The assessment of diabetic macular ischemia and the influence of intravitreal anti-vascular endothelial growth factor therapy to diabetic macular ischemia_Chinese Journal of Ocular Fundus Diseases

Authors：

Wang Desai , Liu Shulin ,  Zhang Xuedong

The First Affiliated Hospital of Chongqing Medical University, Chongqing Key Laboratory of Ophthalmology, Chongqing 400016, China;

Corresponding author：

Zhang Xuedong, Email: 370074@qq.com

Keywords：

Diabetic retinopathy/therapy; Angiogenesis inhibitors/therapeutic use; Antibodies, monoclonal/therapeutic use; Review; Diabetic macular ischemia

DOI：

10.3760/cma.j.issn.1005-1015.2019.03.024

Video：

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Abstract Full text Figures/Tables Video References Cited by

Diabetic macular ischemia (DMI) is one of the manifestation of diabetic retinopathy (DR). It could be associated with diabetic macular edema (DME), which may affect the vision of DR patients. FFA is the gold standard for the diagnosis of DMI, but with the advent of OCT angiography, a more convenient and diversified method for the evaluation of DMI has been developed, which makes more and more researchers start to study DMI. Intravitreal injection of anti-VEGF has become the preferred treatment for DME. When treating with DME patients, ophthalmologists usually avoid DMI patients. But if intravitreal anti-VEGF should be the contradiction of DME is still unclear. To provide references to the research, this article summarized the risk factors, assessment methods and influence of DMI. This article also analyzed the existing studies, aiming to offer evidences to a more reasonable and effective treatment decision for DME individual.

Citation： Wang Desai, Liu Shulin, Zhang Xuedong. The assessment of diabetic macular ischemia and the influence of intravitreal anti-vascular endothelial growth factor therapy to diabetic macular ischemia. Chinese Journal of Ocular Fundus Diseases, 2019, 35(3): 311-315. doi: 10.3760/cma.j.issn.1005-1015.2019.03.024 Copy

1.	Bresnick G, De Venecia G, Myers F, et al. Retinal ischemia in diabetic retinopathy[J]. Arch Ophthalmol, 1975, 93(12): 1300-1310. DOI: 10.1001/archopht.1975.01010020934002.
2.	中华医学会眼科学会眼底病学组. 我国糖尿病视网膜病变临床诊疗指南(2014年[J]. 中华眼科杂志, 2014, 50(11): 851-865. DOI: 10.3760/cam.j.issn.0412-4081.2014.11.014.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association. Clinical practice guidelines of diabetic retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cam.j.issn.0412-4081.2014.11.014.
3.	Lee D, Yi H, Bae S, et al. Risk factors for retinal microvascular impairment in type 2 diabetic patients without diabetic retinopathy[J/OL]. PLoS One, 2018, 13(8): 0202103[2018-08-09]. http://dx.plos.org/10.1371/journal.pone.0202103.DOI:10.1371/journal.pone.0202103.
4.	Gozlan J, Ingrand P, Lichtwitz O, et al. Retinal microvascular alterations related to diabetes assessed by optical coherence tomography angiography: a cross-sectional analysis[J]. Medicine (Baltimore), 2017, 96(15): 6427. DOI: 10.1097/MD.000000000000642.
5.	Benitez-Herreros J, Lopez-Guajardo L, Camara-Gonzalez C, et al. Association between macular perfusion and photoreceptor layer status in diabetic macular edema[J]. Retina, 2015, 35(2): 288-293. DOI: 10.1097/IAE.0000000000000299.
6.	Klefter O, Hommel E, Munch I, et al. Retinal characteristics during 1 year of insulin pump therapy in type 1 diabetes: a prospective, controlled, observational study[J]. Acta Ophthalmol, 2016, 94(6): 540-547. DOI: 10.1111/aos.13066.
7.	Bhanushali D, Anegondi N, Gadde S, et al. Linking retinal microvasculature features with severity of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 519-525. DOI: 10.1167/iovs.15-18901.
8.	Conrath J, Giorgi R, Ridings B, et al. Metabolic factors and the foveal avascular zone of the retina in diabetes mellitus[J]. Diabetes Metab, 2005, 31(5): 465-470. DOI: 10.1016/S1262-3636(07)70217-3.
9.	Karst SG, Deak GG, Gerendas BS, et al. Association of changes in macular perfusion with ranibizumab treatment for diabetic macular edema: a subanalysis of the restore (extension) study[J]. JAMA Ophthalmol, 2018, 136(4): 315-321. DOI: 10.1001/jamaophthalmol.2017.6135.
10.	Sasongko MB, Widyaputri F, Sulistyoningrum DC, et al. Estimated resting metabolic rate and body composition measures are strongly associated with diabetic retinopathy in indonesian adults with type 2 diabetes[J]. Diabetes Care, 2018, 41(11): 2377-2384. DOI: 10.2337/dc18-1074.
11.	Early Treatment Diabetic Retinopathy Study Research Group. Classification of diabetic retinopathy from fluorescein angiograms:ETDRS report number 11[J]. Ophthalmology, 1991, 98(5 Suppl): S807-822.
12.	Michaelides M, Fraser-Bell S, Hamilton R, et al. Macular perfusion determined by fundus fluorescein angiography at the 4-month time point in a prospective randomized trial of intravitreal bevacizumab or laser therapy in the management of diabetic macular edema (bolt study): report 1[J]. Retina, 2010, 30(5): 781-786. DOI: 10.1097/IAE.0b013e3181d2f145.
13.	Erol N, Gursoy H, Kimyon S, et al. Vision, retinal thickness, and foveal avascular zone size after intravitreal bevacizumab for diabetic macular edema[J]. Adv Ther, 2012, 29(4): 359-369. DOI: 10.1007/s12325-012-0009-9.
14.	Comyn O, Sivaprasad S, Peto T, et al. A randomized trial to assess functional and structural effects of ranibizumab versus laser in diabetic macular edema (the lucidate study)[J]. Am J Ophthalmol, 2014, 157(5): 960-970. DOI: 10.1016/j.ajo.2014.02.019.
15.	La Mantia A, Kurt RA, Mejor S, et al. Comparing fundus fluorescein angiography and swept-source optical coherence tomography angiography in the evaluation of diabetic macular perfusion[J]. Retina, 2019, 39(5): 926-937. DOI: 10.1097/iae.0000000000002045.
16.	Tan C, Lim L, Chow V, et al. Optical coherence tomography angiography evaluation of the parafoveal vasculature and its relationship with ocular factors[J]. Invest. Ophthalmol Vis Sci, 2016, 57(9): 224-234. DOI: 10.1167/iovs.15-18869.
17.	Bonini-Filho M, Costa RA, Calucci D, et al. Intravitreal bevacizumab for diabetic macular edema associated with severe capillary loss: one-year results of a pilot study[J]. Am J Ophthalmol, 2009, 147(6): 1022-1030. DOI: 10.1016/j.ajo.2009.01.009.
18.	Campochiaro PA, Wykoff CC, Shapiro H, et al. Neutralization of vascular endothelial growth factor slows progression of retinal nonperfusion in patients with diabetic macular edema[J]. Ophthalmology, 2014, 121(9): 1783-1789. DOI: 10.1016/j.ophtha.2014.03.021.
19.	Ip MS, Domalpally A, Sun J K, et al. Long-term effects of therapy with ranibizumab on diabetic retinopathy severity and baseline risk factors for worsening retinopathy[J]. Ophthalmology, 2015, 122(2): 367-374. DOI: 10.1016/j.ophtha.2014.08.048.
20.	Reddy RK, Pieramici DJ, Gune S, et al. Efficacy of ranibizumab in eyes with diabetic macular edema and macular nonperfusion in ride and rise[J]. Ophthalmology, 2018, 125(10): 1568-1574. DOI: 10.1016/j.ophtha.2018.04.002.
21.	Nesper PL, Scarinci F, Fawzi AA. Adaptive optics reveals photoreceptor abnormalities in diabetic macular ischemia[J/OL].PLoS One, 2017, 12(1): 0169926[2017-01-09].https://doi.org/10.1371/journal.pone.0169926.DOI:10.1371/journal.pone.0169926.
22.	Scarinci F, Nesper PL, Fawzi AA. Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia[J]. Am J Ophthalmol, 2016, 168: 129-138. DOI: 10.1016/j.ajo.2016.05.002.
23.	Freiberg FJ, Pfau M, Wons J, et al. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2016, 254(6): 1051-1058. DOI: 10.1007/s00417-015-3148-2.
24.	Tang F, Ng D, Lam A, et al. Determinants of quantitative optical coherence tomography angiography metrics in patients with diabetes[J/OL]. Sci Rep, 2017, 7(1): 2575[2017-05-31]. https://www.nature.com/articles/s41598-017-02767-0.DOI:10.1038/s41598-017-02767-0.
25.	Shiihara H, Terasaki H, Sonoda S, et al. Objective evaluation of size and shape of superficial foveal avascular zone in normal subjects by optical coherence tomography angiography[J/OL]. Sci Rep, 2018, 8(1): 10143[2018-07-04]. https://www.nature.com/articles/s41598-018-28530-7.DOI:10.1038/s41598-018-28530-7.
26.	Gadde S, Anegondi N, Bhanushali D, et al. Quantification of vessel density in retinal optical coherence tomography angiography images using local fractal dimension[J]. Invest Ophthalmol Vis Sci, 2016, 57(1): 246-252. DOI: 10.1167/iovs.16-19256.
27.	Kim A, Chu Z, Shahidzadeh A, et al. Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 362-370. DOI: 10.1167/iovs.15-18904.
28.	Lu Y, Simonett JM, Wang J, et al. Evaluation of automatically quantified foveal avascular zone metrics for diagnosis of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2018, 59(6): 2212-2221. DOI: 10.1167/iovs.17-23498.
29.	Hwang T, Hagag A, Wang J, et al. Automated quantification of nonperfusion areas in 3 vascular plexuses with optical coherence tomography angiography in eyes of patients with diabetes[J]. JAMA Ophthalmol, 2018, 136(8): 929-936. DOI: 10.1001/jamaophthalmol.2018.2257.
30.	Reif R, Qin J, An L, et al. Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system[J/OL]. Int J Biomed Imaging, 2012, 2012: 509783[2012-06-26].http://dx.doi.org/10.1155/2012/509783. DOI: 10.1155/2012/509783.
31.	Ashraf M, Nesper P, Jampol L, et al. Statistical model of optical coherence tomography angiography parameters that correlate with severity of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2018, 59(10): 4292-4298. DOI: 10.1167/iovs.18-24142.
32.	Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
33.	Scarinci F, Jampol L, Linsenmeier R, et al. Association of diabetic macular nonperfusion with outer retinal disruption on optical coherence tomography[J]. JAMA Ophthalmol, 2015, 133(9): 1036-1044. DOI: 10.1001/jamaophthalmol.2015.2183.
34.	Douvali M, Chatziralli IP, Theodossiadis PG, et al. Effect of macular ischemia on intravitreal ranibizumab treatment for diabetic macular edema[J]. Ophthalmologica, 2014, 232(3): 136-143. DOI: 10.1159/000360909.
35.	Bressler SB, Liu D, Glassman AR, et al. Change in diabetic retinopathy through 2 years: secondary analysis of a randomized clinical trial comparing aflibercept, bevacizumab, and ranibizumab[J]. JAMA Ophthalmology, 2017, 135(6): 558-568. DOI: 10.1001/jamaophthalmol.2017.0821.
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37.	Goel N, Kumar V, Ghosh B. Ischemic maculopathy following intravitreal bevacizumab for refractory diabetic macular edema[J]. Int Ophthalmol, 2011, 31(1): 39-42. DOI: 10.1007/s10792-010-9390-z.
38.	Battaglia Parodi M, Iacono P, Cascavilla ML, et al. Sequential anterior ischemic optic neuropathy and central retinal artery and vein occlusion after ranibizumab for diabetic macular edema[J]. Eur J Ophthalmol, 2010, 20(6): 1076-1078. DOI: 10.1177/112067211002000609.
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1. Bresnick G, De Venecia G, Myers F, et al. Retinal ischemia in diabetic retinopathy[J]. Arch Ophthalmol, 1975, 93(12): 1300-1310. DOI: 10.1001/archopht.1975.01010020934002.
2. 中华医学会眼科学会眼底病学组. 我国糖尿病视网膜病变临床诊疗指南(2014年[J]. 中华眼科杂志, 2014, 50(11): 851-865. DOI: 10.3760/cam.j.issn.0412-4081.2014.11.014.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association. Clinical practice guidelines of diabetic retinopathy in China (2014)[J]. Chin J Ophthalmol, 2014, 50(11): 851-865. DOI: 10.3760/cam.j.issn.0412-4081.2014.11.014.
3. Lee D, Yi H, Bae S, et al. Risk factors for retinal microvascular impairment in type 2 diabetic patients without diabetic retinopathy[J/OL]. PLoS One, 2018, 13(8): 0202103[2018-08-09]. http://dx.plos.org/10.1371/journal.pone.0202103.DOI:10.1371/journal.pone.0202103.
4. Gozlan J, Ingrand P, Lichtwitz O, et al. Retinal microvascular alterations related to diabetes assessed by optical coherence tomography angiography: a cross-sectional analysis[J]. Medicine (Baltimore), 2017, 96(15): 6427. DOI: 10.1097/MD.000000000000642.
5. Benitez-Herreros J, Lopez-Guajardo L, Camara-Gonzalez C, et al. Association between macular perfusion and photoreceptor layer status in diabetic macular edema[J]. Retina, 2015, 35(2): 288-293. DOI: 10.1097/IAE.0000000000000299.
6. Klefter O, Hommel E, Munch I, et al. Retinal characteristics during 1 year of insulin pump therapy in type 1 diabetes: a prospective, controlled, observational study[J]. Acta Ophthalmol, 2016, 94(6): 540-547. DOI: 10.1111/aos.13066.
7. Bhanushali D, Anegondi N, Gadde S, et al. Linking retinal microvasculature features with severity of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 519-525. DOI: 10.1167/iovs.15-18901.
8. Conrath J, Giorgi R, Ridings B, et al. Metabolic factors and the foveal avascular zone of the retina in diabetes mellitus[J]. Diabetes Metab, 2005, 31(5): 465-470. DOI: 10.1016/S1262-3636(07)70217-3.
9. Karst SG, Deak GG, Gerendas BS, et al. Association of changes in macular perfusion with ranibizumab treatment for diabetic macular edema: a subanalysis of the restore (extension) study[J]. JAMA Ophthalmol, 2018, 136(4): 315-321. DOI: 10.1001/jamaophthalmol.2017.6135.
10. Sasongko MB, Widyaputri F, Sulistyoningrum DC, et al. Estimated resting metabolic rate and body composition measures are strongly associated with diabetic retinopathy in indonesian adults with type 2 diabetes[J]. Diabetes Care, 2018, 41(11): 2377-2384. DOI: 10.2337/dc18-1074.
11. Early Treatment Diabetic Retinopathy Study Research Group. Classification of diabetic retinopathy from fluorescein angiograms:ETDRS report number 11[J]. Ophthalmology, 1991, 98(5 Suppl): S807-822.
12. Michaelides M, Fraser-Bell S, Hamilton R, et al. Macular perfusion determined by fundus fluorescein angiography at the 4-month time point in a prospective randomized trial of intravitreal bevacizumab or laser therapy in the management of diabetic macular edema (bolt study): report 1[J]. Retina, 2010, 30(5): 781-786. DOI: 10.1097/IAE.0b013e3181d2f145.
13. Erol N, Gursoy H, Kimyon S, et al. Vision, retinal thickness, and foveal avascular zone size after intravitreal bevacizumab for diabetic macular edema[J]. Adv Ther, 2012, 29(4): 359-369. DOI: 10.1007/s12325-012-0009-9.
14. Comyn O, Sivaprasad S, Peto T, et al. A randomized trial to assess functional and structural effects of ranibizumab versus laser in diabetic macular edema (the lucidate study)[J]. Am J Ophthalmol, 2014, 157(5): 960-970. DOI: 10.1016/j.ajo.2014.02.019.
15. La Mantia A, Kurt RA, Mejor S, et al. Comparing fundus fluorescein angiography and swept-source optical coherence tomography angiography in the evaluation of diabetic macular perfusion[J]. Retina, 2019, 39(5): 926-937. DOI: 10.1097/iae.0000000000002045.
16. Tan C, Lim L, Chow V, et al. Optical coherence tomography angiography evaluation of the parafoveal vasculature and its relationship with ocular factors[J]. Invest. Ophthalmol Vis Sci, 2016, 57(9): 224-234. DOI: 10.1167/iovs.15-18869.
17. Bonini-Filho M, Costa RA, Calucci D, et al. Intravitreal bevacizumab for diabetic macular edema associated with severe capillary loss: one-year results of a pilot study[J]. Am J Ophthalmol, 2009, 147(6): 1022-1030. DOI: 10.1016/j.ajo.2009.01.009.
18. Campochiaro PA, Wykoff CC, Shapiro H, et al. Neutralization of vascular endothelial growth factor slows progression of retinal nonperfusion in patients with diabetic macular edema[J]. Ophthalmology, 2014, 121(9): 1783-1789. DOI: 10.1016/j.ophtha.2014.03.021.
19. Ip MS, Domalpally A, Sun J K, et al. Long-term effects of therapy with ranibizumab on diabetic retinopathy severity and baseline risk factors for worsening retinopathy[J]. Ophthalmology, 2015, 122(2): 367-374. DOI: 10.1016/j.ophtha.2014.08.048.
20. Reddy RK, Pieramici DJ, Gune S, et al. Efficacy of ranibizumab in eyes with diabetic macular edema and macular nonperfusion in ride and rise[J]. Ophthalmology, 2018, 125(10): 1568-1574. DOI: 10.1016/j.ophtha.2018.04.002.
21. Nesper PL, Scarinci F, Fawzi AA. Adaptive optics reveals photoreceptor abnormalities in diabetic macular ischemia[J/OL].PLoS One, 2017, 12(1): 0169926[2017-01-09].https://doi.org/10.1371/journal.pone.0169926.DOI:10.1371/journal.pone.0169926.
22. Scarinci F, Nesper PL, Fawzi AA. Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia[J]. Am J Ophthalmol, 2016, 168: 129-138. DOI: 10.1016/j.ajo.2016.05.002.
23. Freiberg FJ, Pfau M, Wons J, et al. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2016, 254(6): 1051-1058. DOI: 10.1007/s00417-015-3148-2.
24. Tang F, Ng D, Lam A, et al. Determinants of quantitative optical coherence tomography angiography metrics in patients with diabetes[J/OL]. Sci Rep, 2017, 7(1): 2575[2017-05-31]. https://www.nature.com/articles/s41598-017-02767-0.DOI:10.1038/s41598-017-02767-0.
25. Shiihara H, Terasaki H, Sonoda S, et al. Objective evaluation of size and shape of superficial foveal avascular zone in normal subjects by optical coherence tomography angiography[J/OL]. Sci Rep, 2018, 8(1): 10143[2018-07-04]. https://www.nature.com/articles/s41598-018-28530-7.DOI:10.1038/s41598-018-28530-7.
26. Gadde S, Anegondi N, Bhanushali D, et al. Quantification of vessel density in retinal optical coherence tomography angiography images using local fractal dimension[J]. Invest Ophthalmol Vis Sci, 2016, 57(1): 246-252. DOI: 10.1167/iovs.16-19256.
27. Kim A, Chu Z, Shahidzadeh A, et al. Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2016, 57(9): 362-370. DOI: 10.1167/iovs.15-18904.
28. Lu Y, Simonett JM, Wang J, et al. Evaluation of automatically quantified foveal avascular zone metrics for diagnosis of diabetic retinopathy using optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2018, 59(6): 2212-2221. DOI: 10.1167/iovs.17-23498.
29. Hwang T, Hagag A, Wang J, et al. Automated quantification of nonperfusion areas in 3 vascular plexuses with optical coherence tomography angiography in eyes of patients with diabetes[J]. JAMA Ophthalmol, 2018, 136(8): 929-936. DOI: 10.1001/jamaophthalmol.2018.2257.
30. Reif R, Qin J, An L, et al. Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system[J/OL]. Int J Biomed Imaging, 2012, 2012: 509783[2012-06-26].http://dx.doi.org/10.1155/2012/509783. DOI: 10.1155/2012/509783.
31. Ashraf M, Nesper P, Jampol L, et al. Statistical model of optical coherence tomography angiography parameters that correlate with severity of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2018, 59(10): 4292-4298. DOI: 10.1167/iovs.18-24142.
32. Samara WA, Shahlaee A, Adam MK, et al. Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity[J]. Ophthalmology, 2017, 124(2): 235-244. DOI: 10.1016/j.ophtha.2016.10.008.
33. Scarinci F, Jampol L, Linsenmeier R, et al. Association of diabetic macular nonperfusion with outer retinal disruption on optical coherence tomography[J]. JAMA Ophthalmol, 2015, 133(9): 1036-1044. DOI: 10.1001/jamaophthalmol.2015.2183.
34. Douvali M, Chatziralli IP, Theodossiadis PG, et al. Effect of macular ischemia on intravitreal ranibizumab treatment for diabetic macular edema[J]. Ophthalmologica, 2014, 232(3): 136-143. DOI: 10.1159/000360909.
35. Bressler SB, Liu D, Glassman AR, et al. Change in diabetic retinopathy through 2 years: secondary analysis of a randomized clinical trial comparing aflibercept, bevacizumab, and ranibizumab[J]. JAMA Ophthalmology, 2017, 135(6): 558-568. DOI: 10.1001/jamaophthalmol.2017.0821.
36. Chen E, Hsu J, Park CH. Acute visual acuity loss following intravitreal bevacizumab for diabetic macular edema[J]. Ophthalmic Surg Lasers Imaging, 2009, 40(1): 68-70. DOI: 10.3928/15428877-20090101-04.
37. Goel N, Kumar V, Ghosh B. Ischemic maculopathy following intravitreal bevacizumab for refractory diabetic macular edema[J]. Int Ophthalmol, 2011, 31(1): 39-42. DOI: 10.1007/s10792-010-9390-z.
38. Battaglia Parodi M, Iacono P, Cascavilla ML, et al. Sequential anterior ischemic optic neuropathy and central retinal artery and vein occlusion after ranibizumab for diabetic macular edema[J]. Eur J Ophthalmol, 2010, 20(6): 1076-1078. DOI: 10.1177/112067211002000609.
39. Lee S J, Koh HJ. Enlargement of the foveal avascular zone in diabetic retinopathy after adjunctive intravitreal bevacizumab (avastin) with pars plana vitrectomy[J]. J Ocul Pharmacol Ther, 2009, 25(2): 173-174. DOI: 10.1089/jop.2008.0092.
40. Feucht N, Schonbach EM, Lanzl I, et al. Changes in the foveal microstructure after intravitreal bevacizumab application in patients with retinal vascular disease[J]. Clin Ophthalmol, 2013, 7: 173-178. DOI: 10.2147/opth.s37544.
41. Chung EJ, Roh MI, Kwon OW, et al. Effects of macular ischemia on the outcome of intravitreal bevacizumab therapy for diabetic macular edema[J]. Retina, 2008, 28(7): 957-963. DOI: 10.1097/IAE.0b013e3181754209.
42. Byrne AM, Bouchier-Hayes DJ, Harmey JH. Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF)[J]. J Cell Mol Med, 2005, 9(4): 777-794. DOI: 10.1111/jcmm.2005.9.issue-4.
43. Jin KL, Mao X O, Greenberg DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia[J]. Proc Natl Acad Sci USA, 2000, 97(18): 10242-10247. DOI: 10.1073/pnas.97.18.10242.
44. Manousaridis K, Talks J. Macular ischaemia: a contraindication for anti-vegf treatment in retinal vascular disease[J]. Br J Ophthalmol, 2012, 96(2): 179-184. DOI: 10.1136/bjophthalmol-2011-301087.
45. Tolentino MJ, Miller JW, Gragoudas ES, et al. Intravitreous injections of vascular endothelial growth factor produce retinal ischemia and microangiopathy in an adult primate[J]. Ophthalmology, 1996, 103(11): 1820-1828. DOI: 10.1016/S0161-6420(96)30420-X.
46. Kook D, Wolf A, Kreutzer T, et al. Long-term effect of intravitreal bevacizumab (avastin) in patients with chronic diffuse diabetic macular edema[J]. Retina, 2008, 28(8): 1053-1060. DOI: 10.1097/IAE.0b013e318176de48.
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The assessment of diabetic macular ischemia and the influence of intravitreal anti-vascular endothelial growth factor therapy to diabetic macular ischemia

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