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Research Article

Asymptomatic humans transmit dengue virus to mosquitoes

Veasna Duong, Louis Lambrechts, Richard E. Paul, Sowath Ly, Rath Srey Lay, Kanya C. Long, Rekol Huy, Arnaud Tarantola, Thomas W. Scott, Anavaj Sakuntabhai, and Philippe Buchy
PNAS November 24, 2015 112 (47) 14688-14693; first published November 9, 2015; https://doi.org/10.1073/pnas.1508114112
Veasna Duong
aVirology Unit, Institut Pasteur in Cambodia, International Network of Pasteur Institutes, 12201 Phnom Penh, Cambodia;
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Louis Lambrechts
bInsect–Virus Interactions Group, Department of Genomes and Genetics, Institut Pasteur, 75015 Paris, France;
cCentre National de la Recherche Scientifique, Unité de Recherche Associée 3012, 75015 Paris, France;
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Richard E. Paul
cCentre National de la Recherche Scientifique, Unité de Recherche Associée 3012, 75015 Paris, France;
dFunctional Genetics of Infectious Diseases Unit, Department of Genomes and Genetics, Institut Pasteur, 75015 Paris, France;
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Sowath Ly
eEpidemiology and Public Health Unit, Institut Pasteur in Cambodia, International Network of Pasteur Institutes, 12201 Phnom Penh, Cambodia;
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Rath Srey Lay
aVirology Unit, Institut Pasteur in Cambodia, International Network of Pasteur Institutes, 12201 Phnom Penh, Cambodia;
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Kanya C. Long
fDepartment of Entomology and Nematology, University of California, Davis, CA 95616;
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Rekol Huy
gNational Center for Malariology, Ministry of Health, 12302 Phnom Penh, Cambodia;
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Arnaud Tarantola
eEpidemiology and Public Health Unit, Institut Pasteur in Cambodia, International Network of Pasteur Institutes, 12201 Phnom Penh, Cambodia;
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Thomas W. Scott
fDepartment of Entomology and Nematology, University of California, Davis, CA 95616;
hFogarty International Center, National Institutes of Health, Bethesda, MD 20892;
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Anavaj Sakuntabhai
cCentre National de la Recherche Scientifique, Unité de Recherche Associée 3012, 75015 Paris, France;
dFunctional Genetics of Infectious Diseases Unit, Department of Genomes and Genetics, Institut Pasteur, 75015 Paris, France;
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Philippe Buchy
aVirology Unit, Institut Pasteur in Cambodia, International Network of Pasteur Institutes, 12201 Phnom Penh, Cambodia;
iGlaxoSmithKline, Vaccines Value Health Sciences, Singapore 189720
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  • For correspondence: buchyphilippe@hotmail.com
  1. Edited by Luciano A. Moreira, Centro de Pesquisas René Rachou FIOCRUZ-MG, Belo Horizonte, Brazil, and accepted by the Editorial Board October 7, 2015 (received for review April 25, 2015)

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Significance

Our work provides evidence that people who are infected with dengue virus without developing detectable clinical symptoms or prior to the onset of symptoms are infectious to mosquitoes. At a given level of viremia, symptom-free people were markedly more infectious to mosquitoes than clinically symptomatic patients. Our results fundamentally change the current paradigm for dengue epidemiology and control, based on detection of dengue virus-infected cases with apparent illness.

Abstract

Three-quarters of the estimated 390 million dengue virus (DENV) infections each year are clinically inapparent. People with inapparent dengue virus infections are generally considered dead-end hosts for transmission because they do not reach sufficiently high viremia levels to infect mosquitoes. Here, we show that, despite their lower average level of viremia, asymptomatic people can be infectious to mosquitoes. Moreover, at a given level of viremia, DENV-infected people with no detectable symptoms or before the onset of symptoms are significantly more infectious to mosquitoes than people with symptomatic infections. Because DENV viremic people without clinical symptoms may be exposed to more mosquitoes through their undisrupted daily routines than sick people and represent the bulk of DENV infections, our data indicate that they have the potential to contribute significantly more to virus transmission to mosquitoes than previously recognized.

  • mosquito experimental infection
  • Cambodia
  • Aedes aegypti
  • human-to-mosquito transmission
  • dengue

Footnotes

  • ↵1V.D. and L.L. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: buchyphilippe{at}hotmail.com.
  • Author contributions: V.D., L.L., R.E.P., S.L., K.C.L., R.H., A.T., T.W.S., A.S., and P.B. designed research; V.D., S.L., R.S.L., R.H., A.T., and P.B. performed research; V.D., L.L., R.E.P., R.S.L., T.W.S., A.S., and P.B. analyzed data; and V.D., L.L., R.E.P., R.S.L., T.W.S., A.S., and P.B. wrote the paper.

  • Conflict of interest statement: P.B. is currently an employee of GlaxoSmithKline Vaccines, but the research presented does not have any relation with his current position.

  • This article is a PNAS Direct Submission. L.A.M. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1508114112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Dengue transmission from asymptomatic individuals
Veasna Duong, Louis Lambrechts, Richard E. Paul, Sowath Ly, Rath Srey Lay, Kanya C. Long, Rekol Huy, Arnaud Tarantola, Thomas W. Scott, Anavaj Sakuntabhai, Philippe Buchy
Proceedings of the National Academy of Sciences Nov 2015, 112 (47) 14688-14693; DOI: 10.1073/pnas.1508114112

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Dengue transmission from asymptomatic individuals
Veasna Duong, Louis Lambrechts, Richard E. Paul, Sowath Ly, Rath Srey Lay, Kanya C. Long, Rekol Huy, Arnaud Tarantola, Thomas W. Scott, Anavaj Sakuntabhai, Philippe Buchy
Proceedings of the National Academy of Sciences Nov 2015, 112 (47) 14688-14693; DOI: 10.1073/pnas.1508114112
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