Cigarette Smoking and Incidence of Chronic Bronchitis and Asthma in Women*

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1 Cigarette Smoking and ncidence of Chronic Bronchitis and Asthma in Women* Rebecca]. Troisi, SeD; Frank E. Speizer, MD, FCCP; Bernard Rosner, PhD; Dimitrios Trichopoulos, MD; and Walter C. Willett, MD Study objective: To examine the relation of smoking habits and development of asthma in a large cohort of US women. Design: Prospective cohort study. Participants: Among 7 4,072 women, 34 to 68 years of age, who were free of major diseases, we documented 671 incident asthma cases and 798 incident cases of chronic bronchitis during 10 years of follow-up. Methods: Age-adjusted relative risk estimates for smoking categories were calculated separately for chronic bronchitis and asthma. Results: Risk of chronic bronchitis was significantly higher in current smokers than in never smokers (relative risk [RR]=2.85; 95% confidence interval [C]=2.45 to 3.32) and increased with the number of cigarettes smoked per day (p for trend <0.0001). Approximately 5 years after quitting, chronic bronchitis risk in past smokers approached that in never smokers. n contrast, current smokers were at significantly lower risk for asthma than women who never smoked (RR=0.57; 95% Cl=0.46 to 0.71) and women who quit (RR=0.50; 95% C=0.40 to 0.62), possibly because individuals with sensitive airways are less likely to become regular smokers, and smokers who develop respiratory symptoms of any etiology tend to quit. Asthma risk in past smokers initially increased compared with that in never smokers, possibly because of quitting prior to diagnosis in response to symptoms of any etiology, but decreased with time since quitting (p for trend=0.007); within approximately 5 years, the risk did not differ between past and never smokers. Conclusion: These data suggest that smoking in adults may not be an independent cause of asthma but could exacerbate or be perceived as exacerbating asthma symptoms in susceptible individuals. (CHEST 1995; 108: ) Cl=confidence interval; NHS=Nurses' Health Study; RR=relative risk Key words: asthma; chronic bronchitis; cigarette smoking ~ t h othe u relation g h of cigarette smoking to increased risk of chronic bronchitis is well established,1 less is known about the role that smoking plays in the development of adult-onset asthma. Studies attempting to assess this association have reported either no relation 2 -.S or a relatively modest increase in tisk of asthma among smokers 6-8 compared with nonsmokers. Most of these studies have had limited statistical power and minimal information on smoking habits. More important, understanding the relation of smoking and asthma has been limited by several potential biases. First, individuals with sensitive airways or allergies, who are at higher risk of developing asthma, may be less likely to become regular smokers than individuals whose tolerance in terms of airway sensitivity is greater. This self-selection may cause smokers to appear at *From the Channing; Laboratory, Depmtment of Medicine, Harvard Medical Schoo1 and Brigham ana Women's Hospital, <md the De_partments of Epidemiology and Nutrition, Harvard School of Pu5lic Health, Boston, and fue National Cancer nstitute, Environmental Epidemiology Branch, Bethesda, Md. Supported by research grant CA from the National nstitutes of Health. Ms. Troisi was supported by nstitutional Research Award No. HL Manuscript received March 1, 199.5; revision accepted July 17. Reprint requests: Dr. Speizer, Channing Laboratory, 80 Longu;ood Avenue, Boston, MA lower risk of asthma than never smokers. Second, smokers experiencing respiratory symptoms or chronic respiratory infections may be more likely to quit smoking before being diagnosed as having asthma, which would cause a temporary increase in the risk of asthma among former smokers relative to continuing smokers. Furthermore, if smokers primarily quit because of early asthma symptoms, then continuing smokers would make up a survival population at lower risk of asthma. Finally, Fletcher and Pride 9 found that smokers presenting with respiratory symptoms were more likely to be labeled with chronic bronchitis than with asthma. 9 These biases would result in an underestimation of the association of current smolcing and asthma risk. Using the extensive information on smoking habits available from the Nurses' Health Study (NHS ), a large prospective cohmt study of US women, we examine the relationship between smoking and new-onset chronic bronchitis and asthma. The NHS Coh011 M ETHODS The NHS, a prospective investigation of major diseases in women, was initiated in This study has been described in CHEST / 108 / 6/DECEMBER,

2 Table!-ncidence of Asthma and Chronic Bronchitis by Smoking Status and Age: NHS, 1980 to 1990 Age, yr, at Never Smokers No. of Cases Diagnosis P-T* Asthma Bronchitis P-T* , , , , , , , , , , , , , , , ,640 Total 321, ,504 *P-T ;years of person-time. Current Smokers Past Smokers No. of Cases No. of Cases Asthma Bronchitis P-T* Asthma Bronchitis 1 1 1, , , , , , , l 6 2, , detail elsewhere.l 0 Briefly, 121,700 female registered nurses 30 to 55 years of age in 1976 completed a baseline questionnaire requesting information on their medical history and lifestyle variables. Subsequent questionnaires every 2 years allowed participants to update their exposure information and report the occurrence of major illnesses. A dietary component consisting of a food frequency questionnaire was added to the study in Cigarette Smoking n 1976, current and past smokers were asked about the average number of cigarettes they smoked per day, when they began smoking, and, for past smokers, when they quit smoking. Smoking status and cigarettes smoked per day have been updated on biennial questionnaires. Study Population Only the 93,184 women who completed a food-frequency questionnaire in 1980 were eligible for this analysis because cases of asthma were confirmed only among these participants. Since the outcome for this investigation was newly diagnosed cases of asthma and chronic bronchitis, we excluded from the analysis women who reported a physician's diagnosis of asthma, chronic bronchitis, or emphysema before n addition, women reporting a diagnosis of cancer (except nonmelanoma skin cancer), cardiovascular disease, or diabetes were excluded at baseline and throughout follow-up. Thus, at the beginning of each 2-year interval, the population was essentially healthy. Person-time for women for whom complete information on smoking status was missing was excluded from the analysis (5.0% of total person-time after exclusions). n 1980, 74,072 women entered the analysis for the 1980 to 1982 period. At the beginning of each 2-year interval, women who met the inclusion criteria remained in the analysis. During 10 years of follow-up from the return of the 1980 questionnaire to June 1, 1990, 692,423 person-years accrued among these subjects. Case Definition of Asthma Cases of asthma and chronic bronchitis were based on the nurses' response to the 1988 and 1990 NHS questionnaires about whether they had had physician-diagnosed asthma or chronic bronchitis. We attempted to contact by mail subjects who reported a diagnosis of asthma (but not chronic bronchitis) since 1980 and met the study inclusion criteria. Subjects were asked to complete a supplementary questionnaire eliciting information on date of diagnosis and date of first asthma symptoms, medication use, and seasonality, severity, and precipitators of asthma attacks. Nearly 97% of the nurses responded to the questionnaire. Approximately 86% of the original 1558 diagnoses of those who responded were reproduced on the supplementary questionnaire (9% of the nurses contacted denied a diagnosis of asthma, about 4% reported a diagnosis other than asthma [eg, asthmatic bronchitis], and fewer than 0.5% did not provide sufficient information to confirm their diagnosis). Of the nurses reporting a physician's diagnosis of asthma, only 5.5% reported never taking medication specifically for asthma. For this investigation, asthmatics were defined as nurses who confirmed their NHS questionnaire report of a physician's diagnosis of asthma on the supplementary questionnaire, who did not report a diagnosis of chronic bronchitis, and who reported using asthma medication since diagnosis; 671 subjects met these criteria. Since a separate supplementary questionnaire on chronic bronchitis was not used, cases of chronic bronchitis were based on the 1988 and 1990 NHS questionnaires and included only those women who reported chronic bronchitis but did not report a physician's diagnosis of asthma (n;798). Statistical Analysis Since NHS questionnaires were completed by subjects every 2 years, the person-time for the analysis was treated in 2-year intervals. For each participant remaining free of asthma or chronic bronchitis, follow-up time equal to the number of months between the return of the 1980 questionnaire and the return of the 1982 questionnaire (approximately 24 months) was assigned for each smoking category according to status reported by subjects on the 1980 questionnaire. Similarly, for each 2-year interval, additional months of follow-up were assigned until June 1, 1990 according to status at the beginning of the interval as reported on the questionnaire (unless otherwise noted). For participants who reported a diagnosis of asthma, chronic bronchitis, or who died, follow-up time accumulated until the date of diagnosis reported on the supplementary questionnaire (and on the NHS questionnaire for chronic bronchitis) or the date of death. For participants reporting a diagnosis of cardiovascular disease, cancer, or diabetes, follow-up time accumulated until the beginning of the interval during which the disease was diagnosed. The analysis is based on incidence, with person-months of follow-up as the denominator. We used relative risk (RR) estimates as the measure of association defined as the incidence of asthma and chronic bronchitis among women in various smoking categories divided by the corresponding rate among women in the reference category. Age-specific rates by 5-year age groups were individually calculated and used to compute age-adjusted RR estimates. The Mantel extension test 11 was used for linear trend across ordered smoking categories. RRs were adjusted simultaneously for multiple covariates with use of proportional hazards models Ninety-five Clinical nvestigations

3 6 S f- 4 f T -r _1_..._ >25 < >10 Clgaretteo/day (current smokers) Yeara since quitting (past smokers) -r- -- T - ~ L >25 < >10 Clgarottoo/day (current smoking) Years since quitting (past smokers) F GUU: l. Age-adjustetl HH estimates (95% C) for the relation uf cigarette smoking (cigarettes smoked per day in current smokers and time since quitting in past smokers) and (top) chronic bronchitis and (bottom) asthma, with never smokers as the reference group; NHS, 1980 to percent confidence intervals (Cis) were calculated tor each RR. All p values are two tailed. RESULTS Current smokers accounted for 25% and former smokers 28% of follow-up time, with the remaining time distributed among never smokers. During 10 years of follow-up, we documented 671 cases of newonset asthma and 798 cases of new-onset chronic bronchitis (stratified by smoking status and age in Table 1). Using smoking status at the beginning of each 2-year interval, we found, as expected, the crude incidence of physician's diagnosed chronic bronchitis highest in current smokers (2. 1/1,000 person-years) and lowest in never smokers (0.79/1,000 person-years), with the rate among former smokers intermediate (0.88/1,000 person-years). Adjusting for age made httle difference in the RR estimates. Compared with that in never smokers, the relative risk of chronic bronchitis in smokers increased significantly with increasing number of cigarettes smoked per day (p for trend <0.0001) (Fig 1, top). These results provide evidence that the main study questionnaire vahdly measures chronic bronchitis in this cohort. n women who quit, the risk of chronic bronchitis, while initially greater than in never smokers, approached the level of risk in never smokers after approximately 5 years (Fig 1, top). Former smokers showed an immediate decrease in risk of chronic bronchitis on cessation. To determine whether the amount smoked explained the difference in risk for chronic bronchitis between current and former smokers, analyses restricted to current smokers in 1976 and updated for smoking status (to compare women who quit smoking with women who continued to smoke) were performed with and without adjustment for cigarettes smoked per day in Adjustment for amount smoked in 1976 did not alter the estimates of RR, nor did adjustment for age at which smoking began change the estimates of association. n contrast to the results for chronic bronchitis, the crude incidence of asthma was significantly lower in current smokers (0.59/1,000 person-years) than in never smokers (1.02/1,000 person-years). No relation with cigarettes smoked per day was noted (Fig 1, bottom), and adjustment for age did not change the estimates. To reduce the possibility that current smokers represented a survival population resulting from depletion of prechnical disease as symptomatic smokers quit, the analysis was repeated using smoking status in 1980 without update and 10-year risk of asthma. The RR estimates for current smokers were attenuated shghtly but remained below one compared with those for never smokers. The age-adjusted RR of asthma was 0.80 (95% Cl=0.59 to 1.09) for current smokers of 1 to 14 cigarettes per day, 0.69 (Cl=0.52 to 0.90) for smokers of 15 to 24 cigarettes per day, and 0.78 (C=0.57 to 1.06) for smokers of 25 or more cigarettes per day compared with never smokers. Among women diagnosed as having chronic bronchitis, however, smokers were more hkely than never smokers to receive a subsequent diagnosis of asthma (RR=2.02; C=l.01 to 4.02). A comparison of risk of asthma for past and never smokers yielded results similar to those for chronic bronchitis (Fig 1, bottom). After an initial increase in age-adjusted risk, former smokers were at similar risk of asthma compared with never smokers within 5 years of quitting. Age-specific relative risk estimates for chronic bronchitis show some variation by age (Fig 2, top). n general, risk for current smokers relative to never smokers increased with age. Similarly, for former smokers, risk is elevated relative to never smokers after age 55 CHEST DECEMBER,

4 4r ~ ~ Age O L - ~ ~ Age FGURE 2. Age-specific RR estimates for the relation of cigarette smoking status and (top) chronic bronchitis and (bottom) asthma, with never smokers as the reference group; NHS, 1980 to years. Age-specific RR estimates for asthma (Fig 2, bottom) show a decreased risk among current smokers relative to never smokers that approaches unity with increasing age. Asthma risk among former smokers is similar to never smokers in the younger women (an elevated risk noted for 30 to 34-year-olds is based on only three cases), but appears to increase with increasing age. n previous analyses, we found a positive association of postmenopausal hormone use and an inverse association of dietary vitamin E with risk of asthma. Repeating the original analyses with adjustment for menopausal status, postmenopausal hormone use, and dietary vitamin E did not appreciably change the results. DSCUSSON n this prospective study, current cigarette smokers were at higher risk of chronic bronchitis but at lower risk of asthma than women who never smoked. Risk of both chronic bronchitis and asthma among past smok- ers compared with that among never smokers was initially elevated but decreased with increasing time since quitting smoking. A strong relationship between smoking and chronic bronchitis demonstrated in the heavy smokers (>25 cigarettes per d ~ in? this study agrees with several investigations2.l4j that show rates of chronic bronchitis symptoms in smokers that are four to five times those in nonsmokers, and suggests that the NHS questionnaire validly measures the incidence of chronic bronchitis in this cohort. These data are also consistent with the results of a cross-sectional study 15 that demonstrated, within 5 years of quitting smoking, a prevalence of chronic phlegm among both male and female former smokers similar to that among never smokers. Several studies have assessed the relation of smoking and risk of asthma, 2-8 though only a few have been prospective in design. 6 8 Cumulative incidence of self-reported physician -diagnosed asthma ascertained from the first National Health and Nutrition Examination and the Epidemiologic Follow-up Surveys was similar among ever smokers and never smokers adjusted for age, sex, income, and race (RR=l.l [C=0.9 to 1.5]). 5 n a prospective study conducted in Finland, 4 age-adjusted 6-year risk of physician-diagnosed asthma in women was higher in current smokers (RR=l.29; C=0.69 to 2.40) and lower in former smokers (RR=0.76; C=0.28 to 2.05) than in nonsmokers, although the results were not statistically significant. No association between smoking status and asthma risk was noted in the men. n pooled data from longitudinal studies conducted in Tucson, Ariz, and Cracow, Poland, 8 female smokers 19 to 40 years of age had a lower risk of physician-diagnosed asthma than never smokers of the same age (RR=0.60). However, among women 40 years of age and older, the risk of asthma for smokers was about twice that for nonsmokers. Among men, the results showed a similar pattern, although the RR estimates for asthma were increased over fivefold in men 56 years of age and older. The difference in the relation of smoking and asthma by age cannot explain our results, since most subjects in this study were older than 40 years of age. Separate RR estimates for wheeze and attacks of breathlessness were elevated for smokers of all ages compared with nonsmokers among both men and women. No study that we are aware of has assessed the relation of smoking cessation to risk of asthma. n the present study, current smoking was inversely related to risk of asthma. One possible explanation for this finding is that individuals with sensitive airways or allergies, who may be at higher risk of developing asthma, may be less likely to start smoking than individuals whose tolerance in terms of airway sensitivity is greater. This self-selection would explain why smokers appear at lower risk of asthma than never smokers Clinical nvestigations

5 Continuous smokers were also at lower risk of asthma than women who quit because the latter may represent a subgroup of smokers who are susceptible to the effects of smoking. This apparently lower risk of asthma in smokers may be the result of smokers' quitting in response to respiratory symptoms or respiratory illnesses and subsequently being diagnosed as having asthma while smokers without symptoms continue to smoke, a type of "healthy smoker" effect. Comparing former and never smokers provides additional insight into the smoking-asthma relation. Risk of asthma among former smokers vs never smokers was elevated within the first 2 years of quitting but decreased with increasing time since quitting so that after 5 years, risk in former smokers was similar to risk in never smokers. f smoking actually contributed to the development of asthma, then the decrease in risk associated with increasing time since quitting might be ex1jlained by a leveling off that occurs as the subacute effect of smoking abates. Thus, among individuals susceptible to smoking, over time, quitting smoking is beneficial. This explanation, however, is substantially weakened by the lack of an observed association between current smoking and increased risk of asthma in these data. A more plausible alternative explanation is that smokers who develop symptoms quit because they believe that smoking caused or exacerbates their symptoms and are subsequently diagnosed as having asthma. As time since quitting increases, the residual effects of smoking become less important and with persistent cessation the incidence of asthma in former and never smokers becomes similar. The higher risks for chronic bronchitis associated with current and former smoking at older ages may reflect an effect of duration of smoking. Current smokers of long duration may be at even higher risk of chronic bronchitis compared with never smokers. n addition to quitting in response to symptoms, the higher risk in older past smokers may be explained by irreversible effects on pulmonary function after many years of smoking. Risk of asthma relative to never smokers also increased with age. Current smokers, while at lower asthma risk at younger ages, had a similar risk to never smokers at older ages. This pattern suggests that the lower risk associated with self-selection, as described above, dissipates over time. Past smokers were also at elevated risk relative to never smokers at older ages. This may be explained by greater smoking duration among these subjects. The other possible explanation for the increased risk is that in older women the physiologic response to smoking cessation may mimic asthma symptoms. n conclusion, in this cohort, the number of cigarettes smoked per day was positively related to risk of physician's diagnosed chronic bronchitis. Smoking cessation was associated with a significant decrease in risk for chronic bronchitis; approximately 5 years after quitting, risk in former smokers was similar to that in never smokers. The results for asthma risk are compatible with the notion that those susceptible to adverse effects of smoking are less likely to sustain a smoking habit. The evidence that recent former smokers have a higher risk of being diagnosed as having asthma in contrast to the lack of an excess risk in current smokers suggests that the interactions of smoking and other determinants of asthma risk will need to be further explored. ACKNOWLEDGMENTS: The authors gratefully acknowledge the continuing participation of the nurses in this study and the expert assistance of Barbara Egan and Mark Shneyder. REFEREJ\'CES 1 Fletcher C, Peto R, Tinker C, et al. The natural history of chronic bronchitis and emphysema. Oxford: Oxford University Press, Higgins MW, Keller JB, Metzner HL. Smoking, socioeconomic status, and chronic respiratory disease. Am Rev Respir Dis 1977; 116: Burrows B, Barbee RA, Cline MG, et al. Characteristics of asthma among elderly adults in a sample of the general population. Chest 1991; 100: Vesterinen E, Kaprio J, Koskenvuo M. Prospective study of asthma in relation to smoking habits among 14,729 adults. Thorax 1988; 43: Mc\'lhorter WP, Polis MA, Kaslow RA. Occurrence, predictors, and consequences of adult asthma in NHANES and Follow-up Survey. Am Rev Respir Dis 1989; 139: Dodge RR, Burrows B. The prevalence and incidence of asthma and asthma-like symptoms in a general population sample. Am Rev Respir Dis 1980; 122: Dodge R, Cline MG, Burrows B. Comparisons of asthma, emphysema, and chronic bronchitis diagnoses in a general population sample. Am Rev Respir Dis 1986; 133: Krzyzanowski M, Lebowitz MD. Changes in chronic respiratory symptoms in two populations of adults studied longitudinally over 13 years. Eur Respir J 1992; 5: Fletcher CM, Pride NB. Definitions of emphysema, chronic bronchitis, asthma, and airflow obstruction: 25 years on from the CBA symposium. Thorax 1984; 39: Colditz GA, Stampfer MJ, Willett WC, et al. A prospective study of parental history of myocardial infarction and coronary heart disease in women. Am J Epidemiol 1986; 123: Mantel N. Chi-square tests with one degree of freedom: extensions of the Mantel-Haenszel procedure. J Am Stat Assoc 1963; 58: Cox DR. Regression models and life-tables. J R Stat Soc 1972; 32: D' Agostino RB, Lee ML, Belanger AJ, et al. Relation of pooled logistic regression to time dependent Cox regression analysis: the Framingham Heart Study. Stat Med 1990; 9: Tager B, Speizer FE. Risk estimates for chronic bronchitis in smokers: a study of male-female differences. Am Rev Respir Dis 1976; 113: Brown CA, Crombie K, Smith WCS, et al. The impact of quitting smoking on symptoms of chronic bronchitis: results of the Scottish Heart Health Study. Thorax 1991; 46: CHEST /108/6/ DECEMBER,

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