correlations between corneal hysteresis, intraocular pressure, and corneal central pachymetry

Correlations between corneal hysteresis,intraocular pressure, and corneal central

pachymetryDavid Touboul, MD, Cynthia Roberts, PhD, Julien Kerautret, MD, Caroline Garra,

Sylvie Maurice-Tison, MD, Elodie Saubusse, Joseph Colin, MD

PURPOSE: To analyze the correlation between corneal hysteresis (CH) measured with the OcularResponse Analyzer (ORA, Reichert) and ultrasonic corneal central thickness (CCT US) and intraoc-ular pressure measured with Goldmann applanation tonometry (IOP GA).

SETTING: Bordeaux 2 University, Ophthalmology Department, Bordeaux, France.

METHODS: This study comprised 498 eyes of 258 patients. Corneal hysteresis, corneal resistancefactor (CRF), and IOP corneal-compensated (IOPcc) were provided by the ORA device; CCT US andIOP GA were also measured in each eye. The study population was divided into 5 groups: normal(n Z 122), glaucoma (n Z 159), keratoconus (n Z 88), laser in situ keratomileusis (LASIK)(n Z 78), and photorefractive keratectomy (n Z 39). The Pearson correlation was used for statis-tical analysis.

RESULTS: Corneal hysteresis was not strongly correlated with IOP or CCT US. The mean CH in theLASIK (8.87 mm Hg) and keratoconus (8.34 mm Hg) groups was lower than in the glaucoma(9.48 mm Hg) and normal (10.26 mm Hg) groups. The lower the CH, the lower its correlationwith IOPcc and IOP GA. A CH higher than the CRF was significantly associated with the keratoconusand post-LASIK groups.

CONCLUSIONS: Corneal hysteresis, a new corneal parameter, had a moderate dependence on IOPand CCT US. Weaker corneas could be screened with ORA parameters, and low CH could beconsidered a risk factor for underestimation of IOP. The CCT US should continue to be considereda useful parameter.

J Cataract Refract Surg 2008; 34:616–622 Q 2008 ASCRS and ESCRS

ARTICLE

Knowledge of corneal biomechanical properties is im-portant in the fields of intraocular pressure (IOP)measurement, corneal pathology, and corneal refrac-tive surgery. The Ocular Response Analyzer (ORA,Reichert) is the first simple device able to providean in vivo dynamic measurement of the corneal visco-elastic parameter called corneal hysteresis (CH).

Ophthalmologists know that central corneal thick-ness (CCT) is an important concern in estimating thetrue IOP with applanation tonometric systems.1 Untilrecently, CCTwas the only available parameter to cor-relate IOP measurements by applanation in differentcorneas.2,3However, itwas recently theoretically shownthat corneal properties, specifically the elastic modu-lus, have a greater impact on IOP measurement errorin applanation tonometry than corneal thickness orcurvature.4We hypothesize that viscoelastic properties

Q 2008 ASCRS and ESCRS

Published by Elsevier Inc.

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are also important to evaluate in IOP measurement, aswell as in corneal pathology and surgery. In addition,pachymetry may influence viscoelasticity. Cornealhydration, properties of corneal layers, and the biome-chanical nature of the stroma are important to evaluate.Because of its dynamic time-measurement concept, theORA may allow us to improve our understanding inthis field.5

The aim of the current study was to define the rela-tionships between different parameters: ORA data forCH, corneal resistance factor (CRF), corneal-compen-sated IOP (IOPcc), and Goldmann-correlated IOP(IOPg) as well as Goldmann applanation tonometry(IOP GA), ultrasonic CCT (CCT US), and age. Themain objective was to evaluate CH and CRF as newcorneal parameters and to clarify their relationshipwith IOP and CCT US.

0886-3350/08/$dsee front matter

doi:10.1016/j.jcrs.2007.11.051

617CORNEAL HYSTERESIS, IOP, AND PACHYMETRY

PATIENTS AND MATERIALS

Ocular Response Analyzer Method of Operation

The patient was seated in front of the machine and wasasked to fixate on a green light. A fully automated alignmentsystem positions an air tube to a precise position relative tothe apex of the cornea. Once aligned, a 25-millisecond airpulse applies pressure to the cornea. The air pulse causesthe cornea tomove inward, past applanation and into a slightconcavity before returning to normal curvature. Corneal de-formation is recorded via an electrooptical infrared (IR) de-tection system (similar to the classical air-puff tonometers)(Figure 1). The measurement signal consists of a green sym-metric curve, which corresponds to the air-pulse pressure,and a red asymmetric curve, which corresponds to applana-tion of the cornea via the signal produced by the IR detector.The red curve has 2 principal peaks, which correspond topoints P1 and P2 on the green curve. P1 is the pressure atthe first applanation event as the cornea moves inward un-der the increasing force of air pulse (inward applanation).P1 is similar to the air-pulse system usually used in noncon-tact tonometry to measure IOP. P2 is the pressure corre-sponding to the second applanation event as the corneareturns to its normal curvature under the decreasing forceof the air pulse (outward applanation). Due to the dynamicnature of the measurement process, viscous damping inthe cornea causes delays in the inward and outward appla-nation events (energy absorption). This results in 2 differentpressure values at the inward and outward events, with thesecond outward applanation pressure always lower than thefirst inward applanation pressure (Figure 2). If abnormal cor-neal movements or surface irregularities exist, peaks may belower, wider, or otherwise irregular. If corneal structure isvery abnormal, the whole red curve could be very irregularbecause of an abnormal mechanical response. Using this bi-bidirectional applanation measurement, the ORA is able topresent 4 different parameters.

Corneal hysteresis is a function of the corneal viscous-damping properties. Corneal hysteresis is defined as the dif-ference between pressures P1 and P2 and is considered asa numerical value representing viscoelastic corneal tissueresponse to a dynamic deformation. In physics, elastic resis-tance is not a function of the rate of force application. On thecontrary, viscous damping is a function of the rate of force

Accepted for publication November 28, 2007.

From the Department of Ophthalmology (Touboul, Kerautret, Garra,Colin), Keratoconus National Center of Reference, INSERM U593(Maurice-Tisson), and Bordeaux School of Public Health (Sau-busse), Bordeaux 2 University, Bordeaux, France; and the Depart-ment of Ophthalmology (Roberts), Department of BiomedicalEngineering, Ohio State University, Columbus, Ohio, USA.

No author has a financial or proprietary interest in any material ormethod mentioned.

Presented at the annual meeting of the American Academy ofOphthalmology, Las Vegas, Nevada, USA, December 2006.

Corresponding author: David Touboul, MD, Department of Op-hthalmology, CRNK, Pr. J. Colin Ophthalmologic Unit, CHU Pelle-grin, Place Amelie Raba-Leon, 33000, Bordeaux, France. E-mail:[email protected].

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application. Therefore, CH is influenced by the rate of forceapplication and is likely linked to the stromal collagen natureand state of hydration (Rouse EJ, et al. IOVS 2007; 48:ARVOE-Abstract 1247). Normal CH values are between 8 mm Hgand 15 mm Hg.4

Corneal resistance factor is a parameter that is calculatedusing a linear combination of P1 and P2 (Luce DA. IOVS2006; 47:ARVO E-Abstract 2266). From a mathematicalstandpoint, CRF places more emphasis on P1, so it is moreheavily weighted by the underlying corneal elastic proper-ties. Normal values for CRF are similar to those for CH.

Corneal-compensated IOP is also calculated using a spe-cific linear combination of P1 and P2 (Luce DA. IOVS2006; 47:ARVO E-Abstract 2266). This IOP measurement isstrongly correlated to Goldmann tonometry but is designedto reduce the effect of corneal thickness and properties onthe IOP measurement process. As such, IOPcc should havelittle correlation with CCT US, and it has been reported toremain fairly constant after refractive surgery.6

The IOPg is a Goldmann-correlated pressure measure-ment. It is only the average of P1 and P2.

Figure 1. Ocular Response Analyzer method of operation (IR Zinfrared).

Figure 2. Corneal hysteresis calculation (IR Z infrared; ORA Z Oc-ular Response Analyzer).

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mailto:[email protected]

618 CORNEAL HYSTERESIS, IOP, AND PACHYMETRY

Survey Method

In a 10-months prospective single-center survey, a widepopulation was screened with the ORA. The survey in-cluded 498 eyes of 258 patients. The patients were age andsex matched. Five groups were established: normal (n Z122), glaucoma (n Z 159), keratoconus (n Z 88), laser insitu keratomileusis (LASIK) (n Z 78), and photorefractivekeratectomy (PRK) (n Z 39). After a complete slitlamp ex-amination was performed, ORA parameters (CH, CRF,IOP, IOPg, IOPcc), IOP GA, CCT US, sex, and age were tab-ulated in an Excel informatics program (Microsoft). Everypatient who had at least an ORA measurement and aslitlamp examination was included. Each patient’s ORAmeasurement is a mean of 4 consecutive air-puff applana-tions. Irreproducible ORA measures were excluded fromthe study by the clinician. Datawere analyzed by the authorsand by a statistician team from Bordeaux University. Onlyrelationships between parameters with an analysis-of-vari-ance P value less than 0.001 and a Pearson coefficient (r)over G0.65 were considered to have a very high level of cor-relation. For mean IOP, mean CH, and mean CRF, statisticalanalysis was performed within each group and between allgroups (Student t and Fisher-Snedecor tests).

RESULTS

Statistical results are summarized in Figures 3 and 4for the total population and for each group. Only thedark orange square values had a very high level of

Figure 3. Statistical correlations between parameters in groups (1 Znormal; 2 Z glaucoma; 3 Z keratoconus; 4 Z LASIK; 5 Z PRK). Thedark orange squares indicate significance with a high level of corre-lation (P!.001 and r O G0.65). The light orange squares indicatesignificance with a lower correlation (CCT US Z ultrasonic cornealcentral thickness; CH Z corneal hysteresis; CRF Z corneal resis-tance factor; IOPcc Z corneal-compensated intraocular pressure;IOPg Z Goldmann-correlated IOP; IOP GA Z intraocular pressuremeasured with Goldmann applanation tonometry; NS Z notsignificant).

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correlation (P!.001, r O G0.65). Age distribution ineach of the groups is described in Figure 4. Cornealhysteresis, CRF, and CCT US did not have a strongcorrelation with age (Figure 4).

Corneal hysteresis did not have a strong correlationwith IOP or CCT US. All IOP measurements werestrongly correlated with each other. The CRF wasstrongly correlated with IOPg and CCT US. In theglaucoma and LASIK groups, the CRF was less corre-lated with CCT US, although glaucoma eyedrops orthe LASIK flap cut could influence these relationships.In the keratoconus group, IOPGA and IOPcc were lesscorrelated. The CRF and CCT US were also less corre-lated, but IOP GA and CCT US were not easy to mea-sure in eyes with keratoconus.

Comparing the 3 IOP measurements within groups,the differences between the measured IOP valueswere higher in the keratoconus groupandexcimer lasersurgery groups. In all combinations in each group(IOPcc versus IOPg; IOPcc versus IOPGA; IOPg versusIOP GA, there was a statistically significant difference(P!.0001) except in the normal group, in which differ-ences between IOPcc and IOPg were not statisticallysignificant. Differences between IOPcc, IOPg, and IOPGA between groups were always statistically signifi-cant (P!.001) (Figure 5). The IOP values were lowerin the keratoconus group and excimer laser surgerygroups than in the normal group, probably due to dif-ferences in biomechanical properties in keratoconus,LASIK, and PRK when compared with normal eyes.

Analysis of CH versus IOPGA and IOPcc in the nor-mal population showed that the higher the CH, thecloser the measurements of IOPcc and IOP GA. Thetrend was the same in the LASIK Group (Figure 6).

Figure 4. Statistical correlations between parameters (CCT US Z ul-trasonic corneal central thickness; CH Z corneal hysteresis; CRF Zcorneal resistance factor; IOPcc Z corneal-compensated intraocularpressure; IOPg Z Goldmann-correlated IOP; IOP GA Z intraocularpressuremeasuredwith Goldmann applanation tonometry) and agein groups (1 Z normal; 2 Z glaucoma; 3 Z keratoconus; 4 Z LASIK;5 Z PRK) (NS Z not significant).

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In other words, when the cornea had low viscoelas-ticity (low CH), the Goldmann tonometer easily ap-planated the surface and so underestimated the trueIOP.

Analysis of CH and CRF in groups showed the CHvaluewas lower than normal in the keratoconus groupand the excimer laser surgery groups (P!.001). TheCRF value was similar in the normal and glaucomagroups, but was lower in the keratoconus group andthe excimer laser surgery groups than in the normalgroup (Figure 7).

Analysis of the mean difference between CH andCRF in all groups showed the CRF was higher than

Figure 5.Mean IOP in groups (IOP cc Z corneal-compensated intra-ocular pressure; IOP g Z Goldmann-correlated IOP; IOP GA Z in-traocular pressure measured with Goldmann applanationtonometry; KC Z keratoconus; LASIK Z laser in situ keratomileu-sis; PRK Z photorefractive keratectomy).

Figure 7.Mean CH (top) and CRF (bottom) in groups (CH Z cornealhysteresis; CRF Z corneal resistance factor; KC Z keratoconus;LASIK Z laser in situ keratomileusis; PRK Z photorefractivekeratectomy).


CH values in the normal and glaucoma groups; how-ever, CH was higher than the CRF in the keratoconusand LASIK groups (Figure 8).

Analysis of the relationship between ORA and CCTUS showed that the normal group had a trend towardpositive correlation between CH and CCT US witha weak r value (r Z 0.35). This trend was much stron-ger between CRF and CCT US (r Z 0.65) (Figures 3and 9).

Analysis of the relationship between IOP and CCTUS shows that in the normal and glaucoma groups,there was a trend toward a positive correlation be-tween IOP and CCTUSwith a weak r value (Figure 3).

Analysis of the relationship between IOPcc and IOPGA in the total population showed that IOPcc and IOPGA increased in the same proportion with age(Figure 10).

DISCUSSION

Corneal Viscoelasticity and Intraocular Pressure

In each group, measured IOP values were stronglyand positively correlated with each other, confirmingthe ORA device’s effectiveness and reliability.

In our study, CH was not strongly correlated withdifferent IOP values. However, we noticed that in all

Figure 6. Corneal hysteresis versus IOP: Left: Normal; Right: LASIK(CH Z corneal hysteresis; IOP CC Z corneal-compensated intraoc-ular pressure; IOP GA Z intraocular pressure measured with Gold-mann applanation tonometry).

Figure 8. Mean (CH � CRF) in groups (CH Z corneal hysteresis;CRF Z corneal resistance factor; KC Z keratoconus; LASIK Z laserin situ keratomileusis; PRK Z photorefractive keratectomy).



groups, the lower the CH, the wider the differencebetween IOPcc and IOP GA. Because IOPcc takesinto consideration the viscoelastic nature of the corneato evaluate the ‘‘corneal-compensated IOP,’’ we canexpect to find a significant difference between IOPccand IOP GA when tissue viscous damping is abnor-mal. In an underdamped cornea (low CH), themechanical applanation is easier than in an over-damped cornea (high CH). Thus, in all groups, theIOP GA should be underestimated in underdampedcorneas. This finding could be important in glaucomascreening or IOP measurements after corneal refrac-tive surgery. Further studies are needed to confirmthat a low CH may be a risk factor indicating thatIOPmay not be under control in glaucoma treatments7

and to confirm that the decreasing measured IOP aftercorneal refractive surgery is an artifact due to the in-duced changes in corneal properties.6

We also noticed a substantial difference between themean IOPcc and the mean IOP GA in all groups. Itcould be a problem with the ORA device calibrationor our Goldmann tonometer calibration, althoughwe checked the calibration before starting the study.

Figure 9. Mean CCT US in groups (CCT US Z ultrasonic cornealcentral thickness; KC Z keratoconus; LASIK Z laser in situ kerato-mileusis; PRK Z photorefractive keratectomy).

Figure 10.The IOPGAand IOPcc versus age in total population (IOPCC Z corneal-compensated intraocular pressure; IOP GA Z intra-ocular pressure measured with Goldmann applanation tonometry).


Another explanation is that when analyzing IOP ver-sus CH in groups, when the CH is over 11.5 mm Hg,the difference between IOPcc and IOPGA is not signif-icant. For CH less than 11.5 mmHg, the lower the CH,the greater the differences between IOP cc and IOPGA. In our population, the mean CH was approxi-mately 9.3 mm Hg in the whole population and ap-proximately 10.3 mm Hg in the normal group.Martinez-de-la-Casa et al.8 found a similar gap be-tween IOP GA and IOPcc. In addition, it has beenshown that IOP GA measurements are lower thantheir corresponding intracameral manometric pres-sures in cadaver eyes.9

Corneal Viscoelasticity and Pachymetry

The mean CCT US in each group was suitable withwhat one could expect from usual CCTUS. It is impor-tant that the mean CCT US in keratoconus was notas low as might be expected due to the inclusion oflower stages of the keratoconus disease. The eyeswith more advanced keratoconus proved to be diffi-cult to measure with the ORA because corneal surfaceirregularities caused signal variations and measure-ment fluctuations. We completed another study ofkeratoconus patients only; the study has been submit-ted for publication. In that study, the Orbscan thinnestpoint and the CCT US were dissociated, and the conelocation and keratometry was considered.

We noticed that CRF had a strong positive correla-tion with CCT US in the normal group; CH hada lower correlation. We conclude that corneal thick-ness has an important role in the damping processand more so in the elastic properties. Therefore, CCTUS should be considered in studies of corneal visco-elastic properties.10

Corneal Viscoelasticity and Age

Corneal hysteresis and CRF both seemed to be veryindependent of age in all groups. Kirwan et al.11 didnot find any differences between children and adulthysteresis. That could mean that viscoelastic cornealproperties remain constant life long. However, be-cause the CRF is positively correlated with IOP GA(r Z 0.55) and because it is well known that IOP in-creases significantly with age (in the whole populationr IOPcc Z 0.36 and r IOP GA Z 0.35), we could hy-pothesize that viscoelasticity decreases with age andthus CH and CRF variations are compensated withthe IOP elevation at the same time.

Corneal Hysteresis and Corneal Resistance FactorDifferences

Both CH and CRFwere lower than normal in abnor-mal or weak corneas such as in keratoconus, LASIK,



and PRK. This result was much more noticeable withthe CRF than with the CH. In the glaucoma group,the mean CRF was close to that in the normal group;however, the CH mean value was lower than in thenormal group.Meanwhile, themean CCTUSwas sim-ilar in both groups. We hypothesize that eyedrops forglaucoma treatment influence the corneal surface,which can explain a lower CH value (local edema,tear film weakness). In a previous study,12 small diur-nal variations in CHwere independent of IOP. Itmightbe interesting to separate patients with eyedrops fortreatment from those with only surgery to analyzethe tear-film quality in every patient.

Few patients in the normal group had CH or CRFvalues under 8 mm Hg. Almost all keratoconus andLASIK patients had CH values under 10 mm Hg.However, why did some patients in the normal grouphave a low CH value and some with true keratoconushave a normal CH value? In the first case, some nor-mal patients may have had form fruste keratoconus.(Topographic data were not acquired from all the nor-mal patients.). In the second case, the area of the mea-surement may be important in keratoconus patientswith off-centered ectasias. Another study with sys-tematic topographies is important to confirm thesehypotheses.

The differences between CH and CRF, as well as thecontributions of the elastic and viscous components tothe magnitude of these parameters, are not yet wellunderstood. BothCH andCRF are influenced by visco-elastic properties because they are both linear combina-tions of P1 and P2. A lowCHvalue could be associatedwith a high or low elastic modulus, depending on theassociated viscosity, leading to difficulties in interpre-tation (Henry DE, et al. IOVS 2007; 48:ARVO E-Abstract 1854). TheCRF, on the other hand, isweightedmore heavily by elasticity because it was designed formaximum correlation with corneal thickness (HenryDE, et al. IOVS 2007; 48:ARVO E-Abstract 1854; LuceDA. IOVS2006; 47:ARVOE-Abstract 2266).Alterationsin corneal elasticity or viscosity, by a disease process orsurgical intervention, could both influence the IOPmeasurement. However, their fluctuations may notalways be linked.

Emphasizing the difference between the inward andoutward applanation pressures, CH describes thedamping nature of the cornea (eg, collagen structure,hydration state). Furthermore, we did not find a strongcorrelation between CH and IOP GA. However, wedid find greater disparity between IOPcc and IOPGA at lower CH values. Therefore, CH can providean additional factor in interpreting the underestima-tion of true IOP by IOP GA in cases of low CH.

Emphasizing the inward applanation, CRF is morestrongly correlated with IOP and CCT US, which is


consistentwith the interpretation that it ismore heavilyweighted by corneal elasticity.

In our study, a higher CH value than CRF value wasrare in the normal and glaucoma groups, but not in thekeratoconus and LASIK groups. This finding is proba-bly due to a disharmonic vibration in the corneas witha greater lack of elasticity. This new parameter (CH �CRF), which to our knowledge we are the first to de-scribe, could be a new signature of corneal weaknessand should be interesting in form fruste keratoconusscreening. To summarize, CRF under 8 mm Hg incombination with a positive (CH � CRF), may bemore sensitive for screening of weaker corneas thana CH value under 8 mm Hg alone.

Kotecha et al.13 tried to extract more sensitivity fromthe ORA P1 and P2 values with other parameters suchas the corneal constant factor, which is an interestingconcept for prospective evaluations. In addition, al-though the eye alignment and the eye distance fromthe air puffer are well regulated by the ORA device,the applanation area is not yet well defined. Thus,knowing the applanation surface may provide addi-tional information about corneal behavior and cornealproperties. An ultrafast camera system might help de-fine the exact applanation surface during corneal de-formation. Finally, due to the applanation detectiontechnique based on IR specular reflexion, there is stilla risk for confusion between corneal surface qualityresponse and corneal biomechanics.

In conclusion, ORA viscoelasticity measurementsprovided important information for corneal biome-chanics analysis. Low CH and CRF were well corre-lated with the weakest corneas and should be helpfulin keratoconus screening as a new risk factor. TrueIOP was underestimated by Goldmann applanationtonometry in underdampened corneas and should bean interesting factor in glaucoma management.

The ORA introduces 2 very important concepts. TheCH provides a numerical value of the corneal energyabsorption capacity (damping effect). The signalshape provides a specific signature of the cornealacoustic resonance properties (memory of form). Amore precise signal shape analysis and a real-time ap-planation surface size measurement could help iden-tify corneas with abnormal biomechanical behavior.Many prospective studies are necessary to confirmthis.

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First author:David Touboul, MD

Department of Ophthalmology,Keratoconus National Center of Reference,Bordeaux, France

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http://www.iovs.org/cgi/reprint/47/12/5337




correlations between corneal hysteresis, intraocular pressure, and corneal central pachymetry

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