Факторы риска и канцерогенез колоректального рака

Цель: представить данные о факторах риска и их участии в канцерогенезе колоректального рака.

Основные положения. Колоректальный рак (КРР) занимает третье место в структуре заболеваемости злокачественными опухолями в большинстве стран мира, включая Россию. При этом заболеваемость продолжает расти и в мире, и в России, где КРР составляет 12,2 % в общей онкологической заболеваемости. Остановить рост и добиться существенного снижения заболеваемости КРР возможно только на основе определения доказанных причин и факторов риска КРР и внедрения в систему здравоохранения эффективных мер его профилактики. Обзор включает три раздела исследований: распространение КРР в популяциях и динамика показателей заболеваемости; причины и модифицируемые и немодифицируемые факторы риска КРР; механизмы канцерогенеза КРР. Большинство случаев КРР (90–95 %) носит спорадический характер и в значительной степени обусловлено совокупностью модифицируемых факторов риска окружающей среды и образа жизни, таких как определенные характеристики питания, микробиота кишечника, вес, физическая активность, употребление алкоголя, табакокурение, предопухолевые заболевания ободочной и прямой кишки, уровень знаний о причинах злокачественных новообразований и мерах их профилактики. Предполагается, что около 30 % случаев заболеваний КРР в разной степени обусловлено наследственной предрасположенностью или немодифицируемыми факторами риска, но лишь 5 % всех случаев КРР развиваются на фоне известных наследственных синдромов, которые вызваны определенной герминальной мутацией.

Заключение. Представленные в обзоре данные о доказанных модифицируемых и немодифицируемых факторах риска КРР и механизмах их участия в канцерогенезе злокачественных новообразований толстой или прямой кишки будут способствовать разработке и внедрению в практическое здравоохранение эффективных методов профилактики и снижению заболеваемости КРР.

1. Global Burden of Disease 2019 Cancer Collaboration; Kocarnik J.M., Compton K., Dean F.E., Fu W., Gaw B.L., Harvey J.D., et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability- adjusted life years for 29 cancer groups from 2010 to 2019. JAMA Oncology. 2022;8(3):420–44. DOI: 10.1001/jamaoncol.2021.6987

2. Злокачественные новообразования в России в2021 году (заболеваемость и смертность). Под ред. А.Д. Каприна, В.В. Старинского, А.О. Шахзадовой. М., 2022.

3. Baidoun F., Elshiwy K., Elkeraie Y., Merjaneh Z., Khoudari G., Sarmini M.T., et al. Colorectal cancer epidemiology: Recent trends and impact on outcomes. Curr Drug Targets. 2021;22(9):998–1009. DOI: 10.2174/1389450121999201117115717

4. Наврузов С.Н., Алиева Д.А., Кулмиев Э.Э. Эпидемиология колоректального рака: мировые тенденции, заболеваемость раком ободочной кишки в Республике Узбекистан (2012–2017 гг.). Хирургия и онкология. 2020;10(1):56–63. DOI: 10.17650/2686-9594-2020-10-1-56-63

5. Rad A.H., Aghebati-Maleki L., Kafil H.S., Abbasi A. Molecular mechanisms of postbiotics in colorectal cancer prevention and treatment. Crit Rev Food Sci Nutr. 2021;61(11):1787–803. DOI: 10.1080/10408398.2020.1765310

6. O’Sullivan D.E., Sutherland R.L., Town S., Chow K., Fan J., Forbes N., et al. Risk factors for early-onset colorectal cancer: A systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2022;20(6):1229–40.e5. DOI: 10.1016/j.cgh.2021.01.037

7. Sattler E.C., Syunyaeva Z., Reithmair M., Dempke W., Steinlein O.K. Colorectal cancer risk in families with Birt-Hogg-Dubé syndrome increased. Eur J Cancer. 2021;151:168–74. DOI: 10.1016/j.ejca.2021.04.013

8. Pellat A., Netter J., Perkins G., Cohen R., Coulet F., Parc Y., et al. Lynch syndrome: What is new? Bull Cancer.2019;106(7–8):647–55. (In French). DOI: 10.1016/j.bulcan.2018.10.009

9. Xin J., Du M., Gu D., Jiang K., Wang M., Jin M., et al. Risk assessment for colorectal cancer via polygenic risk score and lifestyle exposure: A large-scale association study of East Asian and European populations. Genome Med. 2023;15(1):4. DOI: 10.1186/s13073-023-01156-9

10. Chen X., Jansen L., Guo F., Hoffmeister M., ChangClaude J., Brenner H. Smoking, genetic predisposition, and colorectal cancer risk. Clin Transl Gastroenterol. 2021;12(3):e00317. DOI: 10.14309/ctg.0000000000000317

11. Keskin H., Wang S.M., Etemadi A., Fan J.H., Dawsey S.M., Abnet C.C., et al. Colorectal cancer in the Linxian China Nutrition Intervention Trial: Risk factors and intervention results. PLoS One. 2021;16(9):e0255322. DOI: 10.1371/journal.pone.0255322

12. Dairi O., Anderson J.C., Butterly L.F. Why is colorectal cancer increasing in younger age groups in the United States? Expert Rev Gastroenterol Hepatol. 2021;15(6):623–32. DOI: 10.1080/17474124.2021.1876561

13. Zhou E., Wang L., Santiago C.N., Nanavati J., Rifkin S., Spence E., et al.; Biofilm Study Consortium. Adult-attained height and colorectal cancer risk: A cohort study, systematic review, and meta-analysis. Cancer Epidemiol Biomarkers Prev. 2022;31(4):783–92. DOI: 10.1158/1055-9965.EPI-21-0398

14. Abar L., Vieira A.R., Aune D., Sobiecki J.G., Vingeliene S., Polemiti E., et al. Height and body fatness and colo- rectal cancer risk: An update of the WCRF-AICR systematic review of published prospective studies. Eur J Nutr. 2018;57(5):1701–20. DOI: 10.1007/s00394-017-1557-1

15. Gu M., Thapa S. Colorectal cancer in the United States and a review of its heterogeneity among Asian American subgroups. Asia Pac J Clin Oncol. 2020;16(4):193–200. DOI: 10.1111/ajco.13324

16. Haverkamp D., Redwood D., Roik E., Vindigni S., Thomas T. Elevated colorectal cancer incidence among American Indian/Alaska Native persons in Alaska compared to other populations worldwide. Int J Circumpolar Health. 2023;82(1):2184749. DOI: 10.1080/22423982.2023.2184749

17. Vulcan A., Ericson U., Manjer J., Ohlsson B. A colorectal cancer diet quality index is inversely associated with colorectal cancer in the Malmö diet and cancer study. Eur J Cancer Prev. 2019;28(6):463–71. DOI: 10.1097/CEJ.0000000000000486

18. Ширлина Н.Г., Стасенко В.Л., Турчанинов Д.В., Сохошко И.А. Питание и пищевые привычки, ассоциированные с риском развития колоректального рака у населения Омского региона: исследование случайконтроль. Эпидемиология и вакцинопрофилактика. 2019;18(1):67–73. DOI: 10.31631/2073-3046-2019-18-1-67-73

19. Alegria-Lertxundi I., Bujanda L., Arroyo-Izaga M. Role of dairy foods, fish, white meat, and eggs in the prevention of colorectal cancer: A systematic review of observational studies in 2018-2022. Nutrients. 2022;14(16):3430. DOI: 10.3390/nu14163430

20. Wu B., Zhou R.L., Ou Q.J., Chen Y.M., Fang Y.J., Zhang C.X. Association of plant-based dietary patterns with the risk of colorectal cancer: A large-scale case-control study. Food Funct. 2022;13(20):10790–801. DOI: 10.1039/d2fo01745h

21. Wang X., Yang D.Y., Yang L.Q., Zhao W.Z., Cai L.Y., Shi H.P. Anthocyanin consumption and risk of colorectal cancer: A meta-analysis of observational studies. J Am Coll Nutr. 2019;38(5):470–7. DOI: 10.1080/07315724.2018.1531084

22. Watling C.Z., Kelly R.K., Murphy N., Gunter M., Piernas C., Bradbury K.E., et al. Prospective analysis reveals associations between carbohydrate intakes, genetic predictors of short-chain fatty acid synthesis, and colorectal cancer risk. Cancer Res. 2023;83(12):2066–76. DOI: 10.1158/0008-5472.CAN-22-3755

23. Lopez-Caleya J.F., Ortega-Valín L., Fernández-Villa T., Delgado-Rodríguez M., Martín-Sánchez V., Molina A.J. The role of calcium and vitamin D dietary intake on risk of colorectal cancer: Systematic review and meta-analysis of case-control studies. Cancer Causes Control. 2022;33(2):167–82. DOI: 10.1007/s10552-021-01512-3

24. Al Rajabi A., Lo Siou G., Akawung A.K., McDonald K., Price T.R., Shen-Tu G., et al. Towards refining World Cancer Research Fund/American Institute for Cancer Research cancer prevention recommendations for red and processed meat intake: Insights from Alberta’s Tomorrow Project cohort. Br J Nutr. 2022;127(4):607–18. DOI: 10.1017/S0007114521001240

25. Yu Y.C., Paragomi P., Jin A., Wang R., Schoen R.E., Koh W.P., et al. Low-carbohydrate diet score and the risk of colorectal cancer: Findings from the Singapore Chinese Health Study. Cancer Epidemiol Biomarkers Prev. 2023;32(6):802–8. DOI: 10.1158/1055-9965.EPI-22-0683

26. Schulpen M., van den Brandt P.A. Mediterranean diet adherence and risk of colorectal cancer: The prospective Netherlands Cohort Study. Eur J Epidemiol. 2020;35(1):25–35. DOI: 10.1007/s10654-019-00549-8

27. Zhong Y., Zhu Y., Li Q., Wang F., Ge X., Zhou G., et al. Association between Mediterranean diet adherence and colo- rectal cancer: A dose-response meta-analysis. Am J Clin Nutr. 2020;111(6):1214–25. DOI: 10.1093/ajcn/nqaa083

28. Li H., Boakye D., Chen X., Hoffmeister M., Brenner H. Association of body mass index with risk of early-onset colo- rectal cancer: Systematic review and meta-analysis. Am J Gastroenterol. 2021;116(11):2173–83. DOI: 10.14309/ajg.0000000000001393

29. Li X., Jansen L., Chang-Claude J., Hoffmeister M., Brenner H. Risk of colorectal cancer associated with lifetime excess weight. JAMA Oncol. 2022;8(5):730–7. DOI: 10.1001/jamaoncol.2022.0064

30. Xie F., You Y., Huang J., Guan C., Chen Z., Fang M., et al. Association between physical activity and digestive-system cancer: An updated systematic review and meta-analysis. J Sport Health Sci. 2021;10(1):4–13. DOI: 10.1016/j.jshs.2020.09.009

31. Dashti S.G., Win A.K., Hardikar S.S., Glombicki S.E., Mallenahalli S., Thirumurthi S., et al. Physical activity and the risk of colorectal cancer in Lynch syndrome. Int J Cancer. 2018;143(9):2250–60. DOI: 10.1002/ijc.31611

32. An S., Park S. Association of physical activity and sedentary behavior with the risk of colorectal cancer. J Korean Med Sci. 2022;37(19):e158. DOI: 10.3346/jkms.2022.37.e158

33. Заридзе Д.Г. Табак — основная причина рака. М.: Изд-во «ИМА-ПРЕСС»; 2012.

34. Wang Y., Yang H., Shen C.J., Ge J.N., Lin J. Association between alcohol consumption and colorectal cancer risk: A case-control study in the Han Chinese population. Eur J Cancer Prev. 2018;27(5):433–7. DOI: 10.1097/CEJ.0000000000000355

35. Park S.Y., Wilkens L.R., Setiawan V.W., Monroe K.R., Haiman C.A., Le Marchand L. Alcohol intake and colo- rectal cancer risk in the multiethnic cohort study. Am J Epidemiol. 2019;188(1):67–76. DOI: 10.1093/aje/kwy208

36. Chen X., Li H., Guo F., Hoffmeister M., Brenner H. Alcohol consumption, polygenic risk score, and early- and late-onset colorectal cancer risk. E Clinical Medicine. 2022;49:101460. DOI: 10.1016/j.eclinm.2022.101460

37. Zhang Z., Bahaji Azami N.L., Liu N., Sun M. Research progress of intestinal microecology in the pathogenesis of colorectal adenoma and carcinogenesis. Technol Cancer Res Treat. 2023;22:15330338221135938. DOI: 10.1177/15330338221135938

38. Lythgoe M.P., Mullish B.H., Frampton A.E., Krell J. Polymorphic microbes: A new emerging hallmark of cancer. Trends Microbiol. 2022;30(12):1131–4. DOI: 10.1016/j.tim.2022.08.004

39. Karpiński T.M., Ożarowski M., Stasiewicz M. Carcinogenic microbiota and its role in colorectal cancer development. Semin Cancer Biol. 2022;86(Pt 3):420–30. DOI: 10.1016/j.semcancer.2022.01.004

40. Villar-Ortega P., Expósito-Ruiz M., Gutiérrez-Soto M., Ruiz-Cabello Jiménez M., Navarro-Marí J.M., Gutiérrez-Fernández J. The association between Fusobacterium nucleatum and cancer colorectal: A systematic review and meta-analysis. Enferm Infecc Microbiol Clin (Engl Ed). 2022;40(5):224–34. DOI: 10.1016/j.eimce.2022.02.007

41. Cuellar-Gómez H., Ocharán-Hernández M.E., Calzada-Mendoza C.C., Comoto-Santacruz D.A. Association of Fusobacterium nucleatum infection and colorectal cancer: A Mexican study. Rev Gastroenterol Mex (Engl Ed). 2022;87(3):277–84. DOI: 10.1016/j.rgmxen.2021.07.001

42. Wang N., Fang J.Y. Fusobacterium nucleatum, a key pathogenic factor and microbial biomarker for colo- rectal cancer. Trends Microbiol. 2023;31(2):159–72. DOI: 10.1016/j.tim.2022.08.010

43. Keum N., Giovannucci E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat Rev Gastroenterol Hepatol. 2019;16(12):713– 32. DOI: 10.1038/s41575-019-0189-8

44. Meyer J., Orci L.A., Combescure C., Balaphas A., Morel P., Buchs N.C., et al. Risk of colorectal cancer in patients with acute diverticulitis: A systematic review and meta-analysis of observational studies. Clin Gastroenterol Hepatol. 2019;17(8):1448–56.e17. DOI: 10.1016/j.cgh.2018.07.031

45. Click B., Pinsky P.F., Hickey T., Doroudi M., Schoen R.E. Association of colonoscopy adenoma findings with long-term colorectal cancer incidence. JAMA. 2018;319(19):2021–31. DOI: 10.1001/jama.2018.5809

46. Wan Q., Zhao R., Xia L., Wu Y., Zhou Y., Wang Y., et al. Inflammatory bowel disease and risk of gastric, small bowel and colorectal cancer: A meta-analysis of 26 observational studies. J Cancer Res Clin Oncol. 2021;147(4):1077–87. DOI: 10.1007/s00432-020-03496-0

47. Fantini M.C., Guadagni I. From inflammation to colitis-associated colorectal cancer in inflammatory bowel disease: Pathogenesis and impact of current therapies. Dig Liver Dis. 2021;53(5):558–65. DOI: 10.1016/j.dld.2021.01.012

48. Li L., Fang Y.J., Abulimiti A., Huang C.Y., Liu K.Y., Chen Y.M., et al. Educational level and colorectal cancer risk: The mediating roles of lifestyle and dietary factors. Eur J Cancer Prev. 2022;31(2):137–44. DOI: 10.1097/CEJ.0000000000000697

49. Tran M.T., Jeong M.B., Nguyen V.V., Sharp M.T., Yu E.P., Yu F., et al. Colorectal cancer beliefs, knowledge, and screening among Filipino, Hmong, and Korean Americans. Cancer. 2018;124 Suppl 7(Suppl 7):1552–9. DOI: 10.1002/cncr.31216

50. Moussallem M., Jreij M., Yeretzian J.S., Asmar M.K., Bou-Orm I.R. Colorectal cancer screening knowledge and uptake in Lebanon: A national survey. Rev Epidemiol Sante Publique. 2022;70(2):67–73. DOI: 10.1016/j.respe.2022.01.128

51. Sweeney-Magee M., Gotay C., Karim M.E., Telford J., Dummer T. Patterns and determinants of adherence to colo- rectal cancer primary and secondary prevention recommendations in the BC Generations Project. Health Promot Chronic Dis Prev Can. 2022;42(2):79–93. DOI: 10.24095/hpcdp.42.2.04

52. Ionescu V.A., Gheorghe G., Bacalbasa N., Chiotoroiu A.L., Diaconu C. Colorectal cancer: From risk factors to oncogenesis. Medicina (Kaunas). 2023;59(9):1646. DOI: 10.3390/medicina59091646

53. Hang D., Shen H. Sex hormone and colorectal cancer: The knowns and unknowns. Cancer Epidemiol Biomarkers Prev. 2021;30(7):1302–4. DOI: 10.1158/1055-9965. EPI-21-0472

54. Koch T., Therming Jørgensen J., Christensen J., Duun-Henriksen A.K., Priskorn L., Kildevaeld Simonsen M., et al. Bilateral oophorectomy and rate of colo- rectal cancer: A prospective cohort study. Int J Cancer. 2022;150(1):38–46. DOI: 10.1002/ijc.33776

55. Li Y., Zhao Y., Gao Y., Li Y., Liu M., Xu N., et al. Age-related macrophage alterations are associated with carcinogenesis of colorectal cancer. Carcinogenesis. 2022;43(11):1039–49. DOI: 10.1093/carcin/bgac088

56. Caramujo-Balseiro S., Faro C., Carvalho L. Metabolic pathways in sporadic colorectal carcinogenesis: A new proposal. Med Hypotheses. 2021;148:110512. DOI: 10.1016/j.mehy.2021.110512

57. Cheng T., Lam A.K., Gopalan V. Diet derived polycyclic aromatic hydrocarbons and its pathogenic roles in colorectal carcinogenesis. Crit Rev Oncol Hematol. 2021;168:103522. DOI: 10.1016/j.critrevonc.2021.103522

58. Kossenas K., Constantinou C. Epidemiology, molecular mechanisms, and clinical trials: An update on research on the association between red meat consumption and colorectal cancer. Curr Nutr Rep. 2021;10(4):435–67. DOI: 10.1007/s13668-021-00377-x

59. Ocvirk S., Wilson A.S., Appolonia C.N., Thomas T.K., O’Keefe S.J.D. Fiber, fat, and colorectal cancer: New insight into modifiable dietary risk factors. Curr Gastroenterol Rep. 2019;21(11):62. DOI: 10.1007/s11894-019-0725-2

60. Bull C.J., Bell J.A., Murphy N., Sanderson E., Davey Smith G., Timpson N.J., et al. Adiposity, metabolites, and colorectal cancer risk: Mendelian randomization study. BMC Med. 2020;18(1):396. DOI: 10.1186/s12916-020-01855-9

61. Ugai T., Väyrynen J.P., Haruki K., Akimoto N., Lau M.C., Zhong R., et al. Smoking and incidence of colorectal cancer subclassified by tumor-associated macrophage infiltrates. J Natl Cancer Inst. 2022;114(1):68– 77. DOI: 10.1093/jnci/djab142

62. Wong C.C., Yu J. Gut microbiota in colorectal cancer development and therapy. Nat Rev Clin Oncol. 2023;20(7):429–52. DOI: 10.1038/s41571-023-00766-x

63. Zheng X., Song J., Yu C., Zhou Z., Liu X., Yu J., et al. Single-cell transcriptomic profiling unravels the adenoma-initiation role of protein tyrosine kinases during colo- rectal tumorigenesis. Signal Transduct Target Ther. 2022;7(1):60. DOI: 10.1038/s41392-022-00881-8

64. Porter R.J., Arends M.J., Churchhouse A.M.D., Din S. Inflammatory bowel disease-associated colorectal cancer: Translational risks from mechanisms to medicines. J Crohns Colitis. 2021;15(12):2131–41. DOI: 10.1093/ecco-jcc/jjab102