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First published online on May 2, 2007
Chest, doi:10.1378/chest.07-0038
doi:10.1378/chest.07-0038
(Chest. 2007; 132:238-245)
© 2007 American College of Chest Physicians
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Low Dietary Nutrient Intakes and Respiratory Health in Adolescents*

Jane S. Burns, ScD; Douglas W. Dockery, ScD; Lucas M. Neas, ScD; Joel Schwartz, PhD; Brent A. Coull, PhD; Mark Raizenne, ScD and Frank E. Speizer, MD

* From the Departments of Environmental Health (Dr. Burns and Dockery), Epidemiology (Dr. Schwartz), and Biostatistics (Dr. Coull), Harvard School of Public Health, Boston, MA; Channing Laboratory (Dr. Speizer), Brigham and Women’s Hospital & Harvard Medical School, Boston, MA; National Health and Environmental Effects Research Laboratory (Dr. Neas), U.S. Environmental Protection Agency; and Safe Environments (Dr. Raizenne), Health Canada, Ottawa, ON, Canada.

Correspondence to: Jane S. Burns, ScD, Harvard School of Public Health, Bldg 1, Fourteenth Floor, 665 Huntington Ave, Boston, MA 02115; e-mail: jburns{at}hsph.harvard.edu

Abstract

Background: Epidemiologic studies have indicated that a diet rich in fruit, antioxidants, and n-3 fatty acids may contribute to optimal respiratory health. We investigated whether low dietary nutrient intakes were associated with lower pulmonary function and higher reporting of respiratory symptoms in adolescents.

Methods: We examined the association of dietary factors (fruit, vegetables, vitamins C and E, beta-carotene, retinol, n-3 fatty acids) with respiratory health in a cohort of 2,112 twelfth-grade students in 13 communities in the United States and Canada during the 1998 to 1999 school year. We assessed the associations between dietary factors and pulmonary function with linear mixed models, and respiratory symptoms with logistic regression using a generalized estimating equation adjusted for individual and group-level covariates.

Results: Low dietary fruit intake was associated with lower FEV1 (– 1.3% of predicted; 95% confidence interval [CI], – 2.4 to – 0.2% of predicted), and increased odds of chronic bronchitic symptoms (odds ratio [OR], 1.36; 95% CI, 1.03 to 1.73) compared with higher intake. Low dietary n-3 fatty acids intake was associated with increased odds of chronic bronchitic symptoms (OR, 1.37; 95% confidence interval [CI], 1.05 to 1.81), wheeze (OR, 1.34; 95% CI, 1.06 to 1.69), and asthma (OR, 1.68; 95% CI, 1.18 to 2.39) compared with higher intake. Smokers with lower dietary vitamin C intake had higher ORs of respiratory symptoms compared with smokers who had higher intake.

Conclusions: Adolescents with the lowest dietary intakes of antioxidant and antiinflammatory micronutrients had lower pulmonary function and increased respiratory symptoms, especially among smokers, suggesting that adequate dietary intake may promote respiratory health and lessen the effects of oxidative stress.

Key Words: adolescents • antioxidants • asthma • diet • n-3 fatty acids • pulmonary function • smoking

The effects of diet on respiratory health have been the subject of laboratory studies,1 observational epidemiologic studies,23 and randomized trials.4 Dietary intake of fruit, ascorbic acid (vitamin C), {alpha}-tocopherol (vitamin E), and beta-carotene have been positively associated with levels of FVC, FEV1, and forced expiratory flow, midexpiratory range (FEF25% - 75%) in adults.567 Cough, wheeze, and asthma in adults have also been associated with low dietary intake of fruit, vegetables, antioxidants, and n-3 fatty acids.891011 Several studies121314 have assessed the effects of diet on respiratory health in children, but few have focused on adolescents.

The protective effects of fruit, antioxidants, and other micronutrients may be mediated primarily in the respiratory tract lining fluid and cells.1 Antioxidant vitamins C and E in the respiratory tract are thought to prevent or limit the inflammatory response by reducing reactive oxygen species and inhibiting lipid peroxidation. Beta-carotene may perform a similar function.15 The antiinflammatory effects of n-3 fatty acids may be due to their integration into the cell membranes of the respiratory epithelium, and modulation of the inflammatory cascade.16

Adolescence is a period of rapid physical growth, yet adolescents often have poor dietary habits.17 Micronutrients, such as antioxidants, aid in lung growth and defenses18; consequently, low dietary intake may result in lower attained lung function and increased respiratory symptoms. We examined the associations of low dietary nutrient intakes with low pulmonary function and respiratory symptoms in a cohort of adolescents, the Teen Lung Study.

Materials and Methods

Study Population
Twelfth-grade students in 13 communities in the United States (Oak Ridge, TN; Blacksburg, VA; Charlottesville, VA; Zanesville, OH; Uniontown, PA; State College, PA; Elkins, WV; Monterey, CA; Aberdeen, SD) and Canada (Leamington, ON; Egbert, ON; Yorktown, SK; Penticton, BC) were recruited and tested during the 1998 to 1999 school year. Dietary questionnaires were not distributed in Penticton, BC, which limited the dietary analyses to 12 communities.

Parental permission and student consent were secured. The Harvard School of Public Health Human Subjects Committee and local research committees, where they existed, approved the study.

Respiratory Questionnaire and Lung Function
Students completed a standardized respiratory questionnaire patterned after the American Thoracic Society-Division of Lung Diseases questionnaire,19 with additional questions on race, personal and household members’ tobacco smoking, and household characteristics. Respiratory symptoms included chronic bronchitic symptoms (cough or phlegm for 3 consecutive months a year, or physician diagnosis of chronic bronchitis), attacks of bronchitis (physician diagnosis), wheeze (wheeze without cold or with exertion and shortness of breath), and asthma (current asthma with physician diagnosis).

A single team of technicians administered a forced expiratory test according to American Thoracic Society methods,20 using a rolling-seal spirometer (Spiroflow; PK Morgan; Andover, MA). Each spirometer was calibrated daily using a 3-L syringe and audited annually. Pulmonary function measurements were corrected to body temperature and pressure saturated with water. Low FVC was defined as observed FVC < 85% of predicted, which was estimated by a log-linear model that included log weight, log height, sex, sex and log height interaction, race, and age.

Height and weight were recorded in stocking feet. Overweight was defined as body mass index ≥ 25 kg/m2.21 Before testing, each student was asked a series of questions regarding present respiratory health, asthma and medication use, smoking habits, and recent exercise.

Dietary Questionnaire
Each student completed a semiquantitative food frequency questionnaire designed for adolescent populations.22 Vitamin supplements were included in the total dietary intake. We focused on dietary intake of antioxidant foods (fruit, vegetables) and micronutrients (vitamins C and E and beta-carotene), as well as nutrients with effects on cell function and inflammatory processes (retinol and n-3 fatty acids).

Statistical Analysis
We examined the associations of dietary intakes with pulmonary function using linear mixed models regressing the FEV1/FVC ratio and the natural log of FVC, FEV1, and FEF25–75% against log weight, sex, log height, sex and log height interaction, city, race, age, overweight, current smoking (one or more cigarettes daily), and household smokers. City was treated as a random effect, and other covariates were treated as fixed effects.23

We examined the associations of dietary intakes with FVC < 85% predicted and respiratory symptoms in a marginal logistic regression model for clustered observations, fit via generalized estimating equations,24 assuming an exchangeable correlation structure among subjects within the same city. We adjusted for sex, race, age, overweight, current smoking, household smokers, and mold in the home.

The nutrients were adjusted for caloric intake using the residual method.25 Since the focus of this article is the effect of low dietary nutrient intakes, nutrients were dichotomized into the lowest quintile compared with the upper four quintiles combined. As a sensitivity analysis, we also examined effects by quintile, to see if a dose response was evident through higher levels of intake. We examined potential modification of the smoking and respiratory outcomes associations using nutrient by smoking status interaction terms in the regression models. Significance was evaluated by the Wald test at the 0.05 level. All analyses were performed using statistical software (SAS, version 9.1; SAS Institute; Cary, NC).

Results

Sample Characteristics
There were 5,413 adolescents who were eligible to participate, 4,355 of whom (80%) completed respiratory questionnaires (Fig 1 ). We excluded adolescents who reported a history of a chest operation, heart disease, or a debilitating health condition that limited their physical activity (n = 64), those with age outside the range of 16 to 19 years (n = 22), and those missing information on covariates of interest (n = 280), leaving 3,989 adolescents. Among these respiratory questionnaire respondents, 3,063 subjects (77%) attempted pulmonary function testing. Dietary questionnaires were distributed during pulmonary function testing, except in Penticton, BC (n = 277). We excluded adolescents who were > 19 years old (n = 6) at pulmonary function testing (up to 5 months after questionnaire), were missing height or weight measurements (n = 8), had height or weight > 3 SDs from the sex-specific mean (n = 70), or had fewer than two acceptable pulmonary function test results (n = 157). Among the remaining 2,545 adolescents, the dietary questionnaire response rate was 84%. We excluded adolescents with a reported caloric intake < 500 or > 5,000 calories (n = 22), leaving 2,112 adolescents in the dietary analysis.


Figure 1
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  		Figure 1. Attrition of the Teen Lung Study cohort. *Extremes of height and weight defined as > 3 SD from the sex-specific means. {dagger}Extremes of calories defined as self-reported intake < 500 or > 5,000 calories.

 
The majority of eligible adolescents were white, a third were overweight, and approximately one tenth consumed daily multivitamins (Table 1 ). The majority of adolescents (72%) did not consume multivitamins. Nearly a fourth of the adolescents reported daily smoking (Table 1), with no difference between genders.


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  		Table 1. Descriptive Characteristics (n = 2,112)*

 
Diet
Dietary fruit and vegetables, vitamin E,26 vitamin A,27 beta-carotene,26 and n-3 fatty acid28 intakes were below the recommended levels (Table 2 ) for a third or more of the students. However, dietary vitamin C intake was below the dietary reference intake (DRI)26 for < 20% of students (Table 2).


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  		Table 2. Self-Reported Dietary Intake of Fruits, Vegetables, Vitamins, and n-3 Fatty Acids (n = 2,112)*

 
Most of the nutrients were moderately correlated (Table 3 ). Among the antioxidants, beta-carotene had the highest correlations with vegetables and fruit. Vitamin C was moderately correlated with fruit intake. The highest dietary contribution to vitamin C in this cohort was from vitamin C fortified drinks. n-3 fatty acids had weak, positive correlations with the other nutrients.


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  		Table 3. Correlations Between Fruit, Vegetables, Vitamins, and n-3 Fatty Acids (n = 2,112)*

 
Diet and Pulmonary Function
Low fruit intake (< 0.25 serving a day) was associated with lower FEV1 (Table 4 ) compared with higher intake. Low fruit intake was not associated with FVC or FVC < 85% predicted. When vegetable and fruit intakes were modeled simultaneously, the estimates of effect did not change.


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  		Table 4. Adjusted Mean Pulmonary Function; Lowest Quintile vs Moderate Dietary Intake (n = 2,112)*

 
Lower dietary calorie-adjusted vitamin C intake (< 85 mg/d) was associated with lower FVC and FEV1 compared with higher intake (Table 4). Lower vitamin C was also associated with an increased odds of FVC < 85% predicted (odds ratio [OR], 1.63; 95% confidence interval [CI], 1.05 to 2.50; p = 0.03). There were no associations between FVC < 85% of predicted with other nutrients. Including other correlated antioxidant micronutrients did not change the estimates of effect. There were no associations between nutrients and the FEV1/FVC ratio (data not shown).

Diet and Respiratory Symptoms
Low dietary fruit intake (< 0.25 serving per day) was associated with increased odds of reported chronic bronchitic symptoms and asthma (Table 5 ) compared with higher intake. Low dietary vitamin E intake (< 5.2 mg/d) was associated with increased odds of reported asthma (Table 5) compared with higher intake. Low dietary n-3 fatty acids intake (< 22 mg/d) was associated with increased odds of reported chronic bronchitic symptoms, wheeze, and asthma (Table 5) compared with higher intake.


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  		Table 5. Prevalence of Respiratory Outcomes by Lowest Quintile vs Moderate Dietary Intake (n = 2,112)

 
Dietary Modification of Smoking Effect
The antioxidant vitamins C and E modified the association of smoking with chronic bronchitic symptoms (Fig 2 ). The ORs associated with smoking and chronic bronchitic symptoms were greater among adolescents with the lowest quintiles of dietary intakes of vitamins C (OR, 5.60; 95% CI, 3.32 to 9.55 vs OR, 3.80; 95% CI, 2.87 to 5.08) and E (OR, 5.40; 95% CI, 3.15 to 9.26 vs OR, 3.90; 95% CI, 2.92 to 5.16) compared with the upper four quintiles combined. When dietary vitamin C intake was dichotomized at 110 mg/d, the associations between smoking with chronic bronchitic symptoms and wheeze were stronger among those adolescents whose intake was < 110 mg/d compared with those whose intake was ≥ 110 mg/d (Fig 2).


Figure 2
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  		Figure 2. Associations of smoking and respiratory symptoms by dietary intake (n = 2,112); ORs adjusted for city, sex, age, race, overweight, household smokers, and mold in the home. Reference groups were nonsmokers.

 
Discussion

Most of the adolescents in this cohort had dietary intakes of fruit, vegetables, vitamins, and n-3 fatty acids below the recommended levels. Low dietary intakes of fruit, vitamins C and E, and n-3 fatty acids were associated with lower pulmonary function and increased odds of reported respiratory symptoms, especially chronic bronchitic symptoms and wheeze among smokers.

Low dietary fruit intake was associated with lower pulmonary function and higher reported chronic bronchitic symptoms and asthma, consistent with other studies.121329 Fruit is a rich source of vitamin C and flavonoids, which are associated with antioxidant activity and may function synergistically.30 The associations of fruit with both pulmonary function and respiratory symptoms may be a result of a joint protective effect of flavonoids931 and vitamin C on airway and alveolar epithelium.

The lowest quintile of dietary vitamin C intake, although approximating the DRI, was associated with lower pulmonary function compared with higher intake, consistent with a prior study.13 This suggests the current DRI for vitamin C may not be adequate to protect lung function.

Low dietary vitamin E intake was associated with increased odds of reported asthma compared with higher intake. Vitamin E is a lipophilic antioxidant that terminates lipid peroxidation, which may modify the reactivity of the cell membrane.32 Low vitamin E may make the respiratory epithelium more susceptible to oxidative stress, increasing the occurrence of asthma symptoms.33

Low dietary n-3 fatty acids intake was associated with higher reported chronic bronchitic symptoms, wheeze, and asthma. n-3 fatty acids competitively integrates into the cell membrane with linoleic acid (a precursor of arachidonic acid).34 While arachidonic acid may be converted into proinflammatory eicosanoids, n-3 fatty acids may be converted to less inflammatory eicosanoids.35 Intervention trials of n-3 fatty acids supplementation have been associated with lower proinflammatory cytokines.36 Additionally, n-3 fatty acids may modulate signaling molecules and transcription factors, possibly affecting immune function and inhibiting the inflammatory cascade.3738 Several studies121439 have found lower reporting of cough or wheeze associated with higher dietary intake of n-3 fatty acids rich foods, which is consistent with our findings. This suggests that among the adolescents in our cohort, low dietary n-3 fatty acids intake may have higher respiratory symptoms as a response to more circulating proinflammatory eicosanoids.

Smoking reduces plasma antioxidant capacity.40 Higher dietary antioxidant intake may be protective for smokers.41 Results from our study suggest that low dietary antioxidant intake may enhance adolescents’ susceptibility to smoking associated chronic cough, phlegm, and bronchitis.

There were several limitations to our study. A cross-sectional study such as ours cannot establish the temporal relationship between diet and respiratory outcomes. It may be that the critical period for diet’s effect on the respiratory system is during early childhood when there is rapid differentiation and growth. Additionally, preclinical symptoms and disease may affect dietary habits.42 Assessing the associations between low dietary intake and respiratory health by dichotomizing the nutrients at the lowest quintile may not have been optimal for every nutrient. Consequently, we may have missed important associations due to misspecification of exposure. Our results suggest that both diet and smoking are associated with respiratory outcomes, and smokers often consume less fruits and vegetables. Consequently, the observed associations may be partially explained by residual confounding. Diet and respiratory symptoms were collected by questionnaire, and are subject to random misclassification that may have attenuated the associations. Smoking information was collected by self-report, and may be underreported.

There was no measure of socioeconomic status collected in this cohort; consequently, there was no direct adjustment for this confounder. However, the communities were selected to limit within-city and between-city variations in socioeconomic status.43 The communities were midsized, suburban, and rural communities, and excluded urban areas.

Adolescents often have dietary intake of important nutrients below levels recommended for health promotion. This may affect the attainment of optimal lung function. Although the lower pulmonary function associated with lower fruit and vitamin C dietary intakes was not likely to have a functional impact on current respiratory health, it suggests that these adolescents may not attain their potential maximum pulmonary function. Chronic cough and wheeze, which our study suggest are associated with low dietary micronutrient intakes, may lead to airway remodeling with later impairment of adult pulmonary function.4445 These factors may have long-term consequences because lower pulmonary function in adults has been associated with increased morbidity and earlier mortality.46 Dietary intake among the Teen Lung Study adolescents was similar to that among adolescents in the National Health and Nutrition Examination Survey III,47 suggesting that these results may be generalizable to other US adolescents. Vitamin supplement use does not completely alleviate low dietary micronutrient intake since n-3 fatty acids and flavonoids may not be included. Also, there is evidence that suggests a synergistic biological effect of micronutrients that occurs with the consumption of whole foods, such as fruit.30 Prevention of the onset of smoking in this age group is a primary objective. However, promoting fruit and fish consumption in addition to vitamin supplementation may be an important adjunct to ensure the adequate intake of antioxidants and n-3 fatty acids. This may protect respiratory health in rapidly growing adolescents, especially among those who smoke.

Footnotes

Abbreviations: CI = confidence interval; DRI = dietary reference intake; FEF25–75% = forced expiratory flow, midexpiratory range; OR = odds ratio

This work was performed at the Harvard School of Public Health.

This document has been subjected to review by the U.S. Environmental Protection Agency and approved for publication. Approval does not signify that the contents reflect the views of the Agency, nor does mention of trade names or commercial products constitute endorsement or recommendation for use.

The Teen Lung Study was funded by a grant from the National Institute of Environmental Health Sciences (ES08391 and ES00002). The analysis of dietary impacts was supported in part by a contract from Health Canada. Dr. Burns was supported by National Heart, Lung, and Blood Institute training grant HL07427 and National Institute of Environmental Health Sciences training grant 32-ES007 069-25#.

The authors have no commercial or financial interests, or other conflicts of interest related to the substance of this article.

Received for publication January 5, 2007. Accepted for publication March 27, 2007.

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