Systematic review of bladder cancer outcomes in patients with spina bifida

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Journal of Pediatric Urology (2017) xx, 1.e1e1.e9

Systematic review of bladder cancer outcomes in patients with spina bifida K.O. Rove a, D.A. Husmann b, D.T. Wilcox c, G.J. Vricella d, T.T. Higuchi e a

Division of Pediatric Urology, Washington University in St. Louis, MO, USA

b

Department of Urology, Mayo Clinic, Rochester, MN, USA

c Department of Pediatric Urology, Children’s Hospital Colorado, Aurora, CO, USA

d

Division of Pediatric Urology, Washington University in St. Louis, St. Louis, MO, USA

e

Division of Urology, University of Colorado, Anschutz Medical Campus, Aurora, CO, USA Correspondence to: K.O. Rove, Division of Pediatric Urology, Washington University in St. Louis, St. Louis Children’s Hospital, 1 Children’s Place, Suite 2A, St. Louis, MO, 63110, USA [email protected] (K.O. Rove) Keywords Systematic review; Bladder cancer; Bladder augmentation; Spina bifida; Myelomeningocele Received 10 March 2017 Accepted 6 May 2017 Available online xxx

Summary Background In patients with congenital bladder anomalies, bladder augmentation is used as a last resort to reduce intravesical pressure, but concerns about malignant transformation in augmented patients were first raised in the 1980s. The best evidence to date indicates that augmentation does not appear to increase the risk of bladder cancer in spina bifida patients. To date, oncologic outcomes from patients with spina bifida with and without augmentation have only been available in small case reports. Objective To systematically evaluate factors in myelomeningocele patients with bladder cancer, including bladder augmentation, that contribute to overall survival (OS). Study Design A systematic review using PubMed was conducted by cross referencing terms ‘myelomeningocele,’ ‘cystoplasty,’ ‘bladder cancer’ and respective synonyms according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. Inclusion criteria were studies with patients with an underlying diagnosis of myelomeningocele and bladder cancer with data on age, stage, and mortality status. Studies were excluded for spinal cord injury, history of tuberculosis or schistosomiasis, or prior ureterosigmoidostomy. Results Fifty-two patients were identified from 28 studies with a median age at bladder cancer diagnosis of 41

years (range 13e73); 37 (71%) presented with stage III or IV bladder cancer. Overall survival at 1 year and 2 years was 48.5% and 31.5%, respectively. Overall survival was different between those with and without augmentation (P Z 0.009) by log-rank analysis. No between-group differences in OS were seen based on age, management with indwelling catheter, diversion with ileal conduit or being on a surveillance program. Only stage remained a significant predictor of OS on multivariate analysis (HR 2.011, 95% CI 1.063e3.804, P Z 0.032). Secondary analysis was performed after removing patients with gastric augmentation (n Z 8), and no difference in OS was seen between patients with (n Z 8) and without augmentation (n Z 36, P Z 0.112). Of augmented patients, latency to development of bladder cancer was variable (Summary Figure). Discussion Bladder cancer is a deadly diagnosis in patients with congenital bladder anomalies like spina bifida, and while overall prevalence of the two conditions occurring together is low, bladder cancer will go on to affect 2e4% of spina bifida patients. The present study examined overall survival, and further characterized outcomes in these patients. Presence of a bladder augment did not appear to worsen overall survival. Conclusions Patients with myelomeningocele who developed bladder cancer had aggressive disease. Augmentation did not worsen OS, based on cases reported in the literature. Risk of bladder cancer should be discussed with all myelomeningocele patients.

Summary Fig Histogram of latency to development of bladder cancer in patients that had previously undergone augmentation (n Z 16). http://dx.doi.org/10.1016/j.jpurol.2017.05.006 1477-5131/ª 2017 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Rove KO, et al., Systematic review of bladder cancer outcomes in patients with spina bifida, Journal of Pediatric Urology (2017), http://dx.doi.org/10.1016/j.jpurol.2017.05.006

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Introduction Bladder augmentation is widely recognized in providing increased bladder capacity, reducing intravesical pressures, protecting upper urinary tracts, and improving continence in patients with neurogenic bladder who fail medical management [1,2]. Since its original description in the 1950s, the long-term risks of bladder augmentation are now well known and must be taken into consideration when counseling patients regarding treatment options for neurogenic bladder, particularly since patients with congenital bladder anomalies like spina bifida are living longer [3]. Concerns about malignant transformation in augmented patients were first raised in the 1980s [4e6]. In the absence of known causes for bladder cancer, augmentation was felt to be a potential independent risk factor for the development of bladder cancer [7]. This has been thrown into some dispute and doubt, with recent reports noting that both augmented and non-augmented patients with spina bifida develop bladder cancer [8,9]. However, to date, only a handful of case reports and series have been published about spina bifida patients with bladder cancer, limiting general knowledge about how these patients do and what factors, like bladder augmentation, might otherwise contribute to outcomes. The present study sought to perform a systematic review to quantify patient characteristics that influence overall survival (OS) in spina bifida patients who develop bladder cancer. It was hypothesized that patients with myelomeningocele and bladder cancer who have previously undergone bladder augmentation do not have decreased OS as compared with patients without bladder augmentation.

Methods Search strategy A systematic literature search of the PubMed database was conducted in April 2016 and updated in December 2016 to identify human studies by cross-referencing the terms: ‘myelomeningocele,’ ‘cystoplasty,’ ‘bladder cancer’ and respective synonyms. The full list of search terms and combinations is listed in Appendix Table 1. The methodology used to identify and select studies for patient inclusion in the quantitative synthesis was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [10]. Duplicate studies were identified and removed. Studies were included if they contained one or more patients with an underlying diagnosis of spina bifida and bladder cancer, with data available on age, stage, and mortality status. Study exclusion criteria were: those written in languages other than English or for which no medical translation could be obtained; studies with patients with an underlying congenital bladder anomaly other than myleomeningocele (e.g., PUV, sacral agenesis, classic bladder exstrophy or cloacal exstrophy); patients with cancer arising from non-bladder locations (e.g.,

K.O. Rove et al. catheterizable channel or upper urinary tracts); spinal cord injury patients; and patients with a history of tuberculosis or schistosomiasis, or prior ureterosigmoidostomy. Unique articles returned in the literature search were screened, and those that did not meet inclusion criteria on examination of title or abstract were excluded. Of the fulltext articles that remained, references were further analyzed to locate any studies not returned in the original search, and these were also screened. Finally, full-text articles were assessed for eligibility based on the stated inclusion and exclusion criteria, leaving studies with patients for final quantitative analysis (Fig. 1). Data on demographics, clinical symptoms, bladder management, diagnosis, treatment, follow-up and survival were recorded. Attempts were made to contact authors of those studies with missing data by email, to maximize numbers of patients and completeness of the data.

Institutional database query Institutional Review Board-approved databases at the authors’ respective institutions were retrospectively searched to locate patients with co-diagnoses of bladder cancer and myelomeningocele who met the inclusion and exclusion criteria. Patients meeting these criteria were then abstracted and included in the analysis.

Clinical definitions Symptoms and bladder management were recorded when described. Patients who were noted to have used one bladder management for a period of time and transitioned to another were recorded as having used both treatments. No attempt was made to differentiate time or sequencing of each management strategy secondary to heterogeneity and limited information provided within the case reports. Similarly, the study attempted to determine if patients were being followed regularly in a urology clinic; surveillance, in this regard, was defined as any of the following: regular annual or biannual visits with ultrasound and/or cystoscopy. Finally, it was recorded whether patients had a history of solid organ transplantation or were immunosuppressed, as this has been reported to increase the risk of malignancy [9,11]. Length of time from bladder augmentation to diagnosis of bladder cancer was calculated. Bladder autoaugmentation was not counted as bladder augmentation for the purposes of this paper. Type of intestinal segment used in the creation of the augment was recorded. In some cases, patients with prior ileal conduits underwent undiversion and bladder augmentation. In these cases, length of time to develop bladder cancer was recorded from the time of ileal conduit to diagnosis of bladder cancer; this was consistent with the total amount of time the bowel segment was exposed to urine. Stage was recorded or interpreted from the available data in each report, according to the American Joint Committee on Cancer (AJCC) bladder cancer staging system. Treatments and follow-up times were noted. If no

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Figure 1 Schematic of systematic review of literature using Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) to identify, screen, determine eligibility and ultimately include in final quantitative synthesis. An additional two patients were located via query of institutional databases and included in the analysis for a total of 52 patients.

follow-up was listed, follow-up was listed as zero. Patient mortality status was also recorded.

Statistical analysis Descriptive analyses of the patients from the identified studies were reported in median values (range). For timedependent analyses, KaplaneMeier and log-rank analysis was used, and patients were censored at the mention of the last time they were seen in follow-up or still surviving. Univariate and multivariate logistic regressions for survival analysis using a Cox Proportional Hazards Model were performed to determine effects of covariates on OS. Comparisons of categorical variables were performed using the Fisher’s exact test or Chisquared test, whereas comparisons of continuous variables were performed using the ManneWhitney U test. In all analyses, two-sided P-values <0.05 or a 95% confidence interval (CI) not crossing 1.0 were considered significant.

Results Of the 1840 unique studies located during the literature search, 28 studies met screening and eligibility criteria for inclusion in the systematic review. Fig. 1 depicts the PRISMA schematic for study identification and inclusion. Included studies and patients are listed in Appendix Table 2 [7e9,13,19,20,26e47]. Within these 28 studies, 50 patients with myelomeningocele and bladder cancer with available data were abstracted for this quantitative analysis. Two additional patients were identified in institutional databases and included in the final analysis for a total of 52 patients.

Demographics, presenting symptoms and treatment Demographics, pertinent medical history including presence or absence of bladder augmentation, presenting

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1.e4 symptoms, bladder management, and treatment for bladder cancer are listed in Table 1. Median patient age at bladder cancer diagnosis was 41 years old (range 13e73). Median follow-up was 6 months (range 0e144). Overall

K.O. Rove et al. survival at 1 year and 2 years for all patients was 48.5% and 31.5%, respectively. The KaplaneMeier OS curve for all patients is shown in Fig. 2A. Sixteen patients (31%) of the population had previously undergone bladder

Table 1 Demographics, symptoms, pertinent history, treatment, histology and staging for patients identified during systematic review. Spina bifida patients with bladder cancer Median age (range) Median latency to cancer in cystoplasty patients (range) Median follow up (range) Sex M F History Augmentation Ileal-colonic Gastric On surveillance program s/p renal transplantation Bladder management CIC Ileal conduit (native bladder left in situ) Indwelling (urethral or SPT) AUS Spontaneous voiding Not reported Autoaugmentation Symptoms Recurrent UTI Gross hematuria Pain (perineal, abdominal, suprapubic) Renal failure Difficulty catheterizing Urosepsis Bowel obstruction Other Treatment Radical cystectomy Chemotherapy Radiation Expectant Histology Urothelial cell With squamous differentiation With sarcomatoid differentiation With no additional features Squamous cell carcinoma Adenocarcinoma Signet ring type With no additional features Not reported Stage I II III IV Node positive Distant metastasis

52 patients 41 years (13e73) 14 years (8e53) 6 months (0e144) 23 29

44% 56%

16 8 8 19 1

31% e e 37% 2%

27 8 6 5 2 10 1

52% 15% 12% 10% 4% 19% 2%

27 23 9 4 2 1 1 7

52% 44% 17% 8% 4% 2% 2% 13%

44 14 4 2

85% 27% 8% 4%

22 5 2 15 10 16 3 13 4

42%

2 13 15 22 13 6

19% 31%

8% 4% 25% 29% 42% 25% 12%

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Figure 2 KaplaneMeier curves overall survival (OS) of (A) all patients, (B) those with and without prior bladder augmentation, and (C) patients by type of bladder augmentation. All comparisons performed by log-rank analysis.

augmentation, eight of which were gastric bladder augmentations and eight of which were ileal, ileal-cecal or colonic in nature. A total of 37% of patients were reported to be on a surveillance program with regular follow-up, the majority of which appeared to be clinical visits combined with ultrasound imaging. No difference in OS was noted between those regularly followed with clinical, imaging or cystoscopic surveillance vs not (P Z 0.195). Five patients were asymptomatic at the time of diagnosis of bladder cancer, and were diagnosed through routine imaging or cystoscopy. The remainder of patients was diagnosed on the basis of symptoms. The most common presenting symptoms were recurrent UTI, gross hematuria, or pain in the perineal, suprapubic or pelvic regions. Less common symptoms that led to the diagnosis included sepsis, artificial urinary sphincter (AUS) erosion, pyocystis, and urethral discharge. Radical cystectomy with pelvic lymph node dissection was the most common treatment modality in 44 of 52 patients (85%); 27% of the population received either neoadjuvant or adjuvant chemotherapy. Four patients (8%) received radiation therapy.

Impact of bladder management A total of 81% of reports discussed bladder management, aside from the presence or absence of previous bladder augmentation. As expected, the most common form of management was CIC of either the urethra or a catheterizable channel in 52% of patients. No significant differences in OS were noted on the basis of bladder management alone by log-rank analysis.

Stage and histopathology A majority of patients (37 or 71%) presented with AJCC stage III or IV bladder cancer, as shown in Table 1; 25% were node positive and 12% had distant metastasis at presentation. There was a significant difference in OS between stages I through IV on log-rank analysis (P Z 0.031), with decreasing probability of survival with increasing stage. Median OS for each stage was: not reached for stage I, 27 months for stage II, 24 months for stage III, and 8 months for stage IV. There were no significant differences (P Z 0.146

on log-rank comparison) in OS on the basis of histopathology subtypes, with urothelial cell carcinoma being the most common (22 patients or 42%).

Impact of bladder augmentation There was a significant difference in OS between patients with and without bladder augmentation on both log-rank analysis (Fig. 2B, P Z 0.009) and univariate Cox proportional hazard model (HR 0.283, 95% CI 0.105e0.763, P Z 0.013), favoring those who had previously undergone bladder augmentation of any type prior to diagnosis of bladder cancer. Median OS was not met in the augment group and was 6 months in the no augment group. The median latency from augmentation to time of bladder cancer in the 16 patients with bladder augmentation was 14 years (range 8e53). In considering other variables that might have impacted this result, there were no significant differences in age (P Z 0.138), regular surveillance (P Z 0.541), and history of transplantation (P Z 1.000) between augmented and not augmented groups. There was a difference in sex distribution (33 vs 69% male in the no augment vs augment groups, P Z 0.017). Presenting symptoms and treatment were not significantly different, with the exception of chronic pain (9 vs 0 patients in the no augment vs augment groups, P Z 0.043). There were no significant differences in indwelling catheter use, AUS or spontaneous voiding (P > 0.05). Previous publications have noted the increased risk of gastric augments to neoplastic degeneration, so the present study also performed a separate secondary analysis of the eight gastric augmentation patients. The KaplaneMeier curve in Fig. 2C shows the three groups, which were significantly different on log-rank analysis (P Z 0.024); however, the difference between ileal or colonic augment (n Z 8) vs no augment (n Z 36) was not significant (P Z 0.112).

Multivariate analysis A multivariate model was created including sex, augmentation type, surveillance program, and stage (see Table 2). In this model, stage remained the only significant predictor

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Table 2 Log-rank comparisons for KaplaneMeier time-survival data for listed covariates. Univariate and multivariate hazard ratios (HR) using Cox proportional hazard models are given. CI Z confidence interval, CIC Z clean intermittent catheterization, SPT Z suprapubic tube, AJCC Z American Joint Committee on Cancer. Variable

Log-rank P-value

Univariate HR (95% CI, P-value)

Multivariate HR (95% CI, P-value)

Age

e

0.999 (95% CI 0.973e1.026, P Z 0.952)

e

Sex Female Male

} } 0.179

e 0.832 (95% CI 0.289e2.395, P Z 0.734)

Augmentation

0.017

Reference 0.399 (95% CI 0.173e0.919, P [ 0.031) 0.283 (95% CI 0.105e0.763, P [ 0.013)

Augmentation type None Gastric

} } 0.024

Reference 0.125 (95% CI 0.017e0.940, P [ 0.043) 0.415 (95% CI 0.139e1.238, P Z 0.115) 0.987 (95% CI 0.938e1.039, P Z 0.618) 1.724 (95% CI 0.230e12.928, P Z 0.596) 1.418 (95% CI 0.635e3.166, P Z 0.394) 0.615 (95% CI 0.0819e4.616, P Z 0.636) 0.404 (95% CI 0.112e1.455, P Z 0.166) 2.476 (95% CI 0.703e8.728, P Z 0.158) 0.933 (95% CI 0.125e6.943, P Z 0.946) 0.614 (95% CI 0.279e1.351, P Z 0.226) 2.216 (95% CI 1.249e3.933, P [ 0.006)

e 0.211 (95% CI 0.026e1.688, P Z 0.143)

Ileal or colonic

}

Length prior to augmentation

e

Auto augmentation

0.569

CIC

0.288

Indwelling (urethral or SPT)

0.730

Ileal conduit

0.250

Artificial urinary sphincter

0.166

Spontaneous voiding

0.975

Regular surveillance program

0.336

AJCC stage

0.159

Histopathology Urothelial cell carcinoma Adenocarcinoma

} } 0.146

Squamous cell carcinoma

}

reference 0.444 (95% CI 0.153e1.289, P Z 0.135) 1.299 (95% CI 0.514e3.283, P Z 0.580)

of OS, and the other variables including augmentation type (none vs gastric vs ileal-colonic) did not. The study considered including bladder management strategies in the multivariate model to determine if they might influence the outcomes, but given the heterogeneity of the reports for this data, it was felt that this would introduce too much uncertainty and would not provide a reliable result.

Discussion Prior studies examining oncologic risks of patients with neurogenic bladder have either focused on an array of congenital bladder anomalies, examined only augmented patients, or included patients with spinal cord injuries, history of tuberculosis, and other confounding factors [7,9,12].

e

0.462 (95% CI 0.154e1.388, P Z 0.169) e e e e e e e 0.602 (95% CI 0.230e1.577, P Z 0.302) 2.011 (95% CI 1.063e3.804, P Z 0.032)

e e e

A recent review of bladder cancer in spina bifida patients by Mirkin et al. (which contained four patients included in the present systematic review) provided an excellent summary of the incidence of this problem, risk factors and screening evidence, but highlighted that some data for current practice are still extrapolated from spinal cord injury patients [13]. Each subset of patients with neurogenic and end-stage bladder offers unique challenges and questions regarding the risk of bladder cancer development. Through quantitative review of the literature the present study sought to specifically examine risks in myelomeningocele patients and determine whether bladder augmentation or other patient factors affect patient outcomes. Based on the data presented above, bladder augmentation does not appear to lead to worsened OS in spina

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Systematic review of bladder cancer bifida patients who develop bladder cancer, and confirms other reports that these patients present at advanced stages of disease and generally have poor prognosis, despite interventions, compared with the general population with bladder cancer [14e16]. The reader is cautioned: the present results are not the same as stating that bladder augmentation does not increase the risk of bladder cancer, which still remains somewhat controversial. Seorgel et al. estimated that the risk of bladder cancer was between 1.2 and 3.8% for spina bifida patients undergoing augmentation, and suggested that in the absence of other identifiable risk factors, bladder augmentation might represent an independent risk factor for the development of bladder cancer [7]. Without a comparison group, however, no data were provided to back up this claim. Austin et al. published the largest series (eight patients), with one patient having undergone prior augmentation (included in this systematic review) [8]. Seven of eight patients presented with locally advanced tumors or nodepositive disease. Median OS after diagnosis was 6 months. The authors hypothesized that spina bifida itself and associated bladder dysfunction may be responsible for increased risk of bladder malignancy. This is plausible; given that this is a life-long exposure to mechanical trauma (from catheterization) and chronic inflammation. The best available evidence against bladder augmentation being an independent risk factor was provided by Higuchi et al., who published a case control study in which 153 congenital bladder anomaly patients treated with bladder augmentation were matched 1:1 to a control group treated with CIC. They did not find a significant difference in the incidence of bladder cancer in augmented patients (4.6%) vs controls (2.6%), nor were there any differences in age (51 vs 49.5 years, P Z 0.71), stage (3.4 vs 3.8, P Z 0.56), mortality (71 vs 100%, P Z 0.49) or median survival (18 vs 17 months, P Z 0.80) [9]. Further data to answer this question will only come through large, multi-institutional case-control studies or longitudinal cohort study of a spina bifida population, like the US National Spina Bifida Patient Registry [17]. This registry will track outcomes across multiple specialties in both pediatric and adult spina bifida patients at 21 different centers across the United States. While cancerrelated outcomes are not specifically recorded, urologic procedures will be captured, which may allow for further insight into this issue. Previous reports have noted that there is an even greater risk of neoplastic change in gastric augments [18e21]. Although the analysis (as visually demonstrated in Fig. 2C) might indicate that these patients potentially do better, one of eight gastric augment patients was deceased at last follow-up, and the remaining seven gastric augment patients were censored at various time points. With few patients and even fewer events, caution is recommended in interpreting these results. Regarding screening, five of the 52 patients were diagnosed with bladder cancer on routine follow-up (which was defined as a clinical visit, routine imaging or surveillance cystoscopy). The remainder of patients was diagnosed on symptomatic presentation; 37% of these patients were reported to be seen regularly, highlighting the challenge of following these patients into adulthood and

1.e7 ensuring continuity of urologic care. Previous studies have cast doubt on prior recommendations that urologists follow cystoplasty patients starting 10 years after augmentation with regular cystoscopy and cytology [22e24]. Current practice at the respective institutions mirrors the protocol laid out by Husmann et al., which included annual followup with renal and bladder ultrasound, renal function and electrolyte testing, and urinalysis [25]. Cystoscopy and cross-sectional imaging are reserved for abnormal screening tests or symptoms that warrant further investigation. With 52 patients, the present study was limited by the paucity of reports in the literature. Follow-up was short and publication bias may have influenced these results. Most case reports did not specify presence or absence of bladder cancer risk factors like smoking or occupational exposures. The rarity of this problem was demonstrated by the fact that only two previously unreported patients were located within three large, tertiary care center databases. This study attempted to be as inclusive as possible in the systematic review search, but there were still five articles describing 15 spina bifida patients who developed bladder cancer with incomplete information that could not be included in this analysis. The study explored using national databases like the National Cancer Database, which might have increased the number of patients; but none appeared to capture all the details needed (oncologic outcomes, spina bifida status, and surgical history) to answer these questions.

Conclusion Patients with myelomeningocele who develop bladder cancer have aggressive disease. Bladder augmentation does not appear to result in worse outcomes from bladder cancer. Spina bifida patients are living longer into adulthood, and there is increasing awareness of increased risk of bladder cancer in these patients. It is recommended that these patients receive regular urologic visits, with special attention paid to those who develop gross hematuria, recurrent UTIs or pelvic pain.

Conflicts of interest None.

Funding No sources identified.

Acknowledgements None.

Appendix A. Supplementary data Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.jpurol.2017.05.006.

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Please cite this article in press as: Rove KO, et al., Systematic review of bladder cancer outcomes in patients with spina bifida, Journal of Pediatric Urology (2017), http://dx.doi.org/10.1016/j.jpurol.2017.05.006