DOI QR코드

DOI QR Code

Poor glycemic control is associated with the risk of subclinical hypothyroidism in patients with type 2 diabetes mellitus

  • Cho, Jae Ho (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Kim, Ho Jin (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Lee, Jun Ho (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Park, Il Rae (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Moon, Jun Sung (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Yoon, Ji Sung (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Lee, In-Kyu (Department of Internal Medicine, Kyungpook National University School of Medicine) ;
  • Won, Kyu Chang (Department of Internal Medicine, Yeungnam University College of Medicine) ;
  • Lee, Hyoung Woo (Department of Internal Medicine, Yeungnam University College of Medicine)
  • Received : 2015.06.30
  • Accepted : 2015.09.07
  • Published : 2016.07.01

Abstract

Background/Aims: Overt hypothyroidism is frequently found in patients with type 2 diabetes mellitus (T2DM), but it remains unknown the relationship between subclinical hypothyroidism (SCH) and T2DM. We attempt to evaluate the difference in prevalence of SCH between patients with T2DM and general population, and the association between SCH and glycemic control status ofdiabetic patients. Methods: This was cross-sectional study. Total 8,528 subjects who visited for health check-up were recruited. SCH was defined as an elevated level of serum thyroid stimulating hormone (> 4.0 mIU/L) with a normal level of free thyroxine. T2DM group was categorized into three groups by glycosylated hemoglobin (HbA1c): < 7% (reference), ${\geq}7%$ and < 9%, ${\geq}9%$. Results: Finally, 7,966 subjects were included. The prevalence of SCH was not different between healthy controls and subjects with T2DM (8.1% vs. 7.4%, p = 0.533; in men, 5.7% vs. 5.1%, p = 0.573; in women, 10.9% vs. 11.7%, p = 0.712), but it was increased with highest HbA1c group more than well controlled group, especially in women. The risk of SCH was increased by group with poorer glycemic control; the odds ratio for HbA1c ${\geq}9%$ compared to < 7% was 2.52 (95% confidence interval [CI], 1.09 to 5.86; p = 0.031), and 4.58 (95% CI, 1.41 to 14.87; p = 0.011) in women, but not significant in men. Conclusions: The prevalence of SCH was similar between T2DM and healthy group. Poor glycemic control in T2DM was obviously associated with the risk of SCH, especially in elderly women. These results suggest SCH as comorbidity may be considered in elderly women with poor glycemic control.

Keywords

Acknowledgement

Supported by : Ministry of Health and Welfare

References

  1. Helfand M, Redfern CC. Clinical guideline, part 2. Screening for thyroid disease: an update. American College of Physicians. Ann Intern Med 1998;129:144-158. https://doi.org/10.7326/0003-4819-129-2-199807150-00020
  2. Bindels AJ, Westendorp RG, Frolich M, Seidell JC, Blokstra A, Smelt AH. The prevalence of subclinical hypothyroidism at different total plasma cholesterol levels in middle aged men and women: a need for case-finding? Clin Endocrinol (Oxf ) 1999;50:217-220. https://doi.org/10.1046/j.1365-2265.1999.00638.x
  3. Tsimihodimos V, Bairaktari E, Tzallas C, Miltiadus G, Liberopoulos E, Elisaf M. The incidence of thyroid function abnormalities in patients attending an outpatient lipid clinic. Thyroid 1999;9:365-368. https://doi.org/10.1089/thy.1999.9.365
  4. Pirich C, Mullner M, Sinzinger H. Prevalence and relevance of thyroid dysfunction in 1922 cholesterol screening participants. J Clin Epidemiol 2000;53:623-629. https://doi.org/10.1016/S0895-4356(99)00187-0
  5. Tzotzas T, Krassas GE, Konstantinidis T, Bougoulia M. Changes in lipoprotein(a) levels in overt and subclinical hypothyroidism before and during treatment. Thyroid 2000;10:803-808. https://doi.org/10.1089/thy.2000.10.803
  6. Hak AE, Pols HA, Visser TJ, Drexhage HA, Hofman A, Witteman JC. Subclinical hypothyroidism is an independent risk factor for atherosclerosis and myocardial infarction in elderly women: the Rotterdam Study. Ann Intern Med 2000;132:270-278.
  7. Canaris GJ, Manowitz NR, Mayor G, Ridgway EC. The Colorado thyroid disease prevalence study. Arch Intern Med 2000;160:526-534. https://doi.org/10.1001/archinte.160.4.526
  8. Badman MK, Chowdhury TA. Should thyroid function tests be done annually in all patients with diabetes? Diabet Med 2002;19 Suppl 3:7-9.
  9. McDermott MT, Ridgway EC. Subclinical hypothyroidism is mild thyroid failure and should be treated. J Clin Endocrinol Metab 2001;86:4585-4590. https://doi.org/10.1210/jcem.86.10.7959
  10. Cooper DS. Clinical practice: subclinical hypothyroidism. N Engl J Med 2001;345:260-265. https://doi.org/10.1056/NEJM200107263450406
  11. Hollowell JG, Staehling NW, Flanders WD, et al. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 2002;87:489-499. https://doi.org/10.1210/jcem.87.2.8182
  12. Feely J, Isles TE. Screening for thyroid dysfunction in diabetics. Br Med J 1979;1:1678. https://doi.org/10.1136/bmj.1.6179.1678
  13. Gray RS, Irvine WJ, Clarke BF. Screening for thyroid dysfunction in diabetics. Br Med J 1979;2:1439.
  14. Perros P, McCrimmon RJ, Shaw G, Frier BM. Frequency of thyroid dysfunction in diabetic patients: value of annual screening. Diabet Med 1995;12:622-627. https://doi.org/10.1111/j.1464-5491.1995.tb00553.x
  15. Smithson MJ. Screening for thyroid dysfunction in a community population of diabetic patients. Diabet Med 1998;15:148-150. https://doi.org/10.1002/(SICI)1096-9136(199802)15:2<148::AID-DIA540>3.0.CO;2-H
  16. Ishay A, Chertok-Shaham I, Lavi I, Luboshitzky R. Prevalence of subclinical hypothyroidism in women with type 2 diabetes. Med Sci Monit 2009;15:CR151-CR155.
  17. American Diabetes Association. Standards of medical care in diabetes: 2014. Diabetes Care 2014;37 Suppl 1:S14-S80. https://doi.org/10.2337/dc14-S014
  18. Palma CC, Pavesi M, Nogueira VG, et al. Prevalence of thyroid dysfunction in patients with diabetes mellitus. Diabetol Metab Syndr 2013;5:58. https://doi.org/10.1186/1758-5996-5-58
  19. Papazafiropoulou A, Sotiropoulos A, Kokolaki A, Kardara M, Stamataki P, Pappas S. Prevalence of thyroid dysfunction among Greek type 2 diabetic patients attending an outpatient clinic. J Clin Med Res 2010;2:75-78.
  20. Celani MF, Bonati ME, Stucci N. Prevalence of abnormal thyrotropin concentrations measured by a sensitive assay in patients with type 2 diabetes mellitus. Diabetes Res 1994;27:15-25.
  21. Hage M, Zantout MS, Azar ST. Thyroid disorders and diabetes mellitus. J Thyroid Res 2011;2011:439463.
  22. Gronich N, Deftereos SN, Lavi I, Persidis AS, Abernethy DR, Rennert G. Hypothyroidism is a risk factor for new-onset diabetes: a cohort study. Diabetes Care 2015;38:1657-1664. https://doi.org/10.2337/dc14-2515
  23. Sawin CT, Castelli WP, Hershman JM, McNamara P, Bacharach P. The aging thyroid: thyroid deficiency in the Framingham Study. Arch Intern Med 1985;145:1386-1388. https://doi.org/10.1001/archinte.1985.00360080056006
  24. Tuzcu A, Bahceci M, Gokalp D, Tuzun Y, Gunes K. Subclinical hypothyroidism may be associated with elevated high-sensitive c-reactive protein (low grade inflammation) and fasting hyperinsulinemia. Endocr J 2005;52:89-94. https://doi.org/10.1507/endocrj.52.89
  25. Maratou E, Hadjidakis DJ, Kollias A, et al. Studies of insulin resistance in patients with clinical and subclinical hypothyroidism. Eur J Endocrinol 2009;160:785-790. https://doi.org/10.1530/EJE-08-0797
  26. Kim BY, Kim CH, Jung CH, Mok JO, Suh KI, Kang SK. Association between subclinical hypothyroidism and severe diabetic retinopathy in Korean patients with type 2 diabetes. Endocr J 2011;58:1065-1070. https://doi.org/10.1507/endocrj.EJ11-0199
  27. El-Eshmawy MM, Abd El-Hafez HA, El Shabrawy WO, Abdel Aal IA. Response: subclinical hypothyroidism is independently associated with microalbuminuria in a cohort of prediabetic egyptian adults (Diabetes Metab J 2013;37:450-7). Diabetes Metab J 2014;38:85-86. https://doi.org/10.4093/dmj.2014.38.1.85
  28. Ashwini S, Bobby Z, Joseph M. Mild hypothyroidism improves glucose tolerance in experimental type 2 diabetes. Chem Biol Interact 2015;235:47-55. https://doi.org/10.1016/j.cbi.2015.04.007
  29. Staub JJ, Althaus BU, Engler H, et al. Spectrum of subclinical and overt hypothyroidism: effect on thyrotropin, prolactin, and thyroid reserve, and metabolic impact on peripheral target tissues. Am J Med 1992;92:631-642. https://doi.org/10.1016/0002-9343(92)90782-7
  30. Gray RS, Smith AF, Clarke BF. Hypercholesterolemia in diabetics with clinically unrecognised primary thyroid failure. Horm Metab Res 1981;13:508-510. https://doi.org/10.1055/s-2007-1019318
  31. Hueston WJ, Pearson WS. Subclinical hypothyroidism and the risk of hypercholesterolemia. Ann Fam Med 2004;2:351-355. https://doi.org/10.1370/afm.79

Cited by

  1. OBSERVATIONAL STUDY EVALUATING ASSOCIATION OF TYPE 2 DIABETES MELLITUS AND THYROID DYSFUNCTION vol.5, pp.31, 2016, https://doi.org/10.18410/jebmh/2018/473
  2. The Adverse Effects of Thyrotropin Absence on Pancreatic β Cell Function in Mice vol.2019, pp.None, 2019, https://doi.org/10.1155/2019/9536032
  3. Thyroid-stimulating hormone levels in the normal range and incident type 2 diabetes mellitus vol.56, pp.4, 2016, https://doi.org/10.1007/s00592-018-1231-y
  4. Lack of Association between Poor Glycemic Control in T2DM and Subclinical Hypothyroidism vol.2020, pp.None, 2016, https://doi.org/10.1155/2020/8121395
  5. Thyroid dysfunction and its association with microvascular complications in patients with type 2 diabetes mellitus in south India vol.14, pp.4, 2016, https://doi.org/10.1016/j.dsx.2020.05.005
  6. Thyroid Dysfunction and Dysmetabolic Syndrome: The Need for Enhanced Thyrovigilance Strategies vol.2021, pp.None, 2021, https://doi.org/10.1155/2021/9641846
  7. Prevalence and Clinical Significance of Subclinical Hypothyroidism in Diabetic Peripheral Neuropathy vol.14, pp.None, 2016, https://doi.org/10.2147/ijgm.s337779
  8. Subclinical hypothyroidism contributes to poor glycemic control in patients with type 2 diabetes mellitus, and ellagic acid attenuates methimazole‐induced abnormal glucose metabolism in mice mo vol.45, pp.6, 2016, https://doi.org/10.1111/jfbc.13753
  9. Hypothyroidism: find and neutralize vol.12, pp.None, 2016, https://doi.org/10.21518/2079-701x-2021-12-266-274