ABSTRACT
Background:
Poor sleep quality is observed in patients of hypothyroidism. The patient complains of sleeplessness, excessive day-time sleepiness, snoring, arousals and breathlessness. The decrease in quantity and quality of sleep occurs in various degrees of severity in patients of hypothyroidism.
Objectives:
To evaluate sleep quality and quantitative variables in patients of clinical and subclinical hypothyroidism.
Materials and Methods:
This community-based cross-sectional study was conducted in 30 diagnosed cases of untreated subclinical and clinical hypothyroidism in the ages between 30 and 50; the serum levels of TSH, tT3, tT4 were evaluated by Chemiluminescent Immunoassay (CLIA) method. Participants were asked to fill an Epworth Sleepiness Scale (ESS) questionnaire to assess the quality of sleep. The Polysomnography was conducted using a “Polysomnography System for Sleep Studies (Make SOMNO medics, Germany).” The variables evaluated from PSG report included total sleep time, sleep efficiency, sleep stage percentage, sleep onset latency, arousal index, apnea–hypopnea index (AHI), oxygen desaturation index, and snoring scores. The data were analyzed using statistical software SPSS-23.0. The comparison among the group was carried using unpaired “t” test. The P values <0.05 were considered statistically significant.
Results:
The data analysis showed decreased sleep efficiency (68.93 ± 13.96) and decreased sleep onset latency (6.32 ± 8.87), increased N1 duration- 21.01 ± 16.69 minutes (normal: 5-10%), decreased N3- 8.56 ± 11.21 minutes (normal: 15-25%), REM duration- 12.46 ± 10.07 minutes (normal: 20-25%), and Epworth Sleepiness Scale values were found to be significantly higher in patients of clinical hypothyroidism as compared to patients of subclinical hypothyroidism. AHI (18.74 ± 13.2) (normal: <5) and ODI values (14.16 ± 176.6) are increased in patients of hypothyroidism. AHI was found to be significantly higher in patients of clinical hypothyroidism (23.64 ± 14.58) compared to patients of subclinical hypothyroidism (18.96 ± 20.49). Arousal index (77.5 ± 12.07) and snoring index (82.09 ± 132.34) are found to be elevated in patients of hypothyroidism. Snoring index is found to be significantly higher in patients of clinical hypothyroidism (183.96 ± 163.57) as compared to patients of subclinical hypothyroidism (82.09 ± 132.34).
Conclusions:
Obstruction Sleep Apnea (OSA) is an under-diagnosed complication of hypothyroidism. Patients with risk factors, complaining of loud snoring and excessive day-time sleepiness should be evaluated for Obstruction Sleep Apnea (OSA). This greatly helps in improving their quality of life.
Keywords: Hypothyroidism, obstruction sleep apnea, polysomnography, subclinical thyroidism
Introduction
Poor sleep quality has been observed in patients of hypothyroidism. These patients exhibit complains of sleeplessness, excessive day-time sleepiness, snoring, arousals, and history of breathlessness. The decrease in quantity and quality of sleep occurs in various degrees of severity.[1,2] Subclinical hypothyroidism (SCH), also called mild thyroid failure, is diagnosed when peripheral thyroid hormone levels are within normal reference laboratory range but serum thyroid-stimulating hormone (TSH) levels are mildly elevated. There are the elevated ranges of TSH (usually 4.5-10.0 mlU/L) with normal free T4.[3] The definition of hypothyroidism is based on statistical reference ranges of the relevant biochemical parameters. Clinical manifestations of hypothyroidism range from life threatening to no signs or symptoms. The most common symptoms in adults are fatigue, lethargy, cold intolerance, weight gain, constipation, change in voice, and dry skin, but clinical presentation can differ with age and sex, among other factors. In clinical hypothyroidism, the TSH rises above 10 mU/l, and T3 and T4 levels are reduced from normal levels.[4]
There is a high incidence of sleep apnea in patients with untreated hypothyroidism. Thyroxine treatment is said to significantly reduce the apnea index and length and sleep apnea symptoms.[5]
The various research studies have shown increased prevalence of sleep abnormalities in hypothyroid population. Hypothyroidism is found to be associated with obstructive sleep apnea syndrome (OSAS), Restless Leg syndrome (RLS), and insomnia.[2] On the other hand, healthy sleep reflects a healthy metabolism state of body. This enhances quality of life and its longetivity, and it improves concentration, memory, information processing, enhances immunity, and also aids in regulating our appetite. Sleep quality is also affected in subclinical hypothyroid patients.[2,6,7] Poor sleep quality increases the risk of heart diseases, diabetes mellitus, obesity, and autoimmune diseases. The sleep quality and level of thyroid hormones seem to have an interdependent relationship.[8,9] But the data regarding the sleep architecture in patients of hypothyroidism and subclinical hypothyroidism are lacking in literature in southern Indian setup. Hence, this study is being conducted to report PSG recordings in hypothyroid population and their correlation with T3, T4, TSH levels, if any. Polysomnography (PSG) provides a comprehensive view of the sleep architecture and is now the gold standard for sleep assessment. PSG has the benefit of being able to differentiate between sleep and resting wakefulness as well as offering a thorough measurement of several sleep indices. We planned to assess the quality of sleep through various parameters total sleep time, distribution of sleep in different stages, time taken to fall asleep (sleep latency), sleep efficiency, number of arousals per hour of sleep (arousal index), number of desaturation episodes per hour, number of apneas and hypopnea as per hour of sleep (apnea–hypopnea index), and number of snoring episodes per hour of sleep (snoring index).
Objective
To evaluate sleep quality and quantitative variables in patients of clinical hypothyroidism and subclinical hypothyroidism.
Methodology
The study was conducted in Polysomnography lab of Department of Physiology. The study was approved by the Institutional ethics committee. Thirty patients with a mean age of 40.36 ± 6.171 were recruited through simple random sampling from our hospital setup.
Type of study: Cross-sectional study.
Participants
Inclusion criteria
Diagnosed with untreated subclinical and clinical hypothyroidism
Signed consent forms
Between the ages 30 and 50 years.
Exclusion criteria
Patients with a diagnosis of malignancy, chronic kidney disease, heart and liver failure
Pregnant and lactating women
Psychiatric and epileptic patients.
Patients on any medication affecting sleep and thyroid function (glucocorticoids, dopamine, propranolol, phenytoin, carbamazepine, salicylate, furosemide, lithium, amiodarone, interferon alpha, antihistamines, benzodiazepines, z group drugs).
Each participant had two visits. In the first visit/screening visit, the participant’s demographic details were taken which included name, age, sex, address, education, occupation. Participants were asked to come after fasting overnight, and a blood sample was taken from antecubital vein following aseptic precautions. The samples were taken at the same time everyday (between 8:30 am and 9:30 am). Guidelines for blood storage and infection control were followed. Prior to analysis, serum was separated and kept at 2-8°C. Shortly after, serum levels of TSH, T3, T4 were evaluated by Chemiluminescent Immunoassay (CLIA) method.[9,10] The reference ranges used in the hospital are total T3 (2.5-5.3 pg/mL), total T4 (normal range 0.61-1.12 ng/dL), TSH (normal range 0.38-5.33 IU/mL).[11,12] Participants were asked to fill an ESS questionnaire. The Epworth Sleepiness Scale (ESS) is a self-reported self-assessment scale that asks the respondent to rate how likely they are to fall asleep in a range of situations like reading, watching TV, after lunch or at work. The ESS uses a 4-point scale to rank the likelihood of falling asleep on a scale of 0 (no chance of dozing) to 3 (high chance of dozing). It has been extensively used by researchers studying sleep.[13] The participants were asked to refrain from caffeinated products during the study and scheduled for the next visit. On the second visit, participants arrived at the sleep lab at 20:30. Their anthropometric measures—height and weight, were taken, and BMI was calculated. Eight EEG electrodes were placed (2 frontal, 2 central, 2 occipital, 1 reference, and 1 ground electrode). Two ECG electrodes were placed on the chest. Three EMG electrodes were placed on the chin. The participants were usually in bed by 21:30 and were awakened by 5:30. A standard overnight multichannel Polysomnographic evaluation was carried out in the sleep laboratory in the Department of Physiology. The Polysomnography was conducted using a “Polysomnography System for Sleep Studies (Make SOMNOmedics, Germany).”[14,15] It includes measurements of heart rate via ECG, eight channels of EEG, chin electromyogram (EMG), bilateral electrooculogram (EOG), oxygen saturation via oximeter, air flow, snoring through microphone place near trachea. Sleep staging was done through DOMINO software.
The following variables are considered from the PSG report:
Total Sleep Time
Sleep efficiency
Sleep stage percentage
Sleep onset latency
Arousal index (Number of arousals per hour of sleep)
Apnea–hypopnea index (Number of apnea and hyperpnea episodes per hour of sleep)
Oxygen desaturation index (Number of desaturation episodes per hour of sleep)
Snoring index (Number of snoring episodes per hour of sleep).
Statistical analysis
The data analysis was done by using statistical software SPSS-23.0. The mean and standard deviation were calculated for quantitative variables, while percentage was reported for qualitative variables. Mean comparison was done by dependent t test and independent t test. P value <0.05 was considered as significant.
Results
A total of 30 subjects with diagnosed subclinical and clinical hypothyroidism were included in the study, out of which n = 13 (43.33%) were subclinically hypothyroid and n = 17 (56.67%) were clinically hypothyroid. The mean age of the subclinically hypothyroid participants was 38.36 ± 4.829, and clinically hypothyroid was 42.23 ± 6.79. The other demographic statistics are described in Table 1. The distribution of study subjects percentage-wise based on BMI is depicted in Figure 1.
Table 1.
Demographic characteristics of participants
| Characteristics | Mean+SD of all study subjects (n=30) | Mean+SD of subclinical hypothyroid participants (n=13) | Mean+SD of clinically hypothyroid participants (n=17) |
|---|---|---|---|
| Age (yr) | 40.36±6.171 | 38.36±4.829 | 42.23±6.79 |
| Height (cm) | 158.08±7.636 | 157.18±9.06 | 157.92±5.56 |
| Weight (kg) | 65.68±13.457 | 66.72±14.64 | 64.9±12.85 |
| BMI (kg/m2) | 26.17±4.54 | 26.61±4.49 | 25.96±4.695 |
Figure 1.
Distribution of study subjects percentage wise based on BMI
The sleep architecture of study population and comparative data of sleep architecture are detailed in Tables 2 and 3. The values depicting the sleep architecture including Total sleep time (TST), Sleep Efficiency (SE), Sleep Onset Latency, % of N1, N2, N3, REM are expressed as mean ± SD in Tables 1, 3. Epworth Sleepiness Scale values are also included. The data analysis showed decreased sleep efficiency (68.93 ± 13.96) and decreased sleep onset latency (6.32 ± 8.87) compared to normal values taken from the literature (SE: 85% and SOL: 10-20 min). A disturbed sleep architecture was noticed with increased N1 duration- 21.01 ± 16.69 minutes (normal: 5-10%) and decreased N3- 8.56 ± 11.21 minutes (normal: 15-25%), REM duration- 12.46 ± 10.07 minutes (normal: 20-25%). Epworth Sleepiness Scale values were found to be significantly higher in patients of clinical hypothyroidism compared to patients of subclinical hypothyroidism.
Table 2.
Sleep architecture of the study population
| Variables | Full sample (n=30) | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) |
|---|---|---|---|
| TST (min) | 330.44±67.01 | 341.36±49.44 | 314.84±75.4 |
| SE (%) | 68.93±13.96 | 71.2±10.31 | 65.68±15.7 |
| SOL (min) | 6.32±8.87 | 5.87±5.29 | 6.61±11.29 |
| % REM | 12.46±10.07 | 12.99±8.42 | 12.01±11.59 |
| N1 (min) | 21.01±16.69 | 18.75±18.19 | 23.28±15.64 |
| N2 (min) | 57.9±14.06 | 60.85±14.36 | 55.36±13.85 |
| N3 (min) | 8.56±11.21 | 7.23±13.87 | 9.35±8.67 |
| ESS Score | 7.6±4.06 | 4.09±0.89 | 10.69±3.31 |
TST: Total sleep time; SE: Sleep Efficiency; SOL: Sleep onset latency; ESS: Epworth Sleepiness Scale
Table 3.
Sleep architecture of the study population compared between subclinical and clinical hypothyroid patients
| Variables | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) | t | P |
|---|---|---|---|---|
| TST (min) | 341.36±49.44 | 314.84±75.4 | 1.098 | 0.2815 |
| SE (%) | 71.2±10.31 | 65.68±15.7 | 1.097 | 0.2818 |
| SOL (min) | 5.87±5.29 | 6.61±11.29 | 0.218 | 0.829 |
| % REM | 12.99±8.42 | 12.01±11.59 | 0.2570 | 0.799 |
| ESS Score | 4.09±0.89 | 10.69±3.31 | 6.972 | 0.0001* |
*Statistically significant. TST: Total sleep time; SE: Sleep Efficiency; SOL: Sleep onset latency; ESS: Epworth Sleepiness Scale
The respiratory parameter and comparative data of respiratory parameter between subclinical and clinical hypothyroid patients are detailed in Tables 4 and 5.
Table 4.
Respiratory parameters of PSG in study population
| Variables | Full sample (n=30) | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) |
|---|---|---|---|
| Apnea index | 2.49±8.91 | 0.23±0.34 | 3.76±11.89 |
| Hypopnea index | 16.24±9.33 | 12.20±8.9 | 19.89±8.52 |
| Apnea–Hypopnea index | 18.74±13.2 | 12.45±8.89 | 23.64±14.58 |
| Oxygen desaturation index | 14.16±176.6 | 9.07±8.58 | 18.96±20.49 |
| Average Spo2 | 95±2.24 | 95.63±2.30 | 94.30±2.01 |
| Lowest Spo2 | 87.28±7.49 | 87.18±7.17 | 87.15±7.98 |
Table 5.
Respiratory parameters of PSG compared between subclinical and clinical hypothyroid patients
| Variables | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) | t | P |
|---|---|---|---|---|
| Apnea index | 0.23±0.34 | 3.76±11.89 | 1.065 | 0.295 |
| Hypopnea index | 12.20±8.9 | 19.89±8.52 | 2.403 | 0.02* |
| Apnea–Hypopnea index | 12.45±8.89 | 23.64±14.58 | 2.436 | 0.02* |
| Oxygen desaturation index | 9.07±8.58 | 18.96±20.49 | 1.629 | 0.114 |
*Statistically significant
Apnea–hypopnea index (AHI) and oxygen desaturation index (ODI) values are expressed as mean ± SD values in Tables 1, 5. AHI (18.74 ± 13.2) (normal: <5) and ODI values (14.16 ± 176.6) are increased in patients of hypothyroidism. AHI was found to be significantly higher in patients of clinical hypothyroidism (23.64 ± 14.58) compared to patients of subclinical hypothyroidism (18.96 ± 20.49). Arousal index, snoring index, and duration of snoring are expressed as mean ± SD values in Tables 6 and 7. Arousal index (77.5 ± 12.07) and snoring index (82.09 ± 132.34) are found to be elevated in patients of hypothyroidism. Snoring index is found to be significantly higher in patients of clinical hypothyroidism (183.96 ± 163.57) compared to patients of subclinical hypothyroidism (82.09 ± 132.34) [Figure 2].
Table 6.
Other parameters of PSG in the study population
| Variables | Full sample (n=30) | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) |
|---|---|---|---|
| Arousal index | 78.94±15.35 | 77.5±12.07 | 79.27±17.84 |
| Snoring index | 136.04±155.33 | 82.09±132.34 | 183.96±163.57 |
| Duration of snoring (min) | 20.82±34.26 | 16.06±31.81 | 25.83±36.67 |
Table 7.
Other parameters of PSG compared between subclinical and clinical hypothyroid patients
| Variables | Subclinical hypothyroidism (n=13) | Clinical hypothyroidism (n=17) | t | P |
|---|---|---|---|---|
| Arousal index | 77.5±12.07 | 79.27±17.84 | 0.307 | 0.76 |
| Snoring index | 82.09±132.34 | 183.96±163.57 | 1.813 | 0.05* |
| Duration of snoring (min) | 16.06±31.81 | 25.83±36.67 | 0.764 | 0.45 |
*Statistically significant
Figure 2.
Percentage representation of grades of sleep apnea in the study population
Discussion
This study was performed to find the changes in sleep architecture and the parameters of sleep quality in patients of hypothyroidism. The total sleep time, sleep efficiency, and sleep onset latency were found to be decreased. Disturbed sleep architecture with increased N1 duration and decreased N3, REM duration was also noticed. The apnea–hypopnea index, oxygen desaturation index, snoring index, and arousal index were also found to be inflated.
The altered sleep architecture along with significant changes in respiratory parameters among subclinical thyroid patient and hypothyroid patient in our study is attributed to altered thyroid profile status as hypothyroidism is linked to many changes in lung physiology. Our study finding revealed a relevant decline in apnea–hypopnea index (AHI), oxygen desaturation index (ODI), arousal, and snoring index both in patients of hypothyroidism and subclinical thyroid disorders. All our findings reflected decrement sleep efficiency and sleep quality with significant changes in apnea–hypopnea index and snoring index in patients of hypothyroidism as compared to subclinical thyroid patients. It is known to manifest as slightly lowered forced vital capacity and reduced forced expired flow.[15,16,17] The patients often complain of insomnia and day-time sleepiness. According to reports, choking, snoring, and in extreme cases, respiratory pauses or hypopnea episodes are among the breathing irregularities that might occur throughout the night for 25% to 35% of hypothyroid individuals.[12,15,16,17,18] In addition to the above fact hypothyroidism being a direct causative agent for Obstructive Sleep Apnea (OSA), impaired function of the thyroid gland can also indirectly cause OSA through cardiovascular and neuromuscular problems.[18,19] The high prevalence of sleep apnea in hypothyroid individuals, especially in uncommon myxedematous instances, suggests a connection between hypothyroidism and OSAS.[14,15,19] Although hypothyroidism per se has not been linked to the increased prevalence of OSAS; it does appear to be related to male sex and obesity. Potential contributing factors to OSA in hypothyroidism include hypothyroid myopathy, extravasation of albumin and mucopolysaccharides in upper airway tissues, and decreased ventilatory responses.[18,19]
Moreover, significant changes in apnea–hypopnea index and snoring index in patients of hypothyroidism as compared to subclinical thyroid patients can be attributed to recurrent episodes of cessation or decrement in respiratory flow due to upper airway collapse during sleep with a consequent decrease in oxygen saturation. The development of these respiratory changes and sleep apnea is largely influenced by skeletal or soft tissue abnormalities, such as tonsillar hypertrophy, constricted nasal cavities, and soft tissue swelling in obese individuals appears to be the predominant contributing factor. The restricted passage of air through the respiratory tract leads to hypoxia and hypercapnia.[12,15,18,19] Lowered ventilatory drive and muscle weakness add to the apnea and hypopnea.[15,19] This leads to frequent arousals during night and consequent day-time sleepiness. Partial obstruction of airway may cause snoring as observed in our subjects.
Conclusion
Obstruction Sleep Apnea (OSA) is an under-diagnosed complication of hypothyroidism. Patients with risk factors, complaining of loud snoring and excessive day-time sleepiness, should be evaluated for OSA. This greatly helps in improving their quality of life.
Author contribution
All authors made a significant contribution to the work reported, in the conception, study design, execution, acquisition of data, analysis, and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
References
- 1.Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001;81:1097–42. doi: 10.1152/physrev.2001.81.3.1097. [DOI] [PubMed] [Google Scholar]
- 2.Song L, Lei J, Jiang K, Lei Y, Tang Y, Zhu J, et al. The Association between subclinical hypothyroidism and sleep quality: A population-based study. Risk Manag Healthc Policy. 2019;12:369–74. doi: 10.2147/RMHP.S234552. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Fatourechi V. Subclinical hypothyroidism: An update for primary care physicians. Mayo Clin Proc. 2009;84:65–71. doi: 10.4065/84.1.65. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Chaker L, Bianco AC, Jonklaas J, Peeters RP. Hypothyroidism. Lancet. 2017;390:1550–62. doi: 10.1016/S0140-6736(17)30703-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Grunstein RR, Sullivan CE. Sleep apnea and hypothyroidism: Mechanisms and management. Am J Med. 1988;85:775–9. doi: 10.1016/s0002-9343(88)80020-2. [DOI] [PubMed] [Google Scholar]
- 6.Kim W, Lee J, Ha J, Jo K, Lim DJ, Lee JM, et al. Association between sleep duration and subclinical thyroid dysfunction based on nationally representative data. J Clin Med. 2019;8:2010. doi: 10.3390/jcm8112010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Teliti M, Fanfulla F, Croce L, Coperchini F, Rotondi M. The interplay between subclinical hypothyroidism and poor sleep quality: A systematic review. Eur J Intern Med. 2024;126:49–55. doi: 10.1016/j.ejim.2024.03.013. [DOI] [PubMed] [Google Scholar]
- 8.Akatsu H, Ewing SK, Stefanick ML, Fink HA, Stone KL, Barrett-Connor E, et al. Association between thyroid function and objective and subjective sleep quality in older men: The osteoporotic fractures in men (MrOS) study. Endocr Pract. 2014;20:576–86. doi: 10.4158/EP13282.OR. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med. 1993;328:1230–5. doi: 10.1056/NEJM199304293281704. [DOI] [PubMed] [Google Scholar]
- 10.Thavaraputta S, Dennis JA, Laoveeravat P, Nugent K, Rivas AM. Hypothyroidism and its association with sleep apnea among adults in the United States: NHANES 2007-2008. J Clin Endocrinol Metab. 2019;104:4990–7. doi: 10.1210/jc.2019-01132. [DOI] [PubMed] [Google Scholar]
- 11.Resta O, Pannacciulli N, Di Gioia G, Stefàno A, Barbaro MP, De Pergola G. High prevalence of previously unknown subclinical hypothyroidism in obese patients referred to a sleep clinic for sleep disordered breathing. Nutr Metab Cardiovasc Dis. 2004;14:248–53. doi: 10.1016/s0939-4753(04)80051-6. [DOI] [PubMed] [Google Scholar]
- 12.Kittle WM, Chaudhary BA. Sleep apnea and hypothyroidism. South Med J. 1988;81:1421–5. doi: 10.1097/00007611-198811000-00020. [DOI] [PubMed] [Google Scholar]
- 13.Wang L, Fang X, Xu C, Pan N, Wang Y, Xue T, et al. Epworth sleepiness scale is associated with hypothyroidism in male patients with obstructive sleep apnea. Front Endocrinol (Lausanne) 2022;13:1010646. doi: 10.3389/fendo.2022.1010646. doi:10.3389/fendo.2022.1010646. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Medical Advisory Secretariat. Polysomnography in patients with obstructive sleep apnea: An evidence-based analysis. Ont Health Technol Assess Ser. 2006;6:1–38. [PMC free article] [PubMed] [Google Scholar]
- 15.Kumar P, Rai DK, Kanwar MS. Comparison of clinical and polysomnographic parameters between obese and nonobese obstructive sleep apnea. J Family Med Prim Care. 2020;9:4170–3. doi: 10.4103/jfmpc.jfmpc_56_20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Shah F, Stål P. Myopathy of the upper airway in snoring and obstructive sleep apnea. Laryngoscope Investig Otolaryngol. 2022;7:636–45. doi: 10.1002/lio2.782. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Sadek SH, Khalifa WA, Azoz AM. Pulmonary consequences of hypothyroidism. Ann Thorac Med. 2017;12:204–8. doi: 10.4103/atm.ATM_364_16. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Salome CM, King GG, Berend N. Physiology of obesity and effects on lung function. J Appl Physiol. 2010;108:206–11. doi: 10.1152/japplphysiol.00694.2009. [DOI] [PubMed] [Google Scholar]
- 19.Iyer SK, Menon SK, Bahuleyan B. An analysis of dynamic pulmonary functions of hypothyroid patients. J Clin Diagn Res. 2017;11:CC10–2. doi: 10.7860/JCDR/2017/24653.9579. [DOI] [PMC free article] [PubMed] [Google Scholar]