Ureteral obstructions are challenging conditions to treat in veterinary medicine given the small UD in cats (0.3 to 0.4 mm) and dogs (1 to 2 mm).1 Medical management (eg, IV fluid administration, osmotic diuresis, analgesia, and α-adrenoceptor blockade) has been associated with a low success rate (10%) and a 12-month survival rate of 66%.2 Surgical interventions such as ureterotomy or ureteronephrotomy have been associated with high morbidity rate (21% in cats2 and 35% in dogs3) and mortality rate (31% in cats2 and 25% in dogs3). Common postoperative complications include uroabdomen (16% of cats), persistent ureteral obstruction (6% of cats), and persistent azotemia (52% of cats and 43% of dogs).2,3 Median survival time in dogs following surgery is reportedly 904 days, whereas in cats the 12-month survival rate is 91%.2,3
To date, ureteral stent placement has been used as a palliative treatment for ureteral obstruction in children and veterinary species. Double-pigtail ureteral stents used for this purpose are soft, multifenestrated, hollow polymeric tubes that provide, following insertion, immediate renal drainage and decompression by allowing urine outflow through their lumen. In children, ureteral stent placement leads to PUD.4 In veterinary species, ureteral stents can remain in place for prolonged periods provided that they are not associated with complications.5–7,a
Many complications have been reported for dogs and cats in which ureteral stents have been placed. For dogs, short-term (< 1 month) complications include hematuria (20%), dysuria (< 5%), obstruction (approx 2%), migration (< 2%), and death (< 2%).8,a The most common long-term (> 1 month) complications in dogs include urinary tract infection (10% to 60%), recurrent obstruction (10%), tissue proliferation at the ureteropelvic junction (5% to 25%), and, less commonly, hematuria, migration, encrustation, and dysuria (< 6% each).8,a For cats, the nature of complications associated with ureteral stents can be perioperative (ie, fluid overload [17%], death [7.5%], and pancreatitis [6%]), short-term (ie, temporary inappetence [25%], dysuria [< 10%], and stent migration [3%]), and long-term (ie, dysuria [38%], hematuria [18%], obstruction [19% to 26%], and urinary tract infection [13%]).6,9
Given the considerable complication rate associated with ureteral stents in cats, a subcutaneous ureteral bypass device was developed and is now commonly used. It consists of a locking-loop nephrostomy tube and cystotomy locking-loop tube, connected together to a shunting port placed SC. When this device has been used in cats, the incidence of dysuria in the short and long term has markedly decreased (< 2%), relative to when no such device is used, but similar incidences of short-term (ie, temporary inappetence [25%], fluid overload [< 5%], and device obstruction [2%]) and long-term (ie, hematuria [18%], obstruction [18%], and urinary tract infection [15%]) complications have been reported.9,10
In humans, ureteral obstructions caused by calculi are managed by extracorporeal lithotripsy or intracorporeal laser lithotripsy by use of ureteroscopy.11 Ureteroscopy is often used to biopsy lesions, investigate causes of hematuria and superficial ureteral neoplasia, and manage nephrolithiasis.12,13 Following these procedures, a stent is often placed for a brief period to avoid future ureteral edema and associated obstruction. Ureteral stents are also used to alleviate symptoms associated with acute renal colic caused by ureteral obstruction.14 It is generally recommended that a ureteral stent be removed from or replaced in a human patient after 3 months to avoid encrustation, infection, and discomfort.15
In children, ureteroscopy is challenging because of the small UD, a situation similar to that encountered in veterinary species. Ureteral stent placement for 2 weeks in children can induce PUD, allowing ureteroscopy to be performed after stent removal.4 To the authors’ knowledge, PUD secondary to ureteral stent placement has not been evaluated in dogs. Ureteroscopy was reportedly performed in 1 dog as part of larger study16 in which the use of sclerotherapy was evaluated for the treatment of essential hematuria in dogs. The purpose of the study reported here was to determine whether PUD would occur after an indwelling ureteral stent was left in place for 2 or 6 weeks, ureteroscopy could be performed safely at stent removal, and PUD would be reversible after ureteral stent removal. Our hypotheses were that placement of a ureteral stent for 2 and 6 weeks in dogs would induce PUD, the presence of a ureteral stent would induce sufficient ureteral dilation to allow passage of a 2.9-mm ureteroscope, and PUD would be reversible after removal of the stent.
Materials and Methods
Animals
This study was conducted at the Ontario Veterinary College, University of Guelph and was approved by the university's Animal Care Committee. Five 3-year-old female purpose-bred Beagles (1 sexually intact and 4 spayed) were acquired from a private research organizationb for use in the study. Median body weight was 10.8 kg (range, 10.1 to 11.7 kg). All dogs were deemed healthy on the basis of unremarkable clinical histories and results of physical examination, prothrombin time and partial thromboplastin time tests, CBC, serum biochemical analysis, urinalysis, bacterial culture of urine, and urogenital ultrasonographic examination.
Timeline
Following collection of baseline data from the clinical testing at study entry (week 0), dogs were anesthetized to allow baseline ureteral measurements by CTEU and to undergo ureteral stent placement under cystoscopic and fluoroscopic guidance. Every 2 weeks until week 10, blood and urine samples were collected for analysis, a urogenital ultrasonographic examination was performed, and dogs were again anesthetized to measure UDs by CTEU. For each dog, 1 ureteral stent was removed at week 2 and the contralateral stent was removed at week 6; the side (left or right ureter) of removal was randomized. Ureteroscopy was attempted immediately following stent removal.
Physical examination
Physical examinations were performed once or twice daily by the same observer (CV), including pain assessment by use of the Colorado Pain Scale.c Other daily observers included a veterinary technician (twice daily) and a dog walker (once daily for 30 minutes). Cages and walking space were inspected for evidence of hematuria.
Clinicopathologic data
At weeks 0, 2, 4, 6, 8, and 10, a CBC, renal function tests, urinalysis, and bacterial culture of urine were performed. For urinalysis, any sample with > 5 WBCs/hpf was classified as pyuria.17
Urogenital ultrasonography
At weeks 0, 2, 4, 6, 8, and 10, urogenital ultrasonographic examination was performed to evaluate the urinary tract and to measure the maximum pelvic width (excluding the proximal portion of the ureter) in a transverse plane.
Cystoscopy
After CTEU during week 0, dogs were transferred to the surgery suite. There, they were positioned in dorsal recumbency with the limbs and tail hanging at the end of the table. An area from the pubis to the dorsal aspect of the vulva was clipped of hair and aseptically prepared. Cefazolin (22 mg/kg) was administered IV. A 14.5F rigid cystoscoped with a 30° lens was advanced into the urinary bladder through the urethra, and both ureteral papillae were identified.
Ureteral stent placement
At the time of cystoscopy during week 0, a ureteral stent was placed in each of the left and right ureters as described elsewhere.18 A 0.064-cm-diameter, 150-cm-long or 0.089-cm-diameter, 180-cm long angled-tipped hydrophilic guidewiree,f as well as a 4F or 5F ureteral catheterg,h were used. Ioxeholi (diluted 1:1 with sterile saline [0.9% NaCl] solution) was used to perform retrograde ureteropyelography. Appropriately sized, double-pigtail ureteral stentsj-l were placed bilaterally. Briefly, with cystoscopic and fluoroscopic guidance, the guidewire was advanced through the ureteral papilla into the ureter up to the ureteropelvic junction. Advanced over the guidewire, the ureteral catheter was further advanced and pyelography was performed. Ioxehol (diluted 1:1 with sterile saline solution) was used as contrast medium for the retrograde ureteropyelogram. The guidewire was reintroduced, and the ureteral catheter was removed. Appropriately sized double-pigtail ureteral stents were placed bilaterally, with one pigtail loop of the stent placed in the renal pelvis and the other was pushed into the urinary bladder. Bupivacaine (0.3 mg/kg) diluted in 3 mL of saline solution was infused into the urethral lumen while the cystoscope was removed. Procedure duration was recorded.
After the procedure, dogs were allowed to recover from anesthesia. Enrofloxacin (10 mg/kg) was administered IM at recovery, lactated Ringer solution was administered IV at 40 mL/h for 12 hours after the procedure, and buprenorphine was administered IV (0.02 mg/kg, q 8 h) twice (with a third dose administered if deemed necessary on the basis of pain assessment findings). These treatments were followed by enrofloxacin (mean dose, 10.76 mg/kg [range, 8.55 to 9.90 mg/kg]) administered PO once a day for 17 days (ie, discontinued 3 days after stent removal at week 2) and tramadol (mean dose, 4.65 mg/kg [range, 4.27 to 4.95 mg/kg]) administered PO every 8 hours for 3 days.
Ureteral stent removal and CTEU
Two weeks after the stent placement (ie, at week 2), 1 of 2 ureteral stents (side randomized) was removed, and findings for the ureter from which the stent was removed were considered group 1 data. Six weeks following stent placement (ie, at week 6), the contralateral ureteral stent was removed, and findings for this second ureter were considered group 2 data. The anesthetic protocol, surgical site preparation, analgesia, and perioperative antimicrobial treatments were identical for ureteral stent placement and removal.
For ureteral stent removal, routine transurethral cystoscopy was performed. The distal loop of the ureteral stent was grasped with endoscopic forcepsm and pulled to the level of the vulva with the cystoscope. Under fluoroscopic guidance, an angled-tipped stiff hydrophilic guidewire appropriately sized for the 3.7Fn or 4.7Fo ureteral stent used was passed through the stent and advanced into the ureter to the level of the renal pelvis to confirm stent patency. The stent was removed over the wire, and the wire was left in place in the ureter. The time required to remove the stent was recorded from the time of cystoscope insertion until complete stent removal from the urethra. Immediately following stent removal, a 2.9-mm flexible ureteroscopep was advanced over the guidewire under fluoroscopic guidance to the level of the midportion of the ureter while constant irrigation was provided with saline solution. The guidewire was removed, and the ureteroscope was advanced to the level of the ureteropelvic junction, where the renal pelvis was identified. The ureteroscope was then pulled back to the level of the ureterovesical junction. Duration of the ureteroscopy procedure was recorded as the time elapsed between introduction of the ureteroscope into the ureter at the ureterovesical junction and removal of it from the ureterovesical junction.
CTEU
At baseline and every 2 weeks thereafter, dogs were sedated by IM administration of butorphanol tartrate (0.2 mg/kg) and acepromazine maleate (0.05 mg/kg). A bolus of lactated Ringer solution (5 mL/kg) was administered IV, followed by a continuous rate infusion of the same solution at a rate of 10 mL/kg/h. Anesthesia was induced with propofol (4 mg/kg, IV) and maintained with isoflurane administered in oxygen, and then CTEU was performed.19 Ureteral diameter measurements were made at 3 anatomic sites: cranially at the level of the renal pelvis, at the level of L4 (referred to as the midmeasurement), and caudally at the ureterovesical junction.
Statistical analyses
Statistical software was used for statistical analyses.q Prior to analysis, CBC, renal function, and urinalysis values for the 5 included dogs were averaged for each week of the study period. Descriptive statistics were computed to determine mean UD and pelvic dilation as well as total durations of the ureteroscopy and stent removal procedures. The Shapiro-Wilk test was used to ensure normal data distribution, and logarithmic transformation was performed when necessary. The mean of the UD measurements for each group (stent removal 2 or 6 weeks after placement) was compared over time. Repeated-measures ANOVA was performed to evaluate the effect of time on UD values. Measurement point and ureteral group (group 1 or group 2) and interactions between these variables as well as UD values were included in the model. Values of P < 0.05 were considered significant.
Results
Animals
Throughout the study, all 5 dogs had signs of a good appetite and unremarkable findings on physical examination; all appeared comfortable during abdominal palpation. At week 2 (2 weeks after stent placement), 1 dog (dog 5) was identified as in estrus, which persisted for 7 days. All dogs had intermittent macroscopic evidence of hematuria for a mean total of 9 days (range, 2 to 13 days) in the first 38 days of the 71-day study period. No hematuria was evident after the last stent removals and endoscopic examinations at week 6.
Clinicopathologic data
Analyte values from CBCs and serum biochemical analyses remained within reference ranges throughout the study. However, serum creatinine concentration at weeks 2 (P = 0.001) and 6 (P = 0.009) were significantly higher than at week 8.
Urinalysis revealed significant differences in urine RBC and WBC counts throughout the study period. Urine RBC count was significantly higher at week 2 (when it reached its maximum value) than at weeks 0 (P = 0.03), 8 (P < 0.001), and 10 (P = 0.001). Compared with results at week 4, urine RBC count at week 8 was significantly (P = 0.001) lower, and compared with results at week 6, urine RBC counts at weeks 8 and 10 were significantly (P = 0.005) lower.
Evidence of pyuria was detected in 3 of 30 urine samples collected during the study; 2 of those 3 samples had positive results of bacterial culture. Two of the 27 samples without evidence of pyuria also had positive results of bacterial culture. A significant increase from the week 0 value in mean urine WBC count for all dogs was identified at weeks 2 (P < 0.001), 4 (P < 0.001), 6 (P < 0.001), 8 (P = 0.006), and 10 (P = 0.004). Mean WBC count was at its maximum at week 2, and significant decreases from this value were identified at weeks 8 (P = 0.03) and 10 (P = 0.047).
During the study, 1 dog (dog 4) had positive results of bacterial culture of urine (Enterococcus faecium identified) at weeks 4 (> 105 CFUs/mL), 6 (> 105 CFUs/mL), and 8 (1.3 × 104 CFUs/mL) and negative results by week 10. Another dog (dog 5) had positive results (Streptococcus canis identified) at week 6 only (> 105 CFUs/mL).
Urogenital ultrasonography
Dilation of the renal pelvis was detected in only 2 dogs at week 2. The degree of pelvic dilation was minimal for both dogs (0.19 cm bilaterally for one dog [dog 1] and 0.18 cm unilaterally the other dog [dog 2]). This dilation had resolved in both dogs by week 4.
Cystoscopy
Cystoscopic examination revealed bilateral mildly intramural ectopic ureters in 1 dog (dog 2), with ureteral papillae located at the urethrovesical junction (Figure 1). No abnormalities were detected in the other dogs during cystoscopic examination.
Cystoscopic image of mildly intramural ectopic ureters (ureteral papillae at the urethrovesical junction) in a dog (dog 2) prior to placement of a stent in each ureter. A wire has been inserted in the right ureteral opening (black arrow). The left ureteral opening (white arrow) is visible just beside the right one.
Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.381
Ureteral stent placement
In 3 dogs (dogs 1, 2, and 3), a 4.7F, 20-cm stent was placed bilaterally. Another (dog 4) had a 3.7F, 18-cm stent placed in the left ureter and a 4.7F, 20-cm stent placed in the right ureter, and the remaining dog (dog 5) had a 4.7F, multilength (22- to 32-cm) stent placed bilaterally. Mean procedure duration for unilateral retrograde placement was 18 minutes (range, 13 to 25 minutes).
Ureteral stent removal and ureteroscopy
Mean duration of the ureteral stent removal procedures at weeks 2 and 6 was 13.0 minutes (range, 5 to 24 minutes) and 8.6 minutes (range, 6 to 15 minutes), respectively. Cystoscopy was performed without complication at weeks 0, 2, and 6. Ureteroscopy was successfully performed in all dogs, with mean durations of 3.2 minutes (range, 2 to 5 minutes) and 4.6 minutes (range, 1 to 11 minutes) at weeks 2 and 6, respectively. The flexible ureteroscope was advanced along the guidewire to the level of the ureteropelvic junction.
CTEU
Initially, findings of CTEU were unremarkable. At week 2, CTEU revealed that the distal loop of the left ureteral stent was within the urethra of 1 dog (dog 1). In another dog (dog 5), the ureteral stent was looped within the proximal aspect of the left ureter, and that loop persisted until removal at week 6, with evidence of focal dilation at week 4, but not at week 6. At weeks 8 and 10, the left ureter wall in dog 5 was thickened along its entire length (ie, poor opacification). At week 4, the unstented ureter had been poorly opacified along its entire length and the ureteral papilla was thickened. Another dog (dog 4) also had a thickened right ureteral papilla at week 10, which was identified 4 weeks after the stent had been removed.
One hundred eighty measurements of UD were collected (Table 1; Figure 2). Between week 0 and the point of stent removal, for the ureters from which stents removed at week 2 (ureter group 1), the UD increased by 53% (from 2.16 to 3.32 mm), 81% (from 1.58 to 2.86 mm), and 65% (from 1.86 to 3.06 mm) in the cranial, midportion, and caudal portion, respectively. For the ureters from which stents were removed at week 6 (ureter group 2), the UD increased by 21% (2.52 to 3.06 mm), 53% (1.82 to 2.8 mm), and 53% (1.86 to 2.86 mm) in the cranial portion, midportion, and caudal portion, respectively. The UD peaked at week 2 (cranial portion and midportion) and week 4 (caudal portion) for group 1, whereas it peaked in all 3 portions at week 4 for group 2 (Supplemental Figures S1 to S3, available at: http://avmajournals.avma.org/doi/suppl/10.2460/ajvr.78.3.381).
Representative transverse CTEU images of the cranial portion (A and B), midportion (C and D), and caudal portion (E and F) of the right and left ureters in a healthy adult female Beagle before (A, C, and E) and 4 weeks after (B, D, and F) PUD of the right ureter induced by stent placement.
Citation: American Journal of Veterinary Research 78, 3; 10.2460/ajvr.78.3.381
Summary data for diameters (mm) of the cranial, mid-, and caudal portions of the ureters in 5 healthy Beagles in which a stent was placed in each ureter at week 0 and then removed* at week 2 (ureter group 1) or 6 (ureter group 2).
| Cranial | Mid | Caudal | ||||
|---|---|---|---|---|---|---|
| Week, by group | Mean (SD) | Range | Mean (SD) | Range | Mean (SD) | Range |
| Group 1 | ||||||
| 0 | 2.16 (0.56) | 1.6–3.0 | 1.58 (0.18) | 1.3–1.7 | 1.86 (0.40) | 1.3–2.3 |
| 2 | 3.32 (0.56) | 2.8–4.1 | 2.86 (0.27) | 2.4–3.1 | 3.06 (0.24) | 2.8–3.4 |
| 4 | 3.08 (0.50) | 2.4–3.7 | 2.60 (0.63) | 1.6–3.2 | 3.38 (0.95) | 2.2–4.5 |
| 6 | 2.90 (0.37) | 2.3–3.2 | 2.72 (0.34) | 2.3–3.2 | 2.50 (0.49) | 1.9–3.0 |
| 8 | 2.42 (0.59) | 1.6–3.2 | 2.00 (0.32) | 1.5–2.3 | 2.16 (0.20) | 2.0–2.5 |
| 10 | 2.52 (0.37) | 2.1–3.0 | 2.02 (0.19) | 1.8–2.3 | 2.30 (0.24) | 2.0–2.5 |
| Group 2 | ||||||
| 0 | 2.52 (0.75) | 1.5–3.6 | 1.82 (0.50) | 1.5–2.7 | 1.86 (0.39) | 1.4–2.4 |
| 2 | 3.14 (0.48) | 2.5–3.7 | 3.22 (0.28) | 2.8–3.5 | 3.06 (0.31) | 2.7–3.4 |
| 4 | 3.52 (0.91) | 2.8–5.0 | 3.32 (1.15) | 2.1–4.5 | 3.32 (0.80) | 2.4–4.5 |
| 6 | 3.06 (0.46) | 2.5–3.6 | 2.80 (0.55) | 2.1–3.4 | 2.86 (0.55) | 1.9–3.3 |
| 8 | 2.88 (0.93) | 2.1–4.5 | 2.60 (0.94) | 1.8–4.2 | 2.80 (1.06) | 2.0–4.6 |
| 10 | 3.04 (0.61) | 2.2–3.9 | 2.40 (0.63) | 1.7–3.4 | 2.28 (0.13) | 2.1–2.4 |
Side (left or right) from which the stent was removed was randomized.
For group 1, UDs at weeks 2, 4, and 6 were all significantly greater than week 0 values for all 3 portions of the ureter (Table 2). The UDs of all portions at weeks 8 and 10 were not significantly different from week 0 values. At week 8, the UD of the cranial portion was also significantly less than at week 2. The UDs of the midportion and caudal portion at weeks 8 and 10 were significantly less than values at week 2 values. The UDs of the caudal portion at weeks 6, 8, and 10 were also significantly less than week 4 values.
Values of P for comparisons of diameters of the cranial, mid-, and caudal portions of the ureters of the dogs and ureter groups in Table 1 at various measurement points.
| Week, by group | Portion | Week 2 | Week 4 | Week 6 | Week 8 | Week 10 |
|---|---|---|---|---|---|---|
| Group 1 | ||||||
| 0 | Cranial | 0.002 | 0.01 | 0.03 | 0.41 | 0.22 |
| Mid | < 0.001 | < 0.001 | < 0.001 | 0.08 | 0.06 | |
| Caudal | < 0.001 | < 0.001 | 0.02 | 0.18 | 0.07 | |
| 2 | Cranial | — | 0.57 | 0.34 | 0.02 | 0.05 |
| Mid | — | 0.38 | 0.69 | 0.008 | 0.01 | |
| Caudal | — | 0.57 | 0.08 | 0.007 | 0.02 | |
| 4 | Cranial | — | — | 0.67 | 0.07 | 0.15 |
| Mid | — | — | 0.62 | 0.07 | 0.09 | |
| Caudal | — | — | 0.02 | 0.002 | 0.006 | |
| Group 2 | ||||||
| 0 | Cranial | 0.07 | 0.01 | 0.11 | 0.33 | 0.13 |
| Mid | < 0.001 | < 0.001 | 0.002 | 0.01 | 0.04 | |
| Caudal | < 0.001 | < 0.001 | 0.001 | 0.004 | 0.08 | |
| 2 | Cranial | — | 0.46 | 0.85 | 0.42 | 0.78 |
| Mid | — | 0.89 | 0.25 | 0.06 | 0.02 | |
| Caudal | — | 0.60 | 0.51 | 0.28 | 0.02 | |
| 4 | Cranial | — | — | 0.35 | 0.13 | 0.31 |
| Mid | — | — | 0.33 | 0.08 | 0.03 | |
| Caudal | — | — | 0.23 | 0.12 | 0.006 | |
| 6 | Cranial | — | — | — | 0.51 | 0.92 |
| Mid | — | — | — | 0.45 | 0.21 | |
| Caudal | — | — | — | 0.66 | 0.09 | |
— = Not applicable.
Values of P < 0.05 were considered significant.
For group 2, UDs of the cranial portion of the ureter at week 4, midportion at week 10, and midportion and caudal portion at weeks 4, 6, and 8 were significantly greater than week 0 values (Table 2). For all 3 portions, UDs at weeks 4, 6, and 8 were not significantly lower than those at weeks 2, 4, and 6, respectively. The UDs of the midportion and caudal portion were significantly lower at week 10 than at weeks 2 and 4. In dog 2 (a dog with mildly ectopic ureters), the UD of the ureter from which the stent had been removed at 2 weeks was similar to that of the other dogs, but the ureter from which the stent had been removed at 6 weeks appeared markedly dilated in the midportion and caudal portion (UD, 4.5 and 3.3 mm at weeks 4 and 6, respectively).
To ensure dog 2 had no important influence on the study results, statistical analyses were reviewed. Seventy-two percent of all UD measurements of dog 2 were equal to or below median values, and analysis was repeated excluding that dog. This analysis revealed that, for the remaining dogs, the UDs of the cranial portion of the ureter for group 1 remained significantly greater than week 0 values at weeks 2 (P = 0.04) and 4 (P = 0.0499), but not at week 6 (P = 0.23), and UDs of the midportion remained significantly greater than week 0 values at weeks 2 (P < 0.001) and 6 (P = 0.004), but not at week 4 (P = 0.09). For the caudal portion of the ureter, UDs remained significantly greater than week 0 values for weeks 2 (P < 0.001), 4 (P = 0.001), and 6 (P = 0.04).
For ureter group 2, removal of dog 2 resulted in no significant differences from week 0 values for the cranial portion of the ureter at weeks 2 (P = 0.22), 4 (P = 0.13), and 6 (P = 0.59). For the midportion, UDs were significantly greater than week 0 values at weeks 2 (P < 0.001) and 6 (P = 0.04), but not at week 4 (P = 0.10). For the caudal portion, removal of dog 2 did not change the overall results.
The sexually intact female, dog 5, had signs of proestrus the day prior to removal of 1 ureteral stent at week 2. To ensure this dog had no important influence on the study results, the statistical analysis was repeated without the UD measurements of this dog. Results were significant with or without dog 5 included with respect to PUD occurring in all ureteral segments at week 2 (cranial portion, P = 0.001; midportion and caudal portion, P < 0.001), week 4 (cranial portion, P = 0.007; midportion and caudal portion, P < 0.001), and week 6 (cranial portion, P < 0.001; midportion, P = 0.03; caudal portion, P = 0.001) relative to baseline for group 1. For group 2, results remained significant for the midportion and caudal portion at week 2 (cranial portion, P = 0.12; midportion and caudal portion, P < 0.001), all 3 portions at week 4 (cranial portion, P = 0.02, midportion, P < 0.001; caudal portion, P = 0.002), and the midportion and caudal portion at week 6 (cranial portion, P = 0.09; midportion, P = 0.002; caudal portion, P = 0.01).
Complications
Complications associated with the stent placement procedure included guidewire puncture of the renal parenchyma through a nondilated calix on 3 occasions (dogs 2, 4, and 5) and 1 incident of mild subcapsular extravasation of contrast medium caused by this puncture (dog 4). No complications were observed with ureteroscopy. In dog 1, mild resistance was noted while attempting to advance the flexible ureteroscope, and this resistance resolved with manual irrigation. Continuous manual irrigation while advancing the ureteroscope was performed subsequently for all dogs, with no further incidents of resistance. After stent removal, the safety wire that was previously in the ureter backed out of the ureter while the flexible ureteroscope was being advanced in 3 ureters of 2 dogs. This movement required regaining wire access to the ureter with the aid of fluoroscopic and cystoscopic guidance as described elsewhere.18
Discussion
Results of the study reported here indicated that PUD occurred in healthy female Beagles within 2 weeks after ureteral stent placement and that ureteroscopy could be performed safely and successfully at the time of stent removal. Ureteral diameters increased by 21% to 81% within 2 to 4 weeks of placement of an indwelling ureteral stent. Increases in UD were also found to develop in Yorkshire pigs (n = 36) in which a ureteral stent had been placed for 10 weeks,20 in female pigs (3) in which a ureteral stent was placed for 7 days,21 and in children (26) in which a ureteral stent was placed for 14 days.4 In pigs, retrograde ureteropyelography revealed little change in UD (ie, < 10 mm) for ureters in which no stent was placed but an increase in UD to > 20 mm for ureters in which a stent was placed.20
Since the 1930s,22 an indwelling stent or catheter has been known to cause reversible ureteral dilation, but the mechanism has not been elucidated. Physiologic relaxation or direct cytotoxic effects have being suggested as possible contributors.23 Ureteral dilation is suspected to occur when foreign material (such as a stent) is present in the ureter, but dilation may also be related to alterations in the renal pelvis and ureteral peristalsis induced by the stent, thus slowing down urine transport.24,25 Ureteral dilation is also associated with ureteral wall inflammation in humans and pigs.21,26
The degree of passive ureteral dilation in patients in which ureteral stents are placed may depend on the stent properties and design. In a previous study,21 female pigs (n = 11) were fitted with a flat-shaped stent (also referred to as a ribbon stent), which has a small-diameter tube and 2 flat wings affixed in opposition to each other.21 Placement of the ribbon stent resulted in little immediate interference on peristalsis and induced less PUD than did a standard ureteral stent, probably reflecting its smaller contact surface with the ureteral wall.21 Given these results and the desire to provide PUD for future ureteral interventions and to aid in stone passage, a tubular-shaped stent was considered the best type of stent to induce PUD in dogs in the present study.
The PUD achieved in the present study was reversible. This was observed in ureter group 1, from which stents were removed after 2 weeks and follow-up was provided for additional 8 weeks. Because of the briefer follow-up period in ureter group 2 (ie, only 4 weeks after stent removal in week 6), we were unable to determine whether a longer period of stent placement led to a longer recovery to the initial UD. However, the UD generally reduced in size over time. Performance of CTEU at 12 weeks after stent placement may have provided the data needed to make such a determination. To our knowledge, no study has been reported in which resolution of the ureteral dilation was evaluated after ureteral stent placement in pigs. Prior studies20,21 concluded with euthanasia of participating animals and postmortem evaluation.
In a study27 involving humans, ureteral stents were left in place for periods ranging from 2 to 4 weeks, but the period required for dilation to occur and thus improve the success rate of ureteroscopy was not fully established. In the present study, the maximum UD was reached at 4 weeks for all dogs, even when the stent was left in place for an additional 2 weeks in ureter group 2. The number of ureters in which a stent was placed (n = 10) was too small to allow definitive conclusions, but our results suggested that maximal PUD may be achieved at 4 weeks after stent placement and may plateau no matter how long the ureteral stent is retained. Clinically, if the goal of PUD is to perform future ureteroscopy, then stents need to be left in place for only 4 weeks to allow this to be successfully accomplished. The UDs were greater than those before stent placement at weeks 2, 4, and 6 for ureter group 1 and at weeks 8 and 10 for ureter group 2. The exact time required for a ureter to return to its original diameter in dogs is unknown. It may be possible to perform ureteroscopy after the initial stent removal time in some situations.
Most cases of urolithiasis in humans are currently managed by ureteroscopy.28 Ureteroscopy has supplanted surgical removal of stones and extracorporeal lithotripsy and has been associated with lower morbidity and mortality rates and better stone-free rates.28 Management of renal and ureteral calculi in dogs is challenging. Stones identified within the upper urinary tract are not usually removed but are instead bypassed by use of ureteral stents or a subcutaneous ureteral bypass procedure.7,29,a Ureteroscopy would offer a minimally invasive treatment approach for dogs and could allow the removal of renal or ureteral stones by use of baskets (diameter, 1.5F to 1.9F) or in conjunction with laser lithotripsy.30–32 These techniques could decrease the risk of surgical and implant-related complications, including the risk of recurrent infection and stent-related clinical signs, such as dysuria or pollakiuria.
Whether dogs with ureteral abnormalities would have the same degree of ureteral dilation as healthy dogs after ureteral stent placement is unknown. In rats, fibrotic tissue slowly replaces the smooth muscle layer in obstructed ureters after 21 days of obstruction, and that fibrotic tissue occupies 90% of the muscle layer after 42 days.33 The dilation capacity of fibrotic tissue is certainly less than that of healthy smooth muscle; thus, it may have an impact on the capacity for PUD. Stents may need to remain indwelling for a longer period to achieve sufficient dilation, or dilation may or may not ultimately occur. If dilation does occur, it would likely be to a lesser degree if a considerable amount of fibrotic tissue develops. In previous research involving ureteral stent placement in cats with ureteral strictures, PUD was not observed at the stricture site.6,34 A similar process has not been described for dogs but is suspected to exist. However, it is possible that ureters of cats are more prone to stricture than those of dogs because of their small diameter.
In the study reported here, 1 of the 5 dogs (dog 2) was incidentally found to have bilateral ectopic ureters. Because of their different muscular composition from that of anatomically normal ureters and a larger ureteral orifice with higher outflow pressure during urination, ectopic ureters are likely prone to exaggerated passive dilation secondary to ureteral stent placement, but such a conclusion cannot be made on the basis of a single case. However, ureteral openings in dog 2 were identified in the urinary bladder (at the urethrovesical junction), and no clinical abnormalities were detected. There was also no evidence of ureterocele or ureteral dilation on ultrasonographic and CTEU examinations at week 0. Because of concern about the anatomic abnormality in this dog, the impact of removing that dog from the analysis was evaluated, and despite its removal from the analysis (thereby reducing statistical power), the main results remained significant. Also, almost three-quarters of UD measurements in dog 2 were equal to or below the median of all the other dogs included in the study, further supporting the presumption that this dog's anatomic abnormality did not bias the results and indicating that retention of its data would be appropriate.
The sexually intact female dog in the present study (dog 5) was in proestrus the day prior to removal of 1 ureteral stent at week 2 and thus might have had an increased circulating concentration of progesterone during the study period. The hormonal effect of progesterone on the ureters in humans has yet to be established.35 Hydronephrosis is known to develop in pregnant women, but controversy exists as to whether the physiologic hydroureter is related to a mechanical obstruction caused by the pregnancy or to hormone secretion.35 In rats, progesterone is suspected to cause ureteral dilation owing to stimulation of ureteral β-adrenergic receptors.36 This subject has not been researched in dogs, so it is unclear whether the increase in progesterone associated with the proestrus and estrus in dog 5 may have contributed to the ureteral dilation noted on CTEU. To ensure that this dog had no important influence on the study results, the statistical analyses were repeated without inclusion of its measurements, revealing results similar to when those measurements were included.
Retrograde ureteropyelography and gross measurements have been used to assess ureteral stent placement in pigs.20,21 In the present study, CTEU was used as described by other investigators.19 Retrograde ureteropyelography would likely have worked equally well or better in the present study because it maximally distends the ureteral lumen and is not influenced by ureteral contractions during peristalsis, which will occur on a CTEU. However, because this technique requires ureteral catheterization and cystoscopy, it was not considered a practical approach for UD measurements when cystoscopy was not being performed. Use of retrograde ureteropyelography could have also increased the risk of bacterial contamination of the urinary tract and stents. Consistent methodology was considered ideal and more clinically relevant. The outer UD was measured given that the inner diameter was frequently difficult to differentiate from the indwelling ureteral stent on CT. In another study24 involving dogs in which ureteral stents were placed for a 4-week period, persistent ureteral muscular hypertrophy and collagen deposition in the subepithelial ureteral wall were identified histologically 8 weeks after stent removal and, to a lesser extent, after 4 weeks.24 Such changes may lead to overestimation of the UD by compromising the distinction of the outer ureteral wall from the stent. To avoid such a situation, the wide window width was used on CT in the present study to facilitate clear definition of the ureteral wall without a bloom effect from the contrast medium. This strategy increased the accuracy of measurement by differentiating the outer wall and the stent in the 2 dogs that had thickened ureteral walls.
We observed a discrepancy between the cranial UD measurements and the mid and caudal measurements. This discrepancy was likely attributable to the typical flared shape of the ureter at the ureteropelvic junction and the caudal curvature of the cranial portion of the ureter when viewed in oblique planes.
In children, ureteral stent placement for 2 to 8 weeks allows successful ureteroscopy (by passive dilation of the ureteral papilla) in 100% of patients, even though previous attempts to pass a ureteroscope into the ureteral orifice may have been unsuccessful.4 This eliminates the need for active dilation of the ureteral orifice.4 Other investigators have reported an 84% success rate after ureteral stent placement, compared with a rate of 45% for patients in which no stent was placed, when ureteroscopy was used to treat ureterolithiasis.27
No attempt was made in the present study to pass the ureteroscope before stent placement because of the desire to avoid iatrogenic damage such as mucosal abrasion, ureteral perforation, intussusception, or avulsion, which have all been reported in humans.37 On the basis of the CTEU-measured UD before stent placement at week 0, it appeared unlikely that ureteroscopy would have been successful without active dilation. In 30% of children and 10% of adults, ureters appear to be resistant to active dilation, which precludes ureteroscopy.37–39 Finally, ureteral stent placement induces PUD not only of the ureteral orifice but also of the entire ureter as well as the other 2 known physiologic sites of ureteral narrowing in humans and in pigs: at the ureteropelvic junction and at the crossing of the iliac vessels.4,20,40 Stent placement prior to ureteroscopy likely contributed to our ability to perform complete ureteroscopic evaluation of the entire ureter successfully in the study reported here.
Although results of the study reported here suggested that ureteroscopy is safe in healthy Beagles after 2 and 6 weeks of ureteral stent placement, it remains uncertain whether the same would be true in dogs with diseased ureters. Despite their established efficacy and safety, ureteral stents can result in morbidity rates as high as 80% in human recipients, but this has not been the situation in dogs.5,7,41,42,a In 20% of human patients, ureteral stent placement is associated with troublesome urinary symptoms such as low-grade fever, flank pain, hematuria, dysuria, and urinary tract infection.43 Adverse effects of stent placement are minimal with indwelling polymeric stents left in place for up to 3 months, but longer periods of stent placement are associated with increased frequency of encrustation, infection, secondary stone formation, and stented tract obstruction,44 which typically prompt surgeons to leave stents in place for the shortest period possible in humans.20,24,45–47
The cause of discomfort associated with stent-related symptoms or signs is not completely understood. Some investigators have suggested that high pressure transmitted to the renal pelvis during urination and trigonal irritation by the intravesical portion of the stent could be causal factors.48 It has also been suggested that stent-related pain and urination frequency could be related to lower ureteral spasm or local trigone sensitivity.48 These conditions usually continue until ureteral stents are removed. Early complications of a double-pigtail stent usually manifest during the first 4 weeks after stent insertion.44 A meta-analysis of 9 randomized controlled trials of stent placement following uncomplicated ureteroscopy in humans revealed that the incidence of lower urinary tract symptoms was significantly higher in those in which a stent had been inserted after ureteroscopy.44 Results also indicated that ureteroscopy was well tolerated, compared with ureteral stent placement.44
Clinical signs reported for dogs following ureteral stent placement have been far different than those reported in humans.49,50 A clinical reporta of ureteral stent placement in dogs with benign ureteral obstructions (n = 44) indicated that no signs of dysuria developed, regardless of stent size, length, or pigtail location. Dysuria and signs of pain reportedly develop in < 2% of affected dogs.5,7,41,a The reason for the low rate of dysuria in dogs (< 2%), compared with that in humans (> 80%) and cats (< 38%), is unknown but is suspected to be associated with the location of the ureterovesical junction (which, in cats, is in the proximal portion of the urethra) and the quadruped stance, which results in the pigtail location being at the bladder apex rather than at the trigone, as occurs in humans.6,51,52
In the present study, all dogs had intermittent hematuria throughout the study, which was not related to the cystoscopy or ureteroscopy and resolved after stent removal. These findings suggested that hematuria may have been related to the presence of the stent. In humans, positive results of bacterial culture of urine, crossing of the lower coil of the pigtail stent to the other side of the bladder, calyceal position of the upper coil, longer stents, larger stent diameter, and type of stent used are factors significantly associated with development of stent-related symptoms.53 None of the dogs in the present study with positive results of bacterial culture of urine had signs of discomfort. The dog with the longest ureteral stentsj had signs similar to those of the others. However, we may have underestimated the degree of stent-related urinary signs because micturition could not be carefully assessed given that the dogs were caged, research-colony dogs untrained to urinate on walks. None of the dogs had urinary disease prior to ureteral stent placement, so whether our results are generalizable to diseased dogs is unknown. No dog had any signs of stranguria, pollakiuria, or lethargy, all of which are classic signs of stent-associated discomfort in humans and cats.
Bacteriuria and recurrent urinary tract infections are complications of stents in humans and dogs,37,44,51,54–59 and the longer a stent remains indwelling, the higher the rate of positive results of bacterial culture of urine.20 Stents with the highest bacterial colonization rates (ie, 75% to 100%) are generally those that have been in place for > 3 months.54,55 In a study7 involving dogs, urinary tract infections were identified in approximately 60% of those in which ureteral stents were placed, but the dogs in that study had an infection prior to stent placement. In the present study, 2 dogs had subclinical bacteriuria, defined by positive results of bacterial culture, without evidence of clinically important pyuria or clinical signs. The same organisms were isolated by bacterial culture of the stents removed from these 2 dogs, but bacterial culture results for urine were negative after stent removal. The dogs might have developed a clinical urinary tract infection had the ureteral stents been left in place for > 6 weeks. The low rate of infection in our study may be explained by the short period of stent placement and the absence of concurrent or past urinary tract disease. Enrofloxacin administration after ureteral stent placement also likely contributed to the low infection rate.
The E faecium isolated from the urine sample of 1 dog in the present study was multidrug resistant, whereas the S canis isolated from the urine sample of another dog was suseptible to all drugs tested. Although multidrug resistance is common in E faecium because of its intrinsic antimicrobial resistance,61,62 it was unclear whether enrofloxacin administration contributed to this finding. Prophylactic antimicrobial administration remains controversial for various procedures in humans.58 Appropriate prophylactic regimens, including appropriate drugs to use, if any, remain untested in veterinary medicine. Enrofloxacin was used because of its good efficacy against common uropathogens, particularly Escherichia coli and Staphylococcus spp. A combination of amoxicillin and clavulanic acid or amoxicillin alone would be similarly effective; however, fluoroquinolones prevent biofilm formation on ureteral stents in humans.63–65 For this reason, we chose to use enrofloxacin.
Serum creatinine concentrations in the dogs of the present study changed significantly after stent placement but remained within reference limits throughout the study. In contrast, serum creatinine concentration remained stable in pigs (n = 36) in which ureteral stents were left in place for up to 7 weeks.20 The increased concentrations in the study dogs could have been associated with renal damage secondary to the presence of the stents,24,25 a partial ureteral obstruction, or toxic effects of contrast medium. The degree of renal pelvis dilation was minor and not supportive of an obstruction, which is consistent with findings of other studies involving dogs and cats.66 Results of CTEU did not support the presence of ureteral obstruction. In all dogs, the guidewire could be advanced up the lumen of the stent. This confirmed stent patency and the lack of a ureteral obstruction. Only 2 dogs had a slightly dilated renal pelvis (ie < 2 mm). Pelvic dilation has been identified in dogs with normal renal function, dogs receiving fluid therapy,66 and dogs with inflammation or infection.67 Additionally the renal pelvis could passively dilate, as does the ureter, accommodating the presence of the stent.
The present study had some limitations, including the small sample size, short follow-up period for ureter group 2, and lack of a detailed dysuria evaluation. Questions remain regarding whether the same degree of PUD achieved in the healthy Beagles would be achieved in dogs with ectopic ureters, small-breed dogs with small ureters, and dogs with diseased ureters. Also, by only measuring UD by CTEU rather than by retrograde ureteropyelography, the degree of ureteral dilation was likely underestimated. This likelihood is supported by the fact that the ureteroscope was 2.9 mm in diameter, and many ureters on CTEU measured smaller than that despite our ability to easily pass the endoscope up them. Without active ureteral dilation, measurement of the true UD was not possible.
To the authors’ knowledge, the present study represents the first in which placement of ureteral stents to provide PUD for ureteroscopy was evaluated in dogs. The technique was straightforward, fast, and successful. The need for dogs to undergo an additional anesthetic procedure for stent placement prior to ureteroscopy may be considered a trade off, but the mean procedure time was 18 minutes, making this a simple, outpatient task. It should be made clear that the ureteral stent procedures were performed by operators with a high degree of experience, making the procedure more efficient than would have been possible for a novice operator. The stent removal and ureteroscopy procedures were performed by operators with less experience, yet these too were fast and efficient. Further evaluation of PUD and ureteroscopy in dogs with ureteral diseases is the next obvious step. In the interim, results of the present study suggested that a significant amount of PUD occurred within 2 weeks after ureteral stent placement in healthy Beagles and that the degree of dilation peaked at 4 weeks and was reversible with time. Ureteroscopy was safely performed at the time of ureteral stent removal.
Acknowledgments
Supported by the Ontario Veterinary College Pet Trust Fund. The authors report that there were no conflicts of interest. Presented as an abstract at the Annual Forum of the American College of Veterinary Internal Medicine, Nashville, Tenn, June 2014.
ABBREVIATIONS
| CTEU | Computed tomographic excretory urography |
| PUD | Passive ureteral dilation |
| UD | Ureteral diameter |
Footnotes
Pavia P, Berent A, Weisse C, et al. Outcome following ureteral stent placement in dogs for benign ureteral obstructions: 44 dogs (57 ureters) 2009–2013 (abstr), in Proceedings. Annu Forum Am Coll Vet Intern Med 2015:938.
Vivocore Inc, Toronto, ON, Canada.
Canine Acute Pain Scale, Colorado State University, Fort Collins, Colo. Available at: www.csuanimalcancercenter.org/assets/files/csu_acute_pain_scale_canine.pdf. Accessed Sep 4, 2013.
Hopkins rigid cystoscope (2.7 mm), Karl Storz Veterinary Endoscopy, Goleta, Calif.
Standard hydrophilic Weasel wire (0.025-inch) angled/regular taper (150 cm), Infiniti Medical, Menlo Park, Calif.
Standard hydrophilic Weasel wire (0.035 inch) angled/regular taper (180 cm), Infiniti Medical, Menlo Park, Calif.
Tigertail flexible tip ureteral catheter (4F; 70 cm), CR Bard Inc, Covington, Ga.
Tigertail flexible tip ureteral catheter (5F; 70 cm), CR Bard Inc, Covington, Ga.
Omnipaque, GE Healthcare Canada Inc, Mississauga, ON, Canada.
Small dog kit 3.7F 18-cm ureteral stent, Infiniti Medical, Menlo Park, Calif.
Large dog kit 4.7F 20-cm ureteral stent, Infiniti Medical, Menlo Park, Calif.
InLay Optima multilength ureteral stent (4.7F; 22 to 32 cm), CR Bard Inc, Covington, Ga.
Biopsy forceps (1 mm × 120 cm), Karl Storz veterinary endoscopy, Goleta, Calif.
Stiff hydrophilic Weasel wire (0.025 inch) angled/regular taper (180 cm), Infiniti Medical, Menlo Park, Calif.
Stiff hydrophilic Weasel wire (0.035 inch) angled/regular taper (180 cm), Infiniti Medical, Menlo Park, Calif.
Ureteroscope Flex X2 fiberscope (8.8F, 2.9 mm × 100 cm), Karl Storz veterinary endoscopy, Goleta, Calif.
SAS, version 9.2, SAS Institute, Cary, NC.
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