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Avian renal disease: Endoscopic applications
Avian Renal Disease: Endoscopic Applications MichaelJ. Murray, DVM, and Michael Taylor, DVM
Avian renal disease may occur as a result of bacterial, viral, or parasitic infections; metabolic dysfunction; congenital deformity; toxic insults; or nutritional deficiencies or excesses. In an attempt to diagnose these maladies, a number of ancillary techniques have been advocated for use by the avian clinician. Serum or plasma biochemical parameters, such as uric acid, urea, creatinine, or creatine are either nondiagnostic or do not elevate until pathology has become substantial. Alterations in the urine, as noted in the urinalysis, further aid in the detection of renal disease, but are also typically nonspecific. Other noninvasive diagnostic imaging techniques, such as radiography, ultrasonography, computed tomographic {CT) scans, or magnetic resonance imaging, play limited roles as a result of their cost or inability to provide a definitive diagnosis in most cases. Rigid endoscopy with its inherent focal, directed illumination with magnification allows the clinician the opportunity to directly visualize the urinary system, as well as to collect biopsy specimens that may provide an etiopathogenic diagnosis.
Copyright 9 1999 by HI. B. Saunders Company. Key words: Avian, endoscopy, renal, biopsy, kidney, ureter, laparoscopy, uric acid.
lthough accurate statistics are not available for pet birds, the incidence of renal disease in p o s t m o r t e m surveys of poultry has varied from approximately 3% to 15%. 1 Diagnosis and treatment of disease in the urinary system have been h a m p e r e d by the clinician's limited armam e n t o f diagnostic techniques. The recent develo p m e n t of fine diameter, rigid endoscopic equipm e n t with a system for sample collection has allowed the high resolution examination o f the urinary system, as well as facilitating the collection of precise, targeted biopsy specimens. 2 O f p a r a m o u n t importance in the use of this technology is its application early in the progression o f disease. Biops)4ng the end-stage kidney provides little information of value to either the patient or the client. A traditional left lateral laparoscopic approach will permit access to the abdominal air sac via the caudal thoracic air sac. The focal, directed illumination with magnification enables the visual inspection of the kidney, ureter, and cloaca in most avian species. Appropriate biopsy specimens may then be safely collected using this minimally invasive technique.
A
Anatomy and Physiology The anatomy of the avian kidney encourages the use of relatively small biopsy forceps for the collection of diagnostic samples. The kidneys are paired organs, lying within the symmetrical bony depressions of the renal fossae in the ventral synsacrum. Each kidney is divided into three segments, the cranial, middle, and caudal dMsions. In some species, such as the passerines, the distinction between the last two divisions is blurred. In Spheniscidae (penguins) and Ardeidae (herons), the caudal divisions are fused across the midline. 3 In most species, the boundaries between the three divisions are f o r m e d by the external iliac artery (cranial and middle divisions) and the ischiatic artery (middle and caudal divisions). The architecture of the avian kidney is based on renal lobules, which can be easily recognized as small r o u n d e d projections on the surface of the kidne~ when viewed with the endoscope. Each lobule may be described as a pear-shaped wedge, containing both cortical and medullary tissue, located between the interlobular veins of the renal portal system. An intralobular artery and vein supply each lobule. The collecting tubules for each lobule are interlobular. This arrangement is opposite that of the mammalian kidney, in which the collecting tubules are intralobular and the arteries are interlobular. T h e widest portion of the pear, the cortical region, then drains into the m o r e narrow medullary region where the medullary collecting tubules converge to form collecting ducts that eventually combine to form the secondary, then primary branches of the ureter. Unlike the mammal, the lobules, and there-
From Avian & Exotic Clinic of the Monterey Peninsula, Monterey, CA, and Ontario VeterinaryCollege, Universityof Guelph, Guelph, Ontario, Canada. Address correspondenceto MichaelJ. Mum'ray,DVM, Avian & Exotic Clinic of the Monterey Peninsula, 2 Harris Ct, Ste A-I, Monterey, CA 93940. Copyright9 1999 by W. B. Saunders Company. 1055-937X/99/0803-0005510. 00/0
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fore the lobes, are f o u n d at varying depths within the kidney. As a result, one c a n n o t visualize defined borders between the cortex and medulla. In essence, the greater areas of cortex s u r r o u n d relatively small, cone-shaped regions of medulla. T h e r e are two types of n e p h r o n within the avian kidney. T h e cortical type nephr o n is confined to the cortical r e g i o n of the kidney and lacks the loop of Hen~'le. This reptilian f o r m of n e p h r o n is uricotelic, secreting uric acid in the f o r m o f a precipitate. 4 As most uric acid is secreted and not filtered, levels within the b l o o d do not rise in the face of mild to m o d e r a t e dehydration or decreased g l o m e r u l a r filtration rate. 5 From an endoscopic perspective, however, the accumulation of uric acid within the tubules in the face of decreased urine flow secondary to dehydration creates a visible pale striation to the kidney. Unless long-standing or exceptionally severe, the r e t u r n to n o r m a l hydration status will result in spontaneous resolution of this condition. T h e m a m m a l i a n or medullary n e p h r o n produces urine and does have the intermediate segment, the loop of Henle. 6 T h e distribution of these two types of nephron, medullary (or m a m m a l i a n ) and cortical (or reptilian), is clinically relevant when considering endoscopic renal biopsy. Fortunately, the lobules containing b o t h cortical and medullary nephrons are e m b e d d e d in varying depths within the kidney. Therefore, the typical 3- or 5-French (Fr) biopsy specimen is likely to contain b o t h nephr o n types. 7 T h e ureter is f o r m e d by the confluence of a n u m b e r of p r i m a r y branches. It is initially visualized as it emerges f r o m u n d e r the lliac atery at the cranio-medial b o r d e r of the middle division of the kidney (Fig 1). T h e ureter continues caudally and slightly medially within a groove on the ventral surface of the middle and caudal divisions. T h e ureters then o p e n into the urod e u m on its dorsolateral aspect. Typically, the ureters enter the cloaca m o r e dorsally to the m o r e lateral position of the genital d u c t s . 7 T h e arterial supply to the kidney arises f r o m the cranial, middle, and caudal renal arteries. T h e cranial renal artery tends to be m o r e superficial; therefore, the cranial division may be less desirable as a biopsy site. A venous vascular ring, the renal portal system, surrounds the kidneys. This system allows shunting of b l o o d into the caudal vena cava, into the caudal mesenteric vein
Figure 1. Left cranial and middle divisions of a normal cockatoo kidney. The iliac artery and vein separate the two divisions. The ureter is visible as it emerges from the middle division. Note the normally melanistic testicle in this bird. and towards the liver, or into the internal vertebral venous plexus within the vertebral canal. 7 T h e presence of the renal portal system has theoretical clinical significance when assessing the administration of drugs with p r i m a r y renal metabolism into the pelvic limb. T h e practical consequences have yet to be totally elucidated.
Indications for Endoscopy of the Urinary System Although there are no truly p a t h o g n o m o n i c signs of renal disease, the clinician is e n c o u r a g e d to consider renal disease as a rule-out whenever a patient is presented with a change in urinary output. Polyuria, the most c o m m o n change noted, may be mistaken for diarrhea by the client. Unlike diarrheic droppings, tile polyuric d r o p p i n g contains a n o r m a l fecal mass surr o u n d e d by an increased a m o u n t of fluid (urine). For reasons that are not clearly understood, birds subjected to the stress of transportation and presentation to the veterinary facility will often pass polyuric droppings. Such changes may be the result of increased urine p r o d u c t i o n or
Avian Renal Endoscopy
decreased urine resorption. 8 To avoid misinterpreting the artifacturally altered data, clients should be instructed to present the most recent 24 hours of cage p a p e r for evaluation at the time of the examination. Stress associated with reproduction may result in polyuria. Similarly, elevated environmental t e m p e r a t u r e may result in poydipsia a n d secondary polyuria. Obviously, high water intake in the f o r m of high water content foods may affect the droppings, as well. Collection of a complete history by the clinician is essential. Systemic disease may also cause polyuria. Infectious agents, such as chlamydia, viral, and bacterial organisms, may cause increased urine production. 9 T h e exact etiopathogenesis of this clinical observation is not totally understood. T h e polyuric effect of hyperglycemia is well d o c u m e n t e d . M t h o u g h polyuria is the most c o m m o n alteration in urinary output, oliguria and anuria may occasionally be noted. T h e inability to identify the exact cause of any change in urinary output warrants endoscopic examination of the urinary tract. Mterations in urine color may suggest renal dysfunction; however, most changes are caused by dysfunction in o t h e r organ systems. Biliverdinuria is a result of liver disease or hemolysis. As the circulating levels of biliverdin elevate, the renal threshold is exceeded, and the excess is excreted in the urine. H e m o g l o b i n u r i a or h e m a t u r i a may also indicate renal disease. T h e classically described h e m o g l o b i n u r i a associated with heavy metal intoxication in Amazon parrots (Amazona sp) may not be n o t e d in o t h e r speciesJ ~ H e m a t u ria, on the o t h e r hand, may occur secondary to diseases of the kidney, ureter, or cloaca. Most cases of frank blood in the droppings are associated with cloacal disease. 9 T h e endoscope may be used not only to p e r f o r m the traditional coelomic examination, but also to thoroughly examine the cloaca, u T h e unilateral lameness/paresis associated with renal neoplasia in the budgerigar (Melopsittacus undulatus) is a familiar clinical presentation for the avian practitioner. Similar unilateral or bilateral pelvic limb dysfunction may be observed in cases of renal inflammation. T h e intimate association of the l u m b a r and sacral plexuses as they course through the renal p a r e n c h y m a may result in lower m o t o r n e u r o n signs in certain renal diseases.
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Clinicians too often base the presence or absence of renal disease on the plasma uric acid level (Fig 2). It is, however, too insensitive to rely on solely for the evaluation of renal function. Uric acid is synthesized by the liver and then excreted via tubular secretion by the medullary (reptilian) nephrons, i n d e p e n d e n t of glomerular filtration rate, state of hydration, and of tubular water resorption. 5 Therefore, hyperuricemia is not the result of dehydration, but only is manifested w h e n renal function is below 30% of its original capacity. 12 Birds c o n s u m i n g a high protein meal may exhibit a transient postprandial h y p e r u r i c e m i a J 3 Repeated, fasting samples normally will show uric acid levels within n o r m a l limits. Therefore, an isolated elevation of plasma uric acid does not in itself warrant endoscopic e x a m i n a t i o n . Persistent elevations, or those coupled with o t h e r evidence of renal disease, however, strongly indicate such a diagnostic step (see Table 1). Additionally, serial uric acid determinations showing a rise within the reference range may justify endoscopic examination. Urea is n o t c o m m o n l y evaluated in avian clinical medicine. Only small amounts are produced; therefore, its application is limited) 3 Unlike uric acid, urea is eliminated by glomerular filtration a n d is not resorbed in the n o r m a l bird. T h e r e is, however, a significant elevation in s e r u m urea concentration secondary to renal resorption in the dehydrated bird. 5 Despite this,
Figure 2. Urate accumulations in kidney tubules of an Amazon parrot. This bird had a reference-range plasma uric acid.
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Table 1. Indications for Renal Endoscopy Unexplained changes in urine output: Persistent elevations in uric acid: Difficultymaintaining hydration LethargT and/or weight loss
Especiallypolyuria Fast carnivorous birds, use serial sampling
the clinical significance of blood urea is probably limited in avian nephrology. The applicability of creatinine and creatine to avian renal disease is not well understood. Little creatinine is produced in the bird from its precursor, creatine. 9 The urinalysis is a frequently overlooked, but potentially valuable diagnostic tool in the management of avian renal disease. It is obvious that urine evaluation requires a polyuric patient and careful segregation of the urine from the associated fecal c o m p o n e n t o f the dropping. If the specimen contains flocculent material, it should be clarified by centrifugation before chemical evaluation. Standard dipsticks may be used; however, not all components of the mammalian p r o d u c t are applicable. 9 Urine p H may be influenced by cloacal contents, as well as diet. Proteinuria is typically expected, however, the quantity decreases with increased urine dilution in the normal bird. Glucose is generally present to a trace amount, however, its significance should not be overinterpreted without confirmatory blood glucose determinations. Ketones are not normally present in the urine, but may be n o t e d in individuals that are beta-oxidizing fats secondary to starvation or migration. 14 Evidence of blood or hemoglobin is not normal. One should ensure, however, that the positive test is not the result of myoglobin associated with recent animal muscle meals. Neither bilirubin n o r urobilinogen are expected to be in the urine of the bird. The lack of biliverdin reductase precludes the formation of bilirubin as the end product of hemecatabolism. 12 As a result, urobilinogen will not be formed, as it is p r o d u c e d by the bacterial alteration of conjugated bilirubin in the gastrointestinal tract. Examination of the urine sediment is important in the evaluation of renal disease. Unfortunately, sediment examination is complicated by the relatively large quantity of urate precipitate. Despite this difficulty, the presence of cellular or proteinaceous urinary casts, leukocytes, a n d / o r erythrocytes may indicate renal disease. The sedimentary c o m p o n e n t of the urine is generally
quite labile and is best evaluated immediately, rather than being submitted to a reference laboratory for examination. Changes in the radiographic appearance of the kidneys or perirenal structures may be an indication for endoscopic examination. Loss of the dorsal diverticulum of the abdominal air sac separating the dorsal aspect o f the kidney from the ventral synsacrum may suggest renal enlargement. 9 This change may be artifacturally produced by i m p r o p e r positioning of the lateral exposure. Gross changes in the size of the kidney may be noted, but should not be overinterpreted, as the cranial division may seem enlarged because of its intimate relationship with the gonad and adrenal gland. Increased density of the renal silhouette is often associated with small kidneys. Radiographic evidence of mineralization of the kidney is occasionally noted. The "self insuffiation" of the bird through its air sac system has tremendous advantages for the endoscopist, but limits the use of diagnostic ultrasound for evaluation of the avian urinary system. CT scans and magnetic resonance imaging are both potentially valuable diagnostic tools, but exceed the resources of most veterinary facilities. One of the most c o m m o n indications for renal biopsy is the visual identification of changes in size, shape, color, or consistency of the kidney during routine endoscopic examination for sex identification (Fig 3). Any deviations from the expected normal for the age/species should warrant further work-up. In most cases, the actual biopsy p r o c e d u r e is p r e c e d e d by establishm e n t of m i n i m u m database parameters, as they are generally not obtained during routine "surgical sexing." Other, nonspecific signs of renal disease include lethargy, anorexia, dehydration, regurgitation, generalized weakness, and weight loss. Any of these signs that may be clinically related to the urinary system may warrant endoscopic examination. The clinician is encouraged to aggressively pursue a definitive diagnosis early in the progression of renal disease. Discussion of the potential for endoscopic examination and potential biopsy early in the diagnostic work-up may enhance client acceptance of the procedure, should it become indicated. It is readily apparent that the minimally invasive nature of the fine diam-
Avian Renal Endoscopy
Figure 3. Chronic renal damage may lead to changes in the normal appearance of the parenchyma. This parrot has a very irregular kidney surface caused by chronic, ongoing renal disease. eter rigid e n d o s c o p e coupled with the relative safety of isoflurane anesthesia has resulted in m o r e routine recognition of the i m p o r t a n c e of this technology in the diagnosis and t r e a t m e n t of avian renal disease.
Technique T h e kidneys may be a p p r o a c h e d for either visual examination or biopsy t h r o u g h the traditionally described caudal thoracic air a p p r o a c h and subsequent advance into the abdominal air sac. In this approach, the bird is anesthetized a n d placed in lateral recumbency. T h e wings are e x t e n d e d dorsally and fixed in that position. T h e dorsally positioned leg is e x t e n d e d cranially to expose the area caudal to the last rib. A small skin incision is t h e n m a d e over the area the semitendinosus muscle (m. flexor cruris medialis) crosses the last rib. ~5T h e entry point into the caudal thoracic air sac is then m a d e by bluntly dissecting t h r o u g h the thin body wall musculature just ventral to the flexor cruris medialis. In most species, directing the tip of the telescope slightly cranially a n d medially will p e r m i t entry into the caudal thoracic air sac (CTAS). Entry into the abdominal air sac (AAS), in which the kidney and associated structures may be visualized, is t h e n m a d e by passing the telescope
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t h r o u g h the confluent CTAS/AAS m e m b r a n e located medially f r o m the entry point. An entry p o i n t directly into the AAS may allow better access a n d visualization of the caudal division of the kidney. T h e entry for this postpubic a p p r o a c h is located dorsal to the pubic b o n e and caudal to the ischium. After entry into the most caudal aspect of the intestinal peritoneal cavity, the telescope can advance t h r o u g h the air sac wall into the AAS. At this point, the tip of the telescope is located at the caudal-most aspect of the caudal division of the kidney, looking cranially. 15 Once located within the abdominal air sac, the endoscopist should p e r f o r m a complete examination of the urinary system, as well as all o t h e r coetomic structures available for visualization. T h e entire kidney f r o m its most cranial aspect to its caudal pole should be inspected, initially from some distance and then with greater magnification by moving closer to the tissue. As the tip o f the telescope a p p r o a c h e s the kidney, the clinician will notice an increase in magnification without any loss of detail and resolution. T h e unique optical qualities of m o d e r n small diameter r o d lens telescopes m a k e this clinically useful application possible. W h e n the CTAS a p p r o a c h has b e e n used, the caudal division may be m o r e difficult to examine. Use of the 30 degree offset of the lens tip will enhance the endoscopist's ability to complete the examination. T h e u r e t e r should be followed f r o m its origin to its entry point into the u r o d e u m on the dorsolateral aspect of the cloaca. Although most cases of renal disease are diffuse, occasionally focal disease is encountered. W h e n suspected, a second laparoscopic a p p r o a c h may be indicated with entry on the contralateral side. We advocate the use of aseptic technique for the entire endoscopic procedure. A one- to two-layered closure after removal of the instrumentation is r e c o m m e n d e d using a fine absorbable monofilim e n t suture. T h e d e v e l o p m e n t of a sheath system with an integral i n s t r u m e n t channel allows the delivery of biopsy forceps of a variety of sizes directly to the area visualized by the lens system. 15 Elliptical or r o u n d c u p - s h a p e d biopsy forceps of 3- or 5-Fr size are typically used to collect biopsy specimens f r o m small- to medium-sized birds (Fig 4). These instruments facilitate control of specimen size and d e p t h of penetration, with the 3-Fr r o u n d
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Figure 4. Renal biopsy site in an Amazon parrot 2 minutes'after collection of a 7-Fr kidney biopsy. This is the maximal biopsy recommended for a bird of this size. A 5-Fr cup would be better suited to this bird's kidney mass. cup having the most shallow depth. T h e apparently minute size of the forcep cup nmst be correlated to the size of the renal tissue. It is also i m p o r t a n t that the cutting edges of the biopsy instruments be kept clean and sharp. Excessive force used to excise the tissue may create substantial crushing artifact. Dull instruments may result in an iatrogenic avulsion of the kidney f r o m its sulcus, as the forceps tear rather than cut tissue. Biopsy site selection is d e p e n d e n t on the nature of the disease encountered. In those cases of obviously diffuse disease, ease of access, distance f r o m vasculature, and distance f r o m ureter and genital tract are d e t e r m i n i n g factors in selection of the site. In the case of m o r e focal disease, the biopsy must be targeted, using discretion in the d e p t h of sampling and proximity to vessels and tubular organs. Regardless of the site selected, the o p e r a t o r must be very cautious to avoid vital structures and large vessels. Despite prior publications to the contrary, 12 most hemorrhages are m i n o r and self-limiting. In those cases warranting further hemostasis, direct pressure using the closed biopsy forceps is typically adequate. W h e n possible, the collection of a minim u m of two samples is encouraged. As previously reported, n u m e r o u s renal biop-
sies using the techniques described have b e e n p e r f o r m e d without incident. 16T h e typical instrum e n t a t i o n employed is a 2.7-mm, 30-degree f o r w a r d / o b l i q u e rigid telescope, 14.5-Fr sheath with a 5-Fr i n s t r u m e n t channel. 15,16 In most cases, the biopsy forceps of choice has b e e n a 5-Fr elliptical cup forceps. This p r o c e d u r e has b e e n p e r f o r m e d by us on birds as small as 27 g safely without significant postbiopsy h e m o r rhage. Historically, the concept of renal biopsy has b e e n addressed with a great deal of trepidation. Recent advances in diagnostic endoscopy have facilitated the use of this technology for the diagnosis of a variety of clinical diseases that has thus far b e e n possible only on necropsy. T h e use of the macroscopic laparotomy to p e r f o r m a renal biopsy, although possible, does not enhance one's ability to visualize a n d select specim e n collection sites. T h e degree of tissue trauma is also m u c h greater. A recently described dorsal pelvic a p p r o a c h to renal biopsy 17 does not permit specific targeting of renal parenchyma, does not allow a complete and t h o r o u g h examination of the urinary system, and as an osteotomy is required, must involve a significantly m o r e painful recovery. T h e use of the endoscope is a relatively simple technique, easily mastered with practice, which will enhance the diagnostic capabilities of any avian practitioner. Its potential in the minimally invasive diagnosis of renal disease remains u n t a p p e d .
References 1. Siller WG: Renal pathology in the fowl A review. Avian Pathol 10:187-262, 1982 2. Taylor M: Diagnostic application of a new endoscopic system for birds. Proc Eur Conf Avian Med Surg 127-131, 1993 3. Orosz S: Anatomy of the urogenital system, in Altman RB, Clubb SL, Dorrestein GM, Quesenberry K (eds): Avian Medicine and Surgery. Philadelphia, PA, Saunders, 1997, pp 614-622 4. Skadhauge E: Osmoregulation in Birds. Heidelberg, Germany, Springer-Verlag, 1981, pp 84-91 5. Lumeij JT: Plasma urea, creatinine and uric acid concentrations in response to dehydration in racing pigeons (Columbia livia domestica). Avian Pathol 17:851-864, 1987 6. Sturkie PD: Kidneys, extrarenal salt excretion, and urine, in Sturkie PD (ed): Avian Physiology (ed 4). New York, NY, SpringeI:Verlag, 1986, pp 359-382 7. King AS, McLelland J: Birds Their Structure and Function. London, UK, Baillere-Tindall, 1984, pp 175-186 8. Palmore WP, Fregly MJ, Simpson CE: Catecholamine-
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9. 10.
11.
12.
13.
induced diuresis in turkeys. Proc Soc Exp Biol Med 167:1-7, 1981 Styles DK, Phalen DN: Clinical avian urology. Semin Avian Exotic Pet Med 7:104-113, 1998 Woerpel RW, Rosskopf WJ: Heavy metal intoxication in caged birds: Parts I, II. Comp Cont Ed Pract Vet 4:191196, 1982 Speer BL: Diseases of the urogenital system, in Altman RB, Clubb SL, Dorrestein GM, Quesenberry K (eds): Avian Medicine and Surgery. Philadelphia, PA, Saunders, 1997, pp 625-633 Lumeij JT: Nephrology, in Ritchie BW, Harrison GJ, Harrison LR (eds): Avian Medicine: Principles and Application. Lake Worth, FL, Wingers, 1994, pp 538-555 Lumeij JT, Remple JD: Plasma urea, creatinine and uric
14.
15.
16.
17.
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acid concentrations in relation to feeding in peregrine falcons (Falcoperegrinus).Avian Pathol 20:79-83, 1991 Phalen DN, Ambrus S, Graham DL: The avian urinary system: Form, function, and diseases. Proc Assoc Avian Vet 44-57, 1990 Taylor M: Endoscopic examination and biopsy techniques, in Ritchie BW, Harrison GJ, Harrison LR (eds): Avian Medicine: Principles and Application. Lake Worth, FL, Wingers, 1994, pp 32%354 Murray MJ, Taylor M: The use of endoscopy and endoscopic biopsy as aids in the diagnosis of renal disease. Proc Assoc Avian Vet 133-138, 1997 Suedmeyer WK, Bermudez A: A new approach to renal biopsy in birds.J Avian Med Surg 10:179-186, 1996
Avian renal disease may occur as a result of bacterial, viral, or parasitic infections; metabolic dysfunction; congenital deformity; toxic insults; or nutritional deficiencies or excesses. In an attempt to diagnose these maladies, a number of ancillary techniques have been advocated for use by the avian clinician. Serum or plasma biochemical parameters, such as uric acid, urea, creatinine, or creatine are either nondiagnostic or do not elevate until pathology has become substantial. Alterations in the urine, as noted in the urinalysis, further aid in the detection of renal disease, but are also typically nonspecific. Other noninvasive diagnostic imaging techniques, such as radiography, ultrasonography, computed tomographic {CT) scans, or magnetic resonance imaging, play limited roles as a result of their cost or inability to provide a definitive diagnosis in most cases. Rigid endoscopy with its inherent focal, directed illumination with magnification allows the clinician the opportunity to directly visualize the urinary system, as well as to collect biopsy specimens that may provide an etiopathogenic diagnosis.
Copyright 9 1999 by HI. B. Saunders Company. Key words: Avian, endoscopy, renal, biopsy, kidney, ureter, laparoscopy, uric acid.
lthough accurate statistics are not available for pet birds, the incidence of renal disease in p o s t m o r t e m surveys of poultry has varied from approximately 3% to 15%. 1 Diagnosis and treatment of disease in the urinary system have been h a m p e r e d by the clinician's limited armam e n t o f diagnostic techniques. The recent develo p m e n t of fine diameter, rigid endoscopic equipm e n t with a system for sample collection has allowed the high resolution examination o f the urinary system, as well as facilitating the collection of precise, targeted biopsy specimens. 2 O f p a r a m o u n t importance in the use of this technology is its application early in the progression o f disease. Biops)4ng the end-stage kidney provides little information of value to either the patient or the client. A traditional left lateral laparoscopic approach will permit access to the abdominal air sac via the caudal thoracic air sac. The focal, directed illumination with magnification enables the visual inspection of the kidney, ureter, and cloaca in most avian species. Appropriate biopsy specimens may then be safely collected using this minimally invasive technique.
A
Anatomy and Physiology The anatomy of the avian kidney encourages the use of relatively small biopsy forceps for the collection of diagnostic samples. The kidneys are paired organs, lying within the symmetrical bony depressions of the renal fossae in the ventral synsacrum. Each kidney is divided into three segments, the cranial, middle, and caudal dMsions. In some species, such as the passerines, the distinction between the last two divisions is blurred. In Spheniscidae (penguins) and Ardeidae (herons), the caudal divisions are fused across the midline. 3 In most species, the boundaries between the three divisions are f o r m e d by the external iliac artery (cranial and middle divisions) and the ischiatic artery (middle and caudal divisions). The architecture of the avian kidney is based on renal lobules, which can be easily recognized as small r o u n d e d projections on the surface of the kidne~ when viewed with the endoscope. Each lobule may be described as a pear-shaped wedge, containing both cortical and medullary tissue, located between the interlobular veins of the renal portal system. An intralobular artery and vein supply each lobule. The collecting tubules for each lobule are interlobular. This arrangement is opposite that of the mammalian kidney, in which the collecting tubules are intralobular and the arteries are interlobular. T h e widest portion of the pear, the cortical region, then drains into the m o r e narrow medullary region where the medullary collecting tubules converge to form collecting ducts that eventually combine to form the secondary, then primary branches of the ureter. Unlike the mammal, the lobules, and there-
From Avian & Exotic Clinic of the Monterey Peninsula, Monterey, CA, and Ontario VeterinaryCollege, Universityof Guelph, Guelph, Ontario, Canada. Address correspondenceto MichaelJ. Mum'ray,DVM, Avian & Exotic Clinic of the Monterey Peninsula, 2 Harris Ct, Ste A-I, Monterey, CA 93940. Copyright9 1999 by W. B. Saunders Company. 1055-937X/99/0803-0005510. 00/0
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fore the lobes, are f o u n d at varying depths within the kidney. As a result, one c a n n o t visualize defined borders between the cortex and medulla. In essence, the greater areas of cortex s u r r o u n d relatively small, cone-shaped regions of medulla. T h e r e are two types of n e p h r o n within the avian kidney. T h e cortical type nephr o n is confined to the cortical r e g i o n of the kidney and lacks the loop of Hen~'le. This reptilian f o r m of n e p h r o n is uricotelic, secreting uric acid in the f o r m o f a precipitate. 4 As most uric acid is secreted and not filtered, levels within the b l o o d do not rise in the face of mild to m o d e r a t e dehydration or decreased g l o m e r u l a r filtration rate. 5 From an endoscopic perspective, however, the accumulation of uric acid within the tubules in the face of decreased urine flow secondary to dehydration creates a visible pale striation to the kidney. Unless long-standing or exceptionally severe, the r e t u r n to n o r m a l hydration status will result in spontaneous resolution of this condition. T h e m a m m a l i a n or medullary n e p h r o n produces urine and does have the intermediate segment, the loop of Henle. 6 T h e distribution of these two types of nephron, medullary (or m a m m a l i a n ) and cortical (or reptilian), is clinically relevant when considering endoscopic renal biopsy. Fortunately, the lobules containing b o t h cortical and medullary nephrons are e m b e d d e d in varying depths within the kidney. Therefore, the typical 3- or 5-French (Fr) biopsy specimen is likely to contain b o t h nephr o n types. 7 T h e ureter is f o r m e d by the confluence of a n u m b e r of p r i m a r y branches. It is initially visualized as it emerges f r o m u n d e r the lliac atery at the cranio-medial b o r d e r of the middle division of the kidney (Fig 1). T h e ureter continues caudally and slightly medially within a groove on the ventral surface of the middle and caudal divisions. T h e ureters then o p e n into the urod e u m on its dorsolateral aspect. Typically, the ureters enter the cloaca m o r e dorsally to the m o r e lateral position of the genital d u c t s . 7 T h e arterial supply to the kidney arises f r o m the cranial, middle, and caudal renal arteries. T h e cranial renal artery tends to be m o r e superficial; therefore, the cranial division may be less desirable as a biopsy site. A venous vascular ring, the renal portal system, surrounds the kidneys. This system allows shunting of b l o o d into the caudal vena cava, into the caudal mesenteric vein
Figure 1. Left cranial and middle divisions of a normal cockatoo kidney. The iliac artery and vein separate the two divisions. The ureter is visible as it emerges from the middle division. Note the normally melanistic testicle in this bird. and towards the liver, or into the internal vertebral venous plexus within the vertebral canal. 7 T h e presence of the renal portal system has theoretical clinical significance when assessing the administration of drugs with p r i m a r y renal metabolism into the pelvic limb. T h e practical consequences have yet to be totally elucidated.
Indications for Endoscopy of the Urinary System Although there are no truly p a t h o g n o m o n i c signs of renal disease, the clinician is e n c o u r a g e d to consider renal disease as a rule-out whenever a patient is presented with a change in urinary output. Polyuria, the most c o m m o n change noted, may be mistaken for diarrhea by the client. Unlike diarrheic droppings, tile polyuric d r o p p i n g contains a n o r m a l fecal mass surr o u n d e d by an increased a m o u n t of fluid (urine). For reasons that are not clearly understood, birds subjected to the stress of transportation and presentation to the veterinary facility will often pass polyuric droppings. Such changes may be the result of increased urine p r o d u c t i o n or
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decreased urine resorption. 8 To avoid misinterpreting the artifacturally altered data, clients should be instructed to present the most recent 24 hours of cage p a p e r for evaluation at the time of the examination. Stress associated with reproduction may result in polyuria. Similarly, elevated environmental t e m p e r a t u r e may result in poydipsia a n d secondary polyuria. Obviously, high water intake in the f o r m of high water content foods may affect the droppings, as well. Collection of a complete history by the clinician is essential. Systemic disease may also cause polyuria. Infectious agents, such as chlamydia, viral, and bacterial organisms, may cause increased urine production. 9 T h e exact etiopathogenesis of this clinical observation is not totally understood. T h e polyuric effect of hyperglycemia is well d o c u m e n t e d . M t h o u g h polyuria is the most c o m m o n alteration in urinary output, oliguria and anuria may occasionally be noted. T h e inability to identify the exact cause of any change in urinary output warrants endoscopic examination of the urinary tract. Mterations in urine color may suggest renal dysfunction; however, most changes are caused by dysfunction in o t h e r organ systems. Biliverdinuria is a result of liver disease or hemolysis. As the circulating levels of biliverdin elevate, the renal threshold is exceeded, and the excess is excreted in the urine. H e m o g l o b i n u r i a or h e m a t u r i a may also indicate renal disease. T h e classically described h e m o g l o b i n u r i a associated with heavy metal intoxication in Amazon parrots (Amazona sp) may not be n o t e d in o t h e r speciesJ ~ H e m a t u ria, on the o t h e r hand, may occur secondary to diseases of the kidney, ureter, or cloaca. Most cases of frank blood in the droppings are associated with cloacal disease. 9 T h e endoscope may be used not only to p e r f o r m the traditional coelomic examination, but also to thoroughly examine the cloaca, u T h e unilateral lameness/paresis associated with renal neoplasia in the budgerigar (Melopsittacus undulatus) is a familiar clinical presentation for the avian practitioner. Similar unilateral or bilateral pelvic limb dysfunction may be observed in cases of renal inflammation. T h e intimate association of the l u m b a r and sacral plexuses as they course through the renal p a r e n c h y m a may result in lower m o t o r n e u r o n signs in certain renal diseases.
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Clinicians too often base the presence or absence of renal disease on the plasma uric acid level (Fig 2). It is, however, too insensitive to rely on solely for the evaluation of renal function. Uric acid is synthesized by the liver and then excreted via tubular secretion by the medullary (reptilian) nephrons, i n d e p e n d e n t of glomerular filtration rate, state of hydration, and of tubular water resorption. 5 Therefore, hyperuricemia is not the result of dehydration, but only is manifested w h e n renal function is below 30% of its original capacity. 12 Birds c o n s u m i n g a high protein meal may exhibit a transient postprandial h y p e r u r i c e m i a J 3 Repeated, fasting samples normally will show uric acid levels within n o r m a l limits. Therefore, an isolated elevation of plasma uric acid does not in itself warrant endoscopic e x a m i n a t i o n . Persistent elevations, or those coupled with o t h e r evidence of renal disease, however, strongly indicate such a diagnostic step (see Table 1). Additionally, serial uric acid determinations showing a rise within the reference range may justify endoscopic examination. Urea is n o t c o m m o n l y evaluated in avian clinical medicine. Only small amounts are produced; therefore, its application is limited) 3 Unlike uric acid, urea is eliminated by glomerular filtration a n d is not resorbed in the n o r m a l bird. T h e r e is, however, a significant elevation in s e r u m urea concentration secondary to renal resorption in the dehydrated bird. 5 Despite this,
Figure 2. Urate accumulations in kidney tubules of an Amazon parrot. This bird had a reference-range plasma uric acid.
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Table 1. Indications for Renal Endoscopy Unexplained changes in urine output: Persistent elevations in uric acid: Difficultymaintaining hydration LethargT and/or weight loss
Especiallypolyuria Fast carnivorous birds, use serial sampling
the clinical significance of blood urea is probably limited in avian nephrology. The applicability of creatinine and creatine to avian renal disease is not well understood. Little creatinine is produced in the bird from its precursor, creatine. 9 The urinalysis is a frequently overlooked, but potentially valuable diagnostic tool in the management of avian renal disease. It is obvious that urine evaluation requires a polyuric patient and careful segregation of the urine from the associated fecal c o m p o n e n t o f the dropping. If the specimen contains flocculent material, it should be clarified by centrifugation before chemical evaluation. Standard dipsticks may be used; however, not all components of the mammalian p r o d u c t are applicable. 9 Urine p H may be influenced by cloacal contents, as well as diet. Proteinuria is typically expected, however, the quantity decreases with increased urine dilution in the normal bird. Glucose is generally present to a trace amount, however, its significance should not be overinterpreted without confirmatory blood glucose determinations. Ketones are not normally present in the urine, but may be n o t e d in individuals that are beta-oxidizing fats secondary to starvation or migration. 14 Evidence of blood or hemoglobin is not normal. One should ensure, however, that the positive test is not the result of myoglobin associated with recent animal muscle meals. Neither bilirubin n o r urobilinogen are expected to be in the urine of the bird. The lack of biliverdin reductase precludes the formation of bilirubin as the end product of hemecatabolism. 12 As a result, urobilinogen will not be formed, as it is p r o d u c e d by the bacterial alteration of conjugated bilirubin in the gastrointestinal tract. Examination of the urine sediment is important in the evaluation of renal disease. Unfortunately, sediment examination is complicated by the relatively large quantity of urate precipitate. Despite this difficulty, the presence of cellular or proteinaceous urinary casts, leukocytes, a n d / o r erythrocytes may indicate renal disease. The sedimentary c o m p o n e n t of the urine is generally
quite labile and is best evaluated immediately, rather than being submitted to a reference laboratory for examination. Changes in the radiographic appearance of the kidneys or perirenal structures may be an indication for endoscopic examination. Loss of the dorsal diverticulum of the abdominal air sac separating the dorsal aspect o f the kidney from the ventral synsacrum may suggest renal enlargement. 9 This change may be artifacturally produced by i m p r o p e r positioning of the lateral exposure. Gross changes in the size of the kidney may be noted, but should not be overinterpreted, as the cranial division may seem enlarged because of its intimate relationship with the gonad and adrenal gland. Increased density of the renal silhouette is often associated with small kidneys. Radiographic evidence of mineralization of the kidney is occasionally noted. The "self insuffiation" of the bird through its air sac system has tremendous advantages for the endoscopist, but limits the use of diagnostic ultrasound for evaluation of the avian urinary system. CT scans and magnetic resonance imaging are both potentially valuable diagnostic tools, but exceed the resources of most veterinary facilities. One of the most c o m m o n indications for renal biopsy is the visual identification of changes in size, shape, color, or consistency of the kidney during routine endoscopic examination for sex identification (Fig 3). Any deviations from the expected normal for the age/species should warrant further work-up. In most cases, the actual biopsy p r o c e d u r e is p r e c e d e d by establishm e n t of m i n i m u m database parameters, as they are generally not obtained during routine "surgical sexing." Other, nonspecific signs of renal disease include lethargy, anorexia, dehydration, regurgitation, generalized weakness, and weight loss. Any of these signs that may be clinically related to the urinary system may warrant endoscopic examination. The clinician is encouraged to aggressively pursue a definitive diagnosis early in the progression of renal disease. Discussion of the potential for endoscopic examination and potential biopsy early in the diagnostic work-up may enhance client acceptance of the procedure, should it become indicated. It is readily apparent that the minimally invasive nature of the fine diam-
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Figure 3. Chronic renal damage may lead to changes in the normal appearance of the parenchyma. This parrot has a very irregular kidney surface caused by chronic, ongoing renal disease. eter rigid e n d o s c o p e coupled with the relative safety of isoflurane anesthesia has resulted in m o r e routine recognition of the i m p o r t a n c e of this technology in the diagnosis and t r e a t m e n t of avian renal disease.
Technique T h e kidneys may be a p p r o a c h e d for either visual examination or biopsy t h r o u g h the traditionally described caudal thoracic air a p p r o a c h and subsequent advance into the abdominal air sac. In this approach, the bird is anesthetized a n d placed in lateral recumbency. T h e wings are e x t e n d e d dorsally and fixed in that position. T h e dorsally positioned leg is e x t e n d e d cranially to expose the area caudal to the last rib. A small skin incision is t h e n m a d e over the area the semitendinosus muscle (m. flexor cruris medialis) crosses the last rib. ~5T h e entry point into the caudal thoracic air sac is then m a d e by bluntly dissecting t h r o u g h the thin body wall musculature just ventral to the flexor cruris medialis. In most species, directing the tip of the telescope slightly cranially a n d medially will p e r m i t entry into the caudal thoracic air sac (CTAS). Entry into the abdominal air sac (AAS), in which the kidney and associated structures may be visualized, is t h e n m a d e by passing the telescope
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t h r o u g h the confluent CTAS/AAS m e m b r a n e located medially f r o m the entry point. An entry p o i n t directly into the AAS may allow better access a n d visualization of the caudal division of the kidney. T h e entry for this postpubic a p p r o a c h is located dorsal to the pubic b o n e and caudal to the ischium. After entry into the most caudal aspect of the intestinal peritoneal cavity, the telescope can advance t h r o u g h the air sac wall into the AAS. At this point, the tip of the telescope is located at the caudal-most aspect of the caudal division of the kidney, looking cranially. 15 Once located within the abdominal air sac, the endoscopist should p e r f o r m a complete examination of the urinary system, as well as all o t h e r coetomic structures available for visualization. T h e entire kidney f r o m its most cranial aspect to its caudal pole should be inspected, initially from some distance and then with greater magnification by moving closer to the tissue. As the tip o f the telescope a p p r o a c h e s the kidney, the clinician will notice an increase in magnification without any loss of detail and resolution. T h e unique optical qualities of m o d e r n small diameter r o d lens telescopes m a k e this clinically useful application possible. W h e n the CTAS a p p r o a c h has b e e n used, the caudal division may be m o r e difficult to examine. Use of the 30 degree offset of the lens tip will enhance the endoscopist's ability to complete the examination. T h e u r e t e r should be followed f r o m its origin to its entry point into the u r o d e u m on the dorsolateral aspect of the cloaca. Although most cases of renal disease are diffuse, occasionally focal disease is encountered. W h e n suspected, a second laparoscopic a p p r o a c h may be indicated with entry on the contralateral side. We advocate the use of aseptic technique for the entire endoscopic procedure. A one- to two-layered closure after removal of the instrumentation is r e c o m m e n d e d using a fine absorbable monofilim e n t suture. T h e d e v e l o p m e n t of a sheath system with an integral i n s t r u m e n t channel allows the delivery of biopsy forceps of a variety of sizes directly to the area visualized by the lens system. 15 Elliptical or r o u n d c u p - s h a p e d biopsy forceps of 3- or 5-Fr size are typically used to collect biopsy specimens f r o m small- to medium-sized birds (Fig 4). These instruments facilitate control of specimen size and d e p t h of penetration, with the 3-Fr r o u n d
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Figure 4. Renal biopsy site in an Amazon parrot 2 minutes'after collection of a 7-Fr kidney biopsy. This is the maximal biopsy recommended for a bird of this size. A 5-Fr cup would be better suited to this bird's kidney mass. cup having the most shallow depth. T h e apparently minute size of the forcep cup nmst be correlated to the size of the renal tissue. It is also i m p o r t a n t that the cutting edges of the biopsy instruments be kept clean and sharp. Excessive force used to excise the tissue may create substantial crushing artifact. Dull instruments may result in an iatrogenic avulsion of the kidney f r o m its sulcus, as the forceps tear rather than cut tissue. Biopsy site selection is d e p e n d e n t on the nature of the disease encountered. In those cases of obviously diffuse disease, ease of access, distance f r o m vasculature, and distance f r o m ureter and genital tract are d e t e r m i n i n g factors in selection of the site. In the case of m o r e focal disease, the biopsy must be targeted, using discretion in the d e p t h of sampling and proximity to vessels and tubular organs. Regardless of the site selected, the o p e r a t o r must be very cautious to avoid vital structures and large vessels. Despite prior publications to the contrary, 12 most hemorrhages are m i n o r and self-limiting. In those cases warranting further hemostasis, direct pressure using the closed biopsy forceps is typically adequate. W h e n possible, the collection of a minim u m of two samples is encouraged. As previously reported, n u m e r o u s renal biop-
sies using the techniques described have b e e n p e r f o r m e d without incident. 16T h e typical instrum e n t a t i o n employed is a 2.7-mm, 30-degree f o r w a r d / o b l i q u e rigid telescope, 14.5-Fr sheath with a 5-Fr i n s t r u m e n t channel. 15,16 In most cases, the biopsy forceps of choice has b e e n a 5-Fr elliptical cup forceps. This p r o c e d u r e has b e e n p e r f o r m e d by us on birds as small as 27 g safely without significant postbiopsy h e m o r rhage. Historically, the concept of renal biopsy has b e e n addressed with a great deal of trepidation. Recent advances in diagnostic endoscopy have facilitated the use of this technology for the diagnosis of a variety of clinical diseases that has thus far b e e n possible only on necropsy. T h e use of the macroscopic laparotomy to p e r f o r m a renal biopsy, although possible, does not enhance one's ability to visualize a n d select specim e n collection sites. T h e degree of tissue trauma is also m u c h greater. A recently described dorsal pelvic a p p r o a c h to renal biopsy 17 does not permit specific targeting of renal parenchyma, does not allow a complete and t h o r o u g h examination of the urinary system, and as an osteotomy is required, must involve a significantly m o r e painful recovery. T h e use of the endoscope is a relatively simple technique, easily mastered with practice, which will enhance the diagnostic capabilities of any avian practitioner. Its potential in the minimally invasive diagnosis of renal disease remains u n t a p p e d .
References 1. Siller WG: Renal pathology in the fowl A review. Avian Pathol 10:187-262, 1982 2. Taylor M: Diagnostic application of a new endoscopic system for birds. Proc Eur Conf Avian Med Surg 127-131, 1993 3. Orosz S: Anatomy of the urogenital system, in Altman RB, Clubb SL, Dorrestein GM, Quesenberry K (eds): Avian Medicine and Surgery. Philadelphia, PA, Saunders, 1997, pp 614-622 4. Skadhauge E: Osmoregulation in Birds. Heidelberg, Germany, Springer-Verlag, 1981, pp 84-91 5. Lumeij JT: Plasma urea, creatinine and uric acid concentrations in response to dehydration in racing pigeons (Columbia livia domestica). Avian Pathol 17:851-864, 1987 6. Sturkie PD: Kidneys, extrarenal salt excretion, and urine, in Sturkie PD (ed): Avian Physiology (ed 4). New York, NY, SpringeI:Verlag, 1986, pp 359-382 7. King AS, McLelland J: Birds Their Structure and Function. London, UK, Baillere-Tindall, 1984, pp 175-186 8. Palmore WP, Fregly MJ, Simpson CE: Catecholamine-
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induced diuresis in turkeys. Proc Soc Exp Biol Med 167:1-7, 1981 Styles DK, Phalen DN: Clinical avian urology. Semin Avian Exotic Pet Med 7:104-113, 1998 Woerpel RW, Rosskopf WJ: Heavy metal intoxication in caged birds: Parts I, II. Comp Cont Ed Pract Vet 4:191196, 1982 Speer BL: Diseases of the urogenital system, in Altman RB, Clubb SL, Dorrestein GM, Quesenberry K (eds): Avian Medicine and Surgery. Philadelphia, PA, Saunders, 1997, pp 625-633 Lumeij JT: Nephrology, in Ritchie BW, Harrison GJ, Harrison LR (eds): Avian Medicine: Principles and Application. Lake Worth, FL, Wingers, 1994, pp 538-555 Lumeij JT, Remple JD: Plasma urea, creatinine and uric
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acid concentrations in relation to feeding in peregrine falcons (Falcoperegrinus).Avian Pathol 20:79-83, 1991 Phalen DN, Ambrus S, Graham DL: The avian urinary system: Form, function, and diseases. Proc Assoc Avian Vet 44-57, 1990 Taylor M: Endoscopic examination and biopsy techniques, in Ritchie BW, Harrison GJ, Harrison LR (eds): Avian Medicine: Principles and Application. Lake Worth, FL, Wingers, 1994, pp 32%354 Murray MJ, Taylor M: The use of endoscopy and endoscopic biopsy as aids in the diagnosis of renal disease. Proc Assoc Avian Vet 133-138, 1997 Suedmeyer WK, Bermudez A: A new approach to renal biopsy in birds.J Avian Med Surg 10:179-186, 1996