Racial Difference in Lung Function in African-American and White Children: Effect of Anthropometric, Socioeconomic, Nutritional, and Environmental Factors

Raida I. Harik-Khan1, Denis C. Muller1 and Robert A. Wise2 

1 Clinical Research Branch, National Institute on Aging, Baltimore, MD.
2 Department of Medicine, School of Medicine, Johns Hopkins University, Baltimore, MD.

Received for publication November 3, 2003; accepted for publication May 26, 2004.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
African-American children have lower lung volumes than White children. However, the contributions of anthropometric, socioeconomic, nutritional, and environmental factors to this difference are unknown. From participants in the Third National Health and Nutrition Examination Survey (1988–1994), the authors selected 1,462 healthy nonsmoking children (623 White and 839 African-American) aged 8–17 years. The African-American children were taller and heavier but had lower lung function. African Americans were poorer and had lower levels of the antioxidant vitamins A and C and {alpha}-carotene. The authors performed regression analyses using data on anthropometric, socioeconomic, and nutritional factors and smoke exposure. Adjustment for sitting height explained 42–53% of the racial difference. Socioeconomic factors and antioxidant vitamin levels accounted for an additional 7–10%. Overall, the authors could account for only 50–63% of the racial difference. Exposure to tobacco in the home was weakly associated with forced expiratory volume in 1 second in girls, accounting for 1% of the difference. In children aged 8–12 years (n = 752), birth weight explained 3–5% of the racial difference, whereas in-utero exposure to maternal smoking had no significant effect. The authors conclude that in healthy children, the major explanatory variable for the racial difference in lung function is body habitus; socioeconomic, nutritional, and environmental confounders play a smaller role.

anthropometry; antioxidants; continental population groups; reference values; respiratory function tests; socioeconomic factors

Abbreviations: Abbreviations: FEV1, forced expiratory volume in 1 second; FVC, forced vital capacity; NHANES III, Third National Health and Nutrition Examination Survey.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A difference in pulmonary function between Whites and African Americans has been found in both children and adults (15). Hsi et al. (2) reported that the racial difference in spirometric lung volume between African-American and White children could be completely accounted for by the smaller trunk:leg ratio of African Americans. However, race is confounded by other factors that are associated with lower lung function, including lower socioeconomic status (6, 7), obesity (8, 9), lower dietary intake of antioxidant vitamins (1013), low birth weight (14, 15), and exposure to tobacco smoke (1618).

Recently, we reported that the use of sitting height instead of standing height in adult data from the Third National Health and Nutrition Examination Survey (NHANES III) reduced the racial difference in lung volume between asymptomatic Whites and African Americans by 35–39 percent (19). Smaller proportions of the racial difference were explained by differences in poverty, education, and body mass index (weight (kg)/height (m)2). Overall, we could account for only half of the racial difference in forced expiratory volume in 1 second (FEV1) and forced vital capacity (FVC).

Poverty, nutrition, and exposure to tobacco smoke may affect lung development. Thus, these factors may be more proximate determinants of lung function in children than in adults. For this reason, we undertook to study factors that might contribute to the racial difference in pulmonary function in children. Using the same nationally representative data set, we attempted to determine whether the racial difference between healthy asymptomatic African-American children and White children could be explained by anthropometric, socioeconomic, nutritional, and/or environmental factors.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study group
The study subjects were children and teenage participants in NHANES III, a survey of the US noninstitutionalized population conducted between 1988 and 1994 by the National Center for Health Statistics. The survey consisted of several questionnaires followed by physical examination and laboratory testing that included spirometry. Details on the survey design and examination procedures have been published by the National Center for Health Statistics (20, 21). In this study, we applied the criteria of Hankinson et al. (5) to select asymptomatic, nonsmoking White or African-American children ranging in age from 8 years to 17 years. Of 4,140 children who performed spirometry, 623 Whites and 839 African Americans met the Hankinson et al. (5) criteria for healthy children and had complete records for the relevant data (spirometric, anthropometric, and socioeconomic factors, smoking, and serum levels of antioxidant vitamins). To investigate the effect of low birth weight and maternal smoking on lung function in general and on the racial difference in FEV1 and FVC specifically, we analyzed younger subsets of girls and boys (383 girls and 369 boys) with available information on birth weight. The children in these subsets ranged in age from 8 years to 12 years.

Spirometry
Spirometric measurements were obtained as previously described (5, 21). In this study, we analyzed data from sessions in which at least two acceptable maneuvers had been performed. We used the reference equations derived by Hankinson et al. (5) to calculate the predicted values for spirometric indices.

Statistical analyses
Cross-sectional analysis of the data was conducted with SAS software (SAS Institute, Inc., Cary, North Carolina). Multivariable regression analysis was performed separately by gender, with FEV1 or FVC as the dependent variable. Independent variables included age, sitting or standing height, race, educational level of the family head, and poverty index. The poverty index is defined as the ratio of family income in the past 12 months to the federal poverty line, such that a higher poverty index is indicative of a higher socioeconomic status. To test the effects of environmental tobacco smoke exposure and serum antioxidant levels, we added separately to the above regression model each of the following variables: tobacco smoke exposure at home (1 = the presence of at least one cigarette smoker in the household; 0 = no smokers in the household) and serum concentrations of vitamins A, C, and E and {alpha}- and ß-carotene. We also included terms for the interactions between education of the family head and race and between poverty index and race, in order to assess whether socioeconomic variables affected African Americans differently from Whites. To explore the effect on lung function of birth weight and maternal smoking during pregnancy, we performed regression analyses in the younger subsets of the study population for children with complete information on these variables. We applied Student’s t test by gender to check the significance of the racial difference in potentially explanatory variables between African Americans and Whites. Regression coefficients and the results of t tests were considered significant at p = 0.05. Reduction in the racial difference was calculated as 1 – (adjusted {Delta}/SH-adjusted {Delta}), where "adjusted {Delta}" is the adjusted racial difference obtained when the specified variables were included in the model and "SH-adjusted {Delta}" is the adjusted racial difference obtained when standing height was used in the model.

To determine whether the residual racial difference was the result of covariate selection, we performed regression analyses using all candidate variables. The residual racial differences for the full model were compared with the differences for the parsimonious model.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study population
The numbers of children who were excluded from the study population for various reasons are shown in table 1. The greatest number of exclusions from the combined set of African Americans and Whites (n = 2,306) was due to doctors’ diagnoses of asthma (n = 238). This gave us a final study group of 623 Whites (320 girls and 303 boys) and 839 African Americans (452 girls and 387 boys). Except for the last three exclusions, the study group was similar to the population used by Hankinson et al. (5) to derive the race- and gender-specific spirometric reference equations. Table 2 presents the subjects’ characteristics by gender and race. Girls and boys of both races were similar in age (mean ages were 12.2 years for girls and 12.0 years for boys). African Americans of both sexes were taller, had lower FEV1 and FVC values, had more exposure to environmental tobacco smoke at home, and came from families with heads that were poorer, less educated, and more likely to be unemployed. Table 2 shows that in comparison with Whites, serum levels of vitamin A, vitamin C, and {alpha}-carotene were lower in African Americans of both sexes. When compared with Whites, the African-American girls had a higher body mass index, and the African-American boys had a higher FEV1:FVC ratio.


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TABLE 1. Numbers of subjects excluded from an analysis of lung function in African-American and White children aged 8–17 years, Third National Health and Nutrition Examination Survey, 1988–1994
 

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TABLE 2. Characteristics of subjects included in an analysis of lung function in African-American and White children aged 8–17 years, Third National Health and Nutrition Examination Survey, 1988–1994*
 
Effect of anthropometric, socioeconomic, and nutritional factors
In regression analysis, terms for the interaction between family-head education and race and the interaction between poverty index and race were not significant in either girls or boys, indicating that these socioeconomic variables affected FEV1 and FVC similarly in both racial groups. For this reason, we combined the White and African-American children by gender to study the main effects of socioeconomic status on the racial difference in lung function.

Tables 3 and 4 show the results of regression analyses performed to determine the effect of including sitting height, socioeconomic variables, and serum levels of antioxidant vitamins on the racial difference in lung function in girls and boys. When age, standing height, and race were entered into the regression model, the racial difference in FEV1 between White and African-American subjects was 356 ml in girls and 364 ml in boys (table 3). Adjusting for sitting height instead of standing height reduced the racial difference to 203 ml (~43 percent reduction) in girls and 170 ml (53 percent reduction) in boys. In girls, the most significant socioeconomic variable that was found to affect lung function was the educational level of the family head, whereas in boys it was poverty index. The addition of these socioeconomic variables to the respective models reduced the racial difference further to 184 ml (48 percent reduction) in girls and 140 ml (61 percent reduction) in boys. Of the antioxidants listed in table 2, only serum {alpha}-carotene in girls and vitamin A in boys were significantly associated with FEV1. The subsequent inclusion of these antioxidants in the respective models further reduced the racial difference to 178 ml (50 percent reduction) for the girls and 133 ml (63 percent reduction) for the boys.


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TABLE 3. Effect size{ddagger} of sitting height, socioeconomic status, and serum vitamin levels on the racial difference in forced expiratory volume in 1 second among nonsmoking, asymptomatic African-American and White children aged 8–17 years, Third National Health and Nutrition Examination Survey, 1988–1994
 

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TABLE 4. Effect size{ddagger} of sitting height, socioeconomic status, and serum vitamin levels on the racial difference in forced vital capacity among nonsmoking, asymptomatic African-American and White children aged 8–17 years, Third National Health and Nutrition Examination Survey, 1988–1994
 
We also performed similar regression analyses for FVC. When age, standing height, and race were entered into the regression model, the racial difference in FVC between Whites and African Americans was 416 ml in girls and 459 ml in boys (table 4). Adjusting for sitting height instead of standing height reduced the racial difference to 240 ml (~42 percent reduction) in girls and 225 ml (51 percent reduction) in boys. The addition of socioeconomic variables reduced the racial difference further to 224 ml (46 percent reduction) in girls and 200 ml (56 percent reduction) in boys. The subsequent inclusion of serum antioxidants (vitamin A and {alpha}-carotene for girls; vitamin A for boys) further reduced the racial difference to 208 ml (50 percent reduction) for the girls and 195 ml (58 percent reduction) for the boys.

To determine whether other socioeconomic variables had any effect on FEV1 and FVC, we added to the regression models the socioeconomic and nutritional variables listed in table 1 for which data were available on all subjects (table 5). These full models showed that including a larger set of socioeconomic and nutritional variables accounted for only a slightly larger amount of the residual racial difference.


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TABLE 5. Effect size{ddagger} of sitting height, socioeconomic measures, environmental smoke exposure, and serum antioxidant levels on the racial difference in lung function among nonsmoking, asymptomatic African-American and White children aged 8–17 years, Third National Health and Nutrition Examination Survey, 1988–1994
 
Effect of environmental tobacco smoke exposure
The inverse association between exposure to tobacco smoking at home and the educational attainment of the family head was observed in each of the four gender-race subgroups in this study. The subjects were divided by exposure to tobacco smoke in the home. This yielded 450 girls and 400 boys who came from homes with no smokers and 322 girls and 290 boys who came from homes with at least one tobacco smoker. Values for measures of socioeconomic status, such as poverty index, years of education of the family head, and employment status of the family head, as well as the proportion of Whites, were all higher in the nonexposed subgroups for both genders.

To evaluate the contribution of the greater home exposure to tobacco smoking in African Americans to the racial difference in lung function, we used gender-specific multivariate regression models that adjusted for age, race, and sitting height. Results showed that exposure to tobacco smoke at home, as measured by the presence of at least one smoker in the household, was weakly associated with FEV1 in the girls (p = 0.049), reducing FEV1 by 40.7 ml but accounting for only 4 ml (1 percent) of the FEV1 racial difference. How-ever, in this model, the negative effect of home smoking exposure on FEV1 became nonsignificant (p = 0.15) once education of the family head was taken into account. There was no effect of household smoke exposure on FVC or on the racial difference in FVC in this group of healthy girls (p = 0.8).

Using similar regression models, we could not detect a significant effect of home exposure to tobacco smoking on FEV1 (p = 0.13) or FVC (p = 0.8) in this subset of asymptomatic healthy boys. All of the above findings led us to conclude that there was no significant effect of home tobacco smoke exposure on the racial difference in lung function.

Effect of birth weight and maternal smoking during pregnancy
To investigate the effect of low birth weight on lung function in general, and on explaining the racial difference in FEV1 and FVC specifically, we analyzed subsets of healthy children (383 girls and 369 boys) with available birth weight information. The girls in the female subset (169 Whites and 214 African Americans) ranged in age from 8 years to 12 years (mean = 10.1 years). The mean birth weight of the White girls was significantly higher than that of the African-American girls (3,381 g (standard error, 41) vs. 3,200 g (standard error, 39)). The addition of birth weight to gender-specific regression models that adjusted for age, sitting height, and race showed that a decrease in birth weight of 100 g was associated with reductions in FEV1 and FVC in girls of 6.7 ml and 6.0 ml, respectively; it reduced the racial difference in FEV1 by an additional 11.4 ml (3.7 percent) and reduced the racial difference in FVC by 10 ml (2.9 percent). In this subgroup of younger girls, the overall reductions in the FEV1 and FVC racial differences after the addition of birth weight and education were 53 percent and 55 percent, respectively. The magnitude of the effect of birth weight on lung function stayed essentially the same when education of the household head was taken into account.

In this subgroup, the proportion of children exposed to maternal smoking during pregnancy was 25 percent in Whites and 22 percent in African Americans. However, the difference was not statistically significant (p = 0.7). Regression analyses showed that the effects of maternal smoking during pregnancy on FEV1 (p = 0.096) and FVC (p = 0.9) were not significant. The weak effect on FEV1 became even weaker when birth weight was included in the model. Thus, it appears that in-utero exposure to maternal smoking does not contribute to the racial difference in lung function in this healthy subset of younger girls.

Similar analyses were conducted in the subset of 369 boys with available information on birth weight. The 174 White boys and 195 African-American boys ranged in age from 8 years to 12 years (mean = 10.1). The mean birth weight of the White boys was significantly higher than that of the African-American boys (3,503 g (standard error, 50) vs. 3,214 g (standard error, 46)). In this group of boys, the inclusion of birth weight in regression models that adjusted for age, sitting height, and race showed that a decrease in birth weight of 100 g was accompanied by decreases of 5.3 ml and 6.4 ml in FEV1 and FVC, respectively. Birth weight further reduced the racial difference in FEV1 by 13 ml (4.9 percent reduction) and reduced the racial difference in FVC by 16 ml (4.2 percent reduction). The overall reductions in the FEV1 and FVC racial differences after the addition of birth weight and poverty index were 64 percent and 57 percent, respectively. The effect of birth weight was slightly reduced when poverty index was included in the model.

Moreover, we found in this subset that the proportion of White boys who were exposed to maternal smoking during pregnancy (28 percent) was significantly higher than the proportion of African-American boys (18 percent) (p = 0.02). We did not observe any significant effect of maternal smoking during pregnancy on FEV1 or FVC. This indicates that, as in the girls, maternal smoking during pregnancy does not explain the racial difference in lung volume in this subgroup of younger healthy boys.

Additional analyses carried out in the younger cohort using the available socioeconomic, nutritional, and smoke-exposure variables did not reduce the racial difference in comparison with the parsimonious model.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This cross-sectional study of the US population confirmed earlier findings that African-American children have lower lung volumes than White children (1, 2). After adjusting for anthropometric, socioeconomic, and nutritional variables, we could account for only 50 percent of the racial differences in FEV1 and FVC among girls; we were able to account for 63 percent of the racial difference in FEV1 and 58 percent of the racial difference in FVC among boys. As in the adults from the same nationally representative study (19), the major source of difference was anthropometric, namely the lower trunk:leg ratio of African Americans as compared with Whites. Substituting sitting height for standing height reduced the racial difference in FEV1 by 43 percent in girls and 53 percent in boys and reduced the racial difference in FVC by 42 percent in girls and 51 percent in boys. Although this reduction was larger than that observed in NHANES III adults (19) and in a group of healthy nonsmoking African Americans and Whites aged 6–24 years (3), it was smaller than that reported by Hsi et al. (2), who found that the use of sitting height in children could account for most of the racial difference in lung volume. Presumably, sitting height more closely corresponds to the size of the thorax than standing height.

As in our study of the NHANES III adults (19), socioeconomic variables explained smaller amounts of the racial difference in lung volume between African-American and White children. Adjustment for education of the family head as a surrogate for socioeconomic status reduced FEV1 and FVC by 5 percent and 4 percent, respectively, in girls. In boys, poverty index but not education of the family head influenced lung function, reducing the racial difference in FEV1 by 8 percent and reducing the racial difference in FVC by 5 percent.

We also considered the effect of the major antioxidant vitamins previously shown to influence lung function (12, 13). Of these antioxidants, serum vitamin A and {alpha}-carotene were significantly associated with lung function and were also lower in African Americans in this study group (table 2). The latter finding is consistent with the report by Patterson et al. (22) that African Americans have lower consumption of fruits and vegetables than Whites. However, the addition of these antioxidants to the gender-specific models explained only 1–4 percent of the racial difference in lung function. It is notable that the association of the socioeconomic variables with lung function was reduced when the above antioxidants were included in the model. This suggests that low serum levels of antioxidant vitamins may partially explain the negative effect of low socioeconomic status on lung function.

In this group of healthy children, home exposure to tobacco smoking, as measured by the presence of at least one smoker in the household, was more common in African Americans and was weakly associated with FEV1 only in girls. This is consistent with some other reports that females are more susceptible to tobacco smoke exposure than are males (7, 23). However, this negative effect, which explained very little of the racial difference in FEV1 (1 percent), became nonsignificant after education of the family head was taken into account. Additionally, the lack of effect on FEV1 and FVC in boys indicates that home exposure to tobacco smoke cannot be evoked to explain the racial difference in lung function in this group of asymptomatic healthy girls and boys. The minimal effect of home smoke exposure is different from other results obtained in general population samples (17, 18). Our results should not be used to infer that there is no effect of home tobacco smoke exposure in susceptible children. Our failure to find an effect of home tobacco smoke exposure on lung function was probably due to our exclusion of children with asthma and other lung diseases, who are more susceptible to environmental tobacco smoke.

In the younger subgroup of healthy girls and boys (mean age = 10 years), we also found that in-utero smoke exposure, though more common in White children than in African-American children, was significantly higher only in boys. This finding and the lack of an effect on lung function indicate that maternal smoking during pregnancy does not explain the racial difference in lung function in healthy boys and girls.

Using the same younger subset, we found that the African-American children had lower birth weights than Whites. Even though birth weight was significantly associated with lung function, the birth-weight differential between the two racial groups explained 3–5 percent of the racial difference between African Americans and Whites. The report by Barker et al. (14) that lower birth weight was associated with lower lung function in men and that mean FEV1 at age 59–70 years increased by 60 ml for each pound (0.45 kg) of birth weight suggests that racial differences in birth weight might affect the lung function racial difference in adults. The unavailability of birth weight information for the older children and the adults in NHANES III prevented us from estimating the contribution of birth weight to the observed racial difference in these groups.

The reasons for the lung volume difference between Whites and African Americans are complex, because race is a social as well as a biologic construct. In this study, the largest component of the lung function difference was sitting height. In addition to the socioeconomic variables listed in tables 35, we examined the effects of family head employment status, availability of sufficient food, gender of the family head, and household size. We also examined the effects of such environmental factors as home and in-utero tobacco smoke exposure and the effect of the racial difference in birth weight, all of which are associated with lower lung function. These variables explained only a small proportion of the racial difference in lung function.

The reason for the unexplained portion of the racial difference in lung function is not clear. It may be that we did not adequately adjust for confounding anthropometric and socioeconomic factors. Sitting height is not a perfect measure of the size of the thorax and may not account for all of the anthropometric racial difference. Furthermore, there may be biologic components of this difference that are not explained by sitting height. It is also likely that the socioeconomic variables in NHANES III did not capture all of the environmental factors that affect lung function and that other factors that account for this difference were not measured in NHANES III.

We also considered the possibility that the higher number of African-American children with undiagnosed asthma or other respiratory diseases might be responsible for the racial difference in lung function. However, when we excluded subjects whose FEV1 percent-predicted value was less than 80, we could account for only a slightly greater amount of the adjusted racial difference than was observed for the whole sample.

In conclusion, sitting height explains only 42–53 percent of the racial difference in lung function between White children and African-American children. Socioeconomic, nutritional, and environmental variables measured in NHANES III explained relatively little (7–10 percent) of the lower lung volume in African Americans. Thus, the remaining difference in lung function must be attributable to unmeasured variables or other biologic, environmental, or socioeconomic factors.


    NOTES
 
Correspondence to Dr. Robert A. Wise, Department of Medicine, Johns Hopkins University School of Medicine, 5501 Hopkins Bayview Circle, Baltimore, MD 21224 (e-mail: rwise{at}jhmi.edu). Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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