Imaging artifacts and quality evaluation with ultrawide-field swept-source OCTA in diabetic retinopathy

doi:10.21203/rs.3.rs-3247958/v1

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Imaging artifacts and quality evaluation with ultrawide-field swept-source OCTA in diabetic retinopathy

https://doi.org/10.21203/rs.3.rs-3247958/v1

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published 20 Dec, 2023

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Background: To evaluate the prevalence and types of artifacts in ultrawide-field swept-source optical coherence tomography angiography (SS-OCTA) scans of diabetic retinopathy (DR) patients.

Methods: This study was a prospective, observational study conducted from May 2022 to October 2022. Participants comprised individuals with proliferative diabetic retinopathy (PDR), nonproliferative diabetic retinopathy (NPDR), no diabetic retinopathy, and healthy controls. SS-OCTA imaging was performed, and a 5-scan composite with a larger field of view (23.5 mm * 17.5 mm) was captured using built-in software. Two experienced ophthalmologists analyzed the images independently, and the image quality and artifact prevalence were recorded and analyzed.

Results: The study included 70 eyes (16 with PDR, 24 with NPDR, 12 eyes of diabetic patients without DR, and 18 healthy eyes) in 70 subjects. The most prevalent artifacts were loss of signal in 63 eyes (90%) and displacement artifact and masking artifact in 43 eyes (61.4%). Patients with more severe stages of DR had higher artifact scores (P<0.05). Multivariate regression analysis indicated that DR severity was the most important factor influencing artifact scores (P<0.05).

Conclusions: In OCTA photos, various artifacts arise at different frequencies. It is crucial to qualitatively evaluate the images to ensure their quality. The results demonstrate that DR severity has a significant correlation with artifact scores.

diabetic retinopathy

optical coherence tomography angiography

artifact

wide field

image Quality

Optical coherence tomography angiography (OCTA) is a novel three-dimensional (3D) imaging technique used to evaluate the microcirculation of the retina, choroid, and optic nerve head. This method has been shown to be a valuable alternative to the traditional fluorescein angiography (FA) for evaluating retinal vasculature due to its non-invasive nature and fast imaging time [1–5]. The use of OCTA has allowed for greater understanding of the pathophysiology, categorization, and treatment of retinal and choroidal disorders [6, 7].

The utilization of optical coherence tomography angiography (OCTA) in the diagnosis of diabetic retinopathy (DR) has seen a significant increase in recent years [8]. This is due to the ability of OCTA to visualize microvascular abnormalities that are indicative of DR. These abnormalities include the enlargement and irregularity of the foveal avascular zone (FAZ), capillary nonperfusion, intraretinal microvascular abnormalities (IRMA), and preretinal neovascularization (NV) [9, 10]. The recent advancements in swept-source OCTA (SS-OCTA) technology have allowed for a wider field of view, enabling the detection of early pathological changes in the retinal vasculature. A 12mm x 12mm or 15mm x 9mm field of view (FOV) with SS-OCTA can reveal these changes more accurately than traditional ultra-wide field fluorescein angiography (UWF FA) images [11]. The agreement between OCTA and FA in diagnosing DR was found to be excellent, with a kappa value of 0.916. The montage method used in SS-OCTA can be used to obtain ultra-wide FOV images, allowing for the detection of peripheral lesions (PPL) [12]. Wang et al. reported that a 12mm x 12mm SS-OCTA scan montage can achieve a FOV of 100°. The results showed that the peripheral sector of the wide-field OCTA (FOV 50–100) had a higher ratio of nonperfusion and a stronger diagnostic value in identifying the severity of DR compared to the central sectors [13].

It is crucial to note that imaging artifacts are a prevalent challenge in the application of OCTA, which can negatively impact the accuracy of measurements and lead to incorrect diagnostic conclusions [14, 15]. It is essential to consider the picture quality while utilizing OCTA for the diagnosis and monitoring of DR, as various factors such as poor patient compliance, media opacity, optical aberrations, and machine-related segmentation errors can result in the occurrence of artifacts. A comprehensive understanding of these artifacts is vital before conducting further qualitative and quantitative research with OCTA images. Despite the importance of this topic, limited studies have been conducted to investigate the prevalence of OCTA artifacts in patients with DR.

The goal of this study was to assess the quality of wide-field SS-OCTA images in DR, identify the presence of artifacts, and determine the major factors affecting image quality.

Study design

This prospective, observational study was conducted from May 2022 to October 2022. Individuals with proliferative DR (PDR), non-proliferative DR (NPDR), diabetic patients without DR, and healthy control eyes with no ocular diseases participated in the study. Eyes having associated retinal disorders, significant media opacities, and inadequate picture quality that prevented the device from automatically creating a montage image were also excluded. This study conformed to the tenets of the Helsinki Declarationa and was approved by the Ethics Committee of the Shanghai Sixth People's Hospital (No. 2021-KY-091(K)). Informed consent was obtained from all the participants.

The scans' quality scores were represented as a signal-to-noise ratio (SNR) in decibels (dB) on a scale of 1 (poor quality) to 10 (great quality); scans scoring more than 8 dB were judged satisfactory and included. Each subject had one eye chosen as the analysis eye, and if both eyes satisfied the eligibility requirements, one eye was chosen at random.

Each of the participants completed a comprehensive ophthalmologic test, which included taking a medical history, determining visual acuity, biomicroscopy of the anterior segment with a slit light, ophthalmoscopy of the posterior segment, and wide-field color fundus imaging with the Optos camera (Optos, Dunfermline, UK).

Swept-Source OCTA

A commercial SS-OCTA equipment was used to obtain three-dimensional OCTA scans of 12×12 mm² areas (VG200S; SVision Imaging, China). In the commercial SS-OCT device, an SS laser with a central wavelength of roughly 1050 nm (990–1100 nm full width) and a scanning rate of 20 kA scans/s was employed. At the retinal surface, the device possessed a full-width at half maximum axial resolution of around 5 mm and an estimated lateral resolution of roughly 15 mm. Volume data, which included both OCT and OCTA, were collected using a raster scan protocol of 1024 (horizontal)×1024 (vertical) B-scans repeated twice at each of 1024 B-scan points, which takes about 12 s per scan with an artificial intelligence-assisted tracking system. To capture a broad FOV (23.5 mm×17.5 mm; 5-scan composite), OCTA images were acquired at five fixation positions (central, inferior nasal, superior nasal, inferior temporal, and superior temporal) (Fig. 1). A built-in software was utilized to create a composite picture from five OCTA photographs and placed on UWF color images.[16] Professional ophthalmic photographers carried out the OCTA scanning; they duplicated the picture acquisitions several times to provide photos with good OCT signal penetration and fewer motion artifacts.

Imaging artifacts and quality evaluation

Table 1 summarizes the classification and comprehensive explanation of artifacts in montage OCTA pictures.^{15, 16} The images were assessed for the following artifacts: systemic, image processing and display, and artifacts caused by movement. Each artifact was graded on a severity scale of 0–3. “0” indicated that the artifact area is < 5% of the total. Mild severity, graded as 1, indicated that the affected area is between 5% and 15% of the total. Moderate severity, graded as 2, indicated that the affected area is between 15% and 25% of the total. Severe severity, graded as 3, indicated that the affected area is > 25% of the total. The total score of an image is the cumulative sum of all individual scores. When the total score exceeds 3 points, it is judged as severe severity, i.e., the excess of the affected part leads to a bad image that influences the judgment of the disease or the identification of the lesion.

Table 1

Classification, Definition and Scores of Artifacts in OCTA Montage Images
classification	artifacts	definition	0–5%	5%-15%	15%-25%	≥ 25%
systemic artifacts	masking	Low signal regions originating from the more anterior dense lesions such as vitreous opacities, haemorrhage, scar tissue, pigment clumps and so on blocking the light to reach the deeper layers	0	1	2	3
systemic artifacts	loss of signal	Appeared as a localized area of signal loss on the en face image due to loss of scan focus, more common in eyes with tumor, high myopia, or hyperopia, partially operator-dependent	0	1	2	3
image processing and display	segementation artifact	Errors in (automatic) segmentation may lead to incorrect OCTA results.	0	1	2	3
	duplication of vessels	As a result of image processing, vessels are displayed twice directly next to each other within a layer.	0	1	2	3
	Alignment error	The superior and inferior part of the montage image appeared to be of different depth, possibly due to projection removal	0	1	2	3
artifacts caused by movement	displacement	Very thin vertical lines leading to an apparent interruption or displacement of the vessels caused by eye movements	0	1	2	3
	blink artifact	A region of lost image information related to eye movement. It appears as an end-to-end black line of varying width through all depths of en face scans.	0	1	2	3
	stretch artifact	Short stripes of different brightness at the edges of OCTA images.	0	1	2	3
Total Scores: excellent ≤ 1,༞1good༜3,≥3inferior

Two qualified and certified graders independently examined the photos for the existence and degree of artifacts (S.T.L. and X.C.). In the case that the two graders disagreed, another senior grader (D.L.) served as the adjudicator.

Statistical Analysis

SPSS program, version 27.0, was used to conduct all of the data analyses (IBM Corporation, Chicago, IL, USA). Continuous variables with properly distributed distributions were reported as meanstandard deviation, whereas nonnormally distributed continuous data were presented as median (interquartile range [IQR]). The One Way Variance Analysis/Kruskal Wallis test was used to determine the significance of the difference between the groups. Binary comparisons were performed in groups with differences to determine which groups the difference originated from. Differences in severe rates among different groups were compared using the McNemar’s test or the exact McNemar’s test. A 2-tailed P value of less than 0.05 was considered statistically significant for all analysis.

Demographic and Clinical Characteristics of the Included Subjects

This study included 70 eyes (16 with PDR, 24 with NPDR, 12 diabetic patients without DR, and 18 with healthy eyes) in 70 subjects using montage images (Table 2). The participants' average age was 53.29 ± 12.51 years, and no significant difference in age was found between the four groups (P = 0.125) (Table 3). In this study, a total of 52 individuals with diabetes were enrolled, with 7 (13.46%) having type 1 diabetes mellitus (T1DM). The median logMAR best-corrected visual acuity (BCVA) in patients with proliferative diabetic retinopathy (PDR) was 0.29 ± 0.19, with the lowest recorded value being 0.80 (equivalent to 10/100 Snellen acuity).

Table 2

Demographic Data of Participants Parameter
Parameter	Value
Participants(eyes)	70(70)
Age,y mean ± SD	53.29 ± 12.51
Sex (participants), n(%)
Male	27(51.92)
Female	25(48.08)
Type of diabetes (participants)
T1DM, n(%)	7(13.46)
T2DM, n(%)	45(86.54)
Duration of diabetes (years)	13.78 ± 5.81
HbA1c, %a, mean ± SD	7.88 ± 1.94
Groups (severity of DR, eyes), n (%)
Healthy eye	18(25.71)
No DR in DM patients	12(17.14)
NPDR	24(34.28)
PDR	16(22.87)
Involved eye, n (%)
Right	35(50%)
Left	35(50%)
BCVA (LogMAR), n (IQR)	0.29 ± 0.19 (0, 0.6)

Table 3

Score and severe seventy in different groups
Groups (Eyes)	Healthy (18)	No DR (12)	NPDR (24)	PDR (16)	P Value
Age	48.78 ± 15.40	58.08 ± 15.25	50.06 ± 11.62	53.29 ± 13.87	P = 0.125
BCVA	0.04 ± 0.05	0.07 ± 0.08	0.39 ± 0.21	0.59 ± 0.21	p < 0.001
Scores	2(2,2)	2.16(2,3)	3.42(3,5)	5.38(5,6)	p < 0.001
Severe/total	0/18	2/12	10/24	16/16	p < 0.001

Frequency and Distribution of OCTA Image Artifacts

In this study, 69 out of 70 (98.57%) eyes had at least one type of artifact, with only one healthy control eye without any artifact. The most commonly observed artifact was loss of signal, which was present in 63 (90%) eyes. This was followed by displacement artifacts in 43 (61.4%) eyes and masking artifacts in 43 (61.4%) eyes. Other artifacts observed in this study included alignment error, present in 27 (35.6%) eyes, blink artifacts in 21 (30%) eyes, duplication of vessels in 4 (5.7%) eyes, and segmentation artifacts in 2 (2.8%) eyes.

Scoring System for OCTA Image Artifacts

According to our scoring scale, the average score for all eyes was 3.23 (range: 2–4). Among these, 41 (58.57%) eyes had > 3 points. In the healthy and the no DR groups, the mean scores of the two groups were 2 and 2.16, respectively, which were smaller than those of the NPDR and the PDR groups (3.42 and 5.38, p < 0.001). Moreover, the scores in the PDR group were significantly higher than those in the NPDR group (p < 0.001) (Fig. 2). No statistically significant difference was detected between the healthy and the no DR groups (p = 0.949). The proportion of severe cases (score > 3) was highest in the PDR group at 100% (p < 0.001), followed by 41.67% in the NPDR group (p < 0.001). However, no statistically significant differences were detected between the healthy and the no DR groups (p = 0.097).

Factors Related to Image Quality

In addition, the correlation between the artifact scores and the variables was analyzed. Univariate and multivariate regression analysis revealed that eyes with a severe stage of DR had high artifact score (p < 0.05) (Table 4).

Table 4

Univariate and Multivariate Regression Analysis for artifacts scores
	artifacts scores		artifacts scores
Parameter	B	P	B	P
Age	-0.011	0.487
BCVA, LogMAR	3.656	< 0.001	0.218	0.812
Severity of DR (groups)	1.084	< 0.001	1.051	< 0.001

The results of this study indicate that imaging artifacts are a common issue in OCTA, with 98.57% of eyes having at least one type of artifact. The most prevalent artifacts were loss of signal and displacement artifacts, which were found in 90% and 61.4% of eyes, respectively. The results also showed that the average score for all eyes was 3.23, with 41 (58.57%) eyes having a score greater than 3 points, which was considered severe.

When compared to the central retina, DR presents early pathological vascular alterations in the peripheral/mid-peripheral retina, supporting the necessity for UWF imaging of the retinal vasculature. Silva et al.[17] demonstrated that in approximately 33% of patients, early peripheral changes such as hemorrhages, microaneurysms, venous beading, intraretinal microvascular abnormalities, and retinal neovascularization could not be captured using the protocols of the Early Treatment Diabetic Retinopathy Study (ETDRS) study fields. As a result, if a traditional fundus camera with a narrow FOV is used, a considerable proportion of individuals with DR results may be overlooked. The advantages of OCTA imaging can be integrated with the technology of UWF imaging to completely analyze early peripheral alterations now that UWF OCTA methods are available [18, 19]. Several comparisons have been made in the literature between UWF color fundus photography, FA, and OCTA. For identifying DR lesions, UWF OCTA has been proven to have superior sensitivity and specificity [11, 12, 20–22]. Furthermore, compared to FA, UWF OCTA employing EFI is rather comfortable for the patients [11].

The present study aimed to describe the imaging artifacts and evaluate the quality of the images in UWF SS-OCTA. In comparison to traditional 6 mm× 6 mm or 12 mm× 12 mm photos, capturing the Angio 23.5 mm× 17.5 mm image necessitates numerous additional considerations: (1) Fixation loss is common due to the extended acquisition time, resulting in additional artifacts, especially in the periphery; ¹⁶ (2) The curvature of the eye makes it difficult to keep the 23.5mm× 17.5mm scan span in focus for the montage image throughout acquisition (especially in the peripheral), and thus signal loss is more common than with conventional, shorter scans; (3) the Angio 23.5 mm×17.5-mm image was composed of vertical scans from top to bottom, and the motion artifacts caused by the eye movement were vertical; (4) several eyelash artifacts were mainly located in the inferior far retinal periphery because the imaging range of our research was 80×60°, which is susceptible to shadowing artifacts due to superior eyelashes (Fig. 3) [23].

The most common artifacts in this investigation were signal loss, which manifested as a localized patch of signal loss on the en face image due to scan focus loss. Beyond defocus, other common sources of global signal attenuation are cataracts and tear film break up. This phenomenon was common in eyes with tumors, high myopia, or hyperopia and was partially operator-dependent. Because of our wide acquisition, there is often a loss of signal around the retina, especially the peripheral vision, which may be because the eyeball is similar to an ellipse. During the peripheral scanning process, the curvature of the periphery of the eyeball is enlarged relative to the point of gaze. The curvature of the eye makes it difficult to keep in focus; thus, the signal may be folded or even flipped. The Super Depth technology was utilized to present the surrounding signals in the same 12×12 area to obtain a complete puzzle. Nihaal Mehta et al[24] found that there was a significant significant change in flow impairment area with montage OCTA images, which was more pronounced peripherally than centrally.

Displacement is the second most frequent artifact. Due to eye movements, very thin vertical lines induce an apparent disruption or displacement of the vessels. When acquiring the puzzle, at least 5 OCTA images of 12×12 area need to be scanned. Typically a 12×12 scan takes about 12s. The degree of cooperation of the patient decreases in a time-dependent manner, and eye movements or involuntary blinking of the eyes often occur while acquiring peripheral images, resulting in artifacts [5]. A putative solution is as follows: first, we allowed the patient to obtain a sufficiently comfortable posture before acquiring the image, thereby improving the patient’s ooperation. Second, if such an artifact occurs, the patient can be allowed to rest or relax with proper eye closure between scans. Third, if the patient has dry eye discomfort, sodium hyaluronate eye drops can be administered to relieve the patient’s dry eye symptoms, allowing the patient to complete the examination comfortably. In addition, real-time tracking could be improved to remove bulk motion artifacts [25].

Similarly, as DR progresses, there will be more refractive interstitial opacities, occlusion artifacts, and possibly dry eyes [16, 26], which gives rise to artifacts during image acquisition. Russell JF et al[27] used wide-field SS-OCTA to image diabetic tractional retinal detachments (TRDs) before and after pars plana vitrectomy. This result indicates that if the media are clear and fixation is acceptable, WF SS-OCTA might be the sole imaging modality required for the diagnosis and follow-up of diabetic TRDs. Diabetic TRD eyes with a preoperative BCVA less than 20/400 and/or a thick cataract or VH, on the other hand, cannot be acquired as high-quality preoperative SS-OCTA images.

In the current study, for the first time, we scored and graded the artifacts with ultrawide-field SS-OCTA in DR. The artifact is divided into three grades. When the total score is > 3 points, the quality of the image is poor, which affects the judgment and diagnosis of the disease. Hence, this is only an exploratory grading method. With the continuous development and progress of SS-OCTA technology, the treatment of images is elevated, and there may be a suitable scoring system. Importantly, we hope that our scores can provide a reference for the application of the ultrawide-field SS-OCTA in DR. It is also crucial for researchers to focus on the quality of images. Herein, we did not evaluate the error separation of the system (similar to the segmentation artifact and projection artifact) because the software and algorithms are continuously updated and upgraded. Some separation errors can be corrected by manual adjustment. It is difficult to improve the quality when acquiring images by these methods.

Nevertheless, the present study had some limitations: (1) the sample size was small, and there was a lack of consensus or guidelines for UWF OCTA. Due to the small sample size, data from the same hospital may have biased results. Thus, large sample sizes and multicenter studies are needed; (2) the ocular surface state was not tested objectively; (3) the lens status was not taken into account in the correlation analysis.

In conclusion, this study provides evidence for the high frequency and severity of artifacts in OCTA images of patients with diabetic retinopathy. Assessing the picture quality and understanding the sources of artifacts is crucial for accurate diagnosis and monitoring of diabetic retinopathy using OCTA. As the use of OCTA and wider scanning patterns becomes increasingly prevalent in DR clinical trials, the need for methods to enhance image quality and minimize artifacts becomes imperative for the optimal clinical implementation of this growing, but informative OCTA technology.

SS-OCTA

swept-source optical coherence tomography angiography

Diabetic retinopathy

PDR

proliferative diabetic retinopathy

NPDR

nonproliferative diabetic retinopathy

OCTA

Optical coherence tomography angiography

three-dimensional

FAZ

foveal avascular zone

IRMA

intraretinal microvascular abnormalities

neovascularization

FOV

field of view

UWF FA

ultra-wide field fluorescein angiography

PPL

peripheral lesions

SNR

signal-to-noise ratio

ETDRS

Early Treatment Diabetic Retinopathy Study

TRDs

tractional retinal detachments

T1DM

type 1 diabetes mellitus

BCVA

best-corrected visual acuity.

Ethics approval and consent to participate: The study adhered to the guidelines of the Helsinki Declaration and had the approval of the Ethics Committee of Shanghai Sixth People's Hospital (No. 2021-KY-091(K)). All patients signed written informed consent for participation.

Consent for publication: Not applicable.

Availability of data and materials:The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Competing interests: The authors declare that they have no competing interests.

Funding: Supported by the College-level Project Fund of Shanghai Sixth People's Hospital (Grant No. ynlc201909); the Interdisciplinary Program of Shanghai Jiao tong University (Project No. YG2022QN089) and the Natural Science Foundation for Youths of Jiangsu Province [grant number: BK20190162].

Authors' contributions: Conceived and designed the experiments: XW, SL, QW. Performed the experiments: XW, SL,QW. Analysed the data: XC, TL. Contributed reagents/materials/analysis tools: TL, DL. Wrote the paper: XW, SL. Discussion of the results and critical review of the manuscript:XW, QW. All authors have read and approved the manuscript, and ensure that this is the case.

Acknowledgements: Not applicable.

Authors' information: ¹Department of Ophthalmology, Shanghai Sixth People's Hospital, 600 Yishan Road, Shanghai 200233, China. ² Department of Ophthalmology, The First People's Hospital of Changzhou, Changzhou 223000, China.

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No competing interests reported.

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Imaging artifacts and quality evaluation with ultrawide-field swept-source OCTA in diabetic retinopathy

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Journal Publication

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Abstract

Figures

Background

Methods

Study design

Swept-Source OCTA

Imaging artifacts and quality evaluation

Statistical Analysis

Results

Demographic and Clinical Characteristics of the Included Subjects

Frequency and Distribution of OCTA Image Artifacts

Scoring System for OCTA Image Artifacts

Factors Related to Image Quality

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

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