Double Ureters With Ureteral Ectopia in a Domestic Shorthair Cat

A 5-month-old domestic shorthair cat was presented for evaluation of urinary incontinence since birth. Excretory urography revealed dilated double ectopic ureters draining a hydronephrotic right kidney. Urine culture yielded a pure culture of Klebsiella pneumoniae. The cat was treated initially with bactericidal antibiotics, followed by right-sided nephroureterectomy. The surgery and antibiotic therapy led to complete resolution of urinary incontinence and urinary tract infection. Ureteral duplication is an unusual congenital anomaly that has not been previously reported in the cat. J Am Anim Hosp Assoc 2006;42:462-466.

Seth N. Ghantous, DVM, Diplomate ACVIM
Jason Crawford, DVM, Diplomate ACVR
From the Department of Medical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, Wisconsin 53706.
Doctor Ghantous’ current address is Animal Emergency and Referral Center, 1810 Skokie Boulevard, Northbrook, Illinois 60062.

Introduction
Urinary incontinence in a young animal may be caused by congenital defects, including ureteral ectopia, vaginal stricture, patent urachus, congenital incompetence of the urethral sphincter mechanism, and neurogenic disorders.1 Ectopic ureters are most commonly seen in young, female dogs and appear to be much less common in cats.2 Renal and ureteral duplication have been reported extensively in humans, have rarely been described in the dog, and have never been documented in the cat.3,4 Double ureters drain separate renal collection systems from the same kidney and open separately into the urinary or genital tract.5,6 Given the embryological migration pattern of ureters, their termination sites are often ectopic.5 The purpose of this paper is to describe the first case of a cat with double ureters.

Case Report
A 5-month-old, castrated male domestic shorthair cat was referred to the Veterinary Medical Teaching Hospital of the University of Wisconsin, Madison, School of Veterinary Medicine, for evaluation of urinary incontinence. The owners had noticed a swelling at the end of the cat’s penis at 2 weeks of age, which had partially resolved with application of neomycin 0.25%/triamcinolone 0.1%/nystatin 100,000 U/mL.a The kitten was first presented to the referring veterinarian at 2 months of age because of polydipsia and continuous dribbling of urine from the prepuce. Physical examination revealed a chronic, small injury to the tip of the penis as well as urine scalding of the perineal area. A urinalysis and positive-contrast cystography were normal. A 10-day course of amoxicillinb was prescribed, and the cat was discharged. Six weeks later, the cat was presented for continued incontinence. The owner reported that the urinary incontinence improved while the cat was receiving amoxicillin, but increased in severity when the course of antibiotic ended. On repeat examination, the referring veterinarian noted that the injured area of the penis was now black, and the cat was scheduled for castration. At the time of castration, the penis could not be fully exteriorized from the prepuce. Since the penis was partially necrotic and could not be fully exteriorized, a castration and perineal urethrostomy were performed. The cat continued to exhibit urinary incontinence following the surgery and was referred for further evaluation.

Physical examination revealed a bright young cat with evidence of urine staining of the perineum. The kidneys were enlarged, and the cat resisted abdominal palpation. The remainder of the physical and neurological examination was unremarkable. A complete blood count (CBC) and serum biochemical profile were performed. Hematological abnormalities included a mild thrombocytosis of 606,000 cells/μL (reference range 175,000 to 600,000 cells/μL) and a leukocytosis with a mild left shift. The white blood cell (WBC) count was 27,990 cells/μL (reference range 5000 to 19,500 cells/μL), with numerous band neutrophils (560 cells/μL, reference range 0 to 300 cells/μL), a lymphocytosis (16,230 cells/μL, reference range 1500 to 7000 cells/μL), and an eosinophilia (1960 cells/μL, reference range 0 to 750/μL). Biochemical abnormalities included hypercalcemia (11.4 mg/dL, reference range 9.0 to 11.0 mg/dL), hyperphosphatemia (9.4 mg/dL, reference range 2.6 to 6.8 mg/dL), and elevated alkaline phosphatase (141 U/L, reference range 11 to 70 U/L). Urine was collected by cystocentesis for urinalysis and bacterial culture. There were 20 to 30 WBC per high-power field (HPF) and many bacilli in the urine sediment. The urine culture yielded >100,000 colony-forming units/mL of Klebsiella pneumoniae sensitive to amoxicillin- clavulanic acid. Feline leukemia virus antigen and feline immunodeficiency virus antibody tests were negative.

Given the cat’s history of dribbling urine since birth and partial resolution of the dribbling with antibiotic therapy, the most likely differential diagnoses included ureteral ectopia, congenital incompetence of the urethral sphincter mechanism, chronic or recurrent urinary tract infection (and potential associated congenital anomalies), and neurogenic disorders of micturition (e.g., lesions of the sacral spinal cord, suprasacral spinal cord, peripheral nerves, brain stem, and cerebellum). Since the cat was normal neurologically, resented abdominal palpation, and had an enlarged right kidney, excretory urography and a cystourethrogram were performed.7-9 The nephrogram phase of the left kidney proceeded normally, with initial opacification followed by a gradually decreasing opacification. The nephrogram phase of the right kidney was abnormal, with poor initial opacification of a thin rim of renal cortex that surrounded a 3 × 2- cm radiolucent area centrally. The left kidney was slightly larger than the right. The pyelogram phase of the left kidney appeared 2 minutes following intravenous (IV) injection of contrast materialc and showed moderate dilatation of the pelvic diverticula and a normal ureter that terminated at the trigone of the bladder. Peristaltic activity of the left ureter was confirmed with fluoroscopy, but no contrast material was seen within the right renal pelvis or ureter.

A double-contrast cystogram was performed, and the bladder was normal. The positive-contrast urethrogram showed two distinct areas of dilatation, each 2 to 3 mm in size, along the dorsal wall of the pelvic urethra [Figure 1]. During the urethrogram and approximately 110 minutes after IV administration of contrast material, filling of the right renal pelvis occurred and revealed severe dilatation. Two dilated ureters, each measuring approximately 6 mm in diameter, extended from the right renal pelvis to the pelvic urethra, terminating at the two previously described focal urethral dilatations [Figure 2]. Given the poor opacification of the right nephrogram and initial lack of a right pyelogram, the late visualization of the right renal pelvis and double ureters was believed to result from the retrograde flow of the contrast agent given during the urethrogram. Final radiographic interpretation was severe hydronephrosis and dysfunction of the right kidney, with dilated, duplicate ectopic ureters. Bilateral pyelonephritis (more severe on the right) was also suspected.

Although the cat was not azotemic, the positive urine culture, the hydronephrotic right kidney, the left renal pelvic dilatation, the ureteral ectopia, and prior perineal urethrostomy all increased the cat’s risk for bilateral pyelonephritis.10-12 Alternatively, the dilatation in the left renal pelvis may have developed secondary to increased urine volume from a compensatory response, given the reduced function of the hydronephrotic right kidney. The cat was started on amoxicillin-clavulanic acidd (20 mg/kg orally q 12 hours). The cat’s owners were offered a radioisotope glomerular filtration study, followed by either neoureterocystostomy or nephroureterectomy, with the final decision regarding the surgical technique to be based upon the results of the glomerular filtration rate. Because of financial constraints, further diagnostic tests were declined, and surgery was performed to remove the hydronephrotic right kidney and duplicate ureters. The cat’s owners elected to postpone the surgery for 1 month, and the cat was discharged on amoxicillin-clavulanic acid.

The incontinence improved during the administration of amoxicillin-clavulanic acid. Selected chemistry tests performed prior to surgery showed mild azotemia with an elevated blood urea nitrogen (35 mg/dL, reference range 14 to 34 mg/dL) and normal creatinine (1.1 mg/dL, reference range 0.8 to 2.3 mg/dL). The urine had a specific gravity of 1.053, so the azotemia was considered prerenal. The urinalysis also revealed 5 to 10 red blood cells per HPF, but only a few WBC and no evidence of bacteria. The urine culture was negative. Surgery confirmed that the right kidney had double extramural ectopic ureters separately entering the pelvic urethra. Other than being enlarged, the left kidney did not have any gross abnormalities. Prior to removing the right kidney, the double ureters were catheterized simultaneously from surgical urethrotomy sites. They both yielded urine and appeared to have separate lumens [Figure 3]. The right kidney was dissected from its sublumbar attachments and removed. The ureters were dissected from the surrounding tissues to the level of their separate insertion points on the dorsal aspect of the pelvic urethra and then removed. The kidney and the ureters were submitted for histopathology. The cat recovered uneventfully from surgery.

Gross inspection of the excised kidney revealed a markedly dilated renal pelvis with only thin remnants of renal parenchyma. Histopathology of the right kidney confirmed hydronephrosis with chronic, fibrosing, lymphoplasmacytic pyelonephritis. Also present was an anomalous double ureter. Both ureters were dilated and lined by a thin layer of transitional epithelium. Each ureter was subtended or opposed by a submucosa composed of smooth muscle bundles and connective tissue. Separating each lumen was a shared wall composed of transitional epithelium, submucosa, muscularis, submucosa, and transitional epithelium [Figure 4].

Antibiotics were continued for 2 weeks after the surgery. The owners declined to return for follow-up urinalysis and culture. A telephone conversation with the owners 2 months after surgery revealed the incontinence had resolved, and the cat’s water consumption had decreased. Repeat urinalysis and culture performed by the referring veterinarian con- firmed resolution of the bacterial cystitis.

Discussion
Ureteral ectopia is a common cause of congenital urinary incontinence in dogs (especially females), but it is relatively uncommon in the cat.2 A review of 19 cases of congenital urinary incontinence in cats found 10 to be associated with ureteral ectopia over a 10-year period (from 1981 through 1990).13 Hydronephrosis is a common complication of ureteral ectopia, occurring in approximately 43% of 23 reported cases.13 Pyelonephritis and cystitis also occurred in 13% and 9% of these 23 reported cases, respectively.13 Phimosis has also been associated with ectopic ureters and may explain why the cat’s penis could not be fully exteriorized from the prepuce.2,13 Phimosis is usually treated by performing a surgical enlargement of the preputial orifice; however, a urethrostomy was performed in this cat because a portion of the penis was necrotic.

No known reported case of double ureters in a cat, with or without ureteral ectopia, exists in the veterinary literature.4 In humans, double ureters and associated duplex kidneys are common developmental and often inherited abnormalities.5,14 Duplex kidneys occur in approximately 12% of the human population and may occur unilaterally or bilaterally.5 Renal and ureteral duplication has been reported in the dog, but it is extremely rare.3

A duplex kidney is a kidney in which two pyelocalyceal systems are present.5,6 Humans with this condition are described as having an upper and a lower pole to the kidney that are drained either by a bifid system, bifid ureters, or double ureters.5,6 Double ureters are complete duplications, and each ureter drains a separate pyelocalyceal system and opens separately into the urinary or genital tract.5,6 In a bifid system, the ureters join at the level of the ureteropelvic junction. Bifid ureters join together more distally but still proximal to the level of the bladder.5,6 This terminology may not be completely applicable to cats, because they and other carnivores have unipyramidal or unilobular kidneys, whereas humans have multipyramidal or multilobular kidneys.16 The medullary portion of a lobular kidney is roughly pyramidal in shape and is capped on its base by the cortex.16 Its apex is directed toward the renal sinus, forming a papilla that empties into the renal pelvis.16 Multilobular kidneys have papillae projecting from each pyramid that empty into minor and then major calyces, which are continuous with the ureter.16 Conversely, unipyramidal kidneys have a single broad-based papilla, which forms a structure called the renal crest.16 There are no calyces in unipyramidal systems, and urine from the papilla drains directly into the space between the renal crest and the renal pelvis.16 Therefore, cats may be best described as having separate collection systems rather than two pyelocalyceal systems.

The ureteral bud (i.e., metanephric diverticulum) is an evagination of the caudal end of the Wolffian duct (i.e., mesonephric duct).2,17 The ureteral bud grows craniodorsally via its dichotomously dividing ampullary end, joins the renal blastema, and ultimately forms the collecting tubules, pelvis, and ureter at its terminal branches.2,5,17 It is important to note that the development of the metanephric kidney does not proceed in the absence of the ureteric bud, and the ureteric bud does not divide in the absence of metanephric mesenchyme.6,17 Separate collection systems were not observed in the cat reported here because of the extensive parenchymal destruction. In a reported case of separate collection systems in an English bulldog, the two systems were demonstrated radiographically.3

If a single ureteral bud divides prior to the usual time that the ampulla divides, a duplex kidney with a bifid system or bifid ureter forms.5,6 On the other hand, if two ureteral buds form from the mesonephric duct, a duplex kidney with complete ureteral duplication occurs.3,5,6 The proximal end of the ureteric bud (i.e., closest to the mesonephric duct) develops into the ureter.5,6,17 Its position of origin from the mesonephric duct becomes the ureteral orifice at the trigone of the bladder. That portion of the mesonephric duct that is distal to the origin of the ureteric bud is known as the common excretory duct and is incorporated into the bladder as part of the trigone.6,17 As the common excretory duct is incorporated into the bladder, critical migration of the ureteral orifice occurs in a cranial and lateral direction, assuring its proper position in the trigone.6 Ureteral ectopia may occur if the source of the ureteric bud occurs at a more proximal or distal position of the mesonephric duct than its normal point of origin.6 If the ureteric bud occurs more distally than normal, it is incorporated into the bladder earlier than usual, allowing for a longer period of migration. This results in a ureteral orifice that is more cranial than a normal entrance at the trigone.6 Alternatively, if the origin of the ureteric bud occurs at a position on the mesonephric duct that is more proximal than normal, there is less time for proper migration into the bladder, and caudal ectopia occurs, characterized by a ureteral orifice positioned more caudally (i.e., urethra, vagina) than normal.6

Ureteral ectopia affects female dogs 20 times more frequently than male dogs.2 In cats, ureteral ectopia is also reported to occur more often in females.2,13 Some authors speculate that the increased frequency of this disease in female dogs may be due to their increased manifestation of urinary incontinence, which may occur because the potential termination sites for ectopic ureters in female dogs (e.g., vagina, vestibule) are not under sphincteric control.2 In male dogs, the potential termination sites (e.g., bladder neck, prostatic urethra) occur proximal to the external urethral sphincter, and ectopic ureters are most commonly discovered in male dogs when they occur in the cranial portion of the pelvic urethra, beyond the external urethral sphincter.2 Interestingly, in 10 reported cases of ureteral ectopia in male cats, all cats exhibited urinary incontinence, and the termination site of the ureter was the urethra in all 10 cases.13

Conclusion
This case described a young cat with urinary incontinence secondary to ectopic double ureters. The development of double ureters is an uncommon congenital anomaly that is the result of two ureteric buds originating from the mesonephric duct, and this occurs as part of a duplex kid- ney. Given the embryology of ureteral migration, ectopia may occur. Although it appears that ureteral ectopia is more common in female dogs than male dogs, the sex distribution may not be as well defined in cats. Additionally, although male dogs with ureteral ectopia appear to exhibit urinary incontinence less frequently than affected female dogs, male cats with ureteral ectopia are often incontinent. To the authors’ knowledge, this is the first case of double ureters to be reported in the cat.

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a Panalog; Fort Dodge Animal Health, Fort Dodge, IA 50501
b Amoxi-tabs; Pfizer Animal Health, Exton, PA 19341
c Hypaque 75%; Nycomed Inc., Princeton, NJ 08540
d Clavamox; Pfizer Animal Health, Exton, PA 19341

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