Advertisement

Consumption of modern and traditional Moroccan dairy products and colorectal cancer risk: a large case control study

  • Khaoula El KinanyEmail author
  • Meimouna Mint Sidi Deoula
  • Zineb Hatime
  • Hanae Abir Boudouaya
  • Inge Huybrechts
  • Achraf El Asri
  • Abdelatif Benider
  • Mohammed Ahallat
  • Saïd Afqir
  • Nawfel Mellas
  • Mouna Khouchani
  • Karima El Rhazi
Original Contribution

Abstract

Purpose

The main objective of this study is to describe the association between the consumption of either traditional or modern dairy products or calcium intakes and the risk of colorectal cancer (CRC) in the adult Moroccan population.

Methods

A case–control study was conducted in five Moroccan hospital centers. The study was matched on sex, age (± 5 years) and center. Data were collected using validated food frequency questionnaire (FFQ) taking into account different types of Moroccan dairy products. Conditional logistic regression models were used to assess the association between dairy products consumption, calcium intakes and CRC risk subtypes. In all statistical tests, the significance level was set at 0.05.

Results

Among 1453 cases and 1453 matched controls, 50.7% were women and 49.3% were men. Milk ORb 0.84, 95% CI 0.74–0.96 and yogurt ORb 0.74, 95% CI 0.64–0.86 were inversely associated with CRC risk. Similar inverse associations were observed for traditional dairy products namely Lben ORb 0.77, 95% CI 0.67–0.88, Raib ORb 0.86, 95% CI 0.76–0.96 and Jben ORb 0.77, 95% CI 0.67–0.88. The dairy calcium intake was inversely associated to CRC overall ORb 0.83, 95% CI 0.74–0.93.

Conclusions

Our study supports previous international evidence and suggests that individuals who have a high intake of either modern or traditional dairy products are at lower risk for CRC. These findings should be further confirmed by longitudinal data and studies investigating potential pathways involved.

Keywords

Colorectal cancer Dairy products Prevention Morocco 

Notes

Acknowledgements

Many thanks to Lalla Salma Foundation, Prevention and Treatment of Cancers (FLSC) and Moroccan Society of Diseases of the Digestive System (SMMAD) for the financing of this study. Many thanks also to all contributors to this work in the Five University Hospitals centers; the directors of UHCs: Fez (Pr. Ait Taleb K), Casablanca (Pr. Afif My H); Rabat (Pr. Chefchaouni Al Mountacer C); Oujda (Pr Daoudi A); and Marrakech (Pr. Nejmi H). The heads of medical services and their teams: Casablanca (Pr. Benider A; Pr Alaoui R; Pr. Hliwa W; Pr. Badre W, Pr. Bendahou K, Pr. Karkouri M.), Rabat (Pr. Ahallat M; Pr. Errabih I; Pr. El Feydi AE; Pr. Chad B; Pr. Belkouchi A; Pr. Errihani H; Pr. Mrabti H; Pr. Znati K), Fez (Pr. Nejjari C; Pr Ibrahimi SA; Pr. El Abkari M; Pr. Mellas N; Pr. Chbani L; Pr. Benjelloun MC), Oujda (Pr. Ismaili N; Pr. Chraïbi M; Pr. Abda N, Pr. Abbaoui S) and Marrakech (Pr. Khouchani M; Pr. Samlani Z; Pr. Belbaraka R; Pr. Amine M).

Funding

Funding-source funder-id Lalla Salma Foundation, Prevention and Treatment of Cancers (FLSC), award-id N˚06/AP2013.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. 1.
    Arnold M, Sierra MS, Laversanne M et al (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691.  https://doi.org/10.1136/gutjnl-2015-310912 CrossRefGoogle Scholar
  2. 2.
    Bray F, Ferlay J, Soerjomataram I et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin.  https://doi.org/10.3322/caac.21492 Google Scholar
  3. 3.
    Ferlay J, Colombet M, Soerjomataram I et al (2018) Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer.  https://doi.org/10.1002/ijc.31937 Google Scholar
  4. 4.
    Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Akinyemiju TF et al (2018) Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2016: a systematic analysis for the global burden of disease study. JAMA Oncol 4:1553–1568.  https://doi.org/10.1001/jamaoncol.2018.2706 CrossRefGoogle Scholar
  5. 5.
    Steward BW, Christopher P (2014) World Cancer Report 2014. International Agency for Research on cancer, LyonGoogle Scholar
  6. 6.
    Lalla Salma Foundation Prevention (2017) Detection and treatment of cancers. Registry of Greater Casablanca 2008–2012. http://www.contrelecancer.ma/fr/documents/registre-des-cancers-de-la-region-du-grand-casab-2/. Accessed 12 Sept 2018
  7. 7.
    Kamangar F, Dores GM, Anderson WF (2006) Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol 24:2137–2150.  https://doi.org/10.1200/JCO.2005.05.2308 CrossRefGoogle Scholar
  8. 8.
    McMichael AJ, McCall MG, Hartshorne JM, Woodings TL (1980) Patterns of gastro-intestinal cancer in European migrants to Australia: the role of dietary change. Int J Cancer 25:431–437CrossRefGoogle Scholar
  9. 9.
    Haenszel W, Kurihara M (1968) Studies of Japanese migrants. I. Mortality from cancer and other diseases among Japanese in the United States. J Natl Cancer Inst 40:43–68Google Scholar
  10. 10.
    World Cancer Research Fund/American Institute for Cancer Research (2018) Diet, nutrition, physical activity and cancer: a global perspective. Continuous update project expert report. http://dietandcancerreport.org/
  11. 11.
    Vieira AR, Abar L, Chan DSM et al (2017) 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.  https://doi.org/10.1093/annonc/mdx171 CrossRefGoogle Scholar
  12. 12.
    Barrubés L, Babio N, Mena-Sánchez G et al (2018) Dairy product consumption and risk of colorectal cancer in an older mediterranean population at high cardiovascular risk. Int J Cancer 143:1356–1366.  https://doi.org/10.1002/ijc.31540 CrossRefGoogle Scholar
  13. 13.
    Ralston RA, Truby H, Palermo CE, Walker KZ (2014) Colorectal cancer and nonfermented milk, solid cheese, and fermented milk consumption: a systematic review and meta-analysis of prospective studies. Crit Rev Food Sci Nutr 54:1167–1179.  https://doi.org/10.1080/10408398.2011.629353 CrossRefGoogle Scholar
  14. 14.
    Larsson SC, Bergkvist L, Wolk A (2005) High-fat dairy food and conjugated linoleic acid intakes in relation to colorectal cancer incidence in the Swedish Mammography Cohort. Am J Clin Nutr 82:894–900.  https://doi.org/10.1093/ajcn/82.4.894 CrossRefGoogle Scholar
  15. 15.
    Cho E, Smith-Warner SA, Spiegelman D et al (2004) Dairy foods, calcium, and colorectal cancer: a pooled analysis of 10 cohort studies. J Natl Cancer Inst 96:1015–1022CrossRefGoogle Scholar
  16. 16.
    Kesse E, Boutron-Ruault M-C, Norat T et al (2005) Dietary calcium, phosphorus, vitamin D, dairy products and the risk of colorectal adenoma and cancer among French women of the E3 N-EPIC prospective study. Int J Cancer 117:137–144.  https://doi.org/10.1002/ijc.21148 CrossRefGoogle Scholar
  17. 17.
    Sanjoaquin MA, Appleby PN, Thorogood M et al (2004) Nutrition, lifestyle and colorectal cancer incidence: a prospective investigation of 10998 vegetarians and non-vegetarians in the United Kingdom. Br J Cancer 90:118–121.  https://doi.org/10.1038/sj.bjc.6601441 CrossRefGoogle Scholar
  18. 18.
    Pala V, Sieri S, Berrino F et al (2011) Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort. Int J Cancer 129:2712–2719.  https://doi.org/10.1002/ijc.26193 CrossRefGoogle Scholar
  19. 19.
    Tayyem RF, Bawadi HA, Shehadah I et al (2016) Meats, milk and fat consumption in colorectal cancer. J Hum Nutr Diet 29:746–756.  https://doi.org/10.1111/jhn.12391 CrossRefGoogle Scholar
  20. 20.
    El Kinany K, Deoula M, Hatime Z et al (2018) Dairy products and colorectal cancer in middle eastern and north African countries: a systematic review. BMC Cancer 18:233.  https://doi.org/10.1186/s12885-018-4139-6 CrossRefGoogle Scholar
  21. 21.
    FAO (2011) Profil Nutritionnel du Maroc—Division de la nutrition et de la protection des consommateurs. http://www.fao.org/3/a-bc635f.pdf
  22. 22.
    Belahsen R (2014) Nutrition transition and food sustainability. Proc Nutr Soc 73:385–388.  https://doi.org/10.1017/S0029665114000135 CrossRefGoogle Scholar
  23. 23.
    Benjelloun S (2002) Nutrition transition in Morocco. Public Health Nutr 5:135–140.  https://doi.org/10.1079/PHN2001285 CrossRefGoogle Scholar
  24. 24.
    Slama K (1998) Tobacco control and prevention: a guide for low-income countries. IUATLD ((International union against tuberculosis and lung disease)), ParisGoogle Scholar
  25. 25.
    Global Physical Activity Questionnaire (GPAQ). Surveillance and population-based prevention prevention of non communicable diseases. Department World Health Organization, Geneva, Switzerland. https://www.who.int/ncds/surveillance/steps/GPAQ_EN.pdf
  26. 26.
    World Health Organization WHO|Global recommendations on physical activity for health (2019) In: WHO. https://www.who.int/dietphysicalactivity/factsheet_recommendations/en/. Accessed 28 Dec 2018
  27. 27.
    El Kinany K, Garcia-Larsen V, Khalis M et al (2018) Adaptation and validation of a food frequency questionnaire (FFQ) to assess dietary intake in Moroccan adults. Nutr J 17:61.  https://doi.org/10.1186/s12937-018-0368-4 CrossRefGoogle Scholar
  28. 28.
    Garcia-Larsen V, Luczynska M, Kowalski ML et al (2011) Use of a common food frequency questionnaire (FFQ) to assess dietary patterns and their relation to allergy and asthma in Europe: pilot study of the GA2LEN FFQ. Eur J Clin Nutr 65:750–756.  https://doi.org/10.1038/ejcn.2011.15 CrossRefGoogle Scholar
  29. 29.
    El Ati J, Béji C, Farhat A et al (2007) Table de composition des aliments tunisiens. INNTA, TunisGoogle Scholar
  30. 30.
    Neve J (2008) Aliments et préparations typiques de la population Marocaine. http://www.ciriha.org/index.php/publications/outils-dietetique/product/7-aliments-et-preparations-typiques-de-la-population-marocaine. Accessed 3 Jan 2019
  31. 31.
    Tantaoui-Elaraki A, El Marrakchi A (1987) Study of Moroccan dairy products: Iben and smen. Mircen J 3:211–220.  https://doi.org/10.1007/BF00933574 CrossRefGoogle Scholar
  32. 32.
    Mennane Z, Khedid K, Zinedine A et al (2007) Microbial characteristics of Klila and Jben traditional moroccan cheese from raw cow’s milk. World J Dairy Food Sci 2:23–27Google Scholar
  33. 33.
    Hamama A, Bayi M (1991) Composition and microbiological profile of two Moroccan traditional dairy products: raib and jben. Int J Dairy Technol 44:118–120.  https://doi.org/10.1111/j.1471-0307.1991.tb01921.x CrossRefGoogle Scholar
  34. 34.
    Hal F Le Grand Livre de la cuisine marocaine (2019) https://sites.google.com/site/filhalader/le-grand-livre-de-la-cuisine-marocaine-95933791. Accessed 28 Dec 2018
  35. 35.
    Ferrari P, Slimani N, Ciampi A et al (2002) Evaluation of under- and overreporting of energy intake in the 24-hour diet recalls in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr 5:1329–1345.  https://doi.org/10.1079/PHN2002409 CrossRefGoogle Scholar
  36. 36.
    Pearce N (2016) Analysis of matched case-control studies. BMJ 352:i969.  https://doi.org/10.1136/bmj.i969 CrossRefGoogle Scholar
  37. 37.
    Lamprecht SA, Lipkin M (2001) Cellular mechanisms of calcium and vitamin D in the inhibition of colorectal carcinogenesis. Ann N Y Acad Sci 952:73–87CrossRefGoogle Scholar
  38. 38.
    Newmark HL, Wargovich MJ, Bruce WR (1984) Colon cancer and dietary fat, phosphate, and calcium: a hypothesis. J Natl Cancer Inst 72:1323–1325Google Scholar
  39. 39.
    Huncharek M, Muscat J, Kupelnick B (2009) Colorectal cancer risk and dietary intake of calcium, vitamin D, and dairy products: a meta-analysis of 26,335 cases from 60 observational studies. Nutr Cancer 61:47–69.  https://doi.org/10.1080/01635580802395733 CrossRefGoogle Scholar
  40. 40.
    Park Y, Leitzmann MF, Subar AF et al (2009) Dairy food, calcium, and risk of cancer in the NIH-AARP Diet and Health Study. Arch Intern Med 169:391–401.  https://doi.org/10.1001/archinternmed.2008.578 CrossRefGoogle Scholar
  41. 41.
    Cho Y, Turner ND, Davidson LA et al (2014) Colon cancer cell apoptosis is induced by combined exposure to the n-3 fatty acid docosahexaenoic acid and butyrate through promoter methylation. Exp Biol Med (Maywood) 239:302–310.  https://doi.org/10.1177/1535370213514927 CrossRefGoogle Scholar
  42. 42.
    Pala V, Sieri S, Berrino F et al (2011) Yogurt consumption and risk of colorectal cancer in the Italian European prospective investigation into cancer and nutrition cohort. Int J Cancer 129:2712–2719.  https://doi.org/10.1002/ijc.26193 CrossRefGoogle Scholar
  43. 43.
    Iannitti T, Palmieri B (2010) Therapeutical use of probiotic formulations in clinical practice. Clin Nutr 29:701–725.  https://doi.org/10.1016/j.clnu.2010.05.004 CrossRefGoogle Scholar
  44. 44.
    Urbanska AM, Bhathena J, Martoni C, Prakash S (2009) Estimation of the potential antitumor activity of microencapsulated Lactobacillus acidophilus yogurt formulation in the attenuation of tumorigenesis in Apc(Min/+) mice. Dig Dis Sci 54:264–273.  https://doi.org/10.1007/s10620-008-0363-2 CrossRefGoogle Scholar
  45. 45.
    Lidbeck A, Nord CE, Gustafsson JA, Rafter J (1992) Lactobacilli, anticarcinogenic activities and human intestinal microflora. Eur J Cancer Prev 1:341–353CrossRefGoogle Scholar
  46. 46.
    Rao CV, Sanders ME, Indranie C et al (1999) Prevention of colonic preneoplastic lesions by the probiotic Lactobacillus acidophilus NCFMTM in F344 rats. Int J Oncol 14:939–944Google Scholar
  47. 47.
    Benkerroum N (2013) Traditional Fermented Foods of North African Countries: technology and Food Safety Challenges With Regard to Microbiological Risks. Compr Rev Food Sci Food Saf 12:54–89.  https://doi.org/10.1111/j.1541-4337.2012.00215.x CrossRefGoogle Scholar
  48. 48.
    Norat T, Riboli E (2003) Dairy products and colorectal cancer. A review of possible mechanisms and epidemiological evidence. Eur J Clin Nutr 57:1–17.  https://doi.org/10.1038/sj.ejcn.1601522 CrossRefGoogle Scholar
  49. 49.
    Aune D, Lau R, Chan DSM et al (2012) Dairy products and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Ann Oncol 23:37–45.  https://doi.org/10.1093/annonc/mdr269 CrossRefGoogle Scholar
  50. 50.
    Ralston RA, Truby H, Palermo CE, Walker KZ (2014) Colorectal cancer and nonfermented milk, solid cheese, and fermented milk consumption: a systematic review and meta-analysis of prospective studies. Crit Rev Food Sci Nutr 54:1167–1179.  https://doi.org/10.1080/10408398.2011.629353 CrossRefGoogle Scholar
  51. 51.
    Karagianni V, Merikas E, Georgopoulos F et al (2010) Risk factors for colorectal polyps: findings from a Greek case-control study. Rev Med Chir Soc Med Nat Iasi 114:662–670Google Scholar
  52. 52.
    Del Carmen S, de Moreno de LeBlanc A, Levit R et al (2017) Anti-cancer effect of lactic acid bacteria expressing antioxidant enzymes or IL-10 in a colorectal cancer mouse model. Int Immunopharmacol 42:122–129.  https://doi.org/10.1016/j.intimp.2016.11.017 CrossRefGoogle Scholar
  53. 53.
    Lenoir M, Del Carmen S, Cortes-Perez NG et al (2016) Lactobacillus casei BL23 regulates Treg and Th17 T-cell populations and reduces DMH-associated colorectal cancer. J Gastroenterol 51:862–873.  https://doi.org/10.1007/s00535-015-1158-9 CrossRefGoogle Scholar
  54. 54.
    Davoodi H, Esmaeili S, Mortazavian AM (2013) Effects of Milk and Milk Products Consumption on Cancer: a Review. Compr Rev Food Sci Food Saf 12:249–264.  https://doi.org/10.1111/1541-4337.12011 CrossRefGoogle Scholar
  55. 55.
    Keszei AP, Schouten LJ, Goldbohm RA, van den Brandt PA (2010) Dairy intake and the risk of bladder cancer in the Netherlands Cohort Study on Diet and Cancer. Am J Epidemiol 171:436–446.  https://doi.org/10.1093/aje/kwp399 CrossRefGoogle Scholar
  56. 56.
    Balk EM, Adam GP, Langberg VN et al (2017) Global dietary calcium intake among adults: a systematic review. Osteoporos Int 28:3315–3324.  https://doi.org/10.1007/s00198-017-4230-x CrossRefGoogle Scholar
  57. 57.
    Han C, Shin A, Lee J et al (2015) Dietary calcium intake and the risk of colorectal cancer: a case control study. BMC Cancer 15:966.  https://doi.org/10.1186/s12885-015-1963-9 CrossRefGoogle Scholar
  58. 58.
    Murphy N, Norat T, Ferrari P et al (2013) Consumption of dairy products and colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC). PLoS One 8:e72715.  https://doi.org/10.1371/journal.pone.0072715 CrossRefGoogle Scholar
  59. 59.
    Lim LL, Seubsman S, Sleigh A (2009) Validity of self-reported weight, height, and body mass index among university students in Thailand: implications for population studies of obesity in developing countries. Popul Health Met 7:15.  https://doi.org/10.1186/1478-7954-7-15 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Khaoula El Kinany
    • 1
    • 2
    Email author
  • Meimouna Mint Sidi Deoula
    • 1
  • Zineb Hatime
    • 1
  • Hanae Abir Boudouaya
    • 1
  • Inge Huybrechts
    • 3
  • Achraf El Asri
    • 1
  • Abdelatif Benider
    • 4
  • Mohammed Ahallat
    • 5
  • Saïd Afqir
    • 6
  • Nawfel Mellas
    • 7
  • Mouna Khouchani
    • 8
  • Karima El Rhazi
    • 1
  1. 1.Department of Epidemiology and Public Health, Faculty of Medicine and pharmacy of FezSidi Mohamed Ben Abdellah UniversityFèsMorocco
  2. 2.Laboratory of Microbiology and Molecular Biology, Faculty of Science Dhar MehrazFèsMorocco
  3. 3.Nutritional Epidemiology Group (NEP)International Agency for Research on Cancer, World Health OrganizationLyonFrance
  4. 4.Mohammed VI Center for the Treatment of CancersIbn Rochd University Hospital Center CasablancaCasablancaMorocco
  5. 5.Department of Surgery CAvicenne University Hospital CenterRabatMorocco
  6. 6.Medical Oncology DepartmentMohammed VI University Hospital CenterOujdaMorocco
  7. 7.Medical Oncology DepartmentHassan II University Hospital CenterFèsMorocco
  8. 8.Oncology and Radiotherapy DepartmentMohammed VI University Hospital CenterMarrakechMorocco

Personalised recommendations