Skip to main content
SpringerLink
Log in

Assesment of oxidative status and its association with thyroid autoantibodies in patients with euthyroid autoimmune thyroiditis

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Oxidative stress results from either overproduction of free radicals or insufficiency of several anti-oxidant defense systems. It leads to oxidation of main cellular macromolecules and a resultant molecular dysfunction. Thyroid hormones regulate oxidative metabolism and, thus, play a role in free radical production. Studies evaluating oxidative stress in patients with hypothyroidism and hyperthyroidism have been encountered in recent years; however, oxidative status in patients with euthyroid autoimmune thyroiditis (AIT) was not investigated previously. Thirty-five subjects with euthyroid AIT and 35 healthy controls were enrolled in the study. Serum oxidative status was determined by the measurement of total anti-oxidant status (TAS), total oxidant status (TOS), ischemia-modified albumin (IMA), and oxidized-low density lipoprotein (ox-LDL) levels. Serum TAS levels were significantly lower (p < 0.001), while serum TOS levels and IMA levels were significantly higher (p < 0.001 and p = 0.020, respectively) in patients compared to controls. In both groups, ox-LDL levels were similar (p = 0.608). Serum TAS levels were negatively correlated with anti-thyroid peroxidase and anti-thyroglobulin (anti-TG) levels (rho = −0.415, p = 0.001 and rho = −0.484, p < 0.001, respectively). Serum TOS was positively correlated with anti-TG levels (rho = 0.547, p < 0.001). Further, TAS was positively correlated with free T4 levels (r = 0.279, p = 0.043). No correlation was observed between thyrotropin, free T3 levels, and TOS and TAS levels. These results suggest that oxidants are increased, and anti-oxidants are decreased in patients with euthyroid AIT, and oxidative/anti-oxidative balance is shifted to the oxidative side. Increased oxidative stress might have a role in thyroid autoimmunity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. L. Oziol, P. Faure, N. Bertrand, P. Chomard, Inhibition of in vitro macrophage-induced low density lipoprotein oxidation by thyroid compounds. J. Endocrinol. 177(1), 137–146 (2003)

    Article  CAS  PubMed  Google Scholar 

  2. B. Halliwell, Free radicals, antioxidants and human disease: curiosity, cause or consequence? Lancet 344(8924), 721–724 (1994)

    Article  CAS  PubMed  Google Scholar 

  3. L. Dumitriu, R. Bartoc, H. Ursu, M. Purice, V. Lonescu, Significance of high levels of serum malonyl dialdehyde (MDA) and ceruloplasmin (CP) in hyper- and hypothyroidism. Endocrinologie 26(1), 35–38 (1988)

    CAS  PubMed  Google Scholar 

  4. F. Costantini, S.D. Pierdomenico, D. De Cesare, P. De Remigis, T. Bucciarelli, G. Bittolo-Bon, G. Cazzolato, G. Nubile, M.T. Guanano, S. Sensi, F. Cuccurullo, A. Mezzetti, Effect of thyroid function on LDL oxidation. Arterioscler. Thromb. Vasc. Biol. 18(5), 732–737 (1998)

    Article  CAS  PubMed  Google Scholar 

  5. J.M. Gutteridge, Free radicals in disease processes: a compilation of cause and consequence. Free Radic. Res. Commun. 19(3), 141–158 (1993)

    Article  CAS  PubMed  Google Scholar 

  6. I. Fridovich, Superoxide anion radical (O2-), superoxide dismutases, and related matters. J. Biol. Chem. 272(30), 18515–18517 (1997)

    Article  CAS  PubMed  Google Scholar 

  7. B.S. Berlett, E.R. Stadtman, Protein oxidation in aging, disease and oxidative stress. J. Biol. Chem. 272(33), 20313–20316 (1997)

    Article  CAS  PubMed  Google Scholar 

  8. O. Erel, A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 37(4), 277–285 (2004)

    Article  CAS  PubMed  Google Scholar 

  9. S.G. Ma, W. Xu, C.L. Wei, X.J. Wu, B. Hong, Z.J. Wang, H.R. Hao, H.Q. Guo, Role of ischemia-modified albumin and total homocysteine in estimating symptomatic lacunar infarction in type 2 diabetic patients. Clin. Biochem. 44(16), 1299–1303 (2011)

    Article  CAS  PubMed  Google Scholar 

  10. S. Turedi, O. Cinar, I. Yavuz, A. Mentese, A. Gunduz, S.C. Karahan, M. Topbas, E. Cevik, A.O. Yildirim, A. Uzun, U. Kaldirim, Differences in ischemia-modified albumin levels between end stage renal disease patients and the normal population. J. Nephrol. 23(3), 335–340 (2010)

    PubMed  Google Scholar 

  11. C.Y. Chen, W.L. Tsai, P.J. Lin, S.C. Shiesh, The value of serum ischemia-modified albumin for assessing liver function in patients with chronic liver disease. Clin. Chem. Lab. Med. 49(11), 1817–1821 (2011)

    Article  CAS  PubMed  Google Scholar 

  12. D. Bar-Or, G. Curtis, N. Rao, N. Bampos, E. Lau, Characterization of the Co(2+) and Ni(2+) binding amino-acid residues of the N-terminus of human albumin. Eur. J. Biochem. 268(1), 42–47 (2001)

    Article  CAS  PubMed  Google Scholar 

  13. S. Gidenne, F. Ceppa, E. Fontan, F. Perrier, P. Burnat, Analytical performance of the albumin cobalt binding (ACB) test on the Cobas MIRA Plus analyzer. Clin. Chem. Lab. Med. 42(4), 455–461 (2004)

    Article  CAS  PubMed  Google Scholar 

  14. H. Esterbauer, G. Wag, H. Puhl, Lipid peroxidation and its role in atherosclerosis. Br. Med. Bull. 49(3), 566–576 (1993)

    CAS  PubMed  Google Scholar 

  15. D. Steinberg, S. Parthasarathy, T.E. Carew, J.C. Khoo, J.L. Witztum, Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N. Eng. J. Med. 320(14), 915–924 (1989)

    Article  CAS  Google Scholar 

  16. A.N. Torun, S. Kulaksizoglu, M. Kulaksizoglu, B.O. Pamuk, E. Isbilen, N.B. Tutuncu, Serum total antioxidant status and lipid peroxidation marker malondialdehyde levels in overt and subclinical hypothyroidism. Clin. Endocrinol. (Oxf) 70(3), 469–474 (2009)

    Article  Google Scholar 

  17. M. Aslan, N. Cosar, H. Celik, N. Aksoy, A.C. Dulger, H. Begenik, Y.U. Soyoral, M.E. Kucukoglu, S. Selek, Evaluation of oxidative status in patients with hyperthyroidism. Endocrine 40(2), 285–289 (2011)

    Article  CAS  PubMed  Google Scholar 

  18. K. Ersoy, İ. Anaforoglu, E. Algün, Serum ischemic modified albumin levels might not be a marker of oxidative stress in patients with hypothyroidism. Endocrine 43(2), 430–433 (2013)

    Article  CAS  PubMed  Google Scholar 

  19. S.G. Ma, L.X. Yang, F. Bai, W. Xu, B. Hong, Ischemia-modified albumin in patients with hyperthyroidism and hypothyroidism. Eur. J. Intern. Med. 23(6), 136–140 (2012)

    Article  Google Scholar 

  20. M. Lampka, R. Junik, A. Nowicka, E. Kopczyńska, T. Tyrakowski, G. Odrowaz-Sypniewska, Oxidative stress markers during a course of hyperthyroidism. Endokrynol. Pol. 57(3), 218–222 (2006)

    PubMed  Google Scholar 

  21. A. Oge, E. Sozmen, A.O. Karaoglu, Effect of thyroid function on LDL oxidation in hypothyroidism and hyperthyroidism. Endocr. Res. 30(3), 481–489 (2004)

    Article  CAS  PubMed  Google Scholar 

  22. O. Erel, A new automated colorimetric method for measuring total oxidant status. Clin. Biochem. 38(12), 1103–1111 (2005)

    Article  CAS  PubMed  Google Scholar 

  23. D. Bar-Or, E. Lau, J.V. Winkler, A Novel assay for cobalt-albumin binding and its potential as a marker for myocardial ischemia- a preliminary report. J. Emerg. Med. 19(4), 311–315 (2000)

    Article  CAS  PubMed  Google Scholar 

  24. G. Lippi, M. Montagnana, G.L. Salvagno, G.C. Guidi, Standardization of ischemia-modified albumin testing: adjustment for serum albumin. Clin. Chem. Lab. Med. 45(2), 261–262 (2007)

    Article  CAS  PubMed  Google Scholar 

  25. M.J. Coria, A.I. Pastán, M.S. Gimenez, Serum oxidative stress parameters of women with hypothyroidism. Acta Biomed. 80(2), 135–139 (2009)

    PubMed  Google Scholar 

  26. H. Erdamar, B. Cimen, H. Gülcemal, R. Saraymen, B. Yerer, H. Demirci, Increased lipid peroxidation and impaired enzymatic antioxidant defense mechanism in thyroid tissue with multinodular goiter and papillary carcinoma. Clin. Biochem. 43(7–8), 650–654 (2010)

    Article  CAS  PubMed  Google Scholar 

  27. L.E. Laatikainen, M.D. Castellone, A. Hebrant, C. Hoste, M.C. Cantisani, J.P. Laurila, G. Salvatore, P. Salerno, F. Basolo, J. Näsman, J.E. Dumont, M. Santoro, M.O. Laukkanen, Extracellular superoxide dismutase is a thyroid differentiation marker down-regulated in cancer. Endocr. Relat. Cancer 17(3), 785–796 (2010)

    Article  CAS  PubMed  Google Scholar 

  28. O. Young, T. Crotty, R. O’Connell, J. O’Sullivan, A.J. Curran, Levels of oxidative damage and lipid peroxidation in thyroid neoplasia. Head Neck 32(6), 750–756 (2010)

    PubMed  Google Scholar 

  29. E. Carmeli, A. Bachar, S. Barchad, M. Morad, J. Merrick, Antioxidant status in the serum of persons with intellectual disability and hypothyroidism: a pilot study. Res. Dev. Disabil. 29(5), 431–438 (2008)

    Article  PubMed  Google Scholar 

  30. A. Saad-Hussein, H. Hamdy, H.M. Aziz, H. Mahdy-Abdallah, Thyroid functions in paints production workers and the mechanism of oxidative-antioxidants status. Toxicol. Ind. Health 27(3), 257–263 (2011)

    Article  CAS  PubMed  Google Scholar 

  31. C. Marcocci, L. Bartalena, Role of oxidative stress and selenium in Graves’ hyperthyroidism and orbitopathy. J. Endocrinol. Invest. 36(10 Suppl), 15–20 (2013)

    CAS  PubMed  Google Scholar 

  32. A. Kaur, S. Pandey, S. Kumar, A.A. Mehdi, A. Mishra, Oxidative stress profile in graves’ ophthalmopathy in Indian patients. Orbit 29(2), 97–101 (2010)

    Article  PubMed  Google Scholar 

  33. B. Pereira, L.F. Rosa, D.A. Safi, E.L. Bechara, R. Curi, Control of superoxide dismutase, catalase and glutathione peroxidase activities in rat lymphoid organs by thyroid hormones. J. Endocrinol. 140(1), 73–77 (1994)

    Article  CAS  PubMed  Google Scholar 

  34. A. Swaroop, T. Ramasarma, Heat exposure and hypothyroid conditions decrease hydrogen peroxide generation in liver mitochondria. Biochem. J. 226(2), 403–408 (1985)

    PubMed Central  CAS  PubMed  Google Scholar 

  35. V.S. Reddy, S. Gouroju, M.M. Suchitra, V. Suresh, A. Sachan, P.V. Srinivasa Rao, A.R. Bitla, Antioxidant defense in overt and subclinical hypothyroidism. Horm. Metab. Res. 45(10), 754–758 (2013)

    Article  CAS  PubMed  Google Scholar 

  36. M. Kaçmaz, M. Atmaca, A. Arslan, H. Demir, M.F. Ozbay, Oxidative stress in patients with thyroidectomy and thyroparathyroidectomy under replacement therapy. Endocrine. (2014). doi:10.1007/s12020-014-0270-6

  37. M. Oncel, A. Kıyıcı, S. Onen, Evaluation of the Relationship Between Ischemia-Modified Albumin Levels and Thyroid Hormone Levels. J. Clin. Lab. Anal. (2014). doi:10.1002/jcla.21789

    PubMed  Google Scholar 

  38. N.I. Krinsky, Mechanism of action of biological antioxidants. Proc. Soc. Exp. Biol. Med. 200(2), 248–254 (1992)

    Article  CAS  PubMed  Google Scholar 

  39. B. Halliwell, J.M. Gutteridge, Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186, 1–85 (1990)

    Article  CAS  PubMed  Google Scholar 

  40. U. Resch, G. Helsel, F. Tatzber, H. Sinzinger, Antioxidant status in thyroid dysfunction. Clin. Chem. Lab. Med. 40(11), 1132–1134 (2002)

    Article  CAS  PubMed  Google Scholar 

  41. V. Sundaram, A.N. Hanna, L. Koneru, H.A. Newman, J.M. Falko, Both hypothyroidism and hyperthyroidism enhance low density lipoprotein oxidation. J. Clin. Endocrinol. Metab. 82(10), 3421–3424 (1997)

    CAS  PubMed  Google Scholar 

  42. T. Diekman, P.N. Demacker, J.J. Kastelein, A.F. Stalenhoef, W.M. Wiersinga, Increased oxidizability of low-density lipoproteins in hypothyroidism. J. Clin. Endocrinol. Metab. 83(5), 1752–1755 (1998)

    Article  CAS  PubMed  Google Scholar 

  43. B.T. Kurien, H. Scofield, Autoimmunity and oxidatively modified autoantigens. Autoimmun. Rev. 7(7), 567–573 (2008)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. D. Shah, N. Mahajan, S. Sah, S.K. Nath, B. Paudyal, Oxidative stress and its biomarkers in systemic lupus erythematosus. J. Biomed. Sci. 21, 23 (2014)

    Article  PubMed Central  PubMed  Google Scholar 

  45. N.C. Laddha, M. Dwivedi, M.S. Mansuri, A.R. Gani, M. Ansarullah, A.V. Ramachandran, S. Dalai, R. Begum, Vitiligo: interplay between oxidative stress and immune system. Exp. Dermatol. 22(4), 245–250 (2013)

    Article  CAS  PubMed  Google Scholar 

  46. B. Zhang, C. Lo, L. Shen, R. Sood, C. Jones, K. Cusmano-Ozog, S. Park-Snyder, W. Wong, M. Jeng, T. Cowan, E.G. Engleman, J.L. Zehnder, The role of vanin-1 and oxidative stress-related pathways in distinguishing acute and chronic pediatric ITP. Blood 117(17), 4569–4579 (2011)

    Article  CAS  PubMed  Google Scholar 

  47. M.M. Delmastro, J.D. Piganelli, Oxidative stess and redox modulation potential in type 1 diabetes. Clin. Dev. Immunol. 2011, 593863 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  48. R. Rostami, M.R. Aghasi, A. Mohammadi, J. Nourooz-Zadeh, Enhanced oxidative stress in Hashimoto’s thyroiditis: inter-relationships to biomarkers of thyroid function. Clin. Biochem. 46(4–5), 308–312 (2013)

    Article  CAS  PubMed  Google Scholar 

  49. G. Vitale, S. Salvioli, C. Franceschi, Oxidative stress and the ageing endocrine system. Nat. Rev. Endocrinol. 9(4), 228–240 (2013)

    Article  CAS  PubMed  Google Scholar 

  50. P. Mitrou, S.A. Raptis, G. Dimitriadis, Thyroid disease in older people. Maturitas 70(1), 5–9 (2011)

    Article  PubMed  Google Scholar 

  51. C. Duthoit, V. Estienne, A. Giraud, J.M. Durand-Gorde, A.K. Rasmussen, U. Feldt-Rasmussen, P. Carayon, J. Ruf, Hydrogen peroxide-induced production of a 40 kDa immunoreactive thyroglobulin fragment in human thyroid cells: the onset of thyroid autoimmunity? Biochem. J. 360(Pt 3), 557–562 (2001)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. C.L. Burek, N.R. Rose, Autoimmune thyroiditis and ROS. Autoimmun. Rev. 7(7), 530–537 (2008)

    Article  CAS  PubMed  Google Scholar 

  53. B. Poljsak, D. Suput, I. Milisav, Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxid. Med. Cell. Longev. (2013). doi:10.1155/2013/956792

    PubMed Central  PubMed  Google Scholar 

  54. B. Halliwell, The wanderings of a free radical. Free Radic. Biol. Med. 46(5), 531–542 (2009)

    Article  CAS  PubMed  Google Scholar 

  55. K. Schlesier, M. Harwat, V. Böhm, R. Bitsch, Assessment of antioxidant activity by using different in vitro methods. Free Radic. Res. 36(2), 177–187 (2002)

    Article  CAS  PubMed  Google Scholar 

  56. R.L. Prior, G. Cao, In vivo total antioxidant capacity: comparison of different analytical methods. Free Radic. Biol. Med. 27(11–12), 1173–1181 (1999)

    Article  CAS  PubMed  Google Scholar 

  57. D. Wang, J.F. Feng, P. Zeng, Y.H. Yang, J. Luo, Y.W. Yang, Total oxidant/antioxidant status in sera of patients with thyroid cancers. Endocr. Relat. Cancer 18(6), 773–782 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Standards

This study approved by the local ethical committee (Approval date and number- 26.12.2012/2012-75).

Author information

Authors and Affiliations

  1. Department of Endocrinology and Metabolism, Konya Education and Research Hospital, Meram, Konya, Turkey

    Husniye Baser

  2. Department of Biochemistry, Konya Education and Research Hospital, Konya, Turkey

    Ummugulsum Can

  3. Department of Internal Medicine, Konya Education and Research Hospital, Konya, Turkey

    Salih Baser, Uysaler Aslan & Bahauddin Taha Hidayetoglu

  4. Department of Biochemistry, Faculty of Medicine, Necmettin Erbakan University, Konya, Turkey

    Fatma Humeyra Yerlikaya

Authors
  1. Husniye Baser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ummugulsum Can
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Salih Baser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fatma Humeyra Yerlikaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Uysaler Aslan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bahauddin Taha Hidayetoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Husniye Baser.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baser, H., Can, U., Baser, S. et al. Assesment of oxidative status and its association with thyroid autoantibodies in patients with euthyroid autoimmune thyroiditis. Endocrine 48, 916–923 (2015). https://doi.org/10.1007/s12020-014-0399-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-014-0399-3

Keywords

Search

Navigation