Australian bat lyssavirus

Last updated

Australian bat lyssavirus
CSIRO ScienceImage 1977 Bat Lyssavirus.jpg
Colored transmission electron micrograph of Australian bat lyssavirus. The bullet-like objects are the virions, and some of them are budding off from a cell.
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Negarnaviricota
Class: Monjiviricetes
Order: Mononegavirales
Family: Rhabdoviridae
Genus: Lyssavirus
Species:
Australian bat lyssavirus

Australian bat lyssavirus (ABLV), originally named Pteropid lyssavirus (PLV), is a enzootic virus closely related to the rabies virus. It was first identified in a 5-month-old juvenile black flying fox ( Pteropus alecto ) collected near Ballina in northern New South Wales, Australia, in January 1995 during a national surveillance program for the recently identified Hendra virus. [1] ABLV is the seventh member of the genus Lyssavirus (which includes Rabies virus ) and the only Lyssavirus member present in Australia. ABLV has been categorized to the Phylogroup I of the Lyssaviruses. [2]

Contents

Virology

Molecular structure

The Australian bat lyssavirus (ABVL) shares many structural characteristics with the other Lyssaviruses, despite being genetically and serologically distinct from the others. [2] Visually, ABLV is a bullet shaped virus. Molecularly, ABVL is an enveloped, negative-sense, single-stranded RNA virus. The (-)ssRNA genome is relatively small, containing 12kilobases of genetic material and encoding five viral proteins. The five viral proteins, their symbol, and their functional roles are:

Viral Structure of a Lyssavirus Particle - with the five viral proteins and genome labeled. Vsv virion.jpg
Viral Structure of a Lyssavirus Particle - with the five viral proteins and genome labeled.
SymbolNameStructureFunction
NNucleoproteinInteracts with genome, P, and L to form the ribonucleoprotein complexEncapsulates the RNA genome, making it available for transcription and genome replication
PPhosphoproteinCofactor for LRegulatory functions for viral replication

Helps virus evade host immune system - suppressing host immunity

MMatrixPhysically connecting the viral capsid to the host derived membrane

Interacts with P and L

Aids in viral assembly, coordinates translation and genome replication, and directs budding
GGlycoproteinTrimeric surface protein spikes, associated with M and extends through the host cell derived membrane envelopeUtilized for host cell entry with receptor-mediated endocytosis
LRNA dependent RNA polymeraseEnzyme for transcription (produce mRNA from genome) and viral genome replication

[3] [4]

Viral entry mechanism and intracellular trafficking

ABLV has a similar entry mechanism to other rabies viruses, utilizing receptor-mediated endocytosis by the host cells. The glycoprotein (G) is a trimeric spike protein that extends through the virus's envelope and can interact with surface receptors of host cells. While the specific receptors remain mostly unknown at this time, it is thought that ABLV enters the nervous system of host through the neuromuscular junction of the peripheral nervous system. Additionally, it is believed that the spike protein either binds to a highly specific host receptor or uses a co-receptor in lipid rafts. [3] Some of the proposed receptors include nicotinic acetylcholine receptor (nAchR), p75 neurotrophin receptor (p75NTR), and neuronal cell adhesion molecule (NCAM). [5]

Viral Entry Pathway of Lyssavirus Viruses-06-00909-g002-1024.webp
Viral Entry Pathway of Lyssavirus

After attaching to the host cell surface, ABLV uses a clathrin-dynamin-dependent pathway to invaginate the host membrane and pinch off a vesicle. Actin polymerization at the site of invagination is also required for successful viral entry. The virus is endocytosed fully, unenveloped. The vesicle fuses with a lysosome, causing the pH within the infected vesicle to drop. The lowering of pH in the early-endosome causes a conformational change in the spike protein G. This allows the viral envelope to fuse with the endosome, releasing the nucleocapsid into the cytoplasm of the host cell. [3]

Prevalence

Host reservoir and susceptible species

Bats, both flying foxes and insectivorous bats, are the only known host reservoir for ABLV. The known species of bat reservoirs are the Black Flying Fox (Pteropus alecto), the Grey-headed Flying Fox (P. poliocephalus), the Spectacled Flying Fox (P. conscpicullatus), the Little Red Flying Fox (P. scapulatus), and the Yellow-bellied Sheathtail Bat (Saccolaimus flaviventris). [5] These species are distributed throughout the Australian continent, and ABLV has only been serologically and phylogenetically in Australia. [6] : 251  It is estimated that less than 1% of healthy bats are ABLV carriers. As for sick or injured bats, it is estimated that 5-10% have been infected, detected with fluorescent antibody testing. [5]

As for other species that are susceptible to ABLV infection, human and horse cases have been reported since 1996 and 2013, respectively. No other terrestrial animals have been reported to be infected with ABLV, despite known exposure to infected bats. However, recent studies have found that the ABLV receptor for host cell entry is conserved amongst a variety of mammals, including but not limited to small rodents, monkeys, and rabbits. [5]

Displays the distribution of ABLV based on the known reservoir hosts Distribution-of-ABLV-host-reservoir-species-Adapted-from-12-14.png
Displays the distribution of ABLV based on the known reservoir hosts

Geographical distribution

As of now, ABLV has only been isolated and reported in Australia. The distribution of ABLV across the Australian continent is based on the ecological distribution of the bat reservoirs. From the four flying fox species identified as host reservoirs, ABLV is present in areas of Western Australia, North Territory, Queensland, New South Wales, and Victoria. From the Yellow-bellied Sheathtail Bat, ABLV is present throughout mainland Australia. [5]

Human health

Zoonotic incidences

The first case occurred in November 1996, when an animal caregiver in Rockhampton sustained several scratches from fruit bats she was working with. She reported to the hospital four to five weeks later for shoulder pain, dizziness, vomiting, headache, fever, and chills. While hospitalized, her condition rapidly deteriorated, with slurred speech, diplopia (double-vision), dysphagia (difficulty swallowing), and progressive weakness in her limbs. From cerebrospinal fluid samples, no organisms were found with microscopy or culturing, despite elevated white blood cell levels. She was treated with several broad spectrum antibiotics with no improvement. An electroencephalogram was performed and found diffuse encephalitis. She eventually fell into a depressed conscious state, with a single incidence of extreme agitation. By her 11th day of hospitalization, she was fully ventilation dependent, nonresponsive, and hyperthermic. She died 20 days after her initial admittance. ABLV was identified from brain tissue by polymerase chain reaction and immunohistochemistry. [5] [7] [8]

The second case began in August 1996, 37 year old Monique Todhunter from Mackay was bitten on the finger by a flying fox at a birthday party, while attempting to remove it from a child on whom it had landed. Six months later, following heightened public attention from the first ABLV death, she consulted a general practitioner regarding testing for the virus. Post-exposure prophylaxis was advised, but for an unknown reason she declined the treatment. After a 27-month incubation, a rabies-like illness developed in November of 1998. She came in with symptoms of fever, vomiting, pain in her shoulder, dysphagia, and muscle spasms. Her condition worsened after hospital admission, as her dysphagia increased, her muscle spasms became more pronounced and frequent, and she became increasingly agitated. She became ventilation dependent and unable to communicate due to full paralysis. On the day the woman was hospitalized, cerebrospinal fluid, serum, and saliva were submitted for testing. [9] On the fourth day of her hospital admission, these tests were returned with results of probable ABLV infection. ABLV infection was confirmed by PCR on the 8th day of hospitalization. She died 19 days after the onset of illness. Postmortem tests were all strongly positive for ABLV. [5] [9] A notable feature of this case is that the patient underwent a 27 month incubation period; in comparison, the majority of rabies cases have an incubation period of 20-90 days, with 95% of cases exhibiting symptoms within a year of exposure to the virus. [9]

The third, and most recent, case occurred in December of 2012, when an eight-year-old boy was scratched by a bat in north Queensland. He became ill eight weeks later, showing symptoms including fever, anorexia, and abdominal pain. His condition worsened through his hospitalization, with abnormal and aggressive bouts between normal behavior and intense muscle spasms. He repeatedly needed to be extubated and sedated due to his spasms. The hospital performed several tests through his stay, including sending cerebrospinal fluid and blood samples off for testing, taking computed tomography images of his chest and abdomen, and performing neuroimaging (MRIs, electroencephalography's). Initially, tests for the ABLV antigens were negative, but repeated testing 12 days into his hospitalization provided positive results. The child died 28 days after the onset of symptoms on February 22, 2013. [5] [10] [11]

Pathology and pathogenesis of ABLV in humans

ABLV (and the other Lyssaviruses) present similarly to the traditional encephalitic rabies virus (RABV) in humans. The symptoms first are flu-like with fevers, headaches, and fatigue. [12] The symptoms progress with paralysis, delirium, convulsions, and death. [12] There are no known human survivors of ABLV infection after symptoms have manifested. [5]

The pathogenesis of ABLV is still widely unknown and still being studied. The virus initially infects the host through the peripheral nervous system following a bite or scratch from an infected animal. [5]

For the three reported ABLV cases in humans, the incubation period ranged from a few weeks to almost two years. [5]

Current treatments for ABLV

Due to its difficulty in diagnosing, low number of reported cases, and relative novelty as an endemic virus, there are no successful treatment plans once the symptoms have begun. As previously stated, all intervention methods used on the three human cases of ABLV were not curative and all three cases resulted in fatality.

However, it is highly recommended by physicians to receive the RABV post-exposure prophylaxis (PEP) protocol immediately after potential lyssavirus exposure (i.e.. exposure/interaction with bats). Additionally, the incident should be reported to the relevant public health unit. Currently, the PEP protocol involves thoroughly cleaning the wound and surrounding tissue, administration of the rabies vaccine, and administration of rabies immunoglobulin (RIG). [13] [14] Currently, there are two effective variations of RIGs used in PEP protocol, human RIG (HRIG) and equine RIG (ERIG). Drawbacks for HRIG are that there are limited supplies and the cost of production is high. HRIG is overall inaccessible for the general population. Drawbacks for ERIG are potential immunogenicity, which is when the immune system recognizes the RIG as foreign and causes an immune reaction. [15] In a 2021 study performed by Weir, Coggins, et.al., a new treatment method was proposed that used human monoclonal antibodies over RIGs. They identified two (A6 and F11) that recognized the G protein of lyssaviruses in phylogroup I (including ABLV) and completely neutralized the virus. They also proposed it as a potential diagnostic tool, in which there are only limited methods with PCR and are late into the symptomatic phase to positively identify ABLV. [13]

Prevention

Rabies vaccine and immunoglobulin are effective in prophylactic and therapeutic protection from ABLV infection. Since the emergence of the virus, rabies vaccine is administered to individuals with a heightened risk of exposure, and vaccine and immunoglobulin are provided for post-exposure treatment.

The public health units in Australia advise that the population avoid and limit their interactions and physical contact with bats as much as possible. ABLV is one of four zoonotic viruses discovered in pteropid bats since 1994, the others being Hendra virus, Nipah virus, and Menangle virus. Of these, ABLV is the only virus known to be transmissible to humans directly from bats without an intermediate host. Thus education and awareness in the general population is a must. If a bat is found and/or appears injured, one should avoid contact with it and instead call local pest and animal control to appropriately remove the bat. [16] [17]

Non-human health

ABLV has also been reported to have the ability to transfer to horses. Currently, this is the only other known susceptible species.

ABLV was confirmed in two horses on Queensland's Darling Downs in May 2013. Both horses were euthanized when their condition deteriorated despite treatment and the attending veterinarian performed a post mortem examination obtaining samples that allowed for the laboratory diagnosis. The property was then quarantined. Three dogs and the four horses in closest contact received post exposure prophylaxis, as did all nine in-contact people. The virus was isolated and identified as the insectivorous bat strain. These cases have prompted reconsideration of the potential spillover of ABLV into domestic animal species. Veterinarians are urged to consider ABLV as a differential diagnosis in cases of progressive generalized neurological disease. [5] [18]

See also

Related Research Articles

<i>Rhabdoviridae</i> Family of viruses in the order Mononegavirales

Rhabdoviridae is a family of negative-strand RNA viruses in the order Mononegavirales. Vertebrates, invertebrates, plants, fungi and protozoans serve as natural hosts. Diseases associated with member viruses include rabies encephalitis caused by the rabies virus, and flu-like symptoms in humans caused by vesiculoviruses. The name is derived from Ancient Greek rhabdos, meaning rod, referring to the shape of the viral particles. The family has 40 genera, most assigned to three subfamilies.

<i>Bornaviridae</i> Family of viruses

Bornaviridae is a family of negative-strand RNA viruses in the order Mononegavirales. Horses, sheep, cattle, rodents, birds, reptiles, and humans serve as natural hosts. Diseases associated with bornaviruses include Borna disease, a fatal neurologic disease of mammals restricted to central Europe; and proventricular dilatation disease (PDD) in birds. Bornaviruses may cause encephalitis in mammals like horses or sheep. The family includes 11 species assigned to three genera.

<i>Lyssavirus</i> Genus of viruses

Lyssavirus is a genus of RNA viruses in the family Rhabdoviridae, order Mononegavirales. Mammals, including humans, can serve as natural hosts. The genus Lyssavirus includes the rabies virus traditionally associated with the disease of the same name.

<span class="mw-page-title-main">Rabies virus</span> Species of virus

Rabies virus, scientific name Rabies lyssavirus, is a neurotropic virus that causes rabies in animals, including humans. Rabies transmission can occur through the saliva of animals and less commonly through contact with human saliva. Rabies lyssavirus, like many rhabdoviruses, has an extremely wide host range. In the wild it has been found infecting many mammalian species, while in the laboratory it has been found that birds can be infected, as well as cell cultures from mammals, birds, reptiles and insects. Rabies is reported in more than 150 countries and on all continents except Antarctica. The main burden of disease is reported in Asia and Africa, but some cases have been reported also in Europe in the past 10 years, especially in returning travellers.

Menangle pararubulavirus, also called Menangle virus, is a virus that infects pigs, humans and bats.

<i>Nipah virus</i> Species of virus

Nipah virus is a bat-borne, zoonotic virus that causes Nipah virus infection in humans and other animals, a disease with a very high mortality rate (40-75%). Numerous disease outbreaks caused by Nipah virus have occurred in South East Africa and Southeast Asia. Nipah virus belongs to the genus Henipavirus along with the Hendra virus, which has also caused disease outbreaks.

Lymphocytic choriomeningitis (LCM) is a rodent-borne viral infectious disease that presents as aseptic meningitis, encephalitis or meningoencephalitis. Its causative agent is lymphocytic choriomeningitis mammarenavirus (LCMV), a member of the family Arenaviridae. The name was coined by Charles Armstrong in 1934.

Mokola lyssavirus, commonly called Mokola virus (MOKV), is an RNA virus related to rabies virus that has been sporadically isolated from mammals across sub-Saharan Africa. The majority of isolates have come from domestic cats exhibiting symptoms characteristically associated to rabies virus infection.

Duvenhage lyssavirus (DUVV) is a member of the genus Lyssavirus, which also contains the rabies virus. The virus was discovered in 1970, when a South African farmer died of a rabies-like encephalitic illness, after being bitten by a bat. In 2006, Duvenhage virus killed a second person, when a man was scratched by a bat in North West Province, South Africa, 80 km from the 1970 infection. He developed a rabies-like illness 27 days after the bat encounter, and died 14 days after the onset of illness. A 34-year-old woman who died in Amsterdam on December 8, 2007, was the third recorded fatality. She had been scratched on the nose by a small bat while travelling through Kenya in October 2007, and was admitted to hospital four weeks later with rabies-like symptoms.

Visna-maedi virus from the genus Lentivirus and subfamily Orthoretrovirinae, is a retrovirus that causes encephalitis and chronic pneumonitis in sheep. It is known as visna when found in the brain, and maedi when infecting the lungs. Lifelong, persistent infections in sheep occur in the lungs, lymph nodes, spleen, joints, central nervous system, and mammary glands; The condition is sometimes known as ovine progressive pneumonia (OPP), particularly in the United States, or Montana sheep disease. White blood cells of the monocyte/macrophage lineage are the main target of the virus.

<span class="mw-page-title-main">Rabies</span> Deadly viral disease, transmitted through animals

Rabies is a viral disease that causes encephalitis in humans and other mammals. It was historically referred to as hydrophobia due to the symptom of panic when presented with liquids to drink. Early symptoms can include fever and abnormal sensations at the site of exposure. These symptoms are followed by one or more of the following symptoms: nausea, vomiting, violent movements, uncontrolled excitement, fear of water, an inability to move parts of the body, confusion, and loss of consciousness. Once symptoms appear, the result is virtually always death, regardless of treatment. The time period between contracting the disease and the start of symptoms is usually one to three months but can vary from less than one week to more than one year. The time depends on the distance the virus must travel along peripheral nerves to reach the central nervous system.

The central nervous system (CNS) controls most of the functions of the body and mind. It comprises the brain, spinal cord and the nerve fibers that branch off to all parts of the body. The CNS viral diseases are caused by viruses that attack the CNS. Existing and emerging viral CNS infections are major sources of human morbidity and mortality.

<span class="mw-page-title-main">Influenza</span> Infectious disease

Influenza, commonly known as "the flu" or just "flu", is an infectious disease caused by influenza viruses. Symptoms range from mild to severe and often include fever, runny nose, sore throat, muscle pain, headache, coughing, and fatigue. These symptoms begin from one to four days after exposure to the virus and last for about 2–8 days. Diarrhea and vomiting can occur, particularly in children. Influenza may progress to pneumonia, which can be caused by the virus or by a subsequent bacterial infection. Other complications of infection include acute respiratory distress syndrome, meningitis, encephalitis, and worsening of pre-existing health problems such as asthma and cardiovascular disease.

Almost all human deaths caused by rabies occur in Asia and Africa.

<span class="mw-page-title-main">Rabies in animals</span> Deadly zoonotic disease

In animals, rabies is a viral zoonotic neuroinvasive disease which causes inflammation in the brain and is usually fatal. Rabies, caused by the rabies virus, primarily infects mammals. In the laboratory it has been found that birds can be infected, as well as cell cultures from birds, reptiles and insects. The brains of animals with rabies deteriorate. As a result, they tend to behave bizarrely and often aggressively, increasing the chances that they will bite another animal or a person and transmit the disease.

<span class="mw-page-title-main">Bat virome</span> Group of viruses associated with bats

The bat virome is the group of viruses associated with bats. Bats host a diverse array of viruses, including all seven types described by the Baltimore classification system: (I) double-stranded DNA viruses; (II) single-stranded DNA viruses; (III) double-stranded RNA viruses; (IV) positive-sense single-stranded RNA viruses; (V) negative-sense single-stranded RNA viruses; (VI) positive-sense single-stranded RNA viruses that replicate through a DNA intermediate; and (VII) double-stranded DNA viruses that replicate through a single-stranded RNA intermediate. The greatest share of bat-associated viruses identified as of 2020 are of type IV, in the family Coronaviridae.

European bat 1 lyssavirus(EBLV-1) is one of three rabies virus-like agents of the genus Lyssavirus found in serotine bats in Spain. Strains of EBLV-1 have been identified as EBLV-1a and EBLV-1b. EBLV-1a was isolated from bats found in the Netherlands and Russia, while EBLV-1b was found in bats in France, the Netherlands and Iberia. E. isabellinus bats are the EBLV-1b reservoir in the Iberian Peninsula. Between 1977 and 2010, 959 bat rabies cases of EBLV-1 were reported to the World Health Organization (WHO) Rabies Bulletin.

<span class="mw-page-title-main">Nipah virus infection</span> Disease caused by Nipah virus

A Nipah virus infection is a viral infection caused by the Nipah virus. Symptoms from infection vary from none to fever, cough, headache, shortness of breath, and confusion. This may worsen into a coma over a day or two, and 50 to 75% of those infected die. Complications can include inflammation of the brain and seizures following recovery.

West Caucasian bat lyssavirus (WCBL) is a member of genus Lyssavirus, family Rhabdoviridae and order Mononegavirales. This virus was first isolated from Miniopterus schreibersii, in the western Caucasus Mountains of southeastern Europe in 2002. WCBL is the most divergent form of Lyssavirus, and is found in Miniopterus bats (insectivorous), Rousettus aegyptiacus, and Eidolon helvum. The latter two are both fruit bats. The virus is fragile as it can be inactivated by UV light and chemicals, such as ether, chloroform, and bleach. WCBL has not been known to infect humans thus far.

Ghanaian bat henipavirus (also known Kumasi virus belongs to the genus Henipavirus in the family Paramyxoviridae. Human infections are caused by zoonotic events where the virus crosses over from another animal species. Therefore, humans are not the innate host for this virus family but instead become infected by peripheral viral reservoirs such as bats and other carriers of the virus. When these virus are spread to humans through zoonotic events they have been found to be one of the most deadly viruses with the capability to infect humans, with mortality rates between 50 and 100%. Therefore, these viruses have been classified as a biosafety level four virus with regards to its pathogenesis when it infects humans.

References

  1. ↑
    • Speare R, Skerratt L, Foster R, Berger L, Hooper P, Lunt R, et al. (May 1997). "Australian bat lyssavirus infection in three fruit bats from north Queensland" (PDF). Communicable Diseases Intelligence. 21 (9): 117–120. PMID   9145563. Archived (PDF) from the original on 5 June 2011. Retrieved 26 May 2011.
  2. 1 2 Weir DL, Coggins SA, Vu BK, Coertse J, Yan L, Smith IL, et al. (March 2021). "Isolation and Characterization of Cross-Reactive Human Monoclonal Antibodies That Potently Neutralize Australian Bat Lyssavirus Variants and Other Phylogroup 1 Lyssaviruses". Viruses. 13 (3): 391. doi: 10.3390/v13030391 . PMC   8001737 . PMID   33804519.
  3. 1 2 3 Weir DL, Annand EJ, Reid PA, Broder CC (February 2014). "Recent observations on Australian bat lyssavirus tropism and viral entry". Viruses. 6 (2): 909–926. doi: 10.3390/v6020909 . PMC   3939488 . PMID   24556791.
  4. ↑ Zandi F, Goshadrou F, Meyfour A, Vaziri B (July 2021). "Rabies Infection: An Overview of Lyssavirus-Host Protein Interactions". Iranian Biomedical Journal. 25 (4): 226–242. doi:10.52547/ibj.25.4.226. PMC   8334389 . PMID   34217155.
  5. 1 2 3 4 5 6 7 8 9 10 11 12 Weir DL, Annand EJ, Reid PA, Broder CC (February 2014). "Recent observations on Australian bat lyssavirus tropism and viral entry". Viruses. 6 (2): 909–926. doi: 10.3390/v6020909 . PMC   3939488 . PMID   24556791.
  6. ↑
  7. ↑ Allworth A, Murray K, Morgan J (1996). "A human case of encephalitis due to a lyssavirus recently identified in fruit bats" (PDF). Commun. Dis. Intellig. 20: 504 – via Google Scholar.
  8. ↑ Samaratunga H, Searle JW, Hudson N (August 1998). "Non-rabies Lyssavirus human encephalitis from fruit bats: Australian bat Lyssavirus (pteropid Lyssavirus) infection". Neuropathology and Applied Neurobiology. 24 (4): 331–335. doi:10.1046/j.1365-2990.1998.00129.x. PMID   9775399. S2CID   22171516.
  9. 1 2 3 Hanna JN, Carney IK, Smith GA, Tannenberg AE, Deverill JE, Botha JA, et al. (June 2000). "Australian bat lyssavirus infection: a second human case, with a long incubation period". The Medical Journal of Australia. 172 (12): 597–599. doi:10.5694/j.1326-5377.2000.tb124126.x. PMID   10914106. S2CID   32907529. Archived from the original on 24 July 2008. Retrieved 26 July 2008.
  10. ↑ "Child dies of bat virus in Brisbane hospital". Adelaidenow. Retrieved 22 February 2013.[ permanent dead link ]
  11. ↑ Francis JR, Nourse C, Vaska VL, Calvert S, Northill JA, McCall B, Mattke AC (April 2014). "Australian Bat Lyssavirus in a child: the first reported case". Pediatrics. 133 (4): e1063–e1067. doi:10.1542/peds.2013-1782. PMID   24590754. S2CID   294699.
  12. 1 2 "Rabies and Australian bat lyssavirus infection fact sheet - Fact sheets". www.health.nsw.gov.au. Retrieved 15 February 2024.
  13. 1 2 Weir DL, Coggins SA, Vu BK, Coertse J, Yan L, Smith IL, et al. (March 2021). "Isolation and Characterization of Cross-Reactive Human Monoclonal Antibodies That Potently Neutralize Australian Bat Lyssavirus Variants and Other Phylogroup 1 Lyssaviruses". Viruses. 13 (3): 391. doi: 10.3390/v13030391 . PMC   8001737 . PMID   33804519.
  14. ↑ Francis JR, McCall BJ, Hutchinson P, Powell J, Vaska VL, Nourse C (December 2014). "Australian bat lyssavirus: implications for public health". The Medical Journal of Australia. 201 (11): 647–649. doi:10.5694/mja13.00261. PMID   25495308. S2CID   27818638.
  15. ↑ "Immunogenicity - an overview | ScienceDirect Topics". www.sciencedirect.com. Retrieved 1 November 2023.
  16. ↑ "Don't handle bats, Vic health chief warns". The Sydney Morning Herald. 25 May 2011. Archived from the original on 28 May 2011. Retrieved 25 May 2011.
  17. ↑ Devine M (17 July 2011). "It's batty not to cleanse this scourge". Herald Sun . Archived from the original on 30 December 2012. Retrieved 22 December 2011.
  18. ↑ Shinwari MW, Annand EJ, Driver L, Warrilow D, Harrower B, Allcock RJ, et al. (October 2014). "Australian bat lyssavirus infection in two horses". Veterinary Microbiology. 173 (3–4): 224–231. doi:10.1016/j.vetmic.2014.07.029. PMID   25195190.

Additional reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.