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      Persistent Cellular Metabolic Changes after Hemithyroidectomy for Benign Euthyroid Goiter

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          Abstract

          Background: The significance of perturbations of thyroid-stimulating hormone (TSH) and thyroid hormones within the laboratory reference ranges after hemithyroidectomy is unknown. Our aim was to examine changes in TSH and thyroid hormones after hemithyroidectomy for benign euthyroid goiter, focusing on tissue response by examining the mitochondrial membrane potential (MMP) of peripheral blood mononuclear cells (PBMCs) and basal oxygen consumption (V˙<smlcap>O</smlcap><sub>2</sub>). Materials and Methods: In a prospective study on 28 patients and controls, we examined serum TSH and thyroid hormones before hemithyroidectomy and 1, 3, 6 and 12 months after hemithyroidectomy for benign euthyroid goiter. In the hemithyroidectomy group, flow cytometry was used to measure the MMP of tetramethylrhodamine methyl ester (TMRM)- and MitoTracker Green (MTG)-stained PBMCs, and V˙<smlcap>O</smlcap><sub>2</sub> was measured by an Oxycon Pro apparatus. Results: One year after hemithyroidectomy, TSH had increased from a median of 0.97 mIU/l (interquartile range, IQR: 0.69-1.50 mIU/l) to 2.10 mIU/l (IQR: 1.90-3.00 mIU/l; p < 0.001); free thyroxine (fT<sub>4</sub>) had decreased from a median of 16.0 pmol/l (IQR: 14.9-17.0 pmol/l) to 14.8 pmol/l (IQR: 14.1-16.4 pmol/l; p = 0.009), whereas total triiodothyronine variations did not differ from those in controls. Concomitantly, the MMP of TMRM- and MTG-stained PBMCs was increased by 58% (p < 0.001) and 22% (p = 0.008), respectively. V˙<smlcap>O</smlcap><sub>2</sub> was increased by 14% (p = 0.01). Conclusion: Hemithyroidectomy for benign euthyroid goiter induced persistently increased TSH and decreased fT<sub>4</sub>, sustained mitochondrial hyperpolarization and increased V˙<smlcap>O</smlcap><sub>2</sub>. Our results demonstrate a decrease after hemithyroidectomy of the metabolic state to which the individual is adapted, with persistent cellular metabolic changes in a hemithyroidectomized patient group which is normally considered clinically and biochemically euthyroid.

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          Most cited references14

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          Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus.

          Peripheral blood lymphocytes (PBLs) from systemic lupus erythematosus (SLE) patients exhibit increased spontaneous and diminished activation-induced apoptosis. We tested the hypothesis that key biochemical checkpoints, the mitochondrial transmembrane potential (deltapsim) and production of reactive oxygen intermediates (ROIs), mediate the imbalance of apoptosis in SLE. We assessed the deltapsim with potentiometric dyes, measured ROI production with oxidation-sensitive fluorochromes, and monitored cell death by annexin V and propidium iodide staining of lymphocytes, using flow cytometry. Intracellular glutathione levels were measured by high-performance liquid chromatography, while ATP and ADP levels were assessed by the luciferin-luciferase assay. Both deltapsim and ROI production were elevated in the 25 SLE patients compared with the 25 healthy subjects and the 10 rheumatoid arthritis patients. Intracellular glutathione contents were diminished, suggesting increased utilization of reducing equivalents in SLE. H2O2, a precursor of ROIs, increased deltapsim and caused apoptosis in normal PBLs. In contrast, H2O2-induced apoptosis and deltapsim elevation were diminished, particularly in T cells, and the rate of necrotic cell death was increased in patients with SLE. The intracellular ATP content and the ATP:ADP ratio were reduced and correlated with the deltapsim elevation in lupus. CD3:CD28 costimulation led to transient elevation of the deltapsim, followed by ATP depletion, and sensitization of normal PBLs to H2O2-induced necrosis. Depletion of ATP by oligomycin, an inhibitor of F0F1-ATPase, had similar effects. T cell activation and apoptosis are mediated by deltapsim elevation and increased ROI production. Mitochondrial hyperpolarization and the resultant ATP depletion sensitize T cells for necrosis, which may significantly contribute to inflammation in patients with SLE.
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            Thyroid hormone as a determinant of energy expenditure and the basal metabolic rate.

            Brian Kim (2008)
            It has long been accepted that thyroid hormone is an important determinant of overall energy expenditure and the basal metabolic rate. Indeed, regulating thermogenesis is one of the major tasks of thyroid hormone in adult humans. A wealth of data have demonstrated the effects of thyroid hormone on cellular processes involved with energy expenditure, yet in spite of this body of work it remains unclear which 3,3'-triiodothyronine-responsive energetic processes are most relevant for the determination of the basal metabolic rate. Recently, a novel metabolic role for thyroid hormone has been recognized based on the observation that bile acids can activate local production of thyroid hormone via induction of the type 2 deiodinase. Nevertheless, more work must be done before it can be fully explained how thyroid hormone determines the metabolic rate.
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              A high normal TSH is associated with the metabolic syndrome.

              Obesity and insulin resistance are key features of the metabolic syndrome. In euthyroidism, the relationships between TSH and insulin resistance or the metabolic syndrome are less clear. We investigated the associations between TSH and the features and prevalence of the metabolic syndrome in euthyroid German subjects. In a cross-sectional study, glucose metabolism was defined by an oral glucose tolerance test (oGTT) (except for those with evident diabetes) in 1333 subjects with TSH values between 0.3 and 4.5 mU/l who did not take any thyroid medication. Lipid parameters were measured, blood pressure and anthromopmetric parameters were taken, and insulin resistance was quantified as HOMA%S. TSH was weakly correlated with BMI (R = 0.061, P = 0.025). This association remained significant after adjustment for sex, age, and impaired glucose metabolism (P = 0.002). Subjects with a TSH in the upper normal range (2.5-4.5 mU/l, n = 119) had a significantly higher BMI (30.47 +/- 0.57 vs. 28.74 +/- 0.18 kg/m(2), P = 0.001) and higher fasting triglycerides (1.583 +/- 0.082 vs. 1.422 +/- 0.024 mmol/l, P = 0.023), and their likeliness for fulfilling the ATP III criteria of the metabolic syndrome was 1.7-fold increased (95% CI: 1.11- 2.60). In euthyroidism, subjects with a TSH in the upper normal range (2.5-4.5 mU/l) were more obese, had higher triglycerides, and had an increased likeliness for the metabolic syndrome. Therefore, a TSH below 2.5 mU/l is associated with a favourable metabolic profile. Whether lowering TSH to levels below 2.5 mU/l improves metabolism needs to be investigated in intervention trials.
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                Author and article information

                Journal
                ETJ
                ETJ
                10.1159/issn.2235-0640
                European Thyroid Journal
                S. Karger AG
                2235-0640
                2235-0802
                2014
                March 2014
                12 March 2014
                : 3
                : 1
                : 10-16
                Affiliations
                aDepartment of Otorhinolaryngology, Head and Neck Surgery, Køge Hospital, Region Zealand, Køge, and Departments of bClinical Pathology, cClinical Biochemistry, dGynecology and Obstetrics and eInternal Medicine, Næstved Hospital, Region Zealand, Næstved, Denmark
                Author notes
                *Tina Toft Kristensen, Tornbyvej 10, DK-4600 Køge (Denmark), E-Mail tinatoft@dadlnet.dk
                Article
                357943 PMC4005256 Eur Thyroid J 2014;3:10-16
                10.1159/000357943
                PMC4005256
                24847460
                117be36f-c81e-4c48-98aa-0e710b1a4ac5
                © 2014 European Thyroid Association Published by S. Karger AG, Basel

                Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

                History
                : 09 September 2013
                : 10 December 2013
                Page count
                Figures: 2, Tables: 2, Pages: 7
                Categories
                Translational Thyroidology / Original Paper

                Endocrinology & Diabetes,Neurology,Nutrition & Dietetics,Sexual medicine,Internal medicine,Pharmacology & Pharmaceutical medicine
                Thyroid hormone,Hypothyroidism,Mitochondrial function,Thyrotropin,Thyroidectomy

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