PATHOLOGY OF BATS Cheryl Sangster, DVM, MVSc, Diplomate

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PATHOLOGY OF BATS
Cheryl Sangster, DVM, MVSc, Diplomate ACVP
Taronga Conservation Society Australia
Taronga Zoo, Bradleys Head Road
Mosman NSW 2088
Bats are a highly diverse mammalian order, coming second only to rodents for number of species.
The order is traditionally divided into two suborders, the Megachiroptera which includes the highly
visual, non-echolocating fruit bats and the Microchiroptera which includes the smaller, echo-locating
species. Previously, theories had been put forth suggesting that Chiroptera was not a monophyletic
order, but rather that the megachiropterans were more closely related to primates. However,
molecular technology has now put this theory to rest, solidly placing megabats and microbats within
the same order.
The suborder Megachiroptera includes one family, Pteropodidae, which within Australia is
represented by five genera, Pteropus and Dobsonia (flying foxes), Nyctimene (tube-nosed fruit bats)
and Syconycteris and Macroglossus (blossom bats). The most highly recognised species are the
mainland flying foxes, the grey-headed (Pteropus poliocephalus), the black (Pteropus alecto), the
spectacled (Pteropus conspicillatus) and the little red (Pteropus scapulatus). Numerous species of
Microchiroptera are present in Australia, falling into the families Emballonuridae, Megadermatidae,
Rhinolophidae (horseshoe bats), Hipposideridae (also commonly referred to as horseshoe bats),
Vespertilionidae and Mollosidae.
Fauna of Australia, Australian Government DEWHA website,
http://www.environment.gov.au/biodiversity/abrs/publications/fauna-of-australia/fauna-1b.html.
Accessed June 2008.
Hall L, Richards G. 2000. Flying Foxes, Fruit and Blossom bats of Australia. Sydney: UNSW
Press. Pp 135.
Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ. 2005. A molecular
phylogeny for bats illuminated biogeography and the fossil record. Science 307: 580-584.
THE NEUROLOGICAL BAT
A common history accompanying bats presented to Australian pathology services will include a
combination of neurological signs. These can include musculoskeletal signs such as weakness,
paresis and paralysis, which may be ascending, gastrointestinal signs such anorexia and possibly
diarrhoea, and abnormal behaviour including aggression, obtundence, failure to attempt escape and
abnormal vocalisation. Differential diagnoses for these animals include, but may not be limited to the
following:
Australian bat lyssavirus (ABLV)
Angiostrongylus cantonensis
Lead poisoning
Trauma
Tick paralysis (Ixodes holocyclus)
Toxoplasma gondii
Other neurological disease (e.g. bacterial meningitis)
Since the identification of Australian bat lyssavirus in the early 1990’s, it has become particularly
important to approach these cases with caution and diligence. In cases of human exposure (bites
and scratches) ruling out ABLV is paramount. Co-occurrence of ABLV with other neurological related
aetiologies has been reported (e.g. lead poisoning), highlighting the importance of considering this
pathogen in the face of histological and ancillary test results suggestive of other neurological
diseases. See the following text for complete descriptions of these diseases.
BAT PATHOLOGY BY AETIOLOGIC CATEGORY
VIRAL DISEASES
Disease name
Australian bat lyssavirus
Agent
Australian bat lyssavirus, family Rhabdoviridae, genus Lyssavirus
Significance
Fatal disease affecting all 4 common species of flying foxes, at least one microchiropteran bat, the
yellow-bellied sheath-tailed bat (Saccolaimus flaviventris) and humans. No domestic animals have
been found to be affected to date. This disease is nationally notifiable within Australia
Clinical Signs
Muscle weakness, paresis or paralysis
Aggression, obtundence or a failure to attempt escape
Abnormal vocalisation
Inability to fly
Gross Pathology
None
Microscopic Pathology
May be none on H&E
Nonsuppurative meningoencephalomyelitis in brain and cervical spinal cord, with neuronal necrosis,
gliosis and perivascular cuffing
Nonsuppurative ganglioneuritis of the Gasserian and spinal ganglia
Nonsuppurative sialoadenitis (rare)
Eosinophilic intranuclear inclusions bodies in neurons (Negri bodies, rarely present)
Intracytoplasmic vacuolation of neurons
Differential Diagnoses
Angiostrongylus cantonensis
Lead poisoning
Trauma
Tick paralysis (Ixodes holocyclus)
Toxoplasma gondii
Other neurological disease (e.g. bacterial meningitis)
Diagnostic Pathway
Suspect ABLV based on history of abnormal behaviour and/or neurological deficits.
Absence of microscopic changes does not rule out ABLV.
Submit minimum of half brain frozen or chilled to 4°C to reference lab as per instruction of state
authority.
Confirmation based on fluorescent antibody test, PCR and/or virus isolation on fresh/frozen brain or
immunohistochemistry on fixed brain.
Other nervous tissues, saliva, salivary gland or cerebrospinal fluid can be used for ancillary testing,
but results are less reliable.
Positive identification of an alternative aetiology for neurological signs does not rule out ABLV
(e.g. lead poisoning and ABLV have been confirmed in the same animal).
References
Australian bat lyssavirus, Hendra virus and Menangle virus information for veterinary
practitioners. 2001. http://www.health.gov.au/internet/main/publishing.nsf/Content/cda-pubsother-bat_lyssa.htm
Hooper PT, Fraser GC, Foster RA, Storie GJ. 1999. Histopathology and
immunohistochemistry of bats infected by Australian bat Lyssavirus. Aust Vet J 77: 595-599.
McColl KA, Chamberlain T, Lunt RA, Newberry KM, Middleton D, Westbury HA. 2002.
Pathogenesis studies with Australian bat lyssavirus in grey-headed flying foxes (Pteropus
poliocephalus). Aust Vet J 80: 636-641.
Disease name
Hendra virus
Agent
Hendra virus, genus Henipavirus, family Paramyxoviridae
Significance
Pteropid bats (fruit bats) are believed to be wildlife reservoirs for Hendra virus, which is the cause of
fatal respiratory disease in horses and fatal encephalitis in humans.
Clinical Signs
None, Hendra virus is a subclinical disease in bats
Gross Pathology
None
Microscopic Pathology
Perivascular lymphocytic inflammation and/or fibrinoid vascular degeneration with lymphocytic and
histiocytic infiltration in blood vessels. Mesenteric and alimentary arteries are most often affected
followed by splenic central arteries in periarterial lymphoid sheaths, renal arteries, meningeal arteries,
placental vessels and foetal tissues.
Viral antigen in endothelial and smooth muscle cells of affected vessels can be demonstrated by
immunohistochemistry.
Differential Diagnoses
Nipah virus
Diagnostic Pathway
Identification of suggestive vascular lesions by histopathology followed by confirmation with
immunohistochemistry.
Immunostaining is more effective than virus isolation, as active virus is often neutralised by high
antibody titres, while inactive viral material will remain in lesions.
References
Williamson MM, Hooper PT, Selleck PW, Gleeson LJ, Daniels PW, Westbury HA, Murray PK.
1998. Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and
cats. Aust Vet J 76: 813-818.
Williamson MM, Hooper PT, Selleck PW, Westbury HA, Slocombe RF. 1999. Experimental
Hendra virus infection in pregnant guinea-pigs and fruit bats (Pteropus poliocephalus). J
Comp Path 122: 201-207.
Disease name
Nipah virus
Agent
Nipah virus, genus Henipavirus, family Paramyxoviridae
Significance
Based on serology, pteropid bats (fruit bats) are a hypothesised wildlife reservoir for Nipah virus, the
causative agent of a febrile respiratory and neurological disease in pigs and viral encephalitis in
humans.
Clinical Signs
None
Gross Pathology
None
Microscopic Pathology
Following experimental infection, various histological lesions were identified, the most suspicious
being small intestinal submucosal vasculitis, similar to Hendra virus lesions, and ganglioneuritis,
similar to lesions in Nipah infected cats. However, immunohistochemical staining and virus isolation
for Nipah virus was negative in these lesions.
Differential Diagnoses
Hendra virus
Diagnostic Pathway
Immunohistochemical staining and virus isolation may be able to be attempted.
References
Middleton DJ, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Westbury HA, Halpin K,
Daniels PW. 2007. Experimental Nipah virus infection in pteropid bats (Pteropus
poliocephalus) J Comp Path 136: 266-272.
BACTERIAL DISEASES
Disease name
Abscesses, pneumonia, meningitis
Agent
Various, including Pasteurella sp., Streptococcus sp., Staphylococcus sp. and Enterobacteria
Significance
Bacterial infections are relatively common in bats listed within the Australian Registry of Wildlife
Health, with most occurrences relating to aspiration pneumonia and secondary to bite wounds
Clinical Signs
Related to the organ system affected
Neurological signs can occur with meningitis
Tachypnoea and dyspnoea with pneumonia
Gross Pathology
Purulent exudation can be recognised with abscesses.
Pulmonary infections result in consolidation and abscess formation. Gross lesions can be unilateral.
Microscopic Pathology
Neutrophil dominated inflammation is most common in Registry cases
Differential Diagnoses
Differentials for abscesses include neoplasia and granulomatous disease (e.g. fungal disease).
Diagnostic Pathway
Suspicion based on gross inspection can be confirmed with histological examination and microbial
culture.
References
Helmick KE, Heard DJ, Richey L, Finnegan M, Ellis GA, Nguyen A, Tucker L, Weyant RS. 2004.
A Pasteurella-like bacterium associated with pneumonia in captive megachiropterans. J Zoo
Wild Med 35: 88-93.
MYCOTIC DISEASES
Disease name
White-nose syndrome
Agent
Geomyces destructans
Significance
An emerging disease first documented in New York state in February 2006, which appears to be
responsible for the death of thousands of microchiropteran bats in the eastern US states and
Canadian provinces with continued concentric spread.
Clinical Signs
Emaciation and poor body condition
Accumulation of white, fungal material around nose and elsewhere on body
Deterioration of skin of wing webs and elsewhere
Gross Pathology
Very little body fat
Marked dehydration
Microscopic Pathology
Fungal invasion of viable skin with no inflammatory reaction in hibernating bats, but marked
inflammation in non-hibernating animals
Cup-like epidermal erosions and ulcers on wing web and pinnae with fungal invasion of hair follicles
and sebaceous glands
Fungal hyphae branched and septate with variation from parallel 2µm walls to undulating walls
ranging from 3-5µm wide
Fungal conidia have distinctive curved shape
Differential Diagnoses
Presence of white fungus on muzzle of hibernating bats appears to be quite distinctive
Saprophytic post mortem invaders need to be ruled out on submitted carcasses
Diagnostic Pathway
Evidence of gross changes, although distinctive, is often lost on route to lab
Culture is difficult with a resultant low sensitivity
Fulfilment of histological criteria is sufficient for a diagnosis
PCR on small volumes of tissue is highly specific and sensitive and can be used on live animals
References
Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JTH,
Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. 2009. Bat white-nose
syndrome: an emerging fungal pathogen? Science 323: 227.
Cryan PM, Meteyer CU, Boyles JG, Blehert DS. 2010. Wing pathology of white-nose syndrome
in bats suggests life-threatening disruption of physiology. BMC Biology 8: 135
Lorch JM, Gargas A, Meteyer CU, Berlowski-Zier BM, Green DE, Shearn-Bochsler V, Thomas
NJ, Blehert DS. 2010. Rapid polymerase chain reaction diagnosis of white-nose syndrome in
bats. J Vet Diagn Invest 22: 224-230.
Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ,
Gargas A, Behr M. 2009. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet
Diagn Invest 21: 411-414.
Disease name
Histoplasmosis
Agent
Histoplasma capsulatum
Significance
Bat guano is a common source of Histoplasma capsulatum, the causative agent of histoplasmosis in
humans and other vertebrate animals worldwide, including Australia. Although prevalence of infection
in microchiropteran bats can be moderate to high, little to no morbidity or mortality in bats typically
occurs. No record of infection in megachiropterans could be found.
Clinical Signs
Rare
Gross Pathology
None
Microscopic Pathology
Numerous intracellular yeast-like cells in intra-alveolar and septal pulmonary macrophages
Yeasts appear as small blue dots (1-2µm) surrounded by a thin, clear halo on H&E
Yeasts can be highlighted in tissue using Periodic Acid Schiff (PAS) or methenamine silver (Grocott’s
or Gomori’s) stains.
Differential Diagnoses
Pulmonary infection with Blastomyces dermatitidis has been reported in a bat, but should be easily
differentiated based on its larger yeast size exhibiting broad based budding and the presence of a
granulomatous inflammatory reaction.
Diagnostic Pathway
Identification of yeasts in tissue using histopathology is highly suggestive
Fungal culture of lung, liver, spleen and gut is definitive but should be approached with caution due to
human infection risk
PCR and immunohistochemistry involve less risk (not currently available in Aust.)
References
Jackson S. 2003. Australian Mammals Biology and Captive Management. Collingwood:
CSIRO Publishing. Pp 524.
Maxie MG. 2007. Jubb, Kennedy and Palmer’s Pathology of Domestic Animals, Volume 3,
Fifth Edition. Philadelphia: Elsevier Saunders. Pp 737.
Raymond JT, White MR, Kilbane TP, Janovitz EB. 1997. Pulmonary blastomycosis in an
Indian fruit bat (Pteropus giganteus). J Vet Diagn Invest 9: 85-87.
Taylor ML, Chavez-Tapia CB, Rodriguez-Arellanes G, Pena-Sandoval GR, Toriello C, Perex A,
Reyes-Montes MR. 1999. Environmental conditions favoring bat infection with Histoplasma
capsulatum in Mexican shelters. Am J Trop Med Hyg 61: 914-919.
Disease name
Wing web infections; slimy wing
Agent
Candida spp., often co-infected with Pseudomonas sp. bacteria
Significance
Wing web infections typically occur when bats have insufficient access to sunlight, fresh air and space
to flap wings, usually in situations of poor husbandry or tightly applied bandages.
Clinical Signs
Areas of erythema progress to greyish, pseudomembranous slime. Fur may epilate easily, in matted
clumps. Often accompanied by foul odour.
Gross Pathology
As per clinical signs
Microscopic Pathology
Budding yeasts can be seen on impression smears
Dermatitis with intralesional fungal hyphae, pseudohyphae (chains of yeasts) and individual yeasts
would be expected
Differential Diagnoses
Necrosis secondary to trauma, particularly if gangrenous
Diagnostic Pathway
Identification of yeasts in tissue using histopathology or on impression smears
Fungal culture of wing web scraping
References
Olsson AR, Woods R. 2008. Bats. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
Jackson S. 2003. Australian Mammals Biology and Captive Management. Collingwood:
CSIRO Publishing. Pp 524.
PROTOZOAL DISEASES
Disease name
Toxoplasmosis
Agent
Toxoplasma gondii
Significance
Two reported cases in Australian flying foxes have both occurred in bats experiencing some degree of
captivity, which may have increased exposure to oocysts. No reports exist from free-ranging animals
but increasing encroachment of human urbanisation on bat habitat may increase opportunities for
infection. The presence of neurological signs makes this an important addition to the list of differential
diagnoses for ABLV.
Clinical Signs
Respiratory signs
Lethargy
Anorexia
Twitching and paresis (neurological signs)
Gross Pathology
Mottled appearance to lungs
Small white foci on various organs
Microscopic Pathology
Widespread, multifocal necrosis with pyogranulomatous inflammation
Foci of necrosis and gliosis within nervous tissues
Intralesional tachyzoites and bradyzoites within macrophages and tissue cells
Differential Diagnoses
For neurological changes:
Australian bat lyssavirus
Angiostrongylus cantonensis
Lead poisoning
Trauma
Tick paralysis (Ixodes holocyclus)
Other neurological disease (e.g. bacterial meningitis)
For intracellular protozoa
Neospora caninum
Diagnostic Pathway
Histopathologic appearance of tissue cysts is highly suggestive
Immunohistochemistry
References
Sangster CR, Gordon AN, Hayes D. In Press. Systemic toxoplasmosis in captive flying-foxes.
Aust Vet J.
Disease name
Hepatocystosis
Agent
Hepatocystis spp.
Significance
Vector borne infection found in many Old world mega and microchiropterans, including Australian
species. Infections tend to be self limiting and of little clinical significance.
Clinical Signs
None
Gross Pathology
2-4mm translucent merocysts can been seen on the surface of the liver in affected primates.
Visualisation of cysts in bats is rare (Karrie Rose, personal communication).
Microscopic Pathology
Large (4-6mm) merocysts form in hepatic parenchymal cells. With maturity, a colloid filled vacuole
forms in the middle and merozoites develop around the periphery.
Inflammatory cells can be present around merocyst borders.
Cysts are also present in lung interstitium
Ring shaped trophozoites and round to oblong, nucleated gamonts occur in circulating erythrocytes.
Differential Diagnoses
Plasmodium spp. has very similar ring-shaped trophozoites in erythrocytes, but this organism does
not form mature merocysts in the liver and produces characteristic protozoal pigment.
Diagnostic Pathway
Histopathologic appearance of merocysts is highly diagnostic
Molecular techniques are required for speciation of the pathogen
References
Duval L, Robert V, Csorba G, Hassanin A, Randrianarivelojosia M, Walston J, Nhim T,
Goodman SM, Ariey F. 2007. Multiple host-switching of Haemosporidia parasites in bats.
Malaria Journal 6: 157-164.
Gardiner CH, Fayer R, Dubey JP. 1998. An Atlas of Protozoan Parasites in Animal Tissues,
Second Edition. Washington: Armed Forces Institute of Pathology. Pp 84.
Landau I, Adam JP. ca. 1972. Two types of schizonts of Hepatocystis sp., a parasite of
insectivorous bats in the Congo-Brazzaville. Laboratory meeting notes of the Laboratoire de
Zoologie (Vers) associe au CNRS, Museum National d’Histoire Naturelle, Paris. Pp 2.
Olival KJ, Stiner EO, Perkins SL. 2007. Detection of Hepatocystis sp. in Southeast Asian
flying foxes (Pteropodidae) using microscopic and molecular techniques. J Parasitol 93: 15381540.
Olsson AR, Woods R. 2008. Bats. In Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing
T-W-Fiennes RN. 1972. Pathology of Simian Primates Part II: Infectious and Parasitic
Diseases. Basel: S. Karger. Pp 770.
Disease name
Renal coccidiosis
Agent
Nephroisospora eptesici nov. gen., n. sp.
Significance
Reported in big brown bats with prevalence ranging from 3.5-19%. Infections appear to be incidental.
Most notable is that although Nephroisospora eptesici nov. gen., n. sp. is closely related to Besnoitia,
Hammondia, Toxoplasma and Neospora, it accomplishes sporogony within the host, not apparently
requiring oxygen as do these other species.
No reports in megachiropteran bats.
(Note: Various enteric coccidia identified as Eimeria have been described in bats, again with little
known significance. No further discussion of these will be made.)
Clinical Signs
None that are known
Gross Pathology
0.5 to 1mm diameter white, raised or flat foci are seen in the cortex of the kidney.
Microscopic Pathology
Renal tubules are dilated to form cysts and are lined with hypertrophied epithelium containing asexual
and sexual coccidian stages.
Tubular lumens contain oocysts, which are sporulated with 2 sporocysts each containing 4
sporozoites.
Differential Diagnoses
Klossiella sp. previously reported in kidneys of Myotis sodalis; No dilation of tubules or intratubular
sporogony was described in this case.
Renal coccidiosis with tubular dilation was separately reported in Pipistrellus pipistrellus, Myotis
mystacinus, M. nattereri and Nyctalus noctula. In this report, no intratubular sporogony was seen,
indicating it was possibly a different species.
Diagnostic Pathway
Histopathologic examination of renal tissue
Molecular characterisation may be possible on fresh or frozen tissue
References
Gruber AD, Schulze CA, Brugmann M, Pohlenz J. 1996. Renal; coccidiosis with cystic tubular
dilatation in four bats. Vet Path 33: 442-445.
Kusewitt DF, Wagner JE, Harris PD. 1977. Klossiella sp. in the kidneys of two bats (Myotis
sodalist). Vet Parasitol 3: 365-369.
Wunschmann A, Wellehen JFX, Armien A, Bemrick WJ, Barnes D, Averbeck GA, Roback R,
Schwabenlander M, D’Almeida E, Joki R, Childress AL, Cortinas R, Gardiner CH, Greiner EC.
2010. Renal infection by a new coccidian genus in big brown bats. J Parasitol. 96: 178-183.
Disease name
Babesiosis
Agent
Babesia vesperuginis
Significance
Tick transmitted disease identified in various microchiropteran species in the British Isles, continental
Europe and the Americas. No reports in fruit bats could be found nor reports in Australasian
microchiropteran species.
Clinical Signs
No descriptions in bats, but clinical signs in domestic animals include:
Fever
Regenerative anaemia with reduced blood haemoglobin and increased reticulocytes
Jaundice
Haemoglobinuria
CNS signs when parasitised erythrocytes sludge in brain capillaries
Gross Pathology
Splenomegaly
Microscopic Pathology
Intraerythrocytic trophozoites (round to oval rings, 1.0 to 1.8µm); amoeboid forms (2.0 to 4.0µm rings
with central or marginated nucleus) and merozoites (pear shaped with distinct nucleus, 1.4 to 2.0µm)
Brain capillaries congested with parasitised erythrocytes
Differential Diagnoses
Other haematosporidia (Hepatocystis sp., Plasmodium sp.) have similar appearing trophozoites, but
should be easily differentiated based on the morphology of intravascular merozoites of Babesia sp.
Consider other causes of intravascular haemolytic anaemia (e.g. immune mediated disease or a toxin
such as copper)
Diagnostic Pathway
Suspicion based on clinical and post mortem signs
Blood or organ smears from freshly dead animals can reveal parasitised erythrocytes
PCR on fresh or frozen macerated heart tissue for speciation and diagnosis in further autolysed or
archived animals
References
Concannon R, Wynn-Owen K, Simpson VR, Birtles RJ. 2005. Molecular characterization of
haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology 131: 489-496.
Gardiner CH, Fayer R, Dubey JP. 1998. An Atlas of Protozoan Parasites in Animal Tissues,
Second Edition. Washington: Armed Forces Institute of Pathology. Pp 84.
Gardner RA, Molyneux DH, Stebbings RE. 1987. Studies on the prevalence of haematozoa of
British bats. Mammal Rev 17: 75-80.
Marinkelle CJ. 1996. Babesia sp. in Colombian bats (Microchiroptera). J Wild Dis 32: 534-535.
Kocan AA, Waldrup KA. 2001. Blood-inhabiting Protozoans. In Parasitic Diseases of Wild
Mammals Eds. Samuel WM, Pybus MJ, Kocan AA. Ames: Iowa State University Press. Pp 559.
METAZOAN PARASITIC DISEASES
Disease name
Neuro-angiostrongylosis
Agent
Angiostrongylus cantonensis (Rat lungworm)
Significance
Is a common cause of paresis in Black and Grey-headed flying foxes, and has been reported in Little
Red flying foxes and various other Australian native and introduced fauna. Clinical presentation and
history cannot be differentiated from Australian bat lyssavirus.
Clinical Signs
Hind limb or tetraparesis
Depression
Anorexia
Gross Pathology
Occasional petechial haemorrhages on surface of cerebral cortex
Meningeal congestion or cloudiness
Often no gross changes
Microscopic Pathology
Eosinophilic and granulomatous meningoencephalitis with macrophages, eosinophils, lymphocytes
and lesser plasma cells and multinucleated giant cells, most severe in brainstem and cerebellum
Perivascular cuffs of macrophages, lymphocytes and eosinophils
Tracts of tissue disruption, gliosis and/or haemorrhage
Nematode sections in subarachnoid space of cerebral sulci and/or cerebellar folds and less often in
parenchyma or ventricles
Metastrongyle larval characteristics include: coelomyarian musculature, accessory hypodermal
chords, lateral chords, and a large intestine
In animals with only stage 3 larvae, presence of little inflammation or parenchymous change with few
very small nematodes detectable
Differential Diagnoses
Australian bat lyssavirus
Lead poisoning
Trauma
Tick paralysis (Ixodes holocyclus)
Toxoplasma gondii
Other neurological disease (e.g. bacterial meningitis)
Diagnostic Pathway
Suspect neuro-angiostrongylosis based on history of hind limb paresis and depression. Exert caution,
however, as these signs are also consistent with ABLV. If human exposure has occurred, proceed as
for a lyssavirus suspect.
Parasitological identification of worms found grossly or extracted through maceration of half the brain
allows for definitive diagnosis.
Histological identification of larvae consistent with Angiostrongylus spp. in the brain is highly
suggestive, as the native species of Angiostrongylus, A. mackerrasae, has not been associated with
neurological disease.
Tracts of tissue disruption associated with eosinophils, gliosis and/or haemorrhage are also
suggestive.
References
Barrett JL, Carlisle MS, Procliv P. 2002. Neuro-angiostrongylosis in wild Black and Greyheaded flying foxes. Aust Vet J 80: 554-558.
Reddacliff LA, Bellamy TA, Hartley WJ. 1999. Angiostrongylus cantonensis infection in greyheaded fruit bats (Pteropus poliocephalus). Aust Vet J 77: 466-468.
Disease name
Pulmonary angiostrongylosis
Agent
Angiostrongylus mackerassae (presumed)
Significance
Recent case of pulmonary disease in a flying fox as a result of Angiostrongylus has been described
(manuscript pending). Significance of this disease to flying fox populations is unknown.
Clinical Signs
Unknown
Gross Pathology
Unknown
Microscopic Pathology
Adult worms with characteristic metastrongylid features (smooth cuticle, coelomyarian musculature,
large intestine lined by multinucleate cells, accessory hypodermal chords, lateral chords) in blood
vessels
Larval worms in air spaces
Differential Diagnoses
Other causes of pneumonia (bacterial, secondary to trauma)
Diagnostic Pathway
Parasitological identification of worms found grossly or extracted through maceration of fresh or fixed
lung allows for definitive diagnosis
Histological identification of larvae and adults consistent with Angiostrongylus spp. in the lung
References
Mackie J, Lacasse C, Spratt D. Pulmonary angiostrongylosis in a black flying fox. Manuscript
in progress.
Disease name
Toxocariasis
Agent
Toxocara pteropodis
Significance
Occur in all species of flying fox with up to 50% prevalence, but very low morbidity and mortality.
Pups are infected via transmammary exposure to larvae. Typically 3-5 worms mature in GI tract of
pups and eggs are shed in faeces. Adults consume eggs and hatched larvae migrate to the liver via
the portal circulation, where they remain dormant until mobilised in females at the time of parturition
and migrate to the mammary gland. Disease occurs rarely as the result of aberrant migration, heavy
parasitic burden and intestinal accidents.
Clinical Signs
Small size for age and bloated stomach with heavy burdens
Various other clinical signs are dependent on site of aberrant migration or presence of intestinal
accident
Gross Pathology
Adult worms present in the intestinal tract of pups
Adult worms present in aberrant sites in pups
Volvulus of intestine
Microscopic Pathology
Vascular and degenerative changes related to aberrant migration
Intestinal accidents result in congestion, oedema and necrosis of infarcted tissue
Differential Diagnoses
Other intestinal parasites recorded in bats include trichostrongyles, dendrolecithid trematodes and
one species of cestode.
Diagnostic Pathway
Examination of faeces from pups for presence of ascarid eggs
Identification of adult worms based on presence of three large lips and body size
References
Heard DJ, Garner M, Greiner E. 1995. Toxocariasis and intestinal volvulus in an island flying
fox (Pteropus hypomelanus). J Zoo Wildl Med 26: 550-552.
Prociv P. 1990. Aberrant migration by Toxocara pteropodis in flying-foxes – two case reports.
J Wild Dis 26: 532-534.
Spratt D, Beveridge I, Skerratt L, Speare R. 2008. Guide to the identification of common
parasites of Australian mammals. In Medicine of Australian Mammals Eds. Vogelnest L, Woods
R. Melbourne: CSIRO Publishing.
Disease name
Tick paralysis
Agent
Ixodes holocyclus
Significance
Variably causes loss of large numbers of Spectacled flying foxes in the Atherton Tablelands
rainforests.
Clinical Signs
Ascending flaccid paralysis
Dyspnoea
Cyanotic mucous membranes
Gross Pathology
Trauma associated with fly strike or predation, secondary to paralysis
Microscopic Pathology
No specific changes
Differential Diagnoses
For neurological signs
Australian bat lyssavirus
Angiostrongylus cantonensis
Lead poisoning
Trauma
Toxoplasma gondii
Other neurological disease (e.g. bacterial meningitis)
For tick like ectoparasites
Argus macrodermae (the bat tick of Ghost bats)
Nycteribiid flies
Diagnostic Pathway
Identification of attached tick on bat as Ixodes holocyclus:
Legs form a V-shape line from the snout down the body
First and last pairs of legs are brown, second and third are pale
Body is pear to oval shaped, light grey with dark bands on the side
Scute (face) is oval but wider at base and brown in colour
Snout is very long
Due to similarity of presenting signs, diagnostic testing to rule out ABLV and histopathology to rule out
Angiostrongylus cantonensis are required to make a definitive diagnosis.
References
Campbell FE, Atwell RB, Smart L. 2003. Effects of the paralysis tick, Ixodes holocyclus, on
the electrocardiogram of the Spectacled Flying Fox, Pteropus conspicillatus. Aust Vet J 81:
328-331.
Garnett S, Whybird O, Spencer H. 1999. The conservation status of the Spectacled Flying Fox,
Pteropus conspicillatus in Australia. Aust Zool 31: 38-54.
Paralysis Ticks Agnote DAI-267 Second Edition, NSW Agriculture website,
http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0013/160321/paralysis-ticks.pdf. Accessed
June 2008
Spratt D, Beveridge I, Skerratt L, Speare R. 2008. Guide to the identification of common
parasites of Australian mammals. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
Disease name
Other ectoparasites
Agent
Nycteribiid flies (spider-like flat flies)
Streblid flies (flat flies)
Mites
Fleas
Significance
The impact of these parasites on their chiropteran hosts is not fully understood, but is expected to be
minimal, except in the face of heavy burdens. Nycteribiid and streblid flies are thought to possibly
transmit erythrocytic parasites.
Clinical Signs
Flat flies can be found running through the coat of bats.
Gross Pathology
Presence of ectoparasites on skin surface
Microscopic Pathology
None
Differential Diagnoses
Ixodes holocyclus is the only ectoparasite known to have significant detrimental effects on Australian
bats.
Diagnostic Pathway
Identification of parasite based on morphology
References
Fauna of Australia, Australian Government DEWHA website,
http://www.environment.gov.au/biodiversity/abrs/publications/fauna-of-australia/fauna-1b.html.
Accessed June 2008.
Jackson S. 2003. Australian Mammals Biology and Captive Management. Collingwood:
CSIRO Publishing. Pp 524.
Spratt D, Beveridge I, Skerratt L, Speare R. 2008. Guide to the identification of common
parasites of Australian mammals. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
TOXICOSIS
Disease name
Lead poisoning, plumbism
Agent
Lead, typically from automobile and industrial emissions
Significance
Historically was a disease of urban fruit bats, speculatively due to high levels of atmospheric lead
resulting from automobile and industrial emissions. Recent examination of a series of 100
neurological bats did not identify a single case of lead poisoning.
Clinical Signs
Inability to fly, weakness, ataxia, muscle tremors
Emaciation, no appetite
Excess salivation, diarrhoea
Gross Pathology
No specific changes, but possible secondary traumatic injuries
Microscopic Pathology
Degeneration of renal proximal tubular epithelium with dissociation of cells into lumen
Renal tubular epithelial attenuation +/- tubular dilation and intraluminal accumulation of cellular debris
and hyaline casts
Intranuclear, eosinophilic, inclusion bodies in kidneys with >40 µg/g lead dry weight
Inclusion bodies are occasionally acid fast with Ziehl Neelsen stain
Differential Diagnoses
For neurological changes:
Australian bat lyssavirus
Angiostrongylus cantonensis
Trauma
Tick paralysis (Ixodes holocyclus)
Toxoplasma gondii
Other neurological disease (e.g. bacterial meningitis)
For renal tubular necrosis
Other heavy metal toxicoses
Possibly plant and mycotoxins
Diagnostic Pathway
Lead tissue levels > 10ppm wet weight (or µg/g dry tissue) in liver and > 25 ppm in kidney indicates
toxicity in domestic animals and this measure has been adopted for bats. Chronic exposure can be
measured using bones, teeth and fur. Fresh, frozen or fixed tissue is appropriate for testing heavy
metals.
References
Barrett J, Rodwell B, Lunt R, Rupprecht C, Field H, Smith G, Young P. 2005. Australian bat
Lyssavirus: Observations of natural and experimental infection in bats. Wildlife Disease
Association International Conference Proceedings, Pp.149-150.
Hariano B, Ng J, Sutton RH. 1993. Lead concentrations in tissues of fruit bats (Pteropus sp.)
in urban and non-urban locations. Wildl Res 20: 315-320.
Skerratt LF, Speare R, Berger L, Winsor H. 1995. Lyssaviral infection and lead poisoning in
black flying foxes from Queensland. J Wild Dis 34: 355-361.
Sutton RH. 1983. Lead poisoning in grey-headed fruit bats (Pteropus poliocephalus). J Wild
Dis 19: 294-296.
Disease name
Rodenticide poisoning
Agent
Anti-coagulant rodenticides
Significance
Bats are exposed when buildings are fumigated where bats are roosting and following spraying of
crops. Bats do not typically eat rodenticide baits.
Clinical Signs
Lameness
Swollen joints
Ventral haematoma
Dyspnoea and respiratory depression
Nasal and rectal bleeding
Vomiting of blood
Gross Pathology
Subcutaneous and internal haemorrhage
Microscopic Pathology
Haemorrhage in multiple tissues
Differential Diagnoses
Trauma
Diagnostic Pathway
Identification of grossly apparent haemorrhage in the absence of evidence of physical trauma should
raise suspicion.
Investigation to determine if rodenticide has been applied in the area of the affected animal
Prolonged clotting times in blood obtained from live animal
References
Olsson AR, Woods R. 2008. Bats. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
PHYSICAL INJURY
Disease name
Skeletal injuries
Agent
Collisions with vehicles, fences, powerlines and trees; shooting injuries; predator attacks
Significance
Humeral fractures are very common, followed by radial, metacarpal and phalangeal fractures.
Vertebral compression fractures and luxations can result when animals fly front on into stationary
objects.
Clinical Signs
Inability to fly
Palpable or visible displacement
Posterior paralysis with vertebral injury
Neurological signs with head trauma
Gross Pathology
Long bone fractures are often severely comminuted
Loss of digits is often accompanied by loss of significant portions of the adjacent wing web
Vertebral injuries often occur at the junction of the most caudal thoracic and first lumbar vertebrae.
Similar to birds, bats have a rigid thoracic vertebral column, facilitating injury at the first point of
flexibility, the thoracolumbar junction.
Microscopic Pathology
Spinal cord haemorrhage and degeneration secondary to vertebral injury
Differential Diagnoses
Neurological signs secondary to head trauma and posterior paralysis resulting from vertebral injury
are differentials for Australian bat lyssavirus, Angiostrongylus cantonensis, lead poisoning, Ixodes
holocyclus and other neurological diseases.
Diagnostic Pathway
Gross examination will reveal most skeletal injuries, though vertebral injuries can be subtle and
difficult to assess. Fixation and decalcification of the vertebral column en bloc can facilitate
examination by allowing subsequent longitudinal sectioning of the tissue. Be aware that cranial and
other skeletal trauma can occur secondary to primary neurological disease. If human exposure has
occurred, ruling out Australian bat lyssavirus is warranted.
References
Olsson AR, Woods R. 2008. Bats. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
Rose K. Common diseases of urban wildlife: mammals. ARWH website,
http://www.arwh.org/ARWH/CommonDisease/CDisease_Display.aspx. Accessed June 2008.
Disease name
Electrocution
Agent
Power lines, deterrent electric grids around fruit-growing areas
Significance
Significant numbers of pteropid bats are injured or killed in this manner. Infants often survive when
the dams are electrocuted due to the insulating effects of fur.
Clinical Signs
Sudden death
Singed fur
Burns to pinnae, wing membranes, uropatagium, toes and/or thumbs
Muscle fasciculations, seizures and cardiac arrhythmias in surviving animals
Gross Pathology
Singed fur may be the only change present
Burns to the integument, as described above, with associated necrosis, depending on duration of
survival following electrocution event
Congestion of visceral organs and lymph nodes and multifocal petechiae can be present
Pulmonary oedema
Burns in the mouth of neonates
Microscopic Pathology
Severe burns to skin result in coagulation necrosis of all components (epidermis, dermis and adnexa)
with acute inflammation, vasculitis and thrombosis, given the animal survives for a period of time.
With time, this acute inflammation will be replaced by histiocytes setting up a reparative granulation
process.
Pulmonary oedema may be detectable.
Differential Diagnoses
Burns from bush fires, lightning strikes, etc.
Diagnostic Pathway
History of bat being found on power lines and electric fences or on the ground below and presence of
external burns is highly suggestive.
References
Fairbrother A, Locke LN, Hoff GL. 1996. Noninfectious Diseases of Wildlife, Second Edition.
Ames: Iowa State University Press. Pp 219.
Maxie MG. 2007. Jubb, Kennedy and Palmer’s Pathology of Domestic Animals, Volume 1,
Fifth Edition. Philadelphia: Elsevier Saunders. Pp 899.
Merck MD. 2007. Veterinary Forensics, Animal Cruelty Investigations. Ames: Blackwell
Publishing. Pp 327.
Olsson AR, Woods R. 2008. Bats. In: Medicine of Australian Mammals Eds. Vogelnest L,
Woods R. Melbourne: CSIRO Publishing.
Radostits OM, Blood DC, Gay CC. 1994. Veterinary Medicine, Eighth Edition. London:
Bailliere Tindall. Pp 1763.
Disease name
Fencing entrapments
Agent
Barb wire fence
Significance
Large numbers of bats are injured and killed every year. Fencing injuries are recognised as
threatening processes in the recovery plans for the Spectacled flying fox (Pteropus conspicillatus) and
the Grey-headed flying fox (Pteropus poliocephalus).
Clinical Signs
Most affected bats will be found on the fencing with lacerations, twists and other physical injuries.
Gross Pathology
Mouth: Puncture wounds, teeth fractures
Wing membranes: Lacerations, punctures, twists resulting in ischemic necrosis and loss of the tissue
in days following the entanglement
Bones: Fractures and exposure with tearing of wing membrane
Microscopic Pathology
Histopathological changes related to physical trauma and resulting ischemic necrosis
Differential Diagnoses
Other causes of physical trauma, including predator attacks, hit by cars, etc.
Diagnostic Pathway
Diagnosis is based on history and appropriate gross lesions.
References
Wildlife Friendly Fencing Project website, http://www.wildlifefriendlyfencing.com/ Accessed
June 2008.
NEOPLASTIC DISEASES
Disease name
Round cell: e.g. Lymphosarcoma
Epithelial: e.g. Basosquamous carcinoma
Mesenchymal: e.g. Subcutaneous leiomyosarcoma
Agent
Spontaneous
Papillomavirus
Microchip-associated
Significance
Neoplasia is not commonly seen in wild or captive bats.
Clinical Signs
As per the presentation of the lesion
Gross Pathology
Nodules, thickening, organ enlargement, etc.
Microscopic Pathology
As per the cell of origin and malignancy of the tumour
Differential Diagnoses
Abscesses
Granulomas
Diagnostic Pathway
Histopathology
Immunohistochemistry and PCR to identify cell of origin and pathologic aetiology
References
Andreasen CB, Dulmstra JR. 1996. Multicentric malignant lymphoma in a pallid bat. J Wild
Dis 32: 545-547.
McKnight CA, Wise AG, Maes RK, Howe C, Rector A, Van Ranst M, Kiupel M. 2006.
Papillomavirus-associated basosquamous carcinoma in an Egyptian bat (Rousettus
aegyptiacus). J Zoo Wildl Med 37: 193-196.
Siegal-Willot J, Heard D, Sliess N, Nayden D, Roberts J. Microchip-associated
leiomyosarcoma in an Egyptian fruit bat (Rousettus aegyptiacus). J Zoo Wildl Med 38: 352356.
MISCELLANEOUS DISEASES WITH RARE REPORTS IN BATS WORLDWIDE
Cryptosporidium sp.
Dubey JP, Hamir AN, Sonn RJ, Topper MJ. 1998. Cryptosporidiosis in a bat (Eptesicus fuscus). J
Parasitol 84: 622-623.
Blastomyces dermatitidis
Raymond JT, White MR, Kilbane TP, Janovitz EB. 1997. Pulmonary blastomycosis in an Indian fruit
bat (Pteropus giganteus). J Vet Diagn Invest 9: 85-87.
Iron storage disease
Farina LL, Heard DJ, LeBlanc DM, Hall JO, Stevens G, Wellehan JFX, Detrisac CJ. 2005. Iron
storage disease in captive Egyptian fruit bats (Roussettus aegyptiacus): relationship of blood iron
parameters to hepatic iron concentrations and hepatic histopathology. J Zoo Wildl Med 36: 212-221.
Copper toxicosis
Hoenerhoff M, Williams K. 2004. Copper-associated hepatopathy in a Mexican fruit bat (Artibeus
jamaicensis) and establishment of a reference range for hepatic copper in bats. J Vet Diagn Invest
16: 590-593.
Algal poisoning
Pybus MJ, Hobson DP. 1986. Mass mortality of bats due to probable blue-green algal toxicity. J
Wildl Dis 22: 449-450.
DISEASES FOR WHICH BATS ARE KNOWN OR SUSPECTED TO BE CARRIERS IN AUSTRALIA
Leptospira spp.
Smythe LD, Field HE, Barnett LJ, Smith CS, Dohnt MF, Symonds ML, Moore MR, Rolfe PF. 2002.
Leptospiral antibodies in flying foxes in Australia. J Wild Dis. 38: 182-186.
Menangle virus
Halpin K, Young PL, Field H, Mackenzie JS. 1999. Newly discovered viruses of flying foxes. Vet
Micro. 68: 83-87.
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