Ozone Exposure and Lung Function* Effect Modified by Obesity and Airways Hyperresponsiveness in the VA Normative Aging Study

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1 Original Research ASTHMA Ozone Exposure and Lung Function* Effect Modified by Obesity and Airways Hyperresponsiveness in the VA Normative Aging Study Stacey E. Alexeeff, BSc; Augusto A. Litonjua, MD, MPH, FCCP; Helen Suh, ScD; David Sparrow, ScD; Pantel S. Vokonas, MD; and Joel Schwartz, PhD Background: Ozone has heterogeneous effects on lung function. We investigated whether obesity and airways hyperresponsiveness (AHR) modify the acute effects of ozone on lung function in the elderly. Methods: We studied 904 elderly men from the Normative Aging Study whose lung function (FVC, FEV 1 ) was measured approximately every 3 years from 1995 to We defined obesity as a body mass index of at least 30 kg/m 2. Using a standardized methacholine challenge test, we defined AHR as a FEV 1 decline of 20% after inhalation of a cumulative dosage of 0 to 8.58 mol of methacholine. Ambient ozone in the Greater Boston area was measured continuously. We estimated effects using mixed linear models, adjusting for known confounders. Results: An increase in ozone of 15 parts per billion during the previous 48 h was associated with a greater decline in FEV 1 in the obese ( 2.07%; 95% confidence interval [CI], 3.25 to 0.89%) than in the nonobese ( 0.96%; 95% CI, 1.70 to 0.20%). The same exposure was also associated with a greater decline in FEV 1 for those with AHR ( 3.07%; 95% CI, 4.75 to 1.36%) compared to those without AHR ( 1.32%; 95% CI, 2.06 to 0.57%). A three-way interaction trend test demonstrated a multiplicative effect of those two risk factors (p < 0.001). We found similar associations for FVC. Conclusions: Our results indicate that both obesity and AHR modify the acute effect of ozone on lung function in the elderly, with evidence of interaction between AHR and obesity that causes a greater than additive effect. (CHEST 2007; 132: ) Key words: air pollution; airway hyperresponsiveness; FEV 1 ; FVC; lung function obesity; ozone Abbreviations: AHR airway hyperresponsiveness; BMI body mass index; CI confidence interval; ppb parts per billion Many studies and metaanalyses 1 3 have found associations between acute ambient ozone exposure and increased risk of death. In addition, ambient ozone has been associated with increased respiratory-related emergency department visits and hospital admission in the elderly. 4 6 These findings suggest that the elderly are particularly susceptible to the effects of ozone. Lung function, as measured by spirometry, has been shown to predict all-cause mortality and causespecific (such as respiratory and cardiovascular) mortality. 7 9 Exposure to ozone has been documented to cause decrements in lung function in healthy subjects. 10,11 By identifying the characteristics of people most susceptible to the effects of ozone on lung function, we may gain insight into subpopulations most at risk of other ozone-induced effects on morbidity and mortality, as well as into the mechanisms responsible for the ozone effects. Few studies have examined the lung function response to ozone in the elderly. Many studies have been published examining younger populations, but since susceptibility to the effects of ozone has been shown to vary with age, 12 the effects of ozone in the elderly are still largely unknown. Past studies, which typically include only healthy nonsmokers, have found that functional responsiveness to ozone has been no greater, and usually lower, among older 1890 Original Research

2 adults than in young adults. Unexplained intersubject variability has been observed in responsiveness to ozone as measured by lung function, 17,18 and research to identify sources of this variation is needed, especially in the elderly who are especially susceptible to the morbidity and mortality associated with acute ozone exposure. Airway hyperresponsiveness (AHR), a central feature of asthma, is associated with both low levels of lung function and faster longitudinal lung function decline. 19 Asthmatics appear to be a subset of subjects who are at higher risk for the effects of ozone. For example, exacerbations and emergency department visits for asthma have been associated with ozone exposure. 20,21 It appears that adverse effects of ozone in asthmatics are mediated by effects of ozone on airway inflammation 22 and subsequent AHR. 23 The role of obesity in responsiveness to ozone has not previously been studied in humans but has been documented in mice. These studies have found that acute ozone exposure results in increased AHR and inflammation in obese mice compared to nonobese control mice, 24 and those effects do not depend on the mode of obesity. 25 These results in mice suggest that obesity may be a modifying factor for the response of humans to acute ozone exposure. In this longitudinal epidemiologic study, we examine two possible modifiers of the effect of acute exposure to ambient ozone on lung function. We hypothesized that obesity and AHR would each modify the effect of ozone on lung function. We also investigated whether there is evidence for interaction between obesity and AHR in modification of lung function response. *From the Department of Environmental Health (Ms. Alexeeff, Dr. Suh, and Dr. Schwartz), Harvard School of Public Health; Channing Laboratory (Dr. Litonjua), Brigham and Women s Hospital, Harvard Medical School; and VA Normative Aging Study (Drs. Sparrow and Vokonas), VA Boston Healthcare System and Department of Medicine, Boston University School of Medicine, Boston, MA. This work was supported by the US Environmental Protection Agency grants R and R and by National Institute of Environmental Health Services grants ES and ES0002. The VA Normative Aging Study is supported by the Cooperative Studies Program/Epidemiology Research and Information Center of the US Department of Veterans Affairs and is a component of the Massachusetts Veterans Epidemiology Research and Information Center, Boston, MA. The authors have no conflicts of interest to disclose. Manuscript received May 11, 2007; revision accepted August 17, Reproduction of this article is prohibited without written permission from the American College of Chest Physicians ( org/misc/reprints.shtml). Correspondence to: Stacey E. Alexeeff, BSc, Exposure, Epidemiology and Risk Program, Harvard School of Public Health, Landmark Center West, 415, 401 Park Dr, Boston, MA 02215; sackerma@hsph.harvard.edu DOI: /chest Study Population Materials and Methods Subjects in this study were part of the Veterans Administration Normative Aging Study, 26 a longitudinal study established in 1963, details of which have been published previously. Briefly, the study enrolled 2,280 men from the Greater Boston area, ages 21 to 80 years, who were determined to be free of known chronic medical conditions by an initial health screening. Participants visited the study center repeatedly to undergo physical examinations, including pulmonary function testing, and fill out questionnaires approximately every 3 years. We included the subset of 904 subjects whose lung function was measured between January 1995 and June 2005 and whose AHR was measured during the same visit or at a prior visit. This study was approved by the Institutional Review Boards of all participating institutions, and informed consent was obtained from all subjects. Study center visits took place in the morning after an overnight fast and abstinence from smoking. Physical examinations included measurement of height, weight, lung function (FVC, FEV 1 ), and methacholine challenge testing. Subjects filled out questionnaires on smoking habits and pulmonary disorders (asthma, chronic bronchitis, emphysema) based on the American Thoracic Society-Division of Lung Diseases-1978 questionnaire. 27 Descriptive statistics for these data are listed in Table 1. Lung Function and AHR Data Pulmonary function and methacholine challenge tests were performed as previously reported. 28 Briefly, measures of FVC and FEV 1 were obtained using a water-filled recording spirometer, and values were adjusted by body temperature and pressure. Spirometric tests were performed in accordance with American Thoracic Society guidelines. Methacholine challenge tests were performed using a procedure adapted from that of Chatham and colleagues. 29 Methacholine inhalations were administered at incremental doses corresponding to 0, 0.330, 1.98, 8.58, 16.8, and 49.8 mol. For our analysis, we defined a positive response to methacholine challenge (AHR) when a subject experienced a 20% decline in FEV 1 following any of the doses at or before 8.58 mol. Subjects whose FEV 1 did not decline by 20% in response to any of the administered doses and subjects who demonstrated a 20% decline in FEV 1 only from a higher methacholine dosage (16.8 or 49.8 mol) were categorized as having no AHR response. Methacholine challenge tests were administered between 1984 and We used data from the most recent methacholine challenge test available for each subject at that visit. Subjects were excluded from methacholine challenge testing for having ischemic heart disease or baseline FEV 1 at 60% of the predicted value, and some subjects elected not to participate. Obesity Data At each visit, height and weight were collected and used to calculate the body mass index (BMI). Obesity was defined as a BMI 30 kg/m 2, consistent with the definition given by the National Institutes of Health. 30 Pollution and Weather Data Four monitoring sites measured ambient ozone continuously, with one monitor located in each of four cities in the Greater Boston area: Boston, Chelsea, Lynn, and Waltham. All monitors conformed to US Environmental Protection Agency standards. In CHEST / 132 / 6/ DECEMBER,

3 Table 1 Descriptive Statistics of Study Population (n 904) at First Visit* Table 2 Pollution and Weather Variables for All Averages Used in Analysis Variables Data Variables Mean SD Age, yr BMI, kg/m Obesity Not obese (BMI 30 kg/m 2 ) 698 (77.2) Obese (BMI 30 kg/m 2 ) 206 (22.8) Ethnic background White 882 (98.2) Black 16 (1.8) Smoking status Never smoker 266 (29.4) Former smoker 578 (63.9) Current smoker 60 (6.6) Lifetime smoking, pack-yr Chronic pulmonary diseases Doctor-confirmed asthma 47 (5.2) Unconfirmed asthma 3 (0.33) Doctor-confirmed chronic 50 (5.5) bronchitis Unconfirmed chronic 3 (0.33) bronchitis Doctor-confirmed emphysema 27 (3.0) Unconfirmed emphysema 1 (0.11) Methacholine challenge test No response to 8.58 mol 788 (87.2) Response to 8.58 mol 116 (12.8) FVC, L FEV 1,L *Data are presented as mean SD or No. (%). Pack-years for former or current smokers. Response defined as a 20% drop in FEV 1. our analyses, we used the average of the measurements from each monitor. Although the ozone measurements spanned 10 years, we did not create long-term averages of ambient ozone because all subjects lived in the same metropolitan area and thus the long-term averages would be the same for each subject. Instead, since subjects visited on different days throughout the year, we calculated short-term averages of the ambient ozone concentration a few days before the visit time of that subject and analyzed the data as a repeated-measures study. Since subjects visited on different days, the short-term exposure to ambient ozone before lung function measurement varied from subject to subject. In a previous study, we examined the effect of ozone on lung function using averages ranging from 1 to 5 days prior to the study visit and found that the 48-h average was most significantly associated with decline in both FVC and FEV 1 (S.E. Alexeeff, BSc; unpublished data; November 2006). Hence, we used the average ozone concentration 48 h prior to the study visit for the analyses of effect modification presented here. We obtained meteorologic data including temperature and relative humidity from the Boston airport weather station. To control for outdoor weather, we used the apparent temperature, defined as a person s perceived air temperature. 31,32 We calculated the average apparent temperature for the 48 h before the study visit to correspond with the 48-h ozone concentration average. Descriptive statistics for apparent temperature and ozone concentration are listed in Table 2. Ozone concentrations had low correlations with particulate matter 2.5 m (0.29), carbon monoxide ( 0.21), and nitrogen dioxide ( 0.15), and hence we believed it was reasonable to Apparent temperature, 2-d mean, C Ozone, 2-d mean, ppb examine ozone alone without adjusting for other pollutants. We have limited data on particle components, but for the days we do have data (approximately one third), ozone correlations were as expected: ozone was not correlated with elemental carbon (0.05) but had a moderate correlation with sulfates (0.45). Statistical Methods Lung function measurements FVC and FEV 1 were logtransformed to increase normality and stabilize variance. We chose the following variables a priori and included them in our model: age, height, race, cigarette smoking (smoking status and pack-years), chronic lung conditions (asthma, emphysema, and chronic bronchitis), season, year of visit, weekday, apparent temperature, and ozone concentration. We measured the FVC and FEV 1 of each subject on up to four visits, with a mean of 2.3 visits per subject. We used a mixed model for our regression analyses to account for the repeated measurements on the same subjects. This type of model allows each subject to act as his/her own control, which accounts for intrasubject variability. Hence, in addition to using the variables listed above to account for factors known to affect lung function, our longitudinal design also allows us to control for unmeasured within-subject variation by using a random intercept for each person. An association between the dependent variable and a covariate was considered to be significant if the covariate had a p value 0.05 in the model. We tested the modification effects of AHR and obesity by using an interaction term with ozone. We report the significance of the interaction term and also the effect estimate (and confidence limit) within each category (eg, obese and not obese). We present the estimated effect of ozone as a percentage change in lung function. Because FVC and FEV 1 were log e -transformed in our model, the percentage changes in FVC and FEV 1 were calculated by [exp( O 3 )-1] 100%, with 95% confidence intervals (CIs) [exp( O 3 [ 1.96 SE]) 1] 100%, where exp(x) is the mathematical constant e ( 2.718) raised to the power of X, O 3 is the change in ozone concentration, is the estimated regression coefficient, and SE is the SE of. For the change in ozone concentration, we used the increment of 15 parts per billion (ppb), which is approximately equal to the interquartile range of the 2-day ozone concentration averages. To test the linearity of the association and the possible existence of a threshold, we reran our mixed-effects model using the mixed-model formulation of a penalized spline for ozone concentration. This allowed us to specify a nonlinear regression spline with up to five degrees of freedom for the ozone dose response. The coefficients representing the nonlinear components of the ozone dose-response curve are treated as random, and estimated using restricted maximum likelihood. 33 Results When we fit the spline model for ozone, the restricted maximum likelihood estimation chose one 1892 Original Research

4 Table 3 Effect of 15-ppb Increase in Ozone by AHR and Obesity Variables Change in FEV 1,% 95% CI Change in FVC, % 95% CI Overall effect of ozone to to 0.70 Effect by AHR Nonresponder 1.28* 2.01 to to 0.61 Responder 3.04* 4.70 to to 0.46 Effect by obesity BMI 30 kg/m * 1.91 to to 0.48 BMI 30 kg/m * 3.85 to to 0.91 *Interaction effect is statistically significant (p 0.05). degree of freedom (linear) as the best-fitting model of spline models with up to five degrees of freedom. That is, the random coefficients representing the deviation from linearity were estimated as zero. This indicates that a linear dose response is the best fit across the range of exposure in our study. To evaluate the modifying effects of AHR, subjects were classified in categories of response and no response for a methacholine dosage 8.58 mol, with a response defined in the Materials and Methods section above. For a 15-ppb increase in ozone, greater decreases in FVC and FEV 1 were estimated for those in the response group compared to the noresponse group (Table 3, Fig 1, 2). This interaction between ozone and AHR was significant for predicting FEV 1 (p 0.044) but not significant for FVC. Note that while the CIs for these two groups are overlapping (Fig 1), this effect is indeed significant, and it has been shown in general that an interaction effect can be significant while CIs have some overlap. 34,35 To assess of the effect of obesity as a modifier of response to ozone, we estimated the effect of ozone for the two categories obese and not obese (categories explained above). For a 15-ppb increase in ozone, the obese were estimated to have greater drops in both FVC and FEV 1 than the nonobese (Table 3, Fig 1, 2). This interaction between ozone and obesity was significant when predicting FEV 1 (p 0.022) but not significant for FVC. We also investigated the combined effect of obesity with AHR by separating the cohort into four classes (class 1A, not obese with no AHR; class 1B, not obese with AHR; class 2A, obese with no AHR; and class 2B, obese with AHR). Results are listed in Table 3 and shown in Figures 1, 2. For both FVC and FEV 1, the estimated decrease in lung function associated with ozone exposure was greater in classes 1B and 2A than in class 1A, with the most severe estimates given for class 2B. The results of the interaction model suggested a trend where the effects increased in magnitude across classes 1A through 2B, so we performed a trend test. We were interested in testing the hypothesis that the effect of obesity and AHR would have a % change in FEV A B 1,A 1,B 2,A 2,B All by obesity a by AHR a by obesity-ahr interaction a 1: not obese 2: obese A: no airways hyperresponsiveness B: has airways hyperresponsiveness a Interaction effect is statistically significant, p-value < Figure 1. Percentage change in FEV 1 per 15-ppb increase in ambient ozone, by obesity and AHR. CHEST / 132 / 6/ DECEMBER,

5 % change in FVC A B 1,A 1,B 2,A 2,B All by obesity by AHR by obesity-ahr interaction 1: not obese 2: obese A: no airways hyperresponsiveness B: has airways hyperresponsiveness Figure 2. Percentage change in FVC per 15-ppb increase in ambient ozone, by obesity and AHR. more than additive effect. Because we had no prior hypothesis as to whether obesity or AHR would result in a greater effect modification for ozone, we defined our trend variable as the interaction of a 1,2 variable for obesity with a 1,2 variable for AHR. Our resulting nonlinear trend was 1,2,4, where the presence of either risk factor alone was coded 2. The trend was significant for both FVC (p 0.048) and FEV 1 (p 0.001). Discussion Our analyses support our hypothesis that obesity and AHR each modify the effect of ozone on lung function. We found that a greater lung function decline in response to acute ozone exposure is predicted for those who are obese compared to the nonobese, and for those with AHR compared to those without AHR. In addition, we found evidence of an interaction between AHR and obesity that also modifies the decrease in lung function from ozone exposure. We also found that the response to ozone appears to be linear for the range of exposures in our study, indicating the presence of a response at lower exposure levels. Obesity has not been studied in humans as a modifier of the effect of responsiveness to ozone. However, our results are consistent with studies 24,25 of mice, which have found that responses to ozone (inflammation and increased AHR) were greater in obese mice compared to nonobese control mice. Our findings showing greater decreases in lung function in obese humans compared to the nonobese lend further evidence to indicate that obesity is an important factor in responsiveness to ozone. Our results showing greater decreases in lung function in those with AHR are consistent with the findings of increased responsiveness to ozone in those with asthma. Asthmatics have been shown to exhibit greater declines in lung function in response to ozone than nonasthmatics. 36 Responsiveness to ozone as measured by inflammatory markers has also been shown to be increased in asthmatics compared to those without asthma. 37 In our examination of obesity together with AHR, our findings suggest that obesity and AHR interact. This interaction seems reasonable considering that other studies have linked obesity to AHR and asthma. We previously identified a relationship between obesity and AHR, including a finding that those with a high BMI ( 29.4 kg/m 2 ) were associated with the development of AHR. 38 Additionally, a large body of epidemiologic data, including both cross-sectional and prospective studies, 39,40 suggests that obesity is a risk factor for asthma. Thus, the many studies that have found associations between obesity and AHR or between obesity and asthma lend support to our hypothesis that AHR and obesity may interact in modifying a person s response to ozone. A possible mechanism to explain our findings of the effects of obesity and AHR in ozone responsiveness involves lung inflammation, which is widely known to be an effect of ozone. How closely ozone-induced decline in lung function is related to this inflammation is still unknown. Some controlled studies 41,42 examining the effects of ozone found both increased levels inflammation and decrements in FVC and/or FEV 1 after exposure, but found no correlation between the magnitudes of these responses. However, fibrinogen 1894 Original Research

6 concentration has been correlated with the magnitudes of decrements in forced expiratory flow, midexpiratory range. 43 Inflammation, as measured by blood eosinophil count, has been associated with responsiveness to methacholine in this cohort. 44 Airway inflammation is thought to play a key role in the development of asthma, 45 and the inflammatory response to acute ozone exposure has been shown to be increased in asthmatics compared to normal subjects. 37 Also, systemic inflammation is strongly associated with obesity in both children and adults. 46 Since AHR and obesity are both associated with increased inflammation, we suspect that those with either trait are more likely to be susceptible to the inflammatory effects of ozone, leading to lower FVC and FEV 1. Additionally, it seems plausible that those who have both obesity and AHR experience further increased inflammation, and therefore are even more prone to the effects of ozone, which would explain the interaction seen in our results. In addition to inflammatory responses, other mechanisms have been identified that could explain the link between obesity and asthma, including mechanical factors like the stretching of muscles in the airway and levels of various adipokines (proteins synthesized and released from adipose tissue), including hormones involved in antiinflammatory responses and energy regulation. 47 Given the mounting evidence of a relationship between obesity and asthma, our finding that obesity and AHR appear to interact in response to ozone seems reasonable. In terms of our finding that the size of the interaction between AHR and obesity appears to be more than additive, it is not clear which of the possible mechanisms is most likely responsible. We considered whether obesity may simply be a marker for more severe cases of AHR. After comparing the methacholine dose-response slopes for the obese and not obese who had AHR, we found no difference between the slopes (results not shown). Thus, we believe that obesity is not simply a marker for extreme AHR and is instead having some other effect that is interacting with AHR. As the mechanisms linking obesity to asthma and AHR are further investigated, reason for a greater than additive effect of these factors may be identified. Our analysis of the linearity of the response to ozone indicates that there is no evidence of threshold across the range of exposures in our study. We cannot exclude the possibility of a threshold at lower concentration, but since the tenth percentile of 2-day ozone concentration was only 11 ppb, we expect that any threshold would exist only at a very low exposure level. In addition, the US standard of 80 ppb for an 8-h peak average was exceeded on only 23 days (2.3% of total days used in our study). In conjunction with the evidence of the linearity of the response to ozone, this suggests that the elderly experience acute lung function decrements in response to exposure levels below the US standard. A limitation of this study is that the study population consists of only elderly men, most of whom are white. These results cannot easily be extrapolated across age or gender because ozone responsiveness as measured by lung function varies with age and possibly also with gender. 12 Also, lung function is known to vary with race, 48,49 and lung function response to ozone may also vary with race. 50 Given these differences in responsiveness, we cannot predict the degree to which these factors might modify the response to ozone in other populations. We do suspect, however, that obesity and AHR modify the effect of ozone response in other populations at some level, and this points to an important area for future research. Our study is also limited by relying on ambient exposure without accounting for individual exposure using activity patterns. While the lack of activity pattern data in our study is a concern, we have no reason to believe this could upwardly bias our effect, and the likely direction of the bias is downward. 51 Still, small studies 52,53 of personal exposure have demonstrated moderate to low associations between ambient ozone levels and personal ozone exposure and some correlation with personal exposure to other products of photochemistry, including particulates, with effects varying by season. The only copollutant with a moderate correlation to ozone was sulfate, so we do not know whether some of the effect seen could be attributed to a combination of ozone and sulfates. Additional research is needed to address the association of personal exposure to ozone and other pollutants with pulmonary responses in large longitudinal studies. Table 4 Effect of 15-ppb Increase in Ozone by Interaction Between AHR and Obesity Variables % Change in FEV 1 95% CI % Change in FVC 95% CI Not obese, no AHR to to 0.23 Not obese, has AHR to to 0.49 Obese, no AHR to to 1.01 Obese, has AHR to to CHEST / 132 / 6/ DECEMBER,

7 This study provides evidence of modification of the lung function response to acute ozone exposure in the elderly by both obesity and AHR. The evidence for a possible interaction between obesity and AHR that modifies ozone response suggests the importance of examining combinations of risk factors to help explain the intersubject variability in responsiveness to ozone. ACKNOWLEDGMENT: We thank Elaine R. Dibbs, Shelly Amberg, and Jordan Awerbach for their invaluable contributions to the Veterans Administration Normative Aging Study. References 1 Gouveia N, Fletcher T. Time series analysis of air pollution and mortality: effects by cause, age and socioeconomic status. J Epidemiol Commun Health 2000; 54: Levy JI, Chemerynski SM, Sarnat JA. Ozone exposure and mortality: an empiric Bayes metaregression analysis. Epidemiology 2005; 16: Schwartz J. How sensitive is the association between ozone and daily deaths to control for temperature? 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8 36 Kreit JW, Gross KB, Moore TB, et al. Ozone-induced changes in pulmonary function and bronchial responsiveness in asthmatics. J Appl Physiol 1989; 66: Scannell C, Chen L, Aris RM, et al. Greater ozone-induced inflammatory responses in subjects with asthma. Am J Respir Crit Care Med 1996; 154: Litonjua AA, Sparrow D, Celedon JC, et al. Association of body mass index and the development of methacholine airway hyperresponsiveness in men: the Normative Aging Study. Thorax 2002; 57: Shore SA, Johnston RA. Obesity and asthma. Pharmacol Ther 2006; 110: von Mutius E, Schwartz J, Neas LM, et al. Relation of body mass index to asthma and atopy in children: the National Health and Nutrition Examination Study III. Thorax 2001; 56: Balmes JR, Chen LL, Scannell C, et al. Ozone-induced decrements in FEV 1 and FVC do not correlate with measures of inflammation. Am J Respir Crit Care Med 1996; 153: Schelegle E, Siefkin A, McDonald R. Time course of ozoneinduced neutrophilia in normal humans. Am Rev Respir Dis 1991; 143: Weinmann GG, Liu MC, Proud D, et al. Ozone exposure in humans: inflammatory, small and peripheral airway responses. Am J Respir Crit Care Med 1995; 152: O Connor GT, Sparrow D, Segal MR, et al. Smoking, atopy, and methacholine airway responsiveness among middle-aged and elderly men: the Normative Aging Study. Am Rev Respir Dis 1989; 140: Jarjour NN, Kelly EA. Pathogenesis of asthma. Med Clin North Am 2002; 86: Schwarzenberg SJ, Sinaiko AR. Obesity and inflammation in children. Paediatr Respir Rev 2006; 7: Shore SA. Obesity and asthma: lessons from animal models. J Appl Physiol 2007; 102: Rossiter CE, Weill H. Ethnic differences in lung function: evidence for proportional differences. Int J Epidemiol 1974; 3: Korotzer B, Ong S, Hansen JE. Ethnic differences in pulmonary function in healthy nonsmoking Asian-Americans and European-Americans. Am J Respir Crit Care Med 2000; 161: McDonnell WF, Seal E Jr. Relationships between lung function and physical characteristics in young adult black and white males and females. Eur Respir J 1991; 4: Zeger SL, Thomas D, Dominici F, et al. Exposure measurement error in time-series studies of air pollution: concepts and consequences. Environ Health Perspect 2000; 108: Lee K, Parkhurst WJ, Xue J, et al. Outdoor/indoor/personal ozone exposures of children in Nashville, Tennessee. J Air Waste Manag Assoc 2004; 54: Sarnat JA, Brown KW, Schwartz J, et al. Ambient gas concentrations and personal particulate matter exposures: implications for studying the health effects of particles. Epidemiology 2005; 16: CHEST / 132 / 6/ DECEMBER,

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