Parasitol Res (2010) 107:713719 DOI 10.

1007/s00436-010-1926-7

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 the prevalence 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

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

parasites. Faecal samples were collected and analysed using merthiolate iodine formaldehyde concentration method. A total 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 coevolutionary process between humans and dogs became probably well established in the early village-farming

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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 and their 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 worldwide, 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 disadvantaged 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 roundworm (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 sanguineus; 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 OliveiraSequeira 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 (OliveiraSequeira 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 ectoand 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 identification 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 determination, all ectoparasites were cleared in 10% potassium hydroxide (KOH) solution over 12 h, dehydrated and mounted in Canada balsam. Parasite identification literature 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 recommendations of Bush et al. (1997): prevalence (P) is the number 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 calculated using EPI INFO software, version 6.04d (Centers for Disease Control and Prevenion, Atlanta, GA, USA).
Table 1 Prevalence (P), intensity (I), mean intensity (mI) and mean abundance (A) of intestinal helminths and ectoparasites identified by autopsy of 46 stray dogs in Fortaleza, Brazil Parasite species Cestoda Dipylidium caninum Nematoda Ancylostoma caninum Toxocara canis Trichuris vulpis Insecta Ctenocephalides canis Ctenocephalides felis Heterodoxus spiniger Arachnida Rhipicephalus sanguineus

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 ectoparasite species (two flea, one louse and one tick species; Table 1 and Fig. 1). The dogs usually carried a total of two to 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% and 45.7%, 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
Total number P (%) I mI A

805 2,337 12 8 40 15 131 208

45.7 95.7 8.7 4.3 39.1 17.4 67.4 100.0

1367 1660 24 35 16 15 117 118

38.3 53.1 3.0 4.0 2.2 1.9 4.2 4.5

17.50 50.80 0.26 0.17 0.87 0.33 2.85 4.52

716 Fig. 1 Light micrographs of different endo- and ectoparsites isolated from stray dogs. a Embryonated eggs within oncosphaera 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 with characteristic eggs of the nematode 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 Heterodoxus spiniger (0.38 mm); f ventral view of the habitus of the tick species Rhipicephalus sanguineus (0.65 mm). AB abdomen, AN anus, AT antenna, C caput, CL claw, E egg, ES egg shell, GC genal comb (with several spines), H tooth with hooks, HO hooks of oncosphaera, 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, ST stigma

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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-

Parasitol Res (2010) 107:713719 Fig. 2 Total number of parasite species and infected dogs with ecto- and/or endoparasites. Ec/ En ecto- plus endoparasites, En endoparasites, Ec ectoparasites
n parasite species

717
Ec/En 6 En 5 4 3 2 1 0 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 n dogs Ec

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 hookwormrelated cutaneous larva migrans (Irwin and Traub 2006; Andresiuk et al. 2007; Heukelbach and Hengge 2009). The prevalence of T. 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 Uncinaria 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 distributed 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 (OliveiraSequeira et al. 2002; Ugbomoiko et al. 2008). T. vulpis is distributed worldwide, but most prevalent in warm, humid climates. Adult stages are found in the intestinal 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 endosymbiont 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.

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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 ectoparasites, 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 and Argentina, only C. canis were isolated from the investigated dogs (Gonzlez et al. 2004; Ugbomoiko et al. 2008). The fleas life stages are strongly influenced by microclimate, 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, and thus 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, Hepatozoon, 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 stray dogs in Fortaleza carry a multitude of ecto- and endoparasites, 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 Desenvolvimento Cientfico e Tecnolgico (CNPq/Brazil).

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