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Clear cell carcinoma of the urinary bladder: a systematic review

  • Urology - Review
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Purpose

We conducted a systematic review of the literature on primary clear cell carcinoma (CCC) of the urinary bladder.

Methods

A literature search using keywords and MeSH terms related to “clear cell carcinoma”, “clear cell adenocarcinoma”, “mesonephroma” and “urinary bladder” in EMBASE, MEDLINE and Cochrane Central Register of Controlled Trials was performed. A manual search was performed with web-based search engine Google Scholar. Reference lists of the included studies were screened for additional articles. Articles up till 16th July 2020 were retrieved. Observational human studies on primary CCC in urinary bladder with English full-text were included for further analysis.

Results

904 articles were identified and 44 articles were included for further analysis. Data including clinical features, tumour characteristics, treatment and oncological outcomes were reviewed. There were 70 patients (44 females and 26 males) reported in literatures and included in this review. Gross haematuria was the most common presentation (79.7%), followed by irritative urinary symptoms (47.5%). Regarding the histology, tubulocystic pattern is the most common histologic pattern (49.1%), and 52.6% had muscle invasion. Most cases were CK7 (96.6%) and CK20 (88.9%) positive. CA125 (96%) was commonly positive, indicating its potential origin from mullerian duct. Most patients received surgery (95.5%) as primary treatment. However, the oncological outcomes were unsatisfactory with a 2-year survival rate of 60.0%.

Conclusion

Clear cell carcinoma is an uncommon subtype of bladder cancer which can be diagnosed by histology and immunohistochemical staining result. The majority of patients presented with muscle invasion and had a poor survival despite aggressive treatment.

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Author information

Authors and Affiliations

  1. Department of Surgery, S.H. Ho Urology Centre, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China

    Erica On-Ting Chan, Jade Yin-To Poon, Brian Hang-Kin Chan, Peter Ka-Fung Chiu, Chi-Fai Ng & Jeremy Yuen-Chun Teoh

  2. School of Medicine, Faculty of Medicine and Health, University of Leeds, Leeds, UK

    Vinson Wai-Shun Chan

  3. Li Ping Medical Library, The Chinese University of Hong Kong, Hong Kong, China

    Chun-Pong Yu

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Contributions

EOTC, VWSC and JYCT were responsible for study conception and design. EOTC, JYTP, BHKC and CPY were responsible for data acquisition. EOTC and VWSC were responsible for data analysis, data interpretation and drafting the manuscript. PKFC, CFN and JYCT provided critical revision for important intellectual consent.

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Correspondence to Jeremy Yuen-Chun Teoh.

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Appendices

Appendix 1

Database: EBM Reviews—Cochrane Database of Systematic Reviews < 2005 to July 10, 2020 > , EBM Reviews—ACP Journal Club < 1991 to June 2020 > , EBM Reviews—Database of Abstracts of Reviews of Effects < 1st Quarter 2016 > , EBM Reviews—Cochrane Clinical Answers < June 2020 > , EBM Reviews—Cochrane Central Register of Controlled Trials < June 2020 > , EBM Reviews—Cochrane Methodology Register < 3rd Quarter 2012 > , EBM Reviews—Health Technology Assessment < 4th Quarter 2016 > , EBM Reviews—NHS Economic Evaluation Database < 1st Quarter 2016 > , Embase Classic + Embase < 1947 to 2020 July 16 > , Ovid MEDLINE(R) and Epub Ahead of Print, In-Process & Other Non-Indexed Citations, Daily and Versions(R) < 1946 to July 15, 2020 > 

Search strategy:

––––––––––––––––––––––––––––––––––––––––

1 exp adenocarcinoma, clear cell/ or exp clear cell adenocarcinoma/ (242,436).

2 (((clear cell or clear-cell) adj2 (carcinoma or adenocarcinoma)) or CCA).tw,kw. (38,081).

3 mesonephroma*.tw,kw. (356).

4 or/1–3 (277,139).

5 exp *urinary bladder/ (62,502).

6 ((bladder or vesic*) adj3 (carcinoma or adenocarcinoma)).tw, kw. (33,635).

7 5 or 6 (93,954).

8 7 and 4 (1712).

9 (exp animals/ or exp animal/ or exp nonhuman/ or exp animal experiment/ or animal model/ or animal tissue/ or non human/ or (rat or rats or mice or mouse or swine or porcine or murine or sheep or lambs or pigs or piglets or rabbit or rabbits or cat or cats or dog or dogs or cattle or bovine or monkey or monkeys or trout or marmoset$1).tw.) not (humans/ or human/ or human experiment/ or (human* or men or women or patients or subjects).tw.) (11,407,792).

10 conference abstract.pt. or Congresses as Topic/ or Conference Review.pt. or "Journal: Conference Abstract".pt. (4,130,314).

11 note/ or editorial/ or letter/ or Comment/ or news/ or (note or editorial or letter or Comment or news).pt. (4,684,518).

12 (child/ or Pediatrics/ or Adolescent/ or Infant/ or adolescence/ or newborn/ or (baby or babies or child or children or pediatric* or paediatric* or peadiatric* or infant* or infancy or neonat* or newborn* or new born* or adolescen* or toddler*).tw.) not (adult/ or aged/ or (aged or adult* or elder* or senior* or men or women).tw.) (4,696,049).

13 or/9–12 (23,548,818).

14 8 not 13 (1231).

15 limit 14 to english [Limit not valid in DARE, CLCMR, CLEED; records were retained] (899).

16 gallbladder.ti. (39,425).

17 15 not 16 (891).

18 remove duplicates from 17 (807).

Appendix 2: List of articles

Case report

  1. 1.

    Abbas, Mahmoud, et al. “Adenocarcinoma of the urinary bladder, mesonephroid type: a rare case”. Rare tumors 5.1 (2013): 11–14.

  2. 2.

    Adams, Betsy, et al. “A rare case of clear cell adenocarcinoma of the bladder with unique pathological features”. The American journal of the medical sciences 333.1 (2007): 63–65.

  3. 3.

    Al‐Izzi, M. S., et al. “Malignant transformation in endometriosis of the urinary bladder”. Histopathology 14.2 (1989): 191–198.

  4. 4.

    Alsanjari, N., et al. “Vesical clear cell adenocarcinoma v. nephrogenic adenoma: a diagnostic problem”. Histopathology 27.1 (1995): 43–49.

  5. 5.

    Braslis, K. G. “Clear-cell transitional cell carcinoma”. Aust. NZ J. Surg. 67 (1997): 906–908.

  6. 6.

    Butterworth, D. M., N. Y. Haboubi, and E. W. Lupton. “Mixed mesonephric adenocarcinoma and transitional cell carcinoma of the bladder”. Histopathology 16.6 (1990): 601–604.

  7. 7.

    Dow, James A., and John D. Young. “Mesonephric adenocarcinoma of the bladder”. The Journal of Urology 100.4 (1968): 466–469.

  8. 8.

    Dhaliwal, Catharine A., and Paul W. Fineron. “The progression of nephrogenic metaplasia of the urinary bladder to clear cell adenocarcinoma: a case report”. Current Urology 6.2 (2012): 106–108.

  9. 9.

    Hartmann, Arndt, et al. “Molecular evidence for progression of nephrogenic metaplasia of the urinary bladder to clear cell adenocarcinoma”. Human pathology 37.1 (2006): 117–120.

  10. 10.

    HONDA, Nobuaki, et al. “Mesonephric adenocarcinoma of the urinary bladder: a case report”. (2000).

  11. 11.

    Isono, Makoto, et al. “Urothelial carcinoma clear cell variant of the urinary bladder: a case report”. Hinyokika kiyo. Acta urologica Japonica 56.3 (2010): 163–165.

  12. 12.

    ITO, Kazuto, et al. “A case of adenocarcinoma with clear cell carcinoma of the bladder”. (1999).

  13. 13.

    Jassim, Sarmad H., et al. “Concordant clear cell “mesonephric” carcinoma of the bladder and lung adenocarcinoma with clear cell features–multiple primaries versus metastatic neoplasms: a case report”. Journal of medical case reports 11.1 (2017): 1–6.

  14. 14.

    Kösem, Mustafa, and Erdal Şengül. “Clear cell adenocarcinoma of the urinary bladder”. Scandinavian journal of urology and nephrology 39.1 (2005): 89–92.

  15. 15.

    Kotliar, Sophia N., et al. “Transitional cell carcinoma exhibiting clear cell features. A differential diagnosis for clear cell adenocarcinoma of the urinary tract”. Archives of pathology & laboratory medicine 119.1 (1995): 79–81.

  16. 16.

    Kramer, Mario W., et al. “Clear-cell variant urothelial carcinoma of the bladder: a case report and review of the literature”. Rare tumors 4.4 (2012): 153–155.

  17. 17.

    Kumar, Lalit, et al. “Primary clear-cell urothelial carcinoma of urinary bladder: a not-so-clear entity with review of literature”. BMJ Case Reports CP 12.10 (2019): e231192.

  18. 18.

    Kurosaka, Shinji, et al. “Advanced clear-cell adenocarcinoma of the bladder successfully treated by radical surgery with adjuvant chemoradiotherapy”. International Journal of Clinical Oncology 10.5 (2005): 362–365.

  19. 19.

    Lah, Kevin, et al. “Primary vesical clear cell adenocarcinoma arising in endometriosis: a rare case of mullerian origin”. Anticancer Research 33.2 (2013): 615–617.

  20. 20.

    Loizzi, V., et al. “A rare case of primary clear-cell adenocarcinoma of the bladder arising from bladder endometriosis”. Journal of Obstetrics and Gynaecology 35.7 (2015): 758–760.

  21. 21.

    Lu, Ji, et al. “Primary clear cell adenocarcinoma of the bladder with recurrence: a case report and literature review”. World journal of surgical oncology 10.1 (2012): 33.

  22. 22.

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  23. 23.

    Mai, K. T. “Multicentric clear cell adenocarcinoma in the urinary bladder and the urethral diverticulum: evidence of origin of clear cell adenocarcinoma of the female lower urinary tract from Mullerian duct remnants”. Histopathology 36 (2000): 380–382.

  24. 24.

    Marchalik, Daniel, et al. “Clear cell adenocarcinoma of the bladder with intravesical cervical invasion”. Case Reports 2015 (2015): bcr2015209893.

  25. 25.

    Matsuoka, Yoh, et al. “Clear cell adenocarcinoma of the urinary bladder inducing acute renal failure”. International journal of urology 9.8 (2002): 467–469.

  26. 26.

    Miller, Eirwen M., et al. “Vesical clear cell adenocarcinoma arising from endometriosis: A mullerian tumor, indistinguishable from ovarian clear cell adenocarcinoma”. Gynecologic Oncology Reports 18 (2016): 8–10.

  27. 27.

    Minervini, R., U. Urbano, and L. Fiorentini. “Mesonephric adenocarcinoma of bladder”. European urology 10 (1984): 141–142.

  28. 28.

    Minkowitz, Shaul Yosef, Reubina Wadee, and Ahmed Adam. “The first report of urothelial (clear cell variant) bladder cancer in a child”. Urology 97 (2016): 204–207.

  29. 29.

    Moinzadeh, Alireza, Jerilyn Latini, and Karim J. Hamawy. “Clear cell adenocarcinoma of the urinary bladder within a diverticulum”. Urology 62.1 (2003): 145.

  30. 30.

    Moradi, Mahmoudreza, et al. “Primary clear cell carcinoma of urinary bladder: A case report”. Urology case reports 16 (2018): 41.

  31. 31.

    Odetola, Oluwatobi E., et al. “Unusual BK polyomavirus‐associated urologic malignancies in renal transplant recipients: Report of two cases and review of the literature”. Diagnostic Cytopathology 46.12 (2018): 1050–1059.

  32. 32.

    Pena Álvarez, Carolina, et al. “Clear-cell adenocarcinoma of vesical origin: a case study of metastatic disease treated with chemotherapy”. Chemotherapy research and practice 2010 (2010).

  33. 33.

    Peršec, Zoran, et al. “Clear Cell Variant of Urothelial Carcinoma in Urinary Bladder; a Clinicopathological and Immunohistochemical Study–A Case Report”. Collegium antropologicum 36.3 (2012): 1045–1047.

  34. 34.

    Schultz, Roger E., et al. “Mesonephric adenocarcinoma of the bladder”. The Journal of urology 132.2 (1984): 263–265.

  35. 35.

    Sethi, Somika, Shashi Dhawan, and Prem Chopra. “Clear cell adenocarcinoma of urinary bladder: A case report and review”. Urology Annals 3.3 (2011): 151.

  36. 36.

    Signori, Gianbattista, et al. “Clear cell adenocarcinoma of the bladder in a male patient: clinicopathologic analysis of a case”. Urologia internationalis 71.2 (2003): 228–230.

  37. 37.

    Skor, Arnold B., and Michael M. Warren. “Mesonephric adenocarcinoma of bladder”. Urology 10.1 (1977): 64–65.

  38. 38.

    Terada, Tadashi. “Urinary bladder urothelial carcinoma with expression of KIT and PDGFRA and showing diverse differentiations into plasmacytoid, clear cell, acantholytic, nested, and spindle variants, and into adenocarcinoma, signet-ring cell carcinoma, small cell carcinoma, large cell carcinoma, and pleomorphic carcinoma”. International journal of clinical and experimental pathology 6.6 (2013): 1150.

  39. 39.

    Yamashita, Ryo, et al. “Urothelial carcinoma (clear cell variant) diagnosed with useful immunohistochemistry stain”. International journal of urology 13.11 (2006): 1448–1450.

Case series

  1. 1.

    Drew, Peter A., et al. “The histogenesis of clear cell adenocarcinoma of the lower urinary tract: case series and review of the literature”. Human pathology 27.3 (1996): 248–252.

  2. 2.

    Oliva, Esther, et al. “Clear cell carcinoma of the urinary bladder: a report and comparison of four tumors of mullerian origin and nine of probable urothelial origin with discussion of histogenesis and diagnostic problems”. The American journal of surgical pathology 26.2 (2002): 190–197.

  3. 3.

    Sun, Katherine, Youming Huan, and Pamela D. Unger. “Clear cell adenocarcinoma of urinary bladder and urethra: another urinary tract lesion immunoreactive for P504S”. Archives of pathology & laboratory medicine 132.9 (2008): 1417–1422.

  4. 4.

    Wang, Hanlin L., et al. “Immunohistochemical distinction between primary adenocarcinoma of the bladder and secondary colorectal adenocarcinoma”. The American journal of surgical pathology 25.11 (2001): 1380–1387.

  5. 5.

    Young, Robert H., and Robert E. Scully. “Clear cell adenocarcinoma of the bladder and urethra: a report of three cases and review of the literature”. The American journal of surgical pathology 9.11 (1985): 816–826.

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Chan, E.OT., Chan, V.WS., Poon, J.YT. et al. Clear cell carcinoma of the urinary bladder: a systematic review. Int Urol Nephrol 53, 815–824 (2021). https://doi.org/10.1007/s11255-020-02725-2

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