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Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies

Keum, NaNa, Giovannucci, Edward·2019·Nature Reviews Gastroenterology & Hepatology
DOI 10.1038/s41575-019-0189-8
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Research works printed but not linked: 186

  1. Fleming, M., Ravula, S., Tatishchev, S. F. & Wang, H. L. Colorectal carcinoma: pathologic aspects. J. Gastrointest. Oncol. 3, 153–173 (2012).
  2. Jasperson, K. W., Tuohy, T. M., Neklason, D. W. & Burt, R. W. Hereditary and familial colon cancer. Gastroenterology 138, 2044–2058 (2010). · DOI · Paper page
  3. Graff, R. E. et al. Familial risk and heritability of colorectal cancer in the nordic twin study of cancer. Clin. Gastroenterol. Hepatol. 15, 1256–1264 (2017). · DOI · Paper page
  4. Jiao, S. et al. Estimating the heritability of colorectal cancer. Hum. Mol. Genet. 23, 3898–3905 (2014). · DOI
  5. Brenner, H., Stock, C. & Hoffmeister, M. 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. BMJ 348, g2467 (2014). · DOI · Paper page
  6. Schreuders, E. H. et al. Colorectal cancer screening: a global overview of existing programmes. Gut 64, 1637–1649 (2015). · DOI · Paper page
  7. Center, M. M., Jemal, A. & Ward, E. International trends in colorectal cancer incidence rates. Cancer Epidemiol. Biomarkers Prev. 18, 1688–1694 (2009). · DOI · Paper page
  8. Arnold, M. et al. Global patterns and trends in colorectal cancer incidence and mortality. Gut 66, 683–691 (2017). · DOI · Paper page
  9. Mousavi, S. M., Fallah, M., Sundquist, K. & Hemminki, K. Age- and time-dependent changes in cancer incidence among immigrants to Sweden: colorectal, lung, breast and prostate cancers. Int. J. Cancer 131, E122–E128 (2012). · doi:10.1002/ijc.27334
  10. Wilsnack, R. W., Wilsnack, S. C., Kristjanson, A. F., Vogeltanz-Holm, N. D. & Gmel, G. Gender and alcohol consumption: patterns from the multinational GENACIS project. Addiction 104, 1487–1500 (2009). · DOI · Paper page
  11. Clarke, N., Sharp, L., Osborne, A. & Kearney, P. M. Comparison of uptake of colorectal cancer screening based on fecal immunochemical testing (FIT) in males and females: a systematic review and meta-analysis. Cancer Epidemiol. Biomarkers Prev. 24, 39–47 (2015). · doi:10.1158/1055-9965.epi-14-0774
  12. Murphy, N. et al. A prospective evaluation of endogenous sex hormone levels and colorectal cancer risk in postmenopausal women. J. Natl Cancer. Inst. 107, djv210 (2015). · DOI · Paper page
  13. Augustus, G. J. & Ellis, N. A. Colorectal cancer disparity in african americans: risk factors and carcinogenic mechanisms. Am. J. Pathol. 188, 291–303 (2018). · DOI · Paper page
  14. Ashktorab, H. et al. Identification of novel mutations by exome sequencing in African American colorectal cancer patients. Cancer 121, 34–42 (2015). · DOI
  15. Wang, H. et al. Novel colon cancer susceptibility variants identified from a genome-wide association study in African Americans. Int. J. Cancer 140, 2728–2733 (2017). · doi:10.1002/ijc.30687
  16. Huyghe, J. R. et al. Discovery of common and rare genetic risk variants for colorectal cancer. Nat. Genet. 51, 76–87 (2019). · DOI · Paper page
  17. Ashktorab, H. et al. A meta-analysis of MSI frequency and race in colorectal cancer. Oncotarget 7, 34546–34557 (2016). · DOI
  18. Pawlik, T. M., Raut, C. P. & Rodriguez-Bigas, M. A. Colorectal carcinogenesis: MSI-H versus MSI-L. Dis. Markers 20, 199–206 (2004). · DOI
  19. Guindalini, R. S. et al. Mutation spectrum and risk of colorectal cancer in African American families with Lynch syndrome. Gastroenterology 149, 1446–1453 (2015). · doi:10.1053/j.gastro.2015.07.052
  20. Pitot, H. C. The molecular biology of carcinogenesis. Cancer 72, 962–970 (1993). · DOI · Paper page
  21. Munro, M. J., Wickremesekera, S. K., Peng, L., Tan, S. T. & Itinteang, T. Cancer stem cells in colorectal cancer: a review. J. Clin. Pathol. 71, 110–116 (2018). · DOI · Paper page
  22. Ogino, S. & Goel, A. Molecular classification and correlates in colorectal cancer. J. Mol. Diagn. 10, 13–27 (2008). · DOI · Paper page
  23. Grady, W. M. & Carethers, J. M. Genomic and epigenetic instability in colorectal cancer pathogenesis. Gastroenterology 135, 1079–1099 (2008). · DOI · Paper page
  24. Nazemalhosseini Mojarad, E., Kuppen, P. J., Aghdaei, H. A. & Zali, M. R. The CpG island methylator phenotype (CIMP) in colorectal cancer. Gastroenterol. Hepatol. Bed Bench 6, 120–128 (2013).
  25. Markowitz, S. D. & Bertagnolli, M. M. Molecular origins of cancer: molecular basis of colorectal cancer. N. Engl J. Med. 361, 2449–2460 (2009). · DOI · Paper page
  26. Jia, M., Gao, X., Zhang, Y., Hoffmeister, M. & Brenner, H. Different definitions of CpG island methylator phenotype and outcomes of colorectal cancer: a systematic review. Clin. Epigenetics 8, 25 (2016). · DOI
  27. Funkhouser, W. K. Jr. et al. Relevance, pathogenesis, and testing algorithm for mismatch repair-defective colorectal carcinomas: a report of the association for molecular pathology. J. Mol. Diagn. 14, 91–103 (2012). · DOI · Paper page
  28. Weisenberger, D. J. et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat. Genet. 38, 787–793 (2006). · DOI · Paper page
  29. Conteduca, V., Sansonno, D., Russi, S. & Dammacco, F. Precancerous colorectal lesions (Review). Int. J. Oncol. 43, 973–984 (2013). · DOI
  30. Winawer, S. J. et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology 112, 594–642 (1997). · DOI · Paper page
  31. Brenner, H. et al. Risk of progression of advanced adenomas to colorectal cancer by age and sex: estimates based on 840,149 screening colonoscopies. Gut 56, 1585–1589 (2007). · DOI · Paper page
  32. Strum, W. B. Colorectal adenomas. N. Engl J. Med. 374, 1065–1075 (2016). · DOI · Paper page
  33. East, J. E. et al. British Society of Gastroenterology position statement on serrated polyps in the colon and rectum. Gut 66, 1181–1196 (2017). · DOI · Paper page
  34. Erichsen, R. et al. Increased risk of colorectal cancer development among patients with serrated polyps. Gastroenterology 150, 895–902e5 (2016). · DOI · Paper page
  35. Dow, L. E. et al. Apc restoration promotes cellular differentiation and reestablishes crypt homeostasis in colorectal cancer. Cell 161, 1539–1552 (2015). · DOI · Paper page
  36. Armaghany, T., Wilson, J. D., Chu, Q. & Mills, G. Genetic alterations in colorectal cancer. Gastrointest. Cancer Res. 5, 19–27 (2012).
  37. Pino, M. S. & Chung, D. C. The chromosomal instability pathway in colon cancer. Gastroenterology 138, 2059–2072 (2010). · DOI · Paper page
  38. Leggett, B. & Whitehall, V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 138, 2088–2100 (2010). · DOI · Paper page
  39. Kedrin, D. & Gala, M. K. Genetics of the serrated pathway to colorectal cancer. Clin. Transl Gastroenterol. 6, e84 (2015). · DOI
  40. O’Brien, M. J. et al. Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. Am. J. Surg. Pathol. 30, 1491–1501 (2006). · DOI · Paper page
  41. Kim, K. M. et al. Molecular features of colorectal hyperplastic polyps and sessile serrated adenoma/polyps from Korea. Am. J. Surg. Pathol. 35, 1274–1286 (2011). · DOI
  42. Yang, S., Farraye, F. A., Mack, C., Posnik, O. & O’Brien, M. J. BRAF and KRAS mutations in hyperplastic polyps and serrated adenomas of the colorectum: relationship to histology and CpG island methylation status. Am. J. Surg. Pathol. 28, 1452–1459 (2004). · DOI · Paper page
  43. Itzkowitz, S. H. & Yio, X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G7–G17 (2004). · DOI · Paper page
  44. Buchner, A. M. & Lichtenstein, G. R. Evaluation and detection of dysplasia in IBD: the role of chromoendoscopy and enhanced imaging techniques. Curr. Treat. Options Gastroenterol. 14, 73–82 (2016). · DOI
  45. Robles, A. I. et al. Whole-exome sequencing analyses of inflammatory bowel disease-associated colorectal cancers. Gastroenterology 150, 931–943 (2016). · DOI · Paper page
  46. Triantafillidis, J. K., Nasioulas, G. & Kosmidis, P. A. Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res. 29, 2727–2737 (2009).
  47. Li, F. Y. & Lai, M. D. Colorectal cancer, one entity or three. J. Zhejiang Univ. Sci. B 10, 219–229 (2009). · DOI · Paper page
  48. Murphy, N. et al. Heterogeneity of colorectal cancer risk factors by anatomical subsite in 10 European countries: a multinational cohort study. Clin. Gastroenterol. Hepatol. 17, 1323–1331.e6 (2019). · DOI · Paper page
  49. Wei, E. K. et al. Comparison of risk factors for colon and rectal cancer. Int. J. Cancer 108, 433–442 (2004). · DOI · Paper page
  50. Drewes, J. L., Housseau, F. & Sears, C. L. Sporadic colorectal cancer: microbial contributors to disease prevention, development and therapy. Br. J. Cancer 115, 273–280 (2016). · DOI · Paper page
  51. Yang, L. et al. Proximal shift of colorectal cancer with increasing age in different ethnicities. Cancer Manag. Res. 10, 2663–2673 (2018). · DOI
  52. Murphy, G. et al. Sex disparities in colorectal cancer incidence by anatomic subsite, race and age. Int. J. Cancer 128, 1668–1675 (2011). · DOI · Paper page
  53. Shin, A. et al. Increasing trend of colorectal cancer incidence in Korea, 1999-2009. Cancer Res. Treat. 44, 219–226 (2012). · doi:10.4143/crt.2012.44.4.219
  54. Missiaglia, E. et al. Distal and proximal colon cancers differ in terms of molecular, pathological, and clinical features. Ann. Oncol. 25, 1995–2001 (2014). · DOI · Paper page
  55. Guastadisegni, C., Colafranceschi, M., Ottini, L. & Dogliotti, E. Microsatellite instability as a marker of prognosis and response to therapy: a meta-analysis of colorectal cancer survival data. Eur. J. Cancer 46, 2788–2798 (2010). · DOI · Paper page
  56. Westdorp, H. et al. Opportunities for immunotherapy in microsatellite instable colorectal cancer. Cancer Immunol. Immunother. 65, 1249–1259 (2016). · DOI
  57. Giannakis, M. et al. Genomic correlates of immune-cell infiltrates in colorectal carcinoma. Cell Rep. 15, 857–865 (2016). · DOI · Paper page
  58. Passardi, A., Canale, M., Valgiusti, M. & Ulivi, P. Immune checkpoints as a target for colorectal cancer treatment. Int. J. Mol. Sci. 18, E1324 (2017). · DOI
  59. Jia, M. et al. No association of CpG island methylator phenotype and colorectal cancer survival: population-based study. Br. J. Cancer 115, 1359–1366 (2016). · DOI
  60. Jass, J. R. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 50, 113–130 (2007). · DOI · Paper page
  61. Guinney, J. et al. The consensus molecular subtypes of colorectal cancer. Nat. Med. 21, 1350–1356 (2015). · DOI · Paper page
  62. Alwers, E. et al. Associations between molecular classifications of colorectal cancer and patient survival: a systematic review. Clin. Gastroenterol. Hepatol. 17, 402–410.e2 (2019). · DOI
  63. Butterworth, A. S., Higgins, J. P. & Pharoah, P. Relative and absolute risk of colorectal cancer for individuals with a family history: a meta-analysis. Eur. J. Cancer 42, 216–227 (2006). · DOI · Paper page
  64. Weigl, K. et al. Strongly enhanced colorectal cancer risk stratification by combining family history and genetic risk score. Clin. Epidemiol. 10, 143–152 (2018). · DOI
  65. Rahner, N. & Steinke, V. Hereditary cancer syndromes. Dtsch. Arztebl. Int. 105, 706–714 (2008).
  66. Mork, M. E. et al. High prevalence of hereditary cancer syndromes in adolescents and young adults with colorectal cancer. J. Clin. Oncol. 33, 3544–3549 (2015). · DOI · Paper page
  67. Goodenberger, M. L. et al. PMS2 monoallelic mutation carriers: the known unknown. Genet. Med. 18, 13–19 (2016). · doi:10.1038/gim.2015.27
  68. Win, A. K. et al. Prevalence and penetrance of major genes and polygenes for colorectal cancer. Cancer Epidemiol. Biomarkers Prev. 26, 404–412 (2017). · DOI · Paper page
  69. Lynch, H. T. & de la Chapelle, A. Hereditary colorectal cancer. N. Engl. J. Med. 348, 919–932 (2003). · DOI · Paper page
  70. Lindgren, G., Liljegren, A., Jaramillo, E., Rubio, C. & Lindblom, A. Adenoma prevalence and cancer risk in familial non-polyposis colorectal cancer. Gut 50, 228–234 (2002). · DOI
  71. Jass, J. R. et al. Pathology of hereditary non-polyposis colorectal cancer. Anticancer Res. 14, 1631–1634 (1994).
  72. Half, E., Bercovich, D. & Rozen, P. Familial adenomatous polyposis. Orphanet J. Rare Dis. 4, 22 (2009). · DOI · Paper page
  73. Patel, S. G. & Ahnen, D. J. Familial colon cancer syndromes: an update of a rapidly evolving field. Curr. Gastroenterol. Rep. 14, 428–438 (2012). · DOI
  74. Murphy, C. C. & Singal, A. G. Establishing a research agenda for early-onset colorectal cancer. PLOS Med. 15, e1002577 (2018). · DOI
  75. Pearlman, R. et al. Prevalence and spectrum of germline cancer susceptibility gene mutations among patients with early-onset colorectal cancer. JAMA Oncol. 3, 464–471 (2017). · DOI · Paper page
  76. Crosbie, A. B. et al. Trends in colorectal cancer incidence among younger adults-disparities by age, sex, race, ethnicity, and subsite. Cancer Med. 7, 4077–4086 (2018). · DOI
  77. Ballester, V., Rashtak, S. & Boardman, L. Clinical and molecular features of young-onset colorectal cancer. World J. Gastroenterol. 22, 1736–1744 (2016). · DOI · Paper page
  78. Kim, T. J., Kim, E. R., Hong, S. N., Chang, D. K. & Kim, Y. H. Long-term outcome and prognostic factors of sporadic colorectal cancer in young patients: a large institutional-based retrospective study. Medicine 95, e3641 (2016). · doi:10.1097/md.0000000000003641
  79. Nimptsch, K. & Wu, K. Is timing important? the role of diet and lifestyle during early life on colorectal neoplasia. Curr. Colorectal Cancer Rep. 14, 1–11 (2018). · DOI
  80. Liu, P. H. et al. Association of obesity with risk of early-onset colorectal cancer among women. JAMA Oncol. 5, 37–44 (2019). · DOI · Paper page
  81. Dong, Y. et al. Abdominal obesity and colorectal cancer risk: systematic review and meta-analysis of prospective studies. Biosci. Rep. 37, BSR20170945 (2017). · DOI · Paper page
  82. Kune, G. A. The Melbourne Colorectal Cancer Study: reflections on a 30-year experience. Med. J. Aust. 193, 648–652 (2010). · DOI
  83. Mansournia, M. A. & Altman, D. G. Population attributable fraction. BMJ 360, k757 (2018). · DOI · Paper page
  84. Liang, P. S., Chen, T. Y. & Giovannucci, E. Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int. J. Cancer 124, 2406–2415 (2009). · DOI · Paper page
  85. Song, M. et al. Long-term status and change of body fat distribution, and risk of colorectal cancer: a prospective cohort study. Int. J. Epidemiol. 45, 871–883 (2016). · DOI
  86. Moore, L. L. et al. BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int. J. Obes. Relat. Metab. Disord. 28, 559–567 (2004). · DOI · Paper page
  87. Samaras, K., Botelho, N. K., Chisholm, D. J. & Lord, R. V. Subcutaneous and visceral adipose tissue gene expression of serum adipokines that predict type 2 diabetes. Obesity 18, 884–889 (2010). · DOI · Paper page
  88. Bruun, J. M., Lihn, A. S., Pedersen, S. B. & Richelsen, B. Monocyte chemoattractant protein-1 release is higher in visceral than subcutaneous human adipose tissue (AT): implication of macrophages resident in the AT. J. Clin. Endocrinol. Metab. 90, 2282–2289 (2005). · DOI · Paper page
  89. Park, J., Morley, T. S., Kim, M., Clegg, D. J. & Scherer, P. E. Obesity and cancer–mechanisms underlying tumour progression and recurrence. Nat. Rev. Endocrinol. 10, 455–465 (2014). · DOI · Paper page
  90. Keum, N., Lee, D. H., Kim, R., Greenwood, D. C. & Giovannucci, E. L. Visceral adiposity and colorectal adenomas: dose-response meta-analysis of observational studies. Ann. Oncol. 26, 1101–1109 (2015). · DOI
  91. Lim, U. et al. Asian women have greater abdominal and visceral adiposity than Caucasian women with similar body mass index. Nutr. Diabetes 1, e6 (2011). · DOI · Paper page
  92. Wang, T. et al. Effects of obesity related genetic variations on visceral and subcutaneous fat distribution in a chinese population. Sci. Rep. 6, 20691 (2016). · DOI
  93. Ning, Y., Wang, L. & Giovannucci, E. L. A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies. Obes. Rev. 11, 19–30 (2010). · DOI · Paper page
  94. Kim, H. & Giovannucci, E. L. Sex differences in the association of obesity and colorectal cancer risk. Cancer Causes Control 28, 1–4 (2017). · DOI
  95. Thrift, A. P. et al. Mendelian randomization study of body mass index and colorectal cancer risk. Cancer Epidemiol. Biomarkers Prev. 24, 1024–1031 (2015). · DOI
  96. World Cancer Research Fund/American Institute for Cancer Research. World Cancer Research Fund Internationl Systematic Literature Review: The Associations between Food, Nutrition and Physical Activity and the Risk of Colorectal Cancer, 2017. World Cancer Research Fund https://www.wcrf.org/sites/default/files/colorectal-cancer-slr.pdf (2017).
  97. Rezende, L. F. M. et al. Physical activity and cancer: an umbrella review of the literature including 22 major anatomical sites and 770 000 cancer cases. Br. J. Sports Med. 52, 826–833 (2018). · DOI · Paper page
  98. Ruiz-Casado, A. et al. Exercise and the hallmarks of cancer. Trends Cancer 3, 423–441 (2017). · DOI · Paper page
  99. Giovannucci, E. An integrative approach for deciphering the causal associations of physical activity and cancer risk: the role of adiposity. J. Natl Cancer Inst. 110, 935–941 (2018). · DOI
  100. Ross, R. et al. Exercise-induced reduction in obesity and insulin resistance in women: a randomized controlled trial. Obes. Res. 12, 789–798 (2004). · DOI · Paper page
  101. Keum, N. et al. Association of physical activity by type and intensity with digestive system cancer risk. JAMA Oncol. 2, 1146–1153 (2016). · DOI
  102. Schmid, D. & Leitzmann, M. F. Television viewing and time spent sedentary in relation to cancer risk: a meta-analysis. J. Natl Cancer Inst. 106, dju098 (2014). · DOI · Paper page
  103. Ma, P., Yao, Y., Sun, W., Dai, S. & Zhou, C. Daily sedentary time and its association with risk for colorectal cancer in adults: a dose-response meta-analysis of prospective cohort studies. Medicine 96, e7049 (2017). · DOI
  104. Lynch, B. M. Sedentary behavior and cancer: a systematic review of the literature and proposed biological mechanisms. Cancer Epidemiol. Biomarkers Prev. 19, 2691–2709 (2010). · DOI · Paper page
  105. Cespedes, E. M. & Hu, F. B. Dietary patterns: from nutritional epidemiologic analysis to national guidelines. Am. J. Clin. Nutr. 101, 899–900 (2015). · DOI · Paper page
  106. Tabung, F. K., Brown, L. S. & Fung, T. T. Dietary patterns and colorectal cancer risk: a review of 17 years of evidence (2000-2016). Curr. Colorectal Cancer Rep. 13, 440–454 (2017). · DOI
  107. Garcia-Larsen, V. et al. Dietary patterns derived from principal component analysis (PCA) and risk of colorectal cancer: a systematic review and meta-analysis. Eur. J. Clin. Nutr. 73, 366–386 (2019). · DOI
  108. Vieira, A. R. 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. Ann. Oncol. 28, 1788–1802 (2017). · DOI · Paper page
  109. Cascella, M. et al. Dissecting the mechanisms and molecules underlying the potential carcinogenicity of red and processed meat in colorectal cancer (CRC): an overview on the current state of knowledge. Infect. Agent Cancer 13, 3 (2018).
  110. Helmus, D. S., Thompson, C. L., Zelenskiy, S., Tucker, T. C. & Li, L. Red meat-derived heterocyclic amines increase risk of colon cancer: a population-based case-control study. Nutr. Cancer 65, 1141–1150 (2013). · doi:10.1080/01635581.2013.834945
  111. Gamage, S. M. K., Dissabandara, L., Lam, A. K. & Gopalan, V. The role of heme iron molecules derived from red and processed meat in the pathogenesis of colorectal carcinoma. Crit. Rev. Oncol. Hematol. 126, 121–128 (2018). · DOI
  112. Fung, T. T. et al. A dietary pattern that is associated with C-peptide and risk of colorectal cancer in women. Cancer Causes Control 23, 959–965 (2012). · DOI
  113. Tabung, F. K. et al. Association of dietary inflammatory potential with colorectal cancer risk in men and women. JAMA Oncol. 4, 366–373 (2018). · DOI · Paper page
  114. Burkitt, D. P. Epidemiology of cancer of the colon and rectum. Cancer 28, 3–13 (1971). · DOI · Paper page
  115. Holscher, H. D. Dietary fiber and prebiotics and the gastrointestinal microbiota. Gut Microbes 8, 172–184 (2017). · DOI · Paper page
  116. Zeng, H., Lazarova, D. L. & Bordonaro, M. Mechanisms linking dietary fiber, gut microbiota and colon cancer prevention. World J. Gastrointest. Oncol. 6, 41–51 (2014). · DOI · Paper page
  117. Zeng, H., Taussig, D. P., Cheng, W. H., Johnson, L. K. & Hakkak, R. Butyrate inhibits cancerous HCT116 colon cell proliferation but to a lesser extent in noncancerous NCM460 colon cells. Nutrients 9, E25 (2017). · DOI
  118. Shang, F. M. & Liu, H. L. Fusobacterium nucleatum and colorectal cancer: a review. World J. Gastrointest. Oncol. 10, 71–81 (2018). · DOI · Paper page
  119. Aune, D. et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ 343, d6617 (2011). · DOI · Paper page
  120. Kunzmann, A. T. et al. Dietary fiber intake and risk of colorectal cancer and incident and recurrent adenoma in the prostate, lung, colorectal, and ovarian cancer screening trial. Am. J. Clin. Nutr. 102, 881–890 (2015). · DOI · Paper page
  121. Alberts, D. S. et al. Lack of effect of a high-fiber cereal supplement on the recurrence of colorectal adenomas. phoenix colon cancer prevention physicians’ network. N. Engl. J. Med. 342, 1156–1162 (2000). · DOI · Paper page
  122. Choi, Y. J., Myung, S. K. & Lee, J. H. Light alcohol drinking and risk of cancer: a meta-analysis of cohort studies. Cancer Res. Treat. 50, 474–487 (2018). · DOI · Paper page
  123. Cho, E. et al. Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann. Intern. Med. 140, 603–613 (2004). · DOI · Paper page
  124. Salaspuro, M. Microbial metabolism of ethanol and acetaldehyde and clinical consequences. Addict. Biol. 2, 35–46 (1997). · DOI
  125. Seitz, H. K. & Stickel, F. Molecular mechanisms of alcohol-mediated carcinogenesis. Nat. Rev. Cancer 7, 599–612 (2007). · DOI · Paper page
  126. Giovannucci, E. Alcohol, one-carbon metabolism, and colorectal cancer: recent insights from molecular studies. J. Nutr. 134, 2475S–2481S (2004). · DOI · Paper page
  127. Chang, J. S., Hsiao, J. R. & Chen, C. H. ALDH2 polymorphism and alcohol-related cancers in Asians: a public health perspective. J. Biomed. Sci. 24, 19 (2017). · DOI · Paper page
  128. Li, H. et al. Refined geographic distribution of the oriental ALDH2*504Lys (nee 487Lys) variant. Ann. Hum. Genet. 73, 335–345 (2009). · DOI · Paper page
  129. Mizoue, T. et al. Alcohol drinking and colorectal cancer in Japanese: a pooled analysis of results from five cohort studies. Am. J. Epidemiol. 167, 1397–1406 (2008). · DOI
  130. Zhao, H., Liu, K. J., Lei, Z. D., Lei, S. L. & Tian, Y. Q. Meta-analysis of the aldehyde dehydrogenases-2 (ALDH2) Glu487Lys polymorphism and colorectal cancer risk. PLOS ONE 9, e88656 (2014). · DOI
  131. Giovannucci, E. & Martinez, M. E. Tobacco, colorectal cancer, and adenomas: a review of the evidence. J. Natl Cancer Inst. 88, 1717–1730 (1996). · DOI · Paper page
  132. Limsui, D. et al. Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J. Natl Cancer Inst. 102, 1012–1022 (2010). · DOI · Paper page
  133. Carr, P. R. et al. Lifestyle factors and risk of sporadic colorectal cancer by microsatellite instability status: a systematic review and meta-analyses. Ann. Oncol. 29, 825–834 (2018). · DOI
  134. Figueiredo, J. et al. Smoking-association risks of conventional adenomas and serrated polyps in the colorectum. Cancer Causes Control 26, 377–389 (2015). · DOI
  135. Nishihara, R. et al. A prospective study of duration of smoking cessation and colorectal cancer risk by epigenetics-related tumor classification. Am. J. Epidemiol. 178, 84–100 (2013). · DOI
  136. Bae, J. M., Kim, J. H. & Kang, G. H. Molecular subtypes of colorectal cancer and their clinicopathologic features, with an emphasis on the serrated neoplasia pathway. Arch. Pathol. Lab. Med. 140, 406–412 (2016). · DOI
  137. Rogot, E. & Murray, J. L. Smoking and causes of death among U.S. veterans: 16 years of observation. Public Health Rep. 95, 213–222 (1980).
  138. Heineman, E. F., Zahm, S. H., McLaughlin, J. K. & Vaught, J. B. Increased risk of colorectal cancer among smokers: results of a 26-year follow-up of US veterans and a review. Int. J. Cancer 59, 728–738 (1994). · DOI · Paper page
  139. Lin, J. H. et al. Association between sex hormones and colorectal cancer risk in men and women. Clin. Gastroenterol. Hepatol. 11, 419–424.e1 (2013). · DOI · Paper page
  140. Freeman, E. W., Sammel, M. D., Lin, H. & Gracia, C. R. Obesity and reproductive hormone levels in the transition to menopause. Menopause 17, 718–726 (2010). · DOI · Paper page
  141. Kelly, D. M. & Jones, T. H. Testosterone and obesity. Obes. Rev. 16, 581–606 (2015). · DOI · Paper page
  142. Hillman, E. T., Lu, H., Yao, T. & Nakatsu, C. H. Microbial ecology along the gastrointestinal tract. Microbes Environ. 32, 300–313 (2017). · DOI · Paper page
  143. Flemer, B. et al. Tumour-associated and non-tumour-associated microbiota in colorectal cancer. Gut 66, 633–643 (2017). · DOI · Paper page
  144. Zhang, Y. et al. Changes in gut microbiota and plasma inflammatory factors across the stages of colorectal tumorigenesis: a case-control study. BMC Microbiol. 18, 92 (2018). · DOI
  145. Coker, O. O. et al. Enteric fungal microbiota dysbiosis and ecological alterations in colorectal cancer. Gut 68, 654–662 (2019). · DOI · Paper page
  146. Nakatsu, G. et al. Alterations in enteric virome are associated with colorectal cancer and survival outcomes. Gastroenterology 155, 529–541.e5 (2018). · DOI · Paper page
  147. Cook, N. R., Lee, I. M., Zhang, S. M. M., Moorthy, M. V. & Buring, J. E. Alternate-day, low-dose aspirin and cancer risk: long-term observational follow-up of a randomized trial. Ann. Int. Med. 159, 77–85 (2013). · DOI · Paper page
  148. Giovannucci, E. et al. Aspirin and the risk of colorectal-cancer in women. N. Engl. J. Med. 333, 609–614 (1995). · DOI · Paper page
  149. Cole, B. F. et al. Aspirin for the chemoprevention of colorectal adenomas: meta-analysis of the randomized trials. J. Natl Cancer Inst. 101, 256–266 (2009). · DOI · Paper page
  150. Cao, Y. et al. Population-wide impact of long-term use of aspirin and the risk for cancer. JAMA Oncol. 2, 762–769 (2016). · DOI · Paper page
  151. Zelenay, S. et al. Cyclooxygenase-dependent tumor growth through evasion of immunity. Cell 162, 1257–1270 (2015). · DOI · Paper page
  152. Chan, A. T., Ogino, S. & Fuchs, C. S. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2. N. Engl. J. Med. 356, 2131–2142 (2007). · DOI · Paper page
  153. Cao, Y. et al. Regular aspirin use associates with lower risk of colorectal cancers with low numbers of tumor-infiltrating lymphocytes. Gastroenterology 151, 879–892.e4 (2016). · DOI
  154. Keum, N., Aune, D., Greenwood, D. C., Ju, W. & Giovannucci, E. L. Calcium intake and colorectal cancer risk: dose-response meta-analysis of prospective observational studies. Int. J. Cancer 135, 1940–1948 (2014). · DOI
  155. Bristow, S. M. et al. Calcium supplements and cancer risk: a meta-analysis of randomised controlled trials. Br. J. Nutr. 110, 1384–1393 (2013). · DOI
  156. Wactawski-Wende, J. et al. Calcium plus vitamin D supplementation and the risk of colorectal cancer. N. Engl. J. Med. 354, 684–696 (2006). · DOI · Paper page
  157. Lappe, J. et al. Effect of vitamin D and calcium supplementation on cancer incidence in older women: a randomized clinical trial. JAMA 317, 1234–1243 (2017). · DOI · Paper page
  158. Zhang, X. et al. Calcium intake and colorectal cancer risk: results from the Nurses’ Health Study and Health Professionals Follow-up Study. Int. J. Cancer 139, 2232–2242 (2016). · DOI
  159. Keum, N., Lee, D. H., Greenwood, D. C., Zhang, X. & Giovannucci, E. L. Calcium intake and colorectal adenoma risk: dose-response meta-analysis of prospective observational studies. Int. J. Cancer 136, 1680–1687 (2015). · DOI
  160. Veettil, S. K. et al. Effects of calcium on the incidence of recurrent colorectal adenomas: a systematic review with meta-analysis and trial sequential analysis of randomized controlled trials. Medicine 96, e7661 (2017). · DOI
  161. Lamprecht, S. A. & Lipkin, M. Chemoprevention of colon cancer by calcium, vitamin D and folate: molecular mechanisms. Nat. Rev. Cancer 3, 601–614 (2003). · DOI · Paper page
  162. Tennakoon, S., Aggarwal, A. & Kallay, E. The calcium-sensing receptor and the hallmarks of cancer. Biochim. Biophys. Acta 1863, 1398–1407 (2016). · DOI
  163. Ahearn, T. U., Shaukat, A., Flanders, W. D., Rutherford, R. E. & Bostick, R. M. A randomized clinical trial of the effects of supplemental calcium and vitamin D3 on the APC/β-catenin pathway in the normal mucosa of colorectal adenoma patients. Cancer Prev. Res. 5, 1247–1256 (2012). · DOI
  164. PDQ Screening and Prevention Editorial Board. Colorectal Cancer Screening (PDQ®): Health Professional Version. PDQ Cancer Information Summaries. NIH.gov https://www.ncbi.nlm.nih.gov/books/NBK65825/ (2012).
  165. Wieten, E. et al. Incidence of faecal occult blood test interval cancers in population-based colorectal cancer screening: a systematic review and meta-analysis. Gut 68, 873-881 (2019). · DOI
  166. Brenner, H. & Chen, H. Fecal occult blood versus DNA testing: indirect comparison in a colorectal cancer screening population. Clin. Epidemiol. 9, 377–384 (2017). · DOI
  167. Welch, H. G. & Black, W. C. Overdiagnosis in cancer. J. Natl Cancer Inst. 102, 605–613 (2010). · DOI · Paper page
  168. Lansdorp-Vogelaar, I., Knudsen, A. B. & Brenner, H. Cost-effectiveness of colorectal cancer screening. Epidemiol. Rev. 33, 88–100 (2011). · DOI · Paper page
  169. Tinmouth, J., Lansdorp-Vogelaar, I. & Allison, J. E. Faecal immunochemical tests versus guaiac faecal occult blood tests: what clinicians and colorectal cancer screening programme organisers need to know. Gut 64, 1327–1337 (2015). · DOI · Paper page
  170. Wolf, A. M. D. et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J. Clin. 68, 250–281 (2018). · DOI · Paper page
  171. Inadomi, J. M. et al. Adherence to colorectal cancer screening: a randomized clinical trial of competing strategies. Arch. Intern. Med. 172, 575–582 (2012). · DOI · Paper page
  172. Ebell, M. H., Thai, T. N. & Royalty, K. J. Cancer screening recommendations: an international comparison of high income countries. Public Health Rev. 39, 7 (2018). · DOI · Paper page
  173. Keum, N. & Giovannucci, E. L. Folic acid fortification and colorectal cancer risk. Am. J. Prev. Med. 46, S65–S72 (2014). · DOI
  174. Cokkinides, V., Bandi, P., Shah, M., Virgo, K. & Ward, E. The association between state mandates of colorectal cancer screening coverage and colorectal cancer screening utilization among US adults aged 50 to 64 years with health insurance. BMC Health Serv. Res. 11, 19 (2011). · DOI
  175. James, T. M., Greiner, K. A., Ellerbeck, E. F., Feng, C. & Ahluwalia, J. S. Disparities in colorectal cancer screening: a guideline-based analysis of adherence. Ethn. Dis. 16, 228–233 (2006).
  176. Rex, D. K. et al. Colorectal cancer screening: recommendations for physicians and patients from the U.S. Multi-Society Task Force on Colorectal Cancer. Gastroenterology 153, 307–323 (2017). · DOI · Paper page
  177. Veronese, N. et al. Combined associations of body weight and lifestyle factors with all cause and cause specific mortality in men and women: prospective cohort study. BMJ 355, i5855 (2016). · DOI
  178. Dulai, P. S. et al. Chemoprevention of colorectal cancer in individuals with previous colorectal neoplasia: systematic review and network meta-analysis. BMJ 355, i6188 (2016). · DOI
  179. Cea Soriano, L., Lanas, A., Soriano-Gabarro, M. & Garcia Rodriguez, L. A. Incidence of upper and lower gastrointestinal bleeding in new users of low-dose aspirin. Clin. Gastroenterol. Hepatol. 17, 887-895.e6 (2019). · DOI
  180. Chubak, J., Kamineni, A., Buist, D. S. M., Anderson, M. L. & Whitlock, E. P. Aspirin Use for the Prevention of Colorectal Cancer: An Updated Systematic Evidence Review for the U.S. Preventive Services Task Force (Report No.: 15-05228-EF-1), NIH.gov https://www.ncbi.nlm.nih.gov/books/NBK321661/ (2015).
  181. Drew, D. A. et al. ASPirin Intervention for the REDuction of colorectal cancer risk (ASPIRED): a study protocol for a randomized controlled trial. Trials 18, 50 (2017). · DOI
  182. Han, C. et al. Dietary calcium intake and the risk of colorectal cancer: a case control study. BMC Cancer 15, 966 (2015). · doi:10.1186/s12885-015-1963-9
  183. Shin, A. et al. Dietary intake of calcium, fiber and other micronutrients in relation to colorectal cancer risk: results from the Shanghai Women’s Health Study. Int. J. Cancer 119, 2938–2942 (2006). · DOI
  184. Ishihara, J., Inoue, M., Iwasaki, M., Sasazuki, S. & Tsugane, S. Dietary calcium, vitamin D, and the risk of colorectal cancer. Am. J. Clin. Nutr. 88, 1576–1583 (2008). · DOI
  185. Jones, R. M., Devers, K. J., Kuzel, A. J. & Woolf, S. H. Patient-reported barriers to colorectal cancer screening: a mixed-methods analysis. Am. J. Prev. Med. 38, 508–516 (2010). · DOI · Paper page
  186. Jeon, J. et al. Determining risk of colorectal cancer and starting age of screening based on lifestyle, environmental, and genetic factors. Gastroenterology 154, 2152–2164.e19 (2018). · DOI · Paper page

Cited by

See all 2,661

Metadata

Authors
Keum, N., & Giovannucci, E.
Venue
Nature Reviews Gastroenterology & Hepatology
Publisher
Springer Science and Business Media LLC
Published
2019-08-27
Volume
16
Issue
12
Pages
713-732
ISSN
  • 1759-5045 (ISSN-L)
  • 1759-5053
DOI
10.1038/s41575-019-0189-8
OpenAlex
W2970045605
Cited by
2,661
References
36
FWCI
29.87
Type
journal article
Language
en
Open access
closed
Licence

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CoChat. (2026). Citation check: Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. https://app.cochat.ai/papers/10.1038/s41575-019-0189-8
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Keum, N., & Giovannucci, E. (2019). Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nature Reviews Gastroenterology & Hepatology. https://doi.org/10.1038/s41575-019-0189-8

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