Myopia, the most common type of refractive error, has become an epidemic in some Asian countries.1 Eighty to ninety percent of high school students in Eastern Asian cities suffer from myopia, with 20% of them experiencing high myopia.2 High myopia is associated with various sight-threatening complications, such as retinal detachment, choroidal atrophy, myopic maculopathy, and retinal hemorrhage. It was reported that high myopia is ranked the second cause of visual impairment in Chinese adults.3,4 In addition, many epidemiological studies have suggested that high myopia was a predisposing factor of primary open angle glaucoma, although the intrinsic mechanisms remain elusive.5,6
The ocular structure of high myopia is considered to be different from that of emmetropia, and the intrinsic changes may be partly explained by altered corneal biomechanical properties.7 However, the quantification of corneal biomechanics is not an easy task and is obtainable only in vitro. The ocular response analyzer was first introduced in 2005 and provided an opportunity to measure corneal biomechanics in vivo. The ocular response analyzer provides two corneal biomechanical parameters: corneal hysteresis and corneal resistance factor. Many studies have reported that high myopia is associated with significantly lower corneal hysteresis compared with emmetropia.8,9 However, the ocular response analyzer provides only two biomechanical parameters, and their accurate interpretations are ambiguous, thus calling for better tools for the assessment of corneal biomechanics in vivo.10
Dynamic Scheimpflug imaging technology is a relatively new instrument that enables the assessment of corneal biomechanics in vivo. It provides more than 10 corneal biomechanical parameters via equipment with an ultrahigh-speed Scheimpflug camera, which can record the entire deformation process of corneal response after an air puff. To date, many studies have been performed using this technology to assess corneal biomechanics in healthy subjects or subjects with disease, such as those with glaucoma, diabetes mellitus, or keratoconus and after refractive surgery.11,12 Its reproducibility and repeatability have been validated as well.12,13 However, the knowledge of corneal biomechanics in high myopia is limited. Therefore, a cross-sectional study was performed to evaluate the differences of corneal biomechanics between high myopia, and a further pooling analysis was conducted to obtain more reliable and conservative conclusions.
This cross-sectional study was performed at Hainan Eye Hospital, which is affiliated with the Zhongshan Ophthalmic Center, China, from July 2015 to August 2015. The study was approved by the Institute Ethics Committee and conformed to the tenets of the Declaration of Helsinki. Informed written consent was obtained from each subject. High myopia and emmetropia were defined by spherical equivalent. Subjects with high myopia (spherical equivalent <−6 diopters [D]) and emmetropia (−0.50 D ≤ spherical equivalent ≤ 0.50 D) were consecutively enrolled in this study. Individuals with any corneal diseases, with a history of refractive or intraocular surgery, with any retinal abnormalities, wearing corneal contact lens within 3 months, with topical medication, with cylinders greater than 1.0 D, with intraocular pressure 21 mmHg or greater, and with severe cataracts, diabetes, or systemic hypertension were excluded.
All subjects underwent complete ophthalmic examinations, including best-corrected visual acuity testing, slit-lamp examination, fundus examination, and refractive measurement. Tropicamide phenylephrine eye drops (Santen Pharmaceutical Co., Ltd., Osaka, Japan), containing 0.5% tropicamide and 0.5% phenylephrine, were used to induce cycloplegia, with three drops placed in each eye at one drop every 10 minutes. Cycloplegia and pupil dilation were evaluated after an additional 15 minutes. Pupils were considered fully dilated at 6 mm or greater, and cycloplegia was considered complete if light reflex was absent. Refraction was determined by an autorefractor (KR-8900; Topcon Corp., Japan) at least 20 minutes after the last drop. Spherical equivalent was calculated by spherical power plus half of cylinder power.
Dynamic Scheimpflug Imaging
Corneal biomechanical properties were obtained using a dynamic Scheimpflug imaging technology system (Corvis ST; OCULUS Optikgeräte, Wetzlar, Germany). The scan speed is 4330 frames/s, which covered the 8.0-mm cornea horizontally. The system also presents measurements of intraocular pressure and central corneal thickness. All measurements were taken by a single experienced technician who was masked to other test results and to all of the patients' clinical information. To eliminate the diurnal variation of corneal biomechanics, all assessments were performed at 9 AM to noon. The working principles and applications of the Corvis ST have been described in detail elsewhere.10,11,14 In summary, the Corvis ST records the entire process of corneal deformation response to an air jet by an ultrahigh-speed Scheimpflug camera. The cornea experiences four distinct statuses, that is, first applanation, the highest concavity, second applanation, and natural status (Fig. 1).
The series parameters during each status were derived by analyzing the above processes, including the first applanation time, first applanation length, first applanation velocity, second applanation time, second applanation length, second applanation velocity, highest concavity time, maximal deformation amplitude, peak distance, and highest concavity radius. The latest analysis software (Version Corvis_ST_1.2r1126; OCULUS Optikgeräte) was used in this study.14,15 It has several advantages. First, it is more precise than previous versions are, as the whole eyeball movement was adjusted in the assessment of the displacement of the corneal apex. Second, it provides another two parameters (first and second applanation deformation amplitude). Third, a quality index was used to ensure the correct imaging procedure. In this study, only the images with an “OK” quality index were included in the final analysis. The definitions of each parameter are summarized in Table 1.
The Stata SE 12.0 (StataCorp, College Station, TX) was used for all statistical analyses, and P < .05 was considered statistically significant, except when otherwise specified. Based on data from a previous study, 36 eyes (18 in high-myopic group vs. 18 in emmetropic group) are required to detect a significant intergroup difference in maximum deformation amplitude of at least 0.05 mm with a significance level of .05 and a power of 0.90, for an SD of 0.05 mm.16 The data of the right eyes were used for statistical analyses. The first 15 high-myopic subjects (15 eyes) and 15 emmetropic subjects (15 eyes) underwent test-retest at 5-minute intervals. The test-retest repeatability was quantified by intraclass correlation coefficients with values of greater than 0.80, 0.61 to 0.80, 0.41 to 0.60, and less than 0.40 indicating excellent, good, moderate, and poor repeatability, respectively. The intraclass correlation coefficient was calculated by Stata software through comparing the variations of test-retest in the same subject with the total variation. The Kolmogorov-Smirnov test was used to verify the distribution of normality. The independent t test was used to calculate the crude differences of demographic and corneal biomechanical continuous data between the high-myopia group and emmetropic eyes. The χ2 test was used to compare the sex distributions in both groups. Previous studies demonstrated that age and intraocular pressure are the confounders in the interpretation of corneal biomechanics; thus, the mixed linear model was further used to compare corneal biomechanics after adjusting for confounding factors in high-myopia and emmetropic subjects.17,18
Literature search was performed to identify the studies on changes of corneal biomechanics in high myopia. The electronic databases (PubMed, EMBASE, and Web of Science), academic association Web sites, and Google Scholar engine were searched from inception to May 2016, without language and time restriction. The literature search was updated in May 1, 2017. The following terms were used: “Corvis,” “Scheimpflug,” “Corneal biomechanical,” “biomechanics,” “high myopia,” “near sight,” and “short sight.” The references of reviews and eligible articles were screened for additional eligible studies. Inclusion criteria included (1) cross-sectional or case-control design; (2) comparison between high myopia and controls; (3) corneal biomechanical properties were measured by Corvis ST; and (4) providing adequate data for pooling analysis. If multiple studies have overlapping population, the most comprehensive study was used. We abstracted the mean differences and corresponding 95% confidential interval of each corneal biomechanical parameter.
To obtain more conservative results, a random-effects model was used to calculate the mean differences. The details of pooling analyses were described in our previous report.11 The I2 statistic is the proportion of inconsistency across studies that is due to heterogeneity rather than chance. In brief, the χ2 test and I2 statistics were used to quantify interstudy heterogeneity, with P < 0.10 and/or I2 > 50% indicating significant heterogeneity. Sensitivity analyses were conducted by leave-one-out and pooling again.
Forty high-myopic subjects (40 eyes) and 61 emmetropic subjects (61 eyes) were included in the final analysis, with 55 being male and 38 female. Table 2 shows the repeatability of Corvis ST parameters for test-retest at 5-minute intervals. Six parameters demonstrated excellent repeatability (intraocular pressure, central corneal thickness, first applanation time, highest concavity radius, maximal deformation amplitude, and second applanation velocity). In addition, three parameters (first applanation velocity, first applanation deformation amplitude, and second applanation deformation amplitude) demonstrated moderate repeatability, and five parameters (first applanation length, highest concavity time, peak distance, and second applanation length) had poor repeatability.
The mean age was 27.1 ± 11.5 years in the high-myopic eyes and 30.9 ± 10.5 years in the emmetropic eyes (P = .090). The sex distribution, intraocular pressure, and central corneal thickness were not significantly different between groups (all P > .05). As expected, the high-myopic eyes had higher spherical equivalent compared with the emmetropic eyes (−7.67 ± 1.54 vs. −0.08 ± 0.41; P < .001). When comparing the raw data of corneal biomechanics between groups, the high-myopic eyes were characterized by a longer first applanation time, slower first applanation velocity, shorter highest concavity time, smaller highest concavity radius, shorter second applanation time, and smaller second applanation deformation amplitude (all P < .05) (Fig. 2).
Considering that corneal biomechanical parameters may be influenced by age and intraocular pressure, a mixed linear model was used to compare the differences between the two groups after adjusting for these confounders (Table 3). The high-myopia group demonstrated greater maximum deformation amplitude compared with the emmetropic eyes (mean difference, 0.06 mm [95% confidential interval, 0.03 to 0.08 mm]; P < .001) after adjusting for age and intraocular pressure. The mean differences of the other 11 parameters between groups were not statistically significant.
A pooling analysis was conducted to obtain evidence with greater robustness. Following a comprehensive literature search and strict screening, we identified three eligible reports.16,19,20 Two studies have overlapping participants, and the more complete one was included.16,20 Thus, two studies plus the present study were included.16,19 The similar designs among the studies enabled the pooling analyses involving 118 eyes with high myopia and 107 emmetropic eyes. Table 4 summarizes the characteristics of the included previous and present studies. All of these studies were performed in Chinese urban subjects, one each from Beijing, Hong Kong, and Guangzhou. Except for spherical equivalent, there were no significant differences between the high-myopia and emmetropic eyes in age, sex, intraocular pressure, and central corneal thickness in any study (all P > .05).
Fig. 3 shows the mean differences by combining the data from the present study and previously qualified studies. The pooling results confirmed and extended our primary study. The differences in four corneal biomechanical parameters between both groups remained significant. The high-myopia group exhibited smaller highest concavity radius, greater maximum deformation amplitude, faster second applanation velocity, and shorter second applanation length, with pooled mean differences of −0.21 mm (95% confidential interval, −0.30 to −0.13; P < .001) for radius curvature at the highest concavity, 0.05 mm (95% confidential interval, 0.04 to 0.06; P < .001) for maximum deformation amplitude, −0.03 m/s (95% confidential interval, −0.06 to −0.002; P = .034) for second applanation velocity, and −0.05 mm (95% confidential interval, −0.08 to −0.02; P = .001) for second applanation length. No significant heterogeneity was observed except for second applanation velocity. Leave-one-out analyses demonstrated that no single study changed the pooled results.
Our cross-sectional study demonstrated that the profiles of corneal biomechanical properties in high myopia were different from emmetropia, with higher maximal deformation amplitude in the high-myopic eyes than in the emmetropic eyes after adjusting for other confounding factors. The pooling results confirmed that maximum deformation amplitude is greater in high myopia, which is consistent with our primary findings. The pooling results also observed smaller highest concavity radius, faster second applanation velocity, and shorter second applanation length in high myopia, thus validating and extending previously published studies on this topic.
The cornea is a viscoelastic tissue with viscous and elastic properties. During the deformation process, viscous properties induce energy dissipation, and elastic properties result in energy storage. The first applanation was proposed to be related to elasticity of collagen fibers, whereas the second applanation was associated with viscous and elastic properties of corneal stroma.22 Theoretically, a more deformable cornea in response to an air puff is related to the following features: (1) faster in the first applanation: shorter first applanation time and length, faster first applanation velocity, and larger first applanation deformation amplitude; (2) greater deformation amplitude: greater maximum deformation amplitude, shorter peak distance, and highest concavity radius; (3) later in the second applanation: longer second applanation time, shorter second applanation length, slower second applanation velocity, and smaller second applanation deformation amplitude.11,23 It was reported that large variations exist in highest concavity radius, second applanation velocity, and length in terms of coefficient of variation or intraclass correlation, whereas the maximum deformation amplitude is a stable parameter that can be used.12,24 The maximum deformation amplitude represents the deformability of corneal resistance for the air stress, with higher maximal deformation amplitude meaning greater deformability. Eyes with high myopia demonstrated greater maximum deformation amplitude compared with emmetropia, suggesting that a high-myopic cornea becomes weaker and more deformable. This observation is consistent with previous studies using ocular response analyzer, which reported significantly lower corneal hysteresis in high myopia in comparison with emmetropic eyes.9 It was reported that the cornea in high myopia was less stiff than that in low myopia.25
Corneal deformation indicates the elastic property and the mechanical strength of interaction between matrix collagen fibers and extracellular glycoproteins. Myopia was considered to be closely associated with abnormal scleral constitution and scleral remodeling.26 High myopia was characterized by the reduction of diameter of scleral collagen fibers, fast synthesis of glycoprotein, and increase in collagen hydrolytic enzymes, which induced scleral thinning, loss of scleral tissue, and scleral expansibility.27 Because both the cornea and sclera derive from the same mesoderm, similar changes may exist in the cornea during the development and progression of myopia. A recent electron microscopy study revealed that the elastic fiber network of the central cornea appeared to originate from the limbus and may even be from the sclera.28 A previous study confirmed that a stiff sclera was associated with a stiff cornea in response to air stress.29 Our results demonstrated that high-myopic eyes had higher maximum deformation amplitude than emmetropic eyes, indicating cornea of high myopia was more deformable and less stiff in response to stress. Therefore, corneal biomechanics may be an indicator for scleral mechanical strength in high myopia. It is worth noting that the relationship between the biomechanical parameters from Corvis ST and the standard indicators for viscous and elastic materials, such as Young modulus, remains elusive. Further studies focusing on this issue are warranted.
Epidemiological studies demonstrated that high myopia independently increased the susceptibility to primary open angle glaucoma.30,31 The similar changes of corneal biomechanics may help to explain the association between these two entities. Lee et al.21 reported that primary open angle glaucoma was associated with greater maximum deformation amplitude, peak distance, and second applanation velocity after adjusting for other factors. The cornea, sclera, and lamina cribrosa are closely correlated and composed of a continuous extracellular matrix. There may be a potential correlation of the corneal biomechanics between these tissues. Cornea biomechanics was regarded as a mirror of biomechanics in the whole eyeball.32 It was reported that the lamina cribrosa in eyes with more deformable cornea distorted greater in response to variation of intraocular pressure; that is, this type of eyes was more susceptible for glaucomatous damage during elevation of intraocular pressure and changes of optic nerve head.33,34 A longitudinal cohort study demonstrated that the rate of retinal fiber layer deterioration speeded by 0.13 μm per year for each 1-mmHg lower corneal hysteresis.35 Another study revealed significant relationship between greater maximum deformation amplitude and faster rates of visual field progression in glaucoma.36 Therefore, knowledge of corneal biomechanics is beneficial for us to understand the relationship between high myopia and primary open angle glaucoma.
Although previous studies reported corneal biomechanics in high-myopic eyes, they were limited by small sample sizes and mixed results. Wang et al.19 reported that the high-myopia eye was associated with greater maximum amplitude, shorter second applanation time, and smaller highest concavity radius than were the emmetropic eyes in a study with 33 high-myopic subjects and 21 emmetropic subjects. In another study of 41 high-myopic eyes and 25 emmetropic eyes, Lee et al.16 showed that high-myopic eyes had faster greater maximum deformation amplitude compared with controls. With a greater sample size and power, we confirmed that high myopia was associated with smaller highest concavity radius, faster second applanation velocity, and shorter second applanation length. The difference of the rest of the eight parameters did not differ between the two groups. The following are some reasons. First, the detection of the subtle differences of these parameters may require a large sample size. Second, these parameters themselves may be not representatives of corneal biomechanics, and caution should be taken with these parameters when interpreting corneal biomechanics. Studies with larger sample sizes and various ethnicities are needed to explore the implications of these parameters.
The strength of this study lies in the adoption of a reliable device and latest software, which provides more than 10 corneal biomechanical parameters. In addition, the similar methodologies of previous reports and our cross-sectional study enable pooling analyses, which confirmed our primary results. This study also has limitations. First, axial length was unavailable for the multiple regression analyses. The main reason for high myopia is axial elongation, and a part of myopia is due to high corneal refraction or combination longer axial length and corneal refraction. Ocular rigidity was related with the initial volume of the eyeball. Second, the sample size is relatively small, even pooling the data from previous reports. However, the sample size was larger than estimation, and the positive results strengthened the conclusions. Third, all included studies were based on the Chinese urban population. Ethnic variations of corneal biomechanics may have existed, so our conclusions should be verified with other ethnicities.37 Fourth, the nature of the cross-sectional design prevents cause-and-effect inference. It would be interesting to study the corneal biomechanical properties in myopic eyes and correlate it with the rate of high-myopia development in a prospective study. Finally, the newer software was not used in the earlier studies included in the pooling analysis, which may introduce measurement error. However, our study led to similar results, and the heterogeneity was not significant for most parameters. Thus, the impact of version of the software on the overall findings is limited.
In summary, we compared the corneal biomechanical properties between high myopia and emmetropia using Corvis ST. After adjusting for the confounding factors, high-myopic eyes demonstrated greater maximum deformation amplitude, indicating a weaker and more deformable cornea. The pooling analyses confirmed and extended the primary findings. These findings are helpful for understanding the association between high myopia and primary open angle glaucoma. Cohort studies with large sample sizes and various ethnicities in the future will further our understanding of the role of corneal biomechanics in high myopia.
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