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(Chest. 2004;125:1387-1393.)
© 2004 American College of Chest Physicians

Environmental Tobacco Smoke May Induce Early Lung Damage in Healthy Male Adolescents*

Maurizio Rizzi, MD; Margherita Sergi, MD; Arnaldo Andreoli, MD; Marica Pecis, MD; Claudio Bruschi, MD and Francesco Fanfulla, MD

* From the Respiratory Function Laboratory (Drs. Rizzi, Sergi, Andreoli, and Pecis), Ospedale Sacco, Milano; and Fondazione Salvatore Maugeri IRCCS (Drs. Bruschi and Fanfulla), Istituto Scientifico di Montescano, Montescano, Italy.

Correspondence to: Francesco Fanfulla, MD, Laboratorio di Fisiopatologia Respiratoria, Fondazione S. Maugeri Centro, Medico di Riabilitazione di Montescano, 27040 Montescanp (PV), Italy; e-mail ffanfulla{at}fsm.it


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: Childhood exposure to environmental tobacco smoke (ETS) adversely affects dynamic spirometric indexes as a result of combined early life (including in utero) and current exposure to parental smoking. The aim of our study was to investigate the effect of ETS on lung function and to identify the most sensitive functional parameter for evaluating lung damage.

Design: Cross-sectional survey.

Setting: Health survey on secondary school children.

Subjects: Eighty adolescents boys (mean age ± SD, 16 ± 1 years) classified in three groups: 21 smokers, 30 nonsmokers, and 29 passive smokers.

Measurements: Standardized questionnaire on the smoking habits of the subjects and their parents; assay of urinary cotinine level and measurement of the cotinine/creatine ratio (CCR); and lung function tests, including measurements of lung volumes, spirometric dynamic parameters, and the single-breath diffusing capacity of the lung for carbon monoxide (DLCO).

Results: Passive smokers presented a higher residual volume than nonsmokers, and a lower maximal expiratory flow at 25% of FVC (MEF25) and DLCO. Passive smokers whose mothers had smoked during pregnancy had significantly lower MEF25 percentage, DLCO, carbon monoxide transfer coefficient, and diffusion capacity of the alveolar-capillary membrane (DM) values than did passive smokers whose mothers had given up smoking during pregnancy. Nevertheless, the MEF25 and DM values of subjects with mothers who had given up smoking during pregnancy were lower than those observed in nonsmokers (p < 0.05), suggesting a negative effect of passive smoking independent of the mother’s smoking habit during pregnancy. A statistically significant, negative correlation was found between CCR and DLCO in smokers (r = – 0.63, p < 0.01) and in passive smokers (r = – 0.91, p < 0.001), but not in nonsmokers (r = 0.26, p = not significant), suggesting a dose-effect relationship.

Conclusions: Current exposure to ETS in healthy male adolescents is associated with lung function impairment independently of the effects of maternal smoking during pregnancy. More information may be obtained from determining static lung volumes and DLCO.

Key Words: cigarette • diffusion lung capacity • lung function • passive smoking • spirometry


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
A growing body of scientific evidence indicates that childhood exposure to environmental tobacco smoke (ETS) adversely affects lung function.1234567 Several studies89101112131415 suggest that pulmonary function decrement in school-aged children is a result of combined early life (including in utero) and current exposure to parental smoking. Exposure to maternal smoking during pregnancy is associated with deficits in lung function at birth that may persist into young adulthood.89101112131415 Because in utero exposure to maternal smoking and exposure to ETS during childhood are strongly correlated, both forms of exposure must be considered when assessing the adverse effects of tobacco smoke on pulmonary function. Gilliland et al16 found that exposure to maternal smoking during pregnancy is independently associated with decreased lung function, especially low forced expiratory flow volumes, in children of school age. The detrimental effect of passive smoking on lung function may be amplified in children with asthma. In fact, Li et al17 found that children with asthma have a large deficit in lung function that is associated with in utero exposure to maternal smoking, and that this deficit appears to be independent of the effects of subsequent ETS exposure. In contrast, previous studies1819 reported that in utero exposure had no effect, suggesting that passive smoking represent a major contributing factor to development and persistence of airflow obstruction or respiratory symptoms. Finally, low-level exposure to ETS seems to be associated with lung function alterations also in adolescents.20

Most studies on the effects of parental smoking on children and adolescents have quantified any effects on the lungs by dynamic spirometric indexes, while less is known about the effects on static lung volumes and diffusion capacity of the lung for carbon monoxide (DLCO).21 However, one can hypothesize that functional impairment due to passive smoking may also be evidenced by other lung function tests, and that these might be more sensitive at detecting early lung damage. We studied a group of healthy male adolescents to investigate the effect of exposure to ETS on lung function, and to identify the most sensitive functional parameter for evaluating lung damage.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population
We considered a group of 121 male adolescents attending secondary schools in Milan who were participating in an educational campaign on the harmful effects of active smoking and passive exposure to the smoke. We excluded 41 subjects: 14 subjects because they had a history of cardiopulmonary disease, asthma, or acute respiratory disease in the 3 months preceding the study; and the other 27 subjects because they were exposed to inhalants harmful to the lungs either because they lived in particularly polluted parts of the city or because of a part-time job.

The survey was carried out between April 1998 and May 1998. Informed consent was obtained in all cases from parents or legal guardians. All the 80 subjects studied underwent the following assessments.

Questionnaire
A questionnaire on the smoking habits of the subjects and their parents, sociodemographic factors, personal history of allergies, and pulmonary and cardiovascular diseases was completed by the adolescents included in the study. We recorded data on current smoking habits of the parents and other people living in the home, the frequency of visits to places that are often smoky (community centers, amusement halls), and the overall time exposed to ETS.

Assay of Urinary Cotinine Level
Urinary cotinine is a specific metabolite of nicotine with a half-life of approximately 20 to 40 h. This metabolite is a validated marker of exposure to ETS. The urinary concentrations of cotinine were determined by competitive inhibition radioimmunoassay using rabbit cotinine antiserum and treated cotinine.22 To compensate for the effect of variable dilution on the spot concentration of urinary cotinine, creatinine was measured and the cotinine/creatine ratio (CCR) was calculated.

Lung Function Tests
Lung volumes and spirometric dynamic parameters were assessed by plethysmography (VMAX227Autobox V6200; SensorMedics; Yorba Linda, CA), performed in accordance with European Respiratory Society criteria.23 Single-breath DLCO was measured (Transfer Test; Morgan; Kent, UK) according to the recommendations from the European Respiratory Society.24 Double measurements were accepted when estimates of DLCO and effective alveolar volume differed by < 5%. DLCO was measured using a low oxygen concentration (CO, 0.25%; He, 14%; O2, 20%) and a high oxygen concentration (CO, 0.25%; He, 14%; O2, 85 to 75%); the breath-holding time was at least 10 s. and the washout volume was 0.75 L. The interval between measurements was 5 min, and the tests were performed in the standing position. DLCO was adjusted for the level of carboxyhemoglobin (COHb), measured with a blood gas analyzer (Critical Care Laboratory Synthesis 35; Instrumentation Laboratory; Paderno Dugnano, Italy), using the following equation25:

The carbon monoxide transfer coefficient (KCO) was derived from the following equation: KCO = DLCO/alveolar volume. The diffusing capacity of the alveolar-capillary membrane (DM) and the pulmonary capillary blood volume were calculated using the Roughton and Forster26 equation.

We compared the recorded lung function data with the predicted values proposed by Rosenthal et al.2728 Pubertal stage was evaluated according to the method of Tanner.29 All the adolescents evaluated were in late puberty (stage 4 or 5).

Data on atmospheric pollution were obtained from the regional environmental monitoring system. The pollutants considered in the monitoring were sulfur dioxide, particulate matter, nitrogen dioxide, ground-level ozone, carbon monoxide, lead, fluorine, and total hydrocarbons. The study was temporarily suspended when the levels of pollutants exceeded the alarm threshold for at least 3 days in the week before the planned day of respiratory function testing. All the subjects tested in the study were exposed to the same levels of outdoor pollutants since they lived in the same area, so that the relationship between outdoor pollutant levels and respiratory function data cannot be tested.

Statistical Analysis
Data were stored and analyzed with the STATISTICA/w (StatSoft; Tulsa, OK) and SPSS V.6.1 (SPSS; Chicago, IL) software packages. All the variables entered in the analyses were expressed as mean and SD. One-way analysis of variance was used to compare data among the groups of subjects considered. The Tukey honestly significant difference test for unequal sample sizes (Spjotvoll and Stoline test) was used to compare differences between groups. Unpaired t test analysis was used to compare data between the passive smokers whose mothers had or had not smoked during pregnancy. The relationships between the variables were evaluated using the Pearson product-moment correlation coefficient; p < 0.05 was considered statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The 80 adolescents (mean age ± SD, 16 ± 1 years; height, 167 ± 9 cm; weight, 63 ± 6 kg) were classified into three groups on the basis of the responses to the questions concerning smoking and passive smoke exposure: 30 nonsmokers, 29 passive smokers, and 21 smokers. The three groups did not differ for age (mean, 16 ± 1 years for all the three groups), height (mean, 165 ± 8 cm, 165 ± 9 cm, 165 ± 9 cm, respectively, p = not significant [NS]), weight (mean, 63 ± 7 kg, 63 ± 8 kg, and 63 ± 7 kg, respectively, p = NS), or socioeconomic status. The smokers had been smoking approximately 18 to 26 cigarettes a day (mean, 21 ± 3 cigarettes a day) for 1 to 4 years (mean, 2.9 ± 1.1 years). Of the 29 passive smokers, 10 smokers (35%) were exposed to the smoke of only one family member and 19 smokers (65%) were exposed to the smoke of more family members. The mean number of cigarettes smoked per day by each family member was 34 ± 20 cigarettes, and for each adolescent the time of exposure to the ETS was 280 ± 64 min/d. Eighteen of the passive smokers had also been exposed to maternal smoking during pregnancy. The CCR levels increased significantly from nonsmokers (18.6 ± 9.9 µg/mg) to passive smokers (65.5 ± 23.2 µg/mg), and from passive smokers to smokers (124.7 ± 41 µg/mg) [analysis of variance F, 103.3; p < 0.0001].

Table 1 reports the lung function data in the groups of subjects considered. Smokers had significantly poorer lung function, even in the absence of any clinical symptoms. Indeed, 24% of the smokers had signs of overt bronchial obstruction. Furthermore, smokers had a statistically significant increase in residual volume (RV) and in the ratio between RV and total lung capacity (TLC), and a statistically significant reduction of DLCO, KCO, and DM. Deficits in lung function were also observed in adolescents exposed to ETS. However, the alterations observed in lung volumes in these adolescents were smaller than those observed in the smokers. Maximal expiratory flow at 25% of FVC (MEF25) was lower, RV higher, and RV/TLC ratio greater in adolescents exposed to ETS than among the nonsmokers. Furthermore, DLCO, KCO, and DM were significantly lower in passive smokers than in nonsmokers.


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  		Table 1. Respiratory Function Values in the Three Groups of Subjects*

 
In order to analyze the role of in utero exposure to smoke in determining lung function alterations, we classified passive smokers into two subgroups according to the smoking habit of the mothers during pregnancy. Passive smokers whose mothers had smoked during pregnancy had significantly lower MEF25 percentage, DLCO, KCO, and DM values than did passive smokers whose mothers had given up smoking during pregnancy (Table 2 ). Nevertheless, the MEF25 and DM values of subjects with mothers who had given up smoking during pregnancy were lower than those observed in nonsmokers (p < 0.05), suggesting a negative effect of passive smoking independent of the mother’s smoking habit during pregnancy (Table 3 ). Furthermore, smokers had lower values of MEF25, KCO, and DM (p < 0.05) than did adolescents with mothers who smoked during pregnancy (Table 3). The same functional parameters were lower in subjects exposed to the smoke of more than one family member than in adolescents living in a household with only one parent who smoked (Table 4 ).


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  		Table 2. Comparison of Respiratory Function Data in the Two Subgroups of Passive Smokers Considered*

 

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  		Table 3. Comparison Between Groups Exposed and Not Exposed to Smoke In Utero*

 

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  		Table 4. Differences in Lung Function Between Passive Smokers Exposed to Smoke From One or More Family Members*

 
A strong, statistically significant, negative correlation was found between CCR level and DLCO in smokers (r = – 0.63, p < 0.01; Fig 1 , top), and in passive smokers (r = – 0.91, p < 0.001; Fig 1, middle), but not in nonsmokers (r = 0.26, p = NS; Fig 1, bottom), suggesting a dose-effect relationship. Furthermore, in the passive smokers, the time of exposure to the ETS was negatively correlated with MEF25 (r = – 0.49, p = 0.05) and DLCO (r = – 0.89, p < 0.001).



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  		Figure 1. Correlations between CCR and DLCO (TLCOsb) in smokers (top), in passive smokers (middle), and in nonsmokers (bottom). Dashed lines represent the 95% confidence interval.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We studied a group of apparently healthy adolescents without any chronic respiratory symptoms to assess the influence of passive smoking on lung function. We found that passive smoking is associated with an increase in RV and a reduction in KCO, suggesting early alterations in both bronchial and alveolar structures. Secondly, we found that in utero and current exposure to ETS are both independently associated with lung function abnormalities. A strong relationship between the level of ETS exposure and lung damage was found. The group of healthy adolescent smokers showed evidence of mild airway obstruction; these results are consistent with those given in previous reports.30

Several studies567 have shown that exposure to ETS is associated with poor respiratory health in children; more recent studies31 have also demonstrated this effect in adults. Children have been identified as a population sensitive to the effects of ETS, since exposure during childhood can be high and the children may be particularly vulnerable to noxious stimuli during the period of growth and development. In most studies of lung function in children, ETS is associated with findings of impaired pulmonary function. However, all the studies so far published have used only spirometry to test lung function. In a longitudinal study, Wang et al8 observed that the decrement in pulmonary function found in school-aged children whose mothers smoked seemed to be due to a combination of a persistent deficit associated with earlier (including in utero) exposure and an additional deficit related to current exposure. Cunningham et al9 found that the effect of maternal smoking during pregnancy appeared to be larger than that of current exposure to ETS and not affected by it, while the observed effects of current smoking were NS after adjustment for in utero exposure. Gilliland et al16 reported that in utero exposure to maternal smoking is independently associated with decreased lung function in children of school age, especially when small airway flows are considered. Finally, in a large study of children aged 7 to 19 years with and without asthma, Li et al17 found that both in utero exposure to maternal smoking and ETS exposure were associated with persistent deficits in lung function; deficits in forced expiratory flows associated with current ETS were significant only among children without asthma.

In accordance with results from a previous study,17 the only spirometric index that we found to be lower in passive smokers than in nonsmokers was MEF25, suggesting an initial alteration of small airways. However, in the above-mentioned articles, neither static lung volumes nor KCO were considered. In our study, we demonstrated that the most relevant indicators of lung damage were an increased RV and a decrease in DLCO. These parameters seem to be more sensitive at detecting initial lung damage. The degree of respiratory function impairment observed in passive smokers was lower than that observed in current smokers. A significant negative relationship was found between the amount of exposure to smoke and the degree of functional impairment. In most previous articles,8111617 ETS exposure was considered as a dichotomous variable; in our study, we measured the degree of exposure, recording both daily time of exposure and urinary cotinine levels, and were thus able to detect a clear dose-effect relationship.

We found that in utero exposure to smoking and current exposure to ETS are independent factors in determining lung damage. The values of spirometric and diffusion capacity indexes were lowest in the subgroup exposed both in utero and subsequently to ETS; current passive smokers who had been spared exposure during in utero life had poorer respiratory function than nonsmokers.

The negative effect of tobacco smoke on DLCO, also in the general population, is well known. In 1990 Viegi et al32 studied a general population sample of 1,612 subjects aged 20 to 64 years, and revealed a significantly lower DLCO in smokers than in nonsmokers. Furthermore, DLCO indexes were almost always selected as discriminant variables in multivariate analysis between asymptomatic and symptomatic subjects.30 Neas and Schwartz33 looked for the determinants of pulmonary diffusing capacity and found that in a larger cohort of subjects without clinical respiratory disease, current smokers and former smokers had lower levels of DLCO.

Clark et al34 compared groups of smokers and nonsmokers and recorded a significant negative correlation between KCO and cotinine level, an increased RV, and a reduction of FEV1 and KCO. High-resolution CT demonstrated the presence of emphysematous damage in a moderate number of subjects, and these authors came to the conclusion that emphysema is associated with high alveolar smoke exposure.

The alteration of the DLCO provoked by a decrease of DM in healthy young smokers was described by Bosisio et al35 in 1980. Similar results were obtained in a group of adolescent smokers, and were accompanied by increasing pulmonary air trapping.36 We took care to avoid any possible bias when performing the DLCO analysis. DLCO values were corrected for COHb in order to minimize the confounding factor of carbon monoxide back pressure; similarly, the bias due to different concentrations of hemoglobin was eliminated.

There is evidence that neonatal lung mechanics are altered when the mother smokes during pregnancy. As mentioned above, a couple of studies on in utero exposure and infant lung function suggest that maternal smoking during pregnancy has an important role in causing the lung function deficits. Our findings suggest an independent effect of current ETS. We studied two subgroups of passive smokers: those exposed only after birth, and those exposed both during pregnancy and after birth.

The values of MEF25 and DLCO were lower in the group with mothers who smoked during pregnancy than in the group with mothers who had given up smoking during pregnancy; indeed, the degree of alteration was quite similar to that observed in smokers. Furthermore, the subjects with mothers who had given up smoking during pregnancy had lower values of MEF25 and DM than did nonsmokers. In other words, in healthy male adolescents lung impairment increased, moving from nonsmokers, to passive smokers during childhood (mothers who had given up smoking during pregnancy), to passive smokers during childhood and intrauterine life (mothers who smoked during pregnancy), and to smokers.

In conclusion, our study demonstrates that current exposure to ETS in healthy male adolescents is associated with lung function impairment independently of the effects of maternal smoking during pregnancy. A significant correlation was found between the level of exposure and functional impairment. Finally, our study suggests that more information may be obtained from determining static lung volumes and DLCO. However, longitudinal studies are needed to demonstrate the real role of these functional parameters in identifying subjects more prone to be affected by ETS-induced lung damage.


   Footnotes
 
Abbreviations: CCR = cotinine/creatine ratio; COHb = carboxyhemoglobin; DLCO = diffusing capacity of the lung for carbon monoxide; DM = diffusing capacity of the alveolar-capillary membrane; ETS = environmental tobacco smoke; KCO = carbon monoxide transfer coefficient; MEF25 = maximal expiratory flow at 25% of FVC; NS = not significant; RV = residual volume; TLC = total lung capacity

Received for publication May 13, 2003. Accepted for publication November 6, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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