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REVIEW ARTICLE Parasitic Zoonoses and Role of Wildlife: An Overview

M. B. Chhabra 1 and K. Muraleedharan 2*

1Professor and Head (Retired), Department of , College of Veterinary Sciences, Hisar-125 004, Haryana, 2Professor, University Head and Professor (Retired), University of Agricultural Sciences, Bengaluru- 560 065, Karnataka, India

Present address 1: 2518, Sector D-2, Vasant Kunj, New Delhi-110 070, India ([email protected]). Present address 2: No. B-3, Yasoram Tejus Apartments, Vennala High School Road, Vennala, Kochi-682 028, Kerala, India.

Abstract A significant proportion of emerging diseases caused by various infectious agents including parasites, are of wildlife origin. This

*Corresponding Author: disease emergence has resulted from increasing interaction between wild- life and or domestic . Several factors, mostly anthropogenic K. Muraleedharan like human encroachment into wildlife and changing ecosystems, have contributed to this trend. The heightened interest coupled with Email: [email protected] improved diagnostic techniques has led to increased information flow in the form of published reports and reviews. The objective of the present review is to compile an update and highlight some of the emerging and re- emerging parasitic zoonoses of wildlife origin which are of global concern. Received: 21/02/2016 Brief notes on the present status of zoonotic parasites recorded in different

wildlife in India and the sporadic human case reports of such Revised: 06/03/2016 etiology, are also included. The creation of awareness among public at risk, Accepted: 09/03/2016 and strategies for effective monitoring, surveillance and management of disease in wild populations should be implemented, in line with the ‘one health’ concept.

Key words : Zoonoses, Wildlife, Emerging diseases, Parasitic , Protozoa, Helminths and arthropods.

1. Introduction ecological factors, mostly those associated with human The importance and recognition of free-ranging activities (anthropogenic), have influenced the epi- animals and birds as a major source of emerging demiology of zoonoses having wildlife reservoir. These human pathogenesis are increasing (Daszak et al ., include human population expansion, mobility and 2000; Polley, 2005). Zoonoses affect human health deforestation with elimination/shrinkage of wildlife adversely and wildlife have historically played a role in habitat. As a consequence of human intrusions, there their transmission, such as for bubonic plague, a has been a shift in the interface between wildlife and bacterial disease, or wild canids for rabies virus. people, from sporadic to more permanent and intense Ancient accounts and modern hypothesis suggest that (Polley, 2005). Increased interactions between humans Alexander the Great, who died in Babylon in 323 BC, and their domestic animals on one hand, and the died due to encephalitis caused by West Nile virus wildlife on the other, can create “spill-over” situations (Kruse et al ., 2004) which has wild bird reservoir. In from domestic reservoir to sympatric wildlife recent times, many human pathogens of varied (Thompson et al ., 2009). Such “spill-over” can lead to taxonomies have been found to originate in animals, creation of wildlife reservoir which may have potential several of which were wild. Of the approximately 1500 for spill-back to humans and domestic animals. The presently known human disease agents, an estimated role of wildlife as significant sources, reservoir and 65% to over 75% are of zoonotic origin (Mathews, amplifiers of emerging as well as well-recognized 2009; Mackenstedt et al ., 2015). Moreover, most zoonoses of public health significance has gained emerging infectious diseases, bacterial, viral, rickettsial considerable attention in recent times (Thompson et al ., and parasitic, in humans are zoonoses with 2009; Carmena and Cardona, 2014). involvement of wildlife in their epidemiology. Several

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview

2. Zoonotic Protozoa Associated with animals including C. canis, C. meleagridis and C. felis , Wildlife have occasionally been identified in humans. Of these, Advances in molecular techniques have greatly C. meleagridis is increasingly recognized as being an aided in separating morphologically indistinguishable important human, rather than pathogen. species and genotypes. These technologies are also Wildlife contributes to the overall pool of oocysts greatly improving our ability to follow parasitic flow identified in environmental samples but their among population and providing insight into significance as source for human is uncertain. transmission pathways. Cryptosporidium oocysts have been detected in marine water samples and occasionally in marine hosts. Additionally shellfish like oysters and mussels 2.1 Giardia have been demonstrated to harbour the parasites. Several wildlife species are parasitized and are A study on the epidemiological and molecular often considered reservoir of zoonotic diseases relationships of Cryptosporidium spp. in people, (Appelbee et al ., 2005). Wildlife can harbour both primates and livestock in the region of a national park host-adapted and zoonotic strains of Giardia . The in Western Uganda (Salyer et al ., 2012) concluded that zoonotic genotypes of G. duodenalis –Assemblage A the parasite may be transmitted frequently among and Assemblage B have been detected in several species where people, livestock and wildlife interact wildlife species that encompass nearly all mammalian intensively as a result of anthropogenic changes to orders. Studies in North America have identified forests. Even though of Cryptosporidium has marine like seals, as a potential source of been unsettled, 30 species are currently recognized zoonotic transmission of Giardia . Cysts have also been valid, of which at least 14 are predominantly zoonotic detected in marine water samples. Shellfish like oysters (Slapeta, 2013). and mussels have been demonstrated to harbour

Giardia . Wildlife is considered an important contributor, together with humans, domestic animals 2.3 Toxoplasma and livestock, to the pool of parasites within the The presence of zoonotic protozoa including environment, but the significance of wildlife as a major Toxoplasma in marine ecosystems, in a variety of source is uncertain. marine mammals (Fayer et al ., 2004) is of increasing Molecular typing has found most evidence to interest, as there are vast populations dependent on suggest that more often the spill-over is from domestic marine mammals for food. Human encroachment into cycle to wildlife populations. For example, beavers in wildlife can also play a role in the spread of North America are susceptible to zoonotic strains of Toxoplasma . It has happened in fatal infection of sea Giardia (Thompson et al ., 2004) and were found to be otters in USA due to terrestrial water run-off getting infected from drinking water contaminated with contaminated with cat faeces (Conrad et al ., 2005). Giardia cysts downstream from a sewage works. Similar is the case of Australian wildlife fauna, Similar examples of establishment and maintenance of particularly marsupials in which Toxoplasma may have a sylvatic cycle exist in the finding of Giardia in been introduced initially by humans and their cats, but mountain gorillas in a national park in Uganda; and of is now widespread. However, molecular tools for G. duodenalis –Assemblage A in musk oxen among genetic characterization of the parasite will reveal other ungulates indigenous to arctic tundra of Canada whether identical or separate genotypes/strains exist and Greenland (Thompson et al ., 2009). Available and interaction, if any, between domestic and wildlife evidence also suggests that wildlife, especially wild cycles. Identification of genetic diversity including new rodents and cervids, can act as amplifiers of G. strains/genotypes in wildlife, particularly in marine duodenalis assemblages specific to other hosts (Otranto mammals (like whales, sea otters, seals, dolphins) and et al ., 2015a). marsupials and avian species, is a priority. This will provide clues to whether distinct domestic and sylvatic 2.2 Cryptosporidium parasitic gene pools exist and do they overlap indicating regions of probability of disease emergence As was the case with Giardia , earlier wildlife (Wendte et al ., 2011). were thought to harbour both host-adapted and Wildlife is susceptible to infection which in zoonotic Cryptosporidium (Appelbee et al ., 2005). most cases leads to chronic asymptomatic infection. Application of molecular tools revealed that majority Occasionally, there may be clinical consequence and of Cryptosporidium found in naturally infected wild- or effects on the nervous system leading to life, is different from those infecting human hosts. increased susceptibility to predation. In particular, Humans are primarily infected with C. hominis and C. identification of new, disease-causing strains in parvum . Other species, traditionally associated with wildlife has raised concerns from both conservation

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd 2 Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview and public health perspectives (Wendte et al ., 2011). knowlesi infections have been reported from wide areas The maintenance of Toxoplasma in wildlife ecosystems of SE Asia including , , Indonesia, is considered to result from environmental and (Conlan et al., 2011). These contamination from wild or domestic felids authors opined that the rapid increase in frequency of (Thompson, 2013). Other wildlife contributes to reports may not likely represent an emerging disease, maintain Toxoplasma in the environment via tissue but represents an emerging awareness of P. knowlesi . cysts, which represents a source of infection for Further work from Sarawak, Malaysia suggests that P. predators/scavengers, and of transmission to the knowlesi has another simian wildlife host viz. -tailed offspring (Otranto et al ., 2015a). macaque ( M. nemestrina ). Transmission to humans who visit the forest canopy, occurs through the bite of 2.4 Leishmania and Trypanosoma Anopheles latens mosquitoes (Vythilingam et al., The vector-borne flagellate protozoan parasite 2006). Simian malaria is virulent and fatalities in Leishmania has numerous species and variants, some humans have been recorded (Galinsky and Barnwell, of which affect a variety of wildlife mammalian hosts. 2009). Recent evidence suggests that a species of Leishmania parasitizes kangaroos in Northern Territory of 2.6 Sarcocystis spp. Australia, which could be a source of infection to This is one of the ‘new’ parasitic zoonoses humans (Rose et al., 2004). This finding presumes the arising as a result of human activity (Thompson, 2013). presence of sandflies capable of vector-role in Human muscular sarcocytosis is a zoonotic infection of Australia for imported cases of regular human which an initial cluster of symptomatic cases was Leishmania species and poses a risk of transmission. reported in 1999 affecting 7 US servicemen on The closely related group of vector-borne manoeuvres in a rural remote Malaysian jungle (Arness flagellates of Trypanosoma has also been et al., 1999). In 2011, GeoSentinel Surveillance recorded in marsupials (Smith et al., 2008). This could System, United States identified 32 cases of suspected have the potential to impact health of wildlife but also acute muscular sarcocystosis in travellers returning lead to establishment of a reservoir in wildlife for from Tioman Island off the east coast of peninsular exotic pathogenic trypanosomes like T. cruzi and T. Malaysia (Sonenburg et al ., 2012). By November 2012, brucei. For the latter, human disease has primarily been the number of patients identified in the ongoing the result of a spill-back from wildlife reservoirs. In outbreak associated with travel to Tioman Island had consequence, wildlife conservation and biodiversity reached 100 (Esposito et al ., 2012). Sarcocyst campaign have usually been in conflict with the re- formation provoked eosinophilic myositis in this emergence threat, as wildlife (alongside domestic outbreak, and muscle biopsy demonstrated organisms animals) constitutes an important reservoir of T. brucei consistent with sarcocytosis (Tappe et al ., 2013). rhodesiense and T. brucei gambiense in sub-Saharan According to these workers, the source of infection in (Stich et al., 2003). Malaysia remains to be elucidated but seems to be Trypanosoma cruzi has exhibited marked persisting. Further, food or water contaminated with genetic diversity reflected in differences in host oocysts or sporocysts from faeces of the animal host, specificity which include a wide range of wildlife yet to be identified, are the most likely source of species. Socio-economic factors and close proximity to infection. wildlife habitats provide the reservoir of T. cruzi infection (Karesh et al., 2012). The emerging problem 3. Zoonotic Helminths Involving Wildlife with Chagas disease is globalization (Hotez et al., Emphasis here is on some prominent examples 2012) through migration of millions of infected persons of clearly defined transmission pathways or those to non-endemic regions. which pose significant threat to human health and well- being. 2.5 Plasmodium knowlesi P. knowlesi is regarded as the most important 3.1 Echinococcus spp. vector-borne zoonotic protozoan in Southeast Asia is one of the 17 neglected (Conlan et al., 2011). First identified in Calcutta in tropical diseases listed by the WHO, has a 1931 from a primate, it was rediscovered as a common cosmopolitan distribution and can be transmitted human pathogen in 2004 (Singh et al., 2004) with long- through a variety of domestic, synanthropic and tailed macaque, Macaca fascicularis as the wild host. sylvatic cycles. Bases on available epidemiological and During an investigation of malaria patients in molecular evidence, E. canadensis G8-G10, E. felidis, peninsular Malaysia, 120 of 208 patients tested positive E. multilocularis , E. oligarthrus , E. shiquicus and E. by PCR-assay for P. knowlesi . Since then, human P.

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd 3 Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview vogeli are primarily transmitted in the wild (Carmena but may also represent a source of infection for feral and Cardona, 2014). E. granulosus which has a cats and stray dogs thereby increasing the chances of domestic cycle infecting livestock and dogs, and to human infection. Infection by O. felineus is of public which humans are susceptible to the cystic stage has health concern in Asia and Eastern Europe, and is re- established a widespread prevalence in Australia emerging in Italy (De Liberato et al ., 2011; Pozio et al ., cycling between macropod marsupials and the wild 2013). canids, “dingo” and foxes. The prevalence of E. granulosus in wild dogs encroaching into peri-urban 3.3 Trichinella spp. and urban areas is as high as 46.3% (Jenkins et al ., Nematode worms of the genus Trichinella are 2008) and 45.8% in foxes. The wild canids also act as one of the most widespread zoonotic pathogens “spill-back” reservoir of infection (Thompson et al ., worldwide (Pozio, 2007). Cultural eating habits of raw 2009). Wild animals are also potential sources of or undercooked meat of infected animals represent the human infection with E. granulosus , E. vogeli and main factor favouring human infection (Pozio, 2013). possibly, E. shiquicus and wild felids for E. oligarthrus Globally, most Trichinella infections occur in wildlife (Polley, 2005). In Canada, G8 and G10 forms (cervid documented in 66 countries as against 43 countries for strains) are endemic and are maintained by sylvatic domestic animals. A wide range of wildlife fauna cycle between wild cervids, primarily moose, and wild (mammals, reptiles, birds) may be carriers of carnivores, primarily wolves. Domestic dogs may Trichinella . For example, Trichinella sp. larvae have become infected through consumption of organs of E. been detected in bears, foxes, wild boars, weasels, granulosus infected cervids. Emergence of these raccoon dogs and a variety of rodents in (Wang parasitic zoonoses is of public health concern because et al ., 2007) where it is one of the most important food- indigenous communities hunt wild cervids for food and borne zoonoses, with several outbreaks and also maintain large numbers of free-roaming dogs reported each year. As such, there is a constant (Himsworth et al ., 2010). challenge of spillover from wildlife to domestic foci E. multilocularis primarily maintained in a wild and human infections from hunted wildlife are on the cycle involving foxes and arvicolid rodents. Spill-over rise (Thompson, 2013). to humans results in severe disease, alveolar echinococcosis (Hegglin and Deplazes, 2013). It has 3.4 procyonis emerged as a major urban as a result of The common ascarid nematode of raccoons various anthropogenic factors like deforestation, (and dogs), poses serious threat to humans in North landscape changes and agricultural practices which America and in Europe where raccoons introduced in have led to more favourable conditions for the increase early 20 th century, have become well-adapted. In the in rodent populations. The parasite can be introduced course of thriving in Europe, some populations of into non-endemic areas via travelling dogs or raccoons have adapted to peri-urban and urban areas. translocated wild animals (Davidson et al ., 2012). The eggs of B. procyonis passed in raccoons’ faeces Synanthropic fox populations and those from surround- may remain infectious for four months in humid soil ing rural areas that also exploit anthropogenic food and water (Kazakos, 2001). Humans may acquire sources (Deplazes et al ., 2004). In central Europe, E. infection by uptake of embryonated eggs from multilocularis predominantly cycles between voles and contaminated environment. In humans, the larval stages wild animals including red foxes ( Vulpis vulpis ) as may cause ocular and visceral migrans, which main definitive hosts. Fox population increase (4-fold may become fatal if larvae invade the central nervous 1980 to 1995) in Switzerland as a consequence of anti- system. B. procyonis as parasite and the clinical disease rabies vaccination may have resulted in an emerging it causes in man, are likely underdiagnosed (Sorvillo et epidemic of alveolar echinococcosis, 10-15 year later al ., 2002). The synanthropic behaviour of raccoons has (Schweiger et al ., 2007). exacerbated the public health significance of B. procyonis in USA also (Kellnar et al ., 2012). At the 3.2 felineus same time, the parasite’s low host-specificity and the The parasite occurs in domestic (cats and dogs) pathogenic effect of its migrating larvae is considered and wild mammals (red foxes, pole cats). These hosts to be potential threat to vulnerable species of wildlife acquire the infection by -eating and contribute to (Page, 2013). maintaining parasite’s life cycle by passing embryo- nated eggs in faeces. Proximity of fresh water bodies 3.5 callipaeda increases the chances of being taken up for further Commonly known as the “Oriental eyeworm”, development in a suitable intermediate host. Fish- T. callipaeda infests primarily dogs in the Asian Far eating wildlife can propagate O. felineus on their own

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East. However, in recent years the parasite has been zoonotic and human cases of infection by D. repens are increasingly detected in dogs, red foxes, wolves and increasingly reported in Europe (Otranto et al ., 2015b). beech martens, in several countries of Europe (Otranto D. immitis infections have been reported in a variety of et al ., 2015b). Human infection is prevalent in highly wild felids in their natural habitats as well as in endemic areas like China (Shen et al ., 2006) and has captivity. However, microfilaremia in them was lately also been described in some southern European inconsistent or insufficient to suggest a reservoir role. countries (Otranto and Dutto, 2008; Fuentes et al ., On the other hand, wild canids appeared more 2012). consistent as reservoir hosts for Dirofilaria . For example, coyotes in USA, and jackals and wolves in 3.6 Toxocara sp. Europe were found to harbour microfilariae and/or Domestic and wild canids (dogs and foxes) and adult worms. felids are natural hosts for T. canis and T. cati , respectively. In Europe, human behaviour and 4. Outbreaks of Parasitic Zoonoses from urbanization has resulted in thinning boundaries Wild-life Sources between wild canids and felids, and their domestic Several outbreaks have been recorded from time counterparts (Otranto et al ., 2015a). T. canis to time, mainly of protozoan and helminthic etiology, roundworms have been recorded from red foxes, in various countries. It is of interest and relevance to golden jackals and wolves in various countries of enlist here some recent instances (Table 1). Europe (Otranto et al ., 2015b) and in wild dogs and foxes in Australia (Mackenstedt et al ., 2015). It is 5. Arthropod Zoonoses and Wildlife speculated that foxes play a major role in the Polley (2005) had listed several arthropod maintenance of the wildlife cycle due to their predatory parasites which have wildlife host(s) and human nature: preying on paratenic hosts, including rodents, infections may be acquired by flow through the birds and invertebrates. Moreover, their urbanization environment: other people and/ or domestic animals, as and increased population in Europe strengthens the risk well as wildlife. Most of them were various myiasis- they pose. T. canis can cause ocular and visceral larva causing flies whose hosts include wildlife mammals migrans. and birds, and larvae invade skin, wounds and nasal

chambers. Pentastomids like Linguatula and Armilifer 3.7 Ancylostoma sp. are parasites of canids and snakes, respectively and the A. caninum and Uncinaria stenocephala are route of human infections is through of cosmopolitan of dogs and other canids. infective eggs on food or in water. Several mite species Wild carnivore populations like the red foxes, golden and fleas originating from wild mammals and birds jackals and wolves in several European countries, play may spread to humans by direct contact or through role as reservoirs for one or both of these fomites. The most important and widespread is species. A. ceylanicum and A. brasiliense also occur Sarcoptes scabiei or scabies mite which is a genuine but in more tropical areas (Palmer et al ., 2007). The emergence resulting from higher incidence or increased hookworms are zoonotic as their larvae while detection. S. scabiei has been recovered from migrating through the skin in human hosts, may result approximately 100 species of free-ranging mammals in , also known as ‘creeping (Bornstein et al ., 2001). Human infections from eruptions’ (Bowman et al ., 2010). A. ceylanicum is able wildlife may be acquired the usual way, that is, close to cause patent enteric infection in humans, as in contact with infected animals or fomites. Scabies is dingoes of Cairns district of Queensland, Australia also regarded as a potentially significant threat to the (Smout et al ., 2013). It is likely that wildlife species health and even existence of certain endangered acting as hosts for these parasites may be contributing wildlife populations (Pence and Ueckermann, 2002). to the contamination of environment and thus Ticks, mosquitoes and fleas are important vectors in promoting transmission among wildlife, dogs and the transmission of pathogens including parasites, humans, particularly dog-walkers (Smith et al ., 2014). several of which are zoonotic. The ticks especially Ixodes spp. are highly important vectors in Europe. 3.8 Dirofilaria spp. Three species of Babesia , B. microti , B. venatorum and D. immitis and D. repens are common parasites B. capreoli were detected in ticks in the natural of domestic carnivores, such as dogs and cats as well as environment, while B. venatorum was more frequent in of wild carnivores and humans (McCall et al ., 2008). the pasture and the urban habitats. Significantly, B. While D. immitis has worldwide distribution, D. repens venatorum may infect human and roe is endemic in most of the old world. Both species are

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd 5 Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview

Table 1: Some Recent Outbreaks of Parasitic Zoonoses from Wildlife Sources

Parasitic zoonoses Wildlife source Route of human Locality References infection Leishmaniasis Hares ( Lepus spp.) Sand fly bite Spain Arce et al ., 2013; Millan et al., 2014 Black rats ( Rattus Sand fly bite Northern Israel Jacobson et al ., 2003 rattus ) and several wild carnivores Toxoplasmosis Cougars Water contamin- Victoria (B C), Bowie et al ., 1997 ated with infected Canada oocysts Simian malaria Macaques Mosquitoes Malayasia Singh et al ., 2004 (Plasmodium (Anopheles latens ) knowlesi ) bite Muscular Unknown Food or water Tioman Island Esposito et al ., 2012; sarcocytosis definitive host contaminated with (off the east Sonenburg et al ., 2012; (Eosinophilic f aeces of infected coast Tappe et al ., 2013 myositis) predator animal of Malaysia) Perch fillets (raw) Eating raw/ Switzerland Jackson et al ., 2007 marinated fish Eosinophilic Rats ( Rattus Ingestion of Jamaica Lindo et al ., 2002; meningitis norvegicus and R. infected larvae on (Caribbean) Slom et al ., 2002 (Angiostrongylus rattus ) salad cantonensis ) Baylisascariasis (B. Raccoons Ingestion of California, Russerie et al ., 2003 procyonis ) infected eggs from USA environment

Trichinellosis Bear Consumption of Sasketchewen Schellenberg et al ., 2003; (Trichinella nativa ) infected meat (Canada) Houze et al ., 2009

Trichinellosis Wild pig Consumption of Thailand Khumjui et al ., 2008; (T. papuae ) uncooked infected Kusolsuk et al ., 2010 pork deer are reservoir hosts of the parasite (Mackenstedt et specific instances of zoonotic transmission from al ., 2015). wildlife sources, deserve a mention. A case report of amoebic dysentery in a two month old dog at Anand in 6. Indian Scenario Gujarat (Jani and Dave, 1992) wherein the apparent In India, various reports on parasitic prevalence source was a naturally affected monkey excreting base on coproscopy or autopsy, have been documented -tinged stools containing Entamoeba histolytica on wild animals and birds in captivity of zoological cysts. Plasmodium knowlesi malaria which has been gardens or free-ranging in national parks/sanctuaries. reported endemic in a vast territory of SE Asia The information has been compiled in two including Burma/China border and for which the comprehensive reviews recently (Chhabra and Pathak, macaque reservoir M. fasicularis are found in Indian 2013a and 2013b). Based on these records, the zoonotic Nicobar Island and (Cox-Singh and Singh, parasites are listed here (Table 2). More recently, 2008) is a potential threat. Several findings of hydatid Moudgil et al . (2015) have reviewed the parasites in cysts with protoscolices in wild herbivores, mainly wild felids, confirming that most of the parasitic cervids, were reported (Arora and Chakraborty, 2009). species in these hosts are of public health significance. A cluster of 15 human cases of eosinophilic meningo- Toxoplasma oocysts in the felid faeces were a encephalitis/meningitis due to larval migration of conspicuous absence/omission. Apart from these, some Angiostrongylus cantonensis from eating raw flesh of a

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd 6 Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview

Table 2: Zoonotic parasites prevalent in wildlife in India (Based on authentic records: mostly autopsy)

S. Parasite Human disease Disease syndrome Wildlife species No. (Potential reservoir) 1 Giardia spp. Giardiasis Foul smelling Non-human primates 2. Entamoeba histolytica Amoebiasis Dysentery Non-human primates 3. Balantidium coli Balantidiasis Diarrhoea and other One-horned rhino, blue bull abdominal (Boselaphus tragocamelis ), symptoms giraffe, non-human primates 4. Babesia spp. Babesiosis Pyrexia, anaemia, American bison (in zoo), wild muscular pain felids, mongoose 5. Toxoplasma gondii Toxoplasmosis Abortion, congenital Non-human primates disease, chorio- retinitis 6. Dicrocoelium spp. Dicrocoeliasis Digestive disorders Spotted deer ( Axis axis ) 7. Paragonimus spp. Pulmonary disease, All wild felids ( tiger, cough, thoracic pain lion, panther, golden cat, civet cat, striped hyaena, mongoose 8. Nanophyetus salmincola Nanophyetiasis Occasionally gastro- Lion, leopard, panther, Indian intestinal symptoms civet, palm civet, jackal and eosinophilia 9. Echinostoma spp. Echinostomiasis Abdominal distress Wild/zoo birds, wild cat ( Felis and eosinophilia chaus ), palm civet 10. / Fascioliasis Hepato-biliary Wild cervids, Kashmere goat F. gigantica (Capra sibrica ), one-horned rhino, hippopotamus, non- human primates, elephant 11 buski Mainly gastro- intestinal symptoms 12 Gastrodiscoides hominis Gastrodiscoidiasis Enteritis in heavy Wild boar, non-human infections primates 13 Echinococcus spp. Hydatidosis Depends on location Jackal, wolf, leopard cat of metacestode, (Prionailurus bengalensis ), mostly hepatic or pulmonary 13 a Hydatid cyst Hydatidosis Depends on location One-horned rhino, spotted of metacestode, deer, mountain goat (ibex), mostly hepatic or giraffe, non-human primates pulmonary 14 Diphyllobothrium spp. Diphyllobothriasis Gastro-intestinal Wild cat, leopard, panther, symptoms, striped hyaena B12 anaemia 15 Hymenolepis diminuta Gastro-intestinal Non-human primates symptoms 16 Spirometra spp. Depends on location Wild cat, leopard, panther, of larvae, eye, CNS, civet cat, clouded leopard, kidney non-human primates 17 Dipylidium caninum Dipylidiasis Digestive disorders Wild dog, striped hyaena fox, jackal, panther, leopard 18 Ancyclostoma caninum Cutaneous larva Creeping eruptions Wild dog, fox, hyaena, wolf, migrans bear, lion, panther, civet 18a A. braziliense Cutaneous larva Creeping eruptions Leopard cat, Bengal tiger, migrans hyaena

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19 /T. cati Visceral larva Eosinophilia, Wild canids and felids migrans granulomatous reactions, ocular, neurological 20 Strongyloides spp. Pruritis, oedema, Bengal tiger, lion, panther, abdominal palm civet, wild boar, non- and pulmonary human primates, wild ass, cervids, rock python 21 spp. Trichostrongyliasis Occasionally gastro- Wild ass, cervids intestinal symptoms and anaemia 22 Capillaria aerophila Capillariasis Pulmonary: Fox, dog, wild cat, leopard cough, dyspnoea, eosinophilia 23 Gnathostoma spingerum Cutaneous or Bengal tiger, leopard, wild cat visceral, serpiginous eruptions, intraocular G. hispidum Gnathostomiasis Cutaneous or Wild boar visceral, serpiginous eruptions, intraocular 24 Dirofilaria immitis Occasional Wild canids (wild dog, fox, granulomas, cough, jackal, wolf), hyaena, wild chest pain felids (golden cat, Bengal tiger, clouded leopard, lion, panther), non-human primates 25 Intestinal, Wild boar abdominal, fever, myalgia, headache 26 Myiasis-causing Myiasis Depends on tissue Cervids and other herbivores & haematophagous flies or organ invaded by Gasterophilus intestinalis larvae Zebra 27 Sarcoptes scabiei Scabies Itching, dermatitis Non-human primates 28 Ticks (mainly Tick infestation Bite injuries, blood Cervids, wild canids, wild Haemaphysalis spp.) loss boar, non-human primates 29 Linguatula serrata Linguatuliasis Ocular or Sambar deer ( Cervus unicolor ) nasopharyngeal affections

monitor lizard ( Varanus bengalensis ) which was likely 7. Conclusion paratenic host, was reported from Central Kerala There are many emerging and re-emerging (Panackel et al., 2006; Parmeswaran, 2006) and the zoonotic parasites acquired from wildlife sources adult worms were detected in cardiopulmonary system which have been neglected or not been considered of of bandicoot rats ( Bandicota indica ) from agricultural major significance for human health so far. The areas of the region (Thomas et al ., 2015). Trichinoses outlook needs to change by creating public awareness (T. spiralis ) clusters from undercooked meat of wild of possible sources and the measures that can lessen the boar in Uttarakhand (Sethi et al ., 2010; Pebam et al ., risk of human infection. Persons working with wildlife 2012). Baylisascaris transfuga recorded from a should be alert to the potential of disease transmission. Himalayan black bear (Islam and Nashiruddullah, Effective campaigns for the recognition, prevention 2000) is considered a potential source of larva migrans and control can be designed and implemented (Polley, in mammals including humans (Bauer, 2013). 2005). As the various interfaces between wildlife, domestic animals and humans increase and become

Veterinary Research International | January-March, 2016 | Vol 4 | Issue 1 | Pages 01-11 © 2016 Jakraya Publications (P) Ltd 8 Chhabra and Muraleedharan…Parasitic Zoonoses and Role of Wildlife: An Overview more complex, there is obvious need for strategic of biodiversity should be adopted in line with the “one disease surveillance in wildlife. Host parasite health” philosophy. The “one health” approach also interaction in changing landscapes and ecosystems, lays emphasis that successful veterinary public health transmission pathways and risk factors require interventions are holistic and integrate current continuous updating. Alongside, the management knowledge on human medicine, veterinary medicine practices including disease prevention, for conservation and environmental sciences.

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