Smoking Cessation and Risk of Cataract Extraction among US Women and Men

June M. Weintraub1,2, Walter C. Willett1,,3, Bernard Rosner2,4, Graham A. Colditz1,2, Johanna M. Seddon1,5 and Susan E. Hankinson1,2

1 Department of Epidemiology, Harvard School of Public Health, Boston, MA.
2 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA.
3 Department of Nutrition, Harvard School of Public Health, Boston, MA.
4 Department of Biostatistics, Harvard School of Public Health, Boston, MA.
5 Department of Ophthalmology, Harvard Medical School, and the Massachusetts Eye and Ear Infirmary, Boston, MA.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although the observational evidence linking cigarette smoking with risk of senile cataract is well-established, it is unclear whether any benefit is obtained from quitting smoking. Therefore, in this study, the authors examined the association between time since quitting smoking and incidence of cataract extraction in women and men enrolled in the Nurses' Health Study and the Health Professionals Follow-up Study, respectively. There were 4,281 incident physician-confirmed cases of cataract and 1,038,493 accumulated person-years of follow-up. Compared with current smokers, former smokers who had quit smoking 25 or more years previously had a 20% lower risk of cataract extraction after adjustment for age, average number of cigarettes smoked per day, and other potential risk factors (relative risk (RR) = 0.80, 95% confidence interval (CI): 0.71, 0.91). However, risk among past smokers did not decrease to the level seen among never smokers (for never smokers, RR = 0.64, 95% CI: 0.52, 0.79). The observed relation was similar when data were examined by cataract subtype (>25 years since quitting vs. current smoking: primarily nuclear cataract, RR = 0.82, 95% CI: 0.68, 0.97; primarily posterior subcapsular cataract, RR = 0.90, 95% CI: 0.71, 1.13). These findings suggest that any healing from damage due to cigarette smoking occurs at a very modest pace, and they emphasize the importance of never starting to smoke or quitting early in life.

cataract; smoking; smoking cessation

Abbreviations: CI, confidence interval; PSC, posterior subcapsular


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cataract is the leading cause of blindness worldwide (1Go). While loss of vision due to cataract is correctable by surgery, this procedure is expensive and is not readily available in less developed countries. Cataract extraction is the most common therapeutic surgical procedure performed on elderly Americans (2Go, 3Go). Preventing cataract or delaying progression to visual disability carries the potential for significant benefits, saving money and resources in places where surgical procedures are available and improving the health and well-being of the elderly regardless of access to surgery.

Oxidative damage plays a major role in cataractogenesis, and cigarette smoking is believed to confer increased risk of cataract, at least in part, through this mechanism (4GoGoGoGo–8Go). The observational evidence linking cigarette smoking with risk of cataract is well-established; heavy smokers have up to three times the risk of nuclear, posterior subcapsular (PSC), and mixed opacities as nonsmokers (9GoGoGoGo–13Go).

There is some evidence that former smokers have a reduced risk of cataract compared with current smokers (9Go, 13Go, 14Go). However, the association is unclear, and the differences between past smokers and current smokers have not been examined according to cataract subtype. Therefore, we examined prospectively the association between time since quitting smoking and incidence of cataract extraction among participants in the Nurses' Health Study and the Health Professionals Follow-up Study.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Nurses' Health Study began in 1976 when 121,700 US female registered nurses aged 30–55 years residing in 11 states returned a mailed questionnaire on potential risk factors for cancer and cardiovascular disease (15Go). Information on lifestyle factors and disease has been updated every 2 years since 1976. The Health Professionals Follow-up Study is a prospective study of 51,529 US male health professionals from all 50 states who were aged 40–75 years in 1986 (16Go). The study population consists of 29,683 dentists, 3,743 optometrists, 2,218 osteopathic physicians, 4,185 pharmacists, 1,600 podiatrists, and 10,098 veterinarians. The men are also followed by means of mailed questionnaires every 2 years.

Smoking history
In both of the above cohorts, smoking status was assessed at baseline and is updated on each subsequent questionnaire. In the Nurses' Health Study, no minimum number of cigarettes smoked was required to establish smoking status; in the Health Professionals Follow-up Study, smokers were defined as men who had smoked 20 or more packs of cigarettes in their lifetime. Smoking status was characterized as never, past, or current, with current smokers being further subdivided into categories of average number of cigarettes smoked daily. In the Nurses' Health Study, the initial questionnaire in 1976 determined age at starting to smoke, initial amount smoked, age upon quitting and quantity last smoked for former smokers, and quantity currently smoked for current smokers. In the Health Professionals Follow-up Study, the initial questionnaire in 1986 determined smoking status, time since quitting for former smokers (classified into five categories: <1, 1–2, 3–5, 6–9, and >=10 years), and quantity smoked in the past, classified into average number of cigarettes smoked per day during 10-year age periods. Time since quitting for the 15,175 past smokers who had quit more than 10 years before baseline was imputed by subtracting the median value of the last age category in which the participant indicated smoking from his age in 1986.

Former smokers in both cohorts were classified as having stopped 0–4.9, 5–14.9, 15–24.9, or >=25 years previously. Ever smokers were classified as having smoked, on average, 1–14, 15–24, 25–34, 35–44, or >=45 cigarettes per day. Cumulative dose was calculated in pack-years of smoking by multiplying the number of packs smoked per day (a pack contains 20 cigarettes) by the number of years in which that amount was smoked; pack-years were classified in five categories: <10, 10–24.9, 25–44.9, 45–64.9, and >=65 pack-years.

Other exposure variables
From the baseline questionnaires, we obtained information on age, body weight, height, diagnosis of diabetes mellitus, alcohol intake, physical activity, number of visits with a doctor in the past year, and newly diagnosed medical conditions. The Health Professionals Follow-up Study questionnaire also asked about pipe and cigar smoking. In the Nurses' Health Study, dietary intake, including use of nutritional supplements and alcohol intake, was assessed by semiquantitative food frequency questionnaire in 1980, 1984, 1986, 1990, and 1994; in the Health Professionals Follow-up Study, a similar food frequency questionnaire was completed in 1986 at baseline and again in 1990 and 1994. For the Nurses' Health Study, we averaged nutrient intakes from the 1980 and 1984 questionnaires, and for the Health Professionals Follow-up Study, we used baseline values.

Population for analysis
In this study of senile cataract, we restricted the baseline population to women and men who were older than age 45 years at baseline. Those too young for our study at baseline were entered into the analysis in the 2-year cycle after they reached the age of 45. We also excluded persons who did not complete a baseline food frequency questionnaire and those who had implausible caloric intakes (<500 or >3,500 kcal/day for women and <800 or >4,200 kcal/day for men) or who left more than 70 items blank on the food frequency questionnaire.

The analysis included 16 years of follow-up for the women and 10 years of follow-up for the men. For the women, we selected 1980 as the baseline year, because this was the first year in which diet was assessed (n = 92,468). For the men, a total of 49,933 had eligible data obtained from food frequency questionnaires in 1986. We excluded from the analysis all participants diagnosed as having cataract (n = 2,407) or cancer (except nonmelanoma skin cancer) (n = 5,565) at baseline. We also excluded those for whom we had no information on smoking status at baseline and intermittent smokers (those who stopped and started smoking again during the study) (n = 9,739). This left a total of 81,778 women and 42,912 men available for follow-up.

Outcome
Starting in 1984 for the Nurses' Health Study and in 1988 for the Health Professionals Follow-up Study, participants were asked whether they had had a cataract extraction; if so, they were asked for permission to review their medical records. We then contacted the ophthalmologist who had performed the surgery and, when available, the patient's optometrist or another health care provider who had ophthalmologic records, to confirm the dates of initial diagnosis and extraction and to determine any known cause of the cataract. From the records, we obtained the participant's best corrected visual acuity in both eyes prior to surgery and the location of the lens opacity in each eye. Ninety percent of the ophthalmologists contacted responded to the questionnaire, and all confirmed the extraction. Because 86 percent of the confirmed dates of extraction were within 6 months of the participants' reports, we also included 538 cases confirmed on a supplementary questionnaire by the participant but for whom we had no information from the eye doctor. This resulted in a total of 5,387 confirmed cases.

We excluded cataracts considered by the physician to be either congenital or secondary to chronic steroid use, chronic intraocular inflammation, ocular trauma, previous intraocular surgery, or glaucoma (n = 505). These cases accrued person-time up to the date on which the cataract was initially diagnosed, determined as the earlier of the dates indicated by the participant and the ophthalmologist. We also excluded patients who developed cancer before cataract diagnosis; these individuals accrued person-time up to the date of cancer diagnosis and were not counted as cases (n = 204). Finally, we excluded those for whom no date of diagnosis was available (n = 310) and those whose cataracts were diagnosed prior to age 45 years (n = 87). A total of 3,103 cataract cases in the women and 1,178 cases in the men were included in the analysis.

Opacities in different areas of the lens (nuclear, PSC, or cortical) may have differing etiologies (17GoGo–19Go). For those participants whose ophthalmologist indicated a subtype, we were able to identify persons with only one subtype, those with primarily one subtype, and those in whom a subtype was present but was not necessarily the primary type. The principal analysis was based on the "any cataract" group; however, we also assessed two other case definitions: 1) primarily nuclear cataract, in either eye (if unilateral) or in both eyes (if bilateral), as determined by the participant's eye doctor (n = 2,076); and 2) primarily PSC cataract (n = 1,249). We did not examine the cortical cataract subtype, because while cortical cataracts are common, they do not typically result in disabling impairment of vision, and this type of cataract was underrepresented in our extraction cases (n = 384).

Data analysis
Each participant's follow-up time began with the date of return of the 1980 questionnaire (for women) or the 1986 questionnaire (for men), or the point at which the participant reached age 45, whichever was later. Since ophthalmologists are increasingly likely to recommend smoking cessation after diagnosis of cataract but prior to extraction, we used the date of diagnosis as the end of follow-up for cases of cataract extraction. Because participants who do not have eye examinations may be less likely to have cataracts diagnosed, data were not contributed to the analysis in a given 2-year interval if a participant did not report having an eye examination during that period, as reported on the 1990, 1992, 1994, and 1996 questionnaires (this exclusion was not applied prior to 1990). We also censored participants with cancer at the time of their diagnosis, to avoid any possible bias due to changes in both smoking behavior and risk of cataract extraction related to the illness. Thus, follow-up was continued until cataract diagnosis, death, cancer diagnosis, loss to follow-up, or end of follow-up (June 1996 for the women and January 1996 for the men), whichever came first. This gave us a total of 1,038,493 person-years of follow-up.

We used incidence rates with person-years of follow-up as the denominator. For each participant, person-months were allocated according to the baseline exposure and then updated according to information on subsequent 2-year follow-up questionnaires.

Relative risks were calculated as the rate of occurrence of cataract extraction in each smoking category, divided by the corresponding rate in the reference category. For analyses evaluating the impact of time since quitting smoking on disease risk, we followed the recommendations of the 1990 Surgeon General's report and used current smokers as the reference category (20Go). All relative risks were adjusted for age (in 5-year intervals), and 95 percent confidence intervals were calculated. We used pooled logistic regression analysis with 2-year time increments, which is asymptotically equivalent to Cox regression with time-dependent covariates, to control for age and other risk factors simultaneously (21Go). Trends were assessed by modeling categorical variables as ordinal variables in multivariate models.

Former smokers tend to have smoked fewer cigarettes per day before quitting and to have started smoking at an older age than persons who continue to smoke (22Go). To avoid bias, we adjusted the relative risks among former and current smokers by the moving average of the number of cigarettes consumed daily, updated with information from each questionnaire until the time of quitting or the end of follow-up; for former smokers at baseline, we used the amount last smoked as indicated on the initial questionnaire. Duration of smoking was not included as a variable in these analyses, because at the same cumulative dose of smoking (e.g., pack-years), a former smoker will always have either smoked more cigarettes per day than a current smoker or started smoking at a younger age. Furthermore, former smokers who are the same age, have the same number of pack-years, and have the same number of years since quitting can have vastly different combinations of duration and dose in cigarettes per day. These differences are not captured by adjusting for pack-years in the analysis, whereas by adjusting for average dose, one can validly assess the independent effect of time since quitting, adjusted for smoking dose.

To present a meaningful measure of association for never smokers with which to compare the relative risks for time since quitting, we report relative risks from multivariate models comparing current and never smokers only, with mean-centered adjustment for number of cigarettes smoked daily.

We conducted separate analyses for each cohort and then pooled the two study groups. Tests for heterogeneity between the two study groups were conducted, and meta-analytical methods using a random-effects model were employed to pool the relative risks (23Go). We used the polyt-omous logistic regression model to evaluate differences in risk factors by cataract type. We computed the Lagrange multiplier test statistic as a measure of the differences between type-specific coefficients (24Go, 25Go).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Increased risk in smokers
At baseline, there were 46,293 women and 31,456 men over age 45 years in the analysis. A total of 78,549 women and 39,182 men were included in the analysis. In 1980, 28 percent of the women were current smokers, 27 percent were former smokers, and 45 percent had never smoked. By 1994, 14 percent were current smokers and 42 percent were former smokers. Among the men, in 1986, 9 percent were current smokers, 45 percent were former smokers, and 46 percent had never smoked; in 1994, 5 percent were current smokers and 43 percent were former smokers. Other baseline characteristics are provided in table 1.


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TABLE 1. Age-adjusted* prevalences of risk factors for cataract extraction at baseline (1980 for the Nurses' Health Study and 1986 for the Health Professionals Follow-up Study), by smoking status, in the Nurses' Health Study and Health Professionals Follow-up Study cohorts

 
We considered the following potential confounders in multivariate models: body mass index (weight (kg)/height (m)2) (continuous variable, updated), diabetes (yes/no, updated), energy-adjusted lutein/zeaxanthin intake (in quintiles), state of residence at baseline, and pipe and cigar smoking (for men only). The associations of cigarette smoking status and time since quitting with cataract extraction changed only slightly after we controlled for these confounders. In other models, we evaluated age at starting to smoke, estrogen use (for women), aspirin use, vitamin C intake, intake of other antioxidants (including and not including supplement use), physical activity, race (for men), profession (for men), and alcohol consumption together and separately in multivariate models; however, these variables were not found to be confounders and were not included in the final models.

Smoking was associated with risk of cataract extraction for all types of cataract combined, as well as for primarily nuclear and PSC subtypes. In analyses of cumulative exposure to smoking using pack-years (table 2), the pooled multivariate relative risk of any type of cataract extraction was 1.78 (95 percent confidence interval (CI): 1.58, 2.00) among men and women with 65 or more pack-years as compared with never smokers. In the subtype analysis, the relative risks for 65 or more pack-years of smoking were 1.84 (95 percent CI: 1.56, 2.17) and 2.20 (95 percent CI: 1.73, 2.79) for primarily nuclear opacities and primarily PSC opacities, respectively.


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TABLE 2. Relative risk of cataract extraction by total number of pack-years of cigarette smoking in the Nurses' Health Study and Health Professionals Follow-up Study cohorts, 1980–1996 and 1986–1996

 
When we stratified the data by smoking status and dose, there was an indication that past heavy smokers (>=15 cigarettes/day) had a lower risk of any cataract extraction than current heavy smokers, but the risk for past light smokers (averaging 1–14 cigarettes/day) was not different from that for current light smokers (table 3). The pooled multivariate relative risks for all extractions combined were 1.33 and 1.53 for past and current smokers of 15 or more cigarettes per day, respectively. Past and current light smokers did not have a significantly increased risk compared with never smokers (table 3). Similar results were seen for primarily nuclear and primarily PSC subtypes.


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TABLE 3. Relative risk of cataract extraction by smoking status in the Nurses' Health Study and Health Professionals Follow-up Study cohorts, 1980–1996 and 1986–1996

 
Decrease in risk among former smokers
The risk among former smokers decreased with number of years since quitting, but not to the level of never smokers, even 25 or more years after cessation (table 4). In comparison with current smokers, the pooled multivariate relative risk for any type of cataract extraction among those who had quit smoking more than 25 years previously was 0.80 (95 percent CI: 0.71, 0.91). Results were similar in both cohorts (p value for heterogeneity = 0.88). Among women, the multivariate relative risk of all extractions combined for former smokers who had quit more than 25 years previously (as compared with current smokers) was 0.78 (95 percent CI: 0.68, 0.91), while never smokers had a relative risk of 0.62 (95 percent CI: 0.49, 0.78). Among men, the decrease in risk was less apparent, with a multivariate relative risk of 0.86 (95 percent CI: 0.68, 1.10) for those who had quit 25 or more years previously (as compared with current smokers), while never smokers had a relative risk of 0.74 (95 percent CI: 0.46, 1.19). Similar results were seen for primarily nuclear and primarily PSC subtypes.


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TABLE 4. Relative risk of cataract extraction by time since quitting smoking in the Nurses' Health Study and Health Professionals Follow-up Study cohorts, 1980–1996 and 1986–1996

 
When we examined the association between risk of cataract extraction and time since quitting smoking by cataract subtype using polytomous regression, there were no significant differences by subtype (e.g., in the Nurses' Health Study, the most pronounced difference between Lagrange statistics was 1.00; this difference was distributed as {chi}2 with 1 df, p = 0.32).

We also assessed the relation of time since quitting to risk of cataract extraction within categories of amount smoked per day. Among those participants who smoked an average of 15 or more cigarettes per day, we found risk of all extractions combined to be reduced by 21 percent (pooled multivariate relative risk = 0.79, 95 percent CI: 0.63, 1.01; p value for heterogeneity = 0.16) for those who had quit 25 or more years previously in comparison with current smokers of more than 15 cigarettes per day. Compared with current smokers of less than 15 cigarettes per day, former smokers of the same average level who had quit more than 25 years previously had a nonsignificant 8 percent decreased risk (pooled multivariate relative risk = 0.92, 95 percent CI: 0.63, 1.35; p for heterogeneity = 0.15). However, this apparent interaction was not statistically significant in either cohort (for interaction, p = 0.13 in women and p = 0.79 in men).

Finally, we analyzed the effects of smoking patterns at different ages in the men. (We did not have sufficient variation in patterns to perform this assessment among women.) In this analysis, the referent group was men who had been heavy smokers (>15 cigarettes/day) throughout life; we stratified the data by age and pack-years, thus allowing for comparison of individuals who had the same cumulative exposure but different exposure patterns. Compared with always having been a heavy smoker, the relative risk for heavy smoking before age 40 and light smoking after age 40 was 0.82 (95 percent CI: 0.60, 1.12), and the relative risk for light smoking before age 40 and heavy smoking after age 40 was 1.08 (95 percent CI: 0.80, 1.46).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In these two large prospective studies, we observed a modest inverse association between time since quitting smoking and extraction of cataracts. Compared with persons who never stopped smoking, women and men who had quit smoking 25 or more years previously had a 20 percent lower risk of cataract extraction after adjustment for potential confounders, while those who had never smoked had a 36 percent lower risk compared with current smokers.

In our first assessment of these relations, past smokers who had smoked more than 35 cigarettes per day were at increased risk of cataract extraction compared with never smokers, but no significant differences were found for the association between cataract extraction and time since quitting (13Go). Since that time, the number of cataract cases eligible for study has more than tripled, enabling us to obtain a more precise assessment of the time course of the benefit of smoking cessation. In a cross-sectional study of 838 watermen, West et al. (9Go) found that 10 years after quitting smoking, past smokers had 0.67 times the risk of nuclear opacities as current smokers (95 percent CI: 0.49, 0.92); in a prospective study of 17,824 male physicians, Christen et al. (14Go) found that 20 or more years after quitting smoking, the relative risk of cataract extraction was 0.73 times that of current smokers (95 percent CI: 0.59, 0.85), with never smokers having 0.66 times the risk of current smokers (95 percent CI: 0.54, 0.79).

Smoking is thought to increase risk of cataract, at least in part, by increasing oxidative stress in the lens. Oxidative stress can be caused by free radicals produced by reactions in the presence of tobacco smoke or other air pollutants; these free radicals may directly damage lens proteins and the fiber cell membrane in the lens. Intake of certain antioxidants has been shown to decrease cataract in a number of studies, including our own (26GoGoGo–29Go). Smoking cessation may interrupt or slow the progression of the cataract by removing oxidative stress or improving antioxidant activity, or by allowing recovery from damage that has already occurred. To assess the possibility of a healing process, we analyzed the effects of heavy smoking at different ages in the men. At the same cumulative exposure, men who had been heavy smokers earlier in life appeared to be at a nonsignificantly lower risk than men who had been light smokers earlier in life (the relative risk was 0.82 for heavy smoking before age 40 vs. 1.08 for light smoking before age 40), which could indicate that those who had smoked heavily earlier in life may have experienced some recovery. These results, combined with the finding that risk of cataract extraction among past smokers does not decrease to the level of never smokers even after >25 years since quitting, suggest that any healing which occurs does so at a very modest pace.

Although we excluded approximately 5 percent of the study population because they indicated that they had stopped smoking and started smoking again during follow-up, an unknown number of failed quitters are likely to have been improperly included in the past-smoking category, especially in the early years after quitting. Time since quitting was probably somewhat overestimated for most smokers, which could have attenuated the protective relation we observed. Some current smokers who quit just after being diagnosed may have been misclassified as quitters. These sources of misclassification may explain why we found an increased risk in the Health Professionals Follow-up Study among men who had quit 5 or fewer years previously. The longer follow-up in the Nurses' Health Study probably dampened the effects of such misclassification, and we did not see significantly increased risk among the women who were short-term quitters.

We did not find significant differences between subtypes for the protective effects of time since quitting. Cataract subtype was not assessed in a standard manner, and documentation in medical records may be imperfect; therefore, some cases were probably misclassified by specific type, thus tending to bias type-specific relative risks toward the average effect seen with all cases combined. Consistently with the literature (30GoGo–32Go), we did find differences between the risk of diabetes associated with the primarily PSC subtype and that associated with all other types, which suggests that the cases were reasonably well classified (e.g., for diabetes, the relative risk for primarily PSC opacities was 3.09 and the relative risk for any other type was 1.56; difference between Lagrange statistics with 1 df = 27.855, p < 0.001).

The use of cataract extraction as the endpoint in this study ensured that there would be little misclassification of noncases as cases. In this prospective analysis, underascertainment of cases would not have biased the ratio measures of effect as long as the underascertainment was not differential with respect to exposure (33Go).

Defining the endpoint as cataract extraction rather than cataract diagnosis also decreases the chance of variation in the threshold for diagnosis of disease. Diagnosis of cataracts and progression of cataracts are both determinants of the incidence of cataract extraction. Patients with fee-for-service insurance plans have higher rates of cataract extraction than patients using prepaid plans, and because Medicare covers extractions performed after age 65, it is possible that some extractions would not be performed until the patient reached that age (34Go). Because all of our participants were health professionals, access to medical care was less variable than in the general population. In addition, any differences in health-care-seeking behavior would not have biased our results unless this also varied by smoking status. We assessed the Spearman correlation between time since quitting and visual acuity before surgery in the eye being operated on as a measure of disease severity, and these correlations ranged from –0.04 to 0.05. In secondary analyses, we restricted the baseline population to all persons who had at least one eye examination during the follow-up period, and this did not materially change our results.

Data on exposure were collected before diagnosis; any misclassification would have biased our results toward the null. We used date of diagnosis as our endpoint in order to minimize bias that could arise if women and men were to quit smoking as a result of being diagnosed with cataract. The high follow-up rates in these cohorts (more than 97 percent of total person-time) minimized loss to follow-up as a source of bias. We controlled for several known risk factors for cataract extraction; however, the effect of confounding by unmeasured risk factors may have distorted the associations seen for time since quitting smoking.

These data emphasize the importance of reducing the initiation of smoking in order to prevent risk of cataract extraction. Our finding that the excess risk of cataract extraction persists after quitting smoking and only moderately decreases with years since quitting provides further support for the hypothesis that smoking causes irreversible damage to the lens.


    ACKNOWLEDGMENTS
 
This study was supported by grants CA40356, T32 ES07069, EY09611, and EY12269 from the National Institutes of Health.


    NOTES
 
Reprint requests to Dr. June M. Weintraub, Channing Laboratory, 3rd Floor, 181 Longwood Avenue, Boston, MA 02115 (e-mail: June.Weintraub{at}channing.harvard.edu).


    REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication November 29, 2000. Accepted for publication July 9, 2001.