Advertisement

A Search for Similar Patterns in Hair Trace Element and Mineral Content in Children with Down’s Syndrome, Obesity, and Growth Delay

  • Andrey R. Grabeklis
  • Anatoly V. SkalnyEmail author
  • Olga P. Ajsuvakova
  • Anastasia A. Skalnaya
  • Anna L. Mazaletskaya
  • Svetlana V. Klochkova
  • Susan J. S. Chang
  • Dmitry B. Nikitjuk
  • Margarita G. Skalnaya
  • Alexey A. Tinkov
Article
  • 36 Downloads

Abstract

The objective of the present study was to perform comparative analysis of hair trace element and mineral levels in children with Down’s syndrome, growth delay, and obesity in order to reveal common and specific patterns. Hair Zn (14, 7, and 15%), Ca (38%, 24%, and 47%), and Mg (33%, 31%, and 49%) levels in children with Down’s syndrome, obesity, and growth delay were lower than the respective control values. At the same time, patients with Down’s syndrome and growth delay were characterized by 27% and 21%, as well as 24% and 20% lower hair Co as well as Cu content than healthy examinees. Certain alterations were found to be disease-specific. Particularly, in Down’s syndrome children, hair Cr, Fe, and V levels were significantly lower, whereas hair P content exceeded the control values. Obese children were characterized by significantly increased hair Cr content. At the same time, hair Mn and Si levels in children with growth delay were lower as compared with the controls. In regression models, all three studied diseases were considered as negative predictors of hair Cu content. Down’s syndrome and growth delay, but not obesity, were inversely associated with hair Co content. Both Down’s syndrome and obesity were inversely associated with hair Zn content. Based on the revealed similarities in altered hair element, content it is proposed that deficiency of essential elements may predispose Down’s syndrome patients to certain syndrome comorbidities including growth delay and obesity, although further detailed studies are required.

Keywords

Trisomy 21 Zinc Copper Cobalt Comorbidity 

Notes

Funding Information

The current investigation is supported by the Russian Foundation for Basic Research within project no. 18-013-01026.

Compliance with ethical standards

The present study was performed in agreement with the ethical standards set in the Declaration of Helsinki (1964) and its later amendments. The protocol of the investigation was approved by the Institutional Ethics Committee (Yaroslavl State University, Yaroslavl, Russia). Informed consent was obtained from the parents, who were informed about the study. All procedures involving children (hair sampling, anthropometric analysis) were performed in presence of parents or their legal representatives.

Conflict of interest

The authors declare no conflict of interest

References

  1. 1.
    Kazemi M, Salehi M, Kheirollahi M (2016) Down syndrome: current status, challenges and future perspectives. Int J Mol Cell Med 5(3):125PubMedPubMedCentralGoogle Scholar
  2. 2.
    Asim A, Kumar A, Muthuswamy S, Jain S, Agarwal S (2015) Down syndrome: an insight of the disease. J Biomed Sci 22(1):41.  https://doi.org/10.1186/s12929-015-0138-y CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Geelhoed EA, Bebbington A, Bower C, Deshpande A, Leonard H (2011) Direct health care costs of children and adolescents with Down syndrome. J Pediatr 159(4):541–545.  https://doi.org/10.1016/j.jpeds.2011.06.007 CrossRefPubMedGoogle Scholar
  4. 4.
    Bertapelli F, Pitetti K, Agiovlasitis S, Guerra-Junior G (2016) Overweight and obesity in children and adolescents with Down syndrome—prevalence, determinants, consequences, and interventions: A literature review. Res Dev Disabil 57:181–192.  https://doi.org/10.1016/j.ridd.2016.06.018 CrossRefPubMedGoogle Scholar
  5. 5.
    Basil JS, Santoro SL, Martin LJ, Healy KW, Chini BA, Saal HM (2016) Retrospective study of obesity in children with Down syndrome. J Pediatr 173:143–148.  https://doi.org/10.1016/j.jpeds.2016.02.046 CrossRefPubMedGoogle Scholar
  6. 6.
    Myrelid Å, Gustafsson J, Ollars B, Annerén G (2002) Growth charts for Down’s syndrome from birth to 18 years of age. Arch Dis Child 87(2):97–103.  https://doi.org/10.1136/adc.87.2.97 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Grammatikopoulou MG, Manai A, Tsigga M, Tsiligiroglou-Fachantidou A, Galli-Tsinopoulou A, Zakas A (2008) Nutrient intake and anthropometry in children and adolescents with Down syndrome–a preliminary study. Dev Neurorehabil 11(4):260–267.  https://doi.org/10.1080/17518420802525526 CrossRefPubMedGoogle Scholar
  8. 8.
    Saghazadeh A, Mahmoudi M, Ashkezari AD, Rezaie NO, Rezaei N (2017) Systematic review and meta-analysis shows a specific micronutrient profile in people with Down syndrome: lower blood calcium, selenium and zinc, higher red blood cell copper and zinc, and higher salivary calcium and sodium. PloS one 12(4):e0175437.  https://doi.org/10.1371/journal.pone.0175437 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Grabeklis AR, Skalny AV, Skalnaya AA, Zhegalova IV, Notova SV, Mazaletskaya AL, Skalnaya MG, Tinkov AA (2019) Hair mineral and trace element content in children with Down’s syndrome. Biol Trace Elem Res 188(1):230–238CrossRefGoogle Scholar
  10. 10.
    Mazurek D, Wyka J (2015) Down syndrome-genetic and nutritional aspects of accompanying disorders. Rocz Panstw Zakl Hig 66(3).Google Scholar
  11. 11.
    Ram G, Chinen J (2011) Infections and immunodeficiency in Down syndrome. Clin Exp Immunol 164(1):9–16.  https://doi.org/10.1111/j.1365-2249.2011.04335.x CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Malakooti N, Pritchard MA, Adlard PA, Finkelstein DI Role of metal ions in the cognitive decline of Down syndrome. Front. Aging Neurosci 6:136.  https://doi.org/10.3389/fnagi.2014.00136
  13. 13.
    Romano C, Pettinato R, Ragusa L, Barone C, Alberti A, Failla P (2002) Is there a relationship between zinc and the peculiar comorbidities of Down syndrome? Downs Syndr Res Pract 8(1):25–28.  https://doi.org/10.3104/reports.126 CrossRefPubMedGoogle Scholar
  14. 14.
    Ani C, Grantham-McGregor S, Muller D (2000) Nutritional supplementation in Down syndrome: theoretical considerations and current status. Dev Med Child Neurol 42(3):207–213.  https://doi.org/10.1017/s0012162200000359 CrossRefPubMedGoogle Scholar
  15. 15.
    Thiel R, Fowkes S (2005) Can cognitive deterioration associated with Down syndrome be reduced? Med Hypotheses 64(3):524–532.  https://doi.org/10.1016/j.mehy.2004.08.020 CrossRefPubMedGoogle Scholar
  16. 16.
    Salman MS (2002) Systematic review of the effect of therapeutic dietary supplements and drugs on cognitive function in subjects with Down syndrome. Eur J Paediatr Neurol 6(4):213–219.  https://doi.org/10.1053/ejpn.2002.0596 CrossRefPubMedGoogle Scholar
  17. 17.
    Ishihara K, Akiba S (2017) A comprehensive diverse ‘-omics’ approach to better understanding the molecular pathomechanisms of Down syndrome. Brain Sci 7(4):44.  https://doi.org/10.3390/brainsci7040044 CrossRefPubMedCentralGoogle Scholar
  18. 18.
    Barlow PJ, Sylvester PE, Dickerson JW (1981) Hair trace metal levels in Down syndrome patients. J Ment Defic Res 25(Pt 3):161–168.  https://doi.org/10.1111/j.1365-2788.1981.tb00106.x CrossRefPubMedGoogle Scholar
  19. 19.
    Yenigun A, Ozkinay F, Cogulu O, Coker C, Cetiner N, Ozden G, Aksu O, Ozkinay C (2004) Hair zinc level in Down syndrome. Downs Syndr Res Pract 9(2):53–57.  https://doi.org/10.3104/reports.292 CrossRefPubMedGoogle Scholar
  20. 20.
    Anneren G, Johansson E, Lindh U (1985) Trace element profiles in individual blood cells from patients with Down’s syndrome. Acta Pædiatrica 74(2):259–263.  https://doi.org/10.1111/j.1651-2227.1985.tb10961.x CrossRefGoogle Scholar
  21. 21.
    Kadrabová J, Madáriĉ A, Šustrová M, Ginter E (1996) Changed serum trace element profile in Down’s syndrome. Biol Trace Elem Res 54(3):201–206.  https://doi.org/10.1007/bf02784431 CrossRefPubMedGoogle Scholar
  22. 22.
    Monteiro CP, Varela A, Pinto M, Neves J, Felisberto GM, Vaz C, Bicho MP, Laires MJ (1997) Effect of an aerobic training on magnesium, trace elements and antioxidant systems in a Down syndrome population. Magnes Res 10(1):65–71PubMedGoogle Scholar
  23. 23.
    Nève J, Sinet P, Molle L, Nicole A (1983) Selenium, zinc and copper in Down’s syndrome (trisomy 21): blood levels and relations with glutathione peroxidase and superoxide dismutase. Clinica Chimica Acta 133(2):209–214.  https://doi.org/10.1016/0009-8981(83)90406-0 CrossRefGoogle Scholar
  24. 24.
    Lima AS, Cardoso BR, Cozzolino SF (2010) Nutritional status of zinc in children with Down syndrome. Biol Trace Elem Res 133(1):20–28.  https://doi.org/10.1007/s12011-009-8408-8 CrossRefPubMedGoogle Scholar
  25. 25.
    Kanavin ØJ, Aaseth J, Birketvedt GS Thyroid hypofunction in Down’s syndrome: is it related to oxidative stress? Biol Trace Elem Res 78(1-3):35–42.  https://doi.org/10.1385/bter:78:1-3:35 CrossRefGoogle Scholar
  26. 26.
    Baltaci AK, Mogulkoc R, Akil M, Bicer M (2016) Selenium: its metabolism and relation to exercise. Pak J Pharm Sci 29:1719–1725PubMedGoogle Scholar
  27. 27.
    Dixon NE, Crissman BG, Smith PB, Zimmerman SA, Worley G, Kishnani PS (2010) Prevalence of iron deficiency in children with Down syndrome. J Pediatr 157(6):967–971.  https://doi.org/10.1016/j.jpeds.2010.06.011 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Culp-Hill R, Zheng C, Reisz JA, Smith K, Rachubinski A, Nemkov T, Butcher E, Granrath R, Hansen KC, Espinosa JM (2017) Red blood cell metabolism in Down syndrome: hints on metabolic derangements in aging. Blood Adv 1(27):2776–2780.  https://doi.org/10.1182/bloodadvances.2017011957 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Jacobs J, Schwartz A, McDougle CJ, Skotko BG (2016) Rapid clinical deterioration in an individual with Down syndrome. Am J Med Genet P A 170(7):1899–1902.  https://doi.org/10.1002/ajmg.a.37674 CrossRefGoogle Scholar
  30. 30.
    Torsdottir G, Kristinsson J, Hreidarsson S, Snaedal J, Johannesson T (2001) Copper, ceruloplasmin and superoxide dismutase (SOD1) in patients with Down’s syndrome. Pharmacol Toxicol 89(6):320–325.  https://doi.org/10.1034/j.1600-0773.2001.d01-168.x CrossRefPubMedGoogle Scholar
  31. 31.
    Meguid NA, Dardir AA, El-Sayed EM, Ahmed HH, Hashish AF, Ezzat A (2010) Homocysteine and oxidative stress in Egyptian children with Down syndrome. Clin Biochem 43(12):963–967.  https://doi.org/10.1016/j.clinbiochem.2010.04.058 CrossRefPubMedGoogle Scholar
  32. 32.
    Del Baldo G, Marabini C, Albano V, Lionetti M, Gatti S (2016) Imerslund–Grasbeck Syndrome (selective B12 malabsorption): think about it also in Down’s syndrome! Dig Liver Dis 48:e274.  https://doi.org/10.1016/j.dld.2016.08.088 CrossRefGoogle Scholar
  33. 33.
    Guéant J-L, Guéant-Rodriguez R-M, Anello G, Bosco P, Brunaud L, Romano C, Ferri R, Romano A, Candito M, Namour B (2003) Genetic determinants of folate and vitamin B12 metabolism: a common pathway in neural tube defect and Down syndrome? Clin Chem Lab Med 41(11):1473–1477.  https://doi.org/10.1515/cclm.2003.226 CrossRefPubMedGoogle Scholar
  34. 34.
    Palekar AG (2001) Preconceptional intake of folate and vitamin B12 in the prevention of neural tube defects and Down syndrome. Am J Obstet Gynecol 184(3):517.  https://doi.org/10.1067/mob.2001.110953 CrossRefPubMedGoogle Scholar
  35. 35.
    Anneren G, Gebre-Medhin M (1987) Trace elements and transport proteins in serum of children with Down syndrome and of healthy siblings living in the same environment. Human nutrition. Clin Nutr 41(4):291–299Google Scholar
  36. 36.
    Cutress T (1972) Composition, flow-rate and pH of mixed and parotid salivas from trisomic 21 and other mentally retarded subjects. Arch Oral Biol 17:1081–1094.  https://doi.org/10.1016/0003-9969(72)90183-5 CrossRefPubMedGoogle Scholar
  37. 37.
    Stagi S, Lapi E, Romano S, Bargiacchi S, Brambilla A, Giglio S, Seminara S, de Martino M (2015) Determinants of vitamin D levels in children and adolescents with Down syndrome. Int J Endocrinol.  https://doi.org/10.1155/2015/896758 CrossRefGoogle Scholar
  38. 38.
    Roizen NJ, Patterson D (2003) Down’s syndrome. The Lancet 361(9365):1281–1289.  https://doi.org/10.1016/s0140-6736(03)12987-x CrossRefGoogle Scholar
  39. 39.
    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.  https://doi.org/10.1016/j.jtemb.2007.09.019 CrossRefPubMedGoogle Scholar
  40. 40.
    Fatani SH, Saleh SAK, Adly HM, Abdulkhaliq AA (2016) Trace element alterations in the hair of diabetic and obese women. Biol Trace Elem Res 174(1):32–39.  https://doi.org/10.1007/s12011-016-0691-6 CrossRefPubMedGoogle Scholar
  41. 41.
    Wójciak R, Mojs E, Stanislawska-Kubiak M (2010) Comparison of the hair metals in obese children according to slim therapy. Trace Elem Electroly 27(4).  https://doi.org/10.5414/tep27192 CrossRefGoogle Scholar
  42. 42.
    Baltaci AK, Mogulkoc R, Baltaci SB (2019) The role of zinc in the endocrine system. Pak J Pharm Sci 32(1).Google Scholar
  43. 43.
    García O, Ronquillo D, del Carmen CM, Martínez G, Camacho M, López V, Rosado J Zinc, iron and vitamins A, C and E are associated with obesity, inflammation, lipid profile and insulin resistance in mexican school-aged children. Nutrients 5, 12:5012–5030.  https://doi.org/10.3390/nu5125012 CrossRefGoogle Scholar
  44. 44.
    Kelishadi R, Hashemipour M, Adeli K, Tavakoli N, Movahedian-Attar A, Shapouri J, Poursafa P, Rouzbahani A (2010) Effect of zinc supplementation on markers of insulin resistance, oxidative stress, and inflammation among prepubescent children with metabolic syndrome. Metab Syndr Relat Disord 8(6):505–510.  https://doi.org/10.1089/met.2010.0020 CrossRefPubMedGoogle Scholar
  45. 45.
    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. Diabetes Care 28(5):1175–1181.  https://doi.org/10.2337/diacare.28.5.1175 CrossRefPubMedGoogle Scholar
  46. 46.
    ul Hassan SA, Ahmed I, Nasrullah A, Haq S, Ghazanfar H, Sheikh AB, Zafar R, Askar G, Hamid Z, Khushdil A (2017) Comparison of serum magnesium levels in overweight and obese children and normal weight children. Cureus 9(8).  https://doi.org/10.7759/cureus.1607
  47. 47.
    Zaakouk AM, Hassan MA, Tolba OA (2016) Serum magnesium status among obese children and adolescents. Gaz Egypt Paediatr Assoc 64(1):32–37.  https://doi.org/10.1016/j.epag.2015.11.002 CrossRefGoogle Scholar
  48. 48.
    Niranjan G, Anitha D, Srinivasan AR, Velu VK, Venkatesh C, Babu MS, Saha S (2014) Association of inflammatory sialoproteins, lipid peroxides and serum magnesium levels with cardiometabolic risk factors in obese children of South Indian population. Int J Biomed Sci 10(2):118PubMedPubMedCentralGoogle Scholar
  49. 49.
    Farhanghi MA, Mahboob S, Ostadrahimi A (2009) Obesity induced magnesium deficiency can be treated by vitamin D supplementation. J Pak Med Assoc 59(4):258–261PubMedGoogle Scholar
  50. 50.
    Wiechuła D, Loska K, Ungier D, Fischer A (2012) Chromium, zinc and magnesium concentrations in the pubic hair of obese and overweight women. Biol Trace Elem Res 148(1):18–24.  https://doi.org/10.1007/s12011-012-9339-3 CrossRefPubMedGoogle Scholar
  51. 51.
    Kim HN, Song SW (2014) Concentrations of chromium, selenium, and copper in the hair of viscerally obese adults are associated with insulin resistance. Biol Trace Elem Res 158(2):152–157.  https://doi.org/10.1007/s12011-014-9934-6 CrossRefPubMedGoogle Scholar
  52. 52.
    Hasan HG, Ismael PA, Tofiq DI (2012) Estimation of serum chromium levels in obesity. Middle East J Intern Med 5(5):3–9.  https://doi.org/10.5742/mejim.2011.55148 CrossRefGoogle Scholar
  53. 53.
    Ngala RA, Awe MA, Nsiah P The effects of plasma chromium on lipid profile, glucose metabolism and cardiovascular risk in type 2 diabetes mellitus. A case - control study. PLoS ONE 13(7):e0197977.  https://doi.org/10.1371/journal.pone.0197977 CrossRefGoogle Scholar
  54. 54.
    Cozzolino SMF, Marreiro DDN, Fisberg M Zinc nutritional status in obese children and adolescents. Biol Trace Elem Res 86(2):107–122.  https://doi.org/10.1385/bter:86:2:107 CrossRefGoogle Scholar
  55. 55.
    Fan Y, Zhang C, Bu J Relationship between selected serum metallic elements and obesity in children and adolescent in the U.S. Nutrients 9(2):104.  https://doi.org/10.3390/nu9020104 CrossRefGoogle Scholar
  56. 56.
    Yakinci G, Paç A, Fz K, Tayfun M, Gül A (1997) Serum zinc, copper, and magnesium levels in obese children. Pediatr Int 39(3):339–341.  https://doi.org/10.1111/j.1442-200x.1997.tb03748.x CrossRefGoogle Scholar
  57. 57.
    Błażewicz A, Klatka M, Astel A, Partyka M, Kocjan R (2013) Differences in trace metal concentrations (Co, Cu, Fe, Mn, Zn, Cd, and Ni) in whole blood, plasma, and urine of obese and nonobese children. Biol Trace Elem Res 155(2):190–200.  https://doi.org/10.1007/s12011-013-9783-8 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Suliburska J, Bogdański P, Pupek-Musialik D, Krejpcio Z (2011) Dietary intake and serum and hair concentrations of minerals and their relationship with serum lipids and glucose levels in hypertensive and obese patients with insulin resistance. Biol Trace Elem Res 139(2):137–150.  https://doi.org/10.1007/s12011-010-8650-0 CrossRefPubMedGoogle Scholar
  59. 59.
    Nikonorov AA, Skalnaya MG, Tinkov AA, Skalny AV (2015) Mutual interaction between iron homeostasis and obesity pathogenesis. J Trace Elem Med Biol 30:207–214.  https://doi.org/10.1016/j.jtemb.2014.05.005 CrossRefPubMedGoogle Scholar
  60. 60.
    Klatka M, Błażewicz A, Partyka M, Kołłątaj W, Zienkiewicz E, Kocjan R (2015) Concentration of selected metals in whole blood, plasma, and urine in short stature and healthy children. Biol Trace Elem Res 166(2):142–148.  https://doi.org/10.1007/s12011-015-0262-2 CrossRefPubMedGoogle Scholar
  61. 61.
    Ozmen H, Akarsu S, Polat F, Cukurovali A (2013) The levels of calcium and magnesium, and of selected trace elements, in whole blood and scalp hair of children with growth retardation. Iran J Pediatr 23(2):125PubMedPubMedCentralGoogle Scholar
  62. 62.
    Tabatadze T, Zhorzholiani L, Kherkheulidze M, Karseladze R, Ivanashvili T (2015) Association between short stature and hair elements. Georg Med News 247:25–30Google Scholar
  63. 63.
    Han TH, Lee J, Kim YJ (2016) Hair zinc level analysis and correlative micronutrients in children presenting with malnutrition and poor growth. Pediatr Gastroenterol Hepatol Nutr 19(4):259–268.  https://doi.org/10.5223/pghn.2016.19.4.259 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Imdad A, Bhutta ZA (2011) Effect of preventive zinc supplementation on linear growth in children under 5 years of age in developing countries: a meta-analysis of studies for input to the lives saved tool. BMC Public Health 11(3):S22.  https://doi.org/10.1186/1471-2458-11-s3-s22 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Şıklar Z, Tuna C, Dallar Y, Tanyer G (2003) Zinc deficiency: a contributing factor of short stature in growth hormone deficient children. J Trop Pediatr 49(3):187–188.  https://doi.org/10.1093/tropej/49.3.187 CrossRefPubMedGoogle Scholar
  66. 66.
    Uriu-Adams JY, Scherr RE, Lanoue L, Keen CL (2010) Influence of copper on early development: prenatal and postnatal considerations. BioFactors 36(2):136–152.  https://doi.org/10.1002/biof.85 CrossRefPubMedGoogle Scholar
  67. 67.
    Yang W, Wang J, Liu L, Zhu X, Wang X, Liu Z et al (2011) Effect of high dietary copper on somatostatin and growth hormone-releasing hormone levels in the hypothalami of growing pigs. Biol Trace Elem Res 143(2):893–900.  https://doi.org/10.1007/s12011-010-8904-x CrossRefPubMedGoogle Scholar
  68. 68.
    Roughead ZK, Lukaski HC (2003) Inadequate copper intake reduces serum insulin-like growth factor-I and Bone strength in growing rats Fed graded amounts of copper and zinc. J Nutr 133(2):442–448.  https://doi.org/10.1093/jn/133.2.44 CrossRefPubMedGoogle Scholar
  69. 69.
    Barbosa NO, Okay TS, Leone CR (2005) Magnesium and intrauterine growth restrictioN. J Am Coll Nutr 24(1):10–15.  https://doi.org/10.1080/07315724.2005.10719437 CrossRefPubMedGoogle Scholar
  70. 70.
    Rude R, Gruber H, Wei L, Frausto A, Mills B (2003) Magnesium deficiency: effect on bone and mineral metabolism in the mouse. Calcif Tissue Int 72(1):32–41.  https://doi.org/10.1007/s00223-001-1091-1 CrossRefPubMedGoogle Scholar
  71. 71.
    Baltaci AK, Yuce K (2018) Zinc transporter proteins. Neurochem Res 43:517–530CrossRefGoogle Scholar
  72. 72.
    Miletta MC, Schöni MH, Kernland K, Mullis PE, Petkovic V (2013) The role of zinc dynamics in growth hormone secretion. Horm Res Paediatr 80(6):381–389.  https://doi.org/10.1159/000355408 CrossRefPubMedGoogle Scholar
  73. 73.
    Adamo AM, Oteiza PI (2010) Zinc deficiency and neurodevelopment: the case of neurons. BioFactors 36(2):117–124.  https://doi.org/10.1002/biof.91 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Baltaci AK, Mogulkoc R (2012) Leptin and zinc relation: in regulation of food intake and immunity. Indian J Endocrinol Metab 16:611–616CrossRefGoogle Scholar
  75. 75.
    Olechnowicz J, Tinkov A, Skalny A, Suliburska J (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31.  https://doi.org/10.1007/s12576-017-0571-7 CrossRefPubMedGoogle Scholar
  76. 76.
    Gaier E, Eipper B, Mains R (2012) Copper signaling in the mammalian nervous system: synaptic effects. J Neurosci Res 91(1):2–19.  https://doi.org/10.1002/jnr.23143 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Kodama H, Fujisawa C, Bhadhprasit W (2012) Inherited copper transport disorders: biochemical mechanisms, diagnosis, and treatment. Curr Drug Metab 13(3):237–250.  https://doi.org/10.2174/138920012799320455 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Komiya Y, Su LT, Chen HC, Habas R, Runnels LW (2014) Magnesium and embryonic development. In: Molecular, Genetic, and Nutritional Aspects of Major and Trace Minerals (pp. 343-351). Academic Press. doi:  https://doi.org/10.1684/mrh.2014.0356 PubMedPubMedCentralGoogle Scholar
  79. 79.
    Lingam I, Robertson NJ (2018) Magnesium as a neuroprotective agent: a review of its use in the fetus, term infant with neonatal encephalopathy, and the adult stroke patient. Dev Neurosci 40(1):1–12.  https://doi.org/10.1159/000484891 CrossRefPubMedGoogle Scholar
  80. 80.
    Slutsky I, Abumaria N, Wu LJ, Huang C, Zhang L, Li B, Zhao X, Govindarajan A, Zhao MG, Zhuo M (2010) Enhancement of learning and memory by elevating brain magnesium. Neuron 65(2):165–177.  https://doi.org/10.1016/j.neuron.2009.12.026 CrossRefPubMedGoogle Scholar
  81. 81.
    Dørup I, Flyvbjerg A, Everts ME, Clausen T (1991) Role of insulin-like growth factor-1 and growth hormone in growth inhibition induced by magnesium and zinc deficiencies. Br J Nutr 66(3):505–521.  https://doi.org/10.1079/bjn19910051 CrossRefPubMedGoogle Scholar
  82. 82.
    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 CrossRefPubMedGoogle Scholar
  83. 83.
    Bertinato J, Lavergne C, Rahimi S, Rachid H, Vu N, Plouffe L, Swist E Moderately low magnesium intake impairs growth of lean body mass in obese-prone and obese-resistant rats fed a high-energy diet. Nutrients 8(5):253.  https://doi.org/10.3390/nu8050253 CrossRefGoogle Scholar
  84. 84.
    Skalny AV, Zaitseva IP, Gluhcheva YG, Skalny AA, Achkasov EE, Skalnaya MG, Tinkov AA (2018) Cobalt in athletes: hypoxia and doping – new crossroads. J Appl Biomed.  https://doi.org/10.32725/jab.2018.003 CrossRefGoogle Scholar
  85. 85.
    Guéant J-L, Caillerez-Fofou M, Battaglia-Hsu S, Alberto J-M, Freund J-N, Dulluc I, Adjalla C, Maury F, Merle C, Nicolas J-P (2013) Molecular and cellular effects of vitamin B12 in brain, myocardium and liver through its role as co-factor of methionine synthase. Biochimie 95(5):1033–1040.  https://doi.org/10.1016/j.biochi.2013.01.020 CrossRefPubMedGoogle Scholar
  86. 86.
    Roman-Garcia P, Quiros-Gonzalez I, Mottram L, Lieben L, Sharan K, Wangwiwatsin A, Tubio J, Lewis K, Wilkinson D, Santhanam B (2014) Vitamin B12–dependent taurine synthesis regulates growth and bone mass. J Clin Invest 124(7):2988–3002.  https://doi.org/10.1172/jci72606 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Vincent JB (2014) Is chromium pharmacologically relevant? J Trace Elem Med Biol 28(4):397–405.  https://doi.org/10.1016/j.jtemb.2014.06.020 CrossRefPubMedGoogle Scholar
  88. 88.
    Thompson KH, Orvig C (2004) Vanadium compounds in the treatment of diabetes. Met Ions Biol Syst 41:221–252PubMedGoogle Scholar
  89. 89.
    Tinkov AA, Sinitskii AI, Popova EV, Nemereshina ON, Gatiatulina ER, Skalnaya MG, Skalny AV, Nikonorov AA (2015) Alteration of local adipose tissue trace element homeostasis as a possible mechanism of obesity-related insulin resistance. Med Hypotheses 85(3):343–347.  https://doi.org/10.1016/j.mehy.2015.06.005 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Andrey R. Grabeklis
    • 1
    • 2
  • Anatoly V. Skalny
    • 1
    • 2
    • 3
    Email author
  • Olga P. Ajsuvakova
    • 1
    • 2
    • 3
  • Anastasia A. Skalnaya
    • 4
  • Anna L. Mazaletskaya
    • 1
  • Svetlana V. Klochkova
    • 3
  • Susan J. S. Chang
    • 5
    • 6
  • Dmitry B. Nikitjuk
    • 3
    • 7
  • Margarita G. Skalnaya
    • 1
    • 2
    • 3
  • Alexey A. Tinkov
    • 1
    • 2
    • 3
  1. 1.Yaroslavl State UniversityYaroslavlRussia
  2. 2.Peoples’ Friendship University of Russia (RUDN University)MoscowRussia
  3. 3.IM Sechenov First Moscow State Medical University (Sechenov University)MoscowRussia
  4. 4.Research Center of NeurologyMoscowRussia
  5. 5.College of NutritionTaipei Medical UniversityTaipeiTaiwan
  6. 6.Nutrition Research CenterTaipei Medical University HospitalTaipeiTaiwan
  7. 7.The Federal Research Centre of Nutrition, Biotechnology and Food SafetyMoscowRussia

Personalised recommendations