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ORIGINAL PAPER

Gastrointestinal and ectoparasites from urban stray dogs

in Fortaleza (Brazil): high infection risk for humans?

Sven Klimpel & Jrg Heukelbach & David Pothmann &

Sonja Rckert

Received: 4 May 2010 /Accepted: 18 May 2010 /Published online: 8 June 2010# Springer-Verlag 2010

Abstract Dogs are important definite or reservoir hosts for

zoonotic parasites. However, only few studies on theprevalence of intestinal parasites in urban areas in Brazil

are available. We performed a comprehensive study on

parasites of stray dogs in a Brazilian metropolitan area. We

included 46 stray dogs caught in the urban areas of

Fortaleza (northeast Brazil). After euthanization, dogs were

autopsied. Ectoparasites were collected, and the intestinal

content of dogs were examined for the presence of

parasites. Faecal samples were collected and analysed using

merthiolate iodine formaldehyde concentration method. Atotal of nine different parasite species were found, including

five endoparasite (one protozoan, one cestode and three

nematode species) and four ectoparasite species (two flea,

one louse and one tick species). In the intestinal content,

3,162 specimens of four helminth species were found:

Ancylostoma caninum (prevalence, 95.7%), Dipylidium

caninum (45.7%), Toxocara canis (8.7%) and Trichuris

vulpis (4.3%). A total of 394 ectoparasite specimens were

identified, including Rhipicephalus sanguineus (prevalence,

100.0%), Heterodoxus spiniger (67.4%), Ctenocephalides

canis (39.1%) and Ctenocephalides felis (17.4%). In the

faeces, intestinal parasites were detected in 38 stray dogs

(82.6%), including oocysts of Giardia sp. (2.2%) and eggs

of the nematode A. caninum (82.6%). Neither eggs nor

larval stages of D. caninum, T. canis or T. vulpis were

detected in dog faeces. Sensitivity of faecal examination for

A. caninum was 86.4% (95% confidence interval, 72.0

94.3) but zero percentage for the other intestinal helminth

species. Our data show that stray dogs in northeast Brazil

carry a multitude of zoonotic ecto- and endoparasites,

posing a considerable risk for humans. With the exception

of A. caninum, sensitivity of faecal examination was

negligible.

Introduction

It is generally known that dogs were first tamed then

domesticated from the wolf and that the relationship

between humans and dogs began in prehistoric times some

10,00014,000 years ago. In this time period, the co-

evolutionary process between humans and dogs became

probably well established in the early village-farming

S. Klimpel (*)

Biodiversity and Climate Research Centre (BiK-F),

Johann Wolfgang Goethe-University,Georg-Voigt-Str. 14-16,

60325 Frankfurt am Main, Germany

e-mail: sklimpel@gmx.net

J. Heukelbach

Department of Community Health, School of Medicine,

Federal University of Cear,

Rua Prof. Costa Mendes 1608, 5. andar,

Fortaleza CE 60430-140, Brazil

J. Heukelbach

Anton Breinl Centre for Tropical Medicine and Public Health,

School of Public Health, Tropical Medicine and Rehabilitation

Sciences, James Cook University,

Townsville, Qld 4811, Australia

D. Pothmann

Institute of Zoomorphology, Cell Biology and Parasitology,

Heinrich-Heine University,

Universittsstr. 1,

40225 Dsseldorf, Germany

S. Rckert

Departments of Botany and Zoology,

University of British Columbia,

#3529-6270 University Blvd.,

Vancouver, BC V6T 1R9, Canada

Parasitol Res (2010) 107:713719

DOI 10.1007/s00436-010-1926-7

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communities (e.g. Beck 2000; Matter and Daniels 2000).

To date, dogs play many roles in human societies such as

pets, guard dogs, hounds, sheepdogs, tracker dogs, guide

dogs, and as food source (Szabov et al. 2007). The dog

population in urban and suburban regions is composed of

dogs that roam only with their owners, stray dogs roaming

sporadically and ownerless dogs (Beck 2000). In all three

cases, the animals come into close contact with humans andtheir dwellings and act as reservoirs and transmitters of

zoonotic diseases (Traub et al. 2005; Gracenea et al. 2009).

Of the estimated 500 million dogs worldwide, about 400

million are stray dogs (Matter and Daniels 2000; WSPA

2009).

More than 250 zoonoses have been described world-

wide, caused by a wide variety of pathogens, including

viruses, bacteria, fungi and parasites (Glaser et al. 2000;

Moriello 2003). The fast majority of zoonotic reservoir

species are mammals, and most are domestic livestock

(chicken, ducks, cattle, sheep and pigs), carnivores (dogs

and cats) and rodents (mice and rats; e.g. Moriello 2003;Pedersen et al. 2005; Traub et al. 2005; Klimpel et al.

2007a,b). In this case, dogs play a pivotal role as definitive

or reservoir hosts for many zoonotic parasites, especially in

low income countries and also socio-economically disad-

vantaged communities in middle and high income countries

(Traub et al. 2002, 2005; Salb et al. 2008). Transmission to

humans can occur by swallowing or inhaling pathogens

from the animal reservoir hosts, eating the hosts or being

bitten. Parasites may also be transmitted from animals to

humans by vectors, such as fleas, ticks and mosquitoes

(Ostfeld and Holt 2004).

Typical helminthic parasites of dogs in tropical areas are

the hydatid tapeworm (Echinococcus granulosus), the

cucumber tapeworm (Dipylidium caninum), the dog round-

worm (Toxocara canis), the dog heartworm (Dirofilaria

immitis) and the dog hookworm (Ancylostoma caninum),

while the most frequent ectoparasites are chewing lices

(Trichodectes canis and Heterodoxus spiniger), the dog flea

(Ctenocephalides canis), the jigger or sand flea (Tunga

penetrans) and the brown dog tick (Rhipicephalus sangui-

neus; e.g. Klimpel et al. 2005; Irwin and Traub 2006;

Furtado et al. 2009).

The Brazilian dog population is estimated at 28 million

specimens including over 22 million stray dogs (Stevenson

2004). The high number of stray dogs was attributed to the

climate conditions and the great availability of food, likely

because of garbage scattered in the streets and the many

urban slums, the so-called favelas (Katagiri and Oliveira-

Sequeira 2008). However, only few studies on the

prevalence of intestinal parasites in urban areas in Brazil

are available. Usually, samples were collected from the

rectum of animals or after spontaneous excretion (Oliveira-

Sequeira et al. 2002), while comprehensive investigations

combining both faecal and intestinal analyses are missing.

The aim of the present study was to isolate and identify the

metazoan parasite fauna from stray dogs in a Brazilian

metropolitan area and to compare two analytical methods.

A comparative discussion of the analysed parasite fauna is

provided.

Materials and methods

Study area

The study was carried out in Fortaleza (347 S, 3835 W)

the state capital of Cear, located in northeast Brazil. The

climate is predominantly equatorial and tropical, with an

average annual temperature of 27.8C and relative air

humidity of 77.0%. According to the Brazilian Institute of

Geography and Statistics, the human population was more

than 2.4 million in 2007. Including the metropolitan areas

of Fortaleza, there are about 3.4 million inhabitants.Fortaleza has 402 favelas, of which 82 were classified as

high risk areas. The communities are characterised by poor

housing, crowding, precarious hygienic conditions, a high

rate of illiteracy, unemployment as well as garbage dumps

almost everywhere. Stray dogs are very common, and the

prevalence of zoonotic diseases such as tungiasis and

cutaneous larva migrans in such urban areas is high

(Heukelbach et al. 2003; Feldmeier and Heukelbach

2009). The present study was done at the Centre of Control

of Zoonotic Diseases (CCZ), run by the city council of

Fortaleza. Stray dogs are caught routinely in the urban areas

of Fortaleza by the council service and accommodated in

the CCZ. If dogs are not claimed or adopted within 8 days,

they are euthanised by CCZ staff.

Sample collection and examination for ecto-

and endoparasites

During May and August 2005, a total of 46 euthanised

stray dogs were autopsied. The dogs were examined for

ecto- and endoparasites, by analysing body surface, faecal

samples and intestinal content. Prior to examination, each

dog was photographed. Then, ears, coats, skin, nostrils and

perianal regions were examined for the presence of

ectoparasites, e.g. lice, ticks and fleas. In a next step, faecal

samples were collected from the dogs rectum and placed in

labelled sterile Petri dishes. The body cavities were then

opened and the intestinal tract removed for further

examination. The intestinal tract was separated from

surrounding fat tissue and placed in large plastic dishes

containing physiological saline solution. Subsequently, it

was separated into five portions of similar size, opened by a

longitudinal cut and examined for intestinal helminths.

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Isolated parasites were fixed in 4% borax-buffered formalin

and preserved in 70% ethanol/5% glycerine. For identi-

fication purposes, nematodes were dehydrated in a

gradated ethanol series and transferred to 100% glycerine

(Riemann 1988). Cestodes were stained with acetic

carmine, dehydrated, cleared with eugenol or creosote

and mounted in Canada balsam. For species determina-

tion, all ectoparasites were cleared in 10% potassiumhydroxide (KOH) solution over 12 h, dehydrated and

mounted in Canada balsam. Parasite identification litera-

ture included original descriptions.

Dog faeces were treated with the merthiolate iodine

formaldehyde (MIF) concentration method (Mehlhorn et al.

1993) and examined for parasites on a slide under a light

microscope. Eggs and cysts were identified by means of

morphological characteristics. A dog was classified as

positive if at least one parasite egg or cyst was observed.

The parasitological terms prevalence, mean intensity,

intensity and mean abundance followed the recommen-

dations of Bush et al. (1997): prevalence (P) is thenumber of infected dogs with one or more individuals of a

particular parasite species (or taxonomic group) divided

by the number of hosts examined; intensity (of infection,

I) is the number of individuals of a particular parasite

species in a single infected host (expressed as a numerical

range); mean intensity (of infection, mI) is the average

intensity (total number of parasites of a particular species

found in a sample divided by the number of infected

hosts); and mean abundance (A) is the total number of

individuals of a particular parasite species in a sample of a

particular host species divided by the total number of hosts

of that species examined, including both infected and

uninfected hosts.

Sensitivity of faecal examination as compared to autopsy

and the respective 95% confidence intervals were calculat-

ed using EPI INFO software, version 6.04d (Centers for

Disease Control and Prevenion, Atlanta, GA, USA).

Results

The 46 stray dogs consisted of 30 (65.2%) males and 16

(34.8%) females. A total of nine different parasite species

were found, including five endoparasite (one protozoan,

one cestode and three nematode species) and four ectopar-

asite species (two flea, one louse and one tick species;

Table 1 and Fig. 1). The dogs usually carried a total of twoto six parasite species (mean, 3.8). Separated in ecto- and

endoparasites, the dogs were seized with one to four (mean,

2.2) ectoparasite species, and the endoparasite species

ranged from 1 to 3 (mean, 1.6; Fig. 2).

Gastrointestinal parasite diversity

During the autopsies, a total 3,162 specimens of four

intestinal helminth species were found, including D.

caninum, A. caninum, T. canis and Trichuris vulpis. The

predominant parasite species were A. caninum and D.

caninum with a prevalence of infection of 95.7% and45.7%, respectively (Table 1 and Fig. 1).

Ectoparasite diversity

A total of 394 specimens of four ectoparasite species were

identified. The ectoparasite fauna was characterised by R.

sanguineus and H. spiniger with a high prevalence of

100.0% and 67.4%, respectively, followed by C. canis and

C. felis (Table 1, Fig. 1).

Faecal examinations

Intestinal parasites were found in the faeces of 38 (82.6%)

dogs, including oocysts of Giardia sp. (one specimen;

2.2%) and eggs of the nematode A. caninum (38; 82.6%).

One dog (2.2%) harboured both parasite species. Neither

eggs nor larval stages of the cestode D. caninum and the

Parasite species Total number P (%) I mI A

Cestoda

Dipylidium caninum 805 45.7 1367 38.3 17.50

Nematoda

Ancylostoma caninum 2,337 95.7 1660 53.1 50.80

Toxocara canis 12 8.7 24 3.0 0.26

Trichuris vulpis 8 4.3 35 4.0 0.17

Insecta

Ctenocephalides canis 40 39.1 16 2.2 0.87

Ctenocephalides felis 15 17.4 15 1.9 0.33

Heterodoxus spiniger 131 67.4 117 4.2 2.85

Arachnida

Rhipicephalus sanguineus 208 100.0 118 4.5 4.52

Table 1 Prevalence (P), inten-

sity (I), mean intensity (mI) and

mean abundance (A) of intesti-

nal helminths and ectoparasites

identified by autopsy of 46 stray

dogs in Fortaleza, Brazil

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nematodes T. canis and T. vulpis, which were isolated from

the examined gastrointestinal tracts, could be detected in

faecal examinations. The sensitivity of faecal examination

for the detection of A. caninum infection, as compared to

autopsy, was 86.4% (95% confidence interval, 72.094.3).

In both cases of negative autopsy results, faecal exams were

also negative. In contrast, sensitivity of faecal examination

was 0.0% for the other three helminth species.

Discussion

Throughout their long history of domestication, dogs play a

pivotal role as definitive hosts or reservoirs for different

zoonotic parasites, especially in developing countries and

communities that are socioeconomically disadvantaged

(Traub et al. 2002, 2005; Salb et al. 2008). Our data show

that some helminth and ectoparasite species were highly

prevalent in stray dogs from a Brazilian metropolitan area

but that other parasites, such as Echinococcous granulosus

and D. immitis, did not occur. Previous studies have shown

that in middle and southern parts of Brazil, most dogs were

infected with the cestode D. caninum, the nematodes T.

canis, A. caninum, D. immitis and Acanthocheilonema

reconditum, as well as the ectoparasites C. canis, T.

penetrans and R. sanguineus (e.g. Klimpel et al. 2005;

Dantas-Torres 2008a; Furtado et al. 2009).

A close and frequent contact between dogs and people

increases the risks for the transmission of zoonotic diseases.

Dog bites and their excrements contaminating the environ-

Fig. 1 Light micrographs of

different endo- and ectoparsites

isolated from stray dogs. a Em-

bryonated eggs within oncos-

phaera of the cestode

Dipylidium caninum (scale bar,

0.12 mm); b anterior end and a

part from the middle of the

nematode Ancylostoma caninum

(0.14 mm); c uterus filled withcharacteristic eggs of the nema-

tode Trichuris vulpis (0.75 mm);

d habitus of the flea species

Ctenocephalides canis

(0.70 mm); e lateral view of the

habitus of the lice species Het-

erodoxus spiniger (0.38 mm); f

ventral view of the habitus of

the tick species Rhipicephalus

sanguineus (0.65 mm). AB

abdomen, AN anus, ATantenna,

Ccaput, CL claw, Eegg, ESegg

shell, GC genal comb (with

several spines), H tooth with

hooks, HO hooks of oncos-phaera, HY hypostome, M

mouth part, MP maxillary palp,

OC ocellus, ON oncosphaera,

PC pronotal comb (with several

spines), PG pygidium, PH

pharynx, PP pedipalps, S seta,

STstigma

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ment are the commonest health hazards because the

developmental stages of the parasites (cysts, eggs and

larval stages) can survive in the environment for a long

time, mainly in tropical climates (Robertson et al. 2000).The nematodes identified from the gastrointestinal tract

of stray dogs in the present study may cause zoonotic

diseases and pose a risk for humans, such as T. canis, which

causes the visceral and ocular larva migrans, which may

lead to blindness and A. caninum causing hookworm-

related cutaneous larva migrans (Irwin and Traub 2006;

Andresiuk et al. 2007; Heukelbach and Hengge 2009). The

prevalence ofT. canis (8.7%) is comparable to that obtained

in previous studies with values of 8.7% (Katagiri and

Oliveira-Sequeira 2008), 8.5% (Gennari et al. 1999) and

5.5% (Oliveira-Sequeira et al. 2002).

In our study, 96% of dogs were infected with A.

caninum, but other hookworm species that may cause

cutaneous larva migrans, such as A. braziliense or Unci-

naria stenocephala, were not identified. Cutaneous larva

migrans is caused by the penetration of third stage (L3)

hookworm larvae into the skin of humans. In contrast to

animals, humans are dead-end hosts. The larvae do not

develop further but continue migrating in the skin for

weeks. Besides the ascarids, hookworms are the most

commonly found nematodes in carnivores in tropical

climates, where the abiotic conditions are conducive to

the nematode life cycle (Irwin and Traub 2006). Cutaneous

larva migrans occurs mainly in tropical areas and has also

been reported from temperate climatic regions (Heukelbach

and Hengge 2009). The condition is endemic in humans in

deprived communities (Heukelbach et al. 2004). The high

prevalence of hookworms in stray dogs in the present study

indicates that this condition could be more widely distrib-

uted than it is currently assumed. The present findings are

similar to previous studies from India, with values between

72.0% and 89.0% (Traub et al. 2005), but clearly higher

than in studies from south Brazil and central Nigeria, with

prevalences of 5.5% and 37.5%, respectively (Oliveira-

Sequeira et al. 2002; Ugbomoiko et al. 2008).

T. vulpis is distributed worldwide, but most prevalent in

warm, humid climates. Adult stages are found in theintestinal tract of their carnivorous hosts. In the present

study, the prevalence of infestation was low (4.3%)

compared with other studies. Segoiva et al. (2003) found

a higher prevalence of infestation (10.0%) with T. vulpis in

Canis lupus in Spain, while Katagiri and Oliveira-Sequeira

(2008) found a prevalence of 9.3% in stray dogs from Sa

Paulo State (southern Brazil). Humans become infected

with T. vulpis when they accidentally ingest embryonated

eggs, through contamination of infected soil, food or

fomites, but infections are rare (Dunn et al. 2002).

D. caninum is transmitted by arthropode intermediate

hosts such as fleas (C. canis, C. felis and Pulex irritans) and

lice (H. spiniger; Molina et al. 2003; Dantas-Torres 2008a).

In the life cycle of D. caninum, the final hosts are dogs and

wild carnivores, while humans are occasional hosts.

Recently, de Avelar et al. (2007) analysed the endosymbi-

ont fauna of 1,500 cat fleas isolated from 150 dogs in

Brazil. They were able to isolate six cysticercoids of D.

caninum from the analysed cat fleas with a prevalence of

infection of 0.4% (de Avelar et al. 2007). We identified

high prevalence of infection (45.7%) of D. caninum. This

stands in contrast to other stray dog studies from urban

sampling stations in south Brazil (Oliveira-Sequeira et al.

2002), Venezuela (Ramrez-Barrios et al. 2004) and Nigeria

(Ugbomoiko et al. 2008), with prevalences of 0.7%, 2.9%

and 9.1%. The high frequency of D. caninum observed in

the present study may be due to autopsies as a more

sensitive diagnostic method and also indicates that the

investigated stray dogs harboured a large infected flea

population facilitating transmission. However, in our study,

the infection rate of intermediate hosts (fleas and lice) was

not assessed due to logistic reasons, and thus the risk for

human populations cannot be assessed directly.

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

0

1

2

3

4

5

6

nparasite

species

n dogs

Ec/En

En

Ec

Fig. 2 Total number of parasite

species and infected dogs with

ecto- and/or endoparasites. Ec/

En ecto- plus endoparasites, En

endoparasites, Ec ectoparasites

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The fleas C. felis and C. canis are the most abundant

ectoparasites of dogs worldwide (Barutzki and Schaper

2003; Irwin and Traub 2006; Dantas-Torres 2008a,b;

Xhaxhiu et al. 2009). In our study, the tick R. sanguineus

and the lice H. spiniger were the most abundant ectopar-

asites, followed by the fleas C. felis and C. canis.

Contrary to other studies, we could find both flea species

in single as well as double infestations. In Nigeria andArgentina, only C. canis were isolated from the investi-

gated dogs (Gonzlez et al. 2004; Ugbomoiko et al. 2008).

The fleas life stages are strongly influenced by microcli-

mate, and different studies have shown that flea survival is

compromised at extreme environmental conditions (Rust

2005). Furthermore, the absence of C. felis in other studies

on dog parasites may be a result of misidentification of the

flea species, as morphological differences are subtle. Low

infestation rates for C. canis in the present study in

contrast to data from other studies are attributable to the

sampling procedures. Ectoparasites leave their dead hosts

after a certain amount of time or they may also die, andthus a certain number of fleas may not have been detected

in the euthanised dogs.

Many different tick species have been identified on dogs.

Especially species of the family Ixodidae are valuable

vectors of different pathogens and of veterinary and also

public health importance (Dantas-Torres 2008b; Otranto et

al. 2009). In Europe, the most prevalent tick species on

dogs are Ixodes ricinus and Dermacentor reticulatus with a

wide zoogeographical range. R. sanguineus is the most

cosmopolitan tick species of dogs and reported mainly from

tropical countries such as Brazil (Dantas-Torres 2008b).

Adults of this three-host tick feed almost exclusively on

dogs, but all development stages can be found occasionally

on other wild (e.g. rodents) and domesticated mammalian

hosts, including humans (Dantas-Torres 2008a,b). Recent

data indicate that R. sanguineus is the vector of a wide

range of pathogens including the genera Babesia, Hepato-

zoon, Ehrlichia, Rickettsia and Mycoplasma (e.g. Otranto et

al. 2009). In Brazil, this species is involved in the

transmission of at least nine pathogens affecting dogs,

some of them with zoonotic potential (Dantas-Torres

2008a). However, infections of ticks with potentially

zoonotic bacteria or parasites were not further analysed in

the present study.

Our data indicate that faecal examination, even in a high

risk dog population such as stray dogs in Brazilwith the

exception of hookworm infectionis not an adequate

means to conclude on the infection rates in the animals

and consequently on the risk for zoonotic transmission to

humans. Sensitivity of faecal examination was high in the

case of hookworm infection but low for the other helminth

species. In case of T. canis and T. vulpis, this may be

explained by the low intensity of infection as compared to

that of A. caninum. In addition, the MIF concentration

method is not adequate to detect the cestode D. caninum in

faeces (Mehlhorn et al. 1993). In our study population,

ectoparasites were abundant. However, the calculated

infestation rates for ectoparasites are underestimating the

real values. The total number of parasite species is insecure

due to sampling and handling procedures.

In summary, the present study has shown that straydogs in Fortaleza carry a multitude of ecto- and endo-

parasites, thus posing a risk for the human population.

Adequate diagnostic methods need to be applied when

planning surveys on prevalence and intensity of infections

in dogs.

Acknowledgements We thank the head, Evansia Alves Ventura, and

the staff of the Centro do Controle de Zoonoses of Fortaleza for

supporting our study. Mirela Costa de Miranda, Eduardo Rebouas

Carvalho and Francisco Iure Sampaio Lira assisted in the autopsies.

J.H. is research fellow from the Conselho Nacional de Desenvolvi-

mento Cientfico e Tecnolgico (CNPq/Brazil).

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