The colorectal cancer epidemic: challenges and opportunities for primary, secondary and tertiary prevention

Colorectal cancer (CRC) is both one of the most common and one of the most preventable cancers globally, with powerful but strongly missed potential for primary, secondary and tertiary prevention. CRC incidence has traditionally been the highest in affluent Western countries, but it is now increasing rapidly with economic development in many other parts of the world. CRC shares several main risk factors, such as smoking, excessive alcohol consumption, physical inactivity and being overweight, with other common diseases; therefore, primary prevention efforts to reduce these risk factors are expected to have multiple beneficial effects that extend beyond CRC prevention, and should have high public health impact. A sizeable reduction in the incidence and mortality of CRC can also be achieved by offering effective screening tests, such as faecal immunochemical tests, flexible sigmoidoscopy and colonoscopy, in organised screening programmes which have been implemented in an increasing number of countries. Countries with early and high uptake rates of effective screening have exhibited major declines in CRC incidence and mortality, in contrast to most other countries. Finally, increasing evidence shows that the prognosis and quality of life of CRC patients can be substantially improved by tertiary prevention measures, such as the administration of low-dose aspirin and the promotion of physical activity.

[1]  H. Brenner,et al.  Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy. , 2013, European journal of cancer.

[2]  P. Rothwell,et al.  Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. , 2012, The Lancet. Oncology.

[3]  Ahmedin Jemal,et al.  Global patterns and trends in colorectal cancer incidence and mortality , 2016, Gut.

[4]  H. Brenner,et al.  Comparison of general obesity and measures of body fat distribution in older adults in relation to cancer risk: meta-analysis of individual participant data of seven prospective cohorts in Europe , 2017, British Journal of Cancer.

[5]  David Lieberman,et al.  Colorectal Cancer Screening: Recommendations for Physicians and Patients From the U.S. Multi-Society Task Force on Colorectal Cancer. , 2017, Gastroenterology.

[6]  P. Glasziou,et al.  Cochrane Systematic Review of Colorectal Cancer Screening Using the Fecal Occult Blood Test (Hemoccult): An Update , 2008, The American Journal of Gastroenterology.

[7]  J. Monson,et al.  Tobacco Smoking and Postoperative Outcomes After Colorectal Surgery , 2013, Annals of surgery.

[8]  C. Garland,et al.  Dose-response of serum 25-hydroxyvitamin D in association with risk of colorectal cancer: A meta-analysis , 2017, The Journal of Steroid Biochemistry and Molecular Biology.

[9]  C. Fuchs,et al.  SUNSHINE: Randomized double-blind phase II trial of vitamin D supplementation in patients with previously untreated metastatic colorectal cancer. , 2017 .

[10]  A. Capasso,et al.  Bioactive Nutrients and Nutrigenomics in Age-Related Diseases , 2017, Molecules.

[11]  M. Kloor,et al.  Lifestyle factors and risk of sporadic colorectal cancer by microsatellite instability status: a systematic review and meta-analyses , 2018, Annals of oncology : official journal of the European Society for Medical Oncology.

[12]  R. Wolff,et al.  Infrequently expressed miRNAs in colorectal cancer tissue and tumor molecular phenotype , 2017, Modern Pathology.

[13]  Jennifer S Lin,et al.  Screening for Colorectal Cancer: Updated Evidence Report and Systematic Review for the US Preventive Services Task Force. , 2016, JAMA.

[14]  C. Mathers,et al.  Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012 , 2015, International journal of cancer.

[15]  H. Brenner,et al.  In the era of widespread endoscopy use, randomized trials may strongly underestimate the effects of colorectal cancer screening. , 2013, Journal of clinical epidemiology.

[16]  Stephanie A. Bien,et al.  Determining Risk of Colorectal Cancer and Starting Age of Screening Based on Lifestyle, Environmental, and Genetic Factors. , 2018, Gastroenterology.

[17]  H. Brenner,et al.  Fecal occult blood versus DNA testing: indirect comparison in a colorectal cancer screening population , 2017, Clinical epidemiology.

[18]  Colorectal Cancer Screening in Average-Risk Adults , 2019, Annals of Internal Medicine.

[19]  H. Brenner,et al.  Cost-effectiveness of Colorectal Cancer Screening , 2011, Epidemiologic reviews.

[20]  I. Soerjomataram,et al.  Association of change in physical activity and body weight with quality of life and mortality in colorectal cancer: a systematic review and meta-analysis , 2015, Supportive Care in Cancer.

[21]  H. Brenner,et al.  Vitamin D Supplementation Trials Aimed at Reducing Mortality Have Much Higher Power When Focusing on People with Low Serum 25-Hydroxyvitamin D Concentrations. , 2017, The Journal of nutrition.

[22]  H. Brenner,et al.  Colonoscopy and sigmoidoscopy use among older adults in different countries: A systematic review. , 2017, Preventive medicine.

[23]  Karen M Kuntz,et al.  Estimation of Benefits, Burden, and Harms of Colorectal Cancer Screening Strategies: Modeling Study for the US Preventive Services Task Force. , 2016, JAMA.

[24]  H. Brenner,et al.  On-going improvement and persistent differences in the survival for patients with colon and rectum cancer across Europe 1999-2007 - Results from the EUROCARE-5 study. , 2015, European journal of cancer.

[25]  E. Kuipers,et al.  Adherence to colorectal cancer screening: four rounds of faecal immunochemical test-based screening , 2016, British Journal of Cancer.

[26]  M. Joore,et al.  The effects of school‐based lifestyle interventions on body mass index and blood pressure: a multivariate multilevel meta‐analysis of randomized controlled trials , 2016, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[27]  Mark P Purdue,et al.  Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. , 2012, The New England journal of medicine.

[28]  C. Farquhar,et al.  Long-term hormone therapy for perimenopausal and postmenopausal women. , 2017, The Cochrane database of systematic reviews.

[29]  J. Habbema,et al.  Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy , 2009, Gut.

[30]  G. S. Ranger The role of aspirin in colorectal cancer chemoprevention , 2016 .

[31]  Hermann Brenner,et al.  Colorectal cancer , 2014, The Lancet.

[32]  V. Beral,et al.  Menopausal hormone therapy and risk of gastrointestinal cancer: Nested case–control study within a prospective cohort, and meta‐analysis , 2012, International journal of cancer.

[33]  Yu-Jia Chang,et al.  Nicotine Enhances Colon Cancer Cell Migration by Induction of Fibronectin , 2011, Annals of Surgical Oncology.

[34]  P. Maisonneuve,et al.  Smoking and colorectal cancer: a meta-analysis. , 2008, JAMA.

[35]  M. Viswanathan,et al.  Hormone Therapy for the Primary Prevention of Chronic Conditions in Postmenopausal Women: Evidence Report and Systematic Review for the US Preventive Services Task Force , 2017, JAMA.

[36]  F. Bull,et al.  Physical activity and risks of proximal and distal colon cancers: a systematic review and meta-analysis. , 2012, Journal of the National Cancer Institute.

[37]  W. Willett,et al.  Population-wide Impact of Long-term Use of Aspirin and the Risk for Cancer. , 2016, JAMA oncology.

[38]  B. Vincenzi,et al.  Cigarettes smoking habit may reduce benefit from cetuximab-based treatment in advanced colorectal cancer patients , 2009, Expert opinion on biological therapy.

[39]  Han Wu,et al.  Aspirin use after diagnosis but not prediagnosis improves established colorectal cancer survival: a meta-analysis , 2014, Gut.

[40]  H. Brenner,et al.  Alcohol consumption and survival of colorectal cancer patients: a population-based study from Germany. , 2016, The American journal of clinical nutrition.

[41]  J. Souverijn,et al.  Multitarget stool DNA testing for colorectal-cancer screening. , 2014, The New England journal of medicine.

[42]  D. Lieberman,et al.  Recommendations on Fecal Immunochemical Testing to Screen for Colorectal Neoplasia: A Consensus Statement by the US Multi-Society Task Force on Colorectal Cancer , 2017, The American Journal of Gastroenterology.

[43]  E. Giovannucci,et al.  Integrative analysis of exogenous, endogenous, tumour and immune factors for precision medicine , 2018, Gut.

[44]  P. Schrotz-King,et al.  Administration of adjuvant chemotherapy for stage II‐III colon cancer patients: An European population‐based study , 2018, International journal of cancer.

[45]  H. Brenner,et al.  Relationship of very low serum 25-hydroxyvitamin D3 levels with long-term survival in a large cohort of colorectal cancer patients from Germany , 2017, European Journal of Epidemiology.

[46]  H. Brenner,et al.  Smoking and survival of colorectal cancer patients: systematic review and meta-analysis. , 2014, Annals of oncology : official journal of the European Society for Medical Oncology.

[47]  M. Kloor,et al.  Associations of red and processed meat with survival after colorectal cancer and differences according to timing of dietary assessment. , 2016, The American journal of clinical nutrition.

[48]  H. Brenner,et al.  Strongly enhanced colorectal cancer risk stratification by combining family history and genetic risk score , 2018, Clinical epidemiology.

[49]  Kirsten Bibbins-Domingo,et al.  Aspirin Use for the Primary Prevention of Cardiovascular Disease and Colorectal Cancer: U.S. Preventive Services Task Force Recommendation Statement. , 2016, Annals of internal medicine.

[50]  Michael Goodman,et al.  Effectiveness of screening colonoscopy in reducing the risk of death from right and left colon cancer: a large community-based study , 2016, Gut.

[51]  H. Brenner,et al.  Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: systematic review and meta-analysis of randomised controlled trials and observational studies , 2014, BMJ : British Medical Journal.

[52]  E. Giovannucci,et al.  Molecular pathological epidemiology of colorectal neoplasia: an emerging transdisciplinary and interdisciplinary field , 2010, Gut.

[53]  Recinda L. Sherman,et al.  Annual Report to the Nation on the Status of Cancer, 1975–2014, Featuring Survival , 2017, Journal of the National Cancer Institute.

[54]  H. Brenner,et al.  Beta blockers and cancer prognosis - The role of immortal time bias: A systematic review and meta-analysis. , 2016, Cancer treatment reviews.

[55]  C. la Vecchia,et al.  Alcohol consumption and site-specific cancer risk: a comprehensive dose–response meta-analysis , 2014, British Journal of Cancer.

[56]  P. A. van den Brandt,et al.  Lifestyle, Diet, and Colorectal Cancer Risk According to (Epi)genetic Instability: Current Evidence and Future Directions of Molecular Pathological Epidemiology , 2017, Current Colorectal Cancer Reports.

[57]  J. Lew,et al.  Long-term evaluation of benefits, harms, and cost-effectiveness of the National Bowel Cancer Screening Program in Australia: a modelling study. , 2017, The Lancet. Public health.

[58]  J. Meyerhardt,et al.  Association between Body Mass Index and Prognosis of Colorectal Cancer: A Meta-Analysis of Prospective Cohort Studies , 2015, PLoS ONE.

[59]  H. Brenner,et al.  Natural History of Colorectal Adenomas: Birth Cohort Analysis Among 3.6 Million Participants of Screening Colonoscopy , 2013, Cancer Epidemiology, Biomarkers & Prevention.

[60]  R. Langley,et al.  Metformin as an adjuvant treatment for cancer: a systematic review and meta-analysis , 2016, Annals of oncology : official journal of the European Society for Medical Oncology.

[61]  A. Hofman,et al.  Impact of prediagnostic smoking and smoking cessation on colorectal cancer prognosis: a meta-analysis of individual patient data from cohorts within the CHANCES consortium , 2018, Annals of oncology : official journal of the European Society for Medical Oncology.

[62]  Anurag K. Singh,et al.  Nicotinic modulation of therapeutic response in vitro and in vivo , 2012, International journal of cancer.

[63]  Philip S Rosenberg,et al.  Colorectal Cancer Incidence Patterns in the United States, 1974–2013 , 2017, Journal of the National Cancer Institute.

[64]  C. V. D. van de Velde,et al.  The mortality reducing effect of aspirin in colorectal cancer patients: Interpreting the evidence. , 2017, Cancer treatment reviews.

[65]  P. Schrotz-King,et al.  Minimally Invasive Colorectal Cancer Surgery in Europe , 2016, Medicine.

[66]  E. Giovannucci,et al.  Lifestyle after Colorectal Cancer Diagnosis in Relation to Survival and Recurrence: A Review of the Literature , 2017, Current Colorectal Cancer Reports.

[67]  M. Hernán,et al.  Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. , 2014, JAMA.

[68]  Jillian T Henderson,et al.  Screening for Ovarian Cancer: Updated Evidence Report and Systematic Review for the US Preventive Services Task Force , 2018, JAMA.

[69]  H. Brenner,et al.  Smoking and survival of colorectal cancer patients: Population‐based study from Germany , 2015, International journal of cancer.

[70]  H. Brenner,et al.  Prevention, early detection, and overdiagnosis of colorectal cancer within 10 years of screening colonoscopy in Germany. , 2015, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[71]  Aung Ko Win,et al.  Rising incidence of early‐onset colorectal cancer in Australia over two decades: Report and review , 2015, Journal of gastroenterology and hepatology.

[72]  Angel Lanas,et al.  Aspirin, cyclooxygenase inhibition and colorectal cancer. , 2014, World journal of gastrointestinal pharmacology and therapeutics.

[73]  M. Hernán,et al.  The NordICC Study: Rationale and design of a randomized trial on colonoscopy screening for colorectal cancer , 2012, Endoscopy.

[74]  I. Kralj-Hans,et al.  Long term effects of once-only flexible sigmoidoscopy screening after 17 years of follow-up: the UK Flexible Sigmoidoscopy Screening randomised controlled trial , 2017, The Lancet.

[75]  M. Bizzarri,et al.  Nicotine increases survival in human colon cancer cells treated with chemotherapeutic drugs. , 2013, Toxicology in vitro : an international journal published in association with BIBRA.

[76]  D. Kerr,et al.  Implications of polygenic risk for personalised colorectal cancer screening. , 2016, Annals of oncology : official journal of the European Society for Medical Oncology.

[77]  A. Jemal,et al.  Colorectal cancer statistics, 2017 , 2017, CA: a cancer journal for clinicians.

[78]  H. Brenner,et al.  Genetic Risk Score Is Associated With Prevalence of Advanced Neoplasms in a Colorectal Cancer Screening Population. , 2018, Gastroenterology.

[79]  H. Brenner,et al.  Physical activity and survival of colorectal cancer patients: Population‐based study from Germany , 2017, International journal of cancer.

[80]  C M Mangham,et al.  Nottingham trial of faecal occult blood testing for colorectal cancer: a 20-year follow-up , 2011, Gut.

[81]  A. Tenesa,et al.  Plasma vitamin D concentration influences survival outcome after a diagnosis of colorectal cancer. , 2014, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[82]  L. Bisanti,et al.  Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial--SCORE. , 2011, Journal of the National Cancer Institute.

[83]  P. Schrotz-King,et al.  Declining Bowel Cancer Incidence and Mortality in Germany. , 2016, Deutsches Arzteblatt international.

[84]  M. Bizzarri,et al.  Nicotine stimulates proliferation and inhibits apoptosis in colon cancer cell lines through activation of survival pathways. , 2012, The Journal of surgical research.

[85]  Aasma Shaukat,et al.  Long-term mortality after screening for colorectal cancer. , 2013, The New England journal of medicine.

[86]  D. Lieberman,et al.  Recommendations on fecal immunochemical testing to screen for colorectal neoplasia: a consensus statement by the US Multi-Society Task Force on colorectal cancer. , 2017, Gastrointestinal endoscopy.

[87]  J. Meyerhardt,et al.  Role of physical activity and diet after colorectal cancer diagnosis. , 2015, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[88]  Darren R. Brenner,et al.  Epidemiology and biology of physical activity and cancer recurrence , 2017, Journal of Molecular Medicine.

[89]  H. D. de Koning,et al.  The value of models in informing resource allocation in colorectal cancer screening: the case of the Netherlands , 2015, Gut.

[90]  H. Brenner,et al.  Prognostic relevance of prediagnostic weight loss and overweight at diagnosis in patients with colorectal cancer. , 2016, The American journal of clinical nutrition.

[91]  Gretchen A. Stevens,et al.  Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults , 2017, Lancet.

[92]  D. Ransohoff,et al.  Multitarget stool DNA testing for colorectal-cancer screening. , 2014, The New England journal of medicine.

[93]  T. Radivoyevitch,et al.  RE: Colorectal Cancer Incidence Patterns in the United States, 1974-2013. , 2017, Journal of the National Cancer Institute.

[94]  J. Meyerhardt,et al.  Association of Survival With Adherence to the American Cancer Society Nutrition and Physical Activity Guidelines for Cancer Survivors After Colon Cancer Diagnosis: The CALGB 89803/Alliance Trial , 2018, JAMA oncology.

[95]  David Lieberman,et al.  Colorectal Cancer Screening: Recommendations for Physicians and Patients from the U.S. Multi-Society Task Force on Colorectal Cancer , 2017, The American Journal of Gastroenterology.

[96]  Gerhard Jentzsch,et al.  Working group on , 1991 .

[97]  D. Greenwood,et al.  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 , 2017, Annals of oncology : official journal of the European Society for Medical Oncology.

[98]  P. Schrotz-King,et al.  Quantitative fecal immunochemical tests for colorectal cancer screening , 2018, International journal of cancer.

[99]  C. Flowers,et al.  Colorectal cancer screening for average‐risk adults: 2018 guideline update from the American Cancer Society , 2018, CA: a cancer journal for clinicians.

[100]  K. Hidayat,et al.  Body fatness at an early age and risk of colorectal cancer , 2018, International journal of cancer.

[101]  H. Brenner,et al.  Public health impact of colonoscopy use on colorectal cancer mortality in Germany and the United States. , 2018, Gastrointestinal endoscopy.

[102]  J. Hardcastle,et al.  Colorectal cancer , 1993, Europe Against Cancer European Commission Series for General Practitioners.

[103]  P. Schrotz-King,et al.  Neoadjuvant Therapy in Rectal Cancer Patients With Clinical Stage II to III Across European Countries: Variations and Outcomes , 2017, Clinical colorectal cancer.

[104]  E. Kuipers,et al.  Colorectal cancer screening: a global overview of existing programmes , 2015, Gut.

[105]  H. Brenner,et al.  Multitarget stool DNA testing for colorectal-cancer screening. , 2014, The New England journal of medicine.