- Email: [email protected]
Nephroureteral Obstructions
N e p h ro u re t e r a l Obstructions The Use of Stents and Ureteral Bypass Systems for Renal Decompression Carrie A. Palm,
DVM
a
, William T.N. Culp,
b, VMD *
KEYWORDS Interventional radiology Interventional urology Stent Subcutaneous ureteral bypass Nephroureterolithiasis Ureteral obstruction KEY POINTS The treatment of benign nephroureteral obstructions is challenging and often involves a combination of medical and surgical/interventional therapeutic options. Historical surgical treatments of nephroureteral obstructions have demonstrated varying results; however, newer interventional radiology therapies, such as stent and subcutaneous ureteral bypass system placement, are being used more commonly. The indications for the placement of stents and subcutaneous ureteral bypass systems still need to be fully elucidated, but early results are showing promise.
INTRODUCTION
Canine and feline nephroureteral obstruction is a complex disease process that can be challenging to treat. Although the availability of various imaging modalities allows for a straightforward diagnosis to be made in most cases, the decision-making process for when a case should be taken to surgery, as well as the optimal treatment modality that should be used for renal decompression, remains controversial. In the following discussion, an overview of the perioperative management of cases with nephroureterolithiasis and nephroureteral obstruction is reviewed, with a focus on the use of renal decompressive procedures, such as ureteral stenting and subcutaneous ureteral bypass (SUB) system placement. The authors teach laboratories where some of the instrumentation discussed in this article are utilized. a Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, One Garrod Drive, Davis, CA 95616, USA; b Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, One Garrod Drive, Davis, CA 95616, USA * Corresponding author. Veterinary Medical Teaching Hospital, University of California-Davis, One Garrod Drive, Davis, CA 95616. E-mail address: [email protected] Vet Clin Small Anim 46 (2016) 1183–1192 http://dx.doi.org/10.1016/j.cvsm.2016.06.008 vetsmall.theclinics.com 0195-5616/16/$ – see front matter Ó 2016 Elsevier Inc. All rights reserved.
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Diagnosis
To effectively diagnose, treat, and manage patients with benign upper urinary tract obstructions, it is important to try and identify the underlying causes for these obstructions. The diagnosis of nephroliths and ureteroliths has increased over the last few decades because of advancements in diagnostic imaging and client and clinician education. In cats, nephroliths and ureteroliths are most commonly composed of calcium oxalate1–3; however, other stone types, including dried solidified blood calculi and struvite stones,1,4 are also found. It is also important to note that in many cases of feline ureteral obstruction discrete calculi may not be identified. In these cases, it is likely that ureteritis, scarring from previous inflammation, and/or cellular or crystalline debris may be the cause of obstruction. Identifying the underlying cause for ureteral obstruction will help to guide the optimal treatment plan as well as long-term medical management after renal decompression has been performed. A serum biochemistry profile should be performed in any dog or cat suspected of having an upper urinary tract obstruction. Most cats with ureteroliths have been shown to be azotemic,3,5 even when unilateral ureteral obstruction is present. This finding emphasizes the fact that a large percentage of cats have preexisting chronic kidney disease (often times from a previous obstruction of the contralateral kidney) before diagnosis of obstruction. Evaluating the severity of azotemia, in addition to electrolytes, such as potassium, can help to guide whether patients should be taken to surgery on an emergency basis. The severity of azotemia (in conjunction with diagnostic imaging) also provides information regarding the degree of underlying chronic kidney disease that is present, a variable that may guide an owner’s decision to pursue surgical intervention. The decision to pursue surgical intervention is not always straightforward, especially in nonazotemic patients that may appear clinically healthy. With the discovery of newer biomarkers of early kidney injury and dysfunction that are much more sensitive than creatinine, earlier diagnosis of and intervention for ureteral obstruction may become possible.6,7 The complete blood count often demonstrates anemia in cats with ureteral obstruction; in some cases, this may indicate the presence of longer-standing chronic kidney disease.3,5 Additionally, the presence of an inflammatory leukogram may suggest an underlying infection associated with the presence of a stone or as the sole cause for the obstruction (ie, ureteritis). Urinalysis and urine culture should be performed in all patients affected with nephroureterolithiasis. Assessment of urine pH may be useful in differentiating between stone types. Sediment evaluation can help to identify the presence of bacteria and pyuria. In dogs, struvite stones are most commonly associated with urease-producing bacteria (ie, Staphylococcus, Proteus, Klebsiella). The presence of these bacteria should raise the clinician’s suspicion for the presence of a struvite stone. If a partial ureteral obstruction is present (and the ureteral stone is, therefore, bathed in urine), it is possible that medical management could be used as the sole treatment; however, concurrent ureteral stent placement may be necessary (see later discussion). In the authors’ experience, sterile pyuria is found commonly in patients with ureteral obstruction, likely due to the inflammatory processes that are initiated soon after development of ureteral obstruction. Nonetheless, a urine culture should be performed in all patients with ureteral obstruction. In patients with complete ureteral obstruction, or in anuric patients, a sample of renal pelvic urine can be taken for culture if patients are undergoing surgical decompression. Abdominal ultrasound should be performed in all cases of suspected nephroureteral obstruction. Ultrasound is the primary imaging method used for diagnosis of ureteral
Stents and Ureteral Bypass Systems for Renal Decompression
obstruction; however, it is important to note that ureteral obstruction can be missed in early obstruction, partial obstruction, and in patients that are dehydrated or hypovolemic at the time of evaluation. As discussed earlier, ultrasound can be used to evaluate for chronic changes in the kidneys and can also be used as a monitoring tool for changes in renal pelvic and ureteral diameters that can either indicate spontaneous renal decompression (without surgical intervention) or progressive dilation, indicating a need for surgical intervention. Ultrasound can also be used to visualize stones and other obstructing debris in the kidney and ureter.3 In the authors’ practice, ultrasound is commonly used to monitor response to therapy by evaluating renal pelvic and ureteral size after intervention. In patients with ureteral obstruction, plain abdominal radiographs can be used to complement ultrasound. The sensitivity of radiographs in the identification of ureteral calculi has been shown to be 81%.3 Additionally, in severe cases, hydroureter can also be diagnosed on survey abdominal radiographs. Many surgeons value the use of abdominal radiographs before surgery, as the number and location of stones can often be identified. Fluoroscopy is often used during renal decompression surgery. During these procedures, nephrocentesis is performed to allow for contrast medium injection. During and after contrast medium administration, fluoroscopy is performed to evaluate the degree of hydronephrosis, the location and course of the ureter, and the location of ureteral obstruction. Although performed uncommonly at the authors’ institution, preoperative antegrade nephropyelograms can also be performed with the use of fluoroscopy in cases where diagnosis of obstruction is not straightforward. In veterinary medicine, advanced cross-sectional imaging, including computed tomography (CT) and MRI, is not commonly used in the assessment of patients with nephroureteral obstruction. These imaging modalities provide high-quality, detailed images of the upper urinary tract, including identification of kidney and ureteral size, and the presence of calculi. When more traditional surgeries, such as ureterotomy without stent placement, are performed, CT can be useful for identification of multiple ureteral stones, so that all stones can be addressed at the time of surgery; however, results of these advanced imaging techniques do not typically impact the clinical decision-making when newer minimally invasive techniques (eg, stents and SUBS) are used. In addition, increases in intra-renal pressures secondary to nephroureteral obstruction can prevent contrast uptake by the kidneys and obscure diagnostic results. Decision-making
The decision-making process for optimal treatment timing and modality for cases affected with nephroureteral obstruction is impacted by several factors. Nephroliths that are not causing clinical signs and have been found incidentally are generally monitored without intervention. If patients are experiencing chronic urinary tract infections or the nephrolith has grown large enough to obstruct urine outflow from the renal pelvis, removal can be considered. If a stent or SUB system can be placed to allow urine to flow from the renal pelvis to the bladder in these cases, surgical removal of the nephroliths may not be required. In cases whereby patients are oliguric or anuric secondary to a ureteral obstruction, intervention is mandatory. Historically, treatment options for these cats included stabilization with hemodialysis (if indicated and available), followed by ureterotomy or other traditional ureteral surgery. In the authors’ practice, when a ureteral obstruction is highly suspected or confirmed with imaging, surgery is performed as the first-line
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therapy in nearly every case. As hemodialysis only provides temporary stabilization in this scenario and requires patients to be anticoagulated, performing this procedure before surgery is generally not indicated and may lead to the need for postponement of surgery. The need for systemic anticoagulation can be avoided with the use of extracorporeal citrate anticoagulation. With immediate and aggressive medical management, however, it is the authors’ experience that almost every patient can be stabilized for surgery without instituting hemodialysis. In patients with ureteral calculi that are nonobstructive (ie, no evidence of ureteral dilation or hydronephrosis), intervention to remove or bypass the calculi is generally not indicated, especially given the potential morbidity. However, serial monitoring of these patients with blood work and abdominal ultrasound is recommended, as unilateral obstruction can occur with minimal to no clinical signs present. Serial creatinine trending for each individual patient and the use of newer biomarkers may allow for earlier diagnosis in patients with unilateral ureteral obstruction. In stable patients (ie, no electrolyte derangements and no overhydration) with ultrasonographic evidence of ureteral obstruction, medical management can be considered, although, in the authors’ hands, this is often unsuccessful. The decision to pursue surgical intervention is not always straightforward, especially in nonazotemic patients that may appear clinically healthy. Significant renal injury develops within hours after ureteral obstruction and prolonged obstruction leads to progressive inflammation and fibrosis, which will ultimately develop into chronic kidney disease that will remain after renal decompression. Given this, along with the risk for contralateral obstruction to develop over time and the high incidence of chronic kidney disease (especially in feline patients), preservation of as much renal function via early surgical intervention is likely indicated in many cases. Once the decision to pursue renal decompression is made, there are several factors that play a role in selecting the optimal surgery type for each case. These factors include surgeon expertise and comfort with each procedure as well as availability of equipment (eg, stents, SUBs, fluoroscopy, surgical microscope). The focus of this article is on the use of stents and SUBs for renal decompression, but it is important to note that some clinicians still prefer to manage patients with ureteral obstruction with traditional surgery techniques. The authors prefer ureteral stenting in dogs experiencing ureteral obstruction secondary to urolithiasis, as these stents can be placed minimally invasively (percutaneous or endoscopic guided) and removed minimally invasively and are generally well tolerated. Stents can be exchanged when partial migration or blockage occurs, and often this can be performed without performing a celiotomy. The placement of a SUB system is considered in cases with known ureteral strictures, circumcaval ureters (Fig. 1), when stents cannot be placed successfully, and when stents have not been tolerated by patients.8 Treatment
As stated earlier, this discussion focuses on the use of stents and SUB systems in the treatment of ureteral obstructions in dogs and cats. Different considerations need to be made for dogs as compared with cats, and these are discussed later. In addition, the limited amount of available literature is discussed later, but it is important to note that continued scientific evaluation of outcomes with the different surgery types is warranted so that the best treatment decisions can be made for veterinary patients. Ureteral stenting
Ureteral stents (also called ureteric stents) are tubes placed into the ureter to allow for urine to flow from the kidney (renal pelvis) to the bladder. Additionally, stents can be
Stents and Ureteral Bypass Systems for Renal Decompression
Fig. 1. (A) Intraoperative image of a 12-year-old female spayed domestic longhair. A right circumcaval ureter is seen here. (B) To treat a ureteral obstruction in this case, an SUB system has been placed.
placed as a means of splinting a ureter that has been anastomosed after a surgical incision or trauma.9,10 Ureteral stents have been shown to stimulate ureteral dilation.11 Ureteral stents can be made of various materials; but currently, there are 3 major categories: polymeric compounds, metal, and biodegradable.12–14 Although each stent type has its own advantages, no single ureteral stent is perfect. In human patients undergoing stent placement, morbidity is reported in up to 80% of cases15,16; therefore, an emphasis has been placed on the development of new stents.13 Although complications can occur in dogs and cats with ureteral stents, the tolerance of stents tends to be better than in humans. The use of ureteral stents for treatment of both benign and malignant ureteral obstructions has been described in several veterinary studies.5,17–24 The most commonly reported indications for ureteral stenting in dogs and cats have been for treatment of benign obstructions with calculi or strictures.18,19,21,23 Ureteral stents can be placed in dogs and cats using several different techniques. A percutaneous technique has been described in the treatment of malignant ureteral obstructions in dogs24; but a description of this technique for benign obstructions is lacking in veterinary patients, except for an isolated report in a tiger.25 To perform this technique, ultrasound guidance is used to visualize the renal pelvis and percutaneous nephrocentesis is performed. A guidewire is then passed through the renal access needle and manipulated through the ureter and into the bladder and urethra with fluoroscopic guidance. This technique allows for retrograde placement (from the urethra and into the kidney) of the stent over the guidewire. Antegrade placement can also be performed with use of a sheath placed percutaneously through the nephrocentesis
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puncture site into the renal pelvis. In the authors’ practice, percutaneous stent placement is generally considered only in canine patients, as it has not been successful in cats. Both antegrade and retrograde placement of stents can be performed in dogs and cats after a celiotomy. The authors prefer antegrade placement of ureteral stents, as this allows for through-and-through guidewire access (ie, the guidewire can be grasped outside of the entry point into the kidney and at the exit point from the bladder). This technique has been described in veterinary studies.17–19 After performing a ventral midline celiotomy, the affected kidney is isolated by draping the other abdominal organs away and dissecting perirenal fat as necessary. A 22-gauge over-the-needle catheter is introduced into the greater curvature of the kidney aiming toward the ureteral-pelvic junction; generally, this is a location that is equidistant dorsal-ventral and cranial-caudal on the greater curvature. When urine is obtained from the over-the-needle catheter, the needle is removed and the catheter is left in the renal pelvis. A T-port that had been primed with a 50%/50% mixture of saline/iodinated contrast is attached to the catheter and the renal pelvis is filled under fluoroscopic guidance. Fluoroscopy confirms the presence of the catheter within the renal pelvis. A 0.018-in hydrophilic guidewire is then introduced into the catheter and passed antegrade down the ureter and into the bladder. A cystotomy is performed, and the wire is grasped from the bladder and passed externally (out of the bladder). The catheter is removed over the guidewire. A ureteral dilator is then passed normograde over the guidewire through the renal parenchyma into the renal pelvis and through the ureter until it is exits through the ureterovesicular junction (UVJ). The dilator is then removed, and a ureteral stent is passed over the guidewire. The cranial pigtail of the stent is positioned within the renal pelvis using fluoroscopic guidance. When placement is confirmed, the guidewire is removed normograde from the stent allowing a pigtail to form in the bladder. One study evaluated 12 cats that underwent antegrade placement of ureteral stents. Nine cats underwent unilateral stent placement, and 3 cats received bilateral stents.19 A ureterotomy was required in 3 cats, and 4 cats required ureteral resection and anastomosis to allow for stent placement. Of the 12 cats treated in that study, 11 were discharged and all cats demonstrated improvement in azotemia. Postoperatively, serum creatinine and renal pelvic size improved significantly when compared with preoperative values.19 In the largest study to date, the antegrade technique was the preferred approach by the authors, although other techniques were also described.18 In that study, ureteral stent placement, using a newer stent device specifically designed for cats, was successful in 52 of 53 (98%) cats.18 Complications occurring during the procedure, immediately postoperative, and in the short-term occurred in less than 10% of cases; long-term complications occurred in 33% of cats, although most were considered minor.18 Retrograde stent placement can also be performed with the use of endoscopy or during an open abdominal approach after cystotomy.18,22,26 Endoscopic ureteral stent placement is the preferred technique by the authors for treating benign ureteral obstructions in dogs (Fig. 2). In one study, retrograde ureteral stenting was attempted in the treatment of obstructive ureterolithiasis with secondary pyonephrosis in 13 dogs.26 The procedure was successfully performed with cystoscopic and fluoroscopic guidance in 11 of 13 dogs. Long-term complications were uncommon and included stent encrustation, stent migration, and tissue proliferation at the UVJ. Overall, the procedure was determined to be effective.26 Retrograde ureteral stents placed with endoscopy has also been reported in feline cases, although this is rarely performed.17,18
Stents and Ureteral Bypass Systems for Renal Decompression
Fig. 2. (A) Cystourethroscopic view of the left ureteral orifice. A hydrophilic guidewire has been introduced into the left ureter using cystoscopy. (B) Ventrodorsal fluoroscopic image. The guidewire (black arrow) has been passed into the renal pelvis. (C) Ventrodorsal fluoroscopic image. A ureteral stent (tip marked by yellow arrow) is being passed retrograde into the ureter over the guidewire. (D) Ventrodorsal fluoroscopic image: after placement of the ureteral stent, the guidewire has been removed; the pigtails of the stent can be seen in the renal pelvis and bladder.
For retrograde ureteral stenting performed with cystoscopic and fluoroscopic guidance, patients are placed in dorsal recumbency and cystourethroscopy is performed. Once the UVJ has been identified, a hydrophilic guidewire is introduced through the working channel of the cystoscope and passed into the ureter and past the obstruction into the renal pelvis. Once in the renal pelvis, the guidewire is formed into a curl to prevent backing out. An open-ended ureteral catheter is introduced over the guidewire to allow for nephropyelography and stent sizing. Once a nephropyelogram has been performed, the guidewire is reintroduced into the ureteral catheter and the catheter is removed. A ureteral stent is then introduced over the guidewire (through the working channel of the scope) and into the ureter until the cranial pigtail can be visualized over the leading end of the guidewire. The guidewire is withdrawn while the cystoscope is positioned within the bladder to direct the caudal aspect of the stent (still in the working channel) into the bladder with a ureteral pusher catheter.
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The retrograde placement of ureteral stents has also been described in cats after performance of a celiotomy.17,18 This procedure is performed similar to the endoscopic technique after a cystotomy has been performed to expose the UVJ. With this technique, a cystoscope is not used and the caudal pigtail of the stent is manually placed in the bladder after placement of the cranial pigtail in the renal pelvis. Descriptions of stent placement through ureterotomy sites or after ureteral resection have been reported.17,21 In these cases, a guidewire is introduced into the ureterotomy site or up the open end of the ureter. Dilation is performed when possible, and stents are generally placed in retrograde fashion. Stents can also be placed to support anastomoses that have been performed during stone removal or after trauma.5,17 Traditional ureteral surgery has been compared with ureteral stenting in the treatment of ureteral obstruction in 2 recent studies.5,27 In one study,5 the occurrence of lower urinary tract signs and urinary tract infections was significantly higher in those cases that received a ureteral stent as compared with those that did not.5 In a separate study, cats that underwent ureteral stent placement had significantly greater decreases in blood urea nitrogen and creatinine 1-day postoperatively and at discharge as compared with cats that underwent ureterotomy without stent placement. Additionally, in that study, cats that underwent ureteral stent placement were significantly more likely to have resolution of azotemia in-hospital.27 The short-term outcome associated with ureteral stents is considered good, as most treated dogs and cats survive to discharge from the hospital; in addition, improvement in azotemia and ultrasonographic findings occurs regularly.17,18,20,23,26,27 Long-term complications associated with ureteral stent placement have been described in several studies.5,17–21,23 Dysuria, hematuria, and stranguria have been noted to occur in cats after stent placement5,18; in one study, dysuria was noted in 37% of cats.18 Additionally, stents need to be exchanged or replaced in up to 27% of cases because of stent migration, fracture, encrustation, obstruction, or lower urinary tract signs that are refractory to medical management.5,17,18 Ureteral bypass
The placement of ureteral bypass systems (in particular the SUB) has become more commonplace in companion animals over the last several years. The concept of the SUB system is that a nephrostomy tube and cystostomy tube are placed permanently and connected via a shunting port. Urine can then flow through the attached catheters and is delivered into the bladder. The veterinary literature on the topic is currently limited to 2 case series8,20 and 1 case report.28 Early results associated with the SUB system placement are promising. In a study evaluating both stents and SUBs for the treatment of benign ureteral obstructions in cats, all cases had successful decompression of the renal pelvis postoperatively and survival was considered good.20 In a separate study, a SUB system was used in the treatment of cats with both circumcaval and noncircumcaval ureters, of which most cases had ureterolithiasis.8 In that groups of cats, the SUB system was shown to reobstruct less commonly than ureteral stents.8 The placement of the SUB system is performed after a ventral midline celiotomy. An 18-gauge over-the-needle catheter is inserted into the caudal pole of the kidney equidistant ventral-dorsal and directed to the renal pelvis. Similar to ureteral stent placement, nephropyelography is performed. A 0.035-in guidewire is then placed into the 18-gauge catheter and coiled in the renal pelvis. The 18-gauge catheter is removed over the guidewire. A 6.5F pigtail locking-loop nephrostomy tube is placed over the
Stents and Ureteral Bypass Systems for Renal Decompression
guidewire into the renal pelvis and secured to the renal capsule with tissue glue. A 7F cystostomy tube is then inserted into the bladder and secured to the bladder with sutures. The tube ends of both the nephrostomy and cystostomy tubes are tunneled through the body wall and attached to a titanium shunting port that is secured to the body wall. Proposed benefits of SUB system placement include the fact that ureteral surgery is not required, the cystostomy tube enters at the bladder apex (and not through the UVJ as is the case with stents), and flushing of the SUB system can be done, to possibly prevent obstruction of the tubing. REFERENCES
1. Cannon AB, Westropp JL, Ruby AL, et al. Evaluation of trends in urolith composition in cats: 5,230 cases (1985-2004). J Am Vet Med Assoc 2007;231:570–6. 2. Low WW, Uhl JM, Kass PH, et al. Evaluation of trends in urolith composition and characteristics of dogs with urolithiasis: 25,499 cases (1985-2006). J Am Vet Med Assoc 2010;236:193–200. 3. 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;226:932–6. 4. Westropp JL, Ruby AL, Bailiff NL, et al. Dried solidified blood calculi in the urinary tract of cats. J Vet Intern Med 2006;20:828–34. 5. 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; 248:518–25. 6. Palm CA, Segev G, Cowgill LD, et al. Urinary neutrophil gelatinaseassociated lipocalin as a marker for identification of acute kidney injury and recovery in dogs with gentamicin-induced nephrotoxicity. J Vet Intern Med 2016;30:200–5. 7. Hokamp JA, Nabity MB. Renal biomarkers in domestic species. Vet Clin Pathol 2016;45:28–56. 8. 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;29:63–70. 9. Chew BH, Lange D. Advances in ureteral stent development. Curr Opin Urol 2016;26:277–82. 10. Wormser C, Clarke DL, Aronson LR. End-to-end ureteral anastomosis and double-pigtail ureteral stent placement for treatment of iatrogenic ureteral trauma in two dogs. J Am Vet Med Assoc 2015;247:92–7. 11. Lennon GM, Thornhill JA, Grainger R, et al. Double pigtail ureteric stent versus percutaneous nephrostomy: effects on stone transit and ureteric motility. Eur Urol 1997;31:24–9. 12. Fiuk J, Bao Y, Calleary JG, et al. The use of internal stents in chronic ureteral obstruction. J Urol 2015;193:1092–100. 13. Brotherhood H, Lange D, Chew BH. Advances in ureteral stents. Transl Androl Urol 2014;3:314–9. 14. Auge BK, Preminger GM. Ureteral stents and their use in endourology. Curr Opin Urol 2002;12:217–22. 15. Joshi HB, Stainthorpe A, MacDonagh RP, et al. Indwelling ureteral stents: evaluation of symptoms, quality of life and utility. J Urol 2003;169:1065–9.
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16. Joshi HB, Newns N, Stainthorpe A, et al. Ureteral stent symptom questionnaire: development and validation of a multidimensional quality of life measure. J Urol 2003;169:1060–4. 17. Kulendra NJ, Syme H, Benigni L, et al. Feline double pigtail ureteric stents for management of ureteric obstruction: short- and long-term follow-up of 26 cats. J Feline Med Surg 2014;16:985–91. 18. 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;244:559–76. 19. Manassero M, Decambron A, Viateau V, et al. Indwelling double pigtail ureteral stent combined or not with surgery for feline ureterolithiasis: complications and outcome in 15 cases. J Feline Med Surg 2013;16:623–30. 20. 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;15:1052–62. 21. Nicoli S, Morello E, Martano M, et al. Double-J ureteral stenting in nine cats with ureteral obstruction. Vet J 2012;194:60–5. 22. Lam NK, Berent AC, Weisse CW, et al. Endoscopic placement of ureteral stents for treatment of congenital bilateral ureteral stenosis in a dog. J Am Vet Med Assoc 2012;240:983–90. 23. Zaid MS, Berent AC, Weisse C, et al. Feline ureteral strictures: 10 cases (20072009). J Vet Intern Med 2011;25:222–9. 24. Berent AC, Weisse C, Beal MW, et al. Use of indwelling, double-pigtail stents for treatment of malignant ureteral obstruction in dogs: 12 cases (2006-2009). J Am Vet Med Assoc 2011;238:1017–25. 25. Delk KW, Wack RF, Burgdorf-Moisuk A, et al. Percutaneous ureteral stent placement for the treatment of a benign ureteral obstruction in a Sumatran tiger (Panthera tigris sumatrae). Zoo Biol 2015;34:193–7. 26. Kuntz JA, Berent AC, Weisse CW, et al. Double pigtail ureteral stenting and renal pelvic lavage for renal-sparing treatment of obstructive pyonephrosis in dogs: 13 cases (2008-2012). J Am Vet Med Assoc 2015;246:216–25. 27. Culp WTN, Palm C, Hsueh C, et al. A comparison of perioperative outcome in cats undergoing ureterotomy or ureteral stenting for the treatment of benign ureteral obstructions. J Vet Intern Med 2015;29:1213. 28. Johnson CM, Culp WT, Palm CA, et al. Subcutaneous ureteral bypass device for treatment of iatrogenic ureteral ligation in a kitten. J Am Vet Med Assoc 2015;247: 924–31.
DVM
a
, William T.N. Culp,
b, VMD *
KEYWORDS Interventional radiology Interventional urology Stent Subcutaneous ureteral bypass Nephroureterolithiasis Ureteral obstruction KEY POINTS The treatment of benign nephroureteral obstructions is challenging and often involves a combination of medical and surgical/interventional therapeutic options. Historical surgical treatments of nephroureteral obstructions have demonstrated varying results; however, newer interventional radiology therapies, such as stent and subcutaneous ureteral bypass system placement, are being used more commonly. The indications for the placement of stents and subcutaneous ureteral bypass systems still need to be fully elucidated, but early results are showing promise.
INTRODUCTION
Canine and feline nephroureteral obstruction is a complex disease process that can be challenging to treat. Although the availability of various imaging modalities allows for a straightforward diagnosis to be made in most cases, the decision-making process for when a case should be taken to surgery, as well as the optimal treatment modality that should be used for renal decompression, remains controversial. In the following discussion, an overview of the perioperative management of cases with nephroureterolithiasis and nephroureteral obstruction is reviewed, with a focus on the use of renal decompressive procedures, such as ureteral stenting and subcutaneous ureteral bypass (SUB) system placement. The authors teach laboratories where some of the instrumentation discussed in this article are utilized. a Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, One Garrod Drive, Davis, CA 95616, USA; b Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, One Garrod Drive, Davis, CA 95616, USA * Corresponding author. Veterinary Medical Teaching Hospital, University of California-Davis, One Garrod Drive, Davis, CA 95616. E-mail address: [email protected] Vet Clin Small Anim 46 (2016) 1183–1192 http://dx.doi.org/10.1016/j.cvsm.2016.06.008 vetsmall.theclinics.com 0195-5616/16/$ – see front matter Ó 2016 Elsevier Inc. All rights reserved.
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Diagnosis
To effectively diagnose, treat, and manage patients with benign upper urinary tract obstructions, it is important to try and identify the underlying causes for these obstructions. The diagnosis of nephroliths and ureteroliths has increased over the last few decades because of advancements in diagnostic imaging and client and clinician education. In cats, nephroliths and ureteroliths are most commonly composed of calcium oxalate1–3; however, other stone types, including dried solidified blood calculi and struvite stones,1,4 are also found. It is also important to note that in many cases of feline ureteral obstruction discrete calculi may not be identified. In these cases, it is likely that ureteritis, scarring from previous inflammation, and/or cellular or crystalline debris may be the cause of obstruction. Identifying the underlying cause for ureteral obstruction will help to guide the optimal treatment plan as well as long-term medical management after renal decompression has been performed. A serum biochemistry profile should be performed in any dog or cat suspected of having an upper urinary tract obstruction. Most cats with ureteroliths have been shown to be azotemic,3,5 even when unilateral ureteral obstruction is present. This finding emphasizes the fact that a large percentage of cats have preexisting chronic kidney disease (often times from a previous obstruction of the contralateral kidney) before diagnosis of obstruction. Evaluating the severity of azotemia, in addition to electrolytes, such as potassium, can help to guide whether patients should be taken to surgery on an emergency basis. The severity of azotemia (in conjunction with diagnostic imaging) also provides information regarding the degree of underlying chronic kidney disease that is present, a variable that may guide an owner’s decision to pursue surgical intervention. The decision to pursue surgical intervention is not always straightforward, especially in nonazotemic patients that may appear clinically healthy. With the discovery of newer biomarkers of early kidney injury and dysfunction that are much more sensitive than creatinine, earlier diagnosis of and intervention for ureteral obstruction may become possible.6,7 The complete blood count often demonstrates anemia in cats with ureteral obstruction; in some cases, this may indicate the presence of longer-standing chronic kidney disease.3,5 Additionally, the presence of an inflammatory leukogram may suggest an underlying infection associated with the presence of a stone or as the sole cause for the obstruction (ie, ureteritis). Urinalysis and urine culture should be performed in all patients affected with nephroureterolithiasis. Assessment of urine pH may be useful in differentiating between stone types. Sediment evaluation can help to identify the presence of bacteria and pyuria. In dogs, struvite stones are most commonly associated with urease-producing bacteria (ie, Staphylococcus, Proteus, Klebsiella). The presence of these bacteria should raise the clinician’s suspicion for the presence of a struvite stone. If a partial ureteral obstruction is present (and the ureteral stone is, therefore, bathed in urine), it is possible that medical management could be used as the sole treatment; however, concurrent ureteral stent placement may be necessary (see later discussion). In the authors’ experience, sterile pyuria is found commonly in patients with ureteral obstruction, likely due to the inflammatory processes that are initiated soon after development of ureteral obstruction. Nonetheless, a urine culture should be performed in all patients with ureteral obstruction. In patients with complete ureteral obstruction, or in anuric patients, a sample of renal pelvic urine can be taken for culture if patients are undergoing surgical decompression. Abdominal ultrasound should be performed in all cases of suspected nephroureteral obstruction. Ultrasound is the primary imaging method used for diagnosis of ureteral
Stents and Ureteral Bypass Systems for Renal Decompression
obstruction; however, it is important to note that ureteral obstruction can be missed in early obstruction, partial obstruction, and in patients that are dehydrated or hypovolemic at the time of evaluation. As discussed earlier, ultrasound can be used to evaluate for chronic changes in the kidneys and can also be used as a monitoring tool for changes in renal pelvic and ureteral diameters that can either indicate spontaneous renal decompression (without surgical intervention) or progressive dilation, indicating a need for surgical intervention. Ultrasound can also be used to visualize stones and other obstructing debris in the kidney and ureter.3 In the authors’ practice, ultrasound is commonly used to monitor response to therapy by evaluating renal pelvic and ureteral size after intervention. In patients with ureteral obstruction, plain abdominal radiographs can be used to complement ultrasound. The sensitivity of radiographs in the identification of ureteral calculi has been shown to be 81%.3 Additionally, in severe cases, hydroureter can also be diagnosed on survey abdominal radiographs. Many surgeons value the use of abdominal radiographs before surgery, as the number and location of stones can often be identified. Fluoroscopy is often used during renal decompression surgery. During these procedures, nephrocentesis is performed to allow for contrast medium injection. During and after contrast medium administration, fluoroscopy is performed to evaluate the degree of hydronephrosis, the location and course of the ureter, and the location of ureteral obstruction. Although performed uncommonly at the authors’ institution, preoperative antegrade nephropyelograms can also be performed with the use of fluoroscopy in cases where diagnosis of obstruction is not straightforward. In veterinary medicine, advanced cross-sectional imaging, including computed tomography (CT) and MRI, is not commonly used in the assessment of patients with nephroureteral obstruction. These imaging modalities provide high-quality, detailed images of the upper urinary tract, including identification of kidney and ureteral size, and the presence of calculi. When more traditional surgeries, such as ureterotomy without stent placement, are performed, CT can be useful for identification of multiple ureteral stones, so that all stones can be addressed at the time of surgery; however, results of these advanced imaging techniques do not typically impact the clinical decision-making when newer minimally invasive techniques (eg, stents and SUBS) are used. In addition, increases in intra-renal pressures secondary to nephroureteral obstruction can prevent contrast uptake by the kidneys and obscure diagnostic results. Decision-making
The decision-making process for optimal treatment timing and modality for cases affected with nephroureteral obstruction is impacted by several factors. Nephroliths that are not causing clinical signs and have been found incidentally are generally monitored without intervention. If patients are experiencing chronic urinary tract infections or the nephrolith has grown large enough to obstruct urine outflow from the renal pelvis, removal can be considered. If a stent or SUB system can be placed to allow urine to flow from the renal pelvis to the bladder in these cases, surgical removal of the nephroliths may not be required. In cases whereby patients are oliguric or anuric secondary to a ureteral obstruction, intervention is mandatory. Historically, treatment options for these cats included stabilization with hemodialysis (if indicated and available), followed by ureterotomy or other traditional ureteral surgery. In the authors’ practice, when a ureteral obstruction is highly suspected or confirmed with imaging, surgery is performed as the first-line
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therapy in nearly every case. As hemodialysis only provides temporary stabilization in this scenario and requires patients to be anticoagulated, performing this procedure before surgery is generally not indicated and may lead to the need for postponement of surgery. The need for systemic anticoagulation can be avoided with the use of extracorporeal citrate anticoagulation. With immediate and aggressive medical management, however, it is the authors’ experience that almost every patient can be stabilized for surgery without instituting hemodialysis. In patients with ureteral calculi that are nonobstructive (ie, no evidence of ureteral dilation or hydronephrosis), intervention to remove or bypass the calculi is generally not indicated, especially given the potential morbidity. However, serial monitoring of these patients with blood work and abdominal ultrasound is recommended, as unilateral obstruction can occur with minimal to no clinical signs present. Serial creatinine trending for each individual patient and the use of newer biomarkers may allow for earlier diagnosis in patients with unilateral ureteral obstruction. In stable patients (ie, no electrolyte derangements and no overhydration) with ultrasonographic evidence of ureteral obstruction, medical management can be considered, although, in the authors’ hands, this is often unsuccessful. The decision to pursue surgical intervention is not always straightforward, especially in nonazotemic patients that may appear clinically healthy. Significant renal injury develops within hours after ureteral obstruction and prolonged obstruction leads to progressive inflammation and fibrosis, which will ultimately develop into chronic kidney disease that will remain after renal decompression. Given this, along with the risk for contralateral obstruction to develop over time and the high incidence of chronic kidney disease (especially in feline patients), preservation of as much renal function via early surgical intervention is likely indicated in many cases. Once the decision to pursue renal decompression is made, there are several factors that play a role in selecting the optimal surgery type for each case. These factors include surgeon expertise and comfort with each procedure as well as availability of equipment (eg, stents, SUBs, fluoroscopy, surgical microscope). The focus of this article is on the use of stents and SUBs for renal decompression, but it is important to note that some clinicians still prefer to manage patients with ureteral obstruction with traditional surgery techniques. The authors prefer ureteral stenting in dogs experiencing ureteral obstruction secondary to urolithiasis, as these stents can be placed minimally invasively (percutaneous or endoscopic guided) and removed minimally invasively and are generally well tolerated. Stents can be exchanged when partial migration or blockage occurs, and often this can be performed without performing a celiotomy. The placement of a SUB system is considered in cases with known ureteral strictures, circumcaval ureters (Fig. 1), when stents cannot be placed successfully, and when stents have not been tolerated by patients.8 Treatment
As stated earlier, this discussion focuses on the use of stents and SUB systems in the treatment of ureteral obstructions in dogs and cats. Different considerations need to be made for dogs as compared with cats, and these are discussed later. In addition, the limited amount of available literature is discussed later, but it is important to note that continued scientific evaluation of outcomes with the different surgery types is warranted so that the best treatment decisions can be made for veterinary patients. Ureteral stenting
Ureteral stents (also called ureteric stents) are tubes placed into the ureter to allow for urine to flow from the kidney (renal pelvis) to the bladder. Additionally, stents can be
Stents and Ureteral Bypass Systems for Renal Decompression
Fig. 1. (A) Intraoperative image of a 12-year-old female spayed domestic longhair. A right circumcaval ureter is seen here. (B) To treat a ureteral obstruction in this case, an SUB system has been placed.
placed as a means of splinting a ureter that has been anastomosed after a surgical incision or trauma.9,10 Ureteral stents have been shown to stimulate ureteral dilation.11 Ureteral stents can be made of various materials; but currently, there are 3 major categories: polymeric compounds, metal, and biodegradable.12–14 Although each stent type has its own advantages, no single ureteral stent is perfect. In human patients undergoing stent placement, morbidity is reported in up to 80% of cases15,16; therefore, an emphasis has been placed on the development of new stents.13 Although complications can occur in dogs and cats with ureteral stents, the tolerance of stents tends to be better than in humans. The use of ureteral stents for treatment of both benign and malignant ureteral obstructions has been described in several veterinary studies.5,17–24 The most commonly reported indications for ureteral stenting in dogs and cats have been for treatment of benign obstructions with calculi or strictures.18,19,21,23 Ureteral stents can be placed in dogs and cats using several different techniques. A percutaneous technique has been described in the treatment of malignant ureteral obstructions in dogs24; but a description of this technique for benign obstructions is lacking in veterinary patients, except for an isolated report in a tiger.25 To perform this technique, ultrasound guidance is used to visualize the renal pelvis and percutaneous nephrocentesis is performed. A guidewire is then passed through the renal access needle and manipulated through the ureter and into the bladder and urethra with fluoroscopic guidance. This technique allows for retrograde placement (from the urethra and into the kidney) of the stent over the guidewire. Antegrade placement can also be performed with use of a sheath placed percutaneously through the nephrocentesis
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puncture site into the renal pelvis. In the authors’ practice, percutaneous stent placement is generally considered only in canine patients, as it has not been successful in cats. Both antegrade and retrograde placement of stents can be performed in dogs and cats after a celiotomy. The authors prefer antegrade placement of ureteral stents, as this allows for through-and-through guidewire access (ie, the guidewire can be grasped outside of the entry point into the kidney and at the exit point from the bladder). This technique has been described in veterinary studies.17–19 After performing a ventral midline celiotomy, the affected kidney is isolated by draping the other abdominal organs away and dissecting perirenal fat as necessary. A 22-gauge over-the-needle catheter is introduced into the greater curvature of the kidney aiming toward the ureteral-pelvic junction; generally, this is a location that is equidistant dorsal-ventral and cranial-caudal on the greater curvature. When urine is obtained from the over-the-needle catheter, the needle is removed and the catheter is left in the renal pelvis. A T-port that had been primed with a 50%/50% mixture of saline/iodinated contrast is attached to the catheter and the renal pelvis is filled under fluoroscopic guidance. Fluoroscopy confirms the presence of the catheter within the renal pelvis. A 0.018-in hydrophilic guidewire is then introduced into the catheter and passed antegrade down the ureter and into the bladder. A cystotomy is performed, and the wire is grasped from the bladder and passed externally (out of the bladder). The catheter is removed over the guidewire. A ureteral dilator is then passed normograde over the guidewire through the renal parenchyma into the renal pelvis and through the ureter until it is exits through the ureterovesicular junction (UVJ). The dilator is then removed, and a ureteral stent is passed over the guidewire. The cranial pigtail of the stent is positioned within the renal pelvis using fluoroscopic guidance. When placement is confirmed, the guidewire is removed normograde from the stent allowing a pigtail to form in the bladder. One study evaluated 12 cats that underwent antegrade placement of ureteral stents. Nine cats underwent unilateral stent placement, and 3 cats received bilateral stents.19 A ureterotomy was required in 3 cats, and 4 cats required ureteral resection and anastomosis to allow for stent placement. Of the 12 cats treated in that study, 11 were discharged and all cats demonstrated improvement in azotemia. Postoperatively, serum creatinine and renal pelvic size improved significantly when compared with preoperative values.19 In the largest study to date, the antegrade technique was the preferred approach by the authors, although other techniques were also described.18 In that study, ureteral stent placement, using a newer stent device specifically designed for cats, was successful in 52 of 53 (98%) cats.18 Complications occurring during the procedure, immediately postoperative, and in the short-term occurred in less than 10% of cases; long-term complications occurred in 33% of cats, although most were considered minor.18 Retrograde stent placement can also be performed with the use of endoscopy or during an open abdominal approach after cystotomy.18,22,26 Endoscopic ureteral stent placement is the preferred technique by the authors for treating benign ureteral obstructions in dogs (Fig. 2). In one study, retrograde ureteral stenting was attempted in the treatment of obstructive ureterolithiasis with secondary pyonephrosis in 13 dogs.26 The procedure was successfully performed with cystoscopic and fluoroscopic guidance in 11 of 13 dogs. Long-term complications were uncommon and included stent encrustation, stent migration, and tissue proliferation at the UVJ. Overall, the procedure was determined to be effective.26 Retrograde ureteral stents placed with endoscopy has also been reported in feline cases, although this is rarely performed.17,18
Stents and Ureteral Bypass Systems for Renal Decompression
Fig. 2. (A) Cystourethroscopic view of the left ureteral orifice. A hydrophilic guidewire has been introduced into the left ureter using cystoscopy. (B) Ventrodorsal fluoroscopic image. The guidewire (black arrow) has been passed into the renal pelvis. (C) Ventrodorsal fluoroscopic image. A ureteral stent (tip marked by yellow arrow) is being passed retrograde into the ureter over the guidewire. (D) Ventrodorsal fluoroscopic image: after placement of the ureteral stent, the guidewire has been removed; the pigtails of the stent can be seen in the renal pelvis and bladder.
For retrograde ureteral stenting performed with cystoscopic and fluoroscopic guidance, patients are placed in dorsal recumbency and cystourethroscopy is performed. Once the UVJ has been identified, a hydrophilic guidewire is introduced through the working channel of the cystoscope and passed into the ureter and past the obstruction into the renal pelvis. Once in the renal pelvis, the guidewire is formed into a curl to prevent backing out. An open-ended ureteral catheter is introduced over the guidewire to allow for nephropyelography and stent sizing. Once a nephropyelogram has been performed, the guidewire is reintroduced into the ureteral catheter and the catheter is removed. A ureteral stent is then introduced over the guidewire (through the working channel of the scope) and into the ureter until the cranial pigtail can be visualized over the leading end of the guidewire. The guidewire is withdrawn while the cystoscope is positioned within the bladder to direct the caudal aspect of the stent (still in the working channel) into the bladder with a ureteral pusher catheter.
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The retrograde placement of ureteral stents has also been described in cats after performance of a celiotomy.17,18 This procedure is performed similar to the endoscopic technique after a cystotomy has been performed to expose the UVJ. With this technique, a cystoscope is not used and the caudal pigtail of the stent is manually placed in the bladder after placement of the cranial pigtail in the renal pelvis. Descriptions of stent placement through ureterotomy sites or after ureteral resection have been reported.17,21 In these cases, a guidewire is introduced into the ureterotomy site or up the open end of the ureter. Dilation is performed when possible, and stents are generally placed in retrograde fashion. Stents can also be placed to support anastomoses that have been performed during stone removal or after trauma.5,17 Traditional ureteral surgery has been compared with ureteral stenting in the treatment of ureteral obstruction in 2 recent studies.5,27 In one study,5 the occurrence of lower urinary tract signs and urinary tract infections was significantly higher in those cases that received a ureteral stent as compared with those that did not.5 In a separate study, cats that underwent ureteral stent placement had significantly greater decreases in blood urea nitrogen and creatinine 1-day postoperatively and at discharge as compared with cats that underwent ureterotomy without stent placement. Additionally, in that study, cats that underwent ureteral stent placement were significantly more likely to have resolution of azotemia in-hospital.27 The short-term outcome associated with ureteral stents is considered good, as most treated dogs and cats survive to discharge from the hospital; in addition, improvement in azotemia and ultrasonographic findings occurs regularly.17,18,20,23,26,27 Long-term complications associated with ureteral stent placement have been described in several studies.5,17–21,23 Dysuria, hematuria, and stranguria have been noted to occur in cats after stent placement5,18; in one study, dysuria was noted in 37% of cats.18 Additionally, stents need to be exchanged or replaced in up to 27% of cases because of stent migration, fracture, encrustation, obstruction, or lower urinary tract signs that are refractory to medical management.5,17,18 Ureteral bypass
The placement of ureteral bypass systems (in particular the SUB) has become more commonplace in companion animals over the last several years. The concept of the SUB system is that a nephrostomy tube and cystostomy tube are placed permanently and connected via a shunting port. Urine can then flow through the attached catheters and is delivered into the bladder. The veterinary literature on the topic is currently limited to 2 case series8,20 and 1 case report.28 Early results associated with the SUB system placement are promising. In a study evaluating both stents and SUBs for the treatment of benign ureteral obstructions in cats, all cases had successful decompression of the renal pelvis postoperatively and survival was considered good.20 In a separate study, a SUB system was used in the treatment of cats with both circumcaval and noncircumcaval ureters, of which most cases had ureterolithiasis.8 In that groups of cats, the SUB system was shown to reobstruct less commonly than ureteral stents.8 The placement of the SUB system is performed after a ventral midline celiotomy. An 18-gauge over-the-needle catheter is inserted into the caudal pole of the kidney equidistant ventral-dorsal and directed to the renal pelvis. Similar to ureteral stent placement, nephropyelography is performed. A 0.035-in guidewire is then placed into the 18-gauge catheter and coiled in the renal pelvis. The 18-gauge catheter is removed over the guidewire. A 6.5F pigtail locking-loop nephrostomy tube is placed over the
Stents and Ureteral Bypass Systems for Renal Decompression
guidewire into the renal pelvis and secured to the renal capsule with tissue glue. A 7F cystostomy tube is then inserted into the bladder and secured to the bladder with sutures. The tube ends of both the nephrostomy and cystostomy tubes are tunneled through the body wall and attached to a titanium shunting port that is secured to the body wall. Proposed benefits of SUB system placement include the fact that ureteral surgery is not required, the cystostomy tube enters at the bladder apex (and not through the UVJ as is the case with stents), and flushing of the SUB system can be done, to possibly prevent obstruction of the tubing. REFERENCES
1. Cannon AB, Westropp JL, Ruby AL, et al. Evaluation of trends in urolith composition in cats: 5,230 cases (1985-2004). J Am Vet Med Assoc 2007;231:570–6. 2. Low WW, Uhl JM, Kass PH, et al. Evaluation of trends in urolith composition and characteristics of dogs with urolithiasis: 25,499 cases (1985-2006). J Am Vet Med Assoc 2010;236:193–200. 3. 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;226:932–6. 4. Westropp JL, Ruby AL, Bailiff NL, et al. Dried solidified blood calculi in the urinary tract of cats. J Vet Intern Med 2006;20:828–34. 5. 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; 248:518–25. 6. Palm CA, Segev G, Cowgill LD, et al. Urinary neutrophil gelatinaseassociated lipocalin as a marker for identification of acute kidney injury and recovery in dogs with gentamicin-induced nephrotoxicity. J Vet Intern Med 2016;30:200–5. 7. Hokamp JA, Nabity MB. Renal biomarkers in domestic species. Vet Clin Pathol 2016;45:28–56. 8. 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;29:63–70. 9. Chew BH, Lange D. Advances in ureteral stent development. Curr Opin Urol 2016;26:277–82. 10. Wormser C, Clarke DL, Aronson LR. End-to-end ureteral anastomosis and double-pigtail ureteral stent placement for treatment of iatrogenic ureteral trauma in two dogs. J Am Vet Med Assoc 2015;247:92–7. 11. Lennon GM, Thornhill JA, Grainger R, et al. Double pigtail ureteric stent versus percutaneous nephrostomy: effects on stone transit and ureteric motility. Eur Urol 1997;31:24–9. 12. Fiuk J, Bao Y, Calleary JG, et al. The use of internal stents in chronic ureteral obstruction. J Urol 2015;193:1092–100. 13. Brotherhood H, Lange D, Chew BH. Advances in ureteral stents. Transl Androl Urol 2014;3:314–9. 14. Auge BK, Preminger GM. Ureteral stents and their use in endourology. Curr Opin Urol 2002;12:217–22. 15. Joshi HB, Stainthorpe A, MacDonagh RP, et al. Indwelling ureteral stents: evaluation of symptoms, quality of life and utility. J Urol 2003;169:1065–9.
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16. Joshi HB, Newns N, Stainthorpe A, et al. Ureteral stent symptom questionnaire: development and validation of a multidimensional quality of life measure. J Urol 2003;169:1060–4. 17. Kulendra NJ, Syme H, Benigni L, et al. Feline double pigtail ureteric stents for management of ureteric obstruction: short- and long-term follow-up of 26 cats. J Feline Med Surg 2014;16:985–91. 18. 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;244:559–76. 19. Manassero M, Decambron A, Viateau V, et al. Indwelling double pigtail ureteral stent combined or not with surgery for feline ureterolithiasis: complications and outcome in 15 cases. J Feline Med Surg 2013;16:623–30. 20. 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;15:1052–62. 21. Nicoli S, Morello E, Martano M, et al. Double-J ureteral stenting in nine cats with ureteral obstruction. Vet J 2012;194:60–5. 22. Lam NK, Berent AC, Weisse CW, et al. Endoscopic placement of ureteral stents for treatment of congenital bilateral ureteral stenosis in a dog. J Am Vet Med Assoc 2012;240:983–90. 23. Zaid MS, Berent AC, Weisse C, et al. Feline ureteral strictures: 10 cases (20072009). J Vet Intern Med 2011;25:222–9. 24. Berent AC, Weisse C, Beal MW, et al. Use of indwelling, double-pigtail stents for treatment of malignant ureteral obstruction in dogs: 12 cases (2006-2009). J Am Vet Med Assoc 2011;238:1017–25. 25. Delk KW, Wack RF, Burgdorf-Moisuk A, et al. Percutaneous ureteral stent placement for the treatment of a benign ureteral obstruction in a Sumatran tiger (Panthera tigris sumatrae). Zoo Biol 2015;34:193–7. 26. Kuntz JA, Berent AC, Weisse CW, et al. Double pigtail ureteral stenting and renal pelvic lavage for renal-sparing treatment of obstructive pyonephrosis in dogs: 13 cases (2008-2012). J Am Vet Med Assoc 2015;246:216–25. 27. Culp WTN, Palm C, Hsueh C, et al. A comparison of perioperative outcome in cats undergoing ureterotomy or ureteral stenting for the treatment of benign ureteral obstructions. J Vet Intern Med 2015;29:1213. 28. Johnson CM, Culp WT, Palm CA, et al. Subcutaneous ureteral bypass device for treatment of iatrogenic ureteral ligation in a kitten. J Am Vet Med Assoc 2015;247: 924–31.