Journal of the National Cancer Institute Advance Access originally published online on November 13, 2007
JNCI Journal of the National Cancer Institute 2007 99(22):1729-1735; doi:10.1093/jnci/djm176
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© The Author 2007. Published by Oxford University Press.
Association Between Cigarette Smoking and Colorectal Cancer in the Women’s Health Initiative
Affiliations of authors: Division of Population Sciences, Center for Population Health and Health Disparities, Comprehensive Cancer Center and Division of Epidemiology, School of Public Health, The Ohio State University, Columbus, OH (EDP); Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA (KWR); Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY (TER); Department of Family and Preventive Medicine, University of California, San Diego, CA (MAA); Howard University Cancer Center, Washington, DC (CDW); Department of Preventive Medicine, Stony Brook University, Stony Brook, NY (CRM); Kaiser Permanente Center for Health Research, Portland, OR (EW); Fred Hutchinson Cancer Research Center, Seattle, WA (AS, JRH)
Correspondence to: Electra D. Paskett, PhD, 320 West Tenth Ave, A356 Starling Loving Hall, Columbus, OH 43210 (e-mail: electra.paskett{at}osumc.edu).
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ABSTRACT |
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The evidence linking cigarette smoking to the risk of colorectal cancer is inconsistent. We investigated the associations between active and passive smoking and colorectal cancer among 146877 Women's Health Initiative participants. Women reported detailed smoking histories at enrollment. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated for the association between smoking and overall and site-specific risk of colorectal cancer. Invasive colorectal cancer was diagnosed in 1242 women over an average of 7.8 years (range = 0.003–11.2 years) of follow-up. In adjusted analyses, statistically significant positive associations were observed between most measures of cigarette smoking and risk of invasive colorectal cancer. Site-specific analyses indicated that current smokers had a statistically significantly increased risk of rectal cancer (HR = 1.95, 95% CI = 1.10 to 3.47) but not colon cancer (HR = 1.03, 95% CI = 0.77 to 1.38), compared with never smokers. Passive smoke exposure was not associated with colorectal cancer in adjusted analyses. Thus, active exposure to cigarette smoking appears to be a risk factor for rectal cancer.
Prior knowledge The evidence for the association between cigarette smoking and the risk of colorectal cancer is inconsistent. Study design Pooled analysis of the association between cigarette smoking and colorectal cancer among participants in the observational study and the three clinical trials of the Women's Health Initiative. Contribution Statistically significant positive associations between most measures of cigarette smoking and colorectal cancer were observed. Current smokers have a statistically significantly increased risk of rectal cancer but not colon cancer, compared with never smokers. Passive smoke exposure was not associated with colorectal cancer in adjusted analyses. Implications Active cigarette smoking appears to be a risk factor for rectal cancer. Limitations Smoking exposure was self-reported and does not account for any change in smoking behavior during follow-up. Because multiple comparisons were performed, the findings of this study might be due to chance. The rate of current smoking in women in this study was lower than US women with similar ages.
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Among American women, nearly 11% of incident cancers and 10% of cancer deaths are due to colorectal cancer (1). The association between tobacco exposure and colorectal cancer is controversial. Early studies investigating cigarette smoking and colorectal cancer risk reported no association (2–8), possibly because the reported smoking duration was too short to demonstrate the hypothesized long induction period of smoking-associated colorectal cancer (9). Recent investigations, with more thorough measurement of smoking exposure and longer exposure periods, have reported a positive relationship between cigarette smoking and the risk of colorectal cancer (10–19), although some studies report that this relationship is limited to rectal cancer (20,21). Results from other studies are also inconsistent, with some reporting no association (22,23) and others reporting no association among women (24,25). The few studies examining the effect of passive smoke exposure on risk of colorectal cancer report conflicting results (24,26–28).
We investigated associations between cigarette smoking and colorectal cancer in the Women's Health Initiative (WHI). The WHI includes an observational study and three clinical trials, which have been described previously (29–32). This report includes a pooled analysis of participants in the observational study and three clinical trials, excluding those with prior cancers other than nonmelanoma skin cancer (14193; 2546 in the clinical trials and 11647 in the observational study) or lack of follow-up (678; 220 in the clinical trials and 458 in the observational study). The final sample included 146877 women (81518 in the observational study and 65359 in the clinical trials) with follow-up through March 31, 2005 (mean 7.8 years, range = 0.003–11.2 years). All participants provided written informed consent; protocols and procedures were approved by Institutional Review Boards at participating institutions. Colorectal cancer cases were reported and adjudicated as previously described (33). This analysis included only patients with adjudicated colorectal cancer. We also examined subgroups of invasive colorectal cancer defined as colon, rectal (i.e., rectum and rectal-sigmoid colon), and right-sided (i.e., ascending colon and cecum) and left-sided (i.e., descending and sigmoid colon) cancer.
At baseline, participants were classified as "never," "past," or "current" smokers on the basis of whether they had ever smoked more than 100 cigarettes in their lifetime and if they smoked at the time of the survey. Women reporting any history of smoking provided data about their smoking and smoking cessation behavior with a choice of categoric responses; these categories were collapsed in the present analysis to avoid small cell counts (see Appendix). Women in the observational study also reported their exposure to passive (i.e., secondhand) smoke. Participants who ever lived or worked with a smoker were classified as "ever" exposed to passive smoke, and those who did not were classified as "never." Analyses involving passive smoke exposure excluded women reporting any active smoking history.
Characteristics of the total population and cancer subgroups were compared with t tests for continuous variables and chi-square tests for categoric variables. Cox proportional hazards models were used to estimate the effects of the smoking variables on the risk of invasive colorectal cancer, colon, rectal, and right-sided and left-sided cancer. Separate regressions were performed for each cancer outcome, and one smoking variable was included per regression model. Variables associated with invasive colorectal cancer in bivariate analyses were included as covariates in the regression models if their P value was .10 or less. Hazard ratios (HRs) and 95% confidence intervals (CIs) were reported for the smoking variables in each model. Tests for linear trend were performed by sequentially coding each level of the categoric smoking variables beginning with zero and then testing for a linear trend across the groups. Models were additionally adjusted for the possible effect of study design and hormone trial treatment arm by stratification (categorized as observational study, nonhormone trial–clinical trial, estrogen trial active arm, estrogen trial placebo arm, estrogen and progestin active arm, and estrogen and progestin placebo arm). The proportional hazards assumption was checked by modeling colorectal cancer by a time by smoking interaction term in a proportional hazards model along with a smoking main effects term. This procedure was done for each of the smoking variables; none indicated that the proportional hazards assumption was violated. All tests were two-sided. All analyses were performed in SAS version 9.0 (SAS Institute, Inc, Cary, NC).
The 1242 cases of incident invasive colorectal cancer were distributed as follows: 1075 were colon, 176 were rectal, 461 were right-sided, and 296 were left-sided cancers. Table 1 describes the characteristics of the sample by colorectal cancer status. Women not diagnosed with colorectal cancer were younger (P<.001), less likely to have a family history of colorectal cancer (P = .02), and had lower body mass index (P<.001) than those diagnosed with colorectal cancer. There were statistically significant differences between patients with colorectal cancer and participants without colorectal cancer with respect to current smoking status (P = .05), age at smoking initiation (P = .03), cigarettes smoked per day (P = .006), and duration of smoking (P<.001).
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Table 2 reports multivariable associations between smoking characteristics and total colorectal cancer, colon cancer, and rectal cancer. For total colorectal cancer, statistically significant positive trends were observed for cigarettes per day, duration of smoking, and age at cessation. Similar patterns were observed for colon, rectal, and right-sided cancers, although no statistically significant associations were observed for left-sided cancers (data not shown). Compared with never smokers, current smokers experienced a statistically significantly increased risk of rectal cancer (HR = 1.95, 95% CI = 1.10 to 3.47) but not colon cancer (HR = 1.03, 95% CI = 0.77 to 1.38). No statistically significant associations were observed between passive smoking and colorectal cancer.
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The elevated risk of rectal cancer appears to drive the associations between smoking behavior and overall colorectal cancer risk. This observation has been reported in previous studies (20,21). Comparisons among site-specific cancer subgroups showed positive associations for right-sided but not left-sided colon cancers. Carcinogens found in cigarettes may reach the colorectal mucosa through direct ingestion (34) or through the circulatory system (35). Colorectal adenomas are known to be precursor lesions for colorectal cancer, and an increased risk of adenomas has been observed among past and current smokers (10,11,36–40). Cigarette smoking may increase the risk of developing hyperplastic polyps (41–46), which may also be related to the development of colorectal cancer (47–50).
Our study had several limitations. Given the multiple comparisons performed, our findings could be due to chance. The finding of no association between passive smoking and colorectal cancer is in agreement with a recent study (26). Exposure to passive smoking is difficult to measure; therefore, our results may have been affected by measurement error that obscured a true effect. Our use of self-reported smoking exposures using categories of exposure is a potential limitation. Small cell counts in the highest categories of the smoking variables necessitated collapsing of categories, and the broad groupings used limit our ability to detect dose–response effects. Furthermore, our results do not account for changes in smoking behavior occurring after the baseline visit. External validity may be limited because the rate of current smoking was lower in the study sample (6.9%) than in similar-age US women (8.1%, aged 
65 years) (51), although the prevalence of past smoking in the study sample (41.7%) was identical to the rate reported for US men and women aged 65–74 years (52).
The study population of more than 140000 women, many of whom reported lengthy smoking histories, is a substantial strength. Other strengths include the prospective nature, diverse population, and central adjudication of colorectal cancer outcomes.
In summary, we report an increased risk of colorectal cancer, specifically of rectal cancer, with cigarette smoking, in agreement with previous studies (10–19). Our data add to the extensive evidence indicating that preventing smoking initiation and decreasing the duration of smoking might reduce colorectal cancer risk.
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Funding |
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TopAbstractContext and CaveatsFundingAppendix: original and...ReferencesNotes |
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The Women's Health Initiative was funded by the National Heart, Lung, and Blood Institute, National Institutes of Health, Department of Health and Human Services.
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Appendix: Original and Recategorized Smoking Variables |
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Appendix Table 1. Age at smoking initiation: original and recategorized smoking variables
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Appendix Table 2. Number of cigarettes smoked per day: original and recategorized smoking variables
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Appendix Table 3. Duration of smoking: original and recategorized smoking variables
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NOTES |
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TopAbstractContext and CaveatsFundingAppendix: original and...ReferencesNotes |
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We wish to thank all WHI investigators and participants for their contributions. The following list is a short list of WHI investigators.
Program Office: Elizabeth Nabel, Jacques Rossouw, Shari Ludlam, Linda Pottern, Joan McGowan, Leslie Ford, and Nancy Geller (National Heart, Lung, and Blood Institute, Bethesda, MD).
Clinical Coordinating Centers: Ross Prentice, Garnet Anderson, Andrea LaCroix, Charles L. Kooperberg, Ruth E. Patterson, Anne McTiernan (Fred Hutchinson Cancer Research Center, Seattle, WA); Sally Shumaker (Wake Forest University School of Medicine, Winston-Salem, NC); Evan Stein (Medical Research Labs, Highland Heights, KY); Steven Cummings (University of California at San Francisco, San Francisco, CA).
Clinical Centers: Sylvia Wassertheil-Smoller (Albert Einstein College of Medicine, Bronx, NY); Jennifer Hays (Baylor College of Medicine, Houston, TX); JoAnn Manson (Brigham and Women's Hospital, Harvard Medical School, Boston, MA); Annlouise R. Assaf (Brown University, Providence, RI); Lawrence Phillips (Emory University, Atlanta, GA); Shirley Beresford (Fred Hutchinson Cancer Research Center, Seattle, WA); Judith Hsia (George Washington University Medical Center, Washington, DC); Rowan Chlebowski (Los Angeles Biomedical Research Institute at Harbor–UCLA Medical Center, Torrance, CA); Evelyn Whitlock (Kaiser Permanente Center for Health Research, Portland, OR); Bette Caan (Kaiser Permanente Division of Research, Oakland, CA); Jane Morley Kotchen (Medical College of Wisconsin, Milwaukee, WI); Barbara V. Howard (MedStar Research Institute/Howard University, Washington, DC); Linda Van Horn (Northwestern University, Chicago/Evanston, IL); Henry Black (Rush Medical Center, Chicago, IL); Marcia L. Stefanick (Stanford Prevention Research Center, Stanford, CA); Dorothy Lane (State University of New York at Stony Brook, Stony Brook, NY); Rebecca Jackson (The Ohio State University, Columbus, OH); Cora E. Lewis (University of Alabama at Birmingham, Birmingham, AL); Tamsen Bassford (University of Arizona, Tucson/Phoenix, AZ); Jean Wactawski-Wende (University at Buffalo, Buffalo, NY); John Robbins (University of California at Davis, Sacramento, CA); F. Allan Hubbell (University of California at Irvine, CA); Howard Judd (University of California at Los Angeles, Los Angeles, CA); Robert D. Langer (University of California at San Diego, LaJolla/Chula Vista, CA); Margery Gass (University of Cincinnati, Cincinnati, OH); Marian Limacher (University of Florida, Gainesville/Jacksonville, FL); David Curb (University of Hawaii, Honolulu, HI); Robert Wallace (University of Iowa, Iowa City/Davenport, IA); Judith Ockene (University of Massachusetts/Fallon Clinic, Worcester, MA); Norman Lasser (University of Medicine and Dentistry of New Jersey, Newark, NJ); Mary Jo O’Sullivan (University of Miami, Miami, FL); Karen Margolis (University of Minnesota, Minneapolis, MN); Robert Brunner (University of Nevada, Reno, NV); Gerardo Heiss (University of North Carolina, Chapel Hill, NC); Lewis Kuller (University of Pittsburgh, Pittsburgh, PA); Karen C. Johnson (University of Tennessee, Memphis, TN); Robert Brzyski (University of Texas Health Science Center, San Antonio, TX); Gloria E. Sarto (University of Wisconsin, Madison, WI); Denise Bonds (Wake Forest University School of Medicine, Winston-Salem, NC); Susan Hendrix (Wayne State University School of Medicine/Hutzel Hospital, Detroit, MI).
The sponsor played a role in the design and analysis of the WHI. The authors had full responsibility for the analysis and interpretation of the data and the writing and submission of the manuscript.
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Manuscript received May 29, 2007; revised September 4, 2007; accepted September 5, 2007.
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