Is Schistosomiasis a Red Herring in Carcinoma of the Bladder?
DOI:
https://doi.org/10.21276/apalm.3048Keywords:
Schistosomiasis, bladder, carcinoma, transitional, squamousAbstract
Objective: The specific role Schistosoma ova play in bladder carcinogenesis as well as its association with a specific morphologic subtype has remained inconclusive. This study aims to re-evaluate this relationship morphologically and review the literature.
Materials: A 19-year (1999-2017) review of all cases of carcinoma of the bladder with or without schistosomiasis was conducted. This was supplemented with a review of the literature.
Results: 278 cases of carcinoma of the bladder were diagnosed. These comprised 251 males and 27 females in ratio 9:1 and mean ages 56±15 years and 54±16 years respectively (p 0.6). While none of the 27 carcinomas among females had Schistosoma ova 28 of the 251 carcinomas in males were co-morbid with schistosomiasis. These comprised 13 of the 174 TCC, 14 of the 94 SCC, and 1 of the 10 adenocarcinomas. There were no statistically significant differences in gender (p 0.6), age (p 0.6), or co-morbidity with the parasite (p 0.2) among the various histologic subtypes. A review of the literature shows an association of Schistosoma ova not only with SCC but also with TCC and, but for isolated case reports, there is a paucity of definitive association with cancers outside the bladder.
Conclusion: There were no statistically significant differences in gender, age, or co-morbidity with the parasite among the various histologic subtypes. In addition to this, the literature review suggests there must be other co-factors present only in the bladder, rather than just the ova by itself, responsible for Schistosoma-associated carcinoma in this organ.
References
Schistosomiasis, Fact Sheet No 115; February 2010. World Health Organization. Available at http://www.who.int/mediacentre/factsheets/fs115/en/Accessed: September 5, 2019.
Abdulkadir A, Ahmed M, Abubakar BM, Suleiman IE, Yusuf I, Imam IM, Sule AA, Tela UM, Dogo HM, Yakasai AM, Musa BM. Prevalence of urinary schistosomiasis in Nigeria, 1994–2015: Systematic review and meta-analysis. Afr J Urol 2017;23(3):228-39.
Ferguson AR. Associated bilharziosis and primary malignant disease of the urinary bladder, with observations on a series of forty cases. The J Pathol. 1911;16(1):76-94.
Rambau PF, Chalya PL, Jackson K. Schistosomiasis and urinary bladder cancer in North Western Tanzania: a retrospective review of 185 patients. Infectious Agents and Cancer. 2013;8:19. doi:10.1186/1750-9378-8-19.
Antoni S, Ferlay J, Soerjomataram I, Znaor A, Jemal A, Bray F. Bladder cancer incidence and mortality: a global overview and recent trends. Eur Urol. 2017;71(1):96-108.
Betterton C, Ndifon GT, Bassey SE, Tan RM, Oyeyi T. Schistosomiasis in Kano State, Nigeria: I. Human infections near dam sites and the distribution and habitat preferences of potential snail intermediate hosts. Ann Trop Med Para. 1988;82(6):561-70.
SarkinfadaF, Akande OA,Abubakar I,Iliyasu Z. Urinary schistosomiasis in the Danjarima community in Kano, Nigeria. J Infection DevCountr 2009;3:452-7. 10.3855/jidc.417.
Eni U, Na'aya H, Nggada H, Dogo D. Carcinoma of the urinary Bladder in Maiduguri: The schistosomiasis connection. The Internet JOncol 2007;5(2).
Rollinson D, Knopp S, Levitz S, Stothard JR, Tchuenté LA, Garba A, et al. Time to set the agenda for schistosomiasis elimination. ActaTropica. 2013;128(2):423-40.
Sule A A, Ochicha O, Ibrahim Y, Adam S, Abubakar A, Haruna M S. Update on bladder cancer in Kano, Northern Nigeria. Niger J Basic ClinSci 2019;14:26-9.
Abdullahi M.K, Bassey SE, Oyeyi TI. A comprehensive mapping of urinary schistosomiasis using geographic information systems (GIS) in Kano State, Nigeria. Bayero J Pure Applied Sci 2009;2(1):41-6.
Zheng YL, Amr S, Saleh DA, Dash C, Ezzat S, Mikhail NN, et al. Urinary bladder cancer risk factors in Egypt: a multicenter case-control study. Cancer Epidemiol Biomarkers Prev 2012;21(3):537-46.
Horstmann M, Witthuhn R, Falk M, Stenzl A. Gender-specific differences in bladder cancer: a retrospective analysis. Gender Med 2008; 1;5(4):385-94.
Pakzad R, Mohammadian-Hafshejani A, Mohammadian M, PakzadI, Safiri S, Khazaei S, Salehiniya H. Incidence and mortality of bladder cancer and their relationship with development in Asia. Asian Pacific J Cancer Prev 2015;16(16):7365-74.
Botelho MC, Figueiredo J, Alves H. Bladder cancer and urinary Schistosomiasis in Angola. J NnephRes 2015;1(1):22.
Mapulanga V, Labib M, Bowa K. Pattern of bladder cancer at university teaching hospital, Lusaka, Zambia in the era of HIV epidemic. Med J Zambia. 2012;39(1):22-6.
Waihenya CG, Mungai PN. Pattern of transitional cell carcinoma of the urinary bladder as seen at Kenyatta National Hospital, Nairobi. East AfrMed J 2004;81(3):114-9.
Ferlay J, Randi G, Bosetti C, Levi F, Negri E, Boyle P, et al. Declining mortality from bladder cancer in Europe. Br JUrolInt 2008;101:11-9.
Ries LAG, Melbert D, Krapcho M, Stinchcomb DG, Howlader N, Horner MJ, et al. SEER cancer statistics review, 1975–2005. National Cancer Institute, Bethesda; 2008
Vanderpuye V, Grover S, Hammad N, Simonds H, Olopade F, Stefan DC. An update on the management of breast cancer in Africa. Infectious Agents and Cancer 2017;12(1):13.
Odedina FT, Akinremi TO, Chinegwundoh F, Roberts R, Yu D, Reams RR, et al. Prostate cancer disparities in Black men of African descent: a comparative literature review of prostate cancer burden among Black men in the United States, Caribbean, United Kingdom, and West Africa. Infectious Agents and Cancer 2009;4(1):S2).
Wang Y, Chang Q, Li Y. Racial differences in urinary bladder cancer in the United States. Scientific Reports 2018;8(1):12521.
Porter MP, Voigt LF, Penson DF, Weiss NS. Racial variation in the incidence of squamous cell carcinoma of the bladder in the United States. The J Urol2002;168(5):1960-3.
Mohamed AR, Al Karawi M, Yasawy MI. Schistosomal colonic disease. Gut. 1990 Apr 1;31(4):439-42.
Peterson MR, Weidner N. Gastrointestinal neoplasia associated with bowel parasitosis: real or imaginary? J Trop Med 2011; vol. 2011, Article ID 234254, 8 pages, 2011. https://doi.org/10.1155/2011/234254.
Nacif-Pimenta R, da Silva Orfanó A, Mosley IA, Karinshak SE, Ishida K, Mann VH, et al. Differential responses of epithelial cells from urinary and biliary tract to eggs of Schistosoma haematobium and S. mansoni. Scientific Reports 2019;24;9(1):10731.
http://monographs.iarc.fr/ENG/Classification/List_of_Classifications.pdfAccessed June 20, 2019.
Armengol G, Elisa S, Lozano J, Showman S, Sumoy L, CaballÃn M, Knuutila S. Genomic imbalances in Schistosoma-associated and non-Schistosoma-associated bladder carcinoma. An array comparative genomic hybridization analysis. CancGen Cytogen 2007;177:16-9.
El-Rifai W, Kamel D, Larramendy ML, Shoman S, Gad Y, Baithun S, et al. DNA copy number changes in Schistosoma-associated and non-Schistosoma-associated bladder cancer. Am J Pathol 2000;156(3):871-8. doi: 10.1016/S0002-9440(10)64956-5.
Ishida K, Hsieh MH. Understanding urogenital schistosomiasis-related bladder cancer: an update. Frontiers in Med 2018;5.
Barsoum RS, Esmat G, El-Baz T. Human schistosomiasis: clinical perspective: review. J Adv Res. 2013;4(5):433–444. doi:10.1016/j.jare.2013.01.005
Vale N, Gouveia MJ, Rinaldi G, Santos J, Santos LL, Brindley PJ, da Costa JM. The role of estradiol metabolism in urogenital schistosomiasis-induced bladder cancer. Tumor Biol. 2017;39(3):1010428317692247.
Croft PR, Lathrop SL, Feddersen RM,Joste NE. Estrogen receptor expression in papillary urothelial carcinoma of the bladder and ovarian transitional cell carcinoma. Arch Pathol Lab Med 2015;129(2):194-9.
Kashiwagi E, Fujita K, Yamaguchi S, Fushimi H, Ide H, Inoue S, et al. Expression of steroid hormone receptors and its prognostic significance in urothelial carcinoma of the upper urinary tract. CancBiolTherapy 2016;17(11):1188-96.
Wolpert BJ, Amr S, Ezzat S, Saleh DA, Gouda I, Loay I, et al. Estrogen exposure and bladder cancer risk in Egyptian women. Maturitas 2010;67(4):353-7.
Gouda I, Mokhtar NA, Bilal DA, El-Bolkainy TA, El-Bolkainy NM. Bilharziasis and bladder cancer: a time trend analysis of 9,843 patients. J Egypt NatlCancInst 2007;19(2):158-62.
Ploeg M, Aben KK, Kiemeney LA. The present and future burden of urinary bladder cancer in the world. World J Urol 2009;27(3):289-93. doi: 10.1007/s00345-009-0383-3.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, in press. The online GLOBOCAN 2018 database is accessible at http://gco.iarc.fr/, as part of IARC’s Global Cancer Observatory.
Abdulrahim S, Jawad M. Socioeconomic differences in smoking in Jordan, Lebanon, Syria, and Palestine: A cross-sectional analysis of national surveys. PloS one 2018;13(1):e0189829.
Fouda S, Kelany M, Moustafa N, Abushouk AI, Hassane A, Sleem A, et al. Tobacco smoking in Egypt: a scoping literature review of its epidemiology and control measures. EMHJ-Eastern Mediterranean Health Journal 2018;24(02):198-215.
Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6(7):411–425. 10.1016/S1473-3099(06)70521-7
Odutola M, Jedy-Agba EE, Dareng EO, Oga EA, Igbinoba F, Otu T, Ezeome E, Hassan R, Adebamowo CA. Burden of cancers attributable to infectious agents in Nigeria: 2012–2014. Frontiers in Oncol 2016;6:216.
https://www.afro.who.int/sites/default/files/2017-09/tob-gats-in-nigeria-a-sucess-story-in-afr.pdf Accessed September 10, 2019.
Manley KV, Hubbard R, Swallow D, Finch W, Wood SJ, Biers SM. Risk factors for development of primary bladder squamous cell carcinoma. The Ann Royal Col SurgEngl 2017;99(2):155-60.
Kantor AF, Hartge P, Hoover RN, Fraumeni JF. Epidemiological characteristics of squamous cell carcinoma and adenocarcinoma of the bladder. CancRes1988;48(13):3853-5.
Hicks RM, Ismail MM, Walters CL, Beecham PT, Rabie MF, El Alamy MA. Association of bacteriuria and urinary nitrosamine formation with Schistosoma haematobium infection in the Qalyub area of Egypt. Transactions of the Royal Soc Trop Med Hyg 1982;76(4):519-27.
Martin JW, Carballido EM, Ahmed A, Farhan B, Dutta R, Smith C, Youssef RF. Squamous cell carcinoma of the urinary bladder: systematic review of clinical characteristics and therapeutic approaches. Arab J Urology 2016;14(3):183-91.
Ossai OP, Dankoli R, Nwodo C, Tukur D, Nsubuga P, Ogbuabor D, Ekwueme O, Abonyi G, Ezeanolue E, Nguku P, Nwagbo D. Bacteriuria and urinary schistosomiasis in primary school children in rural communities in Enugu State, Nigeria, 2012. The Pan Afr Med J 2014;18(Suppl 1).
Ifeanyi CI, Matur BM, Ikeneche NF. Urinary schistosomiasis and concomitant bacteriuria in the Federal Capital Territory Abuja Nigeria. New York Sci 2009;2(2):1-8.
Wang C, Symington JW, Ma E, Cao B, Mysorekar IU. Estrogenic modulation of uropathogenic Escherichia coli infection pathogenesis in a murine menopause model. Infection and Immunity 20131;81(3):733-9.
Ali OF, El Shabrawy M, Sabry FH, Fayad S. Relation of schistosomiasis to urinary typhoid carriers in Egypt. The J Egyptian Publ Health Assoc 1978;53(1–2):12–6.
Vermeulen SH, Hanum N, Grotenhuis AJ, Castano-Vinyals G, Van Der Heijden AG, et al. Recurrent urinary tract infection and risk of bladder cancer in the Nijmegen bladder cancer study. Br JCanc 2015;112(3):594.
Forster CS, Cody J, Banskota N, Stroud C, Hsieh YJ, Farah D, Lamanna O, Hammam O, Caldovic L, Hsieh MH. Profiling of urine bacterial DNA to identify an oncobiome in a mouse model of bladder cancer. bioRxiv. 2018 Jan 1:364000.
Neuman H, Debelius JW, Knight R, Koren O. Microbial endocrinology: the interplay between the microbiota and the endocrine system. FEMS MicrobiolRev 2015;39(4):509-21.
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