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1 Primary Signet-Ring Cell Carcinoma of the Urinary Bladder: Review of the Literature and Report of a Case EVALYNNE V. BRAUN, MD,' MAJID ALI, MD,t A. OLUSEGUN FAYEMI, MD,* AND EDOUARD BEAUGARD, MDS A case of primary signet-ring carcinoma of the urinary bladder treated with total cystectomy and clinically disease-free three years and nine months after surgery is described. The signet-ring cell carcinoma of the bladder is a rare neoplasm; among the five cases found in the literature, the neoplasms pursued a fulminant course, diffusely invaded the bladder wall without forming intraluminal growths, and could not be controlled by segmental resection, radiotherapy, and chemotherapy alone or im combinations. The pathogenesis of mucus-producing signet-ring cell carcinoma in the urinary bladder, an organ that normally contains no mucogenic elements, is discussed. The histologic evidence for the origin of this neoplasm from the totipotent urothelium is illustrated. Cancer 47: , HE SIGNET-RING cell carcinoma of the urinary T bladder is a rare variant of mucus-producing vesical adenocarcinoma. It merits recognition as a pathologic entity for two reasons: its histologic morphology is distinctive (predominance of small mucinpositive signet-ring cells), and it follows a highly malignant course. The handfdl of cases of this neoplasm reported in the literature were discovered in advanced stages, and the results of treatment with surgery, radiotherapy, and chemotherapy were poor. The case reported in this paper illustrates the characteristic clinical presentation of this neoplasm, and is noteworthy for relatively long (over three years and nine months) disease-free period after surgical resection. The histologic study of the pathologic specimen furnished evidence supporting the origin of this neoplasm directly from the transitional cells without the presence of intermediate stage of metaplasia of transitional From the Holy Name Hospital, Teaneck, New Jersey; Fairleigh Dickinson School of Dentistry, Teaneck, New Jersey: College of Physicians and Surgeons of Columbia University, and The Mount Sinai School of Medicine, New York, New York. * Attending Pathologist, Holy Name Hospital; Ass't Professor of Pathology (Adj.), Fairleigh Dickinson. t Director, Division of Pathology, Immunology and Laboratories, Holy Name Hospital, and Assistant Professor of Pathology (Adj.), College of Physicians & Surgeons of Columbia University. $ Attending Pathologist, Holy Name Hospital, and Ass't Clinical Professor of Pathology, The Mount Sinai School of Medicine. B Chief, Department of Urology, Holy Name Hospital. Address for reprints: Evalynne V. Braun, MD, Department of Pathology, Holy Name Hospital, 718 Teaneck Road, Teaneck, NJ Accepted for publication March 18, epithelium into benign mucus-producing glandular elements. Such changes were observed both in the surface epithelium of the bladder as well as in the areas involved with cystitis cystica. Case Report A 4s-year-old paraplegic man was hospitalized for evaluation of recurrent hemorrhagic cystitis of eight months duration. Three months previously, the diagnostic work-up including intravenous pyelography and cystoscopy with bladder biopsy had failed to reveal any underlying neoplasm; the urine culture grew Pseudotnonus aeriiginosci and Escherichia coli. The physical examination at this admission did not provide any clues to the urologic lesions. The sensory and motor deficit related to the traumatic transsection of the spinal cord at Tj level, sustained 10 years previously, was noted. Routine urinanalysis showed many red blood cells, leukocytes, and bacteria. The urine culture grew Proteus rnircibilis. The routine hematologic and chemistry profile showed no abnormality except for the value of hemoglobin of 11 gm/dl. At cystoscopy, diffuse mucosal edema with hypertrophy of mucosal folds and intense hyperemia in the region of the trigone of the bladder was observed. The biopsy of the trigone showed small mucin-producing signet-ring carcinoma cells diffusely infiltrating the subepithelial stroma. A complete diagnostic work-up carried out to uncover the presence of an extravesical primary neoplasm was negative. A repeat cystoscopy performed two weeks later for mapping out the extent of the bladder carcinoma disclosed a new ulcerated lesion located in the left lateral wall; the biopsy of this region, proved the existence of infiltrating carcinoma. A total cystectomy with construction of an ileal loop conduit was performed. The patient's convalescence was uneventful X/81/0315/1430 $ American Cancer Society 1430
2 No. 6 SIGNET-RING CELL CARCINOMA Braun et ul. 143 I Follow-up of over three years and nine months since the time of surgery has not shown any clinical or laboratory evidence of recurrence of the tumor in the pelvis or elsewhere. The patient has remained well and free of cancer as of January Pathology The surgical specimen consisted of the urinary bladder, seminal vesicles, and prostate gland. The bladder was contracted and irregular in contour; its wall was markedly thickened with a leather-like texture, most pronounced in the region of the trigone and the posterior wall (Fig. 1). A large superficial ulcer with an irregular outline and an indurated base was located in the posterolateral wall of the bladder and extended to the superior border of the trigone. The mucosal folds at the base of the trigone and in the region of'the neck of the bladder were hypertrophied; their epithelial lining, however, was smooth and pearlywhite in appearance. The bladder mucosa in other areas was edematous, hyperemic, and finely granular. On section, the bladder wall was diffusely thickened and in several areas had a glistening, somewhat gelatinous gray-white appearance. A diffusely infiltrative tumor dissecting through the muscularis of the bladder wall was readily apparent on examination of the sections through the ulcerated area and the trigone (Fig. 2). No significant pathologic changes were observed in the seminal vesicles and the prostate on gross inspection. Microscopically, the sections taken from the bladder wall grossly involved with tumor showed small signetring cells, in clumps as well as single cells, diffusely invading the entire thickness of the wall of the bladder (Figs. 2, 3). The tumor cells (Fig. 3) were mucinpositive and were morphologically very similar to the FIG. 1. Gross photograph of surgical specimen showing a contracted urinary bladder with thickened wall. hypertrophied mucosal folds (arrows), mucosal hyperemia and ulceration (UL), and invasion of perivesical fat (small arrows). Urethra (u) and lateral wall (I) mucosa have the glistening gray-white appearance of squamous metaplasia. small signet-ring cell characteristically observed in gastric carcinoma of linitis plastica type. In addition, small round cells with scant basophilic cytoplasm and irregular hyperchromatic nuclei were also present, in small separate aggregates in some areas and admixed with the signet-ring population in others (Fig. 3); occasionally, transition between these two forms was observed (Fig. 4). Accumulations of mucin, with or without signet-ring cells in their periphery were separating the muscle fibers in many areas. The prominence of the mucosal folds was found to be due to proliferation of signet-ring cells and pools of much within the submucosa; the overlying epithelium in most areas displayed squamous metaplasia and parakeratosis (Fig. Flci. 2. Full mount of bladder wall, prostate (p) and seminal vesicle (v) through the lower trigonal region displaying extensive transmural infiltration by the neoplasm and epidermidization of overlying urethelium. The prostate (p) and seminal vesicle (v) are not involved by tumor (H & E, x5).
3 1432 CANCER March I VOl. 47 FIG. 3. Tumor cells, predominantly signetring type, are dissecting the muscularis of the bladder wall singly and is clusters. Smaller monocyte-like tumor cells (arrows) and mucus pools (m) are also present (H & E, ~200). FIG. 4. Higher power of Figure 3 demonstrating the transition from signet-ring forms to the smaller monocytoid cells (H & E, x450). FIG. 5. Higher power of Figure 2 showing diffusely invasive tumor growing submucosally (t) and mucus pools (m); the overlying epithelium is intact and is thrown into prominent folds (H & E, ~25).
4 No. 6 SIGNET-RING CELL CARCINOMA Bruun et al ). The study of multiple sections, undertaken to shed some light on the origin of signet-ring cell carcinoma, showed transition of dysplastic transitional cells to tumor cells in the lining epithelium (Figs. 6, 7); cystitis cystica was also present (Fig. 6). Extensive search for metaplasia of transitional cells to benign mucusproducing glandular elements proved negative. In many sections taken from the areas of the bladder wall removed from the grossly identifiable tumor, tumor cells were observed in the subepithelial stroma, between the muscle fibers, and within the lymphatics in many areas. Thle prostate and the seminal vesicles were free of tumor (Fig. 2). Discussion Reminiscent of the gastric carcinoma of linnitis plastica type and other extravesical neoplasms with similar morphology, the primary signet-ring cell carcinoma of the urinary bladder usually grows in a diffusely infiltrative ]pattern. The tumor grows laterally in the subepitheliall stroma and invades the muscularis over large areas; tlhe mucosal origin, from the surface urothelium or the epithelial elements within the submucosa, often remains unrecognized. Among the five neoplasms relported in the literature (Table I), exophytic iniraluniinal growth was either absent or information about this aspect of gross appearance of the neoplasm was not available. As in their extravesical counterparts, thickening of mucosal folds in this tumor is produced by proliferation of tumor cells in the submucosa and production of pools of mucin. The lack of large mucosal lesions in the early stages and the high growth vigor of the neoplasm combine to make the early diagnosis of this tumor an unlikely event. Clinically, following a variable period of insidious growth, the neopllasm causes hematuria. Ureteral FIG. 6. Vesical mucosa showing cystitis cystica and the lining urethelium (H E* loo). involvement was observed in two patients (Cases 2 and 3) who were thought to have localized lesions ; ureteral obstruction with pyelonephritis and progressive loss of renal function was observed in all cases FIG. 7. High-power view of urethelium shown in Figure 5. Melaplastic signet-ring cells are within the urethelial lining in areas not involved by the tumor. Cuboidal metaplasia of some of the superficial urethelial cells is also seen (H & E, x450).
5 ~ ~~ 1434 CANCER March Vol. 47 TABLE 1. Reported Cases of Primary Signet-Ring Cell Carcinoma of the Urinary Bladder Author AgeiSex Clinical features Tumor morphology Tr eatment Follow-up Extent of disease at time of death Saphir 60iM Hesitancy. incontinence. Diffuse: Entire bladder except Transurethral prostatic 4 mos after initial dx nocturia dome resection* (2 wks postop) Contracted, rigid bladder with thickened wall, prominent mucosal ulceration. Extension to ureters, prostate. peritoneum. Pyelonephritis Saphir JOIM Intermittent incontinence 16 nos) Hemafuria (I mo) Localized Flat at left lateral wall over left ureter Segmental resection with fulguration of surrounding bladder tissue 10 mos after initial dx (recurrence 3 nos. death 4 mos postresection) Bladder fixed lo surrounding tissue. Pyelonephritis Payan ri <I/. 38iM Hematuria 13 wksl Localized: I-irregular, well-defined 4 x 5 cm graywhite tumor surrounded by a shaggy brownish material: 2-papillary transitional cell car Segmental resection Asymptomatic several mos after resection Rosas-Unhe 48iF Nocturia, burning, & Luna urgency (2 mos): intermittent hematuria: Suprapubic pain Diffuse: Large mass 7 x 5 x 4 cm: iliac + retroperitoneal node metastases Combination chemotherapy including intravesical instillation of methotrexate & thiotepa IS mos after initial symptoms Firm, abnormally thick bladder with dark red mucosal nodules. Uterine extension. Metastases to peritoneum. pleura, ovaries, iliac + retroperitoneal nodes & one lumbar vertebra. Pyelonephritis Rosas-Urlbe 51iM Hematuria. dysuria, Localized: Overlying left Segmental resection. Post- 7 mos & Luna frequency (6 mos) ureter operative irradiation (Cobalt 60) to pubic region Bladder thicker than normal. Metastases to peritoneum. pericardium, pleura, retrv peritoneum. pelvic nodes and meninges Present case 45iM Hematuria (8 mos) Diffuse: Contracted. rigid Radical cystectomy with Asymptomatic with bladder with mucosal ulcer- construction of ileal loop no apparent disease ation t hypertrophied conduit (3 yrs. 9 mos postmucosal folds: focal super- resection) ficial extension to adjacent perivesical fat * Primary diagnosis of prostatic carcinoma t Not available. i Other urothelial tumor reported in the literature except one for which followup information was lacking. The case of Naeim et af. is excluded from the reported cases because the tumor was composed predominantly of grade 2 transitional cell carcinoma with only occasional signet-ring forms; the latter cell population predominated only after the tumor was irradiated. Illustrations of the postradiated neoplasm showed bizarre signet-ring forms; it is possible that these morphologic changes resulted from the regression of the more radiosensitive transitional cell carcinoma, cytologic radiation change, or a combination of these two processes. Pathogenesis The primary signet-ring cell carcinoma of the urinary bladder has been thought to arise from the totipotent cells of the transitional epithelium. The presence of solid nests of transitional cells (Von-Brunn s nests) within the subepithelial stroma is not uncommon in the bladder; their frequent association with recurrent inflammation of the mucosal lining of the bladder lends support to the view that these cells may result from proliferative invagination of the urothelium into the lamina propria evoked by chronic irritation. Subsequent cystic degeneration of these urothelial buds produces the characteristic changes of cystitis cystica. Cystitis glandularis results when the transitional cells abutting the central cystic space of cystitis cystica become transformed into columnar cells and acquire capability for mucus production. It seems highly plausible that the rare mucogenic adenocarcinoma of the urinary bladder arises from such metaplastic cell^,^,^ Further loss of differentiation results in formation of small undifferentiated cells that accumulate mucin within their cytoplasm, resulting in compression of the nucleus to one side of the cell. The signet-ring cell is so formed. Rupture of either the mucin-distended glands or individual cells produces the mucin pools so characteristically observed in these neoplasms. Small cells with scant basophilic cytoplasm are often observed admixed with the signet-ring cells and have been thought to represent degenerated signet-ring cells that have lost their
6 No. 6 SIGNET-RING CELL CARCINOMA. Bruun et ul capacity for mucin production with subsequent cytoplasmic ~hrinkage.~ The transition of the cells of the transitional epithelium to signet-ring cells in the present case (Fig. 7) appears to indicate that undifferentiated signet-ring cell carcinoma may evolve directly from the totipotent transitional cells without passing through the intervening stage of metaplastic columnar mucusproducing cells as seen in adenocarcinoma of the bladder arising from cystitis glandularis.1*4 In regards to the management of signet-ring cell carcinoma of the urinary bladder, the review of the literature does not furnish valid information about the efficacy of various approaches that have been adopted. The diffusely invasive character of this neoplasm and its distinctive proclivity for lateral spread in the subepithelial stroma and the muscularis, render the segmental resection even in apparently well-localized lesions an inadeqluate approach. This is attested to by the prompt recurrence of the tumor after segmental resection in two of the three cases (Cases 2 and 5) of localized tumor treated with this method; the followup of the third cases was limited only to several months. Chemotherapy and radiotherapy have not been shown to be effective in the control of this disease.2 Total cystectomy, though seemingly a radical procedure for early lesions, appears to be the only approach offering some hope for the control of this neoplasm. The relatively long disease-free survival (over three years and nine months) of a patient reported in this paper seems to support such a recommendation, although additional experience and longer follow-up of such patients will be required to establish its efficacy. REFERENCES 1. Edwards PD, Hurm RA, Jaeschke WH. Conversion of cystitis glandularis to adenocarcinoma. J, Urol 1972; 108: Naeim F, Schlezinger RM, de la Vega LM. Primary signet ring cell carcinoma of the bladder. Report of a case and review of the literature. J. Urol. 1972; 108: Mostofi FK. Potentialities of bladder epithelium. J Urol 1954; 7: Mostofi FK, Thomson RV, Dean AL Jr. Mucous adenocarcinoma of the urinary bladder. Cuncrr 1955; 8: Payan HM, MendozaC Jr, Cabinum D, Gerwig WH Jr. Primary signet ring cell carcinoma of the urinary bladder. Arch Surg 1966: 92: Rosas-Uribe A, Luna MA. Primary signet ring cell carcinoma of the urinary bladder. Report of two cases. Arch Parho/ 1969; 88: Saphir 0. Signet-ring cell carcinoma. Milif Surg 1951; 109: Saphir 0. Signet-ring cell carcinoma of the urinary bladder. Am J Prrthol 1955; 31:
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