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OFFICIAL JOURNAL OF THE AUSTRALIAN SOCIETY FOR MICROBIOLOGY INC.
Volume 41
40 Number 1 March 2020
2019
Zoonoses
plus Hot Topic: COVID-19
nt
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The Australian Society
for Microbiology Inc. OFFICIAL JOURNAL OF THE AUSTRALIAN SOCIETY FOR MICROBIOLOGY INC.
9/397 Smith Street
Fitzroy, Vic. 3065
Tel: 1300 656 423 Volume 41 Number 1 March 2020
Fax: 03 9329 1777
Email: admin@theasm.com.au
www.theasm.org.au Contents
ABN 24 065 463 274
Vertical Transmission 2
For Microbiology Australia
correspondence, see address below. Dena Lyras 2
Editorial team
Guest Editorial 3
Prof. Ian Macreadie, Mrs Hayley Macreadie Zoonoses 3
and Mrs Rebekah Clark John S Mackenzie and David Williams
Editorial
. Board In Focus 6
Dr Ipek Kurtböke (Chair) Prof. Wieland Meyer
Prof. Ross Barnard Mr Chris Owens The dynamic landscape of bat borne zoonotic viruses in Australia 6
Prof. Mary Barton Cheryl Power Kim Halpin and David N Durrheim
Prof. Linda Blackall Prof. William Rawlinson Reaching the zero by 30 dog-mediated human rabies goal 10
A/Prof. Prue Bramwell Prof. Tom Ross
Dr Rebecca LeBard Andrea Britton
Dr Paul Selleck
Dr Gary Lum Dr David Smith New insights into chlamydial zoonoses 14
Prof. Dena Lyras Ms Helen Smith Adam Polkinghorne and James Branley
Dr Sam Manna
Subscription rates Leptospirosis: key things to know about this quintessential
Current subscription rates are available zoonotic pathogen 19
from the ASM Melbourne office. Paul Effler
Editorial correspondence One Health: the global challenge of Clostridium difficile
Prof. Ian Macreadie infection 23
Tel: 0402 564 308 (Ian) Su-Chen Lim, Thomas V Riley and Daniel R Knight
Email: ian.macreadie@gmail.com
Rift Valley fever: a review 28
Published four times a year John Bingham and Petrus Jansen van Vuren
in print and open access online by
Seafood-borne parasites in Australia: human health risks,
fact or fiction? 33
Shokoofeh Shamsi
Brucella: not your ‘typical’ intracellular pathogen 38
Anthony L Keyburn and Nicky Buller
Unipark, Building 1, Level 1
195 Wellington Road, Clayton, Vic. 3168 Glanders: re-emergence of an ancient zoonosis 41
http://microbiology.publish.csiro.au Patricia Ellis
Publishing enquiries Hot Topic 45
Jenny Foster
Email: publishing.ma@csiro.au COVID-19: a novel zoonotic disease caused by a coronavirus
Production enquiries from China: what we know and what we don’t 45
Helen Pavlatos John S Mackenzie and David W Smith
Email: helen.pavlatos@csiro.au
Advertising enquiries ASM Affairs 51
Tel: 03 9545 8400
Email: publishing.advertising@csiro.au Obituary: Dr Leila Valerie Asche, PhD, AM, PhD (hon) CDU 51
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ments in Microbiology Australia are not necessarily those
of the Australian Society for Microbiology, the Editorial Cover image: An image of SARS-CoV-2, the virus responsible for COVID-19 disease. This image is a
Board, CSIRO, and CSIRO Publishing.
colourised transmission electron micrograph (TEM) and is work of the Australian Animal Health Laboratory
(AAHL), CSIRO.
M I CRO B I O L O G Y A U S T RALIA • MAR C H 2 0 2 0 1
Vertical Transmission
apologise for this postponement but we look forward to seeing
you at our next Annual Scientific Meeting and will communicate our
new plans as soon as possible. I would like to thank the local
organising committees for their work towards delivering the three
events, and to reassure them that their efforts will go a long way
towards our future planning.
On a related note, bringing our discipline to the attention of the
Dena Lyras
public and the government at this time is more important than ever.
President of ASM
To this end, the chair of our South Australian/Northern Territory
Branch, Peter Traynor, has been instrumental in lobbying for
the establishment of a Parliamentary Friends of Microbiology
As we progress through 2020, Microbiology is dominating the news group. The Australian Society for Microbiology warmly wel-
with the emergence and rapid dissemination of the novel corona- comes the reaffirmation of the Parliamentary Friends of Micro-
virus COVID-19. The impact of COVID-19 on public health, with biology, in the 46th Parliament, and we gratefully acknowledge
significant financial, logistical and social repercussions, has quickly the interest of our Federal parliamentarians and their staff in
become apparent, and is evolving rapidly in Australia. As micro- matters pertaining to our discipline, across its broad range of
biologists we have an important role to play during this time areas. It is intended that this Group will provide a non-partisan
because we can use our knowledge, expertise and experience to forum for MPs to meet and interact with academic, clinical and
educate the community around us, and to reduce the panic that scientific microbiologists on matters relating to infectious dis-
results from fear and misinformation. It is also critical that we eases, biosecurity, public health, veterinary and agricultural
ensure that individuals are not stigmatised because of their per- microbiology, food safety, epidemiology, and research and
ceived role in the transmission of this infectious disease. A co- innovation. We look forward to enabling their knowledge,
ordinated global effort is required to tackle this new infectious context and understanding of all matters microbiological, par-
threat, and we are an important local part of this effort. Indeed, our ticularly at this important time when infectious disease is
public health, medical, teaching and research communities have dominating news headlines and creating overwhelming com-
responded in a remarkable way to protect us against this pandemic, munity and public health concern. Please see the following link
and we are grateful for everything that they are doing. for more information: https://www.aph.gov.au/About_Parlia-
ment/Parliamentary_Friendship.
Unfortunately, due to this evolving global pandemic crisis and its
escalation in Australia, the ASM Executive has decided to postpone As always, please visit our website www.theasm.org.au to access
the Annual Scientific Meeting, CliniCon and EduCon, that were due information regarding upcoming meetings and awards. Note our
to take place in July 2020. We did not make this decision lightly and fresh new website, which is easier to navigate and currently show-
it was essential for us to adopt a responsible stand and to show a cases content created by our wonderful ASM Communication
duty of care to our members. Executive knows that enthusiasm for Ambassadors. You may also like to follow, and contribute to ASM
the conference had gained momentum as the Local Organising on Twitter, @AUSSOCMIC, or on Facebook to make sure you keep
Committee worked hard to build an engaging and exciting pro- up with the latest news, trends and developments in Microbiology
gram. This was a very hard decision to make. We regret and in Australia and around the world.
Have you heard of APPRISE?
It is the Australian Partnership for Preparedness Research on Infectious disease Emergencies. APPRISE says
‘Pandemics are unavoidable’ and lists seven ways their research can save lives.
These include supplying the latest information to decision-makers, investigating the first few hundred cases of each
new pandemic, working with communities, improving national and international data sharing, boosting our infectious
disease research workforce, improving infection prevention in hospitals and fast tracking trials of new treatments.
APPRISE works on a range of high-impact pathogens, for example, SARS-CoV, MERS CoV, EBOV, and Zika virus.
Check out their website: www.apprise.org.au to see their collaborating institutions, projects, and latest news.
2 MICROBIOLOGY AUSTRALIA MARCH 2020
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Guest Editorial
Zoonoses
CoV-2, almost certainly originating from bats and probably via an
as yet unknown intermediary host, such as pangolins. Other im-
portant emerging diseases have jumped from domesticated species,
such as pandemic influenza H1N1 originating from pigs in 2009.
What precipitates the cross-species jump, and what can be done
to prevent or mitigate it? Much of the recent increase in the
emergence and spread of zoonoses can be linked to environ-
mental and societal changes that have brought people and wild
and/or domesticated animals closer together, increasing the
potential for cross-species transmission. Environmental factors
and climate change are altering the habitats of animals or
John S Mackenzie and David Williams
arthropod vectors of zoonoses, changing how and where they
live. Anthropogenic factors have changed the interactions be-
The selection of papers included in this issue of Microbiology tween humans and their domestic animals through intensive
Australia present a broad brush of zoonotic diseases, from those agriculture and altered land use; and with the need to seek meat
known or described in ancient times such as rabies, first described for human consumption, there has been increased hunting of
in the Eshnunna cuneiform law tablets from ancient Mesopotamia wild animals for bushmeat. As cities have expanded and new
dating back to the 18th–19th centuries BC1, and glanders, thought population centres emerged, there has been increasing en-
to be first described in donkeys by Aristotle in Ancient Greece in croachment into wildlife habitats. In addition, increased city
2 3
420–450 BC and subsequently by the Romans , to some discovered living and expanding metropolitan areas are providing new
or recognised as zoonotic within the past 30 years, such as the homes for a variety of wildlife, from rats and mice to foxes,
recently described zoonotic bat-borne pathogens in Australia, and birds, fruit bats, wallabies, bandicoots, possums, and other small
Clostridium difficile, only recently recognised as a zoonotic path- marsupials in Australia, which can live off the plentiful food
ogen. The selection of papers also demonstrates the wide range of supply we discard or which are available in parks and gardens,
zoonotic origins, including arthropod-borne viruses and potential- and in additional green areas4,11. In other countries, many local
ly seafood-borne parasites. wildlife species are commonly making their homes in cities,
including monkeys, squirrels, mongooses and raccoons. Under-
More than 60% of human infectious diseases are caused by
scoring this is that ‘synanthropic’ mammal species, those wildlife
pathogens shared with wild or domestic animals4, and over
species that adapt well in human-modified environments, are
75% of emerging diseases are zoonotic in origin. Over the past
15 times more likely to be the source of emerging infectious
few decades, an increasing number of infectious diseases have
diseases12. As pathogens evolve and emerge, transmission of
jumped the species barrier from animals to humans to cause
zoonotic infections and outbreaks have occurred because of
disease, and in many instances have subsequently spread region-
the everyday practices of people. This often involves the chain
ally and/or globally. Most of these have been viruses jumping
of activities in livestock production, such as intensive growing,
from wildlife to humans, as exemplified by HIV/AIDS in the 1980s
breeding, transport, slaughter and sale of animals. In many
originating from the great apes possibly as early as the 1920s5; Sin
countries, live (‘wet’) animal markets where several species
Nombre virus, recognised as a cause of hantavirus pulmonary
of domestic or wild animals may be caged in close proximity
syndrome in 1993, originating from the deer mouse (Peromyscus
have been the origins of zoonoses. The interactions of
maniculatus)6; Nipah virus in 1998–99 originating from bats via
people with wildlife areas for recreational purposes such as
pigs7; severe acute respiratory syndrome coronavirus (SARS-
hunting, hiking and camping, also lead to zoonotic transmission
CoV) in 2002–03 originating from bats via civets8,9; Middle East
of pathogens.
respiratory syndrome coronavirus (MERS-CoV) in 2012 from
dromedary camels, but probably originating from bats more than Lessons should have been learnt from some of the emergent
10
30 years previously ; and currently, the novel coronavirus, SARS- zoonoses over the past few decades, but despite major outbreaks
M I C R O B I O L O GY A U S T R A L I A MARCH 20 20
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10 .107 1/MA200 02 3
Guest Editorial
of disease, the memories and messages seem to fail to resonate. The addressing zoonotic disease threats in-country and potentially
outbreak of SARS in 2002–03 was clearly associated with transmis- reducing the importation or spread of pathogens into Australia
sion from live wild animals in the wet markets of Guangdong. via people or animals/animal products.
Despite strong recommendations that these markets be stopped
It has been estimated that zoonoses cause about a billion cases of
because of the risks they pose of potential human transmission,
illness in people and millions of deaths every year, and emerging
they continue to flourish selling poultry and wild and often exotic
zoonoses are a rising threat to global health, having caused hun-
animals, often illegally (a temporary ban on the trade in wild animals
dreds of billions of US dollars of economic damage over the past
was introduced from 26 January 2020 by the Chinese Government).
30 years4. With the current emergence of the novel coronavirus in
The same problem exists in the trade and export of bushmeat
China now threatening to develop into a global pandemic, this
in Africa. While it is unlikely that the bushmeat trade will be halted
should surely raise enough concern for a concerted effort to reduce
in Africa as it provides a much-needed source of dietary
potential opportunities for future zoonosis emergence, using One
protein, export of bushmeat to Europe, US and elsewhere provides
Health approaches.
an ongoing risk of disease including Ebola, Marburg and other
exotic diseases13–15. The amount of bushmeat exported is
in surprisingly large amounts, measured in tonnes/airport/year
References
rather than kilograms.
1. Tarantola, A. (2017) Four thousand years of concepts relating to rabies in
animals and humans, its prevention and its cure. Trop. Med. Infect. Dis. 2, 5.
Another recommendation that has not been sufficiently heeded is doi:10.3390/tropicalmed2020005
the need to incorporate surveillance of wildlife disease outbreaks 2. Blancou, J. and Meslin, F.X. (2000) [Brief review of the history of zoonoses]. Rev.
Sci. Tech. Off. int. Epiz 19, 15–22[in French]. doi:10.20506/rst.19.1.1200
into national and global disease surveillance programs. In Australia,
3. Van Zandt, K.E. et al. (2013) Glanders: an overview of infection in humans.
a surveillance system has been implemented to detect outbreaks in Orphanet J. Rare Dis. 8, 131. doi:10.1186/1750-1172-8-131
free-living wildlife, and the information fed into coordination 4. Bradley, C.A. and Altizer, S. (2007) Urbanization and the ecology of wildlife
mechanisms that exist between animal health and public health16, diseases. Trends Ecol. Evol. 22, 95–102. doi:10.1016/j.tree.2006.11.001
5. Hahn, B.H. et al. (2000) AIDS as a zoonosis: scientific and public health implica-
and similar systems are in place in the United States and the
tions. Science 287, 607–614. doi:10.1126/science.287.5453.607
UK. Wildlife disease surveillance is not well resourced or well 6. Childs, J.E. et al. (1994) Serologic and genetic identification of Peromyscus
reported in many countries, and a concerted and cooperative push maniculatus as the primary rodent reservoir for a new hantavirus in the
southwestern United States. J. Infect. Dis. 169, 1271–1280. doi:10.1093/infdis/
is urgently needed to develop improved wild animal disease 169.6.1271
surveillance mechanisms, especially in resource-poor countries. 7. Chua, K.B. et al. (2002) Isolation of Nipah virus from Malaysian Island flying foxes.
Microbes Infect. 4, 145–151. doi:10.1016/S1286-4579(01)01522-2
Understanding the drivers of human behaviours that lead to the 8. Wang, L.F. and Eaton, B.T. (2007) Bats, civets and the emergence of SARS. Curr.
Top. Microbiol. Immunol. 315, 325–344. doi:10.1007/978-3-540-70962-6_13
emergence or re-emergence of zoonoses, not just the behaviours
9. Yang, X.L. et al. (2016) Isolation and characterization of a novel bat coronavirus
themselves, will be equally important to enable comprehensive closely related to the direct progenitor of severe acute respiratory syndrome
disease control and mitigation strategies to be put in place. Fun- coronavirus. J. Virol. 90, 3253–3256. doi:10.1128/JVI.02582-15
damental to this will be the commitment and support of relevant 10. Cui, J. et al. (2019) Origin and evolution of pathogenic coronaviruses. Nat. Rev.
Microbiol. 17, 181–192. doi:10.1038/s41579-018-0118-9
government departments and industry groups within an affected
11. Hassell, J.M. et al. (2017) Urbanization and disease emergence dynamics at the
country to resource zoonotic disease control and prevention wildlife-livestock-human interface. Trends Ecol. Evol. 32, 55–67. doi:10.1016/
j.tree.2016.09.012
through the combined efforts of the human health, livestock and
12. McFarlane, R. et al. (2012) Synanthropy of wild mammals as a determinant of
wildlife sectors. Continued efforts to identify potential zoonoses emerging infectious diseases in the Asian-Australasian region. EcoHealth 9,
through initiatives such as the USAID Expanded Pandemic Threats 24–35. doi:10.1007/s10393-012-0763-9
13. Smith, K.M. et al. (2012) Zoonotic viruses associated with illegally imported
program will also be another key element to zoonotic disease
wildlife products. PLoS One 7, e29505. doi:10.1371/journal.pone.0029505
preparedness. Closer to home, in Australia, zoonotic disease risks 14. Falk, H. et al. (2013) Illegal import of bushmeat and other meat products
are well recognised, and it will be important for those involved in into Switzerland on commercial passenger flights. Rev. Sci. Tech. 32, 727–739.
doi:10.20506/rst.32.2.2221
zoonotic disease diagnosis, research, surveillance and response to
15. Temmam, S. et al. (2017) Screening for viral pathogens in African simian
remain vigilant and vocal about the ongoing threat they pose. bushmeat seized at a French airport. Transbound. Emerg. Dis. 64, 1159–1167.
Continued and expanded support for the disease control capabil- doi:10.1111/tbed.12481
16. Woods, R. et al. (2019) The importance of wildlife disease monitoring as part
ities of our neighbours in the Pacific and Southeast Asia will also pay
of global surveillance for zoonotic diseases: the role of Australia. Trop. Med.
dividends for pre-border disease mitigation with the dual benefit of Infect. Dis 4, 29. doi:10.3390/tropicalmed4010029
4 MICROBIOLOGY AUSTRALIA MARCH 2020 *
Guest Editorial
Biographies Platform, based in Belgium. He is also working for one session a
week at PathWest in Perth.
Professor John Mackenzie is an Emeritus Professor of Curtin
University, and Honorary Professor in the School of Chemistry and Dr David Williams is the leader of the Emergency Disease
Molecular Biosciences at The University of Queensland. He is a past Laboratory Diagnosis group at the CSIRO Australian Animal Health
President of ASM (1992–94), and was awarded Life Membership of Laboratory, Geelong, Victoria. This group comprises multidisci-
the Society in 2019. His recent work has been concerned with global plinary capability in virus diagnostics, contributing to national and
aspects of infectious disease surveillance and response, particularly regional emergency animal and zoonotic disease diagnostics and
with respect to emerging zoonotic and vector-borne diseases. He surveillance. Dr Williams’ research interests have included the
has worked on a number of committees in the World Health detection, diagnosis, and epidemiology of emerging and exotic
Organization, including the Global Outbreak Alert and Response viruses that affect humans and animals in Australia and overseas.
Network, the Asia Pacific Strategy for Emerging Diseases, and was This work has focused on arthropod-borne viruses and has more
Chair of the first IHR Emergency Committee on Pandemic influenza recently extended to the laboratory diagnosis and pathogenesis of
2009. He currently serves on the Emergency Committees on the livestock diseases such as African swine fever, Bluetongue and
Spread of Poliovirus, and on the Novel Coronavirus Disease, influenza. He is a member of the National Arbovirus and Malaria
COVID-19. He currently serves on the National Arbovirus and Advisory Committee and has worked in advisory roles for the
Malaria Advisory Committee. He is also a co-founder of a new United Nations Food and Agriculture Organization and the World
foundation to support the concept of One Health, the One Health Animal Health Organisation (OIE).
M I C R O B I O L O GY A U S T R A L I A M A R C H 2 0 2 0
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5
In Focus
The dynamic landscape of bat borne zoonotic
viruses in Australia
Kim Halpin David N Durrheim
Australian Animal Health Laboratory University of Newcastle
5 Portarlington Road School of Medicine and Public
East Geelong, Vic. 3219, Australia Health, Callaghan Campus
Email: kim.halpin@csiro.au Newcastle, NSW 2287, Australia
This review discusses the history, epidemiology, diagnos- Hendra virus
tics, clinical presentation in humans, as well as control and
Since it was first described in Australia in 1994, HeV has caused
prevention measures, of the high-profile viruses Hendra
horse and human illness and deaths. A high prevalence of neutral-
virus (HeV) and Australian bat lyssavirus (ABLV). Since the
izing antibodies to HeV in bats of the genus Pteropus, and the
discovery of HeV and ABLV in the 1990s, these viruses have
isolation of Hendra virus from the same genus, confirmed flying
only caused disease in areas where spill-over hosts, includ-
foxes as reservoir hosts for this virus2. All four species of pteropus
ing humans, encounter the reservoir host.
bats can be infected (Table 1). From recent work it appears that the
risk of a spill-over event is greatest when either the black flying fox
Bats or the spectacled flying-fox is present3. The reservoir host appears
Australia is home to over 90 species of bats, covering many different to co-exist with this virus in complete harmony. The virus spreads
habitats. All but eight species belong to the suborder Microchir- easily amongst flying-foxes with the HeV seroprevalence in flying-
optera (microbats). See Table 1 for a list of the eight species from fox colonies fluctuating over time and geography. The theory of
the suborder Megachiropteran (megabats) found on mainland viral co-evolution with chiropteran hosts has been previously
Australia, four of which belong to the genus Pteropus (commonly suggested, and all field observations and experimental evidence
called flying foxes or fruit bats). Figure 1 provides a link to an to date supports this hypothesis4. Figure 1 provides a link to the
interactive map showing flying fox camps in Australia. results of Hendra virus research conducted in Australia, as well as
information for horse owners.
The distribution of bats in Australia has changed over time. As their
habitats are destroyed, many have been forced to adapt to life on Figure 2 compares the routes of transmission for HeV and ABLV
the urban fringe. There are many successful flying fox camps in the and other closely related bat viruses which result in human
heart of large and smaller cities across Australia – Brisbane, Sydney, infection. For HeV, horses are the main spill-over host and serve
Melbourne, Geelong and Cairns to name a few. In the past 10 years, as amplifying hosts, capable of infecting humans. The disease in
we have seen the southern limit of the black flying fox (Pteropus horses exhibits seasonality with more spill-over events occurring
alecto) distribution extend further south, and the south-western in winter. Since it was discovered in 1994, only 95 horses have
limit of the grey headed flying fox (Pteropus poliocephalus) dis- died to date. Horses in paddocks where flying foxes either roost
tribution extend across into South Australia as well. By contrast, the or come to feed, are at risk of exposure to infection. Infection in
very small footprint of the spectacled flying fox (Pteropus horses most likely occurs after close contact with bat urine and
conspicillatus) in far north Queensland, is predicted to get even birthing material which contain sufficiently high titres of virus to
smaller over time1. The black flying fox will most likely fill this void. infect a horse15.
The ecological drivers behind these changes are complex but are
highly likely to include loss of natural habitat, changes to food Extreme care must be taken in the handling of samples collected for
availability and warming climates. HeV diagnostic testing. HeV is a Biosafety level four (BSL4) agent, in
6 10 . 1 0 7 1 / M A 2 0 0 0 3 MICROBIOLOGY AUSTRALIA MARCH 2020
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In Focus
Table 1. Megachiropteran bats, all belonging to the family Pteropodidae, found on mainland Australia. One common name for each is listed, noting
that some have several common names. The last two columns highlight whether evidence of infection with HeV or ABLV has been found in that species.
Family Genus Species Common name(s) HeV ABLV
Pteropodidae include
Subfamily Pteropodinae Dobsonia Dobsonia magna Bare-backed Fruit Bat
Pteropus Pteropus alecto Black Flying-fox ü ü
Pteropus conspicillatus Spectacled Flying-fox ü ü
Pteropus poliocephalus Grey-headed Flying-fox ü ü
Pteropus scapulatus Little Red Flying-fox ü ü
Subfamily Macroglossus Macroglossus minimus Lesser Long-tongued
Macroglossinae Fruit Bat
Syconyteris Syconycteris australis Queensland Blossom Bat
Subfamily Nyctimene Nyctimene robinsoni Queensland Tube-nosed
Nyctimeninae Bat
USEFUL RESOURCES
CLICK I C O N T O A C C E S S W E B S I T E S W I T H I N F O R M A T I O N
ABLV BATS STATS
A six-monthly report prepared by the WHA Bat Health Focus Group
presenting information on ABLV testing in bats
FLYING FOX CAMP CENSUS
An interactive flying-fox web viewer that presents camp census data
collected via the National Flying-fox Monitoring Program
HORSE OWNER INFORMATION
Advice for horse owners who want to reduce the risk of Hendra virus
infection in their horses from the Qld government
NATIONAL HENDRA VIRUS RESEARCH
Compendium of findings from 20 projects under the
National Hendra Virus Research Program, 2016
BAT FAQ
Answers to questions about flying foxes and possible impacts on
human health from NSW Department of Health
Figure 1. Useful resources for further information. Underlined headings and icons are hyperlinked. If hyperlinks are not available, the following
URLs can be used: ABLV Bat Stats, https://wildlifehealthaustralia.com.au/ProgramsProjects/BatHealthFocusGroup.aspx; Flying fox camp
census data, https://www.environment.gov.au/webgis-framework/apps/ffc-wide/ffc-wide.jsf; Horse owner information, https://www.business.
qld.gov.au/industries/farms-fishing-forestry/agriculture/livestock/horses/hendra-virus/reducing-risk; National Hendra Virus Research, https://
www.agrifutures.com.au/wp-content/uploads/publications/16-001.pdf; Bat FAQ, https://www.health.nsw.gov.au/environment/factsheets/
Pages/flying-foxes-questions.aspx.
M I C R O B I O L O GY A U S T R A L I A M A R C H 2 0 2 0
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7
In Focus
(a) (b) (c) (d)
Hendra Nipah ABLV Rabies
glycoprotein of Hendra virus is very immunogenic and affords
Reservoir protection against HeV challenge in experimental infections17.
host Since the vaccine was released, no vaccinated horse has been
diagnosed with Hendra virus infection. Vaccination of horses
provides a public health and workplace health and safety benefit
Amplifying
host by reducing the risk of HeV transmission from horses to humans
and other susceptible animals. Whenever HeV infection is sus-
pected, even in vaccinated horses, appropriate biosecurity precau-
Human host
tions, including personal protective equipment (PPE), should be
used by all people in contact with sick horses.
Figure 2. Known transmission pathways that result in human infection:
the zoonotic transmission pathways of Hendra virus, Nipah virus, ABLV
Australian bat lyssavirus and rabies virus: (a) Hendra virus: Pteropus
bats are the reservoir host. Horses are the main spill-over host, and In 1996 a five-month-old female black flying fox was found under a
amplify the virus to very high titres, and succumb to clinical disease and
death. From horses the virus can spread to humans if appropriate PPE fig tree in Wollongbar, NSW, unable to fly. From this bat, a virus with
and other precautions are not taken when handling infected horses and close serologic and genetic relationships to members of the Lyssa-
their secretions. Two apparently healthy dogs became infected after
exposure to infected horses5 and experimentally dogs have been shown virus genus of the family Rhabdoviridae was isolated18. ABLV has
to be susceptible but unlikely to spread the virus6. (b) Nipah virus:
since been found in all four flying fox species and in one species of
Pteropus bats are the reservoir host. Horses can be spill-over hosts
and this was seen in one outbreak in the Philippines where humans microbat, the yellow-bellied sheath tailed bat13. It is assumed that all
became infected after eating infected horse meat7. The first outbreak of
NiV in 1998 had pigs as the main spill-over amplifying hosts and humans Australian bat species have the potential to carry and transmit
involved in pig farming and pig slaughter in Malaysia and Singapore ABLV. ABLV is transmitted to humans by bites or scratches from
became infected from pigs8. In Bangladesh and India there have been
almost annual outbreaks and most humans become infected by contact an infected bat.
with Nipah virus contaminated date palm sap9. Human to human
transmission is also seen10. While pteropus bats are suspected to be No laboratory tests are currently available to diagnose ABLV in
the source of human infection in the most recent outbreaks in Kerala,
India, the source of exposure has not been identified11. (c) ABLV: Direct humans before the onset of clinical disease. In the early stages of
contact with infected bats has been the cause of all outbreaks to date, disease, saliva and cerebrospinal fluid (CSF) can be tested by
with only humans and horses presenting with clinical signs of infection.
Horses have only been infected with a virus from microbats12. Two PCR. Antibody testing can also be performed on CSF. A positive
humans have been infected with virus from pteropus bats and one serum antibody test is diagnostic of lyssavirus infection provided
human has been infected from a microbat13. (d) Rabies: 99% of all
human rabies infections arise from contact with rabid dogs14. Humans the person has never been immunised against rabies and may assist
can also become infected directly from bats, or via another wildlife
in the diagnosis of lyssavirus clinical disease. Any negative test on a
reservoir; however, these modes of transmission account for less
than 1% of all human rabies cases. symptomatic person is not definitive, as viral shedding in body
secretions is intermittent and early tests may be negative for
recognition of its status as one of the most dangerous zoonotic
antibody. Therefore, repeat testing is often indicated.
agents. Safety precautions during field investigation and in the
laboratory are of paramount importance. Blood collected in an For post mortem testing in humans and animals including bats, the
EDTA tube, as well as tissue samples from lung, spleen and kidney standard diagnostic techniques include positive fluorescent anti-
can be tested by PCR, which is specific for Hendra virus. For the body test (FAT) and PCR on fresh brain smears, and PCR from
detection of antibodies to HeV in serum either a virus neutralisation tissues.
test (VNT) or an ELISA can be conducted.
ABLV infection has resulted in three human deaths, two adults and
There have been seven known human cases, four of which were
an eight-year-old child, in Queensland, Australia; 1996, 1998 and
fatal. Clinical presentations ranged from self-limiting influenza-like
201319. Transmission from flying foxes and an insectivorous micro-
illness, to severe pneumonia and encephalitis16. The typical incu-
bat were implicated, with all three cases displaying features of
bation period in humans was 5–21 days, although one person
encephalitic (furious) rabies before their demise. The incubation
experienced an initial aseptic meningitis, appeared to fully recover,
period is thought to mirror rabies (usually 3–8 weeks, but poten-
but succumbed to severe encephalitis 13 months later. All human
tially as short as a few days or as long as several years). Exposure
cases had high level exposure to infected horse secretions or
through wounds close to the central nervous system on the head
tissues16. Human to human HeV transmission has not been de-
and neck or richly innervated areas like the fingers, carry an
scribed to date, unlike the closely related Nipah virus where human
increased infection risk and may result in a shorter incubation
to human spread has been reported overseas10.
period. In furious rabies, prodromal symptoms may precede sen-
In 2012 a vaccine was released for use in horses, to prevent infection sorineural dysfunction, with progression to hyperactivity, aeropho-
with Hendra virus. This subunit vaccine based on the G bia and/or hydrophobia, followed by convulsions20. The clinical
8 MICROBIOLOGY AUSTRALIA MARCH 2020
*In Focus
course following symptom onset is usually rapid, almost invariably 10. Luby, S.P. et al. (2009) Recurrent zoonotic transmission of Nipah virus into
humans, Bangladesh, 2001-2007. Emerg. Infect. Dis. 15, 1229–1235. doi:10.3201/
progressing to death within a few days. eid1508.081237
11. Yadav, P.D. et al. (2019) Nipah virus sequences from humans and bats during
Regarding prevention, the key strategy is for untrained and unvac- Nipah outbreak, Kerala, India, 2018. Emerg. Infect. Dis. 25, 1003–1006.
cinated people to avoid handling bats. Public health authorities doi:10.3201/eid2505.181076
promote this message particularly during periods of high bat 12. Annand, E.J. and Reid, P.A. (2014) Clinical review of two fatal equine cases of
infection with the insectivorous bat strain of Australian bat lyssavirus. Aust. Vet. J.
activity, including fruiting periods, and heat stress events when
92, 324–332. doi:10.1111/avj.12227
bats and especially pups drop to the ground. Prompt post-exposure 13. Si, D. et al. (2016) Potential exposures to Australian bat lyssavirus notified in
vigorous wound cleaning, submission of the bat’s brain for ABLV Queensland, Australia, 2009–2014. PLoS Negl. Trop. Dis. 10, e0005227.
doi:10.1371/journal.pntd.0005227
testing (where possible), rabies vaccination and administration of
14. WHO (2013) Expert consultation on rabies second report. Geneva: WHO.
rabies immunoglobulin, are recommended following bat bites or
15. Halpin, K. et al. (2011) Pteropid bats are confirmed as the reservoir hosts of
scratches. Figure 1 provides a link to statistics on ABLV surveillance henipaviruses: a comprehensive experimental study of virus transmission. Am.
in Australia, as well as answers to questions about flying foxes and J. Trop. Med. Hyg. 85, 946–951. doi:10.4269/ajtmh.2011.10-0567
possible impacts on human health from NSW Department of 16. Playford, E.G. et al. (2010) Human Hendra virus encephalitis associated with
equine outbreak, Australia, 2008. Emerg. Infect. Dis. 16, 219–223. doi:10.3201/
Health.
eid1602.090552
17. Middleton, D. et al. (2014) Hendra virus vaccine, a one health approach to
Conclusions protecting horse, human, and environmental health. Emerg. Infect. Dis. 20,
372–379. doi:10.3201/eid2003.131159
ABLV and HeV can both cause an encephalitis syndrome in humans,
18. Fraser, G.C. et al. (1996) Encephalitis caused by a Lyssavirus in fruit bats in
sometimes with significant delay or recrudescence. Bats are the Australia. Emerg. Infect. Dis. 2(4), 327–331. doi:10.3201/eid0204.960408
reservoirs of these viruses and may well be implicated in transmis- 19. Young, M.K. and McCall, B.J. (2010) Potential exposure to Australian bat lyssavirus
sion of yet to be identified zoonotic pathogens. As the distribution in South East Queensland: what has changed in 12 years? Commun. Dis. Intell. 34,
334–338.
of these reservoir hosts changes, so too does the risk of spill-over
20. Merritt, T. et al. (2018) Australian bat lyssavirus. Aust. J. Gen. Pract 47, 93–96.
events that may involve humans. doi:10.31128/AFP-08-17-4314
Conflicts of interest
Biographies
The authors declare no conflicts of interest.
Kim Halpin leads the Pathology and Pathogenesis Group at the
Acknowledgements Australian Animal Health Laboratory (AAHL). She is a veterinary
graduate from the University of Queensland and has worked in
This research did not receive any specific funding.
research, diagnostic and commercial settings. Her focus has been
References on emerging infectious diseases. After completing her PhD on
1. Martin, G. et al. (2018) Climate change could increase the geographic extent Hendra virus, Kim did her postdoc at the Centres for Disease
of Hendra virus spillover risk. EcoHealth 15, 509–525. doi:10.1007/s10393-018- Control and Prevention in Atlanta, USA, working on a Nipah virus
1322-9
reverse genetics project. In 2003 she returned to Australia and
2. Halpin, K. et al. (2000) Isolation of Hendra virus from pteropid bats: a
natural reservoir of Hendra virus. J. Gen. Virol. 81, 1927–1932. doi:10.1099/ conducted henipavirus experimental transmission studies at
0022-1317-81-8-1927
AAHL. Kim is the OIE Reference Expert for Hendra virus and
3. Edson, D. et al. (2015) Routes of Hendra virus excretion in naturally-infected
flying-foxes: implications for viral transmission and spillover risk. PLoS One 10, Nipah virus.
e0140670. doi:10.1371/journal.pone.0140670
4. Halpin, K. et al. (2007) Emerging viruses: coming in on a wrinkled wing and a David Durrheim is Conjoint Professor of Public Health Medi-
prayer. Clin. Infect. Dis. 44, 711–717. doi:10.1086/511078
cine, University of Newcastle, and Director - Health Protection,
5. Kirkland, P.D. et al. (2015) Hendra virus infection in dog, Australia, 2013. Emerg.
Infect. Dis. 21, 2182–2185. doi:10.3201/eid2112.151324 Hunter New England Health. He is a Public Health Physician with
6. Middleton, D.J. et al. (2017) Experimental Hendra virus infection of dogs: virus an established track record in conducting research that has
replication, shedding and potential for transmission. Aust. Vet. J. 95, 10–18.
an operational focus and is translational in nature. Professor
doi:10.1111/avj.12552
7. Ching, P.K. et al. (2015) Outbreak of henipavirus infection, Philippines, 2014.
Durrheim is an outspoken advocate for equitable global access to
Emerg. Infect. Dis. 21, 328–331. doi:10.3201/eid2102.141433 effective public health measures, particularly immunisation. He
8. Chua, K.B. et al. (2000) Nipah virus: a recently emergent deadly paramyxovirus. has been instrumental in developing novel surveillance
Science 288, 1432–1435. doi:10.1126/science.288.5470.1432
systems to detect and facilitate response to emerging infectious
9. Rahman, M.A. et al. (2012) Date palm sap linked to Nipah virus outbreak in
Bangladesh, 2008. Vector Borne Zoonotic Dis. 12, 65–72. doi:10.1089/vbz.2011.0656 disease risks.
M I C R O B I O L O GY A U S T R A L I A M A R C H 2 0 2 0
*
9In Focus
Reaching the zero by 30 dog-mediated human
rabies goal
the risk of being bitten or scratched by infected animals especially
dogs, and appropriate treatment to follow if exposed3.
Dog-mediated rabies is an ancient, neurotropic viral disease that
should already have been eliminated globally given the tools to
control and prevent the disease have been available for decades12.
Andrea Britton More recently, following the development of the global framework
Burnet Institute to eliminate dog-mediated human rabies and leadership by the
Melbourne, Vic., Australia
Tel.: 0439 402 040 tripartite alliance (WHO, OIE and FAO) and Global Alliance for
Email: andrea.britton21@gmail.com Rabies Control (GARC), many countries are implementing a multi-
sector approach to progress rabies control and elimination. Prac-
tical inter-sectoral linking has been successful in the Philippines
with 15 island and localities becoming rabies free zones13. Addi-
It is unacceptable that as we advance into the 21st century
tionally, multi-stakeholder national rabies prevention and control
rabies is still a threat to humans and animals alike. Given
committees have supported implementation of national programs.
public health interventions that focus solely on disease pre-
vention in humans have no effect on the reduction of infec- Only Singapore remains rabies free within the ASEAN region
tion in the reservoir hosts, the most effective way to combat following the reintroduction of dog-mediated rabies to Malaysia
human rabies infection is to control the disease transmission during 2015 and 2017 from neighbouring endemic countries. Bali
by mass vaccination of the animal source, e.g. dogs and (incursion 2008) continues to progress control of dog-mediated
1 rabies despite challenges in maintaining high dog vaccination
wildlife . This short communication focuses on the global
strategic target to end human deaths from dog-mediated coverage across the island14,15. Responsible dog ownership has
rabies by 20302 in line with the Sustainable Development been highlighted as a key element of National Rabies Elimination
Goals by providing recent updates on World Health Organi- programmes in the OIE terrestrial code for rabies although the
3–5 contribution the control of dog populations plays in dog-mediated
zation (WHO) and OIE guidelines and recommendations
as well as highlighting Australian rabies research activities rabies elimination remains unknown.5
to prevent an incursion of rabies into the country.
International organisations and updates to
Dog-mediated rabies and the regional situation rabies guidelines
Dog-mediated rabies is the cause of ninety-nine percent of the The WHO Technical Report Series on Rabies No. 1012 released in
59 000 human rabies deaths annually with the greatest burden April 2018, provides new recommendations for pre- and post-
being in India and across Africa6. Australia has been free of the exposure prophylaxis, with reduced doses and timing in immuno-
dog rabies virus variant, although Australian Bat Lyssavirus is competent people3,16. Updates on rabies surveillance are included
maintained in native bats, and has spilled over to horses and and cross matched with the revised OIE code on infection with
7–9
people . Travellers to endemic dog-mediated rabies countries rabies virus5. Integrated bite case management is promoted with
should consider the risk of being exposed to the deadly virus and if communication processes developed between human and animal
necessary seek medical advice about pre-exposure prophylaxis health sectors leading to rapid responses and tracing of infected
10,11
rabies vaccination . This risk was sadly evident last year when animals and exposed people. Strengthening of human and animal
a 24-year-old Norwegian woman died from rabies having been health systems is necessary to deliver activities of national rabies
infected by a puppy she rescued while holidaying in the Philippines. elimination programs, although often these become less prioritised
This tragic case highlights the importance of rabies awareness for given competing health emergencies. The WHO and OIE are
travellers and communication of preventative measures to reduce supporting countries to assess and strengthen their One Health
10 10.1071/MA20004 MICROBIOLOGY AUSTRALIA MARCH 2020
*In Focus
capacity to deliver zoonotic control programs through Joint where necessary20. The requirements for inactivated and oral
External Evaluations (JEE) and IHR–PVS (International Health rabies vaccines have been revised and updated to be in line with
Regulations–Performance of Veterinary Services) National WHO, EMA and FDA provisions. The code chapter on rabies now
Bridging Workshops. distinguishes between a country and zone free from infection with
rabies virus and from dog-mediated rabies. There is also a new
The newly introduced progression of countries from endemic
Article on OIE-endorsed official control program for dog-mediated
rabies to elimination of dog-mediated rabies by implementation
rabies (Article 8.14.11) and for surveillance (Article 8.14.12)5.
of sustained mass dog vaccination programmes and validation and
verification of the absence of human deaths from rabies for Given no clinical signs or gross post mortem lesions are patho-
24 months was included to support countries reaching zero human gnomonic for rabies, laboratory diagnosis is necessary for suspect
deaths. Mexico recently obtained WHO recognition for eliminating case confirmation21. To assist neighbouring countries to improve
dog-transmitted human rabies as a public health issue, adding to the diagnosis of animal rabies the Australian government sup-
evidence that virus transmission can be stopped through mass dog ported the developed of an immunoperoxidase antigen detection
vaccination campaigns. test that could be used in provincial laboratories without the need
for expensive fluorescent microscopes22. The AAHL has also been
The OIE Terrestrial Code and Manual for Rabies have recently
building capacity regionally in phylogenetic analysis of rabies
been through cycles of revisions with the primary tests for rabies
viruses to better understand the molecular epidemiology of rabies
diagnosis being direct fluorescent antibody test, direct rapid
outbreaks which is especially important during the final stages of
immunohistochemistry test (dRIT) or lyssavirus polymerase
dog-mediated rabies elimination. Figure 1 illustrates the different
chain reaction assays (PCR) from appropriate brain samples of
wildlife associated lyssaviruses that may also be circulating in some
suspect rabid animals4,5. This testing currently occurs at the
countries and that can spill over into humans23.
Australian Animal Health Laboratories (AAHL) in Geelong for
any suspect cases in Australia. Rapid tests (lateral flow devices)
are being used in the field to assist in diagnosis although these
Australian rabies research building surveillance
have variable sensitivity and specificity17–19. Additionally, oral capacity
vaccination of dogs is now considered a useful supplementary With dog rabies spreading into eastern Indonesian islands, and only
measure to increase vaccination coverage in the dog population 300 km from northern Australia shores, pre-border biosecurity and
RABV
ARAV
EBLV-2 KHUV
100
ABLV
IRKV 81
100 86
EBLV-1
79 100
LBV
100
DUVV 100
100
100
MOKV
0.1 C
A
D B
SHBV
I
II
III WCBV
Figure 1. Phylogenetic analysis of lyssavirus isolates with animals found naturally infected circled. Roman numerals refer to antigenic phylogroups23.
M I C R O B I O L O GY A U S T R A L I A M A R C H 2 0 2 0
*
11In Focus
active surveillance programs are essential to prevent or rapidly
identify an incursion24. Risk assessments have focused on estimat-
ing the probability of a rabies-infected dog on fishing or recreational
boats entering illegally into northern Australian remote indigenous
communities and Papua New Guinea25,26. Large numbers of owned
dogs are free-roaming in these remote communities therefore
research has investigated the roaming behaviour of these domestic
dogs (using GPS tracking collars) to better understand interactions
to enable modelling of a rabies incursion and interventions27–29.
More recent modelling assessed targeted rabies vaccination strat- Why are we worried?
egies in different dog populations associated with roaming behav-
iour30. Currently, the optimal rabies population vaccination
coverage is seventy percent to achieve herd immunity and prevent Figure 2. Diagram from Northern Australia Quarantine Strategy
rabies risk pathways awareness video showing possible entry points
virus transmission. The modelling of targeted rabies vaccination of infected rabid dogs on illegal fishing or recreational boats34.
strategies based on the roaming behaviour of the dogs (directly
associated with risk of rabies transmission) has indicated that lower
vaccination coverage may be feasible which is beneficial when infected rabid dogs on illegal fishing or recreational boats. The
rabies vaccines are in limited supply as well as being more cost- video also promotes awareness about telling a ranger or biosecurity
30
effective . officer about any dogs from boats that are behaving strangely
(hypersalivation, paralysis, lethargy, abnormal aggression, abnor-
mal vocalisation). Data on the incidence of dog bites is also
AUSVETPLAN rabies and Australian bat important to monitor.
lyssavirus
Australia’s national rabies and Australian bat lyssavirus (ABLV) Conclusion
preparedness and emergency response plan (AUSVETPLAN)31 are The correlating updates on rabies guidelines by WHO and OIE will
currently under review with a joint technical workshop recom- greatly support the zero by 30 goal and prevention of rabies
mending the updated manuals be combined. This is because an incursion. Australia’s pre-border biosecurity has successfully facil-
emergency response following an outbreak would be strategically itated continued freedom from dog-mediated rabies. Ongoing
similar and require a coordinated response between the public research has built capacity in rabies surveillance and risk assess-
human and animal health agencies. Given the risk of a rabies ment and in additional has supported our neighbours in dog-
incursion in northern Australian indigenous communities and the mediated rabies control and, hopefully, eventual elimination.
cultural and social importance of dogs and dingo hybrids in these
communities, it is recommended that community appropriate Conflicts of interest
strategies for biosecurity responses to an incursion be developed The author declares no conflicts of interest.
and incorporated into these manuals32.
Reporting of potential rabies cases in these remote indigenous
Acknowledgements
communities requires awareness of the disease and participation in This research did not receive any specific funding.
this surveillance, which in-turn requires communities to perceive a
need for this surveillance33. Qualitative studies have explored References
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Did you know?
Point of care testing in Australia began during the first outbreaks of plague in Sydney (1900 and 1902) and
Brisbane (1902).
Medical officers called to visit suspected patients equipped with a kit containing syringes, platinum wire loops, culture
tubes, spirit lamp and glass slides so that cultures and smears of pus and blood could be made at the bedside.
Sydney’s waterfront, wharves, buildings and nearby houses were filthy and rat infested. Large areas were quarantined,
rat catchers set to work and buildings were demolished. Infected persons and healthy people living in the same house
were transferred to the Quarantine Station at North Head, now known as Q station and well worth a visit if you are
visiting Sydney.
M I C R O B I O L O GY A U S T R A L I A M A R C H 2 0 2 0
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