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Home arrow Environment arrow Bats in the Anthropocene: Conservation of Bats in a Changing World


The most notable viruses from the Paramyxoviridae family in bats are those of the genus Henipavirus, which are the subject of many reviews (e.g. Halpin and Rota 2015; Smith and Wang 2013, Luby and Gurley 2012; Clayton et al. 2013; Middleton and Weingartl 2012; Field and Kung 2011). The first recognised henipavirus, Hendra virus (HeV), was first detected during an outbreak of infectious respiratory disease in horses and then humans in Hendra, Australia, in 1994 (Murray et al. 1995). Ultimately, 13 of 20 infected horses died or were euthanised, and of two humans working closely with horses who became infected, one died from acute pneumonia (Murray et al. 1995; Plowright et al. 2015). This spillover was preceded a month earlier by another involving two horses and one human over 800 km away in Mackay, but which went unrecognised until 1995 (Rogers et al. 1996; O'Sullivan et al. 1997). An initial serological survey of 46 wildlife species (excluding bats) failed to identify a reservoir host; however, serological evidence of HeV infection was later identified in all four species of flying foxes native to Australia (Young et al. 1996). Virus isolation (Halpin et al. 2000) and experimental studies (Halpin et al. 2011) have confirmed pteropodid bats as reservoir hosts for henipaviruses (with a lack of clinical signs), with evidence that black (P. alecto) and spectacled flying foxes (P. conspicillatus) are the main reservoir species for HeV (Smith et al. 2014; Goldspink et al. 2015).

Because HeV is frequently detected in the urine of wild flying foxes (Smith et al. 2014), the predominant transmission route to horses is likely via material recently contaminated with bat urine (e.g. pastures) or via direct transmission (Martin et al. 2015). Recognised spillover events from bats to horses occurred sporadically from 1994 to 2004 and annually since 2006, with five spillover events resulting in ongoing transmission to humans in close contact with horses (a total of seven human cases and four deaths; Field et al. 2010). Spillover events are spatiotemporally clustered, occurring year-round in the northern tropics, but seasonally clustered in winter with a peak in July in subtropical regions (Plowright et al. 2015).

The relative importance of various hypothesised drivers of HeV dynamics in bats and subsequent spillover to horses is still unclear (Plowright et al. 2015).

Nipah virus (NiV), the second henipavirus to be recognised, was first isolated in 1999 from pigs and encephalitic pig workers in Malaysia (Center of Disease Control and Prevention 1999). NiV spillover has not been observed since this time in Malaysia; however, annual seasonal outbreaks with high case fatality (average 73 %) have occurred in people in Bangladesh since 2001 (Hsu et al. 2004; Luby et al. 2009; Luby and Gurley 2012), with occasional spillover also occurring in neighbouring India (Chadha et al. 2006; Harit et al. 2006). Due to the close relatedness of HeV and NiV, fruit bats were targeted, and serological evidence quickly identified them to be the natural reservoir of NiV (Enserink 2000; Yob et al. 2001). This was subsequently supported by isolation of NiV from the urine of P. hypomelanus (Chua et al. 2002a), P. vampyrus (Rahman et al. 2010) and P. lylei (Reynes et al. 2005), and seroconversion in the absence of clinical signs following experimental infections in P. vampyrus (Halpin et al. 2011). Antibodies against NiV and NiV-related viruses have now been detected in a variety of bat species (including non-pteropid bats) across a wide geographical area (summarised in Breed et al. 2013). NiV transmission to humans appears to occur via a wider variety of routes compared with HeV. Infection of domestic animal intermediate hosts (via consumption of salivaor urinecontaminated partially eaten fruits or raw date palm sap) has been implicated as a source of human infections in both Malaysia and Bangladesh (Chua et al. 2002b; Chowdhury et al. 2014). In Malaysia, human infections resulted from direct contacts with infected pigs (Chua et al. 1999; Paton et al. 1999; Parashar et al. 2000), whereas in Bangladesh, transmission to humans regularly occurs via consumption of contaminated date palm sap (Luby et al. 2006; Rahman et al. 2012) or directly from human to human (e.g. via nursing sick individuals or preparation for burial; Hughes et al. 2009). The risk of direct human infection with NiV from bats is considered to be lower than horizontal transmission once the virus enters the human population (Gurley et al. 2007; Luby et al. 2009; Chong et al. 2003).

A third henipavirus, Cedar Virus (Marsh et al. 2012), has been isolated from urine collected under a mixed P. alecto/P. scapulatus roost in Australia. In contrast to HeV and NiV, however, it appears to be of low pathogenicity and failed to induce clinical signs in experimentally infected laboratory animal species (Marsh et al. 2012). Serological evidence from South-East Asia and Australasia (Breed et al. 2013) and the wide diversity of paramyxovirus sequences detected in Australia (Vidgen et al. 2015) suggest more henipaviruses are yet to be found. Additionally, although henipaviruses were long thought to be restricted to Asia and Australia, antibodies cross-reactive to HeV and NiV were detected in Madagascar in 2007, suggesting a potentially wider geographical distribution of henipa-related paramyxoviruses (Iehlé et al. 2007). This was supported by serological findings and molecular detection of henipaor henipa-like viruses in mainland Africa and its offshore islands (Hayman et al. 2008, 2012; Peel et al. 2010, 2013; Drexler et al. 2012). Indeed, a recent serological study indicates that these viruses are also occasionally transmitted to humans in Africa (Pernet et al. 2014), though no African henipavirus has been isolated to date.

Viruses from the paramyxovirus genus Rubulavirus (a genus which includes the human mumps virus) have also been frequently detected in bats (Barr et al. 2015). Menangle virus was isolated from pigs following the birth of unusually high numbers of stillborn and deformed piglets in Australia (Philbey et al. 1998). Two piggery personnel had neutralising antibodies against Menangle virus after having recovered from an unexplained febrile illness (Philbey et al. 1998). Flying fox colonies roosting in close proximity to the piggeries were a suspected source of infection for pigs, with subsequent transmission to humans (Philbey et al. 1998). This was supported by serological evidence from P. poliocephalus, P. alecto and P. conspicillatus, and recent virus isolation from P. alecto (Barr et al. 2012). Other isolated bat rubulaviruses with unknown or limited understanding of their zoonotic potential include Tioman virus from Malaysia (Chua et al. 2001), Tuhokovirus 1, 2 and 3 from China (Lau et al. 2010), Achimota virus 1 and 2 from Ghana (Baker et al. 2013c) and Hervey, Grove, Teviot and Yeppoon paramyxoviruses from Australia (Barr et al. 2015). Neutralising antibodies to Tioman virus and Achimota viruses have been detected in humans, suggesting previous exposure and infection with the virus (Yaiw et al. 2007; Baker et al. 2013c). Pigs experimentally infected with Tioman virus produced neutralising antibodies and excreted virus in saliva, but were either asymptomatic or developed only a fever (Yaiw et al. 2008). Undetected infection in pigs could therefore facilitate transmission to humans.

Finally, viral fragments related to rubulaviruses and the proposed genus Jeilongvirus have also been detected outside the range of fruit bats, in European insectivorous bat species (Kurth et al. 2012). However, nothing is yet known about the relevance of these viruses as potentially zoonotic threats to humans.

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