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Endocrine

, Volume 62, Issue 2, pp 440–447 | Cite as

An assessment of the relationship between thyroid nodule characteristics, insulin resistance and arterial stiffness in euthyroid nodular goiter

  • Yasemin Aydoğan
  • Mustafa Altay
  • Oktay Ünsal
  • Veysel Kaplanoğlu
  • Yavuz Çağır
  • Canan Yıldız
  • Esin Beyan
  • Selma Uysal Ramadan
Original Article
  • 33 Downloads

Abstract

Objectives

Publications suggesting that thyroid nodule might be associated with insulin resistance and metabolic syndrome are quite interesting. There is a need for studies assessing the relationship between nodule presence and cardiovascular risk in individuals with non-functioning nodular goiter. The purpose of the present study is to reveal whether or not insulin resistance, nodule presence, and nodule stiffness affect arterial stiffness, which is a reliable and valid cardiovascular risk indicator, in individuals with euthyroid nodular goiter using the pulse wave analysis (PWA).

Materials and methods

50 patients with euthyroid nodular goiter and 50 healthy volunteers were included in the study. All participants were examined by B-mode thyroid ultrasound, and the participants in the nodular goiter group were also examined by strain elastography (SE). The strain index of nodules was calculated according to the Rago scoring. Also, fasting plasma glucose (FPG) and insulin levels were measured, and HOMA-IR. Arterial stiffness measurements of the participants were performed using a PWA device which employs a cuff-based oscillometric method from the brachial artery.

Results

PWV was found to be significantly higher in the euthyroid nodular goiter group (p < 0.001). PWV was found to be positively correlated with FPG and waist circumference. Fasting plasma glucose was found to be higher in the group with nodular goiter (p = 0.03). However, no difference was found between the groups in terms of HOMA-IR and insulin level. HOMA-IR was not correlated with thyroid volume, nodule volume, and nodule count. Also, HOMA-IR was not correlated with strain index value and PWA data.

Conclusion

We found that PWV was significantly higher in patients with euthyroid nodular goiter. This result suggests that these patients may be at risk for cardiovascular disease.

Keywords

Euthyroid nodular goiter Insulin resistance Strain index Pulse wave velocity 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Research Ethics Committee of University of Health Sciences, Keçiören SUAM (date 13.04.2016 and reference number 1124). All the methods used in the study were carried out in accordance with the approved guidelines and Declaration of Helsinki, Ethical Principles for Medical Research Involving Human Subjects.

References

  1. 1.
    H. Studer, M. Derwahl, Mechanisms of nonneoplastic endocrine hyperplasia—a changing concept: A review focused on the thyroid gland. Endocr. Rev. 16, 411–426 (1995)PubMedGoogle Scholar
  2. 2.
    K. Westermark, F.A. Karlsson, B. Westermark, Thyrotropin modulates EGF receptor function in porcine thyroid follicle cells. Mol. Cell. Endocrinol. 40, 17–23 (1985)CrossRefPubMedGoogle Scholar
  3. 3.
    M.C. Eggo, W.J. King, E.G. Black, M.C. Sheppard, Functional human thyroid cells and their insulin-like growth factor-binding proteins: Regulation by thyrotropin cyclic 3’,5’ adenosine monophosphate, and growth factors. J. Clin. Endocrinol. Metab. 81, 3056–3062 (1996)PubMedGoogle Scholar
  4. 4.
    R. Burikhanov, K. Coulonval, I. Pirson, F. Lamy, J.E. Dumont, P.P. Roger, Thyrotropin via cyclic AMP induces insulin receptor expression and growth factor signaling pathways in dog thyroid epithelial cells. J. Biol. Chem. 271, 29400–29406 (1996)CrossRefPubMedGoogle Scholar
  5. 5.
    N.W. Cheung, S.C. Boyages, The thyroid gland in acromegaly: An ultrasonographic study. Clin. Endocrinol. 46, 545–549 (1997)CrossRefGoogle Scholar
  6. 6.
    T. Kimura, A. Van Keymeulen, J. Golstein, A. Fusco, J.E. Dumont, P.P. Roger, Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr. Rev. 22, 631–656 (2001)CrossRefPubMedGoogle Scholar
  7. 7.
    J. Shin, M.H. Kim, K.H. Yoon et al. Relationship between metabolic syndrome and thyroid nodules in healthy Koreans. Korean J. Intern. Med. 31(1), 98–105 (2016)CrossRefPubMedGoogle Scholar
  8. 8.
    Z. Heidari, M.A. Mashhadi, S. Nosratzehi, Insulin resistance in patients with benign thyroid nodules. Arch. Iran. Med. 18(9), 572–576 (2015)PubMedGoogle Scholar
  9. 9.
    P. Nahon, G. Thabut, M. Ziol, M.T. Htar, F. Cesaro, N. Barget et al. Liver stiffness measurement versus clinicians’ prediction or both for the assessment of liver fibrosis in patients with chronic hepatitis C. Am. J. Gastroenterol. 101, 2744–2751 (2006)CrossRefPubMedGoogle Scholar
  10. 10.
    A. Gotschy, E. Bauer, C. Schrodt, G. Lykowsky, Y.X. Ye, E. Rommel et al. Local arterial stiffening assessed by MRI precedes atherosclerotic plaque formation. Circ. Cardiovasc. Imag. 6, 916–923 (2013)CrossRefGoogle Scholar
  11. 11.
    J. Blacher, B. Pannier, A.P. Guerin, S.J. Marchais, M.E. Safar, G.M. London, Carotid arterial stiffness as a predictor of cardiovascular and all-cause mortality in end-stage renal disease. Hypertension 32, 570–574 (1998)CrossRefPubMedGoogle Scholar
  12. 12.
    J. Wuerfel, F. Paul, B. Beierbach, U. Hamhaber, D. Klatt, S. Papazoglou et al. MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuroimage 49, 2520–2525 (2010)CrossRefPubMedGoogle Scholar
  13. 13.
    M.J. Paszek, N. Zahir, K.R. Johnson, J.N. Lakins, G.I. Rozenberg, A. Gefen et al. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8, 241–254 (2005)CrossRefPubMedGoogle Scholar
  14. 14.
    M.F. Berry, A.J. Engler, Y.J. Woo, T.J. Pirolli, L.T. Bish, V. Jayasankar et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290, H2196–H2203 (2006)CrossRefPubMedGoogle Scholar
  15. 15.
    A.J. Engler, S. Sen, H.L. Sweeney, D.E. Discher, Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006)CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    C.M. Lo, H.B. Wang, M. Dembo, Y.L. Wang, Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144–152 (2000)CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    M.L. Previtera, C.G. Langhammer, B.L. Firestein, Effects of substrate stiffness and cell density on primary hippocampal cultures. J. Biosci. Bioeng. 110, 459–470 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    M.L. Previtera, A. Sengupta, Substrate stiffness regulates proinflammatory mediator production through TLR4 activity in macrophages. PLoS ONE 10(12), e0145813 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    A.B. Dabrowa, M. Wierzbicka, J.H. Goch, Proinflammatory cytokines in cardiovascular diseases as potential therapeutic target. Wiad. Lek. 60(9–10), 433–438 (2007)Google Scholar
  20. 20.
    T. Akkan, M. Altay, Y. Ünsal, M. Dağdeviren, E. Beyan, Nonfunctioning adrenal incidentaloma affecting central blood pressure and arterial stiffness parameters. Endocrine 58(3), 513–520 (2017)CrossRefPubMedGoogle Scholar
  21. 21.
    T. Sehestedt, J. Jeppesen, T.W. Hansen et al. Risk prediction is improved by adding markers of subclinical organ damage to SCORE. Eur. Heart J. 31(7), 883–891 (2010)CrossRefPubMedGoogle Scholar
  22. 22.
    T. Weber, S. Wassertheurer, M. Rammer, A. Haiden, B. Hametner, B. Eber, Wave reflections, assessed with a novel method for pulse wave separation, are associated with end-organ damage and clinical outcomes. Hypertension 60, 534–541 (2012)CrossRefPubMedGoogle Scholar
  23. 23.
    C. Vlachopoulos, K. Aznaouridis, C. Stefanadis, Prediction of cardiovascular events and all-cause mortality with arterial stiffness. A systematic review and meta-analysis. J. Am. Coll. Cardiol. 55(13), 1318–1327 (2010)CrossRefPubMedGoogle Scholar
  24. 24.
    Y. Ben-Shlomo, M. Spears, C. Boustred et al. Aortic pulse wave velocity improves cardiovascular event prediction: An individual participant meta-analysis of prospective observational data from 17,635 subjects. J. Am. Coll. Cardiol. 63(7), 636–646 (2014)CrossRefPubMedGoogle Scholar
  25. 25.
    B. Hametner, S. Wassertheurer, J. Kropf, C. Mayer, B. Eber, T. Weber, Oscillometric estimation of aortic pulse wave velocity: Comparison with intra-aortic catheter measurements. Blood Press. Monit. 18(3), 173–176 (2013)CrossRefPubMedGoogle Scholar
  26. 26.
    S. Wassertheurer, J. Kropf, T. Weber et al. A new oscillometric method for pulse wave analysis: comparison with a common tonometric method. J. Hum. Hypertens. 24(8), 498–504 (2010)CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    D.R. Matthews, J.P. Hosker, S.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: İnsülin resistance and beta cell function from fasting plasma glucose and insülin concentrations in man. Diabetologia 28(7), 412–419 (1985)CrossRefPubMedGoogle Scholar
  28. 28.
    A. Şişik, F. Başak, E. Köse, Tiroid nodüllerine güncel yaklaşım: “2015 ATA” ve “2016 AACE/ACE/AME” kılavuzları derlemesi. Arch. Clin. Exp. Med. 2, 18–23 (2017)CrossRefGoogle Scholar
  29. 29.
    M. Haksever, Tiroit İnce İğne Aspirasyon Biyopsisi ve Sitopatolog Klinisyen İletişimi. Kocatepe Tıp Derg. 15(3), 349–354 (2014)Google Scholar
  30. 30.
    C. Li, E.S. Ford, L.C. McGuire, A.H. Mokdad, R.R. Little, G.M. Reaven, Trends in hyperinsulinemia among nondiabetic adults in the U.S. Diabetes Care 29, 2396–2402 (2006). 26CrossRefPubMedGoogle Scholar
  31. 31.
    J. Rezzonico, M. Rezzonico, E. Pusiol, F. Pitoia, H. Niepomniszcze, Introducing the thyroid gland as another victim of the insulin resistance syndrome. Thyroid 18, 461–464 (2008)CrossRefPubMedGoogle Scholar
  32. 32.
    J. Rezzónico, M. Rezzónico, E. Pusiol, F. Pitoia, H. Niepomniszcze, High prevalence of thyroid nodules in patients with achrocordons(skin tags). Possib. role Insul. -Resist. Med. 69(3), 302–304 (2009)Google Scholar
  33. 33.
    R. Burikhanov, K. Coulonval, I. Pirson, F. Lamy, J.E. Dumont, P.P. Roger, Thyrotropin via cyclic AMP induces insulin receptor expression and insulin co stimulation of growth and amplifies insulin and insulin like growth factor signaling pathways in dog thyroid epithelial cells. J. Biol. Chem. 271, 29400–29406 (1996)CrossRefPubMedGoogle Scholar
  34. 34.
    N.W. Cheung, S.C. Boyages, The thyroid gland in acromegaly: An ultrasonographic study. Clin. Endocrinol. 46, 545–549 (1997)CrossRefGoogle Scholar
  35. 35.
    T. Kimura, J.E. Dumont, A. Fusco, J. Golstein, Insulin and TSH promote growth in size of PC Cl3 rat thyroid cells, possibly via a pathway different from DNA synthesis: Comparison with FRTL-5 cells. Endocr. Rev. 22, 631–656 (2001)CrossRefPubMedGoogle Scholar
  36. 36.
    C. Anıl, A. Kut, B. Atesagaoglu et al. Metformin decreases thyroid volume and nodule size in subjects with insulin resistance. A preliminary study. Med. Princ. Pract. 25, 233–236 (2015)CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Duran O.A., Anıl C., Gürsoy A. et al. Thyroid volume in patients with glucose metabolism disorders. Arq. Bras. Endocrinol. Metab. 58(8), 824–827 (2014)CrossRefGoogle Scholar
  38. 38.
    O.A. Duran, C. Anıl, A. Gürsoy et al. The relationship between glucose metabolism disorders and malignant thyroid disease. Int. J. Clin. Oncol. 18, 585–589 (2013)CrossRefPubMedGoogle Scholar
  39. 39.
    A. Lyshchik, T. Higashi, R. Asato et al. Thyroid gland tumor diagnosis at US elastography. Radiology 237, 202–211 (2005)CrossRefPubMedGoogle Scholar
  40. 40.
    D. Huang, M. Refaat, K. Mohammedi et al. Macrovascular complications in patients with diabetes and prediabetes. Biomed. Res. Int. 2017, 7839101 (2017)PubMedPubMedCentralGoogle Scholar
  41. 41.
    B. Brannick, S. Dagogo-Jack, Prediabetes and cardiovascular disease: Pathophysiology and interventions for prevention and risk reduction. Endocrinol. Metab. Clin. North. Am. 47(1), 33–50 (2018)CrossRefPubMedGoogle Scholar
  42. 42.
    A.G. Dagre, J.P. Lekakis, T.G. Papaioannou et al. Arterial stiffness is increased in subjects with hypothyroidism. Int. J. Cardiol. 103, 1–6 (2005)CrossRefPubMedGoogle Scholar
  43. 43.
    T. Nagasaki, M. Inaba, Y. Kumeda et al. Decrease of arterial stiffness at common carotid artery in hypothyroid patients by normalization of thyroid function. Biomed. Pharmacother. 59, 8–14 (2005)CrossRefPubMedGoogle Scholar
  44. 44.
    E.A. Palmieri, S. Fazio, V. Palmieri et al. Myocardial contractility and total arterial stiffness in patients with overt hyperthyroidism: acute effects of beta1-adrenergic blockade. Eur. J. Endocrinol. 150, 757–762 (2004)CrossRefPubMedGoogle Scholar
  45. 45.
    T. Nagasaki, M. Inaba, Y. Kumeda et al. Increased pulse wave velocity in subclinical hypothyroidism. J. Clin. Endocrinol. Metab. 91, 154–158 (2006)CrossRefPubMedGoogle Scholar
  46. 46.
    M.D. Gammage, J.V. Parle, R.L. Holder et al. Association between serum free thyroxine concentration and atrial fibrillation. Arch. Intern. Med. 167(9), 928–934 (2007)CrossRefPubMedGoogle Scholar
  47. 47.
    H. Nishi, K. Toda, S. Miyagawa, Y. Yoshigawa et al. Novel evaluation of liver stiffness using transient elastography to evaluate perioperative status in severe heart failure patients. Circulation 128, 12745 (2013)Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Yasemin Aydoğan
    • 1
  • Mustafa Altay
    • 2
  • Oktay Ünsal
    • 3
  • Veysel Kaplanoğlu
    • 4
  • Yavuz Çağır
    • 5
  • Canan Yıldız
    • 6
  • Esin Beyan
    • 7
  • Selma Uysal Ramadan
    • 8
  1. 1.Zonguldak Devrek State HospitalZonguldakTurkey
  2. 2.Department of EndocrinologyKeçiören Training and Research HospitalAnkaraTurkey
  3. 3.Department of NefrologyUludağ University Medical Faculty HospitalBursaTurkey
  4. 4.Department of RadiologyKeçiören Training ad Research HospitalAnkaraTurkey
  5. 5.Çankırı Çerkeş State HospitalÇankırıTurkey
  6. 6.Aydın Didim State HospitalAydınTurkey
  7. 7.Department of Internal MedicineKeçiören Training and Research HospitalAnkaraTurkey
  8. 8.Deparment of RadiologyKeçiören Training and Research HospitalAnkaraTurkey

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