Skip to main content

Advertisement

Log in

Serum Trace Elements and Electrolytes Are Associated with Fasting Plasma Glucose and HbA1c in Postmenopausal Women with Type 2 Diabetes Mellitus

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

The primary aim of the research was to assess the level of trace elements and electrolytes in serum of postmenopausal diabetic women. Sixty-four postmenopausal women with type 2 diabetes mellitus (DM2) and 64 age- and body mass index-matched controls were examined. Serum trace elements were assessed using inductively coupled plasma dynamic reaction cell mass spectrometry (ICP-DRC-MS). Fasting plasma glucose (FPG) and glycated hemoglobin (HbA1c) levels were evaluated using Randox kits. The obtained data demonstrate that DM2 patients were characterized by 42 and 34 % higher FPG and HbA1c levels, respectively (p < 0.001). The level of Cu and Se in diabetic postmenopausal women was increased by 10 and 15 % in comparison to the respective control values (p = 0.002 and <0.001). Serum Mn, Zn, and Ni concentrations were lower than the control ones by 32 % (p = 0.003), 8 % (p = 0.003), and 23 % (p = 0.046), respectively. FPG and HbA1c levels directly correlated with serum Se (p < 0.001) and Cu (p = 0.014 and p = 0.028) concentrations and inversely related to Zn (p < 0.001) and Tl (p = 0.023 and p = 0.029) levels. Multiple regression analysis demonstrated a significant association between serum Zn and Se and FPG and HbA1c levels. It is proposed that Zn and Se play an important role in DM2 pathogenesis. Further studies are required to assess the intimate mechanisms of the observed differences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Herman WH, Zimmet P (2012) Type 2 diabetes: an epidemic requiring global attention and urgent action. Diabetes Care 35(5):943–944

    Article  PubMed  PubMed Central  Google Scholar 

  2. Chen L, Magliano DJ, Zimmet PZ (2012) The worldwide epidemiology of type 2 diabetes mellitus—present and future perspectives. Nat Rev Endocrinol 8(4):228–236

    Article  CAS  Google Scholar 

  3. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103(2):137–149

    Article  CAS  PubMed  Google Scholar 

  4. Menke A, Casagrande S, Geiss L, Cowie CC (2015) Prevalence of and trends in diabetes among adults in the United States, 1988-2012. JAMA 314(10):1021–1029

    Article  CAS  PubMed  Google Scholar 

  5. Lam DW, LeRoith D (2012) The worldwide diabetes epidemic. Curr Opin Endocrinol Diabetes Obes 19(2):93–96

    Article  PubMed  Google Scholar 

  6. Szmuilowicz ED, Stuenkel CA, Seely EW (2009) Influence of menopause on diabetes and diabetes risk. Nat Rev Endocrinol 5(10):553–558

    Article  PubMed  Google Scholar 

  7. Wedisinghe L, Perera M (2009) Diabetes and the menopause. Maturitas 63(3):200–203

    Article  CAS  PubMed  Google Scholar 

  8. Scheen AJ (2014) Pathophysiology of type 2 diabetes. Acta Clin Belg 58(6):335–341

    Article  Google Scholar 

  9. Oberleas D (2011) Diabetes type II, a new perspective. Trace Elem Electroly 28(1):52–55

    Article  CAS  Google Scholar 

  10. Skalnaya MG, Demidov VA (2007) Hair trace element contents in women with obesity and type 2 diabetes. J Trace Elem Med Biol 21:59–61

    Article  CAS  PubMed  Google Scholar 

  11. Viktorínová A, Tošerová E, Križko M, Ďuračková Z (2009) Altered metabolism of copper, zinc, and magnesium is associated with increased levels of glycated hemoglobin in patients with diabetes mellitus. Metabolism 58(10):1477–1482

    Article  PubMed  Google Scholar 

  12. Wiernsperger N, Rapin J (2010) Trace elements in glucometabolic disorders: an update. Diabetol Metab Syndr 2(1):1

    Article  Google Scholar 

  13. Vincent JB (2000) The biochemistry of chromium. J Nutr 130(4):715–718

    CAS  PubMed  Google Scholar 

  14. Thompson KH, McNeill JH, Orvig C (1999) Vanadium compounds as insulin mimics. Chem Rev 99(9):2561–2572

    Article  CAS  PubMed  Google Scholar 

  15. Haase H, Maret W (2005) Fluctuations of cellular, available zinc modulate insulin signaling via inhibition of protein tyrosine phosphatases. J Trace Elem Med Biol 19(1):37–42

    Article  CAS  PubMed  Google Scholar 

  16. Flores CR, Puga MP, Wrobel K, Sevilla MEG, Wrobel K (2011) Trace elements status in diabetes mellitus type 2: possible role of the interaction between molybdenum and copper in the progress of typical complications. Diabetes Res Clin Pract 91(3):333–341

    Article  CAS  PubMed  Google Scholar 

  17. Kazi TG, Afridi HI, Kazi N, Jamali MK, Arain MB, Jalbani N, Kandhro GA (2008) Copper, chromium, manganese, iron, nickel, and zinc levels in biological samples of diabetes mellitus patients. Biol Trace Elem Res 122(1):1–18

    Article  CAS  PubMed  Google Scholar 

  18. Serdar M, Bakir F, Hasimi A et al (2009) Trace and toxic element patterns in nonsmoker patients with noninsulin-dependent diabetes mellitus, impaired glucose tolerance, and fasting glucose. Int J Diabetes Dev Ctries 29(1):35

    Article  PubMed  PubMed Central  Google Scholar 

  19. Jayawardena R, Ranasinghe P, Galappatthy P, Malkanthi RLDK, Constantine GR, Katulanda P (2012) Effects of zinc supplementation on diabetes mellitus: a systematic review and meta-analysis. Diabetol Metab Syndr 4(1):1

    Article  Google Scholar 

  20. Thompson KH, Orvig C (2006) Vanadium in diabetes: 100 years from phase 0 to phase I. J Inorg Biochem 100(12):1925–1935

    Article  CAS  PubMed  Google Scholar 

  21. Wang ZQ, Cefalu WT (2010) Current concepts about chromium supplementation in type 2 diabetes and insulin resistance. Curr Diab Rep 10(2):145–151

    Article  PubMed  Google Scholar 

  22. Rayman MP, Stranges S (2013) Epidemiology of selenium and type 2 diabetes: can we make sense of it? Free Radic Biol Med 65:1557–1564

    Article  CAS  PubMed  Google Scholar 

  23. Park K, Rimm EB, Siscovick DS et al (2012) Toenail selenium and incidence of type 2 diabetes in US men and women. Diabetes Care 35(7):1544–1551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Faghihi T, Radfar M, Barmal M, Amini P, Qorbani M, Abdollahi M, Larijani B (2014) A randomized, placebo-controlled trial of selenium supplementation in patients with type 2. Diabetes Res Clin Pract 21(6):491–495

    Google Scholar 

  25. Gao H, Hägg S, Sjögren P, Lambert PC, Ingelsson E, Dam RM (2014) Serum selenium in relation to measures of glucose metabolism and incidence of type 2 diabetes in an older Swedish population. Diabet Med 31(7):787–793

    Article  CAS  PubMed  Google Scholar 

  26. Vinceti M, Grioni S, Alber D et al (2015) Toenail selenium and risk of type 2 diabetes: the ORDET cohort study. J Trace Elem Med Biol 29:145–150

    Article  CAS  PubMed  Google Scholar 

  27. Naka T, Kaneto H, Katakami N et al (2013) Association of serum copper levels and glycemic control in patients with type 2 diabetes. Endocr J 60(3):393–396

    Article  CAS  PubMed  Google Scholar 

  28. Tanaka A, Kaneto H, Miyatsuka T et al (2009) Role of copper ion in the pathogenesis of type 2 diabetes. Endocr J 56(5):699–706

    Article  CAS  PubMed  Google Scholar 

  29. Cooper JSG (2012) Selective divalent copper chelation for the treatment of diabetes mellitus. Curr Med Chem 19(17):2828–2860

    Article  CAS  PubMed  Google Scholar 

  30. Fernández-Real JM, López-Bermejo A, Ricart W (2002) Cross-talk between iron metabolism and diabetes. Diabetes 51(8):2348–2354

    Article  PubMed  Google Scholar 

  31. Lee DH, Folsom AR, Jacobs JDR (2004) Dietary iron intake and type 2 diabetes incidence in postmenopausal women: the Iowa Women’s Health Study. Diabetologia 47(2):185–194

    Article  PubMed  Google Scholar 

  32. Rajpathak S, Ma J, Manson J, Willett WC, Hu FB (2006) Iron intake and the risk of type 2 diabetes in women a prospective cohort study. Diabetes Care 29(6):1370–1376

    Article  CAS  PubMed  Google Scholar 

  33. Jiang R, Manson JE, Meigs JB, Ma J, Rifai N, Hu FB (2004) Body iron stores in relation to risk of type 2 diabetes in apparently healthy women. JAMA 291(6):711–717

    Article  CAS  PubMed  Google Scholar 

  34. Orban E, Schwab S, Thorand B, Huth C (2014) Association of iron indices and type 2 diabetes: a meta-analysis of observational studies. Diabetes Metab Res Rev 30(5):372–394

    Article  CAS  PubMed  Google Scholar 

  35. Simcox JA, McClain DA (2013) Iron and diabetes risk. Cell Metab 17(3):329–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Dyer CA (2007) Heavy metals as endocrine-disrupting chemicals. Endocrine-Disrupting Chemicals. Humana Press, In, pp. 111–133

    Book  Google Scholar 

  37. Chen YW, Yang CY, Huang CF, Hung DZ, Leung YM, Liu SH (2009) Heavy metals, islet function and diabetes development. Islets 1(3):169–176

    Article  PubMed  Google Scholar 

  38. Afridi HI, Kazi TG, Kazi N et al (2008) Evaluation of status of toxic metals in biological samples of diabetes mellitus patients. Diabetes Res Clin Pract 80(2):280–288

    Article  CAS  PubMed  Google Scholar 

  39. American Diabetes Association (2016) Classification and diagnosis of diabetes. Diabetes Care 39:13–22

    Article  Google Scholar 

  40. Tietz NW (1995) Clinical guide to laboratory tests. WB Saunders Co.

  41. Heitland P, Köster HD (2006) Biomonitoring of 37 trace elements in blood samples from inhabitants of northern Germany by ICP–MS. J Trace Elem Med Biol 20(4):253–262

    Article  CAS  PubMed  Google Scholar 

  42. Blaine J, Chonchol M, Levi M (2015) Renal control of calcium, phosphate, and magnesium homeostasis. Clin J Am Soc Nephrol 10(7):1257–1272

    Article  CAS  PubMed  Google Scholar 

  43. Zargar AH, Shah NA, Masoodi SR et al (1998) Copper, zinc, and magnesium levels in non-insulin dependent diabetes mellitus. Postgrad Med J 74(877):665–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Xu J, Zhou Q, Liu G, Tan Y, Cai L (2013) Analysis of serum and urinal copper and zinc in Chinese northeast population with the prediabetes or diabetes with and without complications. Oxidative Med Cell Longev 2013:635214

    Article  Google Scholar 

  45. Walter RM, Uriu-Hare JY, Olin KL, Oster MH, Anawalt BD, Critchfield JW, Keen CL (1991) Copper, zinc, manganese, and magnesium status and complications of diabetes mellitus. Diabetes Care 14(11):1050–1056

    Article  PubMed  Google Scholar 

  46. Masad A, Hayes L, Tabner BJ et al (2007) Copper-mediated formation of hydrogen peroxide from the amylin peptide: a novel mechanism for degeneration of islet cells in type-2 diabetes mellitus? FEBS Lett 581(18):3489–3493

    Article  CAS  PubMed  Google Scholar 

  47. Lu J, Gong D, Choong SY et al (2010) Copper (II)-selective chelation improves function and antioxidant defences in cardiovascular tissues of rats as a model of diabetes: comparisons between triethylenetetramine and three less copper-selective transition-metal-targeted treatments. Diabetologia 53(6):1217–1226

    Article  CAS  PubMed  Google Scholar 

  48. Cooper GJ, Phillips AR, Choong SY et al (2004) Regeneration of the heart in diabetes by selective copper chelation. Diabetes 53(9):2501–2508

    Article  CAS  PubMed  Google Scholar 

  49. Basaki M, Saeb M, Nazifi S, Shamsaei HA (2012) Zinc, copper, iron, and chromium concentrations in young patients with type 2 diabetes mellitus. Biol Trace Elem Res 148(2):161–164

    Article  CAS  PubMed  Google Scholar 

  50. Bleys J, Navas-Acien A, Guallar E (2007) Serum selenium and diabetes in US adults. Diabetes Care 30(4):829–834

    Article  CAS  PubMed  Google Scholar 

  51. Laclaustra M, Navas-Acien A, Stranges S, Ordovas JM, Guallar E (2009) Serum selenium concentrations and diabetes in US adults: National Health and Nutrition Examination Survey (NHANES) 2003-2004. Environ Health Perspect 117(9):1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Vinceti M, Stranges S, Sieri S et al (2009) Association between high selenium intake and subsequent increased risk of type 2 diabetes in an Italian population. Epidemiology 20(6):S47

    Article  Google Scholar 

  53. Stranges S, Marshall JR, Natarajan R et al (2007) Effects of long-term selenium supplementation on the incidence of type 2 diabetes: a randomized trial. Ann Intern Med 147(4):217–223

    Article  PubMed  Google Scholar 

  54. Steinbrenner H, Speckmann B, Pinto A, Sies H (2010) High selenium intake and increased diabetes risk: experimental evidence for interplay between selenium and carbohydrate metabolism. J Clin Biochem Nutr 48(1):40–45

    Article  PubMed  PubMed Central  Google Scholar 

  55. Yang SJ, Hwang SY, Choi HY et al (2011) Serum selenoprotein P levels in patients with type 2 diabetes and prediabetes: implications for insulin resistance, inflammation, and atherosclerosis. J Clin Endocrinol Metab 96(8):E1325–E1329

    Article  CAS  PubMed  Google Scholar 

  56. Kljai K, Runje R (2001) Selenium and glycogen levels in diabetic patients. Biol Trace Elem Res 83(3):223–229

    Article  CAS  PubMed  Google Scholar 

  57. Kornhauser C, Garcia-Ramirez JR, Wrobel K, Pérez-Luque EL, Garay-Sevilla ME, Wrobel K (2008) Serum selenium and glutathione peroxidase concentrations in type 2 diabetes mellitus patients. Prim Care Diabetes 2(2):81–85

    Article  PubMed  Google Scholar 

  58. Song Y, Wang J, Li XK, Cai L (2005) Zinc and the diabetic heart. Biometals 18(4):325–332

    Article  CAS  PubMed  Google Scholar 

  59. Al-Maroof RA, Al-Sharbatti SS (2006) Serum zinc levels in diabetic patients and effect of zinc supplementation on glycemic control of type 2 diabetics. Saudi Med J 27(3):344–350

    PubMed  Google Scholar 

  60. Simon SF, Taylor CG (2001) Dietary zinc supplementation attenuates hyperglycemia in db/db mice. Exp Biol Med 226(1):43–51

    CAS  Google Scholar 

  61. Tinkov AA, Popova EV, Gatiatulina ER et al (2016) Decreased adipose tissue zinc content is associated with metabolic parameters in high fat fed Wistar rats. Acta Sci Pol Technol Aliment 15(1):99–105

    Article  PubMed  Google Scholar 

  62. Anderson RA, Roussel AM, Zouari N, Mahjoub S, Matheau JM, Kerkeni A (2001) Potential antioxidant effects of zinc and chromium supplementation in people with type 2 diabetes mellitus. J Am Coll Nutr 20(3):212–218

    Article  CAS  PubMed  Google Scholar 

  63. Roussel AM, Kerkeni A, Zouari N, Mahjoub S, Matheau JM, Anderson RA (2003) Antioxidant effects of zinc supplementation in Tunisians with type 2 diabetes mellitus. J Am Coll Nutr 22(4):316–321

    Article  CAS  PubMed  Google Scholar 

  64. Jansen J, Karges W, Rink L (2009) Zinc and diabetes—clinical links and molecular mechanisms. J Nutr Biochem 20(6):399–417

    Article  CAS  PubMed  Google Scholar 

  65. Barbagallo M, Dominguez LJ, Galioto A et al (2003) Role of magnesium in insulin action, diabetes and cardio-metabolic syndrome X. Mol Asp Med 24(1):39–52

    Article  CAS  Google Scholar 

  66. Kisters K, Schildheuer M, Matzkies FK et al (2000) Magnesium deficiency and increased fractional magnesium excretion in insulin-dependent diabetes mellitus: magnesium loading test and blood pressure. Trace Elem Electroly 17(2):67–70

    CAS  Google Scholar 

  67. Schulze MB, Schulz M, Heidemann C, Schienkiewitz A, Hoffmann K, Boeing H (2007) Fiber and magnesium intake and incidence of type 2 diabetes: a prospective study and meta-analysis. Arch Intern Med 167(9):956–965

    Article  CAS  PubMed  Google Scholar 

  68. Lorenzo C, Hanley AJ, Rewers MJ, Haffner SM (2014) Calcium and phosphate concentrations and future development of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetologia 57(7):1366–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Pittas AG, Dawson-Hughes B, Li T, Van Dam RM, Willett WC, Manson JE, Hu FB (2006) Vitamin D and calcium intake in relation to type 2 diabetes in women. Diabetes Care 29(3):650–656

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

The work was performed was supported by the Russian Ministry of Education and Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexey A. Tinkov.

Ethics declarations

All procedures were performed in accordance with the principles of the Declaration of Helsinki and its later amendments. All participants took part in the present investigation on a voluntary basis and were informed about the experimental procedures. The informed consent was signed by all volunteers before the investigation. The protocol of the present study was approved by the local ethics committee.

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Skalnaya, M.G., Skalny, A.V., Yurasov, V.V. et al. Serum Trace Elements and Electrolytes Are Associated with Fasting Plasma Glucose and HbA1c in Postmenopausal Women with Type 2 Diabetes Mellitus. Biol Trace Elem Res 177, 25–32 (2017). https://doi.org/10.1007/s12011-016-0868-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-016-0868-z

Keywords

Navigation