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Published in: Cancer Causes & Control 7/2013

01-07-2013 | Original paper

Risk of colorectal cancer associated with active smoking among female teachers

Authors: Susan Hurley, Debbie Goldberg, David O. Nelson, Yani Lu, Katherine Henderson, Leslie Bernstein, Peggy Reynolds

Published in: Cancer Causes & Control | Issue 7/2013

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Abstract

Purpose

The objective of this study was to examine the risk of colorectal cancer associated with active smoking among members of the California Teachers Study (CTS), a large cohort of female public school employees for whom highly detailed smoking information is available.

Methods

The analysis was conducted among the 122,264 CTS participants who lived in California at cohort entry in 1995/1996, had no prior history of colorectal cancer, and provided detailed smoking information. 1,205 cases of invasive colorectal cancer prospectively diagnosed in 1995–2009 were identified from the California Cancer Registry, including 650 in the proximal colon, 267 in the distal colon, and 288 in the rectum. Hazard ratios and 95 % confidence intervals were estimated using Cox proportional hazards models, stratified by age at cohort entry, and adjusted for race/ethnicity.

Results

Compared to never smokers, current smokers had an approximately 30 % increased risk of colorectal cancer. Overall, a slightly elevated risk was also noted for former smokers. Among former smokers, risks appeared to remain elevated for up to 20 years following cessation. Risks among former and current smokers increased with greater intensity and duration of smoking. Little evidence for heterogeneity in risk was noted for colon versus rectal cancer or for different subsites within the colon.

Conclusions

These results provide convincing evidence that heavy and/or long-term smoking is a risk factor for cancers of the colon and rectum. Such evidence should be considered when updating screening guidelines to include targeting people with long active smoking histories.
Literature
1.
go back to reference American Cancer Society (ACS) (2012) Cancer facts and figures 2012. Atlanta, GA USA American Cancer Society (ACS) (2012) Cancer facts and figures 2012. Atlanta, GA USA
2.
go back to reference Zisman AL, Nickolov A, Brand RE, Gorchow A, Roy HK (2006) Associations between the age at diagnosis and location of colorectal cancer and the use of alcohol and tobacco: implications for screening. Arch Intern Med 166(6):629–634PubMedCrossRef Zisman AL, Nickolov A, Brand RE, Gorchow A, Roy HK (2006) Associations between the age at diagnosis and location of colorectal cancer and the use of alcohol and tobacco: implications for screening. Arch Intern Med 166(6):629–634PubMedCrossRef
3.
go back to reference Giovannucci E (2004) Should smokers be considered a high-risk group for colorectal cancer? Dig Liver Dis 36(10):643–645PubMedCrossRef Giovannucci E (2004) Should smokers be considered a high-risk group for colorectal cancer? Dig Liver Dis 36(10):643–645PubMedCrossRef
5.
go back to reference U.S. Department of Health and Human Services (DHHS) (2004) The Health Consequences of Smoking: A Report of the Surgeon General. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office of Smoking and Health, Atlanta, GA, USA U.S. Department of Health and Human Services (DHHS) (2004) The Health Consequences of Smoking: A Report of the Surgeon General. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office of Smoking and Health, Atlanta, GA, USA
6.
go back to reference World Health Organization (WHO) International Agency for Research on Cancer (IARC) (ed) (2002) Tobacco smoke and involuntary smoking: IARC monographs on the evaluation of carcinogenic risks to humans: volume 83. IARC Press, Lyon World Health Organization (WHO) International Agency for Research on Cancer (IARC) (ed) (2002) Tobacco smoke and involuntary smoking: IARC monographs on the evaluation of carcinogenic risks to humans: volume 83. IARC Press, Lyon
7.
go back to reference World Health Organization (WHO) International Agency for Research on Cancer (IARC) (2012) IARC monographs on the evaluation of carcinogenic risks to humans. A review of human carcinogens: personal habits and indoor combustions, vol 100E. Lyon, France World Health Organization (WHO) International Agency for Research on Cancer (IARC) (2012) IARC monographs on the evaluation of carcinogenic risks to humans. A review of human carcinogens: personal habits and indoor combustions, vol 100E. Lyon, France
9.
go back to reference Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M (2009) The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 125(1):171–180. doi:10.1002/ijc.24343 PubMedCrossRef Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M (2009) The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 125(1):171–180. doi:10.​1002/​ijc.​24343 PubMedCrossRef
10.
11.
go back to reference Tsoi KK, Pau CY, Wu WK, Chan FK, Griffiths S, Sung JJ (2009) Cigarette smoking and the risk of colorectal cancer: a meta-analysis of prospective cohort studies. Clin Gastroenterol Hepatol 7(6):682–688 e681–685. doi:10.1016/j.cgh.2009.02.016 Tsoi KK, Pau CY, Wu WK, Chan FK, Griffiths S, Sung JJ (2009) Cigarette smoking and the risk of colorectal cancer: a meta-analysis of prospective cohort studies. Clin Gastroenterol Hepatol 7(6):682–688 e681–685. doi:10.​1016/​j.​cgh.​2009.​02.​016
12.
go back to reference Bernstein L, Allen M, Anton-Culver H, Deapen D, Horn-Ross PL, Peel D, Pinder R, Reynolds P, Sullivan-Halley J, West D, Wright W, Ziogas A, Ross RK (2002) High breast cancer incidence rates among California teachers: results from the California Teachers Study (United States). Cancer Causes Control 13(7):625–635PubMedCrossRef Bernstein L, Allen M, Anton-Culver H, Deapen D, Horn-Ross PL, Peel D, Pinder R, Reynolds P, Sullivan-Halley J, West D, Wright W, Ziogas A, Ross RK (2002) High breast cancer incidence rates among California teachers: results from the California Teachers Study (United States). Cancer Causes Control 13(7):625–635PubMedCrossRef
14.
go back to reference Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L (1986) A data-based approach to diet questionnaire design and testing. Am J Epidemiol 124(3):453–469PubMed Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L (1986) A data-based approach to diet questionnaire design and testing. Am J Epidemiol 124(3):453–469PubMed
15.
go back to reference Horn-Ross PL, Hoggatt KJ, West DW, Krone MR, Stewart SL, Anton H, Bernstei CL, Deapen D, Peel D, Pinder R, Reynolds P, Ross RK, Wright W, Ziogas A (2002) Recent diet and breast cancer risk: the California Teachers Study (USA). Cancer Causes Control 13(5):407–415PubMedCrossRef Horn-Ross PL, Hoggatt KJ, West DW, Krone MR, Stewart SL, Anton H, Bernstei CL, Deapen D, Peel D, Pinder R, Reynolds P, Ross RK, Wright W, Ziogas A (2002) Recent diet and breast cancer risk: the California Teachers Study (USA). Cancer Causes Control 13(5):407–415PubMedCrossRef
16.
18.
go back to reference Therneau TM, Grambsch PM (eds) (2000) Modeling survival data: extending the cox model. Springer, New York Therneau TM, Grambsch PM (eds) (2000) Modeling survival data: extending the cox model. Springer, New York
19.
go back to reference Cress RD, Morris C, Ellison GL, Goodman MT (2006) Secular changes in colorectal cancer incidence by subsite, stage at diagnosis, and race/ethnicity, 1992–2001. Cancer 107(5 Suppl):1142–1152. doi:10.1002/cncr.22011 PubMedCrossRef Cress RD, Morris C, Ellison GL, Goodman MT (2006) Secular changes in colorectal cancer incidence by subsite, stage at diagnosis, and race/ethnicity, 1992–2001. Cancer 107(5 Suppl):1142–1152. doi:10.​1002/​cncr.​22011 PubMedCrossRef
20.
go back to reference Gong J, Hutter C, Baron JA, Berndt S, Caan B, Campbell PT, Casey G, Chan AT, Cotterchio M, Fuchs CS, Gallinger S, Giovannucci E, Harrison T, Hayes R, Hsu L, Jiao S, Lin Y, Lindor NM, Newcomb P, Pflugeisen B, Phipps AI, Rohan T, Schoen R, Seminara D, Slattery ML, Stelling D, Thomas F, Warnick G, White E, Potter J, Peters U (2012) A pooled analysis of smoking and colorectal cancer: timing of exposure and interactions with environmental factors. Cancer Epidemiol Biomarkers Prev 21(11):1974–1985. doi:10.1158/1055-9965.EPI-12-0692 PubMedCrossRef Gong J, Hutter C, Baron JA, Berndt S, Caan B, Campbell PT, Casey G, Chan AT, Cotterchio M, Fuchs CS, Gallinger S, Giovannucci E, Harrison T, Hayes R, Hsu L, Jiao S, Lin Y, Lindor NM, Newcomb P, Pflugeisen B, Phipps AI, Rohan T, Schoen R, Seminara D, Slattery ML, Stelling D, Thomas F, Warnick G, White E, Potter J, Peters U (2012) A pooled analysis of smoking and colorectal cancer: timing of exposure and interactions with environmental factors. Cancer Epidemiol Biomarkers Prev 21(11):1974–1985. doi:10.​1158/​1055-9965.​EPI-12-0692 PubMedCrossRef
21.
go back to reference Giovannucci E (2001) An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 10(7):725–731PubMed Giovannucci E (2001) An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 10(7):725–731PubMed
22.
go back to reference Leufkens AM, Van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, Tjonneland A, Olsen A, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Palli D, Grioni S, Tumino R, Sacerdote C, Mattiello A, Herman S, Kaaks R, Steffen A, Boeing H, Trichopoulou A, Lagiou P, Trichopoulos D, Peeters PH, van Gils CH, van Kranen H, Lund E, Dumeaux V, Engeset D, Rodriguez L, Sanchez MJ, Chirlaque MD, Barricarte A, Manjer J, Almquist M, van Guelpen B, Hallmans G, Khaw KT, Wareham N, Tsilidis KK, Straif K, Leon-Roux M, Vineis P, Norat T, Riboli E, Bueno-de-Mesquita HB (2011) Cigarette smoking and colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition study. Clin Gastroenterol Hepatol 9(2):137–144. doi:10.1016/j.cgh.2010.10.012 PubMedCrossRef Leufkens AM, Van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, Tjonneland A, Olsen A, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Palli D, Grioni S, Tumino R, Sacerdote C, Mattiello A, Herman S, Kaaks R, Steffen A, Boeing H, Trichopoulou A, Lagiou P, Trichopoulos D, Peeters PH, van Gils CH, van Kranen H, Lund E, Dumeaux V, Engeset D, Rodriguez L, Sanchez MJ, Chirlaque MD, Barricarte A, Manjer J, Almquist M, van Guelpen B, Hallmans G, Khaw KT, Wareham N, Tsilidis KK, Straif K, Leon-Roux M, Vineis P, Norat T, Riboli E, Bueno-de-Mesquita HB (2011) Cigarette smoking and colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition study. Clin Gastroenterol Hepatol 9(2):137–144. doi:10.​1016/​j.​cgh.​2010.​10.​012 PubMedCrossRef
23.
25.
go back to reference Paskett ED, Reeves KW, Rohan TE, Allison MA, Williams CD, Messina CR, Whitlock E, Sato A, Hunt JR (2007) Association between cigarette smoking and colorectal cancer in the Women’s Health Initiative. J Natl Cancer Inst 99(22):1729–1735PubMedCrossRef Paskett ED, Reeves KW, Rohan TE, Allison MA, Williams CD, Messina CR, Whitlock E, Sato A, Hunt JR (2007) Association between cigarette smoking and colorectal cancer in the Women’s Health Initiative. J Natl Cancer Inst 99(22):1729–1735PubMedCrossRef
26.
go back to reference Terry PD, Miller AB, Rohan TE (2002) Prospective cohort study of cigarette smoking and colorectal cancer risk in women. Int J Cancer 99(3):480–483PubMedCrossRef Terry PD, Miller AB, Rohan TE (2002) Prospective cohort study of cigarette smoking and colorectal cancer risk in women. Int J Cancer 99(3):480–483PubMedCrossRef
27.
go back to reference Inoue M, Tajima K, Hirose K, Hamajima N, Takezaki T, Hirai T, Kato T, Ohno Y (1995) Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan. Cancer Causes Control 6(1):14–22PubMedCrossRef Inoue M, Tajima K, Hirose K, Hamajima N, Takezaki T, Hirai T, Kato T, Ohno Y (1995) Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan. Cancer Causes Control 6(1):14–22PubMedCrossRef
28.
go back to reference Schottenfeld D, Fraumeni JF (eds) (2006) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York Schottenfeld D, Fraumeni JF (eds) (2006) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York
29.
go back to reference Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC, Colditz GA (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108(3):433–442PubMedCrossRef Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC, Colditz GA (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108(3):433–442PubMedCrossRef
30.
go back to reference Bufill JA (1990) Colorectal cancer: evidence for distinct genetic categories based on proximal or distal tumor location. Ann Intern Med 113(10):779–788PubMedCrossRef Bufill JA (1990) Colorectal cancer: evidence for distinct genetic categories based on proximal or distal tumor location. Ann Intern Med 113(10):779–788PubMedCrossRef
31.
go back to reference Chyou PH, Nomura AM, Stemmermann GN (1996) A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 6(4):276–282PubMedCrossRef Chyou PH, Nomura AM, Stemmermann GN (1996) A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 6(4):276–282PubMedCrossRef
32.
go back to reference Hooker CM, Gallicchio L, Genkinger JM, Comstock GW, Alberg AJ (2008) A prospective cohort study of rectal cancer risk in relation to active cigarette smoking and passive smoke exposure. Ann Epidemiol 18(1):28–35 Hooker CM, Gallicchio L, Genkinger JM, Comstock GW, Alberg AJ (2008) A prospective cohort study of rectal cancer risk in relation to active cigarette smoking and passive smoke exposure. Ann Epidemiol 18(1):28–35
33.
go back to reference Otani T, Iwasaki M, Yamamoto S, Sobue T, Hanaoka T, Inoue M, Tsugane S (2003) Alcohol consumption, smoking, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan Public Health Center-based prospective study. Cancer Epidemiol Biomarkers Prev 12(12):1492–1500PubMed Otani T, Iwasaki M, Yamamoto S, Sobue T, Hanaoka T, Inoue M, Tsugane S (2003) Alcohol consumption, smoking, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan Public Health Center-based prospective study. Cancer Epidemiol Biomarkers Prev 12(12):1492–1500PubMed
34.
go back to reference Tverdal A, Thelle D, Stensvold I, Leren P, Bjartveit K (1993) Mortality in relation to smoking history: 13 years’ follow-up of 68,000 Norwegian men and women 35–49 years. J Clin Epidemiol 46(5):475–487PubMedCrossRef Tverdal A, Thelle D, Stensvold I, Leren P, Bjartveit K (1993) Mortality in relation to smoking history: 13 years’ follow-up of 68,000 Norwegian men and women 35–49 years. J Clin Epidemiol 46(5):475–487PubMedCrossRef
35.
go back to reference Verla-Tebit E, Lilla C, Hoffmeister M, Brenner H, Chang-Claude J (2006) Cigarette smoking and colorectal cancer risk in Germany: a population-based case-control study. Int J Cancer 119(3):630–635PubMedCrossRef Verla-Tebit E, Lilla C, Hoffmeister M, Brenner H, Chang-Claude J (2006) Cigarette smoking and colorectal cancer risk in Germany: a population-based case-control study. Int J Cancer 119(3):630–635PubMedCrossRef
36.
go back to reference Wakai K, Hayakawa N, Kojima M, Tamakoshi K, Watanabe Y, Suzuki K, Hashimoto S, Tokudome S, Toyoshima H, Ito Y, Tamakoshi A (2003) Smoking and colorectal cancer in a non-Western population: a prospective cohort study in Japan. J Epidemiol 13(6):323–332PubMedCrossRef Wakai K, Hayakawa N, Kojima M, Tamakoshi K, Watanabe Y, Suzuki K, Hashimoto S, Tokudome S, Toyoshima H, Ito Y, Tamakoshi A (2003) Smoking and colorectal cancer in a non-Western population: a prospective cohort study in Japan. J Epidemiol 13(6):323–332PubMedCrossRef
37.
go back to reference Ji BT, Dai Q, Gao YT, Hsing AW, McLaughlin JK, Fraumeni JFJ, Chow WH (2002) Cigarette and alcohol consumption and the risk of colorectal cancer in Shanghai, China. Eur J Cancer Prev 11(3):237–244PubMedCrossRef Ji BT, Dai Q, Gao YT, Hsing AW, McLaughlin JK, Fraumeni JFJ, Chow WH (2002) Cigarette and alcohol consumption and the risk of colorectal cancer in Shanghai, China. Eur J Cancer Prev 11(3):237–244PubMedCrossRef
38.
go back to reference Minami Y, Tateno H (2003) Associations between cigarette smoking and the risk of four leading cancers in Miyagi Prefecture, Japan: a multi-site case-control study. Cancer Sci 94(6):540–547PubMedCrossRef Minami Y, Tateno H (2003) Associations between cigarette smoking and the risk of four leading cancers in Miyagi Prefecture, Japan: a multi-site case-control study. Cancer Sci 94(6):540–547PubMedCrossRef
39.
go back to reference Newcomb PA, Storer BE, Marcus PM (1995) Cigarette smoking in relation to risk of large bowel cancer in women. Cancer Res 55(21):4906–4909PubMed Newcomb PA, Storer BE, Marcus PM (1995) Cigarette smoking in relation to risk of large bowel cancer in women. Cancer Res 55(21):4906–4909PubMed
40.
go back to reference Nyren O, Bergstrom R, Nystrom L, Engholm G, Ekbom A, Adami HO, Knutsson A, Stjernberg N (1996) Smoking and colorectal cancer: a 20-year follow-up study of Swedish construction workers. J Natl Cancer Inst 88(18):1302–1307PubMedCrossRef Nyren O, Bergstrom R, Nystrom L, Engholm G, Ekbom A, Adami HO, Knutsson A, Stjernberg N (1996) Smoking and colorectal cancer: a 20-year follow-up study of Swedish construction workers. J Natl Cancer Inst 88(18):1302–1307PubMedCrossRef
41.
go back to reference Sandler RS, Sandler DP, Comstock GW, Helsing KJ, Shore DL (1988) Cigarette smoking and the risk of colorectal cancer in women. J Natl Cancer Inst 80(16):1329–1333PubMedCrossRef Sandler RS, Sandler DP, Comstock GW, Helsing KJ, Shore DL (1988) Cigarette smoking and the risk of colorectal cancer in women. J Natl Cancer Inst 80(16):1329–1333PubMedCrossRef
42.
go back to reference Terry P, Ekbom A, Lichtenstein P, Feychting M, Wolk A (2001) Long-term tobacco smoking and colorectal cancer in a prospective cohort study. Int J Cancer 91(4):585–587PubMedCrossRef Terry P, Ekbom A, Lichtenstein P, Feychting M, Wolk A (2001) Long-term tobacco smoking and colorectal cancer in a prospective cohort study. Int J Cancer 91(4):585–587PubMedCrossRef
43.
go back to reference Luchtenborg M, White KK, Wilkens L, Kolonel LN, Le Marchand L (2007) Smoking and colorectal cancer: different effects by type of cigarettes? Cancer Epidemiol Biomarkers Prev 16(7):1341–1347PubMedCrossRef Luchtenborg M, White KK, Wilkens L, Kolonel LN, Le Marchand L (2007) Smoking and colorectal cancer: different effects by type of cigarettes? Cancer Epidemiol Biomarkers Prev 16(7):1341–1347PubMedCrossRef
44.
go back to reference Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ (2010) Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst 102(14):1012–1022. doi:10.1093/jnci/djq201 PubMedCrossRef Limsui D, Vierkant RA, Tillmans LS, Wang AH, Weisenberger DJ, Laird PW, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ (2010) Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst 102(14):1012–1022. doi:10.​1093/​jnci/​djq201 PubMedCrossRef
45.
go back to reference Poynter JN, Haile RW, Siegmund KD, Campbell PT, Figueiredo JC, Limburg P, Young J, Le Marchand L, Potter JD, Cotterchio M, Casey G, Hopper JL, Jenkins MA, Thibodeau SN, Newcomb PA, Baron JA (2009) Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol Biomarkers Prev 18(10):2745–2750. doi:10.1158/1055-9965.EPI-09-0517 PubMedCrossRef Poynter JN, Haile RW, Siegmund KD, Campbell PT, Figueiredo JC, Limburg P, Young J, Le Marchand L, Potter JD, Cotterchio M, Casey G, Hopper JL, Jenkins MA, Thibodeau SN, Newcomb PA, Baron JA (2009) Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol Biomarkers Prev 18(10):2745–2750. doi:10.​1158/​1055-9965.​EPI-09-0517 PubMedCrossRef
46.
go back to reference Slattery ML, Potter JD, Samowitz W, Bigler J, Caan B, Leppert M (1998) NAT2, GSTM-1, cigarette smoking, and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 7(12):1079–1084PubMed Slattery ML, Potter JD, Samowitz W, Bigler J, Caan B, Leppert M (1998) NAT2, GSTM-1, cigarette smoking, and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 7(12):1079–1084PubMed
47.
go back to reference Limburg PJ, Vierkant RA, Cerhan JR, Yang P, Lazovich D, Potter JD, Sellers TA (2003) Cigarette smoking and colorectal cancer: long-term, subsite-specific risks in a cohort study of postmenopausal women. Clin Gastroenterol Hepatol 1(3):202–210PubMedCrossRef Limburg PJ, Vierkant RA, Cerhan JR, Yang P, Lazovich D, Potter JD, Sellers TA (2003) Cigarette smoking and colorectal cancer: long-term, subsite-specific risks in a cohort study of postmenopausal women. Clin Gastroenterol Hepatol 1(3):202–210PubMedCrossRef
48.
go back to reference Leufkens AM, van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, Tjonneland A, Olsen A, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Palli D, Grioni S, Tumino R, Sacerdote C, Mattiello A, Herman S, Kaaks R, Steffen A, Boeing H, Trichopoulou A, Lagiou P, Trichopoulos D, Peeters PH, van Gils CH, van Kranen H, Lund E, Dumeaux V, Engeset D, Rodriguez L, Sanchez MJ, Chirlaque MD, Barricarte A, Manjer J, Almquist M, van Guelpen B, Hallmans G, Khaw KT, Wareham N, Tsilidis KK, Straif K, Leon-Roux M, Vineis P, Norat T, Riboli E, Bueno-de-Mesquita HB (2011) Cigarette smoking and colorectal cancer risk in the EPIC study. Clin Gastroenterol Hepatol 9(2):137–144 Leufkens AM, van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, Tjonneland A, Olsen A, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Palli D, Grioni S, Tumino R, Sacerdote C, Mattiello A, Herman S, Kaaks R, Steffen A, Boeing H, Trichopoulou A, Lagiou P, Trichopoulos D, Peeters PH, van Gils CH, van Kranen H, Lund E, Dumeaux V, Engeset D, Rodriguez L, Sanchez MJ, Chirlaque MD, Barricarte A, Manjer J, Almquist M, van Guelpen B, Hallmans G, Khaw KT, Wareham N, Tsilidis KK, Straif K, Leon-Roux M, Vineis P, Norat T, Riboli E, Bueno-de-Mesquita HB (2011) Cigarette smoking and colorectal cancer risk in the EPIC study. Clin Gastroenterol Hepatol 9(2):137–144
49.
go back to reference Le Marchand L, Wilkens LR, Kolonel LN, Hankin JH, Lyu LC (1997) Associations of sedentary lifestyle, obesity, smoking, alcohol use, and diabetes with the risk of colorectal cancer. Cancer Res 57(21):4787–4794PubMed Le Marchand L, Wilkens LR, Kolonel LN, Hankin JH, Lyu LC (1997) Associations of sedentary lifestyle, obesity, smoking, alcohol use, and diabetes with the risk of colorectal cancer. Cancer Res 57(21):4787–4794PubMed
50.
go back to reference Akhter M, Nishino Y, Nakaya N, Kurashima K, Sato Y, Kuriyama S, Tsubono Y, Tsuji I (2007) Cigarette smoking and the risk of colorectal cancer among men: a prospective study in Japan. Eur J Cancer Prev 16(2):102–107PubMedCrossRef Akhter M, Nishino Y, Nakaya N, Kurashima K, Sato Y, Kuriyama S, Tsubono Y, Tsuji I (2007) Cigarette smoking and the risk of colorectal cancer among men: a prospective study in Japan. Eur J Cancer Prev 16(2):102–107PubMedCrossRef
51.
go back to reference Luchtenborg M, Weijenberg MP, de Goeij AF, Wark PA, Brink M, Roemen GM, Lentjes MH, de Bruine AP, Goldbohm RA, van ‘t Veer P, van den Brandt PA (2005) Meat and fish consumption, APC gene mutations and hMLH1 expression in colon and rectal cancer: a prospective cohort study (The Netherlands). Cancer Causes Control 16(9):1041–1054. doi:10.1007/s10552-005-0239-0 PubMedCrossRef Luchtenborg M, Weijenberg MP, de Goeij AF, Wark PA, Brink M, Roemen GM, Lentjes MH, de Bruine AP, Goldbohm RA, van ‘t Veer P, van den Brandt PA (2005) Meat and fish consumption, APC gene mutations and hMLH1 expression in colon and rectal cancer: a prospective cohort study (The Netherlands). Cancer Causes Control 16(9):1041–1054. doi:10.​1007/​s10552-005-0239-0 PubMedCrossRef
53.
go back to reference Kim HJ, Lee SM, Choi NK, Kim SH, Song HJ, Cho YK, Park BJ (2006) Smoking and colorectal cancer risk in the Korean elderly. J Prev Med Public Health 39(2):123–129PubMed Kim HJ, Lee SM, Choi NK, Kim SH, Song HJ, Cho YK, Park BJ (2006) Smoking and colorectal cancer risk in the Korean elderly. J Prev Med Public Health 39(2):123–129PubMed
54.
go back to reference Heineman EF, Zahm SH, McLaughlin JK, Vaught JB (1994) Increased risk of colorectal cancer among smokers: results of a 26-year follow-up of US veterans and a review. Int J Cancer 59(6):728–738PubMedCrossRef Heineman EF, Zahm SH, McLaughlin JK, Vaught JB (1994) Increased risk of colorectal cancer among smokers: results of a 26-year follow-up of US veterans and a review. Int J Cancer 59(6):728–738PubMedCrossRef
55.
go back to reference Luchtenborg M, Weijenberg MP, Kampman E, van Muijen GN, Roemen GM, Zeegers MP, Goldbohm RA, van ‘t Veer P, de Goeij AF, van den Brandt PA (2005) Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am J Epidemiol 161(9):806–815. doi:10.1093/aje/kwi114 PubMedCrossRef Luchtenborg M, Weijenberg MP, Kampman E, van Muijen GN, Roemen GM, Zeegers MP, Goldbohm RA, van ‘t Veer P, de Goeij AF, van den Brandt PA (2005) Cigarette smoking and colorectal cancer: APC mutations, hMLH1 expression, and GSTM1 and GSTT1 polymorphisms. Am J Epidemiol 161(9):806–815. doi:10.​1093/​aje/​kwi114 PubMedCrossRef
56.
go back to reference Zhao J, Halfyard B, Roebothan B, West R, Buehler S, Sun Z, Squires J, McLaughlin JR, Parfrey PS, Wang PP (2010) Tobacco smoking and colorectal cancer: a population-based case-control study in Newfoundland and Labrador. Can J Public Health 101(4):281–289PubMed Zhao J, Halfyard B, Roebothan B, West R, Buehler S, Sun Z, Squires J, McLaughlin JR, Parfrey PS, Wang PP (2010) Tobacco smoking and colorectal cancer: a population-based case-control study in Newfoundland and Labrador. Can J Public Health 101(4):281–289PubMed
58.
go back to reference Benjamini Y, Hochberg Y (1995) Controlling the false recovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57(1):289–300 Benjamini Y, Hochberg Y (1995) Controlling the false recovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57(1):289–300
59.
go back to reference Koh WP, Nelson HH, Yuan JM, Van den Berg D, Jin A, Wang R, Yu MC (2011) Glutathione S-transferase (GST) gene polymorphisms, cigarette smoking and colorectal cancer risk among Chinese in Singapore. Carcinogenesis 32(10):1507–1511. doi:10.1093/carcin/bgr175 PubMedCrossRef Koh WP, Nelson HH, Yuan JM, Van den Berg D, Jin A, Wang R, Yu MC (2011) Glutathione S-transferase (GST) gene polymorphisms, cigarette smoking and colorectal cancer risk among Chinese in Singapore. Carcinogenesis 32(10):1507–1511. doi:10.​1093/​carcin/​bgr175 PubMedCrossRef
60.
go back to reference Lilla C, Verla-Tebit E, Risch A, Jager B, Hoffmeister M, Brenner H, Chang-Claude J (2006) Effect of NAT1 and NAT2 genetic polymorphisms on colorectal cancer risk associated with exposure to tobacco smoke and meat consumption. Cancer Epidemiol Biomarkers Prev 15(1):99–107PubMedCrossRef Lilla C, Verla-Tebit E, Risch A, Jager B, Hoffmeister M, Brenner H, Chang-Claude J (2006) Effect of NAT1 and NAT2 genetic polymorphisms on colorectal cancer risk associated with exposure to tobacco smoke and meat consumption. Cancer Epidemiol Biomarkers Prev 15(1):99–107PubMedCrossRef
61.
go back to reference Rudolph A, Hein R, Hoffmeister M, Forsti A, Hemminki K, Risch A, Brenner H, Chang-Claude J (2012) Copy number variations of GSTT1 and GSTM1, colorectal cancer risk and possible effect modification of cigarette smoking and menopausal hormone therapy. Int J Cancer. doi:10.1002/ijc.27428 Rudolph A, Hein R, Hoffmeister M, Forsti A, Hemminki K, Risch A, Brenner H, Chang-Claude J (2012) Copy number variations of GSTT1 and GSTM1, colorectal cancer risk and possible effect modification of cigarette smoking and menopausal hormone therapy. Int J Cancer. doi:10.​1002/​ijc.​27428
62.
go back to reference Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ (2012) Cigarette smoking and colorectal cancer risk by KRAS mutation status among older women. Am J Gastroenterol. doi:10.1038/ajg.2012.21 Samadder NJ, Vierkant RA, Tillmans LS, Wang AH, Lynch CF, Anderson KE, French AJ, Haile RW, Harnack LJ, Potter JD, Slager SL, Smyrk TC, Thibodeau SN, Cerhan JR, Limburg PJ (2012) Cigarette smoking and colorectal cancer risk by KRAS mutation status among older women. Am J Gastroenterol. doi:10.​1038/​ajg.​2012.​21
63.
go back to reference Slattery ML, Edwards S, Curtin K, Schaffer D, Neuhausen S (2003) Associations between smoking, passive smoking, GSTM-1, NAT2, and rectal cancer. Cancer Epidemiol Biomarkers Prev 12(9):882–889PubMed Slattery ML, Edwards S, Curtin K, Schaffer D, Neuhausen S (2003) Associations between smoking, passive smoking, GSTM-1, NAT2, and rectal cancer. Cancer Epidemiol Biomarkers Prev 12(9):882–889PubMed
Metadata
Title
Risk of colorectal cancer associated with active smoking among female teachers
Authors
Susan Hurley
Debbie Goldberg
David O. Nelson
Yani Lu
Katherine Henderson
Leslie Bernstein
Peggy Reynolds
Publication date
01-07-2013
Publisher
Springer Netherlands
Published in
Cancer Causes & Control / Issue 7/2013
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-013-0207-z

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