Korean J Ophthalmol 2018;32(2):140-146

ht tps://doi.org/10.33 41/k jo.2017.0 085

pISSN: 1011-8942 eISSN: 2092-9382

Original Article

Visual Recovery after Macular Hole Surgery and Related Prognostic

Factors
Soo Han Kim1, Hong Kyu Kim2, Jong Yun Yang3, Sung Chul Lee2, Sung Soo Kim2
1
Department of Ophthalmology, Yonsei University Wonju College of Medicine, Wonju, Korea
2
Department of Ophthalmology, Institute of Vision Research, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
3
Siloam Eye Hospital, Seoul, Korea

Purpose: To describe the visual recovery and prognostic factors after macular hole surgery.
Methods: A retrospective chart review was conducted. Charts of patients with idiopathic macular holes who un-
derwent surgery by a single surgeon at Severance Hospital between January 1, 2013 and July 31, 2015 were
reviewed. The best-corrected visual acuity (BCVA) score was recorded preoperatively and at 1 day and 1, 3,
6, 9, and 12 months after surgery. The variables of age, sex, macular hole size, basal hole diameter, choroidal
thickness, and axial length were also noted.
Results: Twenty-six eyes of 26 patients were evaluated. Twenty-five patients (96.2%) showed successful macu-
lar hole closure after the primary operation. The BCVA stabilized 6 months postoperatively. A large basal hole
diameter (p = 0.006) and thin choroid (p = 0.005) were related to poor visual outcomes. Poor preoperative
BCVA (p < 0.001) and a thick choroid (p = 0.020) were associated with greater improvement in BCVA after
surgery.
Conclusions: Visual acuity stabilized by 6 months after macular hole surgery. Choroidal thickness was a pro-
tective factor for final BCVA and visual improvement after the operation.

Key Words: Choroid, Retinal perforations, Visual acuity, Vitrectomy

Optical coherence tomography (OCT) technology has led staining with indocyanine green dye, the primary success
to a deeper understanding of the pathophysiology of macu- rates of MH surgeries have steadily increased [2-4]. Some
lar holes (MHs) [1]. With advancements in surgical tech- efforts have been made to determine the prognostic factors
niques, from gas tamponade to internal limiting membrane of favorable MH surgery outcomes [5-7]. To date, the size
and stage of the MH, duration of symptoms, and preopera-
tive visual acuity have been reported as preoperative fac-
Received: July 11, 2017 Accepted: September 4, 2017
tors [5]; however, recovery of the macular contour, the ex-
Corresponding Author: Sung Soo Kim, MD, PhD. Department of ternal limiting membrane (ELM), and the ellipsoid zone
Ophthalmology, Institute of Vision Research, Severance Hospital, Yonsei
University College of Medicine, #50-1 Yonsei-ro, Seodaemun-gu, Seoul 03722, are known to affect recovery of vision after surgery [6,7].
Korea. Tel: 82-2-2228-3570, Fax: 82-2-312-054, E-mail: [email protected] It has been reported that MH patients have a thin cho-
This study was presented as e-poster at Retina World Congress on Febru- roid and decreased choroidal perfusion [8,9], but it remains
ary 25, 2017 in Fort Lauderdale, FL, USA. unknown whether choroidal thickness or perfusion affect

© 2018 The Korean Ophthalmological Society

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses
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 SH Kim, et al. Recovery and Prognosis after Macular Hole Surgery

the surgical outcome. Additionally, there have been few

reports about the time required for visual recovery after
MH repair. Thus, in this study, we investigated the time to
visual recovery after MH surgery and the related prognos-
tic factors, including choroidal thickness.

Materials and Methods Fig. 1. Macular hole parameters measured in optical coherence
tomography scans. a = hole size; b = basal hole size; c = choroidal
The institutional review board of Yonsei University Col- thickness.
lege of Medicine approved this study (4-2016-1033), which
adhered to the tenets of the Declaration of Helsinki. All single observer (KSH) with enhanced depth imaging, us-
patients provided written informed consent before any ing a method previously described by Boonarpha et al. [10],
procedure was performed. A retrospective chart review as the distance from the hyper-reflective line under the ret-
was performed for all patients with idiopathic MHs, who inal pigment epithelium to the choroid-sclera interface.
underwent surgery by a single surgeon (SSK) at Severance Recovery of the ELM and the ellipsoid zone was moni-
Hospital, Seoul, Korea, between January 1, 2013 and July tored with serial OCT scans during follow-up. Axial length
31, 2015. Patients were excluded if they were lost to fol- was measured preoperatively with the IOL-Master 500
low-up within one year after surgery, developed a second- (Carl Zeiss, Dublin, CA, USA).
ary MH, had an axial length exceeding 26.5 mm, or under- Changes in BCVA were analyzed by repeated measures
went previous vitrectomy. analysis of variance. Multivariate linear regression was
All patients underwent a thorough ophthalmic evalua- performed to determine prognostic factors after MH re-
tion prior to surgery, including assessment of the best-cor- pair. Fisher’s exact test and the Mann-Whitney U-test were
rected visual acuity (BCVA) and a fundus examination used to compare characteristics and outcomes between the
(Spectralis OCT; Heidelberg Engineering, Heidelberg, ELM and ellipsoid zone recovery. Reliability analysis was
Germany). Patients with a full thickness MH were advised used to assess the reproducibility of subfoveal choroidal
to undergo surgery. Surgery was performed using a stan- thickness measurements. Statistical analysis was per-
dard 3-port, 23-gauge pars plana vitrectomy. When a cata- formed using IBM SPSS ver. 21.0 (IBM Corp., Armonk,
ract was present, a combined phacovitrectomy was per- NY, USA). A p-value less than 0.05 was considered statis-
for med. To remove tangential t raction, epiretinal tically significant.
membranectomy was performed when a premacular mem-
brane was present. When there was no visible premacular
membrane, the internal limiting membrane was peeled Results
with indocyanine green staining. After removing tangen-
tial traction around the MH, air-fluid exchange was per- Twenty-six eyes of 26 patients were included in this
formed, followed by 10% to 14% C3F8 tamponade. Patients study. Demographic factors and initial findings are listed
were instructed to remain in a prone position for about one in Table 1. The mean age of the patients was 61.6 years,
week after the surgery. and 73.1% (19 patients) were female. The mean BCVA was
Patient age, sex, and involved eye were noted, and the 0.981 in logarithm of the minimum angle of resolution
BCVA was measured before surgery and at 1 day and 1, 3, scale prior to the operation. Visual acuity decreased to a
6, 9, and 12 months after the operation. Size of the MH, mean of 3.077 1 day after the operation, due to gas filling.
basal hole diameter, and subfoveal choroidal thickness All 26 patients completed all routine follow-up visits. The
were measured using the caliper function in the Heidelberg mean BCVA values at 1, 3, 6, 9, and 12 months were 0.797,
software (Fig. 1). The basal hole diameter of the MH was 0.592, 0.495, 0.496, and 0.427, respectively. When these
measured as the linear length of retinal detachment. Sub- BCVA values were compared with the final (12-month
foveal choroidal thickness was measured three times by a postoperative) BCVA, preoperative vision and 1-day post-

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operative vision were found to be significantly different ( p tive BCVA ( p = 0.543), preoperative choroidal thickness ( p
< 0.001). Differences in BCVA were still significant at 1 = 0.935), 12-month postoperative choroidal thickness ( p =
and 3 months after the operation (1 month, p = 0.034; 3 0.394), or preoperative axial length (p = 0.687).
months, p = 0.040). BCVA did not show improvements be-
yond 6 months after surgery (6 months, p = 1.000; 9
Table 2. Preoperative factors affecting final visual acuity and
months, p = 1.000) (Fig. 2). changes in visual acuity
Measurement of subfoveal choroidal thickness showed B coefficient p-value
good reliability, with an intraclass correlation coefficient Final visual acuity
of 0.992 ( p < 0.001). Postoperative choroidal thickness Sex 0.021 0.903
measured at 3, 6, 9, and 12 months was 227.3 (n = 22), 218.7 Age -0.162 0.835
(n = 26), 214.2 (n = 25), and 223.6 (n = 23), respectively. Preoperative BCVA 0.173 0.371
Thinning of the choroid was noted in all postoperative
Hole size -0.427 0.084
thickness measurements compared to the preoperative
Basal hole size 0.471 0.006
choroidal thickness measurement (3 months, p = 0.001; 6
Choroidal thickness -0.475 0.005
months, p = 0.004; 9 months, p < 0.001; 12 months, p =
Axial length 0.062 0.707
0.001). Changes in choroidal thickness did not correlate
Changes in visual acuity
with preoperative BCVA ( p = 0.427), 12-month postopera-
Sex 0.000 0.999
Age 0.040 0.751
Table 1. Demographic characteristics and preoperative findings Preoperative BCVA 0.816 <0.001
Characteristics Value Hole size -0.011 0.936
Age (yr) 61.6 ± 9.9 Basal hole size -0.269 0.057
Male : female 7 (26.9) : 19 (73.1) Choroidal thickness 0.299 0.020
Laterality (right : left) 14 (53.8) : 12 (46.2) Axial length 0.006 0.961
Preoperative vision (logMAR) 0.981 ± 0.374 BCVA = best-corrected visual acuity.
Hole size (μm) 427.3 ± 201.5
Basal hole size (μm) 821.3 ± 344.0 1.2
R2 = 0.2296
Choroidal thickness (μm) 229.7 ± 66.4
12 mon BCVA ( logMAR)

1
Axial length (mm) 23.5 ± 0.9 0.8

Values are presented as mean ± standard deviation or number (%). 0.6

logMAR = logarithm of the minimum angle of resolution. 0.4

0.2

** 0
0 50 100 150 200 250 300 350 400 450
3.5
A Preoperaive subfoeval choroidal thickness
3.0

2.5
* 1.1
Changes in BCVA ( logMAR)

2.0 R2 = 0.2293
0.8
1.5
0.5
1.0
0.2
0.5
-0.1
0
ive ate om om om om m -0.4
at di
1m 3m 6m 9m mo
per mi 12 0 50 100 150 200 250 300 350 400 450
eo Im
Pr B Preoperaive subfoeval choroidal thickness
BCVA (logMAR)

Fig. 2. Changes in best-corrected visual acuity (BCVA) after Fig. 3. Analysis of correlation of choroidal thickness with (A)
macular hole repair. logMAR = logarithm of the minimum angle final best-corrected visual acuity (BCVA) and (B) changes in
of resolution. *p < 0.05, **p < 0.001. BCVA. logMAR = logarithm of the minimum angle of resolution.

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 SH Kim, et al. Recovery and Prognosis after Macular Hole Surgery

To evaluate the factors affecting final BCVA, the vari- after surgery. No factors were significantly related to a dif-
ables of sex, age, preoperative BCVA, MH size, basal hole ference in ELM recovery. The ellipsoid zone recovered in
diameter, choroidal thickness, and axial length were evalu- 19 (73.1%) patients, by a median time of 3 months (1st to
ated using multivariate linear regression analysis. This re- 3rd quartile, 1 to 8.0 months) after the operation. Patients
vealed that the final visual acuity was affected by basal with a recovered ellipsoid zone had better preoperative
hole diameter and choroidal thickness (R 2 = 0.450, p = BCVA, smaller basal hole diameter, and shorter axial
0.001). A larger basal hole diameter was associated with a length. Although the final BCVA was better in the ellip-
poor final BCVA (95% confidence interval [CI], 0.000 to soid zone-recovered group, the difference was not statisti-
0.001). A greater preoperative choroidal thickness provided cally significant (Table 3).
a protective effect, as patients with a thick choroid had a
better final BCVA (95% CI, 0.000 to 0.001). When these
factors were evaluated against changes in BCVA, preoper- Discussion
ative BCVA and choroidal thickness were significantly as-
sociated (R 2 = 0.680, p < 0.001). Patients with poor preop- In this study, we investigated the time to visual recovery
erative BCVA showed greater visual recovery (95% CI, after MH surgery and the related prognostic factors, in-
0.521 to 0.974). Choroidal thickness also had a positive re- cluding choroidal thickness. Previously, the closure rate
lationship with visual acuity changes (95% CI, 0.000 to after MH surgery was 58%, but advancements in surgical
0.003) (Table 2 and Fig. 3A, 3B). techniques and devices have led to an improvement in the
Twenty-four (92.3%) patients showed ELM recovery at a closure rate to 89% to 100% [4,11,12]. In this study, we
median of 1 month (1st to 3rd quartile, 1 to 4.50 months) were able to achieve closure in 25 (96.2%) of 26 cases, us-

Table 3. Factors affecting ELM and ellipsoid zone recovery

Recovered Non-recovered p-value
ELM 24 (92.3) 2 (7.7)
Male : female 7 : 17 0: 2 1.000
Age 63.50 (59.50−67.75) 67, 70 0.698
Preoperative BCVA 0.912 (0.730−1.301) 1.000, 1.602 0.262
Final BCVA 0.398 (0.242−0.523) 0.301, 0.824 0.726
Changes in BCVA 0.563 (0.242−0.828) 0.700, 0.778 0.394
Hole size 404.0 (258.0−577.5) 291, 470 0.800
Basal hole size 824.0 (576.0−1024.8) 896, 941 0.498
Choroidal thickness 244.0 (188.3−282.3) 245, 128 0.443
Axial length 23.3 (22.9−24.0) 24.37, 24.39 0.055
Ellipsoid zone 19 (73.1) 7 (26.9)
Male : female 5 : 14 2:5 1.000
Age 63.0 (59.0−68.0) 67.0 (61.0−70.0) 0.225
Preoperative BCVA 0.824 (0.699−1.000) 1.301 (1.000−1.602) 0.005
Final BCVA 0.398 (0.222−0.523) 0.523 (0.301−0.824) 0.267
Changes in BCVA 0.523 (0.176−0.699) 0.778 (0.602−1.079) 0.042
Hole size 381.0 (209.0−446.0) 470.0 (395.0−808.0) 0.057
Basal hole size 815.0 (526.0−862.0) 1018.0 (941.0−1397.0) 0.001
Choroidal thickness 239.0 (183.0−285.0) 245.0 (134.0−256.0) 1.000
Axial length 23.2 (22.5−24.0) 24.0 (23.7−24.4) 0.014
Values are presented as number (%), number, or median (25 percentile–75 percentile). Actual records of two patient is presented in non-
recovered ELM group.
ELM = external limiting membrane; BCVA = best-corrected visual acuity.

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Korean J Ophthalmol Vol.32, No.2, 2018

ing a standard 23-gauge vitrectomy system. The single pa- circulation during compression by gas tamponade and can
tient with incomplete closure had a 395-µm sized MH, affect MH healing. If so, prolonged prone positioning of
with a 1,397-µm basal hole diameter. He underwent a sec- patients after surgery might have a hazardous effect on
ond operation 1 month after the first, during which the choroidal circulation. Further studies on the changes in
MH was successfully closed. choroidal circulation during the tamponade period are
Shinoda et al. [13] reported visual recovery at 3 months needed.
after MH surgery in a 25-gauge vitrectomy group and at 9 Choroidal thickness has been reported to decrease with
months after surgery in a 20-gauge vitrectomy group. Less age and with longer axial length [19,20]. It is also known
trauma to the ocular surface, a shorter operation time, and that there is a diurnal variation of approximately 30 μm in
a reduced amount of irrigation fluid were considered to be choroidal thickness, and that the thickness is also affected
reasons for the shorter time to visual recovery in the by changes in blood pressure and drugs, such as sildenafil
25-gauge vitrectomy group. In this study, we performed and steroids [21-23]. In this study, patients with an axial
23-gauge vitrectomy, and vision stabilized by 6 months af- length exceeding 26.5 mm were excluded. However, fur-
ter the operation. Leonard et al. [14] and Purtskhvanidze et ther investigation of the relationship between choroidal
al. [15] reported continuous visual improvement after MH thickness and visual prognosis in myopic MH patients is
surgery after following patients for up to 96 months. We necessary. Choroidal thickness and choroidal circulation
observed continuous elevation in visual acuity for 6 are not synonymous. Sogawa et al. [24] reported that cho-
months after the operation, and recovery of ELM and the roidal blood flow was not correlated with choroidal thick-
ellipsoid zone was still observed at 35 and 38 months after ness, as measured by laser Doppler, but their study sub-
surgery. However, changes in visual acuity were not statis- jects were young, healthy, and few in number.
tically significant. ELM and ellipsoid zone recovery also affect visual re-
In 1986, Morgan and Schatz [16] hypothesized that the covery after MH surgery [6,7]. We compared multiple fac-
first step in the development of a MH is choroidal vascular tors of the ELM and ellipsoid zone-recovered groups with
change. They suggested that the majority of patients with those of the unrecovered group, but we found no factors
an MH had cardiovascular disease, and decreased subfove- affecting ELM recovery. Given that only two patients
al choroidal circulation was noticed during fluorescein an- (7.7%) had unrecovered ELM, the small sample size might
giography. Allen et al. [17] induced MHs in monkeys with underlie the lack of statistically significant differences. In
an Nd-YAG laser, which resulted in a choriocapillaris per- the case of ellipsoid zone recovery, patients with a larger
fusion disorder. Histologically, the choriocapillaris was re- basal hole diameter, poor initial visual acuity, and greater
placed with fibroblasts and connective tissue. Other reports axial length had a poor recovery rate. The change in visual
have also suggested that choroidal thickness is decreased acuity was found to be greater in the group without recov-
in idiopathic MH patients compared to a control group ery of the ellipsoid zone, but this was due to the differenc-
when measured using OCT [8,9]. Aras et al. [18] have re- es in preoperative visual acuity. Landa et al. [25] asserted
ported that patients with stage 4 and stage 1a MHs had re- that recovery of ELM is essential for ellipsoid zone recov-
duced subfoveal choroid circulation compared to controls, ery. We also analyzed OCT data and found that ellipsoid
as determined using a scanning laser Doppler flowmeter. It zone recovery was seen only after the ELM was restored.
is suspected that decreased choroidal circulation and a There are several limitations to this study. First, we did
thinner choroid can cause macular hypoperfusion, and that not measure the choroidal circulation, and further investi-
deficits in several protective factors leave the macula vul- gation is needed to determine whether the choroidal circu-
nerable to various types of damage [16,18]. In this study, lation actually affects prognosis. If so, it will be necessary
choroidal thickness was not only related to the develop- to confirm whether the postoperative course is different in
ment of an MH, but final visual acuity and visual acuity cases where the choroidal circulation is increased. Second-
change were also closely related. Choroidal thickness ly, because this was a single center study of only Korean
showed a protective effect on BCVA and on the degree of patients, the results might not be generalizable to different
visual improvement obtained. We hypothesize that a thin- ethnicities. In addition, there are many patients who were
ner choroid can cause additional decreases in choroidal not assessed for the duration of symptoms; thus, future

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 SH Kim, et al. Recovery and Prognosis after Macular Hole Surgery

studies will need to consider various parameters, including foveal cone outer segment tips line defect and visual acuity
duration of symptoms and choroidal thickness. after macular hole closure. Ophthalmology 2012;119:1438-46.
In conclusion, visual acuity stabilized after 6 months in 8. Reibaldi M, Boscia F, Avitabile T, et al. Enhanced depth
MH patients who underwent 23-gauge vitrectomy. Final imaging optical coherence tomography of the choroid in id-
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diameter. Greater choroidal thickness was a protective Am J Ophthalmol 2011;151:112-7.
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greater axial length. Based on these results, we were able of choroidal thickness measurements using enhanced depth
to identify the factors that influence visual recovery after imaging optical coherence tomography. Int J Ophthalmol
MH surgery. This information will allow for better stratifi- 2015;8:484-91.
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Conflict of Interest domized trial: outcomes of SF6 versus C3F8 in macular
hole surgery. Can J Ophthalmol 2015;50:95-100.
No potential conflict of interest relevant to this article 13. Shinoda H, Shinoda K, Satofuka S, et al. Visual recovery
was reported. after vitrectomy for macular hole using 25-gauge instru-
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