
==== Front
Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

71103
10.1038/s41598-024-71103-0
Article
Comparative of OCT and OCTA parameters in patients with early chronic angle-closure glaucoma and early pituitary adenoma
Tan Zhi 1
Lu Kai-lun 2
Zhang Wan-cheng 2
Peng Shu-ying 1
Wen Xiu-juan 2
Dai Tong-tong 2
Pang Yan-hua pang1049371818@163.com

2
1 grid.410560.6 0000 0004 1760 3078 Radiology Department. Affiliated Hospital of Guangdong Medical University, Zhanjiang, Guangdong Province China
2 grid.410560.6 0000 0004 1760 3078 Ophthalmology Department Affiliated Hospital of Guangdong Medical University, No. 57, South Renmin Avenue, Xiashan District, Zhanjiang, 524023 Guangdong Province China
13 9 2024
13 9 2024
2024
14 2144822 2 2024
26 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Optical coherence tomography (OCT) and optical coherence tomography angiography (OCTA) have the potential application in evaluating pathological structural change of the optic nerve. We aimed to evaluate the value of the OCT and OCTA parameters of the optic disk and macular in differentiating early chronic primary angle-closure glaucoma (CPACG) and early pituitary adenoma (PA) in case of mild visual field defects (the mean defect (MD) > 6 dB). The results showed that regarding OCTA parameters, CPACG patients had lower retinal blood flow density of most layers of the optic disk and macular than PA patients. Regarding OCT parameters, CPACG patients had thinner circumpapillary retinal nerve fiber layer (CP-RNFL) in all quadrants and average CP-RNFL, ganglion cell layer (GCL) and macular ganglion cell complex (GCC) in each quadrant of macular inner and outer rings, and inner plexus layer (IPL) of macular inner ring, superior-outer ring and temporal-outer ring than PA patients. The Z test indicated that OCTA parameters and OCT parameters had similar value in the diagnosis of disease. In conclusion, in the case of similar visual field damage, early CPACG patients have smaller blood flow density and thinner optic disk and macular than early PA. OCTA has similar performance to OCT in diagnosing CPACG and PA.

Keywords

Chronic primary angle-closure glaucoma (CPACG)
Pituitary adenoma (PA)
Optical coherence tomography angiography (OCTA)
Optical coherence tomography (OCT)
Subject terms

Diseases
Eye diseases
Neurological disorders
Science and Technology Program project of Zhanjiang2023A207 Tan Zhi issue-copyright-statement© Springer Nature Limited 2024
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pmcIntroduction

Glaucoma is a progressive structural optic neuropathy characterized by progressive thinning of retinal nerve fiber layer (RNFL) and optic disc depression and is the second leading cause of blindness in the world1. In the two types of glaucoma, although the incidence of primary angle-closure glaucoma (PACG) is lower than that of primary open-angle glaucoma (POAG), but the blindness rate is high, and more than 80% occur in Asia2,3. Improving the diagnosis rate in order to promptly treat and slow or avoid blindness is of great significance for PACG patients, especially for patients with highly concealed chronic PACG (CPACG), a type of PACG characterized by chronic elevation of intraocular pressure. However, CPACG and intracranial optic nerve compression disease are confused in the routine diagnosis. Clinical observation points out that intraocular pressure (fluctuating changes)4, visual field, optic disc characteristics (such as cup enlargement and RNFL thinning)5,6, and narrow anterior chamber angle of CPACG patients overlap with these characteristics in patients with pituitary adenoma (PA). Therefore, misdiagnosis of these two diseases often occurs even among experienced ophthalmologists7.

In recent years, combined macular Optical coherence tomography (OCT) and Optical coherence tomography angiography (OCTA) have also been applied to evaluate the damage to the macular area and optic nerve structure in glaucoma, such as the degree of visual impairment and visual field defect8,9, aiming to provide a basis for the diagnosis and treatment of glaucoma. OCT quantitatively, objectively, and reproducibly analyzes the optic nerve fiber and the structure of the macular area in vivo via common parameters including CP-RNFL, macular ganglion cell layer (GCL), macular ganglion cell complex (GCC) layer, etc., which are used to assist diagnosis and monitoring of glaucoma10. OCTA is a new imaging technology that shows the RNFL and macular microvascular changes in various optic neuropathies, such as in glaucoma, and ischemic and inflammatory optic nerves9,11. OCTA has also been used to assess PA-induced optic nerve damage. For example, Ben Ghezala, I et al. used OCTA to follow up on the changes of radial peripapillary capillaries plexus (RPCP) vessel density in the optic disk of PA patients after optic chiasm decompression12. In addition, few studies have used OCT and OCTA parameters to evaluate the changes in vessel density around the optic disk and macula after optic chiasm decompression in PA patients13,14. These studies indicate the potential application of OCT and OCTA in the study of structural change of the optic nerve. We raise the question of whether there is a difference in OCTA blood flow density between the eyes with early PA with mild compression of the optic chiasm and early CPACG, and whether these differences in OCT and OCTA parameters of the optic disk and macula region provide objective parameters for differentiating PA from glaucoma. Therefore, in this study, we used OCT and OCTA to measure parameters of the optic disk and macular area in early CPACG and early PA patients with mild visual field defects (the mean defect (MD) > 6 dB) to evaluate the efficacy of OCT and OCTA in differentiating early CPACG from early PA. To the best of our knowledge, this is the first study to compare fundus parameters between early CPACG and early PA.

Results

Baseline information

Case group 1 included 28 patients (28 eyes), including 14 males and 14 females, with an average age of (62.857 ± 10.848) years. Case group 2 included 30 patients (30 eyes), including 13 males and 17 females, with an average age of (59.300 ± 6.114) years. The composition of PA patients in case group 2 consisted of 1 adrenocorticotropic adenoma, 1 gonadotroph adenoma, 1 prolactinoma, 1 mixed growth hormone cell and prolactinoma, and the remaining non-secretory adenomas. All 30 patients in case group 2 had grade 1 optic chiasm compression. The 29 healthy controls included 16 males and 13 females, with an average age of (59.069 ± 6.823) years. No significant difference in age and gender existed among the three groups (X2 = 0.83, P > 0.05). Best-corrected visual acuity (BCVA) was significantly lower in patients with early CPACG than in PA patients and controls, while BCVA was not significantly different between PA patients and controls (Fig. 1). Regarding IOP comparisons, patients with early CPACG were significantly higher than PA patients and controls, and the PA patients were not statistically different from the controls. Regarding the comparison of MD values, no significant difference in MD existed between the two case groups, but that of the case groups was significantly higher than that of the controls (Table 1).Fig. 1 (A–J) VD raw images (A–E) and VD binary images (F–J) of each layer of the macular area: A and F: DCP layer B and G: DVC layer. Cand H: ICP layer. D and I: SVC layer. E and J: SVP layer.

Table 1 Comparison of general data between case groups and control group.

	Case group1 (28 eyes)	Case group2 (30 eyes)	Control group (29 eyes)	F	P	P1-2	P1-3	P2-3	
BCVA (LogMAR)	0.407 ± 0.295	0.103 ± 0.118	0.117 ± 0.110	12.657	0.000*	0.000*	0.000*	0.782	
MD (dB)	− 2.157 ± 1.940	− 1.953 ± 2.091	− 0.169 ± 0.071	12.694	0.000*	0.639	0.000*	0.000*	
Age	62.857 ± 10.848	59.300 ± 6.114	59.069 ± 6.823	1.937	0.151	0.100	0.083	0.913	
IOP (mmHg)	22.964 ± 7.366	16.700 ± 2.306	15.241 ± 2.487	22.418	0.000*	0.000*	0.000*	0.229	
Case group 1 represents early CPACG patients. Case group 2 represents newly diagnosed PA patients.

Comparison of OCTA parameters between case groups and control group

Except for the SVP layer of the optic disk, the retinal blood flow density of the optic disk and macular area in early CPACG patients was smaller than that in PA patients (Table 2). Compared with the controls, the blood flow density of all layers of the optic disk and macular area in early CPACG patients decreased except for DCP, DVC and ICP of the optic disk and the optic disc SVP was smaller than the controls (Table 2).Table 2 Comparison of retinal OCTA parameters between case groups and control group (%).

Macular and optic disc OCTA parameters (%)	Case group1 (28 eyes)	Case group2 (30 eyes)	Control group (29 eyes)	F	P	P1-2	P1-3	P2-3	
Macular DCP	15.251 ± 6.501	23.382 ± 4.343	21.259 ± 5.921	11.647	0.000*	0.000*	0.001*	0.229	
Macular DVC	16.926 ± 6.262	26.307 ± 4.254	24.059 ± 5.891	16.418	0.000*	0.000*	0.000*	0.193	
Macular ICP	13.382 ± 5.838	21.746 ± 4.171	20.331 ± 5.770	14.891	0.000*	0.000*	0.000*	0.392	
Macular SVC	13.005 ± 5.511	20.833 ± 6.698	22.589 ± 6.529	13.915	0.000*	0.000*	0.000*	0.368	
Macular SVP	17.312 ± 7.291	27.821 ± 6.692	28.582 ± 8.628	14.496	0.000*	0.000*	0.000*	0.746	
Optic disc DCP	8.248 ± 4.845	11.531 ± 4.438	9.215 ± 4.079	4.183	0.019*	0.006*	0.415	0.050	
Optic disc DVC	10.352 ± 4.257	13.824 ± 4.691	12.083 ± 4.693	3.054	0.049*	0.016*	0.223	0.220	
Optic disc ICP	11.637 ± 4.221	15.459 ± 4.284	14.154 ± 4.795	4.018	0.023*	0.006*	0.071	0.345	
Optic disc SVC	21.061 ± 10.856	32.295 ± 7.043	34.133 ± 9.776	11.994	0.000*	0.000*	0.000*	0.527	
Optic disc SVP	18.412 ± 6.940	20.132 ± 3.808	24.316 ± 6.258	5.704	0.005*	0.325	0.002*	0.023*	
Optic disc RPCP	21.642 ± 12.890	35.667 ± 6.641	37.33 ± 9.994	15.091	0.000*	0.000*	0.000*	0.597	
Case group 1 represents early CPACG patients.

Case group 2 represents newly diagnosed PA patients.

Comparison of OCT parameters between case groups and control group

The thickness of CP-RNFL in each quadrant and average CP-RNFL thickness in early CPACG patients was thinner than those in PA patients. Compared with PA patients, early CPACG patients had thinner GCL and GCC layers in each quadrant of the macular inner ring and outer ring, and thinner IPL layer of the each quadrant of the macular inner ring, superior region of the macular outer ring and temporal region. Compared with the control group, the average CP-RNFL and CP-RNFL in each quadrant were thinner in patients with early CPACG, while there was no significant change in CP-RNFL thickness in PA patients (Fig. 2). Regarding macular region, compared with the controls, early CPACG patients had thinner GCL and GCC layers of each quadrant of the inner and outer ring and the IPL layers of each quadrant of the inner ring, and PA patients had thinner GCL and GCC layers of nasal region of the inner ring. The GCL, IPL and GCC layers of 1 mm macular center were not significantly different among the three groups (Table 3).Fig. 2 (A–L) VD raw images (A–F) and VD binary images (G–L) of each layer of the optic disk: A and G: DCP layer B and H: DVC layer. C and I: ICP layer. D and J: SVC layer. E and K: SVP layer. F and L: RPCP layer.

Table 3 Comparison of OCT parameters between case groups and control group.

OCT parameters (μm)	Case group1 (28 eyes)	Case group2 (30 eyes)	Control group (29 eyes)	F	P	P1-2	P1-3	P2-3	
Average CP-RNFL	82.303 ± 33.624	108.933 ± 11.614	108.284 ± 6.989	15.426	0.000*	0.000*	0.000*	0.904	
Nasal CP-RNFL	62.892 ± 31.458	78.833 ± 15.258	79.034 ± 11.794	5.491	0.006*	0.005*	0.005*	0.971	
Supra CP-RNFL	98.357 ± 45.720	133.333 ± 18.864	131.344 ± 13.672	12.838	0.000*	0.000*	0.000*	0.795	
Temporal CP-RNFL	65.928 ± 25.605	83.466 ± 14.618	80.655 ± 11.796	7.665	0.001*	0.000*	0.003*	0.554	
Inferior CP-RNFL	102.035 ± 44.637	140.366 ± 17.848	142.103 ± 14.283	17.839	0.000*	0.000*	0.000*	0.816	
Macular GCL, IPL, and GCC thickness									
Nasal-inner ring									
	39.785 ± 10.601	47.766 ± 7.074	51.586 ± 3.727	14.557	0.000*	0.000*	0.000*	0.013*	
	36.250 ± 6.107	40.633 ± 3.736	42.275 ± 2.962	13.968	0.000*	0.000*	0.000*	0.159	
	94.892 ± 18.369	108.833 ± 12.793	113.517 ± 7.048	13.145	0.000*	0.000*	0.000*	0.044*	
Supra-inner ring									
	43.571 ± 11.406	51.600 ± 5.340	52.103 ± 4.177	11.345	0.000*	0.000*	0.000*	0.799	
	36.285 ± 6.491	40.666 ± 3.187	41.275 ± 2.877	10.636	0.000*	0.000*	0.000*	0.601	
	101.821 ± 20.367	117.133 ± 9.412	117.379 ± 9.025	11.837	0.000*	0.000*	0.000*	0.946	
Temporal-inner ring									
	36.821 ± 10.694	47.233 ± 6.628	46.931 ± 4.174	20.028	0.000*	0.000*	0.000*	0.870	
	35.392 ± 6.436	41.033 ± 2.953	41.172 ± 2.619	16.626	0.000*	0.000*	0.000*	0.902	
	89.821 ± 16.913	105.466 ± 7.700	104.655 ± 6.677	17.377	0.000*	0.000*	0.000*	0.783	
Inferior-inner ring									
	42.107 ± 9.507	49.766 ± 7.285	51.137 ± 6.220	11.168	0.000*	0.000*	0.000*	0.499	
	35.321 ± 5.869	39.600 ± 4.263	40.724 ± 3.411	10.878	0.000*	0.001*	0.000*	0.351	
	98.857 ± 17.667	112.933 ± 13.763	115.448 ± 12.055	10.612	0.000*	0.000*	0.000*	0.511	
Nasal-outer ring									
	36.285 ± 7.117	40.466 ± 4.754	41.103 ± 3.177	7.094	0.001*	0.003*	0.001*	0.642	
	30.892 ± 5.065	30.000 ± 3.600	31.206 ± 3.783	0.544	0.582	0.317	0.778	0.469	
	104.071 ± 18.086	117.100 ± 13.483	118.655 ± 11.162	8.709	0.000*	0.001*	0.000*	0.681	
Supra-outer ring									
	30.535 ± 6.833	35.833 ± 4.202	35.620 ± 3.016	10.619	0.000*	0.000*	0.000*	0.868	
	27.285 ± 3.441	29.633 ± 3.123	26.896 ± 2.857	6.544	0.002*	0.006*	0.642	0.001*	
	87.892 ± 17.499	103.166 ± 10.379	101.862 ± 9.046	12.555	0.000*	0.000*	0.000*	0.696	
Temporal-outer ring									
	28.250 ± 8.605	37.633 ± 4.262	37.000 ± 4.017	22.122	0.000*	0.000*	0.000*	0.684	
	28.678 ± 4.675	33.866 ± 2.750	28.965 ± 4.221	16.076	0.000*	0.000*	0.784	0.000*	
	74.785 ± 13.436	91.300 ± 7.679	85.137 ± 6.838	21.351	0.000*	0.000*	0.000*	0.017*	
Inferior-outer ring									
	28.000 ± 6.091	33.766 ± 3.430	34.448 ± 3.660	17.445	0.000*	0.000*	0.000*	0.564	
	26.285 ± 3.241	28.066 ± 2.935	27.448 ± 2.873	2.585	0.081	0.270	0.150	0.433	
	83.535 ± 16.782	99.233 ± 10.695	101.793 ± 10.097	16.937	0.000*	0.000*	0.000*	0.445	
Central macula (within 1 mm diameter)									
	12.357 ± 5.806	14.733 ± 8.464	12.827 ± 3.536	1.167	0.316	0.155	0.779	0.249	
	17.214 ± 4.003	18.633 ± 5.235	17.689 ± 3.048	0.860	0.427	0.203	0.671	0.392	
	39.714 ± 12.174	44.933 ± 16.107	41.344 ± 8.303	1.300	0.278	0.120	0.628	0.279	

Comparison of OCT and OCTA parameters in diagnostic test performance

To evaluate the diagnostic ability of OCT and OCTA parameters, we calculated the receiver operating characteristic curve (ROC) of some OCT and OCTA parameters in early CPACG and PA patients, respectively, and the ROC area under the curve (AUC) in Fig. 3. We described the parameters with relatively large AUC values as follows. The AUC of CP-RNFL thickness in the superior and inferior were 0.807 and 0.844, respectively (Fig. 3A), that of the GCL and GCC in the nasal region of the macular inner ring was 0.878 and 0.875 (Fig. 3B), that of GCC and GCL in the macular outer ring were 0.819 and 0.814, respectively (Fig. 3C) and that of the optic disk SVC and macular SVC was 0.840 and 0.889, respectively (Fig. 3D). Z-test showed that the comparison of AUC of maximum OCT parameters and OCTA parameters showed no statistical significance between the two groups (Z optic disc inferior CP-RNFL –optic disc SVC = –0.044, P = 1.035; Zoptic disc inferior CP-RNFL –macular SVC = –0.504, P = 1.386; ZGCL of nasal inner ring –optic disc SVC = 0.426, P = 1.329; ZGCL of nasal inner ring –macular SVC = 0.123, P = 0.901). In PA patients, the AUC of optic disc SVP was 0.760, and the AUC of GCL and GCC in macular inner ring nasal region were 0.673 and 0.637, respectively. Z test showed that there was no statistically significant difference between any two groups (ZSVP-GCL = –0.910, P = 1.637; ZSVP-GCC = –1.268, P = 1.801). These data suggest that OCTA parameters and OCT parameters have similar diagnostic efficacy for early CPACG and PA patients.Fig. 3 AUC area under ROC of OCT and OCTA parameters in early CPACG and PA patients. (A) AUC area under ROC of CP-RNFL thickness in each quadrant in CPACG patients. (B, C) AUC area under the ROC curve of the thickness of the GCL, IPL, and GCC layers in each quadrant of the macular inner ring (B) and the GCL and GCC layers in each quadrant of the macular outer ring (C) in CPACG patients. (D) AUC area under the ROC curve of the thickness of the SVP, SVC and RPCP of the optic disk, and DCP, DVC, ICP, SVC, and SVP of macula in CPACG patients.

Discussion

Despite the different pathogenesis of CPACG and PA, patients with both diseases show impaired retinal circulation and structural thinning of the RNFL. Jo Y.H. et al.15 and Wang X. et al.16 found that persistently elevated IOP in PACG patients may have adverse effects on retinal circulation and induce retinal ischemic damage, leading to retinal VD loss and RNFL thickness reduction. Many possible mechanisms for visual acuity and visual field damage after the compression of the optic chiasm by PA tumors were proposed17, including ischemic damage, demyelinating lesions, retrograde degeneration, and anterograde degeneration, which are manifested as the thinning of the GCC layer in the retina, which has been confirmed by previous studies including our previous study18,19. A study using OCTA measurement found that the density of RPCP and superficial capillary plexus in the macular area of PA patients was reduced20, which was presumed to be due to the tumor growth compressing the optic chiasm, leading to axoplasmic transport block and blood pressure supply reduction, and finally manifested as retinal vascular atrophy. Regarding the differences in the changes in optic nerve retinal structure and blood flow between glaucoma and compressive optic neuropathy, the relevant research literature has been published recently. For example, Alon Zahavi et al. compared the differences in OCT and OCTA parameters of the optic nerve in patients with open-angle glaucoma and pituitary adenoma21. Kun Lei et al. studied the differences in optic nerve retinal structure and blood flow density between open-angle glaucoma and compressive optic neuropathy22. Eun Jung Lee et al. compared the differences in optic nerve retinal structure and blood flow density between patients with normal tension glaucoma and compressive optic neuropathy23. In contrast, the current study is the first to compare the structure and flow density of the optic nerve and retina between patients with early CPACG and early PA.

Our study found that compared with early PA patients, early CPACG patients had lower retinal blood flow density of each layer of the optic disk and macular area except the optic disc SVP layer and thinner average CP-RNFL, GCL and GCC layers in each quadrants of macular inner and outer ring, and IPF layer in each quadrants of macular inner, the superior and temporal regions of the macular outer ring. Our results are similar to those of previous studies, which showed that in the case of a similar degree of structural damage, the degree of retinal vascular damage in compressive optic neuropathy is less severe than that in open Angle glaucoma, especially in the macular area22. In a study in which a silicone balloon was implanted into the orbit of cats to mimic a growing orbital tumor, the nerve fibers were extensively demyelinated within the first week, even some fibers were even completely degenerated, and the axons were partially or completely demyelinated24. But after 5 weeks, many axons had remyelination despite the persistence of the orbital mass. From these findings, it can be speculated that although the demyelination of axons occurs in PA patients after the chiasm is compressed by the tumor, the whole course of the disease is slow, and many damaged axons remyelination during the disease. Based on the above literature, we speculate that part of the reason for the differences in retinal structure and blood flow density between PA patients and PACG patients is as follows. Firstly, In PACG patients, persistently elevated IOP affects retinal blood circulation, and induces apoptosis to cause the thinning of the GCL layer and RNFL, which together lead to the reduction of retinal blood flow density. In PA, the neural axis of the compressed optic chiasm is slowly demyelinated and cooccurs with remyelination, which provides a buffer time for structural changes in the GCL. As a result, the damage of the GCL and RNFL layer is lighter than that of PACG, and the decrease of retinal oxygen demand is slow, resulting in the degree of retinal vascular atrophy also lighter. Previous studies have suggested that patients do not develop visual field defects until at least 30% of retinal ganglion cells die17. Our previous related studies found that the functional damage of PA eyes and the structural damage of the visual pathway seem to be matched21, which also explains why the same degree of visual field defects, but the retinal structural damage of glaucoma is more serious. Of course, further studies are needed to confirm this phenomenon.

Our study also found that the AUC of blood flow density in PACG patients was not statistically different from the AUC of structural parameters, which is similar to the results of Rao et al.25, but different from Lin YD et al.26. The reason for this may be that the average deviation of VF in our study is more similar to the conditions of the former study (< –6.0 dB versus -9.2 dB) rather than the latter study (< –6.0 dB versus –19.4 dB). Compared with functional parameters, structural parameters of advanced glaucoma are more susceptible to the floor effect27, a phenomenon that OCT has limitations in detecting RNFL thickness thinning when retinal RNFL is rarely below 50 μm in advanced glaucoma with residual vascular tissue and glial tissue,

In our study, when VF function was mildly impaired in PA patients, the optic disc SVP became smaller and the deep retinal VD was not statistically different compared with normal controls. Our finding is similar to the results of Dallorto, L et al.28, who found that compared with healthy eyes, the optic disc VD and macular VD of the superficial vascular plexus in PA patients were significantly reduced, and no change was found in the deep retinal VD. Our study also found that the AUC of optic disc SVP in PA patients was not statistically different from that of GCL and GCC on the nasal region of the macular inner ring, which was different from the study of Tang, Y et al.29, who believed that the AUC of RPCP on the temporal region of the optic disk in PA patients was 0.821, which had the highest diagnostic efficiency for VF abnormalities. It can be concluded that OCTA parameters can be used as markers for evaluating nerve damage in PA. Regarding retinal structure, PA patients in our study mainly showed the thinning of GCL and GCC layers on the nasal side of the inner macular ring, which was similar to the results of a previous study that found that early PA mainly manifested as the thinning of the quadrants of GCL, IPL and GCC layers21, especially on the nasal region of the macular30. In view of this phenomenon, we consider the following reasons: we know that the RNFL is composed of RGC axons, the GCL is composed of RGC cell bodies, and the IPL is composed of RGC dendrites31. Under normal conditions, a vertical line is drawn through the fovea, and the RNFL of the retina is divided into nasal crossing fibers and temporal non-crossing fibers. The nasal RNFL drained into the nasal and temporal sides of the optic disk. The temporal RNFL drains predominantly into the superior and inferior regions of the optic disk. The macular RNFL in nasal region belongs to crossing fibers, and its retrograde degeneration after compression can occur in the early stage, leading to RGC dysfunction and/or apoptosis, which are manifested as thinning of the macular GCL and GCC layers in the nasal region. The reasons for this phenomenon are as follows: as crossing fibers, macular RNFL in the nasal region suffers from retrograde degeneration after compression in the early stage and leads to RGC dysfunction and/or apoptosis, which are manifested as the thinning of the GCL and GCC layers in the macular of nasal region.

The limitations of this study are as follows: firstly, this study is a cross-sectional study and lacks follow-up data; secondly, this study included small sample size, only involving early CPACG and early PA patients, and did not include enough cases for stratified study, which is also the experiment we will carry out further.

In conclusion, in the case of similar visual field damage, compared with early PA eyes, the blood flow density of the optic disk and macular area in early CPACG eyes is smaller, and the thickness of the optic disk and macular area is thinner, which is considered to be related to the different pathogenesis of the two diseases. OCTA parameters have similar performance to OCT parameters in the diagnosis of early CPACG and early PA.

Material and methods

Research objects

This was a retrospective clinical case–control study. We enrolled early CPACG patients who were diagnosed in the Department of Ophthalmology (termed case group 1), and early PA patients with mild chiasmal compression who were newly diagnosed by magnetic resonance imaging and postoperative pathological examination in the Department of Neurosurgery (termed case group 2) from the Affiliated Hospital of Guangdong Medical University from March 2022 to September 2023. Twenty-nine normal subjects (29 eyes) were enrolled as the control group. The diagnostic criteria of CPACG met the following characteristics32–34: (1) an elevated IOP (non-contact IOP ≥ 21 mmHg); (2) a narrow synechial angle; (3) no history and no ocular signs of an acute glaucoma attack; (4) more than three cumulative clock-hours of peripheral anterior synechiae by gonioscopy; 5) glaucomatous optic neuropathy or visual field defect. Early CPACG was defined as the visual field MD values > –6 dB based on a previous study8. Similarly, the visual field MD values of subjects included in case group 2 were also > –6 dB. All subjects underwent best corrected visual acuity (BCVA), non-contact tonometry, visual field, optic disk, and macular OCT and OCTA examinations. The study was conducted following the tenets of the Declaration of Helsinki, all participants provided written informed consent, and the study data were approved by the ethics committee of the Affiliated Hospital of Guangdong Medical University (No. PJKT2022-145).

Inclusion and exclusion criteria for case group 1 and case group 2: (1) no previous history of intracranial disease, trauma, or intracranial surgery; no history of ocular trauma, disregard of optic nerve retinal disease, and no history of intraocular surgery; (2) no glaucoma in PA patients; (3) refractive error <  ± 6.0D (spherical lens) and < 3.00D (cylindrical lens). (4) OCT and OCTA images are clear enough for data calculation and analysis; (5) patients with unclear diagnoses of PACG and PA were excluded.

Inclusion and exclusion criteria of normal control group: (1) non-contact intraocular pressure ≤ 21 mmHg; (2) visual acuity or corrected visual acuity ≥ 0.8, refractive error <  ± 6.0D (spherical) and < 3.00 D (cylindrical); (3) no previous history of intracranial disease, trauma, or intracranial surgery; (4) no history of ocular trauma, glaucoma, optic nerve retinal disease, and intraocular surgery; (5) age- and gender-matched with the case groups. (6) OCT and OCTA images are clear enough for data calculation and analysis.

Visual field examination

Visual field examination (KowaAP7000 precision visual field meter, Kowa, Japan) was performed after correction of ametropia in the case group before surgery and in the control group. Reliable visual field tests were performed twice in all subjects. Visual-field tests assessed the central 30 degrees and were considered unreliable if fixation was lost, false negative or false positive errors exceeded 20%. The MD value of the visual field was a parameter used to assess the global visual field defect.

Magnetic resonance imaging of the tumor of PA patients

All patients in the PA group underwent a head magnetic resonance plain scan and enhanced examination (Discovery MR750 3.0t, GE, USA). All patients with PA underwent postoperative pathological examination of the tumor. Tumors were graded according to the compression of the tumor on the optic chiasm35 Grade 0 was defined as no contact between the tumor and the optic chiasm. Grade 1 was defined as contact between the tumor and the optic chiasm but no deformation of the optic chiasm surface. Grade 2 was defined as contact between the tumor and the optic chiasm, and there was deformation of the optic chiasm surface, but the suprachiasmatic cisterna was still visible. Grade 3 was defined as contact between the tumor and the optic chiasm, malformation of the upper surface of the optic chiasm, invisibility of the superior cisterna of the optic chiasm, and anencephaly. Grade 4 had brain malformations in addition to the above changes.

OCT and OCTA examination

The CP-RNFL thickness, GCC thickness, IPL and GCL thickness were measured by OCT (Heideberg Engineering Spectralis, German) by the same experienced ophthalmoscope. Scanning was performed using a swept-frequency laser source with a central wavelength of 870 nm at a rate of 8.8 frames per second with high-speed scanning resolution. The CP-RNFL thickness was collected from the center of the optic disk using the international standard diameter 3.45 mm ring mode (768A-scans). The macular area was acquired by volume scanning mode scanning frame, with the macular fovea as the center, and the scanning area was 8.8 mm × 8.8 mm (31 lines, 240 μm interval, 768A-scans). The total thickness of RNFL, GCL, and IPL was defined as GCC. Vessel density (VD) images were obtained by OCTA with High Res resolution (5.7um/ pixel), foveal as the center, and range of 3 mm × 3 mm (6 μm interval, 512A-scans). An OCTA with a range of 6 mm × 6 mm was used to obtain the peripapillary VD images at each level. The VD of the optic disk includes radial peripapillary capillaries plexus (RPCP), superfical vascular complex (SVC), (superfical vascular plexus, SVP), (intermediate capillary plexus, ICP), (deep vascular complex, DVC), deep capillary plexus (DCP); VD in the macular region included SVC, SVP, ICP, DVC, and DCP.

Image processing and analysis methods

The original VD images of SVC, DVC, SVP, ICP, and DCP of the optic disk and macular area were exported from the OCTA database (Figs. 1A–E and 2A–F), and the images were processed and calculated by Image J software (version 1.53 for Mac) in 8-bit gray scale format with image threshold set. Photographs were binarized to clearly distinguish microvessels (Figs. 1F–J and 2G–L), and then VD at different levels was calculated, which was defined as the percentage of area occupied by blood vessels in the image36.

Statistical analysis

The final sample size was calculated by PASS software (version 23.0.3) according to the mean and standard deviation of each group in the pre-experiment. Data analysis was performed by SPSS 24.0 statistical software (SPSS Inc., Chicago, IL, USA). Continuous variables that met the normality requirements of the Shapiro–Wilk test were expressed as mean ± standard deviation (mean ± SD). Independent sample t-test was used for comparison between groups. The chi-square test was used for comparison of count data between groups. One-way analysis of variance was used to compare the parameters among three groups and multiple groups, followed by an LSD-t test for pairwise comparison. The area under the ROC curve of OCT and OCTA parameters was calculated, and the area under the ROC curve of each parameter was compared by the Z test to evaluate the diagnostic ability of OCT and OCTA parameters. P < 0.05 was considered statistically significant.

Acknowledgements

The authors are grateful to Quan-wen Zhao for his help with the data acquisition in this paper.

Author contributions

P. YH and T. Z contributed to the conception or design of the work. L. KL, Z. WC, Z, P. SY, W. XJ, and D. TT were responsible for data acquisition. P. YH and T. Z were responsible for data analysis, manuscript writing, and manuscript modification and science supervision. P. YH and W. XJ were responsible for manuscript submission and revision. All authors reviewed and approved the final manuscript.

Funding

This study was supported by Science and Technology Program project of Zhanjiang (230830214544759).

Data availability

The datasets generated and analyzed in this study are available from the corresponding author on reasonable request.

Competing interests

The authors declare no competing interests.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References

1. Wu X Wang Y Liu X Li ZH Deng LQ Chen DS Wang DJ Outcomes of chronic angle-closure glaucoma treated by phacoemulsification and endocyclophotocoagulation with or without endoscopically goniosynechialysis Int. J. Ophthalmol. 2022 15 8 1273 1278 10.18240/ijo.2022.08.08 36017042
Wu, X. et al. Outcomes of chronic angle-closure glaucoma treated by phacoemulsification and endocyclophotocoagulation with or without endoscopically goniosynechialysis. Int. J. Ophthalmol. 15(8), 1273–1278 (2022).36017042 10.18240/ijo.2022.08.08
2. Tham YC Li X Wong TY Quigley HA Aung T Cheng CY Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis Ophthalmology 2014 121 11 2081 2090 10.1016/j.ophtha.2014.05.013 24974815
Tham, Y. C. et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology 121(11), 2081–2090 (2014).24974815 10.1016/j.ophtha.2014.05.013
3. George R Panda S Vijaya L Blindness in glaucoma: primary open-angle glaucoma versus primary angle-closure glaucoma-a meta-analysis Eye (Lond) 2022 36 11 2099 2105 10.1038/s41433-021-01802-9 34645961
George, R., Panda, S. & Vijaya, L. Blindness in glaucoma: primary open-angle glaucoma versus primary angle-closure glaucoma-a meta-analysis. Eye (Lond) 36(11), 2099–2105 (2022).34645961 10.1038/s41433-021-01802-9
4. R. Sihota, An Indian perspective on primary angle closure and glaucoma, Indian J Ophthalmol 59 Suppl(Suppl1), S76–81. (2011).
5. Leung CKS Lam AKN Weinreb RN Garway-Heath DF Yu M Guo PY Chiu VSM Wan KHN Wong M Wu KZ Cheung CYL Lin C Chan CKM Chan NCY Kam KW Lai GWK Diagnostic assessment of glaucoma and non-glaucomatous optic neuropathies via optical texture analysis of the retinal nerve fibre layer Nat. Biomed. Eng. 2022 6 5 593 604 10.1038/s41551-021-00813-x 34992272
Leung, C. K. S. et al. Diagnostic assessment of glaucoma and non-glaucomatous optic neuropathies via optical texture analysis of the retinal nerve fibre layer. Nat. Biomed. Eng. 6(5), 593–604 (2022).34992272 10.1038/s41551-021-00813-x
6. Wang X Chou Y Zhu H Xing B Yao Y Lu L You H Gan L Wang M Ma J Zhong Y Retinal Microvascular Alterations Detected by Optical Coherence Tomography Angiography in Nonfunctioning Pituitary Adenomas Transl. Vis. Sci. Technol. 2022 11 1 5 10.1167/tvst.11.1.5 36342707
Wang, X. et al. Retinal Microvascular Alterations Detected by Optical Coherence Tomography Angiography in Nonfunctioning Pituitary Adenomas. Transl. Vis. Sci. Technol. 11(1), 5 (2022).36342707 10.1167/tvst.11.1.5
7. Dias DT Ushida M Battistella R Dorairaj S Prata TS Neurophthalmological conditions mimicking glaucomatous optic neuropathy: Analysis of the most common causes of misdiagnosis BMC Ophthalmol. 2017 17 1 2 10.1186/s12886-016-0395-x 28073365
Dias, D. T., Ushida, M., Battistella, R., Dorairaj, S. & Prata, T. S. Neurophthalmological conditions mimicking glaucomatous optic neuropathy: Analysis of the most common causes of misdiagnosis. BMC Ophthalmol. 17(1), 2 (2017).28073365 10.1186/s12886-016-0395-x
8. Wu JH Moghimi S Nishida T Mohammadzadeh V Kamalipour A Zangwill LM Weinreb RN Association of macular OCT and OCTA parameters with visual acuity in glaucoma Br. J. Ophthalmol. 2023 107 11 1652 1657 10.1136/bjo-2022-321460 36126109
Wu, J. H. et al. Association of macular OCT and OCTA parameters with visual acuity in glaucoma. Br. J. Ophthalmol. 107(11), 1652–1657 (2023).36126109 10.1136/bjo-2022-321460
9. Wong D Chua J Tan B Yao X Chong R Sng CCA Husain R Aung T Garway-Heath D Schmetterer L Combining OCT and OCTA for Focal Structure-Function Modeling in Early Primary Open-Angle Glaucoma Invest. Ophthalmol. Vis. Sci. 2021 62 15 8 10.1167/iovs.62.15.8 34878500
Wong, D. et al. Combining OCT and OCTA for Focal Structure-Function Modeling in Early Primary Open-Angle Glaucoma. Invest. Ophthalmol. Vis. Sci. 62(15), 8 (2021).34878500 10.1167/iovs.62.15.8
10. Mohammadzadeh V Fatehi N Yarmohammadi A Lee JW Sharifipour F Daneshvar R Caprioli J Nouri-Mahdavi K Macular imaging with optical coherence tomography in glaucoma Surv. Ophthalmol. 2020 65 6 597 638 10.1016/j.survophthal.2020.03.002 32199939
Mohammadzadeh, V. et al. Macular imaging with optical coherence tomography in glaucoma. Surv. Ophthalmol. 65(6), 597–638 (2020).32199939 10.1016/j.survophthal.2020.03.002
11. Pujari A Bhaskaran K Sharma P Singh P Phuljhele S Saxena R Azad SV Optical coherence tomography angiography in neuro-ophthalmology: Current clinical role and future perspectives Surv. Ophthalmol. 2021 66 3 471 481 10.1016/j.survophthal.2020.10.009 33157113
Pujari, A. et al. Optical coherence tomography angiography in neuro-ophthalmology: Current clinical role and future perspectives. Surv. Ophthalmol. 66(3), 471–481 (2021).33157113 10.1016/j.survophthal.2020.10.009
12. Ben Ghezala I Haddad D Blanc J Meillon C Madkouri R Borsotti F Bron AM Creuzot-Garcher, Peripapillary Microvascularization Analysis Using Swept-Source Optical Coherence Tomography Angiography in Optic Chiasmal Compression J. Ophthalmol. 2021 2021 5531959 34527375
Ben Ghezala, I. et al. Creuzot-Garcher, Peripapillary Microvascularization Analysis Using Swept-Source Optical Coherence Tomography Angiography in Optic Chiasmal Compression. J. Ophthalmol. 2021, 5531959 (2021).34527375
13. Lee GI Park KA Oh SY Kong DS Changes in parafoveal and peripapillary perfusion after decompression surgery in chiasmal compression due to pituitary tumors Sci. Rep. 2021 11 1 3464 10.1038/s41598-021-82151-1 33568736
Lee, G. I., Park, K. A., Oh, S. Y. & Kong, D. S. Changes in parafoveal and peripapillary perfusion after decompression surgery in chiasmal compression due to pituitary tumors. Sci. Rep. 11(1), 3464 (2021).33568736 10.1038/s41598-021-82151-1
14. Cennamo G Solari D Montorio D Scala MR D'Andrea L Tranfa F Cavallo LM The role of OCT- angiography in predicting anatomical and functional recovery after endoscopic endonasal pituitary surgery: A 1-year longitudinal study PLoS One 2021 16 12 e0260029 10.1371/journal.pone.0260029 34855775
Cennamo, G. et al. The role of OCT- angiography in predicting anatomical and functional recovery after endoscopic endonasal pituitary surgery: A 1-year longitudinal study. PLoS One 16(12), e0260029 (2021).34855775 10.1371/journal.pone.0260029
15. Jo YH Sung KR Shin JW Comparison of Peripapillary Choroidal Microvasculature Dropout in Primary Open-angle Primary Angle-closure, and Pseudoexfoliation Glaucoma J. Glaucoma 2020 29 12 1152 1157 10.1097/IJG.0000000000001650 32890109
Jo, Y. H., Sung, K. R. & Shin, J. W. Comparison of Peripapillary Choroidal Microvasculature Dropout in Primary Open-angle Primary Angle-closure, and Pseudoexfoliation Glaucoma. J. Glaucoma 29(12), 1152–1157 (2020).32890109 10.1097/IJG.0000000000001650
16. Wang X Chen J Kong X Sun X Immediate Changes in Peripapillary Retinal Vasculature after Intraocular Pressure Elevation -an Optical Coherence Tomography Angiography Study Cur. Eye Res. 2020 45 6 749 756 10.1080/02713683.2019.1695843
Wang, X., Chen, J., Kong, X. & Sun, X. Immediate Changes in Peripapillary Retinal Vasculature after Intraocular Pressure Elevation -an Optical Coherence Tomography Angiography Study. Cur. Eye Res. 45(6), 749–756 (2020).10.1080/02713683.2019.1695843
17. Danesh-Meyer HV Yoon JJ Lawlor M Savino PJ Visual loss and recovery in chiasmal compression Prog. Retin. Eye Res. 2019 73 100765 10.1016/j.preteyeres.2019.06.001 31202890
Danesh-Meyer, H. V., Yoon, J. J., Lawlor, M. & Savino, P. J. Visual loss and recovery in chiasmal compression. Prog. Retin. Eye Res. 73, 100765 (2019).31202890 10.1016/j.preteyeres.2019.06.001
18. Biousse V Danesh-Meyer HV Saindane AM Lamirel C Newman NJ Imaging of the optic nerve: Technological advances and future prospects Lancet Neurol. 2022 21 12 1135 1150 10.1016/S1474-4422(22)00173-9 36155662
Biousse, V., Danesh-Meyer, H. V., Saindane, A. M., Lamirel, C. & Newman, N. J. Imaging of the optic nerve: Technological advances and future prospects. Lancet Neurol. 21(12), 1135–1150 (2022).36155662 10.1016/S1474-4422(22)00173-9
19. Pang Y Tan Z Chen X Liao Z Yang X Zhong Q Huang B Zhong Q Zhong J Mo W Evaluation of preoperative visual pathway impairment in patients with non-functioning pituitary adenoma using diffusion tensor imaging coupled with optical coherence tomography Front Neurosci 2023 17 1057781 10.3389/fnins.2023.1057781 36845438
Pang, Y. et al. Evaluation of preoperative visual pathway impairment in patients with non-functioning pituitary adenoma using diffusion tensor imaging coupled with optical coherence tomography. Front Neurosci 17, 1057781 (2023).36845438 10.3389/fnins.2023.1057781
20. Cennamo G Solari D Montorio D Scala MR Melenzane A Fossataro F Somma T Tranfa F Cavallo LM Early vascular modifications after endoscopic endonasal pituitary surgery: The role of OCT-angiography PLoS One 2020 15 10 e0241295 10.1371/journal.pone.0241295 33119707
Cennamo, G. et al. Early vascular modifications after endoscopic endonasal pituitary surgery: The role of OCT-angiography. PLoS One 15(10), e0241295 (2020).33119707 10.1371/journal.pone.0241295
21. Zahavi A Weinberger Y Geffen N Gabbay I Mimouni M Gal-Or O Stiebel-Kalish H Gaton DD Optical Coherence Tomography Angiography for the Differentiation of Glaucoma from Pituitary Macroadenoma Related Optic Disc Measurements Semin. Ophthalmol. 2023 38 7 625 629 10.1080/08820538.2023.2177116 36762773
Zahavi, A. et al. Optical Coherence Tomography Angiography for the Differentiation of Glaucoma from Pituitary Macroadenoma Related Optic Disc Measurements. Semin. Ophthalmol. 38(7), 625–629 (2023).36762773 10.1080/08820538.2023.2177116
22. Lei K Tang Y Pang R Zhou H Yang L Wang N Comparison of the retinal microvasculature between compressive and glaucomatous optic neuropathy Graefes. Arch. Clin. Exp. Ophthalmol. 2023 261 12 3589 3597 10.1007/s00417-023-06137-7 37347246
Lei, K. et al. Comparison of the retinal microvasculature between compressive and glaucomatous optic neuropathy. Graefes. Arch. Clin. Exp. Ophthalmol. 261(12), 3589–3597 (2023).37347246 10.1007/s00417-023-06137-7
23. Lee EJ Han JC Kee C Park KA Kong DS Hong SD Peripapillary vascular density in compressive optic neuropathy and normal-tension glaucoma: a severity-controlled comparison Invest. Ophthalmol. Vis. Sci. 2023 64 12 10 10.1167/iovs.64.12.10 37796490
Lee, E. J. et al. Peripapillary vascular density in compressive optic neuropathy and normal-tension glaucoma: a severity-controlled comparison. Invest. Ophthalmol. Vis. Sci. 64(12), 10 (2023).37796490 10.1167/iovs.64.12.10
24. Clifford-Jones RE Landon DN McDonald WI Remyelination during optic nerve compression J. Neurol. Sci. 1980 46 2 239 243 10.1016/0022-510X(80)90082-9 7381514
Clifford-Jones, R. E., Landon, D. N. & McDonald, W. I. Remyelination during optic nerve compression. J. Neurol. Sci. 46(2), 239–243 (1980).7381514 10.1016/0022-510X(80)90082-9
25. Rao HL Kadambi SV Weinreb RN Puttaiah NK Pradhan ZS Rao DAS Kumar RS Webers CAB Shetty R Diagnostic ability of peripapillary vessel density measurements of optical coherence tomography angiography in primary open-angle and angle-closure glaucoma Br. J. Ophthalmol. 2017 101 8 1066 1070 10.1136/bjophthalmol-2016-309377 27899368
Rao, H. L. et al. Diagnostic ability of peripapillary vessel density measurements of optical coherence tomography angiography in primary open-angle and angle-closure glaucoma. Br. J. Ophthalmol. 101(8), 1066–1070 (2017).27899368 10.1136/bjophthalmol-2016-309377
26. Lin Y Chen S Zhang M Peripapillary vessel density measurement of quadrant and clock-hour sectors in primary angle closure glaucoma using optical coherence tomography angiography BMC Ophthalmol. 2021 21 1 328 10.1186/s12886-021-02093-0 34503457
Lin, Y., Chen, S. & Zhang, M. Peripapillary vessel density measurement of quadrant and clock-hour sectors in primary angle closure glaucoma using optical coherence tomography angiography. BMC Ophthalmol. 21(1), 328 (2021).34503457 10.1186/s12886-021-02093-0
27. Suzuki Y Kiyosawa M Visual Acuity in Glaucomatous Eyes Correlates Better with Visual Field Parameters than with OCT Parameters Curr. Eye Res. 2021 46 11 1717 1723 10.1080/02713683.2021.1924384 33910431
Suzuki, Y. & Kiyosawa, M. Visual Acuity in Glaucomatous Eyes Correlates Better with Visual Field Parameters than with OCT Parameters. Curr. Eye Res. 46(11), 1717–1723 (2021).33910431 10.1080/02713683.2021.1924384
28. Dallorto L Lavia C Jeannerot AL Shor N Jublanc C Boch AL Bodaghi B Tadayoni R Touitou V Bonnin S Retinal microvasculature in pituitary adenoma patients: is optical coherence tomography angiography useful? Acta. Ophthalmol. 2020 98 5 e585 e592 10.1111/aos.14322 31808290
Dallorto, L. et al. Retinal microvasculature in pituitary adenoma patients: is optical coherence tomography angiography useful?. Acta. Ophthalmol. 98(5), e585–e592 (2020).31808290 10.1111/aos.14322
29. Tang Y Liang X Xu J Wang K Jia W The Value of Optical Coherence Tomography Angiography in Pituitary Adenomas J. Integr. Neurosci. 2022 21 5 142 10.31083/j.jin2105142 36137972
Tang, Y., Liang, X., Xu, J., Wang, K. & Jia, W. The Value of Optical Coherence Tomography Angiography in Pituitary Adenomas. J. Integr. Neurosci. 21(5), 142 (2022).36137972 10.31083/j.jin2105142
30. Sun M Zhang Z Ma C Chen S Chen X Quantitative analysis of retinal layers on three-dimensional spectral-domain optical coherence tomography for pituitary adenoma PLoS One 2017 12 6 e0179532 10.1371/journal.pone.0179532 28628662
Sun, M., Zhang, Z., Ma, C., Chen, S. & Chen, X. Quantitative analysis of retinal layers on three-dimensional spectral-domain optical coherence tomography for pituitary adenoma. PLoS One 12(6), e0179532 (2017).28628662 10.1371/journal.pone.0179532
31. Seung HS Sumbul U Neuronal cell types and connectivity: lessons from the retina Neuron 2014 83 6 1262 1272 10.1016/j.neuron.2014.08.054 25233310
Seung, H. S. & Sumbul, U. Neuronal cell types and connectivity: lessons from the retina. Neuron 83(6), 1262–1272 (2014).25233310 10.1016/j.neuron.2014.08.054
32. Huang HL Wang GH Niu LL Sun XH Three-dimensional choroidal vascularity index and choroidal thickness in fellow eyes of acute and chronic primary angle-closure using swept-source optical coherence tomography Int. J. Ophthalmol. 2024 17 1 42 52 10.18240/ijo.2024.01.06 38239961
Huang, H. L., Wang, G. H., Niu, L. L. & Sun, X. H. Three-dimensional choroidal vascularity index and choroidal thickness in fellow eyes of acute and chronic primary angle-closure using swept-source optical coherence tomography. Int. J. Ophthalmol. 17(1), 42–52 (2024).38239961 10.18240/ijo.2024.01.06
33. Shang K Hu X Dai Y Morphological features of parapapillary beta zone and gamma zone in chronic primary angle-closure glaucoma Eye (Lond) 2019 33 9 1378 1386 10.1038/s41433-019-0541-9 31406353
Shang, K., Hu, X. & Dai, Y. Morphological features of parapapillary beta zone and gamma zone in chronic primary angle-closure glaucoma. Eye (Lond) 33(9), 1378–1386 (2019).31406353 10.1038/s41433-019-0541-9
34. Foster PJ Buhrmann R Quigley HA Johnson GJ The definition and classification of glaucoma in prevalence surveys Br. J. Ophthalmol. 2002 86 2 238 242 10.1136/bjo.86.2.238 11815354
Foster, P. J., Buhrmann, R., Quigley, H. A. & Johnson, G. J. The definition and classification of glaucoma in prevalence surveys. Br. J. Ophthalmol. 86(2), 238–242 (2002).11815354 10.1136/bjo.86.2.238
35. Fujimoto N Saeki N Miyauchi O Adachi-Usami E Criteria for early detection of temporal hemianopia in asymptomatic pituitary tumor Eye (Lond) 2002 16 6 731 738 10.1038/sj.eye.6700165 12439668
Fujimoto, N., Saeki, N., Miyauchi, O. & Adachi-Usami, E. Criteria for early detection of temporal hemianopia in asymptomatic pituitary tumor. Eye (Lond) 16(6), 731–738 (2002).12439668 10.1038/sj.eye.6700165
36. Al-Sheikh M Ghasemi Falavarjani K Akil H Sadda SR Impact of image quality on OCT angiography based quantitative measurements Int. J. Retina Vitreous 2017 3 1 6 10.1186/s40942-017-0068-9 28078103
Al-Sheikh, M., Ghasemi Falavarjani, K., Akil, H. & Sadda, S. R. Impact of image quality on OCT angiography based quantitative measurements. Int. J. Retina Vitreous 3, 1–6 (2017).28078103 10.1186/s40942-017-0068-9
