Henipavirus susceptibility to environmental variables
Introduction
Hendra virus (HeV) and Nipah virus (NiV), currently the sole members of the genus Henipavirus, family Paramyxoviridae, are recently emerged zoonotic viruses causing encephalitic and respiratory illness in humans and livestock. Fruit bats of the genus Pteropus are the probable wildlife reservoir for both viruses. HeV is restricted to Australia and of the seven outbreaks to date all have involved infection of horses from unidentified sources, with subsequent direct transmission to humans on three occasions (Hanna et al., 2006, Hooper et al., 1996, Murray et al., 1995a). NiV outbreaks have occurred in Malaysia, Singapore, India and Bangladesh following various chains of transmission including intermediate host species (Chua et al., 2000), human-to-human transmission (ICDDRB, 2004b), possible bat-to-human transmission (Hsu et al., 2004) and vehicle-borne transmission (Luby et al., 2006).
In most cases, the route of transmission from bats to subsequent hosts has not been identified. The most likely route of HeV transmission to horses is through the ingestion of grass or partially eaten fruit contaminated with bat urine, saliva or other fluids. The coincidence of HeV outbreaks with birthing seasons of Australian fruit bat species (Field et al., 2001) and the isolation of HeV from the uterine fluid and aborted foetus of a wild grey-headed fruit bat (P. poliocephalus (Halpin et al., 2000)) indicate that this may be a significant route of HeV infection for horses. We have recently demonstrated vertical transmission of NiV in experimentally infected cats further supporting this route as potentially an important natural route of transmission (Mungall et al., 2007).
Two NiV outbreaks show a reasonably clear chain of transmission from bats to humans: Malaysia in 1998–99 and Tangail, Bangladesh in 2005. During the Malaysian outbreak, 265 people were infected, primarily through contact with infected pigs (Parashar et al., 2000). The pigs were probably infected by P. vampyrus bats that fed on fruit trees adjacent to the pig farms, either through direct exposure to urine or via saliva-contaminated partially eaten fruit dropped into the pigsties (Chua et al., 2002). In the Tangail outbreak, NiV transmission to humans apparently occurred via date palm sap (ICDDRB, 2005, Luby et al., 2006). The sap may have been contaminated by urine, faeces or saliva from P. giganteus which are known to feed on the sap during harvesting.
Little is known about the transmission routes for the remaining NiV outbreaks, although preliminary analysis of the 2007 outbreaks (Kushtia, Bangladesh and Nadia, India) suggests likely human to human transmission (S. Luby, personal communication). The absence of identifiable intermediate hosts may be evidence of bat-to-human transmission. In at least three outbreaks human-to-human transmission is likely to have occurred (Chadha et al., 2006, Gurley et al., 2007, ICDDRB, 2003, ICDDRB, 2004a); however, the mode of transmission is uncertain.
A greater understanding of potential henipavirus modes of transmission may clarify the events that lead to viral spillover into new species and assist in controlling or averting outbreaks. Knowledge of virus survival in the environment is also critical in controlling human-to-human and nosocomial transmission.
The purpose of this study was to define the ability of henipaviruses to survive under a range of environmental conditions and thereby gain an understanding of the likely mechanisms of viral transmission between hosts. While we intended to mimic the natural conditions relevant to bat viral transmission as closely and accurately as possible, certain limitations on fruit selection due to seasonal availability and limitations inherent in the procurement of bat urine and saliva necessitated some generalizations.
Section snippets
Viruses and titrations
HeV was isolated in Vero cells from the lung of a horse infected in the Brisbane outbreak in October 1994 (Murray et al., 1995b) and was passaged five times in Vero cells followed by triple plaque purification and a further five passages in Vero cells (Hyatt and Selleck, 1996). NiV was isolated in Vero cells from the brain of a human fatally infected in the 1998–99 Malaysian outbreak and was passaged three times in Vero cells then double plaque purified and passaged a further three times in
Effect of pH on virus survival
Both HeV and NiV exhibit an extremely broad tolerance to extremes of pH with viable virus recovered after a 60 min incubation in solutions ranging from pH 3 to 11 for NiV and pH 4 to 11 for HeV (Fig. 1).
Effect of desiccation on virus survival
Henipaviruses were rapidly inactivated by desiccation at both 22 and 37 °C. Both viruses survived for less than 15 min at 37 °C (Fig. 2) while HeV decreased by more than 3 logs within 30 min (half-life of 1.2 min) and NiV decreased by more than 2 logs within 60 min (half-life of 1.45 min) at 22 °C.
Discussion
This study demonstrates that survival of henipaviruses in the environment is highly sensitive to temperature and desiccation. Under most conditions survival time was brief, with half-lives limited to a few hours, indicating that transmission to a new host requires close contact with an infected animal or exposure to contaminated material shortly after excretion. However, under optimal conditions henipaviruses can persist for a number of days and under these circumstances, vehicle-borne
Acknowledgements
Financial support: RF, KH, ADH and PD are supported in part by a National Institutes of Health/National Science Foundation “Ecology of Infectious Diseases” (R01-TW05869) award from the John E. Fogarty International Center and by core funding to the Consortium for Conservation Medicine from the V. Kann Rasmussen Foundation.
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