Vortex vein engorgement and different shapes of venous drainage systems in polypoid choroidal vasculopathy vs. age‑related macular degeneration on indocyanine green angiography
- Authors:
- Published online on: February 23, 2023 https://doi.org/10.3892/etm.2023.11861
- Article Number: 162
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Copyright: © Cai et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Owing to the high similarity in clinical manifestations and genetics between polypoid choroidal vasculopathy (PCV) and age-related macular degeneration (AMD), PCV was hypothesized to be an AMD subtype (1). However, unlike AMD, PCV is more common in people of colour and lesions occur outside the vascular arch or the nasal side of the optic disc, in addition to in the macula. AMD, on the other hand, is common in Caucasians, and the lesions are concentrated in the macula (2). The primary difference between the two diseases is response to intravitreal anti-vascular endothelial growth factor (anti-VEGF) drugs in patients with PCV patients is not as good as that in AMD patients (2-4). These findings suggest that the pathological mechanisms of PCV and AMD differ.
To improve the treatment efficacy for PCV and AMD, differences between the two diseases have been explored (2). The pathogenesis of both PCV and AMD is associated with choroidal vessels (2). A typical PCV subtype with choroidal thickness ≥257 µm has a significantly greater choroidal vascular area in the macular and foveal regions compared with that in typical AMD (5). The vortex vessels, located in the middle layer of the eyeball wall, drain the choroid. They are difficult to detect by direct observation but can be observed more clearly with indocyanine green angiography (ICGA) than with other non-invasive techniques (6). However, research on vortex veins mostly transforms the ICGA image into binary image, and then manually segment the quadrants based on the position of the vortex vein to measure the brightness of each quadrant for research (7). The present study aimed to develop a method that is simpler and more suitable for clinical use and easier for evaluating vortex vein filling.
Moreover, the present study aimed to describe the differences in vortex vein engorgement and appearance between PCV, AMD and healthy people of the same age using ICGA to reveal differences in vortex vein anatomy between PCV and AMD.
Patients and methods
Patients
Patients orally agreed to the use of their data in the present study. Ethical approval for this retrospective study was obtained from the Institutional Review Board of the Zhongshan Ophthalmic Centre (approval no. 2022KYPJ173). In total, 180 participants(mean age, 64.12±8.87 years; range, 52-75 years) were recruited in this study, including 109 males and 71 females. All participants underwent ICGA (SPECTRALIS Diagnostic Imaging Platform; Heidelberg Engineering, Inc.) and optical coherence tomography (OCT) (SPECTRALIS® OCT; Heidelberg Engineering Inc.) between January 2018 and January 2022 at the Zhongshan Ophthalmic Centre, Guangzhou, China.
The present study included 63 patients with PCV, 50 with AMD and 67 healthy control group. Based on the results of fundus examination, OCT, fundus fluorescein angiography (FFA) and ICGA, age- and sex-matched patients were grouped based on diagnosis into PCV, AMD and healthy control group. Only one eye was included for patients diagnosed with bilateral PCV or AMD. In healthy participants, only the eye with the best-corrected visual acuity (>20/16) was included.
The following exclusion criteria were adopted: History of prior ocular surgery or trauma(excluded 15 PCV patients); severe vitreous haemorrhage that may affect imaging examination (excluded two PCV patients); any systemic disease that may affect blood flow, such as diabetes mellitus or hypertension (excluded one PCV patients and three AMD patients); central serous chorioretinopathy (CSC); primary glaucoma; optic neuritis; retinal vein occlusion; choroidal melanoma; retinal vasculitis; uveitis; an epiretinal membrane that may affect ocular circulation (excluded one PCV patients and five AMD patients) or moderate to high myopia (defined as a spherical equivalent refractive error in phakic eyes <-3.00 D) (excluded nine healthy participants).
We conducted another screening to exclude the cases who only received monocular ICGA and OCT examination and included 44 cases of unilateral PCV and 18 cases of unilateral AMD. The diseased eye was included in the PCV/AMD group, and the healthy fellow eye was included in the PCV/AMD fellow eye group.
Following intravenous injection of 5 ml 25 mg ICG (Dandong Yichuang Pharmaceutical Co., Ltd), ICGA images were recorded. Early-stage images (5 min after dye injection) were selected for analysis. The vortex veins were separated into four categories according to a previous method (8). The branches of type I vortex veins do not converge and pass directly through the sclera, whereas all branches of type IV (complete with ampulla) converge to form the ampulla, which is a complete vortex system. Type IV systems have a larger root area due to the dilated ampulla (8). The fundus was divided into four quadrants: Superior and inferior temporal and superior and inferior nasal. Patient characteristics, such as sex, age, number, location and type of vortex veins were recorded. The sketching tool of the retinal device was used to mark the root area and diameter of the thickest branch of each vortex vein (Fig. 1). The centre of a concentric circle was placed on the macula, the thickest vortex vein branch intersecting with the outermost circle was selected and its diameter was measured and stored as the central vortex vein diameter (CVVD). The ends of each vortex vein branch were connected with a smooth curve and the area enclosed by the curve was defined as the root area of the vortex vein (RAVV). The width of the thickest first-order branch of the vortex vein was defined as the diameter of the peripheral thickest branch (DPTB). The mean RAVV (MRAVV) and MDPTB were calculated. Vortex vein anastomosis was observed when vortex vein branches connected the two vortex vein systems on IGCA. The percentage of eyes with vortex vein anastomosis in each group was calculated and recorded as the percentage of vortex vein anastomosis (PVVA). Subfoveal choroidal thickness (SFCT) was measured using SPECTRALIS® OCT device. All labelling was performed separately by two experienced ophthalmologists (CXC and XMX) and the mean of the two measurements was used as the final data.
Statistical analysis
One-way ANOVA was used to compare differences in age, sex, number of vortex veins (NVV), CVVD, MRAVV, MDPTB, and SFCT between PCV, AMD and healthy controls, as well as to compare differences in the NVV between the four quadrants. When one-way ANOVA indicated a significant difference between PCV, AMD and healthy groups, the least-significant-difference test was used to perform pairwise comparisons. One-way ANOVA was used to compare PCV group differences in NVV, MRAVV, and MDPTB within each quadrant, followed by post hoc Tukey's test was used to perform pairwise comparisons. χ2 test was used to compare the differences in the proportions of subretinal haemorrhages and four types of vortex veins in each quadrant of the PCV group and differences in the proportions of the four types of vortex veins and PVVA among the PCV, AMD and healthy controls. Paired t test was used to compare affected and healthy eyes in patients with PCV/AMD. Receiver operating characteristic (ROC) curve of the CVVD, MRAVV and MDPTB were drawn between polypoid choroidal vasculopathy and age-related macular degeneration group. Area under the curve (AUC) for CVVD distinguished between PCV and AMD. Data are presented as the mean ± standard deviation. We repeated the independent experiment twice. P<0.05 was considered to indicate a statistically significant difference. Statistical analysis was performed using SPSS for Windows (version 17.0; SPSS, Inc.).
Results
The present study included 180 participants, including 63 patients with PCV, 50 with AMD and 67 healthy age-matched controls. There were no significant differences in sex or age between the three groups (P>0.05; data not shown). A total of 44 contralateral healthy eyes of patients with PCV were included in the PCV fellow eye group. A total of 18 contralateral healthy eyes of patients with AMD were included in the AMD fellow eye group.
Differences in NVV, CVVD, MRAVV, MDPTB, SFCT and PVVA were compared (Fig. 2). There were no significant differences in NVV and SFCT between the three groups (P>0.05; Fig. 2A and E). CVVD in the PCV group was significantly increased by 1.24-fold compared with that in the healthy control group and by 1.14-fold compared with that in the AMD group (P<0.05; Fig. 2B). MRAVV in the PCV group was significantly decreased compared with that in the healthy controls (P=0.004; Fig. 2C). MDPTB in the PCV group was significantly wider compared with that in the AMD group (P=0.013; Fig. 2D). PVVA in the PCV group was significantly increased compared with that in healthy controls (P=0.006; Fig. 2F).
PCV group showed the lowest proportion of type IV vortex veins (complete with ampulla), while the proportion of type I (absent) vortex veins was highest; this was significantly different between the PCV, AMD and healthy controls (P<0.001; Table I). NVV in the inferior temporal quadrant of the PCV group was increased compared with that in the AMD group (P=0.034) and NVV in the superior temporal and nasal and inferior nasal quadrants showed no significant differences between groups (P>0.05; Table II).
NVV, MRAVV and MDPTB of the PCV group were the largest in the inferior temporal region, with significant differences between quadrants (P<0.05; Fig. 3). The mean number of polyps in the PCV group was 3.37±3.47 (range, 0-15). In 15 eyes, polypoid lesions could not be observed due to severe subretinal haemorrhage on ICGA. Subretinal haemorrhage was absent in 24 and present in 39 participants in the PCV group, all of which involved the posterior pole macular area. Subretinal haemorrhages involved both superior and inferior temporal regions in seven eyes, and the posterior pole and peripheral parts in two eyes. The proportion of type I vortex veins in the PCV group was significantly different between quadrants (P<0.001; Table III). Among the PCV participants, subretinal haemorrhage was observed in 47.62% of the inferior temporal and 23.81% in the superior temporal quadrants, with significant differences between the quadrants (P<0.001; Table III).
 | Table IIIProportion of type of vortex veins (complete with ampulla) and subretinal haemorrhage in participants with polypoid choroidal vasculopathy in each quadrant. |
Considering that the area under the curve of CVVD was largest, with its' highest availability and clinical practicability, CVVD was selected as the indicator to reveal the difference between PCV and AMD. Cut-off value of CVVD is 252.5 µm and sensitivity, specificity and AUC of 88.3%, 54.0% and 0.70 respectively (Fig. S1). CVVD in the AMD group was significantly increased compared with that in the AMD fellow eye group (P=0.024; Table IV). Among the 18 participants with unilateral AMD, there were no significant differences in NVV, MRAVV, MDPTB, SFCT and PVVA between the affected and fellow eyes (P>0.05; Table IV). There were no significant differences in NVV, CVVD, MRAVV, MDPTB, SFCT and PVVA between the affected and fellow eyes in the PCV group (P>0.05; Table V).
| Table IVDifferences in vortex veins between affected and fellow eye in patients with age-related macular degeneration. |
| Table VDifferences in vortex veins between affected and fellow eye in patients with polypoid choroidal vasculopathy. |
Discussion
The present study aimed to identify differences in venous system drainage patterns between PCV, AMD and healthy eyes. The branches of the vortex veins in the PCV group were significantly expanded in the posterior pole and periphery compared with those in the AMD group because the CVVD and MDPTB were significantly increased in the PCV group. If the CVVD was >252.5 µm on ICGA, the diagnosis was more likely to be PCV than AMD, indicating that CVVD may serve as a point of differentiation between PCV and AMD. The dilation of the vortex vein was asymmetric in patients with PCV and the inferior temporal vortex vein was more engorged. The appearance of the venous drainage system in patients with PCV was different from that in the healthy control group. Type IV vortex veins were least common, while type I veins were most common in PCV eyes; these may point to the anatomical basis for the pathogenesis of PCV.
Although typical PCV and AMD are not difficult to differentiate using colour fundus photography, OCT, FFA and ICGA (9), there are clinical cases that are difficult to distinguish, requiring new points of differentiation. The present results indicated that CVVD can be used to distinguish between PCV and AMD, with a cut-off value of 252.5 µm. Gupta et al (5) reported no significant differences in choroidal thickness and vascular area between patients with PCV and those with typical AMD after adjusting for age and hypertension. Luo et al (10) found that the choriocapillaris flow density of neovascular AMD fellow eyes is significantly decreased compared with that in PCV and control eyes. Takahashi et al (11) found no significant difference in SFCT between neovascular AMD and PCV but demonstrated that the ratio of the large choroidal vessel layer thickness to SFCT is significantly increased in eyes with PCV compared with that in eyes with typical neovascular AMD.
The present study indicated that PCV vortex vein branches were significantly dilated and compensatory vortex vein anastomosis was formed. The CVVD and PVVA of the PCV group were significantly increased compared with that in healthy controls. PCV vortex vein branches were dilated at the posterior pole and peripheral choroid. PVVA in the PCV group was significantly increased compared with that in the healthy controls. Chung et al (12) found that PCV eyes are more prone to vortex venous congestion than normal eyes using ICGA, suggesting that vortex venous congestion may be associated with PCV pathogenesis. Choroidal hypertension causes secondary dilation of the vortex veins, which are compensatory anastomoses that decrease intraluminal pressure (13). If the disease progresses, the terminal blood vessels bulge locally and manifest as polypoid lesions (12,14). Qiu et al (15) found statistically significant differences in the proportion of diffuse collateral circulation between PCV, neovascular AMD, central serous chorioretinopathy (CSC) and healthy controls. During the progression of pachychoroid spectrum disease, hyperaemia of the vortex veins may gradually improve with the development of anastomosis between the superior and inferior vortex veins (16). Matsumoto et al (17) found that neovascular AMD patients with pachychoroid are significantly younger and include a higher proportion of males and increased SFCT and frequency of macular vortex vein anastomoses compared with patients with neovascular AMD without pachychoroid. Relative choroidal thickening resulting from enlargement of deep choroidal veins might be related to the mechanism of internal choroidal and retinal pigment epithelium damage (18,19). Intravitreal injection of anti-VEGF may also improve vision by decreasing the focus and macular edema. Ryu et al (20) found that choroidal vascular density (CVD) in PCV is correlated positively with choroidal thickness and choroidal hyperpermeability and that a thicker choroid and increased CVD are also associated with poor treatment response to anti-VEGF injections. Subfoveal choroidal watershed zones are associated with foveal PCV growth, suggesting that PCV arises because of aberrant choroidal circulation (2,21). Combined photodynamic therapy and intravitreal bevacizumab significantly thin the total choroid in patients with PCV after 3 months of treatment and an increase in pachy vessel diameter and choroidal vascularity has been observed in 31.33% of eyes with recurrence of PCV (22).
Here, patients with PCV not only had extended engorged vortex veins but also different appearances of venous drainage systems compared with those in healthy controls. The four types of vortex veins are illustrated in Figs. 4 and 5. Although vortex vein branches in the PCV group showed dilation in both the posterior pole and periphery, the MRAVV was significantly decreased compared with that in the healthy controls. The vortex root area depended not only on the degree of vortex dilatation but also on the appearance of the vein. In the present study, the proportion of type IV was the lowest while the proportion of type I drainage systems was the highest in the PCV group, which was significantly different between the three groups. This finding explains why the PCV group had the lowest MRAVV. The vortex ampulla and intrascleral portion of the vortex veins regulate the choroidal outflow site by flow resistance and may be involved in choroidal venous congestion (23,24). The non-expandable intrascleral route of vortex veins limits the upregulation of choroidal venous outflow (25). Although vortex veins converge, the effects on intraluminal pressure are different from pressure that arises when the veins first penetrate the sclera and after penetrating the sclera. The ampulla region of the vortex vein resembles a cistern, which relieves luminal pressure within the vortex vein. The vortex vein drains from the choroid to the outside of the eye through the sclera. The vortex vein segment passing through the sclera has poor diastolic ability, resulting in high luminal pressure of the vortex vein in the intrachoroidal segment. The ampullary region relieves high intraluminal pressure (13,26). The total number of vortex veins in patients with PCV was not significantly different compared with that in healthy controls, but the low proportion of type IV vortex veins and a high proportion of type I vortex veins, which would lead to increased intraluminal pressure in the vortex veins, may be related to the pathogenesis of PCV.
The present study found that choroidal vessels are asymmetric in each ocular quadrant and extended engorged vortex veins are more likely to occur in the inferior-temporal quadrant in PCV, which may be associated with the pathogenic mechanism underlying PCV. The inferior temporal NVV, MRAVV and MDPTB of the PCV group were significantly increased compared with those of the other groups and vortex veins were unevenly distributed among the four quadrants in the PCV group. Subretinal haemorrhage appeared in the inferior and the superior temporal quadrant in 47.62 and 23.81% of the patients in the PCV group, respectively, with significant differences between the quadrants in this group. Similar to the present study, Chung et al (12) found that vortex venous congestion in PCV eyes is most frequently distributed in the inferior, followed by the superior, temporal quadrant. This suggests that PCV lesions tend to occur in the inferior temporal region, which is closely related to the distribution of the vortex veins. In the PCV group, the proportion of type I vortex veins on the temporal side was significantly increased compared with that on the nasal side, with the highest proportion occurring in the superior temporal and the second highest in the inferior temporal region, which might be associated with the predominance of PCV bleeding in the inferior temporal region. Due to gravity, the inferior temporal vortex vein fills with more blood compared with the superior temporal vein. Therefore, submacular haemorrhage is more likely to occur in the inferior than in the superior temporal quadrant. Bacci et al (27) reported asymmetric choroidal drainage in the macula of 59% of pachychoroid eyes, with choroidal vascular hyperpermeability (CVH) and vortex venous anastomosis more prominent in areas with the greatest choroidal thickness. By comparing the brightness of each quadrant on ultra-widefield ICGA, Jung et al (7) found that the inferior temporal quadrant was significantly brighter than the superior nasal quadrant and eyes with CSC and thick choroidal pigment epitheliopathy showed asymmetric choroidal venous outflow. Imbalanced choroidal venous drainage and congestion of specific vortex vein systems may lead to choroidal venous insufficiency, characterized by regional choroidal thickening, CVH and remodelling of venous drainage pathways (27). The unbalanced expansion and congestion of vortex veins facilitate their remodelling to form anastomotic branches, thereby decreasing the local intraluminal pressure (13).
The present study compared vortex vein parameters in the affected and fellow eyes of patients with unilateral PCV and AMD. There were no significant differences in NVV, SFCT, MRAVV, MDPTB or PVVA between the affected and healthy fellow eyes. This suggested that in patients with PCV and AMD with unilateral onset, similar anatomical changes are present in the vortex veins of the affected and fellow eye; therefore, the healthy fellow eye may develop into an affected eye. Wu et al (28) found that 70% of fellow eyes of patients with unilateral PCV show CVH on ICGA. Yanagi et al (29) found that ~1/5 fellow eyes with unilateral neovascular AMD and PCV exhibit non-exudative neovascularization. CNV occurs in 9% of fellow eyes in individuals with unilateral PCV or aneurysmal type 1 neovascularization, usually retinal pigment epithelium and outer retinal abnormalities with pachy vessels (30). A study that followed patients with unilateral PCV and CNV for up to 5 years found that 17% of fellow eyes developed PCV or CNV (31).
In conclusion, the present study describes various parameters, such as the number, branch diameter, root area, location, type and anastomosis of vortex veins, in PCV, AMD and healthy control eyes, and proposed that CVVD, MRAVV and MDPTB are parameters that quantitatively evaluate these vessels. Moreover, it sheds light on the differences in the morphology and types of vortex veins in PCV, AMD, and healthy individuals. The branches of the vortex veins of the PCV were significantly dilated in the posterior pole and periphery, while lower proportion of type IV vortex veins may be pathognomonic for this condition. Based on the present findings, CVVD may be a key distinguishing point between AMD and PCV using ICGA. Patients with unilateral onset of PCV and AMD showed similar vortex vein anatomy in affected and healthy eyes, indicating the potential for the development of disease in the fellow eye. The present study provides a basis for further exploration of PCV pathogenesis based on vortex vein dilatation.
Supplementary Material
ROC curve of the CVVD, MRAVV and MDPTB between polypoid choroidal vasculopathy and age-related macular degeneration group. CVVD, central vortex vein diameter; MDPTB, mean diameter of the peripheral thickest branch; MRAVV, mean root area of the vortex vein; ROC, receiver operating characteristic.
Acknowledgements
Not applicable.
Funding
Funding: The present study was supported by the Bethune·Lumitin Research Funding for the Young and Middle-aged Ophthalmologists (grant no. BJ-LM2021014J).
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
CXC, XMX, TL, BQL, XHH, SSY, ZQL, QW, JLC, LL and YL designed the study. CXC and XMX collected the patient data. CXC analysed data and wrote the manuscript. All authors revised and edited the manuscript. All authors have read and approved the final manuscript. CXC, LL and YL confirm the authenticity of all the raw data.
Ethics approval and consent to participate
Patients orally agreed to the use of their data in the present study. The study was approved by the Ethics Committee of the Zhongshan Ophthalmic Centre (approval no. 2022KYPJ173).
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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