Acessibilidade / Reportar erro

Toxoplasmosis in emperor tamarin (Saguinus imperator): case report

Toxoplasmose em sagüi-de-bigode (Saguinus imperator): relato de caso

Abstracts

A case of toxoplasmosis in an adult male emperor tamarin (Saguinus imperator) is reported. The primate was found dead and no clinical sign was noticed before death. Pathological findings included moderate to severe interstitial pneumonia, multifocal necrotizing hepatitis and multifocal to coalescing necrotizing lymphadenitis. Immunohistochemistry assays (strepto-avidin-biotin-peroxidase) performed on paraffin embedded tissues (lung, lymph nodes, liver, spleen, heart, intestine and adipose tissue) were strongly positive for Toxoplasma gondii.

Toxoplasma gondii; Primates; Saguinus imperator; Immunohistochemistry


É relatado um caso de toxoplasmose ocorrido em sagüi-de-bigode (Saguinus imperator). O animal foi encontrado morto sem que tenham sido observados sinais clínicos. Achados de necropsia e histopatológicos incluíram pneumonia intersticial moderada, hepatite necrótica multifocal e linfadenite necrosante multifocal a coalescente. A técnica imunoistoquímica (strepto-avidina-biotina peroxidase) realizada em pulmão, fígado, linfonodos, baço, coração, intestino e tecido adiposo foi fortemente positiva para Toxoplasma gondii.

Toxoplasma gondii; Primates; Saguinus imperator; Imunoistoquímica


SHORT COMMUNICATION/NOTA PRÉVIA

Toxoplasmosis in emperor tamarin (Saguinus imperator): case report

Toxoplasmose em sagüi-de-bigode (Saguinus imperator): relato de caso

Sabrina EPIPHANIO1 1 Departamento de Patologia da Faculdade de Medicina Veterinária e Zootecnia da USP – SP 2 Fundação Parque Zoológico de São Paulo ; José Luiz CATÃO-DIAS1 1 Departamento de Patologia da Faculdade de Medicina Veterinária e Zootecnia da USP – SP 2 Fundação Parque Zoológico de São Paulo ; Marcelo Alcindo de Barros Vaz GUIMARÃES2 1 Departamento de Patologia da Faculdade de Medicina Veterinária e Zootecnia da USP – SP 2 Fundação Parque Zoológico de São Paulo

CORRESPONDENCE TO:

José Luiz Catão Dias

Departamento de Patologia

Faculdade de Medicina Veterinária e Zootecnia da USP

Cidade Universitária Armando de Salles Oliveira

Av. Orlando Marques de Paiva, 87

05508-000 – São Paulo – SP

e-mail: zecatao@usp.br

SUMMARY

A case of toxoplasmosis in an adult male emperor tamarin (Saguinus imperator) is reported. The primate was found dead and no clinical sign was noticed before death. Pathological findings included moderate to severe interstitial pneumonia, multifocal necrotizing hepatitis and multifocal to coalescing necrotizing lymphadenitis. Immunohistochemistry assays (strepto-avidin-biotin-peroxidase) performed on paraffin embedded tissues (lung, lymph nodes, liver, spleen, heart, intestine and adipose tissue) were strongly positive for Toxoplasma gondii.

UNITERMS: Toxoplasma gondii; Primates; Saguinus imperator; Immunohistochemistry.

Toxoplasmosis is an acute and frequently fatal zoonotic disease caused by Toxoplasma gondii, an obligatory intracellular parasite. It can be transmitted congenitally or by ingestion of contaminated foodstuff8.

Toxoplasmosis has already been described in New World non-human primates1,3,6,7,13. Due to factors not yet completely understood, neotropical primates seem to be much more susceptible to the disease than Old World non-human primates2,6,9,10.

This report describes a case of toxoplasmosis in an adult male Saguinus imperator, the emperor tamarin, belonging to the Fundação Parque Zoológico de São Paulo (FPZSP) primate collection. To our knowledge, this disease has never been reported in this South American primate species.

The monkey was fed twice daily with fruits, vegetables, boiled eggs and cooked meat (frozen beef). Crickets (Grillus sp.) and Tenebrio sp. larvae were offered weekly. Water was offered ad libitum. The animal was kept along with another tamarin of the same species in a metal cage, daily cleaned and exposed to sunlight on a regular basis. No clinical signs were noticed previous to death. Postmortem examination revealed regular body condition, mild hidrotorax, enlargement of the liver and mesenteric lymph nodes, pulmonary and splenic congestion. Other organs, including cerebrum, cerebellum, heart, intestines and kidneys were grossly unremarkable. Fragments from multiple organs were fixed in 10% buffered formalin, embedded in paraffin, sectioned at 4-6 m m, and stained with hematoxylin-eosin (HE).

Microscopically there were multiple lesions, including subacute, diffuse, moderate to severe interstitial pneumonia with desquamation of pneumocytes and exudation of alveolar macrophages into the alveolar lumen. Pneumocyte type II proliferation was seen, along with edema and congestion (Fig. 1). The liver had multifocal, randomly distributed, acute, moderate to severe necrotizing hepatitis (Figs. 2 and 3). Other alterations included coalescing necrotizing lymphadenitis; necrotizing follicular splenitis with lymphoid depletion; subacute, diffuse enteritis. No histopathologic lesions were observed in the brain, cerebellum, adrenals, urinary bladder, tongue and salivary glands.

Figure 1



Microscopically associated with the lesions observed in the lungs, liver, mesenteric lymph nodes and spleen there were oval-shaped to piriform structures, with a central endossome, morphologically compatible with T. gondii organisms11. These zoites were seen individually or forming small groups.

Immunohistochemistry assay for T. gondii was performed on available paraffin-embedded fragments of lung, lymph nodes, liver, spleen, heart, intestine and adipose tissue, using a previously described method14 and modified by Bourne4 and Gimeno12. The polyclonal antibody to T. gondii was acquired from Dako (Carpinteria, CA). The results were strongly positive for T. gondii (Fig. 4).

Figure 4

Toxoplasmosis can affect all homoeothermic animals. Domestic and wild felids are the definitive hosts; cats and other mammals can act as intermediate hosts11. Usually it is a severe and generalized infection in New World primates, being frequently fatal. T. gondii can be transmitted to intermediate hosts both horizontally, by ingestion of contaminated foodstuff or transplacentally.

In the present case, it is not clear how the tamarin was infected. Due to its age, the possibility of transplacental infection was ruled out. A common described source of horizontal infection is uncooked meat8. However, all beef offered to the primates at FPZSP was cooked before frozen. These combined procedures are usually efficient in preventing contamination through ingestion of oocysts and/or cysts9.

The gross and microscopic lesions observed in the present case are similar to the ones previously described in New World primates, including acute and severe pneumonia, associated with edema and congestion; mesenteric necrotizing-hemorrhagic lymphadenitis, splenitis and acute hepatitis. The characteristic microscopic lesion observed in toxoplasmosis is multifocal necrosis induced by tissue multiplication of tachyzoites, associated or not with inflammation and involving multiple organs5,7,11.

The differential diagnosis includes several protozoal and fungal organisms. T. gondii tachyzoites can resemble Histoplasma sp. and Leishmania sp. in macrophages and Trypanosoma sp. in muscular tissue2. T. gondii bradyzoites in tissue cysts must be differentiate from pseudocysts of Encephalitozoon cuniculi in different organs and from Sarcocysts sp. in muscles.

Immunohistochemistry clearly demonstrated the nature of the agent. The results obtained were strongly positive for T. gondii.

Due to the severity and high mortality observed in toxoplasmosis outbreaks in New World primates5,6,7, rigorous control procedures are strongly recommended to prevent the occurrence of this important disease among neotropical primates collections.

ACKNOWLEDGMENTS

The authors would like to thank the Fundação Parque Zoológico de São Paulo and Dr. Maria L. Zaidan Dagli and Silvia Catarina Salgado Oloris, from the Department of Pathology, School of Veterinary Medicine, University of São Paulo, for their assistance with the immunohistochemistry study.

This report is part of the Master dissertation presented by Sabrina Epiphanio to the Department of Pathology, School of Veterinary Medicine, University of São Paulo, Brazil. This project was supported by CNPq and FAPESP.

RESUMO

É relatado um caso de toxoplasmose ocorrido em sagüi-de-bigode (Saguinus imperator). O animal foi encontrado morto sem que tenham sido observados sinais clínicos. Achados de necropsia e histopatológicos incluíram pneumonia intersticial moderada, hepatite necrótica multifocal e linfadenite necrosante multifocal a coalescente. A técnica imunoistoquímica (strepto-avidina-biotina peroxidase) realizada em pulmão, fígado, linfonodos, baço, coração, intestino e tecido adiposo foi fortemente positiva para Toxoplasma gondii.

UNITERMOS: Toxoplasma gondii; Primates; Saguinus imperator; Imunoistoquímica.

Received: 06/11/1997

Accepted: 05/08/1998

  • 1
    - ANDERSON, D.C.; McCLURE, H.M. Acute disseminated fatal toxoplasmosis in a squirrel monkey. Journal of American Veterinary Medical Association, v.181, n.11, p.1363-6, 1982.
  • 2
    - ANDERSON, D.C.; McCLURE, H.M. Toxoplasmosis. In: JONES, T.C.; MOHR, U.; HUNT, R.D. Monographs on pathology of laboratory animals: nonhuman primates I New York : Springer-Verlag, 1993. p.63-9.
  • 3
    - BORST, G.H.A.; VAN KNAPEN, F. Acute acquired toxoplasmosis in primates in a zoo. Journal of Zoologycal Animal and Medicine, v.15, n.2, p.60-2, 1984.
  • 4
    - BOURNE, J.A. Handbook of immunoperoxidase staing methods Santa Barbara : Immunochemistry Laboratory, Dako Corporation, 1983. 37p.
  • 5
    - CUNNINGHAM, A.A.; BUXTON, D.; THOMSON, K.M. An epidemic of toxoplasmosis in a captive colony of squirrel monkeys (Saimiri sciureus). Journal of Comparative Pathology, v.107, p.207-19, 1992.
  • 6
    - DICKSON, J.; FRY, J.; FAIRFAX, R.; SPENCE, T. Epidemic toxoplasmosis in captive squirrel monkeys (Saimiri sciureus). Veterinary Record, v.112, n.13, p.302, 1983.
  • 7
    - DIETZ, H.H.; HENRIKSEN, P.; BILLE-HANSEN, V.; HENRIKSEN, S.A. Toxoplasmosis in a colony of New World monkeys. Veterinary Parasitology, v.68, n.4, p.299-304, 1997.
  • 8
    - DUBEY, J.P. Toxoplasmosis. Journal of American Veterinary Medical Association, v.189, n.2, p.166-70, 1986.
  • 9
    - DUBEY, J.P.; BEATTIE, C.P. Toxoplasmosis of animals and man Boca Raton : CRC Press, 1988. p.155-8: Toxoplasmosis in nonhuman primates.
  • 10
    - ESCAJADILLO, A.; FRENKEL, J.K. Experimental toxoplasmosis and vaccine testes in Aotus monkeys. American Journal of Tropical Medicine and Hygiene, v.44, n.4, p.382-9, 1991.
  • 11
    - GARDINER, C.H.; FAYER, R.; DUBEY, J.P. An atlas of protozoan parasites in animals tissues. U.S. Department of Agriculture, 1988. 83p. (Agriculture Handbook, 651).
  • 12
    - GIMENO, J.E. Fundamentos de imunoistoquímica aplicada a patologia veterinária ENCONTRO NACIONAL DE PATOLOGIA VETERINÁRIA, 7. Belo Horizonte, 1995. 35p./Apostila/
  • 13
    - HESSLER, J.R.; WOODARD, J.C.; TUCEK, P.C. Lethal toxoplasmosis in a Wooly monkey. Journal of American Veterinary Medical Association, v.159, n.11, p.1588-94, 1971.
  • 14
    - HSU, S.M.; RAINE, L.; FANGER, H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. Journal Histochemistry and Citochemistry, v.29, p.577-80, 1981.
  • 1
    Departamento de Patologia da Faculdade de Medicina Veterinária e Zootecnia da USP – SP
    2 Fundação Parque Zoológico de São Paulo
  • Publication Dates

    • Publication in this collection
      21 Sept 2000
    • Date of issue
      1999

    History

    • Accepted
      05 Aug 1998
    • Received
      06 Nov 1997
    Faculdade de Medicina Veterinária e Zootecnia / Universidade de São Paulo Av. Prof. Dr. Orlando Marques de Paiva, 87, Cidade Universitária Armando de Salles Oliveira, 05508-270 São Paulo SP Brazil, Tel.: +55 11 3091-7636, Fax: +55 11 3031-3074 / 3091-7672 / 3091-7678 - São Paulo - SP - Brazil
    E-mail: brazvet@edu.usp.br