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Light Exposure and the Risk of Age-Related Macular Degeneration
The Pathologies Oculaires Liées à l'Age (POLA) Study
Cécile Delcourt, PhD;
Isabelle Carrière, MSc;
Alice Ponton-Sanchez, MSc;
Sylvie Fourrey, BSc;
Annie Lacroux, MSc;
Laure Papoz, PhD;
for the POLA Study Group
Arch Ophthalmol. 2001;119:1463-1468.
ABSTRACT
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Background The role of light exposure in the development of age-related macular
degeneration (ARMD) has been questioned. We present the relationship between
lifetime light exposure and ARMD as examined in the Pathologies Oculaires
Liées à l'Age (POLA) study.
Methods The POLA study is a population-based study on cataract and ARMD and
their risk factors. It included 2584 residents of the town of Sète,
located in the South of France. The presence of early and late ARMD was assessed
on the basis of 50° color fundus photographs using an international classification
system. A questionnaire about light exposure was administered.
Results Late ARMD (n = 38) was not significantly associated with any light exposure
variable. Subjects exposed to high ambient solar radiation and those with
frequent leisure exposure to sunlight had a decreased risk of pigmentary abnormalities
(odds ratio [OR] = 0.61; 95% confidence interval [CI], 0.39-0.93, and OR =
0.70; 95% CI, 0.52-0.95, respectively) and of early signs of ARMD (OR = 0.73;
95% CI, 0.54-0.98, and OR = 0.80; 95% CI, 0.64-1.00, respectively). Subjects
who had used sunglasses regularly had a decreased risk of soft drusen (OR
= 0.81; 95% CI, 0.66-1.00). These relationships were not modified by further
adjustments for potential confounders.
Conclusion Our study does not support a deleterious effect of sunlight exposure
in ARMD.
INTRODUCTION
AGE-RELATED macular degeneration (ARMD) is the leading cause of blindness
among older people in Western countries.1 With
the aging of the population, the burden of ARMD is expected to increase dramatically.
A tremendous effort has been made in the last decade to develop treatments
for choroidal neovascularization, the type of late ARMD that is the most frequent
cause of severe visual loss. In particular, photodynamic therapy has recently
proved beneficial for patients with classic choroidal neovascularization.2 Unfortunately, many patients remain ineligible for
these treatments. In addition, although they are effective, such treatments
do not completely stop the course of the disease; severe visual loss still
occurs in many of the patients. To have a major effect on the extent of severe
vision loss in patients with ARMD, we must attack the disease much earlier
in its course. Therefore, it is urgent to determine factors that may lead
to the prevention of this disorder.
The pathogenesis of ARMD is poorly understood. It is probably multifactorial,
involving genetic factors,3-4
adverse effects caused by tobacco smoking,5
and a possible association with atherosclerosis.6
In addition, exposure to sunlight has long been suggested to play a role in
its etiology. However, previous epidemiological studies have yielded inconsistent
results: whereas most studies found no association between sunlight exposure
and ARMD,7-9 others
found either a positive association with some exposure variables10-11
or a negative association.12
The Pathologies Oculaires Liées à l'Age (POLA) study is
an epidemiological study that took place in Sète, France, and was designed
to identify risk factors for cataract and ARMD. Sète is a harbor town
of 40 000 inhabitants located on the French Mediterranean Sea. Its principal
economic activities are fishing, oyster farming, tourism, and industry. This
town is located near our research center and was chosen because of the various
types and amounts of sunlight exposure in its population (eg, fishers and
oyster farmers with high lifetime-exposure to sunlight, people from other
countries in southern Europe, French people born in northern Africa, and retirees
from northern France). Whereas most epidemiological studies on age-related
eye diseases and sunlight exposure have been conducted in the United States
and Australia, ours is one of the few European studies on this subject and
the first in France. We present the associations between ARMD and sunlight
exposure.
PARTICIPANTS, MATERIALS, AND METHODS
STUDY POPULATION
The objective of the POLA study was to examine age-related eye diseases
(cataract and ARMD) and their risk factors. The methods of this study have
already been published elsewhere.13 The following
criteria were necessary for inclusion: (1) being a resident of the town of
Sète; and (2) being 60 years or older on the day of the baseline examination.
According to the 1990 population census, almost 12 000 residents were
eligible. Our objective was to recruit 3000 participants so that we would
have sufficient statistical power to detect associations between the studied
risk factors and age-related eye diseases. Between June 1995 and July 1997,
we recruited 2584 participants, including 1133 men and 1451 women with an
average age of 70.4 years. Participants gave written consent for their inclusion.
The design of this study was approved by the ethical committee of the University
Hospital of Montpellier, Montpellier, France.
OPHTHALMOLOGIC EXAMINATION
This examination included a record of ophthalmologic history and iris
color (blue or gray, green or light brown, or dark brown) and a measure of
best-corrected far visual acuity in the right and left eyes. After pupil dilation,
a standardized assessment of lens opacities using a slitlamp and one 50°
color photograph (Kodak Gold 100 ASA; Eastman Kodak Co, Rochester, NY) centered
on the macular area was obtained for each eye.
CLASSIFICATION OF ARMD
Late ARMD and early signs of ARMD were defined according to an international
classification system14 on the basis of 50°
color photographs centered on the macular area in each eye. Late ARMD was
defined by the presence of neovascular ARMD or geographic atrophy within the
grid (3000 µm from the foveola). Neovascular ARMD included serous or
hemorrhagic detachment of the retinal pigment epithelium or sensory retina,
subretinal or sub–retinal pigment epithelium hemorrhages, and fibrous
scar tissue. Geographic atrophy was defined as a discrete area of retinal
depigmentation 175 µm or larger characterized by a sharp border and
the presence of visible choroidal vessels.
Soft drusen included soft intermediate drusen (>63 µm but  125
µm) as well as soft distinct and indistinct drusen (>125 µm with
uniform density and sharp edges or with decreasing density from the center
outward and fuzzy edges, respectively). Pigmentary abnormalities were defined
as areas of hyperpigmentation and/or hypopigmentation (without visibility
of choroidal vessels). Early signs of ARMD included the presence of soft drusen
and/or pigmentary abnormalities.
The participants were classified according to their worse eye. Fundus
photographs were not taken in 81 cases (3.1%): in 42 cases because of technical
failure, in 9 cases because of refusal, in 5 cases because of contraindication
of dilation, in 17 cases because of poor dilation or severe opacities of the
lens or cornea, and in 8 cases because of poor cooperation. In addition, for
307 subjects, photographs were ungradable in both eyes because of technical
failure or the presence of opacities. Thus, gradable photographs were available
in at least 1 eye for 2196 subjects (85%). Among those, 1992 participants
(90.7%) had gradable photographs in both eyes.
INTERVIEW DATA
Data were collected by trained study personnel who were unaware of ARMD
status. A standardized interview was performed to assess sociodemographic
variables (eg, marital status, educational level, and major lifetime occupation),
medical history (eg, hypertension, cardiovascular disease, diabetes, or osteoarthritis),
use of medications, and smoking history.
The subject was then asked about residential history, professional exposure
to sunlight (work on the sea [eg, fishing or oyster farming], driving, agriculture,
the construction industry, and others) or to artificial light (arc welding,
photography, the entertainment industry, and others), duration of this professional
exposure (years), leisure exposure to sunlight (beachgoing, sailing, fishing,
skiing, and others), use of sunglasses, and sunbathing habits. Locations in
France were divided into 101 geographical areas, corresponding to the 101
administrative departments. The interviewer then measured height, weight,
waist and hip circumferences, and systolic and diastolic blood pressures.
Body mass index was defined as the weight in kilograms divided by the height
in meters squared. Lipid-standardized plasma  -tocopherol was defined
as -tocopherol in micromoles divided by cholesterol in millimoles plus
triglycerides in millimoles.
AVERAGE ANNUAL AMBIENT SOLAR RADIATION
Methods for estimating average annual ambient solar radiation have been
published elsewhere. In each location, ambient annual solar radiation (a measure
of solar energy including all wavelengths) was estimated using astronomical
formulas and statistics regarding hours of sunshine.15
For each participant, the average annual ambient solar radiation was estimated
using the residential history by weighting the annual ambient solar radiation
at each location by the time spent at that location. The average was based
on the first 60 years of life because nearly all of the subjects lived in
Sète after age 60 years.
In France, statistics regarding hours of sunshine for the past 30 years
are available in 72 departments.16 Departments
without this information were given the value of data from the nearest available
location. For foreign countries, annual solar radiation was generally estimated
for the capital; when the capital was situated far from the middle of the
country, a more centralized location was chosen. Very large countries (for
example, the United States or China) were excluded from this analysis because
an estimation of solar radiation in a single geographic location is meaningless
for these areas.
For several countries, statistics on hours of sunshine were unavailable,
impeding the estimation of solar radiation. When the amount of time spent
in such areas was 3 years or less for a particular subject, these countries
were eliminated from the calculations. Thus, for 56 subjects the average ambient
solar radiation was based on 57, 58, or 59 years instead of 60.
Of the 2196 subjects with available ARMD status, 79 subjects were excluded
from the analysis because they had spent more than 3 years in countries where
solar radiation could not be estimated, and 28 subjects were excluded because
they had missing data for other variables related to sunlight exposure (leisure
and/or professional exposure, use of sunglasses, etc). Therefore, data on
sunlight exposure were available for 2089 (95.1%) of 2196 subjects.
BIOLOGIC MEASUREMENTS
Biologic measurements were made from fasting blood samples obtained
at subjects' homes on the morning of the examination. They included measurements
on plasma (cholesterol, triglycerides, and vitamins A, E, and C) and on red
blood cells (reduced glutathione). In particular, retinol and -tocopherol
were measured by high-performance liquid chromatography according to the method
previously described by Catignani and Bieri.17
One sample of the liotrol mixture was measured in each series as an internal
standard to prevent any shift during the study.
STATISTICAL ANALYSIS
For each light exposure variable, age- and sex-adjusted odds ratios
(ORs) were obtained using logistic regression with either late ARMD, soft
drusen, or pigmentary abnormalities as the dependent variable and age, sex,
and light exposure as the independent variables. Annual ambient solar radiation
was divided into 3 groups (lower quartile, intermediate quartiles, upper quartile).
For each retinal variable (late ARMD, soft drusen, and pigmentary abnormalities),
a multivariate logistic model was performed using age, sex, all light exposure
variables that were close to significance in the first model (P<.10), and potential confounding factors (smoking [current, former],
history of cardiovascular disease [coronary heart disease and/or stroke and/or
angioplasty], obesity [body mass index >30 kg/m2], lipid-standardized -tocopherol
[lower quartile, intermediate quartiles, upper quartile], and educational
level [grade school, middle school, completion of high school or university]).
Subjects with missing data for the confounding factors were excluded from
multivariate analyses. Of the 2089 subjects with available ARMD status and
sunlight exposure data, we excluded 53 subjects. Therefore, the multivariate
analyses were performed on 2036 subjects. All statistical analyses were done
using SAS statistical software (SAS Institute Inc, Cary, NC).
RESULTS
Table 1 presents the prevalence
of ARMD according to age and sex. The prevalence of late ARMD increased sharply
with age, from 0.3% for subjects younger than 70 years to 10.1% for those
80 years and older. There were no differences between men and women. In men,
the prevalence of soft drusen increased from 19.4% for participants younger
than 70 years to 27.5% for those 80 years and older. The prevalence was slightly
higher in women, varying from 20.5% for those younger than 70 years to 33.1%
for subjects 80 years and older. The prevalence of pigmentary abnormalities
was higher in men than in women: in men, it varied from 11.8% for subjects
younger than 70 years to 17.6% for those 80 years and older, and in women,
from 7.5% for participants younger than 70 years to 14.2% for those 80 years
and older.
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Table 1. Prevalence of Age-Related Macular Degeneration According to
Age and Sex in the POLA Study*
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Table 2 presents the distribution
of the light exposure variables in the POLA study. The median of the annual
ambient solar radiation was 562 kJ/cm2 with a range of about 300
kJ/cm2, showing an important inter-individual variability. This
variability was due to differences in geographic origin: almost 60% of the
participants were born in the South of France, about 20% were born in other
parts of France, more than 15% were born in northern Africa (the latter remained
there for a median of 33 years, which corresponds to these countries gaining
independence in the 1960s), and about 5% were born in southern Europe. Professional
exposure to sunlight was frequent in men (32.5%) and rare in women (2.7%).
Professional exposure to artificial light was rare in both sexes (4.5% in
men and 0.4% in women). Leisure exposure to sunlight was extremely common:
three fourths of the participants had frequently participated in leisure activities
at sea (eg, beachgoing, sailing, or fishing), which is not surprising because
the majority had lived in coastal areas for most of their lives. In addition,
about 15% frequently participated in leisure activities involving snow, and
47.6% of men and 37.6% of women often took part in outdoor activities on land
(eg, gardening, hiking, or bicycling). About 40% of the participants had regularly
used sunglasses, and more than 40% of men and 30% of women declared that they
liked to sunbathe.
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Table 2. Distribution of Light Exposure Variables in the POLA Study*
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Table 3 presents the association
between light exposure variables and characteristics of ARMD. Late ARMD was
not significantly associated with any of the light exposure variables. Pigmentary
abnormalities were less frequent in participants exposed to higher ambient
solar radiation (P = .02) and in those who spent
regular leisure time by the sea (P = .02). This was
also true globally for early signs of ARMD (P = .04
and P = .05, respectively); the same tendency was
observed for soft drusen, although this association did not reach statistical
significance (P = .07 for annual ambient solar radiation; P = .11 for leisure time by the sea). Participants who
claimed to have used sunglasses regularly had a reduced risk of soft drusen
(P = .05). The same tendency was observed for late
ARMD, but it did not reach statistical significance (P
= .13). No association was observed for pigmentary abnormalities or early
signs of ARMD. Finally, we observed no strong association between eye color
and any characteristics of ARMD.
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Table 3. Sex- and Age-Adjusted Odds Ratios and 95% Confidence Intervals
Between Light Exposure Variables and Age-Related Macular Degeneration in the
POLA Study*
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Further adjustments for the other risk factors identified in our study
(smoking, cardiovascular disease, body mass index, lipid-standardized plasma -tocopherol
level, and educational level) did not modify these results: a negative association
with ambient solar radiation was found for pigmentary abnormalities (OR =
0.59; 95% confidence interval [CI], 0.38-0.91; P
= .02 for upper quartile vs lower quartile) and to a lesser degree for soft
drusen (OR = 0.76; 95% CI, 0.55-1.05; P = .09 for
upper quartile vs lower quartile). Frequent use of sunglasses was negatively
associated with soft drusen (OR = 0.79; 95% CI, 0.64-0.98; P = .03), and leisure exposure by the sea was negatively associated
with pigmentary abnormalities (OR = 0.72; 95% CI, 0.53-0.98; P = .04).
COMMENT
In the absence of statistics for ambient UV-B levels in France, we estimated
ambient solar radiation, a measure of solar energy reaching the ground that
includes all wavelengths. As in the Beaver Dam Eye Study,18
we used residential history to estimate individual annual ambient solar radiation.
Therefore, this estimate represents potential exposure rather than actual
ocular exposure, such as that estimated in studies performed in Maryland19-21 that included a detailed
assessment of ocular exposure derived from interviews combined with field
and laboratory data.
In our study, ambient solar radiation was not significantly associated
with an increased risk of ARMD. The risk of early signs of ARMD even decreased
in subjects exposed to high ambient solar radiation (OR = 0.73; P = .04). The associations were similar but did not reach statistical
significance for late ARMD (OR = 0.44; P = .14).
Previous studies generally found no association between ARMD and UV-B exposure7-11;
some even found a significant negative association.12
Using identical methods, the same studies consistently found a positive
association between UV-B exposure and cortical cataract.15, 18-19,21
Therefore, it is unlikely that the lack of association between UV-B exposure
and ARMD is due to inappropriate estimation of exposure. Moreover, nearly
all UV light is absorbed by the cornea and lens.22
Phakic subjects are naturally protected against the potentially harmful effect
of UV light on the retina. On the basis of epidemiologic data and biologic
plausibility, it seems unlikely that UV light increases the risk of ARMD in
phakic subjects.
Blue light in the visible spectrum may be harmful to the retina: in
the Watermen Study,10 although UV light was
not related to ARMD, there was a significant association with blue light.
In our study, we could only estimate ambient solar radiation, including all
wavelengths (infrared, visible, and UV). It is difficult to analyze the effects
of the different wavelengths because they are naturally highly correlated.
The use of eyeglasses, which attenuate UV light but not visible light, may
make a difference. In the Watermen Study, the association between ARMD and
blue light was mainly due to a more frequent use of eyeglasses in subjects
with ARMD. The association between ARMD and blue light needs to be examined
further.
In addition to ambient solar radiation, we studied the association between
professional and leisure exposure to light and the different characteristics
of ARMD. Consistent with the findings for ambient solar radiation, leisure
exposure by the sea was negatively associated with pigmentary abnormalities
(OR = 0.70; P = .02). A negative association between
ARMD and ocular light exposure was also found in an Australian study.12 It has been suggested that the relationship between
ARMD and sunlight exposure may be confounded by sun sensitivity. In 2 studies,
ARMD patients showed higher sun sensitivity than controls.12, 23
Sun sensitivity was related to lower sunlight exposure. Unfortunately, we
have no estimation of sun sensitivity in our study and could not take into
account its potential confounding effect.
By contrast, frequent use of sunglasses was associated with a reduction
in the risk of soft drusen (OR = 0.81; P = .05) but
not of late ARMD or pigmentary abnormalities. Other light-related variables
were not significantly associated with early or late ARMD. We found no significant
associations between iris color and ARMD characteristics.
Our study has several limitations. First, our sample underrepresents
the older population and overrepresents the middle and upper social classes
in comparison with the total eligible population.13
Thus, the subjects in this study may be healthier and may have different lifestyle
habits (in particular, concerning light exposure) than the general population.
This is likely to have affected the prevalence of ARMD or the distribution
of sunlight exposure variables. However, it is unlikely to have affected the
association between ARMD and light exposure. Moreover, our sample is probably
not highly biased because the prevalence rates of late ARMD and early signs
of ARMD are similar to those of previous studies using the same grading protocol.24-26
Another limitation is the small number of cases of late ARMD, leading
to low statistical power to detect any association between light exposure
variables and late ARMD. This was also the case in most of the previous studies.8, 10-11 In the 2 studies with
sufficient statistical power, either no association9
or a negative association was found.12 In our
study, the association between late ARMD and ambient solar radiation is also
in the negative direction. Although statistical power is limited, it is unlikely
that the true association is positive.
Our finding of a protective, biologically implausible association between
light exposure and ARMD lesions raises concerns about possible spurious associations
due to uncontrolled confounding. These associations remained significant after
adjustment for the previously identified risk factors (smoking, cardiovascular
disease, body mass index, plasma -tocopherol level) for ARMD and for
socioeconomic status. Other potential confounders include differences in dietary
habits; diets in the South of France are known to be different from those
in the northern part of the country. There may also be genetic differences,
particularly in the genotype of apolipoprotein E, which has recently been
shown to be related to ARMD.27-28
Unfortunately, we have no data for these potential confounders.
Misclassification is also a concern in epidemiological studies because
we usually have limited information on the pathologic characteristics of the
disease. Validation studies using the same international classification have
demonstrated good reproducibility for the classification of early and late
ARMD lesions.26, 29-30
However, with only a single photograph of variable quality per eye, misclassification
may occur and may bias the estimations toward the null hypothesis. Therefore,
we may have underestimated the associations between light exposure and ARMD.
Because this study is cross-sectional, recall bias may have affected
the results, particularly concerning professional and leisure exposure to
sunlight. All previous studies were either cross-sectional or case-control
and may have been equally subject to recall bias. However, because soft drusen
and pigmentary abnormalities are asymptomatic, recall bias is unlikely to
have affected the associations between light exposure variables and early
signs of ARMD.
In conclusion, this study gives no support to a deleterious effect of
sunlight exposure in ARMD. The negative association between ambient solar
radiation and early signs of ARMD needs to be examined further.
AUTHOR INFORMATION
Accepted for publication March 30, 2001.
This study is supported by the Institut National de la Santé
et de la Recherche Médicale, Paris, France; by grants from the Fondation
de France, Department of Epidemiology of Ageing, Paris; the Région
Languedoc-Roussillon, Montpellier, France; the Fondation pour la Recherche
Médicale, Paris; and the Association Retina-France, Toulouse; and by
Rhône Poulenc, Essilor, and the Centre de Recherche et d'Information
Nutritionelles, Paris.
Corresponding author and reprints: Cécile Delcourt, PhD, INSERM
Unité 500, 39 Avenue Charles Flahault, 34093 Montpellier, CEDEX 5,
France (e-mail: delcourt{at}montp.inserm.fr).
From the Institut National de la Santé et de la Recherche Médicale
(INSERM), Montpellier, France. A complete list of the members of the POLA
Study Group was published previously (Arch Ophthalmol.
1998;116:1033).
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Br. J. Ophthalmol. 2006;90:784-792.
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Intraocular Lenses Should Block UV Radiation and Violet but Not Blue Light
Mainster
Arch Ophthalmol 2005;123:550-555.
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Sunlight and the 10-Year Incidence of Age-Related Maculopathy: The Beaver Dam Eye Study
Tomany et al.
Arch Ophthalmol 2004;122:750-757.
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How much blue light should an IOL transmit?
Mainster and Sparrow
Br. J. Ophthalmol. 2003;87:1523-1529.
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A Strong and Highly Significant QTL on Chromosome 6 that Protects the Mouse from Age-Related Retinal Degeneration
Danciger et al.
IOVS 2003;44:2442-2449.
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