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Presence and Risk Factors for Glaucoma in Patients with Diabetes

  • Microvascular Complications—Retinopathy (JK Sun and PS Silva, Section Editors)
  • Published:
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Abstract

Diabetes mellitus represents a growing international public health issue with a near quadrupling in its worldwide prevalence since 1980. Though it has many known microvascular complications, vision loss from diabetic retinopathy is one of the most devastating for affected individuals. In addition, there is increasing evidence to suggest that diabetic patients have a greater risk for glaucoma as well. Though the pathophysiology of glaucoma is not completely understood, both diabetes and glaucoma appear to share some common risk factors and pathophysiologic similarities with studies also reporting that the presence of diabetes and elevated fasting glucose levels are associated with elevated intraocular pressure—the primary risk factor for glaucomatous optic neuropathy. While no study has completely addressed the possibility of detection bias, most recent epidemiologic evidence suggests that diabetic populations are likely enriched with glaucoma patients. As the association between diabetes and glaucoma becomes better defined, routine evaluation for glaucoma in diabetic patients, particularly in the telemedicine setting, may become a reasonable consideration to reduce the risk of vision loss in these patients.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4–14.

    Article  CAS  PubMed  Google Scholar 

  2. NCD Risk Factor Collaboration (NCD-RisC). Worldwide trends in diabetes since 1980: a pooled analysis of 751 population-based studies with 4.4 million participants. Lancet. 2016;387:1513–30.

    Article  Google Scholar 

  3. Zhang P, Zhang X, Brown J, et al. Global healthcare expenditure on diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:293–301.

    Article  PubMed  Google Scholar 

  4. Moss SE, Klein R, Klein BE. The 14-year incidence of visual loss in a diabetic population. Ophthalmology. 1998;105:998–1003.

    Article  CAS  PubMed  Google Scholar 

  5. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124–36.

    Article  PubMed  Google Scholar 

  6. Klein BE. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol. 2007;14:179–83.

    Article  PubMed  Google Scholar 

  7. Ting DS, Cheung GC, Wong TY. Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review. Clin Exp Ophthalmol. 2016;44:260–77.

    Article  PubMed  Google Scholar 

  8. Saaddine JB, Narayan KM, Engelgau MM, et al. Prevalence of self-rated visual impairment among adults with diabetes. Am J Public Health. 1999;89:1200–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35:556–64.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Stanga PE, Boyd SR, Hamilton AM. Ocular manifestations of diabetes mellitus. Curr Opin Ophthalmol. 1999;10:483–9.

    Article  CAS  PubMed  Google Scholar 

  11. Zhao D, Cho J, Kim MH, et al. Diabetes, fasting glucose, and the risk of glaucoma: a meta-analysis. Ophthalmology. 2015;122:72–8. This meta-analysis pooled data from previous epidemiologic studies to further support the relationship between diabetes status with glaucoma risk in addition to examining the relationship of diabetic characteristics, specifically diabetes duration and fasting glucose levels, with glaucoma risk as well.

    Article  PubMed  Google Scholar 

  12. Zhao D, Cho J, Kim MH, et al. Diabetes, glucose metabolism, and glaucoma: the 2005–2008 National Health and Nutrition Examination Survey. PLoS One. 2014;9:e112460.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Ko F, Boland MV, Gupta P, et al. Diabetes, triglyceride levels, and other risk factors for glaucoma in the National Health and Nutrition Examination Survey 2005–2008. Invest Ophthalmol Vis Sci. 2016;57:2152–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tham YC, Li X, Wong TY, et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121:2081–90.

    Article  PubMed  Google Scholar 

  15. Boland MV, Quigley HA. Risk factors and open-angle glaucoma: classification and application. J Glaucoma. 2007;16:406–18.

    Article  PubMed  Google Scholar 

  16. Mitchell P, Smith W, Chey T, et al. Open-angle glaucoma and diabetes: the Blue Mountains eye study, Australia. Ophthalmology. 1997;104:712–8.

    Article  CAS  PubMed  Google Scholar 

  17. Klein BE, Klein R, Jensen SC. Open-angle glaucoma and older-onset diabetes. The Beaver Dam Eye Study. Ophthalmology. 1994;101:1173–7.

    Article  CAS  PubMed  Google Scholar 

  18. Shen L, Walter S, Melles RB, et al. Diabetes pathology and risk of primary open-angle glaucoma: evaluating causal mechanisms by using genetic information. Am J Epidemiol. 2016;183:147–55.

    Article  PubMed  Google Scholar 

  19. Pasquale LR, Kang JH, Manson JE, et al. Prospective study of type 2 diabetes mellitus and risk of primary open-angle glaucoma in women. Ophthalmology. 2006;113:1081–6.

    Article  PubMed  Google Scholar 

  20. Ciulla TA, Amador AG, Zinman B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care. 2003;26:2653–64.

    Article  PubMed  Google Scholar 

  21. Kador PF, Wyman M, Oates PJ. Aldose reductase, ocular diabetic complications and the development of topical Kinostat. Prog Retin Eye Res. 2016;54:1–29.

    Article  CAS  PubMed  Google Scholar 

  22. Brownlee M, Vlassara H, Cerami A. Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann Intern Med. 1984;101:527–37.

    Article  CAS  PubMed  Google Scholar 

  23. Friedman EA. Advanced glycosylated end products and hyperglycemia in the pathogenesis of diabetic complications. Diabetes Care. 1999;22 Suppl 2:B65–71.

    PubMed  Google Scholar 

  24. Monnier VM, Sell DR, Dai Z, et al. The role of the amadori product in the complications of diabetes. Ann NY Acad Sci. 2008;1126:81–8.

    Article  CAS  PubMed  Google Scholar 

  25. Schmidt AM, Yan SD, Wautier JL, et al. Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res. 1999;84:489–97.

    Article  CAS  PubMed  Google Scholar 

  26. Singh R, Barden A, Mori T, et al. Advanced glycation end-products: a review. Diabetologia. 2001;44:129–46.

    Article  CAS  PubMed  Google Scholar 

  27. Hammes HP, Martin S, Federlin K, et al. Aminoguanidine treatment inhibits the development of experimental diabetic retinopathy. Proc Natl Acad Sci U S A. 1991;88:11555–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kowluru RA, Engerman RL, Kern TS. Abnormalities of retinal metabolism in diabetes or experimental galactosemia, VIII: prevention by aminoguanidine. Curr Eye Res. 2000;21:814–9.

    Article  CAS  PubMed  Google Scholar 

  29. Kern TS, Engerman RL. Pharmacological inhibition of diabetic retinopathy: aminoguanidine and aspirin. Diabetes. 2001;50:1636–42.

    Article  CAS  PubMed  Google Scholar 

  30. Aiello LP. The potential role of PKC β in diabetic retinopathy and macular edema. Surv Ophthalmol. 2002;47 Suppl 2:S263–9.

    Article  PubMed  Google Scholar 

  31. Inoguchi T, Battan R, Handler E, et al. Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci U S A. 1992;89:11059–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Xia P, Inoguchi T, Kern TS, et al. Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes. 1994;43:1122–9.

    Article  CAS  PubMed  Google Scholar 

  33. Evicmen ND, King GL. The role of protein kinase C activation and the vascular complications of diabetes. Pharmacol Res. 2007;55:498–510.

    Article  CAS  Google Scholar 

  34. Idris I, Donelly R. Protein kinase Cβ inhibition: a novel therapeutic strategy for diabetic microangiopathy. Diab Vasc Dis Res. 2006;3:172–8.

    Article  PubMed  Google Scholar 

  35. Meier M, King GL. Protein kinase C activation and its pharmacological inhibition in vascular disease. Vasc Med. 2000;5:173–85.

    Article  CAS  PubMed  Google Scholar 

  36. Way KJ, Katai N, King GL. Protein kinase C and the development of diabetic vascular complications. Diabet Med. 2001;18:945–59.

    Article  CAS  PubMed  Google Scholar 

  37. Avignon A, Sultan A. PKC-epsilon inhibition: a new therapeutic approach for diabetic complications? Diabetes Metab. 2006;32:205–13.

    Article  CAS  PubMed  Google Scholar 

  38. Sobhia ME, Grewal BK, Bhat J, et al. Protein kinase C βII in diabetic complications: survey of structural, biological and computational studies. Expert Opin Ther Targets. 2012;16:325–44.

    Article  CAS  PubMed  Google Scholar 

  39. Kubawara T, Cogan DG. Retinal vascular patterns, VI: mural cells of the retinal capillaries. Arch Ophthalmol. 1962;69:492–502.

    Article  Google Scholar 

  40. Sims DE. The pericyte: a review. Tissue Cell. 1986;18:153–74.

    Article  CAS  PubMed  Google Scholar 

  41. Antonelli-Orlidge A, Smith SR, D’Amore PA. Influence of pericytes on capillary endothelial cell growth. Am Rev Respir Dis. 1989;140:1129–31.

    Article  CAS  PubMed  Google Scholar 

  42. Kohner EM, Patel V, Rassam SM. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes. 1995;44:603–7.

    Article  CAS  PubMed  Google Scholar 

  43. Ciulla TA, Harris A, Latkany P, et al. Ocular perfusion abnormalities in diabetes. Acta Ophthalmol Scand. 2002;80:468–77.

    Article  PubMed  Google Scholar 

  44. Miyamoto K, Ogura Y. Pathogenetic potential of leukocytes in diabetic retinopathy. Semin Ophthalmol. 1999;14:233–9.

    Article  CAS  PubMed  Google Scholar 

  45. Aiello LP, Avery RL, Arrigg PG, et al. Vascular endothelial growth factor in ocular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331:1480–7.

    Article  CAS  PubMed  Google Scholar 

  46. Miller JW, Adamis AP, Aiello LP. Vascular endothelial growth factor in ocular neovascularization and proliferative diabetic retinopathy. Diabetes Metab Rev. 1997;13:37–50.

    Article  CAS  PubMed  Google Scholar 

  47. Aiello LP, Northrup JM, Keyt BA, et al. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol. 1995;113:1538–44.

    Article  CAS  PubMed  Google Scholar 

  48. Ng JS, Bearse Jr MA, Schneck ME, et al. Local diabetic retinopathy prediction by multifocal ERG delays over 3 years. Invest Ophthalmol Vis Sci. 2008;49:1622–8.

    Article  PubMed  Google Scholar 

  49. Abu-El-Asrar AM, Dralands L, Missotten L, et al. Expression of apoptosis markers in the retinas of human subjects with diabetes. Invest Ophthalmol Vis Sci. 2004;45:2760–6.

    Article  PubMed  Google Scholar 

  50. Ola MS, Alhomida AS. Neurodegeneration in diabetic retina and its potential drug targets. Curr Neuropharmacol. 2014;12:380–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Barber AJ, Lieth E, Khin SA, et al. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J Clin Invest. 1998;102:783–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ajlan RS, Silva PS, Sun JK. Vascular endothelial growth factor and diabetic retinal disease. Semin Ophthalmol. 2016;31:40–8.

    Article  PubMed  Google Scholar 

  53. Avery RL. Regression of retinal and iris neovascularization after intravitreal bevacizumab (Avastin) treatment. Retina. 2006;26:352–4.

    Article  PubMed  Google Scholar 

  54. Gross JG, Glassman AR. A novel treatment for proliferative diabetic retinopathy: anti-vascular endothelial growth factor therapy. JAMA Ophthalmol. 2016;134:13–4.

    Article  PubMed  Google Scholar 

  55. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90:262–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sommer A, Tielsch JM, Katz J, et al. Relationship between intraocular pressure and primary open angle glaucoma among white and black Americans. The Baltimore Eye Survey. Arch Ophthalmol. 1991;109:1090–5.

    Article  CAS  PubMed  Google Scholar 

  57. Iwase A, Suzuki Y, Araie M, et al. The prevalence of primary open-angle glaucoma in Japan: the Tajimi Study. Ophthalmology. 2004;111:1641–8.

    PubMed  Google Scholar 

  58. Weinreb RN, Aung T, Medeiros FA. The pathophysiology and treatment of glaucoma: a review. JAMA. 2014;18:1901–11.

    Article  CAS  Google Scholar 

  59. Quigley HA, Addicks EM, Green W, et al. Optic nerve damage in human glaucoma, II: the site of injury and susceptibility to damage. Arch Ophthalmol. 1981;99:635–49.

    Article  CAS  PubMed  Google Scholar 

  60. Burgoyne CF, Downs JC, Bellezza AJ, et al. The optic nerve head as a biomechanical structure: a new paradigm for understanding the role of IOP-related stress and strain in the pathophysiology of glaucomatous optic nerve head damage. Prog Retin Eye Res. 2005;24:39–73.

    Article  PubMed  Google Scholar 

  61. Quigley HA, McKinnon SJ, Zack DJ, et al. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci. 2000;41:3460–6.

    CAS  PubMed  Google Scholar 

  62. Fechtner RD, Weinreb RN. Mechanisms of optic nerve damage in primary open angle glaucoma. Surv Ophthalmol. 1994;39:23–42.

    Article  CAS  PubMed  Google Scholar 

  63. Quigley HA, Nickells RW, Kerrigan LA, et al. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774–86.

    CAS  PubMed  Google Scholar 

  64. Alward WL, Kwon YH, Khanna CL, et al. Variations in the myocilin gene in patients with open-angle glaucoma. Arch Ophthalmol. 2002;120:1189–97.

    Article  CAS  PubMed  Google Scholar 

  65. Stone EM, Fingert JH, Alward WL, et al. Identification of a gene that causes primary open angle glaucoma. Science. 1997;275:668–70.

    Article  CAS  PubMed  Google Scholar 

  66. Gong G, Kosoko-Lasaki O, Haynatzki GR, et al. Genetic dissection of myocilin glaucoma. Hum Mol Genet. 2004;13 Spec No 1:R91-102.

  67. Thorleifsson G, Walters GB, Hewitt AW, et al. Common variants near CAV1 and CAV2 are associated with primary open-angle glaucoma. Nat Genet. 2010;42:906–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wiggs JL, Kang JH, Yaspan BL, et al. Common variants near CAV1 and CAV2 are associated with primary open angle glaucoma in Caucasians from the USA. Hum Mol Genet. 2011;20:4707–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Burdon KP, Macgregor S, Hewitt AW, et al. Genome-wide association study identifies susceptibility loci for open angle glaucoma at TMCO1 and CDKN2B-AS1. Nat Genet. 2011;43:574–8.

    Article  CAS  PubMed  Google Scholar 

  70. Wiggs JL, Yaspan BL, Hauser MA, et al. Common variants at 9p21 and 8q22 are associated with increased susceptibility to optic nerve degeneration in glaucoma. PLoS Genet. 2012;8:e1002654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Cooke Bailey JN, Loomis SJ, Kang JH, et al. Genome-wide association analysis identifies TXNRD2, ATXN2, and FOXC1, as susceptibility loci for primary open-angle glaucoma. Nat Genet. 2016;48:189–94.

    Article  CAS  PubMed Central  Google Scholar 

  72. Fingert JH, Robin AL, Stone JL, et al. Copy number variations on chromosome 12q14 in patients with normal tension glaucoma. Hum Mol Genet. 2011;20:2482–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Minegishi Y, Iejima D, Kobayashi H, et al. Enhanced optineurin E50K-TBK1 interaction evokes protein insolubility and initiates familial primary open-angle glaucoma. Hum Mol Genet. 2013;22:3559–67.

    Article  CAS  PubMed  Google Scholar 

  74. Rezaie T, Child A, Hitchings R, et al. Adult-onset primary open-angle glaucoma caused by mutations in optineurin. Science. 2002;295:1077–9.

    Article  CAS  PubMed  Google Scholar 

  75. Harrington DO. The pathogenesis of the glaucoma field: clinical evidence that circulatory insufficiency in the optic nerve is the primary cause of visual field loss in glaucoma. Am J Ophthalmol. 1959;47:177–85.

    Article  CAS  PubMed  Google Scholar 

  76. Haas JS. Low tension glaucoma. Trans Pac Coast Otoophthalmol Soc Annu Meet. 1962;43:153–60.

    CAS  PubMed  Google Scholar 

  77. Chung HS, Harris A, Kagemann L, Martin B. Peripapillary retinal blood flow in normal tension glaucoma. Br J Ophthalmol. 1999;83:466–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Anderson DR. Glaucoma, capillaries and pericytes: 1. Blood flow regulation. Ophthalmologica. 1996;210:257–62.

    Article  CAS  PubMed  Google Scholar 

  79. Johnson DG, Drance SM. Some studies on the circulation in patients with advanced open angle glaucoma. Can J Ophthalmol. 1968;3:149–53.

    CAS  PubMed  Google Scholar 

  80. Tielsch JM, Katz J, Sommer A, et al. Hypertension, perfusion pressure and primary open-angle glaucoma. A population-based assessment. Arch Ophthalmol. 1995;113:216–21.

    Article  CAS  PubMed  Google Scholar 

  81. Leske MC, Wu SY, Nemesure B, et al. Incident open-angle glaucoma and blood pressure. Arch Ophthalmol. 2002;120:954–9.

    Article  PubMed  Google Scholar 

  82. Choi J, Jeong J, Cho H, Kook MS. Effect of nocturnal blood pressure reduction on circadian fluctuation of mean ocular perfusion pressure: a risk factor for normal tension glaucoma. Invest Ophthalmol Vis Sci. 2006;47:831–6.

    Article  PubMed  Google Scholar 

  83. Leske MC. Ocular perfusion pressure and glaucoma: clinical trial and epidemiological findings. Curr Opin Ophthalmol. 2009;20:73–8.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Mroczkowska S, Ekart A, Sung V, et al. Coexistence of macro- and micro-vascular abnormalities in newly diagnosed normal tension glaucoma patients. Acta Ophthalmol. 2012;90:e553–9.

    Article  PubMed  Google Scholar 

  85. Morgan WH, Yu DY, Alder VA, et al. The correlation between the cerebrospinal fluid pressure and retrolaminar tissue pressure. Invest Ophthalmol Vis Sci. 1998;39:1419–28.

    CAS  PubMed  Google Scholar 

  86. Morgan WH, Yu DY, Cooper RL, et al. The influence of cerebrospinal fluid pressure on the lamina cribrosa tissue pressure gradient. Invest Ophthalmol Vis Sci. 1995;36:1163–72.

    CAS  PubMed  Google Scholar 

  87. Wang N, Xie X, Yang D, et al. Orbital cerebrospinal fluid space in glaucoma: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Ophthalmology. 2012;119:2065–73.e1.

    Article  PubMed  Google Scholar 

  88. Ren R, Jonas JB, Tian G, et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology. 2010;117:259–66.

    Article  PubMed  Google Scholar 

  89. Wong VH, Bui BV, Vingrys AJ. Clinical and experimental links between diabetes and glaucoma. Clin Exp Optom. 2011;94:4–23.

    Article  PubMed  Google Scholar 

  90. Schofield JD, Liu Y, Rao-Balakrishna P, et al. Diabetes dyslipidemia. Diabetes Ther. 2016;7:203–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Chapman MJ, Ginsberg HN, Amarenco P, et al. Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol in patients at high risk of cardiovascular disease: evidence and guidance for management. Eur Heart J. 2011;32:1345–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Baigent C, Keech A, Kearney PM, et al. Efficacy and safety of cholesterol-lowering treatment: prospective meta-analysis of data from 90,056 participants in 14 randomised trials of statins. Lancet. 2005;366:1267–78.

    Article  CAS  PubMed  Google Scholar 

  93. Cholesterol Treatment Trialists Collaborators, Kearney PM, Blackwell L, et al. Efficacy of cholesterol-lowering therapy in 18,686 people with diabetes in 14 randomised trials of statins: a meta-analysis. Lancet. 2008;371:117–25.

    Article  CAS  Google Scholar 

  94. Pietri AO, Dunn FL, Grundy SM, Raskin P. The effect of continuous subcutaneous insulin infusion on very-low-density lipoprotein triglyceride metabolism in type I diabetes mellitus. Diabetes. 1983;32:75–81.

    Article  CAS  PubMed  Google Scholar 

  95. Tames FJ, Mackness MI, Arrol S, et al. Non-enzymatic glycation of apolipoprotein B in the sera of diabetic and non-diabetic subjects. Atherosclerosis. 1992;93:237–44.

    Article  CAS  PubMed  Google Scholar 

  96. Huang YS, Horrobin DF, Manku MS, et al. Tissue phospholipid fatty acid composition in the diabetic rat. Lipids. 1984;19:367–70.

    Article  CAS  PubMed  Google Scholar 

  97. Ruiz-Gutierrez V, Stiefel P, Villar J, et al. Cell membrane fatty acid composition in type 1 (insulin-dependent) diabetic patients: relationship with sodium transport abnormalities and metabolic control. Diabetologia. 1993;36:850–6.

    Article  CAS  PubMed  Google Scholar 

  98. Ghebremeskel K, Thomas B, Lowy C, et al. Type 1 diabetes compromises plasma arachidonic and docosahexaenoic acids in newborn babies. Lipids. 2004;39:335–42.

    Article  CAS  PubMed  Google Scholar 

  99. Toda N, Nakanishi-Toda M. Nitric oxide: ocular blood flow, glaucoma and diabetic retinopathy. Prog Retin Eye Res. 2007;26:205–38.

    Article  CAS  PubMed  Google Scholar 

  100. Zheng L, Kern TS. Role of nitric oxide, superoxide, peroxynitrite, and PARP in diabetic retinopathy. Front Biosci (Landmark Ed). 2009;14:3974–87.

    Article  CAS  Google Scholar 

  101. Cavet ME, Vittitow JL, Impagnatiello F, et al. Nitric oxide (NO): an emerging target for the treatment of glaucoma. Invest Ophthalmol Vis Sci. 2014;55:5005–15.

    Article  CAS  PubMed  Google Scholar 

  102. Husain S, Abdul Y, Singh S, et al. Regulation of nitric oxide production by δ-opioid receptors during glaucomatous injury. PLoS One. 2014;9:e110397.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Hara MR, Agrawal N, Kim SF. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol. 2005;7:665–74.

    Article  CAS  PubMed  Google Scholar 

  104. Goldstein IM, Ostwald P, Roth S. Nitric oxide: a review of its role in retinal function and disease. Vision Res. 1996;36:2979–94.

    Article  CAS  PubMed  Google Scholar 

  105. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 2007;87:315–424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Alexander JP, Acott TS. Involvement of protein kinase C in TNFalpha regulation of trabecular matrix metalloproteinases and TIMPs. Invest Ophthalmol Vis Sci. 2001;42:2831–38.

    CAS  PubMed  Google Scholar 

  107. Kuehn MH, Fingert JH, Kwon YH. Retinal ganglion cell death in glaucoma: mechanisms and neuroprotective strategies. Ophthalmol Clin North Am. 2005;18:383–95.

    Article  PubMed  Google Scholar 

  108. Sivak JM, Fini ME. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog Retin Eye Res. 2002;21:1–14.

    Article  CAS  PubMed  Google Scholar 

  109. Nagayach A, Patro N, Patro I. Experimentally induced diabetes causes glial activation, glutamate toxicity and cellular damage leading to changes in motor function. Front Cell Neurosci. 2014;8:355.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Coleman E, Judd R, Hoe L, et al. Effects of diabetes mellitus on astrocyte GFAP and glutamate transporters in the CNS. Glia. 2004;48:166–72.

    Article  PubMed  Google Scholar 

  111. Sandireddy R, Yerra VG, Areti A, et al. Neuroinflammation and oxidative stress in diabetic neuropathy: futuristic strategies based on these targets. Int J Endocrinol. 2014;2014:674987.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Scholz J, Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. 2007;10:1361–8.

    Article  CAS  PubMed  Google Scholar 

  113. Morgan JE. Optic nerve head structure in glaucoma: astrocytes as mediators of axonal damage. Eye (Lond). 2000;14:437–44.

    Article  Google Scholar 

  114. Ju WK, Kim KY, Lindsey JD, et al. Intraocular pressure elevation induces mitochondrial fission and triggers OPA1 release in glaucomatous optic nerve. Invest Ophthalmol Vis Sci. 2008;49:4903–11.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Chong RS, Martin KR. Glial cell interactions and glaucoma. Curr Opin Ophthalmol. 2015;26:73–7.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Tomlinson DR, Fernyhough P, Diemel LT. Role of neurotrophins in diabetic neuropathy and treatment with nerve growth factors. Diabetes. 1997;46 Suppl 2:S43–9.

    Article  CAS  PubMed  Google Scholar 

  117. Fernyhough P, Diemel LT, Tomlinson DR. Target tissue production and axonal transport of neurotrophin-3 are reduced in streptozotocin-diabetic rats. Diabetologia. 1998;41:300–6.

    Article  CAS  PubMed  Google Scholar 

  118. Zhang L, Ino-ue M, Dong K, et al. Retrograde axonal transport impairment of large- and medium-sized retinal ganglion cells in diabetic rat. Curr Eye Res. 2000;20:131–6.

    Article  CAS  PubMed  Google Scholar 

  119. Ino-Ue M, Zhang L, Naka H, et al. Polyol metabolism of retrograde axonal transport in diabetic rat large optic nerve fiber. Invest Ophthalmol Vis Sci. 2000;41:4055–8.

    CAS  PubMed  Google Scholar 

  120. Rudzinski M, Wong TP, Saragovi HU. Changes in retinal expression of neurotrophins and neurotrophin receptors induced by ocular hypertension. J Neurobiol. 2004;58:341–54.

    Article  CAS  PubMed  Google Scholar 

  121. Faiq MA, Dada R, Saluja D, et al. Glaucoma—diabetes of the brain: a radical hypothesis about its nature and pathogenesis. Med Hypotheses. 2014;82:535–46.

    Article  CAS  PubMed  Google Scholar 

  122. Cheng CM, Reinhardt RR, Lee WH, et al. Insulin-like growth factor 1 regulates developing brain glucose metabolism. Proc Natl Acad Sci U S A. 2000;97:10236–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Bingham EM, Hopkins D, Smith D, et al. The role of insulin in human brain glucose metabolism: an 18fluoro deoxyglucose positron emission tomography study. Diabetes. 2002;51:3384–90.

    Article  CAS  PubMed  Google Scholar 

  124. Ott A, Stolk RP, van Harskamp F, et al. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology. 1999;53:1937–42.

    Article  CAS  PubMed  Google Scholar 

  125. Ballotti R, Nielsen FC, Pringle N, et al. Insulin-like growth factor 1 in cultured rat astrocytes: expression of the gene, and receptor tyrosine kinase. EMBO J. 1987;6:3633–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Meyer-Franke A, Kaplan MR, Pfrieger FW, et al. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron. 1995;15:805–19.

    Article  CAS  PubMed  Google Scholar 

  127. Fischer AJ, Dierks BD, Reh TA. Exogenous growth factors induce the production of ganglion cells at the retinal margin. Development. 2002;129:2283–91.

    CAS  PubMed  Google Scholar 

  128. Hepburn DA, Fisher BM, Thomson I, et al. Autonomic mechanisms underlying intraocular pressure changes during insulin-induced hypoglycaemia in normal human subjects: effects of pharmacological blockade. Clin Sci (Lond). 1991;80:333–8.

    Article  CAS  Google Scholar 

  129. van Dijk HW, Verbraak FD, Stehouwer M, et al. Association of visual function and ganglion cell layer thickness in patients with diabetes mellitus type 1 and no or minimal diabetic retinopathy. Vision Res. 2011;51:224–8.

    Article  PubMed  Google Scholar 

  130. Lin HC, Stein JD, Nan B, et al. Association of geroprotective effects of metformin and risk of open-angle glaucoma in persons with diabetes mellitus. JAMA Ophthalmol. 2015;133:915–23.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Shen L, Walter S, Melles RB, et al. Diabetes pathology and risk of primary open-angle glaucoma: evaluating causal mechanisms by using genetic information. Am J Epidemiol. 2016;183:147–55.

    Article  PubMed  Google Scholar 

  132. Sebag J, Thomas JV, Epstein DL, et al. Optic disc cupping in arteritic AION resembles glaucomatous cupping. Ophthalmology. 1986;93:357–61.

    Article  CAS  PubMed  Google Scholar 

  133. Quigley H, Anderson DR. Cupping of the optic disc in ischemic optic neuropathy. Trans Am Acad Ophthalmol Otolaryngol. 1977;83:755–62.

    CAS  Google Scholar 

  134. Piette SD, Sergott RC. Pathological optic-disc cupping. Curr Opin Ophthalmol. 2006;17:1–6.

    Article  PubMed  Google Scholar 

  135. Lim MC, Tanimoto SA, Furlani BA, et al. Effect of diabetic retinopathy and panretinal photocoagulation on retinal nerve fiber layer and optic nerve appearance. Arch Ophthalmol. 2009;127:857–62.

    Article  PubMed  Google Scholar 

  136. Bui BV, Loeliger M, Thomas M, et al. Investigating structural and biochemical correlates of ganglion cell dysfunction in streptozotocin-induced diabetic rats. Exp Eye Res. 2009;88:1076–83.

    Article  CAS  PubMed  Google Scholar 

  137. Antonetti DA, JDRF Diabetic Retinopathy Center Group, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006;55:2401–11.

    Article  CAS  PubMed  Google Scholar 

  138. Stem MS, Gardner TW. Neurodegeneration in the pathogenesis of diabetic retinopathy: molecular mechanisms and therapeutic implications. Curr Med Chem. 2013;20:3241–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. 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 U S A. 2016;113:E2655–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. van Dijk HW, Kok PH, Garvin M, et al. Selective loss of inner retinal layer thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthalmol Vis Sci. 2009;50:3404–9.

    Article  PubMed  PubMed Central  Google Scholar 

  141. van Dijk HW, Verbraak FD, Kok PH, et al. Decreased retinal ganglion cell layer thickness in type 1 diabetic patients. Invest Ophthalmol Vis Sci. 2010;51:3660–5.

    Article  PubMed  PubMed Central  Google Scholar 

  142. Peng PH, Lin HS, Lin S. Nerve fibre layer thinning in patients with preclinical retinopathy. Can J Ophthalmol. 2009;44:417–22.

    Article  PubMed  Google Scholar 

  143. Sugimoto M, Sasoh M, Ido M, et al. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica. 2005;219:379–85.

    Article  PubMed  Google Scholar 

  144. Yücel YH, Zhang Q, Weinreb RN, et al. Effect of retinal ganglion cell loss on magno-, parvo-, koniocellular pathways in the lateral geniculate nucleus and visual cortex in glaucoma. Prog Retin Eye Res. 2003;22:465–81.

    Article  PubMed  Google Scholar 

  145. Yücel YH, Zhang Q, Gupta N, et al. Loss of neurons in magnocellular and parvocellular layers of the lateral geniculate nucleus in glaucoma. Arch Ophthalmol. 2000;118(3):378–84.

    Article  PubMed  Google Scholar 

  146. Quigley HA, Nickells RW, Kerrigan LA, et al. Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis. Invest Ophthalmol Vis Sci. 1995;36:774–86.

    CAS  PubMed  Google Scholar 

  147. Meyer-Rusenberg B, Pavlidis M, Stupp T, et al. Pathological changes in human retinal ganglion cells associated with diabetic and hypertensive retinopathy. Graefes Arch Clin Exp Ophthalmol. 2007;245:1009–18.

    Article  PubMed  Google Scholar 

  148. Moura AL, Raza AS, Lazow MA, et al. Retinal ganglion cell and inner plexiform layer thickness measurements in regions of severe visual field sensitivity loss in patients with glaucoma. Eye (Lond). 2012;26:1188–93.

    Article  Google Scholar 

  149. Harwerth RS, Carter-Dawson L, Shen F, et al. Ganglion cell losses underlying visual field defects from experimental glaucoma. Invest Ophthalmol Vis Sci. 1999;40:2242–50.

    CAS  PubMed  Google Scholar 

  150. Harwerth RS, Crawford ML, Frishman LJ, et al. Visual field defects and neural losses from experimental glaucoma. Prog Retin Eye Res. 2002;21:91–125.

    Article  PubMed  Google Scholar 

  151. Coupland SG. A comparison of oscillatory potential and pattern electroretinogram measures in diabetic retinopathy. Doc Ophthalmol. 1987;66:207–18.

    Article  CAS  PubMed  Google Scholar 

  152. Bresnick GH, Palta M. Oscillatory potential amplitudes. Relation to severity of diabetic retinopathy. Arch Ophthalmol. 1987;105:929–33.

    Article  CAS  PubMed  Google Scholar 

  153. Holopigian K, Seiple W, Lorenzo M, et al. A comparison of photopic and scotopic electroretinographic changes in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 1992;33:2773–80.

    CAS  PubMed  Google Scholar 

  154. Sakai H, Tani Y, Shirasawa E, et al. Development of electroretinographic alterations in streptozotocin-induced diabetes in rats. Ophthalmic Res. 1995;27:57–63.

    Article  CAS  PubMed  Google Scholar 

  155. Shinoda K, Rejdak R, Schuettauf F, et al. Early electroretinographic features of streptozotocin-induced diabetic retinopathy. Clin Exp Ophthalmol. 2007;35:847–54.

    Article  PubMed  Google Scholar 

  156. Moore-Dotson JM, Beckman JJ, Mazade RE, et al. Early retinal neuronal dysfunction in diabetic mice: reduced light-evoked inhibition increases rod pathway signaling. Invest Ophthalmol Vis Sci. 2016;47:1418–30.

    Article  CAS  Google Scholar 

  157. Parisi V, Uccioli L. Visual electrophysiological responses in persons with type 1 diabetes. Diabetes Metab Res Rev. 2001;17:12–8.

    Article  CAS  PubMed  Google Scholar 

  158. Viswanathan S, Frishman LJ, Robson JG. The uniform field and pattern ERG in macaques with experimental glaucoma: removal of spiking activity. Invest Ophthalmol Vis Sci. 2000;41:2797–810.

    CAS  PubMed  Google Scholar 

  159. Rangaswamy NV, Frishman LJ, Dorotheo EU, et al. Photopic ERGs in patients with optic neuropathies: comparison with primate ERGs after pharmacologic blockade of inner retina. Invest Ophthalmol Vis Sci. 2004;45:3827–37.

    Article  PubMed  Google Scholar 

  160. Rangaswamy NV, Zhou W, Harwerth RS. Effect of experimental glaucoma in primates on oscillatory potentials of the slow-sequence mfERG. Invest Ophthalmol Vis Sci. 2006;47:753–67.

    Article  PubMed  PubMed Central  Google Scholar 

  161. Hood DC, Xu L, Thienprasiddhi P, et al. The pattern electroretinogram in glaucoma patients with confirmed visual field deficits. Invest Ophthalmol Vis Sci. 2005;46:2411–8.

    Article  PubMed  Google Scholar 

  162. Kang JH, Loomis SJ, Rosner BA, et al. Comparison of risk factor profiles for primary open-angle glaucoma subtypes defined by pattern of visual field loss: a prospective study. Invest Ophthalmol Vis Sci. 2015;56:2439–48.

    Article  PubMed  PubMed Central  Google Scholar 

  163. Kim JM, Kyung H, Shim SH, et al. Location of visual field defects in glaucoma and their modes of deterioration. Invest Ophthalmol Vis Sci. 2015;56:7956–62.

    Article  PubMed  PubMed Central  Google Scholar 

  164. Nathan DM, Zinman B, Cleary PA, et al. Modern-day clinical course of type 1 diabetes mellitus after 30 years’ duration: the diabetes control and complications trial/epidemiology of diabetes interventions and complications and Pittsburgh epidemiology of diabetes complications experience (1983–2005). Arch Intern Med. 2009;169(14):1307–16.

    Article  PubMed  PubMed Central  Google Scholar 

  165. Hovind P, Tarnow L, Rossing K, et al. Decreasing incidence of severe diabetic microangiopathy in type 1 diabetes. Diabetes Care. 2003;26(4):1258–64.

    Article  PubMed  Google Scholar 

  166. Nordwall M, Bojestig M, Arnqvist HJ, Ludvigsson J. Declining incidence of severe retinopathy and persisting decrease of nephropathy in an unselected population of type 1 diabetes—the Linkoping Diabetes Complications Study. Diabetologia. 2004;47:1266–72.

    Article  CAS  PubMed  Google Scholar 

  167. Fante RJ, Gardner TW, Sundstrom JM. Current and future management of diabetic retinopathy: a personalized evidence-based approach. Diabetes Manag (Lond). 2013;3:481–94.

    Article  CAS  Google Scholar 

  168. Klein R, Knudtson MD, Lee KE, et al. The Wisconsin Epidemiologic Study of Diabetic Retinopathy: XXII the twenty-five-year progression of retinopathy in persons with type 1 diabetes. Ophthalmology. 2008;115:1859–68.

    Article  PubMed  PubMed Central  Google Scholar 

  169. Yau JW, Rogers SL, Kawasaki R, Meta-Analysis for Eye Disease (META-EYE) Study Group, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35:556–64.

    Article  PubMed  PubMed Central  Google Scholar 

  170. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med. 1993;329:977–86.

  171. Abbate M, Cravedi P, Iliev I, et al. Prevention and treatment of diabetic retinopathy: evidence from clinical trials and perspectives. Curr Diabetes Rev. 2011;7:190–200.

    Article  CAS  PubMed  Google Scholar 

  172. Standards of medical care in diabetes—2016: cardiovascular disease and risk management. Diabetes Care. 2016;39 Suppl 1:S60-71.

  173. Dielemans I, Vingerling JR, Algra D, et al. Primary open-angle glaucoma, intraocular pressure, and systemic blood pressure in the general elderly population. The Rotterdam Study. Ophthalmology. 1995;102:54–60.

    Article  CAS  PubMed  Google Scholar 

  174. Mitchell P, Lee AJ, Rochtchina E, et al. Open-angle glaucoma and systemic hypertension: The Blue Mountains Eye Study. J Glaucoma. 2004;13:319–26.

    Article  PubMed  Google Scholar 

  175. Bonomi L, Marchini G, Marraffa M, et al. Vascular risk factors for primary open angle glaucoma: the Egna-Neumarkt Study. Ophthalmology. 2000;107:1287–93.

    Article  CAS  PubMed  Google Scholar 

  176. Leske MC, Connell AM, Wu SY, et al. Risk factors for open-angle glaucoma: The Barbados Eye Study. Arch Ophthalmol. 1995;113:918–24.

    Article  CAS  PubMed  Google Scholar 

  177. Leske MC, Wu SY, Hennis A, et al. Risk factors for incident open-angle glaucoma: the Barbados Eye Studies. Ophthalmology. 2008;115:85–9.

    Article  PubMed  Google Scholar 

  178. Leske MC, Heijl A, Hyman L, EMGT Group, et al. Predictors of long-term progression in the Early Manifest Glaucoma Trial. Ophthalmology. 2007;114:1965–72.

    Article  PubMed  Google Scholar 

  179. Memarzadeh F, Ying-Lai M, Chung J, et al. Blood pressure, perfusion pressure and open angle glaucoma: The Los Angeles Latino Eye Study. Invest Ophthalmol Vis Sci. 2010;51:2872–7.

    Article  PubMed  PubMed Central  Google Scholar 

  180. Bae HW, Lee N, Lee HS, et al. Systemic hypertension as a risk factor for open-angle glaucoma: a meta-analysis of population-based studies. PLoS One. 2014;9:e108226.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  181. Wu SY, Leske MC. Associations with intraocular pressure in the Barbados Eye Study. Arch Ophthalmol. 1997;115:1572–6.

    Article  CAS  PubMed  Google Scholar 

  182. Klein BEK, Klein R, Knudtson MD. Intraocular pressure and systemic blood pressure: longitudinal perspective: the Beaver Dam Eye Study. Br J Ophthalmol. 2005;89:284–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Bulpitt CJ, Hodes C, Everitt MG. Intraocular pressure and systemic blood pressure in the elderly. Br J Ophthalmol. 1975;59:717–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Kahn HA, Leibowitz HM, Ganley JP, et al. The Framingham Eye Study. II. Association of ophthalmic pathology with single variables previously measured in the Framingham Heart Study. Am J Epidemiol. 1977;106:33–41.

    CAS  PubMed  Google Scholar 

  185. Klein BE, Klein R. Intraocular pressure and cardiovascular risk variables. Arch Ophthalmol. 1981;99:837–9.

    Article  CAS  PubMed  Google Scholar 

  186. Klein BE, Klein R, Linton KL. Intraocular pressure in an American community. The Beaver Dam Eye Study. Invest Ophthalmol Vis Sci. 1992;33:2224–8.

    CAS  PubMed  Google Scholar 

  187. Foster PJ, Machin D, Wong TY, et al. Determinants of intraocular pressure and its association with glaucomatous optic neuropathy in Chinese Singaporeans: the Tanjong Pagar Study. Invest Ophthalmol Vis Sci. 2003;44:3885–91.

    Article  PubMed  Google Scholar 

  188. Tan GS, Wong TY, Fong CW, et al. Diabetes, metabolic abnormalities, and glaucoma. Acta Ophthalmol. 2009;127:1354–61.

    CAS  Google Scholar 

  189. Yokomichi H, Kashiwagi K, Kitamura K, et al. Evaluation of the associations between changes in intraocular pressure and metabolic syndrome parameters: a retrospective cohort in Japan. BMJ Open. 2016;6:e010360.

    Article  PubMed  PubMed Central  Google Scholar 

  190. Kim YH, Jung SW, Nam GE, et al. High intraocular pressure is associated with cardiometabolic risk factors in South Korean men: Korean National Health and Nutrition Examination Survey, 2008–2010. Eye (Lond). 2014;28:672–9.

    Article  CAS  Google Scholar 

  191. Wygnaski-Jaffe T, Bieran I, Tekes-Manova D, et al. Metabolic syndrome: a risk factor for high intraocular pressure in the Israeli population. Int J Ophthalmol. 2015;8:403–6.

    Google Scholar 

  192. Wang S, Xu L, Jonas JB, et al. Dyslipidemia and eye diseases in the adult Chinese population: the Beijing eye study. PLoS One. 2012;7:e26871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Kang JH, Pasquale LR, Willett WC, et al. Dietary fat consumption and primary open-angle glaucoma. Am J Clin Nutr. 2004;79:755–64.

    CAS  PubMed  Google Scholar 

  194. Alberti KGMM, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–5.

    Article  CAS  PubMed  Google Scholar 

  195. Vassallo P, Driver SL, Stone NJ. Metabolic syndrome: an evolving clinical construct. Prog Cardiovasc Dis. 2016. doi:10.1016/j.pcad.2016.07.012.

    PubMed  Google Scholar 

  196. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes. 1988;37:1595–607.

    Article  CAS  PubMed  Google Scholar 

  197. Newman-Casey PA, Talwar N, Nan B, et al. The relationship between components of metabolic syndrome and open-angle glaucoma. Ophthalmology. 2011;118:1318–26.

    PubMed  PubMed Central  Google Scholar 

  198. Stein JD, Newman-Casey PA, Talwar N, et al. The relationship between statin use and open-angle glaucoma. Ophthalmology. 2012;119:2074–81.

    Article  PubMed  PubMed Central  Google Scholar 

  199. Yildiz P, Kebapci MN, Mutlu F, et al. Intraocular pressure changes during oral glucose tolerance tests in diabetic and non-diabetic individuals. Exp Clin Endocrinol Diabetes. 2016;124:385–8.

    Article  CAS  PubMed  Google Scholar 

  200. Kim M, Jeong JW, Park KH, et al. Metabolic syndrome as a risk factor in normal-tension glaucoma. Acta Ophthalmol. 2014;92:e637–43.

    Article  PubMed  Google Scholar 

  201. Tan GS, Wong TY, Fong C-W, et al. Diabetes, metabolic abnormalities, and glaucoma. Arch Ophthalmol. 2009;127:1354–61.

    Article  CAS  PubMed  Google Scholar 

  202. Lin HC, Stein JD, Nan B, et al. Association of geroprotective effects of metformin and risk of open-angle glaucoma in persons with diabetes mellitus. JAMA Ophthalmol. 2015;133:915–23. This study utilizes a large health claims data set to demonstrate that open-angle glaucoma risk may be augmented by medication type in diabetic patients, specifically the possible protective role of metformin even after controlling for other confounding effects, such as glycemic control.

    Article  PubMed  PubMed Central  Google Scholar 

  203. Dielemans I, de Jong PT, Stolk R, et al. Primary open angle glaucoma, intraocular pressure, and diabetes mellitus in the general elderly population. The Rotterdam Study. Ophthalmology. 1996;103:1271–5.

    Article  CAS  PubMed  Google Scholar 

  204. Tielsch JM, Katz J, Quigley HA, et al. Diabetes, intraocular pressure, and primary open-angle glaucoma in the Baltimore Eye Survey. Ophthalmology. 1995;102:48–53.

    Article  CAS  PubMed  Google Scholar 

  205. De Voogd S, Ikram MK, Wolfs RC, et al. Is diabetes mellitus a risk factor for open-angle glaucoma? The Rotterdam Study. Ophthalmology. 2006;113:1827–31.

    Article  PubMed  Google Scholar 

  206. Chopra V, Varma R, Francis BA, et al. Type 2 diabetes mellitus and the risk of open-angle glaucoma: the Los Angeles Latino Eye Study. Ophthalmology. 2008;115:227–32.

    Article  PubMed  Google Scholar 

  207. Graw J, Welzl G, Ahmad N, et al. The KORA Eye Study: a population-based study on eye diseases in Southern Germany (KORA F4). Invest Ophthalmol Vis Sci. 2011;52:7778–86.

    Article  PubMed  Google Scholar 

  208. Ellis JD, Evans JM, Ruta DA, et al. Glaucoma incidence in an unselected cohort of diabetic patients: is diabetes mellitus a risk factor for glaucoma? DARTS/MEMO collaboration. Diabetes Audit and Research in Tayside Study. Medicines Monitoring Unit. Br J Ophthalmol. 2000;84:1218–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Wise LA, Rosenberg L, Radin RG, et al. A prospective study of diabetes, lifestyle factors, and glaucoma among African-American women. Ann Epidemiol. 2011;21:430–39.

    Article  PubMed  PubMed Central  Google Scholar 

  210. Gordon MO, Beiser JA, Brandt JD, et al. The Ocular Hypertension Treatment Study: base-line factors that predict the onset of primary open-angle glaucoma. Arch Ophthalmol. 2002;120:714–20.

    Article  PubMed  Google Scholar 

  211. Gordon MO, Beiser JA, Kass MA, Ocular Hypertension Treatment Study Group. Is a history of diabetes mellitus protective against developing open-angle glaucoma? Arch Ophthalmolol. 2008;126:280–1.

    Article  Google Scholar 

  212. Goldacre MJ, Wotton CJ, Keenan TD. Risk of selected eye diseases in people admitted to the hospital for hypertension or diabetes mellitus: record linkage studies. Br J Ophthalmol. 2012;96:872–6.

    Article  PubMed  Google Scholar 

  213. Varma R, Lee PP, Goldberg I, et al. An assessment of the health and economic burdens of glaucoma. Am J Ophthalmol. 2011;152:515–22.

    Article  PubMed  PubMed Central  Google Scholar 

  214. Nielsen NV. The prevalence of glaucoma and ocular hypertension in type 1 and 2 diabetes mellitus. Acta Ophthalmol. 1983;61:662–72.

    Article  CAS  Google Scholar 

  215. Vyas U, Khandekar R, Trivedi N, et al. Magnitude and determinants of ocular morbidities among persons with diabetes in a project in Ahmedabad, India. Diabetes Technol Ther. 2009;11:601–7.

    Article  PubMed  Google Scholar 

  216. Orcutt J, Avakian A, Koepsell TD, et al. Eye disease in veterans with diabetes. Diabetes Care. 2004;27 Suppl 2:B50–3.

    Article  PubMed  Google Scholar 

  217. Dharmadhikari S, Lohiya K, Chelkar V, et al. Magnitude and determinants of glaucoma in type II diabetics: a hospital based cross-sectional study in Maharashtra. India Oman J Ophthalmol. 2015;8:19–23.

    Article  PubMed  Google Scholar 

  218. Mengesha AY. Spectrum of eye disorders among diabetes mellitus patients in Gaborone. Botswana Trop Doct. 2006;36:109–11.

    Article  PubMed  Google Scholar 

  219. Khandekar R, Zutshi R. Glaucoma among Omani diabetic patients: a cross-sectional descriptive study: (Oman diabetic eye study 2002). Eur J Ophthalmol. 2004;14:19–25.

    CAS  PubMed  Google Scholar 

  220. Standards of medical care in diabetes—2016: microvascular complications and foot care. Diabetes Care. 2016;39 Suppl 1:S72-80.

  221. Lee DJ, Kumar N, Feuer WJ, et al. Dilated eye examination screening guideline compliance among patients with diabetes without a diabetic retinopathy diagnosis: the role of geographic access. BMJ Open Diabetes Res Care. 2014;2:e000031.

    Article  PubMed  PubMed Central  Google Scholar 

  222. Olayiwola JN, Sobieraj DM, Kulowski K, et al. Improving diabetic retinopathy screening through a statewide telemedicine program at a large federally qualified health center. J Health Care Poor Underserved. 2011;22:804–16.

    Article  CAS  PubMed  Google Scholar 

  223. Moyer VA, U.S. Preventive Services Task Force. Screening for glaucoma: U.S. Preventive Services Task Force Recommendation Statement. Ann Intern Med. 2013;159:484–89.

    PubMed  Google Scholar 

  224. Joint comments of the American Academy of Ophthalmology and the American Glaucoma Society on the U.S. Preventive Services Task Force. Screening for Glaucoma: Draft Recommendation Statement. AHRQ Publication No. 13-05182-EF-2.

  225. Parrish 2nd RK. Reframing the US Preventive Services Task Force recommendations on screening for glaucoma. Am J Ophthalmol. 2014;158:860–2.

    Article  PubMed  Google Scholar 

  226. Lee PP, Walt JG, Doyle JJ, et al. A multicenter, retrospective pilot study of resource use and costs associated with severity of disease in glaucoma. Arch Ophthalmol. 2006;124:12–9.

    Article  PubMed  Google Scholar 

  227. Lee PP, Kelly SP, Mills RP, et al. Glaucoma in the United States and Europe: predicting costs and surgical rates based upon stage of disease. J Glaucoma. 2007;16:471–8.

    Article  PubMed  Google Scholar 

  228. Heijl A, Leske MC, Bengtsson B, et al. Reduction of intraocular pressure and glaucoma progression: results from the Early Manifest Glaucoma Trial. Arch Ophthalmol. 2002;120:1268–79.

    Article  PubMed  Google Scholar 

  229. Ladapo JA, Kymes SM, Ladapo JA, Nwosu VC, Pasquale LR. Projected clinical outcomes of glaucoma screening in African American individuals. Arch Ophthalmol. 2012;130:365–72.

    Article  PubMed  Google Scholar 

  230. Silva PS, Cavallerano JD, Haddad NM, et al. Comparison of nondiabetic retinal findings identified with nonmydriatic fundus photography vs ultrawide field imaging in an ocular telehealth program. JAMA Ophthalmol. 2016;134:330–4. This study of ultrawide field imaging and nonmydriatic fundus photography showed that approximately 20 % of eyes without diabetic retinopathy had other ocular findings on retinal imaging, with more pathologic findings seen in patients who underwent ultrawide field imaging.

    Article  PubMed  Google Scholar 

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Acknowledgments

Supported in part by the Harvard Vision Clinical Scientist Development Program through the National Institute of Health Grant 5K12 EY016335 (Bethesda, MD), the Harvard Glaucoma Center of Excellence (Boston, MA), and the Massachusetts Lions Eye Research Fund (Belmont, MA).

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Correspondence to Brian J. Song.

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Lloyd Paul Aiello has received travel reimbursement from Optos plc (Dunfermline, United Kingdom).

Outside the scope of this work, Louis R. Pasquale is a paid consultant for Novartis and Bausch+Lomb, Inc. He has received travel support to attend Glaucoma Think Tank meetings by the Glaucoma Foundation (New York, NY).

Brian J. Song has no conflicts of interest.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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This article is part of the Topical Collection on Microvascular Complications—Retinopathy

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Song, B.J., Aiello, L.P. & Pasquale, L.R. Presence and Risk Factors for Glaucoma in Patients with Diabetes. Curr Diab Rep 16, 124 (2016). https://doi.org/10.1007/s11892-016-0815-6

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