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 Table of Contents  
REVIEW ARTICLE
Year : 2018  |  Volume : 9  |  Issue : 3  |  Page : 73-77

Systemic Factors Affecting Diabetic Retinopathy


Dr. Mohan's Diabetes Specialties Centre, Madras Diabetes Research Foundation, Chennai, Tamil Nadu, India

Date of Web Publication22-Aug-2018

Correspondence Address:
Dr. Brijendra Kumar Srivastava
Dr. Mohan's Diabetes Specialities Centre, No. 6, Conran Smith Road, Gopalapuram, Chennai - 600 086, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jod.jod_35_17

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  Abstract 


Diabetic retinopathy (DR) is one of the leading causes of preventable blindness in the world. Apart from local pathophysiological changes happening at the level of retina, various systemic factors also play a role in pathogenesis and progression of DR. In this article, we will discuss systemic factors affecting DR such as hyperglycaemia, hypertension, hyperlipidaemia, nephropathy, pregnancy, anaemia and cardiovascular disease, with their association to progression of DR.

Keywords: Diabetes mellitus, diabetic retinopathy, systemic factors


How to cite this article:
Srivastava BK, Ramya B, Prathiba V, Mohan V. Systemic Factors Affecting Diabetic Retinopathy. J Diabetol 2018;9:73-7

How to cite this URL:
Srivastava BK, Ramya B, Prathiba V, Mohan V. Systemic Factors Affecting Diabetic Retinopathy. J Diabetol [serial online] 2018 [cited 2018 Sep 24];9:73-7. Available from: http://www.journalofdiabetology.org/text.asp?2018/9/3/73/239564




  Introduction Top


Diabetic retinopathy (DR) is one of the leading causes of preventable blindness in the world. Amongst the non-communicable diseases, diabetes mellitus is fast becoming a global epidemic, resulting in huge public health burden. Based on 2015 International Diabetes Federation report, India has 69.2 million people with diabetes, which can increase to 123.5 million by 2040.[1] Diabetes mellitus can cause microvascular (retinopathy, neuropathy and nephropathy) and macrovascular (cardiovascular disease [CVD], peripheral arterial disease and cerebrovascular disease) complications. In the Chennai Urban Rural Epidemiology Study (CURES), the overall prevalence of DR was 17.6%, with 20.8% of the known diabetic patients and 5.1% of patients with newly detected diabetes having DR.[2] The prevalence of DR in the Aditya Jyot Diabetic Retinopathy in Urban Mumbai Slums Study was 15.37%.[3] A recent study from Sankara Nethralaya, Chennai, has also shown the prevalence of DR amongst urban diabetic patients (aged >40 years) to be 18%.[4]

The two sight-threatening stages of DR are proliferative diabetic retinopathy (PDR) and diabetic macular oedema (DME). In the CURES, higher glycated haemoglobin (HbA1c), long duration of diabetes, male gender, microalbuminuria and insulin therapy were found to be risk factors of DR.[5] The other associated risk factors are anaemia, lipid abnormalities, systemic hypertension, pregnancy, nephropathy and CVD.[6] In a recent meta-analysis done in type 1 diabetes across different studies and populations, hyperglycaemia was found to be the most consistent risk factor for DR.[7]

Structural and functional alterations occur in both microvascular and neuroglial components of the retina and number of factors are associated with causation and progression of DR. In this review article, we describe the systemic factors affecting DR.


  Hyperglycaemia Top


The Diabetes Control and Complications Trial (DCCT) has shown that, in type 1 diabetes mellitus, intensive glycaemic therapy reduced the risk for DR by 76% (95% CI: 62% to 85%) and its progression by 54% (95% CI: 39% to 66%).[8],[9] In the United Kingdom, Prospective Diabetes Study (UKPDS) which looked at the effect of improved blood glucose on macro- and microvascular complications in type 2 diabetes, the risk of retinopathy was found to reduce by 31% for 1% decrease in HbA1c.[10] In the DCCT, long-term benefits of intensive insulin treatment greatly outweighed the risks of early worsening.[11] Diabetic patients with long duration of diabetes and advanced stage of retinopathy at baseline were more likely to have early worsening of DR.[12]

Glycaemic control from onset of diabetes mellitus is the key to prevent DR and thus its long-term blinding complications. In CURES, for every 2% elevation of HbA1c, the risk for DR increased by factor of 1.7 (95% CI: 1.545–1.980; P < 0.0001) and for every 5-year increase in the duration of diabetes, the risk for DR increased 1.89-fold (95% CI: 1.679–2.135; P < 0.0001).[2] The Action to Control Cardiovascular Risk in Diabetes Follow-On Eye Study found that progression of DR was seen in only 5.8% of intensive glycaemic treatment compared to 12.7% with standard treatment group (P < 0.0001).[13] The Collaborators on Trials of Lowering Glucose group showed that, in more intensive glucose control arm when compared to the less intensive treatment arm, there was significant 13% relative risk reduction of eye events (a composite of requirement for retinal photocoagulation therapy or vitrectomy, development of PDR or progression of DR) (P = 0·04).[14] During hyperglycaemia, major mediators of coagulation-fibrinolytic system such as fibrinogen, antithrombin-III, plasminogen activator inhibitor-1 and von Willebrand factor get altered. Inhibiting the pathways by which these altered mediators get involved in the pathophysiology of DR can serve as potential targets for the development of an adjuvant novel alternative therapy.[15] It is the glycaemic control rather than drugs to achieve it matters for prevalence and progression of DR.


  Hypertension Top


Hypertension in the diabetic individual markedly increases the risk and accelerates the course of cardiac disease, peripheral vascular disease, stroke, retinopathy and nephropathy.[16] Possible mechanisms of hypertension affecting DR are both haemodynamic (impaired autoregulation and hyperperfusion) and vascular endothelial growth factor (VEGF) induced. Hypertension has been found to upregulate VEGF expression in retinal endothelial cells and ocular fluids.[17]

In the UKPDS, patients assigned to tight control (<150/85 mmHg) had a 34% reduction in progression of retinopathy and 47% reduced risk of deterioration in visual acuity of three lines in association with a 10/5 mmHg reduction in blood pressure (BP).[18] Beneficial effect in DR prevention for up to 4–5 years on BP control has been observed.[19] In otherwise quiescent PDR, uncontrolled hypertension has been found to be risk factor for vitreous haemorrhage.[20] In patients with DR and nephropathy, tight control of BP (<130/80 mmHg) delays the progression of retinopathy and nephropathy in addition to reducing cardiovascular morbidity and mortality.[21] The level of BP control is debatable, but nearer to the normal BP levels have a better chance of preventing the onset and progression of DR. The lowering of BP to a normal range is more important than the type of antihypertensive medication used.[17]


  Nephropathy Top


Diabetic nephropathy, characterised by persistent proteinuria of >500 mg/day, is a serious diabetic complication. Many studies have shown association between diabetic nephropathy and DR.[22],[23] In the Japan Diabetes Complications Study, the presence of microalbuminuria and DR was associated with the fastest glomerular filtration rate decline.[24] In another study, DR was found to be risk factor for rapid progression of diabetic nephropathy.[25] The effects of renal transplantation on DR have been studied. Stabilisation of DR was observed at the final follow-up after renal transplantation done for end-stage renal disease due to diabetic nephropathy.[26]

Increased microalbumin levels in the urine (macroalbuminuria: albumin levels of >500 mg of creatinine in urine) are associated with greater prevalence of DR (60.5% vs. 31.0% vs. 14.1%, P < 0.001) in comparison to microalbuminuria (albumin levels of 30–300 mg of serum creatinine in urine) or normal albumin levels in the urine.[27] There was also increased risk of progression of non-PDR to PDR (hazard ratio [HR] = 2.26, 95% CI [CI] = 1.68–3.03) in diabetic patients with nephropathy.[28] It is thus important to assess blood urea, serum creatinine and presence of microalbuminuria in all diabetic patients.


  Hyperlipidaemia Top


Significant association has been found between retinal hard exudates, total cholesterol and low-density lipoprotein (LDL) levels.[29] In CURES, even after adjusting for HbA1c, serum triglycerides maintained a significant association with DR and LDL cholesterol with DME.[30] Total-to-high density lipoprotein cholesterol ratio and LDL cholesterol were found to be independent risk factors for both clinically significant macular oedema and retinal hard exudates.[31]

Serum apolipoprotein (apo) levels are being evaluated as future biomarkers of DR. Apo-B (P < 0.001) and apo-B-to-apo-AI ratio (P < 0.001) have found to be associated with increasing DR severity levels.[32] Another study has shown one-step progression of DR for every 10 mg/dL increase in serum total cholesterol (odds ratio [OR]: 15.65).[33]

The Fenofibrate Intervention and Event Lowering in Diabetes study was done to assess the effect of long-term lipid-lowering therapy with fenofibrate on DR. There was reduced requirement for laser treatment in the fenofibrate group compared to the placebo group (HR: 0.69, 95% CI: 0.56–0.84; P = 0.0002; absolute risk reduction 1.5% [0.7–2.3]). On long-term follow-up for 5 years, fenofibrate group had demonstrated less likely progression of preexisting DR and also DME development.[34] In another study, statin use significantly lowered the risk of DME (OR: 0.33, P = 0.032). The presence of hypertriglyceridaemia 6 months before development of DME was found to be associated with central retinal thickness (OR: 1.52, P = 0.005).[35]


  Anaemia Top


In type 2 diabetes, the prevalence of anaemia was found to be 12.3%.[36] Anaemia is an important risk factor for DR and its progression. Chronic hyperglycaemia results in anaemia by causing erythropoietin unresponsiveness. Haemoglobin level is not only an independent baseline risk factor for DR but also it factitiously reduces the HbA1c levels, resulting in masking of hyperglycaemia. In the Sankara Nethralaya-Diabetic Retinopathy Epidemiology and Molecular Genetics Study, incident DR and DME were found to be associated with the presence of anaemia (OR 1.96 and 10.14, respectively).[33] In diabetic patients with anaemia (haemoglobin <12 g/dl), a higher risk of DR (OR = 2.0, 95% CI 1.2–3.3) was observed when compared with those with normal levels of haemoglobin.(≥12 g/dl).[37]

The ETDRS showed that lower haematocrit was an also important risk factor for high-risk PDR.[6] Anaemia has been found to be an important risk factor for progression of PDR in spite of prompt laser photocoagulation (P < 0.001).[38] The level of haemoglobin should be thus evaluated periodically in diabetic patients and anaemia treated if present.[39]


  Pregnancy Top


Women with diabetes and childbearing potential should be educated about the need for glycaemic control before pregnancy and should participate in effective family planning.[40] Preconception retinal evaluation is necessary for early detection of DR and management of PDR and DME. During the first trimester, an eye examination should be performed with repeat and follow-up visits scheduled depending on the severity of retinopathy.[41] More frequent ophthalmic examination is recommended in pregnant women with long duration of diabetes and who have DR before pregnancy.[42]

Pregnancy increases the short-term risk of DR progression.[43] The risk factors in pregnancy for progression are longer duration of diabetes, poor glycaemic control, greater severity of retinopathy at conception, presence of hypertension and pregnancy itself.[44] Lower haemoglobin has also been found to be important risk factor for DR during pregnancy (P < 0.01).[45] Laser photocoagulation should be done in sight-threatening DR and there is no contraindication in pregnancy. Gestational diabetes mellitus does not pose a major risk of DR due to short-term exposure of retina to hyperglycaemic milieu.[41] The DCCT also showed that pregnancy induced a transient increase in the risk of retinopathy.[46]


  Cardiovascular Disease Top


Many studies have shown a significant association between CVD and DR. In the CURES study, coronary artery disease was found to be significantly higher in the DR group compared to no DR group (11.3% vs. 6.7%; P = 0.007).[47] Patients with type 2 diabetes mellitus with DME or PDR were more likely to have incident CVD (incidence rate ratio, 1.39; 95% CI, 1.16–1.67) and fatal CVD (incidence rate ratio, 2.33; 95% CI, 1.49–3.67) compared with those without DME or PDR.[48] Macrovascular plaque vulnerability and acute coronary syndrome were found to be significantly greater in DR than in non-DR patients. (P = 0.002 and P = 0.004, respectively).[49] Greater estimated insulin sensitivity at baseline predicted lower odds of developing DR (OR: 0.79, 0.64–0.97), PDR (OR: 0.76, 0.57–0.99) and also reduced odds of coronary artery calcium progression (OR: 0.71, 0.60–0.85).[50] In the Singapore Epidemiology of Eye Disease study, aspirin use has not been significantly associated with the presence of DR. It was, however, co-present with more severe form of DR and indicator of diabetic complications (CVD and chronic kidney disease).[51]


  Conclusion Top


DR is a multifactorial retinal disorder. Keeping blood sugar levels (HbA1c of <7%), BP levels (<140/90 mmHg) and lipid levels (Total cholesterol <200 mg/dl, LDL cholesterol <100 mg/dl and triglycerides <150 mg/dl) under control would be beneficial.[52],[53] DR can be asymptomatic and hence lifelong periodic annual retinal examination is important for early detection and prompt treatment of this blinding disease. Many people with diabetes mellitus are unaware that diabetes can affect the retina and cause blindness. They only undergo refraction and miss the important fundus examination. Hence, all physicians should motivate their patients to have periodic retinal evaluation and undergo laser treatment when required. It is also their responsibility to explain the importance of glycaemic control from onset of diagnosis as DR can be silent. Screening facilities for DR should be available for all people with diabetes to increase compliance and prompt management when required. Collaborative efforts between diabetologists, ophthalmologists and dieticians are the need of the hour to help improve quality of life and reduce public health burden due to diabetic-related complications.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
International Diabetes Federation. IDF Diabetes Atlas. 7th ed. Brussels, Belgium: International Diabetes Federation; 2015.  Back to cited text no. 1
    
2.
Rema M, Premkumar S, Anitha B, Deepa R, Pradeepa R, Mohan V, et al. Prevalence of diabetic retinopathy in urban India: The Chennai Urban Rural Epidemiology Study (CURES) eye study, I. Invest Ophthalmol Vis Sci 2005;46:2328-33.  Back to cited text no. 2
    
3.
Sunita M, Singh AK, Rogye A, Sonawane M, Gaonkar R, Srinivasan R, et al. Prevalence of diabetic retinopathy in urban slums: The Aditya Jyot Diabetic Retinopathy in Urban Mumbai slums study-report 2. Ophthalmic Epidemiol 2017;24:303-10.  Back to cited text no. 3
    
4.
Raman R, Rani PK, Reddi Rachepalle S, Gnanamoorthy P, Uthra S, Kumaramanickavel G, et al. Prevalence of diabetic retinopathy in India: Sankara Nethralaya Diabetic Retinopathy Epidemiology and Molecular Genetics Study Report 2. Ophthalmology 2009;116:311-8.  Back to cited text no. 4
    
5.
Pradeepa R, Anitha B, Mohan V, Ganesan A, Rema M. 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;25:536-42.  Back to cited text no. 5
    
6.
Davis MD, Fisher MR, Gangnon RE, Barton F, Aiello LM, Chew EY, et al. Risk factors for high-risk proliferative diabetic retinopathy and severe visual loss: Early treatment diabetic retinopathy study report #18. Invest Ophthalmol Vis Sci 1998;39:233-52.  Back to cited text no. 6
    
7.
Sabanayagam C, Yip W, Ting DS, Tan G, Wong TY. Ten emerging trends in the epidemiology of diabetic retinopathy. Ophthalmic Epidemiol 2016;23:209-22.  Back to cited text no. 7
    
8.
Diabetes Control and Complications Trial Research Group, Nathan DM, Genuth S, Lachin J, Cleary P, Crofford O, et al. 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;329:977-86.  Back to cited text no. 8
    
9.
Rodriguez-Fontal M, Kerrison JB, Alfaro DV, Jablon EP. Metabolic control and diabetic retinopathy. Curr Diabetes Rev 2009;5:3-7.  Back to cited text no. 9
    
10.
Kohner EM. Microvascular disease: What does the UKPDS tell us about diabetic retinopathy? Diabet Med 2008;25 Suppl 2:20-4.  Back to cited text no. 10
    
11.
Early Worsening of Diabetic Retinopathy in the Diabetes Control and Complications Trial. From the diabetes control and complications trial research group, Bethesda, Md. Arch Ophthalmol 1995;113:49-51.  Back to cited text no. 11
    
12.
Dahl-Jørgensen K, Brinchmann-Hansen O, Hanssen KF, Sandvik L, Aagenaes O. Rapid tightening of blood glucose control leads to transient deterioration of retinopathy in insulin dependent diabetes mellitus: The Oslo study. Br Med J (Clin Res Ed) 1985;290:811-5.  Back to cited text no. 12
    
13.
Action to Control Cardiovascular Risk in Diabetes Follow-On (ACCORDION) Eye Study Group and the Action to Control Cardiovascular Risk in Diabetes Follow-On (ACCORDION) Study Group. Persistent effects of intensive glycemic control on retinopathy in type 2 diabetes in the action to control cardiovascular risk in diabetes (ACCORD) follow-on study. Diabetes Care 2016;39:1089-100.  Back to cited text no. 13
    
14.
Zoungas S, Arima H, Gerstein HC, Holman RR, Woodward M, Reaven P, et al. Effects of intensive glucose control on microvascular outcomes in patients with type 2 diabetes: A meta-analysis of individual participant data from randomised controlled trials. Lancet Diabetes Endocrinol 2017;5:431-7.  Back to cited text no. 14
    
15.
Behl T, Velpandian T, Kotwani A. Role of altered coagulation-fibrinolytic system in the pathophysiology of diabetic retinopathy. Vascul Pharmacol 2017;92:1-5.  Back to cited text no. 15
    
16.
Epstein M, Sowers JR. Diabetes mellitus and hypertension. Hypertension 1992;19:403-18.  Back to cited text no. 16
    
17.
Srivastava BK, Rema M. Does hypertension play a role in diabetic retinopathy? J Assoc Physicians India 2005;53:803-8.  Back to cited text no. 17
    
18.
Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. UK Prospective Diabetes Study Group. BMJ 1998;317:703-13.  Back to cited text no. 18
    
19.
Do DV, Wang X, Vedula SS, Marrone M, Sleilati G, Hawkins BS, et al. Blood pressure control for diabetic retinopathy. Cochrane Database Syst Rev 2015;1:CD006127.  Back to cited text no. 19
    
20.
Pesin N, Mandelcorn ED, Felfeli T, Ogilvie RI, Brent MH. The role of occult hypertension in retinal vein occlusions and diabetic retinopathy. Can J Ophthalmol 2017;52 Suppl 1:S30-3.  Back to cited text no. 20
    
21.
McGill JB. Improving microvascular outcomes in patients with diabetes through management of hypertension. Postgrad Med 2009;121:89-101.  Back to cited text no. 21
    
22.
Manaviat MR, Afkhami M, Shoja MR. Retinopathy and microalbuminuria in type II diabetic patients. BMC Ophthalmol 2004;4:9.  Back to cited text no. 22
    
23.
Boelter MC, Gross JL, Canani LH, Costa LA, Lisboa HR, Três GS, et al. Proliferative diabetic retinopathy is associated with microalbuminuria in patients with type 2 diabetes. Braz J Med Biol Res 2006;39:1033-9.  Back to cited text no. 23
    
24.
Moriya T, Tanaka S, Kawasaki R, Ohashi Y, Akanuma Y, Yamada N, et al. Diabetic retinopathy and microalbuminuria can predict macroalbuminuria and renal function decline in Japanese type 2 diabetic patients: Japan Diabetes Complications Study. Diabetes Care 2013;36:2803-9.  Back to cited text no. 24
    
25.
Hung CC, Lin HY, Hwang DY, Kuo IC, Chiu YW, Lim LM, et al. Diabetic retinopathy and clinical parameters favoring the presence of diabetic nephropathy could predict renal outcome in patients with diabetic kidney disease. Sci Rep 2017;7:1236.  Back to cited text no. 25
    
26.
Roy R, Das MK, Pal BP, Ganesan S, Raman R, Sharma T, et al. The effects of renal transplantation on diabetic retinopathy: Clinical course and visual outcomes. Indian J Ophthalmol 2013;61:552-6.  Back to cited text no. 26
[PUBMED]  [Full text]  
27.
Rani PK, Raman R, Gupta A, Pal SS, Kulothungan V, Sharma T, et al. Albuminuria and diabetic retinopathy in type 2 diabetes mellitus Sankara Nethralaya diabetic retinopathy epidemiology and molecular genetic study (SN-DREAMS, report 12). Diabetol Metab Syndr 2011;3:9.  Back to cited text no. 27
    
28.
Jeng CJ, Hsieh YT, Yang CM, Yang CH, Lin CL, Wang IJ, et al. Diabetic retinopathy in patients with diabetic nephropathy: Development and progression. PLoS One 2016;11:e0161897.  Back to cited text no. 28
    
29.
Sachdev N, Sahni A. Association of systemic risk factors with the severity of retinal hard exudates in a North Indian population with type 2 diabetes. J Postgrad Med 2010;56:3-6.  Back to cited text no. 29
[PUBMED]  [Full text]  
30.
Rema M, Srivastava BK, Anitha B, Deepa R, Mohan V. Association of serum lipids with diabetic retinopathy in urban South Indians – The Chennai Urban Rural Epidemiology Study (CURES) Eye Study-2. Diabet Med 2006;23:1029-36.  Back to cited text no. 30
    
31.
Miljanovic B, Glynn RJ, Nathan DM, Manson JE, Schaumberg DA. A prospective study of serum lipids and risk of diabetic macular edema in type 1 diabetes. Diabetes 2004;53:2883-92.  Back to cited text no. 31
    
32.
Prakash G, Agrawal R, Satsangi SK, Prakash S. Comparison of serum apolipoproteins and traditional lipids in eyes with diabetic retinopathy in Indian population: A case series. Middle East Afr J Ophthalmol 2016;23:212-4.  Back to cited text no. 32
[PUBMED]  [Full text]  
33.
Raman R, Ganesan S, Pal SS, Gella L, Kulothungan V, Sharma T, et al. Incidence and progression of diabetic retinopathy in urban India: Sankara Nethralaya-diabetic retinopathy epidemiology and molecular genetics study (SN-DREAMS II), report 1. Ophthalmic Epidemiol 2017;24:294-302.  Back to cited text no. 33
    
34.
Keech AC, Mitchell P, Summanen PA, O'Day J, Davis TM, Moffitt MS, et al. Effect of fenofibrate on the need for laser treatment for diabetic retinopathy (FIELD study): A randomised controlled trial. Lancet 2007;370:1687-97.  Back to cited text no. 34
    
35.
Chung YR, Park SW, Choi SY, Kim SW, Moon KY, Kim JH, et al. Association of statin use and hypertriglyceridemia with diabetic macular edema in patients with type 2 diabetes and diabetic retinopathy. Cardiovasc Diabetol 2017;16:4.  Back to cited text no. 35
    
36.
Ranil PK, Raman R, Rachepalli SR, Pal SS, Kulothungan V, Lakshmipathy P, et al. Anemia and diabetic retinopathy in type 2 diabetes mellitus. J Assoc Physicians India 2010;58:91-4.  Back to cited text no. 36
    
37.
Qiao Q, Keinänen-Kiukaanniemi S, Läärä E. The relationship between hemoglobin levels and diabetic retinopathy. J Clin Epidemiol 1997;50:153-8.  Back to cited text no. 37
    
38.
Bahar A, Kashi Z, Ahmadzadeh Amiri A, Nabipour M. Association between diabetic retinopathy and hemoglobin level. Caspian J Intern Med 2013;4:759-62.  Back to cited text no. 38
    
39.
Sepúlveda FJ, Pérez P, Medinilla MG, Aboytes CA. Anemia as a factor related to the progression of proliferative diabetic retinopathy after photocoagulation. J Diabetes Complications 2012;26:454-7.  Back to cited text no. 39
    
40.
Kitzmiller JL, Block JM, Brown FM, Catalano PM, Conway DL, Coustan DR,et al. Managing preexisting diabetes for pregnancy: summary of evidence andconsensus recommendations for care. Diabetes Care. 2008;31:1060-79.  Back to cited text no. 40
    
41.
American Academy of Ophthalmology Preferred Practice Pattern. Retinal/Vitreous Panel. Diabetic Retinopathy Preferred Practice Patterns Guidelines. Updated February, 2016.  Back to cited text no. 41
    
42.
Toda J, Kato S, Sanaka M, Kitano S. The effect of pregnancy on the progression of diabetic retinopathy. Jpn J Ophthalmol 2016;60:454-8.  Back to cited text no. 42
    
43.
Morrison JL, Hodgson LA, Lim LL, Al-Qureshi S. Diabetic retinopathy in pregnancy: A review. Clin Exp Ophthalmol 2016;44:321-34.  Back to cited text no. 43
    
44.
Mallika P, Tan A, Aziz S, Ashok T, Alwi SS, Intan G, et al. Diabetic retinopathy and the effect of pregnancy. Malays Fam Physician 2010;5:2-5.  Back to cited text no. 44
    
45.
Axer-Siegel R, Hod M, Fink-Cohen S, Kramer M, Weinberger D, Schindel B, et al. Diabetic retinopathy during pregnancy. Ophthalmology 1996;103:1815-9.  Back to cited text no. 45
    
46.
Diabetes Control and Complications Trial Research Group. Effect of pregnancy on microvascular complications in the diabetes control and complications trial. The Diabetes Control and Complications Trial Research Group. Diabetes Care 2000;23:1084-91.  Back to cited text no. 46
    
47.
Pradeepa R, Surendar J, Indulekha K, Chella S, Anjana RM, Mohan V, et al. Relationship of diabetic retinopathy with coronary artery disease in Asian Indians with type 2 diabetes: The Chennai urban Rural Epidemiology Study (CURES) eye study-3. Diabetes Technol Ther 2015;17:112-8.  Back to cited text no. 47
    
48.
Xie J, Ikram MK, Cotch MF, Klein B, Varma R, Shaw JE, et al. Association of diabetic macular edema and proliferative diabetic retinopathy with cardiovascular disease: A systematic review and meta-analysis. JAMA Ophthalmol 2017;135:586-93.  Back to cited text no. 48
    
49.
Kurihara O, Takano M, Mizuno K, Shibata Y, Matsushita M, Komiyama H, et al. Impact of diabetic retinopathy on vulnerability of atherosclerotic coronary plaque and incidence of acute coronary syndrome. Am J Cardiol 2016;118:944-9.  Back to cited text no. 49
    
50.
Bjornstad P, Maahs DM, Duca LM, Pyle L, Rewers M, Johnson RJ, et al. Estimated insulin sensitivity predicts incident micro- and macrovascular complications in adults with type 1 diabetes over 6 years: The coronary artery calcification in type 1 diabetes study. J Diabetes Complications 2016;30:586-90.  Back to cited text no. 50
    
51.
Shi Y, Tham YC, Cheung N, Chua J, Tan G, Mitchell P, et al. Is aspirin associated with diabetic retinopathy? The Singapore epidemiology of eye disease (SEED) study. PLoS One 2017;12:e0175966.  Back to cited text no. 51
    
52.
American Diabetes Association. Standards of medical care in diabetes: Glycemic targets. Diabetes Care 2017;40 Suppl 1:S48-56.  Back to cited text no. 52
    
53.
American Diabetes Association. Standards of medical care in diabetes: Cardiovascular disease and risk management. Diabetes Care 2017;40 Suppl 1:S75-87.  Back to cited text no. 53
    




 

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  In this article
Abstract
Introduction
Hyperglycaemia
Hypertension
Nephropathy
Hyperlipidaemia
Anaemia
Pregnancy
Cardiovascular D...
Conclusion
References

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