EPMA Journal

pp 1–13 | Cite as

Colorectal cancer in Saudi Arabia as the proof-of-principle model for implementing strategies of predictive, preventive, and personalized medicine in healthcare

  • Mesnad Alyabsi
  • Abdulrahman Alhumaid
  • Haafiz Allah-Bakhsh
  • Mohammed Alkelya
  • Mohammad Azhar AzizEmail author


Colorectal cancer (CRC) is the most commonly diagnosed cancer among Saudi males and ranks third in females with up to 73% of cases diagnosed at late stage. This review provides an analysis of CRC situation in the Kingdom of Saudi Arabia (KSA) from healthcare perspective. A PUBMED (1986–2018) search was done to identify publications focusing on CRC in KSA. Due to reports of increased CRC incidence among young age group (< 50), and given the young population of KSA, the disease may burden the national healthcare system in the next decades. Environmental factors attributed to increasing incidence rates of CRC include red meat consumption, sedentary lifestyle, and increased calorie intake. Despite substantial investment in healthcare, attention to predictive diagnostics and targeted prevention is lacking. There is a need to develop national screening guidelines based on evidence that supports a reduction in incidence and mortality of CRC when screening is implemented. Future approaches are discussed based on multi-level diagnostics, risk assessment, and population screening programs focused on the needs of young populations that among others present the contents of the advanced approach by predictive, preventive, and personalized medicine. Recommendations are provided that could help to develop policies at regional and national levels. Countries with demographics and lifestyle similar to KSA may gain insights from this review to shape their policies and procedures.


Predictive preventive personalized medicine, colorectal cancer Screening Personalized patient profiling Young population Risk factors Treatment tailored to the person Targeted prevention, healthcare strategy, biomarkers Saudi Arabia 


Author contributions

All authors contributed to this paper with conception and design of the study, literature review and analysis, drafting and critical revision and editing, and final approval of the final version.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

Consent of publication

Not applicable.

Ethical approval

Not applicable.

Core tips

The incidence of CRC is rising at an alarming rate especially in affluent nations, a reflection of the prevalent dietary and lifestyle choices known to be conducive to a variety of colonic diseases. No prior study reviewed current CRC epidemiology in Saudi Arabia. Our objective is to consolidate current research on the epidemiology and prevention of CRC in Saudi Arabia.


  1. 1.
    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.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    World Health Organization, Cancer Country Profile - World Health Organization. 2014.Google Scholar
  3. 3.
    KFSHRC, O.C.R.U., TUMOR REGISTRY ANNUAL REPORT 2014. 2017.Google Scholar
  4. 4.
    Aziz MA, Allah-Bakhsh H. Colorectal cancer: a looming threat, opportunities, and challenges for the Saudi population and its healthcare system. Saudi J Gastroenterol. 2018;24(3):196–7.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Golubnitschaja O, Baban B, Boniolo G, Wang W, Bubnov R, Kapalla M, et al. Medicine in the early twenty-first century: paradigm and anticipation-EPMA position paper 2016. EPMA Journal. 2016;7(1):23.CrossRefPubMedGoogle Scholar
  6. 6.
    Golubnitschaja, O., V. Costigliola, and Epma, General report & recommendations in predictive, preventive and personalised medicine 2012: white paper of the European Association for Predictive, Preventive and Personalised Medicine. EPMA J, 2012. 3(1): p. 14.Google Scholar
  7. 7.
    Ng SW, et al. The prevalence and trends of overweight, obesity and nutrition-related non-communicable diseases in the Arabian Gulf States. Obes Rev. 2011;12(1):1–13.CrossRefPubMedGoogle Scholar
  8. 8.
    The Lancet O. Addressing the burden of cancer in the Gulf. Lancet Oncol. 2014;15(13):1407.CrossRefGoogle Scholar
  9. 9.
    Alsanea N, Abduljabbar AS, Alhomoud S, Ashari LH, Hibbert D, Bazarbashi S. Colorectal cancer in Saudi Arabia: incidence, survival, demographics and implications for national policies. Ann Saudi Med. 2015;35(3):196–202.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Bazarbashi S, Al Eid H, Minguet J. Cancer incidence in Saudi Arabia: 2012 data from the Saudi Cancer Registry. Asian Pac J Cancer Prev. 2017;18(9):2437–44.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Murphy G, Devesa SS, Cross AJ, Inskip PD, McGlynn KA, Cook MB. Sex disparities in colorectal cancer incidence by anatomic subsite, race and age. Int J Cancer. 2011;128(7):1668–75.CrossRefPubMedGoogle Scholar
  12. 12.
    Siegel RL, et al. Colorectal cancer statistics, 2017. CA Cancer J Clin. 2017.Google Scholar
  13. 13.
    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.CrossRefGoogle Scholar
  14. 14.
    Ahnen DJ, Wade SW, Jones WF, Sifri R, Mendoza Silveiras J, Greenamyer J, et al. The increasing incidence of young-onset colorectal cancer: a call to action. Mayo Clin Proc. 2014;89(2):216–24.CrossRefPubMedGoogle Scholar
  15. 15.
    Imperiale TF. The rising prevalence of early-onset colorectal cancer: ready and FIT to tackle? Gastrointest Endosc. 2017;86(5):900–2.CrossRefPubMedGoogle Scholar
  16. 16.
    McKay A, Donaleshen J, Helewa RM, Park J, Wirtzfeld D, Hochman D, et al. Does young age influence the prognosis of colorectal cancer: a population-based analysis. World J Surg Oncol. 2014;12:370.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Guraya SY, Eltinay OE. Higher prevalence in young population and rightward shift of colorectal carcinoma. Saudi Med J. 2006;27(9):1391–3.PubMedGoogle Scholar
  18. 18.
    Bailey CE, Hu CY, You YN, Bednarski BK, Rodriguez-Bigas MA, Skibber JM, et al. Increasing disparities in the age-related incidences of colon and rectal cancers in the United States, 1975-2010. JAMA Surg. 2015;150(1):17–22.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Isbister WH. Colorectal cancer below age 40 in the Kingdom of Saudi Arabia. Aust N Z J Surg. 1992;62(6):468–72.CrossRefPubMedGoogle Scholar
  20. 20.
    Mosli MH, Al-Ahwal MS. Colorectal cancer in the Kingdom of Saudi Arabia: need for screening. Asian Pac J Cancer Prev. 2012;13(8):3809–13.CrossRefPubMedGoogle Scholar
  21. 21.
    O'Connell JB, Maggard MA, Liu JH, Etzioni DA, Livingston EH, Ko CY. Rates of colon and rectal cancers are increasing in young adults. Am Surg. 2003;69(10):866–72.PubMedGoogle Scholar
  22. 22.
    Zahir MN, et al. Clinical features and outcome of sporadic colorectal carcinoma in young patients: a cross-sectional analysis from a developing country. ISRN Oncol. 2014;2014:461570.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Doll R, Payne P, Waterhouse J. Cancer incidence in five continents. 1966. 1966. Berlin Springer CrossRef Google Scholar.Google Scholar
  24. 24.
    Al-Ahmadi K, Al-Zahrani A. NO(2) and cancer incidence in Saudi Arabia. Int J Environ Res Public Health. 2013;10(11):5844–62.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Di Sarsina PR, Tassinari M. Person-centred healthcare and medicine paradigm: it’s time to clarify. EPMA Journal. 2015;6(1):11.CrossRefGoogle Scholar
  26. 26.
    Alamri FA, Saeedi MY, Kassim KA. Dietary and other risk factors for colo-rectal cancer in Saudi Arabia. J Med Med Sci. 2014;5:222–9.CrossRefGoogle Scholar
  27. 27.
    Arafa MA, Farhat K. Colorectal cancer in the Arab world—screening practices and future prospects. Asian Pac J Cancer Prev. 2015;16(17):7425–30.CrossRefPubMedGoogle Scholar
  28. 28.
    Azzeh FS, Alshammari EM, Alazzeh AY, Jazar AS, Dabbour IR, el-Taani HA, et al. Healthy dietary patterns decrease the risk of colorectal cancer in the Mecca Region, Saudi Arabia: a case-control study. BMC Public Health. 2017;17(1):607.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Potter JD. Colorectal cancer: molecules and populations. J Natl Cancer Inst. 1999;91(11):916–32.CrossRefPubMedGoogle Scholar
  30. 30.
    Musaiger AO. Diet and prevention of coronary heart disease in the Arab Middle East countries. Med Princ Pract. 2002;11(Suppl 2):9–16.CrossRefPubMedGoogle Scholar
  31. 31.
    Moradi-Lakeh M, el Bcheraoui C, Afshin A, Daoud F, AlMazroa MA, al Saeedi M, et al. Diet in Saudi Arabia: findings from a nationally representative survey. Public Health Nutr. 2017;20(6):1075–81.CrossRefPubMedGoogle Scholar
  32. 32.
    Organization, W.H., Noncommunicable diseases country profiles 2014. 2014.Google Scholar
  33. 33.
    Terry PD, Miller AB, Rohan TE. Prospective cohort study of cigarette smoking and colorectal cancer risk in women. Int J Cancer. 2002;99(3):480–3.CrossRefPubMedGoogle Scholar
  34. 34.
    Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC, et al. Comparison of risk factors for colon and rectal cancer. Int J Cancer. 2004;108(3):433–42.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Al-Othman S, et al. Tackling cancer control in the gulf cooperation council countries. The Lancet Oncology. 2015;16(5):e246–57.CrossRefPubMedGoogle Scholar
  36. 36.
    Abdulmalik M and Thavorncharoensap M.. Burden of cancer attributable to smoking in Gulf Cooperation Council (GCC) countries. in Proceedings of the International Conference on Applied Science and Health. 2018.Google Scholar
  37. 37.
    Doubeni CA, Major JM, Laiyemo AO, Schootman M, Zauber AG, Hollenbeck AR, et al. Contribution of behavioral risk factors and obesity to socioeconomic differences in colorectal cancer incidence. J Natl Cancer Inst. 2012;104(18):1353–62.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lauby-Secretan B, Scoccianti C, Loomis D, Grosse Y, Bianchini F, Straif K. Body fatness and cancer—viewpoint of the IARC Working Group. N Engl J Med. 2016;375(8):794–8.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Boyle T, Keegel T, Bull F, Heyworth J, Fritschi L. Physical activity and risks of proximal and distal colon cancers: a systematic review and meta-analysis. J Natl Cancer Inst. 2012;104(20):1548–61.CrossRefPubMedGoogle Scholar
  40. 40.
    Song JH, Kim YS, Yang SY, Chung SJ, Park MJ, Lim SH, et al. Physical activity and other lifestyle factors in relation to the prevalence of colorectal adenoma: a colonoscopy-based study in asymptomatic Koreans. Cancer Causes Control. 2013;24(9):1717–26.CrossRefPubMedGoogle Scholar
  41. 41.
    Kruijsen-Jaarsma M, et al. Effects of exercise on immune function in patients with cancer: a systematic review. Exerc Immunol Rev. 2013;19.Google Scholar
  42. 42.
    Zheng Q, Cui G, Chen J, Gao H, Wei Y, Uede T, et al. Regular exercise enhances the immune response against microbial antigens through up-regulation of toll-like receptor signaling pathways. Cell Physiol Biochem. 2015;37(2):735–46.CrossRefPubMedGoogle Scholar
  43. 43.
    Li T, Wei S, Shi Y, Pang S, Qin Q, Yin J, et al. The dose-response effect of physical activity on cancer mortality: findings from 71 prospective cohort studies. Br J Sports Med. 2016;50(6):339–45.CrossRefPubMedGoogle Scholar
  44. 44.
    Al-Daghri NM, et al. Diabetes mellitus type 2 and other chronic non-communicable diseases in the central region, Saudi Arabia (Riyadh cohort 2): a decade of an epidemic. BMC Med. 2011;9(1):76.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Alotaibi A, Perry L, Gholizadeh L, al-Ganmi A. Incidence and prevalence rates of diabetes mellitus in Saudi Arabia: an overview. J Epidemiol Glob Health. 2017;7(4):211–8.CrossRefPubMedGoogle Scholar
  46. 46.
    Alhyas L, McKay A, Majeed A. Prevalence of type 2 diabetes in the States of the co-operation council for the Arab States of the Gulf: a systematic review. PLoS One. 2012;7(8):e40948.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin. 2008;58(3):130–60.CrossRefPubMedGoogle Scholar
  48. 48.
    Winawer SJ, Zauber AG, Ho MN, O'Brien MJ, Gottlieb LS, Sternberg SS, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med. 1993;329(27):1977–81.CrossRefGoogle Scholar
  49. 49.
    Alberts DS, Martínez ME, Roe DJ, Guillén-Rodríguez JM, Marshall JR, van Leeuwen JB, 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. 2000;342(16):1156–62.CrossRefPubMedGoogle Scholar
  50. 50.
    Robertson DJ, Greenberg ER, Beach M, Sandler RS, Ahnen D, Haile RW, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology. 2005;129(1):34–41.CrossRefPubMedGoogle Scholar
  51. 51.
    Zauber AG, Winawer SJ, O'Brien MJ, Lansdorp-Vogelaar I, van Ballegooijen M, Hankey BF, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med. 2012;366(8):687–96.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Lin, J., et al., Screening for colorectal cancer: an updated systematic review for the U.S. Preventive Services Task Force. 2015.Google Scholar
  53. 53.
    Beydoun HA, Beydoun MA. Predictors of colorectal cancer screening behaviors among average-risk older adults in the United States. Cancer Causes Control. 2008;19(4):339–59.CrossRefPubMedGoogle Scholar
  54. 54.
    McLachlan SA, Clements A, Austoker J. Patients’ experiences and reported barriers to colonoscopy in the screening context—a systematic review of the literature. Patient Educ Couns. 2012;86(2):137–46.CrossRefPubMedGoogle Scholar
  55. 55.
    Cole AM, Jackson JE, Doescher M. Urban-rural disparities in colorectal cancer screening: cross-sectional analysis of 1998-2005 data from the Centers for Disease Control’s Behavioral Risk Factor Surveillance Study. Cancer Med. 2012;1(3):350–6.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ananthakrishnan AN, Hoffmann RG, Saeian K. Higher physician density is associated with lower incidence of late-stage colorectal cancer. J Gen Intern Med. 2010;25(11):1164–71.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Mainous AG, et al. The relationship between continuity of care and trust with stage of cancer at diagnosis. Fam Med. 2004;36(1):35–9.PubMedGoogle Scholar
  58. 58.
    Plascak JJ, Fisher JL, Paskett ED. Primary care physician supply, insurance type, and late-stage cancer diagnosis. Am J Prev Med. 2015;48(2):174–8.CrossRefPubMedGoogle Scholar
  59. 59.
    Roetzheim RG, et al. The effects of physician supply on the early detection of colorectal cancer. J Fam Pract. 1999;48(11):850–8.PubMedGoogle Scholar
  60. 60.
    Corkum M, Urquhart R, Kendell C, Burge F, Porter G, Johnston G. Impact of comorbidity and healthcare utilization on colorectal cancer stage at diagnosis: literature review. Cancer Causes Control. 2012;23(2):213–20.CrossRefPubMedGoogle Scholar
  61. 61.
    Bibbins-Domingo K, et al. Screening for colorectal cancer: US Preventive Services Task Force recommendation statement. Jama. 2016;315(23):2564–75.CrossRefPubMedGoogle Scholar
  62. 62.
    Rex DK, Boland RC, Dominitz JA, Giardiello FM, Johnson DA, Kaltenbach T, et al. Colorectal cancer screening: recommendations for physicians and patients from the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol. 2017;112(7):1016–30.CrossRefPubMedGoogle Scholar
  63. 63.
    Provenzale D, Gupta S, Ahnen DJ, Markowitz AJ, Chung DC, Mayer RJ, et al. NCCN guidelines insights: colorectal cancer screening, version 1.2018. J Natl Compr Cancer Netw. 2018;16(8):939–49.CrossRefGoogle Scholar
  64. 64.
    Wolf AM, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J Clin. 2018;68(4):250–81.CrossRefPubMedGoogle Scholar
  65. 65.
    Wilt TJ, Harris RP, Qaseem A. Screening for cancer: advice for high-value care from the American College of Physicians. Ann Intern Med. 2015;162(10):718–25.CrossRefPubMedGoogle Scholar
  66. 66.
    Care, C.T.F.o.P.H., Recommendations on screening for colorectal cancer in primary care. Cmaj, 2016. 188(5): p. 340–348.Google Scholar
  67. 67.
    Benard F, et al. Systematic review of colorectal cancer screening guidelines for average-risk adults: summarizing the current global recommendations. World J Gastroenterol. 2018;24(1):124–38.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Alsanea N, Almadi MA, Abduljabbar AS, Alhomoud S, Alshaban TA, Alsuhaibani A, et al. National guidelines for colorectal cancer screening in Saudi Arabia with strength of recommendations and quality of evidence. Ann Saudi Med. 2015;35(3):189–95.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Sabatino SA, White MC, Thompson TD, Klabunde CN, Centers for Disease Control and Prevention (CDC). Cancer screening test use—United States, 2013. MMWR Morb Mortal Wkly Rep. 2015;64(17):464–8.PubMedPubMedCentralGoogle Scholar
  70. 70.
    USPSTF, Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med, 2008. 149(9): p. 627–637.Google Scholar
  71. 71.
    Davis T, Arnold C, Rademaker A, Bennett C, Bailey S, Platt D, et al. Improving colon cancer screening in community clinics. Cancer. 2013;119(21):3879–86.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Fenton JJ, Elmore JG, Buist DSM, Reid RJ, Tancredi DJ, Baldwin LM. Longitudinal adherence with fecal occult blood test screening in community practice. Ann Fam Med. 2010;8(5):397–401.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Whitlock EP, L.J, Liles E, Beil T, Fu R, O'Connor E, Thompson RN, Cardenas T., Screening for colorectal cancer: an updated systematic review [internet]. 2008.Google Scholar
  74. 74.
    Rodriguez-Bigas MA, Boland CR, Hamilton SR, Henson DE, Srivastava S, Jass JR, et al. A National Cancer Institute workshop on hereditary nonpolyposis colorectal cancer syndrome: meeting highlights and Bethesda guidelines. J Natl Cancer Inst. 1997;89(23):1758–62.CrossRefPubMedGoogle Scholar
  75. 75.
    Vasen HF, et al. New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology. 1999;116(6):1453–6.CrossRefPubMedGoogle Scholar
  76. 76.
    Alqahtani M, Grieu F, Carrello A, Amanuel B, Mashour M, Alattas R, et al. Screening for lynch syndrome in young colorectal cancer patients from Saudi Arabia using microsatellite instability as the initial test. Asian Pac J Cancer Prev. 2016;17(4):1917–23.CrossRefPubMedGoogle Scholar
  77. 77.
    Aljumah AA, Aljebreen AM. Policy of screening for colorectal cancer in Saudi Arabia: a prospective analysis. Saudi J Gastroenterol. 2017;23(3):161–8.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Alhumaid A, AlYousef Z, Bakhsh HA, AlGhamdi S, Aziz MA. Emerging paradigms in the treatment of liver metastases in colorectal cancer. Crit Rev Oncol Hematol. 2018;132:39–50.CrossRefPubMedGoogle Scholar
  79. 79.
    Aziz MA., Chapter 6—colorectal cancer metastasis A2 - Ahmad, Aamir, in Introduction to cancer metastasis. 2017, Academic Press. p. 95–116.Google Scholar
  80. 80.
    Janssens JP, Schuster K, Voss A. Preventive, predictive, and personalized medicine for effective and affordable cancer care. EPMA J. 2018;9(2):113–23.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Lu M, Zhan X. The crucial role of multiomic approach in cancer research and clinically relevant outcomes. EPMA J. 2018;9(1):77–102.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Cheng T, Zhan X. Pattern recognition for predictive, preventive, and personalized medicine in cancer. EPMA J. 2017;8(1):51–60.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Grech G, Zhan X, Yoo BC, Bubnov R, Hagan S, Danesi R, et al. EPMA position paper in cancer: current overview and future perspectives. EPMA J. 2015;6(1):9.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Aziz MA, Yousef Z, Saleh AM, Mohammad S, al Knawy B. Towards personalized medicine of colorectal cancer. Crit Rev Oncol Hematol. 2017;118:70–8.CrossRefPubMedGoogle Scholar
  85. 85.
    Aziz M, et al. Abstract# 2436: microarray analysis of the expression levels of molecular components of relevant signaling pathways in response to FUra/IFN-gamma treatment protocols in human colon carcinoma cell lines. Cancer Res. 2009;69(9 Supplement):2436–6.Google Scholar
  86. 86.
    Aziz M, Hussein M, Gabere M. Filtered selection coupled with support vector machines generate a functionally relevant prediction model for colorectal cancer. OncoTargets and Therapy. 2016;9:3313.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Aziz MA, Periyasamy S, Yousef Z, Deeb A, AlOtaibi M. Colorectal cancer driver genes identified by patient specific comparison of cytogenetic microarray. Genom Data. 2014;2:29–31.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer. 2012;12(4):237–51.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Rashid, M., et al., Molecular classification of colorectal cancer using the gene expression profile of tumor samples. Exp Biol Med (Maywood), 2019: p. 1535370219850788.Google Scholar
  90. 90.
    Abubaker J, Bavi P, al-Harbi S, Ibrahim M, Siraj AK, al-Sanea N, et al. Clinicopathological analysis of colorectal cancers with PIK3CA mutations in Middle Eastern population. Oncogene. 2008;27(25):3539–45.CrossRefPubMedGoogle Scholar
  91. 91.
    Al-Kuraya KS, et al. Colorectal carcinoma from Saudi Arabia. Analysis of MLH-1, MSH-2 and p53 genes by immunohistochemistry and tissue microarray analysis. Saudi medical journal. 2006;27(3):323–8.PubMedGoogle Scholar
  92. 92.
    Al-Kuraya KS. KRAS and TP53 mutations in colorectal carcinoma. Saudi journal of gastroenterology: official journal of the Saudi Gastroenterology Association. 2009;15(4):217–9.CrossRefGoogle Scholar
  93. 93.
    Aldiab A, al Khayal KA, al Obaid OA, Alsheikh A, Alsaleh K, Shahid M, et al. Clinicopathological features and predictive factors for colorectal cancer outcome in the Kingdom of Saudi Arabia. Oncology. 2017;92(2):75–86.CrossRefPubMedGoogle Scholar
  94. 94.
    Bader T, Ismail A. Higher prevalence of KRAS mutations in colorectal cancer in Saudi Arabia: propensity for lung metastasis. Alexandria Journal of Medicine. 2014;50(3):203–9.CrossRefGoogle Scholar
  95. 95.
    Siraj AK, et al. MED12 is recurrently mutated in Middle Eastern colorectal cancer. Gut. 2018;67(4):663–71.PubMedGoogle Scholar
  96. 96.
    Alhadheq AM, et al. The effect of poly(ADP-ribose) polymerase-1 gene 3'untranslated region polymorphism in colorectal cancer risk among Saudi cohort. Dis Markers. 2016;2016:8289293.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Alshammari AH, Shalaby MA, Alanazi MS, Saeed HM. Novel mutations of the PARP-1 gene associated with colorectal cancer in the Saudi population. Asian Pac J Cancer Prev. 2014;15(8):3667–73.CrossRefPubMedGoogle Scholar
  98. 98.
    Aljarbou F, Almousa N, Bazzi M, Aldaihan S, Alanazi M, Alharbi O, et al. The expression of telomere-related proteins and DNA damage response and their association with telomere length in colorectal cancer in Saudi patients. PLoS One. 2018;13(6):e0197154.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Di Leo A, et al. HER2 and TOP2A as predictive markers for anthracycline-containing chemotherapy regimens as adjuvant treatment of breast cancer: a meta-analysis of individual patient data. The lancet oncology. 2011;12(12):1134–42.CrossRefPubMedGoogle Scholar
  100. 100.
    Al Obeed OA, et al., IL-17 and colorectal cancer risk in the Middle East: gene polymorphisms and expression. Cancer Manag Res, 2018. 10: p. 2653.Google Scholar
  101. 101.
    Gonbad RA, et al. Influence of cytokinins in combination with GA(3) on shoot multiplication and elongation of tea clone Iran 100 (Camellia sinensis (L.) O. Kuntze). ScientificWorldJournal. 2014;2014:943054.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Goerlitz D, et al. Genetic polymorphisms in NQO1 and SOD2: interactions with smoking, schistosoma infection, and bladder cancer risk in Egypt. Urol Oncol. 2014;32(1):47 e15–20.CrossRefGoogle Scholar
  103. 103.
    Eldai H, Periyasamy S, al Qarni S, al Rodayyan M, Muhammed Mustafa S, Deeb A, et al. Novel genes associated with colorectal cancer are revealed by high resolution cytogenetic analysis in a patient specific manner. PLoS One. 2013;8(10):e76251.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Naser WM, Shawarby MA, al-Tamimi DM, Seth A, al-Quorain A, Nemer AMA, et al. Novel KRAS gene mutations in sporadic colorectal cancer. PLoS One. 2014;9(11):e113350.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Dadduzio V, Basso M, Rossi S, Cenci T, Capodimonti S, Strippoli A, et al. KRAS exon 2 mutations as prognostic indicators in advanced colorectal cancer in clinical practice: a mono-institutional study. Molecular diagnosis & therapy. 2016;20(1):65–74.CrossRefGoogle Scholar
  106. 106.
    Laé M, Gardrat S, Rondeau S, Richardot C, Caly M, Chemlali W, et al. MED12 mutations in breast phyllodes tumors: evidence of temporal tumoral heterogeneity and identification of associated critical signaling pathways. Oncotarget. 2016;7(51):84428–38.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Arriola E, Marchio C, Tan DSP, Drury SC, Lambros MB, Natrajan R, et al. Genomic analysis of the HER2/TOP2A amplicon in breast cancer and breast cancer cell lines. Lab Investig. 2008;88(5):491–503.CrossRefPubMedGoogle Scholar
  108. 108.
    Al-Sheikh YA, et al. Expression profiling of selected microRNA signatures in plasma and tissues of Saudi colorectal cancer patients by qPCR. Oncol Lett. 2016;11(2):1406–12.CrossRefPubMedGoogle Scholar
  109. 109.
    Tong Z, Yang XO, Yan H, Liu W, Niu X, Shi Y, et al. A protective role by interleukin-17F in colon tumorigenesis. PLoS One. 2012;7(4):e34959.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Omrane I, Marrakchi R, Baroudi O, Mezlini A, Ayari H, Medimegh I, et al. Significant association between interleukin-17A polymorphism and colorectal cancer. Tumor Biol. 2014;35(7):6627–32.CrossRefGoogle Scholar
  111. 111.
    Aziz MA, Periyasamy S, al Yousef Z, AlAbdulkarim I, al Otaibi M, Alfahed A, et al. Integrated exon level expression analysis of driver genes explain their role in colorectal cancer. PLoS One. 2014;9(10):e110134.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Deeb AM, Yousef Z, al-Johani M, Aziz MA. Effect of sampling procedure on the quality control metrics of cytoscan HD array for studying cytogenetic aspects of colorectal cancer. Int J Health Sci (Qassim). 2018;12(4):49–55.Google Scholar
  113. 113.
    Brawley OW. The role of government and regulation in cancer prevention. The Lancet Oncology. 2017;18(8):e483–93.CrossRefPubMedGoogle Scholar
  114. 114.
    Lortet-Tieulent J, Siegel R. Expansion of cancer registration in China. Annals of translational medicine. 2014:2(7).Google Scholar
  115. 115.
    Aziz MA. Precision medicine in colorectal cancer. Saudi J Gastroenterol. 2019;25(2):139–40.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Lievre A, et al. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 2006;66(8):3992–5.CrossRefPubMedGoogle Scholar
  117. 117.
    Wilson PM, Lenz HJ. Integrating biomarkers into clinical decision making for colorectal cancer. Clin Colorectal Cancer. 2010;9(Suppl 1):S16–27.CrossRefPubMedGoogle Scholar
  118. 118.
    Joseph DA, DeGroff AS, Hayes NS, Wong FL, Plescia M. The colorectal cancer control program: partnering to increase population level screening. Gastrointest Endosc. 2011;73(3):429–34.CrossRefPubMedGoogle Scholar
  119. 119.
    Peterson NB, Dwyer KA, Mulvaney SA, Dietrich MS, Rothman RL. The influence of health literacy on colorectal cancer screening knowledge, beliefs and behavior. J Natl Med Assoc. 2007;99(10):1105–12.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Moiel D, Thompson J. Early detection of colon cancer-the kaiser permanente northwest 30-year history: how do we measure success? Is it the test, the number of tests, the stage, or the percentage of screen-detected patients? Perm J. 2011;15(4):30–8.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Potter MB. Strategies and resources to address colorectal cancer screening rates and disparities in the United States and globally. Annu Rev Public Health. 2013;34:413–29.CrossRefPubMedGoogle Scholar

Copyright information

© European Association for Predictive, Preventive and Personalised Medicine (EPMA) 2019

Authors and Affiliations

  1. 1.Population Health Research SectionKing Abdullah International Medical Research CenterRiyadhSaudi Arabia
  2. 2.King Saud bin Abdulaziz University for Health SciencesRiyadhSaudi Arabia
  3. 3.King Faisal Specialist Hospital and Research CenterRiyadhSaudi Arabia
  4. 4.Department of Organ Transplant & Hepatobiliary Surgery, Ministry of National Guard Health AffairsKing Abdullah International Medical Research CenterRiyadhSaudi Arabia
  5. 5.Colorectal Cancer Research Program, Department of Cellular Therapy and Cancer ResearchKing Abdullah International Medical Research CenterRiyadhSaudi Arabia
  6. 6.King Abdulaziz Medical CityMinistry of National Guard Health AffairsRiyadhSaudi Arabia

Personalised recommendations