Parasit Vectors. 2022 Jan 10;15(1):23. doi: 10.1186/s13071-021-05143-0.

Ecological and environmental factors affecting transmission of sylvatic yellow fever in the 2017-2019 outbreak in the Atlantic Forest, Brazil.

Parasites & vectors

Filipe Vieira Santos de Abreu, Cecilia Siliansky de Andreazzi, Maycon Sebastião Alberto Santos Neves, Patrícia Soares Meneguete, Mário Sérgio Ribeiro, Cristina Maria Giordano Dias, Monique de Albuquerque Motta, Christovam Barcellos, Anselmo Rocha Romão, Mônica de Avelar Figueiredo Mafra Magalhães, Ricardo Lourenço-de-Oliveira

PMID: 35012637 DOI: 10.1186/s13071-021-05143-0

Abstract

BACKGROUND: Yellow fever virus (YFV) is an arbovirus that, despite the existence of a safe and effective vaccine, continues to cause outbreaks of varying dimensions in the Americas and Africa. Between 2017 and 2019, Brazil registered un unprecedented sylvatic YFV outbreak whose severity was the result of its spread into zones of the Atlantic Forest with no signals of viral circulation for nearly 80 years.

METHODS: To investigate the influence of climatic, environmental, and ecological factors governing the dispersion and force of infection of YFV in a naïve area such as the landscape mosaic of Rio de Janeiro (RJ), we combined the analyses of a large set of data including entomological sampling performed before and during the 2017-2019 outbreak, with the geolocation of human and nonhuman primates (NHP) and mosquito infections.

RESULTS: A greater abundance of Haemagogus mosquitoes combined with lower richness and diversity of mosquito fauna increased the probability of finding a YFV-infected mosquito. Furthermore, the analysis of functional traits showed that certain functional groups, composed mainly of Aedini mosquitoes which includes Aedes and Haemagogus mosquitoes, are also more representative in areas where infected mosquitoes were found. Human and NHP infections were more common in two types of landscapes: large and continuous forest, capable of harboring many YFV hosts, and patches of small forest fragments, where environmental imbalance can lead to a greater density of the primary vectors and high human exposure. In both, we show that most human infections (~ 62%) occurred within an 11-km radius of the finding of an infected NHP, which is in line with the flight range of the primary vectors.

CONCLUSIONS: Together, our data suggest that entomological data and landscape composition analyses may help to predict areas permissive to yellow fever outbreaks, allowing protective measures to be taken to avoid human cases.

© 2022. The Author(s).

Keywords: Functional traits; Haemagogus; Mosquito; Nonhuman primate

References

1. Monath TP, Vasconcelos PFC. Yellow fever. J Clin Virol. 2015;64:160–73. - PubMed
2. Possas C, Lourenço-de-Oliveira R, Tauil PL, Pinheiro FDP, Pissinatti A, Venâncio R, et al. Yellow fever outbreak in Brazil : the puzzle of rapid viral spread and challenges for immunisation. Mem Inst Oswaldo Cruz. 2018;113:1–12. - PubMed
3. Romano APM, Costa ZGA, Ramos DG, Andrade MA, de Jayme VS, de Almeida MAB, et al. Yellow fever outbreaks in unvaccinated populations, Brazil, 2008–2009. PLoS Negl Trop Dis. 2014;8:e2740. - PubMed
4. Dietz JM, Hankerson SJ, Alexandre BR, Henry MD, Martins AF, Ferraz LP, et al. Yellow fever in Brazil threatens successful recovery of endangered golden lion tamarins. Sci Rep. 2019;9(1):12926. - PubMed
5. Vasconcelos PFC, Costa ZG, Travassos da Rosa ES, Luna E, Rodrigues SG, Barros VLRS, et al. Epidemic of jungle yellow fever in Brazil, 2000: implications of climatic alterations in disease spread. J Med Virol. 2001;65:598–604. - PubMed
6. Brasil. Boletim Epidemiológico—Situação epidemiológica da febre amarela—Monitoramento 2020/2021. 2021. https://www.gov.br/saude/pt-br/media/pdf/2021/fevereiro/11/boletim_epidemiologico_svs_4.pdf . Acessed 10 Oct 2021. - PubMed
7. Silva NIO, Sacchetto L, De Rezende IM, Trindade GDS, Labeaud AD, De Thoisy B, et al. Recent sylvatic yellow fever virus transmission in Brazil: the news from an old disease. Virol J. 2020;17:9. - PubMed
8. Faria NR, Kraemer MUG, Hill SC, de Jesus JG, Aguiar RS, Iani FCM, et al. Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science. 2018;361:894–9. - PubMed
9. Gómez MM, de Abreu FVS, dos Santos AAC, de Mello IS, Santos MP, Ribeiro IP, et al. Genomic and structural features of the yellow fever virus from the 2016–2017 Brazilian outbreak. J Gen Virol. 2018;99:536–48. - PubMed
10. Cunha MS, da Costa AC, de Azevedo Fernandes NCC, Guerra JM, dos Santos FCP, Nogueira JS, et al. Epizootics due to yellow fever virus in São Paulo state, Brazil: viral dissemination to new areas (2016–2017). Sci Rep. 2019;9:5474. - PubMed
11. Franco O. História da Febre Amarela no Brasil. Ministério da Saúde. Rio de Janeiro: Departamento Nacional de Endemias Rurais; 1969. - PubMed
12. Bonaldo MC, Gómez MM, dos Santos AA, de Abreu FVS, Ferreira-de-Brito A, de Miranda RM, et al. Genome analysis of yellow fever virus of the ongoing outbreak in Brazil reveals polymorphisms. Mem Inst Oswaldo Cruz. 2017;112:447–51. - PubMed
13. Delatorre E, de Abreu FVS, Ribeiro IP, Gómez MM, dos Santos AAC, Ferreira-de-Brito A, et al. Distinct YFV lineages co-circulated in the Central-Western and Southeastern Brazilian regions from 2015 to 2018. Front Microbiol. 2019;10:1–12. - PubMed
14. de Abreu FVS, Delatorre E, dos Santos AAC, Ferreira-de-Brito A, de Castro MG, Ribeiro IP, et al. Combination of surveillance tools reveals that yellow fever virus can remain in the same Atlantic Forest area at least for three transmission seasons. Mem Inst Oswaldo Cruz. 2019;114:e190076. - PubMed
15. Secretaria de Saúde de Estado do Rio de Janeiro. Dados—Febre Amarela RJ. 2021. http://www.febreamarela.rj.gov.br/dados . Acessed 3 May 2021. - PubMed
16. de Abreu FVS, Ribeiro IP, Ferreira-de-Brito A, dos Santos AAC, de Miranda RM, de Bonelly IS, et al. Haemagogus leucocelaenus and Haemagogus janthinomys are the primary vectors in the major yellow fever outbreak in Brazil, 2016–2018. Emerg Microbes Infect. 2019;8:218–31. - PubMed
17. de Mares-Guia MAMM, Horta MA, Romano A, Rodrigues CDS, Mendonça MCL, dos Santos CC, et al. Yellow fever epizootics in non-human primates, Southeast and Northeast Brazil (2017 and 2018). Parasit Vectors. 2020;13:90. - PubMed
18. de Abreu FVS, Ferreira-de-Brito A, Azevedo ADS, Linhares JHR, de Oliveira SV, Hime Miranda E, et al. Survey on non-human primates and mosquitoes does not provide evidences of spillover/spillback between the urban and sylvatic cycles of yellow fever and zika viruses following severe outbreaks in Southeast Brazil. Viruses. 2020;12:364. - PubMed
19. Hamrick PN, Aldighieri S, Machado G, Leonel DG, Vilca LM, Uriona S, et al. Geographic patterns and environmental factors associated with human yellow fever presence in the Americas. PLoS Negl Trop Dis. 2017;11:e0005897. - PubMed
20. de Almeida MAB, dos Santos E, da Cardoso JC, da Silva LG, Rabelo RM, Bicca-Marques JC. Predicting yellow fever through species distribution modeling of virus, vector, and monkeys. EcoHealth. 2018;16:95–108. - PubMed
21. Childs ML, Nova N, Colvin J, Mordecai EA. Mosquito and primate ecology predict human risk of yellow fever virus spillover in Brazil. Philos Trans R Soc B Biol Sci. 2019;374:20180335. - PubMed
22. IBGE. IBGE divulga estimativa da população dos municípios para 2020. 2020 https://agenciadenoticias.ibge.gov.br/agencia-sala-de-imprensa/2013-agencia-de-noticias/releases/28668-ibge-divulga-estimativa-da-populacao-dos-municipios-para-2020 . Acessed 4 May 2021. - PubMed
23. Myneni RB, Hall FG, Sellers PJ, Marshak AL. The interpretation of spectral vegetation indexes. IEEE Trans Geosci Remote Sens. 1995;33:481–6. - PubMed
24. Consoli RAGB, de Oliveira RL. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Editora Fiocruz; 1994. - PubMed
25. Lane J, Cerqueira NL. Os Sabetíneos da América, (Diptera, Culicidae). Arquivos de Zoologia do Estado de São Paulo. 1942;3:473–849. - PubMed
26. Forattini OP. Culicidologia médica: identificação, biologia, epidemiologia, vol. 2. São Paulo: Edusp; 2002. - PubMed
27. Pavoine S, Vallet J, Dufour A-B, Gachet S, Daniel H. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos. 2009;118:391–402. - PubMed
28. Murtagh F, Legendre P. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? J Classif. 2014;31:274–95. - PubMed
29. Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25:1–18. - PubMed
30. Causey OR, Laemmert HW, Kumm HW. Dispersion of forest mosquitoes in Brazil: further studies 1. Am J Trop Med Hyg. 1950;s1–30:301–12. - PubMed
31. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26:32–46. - PubMed
32. Oksanen AJ, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, et al. Package vegan: community ecology package. R package version 4.0.3. 2019. https://cran.r-project.org/web/packages/vegan/vegan.pdf . Acessed 10 Apr 2021. - PubMed
33. Magurran A. Measuring biologcial diversity. Oxford: Wiley-Blackwell; 2004. - PubMed
34. Villéger S, Mason NWH, Mouillot D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology. 2008;89:2290–301. - PubMed
35. Laliberté E, Legendre P. A distance-based framework for measuring functional diversity from multiple traits. Ecology. 2010;91:299–305. - PubMed
36. Kleyer M, Dray S, Bello F, Lepš J, Pakeman RJ, Strauss B, et al. Assessing species and community functional responses to environmental gradients: which multivariate methods? J Veg Sci. 2012;23:805–21. - PubMed
37. Laliberté, E., Legendre, P. and BS. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. 2014. https://cran.r-project.org/web/packages/FD/FD.pdf . Acessed 10 Apr 2021. - PubMed
38. Burnham K, Anderson D. Model selection and multimodel inference—a practical information-theoretic approach. 2nd ed. New York: Springer; 2002. - PubMed
39. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG. Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol. 2011;24:699–711. - PubMed
40. Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9:378–400. - PubMed
41. Barton MK. MuMIn: Multi-Model Inference. R package version 1.43.17. 2020. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf . Acessed 10 Apr 2021. - PubMed
42. Hurvich CM, Tsai C-L. Regression and time series model selection in small samples. Biometrika. 1989;76:297–307. - PubMed
43. Pinheiro GG, Rocha MN, de Oliveira MA, Moreira LA, Andrade Filho JD. Detection of yellow fever virus in sylvatic mosquitoes during disease outbreaks of 2017–2018 in Minas Gerais state, Brazil. Insects. 2019;10:136. - PubMed
44. Couto-Lima D, Madec Y, Bersot MI, Campos SS, de Motta MA, dos Santos FB, et al. Potential risk of re-emergence of urban transmission of yellow fever virus in Brazil facilitated by competent Aedes populations. Sci Rep. 2017;7:4848. - PubMed
45. Amraoui F, Pain A, Piorkowski G, Vazeille M, Couto-Lima D, de Lamballerie X, et al. Experimental adaptation of the yellow fever virus to the mosquito Aedes albopictus and potential risk of urban epidemics in Brazil, South America. Sci Rep. 2018;8:14337. - PubMed
46. Pereira dos Santos T, Roiz D, Santos de Abreu FV, Luz SLB, Santalucia M, Jiolle D, et al. Potential of Aedes albopictus as a bridge vector for enzootic pathogens at the urban-forest interface in Brazil. Emerg Microbes Infect. 2018;7:191. - PubMed
47. Tátila-Ferreira A, de Maia DA, Alencar J. Development of preimaginal stages of Haemagogus leucocelaenus (Diptera: Culicidae) in laboratory conditions. Entomol News. 2017;127:142–50. - PubMed
48. Alencar J, Gleiser RM, Morone F, de Mello CF, dos Silva JS, Serra-Freire NM, et al. A comparative study of the effect of multiple immersions on Aedini (Diptera: Culicidae) mosquito eggs with emphasis on sylvan vectors of yellow fever virus. Mem Inst Oswaldo Cruz. 2014;109:114–7. - PubMed
49. Alencar J, de Almeida HM, Marcondes CB, Guimarães AÉ. Effect of multiple immersions on eggs and development of immature forms of Haemagogus janthinomys from South-Eastern Brazil (Diptera: Culicidae). Entomol News. 2008;119:239–45. - PubMed
50. Couto-Lima D, Andreazzi CS, Leite PJ, Bersot MIL, Alencar J, Lourenço-de-Oliveira R. Seasonal population dynamics of the primary yellow fever vector Haemagogus leucocelaenus (Dyar & Shannon) (Diptera: Culicidae) is mainly influenced by temperature in the Atlantic Forest, Southeast Brazil. Mem Inst Oswaldo Cruz. 2020;115:e200218. - PubMed
51. Romano APM, Ramos DG, Araújo FAA, de Siqueira GAM, Ribeiro MPD, Leal SG, et al. Febre amarela no Brasil: recomendações para a vigilância, prevenção e controle. Epidemiol e Serviços Saúde. 2011;20:101–6. - PubMed
52. Mucci LF, Medeiros-Sousa AR, Ceretti-Júnior W, Fernandes A, Camargo AA, Evangelista E, et al. Haemagogus leucocelaenus and other mosquitoes potentially associated with sylvatic yellow fever in Cantareira State Park in the São Paulo metropolitan area, Brazil. J Am Mosq Control Assoc. 2016;32:329–32. - PubMed
53. Cunha MS, Tubaki RM, de Menezes RMT, Pereira M, Caleiro GS, Coelho E, et al. Possible non-sylvatic transmission of yellow fever between non-human primates in São Paulo city, Brazil, 2017–2018. Sci Rep. 2020;10:15751. - PubMed
54. Schmidt KA, Ostfeld RS. Biodiversity and the dilution effect in disease ecology. Ecology. 2001;82:609–19. - PubMed
55. Mucci LF, Júnior RPC, de Paula MB, Scandar SAS, Pacchioni ML, Fernandes A, et al. Feeding habits of mosquitoes (Diptera: Culicidae) in an area of sylvatic transmission of yellow fever in the state of São Paulo, Brazil. J Venom Anim Toxins Incl Trop Dis. 2015;21:6. - PubMed
56. Swaddle JP, Calos SE. Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE. 2008;3:e2488. - PubMed
57. Fecchio A, Lima MR, Bell JA, Schunck F, Corrêa AH, Beco R, et al. Loss of forest cover and host functional diversity increases prevalence of avian malaria parasites in the Atlantic Forest. Int J Parasitol. 2021;51:719–28. - PubMed
58. Johnson BJ, Munafo K, Shappell L, Tsipoura N, Robson M, Ehrenfeld J, et al. The roles of mosquito and bird communities on the prevalence of West Nile virus in urban wetland and residential habitats. Urban Ecosyst. 2012;15:513–31. - PubMed
59. De Paiva CA, Oliveira APDS, Muniz SS, Calijuri ML, Dos Santos VJ, Alves SDC. Determination of the spatial susceptibility to yellow fever using a multicriteria analysis. Mem Inst Oswaldo Cruz. 2019;114:e180509. - PubMed
60. Wilk-da-Silva R, Mucci LF, Ceretti-Junior W, de Duarte AMRC, Marrelli MT, Medeiros-Sousa AR. Influence of landscape composition and configuration on the richness and abundance of potential sylvatic yellow fever vectors in a remnant of Atlantic Forest in the city of São Paulo, Brazil. Acta Trop. 2020;204:105385. - PubMed
61. Ilacqua RC, Medeiros-Sousa AR, Ramos DG, Obara MT, Ceretti-Junior W, Mucci LF, et al. Reemergence of yellow fever in Brazil: the role of distinct landscape fragmentation thresholds. J Environ Public Health. 2021;2021:8230789. - PubMed
62. Causey OR, Hughes TP, Laemmert HW. The invasion of small forests by yellow fever virus as indicated by immunity in Cebus monkeys 1. Am J Trop Med Hyg. 1949;S1-29:555–65. - PubMed
63. Hamlet A, Ramos DG, Gaythorpe KAM, Romano APM, Garske T, Ferguson NM. Seasonality of agricultural exposure as an important predictor of seasonal yellow fever spillover in Brazil. Nat Commun. 2021;12:3647. - PubMed
64. Hamer DH, Angelo K, Caumes E, van Genderen PJJ, Florescu SA, Popescu CP, et al. Fatal yellow fever in travelers to Brazil, 2018. Morb Mortal Wkly Rep. 2018;67:340–1. - PubMed
65. Chiarello AG, de Melo FR. Primate population densities and sizes in Atlantic forest remnants of northern Espirito Santo, Brazil. Int J Primatol. 2001;22:379–96. - PubMed
66. Martins MM. Density of primates in four semi-deciduous forest fragments of São Paulo, Brazil. Biodivers Conserv. 2005;14:2321–9. - PubMed
67. Abreu FVS, dos Santos E, Gomes MQ, Vargas WP, Oliveira Passos PH, Nunes e Silva C, et al. Capture of Alouatta guariba clamitans for the surveillance of sylvatic yellow fever and zoonotic malaria: which is the best strategy in the tropical Atlantic Forest? Am J Primatol. 2019;81:e23000. - PubMed
68. Behie AM, Pavelka MS. Primates in fragments: complexity and resilience. New York: Springer; 2013. - PubMed
69. Brasil. Guia de vigilância de epizootias em primatas não humanos e entomologia aplicada à vigilância da febre amarela. 2nd ed. Brasília: Ministério da Saúde; 2017. - PubMed
70. Giovanetti M, de Mendonça MCL, Fonseca V, Mares-Guia MA, Fabri A, Xavier J, et al. Yellow fever virus reemergence and spread in Southeast Brazil, 2016–2019. J Virol. 2019;94:e01623-e1719. - PubMed
71. Almeida MAB, da Cardoso JC, dos Santos E, da Fonseca DF, Cruz LL, Faraco FJC, et al. Surveillance for yellow fever virus in non-human primates in Southern Brazil, 2001–2011: a tool for prioritizing human populations for vaccination. PLoS Negl Trop Dis. 2014;8:e2741. - PubMed
72. Galindo P. Bionomics of Sabethes chloropterus Humboldt, a vector of sylvan yellow fever in Middle America. Am J Trop Med Hyg. 1958;7:429–40. - PubMed
73. Farnesi LC, Menna-Barreto RFS, Martins AJ, Valle D, Rezende GL. Physical features and chitin content of eggs from the mosquito vectors Aedes aegypti, Anopheles aquasalis and Culex quinquefasciatus: connection with distinct levels of resistance to desiccation. J Insect Physiol. 2015;83:43–52. - PubMed
74. Day J. Mosquito oviposition behavior and vector control. Insects. 2016;7:65. - PubMed
75. Arnell JH. Mosquito studies (Diptera, Culicidae) XXXII. A revision of the genus Haemagogus. Contrib Am Entomol Inst. 1973;10:1–174. - PubMed
76. Lounibos LP, Machado-Allison CE. Oviposition and egg brooding by the mosquito Trichoprosopon digitatum in cacao husks. Ecol Entomol. 1983;8:475–8. - PubMed
77. Tátila-Ferreira A, de Maia DA, de Abreu FVS, Rodrigues WC, Alencar J. Oviposition behavior of Haemagogus leucocelaenus (Diptera: Culicidae), a vector of wild yellow fever in Brazil. Rev Inst Med Trop Sao Paulo. 2017;59:e60. - PubMed
78. Shannon RC. The environment and behavior of some Brazilian mosquitoes. Proc Ent Soc Wash. 1931;33:1–27. - PubMed
79. Bates M. The natural history of mosquitoes. New York: The Macmillan Company; 1949. - PubMed
80. Bradshaw WE, Holzapfel CM, Kleckner CA, Hard JJ. Heritability of development time and protandry in the pitcher-plant mosquito Wyeomyia smithii. Ecology. 1997;78:969–76. - PubMed
81. Lima MIB, Motta MA, Lourenço De Oliveira R. Aspectos bionômicos de Sabethes (Peytonulus) identicus Dyar & Knab, 1907 (Diptera: Culicidae) em laboratório. 2014. https://www.arca.fiocruz.br/bitstream/icict/34787/2/maria_bersot_ioc_espec_2014.pdf . Acessed 11 Jun 2021. - PubMed
82. Lourenço-de-Oliveira R. Alguns aspectos da ecologia dos mosquitos (Diptera: Culicidae) de uma área de planície (Granjas Calábria), em Jacarepaguá, Rio de Janeiro. I. frequência comparativa das espécies em diferentes ambientes e métodos de coleta. Mem Inst Oswaldo Cruz. 1984;79:479–90. - PubMed
83. Lourenço-de-Oliveira R, Heyden R. Alguns aspectos da ecologia dos mosquitos (Diptera: Culicidae) de uma área de planície (Granjas Calábria) em Jacarepaguá, Rio de Janeiro: IV. Preferências alimentares quanto ao hospedeiro e freqüência domiciliar. Mem Inst Oswaldo Cruz. 1986;81:15–27. - PubMed
84. Guimarães AÉ, Arlé M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Orgãos, estado do Rio de Janeiro, Brasil: IV. Preferência alimentar. Mem Inst Oswaldo Cruz. 1987;82:277–85. - PubMed
85. Alencar J, Lorosa ES, Dégallier N, Serra-Freire NM, Pacheco JB, Guimarães AÉ. Feeding patterns of Haemagogus janthinomys (Diptera: Culicidae) in different regions of Brazil. J Med Entomol. 2005;42:981–5. - PubMed
86. Nielsen HT. Swarming and some other habits of Mansonia perturbans and Psorophora ferox (Diptera: Culicidae). Behaviour. 1964;24:67–88. - PubMed
87. Lourenço-de-Oliveira R, da Silva TF, Heyden R. Alguns aspectos da ecologia dos mosquitos (Diptera: Culicidae) de uma área de planície (Granjas Calábria), em Jacarepaguá, Rio de Janeiro: II. Frequência mensal e no ciclo lunar. Mem Inst Oswaldo Cruz. 1985;80:123–33. - PubMed
88. Deane LM, Ferreira Neto JA, Lima MM. The vertical dispersion of Anopheles (Kerteszia) cruzi in a forest in Southern Brazil suggests that human cases of malaria of simian origin might be expected. Mem Inst Oswaldo Cruz. 1984;79:461–3. - PubMed
89. Guimarães AE, Arlé M, Machado RNM. Mosquitos no Parque Nacional da Serra dos Órgãos, estado do Rio de Janeiro, Brasil. II. Distribuição vertical. Mem Inst Oswaldo Cruz. 1985;80:171–85. - PubMed
90. Dégallier N, SÁ Filho GC, Monteiro HAO, Castro FC, Vaz Da Silva O, Brandão RCF, et al. Release–recapture experiments with canopy mosquitoes in the Genera Haemagogus and Sabethes (Diptera: Culicidae) in Brazilian Amazonia. J Med Entomol. 1998;35:931–6. - PubMed
91. Alencar J, Morone F, De Mello CF, Dégallier N, Lucio PS, Da Serra-Freire NM, et al. Flight height preference for oviposition of mosquito (Diptera: Culicidae) vectors of sylvatic yellow fever virus near the hydroelectric reservoir of Simplício, Minas Gerais, Brazil. J Med Entomol. 2013;50:791–5. - PubMed
92. Lira-Vieira AR, Gurgel-Goncalves R, Moreira IM, Yoshizawa MAC, Coutinho ML, Prado PS, et al. Ecological aspects of mosquitoes (Diptera: Culicidae) in the gallery forest of Brasilia National Park, Brazil, with an emphasis on potential vectors of yellow fever. Rev Soc Bras Med Trop. 2013;46:566–74. - PubMed
93. Hendy A, Hernandez-Acosta E, Valério D, Mendonça C, Costa ER, Júnior JTA, et al. The vertical stratification of potential bridge vectors of mosquito-borne viruses in a central Amazonian forest bordering Manaus, Brazil. Sci Rep. 2020;10:18254. - PubMed
94. Pereira-Silva JW, Ríos-Velásquez CM, de Lima GR, MarialvadosSantos EF, Belchior HCM, Luz SLB, et al. Distribution and diversity of mosquitoes and Oropouche-like virus infection rates in an Amazonian rural settlement. PLoS ONE. 2021;16:e0246932. - PubMed
95. Galindo P, Carpenter SJ, Trapido H. A contribution to the ecology and biology of tree hole breeding mosquitoes of Panama1. Ann Entomol Soc Am. 1955;48:158–64. - PubMed
96. Galindo P, Trapido H, Carpenter SJ, Blanton FS. The abundance cycles of arboreal mosquitoes during six years at a sylvan yellow fever locality in Panama. Ann Entomol Soc Am. 1956;49:543–7. - PubMed
97. Chadee DD. Seasonal abundance and diel landing periodicity of Sabethes chloropterus (Diptera: Culicidae) in Trinidad, West Indies. J Med Entomol. 1990;27:1041–4. - PubMed
98. Lourenço-de-Oliveira R, Castro MG, Braks MAH, Lounibos LP. The invasion of urban forest by dengue vectors in Rio de Janeiro. J Vector Ecol. 2004;29:94–100. - PubMed
99. Santos EB, Favretto MA, Müller GA. When and what time? On the seasonal and daily patterns of mosquitoes (Diptera: Culicidae) in an Atlantic Forest remnant from Southern Brazil. Austral Entomol. 2020;59:337–44. - PubMed
100. Hendy A, Hernandez-Acosta E, Chaves BA, Fé NF, Valério D, Mendonça C, et al. Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil. Acta Trop. 2020;206:105441. - PubMed
101. Davis NC, Shannon RC. Studies on yellow fever in South America : V. Transmission experiments with certain species of Culex and Aedes. J Exp Med. 1929;50:803–8. - PubMed
102. Davis NC, Shannon RC. Further attempts to transmit yellow fever with mosquitoes of South America. Am J Epidemiol. 1931;14:715–22. - PubMed
103. Whitman L, Antunes PCA. Studies on the capacity of mosquitoes of the genus Haemagogus to transmit yellow fever 1. Am J Trop Med Hyg. 1937;17(suppl. 1):825–31. - PubMed
104. Shannon RC, Whitman L, Franca M. Yellow fever virus in jungle mosquitoes. Science. 1938;88:110–1. - PubMed
105. Dégallier N, Travassos da Rosa APA, Vasconcelos PFC, Travassos da Rosa ES, Rodrigues SG, Sa FGC, et al. New entomological and virological data on the vectors of sylvatic yellow fever in Brazil. J Braz Assoc Advanc Sci. 1992;44:136–42. - PubMed
106. Vasconcelos PFC, Rodrigues SG, Degallier N, Moraes MAP, Travassos Da Rosa JFS, Travassos Da Rosa ES, et al. An epidemic of sylvatic yellow fever in the southeast region of Maranhao State, Brazil, 1993–1994: epidemiologic and entomologic findings. Am J Trop Med Hyg. 1997;57:132–7. - PubMed
107. Vasconcelos PFC, Rosa APAT, Rodrigues SG, Rosa EST, Monteiro HAO, Cruz ACR, et al. Yellow fever in Pará State, Amazon region of Brazil, 1998–1999: entomologic and epidemiologic findings. Emerg Infect Dis. 2001;7:565–9. - PubMed
108. Lourenço-de-Oliveira R, Vazeille M, de Filippis AMB, Failloux A-B. Large genetic differentiation and low variation in vector competence for dengue and Yellow Fever viruses of Aedes albopictus from Brazil, the United States, and the Cayman Islands. Am J Trop Med Hyg. 2003;69:105–14. - PubMed
109. da Cardoso JC, de Almeida MAB, dos Santos E, da Fonseca DF, Sallum MAM, Noll CA, et al. Yellow fever virus in Haemagogus leucocelaenus and Aedes serratus mosquitoes, Southern Brazil, 2008. Emerg Infect Dis. 2010;16:1918–24. - PubMed
110. Moreno ES, Rocco IM, Bergo ES, Brasil RA, Siciliano MM, Suzuki A, et al. Reemergência de febre amarela: Detecção de transmissão no estado de São Paulo, Brasil, 2008. Rev Soc Bras Med Trop. 2011;44:290–6. - PubMed
111. Goenaga S, Fabbri C, Dueñas JCR, Gardenal CN, Rossi GC, Calderon G, et al. Isolation of yellow fever virus from mosquitoes in Misiones province, Argentina. Vector-Borne Zoonotic Dis. 2012;12:986–93. - PubMed
112. Cunha MS, Faria NR, Caleiro GS, Candido DS, Hill SC, Claro IM, et al. Genomic evidence of yellow fever virus in Aedes scapularis, southeastern Brazil, 2016. Acta Trop. 2020;205:105390. - PubMed

Publication Types

• Journal Article

Grant support

• E-26/010.001537/2014/Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
• 430408/2018-8/Conselho Nacional de Desenvolvimento Científico e Tecnológico
• 1912-32354/Instituto Serrapilheira