Routes of Hendra Virus Excretion in Naturally-Infected Flying-Foxes: Implications for Viral Transmission and Spillover Risk.
Abstract: Pteropid bats or flying-foxes (Chiroptera: Pteropodidae) are the natural host of Hendra virus (HeV) which sporadically causes fatal disease in horses and humans in eastern Australia. While there is strong evidence that urine is an important infectious medium that likely drives bat to bat transmission and bat to horse transmission, there is uncertainty about the relative importance of alternative routes of excretion such as nasal and oral secretions, and faeces. Identifying the potential routes of HeV excretion in flying-foxes is important to effectively mitigate equine exposure risk at the bat-horse interface, and in determining transmission rates in host-pathogen models. The aim of this study was to identify the major routes of HeV excretion in naturally infected flying-foxes, and secondarily, to identify between-species variation in excretion prevalence. A total of 2840 flying-foxes from three of the four Australian mainland species (Pteropus alecto, P. poliocephalus and P. scapulatus) were captured and sampled at multiple roost locations in the eastern states of Queensland and New South Wales between 2012 and 2014. A range of biological samples (urine and serum, and urogenital, nasal, oral and rectal swabs) were collected from anaesthetized bats, and tested for HeV RNA using a qRT-PCR assay targeting the M gene. Forty-two P. alecto (n = 1410) had HeV RNA detected in at least one sample, and yielded a total of 78 positive samples, at an overall detection rate of 1.76% across all samples tested in this species (78/4436). The rate of detection, and the amount of viral RNA, was highest in urine samples (>serum, packed haemocytes >faecal >nasal >oral), identifying urine as the most plausible source of infection for flying-foxes and for horses. Detection in a urine sample was more efficient than detection in urogenital swabs, identifying the former as the preferred diagnostic sample. The detection of HeV RNA in serum is consistent with haematogenous spread, and with hypothesised latency and recrudesence in flying-foxes. There were no detections in P. poliocephalus (n = 1168 animals; n = 2958 samples) or P. scapulatus (n = 262 animals; n = 985 samples), suggesting (consistent with other recent studies) that these species are epidemiologically less important than P. alecto in HeV infection dynamics. The study is unprecedented in terms of the individual animal approach, the large sample size, and the use of a molecular assay to directly determine infection status. These features provide a high level of confidence in the veracity of our findings, and a sound basis from which to more precisely target equine risk mitigation strategies.
Publication Date: 2015-10-15 PubMed ID: 26469523PubMed Central: PMC4607162DOI: 10.1371/journal.pone.0140670Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
- Diagnosis
- Disease control
- Disease Diagnosis
- Disease Etiology
- Disease Management
- Disease Outbreaks
- Disease Prevention
- Disease Surveillance
- Disease Transmission
- Disease Treatment
- Epidemiology
- Equine Health
- Hendra Virus
- Horses
- Infectious Disease
- Public Health
- Veterinary Research
- Veterinary Science
- Virus
- Wildlife
- Zoonotic Diseases
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article focuses on investigating the major routes of Hendra virus (HeV) excretion in flying-foxes and the potential difference across species. The highest presence and amount of the virus were detected in the urine of the Pteropus alecto species, making it the most plausible infection source.
Objective and Background
- The research aimed to identify the primary routes of Hendra virus excretion in naturally infected flying-foxes and study the difference in excretion prevalence among species.
- Flying-foxes are the natural host of Hendra virus, a sporadic cause of fatal disease in horses and humans in Eastern Australia.
- The prevalent belief is that urine is a significant infectious medium driving bat-to-bat and bat-to-horse transmission. However, the relative importance of other excretion routes like nasal and oral secretions, and faeces, is not well-known.
- Understanding HeV excretion routes in flying-foxes is crucial to effectively mitigate equine exposure risk and determine transmission rates in host-pathogen models.
Methodology
- The researchers captured and sampled 2840 flying-foxes from three of the four Australian mainland species (Pteropus alecto, P. poliocephalus, and P. scapulatus).
- Collection took place at multiple roost locations in the Eastern states of Queensland and New South Wales between 2012 and 2014.
- The team collected various biological samples (urine, serum, urogenital, nasal, oral, and rectal swabs) from anaesthetized bats.
- Using a qRT-PCR assay, they tested these samples for HeV RNA.
Findings
- Out of 1410 P. alecto, 42 had detectable HeV RNA in at least one sample, procuring a total of 78 positive samples. This yielded a detection rate of 1.76% across all samples tested in this species.
- The highest rate of detection and the most viral RNA was found in urine samples. This was followed by serum, then packed haemocytes, faecal, nasal, and oral samples, hence establishing urine as the most likely source of infection.
- The detection of HeV RNA in urine was more efficient than in urogenital swabs, implying urine as the preferred diagnostic sample.
- There were no detections in P. poliocephalus or P. scapulatus species, supporting previous studies suggesting these species are epidemiologically less significant than P. alecto in HeV infection dynamics.
Conclusion
- The study’s approach, large sample size, and use of a molecular assay to directly determine infection status make it a pioneering study in this field.
- These factors provide an elevated confidence level in the findings and a solid foundation to more accurately target equine risk mitigation strategies.
Cite This Article
APA
Edson D, Field H, McMichael L, Vidgen M, Goldspink L, Broos A, Melville D, Kristoffersen J, de Jong C, McLaughlin A, Davis R, Kung N, Jordan D, Kirkland P, Smith C.
(2015).
Routes of Hendra Virus Excretion in Naturally-Infected Flying-Foxes: Implications for Viral Transmission and Spillover Risk.
PLoS One, 10(10), e0140670.
https://doi.org/10.1371/journal.pone.0140670 Publication
Researcher Affiliations
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia; EcoHealth Alliance, New York, New York, United States of America.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Elizabeth Macarthur Agricultural Institute, New South Wales Department of Primary Industries, Menangle, NSW, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
- Wollongbar Primary Industries Institute, New South Wales Department of Primary Industries, Wollongbar, NSW, Australia.
- Elizabeth Macarthur Agricultural Institute, New South Wales Department of Primary Industries, Menangle, NSW, Australia.
- Queensland Centre for Emerging Infectious Diseases, Department of Agriculture and Fisheries, Coopers Plains, Queensland, Australia.
MeSH Terms
- Animals
- Australia
- Chiroptera / classification
- Chiroptera / virology
- Feces / virology
- Female
- Hendra Virus / genetics
- Hendra Virus / isolation & purification
- Henipavirus Infections / transmission
- Henipavirus Infections / veterinary
- Henipavirus Infections / virology
- Horse Diseases / virology
- Horses
- Male
- Mouth / virology
- Nose / virology
- Rectum / virology
- Serum / virology
- Species Specificity
- Urine / virology
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 48 references
- Allworth A, O'Sullivan J, Selvey L, Sheridan J. Equine morbillivirus in Queensland. Communicable Diseases Intelligence 1995;19(22):575.
- Rogers RJ, Douglas IC, Baldock FC, Glanville RJ, Seppanen KT, Gleeson LJ, Selleck PN, Dunn KJ. Investigation of a second focus of equine morbillivirus infection in coastal Queensland.. Aust Vet J 1996 Sep;74(3):243-4.
- Halpin K, Young PL, Field HE, Mackenzie JS. Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus.. J Gen Virol 2000 Aug;81(Pt 8):1927-1932.
- Young P, Halpin K, Field H, Mackenzie J. Finding the wildlife reservoir of equine morbillivirus. .
- Young PL, Halpin K, Selleck PW, Field H, Gravel JL, Kelly MA, Mackenzie JS. Serologic evidence for the presence in Pteropus bats of a paramyxovirus related to equine morbillivirus.. Emerg Infect Dis 1996 Jul-Sep;2(3):239-40.
- Anon. What is Hendra Virus?. Brisbane, Australia: Department of Agriculture, Forestry and Fisheries, Queensland Government; 2015.
- Williamson MM, Hooper PT, Selleck PW, Gleeson LJ, Daniels PW, Westbury HA, Murray PK. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats.. Aust Vet J 1998 Dec;76(12):813-8.
- Williamson MM, Hooper PT, Selleck PW, Westbury HA, Slocombe RF. Experimental hendra virus infectionin pregnant guinea-pigs and fruit Bats (Pteropus poliocephalus).. J Comp Pathol 2000 Feb-Apr;122(2-3):201-7.
- Halpin K, Hyatt AD, Fogarty R, Middleton D, Bingham J, Epstein JH, Rahman SA, Hughes T, Smith C, Field HE, Daszak P. Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission.. Am J Trop Med Hyg 2011 Nov;85(5):946-51.
- Field H, Young P, Yob JM, Mills J, Hall L, Mackenzie J. The natural history of Hendra and Nipah viruses.. Microbes Infect 2001 Apr;3(4):307-14.
- Baker ML, Schountz T, Wang LF. Antiviral immune responses of bats: a review.. Zoonoses Public Health 2013 Feb;60(1):104-16.
- Little TJ, Shuker DM, Colegrave N, Day T, Graham AL. The coevolution of virulence: tolerance in perspective.. PLoS Pathog 2010 Sep 9;6(9):e1001006.
- Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, Middleton D, Reid PA, McFarlane RA, Martin G, Tabor GM, Skerratt LF, Anderson DL, Crameri G, Quammen D, Jordan D, Freeman P, Wang LF, Epstein JH, Marsh GA, Kung NY, McCallum H. Ecological dynamics of emerging bat virus spillover.. Proc Biol Sci 2015 Jan 7;282(1798):20142124.
- Daniels PW, Halpin K, Hyatt A, Middleton D. Infection and disease in reservoir and spillover hosts: determinants of pathogen emergence.. Curr Top Microbiol Immunol 2007;315:113-31.
- Weaver GV, Domenech J, Thiermann AR, Karesh WB. Foot and mouth disease: a look from the wild side.. J Wildl Dis 2013 Oct;49(4):759-85.
- Field H, de Jong C, Melville D, Smith C, Smith I, Broos A, Kung YH, McLaughlin A, Zeddeman A. Hendra virus infection dynamics in Australian fruit bats.. PLoS One 2011;6(12):e28678.
- Smith I, Broos A, de Jong C, Zeddeman A, Smith C, Smith G, Moore F, Barr J, Crameri G, Marsh G, Tachedjian M, Yu M, Kung YH, Wang LF, Field H. Identifying Hendra virus diversity in pteropid bats.. PLoS One 2011;6(9):e25275.
- Barr J, Smith C, Smith I, de Jong C, Todd S, Melville D, Broos A, Crameri S, Haining J, Marsh G, Crameri G, Field H, Wang LF. Isolation of multiple novel paramyxoviruses from pteropid bat urine.. J Gen Virol 2015 Jan;96(Pt 1):24-29.
- Barr JA, Smith C, Marsh GA, Field H, Wang LF. Evidence of bat origin for Menangle virus, a zoonotic paramyxovirus first isolated from diseased pigs.. J Gen Virol 2012 Dec;93(Pt 12):2590-2594.
- Marsh GA, de Jong C, Barr JA, Tachedjian M, Smith C, Middleton D, Yu M, Todd S, Foord AJ, Haring V, Payne J, Robinson R, Broz I, Crameri G, Field HE, Wang LF. Cedar virus: a novel Henipavirus isolated from Australian bats.. PLoS Pathog 2012;8(8):e1002836.
- Vidgen ME, de Jong C, Rose K, Hall J, Field HE, Smith CS. Novel paramyxoviruses in Australian flying-fox populations support host-virus co-evolution.. J Gen Virol 2015 Jul;96(Pt 7):1619-25.
- Breed AC, Meers J, Sendow I, Bossart KN, Barr JA, Smith I, Wacharapluesadee S, Wang L, Field HE. The distribution of henipaviruses in Southeast Asia and Australasia: is Wallace's line a barrier to Nipah virus?. PLoS One 2013;8(4):e61316.
- McCallum H, Barlow N, Hone J. How should pathogen transmission be modelled?. Trends Ecol Evol 2001 Jun 1;16(6):295-300.
- Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, Daszak P. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.).. Proc Biol Sci 2011 Dec 22;278(1725):3703-12.
- Edson D, Field H, McMichael L, Jordan D, Kung N, Mayer D, Smith C. Flying-fox roost disturbance and Hendra virus spillover risk.. PLoS One 2015;10(5):e0125881.
- Field H, Jordan D, Edson D, Morris S, Melville D, Parry-Jones K, Broos A, Divljan A, McMichael L, Davis R, Kung N, Kirkland P, Smith C. Spatiotemporal Aspects of Hendra Virus Infection in Pteropid Bats (Flying-Foxes) in Eastern Australia.. PLoS One 2015;10(12):e0144055.
- Jonsson NN, Johnston SD, Field H, de Jong C, Smith C. Field anaesthesia of three Australian species of flying fox.. Vet Rec 2004 May 22;154(21):664.
- Smith IL, Halpin K, Warrilow D, Smith GA. Development of a fluorogenic RT-PCR assay (TaqMan) for the detection of Hendra virus.. J Virol Methods 2001 Oct;98(1):33-40.
- Breed AC, Breed MF, Meers J, Field HE. Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus)--implications for disease risk management.. PLoS One 2011;6(12):e28816.
- Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE. Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus).. Proc Biol Sci 2008 Apr 7;275(1636):861-9.
- Rahman SA, Hassan L, Epstein JH, Mamat ZC, Yatim AM, Hassan SS, Field HE, Hughes T, Westrum J, Naim MS, Suri AS, Jamaluddin AA, Daszak P. Risk Factors for Nipah virus infection among pteropid bats, Peninsular Malaysia.. Emerg Infect Dis 2013 Jan;19(1):51-60.
- Bassiouni A, Cleland EJ, Psaltis AJ, Vreugde S, Wormald PJ. Sinonasal microbiome sampling: a comparison of techniques.. PLoS One 2015;10(4):e0123216.
- Daley P, Castriciano S, Chernesky M, Smieja M. Comparison of flocked and rayon swabs for collection of respiratory epithelial cells from uninfected volunteers and symptomatic patients.. J Clin Microbiol 2006 Jun;44(6):2265-7.
- Hernes SS, Quarsten H, Hagen E, Lyngroth AL, Pripp AH, Bjorvatn B, Bakke PS. Swabbing for respiratory viral infections in older patients: a comparison of rayon and nylon flocked swabs.. Eur J Clin Microbiol Infect Dis 2011 Feb;30(2):159-65.
- Dietrich M, Wilkinson DA, Benlali A, Lagadec E, Ramasindrazana B, Dellagi K, Tortosa P. Leptospira and paramyxovirus infection dynamics in a bat maternity enlightens pathogen maintenance in wildlife.. Environ Microbiol 2015 Nov;17(11):4280-9.
- van Dijk JG, Fouchier RA, Klaassen M, Matson KD. Minor differences in body condition and immune status between avian influenza virus-infected and noninfected mallards: a sign of coevolution?. Ecol Evol 2015 Jan;5(2):436-49.
- Goldspink LK, Edson DW, Vidgen ME, Bingham J, Field HE, Smith CS. Natural Hendra Virus Infection in Flying-Foxes - Tissue Tropism and Risk Factors.. PLoS One 2015;10(6):e0128835.
- Berhane Y, Weingartl HM, Lopez J, Neufeld J, Czub S, Embury-Hyatt C, Goolia M, Copps J, Czub M. Bacterial infections in pigs experimentally infected with Nipah virus.. Transbound Emerg Dis 2008 May;55(3-4):165-74.
- Wang HH, Kung NY, Grant WE, Scanlan JC, Field HE. Recrudescent infection supports Hendra virus persistence in Australian flying-fox populations.. PLoS One 2013;8(11):e80430.
- Sohayati AR, Hassan L, Sharifah SH, Lazarus K, Zaini CM, Epstein JH, Shamsyul Naim N, Field HE, Arshad SS, Abdul Aziz J, Daszak P. Evidence for Nipah virus recrudescence and serological patterns of captive Pteropus vampyrus.. Epidemiol Infect 2011 Oct;139(10):1570-9.
- Smith C, Skelly C, Kung N, Roberts B, Field H. Flying-fox species density--a spatial risk factor for Hendra virus infection in horses in eastern Australia.. PLoS One 2014;9(6):e99965.
- Churchill S. Australian bats 2nd ed. Crows Nest: Allen & Unwin; 1998.
- Hall L, Richards G. Flying Foxes: Fruit and Blossom Bats of Australia. Krieger Publishing; 2000.
- Field H, Crameri G, Kung NY, Wang LF. Ecological aspects of hendra virus.. Curr Top Microbiol Immunol 2012;359:11-23.
- Berger A, Scheibe KM, Eichhorn K, Scheibe A, Streich J. Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii), measured through one year under semi-reserve conditions. Applied Animal Behaviour Science 1999;64(1):1–17.
- Keiper RA, Keenan MA. Nocturnal activity patterns of feral ponies. Journal of Mammalogy 1980;16(1):116–8.
- Field HE, Smith CS, de Jong CE, Melville D, Broos A, Kung N, Thompson J, Dechmann DK. Landscape Utilisation, Animal Behaviour and Hendra Virus Risk.. Ecohealth 2016 Mar;13(1):26-38.
- Martin G, Plowright R, Chen C, Kault D, Selleck P, Skerratt LF. Hendra virus survival does not explain spillover patterns and implicates relatively direct transmission routes from flying foxes to horses.. J Gen Virol 2015 Jun;96(Pt 6):1229-1237.
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