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. Author manuscript; available in PMC: 2023 Jun 22.
Published in final edited form as: Curr Opin Ophthalmol. 2022 Feb 21;33(3):243–249. doi: 10.1097/ICU.0000000000000842

Corneal Hysteresis: Ready for Prime Time?

Alessandro A Jammal 1, Felipe A Medeiros 1,2
PMCID: PMC10287060  NIHMSID: NIHMS1781233  PMID: 35190508

Abstract

Purpose of the review

This review summarizes recent findings on corneal hysteresis (CH), a biomechanical property of the cornea. CH measurements can be easily acquired clinically and may serve as surrogate markers for biomechanical properties of tissues in the back of the eye, like the lamina cribrosa and peripapillary sclera, which may be related to the susceptibility to glaucomatous damage.

Recent Findings

Several studies have provided evidence of the associations between CH and clinically relevant outcomes in glaucoma. CH has been shown to be predictive of glaucoma development in eyes suspected of having the disease. For eyes already diagnosed with glaucoma, lower CH has been associated with higher risk of progression and faster rates of visual field loss over time. Such associations appear to be stronger than those for corneal thickness, suggesting that CH may be a more important predictive factor. Recent evidence has also shown that corneal-corrected intraocular pressure measurements may present advantages compared to conventional Goldmann tonometry in predicting clinically relevant outcomes in glaucoma.

Summary

Given the evidence supporting CH as an important risk factor for glaucoma development and its progression, practitioners should consider measuring CH in all patients at risk for glaucoma, as well as in those already diagnosed with the disease.

Keywords: corneal hysteresis, biomechanics, cornea, glaucoma

INTRODUCTION

Hysteresis is a mechanical property that reflects the physical behavior of a viscoelastic material after rapid loading and unloading of an applied force. Like most biological materials, structures in the eye present both elastic and viscous characteristics, and hysteresis represents the ability of a structure to absorb and dissipate mechanical shock and stress, such as elevated intraocular pressure (IOP). It is hypothesized that corneal hysteresis (CH), the only available in-vivo measurement of ocular biomechanics, may act as a surrogate marker for the biomechanical properties of tissues in the back of the eye, like the lamina cribrosa (LC) and peripapillary sclera.[1–5] In simple terms, eyes with low CH would have poor shock absorption and therefore would be more susceptible to experience damaging effects from high IOP and develop glaucoma and progress from the disease. Despite the availability of clinical instruments for many years now,[6] CH measurement is not yet as widely used in clinical practice to estimate risk in glaucoma as is central corneal thickness (CCT), even though there is evidence to suggest that CH may actually be a stronger risk factor. This review discusses the recent evidence-based findings of the use of CH in glaucoma.

CORNEAL BIOMECHANICS AND GLAUCOMA

The cornea possesses both viscous (resistance to deformation) and elastic (regaining shape after deformation) biomechanical properties. Early studies of the biomechanical properties of the cornea were based on the Young’s modulus, a representation of tissue elasticity that relates the force in an area (stress) required to generate a certain proportional deformation (strain). In vivo, clinical devices have been developed to assess corneal biomechanics by monitoring the inward and outward deformation of the cornea through applanation during rapid loading and unloading by a continuous air jet. The measurable difference in the behavior of the cornea is called hysteresis, which is attributable to the viscoelastic properties of the tissue.

Although cornea, optic nerve, and sclera do not have a common embryological origin, it has been demonstrated that the extracellular matrices of those ocular structures are mostly equivalent.[1, 3] Earlier experimental studies demonstrated that the stress/strain characteristics of the anterior segment approximated that of the whole globe.[7] More recently, Lanzagorta-Aresti et al indicated that there was a significant increase in the LC thickness and a reduction in the posterior displacement of LC after medical reduction of IOP, which were associated with CH.[5] Eyes with lower CH, had lesser LC displacement, which supports the hypothesis that lower CH may be related to stiffening of the peripapillary sclera. The reduced capability of displacement and dampening effect would increase the strain in the LC and favor glaucomatous damage at the level of the optic nerve head.[8, 9]

New evidence suggests that CH may indeed represent whole-eye hysteresis. A recently published study reported that eyes that received a scleral buckle to treat retinal detachment showed significantly lower CH than the contralateral eyes with no treatment, despite no statistically significant difference in IOP measured with Goldmann applanation tonometry (GAT) between eyes.[10] This suggests that the biomechanical properties of the sclera contribute to the measured corneal response. In fact, ex vivo and modeling studies have shown that a stiffer sclera will also display resistance when a load is applied to the cornea.[11, 12]* As the air-puff deforms the cornea inward, elastic stress is transmitted from cornea to limbus. A stiffer sclera may limit the stress wave propagation through the globe and restrict corneal deformation, which can be misinterpreted as a stiffer corneal response only.

MEASURING CORNEAL BIOMECHANICS

Currently, two different clinical devices designed to evaluate corneal biomechanical properties in vivo are commercially available. The Ocular Response Analyzer (ORA; Reichert Inc., Depew, NY, USA) uses an air jet to apply force to the cornea and an electrooptical system to measure applanation, while the Corneal Visualization Scheimpflug Technology tonometer (Corvis ST; Oculus, Wetzlar, Germany) uses a high-speed Scheimpflug camera to evaluate corneal movement.

In brief, the moment the air jet reaches the cornea, it exerts an inward pressure that leads to corneal applanation and then to corneal concavity. Milliseconds later, the airflow ceases, and the outward rebound of the cornea leads to a second corneal applanation, ultimately resuming its original shape. The ability of the cornea to resist deformation by the force applied by the air stream reflects the constitution of its extracellular matrix. For the ORA (Figure 1), CH is obtained by subtracting the IOP measurements obtained at the inward (P1) and outward (P2) applanation states. From these parameters, ORA uses a proprietary calculation to obtain a measure of “corneal-compensated” IOP (IOPcc, see section below), by using a correction factor obtained from studies of eyes undergoing LASIK refractive surgery.[6] The correction factor minimizes the impact of cornea-induced artifacts on IOP. The ORA also natively measures a corneal resistance factor (CRF), which is derived similarly as a combination of the 2 pressure measurements. However, the CRF formula reduces the value of P2 and therefore biases CRF toward the pressure at the first applanation event and to initial elastic resistance to deformation, therefore providing information on corneal stiffness (i.e., rigidity).[13]

Figure 1.

Figure 1.

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Ocular response analyzer (ORA) examination from a patient with glaucoma and low corneal hysteresis (CH). CH can be estimated by analyzing corneal responses to deformation induced by an air pulse. The pressure reaches a maximum when the cornea flattens in two occasions: P1 represents the pressure of applanation on inward corneal motion, and P2 represents the pressure of applanation on outward motion of the cornea. The difference between the 2 applanation pressures is the CH parameter. Since energy is always lost in a viscoelastic system, P2 is lower than P1, and this difference represents the dissipation of energy during the loading/unloading response (i.e., CH). The average of P1 and P2 is reported as the Goldmann correlated intraocular pressure (IOPg), and a proprietary formula is used to calculate the corneal-compensated IOP (IOPcc). The device also provides values for the corneal resistance factor (CRF) and the waveform score (WS) for quality assessment.

For the Corvis ST, a standard air puff pressure is applied between measurements. The device then produces Scheimpflug images of the first and second applanation of the cornea and a slow-motion video of the corneal deformation induced by the air pulse. The Corvis ST tonometer does not include a CH result but generates a biomechanical corrected IOP (bIOP) measurement. Previous studies suggested that bIOP is not dependent on CCT,[14] but contrary to IOPcc, bIOP seems to be dependent on CH and CRF, as measured by ORA.[15] This implies that, although bIOP is compensated for the effects of CCT in IOP measurement, effects of CH still influence bIOP. More recently, Pillunat et al[16] described a novel Corvis ST-related parameter biomechanical glaucoma factor (BGF) based on dynamic corneal response deformation and corneal thickness parameters. The parameter was able to discriminate between a small sample of healthy and normal tension glaucoma eyes with an area under the receiving operator characteristic curve (AUC) of 0.81. This finding was not replicated by Aoki and colleagues[17]** in a more diverse population with primary open angle glaucoma (POAG), who reported a much lower AUC value of 0.61 for the BGF. In comparison, the authors found a significantly higher AUC for CH from ORA (0.70) to discriminate normal eyes from eyes with POAG in their sample. Other parameters from the Corvis ST include time to and length of the first applanation, maximum deformation amplitude of the cornea radius of the curvature of the corneal concavity at the time of the maximum deformation, among others. As so far none of the Corvis ST parameters are directly comparable to the CH metric from ORA[18] and no strong evidence supports their use in glaucoma, the following sections will focus on the effect of corneal biomechanics and the IOPcc measured by the ORA.

CORNEAL HYSTERESIS AS A RISK FACTOR FOR GLAUCOMA

Earlier studies have consolidated CH as a risk factor for glaucoma, demonstrating extensively that POAG eyes present lower CH than normal controls, glaucoma suspects, and eyes with ocular hypertension (OH).[19–22] Lower CH was identified as a significant independent risk factor for conversion to glaucoma in a prospective study evaluating glaucoma suspects.[23] In that study, each 1mmHg lower CH was associated with a 20% higher risk of developing visual field defects (HR=1.20; 95% CI: 1.01–1.42; P=0.040), after adjusting for other factors such as age, IOP, CCT, and PSD. Additional evidence comes from the recent availability of population datasets, that allowed the evaluation of CH in large cohorts. The largest population study to date to investigate CH comes from the UK Biobank.[24]** The authors analyzed CH data from 93 345 eligible participants aged 40 to 69 years and observed that the proportion of self-reported glaucoma was the highest in participants with low CH and high Goldmann-correlated IOP (IOPg) from ORA. Perhaps the most remarkable finding was the demonstration of sharp increases in the proportion of patients with glaucoma at CH values less than 10.1 mmHg; from that point up, the rate of the disease remained relatively stable at approximately 1%, even with further increases in CH. The authors estimated that glaucoma and CH were significantly associated, with an odds ratio (OR) of 0.86 (95% CI: 0.79–0.94) per 1 mmHg CH increase (i.e., higher CH confers less risk). The study was limited by the use of self-reported diagnosis as an outcome for glaucoma and lack of association with functional and structural metrics. The findings give further support to a threshold of <10mmHg, which has been used as a rule of thumb for low CH when estimating risk of glaucoma based on studies with smaller cohorts of subjects.[25, 26] The study also provided interesting exploratory analysis with the association of CH and multiple clinical characteristics. The mean CH in the population was 10.6 mmHg and lower levels were significantly associated with male sex, older age, Black and Asian race, higher blood pressure, greater height, and greater myopia, in linear regression models.

Other recent studies attempted to evaluate factors linking lower CH and glaucoma. Uchida et al[27] described an association of systemic antioxidative status and CH, which may contribute to glaucoma pathogenesis. The idea was based on a previous publication by the authors that revealed that biological antioxidant potential (BAP), a systemic measure of antioxidative potential, is associated with disease severity in different groups of patients according to age and sex.[28] Further studies are necessary to confirm such findings. Other recent investigations include the association of lower CH with optic disc hemorrhage,[29] and worse visual field severity.[30]

CORNEAL-COMPENSATED IOP

CCT has been widely regarded as a risk factor for the disease since the demonstration by the Ocular Hypertension Treatment Study (OHTS) that OH eyes with thinner corneas had a higher risk of conversion to glaucoma,[31] Although lower CCT can confer less stiffness to the cornea and corneoscleral shell,[32] CCT is a simple geometric measure that does not represent the full biomechanical response of the cornea. In fact, the association between CCT and glaucoma risk may be largely confounded by the impact of CCT on IOP measurement by applanation tonometry, with IOP being overestimated or underestimated in eyes with thick or thin corneas, respectively. It should be noted that although CCT was shown in the OHTS to be a statistically independent risk factor for conversion to glaucoma, that does not imply true independence as a risk factor. Given the intrinsic relationship between CCT and GAT IOP measurements, an assessment of the independent contribution of CCT would require adjustment for IOP obtained by a method independent of CCT.[33]

IOPcc has been proposed as an alternative measurement that is less influenced by corneal artifacts than GAT IOP and may more closely represent the pressure inside the eye. Unlike GAT IOP, there appears to be little to no relationship between CCT and IOPcc.[33, 34] Susanna and colleagues[35]** investigated the association between IOP measurements by different tonometric methods and rates of visual field progression in glaucoma. Since the ultimate value of IOP measurements reside in their ability to predict clinically relevant outcomes in glaucoma, this approach would arguably represent the best method of comparing the clinical value of different tonometers. The ORA IOPcc had the strongest association with rates of visual field loss (R2 = 24.5% compared to GAT (R2 = 11.1% and the iCare tonometer (R2 = 5.8%).

CORNEAL HYSTERESIS AS A RISK FACTOR FOR PROGRESSION

Robust evidence of the association between lower CH and glaucoma progression has been published over the years. It includes estimations of the effect of CH on rates of visual field loss in patients with glaucoma,[1, 36, 37] with each 1mmHg decrease in CH associated with 55% higher chance of progression and 0.25% faster rates of visual field index (VFI) decline over time. CH has also been shown to have a significant effect on rates of structural loss. Multivariable models showed, on average, 0.13μm/year faster rates of RNFL loss for each 1 mmHg lower CH.[38]

Recent investigations have focused on the effect of CH on specific groups. Susanna et al.[39]* investigated the effects of corneal parameters in a prospective cohort of eyes that had seemingly well-controlled IOPs during follow-up (i.e., IOP below 18 mmHg in all visits). The authors observed that eyes with seemingly well-controlled IOP that still progressed over time showed both lower CH (8.6±1.3mmHg vs. 9.4±1.6mmHg; P=0.014) and thinner CCT (515.1±33.1μm vs. 531.1±42.4μm; P=0.018) than stable eyes. In multivariable models, CH was a stronger risk factor for progression in these eyes compared to CCT, with each 1 standard deviation (SD) lower (1.5mmHg) CH associated with an increase of 65% in the risk of developing visual field loss during follow-up. For CCT, each 1 SD (41μm) lower increased the risk by 56%, after adjusting for potential confounding factors.

In a historical cohort study with 1573 patients diagnosed with early-stage POAG, Jiménez‑Santos et al[40] observed that eyes with perimetric glaucoma progression during follow-up had lower CH (9.1±1.7 vs. 11.4±1.4; P<0.001) and CCT (554.5±23.2 vs. 570.8±17.7, P<0.001) than stable patients. In the multivariate analysis of their sample, each 1 mmHg of lower CH was associated with an increase of 2.13 times in the risk of progression, as assessed by a combination of visual field metrics.

A study by Estrela and colleagues,[41] evaluated the effect of interocular differences in CH, CCT, mean IOP, peak IOP and baseline MD in explaining asymmetric rates of progression in eyes with glaucoma. Despite similar IOP control and follow-up time, only asymmetry of CH (i.e., the difference in CH between right and left eyes of a patient) was a risk factor significantly associated with asymmetry in rates of change in MD between eyes in their study (r=0.22; P=0.01). For comparison, differences in CCT between eyes were not significantly correlated with asymmetry in rates of visual progression (r=−0.05, P=0.57). The authors estimated that for each 1mmHg increase in CH asymmetry in eyes of a same subject, the difference in SAP MD rates increased by 34%.

Fujino and associates[42] retrospectively evaluated the effect of CH on visual field progression in a group of 24 eyes that underwent trabeculectomy showing that lower CH was associated with faster rates of visual field loss. In another study, investigators found an inverse association between pretreatment CH and the magnitude of IOP reduction after minimally invasive glaucoma surgery.[43]

A study by Xu and Chen[44] used confocal scanning laser ophthalmoscopy (CSLO) and OCT at 4-month intervals in 146 eyes with glaucoma in China. Baseline CH was significantly associated with optic nerve head (ONH) surface depression and visual field progression (HR=0.71, P=0.014 and HR=0.54, P=0.018, respectively), but not with RNFL thinning (HR=1.03, P=0.836). Although this contradicted some previous works, the authors argued that identifiable ONH surface depression detected with CSLO may occur prior to identifiable RNFL thinning with OCT and might represent the effect of IOP on the main load-bearing structures of the ONH.

LIMITATIONS AND SPECIAL SITUATIONS

Differently from CCT, which presents relative stability during adulthood, clinicians should be aware that CH is a dynamic metric of a living tissue and can change over time. Older patients present lower values of CH. [24, 45] However, a recent longitudinal study showed that for a clinical follow-up period of up to 4.5 years, CRF and CH seemed to remain stable.[37]*

As an intrinsic biomechanical property of the cornea, CH is closely related to corneal integrity and biological activity. Therefore, CH is expected to change after corneal injury or corneal surgery, and is influenced by modifications in corneal curvature, such as corneal ectasias,[26] and after clear cornea cataract surgery.[46] Other ocular procedures and medications may also affect CH, notably those that substantially change the IOP. Earlier studies have shown an inverse relationship between corneal hysteresis and IOP, i.e., as IOP decreases, CH increases.[47, 48] Katiyar et al[49]* induced a decrease in CH by 21% by doubling IOP from 15 to 30mmHg in human eyes using a ophthalmodynamometer. CH has also been shown to significantly increase after trabeculectomy and tube shunt surgeries,[50] especially when IOP was reduced by more than 10mmHg.[51] Small CH changes have also been found in treatment-naïve patients after initiating topical prostaglandins.[52, 53] However, a more recent prospective study demonstrated that eyes under chronic use of prostaglandins had significantly lower CH, CRF and CCT.[54] These changes were reversible after 6 weeks in POAG eyes after stopping the medication.

CONCLUSION

Lower CH has been associated with the diagnosis, development, severity, and with faster progressive structural and functional loss in glaucoma. Corneal biomechanics can also partially explain why some eyes progress faster than others while maintaining a relatively normal range of IOP. In several studies comparing the two variables, CH was found to be more closely associated with glaucoma than CCT. However, the exact mechanisms explaining the role of CH in glaucoma still need clarification. The applicability of CH may potentially be enhanced in the future by its incorporation into new objective risk calculators and by therapies targeting biomechanical properties of the eye. Given the evidence supporting CH as an important risk factor for glaucoma development and its progression, practitioners should consider measuring CH in all patients at risk for glaucoma, as well as in those already diagnosed with the disease.

KEY POINTS.

  • As a measure of corneal biomechanical properties, it is hypothesized that CH may act as a surrogate marker for the biomechanical properties of tissues in the back of the eye, like the lamina cribrosa (LC) and peripapillary sclera which are linked to glaucoma susceptibility.

  • CH has been shown to be a risk factor for development of visual field loss in eyes suspected of glaucoma.

  • In eyes already diagnosed with glaucoma, lower CH is associated with higher risk of progression and faster rates of visual field loss.

  • By correcting for corneal-induced artifacts, IOPcc measurements show a stronger relationship with rates of glaucoma progression than IOP obtained with Goldmann tonometry.

  • Practitioners should consider measuring CH in all patients at risk for glaucoma, as well as in those already diagnosed with the disease.

Financial Support and Sponsorship

Supported in part by National Institute of Health/National Eye Institute grant EY029885 and EY031898 (FAM). The funding organizations had no role in the design or conduct of this research.

Footnotes

Conflicts of Interest

A.A.J.: none. F.A.M.: Aerie Pharmaceuticals (C); Allergan (C, F), Annexon (C); Biogen (C); Carl Zeiss Meditec (C, F), Galimedix (C); Google Inc. (F); Heidelberg Engineering (F), IDx (C); nGoggle Inc. (P), Novartis (F); Stealth Biotherapeutics (C); Reichert (C, F)

REFERENCES

Papers of particular interest, published within the period of review, have been highlighted as: * = of special interest, ** = of outstanding interest

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