Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus)--implications for disease risk management

Abstract

This study investigated the seroepidemiology of Hendra virus in a spectacled flying-fox (Pteropus conspicillatus) population in northern Australia, near the location of an equine and associated human Hendra virus infection in late 2004. The pattern of infection in the population was investigated using a serial cross-sectional serological study over a 25-month period, with blood sampled from 521 individuals over six sampling sessions. Antibody titres to the virus were determined by virus neutralisation test. In contrast to the expected episodic infection pattern, we observed that seroprevalence gradually increased over the two years suggesting infection was endemic in the population over the study period. Our results suggested age, pregnancy and lactation were significant risk factors for a detectable neutralizing antibody response. Antibody titres were significantly higher in females than males, with the highest titres occurring in pregnant animals. Temporal variation in antibody titres suggests that herd immunity to the virus may wax and wane on a seasonal basis. These findings support an endemic infection pattern of henipaviruses in bat populations suggesting their infection dynamics may differ significantly from the acute, self limiting episodic pattern observed with related viruses (e.g. measles virus, phocine distemper virus, rinderpest virus) hence requiring a much smaller critical host population size to sustain the virus. These findings help inform predictive modelling of henipavirus infection in bat populations, and indicate that the life cycle of the reservoir species should be taken into account when developing risk management strategies for henipaviruses.

Figure 1. Observed (A) and expected (B, C) patterns of HeV seroprevalence through time.

Panel (A) shows observed temporal variation in Pteropus conspicillatus seroprevalence (% ±95 CI) over the period of study. Panel (B) schematically represents a theoretical seroprevalence pattern of endemic or persistent infection transmission dynamics (dotted lines represent 95% CIs). Panel (C) schematically represents a theoretical seroprevalence pattern of an acute, self limiting pathogen; a pattern of seroprevalence that could be seen in a population with episodic infection.

Figure 2. Pteropus conspicillatus HeV seroprevalence (% ±95 CI) across age categories.

The observed seroprevalence pattern of a higher seroprevalence of juveniles (58.3%) than sub-adults (39.9%), and a correspondingly higher seroprevalence in adults (60.3%) suggests predominantly horizontal transmission of virus and that maternal transfer of HeV antibodies to juveniles likely occurs.

Figure 3. Features for classification of age categories of Pteropus conspicillatus used in this study.

Age classification features (highlighted by a red circle in B, C, D, E) for both sexes. Key features include: juvenile bats (A) carried by their mother (estimated age 0 to 3 months old); sub-adult bats (B, C) were free flying that lacked signs of sexual maturity, including the lack of enlarged nipples for females (B) or small or non-descended testes for males (C; estimated age 3 months to 2 years); adults bats (D, E, F) showed signs of sexual maturity, including visibly enlarged nipples indicating a previous pregnancy and suckling of young in females (D) or large and descended testes in males (E), and but did not show signs of severe wear on all molar teeth (F; estimated age 2 to 8 years); aged bats (G) showed signs of severe molar wear on all molar teeth, including at least two molars worn to the level of the gingiva (estimated age 8 years and older).