Evaluation of the efficacy and safety of preoperative intravitreal triamcinolone acetonide combined with internal limiting membrane peeling for the treatment of idiopathic macular epiretinal membrane

doi:10.21203/rs.3.rs-3430303/v1

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Research Article

Evaluation of the efficacy and safety of preoperative intravitreal triamcinolone acetonide combined with internal limiting membrane peeling for the treatment of idiopathic macular epiretinal membrane

https://doi.org/10.21203/rs.3.rs-3430303/v1

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Purpose

To assess the efficacy and safety of preoperative intravitreal triamcinolone acetonide (IVTA) combined with internal limiting membrane (ILM) peeling for idiopathic epiretinal membrane (IMEM).

Methods

This was a retrospective study. Thirty-six phakic eyes of 35 patients were included in this study. IVTA was administered to 18 patients (18 eyes, Group IVTA) 7 days before vitrectomy, while the other 17 patients (18 eyes, Group no-IVTA) only underwent vitrectomy and ILM peeling. Patients were followed up for at least 6 months. Data on best-corrected visual acuity (BCVA), intraocular pressure (IOP), central macular thickness (CMT), inner retinal thickness (IRT), vascular parameters (measured by optical coherence tomography angiography, OCTA), mean macular sensitivity (MMS), 63% bivariate contour ellipse area (BCEA) and P1 (measured by macular integrity assessment, MAIA) were collected.

Results

There were significant differences in BCVA and IRT between the IVTA group and the no-IVTA group at 6 months after surgery (P = 0.000 and P = 0.010). The CMT and MMS of the two groups significantly changed from the preoperative values; however, there were no differences between the 2 groups during the entire study period (P = 0.242 and P = 0.849). The changes in vascular parameters, including foveal avascular zone (FAZ) area and vessel densities of superficial and deep capillary plexus (SCP VD and DCP VD), in the two groups were not statistically significant. There were no statistically significant differences in 63% BCEA and P1 either.

Conclusion

Macular morphology and macular integrity improved after vitrectomy combined with ILM peeling surgery. Compared with the no-IVTA group, preoperative intravitreal triamcinolone acetonide can improve best corrected visual acuity and accelerate the absorption of intraretinal fluid in terms of a significant reduction in IRT.

Macular edema

Vitrectomy

Epiretinal membrane

Triamcinolone acetonide

Intravitreal injection

Idiopathic macular epiretinal membrane (IMEM) is a common disease without an associated specific cause. The incidence rate in the population is approximately 4–12.8%, and it is more common in the elderly^[1]. The avascular membrane can distort the retina and blood vessels of the macular area, causing deteriorating central vision, visual distortion and monocular diplopia^[2]. Currently, medication therapy is still not sufficiently effective for IMEM. Microincision vitrectomy combined with internal limiting membrane peeling surgery has been proven to be the most efficient approach to improve best corrected visual acuity (BCVA) and to reduce recurrence of IMEM^{[3, 4]}.

Prognostic factors of postoperative visual acuity improvement have been identified, including patient age, preoperative visual acuity, central macular thickness (CMT)^[5], length of the ellipsoid zone defect^[6] and inner retinal irregularity index^[7]. Among them, residual macular edema (ME) limits the complete recovery of retinal structure and visual function^[8]. Previous studies have suggested that inflammatory factors and peeling surgical traction might be the pathological mechanism of ME^[9].

Steroid intravitreal injection, instead of waiting for edema to disappear spontaneously, has been proven useful in facilitating morphological structure restoration and improvement of visual acuity^[10]. Steroid drugs, such as triamcinolone acetonide (TA), are considered to accelerate the absorption of intraretinal edema by inhibiting vascular endothelial growth factor (VEGF) synthesis and the inflammation caused by TNF-α and IL-1β^[11]. Ueno et al.^[12] demonstrated that intravitreal triamcinolone acetonide (IVTA) can facilitate excision of the internal limiting membrane (ILM) and improve the visibility of IMEM. However, most studies have focused on the effects of postoperative IVTA, but very few studies have discussed the possibility of preoperative IVTA. In fact, inflammation and vasoactive cytokines are closely associated with the formation of ME in the macular epiretinal membrane^[13], and membrane peeling leads to retinal disruption and perturbs outer retina function. Preoperative steroid injections are applied to eliminate macular edema, perhaps to reduce mechanical damage produced by surgery. Based on the above situations, we assume that preoperative IVTA might be helpful in the treatment of IMEM. The objective of this study was to investigate the safety of preoperative IVTA and to evaluate the efficacy of anatomic and functional recovery after pars plana vitrectomy (PPV) and ILM peeling with or without preoperative IVTA by analyzing the changes in parameters measured by optical coherence tomographic angiography (OCTA) and macular integrity assessment (MAIA).

Patients

Patients who underwent 25-G PPV combined with IMEM and ILM peeling were compared to those who additionally received IVTA before PPV. Follow-up time can be expanded within 7 days before or after the expected timepoint. Thirty-five patients were collected in two groups: one received conjunct IVTA before surgery (IVTA group, 18 patients), whereas the other did not (no-IVTA group, 17 patients).

Thirty-six phakic eyes of 35 patients who were diagnosed with IMEM between November 2019 and December 2020 at Tianjin Eye Hospital were included. More specifically, only patients diagnosed with IMEM documented by optical coherence tomography (OCT) or optical coherence tomographic angiography (OCTA) and their BCVA ≥ 0.4 logMAR or ≥ 0.2 logMAR but with severe metamorphopsia were included in the study.

The exclusion criteria were secondary epiretinal membranes, preexisting macular disease such as lamellar or full-thickness macular holes, age-related macular degeneration or diabetic macular edema, and any other diseases that could impact visual function such as pathologic myopia, glaucoma and uveitis. Patients who had a history of intraocular surgery, ocular trauma or systemic steroid or immunosuppressant use for immune disease were also excluded.

Surgical procedure

The injections of IVTA group patients were performed aseptically by the same physician in a standard operating room. After 3 rounds of surface anesthesia with proparacaine hydrochloride eye drops, a nurse used 5% povidone-iodine to disinfect the surgical field and flush the conjunctiva sac. A total of 0.05 ml of TA was injected (40 mg/mL, Ji da Pharmaceutical, Kunming, China), and the volume was increased to 1 ml with balanced salt solution. After inverting for 15 minutes, the supernatant was removed, and the excipients and preservatives were removed. Injection of TA 0.05 ml (2 mg) was performed 3.5 to 4.0 mm posterior to the limbus with a 30-G needle. Vitrectomy and phacoemulsification were performed 7 days after IVTA.

All vitreous surgeries were performed by the same experienced ophthalmologist (H. QH.). Preoperatively, levofloxacin eye drops were applied 4 times per day for at least 3 days. A 25-G PPV was performed using the Constellation Vision System (Alcon Laboratories, Inc., California, USA) under retrobulbar block. After phacoemulsification, core vitrectomy and posterior vitreous detachment, the internal limiting membrane within the vascular arcade was peeled with the help of indocyanine green (5 mg/mL). At the end of the procedure, implantation of the intraocular lens, intraoperative posterior capsulotomy and air-fluid exchange were performed.

Clinical characteristics collections

The data were collected at baseline and 1 month and 6 months after vitrectomy surgery. The BCVA was assessed using Snellen notation and was converted to the logarithm of the minimum angle of resolution (logMAR) for statistical analysis. Intraocular pressure (IOP) was measured by noncontact tonometers (Canon TX-20P, Canon Inc., Tokyo, Japan). Central macular thickness (CMT), inner retinal thickness (IRT), foveal avascular zone area (FAZ), and vessel densities of superficial and deep capillary plexus (SCP VD and DCP VD) were evaluated by a specific OCTA instrument (RTVue-XR 100-2, OptoVue, Fremont, CA, USA). Scans covered a 3 mm × 3 mm central square region of the fovea, and FAZ, SCP VD and DCP VD were detected automatically by using the built-in software.

Mean macular sensitivity (MMS), fixation stability and the site of fixation were measured to assess macular function by using macular integrity assessment (MAIA, Centervue, Padova, Italy). Prior to the examination, patients underwent 10 minutes of dark adaptation in a dark room. All measurements were performed without any pupil dilation^[14]. The MAIA was conducted for both eyes using a grid of 37 stimuli covering the central 10° of the macula. The MAIA measurement is performed by a 4 − 2 strategy with a Goldmann III stimulus size. The background luminance was 4 asb, the maximum luminance was 1,000 asb and the minimum was 0.25 asb. The stimulus dynamic range of the device was 0 to 36 dB^[15]. We use a bivariate contour ellipse area (BCEA) containing 63% of fixations and P1, which represents the fixation rate in the 2° circle, as the indicators of fixation stability.

Statistical analysis.

All statistical analyses were performed using SPSS statistics software (version 26.0; SPSS Inc., Chicago, IL, USA). Descriptive statistics are presented as the mean value (standard deviation) as described in the legend of the figures and tables. Baseline data were compared among the groups using t test, chi-square analysis, and Mann‒Whitney U test. The time course of statistical changes in the value of macular anatomical structure and visual acuity parameters was evaluated by two-way repeated-measures ANOVA, and p-values < 0.05 were considered statistically significant.

A total of 36 phakic eyes of 35 patients (10 men; 25 women) were included in the study (18 in the preoperative IVTA group and 17 in the no-IVTA group). Basic patient clinical characteristics and demography are demonstrated in Table 1. There were no differences in age, sex, IOP or parameters measured by MAIA. The significant difference in IRT (P = 0.020) and BCVA (P = 0.027) at baseline between groups showed that inherent treatment bias from ophthalmologists is inevitable in a retrospective analysis.

Table 1

Preoperative Baseline Clinical Characteristics and Demographics for Each Group of Patients.
	IVTA	no-IVTA	p-value
Age(yr)	65.56(7.84)	65.29(7.70)	0.921
BCVA(logMAR)	0.14(0.10)	0.46(0.52)	0.027
IOP(mmHg)	14.35(2.52)	13.18(2.37)	0.159
CMT(mm)	533.9(95.12)	508.4(93.49)	0.429
IRT(mm)	174.5(72.71)	125.0(45.99)	0.020
FAZ(mm²)	0.098(0.065)	0.122(0.102)	0.410
SCP VD (%)	41.12 (10.07)	39.31 (8.99)	0.581
DCP VD (%)	41.32(8.74)	37.66(6.86)	0.180
MMS (dB)	22.07(2.03)	22.93(2.45)	0.259
P1 (%)	87.77(13.34)	90.17(9.01)	0.578
P2 (%)	98.09(2.30)	97.6(3.15)	0.863
63% BCEA (°²)	1.32(0.92)	1.27(0.99)	0.725
Gender(male/female)	6(0.33)/12(0.67)	4(0.22)/14(0.78)	0.711
Laterality (OD/OS)	8(0.44)/10(0.56)	10(0.56)/(0.44)	0.740

Data are presented as mean (standard deviation). BCVA = best corrected visual acuity; IOP = intraocular pressure; CMT = central macular thickness; IRT = inner retinal thickness; FAZ = foveal avascular zone area; SCP VD = vessel densities of superficial capillary plexus; DCP VD = vessel densities of deep capillary plexus; MMS = mean macular sensitivity; BCEA = bivariate contour ellipse area.

1. BCVA and IOP

To reduce the impact of the baseline difference, we used the difference value (D-value) to calculate statistics for BCVA and IRT. The BCVA and IOP at baseline, 1 month and 6 months postoperatively are shown in Table 2. There were no significant differences in IOP. The difference in BCVA in the IVTA group was significant at 1 month and 6 months (P = 0.000 and P = 0.000) after surgery. There was a significant difference in BCVA (D-value) between the IVTA group and the no-IVTA group at 6 months after surgery (P = 0.000) (shown in Fig. 1).

Table 2

Comparison of BCVA and IOP between the preoperative and one-month and six-month postoperative visits.
Group	Time	BCVA (Log MAR) (D-value)	IOP(mmHg)
IVTA	Preoperative	0.00(0.00)	14.35(2.52)
	1 month	0.53(0.27)*	14.02(6.99)
	6 month	0.71 (0.29)*	14.06(5.75)
no-IVTA	Preoperative	0.00(0.00)	13.18(2.37)
	1 month	0.12(0.33)	13.83(2.75)
	6 month	0.14 (0.41)	12.87(3.14)
p-value	Column Factor	0.000	0.256
	Time	0.000	0.908
	Time x Column Factor	0.000	0.824

The results of continuous parameters between the two groups using two-way repeated ANOVA. *Indicates a statistically significant difference compared with the preoperative value.

Figure 1. Comparison of preoperative and postoperative BCVA and IOP between different groups. ¶P-value indicates the overall analysis throughout the study period by two-way repeated ANOVA. P-values are presented next to all graphs for each study period, indicating the results of statistical analyses among the 2 groups for that period using Bonferroni post hoc analysis.

2. OCTA

Table 3 and Fig. 2 present the preoperative and postoperative values of OCTA parameters, including CMT, IRT, FAZ, SCP VD and DCP VD, for the two groups. The overall IRT (D-value) was significantly lower in the IVTA group than in the no-IVTA group (P = 0.010) throughout the study period. At 1 month and 6 months postoperatively, the CMT of the two groups significantly decreased from the preoperative values. However, there were no differences between the 2 groups during the entire study period (P = 0.242). The overall change in FAZ, SCP VD and DCP VD was not significantly different between the 2 groups throughout the study period.

Table 3

Comparison of OCTA parameters between the preoperative, one-month and six-month postoperative visits.
Group	Time	CMT(mm)	IRT(mm) (D-value)	FAZ(mm2)	SCP VD(%)	DCP VD(%)
IVTA	Preoperative	533.9(95.1)	0.00(0.00)	0.098(0.064)	41.12(10.07)	41.32(8.74)
	1 month	414.7(69.2)*	75.97(67.60)*	0.100(0.332)	38.60(5.34)	40.17(2.30)
	6 month	377.7(34.5)*	83.14(73.12)*	0.114(0.062)	37.62(5.20)	43.24(4.15)
no-IVTA	Preoperative	508.4(93.5)	0.00(0.00)	0.121(0.102)	39.31(8.99)	37.66(6.86)
	1 month	429.8(74.2)*	29.76(59.96)	0.129(0.112)	36.64(8.18)	39.98(5.44)
	6 month	391.3(33.6)*	31.78(51.53)*	0.107(0.485)	36.46(6.08)	42.03(4.42)
p-value	Column Factor	0.954	0.025	0.312	0.373	0.176
	Time	0.000	0.000	0.000	0.100	0.056
	Time x Column Factor	0.242	0.010	0.354	0.962	0.372

The results of continuous parameters between the two groups using two-way repeated ANOVA. *Indicates a statistically significant difference compared with the preoperative value.

Figure 2. Comparison of preoperative and postoperative OCTA parameters between different groups. ¶P-value indicates the overall analysis throughout the study period by two-way repeated ANOVA. P-values are presented next to all graphs for each study period, indicating the results of statistical analyses among the 2 groups for that period using Bonferroni post hoc analysis.

3. MAIA

Table 4 and Fig. 3 present the preoperative and postoperative values of MAIA parameters, including MMS, P1, P2 and 63% BCEA, for the two groups. At 1 month and 6 months postoperatively, the MMS of the two groups significantly improved compared with the preoperative values. However, there were no differences between the 2 groups during the entire study period (P = 0.849). The overall change in P1, P2 and 63% BCEA was not significantly different between the 2 groups throughout the study period.

Table 4

Comparison of MAIA parameters between the preoperative and one-month and six-month postoperative visits.
Group	Time	MMS	P1	P2	63% area
IVTA	Preoperative	22.07(2.26)	87.77(13.34)	98.09(2.30)	1.32(0.92)
	1 month	23.19(1.89)*	88.80(5.94)	97.86(1.39)	1.34(0.59)
	6 month	24.15(2.64)*	88.55(10.69)	97.73(3.16)	1.33(1.01)
no-IVTA	Preoperative	22.93(2.45)	90.17(9.01)	97.60(3.15)	1.27(0.99)
	1 month	24.37(1.90)*	83.81(20.68)	96.40(5.63)	1.84(1.92)
	6 month	25.40(1.21)*	87.71(8.66)	97.45(2.43)	1.61(1.04)
p-value	Column Factor	0.055	0.722	0.394	0.461
	Time	0.000	0.484	0.470	0.229
	Time x Column Factor	0.849	0.265	0.570	0.268

The results of continuous parameters between the two groups using two-way repeated ANOVA. *Indicates a statistically significant difference compared with the preoperative value.

Figure 3. Comparison of preoperative and postoperative MAIA parameters between different groups. ¶P-value indicates the overall analysis throughout the study period by two-way repeated ANOVA.

Idiopathic macular epiretinal membrane is a macular pathology of the vitreoretinal interface that causes vision impairment and metamorphopsia in elderly individuals. Currently, numerous studies have concluded that vitrectomy combined with ILM peeling is very useful for recovering visual acuity and reducing the recurrence of IMEM^{[16, 17]}. However, residual ME is still an obstacle for complete visual function recovery in terms of decrease in CMT and improvements in BCVA and MMS. Preoperatively, cystoid macular edema, caused by the persistent attachment of vitreous and inflammation, plays the most relevant role in the decline in visual acuity^[18]. Surgical mechanical stimulation could aggravate this condition by damaging the blood‒retinal barrier and promoting extravasation of inflammatory cytokines such as prostaglandins^[8].

Given the above situation, some surgeons were encouraged to use pharmacologic treatments for persistent ME by histological studies of steroids therapies. A long-term 12-month follow-up study of intravitreal dexamethasone intraoperative implantation for the treatment of ME showed a significant reduction in CMT and improved visual acuity ^[19]. The molecular mechanisms involved in this acceleration were revealed, including inhibition of VEGF production, blocking the production of cytokines, inducing leukocyte apoptosis^[20], and stimulating endogenous adenosine signaling in Müller cells^[21].

Interestingly, cystoid macular edema in IEME is similar to that observed in ischemic retinal diseases such as diabetic retinopathy (DR). Preoperative anti-VEGF injection has been extensively used as an adjunct to prevent complications of DR surgery^[22]. Similarly, preoperative injection of TA rather than intraoperative IVTA might be a strategy for the surgical treatment of ME. The main hypotheses were as follows: (1) absorption of intraretinal liquid and microenvironment changes^[23] before surgery might be helpful to improve tolerance for surgical peeling tension and reduce postoperative anatomical damage; and (2) the anti-inflammatory effects of TA may block the secondary cellular effects triggered by surgical mechanical traction^{[17, 24]}. We observed the “crunch” of the proliferative membrane in the IVTA group, which was manifested by the limitation of the proliferative membrane and fibrosis increase simultaneously, and the surgeon was more efficient at removing tenacious fibrous hyperplasia adherent to the retina with less hemorrhage.

According to our results, compared with the no-IVTA group, the use of preoperative IVTA was statistically significant in improving BCVA and reducing IRT at 1 month and 6 months after surgery. This means that preoperative IVTA can accelerate the absorption of intraretinal fluid and speed up the recovery of visual function, while spontaneous restoration will be much slower. These results correspond to those of previous studies: Reinhard et al.^[24] investigated the results of IVTA in small-gauge vitrectomy for the treatment of residual ME, demonstrating the efficacy: additional IVTA accelerated morphological recovery in terms of diminution of CMT and improved visual acuity. The reasons why the effects of preoperative IVTA and postoperative IVTA are similar are assumed to be as follows: To reduce damage to the retina during vitrectomy, part of the basal vitreous is usually preserved during IMEM, and it will continue to release diffused TA as a “slow-release biological device” for a few days, even if drug clearance becomes faster after vitrectomy^{[25, 26]}. Limited by the retrospective nature of this research, more detailed examinations should be performed during the period before vitrectomy and after IVTA to distinguish whether edema absorption occurs postoperatively or preoperatively.

We also observed that the CMT and MMS of the two groups were substantially improved after vitrectomy combined with ILM peeling, and there was no significant difference between the two groups throughout the entire study period. There was also no significant difference in vascular parameters. The two most notable complications of intravitreal steroid injection are cataract progression and intraocular pressure elevation^[27], and none of these complications were observed in our study (mainly because vitrectomy and phacoemulsification were performed 7 days after IVTA). However, what we cannot ignore is that additional preoperative IVTA injection does increase the risk of infectious endophthalmitis, retinal detachment, globe perforation and vitreous hemorrhage^[28].

A limitation of our study is the lack of a postoperative IVTA group for an intuitive comparison, which can decisively indicate whether it is necessary to inject TA before surgery. In addition, this was a retrospective study with a relatively low number of patients and a short follow-up period. This selection bias exhibited at baseline, which was induced by the surgeon, may explain the significant differences in BCVA (D-value) and IRT (D-value). The worse initial IRT and BCVA in the IVTA group may allow a greater improvement in the difference value.

In conclusion, our observations suggest that preoperative intravitreal triamcinolone acetonide can improve best corrected visual acuity and accelerate the absorption of intraretinal fluid in terms of a significant reduction in IRT. A larger sample size and longer-term prospective randomized research may further verify the current study’s results.

BCEA bivariate contour ellipse area

BCVA best-corrected visual acuity

CMT central macular thickness

DCP deep capillary plexus

FAZ foveal avascular zone

ILM internal limiting membrane

IMEM idiopathic epiretinal membrane

IOP intraocular pressure

IRT inner retinal thickness

IVTA intravitreal triamcinolone acetonide

ME macular edema

MMS mean macular sensitivity

PPV pars plana vitrectomy

SCP superficial capillary plexus

TA triamcinolone acetonide

VEGF vascular endothelial growth factor

Acknowledgements

The authors hereby appreciate all the participants included in this study.

Authors’ contributions

Concept and design:Jie Wang, Yuyan Liu, Quanhong Han. Acquisition, analysis, or interpretation of data: Jie Wang, Yuyan Liu, Gouge Han. Drafting of the manuscript: Jie Wang. Critical revision of the manuscript for important intellectual content:Quanhong Han, Yanhua Chu.Statistical analysis:Jie Wang.Supervision: Yanhua Chu, Quanhong Han.

Funding

Not applicable.

Availability of data and materials

The authors hereby appreciate all the participants included in this study.

Ethics approval and consent to participate

This study is an interventional, retrospective study approved by the Institutional Review Board/Ethics Committee of Tianjin Eye Hospital [approval number:TJYKYYLL-201925, and all procedures in this study followed the principles of the Helsinki Declaration (the 2013 revision), and the applicable Chinese laws]. Due to the retrospective nature of this study, written informed consent for research and publication using their clinical data was routinely merged with surgical informed consent, and no additional written informed consent was given.

Consent for publication

Not applicable.

Competing interests

The authors declare that there is no conflict of interest regarding the publication of this paper.

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No competing interests reported.

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Evaluation of the efficacy and safety of preoperative intravitreal triamcinolone acetonide combined with internal limiting membrane peeling for the treatment of idiopathic macular epiretinal membrane

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Abstract

Purpose

Methods

Results

Conclusion

Figures

Introduction

Methods

Patients

Surgical procedure

Clinical characteristics collections

Statistical analysis.

Results

1. BCVA and IOP

2. OCTA

3. MAIA

Discussion

Abbreviations

Declarations

References

Additional Declarations

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