Serologic Evidence of Toxoplasma Gondii Infection

SEROLOGIC EVIDENCE OF TOXOPLASMA GONDII INFECTION IN WILD BIRDS AND MAMMALS FROM SOUTHEAST BRAZIL Author(s): Sérgio Netto Vitaliano , D.V.M., Ph.D., Herbert Sousa Soares , D.V.M., Hilda Fátima de Jesus Pena , D.V.M., Ph.D., Jitender Prakash Dubey , M.V.Sc., Ph.D. and Solange Maria Gennari , D.V.M., Ph.D. Source: Journal of Zoo and Wildlife Medicine, 45(1):197-199. 2014. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0179R.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0179R.1

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SEROLOGIC EVIDENCE OF TOXOPLASMA GONDII INFECTION IN WILD BIRDS AND MAMMALS FROM SOUTHEAST BRAZIL

Se´rgio Netto Vitaliano, D.V.M., Ph.D., Herbert Sousa Soares, D.V.M., Hilda Fa´tima de Jesus Pena, D.V.M., Ph.D., Jitender Prakash Dubey, M.V.Sc., Ph.D., and Solange Maria Gennari, D.V.M., Ph.D.

Abstract: In this study, serum samples of 53 wild animals from two different states from the southeast region of Brazil were analyzed for the presence of anti–Toxoplasma gondii antibodies by the modified agglutination test (MAT), with a cut-off of 1 : 5 for birds and of 1 : 25 for mammals. Out of the sampled animals, 27 were birds and 26 were mammals, and from this total, 83% (n ¼ 44) were free-living animals. Antibodies were found in 13 mammals, from which 11 were free-living animals, and in five birds, all of which were free-living. In this study, T. gondii antibodies were detected in four bird species (crested seriema, Cariama cristata; buff-necked ibis, Theristicus caudatus; picazuro pigeon, Patagioenas picazuro; and burrowing owl, Athene cunicularia) and in a giant anteater (Myrmecophaga tridactyla) for the first time. Key words: Antibodies, Brazil, modified agglutination test, Toxoplasma gondii, wild birds, wild mammals.

BRIEF COMMUNICATION some cases having no sign of clinical infection despite the seroconversion and the presence of Toxoplasma gondii is an intracellular protozoan the parasite in those animal tissues.11 Although parasite capable of infecting several species of studies indicate that wild animals are frequently warm-blooded animals, including humans. Its positive for T. gondii antibodies,1,9,12 the role of infection is widely prevalent worldwide, particu- wildlife in the epidemiology of this parasite is not larly in Brazil, where up to 90% of humans have well understood, nor is the susceptibility of been exposed to this parasite, and it is transmitted different wild species.7 by the ingestion of oocysts present in the envi- In the present article, free-living and captive ronment, by the consumption of bradyzoites wild animals from Minas Gerais and São Paulo present in tissue of infected intermediate hosts, states in the southeast region of Brazil were and by the transplacental transmission of tachy- assayed for the presence of T. gondii antibodies. zoites.4 The animals originated from 10 different muni- In animals, the interest in the evaluation of cipalities, and partners in two different public toxoplasmosis occurrence is greater in species institutions gathered the samples. In Minas Ger- that cohabitate with humans or in species that can ais state, samples were obtained from the Facul- serve as a food source as a result of the possibility dade de Medicina Veterina´ria da Universidade 10 of human infection. The pathogenicity of T. Federal de Uberlandia,ˆ and all samples originated gondii can display great variation within various from the Uberlandiaˆ municipality (1885494199 S, 3 animal species. In the most susceptible species, 4881594499 W). In São Paulo state, samples were such as Australian marsupials, New World mon- obtained from the Faculdade de Cienciasˆ Agra´- keys, and penguins, the acute disease is normally rias e Veterina´rias, Unesp Jaboticabal, and the 8 fatal, while in the most resistant species the samples originated from nine different munici- infection is normally mild and unspecific, with palities: Araraquara (2184794199 S, 4881093699 W), Barretos (2083393399 S, 488349899 W), Jaborandi From Faculdade de Medicina Veterina´ria e Zootecnia (208549099 S, 478169099 W), Jaboticabal (2181591999 S, da Universidade de Saõ Paulo, Avenida Professor Doutor 4881992199 W), Matão (2183691299 S, 4882195999 W), Orlando Marques de Paiva, 87, 05508-270, Cidade Monte Alto (2181594299 S, 4882994899 W), Ribeirão Universita´ria, Saõ Paulo/SP, Brazil (Vitaliano, Soares, Preto (2181093699 S, 4784991599 W), São Simao ˜ Pena, Gennari); Curso de Medicina Veterina´ria das (2182894199 S, 478339399 W), and Taquaritinga Faculdades Metropolitanas Unidas (UniFMU), Rua Min- (2182492399 S, 4883092099 W). In both cases, animals istro Nelson Hungria, 541, 05690-050 Real Parque/ were kept as patients in the veterinary hospital of Morumbi, Saõ Paulo/SP, Brazil (Vitaliano); and the U.S. the respective institutions, and blood was collect- Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic ed. Serum samples from 53 wild animals were Diseases Laboratory, Beltsville, Maryland 20705, USA assayed for the presence of antibodies to T. gondii (Dubey). Correspondence should be directed to Dr. by the modified agglutination test (MAT), as Gennari ([email protected]). described by Dubey and Desmonts,5 with a cutoff

197 198 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Table 1. Presence of Toxoplasma gondii antibodies (modiﬁed agglutination test [MAT] 5) in free-living wild birds from the southeast region of Brazil.

Species No. tested/No. positive Location MAT titers Cariameformes Cariama cristata (crested seriema) 1/1 Jaboticabal 100 Ciiconiformes Theristicus caudatus (buff-necked ibis) 2/2 Jaboticabal, Uberlandiaˆ 20, 160 Columbiformes Patagioenas picazuro (picazuro pigeon) 3/1 Jaboticabal 20 Falconiformes Caracara plancus (crested caracara) 2/1 Monte Alto 10 Strigiformes Athene cunicularia (burrowing Owl) 5/1 Jaboticabal 40

of 1 : 5 for birds and of 1 : 25 for mammals.9 pigeons, in burrowing owls, and in giant anteaters Association between animal species (bird or for the first time. Crested seriemas, buff-necked mammal) and presence of antibodies against T. ibis, and burrowing owls, as well as crested gondii were analyzed using a chi-square test. P- caracaras, are predators and can be infected by values of ,0.05 were considered statistically consumption of parasite-harboring prey, such as significant. small birds and rodents. On the other hand, Out of the sampled animals, 27 were birds and picazuro pigeons, which are granivorous, can be 26 were mammals, and from this total, 83% (n ¼ infected as a result of their foraging habits. These 44) were free-living animals. Antibodies were species feed from the ground, behavior that is also found in 6 of 27 (22.2%) birds, including one shared by crested seriemas and buff-necked ibis crested seriema (Cariama cristata), two buff- when foraging for insects, and, in this case, necked ibis (Theristicus caudatus), one picazuro infection may indicate soil contamination with T. pigeon (Patagioenas picazuro), one crested caraca- gondii oocysts in the environment. ra (Caracara plancus), and one burrowing owl In the case of mammals, gray brocket deer and (Athene cunicularia), all of which are free-living marsh deer are strict herbivores, and their infec- animals (Table 1). In mammals, 13 of 26 (50%) tion is probably due to environmental contami- were seropositive, including two gray brockets nation with oocysts, whereas all the other studied (Mazama gouazoubira), one marsh deer (Blastoce- species of mammals are omnivorous and can be rus dichotomus), two maned wolves (Chrysocyon infected either by environmental contamination brachyurus), one hoary fox (Pseudalopex vetulus), or by consumption of parasite-harboring prey. In one white-eared opossum (Didelphis albiventris), captive animals, the risk of infection is higher as a one capuchin monkey (Sapajus apella), two col- result of factors such as stress associated with lared anteaters (Tamandua tetradactyla), two giant anteaters (Myrmecophaga tridactyla), one six-band- captivity, the presence of synanthropic animals, ed armadillo (Euphractus sexcinctus), and one nine- and possible errors in health management, such as banded armadillo (Dasypus novemcinctus), from feeding carnivores with meat that was not previ- 1 which all were free-living animals except the ously frozen. marsh deer and the capuchin monkey (Table 2). Bird titers ranged from 10 to 160, while in The results of the present study corroborate mammals variation ranged from 25 to 800. previous studies that reported the widespread Seropositivity was significantly higher (P 0.05) presence of T. gondii in wildlife, mostly in in mammals than in birds, but this may not be captivity.1,2,9,12 However, serologic data are only a indicative of more recent infections or of greater tool with which to assess the epidemiology of the exposure because sera from avian species may not parasite. Whenever possible, it is helpful to isolate react in serologic tests for T. gondii as mammalian viable parasites from host tissues. sera,6 and for this reason, caution should be used Toxoplasma gondii antibodies were detected in when interpreting serologic data collected from crested seriemas, in buff-necked ibis, in picazuro birds. VITALIANO ET AL.—T. GONDII SEROPOSITIVITY IN WILD ANIMALS 199

Table 2. Presence of Toxoplasma gondii antibodies (modiﬁed agglutination test [MAT] 25) in captive and free- living wild mammals from the southeast region of Brazil.

Species No. tested/No. positive Location MAT titers Artiodactyla Mazama gouazoubira (gray brocket) 3/2 S. Simão, Rib. Preto 25, 100 Blastocerus dichotomus (marsh deer)a 1/1 Jaboticabal 50 Carnivora Chrysocyon brachyurus (maned wolf) 3/2 Barretos, Jaborandi 25, 400 Pseudalopex vetulus (hoary fox) 1/1 Araraquara 200 Marsupialia Didelphis albiventris (white-eared opossum) 3/1 Jaboticabal 50 Primatas Sapajus apella (capuchin monkey)a 1/1 Jaboticabal 25 Xenarthra Tamandua tetradactyla (collared anteater) 2/1 Jaboticabal 400 Myrmecophaga tridactyla (giant anteater) 2/2 Matão, Taquatiringa 100, 800 Euphractus sexcinctus (six-banded armadillo) 1/1 Uberlandiaˆ 25 Dasypus novemcinctus (nine-banded armadillo) 1/1 Ribeirão Preto 800

a Animals kept in captivity.

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