Invest Clin 63(2): 126 - 136, 2022 https://doi.org/10.54817/IC.v63n2a02

Corresponding Author. Ayşe Tuğba Kartal. Ankara University Faculty of Medicine, Department of Pediatric Neuro-

logy, Ankara, Turkey, 06590, Cebeci/Çankaya/Ankara, Turkey. Telephone: +90 0531 791 7064.

E-mail: atugbakartal@gmail.com.

Evaluation of thyroid function and metabolic

parameters in obese and overweight

children: A prospective case-control study.

Ayşe Tuğba Kartal1, Abdulkadir Bozaykut2, Rabia Gönül Sezer2 and Tülay Güran3

1Ankara University Faculty of Medicine, Division of Pediatric Neurology, Ankara, Turkey.

2Zeynep Kamil Maternity and Children’s Health and Diseases Training and Research

Hospital, Department of Pediatrics, Istanbul, Turkey.

3Marmara University Faculty of Medicine, Division of Pediatric Endocrinology

and Diabetes, İstanbul, Turkey.

Key words: body mass index; insulin; metabolic parameters; obesity; thyroid hormone.

Abstract. Obesity is considered an important global public health chal-

lenge, and its prevalence is rapidly increasing in children. We investigated in

this study if the upper-normal TSH level may be associated with metabolic syn-

drome parameters, including obesity, high blood pressure, and dyslipidemia

and changes in insulin sensitivity in overweight and obese children. We also

investigated whether there is a relationship between BMI and these parameters.

This prospective case-control study comprised 145 participants (74 females,

71 males) aged 5–18 years. Participants were divided into three groups accord-

ing to their BMI z-score, as overweight, obese and control. The control group

included 35 age and sex-matched healthy subjects. Thyroid stimulating hor-

mone levels of control, overweight and obese groups were 2.14 ± 1.27, 2.97 ±

1.26 and 3.13 ± 1.11, respectively (p<0.05). There was a significant positive

correlation between TSH and the BMI, BMI z-scores between overweight and

obese groups (r=0.302, p=0.000), (r=0.121, p=0.004), respectively. The cur-

rent study suggests that increased serum TSH levels, even within the normal

range, in overweight and obese children is associated with the impairment of

metabolic parameters, including dyslipidemia and insulin sensitivity. For that

reason, TSH levels in the high-normal range should be considered as a risk fac-

tor for metabolic syndrome and its components.

Thyroid, metabolic parameters in obese 127

Vol. 63(2): 126 - 136, 2022

Evaluación de la función tiroidea y los parámetros metabólicos

en niños obesos y con sobrepeso: Un estudio prospectivo

de casos y controles.

Invest Clin 2022; 63 (2): 126 – 136

Palabras clave: índice de masa corporal; insulina; parámetros metabólicos; obesidad;

hormona tiroidea.

Resumen. La obesidad se considera un importante desafío de salud públi-

ca mundial y su prevalencia está aumentando rápidamente en los niños. En este

estudio, se investigó si el nivel normal superior de TSH puede estar asociado

con los parámetros del síndrome metabólico, incluida la obesidad, la presión

arterial elevada, cambios en los lípidos y la sensibilidad a la insulina, en niños

con sobrepeso y obesidad. También investigamos si existe una relación entre

el IMC y estos parámetros. En este estudio prospectivo de casos y controles se

incluyeron a 145 participantes (74 hembras, 71 varones) de entre 5 y 18 años.

Los participantes se dividieron en 3 grupos según el puntaje z del IMC, como

sobrepeso, obesidad y control. El grupo de control incluyó 35 sujetos sanos

emparejados por edad y sexo. Los niveles de hormona estimulante de la tiroides

de los grupos de control, con sobrepeso y obesos fueron 2,14 ± 1,27, 2,97 ±

1,26 y 3,13 ± 1,11, respectivamente (p <0,05). Hubo una correlación positiva

significativa entre la TSH y el BMI, la puntuación z del IMC entre los grupos con

sobrepeso y obesidad (r = 0,302, p = 0,000), (r = 0,121, p = 0,004), respec-

tivamente. Por esa razón, el nivel de TSH en el rango normal alto debe consi-

derarse como un factor de riesgo del síndrome metabólico y sus componentes.

Received: 08-09-2021 Accepted: 08-12-2021

INTRODUCTION

Obesity is considered an important glob-

al public health challenge, and its prevalence

is rapidly increasing in children 1,2. Obesity

is defined as a body mass index (BMI) ≥ 95th

percentile for children of the same age and

gender 3. It is believed that obese individu-

als are at an increased risk of metabolic syn-

drome and thyroid dysfunction 4,5.

There is a wide variation in reference

values for thyroid stimulating hormone lev-

els (TSH) in children 6. Many laboratories use

values of about 4.5 to 5.0 μIU/mL as the up-

per-normal range for TSH, and some experts

suggest that the upper-normal TSH level in

children should be lowered due to the risk of

obesity, dyslipidemia, and changes in blood

pressure (BP) and insulin sensitivity 7-10.

Thyroid hormone has a key role in reg-

ulating metabolism. It is well known that

overt hypothyroidism may cause obesity in

individuals; however, there is no clarity re-

garding subclinical hypothyroidism 11. Sub-

clinical hypothyroidism is defined biochemi-

cally as a normal serum free thyroxine level

(FT4) concentration in the presence of an

elevated serum TSH concentration 11. Thy-

roid hormone regulates both basal metabo-

lism and thermogenesis 12,13. Moreover, it is

involved in glucose and fat metabolism 12.

Because of these interactions between thy-

128 Tuğba Kartal et al.

Investigación Clínica 63(2): 2022

roid hormones and metabolic parameters,

there is an increasing doubt of whether even

mild thyroid dysfunction may induce obesity

in children 14,15.

We speculated in this study that the up-

per-normal TSH level may be associated with

metabolic syndrome parameters, including

obesity, blood pressure, lipid and insulin sen-

sitivity in overweight and obese children. We

also investigated whether there is a relation-

ship between BMI and these parameters.

MATERIALS AND METHODS

Study population

This prospective case-control study

comprised 145 participants (74 females, 71

males) aged 5–18 years, and it was conduct-

ed in an ethnically homogeneous population

between 2012 and 2015. Participants were

divided into three groups according to their

BMI z-score, as overweight (n=64), obese

(n=46) and control. The control group in-

cluded 35 age and sex-matched healthy sub-

jects. Written informed consent and assent

were obtained from participants and par-

ents. Ethics approval was obtained from the

Local Ethics Committee (protocol number/

date:9204/09.04.-12) for this research, and

the study was managed in accordance with

the Declaration of Helsinki. Children with

any known disease (any thyroid disease, car-

diovascular disease, etc.) or using any phar-

macologic treatment known to affect BMI

z-score, thyroid hormones, blood pressure,

lipid and glucose metabolism were excluded

from the study.

Anthropometric measurements

Standing height (SH), body weight

(BW), blood pressure measurement, waist

and hip circumferences were obtained from

all participants and made according to the

World Health Organization recommen-

dations 16. Blood pressure was measured

in the sitting position after five minutes

of rest in a quiet environment with a me-

chanical sphygmomanometer. Blood pres-

sure was measured twice and the average

of the measurements was used as the final

value. Standing height was measured with

a Harpenden stadiometer, and participants

were weighed in lightweight clothing. Body

mass index was calculated as body weight

in kilograms divided by the square of stand-

ing height in meters (BMI= kg/m2). We

used BMI z-scores to compare BMI values

across different ages and by gender. Over-

weight was defined as +1< BMI z-score ≤

+2 SDs, and obesity was defined as a BMI

z-score over 2 SDs from the mean of natio-

anal charts 17.

Laboratory studies

The blood samples were obtained af-

ter an 8-12-hour overnight fast for analy-

sis of the lipid profile, fasting plasma glu-

cose (FPG), fasting insulin (FI), TSH and

FT4. Total cholesterol (TC), high density

lipoprotein cholesterol (HDL-C) and tri-

glyceride (TG) levels were measured by an

enzymatic colorimetric assay (Roche Cobas

İntegra® 800, Mannheim, Germany). Low

density lipoprotein cholesterol (LDL-C)

was calculated for samples containing TG

<400 mg/dL using the Friedewald formu-

la. Fasting plasma glucose was measured

by the hexokinase method (Roche Cobas

İntegra® 800, Mannheim, Germany). Fast-

ing Insulin, TSH and FT4 were measured by

the electrochemiluminescence immunoas-

say method (The ADVIA Centaur® CP Im-

munoassay System, Erlangen, Germany).

The reference values of TSH and FT4 in our

center are 0.38-4.5 μIU/mL and 0.58-1.38

ng/dL, respectively. Insulin resistance was

estimated by the homeostatic model [Ho-

meostasis model assessment of insulin re-

sistance (HOMA-IR) = fasting plasma glu-

cose x fasting insulin /405] 9.

Statistical analysis

The data were evaluated using the Sta-

tistical Package for Social Sciences 21.0

program for Windows. Continuous vari-

ables were calculated as mean+standard

Thyroid, metabolic parameters in obese 129

Vol. 63(2): 126 - 136, 2022

deviation. The normality of the distribu-

tion of continuous variables was con-

firmed by the Kolmogorov-Smirnov test.

A one-way analysis of variance tests was

used to evaluate comparisons between the

groups. Pearson correlation analysis was

used to evaluate the relationships. A p-

value <0.05 was accepted as statistically

significant.

The sample size estimation of the study

was calculated by using G*Power 3.1.9.4

(with 90% power and 5% type I error rates).

RESULTS

The study included 110 overweight

and obese participants and 35 healthy con-

trols. The male/female ratio of overweight

and obese groups was 31/33 and 22/24,

respectively, while it was 18/17 for the con-

trol group (p >0.05). Mean age of control,

overweight and obese groups were 9.7 ± 3.6;

10.3 ± 2.6; 10.8 ± 2.7 years, respectively (p

>0.05). The anthropometric and laboratory

characteristics of all participants are sum-

marized in Table 1.

Table 1

Anthropometric and laboratory characteristics of the study participants.

Parameters

Control group

(n=35)

Overweight group

(n=64)

Obese group

(n=46) p

Mean ± SD

Age, yr 9.7 ± 3.6 10.3 ± 2.6 10.8 ± 2.7 0.12

Gender (M/F),

(n,%)

18 (51.4)/17

(48.5)

31 (48.4)/33

(51.5)

22(47.8)/24

(52.1) 0.64

BMI (kg/m²) 20.94 ± 2.46 27.26 ± 1.29 32.98 ± 2.87 <0.01

BMI-Z score 0.63 ± 0.15 1.59 ± 0.48 2.47 ± 0.36 <0.01

WHR (cm/cm) 0.74 ± 0.03 0.82 ± 0.06 0.87 ± 0.07 <0.01

SBP (mmHg 106.6 ± 9.3 107.8 ± 12.2 110.3 ± 10.6 0.22

DBP (mmHg) 69.2 ± 5.9 69.1 ± 7.1 73.5 ± 9 0.13

TC (mg/dL) 156.1 ± 15.8 169.3 ± 38.3 171.93 ± 35.8 <0.01

TG ( mg/dL ) 89.6 ± 22.5 97.2 ± 49.3 101.8 ± 37 <0.01

LDL – C (mg/dL ) 92 ± 14.5 97.4 ± 30 105.3 ± 31.6 0.01

HDL– C (mg/dL) 46.9 ± 10.3 48 ± 11.7 47.7 ± 12.9 0.90

FPG (mg/dL) 78.9 ± 12.7 89.6 ± 5.6 101.9 ± 6.2 0.03

Insulin (μU/mL) 13.32 ± 7.35 15.14 ± 6.32 21.69 ± 10.99 <0.01

HOMA-IR 1.12 ± 1.79 2.05 ± 1.45 2.44 ± 2.54 <0.01

TSH (μIU/mL) 2.14 ± 1.27 2.97 ± 1.26 3.13 ± 1.11 <0.01

FT4 (ng/dL) 1.21 ± 0.18 1.23 ± 0.14 1.18 ± 0.19 0.23

BMI, body mass index; WHR, waist-to-hip ratio; SBP, systolic blood pressure; DBP, diastolic blood pressure; TC, total

cholesterol; TG, triglycerides; LDL-C, low density lipoprotein cholesterol; HDL-C, high density lipoprotein choles-

terol; FPG, fasting plasma glucose; HOMA-IR, homeostasis model assessment of insulin resistance; TSH, thyroid-

stimulating hormone; FT4, free thyroxine.

130 Tuğba Kartal et al.

Investigación Clínica 63(2): 2022

Thyroid stimulating hormone levels of

the control, overweight and obese groups

were 2.14 ± 1.27, 2.97 ± 1.26 and 3.13 ±

1.11, respectively (p<0.05), and the FT4

levels of control, overweight and obese sub-

jects was 1.21 ± 0.18, 1.23 ± 0.14 and 1.18

± 0.19, respectively (p >0.05). TSH levels

were found to be slightly high in 13.6% (15

out of 110 subjects) of overweight and obese

groups. There was a significant positive cor-

relation between TSH and BMI, BMI z-scores

between the overweight and obese groups

(r=0.302, p=0.000), (r=0.121, p=0.004),

respectively. Additionally, FT4 and BMI, BMI

z-score between the overweight and obese

groups (r=-0.042, p=0.009), (r=-0.023,

p=0.011), respectively. Correlation between

thyroid hormones and metabolic parameters

in overweight and obese participants were

summarized in Table 2.

The overweight and obese groups had

higher TC, LDL-C and TG levels than the

control group (p<0.05), however, HDL-C lev-

el was significantly different between groups

(p >0.05). We found a significant positive

correlation between TSH and TC, LDL-C, TG

(r=0.227, p=0.019), (r=0.125, p=0.016)

and (r=0.021, p=0.010), respectively, but

not with HDL-C (r=0.031, p=0.235).

Fasting plasma glucose, insulin and

HOMA-IR values were significantly differ-

ent among groups (p <0.05), (Table 1) and

we found a significant positive correlation

between TSH and FPG, insulin, HOMA-IR

(r=0.011, p=0.018), (r=0.035, p=0.044),

(r=0.023, p=0.032), respectively. However,

there was not a significant correlation be-

tween FT4 and FPG, insulin, HOMA-IR (r=-

0.013, p=0.068), (r=-0.019, p=0.124),

(r=-0.011, p=0.221), respectively.

The correlation between thyroid hor-

mones (TSH and FT4) and BMI, HOMA-IR in

overweight and obese children can be seen

in Fig. 1.

The anthropometric and laboratory

characteristics of overweight and obese

groups according to the gender and age are

summarized in Tables 3 and 4.

DISCUSSION

Obesity is a critical public health prob-

lem associated with many chronic disorders,

including metabolic syndrome and thyroid

dysfunction 18,19. The most common thy-

roid dysfunction is hyperthyrotropinemia,

which is believed to be an adaptive process

to excess body mass, energy expenditure and

thermogenesis 3,20. In the present study, we

found a significant association and correla-

tion between TSH and BMI, BMI z-scores

in overweight and obese children. Thyroid

stimulating hormone levels in these groups

were higher than in the healthy control

group. FT4 had a significant negative corre-

lation with BMI, BMI z-scores, however, not

a significant association. These findings are

consistent with previous studies 16,21,22.

Table 2

Correlation between thyroid hormones

and metabolic parameters in overweight

and obese subjects.

Parameters TSH FT4

r p r p

Age -0.023 0.000 0.010 0.231

BMI 0.302 0.000 -0.042 0.009

BMI-Z score 0.121 0.004 -0.023 0.011

WHR 0.130 0.010 -0.025 0.018

SBP 0.231 0.006 0.173 0.014

DBP 0.181 0.023 0.052 0.031

TC 0.227 0.019 -0.143 0.056

TG 0.021 0.010 -0.041 0.072

LDL – C 0.125 0.016 -0.055 0.133

HDL– C 0.031 0.235 -0.012 0.151

FPG 0.011 0.018 -0.013 0.068

Insulin 0.035 0.044 -0.019 0.124

HOMA-IR 0.023 0.032 -0.011 0.221

Thyroid, metabolic parameters in obese 131

Vol. 63(2): 126 - 136, 2022

The mechanisms of the association be-

tween TSH and obesity is not definitely un-

derstood. However, several mechanisms have

been proposed to explain this complex rela-

tionship, including derangement of the hy-

pothalamic–pituitary axis, thyroid hormone

resistance, changes in the activity of deio-

dinases, the impact of leptin and chronic low

grade inflammation, etc. 23,24.

According to recent studies, the preva-

lence of isolated hyperthyrotropinemia in

overweight and obese children is thought

to be between 15% and 23% 25,26. However,

in our study, it was found to be only 15 out

of 110 children (13.6%). The case selection

and study design may be the reason for this

discrepancy.

Classically, obesity-associated dyslipid-

emia is a well-known condition, and charac-

terized by elevated TC, LDL-C, TG and de-

creased HDL-C level, and has been described

both in overt and subclinical hypothyroid-

ism 27,28. Consistent with this, we found that

TC, LDL-C and TG levels were higher in the

overweight and obese groups than in the

control group. However, the HDL-C level was

significantly different between groups. That

was confirmed in another study conducted

by Aeberli et al. 24. Additionally, we found a

significant positive correlation between TSH

Fig. 1. Correlation between thyroid hormones (TSH and FT4) and BMI, HOMA-IR in overweight and obese

children.

132 Tuğba Kartal et al.

Investigación Clínica 63(2): 2022

and TC, LDL-C, TG, and similar observations

were reported by Le et al. and Canaris et

al.9,29. In contrast to these findings, a retro-

spective analysis of a large community-based

pediatric population in Rochester, which was

conducted by Nader et al., found only a sig-

nificant positive correlations between TSH

and TG 30. These differences may be due to

the sample size and diverse characteristics

of the study participants.

The relationship between thyroid hor-

monal derangement and glucose metabolism

in obesity is a complex interdependent inter-

action 31,32. Recently, the study performed

by Ambrosi et al. in Milan shown that TSH

had a significant positive correlation with

fasting insulin and HOMA-IR in 581 obese

patients33. Similar results were reported by

Reinehr et al., and our findings were also in

line with these studies 26. However, in con-

trast to these findings, this association was

not shown in some other studies 34,35.

In our study, metabolic parameters and

blood pressure values were also compared be-

tween overweight and obese patient groups on

the basis of age and gender. However, we did

not find a significant association. These find-

ings are consistent with previous studies 21,36,37.

The main strength of this study is that

it was conducted prospectively in a healthy

control group and in an ethnically homo-

geneous population. The limitations of the

study include the relatively small sample

size, a lack of evaluation of free triiodothyro-

nine, thyroxine-binding globulin and thyroid

peroxidase.

Table 3

Anthropometric and laboratory characteristics of overweight and obese groups

according to the gender.

Parameters Male Female p

Mean ± SD

Gender, n, (%) 53 (48.2) 57 (51.8) -

Age, yr 10.2 ± 2.8 11.3 ± 3.3 0.09

BMI (kg/m²) 29.36 ± 3.42 29.83 ± 3.59 0.50

BMI-Z score 2.01 ± 0.54 2.18 ± 0.46 0.16

WHR (cm/cm) 0.87 ± 0.05 0.84 ± 0.07 0.23

SBP (mmHg 108.5 ± 12.1 111.9 ± 12.7 0.89

DBP (mmHg) 71.1 ± 7.9 70.8 ± 8.4 0.85

TC (mg/dL) 167.5 ± 36.3 164.6 ± 37.2 0.10

TG (mg/dL) 99.9 ± 45.6 98.7 ± 44.1 0.88

LDL – C (mg/dL ) 102.7 ± 31.6 98 ± 30.2 0.08

HDL– C (mg/dL) 47.7 ± 12.9 48 ± 11.8 0.93

FPG (mg/dL) 96.1 ± 6.7 94.2 ± 8.5 0.41

Insulin (μU/mL) 16.78 ± 8.48 19.12 ± 9.35 0.06

HOMA-IR 2.16 ± 1.96 2.28 ± 2.18 0.08

TSH (μIU/mL) 2.99 ± 1.08 3.09 ± 1.28 0.66

FT4 (ng/dL) 1.22 ± 0.17 1.19 ± 0.13 0.31

BMI, body mass index; WHR, waist-to-hip ratio; SBP, systolic blood pressure; DBP, diastolic blood pressure; TC,

total cholesterol; TG, triglycerides; LDL-C, low density lipoprotein cholesterol; HDL-C, high density lipoprotein

cholesterol; FPG, fasting plasma glucose; HOMA-IR, homeostasis model assessment of insulin resistance; TSH,

thyroid-stimulating hormone; FT4, free thyroxine.

Thyroid, metabolic parameters in obese 133

Vol. 63(2): 126 - 136, 2022

The most important finding of this study

is that increasing serum TSH level, even with-

in the upper-normal level, in overweight and

obese children can be associated with the im-

pairment of metabolic parameters, including

dyslipidemia and insulin sensitivity. Although

the mechanism underlying this condition

has not been fully elucidated yet, it is maybe

an early sign of hypothyroidism, an autoim-

mune thyroid disease, or it may result from

derangement of the hypothalamic–pituitary

axis, the impact of leptin and chronic low

grade inflammation, etc. 23,24,38,39.

As a result, the upper-normal serum

TSH level should be considered as a risk fac-

tor of metabolic syndrome and its compo-

nents in overweight and obese children, and

this condition should be taken into account

by researchers.

Funding

None.

Ethical approval

Given by Ethics Committee of Zeynep

Kamil Maternity and Children’s Health and

Diseases Training and Research Hospital

Ethics Committee (9204/09.04.2012).

Table 4

Anthropometric and laboratory characteristics of overweight and obese groups according to the age.

Parameters <11 years ≥11 years p

Mean ± SD

Male/Female, n, (%) 22 (39.3) / 34 (60.7) 19 (35.2) / 35 (64.8) 0.40

Age, yr 8.39 ± 1.7 13.5 ± 1.9 0.02

BMI (kg/m²) 28.73 ± 2.31 30.64 ± 3.47 0.14

BMI-Z score 2.05 ± 0.57 2.24 ± 0.3 0.21

WHR (cm/cm) 0.83 ± 0.05 0.85 ± 0.07 0.12

SBP (mmHg 108.9 ± 12.8 112.8 ± 9.9 0.31

DBP (mmHg) 69.4 ± 7.1 70.5 ± 8.6 0.42

TC (mg/dL) 168.5 ± 39.1 169.6 ± 35.4 0.87

TG (mg/dL) 98 ± 44.9 104.4 ± 43.8 0.22

LDL – C (mg/dL ) 103.6 ± 32.9 100 ± 29.2 0.58

HDL– C (mg/dL) 47.7 ± 10.9 48.1 ± 13.4 0.85

FPG (mg/dL) 91 ± 5.4 95 ± 6.5 0.39

Insulin (μU/mL) 17.88 ± 5.89 19.98 ± 10.79 0.22

HOMA-IR 2.35 ± 1.39 2.27 ± 2.51 0.34

TSH (μIU/mL) 2.94 ± 1.03 2.81 ± 1.37 0.87

FT4 (ng/dL) 1.22 ± 0.15 1.19 ± 0.13 0.22

BMI, body mass index; WHR, waist-to-hip ratio; SBP, systolic blood pressure; DBP, diastolic blood pressure; TC, total

cholesterol; TG, triglycerides; LDL-C, low density lipoprotein cholesterol; HDL-C, high density lipoprotein choles-

terol; FPG, fasting plasma glucose; HOMA-IR, homeostasis model assessment of insulin resistance; TSH, thyroid-

stimulating hormoneL; FT4, free thyroxine.

134 Tuğba Kartal et al.

Investigación Clínica 63(2): 2022

Conflict of Interest

None.

Author’s ORCID numbers

• Ayşe Tuğba Kartal:

0000-0003-4362-8511

• Abdulkadir Bozaykut:

0000-0001-7589-5978

• Rabia Gönül Sezer:

0000-0002-9447-3583

• Tülay Güran: 0000-0003-2658-6866

Author contributions

All authors made a significant contribu-

tion (concept and design of the study, acqui-

sition of data, analysis and interpretation of

the data, drafting or critically reviewing the

manuscript, and final approval of the version

of the article) to this article.

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