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Exp Clin Endocrinol Diabetes 2018; 126(08): 493-504
DOI: 10.1055/a-0635-0826
Article
© Georg Thieme Verlag KG Stuttgart · New York

The Association Between the Levels of Thyroid Hormones and Peripheral Nerve Conduction in Patients with Type 2 Diabetes Mellitus

Fan-Fan Zhu
1   Division of Endocrinology and Metabolism, Shanghai Ninth People’s Hospital, School of medicine, Shanghai Jiaotong University, Shanghai, China
,
Li-Zhen Yang
1   Division of Endocrinology and Metabolism, Shanghai Ninth People’s Hospital, School of medicine, Shanghai Jiaotong University, Shanghai, China
› Author Affiliations
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Publication History

received 22 March 2018
revised 09 May 2018

accepted 25 May 2018

Publication Date:
26 June 2018 (online)

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Abstract

Background Type 2 diabetes has an underlying pathology with thyroid dysfunction. However, few studies have investigated the association between thyroid hormones and diabetic peripheral neuropathy. Our aim was to evaluate the relationship between thyroid hormones and electrophysiological properties of peripheral nerves in type 2 diabetes.

Patients and Methods The medical records of 308 patients with type 2 diabetes were enrolled in this study. Subjects stratified by sex were divided into subgroups based on the diagnosis of nerve conduction study. The nerve conduction parameters were separately described with the spectrum of thyroid hormones. Multivariate regression models to analyze the potential links between thyroid hormones and nerve conduction parameters.

Results The serum free triiodine thyronine levels between normal and abnormal nerve conduction groups were statistically different in total (4.55±0.65 vs 4.37±0.63, P<0.05) and female diabetic patients (4.46±0.50 vs 4.14±0.57, P<0.01). Moreover, the summed amplitude and velocity Z score of female and male increased with free triiodine thyronine levels (P<0.05). Sex-specific binary logistic regression models showed that free triiodine thyronine levels were associated with decreased odds of abnormal nerve conduction diagnosis (odds ratio [95%CI]=0.151[0.047-0.186]) and low tertile of summed amplitude Z score (odds ratio [95%CI]=0.283[0.099-0.809]) in female. In total patients, free triiodine thyronine level was negatively associated with odds of abnormal nerve conduction (odds ratio [95%CI]=0.436 [0.226-0.842]), low tertile of summed velocity (odds ratio [95%CI]=0.44[0.226-0.858]) and amplitude (odds ratio [95%CI]=0.436[0.227-0.838) Z score.

Conclusions Serum free triiodine thyronine level is associated with nerve conduction in diabetes. Low free triiodine thyronine may be a potential risk for diabetic peripheral neuropathy.

Key words

Type 2 diabetes mellitus - Diabetic peripheral neuropathy - Nerve conduction study - Thyroid hormones - Free triiodine thyronine
 

  • References

  • 1 Said G. Diabetic neuropathy-a review. Nat Clin Pract Neurol 2007; 3: 331-340
    CrossrefPubMedGoogle Scholar
  • 2 Roman-Pintos LM, Villegas-Rivera G, Rodriguez-Carrizalez AD. et al. Diabetic polyneuropathy in type 2 diabetes mellitus: Inflammation, oxidative stress, and mitochondrial function. J Diabetes Res 2016; 2016: 3425617
    PubMedGoogle Scholar
  • 3 Lu B, Hu J, Wen J. et al. Determination of peripheral neuropathy prevalence and associated factors in Chinese subjects with diabetes and pre-diabetes - ShangHai Diabetic neuRopathy Epidemiology and Molecular Genetics Study (SH-DREAMS). PLoS One 2013; 8: e61053
    CrossrefPubMedGoogle Scholar
  • 4 Charles M, Soedamah-Muthu SS, Tesfaye S. et al. Low peripheral nerve conduction velocities and amplitudes are strongly related to diabetic microvascular complications in type 1 diabetes: the EURODIAB prospective complications study. Diabetes Care 2010; 33: 2648-2653
    CrossrefPubMedGoogle Scholar
  • 5 Liu MS, Hu BL, Cui LY. et al. Clinical and neurophysiological features of 700 patients with diabetic peripheral neuropathy. Zhonghua Nei Ke Za Zhi 2005; 4: 173-176
    PubMedGoogle Scholar
  • 6 Malik RA. Pathology of human diabetic neuropathy. Handb Clin Neurol 2014; 126: 249-259
    CrossrefPubMedGoogle Scholar
  • 7 Nukada H. Ischemia and diabetic neuropathy. Handb Clin Neurol 2014; 126: 469-487
    PubMedGoogle Scholar
  • 8 Nie C, Bao HP. Analysis of the related risk factors of diabetic peripheral neuropathy. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 2012; 26: 467-469
    PubMedGoogle Scholar
  • 9 Grisold A, Callaghan BC, Feldman EL. Mediators of diabetic neuropathy: is hyperglycemia the only culprit?. Curr Opin Endocrinol Diabetes Obes 2017; 24: 103-111
    CrossrefPubMedGoogle Scholar
  • 10 Valensi P, Giroux C, Seeboth-Ghalayini B. et al. Diabetic peripheral neuropathy: effects of age, duration of diabetes, glycemic control, and vascular factors. J Diabetes Complications 1997; 11: 27-34
    CrossrefPubMedGoogle Scholar
  • 11 Penza P, Lombardi R, Camozzi F. et al. Painful neuropathy in subclinical hypothyroidism: clinical and neuropathological recovery after hormone replacement therapy. Neurol Sci 2009; 30: 149-151
    CrossrefPubMedGoogle Scholar
  • 12 Yerdelen D, Ertorer E, Koc F. The effects of hypothyroidism on strength-duration properties of peripheral nerve. J Neurol Sci 2010; 294: 89-91
    CrossrefPubMedGoogle Scholar
  • 13 Ramadhan A, Schondorf R, Tamilia M. Rhabdomyolysis and peroneal nerve compression associated with thyroid hormone withdrawal in the setting of remnant ablation: review of the literature. Endocr Pract 2011; 17: 629-635
    CrossrefPubMedGoogle Scholar
  • 14 Han C, He X, Xia X. et al. Subclinical hypothyroidism and type 2 diabetes: A systematic review and meta-analysis. PLoS One 2015; 10: e0135233
    CrossrefPubMedGoogle Scholar
  • 15 Zhao W, Zeng H, Zhang X. et al. A high thyroid stimulating hormone level is associated with diabetic peripheral neuropathy in type 2 diabetes patients. Diabetes Res Clin Pract 2016; 115: 122-129
    CrossrefPubMedGoogle Scholar
  • 16 Magri F, Buonocore M, Oliviero A. et al. Intraepidermal nerve fiber density reduction as a marker of preclinical asymptomatic small-fiber sensory neuropathy in hypothyroid patients. Eur J Endocrinol 2010; 163: 279-284
    CrossrefPubMedGoogle Scholar
  • 17 Sainani KL. The problem of multiple testing. PM R 2009; 1: 1098-1103
    CrossrefPubMedGoogle Scholar
  • 18 Li Q, Yang LZ. Hemoglobin A1c level higher than 9.05% causes a significant impairment of erythrocyte deformability in diabetes mellitus. Acta Endocrinologica 2018; 14: 66-75
    PubMedGoogle Scholar
  • 19 Dyck PJ, Hansen S, Karnes J. et al. Capillary number and percentage closed in human diabetic sural nerve. Proc Natl Acad Sci U S A 1985; 82: 2513-2517
    CrossrefPubMedGoogle Scholar
  • 20 Giannini C, Dyck PJ. Ultrastructural morphometric abnormalities of sural nerve endoneurial microvessels in diabetes mellitus. Annals of Neurol 1994; 36: 408-415
    PubMedGoogle Scholar
  • 21 Esper RJ, Nordaby RA, Vilarino JO. et al. Endothelial dysfunction: a comprehensive appraisal. Cardiovasc Diabetol 2006; 5: 4
    CrossrefPubMedGoogle Scholar
  • 22 Ming LU, Yang CB, Ling G. et al. Mechanism of subclinical hypothyroidism accelerating endothelial dysfunction (Review). Exp Ther Med 2015; 9: 3-10
    CrossrefPubMedGoogle Scholar
  • 23 Vicinanza R, Coppotelli G, Malacrino C. et al. Oxidized low-density lipoproteins impair endothelial function by inhibiting non-genomic action of thyroid hormone- mediated nitric oxide production in human endothelial cells. Thyroid 2013; 23: 231-238
    CrossrefPubMedGoogle Scholar
  • 24 Calza L, Fernandez M, Giardino L. Role of the thyroid system in myelination and neural connectivity. Compr Physiol 2015; 5: 1405-1421
    PubMedGoogle Scholar
  • 25 Zhang M, Ma Z, Qin H. et al. Thyroid hormone potentially benefits multiple sclerosis via facilitating remyelination. Mol Neurobiol 2016; 53: 4406-4416
    CrossrefPubMedGoogle Scholar
  • 26 Duksal T, Tiftikcioglu BI, Bilgin S. et al. Role of inflammation in sensory neuropathy in prediabetes or diabetes. Acta Neurol Scand 2016; 133: 384-390
    CrossrefPubMedGoogle Scholar
  • 27 Shih CH, Chen SL, Yen CC. et al. Thyroid hormone receptor-dependent transcriptional regulation of fibrinogen and coagulation proteins. Endocrinology 2004; 145: 2804-2814
    CrossrefPubMedGoogle Scholar
  • 28 Huang YH, Tsai MM, Lin KH. Thyroid hormone dependent regulation of target genes and their physiological significance. Chang Gung Med J 2008; 31: 325-334
    PubMedGoogle Scholar
  • 29 Weitzel JM, Iwen KA. Coordination of mitochondrial biogenesis by thyroid hormone. Mol Cell Endocrinol 2011; 342: 1-7
    CrossrefPubMedGoogle Scholar
  • 30 Psarra AM, Sekeris CE. Steroid and thyroid hormone receptors in mitochondria. IUBMB Life 2008; 60: 210-223
    CrossrefPubMedGoogle Scholar
  • 31 Cheng SY, Leonard JL, Davis PJ. Molecular aspects of thyroid hormone actions. Endocr Rev 2010; 31: 139-170
    CrossrefPubMedGoogle Scholar
  • 32 Mancini A, Di Segni C, Raimondo S. et al. Thyroid hormones. Oxidative Stress, and Inflammation 2016; 2016: 6757154
    PubMedGoogle Scholar
  • 33 Kabadi UM. Impaired pituitary thyrotroph function in uncontrolled type II diabetes mellitus: normalization on recovery. J Clin Endocrinol Metab 1984; 59: 521-525
    CrossrefPubMedGoogle Scholar
  • 34 Duntas LH, Orgiazzi J, Brabant G. The interface between thyroid and diabetes mellitus. Clin Endocrinol (Oxf) 2011; 75: 1-9
    CrossrefPubMedGoogle Scholar
  • 35 Moura Neto A, Parisi MC, Alegre SM. et al. Relation of thyroid hormone abnormalities with subclinical inflammatory activity in patients with type 1 and type 2 diabetes mellitus. Endocrine 2016; 51: 63-71
    CrossrefPubMedGoogle Scholar