he avian liver is bilobed and relatively largein comparison to the size of the bird. The lefthepatic duct connects to the duodenum. Theright hepatic duct connects to the gall blad-

der in those species that have this organ (gallina-ceous birds, ducks, geese). If the gall bladder is ab-sent (pigeons, parrots, ostriches), the right hepaticduct drains directly into the duodenum. If this ductdilates, it may appear as though a gall bladder ispresent (see Color 14). Birds have no mesentericlymph nodes, and patients with chronic enteritis mayalso have periportal hepatitis. The liver in a normalPsittaciforme rests ventrally against the sternum,wraps cranially around the base of the heart andwraps dorsally along the lateral margins of theproventriculus (see Anatomy Overlay). The size ofthe liver varies among species. In Galliformes, theliver lobes are of similar size while in Psittaciformes,the right lobe is generally larger. Bile acids secretedby the liver function to emulsify fats and activatepancreatic lipase and amylase, all of which aid indigestion. The liver also metabolizes fats, proteinsand carbohydrates and detoxifies metabolites andingested toxins.

TC H A P T E R

20HEPATOLOGY

J. T. Lumeij

Diagnostic Considerations22

Physical findings associated with liver disease areoften nonspecific, and are generally not sufficientlydiagnostic to establish a clinical diagnosis. A greencoloration of the urine and urate fractions in theexcreta is a strong indication of liver disease (Color20.4). Dyspnea is a common finding in birds withhepatomegaly or ascites. Occasionally, an enlargedliver can be palpated and in the smaller Passerifor-mes, an enlarged liver may be visible through thetransparent abdominal wall. Abnormal coloration ofthe liver is also sometimes visible, particularly insmall species and neonates. Polydipsia and vomitingare sometimes associated with liver disease. Pruri-tus occurs commonly in icteric humans and isthought to be caused by the deposition of irritant bilesalts in the skin. Clinical signs suggestive of pruritusand feather picking have been reported in birds withliver disease. Other integumentary disorders thatare loosely discussed in association with liver diseaseinclude pigment changes of feathers (Color 20.2),abnormal molting and softening, flaking and over-growth of beak and nails (Figure 20.1).

Because liver diseases may be associated with manyphysical findings and may even be asymptomatic,fecal examination, hematologic examination (PCV,

WBC and differentiation, buffy coat for parasites),total protein, plasma protein electrophoresis (A:Gratio), AST, LDH, bile acids and a total body radio-graph are considered the ideal database for evaluat-ing a sick bird. The history should involve questionsconcerning contact with birds outside the premises,which might indicate exposure to infectious diseasesthat cause hepatitis like Pacheco’s disease virus orchlamydia.

Clinical Pathology

Bile PigmentsGreen-colored urates are suggestive of liver dis-ease.5,20,38 This discoloration is the result of increasedexcretion of biliverdin (biliverdinuria), which is themost important bile pigment in birds. Icterus or jaun-dice, which is caused by a hyperbilirubinemia, is seenvery infrequently in birds. In chickens, if both bileducts are ligated, the concentration of plasma bilepigments rises immediately but stabilizes after twoweeks at about 85 µmol/l. This is a much lowerconcentration than is found in mammals with totalbiliary obstruction. In sera of healthy ducks, lowlevels of bilirubin may be detected, and significantlyelevated levels have been reported after experimen-tal infection with duck hepatitis virus; however, theobserved levels of about 17 µmol/l were well belowthe serum concentration of 34-51 µmol/l, which isconsidered the level above which jaundice becomesapparent in man. The infrequent occurrence oficterus in birds may also be explained by the fact thatthe enzyme biliverdin reductase, which convertsbiliverdin to bilirubin, is absent in the bird speciesthat have been tested.18,19,39 It has been suggestedthat in birds, some biliverdin may be converted tobilirubin by bacteria or nonspecific reducing en-zymes.17

Avian plasma may be colored yellow because of thepresence of carotenoids, and this normal color shouldnot be misinterpreted as icteric plasma. Some avianspecies, such as Hyacinth Macaws, have a normalyellow coloration of the skin that could be misinter-preted as icterus (see Color 8). A few hours after birdshave received an intramuscular multivitamin injec-tion, the urate fraction can be yellow-brown in color,which should not be confused with liver-inducedchanges in the urates (see Color 8).

Clinical EnzymologyThe application of clinical enzymology in human andveterinary medicine is a common method for estab-FIG 20.1 Liver disease should always be considered in the differ-

ential diagnosis list for birds with beaks and nails that consistentlyovergrow.

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lishing a diagnosis in certain disease conditions. In-creases in plasma enzyme activities are usually re-lated to leakage of enzymes from damaged cells, butsometimes there may be increased production in af-fected tissues. The increased concentration of a par-ticular enzyme in plasma depends on factors such asthe activity of enzyme in the cells, the rate of leakageand the rate of clearance of the enzyme from theplasma. Rational interpretation of elevated plasmaactivity of intracellular enzymes due to cellular dam-age can be performed only if the enzyme profiles ofthe various organs of the species under investigationand the elimination half-lives of these enzymes areknown. The most reliable way to investigate thespecificity and sensitivity of various plasma enzymesfor detecting liver disease is to establish referenceintervals in healthy individuals, and to monitorplasma enzyme changes after selective experimentalliver damage. These data are compared to changesassociated with diseases of other organs.

Enzyme profiles of the various organs have been inves-tigated in chickens, Mallard ducks, turkeys, racingpigeons, budgerigars and African Grey Parrots.

The elimination half-life of an enzyme can be calcu-lated from the exponential decline in activity duringrecovery from acute tissue damage. Alternately, itcan be determined by measuring the decline in activ-ity after intravenous administration of purified en-zymes. After intravenous injection, most enzymesfollow a biphasic exponential decline. The rapid pri-mary phase is related to distribution of enzymes bydiffusion from plasma into other extracellular bodyfluids, and the slower secondary phase is related tothe actual clearance of enzyme from the body fluids.During the secondary phase, a constant fraction ofthe enzyme present is eliminated per unit of time,making the decline linear on a logarithmic scale (firstorder kinetics). The time required for 50 percentcompletion of the latter process is defined as theelimination half-life (t1⁄2ß).

Plasma enzyme profiles have been studied in a num-ber of avian species following experimentally in-duced or spontaneously occurring liver disease. Un-fortunately, there is a large interspecies variation indata and the type of liver disease. Additionally, thepresence of concomitant injury to other organs thatcould alter the results of enzyme activity measure-ments may occur. The results of experimental studiesof liver-specific enzymes in racing pigeons are listedin Table 20.1.22,27,28 Information on enzyme activity in

other tissues may be found in Chapter 11 and in theAppendix.

Glutamate dehydrogenase (GLDH) is the most liver-specific enzyme in the racing pigeon. Since GLDH islocalized within the mitochondria of the liver cells,elevated plasma GLDH activities are seen only aftersevere liver cell damage (necrosis). Liver cell degen-eration without necrosis will not cause elevatedGLDH activities. In the budgerigar, GLDH activityin liver tissue is relatively low when compared toman and most other birds tested, including cockerel,duck, turkey and pigeon.31 However, increasedGLDH activities were observed in Amazon parrotswith extensive liver necrosis due to Pacheco’s diseasevirus, suggesting that this enzyme may be useful forthe detection of liver necrosis in at least some psit-tacine species.

Aspartate aminotransferase (AST, formerly GOT) isthe most sensitive indicator of liver disease in thepigeon. This variable, however, is not specific be-cause elevated AST activities can also be seen withmuscle damage.

Despite relatively low alanine aminotransferase(ALT, formerly GPT) activities in liver tissue of rac-ing pigeons, this enzyme is useful for detecting livercell damage because the elimination half-life inplasma is relatively long.

Lactate dehydrogenase (LDH) disappears rapidlyfrom plasma, making it a poor indicator of liverdamage, despite relatively high concentrations ofthis enzyme in liver tissue. Neither ALT nor LDH isspecific for the liver because these enzymes, like AST,also occur in muscle.

Gamma glutamyl transferase (τ-GT), has been foundto be a specific indicator of liver disease in the racingpigeon. The fact that no activity of this enzyme canbe found in supernatants of liver tissue homogenatesmay be due to the synthesis of τ-GT during choles-tatic liver disease, as has been reported in mammals.This enzyme is not as sensitive as AST.

Alkaline phosphatase (AP) and creatine kinase (CK)are never elevated after liver cell damage, while activi-ties of these enzymes in liver tissue are negligible.

It should be emphasized that elevated activities of“liver enzymes” in plasma may indicate recent dam-age to liver cells and does not give information onliver function.

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Intramuscular injections given within one to fivedays before collection of a blood sample may cause anelevation of some plasma enzyme activities due todamage of muscle tissue. This can lead to an errone-ous diagnosis of liver disease.

TABLE 20.1 Plasma Chemical Variables in Liver and Muscle Disease Based on Experimental Studies in Pigeons.22

Variable Liver Disease Muscle Disease

Specificity Sensitivity Specificity SensitivityBile acids +++ +++ – –

τ−GT +++ + – –

AST – +++ – +++

ALT – + – +++

AP – – – –

GLDH +++ +* – –

CK – – +++ +++

LDH – + – +

– low, + some, ++ moderate, +++ high*Only with liver and kidney cell necrosis.

Bile SaltsPlasma bile acids and bile salts are formed in theliver from cholesterol. It is likely that there is acontinuous secretion of bile into the intestine inbirds, with or without a gall bladder. A slight increasein secretions would be expected postprandially due tothe intrahepatic effects of intestinal hormones likesecretin, avian vasoactive intestinal peptide (VIP)and cholecystokinin (CCK). These hormones are re-leased after the consumption of food.

The exact site responsible for increased bile secretionand the regulatory mechanisms involved are pres-ently unknown.24 Bile acids secreted by the liverenter the small intestines, are absorbed in the lowersmall intestines, enter the portal vein and are ex-tracted from the blood by the liver. Enterohepaticrecirculation accounts for over 90% of the secretedbile acids being reabsorbed in the jejunum and il-eum.9 Plasma bile acid concentrations (PBAC), in-cluding their salts and corresponding glycine andtaurine conjugates, are a reflection of the clearingcapacity for bile acids by the liver. All liver functions(extraction, conjugation and excretion) are involvedin this process, and determination of plasma bile acidconcentration provides information on the combinedeffectiveness of these functions.

Due to the development of specific and sensitiveenzymatic assays for bile acids, bile salts and theircorresponding glycine and taurine conjugates, there

has been substantial progress with respect to the useof PBAC for the diagnosis of hepatobiliary disease.Circulatory levels of bile acids increase if the liver isdamaged and cannot extract bile from the portal veinor if the enterohepatic cycle is blocked and blood fromthe portal vein does not reach the liver. PBAC shouldbe considered a sensitive and specific variable fortesting liver function in birds as it is in mam-mals.3,12,23,36 Reference intervals for PBAC have beenestablished for the racing pigeon and the most com-mon psittacine species found in captivity (see Appen-dix). Experimental studies22 indicate that PBAC isthe single most useful, available test for determiningliver dysfunction in the racing pigeon. In experimen-tally induced liver disease, five- to ten-fold increasesof PBAC over the upper limit of the reference intervalare common.

Food consumption significantly increased PBAC ingranivorous birds with a gall bladder (Mallard Duck)and granivorous birds without a gall bladder (racingpigeon).24 The same effect was seen in carnivorousbirds.30 Although up to a 4.5-fold postprandial in-crease of PBAC was seen in individual birds, theconcentrations were never elevated more than 1.65-fold over the upper limit of the reference range. Inhepatobiliary disease, five- to ten-fold increases overthe upper limit of the reference range were com-mon.27 Although postprandial increase might compli-cate interpretation of PBAC, differentiation betweenpostprandial elevations and elevations due to hepa-tobiliary disease is possible. Experimental findingssuggest that values >70 µmol/l in fasted racing pi-geons and most psittacine species, and values >100µmol/l postprandially should be considered elevated,and therefore suggestive for hepatobiliary disease. InAmazon parrots, PBAC values >145 µmol/l are con-sidered elevated.24,28,29

Hepatic EncephalopathyA tentative diagnosis of hepatic encephalopathy isoften made when neurologic signs are seen in birdswith documented liver disease; however, this syn-drome has not been well documented in avian spe-cies. In man and other mammals, hepaticencephalopathy and hepatic coma are mostly seen inportosystemic shunting as a result of a portocavalanastomosis. It is not a disease in itself but a medicalcondition characterized by neurologic symptomscaused by intoxication of the brain by products ofprotein digestion, which enter the portal circulationand are not detoxified in the liver. It is believed thatdegradation products from protein catabolism act asfalse neurotransmitters. For this reason, protein-rich

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Hepatology

Color 20.1A mature Blue and Gold Macaw was pre-sented with a history of developing necroticlesions in the beak. The bird was severelyobese (1300 g) and had thick, white serum.The bird’s cholesterol level was 1700 mg/dl.A biopsy of the liver indicated severe fattydegeneration. The obesity and lipemia werecontrolled by switching the bird to a formu-lated diet supplemented with fresh fruitsand vegetables. The formulated portion ofthe diet was offered on a limited basis andthe bird’s exercise was increased. The beaklesion was theorized to have occurred sec-ondary to a vascular accident that causedan area of ischemic necrosis.

Color 20.2The occurrence of black discolored feathersin Amazon parrots and macaws is fre-quently discussed as a clinical change in-dicative of hepatitis. While a connectionbetween the appearance of black feathersand hepatitis has not been confirmed, clini-cal experience suggests that hepatitisshould be included in the differential diag-nosis list.

Color 20.3An obese Amazon parrot was presented forexercise intolerance (dyspnea) and inter-mittent depression. The bird weighed 700 gand had difficulty ambulating because offat in the inguinal and abdominal regions.The bird’s blood was yellow; a normal Ama-zon parrot’s blood is provided for compari-son. The bird’s cholesterol level was 2300mg/dl. Most other blood parameters wereconsidered non-diagnostic because of thelipemia. Radiographs indicated severehepatomegaly. Histopathology of a liver bi-opsy confirmed fatty liver degeneration.

Color 20.4Yellow-to-green urates are suggestive ofbiliverdinuria and are most commonly as-sociated with hepatitis.

Color 20.5Normal liver of an adult Umbrella Cocka-too hen with PBFD virus. Note the reddish-brown color, smooth consistency of the sur-face and sharp defined margins of thenormal liver lobes. In Psittaciformes, theright liver (rl) lobe is slightly larger thanthe left liver (ll) lobe. The lung (lu) can beseen lying under the transparent, contigu-ous wall of the cranial and caudal thoracicair sacs (open arrow). The transparent ven-tral hepatic peritoneal membrane can alsobe seen (arrows). Other organs that shouldbe noted include the heart (h), proventricu-lus (p) and ventriculus (v).

Color 20.6A breeding toucanette was found dead in itsenclosure. The abdomen was severely dis-tended. Characterisitics of fluid collectedby abdominocentesis at necropsy were con-sistent with a transudate. The enlargedliver was orange and rough in appearance.Histopathology was suggestive of hemo-chromatosis, and the disease was con-firmed using a Prussian blue stain to dem-onstrate iron-laden hepatocytes.

Color 20.7Swollen, pale-yellow liver from an Amazonparrot with severe hepatic lipidosis. Neo-nates that are mobilizing egg yolk will havea similarly appearing liver for the first twoto three weeks of life. Note that the heart isalso pale and rotund.

Color 20.8A Blue and Gold Macaw chick was pre-sented for evaluation. The bird was in acomatose state and was the sixth baby froma psittacine nursery to die acutely. The birdhad subcutaneous hemorrhages, hepa-tomegaly and swollen, hemorrhagic kid-neys, all suggestive of avian polyomavirus.A polyomavirus infection was suspected byidentifying basophilic intranuclear inclu-sion bodies in the liver, spleen, kidneys andheart, and was confirmed by DNA probedetection of viral nucleic acid on a swabtaken of the cut surface of the liver and

spleen. Note the petechial to ecchymotichemorrhages in the liver and heart.

Color 20.9An Amazon parrot with severe dyspneawas found on the bottom of its enclosure.The bird died while en route to the emer-gency clinic. At necropsy, the bird’s muscletissue was extremely pale. Exsanguinationhad occurred secondary to a tear in the livercapsule. Note the pale heart and left liverbelow the blood clot.

Color 20.10A Blue and Gold Macaw that was beingtreated for aspergillosis air sacculitis waspresented with an acute onset of anorexia,depression and abdominal swelling. Radio-graphs indicated a soft tissue density fill-ing most of the abdominal cavity. Abdomi-nocentesis was unproductive. Anexploratory laparotomy was performed.When the abdominal cavity was opened,unclotted blood flowed from the incisionwith each breath. The bleeding originatedfrom a tear in the right lateral liver lobe(arrow). The hemorrhage was controlledwith pressure. Both liver lobes had multi-ple, raised, white lesions that were sus-pected to be fungal granulomas. The clientelected euthanasia. At necropsy, the liverwas firm and had multiple, granuloma-tous-like lesions. Similar lesions werenoted in the lungs, and the right caudalthoracic air sac was thickened and necrotic.Histopathology confirmed Aspergillus sp.in the lung and air sac. The liver lesionswere characterized by massive hepatocel-lular necrosis and biliary hyperplasia.These lesions are suggestive of aflatoxi-cosis. Interestingly, the LDH=397,AST=141 and bile acids=1.9, determinedtwo weeks before surgery, did not reflectthe severity of the liver damage.

Color 20.11Cut surface of the liver from the Blue andGold Macaw in Color 20.10. Note the sub-stantial involvement of the liver and thescarcity of normal-appearing liver tissue.

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Hepatology

Color 20.12Severe fatty liver degeneration and bacte-rial hepatitis in a 23-year-old Amazon par-rot hen with ovarian cysts.

Color 20.13Multifocal, white-to-yellow discoloration ofthe liver is characteristic of hepatocellularnecrosis. The lesions in this African GreyParrot were caused by Chlamydia sp. Bac-terial and viral infections can cause simi-larly appearing lesions.

Color 20.14Hepatomegaly and multifocal, white-to-yellow foci in the liver and heart of a mynahbird that died from atoxoplasmosis (cour-tesy of Carol Partington).

Color 20.15Iron storage hepatopathy in a mynah bird.Small brown-black foci were clearly visiblethroughout the liver parenchyma. The le-sions can be more clearly visualized usinga magnifying glass (courtesy of Robert E.Schmidt).

Color 20.16Histomonas meleagridis (blackhead) le-sions in the liver of a gallinaceous bird.Multiple round foci with central depres-sions extending into the liver parenchymaare considered pathognomonic (courtesy ofR. Korbel).

Color 20.17Mycobacteriosis hepatitis in a SandhillCrane. Mycobacterium spp. infections fre-quently affect the liver and gastrointestinaltract in birds. Unlike in mammals, infec-

tions rarely occur in the lungs. Mycobacte-riosis should be considered in any bird withgranulomatous hepatitis. A quick diagno-sis can be achieved by acid-fast staining ofan impression smear of the cut surface ofthe liver (courtesy of Robert E. Schmidt).

Color 20.18An Amazon parrot was presented with ano-rexia, dyspnea, depression and weight lossof three days’ duration. Radiographs indi-cated severe hepatomegaly. Abnormalclinicopathologic findings includedWBC=25,000, LDH=700, AST=600 and bileacids=150. A fecal antigen test for Chlamy-dia sp. was positive. Doxycycline therapywas initiated, but the bird did not respondand died the following day. Necropsy indi-cated a severely enlarged, firm, irregularyellow liver. The histopathologic diagnosiswas lymphosarcoma. Chlamydia was notdetected in any tissues, suggesting that thefecal antigen test result was a false positive.

Color 20.19Multiple, disseminated granulomas in theliver of a gallinaceous bird. These lesionswere caused by Mycobacterium tuberculo-sis (courtesy of R. Korbel).

Color 20.20Plasmodium sp. infection in a PeregrineFalcon. The liver (l) and spleen (s) are bothenlarged, but the characteristic change isthe black discoloration of both organs.Other easily distinguishable organs in-clude the lung (lu), proventriculus (p), ven-triculus (v), heart (h) and intestines (i)(courtesy of Robert E. Schmidt).

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diets in patients with liver disease frequently triggerneurologic symptoms.

Fasting plasma ammonia levels and plasma ammo-nia levels 30 minutes after oral loading with NH4Cl(100 mg/kg in a gelatine capsule) have been used indogs to establish the ability of the liver to convertammonia into urea. Fasting plasma ammonia con-centrations in healthy psittacines have shown valuesranging from 36 to 274 µmol/l, which are well abovethe fasting concentrations described in dogs. Fur-thermore, some avian species will normally show upto an eight-fold increase of plasma ammonia concen-tration on oral ammonia tolerance test (ATT) usingthe canine protocol, and therefore an abnormal ATTis not diagnostic for portosystemic shunting in thesespecies.26 Further work is needed to properly diag-nose and document the occurrence of hepaticencephalopathy in birds.

Avian HemochromatosisLimited work has been done on the clinical pathologyassociated with avian hemochromatosis. The ironstatus of an individual bird is determined by meas-uring three main areas of iron: storage iron, trans-port iron and erythrocyte iron. Storage iron can besemiquantitated by histologic examination of liverbiopsies for stainable iron. In humans with hemo-chromatosis, urinary iron excretion in the six hoursfollowing injection of an iron chelating agent, desfer-rioxamine or diethylenetriamine pentacetic acid(DTPA) is significantly higher compared to normalindividuals. Serum concentration of the iron storageprotein ferritin is directly related to the availablestorage iron in the body and is clinically the mostuseful method for assessing iron stores.14

Transport iron in man is determined by measuringserum iron concentration and the total iron bindingcapacity (TIBC). The latter estimation is performedby determining the amount of iron required to satu-rate fully the iron-binding protein present in theserum sample. Reference values for serum or plasmairon concentration and TIBC in man are 10-34 µmol/land 45-72 µmol/l, respectively.37 In pigeons thesevalues are 11-33 µmol/l and 30-45 µmol/l, respec-tively.25 In Ramphastidae, total serum iron concen-trations should be below 63 µmol/l, while TIBCshould fall below 100 µmol/l.42 Total serum iron in amynah bird with confirmed hemochromatosis ex-ceeded 360 µmol/l, while control birds had valuesthat were about 36 µmol/l.32 (See update on need forbiopsy in Chapter 47.)

Erythrocyte iron can be evaluated by determiningthe red blood cell morphology and the various red cellparameters, such as PCV, hemoglobin concentration,mean corpuscular volume, mean corpuscular hemo-globin and mean corpuscular hemoglobin concentra-tion. Low erythrocyte iron will be reflected by abnor-malities in these parameters. Treatments of patientswith hemochromatosis using repeated phlebotomiesrequire frequent evaluation of red cell parameters todetect excessive iron depletion.

Plasma Chemistry and Liver DiseaseTo facilitate interpretation of plasma chemistry, it isadvisable to include specific and sensitive indicatorsof both liver and muscle disease in the plasma chem-istry panel (eg, GLDH, AST, CPK, bile acids). Itshould be stressed that elevated plasma enzyme ac-tivities are a sign of recent cell damage and notnecessarily of impaired organ function. Most en-zymes are not specific for one particular organ. Fur-thermore, in chronic conditions, extensive damageoccurring in the past may have led to major dysfunc-tion of an organ while enzyme activities may havereturned to normal. This is a common finding in birdswith liver fibrosis (normal AST, but elevated bileacids and extremely low protein and albumin) (Fig-ure 20.2). When periodic blood chemistry is per-formed in a bird with liver disease, fluctuation ofplasma enzymes and bile acids are often noted. En-zymes may be elevated while bile acids are not, andvice versa. Occasionally both variables may be foundto be within established reference intervals. Re-peated plasma chemistries are recommended whenevaluating liver disease to prevent misinterpretationof results.

Radiology

Both hepatomegaly and ascites due to liver diseasemay be diagnosed radiographically. Hepatomegalyand microhepatia are common findings in birds (seeChapter 12). It is important to differentiate betweenhepatomegaly and cardio-hepatomegaly, because thelatter indicates the presence of cardiac failure andsecondary congestion of the liver. Caudal displace-ment of the ventriculus on a lateral radiograph isoften caused by enlargement of the liver or associ-ated structures (eg, bile duct or gallbladder in thosespecies that possess one). Loss of the hourglass ap-pearance between the heart and the liver on a ven-trodorsal radiograph and widening of the liver be-yond a line between the scapula and the acetabulumindicate hepatomegaly. Caudodorsal displacement ofthe ventriculus is also possible with hepatomegaly.

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Ascites and peritonitis may complicate radiographicinterpretation and obscure hepatic enlargement byovershadowing the liver. Repeat radiography of theabdomen after removal of peritoneal effusion fluid byparacentesis or diuretic treatment may be needed tovisualize an enlarged liver and heart.

Liver Biopsy

In order for the clinician to establish a definitivediagnosis of liver disease, it is essential to take biop-sies for histologic examination. Indications for liverbiopsy include biochemical and radiographic changessuggestive of liver disease. Laparoscopic examina-tion and biopsy of the liver through a midline ventralapproach just caudal to the sternum is the method ofchoice to confirm a diagnosis of liver disease (seeChapter 13).8,16,22 Alternatively, the liver can be ex-posed through a ventral laparotomy incision and asmall wedge of liver tissue can be excised with smallsurgical scissors. The possibility of severe, life-threatening hemorrhage secondary to liver conges-tion should be considered prior to biopsy in cases

FIG 20.2 A one-year-old Scarlet Macaw was presented with blood-tinged feces two days after destroying a plastic bowl. Radiographsindicated severe microhepatia (arrows). Abnormal clinico-pathologic findings included WBC=18,500, TP=3.1 and bile ac-ids=130. AST=50 and LDH=130 were both normal. High bile acidlevels with normal AST and LDH activities suggest liver dysfunc-tion in the absence of ongoing cellular injury. Histopathologicevaluation of a liver biopsy indicated severe hepatic fibrosis ofunknown etiology.

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531

showing radiographic signs of congestive heart fail-ure or electrocardiographic abnormalities indicativeof cardiac disease. A liver biopsy site will usually clotwithout complication, but caution should be exer-cised when performing biopsies in birds that haveprolonged bleeding times after blood collection. Rou-tine tests to determine the efficiency of the avianclotting mechanism are presently not available. Inbirds with ascites, it is important to perform a biopsyby entering just caudal to the carina to avoid damag-ing the air sacs and asphyxiating the bird with itsown ascitic fluid.4 Liver biopsies should be examinedhistologically and cultured for bacteria. Acid-faststaining is of importance for the detection of myco-bacteria.

Liver Diseases

Liver disease occurs frequently in companion birds.Clinical and clinicopathologic signs may indicateliver disease that can be confirmed by histologic ex-amination of a liver biopsy. The following liver dis-eases discussed below have been documented in gal-linaceous, companion or aviary birds.1,2,6,7,10,13,15,33,34,40

This review is based on known etiologies of avianliver disease, but it should be stressed that an etio-logic diagnosis for many hepatopathies cannot bedetermined.

Infectious Diseases

BacteriaMany bacterial species can cause hepatitis in birds(Color 20.12). A diagnosis can be made by culturingthe organisms from a biopsy specimen. If bacteremiaoccurs, the same organisms can be isolated by bloodculture. Elevated white blood cell counts and mono-cytosis are common with hepatitis caused by Myco-bacterium avium. Bacteria that have been associatedwith hepatitis in birds include: Borrelia, Escherichiacoli, Salmonella typhimurium, Yersinia pseudotuber-culosis, Acinetobacter, Serratia marcescens, Staphy-lococcus, Campylobacter, Corynebacterium, Strepto-coccus zooepidemicus, Pseudomonas, Citrobacter,Pasteurella haemolytica, P. multocida, Mycobac-terium avium, M. bovis, M. tuberculosis (Colors 20.17and 20.19). In gallinaceous birds, bacterial cholecys-titis has been reported. Eubacterium tortuosum has

been associated with hepatic granulomas and ulcera-tion of the lower intestines in turkeys.

ChlamydiosisChlamydia psittaci is an extremely common cause ofhepatitis in psittacine birds (Color 20.13). Hepato-splenomegaly on radiographs of a bird that has beenin recent contact with infected birds is a charac-teristic clinical presentation (Figure 20.3). A tenta-tive diagnosis can be made by using an ELISA-typeantigen capture test for the detection of chlamydialorganisms in a fecal swab. Liver biopsies can bescreened for chlamydiosis with a Stamp, Giemsa orMacchiavello’s stain, or by fluorescent antibody IFAor ELISA.

VirusesMany viruses that infect birds can cause hepatitisalone or in combination with other systemic changes.Elevated plasma GLDH activity has been shown tooccur with Pacheco’s disease virus infections andshould alert the practitioner to extensive liver ne-crosis. Other herpesviruses are known in other avianspecies. Pacheco’s disease virus, adenovirus,polyomavirus, reovirus, coronavirus and avian ser-ositis virus have all been associated with hepatitis incompanion birds (Color 20.8).

Duck virus hepatitis is a highly fatal, rapidly spread-ing viral disease of young ducklings that can becaused by either of one of the three known duckhepatitis viruses: DHV types 1 (worldwide distribu-tion, classified as a picornavirus), 2 (only in England,classified as astrovirus), or 3 (only in USA, classifiedas picornavirus, unrelated to type 1). The suddenonset, rapid spread and acute course of this disease,in combination with hemorrhagic lesions in livers ofducklings up to three weeks of age, are practicallypathognomonic.

Turkey viral hepatitis is a highly contagious, oftensubclinical disease of turkeys that produces lesionsonly in the liver and pancreas (hence the suggestedname hepatopancreatitis). The presence of stress fac-tors is considered to be essential for manifestation ofthe disease. Mortality is usually very low and doesnot occur over six weeks of age.

HelminthsTrematode infections have been reported in the liverand bile ducts of cockatoos (Platynosomum proxilli-cens), penguins (Renicola sp.), cormorants (Am-phimerus elongatus), ducks and turkeys. A diagnosis canbe made by examination of the feces for trematode eggs.

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It should be noted that in birds, trematode eggs inthe feces do not always originate from parasites inthe liver. In pigeons and ducks, trematodes can alsobe found in the alimentary tract (Echinoparyphiumand Echinostoma spp.) or the kidney (Tamerlaniabragai in the pigeon). In various avian species (in-cluding chickens, Passeriformes and Anseriformes),trematodes can be found in the oviduct (Prosthogo-nimus ovatus). Pancreatic trematodes have also beenreported in birds.

ProtozoaA variety of protozoa can cause hepatopathies.Trichomonas gallinae-induced hepatic necrosis hasbeen reported in Columbiformes, Falconiformes andPasseriformes.

Histomonas meleagridis is a common cause of hepa-titis in captive Galliformes (Color 20.16). Sulfur-col-ored feces in turkeys, bloody cecal discharge in chick-ens, leucocytosis with heterophilia, a decreasedalbumin/globulin ratio and elevated liver enzymesare all suggestive of histomoniasis.

Leucocytozoon simondi is a well known cause of mor-tality in ducks and geese; however, the infection canalso occur in other species. Hepatosplenomegaly is

common, and parasites can often be detected in aperipheral blood smear.

Atoxoplasma (Lancesterella sp.) and toxoplasma in-fections are common in Passeriformes, but the latteralso occurs in Psittaciformes (Color 20.14). An en-larged liver can often be seen through the transpar-ent abdominal wall in Passeriformes with atoxoplas-mosis. Sporozoites may be seen in small lymphocytesin a peripheral blood smear.

Microsporidian infections have been associated withhepatitis in lovebirds.

Noninfectious Diseases

Metabolic DisordersIn zoological collections, Psittaciformes show a highprevalance of fatty infiltration of the liver (Color20.7). Hepatic steatosis, hepatic lipidosis and fattydegeneration have all been used to describe the con-dition. It has been well established that an unbal-anced diet (biotin, choline and methionine deficien-cies) or excessive consumption of high-energy dietswith restricted exercise may lead to fatty degenera-tion. It should be stressed that many companion

FIG 20.3 A young Double Yellow-headed Amazon Parrot was presented with lethargy, dyspnea and lime-green excrement. Radiographsindicated massive hepatomegaly causing cranial displacement of the heart (arrows), abdominal swelling (open arrow) and compression of theabdominal air sacs. The bird was positive for chlamydiosis by serology and responded to doxycycline therapy (courtesy of Marjorie McMillan).

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psittacine birds are fed high-energy, multi-nutrient-deficient, all-seed diets that predispose them to fattyliver degeneration.

Fatty liver hemorrhagic syndrome in laying hens hasbeen associated with high-energy diets fed to birdswith restricted exercise. The dramatic estrogen-in-duced increase in liver lipogenesis to supply the de-veloping ova has been suggested as the etiology ofthis condition. Reticulolysis and fibrosis of hepaticparenchyma is sometimes associated with a fattyliver. Reticulolysis is associated with rupture of in-trahepatic portal veins and liver hemorrhage. Af-fected chickens have greatly elevated serum calciumand cholesterol concentrations. The condition can beartificially induced with estrogen injections.

Fatty liver and kidney syndrome of young broilers orlayer pullets is associated with diets with a marginalbiotin content. Extensive fatty infiltration occurs inthe heart, liver and kidney without inflammatory ordegenerative changes. There is a failure of hepaticgluconeogenesis which may lead to an acute hypogly-cemia in biotin-deficient, otherwise healthy birds, ifnormal food intake is interrupted for a short time.

Iron Storage DiseaseHemosiderosis has been defined as an accumulationof an increased amount of hemosiderin in tissueswithout alteration of tissue morphology, while hemo-chromatosis is associated with pathologic lesions inhemosiderin-containing tissues (Color 20.6).21 He-mosiderin is an iron-containing pigment derivedfrom hemoglobin. The abnormal storage of iron ismost frequently seen in the liver, but other organsmay be involved. It has been suggested that exces-sive iron in the diet may be the cause of iron storagedisease but this hypothesis has not been confirmed.

Hemochromatosis is most frequently described inRampastidae (see Chapter 47), Sturnidae (birds ofparadise), mynahs and quetzals, but has also beenreported in Psittaciformes. Rampastidae are gener-ally clinically normal prior to death, but occasionallyaffected birds are listless 24 hours prior to dying.Cardiac disease has been reported in mynahs due toiron storage in the myocardium. Electrocardiog-raphic changes are possible due to cardiomegaly. Inmynahs, generalized weakness, dyspnea and ascitesare common. Radiography may reveal (cardio)hepa-tomegaly and ascites, and blood chemistry may indi-cate a liver function disorder (Figure 20.4). A specificdiagnosis can be made by histologic examination of a

FIG 20.4 A four-year-old mynah bird fed predominately a seed-based diet was presented for severe dyspnea, lethargy and abdominalswelling. Radiographs indicated a diffuse soft tissue opacity in the abdomen suggestive of hepatomegaly and ascites. The heart was displacedcranially (arrows). Fluid collected by abdominocentesis was characterized as a transudate (low cellularity, SpGr=1.012 and TP=2 gm/dl).These findings are typical for iron storage disease.

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liver biopsy after specific staining for iron (see Chap-ter 10). Total serum or plasma iron and TIBC may notbe helpful in evaluating the iron status of the animal.

Circulatory DisordersPortal hypertension can occur as the result of rightatrioventricular valvular insufficiency. Portal hyper-tension may cause hepatic congestion. In the acutestage, the liver is swollen; as the disease progresses,the organ may be fibrotic and have a shrunken ap-pearance. When liver enlargement is caused by con-gestion, a liver biopsy may result in fatal hemor-rhage. The use of an artificial substrate (eg, Gelfoam)at the biopsy site to facilitate clotting may help con-trol bleeding.

Anemic infarctions of the liver, especially of the cau-dal margins, can be seen as a result of bacterialendocarditis. Streptococci or staphylococci are ofteninvolved, but other bacteria like Erysipelothrix rhu-siopathiae (formerly E. insidiosa) and Pasteurellaspp. have also been associated with these lesions.

HepatotoxinsMany plants are known to be hepatotoxic in somebirds including: rapeseed (Brassica napus), ragwort(Senecio jacobea), castor bean (Ricinus communis),

FIG 20.5 A mature Blue and Gold Macaw with a history of asper-gillosis air sacculitis that was being treated with systemic antifun-gals became depressed and anorectic (see Color 20.10). Radiographsindicated a diffuse soft tissue opacity throughout the abdomen(arrows). Gas is seen in the dorsally displaced proventriculus (openarrows).

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hemlock (Conium maculatum), oleander (Neriumoleander), Oxalis spp., Grantia spp., Crotalaria spp.,Daubentonia seed and cotton seed (Gossypium spp.).Interestingly, canaries are routinely fed rapeseedand do not appear to be affected by its toxins.

The following substances are hepatotoxic: arsenic,phosphorus, carbon tetrachloride, toxins from cer-tain blue-green algae, halothane, methoxyfluraneand mycotoxins (especially aflatoxin from Aspergil-lus flavus, A. parasiticus and Penicillium puberu-lum) (Figure 20.5). Degeneration and necrosis ofhepatocytes are typical with aflatoxicosis. Bile ductproliferation and fibrosis leaving only islands ofhepatocytes are common in chronic cases (Colors20.10 and 20.11).

Fatty degeneration and the feeding of feeds contami-nated with mycotoxins causing aflatoxin hepatosisare likely to be involved in the high incidence of liverdisease in birds. Peanuts and Brazil nuts are notori-ous sources of aflatoxins, but many other seed mix-tures can be contaminated. Chemical analysis of foodfor aflatoxin is possible (see Chapter 37).

NeoplasiaLiver tumors can be classed as primary and mul-ticentric (metastatic) (see Chapter 25). Examples ofthe former are hepatoma, hepatocellular carcinoma,cholangioma, cholangiocarcinoma, lipoma, fibroma,fibrosarcoma, hemangioma, and hemangiosarcoma.Examples of metastatic tumors are leukosis/lym-phosarcoma, rhabdomyosarcoma, renal carcinoma,and pancreatic carcinoma (Color 20.18).

It has been suggested that there is an associationbetween cholangiocarcinoma and the presence ofcloacal papillomatosis in Amazon parrots (see Chap-ter 19). Likewise, it has been suggested that hemo-chromatosis in mynah birds and aflatoxicosis inducks are associated with hepatomas.

AmyloidosisAmyloidosis is commonly seen in Anseriformes, gullsand shorebirds. It is caused by deposition of amyloidA (a waxy, transluscent substance) in various organs,including liver and kidney (see Chapter 21). AmyloidA is a degradation product of an acute phase, reac-tant protein. Amyloidosis is often seen in birds withchronic infections (bumblefoot, tuberculosis and as-pergillosis). Severe hypoalbuminemia caused byglomerular and hepatic damage can cause ascitesand peripheral edema of the feet and legs.

Traumatic RuptureRupture of the liver is most likely to occur secondaryto liver diseases, such as fatty degeneration, amyloi-dosis, mycobacteriosis and neoplasia, but can alsooccur as a result of trauma (Color 20.9). The reticu-lolysis that is associated with some liver diseasesmakes the liver more sensitive to traumatic insult.When the bleeding is limited or confined to a subcap-sular hematoma, survival is possible. Birds can alsosurvive liver hemorrhage confined to one of the he-patic peritoneal cavities. This is based on clinicalcases and the documentation of blood clots in thesecavities during laparotomies.

In the acute phase, bleeding birds may show signs ofshock. Radiographically, liver enlargement is indis-tinguishable from perihepatic hematoma (Color20.10). A diagnosis is usually made during endoscopyor exploratory laparotomy. Ultrasonography is a use-ful diagnostic tool in these cases.

Treatmentof Liver Disorders

Generalities about treating avian liver disease can beextracted from known etiologies. The single mostimportant treatment seems to be the administrationof a well balanced diet free of hepatotoxins. Moldyfoods and seed-based diets, particularly those con-taining peanuts (unless certified mycotoxin-free),should be avoided. The use of lactulose, hemicellu-lose and supportive care including IV fluids and as-sisted feeding are indicated in many cases of hepati-tis. Special attention should be given to knowncauses of fatty degeneration or fatty infiltration ofthe liver (biotin, choline and methionine deficienciesor excessive consumption of high-energy diets inbirds with restricted exercise). A multivitamin injec-tion is indicated when malnutrition is suspected. Inbirds with hemochromatosis, the iron content of thediet should be drastically reduced (<100 ppm), al-though high iron content of the diet may not be theonly cause of excessive iron storage in the body.

The treatment of choice for hemochromatosis in manis to remove excess iron from the body by phlebotomy(one percent of body weight once a week for sixmonths, then twice a month for two years). Frequent

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monitoring of hemoglobin and serum iron level isessential.35 A few birds with hemochromatosis haveresponded to phlebotomy therapy (see Chapter 47).32,41

When a microbiologic cause of liver disease can bediagnosed, a specific treatment against the causativeorganism is possible. Doxycycline is the treatment ofchoice for chlamydiosis (see Chapter 34). Pacheco’sdisease virus infections can be treated with acyclovir.Liver flukes may be susceptible to praziquantel.

Outbreaks of duck hepatitis virus can be controlledby IM injection of DHV antiserum into each ducklingat the time the first deaths are noted.

Ascitic fluid should not be removed from birds withliver disease. Removal of this fluid will further de-plete body stores of protein in a bird with an alreadycompromised liver function. The author’s preference

for treating ascites is to use a potent diuretic, such asfurosemide, to effect, and to take only a small amountof ascitic fluid for diagnostic purposes.

Corticosteroids are occasionally used for the treat-ment of hepatopathies in man (eg, viral hepatitis,chronic active hepatitis) and may result in a dra-matic clinical improvement. Limited experience withprednisolone in cases of chronic active hepatitis ofunknown etiology in African Grey Parrots suggeststhat this drug may also be beneficial for treatingsome avian liver disorders. The use of corticosteroidsin mycotoxicosis may limit the formation of fibrosis;however, corticosteroids may exacerbate an underly-ing infection and may be contraindicated in cases ofinfectious hepatitis. Colchicine has been used to pre-vent the progression of hepatic fibrosis in a conure.11

References and Suggested Reading

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4.Degernes LA: A clinical approach toascites in pet birds. Proc Assoc AvianVet, Chicago, 1991, pp 131-136.

5.Galvin C: Laboratory diagnostic aidsin pet bird practice. Proc 47th AmAnim Hosp Assoc, 1980, pp 41-52.

6.Gould J: Liver disease in psittacines.Proc Assoc Avian Vet, Seattle, 1989,pp 125-129.

7.Gratzl E, Köhler H: Spezielle Patholo-gie und Therapie der Geflügelkrank-heiten [Pathology and Therapy ofPoultry Diseases]. Stuttgart, Ferdi-nand Enke Verlag, 1968.

8.Harrison GJ: A clinical comparison ofanesthetics in domestic pigeons andcockatiels. Proc Assoc Avian Vet,Boulder, 1985, pp 7-22.

9.Hill KJ: Physiology of the digestivetract. In Freeman BM (ed): Physiol-ogy and Biochemistry of the Domes-tic Fowl Vol 4. London, AcademicPress, 1983, pp 31-49.

10.Hillyer EV: Cholangiocarcinoma in as-sociation with cloacal papilloma intwo Amazon parrots. Proc Europ As-soc Avian Vet, 1991, pp 332.

11.Hoeffer H: Hepatic fibrosis and col-chicine therapy. J Assoc Avian Vet5:193, 1991.

12.Hoffmann WE, et al: Alterations in se-lected serum biochemical constitu-ents in equids after induced hepaticdisease. Am J Vet Res 48:1343-1347,1987.

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17.Lewandowski AH, Campbell TW, Harri-son GJ: Clinical chemistries. In Har-rison GJ, Harrison LR (eds): ClinicalAvian Medicine and Surgery. Phila-delphia, WB Saunders Co, 1986, pp192-200.

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22.Lumeij JT: Diagnosis of hepatobiliarydisease. In Lumeij JT: A Contribu-tion to Clinical Investigative Methodsfor Birds, with Special Reference tothe Racing Pigeon, Columba livia do-mestica. PhD Thesis, Utrecht Univer-sity, 1987, pp 35-77.

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Cambridge University Press, 1988,pp 161-174.

24.Lumeij JT: Fasting and postprandialplasma bile acid concentrations inracing pigeons (Columba livia domes-tica) and mallards (Anas platyrhyn-chos). J Assoc Avian Vet 5:197-200,1991.

25.Lumeij JT, DeBruijne JJ: Blood chemis-try reference values in racing pigeons(Columba livia domestica). AvianPathol 14:401-408, 1985.

26.Lumeij JT, Peccati C: Suspected hepa-toencephalopathy in an African greyparrot. Proc Europ Assoc Avian Vet,Utrecht, 1993, pp 558-566.

27.Lumeij JT, et al: Enzyme activities intissues and elimination half-lives ofhomologous muscle and liver en-zymes in the racing pigeon (Columbalivia domestica). Avian Pathol 17:851-864, 1988.

28.Lumeij JT, et al: Changes in plasmachemistry after drug-induced liverdisease or muscle necrosis in racingpigeons (Columba livia domestica).Avian Pathol 17:865-874, 1988.

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30.Lumeij JT, Remple JD: Plasma bileacid concentrations in response tofeeding in peregrine falcons (F. pere-grinus). Avian Dis 36:1060-1062,1992.

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40.Wadsworth PF, Jones DM, Pugsley SL:Fatty liver in birds at the ZoologicalSociety of London. Avian Pathol13:231-239, 1984.

41.Worell A: Phlebotomy for treatmentof hemochromatosis in two sulfur-breasted toucans. Proc Assoc AvianVet, Chicago, 1991, pp 9-14.

42.Worell A: Serum iron levels in Ram-phastids. Proc Assoc Avian Vet, Chi-cago, 1991, pp 120-130.

43.Worell A: Further investigation inRamphastids concerning hemochro-matosis. Proc Assoc Avian Vet, Nash-ville, 1993, pp 98-107.

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