Advertisement

Biological Trace Element Research

, Volume 175, Issue 2, pp 367–374 | Cite as

Early High-Fat Feeding Induces Alteration of Trace Element Content in Tissues of Juvenile Male Wistar Rats

  • Alexey A. TinkovEmail author
  • Eugenia R. Gatiatulina
  • Elizaveta V. Popova
  • Valentina S. Polyakova
  • Anastasia A. Skalnaya
  • Eduard F. Agletdinov
  • Alexandr A. Nikonorov
  • Anatoly V. Skalny
Article

Abstract

The primary objective of the current study was to assess the influence of early high-fat feeding on tissue trace element content in young male Wistar rats. Twenty weanling male Wistar rats were divided into two groups fed standard (STD) or high-fat diet (HFD) containing 10 and 31.6 % of total calories from fat, respectively, for 1 month. Serum lipid spectrum, apolipoproteins, glucose, insulin, adiponectin, and leptin levels were assessed. The level of trace elements was estimated using inductively coupled plasma mass spectrometry. High-fat feeding significantly increased epidydimal (EDAT) and retroperitoneal adipose tissue (RPAT), as well as total adipose tissue mass by 34, 103, and 59 %, respectively. Serum leptin levels in HFD animals were twofold higher than those in the control rats. No significant difference in serum lipid spectrum, apolipoproteins, glucose, adiponectin, and insulin was detected between the groups. HFD significantly altered tissue trace element content. In particular, HFD-fed animals were characterized by significantly lower levels of Cu, I, Mn, Se, and Zn in the liver; Cr, V, Co, Cu, Fe, and I content of EDAT; Co, Cu, I, Cr, V, Fe, and Zn concentration in RPAT samples. At the same time, only serum Cu was significantly depressed in HFD-fed animals as compared to the control ones. Hair Co, Mn, Si, and V levels were significantly increased in comparison to the control values, whereas Se and I content was decreased. HFD feeding induced excessive adiposity and altered tissue trace element content in rats without insulin resistance, adiponectin deficiency, and proatherogenic state. Hypothetically, trace element disbalance may precede obesity-associated metabolic disturbances.

Keywords

Adiposity Chromium Vanadium Adipose tissue Obesity 

Notes

Compliance with Ethical Standards

The protocol of investigation was approved by the Local Ethics Committee. All animal studies have been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    World Health Organization (2015) Obesity and overweight. Fact sheet N 311. Updated January 2015Google Scholar
  2. 2.
    Kelly T, Yang W, Chen CS, Reynolds K, He J (2008) Global burden of obesity in 2005 and projections to 2030. Int J Obes 32(9):1431–1437CrossRefGoogle Scholar
  3. 3.
    Thomas DM, Weedermann M, Fuemmeler BF, et al. (2014) Dynamic model predicting overweight, obesity, and extreme obesity prevalence trends. Obesity 22(2):590–597CrossRefPubMedGoogle Scholar
  4. 4.
    Gard M (2010) The end of the obesity epidemic. RoutledgeGoogle Scholar
  5. 5.
    Han JC, Lawlor DA, Kimm SY (2010) Childhood obesity. Lancet 375(9727):1737–1748CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Wright CM, Parker L, Lamont D, Craft AW (2001) Implications of childhood obesity for adult health: findings from thousand families cohort study. BMJ 323(7324):1280–1284CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Liang Y, Hou D, Zhao X, et al. (2015) Childhood obesity affects adult metabolic syndrome and diabetes. Endocrine 50(1):87–92CrossRefPubMedGoogle Scholar
  8. 8.
    Ebbeling CB, Pawlak DB, Ludwig DS (2002) Childhood obesity: public-health crisis, common sense cure. Lancet 360(9331):473–482CrossRefPubMedGoogle Scholar
  9. 9.
    Fraga CG (2005) Relevance, essentiality and toxicity of trace elements in human health. Mol Asp Med 26(4):235–244CrossRefGoogle Scholar
  10. 10.
    Wiernsperger N, Rapin J (2010) Trace elements in glucometabolic disorders: an update. Diabetol Metab Syndr 2(70):1–9Google Scholar
  11. 11.
    Zafon C, Lecube A, Simo R (2010) Iron in obesity. An ancient micronutrient for a modern disease. Obes Rev 11(4):322–328CrossRefPubMedGoogle Scholar
  12. 12.
    Nikonorov AA, Skalnaya MG, Tinkov AA, Skalny AV (2015) Mutual interaction between iron homeostasis and obesity pathogenesis. J Trace Elem Med Biol 30:207–214CrossRefPubMedGoogle Scholar
  13. 13.
    Skalnaya MG, Demidov VA (2007) Hair trace element contents in women with obesity and type 2 diabetes. J Trace Elem Med Biol 21:59–61CrossRefPubMedGoogle Scholar
  14. 14.
    Wojciak RW, Mojs E, Stanislawska-Kubiak M (2010) Comparison of the hair metals in obese children according to slim therapy. Trace Elem Electrolytes 27(4):192–195CrossRefGoogle Scholar
  15. 15.
    Tascilar ME, Ozgen IT, Abaci A, Serdar M, Aykut O (2011) Trace elements in obese Turkish children. Biol Trace Elem Res 143(1):188–195CrossRefPubMedGoogle Scholar
  16. 16.
    Suliburska J, Cofta S, Gajewska E, et al. (2013) The evaluation of selected serum mineral concentrations and their association with insulin resistance in obese adolescents. Eur Rev Med Pharmacol Sci 17(17):2396–2400PubMedGoogle Scholar
  17. 17.
    Jiao HT, Liu P, Lu WT, Qiao M, Ren XF, Zhang Z (2014) Correlation study between simple obesity and serum concentrations of essential elements. Trace Elem Electrolytes 31(2):53–59CrossRefGoogle Scholar
  18. 18.
    Baltaci AK, Mogulkoc R, Halifeoglu I (2005) Effects of zinc deficiency and supplementation on plasma leptin levels in rats. Biol Trace Elem Res 104(1):41–46CrossRefPubMedGoogle Scholar
  19. 19.
    Król E, Krejpcio Z (2010) Chromium (III) propionate complex supplementation improves carbohydrate metabolism in insulin-resistance rat model. Food Chem Toxicol 48(10):2791–2796CrossRefPubMedGoogle Scholar
  20. 20.
    Tuzcu M, Sahin N, Orhan C, et al. (2011) Impact of chromium histidinate on high fat diet induced obesity in rats. Nutr Metab 8(1):1CrossRefGoogle Scholar
  21. 21.
    Tinkov AA, Popova EV, Polyakova VS, Kwan OV, Skalny AV, Nikonorov AA (2015) Adipose tissue chromium and vanadium disbalance in high-fat fed Wistar rats. J Trace Elem Med Biol 29:176–181CrossRefPubMedGoogle Scholar
  22. 22.
    Tinkov AA, Popova EV, Gatiatulina ER, Skalnaya AA, Yakovenko EN, Alchinova IB, Karganov MY, Skalny AV, Nikonorov AA (2016) Decreased adipose tissue zinc content is associated with metabolic parameters in high fat fed Wistar rats. Acta Sci Pol Technol Aliment 15(1):99–105CrossRefPubMedGoogle Scholar
  23. 23.
    Emoto M, Nishizawa Y, Maekawa K, Hiura Y, Kanda H, Kawagishi T, Shoji T, Okuno Y, Morii H (1999) Homeostasis model assessment as a clinical index of insulin resistance in type 2 diabetic patients treated with sulfonylureas. Diabetes Care 22(5):818–822CrossRefPubMedGoogle Scholar
  24. 24.
    Baumgartner RN, Waters DL, Morley JE, Patrick P, Montoya GD, Garry PJ (1999) Age-related changes in sex hormones affect the sex difference in serum leptin independently of changes in body fat. Metabolism 48(3):378–384CrossRefPubMedGoogle Scholar
  25. 25.
    Cottart CH, Bonvin E, Rey C, et al. (2007) Impact of nutrition on phenotype in CFTR-deficient mice. Pediatr Res 62(5):528–532CrossRefPubMedGoogle Scholar
  26. 26.
    Stern N, Osher E, Greenman Y (2007) Hypoadiponectinemia as a marker of adipocyte dysfunction—part II: the functional significance of low adiponectin secretion. J Cardiometab Syndr 2(4):288–294CrossRefPubMedGoogle Scholar
  27. 27.
    de Ferranti S, Mozaffarian D (2008) The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 54(6):945–955CrossRefPubMedGoogle Scholar
  28. 28.
    Maury E, Brichard SM (2010) Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol Cell Endocrinol 314(1):1–16CrossRefPubMedGoogle Scholar
  29. 29.
    Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27(6):1487–1495CrossRefPubMedGoogle Scholar
  30. 30.
    Do GM, Oh HY, Kwon EY, et al. (2011) Long-term adaptation of global transcription and metabolism in the liver of high-fat diet-fed C57BL/6 J mice. Mol Nutr Food Res 55(S2):S173–S185CrossRefPubMedGoogle Scholar
  31. 31.
    Relling DP, Esberg LB, Fang CX, et al. (2006) High-fat diet-induced juvenile obesity leads to cardiomyocyte dysfunction and upregulation of Foxo3a transcription factor independent of lipotoxicity and apoptosis. J Hypertens 24(3):549–561CrossRefPubMedGoogle Scholar
  32. 32.
    Nishikawa S, Yasoshima A, Doi K, Nakayama H, Uetsuka K (2007) Involvement of sex, strain and age factors in high fat diet-induced obesity in C57BL/6 J and BALB/cA mice. Exp Anim 56(4):263–272CrossRefPubMedGoogle Scholar
  33. 33.
    Ghibaudi L, Cook J, Farley C, Heek M, Hwa JJ (2002) Fat intake affects adiposity, comorbidity factors, and energy metabolism of Sprague-Dawley rats. Obes Res 10(9):956–963CrossRefPubMedGoogle Scholar
  34. 34.
    Song M, Schuschke DA, Zhou Z, et al. (2012) High fructose feeding induces copper deficiency in Sprague–Dawley rats: a novel mechanism for obesity related fatty liver. J Hepatol 56(2):433–440CrossRefPubMedGoogle Scholar
  35. 35.
    Kennedy ML, Failla ML, Smith JJC (1986) Influence of genetic obesity on tissue concentrations of zinc, copper, manganese and iron in mice. J Nutr 116(8):1432–1441PubMedGoogle Scholar
  36. 36.
    Donaldson DL, Smith CC, Koh E (1987) Effects of obesity and diabetes on tissue zinc and copper concentrations in the Zucker rat. Nutr Res 7(4):393–399CrossRefGoogle Scholar
  37. 37.
    Feldman A, Aigner E, Weghuber D, Paulmichl K (2015) The potential role of iron and copper in pediatric obesity and nonalcoholic fatty liver disease. BioMed Res Int. doi: 10.1155/2015/287401 Google Scholar
  38. 38.
    Tinkov AA, Polyakova VS, Nikonorov AA (2013) Chronic administration of iron and copper potentiates adipogenic effect of high fat diet in Wistar rats. Biometals 26(3):447–463CrossRefPubMedGoogle Scholar
  39. 39.
    Lima SCVC, Arrais RF, Sales CH, et al. (2006) Assessment of copper and lipid profile in obese children and adolescents. Biol Trace Elem Res 114(1–3):19–29CrossRefPubMedGoogle Scholar
  40. 40.
    Sánchez C, López-Jurado M, Aranda P, Llopis J (2010) Plasma levels of copper, manganese and selenium in an adult population in southern Spain: influence of age, obesity and lifestyle factors. Sci Total Environ 408(5):1014–1020CrossRefPubMedGoogle Scholar
  41. 41.
    Obeid O, Elfakhani M, Hlais S, et al. (2008) Plasma copper, zinc, and selenium levels and correlates with metabolic syndrome components of lebanese adults. Biol Trace Elem Res 123(1–3):58–65CrossRefPubMedGoogle Scholar
  42. 42.
    Hua Y, Clark S, Ren J, Sreejayan N (2012) Molecular mechanisms of chromium in alleviating insulin resistance. J Nutr Biochem 23(4):313–319CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Srivastava AK, Mehdi MZ (2005) Insulino-mimetic and anti-diabetic effects of vanadium compounds. Diabet Med 22(1):2–13CrossRefPubMedGoogle Scholar
  44. 44.
    Tinkov AA, Sinitskii AI, Popova EV, Nemereshina ON, Gatiatulina ER, Skalnaya MG, Skalny AV, Nikonorov AA (2015b) Alteration of local adipose tissue trace element homeostasis as a possible mechanism of obesity-related insulin resistance. Med Hypotheses 85(3):343–347CrossRefPubMedGoogle Scholar
  45. 45.
    Furukawa S, Fujita T, Shimabukuro M, et al. (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 114(12):1752–1761CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Thomson CD (2004) Assessment of requirements for selenium and adequacy of selenium status: a review. Eur J Clin Nutr 58(3):391–402CrossRefPubMedGoogle Scholar
  47. 47.
    Kaidar-Person O, Person B, Szomstein S, Rosenthal RJ (2008) Nutritional deficiencies in morbidly obese patients: a new form of malnutrition? Obes Surg 18(8):1028–1034CrossRefPubMedGoogle Scholar
  48. 48.
    Beems RB (1986) Dietary selenium-and benzo [a] pyrene-induced respiratory tract tumours in hamsters. Carcinogenesis 7(3):485–489CrossRefPubMedGoogle Scholar
  49. 49.
    Mahfouz MM, Kummerow FA (2000) Cholesterol-rich diets have different effects on lipid peroxidation, cholesterol oxides, and antioxidant enzymes in rats and rabbits. J Nutr Biochem 11(5):293–302CrossRefPubMedGoogle Scholar
  50. 50.
    Ramadan KS, Yousef JM, Hamza AH, Abdel SE (2013) Antioxidant and protective effects of selenium against metabolic syndrome induced by high fructose in rats. IJAST 3(5):45–54Google Scholar
  51. 51.
    Biondi B (2010) Thyroid and obesity: an intriguing relationship. J Clin Endocrinol Metab 95(8):3614–3617CrossRefPubMedGoogle Scholar
  52. 52.
    Brito PD, Ramos CF, Passos MCF, Moura EG (2006) Adaptive changes in thyroid function of female rats fed a high-fat and low-protein diet during gestation and lactation. Braz J Med Biol Res 39(6):809–816CrossRefPubMedGoogle Scholar
  53. 53.
    Lin WH, Chen MD, Lin PY (1992) Investigation of the profile of selected trace metals in genetically obese (ob/ob) and lean (+/?) mice. J Formos Med Assoc 91:S27-33PubMedGoogle Scholar
  54. 54.
    Tallman DL, Noto AD, Taylor CG (2009) Low and high fat diets inconsistently induce obesity in C57BL/6 J mice and obesity compromises n-3 fatty acid status. Lipids 44(7):577–580CrossRefPubMedGoogle Scholar
  55. 55.
    Charradi K, Elkahoui S, Karkouch I, Limam F, Hassine FB, El May MV, Aouani E (2014) Protective effect of grape seed and skin extract against high-fat diet-induced liver steatosis and zinc depletion in rat. Dig Dis Sci 59(8):1768–1778CrossRefPubMedGoogle Scholar
  56. 56.
    do NascimentoMarreiro D, Fisberg M, SMF C (2004) Zinc nutritional status and its relationships with hyperinsulinemia in obese children and adolescents. Biol Trace Elem Res 100(2):137–149CrossRefGoogle Scholar
  57. 57.
    Ozata M, Mergen M, Oktenli C, et al. (2002) Increased oxidative stress and hypozincemia in male obesity. Clin Biochem 35(8):627–631CrossRefPubMedGoogle Scholar
  58. 58.
    Choi MK, Lee SH, Kim SK (2014) Relationship between adiposity-related biomarkers and calcium, magnesium, iron, copper, and zinc in young adult men with different degrees of obesity. Trace Elem Electrolytes 31(4):148–155CrossRefGoogle Scholar
  59. 59.
    Yanoff LB, Menzie CM, Denkinger B, Sebring NG, McHugh T, Remaley AT, Yanovski JA (2007) Inflammation and iron deficiency in the hypoferremia of obesity. Int J Obes 31(9):1412–1419CrossRefGoogle Scholar
  60. 60.
    Suliburska J (2013) A six-week diet high in fat, fructose and salt and its influence on lipid and mineral status in rats. Acta Sci Pol Technol Aliment 12:195–202Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Alexey A. Tinkov
    • 1
    • 2
    • 3
    Email author
  • Eugenia R. Gatiatulina
    • 1
  • Elizaveta V. Popova
    • 1
  • Valentina S. Polyakova
    • 4
  • Anastasia A. Skalnaya
    • 5
  • Eduard F. Agletdinov
    • 6
  • Alexandr A. Nikonorov
    • 1
    • 2
  • Anatoly V. Skalny
    • 2
    • 3
    • 7
  1. 1.Department of BiochemistryOrenburg State Medical UniversityOrenburgRussia
  2. 2.Institute of Bioelementology (Russian Satellite Centre of Trace Element – Institute for UNESCO)Orenburg State UniversityOrenburgRussia
  3. 3.Laboratory of Biotechnology and Applied BioelementologyYaroslavl State UniversityYaroslavlRussia
  4. 4.Department of Pathologic AnatomyOrenburg State Medical UniversityOrenburgRussia
  5. 5.Faculty of Fundamental MedicineLomonosov Moscow State UniversityMoscowRussia
  6. 6.Central Research LaboratoryBashkir State Medical UniversityUfaRussia
  7. 7.All-Russian Research Institute of Medicinal and Aromatic Plants (VILAR)MoscowRussia

Personalised recommendations