Impacts of Zika emergence in Latin America on endemic dengue transmission

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Abstract

In 2015 and 2016, Zika virus (ZIKV) swept through dengue virus (DENV) endemic areas of Latin America. These viruses are of the same family, share a vector and may interact competitively or synergistically through human immune responses. We examine dengue incidence from Brazil and Colombia before, during, and after the Zika epidemic. We find evidence that dengue incidence was atypically low in 2017 in both countries. We investigate whether subnational Zika incidence is associated with changes in dengue incidence and find mixed results. Using simulations with multiple assumptions of interactions between DENV and ZIKV, we find cross-protection suppresses incidence of dengue following Zika outbreaks and low periods of dengue incidence are followed by resurgence. Our simulations suggest correlations in DENV and ZIKV reproduction numbers could complicate associations between ZIKV incidence and post-ZIKV DENV incidence and that periods of low dengue incidence are followed by large increases in dengue incidence.

Abstract

Dengue and Zika virus are related flaviviruses, and introduction of Zika in the Americas may have impacted dengue epidemiology. Here, Borchering et al. show that dengue incidence was unusually low in 2017 in Brazil and Colombia, and simulations incorporating immune-mediated interactions predict reductions in dengue following Zika outbreaks with subsequent rebounds.

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Most cited references 18

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Inference from Iterative Simulation Using Multiple Sequences

Andrew Gelman, Donald B Rubin (1992)

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High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus.

Anubis Vega-Rúa, Karima Zouache, Romain Girod … (2014)

Chikungunya virus (CHIKV) causes a major public health problem. In 2004, CHIKV began an unprecedented global expansion and has been responsible for epidemics in Africa, Asia, islands in the Indian Ocean region, and surprisingly, in temperate regions, such as Europe. Intriguingly, no local transmission of chikungunya virus (CHIKV) had been reported in the Americas until recently, despite the presence of vectors and annually reported imported cases. Here, we assessed the vector competence of 35 American Aedes aegypti and Aedes albopictus mosquito populations for three CHIKV genotypes. We also compared the number of viral particles of different CHIKV strains in mosquito saliva at two different times postinfection. Primarily, viral dissemination rates were high for all mosquito populations irrespective of the tested CHIKV isolate. In contrast, differences in transmission efficiency (TE) were underlined in populations of both species through the Americas, suggesting the role of salivary glands in selecting CHIKV for highly efficient transmission. Nonetheless, both mosquito species were capable of transmitting all three CHIKV genotypes, and TE reached alarming rates as high as 83.3% and 96.7% in A. aegypti and A. albopictus populations, respectively. A. albopictus better transmitted the epidemic mutant strain CHIKV_0621 of the East-Central-South African (ECSA) genotype than did A. aegypti, whereas the latter species was more capable of transmitting the original ECSA CHIKV_115 strain and also the Asian genotype CHIKV_NC. Therefore, a high risk of establishment and spread of CHIKV throughout the tropical, subtropical, and even temperate regions of the Americas is more real than ever. Until recently, the Americas had never reported chikungunya (CHIK) autochthonous transmission despite its global expansion beginning in 2004. Large regions of the continent are highly infested with Aedes aegypti and Aedes albopictus mosquitoes, and millions of dengue (DEN) cases are annually recorded. Indeed, DEN virus and CHIK virus (CHIKV) share the same vectors. Due to a recent CHIK outbreak affecting Caribbean islands, the need for a Pan-American evaluation of vector competence was compelling as a key parameter in assessing the epidemic risk. We demonstrated for the first time that A. aegypti and A. albopictus populations throughout the continent are highly competent to transmit CHIK irrespective of the viral genotypes tested. The risk of CHIK spreading throughout the tropical, subtropical, and even temperate regions of the Americas is more than ever a reality. In light of our results, local authorities should immediately pursue and reinforce epidemiological and entomological surveillance to avoid a severe epidemic.

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Interactions between serotypes of dengue highlight epidemiological impact of cross-immunity

Nicholas Reich, Sourya Shrestha, Aaron A. King … (2013)

Dengue, a mosquito-borne virus of humans, infects over 50 million people annually. Infection with any of the four dengue serotypes induces protective immunity to that serotype, but does not confer long-term protection against infection by other serotypes. The immunological interactions between serotypes are of central importance in understanding epidemiological dynamics and anticipating the impact of dengue vaccines. We analysed a 38-year time series with 12 197 serotyped dengue infections from a hospital in Bangkok, Thailand. Using novel mechanistic models to represent different hypothesized immune interactions between serotypes, we found strong evidence that infection with dengue provides substantial short-term cross-protection against other serotypes (approx. 1–3 years). This is the first quantitative evidence that short-term cross-protection exists since human experimental infection studies performed in the 1950s. These findings will impact strategies for designing dengue vaccine studies, future multi-strain modelling efforts, and our understanding of evolutionary pressures in multi-strain disease systems.

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Author and article information

Contributors

Rebecca K. Borchering: rebecca.borchering@uga.edu

Derek A. T. Cummings:

ORCID: http://orcid.org/0000-0002-9437-1907

datc@ufl.edu

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 16 December 2019

Publication date PMC-release: 16 December 2019

Publication date Collection: 2019

Volume: 10

Electronic Location Identifier: 5730

Affiliations

[1 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Department of Biology and Emerging Pathogens Institute, , University of Florida, ; Gainesville, FL 32610 USA

[2 ]ISNI 0000 0004 1936 738X, GRID grid.213876.9, Odum School of Ecology, , University of Georgia, ; Athens, GA 30602 USA

[3 ]ISNI 0000 0001 2171 9311, GRID grid.21107.35, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, , Johns Hopkins University, ; Baltimore, MD 21205 USA

[4 ]ISNI 0000 0004 1936 8091, GRID grid.15276.37, Department of Biostatistics, College of Public Health and Health Professions, , University of Florida, ; Gainesville, FL 32610 USA

[5 ]ISNI 0000 0001 2297 6811, GRID grid.266102.1, Department of Medicine, , University of California, San Francisco, ; San Francisco, CA 94143 USA

Author information

Angkana T. Huang http://orcid.org/0000-0002-9857-3506

Leah C. Katzelnick http://orcid.org/0000-0003-1033-6758

Gregory D. King http://orcid.org/0000-0002-3670-040X

Derek A. T. Cummings http://orcid.org/0000-0002-9437-1907

Article

Publisher ID: 13628

DOI: 10.1038/s41467-019-13628-x

PMC ID: 6915707

PubMed ID: 31844054

SO-VID: 1a0dc01e-2464-48bf-8e3d-61d539656b82

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 27 February 2019

Date accepted : 14 November 2019

Funding

Funded by: FundRef https://doi.org/10.13039/100000030, U.S. Department of Health & Human Services | Centers for Disease Control and Prevention (CDC);

Award ID: U01CK000510

Award Recipient : Gregory D. King

Funded by: FundRef https://doi.org/10.13039/100000002, U.S. Department of Health & Human Services | National Institutes of Health (NIH);

Award ID: R01AI102939

Award Recipient : Justin Lessler

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ScienceOpen disciplines: Uncategorized

Keywords: computational biology and bioinformatics,ecological epidemiology,dengue virus,infectious diseases

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ScienceOpen disciplines: Uncategorized

Keywords: computational biology and bioinformatics, ecological epidemiology, dengue virus, infectious diseases

Impacts of Zika emergence in Latin America on endemic dengue transmission

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Zika Virus

Most cited references 18

Inference from Iterative Simulation Using Multiple Sequences

High level of vector competence of Aedes aegypti and Aedes albopictus from ten American countries as a crucial factor in the spread of Chikungunya virus.

Interactions between serotypes of dengue highlight epidemiological impact of cross-immunity

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