ORIGINAL STUDY
Dynamic Scheimpflug Ocular Biomechanical Parameters
in Healthy and Medically Controlled Glaucoma Eyes
Atsuya Miki, MD, PhD,* Yuichi Yasukura, MD,*† Robert N. Weinreb, MD,‡
Tomomi Yamada, PhD,§ Shizuka Koh, MD, PhD,*∥
Tomoko Asai, MD, PhD,*¶ Yasushi Ikuno, MD,*#
Naoyuki Maeda, MD, PhD,* and Kohji Nishida, MD, PhD*
Purpose: To evaluate the relationship between biomechanical
parameters measured with a dynamic Scheimpflug analyzer and
glaucoma.
Patients and Methods: Cross-sectional observational data of 47 eyes
of 47 consecutive subjects with medically controlled primary open-
angle glaucoma and 75 eyes of 75 healthy subjects examined with a
dynamic Scheimpflug analyzer (Corvis ST) were retrospectively
investigated. Eight biomechanical parameters were compared
between eyes with and without glaucoma using multivariable
models adjusting for intraocular pressure (IOP), central corneal
thickness, age, and axial length.
Received for publication January 11, 2019; accepted March 24, 2019.
From the *Department of Ophthalmology, Osaka University Graduate
School of Medicine; †Department of Ophthalmology, Yodogawa
Christian Hospital; §Department of Medical Innovation, Data
Coordinating Center, Osaka University Hospital; ∥Department of
Innovative Visual Science, Osaka University Graduate School of
Medicine; #Ikuno Eye Center, Osaka; ¶Asai Eye Clinic, Hyogo,
Japan; and ‡Viterbi Department of Ophthalmology and Shiley Eye
Institute, Hamilton Glaucoma Center, University of California, San
Diego, La Jolla, CA.
Disclosure: A.M.: reports personal fees from Santen Pharmaceutical,
Pfizer Japan, Kowa Co. Ltd., Otsuka Pharmaceutical, Alcon Pharma,
Scampo Pharma, Senju Pharmaceutical, Novartis Pharma, Topcon,
Ellex Inc., HOYA, and JFC sales plan, and a grant from JSPS,
outside the submitted work. R.N.W.: reports research support from
Carl Zeiss Meditec, Genentech, Heidelberg Engineering, Konan,
Optovue, Tomey, Topcon, Allergan, Bausch & Lomb, ForSight, and
Unity, National Eye Institute (R01EY029058) and an unrestricted
grant from Research to Prevent Blindness (New York, NY). S.K.:
reports personal fees from Johnson & Johnson, Alcon Pharma,
Santen Pharmaceutical, Otsuka Pharmaceuticals, Menicon, Oculus,
Shire, and SEED, and research support from JSPS and Johnson &
Johnson, outside the submitted work. Y.I.: reports personal fees from
Novartis, Bayer, Alcon Surgical, Senju Pharmaceutical, Santen, and
research support from Tomey, outside the submitted work. N.M.:
reports personal fees from Santen Pharmaceutical, Otsuka Pharma-
ceuticals, Topcon, Abbott Medical Optics, Johnson & Johnson, and
Tomey, and research support from Alcon Laboratories, outside the
submitted work. K.N.: reports personal fees from Otsuka Pharma-
ceutical, Abbott Medical Optics Japan, HOYA, Wacamoto, MSD,
Pfizer, Novartis, Santen, Johnson & Johnson, Senju, and Takeda, and
research support from Otsuka Pharmaceuticals, HOYA, Wakamoto,
Pfizer, Novartis, Santen, and Menicon, and grants from NIBIOHN,
MEXT, NEDO, and JSPS, outside the submitted work. The
remaining authors declare no conflict of interest.
Reprints: Atsuya Miki, MD, PhD, Department of Ophthalmology,
Osaka University Graduate School of Medicine, 2-2 Yamada-Oka,
Suita, Osaka 565-0871, Japan (e-mail: amiki@ophthal.med.osaka-u.
ac.jp).
Supplemental Digital Content is available for this article. Direct URL
citations appear in the printed text and are provided in the HTML
and PDF versions of this article on the journal’s website, www.
glaucomajournal.com.
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
DOI: 10.1097/IJG.0000000000001268
588 | www.glaucomajournal.com J Glaucoma  Volume 28, Number 7, July 2019
Copyright r 2019 Wolters Kluwer Health, Inc. All rights reserved.
Results: In multivariable models, glaucoma was negatively corre-
lated with A1 time (P < 0.001, coefficient = −0.5535), A2 time
(P = 0.008, coefficient = −0.1509), radius (P = 0.011, coefficient =
−0.4034), and whole eye movement (P < 0.001, coefficient =
−0.0622). Negative correlation between glaucoma and 3 parameters
(A1 time, A2 time, and radius) consistently indicate larger
deformability of the cornea and negative correlation between
glaucoma and whole eye movement indicate smaller eye movement,
in glaucoma eyes. There were significant correlations of many bio-
mechanical parameters with other baseline factors (8 parameters
with IOP, 2 with central corneal thickness, 4 with age, and 7 with
axial length).
Conclusions: Eyes with medically controlled glaucoma were more
deformable than healthy eyes, which may increase the risk of optic
nerve damage through an underestimation of IOP and bio-
mechanical vulnerability of the globe. Many parameters showed a
significant correlation with baseline factors, suggesting the impor-
tance of adjustment for these confounding factors when evaluating
the correlation between biomechanical parameters and ocular dis-
eases. These results suggest the relevance of measuring biomechanical
properties of glaucoma eyes for accurate IOP measurement and risk
assessment.
Key Words: glaucoma, biomechanics, cornea, intraocular pressure,
Scheimpflug photography
(J Glaucoma 2019;28:588–592)
C linical relevance of cornea-related factors to glaucoma
is evidenced by studies reporting the association
between thin cornea and an increased risk for glaucoma.1
Positive correlation between corneal thickness and measured
intraocular pressure (IOP) is one possible mechanism link-
ing cornea to glaucoma.2 However, biomechanical proper-
ties of the cornea could have a more significant impact on
glaucoma susceptibility than corneal thickness, which is
only one aspect of biomechanical properties.3 In addition,
the biomechanical characteristics of the cornea might
somehow reflect those of the optic nerve head (ONH) and
the peripapillary sclera. Therefore, evaluation of ocular
biomechanics in glaucoma eyes is necessary for accurately
estimating IOP and calculating risk for glaucoma.
The ocular response analyzer (ORA) was the first clinical
device for in vivo evaluation of biomechanical properties by
measuring an applied force-displacement relationship during
air-puff tonometry.4 The ORA measures corneal hysteresis
(CH), the difference between the inward applanation pressure
and the outward applanation pressure.4,5 Previous studies
have shown associations between CH and glaucoma.6–8
However, the ORA has not been widely used because of its
limitations as a diagnostic tool.5
J Glaucoma  Volume 28, Number 7, July 2019
Another device, the dynamic Scheimpflug analyzer
(Corvis ST, Oculus, Germany), captures ultra–high-speed
dynamic images of the cornea during air-puff–induced
deformation.9 It is potentially superior to simply measure
CH in that it provides a variety of biomechanical parame-
ters and compensates for the movement of whole globe.
Alterations of dynamic Scheimpflug parameters in glau-
comatous eyes have been reported.10–13 However, results of
these previous studies are discrepant, which may be
explained in part by the confounding effects of other base-
line factors such as IOP, central corneal thickness (CCT),
age, and axial length.11,9–16 Most previous studies compen-
sate for none or only a part of these factors.10–13 Therefore,
re-evaluation of the relationship between glaucoma and
Corvis parameters with adjustments for possible confound-
ing factors is required.
In this study, we investigated the difference in bio-
mechanical parameters measured with the dynamic Scheimp-
flug analyzer between glaucomatous eyes and healthy eyes.
MATERIALS AND METHODS
Participants and Design
This was a retrospective, cross-sectional, observational
study investigating consecutive patients with glaucoma and
healthy subjects who were examined using the Corvis ST
from June 2012 to October 2017 at Osaka University Hos-
pital. Exclusion criteria included closed angles, secondary
causes of glaucoma, history of any intraocular or corneal
surgery, or other intraocular diseases except for cataract.
Approximately 10.3% of the examinations were excluded
from the research database because “QS” was not OK. QS is
a quality score for the reliability of the measurements which
is calculated by the analyzing software based on edge
detection, alignment, and pressure property. Glaucoma was
defined by the optic disc appearance (presence of neuro-
retinal rim thinning, excavation, notching, or characteristic
retinal nerve fiber layer defect) based on fundus photog-
raphy and corresponding visual field abnormality in stand-
ard automated perimetry based on Anderson and Patella
criteria17 of 1 or more of the following: a cluster of 3 or
more nonedge points with a P < 5%, including 1 point or
more with a P < 1%, on the pattern deviation map in at least
1 hemifield; a pattern SD with a P < 5%; or glaucoma
hemifield test results outside the normal limits. The healthy
group consisted of patients with cataract or myopia with
any other disease. If both the eyes were eligible, one eye was
randomly enrolled in the healthy group, and an eye with
better visual field sensitivity was selected in the glaucoma
group. This study was conducted as a part of the non-
invasive, noncontact anterior segment imaging study. The
study protocol adhered to the tenets of the Declaration of
Helsinki and was approved by the institutional review board
of Osaka University Hospital. The institutional review
board waived the need for written informed consent because
of the noninvasive and retrospective nature of the study.
The protocol of the study has been published on the
department’s Web site (http://www.med.osaka-u.ac.jp/pub/
ophthal/www/attend/research/index.html).
Examinations
Baseline demographic data such as age and ocular data
such as refractive error, axial length, and lens status were col-
lected from the medical charts. All of these ocular examinations
were performed within 3 months of the Corvis measurement.
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
Copyright r 2019 Wolters Kluwer Health, Inc. All rights reserved.
Corneal Biomechanical Parameters in Glaucoma
The axial length was measured by laser interferometry (IOL-
Master; Carl Zeiss Meditec, Jena, Germany). All participants
underwent corneal deformation response measurements using
the Corvis ST. The high-speed Scheimpflug camera obtains 140
images in the horizontal section of the cornea and anterior
chamber up to 8.5 mm in diameter with a resolution of
640×480 pixels and a speed of 4330 frames/s. This imaging
system allows visualization of the corneal reaction to an air
impulse. Parameters were calculated in 3 defined states during
deformation as follows: inward applanation or applanation 1
(A1), outward applanation or applanation 2 (A2), and highest
concavity (HC) (Fig. 1). The applanation phase was defined as
the transition from a convex to a concave shape (A1) or from a
concave to a convex shape (A2). The HC is the time at which
the cornea is maximally deformed. The new analysis software
(version 1.3r1538) of the dynamic Scheimpflug analyzer pro-
vides 38 parameters, including IOP, CCT, and 36 parameters
that show the deformation responses. Analyses of too many
parameters may cause confusion and an issue with multiple
comparisons. Therefore, we selected 8 relevant parameters that
showed (1) excellent or good reproducibility in our previous
investigation18 and (2) correlation with clinical factors other
than IOP in previous studies. Relevant parameters include time
and velocity at applanation (A1 and A2),16 deflection ampli-
tude (DeflA), peak distance (PD), and radius of curvature at
HC (radius), and whole eye movement (WEM). We selected
DeflA as a parameter showing the vertical movement of the
corneal apex, instead of deformation amplitude (DA) which
was investigated in many previous studies. DeflA can be
interpreted as an improved version of DA, in that WEM is
compensated for in the DeflA but not in the DA. The 8 rele-
vant parameters are detailed in Table 1 (Supplementary Digital
Content, http://links.lww.com/IJG/A263). The details of all 36
Corvis parameters are listed in Table (Supplementary Digital
Content 1, http://links.lww.com/IJG/A257).
Statistical Analysis
Descriptive statistics such as the mean, SD, and range
were computed for the baseline clinical factors and Corvis
parameters to describe the study population. Differences in
biomechanical parameters between glaucomatous and healthy
eyes were evaluated using multivariable linear regression
models. For each Corvis parameter, a set of multivariable
linear regression models were fit with type (glaucoma vs.
healthy), IOP, CCT, age, and axial length as predictors.
Before multivariable analyses, the absence of apparent non-
linear relationships between covariates and outcomes were
confirmed by examining scatterplots for each variable. The
Benjamini and Hochberg method was used to adjust for
the multiple comparisons for multivariable analyses, with the
false discovery rate value < 0.05 was considered significant.19
For reference, multivariable analyses of all 36 parameters were
performed afterward. All statistical analyses were performed
using the statistical programming language R (R Foundation for
Statistical Computing, Vienna, Austria).
RESULTS
Descriptive Statistics
Forty-seven subjects with glaucoma and 75 healthy
subjects were included. There was no significant difference in
age and axial length between glaucomatous and healthy
subjects. Average CCT of glaucomatous eyes was significantly
thinner than that of healthy eyes (P < 0.001). The mean
number of topical antiglaucoma medications in the glaucoma
www.glaucomajournal.com | 589
Miki et al
FIGURE 1. Schematic presentations of the defined status and
parameters of the Corvis ST during corneal deformation
responses. A, The applanation status, defined as the transition
from a convex to a concave shape (applanation 1) or a concave to
a convex shape (applanation 2). The line indicates the flattened
(applanated) area of the cornea. B, Highest concavity (HC): the
time at which the cornea is maximally deformed. C, Radius of
curvature (arc), and deflection amplitude (arrow) were calculated
at the HC. D, Peak distance (arrow) is also calculated at the HC.
E, Whole eye movement is determined by the movement of the
edge points of the cornea. Figure 1 can be viewed in color online
at www.glaucomajournal.com.
group was 1.8 ± 1.2 (range, 1 to 5). Baseline characteristics of
enrolled subjects are summarized in Table 2 (Supplementary
Digital Content, http://links.lww.com/IJG/A263).
Biomechanical Parameters in Glaucomatous
Versus Healthy Eyes
Values of 8 clinically relevant biomechanical parame-
ters in glaucomatous and healthy subjects are shown in
Table 3 (Supplementary Digital Content, http://links.lww.
com/IJG/A263). All of the relevant 8 Corvis parameters
590 | www.glaucomajournal.com Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
Copyright r 2019 Wolters Kluwer Health, Inc. All rights reserved.
J Glaucoma  Volume 28, Number 7, July 2019
were analyzed in multivariable regression models including
IOP, CCT, age, axial length, and group as covariates.
Results of the multivariable regression analyses are sum-
marized in Table 4 (Supplementary Digital Content, http://
links.lww.com/IJG/A263). Four parameters (A1T, A2T,
radius, and WEM) showed significantly smaller values in
glaucoma eyes than healthy eyes. IOP showed positive
association with 3 parameters (A1T, A2V, and radius), and
negative association with 5 parameters (A1V, A2T,
HCDeflA, PD, and WEM). CCT showed positive associa-
tion with 2 parameters (A2T and radius). Age showed
positive association with 2 parameters (radius and WEM),
and negative association with 2 parameters (A1V and A2T).
Axial length showed positive association with 3 parameters
(A1T, HCDeflA, and PD), and negative association with 3
parameters (A2T, A2V, radius, and WEM). Results of the
multivariable analyses of all 36 parameters are listed in
Table (Supplementary Digital Content 2, http://links.lww.
com/IJG/A258).
DISCUSSION
Glaucomatous eyes showed distinct biomechanical prop-
erties from those of healthy eyes (table 4, Supplementary
Digital Content, http://links.lww.com/IJG/A263). They were
less resistant to deformation (compliant) than healthy control
eyes as demonstrated by easier applanation (smaller A1T) and
steeper deformation (smaller radius). Previous studies have
shown that larger deformability of the cornea lead to under-
estimation of IOP.3,20 Larger deformability of glaucomatous
eyes may increase the risk for development and progression of
glaucomatous damage through underestimation of IOP3,20 and
vulnerability of ocular tissues to pressure-induced damage.
Results of this study also suggest lower CH (as shown by
smaller A1T and A2T) in glaucomatous eyes, which is in
agreement with previous studies using ORA.6 Lower CH was
shown to be associated with increased risk of glaucoma
progression.6,8 Together, the dynamic Scheimpflug analyzer
provides information about biomechanical properties such as
deformability or hysteresis, which are related to pathophysio-
logy of glaucoma. The WEM was also significantly altered in
glaucoma eyes (smaller in glaucomatous eyes). The dynamic
Scheimpflug analyzer, unlike the ORA, can compensate for the
movement of the eye. The observation that WEM per se was
influenced by the existence of glaucoma supports our notion
that DeflA (corneal movement with compensation for the
WEM) is more appropriate than DA (without compensation)
to evaluate the properties of the cornea,16 and shows potential
advantages of the dynamic Scheimpflug analyzer over the
ORA.
Recently, a biomechanical hypothesis of glaucomatous
optic neuropathy, in which the overall magnitude of the
optic nerve damage is determined by the interaction between
IOP-related stress and biomechanical properties of the
ONH, has attracted much attention.21 Seen from this
viewpoint, it is necessary to measure biomechanical prop-
erties of the eye not only to accurately measure IOP but to
predict IOP-induced optic nerve damage and to optimize
IOP-lowering therapy to halt it. Although it is impossible to
directly measure biomechanical properties of the ONH in a
clinical setting, previous studies suggested inter-relation
between biomechanical properties of the cornea and those of
the ONH.7,22 Larger corneal deformability in glaucoma eyes
in this study may be related to hypercompliance of the ONH
reported in previous experimental studies.23 Further study is
J Glaucoma  Volume 28, Number 7, July 2019
necessary to elucidate the possible interrelation between
biomechanical properties of various ocular tissues.
We selected 8 relevant biomechanical parameters based
on reproducibility and correlation with baseline factors in
our previous investigation.16,18 Relevant biomechanical
parameters include 2 parameters in A1, 2 parameters in A2,
3 parameters at HC, and the WEM. Because the air pressure
increases with time in the inward indentation phase, smaller
A1T means smaller pressure is necessary to applanate the
cornea, thus suggesting easier applanation (larger deform-
ability). A1V is the velocity of the corneal movement at A1,
thus larger A1V means larger deformability. A2 parameters
also show ease of applanation as A1 parameters but in
opposite direction. Thus, larger A2T value and smaller A2V
show easier applanation. However, A2 parameters should
also be considered in relation to A1 parameters; A2 pressure
is smaller than A1 pressure, and the difference between A1
and A2 pressure is called CH.4,5 In this study, glaucomatous
eyes exhibited smaller A1T (smaller A1 pressure) and A2T
(greater A2 pressure), which means smaller CH in glau-
comatous eyes. HCDeflA and PD are maximum corneal
deformation in vertical and horizontal directions, respec-
tively. Thus, larger values of these parameters simply show
larger deformability of the cornea. DeflA is an improved
version of DA, which is used in many previous studies and
can be interpreted in the same context. Smaller values of
radius mean steeper shape of corneal deformation, thus
more deformability. Biomechanical relevance of WEM has
not been established as it is a relatively new parameter. But
it shows a significant relationship with many clinical factors
in our previous16 and current investigation, suggesting sig-
nificant relevance of this parameter in a clinical setting.
In agreement with prior reports, clinical factors significantly
affected biomechanical parameters (table 4, Supplementary
Digital Content, http://links.lww.com/IJG/A263).11,9–16 Higher
IOP was associated with harder applanation (A1T and A2T)
and flat corneal deformation (radius). All of these associations
suggest smaller deformability. Higher IOP was also associated
with smaller WEM. Thicker CCT also showed smaller
deformability (radius). Higher age was also associated with
smaller deformability (radius) but was associated with larger
WEM. These associations observed in the current study were in
general agreement with our previous study on healthy subjects.16
Longer axial length generally showed association with larger
deformability (HCdeflA, PD, and radius), however, some of the
associations (A1T) suggested smaller deformability. Longer axial
length was also associated with smaller WEM.
Confounding effects of clinical factors may explain, at
least in part, the disagreements between the current study and
previous studies. Specifically, some previous studies demon-
strated smaller deformability of glaucomatous eyes10–12 in
contrast to the current study that showed larger deformability
of those eyes. Most previous studies did not control for the
confounding effects of other factors10,13 or only partly con-
trolled for them.11,12 In both of our previous16 and current
studies, IOP, CCT, and age significantly influence ocular
biomechanical properties, thus, it is impossible to accurately
evaluate biomechanical changes in disease status without
controlling for those baseline factors.
Several limitations of this study should also be mentioned. It
has been suggested that biomechanical properties of glaucoma
eyes may change with disease progression21,24 and treatment,25,26
but associations between dynamic Scheimpflug biomechanical
parameters and glaucoma severity or treatment have not been
elucidated. Design and sample size of the current study were not
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
Copyright r 2019 Wolters Kluwer Health, Inc. All rights reserved.
Corneal Biomechanical Parameters in Glaucoma
appropriate to look at the impact of these factors on bio-
mechanical parameters. The current study enrolled only primary
open-angle glaucoma patients; hence the results cannot be
directly extrapolated to other types of glaucoma such as angle-
closure glaucoma, secondary glaucoma, and preperimetric glau-
coma. Future work should, therefore, be designed to evaluate the
influence of factors that were not sufficiently investigated in this
study, such as race, disease severity, and treatment on bio-
mechanical parameters. In addition, prognostic value of the
Corvis parameters regarding disease progression has not been
clarified, thus requiring further longitudinal research in future.
In conclusion, this study demonstrated significant differ-
ences in ocular biomechanical properties between glaucoma-
tous and healthy eyes in multivariable analyses controlled for
IOP, CCT, age, and axial length. Eyes with medically con-
trolled primary open-angle glaucoma demonstrated larger
deformability of the cornea compared with healthy eyes, which
may influence the susceptibility to glaucoma through an
underestimation of IOP and biomechanical vulnerability of the
globe. Studies on ocular biomechanical parameters should lead
to better understanding of pathophysiology and more accurate
risk assessment of glaucoma.
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J Glaucoma  Volume 28, Number 7, July 2019
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