fig 1. CL scar on the forearm of a man living in a L. major endemic area in Southeastern Morocco (Picture was taken by IB)
Fig 2. CL scar on the hand of a woman living in a L. major endemic area in Southeastern Morocco (Picture was taken by IB)
The aim of this study is to describe the social burden generated by CL in Morocco, by exploring
the community perspective on this illness and social consequences related to CL in the adult
population living in rural endemic areas in Southeastern Morocco.
Social impact of CL | 113
Method
We followed the Consolidated Criteria for Reporting Qualitative research (COREQ) to report our
findings. A checklist is provided as supporting information (S1.file).
Research team
Our research team was multidisciplinary, composed of three public health experts with a medical
background, two psycho-social scientists and one veterinary scientist. The principal investigator
(IB), who is a male Arabic-speaking researcher with a medical background and special training in
qualitative research methods, conducted the fieldwork. He was not involved in clinical care in
the area and was not known to the study participants. He was accompanied by a male health
worker or a female community member known to the respondents.
Study design
Participant selection and setting
Our primary aim was to describe the community perspective on CL following a qualitative
explanatory case study approach [20]. We conducted Focus Group Discussions (FGDs) between
March and April 2015 in two provinces in Southeastern Morocco: Errachidia and Tinghir (Fig 3),
the first endemic for L. major and the second predominantly for L. tropica [7, 21]. Table 1 shows
the recently reported caseload of CL by species in these provinces. According to the High
Commission for Planning in Morocco, poverty rates in both provinces are high (18-24%) and
unemployment rates (9-16%) are higher than in other regions of Morocco.
Fig 3. Map showing Tinghir and Errachidia Provinces located in Deraa-Tafilalet Region,
Morocco. (Source www.hcp.ma)
114 | Chapter 4
Table 1. Number of cases of CL due to L. major and L. tropica in southeastern Morocco
as notified to the Ministry of Health (2013-2016)
L. major cases L. tropica cases
2013 2014 2015 2016 Total 2013 2014 2015 2016 Total
Errachidia
Province
11
12
231
896
1150
0
0
0
0
0
Tinghir
Province
155
90
116
342
703
337
244
110
504
1195
Ouarzazate
Province
89
170
358
353
970
0
85
61
102
248
Total
Morocco
537
460
954
1889
3840
2054
2094
1859
3062
9069
In each province, we purposefully chose the two districts with the highest number of CL cases
notified between 2009 and 2013. Within each district, we used snowballing as purposive
sampling strategy to select study participants from the CL endemic areas aiming for maximum
diversity in age, gender, and socioeconomic background.
We pre-planned a stratification of the FGDs on two dimensions: gender and a cultural preference
for the tradition of medicine (folk or allopathic medicine). The purpose of this stratification was
to allow a free and uninhibited discourse within groups. The users of the allopathic sector were
invited by approaching people who accompanied their relatives to the health centers in villages.
To reach the people who prefer folk healers, we used a snowballing approach starting from key
informants in the villages who put us in touch with traditional healers and their networks.
In total, we conducted sixteen FGDs: in each of the four districts, there were four FGDs: one with
male and one with female clients of the formal health sector (henceforward indicated as
‘allopathic’), and one with male and one with female users of folk medicine (‘folk’). Based on our
findings in Errachidia province, however, we decided to add twelve more FGDs to include the
perspectives of specific communities that were living in very remote and difficult to reach areas.
A total of 251 participants attended the 28 FGDs.
Social impact of CL | 115
FGDs included between seven and fourteen participants in each session. Four men and ten
women in Tinghir and seven men and nineteen women in Errachidia, all users of the allopathic
sector, refused our initial invitation. Reasons invoked were a lack of time, impossibility to leave
their children in the care of someone else, or failure to obtain approval from their spouses. No
participant received any incentive.
We organized the FGD sessions based on what our respondents proposed as suitable time and
location. The discussions took place in quiet rooms that provided sufficient privacy, such as
coffee houses, mosques, schools, private houses or local NGO offices.
Data collection
During the FGD we used a topic guide inspired by Brown et al., [22] who analyzed the
determinants of quality of life in patients with scar tissue (see supporting information S2.file).
Topics included knowledge of CL, physical and psychological consequences, behavior, social
impact, treatment outcome and knowledge of preventive measures. After completion of the first
two FGD, we adapted the topic guide slightly, as we wanted to better understand the perception
of CL scars and the attitude/behavior towards people with CL scars better. Thus, we added two
questions: ‘How can you make the scars go away?’ and ‘How do people, in general, behave with
those affected by this disease?
The two main languages used for these discussions were the Amazigh (local language) and
Moroccan Arabic. Each FGD was recorded with audio and video recording except for three FGDs
for which we only used audio recording at the request of the participants. At the end of each
FGD, the researcher took notes after discussion with the observer. An average of 39 minutes
(range 28-64) duration was observed for the initial 16 FGDs and an average of 31 minutes for all
FGDs (Table 2).
116 | Chapter 4
Table 2. FGD’s duration and participants’ characteristics
Tinghir
Province
Errachidia
Province
Additional
FGD *
Health facility (Allopathic) clients
Number of FGD 4 4 6
FGD mean duration in minutes (min-max) 41 (31-60) 32 (28-35) 18 (15-23)
Total number of female participants [age
range in years]
16 [19-46] 22 [19-58] 23 [19-68]
Total number of male participants [age
range in years]
16 [24-57] 22 [21-60] 22 [20-67]
Traditional medicine (Folk) clients
Number of FGD 4 4 6
FGD mean duration in minutes (min-max) 42 (37-46) 40 (29-64) 23 (14-32)
Total number of female participants [age
range in years]
24 [21-82] 19 [19-58] 23 [19-68]
Total number of male participants [age
range in years]
16 [24-57] 22 [21-60] 22 [20-67]
FGD: Focus group discussion
(*) done in Errachidia province to reach saturation
Data Analysis
We followed the process of directed content analysis to analyze the text data [23]. FGDs were
transcribed and translated into French. Two persons (IB, HF) independently coded data, one
using NVivo 10 software and the other one coded manually. We adopted a single coding
framework, including themes and subthemes, see Table 3. The codes were informed by our
previous work targeting the adolescents [19] and the conceptual model by Brown et al., 2008
[22]. We used the main themes as a structure for reporting our findings.
Social impact of CL | 117
Table 3. Themes and subthemes in the coding framework
CL Knowledge Gender discrimination
CL name
CL causes
CL symptoms
CL transmission ways
Marriage opportunities
Stigma
Coping strategies
Prevention strategies
CL Perception Health seeking patens for CL
CL severity
Skin outcome
Psychological effects
Treatment accessibility
CL traditional remedies
CL conventional therapies
CL scar treatment
Ethical considerations
The Institutional Review Board of the Institute of Tropical Medicine in Antwerp Belgium
(956/July.2014) and the Ethical Committee of Biomedical Research of the Faculty of Medicine
and Pharmacy in Rabat Morocco (1139/04_Nov.2014) have approved the study. We obtained
the authorization to conduct the study from the national and local Ministry of Health authorities.
Participation in the FGD was entirely voluntary. Invited participants were given an information
sheet (Supporting information S3.file) to read, and asked to present themselves at the
appointment for the FGD at a specific day and time if they agreed to participate. At the specific
setting, their oral consents were recorded on audiotape. The participant’s identities were
anonymized in the data. Feedback on our findings will be given to the communities after the
results of this work will be published.
118 | Chapter 4
Results
Without having put ‘young age’ as an exclusion criterion, all respondents in our FGD were more
than 19 years old, and this was the case in both male and female groups (see Table 2). The FGD
participants did not allow the young and adolescents to sit with them and to participate in this
discussion. We present the results within four themes: CL knowledge; CL perception; gender
discrimination; health-seeking patterns for CL.
CL Knowledge
The people in this region know CL as the “disease of the scars” and describe the natural evolution
rather accurately, as a spot or several bumps on the skin you develop after a mosquito bite,
sometimes blistering or ulcerating but not healing for four to six months and eventually leading
to a permanent bluish/black mark or scar. In this rural society, almost everybody has some scar
tissue, but the local names for CL as the “mosquito sore” or the “mosquito scar” clearly
distinguish them and link the skin lesion to an insect vector. All FGDs said that the sore was
caused by the bite of a mosquito (chniwla), and the, distinction between mosquito and sand fly
was not made. However, the causal chain between an insect bite leading to CL and later scar
tissue was very clear for everybody. One person summarized this as “the mosquitoes that destroy
your face”. Other names were used as well, usually referring to the locality where the problem
was first observed, such as “sore of Touroug.”
Respondents also spontaneously used the terms ‘leishmania’ or ‘leishmaniasis’. In Errachidia
province, the term seemed familiar to many in all the allopathic FGD groups and in some of the
folk medicine ones. Contrastingly, in Tinghir, the term ‘leishmaniasis’ was only used in two
allopathic FGD and not in the others. People in Tinghir seemed less familiar with CL in general
and did not think it was common in their area, whereas in Errachidia many respondents had
experienced CL themselves or had relatives and friends affected by it.
FGDs respondents stated that CL is not contagious by direct contact, nor transmitted by water.
Stagnant water, manure, dead rats, and pollution, in general, were repeatedly evoked as risk
factors, as they increase mosquito density. People acknowledge that the risk is seasonal, and
higher in summer. In summer, people tend to sleep outside which exposes them to more
mosquito bites. Insect nuisance was said to be substantial in the villages, and a quiet night of
sleep hard to get by because of this. Women were considered most exposed to mosquito bites
as they engage in farming activities taking care of cattle and dealing with manure and waste.
Little children and tourists were thought to be more vulnerable as well, and a few respondents
attributed this to their lack of immunity, sweeter blood or softer skin.
Social impact of CL | 119
CL perception
Several women in the Errachidia area compared the severity of CL to that of acne and stated that
CL is more severe. “Leishmania is more unpleasant than acne. Acne is not pitting, but leishmania
digs the skin” (FGD15 Women-Allopathic). In some cases, the lesions can be truly incapacitating
depending on the location, such as eyes, foot soles or hands. Active lesions on the hands impair
the daily work of women. “If the disease is not on the hands you use to prepare the bread and
meals, it's not a problem.” (FGD10 Women-Folk).
All FGDs agreed that the scar tissue of CL can be a real problem, mostly for women. “The most
serious is the scar in the middle of the face. If it is on the side of the face it can be hidden by the
veil” (FGD26 Women-Allopathic). A CL scar was considered similar to a burn scar: “The scar does
not disappear. It leaves a mark as if you were burned by fire and even worse. Look at my own
hand for example. I have a Leishmania scar and that is another scar from a burn. There is no
difference! Because of the burn, the muscles located under the skin also disappeared.” (FGD22
Men-Allopathic).
Several participants expressed anxiety about CL, especially that it would affect their children.
“We are afraid that this disease would come back in the future because the mosquito is still
there.” (FGD21 Women-Folk). In addition, three participants worried about the possible
transformation of the scars into skin cancers in the near future. “…maybe this scar will change in
the future into a bad disease [cancer]” (FGD04 Women-Folk).
Contrastingly, some individuals in the male groups considered CL as a benign problem as it is not
contagious and not fatal. One of them said “An epidemic of leishmania occurred in the past, there
were many complaints. Now people forgot this disease. Nowadays if you ask someone something
about leishmaniasis, he or she will say (s)he does not know anything about it…” (FGD14 Men-
Folk). Moreover, several participants, mainly in Tinghir, raised other health issues which were of
more direct concern to them than CL. Access to obstetric care was definitely considered a bigger
problem in these remote rural villages than CL.
Gender discrimination
In these rural societies, marriage is considered as a goal in life and an award for every woman.
All FGD respondents highlighted that a young woman risks never to get married if her face is
affected by CL. “At work, it is not a problem but for the marriage, a man will see the scar on the
girl’s face and he will go away. It’s possible that the girl will never get married” (FGD01 Men-
Allopathic). This was even more clearly expressed by the women in the folk medicine tradition-
FGDs who said they would stay polite with a young woman affected by CL and would share
household chores such as cleaning and cooking but that this did not imply they agreed to get
120 | Chapter 4
their sons married to her. “It’s ok for day-to-day exchanges, some polite words, good morning,
good night. We pay attention not to hurt her feelings. But marriage? No way.” (FGD04 Women-
Folk). Others pointed to CL being a reason for revoking marriage vows. “There was the case of
the girls who were engaged and later got this disease. They were told, we stop [the engagement],
go treat yourselves and get cured before we can go on with the marriage. These girls were
affected either on their faces or on their foreheads.” (FGD20 Women-Folk). As stated above,
some male respondents held contrasting views and considered that: “this was not a huge
problem if the girl will never get married” (FGD01 Men-Allopathic). It seems also that within the
context of customary intra-family marriage, the man cannot reject the woman for this reason.
Interestingly as well, CL scars that would appear after marriage are no reason for divorce. “The
husband cannot divorce his wife if she is affected by this disease. Because she became ill in his
house.” (FGD19 Men-Folk).
The extent to which CL leads to social stigma beyond limiting the marriage prospects for women
is not uniform. In both provinces, people incriminated the nearest locality to have had the
disease earlier before contaminating them via mosquito or rodents. Participants from the area
where the disease first appeared in Errachidia mentioned strong social rejection by other groups
in the neighborhood. Some said to be ashamed to live in a village with CL “Men and women of
the neighboring locality start insulting us and laughing at us.” (FGD28 Men-Folk). Some feel also
rejected by their relatives living abroad who contracted CL during their holidays in Morocco.
Some women affected by CL tend to hide their lesions for fear of stigmatization. Others felt
uncomfortable to share a meal with somebody with an open sore, mostly for fear of
contamination. Nonetheless, many participants described a change in attitudes over time,
towards less discrimination “At the beginning, many persons who saw me told me I must remove
this. My face became less beautiful than before. I was also upset. Every time you touch it, you
feel something on your face. You feel it and it is disturbing. After a while, you forget its presence”
(FGD04 Women-Folk).
Several times the male respondents expressed they did not see any reason for social rejection,
as it is quite common to see scars from various causes in everyday life in this rural context. A scar
becomes a part of the person and the society is accustomed to it. Moreover, CL does not change
their personal relationships and interactions. “What is the matter to have an additional scar? It's
normal!... Even for women, it is the signature stamp of our area.” (FGD01 Men-Allopathic).
Social impact of CL | 121
Health seeking patterns for CL
Everybody had an opinion about CL treatment, best summarized as ‘we try everything, but
nothing works’. More than thirty ways of self-treating the skin bumps were cited including food
items (honey, oil, eggs, saffron, salt, tea, vinegar, chillies), herbs (henna, Aloe-Vera, fenugreek,
basil, rose water), but also harmful products (white spirit, gasoline, tar, bleach water, crushed
outdated pills) or alcohol and soap. People try to get rid of the bump by scratching, cutting or
burning it. Folk healers often apply burning as well, e.g. using sulfur powder. Besides, they apply
water from natural sources, sand, and soil to cure the lesion. The ulcers are treated differently,
with different mixtures, such as dust, hair and crushed glass, or salt and tobacco. Scars are
treated with a long list of different products (lemon to lighten the color, several oils such as oil
of cade, but also used motor oil, white spirit, rose water, salt, ...).
Conventional treatment in health facilities was a matter for debate. Participants noted that
protocols varied, from ointments to a variable number of injections. Some worried about side
effects “They said that the injections have bad effects on the kidneys” (FGD09 Men-Folk).
Though some acknowledged you have to be treated early to see some effect, several pointed
out that the results were often disappointing “She said to me that she followed the treatment
for four weeks every two days per week. But now after the end of those treatments, she has a
blue color.” (FGD02 Women-Allopathic). “Do you see the spot on the hand of this man sitting
near to me, even if it appears like it is healed the margins are full of the disease, if you touch it, it
is not yet cured” (FGD09 Men-Folk). The demand for scar treatment was more pronounced in
Errachidia than in Tinghir province.
Mostly, respondents highlighted the lack of effective remedy for the disfiguring scars. “I tried
everything to make the scar disappear. I became like an herbalist. Until I get tired and I accept
the presence of this scar on my face. For me cosmetic surgery is dangerous, it may even lead to
the development of cancer. So better leave the scar where it is.” (FGD24 Women-Allopathic). Very
few participants, mainly from the allopathic groups, said progressive healing is possible,
especially in children who get early medical treatment.
Some respondents emphasize that cosmetic surgery is not accessible and not affordable “…the
specialists in dermatology are far away. You should go to another town. The doctors there bite
you more than the mosquito-bite (Laugh). People are different, there are some who have money
and some without. Then, many people accept the reality and ignore the presence of this disease.
They use natural treatments which is more economical and better than looking for aesthetic
surgical interventions” (FGD08 Women-Folk). Moreover, cosmetic surgery was considered of
little benefit compared to the huge cost. “Leishmania made muscles under the skin disappear.
122 | Chapter 4
That is why there are doctors who say that even cosmetic surgery is not going to give good results
for the scar of Leishmania” (FGD22 Men-Allopathic).
Discussion
Our extensive discussions with members of these rural Moroccan communities learned us that
CL is definitely not the main health problem in these remote areas, but nonetheless generates
substantial suffering, mainly in women, due to the disfiguring skin outcomes and the social
stigma surrounding it. Our respondents described the psychosocial impact of CL as more severe
than that of acne and as similar to that of scar tissue from burns. We observed substantial gender
differences related to this perceived burden. Women bear the highest burden of CL, as, beyond
the physical discomfort of active lesions on hands etc., they seem more stigmatized. The
emotional well-being of young single women with facial lesions was said to be strongly affected
by CL scars, and this corroborates our earlier findings in adolescent youth [19]. Moreover, our
respondents considered women at higher risk for CL due to their agricultural and household
chores.
The explanation used by these rural community locates the origin of CL clearly in the natural
world: the causal link between the insect bite and the skin lesion is made very clearly and
specifically, even if the insect is mostly (and erroneously) identified as a mosquito, whereas it is,
in fact, a sand fly. Risk factors for CL are also very correctly identified as all factors that increase
vector abundance. One could ask if the link with rodents is made sufficiently strong in the L.
major areas. Unfortunately, there is so far, no effective and sustained community involvement
in CL control. Any ongoing reservoir or vector control interventions target perceived immediate
risks, like the threat of wild rodents to the agricultural production or the insect nuisance
preventing a quiet night sleep in summer days.
At the closer examination of the notion of the stigma surrounding CL, it seems that this is mostly
linked to scars on the face, and then mostly in young women. This type of lesions is only a small
subgroup of all the CL lesions. In our study, CL seemed a lesser problem in the group of users of
“folk medicine”, as they seem to care less about the scars. Due to their very harsh everyday life
conditions, another scar may then make little difference. The main contrast between users of
the folk and allopathic tradition was that the latter considered the CL scars as an unsatisfactory
sequela requiring an effective medical solution. It may be interesting to conduct further research
on differences in perception according to causative species. The larger size of CL and CL scars
may generate more concern in the L. major than in L. tropica areas, though the latter lesions are
more protracted.
Social impact of CL | 123
Health seeking behavior patterns for CL and CL scars were multiple and overlapping
encompassing the health care traditions of self-help, folk, and allopathic medicine. The effect of
the toxic and abrasive products and burns used in self-remedies and by traditional healers on
the extent of scarring should not be underestimated, and there is a scope for better information
and education of the community in this field.
Our findings are consistent with the few available qualitative studies on CL from elsewhere in
the world. In Kabul, Afghanistan, women were at higher risk than men to contract CL and affected
people were excluded from social life leading to emotional and physical isolation. Similarly to our
findings, women faced difficulties to get married if they had a CL lesion or CL scars [24]. Likewise,
in Yemen, a review emphasized the stigmatizing potential of disfiguring CL in women [25]. In
contrast, in Suriname, where CL mainly affected men, the only factor that generated stigma was
the presence of a big (or multiple) CL lesion(s), but no barriers to the marriage were evoked [26].
Contrastingly, mucocutaneous CL in Latin America was linked to constant stigma and permanent
psychological effects [27–31].
Our qualitative approach derives its strength from a conceptual framework, with an iterative
process used in the development of the data collection tools, and the pursuit of saturation in the
information reached with the use of additional FGD. The findings from this set of FGD combined
with informal interviews and observations on the ground is considered by our team more valid
to capture the socio-cultural diversity in interpretations of CL-illness than the use of a restricted
number of in-depth interviews with former or actual CL patients. Our study had some limitations
though. Some statements by respondents may have been subject to social desirability bias, e.g.
when people were informed that the moderator works as a researcher in a national public health
institute, this triggered their interest about national health policies and specific health needs in
the area. However, we do not think it had a major effect on the way the groups voiced their
perception of CL. Secondly, our categorization of FGD into preferred health care tradition (folk
medicine versus allopathic) was not mutually exclusive and may not have captured the full
spectrum of care traditions, but it certainly helped us to explore the community perspective
across a range of socio-cultural groups in this context.
In conclusion, this qualitative study is the first in Morocco to address the perspective of the
population on CL and CL management. As all qualitative research, its main limitations lie in the
generalizability or what is called its external validity. Said otherwise, to what extent are our
findings representative for other provinces in the country and region? As our findings are
consistent though with a larger body of evidence from quantitative KAP studies and
psychological assessments by questionnaire surveys and with qualitative research based on FGD
conducted earlier in Afghanistan and Surinam, we believe the findings are robust and should
inform policy. CL is a true problem in this region, very much intertwined with gender
discrimination and lack of access to basic health care in remote rural areas. In dialogue with the
124 | Chapter 4
community, sound prevention and control policies should be designed. One of the main
implications of our findings was that innovation in CL early diagnosis and treatment is
desperately needed. The management of existing disfiguring CL scars remains also a subject of
further research. In summary, CL is well known but not considered as a major health priority by
these poor rural communities in Southeastern Morocco with lots of competing health problems.
Its psychosocial impact is substantial though and can be in some cases very important, especially
for young single women with facial scars, generating social and self-stigma and diminishing their
marriage prospects. A new treatment for CL with better skin outcomes is urgently needed.
Supporting information
S1_File.pdf: COREQ Checklist (DOCX)
S2_File.pdf: Translated FGD topic guide (DOCX)
S3_File.pdf: Original participant Information sheet (PDF)
Acknowledgments
We wish to thank all participants for their time. Special thanks to Mr. Moulay Ahmed Hajji and
Mr. Smaine Chichaoui from the health delegates of Tinghir and Errachidia and all health
professionals, participants, and hosts who agreed and helped to realize these FGDs in optimal
conditions. Our thanks to Evelien Paessens and Anne Marie Trooskens for support with language
–editing and layout of the manuscript. We wish also to thank the Moroccan Ministry of Health
for facilitating this study.
Author Contributions
IB, the principal investigator was involved in the concept, design, development of the study and
the instruments, as well as in the implementation, collect and analysis and reporting aspects of
the study. He wrote the first draft of the manuscript.
LB, HF, HS provided expert advice for the study design and writing of the manuscript.
HF, VDB, and MB revised the protocol, assisted in data analysis and provided suggestions to
improve the study design and manuscript.
All authors have read and approved the final version of the manuscript
Social impact of CL | 125
Funding
The financial support of the Belgian Directorate General for Development Cooperation for this
research is acknowledged.
The funding organization had no role in the design and conduct of the study; collection,
management, analysis and interpretation of data; preparation, review or approval of the
manuscript; nor the decision to submit for publication.
Competing Interests
The authors have declared that no competing interests exist.
Data Availability Statement
Public deposition of our data would breach compliance with the protocol approved by our
research ethics boards, as we promised to ensure confidentiality of our participants. Our data
are audio and video recordings of our group discussions and written transcripts of those. The
former allows for easy identification of participants and cannot be shared. The written
transcripts allow also for identification in combination with the information on time and location
of the session and knowledge of the village.
We are willing to make the transcripts available to qualified researchers on condition of signing
a data sharing agreement. Qualified researchers can contact the chair of the Antwerp IRB,
Prof.Dr. A. Buve, ([email protected]) in case they would like access to the transcripts.
The corresponding author had full access to all the data in the study and had final responsibility
for the decision to submit for publication
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Review of LCL Psychosocial burden | 129
CHAPTER 5. Psychosocial burden of
localised cutaneous leishmaniasis :
a scoping review.
Bennis, I., De Brouwere, V., Belrhiti, Z., Sahibi, H., & Boelaert, M. (2018). Psychosocial burden of localised cutaneous Leishmaniasis: a scoping review. BMC public health, 18(1), 358.
Review of LCL Psychosocial burden | 131
Psychosocial burden of Localised Cutaneous Leishmaniasis: a scoping review Issam Bennis1,2,3*, Vincent De Brouwere2, Zakaria Belrhiti1,2,4, Hamid Sahibi5, Marleen Boelaert2
Authors’ affiliations
1-National School of Public Health - Ministry of Health, Rabat, Morocco. 2-Department of Public
Health - Institute of Tropical Medicine, Antwerp, Belgium. 3- Department of Biomedical Sciences
- Faculty of Pharmaceutical, Biomedical and Veterinary Sciences- University of Antwerp, Belgium.
4-Vrije Universiteit Brussel 5- Department of Pathology and Veterinary Public Health, Hassan II
Agronomy and Veterinary Institute, Rabat, Morocco.
* Corresponding author
Email: [email protected]
GSM: 00212661259901
Address: National School of Public Health, Lemfedel Cherkaoui Street, Madinat Al Irfane,
10000, Rabat - Morocco
132 | Chapter 5
Abstract
Background
Cutaneous Leishmaniasis (CL) is a parasitic skin disease, linked to poverty, and belonging to the
group of Neglected Tropical Diseases. Depending on the severity, the type of lesions or scars,
and the context, CL can lead to self- and social stigma influencing the quality of life and
psychological well-being of the patient. This dimension is, however, little documented for the
most common, localized form of cutaneous leishmaniasis (LCL).
We aimed to describe the current knowledge on the psychological burden and the stigma related
to LCL.
Methods
The population of interest for this scoping review are patients or their relatives with localized
LCL or related scars.
We searched the electronic databases PubMed, Web of Knowledge, PsycINFO, POPLINE,
Cochrane Library, Science Direct, Global Health, and LILACS, for articles written in Arabic, English,
French, Dutch, Portuguese, or Spanish, and published until the end of August 2017.
Results
From 2485 initial records, fifteen papers met our inclusion criteria. Dermatology life quality index
was the most frequent used scale to assess LCL psychological impact in quantitative studies. Six
qualitative studies used individual interviews and/or focus groups discussions to explore the
psychological and/or the social burden of this disease. Quantitative assessments using standard
scales as well as qualitative research asserts that LCL is a source of psychological suffering,
stigmatization, and decreased the quality of life (QoL).
Conclusion
Most studies showed that LCL has a significant negative effect on the QoL and mental health.
However, the fact that the psychosocial burden generated by LCL is time-dependent makes it
hard to measure. We recommend to develop a more specific and validated assessment scale to
appreciate the full burden of this disease and enhance comparability of findings.
Keywords:
Cutaneous leishmaniasis, Cicatrix, Psychology, Social Stigma, Quality of life
Review of LCL Psychosocial burden | 133
Background Cutaneous leishmaniasis (CL), a neglected tropical disease (NTD), is a parasitic infection of the
skin characterized by slowly healing ulcers that can leave indelible scars. There are various clinical
presentations of CL: localized, diffuse, disseminated and mucocutaneous CL.
The global mean age-standardized disability-adjusted life years (DALYs) lost by CL were
estimated at 0.58 per 100,000 people [1]. However, several authors have criticized the way the
global burden of disease tools, such as DALYs, have quantified the burden of CL. A recent
viewpoint drew attention to the fact that only active forms of CL are included in DALY
calculations. It suggests to consider also the psychological impact linked to the disfiguring scars
of CL [2]. Moreover, the same authors proposed to multiply by ten the actual burden of CL, to
take into account the effect of CL scars [2]. Under this scenario, the global number of people
living with LCL scars is estimated at 40 million. Such claims call for a higher prioritization and
resource allocation to CL [2].
Localized CL (LCL) is by far the most common presentation. Localized CL (LCL) is by far the most
common presentation. The localized form of CL is typically a single papular or nodular skin lesion
that progressively ulcerates and usually self-heals within a few months [3].
In 2013, LCL was primarily reported from fifteen countries. Namely, Afghanistan, Algeria, Brazil,
Colombia, Honduras, Iran, Morocco, Nicaragua, Pakistan, Peru, Saudi Arabia, Syrian Arab
Republic, Tunisia, Turkey and Yemen [4].
LCL is often presented in the literature as a dermatological disorder that is “associated with
stigma” and psychological suffering. That is quite obvious for the severely mutilating or
disseminated types of CL. Severe scar tissue from any cause (acne, burn, injury, Buruli ulcer,
lymphatic filariasis, podoconiosis, a.o.) reduces the quality of life in a direct way but also through
a process of social rejection and self-depreciation [5–13]. In some skin disorders, this
psychosocial effect is predominant, as in vitiligo patients, who experience a reduced quality of
life because of their social rejection [14–18]. The psychological distress generated by skin
ailments is complex and may depend on the severity and visibility of the lesions. Skin disorders
are no exception to the general rule that the degree of fear inspired by a disease is mainly
associated with the perception of severity and also lack of adequate treatment [19]. In the past,
the typical examples were smallpox and leprosy that led to a total isolation of those affected,
and more recently, Ebola, HIV/AIDS, psychiatric and mental illnesses continue to generate this
stigmatizing behavior in many communities. The resulting social isolation affects a human being
psychologically and this was shown in the case of the recent Ebola epidemic to have a negative
impact on survival [20, 21]. However, the experience in psoriasis shows that the relationship
between symptom severity and psychosocial distress reported by psoriasis patients is not
straightforward [22]. Nevertheless, a systematic review showed that clinical depression was 1.5
times more frequent in psoriasis patients than in non-affected peers [23].
134 | Chapter 5
In the literature on the psychosocial burden of disease, stigma is a central concept. Mostly stigma
manifests itself in discriminatory attitudes against those who are different and is related both to
the conception of the ‘other’ as well as the ‘me’[24]. This conceptual complexity makes stigma
difficult to determine. Goffman defines stigma as: ‘The phenomenon whereby an individual with
an attribute which is deeply discredited by his/her society is rejected as a result of the attribute.
Stigma is a process by which the reaction of others spoils normal identity’ [19, 25]. Other authors
define stigma as a social process that is characterized by exclusion, rejection, and blame resulting
from the anticipated perception or expression of an adverse social judgment about a person or
a group [26, 27]. This judgment can be related to the mental disorder, ethnicity or physical
handicap of the stigmatized persons [25]. Stigmatisation also affects people who are not
perceived as a threat to others but who present a disfigured body [28, 29]. The judgments made
are often the result of comparisons to a perfect, idealized body image [30]. Often shaped on the
pictures of ‘celebrities’ as the ideal social appearance, this idealized body image increases the
pressure on those who appear different, pushing some of them to seek cosmetic surgery [31].
Stigma is also typically attached to those conditions in which people are blamed for their
appearance [32]. The social rejection generates suffering, as the stigmatized person interiorizes
what others think of her/him, leading to loss of self-esteem and what is called “self-stigma“ [33].
Once the individual perceives the stigma, it can affect his/her quality of life [15]. The more
general concept of “stigma” has, therefore, two dimensions: how others relate to the stigmatized
person and how that person relates to him/herself. Henceforward in this text, we distinguish
these two dimensions based on the model presented previously by Deacon [34] and adapted by
Weiss in 2008 [27] :
1. Social stigma (public stigma) occurs when society actively adopts negative attitudes of
rejection or exclusion against the stigmatized who undergo inequitable or discriminatory
treatment. Enacted stigma, which is about passive discrimination, is one expression of social
stigma. Even if some people disagree with the stigmatizing behaviors of others, they often
remain passive about it, without trying to stop it.
2. Self-stigma is an internalized mechanism in the stigmatized person, who is anticipating the
social rejection or is adapting to a stigmatizing environment. In this category, we can include: felt
stigma, experienced stigma, internalized stigma, internal stigma, anticipated stigma, imagined
stigma, perceived stigma.
Then, whether the painless nodules, ulcers, and scars of LCL contribute to the global burden of
CL beyond the local discomfort they generate is an open question. So far, little research has been
done to underpin this general statement about LCL, nor to differentiate the burden according to
CL type.
Review of LCL Psychosocial burden | 135
Our review aimed to describe the current evidence related to the psychosocial burden of LCL.
More specifically, our objectives were to (i) explore which quantitative scales were used to assess
this burden; (ii) summarize qualitatively the extent of psychosocial suffering (specifically self-
stigma, social stigma, quality of life) attributable to LCL. Our research question was “Do persons
experiencing a LCL skin lesion suffer from any psychosocial burden?”
Methods
A scoping review is mainly based on a preliminary assessment of the amount/ the extent of
available research in the literature [35]. Following Arksey and O’Malley’s framework, we worked
through five stages, listed hereafter. Stage 1: identifying the research question; Stage 2:
identifying relevant studies; Stage 3: study selection; Stage 4: charting the data; Stage 5:
collating, summarizing and reporting the results [36, 37].
Inclusion and exclusion criteria
Inclusion criteria
Population: Persons (patients or their relatives) experiencing a skin condition linked to LCL
Range of Concepts: LCL-related stigma and its psychological consequences in different LCL skin
conditions, including LCL scars.
Context: All countries.
All articles discussing entirely or partially the stigma types, psychological and social
consequences and quality of life, psychological or psychosocial effects related to Leishmaniasis
skin condition. All types of publications were eligible: original articles, literature review, editorial,
comments, correspondence, abstracts of workshop or conferences, grey literature, as available
online.
Exclusion criteria
As listed in additional file 1, we excluded articles for which no full text was available; books;
articles targeting veterinary studies, vectors, laboratory or in-vitro research; studies describing
CL epidemiology, outbreaks or trends without or with a little indirect information about
psychosocial outcomes; articles exclusively targeting HIV or mental illness or other stigmatising
diseases without any link with CL; articles treating only the visceral form of leishmaniasis or post
dermal kala azar form or exclusively the CL mucosal or tegumentary form; articles on diagnostic
methods for CL; treatment assessment or methods not targeting psychosocial interventions in
CL (e.g. drug effectiveness).
136 | Chapter 5
Search strategy
Eight databases were selected: PubMed, Web of Knowledge, Science Direct, PsycINFO, POPLINE,
LILACS, Global Health CABI and Cochrane Library. We searched these databases from their
inception until the end of August 2017 with language restriction to Arabic, English, French, Dutch,
Portuguese, and Spanish.
The search in the PubMed and Web of Knowledge databases followed the three steps
recommended in Peters et al. [38]. (1) Firstly, we did a limited exploratory search in PubMed
combining three keywords: Cutaneous leishmaniasis AND (Stigma OR Quality of life). Then, we
built a logical grid after analyzing text words contained in the title and abstract with adding the
subject heading and index terms. (2) Secondly, we organized them into blocks by using the
advanced search composed of MeSH terms and free synonymous words categorized into three
blocks (1#Population, 2#Concept, 3#Context) which helped us to build the query question and
perform the primary search strategy (as listed below). For the other databases, shorter search
equations were set to find relevant references to our topic (See Additional file 1).
(3) Thirdly we performed a hand search on the reference list of the selected articles and searched
for any publication by the first, second, third and last authors in those selected articles and
meeting the same inclusion criteria but initially not detected by our initial search strategy. Also,
we looked for overall articles that cited the ones we selected. We repeated this process
iteratively until no other relevant articles were found.
Query search (PubMed) and (Web of Knowledge):
This search strategy was done end of September 2016 and updated on 1st September 2017.
(((Leishmaniasis OR Dermal Leishmaniasis OR Cutaneous Leishmaniasis OR Mucocutaneous
Leishmaniasis OR Diffuse Cutaneous Leishmaniasis NOT Visceral Leishmaniasis)) AND (Social
problems OR Public opinion OR Social discrimination OR Social isolation OR Social exclusion OR
Social distance OR Stereotyping OR Social perception OR Social conditions OR Social adjustment
OR Social behavior OR Social behaviour OR Social behavior disorders OR Social environment OR
Social support OR Social marketing OR Cost of illness OR Stigma* OR Public stigma OR Social
Stigma OR community stigma OR Enacted stigma OR Self-stigma OR Self stigma OR Experienced
stigma OR Perceived stigma OR imagined stigma OR Anticipated stigma OR Felt stigma OR Self-
report OR internalized stigma OR Health related stigma OR Gender Identity OR Quality of Life OR
Perception OR Rejection OR Discrimination OR Parasitic skin diseases/psychology OR Skin
diseases, bacterial/psychology OR Neglected Diseases/psychology OR Psychosocial OR Psycho-
social)) AND ((“1920/01/01”[PDat] : “2017/08/31”[PDat]) AND (Arabic[lang] OR English[lang] OR
French[lang] OR Dutch[lang] OR German[lang] OR Spanish[lang]))
Review of LCL Psychosocial burden | 137
Data collection, extraction, and analysis
Two investigators (IB, ZB) independently reviewed the titles and abstracts of all retrieved records
and selected the articles for full-text review based on eligibility criteria as defined below.
EndnoteX7 (Thomson Reuters 2014) was used as a reference manager software. This software
served to avoid duplication, achieve the first screening of titles or titles and abstracts, download
and manage full texts of selected references for a complete reading step and provide a digital
backup for archiving and enhancing traceability of the search process for this review. In case of
disagreement, the last author (MB) served as the tiebreaker. The other authors, all experts in the
field of CL, stigma and conducting systematic reviews, rechecked the inclusion and exclusion
criteria of selected articles.
The results of the literature search are presented in a flow diagram (Figure 1) describing the
scoping review process [38]. The additional file 1 includes more details on the search: activities
performed with date, the query equation employed, and the reference list found, including
justification for excluding references after full-text reading and the final references of the
included articles.
We extracted the data and mapped them in an Excel sheet (Windows, Microsoft Corporation).
We used a narrative synthesis approach to compile the data and examples from individual
studies. We focused on how studies addressing a different aspect of the same phenomenon can
be narratively summarized to provide a bigger picture of that phenomenon. Using Nvivo11 QRS
International, we classified them under main conceptual categories (Additional file 1).
We followed the fifth steps of reporting scoping reviews with the use of PRISMA flowchart for
reporting the whole search strategy [36, 37, 39].
138 | Chapter 5
Fig 1. Flowchart of the number of literature searched and selected for the psychosocial
burden of Cutaneous Leishmaniasis
Results
Included papers
We included 15 articles matching our criteria for a full review (Table 1) [40–54]. The studies were
done in nine countries: Afghanistan, Iran, Morocco, Sri Lanka, Surinam, Syria, Tunisia, and
Yemen. Nine papers used quantitative research methods, including eight cross-sectional
descriptive surveys and one randomized controlled trial of a psychotherapy intervention in LCL.
One was based on mixed methods while five were based on qualitative research: one of them
was based on focus group discussions, one was a review, and the others were based on
interviews.
Review of LCL Psychosocial burden | 139
Psychosocial burden of LCL measured quantitatively
Anxiety and depression: Seven quantitative studies measured the psychosocial outcome on a
standard scale (Table 2). Yanik et al. [41] assessed the psychological impact of LCL in three groups
of patients in Turkey (LCL-active lesions, LCL-scars, and a control group). They used three
different scales to quantify 1. Anxiety and depression (HAD), 2. Body Image Satisfaction (BIS),
and 3. Dermatology Life Quality Index (DLQI). They concluded that anxiety and depression were
frequent symptoms in patients with LCL at both the active lesion and scar stage and affected
their quality of life. Patients with LCL scars had better quality of life scores than those with active
lesions. Simsek et al. [43] in Turkey used the DSM classification scale of mental illness (DSM-IV)
to study predictors of mental disorders in a sample of women from a rural South-eastern region
in Turkey. In multivariate analysis, LCL was found to be an independent predictor of mental
illness (Odds Ratio (OR) 2.15, 95% C.I. 1.25 to 7.31) at the same level as domestic violence (OR
2.03, 95% C.I. 1.17 to 4.28). In 2015, Turan et al. [50] in the same endemic area in Sanliurfa, used
four scales in children and adolescents from 7 to 18 years and their parents. In the patients with
LCL, depression scores were significantly higher than in the control group, and this was also the
case in the group of mothers of children with LCL. No difference was found in anxiety scores.
Low quality of life: Two studies were conducted in Iran [45, 48] using the DLQI scale to assess
the QoL in LCL patients under treatment. Vares et al. [48] found that the type of LCL lesion had
a significant effect on patient's QoL. The DLQI score in patients with papular LCL lesions was
better than in those with nodular and plaque lesions. Those with ulcerated lesions had the lowest
QoL score. Nilforoushzadeh et al. [45] randomly allocated 40 women with LCL active lesions to
either the standard LCL treatment or standard treatment plus psychotherapy. The intervention
arm showed a more pronounced improvement in DLQI score at the end of the study after eight
weeks (p=0.001). Hanjdani et al. [49] used the Family DLQI scale to assess the impact of chronic
skin disorders in a family member and on the other –non-affected- household members. A
variety of chronic skin disorders of at least one-month duration (vitiligo, pemphigus, psoriasis,
and LCL) were included. There was a reduction of QoL, without a significant difference between
disorders, but the sample size was small. The main problems mentioned were emotional distress,
spending much time with the patient, and reactions of the others to the patient`s condition. The
main complaint in families with a LCL case was the time spent looking after the patient.
Stigma: In Tunisia, Chahed et al. [52] assessed the level of stigma (using the Psoriasis Life Stress
Inventory and QoL (Revised Illness Perception Questionnaire and the World Health Organization
QoL26) in a sample of 41 women with LCL scars and reported a wide range of psychological
effects. 73% of the women had suffered social exclusion and stigmatization. They reported
broken relationships, interpersonal conflicts, reduced employment opportunities, and reduced
marriage prospects for men and women. LCL was a constant source of stress for the study
participants. They thought their scars were degrading, and a source of shame. The “experience
of social rejection” and the “anticipation and avoidance of stress” were significantly and
negatively correlated with age. The younger the person, the more impact CL had in terms of
140 | Chapter 5
stigma. QoL was correlated with the “anticipation of stress” score but negatively correlated with
knowledge about CL. The more a person knew about LCL, the less likely they were to view their
quality of social life negatively.
Fear of scars: The two other quantitative studies included in this review [46, 47] were both based
on a general questionnaire targeting knowledge, attitudes, and practices of LCL patients in
endemic areas from Syria and Sri Lanka. In both studies, no direct information about QoL was
provided except the adverse effect of fear about LCL scars, especially on the face.
Psychosocial burden of LCL reported qualitatively
Very recently five qualitative studies provided more information on the CL psychosocial burden
from the perspective of the general population and affected patients living in LCL endemic areas
(Table 3).
Expectation of stigmatization: The most important effects were linked to LCL patients holding
scars on visible parts of their body, specifically on women faces’ more than men. Chahed et al.
[52] reported feelings of inferiority and the idea that the disease is equal to an apparent social
disadvantage. Fifty percent of all women with scars said scars alter their beauty.
Perception of changed body image: The beauty loss concept has been a frequent feature of all
these studies, especially for young bachelors. The impact of unwanted changes in body image is
considered as a curse or bad luck that will diminish the marriage opportunities of the person
suffering from LCL scar.
Self-stigma: A broad spectrum of psychosocial suffering was reported such as being shy,
ashamed, stressed, anxious, depressed. Feeling embarrassment, sadness, suicidal thoughts and
a decrease of self-concept (self-confidence, self-esteem, self-contempt, self-awareness) lead
patients to perceive or interpret negatively some direct or indirect reactions from partners,
relatives, and the general population.
Some women affected by LCL try to hide their lesions from their partner and look for more
permanent solutions by surgical repair or aesthetic surgery. As Chahed et al. [52] have pointed
out, the extent of the stigma that patients experience is associated with their anticipation of
rejection.
Social stigma: From emotional isolation and emotional distress to firm social rejection and
discrimination within the same household, with friends or/and workmates, or abroad family
visitors. Some affected people felt their chances to find employment, studies or marriage
jeopardized. However, simultaneously, the perceived stigma which was expressed or enacted by
the neighborhood led to psychological consequences as well. In Afghanistan [40], women with
LCL frequently felt rejected. As LCL was relatively new in Kabul, there was a widespread
misconception about its origin, with fear of contagion and an association of LCL with dirt and low
personal hygiene. People attributed LCL to “the fault and sin carried by strangers living in
neighboring provinces or cities.” Such misconceptions raise the level of rejection and social
exclusion.
Review of LCL Psychosocial burden | 141
Mitigating factors of stigma (Resistance to stigma): The tendency to isolate LCL patients from
others contributes to more self-stigma. The patients try to hide or mask the lesion, by using
homemade or commercial makeup, or by wearing the traditional veil. The qualitative studies also
reported that LCL being for some people only a minor source of suffering, for the following
reasons. Firstly, people living in rural areas consider it quite normal to have scars because of the
forestry and agriculture activities which expose them to several abrasions and wounds. Thus, an
ulcer that self-heals over time is not a major problem for them. Such scars are sometimes even
considered as a mark of belonging and membership to a community, even as a mark of glory and
pride. Secondly, religious people tend to accept this kind of ailments, as a submission to the will
of the Almighty. Finally, old people have less fear about aesthetic outcomes than younger
people.
Discussion The main finding of our review is that LCL indeed generates psychological suffering and mental
ill-health, as shown in several countries. LCL leads to the social stigma that eventually causes
self-stigmatization, which amplifies the feelings of fear, anxiety, and depression in those
affected. Extreme self-isolation and self-contempt can sometimes even lead to suicidal ideation.
Moreover, young single women with facial scars face the most substantial psychosocial impact
of LCL [40, 52, 54, 55]. Of course, there is a contrast with the ill-health generated by the more
severe diffuse, disseminated and mutilating mucocutaneous CL forms, which can even be life-
threatening. Getnet's work in Ethiopia [56] and in Latin America [57–61] showed the
psychosocial burden of these non-localized CL types for which the prognosis is much more severe
than that of LCL.
Our review adds some new insights to the stigma theory presented previously for HIV by Deacon
& al [34] and adapted for neglected tropical diseases by Weiss in 2008 [27]. We elaborated
further on this model by including the reflection about body image and its distortions presented
by Thompson & al [62]. We also introduced “change over time” as an important determinant of
the perception of the severity and the psychosocial impact of any acquired skin disorder. Time
adjustments influence the degree of self-stigma on the one hand, and on the other hand, also
influence the attitudes (negative or positive) society has towards the patient (Figure 2).
Like for burn injuries, the evidence shows an adjustment over time independently of the injury
size [63]. Contrastingly, older people will tend to heavily personalize negative social and self-
images within age identity and global wellbeing. Then, change of self-perceptions that could
happen within age is a matter of debate. For some people self-concept could be stable but also
could change in positive and negative ways [64], [65]; depending on the unforgettable memories
[66] and how emotions and memory interact and how these emotions change across lifespan
[67, 68].
142 | Chapter 5
Fig. 2 Time adjustment of stigma types and psychosocial impact of unwanted skin conditions adapted from Deacon & al [34]; Weiss [27]; and
Thompson & al [62] by taking the example of localized cutaneous leishmaniasis (LCL)
Review of LCL Psychosocial burden | 143
This scoping review can only be as strong as the studies it included, and in our case, there were
some limitations. A small sample size characterized most of the included studies, and not all had
appropriate control groups. E.g., the Kassi et al. [44] record is a case report presented at a
symposium, telling the case of one woman with CL. The reports are not all of the same quality
and are sometimes lacking detail. Reithinger et al. [42] is a short communication, describing
summary results of a study that has not yet been fully published in an indexed journal. The
majority of our records had descriptive cross-sectional quantitative survey designs with one
single participant contact. Not all studies distinguished the LCL lesion from the LCL scar, though
there is evidence that the effect is not the same, and that even within LCL it depends on lesion
type.
Future studies should pay more attention to potential confounding factors such as the physical
aspect of the lesion or scar, the socio-economic position of the person with LCL and context
related factors determining the CL-related knowledge, attitudes, and practices of society [69].
Indeed, lack of knowledge about this disease and its transmission patterns can lead to collective
fears, which could fuel stigmatization, rejection, and isolation such as observed in Kabul,
Afghanistan. A mixed methods approach is strongly advised, as so far in many endemic areas
only quantitative patient surveys were done, leaving a lot of unanswered questions about the
community perception. To enhance our understanding, we recommend the development of a
standard validated stigma scale for CL. Furthermore, prospective follow-up studies will more
accurately describe the time-dependent changes in perception. Future qualitative research
should examine stigma and quality of life components from the perspective of the patient and
the healthcare provider and give orientations for interventions.
Our review contains some limitations. Firstly, we acknowledge that we may have missed some
relevant studies because of language restrictions that excluded large parts of the world where
CL is common as well (especially articles published in Chinese and Russian). Secondly, as a
common limitation of scoping reviews, we did not grade the quality of evidence, to avoid loss of
information, but we may have included weak evidence in this way.
Conclusion
The literature on CL in the past 20 years claims that CL lesions like it is the case in any other
neglected infectious diseases related to poverty, influences the psychological state of those
affected and can lead to a reduction in their quality of life and stigma [27, 70–75]. However,
previous literature reviews assessing the burden of disease caused by leishmaniasis usually did
not distinguish between the localized CL self-healing form and the other non-localised forms of
CL (mucocutaneous, diffuse). Our review showed that most qualitative studies concur that LCL
has indeed a negative effect on quality of life and mental health, through a process of social and
self-stigmatization.
144 | Chapter 5
List of abbreviations BIS: Body Image Satisfaction scale; CL: Cutaneous Leishmaniasis; DALYs: Disability-Adjusted Life
Years; DLQI: Dermatology Life Quality Index; DSM-IV: Diagnostic and Statistical Manual of Mental
Disorders, 4th. Edition; HAD: Hospital Anxiety and Depression scale; LCL: a localized form of
cutaneous leishmaniasis; MeSH: Medical Subject Headings; NTD: Neglected Tropical Disease;
PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses; QoL: Quality of
Life.
Declarations
Ethics approval and consent to participate
We followed the relevant standards while conducting this review.
Consent to publish
Not applicable.
Availability of data and materials
The data sets supporting the conclusions of this article are included in the article and its
additional file.
Competing interests
The authors declare that they have no competing interests.
Funding
No specific funding was received for this work.
Authors' contributions
IB, VB, and MB developed the idea for the paper. IB and HS conducted searches. IB and ZB
assessed citations. IB, ZB, and MB assessed the included records. All authors rechecked the
inclusion and exclusion criteria of the selected records. IB, VB, and MB wrote the first draft of
the manuscript. All authors commented on the manuscript. All authors read and approved the
final manuscript.
Acknowledgments
IB and ZB are supported by doctoral grants from the Belgian Directorate General for
Development Cooperation and Humanitarian Aid. The funder had no role in the study design,
data collection, and analysis, decision to publish, or preparation of the paper.
Authors' Information
1-National School of Public Health - Ministry of Health, Rabat, Morocco. 2-Department of Public
Health - Institute of Tropical Medicine, Antwerp, Belgium. 3- Department of Biomedical Sciences
- Faculty of Pharmaceutical, Biomedical and Veterinary Sciences- University of Antwerp, Belgium.
4-Vrije Universiteit Brussel 5- Department of Pathology and Veterinary Public Health, Hassan II
Agronomy and Veterinary Institute, Rabat, Morocco.
Review of LCL Psychosocial burden | 145
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Additional file 1 Logbook, search history, excluded articles, included articles and Data
extraction labels of the main conceptual categories
152 | Chapter 5
Table 1 Studies included in this review by study design, study population characteristics and sample size
Authors Year of
publica
tion
Country of
the study
Methods Study design Timing Study Population Sample size Sex ratio
(M/F)
Age
range
(years)
Patients
with CL
scars
included
Al-Kamel et al. 2017 Yemen Qualitative Interview May 2016 CL patients 11 0.10 12-60 Yes
Bennis et al. 2017 Morocco Qualitative Questionnaire April 2015 Boarding school
students
448 1.36 16-20 Yes
Chahed et al. 2016 Tunisia Quantitative Questionnaire
survey (scale)
Not defined Women with CL
scar
41 All female 12-53 Yes
Ramdas et al. 2016 Surinam Qualitative Ethnography Sep 09 to
Dec 10
CL patients.
General
population
205 CL
patient &
321 people
8.3 & 1.4 20-49 Yes
Turan et al. 2015 Turkey Quantitative Questionnaire
survey (scale)
May 11 to
Apr 13
Paediatric CL
patients and
healthy controls
54 CL
patients
1.16 7-18 No
Handjani et al. 2013 Iran Quantitative Questionnaire
survey (scale)
2013 Relatives of
dermatological
cases
50 relatives 0.85 20-65 No
Vares et al. 2013 Iran Quantitative Questionnaire
survey (scale)
Not defined CL patients 124 0.59 16-80 Yes
Abazid et al. 2010 Syria Quantitative KAP-survey Nov 06 to
Oct 07
CL patients or the
caregiver seeking
treat
70 0.46 ≈32 No
Fernando et al. 2010 Sri Lanka Quantitative KAP-survey Sep 06 to
Feb 08
CL patients 120 2.75 02-70 No
Nilforoushzadeh
et al.
2010 Iran Quantitative RCT 2007 Female CL
patients
2 groups of
20
All female > 10 No
Kassi et al. 2008 Afghanistan Qualitative Case report Not defined Woman with CL
scar
1 All female 28 Yes
Review of LCL Psychosocial burden | 153
Authors Year of
publica
tion
Country of
the study
Methods Study design Timing Study Population Sample size Sex ratio
(M/F)
Age
range
(years)
Patients
with CL
scars
included
Simsek et al. 2008 Turkey Quantitative Questionnaire
survey (scale)
2006 Women in general
population
247 All female 15-47 Yes
Reithinger et al. 2005 Afghanistan Mixed KAP & FGD Oct 2002 KAP: household
head; FGD:
women
KAP: 252;
FGD: 108
FGD All
female
Not
defined
Yes
Yanik et al. 2004 Turkey Quantitative Questionnaire
survey (scale)
Sep 02 to
Aug 03
CL patients,
persons with CL
scar, healthy
controls
3 groups of
33
1:1 12-35 Yes
Reyburn et al. 2000 Afghanistan Qualitative FGD Feb to Jul
1998
CL patients and
unaffected
spouses
8 groups of
6 to 10
1:1 ≈28 Yes
154 | Chapter 5
Table 2 Overview of the quantitative studies included in this review based on scales questionnaire surveys
Reference Measurement scales of psychological, social and
QoL burdens Main findings
Chahed-2016
Revised Illness Perception Questionnaire (IPQ-R),
World Health Organization Quality of Life-26
(WHOQOL-26)
Large range of negative psychological consequences of LCL it is a
source of constant stress and shame. Leading to social rejection
and anticipation/ avoidance behavior.
Turan-2015
The Child Depression Inventory (CDI)
The State-Trait Anxiety Inventories for Children
(STAIC),
The Paediatric Quality of Life Inventory Parent
and
Child Versions (PedQL-P and C)
Depression scores were significantly higher in children and
adolescents with CL compared to age-matched controls. No
significant difference was found in anxiety scores. Depression
scores were also higher in mother of children with LCL.
Handjani-2013 Family Dermatology Life Quality Index (FDLQI) Family members of LCL cases face a reduction in QoL, mainly due to
the time they have to spend looking after the patient
Vares-2013 Dermatology Life Quality Index (DLQI) The type of LCL lesion determines the degree of QoL reduction.
Most reduced in ulcers, least in papular LCL
Nilforoushzadeh-
2010 Dermatology Life Quality Index (DLQI)
The effect of adjunct psychotherapy to drug treatment on QoL was
tested in a randomized controlled trial on women with LCL. QoL
was improved in the intervention group.
Simsek-2008 The Turkish version of the Structured Clinical
Interview for Axes I of the DSM-IV (SCID-I)
This study on mental health of women in rural Turkey identified CL
as one of the main independent predictors of mental disorders
Yanik-2004
Hospital Anxiety Depression Scale (HAD),
Body Image Satisfaction Scale (BIS),
Dermatology Quality of Life Scale (DQL)
Depression and anxiety are higher in LCL compared to control.
Impaired body satisfaction in LCL. LCL have reduced QoL compared
to LCL scars and controls.
Review of LCL Psychosocial burden | 155
Table 3 Overview of the included studies analyzed qualitatively 1st Author
name, Year
of
publication
and country
of the study.
Types of stigma
noticed
Types of psychological
consequences related
to CL
Reasons for stigma Reasons for the Psychosocial burden
Al-Kamel-
2017
(Yemen)
Social stigma
Aesthetic
stigma
Psychological
stigma
Stress
Depression
Anxiousness Shame
Socially denied Feels shame. Fears of infecting their children and
infecting others through food and drink. Fears of
deformity, disability, and death. Fear of malignancy.
Bennis-2017
(Morocco)
Self-stigma
Social stigma
A large spectrum of
negative psychosocial
effects: Anxiety,
Embarrassment,
Sadness, Shame,
Suicidal ideas
Social stigma (Family relationships, social contempt,
fear, marriage difficulties, avoidance by others). Self-
stigma (embarrassment, shame, sadness, anxiety,
depression, suicidal ideas)
The emergence of psychological consequences due to
perceived stigma.
Chahed-2016
(Tunisia)
Social exclusion
and
stigmatization
Loss of self-esteem,
feelings of inferiority
and the idea that the
disease is equal to an
obvious social
disadvantage. There
was also a strong sense
of shame.
The nature of stigma that patients experience is
associated with certain general fears and anticipation
of rejection, rather than the possible rejection that
patient truly experiences from society. It reduced
marriage prospects for men (75%) and women (59%).
ZCL has had no positive effects on their lives. The
consequences have rather been negative. About 73%
suffered social exclusion and stigmatization. Their
relationships have been broken and they face more
interpersonal conflicts in society, regardless of the
context (family, social or professional). The
consequences were seen also in their chances of
getting employment
Respondents are dissatisfied with their self-image and
appearance. Scars alter women’s beauty (58%)
Drugs were seen to have little or no effect, and the
risk of getting the disease again is likely. The more a
person looks at the world anticipating segregation
and rejection, the more they perceive ZCL as a disease
with harmful effects on them-The more they see it as
a mysterious and incomprehensible illness, and the
more they talk about suffering and emotional
difficulties.
156 | Chapter 5
Ramdas-
2016
(Surinam)
Aesthetic
stigma
In the
literature: 1)
experienced or
enacted stigma;
2) anticipated,
felt, or
perceived
stigma; and 3)
internalized or
self-stigma
38 CL patients who
reported having
experienced negative
reactions related to CL
expressed feeling bad
about their looks. Some
said they were
“disgusted” by their
sores, others reported
feeling “shy” or
“ashamed”.
Health-related stigma is linked to patients’ own illness
experiences’
These feelings were experienced when sores became
bigger, or when they had multiple sores. The
gruesome appearance of CL sores contributed to
patients' fear of the disease. Aside from a sore's
appearance, the growth of a sore, the increase in a
number of sores, and their visibility could also cause
overt negative reactions from those in a patient's
environment.
Reyburn-
2000
(Afghanistan)
Enacted stigma
Feeling
rejection and
isolation
Some women
expressed anger at the
situation
Felling bring shame to
the whole family. One
girl said that she
sometimes felt suicidal.
Women tended to express feelings of rejection and
isolation more frequently than men. Widespread and
inappropriate fear of direct or indirect transmission of
CL to others. Fear of contagion and an association
with dirt, low personal hygiene, sinfulness, and
disgust. If you commit a sin or you have done
something wrong, you will get the punishment from
God later on. An insulting word, “soldana” was
commonly reported to be used against CL sufferers,
leading to a general feeling of victimization. Some
respondents were required to eat separately from the
family with his/her own plate, cup, utensils and not to
share a bed with healthy family members. Women
with CL often reported that they were not allowed to
cook for the family. Had lost authority or felt
disempowered from interacting in public or managing
their affairs It seemed that the perceived need to
isolate CL sufferers from others readily developed
into a more personal rejection.
One of the major concerns for young people,
especially women, was their appearance and
adherence to an ideal of beauty. CL was felt to
seriously undermine their prospects for marriage.
Both active lesions and scars were a concern,
particularly on the face. Several men reported that
leishmaniasis caused problems in taking their
ablutions and staying ritually clean throughout the
prayer. They felt that others saw them as unclean and
they were deterred from praying at the mosque.
CL RDT in Morocco |157
CHAPTER 6. Accuracy of a rapid
diagnostic test based on antigen
detection for the diagnosis of cutaneous
leishmaniasis in patients with suggestive
skin lesions in Morocco.
Bennis I, Verdonck K, El Khalfaoui N, Riyad M, Fellah H, Van der Auwera G, Sahibi H,
Bouhout S, Dujardin JC, Boelaert M (2018). Accuracy of a rapid diagnostic test based
on antigen detection for the diagnosis of cutaneous leishmaniasis in patients with
suggestive skin lesions in Morocco. The American journal of tropical medicine and
hygiene
CL RDT in Morocco |159
Accuracy of a rapid diagnostic test based on antigen detection for the diagnosis
of cutaneous leishmaniasis in patients with suggestive skin lesions in Morocco
Issam Bennis1,2,3*, Kristien Verdonck2, Nora el Khalfaoui4, Myriam Riyad4, Hajiba Fellah5, Jean-
Claude Dujardin3,6, Hamid Sahibi7, Souad Bouhout8, Gert Van der Auwera6, Marleen Boelaert2
1 National School of Public Health, Ministry of Health, Rabat, Morocco. 2 Department of Public Health, Institute of Tropical Medicine, Antwerp, Belgium. 3 Department of Biomedical Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary
Sciences, University of Antwerp, Belgium. 4 Laboratory of Parasitology & Research team on Immunopathology of Infectious and Systemic
Diseases, Faculty of Medicine and Pharmacy, University Hassan II of Casablanca, Morocco. 5 National Reference Laboratory of Leishmaniasis, Parasitology Department, National Institute of
Hygiene, Rabat, Morocco. 6 Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium. 7 Department of Parasitology, Hassan II Agronomy, and Veterinary Institute, Rabat, Morocco. 8 Unit of Parasitic Diseases, Directorate of Epidemiology and Disease Control, Ministry of Health,
Rabat, Morocco.
(*) Address correspondence to Issam Bennis, Ecole Nationale de Santé Publique - Rue Lemfedel
Cherkaoui - Madinate Al Irfane - 10000 Rabat Maroc. GSM: 00212661259901 - Email:
Key words: Sensitivity and specificity; diagnostic accuracy; rapid diagnostic test for antigen
detection; cutaneous leishmaniasis; Morocco
160 | Chapter 6
Abstract In rural areas in Morocco, diagnosing cutaneous leishmaniasis (CL) can be challenging. We
evaluated the accuracy of a rapid diagnostic test based on antigen detection (RDT), the CL Detect
Rapid TestTM (Inbios International, Seattle, USA), in this setting.
We consecutively recruited patients with new skin ulcers in nine primary health centers. We took
a dental broach sample for the RDT and two other tissue samples by scraping border and center
of the lesion with a scalpel and smearing it on a slide. We duplicated each smear by pressing a
clean slide against it and processed the slides by microscopy, PCR ITS1, and kDNA minicircle PCR.
In a subgroup with positive PCR, the Leishmania species was identified using PCR-RFLP and PCR-
sequencing of hsp70 genes. A participant with positive microscopy and/or PCR was considered a
confirmed CL case. We computed sensitivity and specificity of the RDT compared to this
reference standard [ClinicalTrials.gov registration: NCT02979002].
Between December 2016 and July 2017, we included 219 patients, 50% of them were under 18
years old. RDT sensitivity was 68% [95% confidence interval (CI), 61-74], specificity 94% [95% CI,
91-97], positive predictive value 95% [95% CI, 92-98] and negative predictive value 64% [95% CI,
58-70].
Despite its low sensitivity, this novel RDT is a useful addition to clinical management of CL in
Morocco, especially in isolated localities. RDT-positive lesions can be treated as CL; but when
RDT-negative, microscopy should be done in a second step. The sensitivity of the RDT can
probably be optimized by improving the sampling procedure.
CL RDT in Morocco |161
Introduction Cutaneous leishmaniasis (CL) is a vector-borne disease which usually leads to slowly self-healing
skin lesions and residual scars on those parts of the body exposed to sandfly bites [1]. In 2016,
Morocco reported 4951 CL cases. In the southeast of the country, CL is mainly due to Leishmania
major, and in the central and northern regions to L. tropica. Some sporadic cases of CL due to L.
infantum have also been described [2, 3]. CL scars on the face can cause considerable
psychosocial suffering. In young women in North Africa and the Middle East, social rejection,
diminished marriage and employment prospects, and suicidal thoughts have been
documented.[4, 5] Women typically use traditional remedies and several cosmetics to mask the
scar tissue or seek plastic surgery [4, 6].
Early diagnosis and prompt and adequate treatment may improve the healing process and
prevent the development of stigmatizing lesions and scars [7]. However, current diagnostic
methods for CL are far from optimal and there is no single gold standard diagnostic technique.
In resource-limited settings, the most used diagnostic test for CL is direct microscopy, i.e.
searching for amastigote forms of the Leishmania parasite in Giemsa-stained skin smears or
biopsies [7]. However, the sensitivity of this test is moderate, between 53% and 76% [8–11]
depending on the disease duration, sampling technique, and skills of the microscopist [12]. In
patients with suggestive lesions and negative microscopy results, the polymerase chain reaction
(PCR) can help to confirm or rule out the diagnosis of leishmaniasis [13]. In Morocco, a PCR based
on the internal transcribed spacer (ITS1) primer showed a sensitivity between 84% and 100%
[14, 15]. Furthermore, Restriction Fragment Length Polymorphism (PCR-RFLP) analysis of the
amplification product allows species identification of the Leishmania parasites [16–18].
Conditions for these diagnostic methods are not always available/optimal in the remote areas
where the disease is endemic [7]. In rural areas in Morocco, patients often have to travel up to
two days to a center where the CL diagnosis is possible, and sometimes the laboratory request
and the sample have to be sent to the national reference laboratory [19]. Therefore, the
diagnosis of CL in the L. major-endemic areas in the southeast is, in practice, often based on the
clinical features of the lesion, whereas in L. tropica and L. infantum-endemic areas in the
northern, central, and mountainous regions, the diagnosis is more often based on a direct
microscopic exam. An accurate and user-friendly rapid diagnostic test for antigen detection
(RDT) would be welcome in these settings.
In general, RDTs are quick and easy to perform, with the ability to give results at the point of
care, meaning that results are available during the first patient visit. RDTs can be used in settings
with limited laboratory infrastructure and staff [20]. Several years after the successful
development of an RDT for visceral leishmaniasis,[21–23] an RDT for CL has been developed. The
CL Detect Rapid TestTM (Inbios International, Seattle, USA) is an antigen detection assay that
detects a membrane-based amastigote antigen (peroxidoxin). The test is recommended for ten
Leishmania species (L. tropica, L. amazonensis, L. donovani, L. infantum, L. mexicana, L.
guyanensis, L. major, L. braziliensis, L. panamensis, L. peruviana), and is to be used on a sample
162 | Chapter 6
taken with a dental broach from a skin ulcer not older than four months. Based on a study in
Tunisia (unpublished), the manufacturer claims a 100% sensitivity for CL due to L. major
compared to microscopy. The present study aimed to estimate the diagnostic accuracy of the CL
DetectTM Rapid Test compared to a composite reference standard test (direct examination of skin
smears by microscopy and/or PCR), in patients with skin ulcers attending primary health centers
in CL-endemic areas in Morocco.
Materials and methods
Study design
This was an observational, prospective, phase III diagnostic accuracy study.
Participants
Study participants were recruited in nine primary health centers located in five CL-endemic
provinces where previous studies had established the dominant species, namely, Ouarzazate
(L. major),[24] Tinghir (L. tropica), Errachidia (L. major),[25] Sefrou (L. tropica and L. infantum)
[26] and Sidi Kacem (L. tropica and L. infantum) [27].
Between December 2016 and July 2017, nurses and physicians working in these primary health
centers consecutively enrolled patients with ulcerative skin lesions. To be included, patients had
to have at least one ulcerative skin lesion suggestive of CL. This lesion had to be of recent onset,
defined as a duration reported by the patient of fewer than four months. In case there were
multiple lesions, the most recent and none superinfected was selected for this study.
Patients were excluded if they had already received antimony treatment or any other physical
(e.g. cryotherapy, thermotherapy, laser) or traditional (e.g. burn, acid, traditional scraping)
treatment for their skin lesion during the last two months. Patients with apparent other diseases
or patients requiring hospitalization or any other anti-parasitic treatment were also excluded, as
were those with ulcerative lesions of suspected bacterial origin which healed completely after a
short course of antibiotic treatment.
Study procedures
After verification of the eligibility criteria and after obtaining informed consent,
sociodemographic and clinical information was collected from each patient. Next, a picture was
taken of the selected lesion. A health professional then took a small sample of the ulcer using a
dental broach, after cleaning the skin with sterile 0.9% saline solution and discarding the crust
or superficial skin with a small sterile scalpel. This first tissue sample was used for the RDT. Then,
two additional skin smear samples (Mic 1 and Mic 2) were taken from the same lesion, from the
center and the border of the ulcer as recommended by Suárez et al [28]. Each smear was put on
a slide and duplicated by pressing a clean slide against it. The four resulting smears were used
for microscopy and PCR analyses. The slides were put in a clean and dust-free area for one to
CL RDT in Morocco |163
four hours, far from direct sunlight exposure, to make sure that they dried well at room
temperature. Two slides (Mic 1 and Mic 2) were transferred to the nearest provincial laboratory
for microscopy reading. The two remaining slides, resulting from the duplication, were sent to
laboratories in Casablanca and Antwerp (Belgium) for PCR testing (as shown in supporting
material 1).
Index test
The CL Detect Rapid Test™, in package CL025 with lot identifier UA1259 and manufacturer
specifications available online (http://www.inbios.com/wp-content/uploads/2016/06/900159-
00-IVD-CL-Detect-Rapid-Test-Package-Insert.pdf) was done on the sample collected by the
dental broach. The health professional recorded the RDT results on a separate sheet, as well as
the time to perform the entire procedure from starting the RDT until reading the result, and the
prevailing room temperature. We followed manufacturer’s instructions regarding reading and
interpretation of results. The RDT was considered positive if both control and test bands were
visible and became red, and negative if only the control band was visible (Figure 1).
Figure 1. Interpretation of CL Detect Rapid TestTM
164 | Chapter 6
Reference standard tests
Microscopy
In the provincial laboratory, two slides per participant were fixed by dipping them in methanol
for 2 to 3 minutes and staining them with Giemsa 10%, before examination under a light
microscope (x1000 magnification). Both slides were examined by the same microscopist, who
reported the number of fields, and the total number of macrophages and Leishmania amastigote
forms found. Then, the best slide of the two (Mic1 or Mic2, depending on the ease to visualize
macrophages if negative and to identify the number of Leishmania amastigote forms if positive)
was sent to the National Institute of Hygiene (NIH) to be verified by a laboratory engineer, who
had no knowledge of the patients or any previous test results. At the NIH, all slides were assessed
for their quality (and scored as bad, average, excellent) according to the standard operating
procedures (SOP). If the provincial laboratory reported a positive and the NIH a negative result,
the other slide was also sent to the NIH. In this case, we took the conclusion from the reader at
the NIH based on the two slides as the final microscopy result.
ITS1-PCR
DNA extraction from the third slide smear was carried out manually according to the phenol-
chloroform method [14, 18]. As a quality control measure, a NanoVue Plus spectrophotometer
(Biochrom US, Massachusetts, USA) was used to measure the DNA concentration in 100 samples.
As described previously,[14, 18] the internal transcribed spacer 1 of the ribosomal DNA repeat
unit (ITS1) was amplified in a Biometra GmbH (Whatman Biometra, UK) thermocycler using
primers L5.8S: 5′-TGATACCACTTATCGCACTT-3′ and LITSR: 5′-CTGGATCATTTTCCGATG-3′
(Biolegio, Nijmegen Netherlands). Amplification was carried out in 25 μl. Cycling conditions were
as follows: denaturation at 94°C for 4 minutes, next at 94°C for 40 seconds, 53°C for 30 seconds,
72°C for 1 minute, 72°C for 10 minutes (40 cycles). The obtained amplification products were
revealed by electrophoresis on a 2% agarose gel stained with ethidium bromide and visualized
under ultraviolet (UV) light. The ITS1-PCR was considered positive for the Leishmania genus if a
band of the expected size (~300-350 base pairs) was obtained.
For species identification, positive samples were subjected to restriction fragment length
polymorphism (RFLP) analysis using the restriction endonuclease HaeIII (BioLabs, USA) [14, 18].
Reference strains of L. infantum (MHOM/ES/90/LEM2205), L. tropica (MHOM/MA/2010/L02)
and L. major (MHOM/IL/81/Friedlin) were included.
kDNA-PCR
Two slides per lesion were used for molecular testing. One of the two slides was systematically
analyzed by ITS1-PCR in Casablanca and the second slides were divided into two groups to be
analyzed by ITS1-PCR in Casablanca or by kDNA-PCR in Antwerp as explained in supporting
material 1. The kDNA-PCR was used as an additional method to detect Leishmania DNA in the
samples. Because this PCR amplifies the parasite’s kinetoplast DNA minicircles, of which 10000
CL RDT in Morocco |165
to 20000 copies are found in each cell, it is more sensitive than ITS1-PCR. DNA was extracted
using either the phenol-chloroform method described above or (for most samples) using the
QiaAmp DNA Mini Kit (Qiagen, www.qiagen.com). Lysis was achieved by 3 hours incubation at
56°C in Tissue Lysis Buffer, and the DNA was eluted in 50 µl elution buffer AE. Primers JW11 and
JW12 were used,[29] in a reaction of 25 µl containing 1x QuantiTect SYBR Green PCR Master Mix
(Qiagen); 1 µM of each primer; 0.1 mg/ml acetylated BSA; and 2.5 µl DNA. Cycling was performed
in a Light Cycler 480 instrument (Roche, molecular.roche.com) using an initial denaturation of 15
minutes at 95°C, followed by 50 cycles of 10 seconds at 95°C, 20 seconds at 57°C, and 30 seconds
at 72°C. The Tm of the amplicons was determined in a melting curve analysis from 67°C to 95°C.
A standard curve was included in each PCR, ranging from 103 down to 10-4 pg L. infantum DNA,
determined spectrophotometrically. The kDNA-PCR was considered positive for Leishmania if
more than 0.2 parasite genome equivalents were detected on the slide, and a melting peak was
observed between 79.5°C and 81°C.
Analysis
Data were entered in duplicate in Microsoft Excel 2016 and a duplicate check was done to detect
typing errors. Data analysis was performed using Stata 13 (Stata Corporation, Texas, USA).
Differences in proportions were tested using Fischer’s exact test. The Sensitivity (Se), Specificity
(Sp), Positive Predictive Value (PPV) and Negative Predictive Value (NPV) of the RDT were
calculated comparing the results of the index test to the composite reference standard. The
composite reference standard was defined as follows. A patient was considered as a confirmed
case of CL if microscopy results and/or PCR results (be it kDNA or ITS1) were positive. Else, the
patent was considered a non-case. Test accuracy was first calculated in the whole study
population and then compared across subgroups defined on the basis of geographical origin,
Leishmania species, and slide quality.
We estimated the required sample size (n = 240) based on an expected frequency of CL in the
patient series of 50%, an anticipated sensitivity of the CL Detect Rapid Test™ of 97% and a
specificity of 84%, an α error of 5%, and a power of 80%.
Quality assurance
The study was registered on clinical trials.gov with the identifier NCT2979002 in November 2016.
Before the start of the study, Standard Operating Procedures (SOPs) were developed (available
on request). These SOPs were carefully explained and validated during three training days for all
health professionals involved in the study procedures. The diagnostic tests in this study were
done blinded to the results of other tests, i.e. readers of the index and reference tests did not
have access to any other test results. Each package of RDTs was subject to internal quality
control, using a positive and negative control following the manufacturer’s recommendations.
These controls of all RDT packages were done during a training workshop prior to the study. We
report the results in compliance with the STARD (Standards for Reporting of Diagnostic Accuracy
studies) checklist.[30]
166 | Chapter 6
Ethical aspects
The protocol of this study was approved by the Institutional Review Board of the Institute of
Tropical Medicine in Antwerp (Reference1060/15), the Ethics committee of Antwerp University
Hospital UZA (Reference15/51/557) and the Comité d’éthique en recherche biomedicale CERB
(Reference41/16) in Rabat. The results of the index test under evaluation and the molecular tests
(PCR) were not communicated to the patients or their physicians. Hence, no therapeutic
decisions were based on the index test results, and CL case management followed current clinical
guidelines in Morocco.
Results
Participants
In total, 219 patients were included (Figure 2), amongst whom there were 113 men (52%) and
106 women (48%). Half of the participants (n = 108; 50%) were under 18 years old. Seventy-four
patients (34%) had two to ten lesions. The diameter of the selected lesions ranged between 0.1
and 5 cm. Most lesions were small: 142 participants (65%) had lesions with a diameter of one cm
or less. Table 1 shows the demographic and clinical characteristics of the study population. None
of the health professionals reported any adverse events from the sampling, even if they did not
systematically use lidocaine ointment (Emla®) or injectable xylocaine. There were no withdrawals
from the study.
Test methods
For the RDT, there were no missing data, nor any invalid results. The RDT gave 97 positives and
122 negative results. The average time to perform the RDT was 32 ± 7 minutes (n = 217) with a
range between 15 minutes and 48 minutes.
For the reference standard tests, some data were (partially) missing, as, during transportation of
microscopy slides between the primary health facilities and provincial laboratories, 17 slides
broke, and one of them was irrecoverable. Moreover, 32 slides were not well fixed, which limited
the second reading by the NIH supervisor. For PCR tests, three partially broken slides were
recoverable and two completely irrecoverable. The mean time (±SD) to obtain the result of
microscopy from the provincial laboratories was 2.7 ± 3 days (n = 198).
CL RDT in Morocco |167
Figure 2. Flowchart of the study
RDT
N = 219
RDT Positive
N = 97
RDT Negative
N = 122
Reference standard
done
N=97
Reference standard
done
N=122
Potentially eligible participants
N = 769
Eligible participants
N = 266
Excluded
N = 503
- Age less than 05 years old (307)
- Non-ulcerative CL form (50)
- Received traditional or physical
treatment of the lesion (21)
- Received antimoniate or anti-
parasite treatment (42)
- Lesion duration of more than
four months (81)
- Other reasons, unspecified (02)
No RDT
N = 47
- Lesions near to the eye (13)
- Refusal to participate (07)
- Impossibility to sign informed
consent (27)
Final diagnosis
Absence of CL (N = 05)
Presence of CL (N = 92)
Final diagnosis
Absence of CL (N = 78)
Presence of CL (N = 44)
168 | Chapter 6
Table 1. Demographic and clinical characteristics of 219 patients enrolled
Characteristics N
Provinces historically endemic for L. major
Errachidia 42
Ouarzazate 35
Provinces historically endemic for L. tropica
Tinghir 65
Sefrou 67
Sidi Kacem 10
All 219
Patient age (years)* [05 - 17] 108
[18 - 87] 110
Sex Women 106
Men 113
Lesion on the face Yes 112
No 107
Lesion duration (days)** ≤ 50 105
> 50 107
Lesion diameter (cm)* ≤ 01 142
> 01 76
Number of lesions per patient 01 145
02-10 74
(*) Information missing for one participant (**) Information missing for seven participants
Diagnostic accuracy
The reference standard classified 136 (62%) participants as CL cases: 75 had both positive
microscopy and positive PCR results, 26 had positive microscopy only, and 35 had positive PCR
only (Figure 3). The frequency of confirmed CL in this patient series varied by region: in the areas
known to be endemic for L. major, it was 70%, compared to 58% in L. tropica regions. The
Leishmania species could be identified in samples of 87 participants: 35 were L. major, 40 L.
tropica, and 10 L. infantum. The geographical distribution of the species is shown in Table 2.
CL RDT in Morocco |169
Table 2. Place of inclusion and index test results according to Leishmania species,
n = 87
L. major L. infantum L. tropica
N RDT + N RDT + N RDT +
Provinces historically endemic for
L. major
Errachidia 19 12 00 - 00 -
Ouarzazate 14 10 00 - 00 -
Provinces historically endemic for
L. tropica
Tinghir 02 01 01 01 22 16
Sefrou 00 - 10 08 18 17
Sidi Kacem 00 - 01 01 00 -
Total 35 23 12 10 40 33
Species identification based on ITS1 RFLP (n = 80) or HSP70 (n = 7).
When compared to the composite reference standard, the RDT showed a Se = 68% [95%
confidence interval (CI), 61-74], Sp = 94% [95% CI, 91-97], PPV = 95% [95% CI, 92-98] and NPV =
64% [95% CI, 58-70] in the whole study population (n = 219). The diagnostic accuracy varied
according to the geographical origin of the samples, though this difference was not statistically
significant. The Se of the RDT was higher in regions historically endemic for L. tropica, i.e. 73%
[95% CI, 66-80], versus 59% [95% CI, 48-70] in L. major regions (Table 3). This species effect was
supported by comparing the results of the RDT after typing of the samples: 83% of the confirmed
L. tropica and 66% of the L. major samples were RDT positive (Table 2); However, in this
comparison, the observed differences in Se and Sp did not reach statistical significance (Fisher
exact = 0.32 and 0.10 respectively). On the other hand, we did find a significant association
between RDT accuracy and smear slide quality: RDT Se was significantly higher among patients
in whom microscopy slides of better quality were obtained compared to the rest of the
population (Table 3) (Fisher exact = 0.001).
170 | Chapter 6
Table 3. Accuracy of the CL Detect RDT™ according to the geographical origin of the samples and slide quality
N
Sensitivity
Specificity
PPV
NPV
Provinces historically
endemic for
L. tropica 142 73% [95% CI, 66-80] 92% [95% CI, 87-96] 92% [95% CI, 88-97] 71% [95% CI, 64-79]
L. major
77 59% [95% CI, 48-70] 100% 100% 51% [95% CI, 40-62]
Slide quality ɸ
Excellent quality 42 88% [95% CI, 78-98] 100% 100% 71% [95% CI, 58-85]
Average quality 92 64% [95% CI, 54-74] 96% [95% CI, 92-100] 98% [95% CI, 95-100] 50% [95% CI, 40-60]
Bad quality
69 53% [95% CI, 42-65] 90% [95% CI, 83-97] 80% [95% CI, 71-89] 72% [95% CI, 61-82]
(ɸ) 16 cases were impossible to assess by the laboratory engineer at the NIH due to the poor fixation of the smear slides.
CL RDT in Morocco | 171
The room temperature during the RDT implementation varied between 8°C and 38°C. Nine RDTs
were performed at a room temperature above 30°C. In total, only 47 samples (21%) were
examined at a room temperature between 20°-30°C, i.e. corresponding to the manufacturer’s
instructions.
Figure 3. Distribution of index and reference test results in the study population (n =
219)
Discussion
We report the first evaluation of an RDT for CL in a series of Moroccan patients with skin lesions
suggestive of CL. In remote and rural endemic areas in Morocco, we can recommend for patients
presenting skin ulcers suggestive of CL to use at first the RDT, followed by microscopy for those
who are RDT negative. Indeed, the sensitivity of this RDT was moderate, and the specificity was
excellent, leading to a high PPV of 95%. This means that 19 out of 20 patients with an RDT-
positive ulcer truly have CL, and that treatment is therefore warranted in this group. The RDT-
negative patients will need a second test to rule out CL, as the NPV was low. The turn-around
time (i.e. the rapidity of getting the results) of less than 40 minutes, the absence of invalid results
and the short time required for training the health center staff are also supporting the use of this
RDT in remote rural areas. The study followed a phase III design, recruiting suspect patients in
real-life conditions in nine different health facilities, and this is representative of the context in
which the RDT will be used in the future. This study design provides a solid basis for eventually
reformulating the diagnostic policy in CL in Morocco.
172 | Chapter 6
Current limitations of this RDT are that its stability in ambient temperature is only assured for
two years, as well as the cost. In Morocco, the current (2016) unit price of this RDT was US$ 8
per patient, which is not affordable in comparison with microscopy that costs less than US$ 1
per patient. However, a recent study in Sri Lanka using the same RDT for L. donovani mentioned
a lower cost, US$ 4 per patient,[31] and future cost may evolve as a function of demand and
offer.
We acknowledge that our study has some limitations. Firstly, our reference standard
classification was probably not 100 percent perfect. The sampling procedures for microscopy
and PCR were the main factor that may have limited the sensitivity of the reference standard.
Secondly, the kDNA-PCR was not systematically done on all the second slides. A suboptimal
sensitivity of the reference standard may have decreased somewhat the specificity estimate of
the RDT, though this seems not so apparent from our results. Thirdly, it was not possible in this
study to systematically determine the alternative diagnoses in patients who did not have CL.
Fourthly, because the age of lesions was based on the subjective declaration of the patient, we
may have unwittingly included a few patients with lesions older than four months [12].
Our results are consistent with those from a study in Afghanistan, in which the same CL RDT was
used in 257 patients with mostly nodular lesions, living in Kabul, where L. tropica is known to be
the predominant species [32]. The accuracy of the RDT compared to a reference standard based
on qPCR and microscopy was: Se = 65% [95% CI, 59-71]; Sp = 100%; PPV = 100% [95% CI, 98-100];
NPV = 16% [95% CI, 09-24] [32].
An economic evaluation of the same RDT compared to microscopy in a population living in L.
tropica areas, reported that the incremental cost-effectiveness ratio per DALY averted was less
than $US 10.15 for the RDT compared to microscopy, which makes it an attractive option.[33]
Other studies suggest that loop-mediated isothermal amplification (LAMP) could be an
alternative as a point of care diagnostic, though the required equipment, training and technology
is less user-friendly than an RDT. Reverse transcriptase LAMP seems especially interesting for CL
diagnosis in regions where a species-specific diagnosis is required because several species
circulate simultaneously [34–37].
Some questions remain unanswered. The study was not powered to show any species-
dependent differences in sensitivity, though our results suggest there is such an effect. If this is
explored further and a species effect is confirmed, further work would need to verify if the
antigen targeted by the assay is not slightly different in L. major areas in Morocco. In the Sri
Lanka study, the low sensitivity of the RDT (36%) was linked to the low expression of the
peroxidoxin antigen in Sri Lankan L. donovani [31]. Alternatively, the ‘species’ effect could simply
be due to differences in parasite load, which could obviously influence the assay’s performance.
The moderate sensitivity of the RDT in this study could also be explained by a low parasite yield
CL RDT in Morocco | 173
within the sample taken by the small saws of a dental broach. There is scope for optimizing the
sampling technique, for example with the use of a sterile disposable punch, as recently
published, or by repeating the procedure.[38] Further work is required to explore these
hypotheses.
In conclusion, this novel RDT for CL in its current format is a useful addition to clinical case
management in Morocco, especially in isolated localities far from provincial laboratories. A
positive RDT has a very good PPV (95%) and warrants treatment in endemic CL areas. This RDT
is a powerful decision-making tool for nurses and other health professionals to improve the
management of CL in remote areas. The RDT can be part of an algorithm that uses microscopy
in a second step. Nevertheless, we recommend improving the sensitivity of this RDT, and this
could probably be reached by optimizing the sampling procedure.
Acknowledgments All authors of this manuscript want to thank all patients and participants in this study. A special
thanks to all health professionals from the five provinces who participated voluntarily at different
steps of this project, namely Mr. Smaine Chichaoui, Mr. My Ahmed Hajji, Mr. Mohamed Sadiki,
Mr. Redouan Lahcen, Mr. Ahmed Fahim, Mr. Lahzen Daoudi, Mrs. Hasna Tifa, Mr. Lahcen Tastift,
Mr. Mohamed El Qadi, Dr Naima Ait Taleb, Mr. Mustapha Hajji, Mr. Ilyas Ezzourguoui, Dr.
Abdelkacem Ezzahidi, Dr. Youssef El Berkaoui, Mr. Bihi Ouchaghoun, Mr. Abdelaziz Oukhouya,
Mr. El Houcine Ico, Mr. Noureddine Belgacha, Mr. Abdellah Rylani, Mrs. Meryem Mesbahi, Mrs.
Hanane El Kihel, Mr. Zakaria El Alaoui, Dr. Chakir El Khiari, Mr. Omar Benselmori, Mr. Abdelhak
Grine, Mrs. Naoual Laaroussi, Mr. Ziane Mohamed, Mr. Khalid El Khalid, Mr. Imad ElBransi, Mr.
M’barek Karzaz, Dr. Bouchra Delouane, Dr. Amina Hajli, Mrs. Bouchra El Mansouri, Mrs. Salwa
Benlkhir, Mr. Redoine Mouida, Dr. Nadia Bennis, Mr. Youssef Amrani Jouti, Dr. Yassine
Aqachmar, Prof. Dr. Chakib Nejjari, Prof. Dr. Abaacrouche Mina, Prof. Mounim Belalia, Mr. Hamid
Jahdi and all Moroccan health authorities at the national, regional and provincial levels who
supported administratively this study. In the Institute of Tropical Medicine, many thanks to Mrs.
Erika D’Haenens, Mrs. Ilse Maes, Mrs. Evelien Paessens, Mrs. Anne Marie Trooskens and Prof.
Dr. Vincent De Brouwere who supported the study.
Financial support Support for the fieldwork came from the Ph.D. grant of the first author allocated by the Belgian
Development Cooperation via the Antwerp Institute of Tropical Medicine and the administrative
support of the National School of Public Health Rabat. GVDA is supported by the Belgian
Development Cooperation.
The Belgian Development Cooperation had no role in study design, data collection, data analysis,
data interpretation, or writing of the manuscript.
174 | Chapter 6
Competing interests None declared. The manufacturer of the RDT did not interfere with the decision to publish nor
with the content of the publication.
Previous presentation of the results of this study
The preliminary results of this study were presented as part of a poster communication (n° = C-
1606) at the 6th World Congress on Leishmaniasis in Toledo, Spain, in May 2017 and as a poster
(n° = 3P17) at the 10th European Congress on Tropical Medicine and International Health in
Antwerp, Belgium, in October 2017.
Authors’ addresses
Issam Bennis National School of Public Health, Ministry of Health, Rabat, Morocco. Department
of Public Health, Institute of Tropical Medicine, Antwerp, Belgium. Department of Biomedical
Sciences, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp,
Belgium. Email: [email protected]; Kristien Verdonck, Department of Public Health,
Institute of Tropical Medicine, Antwerp, Belgium. Email: [email protected] Nora el Khalfaoui,
Myriam Riyad, Laboratory of Parasitology & Research team on Immunopathology of Infectious
and Systemic Diseases, Faculty of Medicine and Pharmacy, University Hassan II of Casablanca,
Morocco. Emails: [email protected]; [email protected]. Hajiba Fellah, National
Reference Laboratory of Leishmaniasis, Parasitology Department, National Institute of Hygiene,
Rabat, Morocco. Email: [email protected]; Gert Van der Auwera, Department of Biomedical
Sciences, Institute of Tropical Medicine, Antwerp, Belgium. Email: [email protected]; Hamid
Sahibi, Department of Parasitology, Hassan II Agronomy, and Veterinary Institute, Rabat,
Morocco. Email: [email protected]; Souad Bouhout, Unit of Parasitic Diseases,
Directorate of Epidemiology and Disease Control, Ministry of Health, Rabat, Morocco. Email:
[email protected]; Jean-Claude Dujardin, Department of Biomedical Sciences, Institute
of Tropical Medicine, Antwerp, Belgium. Email: [email protected]; Marleen Boelaert,
Department of Public Health, Institute of Tropical Medicine, Antwerp, Belgium. Email:
CL RDT in Morocco | 175
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Supplemental file 1: Repartition of the samples
Discussion | 179
CHAPTER 7. General discussion
Discussion | 181
1. Cutaneous leishmaniasis control
The first article in this thesis (Article1) [1], describes the epidemiological trend of CL in the
province of Errachidia as reported by the Moroccan health system and analyses the effect of a
rodent control intervention in this province. The intervention consisted in the use of poisoned
wheat baits to reduce the number of rodents (Meriones shawi), the reservoir host for L.major
[2]. This intervention led to an observed decrease in human CL cases, but, as it was a public
health intervention, there were no randomly selected control groups, and only before/after
comparisons could be made, or comparisons between areas where the intervention started
earlier vs. later. To ensure the success of this control intervention, it was necessary to align the
efforts of teams from several ministries i.e. the Directorate of Epidemiology and Disease Control
(Ministry of Health), Directorate of Local Communities (Ministry of the Interior), the National
Office of Food Safety (Ministry of Agriculture), as well as the local authorities. Civil society
members organized themselves into support groups and deployed the poisoned wheat in the
rodent burrows, in a radius of about 500 meters around the houses. This operation had to be
repeated at least twice or three times a year until there were no further CL cases. The inter-
sectoral collaboration was a success, as the different ministries worked efficiently together and
the coverage of the at-risk area by the intervention was excellent. Whether the intervention was
effective and cost-effective is not so easy to derive from our data. Our study was descriptive in
nature, and no experimental study has ever been done with these poisoned baits. We concluded
that there was an effect on CL incidence, without providing hard causal evidence. Nonetheless,
the effectiveness of CL control strategies by rodent poisoned bait does not come only from
Morocco. In 1973 zinc phosphide was used against rodents in Iran based on a similar intervention
from Azerbaijan (Ex URSS), but it was not successful to reduce the incidence of CL [3]. However,
other studies from Iran, published in 2000, 2005 and 2014, claimed that zinc phosphide-treated
baits placed inside rodents borrow led to a decrease of both Ph. papatasi density and CL human
incidence [4–6]. Zinc phosphide or phostoxin showed similar effectiveness [5]. Authors
suggested that rodent control operations using zinc phosphide within a 500-meter circle around
houses should be deployed once every two years before the start of the sand fly season [6].
In Morocco, the cyclicity of the outbreaks is documented for ZCL cases as shown in the updated
figure 1 from our previous article published [1]. The fluctuation in an epidemic cycle with five to
ten years intervals is attributed by some researchers to loss of herd immunity or to natural
disasters such as floods or dryness. The 2017 outbreak is dominated by the ZCL cases noticed in
three provinces from southeastern Morocco (Errachidia n=1436; Tinghir n=1091 and Zagora
n=1702) representing 90% of all cases reported in the country (n=4737). As explained before, the
Errachidia province had less tendency of cases compared to the neighboring provinces. The 2018
tendency will give a hypothetic answer about the success of the rodents control strategy if the
number of ZCL cases in Errachidia province will remain less important than in other provinces.
However, the relationship is difficult to establish. Longitudinal studies accounting for the genetic
182 | Chapter 7
heterogeneity of human and parasite populations with regard to the global environmental
vulnerability could bring some answers [7].
Figure 1: Number cases of Zoonotic Cutaneous Leishmaniasis per year in Errachidia Province
and other affected Moroccan Provinces between 2004 and 2017.
We did not document the environmental effects of the strychnine baits in Morocco. In other
studies, strychnine use was found harmful to the environment [8, 9]. Moreover, the scope for
replicating this intervention elsewhere depends on its acceptability by the local population as
well as on the quality of inter-sectoral collaboration, which is not necessarily the same in each
province. Furthermore, this control strategy requires sustainable funding and the political
endorsement of the Ministry of Health (MoH). This type of intervention is often seen as an
exclusive task for the Ministry of Agriculture with the primary aim to protect crops and palm
trees by reducing the rodent population, and the link with CL is not always made spontaneously.
High staff turn-over furthermore compromises the sustainability of this intervention. Young
public health staff is not motivated to get involved in vector control operations, because of the
unattractive living conditions typical of these remote areas.
How to be less harmful to the environment when carrying out rodents’ operations should be
addressed by adopting a new technique based on the use of toxic fumes (carbon monoxide,
nitrous oxide, sodium oxide) by gas cartridges to fumigate rodent burrows15. A 2013 report from
the USA agricultural department cited “There are no secondary poisoning risks involved with the
use of gas cartridges as the gas produced dissipates into the atmosphere shortly after activation.
Primary risks to non-targets would be minimized by treating only active burrows”16.
15http://www.wildearthguardians.org/site/PageServer?pagename=priorities_wildlife_war_wildlife_kill_methods_denning accessed in 10 april 2018 16http://www.aphis.usda.gov/regulations/pdfs/nepa/2013_RI_Mammal_EA_website_DRAFT.pdf
0
500
1000
1500
2000
2500
3000
3500
4000
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017
year
ly c
ases
YEARErrachidia District (yearly cases) Other Moroccan Districts (yearly cases)
Discussion | 183
The manual for case management of cutaneous leishmaniasis in the WHO EMR recommends
data collection and analysis with the aim to measure the performance of the health intervention
at different levels of the health system [2]. However, the rodents’ operations quality control or
monitoring system are absent in the Moroccan leishmaniasis guideline, except for an indicator:
the number of active burrows x 5 / mammalogical surveillance station per hectare [10]. A
protocol describing technical standard operating procedures should be developed before
starting field trials to assess the effectiveness of such new preventive measure against rodents’
population in L. major endemic areas.
For the Moroccan MoH, developing a CL control policy is complex. The fight against ZCL, which
occurs predominantly in scantily populated rural areas, proved relatively successful so far, while
control measures were less effective in fighting the anthroponotic CL form (ACL), which affects
peri-urban and urban agglomerations with a higher population density. The National Institute of
Hygiene (INH) in Morocco and the Directorate of Epidemiology and Disease Control conducted
two trials to evaluate the effect of prevention strategies. The primary outcome measure of the
first trial of vector control methods was CL incidence. Three intervention arms were compared:
1) the use of long-lasting insecticide-treated nets (LLINs) (Permanet2®; Vestergaard Frandsen,
Lausanne, Switzerland) or the insecticide-treated bed nets (ITNs) impregnated with deltamethrin
at 55 mg/m² with distribution of ITNs or LLINs to cover all sleeping areas with environmental
management; 2) indoor residual spraying (IRS) using α-cypermethrin with environmental
management; and 3) environmental management that consisted of campaigns to promote
personal protection against exposure to sand flies, cleaning of animal sheds, waste disposal, and
maintenance of hygiene. The study concluded that IRS with α-cypermethrin and LLIN distribution
both reduced the incidence of CL [11]. IRS was highly effective and more cost-effective for the
prevention of CL in L. tropica and L. infantum areas [11].
The second field trial evaluated the use of systemic ivermectin-baited traps in rodent reservoirs
to control the sand fly vector of L. major. This trial showed excellent results on the reduction of
vector density with a preservation of the environment [12]. However, IRS and ivermectin-baited
traps are not yet adopted for widespread use in endemic CL areas in Morocco as the health
authorities require more evidence of their effectiveness under real-life conditions. In the current
context, the rodent control intervention with strychnine baits is still the intervention of choice
in several zoonotic CL endemic areas in Morocco in case of a new outbreak. Similarly, the only
ACL control strategy currently recommended by the MoH in its national Leishmaniasis Control
Guide is a rapid clinical diagnosis of CL patients and permanent covering of lesions with plaster
strips to prevent sand flies getting infected through uncovered ones and subsequently
transmitting the disease to humans. This type of recommendation is neither realistic nor based
on evidence of its effectiveness. A large number of those infected by CL and seeking treatment
in primary health centers are children younger than 10 years of age who are tempted to remove
the plaster strip after only a few hours. Furthermore, the cost of the frequent plaster changes
184 | Chapter 7
over a long period (days or rather months) before the scars start healing is substantial and must
be covered by the patient. Finally, the lesions are often located in areas that are difficult to cover
with an adhesive plaster.
In 2015 a Cochrane review [13] was published about vector and reservoir control interventions
for preventing both visceral and cutaneous leishmaniasis. For CL, the authors reviewed the
effectiveness of 14 interventions. Two Iranian trials studied permethrin-impregnated soldier
uniforms as a personal protection measure, but the sample size was insufficient to conclude on
any effect. An intervention trial of LLINs (Olyset®) showed a decrease of indoor female Ph.
sergenti density compared to a control group [14, 15]. The Cochrane review concluded that
insecticides may be effective at reducing the incidence of CL. However, the level of evidence
remains insufficient to discriminate between IRS, or the use of insecticide-treated bednets,
bedsheets, or curtains [13].
In summary, few data exist on prevention of ACL, and even if the effect of insecticidal
interventions was demonstrated on entomological outcomes in proof-of-concept studies or
small-scale field trials, their effectiveness in real-life conditions is not guaranteed. Moreover, no
studies about the acceptability of these preventive measures are available, while acceptability is
an important determinant of the success of any disease control strategy. A recent study analyzing
risk factors of CL in Southwestern Morocco showed a correlation between ACL and vulnerable
socio-economic conditions [16]. The poverty rate of the affected communities and their
behaviors should be addressed to break the anthroponotic transmission. Like in the case of one
study from Iran demonstrating that the “chance” to get ACL increases when the poor population
lives close to the cattle sheds [17]. Such example matches the social vulnerability in endemic
Moroccan ACL areas where the use of bed nets by rural population does not seem adapted to
their behaviors.
Unfortunately, a new preventive measure against ACL in Morocco cannot work without two
conditions: (1) downsizing the damage of the presence of animal cattle around the shelters and
people at risk of this disease; (2) introducing a long lasting easy rechargeable insecticide tool that
could be portative on necklace and/or bracelet to decrease risk of human contact with the ACL
vector. Such tools should be distributed in mass with the aim to stop the transmission cycle.
Discussion | 185
2. Cutaneous leishmaniasis social representations and psychological suffering
So far none of the studies carried out in Morocco did directly address the psycho-social burden
of CL on Moroccan individuals and/or communities. In southeastern Morocco, the disfiguring
scars resulting from this disease, which are particularly distressing for young girls, led to repeated
demands for cosmetic surgery during our work as public health doctor in the region. On the other
hand, public health policy seems to underscore the benign nature of CL. Therefore, our approach
was to get a broader understanding to what extent a population living in a CL endemic area
suffers psychologically and/or socially from the consequences of this disease. We started by
studying the perception of CL among the general population and carried out Focus Group
Discussions (FGDs) (Article 3) [18], in two different areas, endemic respectively for L. major and
L. tropica. We included both people with a modern and a traditional perspective, and stratified
groups into those who use modern health care facilities and those who have more confidence in
traditional remedies or use traditional healers in a first instance. We took into account local
sensitivities between ethnic groups and had separate groups for men and women to reach
maximum information and create the best possible conditions for uninhibited talks. The impact
of the disease was more felt in the L. major area than in the L. tropica region, probably this was
due to the larger size of L. major scars. No consensus prevailed in these communities on the
psychological effect of CL. However, as discussed by Deacon et al. (2005), in their study of HIV
stigma, there is no need for an explicit consensus for the stigma to be at work [19]. Some
respondents in our Focus Groups asked for a quick start of treatment to reduce the size of final
scarring, while others shared their fear of injections which they believe could damage their
kidneys or just stated that scars became very dark or darker than the rest of the skin because of
the use of this medication. According to the respondents, it is a problem that no therapeutic
options are proposed because health professionals give the same medication to all patients. The
issue of the disfiguring scars came up time and again. Scars were discussed in terms of
treatments that can reduce the lesions or make them disappear and in terms of their location
and psychological impact. CL scars have become linked to a shared social identity, they are “the
label (stamp) of the area”. Some people expressed proud to have CL scars but said to be ashamed
to show it once they went abroad. Nonetheless, there was a consensus that CL diminishes the
marriage prospects of young women, and many illustrations of stigmatizing behavior towards CL
patients were given.
The problem of CL is also perceived quite differently according to age. Adults and the elderly may
consider it as a relatively minor problem, while young people, male and female alike, see it as a
big problem. In Article 2 [20] we analyzed the psychosocial impact of scars caused by L. major in
adolescents attending a boarding school in two CL endemic zones. Students were asked to fill in
a questionnaire about their knowledge of this disease and related psychological effects. Twenty
percent of the boarding school students who were surveyed had been affected by CL in the past.
CL scars led to a considerable psychosocial burden in this adolescent age group. Girls seemed to
186 | Chapter 7
be more affected than boys, but both genders equally expressed their concerns and demands
for scars treatment [20].
We broadened the scope of our analysis by conducting a review of the literature on the
psychosocial weight (stigmatization, psychological consequences, and impact on quality of life)
of CL in its localized form (LCL) in countries other than Morocco, to establish the external validity
of our results. Article 4 [21] is a scoping review of the psychosocial impact of LCL. There are
several studies from Latin America and Ethiopia showing the stigmatizing effect of CL in its
mucocutaneous and diffuse forms. However, little information on stigma among people affected
by the most common form, localized CL (LCL) was found at the beginning of this Ph.D. study.
Fortunately, in the last two years, other articles were published. This scoping review showed that
the psychosocial impact of CL on the affected person is real and corroborates our results
obtained in Morocco. Most of the published work is based on cross-sectional surveys of CL
patients that are asked to answer a standardized scaling questionnaire. Few truly qualitative
published research are available, except for the work carried out by Reyburn in Afghanistan who
documented huge discrimination against and stigma of CL patients, because the disease was
thought to be contagious by direct contact. We also concluded that the psychological effect of
CL is not so easy to measure in cross-sectional studies, as it may evolve over time, and
prospective studies are in fact needed to adequately measure it. We also realized the importance
of documenting the context, as confounding factors (i.e. socioeconomic level, the educational
level, religious and traditional beliefs) may play an important role.
As explained by Moscovici, the researcher working on social representations should keep in mind
the religious, political and cultural context of phenomena that social psychology is supposed to
explain [22]. The way how rural poor Moroccan citizens think about the meaning of scars in their
everyday life, cannot be understood in isolation from the present sociocultural reality and the
desired future. The collective awareness in this society will shape the degree to which CL has or
not a psychological impact.
The comparison of CL’s perception in Latin America with North Africa gave rise to the following
reflections. As described previously, the mucocutaneous CL form is more stigmatizing than the
localized form. However, when comparing LCL in both regions, one should include religion and
traditions that influence behavior and women’s power in the society. In Muslim countries, by
tradition women cover most of their body, so CL scars on unexposed parts do not matter much.
However, when the CL scar cannot be covered, the body image gets seriously damaged and CL
scars may have an impact similar to burns. This impact can be profound, affecting spirituality and
belief in God [23]. Sometimes patients want doctors to talk with them about spirituality as part
of their psychological healing [24]. A study from Iran reported how indelible burn scars and
disfigurement led some of the patients to feel so desperate they began doubting the existence
of God or His mercy [25]. Religion and spirituality play an important role in the quality of life of
Discussion | 187
Moroccan patients, and this will affect their coping strategies when confronted with the loss of
their body image. Physicians should pay attention to the alarm signs of hidden psychological
suffering when patients with LCL explain their dermatological ailments by referring to religion
and God’s will.
3. Cutaneous leishmaniasis clinical management
In the absence of effective treatment against CL scars, and the lack of an effective vaccine to
prevent infection, we focused on improving the clinical management of patients affected by CL
by targeting rapid diagnosis tools at the point of care. The ultimate objective was to ensure, in
remote isolated areas in Morocco, an early start of treatment to may avoid the emergence of a
larger lesion but also avoid the abusive or inappropriate use of the available first-line treatment
(meglumine antimoniate or Glucantime®).
Hence, the assessment of the accuracy of a Rapid Diagnostic Test (RDT) for CL in Morocco in
comparison with reference laboratory tests that were included as manuscript n°5 [26]. Such a
point-of-care test, if considered effective, is an appropriate solution both for healthcare
professionals and patients who work and live far from the provincial laboratories.
Geographically, in endemic areas with anthroponotic cutaneous leishmaniasis (ACL), most
primary health care centers (in the selected provinces Sefrou, Sidi Kacem and Tinghir) are located
more than 50 km away from the nearest provincial laboratory. Our study found that if health
professionals follow the recommendations of the Leishmaniasis Control Guide 2010, they will
not start treatment on suspicion of ACL before receiving microscopic confirmation about the
presence of Leishmania bodies in the skin sample. To get this laboratory confirmation, the smear
should be sent from the primary health center to the nearest qualified technician working in a
fully equipped laboratory. This information then needs to be sent back to the health center
where appropriate treatment can be started. In practice, professionals who follow this
procedure will ask the patient or his/her family to take the prepared glass slides to a laboratory,
return later to the same laboratory to get the results which they then hand back to the health
facility. Many times, they are faced with unpredictable weather conditions and the risk of partial
or complete destruction of the glass slides during transport. Furthermore, some laboratories
take it upon themselves to re-sample suspicious skin lesion(s) to ensure they have enough skin
smear on which to carry out microscopic reading. The result is almost never obtained on the
same day the patient brought the sample. In our study, we noted that almost all microscopic
analyses took on average at least two working days, even with committed laboratory and health
center staff. Moreover, in routine clinical management, most patients, and their families do not
have the means to undertake the trip to these laboratories for analysis of their sample and send
it by other means. There is, in that case, a high probability that the information has not yet
reached the health center before a therapy decision is taken. In case of suspected CL, some
188 | Chapter 7
professionals start by giving one or two intra-lesional test injections of Glucantime® often on
request of the patient. Then, they wait to see what happens and if the result is positive, the
treatment is continued. If the treatment did not give the desired effect, patients are referred to
a dermatologist or given prescriptions of other medicines. In the predominantly L. major
endemic areas, this presumptive treatment is actively promoted by the MoH. Indeed, the MoH
recommends treating based on presumptive clinical signs of CL and using laboratory
confirmation only in the event of an outbreak in a new area not previously known as CL endemic.
“…health professionals make a clinical diagnosis and microscopically confirm the first cases of
leishmaniasis declared in the suspected outbreak. It is recommended that later cases receive
treatment based on a clinical diagnosis in the absence of a microscopic diagnosis.” [10, 27].
Glucantime® also has side-effects which should not be inflicted on patients with skin conditions
other than CL. Indeed, as described in paper #5 [26], our study showed that 38% (83/219) of
patients with skin lesions that were clinically suggestive of CL were not confirmed by the
reference standard. In L. major endemic regions more specifically, this percentage was around
30%. This is a high proportion of patients without laboratory-confirmed CL who risk being
treated. At least one diagnostic test for CL should be positive before the start of any antimoniate
treatment.
The reference standard used in our study was based on the combination of PCR and microscopy.
During the training organized for all health professionals participating in our study, a single
technique for the collection and preparation of laboratory slides was adopted and explained by
an expert from the national leishmaniasis laboratory at INH. All professionals were instructed to
take their samples from the center as well as from the edges of the lesion as recommended by
the literature [28]. This same laboratory expert had to re-read all the microscopic slides after
recoding and anonymization to verify the first microscopic reading by the laboratory technicians
of the participating provinces. In this way, we could optimize the sensitivity of the reference
standard.
We acknowledge that the conventional PCR technique used in our reference standard has its
limitations, that is why we included a repeat PCR in the same lab for one half, and in an
international reference laboratory at ITM-Antwerp for the other half of the samples. The
selection of slides for this second reading was made randomly. At ITM, real-time PCR was used,
which is faster and has a lower contamination risk with fewer manipulations than conventional
PCR based on the ITS1 primer [29]. Also, qRT-PCR is the best tool to quantify Leishmania parasites
with a high sensitivity and reproducibility [30]. However, for species typing, other methods are
better [31, 32]. Standardised protocols of real-time PCR assay to quantify CL parasite load should
be recommended in the WHO Eastern Mediterranean Region particularly for multi-centric
research studies. This was successfully done in Latin America supported by the DNDI and the
WHO initiative [33].
Discussion | 189
Another concern is the possible recall bias of the duration of disease (lesion) prior to enrolment
as reported by patients and/or their relatives. Olliaro et al, [34] published in 2013 methodological
recommendations for doing CL clinical trials in which they explained that the duration of the
lesion is partially species-dependent and there was a concern that natural healing as the example
of L. major may be a confounder. Moreover, until today there is no standardised way to estimate
the duration of the disease and the authors for this clinical trial methodology recommended to
include patients who reported lesions of a duration between 3 to 6 months [34]; another recent
article written by the same first author did not report answers to those questions [35].
So far, we did not perform any cost analysis of any of the laboratory tests used. It is
recommended that the diagnostics in development strike a balance between being sensitive
enough and remaining cheap, usable and having a quick turnaround of results [36]. As the study
project was performed in well-known endemic CL areas, further research is required to
understand how the predictive values might change at the lower transmission level, in off-season
settings or in settings with declining transmission.
Some recent publications recommend the loop-mediated isothermal amplification (LAMP) as
diagnosis tool rather than an RDT [37–39]. We believe that making preparations of 4 to 6 primers
needed for LAMP looks like a real laboratory task that Health Centre nurses would not accept to
perform. Moreover, even if LAMP allows species identification, this seems not useful in the
Moroccan context where the same treatment guidelines apply to the three CL species,
depending only on the localization, the size and the number of CL lesions. This is also the case
for the stepwise algorithm of CL treatment published in 2014 by EMRO where the treatment
decision is based on the risk-benefit ratio of the intervention for each patient [2]. However,
species identification could be valuable for travellers and tourists with suspected CL lesions and
valuable for epidemiological surveillance [2]. Furthermore, nurses will prefer using an RDT which
result stays readable for many months rather than a LAMP that has a limited reading time less
than one hour.
How was this test seen by health professionals? This is another question that needs more
investigation about the acceptability of this new diagnostic tool. Indeed, as reported in another
study from Australia, being able to test and treat on the same day is very valuable, and could
reduce delays for treatment, loss of follow up, recall efforts and unnecessary treatments for false
positives patients [40].
As currently there is no validated treatment of scars, CL treatment should aim at controlling the
size of these scars since smaller scars are more tolerable than the big ones.
190 | Chapter 7
To increase the chance of maintaining the size of the scar at a tolerable dimension, an early and
easy diagnosis is key. This CL RDT can be a gamechanger as it makes diagnosis more accessible
to patients in remote areas. Especially, when the RDT rk 39 for visceral leishmaniasis was found
highly accurate, cheap and simple in a recent publication from Morocco [41]. Furthermore, a
recent update of a Cochrane review assessing the available interventions for old world cutaneous
leishmaniasis found a small data targeting the prevention of CL scarring [42]. One of the choices
that could be accepted by the population in Morocco is the use of heat to accelerate the
ulcerative lesions cure (normalize epithelialization and reduce scarring), by employing a dressing
for the epithelialization stage as reported in this Cochrane review [42].
4. Recommendations and conclusion
Based on our research, we would like to propose a number of recommendations.
4.1. Recommendations for policy and practice
In the Moroccan context, we recommend that MoH policy-makers update the national
Leishmaniasis Control Guide, based on documented patients’ and population felt needs, and
develop more effective strategies that could be sustained at the community level. Nowadays,
the dermatological long-term consequences of CL have become a central theme of discussions
in rural communities in Morocco, a subject of jokes and mockery among individuals, and led to
strained community relations in regions where ethnic and racial relations were already tense.
There is clearly a strong popular demand for better CL and scar care (as well as health care in
general).
More specifically, we recommend, therefore:
More community involvement, i.e. to include citizens as individuals, families, and associations
when developing and deploying CL control policies. This includes two dimensions: responding to
their strong demand for better CL and scar care, by increasing access to diagnosis and treatment,
but also considering the acceptability of any control policy. Indeed, listening to CL patients’
voices means hearing a large poor community living in precarious sanitary and environmental
conditions. This is in line with the new Moroccan Constitution (2011) with its emphasis on the
need to respond to popular demand for better health and protection against diseases linked to
poverty. Secondly, we recommend involving the community before deploying CL control
interventions. Guidelines and protocols should be evidence-based. However, the acceptability
of those actions remains another step of validation that is too often neglected.
Discussion | 191
Consultation/involvement of the exposed population is needed to adapt each strategy to the
regional and local context.
CL control is not possible without the participation of the fully informed community. However,
this should not be used as an excuse for the departments to avoid taking responsibility (fight
against poverty, awareness, and education about possible means of prevention, professional
behaviors for CL case management on the population).
A number of preventive actions can be taken based on what we know now. However, the MoH
must convince all hygiene services in rural endemic communities of the need to carry out
permanent insect control interventions negotiated with the communities depending on their
sleeping behaviors and their cultural beliefs.
Increase access to diagnosis and care. To defend the right of all poor people in Morocco living
in remote areas affected by this disease to be detected correctly and quickly before using the
existing antimonials treatments, we recommend including the RDT we evaluated in a revised
algorithm, that would lead to CL treatment in case of a positive RDT, and to a microscopy smear
in case of a negative RDT. We recommend the Moroccan health authorities to ensure its
availability in all primary health care facilities in CL endemic areas. We note that at present,
although the rapid test for cutaneous leishmaniasis provides only a sensitivity of 68% [95% CI,
61-74], specificity = 94% [95% CI, 91-97], NPV = 64% [95% CI, 58-70], PPV = 95% [95% CI, 92-98],
it is very useful in reference or provincial laboratories in remote areas. It is also useful in the
absence or lack of trained technicians who can respond promptly to the request for microscopic
analysis of samples. RDT should be part of the algorithm for the management of patients with
suspected CL lesions. If RDT is positive, then it is advisable to rapidly start the standard
treatment. If it remains negative, a laboratory test (microscopy) is necessary at least in the
present state of knowledge. Further development is needed to optimize the sensitivity of this
RDT as explained in chapter 6.
Offer psychological support in adolescent health programs. We also recommend the integration
of the psychological follow-up of adolescents enrolled in the national programme promoting
health at school and at the university. MoH should introduce this as soon as possible in
consultation with the Ministry of Education and Higher Education. Psychological group
interventions like the cognitive behavioral therapy can reduce the loss of social support and the
social burden of CL stigma as assessed in a recent Cochrane review publication for HIV patients
[43]. Moreover, the psychological group interventions could work for other diseases and health
conditions that affect the psychological well-being.
192 | Chapter 7
We highlight that the “Framework for action on cutaneous leishmaniasis in the Eastern
Mediterranean Region 2014–2018” published by WHO17 referred briefly and only one time to
‘stigma’. No word about ‘psycho’ or ‘psychosocial’ or ‘psychology’ was found. We hope that the
future framework for action on cutaneous leishmaniasis in the EMR will finally focus on the
psychosocial burden of CL and the operational strategies for a psychological support adapted to
young affected people with CL scars.
4.2. Recommendations for research
Better tools for rapid diagnosis of CL. Though an RDT is already available and can be used, there
is much scope for optimization. Its sensitivity could possibly be increased by e.g. modification of
the sampling technique. WHO highlighted that CL RDT based on antigen detection should allow
making the difference between L. tropica and L. major species [44]. More clinical research on CL
diagnosis is definitely needed as there is not yet any standardized outcome measure.
Better tools for vector and reservoir control. As no vaccine is available, vector or reservoir
control seems the only option. Existing interventions for ZCL seem to work, even if no hard-
experimental evidence is available to inform the policy.
Our review of the evidence has shown the need for better control interventions that should be
evaluated with methodological rigor. The effectiveness of such new interventions should be
tested in a logical order, from small-scale proof of concept studies over field challenges that
measure the effect on entomological outcomes/or rodent population to finally, large-scale
intervention trials that document the impact on CL incidence [45]. Some intense advocacy will
be needed, as CL research in this area remains underfunded and neglected.
Better tools for measuring the CL burden. The overall control strategies implemented in recent
years in high CL burden countries do not bring sustainable solutions as the disease remains
present at the same level or with rising yearly incidences. Moreover, the actual indicator
assessing CL severity by using only the number of patients undergoing systemic CL treatment by
the total number of patients diagnosed is not adequate [2]. An indicator presenting the number
of patients suffering psychologically from the CL scars after 6 months to three years of follow up
could be introduced. Furthermore, areas with a CL burden could be assessed by a general
vulnerability index (a composite index including four vulnerability indices: socio-economical,
epidemiological, climatological and psychosocial components) as partially presented in one
study from Brazil and Morocco [46, 47] and more generally discussed in an integrative review
which documented the wider existing vulnerability synthetic indices [48]. WHO could lead such
a project with the aim to validate an index that would take into account the risk of CL, the
17 http://www.who.int/leishmaniasis/resources/978-92-9021-943-9/en/ Last accessed 10 april 2018
Discussion | 193
possibility to react and the perception of the psychological CL scars suffering or in contrast, the
population resilience. Concomitant coinfections with synergetic or antagonistic interaction
between different species of CL or with visceral leishmaniasis for immunocompetent patients or
the cutaneous CL forms progress to visceral forms or to maligneous disorders (cancers) are other
hidden burdens that need further multi centric research by focusing on the new or atypical
clinical forms [49–52].
5. Conclusion
In conclusion, both our epidemiological and sociological research have emphasized the
importance of the problem of cutaneous leishmaniasis in endemic areas in Morocco.
Epidemiological research has revealed that children and adolescents are the most affected age
group. Our sociological research has shown that adolescents fear this disease most. The facial
lesions or perceived disfigurement due to indelible scars can become a source of stress with an
impact on the individual psycho-social well-being. CL was found more devastating than acne and
even suicidal ideations were mentioned by some adolescents. Therefore, the psychosocial
burden generated by CL should not be neglected. So far, the psychosocial weight of this condition
has not yet sufficiently been taken into account by the health authorities.
The high number of CL scars and cases in Morocco should mobilize more public health attention
to sustain preventive measures against vectors and animal reservoirs. The clinical management
should be reviewed based on current evidence. The introduction of the RDT in its current format-
with a moderate sensitivity- seems beneficial for endemic CL areas marked with difficult
geographical access. We recommend its progressive introduction under closely monitored
operational research conditions, and advocate for further development and optimizing of this
kind of diagnostic tools
194 | Chapter 7
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Supporting information | 201
Supporting information
Chapter 2 - Supporting information | 203
Supporting information Chapter 2
Fig. S1. Maps of the administrative division of districts in Errachidia Province – Kingdom of Morocco.
204 | Chapter 2 - Supporting information
Table S1. The number of burrows before and after operations to control the density of rodent Meriones Shawi by
subdivision in the Errachidia Province
Subdivision
Rodent control 2010 Rodent control 2011 Rodent control 2012
Rodenticides
with
strychnine
poisoned
wheat used
(kg)
Mean number of
burrows per hectare Rodenticides
with
strychnine
poisoned
wheat used
(kg)
Mean number of
burrows per hectare Rodenticides
with
strychnine
poisoned
wheat used
(kg)
Mean number of
burrows per hectare
Active
burrows
before
treatment
Active
burrows
after
treatment
Area
treated
(ha)
Active
burrows
before
treatment
Active
burrows
after
treatment
Area
treated
(ha)
Active
burrows
before
treatment
Active
burrows
after
treatment
Area
treated
(ha)
Rissani 193 115100 4490 613 180 57550 2245 600 45 38365 1496 520
Erfoud Jorf 40 14565 6530 774 26 7282 3265 700 50 4855 2176 600
Goulmima
Mellab 308 192906 3260 360 220 92530 1630 340 95 64300 1086 300
0 0 0 71 120 4485 525 68 10 800 845 20 Errachidia
541 322571 14280 1818 546 161847 7665 1708 200 108320 5603 1440 Total
Chapter 2 - Supporting information | 205
Table S2. Distribution of cases and incidence of cutaneous leishmaniasis due to Leishmania major in Errachidia Province
by districts
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
N° District Area Number of Locali-ties
Number of cases before the National Program against leishmaniasis
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
1 Aarab Sebbah Gheris
Rural 4 0 0 0 1 3 11 3932 39 (992) 3620 2 (55) 4039 0 (0) 4003 0 (0)
2 Aarab Sebbah Ziz
Rural 21 0 0 0 20 46 22 10716 98 (915) 10025 21 (209) 11184 0 (0) 11083 0 (0)
3 Aghbalou N'Kerdous
Rural 19 0 0 0 2 0 1 9701 89 (917) 8722 5 (57) 9731 4 (41) 9643 0 (0)
4 Amellagou Rural 20 0 0 0 0 0 0 4981 2 (40) 4479 4 (89) 4996 0 (0) 4951 0 (0)
5 Aoufous Rural 15 0 1 1 5 7 9 12737 9 (71) 11505 12 (104) † 12777 0 (0) 12694 2 (15)
6 Arfoud Urban 19 0 0 1 20 77 61 31382 179 (570) 28964 31 (107) 31095 0 (0) 31474 0 (0)
7 Bni M'Hamed Sijelmassa
Rural 43 0 0 1 11 239 68 13083 390 (2981) 10848 21 (194) 11703 1 (9) 11596 0 (0)
8 Boudnib Urban 7 0 1 1 5 32 14ǂ 11758 28 (238) 10390 7 (67) 11094 4 (36) 11263 0 (0)
9 Chorfa M'Daghra
Rural 22 0 0 3 3 2 1 17637 2 (11) 17945 7 (39) † 19716 2 (10) 19703 1 (5)
10 Errachidia Urban 22 0 0 3 5 6 38 83711 35 (42) 75708 47 (62) † 80815 9 (11) 82061 1 (1)
11 Errissani Rural 8 0 0 0 0 0 43 3176 74 (2330) 2466 27 (1095) 2751 1 (36) 2726 0 (0)
12 Errteb Rural 8 0 1 1 1 2 3 11779 2 (17) 10590 2 (19) 11813 1 (8) 11707 0 (0)
13 Essfalat Rural 39 0 0 2 28 110 549 13822 387 (2800) 13596 14 (103) 14514 4 (28) 14383 0 (0)
14 Essifa Rural 10 0 0 0 6 11 11 8962 66 (736) 8056 6 (74) 8987 2 (22) 8906 0 (0)
206 | Chapter 2 - Supporting information
2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
N° District Area Number of Locali-ties
Number of cases before the National Program against leishmaniasis
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
Popula-tion
Number of Cases
(incidence*)
15 Ettaous Rural 25 0 0 10 94 28 6 4483 1 (22) 4385 1 (23) 4892 1 (20) 4848 0 (0)
16 Ferkla El Oulia
Rural 19 0 0 3 3 20 134 17157 628 (3660) 15427 92 (596) 17210 0 (0) 17055 0 (0)
17 Ferkla Essoufia
Rural 10 0 0 0 0 0 94 8583 364 (4241) 7717 38 (492) 8609 0 (0) 8532 2 (23)
18 Fezna Rural 5 0 0 0 0 2 8 2923 32 (1095) 4380 3 (68) 4886 0 (0) 4842 0 (0)
19 Gheris El Ouloui
Rural 7 0 0 0 0 1 7 8215 46 (560) 7385 4 (54) 8239 3 (36) 8165 0 (0)
20 Gheris Essoufli
Rural 12 0 0 0 10 391 155ǂ 6356 176 (2769) 7591 7 (92) 8469 2 (24) 8393 0 (0)
21 Goulmima Urban 10 0 0 1 1 1 5 21457 66 (308) 18193 12 (66) 19460 0 (0) 19738 0 (0)
22 Jorf Urban 9 0 0 0 0 3 8 14415 47 (326) 11502 3 (26) 12251 0 (0) 12455 0 (0)
23 Lkheng Rural 31 0 0 1 0 4 1 7264 8 (110) 7687 18 (234) † 8576 1 (12) 8499 0 (0)
24 Melaab Rural 29 0 0 0 2 68 152 15770 322 (2042) 14176 98 (691) 15815 12 (76) 15672 0 (0)
25 Moulay Ali Cherif
Urban 26 0 1 4 18 41 12 29775 58 (195) 27636 9 (33) 30869 0 (0) 29487 0 (0)
26 Ouad Naam Rural 8 1 0 3 9 155 21ǂ 4070 8 (197) 4304 7 (163) 4801 2 (42) 4759 5 (105)
27 Sidi Ali Rural 6 0 0 1 5 3 10 1439 135 (9382) 1339 1 (75) 1494 0 (0) 1651 0 (0)
28 Tadighoust Rural 28 0 0 0 1 2 3 7377 1 (14) 6631 0 (0) 7397 1 (14) 7331 0 (0)
29 Tinejdad Urban 14 0 0 0 0 1 4 13761 191 (1388) 12733 58 (456) 13817 1 (7) 14902 0 (0)
Total 496 1 4 36 250 1255 1261 400422 3483(869) 368000 557 (151) 402000 51(13) 402522 11(3)
* incidence rate per 100,000 inhabitants of all population (in affected area and not)
ǂ Natural decrease in cases of CL before starting the poisoned bait intervention
† Natural increase in cases of CL in four districts which was excluded by the poisoned bait intervention in 2010 (starting intervetion in 2012)
Chapter 3 - Supporting information | 207
Supporting information Chapter 3
Additional file 1: English translation of the self-administered questionnaire
Questionnaire about Cutaneous Leishmaniasis (April 2015)
This questionnaire is part of ongoing research about ‘Control of Cutaneous Leishmaniasis in
Morocco’ with the support of the National School of Public Health in Rabat and the Institute of
Tropical Medicine in Antwerp, Belgium. The principal aim of this study is to understand
knowledge, representations and practices of the population about Cutaneous Leishmaniasis.
Your participation in this questionnaire will help to understand your personal experience with
this disease. You will not be asked to give your name and your identity. You can decide at any
time to stop answering and withdraw from the study, or not participate. 15 minutes will be
enough to complete all the questions by selecting the appropriate answer.
Do you agree to participate in this study?
1. Yes, I agree 2. No, I do not agree
Area: 1.Tinejdad/Ferkla High school 2.My Alicherif/Rissani High school
Actual study level: 1st Year common section 2nd Year 3rd Year
Gender: 1. Man 2. Woman
Age of the participant (in years):
Name of the district where your family home is located:
Do you know a disease named cutaneous leishmaniasis? 1. Yes 2. No
Do you know a local name for this disease, if so, which?
Have you personally experienced this disease?
1. Yes 2. No 3. I do not know
If your last response is “Yes”, in which year have you been affected?
208 | Chapter 3 - Supporting information
Do you know anyone affected by this disease? 1. Yes 2. No
What is your relationship with this/these person(s)?
This disease is transmitted to humans by:
1.Dogs 2.Mosquitoes 3.Water 4.Rodents 5.Garbage 6.I do not know
Do you think girls are more exposed to get cutaneous leishmaniasis?
1.Yes 2.No 3.I do not know
Does this disease leave marks and scars (cicatrices) in the site of its occurrence?
1.Yes 2.No 3.I do not know
Is it possible to have scars (cicatrices) of this disease on the face?
1.Yes 2.No 3.I do not know
Do you think that medical treatment of marks and scars (cicatrices) of Cutaneous Leishmaniasis
exist?
1.Yes 2.No 3.I do not know
Is there any traditional remedy that is used to decrease the scars (cicatrices)?
1.Yes 2.No 3.I do not know
If your answer is “Yes” to the above, write which?
How long to those marks and scars (cicatrices) remain visible in the skin?
1. It becomes less visible in the skin within years
2. It disappears completely
3. It does not disappear and stays visible on the affected skin
Chapter 3 - Supporting information | 209
Do you use, or does your family use at home:
1. Insecticide spray
2.Bednets
3. Smoke or herbs to repel mosquitoes
4. Nothing of the above
During the summer, do you and your family frequently sleep:
1. outside the home or on the terrace
2. inside a room with closed door and windows
3. inside a room with open door and/or windows
Are you afraid for yourself and your family to be affected by cutaneous leishmaniasis in the
future?
1. Yes, I am very afraid
2. Yes, I am a little bit afraid
3. No, I am not afraid at all
Is it possible that the marks and scars (cicatrices) of Cutaneous Leishmaniasis influence the
psychological state of the person affected?
1. Yes 2. Maybe 3. No influence
Could you write a small paragraph about the probable psychological state of the person
(woman or man) affected by those scars?
Thank you very much for finishing this questionnaire
In your point of view, why did the number of CL cases in your area decrease in the last years? (You can select more than one answer)
1. Due to the hygiene campaigns
2. Due to the interventions against the wild rodents (forest)
3. Due to the interventions against the mosquitoes
4. Due to the individual acquired immunity
5. Due to the natural herd immunity of the population
6. Due to the climate change
7. Due to other factors
210 | Chapter 3 - Supporting information
Additional file 3: Sample of French translation of participants’ responses to the last question in
the questionnaire: Could you write a small paragraph about the probable psychological state of
the person (woman or man) affected by those scars?
Réponses écrites des élèves internes des lycées à propos de la dernière question du
questionnaire auto-administré.
La question : est-ce que l’apparence visuelle des cicatrices de la leishmaniose cutanée peut
influencer l’état psychologique de la personne touchée : 1-Oui il y a un effet 2-c’est probable
3-non aucun effet. Elle a été suivie par la question ouverte suivante :
Est-ce que vous pouvez écrire une petite phrase sur l’état psychologique probable de la
personne portant la cicatrice de la leishmaniose cutanée
Voici les réponses des 454 participants :
FR Répondant Féminin du lycée de Rissani Moulay ali cherif province Errachidia
MR Répondant Masculin du lycée de Rissani Moulay ali cherif province Errachidia
FT Répondant Féminin du lycée de Tinejdad Ferkla province Errachidia
MT Répondant Masculin du lycée de Tinejdad Ferkla province Errachidia
FR001 Selon mon point de vu, la maladie de la leishmaniose donne un état psychologique
compliqué chez la personne touchée et surtout chez la femme. Car les femmes ont plus peur sur
leurs visages, peur que le jeune homme qui va se présenter pour demander sa main disparait
après avoir vu ces taches.
FR002 Peut être que l’état psychologique de la personne touchée sera très compliquée et
critique.
+FR003 Selon mon point de vu, la personne touchée par cette maladie va sentir un état
psychologique faible et va perdre confiance en sa beauté
FR004 Elle laisse des marques visibles sur la personne touchée. Mais je ne sais pas si elle influence
ou non son état psychologique c’est à vous de nous le dire
FR005 la personne reste très gênée, car les cicatrices et les effets de cette maladie apparaissent
sur son corps et surtout au niveau du visage
Chapter 3 - Supporting information | 211
FR006 l’état psychologique probable de la personne touchée par ces cicatrices est très mauvais.
Absolument insupportable
+FR007 l’état psychologique de la personne touchée est qualifiée par la gêne et l’embarrât.
Surtout si la maladie se trouve dans une zone qui ne peut être cachée
+FR008 il va sentir la gêne à cause de l’apparition de ses malformations surtout au niveau du
visage
+FR 009 Elle m’influence chaque fois que je rencontre mes amies, elles regardent ma cicatrice,
cette dernière diminue ma valeur devant les gens.
+FR010 la personne touchée se dit pourquoi je suis malade par cette maladie et les autres gens
ne le sont pas et ne diminue pas de leurs personnes
+FR011 la sensation de peur et d’inquiétude de ne pas trouver un traitement à cette maladie est
ce qui affecte la personne touchée par cette maladie
+FR012 la personne touchée par la maladie de la leishmaniose souffre de plusieurs maladies
psychologiques dont les plus importantes sont la tristesse, la dépression et l’inquiétude
permanente
FR013 elle a honte à cause des effets de cette maladie et elle a une sensation d’être une
étrangère.
*FR014 selon mon point de vu je dis que cette maladie influence l’état psychologique de la
personne touchée. Car quand vous êtes touché par cette maladie il reste des effets de cette
maladie. Et le grand problème est que ces marques restent sur ton visage. Tu perds ton auto-
confiance et tu te dis j’ai perdu mon visage. Le visage est trop sensible.
FR015 vide
FR016 vide
FR017 le touché se trouve dans un état très mauvais, car cette maladie apporte la honte et il
peut ne plus être dans un bon état. Cette maladie déforme la peau sur n’importe partie touchée.
212 | Chapter 3 - Supporting information
FR018 L’état psychologique de la personne touchée par ces cicatrices est mauvaise un petit peu.
Car elles déforment la beauté (dans le cas de la femme) car la femme s’occupe beaucoup de son
apparence extérieure. Et dans le cas que ces cicatrices apparaissent au niveau du visage, la fille
a honte de monter son visage ou même les cicatrices peuvent l’empêcher de sortir de la maison
ce qui augmente sa souffrance psychologique.
FR019 La personne touchée par cette maladie a un psychisme effondré à cause de la peur de la
déformation et de l’effet que laisse la maladie quand il saura que les marques ne vont pas
disparaitre.
FR020 La personne touchée par cette maladie ne sens pas la paix de l’esprit car elle a un
sentiment de peur et de manque de réconfort.
FR 021 Je peux dire que l’état psychologique de la personne touchée homme ou femme par ces
cicatrices va conduire à des troubles psychologiques qui vont l’empêcher de sortir à la rue. Et
surtout si ces cicatrices sont sur le visage des filles.
FR 022 Il se peut que l’état psychologique de la personne touchée soit affaibli. Il se peut qu’il
sente la déformation de son visage et qu’il ait honte de sortir de la maison ou quelque chose de
semblable. Et ceci est représenté comme une maladie psychologique.
FR 037 oui la personne touchée par la maladie de la leishmaniose souffre énormément car il est
touché au niveau du visage. Comme vous le savez ce fut une fille dans l'âge des fleurs elle veut
être normale mais elle est exposée à une grande gêne et on l'oblige à mettre des crèmes tout le
temps.
FR 038 l'état psychologique de la personne touchée par leishmaniose à travers ses cicatrices est
un peu difficile surtout si les tâches trouvent sur les visages ce qui crée un sentiment de gêne car
les cicatrices ne disparaissent pas avec le temps et restent visible sur la peau
FR 039 il se peut que la personne touchée par ses cicatrices à un état psychologique détériorée
à cause de cette maladie. Mais ce n'est pas d'une manière systématique. Car plusieurs causes
peuvent creer ses lésions au niveau de son corps laissant les cicatrices et des tâches. Est-ce que
vous pouvez nous proposer le traitement des médicaments pour cette maladie est merci
beaucoup
Chapter 3 - Supporting information | 213
+FR 040 oui ses cicatrices peuvent influencer la personne touchée qui ne pourra plus supporter
de voir ces déformations sur son visage où son corps en général. Les gens peuvent se moquer de
lui et il peut paraître ses qualités de beauté. Donc il peut influencer l'état psychologique de la
personne. C'est juste mon avis
FR 041 si la maladie de la leishmaniose se trouve au niveau du visage cela peut retentir sur son
état psychologique. Il va voir que les autres ont des visages normaux alors que son visage et
cicatrisé.
FR042 états psychologiques propres de personnes touchées par ces cicatrices vont les rendent
insatisfait et tristes surtout les filles
*FR 043 cette maladie n'affecte pas que la peau mais également la psychologie des personnes
touchées et leurs proches. La question qui reste posée qu'elle est la solution pour cette maladie
FR 044 ce que je peux dire sur l'état psychologique probable de la personne touchée par ses
cicatrices c'est qu'il sent une déformation au niveau de son corps avec un sentiment de
déception à cause de cette maladie qui laisse des marques sur son visage. Parfois des personnes
touchées finissent par se détester eux-mêmes.
+FR 045 L’état Psychologique de la personne touchée par ses cicatrices l’influence car elle laisse
des traces sur sa peau visibles, comme c’est le cas chez Les filles qui ont des visages défigurés à
cause de ses cicatrices source de méprise de la part des gens.
FR 046 je peux dire que les personnes touchées par ces phénomènes quand les symptômes
apparaissent il doit aller chercher la solution à l’hôpital
FR 047 case vide
FR 048 je peux dire que les gens touchés par cette maladie de la Leishmaniose doivent partir à
l’hôpital immédiatement avant que la maladie se transmette à d’autres personnes. Il faut réaliser
des compagnes de propreté pour un environnement sain de toute maladie.
FR 049 souvent les cicatrices chez l’homme touché et surtout chez la femme touchée sont un
obstacle lors du mariage car sa cicatrice est visible, chose que ne tolère pas le fiancé.
214 | Chapter 3 - Supporting information
FR 050 il se peut que la situation de la personne touchée féminine soit psychologiquement
instable et complexée à cause de la présence des cicatrices et des tâches sur son visage ceci va
laisser un trouble psychologique à chaque fois qu'elle voit des gens-là regardant par méprise et
l'évitent dans ce cas et sera seule est complexée.
FR 051 il peut sentir qu'il porte un poids sur son corps et il va sentir la fatigue et l'épuisement et
la non satisfaction psychologique et corporelle. Il va sentir une douleur dans la zone touchée.
+FR 068 L'état psychologique de la personne touchée atteint la dépression à cause de
l'inexistence de moyens pour faire disparaître les traces de la leishmaniose. Puisque je suis une
personne touchée par cette maladie et je souffre de ses conséquences et ce qu'il existe une
solution pour guérir les cicatrices ? Merci.
FR 069 case vide
FR 070 exemple chez les femmes et les filles touchées par cette maladie qu'on peut dire que c'est
une cause est un obstacle qui les empêche de se marier.
MR 071 Il sera dans un état psychologique difficile à cause de la longueur de la maladie et de la
perte de plusieurs privilèges de bonne santé surtout lors de l’apparition de cicatrices au niveau
des visages chez les personnes de sexe féminin.
+MR 072 il sent un peu de honte et un malaise. Cette maladie influence de manière très grande
sur la psychologie du malade et également à l’égard de ses sentiments négatifs car il n’accepte
pas qu’il ait ces taches et ces cicatrices.
MR 089 L’état psychologique de la personne touchée n’est pas bonne, car cette maladie
influence beaucoup son état psychologique.
*MR 090 Il faut qu’un traitement à cette maladie soit disponible au niveau de l’ensemble des
dispensaires urbains et surtout ruraux où cette grave maladie est fréquente.
MR 091 Quand cette maladie touche la personne, elle lui fera naitre des effets psychologiques
Chapter 3 - Supporting information | 215
*MR 092 Non elle n’a pas d’effet sur la personne touchée. Il reste juste sa trace pendant une
semaine. Cette maladie n’est pas importante et elle ne crée pas de Paine car on est habituée sur
cette dernière.
MR 093 Peut être que cette maladie laisse un trouble psychologique chez la personne touchée.
C’est pour cela que la commission concernée ou le gouvernement en général doit trouver une
solution pour cette maladie et non pas le peuple
MR 094 il se sent être mépris devant ses amis et avec soi-même, ce qui le rend marginaliser dans
la société.
MR 095 la personne touchée sent la peur et la honte à cause de ces cicatrices et ceci dans sa
famille et avec ses amis. Il a également peur d’avoir des effets négatifs à cause de ces cicatrices.
MR 096 il se peut que la personne touchée par ces cicatrices sente un peu de peur lors des
premières étapes de l’apparition de cette maladie. Sauf qu’il va s’habituer sur ces cicatrices avec
le temps pour que tout ceci redevienne une chose normale.
+MR 097 pour la personne est touchée par cette maladie, il se peut qu’il y est un peu de peur
que ces cicatrices restent durant toute la vie sur sa peau et de ne pas guérir.
MR 098 la personne touchée sent la peur et la faiblesse à cause des cicatrices et elle a peur pour
sa santé
MR 099 il se peut que les cicatrices influence sont état psychologique et créer chez la personne
touchée la sensation de l’isolement des autres à cause de ces effets sur la peau et surtout s’ils
sont sur le visage ce qui rend la personne touchée très honteuse de s’intégrer dans la société. Et
ceci selon mon point de vue va influencer son état psychologique.
+MR 100 dans le cas de l’atteinte par cette maladie il y aura l’apparition d’une fièvre comme
pour toute les autres maladies, en plus qu’il va être exposé à au moins trois piqures et qu’il ne
développera pas cette maladie une deuxième fois selon ce que j’ai entendu.
MR 113 la peur de la mort
+MR 114 Il peut être exposé à la mort lente
216 | Chapter 3 - Supporting information
MR 115 Il se peut qu’elle sente un peu de faiblesse dans sa personnalité. Mais avec le temps il
commence à oublier tout cela même avec la permanence de la cicatrice sur sa peau.
+MR 116 L’état psychologique de la personne touchée peut être influencé après le traitement
car le problème est que les cicatrices ne disparaissent jamais.
+MR 117 il est inquiet et perturbé à cause de cette maladie car cette dernière influence son état
psychologique et laisse des traces sur sa peau.
*MR 118 il faut que toute personne touchée par cette maladie d’être patient et prier Dieu de
l’aider. Et de visiter le médecin régulièrement et suivre ce que dit le médecin. Pour les effets
psychologiques que peut avoir le malade est de ne pas pouvoir affronter sa société et ne pas être
capable de sortir et il va s’isoler totalement à cause de sa honte due aux cicatrices sur sa peau.
* MR 119 oui ces cicatrices influencent la santé psychique de la personne touchée et qui doit
être prudent pour se prévenir de cette maladie.
MR 120 le sentiment de la solitude et l’absence de la stabilité dans la vie quotidienne à cause du
regard négatif de la société vers patient.
*MR 121 quand la maladie de la leishmaniose touche la personne elle doit aller voir le médecin,
car c’est une maladie grave et qui influence les nerfs et l’immunité va s’effondrer. Egalement il
cause chez le patient des effets psychologiques et dermatologiques pendant une durée très
longue ce qui nécessite la visite d’un psychiatre.
+MR 122 case vide
MR 123 Cette maladie influence souvent quelques personnes car elle laisse depuis le début des
cicatrices qui conduisent la personne jusqu’au suicide
MR 124 le remède est le Coran en plus la personne peut utiliser TAMAGHOT qui se trouve à
Merzouga.
*MR 125 Il ne doit pas sentir la peine car pour toute maladie il y a un remède soit maintenant
soit dans le futur.
Chapter 3 - Supporting information | 217
+MR 141 dans la période où la personne est touché par cette maladie il sent la peur ce qui
influence son psychique.
MR 142 on retient que les rats et les moustiques sont l’origine de l’atteinte de la personne par
la leishmaniose cutanée.
MR 143 case vide
MR 144 cette maladie ne donne aucun effet sur la psychologie de la personne touchée, selon
mon point de vue
MR 145 il faut faire attention des moustiques car ils sont à l’origine de l’apparition de cette grave
maladie et aussi faire attention des rats.
MR 146 Dans le cas de l’atteinte par la leishmaniose il se peut que l’état psychologique soit
influencé de la personne touchée et ceci apparait dans la peur et les troubles psychiques
+MR 147 en ce qui concerne l’état psychologique probable est qu’il n’y a aucun effet sur l’état
psychologique même après que les cicatrices restent à cause de cette maladie car il n’y a pas de
grandes peurs
+MR 148 on peut dire que la maladie de la leishmaniose peut être guérie mais après traitement
il reste les cicatrices pour toujours et il faut acheter un traitement “cicatrisol*”
MR 149 dans le cas de la présence des cicatrices sur le visage de la personne touché il y aura bien
évidement un effet psychologique et la personne va sentir la honte.
*MR 150 cette personne touchée n’a pas le pouvoir de dire qu’il est atteint par cette maladie
par peur que les gens s’éloignent de lui.
MR 151 si la personne est touché au niveau du visage, il se peut que la maladie affecte son état
psychique avec l’apparition de la honte de montrer son visage et surtout devant les filles si la
personne touchée est de sexe masculin et il va sentir également une laideur ce qui influence son
état psychologique négativement.
218 | Chapter 3 - Supporting information
+MR 152 pour toute maladie il y a un traitement
MR 174 il faut soigner rapidement cette maladie pour qu’il n’y ai pas d’effet sur l’état
psychologique de la personne touchée
MR 175 cette maladie ne donne aucun effet sur l’état psychologique car ce n’est pas une chose
essentielle. On est habitué à voir cette maladie. Et il faut que le gouvernement trouve une
solution à cette maladie.
FT176 on peut dire que l’état psychologique de la personne touché par ces cicatrices est un très
mauvais état et surtout chez les filles car cela conduit à la diminution de leurs beautés.
+FT177 quand la personne voit les cicatrices il aura un état psychologique lamentable surtout il
va plonger dans la souffrance quand il se rend compte qu’il n’y a pas de traitement.
+FT178 on peut dire que l’état psychologique de la personne touché par ces cicatrices est trop
difficile et surtout chez les filles car cela va faire diminuer leurs beautés
FT179 on peut dire que la personne touché par cette maladie souffre de cette dernière dans tous
les temps, par exemple vous ne voulez pas qu’une autre personne soit touchée par cette maladie
car elle fait souffrir beaucoup.
FT180 son état psychologique est affecté un peu car il a peur de contaminer ses proches et sa
famille
+FT181 l’état psychologique de la personne touché par ces cicatrices est mauvais car il conduit à
l’infériorité chez le porteur de ces cicatrices.
FT182 la réponse sera que la personne ne va absolument pas supporter cela car il conduit à une
perte de performance dans les études et à la démotivation.
FT183 l’état psychologique probable de la personne touché par ces cicatrices sera dangereux ou
bien cela ne va absolument pas l’affecté
*FT184 je prie Dieu qu’il guéri toute personne touché par cette maladie. Amen.
Chapter 3 - Supporting information | 219
FT185 il se peut que l’aspect des cicatrices et les taches de la leishmaniose cutanée qu’elles
influencent l’état psychologique et surtout celui des filles. Car elles vont sentir l’infériorité et la
peur qu’elles apparaissent sur cet aspect devant leurs amis. Elles vont s’auto-détester quand
elles vont se voir dans le miroir à cause des cicatrices et des taches de cette maladie.
FT186 il se peut que l’apparence des cicatrices et des taches de la leishmaniose cutanée qu’elles
influencent l’état psychologique de la personne touchée. Elle va se sentir trop faible pour
paraitre devant les amies avec ces cicatrices et surtout si ces taches sont sur le visage. Car la
personne pense que les gens sont entrain de jeter un regard de méprise. La personne touchée
va se dégouter en se voyant dans le miroir.
FT187 au niveau du visage et surtout chez certaines filles, les cicatrices peuvent représenter un
problème psychologique à cause de l’aspect visuel horrible et la longue période que cela prend
pour commencer à disparaitre de la peau.
FT194 surtout chez les filles quand la maladie laisse une tache sur le visage par exemple, et la
fille va penser que c’est dangereux sur son niveau de beauté ce qui va influencer son état
psychologique. Surtout dans notre société traditionnelle qui n’est absolument pas clémente à
l’égard de ceux qui ont des taches sur le visage car ils pensent que c’est héréditaire.
+FT195 oui les cicatrices de la leishmaniose vont laisser chez l’homme un état psychologique très
grave. Et surtout chez les filles touchées au niveau du visage. Les cicatrices te rendent très
honteux devant les autres. Y a-t-il un traitement pour les cicatrices ? J’aimerai bien que la
réponse sera oui il y a un traitement.
*FT196 oui cette maladie de la leishmaniose influence l’état psychologique de la personne
touchée car lors de l’atteinte par cette maladie tu vas sentir par exemple que les gens sont en
train de s’éloigner de vous et de vous éviter. Et quand la personne touchée par cette maladie
voit les cicatrices sur sa propre peau au niveau des mains et du visage elle a un sentiment de
peur et de dépression. Peur que cette maladie l’influence plus et devienne mortelle.
*FT197 case vide
*FT198 je demande à Dieu qu’il guéri toute personne touchée par cette maladie dans les plus
brèves délais et qu’il épargne ma famille et tous les musulmans
220 | Chapter 3 - Supporting information
+FT199 pour moi je ne souffre d’aucun problème psychologique à cause de cette maladie même
si j’ai une cicatrice mais je n’ai pas souffert à cause d’elle.
FT207 selon ce que j’ai pu constater auprès des personnes touchées que je connaisse, est qu’elles
sont influencées par ces cicatrices. Surtout chez les filles qui ont une atteinte au niveau du visage
ce qui leurs fait perdre leurs beautés. Et cela les poussent à s’isoler et de ne vouloir entendre
aucune remarque ou rumeur sur sa beauté.
FT208 je prie pour la personne touchée par ces cicatrices qu’elle guérisse. Qu’elle utilise des
traitements médicaux ou traditionnelles c’est pareil pour moi, il faut juste qu’il guérisse et de ne
pas développer un problème psychologique.
FT209 Je prie Dieu qu’il guérisse vite les personnes touchées par ces cicatrices et qu’il éloigne de
nous cette maladie de la leishmaniose cutanée.
FT210 il doit suivre quelques injections et les conseils du médecin pour diminuer l’effet de ces
cicatrices
FT211 selon mon point de vue, il se peut qu’il y soit une influence sur l’état psychologique de la
personne touchée. Mais cela dépend de l’évaluation donnée par l’infirmier et l’ampleur de la
dangerosité de la maladie.
FT212 selon ce que j’ai vu et j’ai entendu chez la plupart des filles touchées par cette maladie,
elles sentent qu’elles ont une malédiction et ces cicatrices font obstacle devant leurs beautés.
FT213 Oui il est possible que les cicatrices influencent l’état psychologique de la personne
touchée et surtout si la maladie guérie et laisse des séquelles sur le visage plus précisément.
FT214 Son état psychologique sera très affecté du fait que les cicatrices vont rester sur la peau
surtout au niveau du visage des filles
FT215 je peux dire que l’état psychologique peut être affecté chez les personnes touchées par
cette maladie. Ces taches et cicatrices peuvent représenter un obstacle pour elles. Si les
malformations se situent sur les parties extérieures visibles, ces personnes vont sentir de
l’infériorité et un déséquilibre dans leurs beautés ce qui va menacer l’état psychologique.
Chapter 3 - Supporting information | 221
FT264 la personne touchée par ces cicatrices est probable qu’elle a un état psychologique
perturbé à cause de son sentiment permanent d’isolement et d’anxiété par rapport aux autres,
ce qui conduit obligatoirement vers la dépression.
+FT265 tout à fait, les séquelles laissées par la leishmaniose influencent négativement l’état de
la personne touchée. Il y aura un complexe psychologique et elle va avoir honte de paraitre
devant ses amis car c’est une marque de honte et de méprise.
FT266 on souhaite la guérison de cette maladie et que Dieu avec sa puissance le guérisse.
FT283 toujours la personne sent la peur et la honte surtout si la maladie est localisée sur le
visage. Il va penser qu’il est isolé et qu’il va sentir l’anxiété.
+FT284 on vous demande de pouvoir éviter cette maladie, car plusieurs personnes n’avaient pas
les moyens pour acheter un traitement pour cette maladie dangereuse. Et je souhaite la guérison
à tous ceux qui en souffrent.
FT285 quand la personne est touchée par cette maladie il doit se protéger de plusieurs autres
maladies qui seront causées par cette première maladie.
FT286 quand la personne est touchée par cette maladie il voit qu’il est devenu défiguré dans son
corps à cause de la présence de ces marques cicatricielles sur sa peau, ce qui lui pousse à sentir
la honte et la panique. Et je suis pour la réalisation d’une compagne de sensibilisation contre
cette maladie.
FT287 la leishmaniose cutanée influence l’état psychologique de la personne touchée car elle lui
pousse à avoir peur et même à la mort. C’est pour cela qu’il faut se protéger et protéger nos
familles. Et en cas d’apparition de cette maladie il faut aller voir le médecin spécialiste.
FT288 il est probable que la personne touchée par cette maladie a un état psychologique
perturbé.
222 | Chapter 3 - Supporting information
FT289 la leishmaniose cutanée influence l’état psychologique et conduit à la mort. Et pour
diminuer l’effet de cette maladie contagieuse il faut prévoir assez de traitements médicaux ou
traditionnels.
FT290 la maladie de la leishmaniose est un phénomène dangereux et très répondu surtout dans
les villes. Et cette maladie influence l’état psychologique de la personne touchée car elle conduit
à la peur. Il faut réaliser des compagnes de sensibilisation sur l’intérêt de l’hygiène. Et on
souhaite la guérison aux personnes atteintes.
FT291 il est probable que la personne touchée par cette maladie a un état psychologique
perturbé.
FT292 l’état psychologique de la personne touché est marqué par le fait qu’il devient paniqué
avec une grande peur, et il n’aime plus rencontrer les gens car ils commencent à l’éviter et ceci
le rend triste.
FT293 quand la personne est énervée ou ignorante elle peut avoir des problèmes
psychologiques, on demande à Dieu le pardon et la santé.
FT294 la leishmaniose cutanée influence l’état psychologique et conduit à la peur. La peur même
de la mort. D’où il faut organiser des compagnes de sensibilisation sur l’importance de l’hygiène
pour lutter contre les rats sauvages et les moustiques. Et il faut qu’on se protège de la
leishmaniose cutanée et protéger nos familles. Et je souhaite la guérison rapide aux personnes
touchées par cette maladie.
FT295 la personne touchée aura un état psychologique très effondré à cause du milieu où il vit
et le regard de la société à son égard d’autre part. Il va sentir la dépression et il ne va plus vouloir
sortir avec les amis et les proches et il va s’auto-emprisonner dans la maison.
MT337 en regard que la maladie de la leishmaniose cutanée est difficilement guérissable et laisse
des cicatrices et des taches permanentes sur le corps et qui influencent l’apparence normale
connue de la personne. Ainsi cette maladie provoque beaucoup de problèmes psychologiques
car elle diminue la beauté de son apparence extérieure et cause l’irritation chez lui car la société
n’aperçoit que les défauts et pense que la personne touchée est une personne négligente qui
est non propre et qui ne prend pas soins de son état corporel.
Chapter 3 - Supporting information | 223
+MT338 on peut dire que la lutte contre cette maladie nécessite l’utilisation des insecticides et
les compagnes de chirurgie esthétique.
MT339 il se peut que ces cicatrices causent de nombreuses maladies psychologiques comme la
dépression
MT340 il se peut que ces cicatrices influencent l’état psychologique des personnes touchées par
cette maladie et conduit à des perturbations psychologiques multiples dans la vie quotidienne
et également sentimentale.
MT358 la personne touchée va souffrir et va avoir une crise psychologique surtout si les cicatrices
de cette maladie restent sur le visage par exemple.
MT359 l’impuissance de dormir et ne pas cesser de penser à sa maladie. Et la peur d’être touché
par cette dernière.
MT360 il est probable qu’il sera atteint par un peu de peur et de honte devant ses amis. Et il ne
va pas pouvoir partager les repas avec sa famille
*MT361 Je peux dire que cette maladie n’est pas fréquente dans la société et il y a plusieurs
sociétés où cette maladie n’existe pas car il n’y a pas la présence de certains animaux porteurs
de cette maladie et qui le transmettent à l’humain.
MT362 Il se peut que les cicatrices l’influencent si elles sont présentes dans des zones sensibles
et découvertes et qu’elles ne guérissent pas par les traitements médicaux modernes. On
demande à Dieu le pardon et la santé.
MT363 l’état psychologique de cette personne est un peu difficile. Mais il se peut qu’il y ait une
personne qui peut développer des troubles psychologiques et une autre qui reste normale.
+MT364 la personne touchée par cette maladie peut souffrir s’elle est touchée dans une zone
sensible comme au niveau du visage ce qui le rend embarrassé devant les amis et les collègues
et la société en gros ce qui le pousse à se ralentir dans ses études et son travail.
MT376 la vie devient dure à cause de l’état psychologique de la personne touchée. Les cicatrices
influencent sur sa vie psychologique. Heureusement que cette maladie a commencé à diminuer
par rapport auparavant.
224 | Chapter 3 - Supporting information
MT395 lors de l’atteinte par cette maladie il faut se rendre à l’hôpital pour faire la vaccination.
Car cette maladie est très dangereuse et laisse place à des cicatrices sur les zones touchées de la
peau. Et vive le Roi.
MT396 Pour la femme, ces cicatrices va lui créer un obstacle avec ces amies et son travail et
d’autres choses comme ça.
*MT397 Je souhaite aux personnes touchées par cette maladie la guérison rapide. Il faut faire
des compagnes de propreté et de lutte contre les rats sauvages (de la forêt). J’espère que je ne
serai pas touché ni moi ni les autres par cette maladie qui est dangereuse et qui provoque
beaucoup d’autres maladies.
*MT398 je pense que cette maladie est très forte et elle fait beaucoup de problèmes dans le
monde. Je veux dire tout simplement que je veux souhaiter à l’homme qui a cette maladie
(leishmaniose) la grande santé et merci à tous.
MT413 Oui si un parmi les jeunes personnes est touché par cette maladie au niveau du visage, il
sera incapable d’affronter la société par peur de la discrimination sociale et la méprise et par
peur d’autres facteurs qui rendent sa psychologie épuisée.
MT414 je ne pense pas pouvoir connaitre l’état psychologique de la personne touchée par ces
cicatrices
*MT451 la personne touchée va chercher le médicament idéal et les médecins doivent chercher
les moyens pour combattre cette maladie
+MT452 l’état psychologique est marquée par la complexité psychologique car il n’y a pas de
traitement pour ces cicatrices et ils vont rester pour toujours. Et il voudra juste comment faire
disparaitre ces cicatrices.
MT453 case vide
*MT454 moi je ne connais pas cette maladie pour pouvoir parler à propos de cela. Je m’excuse
d’être ignorant pour cette maladie. « Tout ce que je sais est que je ne sais rien ».
225 | Chapter 4 - Supporting information
Supporting information Chapter 4
Consolidated criteria for reporting qualitative studies (COREQ): 32-item checklist Developed from: Tong A, Sainsbury P, Craig J. Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. International Journal for Quality in HealthCare.;19(6):349–57. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17872937 No. Item Guide questions/description Reported on Page #
Domain 1: Research team and reflexivity
Personal Characteristics
1. Interviewer/facilitator Which author/s conducted the interview or focus group? Issam Bennis
2. Credentials What were the researcher’s credentials? E.g. PhD, MD Issam Bennis - MD, MPH, PhD candidate Loubna Belaid - anthropo sociologist Vincent De Brouwere - MD PhD Professor Hind Filali psychosociologist Professor Hamid Sahibi - Veterinary doctor PhD Professor Marleen Boelaert - MD PhD Professor
3. Occupation What was their occupation at the time of the study? Researcher at the Institute of Tropical Medicine Antwerp and the National school of public Health Rabat
4. Gender Was the researcher male or female? Male reported in Methods
226 | Chapter 4 - Supporting information
No. Item Guide questions/description Reported on Page #
5. Experience and training
What experience or training did the researcher have? Methods - The researcher has a certificated in Qualitative Mixed Methods in international health from the Institute of Tropical Medicine in Antwerp in 2015
Relationship with participants
6. Relationship established
Was a relationship established prior to study commencement? No
7. Participant knowledge of the interviewer
What did the participants know about the researcher? e.g. personal goals, reasons for doing the research
Participant information sheet and Consent Form
8. Interviewer characteristics
What characteristics were reported about the interviewer/facilitator? e.g. Bias, assumptions, reasons and interests in the research topic
Methods
Domain 2: study design
Theoretical framework
9. Methodological orientation and Theory
What methodological orientation was stated to underpin the study? e.g. grounded theory, discourse analysis, ethnography, phenomenology, content analysis
Methods
Participant selection
10. Sampling How were participants selected? e.g. purposive, convenience, consecutive, snowball
Methods
11. Method of approach How were participants approached? e.g. face-to-face, telephone, mail, email
Methods
12. Sample size How many participants were in the study? Methods
Chapter 4 - Supporting information | 227
No. Item Guide questions/description Reported on Page #
13. Non-participation How many people refused to participate or dropped out? Reasons?
Methods
Setting
14. Setting of data collection
Where was the data collected? e.g. home, clinic, workplace
Methods
15. Presence of nonparticipants
Was anyone else present besides the participants and researchers?
Methods
16. Description of sample What are the important characteristics of the sample? e.g. demographic data, date
Methods
Data collection
17. Interview guide Were questions, prompts, guides provided by the authors? Was it pilot tested?
Methods
18. Repeat interviews Were repeat inter views carried out? If yes, how many? No
19. Audio/visual recording
Did the research use audio or visual recording to collect the data? Methods
20. Field notes Were field notes made during and/or after the interview or focus group?
Methods
21. Duration What was the duration of the inter views or focus group? Methods
22. Data saturation Was data saturation discussed? Methods
23. Transcripts returned Were transcripts returned to participants for comment and/or correction?
Methods
228 | Chapter 4 - Supporting information
No. Item Guide questions/description Reported on Page #
Domain 3: analysis and findings
Data analysis
24. Number of data coders
How many data coders coded the data? Methods
25. Description of the coding tree
Did authors provide a description of the coding tree? Methods
26. Derivation of themes Were themes identified in advance or derived from the data? Methods
27. Software What software, if applicable, was used to manage the data? Methods
28. Participant checking Did participants provide feedback on the findings? Methods
Reporting
29. Quotations presented Were participant quotations presented to illustrate the themes/findings? Was each quotation identified? e.g. participant number
Results
30. Data and findings consistent
Was there consistency between the data presented and the findings?
Discussion
31. Clarity of major themes
Were major themes clearly presented in the findings? Results
32. Clarity of minor themes
Is there a description of diverse cases or discussion of minor themes?
Results
Chapter 4 - Supporting information | 229
Supporting information: Translated FGD topic guide
This Focus Group is a part of a study for preparation of a PhD titled "Control of cutaneous
leishmaniasis in Morocco" at the National School of Public Health in Rabat and the Institute of
Tropical Medicine in Antwerp.
The main objectives of this study are to identify the knowledge, attitudes, perceptions and
practices of the population around cutaneous leishmaniasis.
I request your consent to participate in this discussion group that will help us to understand your
experiences related to this disease. The anonymity and freedom of expression is guaranteed.
You can decide at any time to stop the discussion and to withdraw, or else not to participate in
a given theme. 60 minutes will be sufficient to complete this entire discussion.
Familiarity with cutaneous leishmaniasis
The knowledge of the existence of CL in this geographical area
How can we have scars on the skin?
Do you know a disease called leishmaniasis? Do you use other names for this disease?
How long this disease exists in your community? Is this a new disease that appeared recently?
The presence of family antecedents
Did you suffer from this disease before?
Do you know someone who has suffered from this disease in your surroundings?
Is this disease common in this village? Who are the people most affected?
CL Knowledge
How we can recognize this disease? How do you know you are sick with it?
How is this disease transmitted to humans?
On what part of the body do we find lesions? May we have several lesions at once?
What do you think about the origin of these lesions?
How can we avoid this disease? May we develop several times this disease even after healing?
How long can this disease last before healing?
Therapeutic possibilities followed
How can we heal? Is there a cure?
What kind of treatment exists? Where we can find it?
What are the traditional treatments that can be used?
How much does it cost to get treatment?
230 | Chapter 4 - Supporting information
Perception of this disease
The disease severity
Is this a serious condition? Is it fatal? Are we afraid for our children to have this disease? What
is the impact on daily life?
Is it necessary to treat? Would it be better to prevent? How?
The aesthetic appearance of the lesion or scar
Did this disease leave scars? How did they appear? On what body parts?
How can we make them disappear?
The isolation and stigma
What are the activities that we cannot do when we are affected by this disease?
How we behave in general with those affected by this disease?
(Working together, living together, taking common meal together, walk with, let the children
play with the affected person, can cook for your family, possibility of marriage with him or her).
Preventive practices
What are the preventive measures you take personally to avoid getting sick? (Mosquito bed-
nets, insecticides ...)
What measures does the community take to prevent disease in the village? (Waste collection,
sanitation ...)
Service use (Question for formal health users)
Do you know some traditional healers in the area? Have you visited them before?
Even if you have never been to a healer, what do you know about that? Do you know someone
who’s going? Why and for what health problems?
Reasons for not using health facilities for care (Question for Traditional users)
What are reasons for visiting traditional healer rather than health providers?
For what health problem healers are effective? For what disease?
Thank you
Chapter 4 - Supporting information | 231
S3_File.pdf: Original participant Information sheet (In Arabic)
بطاقة معلومات للمواطنين المشاركين في مجموعة التركيز
لداء الليشمانيا الجلدية في المغربالتمثيالت االجتماعية
الدكتور عصام بنيسالباحث الرئيسي:
إقليم الرشيدية / تنغيرالمنطقة: وزارة الصحة؛ المنظمة:
معهد الطب االستوائي، انتويرب و المدرسة الوطنية للصحة العمومية في الرباطالمتعهد:
ة العمومية في الرباط، التابعة لوزارة الصحةمرحبا، اسمي عصام بنيس، أنا باحث بالمدرسة الوطنية للصح .
أدعوكم للمشاركة في المائدة المستديرة التي ستتطلب تقريبا مدة ساعة ونصف، مع سبعة أشخاص آخرين للحديث عن مرض
الجلد
في لقد أصاب هذا المرض على مدى السنوات الخمس الماضية العديد من األشخاص . الذي يعرف باسم داء الليشمانيا
.المنطقة
إن مشاركتك يجب أن تكون طوعية تماما، ولن يتم دفع أي مقابل مادي ألجلها. لك كامل الحرية لرفض المشاركة
لشرح أفضل، ألتمس منك االستماع إلى المعلومات المتواجدة بهذه المذكرة والتي ستحتفظ بها في حالة ما إذا كنت ترغب في
طرح
اتالمزيد من األسئلة أو طلب توضيح .
غرض ووصف الدراسة
.هذه الدراسة تستهدف فهم أحسن لوجهات نظر المواطنين وطريقة تعايشهم مع مرض الليشمانيا الجلدية
مشاركا ومشاركة من عشر جماعات مختلفة بإقليمي الرشيدية وتنغير 150في هذه الدراسة هناك أكثر من .
دا في فهمهااألسئلة التي سيتم طرحها لها طابع عام ولن يتطلب مجهو .
ألتمس موافقتكم على المشاركة في احدى مجموعات التركيز مع احترام الجنس الذكور على حدة واإلناث على حدة. والذين
سيتم
.اختيارهم بنفس الطريقة وفي نفس المكان
(. ( هذه المحادثة ستدوم لمدة تصل الى الساعة وستجرى بالبناية المجاورة للمركز الصحي
الدراسة طريقة إجراء
إذا كنت موافقا على المشاركة في هذه الدراسة، سوف يطلب منك أن تذهب إلى تلك القاعة في المبنى المجاور. سنبدأ الحصة
بعد
الظهيرة على الساعة وسيتم تسجيل الحوار بواسطة الكاميرا أو آلة تسجيل الصوت. كل التسجيالت ستستخدم من اجل تذكر
اإلجابات
حها بعد ذلكمن طرفي وسيتم مس .
.لن يكون هناك أي عرض للشريط المسجل اينما كان
نضمن لك حرية التعبير وتسجيل كل ما تدلون به من األجوبة بطريقة مجهولة دون ذكر اسمكم نهائيا. لديك الحق في التوقف
عن
.المشاركة مؤقتا أو بشكل دائم دون إشعار
على نقط النقاش لديك أيضا الحق في عدم اإلجابة بشكل كلي أو جزئي .
.لن يتم جمع أي معلومات شخصية عنك. لن يطلب منك الحقا أي تحليل مخبري أو عينة
232 | Chapter 4 - Supporting information
الفوائد
هذه هي واحدة من أولى الدراسات بشأن التصورات والمعارف والمواقف والممارسات من طرف السكان الذين يعيشون في
المنطقة
النتائج المنتظرة ستكون لها فوائد على الصحة العامة للمجتمع المتضررة من داء الليشمانيا الجلدية في المغرب. .
لجنة األخالقيات
تمت الموافقة على إجراء هذه الدراسة من قبل لجنة األخالقيات بمعهد الطب االستوائي في أنتورب. ولجنة األخالقيات
.بالرباط
ة العمومية في الرباط، وقسم علم األوبئة باإلضافة إلى تراخيص من وزارة الصحة ممثلة في المدرسة الوطنية للصح
ومحاربة
.األمراض في الرباط
المشاركة الطوعية
.يجب أن تكون مشاركتك في هذه الدراسة تطوعية تماما. إنه اختيارك إذا كنت ترغب في المشاركة أم ال
.لديك أيضا الحق في التوقف عن المشاركة في أي وقت، دون حاجة لشرح السبب
لة حول مجموعة التركيز؟هل لديك أسئ
هل أنت على استعداد للمشاركة؟
.سوف يتم تسجيل الموافقة الشفهية الخاصة بك في بداية الجلسة
إذا كانت لديك أسئلة أخرى حول البحث أو في حال كنت تعتقد أنك عانيت من نتائج هذه الدراسة، يمكنك االتصال اآلن، أثناء
أو بعد
للدراسة: عصام بنيس هذا اللقاء بالباحث الرئيسي
الرباط المغرب 6329العنوان: المدرسة الوطنية للصحة العمومية، شارع المفضل الشرقاوي، مدينة العرفان. صندوق البريد
Chapter 5 - Supporting information | 233
Supporting information Chapter 5
Additional File 1 Logbook, search history, excluded articles, included articles and Data
extraction labels of the main conceptual categories
Log book:
Strategy search performed in the end of September 2016 and updated in first September 2017
ID
Database Search terms
Number
of hits
Without
intra
duplication
R01 LILACS Leish* AND Estigma* 10
323
R02 LILACS Leish* AND Stigma* 45
R03 LILACS Leish* AND Psychol* 56
R04 LILACS Leish* AND Psicol* 46
R05 LILACS Leish* AND scar* 35
R06 LILACS Leish* AND Cicatri* 221
R07 Science
Direct
Leishm*AND Stigma* 801
801
R08 Cochrane
Library
Leish* AND Psych* 03
07
R09 Cochrane
Library
Leish* AND scar* 01
R10 Cochrane
Library
Leishm*AND Stigma* 03
R11 Cochrane
Library
Cicatri* AND Stigma* 03
R12 POPLINE Leish* AND Scar* 10
74
R13 POPLINE Leish* AND stigma* 06
R14 POPLINE Leish* AND Psych* 07
R15 POPLINE Stigma* AND Scar* 54
R16 PsycINFO Leishmaniasis 42
234 | Chapter 5 - Supporting information
R17 PsycINFO Skin Disorders OR Wounds AND Any Field:
Stigma
85
627
R18 PsycINFO Measurement AND Any Field: stigma 90
R19 PsycINFO Measurement AND Any Field: Wounds 64
R20 PsycINFO wounds AND Index Terms: Life Changes OR
Life Satisfaction OR Lifestyle Changes OR
Measurement OR Mental Health OR Positive
Psychology OR Quality of Life OR Wellbeing
OR Work-Life Balance
412
R21 PubMed Search query listed within the article 301
301
R22 Web of
Knowledge
Search query listed within the article 282 282
R23 Global
Health
((Leishmaniasis OR Dermal Leishmaniasis OR
Cutaneous Leishmaniasis OR
Mucocutaneous Leishmaniasis OR Diffuse
Cutaneous Leishmaniasis NOT Visceral
Leishmaniasis) AND (((Stigma) OR (Public
stigma) OR (Social Stigma) OR (community
stigma) OR (Enacted stigma) OR (Self-stigma)
OR (Self stigma) OR (Experienced stigma) OR
(Perceived stigma) OR (imagined stigma) OR
(Anticipated stigma) OR (Felt stigma) OR
(Self-report) OR (internalized stigma) OR
(Health related stigma) OR (Gender Identity )
OR (Quality of Life) OR (Perception) OR
(Rejection) OR (Discrimination)) OR ((Social
problems) OR (Public opinion) OR (Social
discrimination ) OR (Social isolation) OR
(Social exclusion) OR (Social distance) OR
(Stereotyping) OR (Social perception) OR
(Social conditions) OR (Social adjustment) OR
(Social behavior) OR (Social behaviour) OR
(Social behavior disorders) OR (Social
environment) OR (Social support) OR (Social
marketing) OR (Cost of illness)))
70 70
Chapter 5 - Supporting information | 235
Search history and chart flow text description
Step 1- Identification of studies in 08 databases: sold with 2485 references, as shown in the table
above.
Step2- Identification of duplicates: From the initial references treated together, we found 260
duplications for all 08 databases.
Step 3- Screening results: For the 2225 references screened for title or title and abstract, we
excluded 2154 and kept 71.
Step 4- Articles included from hand searching sold with 07 additional references.
Step 5- After reading the full text of the 78 references defined in step 3 and, we excluded 63
references due to not corresponding to our inclusion criteria.
Step 6- 15 Articles included for synthesis after step 5
Step 7- Synthesis of the definitely included articles reported within the flow chart of this study
Excluded articles after full reading text – Final Results 31th August 2017 (n=63)
No or too limited regarding CL stigma or CL psychosocial burden (n=33)
Amin, T. T., et al. (2012). "Public awareness and attitudes towards cutaneous leishmaniasis in an
endemic region in Saudi Arabia." Journal of the European Academy of Dermatology and
Venereology 26(12): 1544-1551.
Bailey, M. S., et al. (2012). "Outbreak of zoonotic cutaneous leishmaniasis with local
dissemination in Balkh, Afghanistan." J R Army Med Corps 158(3): 225-228.
Borghi, S. M., et al. (2017). "Leishmania infection: painful or painless?" Parasitol Res 116(2): 465-
475.
Burki, T. (2009). "Neglected people and a neglected disease." The Lancet Infectious Diseases 9(5):
280.
Carrillo-Bonilla, L. M., et al. (2014). "Study of knowledge, attitudes, and practices related to
leishmaniasis: evidence of government neglect in the Colombian Darien." Cadernos De Saude
Publica 30(10): 2134-2144.
Chaves, L. F., et al. (2008). "Social Exclusion Modifies Climate and Deforestation Impacts on a
Vector-Borne Disease." Plos Neglected Tropical Diseases 2(2): 8.
236 | Chapter 5 - Supporting information
Costa, J. M., et al. (1998). "[Comparative study of American tegumentary leishmaniasis between
childhood and teenagers from the endemic areas Buriticupu, Maranhao and Corte de Pedra,
Bahia, Brazil]." Rev Soc Bras Med Trop 31(3): 279-288.
dos Reis, D. C., et al. (2006). "Health education and social representation: an experience with the
control of tegumentary leishmaniasis in an endemic area in Minas Gerais, Brazil." Cad Saude
Publica 22(11): 2301-2310.
Elsaie, Mohamed L., and Shady M. Ibrahim. "The effect of pulsed dye laser on cutaneous
leishmaniasis and its impact on the dermatology life quality index." Journal of Cosmetic and Laser
Therapy just-accepted (2017).
Guevara, Baílde García. "Aporte de la etnografía en el conocimiento de los códigos
socioculturales de la leishmaniasis cutánea localizada en un programa de educación para la
salud, en Venezuela." Caderno de Saúde Pública 23 (2007): 83.
González, U., et al. (2009) Interventions for American cutaneous and mucocutaneous
leishmaniasis. Cochrane Database of Systematic Reviews DOI:
10.1002/14651858.CD004834.pub2
González, U., et al. (2008) Interventions for Old World cutaneous leishmaniasis. Cochrane
Database of Systematic Reviews DOI: 10.1002/14651858.CD005067.pub3
Haouas, N. (2016). "Estimations of cutaneous leishmaniasis burden: a constant challenge."
Lancet Infect Dis 16(5): 515-516.
Hejazi, S. H., et al. (2010). "Evaluation of knowledge, attitude and performance of the mothers
of children affected by cutaneous leishmaniasis." Infectious Diseases: Research and Treatment
3: 35-40.
Kebede, N., et al. (2016). "Community knowledge, attitude and practice towards cutaneous
leishmaniasis endemic area Ochello, Gamo Gofa Zone, South Ethiopia." Asian Pacific Journal of
Tropical Biomedicine 6(7): 562-567.
Mathers, C. D., et al. (2007). "Measuring the burden of neglected tropical diseases: the global
burden of disease framework." PLoS Negl Trop Dis 1(2): e114.
Moreira Rda, C., et al. (2002). "[knowledge level about of American tegumentary leishmaniasis
(ATL) and use of alternative therapies in an endemic area in the Amazon Region in the State of
Maranhao, Brazil]." Cad Saude Publica 18(1): 187-195.
Murray, C. J., et al. (2015). "Global, regional, and national disability-adjusted life years (DALYs)
for 306 diseases and injuries and healthy life expectancy (HALE) for 188 countries, 1990-2013:
quantifying the epidemiological transition." Lancet 386(10009): 2145-2191.
Chapter 5 - Supporting information | 237
Nandha, B., et al. (2014). "Cutaneous leishmaniasis: Knowledge, attitude and practices of the
inhabitants of the Kani forest tribal settlements of Tiruvananthapuram district, Kerala, India."
Health Education Research 29(6): 1049-1057.
Pimenta, Denise Nacif, Anita Leandro, and Virgínia Torres Schall. "A estética do grotesco e a
produção audiovisual para a educação em saúde: segregação ou empatia? O caso das
leishmanioses no Brasil." (2007)
Qureshi, N. A., et al. (2016). "Prevalence of Leishmania tropica in school boys of khyber agency,
FATA near Pak-Afghan border." Acta Trop 164: 90-94.
Ramdas, Sahienshadebie. "Cruel disease, cruel medicine: self-treatment of cutaneous
leishmaniasis with harmful chemical substances in Suriname." Social Science & Medicine 75.6
(2012): 1097-1105.
Ranawaka, Ranthilaka R., and Hema S. Weerakoon. "The Quality of Life of 146 Sri Lankan Patients
with Cutaneous Leishmaniasis." Transactions of the Royal Society of Tropical Medicine and
Hygiene 97.380 (2003).
Reithinger, R., et al. (2010). "Risk Factors for Anthroponotic Cutaneous Leishmaniasis at the
Household Level in Kabul, Afghanistan." Plos Neglected Tropical Diseases 4(3): 8.
Saberi, S., et al. (2012). "The knowledge, attitude, and prevention practices of students regarding
cutaneous leishmaniasis in the hyperendemic region of the Shahid Babaie Airbase." Vector Borne
Zoonotic Dis 12(4): 306-309.
Sarkari B, Qasem A, Shafaf MR. Knowledge, attitude, and practices related to cutaneous
leishmaniasis in an endemic focus of cutaneous leishmaniasis, Southern Iran. Asian Pac J Trop
Biomed. 2014;4(7):566–9.
Santos, J. B., et al. (2000). "[Socioeconomic factors and attitudes towards household prevention
of American cutaneous leishmaniasis in an endemic area in Southern Bahia, Brazil]." Cad Saude
Publica 16(3): 701-708.
Stewart, Carree Coffee, and William R. Brieger. "Community views on cutaneous leishmaniasis
in Istalif, Afghanistan: implications for treatment and prevention." International quarterly of
community health education 29.2 (2009): 123-142.
Turan, E., et al. (2015). "A Comparison of Demographic and Clinical Characteristics of Syrian and
Turkish Patients with Cutaneous Leishmaniasis." American Journal of Tropical Medicine and
Hygiene 93(3): 559-563.
Uchoa, C. M., et al. (2004). "[Health education: teaching about American tegumentary
leishmaniasis]." Cad Saude Publica 20(4): 935-941.
238 | Chapter 5 - Supporting information
Vazquez ML, Kroeger A, Lipowsky R, Alzate A. [Popular conceptions regarding cutaneous
leishmaniasis in Colombia and their applicability in control programs]. Boletin de la Oficina
Sanitaria Panamericana Pan American Sanitary Bureau. 1991;110(5):402-12. Epub 1991/05/01.
PubMed PMID: 1829895.
Vlassoff, C. (1997). "The gender and tropical diseases task force of TDR: achievements and
challenges." Acta Tropica 67: 173-180.
Wijeyaratne, P. M., et al. (1994). "Endemic disease and development: the leishmaniases." Acta
Trop 56(4): 349-364.
No primary study (n=16)
Al-Kamel, Mohamed A. "Impact of leishmaniasis in women: a practical review with an update on
my ISD-supported initiative to combat leishmaniasis in Yemen (ELYP)." International Journal of
Women's Dermatology 2.3 (2016): 93-101.
Alonso, Laura Moya, and Jorge Alvar. "Enfermedades tropicales desatendidas estigmatizantes:
una revisión sistemática." Medicina Social 5.4 (2011): 246-258.Alvar, Jorge, Sergio Yactayo, and
Caryn Bern. "Leishmaniasis and poverty." Trends in parasitology 22.12 (2006): 552-557.
Bailey, Freddie, et al. "A new perspective on cutaneous leishmaniasis—Implications for global
prevalence and burden of disease estimates." PLOS Neglected Tropical Diseases 11.8 (2017):
e0005739.
Bern, Caryn, James H. Maguire, and Jorge Alvar. "Complexities of assessing the disease burden
attributable to leishmaniasis." PLoS Neglected Tropical Diseases 2.10 (2008): e313.
Dario Vélez, Ivan, et al. "Gender and leishmaniasis in Colombia: a redefinition of existing
concepts." (1997).
Hofstraat, Karlijn, and Wim H. van Brakel. "Social stigma towards neglected tropical diseases: a
systematic review." International health 8. suppl_1 (2016): i53-i70.
Chapter 5 - Supporting information | 239
Homsi, Y., and G. Makdisi. "Leishmaniasis: a forgotten disease among neglected
people." Internet J Health 11.2 (2010).
Karimkhani, Chante, et al. "Global burden of cutaneous leishmaniasis: a cross-sectional analysis
from the Global Burden of Disease Study 2013." The Lancet Infectious Diseases 16.5 (2016): 584-
591.
Khatami, Alireza. Development of a Disease-Specific Instrument for Evaluation of Quality of Life
in Patients with Acute Old World Cutaneous Leishmaniasis in Adult Iranian Patients: A Study
Protocol. Diss. Centre for the Public Health, 2007.
Litt, Elizabeth, Margaret C. Baker, and David Molyneux. "Neglected tropical diseases and mental
health: a perspective on comorbidity." Trends in parasitology 28.5 (2012): 195-201.
Modabber, Farrokh, et al. "Consultative meeting to develop a strategy for treatment of
cutaneous leishmaniasis. Institute Pasteur, Paris. 13–15 June, 2006." Kinetoplastid Biology and
Disease 6.1 (2007): 3.
Mondragon-Shem, Karina, and Alvaro Acosta-Serrano. "Cutaneous leishmaniasis: the truth about
the ‘flesh-eating disease’in Syria." Trends in parasitology 32.6 (2016): 432-435.
Okwa, O. O. "Tropical Parasitic Diseases andWomen." Annals of African medicine 6.4 (2007).
Okwor, Ifeoma, and Jude Uzonna. "Social and economic burden of human leishmaniasis." The
American journal of tropical medicine and hygiene 94.3 (2016): 489-493.
Weigel, M. M., et al. "Gênero e leishmaniose cutânea no Equador rural: risco de doença,
gravidade e conseqüências." Doenças endêmicas: abordagens sociais, culturais e
compartimentais (2000).
240 | Chapter 5 - Supporting information
Weiss, Mitchell G. "Stigma and the social burden of neglected tropical diseases." PLoS neglected
tropical diseases 2.5 (2008): e237.
Not a Localised CL form (n=06)
Costa, Jackson Maurício L., et al. "Aspectos psicossociais e estigmatizantes da leishmaniose
cutâneo-mucosa." Revista da Sociedade Brasileira de Medicina Tropical 20.2 (1987): 77-82.
Getnet, Semeneh. "The Psycho-Social Impact of Cutaneous Leishmaniasis on People Infected by
the Disease." (2012).
Magalhães, Hílman M., et al. "Mudança do componente cognitivo da atitude de uma população
de região endêmica do sul da Bahia diante da leishmaniose tegumentar." Revista da Sociedade
Brasileira de Medicina Tropical 23.1 (1990): 49-52.
Toledo Jr, Antonio Carlos de Castro, et al. "Assessment of the quality of life of patients with
cutaneous leishmaniasis in Belo Horizonte, Brazil, 2009–2010. A pilot study." Transactions of The
Royal Society of Tropical Medicine and Hygiene 107.5 (2013): 335-336.
van ‘t Noordende, Anna T., et al. "Towards a toolkit for cross-neglected tropical disease morbidity
and disability assessment." International health8.suppl_1 (2016): i71-i81.
Weigel, M. M., et al. "Cutaneous leishmaniasis in subtropical Ecuador: popular perceptions,
knowledge, and treatment." (1994).
VL or PKDL or Diffuse form of CL (n=04)
Austveg, B. and C. Vlassoff (1993). Gender and tropical diseases: research to lift women's burden.
Revised, Geneva, Switzerland, World Health Organization [WHO], Special Programme for
Research and Training in Tropical Diseases, 1993.: ii, 14, [12] p.
Basher, A., et al. (2015). "A Study on Health Seeking Behaviors of Patients of Post-Kala-Azar
Dermal Leishmaniasis." Biomed Res Int 2015: 314543.
Chapter 5 - Supporting information | 241
Fenwick, A. (2012). "The global burden of neglected tropical diseases." Public Health 126(3): 233-
236.
Rathgeber, E. M. and C. Vlassoff (1993). "Gender and tropical diseases: A new research focus."
Social Science & Medicine 37(4): 513-520.
Full text not available (n=02)
Carrero Rangel, J. A. and R. E. Contreras Moreno (2008). "Leishmaniasis cutánea: epidemiología
y aspectos psicosociales." 71-71.
Casavechia, M. T. G., et al. (2002). "A leishmaniose tegumentar sob a perspectiva do paciente:
resultado de uma prática educativa." Rev. bras. anal. clin 34(4): 233-239.
No leishmaniasis article (n=02)
Kaur, V. (1997). "Tropical diseases and women." Clinics in Dermatology 15(1): 171-178.
van Beugen, S., et al. (2016). "Implicit stigmatization-related biases in individuals with skin
conditions and their significant others." Health Psychology 35(8): 861-865.
All 15 included final articles:
1. Abazid N, Jones C, Davies CR. Knowledge, attitudes and practices about leishmaniasis
among cutaneous leishmaniasis patients in Aleppo, Syrian Arab Republic. East Mediterr Health J.
2012;18(1):7-14.
2. Al-Kamel MA. Stigmata in cutaneous leishmaniasis Historical and new evidence based
concepts 2017.
3. Bennis I, Thys S, Filali H, De Brouwere V, Sahibi H, Boelaert M. Psychosocial impact of
scars due to cutaneous leishmaniasis on high school students in Errachidia province, Morocco.
Infect Dis Poverty. 2017;6(1):46.
242 | Chapter 5 - Supporting information
4. Chahed MK, Bellali H, Ben Jemaa S, Bellaj T. Psychological and Psychosocial
Consequences of Zoonotic Cutaneous Leishmaniasis among Women in Tunisia: Preliminary
Findings from an Exploratory Study. PLoS Negl Trop Dis. 2016;10(10):e0005090.
5. Fernando SD, Siriwardana H, Guneratne K, Rajapaksa LC. Some sociological aspects of
cutaneous leishmaniasis in patients attending a tertiary referral centre in Colombo, Sri Lanka.
International Health. 2010;2(1):69-74.
6. Handjani F, Kalafi A. Impact of dermatological diseases on family members of the
patients using Family Dermatology Life Quality Index: a preliminary study in Iran. Iranian Journal
of Dermatology. 2013;16(4):128-31.
7. Kassi M, Kassi M, Afghan AK, Rehman R, Kasi PM. Marring Leishmaniasis: The
Stigmatization and the Impact of Cutaneous Leishmaniasis in Pakistan and Afghanistan. Plos
Neglect Trop Dis. 2008;2(10):3.
8. Nilforoushzadeh MA, Roohafza HR, Jaffary F, Khatun M. Comparison of quality of life in
women suffering from Cutaneous leishmaniasis treated with topical and systemic glucantime
along with psychiatric consultation compared with the group without psychiatric consultation.
Journal of Isfahan Medical School. 2012;29(172).
09. Ramdas S, van der Geest S, Schallig H. Nuancing stigma through ethnography: the case
of cutaneous leishmaniasis in Suriname. Social Science & Medicine. 2016;151:139-46.
10. Reithinger R, Aadil K, Kolaczinski J, Mohsen M, Hami S. Social impact of leishmaniasis,
Afghanistan. Emerg Infect Dis. 2005;11(4):634-6.
11. Reyburn h. Social and psychological consequences of cutaneous leishmaniasis in kabul,
afghanistan. Healthnetinternational in partnership with Norwegian Church Aid. 2000.
Chapter 5 - Supporting information | 243
12. Simsek Z, Ak D, Altindag A, Günes M. Prevalence and predictors of mental disorders
among women in Sanliurfa, Southeastern Turkey. J Public Health (Oxf). 2008;30(4):487-93.
13. Turan E, Kandemir H, Yesilova Y, Ekinci S, Tanrikulu O, Kandemir SB, et al. Assessment
of psychiatric morbidity and quality of life in children and adolescents with cutaneous
leishmaniasis and their parents. Postep Dermatol Alergol. 2015;32(5):344-8.
14. Vares B, Mohseni M, Heshmatkhah A, Farjzadeh S, Safizadeh H, Shamsi-Meymandi S, et
al. Quality of Life in Patients with Cutaneous Leishmaniasis. Arch Iran Med. 2013;16(8):474-7.
15. Yanik M, Gurel MS, Simsek Z, Kati M. The psychological impact of cutaneous
leishmaniasis. Clin Exp Dermatol. 2004;29(5):464-7.
244 | Chapter 5 - Supporting information
Data extraction labels of the main conceptual categories used in NVivo 11
Country of the study
Author names, year, journal
Study design (cross sectional, case control …) and type (Quantitative, Qualitative)
Population experiencing CL (characteristics)
Sample size (number of participants, gender, age)
Ratio Men/women CL affected
Cutaneous Leishmaniasis species
Dermatological condition involved (CL lesions, CL scars)
Types of stigma (Cite the exact names and types used by those authors)
Types of psychological consequences
Reasons for stigma related to the dermatological condition
Notion of time change of the perception of stigma
Notion of time change of the perception of psychological consequences
Comparison between CL lesions and CL scars
Comparison between CL and other NTD
Comparison between CL and other (No NTD) dermatological diseases
Coping strategies targeting CL outcomes
Measurement scale of stigma
Measurement of psychological consequences
Main finding
Chapter 6 - Supporting information | 245
Supporting information Chapter 6 Supporting material 1: Repartition of the samples
Dental broach
sample for RDT
Or
Mic 1 =
S1 first sample by scraping
S3 duplicate of
S1
SECOND PCR on S3:
half ITS1 (Casablanca)
and half kDNA
(Antwerp)
Mic 2 =
S2 second
sample by
scraping
S4 duplicate of
S2
FIRST PCR on S4:
(ITS1) (Casablanca)
Microscopy reading of
S1 and S2
SECOND PCR on S4:
half ITS1 (Casablanca)
and half kDNA
(Antwerp)
FIRST PCR on S3:
(ITS1) (Casablanca)
Microscopy reading of
S1 and S2
Acknowledgements | 247
Acknowledgements
My sincere gratitude to Prof. Dr. Marleen Boelaert my promoter for your human qualities, your
vast scientific knowledge, and your unlimited generosity. Your guidance, advice, and reviews
have made the thesis a reality. Working with you and with your team was a real pleasure.
Special words of gratitude to my promoter Prof. Dr. Vincent De Brouwere; for the motivating
discussions and learning trajectory. He was the best support for me in my home institute to help
me finish this thesis.
I am equally grateful to Prof. Dr. Jean Claude Dujardin and Prof. Dr. Hamid Sahibi, my Belgian and
Moroccan promoters, for their supervision of my Ph.D. work.
I would like to thank all my other co-authors with whom I had the privilege to collaborate during
the past years. For the enjoyable field work and generous feedback and suggestions on the
writing process.
I am thankful for all the individual doctoral committee members and the external jury for their
comments and suggestions that helped to enhance the content and the structure of this thesis.
I am indebted to the Institute of Tropical Medicine (ITM), Antwerp, Belgium and the Moroccan
Ministry of Health for giving me the opportunity to work in an intellectually stimulating
environment at the Unit of Epidemiology and Control of Tropical Diseases – Department of Public
Health at the ITM. I am indebted to the team who gave me the opportunity to exchange ideas,
thoughts and work together over the past four years. I heartily thank the support of my Belgian
friends during my stay at ITM, whenever I needed advice or help, you were always ready to help
without any hesitation, and I learned a lot from you all. Séverine Thys with whom I learned what
is the meaning of qualitative research, Kristien Verdonck, the wise scientist and the guardian of
ethics. Anne Marie Trooskens who accomplishes big things with few words. Greet Verhulst who
is the essence of dynamism. Temmy Sunyoto for her ease to communicate without borders. Bart
Ostyn who reminds me to be a doctor before being a researcher. Epco Hasker, who conveyed to
me the meaning and the power of smiling during all my stay; I never saw you losing your smile
even with the huge tasks and competitive deadlines you faced. Rian Snijders, Annette Erhart and
Raquel Inocencio were the best examples of how to combine family responsibilities with high
performance at work. Evelien Paessens and Kristien Cloots, for their kind support and friendly
presence. I would like to thank all other friends with whom I shared the workspace: Veerle
Vanlerberghe, Pierre Lefèvre, Esteban Londoño, Tullia Battaglioli; and all other Ph.D. students
especially Kanika Deshpande Koirala, Dalila Martinez, and all visiting researchers that I never
would have met - was it not for being Marleen’s Ph.D. student.
248 | Acknowledgements
My special thanks to all the ITM coordinators, administrative and financial units, particularly Ann
Verlinden, Nathalie Brouwers, Helga Bodges, Patricia Braat, Fiona Robertson, Hilde Verheyen,
Annelies Croon, Goele Geerinckx and all other former and actual ITM staff members. From the
university of Antwerp, I want to thank Miss Evy Pluym for her administrative help.
The research for this thesis was made possible by a scholarship from the Belgian Development
cooperation DGD administered by the Institute of Tropical Medicine, Antwerp, Belgium.
Thank you to my Moroccan colleagues with whom I collaborated in grants and projects financed
by the Belgian cooperation to enhance the Moroccan Health System Research capacities. Thank
you to all colleagues at the National School of Public Health and the Ministry of Health.
This dissertation is dedicated to all leishmania researchers and all patients suffering from this
disease. I would like to acknowledge all the volunteers, participants, health professionals, local
authorities and villagers who participated and facilitated our fieldwork.
Finally, I would like to thank all people who have helped me navigate through the doctoral
pathway. On the top, my parents and my sister Nadia; they know that my Ph.D. studies were full
of memories that I cannot forget and that changed my way of thinking and beliefs.
About the author
Birthday August 8th, 1976 in Oujda town in Eastern Morocco. Baccalaureate in Mathematical
Sciences in Oujda. Medical studies at the Faculty of Medicine and Pharmacy in Rabat. Worked
since 2003 with the Ministry of Health (MoH) as a general practitioner. Then, followed a
specialization in Public Health at the National Institute of Health Administration in Rabat.
Worked since 2010 as a representative of the MoH in Southeastern Morocco to manage the
public health organizations. There, he was confronted with an epidemic of cutaneous
leishmaniasis motivating him to start a Ph.D. study on the topic since 2014 (Unit of Epidemiology
and Disease Control at the Institute of Tropical Medicine in Antwerp and the Faculty of
Pharmaceutical, Biomedical and Veterinary Sciences - University of Antwerp). Similarly, he was
appointed as a Medical Researcher at the National School of Public Health in Rabat, Morocco.
He succeeded to stay single without children during all these years of studies.