Skip to main content
Top
Published in: Endocrine 1/2016

01-01-2016 | Original Article

Relation of thyroid hormone abnormalities with subclinical inflammatory activity in patients with type 1 and type 2 diabetes mellitus

Authors: Arnaldo Moura Neto, Maria Candida Ribeiro Parisi, Sarah Monte Alegre, Elizabeth Joao Pavin, Marcos Antonio Tambascia, Denise Engelbrecht Zantut-Wittmann

Published in: Endocrine | Issue 1/2016

Login to get access

Abstract

Thyroid hormone (TH) abnormalities are common in patients with diabetes mellitus (DM). These thyroid hormone abnormalities have been associated with inflammatory activity in several conditions but this link remains unclear in DM. We assessed the influence of subclinical inflammation in TH metabolism in euthyroid diabetic patients. Cross-sectional study involving 258 subjects divided in 4 groups: 70 patients with T2DM and 55 patients with T1DM and two control groups of 70 and 63 non-diabetic individuals, respectively. Groups were paired by age, sex, and body mass index (BMI). We evaluated the association between clinical and hormonal variables [thyrotropin, reverse T3 (rT3), total and free thyroxine (T4), and triiodothyronine (T3)] with the inflammation markers C-reactive protein (hs-CRP), serum amyloid A (SAA), and interleukin-6 (IL-6). Serum T3 and free T3 were lower in patients with diabetes (all P < 0.001) compared to the control groups. Interleukin-6 showed positive correlations with rT3 in both groups (P < 0.05). IL-6 was independently associated to FT3/rT3 (B = −0.193; 95 % CI −0.31; −0.076; P = 0.002) and FT4/rT3 (B = −0.107; 95 % CI −0.207; −0.006; P = 0.039) in the T1DM group. In the T2DM group, SAA (B = 0.18; 95 % CI 0.089; 0.271; P < 0.001) and hs-CRP (B = −0.069; 95 % CI −0.132; –0.007; P = 0.03) predicted FT3 levels. SAA (B = −0.16; 95 % CI −0.26; −0.061; P = 0.002) and IL6 (B = 0.123; 95 % CI 0.005; 0.241; P = 0.041) were related to FT4/FT3. In DM, differences in TH levels compared to non-diabetic individuals were related to increased subclinical inflammatory activity and BMI. Altered deiodinase activity was probably involved. These findings were independent of sex, age, BMI, and HbA1c levels.
Literature
1.
go back to reference B. McIver, C.A. Gorman, Euthyroid sick syndrome: an overview. Thyroid 7, 125–132 (2007)CrossRef B. McIver, C.A. Gorman, Euthyroid sick syndrome: an overview. Thyroid 7, 125–132 (2007)CrossRef
2.
go back to reference L.H. Duntas, J. Orgiazzi, G. Brabant, The interface between thyroid and diabetes mellitus. Clin. Endocrinol. (Oxf.) 75, 1–9 (2011)CrossRef L.H. Duntas, J. Orgiazzi, G. Brabant, The interface between thyroid and diabetes mellitus. Clin. Endocrinol. (Oxf.) 75, 1–9 (2011)CrossRef
3.
go back to reference G.E. Umpierrez, K.A. Latif, M.B. Murphy, H.C. Lambeth, F. Stentz, A. Bush, A.E. Kitabch, Thyroid dysfunction in patients with type 1 diabetes: a longitudinal study. Diabetes Care 26, 1181–1185 (2003)PubMedCrossRef G.E. Umpierrez, K.A. Latif, M.B. Murphy, H.C. Lambeth, F. Stentz, A. Bush, A.E. Kitabch, Thyroid dysfunction in patients with type 1 diabetes: a longitudinal study. Diabetes Care 26, 1181–1185 (2003)PubMedCrossRef
4.
go back to reference T. Bulum, B. Kolaric, L. Duvnjak, Insulin sensitivity modifies the relationship between thyroid function and lipid profile in euthyroid type 1 diabetic patients. Endocrine 42, 139–145 (2012)PubMedCrossRef T. Bulum, B. Kolaric, L. Duvnjak, Insulin sensitivity modifies the relationship between thyroid function and lipid profile in euthyroid type 1 diabetic patients. Endocrine 42, 139–145 (2012)PubMedCrossRef
5.
go back to reference J.J. Díez, P. Iglesias, Subclinical hyperthyroidism in patients with type 2 diabetes. Endocrine 42, 157–163 (2012)PubMedCrossRef J.J. Díez, P. Iglesias, Subclinical hyperthyroidism in patients with type 2 diabetes. Endocrine 42, 157–163 (2012)PubMedCrossRef
6.
go back to reference A. Roos, S.J.L. Bakker, T.P. Links, R.O.B. Gans, B.H.R. Wolffenbuttel, Thyroid function is associated with components of the metabolic syndrome in euthyroid subjects. J. Clin. Endocrinol. Metab. 92, 491–496 (2007)PubMedCrossRef A. Roos, S.J.L. Bakker, T.P. Links, R.O.B. Gans, B.H.R. Wolffenbuttel, Thyroid function is associated with components of the metabolic syndrome in euthyroid subjects. J. Clin. Endocrinol. Metab. 92, 491–496 (2007)PubMedCrossRef
7.
go back to reference N. Knudsen, P. Laurberg, L.B. Rasmussen, I. Bülow, H. Perrild, L. Ovesen, T. Jørgensen, Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J. Clin. Endocrinol. Metab. 90, 4019–4024 (2006)CrossRef N. Knudsen, P. Laurberg, L.B. Rasmussen, I. Bülow, H. Perrild, L. Ovesen, T. Jørgensen, Small differences in thyroid function may be important for body mass index and the occurrence of obesity in the population. J. Clin. Endocrinol. Metab. 90, 4019–4024 (2006)CrossRef
8.
go back to reference J.L. Schlienger, A. Anceau, G. Charbrier, M.L. North, F. Stephan, Effect of diabetic control on the level of circulating thyroid hormones. Diabetologia 22, 486–488 (1982)PubMedCrossRef J.L. Schlienger, A. Anceau, G. Charbrier, M.L. North, F. Stephan, Effect of diabetic control on the level of circulating thyroid hormones. Diabetologia 22, 486–488 (1982)PubMedCrossRef
9.
go back to reference N. Stathatos, L. Wartofsky, The euthyroid sick syndrome: is there a physiologic rationale for thyroid hormone treatment? J. Endocrinol. Invest. 26, 1174–1179 (2003)PubMedCrossRef N. Stathatos, L. Wartofsky, The euthyroid sick syndrome: is there a physiologic rationale for thyroid hormone treatment? J. Endocrinol. Invest. 26, 1174–1179 (2003)PubMedCrossRef
10.
go back to reference U.M. Kabadi, Impaired pituitary thyrotroph function in uncontrolled type II diabetes mellitus: normalization on recovery. J. Clin. Endocrinol. Metab. 59, 521–525 (1984)PubMedCrossRef U.M. Kabadi, Impaired pituitary thyrotroph function in uncontrolled type II diabetes mellitus: normalization on recovery. J. Clin. Endocrinol. Metab. 59, 521–525 (1984)PubMedCrossRef
11.
go back to reference R. Naeije, J. Golstein, N. Clumeck, H. Meinhold, K.W. Wenzel, L. Vanhaelst, A low T3 syndrome in diabetic ketoacidosis. Clin. Endocrinol. (Oxf.) 8, 467–472 (1978)CrossRef R. Naeije, J. Golstein, N. Clumeck, H. Meinhold, K.W. Wenzel, L. Vanhaelst, A low T3 syndrome in diabetic ketoacidosis. Clin. Endocrinol. (Oxf.) 8, 467–472 (1978)CrossRef
12.
go back to reference G. Iervasi, A. Pingitori, P. Landi, M. Raciti, A. Ripoli, M. Scarlattini, A. L’Abbate, L. Donato, Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation 107, 708–713 (2003)PubMedCrossRef G. Iervasi, A. Pingitori, P. Landi, M. Raciti, A. Ripoli, M. Scarlattini, A. L’Abbate, L. Donato, Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation 107, 708–713 (2003)PubMedCrossRef
13.
go back to reference F. Karadag, H. Ozcan, A.B. Karul, M. Yilmaz, O. Cildag, Correlates of non-thyroidal illness in chronic obstructive pulmonary disease. Respir. Med. 101, 1439–1446 (2007)PubMedCrossRef F. Karadag, H. Ozcan, A.B. Karul, M. Yilmaz, O. Cildag, Correlates of non-thyroidal illness in chronic obstructive pulmonary disease. Respir. Med. 101, 1439–1446 (2007)PubMedCrossRef
14.
go back to reference M. Borzio, R. Caldara, F. Borzio, V. Piepoli, P. Rampini, C. Ferrari, Thyroid function tests in chronic liver disease: evidence for multiple abnormalities despite clinical euthyroidism. Gut 24, 631–636 (1983)PubMedPubMedCentralCrossRef M. Borzio, R. Caldara, F. Borzio, V. Piepoli, P. Rampini, C. Ferrari, Thyroid function tests in chronic liver disease: evidence for multiple abnormalities despite clinical euthyroidism. Gut 24, 631–636 (1983)PubMedPubMedCentralCrossRef
15.
go back to reference C. Zocalli, F. Mallamaci, G. Tripepi, S. Cutrupi, P. Pizzini, Low triiodothyronine and survival in end-stage renal disease. Kidney Int. 70, 523–528 (2006) C. Zocalli, F. Mallamaci, G. Tripepi, S. Cutrupi, P. Pizzini, Low triiodothyronine and survival in end-stage renal disease. Kidney Int. 70, 523–528 (2006)
16.
go back to reference E. Scoscia, S. Baglioni, A. Eslami, G. Iervasi, S. Monti, T. Todisco, Low triiodothyronine (T3) state: a predictor of outcome in respiratory failure? Results of a clinical pilot study. Eur. J. Endocrinol. 151, 557–560 (2004)PubMedCrossRef E. Scoscia, S. Baglioni, A. Eslami, G. Iervasi, S. Monti, T. Todisco, Low triiodothyronine (T3) state: a predictor of outcome in respiratory failure? Results of a clinical pilot study. Eur. J. Endocrinol. 151, 557–560 (2004)PubMedCrossRef
17.
go back to reference A. Boelen, M.C. Platvoet Schiphorst, W.M. Wiersinga, Association between serum interluekin-6 and serum 3,5,3’-triiodothyronine in non-thyroidal illness. J. Clin. Endocrinol. Metab. 77, 1695–1699 (1993)PubMed A. Boelen, M.C. Platvoet Schiphorst, W.M. Wiersinga, Association between serum interluekin-6 and serum 3,5,3’-triiodothyronine in non-thyroidal illness. J. Clin. Endocrinol. Metab. 77, 1695–1699 (1993)PubMed
18.
go back to reference M. Michalaki, A.G. Vagenakis, M. Makri, F. Kalfarentzos, V. Kyriazopoulou, Dissociation of the early decline in serum T3 concentration and serum IL-6 rise and TNF-a in non-thyroidal illness syndrome induced by abdominal surgery. J. Clin. Endocrinol. Metab. 86, 4198–4205 (2001)PubMed M. Michalaki, A.G. Vagenakis, M. Makri, F. Kalfarentzos, V. Kyriazopoulou, Dissociation of the early decline in serum T3 concentration and serum IL-6 rise and TNF-a in non-thyroidal illness syndrome induced by abdominal surgery. J. Clin. Endocrinol. Metab. 86, 4198–4205 (2001)PubMed
19.
go back to reference A. Moura Neto, M.C. Parisi, M.A. Tambascia, S.M. Alegre, E.J. Pavin, D.E. Zantut-Wittmann, The influence of body mass index and low-grade systemic inflammation on thyroid hormone abnormalities in patients with type 2 diabetes. Endocr. J. 60, 877–884 (2013)PubMedCrossRef A. Moura Neto, M.C. Parisi, M.A. Tambascia, S.M. Alegre, E.J. Pavin, D.E. Zantut-Wittmann, The influence of body mass index and low-grade systemic inflammation on thyroid hormone abnormalities in patients with type 2 diabetes. Endocr. J. 60, 877–884 (2013)PubMedCrossRef
20.
go back to reference A. Moura Neto, M.C. Parisi, M.A. Tambascia, S.M. Alegre, E.J. Pavin, D.E. Zantut-Wittmann, Relationship of thyroid hormone levels and cardiovascular events in patients with type 2 diabetes. Endocrine 45, 84–91 (2014)PubMedCrossRef A. Moura Neto, M.C. Parisi, M.A. Tambascia, S.M. Alegre, E.J. Pavin, D.E. Zantut-Wittmann, Relationship of thyroid hormone levels and cardiovascular events in patients with type 2 diabetes. Endocrine 45, 84–91 (2014)PubMedCrossRef
21.
go back to reference American Diabetes Association, Standards of medical care in diabetes—2012. Diabetes Care 35, S11–S63 (2012)CrossRef American Diabetes Association, Standards of medical care in diabetes—2012. Diabetes Care 35, S11–S63 (2012)CrossRef
22.
go back to reference American Diabetes Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 35, S65–S71 (2012)CrossRef American Diabetes Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 35, S65–S71 (2012)CrossRef
23.
go back to reference N. Custro, V. Scafidi, T. Borsellino, Changes in the thyroid hormone picture that may be found in severely decompensated type II diabetes. Minerva Med. 82, 9–14 (1991)PubMed N. Custro, V. Scafidi, T. Borsellino, Changes in the thyroid hormone picture that may be found in severely decompensated type II diabetes. Minerva Med. 82, 9–14 (1991)PubMed
24.
go back to reference U.M. Kabadi, B.N. Premachandra, Low triiodothyronine and raised reverse triiodothyronine levels in patients over fifty years of age who have type II diabetes mellitus: influence of metabolic control, not age. J. Am. Geriatr. Soc. 32, 375–379 (1984)PubMedCrossRef U.M. Kabadi, B.N. Premachandra, Low triiodothyronine and raised reverse triiodothyronine levels in patients over fifty years of age who have type II diabetes mellitus: influence of metabolic control, not age. J. Am. Geriatr. Soc. 32, 375–379 (1984)PubMedCrossRef
25.
go back to reference A. Rodriguez-Perez, F. Palos-Paz, E. Kaptein, T.J. Visser, L. Dominguez-Gerpe, J. Alvarez-Escudero, J. Lado-Abeal, Identification of molecular mechanisms related to nonthyroidal illness syndrome in skeletal and adipose tissue from patients with septic shock. Clin. Endocrinol. (Oxf.) 68, 821–827 (2008)CrossRef A. Rodriguez-Perez, F. Palos-Paz, E. Kaptein, T.J. Visser, L. Dominguez-Gerpe, J. Alvarez-Escudero, J. Lado-Abeal, Identification of molecular mechanisms related to nonthyroidal illness syndrome in skeletal and adipose tissue from patients with septic shock. Clin. Endocrinol. (Oxf.) 68, 821–827 (2008)CrossRef
26.
go back to reference P.H. Davies, E.G. Black, M.C. Sheppard, J.A. Franklyn, Relation between serum interleukin-6 and thyroid hormone concentrations in 270 hospital in-patients with non-thyroidal illness. Clin. Endocrinol. (Oxf.) 44, 199–205 (1996)CrossRef P.H. Davies, E.G. Black, M.C. Sheppard, J.A. Franklyn, Relation between serum interleukin-6 and thyroid hormone concentrations in 270 hospital in-patients with non-thyroidal illness. Clin. Endocrinol. (Oxf.) 44, 199–205 (1996)CrossRef
27.
go back to reference A. Boelen, J. Kwakkel, E. Fliers, Beyond low plasma T3: local thyroid hormone metabolism during inflammation and infection. Endocr. Rev. 32, 670–693 (2011)PubMedCrossRef A. Boelen, J. Kwakkel, E. Fliers, Beyond low plasma T3: local thyroid hormone metabolism during inflammation and infection. Endocr. Rev. 32, 670–693 (2011)PubMedCrossRef
29.
go back to reference B. Antuna-Puente, B. Feve, S. Fellahi, J.P. Bastard, Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab. 34, 2–11 (2008)PubMedCrossRef B. Antuna-Puente, B. Feve, S. Fellahi, J.P. Bastard, Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab. 34, 2–11 (2008)PubMedCrossRef
30.
31.
go back to reference A.C. Bianco, D. Salvatore, B. Gereben, M.J. Berry, P.R. Larsen, Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 23, 38–89 (2002)PubMedCrossRef A.C. Bianco, D. Salvatore, B. Gereben, M.J. Berry, P.R. Larsen, Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 23, 38–89 (2002)PubMedCrossRef
32.
go back to reference T.L. Wu, I. Chen Tsai, P.Y. Chang, K.C. Tsao, C.F. Sun, L.L. Wu, J.T. Wu, Establishment of an in-house ELISA and the reference range for serum amyloid A (SAA): complimentary between SAA and C-reactive protein as markers of inflammation. Clin. Chim. Acta 376, 72–76 (2007)PubMedCrossRef T.L. Wu, I. Chen Tsai, P.Y. Chang, K.C. Tsao, C.F. Sun, L.L. Wu, J.T. Wu, Establishment of an in-house ELISA and the reference range for serum amyloid A (SAA): complimentary between SAA and C-reactive protein as markers of inflammation. Clin. Chim. Acta 376, 72–76 (2007)PubMedCrossRef
33.
go back to reference J.T. Wu, L.L. Wu, Linking inflammation and atherogenesis: soluble markers identified for the detection of risk factors and for early risk assessment. Clin. Chim. Acta 366, 74–80 (2006)PubMedCrossRef J.T. Wu, L.L. Wu, Linking inflammation and atherogenesis: soluble markers identified for the detection of risk factors and for early risk assessment. Clin. Chim. Acta 366, 74–80 (2006)PubMedCrossRef
34.
go back to reference E. Sánchez, P.S. Singru, C. Fekete, R.M. Lechan, Induction of type 2 iodothyronine deiodinasein the mediobasal hypothalamus by bacterial lipopolysaccharide: role of corticosterone. Endocrinology 149, 2484–2493 (2008)PubMedPubMedCentralCrossRef E. Sánchez, P.S. Singru, C. Fekete, R.M. Lechan, Induction of type 2 iodothyronine deiodinasein the mediobasal hypothalamus by bacterial lipopolysaccharide: role of corticosterone. Endocrinology 149, 2484–2493 (2008)PubMedPubMedCentralCrossRef
35.
go back to reference L. Mebis, L. Langouche, T.J. Visser, G. Van den Berghe, The type II iodothyronine deiodinase is up-regulated in skeletal muscle during prolonged critical illness. J. Clin. Endocrinol. Metab. 92, 3330–3333 (2007)PubMedCrossRef L. Mebis, L. Langouche, T.J. Visser, G. Van den Berghe, The type II iodothyronine deiodinase is up-regulated in skeletal muscle during prolonged critical illness. J. Clin. Endocrinol. Metab. 92, 3330–3333 (2007)PubMedCrossRef
36.
go back to reference A. Marsili, C. Aguayo-Mazzucato, T. Chen, M. Kumar, E.P. Chung, J.W. Lunsford, T. Harney, E. Van-Tran, W. Gianetti, C. Ramadan, S. Chou, P.R. Bonner Weir, J.E. Larsen, A.M. Silva, M. Zavacki, Mice with a targeted deletion of the type 2 deiodinase are insulin resistant and susceptible to diet induced obesity. PLoS One 6, e20832 (2006)CrossRef A. Marsili, C. Aguayo-Mazzucato, T. Chen, M. Kumar, E.P. Chung, J.W. Lunsford, T. Harney, E. Van-Tran, W. Gianetti, C. Ramadan, S. Chou, P.R. Bonner Weir, J.E. Larsen, A.M. Silva, M. Zavacki, Mice with a targeted deletion of the type 2 deiodinase are insulin resistant and susceptible to diet induced obesity. PLoS One 6, e20832 (2006)CrossRef
37.
go back to reference L.B. Leiria, J.M. Dora, S.M. Wajner, A.A. Estivalet, D. Crispim, A.L. Maia, The rs225017 polymorphism in the 3′UTR of the human DIO2 gene is associated with increased insulin resistance. PLoS One 9, e103960 (2014)PubMedPubMedCentralCrossRef L.B. Leiria, J.M. Dora, S.M. Wajner, A.A. Estivalet, D. Crispim, A.L. Maia, The rs225017 polymorphism in the 3′UTR of the human DIO2 gene is associated with increased insulin resistance. PLoS One 9, e103960 (2014)PubMedPubMedCentralCrossRef
38.
go back to reference J.M. Dora, W.E. Machado, J. Rheinheimer, D. Crispim, A.L. Maia, Association of the type 2 deiodinase Thr92Ala polymorphism with type 2 diabetes: case-control study and meta-analysis. Eur. J. Endocrinol. 163, 427–434 (2010)PubMedCrossRef J.M. Dora, W.E. Machado, J. Rheinheimer, D. Crispim, A.L. Maia, Association of the type 2 deiodinase Thr92Ala polymorphism with type 2 diabetes: case-control study and meta-analysis. Eur. J. Endocrinol. 163, 427–434 (2010)PubMedCrossRef
39.
go back to reference K.A. Heemstra, M.R. Soeters, E. Fliers, M.J. Serlie, J. Burggraaf, M.B. van Doorn, A.A. van der Klaauw, J.A. Romijn, J.W. Smit, E.P. Corssmit, T.J. Visser, Type 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J. Clin. Endocrinol. Metab. 94, 2144–2150 (2009)PubMedCrossRef K.A. Heemstra, M.R. Soeters, E. Fliers, M.J. Serlie, J. Burggraaf, M.B. van Doorn, A.A. van der Klaauw, J.A. Romijn, J.W. Smit, E.P. Corssmit, T.J. Visser, Type 2 iodothyronine deiodinase in skeletal muscle: effects of hypothyroidism and fasting. J. Clin. Endocrinol. Metab. 94, 2144–2150 (2009)PubMedCrossRef
40.
go back to reference E.L. Olivares, M.P. Marasi, R.S. Fortunato, A.C. da Silva, R.H. Costa-e-Souza, I.G. Araújo, E.C. Mattos, M.O. Masuda, M.A. Mulcahey, S.A. Huang, A.C. Bianco, D.P. Carvalho, Thyroid function disturbance and type 3 iodothyronine deiodinase induction after myocardial infarction in rats a time course study. Endocrinology 148, 4786–4792 (2007)PubMedCrossRef E.L. Olivares, M.P. Marasi, R.S. Fortunato, A.C. da Silva, R.H. Costa-e-Souza, I.G. Araújo, E.C. Mattos, M.O. Masuda, M.A. Mulcahey, S.A. Huang, A.C. Bianco, D.P. Carvalho, Thyroid function disturbance and type 3 iodothyronine deiodinase induction after myocardial infarction in rats a time course study. Endocrinology 148, 4786–4792 (2007)PubMedCrossRef
41.
go back to reference S.M. Wajner, I.M. Goemann, A.L. Bueno, P.R. Larsen, A.L. Maia, IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J. Clin. Invest. 121, 1834–1845 (2011)PubMedPubMedCentralCrossRef S.M. Wajner, I.M. Goemann, A.L. Bueno, P.R. Larsen, A.L. Maia, IL-6 promotes nonthyroidal illness syndrome by blocking thyroxine activation while promoting thyroid hormone inactivation in human cells. J. Clin. Invest. 121, 1834–1845 (2011)PubMedPubMedCentralCrossRef
42.
go back to reference A. Boelen, M.A. Maas, C.W. Lowik, M.C. Platvoet, W.M. Wiersinga, Induced illness in interleukin-6 (IL-6) knock-out mice: a causal role of IL-6 in the development of the low 3,5,3′-triiodothyronine syndrome. Endocrinology 137, 5250–5254 (1996)PubMed A. Boelen, M.A. Maas, C.W. Lowik, M.C. Platvoet, W.M. Wiersinga, Induced illness in interleukin-6 (IL-6) knock-out mice: a causal role of IL-6 in the development of the low 3,5,3′-triiodothyronine syndrome. Endocrinology 137, 5250–5254 (1996)PubMed
43.
go back to reference L. Mehran, A. Amouzegar, M. Tohidi, M. Moayedi, F. Azizi, Serum free thyroxine concentration is associated with metabolic syndrome in euthyroid subjects. Thyroid 2014(24), 1566–1574 (2014)CrossRef L. Mehran, A. Amouzegar, M. Tohidi, M. Moayedi, F. Azizi, Serum free thyroxine concentration is associated with metabolic syndrome in euthyroid subjects. Thyroid 2014(24), 1566–1574 (2014)CrossRef
44.
go back to reference O. Tarcin, G.B. Abanonu, D. Yazici, O. Tarcin, Association of metabolic syndrome parameters with TT3 and FT3/FT4 ratio in obese Turkish population. Metab. Syndr. Relat. Disord. 10, 137–142 (2012)PubMedCrossRef O. Tarcin, G.B. Abanonu, D. Yazici, O. Tarcin, Association of metabolic syndrome parameters with TT3 and FT3/FT4 ratio in obese Turkish population. Metab. Syndr. Relat. Disord. 10, 137–142 (2012)PubMedCrossRef
45.
go back to reference G. Roef, B. Lapauw, S. Goemaere, H.G. Zmierczak, K. Toye, J.M. Kaufman, Y. Taes, Body composition and metabolic parameters are associated with variation in thyroid hormone levels among euthyroid young men. Eur. J. Endocrinol. 167, 718–726 (2012)CrossRef G. Roef, B. Lapauw, S. Goemaere, H.G. Zmierczak, K. Toye, J.M. Kaufman, Y. Taes, Body composition and metabolic parameters are associated with variation in thyroid hormone levels among euthyroid young men. Eur. J. Endocrinol. 167, 718–726 (2012)CrossRef
46.
go back to reference L.J. Moran, H.J. Teede, M. Moakes, P.M. Clifton, R.J. Norman, G.A. Wittert, Sex hormone binding globulin, but not testosterone, is associated with the metabolic syndrome in overweight and obese women with polycystic ovary syndrome. J. Endocrinol. Invest. 36, 1004–1010 (2013)PubMed L.J. Moran, H.J. Teede, M. Moakes, P.M. Clifton, R.J. Norman, G.A. Wittert, Sex hormone binding globulin, but not testosterone, is associated with the metabolic syndrome in overweight and obese women with polycystic ovary syndrome. J. Endocrinol. Invest. 36, 1004–1010 (2013)PubMed
47.
go back to reference Y. Debaveye, B. Ellger, L. Mebis, V.M. Darras, G. Van den Berghe, Regulation of tissue iodothyronine deiodinase activity in a model of prolonged critical illness. Thyroid 18, 551–560 (2008)PubMedCrossRef Y. Debaveye, B. Ellger, L. Mebis, V.M. Darras, G. Van den Berghe, Regulation of tissue iodothyronine deiodinase activity in a model of prolonged critical illness. Thyroid 18, 551–560 (2008)PubMedCrossRef
48.
go back to reference J. Vidart, S.M. Wajner, R.S. Leite, A. Manica, B.D. Schaan, P.R. Larsen, A.L. Maia, N-acetylcysteine administration prevents nonthyroidal illness syndrome in patients with acute myocardial infarction: a randomized clinical trial. J. Clin. Endocrinol. Metab. 99, 4537–4545 (2014)PubMedPubMedCentralCrossRef J. Vidart, S.M. Wajner, R.S. Leite, A. Manica, B.D. Schaan, P.R. Larsen, A.L. Maia, N-acetylcysteine administration prevents nonthyroidal illness syndrome in patients with acute myocardial infarction: a randomized clinical trial. J. Clin. Endocrinol. Metab. 99, 4537–4545 (2014)PubMedPubMedCentralCrossRef
Metadata
Title
Relation of thyroid hormone abnormalities with subclinical inflammatory activity in patients with type 1 and type 2 diabetes mellitus
Authors
Arnaldo Moura Neto
Maria Candida Ribeiro Parisi
Sarah Monte Alegre
Elizabeth Joao Pavin
Marcos Antonio Tambascia
Denise Engelbrecht Zantut-Wittmann
Publication date
01-01-2016
Publisher
Springer US
Published in
Endocrine / Issue 1/2016
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-015-0651-5

Other articles of this Issue 1/2016

Endocrine 1/2016 Go to the issue