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. 2019;8(1):218-231.
doi: 10.1080/22221751.2019.1568180.

Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018

Filipe Vieira Santos de Abreu  1   2 , Ieda Pereira Ribeiro  3 , Anielly Ferreira-de-Brito  1 , Alexandre Araujo Cunha Dos Santos  3 , Rafaella Moraes de Miranda  1 , Iule de Souza Bonelly  1 , Maycon Sebastião Alberto Santos Neves  1 , Maria Ignez Bersot  1 , Taissa Pereira Dos Santos  4 , Marcelo Quintela Gomes  1 , José Luis da Silva  5 , Alessandro Pecego Martins Romano  6 , Roberta Gomes Carvalho  7 , Rodrigo Fabiano do Carmo Said  8 , Mario Sergio Ribeiro  9 , Roberto da Costa Laperrière  10 , Eduardo Oyama Lins Fonseca  11 , Aloísio Falqueto  12 , Christophe Paupy  4 , Anna-Bella Failloux  13 , Sara Moutailler  14 , Marcia Gonçalves de Castro  1 , Mariela Martínez Gómez  3 , Monique de Albuquerque Motta  1 , Myrna Cristina Bonaldo  3 , Ricardo Lourenço-de-Oliveira  1
Affiliations

Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016-2018

Filipe Vieira Santos de Abreu et al. Emerg Microbes Infect. 2019.

Abstract

The yellow fever virus (YFV) caused a severe outbreak in Brazil in 2016-2018 that rapidly spread across the Atlantic Forest in its most populated region without viral circulation for almost 80 years. A comprehensive entomological survey combining analysis of distribution, abundance and YFV natural infection in mosquitoes captured before and during the outbreak was conducted in 44 municipalities of five Brazilian states. In total, 17,662 mosquitoes of 89 species were collected. Before evidence of virus circulation, mosquitoes were tested negative but traditional vectors were alarmingly detected in 82% of municipalities, revealing high receptivity to sylvatic transmission. During the outbreak, five species were found positive in 42% of municipalities. Haemagogus janthinomys and Hg. leucocelaenus are considered the primary vectors due to their large distribution combined with high abundance and natural infection rates, concurring together for the rapid spread and severity of this outbreak. Aedes taeniorhynchus was found infected for the first time, but like Sabethes chloropterus and Aedes scapularis, it appears to have a potential local or secondary role because of their low abundance, distribution and infection rates. There was no evidence of YFV transmission by Aedes albopictus and Aedes aegypti, although the former was the most widespread species across affected municipalities, presenting an important overlap between the niches of the sylvatic vectors and the anthropic ones. The definition of receptive areas, expansion of vaccination in the most affected age group and exposed populations and the adoption of universal vaccination to the entire Brazilian population need to be urgently implemented.

Keywords: Atlantic forest; Yellow fever.

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Figures

Figure 1.
Figure 1.
Brazilian municipalities sampled before, during and both before and during local YFV transmission. 1 – Além Paraíba; 2 – Belo Horizonte; 3 – Cachoeiras de Macacu; 4 – Cordeiros; 5 – Guapimirim; 6 – Itamonte; 7 – Itanhandu; 8 – Magé; 9 – Miguel Pereira; 10 – Niterói; 11 – Nova Friburgo; 12 – Paraty; 13 – Petrópolis; 14 – Piraí; 15 – Porciúncula; 16 – Queluz; 17 – Resende; 18 – Rio Claro; 19 – Rio de Janeiro; 20 – Silva Jardim; 21 – São Sebastião do Alto; 22 – Saquarema; 23 – Sumidouro; 24 – Três Rios; 25 – Belmiro Braga; 26 – Casimiro de Abreu; 27 – Domingos Martins; 28 – Ibatiba; 29 – Juiz de Fora; 30 – Mangaratiba; 31 – Manhumirim; 32 – Maricá; 33 – Nova Iguaçu; 34 – Salvador; 35 – Serra; 36 – Simonésia; 37 – Valença; 38 – Vitória; 39 – Volta Redonda; 40 – Angra dos reis; 41 – Carmo; 42 – Itatiaia; 43 – Macaé; 44 – Teresópolis.
Figure 2.
Figure 2.
Haemagogus leucocelaenus, Hg. janthinomys and Sabethes chloropterus distribution along sampled municipalities. Geometric forms represented species found positive for yellow fever virus per municipality.
Figure 3.
Figure 3.
Percentage of abundance (1st graph) and presence (2nd graph) of the 29 most abundant species considering both before (between may/2015 and Jan/2017) and during YFV outbreak (between fev/2017 and may/2018) moments. 3rd graph shows the Maximum Likelihood Estimate (MLE) from the same species. Name of cryptic species e.g. Hg. janthinomys, Wy. aporonoma/staminifera, Wy. palmata/galvaoi, Sa. fabricii/undosus are abbreviated.
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Grants and funding

This work was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grants no. 309577/2013-6, RLO and 440865/2016-6, MCB), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Grants no. E-26/010.001537/2014 and E-26/203.064/2016, RLO; E-26/102.351/2013, MCB), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Grant no. COFECUB 799-14, AUXPE 1731/2014), and the Institut Pasteur, Transversal Research Program (PTR Grant no. 528, RLO). The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

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