Abstract
At the end of 2016, Brazil experienced an unprecedented yellow fever (YF) outbreak. Clinical, molecular and ecological aspects of human and non-human primate (NHP) samples collected at the beginning of the outbreak are described in this study. Spatial distribution analyses demonstrated a strong overlap between human and NHP cases. Through molecular analyses, we showed that the outbreak had a sylvatic origin, caused by the South American genotype 1 YFV, which has already been shown to circulate in Brazil. As expected, the clusters of cases were identified in regions with a low vaccination coverage. Our findings highlight the importance of the synchronization of animal surveillance and health services to identify emerging YF cases, thereby promoting a better response to the vulnerable population.
This is a preview of subscription content, log in via an institution to check access.
References
Barbosa, C. M., Di Paola, N., Cunha, M. P., Rodrigues-Jesus, M. J., Araujo, D. B., Silveira, V. B., Oliveira, D. B. L. (2018). Yellow Fever Virus in Urine and Semen of Convalescent Patient, Brazil. Emerg Infect Dis, 24(1). https://doi.org/10.3201/eid2401.171310.
Barrett, A. D., and S. Higgs. 2007. “Yellow fever: a disease that has yet to be conquered.” Annu Rev Entomol 52:209-29. https://doi.org/10.1146/annurev.ento.52.110405.091454.
Bonaldo, M. C., M. M. Gómez, A. A. Dos Santos, F. V. S. Abreu, A. Ferreira-de-Brito, R. M. Miranda, M. G. Castro, and R. Lourenço-de-Oliveira. 2017. “Genome analysis of yellow fever virus of the ongoing outbreak in Brazil reveals polymorphisms.” Mem Inst Oswaldo Cruz 112 (6):447-451. https://doi.org/10.1590/0074-02760170134.
Brasil (2005) Manual de vigilância de epizootias em primatas não humanos, 1 edn., Brasília, DF: Ministério da Saúde. Secretaria de Vigilância em Saúde Departamento de Vigilância Epidemiológica
Brasil (2017a) Atualização sobre a investigação de casos suspeitos de febre amarela silvestre, Minas Gerais, 2017. Secretaria de Estado e Saúde de Minas Gerais. Retrieved March 2017. https://sbim.org.br/images/files/sesmg-febreamarela-13022017.pdf
Brasil (2017b) Informe Especial Febre Amarela No Brasil Nº 01/2017. Ministério da Saúde, Secretaria de Vigilância em Saúde. Retrieved March 2017. http://portalarquivos2.saude.gov.br/images/pdf/2017/marco/18/Informe-especial-COES-FA.pdf
Brasil (2017c) Cobertura Vacinal de febre amarela, por município, no período de 2007 a 2016, Minas Gerais. Retrieved May 2017. http://www.saude.mg.gov.br/component/gmg/page/1615-febre-amarela-2017
Brasil (2017d) Ministério da Saúde anuncia fim do surto de febre amarela, mas alerta para o próximo verão. Ministério da Saúde. Retrieved September 2017. http://u.saude.gov.br/index.php/cidadao/principal/agencia-saude/29502-ministerio-da-saude-declara-fim-do-surto-de-febre-amarela
Carrington, C. V., and A. J. Auguste. 2013. “Evolutionary and ecological factors underlying the tempo and distribution of yellow fever virus activity.” Infect Genet Evol 13:198-210. https://doi.org/10.1016/j.meegid.2012.08.015.
Costa Z, Romano A, Elkhoury A, Flannery B (2011) Evolução histórica da vigilância epidemiológica e do controle da febre amarela no Brasil. Revista Pan-Amazônica de Saúde 2, 11–26. http://scielo.iec.gov.br/pdf/rpas/v2n1/v2n1a02.pdf
De Almeida, M. A., E. Dos Santos, J. da Cruz Cardoso, D. F. da Fonseca, C. A. Noll, V. R. Silveira, A. Y. Maeda, R. P. de Souza, C. Kanamura, and R. A. Brasil. 2012. “Yellow fever outbreak affecting Alouatta populations in southern Brazil (Rio Grande do Sul State), 2008-2009.” Am J Primatol 74 (1):68-76. https://doi.org/10.1002/ajp.21010
De Morais Bronzoni, R. V., F. G. Baleotti, R. M. Ribeiro Nogueira, M. Nunes, and L. T. Moraes Figueiredo. 2005. “Duplex reverse transcription-PCR followed by nested PCR assays for detection and identification of Brazilian alphaviruses and flaviviruses.” J Clin Microbiol 43 (2):696-702. https://doi.org/10.1128/jcm.43.2.696-702.2005.
Dierssen, U., F. Rehren, C. Henke-Gendo, G. Harste, and A. Heim. 2008. “Rapid routine detection of enterovirus RNA in cerebrospinal fluid by a one-step real-time RT-PCR assay.” J Clin Virol 42 (1):58-64. https://doi.org/10.1016/j.jcv.2007.11.016.
Engelmann, F., L. Josset, T. Girke, B. Park, A. Barron, J. Dewane, E. Hammarlund, A. Lewis, M. K. Axthelm, M. K. Slifka, and I. Messaoudi. 2014. “Pathophysiologic and transcriptomic analyses of viscerotropic yellow fever in a rhesus macaque model.” PLoS Negl Trop Dis 8 (11):e3295. https://doi.org/10.1371/journal.pntd.0003295.
Fernandes N, Cunha M, Guerra J, Réssio R, Cirqueira C, Iglezias S, et al. (2017) Outbreak of yellow fever among nonhuman primates, Espirito Santo, Brazil, 2017. Emerging infectious diseases 23(12):2038-2041. https://doi.org/10.3201/eid2312.170685.
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol, 59(3), 307-321. https://doi.org/10.1093/sysbio/syq010.
Jorge, T. R., A. L. Mosimann, L. Noronha, A. Maron, and C. N. Duarte Dos Santos. 2017. “Isolation and characterization of a Brazilian strain of yellow fever virus from an epizootic outbreak in 2009.” Acta Trop 166:114-120. https://doi.org/10.1016/j.actatropica.2016.09.030.
Kuno, G., J. S. Mackenzie, S. Junglen, Z. Hubálek, A. Plyusnin, and D. J. Gubler. 2017. “Vertebrate Reservoirs of Arboviruses: Myth, Synonym of Amplifier, or Reality?” Viruses 9 (7). https://doi.org/10.3390/v9070185.
Leal, S. G., A. P. Romano, R. V. Monteiro, C. B. Melo, P. F. Vasconcelos, and M. B. Castro. 2016. “Frequency of histopathological changes in Howler monkeys (Alouatta sp.) naturally infected with yellow fever virus in Brazil.” Rev Soc Bras Med Trop 49 (1):29-33. https://doi.org/10.1590/0037-8682-0363-2015.
Leo, Y. S., A. L. Chow, L. K. Tan, D. C. Lye, L. Lin, and L. C. Ng. 2009. “Chikungunya outbreak, Singapore, 2008.” Emerg Infect Dis 15 (5):836-7. https://doi.org/10.3201/eid1505.081390.
Mir, D., E. Delatorre, M. Bonaldo, R. Lourenço-de-Oliveira, A. C. Vicente, and G. Bello. 2017. “Phylodynamics of Yellow Fever Virus in the Americas: new insights into the origin of the 2017 Brazilian outbreak.” Sci Rep 7 (1):7385. https://doi.org/10.1038/s41598-017-07873-7.
Monath, T. P. 2001. “Yellow fever: an update.” Lancet Infect Dis 1 (1):11-20. https://doi.org/10.1016/s1473-3099(01)00016-0.
Monath, T. P., and P. F. Vasconcelos. 2015. “Yellow fever.” J Clin Virol 64:160-73. https://doi.org/10.1016/j.jcv.2014.08.030.
Moreira-Soto, A., M. C. Torres, M. C. Lima de Mendonça, M. A. Mares-Guia, C. D. Dos Santos Rodrigues, A. A. Fabri, C. C. Dos Santos, E. S. Machado Araújo, C. Fischer, R. M. Ribeiro Nogueira, C. Drosten, P. C. Sequeira, J. F. Drexler, and A. M. Bispo de Filippis. 2018. “Evidence for multiple sylvatic transmission cycles during the 2016-2017 yellow fever virus outbreak, Brazil.” Clin Microbiol Infect. https://doi.org/10.1016/j.cmi.2018.01.026.
Moreno ES, Spinola R, Tengan CH, Brasil RA, Siciliano MM, Coimbra TL, Silveira VR, Rocco IM, Bisordi I, Souza RP, Petrella S, Pereira LE, Maeda AY, Silva FG, Suzuki A (2013) Yellow fever epizootics in non-human primates, São Paulo state, Brazil, 2008–2009. Revista do Instituto de Medicina Tropical de São Paulo 55(1):45–50. https://www.ncbi.nlm.nih.gov/pubmed/23328725
Patel, P., O. Landt, M. Kaiser, O. Faye, T. Koppe, U. Lass, A. A. Sall, and M. Niedrig. 2013. “Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses.” Virol J 10:58. https://doi.org/10.1186/1743-422x-10-58.
Pessanha JEM (2009) Yellow fever: a vision of the current scenario. Vol. 19, Revista médica de Minas Gerais
Plowright, R. K., Parrish, C. R., McCallum, H., Hudson, P. J., Ko, A. I., Graham, A. L., & Lloyd-Smith, J. O. (2017). Pathways to zoonotic spillover. Nat Rev Microbiol, 15(8), 502-510. https://doi.org/10.1038/nrmicro.2017.45
Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol, 25(7), 1253–1256.https://doi.org/10.1093/molbev/msn083
Saúde (2017) Ministério da Saúde, Guia De Vigilância De Epizootias Emprimatas Não Humanos E Entomologia Aplicada À Vigilância Da Febre Amarela, Brasilia
Saúde (2018) Ministério da Saúde, Retrieved April 2018. www.portalsaude.saude.gov.br
Vasilakis N, Weaver SC (2017) Flavivirus transmission focusing on Zika. Current Opinion in Virology 22:30–35. https://www.ncbi.nlm.nih.gov/pubmed/27936448
WHO (2008) World Health Organization. Detection and investigation of serious adverse events following yellow fever vaccination, Geneva, World Health Organization. Retrieved June 2018. http://www.who.int/csr/resources/publications/HSE_GAR_ERI_2010_2/en/
WHO (2017) World Health Organization. Yellow fever vaccination recomendations in the Americans, 2017. Retrieved May 2017. www.who.int/ith/yellow-fever-risk-mapping/risk_mapping/en/
Acknowledgements
We are thankful to Zoovet Clınica e Consultoria LTDA and Bicho do Mato Meio Ambiente, which provided NHP samples from Conceição do Mato Dentro, Minas Gerais, Brazil. We thank Galileu Barbosa Costa for the critical review of this work and Grant M. Williams for English review. We also thank colleagues from the Laboratório de Vírus (ICB-UFMG) for their excellent technical support. This work has received financial support from Brazilian agencies CAPES and CNPq in accordance with the MCTIC/FNDCT-CNPq/ MEC-CAPES/ MS-Decit / Nº 14/2016 – Prevenção e Combate ao vírus Zika.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Disclaimer: The opinions expressed by authors contributing to this journal do not necessarily reflect the opinions of the institutions with which the authors are affiliated.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Figure 1:
Timeline of disease course. Temporal description of the main signs and symptoms presented by the patient. (TIFF 110 kb)
Supplementary Figure 2:
Phylogenetic tree constructed based on nucleotide sequences of 207 bp of Yellow fiver virus NS5 region. The selection of the best-fit nucleotide substitution model was performed using jModelTest (Posada, 2008). Phylogenetic tree reconstruction using maximum likelihood methods (ML) was performed using MEGA 7 (http://www.megasoftware.net) with 1000 bootstrap replicates by use of the Akaike information criterion (AIC) (Guindon et al., 2010). Based on the AIC, the GTR+G was the best-fit model. These parameters were used for phylogenetic tree reconstruction. Black circles indicate samples in this study and numbers along branches are bootstrap values. (TIFF 313 kb)
Rights and permissions
About this article
Cite this article
Figueiredo, P.O., Silva, A.T.S., Oliveira, J.S. et al. Detection and Molecular Characterization of Yellow Fever Virus, 2017, Brazil. EcoHealth 15, 864–870 (2018). https://doi.org/10.1007/s10393-018-1364-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-018-1364-z