View
10
Download
0
Category
Preview:
Citation preview
ANCYLOSTOMA DUODENALE SEPERATED FROM CONTAMINATED SOIL
SHAHIDA AZHAR ALI1, TANVEER AKHTAR
2, AZHAR MAQBOOL
3, AMMARA HUSSAN
4 &
SAMMAN IKRAM5
1,2,4&5Department of Zoology, University of the Punjab, Quaid-e-Azam Campus, Lahore, Pakistan
3Department of Parasitology, University of Veterinary and Animal Sciences, Lahore, Pakistan
ABSTRACT
Soil samples showed an overall prevalence 1.79 % of Ancylostoma duodenale‟s eggs in six slums of Lahore,
Punjab from Nov 2006 to Oct 2008. Significant prevalence was observed in Missrisha (0.89 %) followed by Bhutto Colony
(0.83 %) , Siddiquia Colony (0.72 %), Khairdin Park (0.53 %), Sheikhupura Road (0.39 %) whereas lowest in Scheme No
2 ( 0.22 %) respectively. Season wise high prevalence was observed in autumn (3.92 %), summer (1.88 %) and winter
(1.29 %) as compared to spring (0.50 %). Month wise highest prevalence (4.83 %) was observed in October followed by
3.67 % in September that gradually decreased to 0.83 % in December and declined to 0.50 % in March respectively.
Demographic data showed 33.47 % people used gurkies / pit, 27 % defecated in open fields, 23 % had very poor sewerage
system and 14.52 % availed satisfactory sewage conditions. Children who had habit of pica (10.50 %), nail biting
(12.51%), sucking thumb (11 %), did not wash hand before meal (12.10 %), after defecation (21.76 %), walked bare footed
(25.51 %) and used junk food (7.54 %) were found respectively.
KEYWORDS: Ancylostomiaisis, Prevalence, Slums, Gurkies, Defecation
Part of Ph.D thesis of first author
INTRODUCTION
Ancylostomiaisis was a widely spread parasitic disease in tropical and subtropical areas (Jiraanankul et al. (2012)
caused by A. duodenale exclusively man parasite, a soil transmitted helminth (STHs) (CDC, 2012), especially in areas with
poor sanitary conditions (Shaikh et al. (2009) ; Ziegelbaueret al. (2012 ). One quarter of the world population i.e. Africa,
Middle East, Eastern Europe and South East Asia (de Silva et al. (2003) were infected with hookworms (Hotez et al.,
2004). out of 122 million, 21 million children of age 1-5 years old were found infected with hookworm, (Kirwan et al.
(2009), 4-15 years of agein India (Norhayati et al. (2003), (52%) hookworm prevalence (Verle et al. (2003) was present in
school going children and decreased with age (Clements et al. (2010) and caused about 22.1 million disabilities annually
in the world (Kirwan et al. (2009). Larvae of A.duodenale survive for several weeks in dirt (WHO, 2011), could also reside
in dogs, cats etc and they acted as paratenic host till they find their way to final host (Brinksworth et al. (2000), it
constituted a significant risk for public health (Kollataj et al. (2012). Ancylostomiaisis was more common in 2-7 years old
children due to habit of pica (Al Mekhlafi et al. (2008) and those who did not wash their hands after defecation and before
meal (Speare et al. (2006) ; Mehmood et al. (2009) ; Khanum et al. (2010). A. duodenale„s eggs from soil could be
transferred onto vegetables (Maipanich et al. (2004) when children eat these contaminated raw vegetables (Ulukanligi et
al. (2001) they might have helminthiasis. In Argentina from city of Resistencia, from 5 public places , 475 soil samples,
17 from kindergarten sandpits and 124 from housing estates were collected, high prevalence of ancylostoma‟s eggs were
observed in 20 % contaminated public park playgrounds with a value of 100%, followed 19.4% found in housing estates
and 11.8% in kindergarten samples (Alonso et al. (2001). Increased urbanization and population density was directly
proportionate to STH infection (Brooker et al. (2006). 288 faecal samples were collected and observed in 2000-2006 from
International Journal of Zoology
and Research (IJZR)
ISSN 2278–8816
Vol.3, Issue 2, Jun 2013, 27-38
© TJPRC Pvt. Ltd.
28 Shahida Azhar Ali, Tanveer Akhtar, Azhar Maqbool, Ammara Hussan & Samman Ikram
contaminated parks; A. duodenale prevalence 20.47% (Rubel and Wisnivesky, 2010) was observed on sidewalks
surrounding the parks. Improvement in socioeconomic status (Rokni, (2009) ; Lin et al. (2010), personal hygiene /
behavior and inadequate sanitation reduced the rate of infection (Ziegelbauer et al. (2012).Many surveys had been
conducted in various parts of Pakistan (Shaikh et al. (2000) Larkana, (Chaudhry et al. (2004) Muzzafarabad, (Kamran et
al. (2005) Karachi and (Khan et al. (2012) in Swat respectively but researchers did not represented relationship among
socioeconomic status (SES), inadequate education, poor sanitation, personal hygiene, family cluster and lack of health care
respectively. Soil contact activity was the basic reason for STHs infection in children.
OBJECTIVE
The study was launched to observe the status of ancylostomiasis in the slums of Lahore to assess the degree of
prevalence (%) in soil samples to improve the health status of children. These studies would be helpful to control
ancylostomiaisis by launching deworming programme at national level with collaboration of veterinarians and health
department.
MATERIAL AND METHOD
Soil samples were collected from the six slums i.e. Bhutto Colony, Siddiquia Colony, Scheme No 2, Sheikhupura
Road, Khairdin Park and Missri Shah of Northern Lahore, Punjab, Pakistan from November 2006 to October 2008 to find
out the prevalence (%) ratio (Map. a and b ). Demographic data was also collected along with social behavior of local
people (Performa 1).
Soil Collection
A total of 25 soil samples from each locality were monthly collected .i.e. from the public parks, fields and
playgrounds where local people defecate i.e. near the filth depots and from the dunghills where stray / wild dogs wander.
Soil was kept in screw caped plastic vial clearly labeled with date and place of collection. These samples were examined
on the same day by Sodium hypochlorite recovery technique (Urquhart et al. (2001) to observe the presence of
helminth‟seggs. The samples not processed on the same day were kept at room temperature.
Sodium Hypochlorite Technique
In a test tube 2 g. of sieved soil sample was placed with 5 ml of 30% sodium hypochlorite (NaOCl) solution. The
tube was shaken intermittently. A few drops of prepared solution was placed on glass slide, placed cover glass and
examined microscopically at 40 magnification, to identify the helminth‟s ovas on the basis of morphology described by
Urquhart et al. (2001).
Statistical Analysis
Collected soil data was entered into Excel Data Sheet version “7” of the computer and transferred to SPSS
Version 15.5, Z-test was applied as it was suitable for analysis, level of significance at the 0.05, 0.01 and 0.001 was
considered as .i.e. *, ** and *** respectively (Steel and Torrie, 1980).The prevalence of the infection / disease was
recorded following the modified formula described as.
RESULTS
3600 soil samples were observed from the 6 slums i.e. Bhutto Colony, Siddiquia Colony, Scheme No 2,
Ancylostoma duodenale Seperated from Contaminated Soil 29
SheikhupuraRoad, Khairdin Park and Missrishah of Northern Lahore, Punjab, Pakistan from Nov 2006 to Oct 2008.
Demographic Status
Out of 3600, children of age 4-10 years old were found with the habit of pica / geophagia (10.50 %), 4-10 years
with nail biting (12.15 %), 5-10 years old sucked thumb (11 %), 3-5 years old did not wash hands before meal (12.10 %)
and 6-11 years old after ( 21.76 %) defecation, 5-13 years old walked bare footed (25.52 %) and 4-11 years old used junk
food (7.54 %) respectively. 35.47% peoples were using gurkies / pit, 27 % defecated in open fields, 23 % had very poor
sewage system and 14.52 % availed satisfactory sanitary system (Table 1; Figure 1a,1b ; Plate 1a, 1b.1c,1d,1e,1f ).
Overall Prevalence
An overall prevalence (%) of A.duodenale’s eggs in the soil was found 1.79 %in Lahore, Punjab from November
2006 to October 2008 (Table 2).
Area Wise Prevalence (%)
Area wise prevalence of geohelminth‟s eggs in soil of six slums of Lahore, Punjab province,Pakistan was
observed, it was highest in Missrishah(0.89 %) followed by Bhutto Colony (0.83 %) Siddiqia Colony (0.72 %) Khairdin
Park (0.53 %) and Sheikhupura Road (0.39 %) whereas lowest in Scheme No 2 (0.22 %) respectively (Table 2; Figure 1c).
Month Wise Prevalence (%)
After analyzing month wise data, highest prevalence was observed 4.83 % in October followed by 3 % in
September that gradually decreased to 0.83 % in December and declined to 0.50 % in March. When statistical analysis (Z-
test) was applied on month wise data, prevalence of the month of the March was the lowest, so it was compared with other
months. There was no significant difference among prevalence (%) of the month January, February, May and July.
Whereas November (P<0.001), August (P<0.001) and Septembers (P< 0.01) showed significant difference with respect to
March (Table2; Figure 1d).
Season Wise Prevalence (%)
Statistically prevalence was significantly higher in autumn (P<0.001), summer (P<0.01) and in winter (P<0.05) as
compared to spring i.e it was observed 3.92 % during autumn followed by 1.88 % in summer, 1.29 % in winter and lowest
0.50 % in spring respectively (Table 2; Figure 1e).
DISCUSSIONS
Soil samples determines the prevalence / infection ratio as eggs deposited in soil by pet / stay animals and man,
hibernate and transmit to person who come in direct contact with that contaminated soil, eggs might be transferred from
soil to vegetables, fruits or being transmitted by insects, animals and man supported by the reports of (WHO, 2011).
Therefore soil contamination constituted a significant zoonotic risk. Unawareness about the transmission and biology of
parasite and inattentively promote ancylostomiasis and these observations are justified with findings of Habluetzel et al.
(2003) and Ejima and Ajugun (2011). Soil acts as a transmitting medium for fertilized eggs of helminth to develop and
mature. Present study showed an overall prevalence (1.79 %) of A. duodenale‟s eggs in the soil less than 14.3 % observed
in China (Uneke et al. (2007), 24.1 % in Lahore, Pakistan (Ashraf et al. (2008) and 53.6 % in Nigeria (Chukwuma et al.
(2009).The conflict existed due to difference in climatic, socioeconomic conditions, personal hygiene, social behavior,
population diversity, density, geographical distribution of helminth. Another reason is increase in soil contamination by the
people who defecate in open fields, sidewalks and on dunghills, throw excreta of animals and man on dunghills, flies, dust
30 Shahida Azhar Ali, Tanveer Akhtar, Azhar Maqbool, Ammara Hussan & Samman Ikram
transmit eggs here and there and ultimately ingested by man and contaminate the topography and playgrounds. Another
reason might be the use of recovery techniques, size, volume of collected data, season of collection, examination and depth
of soil effected prevalence (%) in soil. Similarly it was observed that soil contamination is going to be increased due to the
frequent use of Bhal (the soil taken from the sewerage drain) in lawns to enhance fertility for better growth of plant after
every year. The residents of the posh areas also practiced to add river soil (Kaasuo) in foundations of their houses, in this
way helminth ova along with termite‟s egg were transmitted from one area to another unintentionally. Similarly soil from
other parts of the country was commonly brought by people for construction purposes in old and new housing societies,
indirectly transmitted helminth infection. The children come in contact with soil when play in their lawns or elder sat there,
transmitted ova or infected stage larvae with their shoes inside the houses premises unknowingly. It s therefore suggested
to disinfect the soil before use to avoid ancylostomiaisis and educate people about health care practices.From the present
study infested soil samples with helminth ova were observed from the lawns of the houses, backyards, compoundsand
parks consistent with findings described by Orhun et al. (2009), indicated that direct contact with fur of pets was not
necessary (Zewdu et al. (2011). The outcomes of the present study showed decrease in temperature reduced the rate of
prevalence 3.92 % in autumn, declined to 1.29 % in winter supported by findings in Nigeria (Mabaso et al. (2003) and
increase in age also decreased the prevalence ratio of ancylostomiasis due to the improvement in personal hygiene with
growing age. The common habits of walking barefoot and improper disposal of human faeces were the important features
for high prevalence of helminthes in Pakistan. Present study indicated helminthiaisis had association with SES factors such
as inadequate sewerage, sanitary and education facilities, poor personal hygiene, water supply, social behavior of persons
like nail biting, sucking thumbs, pica, walking bare footed, defecate in open fields, do not wash hands before meal and
after defecation and improper health care facilities supported by the observations of [Khan et al. (2004), Gunawardena et
al. (2005), Speare et al. (2006), Ferguson et al. (2007), Saeed et al. (2008), Shaikh et al. (2009), Mishra et al. (2005),
Muznebin et al. (2007), Al Mekhlafi et al. (2008), Mehmood et al. (2009), Khanum et al. (2010) and Ziegelbauer et al.
(2012)]. Improvement in sewage system, SES, personal hygiene and provision of hygiene and physiology education
minimizes the risk of ancylostomiasis. Similarly poverty played important role to enhance that gusting situation, people
hesitate to spend money on their health.
CONCLUSIONS
Children health was neglected since now and the vulnerable class was of 4-13 years old as
1- They played in parks or playground come in contact with contaminated soil was a risk factor for health.
2- Did not wash their hands before meal and after defecation.
3- Had the habit of nail biting and sucking thumbs too.
5- Always wandered bare footed.
Performa 1
Serial No: Date: _______Area Rural/Urban: _____Fecal Sample No: ______Soil Sample No.: ______
Male/Female: ______
Age: _____Name of Hospital/School: ______________ Name of Patient: ______________
Address: ______________________ Education: _____________B.P.S: _____Monthly income:
__________Occupation: _________
Ancylostoma duodenale Seperated from Contaminated Soil 31
Family Size: ______________ No. of Old: __________No. of Young: ______________ No. of Children:
_______
House constructed of Concrete/Mud: _______________No. of Rooms:_________Fecal
Refuse……Low/Moderate/High: _____________
Domestic Refuse…..Open/Bin: _________
Personal Hygiene: ___________Habit of Nail biting Yes / No , sucking thumb Yes / No, hand washing before meal
and after defecation Yes / No, walk bare-footed Yes / No, fond of street junk food Yes / No.
Well Nourished/Under Nourished/Malnutrition: ______________Drainage…… Open/Underground:
________________
Locality surrounded by Water Body/Fields: _______________Fecal dispersal via Sanitary/Unsanitary/No Facility:
___________
Water supply... Tap/Hand Pump/Well/Spring/River: ___________
APPENDICES
Table 1: Showing the Prevelance (%) Social Habits of Children Residing in Soil Contaminated Slums of Northern
Lahore from Nov 2006-Oct 2008
Factors Habit of
Pica Nail Biting
Suck
Thumb
Don’t
Wash
Hands
Before
Meal
Don’t
Wash
Hands
After
Defecation
Walk Bare
Footed
Use Junk
Food from
Street
Hawkers
Total no
of
children
observed n=
36
00
429 792 871 1567 1837 543 689
Percentage
(%) 10.50% 12.51% 11% 12.10% 21.76% 25.51% 7.54%
Prevalence
(%)±S.E
10.50±0.51
***
12.51±0.39
***
11.00±0.37
***
12.10±0.38
***
21.76±0.49
***
25.51±0.51
***
7.54±0.31**
*
Age (years) 10-Apr 10-Apr 5-Mar 8-May 11-Jun 13-May 11-Apr
Sewerage System
Gurkies (pit) Open
defecation Poor sanitation Satisfactory
1277 972 828 523
35.47% 27% 23% 14.52%
Table 2: Areawise, Monthwise and Seasonwise Prevalence (%) of Ancylosto maduodenalein Soil Samples in Six
Slums of Northern Lahore, Punjab, Pakistan from Nov2006-Oct 2008
Total n=3600
Total No. of Infected Soil Samples (Ancylosto maduodenale) in Soil
Fa
ct
ors
n=1800 Prevalenc
e
(%)±S.E
n=180
0 Prevalence
(%)±S.E
n=3600 Prevalence
(%)±S.E
(1st
Year)
(2nd
Year)
(1+2Ye
ar)
Slu
ms
Bhutto Colony
n=
60
0/Y
ear
/
Are
a
12 0.67±0.19
*
18 1.00±0.23** 30 0.83±0.15*
** Siddiquia Colony 10 0.56±0.18 16 0.89±0.22 26 0.72±0.14
Scheme No. 2 3 0.17±0.10 5 0.28±0.12 8 0.22±0.08
Sheikhupura Road 6 0.33±0.14 8 0.44±0.16 14 0.39±0.10
Khairdin Park 9 0.50±0.17 10 0.56±0.18 19 0.53±0.12
Missri Shah 11 0.61±0.18 21 1.17±0.25 32 0.89±0.16
32 Shahida Azhar Ali, Tanveer Akhtar, Azhar Maqbool, Ammara Hussan & Samman Ikram
Table 2: Contd.,
Total 3600 51 1.42±0.20
*
78 2.17±0.24* 129 1.79±0.16*
Tim
e (M
on
ths)
Nov2006&2007
n=
30
0 /
Mo
nth
/ Y
ear
2 0.67±0.47 4 1.33±0.66 6 1.00±0.41
Dec 2006&2007 3 1.00±0.57 2 0.67±0.47 5 0.83±0.37
Jan 2007&2008 5 1.67±0.74 5 1.67±0.74 10 1.67±0.52
Feb 2007&2008 4 1.33±0.66 6 2.00±0.81 10 1.67±0.52
Mar 2007&2008 2 0.67±0.47 1 0.33±0.33 3 0.50±0.29*
Apr 2007&2008 0 0.00±0.00 3 1.00±0.57 3 0.50±0.29*
May 2007&008 5 1.67±0.74 7 2.33±0.87 12 2.00±0.57
Jun 2007&2008 6 2.00±0.81 6 2.00±0.81 12 2.00±0.57
Jul 2007&2008 3 1.00±0.57 6 2.00±0.81 9 1.50±0.50
Aug 2007&008 5 1.67±0.74 7 2.33±0.87 12 2.00±0.57
Sep 2007&2008 6 2.00±0.81 12 4.00±1.13 18 3.00±0.70
Oct 2007&2008 10 3.33±1.04 19 6.33±1.41** 29 4.83±0.88
Total 3600 51 1.42±0.20
*
78 2.17±0.24* 129 3.58±0.31
Sea
son
s
Winter 1200 14 1.17±0.31 17 1.42±0.34 31 1.29±0.23*
Spring 600 2 0.33±0.24
*** 4
0.67±0.33**
* 6
0.50±0.20*
**
Summer 1200 19 1.58±0.36 26 2.17±0.42**
* 45
1.88±0.28*
**
Autumn 600 16 2.67±0.66 31 5.17±0.90 47 3.92±0.56
Overall Prevelance (%) n=1800*2=3600 / 1+2 Year 129 1.79±0.16*
*P<.05, **P<.01, ***P<.001 Z-Test
Figure 1: Prevalence (%) of Socioeconomic Status of Children (a), Sewerage System (b), Prevalence (%) of
Ancylostomaduodenalein Soil Samples Area Wise (c), Month Wise (d) and Season Wise (e) Nov 2006-Oct 2008
Northern Lahore. Z-test *=P<0.05, **=P<0.01, ***P<.001
Ancylostoma duodenale Seperated from Contaminated Soil 33
Plate 1: Showing the Poor Sewerage System with Uneduquate Supply of Water (a),Open Defecated Ares (b), Poor
Drain Syatem (C), Gurki (D), Poor Sanitation (e)and Contact of Man with Animals and Dunghills (f)
34 Shahida Azhar Ali, Tanveer Akhtar, Azhar Maqbool, Ammara Hussan & Samman Ikram
REFERENCES
1. AL-MEKHLAFI, H.M.S., JOHARI, S., ATIYA, A.S., ARIFFIN, W.A. AND MAHDY A.K.M., ET AL. 2008.
Pattern and predictors of soil-transmitted helminth reinfection among aboriginal school children in rural
Peninsular Malaysia. Acta. Tropica., 107: 200–204.
2. ALONSO, J.M., STEIN, M., CHAMORRO, M.C. AND BOJANICH, M.V., 2001. Contamination of soils with
eggs of Toxocara in a subtropical city in Argentina. J. Helminthol., 75: 165–168.
3. ASHRAF, K., RAFIQUE, S., HASHMI, H.A., MAQBOOL, A. AND CHAUDHARY, Z.I., 2008.
Ancylostomosis and its Therapeutic Control in Dogs. J. Vet. Anim. Sci., 1: 40-44.
4. BRINKSWORTH, R., HARROP, S., PROCIV, P., AND BRINDLEY., P. 2000. Host specificity in blood feeding
parasties: a defining contribution by haemoglobin-degrading enzymes? Int. J. Parasitol., 30: 785-790.
5. BROOKER, S., CLEMENTS, A.C. AND BUNDY, D.A.P., 2006. Global epidemiology ecology and control of
STH infection. Adv. Parasitol ., 62: 221-261.
6. CHAUDHRY, Z.H., AFZAL, M. AND MALIK, M.A., 2004. Epidemiological factors affecting prevalence of
intestinal parasites in children of Muzaffarabad district. Pak. J. Zool., 36: 267-271.
7. CENTERS FOR DISEASE CONTROL AND PREVENTION. 2012. Hookworm. CDC DPDx: Laboratory
Identification of Parasites of Public Health Concern. Available at
Ancylostoma duodenale Seperated from Contaminated Soil 35
http://www.dpd.cdc.gov/DPDx/HTML/Hookworm.htm. Accessed April 22, 2012.
8. CHUKWUMA, M.C., EKEJINDU, I.M., AGBAKOBA, N.R., EZEAGWUNA, D.A., ANAGHALU I.C. AND
NWOSU, D.C., 2009. The prevalence and risk factors of geohelminth infections among primary school children
in Ebenebe Town, Anambra State, Nigeria.Middle-East J. Sci. Res., 4(3): 211-215.
9. CLEMENTS, A.C., DEVILLE, M.A., NDAYISHIMIYE, O., BROOKER, S. AND FENWICK, A., 2010. Spatial
co distribution of neglected tropical diseases in East African Great Lakes regions; revising the justification for
integrated control. Trop. Med. Int. H., 15: 198-207.
10. DE SILVA, N., BROOKER, S. AND HOTEZ, P., 2003.Soil-transmitted helminth infections: updating the global
picture. Trends Parasitol., 19: 547.
11. EJAMA, I.I.A. AND AJUGAN, R.T., 2011. The prevalence and Health application of ova of human intestinal
helminth parasite isolated from faeces collected near students hostils, Fedral Polytechnic, Ideha, Kogi state,
Nigeria. Int. J. Trop.Med., 6(1): 15-18.
12. FERGUSON, H.B., BOVAIRD, S. AND MUELLER, M.P., 2007. The impact of poverty on educational
outcomes for children. Paediat. Child Health., 12(8): 701–706.
13. GUNAWARDENA, G.S.A., KARUNAWEERA, N.D. AND ISMAIL, M.M., 2005. Effects of climatic, socio-
economic and behavioural factors on the transmission of hookworm (Necator americanus) on two low-country
plantations in Sri Lanka. Ann. Trop. Med. Parasitol., 99: 601-9.
14. HABLUETZEL, A., TRALDI, G., RUGGIERI, S., ATTILI, A.R., SCUPPA, P., MARCHETTI, R., MENGHINI,
G. AND ESPOSITO, F., 2003. An estimation of Toxocaracanis prevalence in dogs, environmental egg
contamination and risk of human infection in the Marche region of Italy. J. Vet. Parasitol., 113: 243-252.
15. HOTEZ, P.J., BROOKER, S., BETHONY, J.M., BOTTAZIE M.E., LOUKAS, A. AND XIAO, S., 2004.
Hookworm infection. N. Engl. J. Med., 351: 799–807.
16. JIRANAANKUL, V., APHIJIRAWAT, W., MUNGTHIN, M., KHOSITNITHIKUL, R., RANGSIN, R.,
TRAUB, R.J., PIYARAJ, P., NAAGLOR, T., TAAMASRI, P. AND LEELAYOOVA, S., 2012. Incidence and
Risk Factors of Hookworm Infection in a Rural Community of Central Thailand. Am. J. Trop. Med. Hyg., 84(4):
594-598.
17. KAMRAN, S.A., BILQEES, F.M. AND SALIM, A., 2005. Protozoan intestinal infections fifteen months
observation on in-patients and out-patients of Fatima hospital, Baqai Medical University, Karachi, Karachi,
Pakistan. Proc. Parasitol., 40: 59-87.
18. KHANUM, H., ISLAM, M.R. AND PARVIN, S., 2010. Occurrences of eggs and larvae of gastrointestinal
nematodes in nails of street inhabitants in Dhaka city. J. Life Earth Sci., 5: 75-79.
19. KHAN, A., SULTANA, A., DAR, A.M.K., RASHID ,H. AND NAJMI, S.A.A., 2004. A study of prevalence,
distribution and risk factors of intestinal helminthic infestation in district Bagh (Azad Kashmir). Pak Armed
Forces Med J., 54: 243-248.
20. KIRWAN, P., ASAOLU, S.O., MOLLOY,
S.F., ABIONA, T.C.,
JACKSON, A.L.
AND HOLLAND, C.V., 2009.
Patterns of soil-transmitted helminth infection and impact of four-monthly albendazole treatments in preschool
children from semi-urban communities in Nigeria: a double-blind placebo-controlled randomised trial. BMC
Infect. Dis., 9: 20.
36 Shahida Azhar Ali, Tanveer Akhtar, Azhar Maqbool, Ammara Hussan & Samman Ikram
21. KHAN, W., NISA, N.U., KHAN, A. AND NAQVI, S.M.H.M., 2012. Endemicity of intestinal parasites with
special reference to nematodes in individuals related to education (students, staff and workers) in swat, kpk,
pakistan . Pak. J. Nematol., 30(1): 77-85.
22. KOLLATAJ, W., MILCZAK, A., KOLLATAJ, B., KARWAT, I.D., SYGIT, M. AND SYGIT, K., 2012. Risk
factors for the spread of parasitic zoonoses among dog owners and their families in rural areas. Anna. Agri.
Environ. Med., 19(1): 79-84.
23. LIN, S.X., WANG, S.Q., HU, X.M., CHEN, D.Y., TONG, C.J. AND LI, S.W., 2010. Epidemiology of soil-
transmitted nematode infections in central mountain area of Hainan province. Chinese J. Parasitol. Parasit. Dis.,
28(2): 160-161.
24. MAIPANICH, W., WAIKAGUL, J., WATHANAKULPANICH, D., MUENNOO, C., SANGUANKIAT, S.,
PUBAMPEN, S., ANANTAPHRUTI, M.T., NUAMTANONG, S., YOONUAN, T. AND VISETSUK, K., 2004.
Intestinal parasitic infections among inhabitants of the north, west-central and eastern border areas of Thailand. J.
Trop. Med. Parasitol., 27: 51–58.
25. MABASO, M.L.H., APPLETON, C.C., HUGHES, J.C. AND GOUWS, E., 2003. The effect of soil type and
climate on hookworm (Necator americanus) distribution in KwaZulu-Natal, South Africa. Trop. Med. Int. H., 8:
722-727.
26. MEHMOOD, K., SHERWANI, M.K., AHMED, M., HUSSAIN, M., SAFDAR, S. AND BAITU, M., 2009.
Parasitic Infestation in Children of District Vehari: An Underdeveloped area of Pakistan. Pak. J. Med. Res., 48(1):
8-15.
27. MISHRA, P.K., AGRAWAL, A., JOSHI, M., SANGHVI, B., SHAH, H. AND PARELKAR, S.V., 2005.
Intestinal obstruction in children due to Ascariasis: A tertiary health centre experience. Med. Journal, 5(2): 65-70.
28. MUZNEBIN, F., KHANUM, H. AND HOSSAIN, A., 2007. Incidence of nematode infections among the children
brought to icddr, b hospital, Dhaka, Bangladesh. J. bio-sci.,15: 159-164.
29. NORHAYATI, M., FATAMAH, M.S., YUSOF, S. AND EDARIAH, A.B. 2003. International Parasitic infection
in man; a review. Med. J. Malaysia., 58: 296-305.
30. ORHUN, A., GRÜNER, B., MÜLLER-STÖVER, I., REUTER, S., ROMIG, T., HÄUSSINGER, D., KERN, P.,
2009. Eurosurveillance Ed., 14(22): 6
31. RUBEL, D. AND WISNIVESKY, C., 2010. Magnitude and distribution of canine fecal contamination and
helminth eggs in two areas of different urban structure, Greater Buenos Aires, Argentina. Vet. Parasitol., 133:
339–347.
32. ROKNI, 2009. Echinococcosis /hydatidosis in Iran, Iranian J Parasitol., 4(2): 1-16.
33. SAEED, A., CHEEMA, H.A., ALVI, A. AND SULEMAN, H., 2008. Hookworm Infestation in Children
Presenting with Melena-Case Series. Pak. J. Med. Res., 47: 4.
34. SHAIKH, G.S., BEGUM, R., HUSSAIN, A. AND SHAIKH, R., 2009. Prevalence of intestinal protozoan and
helminth parasites in sukkur, sindh. Sindh Univ. Res. J., 41(2): 53-58.
35. SPEARE, R., LATASI, F. F., NELESONE, T., HARMEN, S., MELROSE, W., DURRHEIM, D. AND
HEUKELBACH, J., 2006. Prevalence of soil transmitted nematodes on Nukufetau, a remote Pacific island in
Tuvalu. BMC Infec. Dis., 6(110): 1-6.
36. SHAIKH, G.S., HARANI, M.S., RATHI, S.L., KHATRI, P.R. AND HARANI, P.K., 2000. Pattern of intestinal
Ancylostoma duodenale Seperated from Contaminated Soil 37
parasitic infestation in Larkana, Proc. Parasitol., 29: 61-66.
37. STEEL, R.G.D. AND TORRIE, J.H., 1980. Principles and Procedures Statistics. 2nd
Ed. McGraw Hill Books,
N.Y, pp.137-171.
38. ULUKANLIGI, M., SEYREK, A., ASLAN, G., OZBILGE, H. AND SULEYMAN, 2001. Environmental
pollution with Soil Transmitted Helminth in Sanliurfa, Turkey. Mem. Inst. Oswaldo Cruz. Rio de. Janeiro, 96(7):
903-909.
39. UNEKE, C.J., EZE, K.O., OYIBO, P.G., AZU, N.C. AND ALI, E. 2007. Soil-Transmitted Helminth Infection In
School Children In South-Eastern Nigeria: The Public Health Implication. Inter. J. Third World Med. ISSN:
1539-4646.
40. URQUHART, G.M., ARMOUR, J., DUNCAN, J.L., DUNN, A.M. AND JENNINGS, F.W. 2001. A Synoptical
review of life historics of digenetic trematode of vertebrates with special reference to the morphology of their
larvae. In: Veterinary Parasitology, Ed. ELBS Langman, UK Yamaguti. Keiguku Publishing Company, Tokyo,
Pp. 410-413.
41. VERLE, P., KONGS, A., NV, D., THIEU, N.Q., DEPRAETERE, K., KIM, H.T. AND DORNY, P., Prevalence
of intestinal parasitic infections in northern Vietnam. Trop. Med. Int. Health., 8(10): 961-4.
42. WHO (2011). First WHO Report on neglected tropical diseases: working to overcome the global impact of
neglected tropical diseases. Edited by; Crompton, D.W.T. ISBN 978 92 4 1564090. NLM Classification: WC 680.
Pp. 1-16.
43. ZEWDU, E., SEMAHEGN, , Y. AND MEKIBIB, B., 2011. Prevalence of helminth parasites of dogs and owners
awareness about zoonotic parasites in Ambo town, central Ethiopia. Ethiop. Vet. J., 14(2): 17-30.
44. ZIEGELBAUER, K., SPEICH, B., MAUSEZAHL, D., BOS, R., KEISER, J. AND UTZINGER, J., 2012. Effect
of Sanitation on Soil-Transmitted Helminth Infection: Systematic Review and Meta-Analysis. Iss.
PLoSMed.;Trop. Biomed., 28(2): 450–456.
Recommended