Given that intraocular pressure (IOP) is a well-recognized risk factor for glaucomatous disease, low-tension glaucoma or normal-tension glaucoma (NTG) may be more difficult to diagnose relative to circumstances when a patient has above-average IOP.1 The clinician must pay careful attention to structural and functional optic nerve parameters in the diagnosis of NTG,2 which can easily be missed if IOP measurement is used as a glaucoma screening tool. Previously described risk factors for NTG include older age, female sex, Japanese and Korean ancestry, migraine headache, sleep apnea, hypotension, anemia, and Raynaud’s disease.2-4 There are also novel putative NTG risk factors linked to genetic polymorphisms such as ones found on the optic atrophy 1 gene.5 Patterns in 24-hour diurnal measurements of IOP and ocular perfusion pressure have been postulated to help exclude false diagnoses of NTG,6 but they are not practical alternatives for NTG screening, particularly given the relatively higher costs associated with such methods compared with serial IOP measurement.7 Thus, there is interest in identifying other pressure-independent biomarkers to aid in early diagnosis of NTG.
Over the past decade, advances in corneal biomechanical assessment of the eye using the Ocular Response Analyzer (ORA; Reichert, Depew, NY, US) have provided clinical insight regarding the complex relationship between IOP and NTG. The ORA tests corneal stiffness by calculating 2 measurements: corneal hysteresis (CH) and corneal resistance factor (CRF). They provide surrogate measures for the magnitude of energy absorption through the cornea; CH is calculated by measurement of the change in corneal pressure during deformation, and CRF is similar to CH but additionally incorporates an estimate of the effect of IOP through a constant factor. Studies have consistently reported that the association between lower CH and a greater likelihood of NTG cannot be fully explained by older age, lower central corneal thickness (CCT), or higher IOP,8-17 which are known strong risk factors for glaucomatous disease. One study found higher CH to be predictive of the success of selective laser trabeculoplasty (SLT) in lowering IOP.18 Increased CH is also associated with decreased mean cup depth, decreased cup-to-disc (C/D) ratio, and increased rim area,19,20 but the mechanisms of such associations remain unknown.
The Oculus Corvis ST (Wetzlar, Germany) allows measurement of 10 novel corneal biomechanical properties, including inward and outward corneal applanation time, length and velocity, as well as highest concavity, peak distance, radius, and deformation amplitude that have the potential for clinical utility in diagnosing NTG, similar to CH and CRF. For example, the CH measurement from the ORA machine is presently used to assist in the diagnosis of primary open-angle glaucoma (POAG),21 for which NTG may be considered a subset. These additional parameters of corneal deformation could help differentiate NTG eyes from other types of POAG.
A preliminary exploratory analysis of Corvis parameters in the NTG subgroup of POAG subjects by Lee et al22 suggested that applanation velocity still remains a risk factor for glaucomatous disease in this subcategory when compared with non-diseased eyes. To expand on this prior exploratory work, the current study investigates if applanation velocity is a significant corneal biomechanical risk factor associated with a diagnosis of NTG in a larger, higher-powered study capable of detecting a difference.
This study was approved by the Institutional Review Board of the Stanford University School of Medicine and the Hospital Authority of the University of Hong Kong, and was conducted in accordance with the Declaration of Helsinki. Informed consent was obtained from all participants after explanation of the nature and possible consequences of the study.
Subjects for the study were recruited from the Ophthalmology Clinic at Queen Mary Hospital, a university teaching hospital in Hong Kong, from June 17 to August 9, 2013. Patient charts were examined before each clinic day to determine eligibility to serve as cases or controls.
Subjects were recruited from all patients who attended the eye clinic with a NTG diagnosis at the time of a regularly scheduled appointment. All enrolled NTG subjects met each of the following criteria in the chosen study eye: i) confirmed perimetric defects consistent with a glaucoma diagnosis on at least 2 visual field tests; ii) C/D ratio of >0.6; iii) untreated IOP between 10 and 21 mm Hg; iv) glaucomatous cupping of the optic disc or retinal nerve fiber layer abnormality with corresponding visual field abnormalities; v) a NTG diagnosis made by an ophthalmologist at Queen Mary Hospital prior to the commencement of the study; and vi) confirmation of the diagnosis via chart review by an independent reviewer (RC) who examined spectral-domain optical coherence tomography (OCT) nerve fiber layer results and multiple Humphrey visual fields (HVF); this reviewer, as was the case of all ophthalmologists involved in this study, was masked to the corneal biomechanical measurements. For participants with bilateral NTG, the eye with greater visual field loss was chosen as the study eye, as determined by mean deviation, a standardized measurement linked to glaucoma onset and progression commonly used in studies.23-25
Control subjects were recruited from among patients who visited the ophthalmology clinic the first time during the same period as the study subjects, with one eye selected through a computer-generated random number seed. The study eye met each of the following inclusion criteria: i) normal-appearing optic nerve; ii) normal retinal nerve fiber layer as judged by an ophthalmologist at Queen Mary Hospital; iii) normal fundus examination; iv) a C/D ratio of <0.5; vi) no C/D asymmetry of >0.2; and vii) no focal thinning, drusen, pallor, or heme of the optic disc.
Exclusion criteria for both cases and controls were: i) younger than 18 years; ii) IOP of <10 mm Hg or >21 mm Hg; iii) closed-angle glaucoma or any secondary glaucoma diagnosis; iv) poor cooperation or unsuccessful Scheimpflug video capture after 3 attempts; v) past corneal or scleral eye surgery other than cataract surgery; vi) history of eye trauma or steroid use; and vii) visually significant cataracts that were deemed to be the cause of visual acuity of <20/40.
Subjects underwent routine IOP measurement by either a Nidek Auto Noncontact Tonometer NT-4000 (Nidek Co. Ltd., Gamagori, Japan) or a Topcon CT 80A Computerized Tonometer (Capelle aan den IJssel, Netherlands), as is normally performed for all patients attending the ophthalmology clinic at Queen Mary Hospital by the technician. All recruited participants were positioned in front of the Corvis ST machine (software version Recalc 1.2b1036 RC) with their head on the chin rest, similar to the position assumed during slit-lamp biomicroscopic examination. The air puff nozzle was centered on the right eye and the machine automatically delivered a 30-ms air pulse following correct alignment allowing measurement of 10 biomechanical parameters. Other measured variables included IOP, CCT, and Scheimpflug video capture of the corneal deformation (Fig. 1-3). If the video showed a smooth progression with no disturbances from eyelash or eyelid obstruction, the operator subsequently repeated the same process for the left eye. If the video indicated an error, or the biomechanical parameters revealed a blank value, then up to 3 more attempts were performed in an effort to get a valid reading before considering the measurement as being unreliable with resultant exclusion from the study. There was a mean of 5-minute delay between eye measurements. All measurements were obtained by one operator (KH) who was blinded to the diagnosis of the participants.
The patient history information collected included: date of birth, ethnicity, ongoing use of topical medications, previous ocular surgery, OCT Spectralis retinal nerve fiber measurements, HVF data, and the most recent CCT and IOP readings. All collected data, including information from the Corvis ST, were uploaded to Stanford REDCap encrypted data management software.
OCULUS Corvis ST: Corneal Visualization Scheimpflug Technology
The Corvis ST uses an ultra-high-speed Scheimpflug camera (4330 frames/sec) to capture and calculate corneal biomechanical properties of the eye as it deforms and reforms in response to an air puff. Unique to the Corvis ST are the measurements of deformation amplitude, applanation length, applanation time, and corneal velocity (Table 1). Scheimpflug-captured images of the highest concavity of the cornea and applanation moments also accompany each data point along with a slow-motion video of the corneal deformation after air pulse (Fig. 1-3). This device has obtained CE Mark registration for all measurements, but can only be used in the United States to measure IOP and CCT based on the Food and Drug Administration labeling.
An a priori sample size power calculation was performed using G*Power 3.1.6 with an assumed effect size of 0.5, alpha of 0.05, and power of 80% based on the applanation velocity results from a Corvis ST glaucoma study also performed at Queen Mary Hospital in POAG patients.22 The calculation estimated that 48 cases and 144 controls would be needed for an 80% likelihood of demonstrating a difference between the study and control groups, if such a difference exists.
One eye per subject was analyzed using SAS Enterprise Guide 6.1. Descriptive data were presented as means and standard deviations, or counts and percentages depending on the variables being presented. T-tests and chi-square tests were used to compare the groups, as appropriate. Logistic regression modeling was used to determine the relationship between biomechanical properties and case/control status after adjusting for CCT and age. The multivariate analysis did not adjust for Corvis ST IOP given that all study subjects, by definition, had normal IOP at recruitment. Applanation velocity was the primary outcome variable with a P value of 0.025 deemed to be statistically significant following Bonferroni correction. Similarly, secondary characteristics were considered significant with a P value of 0.006 based on application of a Bonferroni correction to a P value of 0.05.
There were 586 eyes measured with the Corvis ST for this study. Of these, 153 were excluded because of unsuccessful measurement attempts, borderline or unconfirmed NTG status, use of steroid, past eye trauma and non-cataract corneal disease/surgery. Of the remaining eyes (n = 433), the left or right eye was chosen for analysis between each pair of eyes, as decided by worse severity in NTG eyes (n = 80) and random computer allocation for control eyes (n = 155) (Fig. 4).
Although the mean age of the participants was in the late 60s for both groups, there was a small subset of controls in their 20s, whereas the youngest NTG subject was aged 30 years. Overall, there were 22% more female than male study subjects, but the finding was non-significant when comparing cases with controls. All study subjects were permanent residents of Hong Kong and 97.0% of participants ethnically identified as Han Chinese. Table 2 shows the characteristics of the participants. As measured by the Corvis ST, the mean (± SD) CCT was thinner in cases than in controls (538.0 ± 31.5 μm and 555.2 ± 34.3 μm respectively, P < 0.001, and later adjusted for in the analysis) but the 2 groups were otherwise similar with regard to age, sex, and IOP. Of the NTG subjects, 28% had previously undergone glaucoma-related laser eye surgery and 76% were currently on glaucoma medication. While NTG subjects were more likely to have previously undergone cataract surgery than control subjects; these surgeries all occurred more than 3 months from the time of the Corvis ST measurement.
Corvis ST Corneal Biomechanical Measurements in the NTG and Control eyes
The primary outcome measure, inward applanation velocity, was faster in the NTG eyes (0.15 ± 0.02 m/s) than in the control eyes (0.14 ± 0.02 m/s) (P = 0.016). There was no evidence of differences between the 2 groups with regard to outward applanation velocity. Patients with NTG were 1.15 [95% confidence interval (CI), 1.03-1.28] times more likely to have an increased inward applanation velocity of at least 0.01 m/s compared with controls (P = 0.015). This remained similar when comparing NTG cases with controls, after adjustment for CCT and age (Table 3). A density map of the distribution of inward applanation velocities by NTG or control status illustrates the amount of overlap between groups (Figure 5). None of the secondary outcomes of inward and outward applanation time and length, nor highest concavity features of time, peak distance, radius, or maximum deformation, were significantly correlated with a diagnosis of NTG (Table 3).
We found that NTG eyes had faster inward applanation velocity than control eyes, independent of CCT or age. To our knowledge, this is currently the largest study cohort of NTG eyes (n = 80) examined with the Corvis ST that confirmed the applanation velocity findings found in 2 other studies.26,27
Comparison with the Literature
There have been 2 other studies examining the Corvis ST corneal biomechanics in NTG eyes with similar findings. Li et al26 showed that in 31 asymmetric NTG participants of whom the better eye was used as the control, inward applanation velocity was faster in the eye with visual field damage, with the effect size of 0.156 m/s (95% CI, 0.149-0.163) compared with 0.145 m/s (95% CI, 0.138-0.152) in the control eyes (P = 0.002). Li et al27 later confirmed this finding again, with 0.16 m/s (95% CI, 0.14-0.16) compared with 0.15 (95% CI, 0.14-0.15) m/s (P = 0.009) in a study of 37 NTG eyes where the visually progressing NTG eyes were compared with visually non-progressing NTG patients, as determined by 3 consecutive visits compared with participant’s baseline visual field measurements. Both effect sizes were similar to our study and range down to the tenth in meters per second. While these 2 papers26,27 also identify other biomechanical markers as having potential associations with NTG and progressive visual field loss, neither of them found an association with outward applanation velocity (A2 velocity), similar to our study.
Measurements of biomechanical parameters including CH and CRF in previous studies suggest that corneal structural integrity is likely to be associated with glaucoma risk. Both are surrogate measures of the cornea’s ability to absorb and dissipate energy based on a formula that may be independent of IOP. This is different from applanation velocity, which represents an inherent property of the cornea. Three studies have reported significant differences in CH and CRF between NTG and POAG.12,15,16 Two studies found NTG to be associated with about 1.20 to 1.50 mm Hg lower CH12 and CRF,12,16 suggesting weaker ability to absorb energy when compared with POAG eyes. In contrast, a study found NTG to be associated with about a 0.60 mm Hg higher CH.15 Our finding of a faster inward applanation velocity is consistent with the former 2 studies that found lower CH and CRF because they all suggest that NTG eyes have a weaker corneal structural integrity than those without glaucoma. Unfortunately, although CH and CRF measurements are available on the ORA, they cannot be obtained by the Corvis ST and thus could not be assessed in our study.
Most previous glaucoma studies using the Corvis ST have focused on POAG patients, with only some, but not all, studies including those with NTG.28-33 Interestingly, 3 of these studies29,32,33 showed POAG eyes to have slower, rather than faster, inward applanation velocity relative to normal eyes. The other 3 studies28,30,31 were inconclusive with regard to this association. Given our findings that contradict those found in the POAG studies, we speculate that the cornea of NTG and POAG patients differ in terms of corneal biomechanical pathophysiology.
Comparison with a Current Hypothesis
The leading hypothesis explaining the possible relationship between NTG and corneal biomechanics relates an inherently defective cornea to poor absorption of external energy that may lead to glaucoma. Corneal biomechanical properties are thought to be contiguous to the posterior ocular tissues and thus may act as direct markers for the viscoelastic properties of the lamina cribosa,14,34 an anatomic site considered by many to be where damage to the optic nerve occurs in glaucomatous disease.8,9,12,28 Li et al27 found NTG eyes were faster at developing a flat cornea (as similarly supported by our study) and likely to have more overall deformity in response to an air puff. Further, NTGs have lower CH and CRF,12,16 which suggest their corneas are poor at absorbing shock because they deflate quickly. It is also known that thin corneas are associated with glaucoma.24 If a flimsy cornea is less capable of absorbing energy, the energy is forced to transmit through the eyeball to the posterior portion, which could hypothetically create enough damage to the optic nerve, leading to visual field changes consistent with glaucoma.8 These gross anatomic characteristics is an explanation of how the cornea could be involved in glaucomatous optic nerve disease independent of CCT.
The authors of the studies finding a slower outward applanation velocity in POAG participants did not pose a hypothesis on why it has a converse relationship to what was found in our study with NTG eyes.29,32,33 It may be that high IOP (present in POAG patients but not NTG patients) provides resistance that slows corneal applanation velocity compared with velocity in an eye with normal pressure.
Of note, it is generally recognized that the shorter the time of corneal parameter measurement from a loading condition such as an air puff, the larger the viscoelastic contribution.35 In our study, the inward applanation velocity was measured closer to the time of air puff administration than the outward applanation velocity. Therefore, the current studies may have only observed an effect on inward applanation velocity (rather than both inward and outward) because the difference between the pathologic viscoelastic properties of the NTG cornea and a normal cornea is more apparent immediately after the loading condition.
Limitations and Strengths
This study has several limitations. First, the Corvis ST has high precision for intrarater and interrater correlation for IOP and CCT36,37 but only moderate correlation for applanation velocity.29,31 Salvetat et al29 found a mean intraclass correlation coefficient of 0.65 (95% CI, 0.34-0.83) for inward applanation velocity and 0.78 (0.61-0.86) for outward applanation velocity, suggesting low reliability. This may have reduced our power to detect associations for secondary variables and may have attenuated a relationship between our primary outcome of interest and NTG, given that there is a true association.
Second, the observed biomechanical differences could have resulted from prostaglandin topical drops,38,39 cataract surgery,40-42 or SLT43,44 which are all known to change the corneal biomechanical properties of the eyes. Patients with NTG were more likely to have undergone cataract surgery compared with controls, which may have altered the corneal structure perioperatively. We did not exclude patients with these factors so as to be representative of the true clinical effect that would be seen in the broad NTG population. However, we believe that the impact of surgical treatments was minimal since 95% of our patients had not had surgery within the past 3 months. Previous studies have shown that corneal biomechanical factors return to baseline as early as 1 week postoperatively after phacoemulsion,41 commonly after 1 month after cataract surgery,45 and 3 months after pars plana vitrectomy.42 More importantly, analysis excluding the subjects with SLT or cataract surgery had little effect on our results.
Third, it is unclear how the noncontact tonometer measurement that was taken about 0.5 hour prior to the Corvis ST study measurements may alter corneal biomechanics and should be taken into consideration. Similarly, multiple measurements on the Corvis ST may change the corneal biomechanical properties with each air puff, so only the first non-erroneous reading was used in the analysis. However, this may be less precise than taking the mean of multiple measurements.
Fourth, controls were selected from the same clinic as cases to minimize the likelihood of confounding variables. It is possible that some controls may have had undiagnosed disease, although rigorous exclusion criteria were applied in our study.
Fifth, all of our subjects were recruited in the summer, and it is unknown if corneal biomechanics change with season given the variability in ambient temperature.
Sixth, there have been several single nucleotide polymorphisms located on 1 of the 2 genes that have been linked to an increased risk of NTG in Han Chinese subjects.46 Therefore, our findings may have limited generalizability outside of ethnic Chinese populations.
Seventh, in 2016, OCULUS updated their software for the Corvis ST, notably to include a biomechanically adjusted IOP. The new parameters were designed to optimize clinical relevance. This study was conducted using an older version from 2013. Since the role of IOP in our study was limited to verifying a participant’s NTG status and comparing IOP between disease and control groups, this is unlikely to affect our results. However, it would be ideal to have the most up-to-date software that may reflect parameters of higher clinical significance.47
Lastly, this was a cross-sectional study, so while a relationship between applanation velocity and NTG could be identified, a prospective study could provide additional strength to act as a screening tool for NTG.
Strengths of this study include the number of NTG participants, which allowed for enough power to detect the findings that we observed. In addition, every effort was made to minimize the effect of potentially confounding variables. Further, our results are in alignment with other studies that had a majority of Chinese patients.26,27
To our knowledge, this is the first study with a sample size of NTG and control eyes large enough to perform a true cross-sectional comparison to assess the importance of Corvis ST-measured corneal biomechanical properties. The clinical significance of the higher inward applanation velocity in NTG patients still remains to be determined. The next step would be characterizing NTG patients using the latest version of Corvis ST software, which was designed to have more clinical significance than the earlier version.
In conclusion, NTG eyes demonstrated a small but statistically significant faster corneal inward applanation velocity than normal eyes that could reveal a possible role of the deformed cornea in causing the disease.
The researchers would like to acknowledge Ms Natalie Mok, Ms Katie Liang, Dr Sharon Chow, and Dr Lorraine Chow for their assistance in conducting this study at Queen Mary Hospital, Hong Kong and Lars Michael and Sven Reisdorf from OCULUS. This study was made possible through a MedScholars grant through the Stanford University School of Medicine.
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