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(Investigative Ophthalmology and Visual Science. 2001;42:614-619.)
© 2001 by The Association for Research in Vision and Ophthalmology, Inc.

Relation between Size at Birth and Age-Related Cataract

Nigel F. Hall, Catharine R. Gale, Holly Syddall, Christopher N. Martyn and David I. W. Phillips

From the MRC Environmental Epidemiology Unit, University of Southampton, United Kingdom.


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
PURPOSE. To determine whether poor fetal growth, as determined by size at birth, is associated with an increased risk of age-related cataract.

METHODS. A total of 741 men and women born in Sheffield, England between 1922 and 1930 and whose size at birth was available were traced and invited to take part in the study. Of these, 392 (53%) attended for ophthalmic examination. Lens opacity in these volunteers was graded using the Lens Opacities Classification System (LOCS) III.

RESULTS. After adjusting for age, gender, gestational age, and risk factors for cataract there were no consistent associations between size at birth and age-related cataract. However, the odds ratio for nuclear cataract (opalescence) among subjects whose birth weight was more than 8 lb was 2.4 (95% CI 1.2 to 5.0) compared with those who weighed under 6 lb 12 oz at birth. Risk of cortical cataract by contrast fell with increasing birth weight, but the trend was not significant and became weak after adjusting for gestational age and other risk factors for cataract. No relation was evident between risk of posterior subcapsular cataract and size at birth.

CONCLUSIONS. There is no consistent association between size at birth and age-related cataract. The higher risk of nuclear cataract with increased birth weight was contrary to the expected trend. The apparent difference in direction of the relation between birth weight and different subtypes of cataract may be a chance finding but warrants further exploration.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Although age-related cataract is the commonest form of visual impairment worldwide,1 much remains to be understood about its etiology.2 Although genetic factors3 4 5 and various exposures in adult life6 7 8 9 10 are thought to play a part, little is known about how early development might affect later risk of cataract formation.

The synthesis of lens crystallins by the fiber cells starts in the embryonic period and continues throughout life.11 As the turnover of crystallins is negligible,11 these proteins persist in the lens throughout life,12 their transparency depending on their structural integrity.11 13 It is well established that adverse influences during fetal life including viral infections,14 15 metabolic disturbance,16 premature birth,17 and maternally administered drugs,18 which are thought to disrupt fiber cell maturation, may lead to congenital cataract. It is not known whether less severe perturbations of fetal growth may lead to more minor abnormalities of lens development that could predispose to cataract development in later life, though a recent report showed that a low growth trajectory in early life with reduced weight at the age of 1 year old was associated with a twofold risk of nuclear cataract.19

We have therefore examined the relationships between fetal growth and age-related cataract in a group of men and women born in a maternity hospital in Sheffield, UK, in 1922–1930, whose recorded birth measurements are still available. Because cataract may occur in anatomically distinct sites,2 we examined the influence of fetal growth on nuclear, cortical, and posterior subcapsular cataract.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
All women admitted for childbirth to the Jessop Hospital for Women, Sheffield, had details of their confinement recorded on standard forms. Details included date of last menstrual period, birth weight, placental weight, head and abdominal circumferences, and crown-heel length. We asked the Office of National Statistics to trace all 4793 people whose births were recorded between 1922 and 1930 using the NHS Central Register. To facilitate the contact and examination of subjects, we confined the trace to those individuals still living in the Sheffield area who were thus eligible to be selected to take part in the study. Stratified sampling was used to select all 159 subjects from the highest and all 77 subjects from the lowest fifths of birth weight and 85 randomly chosen subjects of each sex from each of the three intervening fifths of birth weight. Having obtained permission from the General Practitioners, we wrote to 741 people asking whether we could interview them at home. Of these, 412 (56%) agreed, and were interviewed by a fieldworker.

The participants were invited to a clinic at the Northern General Hospital Sheffield, and 392 (95% of those interviewed) agreed to attend. At the clinic we measured participants’ height with a portable stadiometer and weight with a Seca scale. We took a fasting venous blood sample that was subsequently analyzed for percentage of glycosylated hemaglobin. We determined plasma levels of carotenoids using high performance liquid chromatography. We determined the refractive error by measuring subjects’ usual distance glasses with a Lensmeter (Nidek LM-350; Nidek Co. Ltd., Aichi, Japan) after first assessing each eye’s visual acuity (at 4 m) with a Baillie-Lovie LogMAR chart (Lighthouse Enterprises, Long Island City, NY). Retinoscopy and subjective refraction was carried out on all eyes failing to read LogMAR 1.2 or better. Subjects who did not habitually wear distance glasses were assumed to be emmetropic if their unaided visual acuity was LogMAR 1.2 or better. We calculated the spherical equivalent for each eye by adding the spherical error to half the cylindrical component.

One observer graded all subjects for lens opacity at the slit-lamp (Nidek SL-250; Nidek Co. Ltd.) using the Lens Opacities Classification System (LOCS) III,20 21 in a darkened examination room according to the stated protocol. We placed the LOCS III standards on an illuminated viewing box mounted just above and behind the subject’s right shoulder as they were seated at the slit-lamp. We dilated the pupils of each subject with tropicamide 1% and phenylepherine 2.5% before the grading session. The grader (NH) carried out a pilot study using LOCS III standards before beginning the present study.22

The research followed the tenets of the Declaration of Helsinki, and the study was approved by the South Sheffield Research Ethics Committee. All subjects gave written informed consent.

The presence of cataract was classified according to the LOCS III score in the worse eye. The presence of nuclear opalescent and nuclear color cataract was defined by a score of 3.0 or more in the worse eye on the LOCS III NO and NC scales. Cortical cataract was defined by a score of 2.0 or more in the worse eye on the LOCS III C scale, and posterior subcapsular cataract by a score of 0.5 or more in the worse eye on the LOCS III P scale. These definitions of cataract are similar to those adopted by previous investigators.19 23 We excluded 20 subjects, 11 of whom had previously had bilateral cataract surgery (making it impossible to assign them to a category), and 9 of whom had a form of cataract that was not age-related. The analyses that follow are therefore based on 372 subjects. We used the two-sample t-test, the {chi}2 test, and the Wilcoxon Rank–Sum test, to analyze the relation between presence or absence of each form of cataract and known risk factors for cataract. We used logistic regression to analyze the relation between early life measurements and each type of cataract, with adjustment for potential confounding variables. The odds ratios (with 95% confidence intervals) for each form of cataract according to approximate thirds of the distribution of the early life variables are presented, together with P values for the trend in the odds ratios across the groups. Numbers within groupings of early life variables differ because of rounding of the original birth measurements.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Of the 392 subjects who attended the clinic, 198 (50.5%) had at least one type of age-related cataract, or had had previous cataract surgery. Of the 372 men and women who are included in the analysis, 103 (27.7%) had evidence of nuclear opalescence, 123 (33.1%) had increased nuclear color, 99 (26.6%) had cortical cataract, and 43 (11.6%) had posterior subcapsular opacity.

Table 1 summarizes the age, gender, level of obesity, and other known risk factors for cataract in our study subjects according to the presence or absence of the different types of age-related cataract. Women were more likely to develop nuclear opalescent cataract (35% of women vs. 22% of men, {chi}2 = 8.27, P = 0.004) but there were no gender differences in prevalence of other types of cataract. Men and women with nuclear or cortical cataract were significantly older than subjects without these types of opacity. There was no significant age difference, however, between subjects with and without posterior subcapsular cataract. There were no significant differences in body mass index (weight/height2) between subjects with and without any of the three types of cataract. Nuclear opalescent and nuclear color cataract were found to have a very similar profile of associations in the univariate analysis, hence only the results for nuclear opalescent cataract are shown in Table 1 . The subjects with nuclear cataract had significantly lower levels of the antioxidant alpha carotene. They also had lower reported alcohol intake than the subjects without cataract. There were no differences in the prevalence of other risk factors for nuclear cataract except that nonmanual occupational social class was associated with less risk of increased nuclear color cataract (23% vs. 34%, P = 0.03). There was no significant association between female gender and nuclear color cataract. Subjects with cortical cataract were found to have significantly lower plasma concentrations of the carotenoid cis-lycopene, and had significantly higher cigarette consumption. Cortical and posterior subcapsular types of cataract were associated with higher levels of glycosylated hemaglobin (HbA1c). However, the elevation was statistically significant only for cortical opacity. Posterior subcapsular cataract was significantly associated with myopia, and with subjects who reported receiving a course of systemic steroids lasting 2 weeks or more in the 5 years before the study, but not with any of the other factors presented in Table 1 . None of these risk factors were significantly related to birth weight or other measurements of fetal growth (data not shown).


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  		Table 1. Characteristics of the Study Population According to the Presence of Nuclear, Cortical, and Posterior Subcapsular Cataract

 
Table 2 shows how the risk of nuclear cataract is related to the measurements of early growth. In these analyses, the odds ratios (or risk) of nuclear cataract are shown according to approximate thirds of the distribution of birth measurements before and after adjustment for gestation and risk factors for nuclear cataract. The associations between birth measurements and nuclear cataract were similar for both opalescence and color, hence the results are shown for nuclear opalescent cataract only (Table 2) . Nuclear cataract risk was significantly higher in people who had been heavier at birth. After adjustment for known risk factors, men and women whose birth weight was more than 8 lb had an odds ratio for nuclear cataract of 2.4 (95% CI 1.2 to 5.0) compared to those whose birth weight was under 6 lb 12 oz.


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  		Table 2. Odds Ratios (95% CI) for Nuclear Opalescent Cataract According to Thirds of the Distribution of Early Life Variables

 
There were similar associations between nuclear cataract and other indicators of increased fetal growth, although only the trends between abdominal circumference and nuclear opalescent cataract (Table 2) and length and nuclear color were statistically significant (data not shown). To check the consistency of our findings we also carried out a multiple linear regression analysis using the raw LOCS III score for nuclear opalescent cataract as the dependent variable and birth weight as the independent variable. There was a positive association between the two variables ß = 0.06 (95% CI 0.0 to 0.13) per SD increase in birth weight (P = 0.06) after controlling for the effects of age, sex, gestation, smoking, alcohol consumption, myopia, social class, and plasma concentration of alpha carotene. This finding, though not quite significant at the 5% level, is consistent with the previous analysis. We could not check the consistency of our results for cortical or posterior subcapsular cataract in the same way, because their LOCS III scores were highly skewed from normal and were not amenable to transformation.

The risk of cortical cataract fell slightly with increasing birth weight (Table 3) , but the trend was nonsignificant. The odds ratio for cortical cataract for those whose birth weight was over 8 lb was 0.6 (95% CI 0.3 to 1.1) compared with participants whose birth weight was under 6 lb 12oz. After adjustment for gestation and other risk factors however, the trend became very weak. Men and women born before 37 weeks gestation were at increased risk. The odds ratio for cortical cataract among subjects born before 37 weeks was 2.0 (95% CI 1.0 to 4.2) compared with those born at term. However, in a multiple logistic regression analysis with birth weight and gestational age as independent variables, neither birth weight nor gestation remained significant predictors of cortical cataract. None of the early-life measurements appeared to show any trend or association with risk of posterior subcapsular cataract (Table 4) .


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  		Table 3. Odds Ratios (95% CI) for Cortical Cataract According to Thirds of the Distribution of Early Life Variables

 

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  		Table 4. Odds Ratios (95% CI) for Posterior Subcapsular Cataract According to Thirds of the Distribution of Early Life Variables

 
At least one type of cataract (nuclear, cortical, or posterior subcapsular) or cataract surgery was present in either eye of 198 (51.8%) out of 382 subjects. (Also, 10 subjects were excluded because they had non-age–related cataract). In a final series of logistic regression analyses (data not shown), we examined whether parameters of early growth were associated with the presence of at least one type of age-related cataract. We found no associations between any of the parameters of size at birth and subjects who had at least one type of cataract or cataract surgery, either when controlling for the effects of age and sex alone, or when also including age, sex, gestation, and other risk factors for cataract in the model.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
In this group of men and women ages 66 to 75, we have shown a relationship between indicators of early growth and age-related cataract. The pattern of early growth associated with cataract differed, however, according to the type of cataract. In the case of nuclear cataract, the risk of opacity was related to indicators of increased rather than decreased growth. Cortical cataract by contrast was associated with markers of decreased intrauterine growth, although none of these trends were statistically significant. Posterior subcapsular cataract was not related to any marker of early growth. The small number of subjects with this type of opacity limits the statistical power of our study to detect any association between this type of cataract and size at birth.

In this study, we have used the LOCS III technique to evaluate the prevalence of cataract. It has been validated21 and is widely used in clinical and epidemiologic surveys.24 25 The prevalences of the different types of cataract accord with previous surveys; for example, in the Chesapeake Bay study of men ages 60 to 69, the prevalence of nuclear cataract was 33%,26 close to our estimate of 28%. Furthermore, the relationships we found between cataract and other risk factors were consistent with the results of other studies. These included age and gender,27 28 social class,29 cigarette smoking,30 myopia,31 steroid use,30 32 lower levels of antioxidants,30 and diabetes.30 33 34 The finding of an apparently protective effect of alcohol (Table 1) has also been described elsewhere. The Beaver Dam Eye Study8 showed that moderate alcohol consumption was associated with decreased risk of nuclear cataract. A number of recognized or suspected risk factors for cataract including sunlight exposure, childhood nutritional deficiencies, and severe diarrheal illness were not recorded in our study. As these are unlikely to be related to size at birth, we do not think they are a likely cause of confounding. We did, however, have data for 388 subjects on social class at birth (as determined by father’s occupation), which may act as proxy for childhood nutrition. We found that social class at birth was not independently related to risk of any type of cataract. However, the association we found between higher birth weight and increased risk of nuclear cataract was strengthened after controlling for social class at birth and other risk factors for nuclear cataract. The odds ratios for risk of nuclear cataract for the middle and upper thirds of birth weight were 2.7 (95% CI 1.3 to 5.4) and 3.1 (95% CI 1.4 to 6.5) respectively compared with the lowest third (P for trend = 0.004).

Our results differ from the only previous study that has addressed the issue of the effect of early growth on risk of age-related cataract. Evans and colleagues surveyed 717 residents of North Hertfordshire, ages 64 to 74 years, whose birth weight had been measured by an attending midwife.19 In contrast to our study, they found no association between birth weight and any type of age-related cataract. In this study, however, there was no data on other measurements of fetal growth, and the gestational age of the infants was not known.

Our study was based on 392 participants who agreed to attend the hospital clinic—53% of the 741 people we invited to take part in the study. The people in our study were not a representative sample of all people born in Sheffield at the time because they were born in hospital at a time when most births took place at home, and because they continued to live in the city in which they were born. However, in the statistical analysis, all comparisons were made within the group who participated. Selection bias could explain our findings either if subjects with higher birth weight and cataract were more likely to take part, or if subjects with lower birth weight and cataract were less likely to take part or were excluded from the study. We explored this possibility by comparing the mean (SD) birth weight of the 372 subjects included in the analysis with that of various groups of subjects who were not included. We found the mean (SD) birth weight of the 372 subjects included in the analysis–7.3 (1.3)lb—did not differ significantly from that of the 20 subjects excluded from the analysis because of bilateral cataract surgery or non-age–related cataract—7.5 (1.1)lb; t = 0.6, P = 0.6. Furthermore, the mean did not differ significantly from the mean (SD) birth weight of the 348 subjects selected but who did not participate in the study—7.3 (1.4) lb; t = 0.5, P = 0.6. We found the mean (SD) birth weight of the 4793 individuals in the entire sampling frame minus the 372 included in the analysis—7.2 (1.2) lb–was slightly below that of those included in the analysis but this difference was not statistically significant (t = 1.78, P = 0.08). Therefore, we do not think that nonresponse or our ability to follow up all members of the original cohort will have resulted in bias sufficient to cause a substantive change in the relationship between birth weight and later risk of cataract.

Because small size at birth is associated with impaired glucose tolerance,35 and accelerated aging,36 which are both known to be risk factors for cataract, we had hypothesized that the commonest type of cataract, nuclear cataract, would be associated with low birth weight. Rather, we found that nuclear cataract was associated with high birth weight. It was also associated with other indices of increased fetal growth (Table 2) . Although most studies show that reduced, rather than increased, growth in utero has a detrimental effect on health in later life,37 several have shown a U-shaped relation or association with increased growth in utero. For example, mortality from coronary heart disease was associated with both low and high abdominal circumference at birth;38 risk of type II diabetes was increased in both low and high birth weight infants;39 and polycystic ovaries were associated with high birth weight and prolonged gestation.40 We have previously suggested that the physiological basis for these associations is that they represent the long-term effects of maternal hyperglycemia and fetal macrosomia.38 We speculate that the same processes may impair the laying down of lens crystallin protein during lens development.

Cortical cataract (LOCS III C >= 2.0) was present in at least one eye of 27% of study participants. This is consistent with previously published figures for the prevalence for cortical cataract, for example in the Watermen study,26 approximately 25% of eyes had some evidence of cortical opacity at the age of 70. In contrast to nuclear cataract, we found a nonsignificant trend for decreased odds of cortical cataract with increasing birth weight. The trend weakened, however, after adjustment for gestation and risk factors for cortical cataract suggesting either that there is no association between cortical cataract and size at birth, or else a modest effect is present that this study is too small to detect.

The positive association between fetal growth and increased risk of nuclear cataract is unexpected and may be simply a chance finding. On the other hand, as the synthesis of lens crystallins commences during early life, it may indicate that risk of developing this type of cataract is at least partly determined by events occurring before birth.


   Acknowledgements
 
The authors thank the participants for their time, Sheila Walton and Liz Kelleher who did the fieldwork, and Vanessa Cox for data processing.


   Footnotes
 
Supported by grants from the Wellcome Trust and the Medical Research Council, London, United Kingdom.

Submitted for publication July 6, 2000; revised October 25, 2000; accepted November 3, 2000.

Commercial relationships policy: N.

Corresponding author: Nigel F. Hall, MRC Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Tremona Road, Southampton, Hampshire SO16 6YD, UK. nfh{at}mrc.soton.ac.uk


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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