Association between Toenail Magnesium and Type 2 Diabetes in Chinese Adults
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Assessment of Toenail Magnesium
2.3. Outcome Measure
2.4. Other Relevant Variables
2.5. Statistical Analysis
3. Results
3.1. Characteristics of the Participants
3.2. Association of Toenail Magnesium with Type 2 Diabetes
4. Discussion
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Guariguata, L.; Whiting, D.R.; Hambleton, I.; Beagley, J.; Linnenkamp, U.; Shaw, J.E. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res. Clin. Pract. 2014, 103, 137–149. [Google Scholar] [CrossRef] [PubMed]
- Yang, W.; Lu, J.; Weng, J.; Jia, W.; Ji, L.; Xiao, J.; Shan, Z.; Liu, J.; Tian, H.; Ji, Q.; et al. Prevalence of diabetes among men and women in China. N. Engl. J. Med. 2010, 362, 1090–1101. [Google Scholar] [PubMed]
- Xu, Y.; Wang, L.; He, J.; Bi, Y.; Li, M.; Wang, T.; Wang, L.; Jiang, Y.; Dai, M.; Lu, J.; et al. Prevalence and control of diabetes in Chinese adults. JAMA 2013, 310, 948–959. [Google Scholar] [PubMed]
- Weng, J.; Pozzilli, P. Diabetes Metabolism: Research and Reviews—Chinese Diabetes Society special issue: A small but encouraging step toward the successful control of diabetes in China. Diabetes Metab. Res. Rev. 2014, 30, 445–446. [Google Scholar] [CrossRef] [PubMed]
- McEvoy, C.T.; Cardwell, C.R.; Woodside, J.V.; Young, I.S.; Hunter, S.J.; McKinley, M.C. A posteriori dietary patterns are related to risk of type 2 diabetes: Findings from a systematic review and meta-analysis. J. Acad. Nutr. Diet. 2014, 114, 1759–1775. [Google Scholar] [CrossRef] [PubMed]
- Balon, T.W.; Jasman, A.; Scott, S.; Meehan, W.P.; Rude, R.K.; Nadler, J.L. Dietary magnesium prevents fructose-induced insulin insensitivity in rats. Hypertension 1994, 23, 1036–1039. [Google Scholar] [PubMed]
- Balon, T.W.; Gu, J.L.; Tokuyama, Y.; Jasman, A.P.; Nadler, J.L. Magnesium supplementation reduces development of diabetes in a rat model of spontaneous NIDDM. Am. J. Physiol. 1995, 269, E745–E752. [Google Scholar] [PubMed]
- Dong, J.Y.; Xun, P.; He, K.; Qin, L.Q. Magnesium intake and risk of type 2 diabetes: Meta-analysis of prospective cohort studies. Diabetes Care 2011, 34, 2116–2122. [Google Scholar] [PubMed]
- Xu, T.; Chen, G.C.; Zhai, L.; Ke, K.F. Nonlinear Reduction in Risk for Type 2 Diabetes by Magnesium Intake: An Updated Meta-Analysis of Prospective Cohort Studies. Biomed. Environ. Sci. 2015, 28, 527–534. [Google Scholar] [PubMed]
- Larsson, S.C.; Wolk, A. Magnesium intake and risk of type 2 diabetes: A meta-analysis. J. Intern. Med. 2007, 262, 208–214. [Google Scholar] [PubMed]
- Villegas, R.; Gao, Y.T.; Dai, Q.; Yang, G.; Cai, H.; Li, H.; Zheng, W.; Shu, X.O. Dietary calcium and magnesium intakes and the risk of type 2 diabetes: The Shanghai Women’s Health Study. Am. J. Clin. Nutr. 2009, 89, 1059–1067. [Google Scholar] [CrossRef]
- Kirii, K.; Iso, H.; Date, C.; Fukui, M.; Tamakoshi, A.; JACC Study Group. Magnesium intake and risk of self-reported type 2 diabetes among Japanese. J. Am. Coll. Nutr. 2010, 29, 99–106. [Google Scholar] [CrossRef]
- Nanri, A.; Mizoue, T.; Noda, M.; Takahashi, Y.; Kirii, K.; Inoue, M.; Tsugane, S.; Japan Public Health Center-based Prospective Study, Group. Magnesium intake and type II diabetes in Japanese men and women: The Japan Public Health Center-based Prospective Study. Eur. J. Clin. Nutr. 2010, 64, 1244–1247. [Google Scholar] [CrossRef]
- Hata, A.; Doi, Y.; Ninomiya, T.; Mukai, N.; Hirakawa, Y.; Hata, J.; Ozawa, M.; Uchida, K.; Shirota, T.; Kitazono, T.; et al. Magnesium intake decreases type 2 diabetes risk through the improvement of insulin resistance and inflammation: The Hisayama Study. Diabet. Med. J. Br. Diabet. Assoc. 2013, 30, 1487–1494. [Google Scholar] [CrossRef]
- Batis, C.; Mendez, M.A.; Sotres-Alvarez, D.; Gordon-Larsen, P.; Popkin, B. Dietary pattern trajectories during 15 years of follow-up and HbA1c, insulin resistance and diabetes prevalence among Chinese adults. J. Epidemiol. Community Health 2014, 68, 773–779. [Google Scholar] [CrossRef] [PubMed]
- Yan, S.; Li, J.; Li, S.; Zhang, B.; Du, S.; Gordon-Larsen, P.; Adair, L.; Popkin, B. The expanding burden of cardiometabolic risk in China: The China Health and Nutrition Survey. Obes. Rev. 2012, 13, 810–821. [Google Scholar] [CrossRef] [PubMed]
- Zhai, F.Y.; Du, S.F.; Wang, Z.H.; Zhang, J.G.; Du, W.W.; Popkin, B.M. Dynamics of the Chinese diet and the role of urbanicity, 1991–2011. Obes. Rev. 2014, 15, 16–26. [Google Scholar] [CrossRef] [PubMed]
- WHO Expert Committee. Physical Status: The Use and Interpretation of Anthropometry; Report of a WHO Expert Committee; Technical Report Series 854; World Health Organization: Geneva, Switzerland, 1995; pp. 1–452. [Google Scholar]
- Schulze, M.B.; Schulz, M.; Heidemann, C.; Schienkiewitz, A.; Hoffmann, K.; Boeing, H. Fiber and magnesium intake and incidence of type 2 diabetes: A prospective study and meta-analysis. Arch. Intern. Med. 2007, 167, 956–965. [Google Scholar] [CrossRef] [PubMed]
- Kao, W.H.; Folsom, A.R.; Nieto, F.J.; Mo, J.P.; Watson, R.L.; Brancati, F.L. Serum and dietary magnesium and the risk for type 2 diabetes mellitus: The Atherosclerosis Risk in Communities Study. Arch. Intern. Med. 1999, 159, 2151–2159. [Google Scholar] [CrossRef] [PubMed]
- Zhou, M.; Astell-Burt, T.; Bi, Y.; Feng, X.; Jiang, Y.; Li, Y.; Page, A.; Wang, L.; Xu, Y.; Wang, L.; et al. Geographical variation in diabetes prevalence and detection in china: Multilevel spatial analysis of 98,058 adults. Diabetes Care 2015, 38, 72–81. [Google Scholar] [CrossRef] [PubMed]
- Dong, F.; Howard, A.G.; Herring, A.H.; Popkin, B.M.; Gordon-Larsen, P. White Rice Intake Varies in Its Association with Metabolic Markers of Diabetes and Dyslipidemia Across Region among Chinese Adults. Ann. Nutr. Metab. 2015, 66, 209–218. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Hao, G.; Wang, X.; Chen, Z.; Zhang, L.; Guo, M.; Tian, Y.; Shao, L.; Zhu, M. Current prevalence rates of overweight, obesity, central obesity, and related cardiovascular risk factors that clustered among middle-aged population of China. Zhonghua Liu Xing Bing Xue Za Zhi 2014, 35, 354–358. [Google Scholar] [PubMed]
- Reynolds, K.; Gu, D.; Whelton, P.K.; Wu, X.; Duan, X.; Mo, J.; He, J.; Inter, Asia Collaborative Group. Prevalence and risk factors of overweight and obesity in China. Obesity (Silver Spring) 2007, 15, 10–18. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Manson, J.E.; Buring, J.E.; Liu, S. Dietary magnesium intake in relation to plasma insulin levels and risk of type 2 diabetes in women. Diabetes Care 2004, 27, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.J.; Xun, P.; Liu, K.; Loria, C.; Yokota, K.; Jacobs, D.R., Jr.; He, K. Magnesium intake in relation to systemic inflammation, insulin resistance, and the incidence of diabetes. Diabetes Care 2010, 33, 2604–2610. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Oldenburg, B.; Chamberlain, C.; O’Neil, A.; Xue, B.; Jolley, D.; Hall, R.; Dong, Z.; Guo, Y. Diabetes prevalence and determinants in adults in China mainland from 2000 to 2010: A systematic review. Diabetes Res. Clin. Pract. 2012, 98, 226–235. [Google Scholar] [CrossRef] [PubMed]
- Willi, C.; Bodenmann, P.; Ghali, W.A.; Faris, P.D.; Cornuz, J. Active smoking and the risk of type 2 diabetes: A systematic review and meta-analysis. JAMA 2007, 298, 2654–2664. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.; Yu, Z.; Li, H.; Wang, J.; Sun, L.; Qi, Q.; Lin, X. Associations of alcohol consumption with diabetes mellitus and impaired fasting glycemia among middle-aged and elderly Chinese. BMC Public Health 2010, 10, 713. [Google Scholar] [CrossRef] [PubMed]
- Shi, L.; Shu, X.O.; Li, H.; Cai, H.; Liu, Q.; Zheng, W.; Xiang, Y.B.; Villegas, R. Physical activity, smoking, and alcohol consumption in association with incidence of type 2 diabetes among middle-aged and elderly Chinese men. PLoS ONE 2013, 8, e77919. [Google Scholar] [CrossRef] [PubMed]
- Hopping, B.N.; Erber, E.; Grandinetti, A.; Verheus, M.; Kolonel, L.N.; Maskarinec, G. Dietary fiber, magnesium, and glycemic load alter risk of type 2 diabetes in a multiethnic cohort in Hawaii. J. Nutr. 2010, 140, 68–74. [Google Scholar] [CrossRef] [PubMed]
- Pittas, A.G.; Lau, J.; Hu, F.B.; Dawson-Hughes, B. The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 2007, 92, 2017–2029. [Google Scholar] [CrossRef] [PubMed]
- Kobrin, S.M.; Goldfarb, S. Magnesium deficiency. Semin. Nephrol. 1990, 10, 525–535. [Google Scholar] [PubMed]
- Chaudhary, D.P.; Sharma, R.; Bansal, D.D. Implications of magnesium deficiency in type 2 diabetes: A review. Biol. Trace Elem. Res. 2010, 134, 119–129. [Google Scholar] [CrossRef] [PubMed]
- Barbagallo, M.; Dominguez, L.J. Magnesium and type 2 diabetes. World J. Diabetes 2015, 6, 1152–1157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elin, R.J. Laboratory tests for the assessment of magnesium status in humans. Magnes. Trace Elem. 2015, 10, 172–181. [Google Scholar]
- He, K. Trace elements in nails as biomarkers in clinical research. Eur. J. Clin. Investig. 2011, 41, 98–102. [Google Scholar] [CrossRef] [PubMed]
- Garland, M.; Morris, J.S.; Rosner, B.A.; Stampfer, M.J.; Spate, V.L.; Baskett, C.J.; Willett, W.C.; Hunter, D.J. Toenail trace element levels as biomarkers: Reproducibility over a 6-year period. Cancer Epidemiol. Biomark. Prev. 1993, 2, 493–497. [Google Scholar]
- Arnaud, M.J. Update on the assessment of magnesium status. Br. J. Nutr. 2008, 99 (Suppl. 3), S24–S36. [Google Scholar] [CrossRef] [PubMed]
Diabetes | No Diabetes | p | |
---|---|---|---|
N | 429 | 5254 | |
Age (years) | 58.5 ± 11.9 | 50.0 ± 14.4 | <0.001 |
Female (%) | 52.7 | 52.2 | 0.851 |
Urban (%) | 43.4 | 28.4 | <0.001 |
North (%) | 61.5 | 46.2 | <0.001 |
Education (high) (%) | 7.0 | 11.5 | <0.001 |
Current smoker (%) | 26.1 | 28.4 | 0.315 |
Current alcohol drinker (%) | 33.8 | 33.1 | 0.767 |
Tea drinker (%) | 41.3 | 34.3 | 0.026 |
BMI (kg/m2) | 25.7 ± 3.7 | 23.2 ± 3.3 | <0.001 |
Waist circumference (cm) | 90.8 ± 10.1 | 82.3 ± 10.1 | <0.001 |
Toenail magnesium (µg/g) | 263.0 ± 170.9 | 282.3 ± 191.9 | 0.026 |
Serum magnesium (mmol/L) | 0.9 ± 0.1 | 0.9 ± 0.1 | 0.056 |
Dietary intake | |||
Energy (kcal/day) | 2117.9 ± 685.0 | 2205.7 ± 676.1 | 0.010 |
Carbohydrate (% of energy) | 51.2 ± 11.6 | 53.9 ± 11.8 | <0.001 |
Fat (% of energy) | 33.0 ± 10.4 | 31.4 ± 11.8 | 0.002 |
Fiber (g/day) | 12.2 ± 7.1 | 11.9 ± 8.3 | 0.537 |
Calcium (mg/day) | 393.0 ± 207.1 | 395.1 ± 262.1 | 0.844 |
Magnesium (mg/day) | 293.7 ± 110.3 | 301.0 ± 118.8 | 0.187 |
Quartile of Toenail Magnesium | |||||
---|---|---|---|---|---|
Q1 | Q2 | Q3 | Q4 | p † | |
Median (μg/g) | 129.5 | 198.9 | 271.9 | 453.6 | |
Age (years) | 49.8 ± 14.7 | 51.6 ± 13.9 | 50.6 ± 14.5 | 50.5 ± 14.6 | 0.730 |
Female (%) | 56.5 | 53.9 | 48.4 | 50.2 | <0.001 |
Urban (%) | 45.1 | 36.0 | 25.2 | 12.0 | <0.001 |
North (%) | 29.7 | 42.9 | 55.6 | 61.3 | <0.001 |
Education (high) (%) | 16.2 | 13.1 | 10.5 | 4.9 | <0.001 |
Current smoker (%) | 24.6 | 28.3 | 30.3 | 29.6 | 0.001 |
Current alcohol drinker (%) | 30.3 | 31.8 | 34.7 | 35.8 | 0.001 |
Tea drinker (%) | 36.5 | 36.0 | 36.3 | 30.3 | 0.030 |
BMI (kg/m2) | 23.2 ± 3.4 | 23.5 ± 3.4 | 23.6 ± 3.5 | 23.3 ± 3.5 | 0.720 |
Waist circumference (cm) | 81.6 ± 10.5 | 83.2 ± 10.2 | 83.8 ± 10.3 | 83.2 ± 10.2 | 0.001 |
Serum magnesium (mmol/L) | 0.9 ± 0.1 | 0.9 ± 0.1 | 0.9 ± 0.1 | 0.9 ± 0.1 | 0.824 |
Dietary intake | |||||
Energy (kcal/day) | 2115.5 ± 618.4 | 2143.5 ± 673.3 | 2238.9 ± 703.6 | 2298.2 ± 694.8 | <0.001 |
Carbohydrate (% of energy) | 51.1 ± 11.7 | 51.9 ± 11.7 | 54.3 ± 11.3 | 57.6 ± 11.5 | <0.001 |
Fat (% of energy) | 33.5 ± 10.3 | 32.7 ± 10.3 | 30.8 ± 9.9 | 29.1 ± 15.1 | <0.001 |
Fiber (g/day) | 10.8 ± 6.7 | 11.8 ± 10.3 | 12.3 ± 8.0 | 13.0 ± 7.2 | <0.001 |
Calcium (mg/day) | 401.1 ± 256.7 | 402.3 ± 268.8 | 395.0 ± 251.2 | 381.2 ± 255.9 | 0.018 |
Magnesium (mg/day) | 281.8 ± 104.5 | 289.9 ± 116.7 | 307.1 ± 125.6 | 323.0 ± 120.7 | <0.001 |
Quartile of Toenail Magnesium | |||||
---|---|---|---|---|---|
Q1 | Q2 | Q3 | Q4 | p † | |
Type 2 diabetes (%) | 8.0 | 8.2 | 7.7 | 6.2 | |
Model 1 | 1.00 (reference) | 0.96 (0.73–1.27) | 0.93 (0.70–1.23) | 0.73 (0.54–0.98) | 0.026 |
Model 2 | 1.00 (reference) | 0.89 (0.67–1.18) | 0.84 (0.62–1.13) | 0.72 (0.52–0.99) | 0.053 |
Model 3 | 1.00 (reference) | 0.89 (0.66–1.18) | 0.84 (0.62–1.13) | 0.72 (0.52–0.99) | 0.051 |
Quartile of Toenail Magnesium | ||||||
---|---|---|---|---|---|---|
n | Q1 | Q2 | Q3 | Q4 | p for Interaction | |
Subgroups | ||||||
Age | 0.452 | |||||
18–44 | 1933 | 1.00 (reference) | 0.60 (0.28–1.29) | 0.42 (0.19–0.95) | 0.44 (0.20–1.00) | |
45–59 | 2207 | 1.00 (reference) | 0.82 (0.51–1.31) | 0.92 (0.57–1.47) | 0.79 (0.47–1.31) | |
60– | 1543 | 1.00 (reference) | 1.12 (0.74–1.69) | 0.98 (0.62–1.53) | 0.81 (0.49–1.34) | |
Sex | 0.612 | |||||
Male | 2714 | 1.00 (reference) | 0.85 (0.56–1.29) | 0.88 (0.57–1.35) | 0.65 (0.40–1.05) | |
Female | 2969 | 1.00 (reference) | 0.97 (0.65–1.44) | 0.91 (0.60–1.38) | 0.82 (0.52–1.28) | |
Living area | 0.210 | |||||
Urban | 1679 | 1.00 (reference) | 0.93 (0.60–1.43) | 0.39 (0.24–0.64) | 0.61 (0.38–0.98) | |
Rural | 4004 | 1.00 (reference) | 1.31 (0.89–1.95) | 1.18 (0.78–1.78) | 0.97 (0.64–1.49) | |
Geographic region | 0.009 | |||||
North | 2692 | 1.00 (reference) | 0.71 (0.50–1.01) | 0.68 (0.47–0.99) | 0.52 (0.34–0.79) | |
South | 2991 | 1.00 (reference) | 1.11 (0.70–1.76) | 0.97 (0.60–1.58) | 1.30 (0.79–2.15) | |
Education | 0.841 | |||||
Low | 2481 | 1.00 (reference) | 0.82 (0.55–1.22) | 0.90 (0.59–1.36) | 0.71 (0.45–1.11) | |
Middle | 2568 | 1.00 (reference) | 0.68 (0.43–1.06) | 0.68 (0.43–1.08) | 0.65 (0.40–1.08) | |
High | 634 | 1.00 (reference) | 1.99 (0.68–5.85) | 0.85 (0.24–3.01) | 1.27 (0.36–4.45) | |
Smoking | 0.277 | |||||
Yes | 1603 | 1.00 (reference) | 0.69 (0.40–1.21) | 0.76 (0.43–1.34) | 0.43 (0.22–0.84) | |
No | 4080 | 1.00 (reference) | 1.02 (0.73–1.42) | 0.88 (0.62–1.25) | 0.88 (0.60–1.29) | |
Alcohol | 0.225 | |||||
Yes | 1884 | 1.00 (reference) | 0.71 (0.43–1.18) | 0.88 (0.54–1.45) | 0.58 (0.33–1.01) | |
No | 3799 | 1.00 (reference) | 1.10 (0.77–1.56) | 0.88 (0.60`1.28) | 0.88 (0.59–1.32) | |
BMI | 0.568 | |||||
Normal <24 kg/m2 | 3345 | 1.00 (reference) | 0.89 (0.54–1.46) | 0.96 (0.58–1.61) | 0.95 (0.55–1.64) | |
Overweight >=24 kg/m2 | 2338 | 1.00 (reference) | 0.90 (0.63–1.27) | 0.80 (0.56–1.16) | 0.62 (0.41–0.93) |
Dietary Magnesium | Serum Magnesium | Toenail Magnesium | |
---|---|---|---|
Dietary magnesium | 1.000 | 0.031, p = 0.019 | 0.119, p < 0.001 |
Serum magnesium | 0.031, p = 0.019 | 1.000 | 0.020, p = 0.126 |
Toenail magnesium | 0.119, p < 0.001 | 0.020, p = 0.126 | 1.000 |
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Zhang, J.; Wang, H.; Wang, Z.; Zhang, J.; Zhang, B. Association between Toenail Magnesium and Type 2 Diabetes in Chinese Adults. Nutrients 2017, 9, 811. https://doi.org/10.3390/nu9080811
Zhang J, Wang H, Wang Z, Zhang J, Zhang B. Association between Toenail Magnesium and Type 2 Diabetes in Chinese Adults. Nutrients. 2017; 9(8):811. https://doi.org/10.3390/nu9080811
Chicago/Turabian StyleZhang, Jiguo, Huijun Wang, Zhihong Wang, Ji Zhang, and Bing Zhang. 2017. "Association between Toenail Magnesium and Type 2 Diabetes in Chinese Adults" Nutrients 9, no. 8: 811. https://doi.org/10.3390/nu9080811
APA StyleZhang, J., Wang, H., Wang, Z., Zhang, J., & Zhang, B. (2017). Association between Toenail Magnesium and Type 2 Diabetes in Chinese Adults. Nutrients, 9(8), 811. https://doi.org/10.3390/nu9080811