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Research Articles

Smoking and Colorectal Cancer: Different Effects by Type of Cigarettes?

Margreet Lüchtenborg, Kami K.L. White, Lynne Wilkens, Laurence N. Kolonel and Loïc Le Marchand
Margreet Lüchtenborg
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Kami K.L. White
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Lynne Wilkens
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Laurence N. Kolonel
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Loïc Le Marchand
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DOI: 10.1158/1055-9965.EPI-06-0519 Published July 2007
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Tables

  • Table 1.

    Characteristics of colorectal cancer cases and controls: median (interquartile range), except where noted

    Male
    Female
    Case (n = 1,143)Control (n = 1,143)Case (n = 816)Control (n = 816)
    Age, y67 (60-73)67 (60-73)67 (58-73)67 (58-73)
    Ethnicity*
        Japanese605 (53)605 (53)447 (55)447 (55)
        Caucasian303 (27)303 (27)192 (24)192 (24)
        Native Hawaiian116 (10)116 (10)85 (10)85 (10)
        Filipino70 (6)70 (6)50 (6)50 (6)
        Chinese49 (4)49 (4)42 (5)42 (5)
    Family history*,†158 (14)87 (8)129 (16)60 (7)
    Lifetime recreational activities, h3,264 (288-10,080)5,184 (1,008-12,348)384 (0-2,880)624 (0-3,384)
    Body mass index 5 y ago, kg/m225 (23-28)24 (22-27)23 (21-26)23 (21-26)
    Dietary intake‡
        Energy, kcal/d2,338 (1,796-3,035)2,119 (1,657-2,712)1,756 (1,321-2,228)1,650 (1,270-2,120)
        NSP from vegetables, g/d3.0 (1.8-4.4)3.6 (2.2-5.0)3.0 (2.1-4.1)3.5 (2.3-5.0)
        Total calcium§, mg/d718 (507-1,108)782 (543-1,460)763 (489-2,307)984 (510-3,998)
        Alcohol, g/d2.3 (0.1-24)1.3 (0.1-16)0.1 (0-0.4)0.1 (0-0.3)
        Eggs, g/d18 (10-36)15 (7-27)12 (5-22)8 (4-17)
        Methionine, g/d1.8 (1.6-2.1)1.8 (1.6-2.1)1.4 (1.2-1.6)1.4 (1.3-1.6)
    Smoking characteristics*
        Never smoker298 (26)380 (33)489 (60)529 (65)
        Former smoker615 (54)584 (51)214 (26)185 (23)
        Current smoker230 (20)179 (16)113 (14)101 (12)
        Age started∥18 (16-20)18 (16-20)20 (18-25)20 (18-25)
        Time since smoking commenced, y∥48 (41-54)48 (41-55)42 (33-50)41 (33-49)
        Amount∥, cigarettes/pipes/cigars per day20 (15-36)20 (11-30)15 (8-20)10 (6-20)
        Duration∥, y33 (22-43)31 (19-42)31 (18-43)28 (13-37)
        Pack-years
            All tobacco products∥36 (17-59)28 (12-48)20 (7-40)15 (5-35)
            Non-filtered cigarettes¶16 (7-33)11 (5-24)9 (3-20)5 (1,11)
            Filtered cigarettes¶28 (14-45)23 (10-40)19 (7-35)16 (7-30)
            Cigars¶2 (1-6)2 (0-5)3 (2-3)2 (2-4)
            Pipe¶1 (0-4)1 (0-4)****
    • Abbreviation: NSP, non-starch polysaccharides.

    • ↵* n (%).

    • ↵† Family history of colorectal cancer among parents and siblings.

    • ↵‡ Dietary intakes (except energy) are calorie adjusted.

    • ↵§ From foods and supplements.

    • ↵∥ Among smokers.

    • ↵¶ Among smokers of specific tobacco product.

    • ↵** No data available, only two women reported pipe smoking.

  • Table 2.

    Colorectal cancer risk by smoking status, intensity, duration, and latency period

    Male (1,112 case-control pairs)
    Female (815 case-control pairs)
    n*OR (95% CI)†n*OR (95% CI)†
    Never smoker (reference group)363/2821.00529/4891.00
    Smoking status
        Former smoker574/6071.21 (0.97-1.50)185/2131.32 (1.02-1.71)
        Current smoker175/2231.32 (0.99-1.76)101/1131.17 (0.85-1.62)
    Intensity (cigarettes per day)‡
        MalesFemales
            1-101-5175/1590.94 (0.62-1.43)54/641.88 (1.02-3.45)
            11-206-10275/2821.00 (0.67-1.49)81/661.06 (0.58-1.94)
            21-3011-20140/1390.89 (0.56-1.42)90/1101.68 (0.90-3.15)
            >30>20156/2471.51 (0.99-2.29)61/851.73 (0.87-3.43)
        Ptrend§0.0070.33
    Duration (y)‡
        1-1084/741.12 (0.70-1.80)55/531.74 (0.95-3.16)
        11-20130/1130.96 (0.63-1.48)47/441.56 (0.80-3.03)
        21-30153/1771.24 (0.80-1.91)64/651.76 (0.90-3.43)
        31-40168/2041.22 (0.78-1.91)66/711.80 (0.85-3.80)
        >40212/2601.18 (0.71-1.96)54/923.17 (1.40-7.19)
        Ptrend§0.390.06
    Time since smoking commenced (y)∥
        1-3049/471.18 (0.61-2.32)52/511.54 (0.75-3.13)
        31-40119/1451.14 (0.70-1.87)89/931.35 (0.74-2.46)
        41-50284/2921.07 (0.71-1.59)90/1031.23 (0.68-2.24)
        >50297/3441.05 (0.68-1.62)55/791.64 (0.82-3.30)
        Ptrend§0.860.32
    • ↵* Number of controls/number of cases. The analysis of smoking intensity and duration gave rise to missing values for this variable in three male and one female subjects. These case-control pairs were excluded from the analysis.

    • ↵† OR and 95% CI are estimated by conditional logistic regression, matched on age and ethnicity, compared with never smokers, and adjusted for family history of colorectal cancer, body mass index 5 y ago (males only), lifetime hours in recreational activities (males only) and egg, total calcium, non-starch polysaccharides from vegetables, methionine (females only), and alcohol (males only) intake. All levels of the smoking characteristics are compared against never smokers. Separate models were run for intensity, duration, and time since smoking commenced.

    • ↵‡ Further adjusted for smoking status.

    • ↵§ Ptrend is estimated by fitting the medians of each category as a continuous variable in the multivariate model.

    • ↵∥ Further adjusted for smoking status and duration.

  • Table 3.

    Colorectal cancer risk by sex and quartiles of pack-years of all tobacco products and of filtered and non-filtered cigarettes

    Q1*
    Q2
    Q3
    Q4
    Ptrend†
    n‡OR (95% CI)nOR (95% CI)nOR (95% CI)nOR (95% CI)
    Males (1,109 case-control pairs)
        All tobacco185/1441.02 (0.76-1.36)186/1871.14 (0.86-1.51)186/2241.33 (1.00-1.76)189/2721.48 (1.12-1.96)0.002
        Filtered cigarettes132/1160.95 (0.68-1.32)139/1320.91 (0.67-1.26)134/1621.11 (0.81-1.51)138/1731.06 (0.79-1.42)0.63
        Non-filtered cigarettes135/1151.03 (0.75-1.42)135/1160.91 (0.65-1.28)136/1681.30 (0.96-1.78)125/2071.73 (1.27-2.34)0.0002
        Cigars38/461.30 (0.96-1.78)39/621.60 (1.00-2.58)0.04
        Pipes46/440.89 (0.55-1.44)34/500.99 (0.61-1.60)0.98
    Females (814 case-control pairs)
        All tobacco72/741.33 (0.91-1.95)73/570.81 (0.54-1.22)68/951.48 (1.03-2.13)73/991.38 (0.91-1.95)0.04
        Filtered cigarettes62/701.42 (0.95-2.12)61/450.69 (0.45-1.07)62/811.32 (0.88-1.97)61/851.17 (0.78-1.76)0.35
        Non-filtered cigarettes27/210.79 (0.43-1.49)26/321.06 (0.58-1.92)27/371.33 (0.74-2.42)25/552.23 (1.25-3.98)0.004
    • NOTE: OR and 95% CI are estimated by conditional logistic regression, matched on age and ethnicity, and adjusted for family history of colorectal cancer, body mass index 5 y ago (males only), lifetime hours in recreational activities (males only) and egg, total calcium, non-starch polysaccharides from vegetables, methionine (females only), and alcohol (males only) intake. Two separate models were run in each sex, both with never smokers as the reference category: one model included indicator variables for each quartile of pack-years of all tobacco products, and the other model included indicator variables for each quartile of pack-years for each type of cigarettes (filtered and non-filtered cigarettes), and in men, levels (<median; >median) of pack-years of cigars and pipes. In women, the latter model was further adjusted for pack-years of cigars and pipes (continuous).

    • ↵* Q1, 1st quartile; Q2, 2nd quartile; Q3, 3rd quartile; Q4, 4th quartile. Based on male controls who smoked, the quartile cut points (25th-75th percentile) for total pack-years and pack-years of filtered and non-filtered cigarettes are as follows: >0-12, >12-28.3, >28.3-48, and >48 for all tobacco; >0-10.4, >10.4-23, >23-40, and >40 for filtered cigarettes; and >0-4.8, >4.8-11, >11-24 and >24 for non-filtered cigarettes. Median cut points for pipes and cigars are 1.8 pack-years of cigars and 1.0 pack-years of pipes. Based on female controls who smoked, the quartile cut points (25th-75th percentile) for total pack-years and pack-years of filtered and non-filtered cigarettes are as follows: >0-5.3, >5.3-15, >15-34.7, and >34.7 for all tobacco; >0-7, >7-15.6, >15.6-30, and >30 for filtered cigarettes; and >0-1.4, >1.4-5, >5-11, and >11 for non-filtered cigarettes.

    • ↵† Ptrend is estimated by fitting the medians of each quartile as a continuous variable in the multivariate model.

    • ↵‡ Number of controls/number of cases (never smokers: 363/282 and 528/489 for men and women, respectively).

  • Table 4.

    Colorectal cancer risk by ethnicity and quartiles of pack-years of all tobacco products and of filtered and non-filtered cigarettes

    Q1*
    Q2
    Q3
    Q4
    Ptrend†
    n‡OR (95% CI)nOR (95% CI)nOR (95% CI)nOR (95% CI)
    Japanese (1,018 case-control pairs)
        All tobacco108/961.09 (0.78-1.51)141/1210.89 (0.65-1.21)128/1651.34 (0.99-1.82)135/1841.27 (0.94-1.74)0.06
        Filtered cigarettes95/991.22 (0.85-1.75)97/1111.09 (0.77-1.54)116/1351.12 (0.80-1.57)104/1120.95 (0.68-1.34)0.58
        Non-filtered cigarettes89/730.83 (0.57-1.21)77/750.97 (0.64-1.49)91/1021.15 (0.78-1.69)63/1231.96 (1.29-2.98)0.004
    Caucasian (485 case-control pairs)
        All tobacco76/631.17 (0.77-1.78)64/771.50 (0.97-2.31)70/721.47 (0.94-2.28)79/1231.92 (1.27-2.92)0.003
        Filtered cigarettes61/440.74 (0.46-1.21)56/550.95 (0.58-1.54)37/461.35 (0.79-2.31)54/861.53 (0.97-2.40)0.04
        Non-filtered cigarettes46/421.06 (0.64-1.77)48/401.01 (0.59-1.73)39/541.54 (0.92-2.58)63/881.42 (0.90-2.24)0.09
    Native Hawaiian (191 case-control pairs)
        All tobacco30/220.88 (0.40-1.90)32/321.08 (0.55-2.15)33/180.60 (0.28-1.26)24/511.99 (0.97-4.07)0.07
        Filtered cigarettes23/200.94 (0.41-2.14)33/230.62 (0.30-1.29)21/251.06 (0.48-2.33)26/321.01 (0.50-2.04)0.77
        Non-filtered cigarettes23/190.94 (0.40-2.18)17/150.91 (0.34-2.42)10/171.92 (0.61-6.11)13/242.33 (0.93-5.83)0.05
    • NOTE: OR and 95% CI are estimated by conditional logistic regression, matched on age and sex, and adjusted for family history of colorectal cancer, body mass index 5 y ago, lifetime hours in recreational activities as well as egg, total calcium, non-starch polysaccharides from vegetables, methionine, and alcohol intake. Two separate models were run in each ethnicity, both with never smokers as the reference category: one model included indicator variables for each quartile of pack-years of all tobacco products, and the other model included indicator variables for each quartile of pack-years for each type of cigarettes (filtered and non-filtered) and was further adjusted for pack-years of cigars and pipes (continuous).

    • ↵* Q1, 1st quartile; Q2, 2nd quartile; Q3, 3rd quartile; Q4, 4th quartile. Based on controls who smoked, the quartile cut points (25th-75th percentile) for total pack-years are as follows: >0-9.8, >9.8-24.6, >24.6-44, and >44; for pack-years of filtered cigarettes: >0-9.5, >9.5-21, >21-38, and >38; for pack-years of non-filtered cigarettes: >0-4, >4-10, >10-22, and >22.

    • ↵† Ptrend is estimated by fitting the medians of each quartile as a continuous variable in the multivariate model.

    • ↵‡ Number of controls/number of cases (never smokers: 506/452, 196/150 and 72/68 for Japanese, Caucasians, and Native Hawaiians, respectively).

  • Table 5.

    Colorectal cancer risk by anatomical subsite and quartiles of pack-years of all tobacco products and of filtered and non-filtered cigarettes

    Q1*
    Q2
    Q3
    Q4
    Ptrend†
    n‡OR (95% CI)nOR (95% CI)nOR (95% CI)nOR (95% CI)
    Colon (1,349 case-control pairs)
        All tobacco175/1541.14 (0.87-1.50)197/1710.92 (0.70-1.20)179/1991.18 (0.90-1.54)191/2781.39 (1.07-1.81)0.01
        Filtered cigarettes134/1391.20 (0.89-1.62)154/1370.87 (0.65-1.16)134/1571.08 (0.79-1.46)145/1721.05 (0.79-1.39)0.98
        Non-filtered cigarettes129/1080.90 (0.66-1.23)115/990.92 (0.65-1.31)109/1481.38 (1.00-1.92)111/1761.59 (1.15-2.21)0.001
    Rectum (573 case-control pairs)
        All tobacco76/641.13 (0.75-1.69)63/851.78 (1.18-2.70)86/921.41 (0.97-2.07)72/1212.12 (1.43-3.14)0.0003
        Filtered cigarettes62/470.71 (0.44-1.13)49/661.25 (0.80-1.96)66/781.14 (0.74-1.75)51/761.37 (0.88-2.13)0.06
        Non-filtered cigarettes42/501.55 (0.93-2.56)42/511.57 (0.93-2.65)42/461.37 (0.80-2.34)54/891.84 (1.18-2.86)0.02
    • NOTE: OR and 95% CI are estimated by conditional logistic regression, matched on age, sex and ethnicity, and adjusted for family history of colorectal cancer, body mass index 5 y ago, lifetime hours in recreational activities as well as egg, total calcium, non-starch polysaccharides from vegetables, methionine, and alcohol intake. Two separate models were run for each subsite, both with never smokers as the reference category: one model included indicator variables for each quartile of for pack-years of all tobacco products, and the other model included indicator variables for each quartile of pack-years for each type of cigarettes (filtered and non-filtered) and was further adjusted for pack-years of cigars and pipes (continuous).

    • ↵* Q1, 1st quartile; Q2, 2nd quartile; Q3, 3rd quartile; Q4, 4th quartile. Based on controls who smoked, the quartile cut points (25th-75th percentile) for total pack-years are as follows: >0-9.8, >9.8-24.6, >24.6-44, and >44; for pack-years of filtered cigarettes: >0-9.5, >9.5-21, >21-38, and >38; for pack-years of non-filtered cigarettes: >0-4, >4-10, >10-22, and >22.

    • ↵† Ptrend is estimated by fitting the medians of each quartile as a continuous variable in the multivariate model.

    • ↵‡ Number of controls/number of cases (never smokers: 607/547 and 276/211 for males and females, respectively).

  • Table 6.

    Colon and rectal cancer risk by time period before diagnosis for cases and interview for controls

    Pack-years, cumulative up toOR* (95% CI)
    All tobacco productsFiltered cigarettesNon-filtered cigarettes
    Colon (1,349 case-control pairs)
        0 y ago1.05 (1.01-1.08)1.00 (0.97-1.05)1.12 (1.05-1.19)
        5 y ago1.05 (1.01-1.09)1.01 (0.96-1.06)1.11 (1.04-1.19)
        10 y ago1.06 (1.01-1.10)1.01 (0.95-1.08)1.11 (1.04-1.19)
        20 y ago1.05 (1.00-1.11)0.98 (0.90-1.07)1.11 (1.03-1.20)
        30 y ago1.04 (0.96-1.13)0.90 (0.79-1.03)1.09 (0.99-1.20)
        40 y ago1.03 (0.91-1.17)0.75 (0.57-0.98)1.04 (0.90-1.19)
        50 y ago1.08 (0.84-1.38)0.84 (0.40-1.74)0.98 (0.76-1.27)
    Rectum (573 case-control pairs)
        0 y ago1.10 (1.05-1.16)1.10 (1.03-1.17)1.11 (1.03-1.19)
        5 y ago1.10 (1.03-1.16)1.09 (1.00-1.19)1.09 (1.00-1.18)
        10 y ago1.10 (1.03-1.17)1.11 (0.78-1.59)1.07 (0.99-1.17)
        20 y ago1.09 (1.00-1.18)1.08 (0.93-1.24)1.08 (0.98-1.20)
        30 y ago1.05 (0.94-1.17)0.96 (0.76-1.20)1.07 (0.94-1.21)
        40 y ago1.00 (0.85-1.18)0.86 (0.56-1.32)1.01 (0.84-1.21)
        50 y ago1.05 (0.76-1.43)0.85 (0.23-3.15)1.05 (0.75-1.47)
    • ↵* OR and 95% CI are estimated using conditional logistic regression and represent the risk associated with an increment of 10 pack-years in the specified time period, and are adjusted for pack-years accumulated from that time to diagnosis or interview, as well as for family history of colorectal cancer, body mass index 5 y ago, lifetime hours in recreational activities and egg, total calcium, non-starch polysaccharides from vegetables, methionine and alcohol intake, and matched on age, sex, and ethnicity. Fourteen separate models were run for each subsite (seven for pack-years of all tobacco products and seven for pack-years of filtered and non-filtered cigarettes), which were modeled together.

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Cancer Epidemiology Biomarkers & Prevention: 16 (7)
July 2007
Volume 16, Issue 7
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Smoking and Colorectal Cancer: Different Effects by Type of Cigarettes?
Margreet Lüchtenborg, Kami K.L. White, Lynne Wilkens, Laurence N. Kolonel and Loïc Le Marchand
Cancer Epidemiol Biomarkers Prev July 1 2007 (16) (7) 1341-1347; DOI: 10.1158/1055-9965.EPI-06-0519

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Smoking and Colorectal Cancer: Different Effects by Type of Cigarettes?
Margreet Lüchtenborg, Kami K.L. White, Lynne Wilkens, Laurence N. Kolonel and Loïc Le Marchand
Cancer Epidemiol Biomarkers Prev July 1 2007 (16) (7) 1341-1347; DOI: 10.1158/1055-9965.EPI-06-0519
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eISSN: 1538-7755
ISSN: 1055-9965

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