Bilateral renal descensus and intravesicular ureteroneocystostomy for treatment of bilateral ureteral ligation and transection that occurred during ovariohysterectomy in two cats

Shira T. Rosenblum Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA

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Lillian R. Aronson Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA

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Abstract

CASE DESCRIPTION

6-month-old and 7-month-old spayed female domestic shorthair cats were referred because of complications associated with inadvertent bilateral ureteral ligation and transection during ovariohysterectomy.

CLINICAL FINDINGS

Both cats had a 1- to 2-day history of lethargy, inappetence, and vomiting. Initial exam findings included lethargy, signs of abdominal pain, anuria, and dehydration. Clinicopathologic testing revealed azotemia and hyperkalemia. Abdominal ultrasonography revealed peritoneal effusion and bilateral pyelectasia in both cats and retroperitoneal effusion in one. Fluid analysis in both cats supported a diagnosis of uroabdomen.

TREATMENT AND OUTCOME

Exploratory celiotomy was performed in both cats, and bilateral ureteral ligation and transection was confirmed. Bilateral renal descensus and ureteroneocystostomy with an intravesicular mucosal apposition technique was successfully performed in both cats. Clinicopathologic evaluation performed 1 day after surgery in one cat and 5 days after surgery in the other revealed complete resolution of azotemia. Ultrasonographic examination of the urogenital tract performed approximately 4 months after surgery in the first cat and 1 month after surgery in the second cat revealed complete resolution of renal pelvic dilation bilaterally.

CLINICAL RELEVANCE

Bilateral intravesicular ureteroneocystostomy in conjunction with bilateral renal descensus was used successfully to treat bilateral ureteral transection that occurred in 2 cats during routine ovariohysterectomy. Limited treatment options currently exist for this serious complication, and euthanasia is often considered. This technique, which relies on the use of the natural surrounding tissues for successful treatment, can offer a potential treatment option to correct this uncommon but devastating complication.

Abstract

CASE DESCRIPTION

6-month-old and 7-month-old spayed female domestic shorthair cats were referred because of complications associated with inadvertent bilateral ureteral ligation and transection during ovariohysterectomy.

CLINICAL FINDINGS

Both cats had a 1- to 2-day history of lethargy, inappetence, and vomiting. Initial exam findings included lethargy, signs of abdominal pain, anuria, and dehydration. Clinicopathologic testing revealed azotemia and hyperkalemia. Abdominal ultrasonography revealed peritoneal effusion and bilateral pyelectasia in both cats and retroperitoneal effusion in one. Fluid analysis in both cats supported a diagnosis of uroabdomen.

TREATMENT AND OUTCOME

Exploratory celiotomy was performed in both cats, and bilateral ureteral ligation and transection was confirmed. Bilateral renal descensus and ureteroneocystostomy with an intravesicular mucosal apposition technique was successfully performed in both cats. Clinicopathologic evaluation performed 1 day after surgery in one cat and 5 days after surgery in the other revealed complete resolution of azotemia. Ultrasonographic examination of the urogenital tract performed approximately 4 months after surgery in the first cat and 1 month after surgery in the second cat revealed complete resolution of renal pelvic dilation bilaterally.

CLINICAL RELEVANCE

Bilateral intravesicular ureteroneocystostomy in conjunction with bilateral renal descensus was used successfully to treat bilateral ureteral transection that occurred in 2 cats during routine ovariohysterectomy. Limited treatment options currently exist for this serious complication, and euthanasia is often considered. This technique, which relies on the use of the natural surrounding tissues for successful treatment, can offer a potential treatment option to correct this uncommon but devastating complication.

Introduction

A 6-month-old 2.0-kg female domestic shorthair cat (cat 1) was presented to her primary care veterinarian for elective ovariohysterectomy (OVH), which was performed with a CO2 laser. Results of preoperative biochemical testing were within reference limits (BUN, 19 mg/dL [reference range {RR}, 16 to 33 mg/dL]; creatinine, 1.0 mg/dL [RR, 0.6 to 1.6 mg/dL]; potassium, 3.8 mmol/L [RR, 3.7 to 5.9 mmol/L]). The cat recovered uneventfully and was discharged with prescriptions for amoxicillin (dosage and duration not reported) and buprenorphine (dosage and duration not reported). Later that evening, the cat started vocalizing and vomiting, became lethargic, and refused to eat. Serum biochemical testing performed the following day revealed severe azotemia (BUN, 102 mg/dL; creatinine, 3.3 mg/dL), hyperphosphatemia (13.4 mg/dL; RR, 4.5 to 10.4 mg/dL), a high symmetric dimethylarginine concentration (62 μg/dL; RR, 0 to 14 μg/dL), hyperglycemia (202 mg/dL; RR, 77 to 163 mg/dL), hyperalbuminemia (4.0 g/dL; RR, 2.2 to 3.9 g/dL), hypercholesterolemia (206 mg/dL; RR, 62 to 191 mg/dL), hyponatremia (149 mmol/L; RR, 150 to 165 mmol/L), and hypochloremia (110 mmol/L; RR, 115 to 125 mmol/L). A CBC showed hemoconcentration (Hct, 52.6%; RR, 30.3% to 52.3%), leukocytosis (WBC count, 21.78×103 cells/μL; RR, 2.87×103 to 17.02×103 cells/μL), neutrophilia (11.25×103 cells/μL; RR, 2.30×103 to 10.29×103 cells/μL), lymphocytosis (9.93×103 cells/μL; RR, 0.92×103 to 6.88×103 cells/μL), and thrombocytopenia (133×103 platelets/μL; RR, 151×103 to 600×103 platelets/μL). Abdominal effusion was suspected on the basis of physical examination findings, and abdominal fluid creatinine and potassium concentrations were consistent with uroabdomen (creatinine, > 15 mg/dL; potassium, 11.8 mmol/L).

The patient was transferred to a nearby specialty hospital. On presentation, the cat was dull and tachycardic (230 beats/min) with signs of pain on abdominal palpation. Repeated blood work revealed severe azotemia (BUN, > 140 mg/dL; creatinine, 5.0 mg/dL), hyponatremia (128 mmol/L), and hypochloremia (111 mmol/L). Serum potassium concentration was normal (4.7 mmol/L). An abdominal focused assessment with sonography for trauma (AFAST) revealed a large amount of abdominal effusion and a large fluid-filled stomach. Repeated evaluation of the effusion supported the diagnosis of uroabdomen (creatinine, > 14.6 mg/dL; potassium, > 9 mmol/L). A 5F, red rubber urinary catheter was placed, but no urine was obtained while the patient was hospitalized. A 14-gauge chest tube was placed as an abdominal drain and produced 20 to 80 mL of fluid every 2 hours. Retrograde contrast cystourethrography revealed ureteral reflux and extravasation of contrast into the peritoneal cavity (Figure 1). A 5F, triple-lumen left jugular vein catheter was placed, and the patient was treated with lactated Ringer solution (3 mL/kg/h, IV) and fentanyl (3 μg/kg/h, IV as a continuous rate infusion [CRI]). The next morning, the patient remained tachycardic, and blood work revealed persistent azotemia (BUN, 140 mg/dL; creatinine, 5.4 mg/dL). The IV fluid rate was increased to 7.5 mL/kg/h with the addition of metoclopramide (1 mg/kg/d, IV), ketamine (0.3 mg/kg/h, IV), and ampicillin-sulbactam (64.8 mg, IV, q 8 h). Abdominal ultrasonography revealed a moderate to large amount of peritoneal effusion, mild left retroperitoneal effusion, mild to moderate bilateral pelvic dilation with blunting of the left renal pelvis (left renal pelvis diameter, 4.4 mm; right renal pelvis diameter, 2.4 mm), and mild bilateral proximal-to-mid-ureteral dilation (left ureter diameter, 1.7 mm; right ureter diameter, 1.2 mm). Both ureters then tapered and could not be traced further. Blood work at this time identified a developing metabolic acidosis (total CO2, 15 mmol/L; RR, 16.0 to 25.0 mmol/L) and dehydration (PCV, 42%; total solids, 9.8 g/dL). The patient was referred to the Matthew J. Ryan Veterinary Hospital of the University of Pennsylvania (MJR-VHUP) for further management. A urinary catheter, nasogastric tube, abdominal drain, and abdominal bandage were all in place at the time of the patient’s arrival.

Figure 1
Figure 1

Lateral radiographic image obtained during retrograde contrast cystourethrography in a 6-month-old cat (cat 1) in which inadvertent bilateral ureteral ligation and transection had occurred during ovariohysterectomy. Notice the extravasation of contrast into the peritoneal cavity from a distal ureteral segment.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.10.0596

On presentation, the cat was quiet and alert, 5% dehydrated, tachycardic (heart rate, 240 beats/min), and had signs of pain on abdominal palpation. Neither the abdominal drain nor the urinary catheter was draining any fluid. An AFAST showed a large amount of abdominal effusion and a small bladder. Blood work revealed persistence of azotemia (BUN, 164.7 mg/dL; creatinine, 4.4 mg/dL), a primary metabolic acidosis with compensatory respiratory alkalosis (pH, 7.232; Pco2, 33.5 mm Hg; Po2, 39.3 mm Hg; total CO2, 15.3 mmol/L), hyperkalemia (5.66 mmol/L), hyponatremia (135.9 mmol/L), and hyperglycemia (264 mg/dL). The cat was sedated with midazolam (0.2 mg/kg), fentanyl (2 μg/kg), and ketamine (2 mg/kg), IV. The abdominal drain was easily flushed with saline (0.9% NaCl) solution; however, because of limited drainage, it was replaced. Approximately 140 mL of abdominal effusion was subsequently drained.

A full ultrasonographic examination of the urinary system was performed. Mild pyelectasia (renal pelvis diameter up to 3.0 mm) was present bilaterally. Both the left and right ureters were visible proximally with minimal distension (ureter diameter up to 1.4 mm) and then visible distally at the ureterovesicular junction. The mid-portion of each ureter could not be identified. The right ureter was circumcaval. The bladder was empty. A mild to moderate amount of echogenic fluid was visualized in the peritoneal and retroperitoneal spaces consistent with the previously diagnosed uroabdomen. Intravenous excretory urography (4.4 mL of iohexol [350 mg of iodine/mL], over 22 minutes) showed bilateral contrast extravasation at the level of the mid ureter. On the basis of these results, surgical exploration was recommended.

The cat was premedicated with alfaxalone (1 mg/kg, IV), and anesthesia was induced with midazolam (0.3 mg/kg, IV) and alfaxalone (0.5 mg/kg IV). An epidural injection of 0.5% bupivacaine (0.4 mL) was performed. The cat received a balanced electrolyte solution (Plasma Lyte A; 7.5 mL/kg/h, IV) and metoclopramide (1 mg/kg/d, IV). Ampicillin (22 mg/kg, IV) was administered every 90 minutes during surgery. Anesthesia was maintained with isoflurane. During the procedure, the patient received CRIs of remifentanil (0.05 to 0.4 μg/kg/min), dopamine (2 to 12 μg/kg/min), and dexmedetomidine (0.25 to 1 μg/kg/h).

A full exploratory laparotomy was performed, and the kidneys and ureters were isolated by means of blunt dissection with right-angle forceps. A large blood clot surrounding the uterine stump was noted. The left ureter was found to be transected at the level of the uterine stump, and the distal segment of the transected ureter was adhered to the stump. The end of the proximal segment of the left ureter appeared necrotic and was adhered to the left ovarian pedicle ligature. The right ureter was circumcaval and was found to be transected midway between the kidney and bladder. A 5-mm region of necrotic retroperitoneal fat surrounded the distal end of the proximal portion of the right ureter (Figure 2). Areas of tissue necrosis were identified and debrided at the level of ureteral transection where the laser had been used in the previous surgery. The right ureter was brought under the vena cava so that it was no longer circumcaval. The distal segments of each ureter were identified at their insertion into the trigone of the bladder and debrided and ligated with 2 encircling ligatures of 4-0 polydioxanone. Following dissection of both ureters, approximately 3 cm of normal ureter remained on the left side and 4 cm on the right side (Figure 3). Prior to ureteral reimplantation, bilateral renal descensus was performed to decrease tension at the anastomotic site. Both kidneys were dissected from their retroperitoneal attachments and moved approximately 2 to 3 cm caudally. A ventral midline cystotomy was performed and each ureter was pulled into the lumen of the urinary bladder with a mosquito hemostat, one at the left lateral apical region and the other at the right lateral apical region, approximately 2 cm apart. An intravesicular mucosal appositional technique was performed with an operating microscope with 10X magnification as previously described.1 The end of each ureter was debrided and then spatulated with straight microvascular scissors. The bladder was temporarily inverted. Approximately 8 simple interrupted sutures of 8-0 nylon were placed circumferentially, suturing ureteral mucosa to bladder mucosa. Urine flow through each anastomotic site was confirmed. The bladder was closed routinely with 4-0 polydioxanone in a simple continuous pattern. A cystopexy was performed with 2 simple interrupted sutures of 4-0 polypropylene through the lateral muscular and serosal layers of the bladder and the abdominal musculature. The abdomen was lavaged with sterile saline solution, and a nephropexy to the adjacent lateral abdominal body wall was performed bilaterally with 3 or 4 sutures of 4-0 polypropylene in a simple interrupted pattern (Figure 4). Prior to closure, a swab of the abdomen was submitted for aerobic bacterial culture and susceptibility testing. The abdomen was closed routinely. Lyophilized bupivacaine (Nocita; 0.4 mL/kg) was injected SC.

Figure 2
Figure 2

Intraoperative photograph of cat 1 prior to surgical correction. The right ureter is circumcaval (top arrow) and has been transected midway between the kidney and bladder. A 5-mm region of necrotic tissue is evident (bottom arrow) at the distal end of the proximal portion of the right ureter.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.10.0596

Figure 3
Figure 3

Intraoperative photograph of cat 1 following debridement of necrotic tissue and isolation of each ureter prior to ureteroneocystostomy. A—Proximal segment of the left ureter (arrow). Approximately 3 cm of normal ureter is present. B—Proximal segment of the right ureter after being brought under the vena cava so that it was no longer circumcaval (arrow). Approximately 4 cm of normal ureter is present.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.10.0596

Figure 4
Figure 4

Intraoperative photograph of cat 1 following bilateral renal descensus and bilateral intravesicular ureteroneocystostomy. The left of the image is caudal, and the right of the image is cranial. Both ureters can be seen entering the apical region of the bladder, approximately 2 cm apart. Right nephropexy and cystopexy have been performed.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.10.0596

The patient was maintained on the balanced electrolyte solution (5 mL/kg/h, IV), and metoclopramide (1 mg/kg/d, IV); fentanyl (3 μg/kg/h, IV) and dexmedetomidine (0.5 μg/kg/h, IV) were administered for pain relief. Fluid rate and type were adjusted on the basis of urine output, physical examination findings, and regular measurement of serum electrolyte concentrations. A urinary catheter was not left in place after surgery, and urine output was measured by weighing the pads provided to the cat for urination. Antimicrobial treatment was switched from ampicillin-sulbactam to piperacillin-tazobactam (40 mg/kg, IV, q 6 h) because ampicillin-sulbactam was not in stock at the time. Maropitant citrate (Cerenia; 1 mg/kg, IV, q 24 h) was given as an anti-nausea medication. The patient started producing small amounts of urine approximately 1 hour after surgery, and urine output increased to moderate amounts of blood-tinged urine over the next 12 hours. The morning after surgery, the cat urinated a steady stream. A serum biochemistry profile at this time revealed resolution of the azotemia (BUN, 23 mg/dL; creatinine, 0.5 mg/dL), hypoproteinemia (total protein, 4.6 g/dL [RR, 6.0 to 8.6 g/dL]; albumin, 2.2 g/dL [RR, 2.4 to 3.8 g/dL]; globulin, 2.4 g/dL [RR, 3.1 to 5.0 g/dL]), and mild hypochloremia (115 mmol/L). A CBC revealed mild anemia (Hct, 25.6%) and lymphopenia (340 cells/μL). An AFAST revealed a scant amount of anechoic peritoneal fluid, a thickened bladder wall, and a small volume of urine in the bladder. The dosage of dexmedetomidine was reduced to 0.25 mg/kg/h, administration of fentanyl was discontinued, and the cat was started on methadone (0.1 to 0.2 mg/kg, IV, q 4 to 6 hours) as needed for discomfort.

Two days after surgery, the patient was bright and alert and was transferred out of the intensive care unit. Physical examination findings remained within reference limits throughout the day. The cat was weaned off all IV medications and was discharged 3 days after surgery with buprenorphine (0.01 mg/kg, applied to the gums q 8 to 12 hours for 3 days) as needed for pain. Recheck ultrasonography was performed approximately 4, 7, and 18 months after surgery by the cat’s primary care veterinarian, which showed no evidence of renal pelvic dilation. Results of blood work and a urinalysis performed approximately 4 months after surgery were unremarkable.

A 7-month-old 2.5-kg female domestic shorthair cat (cat 2) was presented to her primary care veterinarian for routine OVH. Preanesthetic blood work showed a mildly high serum alanine transaminase activity, but results were otherwise within reference limits. Information regarding the anesthetic protocol was not available. The patient recovered well from surgery, but became progressively weak and lethargic, developed inappetence, and had an episode of vomiting that evening. Two days later, the cat was presented to a referral hospital because of persistent vomiting and surgical site dehiscence. The surgical site was debrided and closed under general anesthesia. Blood work performed at this time showed marked azotemia (BUN, too high to read; creatinine, 8.4 mg/dL) and hyperkalemia (8.19 mmol/L). The cat was hospitalized but did not produce any urine and only minor improvements in electrolyte status were noted. The patient was transferred to a second referral hospital 2 days later where abdominal ultrasonography was performed. Abnormal findings included mild bilateral pylectasia (left renal pelvis diameter, 2.7 mm; right renal pelvis diameter, 2.7 mm) and mild dilation of the proximal portions of the left and right ureters that then tapered to a normal diameter. Both the left and right ureters could be traced several centimeters caudally to small areas of hypoechoic tissue containing multiple hyperechoic foci that were suspected to be the ovarian pedicles. The ureters could not be traced distal to this location. In addition, a mild amount of peritoneal effusion and a moderate to large volume of retroperitoneal effusion was noted bilaterally. The cat was transferred to the MJR-VHUP for further management.

During the initial physical exam, the cat was quiet, alert, and responsive. The cat was tachypneic (60 breaths/min) with harsh lung sound bilaterally, bradycardic (140 beats/min), and had marked ptyalism. The urinary bladder was small on abdominal palpation. An AFAST revealed moderate retroperitoneal effusion and scant peritoneal effusion. Biochemical evaluation revealed a metabolic acidosis with a compensatory respiratory alkalosis (pH, 7.121; Pco2, 25.7 mm Hg; Po2, 46.0 mm Hg; total CO2, 9.2 mmol/L) and hyperkalemia (8.10 mmol/L). Serum creatinine and BUN concentrations were too high to measure. Repeated electrolyte and biochemical testing 4 hours later revealed progression of the metabolic acidosis (pH, 7.099; Pco2, 26.0 mm Hg; Po2, 45.0 mm Hg; total CO2, 8.9 mmol/L) and persistent hyperkalemia (6.40 mmol/L), which was treated with a dextrose bolus (0.5 g/kg, IV), regular insulin (1 unit, IV), and a balanced electrolyte solution containing 2.5% dextrose (2 mL/kg/h, IV). Other treatments included maropitant citrate (1 mg/kg, IV, q 24 h), buprenorphine (0.005 mg/kg, IV, q 6 h), metronidazole (7.5 mg/kg, IV, q 12 h), and pantoprazole (0.7 mg/kg, IV, q 12 h). The cat remained anuric. At this time, exploratory celiotomy was recommended.

Urogenital ultrasonography was repeated to better characterize the ureteral injury and for surgical planning purposes. Findings were similar to those of the previous exam with worsening pyelectasia (left renal pelvis diameter, 3.4 mm; right renal pelvis diameter, 4.7 mm), ureteral dilation (left ureter diameter, 2.0 mm; right ureter diameter, 2.0 mm) and a subjectively increased amount of retroperitoneal effusion. Additionally, the bladder contained amorphous, dependent, echogenic sediment. Given the worsening retroperitoneal effusion, ureteral ligation at the ovariectomy site with concurrent transection was suspected, and surgery was recommended. Anesthesia was induced with midazolam (0.3 mg/kg, IV) and maintained with isoflurane. During the procedure, the patient received a CRI of remifentanil (0.1 to 0.2 μg/kg/min). Cefazolin (22 mg/kg, IV) was given 30 minutes prior to anesthetic induction and every 90 minutes during the surgical procedure.

Abdominal exploration revealed that both ureters had been ligated at the level of the ovarian pedicle and transected. Following ligature removal and debridement of devitalized tissue, approximately 3.0 cm of the proximal aspect of the right ureter and 1.5 to 2.0 cm of the proximal aspect of the left ureter remained. The distal portion of the right ureter was removed, but the distal portion of the left ureter was not resected until the end of the procedure in case that segment would be needed for an alternative repair procedure. Both ovarian pedicles were ligated again with 4-0 polydioxanone. Owing to the short length of the proximal ureters, renal descensus was performed bilaterally.

Ureteroneocystostomy with an intravesicular mucosal appositional technique similar to that described for cat 1 was performed bilaterally. The bladder was closed with 4-0 polydioxanone in a simple continuous pattern. The remaining distal portion of the left ureter was then ligated with 4-0 polydioxanone and resected. Nephropexy was performed bilaterally to the adjacent lateral abdominal body wall with 3 or 4 sutures of 4-0 polypropylene in a simple interrupted pattern (Figure 5). The abdomen was lavaged, and a swab was taken of purulent exudate at the site of the previous ovariectomy for aerobic bacterial culture (no growth was obtained). The abdomen was closed routinely. Lyophilized bupivacaine (0.37 mL/kg, SC) was administered, and immediately after surgery, an esophageal tube and triple-lumen IV catheter were placed. A CBC and serum biochemical testing performed immediately after surgery revealed severe azotemia (BUN, 209 mg/dL; creatinine, 15 mg/dL), hyperphosphatemia (16.1 mg/dL), and hyperkalemia (6.6 mmol/L). Extended testing revealed a primary metabolic acidosis with compensatory respiratory alkalosis (pH, 7.043; Pco2, 37.2 mm Hg; HCO3, 9.9 mmol/L; base excess in blood, –19.9 mmol/L; base excess in extracellular fluid, –20.7 mmol/L).

Figure 5
Figure 5

Intraoperative photograph of a 7-month-old cat (cat 2) in which inadvertent bilateral ureteral ligation and transection had occurred during ovariohysterectomy. Bilateral renal descensus and bilateral intravesicular ureteroneocystostomy have been performed. The top of the image is cranial, and the bottom of the image is caudal. The left and right kidneys can be seen, along with their respective ureters inserting into the apical region of the bladder, approximately 2 cm apart.

Citation: Journal of the American Veterinary Medical Association 260, 1; 10.2460/javma.20.10.0596

Following surgery, urine production began immediately. The patient was maintained on a balanced electrolyte solution (8 mL/kg/h, IV) and CRIs of fentanyl (1 μg/kg/h, IV) and dexmedetomidine (0.25 μg/kg/h, IV). Treatment with piperacillin-tazobactam (50 mg/kg, IV, q 6 h) was also initiated. The cat developed diarrhea following the surgical procedure.

By the next morning, the cat was quiet, alert, and responsive. The cat had no interest in food, but was drinking well, urinating large volumes frequently, and appeared comfortable. An AFAST revealed mild peritoneal effusion. A renal panel performed that morning revealed an improvement in the patient’s azotemia (BUN, 177 mg/dL; creatinine, 10.1 mg/dL), hyperphosphatemia (14.6 mg/dL), and hyperkalemia (5.5 mmol/L). By the afternoon, urine production had decreased (as measured by weighing urine-soaked pads), and a repeated AFAST was performed, which revealed an increased volume of abdominal effusion. Evaluation of creatinine concentrations in paired abdominal effusion (12.9 mg/dL) and blood (6.7 mg/dL) samples confirmed the suspicion of uroabdomen.

To determine the site of leakage, the patient was anesthetized that evening for retrograde contrast cystourethrography with iohexol (2.9 mL/kg [240 mg of iodine/mL]). A scant amount of contrast extravasation was identified after the full volume of contrast medium was given, but it was impossible to tell from which ureteroneocystostomy site it came. A 3.5F, red rubber urinary catheter was placed for 48 hours to keep the bladder decompressed and allow for the ureteroneocystostomy sites to heal. After placement of the catheter, approximately 180 mL of fluid was removed from the patient’s abdominal cavity via abdominocentesis with a 20-gauge catheter. Urine output was consistent throughout the evening and into the next morning. Testing of a venous blood sample at this time revealed an improving primary metabolic acidosis with compensatory respiratory alkalosis (pH, 7.241; Pco2, 41.5 mmHg; HCO3, 17.4 mmol/L; base excess in blood, –9.3 mmol/L; base excess in extracellular fluid, –10.0 mmol/L).

Two days after surgery, the cat was bright, alert, responsive, and ambulating around the cage. Blood work revealed continued improvement in azotemia (BUN, 99 mg/dL; creatinine, 4.8 mg/dL) and hyperphosphatemia (7.8 mg/dL). The patient was anemic (Hct, 25%) and had mild hypoproteinemia (total protein, 5 g/dL); therefore, a unit of packed RBCs was administered. An AFAST revealed persistence of a moderate amount of abdominal effusion. Axillary temperature was 39.1 °C at this time.

Three days after surgery, the cat was still bright, alert, responsive, and ambulating well around the cage. Further improvement in the azotemia (BUN, 62 mg/dL; creatinine, 3.0 mg/dL) and normalization of the serum phosphorus concentration (6.4 mg/dL) were identified. Hypoproteinemia (total protein, 5.0 g/dL; albumin, 2.3 g/dL; globulin, 2.7 g/dL) was still present. A CBC at this time revealed a nonregenerative anemia (27.2%), neutrophilia (11.75×103 cells/μL), and thrombocytopenia (32×103 platelets/μL). Focused thoracic ultrasonography performed at this time revealed a left atrial-to-aortic diameter ratio of 1.28:1; a repeated AFAST revealed persistence of moderate peritoneal effusion.

Given the findings from the AFAST and thoracic ultrasonography, a full ultrasonographic examination of the urinary system was performed. Findings included mildly enlarged kidneys bilaterally with normal corticomedullary ratios. The right renal pelvis measured 3.4 mm and the left measured 4.0 mm in diameter. Both ureters were dilated proximally (right ureter diameter, 3.0 mm; left ureter diameter, 3.6 mm) and tapered gradually until entering the apex of the bladder. Perirenal fat on the right and left kidneys was hyperechoic. The urinary bladder was minimally distended with anechoic fluid and was bordered by thickened hypoechoic walls. The indwelling urinary catheter was visible within the urethra and terminated at the level of the bladder trigone. A large volume of minimally echogenic free peritoneal fluid was noted, as well as lobular caudal abdominal steatitis. The left and right medial iliac lymph nodes and caudal mesenteric lymph nodes were also mildly enlarged. To assess the previous area of possible leakage, positive-contrast cystography was performed. No evidence of leakage was identified.

Four days after surgery, the cat was quiet and sedate with an axillary temperature of 40.7 °C. Administration of piperacillin-tazobactam was discontinued, and administration of clindamycin (10 mg/kg, IV, q 12 h) and ceftazidime (50 mg/kg, IV, q 6 h) was started because of the high axillary temperature, unresponsiveness to current antimicrobial treatment, and preliminary culture results of the peritoneal effusion suggestive of septic peritonitis. A new grade II to III/VI left systolic murmur was noted during a physical exam, and an echocardiogram was performed. The murmur was diagnosed as a suspected physiologic flow murmur, but a round to ovoid, irregularly marginated lesion was noted at the level of the tricuspid valve. Because the tip of the triple-lumen catheter was located so close to this lesion, the catheter was removed and the tip of the catheter was submitted for bacterial culture. Trace tricuspid regurgitation and aortic insufficiency were also noted at this time. An AFAST revealed that the peritoneal effusion had become more echogenic. Abdominocentesis was performed, and 60 mL of blood-tinged fluid was removed. Lactate concentration in the abdominal fluid was 1.7 mg/dL and glucose concentration was 121 mg/dL, whereas blood lactate concentration was 0.32 mg/dL and blood glucose concentration was 154 mg/dL. A sample of the abdominal fluid was submitted for bacterial culture and susceptibility testing.

Five days after surgery, the azotemia had completely resolved (BUN, 18 mg/dL; creatinine, 1.4 mg/dL) and the axillary temperature had decreased to 39.1 °C. A repeat echocardiogram was performed to reassess the suspect tricuspid valve lesion and revealed persistence of a lesion that appeared to move back and forth between the right atrium and right ventricle as the tricuspid valve opened and closed. There also appeared to be subjectively increased tricuspid regurgitation, suggesting that the lesion was not an artifact due to the catheter but a possible vegetative lesion or clot. The following day, bacterial culture of the abdominal fluid yielded a multidrug-resistant Enterococcus faecium strain susceptible to linezolid, tigecycline, and vancomycin. Treatment with vancomycin (15 mg/kg, IV, q 8 h) was started at this time. Axillary temperature that morning was 39.3 °C. The cat underwent abdominal ultrasonography to reassess the urogenital system and abdominal effusion. Ultrasonography revealed improved pyelectasia (2.6 mm) and ureteral dilation (2.2 mm) on the right with slightly progressive pyelectasia (4.7 mm) and proximal ureteral dilation (4.4 mm) on the left. Both ureteral implantation sites were visualized and appeared patent given the presence of ureteral jets. The urinary bladder wall was subjectively less thickened than it had been at the time of the previous examination. The echogenic peritoneal free fluid was improved and overall seemed to have decreased in volume since the last examination. Mild generalized lymphadenopathy was noted.

Approximately 24 hours after treatment with vancomycin was started, the patient’s axillary temperature was 38.2 °C and remained normal until the cat was discharged. To transition from IV to PO antimicrobial treatment, the cat was switched from vancomycin to linezolid (10 mg/kg, PO, q 8 h). A CBC revealed a normal WBC count, but severe nonregenerative anemia (Hct, 16%). Because of the severe anemia, the cat received a unit of cross-matched packed RBCs.

Over the next 5 days, the cat continued to improve clinically. Prior to discharge, urinary ultrasonography and an echocardiogram were performed. Ultrasonography showed that the appearance of the right kidney continued to improve with a decrease in pelvic and ureteral dilation. The pelvis of the left kidney had a similar degree of dilation, compared with that seen during the previous exam; however, fluid within the left renal pelvis contained echogenic content. At the level of the left hilus was a lobular, heterogeneously hyperechoic structure with hypoechoic striations measuring approximately 7.4×11 mm. This tissue was thought to represent inflammation of the peri-renal fat. The neoureterovesicular junctions appeared patent. The bladder wall thickness was within reference limits. To rule out pyelonephritis of the left kidney, ultrasound-guided cystocentesis was performed. Urinalysis showed a urine specific gravity of 1.026, a pH of 5.0, 1+ protein, 4+ blood, 1 to 4 WBC/hpf, and few epithelial cells. Although the cat was receiving antimicrobials, bacterial culture of a urine sample was performed to determine whether treatment was appropriate. A recheck echocardiogram revealed persistence of the previously noted lesion near the tricuspid valve or chordae tendinae as well as a similar amount of mild tricuspid regurgitation. Differential diagnoses for the lesion remained unchanged as vegetative lesion or clot. The patient was discharged 11 days after surgery with instructions for the owner to administer linezolid (25 mg, PO, q 8 h for 4 weeks) and maropitant citrate (4 mg, PO, q 24 h) as needed for nausea. At a recheck examination performed approximately 20 days following discharge, continued improvement of left renal pelvic dilation was identified as well as complete resolution of the vegetative lesion near the tricuspid valve. Complete resolution of the pelvic dilation was noted approximately 4 weeks after discharge.

Discussion

Despite the frequency with which most veterinarians perform elective OVH in cats, iatrogenic ureteral injury remains a possible and devastating complication associated with the procedure.2,3,4,5,6,7,8,9,10,11,12,13,14,15 The true incidence of unilateral ureteral ligation following OVH in cats is unknown and likely underreported, because the contralateral kidney is often able to compensate for the renal damage, so that clinical signs are not observed or are delayed or a diagnosis is avoided altogether.2,4,16,17 When clinical signs do occur, they are often vague and nonspecific, contributing to a delay in presentation and a proper diagnosis.5,10,18 Because azotemia is often not noted on routine blood work, an early diagnosis based on clinical suspicion and imaging studies is extremely important to minimize detrimental effects on renal blood flow and glomerular filtration rate, major systemic disease, and death.19,20 Most of the current literature focuses on unilateral ureteral injury because limited information currently exists on patients with bilateral injury, since acute decompensation in these patients likely results in a recommendation for euthanasia.

Although unilateral ureteral ligation without transection may not cause clinical signs and could go undiagnosed until identified incidentally later in the patient’s life, most cases of bilateral ureteral ligation with or without transection result in rapid clinical deterioration secondary to bilateral renal damage and life-threatening electrolyte abnormalities.2,10,16,21,22,23 Presenting clinical signs, physical examination and serum biochemical abnormalities, and results of diagnostic imaging are extremely important in quickly diagnosing this condition. A delay in surgical repair can cause tubulointerstitial damage resulting in tubulointerstitial fibrosis, tubular apoptosis, and irreversible chronic renal disease.16,19,20 Both cats described in the present report showed signs of systemic disease within 24 hours after surgery, and the owners reported nonspecific signs, including lethargy, inappetence, and vomiting, in the early postoperative period. In general, the presence of nonspecific clinical signs following OVH in an otherwise healthy young patient should generate suspicion as well as a prompt investigation for a potential cause. It is important to note that although clinical signs are generally nonspecific in cats with unilateral ureteral injury, both cats in the present report experienced bilateral injury and were anuric. This finding was also reported in a recent retrospective study10 on treatment and outcomes of ureteral injury following OVH in dogs and cats. In that study, 5 of 7 patients with complete bilateral ureteral obstruction were anuric and the other 2 were thought to be anuric, even though urine output was not mentioned in the patient history. Both patients in the present report had severe azotemia, which could support a diagnosis of bilateral ureteral injury or unilateral ureteral transection with subsequent urine leakage into the peritoneal cavity. The additional finding of anuria in these 2 cats was more suggestive of bilateral involvement. The degree of azotemia is also helpful in assessing the urgency of the situation.2,4,17

For patients with bilateral ureteral injury, diagnostic imaging including abdominal ultrasonography and contrast imaging such as intravenous urography, intravenous pyelography, and cystourethrography can be integral in confirming the presence of obstruction.24 In instances of ureteral transection, contrast imaging can identify the presence of peritoneal and retroperitoneal effusion and the location of urine leakage.10 For cat 1, following an initial diagnosis of uroabdomen by the referring veterinarian, retrograde contrast cystourethrography confirmed extravasation of contrast from a distal ureteral segment (side unknown) into the peritoneal cavity. Had the ureteral transection occurred more proximally, it is possible that a diagnosis would not have been obtained with this imaging method, because contrast material typically does not often travel very far up the ureters. For both cats, initial abdominal ultrasonography on arrival at MJR-VHUP identified both peritoneal (more extensive in cat 1 than cat 2) and retroperitoneal (more extensive in cat 2 than cat 1) effusion, mild to moderate bilateral pyelectasia, and proximal to mid ureteral dilation. For cat 2, both the left and right ureters could be traced to areas of hypoechoic tissue containing multiple hyperechoic foci, which were suspected to be the ovarian pedicles. For cat 1, excretory urography was additionally performed for surgical planning purposes and showed bilateral contrast extravasation at the level of the mid ureter. Cat 2 did not undergo any contrast imaging prior to surgical exploration. Given the recent history of OVH and ultrasonographic findings in both cats, it was unclear whether contrast imaging added a substantial amount of new information in these cases, and in the authors’ experience, the lesion is often evident during surgical exploration. However, contrast imaging could be helpful in identifying a second site of iatrogenic injury in isolated cases. In contrast, if ureteral injury occurred secondary to unknown trauma, contrast imaging can be beneficial in identifying the location of obstruction or leakage. Additionally, because some form of litigation may be involved in cases of iatrogenic injury following OVH, contrast imaging is often recommended.

Limited treatment options exist in the literature when bilateral ureteral injury has occurred following OVH. Reported treatment options include but are not limited to nephrostomy tube placement, ureteroneocystostomy, and placement of a subcutaneous ureteral bypass (SUB) device.23,25,26 In a previous report23 of a 2-year-old cat that had been obstructed for 5 days, temporary nephrostomy tubes were placed to stabilize the patient by allowing physiologic diuresis before definitive bilateral ureteroneocystostomy. In a second report,10 3 of 5 cats with bilateral injury had a SUB device placed at an initial surgery for stabilization, followed by ureteroneocystostomy and unilateral renal descensus (2 cats) 24 to 36 hours later. Subsequent SUB device removal was required in all 3 cats because of chronic urinary tract infections (2 cats) and obstruction (1 cat) associated with the device. A fourth cat had a ureteral stent placed on the left and a ureteroneocystostomy, cystonephropexy, and renal descensus performed on the right. Stent removal was required owing to the development of sterile cystitis and ureteral rupture over the stent. This patient also developed an obstruction at the ureteroneocystostomy site. Definitive bilateral SUB device placement was subsequently performed successfully. One cat had a good outcome, and 3 had an excellent outcome. The final cat experienced cardiopulmonary arrest at the time of anesthetic induction and died. Another case report21 described the use of bilateral SUB devices to treat a kitten that had bilateral ureteral ligation secondary to OVH. Three months after surgery, migration of the left SUB cystostomy catheter out of the bladder resulted in uroabdomen. At this time, normal urine flow through each ureter was noted via fluoroscopy, and so, both SUB devices were removed.

In the current report, bilateral ureteroneocystostomy with an intravesicular mucosal apposition technique in conjunction with bilateral renal descensus, bilateral nephropexy, and cystopexy (cat 1 only) was performed for definitive repair in both cats. A major advantage of ureteroneocystostomy is that it relies on the patient’s natural tissues, as opposed to a synthetic implant. Both intravesicular and extravesicular techniques have been described.1 Reported complications for the intravesicular and extravesicular techniques are similar and include extravasation of urine, bleeding, and stricture formation.27,28 The intravesicular technique typically results in a moderate amount of bladder swelling after eversion of the bladder mucosa, especially in cats. This has the potential to make suturing the ureteroneocystostomy site more challenging.28 The authors chose an intravesicular approach on the basis of their experience with the technique. From the authors’ experience, stricture at the surgical site is often identified within the first week following surgery. Cats 1 and 2 had follow-up abdominal ultrasonography 20 and 120 days, respectively, after surgery with no evidence of renal pelvic dilation or obstruction.

In cat 1, the left ureter was found to be transected at the level of the uterine stump, and the right ureter, which was circumcaval, was found to be transected midway between the kidney and bladder. Owing to the close anatomic relationship between the ureters and the uterine body in cats, the most common location for inadvertent ureteral trauma is at the level of the uterine body.2,4,23 In contrast, for cat 2, both ureters were found to be ligated and transected at the level of the ovarian pedicle. Although the literature suggests that ureteroneocystostomy should be reserved for lesions in the distal third of the ureter, in the authors’ experience this technique can be successfully performed for more proximal lesions, but often needs to be combined with tension-relieving techniques such as renal descensus and nephropexy, cystopexy, or cystonephropexy.1 For cat 2, approximately 3.0 cm of proximal ureter remained on the right and 1.5 to 2.0 cm remained on the left for repair following surgical debridement, and the right and left distal ureteral segments were still present. At the time of surgery, other repair options that were discussed included construction of a modified Boari flap and end-to-end ureteral anastomosis. Both of these techniques rely on the availability of natural tissues, require magnification, and necessitate an experienced surgeon who is familiar with microvascular surgery.2,6,29,30 The modification of the Boari flap would theoretically allow for bilateral repair because the ends of the ureters would be anastomosed end-to-side to a tubular bladder flap,30,31 as opposed to end-to-end as originally described by Boari for human patients. It was ultimately determined that surgical correction in both cats could be performed without the use of a Boari flap. Although end-to-end ureteral anastomosis is an option in conjunction with stent placement and has been performed successfully in cases of ureteral injury secondary to OVH in dogs,32 the small size of the cat ureter can make performing an end-to-end anastomosis difficult, particularly when attempting to place a stent in the non-dilated portion of the distal ureteral segment. Once healing has occurred, stent removal is recommended to prevent morbidity associated with the implant.32 It is worth mentioning that in general, cats do not tolerate ureteral stents well with self-limiting stranguria being a well reported complication.24

Because of the young age of both cats described in the present report, the use of a permanent implant such as a SUB device was not considered a suitable option. In the previous report10 describing 5 cats with bilateral ureteral injury, 3 of 5 cats had a SUB device placed at an initial surgery for stabilization, and all 3 cats subsequently required SUB device removal because of chronic urinary tract infections in 2 cats and device obstruction in a third cat. Other complications that have been reported include noninfectious cystitis, stranguria, pollakiuria, hematuria, kinking of the catheter tubing, obstruction of the nephrostomy catheter and port with debris, skin erosion and abscess formation over the implant ports, urinary tract infections, dislodgement, and urine extravasation.33,34 In the authors’ experience, long-term management of the device is required and includes periodic flushing up to every 3 months for the first year, and then every 3 to 6 months for the rest of the animal’s life. Additionally, serial biochemical evaluation and urine aerobic bacterial culture and susceptibility testing is performed every 3 to 9 months; all of this resulting in a substantial long-term financial commitment on the part of the owner.

The decision of whether to place a urinary catheter immediately following surgical correction of ureteral injury will largely be surgeon and case dependent. Because of the short segment of ureter present on the left side in cat 2, placement of a urinary catheter at the time of surgery was discussed. The benefits include quantifying urine output as well as decreasing the amount of backpressure placed on the surgical site as the bladder fills, which could result in urine leakage from a fresh surgical site. However, a small, empty bladder may result in more tension between the ureter and the bladder leading to dehiscence and leakage, and there was also concern for ascending infection resulting in a pyelonephritis. Ultimately, it was decided not to place a urinary catheter immediately postoperatively in cat 2. However, a urinary catheter was eventually placed approximately 24 hours after surgery because urine production had substantially decreased and a uroabdomen was suspected at this time. Urine leakage is a reported complication following ureteroneocystostomy and likely occurred in this case from intermittent tension on a fresh surgical site as the bladder emptied and filled.1 Although azotemia continued to improve over the next 48 hours following catheter placement and cystourethrography 72 hours after surgery revealed no leakage, a large volume of abdominal effusion recurred and appeared echogenic in character. Ninety-six hours after surgery, the cat became febrile and a new grade II to III/VI left systolic murmur was heard on auscultation. A sample of abdominal effusion was submitted for bacterial culture and came back positive for a multidrug resistant E faecium strain susceptible to linezolid, tigecycline, and vancomycin. Although the exact etiology of the infection was not known, it is possible that it was due to an ascending infection resulting in urosepsis. This is supported by the fact that the patient had a urinary catheter in place and also had diarrhea during this time. Echocardiography performed around this time revealed a possible vegetative lesion or clot associated with the tricuspid valve. Because the lesion was adjacent to the triple lumen catheter, the catheter was removed and the catheter tip was submitted for culture, which revealed no growth. However, cat 2 was receiving clindamycin and ceftazidime at this time. Blood cultures were discussed, but ultimately not pursued. Focal urinary ultrasonography revealed improved pyelectasia on the right with slightly progressive pyelectasia on the left with the presence of echogenic material within the renal pelvis. Because ureteral jets were present bilaterally, the pyelectasia was more suggestive of pyelenophritis than obstruction. Because the tricuspid valve lesion was no longer present at a follow-up examination 20 days after surgery, it was most likely a clot that had broken down over time. Twenty-four hours after the initiation of appropriate antimicrobial treatment, the cat was afebrile, and the azotemia had completely resolved. The patient continued to improve clinically and was discharged approximately 1 week after initiation of antimicrobial treatment. Oral treatment with linezolid was continued for approximately 4 weeks.

The ability to repair ureteral injury expediently directly correlates with the patient’s overall prognosis. In an experimental study where ureteral obstructions were studied in healthy dogs, the degree of ureteral pathology directly correlated with the duration of the obstruction.18 For cats 1 and 2 in the present report, definitive surgical repair was not performed for 3 and 4 days, respectively, following OVH. Glomerular filtration rate was not determined by means of renal scintigraphy for either cat in this report; however, this method as well as other methods for determining glomerular filtration rate remains questionable.35 Following surgical repair, serum creatinine concentrations were monitored to assess renal function. Serum creatinine decreased from 4.4 mg/dL initially to 0.5 mg/dL 1 day after surgery in cat 1. Serum creatinine went from too high to read initially to 6.7 mg/dL 1 day after surgery, and then to 1.7 mg/dL 4 days after surgery in cat 2.

To the authors’ knowledge, the present report represents the first description of surgical correction of bilateral ureteral trauma with bilateral ureteroneocystostomy in conjunction with bilateral renal descensus in 2 cats. In the authors’ experience, the use of an operating microscope as well as training in microvascular surgery is recommended to minimize potential complications with this procedure. This technique, although technically challenging, relies on the surrounding natural tissues for definitive repair and avoids long-term complications associated with the use of synthetic implants. Although both cats had a successful short-term outcome, despite the complications experienced by cat 2 while in the hospital, it is unclear how their long-term renal and overall health will be affected by this procedure. At the time of final follow-up approximately 1 year after surgery, both cats were doing well, according to their owners. Continued periodic monitoring will be critical in gaining more information on the overall long-term prognosis for this type of procedure. In conclusion, this surgical technique may provide a successful treatment option for cats with iatrogenic bilateral ureteral trauma that would otherwise have died or been euthanized.

Acknowledgments

The authors received no specific grant from any funding agency in the public, commercial, or not-for-profit sector in association with the cases described in this report. The authors declare that there were no conflicts of interest.

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  • Figure 1

    Lateral radiographic image obtained during retrograde contrast cystourethrography in a 6-month-old cat (cat 1) in which inadvertent bilateral ureteral ligation and transection had occurred during ovariohysterectomy. Notice the extravasation of contrast into the peritoneal cavity from a distal ureteral segment.

  • Figure 2

    Intraoperative photograph of cat 1 prior to surgical correction. The right ureter is circumcaval (top arrow) and has been transected midway between the kidney and bladder. A 5-mm region of necrotic tissue is evident (bottom arrow) at the distal end of the proximal portion of the right ureter.

  • Figure 3

    Intraoperative photograph of cat 1 following debridement of necrotic tissue and isolation of each ureter prior to ureteroneocystostomy. A—Proximal segment of the left ureter (arrow). Approximately 3 cm of normal ureter is present. B—Proximal segment of the right ureter after being brought under the vena cava so that it was no longer circumcaval (arrow). Approximately 4 cm of normal ureter is present.

  • Figure 4

    Intraoperative photograph of cat 1 following bilateral renal descensus and bilateral intravesicular ureteroneocystostomy. The left of the image is caudal, and the right of the image is cranial. Both ureters can be seen entering the apical region of the bladder, approximately 2 cm apart. Right nephropexy and cystopexy have been performed.

  • Figure 5

    Intraoperative photograph of a 7-month-old cat (cat 2) in which inadvertent bilateral ureteral ligation and transection had occurred during ovariohysterectomy. Bilateral renal descensus and bilateral intravesicular ureteroneocystostomy have been performed. The top of the image is cranial, and the bottom of the image is caudal. The left and right kidneys can be seen, along with their respective ureters inserting into the apical region of the bladder, approximately 2 cm apart.

  • 1.

    Aronson LR, Phillips H. Renal transplant. In: Tobias KM, Johnston SA, eds Veterinary Surgery: Small Animal. Vol 2. Elsevier; 2018:22632279.

    • Search Google Scholar
    • Export Citation
  • 2.

    Adin CA. Complications of ovariohysterectomy and orchiectomy in companion animals. Vet Clin North Am Small Anim Pract. 2011;41(5):10231039.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Ewers RS, Holt PE. Urological complications following ovariohysterectomy in a bitch. J Small Anim Pract. 1992;33(5):236238.

  • 4.

    Hamaide A. Surgery of the urinary bladder. In: Griffon D, Hamaide A, eds. Complications in Small Animal Surgery. Wiley Blackwell; 2016:492496.

    • Search Google Scholar
    • Export Citation
  • 5.

    Kerr WS. Effects of complete ureteral obstruction in dogs on kidney function. Am J Physiol. 1956;184:521526.

  • 6.

    Mehl ML, Kyles AE. Ureteroureterostomy after proximal ureteric injury during an ovariohysterectomy in a dog. Vet Rec. 2003;153(15):469470.

  • 7.

    Okkens AC, van de Gaag I, Biewenga WJ, Rothuizen J, Voorhout G. Urological complications following ovariohysterectomy in dogs. Article in Dutch. Tijdschr Diergeneeskd. 1981;106(23):11891198.

    • Search Google Scholar
    • Export Citation
  • 8.

    Pearson H. The complications of ovariohysterectomy in the bitch. J Small Anim Pract. 1973;14(5):257266.

  • 9.

    Pereira BM, Ogilvie MP, Gomez-Rodriguez JC, et al. A review of ureteral injuries after external trauma. Scand J Trauma Resusc Emerg Med. 2010;18(1):6.

  • 10.

    Plater BL, Lipscomb VJ. Treatment and outcomes of ureter injuries due to ovariohysterectomy complications in cats and dogs. J Small Anim Pract. 2020;61(3):170176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Rawlings CA, Bjorling DE, Christie BA. Kidneys. In: Slatter D, ed. Textbook of Small Animal Surgery. 3rd ed. WB Saunders Co; 2003:16061618.

    • Search Google Scholar
    • Export Citation
  • 12.

    Ruiz de Gopegui R, Espada Y, Majo N. Bilateral hydroureter and hydronephrosis in a nine-year-old female German Shepherd Dog. J Small Anim Pract. 1999;40(5):224226.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    van Goethem B, Schaefers-Okkens A, Kirpensteijn J. Making a rational choice between ovariectomy and ovariohysterectomy in the dog: a discussion of the benefits of either technique. Vet Surg. 2006;35(2):136143.

    • Crossref
    • Search Google Scholar
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