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African-Americans have lower lung function than whites. However, the relative contributions of body habitus and socioeconomic factors are unknown. To address this question, we analyzed data from 1242 white (806 women, 436 men) and 1084 African-American (696 women, 388 men) asymptomatic, nonsmoking adult participants of the third National Health and Nutrition Examination Survey (NHANES III). African-Americans were poorer, had larger FEV1/FVC and body mass index (BMI), but lower sitting height, FEV1 and FVC than whites. Cross-sectional regression analyses using spirometric, anthropometric, and socioeconomic data were performed separately by sex to investigate racial differences in lung function. Sitting height accounted for 35-39% of the race difference in both sexes. Poverty index accounted for about 7.5% and 2.5% of the racial difference in women and men, respectively, whereas the effect of education accounted for about 2% in women and 4.7% in men. With further adjustment for BMI, we could account for only about half of the racial difference in FEV1 and FVC. We conclude that the racial difference in lung function is only partially explained by a shorter upper body segment in African-Americans. Although low socioeconomic indicators are related to lower lung function, they explain only a small proportion of this racial difference.
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Keywords: respiratory function tests; anthropology, physical; social class; body mass index; reference values
It has long been recognized that African-Americans, both adults and children, have lower pulmonary function than whites (1). To account for these differences, the general practice for predicting reference values of lung function for African-Americans is to apply a scaling factor of 0.85 to 0.88 to white reference equations (7, 10). However, some investigators have recommended the use of race-specific prediction equations (3, 6, 8). Recently, Hankinson and coworkers (9) derived spirometric reference equations for whites, African-Americans, and Hispanics based on asymptomatic, nonsmoking men and women participants of the third National Health and Nutrition Examination Survey (NHANES III). When adjusted for standing height, FVC and FEV1 were similar in whites and Mexican-Americans, whereas African-Americans had lower values. This racial difference has been attributed in part to anthropometric factors such as smaller trunk:leg ratio in African-Americans (3, 9). Hsi and colleagues (4) found that the use of sitting height instead of standing height in children markedly reduced the racial difference in FEV1 and FVC, thereby allowing the use of one set of prediction equations. However, other studies, which included young adults, demonstrated that anthropometric factors, including sitting height, could only partially account for the racial difference between African-Americans and whites (1, 6, 11, 12).
Lower socioeconomic status (SES) is also associated with lower pulmonary function in both children (13, 14, 17), and adults (15). Among never smoking men of the Honolulu heart study, lower educational attainment was a predictor of rapid FEV1 decline (16). Moreover, findings in 14,223 subjects aged 20-90 yr from the Copenhagen Heart Study demonstrated that education and income were independently and positively associated with FEV1 and FVC (17). African-Americans have disproportionately greater poverty and less education than whites (18). We therefore wondered if the residual racial difference in lung function after adjusting for sitting height could be attributed to socioeconomic status. Obesity also has adverse effects on lung function (19, 20). Because in affluent countries, obesity is more common, especially among women, in lower socioeconomic strata (21), we also sought to investigate the role of obesity on the racial difference in pulmonary function after controlling for socioeconomic status.
The NHANES III is a cross-sectional multiracial study of the U.S. population with high quality pulmonary function testing, body size measurements, and socioeconomic indicators. Thus, it provides an excellent data set for investigating the relationships between lung function, race, and socioeconomic and anthropometric measures. Specifically we wanted to know how much of the racial difference in lung function between healthy nonsmoking adult African-Americans and whites could be accounted for by sitting height, poverty level, educational status, and body mass index (BMI).
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Study Population
Participants were adults who performed spirometric testing as part of NHANES III. The latter is a cross-sectional representative sample of the U.S. noninstitutionalized civilian population living in households across the country. The survey was conducted between 1988 and 1994 by the National Center for Health Statistics (NCHS) using a stratified multistage probability cluster sampling design. The survey population included an oversampling of African-Americans and Mexican-Americans. Participants completed extensive questionnaires and a comprehensive physical examination, which included spirometry. The details of the survey design and examination procedures have been published by the NCHS (22, 23). In this study, we applied the criteria of Hankinson and colleagues (9) to select asymptomatic, lifelong nonsmoking adults ranging in age from 20 to 80 yr, who described themselves as white or African-American and who, in addition, had the relevant anthropometric and socioeconomic variables available. From the total sample of 16,695 adult participants who performed spirometry, we selected the 2326 who met the criteria listed in Table 1. This sample was similar to that used by Hankinson and coworkers (9) for deriving race and sex-specific reference equations.
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Spirometry
Spirometry was performed as described in detail elsewhere (9, 23). Sessions having at least two acceptable maneuvers were analyzed. We used the reference equations that were previously derived by Hankinson and coworkers (9).
Statistical Analyses
To estimate the effect of anthropometric and socioeconomic variables
on racial differences in lung function, African-American participants
were combined with whites by sex, resulting in 1502 women and 824 men. Separate regression analyses were then performed for men and
women. Regression models were constructed with FEV1 or FVC as
the dependent variable. In addition to age and race (white = 1, African-American = 2), independent variables included sitting or standing height, BMI, defined as weight (kg) divided by the square of
height (m), education (
high school = 0, > high school = 1), poverty
index (defined as the ratio of family income in the last 12 mo to the
federal poverty line). Therefore, in this analysis a higher poverty index indicates a higher socioeconomic status (SES). We also evaluated
the interaction terms between poverty index and race, and between
education and race to investigate whether SES indicators had different effects on African-Americans and whites. ANCOVA models that
adjusted for age and standing height were used separately by sex to
test for the significance of the racial difference of selected spirometric
and anthropometric measures between African-Americans and whites.
Similarly, significance of the racial difference in poverty index and educational status was tested in models that adjusted for age.
To determine the effect of poverty index on FEV1 and FVC by sex
and race, we divided each sex-race subgroup into quintiles of poverty
index. Separate regression analyses by race and sex (PROC GLM)
were done after adjusting for age, sitting height, and quintile of
poverty index. Similarly, the effect of education ( high school = 0, > high school = 1) on FEV1 and FVC was determined for each sex-
race subgroup after adjusting for age and sitting height. Analyses
were done with SAS software (SAS Institute, Cary, NC). Coefficients
were considered significant at a p value of 0.05.
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Study Population
Table 1 shows the number of subjects sequentially excluded from the entire study population. The highest number of exclusions is due to cigarette smoking. The resulting study group of 1242 whites (806 women and 436 men) and 1084 African-Americans (696 women and 388 men) meets the same criteria used by Hankinson and coworkers (9) for the derivation of reference values of spirometry. Table 2 presents the subject characteristics by sex and race. White women were the oldest, followed by white men. When compared with white individuals, African-Americans had larger FEV1/FVC and BMI (p < 0.01). They also had lower FEV1, FVC, and sitting height (p < 0.0001). The African-Americans, especially the women, were poorer (lower poverty index), and had less education than the white participants (p < 0.0001).
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The Effect of Anthropometric and Socioeconomic Factors on the Lung Function Difference between Whites and African-Americans
In regression models that adjusted for age and sitting height, there was no significant racial difference in the effect of poverty or education on lung function in men or women. That is, there was no significant interaction between race and poverty or between race and education on FEV1 or FVC. Consequently we combined whites and African-Americans by sex.
The results of regression analyses to determine the effect of anthropometric and socioeconomic variables on the racial difference in lung function in men and women are presented in Tables 3456. When age, standing height, and race were entered into the regression model, the racial difference in FEV1 between white and African-American women was 469 ml (Table 3). Substituting the sitting height for the standing height reduced the racial difference to 307 ml (about 35% reduction). The sequential addition of the poverty index and BMI to the latter model reduced the racial difference further to 272 and 248 ml, respectively. Table 3 also shows that when education was used as another measure of socioeconomic status, it had a smaller effect on reducing the racial difference than the poverty index (9 ml versus 34 ml).
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The results for FVC in women were similar. Table 4 shows that adjusting for sitting height instead of standing height reduced the FVC racial difference from 611 ml to 384 ml (about 37% reduction). Poverty index and BMI were both significant predictors of FVC, and their inclusion in the model reduced the race difference to 336 and 311 ml, respectively. Education had less effect than the poverty index in accounting for the FVC racial difference between white and African-American women. BMI was inversely correlated with FEV1 and FVC, and its effect was similar on both pulmonary function measures (Tables 3 and 4).
When similar analyses were done for men (Tables 5 and 6), the use of sitting height instead of standing height reduced the racial difference in FEV1 from 606 to 367 ml, and in FVC from 847 to 516 ml (about 39% reduction). In contrast to women, poverty index in men was only of borderline significance for FEV1 or FVC, and had little effect on reducing the racial difference in both measures of pulmonary function. The sequential addition of poverty index and BMI to the latter model reduced the racial difference in FEV1 further to 352 and 315 ml, respectively, and in FVC to 497 and 458 ml, respectively. Having more than a high school education, however, had a greater effect on reducing the racial difference than poverty index (Tables 5 and 6). Adjusting for sitting height, education, and BMI reduced the racial difference in FEV1 from 606 to 303 ml and in FVC from 847 to 445 ml (about 50% reduction). Including both education and poverty index in the above regression models of the two sexes had no additional effect on reducing the racial difference in FEV1 or FVC. Consistent with previous observations, we found that BMI had a greater effect on lung function in men than women (19, 20).
The Effect of Poverty Index and Education on Lung Function in White and African-American Men and Women
To explore the effect of family income on pulmonary function in men and women of each race, we divided each of the four sex-race subgroups into quintiles of poverty index. Overall, the African-Americans were poorer than the whites. Figure 1 shows that the average poverty index in the lowest quintile of the African-American women was less than half that of the white women (0.414 versus 1.102). In both racial groups, higher poverty index (higher income) was associated with higher FEV1 (p = 0.006 for whites, p = 0.04, for African-Americans), and also with higher FVC (p = 0.0002 for whites, and p = 0.03 for African-Americans).
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The relationship between poverty index and pulmonary function measures in men of each race after adjusting for age and sitting height is presented in Figure 2. The average poverty index of the African-American men in the lowest quintile was slightly more than half that of the white men in the same quintile (0.648 versus 1.157). As Figure 2 shows, higher poverty index in white men is associated with higher FEV1 (p = 0.04), and with borderline increases in FVC (p = 0.08). In contrast, African-Americans show no association between poverty index and pulmonary function. Overall, there is a sex difference in the effect of poverty on lung function such that the effect of poverty index was more pronounced in women than in men.
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As Figure 3 shows, low educational status was consistently associated with reduced lung function in all sex-race subgroups except for FEV1 in white men (p = 0.1). In contrast to poverty index, which did not affect lung function in African-American men, education has a significant effect on both FEV1 (p = 0.004) and FVC (p = 0.03) in this group of men.
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The main finding of this analysis is that we can explain only about half of the racial difference in FEV1 and FVC between white individuals and African-Americans by accounting for sitting height, BMI, and socioeconomic indices such as poverty index or education. We found that the use of sitting height instead of standing height reduced the racial difference in FVC by 37% in women and 39% in men, and in FEV1 by 35% in women and 39% in men. Thus, it appears that sitting height accounts for the largest portion of the racial difference in lung function in both sexes. This presumably reflects the racial difference in upper to lower body segment ratio. Although the use of sitting height in this study was not as effective in reducing the racial difference as that observed in children (4), the magnitude of the reduction was still larger than that reported by other investigators (1, 11, 12). In this connection, Schwartz and colleagues reported that the addition of sitting height reduced the lung function racial difference by 16% in healthy nonsmoking blacks and whites 6-24 yr of age in the NHANES II study (6).
Once sitting height is taken into account, we considered the effect of using two SES indicators: poverty index, a measure of current family income, and education, which reflects socioeconomic status during lung development. Poverty index accounted for about 7.5% and 2.5% of the racial difference in lung function in women and men, respectively, whereas the effect of education accounted for about 2% in women and 4.7% in men. Thus socioeconomic status, as measured by poverty index, was a better explanatory variable for the racial difference in women than in men.
In separate sex-race subgroup analyses, we also observed that family income had less impact on lung function in men than in women (Figures 1 and 2). There was only a weak association between poverty index and lung function in white men, and none in African-American men. In contrast, the effect of education on lung function in African-American men was more prominent. In women, however, even though education was less effective than poverty index in explaining the racial difference in lung function, its impact, especially on FEV1, was significant in both races.
Education and income (poverty index) are two imperfect socioeconomic indicators that reflect social status at different times in life. Individuals usually achieve their highest level of education in young adulthood, and for most people, it remains about the same throughout life. Thus, education cannot reflect changes in social status that occur after schooling ends. In contrast, occupational level and hence income generally begin after education is completed. Consequently, income is a better indicator of current socioeconomic status than education. (24, 25).
Obesity adversely affects pulmonary function. Lower levels of education and occupation are associated with more overweight (25). The addition of BMI to the regression models reduced the coefficients of poverty index and education, and also reduced the racial difference in lung function. The effect of BMI on FVC and FEV1 was larger in men than in women. This is consistent with previous reports in the literature (19, 20), and with our recent finding that the differential pattern of fat distribution between the sexes accounts for the sex difference that obesity confers on lung function (26).
We also considered the possibility that a higher degree of environmental tobacco smoke exposure in women (27) may partly explain the greater effect of poverty on women. Additional analyses showed that the concordance of low educational status and the presence of household smokers was greater in women than in men. Further multivariate models, however, showed that passive smoking exposure did not account for the racial difference in lung function when socioeconomic status (educational level) was taken into account.
We cannot account for a large component of the racial difference in lung function. Despite the small racial differences in the accuracy of self-report of smoking status in the NHANES III that Caraballo and coworkers demonstrate (28), the overall accuracy by serum cotinine is high (98% for African-Americans and 98.6% for whites). For this reason we do not think that the racial difference in the accuracy of self-report can explain the racial differences in lung function. Unmeasured factors that might account for this residual difference are prenatal factors or childhood factors such as low birth weight (29), maternal smoking during pregnancy (30), allergy, indoor air pollution, and exposure to environmental toxins (13, 14), or inadequate adjustments for anthropometric and socioeconomic variables. Moreover, sitting height is not a perfect measure of the size of the thorax, and may not account for the entire anthropometric racial difference. It may also be that the socioeconomic variables that we used did not capture all of the environmental factors that influence lung function. We also cannot exclude the possibility that there are intrinsic genetic differences in lung development between the races.
In summary, the NHANES III study shows clearly that the well-established racial difference in lung function cannot be completely explained by measurable differences in body habitus. Furthermore, the striking racial difference in socioeconomic status does not account for much of the residual difference in lung function between asymptomatic nonsmoking whites and African-Americans. Poverty appears to have a greater effect on lung function in healthy women than in healthy men. The reason for this is not clear.
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Footnotes |
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Correspondence and requests for reprints should be addressed to Raida I. Harik-Khan, Clinical Research Branch, National Institute on Aging, Gerontology Research Center, 5600 Nathan Shock Drive, Box 06, Baltimore, MD 21224. E-mail: HarikkhanR{at}grc.nia.nih.gov
(Received in original form June 18, 2001 and accepted in revised form August 29, 2001).
Acknowledgments:
The authors thank Susheel Patil and Junyong Fang for
their comments.
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References |
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