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Effect of altitude on the lung function of high altitude residents of European ancestry.

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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.
ACKNOWLEDGMENTS
This study was made possible by the cooperation and assistance of the Instituto Boliviano de Biologia de Altura and the Clinica
Nacional del Deporte, particularly Drs. G.
Antezana, J. Aguilar and P. Desjeux. We also
express our appreciation to the students and
faculty of the Colegio Aleman, particularly
the Director, J. Frank. This research was
supported by a grant from the Office of Research Administration, Case Western Reserve University.
LITERATURE CITED
American Thoracic Society (1979)Standardization of spirometry. Am. Rev. Respir. Dis. 119:2-11.
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