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Impaired Sensitivity to Thyroid Hormones Is Associated With Diabetes Care 1 Impaired Sensitivity to Thyroid Martin Laclaustra,1,2,3 Belen Moreno-Franco,1,2 Hormones Is Associated With Jose Manuel Lou-Bonafonte,1,4,5 Rocio Mateo-Gallego,1,2 Diabetes and Metabolic Syndrome Jose Antonio Casasnovas,1,2 Pilar Guallar-Castillon,6,7,8 Ana Cenarro,1,2 1,2 https://doi.org/10.2337/dc18-1410 and Fernando Civeira OBJECTIVE Diabetes prevalence and incidence increase among individuals with hypothyroidism but also among those with hyperthyroxinemia, which seems contradictory. Both high free thyroxine (fT4) and high thyroid-stimulating hormone (TSH) are present in the resistance to thyroid hormone syndrome. A mild acquired resistance to thyroid hormone might occur in the general population and be associated with diabetes. We aimed to analyze the association of resistance to thyroid hormone indices (the Thyroid Feedback Quantile-based Index [TFQI], proposed in this work, and the previously used Thyrotroph T4 Resistance Index and TSH Index) with diabetes. RESEARCH DESIGN AND METHODS 1Instituto de Investigacion´ Sanitaria de Aragon´ We calculated the aforementioned resistance to thyroid hormone indices based on (IIS Aragon),´ Universidad de Zaragoza, Zaragoza, ‡ Spain a U.S. representative sample of 5,129 individuals 20 years of age participating in 2Translational Research Unit, Hospital Univer- the 2007–2008 National Health and Nutrition Examination Survey (NHANES). Also, sitario Miguel Servet, Zaragoza, Spain and to approximate TFQI, a U.S.-referenced Parametric TFQI (PTFQI) can be calculated CIBERCV, Madrid, Spain 3 CARDIOVASCULAR AND METABOLIC RISK with the spreadsheet formula 5NORM.DIST(fT4_cell_in_pmol_per_L,10.075, Fundacion´ Agencia Aragonesa para la Inves- 1 2 tigacion´ y el Desarrollo (ARAID), Zaragoza, Spain 2.155,TRUE) NORM.DIST(LN(TSH_cell_in_mIU_per_L),0.4654,0.7744,TRUE) 1. 4Instituto Agroalimentario de Aragon,´ CITA- Outcomes of interest were glycohemoglobin ‡6.5%, diabetes medication, Universidad de Zaragoza, Zaragoza, Spain diabetes-related deaths (diabetes as contributing cause of death), and addi- 5CIBEROBN, Madrid, Spain 6 tionally, in a fasting subsample, diabetes and metabolic syndrome. Logistic Department of Preventive Medicine and Public Health, School of Medicine, Universidad Autonoma´ and Poisson regressions were adjusted for sex, age, and race/ethnicity. de Madrid-IdiPaz, and CIBERESP, Madrid, Spain 7IMDEA Food Institute, CEI UAM+CSIC, Madrid, RESULTS Spain OddratiosforthefourthversusthefirstquartileofTFQI were1.73(95% CI 1.32,2.27) 8Welch Center for Prevention, Epidemiology, (P 5 0.002) for positive glycohemoglobin and 1.66 (95% CI 1.31, 2.10) (P 5 and Clinical Research, Johns Hopkins University, trend trend Baltimore, MD 0.001) for medication. Diabetes-related death rate ratio for TFQI being above versus P 5 Corresponding author: Martin Laclaustra, below the median was 4.81 (95% CI 1.01, 22.94) ( trend 0.015). Further adjustment [email protected] for BMI and restriction to normothyroid individuals yielded similar results. Per 1 SD Received 2 July 2018 and accepted 4 November in TFQI, odds increased 1.13 (95% CI 1.02, 1.25) for diabetes and 1.16 (95% CI 1.02, 2018 1.31) for metabolic syndrome. The other resistance to thyroid hormone indices This article contains Supplementary Data online showed similar associations for diabetes-related deaths and metabolic syndrome. at http://care.diabetesjournals.org/lookup/suppl/ doi:10.2337/dc18-1410/-/DC1. CONCLUSIONS © 2018 by the American Diabetes Association. Higher values in resistance to thyroid hormone indices are associated with obesity, Readers may use this article as long as the work metabolic syndrome, diabetes, and diabetes-related mortality. Resistance to is properly cited, the use is educational and not for profit, and the work is not altered. More infor- thyroid hormone may reflect energy balance problems driving type 2 diabetes. mation is available at http://www.diabetesjournals These indices may facilitate monitoring treatments focused on energy balance. .org/content/license. Diabetes Care Publish Ahead of Print, published online December 14, 2018 2 Resistance to Thyroid Hormone and Diabetes Diabetes Care Recent evidence suggests that hyper- because they can be quantified just approved by the National Center for thyroxinemia may be cross-sectionally observing thyroid hormones and TSH Health Statistics (NCHS) Research Ethics and prospectively associated with type 2 concentrations or indices derived from Review Board (Continuation of Protocol diabetes (1). This is at odds with the them (13,14), although suppression tests no. 2005-06). physiological metabolism-activating have also been described (15). action of thyroid hormones, which Thus, given the thyroid feedback loop, Thyroxine, TSH, and Resistance to is considered capable of ameliorating the aforementioned reports showing Thyroid Hormone Indices obesity-related morbidities (2). It is association of high thyroid hormones Free thyroxine (fT4) was quantified with also in conflict with the increased in- or high TSH with the prevalence and the Access Free T4 assay, a two-step cidence of diabetes reported among incidence of metabolic syndrome and enzyme immunoassay, and TSH was quan- patients with hypothyroidism (3) and diabetes provide apparently contradict- tified with the Access HYPERsensitive with the increased prevalence of met- ing results. In this work, we hypothesized hTSH Assay, a two-site immunoenzymatic abolic syndrome described in the that these conflicting results might be (“sandwich”) assay. Measurements were upper-normal range of the pituitary conciliated if high thyroid hormones and performed at the University of Washing- thyroid-stimulating hormone (TSH) (also high TSH co-occurrence in diabetes re- ton (Seattle, WA). The laboratory normality known as thyrotropin) (4), a range as- flected a central resistance to thyroid reference ranges were 7.74–20.64 pmol/L sociated with lower thyroid activity. Pre- hormone. If that were the case, this for fT4 and 0.34–5.60 mIU/L for TSH. vious evidence is inconsistent (4): some central resistance would probably be Thyrotroph T4 Resistance Index (TT4RI) studies find diabetes or metabolic syn- the expression of a general reduced sen- was calculated as fT4 (pmol/L) z TSH drome to be associated with TSH but not sitivity to thyroid hormones, i.e., not only (mIU/L) (13). TSH index (TSHI) was cal- with thyroid hormones, whereas others central but also peripheral. This resistance culated as ln TSH (mIU/L) + 0.1345 z fT4 find an association only with thyroid hor- to thyroid hormone could be one addi- (pmol/L) (14). mones, occasionally linking opposite tional characteristic of the cardiome- ends of the thyroid hormone concen- tabolic traits predicting diabetes. We TFQI, a New Resistance to Thyroid tration range with diabetes. The effect analyzed continuous National Health Hormone Index of thyroid hormones on insulin sensitiv- and Nutrition Examination Survey Given encouraging preliminary results ity differs by tissue; it enhances glu- (NHANES) (16) data to gain insight from the description of participants cose uptake in the muscle but reduces into this issue and propose the Thyroid who were simultaneously in the extreme it in the liver (5). The overall net effect Feedback Quantile-based Index (TFQI), quartiles of fT4 and TSH (see STATISTICAL in hypothyroidism favors insulin resis- a new resistance to thyroid hormone ANALYSES and RESULTS sections), we developed tance, but in hyperthyroidism it may index focused on deviations close to a new index to quantify, in a continuous also occasionally favor glucose intoler- normality. manner, deviations from the median pi- ance (5). These metabolic mechanisms tuitary response (inhibition) to thyroid described in clinical thyroid diseases hormones: the TFQI, which stands for may not be enough to explain the asso- RESEARCH DESIGN AND METHODS thyroid feedback quantile-based index. ciations found within the normothyroid Design and Participants Ranks (order position from minimum range. Thyroid hormones and TSH were mea- to maximum value) of fT4 and TSH were Physiologically, thyroid hormones and suredinserumin5,222(N1)adults converted to quantiles between 0 and 1, TSH are inversely correlated owing to a 20 years of age and older in the con- taking into account sampling weights. negative feedback loop. However, high tinuous NHANES (16) performed in Fractional quantiles are a generalization thyroid hormones coexist with high TSH 2007and2008,whichrecruitedarep- that summarizes in a single fraction the in individuals with resistance to thyroid resentative sample of the noninstitu- ordering number of each part in the hormone syndrome, an inherited auto- tionalized U.S. population. Data on sequence and the number of parts, somal recessive trait (6–8). Yet, a possibly mortality up to 2011 from the National e.g., the upper limit of the second tertile reversible acquired resistance to thyroid Death Index are available for all but six is the value of the quantile 0.66 and hormone, due to homeostatic compen- individuals. The current study estimates the upper limit of the third quartile is sation, has been hypothesized (9). Pro- cross-sectional associations between the value of the quantile 0.75. That longed fasting produces drops in TSH and resistance to thyroid hormone indices conversion is achieved by applying the increases in pituitary sensitivity to thyroid and diabetes-related conditions as well population empirical cumulative distri- hormones (10,11). In contrast, morbidly as longitudinal associations
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