Abstract
To analyze Mg, Ca, and Zn levels in saliva, comparing patients with type 2 diabetes mellitus and a control group of healthy subjects. This transversal, observational, clinical study included a total sample of 147 patients, 74 with type 2 diabetes mellitus and a control group of 73 healthy subjects. Socio-demographic, anthropometric, diabetological, and metabolic variables were registered. Trace elements in non-stimulated basal saliva were measured using inductively coupled plasma mass spectrometry (ICP-MS): Mg, Ca, and Zn. Concentrations of zinc, calcium, and magnesium were significantly higher in the diabetic group than the control group (p < 0.001). A relation was observed between waist circumference and high cardiovascular risk in men (based on two categories: waist circumference < 102 cm; waist circumference ≥ 102 cm), and magnesium levels in saliva (p = 0.003). Magnesium, zinc, and calcium levels in saliva could be useful markers for differentiating patients with type 2 diabetes mellitus from non-diabetics. The salivary magnesium could be used as a marker of high cardiovascular risk when associated with abdominal obesity represented by a waist circumference ≥ 102 cm in men. The present results do suggest that salivary zinc levels could act as a good marker of type 2 diabetes mellitus, in light of zinc’s well-known role as a co-marker of insulin and its relationship to carbohydrate metabolism.
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References
Strimbu K, Tavel JA (2010) What are biomarkers? Curr Opin HIV AIDS 5:463–466. 9. https://doi.org/10.1097/COH.0b013e32833ed177
Desai GS, Mathews ST (2014) Saliva as a non-invasive diagnostic tool for inflammation and insulin-resistance. World J Diabetes 5:730–738. https://doi.org/10.4239/wjd.v5.i6.730
Srinivasan M, Blackburn C, Mohamed M, Sivagami AV, Blum J (2015) Literature-based discovery of salivary biomarkers for type 2 diabetes mellitus. Biomark Insights 10:39–45. https://doi.org/10.4137/BMI.S22177.
Zhang CZ, Cheng XQ, Li JY, Zhang P, Yi P, Xin X, Zhou XD (2016) Saliva in the diagnosis of diseases. Int J Oral Sci 8:133–137. https://doi.org/10.1038/ijos.2016.38
Walter RM, Uriu-Hare JY, Lewis Olin K, Oster MH, Anawalt BD, Critchfield JW, Keen CL (1991) Copper, zinc, manganese, and magnesium status and complications of diabetes mellitus. Diabetes Care 14:1050–1056. https://doi.org/10.1080/03630260701727077.
Zheng Y, Li XK, Wang Y, Cai L (2008) The role of zinc, copper and Iron in the pathogenesis of diabetes and diabetic complications: therapeutic effects by chelators. Hemoglobin 32:135–145. https://doi.org/10.1080/03630260701727077
Norouzi S, Adulcikas J, Sohal SS, Myers S (2017) Zinc transporters and insulin resistance: therapeutic implications for type 2 diabetes and metabolic disease. J Biomed Sci 24(1):87. https://doi.org/10.1186/s12929-017-0394-0
Mata AD, Marqués D, Rocha S, Francisco H, Santos C, Mesquita MF, Singh J (2004) Effects of diabetes mellitus on salivary secretion and its composition in the human. Mol Cell Biochem 261(1–2):137–142
Lasisi TJ, Fasanmade AA (2012) Salivary flow and composition in diabetic and nondiabetic subjects. Niger J Physiol Sci 27:79–78
American Diabetes Association (2014) Diagnosis and classification of diabetes mellitus. Diabetes Care 37:81–90. https://doi.org/10.2337/dc14-S081
Goday A (2002) Epidemiología de la diabetes y sus complicaciones no coronarias. Rev Esp Cardiol 55:657–670
Bosch X, Alfonso F, Bermejo (2002) Diabetes y enfermedad cardiovascular. Una mirada hacia la nueva epidemia del siglo XXI. Rev Esp Cardiol 55:525–527
Soriano Perera P, De Pablos Velasco PL (2007) Epidemiología de la diabetes mellitus. Endocrinol Nutr 54:2–7
Mafong D, Henry R (2008) Exenatide as a treatment for diabetes and obesity: implications for cardiovascular risk reduction. Curr Atheroscler Rep 10:55–60
Poirier P, Giles TD, Bray GA, Hong Y, Stern JS, Pi-Sunyer FX, Eckel RH (2006) Obesity and cardiovascular disease: pathophysiology, evaluation, and effect of weight loss. Arterioscler Thromb Vasc Biol 26(5):968–976. https://doi.org/10.1161/01.ATV.0000216787.85457.f3
Carda C, Mosquera-Lloreda N, Salom L, Gómez de Ferraris ME, Peydró A (2006) Structural and functional salivary disorders in type 2 diabetic patients. Med Oral Patol Oral Cir Bucal 11:309–314
Borges BC, Fulco GM, Souza AJ, De Lima KC (2010) Xerostomia and hyposalivation: a preliminary report of their prevalence and associated factors in Brazilian elderly diabetic patients. Oral Health Prev Dent 8(2):153–158
Aitken-Saavedra J, Rojas-Alcayaga G, Maturana-Ramírez A, Escobar-Álvarez A, Cortés-Coloma A, Reyes-Rojas M, Viera-Sapiain V, Villablanca-Martínez C, Morales-Bozo I (2015) Salivary gland dysfunction markers in type 2 diabetes mellitus patients. J Clin Exp Dent 7:501–505
López-Pintor RM, Casañas E, González-Serrano J, Serrano J, Ramírez L, de Arriba L, Hernández G (2016) Xerostomia, hyposalivation, and salivary flow in diabetes patients. J Diabetes Res 2016:1–15. https://doi.org/10.1155/2016/4372852
Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 285(19):2486–2497
Panchbhai AS, Deqwekar SS, Bhowte RR (2010) Estimation of salivary glucose, salivary amylase, salivary total protein and salivary flow rate in diabetics in India. J Oral Sci 52:359–368
Wolide AD, Zawdie B, Alemayehu T, Tadesse S (2017) Association of trace metal elements with lipid profiles in type 2 diabetes mellitus patients: a cross sectional study. BMC Endocr Disord 17(1):64. https://doi.org/10.1186/s12902-017-0217-z
Ranasinghe P, Wathurapatha WS, Ishara MH, Jayawardana R, Galappatthy P, Katulanda P, Constantine GR (2015) Effects of zinc supplementation on serum lipids: a systematic review and meta-analysis. Nutr Metab (Lond) 12:26. https://doi.org/10.1186/s12986-015-0023-4
Jansen J, Karges W, Rink L (2009) Zinc and diabetes. Clinical links and molecular mechanisms. J Nutr Biochem 20:399–417. https://doi.org/10.1016/j.jnutbio.2009.01.009
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 29:650–656
Mooren FC (2015) Magnesium and disturbances in carbohydrate metabolism. Diabetes Obes Metab 17:813–823. https://doi.org/10.1111/dom.12492
Bertinato J, Wang KC, Hayward S (2017) Serum magnesium concentrations in the Canadian population and associations with diabetes, glycemic regulation, and insulin resistance. Nutrients 9:1–13. https://doi.org/10.3390/nu9030296
Simić A, Hansen AF, Åsvold BO, Romundstad PR, Midthjell K, Syversen T, Flaten TP (2017) Trace element status in patients with type 2 diabetes in Norway: the HUNT3 survey. J Trace Elem Med Biol 41:91–98. https://doi.org/10.1016/j.jtemb.2017.03.001
Navas-Acien A, Guallar E, Silbergeld EK, Rothenberg S (2007) Lead exposure and cardiovascular disease: a systematic review. Environ Health Perspect 115:472–482. https://doi.org/10.1289/ehp.9785
Karatela S, Paterson J, Ward NI (2017) Trace elements and human obesity: an overview. J Trace Elem Med Biol 41:10–15. https://doi.org/10.1016/j.jtemb.2017.01.003
Badran M, Morsy R, Soliman H, Elnimr T (2016) Assessment of trace elements levels in patients with type 2 diabetes using multivariate statistical analysis. J Trace Elem Med Biol 33:114–119. https://doi.org/10.1016/j.jtemb.2015.10.006
Laires MJ, Moreira H, Monteiro CP, Sardinha L, Limão F, Veiga L, Gonçalves A, Ferreira A, Bicho M (2004) Magnesium, insulin resistance and body composition in healthy postmenopausal women. J Am Coll Nutr 23:510–513
King DE, Mainous AG, Geesey ME, Woolson RF (2005) Dietary magnesium and C reactive protein levels. J Am Coll Nutr 24:166–171
Nielsen FH (2010) Magnesium, inflammation, and obesity in chronic disease. Nutr Rev 68(6):333–340. https://doi.org/10.1111/j.1753-4887.2010.00293.x
Tóthová L, Kamodyová N, Červenka T, Celec P (2015) Salivary markers of oxidative stress in oral diseases. Front Cell Infect Microbiol 5:73. https://doi.org/10.3389/fcimb.2015.00073
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The study protocol was approved by the Ethics Committee of University Of Murcia (Spain) (16/10/2014) and all procedures performed in this study were in accordance with the ethical standards of the institutional research committee.
This study was carried out according to the principles of the Declaration of Helsinki, 2013. Informed consent was obtained from all individual participants included in the study.
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Marín Martínez, L., Molino Pagán, D. & López Jornet, P. Trace Elements in Saliva as Markers of Type 2 Diabetes Mellitus. Biol Trace Elem Res 186, 354–360 (2018). https://doi.org/10.1007/s12011-018-1326-x
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DOI: https://doi.org/10.1007/s12011-018-1326-x