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 Table of Contents  
REVIEW ARTICLE
Year : 2020  |  Volume : 58  |  Issue : 2  |  Page : 94-100

Corneal biomechanics in glaucoma – A review of the current concepts and practice


Department of Glaucoma, Aravind Eye Hospital, Noombal, Chennai, Tamil Nadu, India

Date of Submission08-Mar-2020
Date of Acceptance21-Apr-2020
Date of Web Publication17-Jun-2020

Correspondence Address:
Dr. Prasanna Venkataraman
Glaucoma Services, Aravind Eye Hospital, Poonamallee High Road, Noombal, Chennai - 600 077, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/tjosr.tjosr_16_20

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  Abstract 


Intraocular pressure (IOP) is currently the only modifiable risk factor in glaucoma. Since all our efforts are directed towards maintaining a stable IOP to halt glaucoma progression, proper understanding about the science behind IOP measurement and biomechanics of cornea becomes paramount. In this paper, we address the basics of corneal biomechanics, recent developments and its impact on glaucoma diagnosis and management. An extensive literature search was done using PubMed and Google Scholar with the search terms such as biomechanics, hysteresis, and glaucoma. Relevant articles published in English language were reviewed.

Keywords: Biomechanics, glaucoma, hysteresis, intraocular pressure, ocular response analyzer


How to cite this article:
Venkataraman P, Madhuri M B, Mohan N. Corneal biomechanics in glaucoma – A review of the current concepts and practice. TNOA J Ophthalmic Sci Res 2020;58:94-100

How to cite this URL:
Venkataraman P, Madhuri M B, Mohan N. Corneal biomechanics in glaucoma – A review of the current concepts and practice. TNOA J Ophthalmic Sci Res [serial online] 2020 [cited 2020 Jul 6];58:94-100. Available from: http://www.tnoajosr.com/text.asp?2020/58/2/94/286934




  Introduction Top


Glaucoma is a chronic progressive optic neuropathy with widely known modifiable risk factor – intraocular pressure (IOP). Although there are many IOP-independent factors in glaucoma pathogenesis, we have better understanding of the IOP-dependent mechanisms in glaucoma. IOP reduction has been proven to halt glaucoma progression by many landmark studies in glaucoma. We strive to maintain a target IOP (surgically and medically), so that our patient does not become a fast progressor culminating in blindness. Since all our energy is directed toward IOP reduction, precise measurement of IOP cannot be overemphasized.

Despite the introduction of many new tonometers, the gold standard for IOP measurement is still the Goldmann applanation tonometer (GAT). It is a variable force applanation tonometer based on the Imbert-Fick principle. This principle states that the fluid pressure within a spherical body is directly proportional to the force required to flatten (or applanate) a defined area of the sphere. The assumptions include that the sphere is infinitely thin, perfectly elastic, dry, and perfectly flexible. We all know the flaws associated with this tonometer as cornea is neither a sphere nor dry. During the design of the tonometer, much thought was not invested in central corneal thickness (CCT), which was presumed to be almost the same across individuals. But with the results the Ocular Hypertension Treatment Study (OHTS), the importance of CCT came into limelight. Further research in the field of corneal biomechanics confirmed the superiority of corneal hysteresis over CCT in glaucoma management. This paper reviews impact of corneal biomechanics on glaucoma diagnosis and management. An extensive literature search was done using PubMed and Google Scholar with the search terms such as biomechanics, hysteresis, and glaucoma. Relevant articles published in English language were considered.


  Central Corneal Thickness: the Good and Bad Top


The mean CCT of healthy controls has been shown to be 520 μ with a Gaussian distribution.[1] CCT can be measured by contact and noncontact methods. The CCT derived from these methods are not interchangeable. Of the various tools available, ultrasonic pachymetry [Figure 1] remains the most reliable way of measuring CCT due to its high reproducibility.[2]
Figure 1: Ultrasound pachymeter

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GAT was designed presuming the CCT to be 500 μ, so any deviation from this value can introduce errors in measurement. Goldmann found that his tonometer underestimated IOP in thin corneas and overestimated in thick corneas. GAT considers only the external applanation force and the internal IOP. The intrinsic viscoelastic properties of the cornea can have a bigger impact on IOP measurement. The same external applanation force can cause more deformation of a soft cornea (say in corneal edema) underestimating the IOP, even though the CCT can be high. Conversely, a thin cornea with scarring may have a higher IOP reading due to increased rigidity. Collagen cross-linking used to treat keratoconus can result in corneal stiffening, leading to increase in IOP measured by GAT.[3]

Ehlers et al. found that GAT-IOP was most accurate when the CCT was 520 μ with their manometric studies.[4] They suggested a nomogram to correct GAT-IOP based on CCT, making a correction of 7 mmHg for every 100 μ deviation from 520 μ cutoff. Many investigators have attempted to design linear and nonlinear formulae to obtain a CCT-corrected GAT-IOP, but without satisfactory results. This way of correcting IOP based on CCT serves little purpose, without any measurable clinical benefit to the patient, hence best avoided.

OHTS helped us get a better insight into clinical management of our patients. Eyes that had a CCT of 555 μ or lesser had a 3-fold increased risk of conversion to glaucoma, compared with eyes that a CCT of 588 μ or greater. Furthermore, the hazard ratio for glaucoma conversion was 1.82, for each 40 μ thinning of CCT. The Early Manifest Glaucoma Trial (EMGT) also showed that a lower CCT value was a significant risk factor for progression of early manifest glaucoma in patients with a high baseline IOP. The combined OHTS European Glaucoma Prevention Study (OHTS-EGPS) model also confirmed CCT as a significant predictor for the onset of glaucoma, with every 40 μ decrease in CCT associated with a twofold risk over 5 years.

We now clearly know the impact of CCT on glaucoma, but with no validated nomogram to incorporate into clinical practice, how do we use this data? The answer lies in risk profiling of the patient. The risk factors for conversion to glaucoma in OHTS were baseline older age, higher IOP, thinner CCT, large Cup-to-Disc ratio, greater PSD in visual fields. Instead of just attempting to find the “true” corrected IOP, it would be prudent to take all the risk factors into account, determine the patient's risk and then take clinical decisions.

With the advent of refractive surgeries, CCT has gained a bigger role. The risk of intraoperative IOP spike and the post-LASIK thin CCT related IOP underestimation are the major concerns. In addition, most of these patients undergoing refractive surgery have myopia. Myopia is a known risk factor for glaucoma, compounded by the difficulty of differentiating myopic disc from glaucomatous disc. GAT and CCT-corrected IOP formulae can lead to gross underestimation of glaucoma risk in these young individuals. Hence, is there a way to circumvent CCT during tonometry?

The Pascal dynamic contour tonometer (DCT, Zeimer Ophthalmic Systems AG, Port, Switzerland) is a slit-lamp mounted, non-applanation, digital, contact tonometer [Figure 2] that provides continuous tonometry recordings to measure the IOP. It calculates the difference between systolic IOP and diastolic IOP, which is defined as the ocular pulse amplitude. It represents the pulsatile wave front produced by the varying amount of blood in the eye during the cardiac cycle [Figure 3]. The DCT measurement principle is based on contour matching of anterior corneal surface.[5] The DCT compensates for all forces exerted on the cornea and an electronic sensor measures IOP independent of the corneal properties [Figure 4].
Figure 2: Dynamic contour tonometer

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Figure 3: Ocular pulse amplitude

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Figure 4: Contour matching principle of dynamic contour tonometer

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DCT IOP is less influenced by keratorefractive surgery than GAT IOP, as shown by Kaufmann et al.[6] DCT IOP measurements seem to agree closely with manometric measurements as shown by Boehm et al.[7] DCT is a constant force tonometer, measuring IOP in a continuous fashion, requiring the probe to be in contact with the cornea for about 8 s. Thus, it is a relatively difficult technique with limited clinical adoption due to the need for patient cooperation.

Rebound Tonometer (ICare, Helsinki, Finland) is a hand-held device based on impact-induction principle [Figure 5]. It measures the deceleration of a small magnetic solenoid probe on the surface of the cornea at a distance of 4–8 mm. As the process is fast, it can be done easily even in children and uncooperative patients, without the need for a topical anesthetic. The rebounding velocity closely reflects the IOP and final IOP is displayed after six consecutive measurements. Compared to GAT, ICare overestimates IOP especially at higher CCTs.
Figure 5: ICare tonometer

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With the complexity surrounding CCT, is it possible that the effect of CCT on glaucoma could just be a tonometry artifact? Not really. Many studies including EMGT, Barbados Eye Study, Los Angeles Latino Eye Study have established CCT as an independent risk factor for glaucoma development. CCT is also one of the most heritable of the risk factors for glaucoma. A thin CCT associated with a thin lamina cribrosa might have less rigidity, leading to more displacement by IOP fluctuations.[8] Siegfried et al. associated increased trabecular exposure to oxidative damage as an important risk factor for primary open angle glaucoma (POAG) in patients with thin CCT.[9] Further research into why CCT has an influence on glaucoma has opened up the gates to corneal biomechanics and its association with lamina cribrosa physiology.


  Corneal Biomechanics: Back to Basics Top


Cornea is a complex composite of collagen, proteoglycans, water, and other elements, contributing to 45 D of the total 60 D refractive power of the eye. Hence, many refractive procedures are targeted at the cornea to correct Myopia/Hyperopia. Postrefractive procedures, the biomechanical properties of the residual bed and corneal flap are no longer the same. Using only CCT in this group of patients will make us complacent with respect to glaucoma identification and management. With the advent of collagen cross-linking for keratoconus, corneal biomechanics has gained a bigger role.

A material is said to be elastic when it has a linear relationship between stress-strain [Figure 6]. When a force is applied, the elastic material deforms and reverts back to its original state instantly when the force is removed. Young's modulus is defined as the ratio of the stress (load per unit area) and the strain (deformation/displacement per unit length). Viscoelastic materials, on the other hand, display both viscous and elastic properties, with a slow relaxation time as a portion of applied energy is dissipated.
Figure 6: Stress-strain relationship

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Cornea is a nonlinear viscoelastic structure, comprising up to 80% water in its stroma. Viscoelastic materials are characterized by hysteresis. Hysteresis, in Greek translates to “laggingbehind.” Corneal hysteresis (CH)[10] reflects the ability of corneal tissue to absorb and dissipate energy during a bidirectional applanation process. Hysteresis measures how a material responds to the loading and unloading of an applied force. In simple language, it measures the ability of the eye to absorb shock. CCT is a static geometric parameter, but hysteresis is a dynamic biomechanical property of the cornea. It can be measured with Ocular Response Analyser (ORA Reichert Ophthalmic Instruments, Depew, NY, USA), which was approved in 2005.

The ORA[11] is based on noncontact tonometer technology, which uses a 25 ms air jet to apply force to the cornea [Figure 7]. This causes the cornea to bend inward, past first applanation (P1) and after few milliseconds, the air jet is shut down, bringing the cornea back to the rest stage, past second applanation (P2). The 2 applanations are completed within a short span of 20 ms. An electro-optical collimation detector system monitors the corneal deformation.
Figure 7: Ocular response analyzer

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  Ocular Response Analyser Measurements Top


Goldmann-correlated intraocular pressure

The average of P1 and P2 provides a Goldmann-correlated IOP value referred to as IOPg. Good correlation of IOPg with GAT-IOP has been established by Ehrlich et al.[12]

Corneal hysteresis

The difference between P1 and P2 is termed corneal hysteresis (in mmHg) [Figure 8]. P1 and P2 will be the same if cornea was purely elastic, exhibiting a linear relationship during stress-strain. In reality, P2 is lower than P1, primarily because of the viscoelasticity of cornea. When applanation force is applied on the cornea it deforms to a certain degree. When the force is stopped, it regains its original shape, losing some of the energy in the process, leading to two different applanation pressures. Normal CH values are between 8 mm Hg and 15 mm Hg[13] with considerable inter-individual variation. Eyes with higher CH values can adapt better when subjected to an increase in IOP, whereas eyes with lower CH values have less tissue adaptation to deal with IOP elevation. It has been suggested by Pensyl et al.[14] that low CH eyes have higher risk of glaucomatous optic neuropathy due to reduced capacity of the eyewall to dampen IOP spikes and/or reduced ability of optic nerve structures to respond to IOP fluctuations.
Figure 8: Hysteresis measurement from Ocular Response Analyzer

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Corneal compensated intraocular pressure

Corneal compensated IOP is another measurement given by ORA. It is relatively cornea-independent, unlike other tonometers. It agrees with GAT-IOP on average, hence one can use IOPcc like GAT-IOP, except that it is less affected by corneal biomechanics.[15] It has been reported to remain fairly constant after refractive surgery.[16]

Corneal resistance factor

Corneal resistance factor (CRF) – An index of corneal resistance is calculated as P1-kP2, where k is a constant derived from empirical observation of relationship between P1, P2, and CCT. It is CCT weighted, placing more emphasis on P1 and hence heavily weighted by the elastic properties of cornea. Normal values for CRF are similar to those for CH. CRF is more affected by CCT than CH. It is more useful in corneal pathology such as keratoconus or pellucid marginal degeneration A waveform score of at least 6.5 in a software-generated scale of 0–10 is recommended by the manufacturer for a good quality measurement. If the wave score is <6.5, the test should be repeated. Clinical significance of many other parameters derived from deformation signal waveform is also being studied.

The Corneal Visualisation Scheimpflug Technology tonometer (Corvis ST tonometry: CST; Oculus, Wetzlar, Germany) is the latest instrument that allows quantitative and visual assessment of corneal biomechanics. It is a combination of noncontact air pulse tonometer with an ultrahigh speed scheimpflug camera, capturing 4330 images per se cond, helping us to directly visualize the associated corneal movement [Figure 9]. It measures CCT, deformation amplitude, applanation length and corneal velocity. It also generates a biomechanical corrected IOP, which is corrected for CCT and other corneal properties. Matsuura et al.[17] showed repeatability and usefulness in identifying glaucoma progression. Among the parameters derived from this relatively new tonometer, eyes with large highest concavity deformation amplitude [Figure 10], a large A2 length, or, small A1 deformation amplitude are at high risk of glaucoma progression. Corvis ST is also used to visualize and quantify the effect of cross-linking.
Figure 9: Corvis ST

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Figure 10: Corvis ST measurements (a-e)

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Corneal Hysteresis: How It Behaves in Normal and Abnormal Eyes?

CH is influenced by many factors: Age, CCT, IOP, glycosylated hemoglobin, glaucoma diagnosis and glaucoma severity. CH and CRF have a negative correlation with age, as cornea stiffens with age with reduced ability to dissipate energy.[18] The mean values for CH and CRF respectively were 10.49 ± 1.67 mmHg for CH and 10.50 ± 1.44 mmHg for CRF, in a study published by Pillunat et al.[19] Africans were found to have low CH and CRF than Caucasians in a study by Detry-Morel et al.[20] Corneal hysteresis is lower in patients with glaucoma, acquired optic nerve pits and corneal disorders such as Fuchs', keratoconus. Many studies have reported a positive correlation between CCT and CH and also with CRF.[21] A thicker cornea with more collagen fibers and ground substance can better resist the load of the IOP than a thinner one.

Garcia-Porta[22] noted 1–3 mmHg reduction in CH and CRF after different laser refractive treatments in their review article. The native structure of cornea is altered after these refractive surgeries which involve severing of collagen fibers to varying extent. The biomechancics of laser ablated residual stromal bed and corneal flap will not be the same as native cornea. Mardelli et al.[23] in their study on effect of photorefractive keratectomy on GAT-IOP, found a mild lowering of IOP. They proposed that the presence or absence of Bowman's membrane could alter the corneal resistance, leading to errors in GAT-IOP measurements.

Collagen cross-linking for keratoconus management significantly improves elastic modulus of cornea, but corresponding increase in CH has not been reported in many studies. This likely arises from a simultaneous change in corneal viscosity, which masks the increase in elastic modulus in the viscoelastic response measured by hysteresis.[24] In similar lines, CH is reported to be higher in diabetics, due to glycosylation of proteoglycans and/or increased collagen cross-linking.

Postpenetrating keratoplasty (PK) and Deep Anterior Lamellar Keratoplasty (DALK) eyes were reported to have low CH and CRF, with post DALK eyes faring better than post PK eyes (in terms of CH and CRF). The proposed mechanism was the intact Descemet membrane, which supports the overlying stroma in these lamellar surgeries.[22]

Increasing IOP also has an effect on CH. As IOP increases, CH decreases. As the globe stiffens from high IOP its dampening capacity decreases, resulting in larger increases in IOP from small increases in intraocular volume. The collagen fibers do not yield further and the CH becomes low. This transmits the IOP load to the weakest portion of the eye around the optic nerve head. Wells et al.[25] in their experimental study on changes in optic disc depth during IOP elevation found that CH and not CCT, had a relationship with optic disc surface compliance. CH hence reflects properties of the entire eye rather than just the cornea. It serves as a surrogate measure of the ability of the posterior segment to withstand stress.


  Corneal Hysteresis in Glaucoma: What to Expect? Top


CH and CRF are lower in POAG and pseudoexfoliation glaucoma as shown by many studies including Mangouritsas et al.[26] and Abitbol et al.[27] Narayanaswamy et al. reported that the effect was less pronounced in angle closure glaucoma, however CH values were lower compared with controls.[28] CH has a significant role to play in ocular hypertensives (OHT). CH, CRF were found to be higher in OHT than POAG in studies by Pillunat et al.[19] and Shah et al.[29] The damping effect of CH may explain why, despite high IOP, OHT patients are protected from glaucoma. As expected, CH and CRF were reported to lower in normal tension glaucoma, compared to POAG in studies by Kaushik et al.[30] and Shah et al.[29] Morita et al.[31] studied IOP and corneal mechanical properties of normal and NTG eyes and found high IOPcc, low CRF and CH in NTG eyes.

Many studies have explored CCT and CH in primary congenital glaucoma (PCG), but with mixed results. Paletta Guedes et al.[32] in their longitudinal study on PCG eyes, found that the mean CCT in PCG was thicker before surgery and became comparable to the mean CCT in a normal population after surgical treatment. Kirwan et al.[33] found CH to be lower in majority of congenital glaucoma patients.

Due to the lack of prospective studies, it is not clear whether CH is a risk factor for glaucoma progression or progressing glaucoma produces long term changes in corneal hysteresis. De Moraes et al.[34] found that progressing eyes had lower CH and CCT measurements compared with nonprogressing eyes. Medeiros et al.[35] sought to find the association between CH and glaucoma progression. They studied 68 glaucoma patients with ORA, GAT-IOP, CCT and Visual fields every 6 months for 4 years and found that eyes with CH, lesser than 10 mm Hg had significantly faster glaucoma progression. They also analyzed CH's versus CCT's predictive abilities, and found CH had greater prognostic ability than CCT; each 1 mmHg lower CH was associated with a 0.25% per-year faster rate of visual field index decline.


  Prostaglandins and Biomechanics: What Are We Really Measuring Clinically? Top


Topical medications used to treat glaucoma can have an effect on CCT and CH. Many reports have been published with conflicting results on their effect on corneal properties. Prostaglandin analogues (PGA), by activating matrix metalloproteinases, can degrade extracellular matrix compounds with a possible effect on CCT and CH.

Birt et al.[36] studied the effect of CCT on response to PGA therapy found that the thinner corneas had greater IOP reduction when analyzed at 12 weeks. In OHTS, patients with thicker corneas showed smaller IOP response to medical treatment than patients with thinner corneas. Thicker corneas which are inherently less mechanically compliant may impair drug penetration.[37] This concept of differential corneal compliance has to be kept in mind when treating patients with thicker and thinner corneas, before labeling them as “nonresponders/high responders” to certain classes of topical medications.

Bolivar et al.[38] analyzed the effect of latanoprost on CH and found it increased CH that is not related to the amount of decrease in GAT-IOP. Wu et al.[39] studied the changes in biomechanics after long term PGA therapy in POAG patients with Corvis ST and found that PGA treated eyes had higher deformation amplitude. In addition to the IOP and CCT decrease, PGA increases the corneal deformation properties also. PGA definitely produces extracellular matrix remodeling, but their direct, long-term effect on CCT and CH needs further longitudinal analyses.


  Corneal Hysteresis in Daily Glaucoma Practice: Treat Versus Monitor Top


ORA can help us measure IOP in a more objective way, making it more patient-friendly as it avoids anesthetic drops and fluorescein as well. As it is non-contact, the risk of cross-infection and sterilization concern is also eliminated.

CH has great potential in managing glaucoma suspects. These include patients with borderline IOP, inconclusive visual fields, or poor structure-function correlation. Although many investigations including ganglion cell analysis, OCT angiography and electrophysiological testing can help the clinician, CH is an easy alternative with potential role in glaucoma progression assessment. When considered together with IOP, CCT, optic disc examination, visual fields and OCT, CH can help us in risk profiling of our patients. For example, an OHT patient with thin CCT and low CH deserves more attention than a patient with thick CCT and high CH. This can help us escalate therapy in high risk individuals and provide longer follow-ups in low risk patients, thus reducing strain on patient and clinician resources. It can provide clues in understanding progression despite achieving “target IOP “and in those patients with bilateral but asymmetric disease.


  Conclusion Top


CCT is a strong independent risk factor for conversion from OHT to POAG. OHTS unveiled its importance in glaucoma management. CH is a newly described corneal biomechanical parameter which reflects the ability of the cornea to dampen IOP fluctuations. With the advent of modern refractive surgeries, CH will be a valuable addition to IOP and CCT in our understanding about glaucoma. While the hunt for an ideal tonometer is still on, understanding the inherent flaws of current tonometers and fluctuations of IOP is paramount. More longitudinal studies in the field of biomechanics can help us better incorporate CH in our everyday glaucoma practice.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]



 

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Abstract
Introduction
Central Corneal ...
Corneal Biomecha...
Ocular Response ...
Corneal Hysteres...
Prostaglandins a...
Corneal Hysteres...
Conclusion
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