REVIEW

In vivo characterization of corneal biomechanics David P. Pi~ nero, MD, PhD, Natividad Alc on, PhD

Interest in corneal biomechanics has increased with the development of new refractive surgery techniques aimed at modifying corneal properties and a variety of surgical options for corneal ectasia management. The human cornea behaves as soft biological material. It is a viscoelastic tissue and its response to a force applied to it depends not only on the magnitude of the force, but also on the velocity of the application. There are concerns about the limitations to measuring corneal biomechanical properties in vivo. To date, 2 systems are available for clinical use: the Ocular Response Analyzer, a dynamic bidirectional applanation device, and the Corvis ST, a dynamic Scheimpflug analyzer device. These devices are useful in clinical practice, especially for planning some surgical procedures and earlier detection of ectatic conditions, but further research is needed to connect the clinical measurements obtained with these devices to the standard mechanical properties. Financial Disclosure: Neither author has a financial or proprietary interest in any material or method mentioned. J Cataract Refract Surg 2014; 40:870–887 Q 2014 ASCRS and ESCRS

The cornea is the first cellular surface of the eye's optical system and contributes approximately 45 diopters (D) to the total relaxed eye optical power of about 60 D. This means that minimal changes in the cornea's shape can induce significant variations in the optical properties of the whole eye. Corneal diseases such as corneal ectasia1 as well as corneal refractive surgery2 are able to generate significant changes in the cornea's optical properties. However, changes occur in the mechanical properties as well as the optical properties. The current challenge in ophthalmology is to characterize the changes occurring in the corneal structural and mechanical properties in pathological conditions and after refractive surgery and to understand their evolution over time. It is essential to understand the consequences of modifications in the geometry of the first corneal surface after excimer laser refractive

Submitted: June 17, 2013. Final revision submitted: November 12, 2013. Accepted: November 15, 2013. From the Department of Ophthalmology (Oftalmar) (Pi~nero), Medimar International Hospital, the Fundacion para la Calidad Visual (Pi~ nero), the Departament of Optics (Pi~nero), Pharmacology and Anatomy, University of Alicante, Alicante, and the Instituto Tec nol ogico de Optica (Alcon), Color e Imagen (AIDO), Valencia, Spain. Corresponding author: David P. Pi~nero, MD, PhD, Oftalmar, Department of Ophthalmology, Medimar International Hospital, C/Padre Arrupe 20, 03016 Alicante, Spain. E-mail: [email protected].

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Q 2014 ASCRS and ESCRS Published by Elsevier Inc.

surgery or nonablative interventions such as corneal collagen crosslinking (CXL), to improve the diagnosis and management of ectatic corneal disorders such as keratoconus, and to understand the biomechanics of intraocular pressure (IOP).3 The definition of an appropriate in vivo biomechanical model is crucial for developing an accurate and precise method to evaluate corneal biomechanical properties in vivo. This task involves modeling, material characterization, simulation, visualization of changes with accurate techniques (using real time or near real time), and establishing appropriate predictive models of corneal behavior. Thus, the results obtained may be used to predict the clinical/functional outcome of different corneal surgical procedures or to define the most adequate surgical planning. To date, there are only 2 devices designed for clinical use and to provide corneal biomechanical datadthe Ocular Response Analyzer (Reichert Technologies), a dynamic bidirectional applanation device, and the Corvis ST (Oculus Optikger€ate GmbH), a dynamic Scheimpflug analyzer device. Likewise, only a few techniques have been developed and tested ex vivo for characterization of corneal biomechanics and have potential applicability to clinical practice; these include electronic speckle pattern interferometry,4 ultrasonic elastography,5 and high-frequency ultrasonographic analysis of corneal changes.6 These techniques are beyond the scope of this current review, which aims to report the scientific evidence available to date on the in vivo characterization of corneal 0886-3350/$ - see front matter http://dx.doi.org/10.1016/j.jcrs.2014.03.021

CORNEAL BIOMECHANICS: IN VIVO CHARACTERIZATION OF CORNEAL BIOMECHANICS

Figure 1. The Ocular Response Analyzer.

biomechanical properties, describing the techniques and their advantages and disadvantages and validation of the measurements obtained with each of them. DYNAMIC BIDIRECTIONAL APPLANATION Basis and Measurement Procedure In 2005, Reichert Technologies released the Ocular Response Analyzer, a device for characterizing corneal biomechanics (Figure 1). It was also presented as capable of obtaining an IOP measurement less dependent on corneal thickness than applanation tonometers. The device analyzes corneal behavior during a bidirectional applanation process induced by an air jet. Specifically, the device delivers to the eye an air pulse that causes the cornea to move inward, passing through a specific applanation state or flattening. Milliseconds after the first applanation, the pressure decreases and the cornea passes through a second applanated state while returning from concavity to

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its normal convex curvature (Figure 2). The system monitors the complete process and records 2 independent pressure valuesdP1 and P2dthat are associated with the inward and outward applanation process. These 2 pressure values are not the same due to the viscoelastic nature of the cornea.7 The dynamic bidirectional applanation device has 4 components: an infrared light emitter, a light intensity detector, a solenoid-driven air pump, and a pressure transducer inside the plenum chamber. When the measurement begins, the infrared light shines on the cornea and the intensity of the reflected light is monitored by the detector. After proper alignment with the apex of the cornea, the air pump delivers a collimated stream of air and the cornea begins to flatten. The intensity of the reflected light is maximal when the 2 flattening states are reached, and therefore the pressure values associated with them can be easily recorded. The 2 applanation changes take place within approximately 20 milliseconds. The maximum air pressure applied with this instrument is not constant and is dependent on P1, a value determined by both the true IOP and the structural resistance of each individual eye.7 The initial version of this instrument provided only 2 biomechanical parameters associated with this process: the corneal hysteresis (CH) and the corneal resistance factor (CRF). The CH is defined as the difference between the 2 pressures (P1 and P2) recorded during the measurement process described. The CRF is calculated using a linear equation and is related to the elastic properties of the cornea.8 Specifically, the CRF is derived from the formula (P1 kP2), where k is a constant. The constant k has a value determined from an empirical analysis of the relationship between both P1 and P2 and central corneal thickness (CCT).9 Other measurements provided by the instrument are the Goldmann-correlated IOP (IOPg), which is

Figure 2. Signal diagram obtained with the dynamic bidirectional applanation device in a normal eye. The red line represents the applanation signal and the green line, the pressure changes. As shown, the device delivers an air pulse to the eye, which causes the cornea to move inward achieving a specific applanation state or flattening (Pressure 1). Milliseconds after the first applanation, the pressure decreases and the cornea passes through a second applanated state (Pressure 2) while returning from concavity to its normal convex curvature.

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calculated as the mean value of P1 and P2, and the corneal-compensated IOP (IOPcc), an IOP measurement theoretically less affected by corneal properties such as the CCT because of the use of an empirically derived algorithm for its calculation. Corneal Biomechanical Parameters in the Healthy Human Eye Since its commercial release, the dynamic bidirectional applanation device has been used in many studies to characterize the corneal biomechanics in various corneal and general health conditions,10–41 as summarized in Table 1. In the normal healthy eye, studies have reported the range of normality for CH and CRF,7–14,19–21,26,28–31,33,37–41 even for different age groups. Mean values of CH between 9.3 mm Hg G 1.4 SD20 and 11.43 G 1.52 mm Hg31 and of CRF between 9.2 G 1.4 mm Hg28 and 11.9 G 1.5 mm Hg37 have been reported in the peer-reviewed literature. Therefore, there is a significant variability in CH and CRF among normal healthy individuals. It should be acknowledged that variable IOPcc could have been a confounding factor in the variability of the mean value for normal individuals. The CH has been shown to have a moderate correlation with IOP and CCT.12,42 For this reason, a low CH could be considered a risk factor for underestimation of IOP.43 Lau and Pye43 report that both CH and CRF were associated with CCT (R2 Z 0.252 and R2 Z 0.290, respectively). Kotecha et al.44 describe an IOP-independent biomechanical property of the cornea (corneal constant factor) using the Ocular Response Analyzer system that is calculated as [P1  (P2/1.27)]. This factor increases with thicker CCT and decreases with greater age: corneal constant factor Z [(0.036  CCT)  (0.028  age)] C 1.06 (adjusted R2 Z 0.34; P ! .0001 for CCT, P Z .007 for age). In contrast to CCT, the central corneal curvature does not seem to correlate with CH and CRF,45 although in a Chinese population, corneal curvature and axial length (AL) were reported to be influencing factors of CH and CRF.46 Regarding the effect of age on CH and CRF, different trends have been reported. Kamiya et al.47 report that corneal biomechanical parameters decreased with age without significant changes in CCT or IOP. Ortiz et al.8 also report that CH and CRF were statistically significantly lower in the oldest group of patients of a healthy population than in the youngest group. However, in this same study, a significant but very poor correlation was found between biomechanical parameters and age (CH, r Z 0.14, P Z .02; CRF, r Z 0.22, P Z .004).8 Kirwan et al.10 found that CH in children was similar to that reported

in adults, with no correlation with age. Some scientific evidence has shown that the cornea becomes stiffer with age.48,49 Specifically, Elsheikh et al.48 report that the cornea became considerably stiffer with age, with the behavior closely fitting an exponential power function. However, the equivalence between the reduction in CH and CRF and the increase in stiffness with age cannot be established because the relationship between biomechanical parameters and the standard mechanical properties used for the description of viscous and elastic materials, such as the modulus of elasticity, remains unclear. Glass et al.50 developed a viscoelastic model (a 3component spring and dashpot model) to illustrate how changing viscosity and elasticity may affect CH. The model was validated after confirming that measurements using high-speed photography of induced strain in a corneal phantom during measurement corresponded to predictions from the model.50 With this model, the authors demonstrated that low CH could be associated with high elasticity or low elasticity depending on the viscosity. Therefore, there is not a direct relationship between corneal CH and modulus of elasticity and this suggests that conclusions from studies using the dynamic bidirectional applanation device should be considered cautiously. Avetisov et al.51 mathematically analyzed the device's applanation curve and obtained an estimation of the elasticity coefficient (Ke), a parameter primarily characteristic of the elastic properties of the cornea. These authors obtained Ke values of 11.05 (1.6), 4.91 (1.87), and 5.99 (1.18) in normal healthy, keratoconus, and post-laser in situ keratomileusis (LASIK) groups of eyes.51 In this same study, glaucoma eyes experiencing a 2-fold reduction in IOP developed a statistically significant reduction in Ke (1.06 times lower), whereas their CH value increased 1.25 times. Another potential factor influencing biomechanical properties is ethnicity. Some authors report a tendency toward lower values of CH and CRF in black subjects compared with white subjects.13,30,52 Leite et al.30 found that after adjusting for CCT, age, AL, and corneal curvature, the difference in CH and CRF between blacks and whites lost statistical significance, which was consistent with the findings of Haseltine et al.52 The refractive error has also been found to be a factor correlated with the biomechanical parameters. Specifically, refractive error was reported to account for 4% of the variance in CRF measurements, with higher CRF values in mild to moderate myopia.53 However, in a study evaluating corneal biomechanical properties in 271 Singaporean children, Lim et al.54 found that CH and CRF were not associated with refractive error or AL. These authors also found that flatter corneas were associated with lower CH and

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Table 1. Corneal biomechanical analysis in a variety of eye and general health conditions performed with the Ocular Response Analyzer. Study* Luce7 Ortiz8

Kirwan10 Shah11 Touboul12

Song13 Schroeder14 Ang15 Chen16

Number of Eyes 339 60 165 21 81 207 93 122 159 88 78 1 153 80 82 40 41 43

Kucumen17

51

Kamiya18

36

Del Buey19

12 11 80 80 120 81 27

Goldich20 Sahin21 Kamiya22

31 Dauwe23

Shah24

Castro25

Abitbol26 Fontes27 Emre28 Shin29 Leite30

18

110 110 132 19 25 75 58 63 80 29 29 26 135 46

Sample

CH Mean (SD)

CRF Mean (SD)

Healthy eyes Keratoconus Healthy eyes Keratoconus Post-LASIK Children Healthy eyes Keratoconus Healthy eyes POAG Keratoconus Post-LASIK Children Healthy eyes POAG NTG POAG Before myopic LASIK After myopic LASIK Before phaco After phaco Before PTK After PTK Eyes with granular corneal dystrophy Healthy eyes Fuchs corneal dystrophy Healthy eyes Diabetes mellitus Healthy eyes Diabetes mellitus Before PRK After PRK Before LASIK After LASIK Before ICRS After ICRS Keratoconus Pre-LASIK Post-LASIK Keratoconus Diabetes No diabetes POAG Healthy eyes Glaucomatous eyes Mild keratoconus Healthy eyes Eyes of patients with systemic sclerosis Healthy eyes Post-PK Contralateral healthy eye Healthy eyes of blacks Healthy eyes of whites

9.6 (mean) 8.1 (mean) 10.8 (1.5) 7.7 (1.3) 9.3 (1.9) 12.5 (mean) 10.7 (2.0) 9.6 (2.2) 10.26 (mean) 9.48 (mean) 8.34 (mean) 8.87 (mean) 10.7 (1.6) 10.6 (2.2) 9.3 (2.2) 9.6 (1.3) 9.0 (1.4) 11.52 (1.28) 9.48 (1.24) 10.36 (1.48) 10.94 (2.54) 10.2 (2.2) 8.7 (1.8) d 10.3 (1.6) 6.9 (1.8) 9.3 (1.4) 10.7 (1.6) 9.51 (1.82) 10.41 (1.66) 10.8 (1.3) 9.2 (1.6) 10.8 (1.4) 8.6 (0.9) 7.7 (1.4) 7.4 (1.4) d 11.4 (1.9) 9.2 (2.1) 9.4 (2.2) 9.1 (1.9) 7.8 (1.7) d 10.46 (1.6) 8.77 (1.4) 8.50 (1.36) 10.17 (1.79) 9.8 (1.7) 9.5 (1.2) 8.95 (2.59) 10.26 (2.64) 9.7 10.4

--d 11.0 (1.6) 6.7 (1.3) 8.1 (1.9) ----d --d d d ----d 9.9 (1.4) 10.8 (1.7) 11.68 (1.40) 8.47 (1.53) 9.64 (1.26) 9.99 (1.77) 10.3 (2.0) 8.5 (1.8) d 10.5 (1.5) 8.1 (1.9) 9.6 (1.6) 10.9 (1.7) 10.36 (1.97) 10.32 (1.76) 10.3 (1.5) 8.4 (1.8) 10.3 (1.5) 7.7 (1.3) 6.6 (1.8) 6.1 (1.4) d 10.0 (1.6) 7.6 (1.8) 7.7 (2.6) d d d d d 7.85 (1.49) 10.13 (2.0) 10.0 (1.5) 9.2 (1.4) 9.78 (1.45) 9.75 (1.45) 9.84 10.70 (continued on next page)

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Table 1. (Cont.) Study* Yenerel31

Sedaghat32

Laiquzzaman33

Number of Eyes 34 36 36 63 56

Ryan34

166 34 102

Spoerl35

50

Jafarinasab36

45 23 30 30

Yazici37

Cankaya38

Morita39 Gkika40 Kara41

102 64 78 83 83 50 50 30 30

Sample Forme fruste keratoconus Clinical keratoconus Post-PK Healthy eyes Before CXL After CXL Keratoconus Healthy eyes Post-PK Before epi-LASIK 1 month after epi-LASIK 3 months after epi-LASIK 6 months after epi-LASIK 12 months after epi-LASIK Before CXL After CXL Keratoconus After PK After DALK Healthy eyes Eyes of patients with systemic lupus erythematosus Healthy eyes Exfoliation syndrome Exfoliative glaucoma Healthy eyes Normal tension glaucoma Healthy eyes Keratoconus Healthy eyes Topographically normal relatives of patients with keratoconus

CH Mean (SD)

CRF Mean (SD)

9.21 (1.38) 8.19 (1.49) 10.16 (1.93) 11.43 (1.52) 7.9 (1.5) 8.2 (1.5) d 10.6 (2.0) 8.9 (3.3) 10.22 (1.65) 8.17 (1.25) 8.46 (1.44) 8.63 (1.31) 8.53 (1.49) 7.38 (1.42) 7.37 (1.26) d 10.09 (2.5) 9.64 (2.1) 11.3 (1.3) 10.2 (0.6)

8.21 (1.64) 6.79 (1.81) 9.94 (2.34) 11.53 (1.83) 7.3 (1.4) 7.59 (1.5) d 10.2 (2.0) 8.1 (3.3) 10.01 (1.80) 7.82 (1.68) 8.03 (1.85) 7.77 (1.50) 7.80 (1.66) 6.16 (1.42) 6.16 (1.50) d 10.13 (2.2) 9.36 (2.1) 11.9 (1.5) 9.7 (1.1)

9.4 (1.4) 8.5 (1.5) 6.9 (2.1) 10.8 (1.3) 9.2 (1.3) 10.1 (1.9) 8.2 (1.4) 11.3 (1.0) 9.9 (1.6)

9.8 (1.6) 9.3 (1.8) 9.5 (2.6) 10.6 (1.4) 8.9 (1.5) 9.7 (2.4) 7.4 (2.3) 11.2 (2.1) 9.8 (1.6)

CH Z corneal hysteresis; CRF, corneal resistance factor; CXL Z corneal crosslinking; DALK Z deep anterior lamellar keratoplasty; ICRS Z intrastromal corneal ring segments; LASIK Z laser in situ assisted keratomileusis; NTG Z normal tension glaucoma; PKP Z penetrating keratoplasty; POAG Z primary open-angle glaucoma; PRK Z photorefractive keratectomy; PTK Z phototherapeutic keratectomy; SD Z standard deviation

CRF readings in contrast to the study by Franco and Lira.45 In a study aimed at evaluating biomechanical parameters in a myopic population, Plakitsi et al.55 conclude that any overall systematic changes in CH and CRF with refractive error were small compared with the considerable intersubject scatter at any level of refraction. Consistent evidence of alterations in CH and CRF has been found in only highly myopic eyes that showed decreased values of CH.56–58 Furthermore, a correlation between CH and anterior chamber depth (ACD) was reported by Chang et al.,59 suggesting that differences in corneal biomechanical parameters may indicate more generalized structural differences between eyes. In addition to the notes above, other factors can influence CH and CRF in the normal healthy eye. Studies that characterize the diurnal variations in

biomechanical parameters show a stable profile during daytime acquisitions with no statistically significant variation. 60–63 Therefore, variations in corneal biomechanical characteristics explain only a small proportion of the change in IOP measurements.60 Variations in parameters associated with the ocular pulse amplitude show that within-subject variance of CH and CRF specifically was not positively correlated with the ocular pulse amplitude; however, taking the mean of multiple repeated measurements was recommended to ensure the reliability of measurements.64 In their evaluations of the potential variation of CH and CRF in women during the menstrual cycle, Goldich et al.65 report that CH and CRF temporarily decreased at ovulation, whereas Seymeno glu et al.66 report that these biomechanical parameters did not change significantly during the phases of the menstrual cycle.

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Differences in the populations evaluated may account for this discrepancy. Reliability of Dynamic Bidirectional Applanation The intraexaminer reproducibility and interexaminer concordance of dynamic bidirectional applanation measurements have been evaluated by various authors. Moreno-Monta~ nes et al.67 report that in a normal healthy population, intraexaminer intraclass correlation coefficients (ICC) and interexaminer concordance correlation coefficients ranged from 0.78 to 0.93 and from 0.81 to 0.93, respectively, for all biomechanical parameters. The same authors confirmed that CH reproducibility was the highest, whereas IOPg reproducibility was the lowest. Wasielica-Poslednik et al.68 confirmed the good interobserver and intraobserver short-term reproducibility of CRF and CH, and Kynigopoulos et al.69 found that in normal volunteers, all biomechanical measurements had good short-term repeatability. Kopito et al.70 report reproducible CH and CRF data with the device in normal eyes. In contrast, IOPcc was less reproducible, 4 measurements per eye being necessary to reach a 10% precision and 6 for 5%. Mandalos et al.71 confirm that a high reproducibility of dynamic bidirectional applanation measurement was obtained even by inexperienced examiners when the best 3 measurements per eye were considered. Finally, Gonz alez-Meijome et al.72 evaluated the intraoffice variability of CH and CRF, confirming that both parameters remained stable among young healthy adults during the intra-officehour values. Specifically, they report that the most stable period to measure IOP and biomechanical parameters was in the afternoon.72 These studies confirm the reproducibility of the corneal biomechanical measurements provided by the device in the normal eye. However, there is a lack of scientific evidence about the Ocular Response Analyzer measurement reproducibility in the pathological eye. Curiously, the largest part of reported scientific evidence about dynamic bidirectional applanation is about the evaluation of corneal biomechanical properties in the pathological eye. Corneal Biomechanical Parameters in Glaucoma Many studies have evaluated potential corneal biomechanical alterations in glaucoma patients.14,15,25,26,39,73–89 Some authors26,73,76,78–80,85,87,88 report significantly lower CH values in different types of glaucomatous eyes than in healthy eyes (Table 1). This biomechanical alteration has been shown to be especially useful for the early diagnosis of normal tension glaucoma39,76 and also for glaucoma risk assessment in combination with CCT.37 This alteration has

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been associated with optic nerve and visual field changes.75,78,83,86,87,89 Bochmann et al.87 report that CH was significantly lower in patients with primary open-angle glaucoma (POAG) with acquired pit-like changes in the optic nerve head than in patients who did not have such structural changes in the optic disc. Anand et al.83 report significantly lower values of CH in the worse eye in cases of bilateral POAG with asymmetric visual field affectation. They also show that only CH and IOPCC could discriminate the eye with a worse visual field.83 Using multivariate generalized estimating equation models, Congdon et al.89 report that a lower CH value, but not CCT, was associated with visual field progression. Wells et al.86 report that CH but not CCT or other anterior segment parameters was associated with increased deformation of the optic nerve surface during transient elevations of IOP in glaucoma patients but not in control patients. Ang et al.15 suggest that alterations to the corneal biomechanical parameters may occur as a result of chronic raised IOP in POAG. According to this scientific evidence, a constant elevated IOP may be a determinant for biomechanical alterations of the sclera leading to deformation of the optic nerve surface and progressive visual field deterioration, assuming that scleral biomechanics are associated with corneal biomechanical properties. More studies should be conducted to confirm this hypothesis. Hirneiß et al.80 report that corneal biomechanical parameters did not differ between eyes of patients with unilateral POAG, suggesting that CH but not CRF was dependent on IOP. It should be considered that the biomechanical parameters were corrected for IOP, which is crucial for an accurate evaluation of corneal biomechanics and the conclusions of this study have a strong scientific basis. Another study evaluating CH in 317 eyes (116 POAG, 87 ocular hypertension, 47 glaucoma suspect, and 67 normal) reports that this parameter was independently associated with different variables; of these, CCT and IOP demonstrated twice as much influence on CH than did other factors.88 Pseudoexfoliation has also been proposed as a factor affecting corneal biomechanical parameters.38,81 Regarding the medical and surgical treatment of glaucoma, some studies have confirmed the recovery of corneal biomechanical parameters postoperatively.84,85,90 Iordanidou et al.84 report significant increases in CH with the lowering of IOP after deep sclerectomy with a collagen implant. Using multivariate linear regression modeling, Huang et al.90 confirmed that eyes with less ability of the ocular coat to absorb energy (lower CH) had a greater decrease in AL after trabeculectomy-induced IOP lowering. Sun et al.85 found that CH was significantly lower in chronic primary angle-closure glaucoma

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patients and experienced a partial recovery after successful IOP-lowering therapy. Corneal Biomechanical Parameters After Cataract Surgery A decrease in CH and CRF in the early postoperative period after cataract surgery has been reported by several authors (Table 1),91–95 with a recovery of these parameters to the preoperative values by 1 week to 3 months postoperatively depending on the type of corneal incision. The microincision technique was found to provide more stable corneal biomechanical parameters than standard coaxial phacoemulsification 1 month postoperatively.94 Changes in corneal thickness after surgery have been suggested as the main factor responsible for transient post-cataract-surgery corneal biomechanical alteration. Hager et al.95 concluded that postoperative corneal edema led to the change in corneal viscoelastic properties after phacoemulsification surgery, resulting in a lower damping capacity of the cornea. Corneal Biomechanical Parameters After Corneal Refractive Surgery A decrease in CH and CRF after myopic and hyperopic LASIK surgery has been reported in several studies (Table 1).8,16,22,24,96–103 The weakening of the corneal structure induced by the lamellar keratotomy and laser ablation performed during surgery is reflected in the reduction of these 2 biomechanical parameters. Uzbek et al.96 found that the biomechanical change after myopic LASIK might be predominantly due to the laser ablation, although the flap creation with a femtosecond laser does produce a biomechanical consequence consistent with reduction of corneal stiffness, as measured by the reduced amplitude of Peak 1 of the signal (not characterized by CH and CRF). With comparable flap thickness and attempted ablation volumes, myopic photoablation profiles were associated with greater decreases in CRF and CH than hyperopic profiles.100 Therefore, along with the preoperative corneal biomechanical status and the ablation volume, the spatial distribution of the ablation has been found to be an important factor affecting corneal resistance and viscous dissipative properties.100 Furthermore, thicker flaps have been found to have a greater biomechanical impact on the cornea.97,102 Most of the biomechanical changes after LASIK occurred within 1 week of surgery, and then biomechanical parameters became nearly stable.56 A minimal recovery (approximately 10% of the changes) of biomechanical parameters can be observed in some cases by 3 months after surgery.98

Significant reductions in CH and CRF have been observed after other types of corneal refractive surgery techniques, such as photorefractive keratectomy (PRK),94 laser-assisted subepithelial keratectomy (LASEK),103 and epithelial laser in situ keratomileusis.34,102 However, the amount of biomechanical change was larger after LASIK than after PRK.18 Similar reductions following LASIK and LASEK procedures have been reported, indicating that LASIK involving a thin 120 mm flap did not induce additional biomechanical change.103 In such cases, postoperative reduction in CH did not correlate with the amount or percentage of corneal tissue removed or with the optical zone or patient age.103 Corneal Biomechanical Parameters in Corneal Ectasia Several studies have demonstrated that CH and CRF are significantly reduced in keratoconic eyes compared with normal eyes (Table 1, Figure 3).8,11,24,27,41,101,104–110 This biomechanical alteration may be the consequence of the distortion of the lamellar matrix in the stroma that does not follow an orthogonal pattern, with regions of highly aligned collagen intermixed with regions in which there is little aligned collagen.111,112 In a retrospective study analyzing a large sample of keratoconic eyes,106 the corrected distance visual acuity was significantly correlated with the CRF as well as with mean keratometry, IOP, and spherical equivalence (R2 Z 0.69, P ! .01). This correlation may be the consequence of the relationship between CRF and CCT. Likewise, a significant relationship was present between CRF and corneal higher-order aberrations in keratoconic eyes (R2 Z 0.40, P ! .01), which is represented by the following expression: CRF Z 15:47  0:16  K1  0:71  RMSsph1 where K1 was the dioptric power in the flattest corneal meridian for the 3.0 mm central zone measured in diopters and RMSsph-l was the root-mean-square values corresponding to the corneal spherical-like aberrations

Figure 3. Signal diagram obtained with the dynamic bidirectional applanation device in a keratoconic eye.

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measured in microns (coefficients of the 4th and 6th Zernike orders). Hurmeric et al.113 evaluated the relationship between biomechanical parameters and confocal microscopy in normal and keratoconic eyes. They found a significant relationship between CRF and keratocyte density of the posterior half of the stroma in healthy eyes. However, no significant relationship between CH, CRF, and confocal microscopy findings were found in eyes with keratoconus. The authors conclude that these findings suggested that corneal response was related to not only the stromal matrix but also the cellular structure of the cornea. It should be mentioned that the mean CCT was 536 G 37 mm in the normal group and 473 G 36 mm in the keratoconus group. The difference between groups was statistically significant (P ! .001), and therefore the corneal thickness may have played a role in the relationships found. Despite these findings, it has been demonstrated that CH and CRF are poor parameters for discriminating between mild keratoconus and normal corneas.27 Specifically, Fontes et al.27 performed a receiver operating characteristic (ROC) curve analysis study, obtaining a poor overall predictive accuracy of CH (cutoff, 9.64 mm Hg; sensitivity, 87%; specificity, 65%; test accuracy, 74.83%) and CRF (cutoff, 9.60 mm Hg; sensitivity, 90.5%; specificity, 66%; test accuracy, 76.97%) for detecting mild keratoconus. In another study by the same research group,108 biomechanical parameters were evaluated and compared in keratoconic eyes with normal CCT and matched normal control eyes. The ROC curve analysis also showed a poor overall predictive accuracy of CH (cutoff, 9.90 mm Hg; sensitivity, 78.9%; specificity, 63.2%; test accuracy, 71.05%) and CRF (cutoff, 8.90 mm Hg; sensitivity, 68.4%; specificity, 78.9%; test accuracy, 73.65%) in detecting keratoconus. Likewise, poor overall predictive accuracy of CH (cutoff, 8.95 mm Hg; sensitivity, 63%; specificity, 23.8%; test accuracy, 44.30%) and CRF (cutoff, 7.4 mm Hg; sensitivity, 28.3%; specificity, 40.5%; test accuracy, 34.12%) was found in discriminating keratoconus from normal eyes with thin corneas.107 Galletti et al.104 demonstrated that CRF was better than CH in detecting keratoconus once the effect of CCT on biomechanical measurements was considered. Specifically, the confounding effect of CCT was controlled by stratification (20 mm CCT intervals) and linear transformation. Regarding the screening of forme fruste keratoconus, Schweitzer et al.114 found different levels of sensitivity and specificity for the detection of this condition according to CCT. Sensitivities of 91% and 81% for detection of forme fruste keratoconus were obtained in eyes with CCT less than 500 mm for CH (!9.5 mm Hg) and CRF (!9.5 mm Hg), respectively. In eyes with

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CCT between 500 mm and 539 mm, sensitivities were 91% and 87% for CH (!10.5 mm Hg) and CRF (! 10 mm Hg), respectively; in eyes with CCT between 540 mm and 579 mm, the sensitivities were 79% (CH ! 11.5 mm Hg) and 74% (CRF !11 mm Hg), respectively. Kara et al.41 obtained significantly lower CH and CRF values in the relatives of patients with keratoconus than in healthy controls. Significantly reduced values of CH and CRF have also been reported in post-LASIK ectasia as well as in the signal waveform.115–118 Ambr osio et al.116 confirmed that biomechanical measurements provided additional information that might help identify individuals at high risk for naturally occurring iatrogenic corneal ectasia. The effect of the surgical treatment of keratoconus on corneal biomechanics, specifically changes in biomechanical parameters after intrastromal corneal ring segment (ICRS) implantation23,119–121 and CXL32,35,40,122–124 have been analyzed (Table 1). Various authors report the lack of significant changes after ICRS implantation in keratoconic eyes.23,119,121 It has also been demonstrated that corrected distance visual acuity at 1 month after implantation of a specific modality of ICRS (Keraring) was significantly correlated with the preoperative mean keratometry and difference between CH and CRF (P ! .01, R2 Z 0.66).119 Gorgun et al.120 found a significant temporary decrease in CRF after femtosecond laser–assisted ICRS implantation in the early postoperative period, but neither CH nor CRF showed significant alteration from preoperative values in the late postoperative period. Different trends have been shown in biomechanical changes after CXL. Whereas most authors did not find significant changes in CH or CRF after CXL,32,35,40,122,123 Vinciguerra et al.124 report significant changes in the initial postoperative period; specifically, a significant increase in CH and CRF after CXL intraoperatively and postoperatively at the 1-month follow-up, but the change did not remain statistically significant at 6 and 12 months postoperatively. These data suggest that these 2 biomechanical metrics, CH and CRF, are not useful for analyzing in detail the biomechanical changes occurring after CXL that have been observed in ex vivo experiments.125 Another treatment option for keratoconus is corneal transplantation or keratoplasty, which is necessary in the most advanced cases. Changes in biomechanical parameters reported after keratoplasty are described in the next section. Corneal Biomechanical Parameters After Keratoplasty Corneal biomechanical parameters after penetrating keratoplasty (PKP) have been studied by

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several authors.29,31,33,36,126–128 Some conclude that PKP has a beneficial effect on corneal biomechanics in keratoconic eyes because CH and CRF parameters approach the range of normal eyes after corneal transplantation.31,127 However, others state that corneas after PKP tend to have lower CH values than normal corneas.29,33,126,128 All these outcomes should be interpreted with caution, especially when an increase in CH and CRF is considered beneficial after PKP. The deformation response after PKP is complicated by a scar between donor tissue and recipient. A small corneal area may be involved in the response that influences CH and CRF, and this should not be interpreted as beneficial. Feizi et al.127 showed that graft biomechanics were closer to normal values with larger grafts and greater donor–recipient disparity in size. When corneal biomechanics characterized by the dynamic bidirectional applanation device have been compared after PKP and after deep anterior lamellar keratoplasty (DALK), DALK has shown a more favorable outcome in terms of preservation of the biomechanical parameters of the cornea to almost normal values.126,128 However, Jafarinasab et al.36 found that DALK using the big-bubble technique for keratoconic eyes provided corneal biomechanical parameters comparable to PKP. More research on corneal biomechanics after corneal transplantation is needed, and new biomechanical metrics may be defined for this purpose. Corneal Biomechanical Parameters in Diabetes The dynamic bidirectional applanation device has been used to characterize corneal biomechanics in the diabetic population.20,21,25,129–132 Apparently contradictory outcomes have been shown (Table 1), with some studies reporting a reduction of CH and CRF in diabetic patients21,131 and others reporting the opposite.20,25,132 The main factor in these discrepancies may be the heterogeneity of the patient samples analyzed and the absence of control of IOP and CCT in most of them. For this reason, the conclusions of these studies should be considered carefully. Kotecha et al.131 found altered corneal biomechanics in diabetic patients and suggested this was related to blood glucose concentration. Scheler et al.130 reported that CH and CRF adjusted for IOP and CCT in poorly controlled diabetics were significantly higher than those in the healthy subjects and patients with wellcontrolled diabetes. In contrast, in diabetic children, CH and CRF were unaffected by fasting glucose level, HbA1c, age, or duration of diabetes. It should be remarked that in this last study, CH and CRF were adjusted for IOP and CCT and therefore the results are more conclusive.

Corneal Biomechanical Parameters in Other Ocular Conditions Studies have also evaluated corneal biomechanical changes with the dynamic bidirectional applanation system in a variety of ocular conditions (Table 1).18,19,28,37,133–135 Reduced values of CH and CRF have been reported in Fuchs corneal dystrophy,19 after phototherapeutic keratectomy in granular corneal dystrophy,18 in eyes of patients with systemic lupus erythematosus,37 and in vernal keratoconjunctivitis.133 On the other hand, biomechanical parameters were higher in eyes of patients with scleroderma28 and in nanophthalmic eyes than in the normal healthy eye.134 In a study of dry-eye patients, Firat and Diganay135 concluded that CH and CRF were not influenced by this condition. Regarding the use of specific pharmacological agents, Kara et al.136 reported that topical cyclosporine-A 0.05% did not cause changes in biomechanical parameters and Zare et al.137 reported a similar finding with the application of mitomycin-C in PRK. No significant influence on corneal biomechanical parameters has been observed after 23gauge pars plana vitrectomy in the late postoperative period.138 Corneal Biomechanical Parameters After Contact Lens Use No significant changes in CH and CRF have been reported after contact lens use.139,140 Furthermore, the use of contact lenses did not alter the repeatability of CH and CRF intraobserver measurements.141 Orthokeratology has been shown to alter corneal biomechanical parameters in the short term,141,142 with a correlation of CRF with the corneal response to reverse geometry contact lenses.142 Analysis of the Response Signal Curve Obtained by Dynamic Bidirectional Applanation To overcome the limited diagnostic performance of CH and CRF, new parameters based on analysis of the response signal curve have been developed and tested clinically.35,110,121,143–148 Touboul et al.110 defined new parameters such as the damping-induced delay, defined as the time between the moment P2 is recorded (time 2) and the time corresponding to the symmetrical position of P1 on Peak 2 (Figure 4); the full width at half maximum of the infrared signal peaks (FWHM1 and FWHM2, Figure 4); the maximum heights of the corresponding infrared signal peaks (Peaks 1 and 2, Figure 4); the peak interval time, defined as the difference between time 1 and 2; and the maximum amplitude of the green pressure curve (Pmax, Figure 4). The authors showed that the

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Figure 4. The definition of different parameters derived from the upper 25% of the applanation eak of the applanation response curve using the device's software version 3.0: heights of the peaks 1 and 2 of the infrared signal (h1, h2), widths of peaks 1 and 2 (w1, w2), rate of increase from base to peak 1 and 2 (uslope1, uslope2), rate of decrease from base to peak 1 and 2 (dslope1, dslope2), maximum single increase in the rise of peak 1 (mslew1), and maximum single decrease in the fall of peak 2 (dive 2).

combination of some of these parameters may be useful as clinical tools for the detection of keratoconus, such as the amplitude of the first infrared spike (Peak1) and its corresponding time (time 1), as well the maximum amplitude of the green pressure curve (Pmax).110 Mikielewicz et al.147 evaluated 42 parameters derived from the applanation response curve in a group of normal and keratoconic eyes. In the keratoconus group, the biomechanical evaluation was also performed after CXL and ICRS implantation. For this purpose, the software version 3.0 (Reichert Technologies), which provides a variety of parameters (Figure 4), was used (Figure 5).

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Mikielewicz et al.147 found that besides CRF, the second peak of the signal curve produced the best results in distinguishing between normal and keratoconic eyes.147 Furthermore, 2 parameters after CXL (p2area and time1) and 6 parameters after ICR implantation (aplhf, uslope11, w11, path11, time1, and deltatime) showed significant differences with respect to the preoperative conditions. A similar finding was obtained by Spoerl et al.35 after CXL. Wolffsohn et al.144 also evaluated the parameters derived from the applanation response curve in a sample of keratoconic eyes and found that the speed of corneal concave deformation past applanation was quicker (dive) with increasing keratoconus severity. In another study comparing keratoconus versus post-femtosecond LASIK eyes, 7 parameters (aplhf, w2, dslope1, aindex, uslope1, CH, and p1area) were the most useful in distinguishing between groups after statistically controlling for the differences in CCT and age, which makes the conclusions more consistent.146 Air pressure levels at inward and outward applanation and the maximum air pressure level have been found to be significantly lower and shorter in time in eyes with forme fruste keratoconus than in the normal eye, whereas the shape of the infrared signal is more variable.121 A waveform score to evaluate the reliability of the signal obtained during the measurement procedure has been described.145,148 Lam et al.148 evaluated a waveform score that judged the quality of measurement in terms of a symmetrical waveform and peaks of good magnitude using a proprietary algorithm. They concluded that signals with a waveform score of 3.50 or above may be considered acceptable, recommending taking 3 measurements for obtaining a reliable biomechanical evaluation. Ayala and Chen145 go beyond and estimated a threshold for the waveform score considering a 95% confidence interval of 7.23.

Figure 5. Parameters derived from the applanation response curve and provided by the software of the dynamic bidirectional applanation device.

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Figure 6. The Corvis ST system.

CORNEAL DEFORMATION MEASUREMENT USING SCHEIMPFLUG NONCONTACT TONOMETRY The combination of corneal topography, dynamic bidirectional applanation technology, and highspeed photography has been suggested as a potentially useful concept for integral analysis of the cornea, including corneal biomechanics. This combined technology has been called dynamic corneal topography.149 Corneal imaging can be obtained with a

Scheimpflug camera150 or using spectral optical coherence tomography.151 To this date, the only device commercially available for the clinical practice is the Corvis ST (Oculus Optikger€ate GmbH) (Figure 6). This device is a noncontact tonometer152 that allows visualizing the reaction of the cornea to an air impulse. For such purpose, a high-speed Scheimpflug-camera (4330 frames/sec) records the movements of the cornea, which are then displayed on the built-in control panel in ultra-slow motion. Specifically, the air jet of the tonometer forces the cornea through several distinct phases that are recorded on the Scheimpflug images. The ingoing phase shows the cornea passing from resting shape through applanation into a concave shape, followed shortly by what is described as an oscillation phase, before finally entering the outgoing phase, which features a second point of applanation prior to the cornea returning to its natural resting state. Analysis of the results generates 3 graphs showing deformation amplitude of the cornea, applanation length, and corneal velocity over time (Figure 7). Furthermore, IOP and corneal pachymetry data are provided in addition to some biomechanical response values. In a repeatability study of Corvis ST measurements, Hon and Lam150 found that the most repeatable corneal parameter measured by this device was CCT, followed by deformation amplitude, first applanation time (1st A-time), and IOP. Furthermore, the deformation amplitude and 1st A-time were shown to have good intersession reproducibility. In a study evaluating the intrasession repeatability of biomechanical parameters in 75 eyes of 75 healthy volunteers, Nemeth et al.153 found that the ICC was 0.758 for maximum amplitude at highest concavity, 0.784 for first applanation time, and less than 0.6 for all other biomechanical

Figure 7. Example of measurements obtained with the dynamic Scheimpflug analyzer system.

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parameters provided. According to this moderate repeatability, the authors recommend performing multiple measurements and using the average value. Reznicek et al.154 recently demonstrated that obtaining the CCT and measuring the IOP with the Corvis ST reveals good repeatability and good accuracy in healthy subjects and patients with ocular hypertension and glaucoma when compared with standardized ultrasound pachymetry or Goldmann applanation tonometry. Regarding the biomechanical data reported with this technology, Faria-Correia et al.155 found that ocular hypertension in pressure-induced stromal keratopathy was associated with lower deformation response along with steepening and thickening of the cornea. Valbon et al.156 reported that only the highest concavity time (the time from starting until the highest concavity is reached) correlated significantly with age (r Z 0.18, P Z .04) in healthy eyes, although the correlation was weak. As the Corvis ST is a relatively new technology, more studies of the applicability and capabilities of this imaging technique of characterizing corneal biomechanics are needed. BRILLOUIN OPTICAL MICROSCOPY Brillouin imaging allows visualization of the spatially heterogeneous biomechanical properties of the cornea.157,158 Specifically, Brillouin light-scattering arises from the interaction of incident light with propagating thermodynamic fluctuations, also known as acoustic phonons, in the corneal tissue.157 The frequency shift of this scattered light (U) has been shown to be related to the longitudinal elastic modulus (M0 ) by the expression   0 M Z 1=4U2 l2 r n2 where l is the optical wavelength in air, r is the mass density, and n is the refractive index. Brillouin microscopy measures the frequency shift using an ultra-high-resolution spectrometer. The conversion from the Brillouin shift to the elastic modulus requires knowledge of the index–density factor r/n2. The refractive index and density are not uniform in the cornea, primarily because of the spatial variations of hydration and water/protein content. For this reason, some approximations are done to simplify the calculations. As example, if the cornea is considered an aqueous solution of collagen fibers and extrafibrillar material with spatially varying concentrations, n can be expressed as n Z 1.335 C 0.04/ (0.22 C 0.24 H), where corneal hydration (weight%) H ranges from 3 to 4 in normal corneas, and r Z (rT C H)/(1 C H) where rT Z 1.33 is the density of dry tissue. Considering all these issues, a constant

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value of 0.57 g/cm3 for the factor r/n2 may be used.157 It should be also considered that as the structural and optical properties of the cornea are generally anisotropic, Brillouin frequency can vary according to the optical polarization state. However, they can be considered negligible compared with their variation over depth in the cornea.157 To date, only reports of the use of this technique in ex vivo experiments have been reported in the peerreviewed literature, particularly for evaluating the effect of CXL.159,160 However, some measurements in human eyes have been shown in several scientific congresses during this year (2013)A and a new commercial device is being developed for clinical use by Avedro, Inc. CONCLUSION It is essential to have in vivo evaluation of the corneal biomechanical parameters if we want to understand the behavior of corneal tissue during physical alterations, such as surgical treatments. Although many studies have evaluated these parameters, primarily using the dynamic bidirectional applanation device, it is difficult to obtain global conclusions. The interpretation of biomechanical parameters is difficult because of the complexity of the corneal viscoelastic biomechanical response. Similarly, the biomechanical response is affected by IOP and many studies have not controlled for IOP, making comparisons difficult. This shows that obtaining an accurate evaluation of the corneal characteristics and linking them with their mechanical properties is not an easy task. Additional research and clinical work is needed. New ocular refractive surgery and corrective techniques need precise and accurate methods for mechanical characterization of corneal behavior. If we can meet this challenge, we may be able to develop more adequate in vivo corneal biomechanical models and establish appropriate predictive models of corneal behavior. These tools may allow us to predict the clinical and functional outcomes of ophthalmological interventions before their application. REFERENCES ~ero DP, Alio JL, Barraquer RI, Michael R, Jime nez R. 1. Pin Corneal biomechanics, refraction, and corneal aberrometry in keratoconus: an integrated study. Invest Ophthalmol Vis Sci 2010; 51:1948–1955. Available at: http://www.iovs.org/ content/51/4/1948.full.pdf. Accessed November 30, 2013 2. McAlinden C. Corneal refractive surgery: past to present. Clin Exp Optom 2012; 95:386–398 3. Liu J, Roberts CJ. Influence of corneal biomechanical properties on intraocular pressure measurement; quantitative analysis. J Cataract Refract Surg 2005; 31:146–155 4. Jaycock PD, Lobo L, Ibrahim J, Tyrer J, Marshall J. Interferometric technique to measure biomechanical changes in the

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OTHER CITED MATERIAL A. Rajpal RK, “Phonon Spectroscopy,” presented at the XXXI Congress of the European Society of Cataract and Refractive Surgeons, Amsterdam, the Netherlands, October 2013

J CATARACT REFRACT SURG - VOL 40, JUNE 2014

First author: David P. Pi~ nero, MD, PhD Department of Ophthalmology, Medimar International Hospital, Alicante, Spain

In vivo characterization of corneal biomechanics.

Interest in corneal biomechanics has increased with the development of new refractive surgery techniques aimed at modifying corneal properties and a v...
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