Yonsei Med J.  2013 May;54(3):626-636. 10.3349/ymj.2013.54.3.626.

Relationship between Milk and Calcium Intake and Lipid Metabolism in Female Patients with Type 2 Diabetes

• Kim J
• Hwang JY
• Kim KN
• Choi YJ
• Chang N
• Huh KB

• KMID: 1727875
• DOI: http://doi.org/10.3349/ymj.2013.54.3.626

Abstract

PURPOSE
This study was conducted to determine the association between intake of milk and dairy products as well as calcium and biomarkers related to lipid metabolism in Korean female patients with type 2 diabetes.
MATERIALS AND METHODS
A cohort of 509 female subjects (mean age: 59.0 years; range: 35-80 years) was recruited from Huh's Diabetes Clinic in Seoul between 2005 and 2010. Dietary intake was assessed using a validated food-frequency questionnaire. Subjects were divided into three groups on the basis of their daily intake of milk and dairy products [<50 g/day (0<50 g/day), 50-200 g/day, and >200 g/day (>200-1201 g/day)] and then further divided into two groups according to their daily calcium intake: below and above the estimated average requirement (EAR).
RESULTS
After adjustment for age, body mass index, energy intake, exercise, use of nutritional supplements and cholesterol medication, the level of serum high-density lipoprotein (HDL)-cholesterol was significantly higher in subjects with milk and dairy products consumption of >200 g/day than in subjects in the other two groups. Those subjects with a milk and dairy products consumption of >200 g/day had significantly higher levels of apolipoprotein A-1 and a significantly lower atherogenic index than the other two groups. Patients with a calcium intake above the EAR exhibited a significantly greater serum HDL-cholesterol level than those with a calcium intake below the EAR.
CONCLUSION
Milk and dairy products, good sources of calcium, play a positive role in lipid profiles in female patients with type 2 diabetes.

Keyword

Milk; dairy products; calcium; dyslipidemias

MeSH Terms

Adult
Aged
Aged, 80 and over
Animals
Apolipoprotein A-I/blood
Biological Markers/metabolism
*Calcium, Dietary
Cholesterol, HDL/blood
Diabetes Mellitus, Type 2/*metabolism
Diet
Female
Humans
*Lipid Metabolism
Middle Aged
*Milk
Apolipoprotein A-I
Biological Markers
Calcium, Dietary
Cholesterol, HDL

Reference

1. Prevention KCfDCa. The second Korea National Health and Nutrition Examination Survey (KNHANES II). 2001. Seoul: The Ministry for Health Welfare and Family Affairs.

2. Prevention KCfDCa. The Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV). 2008. Seoul: The Ministry for Health, Welfare and Family Affairs.

3. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care. 1998. 21:1414–1431.

4. Morrish NJ, Wang SL, Stevens LK, Fuller JH, Keen H. Mortality and causes of death in the WHO Multinational Study of Vascular Disease in Diabetes. Diabetologia. 2001. 44:Suppl 2. S14–S21.

5. Cholesterol Treatment Trialists' (CTT) Collaborators. Kearney PM, Blackwell L, Collins R, Keech A, Simes J, et al. Efficacy of cholesterol-lowering therapy in 18,686 people with diabetes in 14 randomised trials of statins: a meta-analysis. Lancet. 2008. 371:117–125.

6. Lamarche B. Review of the effect of dairy products on non-lipid risk factors for cardiovascular disease. J Am Coll Nutr. 2008. 27:741S–746S.

7. Elwood PC, Givens DI, Beswick AD, Fehily AM, Pickering JE, Gallacher J. The survival advantage of milk and dairy consumption: an overview of evidence from cohort studies of vascular diseases, diabetes and cancer. J Am Coll Nutr. 2008. 27:723S–734S.

8. Tong X, Dong JY, Wu ZW, Li W, Qin LQ. Dairy consumption and risk of type 2 diabetes mellitus: a meta-analysis of cohort studies. Eur J Clin Nutr. 2011. 65:1027–1031.

9. Tremblay A, Gilbert JA. Milk products, insulin resistance syndrome and type 2 diabetes. J Am Coll Nutr. 2009. 28:Suppl 1. 91S–102S.

10. Fumeron F, Lamri A, Abi Khalil C, Jaziri R, Porchay-Baldérelli I, Lantieri O, et al. Dairy consumption and the incidence of hyperglycemia and the metabolic syndrome: results from a french prospective study, Data from the Epidemiological Study on the Insulin Resistance Syndrome (DESIR). Diabetes Care. 2011. 34:813–817.

11. Hu FB, Stampfer MJ, Manson JE, Ascherio A, Colditz GA, Speizer FE, et al. Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women. Am J Clin Nutr. 1999. 70:1001–1008.

12. Soedamah-Muthu SS, Ding EL, Al-Delaimy WK, Hu FB, Engberink MF, Willett WC, et al. Milk and dairy consumption and incidence of cardiovascular diseases and all-cause mortality: dose-response meta-analysis of prospective cohort studies. Am J Clin Nutr. 2011. 93:158–171.

13. Choi HK, Willett WC, Stampfer MJ, Rimm E, Hu FB. Dairy consumption and risk of type 2 diabetes mellitus in men: a prospective study. Arch Intern Med. 2005. 165:997–1003.

14. Pereira MA, Jacobs DR Jr, Van Horn L, Slattery ML, Kartashov AI, Ludwig DS. Dairy consumption, obesity, and the insulin resistance syndrome in young adults: the CARDIA Study. JAMA. 2002. 287:2081–2089.

15. Kwon HT, Lee CM, Park JH, Ko JA, Seong EJ, Park MS, et al. Milk intake and its association with metabolic syndrome in Korean: analysis of the third Korea National Health and Nutrition Examination Survey (KNHANES III). J Korean Med Sci. 2010. 25:1473–1479.

16. Lee SS, Kim SL, Kim SH. An association between milk consumption and serum lipid profiles of postmenopausal women in Korea. Korean J Nutr. 2005. 38:144–150.

17. Høstmark AT, Haug A, Tomten SE, Thelle DS, Mosdøl A. Serum HDL cholesterol was positively associated with cheese intake in the oslo health study. J Food Lipids. 2009. 16:89–102.

18. Rossouw JE, Burger EM, Van der Vyver P, Ferreira JJ. The effect of skim milk, yoghurt, and full cream milk on human serum lipids. Am J Clin Nutr. 1981. 34:351–356.

19. Reid IR, Mason B, Horne A, Ames R, Clearwater J, Bava U, et al. Effects of calcium supplementation on serum lipid concentrations in normal older women: a randomized controlled trial. Am J Med. 2002. 112:343–347.

20. Smedman AE, Gustafsson IB, Berglund LG, Vessby BO. Pentadecanoic acid in serum as a marker for intake of milk fat: relations between intake of milk fat and metabolic risk factors. Am J Clin Nutr. 1999. 69:22–29.

21. Innovation Center for U.S. Dairy. http://www.usdairy.com/DairyResearchInstitute/NHanes/Pages/NHanes.aspx.

22. European Food Safety Authority (efsa). www.efsa.europa.eu/en/datexfooddb/docs.

23. Oh SY KE, Shin MH, Lee SH, Kim JE, Lee HS, et al. Development and validation of food frequency questionnaire for adults. 2007. Seoul: The Korean Society of Health Promotion, Annual Spring Conference.

24. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972. 18:499–502.

25. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: the Muscatine Study. Pediatrics. 1988. 82:309–318.

26. Assmann G, Gotto AM Jr. HDL cholesterol and protective factors in atherosclerosis. Circulation. 2004. 109:23 Suppl 1. III8–III14.

27. Ma KY, Yang N, Jiao R, Peng C, Guan L, Huang Y, et al. Dietary calcium decreases plasma cholesterol by down-regulation of intestinal Niemann-Pick C1 like 1 and microsomal triacylglycerol transport protein and up-regulation of CYP7A1 and ABCG 5/8 in hamsters. Mol Nutr Food Res. 2011. 55:247–258.

28. Bell L, Halstenson CE, Halstenson CJ, Macres M, Keane WF. Cholesterol-lowering effects of calcium carbonate in patients with mild to moderate hypercholesterolemia. Arch Intern Med. 1992. 152:2441–2444.

29. Cho GJ, Park HT, Shin JH, Hur JY, Kim YT, Kim SH, et al. Calcium intake is inversely associated with metabolic syndrome in postmenopausal women: Korea National Health and Nutrition Survey, 2001 and 2005. Menopause. 2009. 16:992–997.

30. Denke MA, Fox MM, Schulte MC. Short-term dietary calcium fortification increases fecal saturated fat content and reduces serum lipids in men. J Nutr. 1993. 123:1047–1053.

31. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V, Akbarian-Moghari A. Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci. 2011. 94:3288–3294.

32. Govers MJ, Van der Meet R. Effects of dietary calcium and phosphate on the intestinal interactions between calcium, phosphate, fatty acids, and bile acids. Gut. 1993. 34:365–370.

33. German JB, Gibson RA, Krauss RM, Nestel P, Lamarche B, van Staveren WA, et al. A reappraisal of the impact of dairy foods and milk fat on cardiovascular disease risk. Eur J Nutr. 2009. 48:191–203.

34. Ohlsson L. Dairy products and plasma cholesterol levels. Food Nutr Res. 2010. 54.

35. Attie AD, Krauss RM, Gray-Keller MP, Brownlie A, Miyazaki M, Kastelein JJ, et al. Relationship between stearoyl-CoA desaturase activity and plasma triglycerides in human and mouse hypertriglyceridemia. J Lipid Res. 2002. 43:1899–1907.

36. Carroll MD, Lacher DA, Sorlie PD, Cleeman JI, Gordon DJ, Wolz M, et al. Trends in serum lipids and lipoproteins of adults, 1960-2002. JAMA. 2005. 294:1773–1781.

37. Ahn HJ, Eom YK, Han KA, Kwon HR, Kim HJ, Park KS, et al. The effects of small sized rice bowl on carbohydrate intake and dietary patterns in women with type 2 diabetes. Korean Diabetes J. 2010. 34:166–173.

38. Reid IR, Ames R, Mason B, Bolland MJ, Bacon CJ, Reid HE, et al. Effects of calcium supplementation on lipids, blood pressure, and body composition in healthy older men: a randomized controlled trial. Am J Clin Nutr. 2010. 91:131–139.

39. Park SK, Park MK, Suk JH, Kim MK, Kim YK, Kim IJ, et al. Cause-of-death trends for diabetes mellitus over 10 years. Korean Diabetes J. 2009. 33:65–72.