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Plasma Levels of Magnesium, Calcium, Calcium to Magnesium Ratio, and Associations with Metabolic Syndrome and Cardiometabolic Risk Factors

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Abstract

Magnesium and calcium are elements that have been associated with cardiometabolic risk factors related to metabolic syndrome (MetS). However, there are gaps in the knowledge regarding the impact of the calcium to magnesium (Ca/Mg) ratio in plasma. Thus, we aim to evaluate the associations between magnesium and calcium levels in plasma, and the Ca/Mg ratio in plasma with MetS components and other cardiometabolic risk factors. This cross-sectional study was carried out with 112 adults and older people, distributed into groups with (n = 60) and without MetS (n = 52). We evaluated sociodemographic, anthropometric, and biochemical data. Magnesium and calcium levels in plasma were measured by inductively coupled plasma mass spectrometry technique (ICP-MS). There was a high frequency of MetS, with no significant differences in magnesium and calcium levels and Ca/Mg ratio in plasma observed between groups. There were no associations between magnesium and MetS components or other cardiometabolic risk factors (all p > 0.05). Calcium levels were associated with total cholesterol (β =  − 0.020; p = 0.000) and high-density lipoprotein cholesterol (HDL-c) (β =  − 0.046; p = 0.005). The total cholesterol (β =  − 0.025; p = 0.000) and low-density lipoprotein cholesterol (LDL-c) (β = 0.017; p = 0.020) were preditors of the Ca/Mg ratio. These results indicate important associations of calcium and the Ca/Mg ratio in plasma with cardiometabolic risk factors related to MetS.

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All data generated or analyzed during this study are included in this manuscript and its supplementary information file. Further inquiries can be directed to the corresponding author.

References

  1. Sociedade Brasileira de Hipertensão, Sociedade Brasileira de Cardiologia, Sociedade Brasileira de Endocrinologia e Metabologia, Sociedade Brasileira de Diabetes, Sociedade Brasileira de Estudos da Obesidade (2005) I diretriz Brasileira de diagnóstico e tratamento da síndrome metabólica [I Brazilian guidelines on diagnosis and treatment of metabolic syndrome] Arq Bras Cardiol 84(1):1–28

  2. Siqueira Valadares LT, de Souza LSB, Salgado Junior VA, de Freitas Bonomo L, de Macedo LR, Silva M (2022) Prevalence of metabolic syndrome in Brazilian adults in the last 10 years: a systematic review and meta-analysis. BMC Public Health 22(1):327. https://doi.org/10.1186/s12889-022-12753-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Hirode G, Wong RJ (2020) Trends in the prevalence of metabolic syndrome in the United States, 2011–2016. JAMA. 323(24):2526–2528. https://doi.org/10.1001/jama.2020.4501

    Article  PubMed  PubMed Central  Google Scholar 

  4. Silveira Rossi JL, Barbalho SM, Reverete de Araujo R, Bechara MD, Sloan KP, Sloan LA (2022) Metabolic syndrome and cardiovascular diseases: going beyond traditional risk factors. Diabetes Metab Res Rev 38(3):e3502. https://doi.org/10.1002/dmrr.3502

    Article  PubMed  CAS  Google Scholar 

  5. Kanagasabai T, Alkhalaqi K, Churilla JR, Ardern CI (2019) The association between metabolic syndrome and serum concentrations of micronutrients, inflammation, and oxidative stress outside of the clinical reference ranges: a cross-sectional study. Metab Syndr Relat Disord 17(1):29–36. https://doi.org/10.1089/met.2018.0080

    Article  PubMed  CAS  Google Scholar 

  6. Salinas M, López-Garrigós M, Flores E, Leiva-Salinas C (2023) Improving diagnosis and treatment of hypomagnesemia. Clin Chem Lab Med 62(2):234–248. https://doi.org/10.1515/cclm-2023-0537

    Article  PubMed  CAS  Google Scholar 

  7. Fiorentini D, Cappadone C, Farruggia G, Prata C (2021) Magnesium: biochemistry, nutrition, detection, and social impact of diseases linked to its deficiency. Nutrients 13(4):1136. https://doi.org/10.3390/nu13041136

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Feng J, Wang H, Jing Z, Wang Y, Cheng Y, Wang W et al (2020) Role of magnesium in type 2 diabetes mellitus. Biol Trace Elem Res 196(1):74–85. https://doi.org/10.1007/s12011-019-01922-0

    Article  PubMed  CAS  Google Scholar 

  9. Ye L, Zhang C, Duan Q, Shao Y, Zhou J (2023) Association of magnesium depletion score with cardiovascular disease and its association with longitudinal mortality in patients with cardiovascular disease. J Am Heart Assoc 12(18):e030077. https://doi.org/10.1161/JAHA.123.030077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Zhu J, Xun P, Bae JC, Kim JH, Kim DJ, Yang K et al (2019) Circulating calcium levels and the risk of type 2 diabetes: a systematic review and meta-analysis. Br J Nutr 122(4):376–387. https://doi.org/10.1017/S0007114519001430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Mathew AA, Panonnummal R (2021) ‘Magnesium’-the master cation-as a drug-possibilities and evidences. Biometals 34(5):955–986. https://doi.org/10.1007/s10534-021-00328-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Costello RB, Rosanoff A, Dai Q, Saldanha LG, Potischman NA (2021) Perspective: Characterization of dietary supplements containing calcium and magnesium and their respective ratio—is a rising ratio a cause for concern? Adv Nutr 12(2):291–297. https://doi.org/10.1093/advances/nmaa160

    Article  PubMed  Google Scholar 

  13. Park SH, Kim SK, Bae YJ (2012) Relationship between serum calcium and magnesium concentrations and metabolic syndrome diagnostic components in middle-aged Korean men. Biol Trace Elem Res 146(1):35–41. https://doi.org/10.1007/s12011-011-9224-5

    Article  PubMed  CAS  Google Scholar 

  14. Escobedo-Monge MF, Barrado E, Parodi-Román J, Escobedo-Monge MA, Torres Hinojal MC, Marugán-Miguelsanz JM (2022) Magnesium status and Ca/Mg ratios in a series of children and adolescents with chronic diseases. Nutrients 14(14):2941. https://doi.org/10.3390/nu14142941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA et al (2009) International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120(16):1640–1645 https://doi.org/10.1161/CIRCULATIONAHA.109.192644

  16. 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 Cholesterol. JAMA. 285(19):2486–97. https://doi.org/10.1001/jama.285.19.2486

    Article  Google Scholar 

  17. Faludi AA, Izar MCO, Saraiva JFK, Chacra APM, Bianco HT, Afiune A et al (2017) Atualização da Diretriz Brasileira de Dislipidemias e Prevenção da Aterosclerose – 2017. Arq Bras Cardiol 109(2 Supl 1):1–76. https://doi.org/10.5935/abc.20170121

    Article  PubMed  Google Scholar 

  18. World Health Organization (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894:i-xii, 1–253

  19. Barroso WKS, Rodrigues CIS, Bortolotto LA, Mota-Gomes MA, Brandão AA, Feitosa ADM et al (2021) Brazilian guidelines of hypertension – 2020. Arq Bras Cardiol 116(3):516–658. https://doi.org/10.36660/abc.20201238

    Article  PubMed  PubMed Central  Google Scholar 

  20. Craig CL, Marshall AL, Sjöström M, Bauman AE, Booth ML, Ainsworth BE, et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35(8):1381–95. https://doi.org/10.1249/01.MSS.0000078924.61453.FB

  21. BRASIL (2019) Diretrizes da Sociedade Brasileira de Diabetes 2019–2020. Brasília: Sociedade Brasileira de Diabetes. p 491. https://www.saude.ba.gov.br/wp-content/uploads/2020/02/Diretrizes-Sociedade-Brasileira-de-Diabetes-2019-2020.pdf. Accessed 3 Jan 2024

  22. Geloneze B, Vasques ACJ, Stabe CF, Pareja JC, Rosado LE, Queiroz EC et al (2009) HOMA1-IR and HOMA2-IR indexes in identifying insulin resistance and metabolic syndrome: Brazilian Metabolic Syndrome Study (BRAMS). Arq Bras Endocrinol Metabol 53(2):281–7. https://doi.org/10.1590/s0004-27302009000200020

    Article  PubMed  Google Scholar 

  23. Meyer S, Markova M, Pohl G, Marschall TA, Pivovarova O, Pfeiffer AFH et al (2018) Development, validation and application of an ICP-MS/MS method to quantify minerals and (ultra-)trace elements in human serum. J Trace Elem Med Biol 49:157–163. https://doi.org/10.1016/j.jtemb.2018.05.012

    Article  PubMed  CAS  Google Scholar 

  24. Batista BL, Rodrigues JL, Nunes JA, de Oliveira Souza VC, Barbosa F (2009) Exploiting dynamic reaction cell inductively coupled plasma mass spectrometry (DRC-ICP-MS) for sequential determination of trace elements in blood using a dilute-and-shoot procedure. Anal Chim Acta 639(1–2):13–18. https://doi.org/10.1016/j.aca.2009.03.016

    Article  PubMed  CAS  Google Scholar 

  25. Topf JM, Murray PT (2003) Hypomagnesemia and hypermagnesemia. Rev Endocr Metab Disord 4(2):195–206. https://doi.org/10.1023/a:1022950321817

    Article  PubMed  Google Scholar 

  26. Cooper MS, Gittoes NJ (2008) Diagnosis and management of hypocalcaemia. BMJ 336(7656):1298–302. https://doi.org/10.1136/bmj.39582.589433.BE

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kamoru AA, Japhet OM, Adetunji AD, Musa MA, Hammed OO, Akinlawon AA et al (2017) Castelli risk index, atherogenic index of plasma, and atherogenic coefficient: emerging risk predictors of cardiovascular disease in HIV-treated patients. Saudi J Med Pharm Sci 4929:1101–1110. https://doi.org/10.21276/sjmps.2017.3.10.15

    Article  Google Scholar 

  28. Dobiás̆ová M, Frohlich J (2001) The plasma parameter log (TG/HDL-c) as an atherogenic index: correlation with lipoprotein particle size and esterification rate in ApoB-lipoprotein-depleted plasma (FERHDL). Clin Biochem 34(7):583–588. https://doi.org/10.1016/s0009-9120(01)00263-6

    Article  PubMed  Google Scholar 

  29. Wu TT, Gao Y, Zheng YY, Ma YT, Xie X (2018) Atherogenic index of plasma (AIP): a novel predictive indicator for the coronary artery disease in postmenopausal women. Lipids Health Dis 17(1):197. https://doi.org/10.1186/s12944-018-0828-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Amato MC, Giordano C (2014) Visceral adiposity index: an indicator of adipose tissue dysfunction. Int J Endocrinol 2014:730827. https://doi.org/10.1155/2014/730827

    Article  PubMed  PubMed Central  Google Scholar 

  31. Rył Aleksandra, Ciosek Ż, Szylińska Aleksandra, Jurewicz A, Bohatyrewicz Andrzej, Zietek Paweł et al (2023) Metabolic syndrome in aging men as a factor affecting the relationship between Mg, Ca, and P in serum and bone. Int J Mol Sci 24(13):10947–7. https://doi.org/10.3390/ijms241310947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Malta DC, Pinheiro PC, Teixeira RA, Machado IE, dos Santos FM, Ribeiro ALP (2021) Estimativas do Risco Cardiovascular em Dez Anos na População Brasileira: Um Estudo de Base Populacional. Arq Bras Cardiol 116(3):423–31. https://doi.org/10.36660/abc.20190861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Hallajzadeh J, Khoramdad M, Izadi N, Karamzad N, Almasi-Hashiani A, Ayubi E et al (2018) Metabolic syndrome and its components in premenopausal and postmenopausal women: a comprehensive systematic review and meta-analysis on observational studies. Menopause 25(10):1155–1164. https://doi.org/10.1097/GME.0000000000001136

    Article  PubMed  Google Scholar 

  34. Escobedo-Monge MF, Barrado E, Parodi-Román J, Escobedo-Monge MA, Torres-Hinojal MC, Marugán-Miguelsanz JM (2022) Magnesium status and Ca/Mg ratios in a series of children and adolescents with chronic diseases. Nutrients 14(14):2941. https://doi.org/10.3390/nu14142941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Yuan Z, Liu C, Tian Y, Zhang X, Ye H, Jin L et al (2016) Higher levels of magnesium and lower levels of calcium in whole blood are positively correlated with the metabolic syndrome in a Chinese population: a case-control study. Ann Nutr Metab 69(2):125–134. https://doi.org/10.1159/000450761

    Article  PubMed  CAS  Google Scholar 

  36. Malinowska J, Małecka M, Ciepiela O (2020) Variations in magnesium concentration are associated with increased mortality: study in an unselected population of hospitalized patients. Nutrients 12(6):1836. https://doi.org/10.3390/nu12061836

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Li Q, Chen Q, Zhang H, Xu Z, Wang X, Pang J et al (2020) Associations of serum magnesium levels and calcium-magnesium ratios with mortality in patients with coronary artery disease. Diabetes Metab 46(5):384–391. https://doi.org/10.1016/j.diabet.2019.12.003

    Article  PubMed  CAS  Google Scholar 

  38. Alkazemi D, Alsouri N, Zafar T, Kubow S (2022) Hypomagnesemia and the metabolic syndrome among apparently healthy Kuwaiti adults: a cross-sectional study. Nutrients 14(24):5257. https://doi.org/10.3390/nu14245257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Dinicolantonio JJ, O’Keefe JH, Wilson W (2018) Subclinical magnesium deficiency: a principal driver of cardiovascular disease and a public health crisis. Open Heart 5(1):e000668. https://doi.org/10.1136/openhrt-2017-000668

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kocyigit E, Akturk M, Koksal E (2023) Relationships between serum and dietary magnesium, calcium, and metabolic parameters in women with type 2 diabetes mellitus. Clin Nutr ESPEN 54:304–310. https://doi.org/10.1016/j.clnesp.2023.01.035

    Article  PubMed  Google Scholar 

  41. Bertinato J, Wu Xiao C, Ratnayake WM, Fernandez L, Lavergne C, Wood C et al (2015) Lower serum magnesium concentration is associated with diabetes, insulin resistance, and obesity in South Asian and white Canadian women but not men. Food Nutr Res 59:25974. https://doi.org/10.3402/fnr.v59.25974

    Article  PubMed  Google Scholar 

  42. Alomaim H, Griffin P, Swist E, Plouffe LJ, Vandeloo M, Demonty I et al (2019) Dietary calcium affects body composition and lipid metabolism in rats. PLoS One 14(1):e0210760. https://doi.org/10.1371/journal.pone.0210760

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Soh JF, Bodenstein K, Yu OHY, Linnaranta O, Renaud S, Mahdanian A et al (2022) Atorvastatin lowers serum calcium levels in lithium-users: results from a randomized controlled trial. BMC Endocr Disord 22(1):238. https://doi.org/10.1186/s12902-022-01145-w

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Chou C-W, Fang W-H, Chen Y-Y, Wang C-C, Kao T-W, Wu C-J et al (2020) Association between serum calcium and risk of cardiometabolic disease among community-dwelling adults in Taiwan. Sci Rep 10:3192. https://doi.org/10.1038/s41598-020-60209-w

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Mulet-Cabero AI, Wilde PJ (2023) Role of calcium on lipid digestion and serum lipids: a review. Crit Rev Food Sci Nutr 63(6):813–826. https://doi.org/10.1080/10408398.2021.1954873

    Article  PubMed  CAS  Google Scholar 

  46. Papageorgiou M, Merminod F, Ferrari S, Rizzoli R, Biver E (2022) Associations of calcium intake and calcium from various sources with blood lipids in a population of older women and men with high calcium intake. Nutrients 14(6):1314. https://doi.org/10.3390/nu14061314

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Lee MH, Appleton KM, El-Shewy HM, Sorci-Thomas MG, Thomas MJ, Lopes-Virella MF et al (2017) S1P in HDL promotes interaction between SR-BI and S1PR1 and activates S1PR1-mediated biological functions: calcium flux and S1PR1 internalization. J Lipid Res 58(2):325–338. https://doi.org/10.1038/s41598-020-60209-w

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We gratefully thank all the participants in this study. In addition, we thank the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq), the State of São Paulo Research Foundation (Fundação de Amparo a Pesquisa do Estado de São Paulo—FAPESP), and the Coordination of Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal do Nível Superior—CAPES) for funding support.

Funding

This work was supported by National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq) (Grants numbers: 431053/2016–2 and 406442/2022-3) and the State of São Paulo Research Foundation (Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP) (Grant number: 2018/24069–3). This study was funded in part by the Coordination of Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal do Nível Superior—CAPES) (Grant number 001).

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Authors and Affiliations

  1. Postgraduate Program in Nutrition, Center for Health Sciences, Federal University of Rio Grande do Norte, Av. Senador Salgado Filho 3000 – Lagoa Nova, Natal, Rio Grande do Norte, 59078-900, Brazil

    Melissa Nunes Moia, Francisca Leide da Silva Nunes & Lucia Fátima Campos Pedrosa

  2. Department of Nutrition, Center for Health Sciences, Federal University of Rio Grande do Norte, Av. Senador Salgado Filho 3000 – Lagoa Nova, Natal, Rio Grande do Norte, 59078-900, Brazil

    Severina Carla Vieira Cunha Lima, Clélia de Oliveira Lyra & Karine Cavalcanti Maurício Sena-Evangelista

  3. Postgraduate Program in Collective Health, Health Sciences Center, Federal University of Rio Grande do Norte, Av. Senador Salgado Filho 3000 – Lagoa Nova, Natal, Rio Grande do Norte, 59078-900, Brazil

    Salomão Israel Monteiro Lourenço Queiroz

  4. Department of Nutrition, School of Public Health, University of São Paulo, São Paulo Campus, Av. Dr. Arnaldo, 715 - Cerqueira César, São Paulo, São Paulo, 01246-904, Brazil

    Dirce Maria Lobo Marchioni

  5. Laboratory of Clinical, Toxicological and Bromatological Analysis, Faculty of Pharmaceutical Sciences, University of São Paulo, Ribeirão Preto Campus, Av. Do Café, s/n – Monte Alegre, Ribeirão Preto, São Paulo, 14040-903, Brazil

    Fernando Barbosa Jr

  6. Department of Nutrition, Federal University of Rio Grande do Norte, Av. Senador Salgado Filho 3000 – Lagoa Nova, Natal, Rio Grande do Norte, 59078-900, Brazil

    Karine Cavalcanti Maurício Sena-Evangelista

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  1. Melissa Nunes Moia
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Contributions

KCMSE, FBJ, and MNM conceptualization and design. FLSN, SCVCL, COL, DMLM, and KCMSE investigation and performed research. MNM and FLSN organization and data analysis. FBJ performed chemical element analyses. SIML performed all the statistical analyses. KCMSE and MNM wrote the original draft of the manuscript. SCVCL, COL, DMLM, LFC, and FBJ data interpretation, revision, and correction of the manuscript. COL, DMLM, KCMSE, and FBJ funding acquisition. All the authors approved the final version of the manuscript.

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Correspondence to Karine Cavalcanti Maurício Sena-Evangelista.

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The study was submitted and accepted by the Federal University of Rio Grande do Norte Research Ethics Committee under CAAE number 96294718.4.2001, by the regulated guidelines for research involving human beings (Resolution 466/12 of the National Council of Health).

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Moia, M.N., Lima, S.C.V.C., da Silva Nunes, F.L. et al. Plasma Levels of Magnesium, Calcium, Calcium to Magnesium Ratio, and Associations with Metabolic Syndrome and Cardiometabolic Risk Factors. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-024-04088-6

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