Current Eye Research, 32:11–19, 2007
Copyright 
c Informa Healthcare
ISSN: 0271-3683 print / 1460-2202 online
DOI: 10.1080/02713680601077145
Assessment of Corneal Biomechanical
Properties and Their Variation with Age
Ahmed Elsheikh, Defu Wang,
and Michael Brown
Division of Civil Engineering,
University of Dundee,
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Dundee, UK
Paolo Rama
Ophthalmology Department,
San Raffaelle Hospital,
Milan, Italy
Marino Campanelli
Monza Eye Bank, Solferino,
Monza-Milan, Italy
For personal use only.
David Pye
School of Optometry and
Vision Science, University of
New South Wales, Sydney,
Australia
Received 15 September 2006
Accepted 17 October 2006
Correspondence: Ahmed Elsheikh,
Ph.D., CEng., Division of Civil
Engineering, University of Dundee,
Dundee DD1 4HN, UK.
E-mail: a.i.h.elsheikh@dundee.ac.uk
ABSTRACT Purpose: The aim of this study was to determine the stress-strain
behavior of corneal tissue and how the behavior was affected by age. Methods:
Human corneal specimens ranging in age between 50 and 95 years were tested
under inflation conditions to determine their stress-strain behavior. The corneas
were subjected to two load rates that represent dynamic and static loading con-
ditions. The pressure-deformation results were analyzed using shell theory to
derive the stress-strain behavior. Results: The corneas demonstrated clear nonlin-
ear behavior with an initial low stiffness stage and a final high stiffness stage. The
transition between the two stages coincided with intraocular pressures between
12 and 20 mmHg. There was a considerable increase in stiffness associated
with both age and load rate. Equations were derived to describe the nonlin-
ear stress-strain relationship of corneal tissue for any age between 50 and 95
years, and these equations are presented in a form suitable for use in numerical
simulations. Conclusions: The cornea demonstrates considerable stiffening with
age with the behavior closely fitting an exponential power function typical of
collagenous tissue. The increase in stiffness could be related to the additional
age-related nonenzymatic cross-linking affecting the stromal collagen fibrils.
KEYWORDS Aging; ocular biomechanics; stress-strain behavior
INTRODUCTION
The transparent cornea is a most important component of the outer ocular
tunic. It provides a tough protective envelope for the ocular contents and helps
give the eye its general shape. The anterior corneal surface accounts for about
two-thirds of the optical power of the eye.1 This important role can be defined
in terms of corneal shape, regularity, and clarity and is a function of its refractive
index. The cornea’s contribution to ocular image formation can be degraded by
anomalies in shape produced by disease, injury, surgery, and contact lens wear.
The ability to understand and predict the corneal response to such conditions
is of great clinical importance.
Several mathematical and numerical techniques have been developed to
predict the corneal response to external effects. These techniques need rep-
resentative material constitutive models if they are to produce accurate predic-
tions. However, the material properties of the cornea reported in the literature
11
 vary widely, almost within two orders of magnitude,2
and the variation seems to be caused by a number of
primary factors including the effects of the test method,
corneal viscoelastic behavior, the intraocular pressure,
and the age.
Early evidence suggests that changes in the corneal
microstructure take place with age. Malik et al.3 used
high- and low-angle x-ray diffraction to study inter-
molecular spacing of collagen molecules and interfib-
rillar spacing of stromal collagen fibrils, respectively.
Two changes were identified with age: (1) an increase in
the cross-sectional area associated with each molecule in
corneal collagen (from approximately 3.04 nm2 at birth
to 3.46 nm2 at 90 years; up 14%), which may be due
to an increase in nonenzymatic cross-linking between
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collagen molecules, and (2) a decrease in the stroma in-
terfibrillar spacing, which could be related to changes in
the proteoglycan composition of the interfibrillar ma-
trix. The decrease in stromal interfibrillar spacing with
age was also found by Kanai and Kaufman4 using an
electron microscopy study.
X-ray scattering was also used by Daxer et al.5 who
found the diameter of collagen fibrils to be age depen-
dent. Whereas the fibril diameter was 32.2 ± 1.0 nm
For personal use only.
in persons older than 65 years of age, it was 30.8 ±
1.0 nm in persons younger than 65 years, resulting in
a change in fibril cross-sectional area of approximately
9%. This change in fibril diameter was mostly a result
of some expansion of the intermolecular Bragg spac-
ing probably caused by nonenzymatic cross-linking.
Because the collagen fibrils are the main load-carrying
components of the stroma, changes in their diameter
are expected to considerably influence the corneal me-
chanical behavior.
More direct evidence relating age to the mechanical
behavior, in the form of the ocular rigidity, was ob-
tained by Pallikaris et al.6 They tested 79 eyes undergo-
ing cataract surgery and found a statistically significant
positive correlation between the rigidity coefficient and
the age of patients (p = 0.02). A similar study was car-
ried out earlier by Ytteborg,7 who noticed a slight posi-
tive correlation between the rigidity coefficient and age,
but the correlation was not statistically significant. The
effect of age on tonometry has been given little con-
sideration, but the available evidence suggests that age
could be associated with tissue stiffening, leading to an
overestimation of intraocular pressure.5,8,9
This study aims to determine the corneal stress-strain
behavior both for static and dynamic applications. The
A. Elsheikh et al.
study uses human corneas and adopts inflation test-
ing for its close representation of the corneal working
conditions. The effect of age on corneal biomechan-
ics is given special attention. The average behavior of
corneal tissue under fast and slow loading conditions,
and for ages between 50 and 95 years, is determined and
used to develop material models suitable for use in nu-
merical simulations. This work is part of our efforts to
improve understanding of corneal behavior and how it
is affected by anisotropy, viscoelasticity, hydration, and
age.
MATERIALS AND METHODS
Experimental Measurements
Fresh human corneas were obtained from three eye
banks in Italy, France, and Germany. They included 33
from Monza Eye Bank, Monza-Milano, Italy; two from
Banque de Cornees, Hopital Edouard Herriot, Lyon,
France; and one from Cornea Bank, Center of Head
Care and Dermatology, University of Hamburg Medi-
cal Center, Germany. The corneas were stored in preser-
vation medium, Optisol GS (Alchimia, Italy), from up
to 12 hr after death and used within 14 days of preser-
vation. The limit of 14 days was adhered to based on
earlier research findings10–12 and commercial informa-
tion confirming the maintenance of tissue quality for
this time. The corneas included a 2-mm scleral ring. All
other ocular components had been removed. Care was
taken to ensure, as far as possible, that all corneas used
in this research were free of disease.
The corneas were mounted onto a custom-built pres-
sure chamber (Fig. 1). Mechanical clamps and cyano-
acrylate glue were used to provide watertight edge con-
nection for the specimens along their ring of scleral
FIGURE 1 Inflation test rig. (a) Overview of rig showing main
components including pressure chamber, temperature control
tank, loading tank, and laser beam. (b) Pressure chamber facing
laser beam with digital camera taking a profile view.
12
 FIGURE 2 Schematic cross section of the cornea.
tissue. The pressure chamber was filled with Optisol and
connected to a small reservoir, which was moved verti-
cally up and down using a 12-V motor to control the
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pressure inside the chamber. The connection between
the chamber and the reservoir passed through a large wa-
ter tank equipped with a temperature controller to en-
sure the temperature of Optisol in the pressure chamber
remained at 37◦ C throughout the test. The actual pres-
sure in the chamber was measured using a differential
pressure transducer (RDP Electronics, Differential Pres-
sure Transducer, FDW series, Wolverhampton, UK).
For personal use only.
The motor attached to the reservoir was controlled
to give the reservoir one of two speeds equivalent to
pressure application rates of 37.5 and 3.75 mmHg/min.
These pressure rates were selected, within available ex-
perimental capabilities, to approximate the two ex-
tremes of dynamic and static loading. The maximum
pressure applied was 170 mmHg. This pressure was well
above the level at which the corneas entered a stage
of stable behavior that was expected to continue until
bursting. The motor reversed the direction of motion
of the reservoir automatically upon reaching its max-
imum travel in both directions. All corneas were first
subjected to an initial inflation pressure of 0.75 mmHg,
followed by three cycles of loading and unloading.
A laser (Keyence, CCD Laser Displacement Sensor,
LK series) was used to continually monitor the displace-
ment at the apex of the cornea during the tests. Addi-
tionally, two digital cameras with 8-MB resolution were
positioned in two orthogonal directions in the plane
of the corneo-scleral intersection to monitor changes
in the profile of the corneas during loading. The laser
beam, the cameras, and the pressure transducer were all
connected to a personal computer equipped with the
National Instruments data acquisition device DAQPad-
6015 (Texas, USA) to log the data automatically. Read-
13
ings of the laser beam and the pressure transducer were
recorded every second during the test.
The central and peripheral corneal thickness (CCT
and PCT) were measured prior to the test using a
pachymeter (DGH Pachmate 55, Exton, USA). Mea-
surements were repeated three times, and the values
obtained were 0.572 ± 0.058 and 0.779 ± 0.042 mm, re-
spectively. The anterior radius, Rant , and the average
limbal diameter, 2Ri , were measured from the initial
digital images, and the values were 7.500 ± 0.767 and
11.252 ± 1.148 mm. The radius of the corneal median
surface, R (Fig. 2), was calculated from Rant , CCT, and
PCT for use in the mathematical back analysis required
to derive the stress-strain relationship from the pressure
and apical rise readings.
Mathematical Back Analysis
Mathematical back analysis based on shell
theory13,14 was used to derive the material con-
stitutive relationship from the pressure-apical rise
experimental results. The analysis considered both
in-plane and out-of-plane stiffness components and
assumed that the cornea could be approximated as a
homogenous spherical structure.15 Details of the analy-
sis procedure can be found in earlier publications.16,17
The final equation relating the applied pressure, p, to
the apical rise, r, is
pR2
r= (1 − ν)[1 − e−βη cos (βη)], (1)
2Et
where R is the radius of the corneal median surface,
t the average thickness assumed = 1/2(CCT+PCT), η
is half the central angle of curvature
 (see Fig. 2), η =
−1 √
sin (Ri /R), and β = R/t · (1 − v2 ).
4
Assessment of Corneal Biomechanics
 Because the extrafibrillar matrix of the cornea is prin-
cipally water, the corneal tissue is characterized as an
incompressible material,15,18,19 and therefore, Poisson’s
ratio, ν, is taken as 0.49.
At the inflation point, the corneal height, Ho , and
the radius of the corneo-scleral intersection, Ri , are mea-
sured experimentally from the digital camera images.
The initial radius is determined from
and the corresponding stress is determined from
σ1 = ε1 E1 . (10)
This process is repeated for every pressure increment so
that the pressure-rise readings obtained experimentally
are used to derive the stress-strain relationship of the
tissue.

R2i + Ho2
R20 = R2i + (R0 − H0 )2 or Ro = . (2) RESULTS
2Ho
After the first pressure application, p1 , the corneal The corneas were divided into two groups: 23 corneas
height increases by the apical rise recorded tested with 37.5 mmHg/min pressure rate and 13
experimentally, corneas tested with 3.75 mmHg/min rate. The age range
of the two groups was 51–95 (77.6 ± 13.2) and 50–95
(75.7 ± 14.2) years, respectively. Within each group, the
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H1 = Ho + r1 , (3)
corneas were divided into three age subgroups: 50–64,
and the corresponding radius is obtained from: 65–79, and 80–95 years. The number of corneas tested
under 37.5 mmHg/min was 4, 6, and 13 within the three
R2i + H12 age subgroups, respectively. The corresponding num-
R1 = . (4)
2H1 bers tested under 3.75 mmHg/min were 4, 4, and 5.
Assuming no change in volume of material in the All corneas demonstrated large deformations up to
cornea after loading: about 12–20 mmHg. Beyond this pressure level, which
is close to the normal intraocular pressure range, the
For personal use only.

2π R0 H0 to = 2π R1 H1 t1 . (5) corneas underwent a gradual increase in stiffness that

continued up to about 60 mmHg, followed by a zone
Therefore, the new thickness, t1 , is with an almost constant stiffness. In order to enable a
clear comparison between different age ranges, the re-
R0 H0 t0
t1 = . (6) sults within each range were analyzed to determine their
R1 H1 pressure-rise relationships with the lowest, highest, and
Also, angle η becomes average stiffness. These relationships are compared in
Figure 3, which shows that the corneal resistance to
Ri deformation under inflation conditions increased grad-
η1 = sin−1 . (7)
R1 ually with age.
The values of R1 , p1 , t1 , and η1 are then substituted The pressure rise results were used to derive the stress-
in Eq. (1) to obtain a value for the current modulus strain relationships for each group using the mathe-
of elasticity, E1 . The corresponding strain is calculated matical back analysis described above. The specimen
using the relationship16 dimensions (including the anterior radius, the limbal
diameter, and the thickness), as measured experimen-
1   tally, were used in deriving the stress-strain results. The
εφ = Nφ − ν Nθ , (8) stress-strain results within each range were then grouped
Et
together, and a best-fit equation was derived mathemat-
where
ically to describe the behavior within that range. Equa-
pR pR pR tions with different forms were tried, and the best fit
Nφ = and Nθ = − (1 − ν)e−βη {cosβη}. was achieved with an exponential equation of the form:
2 2 2
σ = A(eBε − 1), where σ and ε are the stress and strain,
Therefore,
respectively, and A and B are constants. The values of
pR A and B that provided the best fit in each group are
εφ = (1 − ν)(1 + νe−βη cos βη), (9) given in Table 1.
2Et
A. Elsheikh et al. 14
Curr Eye Res Downloaded from informahealthcare.com by University Of Arizona on 07/29/13

FIGURE 3 Comparison of pressure rise behavior between corneas with different ages. (a) Pressure rate 37.5 mmHg/min,
(b) pressure rate 3.75 mmHg/min. Age 1 is 50–64 years, age 2 is 65–79 years, age 3 is 80–95 years.

The stress-strain relationships are compared in DISCUSSION

Figure 4 to illustrate the effect of age on the material
The inflation test setup developed for this study
stress-strain behavior for the two pressure rates applied.
enabled a number of improvements in comparison
There is a clear stiffening effect associated with age. In
with earlier work. Compared with the stepped loading
order to quantify this effect, attention was given to the
For personal use only.

used in most earlier work,18,20 the continuous load-

Young’s modulus values that correspond with the fol-
ing adopted in this study enabled a tighter control
lowing specific levels of posterior pressure: 5, 10, 15,
of load rate. The use of the storage medium Opti-
20, 25, and 30 mmHg. These pressure levels cover the
sol prevented to a large extent the swelling of the
normal physiologic range of intraocular pressure (IOP)
corneal specimens. The average central corneal thick-
and extend to include the higher values of IOP com-
ness was slightly larger (by about 5%) than the average
monly seen in ophthalmic practice. In a cornea with
in vivo values reported in the literature.21,22 The laser
the average dimensions (CCT = 0.572 mm, PCT =
beam and the digital cameras with automated data cap-
0.779 mm, Rant = 7.5 mm, 2Ri = 11.252 mm), these
ture allowed noncontact monitoring of behavior during
pressure values correspond with stress levels of 0.0022,
the test and provided sufficient information to derive
0.0044, 0.0066, 0.0088, 0.0110, and 0.0133 MPa, re-
the material constitutive model from the test results.
spectively. The Young’s modulus values obtained are
The information obtained included the radius of cur-
presented in Table 2 and show significant increases with
vature, the limbal diameter, the apical height, and the
age.
apical rise. Further, because the connection with the
pressure chamber effectively provided the cornea with
TABLE 1 Values of Exponential Function Constants A and B a pinned edge, the mathematical analysis used to de-
That Provide the Best Fit Within Each Group of Tests rive the stress-strain relationship became straightfor-
37.5 mmHg/min 3.75 mmHg/min ward as it did not have to consider the complex con-
pressure rate pressure rate nection between the cornea and the sclera in intact
globes.
Age range A (MPa) B A (MPa) B
However, note should be made of possible sources
50–64 years 0.0070 50 0.0014 70 of error in the mathematical analysis. These include
65–79 years 0.0077 59 0.0038 64 the assumptions of spherical topography and material
80–95 years 0.0061 83 0.0075 60
homogeneity. The first assumption, which represents

15 Assessment of Corneal Biomechanics

 FIGURE 4 Comparison between stress-strain behavior of corneas with different age ranges. (a) Pressure rate 37.5 mmHg/min,
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(b) pressure rate 3.75 mmHg/min.

an approximation of the actual aspheric form of the
cornea, was necessary because of the lack of available
corneal topography maps and the need to adopt an
easily definable topography in the mathematical model.
A more significant simplification is the assumption of
material homogeneity as this implies that the proper-
ties obtained are average properties for corneal tissue.
For personal use only.
The two pressure application rates adopted in this
work are intended to simulate the conditions of static
and dynamic loading. This is certainly an approxima-
tion as the cornea can experience load rates outside
the adopted range. For instance, noncontact tonome-
try loads the cornea considerably faster than the high
pressure rate adopted. Similarly, pathologic intraocular

Therefore, these properties should be considered more
suitable for numerical simulations involving the cornea
as a whole such as tonometry and contact lens model-
ing and less suitable for applications where the cornea’s
integrity is compromised, for instance in modeling sur-
gical procedures. A further source of possible error is
the use of ex vivo specimens, which could exhibit dif-
ferent behavior from in vivo eyes. However, the effective
preservation of the corneas by Optisol, demonstrated
by the maintenance of the thickness, and the short pe-
riod of time within which tests were carried out, are
expected to limit the variation of behavior from in vivo
eyes.
pressure elevation, such as in primary open-angle glau-
coma, is normally much slower than the slow rate used.
However, while recognizing these limitations, the ma-
terial properties developed in this study would be ex-
pected to lead to reliable predictions of behavior in
numerical simulations.
The stress-strain results show clear stiffening effect
associated with increased age. The increase in material
stiffness between the youngest and oldest age groups is
approximately 33% and 48% under fast and slow pres-
sure application rates, respectively, resulting in average
increases in stiffness of approximately 11% and 16%
per decade.

TABLE 2 Young’s Modulus Values That Correspond with Specific Levels of Posterior Pressure for Each Age Range

E (MPa) at the following pressure values

Pressure rate Age range
(mmHg/min) (years) 5 mmHg 10 mmHg 15 mmHg 20 mmHg 25 mmHg 30 mmHg

37.5 50–64 0.403 0.451 0.497 0.541 0.583 0.624

65–79 0.515 0.573 0.627 0.679 0.729 0.777
80–95 0.599 0.679 0.755 0.826 0.894 0.961
3.75 50–64 0.159 0.212 0.260 0.305 0.347 0.388
65–79 0.306 0.364 0.417 0.467 0.515 0.561
80–95 0.514 0.572 0.628 0.681 0.732 0.781

A. Elsheikh et al. 16
 This increase in stiffness could in part be related to
the reported increase in collagen fibril diameter with
age. Daxer et al.5 observed an increase in average fib-
ril diameter from 30.8 nm below 65 years to 32.2 nm
above 65 years. This 4.5% increase in diameter results
in 9.2% increase in cross-sectional area. At the same
time, earlier work also found no evidence of age-related
change in corneal thickness.23 This would mean that
while fibril diameter increases with age, the center-to-
center distance between fibrils remains unchanged. Us-
ing these findings in stiffness calculations, and assum-
ing that the extracellular matrix surrounding the fibrils
plays no structural part, the stiffness of the cornea would
be expected to grow only by a factor close to 9.2%.
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For personal use only.
FIGURE 5 Effect of pressure application rate on corneal stress-strain relationships. (a) Age range 50–64 years, (b) age range 65–
79 years, (c) age range 80–95 years.
17
However, the stiffness increases seen in our tests point
at a significantly higher value. The difference could be
related to the increase in cross-linking between fibrils
seen in old age as reported by Malik et al.3 Unlike the
initial fibril cross-linking mediated by enzymes in the
early years of life, the further cross-linking developed
in old age is due to the accumulation of nonenzymatic
glycation end products, and this further cross-linking
is thought to be at least partly responsible for the stiff-
ening trend seen in older corneas. Earlier attempts by
Spoerl et al.24 and Wollensak et al.25,26 to artificially
increase cross-linking in corneal tissue using riboflavin
and ultraviolet-A light resulted in stiffness increases of
more than 100%.
Assessment of Corneal Biomechanics
 The increased stiffness of the cornea with age could
have implications on the progression of glaucoma. In
young age with moderate corneal stiffness, if the in-
traocular pressure is to elevate, the cornea would de-
form relieving part of the pressure increase and reducing
the deformation and damage of the lamina cribrosa. In
contrast, older and stiffer corneas would deform less,
making the lamina cribrosa more vulnerable to dam-
age. This observation should be born in mind when
considering earlier reports of structural changes in the
lamina cribrosa with old age leading to its reduced
resilience.27–29 When combined, these alterations in
both the cornea and the lamina cribrosa could lead
to increased pressure on the lamina cribrosa and in-
creased susceptibility to plastic flow and permanent
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deformation.
The increased stiffness with age is also expected to
lead to errors in IOP measurement using tonometry
techniques. The stiffness increase of 16% per decade re-
ported above would lead to an IOP overestimation of
approximately 0.85 mmHg. This estimate is based on a
suggested relationship between tissue stiffness and IOP
measurements using Goldmann applanation tonome-
try developed in an in earlier study.30
For personal use only.
The association between cross-linking and tissue stiff-
ening has been reported for other biological tissues.
Bruel et al.31 injected rats with an agent to inhibit
the formation of cross-links in the aorta, and as a re-
sult, the content of collagen cross-links was reduced
by 49%. Subsequent mechanical tests on aorta speci-
mens showed that this was associated with 26% reduc-
tion in stiffness and 30% reduction in strength. The
same group32 found an age-related increase in aorta
fibril cross-linking caused by the accumulation of
nonenzymatic glycation end products. This increase in
cross-linking was thought to be linked to the signifi-
cant increase in aorta stiffness seen with age. Similar
findings were reported by Bank et al.33 concerning the
age-related accumulation of glycation end products in
healthy human cartilage, leading to increased collagen
cross-linking and tissue stiffening.
The test results presented here were further assessed
to show the effect of changing the pressure rate on tis-
sue stiffness. Figure 5 shows a comparison between the
behavior under both pressure rates presented for each
age range. There is a consistent increase in stiffness
associated with increasing the pressure rate, as would
be expected for a viscoelastic material like the cornea.
However, it is recognized that corneal viscoelasticity is a
A. Elsheikh et al.
complex topic that would require a more detailed study
than could be afforded by the comparisons in Figure 5.
ACKNOWLEDGMENTS
This research was partly supported by funding from
the United Kingdom’s Royal Academy of Engineer-
ing. The authors greatly appreciate help from Dr. Odile
Damour of Banque de Cornees, Hopital Edouard Her-
riot, Lyon, France, and Dr. Jürgen Bednarz of the
Cornea Bank, Center of Head Care and Dermatology,
University of Hamburg Medical Center, Germany, for
providing some of the corneas tested in this study.
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Assessment of Corneal Biomechanics