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Dec 9, 2010 - The study was based on. 2020 women who provided data on respiratory function, smoking, and menopausal status. A Spirobank G spirom-.
Lung (2011) 189:65–71 DOI 10.1007/s00408-010-9269-9

RESPIRATORY PHYSIOLOGY

Association Between Smoking and Respiratory Function Before and After Menopause Mohammad R. Hayatbakhsh • Jake M. Najman Michael J. O’Callaghan • Gail M. Williams • Anita Paydar • Alexandra Clavarino



Received: 25 March 2010 / Accepted: 4 November 2010 / Published online: 9 December 2010 Ó Springer Science+Business Media, LLC 2010

Abstract There is a lack of evidence about whether menopausal status influences the effect of smoking on lung function. This study examined the association between smoking and menopausal status and lung function independent of each other. Data were from a cohort of women attending the 21-year follow-up of the Mater University of Queensland Study of Pregnancy. The study was based on 2020 women who provided data on respiratory function, smoking, and menopausal status. A Spirobank G spirometer system was used to measure forced vital capacity (FVC), forced expiratory volume in first second (FEV1), and forced expiratory flow between 25 and 75% of forced vital capacity (FEF25–75). Smoking and menopausal status were assessed by self-report. Respiratory function was associated with cigarette smoking, menopausal status, and hormone replacement therapy. Regardless of smoking status, postmenopausal women had poorer lung function when compared with premenopausal women. In multivariate analysis, cigarette smoking was associated with lower FVC, FEV1, and FEF25–75, with the magnitude of effect being stronger for women who were postmenopausal. The data suggest that the impact of smoking intensifies after M. R. Hayatbakhsh (&)  J. M. Najman  G. M. Williams  A. Paydar School of Population Health, University of Queensland, Herston Road, Herston, QLD 4006, Australia e-mail: [email protected] M. J. O’Callaghan Department of Paediatrics and Child Health, University of Queensland, Mater Children’s Hospital, South Brisbane, QLD 4101, Australia A. Clavarino School of Pharmacy, University of Queensland, St Lucia, QLD 4072, Australia

menopause. It seems plausible that effective quit-smoking programs, particularly after menopause, may lead to better lung function and reduced morbidity and mortality in women. Keywords Smoking

Lung function  Women  Menopause 

Introduction The menopausal transition is associated with a series of hormonal and metabolic changes and has been linked to obstructive respiratory presentations, including asthma; however, the findings are inconsistent [1–4]. For example, Balzano et al. [1] indicated that asthma symptoms first appear or increase in severity around the age of menopause, while another study conducted in several northern European countries did not show a significant association between menopause and asthma symptoms [3]. A more recent study has found that postmenopausal women had significantly lower forced expiratory volume in the first second (FEV1) and forced volume capacity (FVC) as well as more respiratory symptoms [4]. Evidence from the literature shows that sex hormones influence women’s lung health [5–8]. Studies have shown that hormone replacement therapy (HRT) usage among women in the postmenopausal period is associated with a higher lung function and lower prevalence of airflow obstruction [9–12]. Similarly, estrogen and progesterone use have also been linked with improved pulmonary function in premenopausal women [12]. Studies have also shown respiratory function improvements in subsets of pregnant women [13–15] and in those using oral contraceptives [16, 17].

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Tobacco smoking is the most well-known risk factor for accelerating lung function decline in adults [18], including increased rate of chronic obstructive pulmonary disease (COPD) among women [19–21]. Cigarette smoking may modify hormonal status in women, which may, in turn, affect their lung function. It has been found that women who are active smokers are more likely to be estrogen-deficient compared with nonsmokers since cigarette smoke alters estrogen metabolism [9, 22]. Studies have shown that as female smokers age, they tend to experience a faster decline in FEV1 when compared with their male counterparts, but they tend to have greater improvement in lung function in response to smoking cessation than men [9, 18, 20]. Notwithstanding the strong evidence about the impact of smoking on respiratory function, there is a lack of information about whether the effect of smoking on lung function is modified by menopause. This study aims to examine the association between smoking status and lung function of women. It also aims to explore whether the association between smoking and lung function is influenced by the occurrence of menopause and the use of HRT.

Materials and Methods Subjects Data for this study were derived from the Mater University of Queensland Study of Pregnancy (MUSP) and its outcomes. Details of this project have been reported previously [23, 24]. Briefly, commencing in 1981, 8556 consecutive women in early pregnancy were invited to participate in the study. Some 8458 agreed to participate and 7223 gave birth to a live singleton baby at the study hospital. Mothers and children were subsequently followed up at 3–5 days, 6 months, and 5, 14, and 21 years after the child’s birth. At the 21-year followup, 3886 women completed a questionnaire. Of these a subsample of 2612 (average age = 46.4 years) were administered a physical assessment, including lung function tests. Persons living outside Brisbane or those who were unable to make an appointment for a face-to-face interview completed a mailed questionnaire and did not undergo the physical assessment. This study was based on 2020 women for whom data on respiratory function, smoking, and menopausal status were available. Informed consent was appropriately obtained from all participants. Measurements Lung Function Tests Pulmonary function testing was performed at the 21-year follow-up using a Spirobank G spirometer system attached

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to a laptop computer. Qualified and trained interviewers familiar with the instrument were employed to perform spirometric tests in accordance with American Thoracic Society (ATS) guidelines [25]. A minimum of three and a maximum of five trials were attempted. If testing was unsatisfactory for any reason, the reason(s) was noted on the record sheets. For the purposes of this study, forced vital capacity (FVC), forced expiratory volume in first second (FEV1), forced expiratory flow, and midexpiratory phase (FEF25–75) were considered as outcomes of interest. Smoking Status At the 21-year follow-up of the MUSP, the women were asked to describe their smoking status. Options were: never smoked before, used to smoke, smoked occasionally, and smoked regularly. Participants were also asked to indicate the number of cigarettes they smoked per day during the last week. Options for this question were structured as none, 1–9, 10–19, 20–29, 30–49, or 50 or more cigarettes per day. The participants’ responses were used to divide them into four categories: nonsmoker and smoking less than 10, 10–19, and 20 or more cigarettes per day. A third question asked: At what age did you start smoking? Responses ranged between 5 and 47 years (mean = 16.7 years, standard deviation [SD] = 4.3). We calculated the duration of smoking by subtracting the age of initiation from the current age. Among the smokers, the average duration of cigarette smoking was 19.6 (SD = 10.2) years. Menopausal Status At the 21-year follow-up, women were asked the following: ‘‘When did you have your last period?’’ (answers were ‘‘in the last month,’’ ‘‘in the last 3 months,’’ ‘‘between 3 and 11 months,’’ and ‘‘12 months ago or more’’). Consistent with other studies, postmenopausal status was defined as the absence of menstruation for 12 months [26–28]. Subsequently, women were divided into two groups: last period within the past 12 months (defined as premenopausal hereafter) and those who had their last period more than 12 months ago (defined as postmenopausal hereafter). Other Variables The age of the participants was assessed at entry into the study. Participants’ height was measured to the nearest centimeter at the 21-year follow-up (mean = 162.1 cm, SD = 6.6). Participants were also asked if they were currently on hormone replacement therapy (options were no and yes). They were also asked: ‘‘How many years in total have you ever used hormone replacement therapy?’’ (alternative

Lung (2011) 189:65–71

answers were ‘‘never used,’’ ‘‘less than one year,’’ ‘‘1–4 years,’’ ‘‘5–10 years,’’ and ‘‘more than 10 years’’).

67 Table 1 Characteristics of women according to menopausal status Participants characteristics

Menopausal status

p value

Premenopausal Postmenopausal

Statistics 45.1 (4.1)

50.1 (5.5)

\0.001a

Height, mean (SD) (cm) 162.4 (6.9)

161.4 (5.8)

\0.01a

Age, mean (SD) (years)

For analysis, we included 2020 women who underwent spirometry at the 21-year follow-up and for whom data were available about smoking and menstrual status. The outcome variables were FVC, FEV1, and FEF25–75. Exposure variables were smoking status, frequency of smoking in the last week, and menopausal status. We used primarily v2 tests (where variables were categorical) and Student t tests (where variables were continuous) to examine the association between characteristics of the participants and menopausal status. Analysis of variances (ANOVA) and Student t tests were used to examine the three spirometry tests according to participants’ smoking status, menopause, and hormone replacement therapy. Subsequently, we used Student t tests to compare the means of respiratory function tests before and after menopause for each category of smoking status. Finally, we conducted stratified analyses to examine the association between women’s smoking and their respiratory function tests according to menopausal status. For these analyses, participants not exposed to smoking were considered the reference group, and their age, height, and hormone replacement therapy were considered potential confounding variables. The results reported are the estimated differences in lung function (in liters [L]) for women exposed to smoking, relative to unexposed women, and separately for women with last menstrual period within or before the past 12 months. The associations were considered statistically significant if p \ 0.05. All analyses were conducted using Stata v.10 (Stata Corp., College Station, TX).

Results Descriptive Findings A total of 2020 women who underwent lung function tests and for whom data were available on cigarette smoking, menopausal status, and other covariates at the 21-year follow-up were included in this study. They had a mean age of 46.4 (SD = 4.9) years. Of those, 1474 (73.0%) had their last period within the past 12 months, while 546 (27.0%) had not had a period for at least 12 months. They had a mean (SD) of FVC = 3.3 (0.6), FEV1 = 2.7 (0.5), and FEF25–75 = 2.9 (0.9) L. Table 1 shows the characteristics of the participants according to their menopausal status. Women categorized in the premenopausal period were, on average, 5 years

\0.05b

Smoking status, n (%) Nonsmoker

624 (42.3)

241 (44.1)

Ex-smoker

451 (30.6)

135 (24.7)

Smoke occasionally Smoke regularly Cigarettes smoked per day in last week None \10 10–19 20? Duration of smoking, mean (SD) (years)

55 (3.7)

17 (3.1)

344 (23.3)

153 (28.0) 0.21b

1075 (72.9)

376 (68.9)

78 (5.3)

39 (7.1)

142 (9.6)

62 (11.4)

179 (12.1) 18.6 (9.7)

69 (12.6) 22.8 (10.9)

\0.001a \0.001b

Hormone replacement therapy No

1423 (96.5)

438 (82.0)

Yes

51 (3.5)

108 (19.8)

a

Derived from Student’s t -test

b

Derived from v2 test

younger and nearly 1 cm taller than postmenopausal women. The premenopausal group were slightly more likely to be ex-smokers, while current regular smoking occurred more commonly among postmenopausal women. The data also show that frequency of cigarette smoking was not significantly different between premenopausal and postmenopausal women, whereas participants in the postmenopausal group reported longer duration (4 years) of cigarette smoking. A total of 159 (7.8%) women claimed to use hormone replacement therapy, of which 108 belonged to the postmenopausal category. The difference in means (SD) of the lung function tests according to women’s smoking, menopausal status, and hormone replacement therapy is presented in Table 2. Univariate ANOVA tests show that ex-smokers had higher FVC and FEV1, while FEV1 and FEF25–75 were statistically significantly lower in regular smokers when compared with nonsmokers. In regard to the number of cigarettes smoked per day, there was a reverse association with lung function so that women who reported smoking 10 or more cigarettes per day had lower FVC, FEV1, and FEF25–75 than nonsmokers. For the premenopausal group, the lung function tests were statistically significantly (p \ 0.001) higher than that of postmenopausal women. The data also show that women who reported having received hormone replacement therapy had lower lung function.

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Table 2 Association of smoking, menopausal status, and hormone replacement therapy with respiratory function Independent variables

Respiratory function tests (L) FVC

FEF25–75

FEV1

Smoking status Never smoker

3.28 (0.57)

2.72 (0.46)

2.96 (0.84)

Ex-smoker

3.36 (0.58)a

2.79 (0.47)a

3.04 (0.84)

Occasional

3.23 (0.57)

2.62 (0.48)

2.79 (0.83)

Regular

3.21 (0.62)

2.60 (0.50)a

2.67 (0.88)a

F (df, p)

6.13 (3, \0.001)

Cigarettes per day in last week None

14.06 (3, \0.001)

19.23 (3, \0.001)

3.31 (0.57)

2.74 (0.46)

2.99 (0.84)

\10

3.30 (0.65)

2.69 (0.51)

2.80 (0.81)

10–19

3.19 (0.53)a

2.58 (0.47)a

2.71 (0.93)a

a

a

2.62 (0.86)a

20? F (df, p)

3.20 (0.66)

5.95 (3, \0.001)

2.58 (0.53)

12.81 (3, \0.001)

19.14 (3, \0.001)

Menopausal status Premenopausal

3.35 (0.57)

2.76 (0.46)

Postmenopausal

3.10 (0.60)

2.55 (0.49)

2.96 (0.86) 2.75 (0.85)

t (df, p)

9.05 (2018, \0.001)

9.65 (2018, \0.001)

5.07 (2018, \0.001)

No

3.30 (0.59)

2.72 (0.48)

2.92 (0.86)

Yes

3.06 (0.57)

2.53 (0.47)

2.75 (0.83)

t (df, p)

4.99 (2018, \0.001)

4.88 (2018, \0.001)

2.43 (2018, \0.001)

Hormone replacement

Data are means (standard deviation) FVC forced vital capacity, FEV1 forced expiratory volume in first second, FEF25–75 forced expiratory flow between 25 and 75% a

Statistically significant difference with reference category derived from Bonferroni test

Table 3 shows an unadjusted association between women’s smoking, menopausal status, and the interaction between smoking and menopausal status and respiratory function tests. Data indicate that current regular smoking is associated with lower measures of FVC, FEV1, and FEF25–75. In addition, smoking more that 10 cigarettes per day predicts statistically significant declines in lung function. Postmenopausal women had lower respiratory function results compared with premenopausal women. Moreover, data indicate that interaction between smoking and menopausal status is statistically significantly associated with the results of spirometry tests. Data show that for each category of smoking status and quantity of cigarettes smoked per day, postmenopausal women have lower FVC, FEV1, and FEF25–75 when compared with the premenopausal group. As menopausal status modifies the association between smoking and respiratory function, we used a series of multivariate regression models to examine the relationship between women’s smoking and their lung function stratified by menopausal status. Table 4 shows these associations controlled for women’s age, height, and use of hormone replacement therapy. Women who reported being regular smokers had lower FVC, FEV1, and FEF25–75, regardless of their menopausal status. For the postmenopausal group,

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occasional smoking was also associated with lower FEV1 and FEF25–75. Interestingly, the magnitude of associations was stronger for women who were postmenopausal. The data in Table 4 also indicate that there is a dose–response relationship between cigarette smoking and lung function tests adjusted for age, height, and hormone therapy. The more cigarettes women smoked at the 21-year follow-up, the lower measures of spirometry test they had, with a stronger effect observed among postmenopausal women.

Discussion To date, there is a lack of evidence about whether the effect of smoking on respiratory function is influenced by menopausal status and hormone replacement therapy. This study showed that women’s cigarette smoking and menopausal status are independently associated with their respiratory function. After controlling for age, height, and hormone replacement therapy, cigarette smoking was associated with impaired respiratory function tests (FVC, FEV1, and FEF25–75). Our data also suggest that regardless of smoking status, postmenopausal women had impaired lung function when compared with premenopausal women. Furthermore,

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Table 3 Unadjusted association of smoking and menopausal status with respiratory function Respiratory function testsa FVC

FEV1

FEF25–75

Never smoker

Ref

Ref

Ref

Ex-smoker Occasional

0.01 (0.03) -0.13 (0.06)*

0.01 (0.02) -0.16 (0.05)**

0.01 (0.04) -0.25 (0.10)*

Regular

-0.18 (0.03)***

-0.21 (0.02)***

-0.40 (0.05)***

that cigarette smoking has a stronger effect on the lung function of postmenopausal women and this effect is not significantly modified by hormone replacement therapy. Mechanisms of the Association

Smoking status

Cigarettes smoked per day in last week None

Ref

Ref

Ref

\10

-0.07 (0.05)

-0.11 (0.04)**

-0.25 (0.08)**

10–19

-0.15 (0.04)***

-0.19 (0.03)***

-0.34 (0.06)***

20?

-0.24 (0.03)***

-0.26 (0.03)***

-0.49 (0.06)***

Menopausal status Premenopause

Ref

Ref

Ref

Postmenopause

-0.08 (0.03)**

-0.06 (0.02)**

-0.03 (0.05)

Hormone replacement therapy No

Ref

Ref

Ref

Yes

-0.12 (0.04)**

-0.08 (0.03)*

-0.06 (0.07)

Interaction (menopause and -0.04 -0.04 -0.07 smoking status) (0.006)*** (0.005)*** (0.01)*** Interaction (menopause and -0.05 cigarettes per day) (0.07)***

-0.05 -0.10 (0.005)*** (0.01) ***

Data are regression coefficient (standard error) FVC forced vital capacity, FEV1 forced expiratory volume in first second, FEF25–75 forced expiratory flow between 25 and 75% a

Adjusted for participant’s age and height; statistically significant difference compared with reference category *p \ 0.05; **p \ 0.01; ***p \ 0.001

the magnitude of association for smoking appears to be stronger for women who were postmenopausal. Review of the literature indicates that the relationship between menopause and lung function has rarely been studied, although there has been some evidence of an association. In a multinational study of women 45–56 years old, Real et al. [4] found that postmenopausal women had impaired lung function when compared with those who were menstruating. Consistent with this finding, our data indicate poorer lung function tests among women who had not menstruated in the 12 months prior to data collection. The finding of this study is also consistent with previous research that indicated the adverse impact of smoking on lung function [9, 19]. However, our findings also suggest

There are several possible explanations for the observed differences in the association between smoking and lung function according to menopausal status. First, it can be argued that the stronger effect of smoking on respiratory function in the postmenopausal period is due to the duration and frequency of cigarette smoking rather than to the menopause per se. In the current study there was no significant difference in the frequency of cigarette smoking according to menopausal status, but postmenopausal women reported a longer duration of smoking. Alternatively, it is hypothesized that the level of estrogen in premenopausal women protects the respiratory system against the harmful effect of smoking. In a study of 2353 women aged 65 years and older, Carlson et al. [12] found that current use of HRT was associated with improved lung function tests. However, our data suggest no protective effect of HRT on the association of smoking and lung function among postmenopausal women. The discrepancy between the findings of these studies concerning the impact of HRT might be due to different methods of measurement, dose, and duration of use of HRT. Limitations There are a few limitations in interpreting the results. The present study relied on self-reports of smoking. There is a possibility that women in this age group under-report their smoking. Such potential misclassification might have led to an underestimation of the impact of smoking on lung function. In the present study participants reported smoking within the preceding week. It can be argued that smoking measurement within a short interval may under-represent the true impact of smoking on respiratory function. We also assessed menopausal status according to women’s self-reports of the timing of their last period. This may be associated with a nondifferential misclassification of menopause and result in a relationship between menopause and lung function tending toward a null value. Another limitation is the sizable reduction in the sample between first clinic visit (recruitment to the study) and the 21-year follow-up. Over the 21 years of the study, women who smoked at any of the data collection phases were more likely to drop out of the study by the 21-year follow-up (p \ 0.01). Attrition from the study may influence our results in two different ways. If the association between smoking and lung function in those women lost to followup was higher than in the study group, our findings would

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Table 4 Adjusted association of smoking with respiratory function stratified by menopausal status Respiratory function testsa Premenopausal (n = 1474)

Postmenopausal (n = 531)

FVC

FEV1

FEF25–75

FVC

FEV1

FEF25–75

Never smoker

Ref

Ref

Ref

Ref

Ref

Ref

Ex-smoker Occasional

0.02 (0.03) -0.08 (0.07)

0.02 (0.03) -0.09 (0.06)

0.05 (0.05) -0.12 (0.12)

-0.07 (0.05) -0.25 (0.12)*

-0.06 (0.04) -0.38 (0.10)***

-0.10 (0.09) -0.62 (0.19)**

Regular

-0.17 (0.03)***

-0.19 (0.03)***

-0.36 (0.06)***

-0.19 (0.05)***

-0.24 (0.04)***

-0.52 (0.08)***

Smoking status

Cigarettes per day in last week None

Ref

Ref

Ref

Ref

Ref

Ref

\10

0.01 (0.06)

-0.07 (0.05)

-0.27 (0.10)**

-0.21 (0.08)*

-0.16 (0.06)*

-0.20 (0.13)

10–19

-0.16 (0.04)***

-0.17 (0.04)***

-0.26 (0.08)***

-0.13 (0.07)*

-0.23 (0.05)***

-0.51 (0.11)***

20?

-0.25 (0.04)***

-0.25 (0.03)***

-0.43 (0.07)***

-0.17 (0.06)**

-0.27 (0.05)***

-0.64 (0.10)***

Data are regression coefficient (standard error) FVC forced vital capacity, FEV1 forced expiratory volume in first second, FEF25–75 forced expiratory flow between 25 and 75% a

Adjusted for participant’s age, height, and hormone replacement therapy; statistically significant difference compared with reference category * p \ 0.05; ** p \ 0.01; *** p \ 0.001

underestimate the true association. There is a threat to the validity of our findings if the association we have observed is either not evident or is in the opposite direction to that of those lost to follow-up. Given the likely causal pathways and the positive association reported by other authors, overestimating the observed relationship is unlikely.

Conclusions The data in this study suggest that women’s smoking, particularly after menopause, has an adverse effect on their respiratory function. Given the existing evidence confirming respiratory function as a strong predictor of mortality due to lung diseases, cardiovascular problems, cancers, and other causes [29, 30], the findings of this study have implications for both clinicians and for public health more generally. While exposure to smoking has negative consequences for respiratory function, our data suggest that its impact is magnified after menopause. The effect of smoking appears to be independent of the use of hormone replacement therapy, women’s age, and height. Clinicians should consider the increasingly adverse effects of smoking on women’s lung function after menopause. It seems plausible that effective quit-smoking programs, particularly after menopause, may lead to better lung function and reduced morbidity and mortality in women. Acknowledgments We thank all participants in the study, the MUSP data collection team, and Greg Shuttlewood of the University of Queensland who has helped to manage the data for the MUSP. The study was funded by the National Health and Medical Research

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Council (NHMRC) of Australia, but the views expressed in the article are those of the authors and not necessarily those of any funding body.

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