Unraveling the Transmission Ecology of Polio

PLoS Biology, Jun 2015

Sustained and coordinated vaccination efforts have brought polio eradication within reach. Anticipating the eradication of wild poliovirus (WPV) and the subsequent challenges in preventing its re-emergence, we look to the past to identify why polio rose to epidemic levels in the mid-20th century, and how WPV persisted over large geographic scales. We analyzed an extensive epidemiological dataset, spanning the 1930s to the 1950s and spatially replicated across each state in the United States, to glean insight into the drivers of polio’s historical expansion and the ecological mode of its persistence prior to vaccine introduction. We document a latitudinal gradient in polio’s seasonality. Additionally, we fitted and validated mechanistic transmission models to data from each US state independently. The fitted models revealed that: (1) polio persistence was the product of a dynamic mosaic of source and sink populations; (2) geographic heterogeneity of seasonal transmission conditions account for the latitudinal structure of polio epidemics; (3) contrary to the prevailing “disease of development” hypothesis, our analyses demonstrate that polio’s historical expansion was straightforwardly explained by demographic trends rather than improvements in sanitation and hygiene; and (4) the absence of clinical disease is not a reliable indicator of polio transmission, because widespread polio transmission was likely in the multiyear absence of clinical disease. As the world edges closer to global polio eradication and continues the strategic withdrawal of the Oral Polio Vaccine (OPV), the regular identification of, and rapid response to, these silent chains of transmission is of the utmost importance.

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Unraveling the Transmission Ecology of Polio

June Unraveling the Transmission Ecology of Polio Micaela Martinez-Bakker 0 1 2 Aaron A. King 0 1 2 Pejman Rohani 0 1 2 0 1 Department of Ecology & Evolutionary Biology, University of Michigan , Ann Arbor , Michigan, United States of America, 2 Center for the Study of Complex Systems, University of Michigan , Ann Arbor , Michigan, United States of America, 3 Fogarty International Center, National Institutes of Health , Bethesda, Maryland , United States of America 1 Funding: MMB is supported by the NSF Graduate Research Fellowship Program and the University of Michigan Rackham Merit Fellowship. PR and AAK are supported by the Research and Policy in Infectious Disease Dynamics program of the Science and Technology Directorate, Department of Homeland Security, the Fogarty International Center, National Institutes of Health and by MIDAS, National Institute of General Medical Sciences U54-GM111274 and U01-GM110744. This research was supported in part through computational resources and services provided by Advanced Research Computing at the 2 Academic Editor: Andrew Fraser Read, The Pennsylvania State University , UNITED STATES Sustained and coordinated vaccination efforts have brought polio eradication within reach. Anticipating the eradication of wild poliovirus (WPV) and the subsequent challenges in preventing its re-emergence, we look to the past to identify why polio rose to epidemic levels in the mid-20th century, and how WPV persisted over large geographic scales. We analyzed an extensive epidemiological dataset, spanning the 1930s to the 1950s and spatially replicated across each state in the United States, to glean insight into the drivers of polio's historical expansion and the ecological mode of its persistence prior to vaccine introduction. We document a latitudinal gradient in polio's seasonality. Additionally, we fitted and validated mechanistic transmission models to data from each US state independently. The fitted models revealed that: (1) polio persistence was the product of a dynamic mosaic of source and sink populations; (2) geographic heterogeneity of seasonal transmission conditions account for the latitudinal structure of polio epidemics; (3) contrary to the prevailing “disease of development” hypothesis, our analyses demonstrate that polio's historical expansion was straightforwardly explained by demographic trends rather than improvements in sanitation and hygiene; and (4) the absence of clinical disease is not a reliable indicator of polio transmission, because widespread polio transmission was likely in the multiyear absence of clinical disease. As the world edges closer to global polio eradication and continues the strategic withdrawal of the Oral Polio Vaccine (OPV), the regular identification of, and rapid response to, these silent chains of transmission is of the utmost importance. - Data Availability Statement: All relevant data are within the paper and its Supporting Information files. University of Michigan, Ann Arbor; and by UAF Life Science Informatics. UAF Life Science Informatics as a core research resource is supported by Grant Number RR016466 from the National Center for Research Resources, a component of the National Institutes of Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Abbreviations: AFP, acute flaccid paralysis; CDC, Centers for Disease Control and Prevention; GPEI, Global Polio Eradication Initiative; IPV, Inactivated polio vaccine; MLE, maximum likelihood estimate; NSF, National Science Foundation; OPV, oral polio vaccine; RSV, Respiratory Syncytial Virus; WPV, wild poliovirus. mathematical models to track poliovirus and to reconstruct the millions of unobserved subclinical infections that propagated the disease. We identified why polio epidemics are explosive and seasonal, and why they vary geographically. Our analyses show that the historical expansion of polio is straightforwardly explained by the demographic “baby boom” during the postwar period rather than improvements in hygiene. We were also able to demonstrate that poliovirus persisted primarily through symptomless individuals, and that in the event of local virus extinction, infection was reintroduced from other geographic locations. Poliovirus, like other members of Picornaviridae, usually generates mildly symptomatic infection. However, the clinical manifestation of polio, Acute Flaccid Paralysis (AFP), can result when the virus invades the central nervous system [1]. Wild poliovirus (WPV) is transmitted fecal–orally and in the Northern Hemisphere exhibits seasonal epidemics in late summer and autumn [1–3]. Polio outbreaks continue today within this narrow seasonal window in Pakistan and Afghanistan [4,5], but the seasonal transmission structure of polio remains unexplored. Propelled by public support, the race for the polio v (...truncated)


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Micaela Martinez-Bakker, Aaron A. King, Pejman Rohani. Unraveling the Transmission Ecology of Polio, PLoS Biology, 2015, Volume 13, Issue 6, DOI: 10.1371/journal.pbio.1002172