Advertisement

Exercise training–induced changes in metabolic syndrome parameters, carotid wall thickness, and thyroid function in middle-aged women with subclinical hypothyroidism

  • Nayoung Ahn
  • Hye Soon Kim
  • Kijin KimEmail author
Original Article

Abstract

This study analyzed the differences in effects of a 12-week combination of exercise training program with resistance training and aerobic exercises on the risk factors of metabolic syndrome, carotid wall thickness, and thyroid function, between subclinical hypothyroidism patients and obese groups, in middle-aged women. Subjects consisted of either 20 middle-aged women in the subclinical hypothyroidism (SCH) group or 20 obese (body mass indices [BMI], ≥ 25 kg/m2) women without hypothyroidism in the obese (OB) group. The body composition, blood lipid factors, hormones associated with thyroid functions, blood pressure (BP), and carotid intima-media thickness were measured, while physical fitness was ascertained. In the SCH group, waist circumference (WC) and high-density lipoprotein cholesterol values were outside the normal ranges, while WC and systolic BP (SBP) were outside the normal ranges in the OB group. Following the 12-week training program, significantly positive changes occurred in body fat percentage, sit and reach test results, and SBP (p < 0.05) in the SCH group, while in the OB group, significantly positive changes in BMI, WC, sit and reach test results, SBP, and diastolic BP (DBP, p < 0.05) were observed. In addition, both groups showed significant decreases in intima-media thickness of the right carotid bifurcation (p < 0.05). However, in the two groups, the 12-week exercise training program did not have similar significant impact on the hormones related to thyroid functions and blood lipids. Therefore, further research on exercise training that can effectively induce changes in the hormones associated with thyroid functions in patients with subclinical hypothyroidism is necessary.

Keywords

Subclinical hypothyroidism Obesity Exercise training Middle-aged women 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The research protocol was approved by the Institutional Review Boards of Keimyung University College of Medicine and Keimyung University Dongsan Medical Center (approval number: 10-184-01.06).

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Alamdari S, Amouzegar A, Tohidi M, Gharibzadeh S, Kheirkhah P, Kheirkhah P, Azizi F (2015) Hypothyroidism and lipid levels in a community based study (TTS). Int J Endocrinol Metab 14:e22827.  https://doi.org/10.5812/ijem.22827
  2. 2.
    Almas SP, Werneck FZ, Coelho EF, Teixeira PF, Vaisman M (2017) Heart rate kinetics during exercise in patients with subclinical hypothyroidism. J Appl Physiol (1985) 122:893–898.  https://doi.org/10.1152/japplphysiol.00094.2016
  3. 3.
    Amati F, Dube JJ, Stefanovic-Racic M, Toledo FG, Goodpaster BH (2009) Improvements in insulin sensitivity are blunted by subclinical hypothyroidism. Med Sci Sports Exerc 41(2):265–269.  https://doi.org/10.1249/MSS.0b013e318187c010 CrossRefGoogle Scholar
  4. 4.
    Baset JHD, Williams GR (2016) Role of thyroid hormones in skeletal development and bone maintenance. Endocr Rev 37(2):135–187CrossRefGoogle Scholar
  5. 5.
    Baylor LS, Hackney AC (2003) Resting thyroid and leptin hormone changes in women following intense, prolonged exercise training. Eur J Appl Physiol 88:480–484CrossRefGoogle Scholar
  6. 6.
    Beck BR, Daly RM, Singh MA, Taaffe DR (2017) Exercise and Sports Science Australia (ESSA) position statement on exercise prescription for the prevention and management of osteoporosis. J Sci Med Sport 20:438–445CrossRefGoogle Scholar
  7. 7.
    Brennan MD, Powell C, Kaufman KR, Sun PC, Bahn RS, Nair KS (2006) The impact of overt and subclinical hyperthyroidism on skeletal muscle. Thyroid 16:375–380CrossRefGoogle Scholar
  8. 8.
    Butcher SK, Killampalli V, Lascelles D, Wang K, Alpar EK, Lord JM (2005) Raised cortisol:DHEAS ratios in the elderly after injury: potential impact upon neutrophil function and immunity. Aging Cell 4:319–324CrossRefGoogle Scholar
  9. 9.
    Chahal HS, Drake WM (2007) The endocrine system and ageing. J Pathol 211:173–180CrossRefGoogle Scholar
  10. 10.
    Cheserek MJ, Wu G, Shen L, Shi Y, Le G (2014) Evaluation of the relationship between subclinical hypothyroidism and metabolic syndrome components among workers. Int J Occup Med Environ Health 27:175–187.  https://doi.org/10.2478/s13382-014-0240-5
  11. 11.
    Cikim AS, Oflaz H, Ozbey N, Cikim K, Umman S, Meric M, Sencer E, Molvalilar S (2004) Evaluation of endothelial function in subclinical hypothyroidism and subclinical hyperthyroidism. Thyroid 14:605–609.  https://doi.org/10.1089/1050725041692891 CrossRefGoogle Scholar
  12. 12.
    Ciloglu F, Peker I, Pehlivan A, Karacabey K, Ī rac N, Saygin O, Ozmerdivenli R (2005) Exercise intensity and its effects on thyroid hormones. Neuroendocrinol Lett 26:830–834Google Scholar
  13. 13.
    Collomp K, Buisson C, Lasne F, Collomp R (2015) DHEA, physical exercise and doping. J Steroid Biochem Mol Biol 145:206–212CrossRefGoogle Scholar
  14. 14.
    Cooper DS, Biondi B (2012) Subclinical thyroid disease. Lancet 24(379):1142–1154CrossRefGoogle Scholar
  15. 15.
    Dahl AR, Iqbal AM, Lteif AN, Pittock ST, Tebben PJ, Kumar S (2018) Mild subclinical hypothyroidism is associated with paediatric dyslipidaemia. Clin Endocrinol 89:330–335.  https://doi.org/10.1111/cen.13752 CrossRefGoogle Scholar
  16. 16.
    Delitala AP, Filigheddu F, Orrù M, AlGhatrif M, Steri Pilia MG, Scuteri A, Lobina M, Piras MG, Delitala G, Lakatta EG, Schlessinger D, Cuccac F (2015) No evidence of association between subclinical thyroid disorders and common carotid intima medial thickness or atherosclerotic plaque. Nutr Metab Cardiovasc Dis 25:1104–1110.  https://doi.org/10.1016/j.numecd.2015.09.001 CrossRefGoogle Scholar
  17. 17.
    Duntas LH (2002) Thyroid disease and lipids. Thyroid 12:287–293CrossRefGoogle Scholar
  18. 18.
    Eckel RH, Grundy SM, Zimmet PZ (2005) The metabolic syndrome. Lancet 365:1415–1428CrossRefGoogle Scholar
  19. 19.
    Evason MD, Carr AP, Taylor SM, Waldner CL (2004) Alterations in thyroid hormone concentrations in healthy sled dogs before and after athletic conditioning. Am J Vet Res 65:333–337CrossRefGoogle Scholar
  20. 20.
    Fisher DA (1996) Physiological variations in thyroid hormones: physiological and pathophysiological considerations. Clin Chem 42:135–139Google Scholar
  21. 21.
    Fommei E, Iervasi G (2002) The role of thyroid hormone in blood pressure homeostasis: evidence from short-term hypothyroidism in humans. J Clin Endocrinol Metab 87:1996–2000CrossRefGoogle Scholar
  22. 22.
    Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502Google Scholar
  23. 23.
    Garces-Arteaga A, Nieto-Garcia N, Suarez-Sanchez F, Triana-Reina HR, Ramírez-Vélez R (2013) Influence of a medium-impact exercise program on health-related quality of life and cardiorespiratory fitness in females with subclinical hypothyroidism: an open-label pilot study. J Thyroid Res 2013(592801):1–5.  https://doi.org/10.1155/2013/592801 CrossRefGoogle Scholar
  24. 24.
    Gulseren S, Gulseren L, Hekimsoy Z, Cetinay P, Ozen C, Tokatlioglu B (2006) Depression, anxiety, health-related quality of life, and disability in patients with overt and subclinical thyroid dysfunction. Arch Med Res 37(1):133–139CrossRefGoogle Scholar
  25. 25.
    Gutch M, Rungta S, Kumar S, Agarwal A, Bhattacharya A, Razi SM (2017) Thyroid functions and serum lipid profile in metabolic syndrome. Biom J 40:147–153.  https://doi.org/10.1016/j.bj.2016.12.006 Google Scholar
  26. 26.
    Harada PHN, Buring JE, Cook NR, Cobble ME, Kulkarni KR, Mora S (2017) Impact of subclinical hypothyroidism on cardiometabolic biomarkers in women. J Endocr Soc 1:113–123.  https://doi.org/10.1210/js.2016-1085 Google Scholar
  27. 27.
    Heaney JLJ, Carroll D, Phillips AC (2013) DHEA, DHEA-S and cortisol responses to acute exercise in older adults in relation to exercise training status and sex. Age 35:395–405CrossRefGoogle Scholar
  28. 28.
    Hollander M, Hak AE, Koudstaal PJ, Bots ML, Grobbee DE, Hofman A, Witteman JCM, Breteler MMB (2003) Comparison between measures of atherosclerosis and risk of stroke: the Rotterdam study. Stroke 34:2367–2372CrossRefGoogle Scholar
  29. 29.
    Jackson AS, Pollock ML, Ward A (1980) Generalized equations for predicting body density of women. Med Sci Sports Exerc 12:15–81Google Scholar
  30. 30.
    Jayasingh IA, Puthuran P (2016) Subclinical hypothyroidism and the risk of hypercholesterolemia. J Family Med Prim Care 5:809–816.  https://doi.org/10.4103/2249-4863.201177 CrossRefGoogle Scholar
  31. 31.
    Jin HY (2018) Prevalence of subclinical hypothyroidism in obese children or adolescents and association between thyroid hormone and the components of metabolic syndrome. J Paediatr Child Health 54:975–980.  https://doi.org/10.1111/jpc.13926 CrossRefGoogle Scholar
  32. 32.
    Jung KY, Ahn HY, Han SK, Park YJ, Cho BY, Moon MK (2017) Association between thyroid function and lipid profiles, apolipoproteins, and high-density lipoprotein function. J Clin Lipidol 11:1347–1353.  https://doi.org/10.1016/j.jacl.2017.08.015 CrossRefGoogle Scholar
  33. 33.
    Khan SH, Fazal N, Ijaz A, Manzoor SM, Asif N, Rafi T, Yasir M, Niazi NK (2017) Insulin resistance and glucose levels in subjects with subclinical hypothyroidism. J Coll Physicians Surg Pak 27:329–333 https://doi: 2630Google Scholar
  34. 34.
    Kim DH, Choi JS, Kim CJ, Cho CS (2007) The effects of Daeyoungjeon (DYJ) on the hypothyroidism in rats. Kor J Herbology 22:35–43Google Scholar
  35. 35.
    Kim H, Kim TH, Kim HI, Park SY, Kim YN, Kim S, Kim M, Jin S, Hur KY, Kim JH, Lee M, Min Y, Chung JH, Kang M, Kim SW (2017) Subclinical thyroid dysfunction and risk of carotid atherosclerosis. PLoS One 27;12:e0182090.  https://doi.org/10.1371/journal.pone.0182090
  36. 36.
    Kim K (2012) Effects of exercise training on thyroid function, body composition, physical fitness, and blood lipid profiles in subclinical hypothyroidism subjects. Korean J Phys Educ 51:385–394Google Scholar
  37. 37.
    Klein I, Danzi S (2007) Thyroid disease and the heart. Circulation 116:1725–1735CrossRefGoogle Scholar
  38. 38.
    Lankhaar JA, de Vries WR, Jansen JA, Zelissen PM, Backx FJ (2014) Impact of overt and subclinical hypothyroidism on exercise tolerance: a systematic review. Res Q Exerc Sport 85(3):365–389.  https://doi.org/10.1080/02701367.2014.930405 CrossRefGoogle Scholar
  39. 39.
    Laragh JH, Sealey JE (2003) Relevance of the plasma renin hormonal control system that regulates blood pressure and sodium balance for correctly treating hypertension and for evaluating ALLHAT. Am J Hypertens 16:407–415CrossRefGoogle Scholar
  40. 40.
    Lehninger AL, Nelson DL, Cox MM (2001) Principle of biochemistry, 2nd edn. Worth Publishers, New York, p 752Google Scholar
  41. 41.
    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419CrossRefGoogle Scholar
  42. 42.
    McCulloch AJ, Johnston DG, Baylis PH, Kendall-Taylor P, Clark F, Younf ET, Albert KG (1983) Evidence that thyroid hormones regulate gluconeogenesis from glycerol in man. Clin Endocrinol 19:67–76CrossRefGoogle Scholar
  43. 43.
    Moon JH, Kim HJ, Kim HM, Choi SH, Lim S, Park YJ, Jang HC, Cha BS (2013) Decreased expression of hepatic low-density lipoprotein receptor-related protein 1 in hypothyroidism: a novel mechanism of atherogenic dyslipidemia in hypothyroidism. Thyroid 23:1057–1065CrossRefGoogle Scholar
  44. 44.
    Moon MK, Lee YJ, Choi SH, Lim S, Yang EJ, Lim J, Paik N, Kim KW, Park KS, Jang HC, Cho BY, Park YJ (2010) Subclinical hypothyroidism has little influences on muscle mass or strength in elderly people. J Korean Med Sci 25(8):1176–1181.  https://doi.org/10.3346/jkms.2010.25.8.1176 CrossRefGoogle Scholar
  45. 45.
    Nagasaki T, Inaba M, Henmi Y, Kumeda Y, Tahara H, Sugiguchi S, Emoto M, Ishimura E, Onoda N, Ishikawa T, Nihizawa Y (2003) Decrease in carotid intima-media thickness in hypothyroid patients after normalization of thyroid function. Clin Endocrinol 59:607–612CrossRefGoogle Scholar
  46. 46.
    Peppa M, Koliaki C, Nikolopoulos P, Raptis SA (2010) Skeletal muscle insulin resistance in endocrine disease. J Biomed Biotechnol 2010:527850CrossRefGoogle Scholar
  47. 47.
    Rochon C, Tauveron I, Dejax C, Benoit P, Capitan P, Fabricio A, Berry C, Champredon C, Thieblot P, Grizard J (2003) Response of glucose disposal to hyperinsulinaemia in human hypothyroidism and hyperthyroidism. Clin Sci 104:7–15CrossRefGoogle Scholar
  48. 48.
    Sengupta S, Jaseem T, Ambalavanan J, Hegde A (2018) Homeostatic model assessment-insulin resistance (HOMA-IR 2) in mild subclinical hypothyroid subjects. Indian J Clin Biochem 33:214–217.  https://doi.org/10.1007/s12291-017-0647-4 CrossRefGoogle Scholar
  49. 49.
    Siri WE (1961) Body composition from fluid spaces and density: analysis of methods. Washington DC National Academy of Sciences: National Research Council pp 223–244Google Scholar
  50. 50.
    Stanickn S, Vondra K, Pelikondra T, Vlcek P, Hill M, Zamrazil V (2005) Insulin sensitivity and counter-regulatory hormones in hypothyroidism and during thyroid hormone replacement therapy. Clin Chem Lab Med 43:715–720Google Scholar
  51. 51.
    Stork S, van den Beld AW, von Schacky C, Angermann CE, Lamberts SW, Grobbee DE, Bots ML (2004) Carotid artery plaque burden, stiffness, and mortality risk in elderly men: a prospective, population-based cohort study. Circulation 110:344–348.  https://doi.org/10.1161/01.CIR.0000134966.10793.C9 CrossRefGoogle Scholar
  52. 52.
    Strasser B (2013) Physical activity in obesity and metabolic syndrome. Ann N Y Acad Sci 1281:141–159CrossRefGoogle Scholar
  53. 53.
    Sunita Mahajan AS, Jain A, Singh N, Mishra T (2013) Heart rate and blood pressure response to exercise and recovery in subclinical hypothyroid patients. Int J Appl Basic Med Res 3:106–110.  https://doi.org/10.4103/2229-516X.117076 CrossRefGoogle Scholar
  54. 54.
    Tagami T, Tamanaha T, Shimazu S, Honda K, Nanba K, Nomura H, Weda YS, Usui T, Shimatsu A, Naruse M (2010) Lipid profiles in the untreated patients with Hashimoto thyroiditis and the effects of thyroxine treatment on subclinical hypothyroidism with Hashimoto thyroiditis. Endocr J 57:253–258CrossRefGoogle Scholar
  55. 55.
    Tremblay A, Fontaine E, Poehlman ET, Mitchell D, Perron L, Bouchard C (1986) The effect of exercise-training on resting metabolic rate in lean and moderately obese individuals. Int J Obes 10:511–517Google Scholar
  56. 56.
    Tzotzas T, Krassas GE, Konstantinidis T, Bougoulia M (2000) Changes in lipoprotein (a) levels in overt and subclinical hypothyroidism hypothyroidism before and during treatment. Thyroid 10:803–808CrossRefGoogle Scholar
  57. 57.
    Udovcic M, Pena RH, Patham B, Tabatabai L, Kansara A (2017) Hypothyroidism and the heart. Methodist Debakey Cardiovasc J 13:55–59CrossRefGoogle Scholar
  58. 58.
    Uusitupa M, Louheranta A, Lindstrom J, Valle T, Sundvall J, Eriksson J (2000) The Finnish diabetes prevention study. Brit J Nutr 83:S137–SS42CrossRefGoogle Scholar
  59. 59.
    Valentina VN, Marijan B, Chedo D, Branka K (2011) Subclinical hypothyroidism and risk to carotid atherosclerosis. Arq Bras Endocrinol Metabol 55:475–480CrossRefGoogle Scholar
  60. 60.
    Vargas F, Moreno JM, Rodriguez-Gomez I, Wangensteen R, Osuna A, Alvarez-Guerra M, García-Estañ J (2006) Vascular and renal function in experimental thyroid disorders. Eur J Endocrinol 154:197–212CrossRefGoogle Scholar
  61. 61.
    Vigário Pdos S, Chachamovitz DS, Cordeiro MF, Teixeira Pde F, de Castro CL, de Oliveira FP et al (2011) Effects of physical activity on body composition and fatigue perception in patients on thyrotropin-suppressive therapy for differentiated thyroid carcinoma. Thyroid 21(7):695–700CrossRefGoogle Scholar
  62. 62.
    Volzke H, Robinson DM, Schminke U, Ludemann J, Rettig R, Felix SB, Kessler C, John U, Meng W (2004) Thyroid function and carotid wall thickness. J Clin Endocrinol Metab 89:2145–2149.  https://doi.org/10.1210/jc.2003-031028 CrossRefGoogle Scholar
  63. 63.
    Wang X, Liu H, Chen J, Huang Y, Li L, Rampersad S, Qu S (2016) Metabolic characteristics in obese patients complicated by mild thyroid hormone deficiency. Horm Metab Res 48:331–337.  https://doi.org/10.1055/s-0042-105150 CrossRefGoogle Scholar
  64. 64.
    Waring AC, Rodondi N, Harrison S, Kanaya AM, Simonsick EM, Miljkovic I, Satterfield S, Newman AB, Bauer DC, for the Health, Ageing, and Body Composition (Health ABC) Study (2012) Thyroid function and prevalent and incident metabolic syndrome in older adults: the Health, Ageing and Body Composition study. Clin Endocrinol 76:911–918CrossRefGoogle Scholar
  65. 65.
    Werneck FZ, Coelho EP, Almas SP, Garcia MM, Bonfante HLM, Lima JRP, Vigário PS, Mainenti MRM, Teixeira PF, Vaisman M (2018) Exercise training improves quality of life in women with subclinical hypothyroidism: a randomized clinical trial. Arch Endocrinol Metab 62(5):529–536CrossRefGoogle Scholar
  66. 66.
    WHO (1997) Obesity; preventing and managing the global epidemic; report of a WHO consultation on obesity. World Health Organization, Geneva, Geneva, GenevaGoogle Scholar
  67. 67.
    Wright CS, Craddock A, Weinheimer-Haus EM, Lim E, Conley TB, Janle EM, Campbell WW (2016) Thyroid status, insulin sensitivity and glucose tolerance in overweight and obese adults before and after 36 weeks of whey protein supplementation and exercise training. Endocr Res 41(2):103–109.  https://doi.org/10.3109/07435800.2015.1094083 CrossRefGoogle Scholar
  68. 68.
    Xiang GD, Pu J, Sun H, Zhao L, Yue L, Hou J (2009) Regular aerobic exercise training improves endothelium-dependent arterial dilation in patients with subclinical hypothyroidism. Eur J Endocrinol 161(5):755–761.  https://doi.org/10.1530/EJE-09-0395 CrossRefGoogle Scholar
  69. 69.
    Zhao M, Yang T, Chen L, Tang X, Guan Q, Zhang B, Zhang X, Zhang H, Wang C, Xu J, Hou X, Li Q, Yu C, Zhao Y, Fang L, Yuan Z, Xue F, Ning G, Gao L, Xu C, Zhao J (2015) Subclinical hypothyroidism might worsen the effects of aging on serum lipid profiles: a population-based case-control study. Thyroid 25:485–493.  https://doi.org/10.1089/thy.2014.0219 CrossRefGoogle Scholar
  70. 70.
    Zhu X, Cheng SY (2010) New insights into regulation of lipid metabolism by thyroid hormone. Curr Opin Endocrinol Diabetes Obes 17:408–413CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Physical Education, College of Physical EducationKeimyung UniversityDaeguSouth Korea
  2. 2.Department of Internal Medicine, School of MedicineKeimyung UniversityDaeguSouth Korea

Personalised recommendations