Relationship between subclinical hypothyroidism and diabetic retinopathy in type 2 diabetic patients_Chinese Journal of Ocular Fundus Diseases

Authors：

Qi Qi , Zhang Qiumei , Li Chunjun , Dong Rongna , Li Jinjin , Guo Juanjuan , Shi Jianying , Yu Demin ,  Zhang Jingyun

Key Laboratory of Hormones and Development (Ministry of Health), Tianjin Key Laboratory of Metabolic Diseases, Tianjin Metabolic Diseases Hospital & Tianjin Institute of Endocrinology, Tianjin Medical University, Tianjin 300070, China;

Corresponding author：

Zhang Jingyun, Email: zhangjingyun7903@hotmail.com

Keywords：

Diabetic retinopathy/etiology; Hypothyroidism; Diabetes mellitus, type 2/complications

DOI：

10.3760/cma.j.issn.1005-1015.2017.03.004

Video：

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Objective To investigate the relationship between subclinical hypothyroidism (SCH) and diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM). Methods A total of 792 patients of T2DM were enrolled in the study. There were 448 males and 344 females, with an average age of (54.13±13.06) years. The average duration of diabetes was (8.03±6.70) years. The patients were grouped according to the degree of DR and thyroid function. Among them, 483 patients (61.0%) were no DR, 240 patients (30.3%) were mild DR, 69 patients (8.7%) were severe DR. 725 patients (91.5%) were normal thyroid function, 67 patients (8.5%) were SCH. The prevalence of SCH among no DR group, mild DR group and severe DR group was compared. And the prevalence of DR between normal thyroid function group and SCH group was compared. Logistic regression analysis was used to estimate the association between SCH and DR. Results No significant differences among the three groups (no DR group, mild DR group, severe DR group) were found in the prevalence of SCH (χ²=1.823,P=0.402). There were no significant differences in the incidences of DR between normal thyroid function group and SCH group (χ²=1.618,P=0.239). Logistic regression analysis demonstrated that SCH was not significant associated with DR [mild DR: odds ratio (OR)=1.361, 95% confidence interval (CI)=0.773−2.399,P=0.286; severe DR:OR=1.326, 95%CI=0.520−3.384,P=0.555; DR:OR=1.353, 95%CI=0.798−2.294,P=0.261). Conclusion SCH is not significant associated with DR in patients with T2DM.

Citation： Qi Qi, Zhang Qiumei, Li Chunjun, Dong Rongna, Li Jinjin, Guo Juanjuan, Shi Jianying, Yu Demin, Zhang Jingyun. Relationship between subclinical hypothyroidism and diabetic retinopathy in type 2 diabetic patients. Chinese Journal of Ocular Fundus Diseases, 2017, 33(3): 235-239. doi: 10.3760/cma.j.issn.1005-1015.2017.03.004 Copy

1.	Schroner Z, Lazurova I, Petrovicova J. Autoimmune thyroid diseases in patients with diabetes mellitus[J]. Bratisl Lek Listy, 2008, 109(3): 125-129.
2.	Chubb SA, Davis WA, Inman Z, et al. Prevalence and progression of subclinical hypothyroidism in women with type 2 diabetes: the Fremantle Diabetes Study[J]. Clin Endocrinol, 2005, 62(4): 480-486.
3.	Radaideh AR, Nusier MK, Amari FL, et al. Thyroid dysfunction in patients with type 2 diabetes mellitus in Jordan[J]. Saudi Med J, 2004, 25(8): 1046-1050.
4.	Yang GR, Yang JK, Zhang L, et al. Association between subclinical hypothyroidism and proliferative diabetic retinopathy in type 2 diabetic patients: a case-control study[J]. Tohoku J Exp Med, 2010, 222(4): 303-310.
5.	Yang JK, Liu W, Shi J, et al. An association between subclinical hypothyroidism and sight-threatening diabetic retinopathy in type 2 diabetic patients[J]. Diabetes Care, 2010, 33(5): 1018-1020. DOI: 10.2337/dc09-1784.
6.	Kim BY, Kim CH, Jung CH, et al. Association between subclinical hypothyroidism and severe diabetic retinopathy in Korean patients with type 2 diabetes[J]. Endocr J, 2010, 58(12): 1065-1070.
7.	Chen HS, Wu TE, Jap TS, et al. Subclinical hypothyroidism is a risk factor for nephropathy and cardiovascular diseases in type 2 diabetic patients[J]. Diabetic Med, 2007, 24(12): 1336-1344.
8.	Ramis JN, Artigas CF, Santiago MA, et al. Is there a relationship between TSH levels and diabetic retinopathy in the Caucasian population?[J]. Diabetes Res Clin Pract, 2012, 97(3): 45-47. DOI: 10.1016/j.diabres.2012.05.015.
9.	World Health Organization. Definition, diagnosis and classification of diabetes mellitus and its complications: report of a WHO consultation[J]. J Med Genet, 1999, 37(12): 927-932.
10.	Wilkinson CP, Iii FLF, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales[J]. Ophthalmology, 2003, 110(9): 1677-1682.
11.	Türemen EE, Çetinarslan B, Şahin T, et al. Endothelial dysfunction and low grade chronic inflammation in subclinical hypothyroidism due to autoimmune thyroiditis[J]. Endocr J, 2011, 58(5): 349-354.
12.	Gao CX, Yang B, Guo Q, et al. High thyroid-stimulating hormone level is associated with the risk of developing atherosclerosis in subclinical hypothyroidism[J]. Horm Metab Res, 2015, 47(3): 220-224. DOI: 10.1055/s-0034-1394370.
13.	Biondi B, Cooper DS. The clinical significance of subclinical thyroid dysfunction[J]. Endocr Rev, 2008, 29(1): 76-131.
14.	Tian L, Gao C, Jing L, et al. Increased carotid arterial stiffness in subclinical hypothyroidism[J]. Eur J Intern Med, 2010, 21(6): 560-563.
15.	Popescu T, Moţa M. Dyslipidemia and hypertension in patients with type 2 diabetes and retinopathy[J]. Rom J Intern Med, 2009, 47(3): 235-241.
16.	Volanakis JE. Human C-reactive protein: expression, structure, and function[J]. Mol Immunol, 2001, 38(2-3): 189-197.
17.	Aksoy DY, Cinar N, Harmanci A, et al. Serum resistin and high sensitive CRP levels in patients with subclinical hypothyroidism before and after L-thyroxine therapy[J]. Med Sci Monit, 2013, 19: 210-215. DOI: 10.12659/MSM.883847.
18.	Nik MHS, Darabi M, Ziaee A, et al. Serum Phospholipase A2-ⅡA, hs-CRP, and lipids in women with subclinical hypo-thyroidism[J/OL]. Int J Endocrinol Metab, 2014, 12(3) : E16967 [2014-06-10]. . DOI: 10.5812/ijem.16967. [published online ahead of print].
19.	Sasongko MB, Wong TY, Jenkins AJ, et al. Circulating markers of inflammation and endothelial function, and their relationship to diabetic retinopathy[J]. Diabetic Med, 2015, 32(5): 686-691. DOI: 10.1111/dme.12640.
20.	Mcdermott MT, Ridgway EC. Subclinical hypothyroidism is mild thyroid failure and should be treated[J]. J Clin Endocrinol Metab, 2001, 86(10): 4585-4590.
21.	Cho HC. The relationship among homocysteine, bilirubin, and diabetic retinopathy[J]. Diabetes Metab J, 2011, 35(6): 595-601. DOI: 10.4093/dmj.2011.35.6.595.
22.	Maeda M, Yamamoto I, Fujio Y, et al. Homocysteine induces vascular endothelial growth factor expression in differentiated THP-1 macrophages[J]. Biochim Biophys Acta, 2003, 1623(1): 41-46.
23.	Maratou E, Hadjidakis DJ, Kollias A, et al. Studies of insulin resistance in patients with clinical and subclinical hypothyroidism[J]. Eur J Endocrinol, 2009, 160(5): 785-790. DOI: 10.1530/EJE-08-0797.
24.	Park CY, Park SE, Bae JC, et al. Prevalence of and risk factors for diabetic retinopathy in Koreans with type Ⅱdiabetes: baseline characteristics of Seoul Metropolitan City-Diabetes Prevention Program (SMC-DPP) participants[J]. Br J Ophthalmol, 2012, 96(96): 151-155.

1. Schroner Z, Lazurova I, Petrovicova J. Autoimmune thyroid diseases in patients with diabetes mellitus[J]. Bratisl Lek Listy, 2008, 109(3): 125-129.
2. Chubb SA, Davis WA, Inman Z, et al. Prevalence and progression of subclinical hypothyroidism in women with type 2 diabetes: the Fremantle Diabetes Study[J]. Clin Endocrinol, 2005, 62(4): 480-486.
3. Radaideh AR, Nusier MK, Amari FL, et al. Thyroid dysfunction in patients with type 2 diabetes mellitus in Jordan[J]. Saudi Med J, 2004, 25(8): 1046-1050.
4. Yang GR, Yang JK, Zhang L, et al. Association between subclinical hypothyroidism and proliferative diabetic retinopathy in type 2 diabetic patients: a case-control study[J]. Tohoku J Exp Med, 2010, 222(4): 303-310.
5. Yang JK, Liu W, Shi J, et al. An association between subclinical hypothyroidism and sight-threatening diabetic retinopathy in type 2 diabetic patients[J]. Diabetes Care, 2010, 33(5): 1018-1020. DOI: 10.2337/dc09-1784.
6. Kim BY, Kim CH, Jung CH, et al. Association between subclinical hypothyroidism and severe diabetic retinopathy in Korean patients with type 2 diabetes[J]. Endocr J, 2010, 58(12): 1065-1070.
7. Chen HS, Wu TE, Jap TS, et al. Subclinical hypothyroidism is a risk factor for nephropathy and cardiovascular diseases in type 2 diabetic patients[J]. Diabetic Med, 2007, 24(12): 1336-1344.
8. Ramis JN, Artigas CF, Santiago MA, et al. Is there a relationship between TSH levels and diabetic retinopathy in the Caucasian population?[J]. Diabetes Res Clin Pract, 2012, 97(3): 45-47. DOI: 10.1016/j.diabres.2012.05.015.
9. World Health Organization. Definition, diagnosis and classification of diabetes mellitus and its complications: report of a WHO consultation[J]. J Med Genet, 1999, 37(12): 927-932.
10. Wilkinson CP, Iii FLF, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales[J]. Ophthalmology, 2003, 110(9): 1677-1682.
11. Türemen EE, Çetinarslan B, Şahin T, et al. Endothelial dysfunction and low grade chronic inflammation in subclinical hypothyroidism due to autoimmune thyroiditis[J]. Endocr J, 2011, 58(5): 349-354.
12. Gao CX, Yang B, Guo Q, et al. High thyroid-stimulating hormone level is associated with the risk of developing atherosclerosis in subclinical hypothyroidism[J]. Horm Metab Res, 2015, 47(3): 220-224. DOI: 10.1055/s-0034-1394370.
13. Biondi B, Cooper DS. The clinical significance of subclinical thyroid dysfunction[J]. Endocr Rev, 2008, 29(1): 76-131.
14. Tian L, Gao C, Jing L, et al. Increased carotid arterial stiffness in subclinical hypothyroidism[J]. Eur J Intern Med, 2010, 21(6): 560-563.
15. Popescu T, Moţa M. Dyslipidemia and hypertension in patients with type 2 diabetes and retinopathy[J]. Rom J Intern Med, 2009, 47(3): 235-241.
16. Volanakis JE. Human C-reactive protein: expression, structure, and function[J]. Mol Immunol, 2001, 38(2-3): 189-197.
17. Aksoy DY, Cinar N, Harmanci A, et al. Serum resistin and high sensitive CRP levels in patients with subclinical hypothyroidism before and after L-thyroxine therapy[J]. Med Sci Monit, 2013, 19: 210-215. DOI: 10.12659/MSM.883847.
18. Nik MHS, Darabi M, Ziaee A, et al. Serum Phospholipase A2-ⅡA, hs-CRP, and lipids in women with subclinical hypo-thyroidism[J/OL]. Int J Endocrinol Metab, 2014, 12(3) : E16967 [2014-06-10]. . DOI: 10.5812/ijem.16967. [published online ahead of print].
19. Sasongko MB, Wong TY, Jenkins AJ, et al. Circulating markers of inflammation and endothelial function, and their relationship to diabetic retinopathy[J]. Diabetic Med, 2015, 32(5): 686-691. DOI: 10.1111/dme.12640.
20. Mcdermott MT, Ridgway EC. Subclinical hypothyroidism is mild thyroid failure and should be treated[J]. J Clin Endocrinol Metab, 2001, 86(10): 4585-4590.
21. Cho HC. The relationship among homocysteine, bilirubin, and diabetic retinopathy[J]. Diabetes Metab J, 2011, 35(6): 595-601. DOI: 10.4093/dmj.2011.35.6.595.
22. Maeda M, Yamamoto I, Fujio Y, et al. Homocysteine induces vascular endothelial growth factor expression in differentiated THP-1 macrophages[J]. Biochim Biophys Acta, 2003, 1623(1): 41-46.
23. Maratou E, Hadjidakis DJ, Kollias A, et al. Studies of insulin resistance in patients with clinical and subclinical hypothyroidism[J]. Eur J Endocrinol, 2009, 160(5): 785-790. DOI: 10.1530/EJE-08-0797.
24. Park CY, Park SE, Bae JC, et al. Prevalence of and risk factors for diabetic retinopathy in Koreans with type Ⅱdiabetes: baseline characteristics of Seoul Metropolitan City-Diabetes Prevention Program (SMC-DPP) participants[J]. Br J Ophthalmol, 2012, 96(96): 151-155.

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