Avian Liver Disease:
Etiology and Pathogenesis
Ron Rees Davies, BVSc, CertZooMed, MRCVS
Hepatic pathology is a common component of many
diseases seen daily by avian practitioners. Some dis-
eases are specific to the liver, but often the liver is
involved in disease processes that also affect a number
of other organ systems. This article gives a brief sum-
mary of the more common types of hepatic pathology
with notes on the predisposing factors and causes of
each.
Copyright 9 2000 by W. B. Saunders Company.
Key words: Avian, birds, liver disease, hepatic disease,
pathology.
vian hepatic disease is a huge subject, incor-
A porating many Widely differing types of
pathological conditions. I have divided liver
disease into a n u m b e r of broad categories. Most
conditions do not fall neatly into a single cat-
egory, and this classification is i n t e n d e d only as a
guideline to the major causative factor. This
article aims only to give a brief overview of the
subject. References to more detailed discussions
are provided. T h e diagnostic procedures used to
evaluate avian liver disease, and the various
treatments available, are discussed elsewhere in
this issue.
Congenital Liver Disease
Congenital extrahepatic biliary cysts have been
reported in an African grey parrot. 1
Traumatic Liver Disease
Traumatic internal injuries are not commonly
seen in clinical avian practice, because blood loss
and shock associated with internal ruptures are
usually rapidly fatal to the bird. Occasionally the
damage is restricted to subcapsular h e m o r r h a g e
or h e m o r r h a g e into a hepatic peritoneal cavity,
and, provided the shock can be managed effec-
tively, the bird may survive. Rupture of the liver
in the absence of significant trauma can occur
when the liver is r e n d e r e d friable b y some other
disease process. Neonatal hepatic h e m a t o m a
(subcapsular h e m o r r h a g e and secondary ane-
Seminars in Avian and Exotic Pet Medicine, Vol 9, No 3 (July), 2000: pp 115-125
mia after blunt trauma to the liver) has been
reported, primarily in macaws. 2 Trauma, leading
to adhesions or abscess formation in the liver,
may follow a lower esophageal or proventricular
foreign body penetration.
Metabolic Liver Disease
Lipidosis or fatty liver syndrome has been
r e p o r t e d for many years in psittacine sPecies and
hummingbirds. 3-5 Various vitamins are involved
in prevention of hepatic lipidosis in the normal
bird, including choline, vitamin B12, and folic
acid. 6 Deficiencies of these vitamins, along with
feeding for excessiye growth rates, have' been
implicated in cases of psittacine neonatal hepatic
lipidosis, seen especially in Umbrella and Moluc-
can cockatoos and in blue and gold macaws.
Chicks often present with severe dyspnea be-
cause the hepatic enlargement red,uces air sac
ventilation. 7 Fatty livers are seen in adult birds
fed diets of predominantly oily seeds (especially
sunflower seeds) or when fatty treats (dairy
produce, chocolate, etc.,) are allowed. Physical
inactivity also predisposes to the condition. In
estrilid finches, the condition may be associated
with the feeding of large quantities of soft foods
and mealworms. 8
In raptors, hepatic lipidosis is associated with
the feeding of obese laboratory vats, spent laying
quail, and day-old chicks with the yolk sacs left
From the Department of Avian~ and Exotic Species Medicine,
Lansdown Veterinary Surgeons, Clo&house Veterinary Hospital,
Wallbridge, Stroud, Gloucestershire, UK.
Address correspondence to Ron Rees Davies~ BVSc, CertZooMed,
MRCVS, RCVS Cer'tified in Zoological Medicine, Department of
Avian and Exotic SpeciesMedicine, Lansdown Veterinary Surgeons,
Clockhouse Veterinary Hospital, Wallbridge, Stroud, Gloucestershire,
6L5 3p,
Copyright ~ 2000 by W. B. Saunders Company.
1055-937X/00/0903-0002510.00/0
doi:l O.1053/ax~ 2 000. 7138
115
116 Ron Rees Davies
attached. These factors also predispose birds to
hyperchGlesterolemia and atherosclerosis. Mer-
lins (Falco columbarius) are affected by a condi-
tion known as fatty liver-kidney syndrome (FLKS),
which has been r e c o r d e d as the single largest
cause of death in this sl~ecies in captivity. 9 This
small raptor relies heavily on insects in its diet in
the wild, and it is proposed that the high levels of
fats contained in captive raptor foods, especially
day-old chicks, may be responsible for the condi-
tion. However, FLKS in young chickens appears
to be prevented by adequate dietary biotin. It i s
postulated that day-old chicks may contain high
levels of avidin in their yolk sac remnants, and
this may reduce the available biotin, leading to
reduced hepatic gluconeogenesis.
Hepatic lipidosis is also seen as a consequence
of increased fat mobilization. In female birds,
estr0gen-controlled lipogenesis d u r i n g egg-
laying increases the fat c o n t e n t of the liver.
Diabetes mellitus is e n c o u n t e r e d in psittacine
medicine, and secondary lipemia and hepatic
lipidosis ale c o m m o n findings. 1~
Visceral gout is a condition in which uric acid
crystals accumulate within the interstitial connec-
tive tissues of the liver and kidneys and on
visceral serosal surfaces. Crystalline deposits are
visible as white flecks on the liver surface endo-
scopically or at postmortem. Gout is most com-
monly seen in budgerigars, cockatiels, waterfowl,
and gallinaceous birds, but also is seen in many
other avian species. Canaries and pigeons' seem
less likely to b e c o m e affected. Gout usually devel-
Ops secondary to hyperuricemia, which occurs
when the a m o u n t of uric acid p r o d u c e d by
digestion and protein catabolism exceeds the
maximal rate of renal uric acid excretion. This
iituation can arise because of in'creased produc-
tion of uric acid (high-protein diet, cachexia) or
decreased renal function (dehydi"ation, circulal-
tory compromise, renal disease). Vitamin A defi-
ciency, causing squamous metaplasia of the renal
tubular and ureteral epithelium (and therefore
decreased tubular flow and decreased renal out-
put), and hypervitaminosisD (causing nephro'cal-
cinosis) are c o m m o n predisposing factors to
hyperuric.emia in caged pet psittacines. 11
Nutritional Liver Diseases
Microhepatica (a smaller than expected liver
outline) is a c o m m o n radiographic finding in
psittacine birds. 12 In some cases, it is attributable
to end-stage hepatic fibrosis, but in some birds it
occurs without an apparent pathological condi-
tion. This is suggested to be associated with birds
on inadequate or seed-based diets. ~
Hemochromatosis is included here u n d e r the
heading of nutritional liver diseases, although
the cause of the condition is very poorly under-
stood9 A n u m b e r of other diseases (eg, lead
poisoning, "oiling" ofseabirds), conditions (star-
vation), and normal physiological states (fasting
during breeding or moulting) cause varying
degrees of increased hepatic iron content. The
distinction should be made between hemosidero-
sis (excessive iron accumulation without toxic
effects of the iron) and hemochromatosis (func-
tional or morphological evidence of iron toxic-
ity). 14 Excessive dietary iron concentrations can
play a part in hemochromatosis, but further
study of the availability and gut uptake of dietary
iron in normal and affected avian individuals is
needed. Specifically, development of avian or
even species-specific ferritin and transferrin as-
says and studies of the function of these sub-
stances, and their relationshi p to various stress
factors would be useful, a5 The condition is rarely
seen in psittacine birds but is extremely c o m m o n
in captive Sturnidae (mynahs, starlings), Paradis-
aeidae (birds of paradise), Contigidae, Ptyono-
rhynchidae (bowOrbirds), Bucerotidae (horn-
bills), and Ramphastidae (toucans, toucanettes)
even when fed apparently low-iron diets. Clinical
signs are rarely n o t e d until the terminal stages of
the disease, when the bird is presented with signs
of cardiac or hepatic failure. ]6 Ascites, dyspnea,
and weakness are the usual clinical sigris, or the
bird may simply b e f o u n d dead. Investigations
usually show hepatomegaly and ascites and some-
times cardiomegaly and splenomegaly. The exces-
sive iron stores can be seen histologically on
biopsy br postmortem liver samples; however, it
is important to r e m e m b e r that t h e presence of
iron does not prove hemochromatosis is the
Causative problem 9 Low-iron diets are commer-
dally avail~ible and are r e c o m m e n d e d as a part of
prevention and attempted treatment protocols.
Foods high in iron such as egg yolk, liVer, raisins,
grapes, and green vegetables shoul d be avoided,
as should foods or supplements rich in vitamin
9 'i . ,
C, which increases Iron uptake.
Hypervitaminosis D3, usually caused by exces-
sive dietary supplementation, Can lead tO miner-
 Etiology of Avian Liver Disease 117

alization of a n u m b e r of tissues, including he- medicine, and in the absence of other data
patic parenchyma, and can predispose birds to should probably be used with caution in birds.
visceral gout. 7

Parasitic Liver Diseases

Toxic Liver Diseases
Toxic diseases of birds are discussed in detail
elsewhere.17,18 Table 1 lists a n u m b e r of potential
hepatotoxins. Some substances listed in the table
may be safe in appropriate amounts, whereas
undoubtedly m o r e substances will, in the future,
be f o u n d hepatotoxic. Most medicines used in
avian medicine have not b e e n fully evaluated for
potential toxic effects in avian species. T h e drugs
listed in the first c o l u m n of Table 1 are drugs in
regular use in avian medicine, which are consid-
ered potentially hepatotoxic in canine and feline
Protozoa
Atoxoplasma serinii and related species are
cyst-forming, systemic coccidial parasites. 22,23
Clinical disease is seen most notably in canaries
and other passerines but has also b e e n r e p o r t e d
in mynahs. Atoxoplasma isolated f r o m house spar-
rows has b e e n f o u n d to be apathogenic to
canaries, and so a degree of host specificity of
Atoxoplasma strains or species is assumed. Clinical
disease is seen in young birds 2 to 9 m o n t h s old,
with a mortality rate of up to 80%. Losses are

Table 1. Hepatotoxic Substances of Potential Relevance to Avian Species

Drugs Reported to Be Drugs Reportedor Suspected HepatotoxicEnvironmental
Hepatotoxicin Canine to Be Hepatotoxic Substances, Plants
and FelineMedicine in Avian Species and Foodstuffs
Ampicillin Alcohol Aflatoxin (Aspergillusspp.) [fungal toxin]
Anabolic steroids Amphotericin B Alcohol
Barbiturates Butorphanol Arsenic
Carbenicillin Cephalosporin Avocado (Perseaspp.) [fruit]
Cimetidine Clindamycin Castor bean (Ricinus communis) [plant & seed]
Corticosteroids Dexamethasone Copper
Diazepam Dimetridazole Pyrrolizidine alkaloids (Crotalanaspp.) [plant
Erythromycin Doxycycline toxins]
Griseoflflvin Fluconazole Crude oil
Haloperidol Isoflurhne Daubentonia SPP" (syn. Sesbania) [seed]
Halothane Isouiazid Ergot (Clavicepspurpurea) [fungal toxin]
Methoxyflurane Itraconazole Furniture pofish
Nitrofurantoin Ketoconazole Gossypol (Cotton seed; Gossypiumspp.) [plant
Nonsteroidal anti-inflammatory drugs Levamisole toxin]
Phenothiazines Medroxyprogesterone Grantia spp. [plant]
Tetracyclines Metronidazole Hemlock (C0nium maculatum) [plant]
Thiabendazole Potentiated sulfonamides Lead
Various antineoplastic agents Quinacrine Metaldehyde [mollusdcide]
Vitamin A Rifampicin Nerioside and Oleandroside (Oleander; Nerium
Ticarcillin oleando) [plant toxins]
Tobramycin Ochratoxin (Penicilliumsl0p. and Aspergillusspp.)
[fungal toxin]
Oxalate (Oxalisslop.) [plant toxin]
Phosphorous
Poinsettaspp. [plant]
Pyrrolizidine alkaloids (Cr0tdlariaspp.) ,[plant
toxins]
Ragwort (Seneci0jac0bea) [plant]
Rapeseed (Brassica napus) [seed]
Tricothecenes (Fusanumspp.) [fungal toxirl]
Vitamin D analog rodenticides
Zinc
Data from LumeijJT,12DavisLIE,19Ritchie BW and Harrison GJ, 20 and Tully TN.21
1~18 Ron Rees Davies
highest a r o u n d the time of fledging. Adult birds
can be asymptomatic carriers and shed the 20.1
19.2-1am oocysts in their feces for m o r e than 8
months. T h e life cycle is direct and asexual, with
y o u n g birds b e c o m i n g infected by ingesting the
oocysts. T h e organism has most effect on cells of
the reticuloendothelial system and the intestinal
epithelium. Clinical signs are nonspecific
lethargy, depression, and weight loss. Pathologi-
cal changes include hepatosplenomegaly, often
with mottling or multiple white to yellow indis-
tinct loci, swelling of the pancreas, hydropericar-
dium, and cardiac lesions. Clinically, the mark-
edly enlarged liver (the black-spot) can be seen
t h r o u g h the thin abdominal wall. Diagnosis is
m a d e by demonstration of the organism within
lymphocytes on Romanowsky-stained impression
smears of liver, spleen, heart, or pancreas, or in
severe cases on examination of small lympho-
cytes in stained blood or buffy coat smears. T h e
organism appears as a pale-staining, r o u n d to
oval intracytoplasmic inclusion compressing the
host cell nucleus into a characteristic crescent
shape. It also may be possible to identify oocytes
on fecal flotation.
Taxoplasma gondii is a parasite of cats that
occasionally can cause disease in birds. The
ingested oocy.tes can encyst in most tissues, a n d
a m o n g other pathological effects, h e p a t o m e g a l y
can be seen. 22,24
Sarcocystisfalcatula is a coccidian parasite that
is seen primarily in N o r t h America, where it is
naturally f o u n d as an intestinal parasite of the
opossum (Didelphis virginiana). A variety of insect
intermediate or transport hosts are involved in
the spread of the organism to birds. 25 In New
World avian species, which have some degree of
natural immunity, the parasite undergoes asexual
reproduction, followed by migration through
the bloodstream to the striated muscles; where
encystment takes place. Old World avian species,
however, often show p e r a c u t e mortality, with
p r e d o m i n a n t findings being p u l m o n a r y lesions
and hepatosplenomegaly. 22,26
Leukocytozoon simondii infection is r e p o r t e d as
a cause bf mortality in ducks and geese and can
affect most avian species. 22 Simulidian blackflies
f . , .
are vectors for the parasite. Initial d e v e l o p m e n t
of parasites is with~in liver and spleen, H'epato-
splenomegaly is, c o m m o n . ' The~ u n p i g m e n t e d
gametocytes are then released into the circula-
tion within white or' red blood cells. Parasites
often can be detected in a peripheral blood
smear.
Plasmodium spp. are relatively c o m m o n h e m o -
parasites in m a n y avian species. 22 Infection is
usually subclinical, but stressed birds may suc-
c u m b to disease a n d show anemia, hepatospleno-
megaly, and p u l m o n a r y edema. Certain avian
species, such as owls (especially snowy owls [Nyc-
taea scandiaca]) and various penguin species
a p p e a r m o r e susceptible than others to clinical
disease. T h e parasite is transferred f r o m wild
corvids, passerines, and waterfowl by mosquitoes
( Culex spp.).
Histomonas meleagridis is a protozoan parasite
that causes the syndrome known as blackhead in
domestic poultry. The parasite infests the embryo-
n a t e d eggs of the cecal worm, Heterakis gaUina-
rum. W h e n the w o r m larvae begin d e v e l o p m e n t
within the host bird. the histomonads are re-
leased and invade the cecal mucosa, causing
n o d u l a r inflammation or ulceration. They then
pass to the liver, where they cause severe focal
hepatocellular necrosis. T h e lesions often have a
characteristic "bullseye" a p p e a r a n c e on the liver
surface. 27
Trichomonas gaUinae is a motile protozoal para-
site usually associated with u p p e r gastrointestinal
disease. 22 In raptors a n d pigeons, the oral cavity
and p h a r y n x are usually affected, whereas in
psittacines infestation m o r e often affects the
crop. Left untreated, the parasite can invade the
mucosa and reach liver tissues, causing hepatocel-
lular necrosis.
Trematodes
Trematodes of the family Dicrocoelidae have
b e e n r e p o r t e d in the liver and bile d u c t s of a
n u m b e r of avian species. Infestation usually oc-
curs in wild birds after ingestion of intermediate
hosts such as arthropods. Hepatic changes occur
because of direct migratory damage, pressure
necrosis, bile duct hyperplasia, and biliary stasis.
Clinical signs vary f r o m mild anorexia or diar-
rhea to severe hepatic dysfunction and death. 22
Nematodes--Visceral Larval Migrans
T h e first-stage larvae of various species of
intestinal n e m a t o d e can penetrate the intestinal
mucosa and track along the portal blood vessels
to the liver. H e r e the larvae migrate t h r o u g h the
p a r e n c h y m a and elicit an intense reaction char-
 Etiology of Avian Liver Disease
acterized by extensive fibrosis, bile duct hyperpla-
sia, and i n f t a m m a t o r y cell infiltrates. 2s
Bacterial Liver Diseases
Bacterial diseases of the liver are many a n d
varied and can be p r i m a r y or secondary to
viruses, parasites, inadequate nutrition, unsuit-
able husbandry, and o t h e r locally i m m u n o s u p -
pressive factors. In many cases, further research
is necessary to identify specific relationships.
Many cases of bacterial hepatitis are seen, often
as an extension of an enteritis or part of a
septicemic condition. Bacteria isolated f r o m such
cases include species of Acinetobact~ Borrelia,
Campylobacter, Citrobacter, Corynebacterium, Esch,
erichia coli, Pasteurella, Pseudomonas, Salmonella,
Serratia, Staphylococcus, and Streptococcus zooepidemi-
cus. 12 Clinical and pathological findings of he-
patic e n l a r g e m e n t with mottling or miliary absces-
sation are similar in m a n y of these cases, although
findings in other organs may vary. Bacterial
endocarditis also can lead to anemic infarctions
of liver tissue, especially at the caudal margins.
Yersiniapseudotuberculosis is the causative organ-
ism of yersiniosis (pseudotuberculosis). This dis-
ease is particularly seen in ramphastid and passe-
rine species, and is characterized by multifocal
miliary abscessation of the liver and other vis-
ceral organs. 29,3~Infections in m a n y o t h e r avian
species have b e e n reported. T h e presence of
subclinical iron storage disease may play a p a r t in
the susceptibility of particular species or individu-
als to the disease, as is the case in humans, s~
Y enterocolitica is a h u m a n p a t h o g e n that can
be carried by gulls and o t h e r scavengers inhabit-
ing sewage farms. Y intermedia, Yfrederiksenii, a n d
Y kristensenii also have b e e n isolated f r o m avian
species, but their pathogenicity remains uncer-
tain. T h e author has also seen a case of yersini-
osis in a commercial partridge-rearing unit in
which Ypestis was isolated f r o m liver samples. An
L-form of Y pseudotuberculosis has b e e n isolated
f r o m free-ranging u r b a n pigeons.
Y pseudotuberculosis is considered native to
N o r t h e r n and Central Europe a n d has b e e n
introduced to o t h e r continents by the introduc-
tion of domestic and feral avian and r o d e n t
species, s,sl T h e organism is capable of growth at
temperatures as low as 4~ and ~the disease is
frequently seen in outbreaks during the winter
months. 29 T h e route of introduction to a previ-
119
ously unaffected aviary is often not ascertained,
but fecal contamination of food or water contain-
ers by wild birds a n d rodents is usually suspected.
A degree of protection can be m a i n t a i n e d by
preventing r o d e n t and wild passerine access to
aviaries and food stores and by covering outside
flights to reduce fecal contamination.
Clinical signs vary f r o m peracute and acute
forms where lethargy, diarrhea, dehydration and
dyspnea may p r e c e d e death, to chronic forms
where the birds b e c o m e emaciated and paretic,
a p p e a r i n g similar to birds affected with mycobac-
terial infections. T h e r e are m a r k e d species differ-
ences in susceptibility--for example, most tou-
raco species are highly susceptible to clinical
disease, yet white-cheeked touracos in adjacent
aviaries may remain unaffected or assume a
carrier state. Pathological changes seen include
hepatosplenomegaly, ascites, hydropericardium,
and multiple submiliary to miliary, sharply demar-
cated, grayish foci within the liver, spleen, lungs,
and kidneys. T h e organism can be readily identi-
fied on squash preparations of the liver lesions as
gram-negative short ovoid bacilli, which have a
characteristic b i p o l a r a p p e a r a n c e with Ro-
manowsky stains. Ducks affected with the disease
may show tarsal j o i n t infections, sl
Pasteurella multocida is the bacterium that
causes avian cholera, a disease with characteris-
tics similar to yersiniosis. It can affect a wide
range of avian species, but is especially i m p o r t a n t
as the cause of massive "die-offs" of wild migra-
tory waterfowl. 31
Mycobacterial Liver Disease
Mycobacteria are the organisms responsible
for avian tuberculosis, a widespread and well-
d o c u m e n t e d disease. Most avian orders can be
affected. T h e species of mycobacteria involved
are Mycobacterium avium and the less pathogenic
M intracellulare, although difficulties distinguish-
ing the two have led to t h e m being g r o u p e d
together as the M avium-intracellulare complex.
M genavense has recently b e e n r e p o r t e d f r o m a
n u m b e r of avian species. M tuberculosis and M
bovis also have b e e n f o u n d on occasion. All of
these organisms are zoonotic, especially to immu-
n o c o m p r o m i s e d individuals. 31
Mycobacteria are primarily gut-associated or-
ganisms and can be carried asymptomatically for
m a n y years. T h e organisms invade the intestinal
120 Ron ReesDavies
mucosa and form paratuberculous lesions of the
intestinal tract, which affect nutrient uptake.
The organisms can then spread hematogenously
and form chronic granulomata in the liver or
other Organs. Clinically, there are nonspecific
signs of chronic illness--wasting, weakness, leth-
argy, and anemia. Atypical mycobacterial infec-
tions can occur in passerine and small psittacine
birds, in which a generalized enlargement of the
liver at postmortem is the only finding. 31 Myco-
bacteriosis is diagnosed by the detection of
acid-fast staining bacilli on fecal smears, cytology
samples, or histopathological examination of
lesions. The organism may be shed in the feces of
affected birds in large numbers. It is extremely
persistent in the environment and infects new
birds when they consume contaminated food or
water or inhale mycobacterial spores. Once a
premises is infected, the disease becomes en-
demic and virtually impossible to eliminate. Be-
cause of their high prevalence of tuberculosis
care should always be taken when using pigeon
carcasses for feeding captive raptors. 32
Chlamydial Liver Disease
Chlamydia psittaci is an obligate intracellular
bacterium that cannot be cultured on cell-free
media. Avian strains can infect humans, dogs,
cats, and possibly other animals. Separate strains
affect cats, guinea pigs, koalas, sheep, and other
mammalian species. Chlamydiosis affects a wide
variety of bird species, especially psittacine birds,
but also raptors, waterfowl, passerine birds, poul-
try, gamebirds, and ratites. 33The disease is spread
very readily in a variety of excreted substances
(saliva, crop milk, feces, urine) and can be either
ingested or inhaled. Respiratory signs are some-
times seen but in many cases simply present as a
nonspecific visceral disease of highly variable
severity. Subclinical carrier states and latent infec-
tion are extremely common. Birds may be pre-
sented with chronic ill thrift, p o o r reproductive
performance, feather plucking, weight loss, ab-
normalities of beak, feathers, or nails, or signs of
serious systemic illness. Clinical investigations
may show combinations of hepatomegaly on
radiographs and elevations of the total white
blood cell count, plasma enzymes consistent with
(though not specific to) hepatic damage, and
plasma bile acids in cases in which the liver is
involved. Splenomegaly and air sacculitis are also
common.
Mycoplasmal Liver Disease
Mycoplasmal infections are generally limited
to the respiratory tract, but Mycoplasma synoviae
causes a more generalized infection in poultry,
waterfowl, and some passerine birds with hepati-
tis in addition to splenomegaly and synovitis. 34
Rickettsial Liver Disease
Aegyptianella pullorum is a causative agent of
anemia and hepatitis in birds, especially in the
Mediterranean region. 34 It is an intraerythro-
cytic parasite producing inclusions visible with
Giemsa stain. The organism is transmitted be-
tween birds by arthropods such as argassid ticks.
Affected birds may show anemia, weight loss,
diarrhea, and death. Species susceptible to the
infection include canaries, chickens, pigeons,
quail, raptors, and some waterfowl, ratites, and
psittacine birds.
Fungal Liver Diseases
Fungal infections in birds are primarily a
result of opportunist fungi invading an immuno-
compromised host. s5 AspergiUus fumigatus is a
ubiquitous fungal organism in soil and any other
areas of damp organic matter and !S the causative
agent of aspergillosis. O t h e r species such as A
flavus and A niger also can be involved. Infection
usually begins at the respiratory epithelium, but
with chronic severe infections the organism can
disseminate hematogenously or spread by local
invasion into visceral organs, including the liver.
The fungal invasion itself can cause areas of
hepatocellular necrosis, but in addition the fun-
gus can produce aflatoxin B1, which is hepato-
toxic. Hepatic involvement in Trichosporonbeigelii
and Penicillium griseofulvum infections also has
been reported. 36,37 Several drugs used in the
treatment of mycoses are also considered poten-
tially hepatotoxic (Table 1).
Mycotoxicosis is the name given to disease of
animals caused by fungal toxins. In addition to
aflatoxin, there are trichothecenes (produced by
Fusarium spp.), ochratoxins (produced by Penicil-
lium and Aspergillus spp.), and ergot (produced
by Claviceps purpurea), which can be toxic if
 Etiology of Avian Liver Disease
ingested with mouldy foodstuffs. All of these
toxins caff produce a large, pale, and often
lipidotic liver with areas of hepatocellular degen-
eration, bile duct hyperplasia, and fibrosis. 12
Viral Liver Diseases
Herpesviruses
A n u m b e r of herpesviruses with moderate
specificity to individual families or orders of
birds exist, including Amazon tracheitis virus,
canary herpesvirus, cormorant herpesvirus, crane
herpesvirus, duck plague virus, eagle herpesvi-
rus, falcon herpesvirus, finch herpesvirus, infec-
tious laryngotracheitis virus, Marek's disease vi-
rus, owl hcrpesvirus, Pacheco's disease virus,
pigeon herpesvirus, quail herpesvirus, stork her-
pesvirus, turkey herpesvirus, and weaver herpes-
virus. Most of these viruseS can cause some
degree of hepatic pathological c o n d i t i o n - - m a n y
causing diseases referred to as inclusion body
hepatitis. 3s This term should be avoided, because
it also can be applied to other viral diseases,
notably adenovirus infections.
Herpesviruses o f d o m e s t i c a t e d p o u l t r y
(Marek's disease virus; infectious laryngotrache-
itis virus; turkey herpesvirus; quail herpesvirus)
have b e e n extremely well d o c u m e n t e d else-
where, and numerous vaccines are available for
prevention of clinical outbreaks. Some degree of
cross-species infection occurs. For example, le-
sions suggestive of Marek's disease have been
reported in ducks, geese, swans, owls, falcons,
canaries, and budgerigars. 3s-4~
Possibly the best-known herpesviral disease in
pet avian species is Pacheco's disease, a rapidly
fatal hepatitis that can be responsible for out-
breaks of severe mortality in breeding colonies
and especially in quarantine stations and dealers
premisesY New World psittacine species appear
more susceptible than those from the Old World.
Transmission is by ingestion of feces and respira-
tory secretions. The incubation period is 3 to 14
days. Most birds are f o u n d dead or moribund,
although some have a more chronic course.
Some birds show no signs but b e c o m e latently
infected and shed the virus at times of stress,
particularly wild-caught Nanday and Patagonian
conures. Postmortem findings vary from no gross
changes to severe hepatosplenorriegaly, hepatic
necrosis, and internal hemorrhage. Histologi-
cally, inclusion bodies are seen within the hepato-
12 1
cytes, although these can be difficult to distin-
guish from adenovirus or polyomavirus.
Duck plague is a herpesviral infection of a
range of waterfowl species, including some swans
and geese, which can cause massive outbreaks of
disease and mortality in susceptible captive and
wild populationsY ,41 Clinical signs include de-
pression, anorexia, neurological symptoms, diar-
rhea, and hematochezia. Virtually all clinically
affected birds die. Pathological findings vary
between species. On postmortem examination,
diphtheritic membranes, petechiation, and annu-
lar bands of h e m o r r h a g e may be seen in the
digestive tract. T h e r e can be an enlarged, friable,
necrotic, a n d S o m e t i m e s orange liver and inter-
nal hemorrhaging from many organs. Some
latently infected birds have sublingual ulceration
at times of stress and are likely to be shedding
virus at this time. Vaccines are available for
protection of valuable susceptible collections.
Where feasible in captive collections, appropri-
ate biosecurity measures should be maintained.
Pigeon herpesvirus is one cause of hepatitis in
pigeons (see also adenovirus) and can cause
outbreaks of vomiting and respiratory signs. 3s,42
Pigeons of any age can be affected, but birds 4 to
16 weeks of age are most at risk. The mixing o f
young pigeons for racing often triggers out-
breaks in multiple lofts in an area at the same
time. Ulcerative lesions may be present around
the mucous membranes and skin of the face.
Cytological preparations from these, or from the
enlarged livers postmortem, may show inclusion
bodies.
Falcon and owl herpesviruses are serologically
very similar to pigeon herpesvirus, and most
affected raptors have fed on pigeon a few days
before becoming affected. Sudden deaths with
hepatitis are again the usual presentation. The
liver is enlarged with pinpoint areas of yellowish
discoloration. Falcon herpesvirus is present in
the United States, Europe, and Asia, but cur-
rently not in the United K i n g d o m 9 ,4~
Polyomavirus
Avian polyomavirus infections can affect a
wide variety of psittacine and passerine birds and
also are thought to affect various poultry, game
species, and ostrichesY Budgerigar, fledgling
disease was the first recognized polyomavirus
infection in any animal species and has been
widely studied) 8 Pathological lesions vary, de-
 122 Ron Rees Davies
pending on the age at which the birds are
infected." Chicks infected soon after hatching
have a period of high mortality, usually at 10 to
15 days of age. Sixty percent to 90% of infected
chicks die, with or without signs of abdominal
distension and subcutaneous hemorrhage. Post-
m o r t e m lesions include hepatosplenomegaly, as-
cites, hydropericardium, and internal hemor-
rhages. Chicks developing clinical signs after 15
days of age have a b e t t e r chance of survival but
often show bilaterally symmetrical dystrophic
flight, tail, contour, and downfeathering. This
presentation is known as French moult amongst
fanciers, although psittacine beak and feather
disease (PBFD) and other factors also can cause
the same .syndrome. T h e feather lesions caused
by polyomavirus often improve over a period of
many months, whereas those of PBFD tend to be
progressive. Adult budgerigars infected with poly-
omavirus show no clinical signs and may develop
an immunity that can be passed on to their
offspring.
Nonbudgerigar psittacine birds affected by
the same virus present differently. Birds often die
after a short (12- to 24-hour) period of lethargy,
crop stasis, regurgitation, diarrhea, and subcuta-
neous hemorrhage, especially over the crop and
cranium. H e m o r r h a g e from injection sites is
often more than expected. Birds that survive
l o n g e r than a few days show yellowing of the
urates, indicating hepatic involvement. Although
the infection is still more prevalent in neonates,
it also can be fatal in young adult birds, particu-
larly eclectus parrots. Feather changes are not
frequently seen in nonbudgerigar psittacine cases.
Some birds develop a more chronic infection or
even seem to recover, but a proportion of these
die some weeks or months later of renal failure.
Others may survive, but often show stunting,
maldigestion, polyuria, and r e c u r r e n t secondary
infections. Overall mortality in "at risk" fledg-
lings has been r e p o r t e d as 27% to 41%. Avaccine
has b e e n developed in the United States and
should prove very useful in prevention of the
disease in nonbudgerigar psittacines.
Finches with polyomavirus infection again
present with peracute hepatitis. T h e r e are peaks
of mortality in birds 2 to 3 days old, in fledglings,
and in mature birds. Surviving birds fledge later,
show p o o r feather development, and may de-
velop long, tubular, misshapen beaks.
Adenoviruses
Adenoviruses can cause hepatitis in a n u m b e r
of species. In psittacines, the condition is rare,
and adenovirus is more likely to be an incidental
finding at p o s t m o r t e m Y Pigeon adenovirus in-
fection is one cause (along with herpesvirus) of
flock outbreaks of hepatitis, presenting as vomit-
ing and lethargy, especially a m o n g young birds at
the start of the racing season. 42 Many adenovi-
ruses, although infecting many species, cause
clinical signs in a very narrow host range. This is
a particular problem seen in raptors fed on
adenovirus-infected day-old chicks. The chicks
seem healthy, and the virus is of no economic
concern to the poultry producer. However, when
the chicks are fed to raptors, certain species (eg,
Mauritius kestrel, Falco punctatus) can have se-
vere to fatal infections, whereas other species fed
on the same diet remain unaffected. 43
Reoviruses
Reovirus infections have b e e n d o c u m e n t e d in
psittacine birds (especially Old World species)
after i m p o r t a t i o n Y T h e r e is a nonspecific acute
systemic illness, including clinical signs and patho-
logical findings attributable to hepatic disease.
C o n c u r r e n t diseases are frequently present. Mul-
tifocal hepatic coagulative necrosis is a c o m m o n
pathological finding. The disease should be seen
less frequently as the trade in wild caught birds
declines. Reovirus has b e e n recovered from the
liver of pigeons with hepatitis, and up to 16% of
E u r o p e a n racing pigeons are seropositive for
reovirus. Reoviruses are also thought to cause
hepatic disease in chickens up to 7 days old and
commercial ducklings between 10 days and 6
weeks of age.
Leukosis
Lymphoid leukosis is the commonest virus-
induced neoplasm of chickens, ss It primarily
affects young fowl (4 to 9 months of age), though
less than 3% of infected birds develop tumors.
Tumors form slowly over several months through-
out the body but especially in the liver. Lym-
phoid leukosis has been reported in several
other species of birds, though in many cases virus
isolation has not been p e r f o r m e d , or has failed
to show the infectious agent. Retroviral involve-
m e n t is suspected to be the reason that budgeri-
gars are so susceptible to neoplastic disease,
 Etiology of Avian Liver Disease
including malignant neoplasms of the kidney,
gonad, and liver.
Paramyxovirus
Experimentally paramyxovirus infections have
been reported to cause hepatomegaly in conures
and quail, but respiratory, gastrointestinal, and
neurological changes are more usual. 3s
Papillomatosis and Hepatocellular
Adenocareinoma
PapiUomatosis is a term used to describe a
syndrome of papilloma-like lesions in the diges-
tive tract of psittacine birds. 3s Despite the name,
there is n o proven link with a papillomavirus or
any other virus type. The occurrence of out-
breaks within previously unaffected colonies sug-
gests a viral cause, and serological and DNA
evidence suggests that there may be an associa-
tion with a herpesvirus. 44 Papillomatous changes
associated with the condition also can be f o u n d
in the liver and pancreas. T h e r e is a strong
association between the presence ofpapillomato-
sis and the development of neoplasms of the
pancreas and liver. Bile duct cancers were f o u n d
in 15 of 24 psittacine birds with alimentary
papillomatosis.45
Togavirus
Eastern equine encephalitis virus (EEE; an
alphavirus) is e n d e m i c in various native bird
species along the eastern side of North, Central,
and South America. The disease is transmitted by
certain mosquito species, and the geographical
range of the mosquito species limits the areas in
which the infection is encountered. In natural
host species, the infection is usually asymptom-
atic. In nonnative bird species the virus can cause
encephalitis, enteritis, or sudden death. Hepato-
megaly and severe liver necrosig are among the
pathological findings, especially in certain passe-
fine species and whooping cranesY Humans
and horses also can b e c o m e infected with EEE
and occasionally develop mild to severe encepha-
lomyelitis.
Other Viruses
Duck viral hepatitis is a term given to a syn-
drome of acute disease outbreaks with mortali-
ties varying from 10% to 100% in young duck-
123
lings. 38 Outbreaks are limited almost exclusively
to farmed ducks. Pathological findings are en-
largement and congestion of the liver with red-
dish mottling. Birds appear weak and ataxic
before death. Severe necrosis of the hepatic
parenchyma is seen histologically. The syndrome
can be caused by a n u m b e r of different viruses.
Duck hepatitis virus (DHV) type 1 is a picornavi-
rus f o u n d worldwide, and has a mortality of up to
100% in neonates. T h e mortality rate is less in
older ducklings, and birds over 6 weeks of age
rarely have clinical disease. DHV type 3 is also
caused by a picornavirus but is less severe,
affecting only ducklings younger than 2 weeks
old and with a mortality of 50% or less. It is only
seen in the United States. An astrovirus causes
DHV type 2, and it has only been recorded in the
United Kingdom. Diarrhea, polyuria, and convul-
sions can be seen before death, with a mortality
of 20% or less. A fourth type, duck hepatitis B, is
caused by an endemic hepadnavirus, but, al-
though hepatitis has been d o c u m e n t e d in experi-
mentally infected ducklings, natural infections
have not b e e n associated with disease.
A n u m b e r of other viruses have been reported
to cause occasional hepatic pathological condi-
tions in birds, including eoronavirus (budgeri-
gar, guinea fowl), orbivirus (cockatiel, budgeri-
gar), rotavirus (lovebird), and parvovirus
(Derszy's disease, a severe, high-mortality hepati-
tis in goslings) .3s Some psittacines with circovirus
(PBFD) infection have hepatic pathological con-
ditions.
Neoplastic Liver Disease
A n u m b e r of neoplastic lesions have been
reported in avian livers. A selection of those
d o c u m e n t e d in nondomesticated birds are listed
below.12,46,47
Pet Avian Species
Bile duct carcinoma (cholangiocarcinoma)
Cholangioma
Fibrosarcoma
Hemangioma
Hemangiosarcoma
Hepatocellular a d e n o m a
Hepatocellular carcinoma
Lipoma
Malignant lymphoma
Myelolipoma
 124 Ron Rees Davies
Raptors
Various s e c o n d a r y c a r c i n o m a s
Adenocarcinoma
Bile d u c t c a r c i n o m a
Fibrosarcoma
Hisfiocytic s a r c o m a
L y m p h o i d leukosis
Malignant lymphoma
M a r e k ' s d i s e a s e (various l y m p h o p r o l i f e r a d v e
changes)
Xanthoma (not a true neoplasm)
Nonspecific Liver Disease
Various viral i n f e c t i o n s a n d s u b c l i n i c a l o r
c h r o n i c toxicities c a n cause d a m a g e to t h e liver
without the bird showing an acute episode of
clinical disease. T h e c o n d i t i o n is o n l y n o t e d by
the owner when the bird develops problems
b e c a u s e o f i m p a i r e d liver f u n c t i o n , b y w h i c h
t i m e t h e causative factors m a y have d i s a p p e a r e d
o r resolved. Signs c a n b e v a g u e a n d variable,
i n c l u d i n g o v e r t signs o f liver f a i l u r e s u c h as
ascites, b u t also i m m u n o s u p p r e s s i o n c a u s e d by
d e c r e a s e d i n f l a m m a t o r y p r o t e i n synthesis, vita-
m i n d e f i c i e n c i e s a t t r i b u t a b l e to d e c r e a s e d stor-
age capacity, a n d c h r o n i c ill t h r i f t a n d malaise.
F o r b e s h a s d e s c r i b e d a s y n d r o m e o f this type,
w h i c h h e t e r m s hepatopathy, as t h e c o m m o n e s t
c h r o n i c d e b i l i t a t i n g d i s e a s e o f captive r a p t o r s . 4s
T h e cause is p r e s u m e d to b e infectious, b e c a u s e
u p to 40% o f f a l c o n s in a c o l l e c t i o n m a y b e c o m e
a f f e c t e d o v e r a p e r i o d o f several weeks. H a w k s d o
n o t d e v e l o p t h e p r o b l e m . Birds g e n e r a l l y a p p e a r
normal when confined, but when taken out and
e x e r c i s e d , t h e y b e c o m e h y p o g l y c e m i c a n d col-
l a p s e o r convulse. T h e h y p o g l y c e m i a is t h o u g h t
to d e v e l o p b e c a u s e o f i n a b i l i t y to s t o r e o r m o b i -
lize h e p a t i c glycogen.
S i m i l a r p a t h o l o g i c a l c h a n g e s in p s i t t a c i n e s
have b e e n r e f e r r e d to as c h r o n i c - a c t i v e h e p a t i t i s
a n d h e p a t i c cirrhosis. A g a i n t h e cause is usually
u n d e t e r m i n e d , b u t c h r o n i c m a l n u t r i t i o n , chla-
m y d i a l disease, t o x i n e x p o s u r e , a n d i m m u n e -
m e d i a t e d factors have b e e n s u g g e s t e d . 49
C a r d i a c insufficiency, with s u b s e q u e n t p o r t a l
h y p e r t e n s i o n , c a n cause h e p a t i c c o n g e s t i o n ; in
t h e a c u t e stage, t h e liver a p p e a r s swollen. I n l a t e r
stages, t h e r e is a s h r u n k e n liver with fibrosis.19
A m y l o i d A is a d e g r a d a t i o n p r o d u c t o f i n f l a m -
matory proteins, and amyloidosis--the deposi-
t i o n o f a m y l o i d A in v a r i o u s o r g a n s , i n c l u d i n g
t h e l i v e r - - i s o f t e n s e e n in b i r d s with c h r o n i c
i n f l a m m a t o r y lesions e i t h e r in t h e liver o r else-
w h e r e , such as p o d o d e r m a t i t i s , aspergillosis, a n d
tuberculosis.12
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