Skip to main content
Ophthalmology Science logoLink to Ophthalmology Science
. 2024 Nov 10;5(2):100654. doi: 10.1016/j.xops.2024.100654

Decreased Choriocapillaris Vessel Density in the Ipsilateral Eye after Carotid Artery Revascularization Detected by Widefield Swept-Source OCT Angiography

Li Zhang 1,, Jia-Wei Liu 1,, Qing-Qing Tang 1,, Chun-Yan Lei 1, Xue Lin 2, Sheng Gao 1, Tian-Yu Yang 1, Fa-Yun Hu 2,, Mei-Xia Zhang 1,∗∗
PMCID: PMC11730213  PMID: 39811266

Abstract

Objective

To investigate the short-term blood flow changes and image features of the retina and choroid in patients who underwent carotid artery revascularization (CAR) for severe carotid artery stenosis using widefield swept-source OCT angiography (OCTA).

Design

Prospective study.

Participants

This prospective study included 112 eyes (56 eyes on the ipsilateral side and 56 eyes on the contralateral side) of 56 participants with severe carotid artery stenosis.

Methods

Participants were examined using widefield swept-source OCTA covering an area of 16 × 16 mm centered on the fovea before and after CAR. Retinal parameters including central macular thickness, vessel density of the retinal superficial vascular complex (VDRSVC), vessel density of the retinal deep vascular complex, and vessel density of the retina (VDR) and choroidal parameters, including central choroidal thickness (CCT), vessel density of the choriocapillaris (VDCC), vessel density of the medium and large choroidal vessels, choroidal vessel volume ratio (CVV/a), and 3-dimensional choroidal vascularity index (3D-CVI) were measured. Besides, preoperative and postoperative OCTA images were screened and compared.

Main Outcome Measures

Retinal and choroidal parameters obtained from swept-source OCTA.

Results

In the ipsilateral eye (56 eyes), an increase in VDRSVC, VDR, CVV/a, CCT, and 3D-CVI and a decrease in VDCC was found after CAR. Thirteen patients were identified with postoperative ipsilateral choriocapillaris flow voids (PICCFVs) with OCTA images, and the presence of PICCFVs was associated with greater postoperative VDCC decrease. In the contralateral eye (56 eyes), we found an increase in VDRSVC, vessel density of the retinal deep vascular complex, and VDR, whereas no difference in choroidal parameters after CAR and no findings of PICCFVs were found.

Conclusions

The findings of this study suggest that ocular microvascular perfusion is improved after CAR in the ipsilateral eye and the contralateral eye within a wide field of the fundus. The VDCC is decreased in the ipsilateral eye, which may indicate infarctions of choriocapillaris or ischemia–reperfusion injury of the choriocapillaris after CAR.

Financial Disclosure(s)

Proprietary or commercial disclosure may be found in the Footnotes and Disclosures at the end of this article.

Keywords: Carotid artery stenosis, Carotid artery revascularization, Optical coherence tomography angiography, Retinal microvasculature


Carotid artery stenosis (CAS) usually refers to plaque developing at the common carotid artery bifurcation involving the origin of the internal carotid artery (ICA) and carotid bulb, which is one of the major causes of acute ischemic stroke.1,2 The ophthalmic artery supplying the eye is the first branch of ICA, and stenosis of ICA will cause decreased blood flow to the eye. Correspondingly, revascularization of the ICA may increase the blood flow of the eye. With the development of imaging devices, especially the advent of OCT angiography (OCTA), blood flow changes in the retina and the choroid can now be quantitatively analyzed. Derived parameters have been used as indicators of severity of stenosis and for correlating with cerebral hemodynamics and cognitive decline associated with CAS.3, 4, 5

Some studies have detected blood flow changes in the retina and the choroid before and after revascularization surgery in CAS patients using OCTA.5, 6, 7 However, the scanned area in previous studies was limited in the macular region, usually with a small scanning range of 3 × 3 mm or 6 × 6 mm. Regions away from the macular may also show significant blood flow changes but have been ignored. Besides, few studies explored the microvascular changes of the contralateral eye. Thus, this study aims to detect the blood flow changes of the retina and the choroid in both eyes within an ultra-widefield range of the fundus in severe CAS patients who underwent carotid artery revascularization (CAR).

Methods

Study Design and Participants

This prospective, single-center, observational cohort study was implemented by the Department of Ophthalmology and Department of Neurology at West China Hospital, Sichuan University, Sichuan, China. The study was designed and performed following the ethical tenets of the 1964 Helsinki Declaration and approved by the Institute Ethics Committee of West China Hospital with verifiable consent (approval number: 20231171). Consecutive patients were recruited from the hospitalized patients at West China Hospital. All patients provided written informed consent before participation in this study. Recruited patients all underwent clinical examination including best-corrected visual acuity, slit lamp bio-microscopy, intraocular pressure (IOP), axial length, color fundus photography, and OCTA.

Inclusion Criteria

The inclusion criteria were as follows: (1) diagnosed with hemodynamically significant stenosis (the grade of carotid stenosis was evaluated using digital subtraction angiography in accordance with the North America Symptomatic Carotid Endarterectomy Trial criteria. Significant stenosis was defined as (1) stenosis ≥ 70% and (2) age between 30 and 90 years.

Exclusion Criteria

The exclusion criteria were as follows: (1) complicated with other ocular diseases, such as glaucoma, diabetic retinopathy, inflammatory retinopathy, etc; (2) previously received any fundus treatment such as retinal laser, intravitreal injection, and vitrectomy, etc.; (3) axial length >26 mm or mean spherical equivalent <−6 diopters; (4) severe postoperative complications including central or branch retinal artery occlusion; (5) complicated with neurodegenerative or demyelinating diseases, such as Alzheimer’s disease, Parkinson’s disease, and multiple sclerosis; (6) with increased IOP (>21 mmHg); (7) best-corrected visual acuity <0.2 (logarithm of the minimum angle of resolution); and (8) poor quality of OCTA images (image quality ≤6).

Imaging Protocols

Preoperatively, all participants underwent detailed ocular examination, including best-corrected visual acuity, IOP (TX-20, Canon), axial length (IOL Master Advanced Technology, Carl Zeiss, Meditec), slit lamp examination, color fundus photography (CLARUS 500 or Daytona, Optos), OCT and OCTA (BM-400K BMizar, TowardPi Medical Technology). Postoperatively (within 1 week); all participants repeated the examination of IOP, slit lamp examination, color fundus photography, OCT, and OCTA at the same time point of the day to avoid diurnal variations. Each type of examination was completed by the same appointed operator. All scans were adjusted based on axial length to avoid its influence on the results.

OCT angiography scans were obtained using a 400 kHz swept-source OCTA instrument (BM-400K BMizar, TowardPi). It uses a swept-source VCSEL laser with a wavelength of 1060 nm and with a scanning rate of 400 000 A-scans per second, providing a transverse resolution of 10 μm and an in-depth resolution (optical) of 3.8 μm. This instrument has an A-scan depth of 6.0 mm in tissue (2560 pixels). Two sequential B-scans were performed at each fixed position before proceeding to the next transverse location on the retina. The built-in software provides the default segmentation layers which include the enface view of superficial and deep inner retina plexus, outer retina plexus, and choriocapillaris, with artifacts minimized by employing volumetric projection artifact removal approaches. All of these segmentations were manually inspected and corrected as needed by 2 ophthalmologists (L.Z. and J.-W.L.) before any calculation. To detect wider ranges of blood flow changes, a 16 × 16 mm volume was captured (Fig 1).

Figure 1.

Figure 1

Widefield fundus blood flow images automatically segmented by swept-source OCT angiography scan within a range of 16 × 16 mm. A, B, Segmentation of retinal superficial vascular complex, which comprises the microvasculature from the inner limiting membrane to 9 μm beneath the inner plexiform layer. C, D, Segmentation of the retinal deep vascular complex, which comprises the microvasculature from 6 μm beneath the inner plexiform layer to 9 μm beneath the outer plexiform layer. E, F, Segmentation of the choriocapillaris, which comprises the microvasculature from the basal border of the retinal pigment epithelium–Bruch’s membrane complex to 29 μm beneath it. G, H, Segmentation of the middle and large choroidal vessels, which comprises the microvasculature from 29 μm beneath the Bruch’s membrane to the choroid-scleral interface.

Measurement Parameters

Retinal Parameters

The retinal parameters were as follows: (1) central macular thickness (CMT); (2) vessel density of the retinal superficial vascular complex (VDRSVC); (3) vessel density of the retinal deep vascular complex; and (4) vessel density of the retina (VDR).

Choroidal Parameters

The choroidal parameters were as follows: (1) central choroidal thickness (CCT); (2) vessel density of the choriocapillaris (VDCC); (3) vessel density of the medium and large choroidal vessels, choroidal vessel volume ratio (CVV/a, defined as the ratio of the choroidal vessel volume to the area of the measured region); and (4) 3-dimensional choroidal vascularity index (3D-CVI, defined as the ratio of the choroidal vessel volume to the total choroidal volume measured with 3-dimensional algorithm, which reflects the volumetric choroidal vessel density).

These parameters were all measured automatically by the built-in software of BK-400 BMizar of TowardPi.

Surgical and Stenting Protocol

Carotid Endarterectomy

After confirmation of carotid stenosis on digital subtraction angiography, an incision along the anterior border of sternocleidomastoid muscles was made. The common carotid artery was encircled with a No. 1 silk loop for control and dissection continued to reach the carotid bifurcation and its branches. Arteriotomy begins on the ICA distal to the plaque gradually extending to the common carotid artery and the tip of the plaque was separated until normal endothelium was seen. Demonstration of the plaque was removed after the arteriotomy was closed using two 6/0 polypropylene sutures.

CAS

Via right femoral artery puncture, selective carotid angiography was performed to confirm the presence of ICA stenosis. With a lateral view of the neck, using double length 0.035 Terumo wire which was positioned in the common carotid artery, an appropriate-size distal protection device was passed through the stenosis and positioned into distal cervical ICA. Balloon angioplasty was then performed. After ensuring a good opening of the artery post angioplasty, an appropriate-size stent was deployed across the lesion. Then, the distal protection device was removed. Finally, flow across the ICA and its intracranial branches was confirmed.

Statistical Analysis

All analyses were conducted using SPSS version 26 (SPSS, Inc) and Microsoft Excel (version 16, Microsoft Corp). The parametric data were reported as mean ± standard deviation, and the nonparametric data were reported as medians and interquartile ranges. Categorical variables were presented as numbers and percentages. The paired t test was used for normally distributed variables, and Wilcoxon tests were used for nonnormally distributed variables. χ2 test or Fisher exact test was used for categorical variables. P values < 0.05 were considered statistically significant.

Results

Demographic Characteristics

Thirty-one patients declined postoperative examination and were excluded. Two patients with remote preoperative branch retinal artery occlusion, 1 patient with macular hole, 2 patients with postoperative branch retinal artery occlusion, 8 patients with epiretinal membrane, 2 patients with glaucoma, and 10 patients with poor-quality OCTA images were excluded. A total of 112 eyes from 56 severe CAS patients with complete preoperative and postoperative data were included in this study between September 2023 and January 2024. Among them, 47 patients (83.9%) received carotid artery stenting and 9 (16.1%) received carotid endarterectomy. The mean age was 65.34 ± 9.65 years. The axial length was 23.68 ± 0.82 and 23.70 ± 0.85 for the ipsilateral and contralateral eye, respectively (Table 1).

Table 1.

Demographic Characteristics

SCAS Patients
Age, yrs 65.34 ± 9.65
Sex 51 male (91.1%); 5 female (8.9%)
AL
Ipsilateral eye 23.68 ± 0.82
Contralateral eye 23.70 ± 0.85
DM 23 (40.4%)
HT 37 (64.9%)
HG 10 (17.5%)
CAC 17 (29.8%)
Smoking 24 (42.9%)
Drinking 24 (42.9%)
Antiaggregant use 38 (67.9%)
Statin use 40 (71.4%)

AL = axial length; CAC = coronary atherosclerotic cardiopathy; DM = diabetes mellitus; HG = hyperlipidemia; HT = hypertension; SCAS = severe carotid artery stenosis.

IOP

Preoperatively, IOP for the ipsilateral eye (12.6 mmHg [11.5–14.8]) was significantly lower than the contralateral eye (13.8 mmHg [11.6–16.2]; P = 0.001). Postoperatively, no difference in IOP was detected between the ipsilateral (13.3 mmHg [11.5–14.8]) and the contralateral eye (13.8 mmHg [11.5–15.4]; P = 0.213). No difference was found between the preoperative and postoperative IOP of the ipsilateral and contralateral eye.

OCTA Parameters

Ipsilateral Eye

The VDRSVC and VDR significantly increased after CAR. Postoperative CMT (245.50 μm [232.00– 258.00]) significantly decreased compared with preoperative CMT (247 μm [229.00–258.00]; P = 0.004). Meanwhile, the postoperative CCT was 221.50 μm [158.00–279.00], which significantly increased compared with the preoperative CCT (212.50 μm [126.75–276.75]; P = 0.001). The postoperative VDCC decreased compared with preoperative VDCC (P = 0.001). The 3D-CVI and CVV/a increased with statistical significance (Table 2).

Table 2.

Comparison of OCTA Parameters of the Ipsilateral Eye before and after CAR

OCTA Parameters Preoperative Postoperative P Value
CMT (median [IQR]) 247.00 [229.00–258.00] 245.50 [232.00–258.00] 0.004
VDRSVC (median [IQR]) 41.00 [39.00–42.00] 42.00 [40.25–43] 0.005
VDRDVC (median [IQR]) 43.00 [41.00–44.00] 43.00 [42.00–44.00] 0.150
VDR (median [IQR]) 41.00 [40.00–42.75] 42.00 [41.00–43.00] 0.001
CCT (median [IQR]) 212.50 [126.75–276.75] 221.50 [158.00–279.00] 0.001
VDCC (median [IQR]) 50.00 [49.00–50.00] 49.00 [48.25–50.00] 0.001
VDMLC (median [IQR]) 50.00 [49.00–50.00] 49.00 [48.00–50.00] 0.119
CVV/a (median [IQR]) 62.00 [44.00–84.50] 65.50 [49.00–83.50] 0.008
3D-CVI (median [IQR]) 30.50 [26.00–34.00] 31.00 [26.25–34.00] 0.024

3D-CVI = 3-dimensional choroidal vascularity index; CCT = central choroidal thickness; CMT = central macular thickness; CVV/a = choroidal vessel volume ratio; IQR = interquartile range; VDCC = vessel density of the choriocapillaris; VDMLC = vessel density of the medium and large choroidal vessels; VDR = vessel density of the retina; VDRDVC = vessel density of the retinal deep vascular complex; VDRSVC = vessel density of the retinal superficial vascular complex.

P values < 0.05.

Contralateral Eye

The VDRSVC, vessel density of the retinal deep vascular complex, and VDR significantly increased after CAR. Postoperative CMT (244.00 μm [229.75–252.00]) significantly decreased compared with preoperative CMT (247.00 μm [232.75–259.50]; P = 0.001). The CCT, VDCC, vessel density of the medium and large choroidal vessels, 3D-CVI, and CVV/a all increased after CAR, but the difference was not statistically significant (Table 3).

Table 3.

Comparison of OCTA Parameters of the Contralateral Eye before and after CAR

OCTA Parameters Preoperative Postoperative P Value
CMT (median [IQR]) 247.00 [232.75–259.50] 244.00 [229.75–252.00] <0.001
VDRSVC (median [IQR]) 41.00 [40.00–42.75] 42.00 [41.00–43.00] 0.008
VDRDVC (median [IQR]) 43.00 [41.00–44.00] 43.00 [42.00–44.00] 0.018
VDR (median [IQR]) 42.00 [41.00–43.00] 42.50 [41.00–43.75] 0.011
CCT (mean [SD]) 232.00 [141.75–285.00] 232.00 [150.50–282.00] 0.209
VDCC (median [IQR]) 50.00 [49.00–50.00] 50.00 [49.00–50.00] 0.770
VDMLC (median [IQR]) 50.00 [49.00–58.00] 50.00 [50.00–58.00] 0.186
CVV/a (median [IQR]) 65.00 [46.00–80.00] 66.00 [47.00–80.00] 0.217
3D-CVI (median [IQR]) 30.50 [27.00–34.00] 31.00 [27.00–34.00] 0.089

3D-CVI = 3-dimensional choroidal vascularity index; CCT = central choroidal thickness; CMT = central macular thickness; CVV/a = choroidal vessel volume ratio; IQR = interquartile range; VDCC = vessel density of the choriocapillaris; VDMLC = vessel density of the medium and large choroidal vessels; VDR = vessel density of the retina; VDRDVC = vessel density of the retinal deep vascular complex; VDRSVC = vessel density of the retinal superficial vascular complex.

P values < 0.05.

Decreased VDCC in Patients Who Underwent Carotid Artery Stenting

We further evaluated OCTA image features and identified postoperative blood flow voids in the choriocapillaris of the ipsilateral eye (representative cases are presented in Figure 2, Figure 3, Figure 4). After reviewing and comparing the preoperative and postoperative OCTA images, we finally identified a total of 13 patients who presented with postoperative ipsilateral choriocapillaris flow voids (PICCFVs). All patients with choriocapillaris flow voids received carotid artery stenting other than carotid endarterectomy. In the 47 patients who received carotid artery stenting, patients were divided into the PICCFV group and the non-PICCFV group. No significant difference in demographic characteristics between patients with PICCFVs and patients without PICCFVs was found. However, we found a greater decrease in VDCC in patients with PICCFVs than in patients without PICCFVs (Table 4).

Figure 2.

Figure 2

A 61-year-old male received carotid angioplasty and stenting for severe left carotid artery stenosis and was found to have postoperative ipsilateral choriocapillaris flow voids detected by widefield swept-source OCT angiography. (Top left) Normal blood flow of the choriocapillaris obtained 1 day before the stenting procedure. (Bottom left) Multiple choriocapillaris blood flow deficits were detected by widefield OCT angiography 2 days after the stenting procedure, and this patient noted no symptoms. (Top right and bottom right) 1-day preoperative and 2-day postoperative B-scan images at the same region (green arrows) of the lesion showing decreased blood flow signal in the choriocapillaris after the stenting procedure.

Figure 3.

Figure 3

A 65-year-old male received carotid angioplasty and stenting for severe right carotid artery stenosis and was found to have postoperative ipsilateral choriocapillaris flow voids detected by widefield swept-source OCT angiography. (Top left) Normal blood flow of the choriocapillaris obtained 1 day before the stenting procedure. (Bottom left) Multiple choriocapillaris blood flow deficits were detected by widefield OCT angiography 3 days after the stenting procedure, and this patient noted no symptoms. (Top right and bottom right) 1-day preoperative and 3-day postoperative B-scan images at the same region (green arrows) of the lesion showing decreased blood flow signal in the choriocapillaris after the stenting procedure.

Figure 4.

Figure 4

A 60-year-old female received carotid angioplasty and stenting for severe left carotid artery stenosis and was found to have blood flow voids within the choriocapillaris detected by widefield swept-source OCT angiography. (Top left) Normal blood flow of the choriocapillaris obtained 1 day before the stenting procedure. (Bottom left) The lobular appearance of choriocapillaris blood flow deficits was detected by widefield OCT angiography 7 days after the stenting procedure, and this patient noted floating dots at the inferior temporal visual field of the left eye. (Top right and bottom right) 1-day preoperative and 7-day postoperative B-scan images at the same region (green arrows) of the lesion showing decreased blood flow signal in the choriocapillaris after the stenting procedure.

Table 4.

Demographic Characteristics of Patients with PICCFV and Patients without PICCFV

PICCFV Non-PICCFV P Value
Number of patients 13 (27.7%) 34 (72.3%)
Age, yrs 67.46 ± 7.66 65.74 ± 10.43 0.590
Sex 12 M, 1 F 31 M, 3 F 0.901
Ipsilateral AL 23.54 ± 0.44 23.65 ± 0.81 0.632
DM 8 14 0.211
HT 8 26 0.306
HG 1 8 0.217
CAC 5 6 0.132
Smoking 3 16 0.134
Drinking 5 14 0.865
VDCC change 2 [1.00 to 2.00] 0.00 [−1.00 to 1.00] <0.001∗

AL = axial length; CAC = coronary atherosclerotic cardiopathy; DM = diabetes mellitus; F = female; HG = hyperlipidemia; HT = hypertension; M = male; PICCFV = postoperative ipsilateral choriocapillaris flow voids; VDCC = vessel density of choriocapillaris.

Discussion

This study aims to investigate the ocular microvascular change after CAR in a wider field of the fundus. Although earlier studies have explored the microvascular changes in patients with CAS within a small range of scanning field of 3 × 3 mm or 6 × 6 mm covering the macular region, they have not detected the microvascular blood flow changes in a wider field which would be more comprehensive to reflect the blood flow changes of the entire fundus.

IOP

Significantly lower preoperative IOP was found in the ipsilateral eye compared with the contralateral eye in this study. The study by Kaplan et al8 has demonstrated that severe carotid artery disease may reduce aqueous humor formation by lowering ciliary body blood flow to a point beyond which the eye cannot compensate. The lower preoperative ipsilateral IOP may indicate a more severe ischemic condition in the ipsilateral eye before CAR. Postoperatively, no increase in IOP in the ipsilateral or the contralateral eye was found. However, no difference in postoperative IOP between the ipsilateral eye and the contralateral eye after CAR was found, which may indicate the establishment of a more balanced ocular perfusion status between eyes of both sides after CAR.

OCTA Retinal Parameters Change after CAR

According to the results, the VDRSVC and VDR in the ipsilateral eye significantly improved after revascularization surgery in a wide field of the fundus. Meanwhile, we found significantly decreased CMT after CAR, which has never been reported in the literature. Previous studies have found decreased ocular perfusion and retinal blood flow in CAS patients compared with normal controls,4,7,9, 10, 11, 12 which indicated that the retina is under ischemic condition when the carotid artery is occluded. With increased retinal perfusion after CAR, resolved retinal ischemia might lead to a CMT decrease.13

We also found increased VDRSVC, vessel density of the retinal deep vascular complex, and VDR in the contralateral eye after CAR in this study, which indicated retinal blood supply improvement in the contralateral eye. This is consistent with a few studies that have reported improved retinal perfusion of the contralateral eye.11,12,14 Previous studies have reported improvement in contralateral hemisphere cerebral blood flow, retrobulbar ocular blood flow, and neuroretinal function.15, 16, 17, 18 Preoperatively, to relieve the ipsilateral compromised cerebral vascular condition, blood flow to the contralateral hemisphere would be directed to the ipsilateral hemisphere, and when the occlusion of the ipsilateral carotid artery is removed, blood flow of both hemispheres will be increased.19,20 We also found decreased CMT in the contralateral eye, and we assumed that this was also a manifestation of the resolution of relative retinal hypoxia caused by decreased ocular blood flow.

OCTA Choroidal Parameters Change after CAR

According to the results, significantly increased ipsilateral CCT, CVV/a, and 3D-CVI were demonstrated, indicating an increase in choroidal perfusion after CAR. Increased CCT after CAR has been reported in some studies7,21, 22, 23, 24; however, other studies have reported no CCT change after CAR.25,26 Various studies showed variability in CCT results, because CCT is influenced by age, sex, and axial length. Besides, diurnal fluctuations were identified in choroidal thickness measurements.27 Compared with CCT, CVI is more reliable in reflecting choroid vascularity.28 The findings of this study confirmed the increased perfusion of the choroid after the occlusion of the carotid artery was removed.

Interestingly, we found significantly decreased VDCC after CAR in the ipsilateral eye but not in the contralateral eye. Utsugi et al29 found severe choroidal hypoperfusion resulted in multiple occlusions of the choriocapillaris and attenuated choroidal vessels. Recently, Saito et al30 reported a case of focal choroidal infarction in a patient who underwent carotid stenting. In this study, we identified PICCFVs in 13 patients (27.7%) with evidence from OCTA images and this was further confirmed with a greater decrease in VDCC in patients with PICCFVs compared with patients without PICCFVs. We brought out 2 possible explanations for the decrease in VDCC. First, after CAR, small particles or emboli from the ipsilateral carotid artery may travel with increased blood flow and finally reach the choriocapillaris which are terminal blood vessels, causing focal infarctions of the choriocapillaris. This mechanism was adequately identified in retinal embolization in the ipsilateral eye but not in the contralateral eye after CAR.31 In this study, all patients with PICCFVs received carotid artery stenting other than carotid endarterectomy; this is consistent with previous findings of a higher prevalence of embolization rate in carotid artery stenting than carotid endarterectomy.31 Another possible mechanism was ischemia–reperfusion injury caused by increased choroidal blood flow after CAR in the ipsilateral eye but not in the contralateral eye with lesser hemodynamic change.32,33

In the contralateral eye, though increased CCT, vessel density of the medium and large choroidal vessels, 3D-CVI, and CVV/a after CAR were noted, the difference was not statistically significant. This may indicate an improvement in the contralateral microvascular perfusion but to a lesser extent compared with the ipsilateral eye.

There are several limitations in this study. First, we only detected short-term microvascular change after CAR. Longitudinal studies monitoring the long-term microvascular change may help us better understand the influence of CAR on the eye. Besides, variation from 2 to 7 days existed in the postoperative examination time point which may affect the results. Second, the sample size is relatively small, and this may have hindered the exploration of choroidal change in the contralateral eye, which showed a tendency of improvement but was not statistically significant. We only included 9 patients who underwent carotid endarterectomy in this study, which may be responsible for no PICCFV findings in this group. Besides the difference in OCTA parameters between 2 methods of revascularization was not explored. Third, this is an image-based study, the results of which could be influenced by confounding factors like imaging quality and the so-called blooming effect when exploring images from the choriocapillaris.34,35

Future studies with large sample sizes may explore the occurrence, pathology, and risk factors for choriocapillaris infarctions after CAR and the association between ocular microvascular hemodynamics and cerebral hemodynamics.

Manuscript no. XOPS-D-24-00302R1

Footnotes

Disclosure(s):

All authors have completed and submitted the ICMJE disclosures form.

The author(s) have made the following disclosure(s):

M.-X.Z.: All support for the present manuscript – This work was supported by Chengdu Municipal Science and Technology Bureau Key R&D Support Program (no. 2023-YF09-00041-SN).

The other authors have no proprietary or commercial interest in any materials discussed in this article.

Financial Support: This work was supported by the Chengdu Municipal Science and Technology Bureau Key R&D Support Program (no. 2023-YF09-00041-SN). The sponsor or funding organization had no role in the design or conduct of this research.

HUMAN SUBJECTS: Human subjects were included in this study. The study was designed and performed following the ethical tenets of the 1964 Declaration of Helsinki and approved by the Institute Ethics Committee of West China Hospital with verifiable consent (approval number: 20231171). All patients provided written informed consent before participation in this study.

No animal subjects were used in this study.

Author Contributions:

Conception and design: L. Zhang, Hu, M.-X. Zhang

Data collection: L. Zhang, Liu, Lei, Lin, Gao, Yang, Hu, M.-X. Zhang

Analysis and interpretation: L. Zhang, Tang, Gao, Yang, Hu, M.-X. Zhang

Obtained funding: M.-X. Zhang

Overall responsibility: L. Zhang, Liu, Tang, Lei, Lin, Hu, M.-X. Zhang

Contributor Information

Fa-Yun Hu, Email: hufayun2006@163.com.

Mei-Xia Zhang, Email: zhangmeixia@scu.edu.cn.

References

  • 1.Cheng S.F., Brown M.M., Simister R.J., Richards T. Contemporary prevalence of carotid stenosis in patients presenting with ischaemic stroke. Br J Surg. 2019;106:872–878. doi: 10.1002/bjs.11136. [DOI] [PubMed] [Google Scholar]
  • 2.Jusufovic M., Skagen K., Krohg-Sørensen K., Skjelland M. Current medical and surgical stroke prevention therapies for patients with carotid artery stenosis. Curr Neurovasc Res. 2019;16:96–103. doi: 10.2174/1567202616666190131162811. [DOI] [PubMed] [Google Scholar]
  • 3.István L., Czakó C., Élő Á., et al. Imaging retinal microvascular manifestations of carotid artery disease in older adults: from diagnosis of ocular complications to understanding microvascular contributions to cognitive impairment. Geroscience. 2021;43:1703–1723. doi: 10.1007/s11357-021-00392-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Liu J., Wan J., Kwapong W.R., et al. Retinal microvasculature and cerebral hemodynamics in patients with internal carotid artery stenosis. BMC Neurol. 2022;22:386. doi: 10.1186/s12883-022-02908-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Rocha-Sousa A., Moleiro A.F., Rocha-Neves J., et al. Optical coherence tomography angiography assessment of retinal microvasculature before and after carotid endarterectomy. Invest Ophthalmol Vis Sci. 2022;63:2908. F0061. [Google Scholar]
  • 6.Durusoy G.K., Gumus G., Onay M., et al. Early choroidal structure and choroidal vascularity index change after carotid stenting. Photodiagn Photodyn Ther. 2022;38:102748. doi: 10.1016/j.pdpdt.2022.102748. [DOI] [PubMed] [Google Scholar]
  • 7.Akca Bayar S., Kayaarası Öztürker Z., Pınarcı E.Y., et al. Structural analysis of the retina and choroid before and after carotid artery surgery. Curr Eye Res. 2020;45:496–503. doi: 10.1080/02713683.2019.1666994. [DOI] [PubMed] [Google Scholar]
  • 8.Kaplan B.H., Kalina P.H., Larsson L.I., et al. Aqueous humor flow in unilateral carotid stenosis. J Glaucoma. 1996;5:237–240. [PubMed] [Google Scholar]
  • 9.Liu X., Yang B., Tian Y., et al. Quantitative assessment of retinal vessel density and thickness changes in internal carotid artery stenosis patients using optical coherence tomography angiography. Photodiagn Photodyn Ther. 2022;39:103006. doi: 10.1016/j.pdpdt.2022.103006. [DOI] [PubMed] [Google Scholar]
  • 10.Ozdogru D., Kurumoglu Incekalan T., Simdivar G.H.N., et al. Comparison of optical coherence tomography angiography results in patients with internal carotid artery stenosis who underwent carotid artery stenting and carotid endarterectomy. Med (Baltim) 2024;103:e39235. doi: 10.1097/MD.0000000000039235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Li X., Zhu S., Zhou S., et al. Optical coherence tomography angiography as a noninvasive assessment of cerebral microcirculatory disorders caused by carotid artery stenosis. Dis Markers. 2021;2021:2662031. doi: 10.1155/2021/2662031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Lee C.W., Cheng H.C., Chang F.C., Wang A.G. Optical coherence tomography angiography evaluation of retinal microvasculature before and after carotid angioplasty and stenting. Sci Rep. 2019;9:14755. doi: 10.1038/s41598-019-51382-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Duan J., Shen S., Lei C., et al. Choroidal and retinal abnormalities in Cushing syndrome: correlation with the cortisol level. Retina. 2024;44:861–867. doi: 10.1097/IAE.0000000000004023. [DOI] [PubMed] [Google Scholar]
  • 14.Yusef Y.N., Semitko S.P., Durzhinskaya M.H., et al. Ocular microcirculation after revascularization of the internal carotid artery in the early postoperative period. Vestn Oftalmol. 2022;138:186–195. doi: 10.17116/oftalma2022138052186. [in Russian] [DOI] [PubMed] [Google Scholar]
  • 15.Rutgers D.R., Klijn C.J., Kappelle L.J., et al. Sustained bilateral hemodynamic benefit of contralateral carotid endarterectomy in patients with symptomatic internal carotid artery occlusion. Stroke. 2001;32:728–734. doi: 10.1161/01.str.32.3.728. [DOI] [PubMed] [Google Scholar]
  • 16.Sadato A., Maeda S., Hayakawa M., et al. Carotid stenting for unilateral stenosis can increase contralateral hemispheric cerebral blood flow. J Neurointerv Surg. 2018;10:351–354. doi: 10.1136/neurintsurg-2017-013193. [DOI] [PubMed] [Google Scholar]
  • 17.Kozobolis V.P., Detorakis E.T., Georgiadis G.S., et al. Perimetric and retrobulbar blood flow changes following carotid endarterectomy. Graefes Arch Clin Exp Ophthalmol. 2007;245:1639–1645. doi: 10.1007/s00417-007-0589-2. [DOI] [PubMed] [Google Scholar]
  • 18.Machalińska A., Kowalska-Budek A., Kawa M.P., et al. Effect of carotid endarterectomy on retinal function in asymptomatic patients with hemodynamically significant carotid artery stenosis. Pol Arch Intern Med. 2017;127:722–729. doi: 10.20452/pamw.4064. [DOI] [PubMed] [Google Scholar]
  • 19.Rijbroek A., Boellaard R., Vermeulen E.G.J., et al. Hemodynamic changes in ipsi- and contralateral cerebral arterial territories after carotid endarterectomy using positron emission tomography. Surg Neurol. 2009;71:668–676. doi: 10.1016/j.surneu.2008.04.027. [DOI] [PubMed] [Google Scholar]
  • 20.Wang T., Wang X., He Y., et al. Decreased 1³N-labeled ammonia uptake in the ipsilateral and contralateral hemispheres following carotid endarterectomy. Mol Med Rep. 2015;12:6598–6604. doi: 10.3892/mmr.2015.4303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Lareyre F., Nguyen E., Raffort J., et al. Changes in ocular subfoveal choroidal thickness after carotid endarterectomy using enhanced depth imaging optical coherence tomography: a pilot study. Angiology. 2018;69:574–581. doi: 10.1177/0003319717737223. [DOI] [PubMed] [Google Scholar]
  • 22.Krytkowska E., Masiuk M., Kawa M.P., et al. Impact of carotid endarterectomy on choroidal thickness and volume in enhanced depth optical coherence tomography imaging. J Ophthalmol. 2020;2020 doi: 10.1155/2020/8326207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Biberoglu E., Eraslan M., Midi I., Baltacioglu F., Bitargil M. Ocular blood flow and choroidal thickness changes after carotid artery stenting. Arq Bras Oftalmol. 2020;83:417–423. doi: 10.5935/0004-2749.20200081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Zhang Y., Zhou S.W., Noam N., et al. Influence of carotid endarterectomy on choroidal perfusion: the INFLATE study. Ophthalmol Retina. 2024;8:62–71. doi: 10.1016/j.oret.2023.07.026. [DOI] [PubMed] [Google Scholar]
  • 25.Rabina G., Barequet D., Mimouni M., et al. Carotid artery endarterectomy effect on choroidal thickness: one-year follow-up. J Ophthalmol. 2018;2018 doi: 10.1155/2018/8324093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Ala-Kauhaluoma M., Koskinen S.M., Silvennoinen H., et al. Subfoveal choroidal thickness in ipsi- and contralateral eyes of patients with carotid stenosis before and after carotid endarterectomy: a prospective study. Acta Ophthalmol. 2021;99:545–552. doi: 10.1111/aos.14648. [DOI] [PubMed] [Google Scholar]
  • 27.Brown J.S., Flitcroft D.I., Ying G.S., et al. In vivo human choroidal thickness measurements: evidence for diurnal fluctuations. Invest Ophthalmol Vis Sci. 2009;50:5–12. doi: 10.1167/iovs.08-1779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Betzler B.K., Ding J., Wei X., et al. Choroidal vascularity index: a step towards software as a medical device. Br J Ophthalmol. 2022;106:149–155. doi: 10.1136/bjophthalmol-2021-318782. [DOI] [PubMed] [Google Scholar]
  • 29.Utsugi N., Takahashi K., Kishi S. Choroidal vascular occlusion in internal carotid artery obstruction. Retina. 2004;24:915–919. doi: 10.1097/00006982-200412000-00012. [DOI] [PubMed] [Google Scholar]
  • 30.Saito K., Uchida Y., Tokui S., Akiyama H. A case of Elschnig’s spots observed using optical coherence tomography-angiography after stenting for internal carotid artery dissection. Retin Cases Brief Rep. 2023 doi: 10.1097/ICB.0000000000001496. [DOI] [PubMed] [Google Scholar]
  • 31.Song G., Sun R., Chen Y.F., et al. Retinal embolization after carotid endarterectomy and stenting for carotid artery stenosis. J Clin Neurosci. 2015;22:1298–1302. doi: 10.1016/j.jocn.2015.01.033. [DOI] [PubMed] [Google Scholar]
  • 32.Ishizuka F., Shimazawa M., Inoue Y., et al. Toll-like receptor 4 mediates retinal ischemia/reperfusion injury through nuclear factor-κB and spleen tyrosine kinase activation. Invest Ophthalmol Vis Sci. 2013;54:5807–5816. doi: 10.1167/iovs.13-11932. [DOI] [PubMed] [Google Scholar]
  • 33.Abdallah W., Ameri H., Barron E., et al. Vitreal oxygenation in retinal ischemia reperfusion. Invest Ophthalmol Vis Sci. 2011;52:1035–1042. doi: 10.1167/iovs.09-4516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Sannino C., Marino A. Letter: Early choroidal structure and choroidal vascularity index change after carotid stenting. Photodiagn Photodyn Ther. 2022;38:102832. doi: 10.1016/j.pdpdt.2022.102832. [DOI] [PubMed] [Google Scholar]
  • 35.Ng D.S., Chan L.K., Ng C.M., Lai T.Y.Y. Visualising the choriocapillaris: histology, imaging modalities and clinical research - a review. Clin Exp Ophthalmol. 2022;50:91–103. doi: 10.1111/ceo.13984. [DOI] [PubMed] [Google Scholar]

Articles from Ophthalmology Science are provided here courtesy of Elsevier

RESOURCES