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Kodzo-Grey Venyo and Baiden-Amissah: Plasmacytoid urothelial carcinoma of the urinary bladder – a review of the literature

Introduction

Plasmacytoid urothelial carcinomas of the urinary bladder are rare tumours. To our knowledge, approximately 100 cases have been reported globally. This article reviews the literature on these tumours and gives an anecdotal summary of the only reported case of plasmacytoid urothelial carcinoma of the ureter.

Materials and methods

Various internet databases were searched to identify cases of plasmacytoid urothelial carcinoma of the urinary bladder in order to document the presentation, investigation, management and outcome of the disease before treatment. To our knowledge, only one case of plasmacytoid urothelial carcinoma of the ureter has been reported in the literature, and is included in the literature review below.

Literature review

Plasmacytoid urothelial carcinoma is a recently described variant of urothelial carcinoma that was added to the World Health Organization (WHO) classification list in 2004.1

The first case of plasmacytoid urothelial carcinoma was first described by Sahin et al. in 1991.2 Since then, approximately 62 cases of plasmacytoid carcinoma of the urinary bladder have been reported in the English literature1,3 and fewer than 100 cases have been reported in the world literature.3

Presentation

A number of patients who were later diagnosed with plasmacytoid urothelial carcinoma were reported to have presented with macroscopic haematuria,46 urinary urgency and microscopic haematuria,6 macroscopic haematuria and painful micturition,7 lower urinary tract symptoms,7 persistent dysuria,8 non-specific abdominal pain without any associated haematuria,1 vague lower abdominal pain with associated urinary frequency and urgency requiring oxybutynin,9 dysplasia10 and urinary frequency.11

Cystoscopic findings

Some of the cystoscopic findings that were described in relation to plasmacytoid urothelial carcinoma of the urinary bladder include a solid mass with surrounding multiple papillary lesions,6 multiple massive lesions,6 diffusely thickened and erythematous bladder wall with bullous lesions with no apparent visible tumour,3 an extensive tumour,5 oedematous and ulcerated mucosa throughout the urinary bladder4 and a non-papillary tumour in the urinary bladder.1

Urine cytology

Zhang et al. 12 reported the first description of urinary cytology of plasmacytoid urothelial carcinoma in 2002. Cytological examination of the patient’s urine before and after cystoscopy and biopsy demonstrated large, dyscohesive tumour cells with plasmacytoid features.

Morphology

A number of authors stipulated that the tumour cells exhibit eosinophilic cytoplasm and eccentric nuclei, which produce a plasmacytoid appearance, thus suggesting multiple myeloma/lymphoma.2,1316 Various authors1620 have stated that the epithelial nature of the malignancy is confirmed by positive immunohistochemistry of cytokeratin (CK) markers and negativity for lymphoma/plasmacytoma markers and that the tumour is an aggressive neoplasm with stage-related outcome and frequent positive lymph node positivity. Figures 1 to 8 depict the morphology and immunohistochemical features of a plasmacytoid urothelial carcinoma of the urinary bladder.

FIGURE 1

Plasmacytoid urothelial carcinoma of urinary bladder, plasmacytoid tumour cells showing nested growth pattern. Haematoxylin and eosin staining, ×10 magnification.

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FIGURE 2

Plasmacytoid urothelial carcinoma of urinary bladder, tumour showing sheet-like pattern. Haematoxylin and eosin staining, ×10 magnification.

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FIGURE 3

Plasmacytoid urothelial carcinoma of urinary bladder, plasmacytoid cells showing nested growth pattern. Haematoxylin and eosin staining, ×20 magnification.

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FIGURE 4

Plasmacytoid urothelial carcinoma of urinary bladder, immunohistochemical staining for CD138 tumour cells staining positive for CD138, ×20 magnification.

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FIGURE 5

Plasmacytoid urothelial carcinoma of urinary bladder, medium sized tumour cells with eosinophilic cytoplasm and eccentric nuclei producing plasmacytoid appearance. The tumour cells are arranged as single cells in a loose stroma. Haematoxylin and eosin staining, ×20 magnification.

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FIGURE 6

Immunohistochemical staining for CD138, plasmacytoid urothelial carcinoma of the urinary bladder. The tumour cells showing positive staining with CD138, ×20 magnification.

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FIGURE 7

Immunohistochemical staining epithelial marker [cytokeratin (CK)7], plasmacytoid urothelial carcinoma of urinary bladder. The tumour cells showing positive staining with CK7, ×10 magnification.

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FIGURE 8

Immunohistochemical staining for CK MNF116, plasmacytoid urothelial carcinoma of the urinary bladder. The tumour cells are staining positive with MNF116 (a broad spectrum epithelial marker), ×10 magnification.

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Immunostaining

With regard to immunohistochemical staining of plasmacytoid urothelial carcinoma, Lopez-Beltran et al. 16 reported that both plasmacytoid cells and their associated conventional urothelial carcinomas were positive for CKs7, 20 and AE1/AE3 and the epithelial membrane antigen (EMA), CD138, was positive in three cases (see Figures 1 to 8).

Outcome

Ricardo-Gonzalez et al. 17 observed that plasmacytoid urothelial carcinoma had a predilection for intraperitoneal spread and could present with discontinuous involvement of serosal surfaces.

Lopez-Beltran et al. 16 reported that on follow-up of their 11 cases, nine patients died of their disease within 2–11 months and two patients were alive with disease at 8 and 16 months. In view of these findings, they concluded that the plasmacytoid variant of urothelial carcinoma is an aggressive variant that is associated with poor prognosis and also presents at an advanced stage.

However, there are recent anecdotal reports of improved survival of patients suffering from plasmacytoid urothelial carcinoma who have been treated by means of radical cystectomy and neoadjuvant/adjuvant chemotherapy.

Differential diagnosis

According to Lopez-Beltran et al.,16 the differential diagnosis of plasmacytoid urothelial carcinoma includes lymphoma and multiple myeloma. They also stated that:

  • Identification of an epithelial component by immunohistochemistry confirms the diagnosis.

  • Immunohistochemistry using CD45 (leucocyte common antigen) or CKs is useful.

  • In limited samples, plasmacytoid urothelial carcinoma may be misdiagnosed as chronic cystitis or plasmacytoma, a pitfall that is further compounded by CD138 (a marker of plasma cells) expression in some cases.

Discussion

Aldousari et al. 9 reported the case of a 57-year-old man who presented with haematuria and worsening lower urinary tract symptoms. He was known to have a history of recurrent superficial transitional cell carcinoma, which was refractory to two induction courses of bacillus Calmette–Guérin (BCG) instillations. He had a long history of smoking but did not have any family history of genitourinary malignancy. Urine cytology was negative and cystoscopy revealed abnormally ‘oedematous-appearing’ mucosa in the posterior wall of the urinary bladder. Metastatic workup included computed tomography (CT) of the chest, abdomen and pelvis and colonoscopy, which returned negative results, following which the patient was then scheduled to undergo radical cystectomy. Following exploratory laparotomy, he was found to have multiple metastatic lesions in the gastrointestinal tract and mesentery. Frozen sections of the lesions were sent for pathological examination, which revealed that the specimens were consistent with metastatic poorly differentiated transitional cell carcinoma. In view of the fact that the patient was significantly symptomatic, he underwent palliative cystectomy and ileal conduit diversion. Prior to microscopic examination and immunohistochemical study of the specimen, the pathologist reported that the tumour was a muscle-invasive high-grade urothelial carcinoma of the urinary bladder with plasmacytoid features that had penetrated through the entire bladder wall into the serosa. Immunostaining of the specimen was positive for CKs, confirming the diagnosis of plasmacytoid urothelial carcinoma. The metastatic lesions were also positive for plasmacytoid features. The pathological stage of the urothelial carcinoma was pT3a, N0, M1. The patient had an uneventful postoperative recovery and was discharged after 10 days. He received systemic gemcitabine and cisplatin chemotherapy; however, he died within 6 months as a result of rapid progression of disease.

The authors9 stated that:

  • Treatment of this variant of urothelial carcinoma is very difficult in view of the late presentation with metastases and lack of data on its response to systemic chemotherapy.

  • Kohno et al. 18 reported, in 2006, the first pathological complete response found at radical cystectomy for cT4N0M0 plasmacytoid urothelial carcinoma treated with neoadjuvant chemotherapy (methotrexate, vinblastine, etoposide and cisplatin).

Fritsche et al.,19 in 2008, claimed that urothelial carcinoma with plasmacytoid morphology is a rare and only recently described histological variant; at that time, only 22 cases had been reported in the literature. They presented the clinical and histopathological features of five cases of plasmacytoid urothelial carcinoma in their institution. They stated that, in a consecutive series of cases of 130 muscle-invasive urothelial carcinoma, three cases of plasmacytoid urothelial carcinoma (2.3%) were identified. They also studied two more plasmacytoid urothelial carcinoma cases, one of which was non-invasive. They collected data from the clinical charts, histological reviews and follow-up records of the patients and reported that:

  • Four patients had a muscle-invasive tumour at presentation.

  • The non-muscle invasive plasmacytoid urothelial carcinoma was only the second published case in the literature.

  • Conventional differentiated urothelial carcinoma was focally present in every case.

  • Plasmacytoid urothelial carcinoma cells were dyscohesive and exhibited abundant eosinophilic cytoplasm, leading to a plasmacytoid appearance.

  • Positive immunostaining for epithelial markers confirmed the epithelial nature of the tumour. All the tumours showed negative E-cadherin expression.

  • Adjuvant or neoadjuvant chemotherapy seemed to have a beneficial effect on survival in patients with advanced tumours as they experienced prolonged survival.

Fritsche et al. 19 concluded that (a) plasmacytoid urothelial carcinoma is a rare variant of urothelial carcinoma with defined clinical and pathological characteristics; (b) diagnostic pitfalls include the absence of haematuria and of grossly identifiable tumour, despite a muscle-invasive tumour stage; and (c) some cases show mucosal induration and thickened bladder walls. In addition, the data found by Fritsche et al. 19 raise the possibility that the loss of E-cadherin expression is a prerequisite for plasmacytoid urothelial carcinoma and awareness of these aspects should lead to earlier diagnosis and improved long-term survival in patients with plasmacytoid urothelial carcinoma.

In 2009, the plasmacytoid variant of urothelial carcinoma was reported to be rare as, up until then, only 40 cases had been reported in the English literature.20 Niqweker et al. 20 reported a series of 17 cases of urothelial carcinoma with plasmacytoid features and their associated clinicopathological findings constituted the largest reported series in the literature at that time. The authors summarized their findings as follows:

  • The architectural pattern of the tumour was highly variable and included, in decreasing order of frequency, cells arranged in cords and single cells, solid sheet-like growths, diffuse dyscohesive patternless architecture and small nests.

  • The plasmacytoid component of the specimens analysed varied from 15% to 100%. In 12 cases, the plasmacytoid component was more than 50% of the tumour.

  • The individual tumour cells had striking morphological overlap, with plasma cells with an eccentrically placed nuclei and abundant amphophilic to eosinophilic cytoplasm. The nuclei were of low to intermediate nuclear grade with minimal nuclear pleomorphism.

  • Thirteen of 17 cases (76%) were associated with conventional high-grade invasive urothelial carcinoma and nine cases (53%) exhibited very focal intracytoplasmic vacuoles mimicking signet ring cells. One case (6%) also exhibited sarcomatoid dedifferentiation.

  • With regard to immune staining, the tumour cells were positive for CK7 (94%) and CK20 (31%); CD138 was positive in 94% of cases.

  • All tumours were invasive, in seven cases into at least the lamina propria, in seven into at least the muscularis propria and in three cases into the perivesical fat.

  • Follow-up information was available in 16 cases (mean 10 months, median 5.5 months, range 2–43 months). Five patients were alive with disease but 11 patients had died.

Niqwekar et al. 20 concluded that:

  • The plasmacytoid variant of urothelial carcinoma is an aggressive subtype that is associated with poor prognosis.

  • In limited samples, it may be misdiagnosed as chronic cystitis or plasmacytoma, a pitfall further compounded by CD138 expression.

  • Distinction from metastatic carcinoma from other sites, such as the stomach and breast, is critical in view of differing therapeutic implications.

Nabbout et al. 3 reported the case of a 75-year-old man with a presumed history of high-grade urothelial carcinoma of the urinary bladder who underwent transurethral resection of bladder tumour and instillations of BCG in 2004. Six years following treatment, he underwent gastrectomy for an undifferentiated carcinoma of the stomach. Over the course of follow-up, the patient developed right hydroureteronephrosis and peritoneal carcinomatosis. He underwent insertion of ureteric stent, during which a biopsy was taken from the bladder. Histological examination of this specimen revealed a plasmacytoid urothelial carcinoma of the urinary bladder. A review of the initial bladder tumour and the gastric malignancies revealed that they were also plasmacytoid carcinomas, which indicated that the patient had a plasmacytoid urothelial carcinoma of the urinary bladder that had spread to the stomach and peritoneal cavity. The authors suggested that, based upon their case and the literature review, this type of tumour may be misdiagnosed because of its rarity, leading to a delay in treatment. They also recommended that urologists and pathologists should have a high index of suspicion for plasmacytoid urothelial carcinoma whenever they encounter unusual clinical and/or pathological findings.

Peck et al. 21 reported a 57-year-old man with a history of hypertension who presented with shortness of breath, intermittent substernal chest pain, subjective fevers and weight loss of 30 pounds. Four months prior to this presentation, cystoscopy revealed a bladder mass that was surgically removed. Histological examination of the specimen revealed a high-grade superficial plasmacytoid urothelial carcinoma that had extended into the submucosa but not the muscularis propria. In view of the superficial nature of the carcinoma of the urinary bladder, cystectomy was deferred. During this presentation, his physical examination revealed tachycardia, tachypnoea and distant heart sounds. The patient underwent electrocardiography, which revealed an incomplete right bundle branch block as well as sinus tachycardia. Subsequent CT–pulmonary angiography revealed a 3-cm pericardial effusion and transthoracic echocardiography confirmed the findings and also revealed a mass in the right ventricle extending into the outflow tract and infiltrating the free wall. The right ventricle was dilated with an estimated right ventricular systolic pressure of 37 mmHg. He had pericardiocentesis, which yielded nearly 1 litre of serosanguinous fluid with no diagnostic cytology. He then underwent partial median sternotomy with biopsy, which showed pathological findings consistent with metastatic plasmacytoid urothelial carcinoma. Positron emission tomography revealed increased uptake exclusively in the heart. The oncology team discussed the management options with the patient and these included chemotherapy and palliative care. The patient decided to decline further therapy and was discharged into the care of a hospice and died 2 months later. Peck et al. 21 stated that, at the time of publication, they were aware of only three other reported instances of isolated cardiac metastasis with urothelial bladder origin, none of which was the plasmacytoid variant.

Wang et al. 1 reported the clinical and histopathological features for a new case of plasmacytoid urothelial carcinoma. They stated that, by combining their reported case with the findings of previous reported cases, they intended to provide a therapeutic and prognostic guidance for the disease. Wang et al.’s1 index case was a patient who complained of lower abdominal pain but had no urological symptoms. The patient underwent radical cystectomy and representative sections of the tumour were submitted for immunohistochemical analysis. They collected the patient’s data from clinical charts, histological review and follow-up studies. They also undertook an extensive literature review of plasmacytoid urothelial carcinoma and documented the clinical presentation, pathological features, therapy and prognosis. Their findings can be summarised as follows:

  • Clinically, plasmacytoid urothelial carcinoma is associated with non-specific abdominal pain but absent haematuria.

  • Cystoscopic analysis has revealed that the plasmacytoid urothelial carcinoma is characterised by coarse indurated mucosal folds.

  • Macroscopic studies revealed an ulcerated firm mass in the left lateral wall of the bladder.

  • Histologically, plasmacytoid urothelial carcinoma appears to comprise dyscohesive, plasmacytoid cells with eccentric nuclei and abundant eosinophilic cytoplasm with characteristics of plasmacytoid morphology.

  • The tumour cells were negative for E-cadherin but positive for CD138 expression.

  • Their reported patient died 3 months after radical cystectomy and a single course of adjuvant chemotherapy.

  • Their literature review revealed that most cases of plasmacytoid urothelial carcinoma showed similar clinical and pathological features along with poor prognosis.

Wang et al. 1 concluded that plasmacytoid urothelial carcinoma is a rare tumour that is associated with poor prognosis because it is typically at an advanced clinical stage at the time of its diagnosis and because diagnosis is frequently delayed owing to the late occurrence of haematuria and the absence of papillary mucosal surface at diagnosis. The diagnosis is based upon the typical histological features, clinical history and immunohistochemical results.

Wang et al. 1 suggested that other than radical cystectomy, postoperative adjuvant treatment could be a good approach to a prolonged survival time for plasmacytoid urothelial carcinoma patients.

Lopez-Beltran et al. 16 presented the clincopathological features of 11 cases of plasmacytoid urothelial carcinoma. They reported that the plasmacytoid component of the tumour specimen varied from 30% to 100%; in eight cases the plasmacytoid component constituted more than 50% of the tumour, while two cases were purely plasmacytoid. The architectural pattern varied from solid expansile nests with non-cohesive cells to mixed solid and alveolar growth; a streaking dyscohesive architecture was also present in 18% of cases. Histological examination of the tumours revealed that the individual tumour cells had eccentrically placed nuclei and abundant eosinophilic cytoplasm reminiscent of plasma cells. Most of the neoplastic cells had nuclei of low to intermediate nuclear grade and occasional nuclear pleomorphism. Seven of the nine mixed cases had concurrent high-grade urothelial carcinoma and the remaining two cases exhibited features of nested or micropapillary urothelial carcinoma. Small intracytoplasmic vacuoles were variably present in all cases. All patients suffered from advanced cancer (> pT3) and eight patients (73%) had lymph node metastasis. Lopez-Beltran et al. 16 also reported that immunohistochemical staining demonstrated that both plasmacytoid and associated conventional urothelial carcinoma were positive for CKs 7 and 20 and AE1/AE3 and the EMA, CD138, was positive in three cases. They also reported that follow-up data were available in all cases (mean 7 months and range 2–16 months). Nine of the patients died of the disease after 2–11 months; two patients were alive with disease at 8 and 16 months.

Rahman et al. 4 reported the case of a 54-year-old man with a history of smoking who presented with haematuria and lower abdominal pain. He underwent cystoscopy, which revealed oedema and ulceration of the entire bladder mucosa. CT of the abdomen and pelvis showed a thickened urinary bladder wall with irregularity of the mucosa involving the whole bladder. The other pelvic and abdominal organs were unremarkable. Transurethral bladder biopsy revealed a malignant urothelial tumour with plasmacytoid appearance. The patient then underwent radical cystectomy and histological examination of the specimen revealed a grey/white and firm to hard, ill-circumscribed ulcerative tumour that had involved almost the entire bladder and measured 2 cm in thickness. The tumour had infiltrated the perivesical fat as far as the circumferential margin. Microscopic examination revealed a high-grade tumour that was composed of dyscohesive plasmacytoid cells replacing the lamina propria; the tumour cells were observed to have extended from the mucosal aspect through the detrusor muscle to invade the perivesical fat and serosa. There was evidence of perineural invasion. The tumour cells were seen extending along the adventitia of both ureters and even up to the surgical cut margins, and were also seen undermining the prostatic urothelial lining. The distal urethral cut margin was also encompassed by the tumour but the bilateral iliac lymph nodes were free of tumour invasion. Immunostaining revealed that the tumour cells were positive for CK7 and CD138 and negative for leucocyte common antigen and CD20 as well as kappa and lambda light chains. Rahman et al. 4 did not report the follow-up data or outcome of the patient.

Manousakas et al. 22 reported the case of a 52-year-old man who had been suffering from gross haematuria for 2 years. He underwent ultrasonography, intravenous urography and CT of the abdomen, which revealed a diffuse mass occupying most of the urinary bladder but no evidence of upper urinary tract involvement or locoregional metastatic disease. Subsequent cystoscopy revealed a huge sessile tumour of the dome of the bladder, which was resected. Histological examination of the specimen showed a diffuse monotonous cellular infiltration that invaded the lamina propria and muscularis propria. The tumour cells were medium-sized and round with eosinophilic cytoplasm and eccentric nuclei, producing a plasmacytoid appearance. The tumour cells were in continuum with the overlying urothelium. Immunoperoxidase staining of paraffin-embedded sections revealed strong diffuse intracytoplasmic staining for CKs (low/high molecular weight) and EMA in tumour cells, confirming their epithelial origin. There was no reactivity for leucocyte common antigen, kappa and lambda light chains, S-100 protein or neuroendocrine markers (neurone-specific enolase, chromogranin, synaptophysin).

Based upon the histological findings and immunophenotype, the carcinoma was characterized as plasmacytoid transitional cell carcinoma. The patient received six monthly courses of adjuvant chemotherapy (methotrexate, vinblastine, doxorubicin and cisplatin). He tolerated the chemotherapy relatively well, with the principal side-effects being moderate haematological toxicity and mild mucositis. Eight months after the initial operation, the patient was re-evaluated and a follow-up cystoscopy revealed a small recurrence (< 2 cm) at the dome of the urinary bladder, which was resected. Histological examination of the resected specimen revealed identical morphological and immunohistochemical features; however, this time the tumour involved the lamina propria only (pT1a) and the patient was disease free 11 months after the resection. Manousakas et al. 22 stated that:

  • Their case was the fourth case of plasmacytoid transitional cell carcinoma of the urinary bladder to be reported and the second case to be confined to the urinary bladder.

  • Lymphomas and plasmacytomas usually involve the urinary bladder secondarily and may respond to systemic chemotherapy.

  • In contrast, first-line therapy for invasive, non-metastatic transitional cell carcinoma is urinary cystectomy.

  • Although there is very little experience in managing plasmacytoid transitional cell carcinoma, it seems that plasmacytoid transitional cell carcinoma of the urinary bladder responds to chemotherapy.

  • Their patient received adjuvant chemotherapy successfully and was disease free for 9 months after the second resection; two of the other three reported patients who also underwent chemotherapy were disease free for at least 1.5 years. Therefore, an attempt to preserve the bladder should be made in patients with plasmacytoid transitional cell carcinoma.

Nicolas et al. 23 reported two cases of plasmacytoid urothelial carcinoma of the urinary bladder as follows.

  • Case 1 A 58-year-old man presented with abdominal pain and changes in his bowel habit. He underwent CT, which revealed thickening of rectal wall and a pararectal mass. Subsequent colonoscopy did not reveal any mucosal lesions in the large bowel, and cystoscopy revealed an irregular and erythematous bladder mucosa that was biopsied. Histological examination of the specimen showed an invasive high-grade urothelial carcinoma and urothelial carcinoma in situ. Transrectal biopsy of the pararectal mass also revealed the presence of high-grade carcinoma; therefore, the patient was given neoadjuvant chemotherapy. Four months later, he developed a perineal mass and a separate scrotal mass. Excision of the mass lesions in the perineum and scrotum revealed a carcinoma histologically similar to the tumours from the urinary bladder and pararectal region. He received radiotherapy to the perineum and scrotum and subsequently underwent imaging procedures that revealed the spread of tumour to the perineum, abdominal wall, axilla and biliary tree, which necessitated biliary stent placement.The routinely processed tissue sections that were stained with haematoxylin and eosin were reviewed. Among the histological findings were that the tumour in the urinary bladder was composed of dyscohesive polygonal to round tumour cells with pleomorphic nuclei and scant to moderate pink cytoplasm; many of the tumour cells had eccentrically located nuclei that resembled plasma cells; the muscularis propria was infiltrated by dispersed tumour cells arranged in clusters or single files; rare signet ring cells were noted; and urothelial carcinoma in situ was found in the bladder mucosa. In addition, sections of the scrotal, pararectal and axillary lesions revealed similar-appearing infiltrating tumour cells, the urothelial carcinoma in situ and invasive carcinoma of the urinary bladder were positive for CK7 and CK20 by immunohistochemistry, which was performed using the standard avidin–biotin technique, and the infiltrating scrotal carcinoma was positive for CK7 and focally positive for CK20.

  • Case 2 A 56-year-old man presented with haematuria and underwent cystoscopy, which revealed a urinary bladder mass and areas of erythema of the mucosa of the urinary bladder. Biopsies of the tumour and urinary bladder mucosa revealed a muscle-invasive high-grade urothelial carcinoma and urothelial carcinoma in situ. The patient underwent a negative preoperative radiological workup in advance of a cystoprostatectomy. Macroscopic examination of the specimen revealed a focally ulcerated and ill-defined mass lesion in the urinary bladder, which was associated with bladder wall thickening. The prostate gland was grossly uninvolved and microscopic examination of the tissue sections revealed an infiltrating tumour that was composed of round and polygonal plasmacytoid cells arranged in loose clusters and dispersed single cells. Urothelial carcinoma in situ was found in the urinary bladder and prostatic urethra. High-grade papillary urothelial carcinoma was also identified and there was a transmural infiltration of the tumour cells into the perivesical adipose tissue through the muscularis propria. Tumour cells were also observed in soft tissue surrounding the seminal vesicles. Signet ring cells were present and intracytoplasmic mucin was exhibited in these cells. Metastatic carcinoma in a perivesical lymph node was found. The tumour cells in the lymph node appeared in clusters as well as single cells and extended to the perinodal soft tissue.

There have not been any documented reports of plasmacytoid urothelial carcinoma involving the ureter prior to 2013. However, in 2013, Chang et al. 24 reported a case of a 75-year-old woman who presented with left flank pain and gross haematuria that she had been suffering from for a period of 1 day. She underwent CT, which revealed a mass occupying the upper third of the left ureter. Ureteroscopic biopsy of the lesion confirmed it was malignant, and thus left nephroureterectomy with excision of the bladder cuff was performed. Follow-up cystoscopies at 4 months and again at 9 months post operation revealed multiple recurrent tumours in her urinary bladder, and these were resected on each occasion. The patient was alive without any evidence of recurrence at her latest follow-up 12 months after the initial diagnosis.

Following macroscopic examination, the original tumour was found to be located in the wall of the ureter with an exophytic growth pattern and measured 1.5 cm × 1.3 cm × 0.3 cm. Microscopic examination revealed mixed architectural patterns of both conventional high-grade infiltrating urothelial carcinoma at the bottom and plasmacytoid variant of urothelial carcinoma at the top. The tumour contained solid expansile nests of neoplastic epithelial cells infiltrating into the muscularis. The plasmacytoid variant showed mixed diffuse and alveolar growth patterns of non-cohesive neoplastic cells bearing eccentrically placed nuclei and amphophilic cytoplasm with eosinophilic paranuclear reminiscent of plasma cells. The plasmacytoid component constituted 35% of the tumour in the specimen. There was no evidence of regional lymph node or lymphovascular invasion. The bladder cuff and radial margins were free from tumour involvement but the pathological stage of the ureteral tumour was pT2N0Mx. Immunohistochemical staining revealed that both the plasmacytoid and conventional urothelial carcinoma were positive for CK7, CK20, high-molecular-weight CK [clone 34beta(β)E12], low-molecular-weight CK (clone 35βH11) and CD138. A strong membranous staining of E-cadherin was detected in the conventional urothelial carcinoma. In contrast, the plasmacytoid component exhibited markedly reduced E-cadherin staining. Furthermore, both components were immunoreactive to β-catenin in mainly membranous cytoplasmic patterns: CD3, CD20, CD79a and MUM-1, and kappa and lambda light chain were negative in both components. The bladder tumours that were resected at the subsequent follow-up appointments (at 4 and 9 months) showed conventional high-grade infiltrating urothelial carcinoma that had invaded the subepithelial connective tissue (pT1).

Demirovic et al. 25 reported the case of a 76-year-old man who presented with painless, but visible, haematuria. He underwent cystoscopy, which revealed a smooth-surfaced bladder tumour near the left vesicoureteral orifice and measured 5 cm. He underwent incomplete transurethral resection of the bladder tumour and 20 sections of the tumour measuring 0.7 cm each were sent to the pathology department. Histological examination of the specimen revealed small nests and individual atypical epithelial cells resembling plasma cells. The tumour cells infiltrated the muscularis propria. Magnetic resonance imaging (MRI) showed a tumour that was located to the left of the posterior bladder wall and measured up to 5 cm in diameter at its largest. The tumour exhibited signs of infiltration of the left vesicoureteral orifice with left-sided hydronephrosis and perivesical adipose tissue infiltration. Intravenous urography revealed no contrast opacification of the left renal pelvis but showed a large filling defect of the left bladder contour, which measured up to 5 cm and resulted in the patient having to undergo radical cystoprostatectomy. Macroscopically, the tumour measured up to 4.5 cm and extended beyond the bladder wall but not into the prostate. Subsequent histological examination of the specimen showed invasive urothelial carcinoma with plasmacytoid features and foci of micropapillary growth. The plasmacytoid tumour cells constituted more than 50% of the tumour tissue and were dyscohesive and round to oval in shape with abundant eosinophilic cytoplasm and eccentrically placed nuclei. Immunohistochemical staining of the tumour revealed diffuse intracytoplasmic staining for EMA and pancytokeratin. The majority of the cells exhibited a diffuse positive intracytoplasmic reaction for CD138. Immunohistochemical analysis of the tumour cells that constituted micropapillary growth depicted a diffuse positive intracytoplasmic reaction for EMA and pancytokeratin and only a focally positive intracytoplasmic reaction to CD138. The tumour cells penetrated the perivesical adipose tissue with perineural and perivesical invasion. Additional chemotherapy was given and, 8 months after cystoprostatectomy, the patient was alive and there were no signs of tumour spread.

Ro et al. 6 reported nine cases of plasmacytoid transitional cell carcinoma of the urinary bladder. All nine patients were men with a mean age of 64.3 years (range 46–81 years). Eight of the patients presented with visible haematuria and the remaining patient presented with urinary urgency and microscopic haematuria. Ro et al. 6 also reported that the cystoscopic examination of the patients revealed a dominant solid mass with surrounding multiple papillary lesions in six cases and multiple massive lesions in three other cases. Plasmacytoid transitional cell carcinoma was initially diagnosed following transurethral resection in eight cases and cystoscopic biopsy in one case. The tumour, nodes, metastases (TNM) stage of one patient was stage I; two patients had stage II disease, three had stage III disease and three had stage IV disease. Four of the patients were treated by radical cystectomy with chemotherapy, two by radical cystectomy alone and one each by chemotherapy or intravesical BCG alone; one did not receive any further treatment. Microscopic examination of the tumours showed that all the tumours contained plasmacytoid cells, which constituted 30–100% of the entire tumour. Eight of the nine cases were associated with high-grade transitional cell carcinoma, and transitional cell carcinoma in situ was apparent in four cases. The plasmacytoid cells were characterized by eccentrically located nuclei and abundant eosinophilic cytoplasm and plasmacytoid transitional carcinoma in situ was present in one case. Ro et al. 6 also reported that immunohistochemical staining showed that both the plasmacytoid and conventional transitional cell carcinoma components of the tumour were positive for CK7 and CK20. The mean Ki-67 labelling index was 30% (range 10–50%) and p53 expression in the majority of cases was low (5–10%), except for two cases (70% and 80%). The mean follow-up of eight of the patients was 24.5 months (range 5–47 months) and the ninth patient was lost to follow-up. With regard to outcome, Ro et al. 6 reported that five patients died 5–36 months after treatment, two patients were alive with the disease at 30 and 47 months and one patient was alive and well at 36 months, with no evidence of disease. Ro et al. 6 concluded that plasmacytoid transitional cell carcinoma tends to present at an advanced stage and is associated with a poor prognosis and that morphological recognition and distinction from other plasmacytoid malignant neoplasms is critical for its clinical management. In addition, immunohistochemical studies may be required for differential diagnosis.

Mai et al. 26 reported seven cases of plasmacytoid urothelial carcinoma of the urinary bladder in patients who were reviewed in their institution. These seven cases were evaluated from 260 cases of invasive urothelial carcinomas that had been reviewed over a period of 7 years to identify plasmacytoid urothelial carcinoma. The authors submitted representative sections from each of the seven cases for immunohistochemical study. They reported that the common type of urothelial carcinoma was present in focal areas in five cases, and cases with extensive plasmacytoid urothelial carcinoma showed coarse and indurated mucosal folds and thickened bladder walls, with no grossly identifiable tumour. Urine cytology showed a scant number of atypical cells, frequently without tumour diathesis, leading to a shortfall in positive cytological diagnosis. Histologically, plasmacytoid urothelial carcinoma appeared as dyscohesive, plasmacytoid cells with eccentric nuclei extending widely into the bladder walls and extensively into adjacent pelvic organs.

Gaafar et al. 27 reported seven cases of plasmacytoid urothelial carcinoma that were found among 720 high-grade urothelial carcinomas of the urinary bladder. They reported that, in their series, 0.97% of high-grade urothelial carcinomas of the urinary bladder exhibited a plasmacytoid phenotype. All the patients were male smokers aged between 58 and 75 years. Histologically, two cases showed pure plasmacytoid features; in the remaining five cases, the plasmacytoid phenotype was mixed with conventional transitional cell or glandular histology. All the plasmacytoid areas showed fair epithelial differentiation. The clinical behaviour of the tumour was aggressive in all the cases, with distant metastases at diagnosis in three cases and early tumour recurrence after chemotherapy in four cases. Gaafar et al. 27 concluded that, in their experience, plasmacytoid urothelial carcinoma of the urinary bladder is a rare tumour that can be detected in association with areas of conventional urothelial carcinoma and it is mandatory to recognize this histological subtype owing to the clinical and prognostic implications of its diagnosis.

Ricardo-Gonzalez et al. 17 identified cases of plasmacytoid urothelial carcinoma that were diagnosed on cystectomy and they documented the patients’ age, sex, American Joint Committee on Cancer stage, metastatic spread/recurrence, sites and clinical disease status at last follow-up. The 10 male and five female patients were aged between 42 and 81 years. One tumour was stage pT2, 11 were stage pT3 and three were stage pT4. Six of the 15 patients (40%) presented with lymph node metastasis and 5 (33%) had intraperitoneal metastasis at cystectomy. This initial metastatic spread was seen in the prerectal space, ovary and vagina, ovary and fallopian tube, bowel serosa and omentum and bowel serosa in one case each. Three patients subsequently developed metastasis involving the prerectal space, pleural fluid and small bowel serosa and bowel serosa in one case each. Follow-up information was available for eight patients: three who died of disease, three living with disease and two with no evidence of disease. The authors concluded that, of all the patients, 33% with plasmacytoid variant of urothelial carcinoma presented with intraperitoneal disease spread and 20% had subsequent metastasis involving serosal surfaces. The possibility of non-contiguous intraperitoneal spread involving serosal surfaces should be recognized to ensure proper intraoperative staging and clinical follow-up for patients with plasmacytoid carcinoma.

Dayyani et al. 28 conducted a retrospective analysis of treatments and outcomes in patients with predominant plasmacytoid urothelial carcinoma who were treated at the MD Anderson Cancer Center from 1990 to 2000. They used the Kaplan–Meier method to calculate overall survival and progression-free survival. They identified 31 patients (median age 63.5 years, 83.3% male, four with TNM stage cT1N0, seven with stage cT2N0, five with stage cT3b–4aN0 and 15 with stage cT4b, N+ or M+). They reported that the mean overall survival for all patients was 17.7 months (stages I–III vs. IV: 48.5 months vs. 13.3 months). Of the 16 patients with potentially surgically resectable plasmacytoid urothelial carcinoma (≤ stage pT4a, N0, M0), five received neoadjuvant chemotherapy, 10 had initial surgery and one was treated with transurethral resection of bladder tumour alone. Despite pathology downgrading in 80% of patients who were treated with neoadjuvant chemotherapy, relapses were common and there was no difference in survival between patients who were treated with neoadjuvant chemotherapy and those treated with initial surgery, although adjuvant chemotherapy was given to seven patients only. Surgical upstaging with positive margins was also common with surgery alone. The most common site of recurrence was in the peritoneum (19/23), with relapses occurring even in those with a pathological complete response during surgery. They also reported that the median survival for patients who presented with metastatic disease and were treated with chemotherapy was 12.6 months. Dayyani et al. 28 concluded that plasmacytoid urothelial carcinoma is a very aggressive tumour subset with a poor overall outcome and, although neoadjuvant chemotherapy can result in downstaging, there are few long-term survivors and there is a strong predilection for recurrences along the peritoneal lining.

Sakuma et al. 29 reported two cases of plasmacytoid urothelial carcinoma of the urinary bladder. Both cases were of advanced cancer with extravesical invasion and lymph node metastases as well as coexisting prostatic carcinoma; one was preoperatively diagnosed and the other was incidentally found after surgery. The authors stated that these two cases were the first reported cases of plasmacytoid urothelial carcinoma simultaneously associated with prostatic carcinoma.

Tanaka et al. 7 reported the case of an 85-year-old man who presented with visible haematuria and painful urination. He underwent cystoscopy, which revealed a non-papillary tumour at the bladder neck, extending to the trigone. CT revealed thickening of the bladder wall in the same area but no lymph node swelling. His urine cytology was reported as class IIIb (suspicious). Transurethral resection of the bladder tumour and histopathological examination of the specimen showed urothelial carcinoma, G3 pT2. Six days post operation, the patient developed a severe fever which persisted despite administration of various antibiotics and his general condition deteriorated. He died from an acute myocardial infarction 37 days following his operation. Histopathological examination at autopsy revealed extensive urothelial carcinoma, a plasmacytoid variant of bladder cancer that had invaded his lungs, liver, kidneys, adrenal glands and veins, even though tumour cells were not identified in the lymph nodes.

Zukerberg et al. 30 reported five carcinomas of the urinary bladder, four transitional cell carcinomas and one undifferentiated carcinoma, with unusual features that had received little comment in the literature but which the authors suggested may be the cause of diagnostic difficulty in view of their possible confusion with malignant lymphoma. At that time, the terminology of plasmacytoid urothelial carcinoma of the urinary bladder had not been added to the WHO classification of variants of urothelial carcinoma. Four patients were male and one was female and they were aged between 61 and 76 years. Three of the tumours had a prominent (two cases) or massive (one case) lymphoid infiltrate that partially obscured the invasive carcinoma in two cases and largely obscured it in the third case, closely resembling a lymphoepithelioma. The diagnosis of malignant lymphoma was excluded with confidence in the final case only after thorough immunohistochemical study. The lymphoid infiltrate was composed of numerous T-cells [ubiquitin carboxy-terminal hydrolase L1 (UCHL-1) and Leu 22 positive] and polytypic plasma cells with admixed eosinophils. Occasional germ centres were present in one case and the tumours were deeply invasive in two patients, one of whom was alive with no evidence of the disease 4 years after treatment with chemotherapy and radiotherapy; however, the other two cases were too recent for a meaningful follow-up. The two other transitional cell carcinomas had diffuse patterns that simulated lymphoma or plasmacytoma. Zukerberg et al. 30 stated that the recognition of these patterns of vesical carcinoma was important in order to avoid the misdiagnosis of the very rare malignant lymphoma. Zukerberg et al. 30 reported these five cases before the inclusion of the terminology of plasmacytoid urothelial carcinoma in the WHO classification during 2004 and it is possible that one or two of the cases reported by Zukerberg et al. 30 would be classified as plasmacytoid urothelial carcinoma today if all the slides were reviewed and further immunohistochemical studies were carried out.

Kohno et al. 18 reported the case of a 76-year-old man who was diagnosed with plasmacytoid urothelial carcinoma (T4, N0, M0) based on the microscopically plasmacytoid appearance of the specimen following transurethral resection. Immunohistochemical studies were positive for epithelial markers and negative for lymphoid markers. He received two cycles of systemic chemotherapy with methotrexate, etoposide, vinblastine and cisplatin followed by radical cystectomy. The pathological examination revealed no residual cancer cells in the resected specimen and the authors stated that their case was the first case of pathological complete response for plasmacytoid urothelial carcinoma of the bladder.

Mitsogiannis et al. 31 reported the case of a 60-year-old man who presented with end-stage disease which did not allow for efficacious therapy. Immunohistochemistry revealed the tumour cells to be reactive for epithelial markers and syndecan-1 (CD138), consistent with plasmacytoid urothelial carcinoma of the urinary bladder.

Sato et al. 32 reported the case of a 50-year-old man who presented with pollakiuria and urinary incontinence. MRI detected a bladder tumour invading the rectum and associated bilateral hydroureteronephrosis. Radical cystectomy with partial resection of the rectum was performed. However, the patient developed ileus due to peritoneal dissemination of the tumour 2 years after his operation and he died 42 months after the initial presentation. Histological examination of the cystectomy specimen revealed urothelial carcinoma in situ with a focal invasive urothelial component and widespread plasmacytoid urothelial carcinoma. There was no lymph node metastasis and the plasmacytoid urothelial carcinoma cells were reported to have eccentrically placed nuclei and eosinophilic cytoplasm resembling plasmacytoid cells and to have proliferated with a single-cell infiltrative pattern to the outside of the bladder. Invasive urothelial carcinoma cells with intracytoplasmic lumina were focally intermingled with plasmacytoid urothelial carcinoma cells. Sato et al. 32 also reported that immunohistochemical examination revealed that the plasmacytoid urothelial carcinoma cells were positive for CK7, EMA and carbohydrate antigen (CA) 19-9, but negative for CK20, E-cadherin, p63 and lymphoid markers. The Ki-67 labelling index of plasmacytoid urothelial carcinoma cells was 9.3%. Invasive urothelial carcinoma containing intracytoplasmic lumina morphologically and immunohistochemically showed intermediate levels of conventional invasive urothelial carcinoma and plasmacytoid urothelial carcinoma. Sato et al. 32 concluded that plasmacytoid urothelial carcinoma is a distinct entity of bladder cancer with a high propensity for invasion and a poor prognosis.

Shimada et al. 33 reported the case of a 46-year-old man who presented with visible haematuria and increased serum concentrations of CA 19-9 and β-human chorionic gonadotrophin (β-HCG) levels. He underwent transurethral resection of bladder tumour followed by radiotherapy and chemotherapy. The tumour was composed of both conventional urothelial carcinoma and a plasmacytoid variant and both components of the tumour were positive for epithelial markers. In addition, the plasmacytoid cells were positive for an accepted marker of plasma cell origin, CD138. CA 19-9 was mainly expressed in conventional urothelial carcinoma cells and β-HCG was mainly produced by plasmacytoid tumour cells. The patient died of the disease 24 months after presentation. According to the authors, their case was, to their knowledge, the first reported case to indicate that β-HCG can be produced by plasmacytoid bladder cancer cells lacking trophoblastic features.

Soylu et al. 34 reported the case of a 67-year-old man who was diagnosed with an aggressive urothelial carcinoma which was classified as lipid cell variant with plasmacytoid features. He survived for 18 months after surgery (insertion of percutaneous bilateral nephrostomies and salvage cystectomy) followed by chemotherapy. The histopathological features of the tumours were the same in each recurrence.

Naselli and Spine35 reported two cases of plasmacytoid urothelial carcinoma of the urinary bladder as follows.

  • Case 1 The first patient was a 67-year-old man who presented with gross haematuria. Ultrasonography of the renal tract was found to be normal. As cytological examination revealed the presence of low-grade tumour cells in his urine, cystoscopy was performed, which revealed a 1-cm papillary tumour on the left lateral wall of the bladder extending distally to the left ureteric orifice. He underwent transurethral resection of bladder tumour. Histological examination of the resected tumour revealed a high-grade muscle-invasive tumour, which was staged as a pT2 tumour, and evidence of a plasmacytoid urothelial carcinoma near the edge of a conventional low-grade conventional papillary urothelial neoplasm. CT of the thorax, abdomen and pelvis and isotope bone scanning did not reveal any metastasis. He then underwent radical cystectomy and an ileal conduit operation and was discharged after 2 weeks. Macroscopic examination of the specimen revealed an area of ulceration associated with thickening of the bladder wall and the presence of neoplastic white-grey bundles on the cut surface. Microscopic examination revealed that the tumour was predominantly characterized by a relatively uniform population of dyscohesive round to ovoid cells, with diffuse plasmacytoid features and abundant intensely eosinophilic cytoplasm and eccentrically located nuclei, but indistinct nuclei and sparse chromatin. The tumour cells invaded the muscularis propria of the bladder wall and the perivesical adipose tissue, often arranged in single file and surrounded by a myxoid stroma. Rare superficial areas morphologically consisting of conventional papillary urothelial carcinoma were observed in the tumour. No neoplastic invasion of blood vessels or nervous structures was detected. The prostate and seminal vesicles were free of disease and no metastasis was observed in the examined lymph nodes. He then received cisplatin-based chemotherapy and regular follow-up by CT and urethroscopy. Two years after this treatment, the follow-up investigations revealed disease in the form of peritoneal and retroperitoneal metastases causing intestinal obstruction and obstructive acute renal failure and ascites. He underwent insertion of a left percutaneous nephrostomy, a palliative transversostomy and peritoneal drainage but he subsequently died approximately 33 months after his operation from septic complications.

  • Case 2A 72-year-old man presented with urinary urgency and frequency. Urinalysis and urine cytology were normal; however, ultrasonography of the renal tract showed left-sided hydronephrosis and a post-voiding residual volume of 60 ml, with protrusion of the middle lobe into the bladder. Cystoscopy showed no evidence of abnormality of the urothelial mucosa so CT urography was performed. This also failed to show any evidence of a lesion in the upper urinary tract; it showed only thickness of the bladder wall. The patient was scheduled for transurethral resection of the prostate and 1 month later was admitted to the emergency room for anuria secondary to acute renal failure. His serum creatinine level was 12 mg/dl and abdominal ultrasonography revealed a slight bilateral hydronephrosis. Two ureteral catheters were inserted and bladder biopsies revealed a neoplasm of urothelial origin. Again, the bladder mucosa appeared normal during the endoscopic inspection but later MRI revealed a bulky mass between the rectum and bladder extending proximally to the retroperitoneum. An exploratory open procedure was performed; however, it was impossible to develop the retropubic space. After opening the peritoneum, a solid mass infiltrating the peritoneal cul-de-sac was noted and biopsied. The ureters were then isolated in the retroperitoneum and an ileal conduit constructed. The pathological examination of the biopsies revealed a plasmacytoid urothelial carcinoma. The resulting health of the patient was poor and he died within 2 months as a result of complications secondary to the local progression of the disease.

Conclusions

Plasmacytoid urothelial carcinoma of the urinary bladder is a rare tumour that may present with haematuria, lower urinary tract symptoms or non-specific abdominal symptoms.

Diagnosis of plasmacytoid urothelial carcinoma of the urinary bladder can be established based upon its characteristic histological/morphological features of dyscohesive, plasmacytoid cells with eccentric nuclei and abundant eosinophilic cytoplasm. Immunohistochemical stains for plasmacytoid urothelial carcinoma usually stain positively for CK7, CK20, and CD138 and negatively for E-cadherin. Plasmacytoid urothelial carcinomas of the urinary bladder are usually high stage and high grade and associated with poor prognosis and, ultimately, death of the patient. However, there are reports of improved survival following radical cystectomy and neoadjuvant/adjuvant chemotherapy. In view of the rarity of plasmacytoid urothelial carcinoma and lack of consensus on which chemotherapeutic regimen should be the first choice adjunctive treatment, we would recommend that urologists and oncologists throughout the world submit their patients who are suffering from plasmacytoid urothelial carcinoma of the urinary bladder to a multicentre trial in order to arrive at a consensus regarding the best treatment chemotherapy regimen for such patients.

Acknowledgement

We would like to thank Dr Brian Benatar, Consultant Histopathologist at Royal Oldham Hospital, UK, for his help and support with taking the photographs to illustrate the pathological features of plasmacytoid urothelial carcinoma.

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