Neighbor danger: Yellow fever virus epizootics in urban and urban-rural transition areas of Minas Gerais state, during 2017-2018 yellow fever outbreaks in Brazil

PLoS Negl Trop Dis. 2020 Oct 5;14(10):e0008658. doi: 10.1371/journal.pntd.0008658. eCollection 2020 Oct.

Abstract

Background: From the end of 2016 until the beginning of 2019, Brazil faced a massive sylvatic yellow fever (YF) outbreak. The 2016-2019 YF epidemics affected densely populated areas, especially the Southeast region, causing thousands of deaths of humans and non-human primates (NHP).

Methodology/principal findings: We conducted a molecular investigation of yellow fever virus (YFV) RNA in 781 NHP carcasses collected in the urban, urban-rural interface, and rural areas of Minas Gerais state, from January 2017 to December 2018. Samples were analyzed according to the period of sampling, NHP genera, sampling areas, and sampling areas/NHP genera to compare the proportions of YFV-positive carcasses and the estimated YFV genomic loads. YFV infection was confirmed in 38.1% of NHP carcasses (including specimens of the genera Alouatta, Callicebus, Callithrix, and Sapajus), from the urban, urban-rural interface, and rural areas. YFV RNA detection was positively associated with epidemic periods (especially from December to March) and the rural environment. Higher median viral genomic loads (one million times) were estimated in carcasses collected in rural areas compared to urban ones.

Conclusions/significance: The results showed the wide occurrence of YF in Minas Gerais in epidemic and non-epidemic periods. According to the sylvatic pattern of YF, a gradient of viral dissemination from rural towards urban areas was observed. A high YF positivity was observed for NHP carcasses collected in urban areas with a widespread occurrence in 67 municipalities of Minas Gerais, including large urban centers. Although there was no documented case of urban/Aedes YFV transmission to humans in Brazil during the 2016-2019 outbreaks, YFV-infected NHP in urban areas with high infestation by Aedes aegypti poses risks for YFV urban/Aedes transmission and urbanization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aedes / virology
  • Alouatta / virology
  • Animals
  • Brazil / epidemiology
  • Callicebus / virology
  • Callithrix / virology
  • Disease Reservoirs / virology
  • Epidemics
  • Genome, Viral
  • Humans
  • Mosquito Vectors / virology
  • Primates / virology
  • Sapajus / virology
  • Yellow Fever / epidemiology*
  • Yellow Fever / prevention & control*
  • Yellow Fever / transmission*
  • Yellow fever virus / isolation & purification
  • Yellow fever virus / pathogenicity
  • Zoonoses / epidemiology
  • Zoonoses / transmission
  • Zoonoses / virology*

Grants and funding

This work was supported by different agencies. BPD was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), under Grant APQ-01574-17, and Secretaria de Estado de Saúde de Minas Gerais (SES-MG)/Secretaria de Estado de Planejamento de Minas Gerais (SEPLAG-MG)/Instituto René Rachou/Fundação Oswaldo Cruz (IRR/FIOCRUZ) under Grant Yellow fever. GST was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under grant 440593/2016-6 and Decit/SCTIE/MoH under grant 440593/2016-6. APP was supported by FAPEMIG and Coodernação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). BdT was supported by the RESERVOIRS program supported by European (ERDF/FEDER) funds and assistance from Collectivité Territoriale de la Guyane and Direction Régionale pour la Recherche et la Technologie, and the MicroBIOME project granted by the Laboratoire d’Excellence CEBA “Investissement d’Avenir” under Grant ANR-10-LABX-2501. PAA was supported by FAPEMIG under grant APQ-01989-18. MLN was supported by Fundação de Amparo à Pesquisa do estado de São Paulo (FAPESP) under grant 13/21719-3. LS and IMR were supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)/Brazil under graduate scholarship grant (0001) and NIOS was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under graduate scholarship grant, VEM was supported by Pró-Reitoria de Graduação-Universidade Federal de Minas Gerais (UFMG) under graduate scholarship grant. MAS, TAC, and GFGO were supported by CNPq FAPEMIG, and CAPES undergraduate scholarship grants. BPD, APP, GST, EGK, and MLN are CNPq Research Fellows. CNPq: http://www.cnpq.br/ CAPES: https://www.capes.gov.br/ FAPEMIG: https://fapemig.br/pt/ FAPESP: http://www.fapesp.br/ Pró-Reitoria de Graduação-Universidade Federal de Minas Gerais: https://www2.ufmg.br/prograd/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.