Comparison of full-thickness traumatic macular holes and idiopathic macular holes by optical coherence tomography

Transcription

1 Graefes Arch Clin Exp Ophthalmol (2010) 248: DOI /s z RETINAL DISORDERS Comparison of full-thickness traumatic macular holes and idiopathic macular holes by optical coherence tomography Jingjing Huang & Xing Liu & Ziqiang Wu & Srinivas Sadda Received: 23 August 2009 / Revised: 11 October 2009 / Accepted: 20 October 2009 / Published online: 24 February 2010 # Springer-Verlag 2010 Abstract Background The optical coherence tomography (OCT) and clinical characteristics of traumatic macular holes (TMHs) can be compared to those of idiopathic macular holes (IMHs) to gain insights into the pathogenesis of both. Methods The demographic data and visual acuity of 73 consecutive patients with unilateral, full-thickness TMHs and 182 consecutive patients with idiopathic IMHs were recorded. All patients with TMH and 60 patients with IMH underwent OCT scanning and quantitative measurements. The apical and basal diameters and marginal retinal thicknesses were recorded for each hole. The hole areas and eccentricities were calculated. These parameters were compared between the two types of macular holes, and correlated with visual acuity. Results Compared to IMHs, TMHs were generally thinner, larger at the base, less circular, and were associated with worse vision. Vitreous detachment was more commonly associated with IMHs than TMHs. Both IMHs and TMHs were wider horizontally than vertically. Visual acuity was Supported by Grant from National Natural Science Foundation of China. J. Huang : X. Liu (*) State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, 54 Xianlienan Road, Guangzhou , People s Republic of China drliuxing@163.com Z. Wu Center for Advanced Eye Care, Carson City, NV, USA S. Sadda Doheny Image Reading Center, Doheny Eye Institute, Los Angeles, CA, USA negatively correlated with the size of IMHs, but not with any tomographic parameters in TMHs. Conclusion The tomographic and clinical findings associated with TMHs and IMHs provide useful insights into the pathogenesis of these two types of macular holes. Keywords Optical coherence tomography. Traumatic macular holes. Idiopathic macular holes Introduction Optical coherence tomography (OCT) has refined Gass s original description of idiopathic macular holes (IMHs) [1, 2]. The tomographic and clinical characteristics of IMHs have been studied extensively in the literature. Traumatic macular holes (TMHs), which occur in only 1.4% of closed eye trauma patients and 0.15% of open eye trauma patients [3], are associated with forceful blunt injury. Because of its relatively low prevalence, TMH has not been studied systematically with the aid of OCT until recently [4, 5]. In this study, we directly compare the tomographic and clinical characteristics of two cohorts of patients with these two types of full-thickness macular holes. Materials and methods The clinical charts of 73 consecutive patients diagnosed with unilateral TMH at the outpatient clinics of Zhongshan Ophthalmic Center of Sun Yat-sen University (Guangzhou, China) from January 2005 to June 2006 were retrospectively reviewed. The inclusion criteria were: 1) reliable history of eye trauma and no prior intraocular surgery, 2) significant decrease of visual acuity within 4 weeks after trauma, 3) full-

2 1072 Graefes Arch Clin Exp Ophthalmol (2010) 248: thickness macular hole demonstrated on dilated stereoscopic examination and on OCT, 4) no retinal detachment except for that related to the macular hole, and 5) no history of high myopia (no more than 6D). Additional details of this TMH cohort were described previously [5]. The clinical charts of 182 consecutive patients diagnosed with unilateral or bilateral IMH in the same period and same outpatient clinics were also reviewed. The inclusion criteria were: 1) no history of trauma or surgery in either eye, 2) full-thickness macular hole demonstrated on dilated stereoscopic examination and on OCT, 3) no history of high myopia (no more than 6D), 4) no other ocular disease except age-related cataract, and 5) the opacity of lens less than C2N1P1 by LOCS II (lens opacities classification system II) [6]. Of the 203 eyes with IMH, 60 eyes of 60 patients were randomly selected for additional manual quantitative OCT image analysis and comparison with TMHs. The study was conducted in accordance with the tenets of the Declaration of Helsinki, and was approved by the Institutional Review Board. Informed consent was obtained from all patients. For each subject, data which were collected included age, gender, best-corrected visual acuity, slit-lamp biomicroscopic findings including lens assessment, dilated stereoscopic ophthalmoscopy assessment, and fundus photography. For traumatic cases, the time between injury and examination was also recorded. The maculae of all patients were scanned using Stratus OCT s (Carl Zeiss, Dublin, CA, USA) line scan protocol, with resolution of 512 A-scans over a length of 5 mm, obtaining both a horizontal and vertical scan for each eye. All scans were performed by a trained physician (JH) who specifically attempted to center each scan on the foveal center. Scans were repeated until signal strengths of at least 6 were obtained, and good centration had been achieved. Quantitative measurements (in µm) using the Stratus OCT software s calipers were performed according to the following definitions: retinal thickness was defined as the distance from the outer border of neurosensory retina to the internal limiting membrane (i.e., areas of subretinal fluid were not included in the retinal thickness measurement); the apical diameter of the macular hole was defined as the width of the narrowest neuroretinal defect; and the basal diameter of macular hole was the widest distance at the base of the hole, immediately above the retinal pigment epithelium. The nasal, temporal, superior, and inferior thicknesses of the neurosensory retina at the apical margin of the hole were measured. The average retinal thickness was the mean of these four measurements. Assuming all macular holes to be approximately elliptical, we defined a to be the radius of the larger axis (the longer of the two apical radii obtained by the vertical and horizontal line scans) and b to be the radius of the smaller axis of the ellipse. The apical area was thus πab, inµm 2. The apical eccentricity was calculated by the formula [5]: rffiffiffiffiffiffiffiffiffiffiffiffiffi " ¼ 1 b2 a 2 The basal area and eccentricity were similarly computed. Eccentricity is a measure of the circularity of an ellipse. When the major and minor axes are equal in length, i.e. a circle, the eccentricity is zero. However, if the major axis is much longer than the minor axis, the eccentricity approaches 1. Statistical methods The means and standard deviations of the above parameters were calculated for each type of macular hole. Paired t-test was used to compare the nasal, temporal, superior, inferior, and average retinal thicknesses. Independent t-test was used to compare the visual acuity, apical and basal diameters, and the sizes of macular holes. Chi square test was used to compare the laterality (left vs right eye) and gender. Univariate regression analysis was performed to analyze the relationships between visual acuity and the above indices. P<0.05 was considered statistically significant. Results Compared to IMH patients, TMH patients were predominantly younger and male (Table 1). They also had worse visual acuity (Table 1). Among the cohort of IMH eyes, there was no difference between the subset of sixty subjects/eyes randomly chosen for detailed OCT analysis, and the rest of the IMH cohort with respect to age, gender, and visual acuity (P>0.1, data not shown). Compared to IMHs, TMHs had lower average retinal thickness but greater basal diameters and areas (Table 2). There were no differences in apical diameters and areas (Table 2). IMHs were more circular than TMHs (lower Table 1 Clinical and demographic data of full-thickness traumatic (TMH) and idiopathic macular holes (IMH) TMH IMH P Eyes/cases 73/73 203/182 / Eye right a left Sex male a female Age 27.11± ± b LogMar VA 1.23± ± b a Chi square test b independent t test

3 Graefes Arch Clin Exp Ophthalmol (2010) 248: Table 2 Averages of tomographic measurements of full-thickness traumatic (TMH) and idiopathic macular holes (IMH) a independent t test TMH IMH T P a Eye / / Retinal thickness (µm) ± ± Basal diameter (µm) ± ± Apical diameter (µm) ± ± Apical area (10,000 µm2) 21.82± ± Basal area (10,000 µm2) ± ± eccentricity) (Table 3). The horizontal dimensions were greater than the vertical dimensions in both TMHs and IMHs (Table 4). Among the IMH subset studied by OCT, 36 out of 60 had either detectable PVD (33/60) and/or operculum (32/60). By comparison, no PVD or operculum was demonstrated by OCT or on clinical examination in any of the 73 TMH eyes (P<0.05). The LogMAR visual acuity of IMH patients was positively correlated with the basal and apical areas of the hole, which meant that the larger the area, the poorer the visual acuity (Table 5). However, none of the tomographic measurement parameters correlated with visual acuity in TMH patients (Table 5). Age was negatively correlated with retinal thickness of IMHs (r= 0.322, P=0.012), while the duration of TMH (from injury to presentation) was positively correlated with the apical area (r=0.418, P=0.001). Discussion In this retrospective, comparative study we observed several significant differences between the demographic and morphologic characteristics of idiopathic versus traumatic macular holes. The apparent differences between these two types of holes may be a reflection of their different pathophysiologies. Both anteroposterior and tangential vitreous traction were hypothesized to be responsible for the pathogenesis of IMH [7]. OCT studies confirmed the importance of vitreous traction in the formation of IMHs [8 10]. A close relationship between the stage of IMHs and the degree of posterior vitreous detachment has been well-documented [11]. On the other hand, the etiology of TMHs remains controversial. Both early- and late-onset TMHs have been reported [12], but our retrospective study could not reliably distinguish the type of hole in a particular patient based solely on the history provided. The early-onset type occurs immediately after injury, and is thought to be partly due to avulsive force applied to the fovea by the vitreous as a result of anteroposterior compression [13]. TMH patients are typically younger with stronger vitreofoveal adhesion, which increases the risk of foveal avulsion. Therefore, patients with pre-existing PVD should have lower risk of TMH formation. In our series, none of the TMH patients had clinical or OCT-detectable PVD. This is consistent with previous studies that found relatively low rates of PVD in TMH patients [14, 15]. Additionally, foveal avulsion is likely to cause jagged, irregular edges, whereas IMHs form more gradually. Therefore, it was not surprising that our study found significantly higher eccentricity in TMHs compared to IMHs. Lastly, because avulsive forces from trauma are much stronger than the vitreoretinal tractional forces that cause IMHs, TMHs are probably also much more likely to be associated with localized retinal detachment, which may explain their greater basal diameters and areas in our study. ILM rupture and disruption in the retinal layers with secondary vitreous fluid accumulation may cause intraretinal swelling and delayed-onset TMH formation [16, 17]. Most documented cases of delayed-onset TMH occur within a few weeks after injury. However, even this is short compared to the typical formative period for IMHs. The longer duration of vitreoretinal traction may cause greater macular edema in IMHs. Such differences in pathogenesis may explain the difference in average retinal thickness between TMHs and IMHs seen in our study. Older IMH patients also have weaker vitreoretinal tractional forces compared to Table 3 Comparing eccentricities of the apex and the base of fullthickness traumatic (TMH) and idiopathic macular holes (IMH) Eccentricity TMH IMH T P a Apical 0.64± ± Basal 0.68± ± a independent t-test Table 4 Horizontal and vertical dimensions of full-thickness traumatic (TMH) and idiopathic macular holes (IMH) at the apex (µm) Horizontal Vertical T P a TMH ± ± IMH ± ± a paired t-test

4 1074 Graefes Arch Clin Exp Ophthalmol (2010) 248: Table 5 Correlation between LogMAR visual acuity and clinical/ tomographic variables in full-thickness traumatic (TMH) and idiopathic macular hole (IMH) patients TMH IMH r a P r a P Age Marginal retinal thickness Basal area Apical area Time from injury to exam b / / a Pearson correlation. b Spearman correlation. younger patients, possibly explaining the negative correlation between age and retinal thickness. It appears that TMHs may on average enlarge with time (increased apical area), even though cases of spontaneous closure have been documented [18]. Our study also showed that retinal thicknesses were similar circumferentially around TMHs, but the superior and nasal margins were thicker than the inferior and temporal margins in IMHs (Fig. 1, P<0.05 in pairwise comparisons). Additionally, the horizontal dimensions of both IMHs and TMHs were greater than the vertical dimensions. In early stages of posterior vitreous detachment, the first step is usually a focal detachment of one quadrant in the perifoveal region, with a predilection for the superior quadrant [11, 19]. Subsequent detachment usually extends superiorly, probably due to the downward pull of gravity on the superior vitreous. Over time, vitreous detachment extends temporally, then inferiorly. The relatively strong vitreopapillary adhesion anchors the vitreous Fig. 1 Average retinal thicknesses at the margins of traumatic (TMH) and idiopathic macular holes (IMH) more firmly, resulting in vitreous detachment occurring last in the nasal quadrant. This mechanism would result in a longer duration of persistent traction in the nasal/temporal direction, which could possibly account for the greater horizontal expansion of IMHs. It would also explain the thicker nasal margins of IMHs in our study and in a previous study [20]. Because TMHs occur much more rapidly and the vitreous tends to not be detached from the fovea, vitreoretinal tractional forces are probably similar circumferentially, resulting in a more even retinal thickness distribution. Applying our theory, however, it is not clear why TMHs were also observed to have greater horizontal than vertical diameters, similar to IMHs. One proposed mechanism of rapid-onset TMH formation is the stretching of the posterior pole as a result of anteroposterior compression of the eyeball [16]. It is possible that the stretching forces acting in the vertical direction may be weaker, being restricted by the smaller vertical dimension of the orbit. Clinical and tomographic correlates to visual acuity in TMH and IMH patients appear to be different. No statistically significant correlations were found with TMHs, though average retinal thickness showed a trend for a positive association with visual acuity. A thinner retina may imply a greater degree of retinal atrophy or loss of retinal tissue in this case. Our finding that larger IMHs (basal and apical areas) were associated with worse visual acuity may not be surprising, but it is not immediately clear why the size of TMHs was not correlated with visual acuity. One possible explanation is that since TMHs typically feature a true avulsion of retinal tissue with or without subsequent enlargement of the hole, the actual amount of avulsed retinal tissue may vary and not correlate with the actual area of the hole. Another possible explanation is that the traumatic event which precipitated the hole could cause other secondary damage (e.g. to the RPE or photoreceptors) which could also affect the vision, even though such damage may not be easily detected on clinical or tomographic examination. For example, the photoreceptor inner segment outer segments junctions were shown to be disrupted beyond the boundary of the macular hole itself [21]. Therefore, the size of a macular hole may not reflect the extent of functional disturbance. A final possible confounding factor is the generally worse visual acuity among TMH patients (~20/340 Snellen acuity), compared with IMH patients (~20/230). There is probably more variability and less precision in measuring visual acuity at such low levels. The apparently superior clinical outcome in IMH patients, coupled with lower coefficients of variation (standard deviation/mean) of the apical and basal areas in IMHs, may have favored a higher probability that a correlation could be found between macular hole dimensions and visual acuity.

5 Graefes Arch Clin Exp Ophthalmol (2010) 248: There are several important limitations to our study. The most important may be the method of OCT image acquisition. Though the experienced physician OCT examiner obtained multiple scans as needed, scan centration for full-thickness macular holes was still a challenge for many patients. Even for patients in which the scan appeared to be centered to the examiner at the initiation of acquisition, because of the relatively slow (compared with new spectral OCT instruments) scanning speed of time-domain Stratus OCT, it is possible that the patient s eye moved during the acquisition. Therefore, we cannot be entirely confident that the vertical and horizontal diameters are accurate for a given patient. Inaccuracies may be further compounded if the circumference was irregular, as seen in some TMHs. Because calculations of apical and basal areas and eccentricities were based on the respective diameters, errors in the initial OCT measurements were propagated into other secondary parameters. In addition, this retrospective study relied mainly on history to classify macular holes into these two groups. The clinical setting where the study was performed was also challenging because of access-to-care issues. It is possible that these factors may lead to a recall bias or selection bias in our approach. Nonetheless, we do believe that the analysis does provide some useful information that may aid our understanding of the pathogenesis of idiopathic and traumatic macular holes. In summary, idiopathic and traumatic macular holes differ with respect to several clinical and OCT characteristics including age, gender predilection, OCT retinal thickness and thickness distribution, and hole eccentricity, These differences likely reflect the different pathophysiologic mechanisms which result in the development of these lesions. References 1. Gass JD (1995) Reappraisal of biomicroscopic classification of stages of development of a macular hole. Am J Ophthalmol 119: Altaweel M, Ip M (2003) Macular hole: improved understanding of pathogenesis, staging, and management based on optical coherence tomography. Semin Ophthalmol 18: Kuhn F, Morris R, Mester V, Witherspoon CD (2001) Internal limiting membrane removal for traumatic macular holes. Ophthalmic Surg Lasers 32: Arevalo JF, Sanchez JG, Costa RA, Farah ME, Berrocal MH, Graue-Wiechers F, Lizana C, Robledo V, Lopera M (2008) Optical coherence tomography characteristics of full-thickness traumatic macular holes. Eye 22: Huang J, Liu X, Wu Z, Lin X, Li M, Dustin L, Sadda S (2009) Classification of full-thickness traumatic macular holes by optical coherence tomography. Retina 29: Chylack LT Jr, Leske MC, McCarthy D, Khu P, Kashiwagi T, Sperduto R (1989) Lens opacities classification system II (LOCS II). Arch Ophthalmol 107: Gass JD (1988) Idiopathic senile macular hole: its early stages and pathogenesis. Arch Ophthalmol 106: Gaudric A, Haouchine B, Massin P, Paques M, Blain P, Erginay A (1999) Macular hole formation: new data provided by optical coherence tomography. Arch Ophthalmol 117: Chauhan DS, Antcliff RJ, Rai PA, Williamson TH, Marshall J (2000) Papillofoveal traction in macular hole formation: the role of optical coherence tomography. Arch Ophthalmol 118: Kishi S, Takahashi H (2000) Three-dimensional observations of developing macular holes. Am J Ophthalmol 130: Ito Y, Terasaki H, Suzuki T, Kojima T, Mori M, Ishikawa K, Miyake Y (2003) Mapping posterior vitreous detachment by optical coherence tomography in eyes with idiopathic macular hole. Am J Ophthalmol 135: Yamashita T, Uemara A, Uchino E, Doi N, Ohba N (2002) Spontaneous closure of traumatic macular hole. Am J of Ophthalmol 133: Delori F, Pomerantzeff O, Cox MS (1969) Deformation of the globe under high-speed impact: its relation to contusion injuries. Invest Ophthalmol 8: Yanagiya N, Akiba J, Takahashi M, Shimizu A, Kakehashi A, Kado M, Hikichi T, Yoshida A (1996) Clinical characteristics of traumatic macular hole. Jpn J Ophthalmol 40: Johnson RN, McDonald LH, Grand MG, Murray TG, Mieler WF, Johnson MW, Boldt HC, Olsen KR, Tornambe PE, Folk JC (2001) Traumatic macular hole: observations, pathogenesis, and results of vitrectomy surgery. Ophthalmology 108: Hirata A, Tanihara H (2004) Ruptured internal limiting membrane associated with blunt trauma revealed by indocyanine green staining. Graefes Arch Clin Exp Ophthalmol 242: Tornambe PE (2003) Macular hole genesis: the hydration theory. Retina 23: Yamada H, Sakai A, Yamada E, Nishimura T, Matsumura M (2002) Spontaneous closure of traumatic macular hole. Am J Ophthalmol 134: Uchino E, Uemura A, Ohba N (2001) Initial stages of posterior vitreous detachment in healthy eyes of older persons evaluated by optical coherence tomography. Arch Ophthalmol 119: Liu X, Ling Y, Mei L, Zheng X, Hu Z, Liu S (1999) Characteristic and quantitative measurement of idiopathic macular hole with optical coherence tomography. Zhonghua Yan Di Bing Za Zhi 15: (In Chinese) 21. Chang LK, Koizumi H, Spaide RF (2008) Disruption of the photoreceptor inner segment-outer segment junction in eyes with macular holes. Retina 28: