, Volume 10, Issue 1, pp 48–53 | Cite as

Survey of Plasmodium spp. in Free-Ranging Neotropical Primates from the Brazilian Amazon Region impacted by Anthropogenic Actions

  • Marina G. BuenoEmail author
  • Fabio Rohe
  • Karin Kirchgatter
  • Silvia M. F. Di Santi
  • Lilian O. Guimarães
  • Carmel L. Witte
  • Maria J. Costa-Nascimento
  • Christina R. C. Toniolo
  • José Luiz Catão-Dias
Short Communication


This study investigated Plasmodium spp. infection in free-ranging neotropical primates from Brazilian Amazon regions under the impact of major anthropogenic actions. Blood samples from 19 new world primates were collected and analyzed with microscopic and molecular procedures. The prevalence of Plasmodium infection was 21.0% (4/19) and PCR positive samples were identified as P. brasilianum. Considering the social-economic changes that the Amazon is facing, the prevalence of P. brasilianum infection highlights the necessity to closely monitor the movement of both human and non-human primate populations, in order to mitigate pathogen exposure and the introduction of new agents into previously naïve areas.


Plasmodium spp. neotropical primates Amazon regions Brazil 



We would like to thank Dr. Luis Fabio Silveira (Museu de Zoologia da Universidade de São Paulo) and the WCS Brazil team for their support during sample collection. We are grateful to Marco Antonio Rego (Museu de Zoologia da Universidade de São Paulo) for creating the maps (Fig. 1). José Luiz Catão-Dias is a recipient of a scholarship by the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (301517/2006-1). The author would also like to thank FAPESP for financial support (Grants 09/51466-4; 09/53561-4).


  1. Alemayehu T, Ye-Ebiyo Y, Ghebreyesus TA, Witten KH, Bosman A, Teklehaimanot A (1998) Malaria, schistosomiasis and intestinal helminths in relation to microdams in Tigray, northern Ethiopia. Parassitologia 40:259–267PubMedGoogle Scholar
  2. Ayala FJ, Escalante AA, Rich SM (1999) Evolution of Plasmodium and the recent origin of the world populations of Plasmodium falciparum. Parassitologia, 41:55-68PubMedGoogle Scholar
  3. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25:3389–3402PubMedCrossRefGoogle Scholar
  4. Bickel SE, Catterson T, Crow M, Fisher WA, Lewandowski A, Stoughton M, Taylor II JF (2003) Environmental Guidelines for Development Activities in Latin America and the Caribbean, Prepared for USAID/LAC/RSD/E. Environmental Policy and Institutional Strengthening Indefinite Quantity Contract (EPIQ) 2003,, Accessed June 5, 2011
  5. Brasil, Ministério da Saúde, Secretaria de Vigilância em Saúde (2005a) Guia de vigilância epidemiológica/Ministério da Saúde, Secretaria de Vigilância em Saúde, Brasília: Ministério da Saúde, 816 pp., Accessed June 5, 2010
  6. Brasil, Ministério da Saúde, Secretaria de Vigilância em Saúde (2005b) Manual de Diagnóstico Laboratorial da Malária/Ministério da Saúde. Secretaria de Vigilância em Saúde, Brasília: Ministério da Saúde, 112 pp,, Accessed June 5, 2010
  7. Bruce-Chwatt LJ (1985) Essential Malariology, 2nd edition. London, William Heinemann Medical BooksGoogle Scholar
  8. Carvalho R, Bernard E, Pavan M, Cenamo M, Hoogmoed M, Waldez F, Rohe F, Mark MVD, Lira R (2009) BR-319 PROJETO DE RE-CONSTRUÇÃO: Contribuições ao processo de Licenciamento e Análise do Estudo de Impactos Ambientais, Manaus—Amazonas., Accessed April 3, 2011
  9. Coatney GR, Collins WE, Warren M, Contacos PG (1971) The Primate Malarias, Washington: Government Printing Office, 366 ppGoogle Scholar
  10. Collins, WE, Contacos, P, Guinn, EG (1990) Observations on the sporogonic cycle of Plasmodium simium da Fontseca. Journal Parasitology, 55:814-816CrossRefGoogle Scholar
  11. Cox-Singh J, Davis TME, Lee KS, Shamsul SSG, Matusop A, Atnam S, Rahman HA, Conway DJ, Singh B (2008) P. knowlesi malaria in humans is widely distributed and potentially life threatening. Clinical Infectious Diseases 46: 165-171PubMedCrossRefGoogle Scholar
  12. Cunningham AA (1996) Disease Risk of Wildlife Translocation. Conservation Biology, 10(2):349-353CrossRefGoogle Scholar
  13. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging Infectious Diseases of Wildlife - Threats to Biodiversity and Human Health. Science, 287:443PubMedCrossRefGoogle Scholar
  14. Deane LM (1992) Simian malaria in Brazil. Memória do Instituto Oswaldo Cruz. 87 (Suppl 3):1-20CrossRefGoogle Scholar
  15. Deane LM, Neto JAF (1969) Encontro do Plasmodium brasilianum em macacos do território federal do Amapá, Brasil. Revista do Instituto de Medicina Tropical de São Paulo, 11(3):199-202PubMedGoogle Scholar
  16. De Arruda M, Nardin HE, Nussenzwieg RS, Cochrane AH (1989) Sero-epidemiological studies of malaria in Indian tribes and monkeys of the Amazon Basin of Brazil. American Journal Tropical Medicine and Hygiene, 41(4):379-85Google Scholar
  17. Duarte AMRC, Malafronte RS, Cerutti C Jr, Curado I, Paiva BR, Maeda AY, Yamasaki T, Summa MEL, Neves DVDA, Oliveira SG, Gomes AC (2008) Natural Plasmodium Infections in Brazilian Wild Monkeys: are Reservoirs for Human Infections? Acta Tropica, 107(2):179-185PubMedCrossRefGoogle Scholar
  18. Escalante AA; Barrio E; Ayala FJ (1995) Evolutionary origin of human and primates malarias: evidence from the circumsporozoite protein gene. Molecular Biology and Evolution, 12(4):616-626PubMedGoogle Scholar
  19. Fandeur T, Volney B, Peneau C, De Thoisy B (2000) Monkeys of the rainforest in French Guiana are natural reservoirs for P.brasilianum/P.malariae malaria. Parasitology. 120:11-21.PubMedCrossRefGoogle Scholar
  20. Greenwood BM, Bojang K, Whitty CJ, Targett GA (2005) Malaria. Lancet 356:1487-1498CrossRefGoogle Scholar
  21. Guimarães LO, Bajay MM, Wunderlich G, Bueno MG, Röhe F, Catão-Dias JL, Neves A, Malafronte RS, Curado I, Kirchgatter K (2012) The genetic diversity of Plasmodium malariae and Plasmodium brasilianum from human, simian and mosquito hosts in Brazil. Acta Tropica, Doi:  10.1016/j.actatropica.2012.05.016 [Online June, 2012]Google Scholar
  22. Hayakawa T., Nobuko A., Toshifumi, U., Hiroshisa H., Sattabongkot J., Toyama T., Tsuboi T., Horii T., Tanabe K. (2009). Identification of Plasmodium malariae, a Human Malaria Parasite, in Imported Chimpanzees. PlosOne, 4:10PubMedCrossRefGoogle Scholar
  23. Hunter JM, Rey L, Scott D (1982) Man-made lakes and man-made diseases. Towards a policy resolution. Social Science and Medicine 16:1127–1145PubMedCrossRefGoogle Scholar
  24. Katsuragawa TH, Gil LHS, Tada MS, Da Silva LHP (2008) Endemias e epidemias na Amazônia. Malária e doenças emergentes em áreas ribeirinhas do Rio Madeira, Um caso de escolar, Estudos Avançados, 22:64Google Scholar
  25. Oliveira-Ferreira J, Lacerda MV, Brasil P, Ladislau JL, Tauil PL, Daniel-Ribeiro CT (2010) Malaria in Brazil: an overview. Malaria Journal 9:115PubMedCrossRefGoogle Scholar
  26. Paglia AP, Fonseca GBA da, Rylands AB, Herrmann G, Aguiar LMS, Chiarello AG, Leite YLR, Costa LP, Siciliano S, Kierulff MCM, Mendes SL, Tavares V da C, Mittermeier RA, Patton JL (2012) Lista Anotada dos Mamíferos do Brasil/Annoted Checklist of Brasilian Mammals, 2a edição/2nd edition, Occasional Papers in Conservation Biology, No 6, Arlington, VA: Conservation International, 76 ppGoogle Scholar
  27. Perkins SL, Schall JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88:972–978PubMedGoogle Scholar
  28. Santos LC, Curotto SMR, Moraes W, Cubas ZS, Costa-Nascimento MJ, Barros Filho IR, Biondo AW, Kirchgatter K (2009) Detection of Plasmodium sp. in capybara. Veterinary Parasitology 163:148–151PubMedCrossRefGoogle Scholar
  29. Tazi L, Ayala FJ (2011) Unresolved direction of host transfer of Plasmodium vivax v. P.simium and P. malariae v. P. brasilianum. Infection, Genetics and Evolution, 11:209-221PubMedCrossRefGoogle Scholar
  30. Thoisy B, Vogel I, Reynes JM, Pouliquen JF, Carme B, Kazanji M, Vié JC (2001) Health Evaluation of Translocated Free-Ranging Primates in French Guiana. American Journal of Primatology, 54:1–16PubMedCrossRefGoogle Scholar
  31. Woodford MH, Rossiter PB (1993) Diseases risk associated with wildlife translocation projects. Revue Scientifique et Technique de l’Office International des Epizooties 12(1):115-135Google Scholar

Copyright information

© International Association for Ecology and Health 2013

Authors and Affiliations

  • Marina G. Bueno
    • 1
    • 2
    Email author
  • Fabio Rohe
    • 3
  • Karin Kirchgatter
    • 4
  • Silvia M. F. Di Santi
    • 4
  • Lilian O. Guimarães
    • 4
  • Carmel L. Witte
    • 5
  • Maria J. Costa-Nascimento
    • 4
  • Christina R. C. Toniolo
    • 4
  • José Luiz Catão-Dias
    • 1
  1. 1.Departamento de Patologia, Faculdade de Medicina Veterinária e ZootecniaUniversidade de São PauloSão PauloBrazil
  2. 2.Tríade—Instituto Brasileiro Para Medicina da ConservaçãoPernambucoBrazil
  3. 3.Wildlife Conservation Society/WCSRio de JaneiroBrazil
  4. 4.Núcleo de Estudos em Malária, Superintendência de Controle de Endemias/Instituto de Medicina Tropical de São PauloUniversidade de São PauloSão PauloBrazil
  5. 5.Wildlife Disease LaboratoriesInstitute for Conservation Research San Diego Zoo GlobalEscondidoCA

Personalised recommendations