Biological Trace Element Research

, Volume 143, Issue 2, pp 835–843

Intra-erythrocyte Magnesium Is Associated with Gamma-Glutamyl Transferase in Obese Children and Adolescents

  • Maryam Tohidi
  • Asghar Ghasemi
  • Farzad Hadaegh
  • Shamsi Arbabi
  • Firoozeh Hosseini Isfahani


This study aims at determining the association between markers of hepatic injury and serum, urinary, and intra-erythrocyte magnesium concentrations and dietary magnesium intake in obese children and adolescents. In a case–control study, 42 obese children and adolescents (8–18 years) and 42 sex- and puberty-matched controls were studied. Serum, urinary, and intra-erythrocyte magnesium levels, indices of insulin sensitivity, and liver enzymes were measured. Dietary magnesium intake was assessed using a food frequency questionnaire. Obese children and adolescents exhibited insulin resistance as determined by a higher fasting insulin and the HOMA-IR (p < 0.001) and lower QUICKI indices (p = 0.001); in addition these subjects had significantly higher intra-erythrocyte magnesium (IEM) concentrations, than non-obese ones (3.99 ± 1.05 vs. 3.35 ± 1.26 mg/dL of packed cell; p = 0.015). Among liver enzymes, only gamma-glutamyl transferase (GGT) was significantly higher in obese than in non-obese subjects (22.7 ± 9.4 vs. 17.1 ± 7.9 U/l; p = 0.002). A positive association was found between GGT and IEM in both groups; however in multivariate analysis, in obese subjects, only GGT (p = 0.026) and, in non-obese subjects, only age (p = 0.006) remained as significant predictors of IEM. In conclusion, increased IEM concentration was seen in insulin-resistant obese children and adolescents; furthermore, serum GGT was associated with IEM, independently of body mass index and HOMA-IR.


Adolescent Children Gamma-glutamyl transferase Magnesium Obesity 


  1. 1.
    Huerta MG, Roemmich JN, Kington ML, Bovbjerg VE, Weltman AL, Holmes VF, Patrie JT, Rogol AD, Nadler JL (2005) Magnesium deficiency is associated with insulin resistance in obese children. Diab Care 28:1175–1181CrossRefGoogle Scholar
  2. 2.
    Moayeri H, Bidad K, Aghamohammadi A, Rabbani A, Anari S, Nazemi L, Gholami N, Zadhoush S, Hatmi ZN (2006) Overweight and obesity and their associated factors in adolescents in Tehran, Iran, 2004–2005. Eur J Pediatr 165:489–493PubMedCrossRefGoogle Scholar
  3. 3.
    Baker JL, Olsen LW, Sorensen TI (2007) Childhood body-mass index and the risk of coronary heart disease in adulthood. N Engl J Med 357:2329–2337PubMedCrossRefGoogle Scholar
  4. 4.
    Fawcett WJ, Haxby EJ, Male DA (1999) Magnesium: physiology and pharmacology. Br J Anaesth 83:302–320PubMedGoogle Scholar
  5. 5.
    Chaudhary DP, Sharma R, Bansal DD (2010) Implications of magnesium deficiency in type 2 diabetes: a review. Biol Trace Elem Res 134:119–129PubMedCrossRefGoogle Scholar
  6. 6.
    Malon A, Brockmann C, Fijalkowska-Morawska J, Rob P, Maj-Zurawska M (2004) Ionized magnesium in erythrocytes—the best magnesium parameter to observe hypo- or hypermagnesemia. Clin Chim Acta 349:67–73PubMedCrossRefGoogle Scholar
  7. 7.
    Paolisso G, Ravussin E (1995) Intracellular magnesium and insulin resistance: results in Pima Indians and Caucasians. J Clin Endocrinol Metab 80:1382–1385PubMedCrossRefGoogle Scholar
  8. 8.
    Kao WH, Folsom AR, Nieto FJ, Mo JP, Watson RL, Brancati FL (1999) Serum and dietary magnesium and the risk for type 2 diabetes mellitus: the atherosclerosis risk in communities study. Arch Intern Med 159:2151–2159PubMedCrossRefGoogle Scholar
  9. 9.
    Laires MJ, Moreira H, Monteiro CP, Sardinha L, Limao F, Veiga L, Goncalves A, Ferreira A, Bicho M (2004) Magnesium, insulin resistance and body composition in healthy postmenopausal women. J Am Coll Nutr 23:510S–513SPubMedGoogle Scholar
  10. 10.
    Basso LE, Ubbink JB, Delport R (2000) Erythrocyte magnesium concentration as an index of magnesium status: a perspective from a magnesium supplementation study. Clin Chim Acta 291:1–8PubMedCrossRefGoogle Scholar
  11. 11.
    De Leeuw I, Vansant G, Van Gaal L (1992) Magnesium and obesity: influence of gender, glucose tolerance, and body fat distribution on circulating magnesium concentrations. Magnes Res 5:183–187PubMedGoogle Scholar
  12. 12.
    Tohidi M, Harati H, Hadaegh F, Mehrabi Y, Azizi F (2008) Association of liver enzymes with incident type 2 diabetes: a nested case control study in an Iranian population. BMC Endocr Disord 8:5PubMedCrossRefGoogle Scholar
  13. 13.
    Strauss RS, Barlow SE, Dietz WH (2000) Prevalence of abnormal serum aminotransferase values in overweight and obese adolescents. J Pediatr 136:727–733PubMedCrossRefGoogle Scholar
  14. 14.
    Ortega E, Koska J, Salbe AD, Tataranni PA, Bunt JC (2006) Serum gamma-glutamyl transpeptidase is a determinant of insulin resistance independently of adiposity in Pima Indian children. J Clin Endocrinol Metab 91:1419–1422PubMedCrossRefGoogle Scholar
  15. 15.
    Rantala AO, Lilja M, Kauma H, Savolainen MJ, Reunanen A, Kesaniemi YA (2000) Gamma-glutamyl transpeptidase and the metabolic syndrome. J Intern Med 248:230–238PubMedCrossRefGoogle Scholar
  16. 16.
    Kaushik GG, Sharm S, Sharma R, Mittal P (2009) Association between gamma glutamyl transferase and insulin resistance markers in healthy obese children. J Assoc Physicians India 57:695–698PubMedGoogle Scholar
  17. 17.
    Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243PubMedCrossRefGoogle Scholar
  18. 18.
    Goran MI, Gower BA (2001) Longitudinal study on pubertal insulin resistance. Diabetes 50:2444–2450PubMedCrossRefGoogle Scholar
  19. 19.
    Millart H, Durlach V, Durlach J (1995) Red blood cell magnesium concentrations: analytical problems and significance. Magnes Res 8:65–76PubMedGoogle Scholar
  20. 20.
    Esmaillzadeh A, Mirmiran P, Azizi F (2005) Whole-grain consumption and the metabolic syndrome: a favorable association in Tehranian adults. Eur J Clin Nutr 59:353–362PubMedCrossRefGoogle Scholar
  21. 21.
    Willett W, Stampfer M (1998) Implications of total energy intake for epidemiologic analyses. In: Willett W (ed) Nutritional epidemiology. Oxford University Press, New York, pp 273–301CrossRefGoogle Scholar
  22. 22.
    Romani AM, Matthews VD, Scarpa A (2000) Parallel stimulation of glucose and Mg 2+ accumulation by insulin in rat hearts and cardiac ventricular myocytes. Circ Res 86:326–333PubMedGoogle Scholar
  23. 23.
    Kjeldsen SE, Sejersted OM, Frederichsen P, Leren P, Eide IK (1990) Increased erythrocyte magnesium content in essential hypertension. Scand J Clin Lab Invest 50:395–400PubMedCrossRefGoogle Scholar
  24. 24.
    Barbagallo M, Gupta RK, Dominguez LJ, Resnick LM (2000) Cellular ionic alterations with age: relation to hypertension and diabetes. J Am Geriatr Soc 48:1111–1116PubMedGoogle Scholar
  25. 25.
    Schimatschek HF, Classen HG (1993) Age, sex and seasonal effects on plasma magnesium and calcium levels of 4859 children. In: Golf S, Dralle D, Vecchiet L (eds) magnesium. John Libbey & Company Ltd., London, pp 135–146Google Scholar
  26. 26.
    Hanley AJ, Williams K, Festa A, Wagenknecht LE, D’Agostino RB Jr, Kempf J, Zinman B, Haffner SM (2004) Elevations in markers of liver injury and risk of type 2 diabetes: the insulin resistance atherosclerosis study. Diabetes 53:2623–2632PubMedCrossRefGoogle Scholar
  27. 27.
    Neuschwander-Tetri BA, Caldwell SH (2003) Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology 37:1202–1219PubMedCrossRefGoogle Scholar
  28. 28.
    Erol A (2007) Insulin resistance is an evolutionarily conserved physiological mechanism at the cellular level for protection against increased oxidative stress. BioEssays 29:811–818PubMedCrossRefGoogle Scholar
  29. 29.
    Barbagallo M, Dominguez LJ, Tagliamonte MR, Resnick LM, Paolisso G (1999) Effects of glutathione on red blood cell intracellular magnesium: relation to glucose metabolism. Hypertension 34:76–82PubMedGoogle Scholar
  30. 30.
    Patrick L (2002) Nonalcoholic fatty liver disease: relationship to insulin sensitivity and oxidative stress. Treatment approaches using vitamin E, magnesium, and betaine. Altern Med Rev 7:276–291PubMedGoogle Scholar
  31. 31.
    Minnich V, Smith MB, Brauner MJ, Majerus PW (1971) Glutathione biosynthesis in human erythrocytes. I. Identification of the enzymes of glutathione synthesis in hemolysates. J Clin Invest 50:507–513PubMedCrossRefGoogle Scholar
  32. 32.
    Samuel VT, Liu ZX, Qu X, Elder BD, Bilz S, Befroy D, Romanelli AJ, Shulman GI (2004) Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease. J Biol Chem 279:32345–32353PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Maryam Tohidi
    • 1
  • Asghar Ghasemi
    • 2
  • Farzad Hadaegh
    • 1
  • Shamsi Arbabi
    • 1
  • Firoozeh Hosseini Isfahani
    • 3
  1. 1.Prevention of Metabolic Disorders Research Center, Research Institute for Endocrine SciencesShahid Beheshti University of Medical SciencesTehranIran
  2. 2.Endocrine Research Center, Research Institute for Endocrine SciencesShahid Beheshti University of Medical SciencesTehranIran
  3. 3.Obesity Research Center, Research Institute for Endocrine SciencesShahid Beheshti University of Medical SciencesTehranIran

Personalised recommendations