Advertisement

Smoking and Bladder Cancer: A Systematic Review of Risk and Outcomes

      Abstract

      Context

      Cigarette smoking is an established risk factor for urothelial carcinoma.

      Objective

      To elucidate the association between pretreatment smoking status, cumulative exposure, and time since smoking cessation and the development of and outcomes for urothelial carcinoma of the bladder (UCB) in patients treated with transurethral resection of the bladder (TURBT) or radical cystectomy (RC).

      Evidence acquisition

      A literature search was performed in September 2014 using the PubMed and Scopus databases limited to articles published in English since 1990. Eight contemporary studies on smoking and UBC development and 26 studies on smoking and UBC prognosis met the inclusion criteria.

      Evidence synthesis

      Current cigarette smoking increases the risk of UCB incidence by two to fourfold, while smoking cessation attenuates this risk. Smoking status, exposure, and cessation have an evident impact on disease recurrence for patients who undergo TURBT, with weaker associations between smoking and other endpoints for TURBT and RC patients.

      Conclusion

      Retrospective evidence suggests that smoking markedly increases UCB risk and may lead to unfavorable outcomes for patients who already have UCB; smoking cessation can attenuate these undesirable effects.

      Patient summary

      Current evidence proves that cigarette smoking is an established risk factor for the development of urothelial carcinoma of the bladder (UCB). There is a growing body of evidence that smoking negatively affects outcomes for UCB patients treated with transurethral resection and/or radical cystectomy, although not uniformly. Long-term smoking cessation seems to mitigate the detrimental effects of smoking in non–muscle-invasive and muscle-invasive bladder cancer.

      Keywords

      To read this article in full you will need to make a payment

      References

        • Siegel R.
        • Ma J.
        • Zou Z.
        • Jemal A.
        Cancer statistics, 2014.
        CA Cancer J Clin. 2014; 64: 9-29
        • Babjuk M.
        • Burger M.
        • Zigeuner R.
        • et al.
        EAU guidelines on non–muscle-invasive urothelial carcinoma of the bladder: update 2013.
        Eur Urol. 2013; 64: 639-653
        • Kirkali Z.
        • Chan T.
        • Manoharan M.
        • et al.
        Bladder cancer: epidemiology, staging and grading, and diagnosis.
        Urology. 2005; 66: 4-34
        • Witjes J.A.
        • Comperat E.
        • Cowan N.C.
        • et al.
        EAU guidelines on muscle-invasive and metastatic bladder cancer: summary of the 2013 guidelines.
        Eur Urol. 2014; 65: 778-792
        • World Health Organization
        Global health risks.
        World Health Organization, Geneva, Switzerland2009
        • Centers for Disease Control, Prevention
        Vital signs: current cigarette smoking among adults aged ≥18 years—United States, 2005-2010.
        Morb Mortal Wkly Rep. 2011; 60: 1207-1212
        • Giskes K.
        • Kunst A.E.
        • Benach J.
        • et al.
        Trends in smoking behaviour between 1985 and 2000 in nine European countries by education.
        J Epidemiol Community Health. 2005; 59: 395-401
        • Simonis K.
        • Shariat S.F.
        • Rink M.
        Urothelial Cancer Working Group of the Young Academic Urologists Working Party of the European Association of Urology. Smoking and smoking cessation effects on oncological outcomes in nonmuscle invasive bladder cancer.
        Curr Opin Urol. 2014; 24: 492-499
        • Zeegers M.P.
        • Tan F.E.
        • Dorant E.
        • van Den Brandt P.A.
        The impact of characteristics of cigarette smoking on urinary tract cancer risk: a meta-analysis of epidemiologic studies.
        Cancer. 2000; 89: 630-639
        • Jha P.
        • Peto R.
        Global effects of smoking, of quitting, and of taxing tobacco.
        N Engl J Med. 2014; 370: 60-68
        • Rink M.
        • Chun F.K.
        • Chromecki T.F.
        • et al.
        [Advanced bladder cancer in elderly patients. Prognostic outcomes and therapeutic strategies].
        Urologe A. 2012; 51: 820-828
        • Krabbe L.M.
        • Svatek R.S.
        • Shariat S.F.
        • Messing E.
        • Lotan Y.
        Bladder cancer risk: use of the PLCO and NLST to identify a suitable screening cohort.
        Urol Oncol. 2015; 33: 65.e19-65.e25
        • Sievert K.D.
        • Amend B.
        • Nagele U.
        • et al.
        Economic aspects of bladder cancer: what are the benefits and costs?.
        World J Urol. 2009; 27: 295-300
        • Baser S.
        • Shannon V.R.
        • Eapen G.A.
        • et al.
        Smoking cessation after diagnosis of lung cancer is associated with a beneficial effect on performance status.
        Chest. 2006; 130: 1784-1790
        • Land S.R.
        Methodologic barriers to addressing critical questions about tobacco and cancer prognosis.
        J Clin Oncol. 2012; 30: 2030-2032
        • Dresler C.M.
        • Leon M.E.
        • Straif K.
        • Baan R.
        • Secretan B.
        Reversal of risk upon quitting smoking.
        Lancet. 2006; 368: 348-349
        • Liberati A.
        • Altman D.G.
        • Tetzlaff J.
        • et al.
        The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
        PLoS Med. 2009; 6: e1000100
        • Freedman N.D.
        • Silverman D.T.
        • Hollenbeck A.R.
        • Schatzkin A.
        • Abnet C.C.
        Association between smoking and risk of bladder cancer among men and women.
        JAMA. 2011; 306: 737-745
        • Alguacil J.
        • Kogevinas M.
        • Silverman D.T.
        • et al.
        Urinary pH, cigarette smoking and bladder cancer risk.
        Carcinogenesis. 2011; 32: 843-847
        • Erdurak K.
        • Dundar P.E.
        • Ozyurt B.C.
        • Negri E.
        • La Vecchia C.
        • Tay Z.
        Smoking, occupation, history of selected diseases and bladder cancer risk in Manisa, Turkey.
        Eur J Cancer Prev. 2014; 23: 58-61
        • Ferreccio C.
        • Yuan Y.
        • Calle J.
        • et al.
        Arsenic, tobacco smoke, and occupation: associations of multiple agents with lung and bladder cancer.
        Epidemiology. 2013; 24: 898-905
        • Jiang X.
        • Castelao J.E.
        • Yuan J.-M.
        • et al.
        Cigarette smoking and subtypes of bladder cancer.
        Int J Cancer. 2012; 130: 896-901
        • Moura M.A.
        • Bergmann A.
        • Aguiar S.S.
        • Thuler L.C.S.
        The magnitude of the association between smoking and the risk of developing cancer in Brazil: a multicenter study.
        BMJ Open. 2014; 4: e003736
        • Welty C.J.
        • Wright J.L.
        • Hotaling J.M.
        • Bhatti P.
        • Porter M.P.
        • White E.
        Persistence of urothelial carcinoma of the bladder risk among former smokers: results from a contemporary, prospective cohort study.
        Urol Oncol. 2014; 32 (25.e1–5)
        • Wu C.-C.
        • Chen M.-C.
        • Huang Y.-K.
        • et al.
        Environmental tobacco smoke and arsenic methylation capacity are associated with urothelial carcinoma.
        J Formos Med Assoc. 2013; 112: 554-560
        • Zheng Y.-L.
        • Amr S.
        • Saleh D.A.
        • et al.
        Urinary bladder cancer risk factors in Egypt: a multicenter case-control study.
        Cancer Epidemiol Biomarkers Prev. 2012; 21: 537-546
        • Sopori M.
        Effects of cigarette smoke on the immune system.
        Nat Rev Immunol. 2002; 2: 372-377
        • Zhang Z.F.
        • Sarkis A.S.
        • Cordon-Cardo C.
        • et al.
        Tobacco smoking, occupation, and p53 nuclear overexpression in early stage bladder cancer.
        Cancer Epidemiol Biomarkers Prev. 1994; 3: 19-24
        • Zhang Z.F.
        • Shu X.M.
        • Cordon-Cardo C.
        • et al.
        Cigarette smoking and chromosome 9 alterations in bladder cancer.
        Cancer Epidemiol Biomarkers Prev. 1997; 6: 321-326
        • Garcia-Closas M.
        • Rothman N.
        • Figueroa J.D.
        • et al.
        Common genetic polymorphisms modify the effect of smoking on absolute risk of bladder cancer.
        Cancer Res. 2013; 73: 2211-2220
        • Ajili F.
        • Manai M.
        • Darouiche A.
        • Chebil M.
        • Boubaker S.
        Tumor multiplicity is an independent prognostic factor of non–muscle-invasive bladder cancer treated with bacillus Calmette-Guerin immunotherapy.
        Ultrastruct Pathol. 2012; 36: 320-324
        • Allard P.
        • Fradet Y.
        • Têtu B.
        • Bernard P.
        Tumor-associated antigens as prognostic factors for recurrence in 382 patients with primary transitional cell carcinoma of the bladder.
        Clin Cancer Res. 1995; 1: 1195-1202
        • Chen C.-H.
        • Shun C.-T.
        • Huang K.-H.
        • et al.
        Stopping smoking might reduce tumour recurrence in nonmuscle-invasive bladder cancer.
        BJU Int. 2007; 100: 281-286
        • Fleshner N.
        • Garland J.A.
        • Moadel A.
        • et al.
        Influence of smoking status on the disease-related outcomes of patients with tobacco-associated superficial transitional cell carcinoma of the bladder.
        Cancer. 1999; 86: 2337-2345
        • Gangawar R.
        • Ahirwar D.
        • Mandhani A.
        • Mittal R.D.
        Impact of nucleotide excision repair ERCC2 and base excision repair APEX1 genes polymorphism and its association with recurrence after adjuvant BCG immunotherapy in bladder cancer patients of North India.
        Med Oncol. 2010; 27: 159-166
        • Gee J.R.
        • Jarrard D.F.
        • Bruskewitz R.C.
        • et al.
        Reduced bladder cancer recurrence rate with cardioprotective aspirin after intravesical bacille Calmette-Guérin.
        BJU Int. 2009; 103: 736-739
        • Grotenhuis A.J.
        • Ebben C.W.
        • Aben K.K.
        • et al.
        The effect of smoking and timing of smoking cessation on clinical outcome in non–muscle-invasive bladder cancer.
        Urol Oncol. 2015; 33: 65.e9-65.e17
        • Hwang E.C.
        • Kim Y.J.
        • Hwang I.S.
        • et al.
        Impact of diabetes mellitus on recurrence and progression in patients with non–muscle invasive bladder carcinoma: a retrospective cohort study.
        Int J Urol. 2011; 18: 769-776
        • Kashif Khan M.
        • Ahmed I.
        • Raza S.J.
        Factors effecting recurrence and progression of high grade non invasive bladder cancer treated by intravesical BCG.
        Pak J Med Sci. 2014; 30: 326-330
        • Lammers R.J.M.
        • Witjes W.P.J.
        • Hendricksen K.
        • Caris C.T.M.
        • Janzing-Pastors M.H.C.
        • Witjes J.A.
        Smoking status is a risk factor for recurrence after transurethral resection of non–muscle-invasive bladder cancer.
        Eur Urol. 2011; 60: 713-720
        • Rausch S.
        • Hennenlotter J.
        • Todenhöfer T.
        • et al.
        Impaired estimated glomerular filtration rate is a significant predictor for non–muscle-invasive bladder cancer recurrence and progression—introducing a novel prognostic model for bladder cancer recurrence.
        Urol Oncol. 2014; 31: 1178-1183
        • Rink M.
        • Xylinas E.
        • Babjuk M.
        • et al.
        Impact of smoking on outcomes of patients with a history of recurrent nonmuscle invasive bladder cancer.
        J Urol. 2012; 188: 2120-2127
        • Rink M.
        • Furberg H.
        • Zabor E.C.
        • et al.
        Impact of smoking and smoking cessation on oncologic outcomes in primary non–muscle-invasive bladder cancer.
        Eur Urol. 2013; 63: 724-732
        • Serretta V.
        • Altieri V.
        • Morgia G.
        • et al.
        Cigarette smoking status at diagnosis and recurrence in intermediate-risk non–muscle-invasive bladder carcinoma.
        Urology. 2013; 81: 277-282
        • Sfakianos J.P.
        • Shariat S.F.
        • Favaretto R.L.
        • Rioja J.
        • Herr H.W.
        Impact of smoking on outcomes after intravesical bacillus Calmette-Guérin therapy for urothelial carcinoma not invading muscle of the bladder.
        BJU Int. 2011; 108: 526-530
        • Wyszynski A.
        • Tanyos S.A.
        • Rees J.R.
        • et al.
        Body mass and smoking are modifiable risk factors for recurrent bladder cancer.
        Cancer. 2014; 120: 408-414
        • Cheng L.
        • Neumann R.M.
        • Weaver A.L.
        • Spotts B.E.
        • Bostwick D.G.
        Predicting cancer progression in patients with stage T1 bladder carcinoma.
        J Clin Oncol. 1999; 17: 3182-3187
        • Segal R.
        • Yafi F.A.
        • Brimo F.
        • Tanguay S.
        • Aprikian A.
        • Kassouf W.
        Prognostic factors and outcome in patients with T1 high-grade bladder cancer: can we identify patients for early cystectomy?.
        BJU Int. 2012; 109: 1026-1030
        • Rink M.
        • Xylinas E.
        • Trinh Q.-D.
        • et al.
        Gender-specific effect of smoking on upper tract urothelial carcinoma outcomes.
        BJU Int. 2013; 112: 623-637
        • Rink M.
        • Xylinas E.
        • Babjuk M.
        • et al.
        Smoking reduces the efficacy of intravesical bacillus Calmette-Guérin immunotherapy in non–muscle-invasive bladder cancer.
        Eur Urol. 2012; 62: 1204-1206
        • Xylinas E.
        • Kent M.
        • Kluth L.
        • et al.
        Accuracy of the EORTC risk tables and of the CUETO scoring model to predict outcomes in non–muscle-invasive urothelial carcinoma of the bladder.
        Br J Cancer. 2013; 109: 1460-1466
        • Figueroa J.D.
        • Han S.S.
        • Garcia-Closas M.
        • et al.
        Genome-wide interaction study of smoking and bladder cancer risk.
        Carcinogenesis. 2014; 35: 1737-1744
        • Baumann B.C.
        • Guzzo T.J.
        • He J.
        • et al.
        A novel risk stratification to predict local-regional failures in urothelial carcinoma of the bladder after radical cystectomy.
        Int J Radiat Oncol Biol Phys. 2013; 85: 81-88
        • Boorjian S.A.
        • Kim S.P.
        • Weight C.J.
        • Cheville J.C.
        • Thapa P.
        • Frank I.
        Risk factors and outcomes of urethral recurrence following radical cystectomy.
        Eur Urol. 2011; 60: 1266-1272
        • Boström P.J.
        • Alkhateeb S.
        • Trottier G.
        • et al.
        Sex differences in bladder cancer outcomes among smokers with advanced bladder cancer.
        BJU Int. 2012; 109: 70-76
        • Kim P.H.
        • Kent M.
        • Zhao P.
        • et al.
        The impact of smoking on pathologic response to neoadjuvant cisplatin-based chemotherapy in patients with muscle-invasive bladder cancer.
        World J Urol. 2014; 32: 453-459
        • Lee C.
        • Kim K.H.
        • You D.
        • et al.
        Smoking and survival after radical cystectomy for bladder cancer.
        Urology. 2012; 80: 1307-1312
        • Rink M.
        • Zabor E.C.
        • Furberg H.
        • et al.
        Impact of smoking and smoking cessation on outcomes in bladder cancer patients treated with radical cystectomy.
        Eur Urol. 2013; 64: 456-464
        • Thrasher J.B.
        • Frazier H.A.
        • Robertson J.E.
        • Dodge R.K.
        • Paulson D.F.
        Clinical variables which serve as predictors of cancer-specific survival among patients treated with radical cystectomy for transitional cell carcinoma of the bladder and prostate.
        Cancer. 1994; 73: 1708-1715
        • Yafi F.A.
        • Aprikian A.G.
        • Chin J.L.
        • et al.
        Contemporary outcomes of 2287 patients with bladder cancer who were treated with radical cystectomy: a Canadian multicentre experience.
        BJU Int. 2011; 108: 539-545
        • Gritz E.R.
        • Dresler C.
        • Sarna L.
        Smoking, the missing drug interaction in clinical trials: ignoring the obvious.
        Cancer Epidemiol Biomarkers Prev. 2005; 14: 2287-2293
        • Rink M.
        • Shariat S.F.
        Re: Global effects of smoking, of quitting, and of taxing tobacco.
        Eur Urol. 2014; 66: 176-178
        • Sosnowski R.
        • Przewozniak K.
        The role of the urologist in smoking cessation: why is it important?.
        Urol Oncol. 2015; 33: 30-39
        • Guzzo T.J.
        • Hockenberry M.S.
        • Mucksavage P.
        • Bivalacqua T.J.
        • Schoenberg M.P.
        Smoking knowledge assessment and cessation trends in patients with bladder cancer presenting to a tertiary referral center.
        Urology. 2012; 79: 166-171
        • Bassett J.C.
        • Gore J.L.
        • Chi A.C.
        • et al.
        Impact of a bladder cancer diagnosis on smoking behavior.
        J Clin Oncol. 2012; 30: 1871-1878
        • Kowalkowski M.A.
        • Goltz H.H.
        • Petersen N.J.
        • Amiel G.E.
        • Lerner S.P.
        • Latini D.M.
        Educational opportunities in bladder cancer: increasing cystoscopic adherence and the availability of smoking-cessation programs.
        J Cancer Educ. 2014; 29: 739-745
        • Strope S.A.
        • Montie J.E.
        The causal role of cigarette smoking in bladder cancer initiation and progression, and the role of urologists in smoking cessation.
        J Urol. 2008; 180: 31-37
        • Fajkovic H.
        • Halpern J.A.
        • Cha E.K.
        • et al.
        Impact of gender on bladder cancer incidence, staging, and prognosis.
        World J Urol. 2011; 29: 457-463
        • Rink M.
        • Lee D.J.
        • Kent M.
        • et al.
        Predictors of cancer-specific mortality after disease recurrence following radical cystectomy.
        BJU Int. 2013; 111: E30-E36
        • Rink M.
        • Shariat S.F.
        Can we apply nomograms derived in the United States to European patients?.
        Yes, we can! Eur Urol. 2012; 61: 65-66
        • Shariat S.F.
        • Karakiewicz P.I.
        • Palapattu G.S.
        • et al.
        Nomograms provide improved accuracy for predicting survival after radical cystectomy.
        Clin Cancer Res. 2006; 12: 6663-6676
        • Shariat S.F.
        • Rink M.
        • Ehdaie B.
        • et al.
        Pathologic nodal staging score for bladder cancer: a decision tool for adjuvant therapy after radical cystectomy.
        Eur Urol. 2013; 63: 371-378
        • Rink M.
        • Cha E.K.
        • Green D.
        • et al.
        Biomolecular predictors of urothelial cancer behavior and treatment outcomes.
        Curr Urol Rep. 2012; 13: 122-135
        • Wang L.C.
        • Xylinas E.
        • Kent M.T.
        • et al.
        Combining smoking information and molecular markers improves prognostication in patients with urothelial carcinoma of the bladder.
        Urol Oncol. 2014; 32: 433-440