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Jpn J Ophthalmol (2014) 58:483–489

DOI 10.1007/s10384-014-0344-2

CLINICAL INVESTIGATION

Corneal biomechanical properties in 3 corneal transplantation


techniques with a dynamic Scheimpflug analyzer
Naoyuki Maeda • Ryotaro Ueki • Mutsumi Fuchihata •

Hisataka Fujimoto • Shizuka Koh • Kohji Nishida

Received: 24 February 2014 / Accepted: 17 July 2014 / Published online: 5 September 2014
Ó Japanese Ophthalmological Society 2014

Abstract Conclusions The dynamic Scheimpflug analyzer provides


Purpose To compare the corneal biomechanical proper- a method to obtain new biomechanical information on the
ties of eyes that have undergone penetrating keratoplasty cornea such as the DA and Rhc, and these parameters dif-
(PK), deep anterior lamellar keratoplasty (DALK), and fered among eyes that had undergone 3 different types of
Descemet stripping automated endothelial keratoplasty corneal surgery. Abnormalities in these parameters after
(DSAEK). the different corneal transplantation techniques may indi-
Methods This case–control study comprised 20 post-PK cate larger deviations in the stress–strain reaction of the
eyes, 14 post-DALK eyes, 15 post-DSAEK eyes, and 50 cornea and more uncertainty in the intraocular pressure
normal control eyes. A dynamic Scheimpflug analyzer (the measurements than in normal eyes.
Corvis ST) was used to evaluate the corneal biomechanical
properties including deformation amplitude (DA) and Keywords Corneal biomechanics  Corneal integrity 
radius at the highest concavity (Rhc). Keratoplasty  Scheimpflug image
Results In post-PK eyes, the mean DA was
1.20 ± 0.13 mm, which was significantly higher than those
of the control eyes (1.07 ± 0.09) and the post-DSAEK Introduction
eyes (1.08 ± 0.12). The DA (1.18 ± 0.18) in the post-
DALK eyes was significantly higher than in the control Penetrating keratoplasty (PK) has been the predominant
eyes. The Rhc in the post-PK (6.34 ± 0.37 mm), -DALK technique used for corneal transplantation for many years.
(6.04 ± 1.22), and -DSAEK (6.44 ± 0.58) eyes was sig- However, recent developments in selective lamellar kera-
nificantly smaller than in the control eyes (7.57 ± 0.78). toplasty including deep anterior lamellar keratoplasty
(DALK) [1–3], Descemet stripping automated endothelial
keratoplasty (DSAEK) [4–7], and Descemet membrane
endothelial keratoplasty (DMEK) [8, 9] have markedly
Electronic supplementary material The online version of this altered the indications for PK. DSAEK and DMEK have
article (doi:10.1007/s10384-014-0344-2) contains supplementary
material, which is available to authorized users.
been used for cases with corneal endothelial dysfunction
but an intact stroma and anterior shape. Such endothelial
N. Maeda (&)  M. Fuchihata  H. Fujimoto  S. Koh  keratoplasty can reduce postoperative corneal regular and
K. Nishida irregular astigmatism [10, 11]. DALK is used in patients
Department of Ophthalmology, Osaka University Graduate
with a healthy endothelium and eliminates the risk of
School of Medicine, Room E7, 2-2 Yamadaoka, Suita,
Osaka 565-0871, Japan endothelial rejection. These selective lamellar keratopla-
e-mail: nmaeda@ophthal.med.osaka-u.ac.jp sties also have advantages over PK, i.e., reduced risks of
wound dehiscence and globe rupture due to trauma [12,
R. Ueki
13].
Department of Ophthalmology and Visual Sciences, Graduate
School of Biomedical Sciences, Nagasaki University, Nagasaki, To evaluate the integrity of the cornea following kera-
Japan toplasty, the biomechanical properties of the cornea must

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484 N. Maeda et al.

be quantified. Because the ocular response analyzer (ORA; Surgical technique


Reichert Technologies, Buffalo, NY, USA) enables in situ
determination of the biomechanical properties of the cor- The PK procedure was performed in a conventional way;
nea [14], various studies have examined the effects on the the donor and host trephination sizes were 7.5 and 7.0 mm
corneal biomechanics of diseases such as keratoconus and or 8.0 and 7.5 mm in all cases, and the donor graft was
of surgical procedures such as LASIK and corneal cross- sutured with combined 10-0 nylon. The DALK procedure
linking [15–17]. was performed as described by Sugita and Kondo [2]. The
Several studies have also determined the corneal bio- donor corneas were punched out with a diameter 0.25 mm
mechanics by measuring the degree of corneal hysteresis larger than the recipient bed of 7.5 or 8.0 mm, and the
and the corneal resistance factor following keratoplasty donor cornea was sutured with combined 10-0 nylon
[18–21]. Recovery of corneal hysteresis and the corneal sutures. The DSAEK procedure included stripping the
resistant factor in patients with keratoconus after PK has Descemet membrane and endothelium from the recipient’s
been reported [18]. The results of earlier studies comparing central cornea and transplanting a 7.75- or 8.0-mm disc of
selective lamellar keratoplasty with PK were inconclusive: donor endothelium and posterior stroma that were dis-
1 study reported comparable corneal hysteresis after PK sected with a microkeratome and inserted using the pull-
and DALK [19], while 2 other studies showed more through technique.
favorable results on corneal hysteresis after DALK than During the follow-up period, after PK and DALK, only
after PK [20, 21]. loose sutures were removed, and after DALK, all of the
A new dynamic Scheimpflug analyzer (the Corvis ST; sutures in 8 eyes were removed.
Oculus Optikgeräte, Wetzlar, Germany) has become
available for clinical use [22–26]. Because dynamic Measurements
deformation of the cornea by a constant pressure air pulse
is recorded through this ultra-high-speed Scheimpflug The Corvis ST can record 140 Scheimpflug images for
camera, not only the intraocular pressure (IOP) and corneal 31 ms with a speed of 4,330 frames/s. It can then calculate
thickness but also several parameters associated with the the IOP and corneal biomechanical parameters on the basis
corneal biomechanics can be obtained. of the dynamic deformation of the cornea while the air
The purpose of this study was to determine the biome- pulse is being applied to it. The high-speed Scheimpflug
chanical properties of the cornea after DSAEK, DALK, and camera takes images of the horizontal section of the cornea
PK. The dynamic Scheimpflug analyzer was used to obtain and anterior chamber up to 8.5 mm in diameter with a
the biomechanical characteristics of the corneas after each resolution of 640 9 480 pixels.
of these 3 keratoplasties, and the findings were compared Measurements were continued until 2 reproducible
with those of normal eyes. results were obtained for each eye. The results of the
measurements of the better image for automated digitiza-
tion in the anterior and posterior corneal surfaces were
Patients and methods selected.
The parameters collected from the dynamic Scheimpflug
Patients images were time (Thc; in ms) at the highest concavity,
peak distance (PDhc; in mm) at the highest concavity,
The study comprised 20 eyes of 20 patients who had radius (Rhc; in mm) at the highest concavity, deformation
undergone PK (mean age 62.3 ± 12.4 years; men/women amplitude (DA; in mm) at the highest concavity, time (Ti;
11/9), 14 eyes of 14 patients who had undergone DALK in ms) at the inward applanation, length (Li; in mm) at the
(mean age 63.5 ± 15.6 years; men/women 6/8), and 15 inward applanation, velocity (Vi; in m/s) at the inward
eyes of 15 patients who had undergone DSAEK (mean age applanation, time (To; in ms) at the outward applanation,
71.3 ± 7.5 years; men/women 5/10) at Osaka University length (Lo; in mm) at the outward applanation, and velocity
Hospital. Patients included were those who had no clini- (Vo; in m/s) at the outward applanation. The IOP (mmHg)
cally relevant postoperative corneal edema and who had and central corneal thickness (CCT; in lm) were also
reliable Corvis ST measurements. All of the patients were recorded.
followed for at least 3 months. Fifty normal eyes of 50
individuals with no ocular pathologies other than refractive Statistical analyses
errors served as controls (mean age 62.7 ± 13.7 years;
men/women 16/34). The institutional review board of Data were analyzed using JMP version 9 software (SAS,
Osaka University Hospital approved this study. The Cary, NC, USA). One-way analysis of variance (ANOVA)
research followed the tenets of the Declaration of Helsinki. and the Tukey–Kramer test were used to compare the

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Biomechanics after keratoplasty 485

Fig. 1 Representative displays of the dynamic Scheimpflug analyzer corneal velocity. Note the DA in PK eyes (1.47 mm) is deeper than in
in a normal eye (left) and in an eye following penetrating keratoplasty normal eyes (1.06 mm) and that the radius at the highest concavity
(right). The Scheimpflug image at the highest concavity is shown in (Rhc) in the PK eyes (4.55 mm) is steeper than in normal eyes
addition to the IOP, pachymetry, and 10 biomechanical parameters (6.62 mm)
and graphs for deformation amplitude (DA), applanation length, and

Table 1 Output of dynamic Scheimpflug analyzer in normal eyes and eyes that underwent one of three corneal transplantation techniques
Control DSAEK DALK PK P value

IOP 14.63 ± 1.49 15.03 ± 3.74 14.14 ± 3.16 14.28 ± 1.23 0.6678
CCT 552 ± 31*, ** 652 ± 61*, # 628 ± 63**, ##
552 ± 56#, ## \0.0001
DA 1.07 ± 0.09*, ** 1.08 ± 0.12# 1.18 ± 0.18* 1.20 ± 0.13**, #
0.0004
, , # #
Rhc 7.57 ± 0.78* ** 6.44 ± 0.58* 6.04 ± 1.22** 6.34 ± 0.37 \0.0001
Thc 17.19 ± 0.75 17.31 ± 0.67 16.93 ± 0.62 17.17 ± 0.42 0.4644
PDhc 3.62 ± 1.30 2.76 ± 1.08* 3.56 ± 1.37 4.37 ± 1.19* 0.0043
Ti 7.67 ± 0.24 7.72 ± 0.55 7.46 ± 0.47 7.60 ± 0.22 0.1456
Li 1.81 ± 0.24 1.81 ± 0.21 1.80 ± 0.24 1.80 ± 0.23 0.9968
Vi 0.16 ± 0.03 0.14 ± 0.03 0.15 ± 0.05 0.15 ± 0.03 0.3990
To 22.30 ± 0.39* 20.07 ± 0.69 21.85 ± 1.02* 22.11 ± 0.26 0.0471
Lo 1.86 ± 0.39 1.89 ± 0.11 1.93 ± 0.45 2.00 ± 0.48 0.6712
Vo -0.33 ± 0.07 -0.34 ± 0.12 -0.34 ± 0.12 -0.35 ± 0.11 0.8297
DSAEK Descemet stripping automated endothelial keratoplasty, DALK deep anterior lamellar keratoplasty, PK penetrating keratoplasty, IOP
intraocular pressure (mmHg), CCT central corneal thickness (lm), DA deformation amplitude at the highest concavity (mm), Rhc radius at the
highest concavity (mm), Thc time at the highest concavity (ms), PDhc peak distance at the highest concavity (mm), Ti time at the inward
applanation (ms), Li length at the inward applanation (mm), Vi velocity at the inward applanation (m/s), To time at the outward applanation (ms),
Lo length at the outward applanation (mm), Vo velocity at the outward applanation (m/s)
P value: 1-way ANOVA; *, **, #, ##
: Tukey–Kramer test, P \ 0.05

values of the different parameters obtained by the dynamic a patient who had undergone PK are shown in Fig. 1.
Scheimpflug analyzer for the 4 groups of eyes. Probability Supplemental digital videos of these eyes during the
values below 0.05 were considered significant for all measurements are shown in Video 1. The DA at the highest
analyses. concavity for the PK eye was 1.47 mm, which was larger
than the 1.06 mm in the normal eye. Moreover, the Rhc in
the PK eye was 4.55 mm, which was steeper than the
Results 6.22 mm in the normal eye.
Statistical comparisons for the 4 groups of the parame-
Typical Scheimpflug images at the time of highest con- ters obtained by the dynamic Scheimpflug analyzer are
cavity due to the air pulse in a normal eye and in an eye of shown in Table 1. One-way ANOVA showed significant

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486 N. Maeda et al.

Fig. 2 Scatterplot of deformation amplitude (DA) (left) and radius at normal zone, some of the PK and DALK eyes have higher DA and
the highest concavity (Rhc) (right) as a function of age. Although lower Rhc values than those of the normal eyes of the same age
some of the DSAEK, PK, and DALK eyes are distributed inside the

differences among the 4 groups in CCT, DA, Rhc, peak found in all eyes (control eyes: R2 = 0.5519, P \ 0.0001;
distance at the highest concavity, and time at the outward DSAEK eyes: R2 = 0.8437, P \ 0.0001; PK eyes:
applanation. R2 = 0.2923, P = 0.0138) except the DALK eyes
The CCT of the DSAEK or DALK eyes was signifi- (P = 0.1644). A significant positive correlation between
cantly thicker than that of the control or PK eyes. IOP and Rhc was found in the control eyes (R2 = 0.1051,
The PK eyes had significantly larger DA than did the P = 0.0217) and the DALK eyes (R2 = 0.3877,
control and DSAEK eyes, and the DALK eyes also had P = 0.0174), but not in the DSAEK eyes (P = 0.4768) or
significantly larger DA than did the control eyes. The the PK eyes (P = 0.6801).
DSAEK, DALK, and PK eyes had shorter Rhc than did the The scatterplots in Fig. 4 show the relationships
control eyes. The DSAEK eyes had a significantly shorter between CCT and DA (left) and between CCT and Rhc
peak distance at the highest concavity than did the PK eyes. (right). A significant negative correlation between CCT and
The DALK eyes had significantly faster time at the out- DA was found in the control eyes (R2 = 0.1080,
ward applanation than did the control eyes. P = 0.0197), but not in the other eyes (DSAEK eyes:
The scatterplots in Fig. 2 show the relationships 0.9842; DALK eyes: 0.3306; and PK eyes: 0.9305). A
between age and DA (left) and between age and Rhc (right). significant positive correlation between CCT and Rhc was
Although most of the DSAEK eyes and some of the DALK found in the control eyes (R2 = 0.2319, P = 0.0004), but
and PK eyes were located close to the distribution of the not in the other eyes (DSAEK eyes: P = 0.0720; DALK
normal eyes, all of the eyes that had DA greater than 1.29 eyes: P = 0.4008; and PK eyes: P = 0.4929).
were PK or DALK eyes. The DA in all of the normal and
the DSAEK eyes was 1.29 or less. Significant correlations
between age and DA were not found in any of the eyes:
normal eyes: P = 0.9996; DSAEK eyes: P = 0.1223; Discussion
DALK eyes: P = 0.6638; and PK eyes: P = 0.2106.
Similarly, in all of the control eyes, the Rhc was 6.2 mm The in situ measurement of corneal biomechanics with the
or larger. However, some of the DSAEK, DALK, and PK Ocular Response Analyzer (ORA) uses 2 biomechanical
eyes had a Rhc less than 6.2 mm. Significant correlations parameters: corneal hysteresis (CH) and corneal resistance
between age and Rhc were not found in any of the eyes: factor (CRF). These values are derived by measuring the
control eyes: P = 0.8587; DSAEK eyes: P = 0.6059; time of the 2 peak signals that correspond to the inward and
DALK eyes: P = 0.9972; and PK eyes: P = 0.5341. outward times of applanation of the cornea in response to a
The scatterplots in Fig. 3 show the relationships variable air pulse. In contrast, the dynamic Scheimpflug
between IOP and DA and between IOP and Rhc. A sig- analyzer, the Corvis ST, records the dynamic deformation
nificant positive correlation between DA and IOP was of the horizontal Scheimpflug images in response to

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Biomechanics after keratoplasty 487

Fig. 3 Scatterplot of deformation amplitude (DA) (left) or radius at PK eyes: R2 = 0.2923, P = 0.0138). A significant positive correla-
the highest concavity (Rhc) (right) as a function of IOP. A significant tion between IOP and Rhc was found in the control eyes
positive correlation was found between DA and IOP (control eyes: (R2 = 0.1051, P = 0.0217) and the DALK eyes (R2 = 0.3877,
R2 = 0.5519, P \ 0.0001; DSAEK eyes: R2 = 0.8437, P \ 0.0001; P = 0.0174)

Fig. 4 Scatterplot of deformation amplitude (DA) (left) or radius at (CCT) and DA (R2 = 0.1080, P = 0.0197) or between CCT and Rhc
highest concavity (Rhc) (right) as a function of central corneal (R2 = 0.2319, P = 0.0004) was found only in the control eyes
thickness. A significant correlation between central corneal thickness

pressure by a constant air pulse [22] In addition to the Under the constant strain of the air pulse, eyes with
inward and outward applanation times, the dynamic higher ocular rigidity will show lower DA and larger Rhc.
deformation of the cornea in response to the air pulse is In contrast, eyes with lower ocular rigidity will have higher
recorded, as shown in the supplemental digital content DA and smaller Rhc.
(Video 1). The biomechanical parameters such as the DA Our findings showed that the DA in the PK eyes was
at the highest concavity and the radius at the highest con- significantly greater than in the control eyes and the
cavity can be obtained from these images [25]. To the best DSAEK eyes, and the DA in the DALK eyes was also
of our knowledge, this is the first study to use a dynamic significantly higher than in the control eyes. No significant
Scheimpflug analyzer to investigate the corneal biome- difference in DA was found between the DSAEK and the
chanics following corneal transplantation. control eyes. That eyes after PK or DALK have lower

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488 N. Maeda et al.

rigidity than do normal eyes is reasonable because the The relationship between the parameters obtained with
stromal wound healing at the host-graft junction and/or the ORA and those obtained with the Corvis ST should be
pathologic peripheral host cornea is not strong enough to clarified in the future. Although both instruments use air
keep the structural integrity of the cornea. Lower DA in pulse pressure to induce strain, the air-pulse pressure is
DSAEK eyes might suggest better corneal integrity than in variable with the ORA and constant with the Corvis ST.
PK or DALK eyes. The Corvis ST may have potential advantages for deter-
On the other hand, the Rhc in all postkeratoplasty groups mining the stress–strain relationship of the eye. In addition,
was significantly smaller than in the control group. This the stress is evaluated by different principles, i.e., corneal
may suggest that the ocular integrity after these corneal light reflex and Scheimpflug images. Therefore, it might be
transplantations is not as good as that of normal eyes. The difficult to develop interchangeable parameters for both
discrepancy between DA and Rhc in DSAEK eyes should instruments.
be investigated further. This study has some limitations. The numbers of par-
Significant difference in the peak distance at the highest ticipants was small, and there were many variables among
concavity between DSAEK and DALK eyes may indicate the participants and procedures. The mean age of the
differences among the procedures in centrifugal deforma- DSAEK eye group was significantly higher than those of
tion to the same load. The time of outward applanation also the other groups. Such variations might lead to a scattering
behaved differently in the DALK eyes. The shorter time of of data. However, this preliminary study with a dynamic
outward applanation in DALK eyes may suggest that a Scheimpflug analyzer showed that differences in corneal
thicker cornea will return to normal shape more easily. The biomechanical properties exist between eyes with normal
relationships among the biomechanical parameters corneas and eyes after corneal transplantation, or among
obtained with the Corvis ST are unknown. At least, we can eyes that have undergone different types of corneal
say that these indices following keratoplasty show some transplantation.
abnormalities. Further studies will be necessary to clarify Future studies will be necessary to clarify the effects of
the significance of each parameter. keratoplasty on the integrity of the eye and to evaluate the
The rigidity of the eye is generally thought to be accuracy of IOP measurements in such eyes with different
affected by age, corneal thickness, IOP, and corneal bio- corneal biomechanics. As shown in the video images, only
mechanics. In this study, significant correlations were not limited data are currently available for the dynamic Sche-
found between age and DA or between age and Rhc in any impflug analyzer. In other words, this technology may have
of the groups. This may be due to the limited age range of the potential to elucidate the detailed biomechanical
the patients studied. Significant correlations between IOP behavior of the eye in future investigations.
and DA were found in normal, DSAEK, and PK eyes, and
significant differences were also found between IOP and Acknowledgments Publication of this article was supported in part
by a Grant-in-Aid for Scientific Research (no. 24592669; to Naoyuki
Rhc in normal and DALK eyes. These results suggest that Maeda) from the Japanese Ministry of Education, Culture, Sports,
IOP should be matched when comparing the corneal bio- Science and Technology. The authors would like to thank Duco
mechanics among groups. A significant correlation Hamasaki, PhD, for the English language review.
between the CCT and biomechanical parameters was found
Conflicts of interest N. Maeda, Research Grant (Topcon), Instru-
only in the control group. Although higher ocular rigidity ment (CorvisÒ ST: Oculus); R. Ueki, None; M. Fuchihata, None;
can be expected in normal eyes with thicker corneas than in H. Fujimoto, None; S. Koh, None; K. Nishida, None.
eyes with thinner corneas, the integrity of the thicker cor-
nea after keratoplasty might not be similar to that of the
normal thicker cornea.
As shown in Figs. 2, 3, and 4, the variations in the
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