Histopathologic features and clinical outcomes in 71 cases of bladder diverticula.
Context.--Bladder diverticula often come to clinical attention when
complications or malignancy occur, although limited information is
available regarding histopathologic features and clinical outcomes.
Objective.--To identify the morphologic findings, neoplastic subtypes, and clinical outcomes by reviewing all bladder diverticula that underwent pathologic sampling for primary diverticular processes at the Cleveland Clinic.
Design.--Hematoxylin-eosin slides from 71 cases of bladder diverticula were reviewed. Clinicopathologic features and patient outcomes were obtained from a retrospective review of patient records.
Results.--Patient ages ranged from 1 to 81 years (mean, 55 years), and the ratio of males to females was 68:3. Diverticular size ranged from 1 to 18 cm (mean, 5.3 cm) and often involved the lateral walls (38/71; 54%). Neoplastic changes were present in half of cases (36/71; 51%), including both noninvasive (16/36; 44%) and invasive (20/36; 56%) carcinoma. Of the invasive carcinomas, less-common subtypes included small cell carcinoma (n = 3), squamous cell carcinoma (n = 2), and adenocarcinoma (n = 1); 9 cases were pT1 (45%) and 11 cases were pT3 (55%). Follow-up for patients with benign findings demonstrated no subsequent neoplastic bladder disease. Patient follow-up for neoplastic diverticula (median, 27 months) demonstrated 4 cases of local recurrence and 3 cases of subsequent metastases. Of 9 patients with pT1 disease, only 1 patient (11%) developed subsequent metastases, whereas patients with pT3 disease demonstrated a higher rate of both local recurrence (3/11; 27%) and subsequent metastases (2/11; 18%).
Conclusions.--Patients with invasive carcinoma in diverticula have an increased frequency of less-common bladder cancer subtypes, and those with pT3 disease are at increased risk for subsequent progression.
(Arch Pathol Lab Med. 2009;133:791-796)
Diverticulum (Care and treatment)
Diverticulum (Patient outcomes)
Bladder cancer (Diagnosis)
Bladder cancer (Care and treatment)
Bladder cancer (Patient outcomes)
Histology, Pathological (Analysis)
Tamas, Ecaterina F.
Stephenson, Andrew J.
Campbell, Steven C.
Montague, Drogo K.
Trusty, Dante C.
Hansel, Donna E.
|Publication:||Name: Archives of Pathology & Laboratory Medicine Publisher: College of American Pathologists Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2009 College of American Pathologists ISSN: 1543-2165|
|Issue:||Date: May, 2009 Source Volume: 133 Source Issue: 5|
Bladder diverticula are outpouchings of the urothelial lining that
project through the muscular wall of the bladder and are caused by
congenital or acquired defects of the bladder wall. (1,2) Although most
bladder diverticula are small and asymptomatic, a subset of patients
develops problems associated with inflammation, calculi, infections,
large diverticular size, urinary retention, or malignancy. In many of
these cases, patients undergo biopsy and transurethral resection (TUR)
or surgical resection of the diverticulum for further evaluation and
Bladder diverticula affect a broad age range and, in general, histopathologic features tend to correlate with patient age, with younger patients typically demonstrating benign histopathologic findings and older patients demonstrating an increased risk of malignancy. To date, only a limited number of studies have examined the histopathologic features of bladder diverticula. (3-8) Neoplastic changes of the diverticular lining have been reported to occur in approximately 1% to 10% of all bladder diverticula, and carcinomas arising in diverticula account for approximately 1.5% of all carcinomas arising in the bladder, (9-12) although this number has been difficult to accurately determine because of the unknown number of small, asymptomatic diverticula that remain undetected in the general population, which would influence incidence rates. (13) In addition, several uncommon variants of invasive bladder carcinoma, including squamous cell carcinoma, adenocarcinoma, and sarcomatoid carcinoma, (14-16) have been documented in case reports, although the frequency of these entities in larger series of bladder diverticula are unknown.
In patients diagnosed with diverticular carcinoma, an additional challenge arises in assessing the depth of invasion because of the structure of the bladder wall at that location, which lacks the conventional muscularis propria (detrusor muscle) layer. This issue is further compounded in biopsy and TUR specimens, in which extensive deep sampling of the diverticular wall at that location is prohibitive because of the risk of perforation. In light of these complicating factors, prior studies that have addressed the clinical outcomes of patients with invasive carcinoma arising in a bladder diverticulum have obtained variable results. (4)
To address the histopathologic features most commonly identified in bladder diverticula, including features associated with invasive carcinoma, and to address the clinical outcomes in this population, we evaluated all bladder diverticula histopathologically sampled at the Cleveland Clinic.
MATERIALS AND METHODS
This study was approved by the Cleveland Clinic Institutional Review Board. Demographics and patient follow-up data were obtained from a retrospective review of patient records. Seventy-one cases of bladder diverticula reviewed at surgical pathology for primary diverticular processes between the years 1981 and 2006 were identified, and all hematoxylin-eosin slides were rereviewed for this study.
Specimens included 8 radical cystectomies (11%), 18 partial cystectomies (25%), 30 diverticulectomies (42%), and 15 extensive TUR specimens (21%). The radical cystectomies included 7 cystoprostatectomies and 1 radical cystectomy with total abdominal hysterectomy and bilateral salpingo-oophorectomy. In patients who underwent diverticulectomy, partial cystectomy, or radical cystectomy, the prior biopsy and/or TUR material was reviewed in 3, 9, and 4 cases, respectively, which demonstrated similar histopathologic findings to those reported in the larger resection specimens. Diverticular size as determined by cystogram measurements was available in a large proportion of cases (n = 47; 66%).
Patient Demographics and Clinical Findings
Seventy-one cases of bladder diverticula that underwent histopathologic sampling for primary diverticular processes were identified. The majority of patients were male, with a male-female ratio of 68:3. Patient ages ranged from 1 year to 81 years, and most (64/71; 90%) patients were adults (mean, 59 years; median, 66 years). The remaining 10% of patients were children, ranging in age from 1 year to 13 years (mean, 7 years; median, 7 years). Most patients in this series were white (63/71; 89%), and the rest were African-American (2/71; 3%) or of unknown (6/71; 8%) race.
Within the adult patient subgroup, clinical signs and symptoms were reported in 45 patients (45/64; 70%). The most commonly reported clinical finding was hematuria (22/45; 49%), followed thereafter by urinary retention (10/45; 22%), urinary tract infection (6/45; 13%), urinary incontinence (5/45; 11%), and dysuria (2/45; 4%). Six patients demonstrated additional urinary tract abnormalities, including bulbar urethral strictures (3/64; 5%), neurogenic bladder (2/64; 3%), and a duplicated collecting system extending from the renal pelvis to the distal ureter (1/64; 2%).
The pediatric subset (n = 7) presented with recurrent urinary tract infections (2/7; 29%), urinary incontinence (2/7; 29%), and hydronephrosis (1/7; 14%) or were identified incidentally (2/7; 29%). No patient demonstrated a history of Ehlers-Danlos syndrome or other syndrome reported in association with bladder diverticula. (17)
A complete summary of all patient demographics and clinical findings is presented in Table 1.
Gross Pathologic Findings
Locations of bladder diverticula were specified in 58/ 71 cases (82%), and most diverticula were solitary in nature (52/58; 90%). The most common locations included the left lateral wall (24/58;41%) and right lateral wall (14/ 58; 24%) of the bladder. Additional sites included the posterior wall (7/58;12%), dome (2/58;3%), and left ureteral orifice (5/58; 9%). Diverticula size ranged from 1 to 18 cm (average, 5.3 cm). Figure 1 demonstrates the gross appearance of a solitary focus of invasive urothelial carcinoma arising within a bladder diverticulum.
Histopathologic Findings in Benign Bladder Diverticula
Of all examined cases, 35 (35/71; 49%) demonstrated benign histopathologic features, including all cases of diverticula identified in children (7/7). The most common histologic findings included inflammation (13/35; 37%), granulation tissue formation (3/35; 9%), erosion (2/35; 6%), florid cystitis cystica et glandularis (3/35; 9%), non-keratinizing squamous metaplasia (3/35; 9%), and reactive urothelial atypia (2/35; 6%). The boundary between the lamina propria and the perivesical fat in most of the bladder diverticula was usually readily defined by a band of dense fibrous tissue of variable thickness (Figure 2, A), although fibroadipose tissue occasionally was present within this fibrous tissue (Figure 2, B). We used this dense fibrous tissue to define the boundary between the perivesical fat, which consisted almost entirely of fibroadipose tissue, from the lamina propria, which contained fibrovascular tissue and more abundant stomal tissue. Although individual fat cells and small collections of fibroadipose tissue were present in the lamina propria of 12 cases of diverticula examined, (18) including 7 benign diverticula and 5 neoplastic diverticula, the quantity was limited and consisted of less than 5% of the total tissue within the lamina propria.
[FIGURES 1-2 OMITTED]
Histopathologic Findings in Neoplastic Bladder Diverticula
The remainder of the resected diverticula (36/71; 51%) demonstrated neoplastic features (Table 2), including the presence of noninvasive (16/36; 44%) and invasive (20/36; 56%) lesions. Noninvasive lesions included low-grade papillary urothelial carcinoma (3/36; 8%), high-grade papillary urothelial carcinoma (7/36; 19%), flat urothelial carcinoma in situ (3/36; 8%), and combined flat urothelial carcinoma in situ and high-grade papillary urothelial carcinoma (3/36; 8%). In many instances, these findings represented recurrent lesions within the diverticula of the same neoplastic grade, including 3 cases of flat urothelial carcinoma in situ, 2 cases of low-grade papillary urothelial carcinoma, and 6 cases of high-grade papillary urothelial carcinoma. Eight patients with noninvasive, recurrent lesions received bacillus Calmette-Guerin treatment, including 1 patient with low-grade noninvasive papillary urothelial carcinoma, 2 patients with flat urothelial carcinoma in situ, and 5 patients with noninvasive high-grade papillary urothelial carcinoma.
[FIGURE 3 OMITTED]
A large percentage of invasive carcinomas identified in this study consisted of urothelial carcinoma (14/20; 70%), including 2 cases of urothelial carcinoma with extensive squamous differentiation and 2 cases of urothelial carcinoma with extensive sarcomatoid differentiation (Figure 3, A). The remaining 30% of cases consisted of less-common forms of bladder cancer, including small cell carcinoma (3/20; 15%; Figure 3, B), squamous cell carcinoma (2/20; 10%; Figure 3, C), and adenocarcinoma (1/20; 5%; Figure 3, D). Of the small cell carcinomas examined, 1 demonstrated associated flat urothelial carcinoma in situ, 1 demonstrated invasive urothelial carcinoma on prior biopsy, and 1 demonstrated associated urothelial carcinoma with squamous differentiation. Average invasive tumor size was 2.6 cm (range, <1 cm to 7 cm), and invasion was present either into the lamina propria (pT1; 9/20; 45%) or into perivesical fat (pT3; 11/20; 55%). Tumors that were considered invasive into the lamina propria frequently demonstrated the presence of a dense fibroconnective tissue band defining the boundary of the lamina propria and perivesical fat, whereas invasion into the perivesical fat demonstrated tumor cells involving extensive fibroadipose tissue beyond the junction of the dense connective tissue defining the lamina propria boundary. In no case was any tumor identified extending into adjacent organ structures (pT4), and depth of invasion did not appear to correlate with the morphologic subtype of the tumor.
Of 8 radical cystectomy specimens and 6 partial cystectomy specimens with associated pelvic lymph node dissections, only 1 case of small cell carcinoma demonstrated lymph node metastases at the time of surgery. Three cases demonstrated a positive resection margin, including 2 cases with a positive mucosal resection margin on partial cystectomy (containing flat urothelial carcinoma in situ in one case and invasive small cell carcinoma in a second case) and 1 case of a positive soft tissue resection margin on partial cystectomy in a case of invasive urothelial carcinoma. Abnormal findings of the bladder mucosa, separate from the diverticula, were identified in 5 cases and consisted of 4 high-grade papillary urothelial carcinomas and 1 low-grade papillary urothelial carcinoma, which reflected the grade of the paired papillary neoplasm within the diverticula. The remaining cases demonstrated a normal-appearing mucosal lining of the bladder on cystoscopic examination and were not histologically sampled.
Clinical follow-up was available for 51 patients (51/71; 72%; Table 3). Of patients with benign histopathologic findings, follow-up was available for 24 patients (24/35; 69%) with a range of 2 to 124 months (mean, 36 months; median, 16 months). No patient in this subset demonstrated any subsequent neoplastic bladder findings or metastatic disease during the course of follow-up.
In comparison, follow-up was available for 27 patients (27/36; 75%) with neoplastic diverticular disease, with a median follow-up of 27 months (range, 1-126 months; mean, 38 months). For patients with noninvasive disease, only 2 patients with high-grade papillary urothelial carcinoma demonstrated recurrent noninvasive high-grade papillary lesions at other locations within the bladder at 25 and 54 months following TUR and partial cystectomy, respectively.
Of the 9 patients with invasive carcinoma into the lamina propria (pT1), 1 patient with urothelial carcinoma with focal glandular differentiation demonstrated subsequent metastatic disease to the vertebral bodies at 27 months following partial cystectomy with negative margins. No local recurrence was documented in the pT1 population. Of the 11 patients with invasive carcinoma into the perivesical fat (pT3), 2 patients demonstrated subsequent metastatic disease, including 1 patient with invasive urothelial carcinoma showing metastases to the liver and spleen at 8 months following radical cystectomy with negative margins, and 1 patient with small cell carcinoma showing metastases to the brain and lung at 11 months following radical cystectomy with negative margins. In addition to these patients, 3 additional patients with pT3 disease demonstrated local recurrence of disease in the bladder or pelvis, including 2 cases of partial cystectomy for urothelial carcinoma with negative margins, and 1 case of radical cystectomy for small cell carcinoma.
All 3 patients demonstrating subsequent metastatic disease were dead of disease on long-term follow-up and 3 (75%) of 4 patients with local recurrence were dead of disease on long-term follow-up. All other patients who demonstrated neoplastic findings in this study were alive without disease at the time of last follow-up.
Bladder diverticula represent a herniation of the bladder mucosa through the muscular wall (detrusor muscle) of the bladder (1,2) and may be single or multiple in nature. Congenital diverticula occur more frequently in men and are associated with recurrent urinary tract infection, urinary retention, and vesicoureteral reflux, especially when the diverticulum is situated adjacent to the ureterovesical junction (Hutch diverticulum). (19,20) Acquired diverticula may be secondary to bladder outlet obstruction caused by prostatic enlargement or bladder neck stricture, as well as neurogenic bladder. (6) Finally, bladder diverticula may occur in association with a variety of heritable syndromes. (17) To date, only limited studies, to our knowledge, have examined the histopathologic features of bladder diverticula, and this study on 71 cases represents one of the larger studies to address this issue.
The majority of patients in our study who underwent histopathologic sampling of bladder diverticula were middle-aged to elderly men, which is similar to the age range previously reported by other studies. (5,6) Only 3 patients were women, and only 7 patients were younger than 18 years. In general, neoplastic alterations were only identified in the adult subset of patients in our study, which may reflect the underlying increased risk of general bladder neoplasia with increasing age.
In our series, approximately half of all diverticula that underwent histopathologic sampling for primary diverticular processes, including complications or concern for malignancy, demonstrated neoplastic findings that ranged from in situ lesions to invasive carcinoma. This percentage of neoplastic alterations in this study is significantly higher than that previously reported within diverticula and is most likely due to the study population, which included histopathologically sampled diverticula that often were biopsied or resected because of abnormal cystoscopy findings, rather than a study on all clinical diverticula identified on imaging or cystoscopy. Most noninvasive lesions (81%) demonstrated either flat urothelial carcinoma in situ or high-grade papillary urothelial carcinoma. The true incidence of low-grade papillary urothelial carcinomas, papillary urothelial neoplasm of low malignant potential, and papillomas in this population may be somewhat skewed, however, because a significant proportion of patients may undergo ablation of these lesions without histopathologic sampling.
All patients clinically identified at the Cleveland Clinic with invasive carcinoma within diverticula, in contrast, subsequently underwent histopathologic sampling to determine tumor type and pathologic stage. Of these 20 patients, approximately half demonstrated more aggressive subtypes of bladder cancer within diverticula, including small cell carcinoma, squamous cell carcinoma, adenocarcinoma, and sarcomatoid carcinoma. Although the number of cases of invasive carcinoma is somewhat limited in this study, the increased frequency of these generally uncommon bladder cancer subtypes within diverticula appears to be significantly higher than that reported for the bladder in general (21) and should prompt further studies into the incidence and subtypes of invasive carcinoma within diverticula.
One of the challenging aspects in the histopathologic examination of bladder diverticula, especially in the setting of invasive disease, is the distinction between lamina propria (pT1) and perivesical fat (pT3). Although the majority of cases demonstrated a distinct transition between the dense fibrotic tissue associated with the lamina propria and adjacent loose fibroadipose tissue associated with the perivesical fat, this distinction may not always be readily apparent, especially in smaller biopsy or TUR specimens. The examination of histologically benign diverticula may reveal occasional stranding of the connective tissue of the lamina propria into the perivesical fat, resulting in a more indistinct boundary between these layers. In addition, foci of fibroadipose tissue may be found normally in all layers of the bladder wall, (18) although the amount of this fibroadipose tissue is generally more limited than that present in association with perivesical fat. In our study, 12 cases demonstrated individual fat cells or small collections of fibroadipose tissue that consisted of approximately 5-6 fat cells within the lamina propria, and these small collections were readily distinguishable from the larger collections of fibroadipose tissue present within the perivesical fat. Finally, depth of invasion may be especially challenging to assess in biopsy and TUR specimens; in which, only limited sampling may be possible, and a distinct muscularis propria (detrusor muscle) layer is not present for evaluation. Specifically, more than half of the patients with invasive disease who had a prior biopsy or TUR were upstaged on more extensive resection of the diverticulum.
Clinical outcomes in patients with carcinoma arising within bladder diverticula has been highly variable, and it has been proposed that tumors present in the perivesical fat surrounding diverticula may not behave as aggressively as those that have traversed muscularis propria to reach this depth of invasion in a normally structured bladder wall. (4) However, these tumors may indeed behave in a similar aggressive manner as those found in other bladder locations because tumor cells have ready access to surrounding organs and angiolymphatic spaces once they have reached this depth of invasion, irrespective of the presence of a muscularis propria (detrusor muscle) layer. To attempt to address the clinical outcomes in this population, we collected follow-up data on 75% of our patients with neoplastic findings in bladder diverticula. In general, patients with invasive tumors demonstrated worse outcomes than patients with noninvasive tumors, and patients with invasion into the perivesical fat (pT3) demonstrated worse outcomes than patients with invasion into the lamina propria (pT1). Specifically, 5 (45%) of 11 patients with pT3 disease demonstrated either local recurrence or distant metastases, whereas only 1 patient with pT1 disease demonstrated subsequent metastatic disease. Only 1 patient with pT3 disease and local recurrence, however, was alive without disease at long-term follow-up, suggesting that subsequent disease, irrespective of morphologic subtype or depth of invasion on initial resection, demonstrates poor outcomes in this population.
In summary, patients who undergo histopathologic examination of bladder diverticula for primary diverticular processes frequently demonstrate neoplastic alterations at surgical pathology. Notably, a marked increase in unusual variants of bladder carcinoma was identified in these specimens, which may represent the distinct microenvironment that influences the urothelium in these situations. Although invasion into the perivesical fat appears to present an increased risk of subsequent local recurrence and metastatic disease, the overall number of patients in this study is limited, and future studies that examine a larger series of patients with invasive carcinoma within bladder diverticula would be valuable in determining ultimate long-term outcomes and best treatment options in this patient population.
This work was made possible by the generous support of the M. Frank and Margaret Domiter Rudy Chair fund.
Accepted for publication August 11, 2008.
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Ecaterina F. Tamas, MD; Andrew J. Stephenson, MD; Steven C. Campbell, MD, PhD; Drogo K. Montague, MD; Dante C. Trusty; Donna E. Hansel, MD, PhD
From the Department of Pathology, Quest Diagnostics, Teterboro, NJ (Dr Tamas); the Glickman Urological and Kidney Institute (Drs Stephenson, Campbell, Montague, and Hansel), the Taussig Cancer Institute (Drs Campbell and Hansel), and the Department of Anatomic Pathology (Dr Hansel), The Cleveland Clinic, Cleveland, Ohio; and the Department of Pathology, The Johns Hopkins Hospital, Baltimore, Md (Dr Trusty).
The authors have no relevant financial interest in the products or companies described in this article.
Presented in part at the annual meeting or the United States and Canadian International Academy of Pathology, Denver, Colorado, March 5, 2008.
Reprints: Donna E. Hansel, MD, PhD, Department of Anatomic Pathology, The Cleveland Clinic, 9500 Euclid Ave, Desk L25, Cleveland, OH 44195 (e-mail: email@example.com).
Table 1. Patient Demographics and Clinical Presentation Patient and Clinical Characteristics * Cases Total cases, No. 71 Specimen type, No. (%) TUR only 15 (21) Diverticulectomy 30 (42) Partial cystectomy 18 (25) Radical cystectomy 8 (11) Age, mean (range) 55 (1-81) Children (n = 7) 7 (1-13) Adult (n = 64) 59 (2 7-81) Sex: male to female ratio 68:3 Race, No. (%) White 63 (89) African-American 2 (3) Unknown 6 (8) Symptoms/clinical signs, No. (%), n = 50/71 (70%) [dagger] Hematuria 22 (44) Urinary retention 10 (20) Urinary tract infection 8 (16) Urinary incontinence 7 (14) Dysuria 2 (4) Frequency 1 (2) Flank pain 1 (2) Constipation 1 (2) Hydronephrosis 1 (2) Additional urinary tract abnormalities, No. (%), N = 71 Bulbar urethral stricture 3 (4) Neurogenic bladder 2 (3) Duplicated collecting system 1 (1) Location of diverticula, No. (%), n = 58/71 (82%) L lateral wall 24 (41) R lateral wall 14 (24) Posterior wall 7 (12) L ureteral orifice 5 (9) Dome 2 (3) Bilateral/multiple 6 (10) * TUR indicates transurethral resection of the bladder. ([dagger]) Some patients demonstrated multiple signs/symptoms. Table 2. Pathologic Findings in 36 Patients With Neoplastic Bladder Diverticula * Findings ([dagger]) Cases Morphology, No. (%) Noninvasive low-grade UCC 3 (8) Noninvasive high-grade UCC 7 (19) Flat urothelial carcinoma in situ 3 (8) Flat urothelial carcinoma in situ and non- invasive high-grade UCC 3 (8) Invasive conventional urothelial carci 10 (28) Invasive small cell carcinoma 3 (8) Invasive urothelial carcinoma with exten- sive squamous differentiation 2 (6) Invasive squamous cell carcinoma 2 (6) Invasive adenocarcinoma 1 (3) Invasive sarcomatoid carcinoma 2 (6) Depth of invasion, No. (%) Noninvasive (pTa or pTis) 16 (44) Lamina propria (pT1) 9 (25) Perivesical fat (pT3) 11 (31) Adjacent organs (pT4) 0 (0) Invasive tumor size, mean (range) cm 2.6 (0.1-7) Positive margin status, No. (%) 3 (8) Mucosal margin/partial cystectomy 2 (6) Soft tissue resection margin 1 (3) Associated metastases at surgery (pelvic lymph nodes), No. (%) 1 (3) * The staging system shown is the TNM staging system put forth by the American Joint Committee on Cancer. [dagger] UCC indicates papillary urothelial carcinoma. Table 3. Clinical Follow-up in Benign and Neoplastic Diverticula Characteristics Total Benign Diverticula * Clinical follow-up, No. (%) 46/56 (78) 19/23 (83) Time, mean (range), mo 36 (1-124) Time, median, mo 16 pT1 carcinoma, No. (%) 9 (15) Subsequent bladder recurrence N/A Subsequent metastatic disease N/A pT3 carcinomas, No. (%) 11 (19) Subsequent bladder recurrence N/A Subsequent metastatic disease N/A Characteristics Neoplastic Diverticula Clinical follow-up, No. (%) 27/36 (75) Time, mean (range), mo 38 (1-126) Time, median, mo 27 pT1 carcinoma, No. (%) Subsequent bladder recurrence 0/9 (0) Subsequent metastatic disease 1/9 (11) pT3 carcinomas, No. (%) Subsequent bladder recurrence 3/11 (27) Subsequent metastatic disease 2/11 (18) * NA indicates not applicable.
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