Abstract
We proceeded with this study to investigate the relationship between hypothyroidism and lipid profile disturbance. A cross-sectional study at Al- Mowasat University Hospital in Damascus was conducted from March 2021 to March 2022, and included 324 adults. For each participant with abnormal thyroid stimulating hormone (TSH), free thyroxine (FT4) was requested. The participants were categorized into 3 groups: euthyroid (226 participants), subclinical hypothyroidism (SCH) (75 participants), and overt hypothyroidism (23 participants). Fasting lipid profile was tested as: cholesterol (Chol), triglycerides (TG), low density lipoprotein (LDL), and high density lipoprotein (HDL). A significant relationship between hypothyroidism and dyslipidemia was noticed. LDL, TG, and Chol but not HDL showed a significant difference between study groups (euthyroidism, subclinical, and overt hypothyroidism). The lowest levels of these parameters were in euthyroidism and increased in subclinical and overt hypothyroidism subsequently. Overt hypothyroidism showed a significant difference in LDL, TG, and Chol compared to euthyroidism, however, we did not find a difference in lipid parameters in SCH compared to euthyroidism. LDL and Chol showed significant differences between subclinical and overt hypothyroidism. TSH had a positive weak correlation with LDL, TG, and Chol, however, there was no correlation with HDL. Also, FT4 had a negative weak correlation with LDL, TG, and Chol, however, there was a positive correlation with HDL. Our findings suggest a higher level of lipids (LDL, TG, and Chol) among SCH and overt hypothyroidism compared to general population. A weak correlations of lipid parameters with TSH and FT4 were detected. It is not well evident whether a restoration of euthyroidism might influence the morbidity and mortality, especially cardiovascular comorbidities, in this population, which mandates future studies.
Keywords: cholesterol, high density lipoprotein, low density lipoprotein, overt hypothyroidism, subclinical hypothyroidism, triglycerides
1. Introduction
Hypothyroidism is thyroid inability of synthesis and secrete sufficient amount of thyroid hormones, which stimulates the pituitary to produce thyroid stimulating hormone (TSH).[1] The prevalence of overt and subclinical hypothyroidism (SCH) is varied worldwide (5% and 3–12%; respectively). Meanwhile 4.6% of adults in USA and 5% of adults in Europe have hypothyroidism.[1–3] On the other hand, the prevalence of overt hypothyroidism is 29.1% in Saudi Arabia, while the prevalence of overt and SCH in Libya is 1.12% and 6.18%; respectively.[4,5] Hypothyroidism increases with aging, and it is more common in women than men.[2] Iodine deficient is the most common cause in underdeveloped parts of the world.[3] The long-standing adaption of iodine–deficient diet may be the cause of hypothyroidism, along with many environmental causes like vitamin D and selenium deficiency.[3]
Thyroid hormone regulates normal growth and development, essential in regulating metabolism process, and increases metabolism rate through its effects on protein, carbohydrate, and fat.[6,7] Thyroid hormone affects synthesis, mobilization, and degradation of lipids. The degradation is affected more than the synthesis by the thyroid hormone.[7] Beyond their effect on lipid profile thyroid hormones can equally affect a number of other metabolic parameters related to cardiovascular disease risk.[8,9]
Thyroid hormone has many effects on the cardiovascular system, that increases heart rate, stroke volume, and blood volume, hence increases cardiac output.[10] The relaxation of vascular smooth muscle is impaired in hypothyroidism, and the endothelial nitric oxide availability is also decreased, which increases systemic vascular resistance.[11] Hypothyroidism is associated with QTC prolongation and a heightened risk for torsades de pointes. About one-fourth of patients with overt hypothyroidism have reversible predominantly diastolic hypertension.[4] SCH is also associated with an increased risk of congestive heart disease events and mortality particularly with higher TSH levels, when TSH concentration reached to 10 mIU/L or greater.[5] Profound and prolonged untreated hypothyroidism can cause biventricular heart failure.[4]
Dyslipidemia is also associated with cardiovascular disease, strokes and peripheral vascular diseases.[6] Cholesterol (Chol) deposition within the arterial wall is a major component of atherosclerosis, and Chol-lowering therapies have shown a reduction in the incidence of cardiovascular events, like stroke and myocardial infarction.[7]
Many worldwide studies were conducted to evaluate the relation between hypothyroidism and dyslipidemia. Since a high proportion of hypothyroidism patients were seen in our daily practice and limited studies were published from Syria, we proceeded with this study to investigate the lipid profile disturbances between thyroid subgroups. Also, the second aim was to study the relationship of lipid parameters with free thyroxine (FT4) and TSH.
2. Material and methods
This cross-sectional study was conducted at Al-Mowasat University Hospital, Damascus, Syria, from March 2021 to March 2022. The study sample comprised of 324 participants including out- patient and in-patient departments. An informed consent has been taken from participants and the study was approved by the Damascus University Review Board and in accordance with the Declaration of Helsinki.
Inclusion criteria was as follow: newly diagnosed hypothyroid patients (subclinical and overt), age ≥18 years with no history of thyroxine and hypolipidemic drugs. Exclusion Criteria was as follow: diabetes mellitus, pregnancy, hypercortisolism or pituitary diseases, and history of drugs including; thyroxine, hypolipidemic, oral contraceptives, androgens, steroids, and immunosuppressants.
A questionnaire was filled out for each participant, which included questions about personal information, medical and pharmacological history and personal habits. For each participant with abnormal TSH followed by FT4 test. Participants were categorized according to the American Thyroid Association criteria into 3 groups[12]; euthyroid, when TSH between 0.4 and 4.5 mic IU/mL, SCH, when TSH >4.5 with normal level of FT4, and overt hypothyroidism, when TSH >4.5 with low level of FT4. Automated electrochemiluminescence immunoassay (Elecsys 2010 analyzers, Mannheim, Germany) was used for TSH (Third generation) and FT4 measurement.
Blood samples were drawn in the morning between 8 and 10 AM after overnight fasting (at least ≥12 h). Fasting lipid profile was tested according to their availability in the hospital, which included Chol, triglycerides (TG), low density lipoproteins (LDL), high density lipoprotein (HDL) and Friedewald formula was used in calculating lipids levels. Lipid parameters were measured using an enzymatic colorimetric assay (Hitachi 912 device). Fasting plasma glucose after overnight fasting (at least 8–10 hours) was obtained. Weight was measured in light clothing and without shoes and height was measured in the standing position without shoes. Body mass index (BMI) was calculated as weight (kg) divided by squared height (m2). Participants were divided into 5 groups based on BMI: normal weight (BMI: ≥18.5–<25 kg/m2), overweight (BMI: ≥25–<30 kg/m2), obesity Class I (BMI: ≥30–<35 kg/m2), obesity Class II (BMI: ≥35–<40 kg/m2), and obesity Class III (BMI ≥40 kg/m2).[13]
2.1. Statistical analysis
The data obtained has been inserted into Microsoft Excel Worksheet. The categorical data has been expressed as rates, ratios and proportions has been used to compare the data. The continuous data have been expressed as mean ± standard deviation and the comparison has been done using unpaired “t” test. A probability value (“P” value) of less than or equal to 0.05 has been considered as statistically significant. SPSS software version 23.0 (IBM, Armonk, NY) was used. One Way ANOVA test to assess deference between the median of more than 2 samples. Tukey test to assess deference between 2 symmetric samples. Games-Howell test to assess deference between 2 asymmetric samples. Spearman correlation was used to assess a statically important relation between 2 variables. Pearson Correlation was used to measure the linear correlation between 2 variables.
3. Results
3.1. Baseline characteristics (Table 1)
Table 1.
Baseline demographic, hormonal profile, and lipids profile of patients.
| N | Mean | SD | Minimum | Maximum | |
|---|---|---|---|---|---|
| Age (yr) | 323 | 42 | 13.4 | 18 | 86 |
| Height (cm) | 315 | 159.79 | 11.9 | 1.68 | 190 |
| Weight (kg) | 321 | 80.16 | 17.34 | 41.0 | 129 |
| BMI (kg/m2) | 315 | 31.25 | 6.72 | 17 | 51 |
| SBP (mm Hg) | 321 | 115.44 | 15.9 | 90 | 180 |
| DBP (mm Hg) | 321 | 74.03 | 9.32 | 60 | 100 |
| TSH (mIU/mL) | 324 | 6.74 | 17.15 | 0.4 | 189 |
| FT4 (ng/dL) | 172 | 1 | 0.3 | 0.2 | 1.9 |
| CHOL (mg/dL) | 254 | 182.64 | 40.11 | 95 | 361 |
| LDL (mg/dL) | 196 | 110.11 | 34.15 | 40 | 225 |
| HDL (mg/dL) | 63 | 43.76 | 11.06 | 20 | 72 |
| TG (mg/dL) | 317 | 132.78 | 63.51 | 30 | 581 |
| GLU (mg/dL) | 315 | 92.22 | 11.48 | 60 | 124 |
BMI = body mass index, CHOL = cholesterol, DPB = diastolic blood pressure, GLU = fasting glucose, HDL = high density lipoprotein, LDL = low density lipoprotein, SBP = systolic blood pressure, SD = standard deviation, TG = triglycerides, TSH = thyroid stimulating hormone, FT4 = free thyroxine.
Of a total of 324 patients, euthyroidism -TSH (0.4–4.5 mIU/mL)- was reported in 226 (69.7%) participants, SCH (TSH > 4.5 with normal level of FT4) was reported in 75 (23.1%) participants, and overt hypothyroidism (TSH > 4.5 with low level of FT4) was reported in 23 (7%) participants. The study sample comprised of 36 (11.1%) males and 288 (88.9%) females, with a mean age of 42 ± 13.4 years (ranged 18–86 years), and a mean BMI of 31.2 ± 6.6 kg/m2 (ranged 17–51 kg/m2).
The mean TSH level was 6.74 ± 17.15 mIU/mL and the mean FT4 level was 1 ± 0.3 ng/dL. While the mean levels of lipid parameters were as follows; Chol (182.64 ± 40.11 mg/dL), LDL (110.11 ± 34.15 mg/dL), HDL (43.76 ± 11.06 mg/dL), TG (132.78 ± 63.51 mg/dL).
3.2. Lipid profile with thyroid subgroups (Tables 234)
Table 2.
Comparison of lipid profile between thyroid subgroups.
| Variables | TSH Groups | N | Mean | ± SD | 95% CI for Mean | Min | Max | P value | |
|---|---|---|---|---|---|---|---|---|---|
| Lower level | Upper level | ||||||||
| HDL | Euthyroid | 84 | 49.45 | 21.3 | 44.8 | 54.1 | 7 | 160 | .621 |
| SCH | 35 | 47.57 | 16.24 | 42 | 53.2 | 15 | 92 | ||
| Overt | 17 | 44.41 | 21.6 | 33.3 | 55.5 | 8 | 99 | ||
| Total | 136 | 48.34 | 20 | 44.9 | 51.7 | 7 | 160 | ||
| LDL | Euthyroid | 136 | 104.51 | 30.6 | 99.3 | 109.7 | 50 | 169 | .000 |
| SCH | 46 | 109.7 | 31.3 | 100.4 | 119 | 40 | 179 | ||
| Overt | 20 | 144.8 | 42 | 125.1 | 164.5 | 56 | 225 | ||
| Total | 202 | 109.7 | 34 | 105 | 114.4 | 40 | 225 | ||
| TG | Euthyroid | 222 | 126.4 | 54.3 | 119.2 | 133.6 | 30 | 335 | .016 |
| SCH | 75 | 138.6 | 68.2 | 122.9 | 154.3 | 53 | 426 | ||
| Overt | 23 | 187 | 104.2 | 142 | 232 | 45 | 581 | ||
| Total | 320 | 133.6 | 64.2 | 126.6 | 140.7 | 30 | 581 | ||
| CHOL | Euthyroid | 173 | 177.9 | 38.2 | 172.2 | 183.6 | 95 | 361 | .000 |
| SCH | 64 | 184 | 36.1 | 175 | 193 | 106 | 262 | ||
| Overt | 19 | 223.1 | 47.8 | 200 | 246.1 | 160 | 309 | ||
| Total | 256 | 182.8 | 40.1 | 177.8 | 187.7 | 95 | 361 | ||
| BMI | Euthyroid | 220 | 31.2 | 6.9 | 30.2 | 32.1 | 0.25 | 51 | .929 |
| SCH | 75 | 31 | 7.1 | 29.4 | 32.6 | 18.7 | 50 | ||
| Overt | 22 | 30.6 | 6.3 | 27.8 | 33.4 | 21 | 46.4 | ||
| Total | 317 | 31.1 | 6.9 | 30.3 | 31.8 | 0.25 | 51 | ||
HDL = high density lipoprotein, LDL = low density lipoprotein, SCH = subclinical hypothyroidism, SD = standard deviation, TG = triglycerides, TSH = thyroid stimulating hormone, Overt = overt hypothyroidism.
Table 3.
Comparison of lipid parameters between thyroid subgroups.
| Variables | TSH group (I) | Other TSH groups (J) | Mean difference (I–J) | P value |
|---|---|---|---|---|
| LDL | Euthyroid | SCH | −5.19 | .342 |
| Overt | −40.3 | .000 | ||
| SCH | Overt | −35.1 | .000 | |
| TG | Euthyroid | SCH | −12.2 | .343 |
| Overt | −60.6 | .029 | ||
| SCH | Overt | −48.4 | .109 | |
| CHOL | Euthyroid | SCH | −6.1 | .280 |
| Overt | −45.2 | .000 | ||
| SCH | Overt | −39.1 | .000 |
CHOL = cholesterol, LDL = low density lipoprotein, Overt = overt hypothyroidism, SCH = subclinical hypothyroidism, TG = triglycerides, TSH = thyroid stimulating hormone.
Table 4.
Correlation of lipid parameters with FT4 and TSH.
| Variables | TSH | FT4 | ||||
|---|---|---|---|---|---|---|
| N | Correlation coefficient | P value* | N | Correlation coefficient | P value* | |
| CHOL | 256 | 0.167 | .007 | 141 | −0.255 | .002 |
| LDL | 202 | 0.195 | .005 | 107 | −0.374 | .000 |
| HDL | 136 | −0.138 | .108 | 76 | 0.285 | .013 |
| TG | 320 | 0.207 | .000 | 170 | −0.272 | .000 |
CHOL = cholesterol, FT4 = free thyroxine, HDL = high density lipoprotein, LDL = low density lipoprotein, TG = triglycerides, TSH = thyroid stimulating hormone.
Correlation is significant at the 0.05 level (2-tailed).
LDL, TG, and Chol showed significant differences between study groups (euthyroidism, SCH, and overt hypothyroidism) (P < .0001, .016, <.0001; respectively). Also, the levels of LDL, TG, and Chol were lower in euthyroidism compared to subclinical and overt hypothyroidism. The lowest levels of these parameters were in euthyroidism and increased in subclinical and overt hypothyroidism subsequently (Table 2).
The mean level of LDL in the total sample was (109.7 ± 34), where the lowest levels was in euthyroid group (104.51 ± 30.6), slightly increased in SCH (109.7 ± 31.3), and overtly increased in overt hypothyroidism (144.8 ± 42). The mean level of TG in the total sample was (133.6 ± 64.2), where the lowest levels was in euthyroid group (126.4 ± 54.3), followed by increasing levels in SCH (138.6 ± 68.2), and the highest levels were observed in overt hypothyroidism (187 ± 104.2). The mean level of Chol in the total sample was (182.8 ± 40.1), where the lowest levels was in euthyroid group (177.9 ± 38.2), slightly increased in SCH (184 ± 36.1), and overtly increased in overt hypothyroidism (223.1 ± 47.8), (Table 2).
On the other hand, HDL and BMI did not show significant differences between study groups (P = .62 and .92; respectively). However, a higher level of HDL was observed in euthyroid group (49.45 ± 21.3) compared to decreasing levels in SCH and overt hypothyroidism (47.57 ± 16.24 and 44.41 ± 21.6; respectively). However, means of BMI were nearly comparable between study groups, it showed abnormal levels and the mean BMI of the total sample was high (31.1 ± 6.9), (Table 2).
LDL, TG, and CHOL did not show a significant difference in comparing euthyroidism to SCH (P = .342, .343, .28; respectively) (Table 3); however, the difference between mean lipid levels demonstrated higher levels in SCH compared to euthyroidism.
LDL, TG, and CHOL showed significant differences in comparing euthyroidism to overt hypothyroidism (P < .0001 for LDL and Chol, P = .029 for TG) (Table 3). The difference between mean lipid levels demonstrated higher levels in overt hypothyroidism compared to euthyroidism.
LDL and Chol showed significant differences between SCH and overt hypothyroidism (P < .0001 for both), however TG did not differ between SCH and overt hypothyroidism (P = .109) (Table 3). On the other hand, the difference between mean lipid levels demonstrated higher levels in overt hypothyroidism compared to SCH.
There was a weak and significant correlation between lipid profile with TSH levels, where TSH positively correlated with LDL, TG, and Chol, however, there was no correlation with HDL (Table 4). Also, all lipid parameters also showed a weak and significant correlation with FT4 levels. There was a negative correlation with LDL, TG, and Chol, however, there was a positive correlation with HDL (Table 4).
4. Discussion
In this prospective cross-sectional study, the prevalence of subclinical and overt hypothyroidism was 23.1% and 7%; respectively. A significant relationship between hypothyroidism and dyslipidemia was noticed. Lipid profile (LDL, TG, and Chol but not HDL) showed a significant difference between study groups (euthyroidism, SCH, and overt hypothyroidism), where the lowest levels of these parameters were in euthyroidism and increased in subclinical and overt hypothyroidism subsequently. Overt hypothyroidism showed a significant difference in lipid parameters (LDL, TG, and Chol) compared to euthyroidism, however, we did not find a difference in lipid parameters in SCH compared to euthyroidism. LDL and Chol showed significant differences between subclinical and overt hypothyroidism. There was a weak and significant correlation between lipid profile with FT4 and TSH levels.
The prevalence of hypothyroidism in the general population is 4.6% from the third National Health and Nutrition Examination Survey (NHANES III), while 9.5% of the Colorado prevalence study participants had elevated levels of TSH.[14] The worldwide variance in the prevalence of hypothyroidism depending on age, sex, and diet.[1–3,11] Indeed, the prevalence is 1.4% to 13% in patients with hyperlipidemia, indicating that thyroid failure is common and may be undetected in these patients.[11,15] SCH is a far more common disorder than overt hypothyroidism ranging from 4.3% to 9% and may progress to overt hypothyroidism.[3,16,17]
In this study, a high prevalence of subclinical and overt hypothyroidism were detected; 23.1% and 7%; respectively. This might be due to a small sample that did not represent the real prevalence in the Syrian population. Also this sample comprised of a high number of females (88.9%), which showed more common thyroid abnormalities in previous studies.[18–21] Moreover, this sample was conducted among out- and in-patient departments, which resulted in high prevalence of SCH and overt hypothyroidism.
It is well known that thyroid dysfunction has a great impact on lipids and several studies have been conducted and proved this association. The dyslipidemia is mainly caused by a shift to increased synthesis rate, which cause increased total Chol and LDL levels in patients with overt hypothyroidism.[19,21–23] Also, the decreased LDL-receptors’ activity resulting in decreased catabolism of LDL.[24,25] Moreover, this population may also present with elevated TG and VLDL levels due to decrease the activity of lipoprotein lipase that found in overt hypothyroidism.[14,20,26] A large Korean study, that involved more than 66,000 subjects, showed an increased in serum Chol, and LDL in overt hypothyroidism compared to normal group.[21] Another study of 5154 subjects from Iran showed a higher serum levels of total Chol, LDL and TG in overt hypothyroidism in comparison to SCH and normal group.[14]
In our study, there was a significant difference of lipid profile (LDL, TG, and Chol) between study groups (euthyroidism, SCH, and overt hypothyroidism). Similar to previous studies, overt hypothyroidism had significant differences in LDL, TG, and Chol compared to euthyroidism. Also, the highest levels of Chol, TG, and LDL were observed in overt hypothyroidism. Levels of these parameters were tended to increase as the thyroid dysfunction increase, where the lowest levels in euthyroidism and increased subsequently in SCH followed by overt hypothyroidism (Tables 2 and 3).
On the other hand, this relation between TSH and lipids were less prominent in SCH compared to general population or overt hypothyroidism. There is some controversy regarding the presence or the severity of SCH-induced dyslipidemia. Indeed, there have been studies indicating no significant difference in lipid profile between SCH patients and controls.[26–28] Data from the NHANES III revealed increased total Chol levels in SCH patients versus controls. However, when adjusted for age, race, sex and the use of lipid-lowering drugs no difference was observed.[29] Also, among the previous mentioned Korean study, a total Chol and LDL were significantly higher in SCH than normal population.[21] A meta-analysis of sixteen observational studies, including 41 931 adults from 1990 to 2014, suggested that the serum total Chol, LDL, and TG levels were significantly increased in patients with SCH compared with euthyroid individuals.[30] Another study did not find differences in serum levels of total Chol, LDL, and TG between SCH group and controls.[14]
In this study, no significant difference of lipid parameters (LDL, TG, and Chol) was observed between SCH compared to euthyroidism (Table 3), however, LDL and Chol showed significant differences between SCH and overt hypothyroidism. With respect to serum HDL concentrations, previous results were more complicated, since high, normal, or low values have been reported in different series.[31,32] Our study did not show significant differences in HDL levels between study groups and there was no correlation between HDL and TSH (Table 2 and 4), however, a higher level of HDL was observed in euthyroid group compared to decreasing levels in SCH and overt hypothyroidism. This corresponding with a meta-analysis included a total 40,516 participants, where no significant difference was observed for serum HDL. Three of reported studies showed significant lower HDL levels in SCH patients and 1 reported significant higher level compared with euthyroid participants. The overall serum HDL level in SCH patients was lower than in euthyroid participants, but was not statistically significant.[30]
On a cross-sectional study of 20 783 subjects, TSH, even within the normal range; was positively correlated with total Chol, TG, and LDL levels. This study suggested a cutoff level of TSH (2.57 mU/L) for detecting significant differences in circulating lipid levels. These results were remained significant after adjusted by age, gender, BMI, and smoking status.[23] Another study found no significant correlations between serum TSH levels and total Chol, LDL, HDL, and TG. Also, this study found no correlations between TSH and lipid profiles in individuals with SCH, but there was a weak negative correlation between serum concentrations of FT4 and LDL, TG, total Chol and HDL.[14]
In our study, a weak and significant correlation between levels of TSH and FT4 with lipid profile was observed. TSH was positively correlated with lipid profile (LDL, TG, and Chol), however, HDL did not show a significant correlation. FT4 also showed a weak and significant negative correlation with all lipid profile (LDL, TG, and Chol) except a positive correlation with HDL.
Limitations of the presented study were a small sample size, mostly females, and patients referred to single center, which resulted in high prevalence of thyroid abnormalities. Despite the previous limits, this study reports significant results of lipids abnormalities in the context of thyroid disorders.
5. Conclusion
Overall, our findings suggest a higher level of lipids (LDL, TG, and Chol) among SCH and overt hypothyroidism compared to general population. A weak correlations of lipid parameters with TSH and FT4 were detected. It is not well evident whether a restoration of euthyroidism might influence the morbidity and mortality, especially cardiovascular comorbidities, in this population, which mandates future studies.
Acknowledgment
The authors thank Dr. Lelian Haj Hasan for valuable contribution in data collection.
Author contributions
Conceptualization: Fatima Tarboush.
Data curation: Fatima Tarboush.
Formal analysis: Mohammad Alsultan.
Methodology: Fatima Tarboush.
Supervision: Zaynab Alourfi.
Visualization: Zaynab Alourfi.
Writing – original draft: Fatima Tarboush, Mohammad Alsultan.
Writing – review & editing: Fatima Tarboush, Mohammad Alsultan, Zaynab Alourfi.
Abbreviations:
- BMI
- body mass index
- Chol
- cholesterol
- FT4
- free thyroxine
- HDL
- high density lipoprotein
- LDL
- low density lipoprotein
- SCH
- subclinical hypothyroidism
- TG
- triglycerides
- TSH
- thyroid stimulating hormone
The authors have no funding and conflicts of interest to disclose.
All data generated or analyzed during this study are included in this published article [and its supplementary information files].
The study was approved in accordance with the Declaration of Helsinki and in line with the STROBE criteria.
How to cite this article: Tarboush F, Alsultan M, Alourfi Z. The correlation of lipid profile with subclinical and overt hypothyroidism: A cross-sectional study from Syria. Medicine 2023;102:37(e34959).
Contributor Information
Fatima Tarboush, Email: dr.fatima.tarboush@hotmail.com.
Zaynab Alourfi, Email: zaynabarfi@hotmail.com.
References
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