Abstract
Background
Smoking is a risk factor for mucinous ovarian cancer (OvCa) in Caucasians. Whether a similar association exists in African Americans (AA) is unknown.
Methods
We conducted a population-based case–control study of incident OvCa in AA women across 11 geographic locations in the US. A structured telephone interview asked about smoking, demographic, health, and lifestyle factors. Odds ratios and 95% confidence intervals (OR, 95% CI) were estimated from 613 cases and 752 controls using unconditional logistic regression in multivariable adjusted models.
Results
Associations were greater in magnitude for serous OvCa than for all OvCa combined. Compared to never smokers, increased risk for serous OvCa was observed for lifetime ever smokers (1.46, 1.11–1.92), former smokers who quit within 0–2 years of diagnosis (5.48, 3.04–9.86), and for total pack-years smoked among lifetime ever smokers (0–5 pack-years: 1.79, 1.23–2.59; >5–20 pack-years: 1.52, 1.05–2.18; >20 pack-years: 0.98, 0.61–1.56); however, we observed no dose–response relationship with increasing duration or consumption and no significant associations among current smokers. Smoking was not significantly associated with mucinous OvCa. Associations for all OvCa combined were consistently elevated among former smokers. The proportion of ever smokers who quit within 0–2 years was greater among cases (23%) than controls (7%).
Conclusions
Cigarette smoking may be associated with serous OvCa among AA, which differs from associations reported among Caucasians. Exposure misclassification or reverse causality may partially explain the absence of increased risk among current smokers and lack of dose–response associations. Better characterization of smoking patterns is needed in this understudied population.
Similar content being viewed by others
References
Jamal A, Agaku IT, O’Connor E, King BA, Kenemer JB, Neff L (2014) Current cigarette smoking among adults–United States, 2005–2013. MMWR Morb Mortal Wkly Rep 63:1108–1112
U.S. Department of Health and Human Services (2014) The health consequences of smoking—50 years of progress: a report of the Surgeon General. Department of Health and Human Services. Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta
American Cancer Society (2015) Cancer facts and figures 2015. Estimated new cancer cases and deaths by sex, U.S., all sites, 2015. American Cancer Society, Atlanta
Faber MT, Kjaer SK, Dehlendorff C et al (2013) Cigarette smoking and risk of ovarian cancer: a pooled analysis of 21 case−control studies. Cancer Causes Control 24:989–1004
Collaborative Group on Epidemiological Studies of Ovarian C, Beral V, Gaitskell K et al (2012) Ovarian cancer and smoking: individual participant meta-analysis including 28,114 women with ovarian cancer from 51 epidemiological studies. Lancet Oncol. 13:946–956
Gram IT, Lukanova A, Brill I et al (2012) Cigarette smoking and risk of histological subtypes of epithelial ovarian cancer in the EPIC cohort study. Int J Cancer 130:2204–2210
Wentzensen N, Poole EM, Trabert B et al (2016) Ovarian cancer risk factors by histologic subtype: an analysis from the Ovarian Cancer Cohort Consortium. J Clin Oncol 34:2888–2898
Marchbanks PA, Wilson H, Bastos E, Cramer DW, Schildkraut JM, Peterson HB (2000) Cigarette smoking and epithelial ovarian cancer by histologic type. Obstet Gynecol 95:255–260
Green A, Purdie D, Bain C, Siskind V, Webb PM (2001) Cigarette smoking and risk of epithelial ovarian cancer (Australia). Cancer Causes Control 12:713–719
Terry PD, Miller AB, Jones JG, Rohan TE (2003) Cigarette smoking and the risk of invasive epithelial ovarian cancer in a prospective cohort study. Eur J Cancer 39:1157–1164
Rossing MA, Cushing-Haugen KL, Wicklund KG, Weiss NS (2008) Cigarette smoking and risk of epithelial ovarian cancer. Cancer Causes Control 19:413–420
Gram IT, Braaten T, Adami HO, Lund E, Weiderpass E (2008) Cigarette smoking and risk of borderline and invasive epithelial ovarian cancer. Int J Cancer 122:647–652
Baker JA, Odunuga OO, Rodabaugh KJ, Reid ME, Menezes RJ, Moysich KB (2006) Active and passive smoking and risk of ovarian cancer. Int J Gynecol Cancer 16(Suppl 1):211–218
Goodman MT, Tung KH (2003) Active and passive tobacco smoking and the risk of borderline and invasive ovarian cancer (United States). Cancer Causes Control 14:569–577
Cohen SS, Sonderman JS, Mumma MT, Signorello LB, Blot WJ (2011) Individual and neighborhood-level socioeconomic characteristics in relation to smoking prevalence among black and white adults in the Southeastern United States: a cross-sectional study. BMC Public Health 11:877
Chornokur G, Amankwah EK, Schildkraut JM, Phelan CM (2013) Global ovarian cancer health disparities. Gynecol Oncol 129:258–264
Moorman PG, Palmieri RT, Akushevich L, Berchuck A, Schildkraut JM (2009) Ovarian cancer risk factors in African-American and white women. Am J Epidemiol 170:598–606
John EM, Whittemore AS, Harris R, Itnyre J (1993) Characteristics relating to ovarian cancer risk: collaborative analysis of seven U.S. case–control studies. Epithelial ovarian cancer in black women. Collaborative Ovarian Cancer Group. J Natl Cancer Inst 85:142–147
Schildkraut JM, Alberg AJ, Bandera EV et al (2014) A multi-center population-based case–control study of ovarian cancer in African-American women: the African American Cancer Epidemiology Study (AACES). BMC Cancer 14:688
Qin B, Moorman PG, Alberg AJ et al (2016) Dietary carbohydrate intake, glycaemic load, glycaemic index and ovarian cancer risk in African–American women. Br J Nutr 115:694–702
Rothman KJ, Greenland S (1998) Modern epidemiology, 2nd edn. Lippincott-Reaven Publishers, Philadelphia
Hosmer DW, Lemeshow SL (2000) Applied logistic regression, 2nd edn. Wiley, New York
Kobel M, Kalloger SE, Boyd N et al (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med 5:e232
Warren GW, Arnold SM, Valentino JP et al (2012) Accuracy of self-reported tobacco assessments in a head and neck cancer treatment population. Radiother Oncol 103:45–48
Morales NA, Romano MA, Michael Cummings K et al (2013) Accuracy of self-reported tobacco use in newly diagnosed cancer patients. Cancer Causes Control 24:1223–1230
Marquis GS, Habicht JP, Lanata CF, Black RE, Rasmussen KM (1997) Association of breastfeeding and stunting in Peruvian toddlers: an example of reverse causality. Int J Epidemiol 26:349–356
Seidman JD, Kurman RJ, Ronnett BM (2003) Primary and metastatic mucinous adenocarcinomas in the ovaries: incidence in routine practice with a new approach to improve intraoperative diagnosis. Am J Surg Pathol 27:985–993
Caraballo RS, Giovino GA, Pechacek TF et al (1998) Racial and ethnic differences in serum cotinine levels of cigarette smokers: third National Health and Nutrition Examination Survey, 1988–1991. JAMA 280:135–139
Clark PI, Gautam S, Gerson LW (1996) Effect of menthol cigarettes on biochemical markers of smoke exposure among black and white smokers. Chest 110:1194–1198
Murray RP, Connett JE, Buist AS, Gerald LB, Eichenhorn MS (2001) Experience of Black participants in the Lung Health Study smoking cessation intervention program. Nicotine Tob Res 3:375–382
Mustonen TK, Spencer SM, Hoskinson RA, Sachs DP, Garvey AJ (2005) The influence of gender, race, and menthol content on tobacco exposure measures. Nicotine Tob Res 7:581–590
Ahijevych K, Gillespie J (1997) Nicotine dependence and smoking topography among black and white women. Res Nurs Health 20:505–514
Ahijevych KL, Tyndale RF, Dhatt RK, Weed HG, Browning KK (2002) Factors influencing cotinine half-life during smoking abstinence in African American and Caucasian women. Nicotine Tob Res 4:423–431
Perez-Stable EJ, Herrera B, Jacob P 3rd, Benowitz NL (1998) Nicotine metabolism and intake in black and white smokers. JAMA 280:152–156
Giovino GA, Sidney S, Gfroerer JC et al (2004) Epidemiology of menthol cigarette use. Nicotine Tob Res 6(Suppl 1):S67–S81
Benowitz NL, Herrera B, Jacob P 3rd (2004) Mentholated cigarette smoking inhibits nicotine metabolism. J Pharmacol Exp Ther 310:1208–1215
Albanes D, Jones DY, Micozzi MS, Mattson ME (1987) Associations between smoking and body weight in the US population: analysis of NHANES II. Am J Public Health 77:439–444
Olsen CM, Nagle CM, Whiteman DC et al (2013) Obesity and risk of ovarian cancer subtypes: evidence from the Ovarian Cancer Association Consortium. Endocr Relat Cancer 20:251–262
Dixon SC, Nagle CM, Thrift AP et al (2016) Adult body mass index and risk of ovarian cancer by subtype: a Mendelian randomization study. Int J Epidemiol 45:884–895
Marom-Haham L, Shulman A (2016) Cigarette smoking and hormones. Curr Opin Obstet Gynecol 28:230–235
Acknowledgments
We would like to acknowledge the AACES interviewers, Christine Bard, LaTonda Briggs, Whitney Franz (North Carolina), and Robin Gold (Detroit). We also acknowledge the individuals responsible for facilitating case ascertainment at the 11 geographic locations across the 10 study centers including Jennifer Burczyk-Brown (Alabama); Rana Bayakly and Vicki Bennett (Georgia); the Louisiana Tumor Registry; Manisha Narang (New Jersey); Diana Slone, Yingli Wolinsky, Steven Waggoner, Anne Heugel, Nancy Fusco, Kelly Ferguson, Peter Rose, Deb Strater, Taryn Ferber, Donna White, Lynn Borzi, Eric Jenison, Nairmeen Haller, Debbie Thomas, Vivian von Gruenigen, Michele McCarroll, Joyce Neading, John Geisler, Stephanie Smiddy, David Cohn, Michele Vaughan, Luis Vaccarello, Elayna Freese, James Pavelka, Pam Plummer, William Nahhas, Ellen Cato, John Moroney, Mark Wysong, Tonia Combs, Marci Bowling, Brandon Fletcher, Yingli Wolinsky (Ohio); Susan Bolick, Donna Acosta, Catherine Flanagan (South Carolina); Martin Whiteside (Tennessee) and Georgina Armstrong and the Texas Registry, Cancer Epidemiology and Surveillance Branch, Department of State Health Services.
Funding
The AACES study was funded by NCI (R01CA142081). Additional support was provided by Metropolitan Detroit Cancer Surveillance System (MDCSS) with federal funds from the National Cancer Institute, National Institute of Health, Dept. of Health and Human Services, under Contract No. HHSN261201000028C and the Epidemiology Research Core, supported in part by NCI Center Grant (P30CA22453) to the Karmanos Cancer Institute, Wayne State University School of Medicine, and NCI Center Grant (P30CA072720) to the Rutgers Cancer Institute of New Jersey. The funders had no role in the design, analysis, or writing of this article.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kelemen, L.E., Abbott, S., Qin, B. et al. Cigarette smoking and the association with serous ovarian cancer in African American women: African American Cancer Epidemiology Study (AACES). Cancer Causes Control 28, 699–708 (2017). https://doi.org/10.1007/s10552-017-0899-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-017-0899-6