Parasitic zoonoses in India: an overview

Rev. sci. tech. Off. int. Epiz., 2010, 29 (3), 629-637

Parasitic zoonoses in India: an overviewB.B. Singh (1), R. Sharma (1), J.K. Sharma (1) & P.D. Juyal (2)*

(1) Department of Veterinary Public Health, College of Veterinary Science, Guru Angad Dev Veterinary &Animal Sciences University, Ludhiana, Punjab, India(2) Department of Veterinary Parasitology, College of Veterinary Science, Guru Angad Dev Veterinary &Animal Sciences University, Ludhiana, Punjab, India *Corresponding author: [email protected]

Submitted for publication: 27 January 2009Accepted for publication: 24 February 2010

SummaryParasitic zoonotic diseases are prevalent throughout India at varying rates. Firstreports of zoonotic parasites and new emerging diseases have been recorded inboth the human and animal populations in recent decades. The prevalence of zoonotic parasites is likely to be an underestimate, owing to the lack of propersurveillance and the shortage of information about the existence of asymptomatic animal carriers. Emergence of diseases such as humanechinococcosis/hydatidosis, neurocysticercosis, cryptosporidiosis andtoxoplasmosis in those with acquired immune deficiency syndrome, togetherwith the re-emergence of cutaneous leishmaniosis, poses a serious threat inIndia and the prevention and control of these parasitic zoonoses, and others, isa great challenge.

KeywordsEpidemiology – India – Parasitic zoonosis.

IntroductionIndia is the seventh-largest country in the world; anunimaginable disparity exists in the geography, ethnicity,religion, food and personal habits, level of education andstandards of living within the country (83). The 2001 census showed that 72.2% of the population lived invillages and over 70% of the rural population ownedlivestock. Thus, livestock plays a pivotal role in the socio-economic life of India. Parasitic zoonoses affect human andanimal health directly, and consequently affect livestockproduction. Zoonoses of parasitic origin are prevalentthroughout India at varying rates (62). Factors such aspoverty, lack of personal hygiene, defecating in openspaces, scarcity of potable water, abundance of strayanimals, high population density, and certain culinaryhabits are responsible for the rising prevalence of zoonosesin India. These factors have a direct bearing on thefrequency of parasitic infection(s), and consequently the prevalence of infection varies in different states ofIndia. Protozoa are the best-represented group of parasitesthat infect humans and other animals, of which

Cryptosporidium parvum, Toxoplasma gondii, Leishmaniaspp., Giardia duodenalis, Sarcocystis spp. and Entamoebahistolytica are the major examples. The main helminthzoonoses include echinococcosis and cysticercosis, asdiscussed later in this review. The emergence of diseasessuch as echinococcosis, cysticercosis, cryptosporidiosisand toxoplasmosis and the re-emergence of diseases suchas leishmaniosis are a serious threat and their preventionand control is difficult. This review focuses on the majorparasitic zoonotic infections that are prevalent in India.

CryptosporidiosisCryptosporidiosis has been reported worldwide.Cryptosporidium parvum (genotype 2) is widespread inhumans and other mammals. Cryptosporidium parvum is anemerging zoonotic protozoan parasite of calves, and isassociated with diarrhoea in children (47).Cryptosporidiosis in India has been reported from thenorth (90), south (43), east (16) and west (71), withprevalence values of 4.3%, 13.0%, 5.5% and 5.6%,

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among those with no such history (n = 68) (8). A higherprevalence of T. gondii infection has been recorded in women belonging to low socio-economic groups. It hasalso been observed that the seroprevalence of T. gondii inhumans in India is low, compared with that in Westerncountries (24). This may be due to a preference for petdogs rather than cats and a large vegetarian population.The overall prevalence measured using the indirecthaemagglutination antibody test (titre 1:64 or more) variedbetween 2.2% and 4.8% in buffaloes, cats, cattle, dogs andhorses (as well as mules and donkeys). Higherseroprevalence was observed in pigs (14.0%), sheep(7.9%), goats (8.8%) and camels (7.5%) (cited in 22). Theprevalence of T. gondii in cats (2.5%) is low whencompared with that in Western countries (cited in 22).Overall, the seroprevalence of 8% in sheep and goats in India is also low compared with that in other countries(23, 25). The prevalence of T. gondii antibodies in sera fromnaturally infected pigs varies from around 14% to 31% indifferent parts of India (24).

Higher titres and seropositivity were observed frequentlyin older ewes and does (10). A prevalence of approximately10% has been reported in pigeons. A study was conductedto isolate and genotype T. gondii from free-range chickens(Gallus domesticus) in villages in the Maharashtra and TamilNadu states of central and south India, respectively (87).Genotyping using the SAG 2 locus identified isolates oftypes II and III. Antibodies to T. gondii, as assayed with themodified agglutination test (≥1:5), were found in 133 chickens (17.9%).

LeishmaniosisLeishmaniosis is a complex group of syndromes which areendemic throughout the world and affect 88 countries (50).

Cutaneous leishmaniosis

Cutaneous leishmaniosis (CL), caused by Leishmaniatropica, was confined to hot dry north-western regions of India and it is endemic in the western Thar deserts ofRajasthan (50), with reports of sporadic cases from Punjab,Delhi, Haryana and Gujarat (41, 75). There are reports ofnew foci of infection in various parts of India (7, 77); forexample, CL was not reported from Kerala State before1988, but many cases have been recorded since then (7, 40). This is of considerable public health interest inview of a newly recognised reservoir area of CL in southIndia. Further investigations are required to identifypotential vectors and the reservoir host. Both dogs androdents serve as the zoonotic reservoir for CL in the Thardesert (1). In Bikaner, in dogs, a major reservoir, incidencerates of 6.8% and 6.12% were recorded during 1985 (53)and 1999 (11), respectively.

respectively. The rate of Cryptosporidium infection has beenfound to be significantly higher in urban slum areas (49)and in patients with diarrhoea (15, 48). Cryptosporidiumparvum has been reported to be the most common parasiteobserved in individuals positive for humanimmunodeficiency virus (HIV) (46). Cryptosporidiumoocysts have also been detected in drinking water supplies(3). The infection in bovids has been found to be moreprevalent (35.4%) in the northern parts of the countrythan in the eastern or southern parts (64). A recent two-year study in Kolkatta that tested 470 bovine faecalsamples per year reported the prevalence to be 17.46% inthe first year and 18.04% in the second (68). The sheddingand intensity of shedding have been found to besignificantly higher in calves with diarrhoea (82).Genotype surveys are required to determine whethercalves or other bovids serve as a major reservoir forC. parvum infection in humans.

ToxoplasmosisToxoplasma gondii is an intestinal coccidium of felids, withan unusually wide range of intermediate hosts that includesheep, goats, pigs, and humans. Central nervous systemtoxoplasmosis in individuals with acquired immunedeficiency syndrome (AIDS) is an emerging disease inIndia (44). In the first national serological survey ofT. gondii in India (21), a total of 23,094 serum sampleswere tested for antibodies to the parasite.Immunoglobulins (Ig) IgG and IgM were detected with theuse of a solid-phase immune capture enzyme-linkedimmunosorbent assay; IgG and IgM antibodies were foundin 24.3% and 2% of the samples, respectively. The lowestseroprevalence values were obtained in the northern partsof India, with the highest in the south. The data probablyreflect the effect of significantly drier conditions in thenorth and, therefore, reduced survivability of T. gondiioocysts. Other workers have also reported theseropositivity to one or both classes of antibodies to varyfrom 17.2% to 22.6% (31, 51). Toxoplasma encephalitis(TE) is the most frequent cause of focal nervous systemdisorder complicating AIDS. There have been variousreports of TE from India (9).

The prevalence of toxoplasmosis in India shows a widevariation, and one study has reported a figure as high as77% in women of reproductive age (85). This might be dueto the fact that the study was conducted in patientsclinically suspected to have toxoplasmosis. There are veryfew reports of the prevalence of this parasitic infectionamong pregnant women from north-east India; however,one report showed that the seroprevalence of T. gondiiinfection among pregnant women in the area, measuredusing enzyme immunoassay kits, was 44.6% in womenwith a history of pregnancy loss (n = 112) and 36.8%

Taeniosis and cysticercosisThe prevalence of taeniosis in humans varies from 0.75%to 1.0% in certain communities, particularly in rural areas,where there is more contact with the pig population (83).In India, neurocysticercosis is an important emergingdisease of the central nervous system, second totuberculosis. Neurocysticercosis is also emerging as one ofthe principal causes of epilepsy (83). The occurrence ofCysticercus cellulosae in the muscles of pigs is very wellestablished in different parts of India, with an overallprevalence ranging from 3% to 26% (13, 18, 65, 66, 72,76, 92). In India, little information on Taenia saginata isavailable due to a ban on the slaughter of cows and the factthat beef is not consumed on religious grounds.

Echinococcosis/hydatidosisEchinococcosis or hydatidosis is an infection caused by alarval stage (the metacestode) of Echinococcus species. It can range in severity in humans from asymptomaticinfection to serious disease, and can even be fatal in somecases. Human echinococcosis caused by Echinococcusgranulosus continues to be a significant public healthproblem. In several regions of India, there are alarmingindications of increasing human health risks associatedwith echinococcosis (93). Increasing trends in theseroprevalence of human hydatidosis have been observedin north India (38) and there are numerous reports andsurveys that reveal the occurrence of human hydatidosis inmost states (12, 36, 38, 39, 57, 91). The conditions in thecountry are ideal for the establishment and transmission ofhydatidosis in both livestock and humans. Cultural,educational, socio-economic, agricultural andenvironmental factors contribute to the transmission of thedisease. The presence of stray dogs and fallen carcassesplays an important role in the transmission of the diseasein the country. Echinococcus granulosus has a widegeographical distribution in livestock (32, 93), and it isprevalent throughout the country. The overall prevalenceof E. granulosus cysts in southern India was 7.0%(106/1,519), 7.1% (31/439), 9.4% (46/489) and 11.5%(10/87) in sheep, cattle, buffalo and pigs, respectively (29).Another study carried out from 1995 to 1997 inPuducherry showed higher infection rates: 37.8% in 325 sheep and 47.6% in 680 goats (17). In Uttar Pradesh,the prevalence of E. granulosus was found to be 2.9%(9/312), 1.4% (39/2,710) and 0.9% (27/2,980) in sheep,goats and pigs, respectively (19).

TrichinellosisAlthough infection with Trichinella spp. is globallydistributed, it has been documented only rarely in India.

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Human trichinellosis has been recorded only once, in 1996(2). A few case reports have been documented fromBombay and Kolkatta, in cats and in domestic pigs in 1967and 1968 (63, 73). In Maharashtra, out of 500 samplesfrom adult pigs, larvae of T. spiralis were detected in threecases (52). Epidemiological studies are required urgently,because the infection is likely to be under-diagnosed, andit is necessary to explore the existence of the parasiteamong wildlife reservoirs.

Larva migransMore than 200 million people are affected by hookwormsin India. Cases of cutaneous larva migrans (37, 42, 55) andvisceral larva migrans (30, 84) have been reportedthroughout the country. Seventy-two percent of dogs werefound to harbour Ancylostoma caninum, 60% A. braziliense,and 37% harboured mixed infections with bothhookworms (89). However, no A. ceylanicum was detectedin the dog population associated with a tea-growingcommunity that was endemic for the parasite in north-eastIndia (89).

Amoebiasis and giardiasisHuman infection with Entamoeba histolytica has beenreported in India. Study of the epidemiology of amoebiasisshows that many animals are potential reservoirs ofinfection (61). The parasite has been detected throughidentification of cysts and trophozoites (45), and through seroprevalence studies (79). Epidemiologicalstudies have revealed the presence of Giardia intestinalisamong children (5, 35) and HIV-seropositive individuals(46). Phylogenetic and epidemiological analyses (89)provided substantiating evidence to support the zoonotictransmission of canine Giardia in a parasite-endemic tea-growing community in north-eastern India.

SarcocystosisCases of human sarcocystosis have been reported fromLucknow. A preliminary survey of children belonging tofamilies who slaughter domestic pigs without any meatinspection (6) revealed that Sarcocystis suihominis wasprevalent in the selected population. The prevalence ofS. hominis was 6.9% (58) and 3.79% (81) in cattle in UttarPradesh and Punjab, respectively. The prevalence ofS. suihominis was 49.5% (86), 56.66% (20) and 53.62%(4), in pigs from three different parts of the country. Theprevalence of S. suihominis is much higher than that ofS. hominis owing to the non-consumption of beef in Indiadue to religious beliefs.

Other parasitic zoonosesMany other zoonotic parasites have been reported (Table I)from different parts of the country.

echinococcosis/hydatidosis, neurocysticercosis, crypto-sporidiosis, and toxoplasmosis in AIDS pose a great threatin India and the prevention and control of these parasiticzoonoses will be challenging. The use of molecularepidemiological investigations and spatial analytical tools

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Table IZoonotic parasites recorded in IndiaIn addition to the major parasites discussed elsewhere in this article other parasites have been reported in India, examples of which are providedhere

Disease Parasite Species States involved References

Angiostrongylosis Angiostrongylus cantonensis Humans Maharashtra 59Diphyllobothriosis Diphyllobothrium latum Humans Puducherry, Tamil Nadu 56, 78Dipylidiasis Dipylidium caninum Humans via pet cats Delhi 26Dirofilariosis Dirofilaria repens, Humans Kerala, Southern India 14, 54, 69, 74

Dirofilaria tenuis Dracunculosis Dracunculus medinensis Humans Andhra Pradesh, Gujarat, 88

Madhya Pradesh, Maharashtra, Rajasthan, Karnataka

Echinostomiasis Echinostoma ilocanum Humans Delhi, West Bengal 28Fasciolopsiosis Fasciolopsis buski Pigs Assam 88Gastrodiscoidiosis Gastrodiscoides hominis Pigs Madhya Pradesh 80Gnathostomosis Gnathostoma spinigerum Humans Tamil Nadu 67

Tigers Bengal 70Cats MadrasDogs Assam, KeralaPigs Meghalaya

Human intestinal capillariasis Capillaria spp. Humans Tamil Nadu 34Malaria, zoonosis Plasmodium spp. Humans Greater Nicobars, Andaman 33of simian origin & Nicobar islandsParagonimiosis Paragonimus westermani Humans Madras, West Bengal, Assam, Manipur 60Schistosomiosis Schistosoma haematobium Humans Maharashtra 27

ConclusionsClimatic change associated with global warming, increasedvector populations, world tourism, the demand forlivestock food products, changing socio-economicconditions, poverty, the lack of safe drinking water, thelarge number of stray animals, certain cooking practices,defecating outdoors, poor personal hygiene, and the highpopulation density are responsible for the rising prevalenceof parasitic zoonoses in India. In this changing scenario,food safety is of the utmost importance. Leishmaniosis,

can improve our understanding of the current status ofparasitic zoonoses in India. Health education, vectorcontrol, control of animal movements, controlled slaughter,higher socio-economic development and improved riskassessments can help to control parasitic zoonoses in thecountry. There is a need for better coordination of medicalveterinary sciences and improvement of collaborativeapproaches to formulate appropriate control strategies in India.


Tour d’horizon des zoonoses parasitaires en Inde

B.B. Singh, R. Sharma, J.K. Sharma & P.D. Juyal

RésuméLes maladies zoonotiques d’origine parasitaire sont présentes dans toutes lesrégions de l’Inde avec des taux de prévalence variables. Les premiers rapportssignalant la présence de parasites zoonotiques et de nouvelles maladiesémergentes affectant les populations animales et humaines ont commencé àêtre publiés il y a quelques décennies. La prévalence des parasites zoonotiquesest probablement sous-estimée, en raison de l’inadéquation de la surveillanceexercée et du manque d’informations sur les animaux porteursasymptomatiques. L’émergence de maladies humaines telles que l’hydatidose, laneurocysticercose, la cryptosporidiose et la toxoplasmose chez les personnesatteintes du syndrome d’immunodéficience acquise, ainsi que la réémergencede la leishmaniose cutanée représentent une grave menace sanitaire et un défipour la prévention et le contrôle des zoonoses parasitaires en Inde.

Mots-clésÉpidémiologie – Inde – Zoonose parasitaire.

Repaso de las zoonosis parasitarias en la India

B.B. Singh, R. Sharma, J.K. Sharma & P.D. Juyal

ResumenEn la India, la prevalencia de las enfermedades zoonóticas parasitarias varíasegún las regiones. En los últimos decenios han comenzado a aparecer informesque describen parásitos zoonóticos y nuevas enfermedades emergentes enpoblaciones tanto humanas como animales. Es probable además que la prevalencia de parásitos zoonóticos esté subestimada debido a la falta devigilancia adecuada y a la escasez de información sobre portadores animalesasintomáticos. La aparición de dolencias como la hidatidosis, la neurocisticercosis, la criptosporidiosis o la toxoplasmosis en personasafectadas por el síndrome de inmunodeficiencia adquirida, junto con lareaparición de la leishmaniasis cutánea, hace pesar graves amenazas y planteaun gran problema para la prevención y el control de las zoonosis parasitarias enla India.

Palabras claveEpidemiología – India – Zoonosis parasitarias.

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Parasitic zoonoses in India: an overview

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