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Subclinical Hypothyroidism Has No Association with Insulin Resistance Indices in Adult Females: a Case‑Control Study

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Subclinical Hypothyroidism Has No Association with Insulin Resistance Indices in Adult Females: a Case‑Control Study EXPERIMENTAL AND THERAPEUTIC MEDICINE 22: 1033, 2021 Subclinical hypothyroidism has no association with insulin resistance indices in adult females: A case‑control study ROXANA ADRIANA STOICA1*, ROBERT ANCUCEANU2, ADRIAN COSTACHE3*, SIMONA DIANA ȘTEFAN1, ANCA PANTEA STOIAN1, CRISTIAN GUJA1, RALUCA IOANA ȘTEFAN‑VAN STADEN4, IOANA POPA‑TUDOR4, CRISTIAN SERAFINCEANU1 and CONSTANTIN IONESCU‑TÎRGOVIȘTE1* 1Department of Diabetes, Nutrition and Metabolic Diseases, ‘Carol Davila’ University of Medicine and Pharmacy, 050474 Bucharest; 2Department of Botanical Pharmaceutics, ‘Carol Davila’ University of Medicine and Pharmacy, 020956 Bucharest; 3Department of Pathology, ‘Carol Davila’ University of Medicine and Pharmacy, 020021 Bucharest; 4Laboratory of Electrochemistry and PATLAB, National Institute of Research for Electrochemistry and Condensed Matter, 060021 Bucharest, Romania Received May 17, 2021; Accepted June 16, 2021 DOI: 10.3892/etm.2021.10465 Abstract. Longitudinal studies have indicated an association coexistence of other elements of this syndrome that prevailed between thyroid function and insulin resistance (IR) or a in determining IR. Advantages to the study are the design that neutral relationship. Both the lowest tertile of free thyroxine permitted evaluation of IR and the thyroid function at different (fT4) and the highest tertile of free triiodothyronine (fT3) moments in time as well as the uniformity of the blood tests. were found to be associated with IR in cross‑sectional studies. The multivariate analyses were adjusted for age, lipid profile The aim of the present study was to analyze the association and treatment; however, one limiting factor was the absence between IR and subclinical hypothyroidism in a female adult of other hormonal blood tests. In summary, there was no asso‑ population from Bucharest, Romania. This is a retrospec‑ ciation between the thyroid function tests (TSH, fT4) and IR tive pilot case‑control study that included female patients indices in adult Romanian women in a case‑control study with examined by two endocrinologists and a diabetologist in an one‑year retrospective follow‑up. outpatient clinic. The retrospective follow‑up had a one‑year duration and included the evaluation of thyroid function tests Introduction and IR indices based on fasting insulinemia and C‑peptide. The study included 176 women, 91 with subclinical hypothy‑ Although no unanimous definition of insulin resistance (IR) roidism, with a median age of 60±17 years and a mean body exists, this condition can be described as the decreased mass index (BMI) of 27.79±4.76 kg/m2. The majority of the capacity of hepatic, muscular and adipose tissue to make population (50%) was diagnosed with autoimmune thyroiditis, use of glucose in the presence of insulin levels that would and 17.05% with goitre. The univariate logistic regression using normally elicit this process in healthy subjects (1). This hypothyroidism as the explaining variable found no evidence of phenomenon has been described in anabolic states such as a significant relationship between a decreased thyroid function obesity (2), inflammation (3), cancer (4), and is a core element and IR (OR 1.32; P=0.36). Metabolic syndrome was probably of the metabolic syndrome (5), or type 2 diabetes mellitus (6). the most important determinant of IR in the population group In an epidemiological study including a large Romanian studied. Thus, it was not the thyroid function per se, but the population, there were higher levels of IR in metabolically unhealthy lean, and metabolically healthy obese patients vs. controls (7). In addition, longitudinal studies have indicated an association between thyroid function and IR (8,9). Both the lowest tertile of free thyroxine (fT4) (8) and the highest tertile Correspondence to: Dr Roxana Adriana Stoica, Department of free triiodothyronine (fT3) (9) have been associated with IR of Diabetes, Nutrition and Metabolic Diseases, ‘Carol Davila’ in cross‑sectional studies. University of Medicine and Pharmacy, 5‑7 Ion Movila Street, The loss of insulin sensitivity could be determined by 050474 Bucharest, Romania E‑mail: [email protected] a decreased insulin‑dependent glucose utilization in all tissues (10), a reduction in muscle and liver glycogenolysis *Contributed equally and gluconeogenesis (11,12), or interference with adipo‑ cyte‑myocyte cross‑talk (13). Another mechanism possibly Key words: hypothyroidism, metabolic syndrome, insulin involved in the indirect action on lipid metabolism fraction resistance, insulin sensitivity, obesity and subsequent lipotoxicity, leads to increased IR (14). Moreover, the early administration of levothyroxine or metformin in subclinical hypothyroidism was associated 2 STOICA et al: SUBCLINICAL HYPOTHYROIDISM AND INSULIN RESISTANCE Table I. General characteristics of the study population. Variable IR (n=91) Non‑IR (n=85) Age (years)a 64±13.5 58±16 Glycemia (mg/dl)a 104.98±19.48 98.13±12.2 HbA1c (%)a 5.4±0.8 5.1±0.6 Total cholesterol (mg/dl) 185.68±58.07 199.61±53.79 HDLc (mg/dl) 63±29.5 68±25 LDLc (mg/dl) 96.3±58.6 110.6±52.34 TG (mg/dl) a 121.86±52.39 83.37±43.48 TSH (µUI/ml) 4.11±4.53 2.99±3.6 FT4 (ng/dl) 1.1±0.19 1.08±0.18 Fasting insulin (µUI/ml) a 9.21±9.6 5.32±4.87 Fasting C‑peptide (ng/ml)a 1.55±1.9 1.38±0.73 HOMA‑IR1 (insulin)a 2.62±2.81 1.29±1.2 HOMA‑IR2 (insulin)a 1.32±1.32 0.71±0.67 HOMA‑IR1 (C‑peptide)a 2.96±1.32 2.40±0.53 HOMA‑IR2 (C‑peptide)a 1.60±1.5 1.05±0.55 aP<0.05. IR, insulin resistance; HOMA‑IR, Homeostatic Model Assessment of Insulin Resistance; HbA1c, glycosylated hemoglobin; HDLc, high‑density cholesterol; LDLc, low‑density lipoprotein cholesterol; TG, triglycerides; TSH, thyroid‑stimulating hormone; fT4, free thyroxine. with improved IR in some (15,16), but not all (17,18) studies. (C‑peptide)=1.5 + fasting glycemia (mmol/l) x [fasting Consequently, the aim of the present study was to analyze the C‑peptide (nmol/l)/2800 (19), and HOMA‑IR2 (insulin), association between subclinical hypothyroidism (SHO) and IR HOMA‑IR2 (C‑peptide)] was calculated with HOMA‑IR soft‑ in a female adult population from Bucharest, Romania. ware version 2.2.3, available online (20). The cut‑off value for defining IR was at 2.5 (19). Case study Microsoft Office Excel® file (Microsoft Corp.) was used to create the database. Inferential statistical analyses were carried A pilot, retrospective, case‑control study was designed out with the R computing and programming environment that included female patients examined by two endocri‑ v. 4.0.3 [R Core Team (2021). R: A language and environ‑ nologists and a diabetologist in an outpatient clinic in ment for statistical computing. R Foundation for Statistical Bucharest, Romania. The patients presented for a routine Computing, Vienna, Austria. URL https://www.R‑project. evaluation of obesity, thyroid disease or osteoporosis. org/.], under an RStudio local terminal, v. 1.1.456. Patients that were analyzed by the same laboratory Assuming that the probability of the exposure variable and had the complete hormonal and biochemical blood (hypothyroidism) in women from the general population is parameters were included. The variables considered were: ~8% (21), with a 1:1 ratio for cases and controls, a prevalence glycemia (mg/dl), glycosylated hemoglobin (HbA1c) (%), total of 25% of IR (22), and 80% power, a minimum (total) sample cholesterol (mg/dl), high‑density (HDLc) and low‑density size of 150 was necessary for a univariate logistic regression lipoprotein cholesterol (LDLc) (mg/dl), triglycerides (TG) model using a score test and a minimum (total) sample size (mg/dl), thyroid‑stimulating hormone TSH (µUI/ml), free of 187 for the same model using a Wald test, to be able to thyroxine‑fT4 (ng/dl), fasting insulin (µUI/ml) and fasting detect an odds ratio of 4 (log OR, 1.39). For the multivariate C‑peptide (ng/ml). Previous values (within one year) for these analysis, the sample size needed was much larger, but the pilot blood tests were searched retrospectively for each patient. study data allowed for the assessment of such a study and The study followed the Helsinki Declaration. Approval more precise calculations for such a study. Statistical power was obtained from the Ethics Committee of the Diabetes was computed using the ‘sample size logistic case‑control’ Department of ‘Carol Davila’ University of Medicine and R package V.0.0.6 (23). A P‑value (two‑tailed) <0.05 was Pharmacy (National Institute of Diabetes, Nutrition and considered significant. Metabolic Diseases N. C. Paulescu), Bucharest, Romania. Following univariate analysis (IR as a function of the presence or absence of hypothyroidism), a pre‑specified multi‑ Patient data. Data regarding age, weight, height, comor‑ variate model including BMI, age, and parameters of the lipid bidities and concomitant treatment were collected. Body profile (total cholesterol, LDLc, HDLc, and TG) as covariates mass index (BMI) was estimated as weight (kg)/height (m)2. (including relevant interactions) was developed. Assessment IR evaluation was carried out as follows. The homeostatic of the model fit was performed using specific functions from model assessment HOMA‑IR1 equation (insulin)=fasting the ‘LogisticDx’ R package [Osius and Rojek's tests, Stukels glycemia (mg/dl) x fasting insulin (µUI/ml)/405; HOMA‑IR1 tests, the area under the receiver‑operating curve (AUC) EXPERIMENTAL AND THERAPEUTIC MEDICINE 22: 1033, 2021 3 Table II. Comparison of the hypothyroidism and control groups, according to IR risk factors. Cases (n=91) Controls
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