This publication does not have an abstract

Allworth A

Baldock FC

Bolker B

Field H

Hall L

Halpin K

Hanna J

Rogers RJ

Young PL

Field, H.E.

Breed, A.C.

Sheild, J.

Hedlefs, R.M.

Pittard, K.

Pott, B.

Summers, P.M.

ResearchOnline at James Cook University

EQUINE EQUINE Australian Veterinary Journal   Volume 85, No 7, July 2007 © 2007 The State of Queensland, Department of Primary Industries and FisheriesJournal compilation © 2007 Australian Veterinary Association 268 Blackwell Publishing AsiaEpidemiological perspectives on Hendra virus infection in horses and flying foxes HE FIELD, a  AC BREED, b  J SHIELD, c  RM HEDLEFS, d  K PITTARD, e  B POTT f  and PM SUMMERS g Key words: Hendra virus, fruit bats, horses, epidemiology Aust Vet J  2007;85:268–270 doi: 10.1111/j.1751-0813.2007.00170.xH endra virus was first described in 1994 in Australia aftera sudden outbreak of an acute respiratory syndrome inThoroughbred horses in a Brisbane racing stable. Thesyndrome was characterised by severe respiratory signs andhigh mortality. A previously undescribed virus of the family Paramyxoviridae , initially named equine morbillivirus, wasidentified as the causal agent. 1  The virus was later renamedHendra virus after the Brisbane suburb where the outbreakoccurred. Thirteen of 20 infected horses died, and a stablehandand the trainer were infected, the latter fatally. Fruit bats ofthe genus  Pteropus  (family  Pteropodidae ), colloquially known asflying foxes, were subsequently shown to be the likely reservoirhost of Hendra virus and the putative source of infection forhorses. 2,3  The second identified outbreak in horses (involvingthe fatal infection of two horses on a Thoroughbred stud nearMackay in central Queensland) actually preceded the Brisbaneoutbreak by several weeks but was identified retrospectively afterthe Hendra virus–attributed death of the stud owner 15 monthslater. 4,5  The third known incident involved a single fatal case in a9-year-old Thoroughbred mare in the Cairns region of northernQueensland in January 1999. 6  No human cases were involved.Two new cases of Hendra virus infection (or probable infection)in horses in northern Queensland, described below, prompt thisreview of epidemiological aspects of Hendra virus infection inhorses and flying foxes.On 25 October 2004, a 10-year-old Thoroughbred gelding(Case A), one of eight horses on a 5.6 ha semi-rural property26 km south of Cairns, died after an acute illness. During anobserved 24 h clinical course, the horse was reported to be ‘offcolour’, exhibiting restlessness, inappetence, profuse sweatingand increased respiratory effort. On veterinary examination,the horse was in lateral recumbency with a rectal temperature of> 41 ° C, a heart rate of > 120 beats per minute, distended jugularveins, a capillary refill time of 3 s, injected mucous membranes,severe dyspnoea with a respiratory rate of > 100 breaths perminute, and a large amount of red froth flowing from the nos-trils. He was very weak, unable to stand or hold his head off theground, but was not rolling or thrashing. The horse died and anecropsy was done. Hendra virus was not considered as a differ-ential diagnosis at the time, and no samples were taken to enablea definitive retrospective diagnosis of Hendra virus infection.The veterinarian who undertook a necropsy reported the onsetof influenza-like symptoms on 2 November 2004. Two otherpeople assisting with the necropsy reported similar symptoms.All three were negative for antibodies to Hendra virus by immuno-fluorescent antibody test (IFT) and enzyme-linked immuno-sorbent assay (ELISA) at that time. A second sample taken fromthe veterinarian on 16 November 2004 was positive for anti–Hendra virus antibodies by IFT and ELISA, and neutralisingantibodies to Hendra virus were detected by serum neutrali-sation test. The symptoms in the two necropsy assistants wereattributed to illnesses unrelated to Hendra virus. Case A wasregarded as a probable case of Hendra virus infection, and thesource of infection to the veterinarian, based on a clinical historyconsistent with Hendra virus infection, the absence of such clinicalhistory in all 12 horses that the veterinarian had attended in thepreceding 8 weeks, and the rising antibody titre exhibited by theveterinarian. Aspects of this case are also reported by Hanna et al. 12 On 1 December 2004, a solitary 14-year-old Thoroughbredgelding (Case B) on a 0.75 ha semi-rural property 20 km southof  Townsville (and 400 km south of Case A) was humanely killedafter veterinary examination revealed a 40 ° C rectal temperature,moist rales, increased heart rate and toxic mucous membranes.The owners reported that the horse had shown a nasal dischargeand a variable appetite during the previous week but had deteri-orated in the final 48 h, walking abnormally and repeatedlyattempting to lie down (signs suggestive of colic). On necropsy,blood stained froth was present in the trachea and bronchi, thelungs were uniformly congested and oedematous and petechialhaemorrhages were present in the apical lobes of the lungs, dorsalthorax and epiglottis. There was no increase in pleural fluid.Microscopic examination of lung tissue revealed extensive alveo-lar haemorrhage and oedema, necrosis of alveolar macrophages,intra-vascular coagulation, scattered endothelial syncytium and amononuclear vasculitis. Fibrinoid necrosis of small arteries andassociated mild interstitial mononuclear infiltration as well as a Department of Primary Industries and Fisheries, Yeerongpilly QLD 4105; hume.field@dpi.qld.gov.au b School of Veterinary Science, The University of Queensland, St Lucia QLD 4072 c Department of Primary Industries and Fisheries, Cairns QLD 4870 d Department of Primary Industries and Fisheries, Townsville QLD 4810 e Cairns Veterinary Clinic, Manoora QLD 4870 f Townsville Veterinary Clinic, Aitkenvale QLD 4814 g School of Veterinary and Biomedical Sciences, James Cook University, Townsville QLD 4811. avj_170.fm  Page 268  Wednesday, June 20, 2007  10:57 AM EQUINE EQUINE © 2007 The State of Queensland, Department of Primary Industries and Fisheries Australian Veterinary Journal   Volume 85, No 7, July 2007Journal compilation © 2007 Australian Veterinary Association 269 focal necrosis was present in the myocardium. No changes wereseen in the liver, spleen, right kidney or gastro-intestinal tract.The cortex of the anterior left kidney was atrophied and thedilated pelvis contained several uroliths, the largest 4  ×  6 cm. Adiagnosis of Hendra virus infection was confirmed on the basisof viral antigen detection by immunohistochemical staining andviral RNA detection by PCR. Eighteen people with possibleat-risk exposure (including the two veterinarians who performedthe clinical examination and necropsy respectively) were negativefor neutralising antibodies to Hendra virus on serial blood tests.The two cases above have a number of features in commonwith previous index cases, namely breed (Thoroughbred), age(> 8 years old), housing (paddocked), season (spring to summer),and presence of flying fox food or roost trees in the horse pad-dock. 6  Case A was a 10-year-old Thoroughbred; Case B was a14-year-old Thoroughbred. Case A grazed pasture under exoticfruit trees and native eucalypts, both seasonally favoured byflying foxes; Case B was primarily handfed (his food bin attachedto the trunk of a eucalyptus tree) and grazed a small area adjoin-ing native riparian vegetation, again including seasonally favouredfood trees. Natural and experimental infections in horses indi-cate an incubation period in horses of 8 to 16 d 7  and 4 to 10 d 1 respectively, so it is likely that Case A was exposed in midOctober, and Case B in mid to late November, overlapping thepeak September to November birthing season of  Pteropus alecto (black flying fox) and  P conspicillatus  (spectacled flying fox). 8 Female gender and pregnancy, features common to previouscases, were not features of either case reported here.While overinterpretation of features of the spillover events todate is unwise given the limited sample size, some considerationof possible patterns is appropriate. These two cases are tempo-rally and spatially clustered, as were the earlier Mackay (August1994) and Brisbane (September 1994) cases, although the spatialclustering is weaker in the latter. Thus spillover to horses, ratherthan being sporadic, may reflect an episodic pattern of infectionin flying foxes. An outbreak of infection in a colony of flyingfoxes could result in a peak of virus excretion with a resultantincreased probability of exposure and possible infection of horsesin the vicinity for a limited time. Such a pattern of pulsatingendemicity of infection 13  in flying foxes would require the attain-ment of a threshold proportion of susceptible flying foxes withina colony sufficient to support an outbreak, and the subsequentintroduction of infection by a nomadic individual or group froma currently infected colony. This process of metapopulationdynamics is well recognised for other paramyxoviruses such asmeasles 10  and phocine distemper. 11  In Australia, flying foxes havethe necessary spatially structured population to support meta-population dynamics, and are seasonally nomadic, and it is plau-sible that the means by which Hendra virus maintains itselfwithin its reservoir would incorporate these host features.Spatial clustering of equine cases is also evident on a regionalscale, in that all known spillovers to date have been in north-eastern Australia (Figure 1). Yet the distribution of neither horsesnor flying foxes is restricted to this region. However, north-eastern Australia does have the greatest diversity of flying foxspecies (four species), with  P conspicillatus  endemic to northernQueensland, and the eastern distribution of  P alecto  confinedto Queensland and northern New South Wales. 8  Thus, if speciesand/or species biodiversity are important determinants of thepattern of Hendra virus infection in flying foxes or the risk ofspillover, then the limited geographic occurrence in horses todate is plausibly explained. Further investigation of the dynamicsof Hendra virus infection in flying foxes and the mode of trans-mission to horses is warranted.The recent cases in northern Queensland provide an opportu-nity to investigate the dynamics of Hendra virus infection inflying foxes. Flying fox colonies were identified in the vicinityof both index case paddocks, and their putative infected statusat the time the horses were infected, provides a baseline forproposed longitudinal serologic survey. If a pattern of pulsatingendemicity of infection does occur in flying foxes as previouslydiscussed, a peak seroprevalence could be expected immediatelypost epidemic, with seroprevalence falling over subsequent yearsas the proportion of susceptible flying foxes increases again.The survey data will be used to test this hypothesis and to sup-port predictive modelling of Hendra virus infection dynamics inflying foxes, and thereby contribute to spillover risk managementby identifying any pattern of infection in the reservoir host andthus any periodicity of increased risk of spillover. Addendum Two further cases of Hendra virus infection occurred in north-eastern Australia in 2006 in two separate incidents. The first wasat Peachester in south-east Queensland ( June), and the secondat Murwillumbah in northern New South Wales (October). Thefeatures of breed (Thoroughbred), age (> 8 years old), housing(paddocked), and the presence of flying fox food trees wereconsistent with previous index cases, and spatial and temporalclustering was again evident.Figure 1. Distribution of flying foxes on mainland Australia and location ofHendra virus spillover events to horses.Adapted from Hall and Richards, 20008 avj_170.fm  Page 269  Wednesday, June 20, 2007  10:57 AM EQUINE EQUINE Australian Veterinary Journal   Volume 85, No 7, July 2007 © 2007 The State of Queensland, Department of Primary Industries and FisheriesJournal compilation © 2007 Australian Veterinary Association 270 Acknowledgments The authors acknowledge the owners of both horses for theircooperation during the investigations, the Diagnostic, Responseand Surveillance Group at the CSIRO Australian Animal HealthLaboratory who conducted the PCR, immunohistochemistryand serology on forwarded samples from Case B, and CarmelTaylor, Ina Smith and Scott Craig at Queensland HealthScientific Services Laboratories who conducted the humanserology associated with both cases. References 1. Murray K, Selleck P, Hooper P et al. A morbillivirus that caused fatal diseasein horses and humans.  Science  1995;268:94–97.2. Young PL, Halpin K, Selleck PW et al. Serologic evidence for the presence inPteropus bats of a paramyxovirus related to equine morbillivirus.  Emerg InfectDis . 1996;2:239–240.3. Halpin K, Young P, Field H, Mackenzie J. Isolation of Hendra virus from pter-opid bats: a natural reservoir of Hendra virus.  J Gen Virol  2000;81:1927–1932.4. Rogers RJ, Douglas IC, Baldock FC et al. Investigation of a second focus ofequine morbillivirus infection in coastal Queensland.  Aust Vet J  1996;74:243–244.5. Allworth A, O’Sullivan J, Selvey L, Sheridan J. Equine morbillivirus in Queens-land.  Communicable Disease Intelligence  1995;19:575.6. Field H, Barratt P, Hughes R, Shield J, Sullivan N. A fatal case of Hendra virusinfection in a horse in north Queensland: clinical and epidemiological features. Aust Vet J  2000;78:279–280.7. Baldock FC, Douglas IC, Halpin K et al. Epidemiological investigations into the 1994equine morbillivirus outbreaks in Queensland, Australia.  Sing Vet J  1996;20:57–61.8. Hall L, Richards G. Flying foxes: Fruit and Blossom Bats of Australia. In: Daw-son TJ, editor.  Australian Natural History Series . University of New South WalesPress Ltd, Sydney, 2000.9. Field H. The ecology of Hendra virus and Australian bat lyssavirus. PhD thesis,The University of Queensland, Brisbane. http://espace.library.uq.edu.au/view.php?pid=UQ:13859. 2005.10. Bolker B, Grenfell B. Space, persistence and dynamics of measles epidemics. Phil Trans R Soc Lond  1995;348:309–320.11. Swinton J, Harwood J, Grenfell B, Gilligan C. Persistence thresholds forphocine distemper virus infection in harbour seal  Phoca vitulina  metapopulations. J Anim Ecol  1998;67:54–68.12. Hanna J, McBride W, Brookes D et al. Hendra virus infection in a veterinar-ian.  MJA  2006;185:562–564.13. Thrusfield M.  Veterinary Epidemiology  2nd edn. Blackwell Science Ltd,Oxford, 1995.  (Accepted for publication 28 March 2007)            avj_170.fm  Page 270  Wednesday, June 20, 2007  10:57 AM

English

Epidemiological perspectives on Hendra virus infection in horses and flying foxes

Crossref

ResearchOnline@JCU

https://researchonline.jcu.edu.au/2272/1/16210_C1_2007.pdf

Epidemiological perspectives on Hendra virus infection in horses and flying foxes

Abstract

Similar works

Full text

Available Versions

ResearchOnline at James Cook University

Crossref

ResearchOnline@JCU