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Evaluation of Oxidative Stress Parameters and Antioxidant Status in Plasma and Erythrocytes of Elderly Diabetic Patients with Sarcopenia

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The journal of nutrition, health & aging

Abstract

Objectives

Oxidative stress may play a role in the pathogenesis of both sarcopenia and diabetes. Although the risk of sarcopenia is increased in people with type 2 diabetes, the relationship between sarcopenia oxidative stress and antioxidant status among the older diabetes population is not well studied. The aim of this present study was to evaluate the relationship between oxidative stress and antioxidant status and sarcopenia in elderly diabetic patients.

Design

This was a cross-sectional designed study with a control group. A total of 60 type 2 diabetic elderly patients were enrolled in the study (30 sarcopenic and 30 controls).

Measurements

Comprehensive geriatric assessments and anthropometric measurements were performed. Sarcopenia was diagnosed according to the European Working Group on Sarcopenia in Older People. Skeletal muscle mass was measured using bioelectrical impedance analysis. A handheld dynamometer was used for skeletal muscle strength measurements. Gait speed was measured using a 4 meter walking test. Plasma malondialdehyde (MDA), glutathione peroxidase (GSH-Px) and erythrocyte MDA, GSH-Px, superoxide dismutase (SOD), catalase and xanthine oxidase (XO) measurements were performed.

Results

While plasma XO was significantly higher in sarcopenic individuals (0.406(0.225-0.775)) compared to controls (0.312(0.112-0.712)) (p=0.006), plasma GSHPx was significantly lower in sarcopenic individuals (0.154(0.101-0.274)) compared to controls (0.204(0.12-.0312)) (p=0.003). Plasma XO (OR: 2.69 (CI 95% 0.13-52.76, p=0.041) and BMI (OR: 0.6 (CI 95% 0.41-0.89, p=0.009) were independently associated with sarcopenia of diabetes in multivariate analysis.

Conclusions

Only plasma XO was found to be independently associated with sarcopenia. XO can be important in the pathogenesis of sarcopenia in diabetes. Oxidative stress and antioxidant status might be associated with sarcopenia in diabetic older individuals but this association seems to be mediated by other factors. Further studies are needed on this subject.

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References

  1. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23. doi:10.1093/ageing/afq034.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y et al. Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing. 2014;43(6):748–59. doi:10.1093/ageing/afu115.

    PubMed  PubMed Central  Google Scholar 

  3. Muscaritoli M, Anker SD, Argiles J, Aversa Z, Bauer JM, Biolo G et al. Consensus definition of sarcopenia, cachexia and pre-cachexia: joint document elaborated by Special Interest Groups (SIG) “cachexia-anorexia in chronic wasting diseases” and “nutrition in geriatrics”. Clin Nutr. 2010;29(2):154–9. doi:10.1016/j.clnu.2009.12.004.

    Article  PubMed  CAS  Google Scholar 

  4. Sorg O. Oxidative stress: a theoretical model or a biological reality? C R Biol. 2004;327(7):649–62.

    Article  PubMed  CAS  Google Scholar 

  5. Meng SJ, Yu LJ. Oxidative stress, molecular inflammation and sarcopenia. Int J Mol Sci. 2010;11(4):1509–26. doi:10.3390/ijms11041509.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Morley JE, Malmstrom TK, Rodriguez-Manas L, Sinclair AJ. Frailty, sarcopenia and diabetes. J Am Med Dir Assoc. 2014;15(12):853–9. doi:10.1016/j.jamda.2014.10.001.

    Article  PubMed  Google Scholar 

  7. Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care. 2007;30(6):1507–12. doi:10.2337/dc06-2537.

    Article  PubMed  Google Scholar 

  8. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep. 2016;6:38937. doi:10.1038/srep38937.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol (1985). 2000;89(2):465–71.

    Article  CAS  Google Scholar 

  10. Dahle LK, Hill EG, Holman RT. The thiobarbituric acid reaction and the autoxidations of polyunsaturated fatty acid methyl esters. Arch Biochem Biophys. 1962;98:253–61.

    Article  PubMed  CAS  Google Scholar 

  11. Durak I, Canbolat O, Kavutcu M, Ozturk HS, Yurtarslani Z. Activities of total, cytoplasmic, and mitochondrial superoxide dismutase enzymes in sera and pleural fluids from patients with lung cancer. J Clin Lab Anal. 1996;10(1):17–20. doi:10.1002/(SICI)1098-2825(1996)10:1<17::AID-JCLA4>3.0.CO;2-I.

    Article  PubMed  CAS  Google Scholar 

  12. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967;70(1):158–69.

    PubMed  CAS  Google Scholar 

  13. Bergmeyer HU. Methods of enzymatic analysis. 2d English ed. Weinheim New York: Verlag Chemie; Academic Press; 1974.

    Google Scholar 

  14. Hashimoto S. A new spectrophotometric assay method of xanthine oxidase in crude tissue homogenate. Anal Biochem. 1974;62(2):426–35.

    Article  PubMed  CAS  Google Scholar 

  15. Lambertucci RH, Levada-Pires AC, Rossoni LV, Curi R, Pithon-Curi TC. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Ageing Dev. 2007;128(3):267–75. doi:10.1016/j.mad.2006.12.006.

    Article  PubMed  CAS  Google Scholar 

  16. Ryan MJ, Jackson JR, Hao Y, Leonard SS, Alway SE. Inhibition of xanthine oxidase reduces oxidative stress and improves skeletal muscle function in response to electrically stimulated isometric contractions in aged mice. Free Radic Biol Med. 2011;51(1):38–52. doi:10.1016/j.freeradbiomed.2011.04.002.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Derbre F, Ferrando B, Gomez-Cabrera MC, Sanchis-Gomar F, Martinez-Bello VE, Olaso-Gonzalez G et al. Inhibition of xanthine oxidase by allopurinol prevents skeletal muscle atrophy: role of p38 MAPKinase and E3 ubiquitin ligases. PLoS One. 2012;7(10):e46668. doi:10.1371/journal.pone.0046668.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Delample D, Durand F, Severac A, Belghith M, Mas E, Michel F et al. Implication of xanthine oxidase in muscle oxidative stress in COPD patients. Free Radic Res. 2008;42(9):807–14. doi:10.1080/10715760802429039.

    Article  PubMed  CAS  Google Scholar 

  19. Ji LL, Dillon D, Wu E. Alteration of antioxidant enzymes with aging in rat skeletal muscle and liver. Am J Physiol. 1990;258(4 Pt 2):R918–23.

    PubMed  CAS  Google Scholar 

  20. Kumaran S, Savitha S, Anusuya Devi M, Panneerselvam C. L-carnitine and DL-alphalipoic acid reverse the age-related deficit in glutathione redox state in skeletal muscle and heart tissues. Mech Ageing Dev. 2004;125(7):507–12. doi:10.1016/j. mad.2004.05.004.

    Article  PubMed  CAS  Google Scholar 

  21. Pansarasa O, Bertorelli L, Vecchiet J, Felzani G, Marzatico F. Age-dependent changes of antioxidant activities and markers of free radical damage in human skeletal muscle. Free Radic Biol Med. 1999;27(5-6):617–22.

    Article  PubMed  CAS  Google Scholar 

  22. Baumann CW, Kwak D, Liu HM, Thompson LV. Age-induced oxidative stress: how does it influence skeletal muscle quantity and quality? J Appl Physiol (1985. 2016;121(5):1047–52. doi:10.1152/japplphysiol.00321.2016.

    Article  CAS  Google Scholar 

  23. Buford TW, Anton SD, Judge AR, Marzetti E, Wohlgemuth SE, Carter CS et al. Models of accelerated sarcopenia: critical pieces for solving the puzzle of age-related muscle atrophy. Ageing Res Rev. 2010;9(4):369–83. doi:10.1016/j.arr.2010.04.004.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Park SW, Goodpaster BH, Strotmeyer ES, de Rekeneire N, Harris TB, Schwartz AV et al. Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes. 2006;55(6):1813–8. doi:10.2337/db05-1183.

    Article  PubMed  CAS  Google Scholar 

  25. Ferrando B, Olaso-Gonzalez G, Sebastia V, Viosca E, Gomez-Cabrera MC, Vina J. [Allopurinol and its role in the treatment of sarcopenia]. Rev Esp Geriatr Gerontol. 2014;49(6):292–8. doi:10.1016/j.regg.2014.05.001.

    Article  PubMed  Google Scholar 

  26. Konishi M, Pelgrim L, Tschirner A, Baumgarten A, von Haehling S, Palus S et al. Febuxostat improves outcome in a rat model of cancer cachexia. J Cachexia Sarcopenia Muscle. 2015;6(2):174–80. doi:10.1002/jcsm.12017.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bravard A, Bonnard C, Durand A, Chauvin MA, Favier R, Vidal H et al. Inhibition of xanthine oxidase reduces hyperglycemia-induced oxidative stress and improves mitochondrial alterations in skeletal muscle of diabetic mice. Am J Physiol Endocrinol Metab. 2011;300(3):E581–91. doi:10.1152/ajpendo.00455.2010.

    Article  PubMed  CAS  Google Scholar 

  28. Agarwal E, Miller M, Yaxley A, Isenring E. Malnutrition in the elderly: a narrative review. Maturitas. 2013;76(4):296–302. doi:10.1016/j.maturitas.2013.07.013.

    Article  PubMed  CAS  Google Scholar 

  29. Rubbieri G, Mossello E, Di Bari M. Techniques for the diagnosis of sarcopenia. Clin Cases Miner Bone Metab. 2014;11(3):181–4.

    PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Geriatric Medicine, Ankara University School of Medicine, Ankara, Turkey

    A. H. E. Küçükdiler, M. Varli, H. Selvi Öztorun & S. Aras

  2. Department of Biochemistry, Ankara University School of Medicine, Ankara, Turkey

    Ö. Yavuz & E. Devrim

  3. Department of Geriatric Medicine, Ataturk’s Research and Training Hospital, Eskibağlar Street, No:47, Safir Life apartments, A block flat no:14, Bağlıca, Etimesgut, Ankara, Turkey

    Ahmet Yalçin

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  1. A. H. E. Küçükdiler
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Correspondence to Ahmet Yalçin.

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Küçükdiler, A.H.E., Varli, M., Yavuz, Ö. et al. Evaluation of Oxidative Stress Parameters and Antioxidant Status in Plasma and Erythrocytes of Elderly Diabetic Patients with Sarcopenia. J Nutr Health Aging 23, 239–245 (2019). https://doi.org/10.1007/s12603-018-1137-y

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  • DOI: https://doi.org/10.1007/s12603-018-1137-y

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