Lifetime and baseline alcohol intake and risk of colon and rectal cancers in the European prospective investigation into cancer and nutrition (EPIC)
Corresponding Author
Pietro Ferrari
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Fax: +33-472-73-83-61.
IARC-WHO, 150 cours Albert-Thomas, 69372 Lyon Cedex 08, FranceSearch for more papers by this authorMazda Jenab
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorTeresa Norat
Department of Epidemiology and Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorAurelie Moskal
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorNadia Slimani
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorAnja Olsen
Institute of Cancer Epidemiology, The Danish Cancer Society, Copenhagen, Denmark
Search for more papers by this authorAnne Tjønneland
Institute of Cancer Epidemiology, The Danish Cancer Society, Copenhagen, Denmark
Search for more papers by this authorKim Overvad
Department of Clinical Epidemiology, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark
Search for more papers by this authorMajken K. Jensen
Department of Clinical Epidemiology, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark
Search for more papers by this authorMarie-Christine Boutron-Ruault
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorFrançoise Clavel-Chapelon
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorSophie Morois
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorSabine Rohrmann
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorJakob Linseisen
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorHeiner Boeing
Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany
Search for more papers by this authorManuela Bergmann
Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany
Search for more papers by this authorDimitra Kontopoulou
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorAntonia Trichopoulou
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorChristina Kassapa
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorGiovanna Masala
Molecular and Nutritional Epidemiology Unit, CSPO-Scientific Institute of Tuscany, Florence, Italy
Search for more papers by this authorVittorio Krogh
Nutritional Epidemiology Unit, National Cancer Institute, Milan, Italy
Search for more papers by this authorPaolo Vineis
Department of Epidemiology and Public Health, Imperial College, London, United Kingdom
Department of Biomedical Sciences and Human Oncology, University of Torino, Italy
Search for more papers by this authorSalvatore Panico
Department of Clinical and Experimental Medicine, Federico II University, Naples, Italy
Search for more papers by this authorRosario Tumino
Cancer Registry, Azienda Ospedaliera “Civile M.P. Arezzo,” Ragusa, Italy
Search for more papers by this authorCarla H. van Gils
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, The Netherlands
Search for more papers by this authorPetra Peeters
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, The Netherlands
Search for more papers by this authorH. Bas Bueno-de-Mesquita
Cancer Epidemiology, Centre for Nutrition and Health, National Institute of Public Health and the Environment, Bilthoven, The Netherlands
Search for more papers by this authorMarga C. Ocké
Cancer Epidemiology, Centre for Nutrition and Health, National Institute of Public Health and the Environment, Bilthoven, The Netherlands
Search for more papers by this authorGuri Skeie
Institute of Community Medicine, University of Tromsø, Tromsø, Norway
Search for more papers by this authorEiliv Lund
Institute of Community Medicine, University of Tromsø, Tromsø, Norway
Search for more papers by this authorAntonio Agudo
Group of Nutrition, Environmental and Cancer, Department of Epidemiology and Cancer Registry, Catalan Institute of Oncology, Barcelona, Spain
Search for more papers by this authorEva Ardanaz
Public Health Institute of Navarra, Pamplona, Spain
Search for more papers by this authorDolores C. López
Epidemiology Department, Murcia Health Council, Murcia, Spain
Search for more papers by this authorMaria-Jose Sanchez
Andalusian School of Public Health, Granada, Spain
Search for more papers by this authorJosé R. Quirós
Public Health and Health Planning Directorate, Asturias, Spain
Search for more papers by this authorPilar Amiano
Public Health Division of Gipuzkoa, Health Department of the Basque Country, Donostia-San Sebastian, Spain
Search for more papers by this authorGöran Berglund
Institutionen för Kliniska Vetenskaper, Kirurgiska Kliniken, Universitetssjukhuset MAS, Malmö, Sweden
Search for more papers by this authorJonas Manjer
Institutionen för Kliniska Vetenskaper, Kirurgiska Kliniken, Universitetssjukhuset MAS, Malmö, Sweden
Search for more papers by this authorRichard Palmqvist
Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden
Search for more papers by this authorBethany Van Guelpen
Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden
Search for more papers by this authorNaomi Allen
Cancer Research UK Epidemiology Unit, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorTim Key
Cancer Research UK Epidemiology Unit, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorSheila Bingham
MRC Centre for Nutritional Epidemiology in Cancer Prevention and Survival, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorMathieu Mazuir
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorPaolo Boffetta
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorRudolf Kaaks
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorElio Riboli
Department of Epidemiology and Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorCorresponding Author
Pietro Ferrari
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Fax: +33-472-73-83-61.
IARC-WHO, 150 cours Albert-Thomas, 69372 Lyon Cedex 08, FranceSearch for more papers by this authorMazda Jenab
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorTeresa Norat
Department of Epidemiology and Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorAurelie Moskal
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorNadia Slimani
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorAnja Olsen
Institute of Cancer Epidemiology, The Danish Cancer Society, Copenhagen, Denmark
Search for more papers by this authorAnne Tjønneland
Institute of Cancer Epidemiology, The Danish Cancer Society, Copenhagen, Denmark
Search for more papers by this authorKim Overvad
Department of Clinical Epidemiology, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark
Search for more papers by this authorMajken K. Jensen
Department of Clinical Epidemiology, Aalborg Hospital, Aarhus University Hospital, Aalborg, Denmark
Search for more papers by this authorMarie-Christine Boutron-Ruault
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorFrançoise Clavel-Chapelon
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorSophie Morois
Nutrition, Hormones and Cancer Unit, E3N, EMT, Institut Gustave Roussy, Villejuif Cedex, France
Search for more papers by this authorSabine Rohrmann
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorJakob Linseisen
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorHeiner Boeing
Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany
Search for more papers by this authorManuela Bergmann
Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany
Search for more papers by this authorDimitra Kontopoulou
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorAntonia Trichopoulou
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorChristina Kassapa
Department of Hygiene and Epidemiology, Medical School, University of Athens, Greece
Search for more papers by this authorGiovanna Masala
Molecular and Nutritional Epidemiology Unit, CSPO-Scientific Institute of Tuscany, Florence, Italy
Search for more papers by this authorVittorio Krogh
Nutritional Epidemiology Unit, National Cancer Institute, Milan, Italy
Search for more papers by this authorPaolo Vineis
Department of Epidemiology and Public Health, Imperial College, London, United Kingdom
Department of Biomedical Sciences and Human Oncology, University of Torino, Italy
Search for more papers by this authorSalvatore Panico
Department of Clinical and Experimental Medicine, Federico II University, Naples, Italy
Search for more papers by this authorRosario Tumino
Cancer Registry, Azienda Ospedaliera “Civile M.P. Arezzo,” Ragusa, Italy
Search for more papers by this authorCarla H. van Gils
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, The Netherlands
Search for more papers by this authorPetra Peeters
Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, The Netherlands
Search for more papers by this authorH. Bas Bueno-de-Mesquita
Cancer Epidemiology, Centre for Nutrition and Health, National Institute of Public Health and the Environment, Bilthoven, The Netherlands
Search for more papers by this authorMarga C. Ocké
Cancer Epidemiology, Centre for Nutrition and Health, National Institute of Public Health and the Environment, Bilthoven, The Netherlands
Search for more papers by this authorGuri Skeie
Institute of Community Medicine, University of Tromsø, Tromsø, Norway
Search for more papers by this authorEiliv Lund
Institute of Community Medicine, University of Tromsø, Tromsø, Norway
Search for more papers by this authorAntonio Agudo
Group of Nutrition, Environmental and Cancer, Department of Epidemiology and Cancer Registry, Catalan Institute of Oncology, Barcelona, Spain
Search for more papers by this authorEva Ardanaz
Public Health Institute of Navarra, Pamplona, Spain
Search for more papers by this authorDolores C. López
Epidemiology Department, Murcia Health Council, Murcia, Spain
Search for more papers by this authorMaria-Jose Sanchez
Andalusian School of Public Health, Granada, Spain
Search for more papers by this authorJosé R. Quirós
Public Health and Health Planning Directorate, Asturias, Spain
Search for more papers by this authorPilar Amiano
Public Health Division of Gipuzkoa, Health Department of the Basque Country, Donostia-San Sebastian, Spain
Search for more papers by this authorGöran Berglund
Institutionen för Kliniska Vetenskaper, Kirurgiska Kliniken, Universitetssjukhuset MAS, Malmö, Sweden
Search for more papers by this authorJonas Manjer
Institutionen för Kliniska Vetenskaper, Kirurgiska Kliniken, Universitetssjukhuset MAS, Malmö, Sweden
Search for more papers by this authorRichard Palmqvist
Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden
Search for more papers by this authorBethany Van Guelpen
Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden
Search for more papers by this authorNaomi Allen
Cancer Research UK Epidemiology Unit, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorTim Key
Cancer Research UK Epidemiology Unit, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorSheila Bingham
MRC Centre for Nutritional Epidemiology in Cancer Prevention and Survival, Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorMathieu Mazuir
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorPaolo Boffetta
International Agency for Research on Cancer (IARC-WHO), Lyon, France
Search for more papers by this authorRudolf Kaaks
Deutsches Krebsforschungszentrum/German Cancer Research Centre, Klinische Epidemiologie/Clinical Epidemiology, C020, AG Ernährungsepidemiologie/Nutritional Epidemiology, Heidelberg, Germany
Search for more papers by this authorElio Riboli
Department of Epidemiology and Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorAbstract
Alcohol consumption may be associated with risk of colorectal cancer (CRC), but the epidemiological evidence for an association with specific anatomical subsites, types of alcoholic beverages and current vs. lifetime alcohol intake is inconsistent. Within the European Prospective Investigation into Cancer and Nutrition (EPIC), 478,732 study subjects free of cancer at enrolment between 1992 and 2000 were followed up for an average of 6.2 years, during which 1,833 CRC cases were observed. Detailed information on consumption of alcoholic beverages at baseline (all cases) and during lifetime (1,447 CRC cases, 69% of the cohort) was collected from questionnaires. Cox proportional hazard models were used to examine the alcohol-CRC association. After adjustment for potential confounding factors, lifetime alcohol intake was significantly positively associated to CRC risk (hazard ratio, HR = 1.08, 95%CI = 1.04–1.12 for 15 g/day increase), with higher cancer risks observed in the rectum (HR = 1.12, 95%CI = 1.06–1.18) than distal colon (HR = 1.08, 95%CI = 1.01–1.16), and proximal colon (HR = 1.02, 95%CI = 0.92–1.12). Similar results were observed for baseline alcohol intake. When assessed by alcoholic beverages at baseline, the CRC risk for beer (HR = 1.38, 95%CI = 1.08–1.77 for 20–39.9 vs. 0.1–2.9 g/day) was higher than wine (HR = 1.21, 95%CI = 1.02–1.44), although the two risk estimates were not significantly different from each other. Higher HRs for baseline alcohol were observed for low levels of folate intake (1.13, 95%CI = 1.06–1.20 for 15 g/day increase) compared to high folate intake (1.03, 95%CI = 0.98–1.09). In this large European cohort, both lifetime and baseline alcohol consumption increase colon and rectum cancer risk, with more apparent risk increases for alcohol intakes greater than 30 g/day. © 2007 Wiley-Liss, Inc.
References
- 1 Parkin DM,Bray F,Ferlay J,Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74–108.
- 2 Doll R,Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981; 66: 1191–308.
- 3 Platz EA,Willett WC,Colditz GA,Rimm EB,Spiegelman D,Giovannucci E. Proportion of colon cancer risk that might be preventable in a cohort of middle-aged US men. Cancer Causes Control 2000; 11: 579–88.
- 4 Breslow NE,Enstrom JE. Geographic correlations between cancer mortality rates and alcohol-tobacco consumption in the United States. J Natl Cancer Inst 1974; 53: 631–9.
- 5 Enstrom JE. Colorectal cancer and beer drinking. Br J Cancer 1977; 35: 674–83.
- 6 Potter JD,McMichael AJ,Hartshorne JM. Alcohol and beer consumption in relation to cancers of bowel and lung: an extended correlation analysis. J Chronic Dis 1982; 35: 833–42.
- 7 Kabat GC,Howson CP,Wynder EL. Beer consumption and rectal cancer. Int J Epidemiol 1986; 15: 494–501.
- 8 Freudenheim JL,Graham S,Marshall JR,Haughey BP,Wilkinson G. Lifetime alcohol intake and risk of rectal cancer in western New York. Nutr Cancer 1990; 13: 101–9.
- 9 Longnecker MP,Orza MJ,Adams ME,Vioque J,Chalmers TC. A meta-analysis of alcoholic beverage consumption in relation to risk of colorectal cancer. Cancer Causes Control 1990; 1: 59–68.
- 10 Riboli E,Cornee J,Macquart-Moulin G,Kaaks R,Casagrande C,Guyader M. Cancer and polyps of the colorectum and lifetime consumption of beer and other alcoholic beverages. Am J Epidemiol 1991; 134: 157–66.
- 11 Peters RK,Pike MC,Garabrant D,Mack TM. Diet and colon cancer in Los Angeles County, California. Cancer Causes Control 1992; 3: 457–73.
- 12 Shimizu N,Nagata C,Shimizu H,Kametani M,Takeyama N,Ohnuma T,Matsushita S. Height, weight, and alcohol consumption in relation to the risk of colorectal cancer in Japan: a prospective study. Br J Cancer 2003; 88: 1038–43.
- 13 Su LJ,Arab L. Alcohol consumption and risk of colon cancer: evidence from the national health and nutrition examination survey I epidemiologic follow-up study. Nutr Cancer 2004; 50: 111–19.
- 14 Singh PN,Fraser GE. Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 1998; 148: 761–74.
- 15 Otani T,Iwasaki M,Yamamoto S,Sobue T,Hanaoka T,Inoue M,Tsugane S. 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 2003; 12: 1492–500.
- 16 Chyou PH,Nomura AM,Stemmermann GN. A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 1996; 6: 276–82.
- 17 Murata M,Takayama K,Choi BC,Pak AW. A nested case–control study on alcohol drinking, tobacco smoking, and cancer. Cancer Detect Prev 1996; 20: 557–65.
- 18 Wei EK,Giovannucci E,Wu K,Rosner B,Fuchs CS,Willett WC,Colditz GA. Comparison of risk factors for colon and rectal cancer. Int J Cancer 2004; 108: 433–42.
- 19 Moskal A,Norat T,Ferrari P,Riboli E. Alcohol intake and colorectal cancer risk: a dose–response meta-analysis of published cohort studies. Int J Cancer 2007; 120: 664–71.
- 20 Corrao G,Bagnardi V,Zambon A,La Vecchia C. A meta-analysis of alcohol consumption and the risk of 15 diseases. Prev Med 2004; 38: 613–19.
- 21 Boffetta P,Hashibe M. Alcohol and cancer. Lancet Oncol 2006; 7: 149–56.
- 22 Pedersen A,Johansen C,Gronbaek M. Relations between amount and type of alcohol and colon and rectal cancer in a Danish population based cohort study. Gut 2003; 52: 861–7.
- 23 Klatsky AL,Armstrong MA,Friedman GD,Hiatt RA. The relations of alcoholic beverage use to colon and rectal cancer. Am J Epidemiol 1988; 128: 1007–15.
- 24 Stemmermann GN,Nomura AM,Chyou PH,Yoshizawa C. Prospective study of alcohol intake and large bowel cancer. Dig Dis Sci 1990; 35: 1414–20.
- 25 Newcomb PA,Storer BE,Marcus PM. Cancer of the large bowel in women in relation to alcohol consumption: a case–control study in Wisconsin (United States). Cancer Causes Control 1993; 4: 405–11.
- 26 Miller AB,Howe GR,Jain M,Craib KJ,Harrison L. Food items and food groups as risk factors in a case–control study of diet and colo-rectal cancer. Int J Cancer 1983; 32: 155–61.
- 27 Cho E,Smith-Warner SA,Ritz J,van den Brandt PA,Colditz GA,Folsom AR,Freudenheim JL,Giovannucci E,Goldbohm RA,Graham S,Holmberg L,Kim DH et al. Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann Intern Med 2004; 140: 603–13.
- 28 Williams RR,Horm JW. Association of cancer sites with tobacco and alcohol consumption and socioeconomic status of patients: interview study from the Third National Cancer Survey. J Natl Cancer Inst 1977; 58: 525–47.
- 29 Meyer F,White E. Alcohol and nutrients in relation to colon cancer in middle-aged adults. Am J Epidemiol 1993; 138: 225–36.
- 30 Giovannucci E,Rimm EB,Ascherio A,Stampfer MJ,Colditz GA,Willett WC. Alcohol, low-methionine–low-folate diets, and risk of colon cancer in men. J Natl Cancer Inst 1995; 87: 265–73.
- 31 Riboli E,Hunt KJ,Slimani N,Ferrari P,Norat T,Fahey M,Charrondiere UR,Hemon B,Casagrande C,Vignat J,Overvad K,Tjonneland A, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 2002; 5: 1113–24.
- 32 Kaaks R,Slimani N,Riboli E. Pilot phase studies on the accuracy of dietary intake measurements in the EPIC project: overall evaluation of results. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol 1997; 26 ( Suppl 1): S26–S36.
- 33 Slimani N,Ferrari P,Ocke M,Welch A,Boeing H,Liere M,Pala V,Amiano P,Lagiou A,Mattisson I,Stripp C,Engeset D, et al. Standardization of the 24-hour diet recall calibration method used in the European prospective investigation into cancer and nutrition (EPIC): general concepts and preliminary results. Eur J Clin Nutr 2000; 54: 900–17.
- 34 Sieri S,Agudo A,Kesse E,Klipstein-Grobusch K,San Jose B,Welch AA,Krogh V,Luben R,Allen N,Overvad K,Tjonneland A,Clavel-Chapelon F, et al. Patterns of alcohol consumption in 10 European countries participating in the European Prospective Investigation into Cancer and Nutrition (EPIC) project. Public Health Nutr 2002; 5: 1287–96.
- 35 Klipstein-Grobusch K,Slimani N,Krogh V,Keil U,Boeing H,Overvad K,Tjonneland A,Clavel-Chapelon F,Thiebaut A,Linseisen J,Schulze MB,Lagiou P, et al. Trends in self-reported past alcoholic beverage consumption and ethanol intake from 1950 to 1995 observed in eight European countries participating in the European Investigation into Cancer and Nutrition (EPIC). Public Health Nutr 2002; 5: 1297–310.
- 36
Cox DR.
Regression models and life tables.
J R Stat Soc Ser B
1972;
34:
187–220.
10.1111/j.2517-6161.1972.tb00899.x Google Scholar
- 37 Day N,McKeown N,Wong M,Welch A,Bingham S. Epidemiological assessment of diet: a comparison of a 7-day diary with a food frequency questionnaire using urinary markers of nitrogen, potassium and sodium. Int J Epidemiol 2001; 30: 309–17.
- 38 Thurston SW,Liu G,Miller DP,Christiani DC. Modeling lung cancer risk in case–control studies using a new dose metric of smoking. Cancer Epidemiol Biomarkers Prev 2005; 14: 2296–302.
- 39 Durrleman S,Simon R. Flexible regression models with cubic splines. Stat Med 1989; 8: 551–61.
- 40 Greenland S,Longnecker MP. Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol 1992; 135: 1301–9.
- 41 SAS Institute. SAS Online Doc®, Version 8. Cary, NC: SAS Institute Inc., 1999.
- 42 Ferlay J,Bray F,Sankila R,Parkin DM. EUCAN: cancer incidence, mortality and prevalence in the European Union 1997 (IARC CancerBase no. 4, version 4.1). Lyon: IARC, 1999.
- 43 International Agency for Research on Cancer. Monographs on the evaluation of carcinogenic risks to humans: alcohol drinking, vol. 44. Lyon: IARC, 1988.
- 44 Seitz HK,Poschl G,Simanowski UA. Alcohol and cancer. Recent Dev Alcohol 1998; 14: 67–95.
- 45 Lieber CS. Mechanisms of ethanol–drug–nutrition interactions. J Toxicol Clin Toxicol 1994; 32: 631–81.
- 46 Seitz HK,Simanowski UA. Alcohol and carcinogenesis. Annu Rev Nutr 1988; 8: 99–119.
- 47 Kune GA,Vitetta L. Alcohol consumption and the etiology of colorectal cancer: a review of the scientific evidence from 1957 to 1991. Nutr Cancer 1992; 18: 97–111.
- 48 Hirayama T. Association between alcohol consumption and cancer of the sigmoid colon: observations from a Japanese cohort study. Lancet 1989; 2: 725–7.
- 49 Glynn SA,Albanes D,Pietinen P,Brown CC,Rautalahti M,Tangrea JA,Taylor PR,Virtamo J. Alcohol consumption and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 1996; 7: 214–23.
- 50 Seitz HK,Czygan P,Waldherr R,Veith S,Kommerell B. Ethanol and intestinal carcinogenesis in the rat. Alcohol 1985; 2: 491–4.
- 51 McGarrity TJ,Peiffer LP,Colony PC,Pegg AE. The effects of chronic ethanol administration on polyamine content during dimethylhydrazine-induced colorectal carcinogenesis in the rat. Carcinogenesis 1988; 9: 2093–8.
- 52 Rampersaud GC,Kauwell GP,Hutson AD,Cerda JJ,Bailey LB. Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 2000; 72: 998–1003.
- 53 Folate, alcohol, methionine, and colon cancer risk: is there a unifying theme? Nutr Rev 1994; 52: 18–20.
- 54 Laird PW,Jaenisch R. DNA methylation and cancer. Hum Mol Genet 1994; 3: 1487–95.
- 55 Freudenheim JL,Graham S,Marshall JR,Haughey BP,Cholewinski S,Wilkinson G. Folate intake and carcinogenesis of the colon and rectum. Int J Epidemiol 1991; 20: 368–74.
Citing Literature
