Effect of altitude on the lung function of high altitude residents of European ancestry.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 75:77-85 (1488) Effect of Altitude on the Lung Function of High Altitude Residents of European Ancestry LAWRENCE P. GREKSA, HILDE SPIELVOGEL, MARIO PAZ-ZAMORA, ESPERANZA CACERES, AND LUIS PAREDES-FERNANDEZ Department of Anthropology, Case Western Reserve University, Cleveland, Ohio (L€! G.); Instituto Boliviano de Biologia de Altura, Universidad Mayor de S a n Andres (H.S., M.l?-Z., E.C.)and Clinica Nacional del Deporte L a Paz, Bolivia (L.l?-R) KEY WORDS Lung function, High altitude, Hypoxia, Developmental adaptation ABSTRACT The forced vital capacity (FVC), forced expiratory volume in one second (FEV), and ratio of FEV to FVC (%FEWof 161 male and 158 female youths of European ancestry who were born at high altitudes and who were residing in La Paz, Bolivia (average altitude of 3,600 m) were examined and compared with those for lowland Europeans and highland Aymara Amerindians. FVC and FEV were significantly larger (p < .001) in the La Paz Europeans than in two lowland control samples of European ancestry, with the relative differences between samples varying from small (1.5-4.1%) to moderate (7.7-11.9%). It could not be determined whether the enhanced lung volumes of the La Paz European children were acquired through an accelerated development of lung volumes relative to stature during adolescence, as is the case for Amerindian highlanders. After controlling for body and chest size, FVC and FEV were significantly smaller in the La Paz Europeans than in highland Aymara (p < .001), suggesting that the lung volumes of the Aymara are influenced by factors other than simply growth and development at high altitude. Finally, as found in Amerindians, chest size is an important determinant of intra-individual variation in lung function among highland Europeans. The effects of a temporary high altitude sojourn on the respiratory function of adult European lowlanders have been extensively investigated (West and Lahiri, 1984). However, little is known about the effect on respiratory function of permanent residence at altitudes above 3000 m, from birth on, among Europeans. In earlier reports (Greksa, 1986a,b; Greksa et al., 1985a,b), we evaluated the effect of permanent residence at high altitudes on the linear growth, chest morphology, and exercise performance of European youths residing in La Paz, Bolivia (average altitude of about 3,600 m). The present report describes pulmonary function in these children and, in particular, examines the effect on their lung function of growth and development within an hypoxic environment. 0 1988 ALAN R. LISS. INC. SUBJECTS AND METHODS Subjects The sample consists of 161 male and 158 female middle and upper socioeconomic status children of European ancestry (9.0-19.9 years of age) residing in La Paz, Bolivia. The age and sex distribution of the sample are presented in Table 1.All subjects were born and raised at high altitudes (> 2,500 m) and were sampled from a private school located at an altitude of about 3,700 m. Both surnames of all children were of European origin: 57% had two Spanish surnames, 13% had two non-Spanish (primarily German) surnames, and 30% had mixed surnames. Children with two Spanish surnames tend to Received September 23, 1986;revision accepted May 13,1987. 78 L.P. GREKSA ET AL. TABLE 1. Ace and sex distribution o f the samole Age 9.0 - 9.9 10.0 - 11.9 12.0 - 13.9 14.0 - 15.9 16.0 - 17.9 18.0 - 19.9 Males Fe ma1es 9 41 36 33 21 21 8 37 44 25 28 16 be from families with a long history of residence in South America while those with two non-Spanish European surnames tend to be from families that had migrated to high altitude relatively recently. Further details on these children are available elsewhere (Greksa et al., 1985a). Thirty-six children (19 males and 17 females) reported that they occasionally smoked cigarettes. A comparison between the smokers and their nonsmoking classmates, after controlling for anthropometry, indicated that there were no significant differences in lung function between these groups (p > .05). The occasional smokers were therefore retained in the sample. Anthropometry The anthropometric measurements considered in this report are stature, weight, sitting height, transverse chest diameter (chest width), and anterior-posterior chest diameter (chest depth). An index of chest shape [(chest depth x 100)/chest width] was also calculated. All measurements were made by one researcher according to standard procedures (Weiner and Lourie, 1981). Pulmonary function The pulmonary data reported in this paper are forced vital capacity (FVC), forced expiratory volume in one second (FEV), and FEV relative to FVC [%FEV x lOO)/FVC]. These data were collected a t the school by one researcher using a noncomputerized Collins 13.5 1 spirometer. Average barometric pressure (mm Hg) and ambient temperature ("C) were 496.2 (SD 1.6) and 17.1 (SD 1.6), respectively. All procedures were in accordance with recommended guidelines (American Thoracic Society, 1979; Taussig et al., 1980). Thus, all tests were performed by a trained and experienced technician, nose clips were used, and all subjects were seated and remained erect during the test. After instruction in the proper techniques, the researcher attempted to obtain a minimum of 3 accept- able FEV curves from each subject, based on standard criteria (American Thoracic Society, 1979). The reported data are the maximum FVC and FEV for each child, even if the two values were obtained from different curves. Population comparisons Substantial variation has been found in the lung volumes of low-altitude European children (Polgar and Promadhat, 1971).Also, the La Paz European sample is heterogeneous, consisting primarily of children of Spanish ancestry but including a number of children of Western European ancestry. Thus, it is no simple matter to select a n appropriate low-altitude European control sample. Two different samples were therefore chosen for this purpose: children of Mexican-American ancestry studied by Hsu et al. (1979) and reference standards developed by Polgar and Promadhat (1971) from studies of children of European ancestry which were published between 1921 and 1969. Studies completed after 1969 have not been found to differ substantially from these reference curves (Polgar and Weng, 1979; Taussig et al., 1980).The La Paz European children were also compared with children of Aymara ancestry residing in La Paz (Greksa et al., 1987). The Aymara children were also born and raised at high altitudes and attended schools in La Paz which are located at a similar altitude as the school of the European children. Statistical analyses All statistical analyses were performed with Statistical Package for the Social Sciences (SPSS)(Nie et al., 1975), following the procedure outlined by Polgar and Promadhat (1971) and refined by others (e.g., Cotes et al., 1979; Hsu et al., 1979; Patrick and Patel, 1986). Thus, all analyses were performed on the common logarithm transforms of the dependent (lung function) and independent (age and anthropometry) variables. As found by Hsu et al. (1979), the transformed data meet the assumptions of parametric statistical techniques as well as or better than the untransformed data. In addition, such a model facilitates the incorporation of a curvilinear component into the analyses. Regression analysis was used to examine the relationships of lung function with age and anthropometry. A classic analysis of covariance (ANCOVA) model was used to compare lung function between sexes and ethnic LUNG FUNCTION AT HIGH ALTITUDE 79 cant (p < .05) while none of these relationships were significant in females. In both cases, the explained variation was low. Finally, the slopes of the FVC and FEV relationships, with the exception of those with stature, sitting height, and chest shape, were significantly larger in males than females (p < .05). There were no significant sex differences for the slopes of any of the %FEV relationships (p > .05). After controlling for body and chest size, FVC and FEV were significantly larger in males than in females (p < .001) by, on average, 298 and 130 ml, respectively (Table 3). %FEV, however, did not differ between sexes (p > .05). After controlling for all other covariates, only stature, chest width, and chest depth were significant determinants of FVC and FEV in La Paz European children (p < .001), with each, based on the magnitude of the F-ratios, being of similar importance. Only chest depth explained a significant proportion of the %FEV variance, after controlling for all other covariates (p < .05). Although not included here, ANCOVAs of lung function between surname categories (two Spanish surnames, two non-Spanish European surnames, and mixed surnames) were also performed. After controlling for anthropometry, FVC and FEV differed significantly between male surname categories (F = 5.96.5; p < .05). In each case, males with two Spanish surnames had the largest adjusted mean lung volumes while males with two non-Spanish European surnames had the smallest adjusted volumes. There were no significant differences between male surname categories in %FEV,however (F = 0.3; p > .05). A different pattern was observed in females, where lung volumes (F = 0.0-0.4; p > .05) and %FEV (F = 1.7; p > .05) were all virtually identical between surname RESULTS categories. The mean residuals calculated by deterThe results of univariate logarithmic regressions of each lung function measure mining the differences between actual lung with age and anthropometry are included in volumes and lung volumes predicted for lowTable 2. (Sex-specificdescriptive statistics of altitude children of the same stature are preeach measure by age and stature groups can sented in Table 4. FVC by stature in the be obtained upon request.) With the excep- same samples is portrayed in Figure 1. The tion of the FVC and FEV relationships with FVC and FEV residuals tend to differ signifchest shape, all FVC and FEV relationships icantly from zero for both males and females were positive and highly significant (p < (p < .05), with the exception of the relative .001). The explained variation for these rela- FEV residuals based on Hsu et al.’s (1979) tionships tends to be substantially greater in data for Mexican-Americans, although the males than in females. The majority of the significant FEV residuals are just barely so. %FEV relationships for males were signifi- Also, although the absolute residuals based groups. Thus, lung function was compared between groups after controlling for all covariates. A maximum of five covariates could be controlled simultaneously with the available statistical package. The anthropometric variables of greatest interest (weight, height, sitting height, chest width, and chest depth) were therefore employed as covariates. The effect of growth and development at altitude on the static lung volumes (FVC, FEV) of the La Paz European children was estimated by determining the differences (residuals) between the actual FVC and FEV of each child and values predicted for low-altitude European children of the same stature, using prediction equations provided by Hsu et al. (1979) and Polgar and Promadhat (1971). Both absolute and relative (%) residuals were calculated. Only children with statures within the limits of the prediction equations were used for these analyses: 161 males and 158 females for residuals based on the Hsu et al. (1979)equations and 125 males and 151 females for the Polgar and Promadhat (1971) equations. Given the well-known positive effect of growth and development at high altitude on the lung volumes of Amerindian highlanders (Frisancho, 1969; Mueller et al., 1978), one would predict a similar response in the European children. A onetail t test of whether the mean residuals differed significantly from zero was used to test this hypothesis. Finally, the slopes of the log regressions of lung function on stature in La Paz European children were compared with those provided by Hsu et al. (19791, Polgar and Promadhat (1971),and Polgar and Weng (1979) in order to determine whether the La Paz European children display an accelerated growth in lung volumes relative to stature, as has been found in Amerindians (Frisancho, 1969; Mueller et al., 1978). 1371.5** 273.4** 546.0** 221.4** 147.7** 3.11 2.49 2.07 -0.20 0.92 0.79 2.99 2.81 1.95 1.37 -2.39 0.16 1.02 3.92 2.44 2.20 -3.04 - 1.88 0.88 1.85 2.76 89.6 81.8 65.1 0.3 63.7 77.8 74.7 71.2 58.7 48.6 2.1 0.39 1064.3** 2.97 -2.96 87.0 3.4 386.1** 459.4** 0.4 296.6** 712.2** 1186.5** 1.00 1.92 88.2 732.4** 1.40 1.95 82.2 "F ratio for a test of the significance of the slope *P < .05. **P < .001. Male Age (log yr) Weight (log kg) Stature (log cm) Sitting height (log cm) Chest width (log cm) Chest depth (log cm) Chest shape (log %) Female Age (log yr) Weight (log kg) Stature (log cm) Sitting height (log cm) Chest width (log cm) Chest depth (log cm) Chest shape (log %) x log FVC 1.4 44.5 56.9 67.3 71.0 73.1 62.3 0.4 63.5 81.3 89.6 87.3 87.9 83.0 2.84 1.85 0.84 -1.84 -3.00 2.17 2.39 3.93 1.06 0.20 -2.28 -2.86 1.90 1.93 a 0.31 1.32 1.94 2.76 2.94 0.78 0.92 -0.24 1.98 2.42 3.02 2.90 0.97 1.37 log FEV b ~ a 2.2 125.0** 205.7** 321.6** 382.1** 424.0** 257.7** 0.6 276.7** 689.0** 1.7 1.3 0.0 0.5 0.4 0.8 0.0 0.4 4.2 3.1 2.8 2.4 1095.5* * 1371.4** 3.1 1.7 r2 = 1155.5** 774.6** F TABLE 2. Results o f regressions of FVC, F E Y and %FEV by age and anthropometry, where log Y 2.08 2.00 1.96 2.05 2.05 1.97 1.95 2.01 2.04 2.04 2.10 2.11 1.99 - -0.07 -0.05 -0.01 -0.05 -0.05 0.02 0.00 -0.04 -0.08 -0.08 -0.08 -0.08 -0.03 -0.03 log %FEV b 1.98 a + b (log X ) 2.7 2.0 0.1 0.9 0.6 1.3 0.0 0.6 6.9* 5.1* 4.5* 3.8 5.0* 2.8 F 81 LUNG FUNCTION AT HIGH ALTITUDE on the Polgar and Promadhat (1971) reference standards are fairly large, this is not the case for the residuals based on MexicanAmericans, especially for FEV. The slopes from logarithmic regressions of lung function on stature in several studies of children of European ancestry are presented in Table 5. The slopes for La Paz European males are within the range of those for lowaltitude European children while the slopes for La Paz European females are somewhat larger than found at low altitude. Finally, the results of an ANCOVA of lung function between La Paz European and Aymara children is presented in Table 6. After controlling for body and chest size, FVC and FEV were significantly larger in Aymara than European children (p < .001) but only by, on average, about 130-155 ml. %FEV did not differ significantly between ethnic groups (p > .05).With the exception of weight in the comparison of FEV between European and Aymara females, all covariates explained a significant proportion of the variance in FVC and FEV, after controlling for all other covariates. As evaluated by the magnitude of the F-ratios, chest width and chest depth were among the most important deteminants of the FVC and FEV differences, especially in males. The importance of these measures in explaining the differences in lung volumes between groups can be seen from the results of an ANCOVA controlling for only stature, sitting height and weight (Fig. 1). For example, in this case, mean adjusted FVC was, on average, 312 ml larger in Aymara than European males (F = 84.6; p < .001) while the corresponding value in females was 291 ml (F = 36.7, p < .001). DISCUSSION Given the long history of residence of Europeans of Spanish ancestry in South America and the possibility that native Amerindians have adapted genetically t o their hypoxic environment (Baker, 19691, Amerindian admixture within the European population of Bolivia could confound the results of the present study. The comparisons between surname categories, which are basically between children from families with a long history of residence in South America and children whose families migrated relatively recently, were designed to test this possibility. The results of these analyses were contradictory, however, with males demonstrating a pattern which is consistent with TABLE 3. Results of analyses of couariance of lung function bv sex log FVC log FEV log %FEV Source of variation Sex: F ratio Covariates: F ratio Weight (log kg) Stature (log cm) Sitting height (log cm) Chest width (log 30.4** 19.4** 2.7 0.1 37.1** 3.3 0.0 33.3** 2.4 0.2 0.0 0.1 49.2** 43.8** 0.0 33.5** 19.4** 4.7* 89.1 87.3 4.2 3,388 3,090 2,884 2,754 87.1 87.1 cm) Chest depth (log cm) Explained variation, rz(%) Adjusted means Males Females *P < .05 **P < .001. the expectations of admixture (i.e., males with two Spanish surnames having the largest adjusted mean volumes and males with two non-Spanish European surnames having the smallest adjusted volumes)while females exhibited no differences between surname categories. However, similar comparisons detected no differences in stature or chest dimensions between surname categories in males or females (Greksa, 1986a,b; Greksa et al., 1985a,b).The lack of differences in chest dimensions is particularly pertinent since chest size and lung function are closely related at altitude (Frisancho, 1969; Mueller et al., 1978). Also, no differences in lung function were found between surname categories in two studies of Aymara highlanders (Greksa et al., 1987; Mueller et al., 1978). Thus, taking into consideration this auxiliary information and the inconsistent nature of the results of the surname comparisons in the present study, it seems reasonable to conclude that the male pattern is fortuitous and that any admixture which has occurred has probably had minimal effect on the lung function of the La Paz European children. The nature of the relationships of FVC, FEV and %FEV with age and anthropometry (Table 21, as well as the sex differences in the strengths and slopes of these relationships, are consistent with the findings of studies of lowland European children (Binder et al., 1976; Dickman et al., 1971; Hsu et al., 1979; Lange Anderson et al., 1984; Polgar L.P. GREKSA ET AL. TABLE 5. Slopes derived from log regressions of FVC and FEV on stature, where log Y = a + b (log X ) Source Polgar and Promadhat Polgar and Weng Hsu et al.: Whites Hsu et al: MexicanAmericans Present study !+ Males FVC FEV Females FVC FEV 2.67 2.81 3.18 2.97 3.00 2.83 2.72 2.78 2.78 2.92 2.68 2.85 2.97 2.90 2.99 2.94 - - - and Promadhat, 1971). These findings are also similar to those for highland Aymara children (Greksa et al., 1987; Mueller et al., 1978),with one major exception. Chest shape was found to be an important determinant of lung function in male and female Aymara highlanders by Mueller et al. (1978) and in female Aymara highlanders by Greksa et al. (1987). In the present study, however, chest shape was not significantly related to any of the lung function measures (Table 2). The reason for this difference is not clear. It may be due to sampling error in the present study. However, it may indicate that, although both Europeans and Amerindians display enhanced chest dimensions at altitude, the pattern of development of chest depth relative t o chest width differs between groups. Such a pattern would be consistent with the hypothesis that there is a genetic basis to the distinctive Amerindian thoracic morphology (Beall et al., 1977; Hoff, 1974). After controlling for all other covariates, stature, chest width and chest depth were significant determinants of FVC and FEV in the La Paz European children (Table 3). Also, mean-adjusted FVC and FEV, after controlling for anthropometry, were significantly larger, by about 4.7%, in La Paz Aymara than La Paz European children (Table 6). Based on an examination of the magnitude of the F-ratios of chest width and chest depth in an ANCOVA controlling for both body and chest size (Table 6), the fact that the average lung volume differences between groups approximately doubled when only body size was controlled, and the fact that chest dimensions are significantly larger in Aymara than European children (Greksa, 1986a,b), the most important anthropometric determinant of the differences in lung volumes between 83 LUNG FUNCTION AT HIGH ALTITUDE TABLE 6. Results o f analyses o f covariance o f lung function between European and Aymara children residing in La Paz European vs. Aymara males lop FVC loe FEV loe %FEV Source of variation Ethnic group Covariates Weight (log kg) Stature (log cm) Sitting height (log cm) Chest width (log cm) Chest depth (log cm) Explained variation r2 (%) Adjusted means European Aymara European vs. Aymara females lop FVC loa FEV loe QFEV 19.6** 25.5** 1.7 14.4** 5.5** 15.9** 37.6** 118.5** 72.6** 92.4 16.0** 7.7* 40.3** 117.6** 47.2** 91.6 0.1 0.7 0.6 0.4 4.8* 3.3 5.2* 5.7* 11.0** 15.5** 15.3** 75.4 7.7** 14.6** 12.4** 70.8 3,311 3,467 2,884 3,020 3,090 3,236 2,691 2,818 87.1 87.1 14.2** 0.2 2.0 2.1 1.9 0.4 0.1 0.1 3.5 8.5** 89.1 89.1 *P < .05. **P < ,001. 6000 ... ...... --- - - L a Paz European L a Paz Aymara Mexican -American European standards -/; A v) a 5000+ m 4000g 30002000 - -.-.-. Y IL *.*I I I I ...' I /* FEMALE I I I I Fig. 1. Forced vital capacity (ml) by stature in selected populations. these ethnic groups (Fig. 1)would appear to varied from 1.6-4.1% when using the sample be chest size. Thus, chest dimensions are im- of Mexican-American children as the control portant determinants of both within and be- and from 7.7-11.9% when using the Polgar tween sample variation in lung volumes, a and Promadhat standards as the control. It finding that is consistent with the results of thus appears that growth and development previous studies (Frisancho, 1969; Greksa et at high altitudes have a small to moderate, although statistically significant, effect on al., 1987; Mueller et al., 1978). %FEV in the La Paz Europeans, after con- the average lung volumes of children of Eutrolling for anthropometry, was within the ropean ancestry. It would be interesting to normal range found at low altitude (Lange determine the extent to which the differences Anderson et al., 19841, which is consistent in lung volumes between the La Paz Eurowith the finding of Boyce et al. (1974) of no peans and the low-altitude controls are realtitude effect on %FEV. The estimates of the lated to differences in thoracic morphology effect of growth and development at high but, unfortunately, the data needed to test altitude on the lung volumes of the La Paz this hypothesis are not available. Europeans were all statistically significant If, as argued earlier, the mean lung vol(Table 4; p < .001). The relative magnitude umes of the La Paz Europeans are not greatly of the suggested hypoxia-induced increase in affected by Amerindian admixture, one may the FVC and FEV of the La Paz Europeans conclude that the lung volumes of these chil- 84 L.P. GREKSA ET AL. dren represent an unmediated (by genetic adaptation to hypoxia) developmental response to chronic hypoxia. Since lung volumes are significantly greater in La Paz Aymara than La Paz European children (by about 4.7%, on average), after controlling for body and chest size, it follows that factors other than growth and development at high altitude, presumably with a genetic basis, are required to explain the larger Aymara lung volumes. However, since ethnic differences in lung function which are unrelated to altitude are well-documented (Binder et al., 1976; Hsu et al., 1979; Schoenberg et al., 1978), it would be premature, in the absence of studies demonstrating the functional importance of the enhanced Aymara lung volumes, to assume that the ethnic differences found in the present study necessarily reflect genetic adaptations to hypoxia. Amerindian highlanders display an accelerated growth in lung volumes relative t o stature during childhood and especially adolescence (Frisancho, 1969; Frisancho et al., 1973; Mueller et al., 1979). The slopes of the log regressions of FVC and FEV on stature are somewhat greater in La Paz European females than in lowland females but those for males are within the lowland range (Table 5). In contrast, examination of Figure 1 indicates that highland European males exhibit a slight acceleration in FVC relative to stature in comparison to lowland European males after a stature of about 160 cm while females do not. Both the analytic and graphic data used to examine the rate of development of FVC are thus contradictory and neither provides much support for the presence of developmental responses to hypoxia among highland European children. However, due t o individual variation in growth patterns, it may be unrealistic to expect to detect alterations in developmental processes with crosssectional data. Longitudinal data may thus be necessary to unequivocally demonstrate developmental responses to stress (Greksa et al., 1987; Mueller et al., 1978). In conclusion, the data from the present study suggest that growth and development under conditions of chronic hypoxia have a relatively small, although statistically significant, independent effect on the development of lung volumes. Although chest size is clearly an important determinant of intraindividual variation in lung function, it is not clear to what extent it is involved in explaining the differences between lowland and highland Europeans. Finally, it is unclear if the increased lung volumes of the La Paz European children are acquired through an accelerated development of lung volumes relative to stature during adolescence, as is found among Amerindian highlanders. 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