Introduction: To investigate the characteristics of macular pseudoholes (MPHs) with different foveal profiles and their impact on preoperative and postoperative visual acuity (VA). Methods: A retrospective review of 47 eyes from 46 consecutive patients with MPH who had undergone vitrectomy was conducted. The MPHs were classified into u-shape and v-shape according to the morphological description of the foveola base. The best-corrected visual acuity (BCVA), central foveal point thickness, parafoveal thickness, parafoveal inner and outer retinal thickness, stretched lamellar cleavage, microcystic macular edema (MME), disorganization of retinal inner layers (DRIL), and the integrity of outer retinal layers were recorded. Results: The eyes in the v-shaped group (n = 31) had lower BCVA, thicker retinal thickness, more intraretinal cleavage, MME, and DRIL than the u-shaped (n = 16) group (all p < 0.05). Multiple regression analysis revealed that the morphology of the foveola base was significantly related to the preoperative BCVA (p = 0.025). The VA was significantly improved in both groups, and the improvement was greater in the v-shaped group (p = 0.024). No significant difference was found in the postoperative BCVA between the two groups (all p > 0.05). Conclusion: The v-shape, reflecting the stretch in the foveola, had a significant impact on preoperative BCVA. However, the VA was improved after surgery whatever their initial foveal profile.

A macular pseudohole (MPH) was initially described as a round, reddish image when visualized by biomicroscopy, usually similar to the full-thickness macular hole. As previous studies indicated, MPH and idiopathic epiretinal membrane (iERM) may be different manifestations of the same disease [1, 2]. In the eyes diagnosed with ERMs, the reported prevalence of MPH is about 8–20% [3‒6]. The mechanism of MPH development relies on a chronic contraction of the ERM surrounding the fovea. Because the ERM does not cover the foveal pit, the retinal structure and visual function changes induced by the ERM contraction in MPHs may differ from the iERMs [2, 7‒9].

Surgical removal of the ERM is a standard treatment for symptomatic ERMs. And the results show that the functional and anatomical outcomes in iERM patients will be significantly improved after the pars plana vitrectomy (PPV) [10‒16]. However, the surgical indications and the significance of surgical treatment for MPHs are still controversial. Because most MPH patients can maintain a good visual acuity (VA) and are relatively stable for a long time, some studies believed that there was no significant improvement in VA in MPH patients after relieving the ERM-induced traction [7, 17, 18]. These controversies make it necessary to evaluate which patients benefit from ERM surgery and which do not.

Recently, Bringmann et al. [19] classified the MPH into u-shape and v-shape according to the morphology of the foveal pit base. And the v-shape was considered due to the stretching of the Müller cell cone in the foveal pit area [19]. The ERM-induced traction to the fovea could lead to subsequent retina structural changes [1, 19‒23]. However, there was no study to determine whether differences in clinical features and prognosis exist between these two MPH types. Therefore, by analyzing the morphology of the foveal pit base from spectral-domain optical coherence tomography (SD-OCT) images, this study aims to compare the anatomical and visual functional characteristics and the response to surgery of MPHs with different foveola profiles. Furthermore, to determine the related factors in preoperative and postoperative VA for the patients who are diagnosed with MPH, to provide suggestions for retinal surgeons to select an optimal operation time.

Patients

This retrospective study was approved by the Beijing Tongren Hospital Ethics Committee and was adherent to the tenets of the Declaration of Helsinki. Consecutive enrollment of the patients diagnosed with MPH was performed at Beijing Tongren Hospital from September 2016 to October 2021. Eye with secondary ERM, high myopia (axial length >26.0 mm, refractive error <−6 diopters), history of vitreoretinal surgery, combined with other macular and anterior diseases that could confound the visual outcomes were excluded.

The diagnosis of MPHs was based on the following criteria proposed by The International Vitreomacular Traction Study (IVTS) Group: concomitant ERM with a central opening, invaginated or heaped foveal edges, steeped macular contour to the central fovea with near-normal central foveal thickness, no loss of retinal tissue [24].All patients diagnosed with MPH underwent a comprehensive ophthalmic evaluation and examination at baseline and 1, 4, 10, and 24 months after the operation.

SD-OCT Analysis

An SD-OCT device (Cirrus high-definition OCT; Carl Zeiss Meditec, Dublin, CA) was used to obtain the macular structural image of all patients. Each eye was imaged with the macular cube 518 × 128 scans and the HD 5-line raster. According to the OCT images, the foveal pit in the u-shaped group had vertical, straight edges and smooth bases, whereas the foveal pit in the v-shaped group had stretched edges and bases, with or without retinal cleavage (shown in Fig. 1). The central foveal point thickness was measured from the outer edge of the retinal pigment epithelium (RPE) to the innermost retinal layer at the foveal center. The mean parafoveal thickness (inner limiting membrane [ILM]-RPE), parafoveal inner retinal thickness (ILM-inner nuclear layer), and parafoveal outer retinal thickness (outer plexiform layer-RPE) were measured from either side of the fovea at the location approximately 750 μm from the foveal center, and the two measurements were averaged. Pseudohole depth was the vertical distance from the innermost retinal layer to the pseudohole base. Pseudohole diameter was measured at half pseudohole depth from nasal to temporal margin. All these quantitative parameters were manually measured using the caliper function of the OCT instrument. As shown in Figure 2, the stretched lamellar cleavage, microcystic macular edema (MME), and disorganization of retinal inner layers (DRIL) were also recorded. The integrity of the outer retinal layers was evaluated with regard to the interdigitation zone (IZ).

Fig. 1.

Examples of different foveal pit configurations in MPH: the u-shaped foveal pit base had vertical, straight edges and a smooth base (a); and the v-shaped foveal pit base had stretched edges and base (b).

Fig. 1.

Examples of different foveal pit configurations in MPH: the u-shaped foveal pit base had vertical, straight edges and a smooth base (a); and the v-shaped foveal pit base had stretched edges and base (b).

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Fig. 2.

Two MPH cases with a v-shaped foveal pit base. a The stretched lamellar cleavage (white arrow), and a disruption of the interdigitation zone (IZ) can be seen (black arrow). b The presence of microcystic macular edema (MME; green arrow), and disorganization of retinal inner layers (DRIL; white rectangle) were also recorded.

Fig. 2.

Two MPH cases with a v-shaped foveal pit base. a The stretched lamellar cleavage (white arrow), and a disruption of the interdigitation zone (IZ) can be seen (black arrow). b The presence of microcystic macular edema (MME; green arrow), and disorganization of retinal inner layers (DRIL; white rectangle) were also recorded.

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Surgical Procedure

All patients underwent 23-gauge transconjunctival 3-port PPV by one surgeon (W.L.). After core and peripheral vitrectomy, the ERM and ILM were then removed by 23-gauge micro forceps. The area of the ILM peeling was about 2–3 optic disc diameter and, depending on the surgeon’s decision, 0.25% indocyanine green dye was used to make the ILM more visible. After the air-fluid exchange, sterile air tamponade was made for all patients.

Statistical Analysis

Analyses were performed using version 26.0 SPSS software (SPSS Inc, Chicago, IL). Mean ± SD was calculated for continuous variables. Qualitative data were presented as frequency and percentage. For data analysis, the decimal best-corrected visual acuity (BCVA) was converted to a logarithm of the minimum angle resolution (logMAR) acuity. For bivariate analyses, the t test was used for continuous data with normal distribution, the Mann-Whitney U test was used for non-normal data, and the χ2 test was used for count data. Multivariate linear regression analysis was performed to determine the factors associated with the preoperative BCVA.

Study Population

Forty-six eligible patients (47 eyes) were included in this study. Eleven (23.9%) were men and 35 (76.1%) were women. The mean age of this cohort was 65.2 ± 8.5 years. The mean logMAR BCVA was 0.4 ± 0.3. The mean central foveal point thickness was 217.1 ± 36.8 μm in the MPH eyes, 210.9 ± 19.7μm in the fellow healthy eyes (p = 0.265). Detailed baseline characteristics of the enrolled eyes are summarized in Table 1. At the time of operation, in addition to 2 eyes being already pseudophakic, 38 of the 45 patients (84.4%) had undergone combined PPV and cataract surgery. The ERM was successfully removed in all treated eyes, and no intraoperative or postoperative complications happened.

Table 1.

Patients’ baseline characteristics

CharacteristicsPatients
Patients/Eyes, n 46/47 
Male/Female, n (%) 11 (23.9)/35 (76.1) 
Age, years 65.2±8.5 
Log MAR BCVA 0.4±0.3 
Axial length, mm 23.4±1.5 
Intraocular pressure, mm Hg 15.0±3.3 
Duration of symptoms, months 17.8±18.4 
Lens status, phakia/pseudophakia, n (%) 45 (95.7)/2 (4.3) 
The morphology of foveal pit base, U-/V-shaped, n (%) 16 (34.0)/31 (66.0) 
The presence of MME, n(%) 22 (46.8) 
The presence of stretched lamellar cleavage, n (%) 30 (63.8) 
The presence of DRIL, n (%) 19 (40.4) 
The disruption of IZ layer, n (%) 6 (12.8) 
Central foveal point thickness, μm 217.1±36.8 
Parafoveal thickness, μm 475.1±69.3 
Parafoveal inner retinal thickness, μm 223.5±50.5 
Parafoveal outer retinal thickness, μm 253.7±49.5 
Pseudohole depth, μm 310.4±98.3 
Pseudohole diameter, μm 432.2±187.2 
CharacteristicsPatients
Patients/Eyes, n 46/47 
Male/Female, n (%) 11 (23.9)/35 (76.1) 
Age, years 65.2±8.5 
Log MAR BCVA 0.4±0.3 
Axial length, mm 23.4±1.5 
Intraocular pressure, mm Hg 15.0±3.3 
Duration of symptoms, months 17.8±18.4 
Lens status, phakia/pseudophakia, n (%) 45 (95.7)/2 (4.3) 
The morphology of foveal pit base, U-/V-shaped, n (%) 16 (34.0)/31 (66.0) 
The presence of MME, n(%) 22 (46.8) 
The presence of stretched lamellar cleavage, n (%) 30 (63.8) 
The presence of DRIL, n (%) 19 (40.4) 
The disruption of IZ layer, n (%) 6 (12.8) 
Central foveal point thickness, μm 217.1±36.8 
Parafoveal thickness, μm 475.1±69.3 
Parafoveal inner retinal thickness, μm 223.5±50.5 
Parafoveal outer retinal thickness, μm 253.7±49.5 
Pseudohole depth, μm 310.4±98.3 
Pseudohole diameter, μm 432.2±187.2 

BCVA, best corrected visual acuity; logMAR, logarithm of the minimal angle of resolution; MME, microcystic macular edema; DRIL, disorganization of retinal inner layers; IZ, interdigitation zone.

Clinical Characteristics in Different MPH Types and Their Impact on Preoperative BCVA

The eyes were categorized into two groups according to their profile of the foveal pit base: the u-shaped group (n = 16) and the v-shaped group (n = 31). There were statistical differences between the clinical characteristics of MPH with a u-shape or v-shape foveola base, as shown in Table 2. The v-shaped group had a statistically significant lower BCVA of 0.5 ± 0.3 logMAR compared with that of the u-shaped group 0.3 ± 0.2 logMAR (p = 0.001). In addition, the v-shaped group had a thicker central foveal point thickness (p = 0.009), a thicker parafoveal thickness (p = 0.001), a thicker parafoveal inner retinal thickness (p = 0.003), a deeper pseudohole depth (p = 0.002), and a shorter pseudohole diameter (p = 0.013) than the u-shaped group. Furthermore, the v-shaped group had more intraretinal structural changes caused by ERM-induced stretches, such as MME (p = 0.001), stretched lamellar cleavage (p < 0.001), and DRIL (p = 0.005). Although the percentage of IZ defects was higher in the v-shaped group, there was no significant statistical difference (p = 0.155).

Table 2.

Preoperative characteristic difference between the macular pseudoholes with u-shape and v-shape foveola base

VariablesMorphology of foveal pit basep value
U-shape (n = 16)V-shape (n = 31)
Age, years 66.9±7.1 64.3±9.1 0.321* 
Log MAR BCVA 0.3±0.2 0.5±0.3 0.001* 
Axial length, mm 23.3±2.1 23.5±1.1 0.057a 
IOP, mm Hg 14.3±4.4 15.4±2.6 0.281* 
Duration of symptoms, months 17.6±18.4 17.8±18.8 0.613a 
The presence of MME, n (%) 2 (12.5) 20 (64.5) 0.001** 
The presence of stretched lamellar cleavage, n (%) 3 (18.8) 27 (87.1) <0.001** 
The presence of DRIL, n (%) 2 (12.5) 17 (54.8) 0.005** 
The disruption of IZ layer, n (%) 0 (0) 6 (19.4) 0.155** 
Central foveal thickness, μm 202.0±21.5 225.13±40.8 0.009a 
Parafoveal thickness, μm 436.0±45.5 496.0±71.3 0.001* 
Parafoveal inner retinal thickness, μm 208.8±39.3 231.3±54.6 0.003* 
Parafoveal outer retinal thickness, μm 231.8±30.0 265.3±54.1 0.206a 
Pseudohole depth, μm 258.9±46.5 337.8±107.9 0.002a 
Pseudohole diameter, μm 524.6±186.1 382.9±170.9 0.013* 
VariablesMorphology of foveal pit basep value
U-shape (n = 16)V-shape (n = 31)
Age, years 66.9±7.1 64.3±9.1 0.321* 
Log MAR BCVA 0.3±0.2 0.5±0.3 0.001* 
Axial length, mm 23.3±2.1 23.5±1.1 0.057a 
IOP, mm Hg 14.3±4.4 15.4±2.6 0.281* 
Duration of symptoms, months 17.6±18.4 17.8±18.8 0.613a 
The presence of MME, n (%) 2 (12.5) 20 (64.5) 0.001** 
The presence of stretched lamellar cleavage, n (%) 3 (18.8) 27 (87.1) <0.001** 
The presence of DRIL, n (%) 2 (12.5) 17 (54.8) 0.005** 
The disruption of IZ layer, n (%) 0 (0) 6 (19.4) 0.155** 
Central foveal thickness, μm 202.0±21.5 225.13±40.8 0.009a 
Parafoveal thickness, μm 436.0±45.5 496.0±71.3 0.001* 
Parafoveal inner retinal thickness, μm 208.8±39.3 231.3±54.6 0.003* 
Parafoveal outer retinal thickness, μm 231.8±30.0 265.3±54.1 0.206a 
Pseudohole depth, μm 258.9±46.5 337.8±107.9 0.002a 
Pseudohole diameter, μm 524.6±186.1 382.9±170.9 0.013* 

logMAR, logarithm of the minimal angle of resolution; BCVA, best corrected visual acuity; IOP, intraocular pressure; MME, microcystic macular edema; DRIL, disorganization of retinal inner layers; IZ, interdigitation zone.

*Independent samples t test.

**χ2 test.

aMann-Whitney U test.

According to the step-wise multiple linear regression analysis, the duration of symptoms (p = 0.011, 95% CI: −0.011∼−0.009), the morphology of foveal pit base (p = 0.025, 95% CI: 0.024∼0.025), and central foveal point thickness (p = 0.006, 95% CI: 0.001∼0.005) were significantly associated with the preoperative BCVA (F = 8.973, p < 0.001).

Visual and Anatomical Outcomes in Two MPH Patterns

The retinal structure of most patients recovered well. Figure 3 is a sample case of v-shaped and u-shaped patients representing the microstructure recovery process of most patients. Table 3 demonstrates the retinal thickness changes in the whole cohort. There was no significant change in retinal thickness in the u-shaped group (all p > 0.05). A significant difference was found in the v-shaped group, such as a significant increase in the central foveal point thickness (p = 0.042) and a significant decrease in the parafoveal retinal thickness (p = 0.005), PIRL thickness (p = 0.014), and PORL thickness (p = 0.012). In addition, after surgery, stretched lamellar cleavage was resolved in 43.3% (13/30) of eyes, MME was resolved in 68.2% (15/22) of eyes, DRIL was resolved in 78.9% (15/19) of eyes, and the IZ band was recovered in 83.3% (5/6) of eyes.

Fig. 3.

Examples of the retinal structure changes in two types of macular pseudoholes before and after the operation. a The OCT images in a u-shaped eye before and 1, 4, and 10 months after surgery. b The OCT images in a v-shaped eye before and 1, 4, and 10 months after surgery.

Fig. 3.

Examples of the retinal structure changes in two types of macular pseudoholes before and after the operation. a The OCT images in a u-shaped eye before and 1, 4, and 10 months after surgery. b The OCT images in a v-shaped eye before and 1, 4, and 10 months after surgery.

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Table 3.

Changes in the retinal thickness and VA in the whole cohort and subgroups

VariablesBaselineMonth 1Month 4Month 10Month 24p value
Total 
 Central foveal point thickness, μm 217.1±36.8a 346.3±96.5 316.6±91.5 282.2±88.6 268.3±85.2 <0.001* 
 Parafoveal thickness, μm 475.1±69.3a 416.1±46.6 403.5±37.5 385.4±34.8 381.5±27.0 0.002* 
 Parafoveal inner retinal thickness, μm 223.5±50.5b 191.5±19.5 174.3±22.3 168.9±23.8 168.5±21.2 0.003c 
 Parafoveal outer retinal thickness, μm 253.7±49.5a 239.5±32.8 228.0±22.8 218.4±20.2 217.5±16.1 <0.001* 
 Log MAR BCVA 0.4±0.3a 0.3±0.2 0.2±0.2 0.1±0.1 0.1±0.1 <0.001* 
U-shaped group 
 Central foveal point thickness, μm 202.0±21.5 326.3±83.9 332.4±81.4 272.6±75.7 227.0±39.9 0.054* 
 Parafoveal thickness, μm 436.0±45.5 401.8±27.0 392.9±32.5 364.6±27.2 363.4±10.3 0.120c 
 Parafoveal inner retinal thickness, μm 208.8±39.3 185.5±17.0 161.6±24.2 150.1±13.1 153.8±10.3 0.308* 
 Parafoveal outer retinal thickness, μm 231.8±30.0 234.1±30.6 224.5±21.5 216.9±18.7 221.8±14.1 0.339* 
 Log MAR BCVA 0.3±0.2b 0.2±0.1 0.1±0.1 0.1±0.1 0.0±0.1 0.042* 
V-shaped group 
 Central foveal point thickness, μm 225.1±40.8b 358.2±102.9 308.4±97.0 288.6±99.0 289.0±96.2 0.001c 
 Parafoveal thickness, μm 496.0±71.3b 425.4±54.4 409.0±39.4 399.3±33.2 390.6±28.6 0.012* 
 Parafoveal inner retinal thickness, μm 231.3±54.6b 195.1±20.3 180.8±18.6 181.5±21.0 175.9±21.7 0.013c 
 Parafoveal outer retinal thickness, μm 265.3±54.1a 242.8±34.2 229.8±23.8 219.4±21.9 215.3±17.5 0.002* 
 Log MAR BCVA 0.5±0.3a 0.3±0.2 0.3±0.2 0.2±0.1 0.1±0.1 <0.001* 
VariablesBaselineMonth 1Month 4Month 10Month 24p value
Total 
 Central foveal point thickness, μm 217.1±36.8a 346.3±96.5 316.6±91.5 282.2±88.6 268.3±85.2 <0.001* 
 Parafoveal thickness, μm 475.1±69.3a 416.1±46.6 403.5±37.5 385.4±34.8 381.5±27.0 0.002* 
 Parafoveal inner retinal thickness, μm 223.5±50.5b 191.5±19.5 174.3±22.3 168.9±23.8 168.5±21.2 0.003c 
 Parafoveal outer retinal thickness, μm 253.7±49.5a 239.5±32.8 228.0±22.8 218.4±20.2 217.5±16.1 <0.001* 
 Log MAR BCVA 0.4±0.3a 0.3±0.2 0.2±0.2 0.1±0.1 0.1±0.1 <0.001* 
U-shaped group 
 Central foveal point thickness, μm 202.0±21.5 326.3±83.9 332.4±81.4 272.6±75.7 227.0±39.9 0.054* 
 Parafoveal thickness, μm 436.0±45.5 401.8±27.0 392.9±32.5 364.6±27.2 363.4±10.3 0.120c 
 Parafoveal inner retinal thickness, μm 208.8±39.3 185.5±17.0 161.6±24.2 150.1±13.1 153.8±10.3 0.308* 
 Parafoveal outer retinal thickness, μm 231.8±30.0 234.1±30.6 224.5±21.5 216.9±18.7 221.8±14.1 0.339* 
 Log MAR BCVA 0.3±0.2b 0.2±0.1 0.1±0.1 0.1±0.1 0.0±0.1 0.042* 
V-shaped group 
 Central foveal point thickness, μm 225.1±40.8b 358.2±102.9 308.4±97.0 288.6±99.0 289.0±96.2 0.001c 
 Parafoveal thickness, μm 496.0±71.3b 425.4±54.4 409.0±39.4 399.3±33.2 390.6±28.6 0.012* 
 Parafoveal inner retinal thickness, μm 231.3±54.6b 195.1±20.3 180.8±18.6 181.5±21.0 175.9±21.7 0.013c 
 Parafoveal outer retinal thickness, μm 265.3±54.1a 242.8±34.2 229.8±23.8 219.4±21.9 215.3±17.5 0.002* 
 Log MAR BCVA 0.5±0.3a 0.3±0.2 0.3±0.2 0.2±0.1 0.1±0.1 <0.001* 

A pairwise comparison was performed between the baseline and the final follow-up period.

*Freidman test.

a, b means p < 0.05, assessed by paired-samples t test and Wilcoxon matched-pairs signed-rank test, respectively.

cOne-way Repeated Measures ANOVA analysis.

As shown in Table 3, the final BCVA was significantly improved in the whole cohort, and it also improved in both the u-shaped and v-shaped groups, respectively. In our study, the VA was improved in 39 eyes (83.0%) postoperatively. Among the eight eyes (17.0%) with VA not improved, 5 eyes were decreased and 3 eyes remained unchanged. In the comparison of the baseline characteristics between the two groups, we found that the eyes with the VA not improved tended to have a better baseline VA (LogMAR BCVA: 0.2 ± 0.1 vs. 0.5 ± 0.3, p = 0.001). There was no significant difference in follow-up time and the proportion of combined cataract surgery between the two groups (p = 0.059, and p = 1.000). The BCVA before (LogMAR BCVA: 0.3 ± 0.2 vs. 0.5 ± 0.3, p = 0.001) and early after the operation (LogMAR BCVA: 0.2 ± 0.1 vs. 0.3 ± 0.2, p = 0.042) was significantly different between the two groups, whereas this difference disappeared 4 months after surgery (LogMAR BCVA: 0.1 ± 0.1 vs. 0.2 ± 0.2, p = 0.056 at 4 months; 0.1 ± 0.1 vs. 0.2 ± 0.1, p = 0.459 at 10 months; 0.0 ± 0.1 vs. 0.2 ± 0.2, p = 0.231 at 24 months). The improvement of BCVA in eyes with u-shaped foveola was significantly lower than that in eyes with v-shape (Log MAR BCVA: 0.2 ± 0.1 vs. 0.3 ± 0.3, p = 0.024).

This 2-year follow-up study systematically and comprehensively revealed that PPV combined ERM and ILM peeling was effective in restoring visual function in patients with MPHs in different foveal pit morphologies. Moreover, our study further illustrated the related factors for baseline visual impairment and prognostic factors for postoperative VA improvement.

Recently, according to the morphological description of the foveal pit base, Bringmann et al. [19] divided the MPHs into two categories: u-shape and v-shape. And the mechanism of the v-shaped base was mainly caused by the stretching of the Müller cell cone in the foveal pit area [19]. The ERM-induced traction to the fovea could lead to a subsequent elevation of the inner retinal layers of the foveal walls, which progressed to become a foveoschisis characterized as a schistic splitting between the inner and outer retina connected by stretched Henle fibers [1, 19‒21]. Previous studies indicated that as Müller cells were straightened, their stiffness would be increased, and their ability to transmit mechanical force across the entire retinal layers would be strengthened [19, 22, 23]. And then, it might further cause damage to the outer retinal layers. Coherent with the results of Bringmann et al. [19], our study demonstrated that the incidence rate of MME (p = 0.001), stretched lamellar cleavage (p < 0.001), and DRIL (p = 0.005) in the v-shaped group was significantly higher compared with the results in the u-shaped group. However, if the u-shaped MPH could be developed into the v-shaped counterpart is still unclear. In other words, the u-shaped MPH and v-shaped MPH are two distinct entities, or just represent temporally distant steps in the MPH evolution, which still need a further prospective study to confirm.

Based on the conventional classification system confirmed by the IVTS Group, the presence of foveoschisis was one of the diagnostic criteria for lamellar macular holes [24]. Until 2013, Gaudric et al. [1] proposed that the MPHs with stretched edges belonged to the MPH spectrum. However, the prognostic value of this factor remains controversial. Toyama et al. [6] categorized the MPHs into 3 stages according to the extent of retinal cleavages, and found that the advanced cleavage was associated with worse VA preoperatively and the extensive cleavage could independently predict greater postoperative VA recovery. However, Gaudric et al. [1] found that there was no significant difference between the groups with stretched edges and without stretched edges in preoperative or postoperative VA. In our study, the eyes with retinal cleavages had lower baseline BCVA compared with the eyes without retinal cleavages (p = 0.025). However, in the univariate and multiple regression analysis, we found no significant relationship between the retinal cleavage and VA. This discrepancy might result from the study performed by Toyama et al. [6] who only adjusted the age, gender, and lens status. However, the other retinal structural changes caused by ERM traction that might influence the VA was not included in their analysis. Based on these results, we believed that the intraretinal splitting could be regarded as a manifestation of macular traction. With the aggravation of ERM traction, there will be many changes such as increased parafoveal thickness and central retinal thickness, the presence of stretched retinal cleavage, DRIL, MME, and defective outer retinal layers. A combination of these factors may be responsible for the decrease in the VA.

In the foveal-attached iERMs, there was a possible relationship between the central foveal thickness increase and visual function damage [25, 26]. The MPH is defined by a normal or slightly increased central foveal thickness and a significantly increased parafoveal thickness [27]. The correlations between these parameters and visual function remain controversial. In the present study, although the baseline central foveal point thickness of the v-shaped group was significantly greater than that in the u-shaped group (p = 0.009), they were all within the normal range compared with the fellow healthy eyes (PV = 0.346, and Pu = 0.244, respectively). The multiple linear regression analysis proved that, other than the morphology of foveal pit base, the duration of symptoms (p = 0.011) and central foveal point thickness (p = 0.006) were also significantly associated with the preoperative BCVA after adjusting for age, gender, and other OCT findings. This finding is in agreement with the study conducted by Suzuki et al. [9] who reported that the BCVA in MPHs with a normal foveal pit base thickness was significantly better than that with an increased base thickness. In the contrary, Ku et al. [7] reported that a significant increase in parafoveal thickness could affect VA more than a slight change in central foveal thickness. Based on the theories proposed by Bringmann et al. [19], the contraction induced by ERMs could increase the thickness of the IRL of the parafovea. Then it could further lead to an elevation of the foveal walls. The Müller cells of the foveal walls could transmit the subtle traction to the central fovea. The mechanical forces transmitted to the central outer retina from the inner retina could subsequently cause damage to the photoreceptor, which was not visible on the OCT images. Therefore, we hypothesized that the chronic contraction of the ERM surrounding the fovea would first increase the thickness of the parafoveal layers. When the central fovea is affected, the VA will be significantly decreased.

We found that the macular structure significantly improved in MPHs after surgery. In addition to a significant reduction in the parafoveal thickness (p = 0.002), PIRL thickness (p = 0.003), and PORL thickness (p < 0.001), the stretched lamellar cleavage (43.3%), MME (68.2%), and the DRIL (78.9%) also recovered significantly. However, the central foveal point thickness was thickened after the operation (p < 0.001). These changes could also be observed in the u-shaped and v-shaped groups, respectively. But we found no significant difference in these parameters between baseline and final follow-up in the u-shaped group. Through correlation analysis, we did not find a significant correlation between the central foveal point thickness and postoperative BCVA (p = 0.746). Therefore, although the thickness of the central fovea is thicker than that in baseline, it does not seem to affect the VA.

Although a significant difference in BCVA was found between the two groups at baseline (p = 0.001) and 1 month (p = 0.042) after the operation, this discrepancy disappeared during the final follow-up period (p = 0.213). Our results were concordant with the results reported by Gaudric et al. [1], who classified the MPHs into two groups, with straight or stretched edges, according to their foveal profile. They found that the VA was improved in both groups, and no significant difference was found between the two groups in postoperative VA. These findings emphasized that PPV combined ERM peeling is an effective treatment for symptomatic MPHs. No matter the baseline foveal profile, there was a significant improvement in anatomic and function postoperatively.

This study has some limitations. A major source of limitation is due to its retrospective design. In addition, the number of patients who need to be operated on is restricted because of a relatively lower incidence rate and a stable VA for MPH. Therefore, future prospective studies with large samples are needed to confirm our findings further.

In conclusion, a comparison of MPHs in v-shaped foveal profiles with those of u-shaped profiles revealed significant differences in visual function and retinal structure. The morphology of the foveola base was significantly associated with lower preoperative BCVA in a multivariate linear regression model controlling for other possible causes of reduced BCVA. Therefore, the morphology of the foveola is likely to be clinically used for evaluating the severity of the MPH. However, no matter their initial foveal profiles, PPV combined ERM peeling showed significant structural and visual functional recovery improvement.

All procedures performed in studies involving human participants were adhered to the Helsinki declaration and its lateral amendments. Approval was granted by the ethical review committee of Beijing Tongren Hospital, Capital Medical University. Approval number [TRECKY2020-149]. WRITTEN INFORMED consent was obtained for participation in this study. Informed consent was obtained from all individual participants included in this study. The Ethical Review Committee of Beijing Tongren Hospital, Capital Medical University. Patients signed informed consent regarding publishing their data and photographs.

The authors have no conflicts of interest with regard to the article.

This study was supported by National Key Research and Development Program of China, Grant/Award No. 2017YFA0104103.

Study design, statistical analysis, and drafting and editing: Xiaohan Yang; Data acquisition: Xiaohan Yang and Xijin Wu; Interpretation of data: Xiaohan Yang, Yanping Yu, Ke Zhang, Biying Qi, Xijin Wu, Xinbo Wang, and Wu Liu; Supervision and surgical support: Wu Liu.

All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.

1.
Gaudric
A
,
Aloulou
Y
,
Tadayoni
R
,
Massin
P
.
Macular pseudoholes with lamellar cleavage of their edge remain pseudoholes
.
Am J Ophthalmol
.
2013 Apr
155
4
733
42
, 742.e1–4.
2.
Pierro
L
,
Iuliano
L
,
Marchese
A
,
Arrigo
A
,
Rabiolo
A
,
Bandello
F
.
Reduced vascular perfusion density in idiopathic epiretinal membrane compared to macular pseudohole
.
Int Ophthalmol
.
2019 Dec
39
12
2749
55
.
3.
Klein
BR
,
Hiner
CJ
,
Glaser
BM
,
Murphy
RP
,
Sjaarda
RN
,
Thompson
JT
.
Fundus photographic and fluorescein angiographic characteristics of pseudoholes of the macula in eyes with epiretinal membranes
.
Ophthalmology
.
1995 May
102
5
768
74
.
4.
Sidd
RJ
,
Fine
SL
,
Owens
SL
,
Patz
A
.
Idiopathic preretinal gliosis
.
Am J Ophthalmol
.
1982 Jul
94
1
44
8
.
5.
Margherio
RR
,
Cox
MS
Jr
,
Trese
MT
,
Murphy
PL
,
Johnson
J
,
Minor
LA
.
Removal of epimacular membranes
.
Ophthalmology
.
1985 Aug
92
8
1075
83
.
6.
Toyama
T
,
Roggia
MF
,
Yamaguchi
T
,
Noda
Y
,
Ueta
T
.
The extent of stretched lamellar cleavage and visual acuity in macular pseudoholes
.
Br J Ophthalmol
.
2016 Sep
100
9
1227
31
.
7.
Ku
HC
,
Cho
EH
,
Han
JM
,
Lee
EK
,
Park
YH
.
Angulation of the inner nuclear layer as an indicator of the severity of macular pseudohole
.
Graefes Arch Clin Exp Ophthalmol
.
2021 Jan
259
1
69
79
.
8.
Allen
AW
Jr
,
Gass
JD
.
Contraction of a perifoveal epiretinal membrane simulating a macular hole
.
Am J Ophthalmol
.
1976 Nov
82
5
684
91
.
9.
Suzuki
T
,
Terasaki
H
,
Niwa
T
,
Mori
M
,
Kondo
M
,
Miyake
Y
.
Optical coherence tomography and focal macular electroretinogram in eyes with epiretinal membrane and macular pseudohole
.
Am J Ophthalmol
.
2003 Jul
136
1
62
7
.
10.
Flaxel
CJ
,
Adelman
RA
,
Bailey
ST
,
Fawzi
A
,
Lim
JI
,
Vemulakonda
GA
.
Idiopathic epiretinal membrane and vitreomacular traction preferred practice pattern®
.
Ophthalmology
.
2020 Feb
127
2
145
83
.
11.
Fleissig
E
,
Zur
D
,
Moisseiev
E
,
Keren
S
,
Ohana
O
,
Barak
A
.
Five-year follow-up after epiretinal membrane surgery: a single-center experience
.
Retina
.
2018 Jul
38
7
1415
9
.
12.
González-Saldivar
G
,
Berger
A
,
Wong
D
,
Juncal
V
,
Chow
DR
.
Ectopic inner foveal layer classification scheme predicts visual outcomes after epiretinal membrane surgery
.
Retina
.
2020 Apr
40
4
710
7
.
13.
Zur
D
,
Iglicki
M
,
Feldinger
L
,
Schwartz
S
,
Goldstein
M
,
Loewenstein
A
.
Disorganization of retinal inner layers as a biomarker for idiopathic epiretinal membrane after macular surgery-the DREAM study
.
Am J Ophthalmol
.
2018 Dec
196
129
35
.
14.
Michels
RG
.
Vitreous surgery for macular pucker
.
Am J Ophthalmol
.
1981 Nov
92
5
628
39
.
15.
Kim
JH
,
Kim
YM
,
Chung
EJ
,
Lee
SY
,
Koh
HJ
.
Structural and functional predictors of visual outcome of epiretinal membrane surgery
.
Am J Ophthalmol
.
2012 Jan
153
1
103
10.e1
.
16.
Yang
X
,
Wang
Z
,
Yu
Y
,
Liu
L
,
Qi
B
,
Zhang
K
.
Changes of fixation stability and location after epiretinal membrane surgery
.
Retina
.
2022 May 1
42
5
883
91
.
17.
García-Fernández
M
,
Navarro
JC
,
Sanz
AFV
,
Castaño
CG
.
Long-term evolution of idiopathic lamellar macular holes and macular pseudoholes
.
Can J Ophthalmol
.
2012 Oct
47
5
442
7
.
18.
Schumann
RG
,
Compera
D
,
Schaumberger
MM
,
Wolf
A
,
Fazekas
C
,
Mayer
WJ
.
Epiretinal membrane characteristics correlate with photoreceptor layer defects in lamellar macular holes and macular pseudoholes
.
Retina
.
2015 Apr
35
4
727
35
.
19.
Bringmann
A
,
Unterlauft
JD
,
Barth
T
,
Wiedemann
R
,
Rehak
M
,
Wiedemann
P
.
Müller cells and astrocytes in tractional macular disorders
.
Prog Retin Eye Res
.
2022 Jan
86
100977
.
20.
Bringmann
A
,
Unterlauft
JD
,
Wiedemann
R
,
Rehak
M
,
Wiedemann
P
.
Morphology of partial-thickness macular defects: presumed roles of Müller cells and tissue layer interfaces of low mechanical stability
.
Int J Retina Vitreous
.
2020 Jul 6
6
28
.
21.
Hubschman
JP
,
Govetto
A
,
Spaide
RF
,
Schumann
R
,
Steel
D
,
Figueroa
MS
.
Optical coherence tomography-based consensus definition for lamellar macular hole
.
Br J Ophthalmol
.
2020 Dec
104
12
1741
7
.
22.
Govetto
A
,
Bhavsar
KV
,
Virgili
G
,
Gerber
MJ
,
Freund
KB
,
Curcio
CA
.
Tractional abnormalities of the central foveal bouquet in epiretinal membranes: clinical spectrum and pathophysiological perspectives
.
Am J Ophthalmol
.
2017 Dec
184
167
80
.
23.
Govetto
A
,
Hubschman
JP
,
Sarraf
D
,
Figueroa
MS
,
Bottoni
F
,
dell’Omo
R
.
The role of Müller cells in tractional macular disorders: an optical coherence tomography study and physical model of mechanical force transmission
.
Br J Ophthalmol
.
2020 Apr
104
4
466
72
.
24.
Duker
JS
,
Kaiser
PK
,
Binder
S
,
de Smet
MD
,
Gaudric
A
,
Reichel
E
.
The International Vitreomacular Traction Study Group classification of vitreomacular adhesion, traction, and macular hole
.
Ophthalmology
.
2013 Dec
120
12
2611
9
.
25.
Kinoshita
T
,
Imaizumi
H
,
Miyamoto
H
,
Katome
T
,
Semba
K
,
Mitamura
Y
.
Two-year results of metamorphopsia, visual acuity, and optical coherence tomographic parameters after epiretinal membrane surgery
.
Graefes Arch Clin Exp Ophthalmol
.
2016 Jun
254
6
1041
9
.
26.
Kinoshita
T
,
Imaizumi
H
,
Okushiba
U
,
Miyamoto
H
,
Ogino
T
,
Mitamura
Y
.
Time course of changes in metamorphopsia, visual acuity, and OCT parameters after successful epiretinal membrane surgery
.
Invest Ophthalmol Vis Sci
.
2012 Jun 14
53
7
3592
7
.
27.
Haouchine
B
,
Massin
P
,
Tadayoni
R
,
Erginay
A
,
Gaudric
A
.
Diagnosis of macular pseudoholes and lamellar macular holes by optical coherence tomography
.
Am J Ophthalmol
.
2004 Nov
138
5
732
9
.