The blood perfusion changes of peripapillary and macular vessels in patients with nonarteritic anterior ischemic optic neuropathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Liu Juejun ,  Chen Changzheng , Li Lu , Yi Zuohuizi , Zheng Hongmei

Eye Center, People's Hospital of Wuhan University, Wuhan 430060, China;

Corresponding author：

Chen Changzheng, Email: whuchenchzh@163.com

Keywords：

Optic neuropathy ischemic; Optic disk; Macula lutea; Regional blood flow; Tomography, optical coherence

DOI：

10.3760/cma.j.issn.1005-1015.2019.03.002

Video：

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Objective To observe the blood perfusion changes of peripapillary and macular vessels in patients with nonarteritic anterior ischaemic optic neuropathy (NAION).Methods Retrospective cohort study. Thirty-six eyes (19 affected eyes and 17 fellow eyes) of 19 patients with NAION diagnosed in People’s Hospital of Wuhan University from November 2017 to January 2019 were included in this study. There were 10 males and 9 females, with the mean age of 55.05±7.11 years. Forty eyes of 20 normal subjects matched with NAION patients were included as controls. BCVA, fundus color photography, SD-OCT and OCT angiography were performed in normal controls and repeated in NAION affected eyes at 1-2 weeks, 1-2 months, 3-5 months intervals. OCT quantitative measurements: average retinal nerve fiber layer thickness (aRNFL) of the disc and its superior values (sRNFL) and the inferior values (iRNFL), average ganglion cell complex thickness (aGCC) in macular region and its superior values (sGCC) and the inferior values (iGCC). OCTA quantitative measurements: average radial peripapillary capillary density (aRPC) and its superior values (sRPC) and the inferior values (iRPC), average vascular density of superficial retina (aSVD) in macular region and its superior values (sSVD) and the inferior values (iSVD), average vascular density of deep layer retina (aDVD), areas of foveal avascular zone (FAZ). The differences of OCT and OCTA quantitative measurements between NAION eyes and the fellow eyes and normal controls were comparatively analyzed. Independent sample t test, paired sample t test or nonparametric rank sum test were performed for comparison among three groups. Pearson or Spearman correlation analysis were used to analyze the correlation between RNFL and RPC, GCC and SVD, RNFL and GCC, RPC and SVD.Results At baseline, the aRNFL, aRPC and aDVD of NAION patients were significantly higher than those of normal controls. Compared with the fellow eyes, the aRNFL increased significantly and the aRPC decreased significantly in NAION affected eyes. The overall differences of aRNFL, aRPC, aGCC and aSVD at four intervals within NAION affected eyes were statistically significant (P＜0.05). The average sRNFL, sRPC, sGCC and sSVD at 1-2 months interval were significantly lower than the average iRNFL, iRPC, iGCC and iSVD (P＜0.05). Correlation analysis: at 1-2 months interval, aGCC was positively correlated with aSVD (r=0.482, P=0.037); at 3-5 months interval, aRNFL was positively correlated with aRPC (r=0.631, P=0.037).Conclusion There is a sectorial reduction of vascular density of peripapillary RPC and macular SVD with the disease progression of NAION.

Citation： Liu Juejun, Chen Changzheng, Li Lu, Yi Zuohuizi, Zheng Hongmei. The blood perfusion changes of peripapillary and macular vessels in patients with nonarteritic anterior ischemic optic neuropathy. Chinese Journal of Ocular Fundus Diseases, 2019, 35(3): 219-225. doi: 10.3760/cma.j.issn.1005-1015.2019.03.002 Copy

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2.	王建民, 马景学, 王长龄, 等. 前部缺血性视神经病变的吲哚青绿和荧光素眼底血管造影[J]. 中华眼底病杂志, 2001, 17(2): 111-114. DOI: 10.3760/j.issn.1005-1015.2001.02.010.Wang JM, Ma JX, Wang CL, et al. Indocyanine green and fundus fluorescein angiography in anterior ischemic optic neuropathy[J]. Chin J Ocul Fundus Dis, 2001, 17(2): 111-114. DOI: 10.3760/j.issn.1005-1015.2001.02.010.
3.	Nagiel A, Sadda SR, Sarraf D. A promising future for optical coherence tomography angiography[J]. JAMA Ophthalmol, 2015, 133(6): 629-30. DOI: 10.1001/jamaophthalmol.2015.0668.
4.	杨沫, 王伟, 魏世辉, 等. 非动脉炎性前部缺血性视神经病变光相干断层扫描血管成像特征及其与视野的相关性分析[J]. 中华眼底病杂志, 2017, 33(5): 453-457. DOI: 10.3760/cma.j.issn.1005-1015.2017.05.004.Yang M, Wang W, Wei SH, et al. The characteristics of optical coherence tomography angiography and its relationship with visual field defect in nonarteritic anterior ischemic optic neuropathy[J]. Chin J Ocul Fundus Dis, 2017, 33(5): 453-457. DOI: 10.3760/cma.j.issn.1005-1015.2017.05.004.
5.	Mastropasqua R, Agnifili L, Borrelli E, et al. Optical coherence tomography angiography of the peripapillary retina in normal-tension glaucoma and chronic nonarteritic anterior ischemic optic neuropathy[J]. Curr Eye Res, 2018, 43(6): 778-784. DOI: 10.1080/02713683.2018.1438630.
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7.	Wylegala A. Principles of OCTA and applications in clinical neurology[J]. Curr Neurol Neurosci Rep, 2018, 18(12): 96. DOI: 10.1007/s11910-018-0911-x.
8.	中华医学会, 中国医师协会. 我国眼底相干光层析血管成像术的操作和阅片规范(2017年)[J]. 中华眼科杂志, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association;Professional Committee of Fundus Diseases, Ophthalmologist Branch of Chinese Doctors Association. Standards for operations and reading of coherent optical tomography angiography in China (2017)[J]. Chin J Ophthalmol, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.
9.	Kraus MF, Liu JJ, Schottenhamml J, et al. Quantitative 3D-OCT motion correction with tilt and illumination correction, robust similarity measure and regularization[J]. Biomed Opt Express, 2014, 5(8): 2591-2613. DOI: 10.1364/BOE.5.002591.
10.	中华医学会眼科学分会神经眼科学组. 我国非动脉炎性前部缺血性视神经病变诊断和治疗专家共识(2015年)[J]. 中华眼科杂志, 2015, 51(5): 323-326. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.002.Ophthalmology Branch of Chinese Medical Association. Diagnosis and treatment guideline of nonarteritic anterior ischemic optic neuropathy in china[J]. Chin J Ophthalmol, 2015, 51(5): 323-326. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.002.
11.	Sharma S, Ang M, Najjar RP, et al. Optical coherence tomography angiography in acute non-arteritic anterior ischaemic optic neuropathy[J]. Br J Ophthalmol, 2017, 101(8): 1045-1051. DOI: 10.1136/bjophthalmol-2016-309245.
12.	Rebolleda G, Díez-Álvarez L, de Dompablo E, et al. early macular vessel density loss in acute ischemic optic neuropathy compared to papilledema: implications for pathogenesis[J]. Transl Vis Sci Technol, 2018, 8(1): 6. DOI: 10.1167/tvst.8.1.6.
13.	Fard MA, Jalili J, Sahraiyan A, et al. Optical coherence tomography angiography in optic disc swelling[J]. Am J Ophthalmol, 2018, 191: 116-123. DOI: 10.1016/j.ajo.2018.04.017.
14.	Hayreh SS, Zimmerman MB. Nonarteritic anterior ischemic optic neuropathy: natural history of visual outcome[J]. Ophthalmology, 2008, 115(2): 298-305. DOI: 10.1016/j.ophtha.2007.05.027.
15.	Mase T, Ishibazawa A, Nagaoka T, et al. Radial peripapillary capillary network visualized using wide-field montage optical coherence tomography angiography[J]. Invest Ophth Vis Sci, 2016, 57(9): 504-510. DOI: 10.1167/iovs.15-18877.
16.	Lim HB, Lee MW, Park JH, et al. Changes in ganglion cell-inner plexiform layer thickness and retinal microvasculature in hypertension: an OCT angiography study[J]. Am J Ophthalmol, 2019, 199: 167-176. DOI: 10.1016/j.ajo.2018.11.016.
17.	Goto K, Miki A, Araki S, et al. Time course of macular and peripapillary inner retinal thickness in non-arteritic anterior ischaemic optic neuropathy using spectral-domain optical coherence tomography[J]. Neuroophthalmology, 2016, 40(2): 74-85. DOI: 10.3109/01658107.2015.1136654.
18.	Akbari M, Abdi P, Fard MA, et al. Retinal ganglion cell loss precedes retinal nerve fiber thin ning in nonarteritic anterior ischemic optic neuropathy[J]. J Neuroophthalmol, 2016, 36(2): 141-146. DOI: 10.1097/WNO.0000000000000345.
19.	Yu J, Gu RP, Zong Y, et al. Relationship between retinal perfusion and retinal thickness in healthy subjects: an optical coherence tomography angiography study[J]. Invest Ophth Vis Sci, 2016, 57(9): 204-510. DOI: 10.1167/iovs.15-18630.
20.	Zeng Y, Cao D, Yu H, et al. Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy[J/OL]. Br J Ophthalmol, 2019, 2019: E1[2019-01-23]. http://dx.doi.org/10.1136/bjophthalmol-2018-313582. DOI: 10.1136/bjophthalmol-2018-313582. [published online ahead of print].
21.	Wang H, Meng ZY, Li SG, et al. Macular evaluation of the retinal and choroidal vasculature changes in anterior ischemic optic neuropathy-a case control study[J]. BMC Ophthalmol, 2018, 18(1): 341. DOI: 10.1186/s12886-018-1007-8.
22.	Aggarwal D, Tan O, Huang D, et al. Patterns of ganglion cell complex and nerve fiber layer loss in nonarteritic ischemic optic neuropathy by Fourier-domain optical coherence tomography[J]. Invest Ophthalmol Vis Sci, 2012, 53(8): 4539-4545. DOI: 10.1167/iovs.11-9300.
23.	De Dompablo E, García-Montesinos J, Muñoz-Negrete FJ, et al. Ganglion cell analysis at acute episode of nonarteritic anterior ischemic optic neuropathy to predict irreversible damage: a pros pective study[J]. Grae'f Arch Clin Exp, 2016, 254(9): 1793-1800. DOI: 10.1007/s00417-016-3425-8.
24.	Cestari DM, Gaier ED, Bouzika P, et al. Demographic, systemic, and ocular factors associated with nonarteritic anterior ischemic optic neuropathy[J]. Ophthalmology, 2016, 123(12): 2446-2455. DOI: 10.1016/j.ophtha.2016.08.017.
25.	Hayreh SS, Zimmerman MB. Nonarteritic anterior ischemic optic neuropathy: clinical charac teristics in diabetic patients versus nondiabetic patients[J]. Ophthalmology, 2008, 115(10): 1818-1825. DOI: 10.1016/j.ophtha.2008.03.032.
26.	Chen Q, Ma QK, Wu CM, et al. Macular vascular fractal dimension in the deep capillary layer as an early indicator of microvascular loss for retinopathy in type 2 diabetic patients[J]. Invest Ophth Vis Sci, 2017, 58(9): 3785-3794. DOI: 10.1167/iovs.17-21461.

1. Hayreh SS. Ischemic optic neuropathy[J]. Prog Retin Eye Res, 2009, 28(1): 34-62. DOI: 10.1016/j.preteyeres.2008.11.002.
2. 王建民, 马景学, 王长龄, 等. 前部缺血性视神经病变的吲哚青绿和荧光素眼底血管造影[J]. 中华眼底病杂志, 2001, 17(2): 111-114. DOI: 10.3760/j.issn.1005-1015.2001.02.010.Wang JM, Ma JX, Wang CL, et al. Indocyanine green and fundus fluorescein angiography in anterior ischemic optic neuropathy[J]. Chin J Ocul Fundus Dis, 2001, 17(2): 111-114. DOI: 10.3760/j.issn.1005-1015.2001.02.010.
3. Nagiel A, Sadda SR, Sarraf D. A promising future for optical coherence tomography angiography[J]. JAMA Ophthalmol, 2015, 133(6): 629-30. DOI: 10.1001/jamaophthalmol.2015.0668.
4. 杨沫, 王伟, 魏世辉, 等. 非动脉炎性前部缺血性视神经病变光相干断层扫描血管成像特征及其与视野的相关性分析[J]. 中华眼底病杂志, 2017, 33(5): 453-457. DOI: 10.3760/cma.j.issn.1005-1015.2017.05.004.Yang M, Wang W, Wei SH, et al. The characteristics of optical coherence tomography angiography and its relationship with visual field defect in nonarteritic anterior ischemic optic neuropathy[J]. Chin J Ocul Fundus Dis, 2017, 33(5): 453-457. DOI: 10.3760/cma.j.issn.1005-1015.2017.05.004.
5. Mastropasqua R, Agnifili L, Borrelli E, et al. Optical coherence tomography angiography of the peripapillary retina in normal-tension glaucoma and chronic nonarteritic anterior ischemic optic neuropathy[J]. Curr Eye Res, 2018, 43(6): 778-784. DOI: 10.1080/02713683.2018.1438630.
6. Augstburger E, Zeboulon P, Keilani C, et al. Retinal and choroidal microvasculature in nonarteritic anterior ischemic optic neuropathy: an optical coherence tomography angiography study[J]. Invest Ophthalmol Vis Sci, 2018, 59(2): 870-877. DOI: 10.1167/iovs.17-22996.
7. Wylegala A. Principles of OCTA and applications in clinical neurology[J]. Curr Neurol Neurosci Rep, 2018, 18(12): 96. DOI: 10.1007/s11910-018-0911-x.
8. 中华医学会, 中国医师协会. 我国眼底相干光层析血管成像术的操作和阅片规范(2017年)[J]. 中华眼科杂志, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association;Professional Committee of Fundus Diseases, Ophthalmologist Branch of Chinese Doctors Association. Standards for operations and reading of coherent optical tomography angiography in China (2017)[J]. Chin J Ophthalmol, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.
9. Kraus MF, Liu JJ, Schottenhamml J, et al. Quantitative 3D-OCT motion correction with tilt and illumination correction, robust similarity measure and regularization[J]. Biomed Opt Express, 2014, 5(8): 2591-2613. DOI: 10.1364/BOE.5.002591.
10. 中华医学会眼科学分会神经眼科学组. 我国非动脉炎性前部缺血性视神经病变诊断和治疗专家共识(2015年)[J]. 中华眼科杂志, 2015, 51(5): 323-326. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.002.Ophthalmology Branch of Chinese Medical Association. Diagnosis and treatment guideline of nonarteritic anterior ischemic optic neuropathy in china[J]. Chin J Ophthalmol, 2015, 51(5): 323-326. DOI: 10.3760/cma.j.issn.0412-4081.2015.05.002.
11. Sharma S, Ang M, Najjar RP, et al. Optical coherence tomography angiography in acute non-arteritic anterior ischaemic optic neuropathy[J]. Br J Ophthalmol, 2017, 101(8): 1045-1051. DOI: 10.1136/bjophthalmol-2016-309245.
12. Rebolleda G, Díez-Álvarez L, de Dompablo E, et al. early macular vessel density loss in acute ischemic optic neuropathy compared to papilledema: implications for pathogenesis[J]. Transl Vis Sci Technol, 2018, 8(1): 6. DOI: 10.1167/tvst.8.1.6.
13. Fard MA, Jalili J, Sahraiyan A, et al. Optical coherence tomography angiography in optic disc swelling[J]. Am J Ophthalmol, 2018, 191: 116-123. DOI: 10.1016/j.ajo.2018.04.017.
14. Hayreh SS, Zimmerman MB. Nonarteritic anterior ischemic optic neuropathy: natural history of visual outcome[J]. Ophthalmology, 2008, 115(2): 298-305. DOI: 10.1016/j.ophtha.2007.05.027.
15. Mase T, Ishibazawa A, Nagaoka T, et al. Radial peripapillary capillary network visualized using wide-field montage optical coherence tomography angiography[J]. Invest Ophth Vis Sci, 2016, 57(9): 504-510. DOI: 10.1167/iovs.15-18877.
16. Lim HB, Lee MW, Park JH, et al. Changes in ganglion cell-inner plexiform layer thickness and retinal microvasculature in hypertension: an OCT angiography study[J]. Am J Ophthalmol, 2019, 199: 167-176. DOI: 10.1016/j.ajo.2018.11.016.
17. Goto K, Miki A, Araki S, et al. Time course of macular and peripapillary inner retinal thickness in non-arteritic anterior ischaemic optic neuropathy using spectral-domain optical coherence tomography[J]. Neuroophthalmology, 2016, 40(2): 74-85. DOI: 10.3109/01658107.2015.1136654.
18. Akbari M, Abdi P, Fard MA, et al. Retinal ganglion cell loss precedes retinal nerve fiber thin ning in nonarteritic anterior ischemic optic neuropathy[J]. J Neuroophthalmol, 2016, 36(2): 141-146. DOI: 10.1097/WNO.0000000000000345.
19. Yu J, Gu RP, Zong Y, et al. Relationship between retinal perfusion and retinal thickness in healthy subjects: an optical coherence tomography angiography study[J]. Invest Ophth Vis Sci, 2016, 57(9): 204-510. DOI: 10.1167/iovs.15-18630.
20. Zeng Y, Cao D, Yu H, et al. Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy[J/OL]. Br J Ophthalmol, 2019, 2019: E1[2019-01-23]. http://dx.doi.org/10.1136/bjophthalmol-2018-313582. DOI: 10.1136/bjophthalmol-2018-313582. [published online ahead of print].
21. Wang H, Meng ZY, Li SG, et al. Macular evaluation of the retinal and choroidal vasculature changes in anterior ischemic optic neuropathy-a case control study[J]. BMC Ophthalmol, 2018, 18(1): 341. DOI: 10.1186/s12886-018-1007-8.
22. Aggarwal D, Tan O, Huang D, et al. Patterns of ganglion cell complex and nerve fiber layer loss in nonarteritic ischemic optic neuropathy by Fourier-domain optical coherence tomography[J]. Invest Ophthalmol Vis Sci, 2012, 53(8): 4539-4545. DOI: 10.1167/iovs.11-9300.
23. De Dompablo E, García-Montesinos J, Muñoz-Negrete FJ, et al. Ganglion cell analysis at acute episode of nonarteritic anterior ischemic optic neuropathy to predict irreversible damage: a pros pective study[J]. Grae'f Arch Clin Exp, 2016, 254(9): 1793-1800. DOI: 10.1007/s00417-016-3425-8.
24. Cestari DM, Gaier ED, Bouzika P, et al. Demographic, systemic, and ocular factors associated with nonarteritic anterior ischemic optic neuropathy[J]. Ophthalmology, 2016, 123(12): 2446-2455. DOI: 10.1016/j.ophtha.2016.08.017.
25. Hayreh SS, Zimmerman MB. Nonarteritic anterior ischemic optic neuropathy: clinical charac teristics in diabetic patients versus nondiabetic patients[J]. Ophthalmology, 2008, 115(10): 1818-1825. DOI: 10.1016/j.ophtha.2008.03.032.
26. Chen Q, Ma QK, Wu CM, et al. Macular vascular fractal dimension in the deep capillary layer as an early indicator of microvascular loss for retinopathy in type 2 diabetic patients[J]. Invest Ophth Vis Sci, 2017, 58(9): 3785-3794. DOI: 10.1167/iovs.17-21461.

Chinese Journal of Ocular Fundus Diseases

The blood perfusion changes of peripapillary and macular vessels in patients with nonarteritic anterior ischemic optic neuropathy

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