Anterior urethral valves – A rare but challenging congenital pathology

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Journal of Pediatric Urology (xxxx) xxx xxx

Anterior urethral valves e A rare but challenging congenital pathology a

Division of Pediatric Urology, Stanford Medicine, USA

Kunj R. Sheth a,*, Jeffrey T. White b, Aylin N. Bilgutay c, Abhishek Seth d,e, Angela G. Mittal d,e Summary

b

Division of Pediatric Urology, Norton Children’s Hospital, USA

c Division of Pediatric Urology, Hackensack Meridian Health, Jersey Shore University Medical Center, USA

d

Department of Surgery, Texas Children’s Hospital, USA

Background Anterior urethral valves (AUV) and associated anterior urethral diverticula (AUD) are a rare cause of congenital lower urinary tract obstruction. They occur 25e30 times less frequently than posterior urethral valves (PUV) and historically tend to have a less aggressive presentation and outcome. However, due to the low incidence, little is known about management and long-term prognosis.

e

Scott Department of Urology, Baylor College of Medicine, USA * Corresponding author. 750 Welch Rd, Suite 218, Palo Alto, CA 94304, USA. [email protected] (K.R. Sheth) Keywords Anterior urethral valves; Urethral diverticulum; End-stage renal disease; Bladder outlet obstruction; Hydronephrosis; Vesicoureteral reflux

Abbreviations PUV, Posterior Urethral Valves; AUV, Anterior Urethral Valves; AUD, Anterior Urethral Diverticulum; LUTO, Lower Urinary Tract Obstruction; VCUG, Voiding Cystourethrogram; UTI, Urinary Tract Infection; IRB, Institutional Review Board; CPT, Current Procedural Technology; VUR, Vesicoureteral Reflux; OR, Operating Room; CKD, Chronic Kidney Disease; ESRD, End Stage Renal Disease; EPA, End-to-end Primary Anastomosis

Objective We aim to evaluate the outcomes after AUV valve ablation and compare this group to a previously studied PUV cohort. Study design In this IRB-approved study, we retrospectively identified all patients from 2002 to 2017 undergoing valve ablation using CPT code 52400. Charts were manually reviewed to identify AUV patients, their presenting symptoms, timing of diagnosis, pre and postnatal imaging findings, age at presentation and valve ablation, creatinine, recurrences, additional surgeries and follow-up. The AUV group was then compared to a previously studied PUV cohort of 104 patients from our institution. Results Nine AUV patients were identified. Only four (44%) patients were diagnosed prenatally. Three (33%) patients were diagnosed neonatally, one for weak stream/dribbling and two for febrile UTIs. The

remaining two patients were diagnosed at ages 3 and 4 due to dysuria and penile swelling with micturition. Patients presenting later in life had no evidence of renal dysfunction or VUR. All patients underwent primary TUR-AUV (1 laser, 4 cold knife, 4 cautery), but 55% had residual valves and/or diverticula identified on routine postoperative imaging in two patients and due to development of clinic symptoms in three patients. All five patients with recurrences underwent repeat endoscopic evaluation, and thereafter two patients required urethral reconstruction. In contrast, only 15% (16/104) of PUV patients required re-TUR (p Z 0.01). At an average follow-up time of 4.24 years (range 0.6e11.4 years), 44% of patients had no evidence of CKD, and two patients (22%) had progressed to CKD of at least stage IIIA, compared to 21.4% in the PUV cohort at a mean follow-up of 2.3 years. Discussion The overall incidence of AUV is low, making it difficult to characterize these patients definitively. However, despite a milder phenotype and later presentation in most AUV patients, they do require more aggressive surgical treatment for complete resolution of the AUV. Furthermore, the long-term renal outcomes appear more severe than previously reported. Conclusions The poorer outcomes of AUV patients both with respect to recurrence and long-term CKD indicate that close urologic follow-up is essential in this group.

Received 31 December 2019 Accepted 26 March 2020 Available online xxx

https://doi.org/10.1016/j.jpurol.2020.03.024 1477-5131/ª 2020 Published by Elsevier Ltd on behalf of Journal of Pediatric Urology Company.

Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024

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1.e2

K.R. Sheth et al.

Extended Summary Figure

Anterior Urethral Valve Diagnosis and Treatment

Introduction The incidence of lower urinary tract obstruction is 2.2e3.4 per 10,000 births and occurs due to a variety of etiologies [1]. Amongst these pathologies, posterior urethral valves (PUVs) are the most common with a reported incidence of 1 in 3000 to 8000 live births [2]. In comparison, anterior urethral valves (AUVs) occur 25e30 times less frequently than PUVs [3]. As the most common congenital obstructive lesion of the anterior urethra, AUVs consist of semilunar folds arising from the anterior urethral floor [4]. The specific location of AUVs can vary from the fossa navicularis to just distal to the membranous urethra [5e7], with a reported incidence of 30% in the penile urethra, 30% in the penoscrotal junction and 40% in the bulbar urethra [8,9]. The exact etiology of AUVs has not been well-studied, although a variety of theories exist. Potential causes include incomplete hypospadias, an aborted attempt at urethral duplication in the first trimester, faulty alignment between glandular and penile urethra, incomplete focal corpus spongiosum development, an imbalance in developing urethral tissue resulting in a remnant valve, and cystic urethral glandular dilation [10e12]. In addition, AUVs are often associated with an anterior urethral diverticulum (AUD), but there is continued debate regarding which one is the initial insult. On the one hand, the presence of a spongy urethral defect can lead to AUD formation with the anterior lip of a filled diverticulum acting like a valve. On the other hand, if the AUV is the initial pathology, resulting

obstruction and turbulent flow proximally can lead to a urethral bulge resulting in a diverticulum [13]. Regardless of the etiology, the diagnosis and treatment of AUVs are often not so straightforward. The presentation can vary significantly from high grade lower urinary tract obstruction (LUTO) in utero to late diagnosis after presentation with lower urinary tract symptoms, such as urinary incontinence, weak stream, ventral bulge or UTIs. Therefore, the diagnosis can often be missed and a high level of suspicion in important in guiding the decision to obtain a diagnostic voiding cystourethrogram (VCUG). While treatment after diagnosis tends to favor endoscopic management as first line, followed by open reconstruction, there is minimal information about the future prognosis and outcomes in such patients with AUVs. While comparisons and data from PUV patients have been made and extrapolated, the two disease pathologies stand as separate entities. Therefore, in this study we aim to evaluate our experience with the diagnosis, management and prognosis of anterior urethral valves. In addition, we compare the long-term outcomes with a cohort of PUV patients also treated at our institution.

Methods After obtaining IRB approval, we used CPT code 52400 to identify all patients undergoing transurethral valve ablation between the years 2002 and 2017 at a single institution. As

Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024

Presentation, management and outcomes of each individual AUV patient. Timing of diagnosis

Presenting symptoms

VUR Grade

Concomitant PUVs?

Age at TUR valves

Valve ablation technique

Recurrence treatment

Stricture at old valve site IV dilated and incised with cautery, followed by perineal urethroplasty Ablation of residual valves withV cold knife Ablation of residual anterior II valves only with cold knife N/A I

2.7 yrs

N/A

I

4.0 yrs

Ablation of residual valves with0 cold knife N/A 0

2.4 yrs 0.63 yrs

N/A

0

12.3 yrs

SPT at time of residual valve ablation, followed by open reconstruction and diverticulectomy

0

2.2 yrs

13 days

Laser

Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Patient 7 Patient 8 Patient 9

1 year

Cold knife

7 days

Cold knife

3 days

Neonatal

LUTO, Oligohydramnios Bilateral Grade No 5 LUTO, Oligohydramnios Bilateral Grade Yes 5 LUTO s/p VAS in utero Bilateral Grade Yes 5 Weak stream, dribbling Right Grade 5 No

5 days

Neonatal

Febrile UTI

Neonatal

Febrile UTI

Delayed

Dysuria, deflected stream Palpable AUD, slow stream,

Prenatal Prenatal Prenatal

Delayed

Bilateral Grade No 5 None No

4 months

Resectoscope e cautery Resectoscope e cautery Cold knife

5 months

Cold knife

None

No

5 years

None

No

5 years

Resectoscope e cautery Resectoscope e cautery

13.6 yrs 14.0 yrs 4.2 yrs

MODEL

LUTO, Oligohydramnios Right Grade 5 No

Followup

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Patient Prenatal 1

CKD Stage

Management of anterior urethral valves 1.e3

Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024

Table 1

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1.e4 no specific code exists for AUVs, these charts were manually reviewed to find patients with AUVs identified on cystoscopy, comprising our study group. For the AUV cohort, basic demographic information was collected as well as initial presentation signs and symptoms. The timing of diagnosis was noted and separated into prenatal, neonatal or delayed diagnosis, defined as any time after 1 year of age. Renal bladder ultrasound images and VCUGs were reviewed from initial presentation through last follow-up. Renal function was documented at presentation by nadir creatinine and long-term renal disease was also recorded at the time of last follow-up. Management and surgical treatments were noted for all the patients along with associated outcomes. The presence of persistent valves and need for additional surgeries and associated outcomes were also noted. For comparison, we used a previously studied PUV cohort from our institution. Between the AUV and PUV study groups, we compared surgical outcomes and need for additional procedures after initial valve ablation. We also evaluated long-term renal function prognosis between the two groups. Descriptive statistics and Fischer’s exact tests were used to characterize and compare the study groups.

Results Over the 16 years, we identified 9 AUV patients with a mean follow-up of 5.32 years (Table 1). Only four (44%) patients were diagnosed prenatally, three (33%) were diagnosed in the neonatal period and two (22%) patients had a delayed diagnosis. All four patients diagnosed prenatally had oligohydramnios on prenatal ultrasound with evidence of LUTO noted by a dilated bladder and bilateral hydronephrosis. One patient underwent a vesicoamniotic shunt in utero, and another patient was born with pulmonary hypoplasia. On VCUG, all four patients had grade 5 VUR (3 bilateral, 1 unilateral). All four prenatal diagnoses were taken to the operating room (OR) soon after birth for cystoscopy, with two patients were found to have concomitant PUVs and AUVs, while the remaining two patients both had isolated AUVs. Three patients underwent transurethral ablation of valves, but one patient had a vesicostomy performed with return to the OR at 1 year of age for AUV ablation. Amongst the three patients diagnosed neonatally, one was diagnosed at birth due to a weak stream and dribbling, while two presented with a febrile UTI. The remaining two patients were diagnosed at ages 3 and 4 years with dysuria and penile swelling during voiding, respectively. All of these patients were taken for to the OR for valve ablation shortly after VCUG diagnosis. At the time of diagnosis, 6/9 (67%) had high grade VUR identified, 2 unilateral and 4 bilateral. The two patients with a delayed presentation and one neonatal patient that presented with a UTI had no VUR at presentation. Nadir creatinine was elevated in all patients presenting prenatally (Cr 0.6e1.38) and one patient presenting neonatally immediately after birth due to weakened stream (Cr 0.74).

K.R. Sheth et al. Initial valve ablation was performed with laser in 1 patient, cold knife in 4 patients, and cautery in 4 patients (Extended Summary Figure). After initial valve ablation, 5/ 9 patients (55%) required additional cystoscopy and intervention for residual valves and/or AUD. In 2/5 patients, initial postoperative VCUG showed no evidence of residual valves. One patient was difficult to catheterize during 1year postop VCUG. He was taken to the OR for cystoscopy and found to have a stricture at the site of prior valve ablation, which was dilated and opened with cautery followed by catheter placement. He was thereafter taken for a formal bulbar urethroplasty. The other patient with a history of concomitant AUV and PUV, presented with urinary incontinence at age 7, and was found to have residual AUVs, which were again ablated, and a clear posterior urethra. The remaining 3 patients that underwent additional procedures were identified much earlier. One patient had worsening penile edema after catheter removal on 2 separate occasions, and was unable to have a catheter placed for VCUG. He was taken back for a cystoscopy, at which time a large AUD was found and a suprapubic tube was placed to enable healing. Since the diverticulum did not heal, he had a formal urethral diverticulectomy and reconstruction. Of the other two patients, one was found to have residual valves on routine postop VCUG with no associated symptoms, and the second was noted to have decreased voiding stream with residual valves on VCUG. Both of these patients underwent a repeat ablation of the residual valves with no further urethral procedures needed. Two patients had other additional urologic procedures. Specifically, patient 2 underwent left ureteral reimplantation at the time of initial valve ablation (age 1) due to recurrent UTIs with the vesicostomy. Postoperatively residual valves were found and new grade 5 right VUR to a less-functioning kidney. Thus, at the time of repeat valve ablation a right deflux injection was also performed. Thereafter, at age 14, an appendicovesicostomy was done to allow for easy catheterization so he could be dry between voids. The second patient underwent a nephroureterectomy for a nonfunctioning kidney with persistent reflux. No other patients required ureteral reimplantation after valve treatment. At last follow-up, two prenatallydiagnosed patients had CKD Grade 4e5, with one patient, requiring a renal transplantation. The remaining two patients diagnosed prenatally had CKD stage 1 and 2. One patient with a solitary functional kidney that was identified as a neonate had CKD stage 1, but the remaining 4 patients diagnosed after birth had no renal disease. The PUV cohort previously studied at our institution was comprised of 104 patients presenting with PUV over a 9year period. Only 15% (16/104) of PUV patients underwent repeat valve ablation, while 55% (5/9) of AUV patients underwent repeat endoscopic evaluation with valve ablation and/or urethral reconstruction (p Z 0.01). The rate of clinically significant CKD (Stage IIIA or higher) was similar between the two groups e 20.2% (21/104) in PUV patients and 22% (2/9) in AUV patients. End stage renal disease (ESRD) rates were also similar with an 8.6% (9/104)

Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024

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Management of anterior urethral valves incidence in the PUV cohort and 11% (1/9) incidence in the AUV cohort (p Z 0.5).

Discussion Since the initial description of anterior urethral obstruction in 1906 [14], there have been case reports and small case series describing AUV and AUD, but the numbers still remain small for this rare disease, making characterization of these patients difficult. Within our study group, the presentation varied from early prenatal diagnoses for more severe cases to delayed diagnoses in milder presentations. When compared to patients with PUVs that mostly present at birth, we more frequently see a delayed and milder presentation of AUV, which has often been supported in the literature [15]. However, comparison of our AUV and PUV cohort has shown similar renal outcomes with a higher need for additional valve ablation and urethroplasty in AUV patients. While initial placement of a catheter in early presentations of valves can temporize the situation with urinary drainage as electrolytes stabilize, the definitive treatment is surgical. Historically open urethrotomy with resection of the valve and urethroplasty with end-to-end primary anastomosis (EPA) was the preferred modality of treatment [16,17]. However, as endoscopic instrumentation has improved with smaller instruments, valve ablation using cold-cut, electrocautery or laser has become the first line of treatment for AUVs [18]. However, if infants are too small at initial presentation, a temporizing vesicostomy, as performed in one of our patients, can avoid potential complications of stricture and inadequate valve resection until the urethra has grown [19]. One patient developed a stricture at the prior valve ablation site and required a formal EPA. In this patient, no clear symptoms had been noted as the patient was only 1 year of age, but on routine surveillance VCUG for VUR surveillance, there was difficulty placing a catheter. This patient was the only one treated with laser ablation and it is possible that the urethra was too small initially to accommodate a resectoscope for coldcut or cautery. Furthermore, 3 other patients in our cohort were found to have residual valves on routine postop VCUG, 2 presenting with voiding symptoms. The high incidence of residual valves in the AUV cohort brings into question the need for a re-look cystoscopy in all patients. Similar suggestions have been made in PUV patients, where a prospective study of 50 patients found a 78% rate of residual PUVs [20], which is far greater than the 15% rate of repeat valve ablation in our PUV cohort. While, all the cases of residual valves found on repeat cystoscopy may not be clinically significant, the higher rate of residual valves seen in our AUV cohort shows the importance of close follow-up in these patients. Furthermore, the concomitant presence of an AUD with AUV may imply additional interventions. In our cohort two patients had a concomitant AUD noted on endoscopic evaluation. While a small AUD can be conservatively managed with endoscopic valve ablation, a large AUD will likely cause significant lower urinary tract symptoms, necessitating an open urethral diverticulectomy and urethroplasty [12]. This was the case in one of our patients who

1.e5 required formal urethral reconstruction. Attempts were made to leave a suprapubic tube and allow for healing after the initial valve ablation, but the patient ultimately required formal reconstruction. On the other hand, Patient 2, who was found to have residual valves and an anterior urethral diverticulum, was successfully managed with repeat valve ablation alone, likely due to a smaller associated diverticulum. Identification of a large diverticulum may avoid additional surgeries by moving straight to urethral diverticulectomy and no endoscopic procedures that carry the risk of iatrogenic stricture development. Two of our patients presented with concomitant posterior and anterior urethral valves. A comprehensive literature review has shown at least 20 reported cases of concomitant AUV/AUD and PUV at presentation, although many other cases may never have been reported due to the rarity [13]. The presentation is again variable, with any combination of presenting symptoms for both anterior and posterior urethral obstruction. However, because only one valve could account for all the symptoms, urologists must carefully evaluate the entire urethra at the time of valve ablation to ensure that there is only one site of obstruction. The etiologies of posterior and anterior urethral valves are mostly thought to be distinct and therefore the concomitant presentation is usually explained as a coincidence [21]. However, an alternative explanation linking the two disease pathologies may support the now more than 20 reports of concomitant AUV and PUVs, and the 22% occurrence in our AUV cohort. The hypothesis to connect multiple urethral anomalies, including hypospadias, is that incomplete mesenchymal reabsorption in the anterior urethra may carry a migratory effect in the posterior urethra leading to defective Wolffian duct absorption, leaving remnants along the urethra that act as valves [13]. One report also linked the concomitant defect to delays in testosterone production, but not much further research has been done on this theory [22]. In comparison to PUV patients, those with AUVs have been shown to have overall better long-term prognoses, but in our patient cohort we found a similar rate of CKD between our AUV and PUV cohorts. The rate of CKD stage IIIa or worse in our cohort was 22% (2/9) with one patient requiring renal transplantation and one patient being monitored at present with CKD 4. However, it is important to know that this patient with CKD 4 is currently only 2 years old, and longer-term follow-up may lead to ESRD. In contrast, Routh et al. found the rate of ESRD to be only 4% and the rate of death to be 6% on an AUV meta-analysis [15]. Our results suggest a higher incidence of poor renal outcomes, similar to the 18% rate noted in a more recent report of 11 patients [10]. Knowing that the rate of ESRD may be higher in AUV patients, longer term follow-up is imperative, ideally with risk-stratification. We see in our group, that the patients diagnosed prenatally had the highest chance of poor renal outcomes. Of note, patient 4 had a vesicoamniotic shunt placed in utero, and on last follow up only had CKD stage 1. It is possible that the early intervention protected his renal development and avoided a more severe long-term renal disease. Those that were diagnosed later in life, and even those that were diagnosed a few months after birth during presentation with a UTI, all had no renal dysfunction at

Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024

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1.e6 time of last follow-up. Thus, it would seem reasonable to guide the frequency of follow-up by timing of initial diagnosis. Routh et al. identified certain risk factors for poor renal function, which included elevated pre-operative creatinine levels, VUR, and UTIs, with the combination of all three having a 25-fold increase in poor renal function [15]. In our cohort the one patient with a renal transplantation for ESRD had all three of these prognostic factors. The other patient with CKD stage IV had high grade VUR and an elevated nadir Cr greater than 1. The overall incidence of high-grade VUR in our study cohort was 67%, much higher than the reported rate of only 30% [15] in AUV patients, which may account for our higher rate of poor renal outcomes. However, only 2/6 patients with high-grade VUR have required reimplantation or nephroureterectomy. In contrast, Cruz-Diaz et al. reported that while patients with low-grade VUR had resolution after valve ablation, those with high-grade VUR required reimplantation [10]. This difference may be related to a different threshold for surgery in the VUR patients between the two cohorts. Patients with no VUR had normal renal function at the time of last follow up, but there were also four patients with highgrade VUR that had normal renal function or mild CKD 1e2 at the time of long-term follow-up. With respect to the occurrence of febrile UTIs, the two patients that presented with UTIs as newborns did not have any renal dysfunction at the time of follow-up. While this cohort is similar in size to the other large AUV series in the literature, it is still small in size, making it difficult to draw conclusions on AUV outcomes. Additionally, the retrospective nature and potential for inadequate follow-up at a tertiary care center, where many patients present from farther away, can cause further limitations on our results. This paper is the first to directly compare valve ablation and renal function long-term outcomes with a PUV cohort from the same institution. While the relationship between these disease pathologies may be debated, the long-term management goals and outcomes are similar. Thus, a direct comparison really allows clinicians to evaluate which principles to keep when treating the far rarer AUV patient.

Conclusions Overall the presentation of anterior urethral valves is highly variable, ranging from in utero lower urinary tract obstruction with oligohydramnios to mild lower urinary tract symptoms later in life. The severity of the diagnosis appears to vary inversely with the time of presentation, but because the diagnosis can often be overlooked, careful follow-up is imperative. While, many prior reports have indicated that AUVs are a more benign entity with less severe outcomes, the technical challenges of treatment, mainly adequate valve resection, potential stricture formation, and need for formal urethroplasty mandate close follow-up. Additionally, the incidence of poor renal outcomes appears to be similar to that of PUVs, again requiring routine monitoring by both urology and nephrology.

K.R. Sheth et al.

Funding None.

Conflicts of interest There are no personal, professional, or financial conflicts of interest.

Acknowledgements None.

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Please cite this article as: Sheth KR et al., Anterior urethral valves e A rare but challenging congenital pathology, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2020.03.024