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Dietary Calcium and Magnesium, Major Food Sources, and Risk of Type 2 Diabetes in U.S. Black Women

¹ Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts
² Institute for Health Sciences, Vrije Universiteit Amsterdam, the Netherlands
³ Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts
⁴ Channing Laboratory, Harvard Medical School and Brigham and Women’s Hospital, Boston, Massachusetts
⁵ Slone Epidemiology Center, Boston University, Boston, Massachusetts

Address correspondence and reprint requests to Rob M. van Dam, Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115. E-mail: rvandam{at}hsph.harvard.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION RESEARCH DESIGN AND METHODS RESULTS CONCLUSIONS References

 
OBJECTIVE—Inverse associations between magnesium and calcium intakes and risk of type 2 diabetes have been reported for studies in predominantly white populations. We examined magnesium, calcium, and major food sources in relation to type 2 diabetes in African-American women.

RESEARCH DESIGN AND METHODS—This is a prospective cohort study including 41,186 participants of the Black Women’s Health Study without a history of diabetes who completed validated food frequency questionnaires at baseline. During 8 years of follow-up (1995–2003), we documented 1,964 newly diagnosed cases of type 2 diabetes.

RESULTS—The multivariate-adjusted hazard ratio of type 2 diabetes for the highest compared with the lowest quintile of intake was 0.69 (95% CI 0.59–0.81; P trend <0.0001) for dietary magnesium and 0.86 (0.74–1.00; P trend = 0.01) for dietary calcium. After mutual adjustment, the association for calcium disappeared (hazard ratio 1.04 [95% CI 0.88–1.24]; P trend = 0.88), whereas the association for magnesium remained. Daily consumption of low-fat dairy (0.87 [0.76–1.00]; P trend = 0.04) and whole grains (0.69 [0.60–0.79]; P trend <0.0001) were associated with a lower risk of type 2 diabetes compared with a consumption less than once a week. After mutual adjustment, the hazard ratio was 0.81 (0.68–0.97; P trend = 0.02) for magnesium and 0.73 (0.63–0.85; P trend <0.0001) for whole grains.

CONCLUSIONS—These findings indicate that a diet high in magnesium-rich foods, particularly whole grains, is associated with a substantially lower risk of type 2 diabetes in U.S. black women.

	INTRODUCTION

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The prevalence of diabetes is increasing in the U.S. and worldwide (1). It has been estimated that 11% of U.S. blacks aged 20 years have diabetes, which is 60% higher than the prevalence in non-Hispanic whites of similar ages (2). Insight into the relation between dietary factors and risk of type 2 diabetes may contribute to the efforts to prevent this chronic condition. In previous studies in predominantly white populations, higher intakes of magnesium (3–6) and calcium (7) and their major food sources, such as whole grains (6,8–10) and low-fat dairy (11), were associated with a lower risk of type 2 diabetes. It is unclear whether these findings can be extrapolated to blacks. In one U.S. cohort study, serum magnesium concentrations were inversely associated with risk of type 2 diabetes in white, but not in black, participants (12). Possible protective effects of magnesium and calcium intake against the development of type 2 diabetes would be particularly relevant for U.S. blacks, who tend to have a substantially lower intake of these minerals than other U.S. ethnic groups (13,14). We therefore examined the association between magnesium, calcium intake, and major food sources in relation to risk of type 2 diabetes in the prospective Black Women’s Health Study.

	RESEARCH DESIGN AND METHODS

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The Black Women’s Health Study of Boston University and Howard University is a prospective cohort study of 59,000 women who were aged 21–69 years at baseline in 1995. Women were enrolled through questionnaires mailed mainly to subscribers of Essence magazine (a national lifestyle magazine whose readership consists almost entirely of African-American women) (15). Participants were from all parts of the U.S., and the education level was only slightly higher than reported for nationally representative data on African-American women (16). Information has been collected using biennial mailed questionnaires, and response rates have been >80% of the original cohort for each follow-up questionnaire. For the current analysis, baseline exclusions included a history of diabetes (including gestational diabetes), cancer (except nonmelanoma skin cancer), myocardial infarction, or stroke (n = 5,424); current pregnancy (n = 956); and 10 items on the dietary questionnaire left blank or implausible reported total energy intakes (<500 kcal/day or >3,800 kcal/day) (n = 5,967). We also excluded women who did not reach the age of 30 years during follow-up or had diabetes diagnosed before age 30 years during follow-up (as these cases may include a substantial number of women with type 1 diabetes) (n = 2,034) and those that did not complete any follow-up questionnaires (n = 268). In addition, we excluded women with missing values for BMI, calcium intake, or magnesium intake (n = 3,232). A total of 41,186 women remained for the current analysis. The study was approved by the institutional review boards of Boston University and Howard University.

Ascertainment of type 2 diabetes
Diabetes was assessed on each biennial follow-up questionnaire by asking whether the women had been diagnosed with diabetes. The accuracy of self-reports of diabetes was examined using questionnaires filled out by the physicians of a random sample of participants who reported having been diagnosed with diabetes. Of 424 women who were sent release forms asking permission to contact their physicians, 184 returned signed releases. Physician questionnaires were obtained for 141 women and indicated a diagnosis of type 2 diabetes for 134 (95%) women. Of seven other women, two had type 1 diabetes, three had metabolic syndrome, one had steroid-induced diabetes, and one did not have diabetes or related conditions.

Information on diet and potential confounders
Diet was assessed using the 68-item baseline Block food frequency questionnaire that inquired about the consumption of foods and drinks during the previous year (17). Questions included nine response categories ranging from "never to <1 per month" to "2 or more per day" for foods and from "never to <1 per month" to "6 or more per day" for drinks. We calculated whole-grain and dairy consumption by adding the daily number of servings of individual items (whole grains: "dark breads, such as wheat, rye, pumpernickel" ["2 slices"] and "high fiber, bran or granola cereals, shredded wheat" ["1 medium bowl"]; dairy: "whole milk" ["8 ounce glass"], "2% milk" ["8 ounce glass"], "skim milk, 1% milk or buttermilk" ["8 ounce glass"], "milk or cream in coffee or tea" ["1 tablespoon"], "yoghurt" ["8 ounces"], "frozen yoghurt" ["1 scoop"], "ice cream" ["1 scoop or 1/2 cup"], "butter on bread or rolls" ["2 pats"], and "cheeses and cheese spreads not including cottage cheese" ["2 slices or two ounces"]). For milk/cream in coffee, we first divided the number of daily servings by 16 to make the serving size comparable with that for other milk items. Low-fat dairy included reduced-fat milk (2% fat), reduced-fat yogurt, and reduced-fat frozen yogurt, and high-fat dairy included all other dairy items. Yogurt and frozen yogurt were assumed to be high-fat if women indicated that they rarely used a low-fat version of these. Nutrient intakes were calculated using the National Cancer Institute’s DIETSYS software (version 4.01, food database version 3.7c) (18). The dietary questionnaire was validated in 408 cohort members by comparison with one 3-day dietary record and three telephone 24-h recalls (19). The energy-adjusted deattenuated Pearson correlation coefficients for the food frequency data compared with diet records and 24-h recalls were 0.40 and 0.63 for saturated fat, 0.32 and 0.79 for calcium, and 0.57 and 0.67 for fiber, respectively (19).

The baseline questionnaire requested information about age, number of years of school finished, parental history of diabetes, consumption of alcoholic drinks in the past year, cigarette smoking history, average number of hours per week spent on strenuous physical activity in the past year, weight, and height. BMI was calculated as weight in kilograms divided by the square of height in meters.

Statistical analysis
Person-years of exposure were calculated from the year of return of the baseline questionnaire or age 30 for participants who only reached age 30 during follow-up to the year on which the first diagnosis of diabetes was indicated on the questionnaire, the year of the last completed questionnaire, or 2003. Cox proportional hazards regression models using age as the time scale were used to calculate hazard ratios for type 2 diabetes and corresponding 95% CIs comparing categories of dietary intake with the lowest category of dietary intake. Categories for the dietary variables were defined using quintiles or the cutoff points specified on the questionnaires. Some questionnaire categories were combined to avoid small numbers and lack of precision for estimates of association. All hazard ratios were adjusted for age (years) and total energy intake (kilocalories per day). The multivariate hazard ratios were further adjusted for BMI (weight in kilograms divided by the square of height in meters), smoking status (never, past, current <15/day, or current 15/day), strenuous physical activity (0, <1, 1–2, 3–6, or 7 h/week), alcohol consumption (0, 0.1–0.4, 0.5–0.9, 1.0–1.9, or 2 drinks/day), parental history of diabetes (yes/no), education level (<13, 13–15, 16, or 17 years), coffee consumption (none, less than five cups/week, five to six cups/week, one cup/day, two to three cups/day, and four or more cups/day), sugar-sweetened soft drink consumption (none, less than five cups/week, five to six cups/week, one cup/day, or two or more cans/day), and quintiles of processed meat and other red meat consumption. We used baseline (1995) data for all exposure variables and potential confounders. To test for linear trends across categories, we modeled the median of each category of consumption as a continuous variable. Nutrient intakes were adjusted for total energy intake using the residual method (20). We calculated Pearson correlations between dietary intakes with adjustment for total energy intake. All reported P values were two tailed, and P values <0.05 were considered statistically significant. All analyses were performed using SAS software, version 8.2 (SAS Institute, Cary, NC).

	RESULTS

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Characteristics of the study population according to dietary magnesium and calcium intakes are shown in Table 1. Women with a higher magnesium intake tended to be older, more highly educated, leaner, more physically active, and nonsmokers. Women with a higher calcium intake tended to be more highly educated, more physically active, and nonsmokers. In addition, higher intakes of magnesium and calcium were associated with higher intakes of fiber, whole grains, dairy, and coffee and lower intakes of alcohol, saturated fat, linoleic acid, red meat, and sugar-sweetened soft drinks. Correlations with dietary magnesium were 0.58 for calcium, 0.25 for dairy, 0.38 for low-fat dairy, –0.08 for high-fat dairy, and 0.54 for whole grains. Correlations with dietary calcium were 0.74 for dairy, 0.73 for low-fat dairy, 0.23 for high-fat dairy, and 0.22 for whole grains.

Higher consumption of whole grains was associated with a lower risk of type 2 diabetes, and this association was independent of other risk factors (Table 3). The inverse association remained after additional adjustment for magnesium intake (hazard ratio 0.73 [95% CI 0.63–0.85] for 1/day vs. <1/week; P trend <0.0001), suggesting that the results for whole grains could not be explained by its contribution to magnesium intake. Dairy consumption was associated with a lower risk of type 2 diabetes, but in multivariate models only an inverse association for low-fat dairy remained (Table 3) that was further weakened after adjustment for magnesium intake (0.90 [0.78–1.03] for 1/day vs. <1/week; P trend = 0.13). The inverse association between magnesium intake and risk of type 2 diabetes remained after adjustment for whole grains (0.81 [0.68–0.97] for highest vs. lowest quintiles; P trend = 0.02) or low-fat dairy (0.72 [0.61–0.84]; P trend <0.0001).

	CONCLUSIONS

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Although African Americans are at increased risk of type 2 diabetes, few studies have examined whether diet may affect diabetes risk in this group (12,21). In the Atherosclerosis Risk in Communities study, low serum magnesium concentrations predicted type 2 diabetes in white, but not in black, participants and no association with dietary magnesium was observed in either group (12). However, serum magnesium concentrations may not accurately reflect magnesium status of other tissues (12). In a cross-sectional study of African Americans without diabetes, higher magnesium intakes were associated with higher insulin sensitivity (22). The low median magnesium intake observed in the current study agrees with that reported for a national sample of African-American women based on 24-h recalls (median 183 mg/day) and is well below the recommended dietary allowance for women aged >30 years (320 mg/day) (13). Effects of poor magnesium status on glucose homeostasis are plausible and may be mediated through oxidative stress, the role of magnesium as cofactor for enzymes involved in glucose metabolism, or the effects of intracellular ion levels on insulin sensitivity and insulin secretion (23). Some short-term intervention studies also provide support for a beneficial effect of magnesium intake on glucose metabolism, but results have not been consistent (24). In the absence of more definitive results on magnesium from larger, longer-term, intervention studies, the recommendation of magnesium-rich foods seems prudent. In adult participants of the National Health and Nutrition Examination Survey 1999–2000, the most important sources of magnesium were vegetables (12.9%), bread and cold cereals (10.7%), and milk (7.5%) (13). In addition to magnesium, many other components of whole grains including fibers, vitamin E, several B vitamins, and lignans may contribute to beneficial effects on glucose metabolism (25).

Dairy consumption was strongly associated with a lower incidence of the metabolic syndrome and hyperglycemia in both white and black participants of the CARDIA study (26). In the current study and a study of male health professionals (11), more modest associations were observed and these associations were limited to low-fat dairy. Calcium intake was inversely associated with risk of type 2 diabetes in female nurses (7). Further studies of calcium and dairy intakes in relation to type 2 diabetes are needed to establish whether effects are independent of other dietary and lifestyle factors.

We controlled for confounding by known risk factors of type 2 diabetes in detail. However, because of the nonrandomized study design, residual confounding cannot be completely excluded as a potential explanation of the observed associations. The assessment of type 2 diabetes relied on self-reports of physician diagnosis. Our validation study indicated that the specificity of self-report was high. Underascertainment of diabetes in the cohort would only have affected hazard ratios if diabetes detection was associated with the studied exposures (27). Measurement error in the assessment of dietary intakes is inevitable and will have led to some misclassification of the studied dietary exposures. We only used dietary intake assessed at baseline, which may have contributed to misclassification because of dietary changes during follow-up. Given the prospective design of the study, this misclassification was unlikely to be associated with the studied outcome and therefore probably led to underestimation of hazard ratios. Furthermore, our results for dietary magnesium and whole grains are consistent with observational data from diverse populations (3–6,8–10) and results of metabolic studies (24,28).

We observed an inverse association between magnesium intake and risk of type 2 diabetes in this cohort of African-American women, whereas no independent association for calcium intake was observed. Because coconstituents of magnesium in foods may contribute to the observed association for magnesium intake, it is not clear whether the results apply to supplemental magnesium intake. These findings indicate that higher consumption of magnesium-rich foods, particularly whole-grain products, is associated with a lower risk of type 2 diabetes in African-American women.

	Acknowledgments

 
This work was supported by National Cancer Institute Grant CA58420 and National Institute of Diabetes and Digestive and Kidney Diseases Grant 1R01DK068738. R.M.V.D. was supported by the Netherlands Organization for Scientific Research (ZonMw VENI Grant no. 916.46.077).

	Footnotes

 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received for publication May 17, 2006. Accepted for publication June 23, 2006.

	References

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1. Wild S, Roglic G, Green A, Sicree R, King H: Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27:1047–1053, 2004[Abstract/Free Full Text]
   
2. Centers for Disease Control and Prevention: National Diabetes Fact Sheet: General Information and National Estimates on Diabetes in the United States, 2002. Atlanta, GA, U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 2003
   
3. Lopez-Ridaura R, Willett WC, Rimm EB, Liu S, Stampfer MJ, Manson JE, Hu FB: Magnesium intake and risk of type 2 diabetes in men and women. Diabetes Care 27:134–140, 2004[Abstract/Free Full Text]
   
4. Song Y, Manson JE, Buring JE, Liu S: Dietary magnesium intake in relation to plasma insulin levels and risk of type 2 diabetes in women. Diabetes Care 27:59–65, 2004[Abstract/Free Full Text]
   
5. Hodge AM, English DR, O’Dea K, Giles GG: Glycemic index and dietary fiber and the risk of type 2 diabetes. Diabetes Care 27:2701–2706, 2004[Abstract/Free Full Text]
   
6. Meyer KA, Kushi LH, Jacobs DRJ, Slavin J, Sellers TA, Folsom AR: Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. Am J Clin Nutr 71:921–930, 2000[Abstract/Free Full Text]
   
7. Pittas AG, Dawson-Hughes B, Li T, Van Dam RM, Willett WC, Manson JE, Hu FB: Vitamin D and calcium intake in relation to type 2 diabetes in women. Diabetes Care 29:650–656, 2006[Abstract/Free Full Text]
   
8. Liu S, Manson JE, Stampfer MJ, Hu FB, Giovannucci E, Colditz GA, Hennekens CH, Willett WC: A prospective study of whole-grain intake and risk of type 2 diabetes mellitus in US women. Am J Public Health 90:1409–1415, 2000[Abstract/Free Full Text]
   
9. Fung TT, Hu FB, Pereira MA, Liu S, Stampfer MJ, Colditz GA, Willett WC: Whole-grain intake and the risk of type 2 diabetes: a prospective study in men. Am J Clin Nutr 76:535–540, 2002[Abstract/Free Full Text]
   
10. Montonen J, Knekt P, Jarvinen R, Aromaa A, Reunanen A: Whole-grain and fiber intake and the incidence of type 2 diabetes. Am J Clin Nutr 77:622–629, 2003[Abstract/Free Full Text]
    
11. 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 165:997–1003, 2005[Abstract/Free Full Text]
    
12. Kao WH, Folsom AR, Nieto FJ, Mo JP, Watson RL, Brancati FL: Serum and dietary magnesium and the risk for type 2 diabetes mellitus: the Atherosclerosis Risk in Communities Study. Arch Intern Med 159:2151–2159, 1999[Abstract/Free Full Text]
    
13. Ford ES, Mokdad AH: Dietary magnesium intake in a national sample of US adults. J Nutr 133:2879–2882, 2003[Abstract/Free Full Text]
    
14. Ford ES: Race, education, and dietary cations: findings from the Third National Health and Nutrition Examination Survey. Ethn Dis 8:10–20, 1998[Medline]
    
15. Rosenberg L, Adams-Campbell L, Palmer JR: The Black Women’s Health Study: a follow-up study for causes and preventions of illness. J Am Med Womens Assoc 50:56–58, 1995
    
16. Adams-Campbell LL, Rosenberg L, Washburn RA, Rao RS, Kim KS, Palmer J: Descriptive epidemiology of physical activity in African-American women. Prev Med 30:43–50, 2000[Medline]
    
17. Block G, Hartman AM, Naughton D: A reduced dietary questionnaire: development and validation. Epidemiology 1:58–64, 1990[Medline]
    
18. Block G, Coyle LM, Hartman AM, Scoppa SM: Revision of dietary analysis software for the Health Habits and History Questionnaire. Am J Epidemiol 139:1190–1196, 1994[Abstract/Free Full Text]
    
19. Kumanyika SK, Mauger D, Mitchell DC, Phillips B, Smiciklas-Wright H, Palmer JR: Relative validity of food frequency questionnaire nutrient estimates in the Black Women’s Health Study. Ann Epidemiol 13:111–118, 2003[Medline]
    
20. Willett W, Stampfer MJ: Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27, 1986[Free Full Text]
    
21. Stevens J, Ahn K, Juhaeri, Houston D, Steffan L, Couper D: Dietary fiber intake and glycemic index and incidence of diabetes in African-American and white adults: the ARIC study. Diabetes Care 25:1715–1721, 2002[Abstract/Free Full Text]
    
22. Humphries S, Kushner H, Falkner B: Low dietary magnesium is associated with insulin resistance in a sample of young, nondiabetic black Americans. Am J Hypertens 12:747–756, 1999[Medline]
    
23. Barbagallo M, Dominguez LJ, Galioto A, Ferlisi A, Cani C, Malfa L, Pineo A, Busardo A, Paolisso G: Role of magnesium in insulin action, diabetes and cardio-metabolic syndrome X. Mol Aspects Med 24:39–52, 2003[Medline]
    
24. de Valk HW: Magnesium in diabetes mellitus. Neth J Med 54:139–146, 1999[Medline]
    
25. Slavin JL, Martini MC, Jacobs DR Jr, Marquart L: Plausible mechanisms for the protectiveness of whole grains. Am J Clin Nutr 70(Suppl. 3):459S–463S, 1999
    
26. 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 287:2081–2089, 2002[Abstract/Free Full Text]
    
27. Rothman K, Greenland S: Precision and validity in epidemiological studies. In Modern Epidemiology. 2nd ed. Rothman K, Greenland S, Eds. Philadelphia, Lippincott-Raven, 1998, p. 115–134
    
28. Pereira MA, Jacobs DR Jr, Pins JJ, Raatz SK, Gross MD, Slavin JL, Seaquist ER: Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr 75:848–855, 2002[Abstract/Free Full Text]
    

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