Serosurvey of anti- Leptospira sp. and anti- Toxoplasma gondii antibodies in capybaras and collared and white-lipped peccaries

Abstract

INTRODUCTION:

Brazilian native species are reemerging as increasingly free-ranging populations.

METHODS:

Sera from 31 capybaras (Hydrochoerus hydrochaeris) and 28 peccaries (Pecari tajacu and Tayassu pecari) were tested for anti-Leptospira and anti-Toxoplasma gondii antibodies using microscopic seroagglutination test.

RESULTS:

Nineteen percent of free-ranging and 10.0% of captive capybaras, along with 31.8% of collared peccaries, were seropositive for T. gondii. None was seropositive for Leptospira sp.

CONCLUSIONS:

The present findings indicated low risk of disease, particularly among capybaras and white-lipped peccaries; however, active surveillance programs are important for monitoring wildlife health and public health once they are in public parks around cities.

Key words:
Leptospirosis; Toxoplasmosis; Captive; Free-ranging

Wild animals play an important role in the epidemiology of zoonotic diseases such as infections of Leptospira sp. and Toxoplasma gondii^1,2. Capybaras (Hydrochoerus hydrochaeris), collared peccaries (Pecari tajacu), and white-lipped peccaries (Tayassu pecari) are very valuable, for their meat and leather, when commercially raised, in both national and international markets². Furthermore, these animals may play an important role in zoonotic pathogen cycles by serving as sentinels with active surveillance in both captive and free-ranging populations.

Leptospirosis is caused by bacteria of the genus Leptospira¹ considered the most widespread zoonotic disease worldwide³, and the unsanitary conditions maintained in urban areas using sewer rats as reservoirs⁴. Several domestic and wild animals, including the species studied here, are considered as potential reservoirs and may shed leptospires in their urine, spreading infection directly or indirectly, through urine or contaminated water, respectively¹.

Toxoplasmosis, caused by the protozoon, Toxoplasma gondii, is another important zoonotic disease. It mostly occurs through the ingestion of sporulated oocysts present in soil, food, water, or the musculature of intermediate hosts⁵. Both captive and free-ranging wild animals may be infected and act as reservoirs for spreading infection to other animals and humans. The aim of this study was to perform a serosurvey of anti-Leptospira sp. and anti-T. gondii antibodies among wild animals in different free-ranging and captive settings in southern Brazil.

Serum samples that had previously been surveyed for other pathogens were used in the present study. Sera from 31 capybaras (10 captive and 21 free-ranging) and six captive collared peccaries from the Bela Vista Sanctuary, Foz do Iguaçu and 22 captive peccaries (6 white-lipped and 16 collared peccaries) from Curitiba Zoo, Curitiba, both located in the Paraná State of Southern Brazil, were tested.

All serum samples were initially tested for anti-Leptospira sp. antibodies by the microscopic seroagglutination test (MAT), as described in a previous study⁶. All samples were tested against 28 serovars: Andamana, Australis, Autumnalis, Bataviae, Bratislava, Butembo, Canicola, Castellonis, Copenhageni, Cynopteri, Djasiman, Grippotyphosa, Hardjo (Bovis), Hardjo (Prajitno), Hebdomadis, Icterohaemorrhagiae, Javanica, Mini (Ctg), Panama, Patoc, Pomona, Pyrogenes, Sentot, Shermani, Szwajisak, Tarassovi, Whitcombi, and Wolffi. Samples were considered positive if reactions were observed at dilutions > 1:100.

Anti-T. gondii antibodies were detected using the MAT, as previously described. Samples were considered if reactions were observed at dilutions > 1:16. The 95% confidence interval and p values were calculated separately for each variable, and the results were considered significantly different when p < 0.05.

All the free-ranging and captive capybaras, as well as the collared peccaries and white-lipped peccaries, were non-reactive to anti-Leptospira antibodies. Five out of the 31 capybaras (16.1%; 95% CI: 5.4-33.7%), four out of the 21 free-ranging (19.0%; 95% CI: 5.4-41.9%) and one out of the 10 captive (10.0%; 95% CI: 0.2-44.5%), were seroreactive with T. gondii at antibody titers of 16 and 64, respectively. Although all the white-lipped peccaries were seronegative for T. gondii, seven out of the 22 collared peccaries (31.8%; 95% CI: 13.7-54.9%) were seropositive for this protozoon, with antibody titers ranging from 16 to 1,024 (Table 1).

TABLE 1
Distribution and frequency of presence of anti-Toxoplasma antibodies in free-ranging and captive capybaras from Bela Vista Sanctuary and collared peccaries and white-lipped peccaries from Curitiba Zoo, Parana State, Brazil.

Species	Population (n)	Titer	Frequency (%)
Capybara	Free-ranging (21)	0	17/21 (80.9)
		16	1/21 (4.8)
		64	3/21 (14.3)
	Captive (10)	0	9/10 (90.0)
		16	1/10 (10.0)
Collared peccary	Captive (22)	0	15/22 (68.2)
		16	1/22 (4.5)
		64	1/22 (4.5)
		256	2/22 (9.1)
		1,024	3/22 (13.7)
White-lipped peccary	Captive (6)	0	0/6 (0)

The prevalence of anti-Leptospira antibodies reported in previous studies is highly variable: from 10.4%⁷ to 25.8%² using MAT and 71.4%¹ to 100%³ using polymerase chain reaction (PCR) among free-ranging capybaras; from 9.8%⁸ to 64.6%⁴ among captive collared peccaries; and 70.4%⁹ in free-ranging white-lipped peccaries. However, in the present study, all the animals were found to be unreactive to all 28 serovars, using MAT. These unexpected findings may be attributed to low environmental contamination in both free-ranging and captive settings, since rodents have been considered the reservoirs responsible for leptospirosis transmission². Nonetheless, wild species in urban areas and in captivity should be always screened as potential reservoirs of environmental contamination, and further studies should be conducted to fully establish the role of each of these species in the disease cycle.

Toxoplasmosis has been reported in capybaras and peccaries, and wild rodents have been reported to be positive for T. gondii antigens⁹, with prevalence rates ranging from 0%² to 76.6%¹⁰ among free-ranging and captive capybaras, and from 29.1%¹¹ to 61.5%¹² among hunted or free-ranging collared peccaries. These reports differed from the results of the present study, which evaluated majority captive animals. When prevalence rates were calculated for free-ranging white-lipped peccaries using different diagnostic methods, they were found to be 60% to 100%^12,13,14. Although the indirect immunofluorescence assay (IFA) has been considered the gold-standard test for toxoplasmosis, IFA and MAT have been shown to share a correlation of more than 80%¹⁰. Furthermore, MAT is an easy-to-run, non-species specific test; in contrast, IFA has prerequisites of species-specific anti-antibodies, which may be hard to obtain and not always available for wild species.

Both leptospirosis and toxoplasmosis are water-borne diseases. Although the animals assessed in the present study were found to be negative for Leptospira sp., these wild mammals might act as environmental sentinels and/or infection disseminators, particularly for toxoplasmosis, and pose a risk of human contamination through meat consumption. In addition, vertical transmission of T. gondii through gestation and horizontal transmission through oocyst ingestion from contaminated soil, food, or water might occur among humans or animal species^4,15. More free-ranging capybaras were found to be positive for T. gondii than captive capybaras in the present study, indicating that the captive environment was more controlled, thereby impeding pathogen transmission between wild and domestic felids (definitive hosts), capybaras, and peccaries.

In summary, the results of the study indicate low risk of leptospirosis and toxoplasmosis, particularly among capybaras and white-lipped peccaries. However, active surveillance programs are important for monitoring wildlife health status and public health risks, as these species might act as sentinels.

REFERENCES

• ¹
  Marvulo MFV, Silva JCR, Ferreira PM, Morais ZM, Moreno AM, Doto DS, et al. Experimental leptospirosis in capybaras (Hydrochoerus hydrochaeris) infected with Leptospira interrogans serovar Pomona. J Zoo Wildl Med. 2009;40(4):726-30.
• ²
  Chiacchio RG, Prioste FES, Vanstreels RET, Knöbl T, Kolber M, Miyashiro SI, et al. Health evaluation and survey of zoonotic pathogens in free-ranging capybaras (Hydrochaeris hydrochaeris). J Wildl Dis. 2014;50(3):496-504.
• ³
  Jorge S, Monte LG, Coimbra MA, Albano APN, Hartwig DD, Lucas C, et al. Detection of virulence factors and molecular typing of pathogenic Leptospira from capybara (Hydrochoerus hydrochaeris). Curr Microbiol. 2012;65(4):461-4.
• ⁴
  Mendoza P, Mayor P, Gálvez HA, Céspedes MJ, Jori F. Antibodies against Leptospira spp. in Captive collared peccaries, Peru. Emerg Infect Dis. 2007;13(5):793-4.
• ⁵
  Desmonts G, Remington JS. Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. J Clin Microbiol. 1980;11(6):562-8.
• ⁶
  Milagres BS. Perfil sorológico de algumas infecções em capivara (Hydrochaeris hydrochaeris) capturada nos estados de São Paulo e Minas Gerais, Brasil. Tese de Mestrado. Viçosa: Universidade Federal de Viçosa; 2004. 77p.
• ⁷
  Mayor P, Le Pendu Y, Guimarães DA, da Silva JV, Tavares HL, Tello M, et al. A health evaluation in a colony of captive collared peccaries (Tayassu tajacu) in the eastern Amazon. Res Vet Sci. 2006;81(2):246-53.
• ⁸
  de Freitas TPT, Keuroghlian A, Eaton DP, de Freitas EB, Figueiredo A, Nakazato L, et al. Prevalence of Leptospira interrogans antibodies in free-ranging Tayassu pecari of the Southern Pantanal, Brazil, an ecosystem where wildlife and cattle interact. Trop Anim Health Prod. 2010;42(8):1695-703.
• ⁹
  Truppel JH, Reifur L, Montiani-Ferreira F, Lange RR, de Castro Vilani RG, Gennari SM, et al. Toxoplasma gondii in Capybara (Hydrochaeris hydrochaeris) antibodies and DNA detected by IFAT and PCR. Parasitol Res. 2010;107(1):141-6.
• ¹⁰
  Yai LE, Ragozo AMA, Aguiar DM, Damaceno JT, Oliveira LN, Dubey JP, et al. Isolation of Toxoplasma gondii from capybaras (Hydrochaeris hydrochaeris) from São Paulo State, Brazil. J Parasitol. 2008;94(5):1060-3.
• ¹¹
  Aston EJ, Mayor P, Bowman DD, Mohammed HO, Liotta JL, Kwok O, et al. Use of filter papers to determine seroprevalence of Toxoplasma gondii among hunted ungulates in remote Peruvian Amazon. Int J Parasitol Parasites Wildl. 2013;3(1)15-9.
• ¹²
  Carme B, Aznar C, Motard A, Demar M, de Thoisy B. Serologic Survey of Toxoplasma gondii in Noncarnivorous Free-Ranging Neotropical Mammals in French Guiana. Vector Borne Zoonotic Dis. 2002;2(1):11-7.
• ¹³
  Solorio MR, Gennari SM, Soares HS, Dubey JP, Hartley ACZ, Ferreira F. Toxoplasma gondii antibodies in wild white-lipped peccary (Tayassu pecari) from Peru. J Parasitol . 2010;96(6):1232.
• ¹⁴
  Vitaliano SN, Soares HS, Minervino AHH, Santos ALQ, Werther K, Marvulo MFV, et al. Genetic characterization of Toxoplasma gondii from Brazilian wildlife revealed abundant new genotypes. Int J Parasitol Parasites Wildl. 2014;3(3):276-83.
• ¹⁵
  Cañon-Franco WA, Yai LEO, Joppert AM, Souza CE, D'Auria SRN, Dubey JP, et al. Seroprevalence of Toxoplasma gondii antibodies in the rodent capybara (Hydrochoerus hydrochaeris) from Brazil. J Parasitol . 2003;89(4):850.

Publication Dates

• Publication in this collection
  Mar-Apr 2017

History

• Received
  04 Aug 2016
• Accepted
  20 Dec 2016