Nipah virus dynamics in bats and implications for spillover to humans

Jonathan H. Epstein; Simon J. Anthony; Ariful Islam; A. Marm Kilpatrick; Shahneaz Ali Khan; Maria D. Balkey; Noam Ross; Ina Smith; Carlos Zambrana-Torrelio; Yun Tao; Ausraful Islam; Phenix Lan Quan; Kevin J. Olival; M. Salah Uddin Khan; Emily S. Gurley; M. Jahangir Hossein; Hume E. Field; Mark D. Fielder; Thomas Briese; Mahmudur Rahman; Christopher C. Broder; Gary Crameri; Lin Fa Wang; Stephen P. Luby; W. Ian Lipkin; Peter Daszak

doi:10.1073/pnas.2000429117

Nipah virus dynamics in bats and implications for spillover to humans

Jonathan H. Epstein
, Simon J. Anthony
, Ariful Islam
, A. Marm Kilpatrick
, Shahneaz Ali Khan
, Maria D. Balkey
, Noam Ross
, Ina Smith
, Carlos Zambrana-Torrelio
, Yun Tao
, Ausraful Islam
, Phenix Lan Quan
, Kevin J. Olival
, M. Salah Uddin Khan
, Emily S. Gurley
, M. Jahangir Hossein
, Hume E. Field
, Mark D. Fielder
, Thomas Briese
, Mahmudur Rahman

Christopher C. Broder, Gary Crameri, Lin Fa Wang, Stephen P. Luby, W. Ian Lipkin, Peter Daszak

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Abstract

Nipah virus (NiV) is an emerging bat-borne zoonotic virus that causes near-annual outbreaks of fatal encephalitis in South Asia-one of the most populous regions on Earth. In Bangladesh, infection occurs when people drink date-palm sap contaminated with bat excreta. Outbreaks are sporadic, and the influence of viral dynamics in bats on their temporal and spatial distribution is poorly understood. We analyzed data on host ecology, molecular epidemiology, serological dynamics, and viral genetics to characterize spatiotemporal patterns of NiV dynamics in its wildlife reservoir, bats, in Bangladesh. We found that NiV transmission occurred throughout the country and throughout the year. Model results indicated that local transmission dynamics were modulated by density-dependent transmission, acquired immunity that is lost over time, and recrudescence. Increased transmission followed multiyear periods of declining seroprevalence due to bat-population turnover and individual loss of humoral immunity. Individual bats had smaller host ranges than other species (spp.), although movement data and the discovery of a Malaysia-clade NiV strain in eastern Bangladesh suggest connectivity with bats east of Bangladesh. These data suggest that discrete multiannual local epizootics in bat populations contribute to the sporadic nature of NiV outbreaks in South Asia. At the same time, the broad spatial and temporal extent of NiV transmission, including the recent outbreak in Kerala, India, highlights the continued risk of spillover to humans wherever they may interact with pteropid bats and the importance of limiting opportunities for spillover throughout 's range. [Abstract copyright: Copyright © 2020 the Author(s). Published by PNAS.]

Original language	English
Pages (from-to)	29190-29201
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Issue number	46
Early online date	2 Nov 2020
DOIs	https://doi.org/10.1073/pnas.2000429117
Publication status	Published - 17 Nov 2020

Bibliographical note

Impact: This study was funded by NIH National Institute of Allergy and Infectious Diseases (NIAID) Awards AI067549 and U01AI153420 (to J.H.E.) and AI054715 (to C.C.B.); NIH Fogarty International Center Ecology and Evolution of Infectious Diseases (EEID) Award R01 TW005869 (to P.D.); NSF-NIH EEID Award EF-0914866 (to A.M.K.); NIH NIAID Award U19 AI109761 (to W.I.L.); US Agency for International Development PEER Award 226 (to M.S.U.K.); and the US Agency for International Development Emerging Pandemic Threats: PREDICT Program (P.D., J.H.E., Ariful Islam, S.J.A., N.R., C.Z.-T., and K.J.O.). The ICDDR,B is also grateful to the Governments of Bangladesh, Canada, Sweden, and the United Kingdom for providing core/unrestricted support.

Keywords

Epidemiology and public health
Nipah virus
Pteropus
bats
disease modeling
henipavirus

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10.1073/pnas.2000429117

Fielder-M-47470-VoRFinal published version, 1.69 MBLicence: CC BY-NC-ND

https://doi.org/10.1073/pnas.2000429117

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Epstein, J. H., Anthony, S. J., Islam, A., Marm Kilpatrick, A., Khan, S. A., Balkey, M. D., Ross, N., Smith, I., Zambrana-Torrelio, C., Tao, Y., Islam, A., Quan, P. L., Olival, K. J., Salah Uddin Khan, M., Gurley, E. S., Jahangir Hossein, M., Field, H. E., Fielder, M. D., Briese, T., ... Daszak, P. (2020). Nipah virus dynamics in bats and implications for spillover to humans. Proceedings of the National Academy of Sciences of the United States of America, 117(46), 29190-29201. https://doi.org/10.1073/pnas.2000429117

@article{a5dee1a07be24e468532efc4794b28d7,

title = "Nipah virus dynamics in bats and implications for spillover to humans",

abstract = "Nipah virus (NiV) is an emerging bat-borne zoonotic virus that causes near-annual outbreaks of fatal encephalitis in South Asia-one of the most populous regions on Earth. In Bangladesh, infection occurs when people drink date-palm sap contaminated with bat excreta. Outbreaks are sporadic, and the influence of viral dynamics in bats on their temporal and spatial distribution is poorly understood. We analyzed data on host ecology, molecular epidemiology, serological dynamics, and viral genetics to characterize spatiotemporal patterns of NiV dynamics in its wildlife reservoir, bats, in Bangladesh. We found that NiV transmission occurred throughout the country and throughout the year. Model results indicated that local transmission dynamics were modulated by density-dependent transmission, acquired immunity that is lost over time, and recrudescence. Increased transmission followed multiyear periods of declining seroprevalence due to bat-population turnover and individual loss of humoral immunity. Individual bats had smaller host ranges than other species (spp.), although movement data and the discovery of a Malaysia-clade NiV strain in eastern Bangladesh suggest connectivity with bats east of Bangladesh. These data suggest that discrete multiannual local epizootics in bat populations contribute to the sporadic nature of NiV outbreaks in South Asia. At the same time, the broad spatial and temporal extent of NiV transmission, including the recent outbreak in Kerala, India, highlights the continued risk of spillover to humans wherever they may interact with pteropid bats and the importance of limiting opportunities for spillover throughout 's range. [Abstract copyright: Copyright {\textcopyright} 2020 the Author(s). Published by PNAS.]",

keywords = "Epidemiology and public health, Nipah virus, Pteropus, bats, disease modeling, henipavirus",

author = "Epstein, \{Jonathan H.\} and Anthony, \{Simon J.\} and Ariful Islam and \{Marm Kilpatrick\}, A. and Khan, \{Shahneaz Ali\} and Balkey, \{Maria D.\} and Noam Ross and Ina Smith and Carlos Zambrana-Torrelio and Yun Tao and Ausraful Islam and Quan, \{Phenix Lan\} and Olival, \{Kevin J.\} and \{Salah Uddin Khan\}, M. and Gurley, \{Emily S.\} and \{Jahangir Hossein\}, M. and Field, \{Hume E.\} and Fielder, \{Mark D.\} and Thomas Briese and Mahmudur Rahman and Broder, \{Christopher C.\} and Gary Crameri and Wang, \{Lin Fa\} and Luby, \{Stephen P.\} and \{Ian Lipkin\}, W. and Peter Daszak",

note = "Impact: This study was funded by NIH National Institute of Allergy and Infectious Diseases (NIAID) Awards AI067549 and U01AI153420 (to J.H.E.) and AI054715 (to C.C.B.); NIH Fogarty International Center Ecology and Evolution of Infectious Diseases (EEID) Award R01 TW005869 (to P.D.); NSF-NIH EEID Award EF-0914866 (to A.M.K.); NIH NIAID Award U19 AI109761 (to W.I.L.); US Agency for International Development PEER Award 226 (to M.S.U.K.); and the US Agency for International Development Emerging Pandemic Threats: PREDICT Program (P.D., J.H.E., Ariful Islam, S.J.A., N.R., C.Z.-T., and K.J.O.). The ICDDR,B is also grateful to the Governments of Bangladesh, Canada, Sweden, and the United Kingdom for providing core/unrestricted support.",

year = "2020",

month = nov,

day = "17",

doi = "10.1073/pnas.2000429117",

language = "English",

volume = "117",

pages = "29190--29201",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Epstein, JH, Anthony, SJ, Islam, A, Marm Kilpatrick, A, Khan, SA, Balkey, MD, Ross, N, Smith, I, Zambrana-Torrelio, C, Tao, Y, Islam, A, Quan, PL, Olival, KJ, Salah Uddin Khan, M, Gurley, ES, Jahangir Hossein, M, Field, HE, Fielder, MD, Briese, T, Rahman, M, Broder, CC, Crameri, G, Wang, LF, Luby, SP, Ian Lipkin, W & Daszak, P 2020, 'Nipah virus dynamics in bats and implications for spillover to humans', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, no. 46, pp. 29190-29201. https://doi.org/10.1073/pnas.2000429117

TY - JOUR

T1 - Nipah virus dynamics in bats and implications for spillover to humans

AU - Epstein, Jonathan H.

AU - Anthony, Simon J.

AU - Islam, Ariful

AU - Marm Kilpatrick, A.

AU - Khan, Shahneaz Ali

AU - Balkey, Maria D.

AU - Ross, Noam

AU - Smith, Ina

AU - Zambrana-Torrelio, Carlos

AU - Tao, Yun

AU - Islam, Ausraful

AU - Quan, Phenix Lan

AU - Olival, Kevin J.

AU - Salah Uddin Khan, M.

AU - Gurley, Emily S.

AU - Jahangir Hossein, M.

AU - Field, Hume E.

AU - Fielder, Mark D.

AU - Briese, Thomas

AU - Rahman, Mahmudur

AU - Broder, Christopher C.

AU - Crameri, Gary

AU - Wang, Lin Fa

AU - Luby, Stephen P.

AU - Ian Lipkin, W.

AU - Daszak, Peter

N1 - Impact: This study was funded by NIH National Institute of Allergy and Infectious Diseases (NIAID) Awards AI067549 and U01AI153420 (to J.H.E.) and AI054715 (to C.C.B.); NIH Fogarty International Center Ecology and Evolution of Infectious Diseases (EEID) Award R01 TW005869 (to P.D.); NSF-NIH EEID Award EF-0914866 (to A.M.K.); NIH NIAID Award U19 AI109761 (to W.I.L.); US Agency for International Development PEER Award 226 (to M.S.U.K.); and the US Agency for International Development Emerging Pandemic Threats: PREDICT Program (P.D., J.H.E., Ariful Islam, S.J.A., N.R., C.Z.-T., and K.J.O.). The ICDDR,B is also grateful to the Governments of Bangladesh, Canada, Sweden, and the United Kingdom for providing core/unrestricted support.

PY - 2020/11/17

Y1 - 2020/11/17

N2 - Nipah virus (NiV) is an emerging bat-borne zoonotic virus that causes near-annual outbreaks of fatal encephalitis in South Asia-one of the most populous regions on Earth. In Bangladesh, infection occurs when people drink date-palm sap contaminated with bat excreta. Outbreaks are sporadic, and the influence of viral dynamics in bats on their temporal and spatial distribution is poorly understood. We analyzed data on host ecology, molecular epidemiology, serological dynamics, and viral genetics to characterize spatiotemporal patterns of NiV dynamics in its wildlife reservoir, bats, in Bangladesh. We found that NiV transmission occurred throughout the country and throughout the year. Model results indicated that local transmission dynamics were modulated by density-dependent transmission, acquired immunity that is lost over time, and recrudescence. Increased transmission followed multiyear periods of declining seroprevalence due to bat-population turnover and individual loss of humoral immunity. Individual bats had smaller host ranges than other species (spp.), although movement data and the discovery of a Malaysia-clade NiV strain in eastern Bangladesh suggest connectivity with bats east of Bangladesh. These data suggest that discrete multiannual local epizootics in bat populations contribute to the sporadic nature of NiV outbreaks in South Asia. At the same time, the broad spatial and temporal extent of NiV transmission, including the recent outbreak in Kerala, India, highlights the continued risk of spillover to humans wherever they may interact with pteropid bats and the importance of limiting opportunities for spillover throughout 's range. [Abstract copyright: Copyright © 2020 the Author(s). Published by PNAS.]

AB - Nipah virus (NiV) is an emerging bat-borne zoonotic virus that causes near-annual outbreaks of fatal encephalitis in South Asia-one of the most populous regions on Earth. In Bangladesh, infection occurs when people drink date-palm sap contaminated with bat excreta. Outbreaks are sporadic, and the influence of viral dynamics in bats on their temporal and spatial distribution is poorly understood. We analyzed data on host ecology, molecular epidemiology, serological dynamics, and viral genetics to characterize spatiotemporal patterns of NiV dynamics in its wildlife reservoir, bats, in Bangladesh. We found that NiV transmission occurred throughout the country and throughout the year. Model results indicated that local transmission dynamics were modulated by density-dependent transmission, acquired immunity that is lost over time, and recrudescence. Increased transmission followed multiyear periods of declining seroprevalence due to bat-population turnover and individual loss of humoral immunity. Individual bats had smaller host ranges than other species (spp.), although movement data and the discovery of a Malaysia-clade NiV strain in eastern Bangladesh suggest connectivity with bats east of Bangladesh. These data suggest that discrete multiannual local epizootics in bat populations contribute to the sporadic nature of NiV outbreaks in South Asia. At the same time, the broad spatial and temporal extent of NiV transmission, including the recent outbreak in Kerala, India, highlights the continued risk of spillover to humans wherever they may interact with pteropid bats and the importance of limiting opportunities for spillover throughout 's range. [Abstract copyright: Copyright © 2020 the Author(s). Published by PNAS.]

KW - Epidemiology and public health

KW - Nipah virus

KW - Pteropus

KW - bats

KW - disease modeling

KW - henipavirus

U2 - 10.1073/pnas.2000429117

DO - 10.1073/pnas.2000429117

M3 - Article

SN - 0027-8424

VL - 117

SP - 29190

EP - 29201

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 46

ER -

Nipah virus dynamics in bats and implications for spillover to humans

Abstract

Bibliographical note

Keywords

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