Differential and enhanced response to climate forcing in diarrheal disease due to rotavirus across a megacity of the developing world

Edited by Burton H. Singer, University of Florida, Gainesville, FL, and approved February 24, 2016 (received for review September 26, 2015)
March 28, 2016
113 (15) 4092-4097

Significance

Rotavirus is the most common cause of diarrhea among infants and children worldwide, and is still responsible for over 400,000 deaths per year, affecting mainly developing countries. This study investigates its transmission dynamics and their response to climate forcing, specifically flooding, in the megacity of Dhaka, Bangladesh, with an extensive surveillance record that spans over two decades and is spatially resolved. With a transmission model informed by these data, we show that consideration of different parts of the city, core and periphery, is critical to uncover important differences in seasonal outbreaks and in the effect of the monsoons. Infectious diseases not typically considered climate-sensitive can become so under demographic and environmental conditions of large urban centers of the developing world.

Abstract

The role of climate forcing in the population dynamics of infectious diseases has typically been revealed via retrospective analyses of incidence records aggregated across space and, in particular, over whole cities. Here, we focus on the transmission dynamics of rotavirus, the main diarrheal disease in infants and young children, within the megacity of Dhaka, Bangladesh. We identify two zones, the densely urbanized core and the more rural periphery, that respond differentially to flooding. Moreover, disease seasonality differs substantially between these regions, spanning variation comparable to the variation from tropical to temperate regions. By combining process-based models with an extensive disease surveillance record, we show that the response to climate forcing is mainly seasonal in the core, where a more endemic transmission resulting from an asymptomatic reservoir facilitates the response to the monsoons. The force of infection in this monsoon peak can be an order of magnitude larger than the force of infection in the more epidemic periphery, which exhibits little or no postmonsoon outbreak in a pattern typical of nearby rural areas. A typically smaller peak during the monsoon season nevertheless shows sensitivity to interannual variability in flooding. High human density in the core is one explanation for enhanced transmission during troughs and an associated seasonal monsoon response in this diarrheal disease, which unlike cholera, has not been widely viewed as climate-sensitive. Spatial demographic, socioeconomic, and environmental heterogeneity can create reservoirs of infection and enhance the sensitivity of disease systems to climate forcing, especially in the populated cities of the developing world.

Acknowledgments

We thank two anonymous referees for their insightful comments. This work was completed in part with resources provided by the University of Chicago Research Computing Center. This research was partially supported by the National Oceanic and Atmospheric Administration (Grant F020704). The case data used in this paper were collected with the support of the ICDDR,B and its donors, who provide unrestricted support to the ICDDR,B for its operation and research. Current donors providing unrestricted support include the Government of the People’s Republic of Bangladesh; the Department of Foreign Affairs, Trade, and Development Canada; the Swedish International Development Cooperation Agency; and the Department for International Development (UK Aid). We thank these donors for their support and commitment to the ICDDR,B’s research efforts. A.A.K. was supported by the Research and Policy in Infectious Disease Dynamics program of the Science and Technology Directorate, US Department of Homeland Security; by the Fogarty International Center, US NIH; and also by research grants from the NIH (Grant 1R01AI101155) and Models of Infectious Disease Agent Study (MIDAS), National Institute of General Medical Sciences (Grant U54-GM111274).

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 113 | No. 15
April 12, 2016
PubMed: 27035949

Classifications

Submission history

Published online: March 28, 2016
Published in issue: April 12, 2016

Keywords

  1. monsoon flooding
  2. diarrheal disease
  3. rotavirus transmission
  4. epidemiological model
  5. urban health

Acknowledgments

We thank two anonymous referees for their insightful comments. This work was completed in part with resources provided by the University of Chicago Research Computing Center. This research was partially supported by the National Oceanic and Atmospheric Administration (Grant F020704). The case data used in this paper were collected with the support of the ICDDR,B and its donors, who provide unrestricted support to the ICDDR,B for its operation and research. Current donors providing unrestricted support include the Government of the People’s Republic of Bangladesh; the Department of Foreign Affairs, Trade, and Development Canada; the Swedish International Development Cooperation Agency; and the Department for International Development (UK Aid). We thank these donors for their support and commitment to the ICDDR,B’s research efforts. A.A.K. was supported by the Research and Policy in Infectious Disease Dynamics program of the Science and Technology Directorate, US Department of Homeland Security; by the Fogarty International Center, US NIH; and also by research grants from the NIH (Grant 1R01AI101155) and Models of Infectious Disease Agent Study (MIDAS), National Institute of General Medical Sciences (Grant U54-GM111274).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Pamela P. Martinez
Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637;
Aaron A. King
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109;
Department of Mathematics, University of Michigan, Ann Arbor, MI 48109;
Mohammad Yunus
International Centre for Diarrheal Disease Research, Dhaka 1000, Bangladesh;
A. S. G. Faruque
International Centre for Diarrheal Disease Research, Dhaka 1000, Bangladesh;
Mercedes Pascual1 [email protected]
Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637;
Santa Fe Institute, Santa Fe, NM 87501

Notes

1
To whom correspondence should be addressed. Email: [email protected].
Author contributions: P.P.M., A.A.K., and M.P. designed research; P.P.M. performed research; P.P.M. analyzed data; P.P.M., A.A.K., M.Y., A.S.G.F., and M.P. wrote the paper; and M.Y. and A.S.G.F. provided data and knowledge on the system.

Competing Interests

The authors declare no conflict of interest.

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    Differential and enhanced response to climate forcing in diarrheal disease due to rotavirus across a megacity of the developing world
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 15
    • pp. 3903-E2208

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