Under the Microscope

Hendra virus – a One Health success story

Hume Field Queensland Centre for Emerging Brad McCall Infectious Diseases 39 Kessels Road, Coopers Plains Brisbane Southside Public Health Unit, Brisbane, Qld 4108, Australia PO Box 333, Archerfield Tel +61 7 3276 6054 Qld 4108, Australia Fax +61 7 3216 6591 Tel +61 7 3000 9148 Email [email protected] Fax +61 7 3000 9130

Zoonoses account for 60% of emerging diseases spp.) as the natural reservoir of the virus in 1996 provided threatening humans. Wildlife are the origin of an the complex wildlife-livestock-human continuum illustrated increasing proportion of zoonoses over recent decades to by Daszak et al., 20005, and thus invited a cross-disciplinary a point where they now account for 75% of all zoonoses1. approach. A succession of equine incidents (some single cases,

Concurrently and/or consequentially, there has been some involving horse to horse transmission) has occurred since an increasing recognition of the inter-connectedness 1994, several involving horse to human transmissions6 (Figure 1). of wildlife, livestock and human health, and increasing In 2012, the response to diagnosis of an equine case invokes momentum of an ecosystem-level approach (most a coordinated multi-agency threat abatement team approach. commonly termed One Health) to complex emerging Animal health authorities report a positive diagnosis to public disease scenarios2. This paper describes the evolution health, wildlife and workplace health and safety authorities. and application of such an approach to periodic Hendra There is cross-agency coordination not only at the policy and virus incidents in horses and humans in Australia. operational level, but also more broadly in communication

Hendra virus, a novel member of the virus family with industry, community and media. However, the current

Paramyxoviridae, was first described in 1994 in the Brisbane unambiguous One Health approach reflects an evolutionary suburb of Hendra. It appeared suddenly and dramatically in a process rather than a proscriptive process, and is in strong

Thoroughbred racing stables in suburban Hendra as an acute contrast to the situation at the time of the first identified Hendra equine respiratory disease outbreak, resulting in the deaths of virus incident in 1994. This evolution is elaborated in Hayman et

13 of 20 infected horses over a 16-day period3. But the al., 20127, and summarised here by way of illustration. subsequent infection of the trainer and the stable-hand, who In early September 1994, a gravely ill horse named Drama had tended the sick and dying horses, caused even greater Series was moved from a spelling paddock to a training stable consternation in both animal health and public health authorities. in the Brisbane suburb of Hendra for veterinary care. This Industry and public alarm was magnified when the trainer action inadvertently precipitated the first recognised and largest succumbed to the infection after a short illness4. Hendra virus outbreak to date. A cascade of horses succumbed

The subsequent identification of species of fruit bats (Pteropus to a highly pathogenic and novel syndrome over the ensuing

MICROBIOLOGY AUSTRALIA • NOVEMBER 2012 167 Under the Microscope

days, culminating in a total 20 equine and two human cases. retrospective investigations would show that the Brisbane

Thirteen References:horses died or were euthanased terminally after outbreak did not mark the first emergence of Hendra virus. A an acute clinical course, a case fatality rate of 65%. Hendra month earlier and 800 kilometres north, two horses in adjoining 1. Jones, K.E. et al. (2008) Global trends in emerging infectious diseases. Nature virus had emerged3,8,9. The outbreak prompted quarantine paddocks on a Thoroughbred stud near Mackay in north 451, 990-993. declarations,2. horse Anonmovement (2010) restrictions, The FAO and the-OIE cancellation-WHO Collaboration.Queensland died A afterTripartite acute illness Concept characterised Note. respectively by of race meetingshttp://web.oie.int/downld/FINAL_CONCEPT_NOTE_Hanoi.pdf in south-east Queensland as investigation of respiratory and neurological symptoms3. The veterinarian owner, 3. Baldock, F.C. et al. (1996) Epidemiological investigations into the 1994 the aetiology proceeded. Within a week, both the Queensland assisted by her husband, performed necropsies on both horses. Equine Morbillivirus outbreaks in Queensland, Australia. Singapore Veterinary J. 20, Animal Research57-61. Institute and the CSIRO Australian Animal The husband became ill shortly after, and was diagnosed with a 10 Health Laboratory4. Selvey,had isolated L.A. a virus, et initiallyal. (1995) named Infectionequine mildof meningo-encephalitis.humans and horses After bya short a illness,newly he recovered . described morbillivirus. Med. J. Aust. 162, 642-645. morbillivirus, and subsequently renamed Hendra virus8. The following year, he developed severe encephalitis which 5. Daszak, P. et al. (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287, 443resulted-448. in his hospitalisation and subsequent death, 14 months Within a week of Drama Series' death, both the trainer and a 6. Mahalingam, S. et al. (2012) Hendra aftervirus: assisting an emergingwith the horse paramyxovirus necropsies11. Matching in Hendra virus stable-hand became ill, presenting with an influenza-like illness. Australia. The Lancet 12 (epub ahead of print). genome sequence was subsequently detected in the human and The trainer,7. in particular,Hayman, had directD.T. and et repeatedal. (2012) contact The with development of One Health approaches in (archived) horse samples. henipavirus research. Curr. Top. Microbiol. Immunol. (in press). oro-nasal secretions as he endeavoured to force-feed by hand the 8. Murray, K. et al. (1995) A Morbillivirus that caused fatal disease in horses and While the outbreak in Brisbane required significant professional gravely ill humans.horse. The Science stable-hand 268 recovered, 94-97. with symptomatic interaction between public health and animal health authorities, treatment,9. but theDouglas, trainer’s conditionI.C. et al.deteriorated. (1997) OutbreakAs the investigation of an emerging disease (Equine Morbillivirus). In Epidemiologie et Santeit was arguablyAnimale the Proceedings "reinforcement" of provided the 8th by the Mackay equine outbreakISVEE peakedconference at his stables,, 04.08.01 the trainer-04.08.03, was in an International society for veterinary incident that marked the beginning of an enduring change intensive careepidemiology unit. The differential and economics diagnoses were. legionnaire’s in the relationship between animal health and public health disease, viral10. pneumonitis,Allworth, melioidosis A. et al.or glanders,(1995) Equineand toxic morbillivirus in Queensland. Comm. Dis. Intell. 19, 575. authorities. Both continued to operate as discrete agencies, but pneumonitis4. The trainer subsequently died; Hendra virus was 11. Osullivan, J.D. et al. (1997) Fatal encephalitiscommunication due and to collaborationnovel paramyxovirus increasingly occurred at the isolated fromtransmitted kidney tissue. from horses. Lancet 349, 93-95. 12. Field, H. et al. (2010) Hendra virus senioroutbreak management with n level,ovel the clinical research flevel,eatures, and the operational While theAustralia. animal and Emerg human. Infect health. Disagencies. 16, 338successfully-340. level. Cooperation was strengthened by the emergence of two coordinated and managed this initial outbreak response, other zoonoses in the mid-1990s – Japanese encephalitis virus the equine and human components of the response were and Australian bat lyssavirus – which both precipitated a series primarily Figureconducted 1. as Independent discrete, parallel Hendra activities. virus Subsequent incidents of byinter-agency year (to assessments. 31 August Thus, 2012) when, withsubsequent Hendra illustration of the number of associated human cases by year.

Figure 1. Independent Hendra virus incidents by year (to 31 August 2012), with illustration of the number of associated human cases by year.

168 MICROBIOLOGY AUSTRALIA • NOVEMBER 2012

Under the Microscope

incidents occurred, strong cross-agency linkages already existed, necessary skill-sets. These aspects need to be underpinned by facilitating ready communication and coordination of response formal Memoranda of Understanding and agreements between activities. Another milestone in the One Health evolution was the agencies which facilitate good outcomes by defining the the 2008 Hendra virus incident, which involved multiple equine roles and expectations of each agency, and the communication and human cases at a veterinary clinic12. Subsequent to this pathways which support the management of the incident. incident, an inter-agency technical working group was formed to provide current, science-based, best practice recommendations References to limit Hendra virus transmission, informing both animal 1. Jones, K.E. et al. (2008) Global trends in emerging infectious diseases. Nature 451, 990–993. health and public health policy. External review of inter-agency 2. Anon (2010) The FAO-OIE-WHO Collaboration. A Tripartite Concept Note. cooperation in the form of commissioned Incident Reviews and http://web.oie.int/downld/FINAL_CONCEPT_NOTE_Hanoi.pdf

Ombudsman’s Reports have further strengthened and indeed 3. Baldock, F.C. et al. (1996) Epidemiological investigations into the 1994 Equine championed the One Health approach. Morbillivirus outbreaks in Queensland, Australia. Singapore Veterinary J. 20, 57–61.

The identification of species of fruit bats as the natural host 4. Selvey, L.A. et al. (1995) Infection of humans and horses by a newly described morbillivirus. Med. J. Aust. 162, 642–645. of Hendra virus brought a third perspective that invited a 5. Daszak, P. et al. (2000) Emerging infectious diseases of wildlife – threats to broader One Health approach. However, the involvement of biodiversity and human health. Science 287, 443–448. environmental agencies was slower to occur, perhaps reflecting a 6. Mahalingam, S. et al. (2012) Hendra virus: an emerging paramyxovirus in fundamental wildlife management focus and a limited infectious Australia, Lancet Infect. Dis. 12, 799-807. disease focus. Thus, an emerging zoonosis involving horse 7. Hayman, D.T. et al. (2012) The development of One Health approaches in henipavirus research. Curr. Top. Microbiol. Immunol. (in press) to human transmission (notwithstanding the virus’s wildlife 8. Murray, K. et al. (1995) A morbillivirus that caused fatal disease in horses and reservoir) may not initially have been viewed as a priority. It is humans. Science 268, 94–97. now recognised that awareness and consideration of ecological 9. Douglas, I.C. et al. (1997) Outbreak investigation of an emerging disease factors that contribute to Hendra virus spillover events are (Equine Morbillivirus). In Epidemiologie et Sante Animale Proceedings of the 8th ISVEE conference, 04.08.01–04.08.03, International society for veterinary fundamental to effective risk mitigation, and that this perspective epidemiology and economics. informs and complements the risk management and response 10. Allworth, A. et al. (1995) Equine morbillivirus in Queensland. Comm. Dis. perspectives of the other agencies. Intell. 19, 575.

11. O'Sullivan, J.D. et al. (1997) Fatal encephalitis due to novel paramyxovirus The evolution of a One Health approach to Hendra virus in transmitted from horses. Lancet 349, 93–95.

Australia has resulted in more informed, efficient and effective 12. Field, H. et al. (2010) Hendra virus outbreak with novel clinical features, Australia. Emerg. Infect. Dis. 16, 338–340. management of what is a complex personal, political, social and biological system. However, the transition to One Health Biographies has involved something of a cultural shift for animal health and Dr Hume Field is the Principal Veterinary Epidemiologist at public health practitioners in Australia. Historically, veterinarians Biosecurity Queensland. have tended to believe that they have a greater awareness Dr Brad McCall graduated in medicine from the University of threatening zoonoses than their medical counterparts – a of Queensland in 1985 and as a specialist in Public Health scenario with a tendency to foster professional tension. A One Medicine in 1995. Since then he has been the Director of the Disease Control team in Brisbane Southside Public Health Unit Health approach, like all effective collaboration, requires mutual with responsibility for immunisation and communicable disease respect, trust and acknowledgement of the complementary control programs locally. His interests include immunisation, skills of all parties. It also requires dynamic expert leadership, communicable disease control, health systems and disaster practice in complex incident management structures, and the management.

MICROBIOLOGY AUSTRALIA • NOVEMBER 2012 169