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Vol 71, No 2 (2020)
Review paper
Submitted: 2019-12-08
Accepted: 2020-02-02
Published online: 2020-04-29
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Thyroid dysfunction in patients with diabetic retinopathy

Magdalena M. Stefanowicz-Rutkowska1, Angelika Baranowska-Jurkun1, Wojciech Matuszewski1, Elżbieta M. Bandurska-Stankiewicz1
DOI: 10.5603/EP.a2020.0013
·
Pubmed: 32396211
·
Endokrynol Pol 2020;71(2):176-183.
Affiliations
  1. Clinical Department of Endocrinology, Diabetology, and Internal Diseases, School of Medicine, Collegium Medicum, University of Warmia and Mazury in Olsztyn, Poland

open access

Vol 71, No 2 (2020)
Review Article
Submitted: 2019-12-08
Accepted: 2020-02-02
Published online: 2020-04-29

Abstract

Thyroid disease and diabetes mellitus (DM) are the most common endocrinopathies in clinical practice that interact with each other. On the one hand, thyroid hormones regulate carbohydrate metabolism and pancreas functions, and on the other hand DM affects the function and work of the thyroid gland. Diabetic retinopathy (DR) is a highly specific neurovascular complication of both type 1 and type 2 DM, which is a significant cause of vision loss on a global scale. In DM, the internal blood-retinal barrier is the earliest to be damaged, and changes in neuroretina result from the loss of its adaptation to metabolic disorders. Patients with DM have a higher incidence of thyroid disease compared to people without DM. The coexistence of DM with thyroid disease leads to endothelial damage, and the degree of its dysfunction has a significant impact on the course of macro- and microangiopathic complications in patients. There are few reports in the literature about the impact of thyroid disease and substitution of levothyroxine preparations on the development and course of DR in patients with DM. It is unknown whether the fact that patients with unrecognised hypothyroidism are not treated with levothyroxine preparations disrupts thyroid hormone homeostasis to the extent that it may contribute to a higher incidence of DR. This review discusses recent clinical trials for thyroid dysfunction in patients with DR. 

Abstract

Thyroid disease and diabetes mellitus (DM) are the most common endocrinopathies in clinical practice that interact with each other. On the one hand, thyroid hormones regulate carbohydrate metabolism and pancreas functions, and on the other hand DM affects the function and work of the thyroid gland. Diabetic retinopathy (DR) is a highly specific neurovascular complication of both type 1 and type 2 DM, which is a significant cause of vision loss on a global scale. In DM, the internal blood-retinal barrier is the earliest to be damaged, and changes in neuroretina result from the loss of its adaptation to metabolic disorders. Patients with DM have a higher incidence of thyroid disease compared to people without DM. The coexistence of DM with thyroid disease leads to endothelial damage, and the degree of its dysfunction has a significant impact on the course of macro- and microangiopathic complications in patients. There are few reports in the literature about the impact of thyroid disease and substitution of levothyroxine preparations on the development and course of DR in patients with DM. It is unknown whether the fact that patients with unrecognised hypothyroidism are not treated with levothyroxine preparations disrupts thyroid hormone homeostasis to the extent that it may contribute to a higher incidence of DR. This review discusses recent clinical trials for thyroid dysfunction in patients with DR. 

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Keywords

thyroid disease; diabetes mellitus; diabetic retinopathy

About this article
Title

Thyroid dysfunction in patients with diabetic retinopathy

Journal

Endokrynologia Polska

Issue

Vol 71, No 2 (2020)

Article type

Review paper

Pages

176-183

Published online

2020-04-29

Page views

2501

Article views/downloads

1783

DOI

10.5603/EP.a2020.0013

Pubmed

32396211

Bibliographic record

Endokrynol Pol 2020;71(2):176-183.

Keywords

thyroid disease
diabetes mellitus
diabetic retinopathy

Authors

Magdalena M. Stefanowicz-Rutkowska
Angelika Baranowska-Jurkun
Wojciech Matuszewski
Elżbieta M. Bandurska-Stankiewicz

References (85)
  1. Mamun M, Nahar N, Salekin M, et al. Thyroid Hormonal Status in Newly Diagnosed Type 2 Diabetes Mellitus. Bangl J Nucl Med. 2018; 20: 1–27.
    CrossRef
  2. Nishi M. Diabetes mellitus and thyroid diseases. Diabetol Int. 2018; 9(2): 108–112.
    CrossRefPubMed
  3. Donckier JE. Endocrine diseases and diabetes. In: Pickup JC, Williams G. ed. Diabetes Mellitus. Blackwell Publishing Company, Chichester 2003: 21–27.
  4. Biondi B, Kahaly GJ, Robertson RP. Thyroid Dysfunction and Diabetes Mellitus: Two Closely Associated Disorders. Endocr Rev. 2019; 40(3): 789–824.
    CrossRefPubMed
  5. Chutia H, Bhattacharyya H, Ruram AA, et al. Evaluation of thyroid function in type 2 diabetes in north-eastern part of India: A hospital-based study. J Family Med Prim Care. 2018; 7(4): 752–755.
    CrossRefPubMed
  6. Chawla A, Chawla R, Jaggi S. Microvasular and macrovascular complications in diabetes mellitus: Distinct or continuum? Indian J Endocrinol Metab. 2016; 20(4): 546–551.
    CrossRefPubMed
  7. Solomon SD, Chew E, Duh EJ, et al. Diabetic Retinopathy: A Position Statement by the American Diabetes Association. Diabetes Care. 2017; 40(3): 412–418.
    CrossRefPubMed
  8. Zalecenia kliniczne dotyczące postępowania u chorych na cukrzycę Stanowisko Polskiego Towarzystwa Diabetologicznego. Diabetologia Praktyczna. 2018; 4(1): 1–94.
  9. Sheldon J. Laboratory testing in autoimmune rheumatic diseases. Best Pract Res Clin Rheumatol. 2004; 18(3): 249–269.
    CrossRefPubMed
  10. McCoy L, Tsunoda I, Fujinami RS. Multiple sclerosis and virus induced immune responses: autoimmunity can be primed by molecular mimicry and augmented by bystander activation. Autoimmunity. 2006; 39(1): 9–19.
    CrossRefPubMed
  11. Guilherme L, Kalil J. Rheumatic fever: the T cell response leading to autoimmune aggression in the heart. Autoimmun Rev. 2002; 1(5): 261–266.
    CrossRefPubMed
  12. Hayter SM, Cook MC. Updated assessment of the prevalence, spectrum and case definition of autoimmune disease. Autoimmun Rev. 2012; 11(10): 754–765.
    CrossRefPubMed
  13. Sfriso P, Ghirardello A, Botsios C, et al. Infections and autoimmunity: the multifaceted relationship. J Leukoc Biol. 2010; 87(3): 385–395.
    CrossRefPubMed
  14. Desai MK, Brinton RD. Autoimmune Disease in Women: Endocrine Transition and Risk Across the Lifespan. Front Endocrinol (Lausanne). 2019; 10: 265.
    CrossRefPubMed
  15. Golden SH, Robinson KA, Saldanha I, et al. Clinical review: Prevalence and incidence of endocrine and metabolic disorders in the United States: a comprehensive review. J Clin Endocrinol Metab. 2009; 94(6): 1853–1878.
    CrossRefPubMed
  16. Iddah MA, Macharia BN. Autoimmune thyroid disorders. ISRN Endocrinol. 2013; 2013: 509764.
    CrossRefPubMed
  17. Sawicka-Gutaj N, Zybek-Kocik A, Klimowicz A, et al. Circulating Visfatin in Hypothyroidism Is Associated with Free Thyroid Hormones and Antithyroperoxidase Antibodies. Int J Endocrinol. 2016; 2016: 7402469.
    CrossRefPubMed
  18. Delemer B, Aubert JP, Nys P, et al. An observational study of the initial management of hypothyroidism in France: the ORCHIDÉE study. Eur J Endocrinol. 2012; 167(6): 817–823.
    CrossRefPubMed
  19. Caturegli P, De Remigis A, Rose NR. Hashimoto thyroiditis: clinical and diagnostic criteria. Autoimmun Rev. 2014; 13(4-5): 391–397.
    CrossRefPubMed
  20. Bloodworth J. Diabetic retinopathy. Diabetes. 1962; 11: 1–22.
    PubMed
  21. Wolter JR. Diabetic retinopathy. Am J Ophthalmol. 1961; 51: 1123–1141.
    CrossRefPubMed
  22. Cunha-Vaz J. Neurodegeneration as an early event in the pathogenesis of Diabetic Retinopathy: A multicentric, prospective, phase II-III, randomised controlled trial to assess the efficacy of neuroprotective drugs administered topically to prevent or arrest Diabetic Rethinopathy. EUROCONDOR — EU FP7 Project. Acta Ophthalmol. 2012; 90(249): 0–0.
    CrossRef
  23. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med. 2012; 366(13): 1227–1239.
    CrossRefPubMed
  24. Cunha-Vaz J, Ribeiro L, Lobo C. Phenotypes and biomarkers of diabetic retinopathy. Prog Retin Eye Res. 2014; 41: 90–111.
    CrossRefPubMed
  25. Ratajczak W, Tokarz-Deptuła B, Deptuła W. Immunologia oka. Postepy Hig Med Dosw (online). 2018; 72: 318–325.
  26. Abcouwer SF, Gardner TW. Diabetic retinopathy: loss of neuroretinal adaptation to the diabetic metabolic environment. Ann NY Acad Sci. 2014; 1311: 174–190.
    CrossRefPubMed
  27. Sohn EH, van Dijk HW, Jiao C, et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus. Proc Natl Acad Sci USA. 2016; 113(19): E2655–E2664.
    CrossRefPubMed
  28. Eshaq RS, Aldalati AMZ, Alexander JS, et al. Diabetic retinopathy: Breaking the barrier. Pathophysiology. 2017; 24(4): 229–241.
    CrossRefPubMed
  29. Rusin P, Majsterek I. Molekularne podstawy retinopatii cukrzycowej. Postępy Hig. Med. Dośw. (online). 2007; 61: 786–796.
  30. Yau JWY, Rogers SL, Kawasaki R, et al. Meta-Analysis for Eye Disease (META-EYE) Study Group. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012; 35(3): 556–564.
    CrossRefPubMed
  31. Kollias AN, Ulbig MW. Diabetic retinopathy: Early diagnosis and effective treatment. Dtsch Arztebl Int. 2010; 107(5): 75–83; quiz 84.
    CrossRefPubMed
  32. Wu L, Fernandez-Loaiza P, Sauma J, et al. Classification of diabetic retinopathy and diabetic macular edema. World J Diabetes. 2013; 4(6): 290–294.
    CrossRefPubMed
  33. Fong DS, Aiello L, Gardner TW, et al. Diabetic Retinopathy. Diabetes Care. 2003; 26(Supplement 1): S99–S102.
    CrossRefPubMed
  34. Rajalakshmi R, Prathiba V, Mohan V. Does tight control of systemic factors help in the management of diabetic retinopathy? Indian J Ophthalmol. 2016; 64(1): 62–68.
    CrossRefPubMed
  35. Pradeepa R, Anitha B, Mohan V, et al. Risk factors for diabetic retinopathy in a South Indian Type 2 diabetic population — the Chennai Urban Rural Epidemiology Study (CURES) Eye Study 4. Diabet Med. 2008; 25(5): 536–542.
    CrossRefPubMed
  36. Shichiri M, Kishikawa H, Ohkubo Y, et al. Long-term results of the Kumamoto Study on optimal diabetes control in type 2 diabetic patients. Diabetes Care. 2000; 23(Suppl 2): B21–B29.
    PubMed
  37. Chew EY, Ambrosius WT, Davis MD, et al. ACCORD Study Group, ACCORD Eye Study Group. Effects of medical therapies on retinopathy progression in type 2 diabetes. N Engl J Med. 2010; 363(3): 233–244.
    CrossRefPubMed
  38. Nathan DM, Genuth S, Lachin J, et al. Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993; 329(14): 977–986.
    CrossRefPubMed
  39. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet. 1998; 352(9131): 837–853.
    PubMed
  40. Matuszewski W, Bandurska-Stankiewicz E, Modzelewski R, et al. Diagnosis and treatment of diabetic retinopathy — historical overview. Clin Diab. 2017; 6(5): 182–188.
    CrossRef
  41. Silva PS, Cavallerano JD, Sun JK, et al. Effect of systemic medications on onset and progression of diabetic retinopathy. Nat Rev Endocrinol. 2010; 6(9): 494–508.
    CrossRefPubMed
  42. Kozak I, Luttrull JK. Modern retinal laser therapy. Saudi J Ophthalmol. 2015; 29(2): 137–146.
    CrossRefPubMed
  43. Yun SH, Adelman RA. Recent developments in laser treatment of diabetic retinopathy. Middle East Afr J Ophthalmol. 2015; 22(2): 157–163.
    CrossRefPubMed
  44. Zhao Y, Singh RP. The role of anti-vascular endothelial growth factor (anti-VEGF) in the management of proliferative diabetic retinopathy. Drugs Context. 2018; 7: 212532.
    CrossRefPubMed
  45. Brănişteanu DC, Bilha A, Moraru A. Vitrectomy surgery of diabetic retinopathy complications. Rom J Ophthalmol. 2016; 60(1): 31–36.
    PubMed
  46. Papadopoulos N, Martin J, Ruan Q, et al. Binding and neutralization of vascular endothelial growth factor (VEGF) and related ligands by VEGF Trap, ranibizumab and bevacizumab. Angiogenesis. 2012; 15(2): 171–185.
    CrossRefPubMed
  47. Hage M, Zantout MS, Azar ST. Thyroid disorders and diabetes mellitus. J Thyroid Res. 2011; 2011: 439463.
    CrossRefPubMed
  48. Perros P, McCrimmon RJ, Shaw G, et al. Frequency of thyroid dysfunction in diabetic patients: value of annual screening. Diabet Med. 1995; 12(7): 622–627.
    CrossRefPubMed
  49. Hansen D, Bennedbaek FN, Hansen LK, et al. Thyroid function, morphology and autoimmunity in young patients with insulin-dependent diabetes mellitus. Eur J Endocrinol. 1999; 140(6): 512–518.
    CrossRefPubMed
  50. 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(1): 15–25.
    PubMed
  51. Ray S, Ghosh S. Thyroid Disorders and Diabetes Mellitus: Double Trouble . J Dia Res Ther. 2016; 2(1).
    CrossRef
  52. Palma CC, Pavesi M, Nogueira VG, et al. Prevalence of thyroid dysfunction in patients with diabetes mellitus. Diabetol Metab Syndr. 2013; 5(1): 58.
    CrossRefPubMed
  53. Kordonouri O, Charpentier N, Hartmann R. GADA positivity at onset of type 1 diabetes is a risk factor for the development of autoimmune thyroiditis. Pediatr Diabetes. 2011; 12(1): 31–33.
    CrossRefPubMed
  54. Kadiyala R, Peter R, Okosieme OE. Thyroid dysfunction in patients with diabetes: clinical implications and screening strategies. Int J Clin Pract. 2010; 64(8): 1130–1139.
    CrossRefPubMed
  55. Ahmed A, Waris A, Naheed A, et al. Diabetic Retinopathy and its Correlation with Thyroid Profile and Anti Thyroid Antibodies. IOSR-JDMS. 2017; 16(1): 96–98.
    CrossRef
  56. Kordonouri O, Deiss D, Danne T, et al. Predictivity of thyroid autoantibodies for the development of thyroid disorders in children and adolescents with Type 1 diabetes. Diabet Med. 2002; 19(6): 518–521.
    CrossRefPubMed
  57. Kordonouri O, Hartmann R, Deiss D, et al. Natural course of autoimmune thyroiditis in type 1 diabetes: association with gender, age, diabetes duration, and puberty. Arch Dis Child. 2005; 90(4): 411–414.
    CrossRefPubMed
  58. Lindberg B, Ericsson UB, Ljung R, et al. High prevalence of thyroid autoantibodies at diagnosis of insulin-dependent diabetes mellitus in Swedish children. J Lab Clin Med. 1997; 130(6): 585–589.
    CrossRefPubMed
  59. Gursoy NT, Tuncel E. The relationship between the glycemic control and the hypothalamus–pituitary–thyroid axis in diabetic patients. Turk J Endocrinol Metab. 1999; 4: 163–168.
  60. Ortiz-Caro J, Obregón MJ, Pascual A, et al. Decreased T4 to T3 conversion in tissues of streptozotocin-diabetic rats. Acta Endocrinol (Copenh). 1984; 106(1): 86–91.
    CrossRefPubMed
  61. Bagchi N, Palaniswami N, Desai H, et al. Decreased thyroidal response to thyrotropin in type II diabetes mellitus. Metabolism. 1988; 37(7): 669–671.
    CrossRefPubMed
  62. Rezzonico J, Rezzonico M, Pusiol E, et al. Introducing the thyroid gland as another victim of the insulin resistance syndrome. Thyroid. 2008; 18(4): 461–464.
    CrossRefPubMed
  63. Ayturk S, Gursoy A, Kut A, et al. Metabolic syndrome and its components are associated with increased thyroid volume and nodule prevalence in a mild-to-moderate iodine-deficient area. Eur J Endocrinol. 2009; 161(4): 599–605.
    CrossRefPubMed
  64. Chutia H, Bhattacharyya H, Ruram AA, et al. Evaluation of thyroid function in type 2 diabetes in north-eastern part of India: A hospital-based study. J Family Med Prim Care. 2018; 7(4): 752–755.
    CrossRefPubMed
  65. Martino E, Seo H, Lernmark A, et al. Ontogenetic patterns of thyrotropin-releasing hormone-like material in rat hypothalamus, pancreas, and retina: selective effect of light deprivation. Proc Natl Acad Sci USA. 1980; 77(7): 4345–4348.
    CrossRefPubMed
  66. Mendoza A, Hollenberg AN. New insights into thyroid hormone action. Pharmacol Ther. 2017; 173: 135–145.
    CrossRefPubMed
  67. Pinazo-Durán MD, Pons-Vázquez S, Gallego-Pinazo R, et al. Thyroid hormone deficiency disrupts rat eye neurodevelopment. Brain Res. 2011; 1392: 16–26.
    CrossRefPubMed
  68. Kocaturk T, Ergin K, Cesur G, et al. The effect of methimazole-induced postnatal hypothyroidism on the retinal maturation and on the Sirtuin 2 level. Cutan Ocul Toxicol. 2016; 35(1): 36–40.
    CrossRefPubMed
  69. Waber S, Meister V, Rossi GL, et al. Studies on retinal microangiopathy and coronary macroangiopathy in rats with streptozotocin-induced diabetes. Virchows Arch B Cell Pathol Incl Mol Pathol. 1981; 37(1): 1–10.
    CrossRefPubMed
  70. Takiguchi Y, Satoh N, Hashimoto H, et al. Reversal effect of thyroxine on altered vascular reactivity in diabetic rats. J Cardiovasc Pharmacol. 1989; 13(4): 520–524.
    PubMed
  71. Ittermann T, Dörr M, Völzke H, et al. High serum thyrotropin levels are associated with retinal arteriolar narrowing in the general population. Thyroid. 2014; 24(10): 1473–1478.
    CrossRefPubMed
  72. Czarnywojtek A, Owecki M, Zgorzalewicz-Stachowiak M, et al. The role of serum C-reactive protein measured by high-sensitive method in thyroid disease. Arch Immunol Ther Exp (Warsz). 2014; 62(6): 501–509.
    CrossRefPubMed
  73. Iitaka M, Miura S, Yamanaka K, et al. Increased serum vascular endothelial growth factor levels and intrathyroidal vascular area in patients with Graves' disease and Hashimoto's thyroiditis. J Clin Endocrinol Metab. 1998; 83(11): 3908–3912.
    CrossRefPubMed
  74. Kajdaniuk D, Marek B, Foltyn W, et al. Vascular endothelial growth factor (VEGF) — part 2: in endocrinology and oncology. Endokrynol Pol. 2011; 62(5): 456–464.
    PubMed
  75. Rizos CV, Elisaf MS, Liberopoulos EN. Effects of thyroid dysfunction on lipid profile. Open Cardiovasc Med J. 2011; 5: 76–84.
    CrossRefPubMed
  76. Popescu T, Moţa M. Dyslipidemia and hypertension in patients with type 2 diabetes and retinopathy. Rom J Intern Med. 2009; 47(3): 235–241.
    PubMed
  77. Baskol G, Atmaca H, Tanriverdi F, et al. Oxidative stress and enzymatic antioxidant status in patients with hypothyroidism before and after treatment. Exp Clin Endocrinol Diabetes. 2007; 115(8): 522–526.
    CrossRefPubMed
  78. Rodacki M, Zajdenverg L, Dantas JR, et al. Should thyroid-stimulating hormone goals be reviewed in patients with type 1 diabetes mellitus? Results from the Brazilian Type 1 Diabetes Study Group. Diabet Med. 2014; 31(12): 1665–1672.
    CrossRefPubMed
  79. Rogowicz-Frontczak A, Pilacinski S, Chwialkowska AT, et al. Patients with diabetes type 1 and thyroid autoimmunity have low prevalence of microangiopathic complications. Endocrine. 2016; 51(1): 185–188.
    CrossRefPubMed
  80. Glastras SJ, Craig ME, Verge CF, et al. The role of autoimmunity at diagnosis of type 1 diabetes in the development of thyroid and celiac disease and microvascular complications. Diabetes Care. 2005; 28(9): 2170–2175.
    CrossRefPubMed
  81. Schneider T, Meyerson L. Thyroid therapy in diabetic retinopathy. S Afr Med J. 1969; 43(14): 414–417.
    PubMed
  82. Sailesh S. The THOR Effect: Thyroid Hormone Offsets Retinopathy. J Endocrinol Thyroid Res. 2018; 3(1): 555605.
    CrossRef
  83. Wu J, Yue S, Geng J, et al. Relationship between Diabetic Retinopathy and Subclinical Hypothyroidism: a meta-analysis. Sci Rep. 2015; 5: 12212.
    CrossRefPubMed
  84. Borooah M, Phukan S. A study on relationship between severity of diabetic retinopathy and subclinical hypothyroidism. Int J Res Med Sci. 2017; 5(5): 1818–1822.
  85. Porta M, Sjoelie AK, Chaturvedi N, et al. EURODIAB Prospective Complications Study Group. Risk factors for progression to proliferative diabetic retinopathy in the EURODIAB Prospective Complications Study. Diabetologia. 2001; 44(12): 2203–2209.
    CrossRefPubMed

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