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ABSTRACT |
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The possibility of a causal relationship is suggested by recent concomitant increases in the prevalence of obesity and asthma. In a general population sample, prevalence and incidence of asthma symptoms, skin tests, and body mass index (BMI) were ascertained at mean ages of 6.3 (n = 688) and 10.9 (n = 600) yr. Lung function, bronchodilator responsiveness, and daily peak flow variability were measured at 11 yr of age. There was no association between BMI at age 6 and wheezing prevalence at any age. Females, but not males, who were overweight or obese at 11 yr of age were more likely to have current wheezing at ages 11 and 13 but not at ages 6 or 8. This effect was strongest among females beginning puberty before the age of 11. Females who became overweight or obese between 6 and 11 yr of age were 7 times more likely to develop new asthma symptoms at age 11 or 13 (p = 0.0002); at age 11 their peak flow variability and bronchodilator responsiveness were significantly more likely to be increased. In females, becoming overweight or obese between 6 and 11 yr of age increases the risk of developing new asthma symptoms and increased bronchial responsiveness during the early adolescent period.
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INTRODUCTION |
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The increasing prevalence of both obesity (1) and asthma (2) are major public health concerns. These increases seem to have occurred concomitantly, which suggests the possibility that they may be causally related in some way. Results of several recent cross-sectional studies do indicate that there is an association between being overweight or obese and the likelihood of having asthma (3, 4). This association however, seems to be much stronger in females than in males (5, 6). Camargo and coworkers (7) have shown that females who gained weight after 18 yr of age were at a significantly increased risk of developing asthma during the 4-yr follow-up period. This has suggested the possibility that female hormones may directly or indirectly be involved in the putative causal pathway that relates obesity to asthma.
We reasoned that, if female hormones do play a decisive role in the association between obesity and asthma, changes in weight status occurring during the prepubertal years could be strong determinants of increased asthma risk. It is now well established that new cases of asthma are particularly frequent among females during the adolescent years (8), and that the male-female prevalence ratio changes from 2:1 during the early school years to parity during puberty (11). Menarche is known to occur earlier in girls who become overweight or obese during the early school years (12, 13) than in those who do not. Although the factors that determine the association between body mass and early menarche are not well understood, it is reasonable to surmise that early activation of the hormone processes responsible for the initiation of puberty is involved. We hypothesized that these same processes could determine an increased incidence of asthma in prepubertal girls who become overweight or obese.
To test this hypothesis, we assessed changes in percentile of body mass index (BMI) occurring between the early school years and early adolescence in both males and females enrolled in a longitudinal study of asthma and allergies in Tucson, Arizona. We related these changes to the incidence of asthma during the school years and to the prevalence of increased peak flow variability and increased bronchodilator responsiveness at 11 yr of age.
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METHODS |
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Children (n = 1,246) participating in a birth cohort enrolled between 1980 and 1984 in the longitudinal Tucson Children's Respiratory Study (14) were included. Parents completed questionnaires when the children were age 6 yr (Yr6: mean age ± SD, 6.3 ± 0.9 yr), 8 yr (Yr8: 8.6 ± 0.7 yr), 11 yr (Yr11: 10.9 ± 0.6 yr), and 13 yr (Yr13: 13.5 ± 0.6 yr) (15); the questionnaires reported the child's respiratory symptoms (all surveys), start of puberty (Yr13), and exercise (all surveys). Parental data were ascertained through questionnaires after the child's birth.
Mutually exclusive categories of "infrequent wheezing" and "frequent wheezing" (
3 and > 3 wheezing episodes during the previous year, respectively) were defined for each survey. Children wheezing at
11 or 13 yr of age were further classified as "persistent" if they
wheezed at age 6 and "incident" if they did not. Analyses using these
groups removed persistent cases from the denominator for assessing
incident cases, and vice versa.
At Yr6 and Yr11 beam balance scales were used to measure
weight (Heath-o-meter; Continental Scale Corp., Chicago, IL); height was measured with the subject barefoot and erect against a vertical backboard or wall-mounted scale (Accustat-Stadiometer; Genentech, San Francisco, CA). BMI [weight (kg) divided by the square of height
(m)] percentile was calculated for each child using current U.S. sex
and age standardized values for children (16). Children < 85th percentile were "non-overweight",
85th to < 95th percentile were
"overweight", and
95th percentile were "obese."
Children with
1 positive reaction (wheal size minus control
value of
3 mm) to skin-prick tests were considered positive. Allergens used at Yr6 were house dust, Bermuda grass, olive, careless weed, Alternaria alternata, mesquite, and mulberry (Holister-Stier Laboratories, Everett, Washington, DC); Dermatophagoides farinae and cat dander were added at Yr11.
Children were trained at Yr11 to record peak expiratory flow
(PEF) three times daily for 1 wk using a home peak flow meter. Only
children who recorded PEF measurements at least twice a day for
4 d
(n = 548, 44% of total 1,246 enrolled) were included. Positive PEF
variability was defined as an amplitude percent mean value above the
90th percentile of a healthy reference subgroup (17). Bronchodilator
response was assessed at Yr11 using two inhalations (180 µg) of albuterol administered with a metered-dose inhaler and a spacer.
Spirometry was performed before and 15 min after the albuterol dose
using a standardized pneumotachographic method (18). Subjects
whose postbronchodilator percent predicted FEV1 was
15.2%
higher than the prebronchodilator value were considered to have responded to albuterol based on the distribution of change in FEV1 responses in the population (19).
Statistical Analysis
FEV1 values at Yr11 were logarithmically transformed and adjusted for height. Results were standardized to the children's average height (143.2 cm for boys, 144.9 cm for girls) and expressed as geometric means ± 95% confidence intervals (95% CI). Analysis of variance and Duncan's multiple-comparison test were used to compare means, the chi-square distribution to compare proportions (20), and logistic regression to control for potential confounders. Statistical significance was defined by a two-sided alpha level of 0.05.
This study was approved by the Human Subjects Committee of the University of Arizona, and informed consent was obtained from parents.
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RESULTS |
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Population
Of the 1,246 children originally included in the study, 688 (55.2%) and 600 (48.2%) had anthropometric measurements at the Yr6 and Yr11 surveys, respectively. Among 349 males 84.2% were classified as nonoverweight, 10.3% as overweight, and 5.4% as obese at Yr6; at Yr11 among 300 males, the proportions were 78.7%, 14.7%, and 6.7%, respectively. At Yr6, among 339 females, 76.7% were classified as nonoverweight, 15.0% as overweight, and 8.3% as obese; at Yr11, among 300 females, the proportions were 80.7%, 10.3%, and 9.0%, respectively. These proportions were significantly different at 6 yr of age only (p = 0.04).
There were no differences between those children who had measurements of BMI at Yr6 and Yr11 and those without measurements in terms of wheezing prevalence at any of the four surveys. The only exception was that those children who did not have BMI measurements at Yr6 had a lower prevalence of frequent wheezing at the Yr8 survey than those with BMI measurement (6.0% versus 10.9%, respectively, p = 0.04).
Factors Related to BMI
Among children who had BMI measurements at Yr6 or Yr11,
or at both points, there were 473 (60.9%) with both white parents, 97 (12.5%) with both Hispanic parents, and 207 (26.6%)
with parents of other ethnicities or combinations (white/Hispanic, African-American, Native American, Asian-American).
This distribution was very similar to that for the whole enrolled population (58.8%, 10.8%, 30.4%, respectively). Comparing children with both white parents with those with both
Hispanic parents, no significant ethnic differences in the distribution of BMI categories at Yr6 (p = 0.19) and at Yr11 (p = 0.99) were observed for males. However, females with both
Hispanic parents were significantly more likely to be overweight or obese at Yr6 than females with both white parents
(41.3% versus 20.2%, respectively, p
0.01) and the same was
true at Yr11 (40.0% versus 14.5%, respectively, p < 0.001).
BMI categories at Yr6 and Yr11 showed no significant relation with prenatal maternal smoking, maternal education
level, number of siblings, parental history of physician-diagnosed asthma, and parental history of physician-diagnosed allergic rhinitis, except for a higher prevalence of overweight or
obese subjects at Yr6 among children whose mothers had
12 yr of education compared with those with < 12 yr of education (25.1% versus 17.4%, respectively, p = 0.02); a similar
trend was found for BMI at Yr11 (25.8% versus 18.6%, respectively, p = 0.07).
In addition, methacholine challenge (17) was unrelated to becoming overweight or obese at Yr11, either in the total group (p = 0.31) or for boys (p = 0.90) or girls (p = 0.22) separately. Also, peripheral eosinophil counts (21) were unrelated to becoming overweight or obese at Yr11, either in the total group (p = 0.09) or for boys (p = 0.32) or girls (p = 0.15) separately.
There were no significant differences in reported participation in sport teams or numbers of hours/week of sports practice at the time of Yr6, Yr8, Yr11, and Yr13 by BMI categories
(overweight or obese versus nonoverweight) at Yr6 (all p values were
0.08) and Yr11 (all p values were
0.27).
Asthma and BMI
There was no association between being overweight or obese at Yr6 and the prevalence of frequent (p values 0.43 to 0.85) or infrequent (p values 0.07 to 0.96) wheezing at any of the surveys, or for males (p values 0.32 to 0.99) or females (0.08 to 0.80). However, females who were overweight or obese at Yr11 were more likely to have frequent and infrequent wheezing at Yr11 and Yr13 compared with females who were not overweight at Yr11 (Table 1). Similar trends were observed for males, but these trends did not reach statistical significance (Table 1).
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Eosinophil counts (21) and methacholine challenge (17) results were used to characterize the wheezing symptoms. Higher eosinophil counts were significantly related to frequent and infrequent wheezing outcomes at all surveys overall (all p values < 0.002 for eosinophils) and in boys, and showed similar trends but fewer surveys statistically significant in girls. A statistically significant response to methacholine challenge was seen overall for Surveys 8, 10, and 13 for frequent wheeze, and all surveys for infrequent wheeze. Boys with frequent wheeze showed a statistically significant response to methacholine at Surveys 10 and 13, and at all surveys for infrequent wheeze. In contrast, girls, while showing similar trends to boys, only reached statistical significance for Survey 8 for frequent wheeze and Survey 10 for infrequent wheeze. It is of note that the methacholine challenge test was performed at mean age 11 yr, and was not performed for children who had required asthma treatment in the last 3 mo. Eosinophil counts were performed at a mean age of 7 yr.
Puberty
At the time of the Yr13 survey, 124/708 (17.5%) of the children
evaluated had not yet started puberty according to parental questionnaire responses, 57 (8%) started puberty before age 11, and 527 (74.4%) started puberty at
11 yr of age. Among females who started puberty before age 11, those who were overweight or obese at Yr11 had a significantly higher prevalence of
infrequent wheezing at Yr11 and at Yr13 than females who
were not overweight or obese (at Yr11: 54.4% versus 13.0%,
p = 0.01, respectively and at Yr13: 80.0% versus 26.1%, p = 0.004, respectively). Similarly, females who were overweight or
obese at Yr11 and who started puberty before 11 yr of age had a
significantly higher prevalence of frequent wheezing at Yr11
and Yr13 than females in the nonoverweight group (at Yr11:
28.6% versus 0.0%, respectively, p = 0.01 and at Yr13: 66.7%
versus 10.5%, respectively, p = 0.005). These differences in
prevalence of wheezing did not occur in those females who
started puberty at
11 yr of age. Stratifying by age of puberty
did not change the results for males reported previously.
Change in BMI and Asthma
Children were also classified into three groups according to change in BMI status from Yr6 to Yr11: those whose BMI status remained stable (n = 416), those whose BMI status changed from nonoverweight to overweight or from overweight to obese (n = 57), and those whose BMI status changed from overweight to nonoverweight or from obese to overweight (n = 38). In order to have sufficient subjects for comparisons, we combined all children who did not become overweight or obese (first and last category described earlier) into a single group. Females who became overweight or obese had a higher prevalence of infrequent and frequent wheeze at Yr11 and of frequent wheeze at Yr13 compared with females who did not become overweight or obese (Table 2). Conversely, males who became overweight or obese had similar prevalence of infrequent and frequent wheezing at all surveys compared with males who did not become overweight or obese (Table 2).
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New and Persistent Asthma Symptoms
Table 3 shows that most of the association between changes in BMI status and asthma symptoms was due to new cases. Females who became overweight or obese between Yr6 and Yr11 were between 5.5 and 6.8 times more likely to develop new asthma symptoms at Yr11 or Yr13 compared with females who did not become overweight or obese during that same time interval. Similar trends were observed after stratifying by ethnicity. Thus, in those with both white parents 80% of girls with weight gain between 6 and 11 yr of age have new wheeze (infrequent wheeze) whereas only 15.8% of those without weight gain have new wheeze (p = 0.001). In those with at least one Hispanic parent the equivalent percentages are 40% versus 17% with a borderline p value of 0.08. Repeating this analysis using new cases of asthma at Yr13 only, confirmed that new weight gain between ages 6 and 11 yr was associated with new asthma symptoms (infrequent wheeze) at age 13 yr with an odds ratio (OR) of 8.7 (95% CI 1.8 to 42.4), p = 0.0002. There were insufficient new cases of frequent wheeze to analyze at the age 13 survey.
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Skin-prick Tests
Among females, a trend was observed for an association between change in BMI status and the prevalence of at least one positive skin test to local allergens at Yr6: 54.2% of females who became overweight or obese were skin-test-positive at Yr6 compared with 35.9% of females who did not become overweight or obese, p = 0.08. No such trend was observed among males (51.5% versus 48.0%, p = 0.7). There was no relation between changes in BMI status and the prevalence of at least one positive skin test to local allergens at Yr11 for either sex (data not shown).
PEF Variability and Bronchodilator Responsiveness
Females who became overweight or obese between Yr6 and
Yr11 had a significantly higher prevalence of positive PEF
variability compared with females who did not become overweight or obese in that same time interval (Table 4). Similarly,
females who became overweight or obese between Yr6 and
Yr11 were significantly more likely to show positive responses
to albuterol (based on a cut point of
15.2 change in percent
of predicted FEV1 after administration of albuterol) than
those who did not become overweight or obese during the
same time interval (Table 4). No association was observed between either peak flow variability or response to albuterol and
changes in BMI status among males.
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Table 5 shows height-adjusted, prebronchodilator and postbronchodilator FEV1 values at age 11 for children who became or who did not become overweight or obese between Yr6 and Yr11. No differences in FEV1 by BMI status were observed among males. Conversely, females who became overweight or obese had significantly higher postbronchodilator FEV1 compared with females who did not become overweight or obese.
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DISCUSSION |
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We found that girls who became overweight between 6 and 11 yr of age were between 5.5 and 7 times more likely to develop
new asthma symptoms at the ages of 11 and 13 compared with
girls who did not become overweight or obese between ages 6 and 11. Girls who became overweight or obese in this same age
interval were significantly more likely to have increased daily
peak flow variability and to show
2-adrenergic responsiveness
than girls whose BMI status remained unchanged or decreased. No significant increased risk of having asthma symptoms, increased peak flow variability, or increased responsiveness to
2-adrenergic agonist was observed among males who
became overweight or obese between the ages of 6 and 11.
Our longitudinal data are in agreement with recent cross-sectional studies showing a strong association between overweight status and asthma prevalence in females but not in males. Chen and coworkers (5) in Canada reported that, for all age groups above age 12, overweight and obese women were as much as 1.9 times more likely to have asthma than women who were not overweight. Shaheen and coworkers (3) using the 1970 British cohort study found that overweight and obese women age 26 yr were 1.5 and 1.8 times more likely to have asthma than women who were not overweight. Neither study showed a significant association between BMI status and asthma prevalence in males.
The strong sex differences observed in our study and in those of Chen and coworkers (5) and Shaheen and coworkers (3) argue against the hypothesis that the overweight status can cause asthma directly, because similar effects would be expected in both sexes if this were true. Similarly, our results do not support the idea that asthma, by fostering a more sedentary lifestyle during the school years, may increase the risk of becoming overweight by early adolescence. Moreover, the association between asthma symptoms and changes in BMI status was mainly due to new cases of asthma developing after 6 yr of age and not observed in girls who already had symptoms at that age.
There are two most likely explanations for the pattern of
sex-specific associations that we have observed in this study.
First, it is possible that obesity may influence female sex hormones, and this in turn, alter asthma risk. In support of this
hypothesis, we found that the strongest association between
overweight status and asthma risk was observed among females whose puberty started before the age of 11. Obesity is a
strong risk factor for early onset of puberty and early menarche in females (12, 13). Although the mechanism for this
association has not been clearly established, both increased
peripheral availability of estrone (5) and increased production
of leptin (22) by adipose tissue have been implicated. Female
hormones also alter
2-adrenergic responsiveness (1). Interestingly, we found that, for girls who became overweight or
obese after age 6, height-adjusted, postbronchodilator FEV1 was significantly higher than that of children whose BMI level did not change or decreased after age 6. This observation is
compatible with that of other investigators (23) who have shown
that height-adjusted levels of airway lung function are strongly
correlated with BMI in schoolchildren of both sexes. Serum
leptin concentrations correlate strongly with body fat mass in
humans (22). The recent findings that both airway and lung
cells show proliferative responses when exposed to leptin and
that leptin receptors are present in both types of cells (24)
suggest a potential mechanism for the finding of higher postbronchodilator FEV1 in overweight children. However, in our
population, height-adjusted prebronchodilator FEV1 was not
significantly different between girls who became obese and those whose BMI was stable or decreased, and increased responsiveness to bronchodilators was observed in girls who became overweight or obese during the school years. This suggests the presence of an abnormality in the regulation of
airway tone in these girls. In support of this conclusion, we
found a higher prevalence of daily peak flow variability in girls
who became overweight or obese during the school years as
compared with those whose BMI level did not change or decreased during that same period. It is plausible to surmise that
such differences in the regulation of airway tone may underlie
the increased risk for developing asthma among girls who become overweight or obese during the school years.
A second plausible explanation for our findings is the presence of a subgroup of girls with genetic alterations in female hormone receptor responsiveness. Such abnormalities could determine an increased susceptibility to becoming overweight associated with increased exposure to female hormones during puberty. Some support for this hypothesis comes from our observation that, at the mean age of 6 yr (i.e., at the beginning of the observation period), girls who would become overweight or obese were more likely (albeit only borderline significantly) to be atopic than those whose BMI did not change or decreased. Huang and coworkers (6) recently reported that increased BMI was significantly associated with positive skin test reactivity to local allergens among girls but not among boys from Taiwan. Interestingly, female hormones have been shown to increase the production of interleukin-4 (IL-4) and IL-13 by peripheral blood mononuclear cells (25). These interleukins are known to be the two main T-helper signals needed for the production of IgE (26). Increased susceptibility to allergy in overweight girls may determine increased risk both for persistent asthma and for the abnormalities in the regulation of airway tone associated with it.
Most likely, both genetic and environmental mechanisms may be important in determining the increase in asthma risk that we observed among girls who become overweight and obese. One additional environmental factor that needs to be explored is exercise. Although we found no association between BMI status and reported participation in organized sports, more detailed studies of the role of exercise (or lack thereof) in determining the association between BMI and asthma are warranted.
Our results have important implications for public health. The marked increases in obesity observed during the last 20 yr may in part be causing the increase in asthma prevalence observed concomitantly. Specific interventions aimed at preventing excessive weight gain during the school years, especially in girls, may thus be a valuable tool in preventing asthma-related morbidity during adolescence.
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Footnotes |
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Correspondence and requests for reprints should be addressed to Fernando D. Martinez, M.D., 1501 N. Campbell Avenue, Suite 2349, P.O. Box 245030, Tucson, AZ 85724. E-mail: fernando{at}resp-sci.arizona.edu
(Received in original form June 27, 2000 and in revised form February 2, 2001).
Acknowledgments: The authors thank The Group Health Medical Associates' Personnel: John Bean, Henry Bianchi, John Curtiss, John Ey, Alejandro Sanguineti, Barbara Smith, Terry Vondrak, and Neil West (study pediatricians), and Maureen McLellan, Marilyn Smith, and Lydia De La Ossa (study nurses); Shelley Radford and Bruce Saul for technical help; and Maureen Driscoll for secretarial assistance.
Supported by grants from the National Heart, Lung, and Blood Institute (HL 14136, HL 56177, and HL 03154).
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L. Garcia-Marcos, I. M. Canflanca, J. B. Garrido, A. L.-S. Varela, G. Garcia-Hernandez, F. G. Grima, C. Gonzalez-Diaz, I. Carvajal-Uruena, A. Arnedo-Pena, R. M Busquets-Monge, et al. Relationship of asthma and rhinoconjunctivitis with obesity, exercise and Mediterranean diet in Spanish schoolchildren Thorax, June 1, 2007; 62(6): 503 - 508. [Abstract] [Full Text] [PDF] |
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M. O.M. Van De Ven, R. J.J.M. Van Den Eijnden, and R. C.M.E. Engels Atopic diseases and related risk factors among Dutch adolescents Eur J Public Health, October 1, 2006; 16(5): 549 - 558. [Abstract] [Full Text] [PDF] |
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D. A. Beuther, S. T. Weiss, and E. R. Sutherland Obesity and Asthma Am. J. Respir. Crit. Care Med., July 15, 2006; 174(2): 112 - 119. [Abstract] [Full Text] [PDF] |
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F. L. Lu, R. A. Johnston, L. Flynt, T. A. Theman, R. D. Terry, I. N. Schwartzman, A. Lee, and S. A. Shore Increased pulmonary responses to acute ozone exposure in obese db/db mice Am J Physiol Lung Cell Mol Physiol, May 1, 2006; 290(5): L856 - L865. [Abstract] [Full Text] [PDF] |
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A Sood, E S Ford, and C A Camargo Jr Association between leptin and asthma in adults Thorax, April 1, 2006; 61(4): 300 - 305. [Abstract] [Full Text] [PDF] |
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V Flaherman and G W Rutherford A meta-analysis of the effect of high weight on asthma Arch. Dis. Child., April 1, 2006; 91(4): 334 - 339. [Abstract] [Full Text] [PDF] |
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W. J. Morgan, D. A. Stern, and F. D. Martinez Does Most Asthma Really Begin during the Preschool Years? Am. J. Respir. Crit. Care Med., March 1, 2006; 173(5): 576 - 576. [Full Text] [PDF] |
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G. M. Hunninghake, S. T. Weiss, and J. C. Celedon Asthma in Hispanics Am. J. Respir. Crit. Care Med., January 15, 2006; 173(2): 143 - 163. [Abstract] [Full Text] [PDF] |
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R. A. Johnston, T. A. Theman, and S. A. Shore Augmented responses to ozone in obese carboxypeptidase E-deficient mice Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2006; 290(1): R126 - R133. [Abstract] [Full Text] [PDF] |
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V. J Vieira, A. M Ronan, M. R Windt, and A. R Tagliaferro Elevated atopy in healthy obese women Am. J. Clinical Nutrition, September 1, 2005; 82(3): 504 - 509. [Abstract] [Full Text] [PDF] |
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L. G. Sulit, A. Storfer-Isser, C. L. Rosen, H. L. Kirchner, and S. Redline Associations of Obesity, Sleep-disordered Breathing, and Wheezing in Children Am. J. Respir. Crit. Care Med., March 15, 2005; 171(6): 659 - 664. [Abstract] [Full Text] [PDF] |
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R. J. Hancox, B. J. Milne, R. Poulton, D. R. Taylor, J. M. Greene, C. R. McLachlan, J. O. Cowan, E. M. Flannery, G. P. Herbison, and M. R. Sears Sex Differences in the Relation between Body Mass Index and Asthma and Atopy in a Birth Cohort Am. J. Respir. Crit. Care Med., March 1, 2005; 171(5): 440 - 445. [Abstract] [Full Text] [PDF] |
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R. Varraso, V. Siroux, J. Maccario, I. Pin, F. Kauffmann, and on behalf of the Epidemiological Study on the Gene Asthma Severity Is Associated with Body Mass Index and Early Menarche in Women Am. J. Respir. Crit. Care Med., February 15, 2005; 171(4): 334 - 339. [Abstract] [Full Text] [PDF] |
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E. Ronmark, C. Andersson, L. Nystrom, B. Forsberg, B. Jarvholm, and B. Lundback Obesity increases the risk of incident asthma among adults Eur. Respir. J., February 1, 2005; 25(2): 282 - 288. [Abstract] [Full Text] [PDF] |
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S Chinn Concurrent trends in asthma and obesity Thorax, January 1, 2005; 60(1): 3 - 4. [Full Text] [PDF] |
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K Wickens, D Barry, A Friezema, R Rhodius, N Bone, G Purdie, and J Crane Obesity and asthma in 11-12 year old New Zealand children in 1989 and 2000 Thorax, January 1, 2005; 60(1): 7 - 12. [Abstract] [Full Text] [PDF] |
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E.S. Ford, D.M. Mannino, S.C. Redd, A.H. Mokdad, and J.A. Mott Body mass index and asthma incidence among USA adults Eur. Respir. J., November 1, 2004; 24(5): 740 - 744. [Abstract] [Full Text] [PDF] |
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W. H. Oddy, J. L. Sherriff, N. H. de Klerk, G. E. Kendall, P. D. Sly, L. J. Beilin, K. B. Blake, L. I. Landau, and F. J. Stanley The Relation of Breastfeeding and Body Mass Index to Asthma and Atopy in Children: A Prospective Cohort Study to Age 6 Years Am J Public Health, September 1, 2004; 94(9): 1531 - 1537. [Abstract] [Full Text] [PDF] |
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J. S. Lucas, H. M. Inskip, K. M. Godfrey, C. T. Foreman, J. O. Warner, R. K. Gregson, and J. B. Clough Small Size at Birth and Greater Postnatal Weight Gain: Relationships to Diminished Infant Lung Function Am. J. Respir. Crit. Care Med., September 1, 2004; 170(5): 534 - 540. [Abstract] [Full Text] [PDF] |
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D. R. Gold Less Childhood Obesity--Less Persistence of Wheeze in Teenage Girls and Boys? Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 8 - 9. [Full Text] [PDF] |
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S. Chinn, R. J. Rona, S. T. Weiss, and S. Shore Obesity and Asthma in Children Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 95 - 96. [Full Text] |
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S. Guerra, A. L. Wright, W. J. Morgan, D. L. Sherrill, C. J. Holberg, and F. D. Martinez Persistence of Asthma Symptoms during Adolescence: Role of Obesity and Age at the Onset of Puberty Am. J. Respir. Crit. Care Med., July 1, 2004; 170(1): 78 - 85. [Abstract] [Full Text] [PDF] |
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S. Ten and N. Maclaren Insulin Resistance Syndrome in Children J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2526 - 2539. [Abstract] [Full Text] [PDF] |
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Y. M. Rivera-Sanchez, R. A. Johnston, I. N. Schwartzman, J. Valone, E. S. Silverman, J. J. Fredberg, and S. A. Shore Differential effects of ozone on airway and tissue mechanics in obese mice J Appl Physiol, June 1, 2004; 96(6): 2200 - 2206. [Abstract] [Full Text] [PDF] |
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S. T. Weiss and S. Shore Obesity and Asthma: Directions for Research Am. J. Respir. Crit. Care Med., April 15, 2004; 169(8): 963 - 968. [Full Text] [PDF] |
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K G Tantisira, A A Litonjua, S T Weiss, and A L Fuhlbrigge Association of body mass with pulmonary function in the Childhood Asthma Management Program (CAMP) Thorax, December 1, 2003; 58(12): 1036 - 1041. [Abstract] [Full Text] [PDF] |