Small Animals & Exotic

Surgical management of vesicoureteral reflux with recurrent urinary tract infection after renal transplantation in a dog CASE DESCRIPTION A 3-year-old male Cocker Spaniel renal transplant recipient was readmitted 39 weeks after transplantation because of acute clinical signs of pollakiuria, intermittent vomiting, decreased appetite, lethargy, and mild fever.

Kyung-Mee Park DVM, PhD Hyun-Suk Nam DVM, PhD Kamal Hany Hussein DVM Heung-Myong Woo DVM, PhD From the Section of Veterinary Surgery, College of Veterinary Medicine, and the Stem Cell Institute-KNU, Kangwon National University, Chuncheon, Republic of Korea, 200-701. Address correspondence to Dr. Heung-Myong Woo ([email protected]).

CLINICAL FINDINGS Hydronephrosis and hydroureter were observed with ultrasonography and contrast cystography, and a diagnosis of vesicoureteral reflux (VUR) was made. Urinary tract infection (UTI) caused by Escherichia coli was also diagnosed on the basis of results of urine culture. TREATMENT AND OUTCOME Despite treatment of the UTI with an appropriate antimicrobial for 6 weeks, the VUR persisted and the UTI recurred 9 weeks after cessation of antimicrobial treatment. Therefore, surgical correction by means of revision extravesicular ureteroneocytostomy was performed. Both VUR and hydronephrosis resolved after surgery. No recurrences of clinical signs of urinary tract complications were observed during the subsequent 22-month follow-up period. CLINICAL RELEVANCE Results suggested that ureteral reimplantation with an extravesicular technique incorporating a long submucosal tunnel may be an effective treatment for VUR when medical management fails in canine renal transplant recipients with recurrent UTIs. (J Am Vet Med Assoc 2016;248:309–314)

A

3-year-old 7.8 kg (17.2 lb) male Cocker Spaniel was referred to the Kangwon National University Veterinary Teaching Hospital for renal transplantation because of chronic renal failure. Renal failure had been diagnosed at a local veterinary hospital 10 months prior to referral, and the dog had failed to respond to supportive care, including feeding a commercial diet. a At admission, the dog had a body condition score of 4 on a scale from 1 to 9, severe azotemia (serum creatinine concentration, 6.2 mg/dL; BUN concentration, 210 mg/dL), and oliguria. Bilateral small hyperechoic kidneys with an unclear corticomedullary junction were evident on ultrasonography. Hemodialysis was performed with a dialysis machine b and a cellulose hollow fiber hemodialyzer c at a rate of 20 mL/min for 120 minutes via the jugular vein. The owners provided a samebreed healthy donor dog from an acquaintance, and informed consent was obtained for all proABBREVIATIONS UTI Urinary tract infection VUR Vesicoureteral reflux

cedures. Preoperative examination of the donor and recipient dogs consisted of a CBC, serum biochemical analyses, urinalysis, urine culture, heartworm antigen test, indirect (noninvasive) blood pressure monitoring, transabdominal ultrasonography, and abdominal radiography (dorsoventral and ventrodorsal views). Blood typing, erythrocyte crossmatching, and complementdependent cytotoxic crossmatching were performed according to previously described renal transplantation protocols. 1 Serologic testing for tick-borne diseases and leptospirosis was not performed because the donor and recipient dog were indoor dogs, were vaccinated annually including leptospirosis, and were treated monthly with a parasiticide. d,e The recipient dog was premedicated with butorphanol f (0.4 mg/kg [0.18 mg/lb], IM) and atropine sulfate g (0.04 mg/kg [0.018 mg/lb], SC) for surgery. Anesthesia was induced with propofol h (4 mg/kg [1.8 mg/lb], IV) and maintained with isoflurane i in oxygen. Ventilation was controlled with a volume-controlled ventilator. During surgery, an ECG, oxygen saturation, a capnogram, blood pressure, and body temperature

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were monitored. The renal artery of the donor kidney was anastomosed end-to-end with the iliac artery of the recipient, and the renal vein was anastomosed end-to-side with the iliac vein with 7-0 polypropylene. j The ureteroneocytostomy was performed by means of an extravesicular technique with a submucosal tunnel that provided an approximate 3:1 tunnel length-to-ureteral diameter ratio in accordance with a previously described technique. 2 Three immunosuppressants—cyclosporine k (20 mg/kg [9.1 mg/lb], PO, q 24 h), prednisolone l (1 mg/kg [0.45 mg/lb], PO, q 24 h), and azathioprine m (5 mg/kg [2.3 mg/lb], PO, q 48 h)—were administered to prevent graft rejection according to a previously described protocol. 1 Cefazolin n (22 mg/kg [10 mg/lb], IV, q 12 h) was administered for 5 days after surgery as antimicrobial prophylaxis. The recipient dog recovered well and was discharged from the hospital 1 week after surgery without any evidence of postoperative complications. After discharge, the recipient dog was evaluated once per week for the first 6 weeks and then monthly for 6 months, and the dog’s condition was stable. At each examination, a physical examination, CBC, serum biochemical analyses, and urinalysis were performed and cyclosporine concentration was measured. At 39 weeks after transplantation, the recipient dog was readmitted with acute clinical signs of pollakiuria, intermittent vomiting, decreased appetite, and lethargy. A physical examination revealed a body condition score of 4 and a mild fever (39.4°C [102.9°F]); however, a CBC and serum biochemical analyses did not reveal any abnormalities except a neutrophil count (14.3 X 10 3 neutrophils/µL; reference range, 4 X 10 3 neutrophils/µL to 15.5 X 10 3 neutrophils/µL) in the upper end of the reference range. On an ultrasonographic examination, hydroureter (ureteral diameter, 4 to 6.5 mm) and hydronephrosis (transverse diameter of renal pelvis, 20 to 22 mm; ventrodorsal diameter of renal pelvis, 2 to 6 mm; width of renal pelvis, 8 mm) of the grafted kidney were observed (Figure 1). 310

Figure 1—Ultrasonographic appearance of the abdomen in a 3-year-old 7.8-kg (17.2 lb) male Cocker Spaniel renal transplant recipient that was readmitted 39 weeks after transplantation because of acute clinical signs of pollakiuria, intermittent vomiting, decreased appetite, lethargy, and mild fever. The proximal (A; arrow) and distal (B; white arrows) sections of the ureter near the bladder (black arrow) are dilated. Mild hydronephrosis (arrow) can be seen in the pelvic region in transverse (C) and sagittal (D) views of the transplanted kidney.

Figure 2—Ventrodorsal (A) and lateral (B) views of the abdomen of the dog in Figure 1 obtained during positive-contrast cystography. The renal pelvis (arrowhead) and ureter (black arrow) are filled with contrast medium, indicative of VUR. The urinary bladder (white arrow) can also be seen.

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leukocytes or bacteria were detected in the urine, and the clinical signs resolved; however, VUR and pyeloureteral dilatation persisted during the antimicrobial treatment period. The E coli–induced UTI recurred 9 weeks after cessation of cephradrine treatment. Ureteral reimplantation was performed to treat the VUR and limit additional renal damage (Figure 3). Prior to revision surgery, cefazolin was administered (22 mg/kg, IV, q 12 h) for a week to treat the UTI and alleviate the clinical signs. The dog was anesthetized with the previously described protocol. For ureteral reimplantation, the distal portion of the grafted ureter adjacent to the bladder was ligated with 3-0 silk and transected. An incision that was 5 times the ureteral diameter was created in the bladder seromuscular layer, and a small caudal mucosal incision was made. The spatulated ureteral mucosa was sutured to the bladder mucosa by means of an end-to-side anastomosis with 7-0 polypropylene in a simple continuous pattern. The ureteral tunnel was created by suturing the bladder seromuscular layer with simple interFigure 3—Intraoperative photographs obtained during ureteral reimplantation rupted 4-0 polypropylene sutures. in the dog in Figure 1. The grafted kidney (black arrow) in the iliac fossa and bladder (white arrow) are shown (A). The implanted ureter (white arrow) was tied The length of the tunnel was apwith 2-0 silk and dissected from the bladder (B and C). The spatulated ureteral proximately 5 times the inner diammucosa (white arrow) was anastomosed with the bladder mucosa (black arrow) eter of the ureteral orifice, as recwith simple continuous sutures (D and E). A seromucosal tunnel approximately ommended for human patients. 3,4 5 times the diameter of the ureteral orifice was made by suturing the bladder Recovery from anesthesia was unseromuscular layer in a simple interrupted pattern (F). complicated. For analgesia, butorphanol (0.2 mg/kg [0.09 mg/lb], IM, q 6 h) and tramadol q (1 mg/kg, IV, q 6 h) were given for 3 days after the surgery. Cephradine (25 mg/ Positive contrast cystography was performed by kg, PO, q 12 h) was administered for 6 weeks on filling the bladder with warm contrast medium, o the basis of results of antimicrobial susceptibiland retrograde urine f low through the dilated ity testing of the E coli strain recovered at the ureter into the renal pelvis was observed (Figtime the recurrent UTI was diagnosed. A physiure 2). A urine sample obtained by means of cyscal examination, ultrasonography, CBC, serum tocentesis and blood samples were submitted for biochemical analyses, and urinalysis were perbacterial culture and antimicrobial susceptibility formed weekly for the first 2 months after surtesting. A renal transplant biopsy was not pergery, then monthly for the subsequent 4 months, formed because of concerns of iatrogenic graft and then every 3 to 4 months. damage. The hydronephrosis and hydroureter reAn Escherichia coli strain was isolated from the solved within a week after ureteral reimplantaurine sample, but results of aerobic and anaerobic tion (Figure 4), and contrast medium did not bacterial culture of blood samples were negative. ref lux into the renal pelvis or ureter. The dog The UTI was treated with cephradinep (25 mg/kg had no further episodes of UTI after cessation of [11.4 mg/lb], q 12 h, PO) for 6 weeks on the baantimicrobial treatment, and renal function was sis of results of antimicrobial susceptibility testing. maintained during the subsequent 22 months of The UTI responded to antimicrobial treatment. No follow-up. JAVMA • Vol 248 • No. 3 • February 1, 2016

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been reported in human patients13–15; however, insufficiency of these data has made it difficult to apply the information to clinical canine renal transplant patients. Vesicoureteral reflux frequently occurs after renal transplantation in humans, and the incidence may be as high as 86%16,17; however, recurrent UTI with VUR is rare (0% to 2%) in human patients.13 The incidence of VUR following renal transplantation in dogs has not been reported. The mean time reported for a diagnosis of VUR after renal transplantation in humans is 9 months (range, 2 to 23 months).18 In the dog of the present report, signs of VUR were evident 39 weeks after surgery. Management of VUR is critical in renal transplant recipients because this complication can induce chronic recurrent UTIs, pyelonephritis, graft damage, and even renal failure.19,20 However, an effective management protocol for VUR after renal transplantation has not been described in dogs. In the present report, we described surgical correction of VUR by means of ureteral reimplantaFigure 4—Transverse (A) and sagittal (B) ultrasonographic and ventrodorsal (C) tion in a canine renal transplant recipiand lateral (D) positive-contrast cystographic views of the dog in Figure 1 obtained ent with recurrent UTIs. following ureteral reimplantation. Notice on the ultrasonographic images that the Vesicoureteral reflux is highly ashydronephrosis has resolved and on the cystographic images that VUR is no longer sociated with UTI in children,21–23 and present. management of VUR is recommended to decrease the risk of UTI and renal damage.24 The severity of VUR can be Discussion classified according criteria developed for the International Reflux Study in Children25 as follows: grade Renal transplantation is one of the most difficult I, results in urine reflux into the ureter only; grade II, clinical challenges in veterinary patients and has results in urine reflux into the ureter and the renal high mortality and morbidity rates associated with pelvis without dilation; grade III, results in urine reflux 5,6 various postsurgical complications in dogs. Meinto the ureter and the renal pelvis, causing mild to dian survival time of clinical renal transplant cases moderate dilation of the ureter and renal pelvis; grade has been reported to be as low as 24 days (range, IV, results in moderate hydronephrosis; and grade V, re0.5 to 4,014 days), with a 100-day survival probabilsults in severe hydronephrosis and tortuosity of the ity rate of 36%.5 However, other studies7–10 of renal ureter. According to this grading system, the dog detransplantation in dogs found longer survival times scribed in the present report had grade III VUR. In huof 7 months to > 5 years, likely because dogs used man patients, a conservative nonoperative approach in those studies were healthy and histocompatibilitywith prophylactic antimicrobial administration to prematched donors and recipients were used in some vent UTI and renal scarring is the initial approach for studies. Because of aggressive rejection episodes, grades I to III VUR because mild-to-moderate VUR has dogs show poorer outcomes after renal transplantabeen found to have a high rate of spontaneous resolution, compared with feline and human patients.5 To tion in pediatric patients.26 In patients with grade III overcome severe immune rejection, intensive immuto IV VUR, medical management is appropriate, with nosuppression is needed but unfortunately causes disurgical intervention indicated for patients with reverse complications.Thromboembolism is one of the current UTIs. In patients with grade V VUR, surgical leading causes of death in recipient dogs, and other repair may be required because of the low incidence complications such as secondary infection, intestinal of spontaneous resolution. intussusception, lymphoma, and gingival overgrowth Recently, an endoscopic approach with a dextrahave been reported in previous studies.1,5,11,12 nomer-hyaluronic acid polymer has been successfully A number of urinary complications after renal used for treatment of mild-to-moderate VUR in human transplantation and their successful management have patients.26,27 However, an open surgical approach is 312

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performed for patients in whom an endoscopic technique has failed or when this is not available.26 In the present report, we chose an open surgical approach because medical treatment had failed and because the successful use of an endoscopic revision technique has not been established in canine patients. A recent study13 found that approximately 3.6% of human renal transplant recipients with VUR and recurrent UTIs underwent open surgical correction despite the use of prophylactic antimicrobial administration. The extravesicular technique is the most commonly used surgical method for ureteral reimplantation.13 Submucosal tunnel length at the time of transplantation is an important consideration for implantation. Previous reports4,24,26,28–31 recommend a longer submucosal tunnel (a 5:1 ratio between submucosal length and ureteral diameter) with the use of a Lich-Gregoir technique to prevent reflux in patients with VUR. As the bladder fills with urine, the bladder wall and intramural portion of the ureter stretch, functioning as a flap-valve mechanism. Results of an experimental study28 in dogs suggest that this process prevents retrograde reflux of urine from the bladder to the kidney. In the present case, we created a seromuscular tunnel approximately 5 times the diameter of the ureteral orifice during the corrective surgery. A submucosal tunnel length 3 times the ureteral orifice diameter has been reported to be effective in dogs2; however, the optimal seromuscular tunnel length for either a normal or dilated ureter has not been well established to date in canine patients and requires further study. The recommended radiographic evaluation of VUR in human patients includes voiding cystoureterography, ultrasonography, and, in some cases, nuclear renal scintigraphy. Voiding cystoureterography provides anatomic detail and allows accurate grading of VUR.32 Ultrasonography may be used to screen for renal and bladder abnormalities. Nuclear renal scintigraphy has many advantages because of its high sensitivity and relatively lower radiation exposure. In human patients, it is a voided study and no external pressure is applied, whereas in veterinary patients, the bladder is filled with contrast medium and external pressure is applied to obtain a cystourethrogram. A good voiding urethral view is recommended in human patients because it has been reported33 that approximately 20% of reflux may be missed if voiding has not occurred. Comparative data for voiding versus nonvoiding techniques have not been reported, and future studies should compare the clinical accuracy in veterinary patients. Diverse factors have been reported to increase the risk of UTIs in human patients, including female gender, intermittent or continuous bladder catheterization, lower urinary tract abnormalities, and VUR.34 The most frequent causes of UTIs in human renal transplant recipients are E coli, Klebsiella spp, Pseudomonas spp, Morganella spp, Enterococcus spp, Enterobacter spp, Corynebacterium spp, Candida spp,

and BK virus.6 In dogs, the most common bacteria are E coli, Klebsiella spp, Staphylococcus spp, Enterococcus spp, Proteus spp, and Pseudomonas spp.35 We did not identify the primary cause of the VUR with recurrent UTIs in the patient of this report. However, we speculate that malfunction of the submucosal tunnel as an antireflux valve due to impairment of the bladder mucosa by infection may have induced VUR. Recurrent UTIs with VUR can occur in immunosuppressed human patients,18,36 and UTI has been reported as a complication in cyclosporine-treated dogs.37,38 Our patient was administered cyclosporine for the first 6 months to maintain blood trough concentrations of 400 to 800 ng/mL, and then the cyclosporine dosage was gradually reduced. At the time of VUR occurrence, the dog had a blood cyclosporine trough concentration of approximately 250 ng/mL, and we do not know why the UTI occurred after reduction of the cyclosporine dosage rather than during the highdosage cyclosporine period. Vesicoureteral reflux can also be a primary cause of UTI in human renal transplant recipients,13 but we did not determine which complication came first in our case. Inappropriate ureteroneocytostomy technique can induce VUR.39 The extravesicular technique with a submucosal tunnel is one of the recommended protocols that is associated with fewer urinary complications for both human and canine renal recipients.2,40 In our hospital, we also use this technique for canine kidney transplantation and no other cases of VUR with UTIs have occurred. The combination of VUR and a UTI can result in deterioration of kidney function by causing permanent renal scarring.41 However, our patient did not develop other urinary complications such as urinary leakage, ureteral stricture, or calculi formation, which are common in human renal recipients,20 or any signs of renal failure after surgery. We speculate that the dog did not develop kidney damage as a result of VUR and a UTI because the condition was in its initial phase and antimicrobial treatment prevented severe kidney damage. However, a conflicting report42 stated that VUR does not have detrimental effects on grafted kidney function.Thus, the relationship among VUR, UTI, and grafted kidney function should be further studied in canine patients. In this report, we describe a dog with VUR and recurrent UTI after renal transplantation. Regular recheck examinations with repeated ultrasonography and urinalysis were important to detect postsurgical complications. Although recommendations cannot be made on the basis of a single case, we suggest that clinicians performing renal transplantation in dogs might consider creating a sufficiently long tunnel during transplantation to avoid VUR.

Acknowledgments Supported by 2014 research grant from Kangwon National University (C1010831-01-01), the Korea Research Foundation grant funded by the Korean government (KRF-2010-0025387), and a grant (Project Code No. Z-1541745-2013-14-01, Z-1541745-2013-14-02) from Animal and Plant Quarantine Agency, Ministry of Agriculture, Food and Rural Affairs (MAFRA), Republic of Korea in 2013. The authors declare that there were no conflicts of interest.

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Footnotes a. b. c. d. e. f. g. h. i. j. k. l. m. n. o. p. q.

Veterinary Diet Renal Support Dry Dog Food, Royal Canin, Aimargues, France. NBM-1000, MERA Pharmaceuticals Inc,Tokyo, Japan. MCA 0.1L, MERA Pharmaceuticals Inc,Tokyo, Japan. Revolution, Pfizer Inc, New York, NY. Advocate, Bayer Corp, Leverkusen, Germany. Butophan, Myungmoon Pharmaceutical Co, Seoul, South Korea. Atropine, Daehan New Pharmaceutical Co Ltd, Seoul, South Korea. Provive, Myungmoon Pharmaceutical Co Ltd, Seoul, South Korea. Forane, Choongwae Corp, Seoul, South Korea. Prolene, Ethicon Inc, San Angelo,Tex. Implanta, Hanmi Pharmaceutical Co Ltd, Seoul, South Korea. Solondo,Yuhan Medica Corp, Ochang, South Korea. Immuthera, Celltrion Inc, Incheon, South Korea. Cefazolin, Chong Kun Dang Pharmaceutical Corp, Seoul, South Korea. Omnipaque, Armersham Health Co, Cork, Ireland. Cephradine, Myungmoon Pharmaceutical Co, Seoul, South Korea. Tramadol, Huons Co Ltd, Seongnam, South Korea.

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Surgical management of vesicoureteral reflux with recurrent urinary tract infection after renal transplantation in a dog.

CASE DESCRIPTION A 3-year-old male Cocker Spaniel renal transplant recipient was readmitted 39 weeks after transplantation because of acute clinical s...
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