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Review
. 2018 Sep 3;113(10):e180278.
doi: 10.1590/0074-02760180278.

Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation

Cristina Possas  1 , Ricardo Lourenço-de-Oliveira  2 , Pedro Luiz Tauil  3 , Francisco de Paula Pinheiro  1 , Alcides Pissinatti  4 , Rivaldo Venâncio da Cunha  5 , Marcos Freire  1 , Reinaldo Menezes Martins  1 , Akira Homma  1
Affiliations
Review

Yellow fever outbreak in Brazil: the puzzle of rapid viral spread and challenges for immunisation

Cristina Possas et al. Mem Inst Oswaldo Cruz. .

Abstract

We discuss the complex eco-social factors involved in the puzzle of the unexpected rapid viral spread in the ongoing Brazilian yellow fever (YF) outbreak, which has increased the reurbanisation risk of a disease without urban cases in Brazil since 1942. Indeed, this rapid spatial viral dissemination to the Southeast and South regions, now circulating in the Atlantic Forest fragments close to peri-urban areas of the main Brazilian megalopolises (São Paulo and Rio de Janeiro) has led to an exponential increase in the number of yellow fever cases. In less than 18 months, 1,833 confirmed cases and 578 deaths were recorded most of them reported in the Southeast region (99,9%). Large epizooties in monkeys and other non-human primates (NHPs) were communicated in the country with 732 YF virus (YFV) laboratory confirmed events only in the 2017/2018 monitoring period. We also discuss the peculiarities and similarities of the current outbreak when compared with previous great epidemics, examining several hypotheses to explain the recent unexpected acceleration of epizootic waves in the sylvatic cycle of the YFV together with the role of human, NHPs and mosquito mobility with respect to viral spread. We conclude that the most feasible hypothesis to explain this rapidity would be related to human behavior combined with ecological changes that promoted a significant increase in mosquito and NHP densities and their contacts with humans. We emphasize the urgent need for an adequate response to this outbreak such as extending immunisation coverage to the whole Brazilian population and developing novel strategies for immunisation of NHPs confined in selected reserve areas and zoos. Finally, we stress the urgent need to improve the quality of response in order to prevent future outbreaks and a catastrophic reurbanisation of the disease in Brazil and other South American countries. Continuous monitoring of YFV receptivity and vulnerability conditions with effective control of the urban vector Aedes aegypti and significant investments in YF vaccine production capacity and research and development for reduction of adverse effects are of the highest priority.

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Figures

Fig. 1:
Fig. 1:. yellow fever: human cases and case fatalities in Brazil 1930-2017. Source: Brazilian Ministry of Health, YF Epidemiological reports 1930-2018.
Fig. 2:
Fig. 2:. yellow fever virus spread: rapid dislocation into and between Brazilian biomes. Black dashed line: viral spread from late 1980’ until 2010; white line: viral spread from the first half of the 2010 decade onward, including the ongoing outbreak in the Southeast. Sources: IBGE/MMA 2004 for map of Brazilian biomes. Brazilian Ministry of Health//SVS, YF reports from 1999-2018 for epidemiological information on epizootic waves and human cases (http://portalms.saude.gov.br/saude-de-a-z/febre-amarela-sintomas-transmissao-e-prevencao/situacao-epidemiologica-dados).
Fig. 3:
Fig. 3:. probable route of spread of yellow fever (YF) epizootics of 1934-40 in Brazil as indicated by chronologic appearance of jungle YF. Sources: Benchimol 6 ) and Strode.
Fig. 4:
Fig. 4:. yellow fever virus (YFV) transmission dynamics in Atlantic Forest biome: overlap of ecosystems and ecotone. In the last decades, the progressive combination of several factors has contributed to gradually expand the overlap of ecosystems (sylvatic and anthropic) and the ecotone as well as to imbricate the Haemagogus-vectored YFV cycle and the territory of synathropic species, facilitating YFV expansion, human infections and increasingly jeopardised the reemergence of Aedes transmission in the urban areas. Among those factors are: (a) the augmentation of areas with environmental and ecological conditions to support mosquito and non-human primate (NHP) diversity and population growth due to the success of recent environmental policies; (b) the loss of some natural habitats forcing NHPs (e.g., marmosets, capuchins) to exploit the ecotone and the modified environments and their overpopulation of remaining forest fragments; (c) adoption of new life styles and practices by the contemporary man leading to an increasing approach to the woods; (d) rapid and intense human displacements; (e) the ecological plasticity of vectors, specially the liability of Haemagogus to span long distances beyond the forest limits and Ae. albopictus to colonise and disperse from the modified into the sylvatic ecosystem; (f) the crescent infestation rates by Ae. aegypti in expanding urban and peri-urban areas near the Haemagogus-transmitted YFV cycle.
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