Skip to main content
Top
Published in: BMC Medicine 1/2014

Open Access 01-12-2014 | Research article

Combined impact of healthy lifestyle factors on colorectal cancer: a large European cohort study

Authors: Krasimira Aleksandrova, Tobias Pischon, Mazda Jenab, H Bas Bueno-de-Mesquita, Veronika Fedirko, Teresa Norat, Dora Romaguera, Sven Knüppel, Marie-Christine Boutron-Ruault, Laure Dossus, Laureen Dartois, Rudolf Kaaks, Kuanrong Li, Anne Tjønneland, Kim Overvad, José Ramón Quirós, Genevieve Buckland, María José Sánchez, Miren Dorronsoro, Maria-Dolores Chirlaque, Aurelio Barricarte, Kay-Tee Khaw, Nicholas J Wareham, Kathryn E Bradbury, Antonia Trichopoulou, Pagona Lagiou, Dimitrios Trichopoulos, Domenico Palli, Vittorio Krogh, Rosario Tumino, Alessio Naccarati, Salvatore Panico, Peter D Siersema, Petra HM Peeters, Ingrid Ljuslinder, Ingegerd Johansson, Ulrika Ericson, Bodil Ohlsson, Elisabete Weiderpass, Guri Skeie, Kristin Benjaminsen Borch, Sabina Rinaldi, Isabelle Romieu, Joyce Kong, Marc J Gunter, Heather A Ward, Elio Riboli, Heiner Boeing

Published in: BMC Medicine | Issue 1/2014

Login to get access

Abstract

Background

Excess body weight, physical activity, smoking, alcohol consumption and certain dietary factors are individually related to colorectal cancer (CRC) risk; however, little is known about their joint effects. The aim of this study was to develop a healthy lifestyle index (HLI) composed of five potentially modifiable lifestyle factors - healthy weight, physical activity, non-smoking, limited alcohol consumption and a healthy diet, and to explore the association of this index with CRC incidence using data collected within the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort.

Methods

In the EPIC cohort, a total of 347,237 men and women, 25- to 70-years old, provided dietary and lifestyle information at study baseline (1992 to 2000). Over a median follow-up time of 12 years, 3,759 incident CRC cases were identified. The association between a HLI and CRC risk was evaluated using Cox proportional hazards regression models and population attributable risks (PARs) have been calculated.

Results

After accounting for study centre, age, sex and education, compared with 0 or 1 healthy lifestyle factors, the hazard ratio (HR) for CRC was 0.87 (95% confidence interval (CI): 0.44 to 0.77) for two factors, 0.79 (95% CI: 0.70 to 0.89) for three factors, 0.66 (95% CI: 0.58 to 0.75) for four factors and 0.63 (95% CI: 0.54 to 0.74) for five factors; P-trend <0.0001. The associations were present for both colon and rectal cancers, HRs, 0.61 (95% CI: 0.50 to 0.74; P for trend <0.0001) for colon cancer and 0.68 (95% CI: 0.53 to 0.88; P-trend <0.0001) for rectal cancer, respectively (P-difference by cancer sub-site = 0.10). Overall, 16% of the new CRC cases (22% in men and 11% in women) were attributable to not adhering to a combination of all five healthy lifestyle behaviours included in the index.

Conclusions

Combined lifestyle factors are associated with a lower incidence of CRC in European populations characterized by western lifestyles. Prevention strategies considering complex targeting of multiple lifestyle factors may provide practical means for improved CRC prevention.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ferlay JS, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F: Cancer incidence and mortality worldwide: IARC CancerBase. GLOBOCAN 2012 v10. 2013, International Agency for Research on Cancer, Lyon, France Ferlay JS, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F: Cancer incidence and mortality worldwide: IARC CancerBase. GLOBOCAN 2012 v10. 2013, International Agency for Research on Cancer, Lyon, France
2.
go back to reference Bingham S: The fibre-folate debate in colo-rectal cancer. Proc Nutr Soc. 2006, 65: 19-23. 10.1079/PNS2005472.CrossRefPubMed Bingham S: The fibre-folate debate in colo-rectal cancer. Proc Nutr Soc. 2006, 65: 19-23. 10.1079/PNS2005472.CrossRefPubMed
3.
go back to reference Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjønneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E: Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003, 361: 1496-1501. 10.1016/S0140-6736(03)13174-1.CrossRefPubMed Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjønneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E: Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet. 2003, 361: 1496-1501. 10.1016/S0140-6736(03)13174-1.CrossRefPubMed
4.
go back to reference Ferrari P, Jenab M, Norat T, Moskal A, Slimani N, Olsen A, Tjonneland A, Overvad K, Jensen MK, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Rohrmann S, Linseisen J, Boeing H, Bergmann M, Kontopoulou D, Trichopoulou A, Kassapa C, Masala G, Krogh V, Vineis P, Panico S, Tumino R, van Gils CH, Peeters P, Bueno-de-Mesquita HB, Ocké MC, Skeie G, Lund E, et al: Lifetime and baseline alcohol intake and risk of colon and rectal cancers in the European prospective investigation into cancer and nutrition (EPIC). Int J Cancer. 2007, 121: 2065-2072. 10.1002/ijc.22966.CrossRefPubMed Ferrari P, Jenab M, Norat T, Moskal A, Slimani N, Olsen A, Tjonneland A, Overvad K, Jensen MK, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Rohrmann S, Linseisen J, Boeing H, Bergmann M, Kontopoulou D, Trichopoulou A, Kassapa C, Masala G, Krogh V, Vineis P, Panico S, Tumino R, van Gils CH, Peeters P, Bueno-de-Mesquita HB, Ocké MC, Skeie G, Lund E, et al: Lifetime and baseline alcohol intake and risk of colon and rectal cancers in the European prospective investigation into cancer and nutrition (EPIC). Int J Cancer. 2007, 121: 2065-2072. 10.1002/ijc.22966.CrossRefPubMed
5.
go back to reference Jenab M, Ferrari P, Slimani N, Norat T, Casagrande C, Overad K, Olsen A, Stripp C, Tjonneland A, Boutron-Ruault MC, Clavel-Chapelon F, Kesse E, Nieters A, Bergmann M, Boeing H, Naska A, Trichopoulou A, Palli D, Krogh V, Celentano E, Tumino R, Sacerdote C, Bueno-de-Mesquita HB, Ocké MC, Peeters PH, Engeset D, Quirós JR, González CA, Martínez C, Chirlaque MD, et al: Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomarkers Prev. 2004, 13: 1595-1603.PubMed Jenab M, Ferrari P, Slimani N, Norat T, Casagrande C, Overad K, Olsen A, Stripp C, Tjonneland A, Boutron-Ruault MC, Clavel-Chapelon F, Kesse E, Nieters A, Bergmann M, Boeing H, Naska A, Trichopoulou A, Palli D, Krogh V, Celentano E, Tumino R, Sacerdote C, Bueno-de-Mesquita HB, Ocké MC, Peeters PH, Engeset D, Quirós JR, González CA, Martínez C, Chirlaque MD, et al: Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomarkers Prev. 2004, 13: 1595-1603.PubMed
6.
go back to reference Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjonneland A, Clavel F, Boutron-Ruault MC, Kesse E, Boeing H, Bergmann MM, Nieters A, Linseisen J, Trichopoulou A, Trichopoulos D, Tountas Y, Berrino F, Palli D, Panico S, Tumino R, Vineis P, Bueno-de-Mesquita HB, Peeters PH, Engeset D, Lund E, Skeie G, Ardanaz E, et al: Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst. 2005, 97: 906-916. 10.1093/jnci/dji164.CrossRefPubMedPubMedCentral Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjonneland A, Clavel F, Boutron-Ruault MC, Kesse E, Boeing H, Bergmann MM, Nieters A, Linseisen J, Trichopoulou A, Trichopoulos D, Tountas Y, Berrino F, Palli D, Panico S, Tumino R, Vineis P, Bueno-de-Mesquita HB, Peeters PH, Engeset D, Lund E, Skeie G, Ardanaz E, et al: Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J Natl Cancer Inst. 2005, 97: 906-916. 10.1093/jnci/dji164.CrossRefPubMedPubMedCentral
7.
go back to reference Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, Tjonneland A, Halkjaer J, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Guernec G, Bergmann MM, Linseisen J, Becker N, Trichopoulou A, Trichopoulos D, Sieri S, Palli D, Tumino R, Vineis P, Panico S, Peeters PH, Bueno-de-Mesquita HB, Boshuizen HC, Van Guelpen B, Palmqvist R, Berglund G, Gonzalez CA, Dorronsoro M, Barricarte A, et al: Body size and risk of colon and rectal cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst. 2006, 98: 920-931. 10.1093/jnci/djj246.CrossRefPubMed Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, Tjonneland A, Halkjaer J, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Guernec G, Bergmann MM, Linseisen J, Becker N, Trichopoulou A, Trichopoulos D, Sieri S, Palli D, Tumino R, Vineis P, Panico S, Peeters PH, Bueno-de-Mesquita HB, Boshuizen HC, Van Guelpen B, Palmqvist R, Berglund G, Gonzalez CA, Dorronsoro M, Barricarte A, et al: Body size and risk of colon and rectal cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst. 2006, 98: 920-931. 10.1093/jnci/djj246.CrossRefPubMed
8.
go back to reference van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P, Jenab M, Boshuizen HC, Ros MM, Casagrande C, Tjonneland A, Olsen A, Overvad K, Thorlacius-Ussing O, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Kaaks R, Linseisen J, Boeing H, Nöthlings U, Trichopoulou A, Trichopoulos D, Misirli G, Palli D, Sieri S, Panico S, Tumino R, Vineis P, Peeters PH, van Gils CH, Ocké MC, Lund E, et al: Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2009, 89: 1441-1452. 10.3945/ajcn.2008.27120.CrossRefPubMed van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P, Jenab M, Boshuizen HC, Ros MM, Casagrande C, Tjonneland A, Olsen A, Overvad K, Thorlacius-Ussing O, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Kaaks R, Linseisen J, Boeing H, Nöthlings U, Trichopoulou A, Trichopoulos D, Misirli G, Palli D, Sieri S, Panico S, Tumino R, Vineis P, Peeters PH, van Gils CH, Ocké MC, Lund E, et al: Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2009, 89: 1441-1452. 10.3945/ajcn.2008.27120.CrossRefPubMed
9.
go back to reference Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, Dahm CC, Overvad K, Olsen A, Tjonneland A, Clavel-Chapelon F, Boutron-Ruault MC, Racine A, Kaaks R, Teucher B, Boeing H, Bergmann MM, Trichopoulou A, Trichopoulos D, Lagiou P, Palli D, Pala V, Panico S, Tumino R, Vineis P, Siersema P, van Duijnhoven F, Peeters PH, Hjartaker A, Engeset D, et al: Dietary fibre intake and risks of cancers of the colon and rectum in the European prospective investigation into cancer and nutrition (EPIC). PLoS One. 2012, 7: e39361-10.1371/journal.pone.0039361.CrossRefPubMedPubMedCentral Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, Dahm CC, Overvad K, Olsen A, Tjonneland A, Clavel-Chapelon F, Boutron-Ruault MC, Racine A, Kaaks R, Teucher B, Boeing H, Bergmann MM, Trichopoulou A, Trichopoulos D, Lagiou P, Palli D, Pala V, Panico S, Tumino R, Vineis P, Siersema P, van Duijnhoven F, Peeters PH, Hjartaker A, Engeset D, et al: Dietary fibre intake and risks of cancers of the colon and rectum in the European prospective investigation into cancer and nutrition (EPIC). PLoS One. 2012, 7: e39361-10.1371/journal.pone.0039361.CrossRefPubMedPubMedCentral
10.
go back to reference Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, Olsen A, Tjonneland A, Dahm CC, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Nailler L, Kaaks R, Teucher B, Boeing H, Bergmann MM, Trichopoulou A, Lagiou P, Trichopoulos D, Palli D, Pala V, Tumino R, Vineis P, Panico S, Peeters PH, Dik VK, Weiderpass E, Lund E, Garcia JR, et al: Consumption of dairy products and colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). PLoS One. 2013, 8: e72715-10.1371/journal.pone.0072715.CrossRefPubMedPubMedCentral Murphy N, Norat T, Ferrari P, Jenab M, Bueno-de-Mesquita B, Skeie G, Olsen A, Tjonneland A, Dahm CC, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Nailler L, Kaaks R, Teucher B, Boeing H, Bergmann MM, Trichopoulou A, Lagiou P, Trichopoulos D, Palli D, Pala V, Tumino R, Vineis P, Panico S, Peeters PH, Dik VK, Weiderpass E, Lund E, Garcia JR, et al: Consumption of dairy products and colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). PLoS One. 2013, 8: e72715-10.1371/journal.pone.0072715.CrossRefPubMedPubMedCentral
11.
go back to reference Gonzalez CA, Riboli E: Diet and cancer prevention: contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Cancer. 2010, 46: 2555-2562. 10.1016/j.ejca.2010.07.025.CrossRefPubMed Gonzalez CA, Riboli E: Diet and cancer prevention: contributions from the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Cancer. 2010, 46: 2555-2562. 10.1016/j.ejca.2010.07.025.CrossRefPubMed
12.
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, Tjønneland 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, et al: Cigarette smoking and colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition study. Clin Gastroenterol Hepatol. 2011, 9: 137-144. 10.1016/j.cgh.2010.10.012.CrossRefPubMed Leufkens AM, Van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, Tjønneland 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, et al: Cigarette smoking and colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition study. Clin Gastroenterol Hepatol. 2011, 9: 137-144. 10.1016/j.cgh.2010.10.012.CrossRefPubMed
13.
go back to reference Friedenreich C, Norat T, Steindorf K, Boutron-Ruault MC, Pischon T, Mazuir M, Clavel-Chapelon F, Linseisen J, Boeing H, Bergman M, Johnsen NF, Tjønneland A, Overvad K, Mendez M, Quirós JR, Martinez C, Dorronsoro M, Navarro C, Gurrea AB, Bingham S, Khaw KT, Allen N, Key T, Trichopoulou A, Trichopoulos D, Orfanou N, Krogh V, Palli D, Tumino R, Panico S, et al: Physical activity and risk of colon and rectal cancers: the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev. 2006, 15: 2398-2407. 10.1158/1055-9965.EPI-06-0595.CrossRefPubMed Friedenreich C, Norat T, Steindorf K, Boutron-Ruault MC, Pischon T, Mazuir M, Clavel-Chapelon F, Linseisen J, Boeing H, Bergman M, Johnsen NF, Tjønneland A, Overvad K, Mendez M, Quirós JR, Martinez C, Dorronsoro M, Navarro C, Gurrea AB, Bingham S, Khaw KT, Allen N, Key T, Trichopoulou A, Trichopoulos D, Orfanou N, Krogh V, Palli D, Tumino R, Panico S, et al: Physical activity and risk of colon and rectal cancers: the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev. 2006, 15: 2398-2407. 10.1158/1055-9965.EPI-06-0595.CrossRefPubMed
14.
go back to reference Continuous Update Project Report. Food, Nutrition, Physical Activity, and the Prevention of Colorectal Cancer. 2011 Continuous Update Project Report. Food, Nutrition, Physical Activity, and the Prevention of Colorectal Cancer. 2011
15.
go back to reference Wiseman M: The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc. 2008, 67: 253-256. 10.1017/S002966510800712X.CrossRefPubMed Wiseman M: The second World Cancer Research Fund/American Institute for Cancer Research expert report. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Proc Nutr Soc. 2008, 67: 253-256. 10.1017/S002966510800712X.CrossRefPubMed
16.
go back to reference Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. 2007, AICR, Washington DC Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. 2007, AICR, Washington DC
17.
go back to reference Eide GE, Heuch I: Average attributable fractions: a coherent theory for apportioning excess risk to individual risk factors and subpopulations. Biom J. 2006, 48: 820-837. 10.1002/bimj.200510228.CrossRefPubMed Eide GE, Heuch I: Average attributable fractions: a coherent theory for apportioning excess risk to individual risk factors and subpopulations. Biom J. 2006, 48: 820-837. 10.1002/bimj.200510228.CrossRefPubMed
18.
go back to reference Aleksandrova K, Nimptsch K, Pischon T: Obesity and colorectal cancer. Front Biosci. 2013, 5: 61-77.CrossRef Aleksandrova K, Nimptsch K, Pischon T: Obesity and colorectal cancer. Front Biosci. 2013, 5: 61-77.CrossRef
19.
go back to reference Robsahm TE, Aagnes B, Hjartaker A, Langseth H, Bray FI, Larsen IK: Body mass index, physical activity, and colorectal cancer by anatomical subsites: a systematic review and meta-analysis of cohort studies. Eur J Cancer Prev. 2013, 22: 492-505. 10.1097/CEJ.0b013e328360f434.CrossRefPubMed Robsahm TE, Aagnes B, Hjartaker A, Langseth H, Bray FI, Larsen IK: Body mass index, physical activity, and colorectal cancer by anatomical subsites: a systematic review and meta-analysis of cohort studies. Eur J Cancer Prev. 2013, 22: 492-505. 10.1097/CEJ.0b013e328360f434.CrossRefPubMed
20.
go back to reference Harriss DJ, Atkinson G, Batterham A, George K, Cable NT, Reilly T, Haboubi N, Renehan AG: Lifestyle factors and colorectal cancer risk (2): a systematic review and meta-analysis of associations with leisure-time physical activity. Colorectal Dis. 2009, 11: 689-701. 10.1111/j.1463-1318.2009.01767.x.CrossRefPubMed Harriss DJ, Atkinson G, Batterham A, George K, Cable NT, Reilly T, Haboubi N, Renehan AG: Lifestyle factors and colorectal cancer risk (2): a systematic review and meta-analysis of associations with leisure-time physical activity. Colorectal Dis. 2009, 11: 689-701. 10.1111/j.1463-1318.2009.01767.x.CrossRefPubMed
21.
go back to reference Hoffmann K, Heidemann C, Weikert C, Schulze MB, Boeing H: Estimating the proportion of disease due to classes of sufficient causes. Am J Epidemiol. 2006, 163: 76-83. 10.1093/aje/kwj011.CrossRefPubMed Hoffmann K, Heidemann C, Weikert C, Schulze MB, Boeing H: Estimating the proportion of disease due to classes of sufficient causes. Am J Epidemiol. 2006, 163: 76-83. 10.1093/aje/kwj011.CrossRefPubMed
22.
go back to reference Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, Overvad K, Tjønneland A, Clavel-Chapelon F, Thiébaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-De-Mesquita HB, Peeters PH, Lund E, Engeset D, González CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, et al: European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002, 5: 1113-1124. 10.1079/PHN2002394.CrossRefPubMed Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondiere UR, Hemon B, Casagrande C, Vignat J, Overvad K, Tjønneland A, Clavel-Chapelon F, Thiébaut A, Wahrendorf J, Boeing H, Trichopoulos D, Trichopoulou A, Vineis P, Palli D, Bueno-De-Mesquita HB, Peeters PH, Lund E, Engeset D, González CA, Barricarte A, Berglund G, Hallmans G, Day NE, Key TJ, et al: European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002, 5: 1113-1124. 10.1079/PHN2002394.CrossRefPubMed
23.
go back to reference Bramer GR: International statistical classification of diseases and related health problems. Tenth revision. Colorectal Dis. 1988, 41: 32-36. Bramer GR: International statistical classification of diseases and related health problems. Tenth revision. Colorectal Dis. 1988, 41: 32-36.
24.
go back to reference World Health Organization: International classification of diseases for oncology. 2nd edition. Geneva, Switzerland; 1990. World Health Organization: International classification of diseases for oncology. 2nd edition. Geneva, Switzerland; 1990.
25.
go back to reference Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, Salvini S, Parpinel M, Moller A, Ireland J, Becker W, Farran A, Westenbrink S, Vasilopoulou E, Unwin J, Borgejordet A, Rohrmann S, Church S, Gnagnarella P, Casagrande C, van Bakel M, Niravong M, Boutron-Ruault MC, Stripp C, Tjønneland A, Trichopoulou A, Georga K, Nilsson S, Mattisson I, Ray J, et al: The EPIC nutrient database project (ENDB): a first attempt to standardize nutrient databases across the 10 European countries participating in the EPIC study. Eur J Clin Nutr. 2007, 61: 1037-1056. 10.1038/sj.ejcn.1602679.CrossRefPubMed Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, Salvini S, Parpinel M, Moller A, Ireland J, Becker W, Farran A, Westenbrink S, Vasilopoulou E, Unwin J, Borgejordet A, Rohrmann S, Church S, Gnagnarella P, Casagrande C, van Bakel M, Niravong M, Boutron-Ruault MC, Stripp C, Tjønneland A, Trichopoulou A, Georga K, Nilsson S, Mattisson I, Ray J, et al: The EPIC nutrient database project (ENDB): a first attempt to standardize nutrient databases across the 10 European countries participating in the EPIC study. Eur J Clin Nutr. 2007, 61: 1037-1056. 10.1038/sj.ejcn.1602679.CrossRefPubMed
26.
go back to reference Kaaks R, Riboli E: Validation and calibration of dietary intake measurements in the EPIC project: methodological considerations. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997, 26: S15-S25. 10.1093/ije/26.suppl_1.S15.CrossRefPubMed Kaaks R, Riboli E: Validation and calibration of dietary intake measurements in the EPIC project: methodological considerations. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997, 26: S15-S25. 10.1093/ije/26.suppl_1.S15.CrossRefPubMed
27.
go back to reference Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. Tech Rep Ser. 1995, 854: 1-452. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. Tech Rep Ser. 1995, 854: 1-452.
28.
go back to reference Alberti KG, Zimmet P, Shaw J: The metabolic syndrome–a new worldwide definition. Lancet. 2005, 366: 1059-1062. 10.1016/S0140-6736(05)67402-8.CrossRefPubMed Alberti KG, Zimmet P, Shaw J: The metabolic syndrome–a new worldwide definition. Lancet. 2005, 366: 1059-1062. 10.1016/S0140-6736(05)67402-8.CrossRefPubMed
29.
go back to reference Fieller E: The biological standardization of insulin. J R Stat Soc. 1940, 7: 1-15. Fieller E: The biological standardization of insulin. J R Stat Soc. 1940, 7: 1-15.
30.
go back to reference Lunn M, McNeil D: Applying Cox regression to competing risks. Biometrics. 1995, 51: 524-532. 10.2307/2532940.CrossRefPubMed Lunn M, McNeil D: Applying Cox regression to competing risks. Biometrics. 1995, 51: 524-532. 10.2307/2532940.CrossRefPubMed
31.
go back to reference Miettinen OS: Proportion of disease caused or prevented by a given exposure, trait or intervention. Am J Epidemiol. 1974, 99: 325-332.PubMed Miettinen OS: Proportion of disease caused or prevented by a given exposure, trait or intervention. Am J Epidemiol. 1974, 99: 325-332.PubMed
32.
go back to reference Bruzzi P, Green SB, Byar DP, Brinton LA, Schairer C: Estimating the population attributable risk for multiple risk factors using case-control data. Am J Epidemiol. 1985, 122: 904-914.PubMed Bruzzi P, Green SB, Byar DP, Brinton LA, Schairer C: Estimating the population attributable risk for multiple risk factors using case-control data. Am J Epidemiol. 1985, 122: 904-914.PubMed
33.
go back to reference Whittemore AS: Statistical methods for estimating attributable risk from retrospective data. Stat Med. 1982, 1: 229-243. 10.1002/sim.4780010305.CrossRefPubMed Whittemore AS: Statistical methods for estimating attributable risk from retrospective data. Stat Med. 1982, 1: 229-243. 10.1002/sim.4780010305.CrossRefPubMed
34.
go back to reference Ford ES, Bergmann MM, Kroger J, Schienkiewitz A, Weikert C, Boeing H: Healthy living is the best revenge: findings from the European Prospective Investigation Into Cancer and Nutrition-Potsdam study. Arch Intern Med. 2009, 169: 1355-1362. 10.1001/archinternmed.2009.237.CrossRefPubMed Ford ES, Bergmann MM, Kroger J, Schienkiewitz A, Weikert C, Boeing H: Healthy living is the best revenge: findings from the European Prospective Investigation Into Cancer and Nutrition-Potsdam study. Arch Intern Med. 2009, 169: 1355-1362. 10.1001/archinternmed.2009.237.CrossRefPubMed
35.
go back to reference Pischon T, Mohlig M, Hoffmann K, Spranger J, Weikert C, Willich SN, Pfeiffer AF, Boeing H: Comparison of relative and attributable risk of myocardial infarction and stroke according to C-reactive protein and low-density lipoprotein cholesterol levels. Eur J Epidemiol. 2007, 22: 429-438. 10.1007/s10654-007-9141-2.CrossRefPubMed Pischon T, Mohlig M, Hoffmann K, Spranger J, Weikert C, Willich SN, Pfeiffer AF, Boeing H: Comparison of relative and attributable risk of myocardial infarction and stroke according to C-reactive protein and low-density lipoprotein cholesterol levels. Eur J Epidemiol. 2007, 22: 429-438. 10.1007/s10654-007-9141-2.CrossRefPubMed
36.
go back to reference Heidemann C, Hoffmann K, Klipstein-Grobusch K, Weikert C, Pischon T, Hense HW, Boeing H: Potentially modifiable classic risk factors and their impact on incident myocardial infarction: results from the EPIC-Potsdam study. Eur J Cardiovasc Prev Rehabil. 2007, 14: 65-71. 10.1097/01.hjr.0000238392.19847.4c.CrossRefPubMed Heidemann C, Hoffmann K, Klipstein-Grobusch K, Weikert C, Pischon T, Hense HW, Boeing H: Potentially modifiable classic risk factors and their impact on incident myocardial infarction: results from the EPIC-Potsdam study. Eur J Cardiovasc Prev Rehabil. 2007, 14: 65-71. 10.1097/01.hjr.0000238392.19847.4c.CrossRefPubMed
37.
go back to reference Zavoral M, Suchanek S, Zavada F, Dusek L, Muzik J, Seifert B, Fric P: Colorectal cancer screening in Europe. World J Gastroenterol. 2009, 15: 5907-5915. 10.3748/wjg.15.5907.CrossRefPubMedPubMedCentral Zavoral M, Suchanek S, Zavada F, Dusek L, Muzik J, Seifert B, Fric P: Colorectal cancer screening in Europe. World J Gastroenterol. 2009, 15: 5907-5915. 10.3748/wjg.15.5907.CrossRefPubMedPubMedCentral
38.
go back to reference Correa Lima MP, Gomes-da-Silva MH: Colorectal cancer: lifestyle and dietary factors. Nutr Hosp. 2005, 20: 235-241.PubMed Correa Lima MP, Gomes-da-Silva MH: Colorectal cancer: lifestyle and dietary factors. Nutr Hosp. 2005, 20: 235-241.PubMed
39.
go back to reference Ahmed FE: Effect of diet, life style, and other environmental/chemopreventive factors on colorectal cancer development, and assessment of the risks. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2004, 22: 91-147. 10.1081/LESC-200038263.CrossRefPubMed Ahmed FE: Effect of diet, life style, and other environmental/chemopreventive factors on colorectal cancer development, and assessment of the risks. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2004, 22: 91-147. 10.1081/LESC-200038263.CrossRefPubMed
40.
go back to reference Qasim A, O’Morain C: Primary prevention of colorectal cancer: are we closer to reality?. Eur J Gastroenterol Hepatol. 2010, 22: 9-17. 10.1097/MEG.0b013e328330d0d6.CrossRefPubMed Qasim A, O’Morain C: Primary prevention of colorectal cancer: are we closer to reality?. Eur J Gastroenterol Hepatol. 2010, 22: 9-17. 10.1097/MEG.0b013e328330d0d6.CrossRefPubMed
41.
go back to reference 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: 579-588. 10.1023/A:1008999232442.CrossRefPubMed 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: 579-588. 10.1023/A:1008999232442.CrossRefPubMed
42.
go back to reference Kirkegaard H, Johnsen NF, Christensen J, Frederiksen K, Overvad K, Tjonneland A: Association of adherence to lifestyle recommendations and risk of colorectal cancer: a prospective Danish cohort study. BMJ. 2010, 341: c5504-10.1136/bmj.c5504.CrossRefPubMedPubMedCentral Kirkegaard H, Johnsen NF, Christensen J, Frederiksen K, Overvad K, Tjonneland A: Association of adherence to lifestyle recommendations and risk of colorectal cancer: a prospective Danish cohort study. BMJ. 2010, 341: c5504-10.1136/bmj.c5504.CrossRefPubMedPubMedCentral
43.
go back to reference Wei EK, Colditz GA, Giovannucci EL, Fuchs CS, Rosner BA: Cumulative risk of colon cancer up to age 70 years by risk factor status using data from the Nurses’ Health Study. Am J Epidemiol. 2009, 170: 863-872. 10.1093/aje/kwp210.CrossRefPubMedPubMedCentral Wei EK, Colditz GA, Giovannucci EL, Fuchs CS, Rosner BA: Cumulative risk of colon cancer up to age 70 years by risk factor status using data from the Nurses’ Health Study. Am J Epidemiol. 2009, 170: 863-872. 10.1093/aje/kwp210.CrossRefPubMedPubMedCentral
44.
go back to reference Romaguera D, Vergnaud AC, Peeters PH, van Gils CH, Chan DS, Ferrari P, Romieu I, Jenab M, Slimani N, Clavel-Chapelon F, Fagherazzi G, Perquier F, Kaaks R, Teucher B, Boeing H, von Rüsten A, Tjønneland A, Olsen A, Dahm CC, Overvad K, Quirós JR, Gonzalez CA, Sánchez MJ, Navarro C, Barricarte A, Dorronsoro M, Khaw KT, Wareham NJ, Crowe FL, Key TJ, et al: Is concordance with World Cancer Research Fund/American Institute for Cancer Research guidelines for cancer prevention related to subsequent risk of cancer? Results from the EPIC study. Am J Clin Nutr. 2012, 96: 150-163. 10.3945/ajcn.111.031674.CrossRefPubMed Romaguera D, Vergnaud AC, Peeters PH, van Gils CH, Chan DS, Ferrari P, Romieu I, Jenab M, Slimani N, Clavel-Chapelon F, Fagherazzi G, Perquier F, Kaaks R, Teucher B, Boeing H, von Rüsten A, Tjønneland A, Olsen A, Dahm CC, Overvad K, Quirós JR, Gonzalez CA, Sánchez MJ, Navarro C, Barricarte A, Dorronsoro M, Khaw KT, Wareham NJ, Crowe FL, Key TJ, et al: Is concordance with World Cancer Research Fund/American Institute for Cancer Research guidelines for cancer prevention related to subsequent risk of cancer? Results from the EPIC study. Am J Clin Nutr. 2012, 96: 150-163. 10.3945/ajcn.111.031674.CrossRefPubMed
45.
go back to reference Aleksandrova K, Nimptsch K, Pischon T: Influence of obesity and related metabolic alterations on colorectal cancer risk. Curr Nutr Repts. 2013, 2: 1-9. 10.1007/s13668-012-0036-9.CrossRef Aleksandrova K, Nimptsch K, Pischon T: Influence of obesity and related metabolic alterations on colorectal cancer risk. Curr Nutr Repts. 2013, 2: 1-9. 10.1007/s13668-012-0036-9.CrossRef
46.
go back to reference Aleksandrova K, Drogan D, Boeing H, Jenab M, Bas Bueno-de-Mesquita H, Jansen E, van Duijnhoven FJ, Rinaldi S, Fedirko V, Romieu I, Kaaks R, Riboli E, Gunter MJ, Romaguera D, Westhpal S, Overvad K, Tjønneland A, Halkjaer J, Boutron-Ruault MC, Clavel-Chapelon F, Lukanova A, Trichopoulou A, Trichopoulos D, Vidalis P, Panico S, Agnoli C, Palli D, Tumino R, Vineis P, Buckland G, et al: Adiposity, mediating biomarkers and risk of colon cancer in the European prospective investigation into cancer and nutrition study. Int J Cancer. 2014, 134: 612-621. 10.1002/ijc.28368.CrossRefPubMed Aleksandrova K, Drogan D, Boeing H, Jenab M, Bas Bueno-de-Mesquita H, Jansen E, van Duijnhoven FJ, Rinaldi S, Fedirko V, Romieu I, Kaaks R, Riboli E, Gunter MJ, Romaguera D, Westhpal S, Overvad K, Tjønneland A, Halkjaer J, Boutron-Ruault MC, Clavel-Chapelon F, Lukanova A, Trichopoulou A, Trichopoulos D, Vidalis P, Panico S, Agnoli C, Palli D, Tumino R, Vineis P, Buckland G, et al: Adiposity, mediating biomarkers and risk of colon cancer in the European prospective investigation into cancer and nutrition study. Int J Cancer. 2014, 134: 612-621. 10.1002/ijc.28368.CrossRefPubMed
47.
go back to reference Fu Z, Shrubsole MJ, Smalley WE, Wu H, Chen Z, Shyr Y, Ness RM, Zheng W: Lifestyle factors and their combined impact on the risk of colorectal polyps. Am J Epidemiol. 2012, 176: 766-776. 10.1093/aje/kws157.CrossRefPubMedPubMedCentral Fu Z, Shrubsole MJ, Smalley WE, Wu H, Chen Z, Shyr Y, Ness RM, Zheng W: Lifestyle factors and their combined impact on the risk of colorectal polyps. Am J Epidemiol. 2012, 176: 766-776. 10.1093/aje/kws157.CrossRefPubMedPubMedCentral
Metadata
Title
Combined impact of healthy lifestyle factors on colorectal cancer: a large European cohort study
Authors
Krasimira Aleksandrova
Tobias Pischon
Mazda Jenab
H Bas Bueno-de-Mesquita
Veronika Fedirko
Teresa Norat
Dora Romaguera
Sven Knüppel
Marie-Christine Boutron-Ruault
Laure Dossus
Laureen Dartois
Rudolf Kaaks
Kuanrong Li
Anne Tjønneland
Kim Overvad
José Ramón Quirós
Genevieve Buckland
María José Sánchez
Miren Dorronsoro
Maria-Dolores Chirlaque
Aurelio Barricarte
Kay-Tee Khaw
Nicholas J Wareham
Kathryn E Bradbury
Antonia Trichopoulou
Pagona Lagiou
Dimitrios Trichopoulos
Domenico Palli
Vittorio Krogh
Rosario Tumino
Alessio Naccarati
Salvatore Panico
Peter D Siersema
Petra HM Peeters
Ingrid Ljuslinder
Ingegerd Johansson
Ulrika Ericson
Bodil Ohlsson
Elisabete Weiderpass
Guri Skeie
Kristin Benjaminsen Borch
Sabina Rinaldi
Isabelle Romieu
Joyce Kong
Marc J Gunter
Heather A Ward
Elio Riboli
Heiner Boeing
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2014
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-014-0168-4

Other articles of this Issue 1/2014

BMC Medicine 1/2014 Go to the issue