Complications and clinical utility of ultrasonographically guided pyelocentesis and antegrade pyelography in cats and dogs: 49 cases (2007–2015)

Nahvid M. Etedali 1Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104

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Jennifer A. Reetz 1Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104

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Jonathan D. Foster 1Department of Clinical Sciences and Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104

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Abstract

OBJECTIVE

To describe the diagnostic utility and clinical safety of ultrasonographically guided percutaneous pyelocentesis and antegrade pyelography in cats and dogs.

DESIGN

Retrospective case series.

ANIMALS

39 cats and 10 dogs with 55 affected kidneys.

PROCEDURES

Medical records were reviewed to identify cats and dogs that underwent ultrasonographically guided pyelocentesis and antegrade pyelography between June 1, 2007, and December 31, 2015. Data collected included procedure descriptions; results of diagnostic imaging, urine cytologic evaluation, and bacterial culture; and evidence of complications. Animals were assigned to the pyelocentesis group (underwent only pyelocentesis) or to the antegrade pyelography group (underwent pyelocentesis followed immediately by pyelography).

RESULTS

The diagnostic rate for pyelography was 94% (31/33; 95% confidence interval [CI], 80.4% to 98.9%). The total, minor, and major complication rates for both treatment groups combined were 25% (95% CI, 15.8% to 38.3%), 24% (95% CI, 14.4% to 36.3%), and 2% (95% CI, 0.09% to 9.6%), respectively. Performing bacterial culture of urine obtained by pyelocentesis did not provide an advantage over performing bacterial culture of urine obtained from the lower urinary tract.

CONCLUSIONS AND CLINICAL RELEVANCE

Findings indicated that ultrasonographically guided pyelocentesis and antegrade pyelography were well-tolerated techniques for investigating upper urinary tract disease in cats and dogs and that pyelography had a higher diagnostic rate than previously reported; therefore, pyelography should be considered for identification of mechanical and functional ureteral patency abnormalities in cats and dogs.

Abstract

OBJECTIVE

To describe the diagnostic utility and clinical safety of ultrasonographically guided percutaneous pyelocentesis and antegrade pyelography in cats and dogs.

DESIGN

Retrospective case series.

ANIMALS

39 cats and 10 dogs with 55 affected kidneys.

PROCEDURES

Medical records were reviewed to identify cats and dogs that underwent ultrasonographically guided pyelocentesis and antegrade pyelography between June 1, 2007, and December 31, 2015. Data collected included procedure descriptions; results of diagnostic imaging, urine cytologic evaluation, and bacterial culture; and evidence of complications. Animals were assigned to the pyelocentesis group (underwent only pyelocentesis) or to the antegrade pyelography group (underwent pyelocentesis followed immediately by pyelography).

RESULTS

The diagnostic rate for pyelography was 94% (31/33; 95% confidence interval [CI], 80.4% to 98.9%). The total, minor, and major complication rates for both treatment groups combined were 25% (95% CI, 15.8% to 38.3%), 24% (95% CI, 14.4% to 36.3%), and 2% (95% CI, 0.09% to 9.6%), respectively. Performing bacterial culture of urine obtained by pyelocentesis did not provide an advantage over performing bacterial culture of urine obtained from the lower urinary tract.

CONCLUSIONS AND CLINICAL RELEVANCE

Findings indicated that ultrasonographically guided pyelocentesis and antegrade pyelography were well-tolerated techniques for investigating upper urinary tract disease in cats and dogs and that pyelography had a higher diagnostic rate than previously reported; therefore, pyelography should be considered for identification of mechanical and functional ureteral patency abnormalities in cats and dogs.

Ureteral obstruction, whether from calculi or other factors, is a cause of acute kidney injury in veterinary patients, particularly in cats.1–5 In an 18-year multicenter study from 1984 to 2002, there was a roughly 30-fold increased incidence of ureteral urolithiasis in cats.5 However, it is unknown if this increased incidence is attributable to improved diagnostic imaging technologies to detect the condition, increased clinician awareness to look for it, or an actual increased incidence of the condition. Causes of ureteral obstruction include calculi, strictures, circumcaval ureters, neoplasia, mucus plugs, dried solidified blood stones, fibrosis, and surgical trauma.6–9 Further, ureteral obstruction can be diagnostically elusive when it is partial or caused by material that is not ultrasonographically obvious (eg, echogenic or acoustically shadowing). This is particularly important because there has been increased recognition of dried solidified blood stones and ureteral strictures as causes of ureteral obstruction in cats.8,9

Dilation of the renal pelvis is often one of the first detectable abnormalities suggestive of a potential ureteral obstruction. In a study10 evaluating the clinical relevance of ultrasonographically apparent renal pelvis dilation in cats and dogs, a renal pelvis width > 12.5 mm was always associated with ureteral obstruction. However, there are numerous causes (eg, pyelonephritis, increased diuresis or polyuria secondary to non-renal causes, renal insufficiency, and ureteral obstruction) that can result in pelvic dilation up to 12.5 mm.10

When ureteral obstruction is suspected, ultrasonographically guided percutaneous antegrade pyelography can provide excellent visualization of the affected renal pelvis and ureter, allowing for localization of an obstruction and identifying whether obstruction is complete or partial.1 For this procedure, ultrasonographic guidance is often used to perform pyelocentesis on the affected kidney whereby a needle is inserted into the renal pelvis, urine from the renal pelvis is drained, and iodinated contrast medium is then injected into the renal pelvis. Immediately afterward, diagnostic imaging (ie, radiography or fluoroscopy) is performed. Normally, the contrast medium should move down the ureter and into the urinary bladder immediately.11 Antegrade pyelography can be particularly useful when a ureteral obstruction is suspected to be caused by a factor other than urolithiasis (eg, obstruction by strictures). Furthermore, ultrasonographically guided percutaneous pyelocentesis provides an opportunity to collect urine directly from the renal pelvis for cytologic examination and bacterial culture, which may be useful because urine from the bladder may not be representative of urine from an obstructed kidney.

There is a paucity of scientific literature regarding the diagnostic value and associated risks and complications of pyelocentesis and pyelography in cats and dogs. In a study12 of 11 cats undergoing antegrade pyelography for suspected ureteral obstructions, images obtained for 8 of the 18 affected kidneys showed evidence of contrast leakage and, as a result, were nondiagnostic for 5 of the affected kidneys. Nonetheless, in that study,12 antegrade pyelography had 100% sensitivity and specificity for ureteral obstruction, and the anatomic location of obstruction was correctly identified on all of the diagnostic pyelograms. Another study,13 however, reported that 1 cat of a group of 2 dogs and 2 cats developed a ureteral obstruction from a blood clot following antegrade pyelography.

Because of the increased recognition of ureteral obstructions that during initial examinations are suspected not to be caused by calculi, use of ultrasonographically guided pyelocentesis and antegrade pyelography may serve an important role in the diagnosis of underlying causes of obstruction and the management of affected animals. Therefore, the objective of the study reported here was to describe the diagnostic utility and clinical safety of ultrasonographically guided percutaneous pyelocentesis and antegrade pyelography in cats and dogs.

Materials and Methods

Animals

The medical records from the University of Pennsylvania Matthew J. Ryan Veterinary Hospital were searched with the terms “pyelocentesis” and “pyelogram” to identify cats and dogs that underwent pyelocentesis or pyelography between June 1, 2007, and December 31, 2015. From the initial patient population identified, cats and dogs were included as cases if they had undergone ultrasonographically guided pyelocentesis alone or in combination with antegrade pyelography but were excluded if the procedures had been performed intraoperatively or under fluoroscopic guidance. Included animals were then assigned to the pyelocentesis group if they had undergone only pyelocentesis or to the antegrade pyelography group if they had undergone antegrade pyelography immediately following pyelocentesis.

Data collection

Data collected from medical records and diagnostic imaging reports included results of physical examination, biochemical analyses, and abdominal effusion analyses; identification of the kidney or kidneys treated (ie, right, left, both, or allograft); maximum diameter (median and range) of the renal pelvis as measured in the transverse plane during ultrasonography prior to treatment (pyelocentesis with or without antegrade pyelography); whether the patient underwent chemical restraint (sedation or general anesthesia) for treatment; needle size used for pyelocentesis and antegrade pyelography; duration of pyelographic study (from the time of injection of the contrast medium to the time the last pyelographic image was obtained); evidence of major or minor complications from the procedures; whether any concurrent procedures were performed (yes or no); and results of cytologic examination and bacterial culture performed on urine obtained by pyelocentesis. Results of bacterial culture performed on urine obtained by cystocentesis or urinary bladder catheterization were included when the procedures were performed within 72 hours before or after the pyelocentesis.

Uroabdomen

Uroabdomen was diagnosed on the basis of abnormalities detected on physical examination and clinicopathologic analyses as previously described.14 Physical examination abnormalities could include tachycardia, bradycardia, abdominal pain, bruising of the peritoneal or inguinal skin, or a palpable fluid wave in the abdomen. Definitive diagnosis of uroabdomen was made by comparing patient abdominal effusion potassium and creatinine concentrations with concurrent serum potassium and creatinine concentrations. An abdominal effusion with a creatinine concentration ≥ 2 times the serum creatinine concentration was considered diagnostic for uroabdomen. An abdominal effusion with a creatinine concentration between 1 and 2 times the serum creatinine concentration or with a potassium concentration greater than the serum potassium concentration was considered suggestive of, but not diagnostic for, uroabdomen. Uroabdomen in this latter scenario was confirmed during exploratory laparotomy or necropsy by identification of a source of urine leakage.

Antegrade pyelography

All pyelograms were reviewed by a board-certified radiologist (JAR). Results of pyelographic studies were considered diagnostic if they indicated a condition that could be classified into 1 of 4 diagnostic categories: clinically normal, complete obstruction, partial mechanical obstruction, or functional (nonmechanical) obstruction. Results of pyelographic studies were considered nondiagnostic if they were deemed inconclusive by the radiologist. A pyelographic study was considered clinically normal if contrast medium was evident in the ureter and bladder immediately after injection of the contrast medium into the renal pelvis, the ureteral diameter was subjectively normal (ie, diameter ≤ approx 1 mm), and progressive emptying of the renal pelvis was evident in subsequent pyelographic images. Given that an injection of contrast medium into the renal pelvis would have presumably created some degree of pelvic distention and that the patients undergoing pyelography had some degree of distention noted on ultrasonographic examination prior to pyelography, subjective interpretation of renal pelvis distention was not considered alone in distinguishing clinically normal from abnormal pyelography results. A complete obstruction was defined as pyelographic evidence of renal pelvic and segmental ureteral dilation (with or without ureteral tortuosity) to the point of a contrast filling defect or to an abrupt termination of the contrast medium in the ureter suggestive of ureteral stricture, combined with a complete lack of contrast medium distal (in the ureter or bladder) to the point of obstruction over the course of the pyelography procedure. A partial obstruction was defined as pyelographic evidence of renal pelvic and segmental ureteral dilation (with or without ureteral tortuosity) to the point of a contrast filling defect or to an abrupt decrease in ureteral diameter suggestive of ureteral stricture combined with a delayed transit of contrast medium into the urinary bladder. A functional (nonmechanical) obstruction was defined as pyelographic evidence of renal pelvic and ureteral dilation, segmental or diffuse ureteral tortuosity without an abrupt change in ureteral diameter, immediate presence of contrast medium in the urinary bladder, and a subjective delay in renal pelvic or ureteral emptying indicated by persistent renal pelvic and ureteral dilation on subsequent pyelographic images.

Complications

Minor complications were defined as any complication (eg, mild contrast medium leakage, renal subcapsular contrast accumulation, or retroperitoneal contrast accumulation) that did not require specific treatment (eg, surgery or blood transfusion) and did not pose a substantial risk to the patient. Major complications were defined as any complication that required surgical intervention or that placed a patient's health at substantial risk (eg, uroabdomen or uroretroperitoneum, severe hemorrhage, subsequent ureteral obstruction, or death).

Statistical analysis

The total complication rate was calculated as the number of complications divided by the number of affected kidneys treated. Similarly, the major and minor complication rates for each of the treatment groups were calculated as the number of respective complications in each group divided by the number of kidneys treated in each group. The 95% CI for each rate was calculated with the Wilson method. Statistical analysis was performed with available software.a

Results

Animals

Search of the medical records identified 157 radiographic reports for 106 individual cats and dogs. Of these, 57 cats and dogs were excluded because they did not undergo ultrasonographically guided pyelography or pyelocentesis or because procedures were performed intraoperatively or with fluoroscopic guidance. Overall, the final population in the study consisted of 49 animals (39 cats and 10 dogs) and 55 treated kidneys, including 5 renal allografts in cats.

Breeds reported for the 39 cats included 32 domestic shorthair cats, 2 domestic longhair cats, and 1 each of Abyssinian, Birman, Maine Coon, Russian Blue, and Siamese. The median age for cats was 10.25 years (range, 0.5 to 18 years), and there were 23 castrated males and 16 spayed females. The 10 dogs included 1 each of Australian Shepherd, Bernese Mountain Dog, Bichon Frise, Border Collie, Dachshund, Golden Retriever, Labrador Retriever, mixed-breed dog, Old English Sheepdog, and Shih Tzu. The median age for dogs was 8.5 years (range, 0.58 to 15.2 years), and there were 5 castrated males, 3 spayed females, and 2 sexually intact females.

Pyelocentesis and antegrade pyelography groups and procedures

Twenty-two cats and dogs with 22 treated kidneys were assigned to the pyelocentesis group, and 28 cats and dogs with 33 treated kidneys (including 5 animals that underwent bilateral pyelography) were assigned to the antegrade pyelography group. One animal was categorized in both groups because pyelocentesis was performed on 1 kidney, and pyelocentesis combined with pyelography was performed on the other. Of the 55 treated kidneys, 20 were right kidneys, 30 were left kidneys, and 5 were renal allografts. Forty-three patients had unilateral procedures, and 6 had bilateral procedures.

The needle gauge used for the procedure was reported for 25 of the 49 cats and dogs. A 22-gauge needle was used in all animals except for 1 dog (a Golden Retriever) in which an 18-gauge needle was used. The recorded magnitude of renal pelvic dilation was available for 52 of 55 kidneys. In the pyelocentesis group, the median maximum renal pelvic diameter was 6.0 mm (range, 4 to 12 mm) for cats and 6.0 mm (range, 2.2 to 37 mm) for dogs. In the antegrade pyelography group, the median renal pelvic diameter was 10.5 mm (range, 2 to 34 mm) for cats and 19.5 mm (range, 17 to 22 mm) for dogs. Of the kidneys from which urine volume removed from the renal pelvis was quantified (pyelocentesis group, n = 10; antegrade pyelography group, 25), the median volumes were 2.0 mL (range, 0.3 to 4.0 mL) and 6.2 mL (range, 0.8 to 55.0 mL), respectively, for cats and dogs in the pyelocentesis group and were 2.3 mL (range, 0.3 to 16.0 mL) and 6.0 mL (range, 5.0 to 7.0 mL), respectively, for cats and dogs in the antegrade pyelography group. In the antegrade pyelography group, the contrast medium used was iohexol (240 or 350 mg of iodine/mL) in all animals, except 1 cat in which diatrizoate meglumine (240 mg of iodine/mL) was used instead. The median volumes of contrast medium were 1.7 mL (range, 0.35 to 6.0 mL) and 4.5 mL (range 4.0 to 5.0 mL) in cats and dogs, respectively. At the discretion of the radiologist performing the procedure, the volume of contrast medium injected ranged from 50% to 100% of the volume of urine removed during pyelocentesis.

For the pyelocentesis group, 18 procedures were performed with the animal sedated and 4 were performed with the animal undergoing general anesthesia. Concurrent procedures were performed in 11 patients in the pyelocentesis group and included fine-needle aspiration of intra-abdominal lesions (n = 7), renal biopsy (2 [1 of which was immediately followed by laparoscopic-assisted ovariohysterectomy and gastropexy]), cardiac pacemaker placement (1), and central venous catheter placement (1). For the antegrade pyelography group, 6 pyelographic studies were performed with the animal sedated and 20 were performed with the animal undergoing general anesthesia. Sedation and anesthesia data were unavailable from the medical records for 2 animals. Concurrent procedures were performed in 14 patients in the antegrade pyelography group and included abdominal surgeries (n = 7), esophagostomy tube placement (4 [2 of which were performed with concurrent abdominal surgery]), fine-needle aspiration of intra-abdominal lesions (3), colonoscopy (1), and central venous catheter placement (1).

Complications

For the 55 kidneys treated, a total of 14 complications were identified, of which 13 were considered minor and 1 was considered major. The total, minor, and major complication rates for the 2 treatment groups combined were 25% (14/55; 95% CI, 15.8% to 38.3%), 24% (13/55; 95% CI, 14.4% to 36.3%), and 2% (1/55; 95% CI, 0.09% to 9.6%), respectively.

In the pyelocentesis group, there were no major complications, but 4 of the 22 (18%) procedures involved minor complications, such as mild perirenal hemorrhage and self-limiting hemorrhage into the renal pelvis following the procedure. The total, minor, and major complication rates for the pyelocentesis group were 18% (4/22; 95% CI, 7.3% to 38.5%), 18% (4/22; 95% CI, 7.3% to 38.5%), and 0% (0/22; 95% CI, 0.0% to 14.9%), respectively.

In the antegrade pyelography group, 9 of the 33 (27%) procedures involved minor complications (mild to moderate fluid or contrast leakage [n = 5], subcapsular injection or fluid leakage [3], and accidental contrast injection into the retroperitoneal space [1]), and 1 (3%) procedure on a cat involved a major complication. This cat had leakage of contrast medium into the subcapsular and retroperitoneal regions during injection and continued leakage of contrast medium from the renal pelvis with accumulation of fluid in the retroperitoneal region after the injection. The pyelogram was suggestive for ureteral obstruction in this patient, with potential rupture of the renal parenchyma; therefore, exploratory laparotomy was performed. The leak, along with renal hemorrhage and a blood clot at the contrast medium injection site, was confirmed during surgery. However, a separate portion of the renal parenchyma of the affected kidney in this cat was identified as necrotic and ruptured and was considered to have been the source of leakage, likely unrelated to the pyelocentesis and pyelography. Therefore, it was unclear whether this was truly a complication of the procedure or a consequence of the underlying pathological process related to the ureteral obstruction. The total, minor, and major complication rates for the antegrade pyelography group were 30% (10/33; 95% CI, 17.4% to 47.3%), 27% (9/33; 95% CI, 15.1% to 44.2%), and 3% (1/33; 95% CI, 0.16% to 15.3%), respectively.

Diagnostic utility

Thirty-one of the 33 (94%) pyelographic studies were diagnostic for complete obstruction (n = 14 [42%]; Figure 1), partial obstruction (9 [27%]; Figure 2), or functional obstruction (7 [21%]; Figure 3) or were clinically normal (1 [3%]; Figure 4); however, the results of 2 (6%) pyelographic studies were inconclusive. Thus, the overall diagnostic rate for ultrasonographically guided antegrade pyelography was 94% (31/33; 95% CI, 80.4% to 98.9%).

Figure 1—
Figure 1—

Pyelographic image (left lateral radiographic view) taken almost immediately after contrast medium was injected into the renal pelvis of the left kidney of an 8-year-old 3.3-kg (7.3-lb) spayed female Abyssinian cat with complete ureteral obstruction secondary to a ureteral calculus. Contrast medium is evident in the dilated renal pelvis (arrow) and in the ureteral lumen, which is segmentally dilated and slightly tortuous until the level of L6-L7, at which point there is abrupt termination of the contrast medium combined with a small contrast-filling defect (asterisk). Contrast medium was not evident distal to this point on subsequent pyelographic images obtained up to 45 minutes after contrast medium was injected. This cat also had pyelography performed on the right kidney, and a small amount of perirenal leakage of contrast medium (arrowhead) is evident.

Citation: Journal of the American Veterinary Medical Association 254, 7; 10.2460/javma.254.7.826

Figure 2—
Figure 2—

Pyelographic images (right lateral radiographic views) taken almost immediately (A) and 10 minutes after (B) contrast medium was injected into the renal pelvis of a 10-year-old 3.8-kg (8.4-lb) castrated male domestic shorthair cat with partial obstruction of the ureter of a renal allograft secondary to multiple periureteral adhesions. A—Contrast medium is evident in the dilated renal pelvis (arrow) and the lumen of the segmentally dilated and tortuous ureter (asterisk), with only a small amount of contrast medium evident in the urinary bladder (arrowhead). B—More contrast medium has passed from the renal pelvis, through the ureter, and into the urinary bladder, evident by the increased amount of contrast medium in the bladder, compared with the earlier image. However, the renal pelvic and proximal ureteral dilation persist.

Citation: Journal of the American Veterinary Medical Association 254, 7; 10.2460/javma.254.7.826

Figure 3—
Figure 3—

Pyelographic images (left lateral radiographic views) taken almost immediately after injection of contrast medium into the renal pelvis of the left kidney (A) and right kidney (B) in a 4-year-old 6.3-kg (13.9-lb) castrated male domestic shorthair cat with bilateral functional (nonmechanical) obstruction of its ureters, the cause for which was later presumptively diagnosed as inflammatory ureteritis. On each side, the renal pelvis (right, black arrow; left, white arrow) is dilated and the ureter (right, black asterisk; left, white asterisk) is diffusely dilated and tortuous, with a stream of contrast medium entering the bladder (arrowhead). A—The focal areas where minimal to no contrast is seen in the ureter were caused by ureteral peristalsis because subsequent images showed ureteral dilation in these areas. B—Contrast medium from pyelography performed on the contralateral side (with injection 22 minutes before this image was obtained) is still evident in the left renal pelvis (white arrow) and ureter (white asterisk).

Citation: Journal of the American Veterinary Medical Association 254, 7; 10.2460/javma.254.7.826

Figure 4—
Figure 4—

Pyelographic images (right lateral [A] and oblique ventrodorsal [B] radiographic views) of the same cat in Figure 1 after pyelography was performed on the right kidney, the results of which were considered normal. However, pyelographic features of the left renal pelvis (white arrow) and segmental ureteral dilation (white asterisks) remain unchanged compared with Figure 1. A—Image was obtained immediately after contrast medium was injected into the right kidney and 34 minutes after contrast medium was injected into the left kidney. Note that the right kidney has mild pelvic dilation (black arrow), and the right ureter (black asterisks) has a relatively normal and uniform diameter throughout its course along with a stream of contrast medium evident entering the bladder (arrowhead). B—Image obtained 8 minutes after injection of contrast medium into the pelvis of the right kidney and 42 minutes after contrast medium was injected into the pelvis of the left kidney. Almost all contrast medium has emptied from the right renal pelvis (black arrow), and contrast is no longer evident in the right ureter.

Citation: Journal of the American Veterinary Medical Association 254, 7; 10.2460/javma.254.7.826

For the 30 obstructed kidneys, additional pyelographic images were obtained after injection of contrast medium into the animal's renal pelvis, and mean duration from the time of injection to the time of acquisition of the final pyelographic image was 17.4 minutes (median, 15 minutes; range, 2 to 47 minutes); yet, none depicted complete or near complete emptying of contrast medium from the affected renal pelvis and ureter over the course of the pyelographic study. However, for the single pyelographic study that was considered clinically normal, images were obtained for 13 minutes following injection of contrast medium and depicted progressive, nearly complete emptying of contrast medium from the renal pelvis and ureteral lumen (Figure 4).

The 2 inconclusive pyelographic studies could not be interpreted because of poor filling of the renal pelvis and ureter with contrast medium and because of leakage of contrast medium. One of the inconclusive pyelographic studies involved an inadequate volume of contrast medium injected into the renal pelvis and concurrent contrast medium leakage. The other inconclusive study had radiographic evidence of marked leakage of contrast medium from the pyelocentesis site but no contrast medium entering the ureter. Because this second animal had ultrasonographically evident mild ureteral distention, an obstruction at the ureteropelvic junction was considered unlikely, and the pyelographic study was deemed nondiagnostic.

Cytologic examination of urine

Cytologic examination, including urine sediment analysis, was performed on urine samples collected by pyelocentesis from 19 kidneys in 18 animals (16 cats and 2 dogs). None of the results provided information that influenced case management or helped obtain a diagnosis. Results for 4 of the 19 (21%) urine samples provided evidence of inflammation or infection (moderate number of cocci present [n = 1], histiocytic inflammation with hemophagocytosis [1], chronic neutrophilic inflammation [1], and mild mixed histiocytic and neutrophilic inflammation [1]). The remaining 15 urine samples were nondiagnostic or hemodilute, had an inactive sediment, or contained incidental abnormalities (eg, crystalluria).

Bacterial culture results

Bacterial culture results (2 positive and 46 negative) were available for 48 of the 55 renal pelvis urine samples collected. For the remaining 7 renal pelvis urine samples, bacterial culture was not performed (n = 3), the medical records did not indicate results (2), or the quantity of urine obtained was insufficient for bacterial culturing (2). Each of the 2 positive urine culture results was for a separate cat: one from which Escherichia coli was isolated, and the other from which Staphylococcus epidermidis was isolated. Of the 46 renal pelvis urine samples that did not yield growth on bacterial culture, 25 (54%) were from animals that had previously received ≥ 1 dose of an antimicrobial.

Concurrent bacterial culture was performed on urine samples obtained from the renal pelvis by pyelocentesis and from the urinary bladder by cystocentesis or catheterization within 72 hours of pyelocentesis for 25 animals (pyelocentesis group, n = 11; antegrade pyelography group, 14) but not for 22 animals (pyelocentesis group, 8; antegrade pyelography group, 14). Information regarding bacterial culture was not available from the medical records for 2 animals (pyelocentesis group, 0; antegrade pyelography group, 2). Of the 25 concurrent bacterial cultures performed, 2 (8%) urine samples from bladders yielded positive results (E coli), and in only 1 of these animals was the same isolate cultured from urine obtained from the patient's renal pelvis. The other positive bacterial culture result on urine obtained from the bladder was for an animal that had negative results on urine obtained by pyelocentesis the day following cystocentesis and initiation of antimicrobial treatment. In addition, 2 of the 25 patients with concurrent bacterial cultures underwent cystocentesis within 48 hours after receiving contrast medium for pyelography. Both of these patients had negative results on bacterial culture; however, it was unknown whether the contrast medium affected these results. Further, 5 animals with negative results on bacterial culture had received antimicrobial treatment before urine collection, and 4 of the 5 were receiving antimicrobials at the time of pyelocentesis. No animals had the combination of positive results for bacterial culture of urine from the renal pelvis and negative results for bacterial culture of urine from the bladder. The single cat from which S epidermidis was cultured from a renal pelvis sample of urine did not have a concurrent bacterial culture performed on urine from the bladder.

For the urine samples obtained by pyelocentesis from the 30 kidneys with complete, partial, or functional obstructions, none had positive results on bacterial culture (negative bacterial culture results [n = 25, including samples from 18 patients treated with antimicrobials at the time of sample collection], bacterial culture not performed [3], or information regarding bacterial culture unavailable from the medical record [2]). Twelve of the animals with obstructions had concurrent bacterial cultures performed on urine obtained from the bladder within 72 hours, and results for all 12 concurrent samples were negative. Only 2 of these 12 animals had received antimicrobials before their urine was sampled.

Discussion

Results suggested that ultrasonographically guided percutaneous pyelocentesis and antegrade pyelography were well-tolerated procedures with low complication rates in cats and dogs of the present study. Although diagnostic insight was not provided by results of cytologic examination or bacterial culture performed on urine obtained by pyelocentesis, antegrade pyelography was a useful diagnostic procedure and had a higher diagnostic rate (94%) in the present study than has been previously reported (72%).12

Antegrade pyelography has previously been reported to have a 44% complication rate,12 whereas the present study had a total complication rate of 30% (27% minor and 3% major complications) for the procedure. The lower total complication rate observed in the present study was not likely related to needle size because a 22-gauge needle was used in all but 1 animal, whereas 25-gauge needles were used in all 11 cats of a previous retrospective study.12 It was possible that the longer length of 22-gauge needles, compared with 25-gauge needles, made appropriate needle placement easier to achieve. Furthermore, the lower complication rate observed in the present study could not have been attributed to increased patient immobilization because 6 of 28 patients in the present study underwent pyelography with sedation alone, whereas pyelography in the previous study12 was performed with all animals undergoing general anesthesia. Similar to previously reported findings,1 there has been a subjective increase in the incidence of ureteral obstruction, particularly in cats, at the authors’ institution, and performing pyelocentesis and antegrade pyelography has become more common at the authors’ institution; therefore, increased operator comfort and proficiency with performing the procedures could have contributed to the lower complication rate in the present study.

In a previous study,12 antegrade pyelography was diagnostic for ureteral obstruction in 13 of 18 pyelographic studies; however, the procedure was nondiagnostic when contrast medium leaked. In the present study, 31 of 33 (94%) pyelographic studies were diagnostic. Although complete (14/33 [42%]) or partial (9/33 [27%]) obstructions were diagnosed most often, a subset of animals (7/33 [21%]) did not have evidence of complete or partial obstruction but had contrast medium retention in the dilated renal pelvis, diffuse ureteral dilation, and ureteral tortuosity. Therefore, functional obstruction was diagnosed in these 7 animals because they had movement of contrast medium into their urinary bladders as expected11 and did not have any focal areas of ureteral narrowing suggestive of a mechanical obstruction to urine flow. It was unknown whether their functional obstructions were caused by scant intraluminal debris, impaired ureteral peristalsis (eg, secondary to ureteritis), an unidentified ureteral stricture, or other unknown causes.

In humans, ureteral dilation with no apparent source of mechanical obstruction is associated with urinary tract infections15,16 and is thought to be caused by decreased ureteral peristalsis secondary to ureteral inflammation. Although the prevalence of documented urinary tract infection was low in the present study, such infection could have been an underlying cause for decreased ureteral peristalsis because many of the animals with negative results on bacterial culture had been given antimicrobial treatment before urine samples were collected for bacterial culture. Alternatively, noninfectious ureteritis of unknown causes could have been present in these animals. In humans, genitourinary complications occur in 4% to 23% of patients with inflammatory bowel disease, secondary to either metabolic derangements or extension of inflammatory disease to the urinary tract (ie, periureteral fibrosis).17 The 3 most commonly encountered urinary complications in humans are urinary tract calculi, ureteral obstruction, and vesical fistulas.17 Interestingly, the 5 animals in the present study with functional (not mechanical) obstructions were all cats. Given that inflammatory bowel disease is common in cats, follow-up studies are warranted to investigate the potential relationship between gastrointestinal disease and urinary tract disease, particularly functional ureteral obstruction, in cats.

The delay in renal pelvic and ureteral emptying of contrast medium noted in the present study was not likely from insufficient volume of contrast medium because all patients with diagnostic studies had obvious and substantial contrast medium accumulation in the renal pelvis evident on pyelographic images. Further, animals not affected by complete blockage had contrast medium documented to have reached their urinary bladder. However, 2 of the 33 (6%) pyelography procedures performed in the present study were inconclusive owing to poor filling of the renal pelvis and ureter with contrast medium and leakage of contrast medium that prevented definitive interpretation of the particular pyelographic studies.

Regardless of whether an obstruction is partial versus complete or mechanical versus functional, the result is inappropriate accumulation of urine in the ipsilateral renal pelvis and ureter. Ureteral obstruction and subsequent increased renal pelvic hydrostatic pressure can result in the worsening of renal function because of damage to the renal parenchyma. Further, the longer an obstruction is present, the lower the likelihood there is for renal recovery.18 In 2 retrospective studies,6,19 cats that underwent interventional treatment for ureteral obstruction had at the time of last follow-up a median serum creatinine concentration of 2.6 mg/dL, consistent with stage 2 chronic kidney disease. Further highlighting the importance of maximizing chances of renal recovery in affected animals, a recent study3 evaluating outcomes of ureteral surgery and stenting in cats shows that 25 of 87 (29%) cats for which follow-up data were available died of progressive chronic kidney disease. Therefore, it is imperative that ureteral obstruction remain a differential diagnosis for animals with acute kidney injury and renal pelvic dilation, and antegrade pyelography is an important tool for investigating ureteral obstruction when a stricture or intraluminal obstructive lesion is not readily identified.

The diagnosis of ureteral obstruction is not always straightforward because some cats lack clinically substantial pelvic or ureteral dilation. One study10 shows that the maximum renal pelvic width with obstructive urinary disease may be as low as 1.2 mm for cats and 5.1 mm for dogs and that a maximum pelvic width ≥ 12.5 mm was only associated with obstructive disease. Another study5 shows that dilation of the renal pelvis, ureter, or both is equivocal or absent in 12 of 155 (8%) cats evaluated for ureteral calculi. A more recent reportb in cats with confirmed ureteral obstruction shows that the median renal pelvic height on a transverse ultrasonographic image is 6.9 mm (range, 0 to 37 mm), with 11 of 45 (24%) renal pelvic heights ≤ 4 mm and 2 (4%) < 2 mm, and that the median intraluminal ureteral diameter is 3.2 mm (range, 0 to 11 mm), with 12 of 45 (27%) ureters having intraluminal diameters < 2 mm. Compared with antegrade pyelography as a gold standard for diagnosing ureteral obstruction, when a 7.0-mm renal pelvic diameter is used as a criterion for renal dilation and ureteral obstruction in cats, routine ultrasonography has a diagnostic sensitivity and specificity of 68% and 67%, respectively,c which are less than that for antegrade pyelography.12

Results of the present study indicated that performing pyelocentesis to obtain urine for cytologic examination and bacterial culture did not provide clinically useful information; however, this could have been because many of the animals received antimicrobial treatment prior to pyelocentesis. In addition, none of the animals with a ureteral obstruction had positive results on bacterial culture performed on urine obtained from the renal pelvis or the urinary bladder. This finding conflicted with previous studies showing that 8% to 33% of cats1,20 and 77% of dogs21 with ureteral obstruction have had urinary tract infections.

The present study was not without limitations. Owing to the retrospective nature of the study, it was not possible to standardize the techniques for pyelocentesis and pyelography or the methods used to screen for complications. Another limitation was the inability to control when antimicrobial treatments were started relative to collection of urine samples. For instance, many patients in the present study had pyelocentesis and pyelography performed following abdominal ultrasonography, cystocentesis, and initiation of antimicrobial treatment. Therefore, many of the urine samples obtained by pyelocentesis were collected after affected animals had received ≥ 1 dose of antimicrobials, which could have caused false-negative results for bacterial cultures performed on urine samples obtained by pyelocentesis. Because of this, it was possible that the present study could have underestimated the percentage of animals that had positive results for bacterial culture on urine obtained from the renal pelvis and negative results on urine from the urinary bladder. Finally, incomplete medical records made it difficult to assess bacterial culture results and methods of chemical restraint (sedation vs general anesthesia) for some animals in the present study.

Results of the present study indicated that ultrasonographically guided percutaneous pyelocentesis and antegrade pyelography were well-tolerated techniques for use in investigating upper urinary tract disease, regardless of the degree of pyelectasia. Findings also suggested that ultrasonographically guided antegrade pyelography had a high diagnostic rate for identifying complete, partial, and functional ureteral obstructions and should be considered a valuable tool for identifying mechanical and functional ureteral patency abnormalities. Further studies are needed to evaluate the impact of subclinical functional obstructions and partial obstructions on kidneys (eg, renal injury and renal function) of animals. Furthermore, studies are warranted to investigate the potential relationship of gastrointestinal disease with ureteral obstruction in cats. Finally, further prospective studies should be performed to evaluate sample site, timing, and testing of urine from affected animals because results of the present study suggested that, even for animals with ureteral obstruction, performing bacterial culture on urine obtained by pyelocentesis did not provide an advantage, compared with performing bacterial culture on urine obtained from the bladder, and that results of bacterial cultures performed on urine from the bladder appeared to have been representative of bacterial culture results for urine from the renal pelvis.

Acknowledgments

Presented in abstract form at International Renal Interest Society (IRIS) Renal Week, Davis, Calif, March 2016.

ABBREVIATIONS

CI

Confidence interval

Footnotes

a.

Prism Mac, version 7.0d, GraphPad Software Inc, La Jolla, Calif.

b.

Anne-Archard N, Dunn M, d'Anjou MA. Sonographic features of ureteral obstruction in cats (abstr), in Proceedings. Am Coll Vet Radiol Annu Sci Meet 2016;92.

c.

Lamb CR, Cortellini S. Ultrasonography in the diagnosis and management of cats with azotemia (abstr), in Proceedings. Am Coll Vet Radiol Annu Sci Meet 2016;91.

References

  • 1. Berent AC. Ureteral obstructions in dogs and cats: a review of traditional and new interventional diagnostic and therapeutic options. J Vet Emerg Crit Care (San Antonio) 2011;21:86103.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Livet V, Pillard P, Goy-Thollot I, et al. Placement of subcutaneous ureteral bypasses without fluoroscopic guidance in cats with ureteral obstruction: 19 cases (2014–2016). J Feline Med Surg 2017;19:10301039.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Wormser C, Clarke DL, Aronson LR. Outcomes of ureteral surgery and ureteral stenting in cats: 117 cases (2006–2014). J Am Vet Med Assoc 2016;248:518525.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Hardie EM, Kyles AE. Management of ureteral obstruction. Vet Clin North Am Small Anim Pract 2004;34:9891010.

  • 5. Kyles AE, Hardie EM, Wooden BG, et al. Clinical, clinicopathologic, radiographic, and ultrasonographic abnormalities in cats with ureteral calculi: 163 cases (1984–2002). J Am Vet Med Assoc 2005;226:932936.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Horowitz C, Berent A, Weisse C, et al. Predictors of outcome for cats with ureteral obstructions after interventional management using ureteral stents or a subcutaneous ureteral bypass device. J Feline Med Surg 2013;15:10521062.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Steinhaus J, Berent AC, Weisse C, et al. Clinical presentation and outcome of cats with circumcaval ureters associated with a ureteral obstruction. J Vet Intern Med 2015;29:6370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Westropp JL, Ruby AL, Bailiff NL, et al. Dried solidified blood calculi in the urinary tract of cats. J Vet Intern Med 2006;20:828834.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Zaid MS, Berent AC, Weisse C, et al. Feline ureteral strictures: 10 cases (2007–2009). J Vet Intern Med 2011;25:222229.

  • 10. D'Anjou MA, Bédard A, Dunn ME. Clinical significance of renal pelvic dilatation on ultrasound in dogs and cats. Vet Radiol Ultrasound 2011;52:8894.

    • Search Google Scholar
    • Export Citation
  • 11. Shipov A, Segev G. Ureteral obstruction in dogs and cats. Isr J Vet Med 2013;68:7177.

  • 12. Adin CA, Herrgesell EJ, Nyland TG, et al. Antegrade pyelography for suspected ureteral obstruction in cats: 11 cases (1995–2001). J Am Vet Med Assoc 2003;222:15761581.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Rivers BJ, Walter PA, Polzin DJ. Ultrasonographic-guided, percutaneous antegrade pyelography: technique and clinical application in the dog and cat. J Am Anim Hosp Assoc 1997;33:6168.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Stafford JR, Bartges JW. A clinical review of pathophysiology, diagnosis, and treatment of uroabdomen in the dog and cat. J Vet Emerg Crit Care (San Antonio) 2013;23:216229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Zelenko N, Coll D, Rosenfeld AT, et al. Normal ureter size on unenhanced helical CT. AJR Am J Roentgenol 2004;182:10391041.

  • 16. Rathi V, Agrawal S, Bhatt S, et al. Ureteral dilatation with no apparent cause on intravenous urography: normal or abnormal? A pilot study. Adv Urol 2015;2015:681836.

    • Search Google Scholar
    • Export Citation
  • 17. Banner MP. Genitourinary complications of inflammatory bowel disease. Radiol Clin North Am 1987;25:199209.

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

  • 19. Berent AC, Weisse CW, Todd K, et al. Technical and clinical outcomes of ureteral stenting in cats with benign ureteral obstruction: 69 cases (2006–2010). J Am Vet Med Assoc 2014;244:559576.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Kyles AE, Hardie EM, Wooden BG, et al. Management and outcome of cats with ureteral calculi: 153 cases (1984–2002). J Am Vet Med Assoc 2005;226:937944.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Snyder DM, Steffey MA, Mehler SJ, et al. Diagnosis and surgical management of ureteral calculi in dogs: 16 cases (1990–2003). N Z Vet J 2005;53:1925.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Figure 1—

    Pyelographic image (left lateral radiographic view) taken almost immediately after contrast medium was injected into the renal pelvis of the left kidney of an 8-year-old 3.3-kg (7.3-lb) spayed female Abyssinian cat with complete ureteral obstruction secondary to a ureteral calculus. Contrast medium is evident in the dilated renal pelvis (arrow) and in the ureteral lumen, which is segmentally dilated and slightly tortuous until the level of L6-L7, at which point there is abrupt termination of the contrast medium combined with a small contrast-filling defect (asterisk). Contrast medium was not evident distal to this point on subsequent pyelographic images obtained up to 45 minutes after contrast medium was injected. This cat also had pyelography performed on the right kidney, and a small amount of perirenal leakage of contrast medium (arrowhead) is evident.

  • Figure 2—

    Pyelographic images (right lateral radiographic views) taken almost immediately (A) and 10 minutes after (B) contrast medium was injected into the renal pelvis of a 10-year-old 3.8-kg (8.4-lb) castrated male domestic shorthair cat with partial obstruction of the ureter of a renal allograft secondary to multiple periureteral adhesions. A—Contrast medium is evident in the dilated renal pelvis (arrow) and the lumen of the segmentally dilated and tortuous ureter (asterisk), with only a small amount of contrast medium evident in the urinary bladder (arrowhead). B—More contrast medium has passed from the renal pelvis, through the ureter, and into the urinary bladder, evident by the increased amount of contrast medium in the bladder, compared with the earlier image. However, the renal pelvic and proximal ureteral dilation persist.

  • Figure 3—

    Pyelographic images (left lateral radiographic views) taken almost immediately after injection of contrast medium into the renal pelvis of the left kidney (A) and right kidney (B) in a 4-year-old 6.3-kg (13.9-lb) castrated male domestic shorthair cat with bilateral functional (nonmechanical) obstruction of its ureters, the cause for which was later presumptively diagnosed as inflammatory ureteritis. On each side, the renal pelvis (right, black arrow; left, white arrow) is dilated and the ureter (right, black asterisk; left, white asterisk) is diffusely dilated and tortuous, with a stream of contrast medium entering the bladder (arrowhead). A—The focal areas where minimal to no contrast is seen in the ureter were caused by ureteral peristalsis because subsequent images showed ureteral dilation in these areas. B—Contrast medium from pyelography performed on the contralateral side (with injection 22 minutes before this image was obtained) is still evident in the left renal pelvis (white arrow) and ureter (white asterisk).

  • Figure 4—

    Pyelographic images (right lateral [A] and oblique ventrodorsal [B] radiographic views) of the same cat in Figure 1 after pyelography was performed on the right kidney, the results of which were considered normal. However, pyelographic features of the left renal pelvis (white arrow) and segmental ureteral dilation (white asterisks) remain unchanged compared with Figure 1. A—Image was obtained immediately after contrast medium was injected into the right kidney and 34 minutes after contrast medium was injected into the left kidney. Note that the right kidney has mild pelvic dilation (black arrow), and the right ureter (black asterisks) has a relatively normal and uniform diameter throughout its course along with a stream of contrast medium evident entering the bladder (arrowhead). B—Image obtained 8 minutes after injection of contrast medium into the pelvis of the right kidney and 42 minutes after contrast medium was injected into the pelvis of the left kidney. Almost all contrast medium has emptied from the right renal pelvis (black arrow), and contrast is no longer evident in the right ureter.

  • 1. Berent AC. Ureteral obstructions in dogs and cats: a review of traditional and new interventional diagnostic and therapeutic options. J Vet Emerg Crit Care (San Antonio) 2011;21:86103.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Livet V, Pillard P, Goy-Thollot I, et al. Placement of subcutaneous ureteral bypasses without fluoroscopic guidance in cats with ureteral obstruction: 19 cases (2014–2016). J Feline Med Surg 2017;19:10301039.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Wormser C, Clarke DL, Aronson LR. Outcomes of ureteral surgery and ureteral stenting in cats: 117 cases (2006–2014). J Am Vet Med Assoc 2016;248:518525.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Hardie EM, Kyles AE. Management of ureteral obstruction. Vet Clin North Am Small Anim Pract 2004;34:9891010.

  • 5. Kyles AE, Hardie EM, Wooden BG, et al. Clinical, clinicopathologic, radiographic, and ultrasonographic abnormalities in cats with ureteral calculi: 163 cases (1984–2002). J Am Vet Med Assoc 2005;226:932936.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Horowitz C, Berent A, Weisse C, et al. Predictors of outcome for cats with ureteral obstructions after interventional management using ureteral stents or a subcutaneous ureteral bypass device. J Feline Med Surg 2013;15:10521062.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Steinhaus J, Berent AC, Weisse C, et al. Clinical presentation and outcome of cats with circumcaval ureters associated with a ureteral obstruction. J Vet Intern Med 2015;29:6370.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Westropp JL, Ruby AL, Bailiff NL, et al. Dried solidified blood calculi in the urinary tract of cats. J Vet Intern Med 2006;20:828834.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Zaid MS, Berent AC, Weisse C, et al. Feline ureteral strictures: 10 cases (2007–2009). J Vet Intern Med 2011;25:222229.

  • 10. D'Anjou MA, Bédard A, Dunn ME. Clinical significance of renal pelvic dilatation on ultrasound in dogs and cats. Vet Radiol Ultrasound 2011;52:8894.

    • Search Google Scholar
    • Export Citation
  • 11. Shipov A, Segev G. Ureteral obstruction in dogs and cats. Isr J Vet Med 2013;68:7177.

  • 12. Adin CA, Herrgesell EJ, Nyland TG, et al. Antegrade pyelography for suspected ureteral obstruction in cats: 11 cases (1995–2001). J Am Vet Med Assoc 2003;222:15761581.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Rivers BJ, Walter PA, Polzin DJ. Ultrasonographic-guided, percutaneous antegrade pyelography: technique and clinical application in the dog and cat. J Am Anim Hosp Assoc 1997;33:6168.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Stafford JR, Bartges JW. A clinical review of pathophysiology, diagnosis, and treatment of uroabdomen in the dog and cat. J Vet Emerg Crit Care (San Antonio) 2013;23:216229.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Zelenko N, Coll D, Rosenfeld AT, et al. Normal ureter size on unenhanced helical CT. AJR Am J Roentgenol 2004;182:10391041.

  • 16. Rathi V, Agrawal S, Bhatt S, et al. Ureteral dilatation with no apparent cause on intravenous urography: normal or abnormal? A pilot study. Adv Urol 2015;2015:681836.

    • Search Google Scholar
    • Export Citation
  • 17. Banner MP. Genitourinary complications of inflammatory bowel disease. Radiol Clin North Am 1987;25:199209.

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

  • 19. Berent AC, Weisse CW, Todd K, et al. Technical and clinical outcomes of ureteral stenting in cats with benign ureteral obstruction: 69 cases (2006–2010). J Am Vet Med Assoc 2014;244:559576.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Kyles AE, Hardie EM, Wooden BG, et al. Management and outcome of cats with ureteral calculi: 153 cases (1984–2002). J Am Vet Med Assoc 2005;226:937944.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Snyder DM, Steffey MA, Mehler SJ, et al. Diagnosis and surgical management of ureteral calculi in dogs: 16 cases (1990–2003). N Z Vet J 2005;53:1925.

    • Crossref
    • Search Google Scholar
    • Export Citation

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