Introduction

Ureteral duplication is a relatively rare condition in veterinary medicine, with only six documented cases in the veterinary literature. This congenital malformation can exhibit significant anatomical variability and diverse clinical presentations. Urinary incontinence and bacteriuria are frequently reported. Anatomically, the duplicated ureters can either be functional and connected to the kidney through a unique or separate pelvicalyceal system or nonfunctional with no communication to the distal urinary tract. ^1–6

In human medicine, duplicated ureters have been reported with an incidence ranging from 0.75% to 0.8%.^7–9 Embryologically, ureters develop from metanephric ducts, which originate from the mesonephric ducts and grow toward the metanephros, ultimately forming the kidneys.¹⁰ In cases of duplicated ureters, two metanephric ducts arise from the mesonephric ducts and both connect to the metanephros. As a result, the formed kidney possesses two distinct pelvicalyceal systems.¹⁰ Frequently, one of these duplicated ureters is ectopically implanted, which can lead to urinary incontinence.

The case presented here details a 7 yr old French bulldog with a duplicated, infected, and nonfunctional ureter. To the best of the authors’ knowledge, this is the first documented case of a successfully treated infected duplicated ureter through ureterectomy.

Case Report

A 7 yr old female French bulldog was initially presented for anorexia, vomiting, and purulent vulvar discharge. Pyometra was diagnosed based on abdominal ultrasound examination and was surgically treated (ovariohysterectomy [OVH]) without complications. No other associated abnormalities were identified during preoperative workup or surgery. The dog was treated with amoxicillin-clavulanate^a (15 mg/kg q12 hr per os [PO] for 5 days) and paracetamol^b (10 mg/kg q 8 hr PO for 3 days) and discharged on day 2.

Thirteen days after surgery, the dog exhibited recurrence of a mild purulent vulvar discharge, along with stranguria and pollakiuria. A follow-up visit was scheduled by the owner 22 days after the initial surgery. Physical examination was unremarkable except purulent vulvar discharge. Complete blood cell count and serum biochemistry were within reference ranges. A urine sample was collected by cystocentesis, and analysis revealed leukocytes and red blood cells. The urinary culture was positive for Staphylococcus pseudintermedius. The sensitivity test showed that the isolated bacteria was pansensitive, including to amoxicillin-clavulanate.

An abdominal ultrasound at this stage revealed a long, dilated structure measuring 2 cm in width near the bladder and the cervix. Initially suspected to be an abscess of the residual cervix, medical management was initiated with amoxicillin-clavulanic acid^a (15 mg/kg q 12 hr PO for 5 days), meloxicam^c (0.1 mg/kg q 24 hr PO for 4 days), phloroglucinol^d (2.5 mg/kg q 12 hr PO for 5 days) and trimethylphloroglucinol^d (3.3 mg/kg q 12 hr PO for 5 days).

Thirty-four days after the initial surgery, stranguria and pollakiuria were still present, and the abdominal ultrasound examination was unchanged. A computed tomography (CT) scan confirmed the presence of a large tubular fluid-filled structure connecting the pelvis area of the right kidney to the bladder. The structure closely followed the right ureter and extended toward the bladder (Figure 1). Post-IV contrast images (IV urography) did not demonstrate a functional connection between the renal pelvis and the dilated tubular structure, whereas the left and right ureters displayed contrast within their lumens. Surgical management was proposed at this stage, but the owner declined, leading to an extended antibiotic treatment (Trimethoprim-Sulfamethoxazole^e, 16 mg/kg q 12 hr PO) over 5 wk.

View Figure

• Download as Powerpoint
• Download Figure

After the medical treatment period, the dog’s condition did not improve, prompting the owner to agree to a surgical exploration 4 mo after the initial OVH. Presurgery abdominal ultrasound examination and CT re-examination were unchanged when compared to previous results. A vagino-urethro-cystoscopy was performed and did not reveal any relevant findings in the urethra, bladder, or vagina, with both ureter papillae found in their normal positions.

Under general anaesthesia, a standard median laparotomy was performed. A tubular mass measuring 19 cm in length and 2 cm in width was observed in the retroperitoneum, extending from the cranial pole of the right kidney to the bladder neck (Figure 2). A small cystotomy was performed to facilitate antegrade urethral catheterization. An incision was made in the retroperitoneum over the right kidney, revealing a macroscopically normal kidney except for the cranial pole where the tubular structure connected to the renal parenchyma. The structure was intracapsular but seemed to culminate as a blind pouch in the renal parenchyma. Along its retroperitoneal course, the right ureter and the dilated structure were adjacent but entirely separated.

View Figure

• Download as Powerpoint
• Download Figure

At the other end, the structure entered the right side of the bladder wall near the trigone. At this point, it seemed to have an intramural course, extending further caudally on the bladder neck and ending in a blind lateral and dorsal pouch. The resection of the tubular structure was carried out from the kidney, close to the renal cortex, leaving the blind pouch open, and to the bladder wall without removing the intramural pathway. Bacterial culture was performed on the luminal contents of the duplicated ureter. Because of the close proximity between both structures, the normal ureter was also dissected from the retroperitoneal space without damaging the cranial and caudal ureteral arteries.

The remaining intramural tunnel was probed with a urinary catheter, which followed a short intramural course before exiting the bladder wall to end in a dorsolateral pouch close to the bladder neck and the urethra. This blind pouch was opened, revealing no clear communication with the bladder lumen, residual cervix, or vagina, although it may have continued further with an unseen small communication.

After resection of the tubular structure, the blind pouch of the right kidney and the intramural course of the bladder wall were omentalized. The abdomen was closed routinely following a thorough abdominal lavage. Normal urination was observed immediately after the procedure, and the dog was discharged 2 days after surgery with amoxicillin-clavulanate^a (15 mg/kg q 12 hr PO for 7 days) and meloxicam^b (0.1 mg/kg q 24 hr PO for 4 days).

The histopathology analysis of the resected structure confirmed that the sample displayed the microscopic morphology of the ureter wall, leading to the final diagnosis of a duplicated ureter. It consisted of a tubular structure lined by a transitional epithelium (urothelium), and underlying lamina propria and an outer circular layer of smooth muscle, modified by interstitial fibrosis. Intraepithial leucocytic cytosis, mainly composed of neutrophilic granulocytes, and subepithelial lymphocytic and plasmacytic infiltration of the superficial lamina propria were observed. The lumen was filled with degenerated neutrophils and contained numerous bacterial colonies. Bacterial culture revealed the presence of the same bacteria as previously identified, S pseudintermedius, which remained sensitive to amoxicillin and clavulanic acid.

Two weeks after surgery, the dog had completed her medical treatment and exhibited a complete resolution of all previously mentioned clinical signs. On abdominal ultrasound examination, the right kidney appeared nearly normal, with a residual 5 mm hyperechogenic structure within the cranial part of the cortex corresponding to the omentalization site. In addition, the right ureter appeared normal with no signs of stenosis or dilatation. Serum biochemistry analysis indicated normal urea and creatinine concentrations, and urine analysis including bacterial culture revealed no sign of urinary tract infection.

During the second follow-up, conducted 6 wk after surgery, the dog remained in good health with no reported abnormalities. Abdominal ultrasound examination and serum biochemistry analysis were unchanged. At a long-term follow-up performed 11 mo after surgery, the owner reported a favorable clinical outcome with no recurrence of clinical signs.

Informed consent was obtained from the pet owners. Additionally, the dog described in this report was clinically treated according to contemporary standards of care.

Discussion

The case reported here presented the diagnosis and management of an incomplete nonfunctional infected right ureteral duplication with a distal intramural course in a French bulldog. To the best of the authors’ knowledge, only six cases of duplicated ureters have been documented in veterinary literature, five cases in dogs and one in a cat. The anatomical descriptions of reported cases exhibit significant variations. Among these cases, only one dog appeared to have a distal blind-ended duplicated ureter, similar to the case reported here, with no apparent communication between the ureter and the bladder or urethra.¹ In that particular case, information about the functional aspect of the ureter was not provided, and there was no sign of a concurrent infection of the duplicated ureter, with a negative culture of the fluid within the lumen. In four other cases, the duplicated ureters had ectopic implantation, either intramural or extramural.^2–4,6 Among these four cases, three involved young animals.

In humans, ureteral duplication is a relatively common abnormality of the urinary tract, with an incidence ranging from 0.75% to 0.80%.^7–9 Duplicated ureters can exhibit anatomical variations and can be classified as complete or incomplete.¹¹ Complete duplication involves a duplicated ureter that drains a portion of the kidney, typically at the cranial pole with two distinct pyelocaliceal systems. In that configuration, the drained portion is usually smaller than the one served by the normal ureter. The duplicated ureter is usually functional, allowing urine to flow to the bladder.¹² In contrast, incomplete duplication is less common and can exhibit various patterns: two portions of the kidney can be drained by separate ureters that may fuse into one bladder insertion; or one renal pelvis can be drained by one ureter that splits into two portions, each one having its own bladder insertion also known as a caudal bifid ureter.¹² In those cases, the incomplete duplication may be functional. Finally, a partial development of the duplicated ureter may occur and exhibit three distinct anatomies: the duplicated portion of the ureter can be blind distally, proximally, or double-blind. Double-blind ureters are the rarest.¹³ In proximal blind ureters, the duplication is usually nonfunctional. Conversely, distal blind-ending ureters may be functional and may lead to complications such as infection, urine stasis, hydroureter, hydronephrosis, and pain due to pressure within the blind sac.^14,15 In humans, incomplete ureteral duplication is diagnosed less frequently.¹⁶

In the current case study, the duplicated ureter presented as an incomplete, nonfunctional duplication. Firstly, the duplicated ureter seemed to be blind distally: no evidence of communication between the duplicated ureter and the lower urinary tract was found on CT, vaginoscopy, or surgery, making the presence of ectopic implantation unlikely. Secondly, the absence of contrast within the duplicated ureter’s lumen during the IV urography performed during the CT examination supports its nonfunctionality despite the fact that the ureter was apparently connected to the kidney. Thirdly, there was no uroabdomen reported after the removal of the ureter or any type of urine collection in the right renal cranial omentalized cavity observed on the postoperative ultrasonography. Moreover, the lack of hydronephrosis is consistent with a nonfunctional ureter even during the early life of the dog. In 2006, Ghantous and Crawford² reported the case of a young cat with a complete duplicated functional ureter with an extramural ectopic implantation, associated with severe hydronephrosis. In the case reported here, suture around an initially patent duplicated ureter secondary to the ovariohysterectomy performed a few months earlier could have led to an apparent blind-ended ureter. However, no suture or stricture was observed during the surgery over the distal end of the duplicated ureter.

Urinary incontinence was a common clinical sign, affecting four out of the six animals in the literature, suggesting that the duplicated ureters described were functional. Although urinary incontinence is often observed in young animals, it can also be present in older patients. In 2013, Novellas and colleagues⁴ reported the case of a 9 yr old Labrador retriever with chronic urinary infection and occasional urine dribbling. The dog had a duplicated ureter originating from the left renal pelvis, entering the bladder wall near the trigone with an intramural course, and an ectopic opening in the prostatic urethra. Histological analysis was performed in only two cases and showed similar aspects to what we observed in this study.^1,2

In contrast to the classic presentation, the case presented here involved a 7 yr old female dog with no previous history of urinary incontinence. Clinical signs appeared after the treatment of a pyometra with OVH and were primarily characterized by persistent vulvar discharge, pollakiuria, and dysuria. The ultrasound examination carried out during the diagnosis of pyometra was unable to identify the dilation of the duplicated ureter. We may suspect that the anomaly was missed or that it was not visible because it was not dilated. The dilation may have occurred after the OVH procedure if the infection started at that time. Surgical removal of the duplicated ureter resolved the clinical signs, and the dog fully recovered with no complications during long-term follow-up.

For the diagnosis, a combination of imaging modalities has been used in other documented cases in the literature.^1–6 The most frequently used modalities are radiography and CT. As for the management of this condition, there are currently no standardized recommendations. In the current case study, a combination of ultrasound, CT with contrast, and vaginoscopy was used and failed to precisely describe the anatomy of the duplicated ureter before surgery. A retrograde urethrography could have helped us find the potential distal implantation of the duplicated ureter.

The management of duplicated ureters varies on a case-by-case basis, ranging from medical treatment to surgical procedures.^1–6 In the veterinary literature, due to the close association between the kidney, the normal ureter, and the duplicated one, nephrectomy is often chosen over other surgical approaches. Among the six reported cases, one dog was treated medically,⁵ one dog underwent ureteroneocystostomy,³ and two dogs and one cat underwent nephro-ureterectomy.^1,2,6 Additionally, one dog was treated similarly to the dog reported in this study, with the removal of the duplicated ureter.⁴ Unfortunately, this dog experienced a recurrence of anorexia, abdominal pain, and urinary incontinence 5 mo after surgery and was euthanatized. In cases of functional duplicated ureter, ureteroneocystostomy should be considered to prevent urine leakage and preserve renal function. In such cases, the duplicated ureter drains a portion of the renal parenchyma, and maintaining function in these nephric tubes, as demonstrated in the case treated by Newman and Landon³ in 2014, is essential. In the case reported here, because the duplicated ureter was deemed nonfunctional and blind distally, a subtotal ureterectomy leaving only the distal portion of the ureter was feasible. To preserve the integrity of the bladder wall and conserve renal parenchyma, we chose to omentalize the proximal and distal ends of the ureter rather than performing a complete excision, which would have required a partial nephrectomy and partial cystectomy near the trigone and potentially damaging the normal course of the right ureter. This treatment approach resulted in a rapid and complete recovery with the resolution of all clinical signs.

The reason for the recurrence of purulent vulvar discharge and the development of a urinary tract infection after the ovariohysterectomy remains unclear. As discussed earlier, infection of a blind-ended duplicated ureter has been already reported in human literature.^14,15 In the case reported here, a urinary culture revealed the presence of a urinary tract infection with S pseudintermedius during the initial recurrence of purulent vulvar discharge. Bacterial culture during surgery identified the same bacteria. Because there was no clear communication between the blind ureter and the urogenital system, a simple ascending infection appears less likely but possible. Otherwise, it can only be speculated that bacterial contamination from the lower urinary tract to the duplicated ureter could have occurred via hematogenous translocation or through the bladder wall. In this case, the same bacteria may have caused the infection of the duplicated ureter, the lower urinary tract, and the remaining genital tract, causing the purulent discharge. The removal of the duplicated infected ureter may have suppressed the source of bacteria, which remained persistent despite the previous antibiotherapy.

Conclusion

The case reported here describes the successful treatment of an infected duplicated ureter in a 7 yr old dog. Surgical resection of the duplicated ureter resolved the clinical signs and can offer a viable treatment option for similar cases.