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onfirming a diagnosis of renal disease inbirds is often difficult because clinicalsigns are generally nonspecific and are fre-quently complicated by secondary changes

caused by renal dysfunction. Lethargy, with a dimin-ished appetite leading to emaciation, is typical ofrenal disease. Birds may appear unable to fly, whilein reality they are too weak to fly. A distended abdo-men with or without ascites may be seen with renaltumors. In over 50% of renal neoplasms, the tumorcan be palpated (Color 21.11).2 Renal masses andascites may prevent normal air flow and cause dysp-nea because of compression on the abdominal andcaudal thoracic air sacs (Color 21.4). Urinary outputmay vary from anuria to polyuria. In oliguric pa-tients, the possibility of acute nephrotoxic renal fail-ure should be considered, and the client should becarefully questioned concerning the administrationof nephrotoxic drugs (eg, allopurinol, aminogly-cosides, polypeptide antibiotics and sulfonamides) orexposure to sodium chloride (eg, saline as drinkingwater, sea sand for bedding material, heavily saltedfoods) or other nephrotoxic substances (eg, heavymetals, ethylene glycol, carbon tetrachloride).

Clinical findings can be quite suggestive of renaldisease. During the physical examination, signs ofdehydration or shock may suggest a diagnosis ofprerenal renal failure. Dehydrated birds have a re-duced skin elasticity and dry mucous membranes.Subcutaneous urate tophi or urate accumulations injoints are signs of articular gout (Color 21.3), a clini-cal sequela to hyperuricemia, which in birds iscaused by a renal disorder. Unilateral or bilateralparesis of the legs is often the first clinical sign ofrenal neoplasm in psittacine birds (particularlybudgerigars). Neurologic signs are seen in about one-third of renal neoplasms, but may also be caused byother space-occupying lesions in the ipsilateral kid-ney (eg, iatrogenic hematoma, renal aspergillosis)(Color 21.2). Neurologic changes are secondary tocompression or inflammation of branches of the lum-bosacral plexus, which pass through the kidneys(Color 21.1). Constipation may also occur if the renalmass compresses the large intestine. In large birds,a lubricated, gloved finger can be inserted and moveddorsally in the cloaca in order to palpate the caudaldivision of the kidney. Any swelling, asymmetry ortenderness may be an indication of renal disease.4

CC H A P T E R

21NEPHROLOGY

J.T. Lumeij

Clinicopathologic changes in the blood and urinedepend on location and severity of the renal lesions(eg, glomerulopathies may lead to severe protein lossand hypoalbuminemia, while tubular lesions maylead to hyperuricemia or polydipsia).

Anatomy and Physiologyof the Kidney

The paired kidneys are located dorsally in a depres-sion of the pelvis. Each kidney is made up of threedivisions that are frequently referred to as lobes(cranial, middle and caudal). The divisions are com-posed of lobules with a large cortical mass and asmall medullary mass. It is difficult to demarcatebetween the cortical and medullary portions of thelobules. The cortex is composed of both reptilian-typenephrons that do not contain loops of Henle andmammalian-type nephrons that do contain loops ofHenle. The reptile-type nephrons are most numer-ous, and birds are less efficient in the excretion ofelectrolytes than mammals. The cortical-type neph-rons are uricotelic and the medullary-type produceurine. The former are located on the surface of thekidney, and the latter are located in a deeper orien-tation. The nephrons’ collecting ducts and ureters arecontiguous. The kidneys of birds are larger by weightthan in mammals. There are three pairs of renalarteries. The anterior branch arises from the aorta,and the middle and posterior branches arise from thesciatic artery or external iliac artery. The anteriorbranch supplies the cranial division of the kidney,and the middle and posterior branches supply themiddle and caudal divisions of the kidney.

Birds have a renal portal system in which the renalportal vein functions like an artery by carrying bloodto the tubules. Flow of blood into the kidneys fromthe renal portal system is controlled by valves. Thesevalves are bilateral and are located at the junction ofthe external iliac vein and the renal vein. Studiessuggest that acetylcholine causes the valves to closeand epinephrine causes them to open. If agents ex-creted by the renal tubules are injected into the legs,they are excreted by the tubules on the injection sideof the body before entering the general circulation.

Glucose is completely filterable and is normally ab-sorbed by the kidney. Glucosuria indicates that renalabsorption is damaged or that excessively high levelsof glucose are being presented to the kidneys. Theavian kidney has a reduced capacity to secrete creat-inine in comparison to uric acid.

Renal output varies with the water intake and stresslevels of the bird, but is generally considered to be100 to 200 ml/kg/day. By comparison, dehydratedbirds may have a renal output of 25 ml/kg/day. Thereis a physiologic polyuria that occurs a few hoursbefore egg laying.

Some urine water that is excreted into the cloaca ispassed by antiperistaltic movement of the cloaca intothe colon where absorption of the liquid occurs. Indehydrated birds, 15% of urine water may be reab-sorbed from the colon. The amount of water absorbedby the colon is decreased with polyuria or with astress-induced defecation creating a moist-appearingexcrement.

Pathophysiology

Etiology of GoutUric acid (UA) is produced in the liver and is themajor end product of deamination of amino acids inbirds. It constitutes approximately 60 to 80% of thetotal excreted nitrogen in avian urine. Uricotelismpermits excretion or storage of nitrogen waste in asmall volume of water. Uric acid is relatively non-toxic when compared to urea or ammonia. Thismethod of handling nitrogenous waste is essentialfor embryo development within an egg. Uricotelismmay also be viewed as an adaptation for water con-servation.

Uric acid is synthesized in the liver. Ninety percentof its excretion is via tubular secretion from reptil-ian-type nephrons and therefore largely independentof urine flow rate. The clearance of uric acid sur-passes the glomerular filtration rate by a factor ofeight to sixteen and is occasionally even higher. Therate of secretion is largely independent of the state ofhydration because UA excretion is independent oftubular water reabsorption. Very high concentra-tions of uric acid can be found in ureteral urine indehydrated birds. Renal function disorders can even-tually lead to elevated uric acid concentrations. How-ever, non-protein nitrogen substances in plasma,such as uric acid, creatinine and urea will be elevatedonly when renal function is below 30% of its originalcapacity.

CHAPTER 21 NEPHROLOGY

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Hyperuricemia is defined as any plasma uric acidconcentration higher than the calculated limit ofsolubility of sodium urate in plasma and is an indica-tion of nephrosis or impaired renal function. Anordinary aqueous solution at 37°C, with a sodiumconcentration equal to that of normal human plasmais saturated when the urate concentration reaches383 to 407 µmol/l. It is generally accepted that theupper limit of solubility of urate in human plasma, is420 µmol/l.3 Urate solubility increases with highersodium concentrations and higher temperatures.When the higher body temperature of birds (up to43°C) is taken into account, the theoretical limit ofsolubility would be about 600 µmol/l. Because avianspecies have a higher plasma sodium concentrationthan humans (136-145 mmol/l), the theoretical limitof urate solubility is even higher. Hyperuricemia canresult in urate precipitation in joints (articular gout)(Colors 21.10 and 21.12) and in visceral organs orother extra-visceral sites (visceral gout) (Color 21.7).The exact mechanism of deposition or the predilec-tion for gout to occur in certain sites is unknown.Gout should not be regarded as a disease entity, butas a clinical sign of any severe renal dysfunction thatcauses a chronic, moderate hyperuricemia.

When birds are provided with dietary protein inexcess of their requirements, the surplus protein iscatabolized and the nitrogen released is converted touric acid. The total amount of uric acid formed maysurpass the clearing capacity of this substance fromthe body, and hyperuricemia and articular gout mayresult. The use of high-protein poultry pellets as thebulk food in psittacine aviaries may result in anincreased incidence of gout (See Chapter 3).

Articular and Visceral Gout There is no consensuson the different etiologies of articular and visceralgout in birds. The following hypothesis seems toexplain all known facts.

A plasma uric acid concentration that is slightlyabove the solubility of sodium urate will lead to uricacid precipitates in the body. Predilection sites arethose areas where the solubility of sodium urate, forwhatever reason, is lower than in other areas (Figure21.1). The joints and synovial sheaths may be predi-lection sites because of a lower temperature than therest of the body. Once uric acid deposits have occurredin a specific area, these deposits will grow with time,forming tophi (accumulations of uric acid) (Color21.8).

If, for whatever reason, uric acid crystals precipitatein the tubules or collecting ducts of the kidney (eg,severe dehydration of long duration, hypovitami-nosis A) or the ureters, an acute obstructive uropathy(postrenal obstruction) will occur (Color 21.3). Thesebirds develop anuria or gross oliguria, and tubularsecretion of uric acid is severely compromised orstops. This results in a rapid and severe elevation ofplasma uric acid concentration with precipitation ofurates on many visceral surfaces, including thosepredilection sites for articular gout. Visceral gout willrapidly lead to death of the affected animal. Thishypothesis is supported by the fact that inflamma-tion and tophi formation are rare with visceral gout,because the condition has a rapidly fatal course.There is simply no time for an inflammatory reactionor tophi to develop. The kidney tubules, collectingducts and ureters may contain uric acid deposits.

Acute, renal tubular failure, which would lead toacute abolishment of uric acid secretion, would resultin a similar course of events. In this situation, vis-ceral gout could develop without uric acid depositsforming in the tubules, collecting ducts and ureters.

The acute mortality seen in birds with visceral goutis probably not due to the effects of hyperuricemia,because uric acid is generally a nontoxic, insolublesubstance. It is likely that these birds die from car-diac arrest caused by hyperkalemia, although thishypothesis needs confirmation.

FIG 21.1 A six-year-old male budgerigar was presented for lame-ness of several days’ duration. Multiple, firm, raised nodules (tophi)were noted at several periarticular locations. The severe articulargout was considered unresolvable and the bird was euthanatized.Histopathology revealed severe nephritis.

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Acute and Chronic Renal FailureRenal dysfunction may result from any progressivedestructive condition affecting both kidneys (chronicrenal failure), but can also occur in conditionswherein the function of the kidneys is rapidly andseverely, but often reversibly, compromised (acuterenal failure) (Figure 21.2). In the latter condition,oliguria usually occurs, while in the former situation,polyuria is normally seen. Dehydration and shock(prerenal renal failure), urolithiasis (postrenal renalfailure) and urinary tract infections and the admini-stration of nephrotoxic drugs can all cause changesthat mimic irreversible chronic renal failure. Appro-priate and timely treatment of the former conditionscan often prevent further damage and in some casesresult in improved function. Extrarenal factors suchas infection, gastrointestinal hemorrhage and hypo-volemia can disturb an otherwise stable, well com-pensated, asymptomatic patient with chronic renaldisease and precipitate a life-threatening, acuteclinical change.

Prerenal AzotemiaPrerenal azotemia can be defined as the clinical con-dition associated with reduced renal arterial pres-sure or perfusion leading to oliguria and retention of

FIG 21.2 An adult male Umbrella Cockatoo was presented withsevere depression, emaciation (470 g) and putrid, watery diarrhea.Abnormal clinical pathologic findings included WBC=46,000,PCV=34%, TP=7.5 and LDH=500. Radiographic lesions included amicrocardia (open arrow) and radiodense kidneys (arrows), both ofwhich are indicative of dehydration and hypovolemia. Necropsyfindings included small irregular kidneys with multiple granu-lomas and granulomatous tubulointerstitial nephritis.


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nitrogenous urinary waste products in the blood. It isoften seen during shock or severe dehydration. Inclinical textbooks, it is commonly stated that dehy-drated birds have elevated plasma uric acid concen-trations. In recent experimental studies, elevatedplasma uric acid concentrations were not observed inracing pigeons that were deprived of water for fourdays, while plasma urea concentration showed a sig-nificant 6.5- to 15.3-fold increase above referencevalues. Urea is normally present in low concentra-tion in avian plasma and determination of this hastraditionally been considered of little value in evalu-ating renal function in birds; however, plasma ureaappears to be the single most useful variable for earlydetection of prerenal causes of renal failure (dehy-dration).21

These observations can be explained by the fact thaturea is excreted in the kidneys by glomerular filtra-tion, while tubular reabsorption is dependent on tu-bular urine flow, which in turn depends on the stateof hydration. In a hydrated bird, almost all of thefiltered urea is excreted. When a bird is dehydrated,nearly all of the filtered urea is reabsorbed. Thetubular reabsorption of urea in conditions of renalfailure, accompanied by a low urine flow (eg, dehy-dration) in combination with a nearly unchangedexcretion of uric acid, causes a disproportionate in-crease in plasma urea concentration, which results inan elevated urea:uric acid ratio.

Chronic, progressive dehydration may eventuallylead to hyperuricemia. This might be caused by re-duced tubular blood supply that leads to reduced uricacid secretion or by uric acid precipitation in thetubuli caused by active tubular secretion of uric acidin the absence of urine flow. The latter conditionappears similar to acute uric acid nephropathy de-scribed in man.

Postprandial EffectsIt has been demonstrated that a significant post-prandial increase in plasma uric acid (UA) and ureaconcentration occurs in Peregrine Falcons and Red-tailed Hawks.24,25

Postprandial plasma UA levels were similar to thosein birds suffering from hyperuricemia and gout andwere well above the theoretical limit of solubility ofurate in plasma. It is not clear why at least twelvehours of postprandial hyperuricemia does not resultin uric acid deposition in the tissues. The fact thatPeregrine Falcons have relatively high plasma so-dium concentrations might partially explain their

tolerance of high plasma UA levels. In order to pre-vent misinterpretation of high plasma UA levelscaused by the ingestion of food, it is recommendedthat repeat samples be evaluated following a fastingperiod in any bird that initially has a high plasma UAor urea concentration.

Evaluation of Urate TophiMacroscopically, the aspirated material from articu-lar gout looks like toothpaste (Color 21.10). The pres-ence of urate can be confirmed by performing themurexide test or by microscopic examination of aspi-rates from suspected tophi. The murexide test isperformed by mixing a drop of nitric acid with a smallamount of the suspected material on a slide. Thematerial is dried by evaporation in a flame and al-lowed to cool. One drop of concentrated ammonia isadded, and if urates are present, a mauve color willdevelop. Microscopically, sharp, needle-shaped crys-tals can be seen in smears. A polarizing microscope ishelpful in identifying the typical crystals.

Blood ChangesApart from elevated concentrations of nonproteinnitrogen substances, a number of other variables areknown to change in mammals as a result of acute orchronic renal failure. Hyperkalemia, which may leadto severe electrocardiographic changes and cardiacarrest, is a particular problem in acute renal failure.Hyperkalemia (5.2 mmol/l) was described in a Red-tailed Hawk with acute renal failure.24 In man,plasma potassium concentration can be loweredpromptly and for a number of hours by infusion of oneliter of 10% glucose solution containing 10 to 20 IUinsulin; however, in birds, insulin may cause acutehypoglycemia, CNS swelling and death. Infusion of10% calcium gluconate solution may reverse thecardiotoxic effects of severe hyperkalemia withoutaffecting plasma potassium concentration. Hypocal-cemia and hyperphosphatemia are common in mam-mals with renal failure. The former may lead tohypocalcemic tetany, especially with rapid correctionof acidosis. Because these variables have significanttherapeutic implications, documentation of their oc-currence in avian renal disease is necessary. Anemiahas also been documented in birds with chronic renalfailure.


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Clinicopathologic Diagnosisof Renal Dysfunction

Urinalysis

Analysis of urine has been shown to be a valuablediagnostic tool in veterinary medicine. Examinationof urinary sediment and determination of urinaryprotein concentration are the most valuable proce-dures in the differential diagnosis of renal diseases.Renal function tests provide information on the de-gree of functional impairment. Urinalysis may givean early warning of renal damage or impaired renalfunction long before there is an increase in plasmanonprotein nitrogen concentrations. Signs of renaldamage or impaired renal function include prote-inuria, glucosuria without hyperglycemia and castsor cells in urinary sediment.

Despite its high diagnostic value, urinalysis is notroutinely performed in avian medicine, perhaps be-cause it seems difficult to separate urine from feces.Practical guidelines for urinalysis in companionbirds have been developed and are an indispensablepart of the diagnostic workup in polyuric birds.38,39

The identification of casts in urinary sediment isstrongly suggestive of renal disease. In polyuriccases, collection of a urine sample is relatively simpleand can be performed by aspirating the fluid part ofthe excreta into a syringe from a clean enclosure floorcovered by wax paper. It is important that the urinesample be relatively free of urates to ensure thediagnostic value of microscopic examination of thesediment. Sediments obtained from the total renalfraction of the excreta will contain excessive urates;the results are of limited diagnostic value. Clinicallynormal birds have a tendency to become polyuricwhen in a stressful environment (eg, the veterinaryclinic). In these birds, a urine sample is easy to obtainbecause of the bird’s tendency to increase the fre-quency of cloacal emptying when nervous (Color21.13). This will result in the excretion of urine frac-tion that has not moved retrograde into the largeintestine where absorption of water and salts typi-cally occurs.

Urate-free urine samples should be examined forspecific gravity or osmolality, color, clearness, pH,protein, glucose, hemoglobin and the sedimentshould be examined microscopically.

Several methods for collecting avian urine from non-polyuric birds have been reported. The modified cloa-cal cannula method5,15 is the most appropriate forclinical use in docile birds (eg, racing pigeons) be-cause it is the least invasive and is useful underclinical conditions. Reference values for twelvechemical and physical variables established in super-natants of pigeon urine (7000 G for 2 minutes) col-lected with the cloacal cannula method have beenestablished (Table 21.1) and might provide a newperspective for the application of urinalysis in avianmedicine.

TABLE 21.1 Reference Values (P2.5- P97.5) for Pigeon Urine15

Variable Reference Values (SI units)

Urine production 2.3-19.7 ml/kg/h

Osmolality 27-193 mOsmol/kg

Flow-osmol factor 237-1847mOsmol/ml/kg/h

Glucose 0-3.2 mmol/liter

Total protein 0.11-1.99 g/liter

Uric acid 1.2-10.1 mmol/liter

pH 5.5-6.9

Na+ 2.0-27 mmol/liter

K+ 4.0-27 mmol/liter

Inorganic P 0.2-10.9 mmol/liter

Cl– 5.0-56 mmol/liter

NH4+ 4.6-39.5 mmol/liter

Osmolality and Specific GravityThe low urine osmolality as reported in Table 21.1can be explained by the fact that birds can produceurine with a considerably lower osmolality than theosmolality of blood plasma, due to the presence ofreptilian-type nephrons as well as mammalian typenephrons.29,44 High urine osmolalities are common inavian species that are adapted to desert situations(Zebra Finch and budgerigar). Budgerigars can sur-vive long periods (up to a month) without waterunder certain conditions;41 however, domesticatedbudgerigars and finches that are provided free-choicewater may lose much of their compensatory ability.Maximum urine osmolalities in birds vary from 500to 1000 mOsmol/kg.41 The emu is adapted to theAustralian semidesert and has a low turnover rate ofwater, but has a limited renal concentrating abilitywith a maximal urine:plasma osmotic ratio of only1.4:1.5. In this species, the large intestine has beenadapted to preserve water. The high resorptive ca-pacity may be related to increased folding of themucosal surface, which increases the surface area bya factor of five.43


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Nephrology

Color 21.1 In health, the kidneys are dark red-brownand consistent in color. Cranial (k1), middle(k2) and caudal (k3) divisions of the kidneyadhere tightly to the synsacrum in the dor-sal abdominal wall. The right kidney hasbeen removed to show the relationship ofthe kidneys with the synsacrum (s) and thesacral nerve plexus (arrow). Other struc-tures that are easily identified include thelung (lu), left ovary (o) and oviduct (openarrow).

Color 21.2 A Black Palm Cockatoo with a history ofprogressive rear limb ataxia died and waspresented for necropsy. The walls of the leftabdominal and caudal thoracic air sacswere thickened, and a velvet-like yellowmaterial was present on the surface of themembranes (arrow). The cranial and mid-dle divisions of the left kidney and the is-chiatic nerve (open arrow) were also in-volved. Aspergillosis air sacculitis withextension to the kidneys and nerves wasthe cause of death in this bird.

Color 21.3 Birds with decreased renal function maydevelop uric acid deposits (gout) in visceralorgans or in joints. The linear white streaks

within the renal parenchyma in this Afri-can Grey Parrot are characteristic for gout.This was a breeding male that died after abrief period of severe depression. Uric aciddeposits were also present in the pericar-dium and liver (see Color 21.7). Structuresthat are clearly visible are cranial (k1),middle (k2) and caudal (k3) divisions of thekidney, right and left testicles (t), lung (lu),ureter (open arrow), caudal renal vein (ar-row).

Color 21.4 A mature, female African Grey Parrot waspresented for evaluation of severe dyspnea.Radiographs indicated a large mass in theleft thoracic cavity. Histologic evaluation ofa fine-needle aspirate was suggestive ofadenocarcinoma in the lung. A renal massidentified at gross necropsy was confirmedto be a renal adenocarcinoma. This bird hadno clinical changes suggestive of rear limbataxia or weakness, which frequently ac-company renal masses. The ovary (o), ovi-duct (open arrow), ischium (i), external iliacvein (arrow) and ureter (u) are clearly vis-ible.


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Nephrology

Color 21.5 Hemorrhage and swelling of the right cra-nial division of the kidney (arrow) in a ju-venile Umbrella Cockatoo. The left kidney(k) is unusually pale.

Color 21.6 Iron storage disease is a common cause ofdeath in toucans and mynahs. Excessiveaccumulation of iron is usually present inthe liver but can also occur in the kidney(k), as seen in this toucan. These affectedkidneys are swollen and orange in color.Other structures that are clearly visibleinclude the ovary (o), oviduct (arrow) andthe caudal renal vein (open arrow) (cour-tesy of Robert E. Schmidt).

Color 21.7 Deposits of uric acid in the pericardium andliver of an African Grey Parrot with renalfailure (see Color 21.3).

Color 21.8 Multiple urate masses in the kidney of animmature gallinaceous hen in end-stage re-nal failure. Note the immature ovary (o)and oviduct (arrow) coursing over the leftureter; urates are visible near the bottomof the photo (courtesy of R. Korbel).

Color 21.9 Gout in a five-day-old rhea chick. Note thatthe tubules are white and filled with urates(courtesy of Brett Hopkins).

Color 21.10 A mature pigeon was presented for lame-ness and an inability to fly. Prior to dissec-tion, the firm, white, periarticular massescould be visualized through the skin (as inColor 21.12). Cytology of material collectedfrom the masses revealed numerous uric

acid crystals. Articular gout is common insome birds secondary to renal dysfunction.

Color 21.11 A three-year-old budgerigar was presentedwith a two-week history of progressiveataxia and inability to stand. The bird wasfirst noted with dyspnea about threemonths prior to presentation and was se-verely dyspneic during the physical exami-nation. A large mass could be palpated inthe caudal abdomen. Necropsy revealedlarge cystic kidneys. Histologic changes inthe right kidney (rk) were consistent witha renal adenocarcinoma, and the left kid-ney (lk) had undergone cystic changes.

Color 21.12 Articular gout in the elbow of a pigeon withrenal failure (see Color 21.10).

Color 21.13 Polyuria can be caused by excitement, poly-dipsia, high-moisture diets (fruits) or renaldisease. In this case, polyuria in a juvenileBlue and Gold Macaw occurred secondaryto the excitement associated with handling.

Color 21.14 Hematuria is occasionally seen in birds.The blood can originate from the kidneyand ureters, which is rare, or from the gas-trointestinal tract or cloaca, which is com-mon. In this African Grey Parrot, hema-turia was occurring secondary to abacterial nephritis.

Color 21.15 The presence of a large concentration ofWBCs can cause urine to appear cloudy. Inthis cockatiel with severe metritis, bothWBCs and RBCs were identified in theurine by cytology.


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As an alternative to the cloacal cannula method, thefluid part of the excreta (urine) can be recoveredimmediately after excretion. The values for urineosmolality in excreted samples tend to be higher thanthose obtained from cloacal cannula samples. Thismight be explained by water resorption from theurine in the large intestine, which occurs underphysiologic conditions41 but is prevented when usingthe cloacal cannula method. The cloacal cannulamethod would be expected to provide a better impres-sion of the renal concentrating capacity of a patient.

A test for urine concentrating capacity of the racingpigeon has been developed as a model for differentia-tion of polyuric disorders in birds.1 It was concludedthat urine osmolality of 450 mOsmol/kg is indicative ofthe normal concentrating capacity of the kidneys. Inpolyuric birds without a diminished concentrating ca-pacity, one day of water deprivation should be sufficientto cause a demonstrable rise in urine osmolality.

Because the specific gravity of urine has a positivecorrelation with the osmolality, it should be possibleto determine specific gravity of avian urine with arefractometer. Further work is needed to establishthe correlation between refractometric readings andosmometric values before refractometry can be rec-ommended. Some practitioners believe that they canmake an empirical prognostic determination basedon the specific gravity of the urine in a patient.

Polyuria is confirmed by demonstrating hypotonicurine (osmolality, mOsmol/l or specific gravity ).

Flow-osmol FactorThe flow-osmol factor can be defined as the productof the osmolality and urine volume per hour perkilogram. This value provides the limits withinwhich the combination of both factors can be consid-ered to be normal. There is a negative correlationbetween osmolality and urine flow. In this way, a lowurine osmolality and a low urine flow, while bothwithin their respective limits, should be consideredabnormal when their combined value is below thenormal values of the flow-osmol factor.

Nonprotein Nitrogen and pHUric acid concentrations, as mentioned in Table 21.1,are those that are found in supernatants of pigeonurine. The sediment has a much higher concentra-tion of uric acid.

It is known that large quantities of cations aretrapped in uric acid precipitates.32,33,44 The degree ofcation trapping varies from 3-75% for Na+, 8-84% for

K+ and 17-32% for Ca+ and Mg++. This should beconsidered when evaluating the values for these cat-ions provided in Table 21.1. The Cl– concentration inthe urine mainly depends on the concentration ofsodium chloride in the food.

Dietary protein does influence the total ammoniaexcreted but it has little effect on the urine ammoniaconcentration.31 Dehydration produces an increasedammonia concentration in urine, which is caused bythe role of ammonia in regulating the acid-base bal-ance.20 Table 21.1 provides an indication of the pHrange to be expected in the urine of granivorousbirds. Determination of urine pH can be helpful inthe diagnosis of acidosis in birds.a

ProteinIn healthy pigeons, protein concentrations in urinecollected with the cloacal cannula method can be ashigh as 2 g/l. The excretion of mucoproteins andglycoproteins in the distal portion of the nephronsand the ureters is responsible for this low level pro-teinuria.30 Severe, persistent proteinuria is a sign ofincreased glomerular permeability (eg, glomeru-lonephritis). Proteinuria is usually minimal or ab-sent in diseases that primarily involve the tubules orinterstitial tissue. Extreme protein loss through thekidneys can lead to severe hypoproteinemia.

Most urine dip-sticks are too insensitive to distin-guish between moderate and severe proteinuria andmay not properly detect proteinuria in polyuric pa-tients. A false-positive protein result is common inpsittacine birds that have had an alkaline urine. Theuse of the Ponceau S method16 for determination ofurine protein concentration is recommended. Withthis method, protein is precipitated with trichlo-roacetic acid in the presence of the dye Ponceau S.The precipitate is then dissolved in sodium hydrox-ide, and the color intensity is measured spectro-photometrically at 545 nm.

GlucoseGlucose is normally absent from chicken urine,6,45

though small quantities (1.6 mmol/l) of monosaccha-rides have been described in ureteral urine samplescollected from birds.42 The glucose concentrationsmentioned in Table 21.1 are too low to be detected byrapid screening tests like Testape.b

Polyuria and polydipsia accompanied by glucosuriado not always indicate diabetes mellitus. Diabetesmellitus can be diagnosed only if elevated plasmaglucose concentrations have been demonstrated. In


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mammals, Fanconi’s syndrome is characterized byrenal glucosuria, hyperaminoaciduria and hyper-phosphaturia, as well as renal loss of potassium,bicarbonate, water and other substances conservedby the proximal tubule. Fanconi’s syndrome shouldbe considered as the final result of any one of manypossible primary insults to proximal tubular func-tion. The syndrome may be inherited or acquired. Acase of renal glucosuria and proteinuria in an AfricanGrey Parrot with severe renal damage was consid-ered to be similar to the Faconi’s syndrome. Gluco-suria is frequently seen in psittacine hens with egg-related peritonitis. The problem is transitory if theperitonitis can be successfully managed.

KetonuriaKetonuria in mammals occurs when fatty acids areused instead of carbohydrates as the body’s mainenergy source. It has been stated that ketonuria is apoor prognostic sign in birds, suggesting that cata-bolic processes lead to mobilization of fat and ketoaci-dosis.39 This statement is probably incorrect for mi-gratory birds. The primary energy source duringmigration is fat. In the premigratory state, the dryweight basis of some migratory birds is two-thirdsfat. When this fat is used for energy during migra-tion, it is broken down to fatty acids and glycerol. Thebody of migratory birds seems to have a metabolicsystem for preventing the accumulation of ketonebodies.12 Diabetes mellitus has been mentioned as acause of ketonuria in birds;11,38 however, in theauthor’s opinion, the clinical importance of ketonurianeeds further clarification.

ColorThe color of urine varies but is generally white oroff-white, pale yellow or light beige. Pigmented fooditems and medications may alter urinary color. B-complex vitamins can cause a yellow or brownishdiscoloration of the urine that can be misinterpretedas bilirubinuria (see Color 8). Berries in the diet cancause a blue-red discoloration of the urine (see Color8). In liver diseases, biliverdinuria may result in agreen-tinged urine (see Color 8).

Microscopic Examination of Urinary SedimentMicroscopic examination of urine sediment is diag-nostic only when evaluating urine that contains rela-tively little uric acid. Furthermore, contamination ofthe urine with nonrenal components, such as feces orblood originating from the cloaca, must be consid-ered. If performed properly, microscopic evaluation ofthe urine and protein determination are the mostimportant methods for early detection of renal dis-

ease. Various cast types and cellular elements can beencountered in urinary sediment (Color 21.15). Cel-lular casts can contain epithelial cells, erythrocytes,leukocytes, bacteria and fungi. Granular casts arecomposed of degraded cellular components. Caststhat have no cellular elements but have a yellow-or-ange color are suggestive of hemoglobin casts.38 Eos-inophilic tubular casts were suspected to containmyoglobin in an ostrich with acute muscle necrosisand toxic nephropathy.37 Clinical experience suggeststhat the transition from cellular or granular casts tohemoglobin casts is a favorable prognostic sign andindicates resolution of the inflammatory process.39

Microorganisms found in urine sediments are usu-ally from fecal contamination; however, high bacte-rial counts in a relatively clean sample, together withurinary cast formation, is indicative of urinary tractinfection. In male birds, sperm cells may be seen onroutine microscopic examination of urinary sedi-ment. Avian urine contains many amorphous urates,but other crystals may sometimes be noted.

Urinary EnzymesTissue enzyme profile studies in racing pigeons22 andbudgerigars26 have shown that renal tissues of thesebirds contain relatively high amounts of various en-zymes. LDH, AST, CPK, AP, GLDH and ALT can befound in decreasing concentrations in renal tissue.From studies in dogs,18 it is known that the enzymesthat are released during renal damage do not enterthe systemic circulation but are voided with theurine. For this reason, determination of urinary en-zyme activities could be of value for the diagnosis ofrenal cell damage, and the severity of cell damagemight be judged by considering the site of origin ofthe various enzymes. For example, GLDH is knownto be a mitochondrial enzyme and is expected to bereleased only after renal cell necrosis in which thecell organelles are damaged. In renal cell degenera-tion only the release of cytoplasmic enzymes is ex-pected to occur. Further experimental studies inbirds are needed.

Abnormal Urine ColorationHematuria is macroscopically visible when 0.1% ofthe urine contains blood (Color 21.14). Chemical teststrips, like Hemastix,c will show a positive reactionwhen 0.002-0.001% of the urine contains blood. Thecombination of microscopic examination of the sedi-ment and the use of a test strip is more sensitive forthe detection of hematuria than when either test isused alone. In mammals, hematuria is alwayspathologic. Red blood cells can originate all along the


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urinary tract. In birds, hematuria is also possiblewhen blood cells from the gastrointestinal and geni-tal tract or cloaca are mixed with the urine sample.In carnivorous birds, the meat diet frequently resultsin a positive reaction. Both hematuria and hemoglo-binuria can be demonstrated using test strips forhemoglobin. Hemoglobinuria will be seen when thereis an increased erythrolysis.

Myoglobinuria can also cause a red coloration ofurine, which cannot be distinguished from hemoglo-binuria on routine chemical urinalysis. Myoglo-binuria can be demonstrated spectrophotometrically.Exertional rhabdomyolysis is well known in a num-ber of mammalian species (eg, man, horse, whippet,kangaroo) and has also been reported in flamingos9,10

and ostriches.37 The resulting myoglobinuria can in-duce a severe toxic nephropathy.

Porphyrinuria is another cause of red coloration ofthe urine. In birds, the most common cause of por-phyrinuria is lead poisoning. Amazon parrots withlead poisoning often produce a red or brown urine,which is assumed to be hemoglobinuria.38 Lead isknown to inhibit the activity of various enzymesinvolved in heme synthesis, which leads to por-phyrinemia and porphyrinuria. Urine that containshigh concentrations of porphyrins is wine-red inmammals. It is possible that the red or brown urineseen in Amazon parrots with lead poisoning is causedby porphyrins mixed with urates rather than hemo-globinuria. Porphyrins in urine will show a red fluo-rescence in ultraviolet light. When the test is nega-tive, a blue fluorescence will be seen.

Radiology of the Urinary Tract

Survey radiographs provide information about thesize, location and radiopacity of the kidneys. Thepaired kidneys are located in the ventral renal fossaeof the synsacrum. The kidneys are surrounded by theabdominal air sacs, which extend as diverticuli be-tween the kidneys and the pelvis. This finding ex-plains why, at least in Psittaciformes, a rim of air canbe seen dorsal to the kidneys. The loss of this dorsalrim of air is seen during pathologic swelling of thekidneys.28 On a lateral radiograph, the kidneys ap-pear as bean-shaped structures posterior to the lastrib. The cranial part is more easily visualized radiog-raphically because the caudal part is superimposedby the intestinal tract and pelvis. On a ventrodorsalradiograph, the kidneys are superimposed by theliver and the intestinal tract. Abnormalities that canbe detected on survey radiographs include swelling

and crystalline inclusions indicative of urate deposits(Figure 21.3).19 Nephrocalcinosis or concrements inthe kidney, ureters or cloaca can also be detected.Barium sulphate contrast of the gastrointestinaltract may be helpful in localizing intra-abdominalspace-occupying lesions such as renal tumors. Occa-sionally, urate tophi of articular gout are visible onradiographs.8

Endoscopy and Biopsy

Endoscopy allows direct visualization of the completeurinary system (kidneys, ureters and cloaca). Theendoscopic approach of choice is through a puncturesite dorsal to the pubic bone and caudal to the is-chium on the left side of the bird (see Chapter 13).23

Although it is feasible to take renal biopsies inhealthy birds,23 there is considerable risk of fatalhemorrhage from this procedure, and it should al-ways be performed with the appropriate equipmentand ample experience.

In visceral gout, urate deposits can be seen on vis-ceral organs, especially the pericardium and cranialborder of the liver capsule (Color 21.7). A ventralmidline approach just caudal to the sternum is pre-ferred to endoscopically evaluate these structures.23

Diseases of the Kidney2,7,13,14,35,37,40

Infectious Diseases

Bacterial InfectionsBacterial infections of the kidney often occur secon-dary to septicemia but may also result from bacteriathat ascend from the cloaca. Staphylococcus, Strepto-coccus, Listeria, Escherichia coli, Klebsiella, Salmo-nella, Yersinia, Proteus, Citrobacter, Edwardsiella,Enterobacter, Morganella, Providencia, Serratia,Pasteurella and Mycobacterium spp. have all beenassociated with nephritis. Diagnostically, WBCevaluation, total protein and protein electrophoresisprovide useful information on the systemic inflam-matory reaction. Bacterial cultures of blood andurine may reveal the causative organism. Mycobac-terial infections often cause monocytosis that can bedemonstrated on a peripheral blood smear.


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Viral InfectionsViral infections are usually multisystemic, althoughsome viruses like avian polyomavirus and infectiousbronchitis virus in chickens demonstrate a trophismfor the kidney. Other viruses that have been associ-ated with renal lesions include Newcastle diseasevirus, paramyxovirus of pigeons, reoviruses, virusesbelonging to the leukosis/sarcoma group and herpes-viruses (eg, Pacheco’s disease virus and pigeon her-pesvirus).

Mycotic InfectionsRenal infarction as a complication of mycelium inva-sion of blood vessels secondary to pulmonary mycoticdisease is common. Abdominal air sac aspergillosiswith renal involvement per continuitatem has alsobeen reported (Color 21.2). In the latter case, is-chiatic nerve involvement resulted in unilateral pa-ralysis.

Parasitic InfectionsGranulomatous nephritis due to Isospora, Crypto-sporidium, Microsporidium an d Encephalitozoonspp. has been reported in a variety of avian species.

Eimeria truncata is a well known cause of renalcoccidiosis in geese. Adult trematodes of Tanaisiabragai can be found in collecting ducts of chickens,turkeys and pigeons.

Noninfectious Diseases

Congenital DefectsAgenesis and hypoplasia of part of the kidneys havebeen described in birds. Compensatory hypertrophyof the intact poles is common (Figure 21.4). Renalcysts have also been described and may be congenitalin origin (Color 21.11). Diagnosis can be made withurography and laparoscopy.

Metabolic DisordersHypervitaminosis D and elevated dietary calciumcan both cause hypercalcemia and lead to depositionof calcium salts in the renal parenchyma (nephrocal-cinosis). Calcinosis of other organs may also be noted.This condition can be detected radiographically, andthe history may indicate oversupplementation of cal-cium or vitamin D in the diet. Nephrocalcinosisshould not be confused with urolithiasis. The latter

FIG 21.3 An African Grey Parrot of unknown age was presented for a pre-purchase examination two years after being imported into thecountry. A CBC and avian profile were unremarkable. Radiographs indicated nephrocalcinosis (arrows). This is considered an abnormalfinding that occurs frequently in African Grey Parrots. Nephrocalcinosis has been associated with hypervitaminosis D.37


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condition is the most prevalent renal disorder oflaying hens. Suggested causes include excess dietarycalcium, low phosphorous and infectious bronchitisvirus. Unilateral or bilateral ureteral concrements ofcalcium urate can lead to postrenal renal failure. Adiagnosis may be possible with cloacal palpation,radiography, excretory urography and endoscopy.

Hypovitaminosis A can cause metaplasia of the epi-thelium of the ureters and collecting ducts and de-creased secretions of mucus in these structures. Thismay lead to precipitation of urates and ureteral im-paction.

AmyloidosisRenal amyloidosis often occurs in Anseriformes in con-junction with amyloidosis of other organs (eg, liver)secondary to chronic inflammation. There is a deposi-tion of amyloid A, a degraded fragment of an acutephase reactant. In ducks, renal amyloidosis can lead tomassive proteinuria and nephrotic syndrome due tosevere glomerular damage. Clinically, this may be rec-ognized as ascites, or edema of the feet and legs.

FIG 21.4 An African Grey Parrot with agenesis of the cranial andmiddle divisions of the right kidney. Visualization of the kidneysis enhanced by the presence of calcium phosphate crystals. Pneu-monia and consolidation of the left air sacs (arrows) are alsopresent (courtesy of Marjorie McMillan).


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Toxic NephropathiesMany nephrotoxins cause renal tubular necrosis in-cluding aminoglycosides, heavy metals, and myco-toxins such as aflatoxin (A. flavus and A. parasi-ticus), ochratoxin (A. ochraceus and Penicilliumviridicatum), oosporein (Chaetomium trilaterale)and citrinin (P. citrinum).

Salt (NaCl) poisoning has been documented in vari-ous species. Salt poisoning via drinking water canlead to right ventricular failure and ascites. Saltpoisoning via food leads to acute renal failure withurate impaction of the ureters. Clinical signs includepolydipsia and polyuria, or anuria if urate impactionof the ureters occurs. The principal toxic effect is animbalance in sodium and potassium homeostasis.Right ventricular failure should be suspected withascites and can be diagnosed by ECG (see Chapters27 and 37).

NeoplasiaBudgerigars have a high incidence of primary renaltumors, especially adenocarcinoma and nephrobla-stoma (younger birds) (Color 21.11). A viral origin hasbeen suggested.35 The kidney is a potential meta-static site for tumors of nonrenal origin, especiallylymphoproliferative diseases (leukosis). Unilateral orbilateral paralysis caused by compression of the ischia-tic nerve is a common clinical sign associated with renalmalignancies in birds (Color 21.4). Abdominal enlarge-ment is common when a renal mass causes caudoven-tral displacement of the ventriculus or ascites. A renaltumor may be radiographically detectable with or with-out the use of barium sul-phate to differentiate themargins of the gastrointestinal tract.

Ureteral ObstructionDisplacement or obstruction of ureteral orifices canoccur due to intestinal or cloacal prolapse or cloacalobstruction caused by fecaliths, uroliths, foreign bod-ies, tumors or inflammatory processes. A bilateralobstruction will rapidly lead to visceral gout. Unilat-eral obstructions will lead to atrophy and compensa-tory hypertrophy of the contralateral kidney.

Renal HemorrhageRenal hemorrhage can be caused iatrogenically dur-ing endoscopy if improper technique is used. Spor-adic renal hemorrhage in male turkeys and Psittaci-formes has been documented with extravasatedblood remaining confined under the renal capsule orretroperitoneally (Color 21.5). It can also occur as acomplication of renal pathology (eg, tumor). Peracutemortality is common.

Therapeutic Considerations

Prerenal Renal Failure

Treatment of prerenal renal failure caused by dehy-dration or shock is usually successful; however, thechallenge is diagnosing and treating the initial causeof dehydration. Rapidly expanding the circulatoryvolume with intravenous fluids will usually restorenormal renal function within hours (see Chapter 15).

Postrenal Renal Failure

The treatment of postrenal renal failure caused byurolithiasis requires removal of the uroliths. This isa substantial surgical challenge. Successful extracor-poreal shock wave lithotripsy for removal of uric acidconcrements in the urinary tract has been reportedin a Magellanic Penguin and may be attempted inother affected birds.27

Acute Renal Failure

Once a diagnosis of acute (reversible) renal failure ismade, immediate and aggressive therapy is indi-cated to prevent further damage. Suggested therapyfor managing uric acid nephropathy in mammalsprovides some insight into the treatment of birdswith a similar condition but different etiology. Acuteoliguric renal failure associated with hyperuricemiaand marked hyperuricaciduria in man occurs spo-radically due to the precipitation of uric acid crystalsin the distal parts of the renal tubules, the collectingducts, the renal pelvis or the ureters.

This condition most frequently occurs secondary tothe administration of cytotoxic drugs or irradiation,whereby the dissolution of a neoplastic mass liber-ates a heavy load of nucleic acid that must be catabol-ized and excreted by the kidneys. The uric acid excre-tion rises suddenly, uric acid precipitates in renaltubules and acute oliguric renal failure ensues. Con-tributing factors include excretion of an acid urinesecondary to metabolic acidosis, dehydration and theuse of uricosuric drugs (adrenocorticosteroids).Plasma uric acid concentrations may be as high as4770 µmol/l (80 mg/dl). Treatment includes main-taining a high alkaline urine flow by infusing manni-tol 20% (1000 mg/kg) every 15-20 min and sodiumbicarbonate supplemented with intravenous fu-


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rosemide. The prognosis for recovery of renal func-tion is good if diuresis can be achieved.46

Successful treatment of a Red-tailed Hawk withacute obstructive nephropathy that was induced byadministration of allopurinol has been reported.24

The bird showed signs of depression 18 hours afterthe third dose of allopurinol was given. Plasma chem-istry revealed hyperuricemia (uric acid 5,721.6µmol/l). A diagnosis of renal tubular nephrosiscaused by oxypurinol, xanthine or uric acid depositsin the tubuli was made. Intravenous and subcutane-ous saline, corticosteroids and furosemide (1 mg/kg)were administered twice daily in an attempt to re-store renal function. Urine production was restoredand, after 24 hours, plasma uric acid concentrationhad decreased to 3,814 µmol/l. Fluid therapy, corti-costeroids and diuretics were continued. Plasma uricacid had decreased to 1,639 µmol/l 72 hours later. Thebird fully recovered after two weeks of intensivetreatment with intravenous fluids and supportivealimentation. Although corticosteroids were used inthis case, these drugs have been shown to be uricosu-ric in man and should be considered contraindicatedin most cases of renal failure.

In anuric/oliguric renal failure, fluid intake in thepatient should be restricted to fluid loss (renal loss,loss from the gastrointestinal tract and insensibleloss of about 20 ml/kg/day). Assessment of fluid re-quirements can be based on this general outline butmust be monitored by daily weight determinationand observation for clinical signs that would indicateoverhydration or dehydration. In patients that areanorectic and not receiving assisted feedings, someallowance should be made to account for tissue ca-tabolism. Losses of 2.5% body weight per day arepossible in totally anorectic parrots. Sodium, potas-sium and protein intake should be discontinued andcalories should be given in the form of fat and carbo-hydrates. Alternatively, a low-protein diet containingall essential amino acids can be given. Furosemideshould be used in an attempt to restore or increaseurine flow and potassium excretion.

In the polyuric phase that follows the anuric phase,fluid and electrolyte balance should be carefullymonitored to prevent dehydration, hyponatremiaand hypokalemia. Intravenous and subcutaneous in-fusions with lactated Ringer’s solution should becontinued on a daily basis. Because bacteria are oftenincriminated as the cause of renal failure, use ofnon-nephrotoxic bactericidal antibiotics that are ef-fective against the most commonly encountered bac-

teria are indicated. A combination of piperacillin andclaforan has been suggested, although these drugshave a similar mode of action.39 Vitamin A supple-mentation is always indicated in hyperuricemia, be-cause hypovitaminosis A is a common cause of renalfailure.

Effects of Drugs

AllopurinolA recent study24 has demonstrated that oral admini-stration of allopurinol does not prevent the occur-rence of physiologic postprandial hyperuricemia inRed-tailed Hawks. Contrary to expected findings,administration of allopurinol caused a severe hype-ruricemia and induced gout in three out of six, clini-cally normal Red-tailed Hawks. This drug is knownto reduce plasma uric acid concentration in man withhyperuricemia. The results of this study seem toindicate that allopurinol is contraindicated for thetreatment of hyperuricemia in Red-tailed Hawks.Previous reports discussing effective therapy in par-rots with allopurinol may have been coincidental36

and related to physiologic variations in plasma UAconcentrations in relation to food intake. Furtherwork is needed in carnivorous and granivorous birdsto establish fasting and postprandial reference inter-vals of plasma UA concentrations and the possibleeffects of allopurinol in birds. Recommendations fortherapy based on single observations in individualbirds must be cautiously applied to the managementof any avian disease (including gout) until researchcan determine that a therapy is safe.

The extreme renal tubular nephrosis observed fol-lowing allopurinol administration in Red-tailedHawks24 might be explained by the formation of oxy-purinol, the relatively insoluble and nephrotoxic end-product of allopurinol. Alternatively, renal damagemight have been caused by the deposition of xanthinecrystals. Xanthine and hypoxanthine are precursorsof uric acid, and concentrations of these substancesincrease when the xanthine oxidase inhibitor, al-lopurinol, is administered. High-pressure liquidchromatography is necessary to determine whichmetabolic product is being deposited in the tubules.Histologic techniques are not sufficient to determinethe character of the deposits in the tubules, becausethey are generally washed away during preparationof the tissues for sectioning.

CorticosteroidsCorticosteroids are known to be uricosuric in man46

and may be contraindicated in avian hyperuricemic


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conditions. Prednisolone has been used in budgeri-gars with renal tumors. The author states that al-though she does not know whether the prednisoloneprolongs life, it may improve the quality of life bydiminishing the pressure on the ischiatic nerve andstimulating appetite.2

Products Mentioned in the Texta. Clinistix, Miles Diagnostics, Elkhart, INb. Testape, Eli-Lily Benelux NV, Amsterdamc. Hemastix, Miles Diagnostics, Elkhart, IN

References and Suggested Reading

1.Alberts H, et al: A water deprivationtest for the differentiation of polyuricdisorders in birds. Avian Pathol17:385-389, 1988.

2.Bauck L: Renal disease in the budg-erigar - A review of cases seen at theWestern College of Veterinary Medi-cine. Proc Assoc of Avian Vet,Toronto, 1984, pp 1-8.

3.Chonko AM, Grantham JJ: Disordersof urate metabolism and excretion. InBrenner BM, Rector FC (eds): TheKidney. Philadelphia, WB SaundersCo, 1981, pp 1023-1055.

4.Cooper JE, Lawton MPC: The urogeni-tal system. In Price CJ (ed): Manualof Parrots, Budgerigars and OtherPsittacine Birds. Cheltenham,Gloucestershire (UK). British Veteri-nary Small Animal Association, pp91-101, 1988.

5.Coulson EJ, Hughes JS: Collection andanalysis of chicken urine. Poult Sci10:53-57, 1930.

6.Dantzler WH: Renal response of chick-ens to infusion of hyperosmotic so-dium chloride solution. Am J Physiol210:640-646, 1966.

7.Eber A, Pallaske-Eber R: Die durch Ob-duktion feststellbaren Geflügelkrank-heiten [Poultry diseases diagnosedpostmortally]. Hannover, Verlag vonM & H Schaper, 1934, pp 262-268.

8.Ekstrom DD, Degernes L: Avian gout.Proc Assoc Avian Vet, Seattle, 1989,pp 130-138.

9.Fowler ME: Miscellaneous water-birds. In Fowler ME (ed): Zoo andWild Animal Medicine. Philadelphia,WB Saunders Co, 1978, p 215.

10.Fowler ME: Stress. In Fowler ME(ed): Zoo and Wild Animal Medicine.Philadelphia, WB Saunders Co, 1978,pp 33-34.

11.Galvin C: Laboratory diagnostic aidsin pet bird practice. Proc 47th AnnMeet Am Anim Hosp Assoc, 1980, pp41-52.

12.George JC, Berger AJ: The energyproblem in bird migration. Avian My-ology. New York, Academic Press,1966, pp 199-223.

13.Gratzl E, Köhler H: Spezielle Patholo-gie und Therapie der Geflügelkrank-heiten [Pathology and Therapy of

Poultry Diseases]. Stuttgart, Ferdi-nand Enke Verlag, 1968.

14.Greenacre CB, Latimer KS, Ritchie BW:Leg paresis in a black palm cockatoo(Probosciger aterrimus). J Zoo &Wildl Med 23(1):122-126, 1992.

15.Halsema WB, et al: Collection andanalysis of urine in racing pigeons(Columba livia domestica). AvianPathol 17:221-225, 1988.

16.Hendriks HJ, Haage A, De Bruijne JJ:Determination of the protein concen-tration in canine urine. Zentralblattfür Veterinärmedizin A 23: 683-687,1976.

17.Johnson OW, Muggaas JN: Some his-tological features of the avian kid-neys. Am J Anatomy 127:423-436,1970.

18.Keller P: Enzymaktivitäten in Or-ganen, Zellfraktionen und Körperflüs-sigkeiten des Hundes unter speziel-len Berücksichtigung klinisch-diag-nostischer Aspekte und der an-aeroben Glykolyse [Enzyme activitiesin organs, cell fractions and body flu-ids with special attention for clinicaldiagnostic aspects and anaerobic gly-colysis]. Basel, F. Hoffmann-La Ro-che & Co, AG, 1984.

19.Krautwald-Junghanns ME: Radio-graphic examination of the urinarysystem of birds with organic iodi-nated contrast media. Proc 1st IntlConf Zoo & Avian Med, Hawaii, 1987,pp 177-193.

20.Long S: Acid-base balance and uri-nary acidification in birds. Comp Bio-chem Phys 71(A):519-526, 1982.

21.Lumeij JT: Plasma urea, creatinineand uric acid concentrations in re-sponse to dehydration in racing pi-geons (Columba livia domestica).Avian Pathol 16:377-382, 1987.

22.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.

23.Lumeij JT, Hasselaar JC: Endoscopicapproaches for the racing pigeon (Co-lumba livia domestica). In Lumeij JT:A Contribution to Clinical Investiga-tive Methods for Birds, with SpecialReference to the Racing Pigeon, Co-

lumba livia domestica. PhD Thesis,Utrecht University, 1987, pp 152-158.

24.Lumeij JT, Redig PT: Hyperuricaemiaand visceral gout induced by allopuri-nol in red-tailed hawks (Buteojamaicensis). Proc Tagung Vogelk-rankheiten der Deutsche Veterinar-medizinische Gesellschaft e.V.,München, 1992.

25.Lumeij JT, Remple JD: Plasma urea,creatinine and uric acid concentra-tions in relation to feeding in pere-grine falcons (Falco peregrinus).Avian Pathol 20:79-83, 1991.

26.Lumeij JT, Wolfswinkel J: Tissue en-zyme profiles of the budgerigar(Melopsittacus undulatus). In LumeijJT: A Contribution to Clinical Investi-gative Methods for Birds, with Spe-cial Reference to the Racing Pigeon,Columba livia domestica. PhD The-sis, Utrecht University, 1987, pp 71-77.

27.Machado C, et al: Disintegration ofkidney stones by extracorporealshockwave lithotripsy in a penguin.Proc 1st Intl Conf Zoo & Avian Med,Hawaii, 1987, pp 343-349.

28.McMillan MC: Avian radiographic di-agnosis. Proc Assoc Avian Vet, Hous-ton, 1988, pp 301-308.

29.McNabb FMA: Kidneys. In Abs M(ed): Physiology and Behaviour of thePigeon. London, Academic Press,1983, pp 42-53.

30.McNabb FMA, McNabb RA, Steeves HR:Renal mucoid materials in pigeonsfed high and low protein diets. Aukjaf90:14-18, 1973.

31.McNabb FMA, McNabb RA, Ward JM:The effects of dietary protein contenton water requirements and ammoniaexcretion in pigeons, Columba livia.Comp Biochem Phys 43(A):181-185,1972.

32.McNabb RA, McNabb FMA: Urate ex-cretion by the avian kidney. CompBiochem Phys 51(A): 253-258, 1975.

33.McNabb RA, McNabb FMA: Avian uri-nary precipitates: Their physicalanalysis and their differential inclu-sion of cations (Ca, Mg) and anions(Cl). Comp Biochem Phys 56(A):621-625, 1977.

34.McNeel SV: Avian urography. J AmVet Med Assoc 178:366-368, 1981.

35.Neumann U, Kummerfeld N: Neo-plasms in budgerigars: Clinical,pathomorphological and serologicalfindings with special consideration ofkidney tumors. Avian Pathol 12:353-362, 1983.

36.Petrak, ML: Diseases of Cage and Avi-ary Birds. Philadelphia, Lea & Fe-biger, 1982, pp. 643-645.

37.Phalen DN, Ambrus S, Graham DL:The avian urinary system: Form,function, diseases. Proc Assoc AvianVet, Phoenix, 1990, pp 44-57.

38.Rosskopf WJ, Woerpel RW, Lane RA:The practical use and limitations ofthe urinalysis in diagnostic pet avianmedicine: With emphasis on the dif-ferential diagnosis of polyuria, theimportance of cast formation in theavian urinalysis and case reports.Proc Assoc Avian Vet, Miami, 1986,pp 61-73.

39.Rosskopf WJ, Woerpel RW: Kidneydisease in a military macaw, a yel-low-naped Amazon parrot, and anumbrella cockatoo. Proc Assoc AvianVet, Houston, 1988, pp 207-218.

40.Siller WG: Renal pathology of thefowl- a review. Avian Pathol 10:187-262, 1981.

41.Skadhauge E: Osmoregulation inbirds. Berlin, Springer Verlag, 1981.

42.Skadhauge E: Formation and compo-sition of urine. In Freeman BM (ed):Physiology and Biochemistry of theDomestic Fowl vol IV. London, Aca-demic Press, 1983, pp 107-133.

43.Skadhauge E, Maloney SK, Dawson TJ:Osmotic adaptation of the Emu (Dro-maius novaehollandiae). J CompPhys B161:173-178, 1991.

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45.Sperber I: Excretion. In Marshal AJ(ed): Biology and Physiology of Birdsvol I. London, Academic Press, 1960,pp 469-492.

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