Evidence of leptospiral exposure in neotropical primatesrescued from illegal trade and a Zoo in Bahia, Brazil

Indícios de exposição a leptospiras em primatas neotropicais resgatados do comércio ilegal e de um Zoológico da Bahia

Daniela S. Almeida Andréia C. dos Santos Caroline Luane R. da Silva Arianne P. Oriá Alberto Vinicius D. Oliveira Fernanda A. Libório Daniel A. Athanazio Melissa H. Pinna About the authors

Abstract:

Few studies have compared the seroprevalence of antileptospiral agglutinins with the demonstration of urinary shedding of leptospires or evidence of active infection in the bloodstreams of non-human primates. The study population consists of 58 animals, including d 42 monkeys from the Zoological Park of Salvador (Parque Zoobotânico Getúlio Vargas), Bahia, Brazil. The study also evaluated 16 primates (Cebus sp.) rescued from illegal trade that were housed in the Wildlife Rehabilitation Center of Salvador (CETAS), Bahia, Brazil. The seroprevalence of antileptospiral antibodies was low (2%) in the animals from the Zoo. A higher rate (31%) was observed among the animals that were rescued from illegal trade in the state of Bahia. Even if all the blood and urine samples were negative for leptospiral DNA fragments, the high frequency of serological evidence of exposure suggests a potential risk of leptospirosis transmission when keeping these animals as pets.

Index Terms:
Leptospirosis; Leptospira; Primates

Resumo:

Poucos estudos compararam a soroprevalência de aglutininas antileptospira com a demonstração de excreção urinária de leptospiras ou evidência de infecção ativa em primatas não humanos. A população estudada consistiu em 58 animais, sendo 42 primatas do Parque Zoobotânico Getúlio Vargas, Bahia, Brasil. O estudo avaliou ainda 16 primatas (Cebus sp.) resgatados do tráfico ilegal e abrigados no Centro de Triagem de Animais Silvestres Chico Mendes, Salvador, Bahia, Brasil. A soroprevalência de anticorpos antileptospira foi baixa (2%) nos animais do Zoológico. Uma taxa mais elevada (31%) foi observada nos animais resgatados do tráfico ilegal. Mesmo que todas as amostras de sangue e urina tenham sido negativas para DNA de leptospiras, a alta frequência de evidência de exposição nos animais de origem selvagem indicam o risco potencial da adoção de primatas como animais de estimação.

Termos de Indexação:
Leptospirose; Leptospira; Primatas

Introduction

Leptospirosis is a widespread zoonosis caused by pathogenic leptospires. Humans acquire infection by direct exposure to contaminated urine from mammalian reservoirs or, more commonly, by exposure to contaminated soil or water. The disease occurs in different settings associated with a wide range of reservoirs, such as field mice in paddy fields, farm animals in occupational exposures, urban rodents in large urban areas with poor sanitation, and wild animals in water sports and ecotourism related exposures (Bharti et al. 2003Bharti A.R., Nally J.E., Ricaldi J.N., Matthias M.A., Diaz M.M., Lovett M.A., Levett P.N., Gilman R.H., Willig M.R., Gotuzzo E. & Vinetz J.M. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect. Dis.3:757-771.). Most human infections are asymptomatic or cause mild febrile illness that is indistinguishable from diseases caused by other infectious agents. However, 5-10% of human infections will become severe, resulting in the Weil's triad of acute renal failure, hemorrhages, and jaundice (with 5-30% fatality) or severe pulmonary hemorrhagic syndrome (SPHS, with ≥ 50% fatality) (WHO 2003WHO 2003. Human Leptospirosis: guidance for diagnosis, surveillance and control. Malta., McBride et al. 2005McBride A.J., Athanazio D.A., Reis M.G. & Ko A.I. 2005. Leptospirosis. Curr. Opin. Infect. Dis.18: 376-386., Medeiros et al. 2010Medeiros F.R., Spichler A. & Athanazio D.A. 2010. Leptospirosis-associated disturbances of blood vessels, lungs and hemostasis. Acta Trop.115:155-162.).

Non-human primates usually develop a self resolving, mild illness in naturally acquired or experimental infections ( Minette 1966Minette H.P. 1966. Leptospirosis in primates other than man. Am. J. Trop. Med. Hyg.15:190-198., Minette & Shaffer 1968Minette H.P. & Shaffer M.F. 1968. Experimental leptospirosis in monkeys. Am. J. Trop. Med. Hyg.17:202-212., Hambleton et al. 1980Hambleton P., Baskerville A., Marshall R.B., Harris-Smith P.W. & Adams G.D. 1980. Metabolic sequelae of experimental leptospirosis in grivet monkeys. Brit. J. Exp. Pathol.61:16-21., Marshall et al. 1980Marshall R.B., Baskerville A., Hambleton P. & Adams G.D. 1980. Benign leptospirosis: the pathology of experimental infection of monkeys with Leptospira interrogans serovars balcanica and tarassovi. Brit. J. Exp. Pathol.61:124-131.), but some species may develop severe disease. Experimental infection mirrored lethal human cases with pulmonary hemorrhages, liver necrosis, and tubular nephritis in marmoset monkeys (Callithrix jacchus), and an outbreak of pulmonary hemorrhage spreaded among naturally infected capuchin monkeys in a wildlife rehabilitation center in Colombia (Pereira et al. 2005Pereira M.M., Da Silva J.J., Pinto M.A., Da Silva M.F., Machado M.P., Lenzi H.L. & Marchevsky R.S. 2005. Experimental leptospirosis in marmoset monkeys (Callithrix jacchus): a new model for studies of severe pulmonary leptospirosis. Am. J. Trop. Med. Hyg.72:13-20.). There is a significant public health concern associated with illegal wildlife ownership, as wild animals are estimated to be the source of over 70% of all emerging infections (Chomel et al. 2007Chomel B.B., Belotto A. & Meslin F.X. 2007. Wildlife, exotic pets, and emerging zoonoses. Emerg. Infect. Dis.13:6-11.). Seroprevalence of antileptospiral antibodies in Neotropical primates from zoos in Latin America or from wildlife is variable, partly due to the diverse species studied and the different cutoffs employed (Table 1 and 2) (Baulu et al. 1987Baulu J., Everard C.O. & Everard J.D. 1987. Leptospires in vervet monkeys (Cercopithecus aethiops sabaeus) on Barbados. J. Wildl. Dis.23:60-66., Kessler & Everard 1988Kessler M.J. & Everard C.O.R. 1988. Leptospiral agglutinins in the Cayo Santiago macaques. Am. J. Primatol. 14:369-373., Perolat et al. 1992Perolat P., Poingt J.P., Vie J.C., Jouaneau C., Baranton G. & Gysin J. 1992. Occurrence of severe leptospirosis in a breeding colony of squirrel monkeys. Am. J. Trop. Med. Hyg.46:538-545., Luna-Alvarez et al. 1996Luna-Alvarez M.A., Moles-Cervantes L.P., Torres-Barranca J.I. & Gual-Sill F. 1996. Serological survey of leptospirosis in captive wildlife at the Chapultepec Zoo in Mexico City. Veterinaria, Mexico,27:229-234., Lilenbaum et al. 2002Lilenbaum W., Monteiro R.V., Ristow P., Fraguas S., Cardoso V.S. & Fedullo L.P. 2002. Leptospirosis antibodies in mammals from Rio de Janeiro Zoo, Brazil. Res. Vet. Sci.73:319-321., Correa et al. 2004Correa S.H.R., Vasconcellos S.A., Morais Z., Teixeira A.A., Dias R.A., Guimarães M.A.B.V., Ferreira F. & Neto J S.F. 2004. Epidemiologia da Leptospirose em animais silvestres na Fundação Parque Zoológico de São Paulo. Braz. J. Vet. Res. Anim. Sci. 41:189-193., Lilenbaum et al. 2005Lilenbaum W., Varges R., Moraes I.A., Ferreira A.M. & Pissinatti A. 2005. Leptospiral antibodies in captive lion tamarins (Leontopithecus sp) in Brazil. Vet. J.169: 462-464., Souza Júnior et al. 2006Souza Júnior M.F., Lobato Z.I.P., Lobato F.C.F., Moreira E.C., Oiveira R.R., Leite G.G., Freitas T.D. & Assis R.A. 2006. Presença de anticorpos da classe IgM de Leptospira interrogans em animais silvestres do Estado do Tocantins, 2002. Revta Soc. Bra. Med. Trop.39:292-294., Pimentel et al. 2009Pimentel J.S., Gennari S.M., Dubey J.P., Marvulo M.F.V., Vasconcellos S.A., Morais Z.M., Silva J.C.R. & Evêncio Neto J. 2009. Inquérito sorológico para toxoplasmose e leptospirose em mamíferos selvagens neotropicais do Zoológico de Aracaju, Sergipe. Pesq. Vet. Bras.29:1009-1014., Ibáñez-Contreras et al. 2010Ibáñez-Contreras A., Hernández-Godínez B., Torres- Barranca J.I. & Meléndez-Vélez P. 2010. Hallazgos de anticuerpos contra Leptospira sp., serovariedades Panama, Lai, Australis, Shermani y Patoc, en un grupo de monos rhesus (Macaca mulatta) en condiciones de cautiverio. Archivos de Medicina Veterinaria42:101-104., Ferreira et al. 2011Ferreira D.R.A., Laroque P.O., Wagner P.G.C., Higino S.S.S., Azevedo S.S., Rego E.W. & Mota R.A. 2011. Ocorrência de anticorpos e fatores de risco associados à infecção por Leptospira spp. em Cebus spp. mantidos em cativeiro no Nordeste do Brasil. Pesq. Vet. Bras.31:1019-1023., Romero et al. 2011Romero M.H., Astudillo M., Sanchez J.A., Gonzalez L.M. & Varela N. 2011. Anticuerpos contra Leptospira sp. en primates neotropicales y trabajadores de un zoológico colombiano. Revta Salud Publica13:814-823., Szonyi et al. 2011Szonyi B., Agudelo-Florez P., Ramirez M., Moreno N. & Ko A.I. 2011. An outbreak of severe leptospirosis in capuchin (Cebus) monkeys. Vet. J.188:237-239., Pinna et al. 2012Pinna M.H., Martins G., Pinheiro A.C., Almeida D.S., Oria A.P. & Lilenbaum W. 2012. Detection of anti-Leptospira antibodies in captive nonhuman primates from Salvador, Brazil. Am. J. Primatol.74:8-11., Ullmann et al. 2012Ullmann L.S., Neto R N.D., Teixeira R.H.F., Nunes A.V., Silva R.C., Pereira-Richini V.B. & Langoni H. 2012. Epidemiology of leptospirosis at Sorocaba Zoo, São Paulo state, Southeastern Brazil. Pesq. Vet. Bras.32:1174-1178.). Few studies have compared the serological evidence of leptospirosis exposure with the molecular evidence of active infection (detection of DNA fragments in blood samples) or the renal carrier state (detection of DNA in urine) in non-human primates (Ullmann et al. 2012Ullmann L.S., Neto R N.D., Teixeira R.H.F., Nunes A.V., Silva R.C., Pereira-Richini V.B. & Langoni H. 2012. Epidemiology of leptospirosis at Sorocaba Zoo, São Paulo state, Southeastern Brazil. Pesq. Vet. Bras.32:1174-1178.). The aim of this study was to investigate the serological evidence of exposure and the presence of DNA fragments of pathogenic leptospires in the blood and urine samples of Neotropical primates from two sources, a zoological park and a wild life rehabilitation center in Salvador, Bahia, Brazil.

Materials and Methods

In the present study, 58 of non-human primates were evaluated. The population included 42 monkeys from the Zoological Park of Salvador (Parque Zoobotânico Getúlio Vargas), Bahia, Brazil. These animals belonged to the following species: Cebus xanthosternos (n=23), Cebus flavius (n=11), Alouatta caraya (n=3), Aottus sp. (n=4), and Saimiri sciureus (n=1). The study also evaluated 16 primates rescued from illegal trade that were housed in the wildlife rehabilitation center of Salvador (Centro de Triagem de Animais Silvestres Chico Mendes, CETAS), Bahia, Brazil. All these animals were identified as Cebus sp., as many of them are hybrids.

Microscopic agglutination tests (MAT) were performed, according to recommended protocols (Faine et al. 1999Faine S.B., Adler B., Bolin C. & Perolat P. 1999. Leptospira and Leptospirosis. 2nd ed. MediSci, Melbourne., WHO 2003WHO 2003. Human Leptospirosis: guidance for diagnosis, surveillance and control. Malta.), and included twenty-three WHO reference strains and a local isolate (serovar Copenhageni strain L1130) (Ko et al. 1999Ko A.I., Galvao Reis M., Ribeiro Dourado C.M., Johnson Jr W.D. & Riley L.W. 1999. Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis Study Group. Lancet354:820-825., Nascimento et al. 2004Nascimento A.L., Ko A.I., Martins E.A., Monteiro-Vitorello C.B., Ho, P.L., Haake D.A., Verjovski-Almeida S., Hartskeerl R.A., Marques M.V., Oliveira M.C., Menck C.F., Leite L.C., Carrer H., Coutinho L.L., Degrave W.M., Dellagostin O.A., El-Dorry H., Ferro E.S., Ferro M.I., Furlan L.R., Gamberini M., Giglioti E.A., Goes-Neto A., Goldman G.H., Goldman M.H., Harakava R., Jeronimo S.M., Junqueira-de-Azevedo I.L., Kimura E.T., Kuramae E.E., Lemos E.G., Lemos M.V., Marino C.L., Nunes L.R., Oliveira R.C. de, Pereira G.G., Reis M.S., Schriefer A., Siqueira W.J., Sommer P., Tsai S.M., Simpson A.J., Ferro J.A., Camargo L.E., Kitajima J.P., Setubal J.C. & Van S.M.A. 2004. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J. Bacteriol.186:2164-2172.). Titers ≥1:100 were considered positive. Polymerase chain reaction for the detection of the lipL32 gene was performed as previously described (Rojas et al. 2010Rojas P., Monahan A.M., Schuller S., Miller I.S., Markey B.K. & Nally J.E. 2010. Detection and quantification of leptospires in urine of dogs: a maintenance host for the zoonotic disease leptospirosis. Eur. J. Clin. Microbiol. Infect. Dis.29:1305-1309., Chagas-Junior et al. 2012Chagas-Junior A.D., Silva C.L., Soares L.M., Santos C.S., Silva C.D., Athanazio D.A., Reis M.G., McBride F.W. & McBride A.J. 2012. Detection and quantification of Leptospira interrogans in hamster and rat kidney samples: immunofluorescent imprints versus real-time PCR. PloS one7:e32712.).

The research protocols were approved by the Research Ethics Committee of the Faculdade Franca - SP (025/2009-A). In addition, they were in accordance with guidelines System Authorization and Information on Biodiversity the Ministry of Environment of Brazil (number 20831-1)

Results and Discussion

In the present study, only one of 42 primates (2%) from the Zoological Park of Salvador had positive serum samples, according to the MAT. This animal was an adult female Alouatta caraya (black howler) that had a positive serum sample of 1:100 with mixed reactions for the Bratislava and Icterohaemorrhagiae serogroups. This animal was housed in a cage with two other adults of the same species. The positive animal and one negative black howler were born in the Zoological Park, while the other negative adult came from illegal trade (CETAS). Urine and blood samples were negative for all 42 monkeys evaluated at the Zoological Park.

Such low seroprevalence was not expected. Salvador is the third most populated city in Brazil, with an estimated 2.6 million inhabitants, and 60% of those inhabitants live in slum communities (Riley et al. 2007Riley L.W., Ko A.I., Unger A. & Reis M.G. 2007. Slum health: diseases of neglected populations. BMC Int. Health Hum. Rights7:2.). It is a large urban center with poor sanitation, and incidence of severe leptospirosis cases peak during rainy seasons and in association with floods (Ko et al. 1999Ko A.I., Galvao Reis M., Ribeiro Dourado C.M., Johnson Jr W.D. & Riley L.W. 1999. Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis Study Group. Lancet354:820-825., Costa et al. 2001Costa E., Costa Y.A., Lopes A.A., Sacramento E. & Bina J.C. 2001. Formas graves de leptospirose: aspectos clínicos, demográficos e ambientais. Revta Soc. Bras. Med. Trop.34:261-267., Riley et al. 2007Riley L.W., Ko A.I., Unger A. & Reis M.G. 2007. Slum health: diseases of neglected populations. BMC Int. Health Hum. Rights7:2.). Reports from the Zoological personnel indicated that there is a high population of rodents in the park, and rodents are frequently observed to be in contact with the animals in their cages. In some surveys from Latin American zoos, the seroprevalence of antileptospiral antigens is highly variable among different species (Table 1), and higher rates were attributed to the contact of primates with urban rodents. Additionally, there is a high prevalence of Icterohaemorrhagiae as the predicted infecting serogroup in some of these studies (as implied by MAT highest titers), and this suggests that rodents are the source of non-primate infection because these serovars are known to be selectively carried by urban rodents such as the Brown (Rattus norvegicus) and Black rats (R. rattus) (Bharti et al. 2003Bharti A.R., Nally J.E., Ricaldi J.N., Matthias M.A., Diaz M.M., Lovett M.A., Levett P.N., Gilman R.H., Willig M.R., Gotuzzo E. & Vinetz J.M. 2003. Leptospirosis: a zoonotic disease of global importance. Lancet Infect. Dis.3:757-771.). In a survey of captured rats in Salvador, 80% of a total 142 animals had positive cultures for leptospires from kidney or urine samples, and all 59 serotypes isolated by monoclonal antibodies were characterized as serovar Copenhageni (serogroup Icterohaemorrhagiae) (de Faria et al. 2008de Faria M.T., Calderwood M.S., Athanazio D.A., McBride A.J., Hartskeerl R.A., Pereira M.M., Ko A.I. & Reis M.G. 2008. Carriage of Leptospira interrogans among domestic rats from an urban setting highly endemic for leptospirosis in Brazil. Acta Tropica 108:1-5.), which is the main cause of severe leptospirosis in Salvador and in other large urban Brazilian centers (Ko et al. 1999Ko A.I., Galvao Reis M., Ribeiro Dourado C.M., Johnson Jr W.D. & Riley L.W. 1999. Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis Study Group. Lancet354:820-825., Pereira et al. 2000Pereira M.M., Matsuo M.G.S., Bauab A.R., Vasconcelos S.A., Moraes Z.M., Baranton G. & Saint G.I. 2000. A clonal subpopulation of Leptospira interrogans sensu stricto is the major cause of leptospirosis outbreaks in Brazil. J. Clin. Microbiol.38:450-452.). It is not possible to infer that the single Black Howler with a positive MAT acquired the infection from exposure to rats because it had a mixed reaction with the Bratislava serogroup, which has no known selectivity for rodents.

In summary, the results from the Zoological Park suggest that the Neotropical primates' contact with rodents was not associated with an increased seroprevalence of antileptospiral antibodies. These species may be intrinsically more resistant than others in terms of acquiring leptospiral infection, or conversely, these animals may have had previous exposure in the wild that is associated with a progressive decrease in antileptospiral antibodies during the period of captivity.

In 2009, a previous survey performed in the wildlife rehabilitation center of Salvador (CETAS) found 57% (25/44) seropositivity by MAT. In that study, marmosets were mainly affected, and positive samples were distributed as follows: Callithrix jacchus (common marmoset, 16/28: 57%), Callithrix pennicilata (Black-tufted marmoset, 4/8: 50%), and Cebus sp. (capuchin monkeys, 5/8: 63%) (Pinna et al. 2012Pinna M.H., Martins G., Pinheiro A.C., Almeida D.S., Oria A.P. & Lilenbaum W. 2012. Detection of anti-Leptospira antibodies in captive nonhuman primates from Salvador, Brazil. Am. J. Primatol.74:8-11.). In this study were found 5/16 (31%) positive serum samples by MAT from Cebus sp. Thus, the high rate of serological evidence of Leptospira exposure seems to be a consistent finding among animals from the wild that are rescued from illegal trade in the state of Bahia. It is important to note, however, that the predicted infecting serogroup inferred by MAT highest titers was Icterohaemorrhagiae in 84% of the cases in a former study. In this study, the five positive samples were distributed in the following predicted serogroups: Ballum (1:100), Semaranga (1:200), Grippotyphosa (1:100), Cynopeteri (1:100), and a mixed reaction of Tarassovi/Autumnalis (1:100). Thus, while the high frequency of Icterohaemorrhagiae indicated that monkeys could have acquired infection after they were caught in the wild, the wide range of predicted serogroups in the present study indicates that these animals may have been exposed to many potential sources of infection in the wild. In addition to conservation concerns, these data point toward the potential risk of keeping these animals as pets as it appears that they may be exposed to leptospiral infection in the wild or after entrapment.

This study also evaluated the possible association of serological evidence of exposure with active infection and renal carriage using PCR detection of leptospiral DNA in blood and urine samples, respectively. None of the evaluated samples yielded positive results. Further studies with larger sample groups of animals rescued from illegal trade are warranted to estimate the risks of infection from intimate contact with exotic animals, including Neotropical primates, when kept as pets.

Conclusions

The seroprevalence of antileptospiral antibodies was low (2%) in the Zoological Park of Salvador, Brazil, despite the high frequency of rodents in the area and the endemicity of human leptospirosis in Salvador.

A higher rate (31%) was observed among the animals rescued from illegal trade in the state of Bahia.

Serological evidence of exposure does not predict an active infection or the renal carrier state in non-human primates.

Even if all the blood and urine samples were negative for leptospiral DNA fragments, the high frequency of serological evidence of exposure suggests a potential risk of leptospirosis transmission when keeping these animals as pets.

Acknowledgements

The authors are grateful to Victor Pereira Curvelo for technical assistance on animal capture and contention during the survey performed in the Zoological Park of Salvador, Brazil.

References

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Publication Dates

  • Publication in this collection
    Sept 2016

History

  • Received
    29 Sept 2015
  • Accepted
    31 May 2016
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