Risk Factors for Nipah Virus Infection among Pteropid Bats, Peninsular Malaysia

Sohayati A. Rahman, Latiffah Hassan

, Jonathan H. Epstein, Zaini C. Mamat, Aziz M. Yatim, Sharifah S. Hassan, Hume E. Field, Tom Hughes, Justin Westrum, M.S. Naim, Arshad S. Suri, A. Aziz Jamaluddin, Peter Daszak, and the Henipavirus Ecology Research Group

Author affiliations: Author affiliations: Veterinary Research Institute, Ipoh, Malaysia (S.A. Rahman, Z.C. Mamat, A.M. Yatim, M.S. Naim, A.A. Jamaluddin); Universiti Putra Malaysia, Serdang, Malaysia (L. Hassan, A.S. Suri); EcoHealth Alliance, New York, New York, USA (J.H. Epstein, T. Hughes, J. Westrum, P. Daszak); Monash University, Selangor, (S.S. Hassan); Queensland Primary Industries and Fisheries, Brisbane, Queensland, Australia (H.E. Field)

Abstract

We conducted cross-sectional and longitudinal studies to determine the distribution of and risk factors for seropositivity to Nipah virus (NiV) among Pteropus vampyrus and P. hypomelanus bats in Peninsular Malaysia. Neutralizing antibodies against NiV were detected at most locations surveyed. We observed a consistently higher NiV risk (odds ratio 3.9) and seroprevalence (32.8%) for P. vampyrus than P. hypomelanus (11.1%) bats. A 3-year longitudinal study of P. hypomelanus bats indicated nonseasonal temporal variation in seroprevalence, evidence for viral circulation within the study period, and an overall NiV seroprevalence of 9.8%. The seroprevalence fluctuated over the study duration between 1% and 20% and generally decreased during 2004–2006. Adult bats, particularly pregnant, with dependent pup and lactating bats, had a higher prevalence of NiV antibodies than juveniles. Antibodies in juveniles 6 months–2 years of age suggested viral circulation within the study period.

Nipah virus (NiV) disease emerged in Peninsular Malaysia during September 1998–April 1999 and resulted in 105 human deaths (≈40%) and compulsory culling of 1.1 million pigs (1). NiV disease has been successfully controlled in Malaysia. However, elsewhere in Bangladesh and India, 12 NiV outbreaks have since occurred (2). Pteropid bats (family Pteropodidae, genus Pteropus) were the most likely reservoir host of the virus, and evidence of NiV in these bats had been consistently found in populations across southern Asia (3–6) and Africa (7) despite an absence of outbreaks in some areas.
Characteristics of bats that promote their competency as a natural host and reservoir for many emerging pathogens from evolutionary, ecologic, sociobehavioral, and immunologic perspectives are progressively being reported (8–11). In Malaysia, previous surveillance work suggest 2 pteropid species, Pteropus hypomelanus (variable flying fox) and P. vampyrus (large flying fox) bats, as reservoir hosts for NiV (12). P. hypomelanus bats reside on offshore islands along the eastern (n = 14) and western (n = 4) coasts of the peninsula (13). NiV was first isolated from pooled urine samples from these bats on the island of Pulau Tioman off the eastern coast of the state of Pahang (14). P. vampyrus bats, the pteropid species identified during the first NiV disease outbreak location in 1998 (3), are anthropogenic-susceptible bats residing in remote and inaccessible areas such as mangroves and dense forests (15). P. vampyrus bats roost mainly on the mainland but may have focal transitory points on surrounding islands as they travel (16,17).
Our recent follow-up work on a cohort of P. vampyrus bats (18,19) showed a possible NiV recrudescent event leading to horizontal viral transmission to other bats in the colony. The findings further elucidated maintenance and transmission dynamics of the virus within and among roosts, colonies, and the bat metapopulation. In this report, we present results of 2 studies conducted concurrently to determine the geographic extent and prevalence of NiV-neutralizing antibody for P. vampyrus and P. hypomelanus bats, and to identify the sexual and reproductive maturity determinants for NiV seropositivity in the wild.