Abstract

When discussing the urinary system and its unique aspects in birds, the important consideration is how do birds osmoregulate? All animals need to have adequate water in their extracellular fluid compartment to regulate cellular functions. In order to achieve water and ion homeostasis, animals range from osmoconformers to osmoregulators of their internal environment. Birds are osmoregulators.

Birds fall between mammals and other non-mammalian vertebrates for the organs of osmoregulation. Many avian species have salt glands that perform important osmoregulatory function, particularly in a marine environment. Like reptiles, birds utilize the lower portion of the GI tract as an important component for osmoregulation. This first part of the lecture for this discussion today will focus on the gross anatomy of the kidneys, including an overview of the blood supply in the area along with nerves. Based on this anatomy, it will include radiology and CT images of the kidneys.

The Kidney

External Anatomy

The renal system consists of the kidneys, ureters, and the urodeal portion of the cloaca. The kidneys of birds are fixed in ventral depressions of the synsacrum called the renal fossae, and they are symmetrical and retroperitoneal. They extend from the proximal end of the synsacrum just distal to the caudal extent of the lungs to the cranial end of the synsacrum. There can be diverticula of the abdominal air sacs that extend between the kidneys and the pelvis.

Unlike mammalian kidneys, the kidneys of birds are not divided into lobes grossly, but into divisions. Birds tend to have three divisions: cranial, middle, and caudal. The external iliac artery cranially and the ischiatic artery caudally run through the kidney so that it forms the three divisions. The portion of the kidney cranial to the external iliac artery is the cranial division; the portion between the two arteries is the middle; and that portion caudal to the ischiatic artery is the caudal division. In chickens and many of the parrot species, these divisions are distinct. The middle division in passerines is not distinct, as this portion blends with the cranial and more often the caudal division. In puffins, penguins, and herons, the caudal divisions are fused in the midline.

The spinal nerves from the lumbar and sacral plexuses move through the substance of the kidney to innervate their respective muscles to the lower body wall and the leg or are sensory to that area of the body. This is important clinically, as swelling of the kidneys causes reduction in nerve function, and the patient may present with inability to use the leg. This more often occurs in budgerigars, and they are presented to the veterinarian for a possible leg fracture.

In the domestic fowl, each division has on its surface slightly rounded projections that represent the renal lobules as they reach the surface. In general, the basic unit of the avian kidney is the lobule. They tend to be pear-shaped and wedged between the interlobular veins of the renal portal system. The wide, superficial portion represents the cortical region of the lobule and contains nephrons of both the cortical- and medullary-type nephrons.

The artery that supplies each lobule is found in its center with radiating branches. The drainage of the lobule consists of a vein that is intralobular like the artery. The collecting ducts of birds are found on the periphery of each lobule, which has been likened to the outer staves of a barrel. This is the opposite of mammals where the collecting ducts are intralobular and the arteries are interlobular.

The Arterial Supply to the Kidneys

The cranial, middle, and caudal divisions of the kidney are supplied by their respective arteries that arise from the abdominal aorta. The caudal division has a branch off the aorta that bifurcates on the surface of the kidney, resulting in two arteries that enter the parenchyma of this larger division.¹ These arteries then branch within the substance of the kidneys to eventually form the intralobular arteries. The intralobular arteries are found in the lobule approximately halfway between the inter- and intralobular veins.

The intralobular arteries form the short afferent glomerular arteries that immediately form the glomerulus. Each of these capillary tufts is simpler and much smaller than mammalian ones, as they consist of only 2–3 capillaries that have limited interconnections compared with mammalian capillary tufts. The capillary tufts of the loopless nephrons can consist of only one capillary loop that such an afferent arteriole forms a single capillary loop and then widens to form an efferent arteriole.

The arterial supply continues as efferent glomerular arterioles. These arterioles divide to form the second capillary plexus, the peritubular capillary plexus, which surrounds the epithelium of the convoluted tubules in the cortical region. In the medullary region, these arterioles from the efferent glomerular arterioles form arteriolar recta that lie alongside the loops of Henle before forming the venulae recta that drains the area.

The Venous Supply to the Kidneys

Blood from the area around the loops of Henle are drained by the venulae recta into the intralobular veins. The intralobular veins drain blood into the efferent renal veins or branches. Depending on the division of the kidney, the blood then flows into renal veins of its appropriate division. In the cranial division of the kidney, there can be several cranial renal vessels that then drain into the common iliac vein after the renal portal valve or into the abdominal vena cava directly. The caudal renal vein drains the middle and caudal divisions of the kidneys. Blood from the intralobular veins drains into the efferent renal veins or branches before draining into the caudal renal vein. The caudal renal vein, like the cranial renal vein, empties into the common iliac vein after the renal portal valve.

The renal portal system is involved in the secretion of urates in the blood so that it can be excreted by the kidneys in birds. The renal portal system supplies venous blood to the peritubular capillary plexuses that surround the proximal convoluted tubules at the periphery of the lobule. These tubules are responsible for the secretion of the urates into its lumen from these blood vessels. Urates are also filtered by the glomerulus, but its rate is insufficient. It has been suggested that the renal portal system provides about two-thirds of the blood supply to the kidneys that bypasses the glomeruli. This has important ramifications for the removal of urates along with other components, including drugs.

The renal portal system forms a venous ring with both kidneys. It consists of the right and left cranial and caudal renal portal veins. At the cranial end, the right and left cranial renal portal veins are connected via the internal vertebral venous sinus, which drains the vertebral column. The caudal end of the ring is completed by its anastomoses with the caudal mesenteric vein. There are numerous small venous branches that take origin from this ring to penetrate the parenchyma of the kidney. Each afferent renal branch has a muscular sphincter at its base to control the volume of blood that enters the substance of the kidney. These afferent renal venous branches are connected with the interlobular veins, which are connected to the peritubular capillary plexus at the periphery of each lobule.

In addition to the valves in the afferent renal venous branches, there are renal portal valves that control blood flow as well. These valves are found within the lumen of the common iliac veins between the renal and the portal veins. Blood can enter the portal venous ring from the external iliac veins, the internal iliac veins, the caudal mesenteric vein, and the ischiatic veins. Each valve is innervated by adrenergic and acetylcholine receptors. If the valves are open, then blood will flow directly into the caudal vena cava and not the substance of the kidney. Valve closure is inhibited by norepinephrine and epinephrine so that with “flight” there is available venous return to the heart. When the valve is closed, blood flows into the parenchyma of the kidney. Acetylcholine stimulates its closure.

From a clinical perspective, understanding these connections with the renal portal system helps explain the spread of neoplasia and infectious agents to other parts of the body. Blood from the renal portal system can flow through the portal valve into the vena cava, into the caudal mesenteric vein to the liver, and/or into the internal vertebral venous plexus within the vertebral canal. This shunt can result in the bypass of the kidney completely but often is only partially activated so that blood may go a variety of directions.

Diagnostics

Characterizing renal disease can be challenging and is often best performed by using a combination of diagnostic methods. Some diagnostics rely in blood and urine chemistry values such as uric acid and urinary gamma-glutamyl transferase (GGT), respectively. A thorough understanding of avian renal anatomy is needed when considering radiology, ultrasound, endoscopy, and advanced imaging (especially computed tomography [CT]).

A lateral view is the best method to radiographically view the kidneys. As viewed with a lateral radiograph, the absence of the normal dorsal diverticulum of the abdominal air sac (dorsal to the kidney and ventral to the synsacrum) may indicate renal enlargement. Also, most normal-sized kidneys do not extend ventral to an imaginary horizontal line (which is parallel to the spine) that passes through the ventral border of the acetabulum. Improper positioning can artifactually change the appearance of this air-filled diverticulum. Because the renal silhouettes are superimposed on a lateral view of the abdomen, an oblique view may also be used to distinguish each kidney. Renal density and gross size changes may indicate renal disease.

A barium series on the ventrodorsal view may also be helpful in identifying severe renal swelling. In normal birds, the angle between the proventriculus and the ventriculus relative to the spine should be about 45 degrees. With massive renal enlargement and lateral displacement of the proventriculus, and sometimes ventriculus, this angle increases.

Due to the presence of surrounding air sacs (ventrally) and bone (dorsally and laterally), ultrasonographic imaging of normal avian kidneys is difficult. In one study of 386 mixed bird species that underwent ultrasonographic evaluation of the urogenital tract, abnormalities such as renal cysts (6), cancer (12), and inflammatory nephromegaly (11) were identified in only 29 patients. The authors concluded that sonographic imaging of the normal kidney was not possible. Some disease conditions that either obliterate the air sacs or result in fluid accumulation in the coelomic cavity may actually improve renal ultrasonographic imaging. Renal tumors can be heterogenous compared to homogeneous with normal tissue, and they have no discernible border with the synsacrum dorsally as viewed with ultrasound. In these abnormal situations, ultrasonography can serve as a noninvasive and safe means to evaluate coelomic structures such as the kidneys. Also, contrary to statements above, some skilled ultrasonographers can position birds such that the kidneys are visible via ultrasound even if there is no pathology present.

Intravenous excretory urography has been described in birds as a method to gain information on kidney size, shape, and function. Lumeij reports using organic iodine compounds given IV at 2 mg/kg in the basilic vein. The organic iodine can be visualized radiographically in the heart and pulmonary artery within 10 seconds and outlining the kidneys and ureters 20 to 50 seconds later. After 2 to 5 minutes, the cloaca will be outlined. This technique should not be used in birds with severe renal compromise.

Intravenous excretory urography may have some limited uses in a clinical setting as demonstrated in the case report below. Dennis and Bennett successfully used a water-soluble, iodinated contrast agent (Renografin-76, Squibb Diagnostics, Princeton, NJ, USA) to evaluate the ureters post-ureterotomy in a double yellow-headed amazon parrot (Amazona ochrocephala). The agent was dosed at 400 mg/kg and was given in the right medial metatarsal vein. Radiographic images were taken at 1, 2, 7, and 10 minutes post-injection. Ureter peristaltic movement and size were successfully evaluated using this technique.

However, excretory urography combined with CT can provide significant information about the avian kidney. CT (computed tomography) is essentially a series of x-rays compiled to form 3D images. High-quality CT scans (generally 200-µm slice thickness or less) can provide unparalleled 3D information about kidneys in health and disease. MSE uses the following protocol for contrast CT studies in birds:

• First: Whole-body or region of interest (ROI) plain CT scan.
• Second: 4–6 ml/kg of Isovue 370 IV delivered over 2 minutes. Thirty seconds into the contrast perfusion, start the second whole-body or ROI CT scan.
• Third: Complete a last whole-body or ROI scan immediately after completing the contrast perfusion.

This form of CT angiography can demonstrate not only anatomic features of the kidney, but it also gives information about renal contrast clearance. Tumors, cysts, vasculature, and more can be highlighted by the contrast study giving anatomic information. In a normal (third) post-contrast CT scan, the ureters and cloaca fill with contrast. Lack of contrast filling in the ureters gives information about renal clearance and patency of the ureters.

When history, physical examination, and/or laboratory abnormalities support the presence of renal disease, consider biopsy. Currently, the only means to definitively diagnose avian renal disease and specific pathologic patterns is with a kidney biopsy and histopathologic evaluation. A renal biopsy is most frequently performed during endoscopic examination of the coelomic cavity and specifically, kidneys. Alternatively, the kidneys can be approached dorsally by cutting through the synsacrum. This dorsal approach obviously requires cutting through bone and increases the risk of damaging the more dorsally located lumbar and sacral nerve plexuses. Before a renal biopsy is performed, the cost–benefit analysis of the surgical procedure versus conservative therapy must be considered, as many birds have compromised health, especially if they have kidney disease.

In a study of 89 free-living birds of prey, 126 endoscopic coelomic-approach renal biopsy samples (two biopsies from 37 birds) using 1.8-mm biopsy forceps were taken. Post-biopsy hemorrhage averaged 67 seconds (10–172 seconds). The average biopsy was 2.2 mm long, 1.3 mm wide, and 1.0 mm deep. All samples contained proximal and distal tubuli and one to 89 glomeruli, with most having 25–29 glomeruli per histologic slide. One hundred thirteen of 126 samples could be evaluated well or very well. Sixty-six samples revealed lesions including subcapsular bleeding (19/66), inflammation (16/66), cell casts (12/66), periodic acid–Schiff-positive reactions (8/66), and protein casts (6/66). Correlation between endoscopically visible change and histologic disease was 76.1% (96/126). The cranial division was considered the best site to collect biopsy samples due to its size and visibility. The authors, Müller et al., noted it was possible to obtain specimens from the middle and caudal renal divisions in larger birds.

Renal histologic lesions are rarely pathognomonic for a specific disease process. Many different diseases cause similar renal lesions. Additionally, different pathologists may make differing morphologic diagnoses on the same renal tissue. The author (MSE) encourages veterinarians to work with a pathologist familiar with normal and abnormal avian histology. Oftentimes, it is the pathologist’s interpretation of a renal biopsy combined with the attending veterinarian’s case familiarity that enables both parties to make a definitive diagnosis or build a reasonable differential diagnoses list compatible with the kidney lesions noted.

References

References are available upon request.