Quantitative Analysis of the Changes of Retinal Blood Flow Density and Retinal Thickness in Patients with Diabetic Retinopathy by OCTA

doi:10.21203/rs.3.rs-4103894/v1

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Quantitative Analysis of the Changes of Retinal Blood Flow Density and Retinal Thickness in Patients with Diabetic Retinopathy by OCTA

https://doi.org/10.21203/rs.3.rs-4103894/v1

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In our current study, we aim to quantitatively analyze the alterations in retinal BFD and retinal thickness in patients with diabetic retinopathy using optical coherence tomography angiography (OCTA). We analyzed retinal blood flow density (BFD) and thickness in 60 diabetic retinopathy patients using OCTA, comparing them with 60 healthy individuals. Results showed significant lower retinal BFD in the observation group in both superficial and deep capillaries. The retinal thickness of the patients in the observation group was greater. the overall and paracentric concave of the BFD in the superficial capillary layer, the overall and paracentric concave, and subcentral concave of BFD in deep capillary layer, and the overall, central concave, paracentric concave, and subcentral concave of retinal thickness had a certain correlation with diabetic retinopathy. The overall, central concave, paracentric concave, and subcentral concave of the BFD in superficial and deep capillary layer and retinal thickness all had certain predictive values for diabetic retinopathy, and predictive values for the disease were indicated by AUC values ranging from 0.616 to 0.990 (p < 0.05). OCTA examination revealed a notable decrease in retinal BFD and increase in retinal thickness, suggesting its potential as a diagnostic tool for diabetic retinopathy.

OCTA

diabetic retinopathy

retinal blood flow density

retinal thickness

Diabetes is a common clinical chronic illness. The global prevalence of diabetes is approximate 9%. It is estimated 1 out of 10 adults will suffer from diabetes by 2040 ^[1–2]. Diabetic retinopathy, a common complication of diabetes, stands as the leading cause of vision impairment and potential blindness in individuals during their most productive years ^[3–4]. As China's economy expands and the duration of diabetes cases extends, the incidence of diabetic retinopathy continues to rise annually, accompanied by an increasing rate of blindness associated with this condition. ^[5–6]. As the disease progresses, patients may encounter a range of symptoms including different levels of vision loss, floaters, and other issues such as palpitations, fainting, diarrhea, and constipation. These symptoms present a significant risk to both physical and mental well-being. ^[7–8]. Therefore, early diagnosis and appropriate intervention are crucial in effectively reducing the rate of blindness caused by this disease.

Several clinical diagnostic techniques are available for early diagnosis, yet they often come with drawbacks like invasive procedures and potential allergies to contrast agents. Consequently, the use of optical coherence tomography angiography (OCTA) has gained popularity in recent years due to its higher resolution. OCTA excels in vividly depicting the retina and choroid images, allowing for precise detection of vascular abnormalities in the patient's retina. Moreover, it can quickly and significantly ascertain vascular damage ^[9–10]. In addition, it can also quantitatively analyze the blood flow density, with good repeatability and consistency ^[11–12]. OCTA offers an effective approach for early monitoring and tracking the progress of diabetes and related complications. Substantial amount of qualitative and quantitative research has been conducted on the retinal and choroidal blood flow systems in various eye diseases ^[13–14]. Yet, quantitative analysis of changes in retinal blood flow density (BFD) and retinal thickness in individuals affected by diabetic retinopathy has not been reported. Hence, this study aims to quantitatively analyze the alterations in retinal BFD and retinal thickness in patients with diabetic retinopathy using OCTA, thus deepen our comprehension of the disease.

General data

All of 60 patients with diabetic retinopathy received in our hospital from May 2020 to September 2022 were included as subjects in the observation group. Inclusion criteria were 1) individuals met the diagnostic criteria for type 2 diabetes ^[15]; 2) individuals matched the diagnostic criteria for diabetic retinopathy ^[16]; 3) individuals who were > 18 years old. Exclusion criteria included 1) patients with retinopathy caused by other reasons except diabetes; 2) patients exhibiting solely optic neuropathy with no apparent systemic diseases; 3) patients who received treatment (e.g., retinal laser photocoagulation) in the past. A total of 60 healthy physical examiners who were matched in age and gender with the patients were included as the control group. Inclusion criteria were 1) individuals who were > 18 years old; 2) individuals without obvious abnormal eye lesions. Exclusion criteria included 1) individuals with eye diseases in the past; 2) individuals with eye surgery in the past; 3) individuals with hypertension, cardiovascular or cerebrovascular illnesses. This research was approved by the Ethics Committee of our hospital, and the participants and their families gave informed consent.

Methods

Inspection method

Angio retina mode (3 mm × 3 mm) was used to scan the macular area during OCTA examination, and then the images with SQI ≥ 6 was saved. During the operation, the objective factors that affected image quality, such as severe jitter and unstable tear film should try to be avoided. All inspections were completed by the same ophthalmologist with rich experience in operation. The two measurement results were collected, and the average value was taken as the final result for subsequent comparison. The software automatically took the central fovea of the macula as the center, divided the area within the diameter of 1 mm into the central concave area, and divided the area within the diameter of 1–3 mm into the paracentric concave area. The system's own software was used to analyze the overall, central concave, paracentric concave, and subcentral concave blood flow density of the superficial retinal capillary layer and the deep retinal capillary layer, as well as the overall, central concave, paracentric concave, and subcentral concave retinal thickness (Fig. 1).

Observation indicators

The common data for example age and gender of the 2 groups of research objects were observed; the retinal BFD of the 2 groups of research objects was observed; the changes in retinal thickness of the two groups of research objects were observed; the correlation between OCTA inspection parameters and retinopathy in sufferers with diabetic retinopathy was analyzed; analyze the diagnostic values of OCTA inspection parameters on retinopathy in sufferers with diabetic retinopathy were analyzed.

Statistical methods

SPSS 22.0 statistical software was used to process and statistically analyze the experimental data. The measurement data were represented by mean ± standard deviation (‾χ ± s), and independent sample t-test was used for comparison between two groups; count data were represented by rate (%), and conducted with χ²-test, and Pearson was used for correlation analysis; ROC was used for predictive value diagnosis, and p < 0.05 was considered as a statistically obvious distinction.

Clinical characteristics of participants indicated no statistically obvious difference between the control and observation group (p > 0.05) (Table 1).

Table 1

The clinical characteristics of subjects
Group	Number of eyes	Age (Mean ± SD)	Gender: (Male/Female)	BMI (kg/m² )	Eyes (Left/Right)
observation group	60	57.60 ± 10.50	33/27	24.55 ± 2.96	35/25
control group	60	55.60 ± 13.50	31/29	23.98 ± 3.05	29/31
t		0.906	0.134	0.004	1.205
P		0.367	0.714	0.997	0.272

We next measured BFD for the participants. BFD in the superficial retinal capillary layer in the observation group was significantly lower than those of the control group (Table 2). Specifically, the overall BFD in the superficial retinal capillary layer in the observation group was lower than the control group (44.05 ± 4.05 vs 49.56 ± 2.30, p < 0.001). Similarly, BFD of the central concave (13.05 ± 3.95 vs 15.85 ± 5.95, p < 0.003), aracentric concave (44.05 ± 4.52 vs 51.70 ± 2.86, p < 0.001), and suncentral concave (44.80 ± 4.69 vs 50.40 ± 5.74, p < 0.001) in the observation group was significantly lower than those in the observation group.

Table 2

The BFD in the superficial retinal capillary layer ( x̅ ± s, %)
group	Number of eyes	overall	Central concave	Aracentric concave	Subcentral concave
Observation group	60	44.05 ± 4.05	13.05 ± 3.95	44.05 ± 4.52	44.80 ± 4.69
Control group	60	49.56 ± 2.30	15.85 ± 5.95	51.70 ± 2.86	50.40 ± 5.74
t		9.164	3.037	11.093	5.847
P		< 0.001	0.003	< 0.001	< 0.001

We also investigated BFD for the participant in the deep retinal capillary layer. The results indicated that BFD in the deep capillaries in the observation group was statistically significantly lower than those of the control group (Table 3). Specifically, the overall BFD in the superficial retinal capillary layer in the observation group (42.20 ± 3.85) was lower than the control group (61.58 ± 8.55) Similarly, BFD of the central concave (26.05 ± 6.53 vs 28.41 ± 5.96, p = 0.041), aracentric concave (45.10 ± 5.96 vs 53.10 ± 3.52, p < 0.001), and suncentral concave (42.09 ± 4.35 vs 49.52 ± 5.10, p < 0.001) in the observation group was significantly lower than those in the observation group.

Table 3

**The BFD in the deep retinal capillary layer** ( x̅ ± s, %)
Group	Number of eyes	Overall	Central concave	Aracentric concave	Subcentral concave
Observation group	60	42.20 ± 3.85	26.05 ± 6.53	45.10 ± 5.96	42.09 ± 4.35
Control group	60	61.58 ± 8.55	28.41 ± 5.96	53.10 ± 3.52	49.52 ± 5.10
t		16.001	2.064	8.955	8.594
P		< 0.001	0.041	< 0.001	< 0.001

Next, we measured retinal thickness of the 2 groups. In comparison of the control group, the retinal thickness of the observation group was greater (315.50 ± 13.50 vs 285.30 ± 9.50, p < 0.001) (Table. 4). We observed similar trends in the central concave, aracentric concave, and subcentral concave (Table. 4).

Table 4

Retinal thickness (x̅± s, µm)
Group	Number of eyes	Overall	Central concave	Aracentric concave	Subcentral concave
Observation group	60	315.50 ± 13.50	280.80 ± 10.50	340.20 ± 15.90	340.25 ± 30.40
Control group	60	285.30 ± 9.50	235.80 ± 15.60	315.20 ± 12.30	288.50 ± 26.60
t		14.173	18.541	9.634	9.923
P		< 0.001	< 0.001	< 0.001	< 0.001

We performed a correlation analysis of BFD and retinal thickness with diabetic retinopathy. The results indicated that BFD in superficial capillary layer was negatively correlated with diabetic retinopathy (Table 5a). Overall BFD in deep capillary layer was negatively associated with diabetic retinopathy (p < 0.001), as well as the central concave and aracentric concave. However, the subcentral concave BFD in deep capillary layer was positively associated with diabetic retinopathy (Table 5b). Retinal thickness was positively correlated with diabetic retinopathy (Table 5c).

Table 5

a. Correlation analysis of BFD in superficial capillary layer with diabetic retinopathy
Statistics	BFD in superficial capillary layer
Statistics	Overall	Central concave	Aracentric concave	Subcentral concave
r	-0.645	-0.269	-0.714	-0.474
p	< 0.001	0.003	< 0.001	< 0.001

Table 5

b. Correlation analysis of BFD in deep capillary layer with diabetic retinopathy
Statistics	BFD in deep capillary layer
	Overall	Central concave	Aracentric concave	Subcentral concave
r	-0.827	-0.187	-0.636	0.620
p	< 0.001	0.041	< 0.001	< 0.001

Table 5

c. Correlation analysis of retinal thickness with diabetic retinopathy
Statistics	Retinal thickness
	Overall	Central concave	Aracentric concave	Subcentral concave
r	0.794	0.863	0.664	0.674
p	< 0.001	< 0.001	< 0.001	< 0.001

At last, we calculated the ROC to evaluate the predictive power of the variables for diabetic retinopathy. The overall BFD in superficial capillary layer showed a ROC of 0.888, with central concave, aracentric concave, and subcentral concave of 0.627, 0.923, and 0.771, respectively (Table 6 and Fig. 2). The overall, central concave, aracentric concave, and subcentral concave of BFD in deep capillary layer exhibited a ROC value of 0.983, 0.616, 0.882, 0.862, respectively (Table 7 and Fig. 3). Retinal thickness also displayed high predictive value for diabetic retinopathy of 0.960, 0.990, 0.897, 0.899 for overall, central concave, aracentric concave, and subcentral concave (Table 8 and Fig. 4).

Table 6

ROC of BFD-related variables in superficial capillary layer
Variables	AUC	Best cut-off value	Youden index	SE	95% CI	p	Sensitivity (%)	Specificity (%)
Overall	0.888	46.57	0.667	0.031	0.818–0.939	< 0.001	75.00	91.67
Central concave	0.627	16.62	0.267	0.051	0.534–0.714	0.013	83.33	43.33
Aracentric concave	0.923	48.14	0.750	0.027	0.860–0.964	< 0.001	83.33	91.67
Subcentral concave	0.771	47.39	0.433	0.042	0.686–0.843	< 0.001	73.33	70.00

Table 7

ROC of BFD-related variables in deep capillary layer
Variables	AUC	Best cut-off value	Youden index	SE	95% CI	p	Sensitivity (%)	Specificity (%)
Overall	0.983	48.65	0.900	0.012	0.940–0.998	< 0.001	96.67	93.33
Central concave	0.616	25.96	0.233	0.052	0.523–0.703	0.025	55.00	68.33
Aracentric concave	0.882	48.75	0.717	0.033	0.811–0.934	< 0.001	78.33	93.33
Subcentral concave	0.862	46.56	0.600	0.033	0.787–0.918	< 0.001	88.33	71.67

Table 8

ROC of retinal thickness-related variables
Variables	AUC	Best cut-off value	Youden index	SE	95% CI	p	Sensitivity (%)	Specificity (%)
Overall	0.960	299	0.833	0.016	0.908–0.988	< 0.001	86.67	96.67
Central concave	0.990	261	0.933	0.007	0.951-1.000	< 0.001	98.33	95.00
Aracentric concave	0.897	326	0.667	0.028	0.828–0.945	< 0.001	85.00	81.67
Subcentral concave	0.899	319	0.683	0.027	0.830–0.946	< 0.001	78.33	90.00

Diabetic retinopathy is a prevalent fundus vascular disorder, characterized as a progressively visual impairment, primarily marked by damage to the microvasculature of the retina. In patients with a long history of the disease, nearly all will experience varying degrees of retinal microvascular complications, often accompanied by retinopathy. This condition significantly impacts vision, particularly in younger patients, who not only tend to experience a more rapid onset of the disease but also face a higher recurrence rate post-treatment ^[17–18]. As a new diagnostic technique, OCTA achieves the purpose of visualizing retinal and choroid capillaries through layered vascular reconstruction, and uses new algorithms to generate high-resolution images. Compared with other diagnostic techniques, it has the advantages of non-invasiveness, no mydriasis, and no time window limitation, and can quantitatively analyze the blood flow in each layer of blood vessels, so it has been widely used in ophthalmology at home and abroad ^[19–20]. This technology can not only detect the retinopathy in patients, accurately diagnose diabetic eyes with higher risk, but even screen out diabetes before systematic diagnosis, which has a good predictive effect. However, no research has done a clear quantitative analysis on the changes of retinal BFD and retinal thickness in sufferers with diabetic retinopathy, and no diagnostic prediction has been made. Therefore, this study conducted quantitative analysis through OTCA and observed its predictive values on the disease.

In this study, the clinical characteristics of the objects were first observed, and the outcomes showing that the clinical data of the 2 groups of research objects had no significant statistical significance, which indicates that the baseline data of all the research objects are evenly distributed and comparable, also proves that the randomness characteristics of the study subjects' enrollment and means that the final results of this study are more reliable. In addition, the outcomes of the blood flow density experiment in this research showed that in comparison of the control one, the BFD of the superficial and deep capillaries in the observation one was less, which indicates that the BFD in the superficial retina after retinopathy in diabetic patients begins to be significantly decreased, and it is possible that as the disease progresses, the blood flow density may continue to be decreased, but this study did not conduct such analysis. Some studies suggest that there is a significant difference in paracentric concave, and subcentral concave BFD, and the BFD in the deep part is decreased more obviously with the increasing severity of the disease, and the BFD in the whole paracentric concave is decreased more obviously ^[21–22]. This is also somewhat similar to the outcomes of this research. In addition, the outcomes in the experiment of the retinal thickness showing that in comparison of the control one, the retinal thickness of the sufferers in the observation one was greater. The study showed that the comparative difference in the thickness of the central concave was the most significant, which is due to the reduction of retinal blood flow density, resulting in retinal tissue ischemia and hypoxia, secondary edema, and central concave traction. Because of the lower thickness of central concave itself, the change scope is more pronounced. In addition, the cone cells of central concave have powerful metabolic functions and are extremely sensitive to hypoxia. When there is circulatory disturbance, due to insufficient oxygen supply, the cone cells will accumulate a large number of metabolites, resulting in edema that is more pronounced than the surrounding area ^[23–24]. In order to verify the correlation between OCTA and diabetic retinopathy, this study conducted a correlation analysis, and the results showed that: the overall and paracentric concave of the blood flow density in the superficial capillary layer, the overall and paracentric concave, and subcentral concave of BFD in deep capillary layer, and the overall, central concave, paracentric concave, and subcentral concave of retinal thickness had a certain correlation with diabetic retinopathy (r=-0.645, -0.714, -0.827, -0.636, -0.620, 0.794, 0.863, 0.664, 0.674, P < 0.05). This shows that OCTA examination may be able to predict the disease; it shows that OCTA examination does have a high diagnostic value for retinopathy in patients with diabetic retinopathy. Early studies have found that OCTA image analysis has an exact diagnostic value for macular microvascular lesions in patients with diabetic retinopathy. OCTA subdivides the detection range with the center of the macular fovea, which can accurately reflect the hemorrhage in macular region in patients with diabetic retinopathy. Retinal surface capillaries can reveal the border of the avascular area of macular fovea. Due to the high definition and high measurement accuracy, the area, perimeter and shape indices of the macular foveal avascular zone can be understood. Analyzing the severity of capillary arch damage in the macular area facilitates the targeted scientific intervention ^[25–26]. Not only that, OCTA is a tool that can detect microvascular changes in diabetic retinopathy, including microvascular tumors, non-perfused areas, retinal edema, vascular rings, and intraretinal microvascular changes ^[27–28]. In addition, OCTA can also provide measurement and quantification of foveal avascular area, vessel density, perfusion density, etc. Changes in these measures of vascular function have almost universally been shown to be associated with increased severity of diabetic retinopathy and worsening vision ^[28–30]. These indicators may serve as potential biomarkers of diabetic retinopathy in different courses of disease, and are crucial for predicting the grade of diabetic retinopathy, identifying patients at risk, selecting treatment methods, and observing the effects of follow-up treatment. Therefore, based on this, the ROC curve was also drawn in this study to analyze the predictive values of OCTA for the disease. The results showed that the overall, central concave, paracentric concave, and subcentral concave of the BFD in superficial and deep capillary layer and retinal thickness all have certain predictive values for diabetic retinopathy, and AUC were: 0.888, 0.627, 0.923, 0.771, 0.983, 0.616, 0.882, 0.862, 960, 0.990, 0.897, 0.899, respectively, with good predictive values, indicating that is has a good clinical application value.

In summary, OCTA examination can clarify the changes of retinal BFD and retinal thickness, and the retinal BFD of the patients is decreased significantly, while the retinal thickness is increased, which may be able to monitor the severity of the patients' conditions, and OCTA examination can be used to predict the disease to a certain extent. It has a significant clinical application value, and it is recommended to be popularized and applied. However, this research is a retrospective analysis with a small sample size, so more samples need to be accumulated to analyze more detailed results, and the correlation between OCTA examination and the severity of the disease has not been analyzed, which needs to be further explored.

Author Contribution

guarantor of integrity of the entire study： R.L. study concepts： R.L.study design： R.L.,Y.W.definition of intellectual content： R.L.literature research：Y.W.experimental studies：Y.W.manuscript preparation：Y.W.manuscript review： R.L.All authors reviewed the manuscript.

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Quantitative Analysis of the Changes of Retinal Blood Flow Density and Retinal Thickness in Patients with Diabetic Retinopathy by OCTA

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