Nipah virus dynamics in bats and implications for spillover to humans.

Jonathan H Epstein1,2 Simon J Anthony3 Ariful Islam4 A Marm Kilpatrick5 Shahneaz Ali Khan4,6 Maria D Balkey3,7 Noam Ross4 Ina Smith8 Carlos Zambrana-Torrelio4 Yun Tao4 Ausraful Islam9 Phenix Lan Quan3 Kevin J Olival4 M Salah Uddin Khan9 Emily S Gurley9,10 M Jahangir Hossein11 Hume E Field4 Mark D Fielder12 Thomas Briese3 Mahmudur Rahman13 Christopher C Broder14 Gary Crameri8 Lin-Fa Wang15 Stephen P Luby9,16 W Ian Lipkin3 Peter Daszak4
Affiliations 16 institutions
  1. EcoHealth Alliance, New York, NY 10018
  2. [email protected].
  3. Center for Infection and Immunity, Columbia University, New York, NY 10032.
  4. EcoHealth Alliance, New York, NY 10018.
  5. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064.
  6. Chattogram Veterinary and Animal Sciences University, Chattogram, Khulshi 4225, Bangladesh.
  7. Center for Food Safety & Applied Nutrition, U.S. Food & Drug Administration, College Park, MD 20740.
  8. CSIRO Australian Animal Health Laboratory, Commonwealth Scientific and Industrial Research Organisation, Geelong, VIC 3219, Australia.
  9. International Centre for Diarrhoeal Diseases Research, Bangladesh, Dhaka 1212, Bangladesh.
  10. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205.
  11. Medical Research Council Unit The Gambia, London School of Hygiene and Tropical Medicine, Banjul, The Gambia.
  12. School of Life Sciences, Science, Engineering and Computing Faculty, Kingston University, London KT1 2EE, United Kingdom.
  13. Institute of Epidemiology, Disease Control, and Research, Government of Bangladesh, Dhaka 1212, Bangladesh.
  14. Department of Microbiology and Immunology, Uniformed Services University, Bethesda, MD 20814.
  15. Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore 169857.
  16. Department of Infectious Diseases & Geographic Medicine, Stanford University, Stanford, CA 94305.

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, Pteropus medius 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 Pteropus 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 Pteropus's range.

Supporting text Virus Host Location
bats 46 disease modeling 1 henipavirus 30 Nipah virus 55 Pteropus 7 Animals 1948 Asia 13 Bangladesh 25 Chiroptera 371 Disease Outbreaks 170 Female 289 Henipavirus Infections 65 Host Specificity 132 Humans 1440 Immunity 1 Male 224 Models, Biological 16 Molecular Epidemiology 21 Nipah Virus 45 Phylogeny 805 Zoonoses 397

Evidence records

5 total
Zoonotic Surveillance
3 records · 2 evidence types
Evidence type
1 records
OVE4240
Key finding

Nipah virus seroprevalence in bat populations declined over several years due to population turnover and loss of humoral immunity, preceding periods of increased viral transmission.

Virus
Host
Location
Not specified
Supporting text

Increased transmission followed multiyear periods of declining seroprevalence due to bat-population turnover and individual loss of humoral immunity.

Method
serological analysis | antibody detection
Sample type
serum (antibody testing)
Evidence type
2 records
OVE4238
Key finding

Nipah virus circulated year-round across Bangladesh within Pteropus medius bats, supporting continuous reservoir transmission.

Virus
Host
Location
Supporting text

We analyzed data on host ecology, molecular epidemiology, serological dynamics, and viral genetics to characterize spatiotemporal patterns of NiV dynamics in its wildlife reservoir, Pteropus medius bats, in Bangladesh. We found that NiV transmission occurred throughout the country and throughout the year.

Method
analysis of spatiotemporal transmission patterns | molecular epidemiology | serological dynamics modeling
Geographic raw
Bangladesh
Country inferred
BGD
OVE4239
Key finding

Multiannual local epizootics in bat populations were linked to sporadic Nipah virus outbreaks in South Asia, suggesting periodic reservoir cycles.

Virus
Host
Location
Supporting text

These data suggest that discrete multiannual local epizootics in bat populations contribute to the sporadic nature of NiV outbreaks in South Asia.

Method
modeling of bat-population transmission cycles | longitudinal serological and viral dynamics analysis
Geographic raw
South Asia
Transmission Evidence
1 records · 1 evidence types
Evidence type
1 records
OVE4237
Key finding

Nipah virus spillover to humans occurs in Bangladesh when people drink date-palm sap contaminated with bat excreta.

Virus
Host
Location
Supporting text

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.

Method
epidemiological association between human cases and bat contamination of sap
Study design
epidemiological observation
Transmission direction
animal-to-human
Geographic raw
Bangladesh
Country inferred
BGD
Genomic Evolution
1 records · 1 evidence types
Evidence type
1 records
OVE4241
Key finding

Phylogenetic identification of a Malaysia-clade Nipah virus strain in eastern Bangladesh indicates genetic connectivity between bat populations of Bangladesh and Malaysia.

Virus
Host
Location
Not specified
Supporting text

Movement data and the discovery of a Malaysia-clade NiV strain in eastern Bangladesh suggest connectivity with bats east of Bangladesh.

Analysis methods
phylogenetic analysis