Journal of Refractive Surgery

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Biomechanics 

Effect of Aging on Corneal Biomechanical Parameters Using the Ocular Response Analyzer

Kazutaka Kamiya, MD, PhD; Kimiya Shimizu, MD, PhD; Fumiko Ohmoto, MD

Abstract

Purpose:

To assess the effect of aging on corneal biomechanical parameters in a normal population.

Methods:

We prospectively examined 204 normal eyes of 204 healthy Japanese volunteers (68 men, 136 women; mean age 46.7±19.4 years [range: 19 to 89 years]). Corneal hysteresis, corneal resistance factor, corneal-compensated intraocular pressure (IOPcc), and Goldmann-correlated intraocular pressure (IOPG) were qualitatively assessed using a Reichert Ocular Response Analyzer. Central corneal thickness was measured using an ultrasound pachymeter. This measurement was performed 3 times, and the mean value obtained was used for statistical analysis. The relationships between patient age and corneal biomechanical parameters, or age and intraocular pressure (IOP), were investigated.

Results:

Mean corneal hysteresis and corneal resistance factor were 10.1±1.5 mmHg and 10.1±1.6 mmHg, respectively. Mean central corneal thickness was 539.1±30.9 μm. A weak, but significant, negative correlation was found between age and corneal hysteresis (Pearson’s correlation coefficient r=−0.17, P=.02) and corneal resistance factor (r=−0.18 P=.01). On the other hand, no significant correlation was found between age and central corneal thickness (r=−0.06, P=.41), age and IOPcc (r=−0.02, P=.82), or age and IOPG (r=−0.11, P=.11).

Conclusions:

Corneal biomechanical parameters are significantly decreased by aging without significant changes in central corneal thickness or IOP, suggesting that age-related structural changes resulting from collagen cross-linking may lead to a reduction of corneal biomechanical variables independent of central corneal thickness or IOP.

Abstract

Purpose:

To assess the effect of aging on corneal biomechanical parameters in a normal population.

Methods:

We prospectively examined 204 normal eyes of 204 healthy Japanese volunteers (68 men, 136 women; mean age 46.7±19.4 years [range: 19 to 89 years]). Corneal hysteresis, corneal resistance factor, corneal-compensated intraocular pressure (IOPcc), and Goldmann-correlated intraocular pressure (IOPG) were qualitatively assessed using a Reichert Ocular Response Analyzer. Central corneal thickness was measured using an ultrasound pachymeter. This measurement was performed 3 times, and the mean value obtained was used for statistical analysis. The relationships between patient age and corneal biomechanical parameters, or age and intraocular pressure (IOP), were investigated.

Results:

Mean corneal hysteresis and corneal resistance factor were 10.1±1.5 mmHg and 10.1±1.6 mmHg, respectively. Mean central corneal thickness was 539.1±30.9 μm. A weak, but significant, negative correlation was found between age and corneal hysteresis (Pearson’s correlation coefficient r=−0.17, P=.02) and corneal resistance factor (r=−0.18 P=.01). On the other hand, no significant correlation was found between age and central corneal thickness (r=−0.06, P=.41), age and IOPcc (r=−0.02, P=.82), or age and IOPG (r=−0.11, P=.11).

Conclusions:

Corneal biomechanical parameters are significantly decreased by aging without significant changes in central corneal thickness or IOP, suggesting that age-related structural changes resulting from collagen cross-linking may lead to a reduction of corneal biomechanical variables independent of central corneal thickness or IOP.

From the Department of Ophthalmology, University of Kitasato School of Medicine, Kanagawa, Japan.

The authors have no financial or proprietary interest in the materials presented herein.

AUTHOR CONTRIBUTIONS

Study concept and design (K.K., K.S., F.O.); data collection (K.K., K.S., F.O.); analysis and interpretation of data (K.K., K.S., F.O.); drafting of the manuscript (K.K., K.S., F.O.); critical revision of the manuscript (K.K., K.S., F.O.); statistical expertise (K.K., K.S., F.O.); administrative, technical, or material support (K.K., K.S., F.O.)

Correspondence: Kazutaka Kamiya, MD, PhD, Dept of Ophthalmology, University of Kitasato School of Medicine, 1-15-1 Kitasato, Sagamihara, Kanagawa, 228–8555, Japan. Tel: 81 42 778 9012; Fax: 81 42 778 9920; E-mail: kamiyak-tky@umin.ac.jp

Received: July 03, 2008
Accepted: November 20, 2008
Posted Online: October 12, 2009

The biomechanical properties of the cornea may affect not only the refractive outcomes after keratorefractive surgery such as LASIK or photorefractive keratectomy, leading to unpredictability of these surgical techniques,1–5 but also the measurement of intraocular pressure (IOP) in eyes undergoing keratorefractive surgery.6–9 These findings support the significance of clinical assessment of the corneal biomechanics, but the methodology for the in vivo assessment of corneal biomechanics was established only in recent years.

Considering that an increase in collagen cross-linking as a result of aging may add to the stiffness of the cornea,10–14 it is possible that corneal biomechanics may be altered in older patients. However, large cohort studies of corneal biomechanics on aging have not been conducted in an ophthalmologically normal population. The aim of this study is to prospectively investigate the relationship between patient age and corneal biomechanical factors, or age and IOP, for a wide range of ages, in healthy individuals.

Patients and Methods

Two hundred four eyes of 204 healthy Japanese individuals (68 men and 136 women) who had corneal astigmatism ≤3.00 diopters (D) and no history of corneal disease or eye surgery were enrolled in this study. Mean patient age was 46.7±19.4 years (range: 19 to 89 years). Mean manifest refraction spherical equivalent was −1.27±2.15 D (range: −6.88 to 3.88 D). Informed consent was obtained from all participants. The study adhered to the tenets of the Declaration of Helsinki. Institutional review board approval was not required for this study.

The biomechanical parameters of the cornea, such as corneal hysteresis or corneal resistance factor, were measured using an Ocular Response Analyzer (Reichert Ophthalmic Instruments, Depew, NY).15 This device utilizes a sudden air impulse to deform the cornea, and the shape changes are monitored by an electro-optical system. The puff of air induces two applanations of the cornea, inward and outward. The air stream deforms the cornea through an initial applanation event (peak 1), then beyond it into a concavity, which subsides, allowing the cornea to rebound through a second applanation (peak 2). The corneal hysteresis was calculated as the difference between pressures (mmHg) where the infrared peaks 1 and 2 occur. The corneal resistance factor was calculated as a linear function of peak 1 and peak 2, based on the results of a large-scale clinical data analysis, according to the manufacturer.16 Moreover, this device provides the two IOP measurements: Goldmann-correlated IOP (IOPG), which is the average of pressure peaks 1 and 2, and corneal-compensated IOP (IOPcc), which is less affected by corneal properties, and is intended by the manufacturer, on the basis of the results of a large-scale clinical data analysis, to be a more accurate indicator of true IOP than IOPG.16 Central corneal thickness was measured using an ultrasound pachymeter (DGH-500; DGH Technologies, Exton, Pa). This measurement was performed three times, and the average value was used for statistical analysis.

The relationship between patient age and corneal biomechanical factors such as corneal hysteresis, corneal resistance factor, and central corneal thickness, as well as that between age and IOPcc and age and IOPG was investigated. Topical anesthetic was placed in each eye before ultrasonic pachymetry. All measurements were performed at the same time of day to decrease the effect of the diurnal curve. All statistical analyses were performed using SPSS software (SPSS Inc, Chicago, Ill). The results are expressed as mean±standard deviation, and P<.05 is considered statistically significant.

Results

The demographic data of the healthy individuals are shown in the Table. Mean corneal hysteresis was 10.1±1.5 mmHg (range: 6.0 to 14.2 mmHg). Mean corneal resistance factor was 10.1±1.6 mmHg (range: 5.8 to 14.4 mmHg). Mean central corneal thickness was 539.1±30.9 μm (range: 459 to 605 μm). Mean IOPcc was 15.9±3.1 mmHg (range: 9.4 to 22.7 mmHg). Mean IOPG was 15.2±3.4 mmHg (range: 6.9 to 21.9 mmHg). A weak but significant negative correlation was found between patient age and corneal hysteresis (Pearson’s correlation coefficient r=−0.17, P=.02) (Fig 1), and age and corneal resistance factor (r=−0.18, P=.01) (Fig 2). On the other hand, no significant correlation was found between patient age and central corneal thickness (r=−0.06, P=.41) (Fig 3), patient age and IOPcc (r=−0.02, P=.82) (Fig 4), or age and IOPG (r=−0.11, P=.11) (Fig 5).

Demographic Data of 204 Eyes that Underwent Measurements with the Ocular Response Analyzer

Table: Demographic Data of 204 Eyes that Underwent Measurements with the Ocular Response Analyzer

Graph Showing a Significant Correlation Between Patient Age and the Value of Corneal Hysteresis (Pearson’s Correlation Coefficient r=−0.17, P=.02).

Figure 1. Graph Showing a Significant Correlation Between Patient Age and the Value of Corneal Hysteresis (Pearson’s Correlation Coefficient r=−0.17, P=.02).

Graph Showing a Significant Correlation Between Patient Age and the Value of Corneal Resistance Factor (Pearson’s Correlation Coefficient r=−0.18, P=.01).

Figure 2. Graph Showing a Significant Correlation Between Patient Age and the Value of Corneal Resistance Factor (Pearson’s Correlation Coefficient r=−0.18, P=.01).

Graph Showing No Significant Correlation Between Patient Age and Central Corneal Thickness (Pearson’s Correlation Coefficient r=−0.06, P=.41).

Figure 3. Graph Showing No Significant Correlation Between Patient Age and Central Corneal Thickness (Pearson’s Correlation Coefficient r=−0.06, P=.41).

Graph Showing No Significant Correlation Between Patient Age and Corneal-Compensated Intraocular Pressure (IOPcc) (Pearson’s Correlation Coefficient r=−0.02, P=0.82).

Figure 4. Graph Showing No Significant Correlation Between Patient Age and Corneal-Compensated Intraocular Pressure (IOPcc) (Pearson’s Correlation Coefficient r=−0.02, P=0.82).

Graph Showing No Significant Correlation Between Patient Age and Goldmann-Correlated Intraocular Pressure (IOPg) (Pearson’s Correlation Coefficient r=−0.11, P=.11).

Figure 5. Graph Showing No Significant Correlation Between Patient Age and Goldmann-Correlated Intraocular Pressure (IOPg) (Pearson’s Correlation Coefficient r=−0.11, P=.11).

Discussion

As shown in the results, a weak but significant negative correlation was found between age and corneal hysteresis and age and corneal resistance factor in healthy eyes. By contrast, in a different study of 86 eyes of 43 volunteers aged 19 to 68 years, we demonstrated no significant correlation between age and corneal hysteresis, but the eyes of older patients had a tendency toward lower corneal hysteresis values.17 We assume that this discrepancy can be explained by the differences in the range of patient age (19 to 68 vs 19 to 89 years) and in sample size (86 eyes vs 204 eyes). Coupled with our present and previous findings, the corneal biomechanical variables may have been decreased, especially in patients older than 70 years.

Kotecha et al18 reported in a study of patients attending the Glaucoma Research Unit that corneal hysteresis was dependent on age. However, their study group included ocular hypertension, pigment dispersion syndrome, normal tension glaucoma, and primary open angle glaucoma. Considering that glaucomatous eyes with visual field progression19 or with acquired pit-like changes of the optic nerve head20 had lower corneal hysteresis values, it remains unclear whether patient age plays a role on corneal biomechanics in healthy eyes.

Ortiz et al21 also reported that the corneal hysteresis value was lower in older eyes, and that the difference between the youngest age group (9 to 14 years) and the oldest age group (60 to 80) was statistically significant. More recently, Elsheikh et al22 demonstrated, via experimental means, that the corneal hysteresis area was significantly larger with faster loading and with decreased age, which is in accordance with our present clinical findings. On the other hand, Kirwan et al23 reported that corneal hysteresis in children was similar to that reported in adults.

Corneal hysteresis is a dynamic measure of the viscous damping in corneal tissue, which represents the energy absorption capability of the cornea, and corneal resistance factor is an indicator of the total corneal response, including the elastic resistance of corneal tissue. Our present findings suggest that the energy absorption capability as well as the elastic resistance of corneal tissue may decrease with aging. Patient age may play some role in the biomechanics of the cornea; however, the correlation between age and these parameters is weak.

It has already been demonstrated that the cornea appears to stiffen with age as a result of glycation-induced cross-linking of collagen molecules.10–14 Presently, no clear explanation exists as to why this age-related stiffening of the cornea leads to a reduction of corneal hysteresis and corneal resistance factor. Malik et al10 demonstrated that the cross-sectional area associated with each molecule in corneal collagen increased with age, and that the stroma interfibrillar spacing decreased with age. Daxer et al12 reported small but significant age-related increases in collagen fibril diameter in intermolecular spacing with the collagen fibrils and in elongation of the collagen fibrils, suggesting that these structural changes may contribute to an increase in the biomechanical parameters of the cornea. However, he also stated that age-related increases in fibril orientation and/or macroscopic dimensions may act in opposition to the biomechanics of the cornea.24 We speculate that the latter biomechanical effect may be stronger than the former, resulting in a reduction of corneal hysteresis and corneal resistance factor. We await further investigations to clarify the exact reason why these biomechanical parameters are decreased by aging.

Mean corneal hysteresis and corneal resistance factor were 10.1±1.5 mmHg and 10.1±1.6 mmHg, respectively, in our study of a normal Japanese population, figures which tended to be slightly lower than those reported in previous studies.25,26 Considering that the central corneal thickness in the Japanese population has reportedly shown a tendency to be thinner than that in other populations,27 differences of corneal thickness or of race may contribute to this tendency toward a lower corneal hysteresis in Japanese eyes. It is known that the Japanese have a higher potential risk of normal-tension glaucoma.28 More recently, Wells et al29 reported that corneal hysteresis, but not corneal thickness, was correlated with optic nerve surface compliance in glaucoma patients. Given that the cornea as well as the lamina cribrosa in an individual eye are essentially formed from extracellular matrix constituents coded for the same gene, it is possible that an eye with less viscous damping might also have an optic disc that is more vulnerable to glaucoma damage from a raised IOP. Moreover, the cornea as well as the lamina cribrosa showed a tendency, with aging, to become more rigid, less resilient structures. These results appear to support our hypothesis that the lower corneal hysteresis value accounts partly for the higher prevalence of normal tension glaucoma in the Japanese population.

Concerns exist about the relationship between corneal biomechanical factors such as corneal hysteresis or corneal resistance factor and central corneal thickness. Lu et al30 demonstrated no significant correlation between corneal hysteresis and central corneal thickness induced by wearing soft contact lenses during eye closure. On the other hand, Lam et al31 reported that corneal hysteresis was positively associated with central corneal thickness in normal eyes. Broman et al32 showed that corneal hysteresis was significantly correlated with central corneal thickness with a modest correlation coefficient in patients presenting at a glaucoma clinic. Shah et al25 also demonstrated that corneal hysteresis increased with increasing central corneal thickness in normal eyes, but the correlation was moderate. We demonstrated that central corneal thickness was the most relevant factor affecting corneal hysteresis as well as corneal resistance factor, suggesting that central corneal thickness may play an important role in the biomechanics of the cornea.17 The exact reason why both corneal hysteresis and corneal resistance factor decrease with advanced age remains unclear, but we found no significant age-related changes in central corneal thickness in this study (r=−0.06, P=.41), indicating that this age-related decrease in corneal hysteresis and corneal resistance factor cannot be explained by these changes in central corneal thickness. However, we accept that there is controversy about the age-related changes in central corneal thickness. Some studies have found a significant negative correlation between age and central corneal thickness.33–36 Others, however, have found no significant association between age and central corneal thickness.37–40 The differences of sample size, race, or methodology for pachymetric measurement may be responsible for this discrepancy. Further investigations are necessary to clarify this point.

In the current study, no significant correlation was found between patient age and IOPcc (r=−0.02, P =.82). By contrast, IOPG tended to decrease with age (r=−0.11, P=.11), although we cannot refute the possibility that these age-related changes in corneal biomechanics may induce greater errors in IOP measurements in older patients. Given that IOPG may reflect the IOP measurements with a Goldmann applanation tonometer, these findings are in good agreement with previous findings that IOP measured with a Goldmann tonometer decreased with age in the Japanese population.41–45 This indicated that the IOP adjusted by corneal biomechanical factors may remain comparatively constant despite aging, assuming that IOPcc reflects true IOP more accurately than IOPG. Unfortunately, we did not perform IOP measurements with a Goldmann tonometer in all eyes. Detailed analysis of these three IOP measurements may provide further information for more accurate IOP measurements.

To assess the repeatability of the measurements, we previously made three consecutive measurements of corneal hysteresis and corneal resistance factor with the Ocular Response Analyzer in 18 normal eyes at the same time of day on two days, showing that the mean difference between two consecutive measurements with this instrument (±95% limits of agreement) was 0.1±0.5 mmHg (range: −1.1 to 1.0 mmHg) for corneal hysteresis and 0.0±0.5 mmHg (range: −0.9 to 1.0 mmHg) for corneal resistance factor.17 In addition, Lu et al30 reported that the repeatability of corneal hysteresis was 0.8 mmHg, which is the standard deviation of the differences between two measurements. Therefore, we believe that this device offers reasonable repeatability in the evaluation of the biomechanical parameters of the cornea in normal eyes.

Corneal biomechanical parameters such as corneal hysteresis or corneal resistance factor are significantly decreased by aging without significant changes in central corneal thickness or IOP. It is suggested that age-related structural changes resulting from collagen cross-linking may lead to a reduction of corneal biomechanical factors independent of central corneal thickness or IOP. Patient age should be taken into account when assessing the biomechanics of the cornea.

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Demographic Data of 204 Eyes that Underwent Measurements with the Ocular Response Analyzer

Demographic DataMean±SD (Range)
Age (y)46.7±19.4 (19 to 89)
Gender (% female)66.7
Corneal hysteresis (mmHg)10.1±1.5 (6.0 to 14.2)
Corneal resistance factor(mmHg)10.1±1.6 (5.8 to 14.4)
Central cornea thickness (μm)539.1±30.9 (459 to 605)
Corneal-compensated IOP(mmHg)15.9±3.1 (9.4 to 22.7)
Goldmann-correlated IOP(mmHg)15.2±3.4 (6.9 to 21.9)
Authors

From the Department of Ophthalmology, University of Kitasato School of Medicine, Kanagawa, Japan.

The authors have no financial or proprietary interest in the materials presented herein.

Correspondence: Kazutaka Kamiya, MD, PhD, Dept of Ophthalmology, University of Kitasato School of Medicine, 1-15-1 Kitasato, Sagamihara, Kanagawa, 228–8555, Japan. Tel: 81 42 778 9012; Fax: 81 42 778 9920; E-mail: kamiyak-tky@umin.ac.jp

10.3928/1081597X-20090917-10

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