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International Ophthalmology

, Volume 34, Issue 3, pp 493–499 | Cite as

Spectral domain optical coherence tomography study of macular microhole morphology and its correlation with vitreomacular interface abnormalities

  • Batmanabane Prakash Vaishnavi
  • Unnikrishnan Nair
  • Manoj Soman
  • K. G. R. Nair
Original Paper
  • 189 Downloads

Abstract

To describe the demographic, clinical and optical coherence tomography (OCT) characteristics of macular microholes and to determine if the size or character of the microholes has any correlation with vitreomacular interface abnormalities. Case records of 46 eyes of 39 consecutive patients with diagnosed macular microholes were reviewed as a non-interventional retrospective case study. Demographic and clinical features were noted from the detailed case records. Spectral domain OCT images were analysed for microhole and retinal characteristics. SPSS 16.0 was used for statistical analysis. Main outcome measure was the presence of vitreomacular interface abnormalities in large and small macular microholes. Of 39 patients, 21 were male and 18 were female. Most of these patients (56.4 %) presented with visual complaints. Clinically, the commonest feature was a ‘red spot’ at the fovea on indirect ophthalmoscopy (25 of 44 eyes; 54.3 %). Mean logMAR vision was 0.117 (±SD 0.21). 34 (76.08 %) eyes exhibited a photoreceptor loss, 38 eyes (82.6 %) had lamellar tissue defects involving layers posterior to the outer nuclear layer. The difference between means of the groups with and without vitreomacular interface abnormalities was analysed using the unpaired t test. The presence of vitreomacular interface abnormalities was significantly associated with the size of the microhole, with larger microholes being more likely to have vitreomacular interface abnormalities than smaller ones (p < 0.05). We concluded that there was a positive correlation between the size of the microhole and the presence of vitreomacular interface abnormalities. Visual acuity had no correlation with the size of the microhole; functional vision was generally well preserved in the affected eyes.

Keywords

Macular microhole SD-OCT Vitreomacular interface abnormalities 

Introduction

Macular microholes, originally described by Cairns and McCombe [1], are retinal tissue defects typically <150 μm in size, involving the central macular area either uniocularly or binocularly and are clinically non-progressive [2]. While trauma and abnormalities of vitreoretinal interaction are known inciting factors [3], the definitive etiological factors of this retinal condition are still unknown. The diagnosis of macular microholes is often incidental in asymptomatic patients, and less commonly, patients present with a decrease in visual acuity. Although afflicted patients are traditionally thought to have few complaints, studies have shown that they may in fact present with a variety of symptoms like scotomas and metamorphopsia [2], indicating that not all microholes are benign. A study by Gella et al. [4] using investigative microperimetry showed that macular microholes are definitely associated with a decrease in retinal sensitivity although this study also looked at microhole variants. Until recently, much speculation regarding the precise anatomical location of these defects existed, as pinpointing the depth of the microhole was difficult. Currently, spectral domain optical coherence tomography (SD-OCT), which has considerably aided the understanding of various vitreoretinal interactions [5] and retinal conditions [6] which were previously unexplained, provides high-definition images of the retina similar to histopathological representation, and has dispelled much of the enigma surrounding microholes. SD-OCT generates real-time two-dimensional retinal images by assembling multiple cross-sectional z-axis scans, taken by examining a predesignated portion of the retina. Several investigators have previously studied microholes using SD-OCT [1, 2, 3, 4] and one such study suggested that an elevated foveal photoreceptor layer (PRL) associated with the perifoveal posterior vitreous detachment (PVD) could predispose macular microhole formation [7]. It has already been mentioned that microholes are definitely associated with microperimetric abnormalities in accordance with the size of the defect [4]. Our study researched the clinical and SD-OCT characteristics of retinas harbouring microholes, and aimed to see if there was a correlation between defect size and vitreomacular interface abnormalities (VMIAs), indirectly affecting vision, which would give an insight into the pathogenesis of the condition.

Methods

This study, approved by the Institute Study Review Board, was a retrospective observational review of case records of patients with macular microholes who presented to us between January 2009 and January 2012. Parameters assessed from each patient’s ophthalmological case record were details of the presenting symptoms, previous ocular history and past medical history. All patients had documented best-corrected visual acuity using the Snellen’s chart, designated as the Snellen equivalent of the smallest line read with no error. Vision was converted into respective logMAR equivalents for data analysis. Each patient had received a complete ocular examination including slit-lamp biomicroscopy, intraocular pressure measurement using Goldmann’s applanation tonometry, and dilated fundus evaluation using slit-lamp biomicroscopy and a 78 D Volk and indirect ophthalmoscopy with a 20 D Volk lens (Fig. 1a, b). Anterior and posterior segment details were recorded for each patient. Retinal features were diagrammatically represented using standard colour coding. The presence of a complete PVD was diagnosed if a Weiss ring was present on indirect ophthalmoscopy and confirmed with SD-OCT. SD-OCT (Carl Zeiss, Meditec, Inc., CA, USA) characteristics of 46 involved eyes were noted from retrieved retinal scans of the respective patients (Fig. 1c). Signal strength for the images analysed were at least 6/10. Retinal pigment epithelium (RPE) features, and PRL characteristics such as the PRL thickness were documented. ‘Rarefaction’ was defined as reduced intensity of the reflectance pattern of the retinal layer being studied while a particular layer was deemed ‘discontinuous’ when there was a complete absence of any reflectance from that retinal layer in question. Position of the macular microhole (whether central or paracentral, outer lamellar or inner lamellar), integrity of the external limiting membrane (ELM) and the inner segment-outer segment layer were also recorded. Central microholes were those present sub-foveally while paracentral microholes constituted those not falling under this category. Outer lamellar microholes were those with defects involving the layers posterior to the ELM. High-definition images of the 5-line raster scans were used for measuring the microholes. We measured the optically reflection-free space within the retinal tissue corresponding to tissue loss using the calliper tool of the SD-OCT Carl Zeiss software. The length, breadth and height of the microhole were noted by a single observer (VP). VMIAs were defined in accordance with described features in OCT by previous investigators [8, 9]. VMIAs were considered present if there was partial PVD with vitreous adherence at the macula but elevated off other sites on the macular surface as detected on the macular cube scans (Fig. 1d) or the presence of epiretinal membranes or vitreomacular traction. An epiretinal membrane was noted as a thin, distinct hyper-reflective layer seen on the inner retinal surface, which may be associated with folds of the internal limiting membrane. If the eye had none of these characteristics, it was categorised as no VMIA. These characteristics were studied using the thickness analysis option of the macular cube scan which scans 512 vertical sections and 128 horizontal sections at 5-μm cuts, repeated three times for reliability. This way, we were able to scrutinise the vitreomacular interface at the region of the microhole and the surrounding area for at least 6 mm around the foveal centre.
Fig. 1

a, b Right and left fundus images of a patient presenting with blurred vision. The fovea of the left eye appeared to have a ‘red spot’ (black arrow) which on SD-OCT turned out to be a microhole. c SD-OCT of a central macular microhole. Note the rarefaction of the RPE under the defect and the altered foveal contour. d Another SD-OCT of a central macular microhole with vitreomacular adhesion visible. The external limiting membrane is discontinuous. e Slit-like microhole included in group A. The external limiting membrane has not been breached. f Cylindrical-shaped macular microhole included in Group B. Of interest is the vitreomacular adhesion and the photoreceptor rarefaction immediately adjacent to the right of the microhole

We used Pearson’s correlation coefficient to assess correlation of area and volume of the retinal microhole with logMAR vision. For this purpose we excluded eyes with other causes of defective vision such as cataract or macular scar (43 eyes) from analysis. We grouped the microhole defects based on dimensions—slit-like defects or defects with all dimensions <80 μm (mean dimension of all 46 microholes was 79.33 ± 15.29 μm) as Group A (Fig. 1e) and those with larger dimensions as Group B (Fig. 1f). Each group was further sub-classified, based on the presence or absence of VMIAs for analysis. A p-value of <0.05 % was considered statistically significant. Unpaired t-test was used for significance of difference between means of groups with and without VMIA. Statistical analysis was performed using SPSS version 16.0 software package (SPSS, Chicago, IL, USA).

Results

There were 39 eligible patients (21 male, 18 female) with macular microholes. Of these, seven had bilateral microholes, yielding 46 affected ocular units for analysis. Of the 39 patients who were included in the study, only eight were <40 years of age (mean 50.25 years, range 15–75 years). Only 11 (28.20 %) were asymptomatic and most patients (56.4 %) presented with visual complaints—four (10.25 %) patients had blurred vision while two (5.12 %) complained of missing letters while reading. The mean duration of visual complaints was 19.44 months (range 1 week to 6 years). Six patients (15.38 %) were hypertensive and four (10.25 %) were diagnosed diabetics, receiving treatment for a mean duration of 76.5 months and 60 months, respectively. Only one patient (2.56 %) had an abnormal lipid profile and one had been diagnosed with coronary artery disease. Of the 46 eyes, eight (17.4 %) had undergone surgery for cataracts with intraocular lens (IOL) implantation. One patient gave a history of trivial trauma to the eye preceding symptoms. Mean logMAR vision was 0.117 (±SD 0.21). Of the 46 involved eyes, 29 had a vision of 6/6, 16 had a vision of 6/9–6/18 and only one eye had a vision <6/18. All 39 patients had a follow-up of >6 months (range 6−19.5 months, average 11.67 ± 3.63 months) and the vision in the involved eyes during this period and at last follow-up remained unchanged. Clinically, the commonest feature was a ‘red spot’ at the fovea on ophthalmoscopy (25 of 46 eyes; 52.13 %). A lamellar defect was suspected in eight eyes (17.4 %) while foveal reflex was dull in eight eyes. The indirect ophthalmoscopic findings are summarised in Table 1. Of the four patients who were diabetic only one had features of mild non-proliferative diabetic retinopathy, while the rest had no diabetic changes in the fundus. All the hypertensive patients had grade 1 hypertensive retinopathy clinically.
Table 1

Clinical fundus characteristics on posterior segment examination with 20 D indirect ophthalmoscopy in 46 eyes

Clinical characteristic

Number (%)

Red spot

24 (52.13)

Indistinct foveal reflex

8 (17.39)

Lamellar defect

4 (8.69)

Clinically noticeable PVD

2 (4.34)

Lattice

2 (4.34)

Other co-existent features

 Grade 1 hypertensive retinopathy

6 (13.03)

 Drusen

4 (8.68)

 Peripheral chorioretinal atrophic patch

2 (4.34)

 Mild non-proliferative diabetic retinopathy

1 (2.17)

Some eyes had more than one fundus abnormality

SD-OCT characteristics

The various morphological characteristics of the studied microholes are listed in Table 2. The RPE and PRL were also evaluated for anatomical variations associated with the retinal microhole.
Table 2

Microhole characteristics on SD-OCT

Microhole characteristic

Number

Defect shape

Group Aa

29 (63.04 %)

Group Bb

17 (36.95 %)

Defect position

Central

36 (78.2 %)

Paracentral

10 (21.73 %)

Average horizontal diameter of defect (±SD)

90.35 ± 34.08 μm

Average vertical diameter of defect (±SD)

81.15 ± 31.83 μm

Average height of defect (±SD)

57.62 ± 28.78 μm

Mean logMAR visual acuity (±SEM)

0.117 ± 0.03

Mean defect area (±SD)

259.75 (±151.01) μm2

Mean defect volume (±SD)

15,873.13 (±13,717.75) μm3

Area and logMAR (Pearsons)

r = 0.0917

2-tailed p-value 0.39

95 % CI 0.117–0.293

Volume and logMAR (Pearsons)

r = 0.0026

2-tailed p-value 0.98

95 % CI 0.291–0.295

Difference between means of presence or absence of VMIAs and computed area of microhole defect

4876.37 μm2

(95 % CI 13.92–9,738.82 μm2)

p = 0.05 (unpaired t test)

Difference between means of presence or absence of VMIAs and computed volume of microhole defect

466,213.99 μm3

(95 % CI 35,628.16–896,799.82 μm3)

p = 0.03 (unpaired t test)

Comparison of means of small versus large microhole defect volumes and presence versus absence of VMIAs

p = 0.0488 (one-way ANOVA)

Kruskal−Wallis test p < 0.0001

(Kruskal−Wallis statistic = 26.03—corrected for ties)

aGroup A comprised microholes which were slit-like with no dimension being >80 μm

bGroup B comprised larger microholes with irregular walls, or non-parallel sides and at least one dimension >80 μm

The average thickness of the central fovea of the involved eyes was 170.84 μm (SD ± 21.02 μm). The mean thickness of the PRL was 61.10 μm (SD ± 7.81 μm) and there was no statistical difference between the PRL thickness of involved and uninvolved eyes (p = 0.81, 95 % CI 5.95–4.75) of patients who had unilateral microholes (n = 39). Thirty-four (76.08 %) eyes exhibited a focal PRL loss, 12 eyes (26.08 %) showed a rarefaction of the PRL in areas adjacent to the microhole. Eight eyes (17.38 %) showed a discontinuity in the ELM; four of these eyes were associated with VMIAs. The two sided p-value by Fisher’s exact test was 0.712 when comparing eyes with and without VMIAs and the presence or absence of ELM defects, indicating that there was no significant association between the two characteristics. Of the 46 eyes, 38 eyes (82.6 %) had outer lamellar defects and eight eyes (17.38 %) had inner lamellar defects. There was no statistically significant difference in the mean PRL thickness between eyes with and without VMIAs (p = 0.86, 95 % CI 5.12–3.95). Epiretinal membranes were noted in two eyes and foveal contour alterations seen in three (6.52 %). The other SD-OCT characteristics are summarised in Table 3.
Table 3

SD-OCT characteristics of the retina adjacent to the macular microholes in the involved eyes

Characteristic

Values

RPE rarefaction (%)

13 (28.26 %)

RPE discontinuity (%)

9 (19.55 %)

Drusen

8 (16.6 %)

Mean PRL thickness

61.10 μm (SD ± 7.81 μm)

16 involved eyes did not have any appreciable abnormality of the RPE. Three eyes had more than one feature

Out of 46 eyes, 17 (37 %) had defects with the horizontal dimension of the lamellar defect being the greatest while 19 (41.3 %) had the vertical dimension as the greatest. VMIAs were apparent in a total of 26 eyes (56.5 %). The difference between means using the unpaired t-test between the presence or absence of VMIAs and the area of the microhole defect yielded a two-tailed p-value of 0.05 (statistically significant). A similar test with the volume of the microhole defect yielded a p-value of 0.03, also statistically significant.

In the groups based on size of the microhole defect, there were 29 eyes in group A and 17 in group B. There was no statistically significant difference in the mean visual acuities between the eyes in both groups (p = 0.89). Seventeen and nine eyes in Group A and B, respectively, were associated with VMIAs, and when comparing the means of the microhole volumes of each group with and without VMIAs, we found a statistically significant difference between them. Dunn’s multiple comparisons test showed that the mean rank difference between eyes with VMIAs in Group A and B yielded a p-value of <0.001.

Optical coherence tomography taken at the final follow-up visit showed that the microhole dimensions remained within 10 μm of the measurements taken at the first visit in all patients. Only three patients showed changes in the vitreomacular interaction, seen as a decrease in the area of vitreous adhesion at the macula but none of the three proceeding to vitreomacular traction.

Discussion

To the best of our knowledge, this study of 46 macular microholes is the largest case series described in literature to date. We were able to definitively identify an association between the size of the microhole defect and the presence of VMIAs. Vision in eyes with microholes is generally believed to be good [3] and stable over follow-up [10], a finding corroborated by our study. Each of the eyes included in our study did not have any other discernible macular pathology that could have adversely affected the vision. Therefore, the fact that most of our patients had some presenting symptom of visual disturbance, albeit vague, can only be put down to the presence of the microhole. Regarding the etiology of macular microholes, many theories have been propounded [11, 12], but there was no conclusive evidence in our study to support any one in particular. None of our patients had a history of sungazing, phototoxicity or significant ocular trauma, although we cannot be absolutely sure that these were not the pathogenetic mechanisms. One recent series by Davies et al. pointed out defects in the RPE in patients with poppers maculopathy. We had not elicited a history of poppers use from our patients as our study pre-dated this report. We also had not questioned our patients on laser pointer injury, a history that should have probably been elicited. Our study did not find any association between the size of the microhole and the presence of systemic conditions like diabetes, hypertension or coronary artery disease. This was probably due to the limited number of patients who had these systemic illnesses.

When the visual acuities of the involved eyes were analysed against the size of the microholes, there was no significant correlation observed. This means that even if the microhole is large there is no corresponding fall in functional vision despite the fact that most microholes are associated with a PRL loss. This finding is similar to previous work by Emerson et al. [3]. This could mean that the retina is able to compensate for this exceptionally small loss of functional elements and provide an overall well-functioning vision for the patient. Clinically, approximately half the involved eyes had a ‘red spot’ identified at the fovea, which was a finding consistent with eyes studied by Douglas et al. [13]; however, this also means that the ophthalmologist was unable to detect such a defect in almost 40 % of the eyes. Therefore this finding is neither consistent nor pathognomonic and the microhole was detected only on retinal imaging, reinforcing the advantage of having such a modality to arrive at a diagnosis.

The SD-OCT findings revealed RPE alterations in half the number of studied eyes similar to findings by Gella et al. [4]. The microholes per se were more likely to be centrally located and, as in another study [3], irregular in configuration, i.e., the lateral walls of the defect were ragged; these were often difficult to categorise as a particular shape. Nearly all eyes had involvement of the PRL, and this seems to be a feature uniformly described by other investigators [2, 4]. Involvement of the ELM was not a regular feature, and outer lamellar defects were more common, suggesting that the defect probably arises from the PRL and progresses inwards. The significance of this observation is not yet known, but the likelihood of formation of a full-thickness macular hole in such cases needs to be studied, to see if the incidence is higher if the ELM has been breached. Microholes are considered stable and non-progressive. Our study had follow-up of most patients over a 12-month period, during which there was no significant change in the microhole characteristics, with none of them progressing to full-thickness defects. Some investigators hypothesise that microholes may be part of the evolution spectrum of macular holes or are perhaps seen in spontaneous macular hole closure [14, 15, 16], while others postulate that the reason for their non-progression [2] is the same as why stage 1 and 2 macular holes with vitreomacular separation do not progress [17, 18]. To prove an association between the size of the microhole and the presence of VMIAs, the mean dimension of the microholes, which was calculated at around 80 μm, was taken as a cut-off between small and large. We proved a statistically significant correlation between the presence of VMIAs and a greater volume of microholes, suggesting that some unknown effect of the vitreous on the macula may be a root cause in microhole evolution. Lai et al. [16] reported a single case of a full-thickness microhole spontaneously closing in an eye after PVD occurrence. This is in contrast to other reports which propose that PVD plays a vital role in the formation of microholes [3, 10]. Since our data suggest that VMIAs are more common in larger microholes, we hypothesise that perhaps the vitreous tractional force keeps the walls of the microhole from reapposing and may therefore be associated with larger sized microholes. However, this theory does not completely explain the formation of large microholes with no VMIAs. As slit-like microholes are less likely to be associated with VMIAs we propose that these slit defects are probably a result of some inherent retinal lamellar weakness, not caused by tractional forces.

Although our study had a large number of patients with macular microholes, lack of long-term follow-up with most of them limited our assessment of the evolution of this condition and the cross-sectional nature of this study was a major limitation. We propose further investigation into the association between VMIAs and the size of the microhole with OCT, which is an ideal tool for their evaluation [6], by comparing with matched groups for the presence and absence of VMIAs in a longitudinal study, to fully understand the significance of this finding.

Notes

Acknowledgments

We sincerely thank Chaithanya Eye Hospital and Research Institute for financial assistance.

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Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Batmanabane Prakash Vaishnavi
    • 1
  • Unnikrishnan Nair
    • 1
  • Manoj Soman
    • 1
  • K. G. R. Nair
    • 1
  1. 1.Chaithanya Eye Hospital and Research InstituteKesavadasapuram, TrivandrumIndia

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