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The effect of long-term hemodialysis on diabetic retinopathy observed by swept-source optical coherence tomography angiography

BMC Ophthalmology volume 24, Article number: 334 (2024) Cite this article

Abstract

Background

Diabetes can cause chronic microvascular complications such as diabetic retinopathy (DR) and diabetic nephropathy (DN). DR and DN can lead to or exacerbate diabetic macular edema (DME). Hemodialysis (HD) is the main treatment method for patients with end-stage kidney disease (ESKD) secondary to DN.

Purpose

The aim of this prospective cohort study was to determine the immediate effect of single HD session on retinal and choroidal thickness in DR patients with ESKD and the features of DR and the prevalence of DME in these patients who have received long-term HD.

Methods

Eighty-five eyes of 44 DR patients with ESKD who underwent long-term HD were examined by swept-source optical coherence tomography angiography (SS-OCTA). Based on OCTA images, the characteristics of DR and the prevalence of DME in these patients were analyzed. Changes in central retinal thickness (CRT), central retinal volume (CRV), subfoveal choroidal thickness (SFCT) and subfoveal choroidal volume (SFCV) within 30 min before and after single HD session were compared. CRT, CRV, SFCT and SFCV were compared before single HD session and before the next single HD session.

Results

There was no significant difference in the average CRT (251.69 ± 39.21 μm vs. 251.46 ± 39.38 μm, P = 0.286) or CRV (0.15 ± 0.62 μm vs. 0.15 ± 0.63 μm, P = 0.324) between before and after single HD session. After single HD session, SFCT (243.11 ± 77.15 μm vs. 219.20 ± 72.84 μm, P < 0.001) and SFCV (0.15 ± 0.10 μm vs. 0.13 ± 0.90 μm, P < 0.001) significantly decreased. There was no statistically significant difference in CRT (251.69 ± 39.21 μm vs. 251.11 ± 38.47 μm, P = 0.206), CRV (0.15 ± 0.62 μm vs. 0.15 ± 0.61 μm, P = 0.154), SFCT (243.11 ± 77.15 μm vs. 245.41 ± 76.23 μm, P = 0.108), or SFCV (0.15 ± 0.10 μm vs. 0.16 ± 0.10 μm, P = 0.174) before HD and before the next single HD session. On en face OCTA images, eighty-five eyes (100%) had retinal nonperfusion areas, foveal avascular zone (FAZ) enlargement, and abnormal retinal microvasculature. Based on cross-sectional OCTA images, retinal neovascularization (RNV) was confirmed in 42 eyes (49.41%), and intraretinal microvascular abnormalities (IRMAs) were detected in 85 eyes (100%). Seventeen eyes (20%) still had DME, all of which were cystoid macular edema (CME). Among eyes with DME, the epiretinal membrane (ERM) was present in 7 eyes (8.24%).

Conclusions

For DR patients with ESKD who have undergone long-term HD, the choroidal thickness still changes significantly before and after single HD session, which may be related to short-term effects such as reduced blood volume and plasma osmotic pressure caused by single HD session. Although macular features seem to have stabilized in DR patients undergoing long-term dialysis, the DR of patients with ESKD should still be given attention.

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Introduction

Diabetes can cause chronic microvascular complications such as diabetic retinopathy (DR) and diabetic nephropathy (DN). DR is one of the main causes of blindness in the working population. DN may lead to proteinuria, systemic edema, hypertension, and life-threatening end-stage kidney disease (ESKD) [1]. Since the pathogenesis of DR and DN is similar, both are affected by hyperglycemia, genetic factors, advanced glycation end products (AGEs), polyol pathways, cytokines, and immune inflammation. DR and DN often occur at the same time, and DN may also affect the progression and prognosis of DR [2, 3]. Studies have confirmed that changes in the glomerular basement membrane and increased permeability caused by DN, followed by proteinuria, hypo-proteinaemia, and renal failure, can also lead to increased retinal microvascular permeability and subsequently exacerbate diabetes macular edema (DME) [2,3,4].

Hemodialysis (HD) is the most common form of kidney replacement therapy for removing metabolic waste and excess water from the body, improving renal function and prolonging the survival time of patients with ESKD [5]. DME in ESKD patients who are unresponsive or have a poor response to anti-vascular endothelial growth factor (VEGF) therapy can also be significantly improved after HD, which may filter out excess water in the blood, increase plasma protein concentration, and increase plasma osmotic pressure, leading to a decrease in central retinal thickness (CRT) [5, 6].

Choroid morphology and the vascular system can also change due to diabetes [7]. However, it is still controversial whether diabetes leads to an increase or decrease in choroidal thickness. Temel et al. [8] conducted research using the enhanced depth imaging (EDI) mode of spectral-domain optical coherence tomography (SD-OCT) and showed that choroidal thickness in non-proliferative DR (NPDR) patients and diabetes patients was reduced compared with that in normal controls. Xu et al. [9] evaluated the effect of diabetes on choroidal thickness using SD-OCT and showed that the choroidal thickness of diabetic patients and DR patients was greater than that of normal controls, but the severity of DR was not related to choroidal thickness.

There are significant anatomical differences between the retina and choroid, as well as differences in the blood flow regulatory mechanisms of the retina and choroid. Retinal blood flow does not rely on sympathetic nerve activation and remains constant, and retinal blood flow adapts to fluctuations in intraocular pressure and arterial pressure through its own regulatory mechanisms [10]. The choroid is mainly composed of blood vessels, and its thickness often varies greatly due to the filling state of vessels. Blood flow in the choroid is mainly regulated by the autonomic nervous system [11, 13]. Therefore, choroidal thickness is more susceptible to the influence of intraocular pressure, systemic blood pressure, and endogenous catecholamines [12, 13], and the impact of HD on choroidal and retinal thickness should differ.

However, studies have revealed that HD may lead to a short-term reduction in choroidal thickness [14]. There is relatively little research on the effects of long-term HD on choroidal thickness and DME. In this study, we used swept-source optical coherence tomography angiography (SS-OCTA), which can provide a greater imaging speed and increased depth scan range than SD-OCT [15]. SS-OCTA is beneficial for elucidating the impact of HD on the prognosis of DME and DR patients and the immediate effect of single HD session on retinal and choroidal thickness in ESKD patients who have received long-term HD.

Patients and methods

This study was approved by the Ethics Committee of Xi’an No.3 The hospital and the research process complied with the Helsinki Declaration. The subjects were DR patients with ESKD induced by DN who were undergoing HD at Xi’an No.3 Hospital from January 2023 to March 2024. All patients provided signed informed consent before being enrolled in this study. All participants were imaged using a 400-kHz SS-OCTA instrument (TowardPi BMizar; TowardPi Medical Technology, Beijing, China) with 400,000 scans per second. It utilizes a swept-source verticalcavity surface-emitting laser (VCSEL) with a wavelength of 1060 nm, providing a transverse resolution of 10 μm and in-depth resolution (optical) of 3.8 μm in tissue. Each OCT volume was 2560 pixels deep × 1536 pixels wide × 1280 B-scans which corresponded to nominal physical dimensions of 6 mm deep × 24 mm wide × 20 mm. The 24 × 20-mm rectangle scans, corresponding to a 120° angular field of view.

The inclusion criterion for patients who were previously diagnosed with DR and who were undergoing regular HD sessions for ESKD three times a week for approximately 4h at least 6 months. The exclusion criterion was as follows: (1) Any eye received an intravitreal injection of anti-VEGF drugs within 6 months. (2) Any eye received intravitreal or Tenon subcapsular injections of glucocorticoids within 6 months. (3) Any eye received retinal laser photocoagulation within 6 months. (4) The presence of media opacities of any eye due to cataracts or corneal disease, vitreous hemorrhage affects the quality of SS-OCT images. According to the exclusion criteria of this study, 18 patients were excluded because of vitreous hemorrhage and cataract clouding that affected the image quality, and 12 patients were excluded because of the vitreous cavity injection of anti-VEGF or steroids within 6 months.

A total of 85 eyes of 44 patients with ESKD were enrolled in this study. All patients had a long history of diabetes with severe non-proliferative diabetic retinopathy (NPDR) or proliferative diabetic retinopathy (PDR). We checked the medical records of these patients in ophthalmology through Computer-based Patient Record System, the diagnosis of DME in 32 patients (57 eyes, 67.06%) prior to HD was confirmed. Forty patients (77 eyes) received retinal laser photocoagulation, and 4 patients (8 eyes) had never received standardized ophthalmic treatment.

All patients underwent a complete ophthalmic examination, including ETDRS (early treatment diabetic retinopathy study), best corrected visual acuity (BCVA), intraocular pressure, anterior segment examination using slit-lamp biomicroscopy, fundus examination using slit lamp lenses, and OCTA within 30 min before and after single HD session, as well as within 30 min before the next single HD session.

In addition, the patient’s body weight was measured, and arterial line blood samples for biochemical parameters were collected within 30 min before and after single HD session. Complete blood counts and plasma sodium, blood potassium, blood urea nitrogen (BUN), blood glucose, and hemoglobin A1 (HbA1c) levels were measured by a fully automatic biochemical analyzer (HITACHI 7600, Tokyo, Japan).

The plasma osmotic pressure and average arterial pressure were calculated. The formula for calculating plasma osmotic pressure was 2× (blood sodium + blood potassium) (mmol/L) + blood glucose (mmol/L) + urea nitrogen (mmol/L). The formula for calculating average arterial pressure was diastolic pressure + 1/3 (systolic diastolic pressure).

The OCT images were acquired through a dilated pupil by two experienced ophthalmologists. OCT was performed using an SS-OCTA (TowardPi BM-400 K BMizar, Beijing, China). The scanning protocol used was as follows: fundus blood flow examination mode, scanning range: 24 mm × 20 mm, scanning depth: 6 mm, and scanning frequency: 40,0000 times/second. We used built-in software to automatically measure central retinal thickness (CRT), central retinal volume (CRV) (Fig. 1A), subfoveal choroidal thickness (SFCT) and subfoveal choroidal volume (SFCV) (Fig. 1B). If the retinal or choroidal boundary provided by SS-OCT automatically does not match the actual tissue layer, two ophthalmologists will manually select the retinal or choroidal boundary on cross-sectional images and measure it separately.

Fig. 1
figure 1

Representative cross-sectional SS-OCT images of patients with ESKD and DR. A 52-year-old woman with bilateral DR and DME underwent intravitreal anti-VEGF injections of aflibercept 7 times at 1-month intervals 2 years prior. Because of her ESKD, the patient denied subsequent treatment with anti-VEGF therapy and subsequently received HD. Currently, the patient has been undergoing HD for two years, and SS-OCT shows that the DME in both eyes has completely improved. (A) On the SS-OCT image of the right eye (acquired 30 min before single HD session), the retina is located between the red lines (corresponding to the inner boundary membrane and RPE, respectively). (B) On the SS-OCT image of the right eye (acquired 30 min before single HD session), the choroid is located between the red lines (corresponding to Bruch’s membrane and the scleral inner boundary, respectively)

SS-OCT, swept-source optical coherence tomography; ESKD, end-stage kidney disease; DR, diabetic retinopathy; DME, diabetic macular edema; VEGF, vascular endothelial growth factor; RPE, retinal pigment epithelium; HD, hemodialysis

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En face images of the superficial capillary plexus (SCP) and the deep capillary plexus (DCP) were automatically visualized through the segmentation of two distinct slabs, defined by the arbitrary segmentation lines created by the device software. The SCP is defined as the layer originating from the internal limiting membrane to the inner plexiform layer. The DCP is defined as the layer that starts from the outer border of the inner plexiform layer and extends to the outer border of the outer plexiform layer. Subsequently, two graders manually outlined the FAZ on en face image of SCP, and measured its area using the inbuilt program that designed for outlined area measurements. An average value of the two measurements was utilized for analysis.

Macular edema was defined as a CRT > 250 μm or an accumulation of intra- or subretinal fluid in the macular region on SS-OCT images.

Statistical methods

All the data are expressed as the means ± SEMs. SPSS version 22.0 software (IBM Corp., Armonk, NY, USA) was used to perform the statistical analysis. Differences in parameters before and after single HD session or before and before the next single HD session were evaluated by using paired t tests. P < 0.05 was considered to indicate statistical significance.

Results

The characteristics of the patients (gender, age, diabetes history, HD history, and glycosylated hemoglobin level) are shown in Table 1.

Table 1 Patient characteristics
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The changes in average intraocular pressure, ETDRS BCVA, body weight, average arterial pressure, and plasma osmotic pressure before and after single HD session are shown in Table 2. The average weight of patients after single HD session decreased by 2.59 ± 0.80 kg (P < 0.001), and the average IOP decreased by 0.07 ± 0.63 mmHg (P = 0.282). There was no statistically significant difference in average arterial pressure before and after single HD session (P = 0.298), while the average plasma osmotic pressure after single HD session decreased by 13.17 ± 16.60 mOsm/kg (P < 0.001).

Table 2 Changes in the clinical parameters of patients before and after single HD session
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Table 3 shows the average CRT, CRV, SFCT and SFCV in patients measured within 30 min before and after single HD session. The average CRT and CRV did not change significantly after single HD session (P = 0.286, 0.324). The average SFCT decreased significantly from 243.11 ± 77.15 μm to 219.20 ± 72.84 μm, with an average reduction of 23.91 ± 14.15 μm (P < 0.001), and the average SFCV decreased significantly from 0.15 ± 0.10 mm3 to 0.13 ± 0.90 mm3, with an average reduction of 0.28 ± 0.23 mm3 (P < 0.001) after single HD session (Fig. 2). CRV is the retinal volume within 1000 μm of the macular central sulcus diameter. SFCV is the choroidal volume within 1000 μm of the macular central sulcus diameter.

Table 3 Comparison of CRT, CRV, SFCT and SFCV before and after single HD session
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Fig. 2
figure 2

Representative central retinal thickness and central choroidal thickness maps of patient with ESKD and DR before and after single HD session. A 47-year-old man with bilateral DR and DME underwent panretinal photocoagulation 3 years prior. Because of his ESKD, the patient received HD since then. (A) Thirty minutes before single HD session, the central retinal thickness was 227 μm on retinal thickness map (top left), the central choroidal thickness was 105 μm on choroidal thickness map (top right). On cross-sectional SS-OCT images, the retina is located between the green lines corresponding to the inner boundary membrane and RPE (bottom left), the choroid is located between the green lines, corresponding to Bruch’s membrane and the scleral inner boundary (bottom right). (B) Thirty minutes after single HD session, the central retinal thickness was 224 μm on retinal thickness map, the central choroidal thickness was 90 μm on choroidal thickness map

HD, hemodialysis; ESKD, end-stage kidney disease; DR, diabetic retinopathy; DME, diabetic macular edema; SS-OCT, swept-source optical coherence tomography; RPE, retinal pigment epithelium

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On en face OCTA images with a scanning range of 24 mm x 20 mm, eighty-five (100%) eyes showed nonperfusion areas of retinal capillaries, and abnormal retinal microvasculature (Fig. 3A). On en face OCTA images with a VRI slab and cross-sectional OCTA images, retinal flow signals projecting through the internal limiting membrane (ILM) into the vitreous cavity (RNV) were confirmed in 42 (49.41%) eyes (Fig. 3C and D), and retinal flow signals remaining under the ILM and showing no breach in the ILM (IRMA) were confirmed in all (100%) eyes (Fig. 3E and F).

Fig. 3
figure 3

Representative OCTA images of patients with ESKD and DR acquired 30 min before HD in the same patient described in Fig. 1. (A) En face OCTA image with full-thickness retinal circulation of the right eye indicating regions of nonperfusion, disintegrity of foveal capillary network, retinal neovascularization (RNV) or intraretinal microvascular abnormalities (IRMA). (B) Image of retinal vessel density illustrating regions of nonperfusion (labeled blue). (C, D) RNV is recognizable as a vascular network on en face OCTA image with a VRI slab (white arrow), corresponding to blood flow signals penetrating the internal limiting membrane and posterior hyaloid region (white arrow) on cross-sectional OCTA. (E, F) En face OCTA image of the deep capillary plexus showing the IRMA as a tortuous shunt vessel, corresponding to blood flow signals under the ILM (white arrow) on cross-sectional OCTA

OCTA, optical coherence tomography angiography; ESKD, end-stage kidney disease; DR, diabetic retinopathy; HD, hemodialysis; FAZ, foveal avascular zone; RNV, retinal neovascularization; IRMA, intraretinal microvascular abnormalities; VRI, vitreoretinal interface; ILM, internal limiting membrane

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Eleven (17 eyes, 20%) of 44 patients (85 eyes) treated with long-term HD for ESKD still had DME, and 7 (41.18%) of these 17 eyes had ERM before single HD session (Fig. 4). After a single HD session, DME still existed in these 17 eyes of 11 patients.

Fig. 4
figure 4

SS-OCT images of patients with ESKD, CME, DR and ERM. A 56-year-old woman with bilateral DR and DME underwent intravitreal anti-VEGF injections of aflibercept 14 times at 1-month intervals 3 years prior. Because of her ESKD, she stopped subsequent treatment with anti-VEGF therapy and subsequently received HD. (A) En face OCT image at the level of the deep retinal plexus showing numerous hypo-reflective cystoid spaces in the macular area of the right eye (acquired 30 min before HD). (B) A cross-sectional OCT image revealing a unified ERM overlying the CME

SS-OCT: swept-source optical coherence tomography; ESKD, end-stage kidney disease; CME: cystoid macular edema; ERM: epiretinal membrane; DR: diabetic retinopathy; DME: diabetic macular edema; HD, hemodialysis; VEGF: vascular endothelial growth factor; HD, hemodialysis

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There was no statistically significant difference in the average CRT (P = 0.206), CRV (P = 0.154), SFCT (P = 0.108) or SFCV (P = 0.174) before single HD session or before the next single HD session (Table 4).

Table 4 Comparison of CRT, CRV, SFCT and SFCV before single HD session and before the next single HD session
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All eyes (100%) enrolled in this study presented with disintegrity of capillary network around FAZ, resulting in an enlarged FAZ, the average FAZ area was 0.51 ± 0.11mm2.

Discussion

In this study, a total of 85 eyes of 44 patients with ESKD were enrolled, the mean HD history for these patients was 59.95 months. Based on previous medical records, the diagnosis of DME in 32 patients (57 eyes, 67.06%) prior to HD was confirmed. Of the 44 patients (85 eyes) who received long-term HD treatment for ESKD, only 11 (17 eyes, 20%) still had DME, and 7 (8.24%) of these 17 eyes had ERM. Eighty-five (100%) eyes had abnormal circulation in the retina, such as capillary nonperfusion, microaneurysm and IRMA, which indicated that the condition of DR in these patients was still serious, although 12 of them had received intravitreal anti-VEGF drug injection, and 2 had received intravitreal dexamethasone implant injection. However, the patients enrolled in this study did not receive any form of anti-VEGF or glucocorticoid treatment within the past 6 months, and the lower incidence of DME in this study may be related to long-term HD. Hwang et al. [16] evaluated the effect of HD on CRT and SFCT in a study including 15 DME patients with DN and reported that the average CRT decreased from 317.92 ± 91.41 μm to 287.77 ± 57.55 μm after the first HD and that the SFCT decreased from 313.31 ± 85.89 μm to 288.81 ± 92.02 μm after the first HD session.

The onset and progression of DME are not only related to ocular factors such as VEGF overexpression caused by retinal ischemia, retinal capillary hyperpermeability, and decreased retinal pigment epithelial (RPE) pump function, but also to the hypoproteinaemia caused by DN [17,18,19]. Since both DR and DN are chronic vascular diseases, the severity of DR correlates with the condition of DN, and DR can be used as a marker to predict the severity of DN [20, 21]. Intensive glycemic control is not only essential for preventing the occurrence and progression of DR and DME but also important for reducing the risk of DN progression [21].

For patients with ESKD, HD remains the most common treatment modality for improving quality of life and prolonging survival, even if severe DR remains [6]. In this study, the 44 patients no longer received ophthalmic treatment for DR. In department of HD, patients get HD three times a week in sessions of 3 to 5 h each. Therefore, year-round HD is the major part of their lives.

Epidemiological research shown that the incidence of DME in diabetes patients is approximately 5.5% [22], which reaches 21.1% in DR patients [23], as high as 66.2% in patients with PDR [24]. Since the condition of DN is positively correlated with the severity of DME and DR [25], theoretically, the incidence of DME is greater in patients with DN and PDR.

In this study, we found that the incidence of DME in patients undergoing HD was only 20%. After single HD session, the patients’ average plasma osmolality decreased by 13.17 ± 16.60 mOsm/kg (P < 0.001), and the average body weight decreased by 2.59 ± 0.80 kg (P < 0.001). Both the volume and composition of extracellular fluid decreased dramatically, leading to a decrease in body weight and plasma osmolality after single HD session [26], which may be related to the low incidence of DME in ESKD patients undergoing HD.

Among the 44 patients (85 eyes) enrolled in this study, 17 (20%) had DME, and all had CME. Among them, ERM was present in 7 eyes with DME (8.24%). The lack of regression of these CMEs after long-term HD may be related to the presence of advanced glycation end products (AGEs). Methylglyoxal (MGO) derived from AGEs may induce alterations in the characteristics of cystoid lesion components in diabetic CME due to posttranscriptional modification, leading to resistance of fibrin in CME to plasmin [27, 28].

ERM is a pathology caused by fibrocellular proliferation on the ILM followed by intravitreal injections for DME treatment or secondary to a wide variety of diseases, such as DN and cataract surgery [29, 30]. ERM formation causes anteroposterior and tangential forces in the retina, resulting in further damage to the blood retina barrier (BRB), the release of inflammatory factors and the deterioration of DME [29]. Clinical studies have revealed that vitrectomy has a beneficial effect on the management of DME with ERM [31].

Fang et al. [32] conducted a two-year study on 108 patients with DME who received intravitreal injections of anti-VEGF drugs to estimate changes in the glomerular filtration rate (eGFR), confirming that although DME can improve with anti-VEGF intervention, the eFGR continues to deteriorate.

Therefore, ophthalmologists should pay close attention to the renal function of patients while using anti-VEGF drugs or corticosteroid intravitreal injections to treat DME in clinical practice. If renal dysfunction meets the HD treatment standard, patients should be promptly referred to nephrologists. For DME patients who are unresponsive or have a poor response to anti-VEGF or glucocorticoid therapy, it is necessary to evaluate renal function as early as possible. Improving renal function may be more conducive to improving DME in patients with ESKD.

To clarify the impact of single HD session on retina and choroid, we used SS-OCTA to analyze the CRT, CRV, SFCT and SFCV in patients before and after single HD session. We found that there was no significant change in the average CRT or CRV before and after single HD session, while the average SFCT decreased significantly from 243.11 ± 77.15 μm to 219.20 ± 72.84 μm, with an average reduction of 23.91 ± 14.15 μm (P < 0.001), and the average SFCV decreased significantly from 0.15 ± 0.10 mm3 to 0.13 ± 0.90 mm3, with an average reduction of 0.28 ± 0.23 mm3 (P < 0.001), after single HD session. Before the next single HD session, the average SFCT recovered to 245.41 ± 76.23 μm, and the SFCV recovered to 0.16 ± 0.10 mm3. There was no statistically significant difference in the CRT (P = 0.206), CRV (P = 0.154), SFCT (P = 0.108) or SFCV (P = 0.174) before the two single HD sessions.

This finding may be related to the fact that the choroid is mainly composed of blood vessels, and HD leads to the elimination of water and small molecule metabolic waste, such as BUN and creatinine, in the patient’s body. The blood volume in the systemic circulation, including the choroidal vascular system, decreases in a short period of time [33].

In this study, we also observed that within 30 min after single HD session, the average weight of patients decreased by 2.59 ± 0.80 kg (P < 0.001), and the average IOP decreased by 0.07 ± 0.63 mmHg (P = 0.282). However, the renal function of patients with ESKD tends to fail, and the water and metabolic waste discharged previously can gradually accumulate again after HD. Therefore, the SFCT and SFCV of patients in this study increased again before the next single HD session.

However, the retinal thickness did not change due to single HD session, which may be related to the fact that the patients in this study had already undergone long-term HD. Subsequently, long-term HD led to the stabilization of the macular anatomical structure of the retina. Moreover, retinal blood vessels run between the nerve fiber layer and the inner nuclear layer, while the layers outside the inner nuclear layer in the retina are avascular [34]. Even if single HD session leads to a decrease in blood volume throughout the body, including in the retinal vascular plexus, its impact on retinal thickness is difficult to detect.

Although all the patients in this study have undergone long-term HD, whose renal function is relatively stable, and DME has significantly improved, it cannot be denied that all patients still had severe DR, including the presence of nonperfused capillaries in the retina, foveal avascular zone (FAZ) enlargement, and IRMA in 85 (100%) eyes. RNV was still observed in 42 (49.41%) eyes. The average FAZ area was 0.51 ± 0.11mm2 in our study. Shahlaee et al. [35] found that the FAZ area of the superficial layer in normal adults was 0.27 ± 0.101 mm2, as measured by OCTA. FAZ surrounded by capillary network, a case control study confirmed that patients with diabetes had a larger FAZ, and patients with more severely damaged retinas had a much larger FAZ [36].

Fundus fluorescence angiography (FFA) could not be performed in ESKD patients in this study because sodium fluorescein may lead to contrast-induced nephropathy (CIN) and appears to be a possible risk factor for the progression of ESRD [37]. Stino et al. [38] demonstrated that wide-field OCTA imaging is highly reliable in the detection of PDR, and has the potential to replace FFA as a single diagnostic tool.

The basis for distinguishing IRMA and RNV was to observe the location of blood flow signals on cross-sectional OCTA images. The blood flow signal of the IRMA is located below the ILM, and if the blood flow signal protrudes from the ILM and enters the vitreous cavity, it is considered a RNV [39, 40].

These RNVs still pose a risk of causing vitreous hemorrhage and traction retinal detachment [41]. However, the impact of ESKD on quality of life and survival time may make these patients more inclined to receive frequent HD rather than ophthalmic treatment. Therefore, ESKD patients with DR still need to be examined and/or treated by an ophthalmologist in a timely manner in order to permanently preserve their limited vision.

Other studies have also confirmed that long-term hemodialysis can effectively improve CRT and visual acuity in patients with DME [5, 6]. However, our study focused on the retinal status of DR patients on long-term HD (mean 59.95 months), and analyzed the retinal and choroidal thickness before and after single HD session. Our study may provide an available reference for the follow-up and treatment of DR patients undergoing HD.

The main limitation of this study was its small sample size. Further large-scale prospective studies are needed to further clarify the impact of long-term HD on the retina, choroid and optic nerve.

Conclusion

HD can not only effectively improve the renal function of diabetes patients with ESKD but also promote the stability of DR in such patients. For patients who have received long-term HD, their choroidal thickness still changes significantly before and after single HD session, which may be related to short-term effects such as a reduction in blood volume and plasma osmolality caused by HD, but the CRT or CRV does not significantly change. The DR of patients with ESKD still needs to be considered by ophthalmologists and treated in a timely manner.

Data availability

No datasets were generated or analysed during the current study.

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  1. Ke He and Suijun Liu are co-first authors.

Authors and Affiliations

  1. Department of Ophthalmology, Xi’an No. 3 Hospital, the Affiliated Hospital of Northwest University, Xi’an, 710018, China

    Ke He, Peng Zhang, Lian Chen, Bozhao Wang & Juan Zhang

  2. Department of Hemodialysis, Xi’an No. 3 Hospital, the Affiliated Hospital of Northwest University, Xi’an, 710018, China

    Suijun Liu & Jingbo Shi

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Contributions

Z.P., H.K., and L.S. wrote the paper and acquired the clinical data. S.J., C.L. and Z.J. reviewed the paper and interpreted the clinical data. Z.P. and W.B. performed the clinical revision and supervised the data interpretation. All authors have read and approved the final manuscript.

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Correspondence to Peng Zhang.

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This case study was conducted in accordance with the tenets of the Declaration of Helsinki. and approved by the Ethics Committee of Xi’an No.3 Hospital, the Affiliated Hospital of Northwest University (approval number: SYLL-2023-182). Written informed consent was obtained from the patients.

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He, K., Liu, S., Shi, J. et al. The effect of long-term hemodialysis on diabetic retinopathy observed by swept-source optical coherence tomography angiography. BMC Ophthalmol 24, 334 (2024). https://doi.org/10.1186/s12886-024-03612-5

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BMC Ophthalmology

ISSN: 1471-2415

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