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Research Article

Ophthalmic Res Received: November 6, 2018


Accepted after revision: January 11, 2019
DOI: 10.1159/000496865 Published online: March 28, 2019

Cortical Cataract and Refractive Error


Ralph Michael a, b Luis Pareja-Aricò b, c Franziska G. Rauscher d, e
     

Rafael I. Barraquer a, b, f  

a Centro de Oftalmología Barraquer, Barcelona, Spain; b Institut Universitari Barraquer, Universitat Autònoma de
   

Barcelona, Barcelona, Spain; c Hospital Clinico Universitario Valladolid, Universidad de Valladolid, Valladolid, Spain;
 

d Institute for Medical Informatics, Statistics and Epidemiology, Leipzig University, Leipzig, Germany; e Leipzig
   

Research Centre for Civilization Diseases, Leipzig University, Leipzig, Germany; f Universitat Internacional de
 

Catalunya, Barcelona, Spain

Keywords more cortical cataract than myopes. These cortical cataracts


Cortical cataract · Refraction · Accommodation · Presbyopia might be caused by shear stress inside the crystalline lens
due to accommodation efforts at the time of onset of pres-
byopia. © 2019 S. Karger AG, Basel
Abstract
Purpose: To evaluate the relationship between the presence
of cortical cataract and accommodation effort, using refrac-
tive error as a proxy. Methods: Patients between 50 and 90 Introduction
years, scheduled for cataract surgery, were selected with the
help of a photographic database. Nuclear and cortical cata- It is known that the lens cortex and nucleus have dif-
ract were graded and patients grouped having no cataract, ferent viscoelastic properties in young and old lenses [1–
pure cortical, mixed or pure nuclear cataract. Refraction data 3], the nucleus being softer than the cortex in younger
at the time of the photograph was converted to estimated lenses (below 40 years of age), both cortex and nucleus
spherical equivalent refractive error each patient would stiffening with age and resulting in a much stiffer nucleus
have had at the age of 45 years. Results: From the initial 239 as compared to the cortex in older lenses (above 50 years
eyes from 239 patients, cases with myopia below –6.5 dpt of age) (Fig. 1). It should also be noted that during accom-
and hyperopia above 6.5 dpt were excluded, resulting in 199 modation the thickness of the nucleus changes whilst the
cases for final analysis. Eyes with no cataract showed the dimensions of the cortex remain mostly constant [4, 5].
lowest median refractive error (–3.65 dpt), followed by the Human cortical or cuneiform opacities are accompa-
pure nuclear group (–2.69 dpt). The median refractive error nied by changes in lens fiber structure and architecture
for pure cortical (–0.23 dpt) and mixed cataracts (–0.87 dpt) mainly in the equatorial border zone between the lens nu-
were close to emmetropia. Cortical cataracts were found in cleus and the cortex [6]. This has been studied in crystal-
37% of myopes, 82% of emmetropes, and 85% of hyperopes. line lenses from human donor eyes, where not only the
Conclusion: Emmetropes and hyperopes tend to develop frontal view, but also the cross-section of the lens was
129.127.145.240 - 3/29/2019 5:24:03 PM

© 2019 S. Karger AG, Basel Ralph Michael


Institut Universitari Barraquer
Laforja 88
E-Mail karger@karger.com
ES–08021 Barcelona (Spain)
www.karger.com/ore
Univ.of Adelaide
Downloaded by:

E-Mail ralphm @ barraquer.com


Model D
104
Shear modulus, Pa

Cortex (Gc)
103

Nucleus (GN)
102

0 10 20 30 40 50 60
Age, years 1,000 µm 1,000 µm

Fig. 1. On the left side, the age-stiffness relationship for the human right, dark-field images from human donor eyes with frontal view
lens cortex and nucleus is shown derived from lens spinning tests of an intact lens and cross-section of a lens slice showing a typical
[1]. Lower values of the shear modulus relate to softer tissue and cortical cataract [6].
higher values represent more stiffness. In the center and to the

evaluated (Fig. 1). Measured at the lens equator, cortical for cataract surgery in order to complement our earlier
opacities are usually found between 500 and 700 µm be- morphological studies and to support the mechanical
low the lens capsule [6]. This is also seen in in vivo studies stress theory for cortical cataract. The hypothesis of our
using optical coherence tomography [7, 8]. This location current study is that people who accommodate more have
corresponds to the outer dimensions of the adult lens nu- more cortical cataract. We will use the refractive error of
cleus as defined by Taylor et al. [9] based on the lens ul- a person as a proxy for his or her accommodation efforts.
trastructure. The morphology of cortical cataracts is An eye with for instance 3 dpt of myopia and without dis-
characterized by local disintegration of the cytoplasm tance correction does not need to accommodate for near
into membrane-bound vesicles and undulated, folded work and accommodation for this eye’s distance vision is
and fractured groups of fiber cells at the border zone be- not possible. On the other hand, an eye with 3 dpt of hy-
tween the cortex and nucleus [6]. peropia has to accommodate for near and far work.
These observations in morphology and changes with
age of the elastic properties inside the lens suggested that
shear stress between the stiff nucleus and the softer cortex Methods
of the lens are responsible for the cellular damage seen in
Patients scheduled for cataract surgery with a minimum age of
cortical cataracts. These shearing forces are expected to
50 years were selected with the help of a photographic database of
occur during attempted accommodation after the onset slit lamp images; photographs taken between 2003 and 2017. A
of presbyopia, when the nucleus is resistant to deforma- frontal view and a cross-sectional view of the eye, both with pupil-
tion and the cortex remains softer [6, 10, 11]. lary dilation had to be available (Fig.  2). We focused on pro-
The suggestion that external forces during accommoda- nounced cortical cataracts and pronounced nuclear cataracts dur-
ing the selection; posterior subcapsular cataracts and other unspe-
tion or attempted accommodation cause shear stress inside
cific cataracts were not included.
the lens and induce cortical cataracts is not at all new. To After the selection, the cataract images were graded by three
our knowledge, Wilhelm Schoen [12] already described in ophthalmologists. The nuclear component of the cataract was
a lecture at Leipzig University in 1896 that accommodation graded according to the BCN10 grading scale, a combined scale of
might be the cause for cortical cataract. This theory has nucleus color and opacity, ranging from 0 to 10 [17]. The cortical
component was graded on a scale from 0 to 5, similar to the Lens
been brought up several times during the past 100 years but
Opacities Classification System III (LOCS) intended for retro il-
was always forgotten or ignored [13–16]. lumination images [18].
Our aim was to study the relationship between cortical The definition of “cataract” will always be arbitrary because
cataract and accommodation effort in patients scheduled lens opacities increase gradually with age [19, 20]. Everyone above
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2 Ophthalmic Res Michael/Pareja-Aricò/Rauscher/


DOI: 10.1159/000496865 Barraquer
Univ.of Adelaide
Downloaded by:
No cataract Pure nuclear Mixed cataract Pure cortical

Cortical grade: 0 Cortical grade: 0 Cortical grade: 3 Cortical grade: 4


Nuclear grade: 2 Nuclear grade: 8 Nuclear grade: 4 Nuclear grade: 2

Fig. 2. Sample cases for the 4 cataract groups as defined in the ed on a scale from 0 to 5 and nuclear cataract from 0 to 10. G
­ rading
Methods with cross-sectional view (top) and frontal view (bot- results are given below.
tom) of the eye, taken with a slit lamp. Cortical cataract was grad-

50 years has some degree of nuclear opacity. Therefore, we choose A literature search revealed 7 major studies on refractive
a nuclear cataract grade of 4 and above on the BCN10 scale (0–10) change with age, 3 cross-sectional studies [23–25], and 4 longitu-
as “nuclear cataract” for the current study. Cortical cataract, how- dinal studies [26–29]. The data from these studies were trans-
ever, starts to develop at the lens equator, which is not visible in formed into a format giving the refractive change in diopters per
vivo, even with a dilated pupil (Fig. 1) [21, 22]. Cortical cataracts year against age in years (Fig. 3). With the help of the data in this
are already advanced when they are visible inside the pupillary graph, the common association with refraction and age was estab-
area. Therefore, we choose already a low grade of 0.5 and above on lished, we approximated an average refractive increase of 0.05 dpt
our scale from 0 to 5 as “cortical cataract.” In this way, we defined per year between the age of 35 and 65 years and a refractive de-
4 cataract groups as follows and grouped the patients accordingly: crease of 0.05 dpt per year above the age of 75 years. Between 65
“no cataract” with cortical scale (CS) <0.5 and nuclear scale (NS) and 75 years, we interpolated between the two values of the refrac-
< 4.0; “pure cortical” cataract with CS ≥0.5 and NS < 4.0; “pure tive change. These estimations of the refractive change with age
nuclear” cataract with CS <0.5 and NS ≥4.0; and “mixed cataract” were used to calculate the individual spherical equivalent refractive
with CS ≥0.5 and NS ≥4.0 (Fig. 2). error each patient would have had at the age of 45 years.
Subsequently, the following patient data was collected: age at Because most subgroups for spherical equivalent refractive er-
the time of the photograph; sex; axial length of the eye globe; re- ror, axial length and age were not normally distributed, we used
fraction and visual acuity at the time of the photograph; and refrac- median values and Mann-Whitney U tests for comparison.
tion and visual acuity at an earlier age, if available. Eyes with vi-
sual acuity less than 0.7 logMAR (0.2 on decimal scale) were ex-
cluded. Only one randomly selected eye per patient was included
in the analysis to avoid statistical bias. Spherical equivalent refrac- Results
tive error was calculated. Myopia was defined as refractive error
below –1 dpt and hyperopia as above 1 dpt. The analysis included 239 eyes from 239 patients with
Considering the large age range among our patients (50–90 valid photographs, and a visual acuity of at least 0.7 log-
years) and the refractive change which occurs with age, we decided
to calculate an estimated spherical equivalent refractive error for a MAR (0.2 on decimal scale), aging from 50 to 90 years,
fixed age; as an intent to normalize the refraction to allow a mean- with 76% of cases between 60 and 80 years.
ingful comparison of refraction for the different cataractous Cataract grading was done with whole digits, taking
groups. Because we wanted to use the refractive error as an indica- the mean from three graders. If the variation between the
tor of accommodation efforts, we decided to calculate the refrac- graders was larger than 2, the extreme value was excluded
tive error for the age of 45 years. At this age, there is still some ac-
commodation left and cataracts have not yet developed. An esti- before calculating the mean; this was the case in 15% of
mation of refractive error for even younger ages would introduce eyes for the nuclear gradings and in none for the cortical
considerably more errors for such an estimate. gradings. Nuclear cataract grades ranged from 0 to 8 and
129.127.145.240 - 3/29/2019 5:24:03 PM

Cortical Cataract and Refractive Error Ophthalmic Res 3


DOI: 10.1159/000496865
Univ.of Adelaide
Downloaded by:
0.15

0.10

0.05
Refraction change, dpt/year

-0.05

–0.10

–0.15
30 40 50 60 70 80 90
Age, years

Study Country Type Sample size Years considered


Beaver Dam Eye Study [29] USA Longitudinal 2,783 1987–2017
Blue Mountains Eye Study [27] Australia Longitudinal 2,335 1992–1999
Shufelt et al. 2005 [24] USA Cross-sectional 5,588 1999–2003
Slataper 1950 [25] USA Cross-sectional 4,200 1940–1950
Saunders 1981 [23] UK Cross-sectional 2,688 1985–1987
Saunders 1986 [26] UK Longitudinal 140 1950–1980
Grosvenor et al. 2003 [28] New Zealand Longitudinal 45 1975–1995
Approximated average
Present Spain longitudinal 30 2007–2017

Fig. 3. Data on spherical equivalent refractive error change in di- studies (black continuous line). Longitudinal data from our pres-
opters per year (dpt/year) with age derived from population-based ent study is given as well (thin continuous green line). Data in-
studies: cross-sectional (dashed lines) and longitudinal (continu- cluded from the following studies: Beaver Dam Eye Study [29],
ous lines). Thicker lines indicate studies with larger samples sizes. Blue Mountains Eye Study [27], Shufelt et al. 2005 [24], Slataper
Studies before about 1970 are shown in red, between 1970 and 1950 [25], Saunders 1981 [23], Saunders 1986 [26], Grosvenor et
1990 in blue, and recent studies after about 1990 are shown in al. 2003 [28].
green. An average refractive change was approximated from these

cortical grades from 0 to 4. The estimated spherical equiv- refraction data in order not to skew those results. All cas-
alent refractive error at the age of 45 years for each respec- es of myopia below –6.5 dpt and hyperopia above 6.5 dpt
tive patient was plotted against their cataract grading were excluded. The remaining 199 cases were subdivided
(Fig. 4). This graph revealed some cases with high myo- in the cataract groups defined in the Methods, resulting
pia, which had to be excluded for further analysis of the in 22 cases with “no cataract,” 62 cases with “pure nucle-
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4 Ophthalmic Res Michael/Pareja-Aricò/Rauscher/


DOI: 10.1159/000496865 Barraquer
Univ.of Adelaide
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Nuclear cataract No cataract No cataract Cortical cataract

10 10

Refractive error at 45 years, dpt

Refractive error at 45 years, dpt


0 0

–10 –10

–20 –20 Scale


40
–30 –30 30
20
10
–40 –40 1

10 8 6 4 2 0 0 1 2 3 4 5
Nuclear grading Cortical grading

Fig. 4. Cataract grading of all 239 cases with the corresponding than 0.5 were defined as “no cataract.” Cases with a nuclear grade
spherical equivalent estimated refractive error at the age of 45 equal or above 4 and a cortical grade equal or above 0.5 were de-
years; left panel for the nuclear grading and right panel for the cor- fined as “mixed cataract” (dotted lines). Cases with spherical
tical grading. Data points are binned for whole grading digits. Cas- equivalent refractive error above 6.5 and below –6.5 dpt were ex-
es with a nuclear grade smaller than 4 and a cortical grade smaller cluded from further analysis (dashed lines).

ar” cataract, 42 cases with “mixed cataracts” (cortical-nu- dpt), emmetropes (between –1.0 and +1.0 dpt) and hy-
clear), and 73 cases with “pure cortical” cataract (Fig. 4). peropes (> +1.0 dpt). Cortical cataracts were found in
The majority of subjects within the “pure cortical” 37% of myopes, 82% of emmetropes, and 85% of hyper-
group had refractive error above –2 dpt, whereas the ma- opes (Fig. 6).
jority of “pure nuclear” cataracts were found below –1 dpt
(Fig. 5). Almost all cases according to our “no cataract”
definition had a refractive error below –1 dpt. The “mixed Discussion
cataract” group showed a broad and quite even distribu-
tion over the entire range of refractive error studied. The Starting from our hypothesis that people who accom-
“no cataract” group showed the lowest median refractive modate more have more cortical cataract, we needed a
error (–3.65 dpt), followed by the “pure nuclear” group proxy to estimate accommodation efforts. We choose re-
(–2.69 dpt), both clearly myopic. The median refractive fractive error, because it is common knowledge that
error for “pure cortical” (–0.23 dpt) and “mixed cata- myopes accommodate less than emmetropes and hyper-
racts” (–0.87 dpt) were close to emmetropia (Fig. 5). opes. It was shown that pre-presbyopic myopes have a
For further analysis, we grouped all our cases into two reduced distance facility of accommodation [30, 31]. Two
new groups, having cortical cataract or not. Patients with small limitations are possibly attached to this proxy. First,
cortical cataract had a median refractive error at 45 years we did not know the occupation of each patient with re-
of –0.52 dpt, and without cortical cataract of –2.79 dpt; gard to more near or more far work. However, all our pa-
this difference of 2.27 dpt was significant (p < 0.001). In- tients are from developed, industrialized countries where
terestingly, there was no difference between both groups in the past 40 years the large majority has an occupation
when comparing axial length (22.9 and 23.2, respectively requiring mostly near work. Thus, we assumed that the
with p = 0.223) and age of the patient (72.6 and 69.7, re- large majority had a very similar demand for accommo-
spectively with p = 0.091). dation. Secondly, the use of glasses for far and near work
Figure 6 shows the histogram of refractive error for the was not known for each individual. However, myopes at
cortical cataract group and the group without cortical cat- the onset of presbyopia can remove their distance glasses
aract. Both histograms were divided for myopes (< –1.0 for near work to avoid accommodation and hyperopes
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Cortical Cataract and Refractive Error Ophthalmic Res 5


DOI: 10.1159/000496865
Univ.of Adelaide
Downloaded by:
Cortical n = 73
8 M = –0.23 dpt

Mixed n = 42
8 M = –0.87 dpt

Nuclear n = 62
8 M = –2.69 dpt
Frequency

No cataract n = 22
8 M = –3.65 dpt

All cases n = 199


20 M = –1.48 dpt

10
Fig. 5. Histogram distribution of spherical
equivalent estimated refractive error at the 0
age of 45 years for our 4 different cataract –6 –4 –2 0 2 4
groups. Median (M) is shown as dashed Refractive error at 45 years, dpt
line. Below, the overall distribution is given
for all 199 evaluated cases.

can be reluctant to use reading glasses resulting in contin- literature quite well until ages of 70 years. For ages
ued more accommodation efforts. Therefore, the un- above 70 years, our data showed a higher myopic shift
known use of glasses probably only induced small varia- as the much larger longitudinal studies Beaver Dam and
tion overall in our estimation on accommodation efforts. Blue Mountains and was closer to an older cross-sec-
The estimation of the refractive error at the age of 45 tional study.
years was based on literature data on refractive change Patient for our study were selected based on photo-
with age. The data from the literature was based on al- graphs prior to cataract surgery. The refraction was not
together more than 17,000 individuals and was quite known at that stage of the study. We found a considerable
consistent (Fig. 3). In order to check the mean refractive number of high and very high myopes in our patient co-
change obtained from the literature with our sample of hort. Because high myopia was not the topic of our study
patients, we calculated the longitudinal refractive error and to avoid bias with our statistical calculations, we de-
change in 30 cases, where this data was available. As can cided to exclude all cases with high myopia and do the
be seen in Figure 3, our data match the data from the same for any cases of high hyperopia. We choose –6.5 dpt
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6 Ophthalmic Res Michael/Pareja-Aricò/Rauscher/


DOI: 10.1159/000496865 Barraquer
Univ.of Adelaide
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20 Cortical cataract n = 115
M = –0.52 dpt
15 37% 82% 85%

10

Frequency
20 No cortical cataract n = 84
M = –2.79 dpt
15 63% 18% 15%

10
Fig. 6. Histogram distribution of spherical
equivalent estimated refractive error at the 5
age of 45 years grouped for having cortical
cataract or not. Both histograms are divid- 0
ed for myopes, emmetropes, and hyper-
opes and the percentage of cases with or –6 –4 –2 0 2 4
without cortical cataract within each re- Refractive error at 45 years, dpt
fractive group are given. Median (M) is
shown as dashed line.

as cutoff because definitions in the literature vary be- with 3,400 cases) differentiated between hyperopia, em-
tween < –5 and < –8 dpt according to a report from WHO metropia, mild myopia, moderate myopia, and high my-
[32] with most common values around –6 dpt. opia and found a higher risk for nuclear cataract with my-
Even after excluding cases with high myopia, we had a opia as compared with hyperopia and a higher risk of cor-
large proportion, 55%, of myopes, 25% emmetropes, and tical cataract with hyperopia as compared with myopia
20% hyperopes in our cohort (Fig. 5). This compares to a [39]. A cross-sectional study of 3,650 people showed that
proportion of 38% myopes, 46% emmetropes, and 17% a history of wearing distance glasses was associated with
hyperopes, aged 40–59 years in a general population in the presence of nuclear cataract, but not with cortical cat-
the USA [33]. Other studies of the general population for aract. A weak association was found between cortical cat-
the same age range but defining myopia as < –0.5 dpt find aract and hyperopia [40].
proportions of myopes of 25, 43 or 44% [34–36]. This dif- A comparative study of refraction before cataract sur-
ference is probably explained by our cohort of patients gery in India revealed that eyes with cortical cataract had
scheduled for cataract surgery, which considers only 50– a mean refraction of +2.75 and with nuclear cataract
70% of the general aged population [37]. Furthermore, –3.75 dpt [15]. Our results showed the same tendency,
most cataract patients are operated to remove nuclear but with less difference between groups; we found for
lens opacities which are known to be related to more my- pure cortical cataracts a median refractive error of –0.23
opic eyes [38]. dpt and for pure nuclear cataracts it was –2.69 dpt. A pos-
Based on the analysis of the current article, we found sible reason for this might be the different age of the cata-
that myopes have considerably less cortical cataracts ract patients, in the study from India between 30 and 45
(37%) as compared to emmetropes (82%) and hyperopes years and in our present study it was between 50–90 years
(85%) (Fig. 6). This corresponds well with earlier popula- with a median of 71 years.
tion-based studies. A meta-analysis which combined 12 Early cortical cataracts begin near the lens equator, be-
studies with 38,000 cases showed that myopia is associ- hind the iris and are therefore seldom detected in vivo.
ated with nuclear cataract, but not with cortical cataract Studies in postmortem lenses, where the entire lens can
[38]. One major population-based, cross-sectional study be seen, show that segmental or annular cortical cataracts
from this meta-analysis (The Singapore Indian Eye Study have a low prevalence of 11% at the age between 31 and
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Cortical Cataract and Refractive Error Ophthalmic Res 7


DOI: 10.1159/000496865
Univ.of Adelaide
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45 years which increases to 45% in the age group 61–75 Acknowledgments
years and remains rather stable in older age groups with
Dr. F.G. Rauscher is supported by a grant from the German
48% between 76–90 years [10, 21]. This shows that corti- Federal Ministry of Education and Research: i:DSem – Integrative
cal cataracts develop at the time of the onset of presbyopia data semantics in systems medicine (grant number 031L0026).
and – in contrast to nuclear cataracts – do not gradually
increase with aging [11].
Statement of Ethics
Cataracts are generally considered a multifactorial dis-
ease and largely caused by lifelong accumulation of oxida- Ethics committee approval was not required for this retrospec-
tive stress, influenced by environmental and genetic fac- tive observational study. The work was carried out in accordance
tors, life style, exposure to ultraviolet radiation, diet and with the Code of Ethics of the World Medical Association (Decla-
other systemic diseases [10, 41]. The mechanical force ration of Helsinki).
acting on the lens during accommodation may induce di-
rectly morphological damage to the lens fibers leading to Disclosure Statement
cortical cataract or they may make the zones of shear
stress inside the lens more vulnerable to environmental The authors have no conflicts of interest to declare.
factors, like ultraviolet radiation, and in this way lead to
cortical cataract [15]. Author Contributions
In summary, emmetropes and hyperopes tend to de-
velop more cortical cataract than myopes. These cortical R.M. designed the study, acquired data, analyzed data, inter-
preted data, wrote the manuscript, revised the manuscript; L.P.-A.
cataracts might be caused by shear stress inside the crys- acquired data, revised the manuscript; F.G.R. interpreted data, re-
talline lens due to accommodation efforts at the time of vised the manuscript; R.I.B. revised the manuscript, obtained
onset of presbyopia. funding.

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129.127.145.240 - 3/29/2019 5:24:03 PM

Cortical Cataract and Refractive Error Ophthalmic Res 9


DOI: 10.1159/000496865
Univ.of Adelaide
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