Skip to main content
Log in

No Evidence of Rabies Exposure in Wild Marmosets (Callithrix jacchus) of Northeast Brazil

  • Short Communication
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Rabies transmitted by wildlife is the main source of human rabies mortality in Latin America and considered an emerging disease. The common marmoset Callithrix jacchus of Brazil is the only known primate reservoir of rabies worldwide. We tested whether alive free-ranging C. jacchus were exposed to rabies in four northeast states that have previously reported rabies-positive dead C. jacchus (Pernambuco and Bahia) or not (Paraíba and Rio Grande do Norte). Our results show no evidence of rabies antibodies or infection in the sampled C. jacchus, suggesting that apparently healthy marmosets are not widely exposed to rabies over their natural range.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aguiar TD, Costa EC, Rolim BN, Romijn PC, Morais NB, Teixeira MF (2011) Risks of transmitting rabies virus from captive domiciliary common marmoset (Callithrix jacchus) to human beings, in the metropolitan region of Fortaleza, state of Ceará, Brazil. Rev Soc Bras Med Trop. https://doi.org/10.1590/S0037-86822011005000031.

    Article  PubMed  Google Scholar 

  • Almeida MF, Massad E, Aguiar EAC, Martorelli LFA, Joppert AMS (2001) Neutralizing antirabies antibodies in urban terrestrial wildlife in Brazil. Journal of Wildlife Diseases 37:394–398. https://doi.org/10.7589/0090-3558-37.2.394

    Article  PubMed  CAS  Google Scholar 

  • Andrade MCR, de Oliveira AN, Romijn PC, Kimura LMS (1999) Immune response produced by rabies vaccines in marmosets (Callithrix sp). Rev Soc Bras Med Trop. https://doi.org/10.1590/S0037-86821999000500011

    Article  PubMed  Google Scholar 

  • Antunes JMAP, Demoner LC, Cruvinel TMA, Kataoka AP, Martorelli LFA, Machado GP, Megid J (2017) Rabies virus exposure of brazilian free-ranging wildlife from municipalities without clinical cases in humans or in terrestrial wildlife. Journal of Wildlife Diseases 53, 662–666, DOI: https://doi.org/10.7589/2016-09-204

    Article  Google Scholar 

  • Araujo DB, Martorelli LA, Kataoka APGA, Campos ACA, Rodrigues CS, Sanfilippo LF, Cunha ES, Durigon EL, Favoretto SR (2014) Antibodies to rabies virus in terrestrial wild mammals in native rainforest on the north coast of São Paulo state, Brazil. Journal of Wildlife Diseases 50:469–477. https://doi.org/10.7589/2013-04-099

    Article  PubMed  Google Scholar 

  • Benavides JA, Valderrama W, Streicker DG (2016) Spatial expansions and travelling waves of rabies in vampire bats. Proceedings of the Royal Society b: Biological Sciences 283:20160328. https://doi.org/10.1098/rspb.2016.0328

    Article  PubMed Central  Google Scholar 

  • Benavides JA, Megid J, Campos A, Hampson K (2020a) Using surveillance of animal bite patients to decipher potential risks of rabies exposure from domestic animals and wildlife in Brazil. Frontiers in Public Health 8:318

    Article  PubMed  PubMed Central  Google Scholar 

  • Benavides JA, Valderrama W, Recuenco S, Uieda W, Suzán G, Avila-Flores R, Velasco-Villa A, Almeida M, de Andrade FAG, Molina-Flores B, Vigilato MAN, Pompei JCA, Tizzani P, Carrera JE, Ibanez D, Streicker DG (2020b) Defining new pathways to manage the ongoing emergence of bat rabies in Latin America. Viruses 12:1002. https://doi.org/10.3390/v12091002

    Article  PubMed  PubMed Central  Google Scholar 

  • Benavides JA, Raghavan RK, Boere V, Rocha SM, Wada MY, Vargas A, Voietta F, e Silva IO, Leal S, de Castro A, Arruda MF, Towsend Peterson A, Megid J, Carrieri ML, Kotait I (2022) Spatio-temporal dynamics of rabies and habitat suitability of the common marmoset Callithrix jacchus in Brazil. PLOS Neglected Tropical Diseases 16, e0010254, DOI: https://doi.org/10.1371/journal.pntd.0010254.

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackwood JC, Streicker DG, Altizer S, Rohani P (2013) Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proceedings of the National Academy of Sciences 110:20837–20842. https://doi.org/10.1073/pnas.1308817110

    Article  ADS  CAS  Google Scholar 

  • Campos AA, Dos Santos RN, Benavides JA, de Carvalho Ruthner Batista HB, Finoketti F, Wagner PG, Zafalon-Silva B, Alievi M, da Silva FB, Witt A, Tartaroritti A, Rodrigues da Silva AdeC, Sheffer Pereira KC, Frazzon APG, Roehe PM, Franco AC (2020) Rabies surveillance in wild mammals in South of Brazil. Transboundary and Emerging Diseases 67:906–913. https://doi.org/10.1111/tbed.13415

    Article  PubMed  CAS  Google Scholar 

  • Campos ACA, Melo FL, Romano CM, Araujo DB, Cunha EM, Sacramento DR, de Andrade Zanotto PM, Durigon EL, Favoretto SR (2011) One-step protocol for amplification of near full-length cDNA of the rabies virus genome. J Virol Methods 174, 1–6, https://doi.org/10.1016/j.jviromet.2011.03.030

    Article  CAS  Google Scholar 

  • Castilho JG Jr, Carnieli P, Durymanova EA, de Oliveira Fahl W, de Novaes Oliveira R, Macedo CI, da Rosa ES, Mantilla A, Carrieri ML, Kotait I (2010) Human rabies transmitted by vampire bats: antigenic and genetic characterization of rabies virus isolates from the Amazon region (Brazil and Ecuador). Virus Research 153(1):100–105

    Article  PubMed  CAS  Google Scholar 

  • Costa LJ, Andrade FA, Uieda W, Martorelli LF, Kataoka AP, Fernandes ME (2013) Serological investigation of rabies virus neutralizing antibodies in bats captured in the eastern Brazilian Amazon. Trans R Soc Trop Med Hyg 107(11):684–689. https://doi.org/10.1093/trstmh/trt080

    Article  PubMed  CAS  Google Scholar 

  • de Moura WC, Gallina NMF, Fuches RMM, Romijn PC, Leite JPG (2008) Validation of a virus neutralization potency test in BHK-21 cells for rabies immunoglobulins in a two-center study. Journal of Virological Methods 154:7–13. https://doi.org/10.1016/j.jviromet.2008.09.010

    Article  PubMed  CAS  Google Scholar 

  • Dean AG, Sullivan KM, Zubieta J, Delhumeau C (2011) Epi InfoTM, a database and statistics program for public health professionals. Atlanta, GA, USA

  • Favoretto SR, de Mattos CC, Morais NB, Alves Araújo FA, de Mattos CA (2001) Rabies in marmosets (Callithrix jacchus), Ceará, Brazil. Emerging Infectious Diseases 7:1062–1065

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Favoretto SR, de Mattos CC, de Mattos CA, Campos ACA, Sacramento DRV, Durigon EL (2013) The emergence of wildlife species as a source of human rabies infection in Brazil. Epidemioly and Infection 141:1552–1561. https://doi.org/10.1017/S0950268813000198

    Article  CAS  Google Scholar 

  • Jorge RS, Pereira MS, Morato RG, Scheffer KC, Carnieli P Jr, Ferreira F, Furtado MM, Kashivakura CK, Silveira L, Jacomo AT, Lima ES, de Paula RC, May-Junior JA (2010) Detection of rabies virus antibodies in Brazilian free-ranging wild carnivores. J Wildl Dis 46(4):1310–1315. https://doi.org/10.7589/0090-3558-46.4.1310

    Article  PubMed  Google Scholar 

  • Kotait I, Oliveira RN, Carrieri ML, Castilho JG, Macedo CI, Pereira PMC, Boere V, Montebello L, Rupprecht CE (2019) Non-human primates as a reservoir for rabies virus in Brazil. Zoonoses Public Health 66, 47–59, DOI: https://doi.org/10.1111/zph.12527

  • Macedo CI Jr, Carnieli P, Brandão PE, Rosa ES, Oliveira RDN, Castilho JG, Medeiros R, Machado RR, Oliveira RCD, Carrieri ML, Kotait I (2006) Diagnosis of human rabies cases by polymerase chain reaction of neck-skin samples. Brazilian Journal of Infectious Diseases 10:341–345

    Google Scholar 

  • Machado GP, de Paula Antunes JM, Uieda W, Biondo AW, de Andrade Cruvinel TM, Kataoka AP, Martorelli LF, De Jong D, Amaral JM, Hoppe EG, Neto GG, Megid J (2012) Exposure to rabies virus in a population of free-ranging capuchin monkeys (Cebus apella nigritus) in a fragmented, environmentally protected area in southeastern Brazil. Primates 53, 227–231, DOI: https://doi.org/10.1007/s10329-012-0306-6

    Article  PubMed  Google Scholar 

  • Meske M, Fanelli A, Rocha F, Awada L, Soto PC, Mapitse N, Tizzani P (2021) Evolution of Rabies in South America and Inter-Species Dynamics (2009–2018). Trop Med Infect Dis 6:98. https://doi.org/10.3390/tropicalmed6020098

    Article  PubMed  PubMed Central  Google Scholar 

  • Ministério da Saúde (2014) Guia de vigilância de epizootias em primatas não humanos e entomologia aplicada à vigilância da febre amarela2a edição. Brasília, D.F., Brasil: Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissiveis.

  • Mochizuki N, Kobayashi Y, Sato G, Hirano S, Itou T, Ito FH, Sakai T (2011) Determination and molecular analysis of the complete genome sequence of two wild-type rabies viruses isolated from a haematophagous bat and a frugivorous bat in Brazil. J Vet Med Sci 73:759–766. https://doi.org/10.1292/jvms.10-0238

    Article  PubMed  CAS  Google Scholar 

  • Moreno JA, Baer GM (1980) Experimental rabies in the vampire bat. Am Soc Trop Med Hyg 29:254–259

    Article  CAS  Google Scholar 

  • Moutinho FFB, Andrade MGA, Nunes VMA, Rubião ECN, Batista HBCR, Romijn PC, Cattaneo CA, Oliveira FG, Oliveira RN, Marcanth N, Silvestre LGGR, Borges FVB, Bruno SF (2020) Rabies in Callithrix sp. in the urban area of Niterói, Rio de Janeiro, Brazil. Rev Soc Bras Med Trop. 53, e20190402, DOI: https://doi.org/10.1590/0037-8682-0402-2019.

    Article  PubMed  PubMed Central  Google Scholar 

  • Orlowska A, Smreczak MARCIN, Trebas P, Zmudzinski JF (2008) Comparison of real-time PCR and heminested RT-PCR methods in the detection of rabies virus infection in bats and terrestrial animals. Bull Vet Inst Pulawy 52(3):313–318

    Google Scholar 

  • R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

  • Rocha SM, de Oliveira SV, Heinemann MB, Gonçalves VSP (2017) Epidemiological Profile of Wild Rabies in Brazil (2002–2012). Transboundary and Emerging Diseases 64:624–633. https://doi.org/10.1111/tbed.12428

    Article  PubMed  CAS  Google Scholar 

  • Rupprecht CE, Hanlon CA, Hemachudha T (2002) Rabies re-examined. The Lancet Infectious Diseases 2:327–343. https://doi.org/10.1016/S1473-3099(02)00287-6

    Article  PubMed  Google Scholar 

  • Smith TG, Gilbert AT (2017) Comparison of a micro-neutralization test with the rapid fluorescent focus inhibition test for measuring rabies virus neutralizing antibodies. Trop Med Infect Dis 2(3):24. https://doi.org/10.3390/tropicalmed2030024

    Article  PubMed  PubMed Central  Google Scholar 

  • Vargas A, Romano APM, Merchán-Hamann E (2019) Human rabies in Brazil: a descriptive study, 2000–2017. Epidemiol Serv Saude 28:e2018275. https://doi.org/10.5123/S167949742019000200001

    Article  PubMed  Google Scholar 

  • WHO (2018) WHO Expert Consultation on rabies -third report. Geneva: World Health Organization technical report series, p 931

    Google Scholar 

  • Zalan E, Wilson C, Pukitis D (1979) A microtest for the quantitation of rabies virus neutralizing antibodies. Journal of Biological Standardization 7:213–220. https://doi.org/10.1016/S0092-1157(79)80024-4

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank all the staff from the state’s health secretaries that participated in the study, environmental authorities (e.g., IBAMA), and all personnel from parks and universities that contributed to this project with their relentless effort to locate marmoset groups, provide logistical support, and great interactions in the field. We thank veterinarian Caio Shivuya Pessoa for his help with marmoset capturing in Paraíba. A very special thanks to all community members that helped us locating and capturing marmosets, usually within their property. This project was directed and is dedicated to the beloved memory of Ivanete Kotait, whose perseverance and tenacity made this project happen. IK, JAB, JM, and MLC were funded by the project ‘Fatores ecológicos e antropogenicos associados à transmissão da raiva em primatas’ from the Pan American Health Organization (SCON2018-00287) and the Ministry of Health of Brazil.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julio A. Benavides.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. This study was approved by the Ethics Committee for the use of Animals (CEUA) from the Research of the Faculty of Veterinary Medicine and Zootecnia of Botucatu at the São Paulo State University (UNESP) (protocol number: 0258/2018) and by the Sistema de Autorização e Informação em Biodiversidade (SISBIO) at the Chico Mendes Institute for Biodiversity Conservation (ICMBio) (Protocol number: 66995).

Additional information

Deceased: Ivanete Kotait.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Benavides, J.A., Megid, J., Castilho, J.G. et al. No Evidence of Rabies Exposure in Wild Marmosets (Callithrix jacchus) of Northeast Brazil. EcoHealth 20, 355–361 (2023). https://doi.org/10.1007/s10393-023-01663-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-023-01663-6

Keywords

Navigation