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Endoscopic laser‐ablation for the treatment of orthotopic and ectopic ureteroceles in dogs: 13 cases (2008‐2017)

Background Ureteroceles are a rare condition in dogs in which conventional treatments can result in substantial morbidity. Cystoscopic and fluoroscopic‐guided laser ablation (CLA) of ureteroceles can successfully relieve obstruction. Objectives To describe the technique and outcomes of attempting CLA for treatment of ureteroceles in dogs. Animals Thirteen client‐owned dogs that underwent CLA for treatment of ureteroceles. Methods Retrospective multicentered study. Medical records were reviewed in all dogs that underwent CLA for ureterocele(s). A laser was used to extend the opening of the ureteral orifice (UO) unless surgical conversion was necessary. Data collected included signalment, clinicopathologic data, imaging, procedural findings, complications, and short‐ and long‐term outcome. Results Thirteen dogs with 13 ureteroceles associated with 14 UOs resulting in ureteral obstruction were included. One ureterocele extended bilaterally. Treatment was initiated via retrograde cystoscopy (7 females), percutaneous perineal urethrocystoscopy (4 males), or percutaneous antegrade cystoscopy (2 males). Surgical conversion was necessary in 2 males. Ten of 14 (71%) UOs associated with the ureteroceles were ectopic. Thirteen of 14 had stenotic or imperforate UOs. No postoperative complications were noted. Preoperative incontinence or pollakiuria was present in 9 of 13 and 3 of 13 dogs and resolved in 8 of 9 and 3 of 3 dogs, respectively. Follow‐up imaging showed resolution of all ureteroceles and improved ureteral/renal pelvic dilatation. Median follow‐up time was 27 months (range, 3‐96 months). Conclusions and Clinical Importance Cystoscopic‐guided laser ablation was effective for the treatment of ureteroceles(s) in 11 of 13 dogs.


| Medical records review
Data collected included signalment, clinical signs, physical examination findings, continence scores, diagnostic imaging findings, laboratory biochemical, hematologic, and microbiologic findings, procedural report, length of the procedure, and complications. Preoperative, intraoperative, and postoperative (short-term [<30 days], long-term [>30 days]) were recorded. Incontinence was defined as any persistent or intermittent involuntary leakage of urine. Continence was graded on a scale of 1 through 10, 32 where 1 was minimally continent (leaking all the time), 5 was moderately continent (leaking when lying down or when the bladder is full but able to hold urine between urinations and to produce a normal stream and volume of urine), and 10 was perfectly continent (no leakage at all). If omitted from the record, continence scores were assigned retrospectively. Follow-up information was obtained via medical record or telephone interview with the owner of each dog or primary veterinarian. Ultrasound reports were generated by radiologists, internists, and general practitioners. Computed tomography reports were generated by radiologists. Images were not retrospectively reviewed.
Information regarding presence of a ureterocele, renal architecture, renal pelvic diameter, ureteral diameter, and ureteral ectopia was recorded.

| Procedures
Cystoscopic laser procedures were performed by the authors A. C. Berent (Figure 1). If the ureterocele was unable to be catheterized (imperforate) (Figure 2), laser puncture was performed before catheterization. The cystoscope was deflected toward the urethral lumen to angle the laser fiber tip toward the medial aspect of the ureterocele, avoiding the lateral aspect of the bladder or urethral wall. The medial aspect of the ureterocele was cut in a linear continuous manner by use of the diode laser at 5-25 W None of these dogs were excluded from the study. Three dogs from the Animal Medical Center had been previously included in a prior publication describing treatment of a series of dogs with UO obstruction. 30 The focus of that paper was not on ureteroceles, so these individual dogs were not thoroughly described and were therefore included in this study. 30

| Signalment
Six male dogs (4 neutered and 2 sexually intact) and 7 female dogs (4 neutered and 3 sexually intact) were included, with a median age of 1 year (range, 2 months to 9 years) and weight of 23 kg (range, 7.88-45.2 kg). Dogs included 7 Labrador Retrievers, 2 Golden Retrievers,  Endoscopic and fluoroscopic images of a 2-month-old male intact Labrador Retriever with severe left hydroureter and hydronephrosis and an imperforate orthotopic ureterocele on the left and an ectopic ureter on the right. This procedure was performed from an antegrade cystoscopy approach owing to the small size of the canine pelvic urethra limiting the ability to perform percutaneous perineal access cystourethroscopy. The dog is in dorsal recumbency. A, A large fluid-filled structure covering the left ureteral orifice. There is no orifice seen. B, A diode laser is used to puncture the fluid-filled structure. C, The orifice in the structure is expanded with the laser and then the scope is used to explore the structure (D). D, The ureteral opening is seen inside this fluid-filled structure and is largely dilated. E, A digital subtraction contrast study is done using as a retrograde ureterogram up the ureteral orifice showing the severe hydroureter and hydronephrosis. F, Contrast is injected into the cyst after it is opened using a ureteral catheter, and the cyst and wall can be seen inside the urinary bladder as contrast refluxes retrograde up the ureteral orifice. G, Laser ablation of the contralateral ectopic ureter from an antegrade approach as the ureteral orifice could not be cannulated retrograde owing to the small size of the canine penis at this young age. H, Endoscopic image after both orifices are open and the filled cystic structure was ablated and 1 of each of the following Basset Hound, Chow Chow, Cocker Spaniel, and mixed breed.

| Clinical signs
Data regarding clinical signs was available for all dogs. Nine of 13 dogs were incontinent and 3 of 13 dogs were pollakiuric. One dog had vomiting and difficulty rising. No dogs were both incontinent and pollakiuric. Duration of presenting clinical signs was available for 12 dogs.
Median duration of clinical signs was 6 months (range, 2 weeks-3 years). One dog had a history of struvite cystolithiasis. One dog had previously undergone episioplasty surgery. Nine of 13 dogs presented for incontinence, and 3 of 13 dogs presented for pollakiuria. One dog presented for vomiting and difficulty rising.

| Physical examination
Vital signs were within normal limits for all animals. One dog was painful on abdominal palpation. One dog had referred upper airway sounds on thoracic auscultation and was diagnosed with an elongated soft palate and hiatal hernia. One dog had perivulvar urine scald. None of the dogs had an abnormal rectal examination. None of the females had digital vaginal palpation performed.

| Continence scoring
Data regarding continence was available for all dogs (Appendix 1). The median preprocedure continence score was 5 (range, 1-10). Nine of 13 were noted to be incontinent and 4 continent, preoperatively. The 4 dogs noted to be continent were pollakiuric (n = 3) and had vomiting/ difficulty standing (n = 1). Two of the incontinent dogs were being treated with continence medications preoperatively but remained inconti- Preoperative urine bacteriologic culture and sensitivity was performed in 9 of 13 dogs (69%) within 60 days before the procedure (median, 15.5 days; range, 5-57 days). Urine was obtained via cystocentesis. Six cultures were negative for bacterial growth. However, 3 of 6 dogs with cultures negative for growth were on antibiotics for previously diagnosed bacterial cystitis at the time of the culture. Three cultures were positive for growth including Alpha-hemolytic streptococcus (1), Escherichia coli (1), and a combination of E. coli and Proteus mirabilis (1).
Ten of 12 (83%) ultrasound reports described a hydroureter (ipsi- were not at all consistent with ultrasound findings. Of the 7 Labrador Retrievers, 2 (29%) had completely imperforate or unidentifiable UOs, 3 (43%) had patent but stenotic UOs, and 2 did not have data regarding patency of the UOs. One Labrador Retriever and 1 mixed breed dog had bilateral UO stenosis. All ectopic ureters and ectopic ureteroceles were intramural.

| Procedures
Treatment was accomplished via retrograde cystoscopy (7 females), APC (2 males), or PPAC (4 males). In another dog, a PPAC approach was performed and a ureterocele was noted in the central trigone with unidentifiable orifices. A blind incision was made into the ureterocele with a 600-μm diode laser (Lumenis Inc). No urine was noted coming from incision; there was concern for contrast extravasation from this incision, so the procedure was converted to a laparotomy. No leakage was confirmed upon opening.
The ureterocele was resected with a 600-μm diode laser (Lumenis Inc) during antegrade transurethral cystoscopy that was performed concurrently during a laparotomy to assist in gaining access to the remnant ureteral lumen. Because the orifice within the urethra was imperforate, access was unable to be obtained with cystourethroscopy alone. This approach also allowed external ureteral resection surgically and intraluminal orifice extension endoscopically, without the need for a urethrotomy. Closure of the urinary bladder and resection of the distal ureter was routine. Contrast cystography showed no leakage from the bladder after closure.
Duration of the procedure was available for 5 of 6 male dogs and was a median of 88 minutes (range, 79-95 minutes) when CLA of ureteroceles was performed. In the 2 cases that required surgical conversion, duration of procedure was 210 and 110 minutes, respectively. Seven of 13 dogs had additional surgical procedures performed, which were not distinguished in surgical times from ureterocele ablation.

| Clinical signs
Short-term follow-up data was available for 12 of 13 dogs. Eleven of 12 (92%) dogs had continence scores of 10/10; these dogs had a median continence score of 5 (range, 1-10) preoperatively. One dog scored 7.5/10, increased from 5/10 preoperatively. Two of the 11 fully continent dogs remained on continence medications indefinitely (1 dog was receiving phenylpropanolamine and estriol and 1 was receiving phenylpropanolamine and diethylstilbestrol, doses unknown), and it was unclear whether they had been attempted to be weaned off from the history, records, or client interview. These 2 dogs had scores of 5 and 1 preoperatively. The 2 of 3 dogs with pollakiuria before CLA had resolution of the pollakiuria; the final dog had resolution with initiation of doxycycline 11.6 mg/kg PO q24h (Merrem, Pfizer, New York City, New York).

| Long-term outcomes
The median long-term follow-up for all dogs was 27 months (range, 3-96 months). No long-term complications were noted from the CLA procedure.

| Clinical signs
The median postoperative continence score at the time of last followup was 10 (range, [3][4][5][6][7][8][9][10]. Twelve of 13 dogs were fully continent at last follow-up. The dog with a continence score of 7.5 two weeks postoperatively became fully continent within weeks of discharge. One dog with a continence score of 1 preoperatively and no 2-week follow-up score available remained incontinent. This dog was estimated to have a continence score of 2-4 long term despite continence medications (medications and dose unknown) 2 years postoperatively.
This was based on referring veterinarian communications, because the owner was deceased. After treatment, incontinence resolved in 8 of 9 (89%) dogs.
For the 3 dogs who presented with pollakiuria, all had long-term resolution.

| Long-term Outcomes
One dog was euthanized due to diffuse hepatic and splenic neoplasia 2 years post-CLA. One dog had a 1.5 cm apical bladder mass diagnosed 2 years post-CLA. A urothelial carcinoma, grade 2, was completely surgically excised. Postoperative chemotherapy was pursued, and the dog was followed up for 538 days until death from cause unknown.

| DISCUSSION
Results of the present study suggest that the use of a minimally invasive CLA procedure is a safe and effective treatment for ureteroceles in most dogs. This technique can avoid the need for more invasive surgery in most cases, especially in female dogs. It also suggests that ureteroceles in dogs are most commonly associated with a stenotic UO which can be associated with an ectopic ureter. They typically cause at least partial ureteral obstruction and should be treated to prevent renal injury. When successful, this procedure enabled a rapid and effective decompression of the ureterocele with low morbidity. In this population, 12 of 13 dogs (5/6 males, 7 females) had cystourethroscopy to diagnose a ureterocele. Eleven of 13 were able to be successfully approached using endoscopy alone, with the other 2 dogs being diagnosed with a UO stenosis using endoscopy, which then subsequently required surgical assistance for fixation. In all dogs, clinical assessments after fixation of the ureterocele were consistent with resolution of ureterocele. Surgical conversion was needed in 2 males.
No postoperative complications were noted. Resolution of pollakiuria was noted in all cases and resolution of urinary incontinence was noted in most cases.
In the human literature, there is controversy regarding etiology of ureteroceles identified in adulthood; it is thought that trauma or inflammation to the UO can result in stenosis and subsequent dilatation of the intramural distal ureter, appearing as an intravesicular cystic structure. [37][38][39] Based on the history of this dog, this was considered a remnant ureterocele that was intermittently infected owing to stagnant urine accumulation. This study included 4 dogs older than 2 years, suggesting that an acquired pathogenesis cannot be excluded. One of the ureteroceles was suspected to be acquired secondary to surgical ligation of intramural ectopic ureters. Formation of a ureterocele after intramural ectopic ureter anastomosis and continued reflux of urine into the intramural ureter has been reported. 25 Additional research is needed to understand etiology of ureteroceles in dogs.
In this case series, incontinence and pollakiuria resolved in 8 of than the dog with a prior ureteral reimplantation. In a human study of the sensitivity of ultrasound for hydroureter resulting from nephrolithiasis and ureterolithiasis, the sensitivity for detection of hydroureter was only 50%. 41 In this study, these differences could have been due to differences in operator skill and variation in dog conformation.
Human studies similarly cite the sensitivity and specificity of ultrasound for the detection of hydronephrosis as being highly dependent on hydration status with values of 100% and 84%, respectively, for hydrated patients and 35%-73% and 74%, respectively, for nonhydrated patients. 42 The previously reported clinical findings of pollakiuria, bacterial cystitis, and urinary incontinence in dogs with ureteroceles, 42 were consistent with findings in the 12 of 13 dogs in this study, with 1 dog presenting for vomiting/difficulty standing. In the latter dog, the ureteroceles was likely an incidental finding to gastroenteritis that resolved with supportive care. In the human literature, the treatment of clinically silent ureteroceles is recommended due to the potential risk of UTI, persistent ureteral outflow tract obstruction, and the loss of renal function. 12 The treatment of asymptomatic ureteroceles in veterinary medicine should also be considered.
Azotemia was present in only 2 of 13 dogs preoperatively and 1 of 7 dogs postoperatively. The dog with progressive persistent azotemia was noted to have dysplastic architecture of the kidneys on preoperative and postoperative ultrasound imaging. However, without obtaining renal biopsies, the exact etiology is unknown. Hydroureter has been reported to predispose to increased hydrostatic pressure and permanent renal damage. 15 Additional research would be required to understand if the progressive disease was primary renal dysplasia, progressive renal damage from chronic ureteral obstruction, or vesiculoureteral reflux from a large UO after fixation.
In this study, a single laser incision was utilized. No evidence of vesicoureteral reflux was appreciated on postoperative imaging, but follow-up contrast retrograde cystourethrography to test for ureterovesicular reflux was not performed. Assessing outcomes of multiple, solitary punctures creating a "watering-can" appearance 44 versus a single laser incision in the cystoscopic treatment of ureteroceles in dogs is another potential area of research, but with the positive outcomes shown here, this might be unnecessary.
Evaluation for long-term ureterovesicular reflux using voiding cystourethrograms would be helpful to determine if there is concern.
Because of the excessively long ureter seen in dogs, compared to people, the development of clinically relevant UVJ reflux is highly unlikely.
Clinically, with the resolution of ureteral dilatation, improvement of renal pelvic dilatation, improvement in urinary incontinence, and pollakiuria, along with the improved rate of UTIs, and failure of progressive azotemia, the likelihood of reflux creating a clinical problem is low.
The limitations of this study include its retrospective nature and lack of standardized follow-up. However, these results represent a standardized cystoscopic approach performed by 2 institutions with specialists trained in endourology. Both institutions had comparable outcomes. Differential glomerular filtration rate (GFR) studies were not performed to evaluate renal function before and after CLA. Urethral pressure profilometry was not performed to assess concurrent urethral sphincter mechanism incompetence; it is possible that urethral sphincter mechanism incompetence contributed to clinical signs.
However, given the high resolution of incontinence with CLA, this was not clinically impactful. Given the rare incidence of ureteroceles in dogs, this case series possesses the largest number of cases when compared to the current literature and can help form the basis for further comparison studies.
In conclusion, ureteroceles are a rare condition in dogs but should be considered as a differential for dysuria or incontinence, with concurrent hydroureter. Cystoscopic-guided ureteral ablation was a safe, effective, and minimally invasive technique for treating UO stenosis associated ureteroceles in most dogs. Ureteroceles are commonly associated with ureteral ectopia but can be orthotopic as well. They are uncommonly associated with azotemia. Dogs with ureteroceles should be considered to have a good to excellent prognosis and renal sparing treatments should be encouraged. Prospective studies are warranted to assess short-and long-term outcomes, the presence of ureterovesicular reflux, and to compare laser ablation to other surgical techniques.

CONFLICT OF INTEREST DECLARATION
Authors declare no conflict of interest.

OFF-LABEL ANTIMICROBIAL DECLARATION
Authors declare no off-label use of antimicrobials.

INSTITUTIONAL ANIMAL CARE AND USE COMMITTEE (IACUC) OR OTHER APPROVAL DECLARATION
Authors declare no IACUC or other approval was needed.

HUMAN ETHICS APPROVAL DECLARATION
Authors declare human ethics approval was not needed for this study.