Differential Distribution of Fibrovascular Proliferative Membranes in 25-Gauge Vitrectomy for Proliferative Diabetic Retinopathy

doi:10.21203/rs.3.rs-1946940/v1

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Differential Distribution of Fibrovascular Proliferative Membranes in 25-Gauge Vitrectomy for Proliferative Diabetic Retinopathy

https://doi.org/10.21203/rs.3.rs-1946940/v1

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Purpose: To analyze the distribution of fibrovascular proliferative membrane (FVPM) in proliferative diabetic retinopathy (PDR) patients that need treated with pars plana vitrectomy (PPV), and to evaluate the outcomes separately.

Methods: Retrospective review of consecutive 25-G PPV cases operated for PDR between September 2018 and April 2020. All FVPMs were outlined and assigned to three groups: arcade type, juxtapapillary type and central type. General characteristics, operation-related variables, best-corrected visual acuity (BCVA) 12 month postoperative and complications were recorded. , All patients were followed up for over one year

Results: In total, 93 eyes were recruited. Among them, the FVPMs distribution of nasotemporal and inferiosuperioral were significantly different (both p < 0.01), with 87 (93.55%) FVPMs located in the nasal hemispheres, and 67 (72.04%) in the inferior hemispheres. The eyes with a central FVPM required the longest operation time, with silicon oil used in most patients, generally combined with tractional retinal detachment (RD) and rhegmatogenous RD, as well as the worst postoperative best-corrected visual acuity and the highest rates of recurrent RD and iatrogenic retinal break formation (all p < 0.05).

Conclusion: FVPMs were more commonly found in the nasal and inferior mid-peripheral retina in addition to the area of arcade vessels. Performing 25-G PPV for treating PDR eyes with a central FVPM had a relatively worse prognosis.

proliferative diabetic retinopathy

fibrovascular proliferative membrane

25-gauge pars plana vitrectomy

Diabetic retinopathy (DR) is the most common ocular complication of diabetes mellitus (DM), and it is a leading cause of blindness in working-age adults who have jobs and families to maintain ^{[1, 2]}. Those individuals with DM who have a poor command of diabetes care knowledge always consult at an extremely severe stage of proliferative DR (PDR) and unfortunately require surgical treatment mainly due to non-clearing vitreous hemorrhage (VH), followed by tractional retinal detachment (TRD) threatening the macula and extensive fibrovascular proliferation unresponsive to laser therapy ^[3].

Pars plana vitrectomy (PPV) is the most cost-effective and long-term stabilizing treatment performed in cases with advanced PDR^{[2, 4]}. During the process of this operation, segmentation and removal of the fibrovascular proliferative membranes (FVPMs) which are prone to cause hemorrhage and iatrogenic retinal break (IRB) is the key point regarding the visual prognosis and postoperative complications ^[5]. Retinal hypoxia elevated by DM is the main reason for diabetic FVPMs, which are principally composed of neovascular stromal tissue. Furthermore, immune-mediated processes also play a role in FVPMs formation in PDR^{[6, 7]}. In addition to the region of the posterior pole, it has been well documented that the neovascularization is more commonly found in the nasal and inferior nasal peripheral retina by fundus imaging techniques ^{[8, 9]}. To the best of our knowledge, there are no studies focusing on the differential distribution of FVPMs attaching to the retina developing in operation.

Since the 25-gauge PPV (25-G PPV) was first described in 2002^{[10, 11]}, the smaller vitrector in limiting the flexibility of the instruments meant that it was considered inappropriate for use in complex cases compared with wider-gauge vitrectomy. However, with the development of 25-G forceps, scissors and directional endolaser probes, the 25-G PPV has been proven to be more effective, safer and with more rapid visual recovery when applied to complications of PDR^[12–16]. In this study, we will analyze the distribution of FVPMs in PDR eyes that required surgical treatment through schematic images sketched by an experienced surgeon after the operations. Most importantly, we will assess the different outcomes of 25-G PPV for the management of PDR with different types of FVPM. It will be useful for the management of expectations and the subsequent treatment to investigate the relevance of FVPMs to the anatomy and visual prognosis.

Study Population

In a retrospective study, the medical records were reviewed from all consecutive surgical cases from September 2018 to April 2020 who underwent primary 25-G PPV for complications of PDR, including persistent or recurrent VH, TRD threatening or involving the macula, combined tractional and rhegmatogenous detachment (TRD/ RRD), at the First hospital of Qinhuangdao. All surgeries were performed by the same and experienced vitreoretinal surgeon (Prof. Zhao). The exclusion criteria were as follows: 1) the follow-up duration was < 12 months, 2) with other reasons leading to proliferative vitreoretinal disease, 3) intraoperative data or follow-up data one year postoperative of the primary vitrectomy were incompleted, 4) without any distinct FVPM in the retina. The study was performed in accordance with the tenets of the Declaration of Helsinki and was approved by the Institutional Review Board of The First Hospital of Qinhuangdao. Written informed consent was obtained from all participants.

Surgical Procedures

Intravitreal Lucentis injection (0.05ml) was performed using a 30-gauge needle through the pars plana under sterile conditions 4–7 days before PPV. All patients underwent retrobulbar anesthesia. If the patients had a cataract that interfered with the surgeon’s observation of the fundus, phacoemulsification were performed through a clear corneal incision before the scleral incision for vitrectomy was made. The Alcon Constellation system (Alcon Laboratories, Inc., Fort Worth, TX, USA) was used with a maximum cut rate of 5000 cuts per min and maximum vacuum rate of 650 mmHg were used to perform 25-G PPV. A conventional three-port PPV was performed. Under a non-contact wide-angle viewing system (BIOM 3, Oculus, Inc., Munich, Germany), a core vitrectomy was firstly performed and subsequently the posterior hyaloid was separated and removed. A suspension of triamcinolone acetonide was injected into the vitreous cavity to mark the posterior cortical vitreous for better visualization. Subsequently, FVPMs were dissected and removed as completely as possible. When required, bimanual technique was applied with vitreoretinal scissors and forceps to remove the FVPMs to relieve traction under the chandelier light. With the aid of scleral indentation, the peripheral vitreous base was shaved. Pan-retinal photocoagulation (PRP) was applied or supplemented following fluid–air exchange. Intraocular lens implantation was performed before completing the surgery. Balanced salt solution (BSS), sterile air or silicon oil tamponade was employed resting with the aspect of the retina. Because of restrictions, sulfur hexafluoride and octafluoropropane used in the operation was prohibited at that time in China.

When the entry sites displayed leakage through localized bleb formation when using BSS, suturing of the sclerotomy sites was performed. Finally, TobraDex ophthalmic ointment was applied to the eye, which was patched and shielded. Patients maintained a face-down position if silicone oil (for 1–2 weeks) or air infusion (for 5–7 days) was employed.

Data Collection

General patient characteristics including sex, age, laterality, age at diabetes onset, diabetes duration, glycated hemoglobin (HbA1c), body mass index (BMI), and the presence of nephropathy, ischaemic heart disease and hypertension were recorded. The following ophthalmological parameters were obtained: a best-corrected visual acuity (BCVA) that was assessed using the Snellen chart, lens status and prior PRP treatment.

All FVPM schematic images were completed in the Paint 3D software (Windows, Version 6.2105.4017) by the surgeon after completing the surgeries and controlled by assistants using surgery videos. The outline of the FVPMs were sketched on a specific layer, which had a standardized background with a macular center surrounded by circles representing the equator, ora serrata, and limbus, for convenient analysis. If needed, correction of the images was performed in cooperation of the surgeons and assistants. Firstly, FVPMs were assigned to three categories^[17]: Group 1 (arcade type): FVPMs encompassed upper and/or lower arcade vessels with or without disc involvement; Group 2 (juxtapapillary type): FVPMs were present around the disk and nasal to the disk; Group 3 (central type): FVPMs were mainly observed in the macular area, with or without arcade vessels involvement. The ‘macular area’ was defined as the area with a diameter of approximately 5.5 mm centered on the foveal depression. Subsequently, the retinal images of the left eyes were flipped across the vertical axis to be analyzed as right eyes. All images were superimposed into a map and normalized. Each pixel in the map represented the overlap probability of an FVPM, and was represented by different gray values. The top of the scale represented the maximum rate of FVPM overlapping and the bottom indicates no FVPM. The location of the FVPM was determined according to its geometric center. The superior, inferior, nasal and temporal hemispheres were defined by a horizontal and a vertical axis across through the fovea.

Primary outcome measures included BCVA 12 month postoperative and rates of patients with BCVA improvement by > 0.3 logMAR. The postoperative complications included vitreous rebleeding which was not absorb over a month required a second surgery to be washed out, recurrent retinal detachment (RD) that require a second operation, elevated intraocular pressure (≥ 21 mmHg) for > 1 week, hypotony (< 6 mmHg), endophthalmitis and neovascular glaucoma (NVG) or neovascular iris (NVI).

Statistical Analysis

To facilitate statistical analysis, the BCVA was converted into the logarithm of the minimum angle of resolution (logMAR). We assigned perception of finger counting equivalent to 2.0 logMAR, and hand motion equivalent to 3.0 logMAR. The normal distribution and homogeneity of variance of the parameters in analysis were preliminarily verified. The Student’s t test or analysis-of-variance (ANOVA) were applied to evaluated continuous variables. If ANOVA proved positive, post hoc tests were used between group pairs. Chi-square test or Fisher’s exact test was used to compare categorical variables. The above statistical analysis was performed using a commercially available statistical software program (SPSS for Mac, version 25.0; IBM/SPSS, Chicago, IL, USA). A two-tailed p-value < 0.05 was considered to be statistically significant.

A total of 93 eyes from 93 patients (41 male, 52 female) were included in the study. Patients’ pre-, intra- and postoperative characteristics are summarized in Table 1. The distribution of patient numbers among the three groups was statistically significant (p < 0.001). While the patients with central type FVPMs had the youngest mean age and that of DM onset, there was no statistically significant difference. The mean BMI, HbA1c and preoperative BCVA were not statistically significant different among the three groups, as were the rates of patients with nephropathy, dialysis, brain infarction, ischaemic heart disease or had received retina photocoagulation.

Table 1

Preoperative, intraoperative, and postoperative clinical characteristics of eyes with FVM that received 25 G vitrectomy
	All		Group 2	Group 3	P-value
Preoperative clinical characteristics
Number of patients, n (%)	93(100%)	53(56.99%)	29(31.18%)	11(11.83%)	< 0.001†
Sex, male, n (%)	43(46.24%)	26(49.06%)	12(41.38%)	5(45.45%)	0.800†
Age, years, mean ± SD	51.22 ± 10.12	51.45 ± 9.33	52.03 ± 11.98	47.91 ± 8.55	0.503*
Operated eye, right, n (%)	36(38.71%)	22(41.51%)	7(24.14%)	7(63.64%)	0.059§
Duration of DM, years, mean ± SD	10.97 ± 6.25	10.57 ± 6.34	11.72 ± 6.22	10.91 ± 6.25	0.729*
Age of onset DM, years, mean ± SD	40.45 ± 9.85	41.25 ± 10.53	40.31 ± 9.33	37.00 ± 7.44	0.432*
HbA1c, %, mean ± SD	8.94 ± 2.12	8.82 ± 2.19	8.73 ± 1.80	10.06 ± 2.37	0.170*
BMI, kg/㎡, mean ± SD	25.64 ± 3.67	25.44 ± 3.60	26.22 ± 4.15	25.04 ± 2.63	0.558*
Nephropathy, n (%)	19(20.43%)	10 (18.87%)	7 (24.14%)	2 (18.18%)	0.838§
Dialysis, n (%)	7(9.68%)	4(7.55%)	2(6.90%)	1(9.09%)	1.000§
Hypertention, n (%)	44(47.31%)	26(49.06%)	13(44.83%)	5(45.45%)	0.927†
Obsolete brain infarction, n (%)	13(13.98%)	9 (16.98%)	3 (10.34%)	1 (9.09%)	0.934§
Ischaemic heart disease, n (%)	8(8.60%)	5 (9.43%)	1 (3.45%)	2 (18.18%)	0.253§
Patients with VH, n(%)	72(77.42%)	43(81.13%)	22(75.86%)	7(63.64%)	0.399§
Patients with previous photocoagulation, n (%)	47(50.54%)	24(45.28%)	18(62.07%)	5(45.45%)	0.326†
Pseudophakic, n (%)	7(7.53%)	6 (11.32%)	1 (3.45%)	0 (0.00%)	0.430§
Preoperative BCVA, LogMAR, mean ± SD	1.67 ± 0.44	1.62 ± 0.49	1.70 ± 0.39	1.83 ± 0.23	0.327*
Snellen visual acuity ratio	20/925	20/800	20/1000	20/1400	NA
Intraoperative clinical characteristics
Operation time, minutes, mean ± SD	73.23 ± 25.13	65.43 ± 18.66	77.62 ± 28.39	99.18 ± 25.00	< 0.001*
Combined with cataract extraction, n (%)	35(37.63%)	16 (30.19%)	13 (44.83%)	6 (54.55%)	0.199†
Tamponade
gas, n (%)	22(23.66%)	14 (26.42%)	6 (20.69%)	2 (18.18%)	0.777§
silicon oil, n (%)	20(21.51)	7 (13.21%)	6 (20.69%)	7(63.64%)	0.002§
Photocoagulation, shots, mean ± SD	1025 ± 445	977 ± 396	1033 ± 515	1243 ± 442	0.194*
Patients with TRD, n (%)	58(62.37%)	36 (67.92%)	18 (62.07%)	4 (36.36%)	0.144§
Patients with combined RRD-TRD, n (%)	21(22.58%)	8 (15.09%)	6 (20.69%)	7 (63.64%)	0.004§
Postoperative clinical characteristics
BCVA 12 month postoperative, LogMAR, mean ± SD	0.98 ± 0.67	0.78 ± 0.53	1.09 ± 0.64	1.63 ± 0.91	< 0.001*
Snellen visual acuity ratio	20/200	20/120	20/245	20/850	NA
Patients with BCVA improvement by > 0.3 logMAR‡, n (%)	68 (73.12%)	43(81.13%)	20(68.97%)	5(45.45%)	0.044†

BMI, Body Mass Index. logMAR, logarithm minimum angle of resolution; BCVA, best corrected visual acuity; NA, not applicable;
* ANOVA; † c2 test; §Fisher exact test; ‡ 0.3 logMAR units were assigned equivalent of 15 ETDRS letters

The operation time was significantly different among the three groups (p < 0.001). The post hoc tests showed that the operation time of central type group was significantly longer than that of juxtapapillary type group (p = 0.023) and arcade type group (p < 0.001), as well as the juxtapapillary type group versus arcade type group (p = 0.009). The rates of silicon oil used as a tamponade in the operation and patients with a combined tractional-rhegmatogenous RD (TRD/ RRD) were significantly different among the three groups (p = 0.002 and p = 0.004, respectively). All eyes of central type group underwent or were supplemented by PRP with the highest mean shot number of 1243 ± 442, but there was no statistically significant difference among the three groups (p = 0.194).

Figure 1 shows the distribution of the FVPMs represented by the overlapped retinal images. They were mostly confined to equator (92 FVPMs) and mainly along the vascular arcades around the optic disc, with the majority concentrated nasally to the macula. Because 87 (93.55%) were located in the nasal and 6 (6.45%) in the temporal hemisphere, the FVPM centroids had a significant asymmetry between the nasal and temporal distribution (p < 0.001). Furthermore, the distribution between the superior and inferior hemispheres was 26 (27.96%) and 67 (72.04%), respectively, which was statistically different (p < 0.001).

The mean LogMAR BCVA of all patients and of those from arcade type and juxtapapillary type group were significantly improved at the final visit compared to that preoperatively (all p < 0.001). Only the improvement of patients with central type FVPM was not statistically significant (p = 0.456). The BCVA improved by > 0.3 logMAR units, approximately equal to the 15 Early Treatment Diabetic Retinopathy Study (ETDRS) letters, in 43 eyes (81.13%) of the arcade type, 20 eyes (68.97%) of group 2 and 5 eyes (45.45%) of central type group. However, this rate of improvement was not significantly different among the three groups. Although the average preoperative visual acuity was not statistically significantly different among the three groups, arcade type group at the final visit had the best BCVA compared with that of juxtapapillary type (p = 0.029) and central type (p < 0.001) group. Post hoc tests also showed that the BCVA of juxtapapillary type group was significantly better than that of central type group (p = 0.016).

In our cohort, there were no cases of endophthalmitis or hypotony, and only nine cases (9.68%) presented with recurrent RD that required a second PPV procedure. IRBs were distinguished by intraoperative endocautery and identified in 16 (17.2%) eyes. There was a significant difference among three groups regarding the rates of eyes with recurrent RD and IRBs (p = 0.006 and p = 0.005, respectively). The rate of recurrent VH that required a re-vitrectomy was 4.30%. High intraocular pressure sustained for > 1 week presented in 13 (13.98%) patients and NVG/NVI occurred in four (4.30%) eyes. There were no significant differences in the distributions of eyes with high intraocular pressure, NVG/NVI and recurrent VH among the three groups. These outcomes are presented in Table 2.

Table 2

Intraoperative and postoperative complications.
	All	Group 1	Group 2	Group 3
Iatrogenic retinal breaks	16 (17.20%)	6 (11.32%)	4 (13.79%)	6 (54.55%)	0.006§
Retinal detachment	9 (9.68%)	1 (1.89%)	5 (17.24%)	3 (27.27%)	0.005§
Recurrent vitreous hemorrhage	4 (4.30%)	2 (3.77%)	2 (6.90%)	0 (0.00%)	0.767§
IOP evaluation	13 (13.98%)	5 (9.43%)	4 (13.79%)	4 (36.36%)	0.067§
Neovascularizations (angle and/or iris)	4 (4.30%)	1 (1.89%)	2 (6.90%)	1 (9.09%)	0.237§
Data are presented as number (%) of cases
§Fisher exact test.

Location variation of FVPMs in PDR eyes will affect the macular structure, which is closely associated with the visual and anatomic prognosis postoperatively ^{[17, 18]}. In the current report and other studies ^{[3, 13]}, approximately 80% of patients require PPV surgery due to a non-clearing or recurrent VH. Therefore, the fundus of most patients was only firstly observed clearly during the operation, and the FVPM was the most distinguishable sign that could be detected without any auxiliary equipment. In the current study, we investigated the approximate distributions of FVPMs through the schematic images and evaluated the different outcomes of 25-G PPV for the management of PDR with different FVPM types.

Previous studies showed that microaneurysms mainly occur around the macular region at the early stage of DR ^[19]. As NPDR develops, the retinal nonperfusion areas extend to the larger vascular arcades and midperipheral retina ^{[20, 21]}, mainly appearing in the nasal hemisphere ^[9]. In PDR, it was also reported that the majority of the neovascularization was located in the nasal hemisphere and along the superior vascular arcades ^{[8, 9]}. There are four layers of capillary network together with nerve fiber axons around the optic disc but only three layers in the macula ^[22], such that the nasal side has relatively abundant blood vessels and is more susceptible to ischemia. This could be the reason that neovascularization induced by ischemia always spreads on the nasal hemisphere of retina. In the current study, the overlapped fundus map was consistent with previous studies and showed that a large amount of FVPMs spread along the vascular arcades and nasally to the macular. Because FVPMs are mainly composed of neovascular stromal tissue, their distribution is almost consistent with NVE. Furthermore, it was also affected by common process of posterior vitreous detachment (PVD). This frequently starts in the foveal areas and extends first in a superior direction. Subsequently, the PVD extends further in superotemporal and nasal direction and continues in inferotemporal direction before extending further nasally^[23]. The occurrence of NVE and FVPMs on the retinal surface are based on an appropriate scaffold of collagenous material, such that PDR progression is not significantly associated with no PVD or partial PVD^[24]. This PVD process depicted above may also be a possible reason for the phenomenon that among the three categories of FVPM described here, the rarest was the central type.

In the current study, the distribution of FVPMs was not associated with age, sex, laterality, DM duration or age of onset, HbA1c or BMI. Suffering from nephropathy, hypertension or obsolete brain infarction or requiring dialysis or preoperative photocoagulation treatment also did not affect the FVPM distribution. Theoretically, PVD does not initiate in younger patients, who were thus prone to present with a central type FVPM. Although the patients of group 3 had the youngest mean age and DM onset in our study, there was no statistically significant difference among the three groups.

Our results demonstrated that 25-G PPV was safe and effective in the management of PDR complicated with FVPM, particularly the PDR eyes with arcade or juxtapapillary type FVPM. By comparison, the recruited eyes of central type group displayed the highest rates of combined TRD/RRD, IRB formation, silicon oil tamponade, recurrent RD and worst BCVA 1 year, postoperatively. All of the central type FVPMs involving macular unexpectedly promoted a poor visual prognosis than the other two types, as well as the anatomic results. Therefore, it will raise concern when the fundus photograph or ultrasonography providing insight into the prognosis following vitrectomy to patients indicate that FVPMs are present around the posterior pole. Additionally, early intervention is essential for PDR patients with neovascularization concentrated on the macula with no or partial PVD.

It has been confirmed that the high incidence of IRBs formation was associated with increased postoperative complications, including rebleeding, recurrent RD and NVG, as well as worse postoperative BCVA^{[5, 25]}. Smaller gauge PPV with high cut rates was reported to display more stable fluidics due to diminished flow and a better ability to preserve the vitreous base that prevents vitreal incarceration and dragging, which will minimize the risk for IRBs^{[13, 26]}. Studies which recruited > 100 eyes showed that the incidence of IRBs formed in 20-gauge surgery ranged from 33–41%^{[5, 25]}. Using 23-gauge vitrectomy systems, Celik et al^[27] observed IRBs in 15% of eyes with diabetic FVPM threatening the macula. Using 25-G vitrectomy systems, Mikhail et al^[12] reported only six IRBs in 109 eyes in the management of diabetic TRDs and Atlan et al^[14] reported that retinal tear formation occurred in 28.5% of eyes in diabetic TRD. In the present study, the IRBs incidence was 11.32%, 13.79%, and 54.55% in the eyes of arcade type group, juxtapapillary type group and central type group, respectively. A possible explanation for the highest IRB incidence rate in eyes with central type FVPMs is that this group had the highest incidence of combined TRD/RRD. Combined TRD/RRD is a serious and challenging complication in PDR and requires more effective surgical management, which is frequently associated with poor visual outcomes and anatomic complications following PPV ^{[28, 29]}. The broader FVPM is prone to trigger tangential traction, which may create retinal breaks and transforms a pure TRD to a combined TRD/RRD. The incidence of IRB formation during an operation was increased by relatively complex ocular conditions, such as combined TRD/RRD, which will induce retinal atrophy and fragility.

Our study has several limitations. Firstly, we were only able to retrospectively evaluate inaccurate images outlined roughly after the operation because most patients recruited in the current study also displayed VH or opacified vitreous or lens. The inaccurate drawings could not provide the specific size or length or distance from the macula. Secondly, our study included only patients with completed review data in the first year of follow-up. Those patients with a follow-up < 12 months were excluded. The consequences of this bias may have affected the results. Furthermore, review data from the third and sixth months were incomplete. Consequently, the change in visual acuity could not be observed continuously.

In summary, our study demonstrated that FVPMs were more commonly found in the area of arcade vessels, followed by nasal and inferior mid-peripheral retina. Performance of 25-G vitrectomy proved to be safe in managing complicated PDR and was able to achieve satisfactory anatomical outcomes to preserve or improve vision in a large proportion of cases with complicated FVPMs. Given that PDR patients with central type FVPM had a relatively worse visual and anatomic prognosis in comparison, further research into earlier intervention of PDR with central type FVPM are warranted.

Acknowledgments

Thanks to Prof. Lu and colleagues in endocrinology department for their contributions to data

collection.

Disclosure

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding：none

Conflict of Interest: The authors declare no commercial interest that they may have in the subject of study and the source of any financial or material support.

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Differential Distribution of Fibrovascular Proliferative Membranes in 25-Gauge Vitrectomy for Proliferative Diabetic Retinopathy

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