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Published in: BMC Medicine 1/2021

Open Access 01-12-2021 | Colorectal Cancer | Research article

Development and validation of a lifestyle-based model for colorectal cancer risk prediction: the LiFeCRC score

Authors: Krasimira Aleksandrova, Robin Reichmann, Rudolf Kaaks, Mazda Jenab, H. Bas Bueno-de-Mesquita, Christina C. Dahm, Anne Kirstine Eriksen, Anne Tjønneland, Fanny Artaud, Marie-Christine Boutron-Ruault, Gianluca Severi, Anika Hüsing, Antonia Trichopoulou, Anna Karakatsani, Eleni Peppa, Salvatore Panico, Giovanna Masala, Sara Grioni, Carlotta Sacerdote, Rosario Tumino, Sjoerd G. Elias, Anne M. May, Kristin B. Borch, Torkjel M. Sandanger, Guri Skeie, Maria-Jose Sánchez, José María Huerta, Núria Sala, Aurelio Barricarte Gurrea, José Ramón Quirós, Pilar Amiano, Jonna Berntsson, Isabel Drake, Bethany van Guelpen, Sophia Harlid, Tim Key, Elisabete Weiderpass, Elom K. Aglago, Amanda J. Cross, Konstantinos K. Tsilidis, Elio Riboli, Marc J. Gunter

Published in: BMC Medicine | Issue 1/2021

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Abstract

Background

Nutrition and lifestyle have been long established as risk factors for colorectal cancer (CRC). Modifiable lifestyle behaviours bear potential to minimize long-term CRC risk; however, translation of lifestyle information into individualized CRC risk assessment has not been implemented. Lifestyle-based risk models may aid the identification of high-risk individuals, guide referral to screening and motivate behaviour change. We therefore developed and validated a lifestyle-based CRC risk prediction algorithm in an asymptomatic European population.

Methods

The model was based on data from 255,482 participants in the European Prospective Investigation into Cancer and Nutrition (EPIC) study aged 19 to 70 years who were free of cancer at study baseline (1992–2000) and were followed up to 31 September 2010. The model was validated in a sample comprising 74,403 participants selected among five EPIC centres. Over a median follow-up time of 15 years, there were 3645 and 981 colorectal cancer cases in the derivation and validation samples, respectively. Variable selection algorithms in Cox proportional hazard regression and random survival forest (RSF) were used to identify the best predictors among plausible predictor variables. Measures of discrimination and calibration were calculated in derivation and validation samples. To facilitate model communication, a nomogram and a web-based application were developed.

Results

The final selection model included age, waist circumference, height, smoking, alcohol consumption, physical activity, vegetables, dairy products, processed meat, and sugar and confectionary. The risk score demonstrated good discrimination overall and in sex-specific models. Harrell’s C-index was 0.710 in the derivation cohort and 0.714 in the validation cohort. The model was well calibrated and showed strong agreement between predicted and observed risk. Random survival forest analysis suggested high model robustness. Beyond age, lifestyle data led to improved model performance overall (continuous net reclassification improvement = 0.307 (95% CI 0.264–0.352)), and especially for young individuals below 45 years (continuous net reclassification improvement = 0.364 (95% CI 0.084–0.575)).

Conclusions

LiFeCRC score based on age and lifestyle data accurately identifies individuals at risk for incident colorectal cancer in European populations and could contribute to improved prevention through motivating lifestyle change at an individual level.
Appendix
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Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.CrossRefPubMed Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424.CrossRefPubMed
2.
go back to reference Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91.PubMedCrossRef Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91.PubMedCrossRef
3.
go back to reference Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, Gavin A, Visser O, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356–87.PubMedCrossRef Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, Gavin A, Visser O, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356–87.PubMedCrossRef
4.
go back to reference Islami F, Goding Sauer A, Miller KD, Siegel RL, Fedewa SA, Jacobs EJ, McCullough ML, Patel AV, Ma J, Soerjomataram I, et al. Proportion and number of cancer cases and deaths attributable to potentially modifiable risk factors in the United States. CA Cancer J Clin. 2018;68(1):31–54.PubMedCrossRef Islami F, Goding Sauer A, Miller KD, Siegel RL, Fedewa SA, Jacobs EJ, McCullough ML, Patel AV, Ma J, Soerjomataram I, et al. Proportion and number of cancer cases and deaths attributable to potentially modifiable risk factors in the United States. CA Cancer J Clin. 2018;68(1):31–54.PubMedCrossRef
5.
go back to reference Zhang FF, Cudhea F, Shan Z, Michaud DS, Imamura F, Eom H, Ruan M, Rehm CD, Liu J, Du M, et al. Preventable cancer burden associated with poor diet in the United States. JNCI Cancer Spectr. 2019;3(2):pkz034.PubMedPubMedCentralCrossRef Zhang FF, Cudhea F, Shan Z, Michaud DS, Imamura F, Eom H, Ruan M, Rehm CD, Liu J, Du M, et al. Preventable cancer burden associated with poor diet in the United States. JNCI Cancer Spectr. 2019;3(2):pkz034.PubMedPubMedCentralCrossRef
6.
7.
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, et al. 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(9368):1496–501.PubMedCrossRef Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, et al. 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(9368):1496–501.PubMedCrossRef
8.
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, 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(9):2065–72.PubMedCrossRef Ferrari P, Jenab M, Norat T, Moskal A, Slimani N, Olsen A, Tjonneland A, Overvad K, Jensen MK, Boutron-Ruault MC, 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(9):2065–72.PubMedCrossRef
9.
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, et al. Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomark Prev. 2004;13(10):1595–603. Jenab M, Ferrari P, Slimani N, Norat T, Casagrande C, Overad K, Olsen A, Stripp C, Tjonneland A, Boutron-Ruault MC, et al. Association of nut and seed intake with colorectal cancer risk in the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomark Prev. 2004;13(10):1595–603.
10.
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, et al. Cigarette smoking and colorectal cancer risk in the EPIC study. Clin Gastroenterol Hepatol. 2011;9(2):137–44. Leufkens AM, van Duijnhoven FJ, Siersema PD, Boshuizen HC, Vrieling A, Agudo A, Gram IT, Weiderpass E, Dahm C, Overvad K, et al. Cigarette smoking and colorectal cancer risk in the EPIC study. Clin Gastroenterol Hepatol. 2011;9(2):137–44.
11.
go back to reference Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjonneland A, Clavel F, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. J Natl Cancer Inst. 2005;97(12):906–16.PubMedCrossRef Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjonneland A, Clavel F, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. J Natl Cancer Inst. 2005;97(12):906–16.PubMedCrossRef
12.
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, 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(13):920–31.PubMedCrossRef Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, Tjonneland A, Halkjaer J, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, 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(13):920–31.PubMedCrossRef
13.
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, et al. Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2009;89(5):1441–52.PubMedCrossRef van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P, Jenab M, Boshuizen HC, Ros MM, Casagrande C, Tjonneland A, Olsen A, Overvad K, et al. Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 2009;89(5):1441–52.PubMedCrossRef
14.
go back to reference Vieira AR, Abar L, Chan DSM, Vingeliene S, Polemiti E, Stevens C, Greenwood D, Norat T. Foods and beverages and colorectal cancer risk: a systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR Continuous Update Project. Ann Oncol. 2017;28(8):1788–802.PubMedCrossRef Vieira AR, Abar L, Chan DSM, Vingeliene S, Polemiti E, Stevens C, Greenwood D, Norat T. Foods and beverages and colorectal cancer risk: a systematic review and meta-analysis of cohort studies, an update of the evidence of the WCRF-AICR Continuous Update Project. Ann Oncol. 2017;28(8):1788–802.PubMedCrossRef
15.
go back to reference World Cancer Research Fund/American Institute for Cancer Research Diet, Nutrition, Physical Activity and Cancer: A Global Perspective. Continuous Update Project Expert Report 2018. Available online: http://dietandcancerreport.org. Accessed 2 Mar 2020. World Cancer Research Fund/American Institute for Cancer Research Diet, Nutrition, Physical Activity and Cancer: A Global Perspective. Continuous Update Project Expert Report 2018. Available online: http://​dietandcancerrep​ort.​org. Accessed 2 Mar 2020.
16.
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(14):2555–62.PubMedCrossRef 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(14):2555–62.PubMedCrossRef
17.
go back to reference Freedman AN, Seminara D, Gail MH, Hartge P, Colditz GA, Ballard-Barbash R, Pfeiffer RM. Cancer risk prediction models: a workshop on development, evaluation, and application. J Natl Cancer Inst. 2005;97(10):715–23.PubMedCrossRef Freedman AN, Seminara D, Gail MH, Hartge P, Colditz GA, Ballard-Barbash R, Pfeiffer RM. Cancer risk prediction models: a workshop on development, evaluation, and application. J Natl Cancer Inst. 2005;97(10):715–23.PubMedCrossRef
18.
go back to reference Usher-Smith JA, Walter FM, Emery JD, Win AK, Griffin SJ. Risk prediction models for colorectal cancer: a systematic review. Cancer Prev Res (Phila). 2016;9(1):13–26.CrossRef Usher-Smith JA, Walter FM, Emery JD, Win AK, Griffin SJ. Risk prediction models for colorectal cancer: a systematic review. Cancer Prev Res (Phila). 2016;9(1):13–26.CrossRef
19.
go back to reference McGeoch L, Saunders CL, Griffin SJ, Emery JD, Walter FM, Thompson DJ, Antoniou AC, Usher-Smith JA. Risk prediction models for colorectal cancer incorporating common genetic variants: a systematic review. Cancer Epidemiol Biomark Prev. 2019;8(10):1580–93.CrossRef McGeoch L, Saunders CL, Griffin SJ, Emery JD, Walter FM, Thompson DJ, Antoniou AC, Usher-Smith JA. Risk prediction models for colorectal cancer incorporating common genetic variants: a systematic review. Cancer Epidemiol Biomark Prev. 2019;8(10):1580–93.CrossRef
20.
go back to reference Smith T, Muller DC, Moons KGM, Cross AJ, Johansson M, Ferrari P, Fagherazzi G, Peeters PHM, Severi G, Husing A, et al. Comparison of prognostic models to predict the occurrence of colorectal cancer in asymptomatic individuals: a systematic literature review and external validation in the EPIC and UK Biobank prospective cohort studies. Gut. 2019;68(4):672–83.PubMedCrossRef Smith T, Muller DC, Moons KGM, Cross AJ, Johansson M, Ferrari P, Fagherazzi G, Peeters PHM, Severi G, Husing A, et al. Comparison of prognostic models to predict the occurrence of colorectal cancer in asymptomatic individuals: a systematic literature review and external validation in the EPIC and UK Biobank prospective cohort studies. Gut. 2019;68(4):672–83.PubMedCrossRef
21.
go back to reference Ma GK, Ladabaum U. Personalizing colorectal cancer screening: a systematic review of models to predict risk of colorectal neoplasia. Clin Gastroenterol Hepatol. 2014;12(10):1624–34. e1621.PubMedCrossRef Ma GK, Ladabaum U. Personalizing colorectal cancer screening: a systematic review of models to predict risk of colorectal neoplasia. Clin Gastroenterol Hepatol. 2014;12(10):1624–34. e1621.PubMedCrossRef
22.
go back to reference Usher-Smith JA, Harshfield A, Saunders CL, Sharp SJ, Emery J, Walter FM, Muir K, Griffin SJ. External validation of risk prediction models for incident colorectal cancer using UK Biobank. Br J Cancer. 2018;118(5):750–9.PubMedPubMedCentralCrossRef Usher-Smith JA, Harshfield A, Saunders CL, Sharp SJ, Emery J, Walter FM, Muir K, Griffin SJ. External validation of risk prediction models for incident colorectal cancer using UK Biobank. Br J Cancer. 2018;118(5):750–9.PubMedPubMedCentralCrossRef
23.
go back to reference Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent Reporting of a multivariable prediction model for Individual Prognosis Or Diagnosis (TRIPOD): the TRIPOD statement. Br J Surg. 2015;102(3):148–58.PubMedCrossRef Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent Reporting of a multivariable prediction model for Individual Prognosis Or Diagnosis (TRIPOD): the TRIPOD statement. Br J Surg. 2015;102(3):148–58.PubMedCrossRef
24.
go back to reference Pavlou M, Ambler G, Seaman S, De Iorio M, Omar RZ. Review and evaluation of penalised regression methods for risk prediction in low-dimensional data with few events. Stat Med. 2016;35(7):1159–77.PubMedCrossRef Pavlou M, Ambler G, Seaman S, De Iorio M, Omar RZ. Review and evaluation of penalised regression methods for risk prediction in low-dimensional data with few events. Stat Med. 2016;35(7):1159–77.PubMedCrossRef
25.
go back to reference Cueto-Lopez N, Garcia-Ordas MT, Davila-Batista V, Moreno V, Aragones N, Alaiz-Rodriguez R. A comparative study on feature selection for a risk prediction model for colorectal cancer. Comput Methods Prog Biomed. 2019;177:219–29.CrossRef Cueto-Lopez N, Garcia-Ordas MT, Davila-Batista V, Moreno V, Aragones N, Alaiz-Rodriguez R. A comparative study on feature selection for a risk prediction model for colorectal cancer. Comput Methods Prog Biomed. 2019;177:219–29.CrossRef
27.
go back to reference Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondière UR, Hémon B, Casagrande C, Vignat J, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2007;5(6b):1113–24.CrossRef Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, Charrondière UR, Hémon B, Casagrande C, Vignat J, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2007;5(6b):1113–24.CrossRef
28.
go back to reference Aleksandrova K, Pischon T, Jenab M, Bueno-de-Mesquita HB, Fedirko V, Norat T, Romaguera D, Knuppel S, Boutron-Ruault MC, Dossus L, et al. Combined impact of healthy lifestyle factors on colorectal cancer: a large European cohort study. BMC Med. 2014;12:168.PubMedPubMedCentralCrossRef Aleksandrova K, Pischon T, Jenab M, Bueno-de-Mesquita HB, Fedirko V, Norat T, Romaguera D, Knuppel S, Boutron-Ruault MC, Dossus L, et al. Combined impact of healthy lifestyle factors on colorectal cancer: a large European cohort study. BMC Med. 2014;12:168.PubMedPubMedCentralCrossRef
29.
go back to reference Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, Salvini S, Parpinel M, Moller A, Ireland 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(9):1037–56.PubMedCrossRef Slimani N, Deharveng G, Unwin I, Southgate DA, Vignat J, Skeie G, Salvini S, Parpinel M, Moller A, Ireland 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(9):1037–56.PubMedCrossRef
30.
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(Suppl 1):S15–25.PubMedCrossRef 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(Suppl 1):S15–25.PubMedCrossRef
31.
go back to reference Moons KG, Altman DG, Reitsma JB, Ioannidis JP, Macaskill P, Steyerberg EW, Vickers AJ, Ransohoff DF, Collins GS. Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med. 2015;162(1):W1–73.PubMedCrossRef Moons KG, Altman DG, Reitsma JB, Ioannidis JP, Macaskill P, Steyerberg EW, Vickers AJ, Ransohoff DF, Collins GS. Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med. 2015;162(1):W1–73.PubMedCrossRef
32.
go back to reference Laurin C, Boomsma D, Lubke G. The use of vector bootstrapping to improve variable selection precision in Lasso models. Stat Appl Genet Mol Biol. 2016;15(4):305–20.PubMedCrossRef Laurin C, Boomsma D, Lubke G. The use of vector bootstrapping to improve variable selection precision in Lasso models. Stat Appl Genet Mol Biol. 2016;15(4):305–20.PubMedCrossRef
39.
go back to reference Austin PC, Latouche A, Fine JP. A review of the use of time-varying covariates in the Fine-Gray subdistribution hazard competing risk regression model. Stat Med. 2020;39(2):103–13.PubMedCrossRef Austin PC, Latouche A, Fine JP. A review of the use of time-varying covariates in the Fine-Gray subdistribution hazard competing risk regression model. Stat Med. 2020;39(2):103–13.PubMedCrossRef
40.
go back to reference Muller-Riemenschneider F, Holmberg C, Rieckmann N, Kliems H, Rufer V, Muller-Nordhorn J, Willich SN. Barriers to routine risk-score use for healthy primary care patients: survey and qualitative study. Arch Intern Med. 2010;170(8):719–24.PubMedCrossRef Muller-Riemenschneider F, Holmberg C, Rieckmann N, Kliems H, Rufer V, Muller-Nordhorn J, Willich SN. Barriers to routine risk-score use for healthy primary care patients: survey and qualitative study. Arch Intern Med. 2010;170(8):719–24.PubMedCrossRef
41.
go back to reference Usher-Smith JA, Sharp SJ, Luben R, Griffin SJ. Development and validation of lifestyle-based models to predict incidence of the most common potentially preventable cancers. Cancer Epidemiol Biomark Prev. 2019;28(1):67–75.CrossRef Usher-Smith JA, Sharp SJ, Luben R, Griffin SJ. Development and validation of lifestyle-based models to predict incidence of the most common potentially preventable cancers. Cancer Epidemiol Biomark Prev. 2019;28(1):67–75.CrossRef
42.
go back to reference Emmons KM, McBride CM, Puleo E, Pollak KI, Clipp E, Kuntz K, Marcus BH, Napolitano M, Onken J, Farraye F, et al. Project PREVENT: a randomized trial to reduce multiple behavioral risk factors for colon cancer. Cancer Epidemiol Biomark Prev. 2005;14(6):1453–9.CrossRef Emmons KM, McBride CM, Puleo E, Pollak KI, Clipp E, Kuntz K, Marcus BH, Napolitano M, Onken J, Farraye F, et al. Project PREVENT: a randomized trial to reduce multiple behavioral risk factors for colon cancer. Cancer Epidemiol Biomark Prev. 2005;14(6):1453–9.CrossRef
43.
go back to reference Smith-Warner SA, Elmer PJ, Tharp TM, Fosdick L, Randall B, Gross M, Wood J, Potter JD. Increasing vegetable and fruit intake: randomized intervention and monitoring in an at-risk population. Cancer Epidemiol Biomark Prev. 2000;9(3):307–17. Smith-Warner SA, Elmer PJ, Tharp TM, Fosdick L, Randall B, Gross M, Wood J, Potter JD. Increasing vegetable and fruit intake: randomized intervention and monitoring in an at-risk population. Cancer Epidemiol Biomark Prev. 2000;9(3):307–17.
44.
go back to reference Caswell S, Anderson AS, Steele RJ. Bowel health to better health: a minimal contact lifestyle intervention for people at increased risk of colorectal cancer. Br J Nutr. 2009;102(11):1541–6.PubMedCrossRef Caswell S, Anderson AS, Steele RJ. Bowel health to better health: a minimal contact lifestyle intervention for people at increased risk of colorectal cancer. Br J Nutr. 2009;102(11):1541–6.PubMedCrossRef
45.
go back to reference Robb KA, Power E, Kralj-Hans I, Atkin WS, Wardle J. The impact of individually-tailored lifestyle advice in the colorectal cancer screening context: a randomised pilot study in North-West London. Prev Med. 2010;51(6):505–8.PubMedCrossRef Robb KA, Power E, Kralj-Hans I, Atkin WS, Wardle J. The impact of individually-tailored lifestyle advice in the colorectal cancer screening context: a randomised pilot study in North-West London. Prev Med. 2010;51(6):505–8.PubMedCrossRef
46.
go back to reference Craigie AM, Caswell S, Paterson C, Treweek S, Belch JJ, Daly F, Rodger J, Thompson J, Kirk A, Ludbrook A, et al. Study protocol for BeWEL: the impact of a BodyWEight and physicaL activity intervention on adults at risk of developing colorectal adenomas. BMC Public Health. 2011;11:184.PubMedPubMedCentralCrossRef Craigie AM, Caswell S, Paterson C, Treweek S, Belch JJ, Daly F, Rodger J, Thompson J, Kirk A, Ludbrook A, et al. Study protocol for BeWEL: the impact of a BodyWEight and physicaL activity intervention on adults at risk of developing colorectal adenomas. BMC Public Health. 2011;11:184.PubMedPubMedCentralCrossRef
47.
go back to reference Anderson AS, Mackison D, Boath C, Steele R. Promoting changes in diet and physical activity in breast and colorectal cancer screening settings: an unexplored opportunity for endorsing healthy behaviors. Cancer Prev Res (Phila). 2013;6(3):165–72.CrossRef Anderson AS, Mackison D, Boath C, Steele R. Promoting changes in diet and physical activity in breast and colorectal cancer screening settings: an unexplored opportunity for endorsing healthy behaviors. Cancer Prev Res (Phila). 2013;6(3):165–72.CrossRef
48.
go back to reference Usher-Smith JA, Silarova B, Ward A, Youell J, Muir KR, Campbell J, Warcaba J. Incorporating cancer risk information into general practice: a qualitative study using focus groups with health professionals. Br J Gen Pract. 2017;67(656):e218–26.PubMedPubMedCentralCrossRef Usher-Smith JA, Silarova B, Ward A, Youell J, Muir KR, Campbell J, Warcaba J. Incorporating cancer risk information into general practice: a qualitative study using focus groups with health professionals. Br J Gen Pract. 2017;67(656):e218–26.PubMedPubMedCentralCrossRef
49.
go back to reference Demark-Wahnefried W, Rock CL, Patrick K, Byers T. Lifestyle interventions to reduce cancer risk and improve outcomes. Am Fam Physician. 2008;77(11):1573–8.PubMed Demark-Wahnefried W, Rock CL, Patrick K, Byers T. Lifestyle interventions to reduce cancer risk and improve outcomes. Am Fam Physician. 2008;77(11):1573–8.PubMed
50.
go back to reference Guo LW, Li N, Chen HD, Lyu ZY, Feng XS, Wei LP, Li X, Wen Y, Lu M, Dai M. Progress in construction and verification of colorectal cancer risk prediction models: a systematic review. Zhonghua Yu Fang Yi Xue Za Zhi. 2019;53(6):603–10.PubMed Guo LW, Li N, Chen HD, Lyu ZY, Feng XS, Wei LP, Li X, Wen Y, Lu M, Dai M. Progress in construction and verification of colorectal cancer risk prediction models: a systematic review. Zhonghua Yu Fang Yi Xue Za Zhi. 2019;53(6):603–10.PubMed
51.
go back to reference Williams TG, Cubiella J, Griffin SJ, Walter FM, Usher-Smith JA. Risk prediction models for colorectal cancer in people with symptoms: a systematic review. BMC Gastroenterol. 2016;16(1):63.PubMedPubMedCentralCrossRef Williams TG, Cubiella J, Griffin SJ, Walter FM, Usher-Smith JA. Risk prediction models for colorectal cancer in people with symptoms: a systematic review. BMC Gastroenterol. 2016;16(1):63.PubMedPubMedCentralCrossRef
52.
go back to reference Carr PR, Weigl K, Edelmann D, Jansen L, Chang-Claude J, Brenner H, Hoffmeister M. Estimation of absolute risk of colorectal cancer based on healthy lifestyle, genetic risk, and colonoscopy status in a population-based study. Gastroenterology. 2020;159(1):129–38. Carr PR, Weigl K, Edelmann D, Jansen L, Chang-Claude J, Brenner H, Hoffmeister M. Estimation of absolute risk of colorectal cancer based on healthy lifestyle, genetic risk, and colonoscopy status in a population-based study. Gastroenterology. 2020;159(1):129–38.
53.
go back to reference Aleksandrova K, Nimptsch K, Pischon T. Influence of obesity and related metabolic alterations on colorectal cancer risk. Curr Nutr Rep. 2013;2(1):1–9.PubMedCrossRef Aleksandrova K, Nimptsch K, Pischon T. Influence of obesity and related metabolic alterations on colorectal cancer risk. Curr Nutr Rep. 2013;2(1):1–9.PubMedCrossRef
54.
go back to reference Aleksandrova K, Schlesinger S, Fedirko V, Jenab M, Bueno-de-Mesquita B, Freisling H, Romieu I, Pischon T, Kaaks R, Gunter MJ, et al. Metabolic mediators of the association between adult weight gain and colorectal cancer: data from the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Am J Epidemiol. 2017;185(9):751–64.PubMedPubMedCentralCrossRef Aleksandrova K, Schlesinger S, Fedirko V, Jenab M, Bueno-de-Mesquita B, Freisling H, Romieu I, Pischon T, Kaaks R, Gunter MJ, et al. Metabolic mediators of the association between adult weight gain and colorectal cancer: data from the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Am J Epidemiol. 2017;185(9):751–64.PubMedPubMedCentralCrossRef
55.
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, 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(3):612–21.PubMedCrossRef Aleksandrova K, Drogan D, Boeing H, Jenab M, Bas Bueno-de-Mesquita H, Jansen E, van Duijnhoven FJ, Rinaldi S, Fedirko V, Romieu I, 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(3):612–21.PubMedCrossRef
56.
go back to reference Colditz GA, Atwood KA, Emmons K, Monson RR, Willett WC, Trichopoulos D, Hunter DJ. Harvard report on cancer prevention volume 4: Harvard Cancer Risk Index. Risk Index Working Group, Harvard Center for Cancer Prevention. Cancer Causes Control. 2000;11(6):477–88.PubMedCrossRef Colditz GA, Atwood KA, Emmons K, Monson RR, Willett WC, Trichopoulos D, Hunter DJ. Harvard report on cancer prevention volume 4: Harvard Cancer Risk Index. Risk Index Working Group, Harvard Center for Cancer Prevention. Cancer Causes Control. 2000;11(6):477–88.PubMedCrossRef
57.
go back to reference Shin A, Joo J, Yang HR, Bak J, Park Y, Kim J, Oh JH, Nam BH. Risk prediction model for colorectal cancer: National Health Insurance Corporation study, Korea. PLoS One. 2014;9(2):e88079.PubMedPubMedCentralCrossRef Shin A, Joo J, Yang HR, Bak J, Park Y, Kim J, Oh JH, Nam BH. Risk prediction model for colorectal cancer: National Health Insurance Corporation study, Korea. PLoS One. 2014;9(2):e88079.PubMedPubMedCentralCrossRef
58.
go back to reference Garcia J, Quintana-Domeque C. The evolution of adult height in Europe: a brief note. Econ Hum Biol. 2007;5(2):340–9.PubMedCrossRef Garcia J, Quintana-Domeque C. The evolution of adult height in Europe: a brief note. Econ Hum Biol. 2007;5(2):340–9.PubMedCrossRef
59.
go back to reference Gorczyca AM, Eaton CB, LaMonte MJ, Garcia DO, Johnston JD, He K, Bidulescu A, Goodman D, Groessl E, Lane D, et al. Association of physical activity and sitting time with incident colorectal cancer in postmenopausal women. Eur J Cancer Prev. 2018;27(4):331–8.PubMedPubMedCentralCrossRef Gorczyca AM, Eaton CB, LaMonte MJ, Garcia DO, Johnston JD, He K, Bidulescu A, Goodman D, Groessl E, Lane D, et al. Association of physical activity and sitting time with incident colorectal cancer in postmenopausal women. Eur J Cancer Prev. 2018;27(4):331–8.PubMedPubMedCentralCrossRef
60.
go back to reference Aleksandrova K, Jenab M, Leitzmann M, Bueno-de-Mesquita B, Kaaks R, Trichopoulou A, Bamia C, Lagiou P, Rinaldi S, Freisling H, et al. Physical activity, mediating factors and risk of colon cancer: insights into adiposity and circulating biomarkers from the EPIC cohort. Int J Epidemiol. 2017;46(6):1823–35.PubMedCrossRef Aleksandrova K, Jenab M, Leitzmann M, Bueno-de-Mesquita B, Kaaks R, Trichopoulou A, Bamia C, Lagiou P, Rinaldi S, Freisling H, et al. Physical activity, mediating factors and risk of colon cancer: insights into adiposity and circulating biomarkers from the EPIC cohort. Int J Epidemiol. 2017;46(6):1823–35.PubMedCrossRef
61.
go back to reference Wells BJ, Kattan MW, Cooper GS, Jackson L, Koroukian S. Colorectal cancer predicted risk online (CRC-PRO) calculator using data from the multi-ethnic cohort study. J Am Board Fam Med. 2014;27(1):42–55.PubMedPubMedCentralCrossRef Wells BJ, Kattan MW, Cooper GS, Jackson L, Koroukian S. Colorectal cancer predicted risk online (CRC-PRO) calculator using data from the multi-ethnic cohort study. J Am Board Fam Med. 2014;27(1):42–55.PubMedPubMedCentralCrossRef
62.
go back to reference Driver JA, Gaziano JM, Gelber RP, Lee IM, Buring JE, Kurth T. Development of a risk score for colorectal cancer in men. Am J Med. 2007;120(3):257–63.PubMedCrossRef Driver JA, Gaziano JM, Gelber RP, Lee IM, Buring JE, Kurth T. Development of a risk score for colorectal cancer in men. Am J Med. 2007;120(3):257–63.PubMedCrossRef
63.
go back to reference Freedman AN, Slattery ML, Ballard-Barbash R, Willis G, Cann BJ, Pee D, Gail MH, Pfeiffer RM. Colorectal cancer risk prediction tool for white men and women without known susceptibility. J Clin Oncol. 2009;27(5):686–93.PubMedCrossRef Freedman AN, Slattery ML, Ballard-Barbash R, Willis G, Cann BJ, Pee D, Gail MH, Pfeiffer RM. Colorectal cancer risk prediction tool for white men and women without known susceptibility. J Clin Oncol. 2009;27(5):686–93.PubMedCrossRef
64.
go back to reference Park Y, Freedman AN, Gail MH, Pee D, Hollenbeck A, Schatzkin A, Pfeiffer RM. Validation of a colorectal cancer risk prediction model among white patients age 50 years and older. J Clin Oncol. 2009;27(5):694–8.PubMedCrossRef Park Y, Freedman AN, Gail MH, Pee D, Hollenbeck A, Schatzkin A, Pfeiffer RM. Validation of a colorectal cancer risk prediction model among white patients age 50 years and older. J Clin Oncol. 2009;27(5):694–8.PubMedCrossRef
Metadata
Title
Development and validation of a lifestyle-based model for colorectal cancer risk prediction: the LiFeCRC score
Authors
Krasimira Aleksandrova
Robin Reichmann
Rudolf Kaaks
Mazda Jenab
H. Bas Bueno-de-Mesquita
Christina C. Dahm
Anne Kirstine Eriksen
Anne Tjønneland
Fanny Artaud
Marie-Christine Boutron-Ruault
Gianluca Severi
Anika Hüsing
Antonia Trichopoulou
Anna Karakatsani
Eleni Peppa
Salvatore Panico
Giovanna Masala
Sara Grioni
Carlotta Sacerdote
Rosario Tumino
Sjoerd G. Elias
Anne M. May
Kristin B. Borch
Torkjel M. Sandanger
Guri Skeie
Maria-Jose Sánchez
José María Huerta
Núria Sala
Aurelio Barricarte Gurrea
José Ramón Quirós
Pilar Amiano
Jonna Berntsson
Isabel Drake
Bethany van Guelpen
Sophia Harlid
Tim Key
Elisabete Weiderpass
Elom K. Aglago
Amanda J. Cross
Konstantinos K. Tsilidis
Elio Riboli
Marc J. Gunter
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2021
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-020-01826-0

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