Influence of Developmental Adaptation on Lung Function at High Altitude

Author(s): A. Roberto Frisancho, Tulio Velásquez and Jorge Sanchez

Source: Human Biology, Vol. 45, No. 4 (December 1973), pp. 583-594
Published by: Wayne State University Press
Stable URL: https://www.jstor.org/stable/41459906
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Influence of Developmental Adaptation
on Lung Function at High Altitude

By A. Roberto Frisancho,1 Tulio Velasquez,2 and Jorge Sanchez3

ABSTRACT

The Forced Vital Capacity (FVC) was measured on a total sample of 104
subjects and residual lung volume (RV) was measured on a total of 36
subjects living at 3840m and 3400m altitude in southern Peru. The Forced
Vital Capacity (FVC) of the high altitude natives, when adjusted for age,
height and weight by covariance analyses, significantly exceeded the values
attained by sea level subjects acclimatized to high altitude in the adult
stage. In contrast, the FVC of the sea level subjects acclimatized to high
altitude in the developmental period was comparable to those attained by
the high altitude natives. These findings suggest that the attainment of in-
creased forced expiratory lung volumes at high altitude are probably in-
fluenced by adaptations which occurred during the developmental period.
The high altitude natives tested at 3840m, despite their markedly
smaller body size, attained a significantly greater mean residual lung volume
than U.S.A. sea level subjects. It is quite possible that the increased residual
lung volume at high altitude may also be influenced by developmental
factors. However, further research is necessary in order to define the com-
ponents of increased residual lung volumes at high altitude.
Among high altitude natives, the best prediction of FVC was obtained
from a regression equation which included the subject's chest circumference
at maximum inspiration, height, weight, and age. For total lung capacity
the best predictive equation included the subject's forced vital capacity,
chest volume, ponderal index, and age.

It has been known for many years that the process of adaptation o
high altitude involves changes in lung volumes. Several investigato
have uniformly demonstrated that the vital capacity and resid
volume decrease upon initial exposure and increase with contin

1 Center for Human Growth and Development and Department of Anthr

pology, 1111 East Catherine, University of Michigan, Ann Arbor, Michigan
48104.
2 Instituto de Biología Andina, Universidad Nacional Mayor de San Marcos,
Lima, Peru.
3 Departamento de Antropología, Universidad Nacional del Cuzco, Peru.

Human Biology , December 1973 , Vol. 45 , No. 4 , pp. 583-594

© Wayne State University Press , 1973

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584 A. Roberto Frisancho et al.

residence at high altitude (Rahn and Ham

1952; Ulvedal et al. 1963; Shields et al. 19
However, these investigations also indicat
complete even after 30 days of residence at
volumes of sea level subjects are lower than
Thus, the extent to which sea level subjects
the same lung volumes as those attained
hibited by high altitude natives is not yet
vestigation of the mechanisms of functiona
(Frisancho et al. 1973), we obtained measu
of both sea level subjects acclimatized to
altitude natives. This paper reports data on
Residual Lung Volume of these subjects l
altitude in southern Peru.

Methods and Materials

Subjects and Location

The study included a total of 104 subjects and was conducted i
locations: (1) 3840m altitude in the city of Puno, and (2) 340
the city of Cuzco, located in the southern Peruvian highlands.
There were 53 subjects tested at the first location (3840m
prising the following groups:

(a) 40 Peruvian high altitude natives. These subjects were bor

raised above an altitude of 3,700m and lived all their lives a
altitudes. They were serving as soldiers at the Army headquart
the city of Puno (3840m). They were of highland Quechua
descent and their parents were highland natives. They all w
blood type О and Rh-K
(b) 13 Peruvian sea level natives acclimatized to high altit
adults. They were born and raised at sea level and moved t
altitude as adults. These subjects were serving on the Navy base
city of Puno (3840m) and had lived at high altitudes from 9 mo
to 2.3 years. They were of highland Indian descent and their pa
were from the lowlands. They were of blood type 0 and Rh+.

There were 51 subjects tested at the second location ( 3400m )

prising the following groups:

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 Altitude Adaptation of Lung Function 585

(a) 20 Peruvian high altitude natives. These subjects were

and raised above an altitude of 3,000 meters and lived all their
high altitudes except for short visits to lower elevations. They
students at the University of Cuzco (3400m) and were of hi
Quechua Indian descent. Their parents were highland natives.
(b) 21 Peruvian sea level natives acclimatized to high altitu
the developmental period of childhood and adolescence. These su
were born below an altitude of 1,000 meters and migrated t
altitudes (above 3,000 meters) between the ages of 2 and 16
They were students at the University of Cuzco (3400m) and wer
mixed highland Indian and southern Peruvian descent ("Mes
Their parents were from the lowlands.
(c) 10 U.S. (White) sea level natives acclimatized to high al
as adults. These subjects were born and raised at altitudes
1,000 meters and moved to high altitudes (above 3,000 mete
adults. Length of continuous residency at high altitude ranged f
months to 2.5 years. They were of northern European desce
were members of the Peace Corps assigned to the region of
Peru.

Pulmonary Function
Forced expiratory volumes. Measurements of Forced Vital Ca
(FVC) were made with a dry spirometer ( Jones-Pulmanor
procedures were the same as employed in our previous investig
(Frisancho, 1969). After practicing the technique several tim
subjects were given three trials. The highest of the three trials
taken as the actual value of Forced Vital Capacity (FVC
measurements were obtained in the standing position. Nose clip
used in all tests.
Residual volume. Residual Lung Volumes were measured at 3840m
by one of the investigators (T.V.) according to standard procedures
using the closed circuit nitrogen dilution method (Cotes, 1965). A
Collins' 9-liter respirometer was used, to which 5 liters of oxygen was
added. The procedure was carefully explained to the subject, the nose-
clip was secured firmly on his nose, and the mouthpiece was positioned
comfortably in his mouth. After 3 to 4 normal respirations, with the
breathing valve turned to the outside air, the subject was instructed to
inhale deeply and then exhale maximally. At the end of this maximal
expiration, the breathing valve was turned to connect the subject with

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586 A. Roberto Frisancho et al.

the spirometer circuit and a sample of alveol

6 minutes of normal respiration, the subjec
maximal expiration and the valve was turned
time, an air sample from the respirometer
consumption and the volume of oxygen used
were read from the records on the Kymogra
eter. The effective dead space of the res
periodically, giving an average of 3195.75
and barometric pressure were recorded to c
(body temperature, ambient pressure, sa
analyzed by a Scholander micrometer gas an
The Residual Volume was calculated acco
formula:

™_Vt(F«,-FcN.) (Vo, -FflO

г AN2 Г fN2
Kv

where
RV = Residual Volume,
Vt = Volume of gas in the respirometer at t
Vo2 = Total volume of oxygen consumption,
FfN2 = Fraction of nitrogen in alveolar air at
Fcn2 = Fraction of nitrogen in the oxygen tan
nation) divided by 100.
Fan2 = Fraction of nitrogen in alveolar air in
room air, divided by 100,
D.S. = Dead Space.

Each subject was tested twice. The inter-test r

was found to be r = 0.95 and the mean inter-test difference was 33 ml.
The Functional Residual Capacity was calculated by adding the Ex-
piratory Capacity and the Residual Volume.

Anthropometry
All subjects were measured through standard anthropometric tech-
niques (Weiner and Lourie, 1969). These included weight (nude),
height, chest width, chest depth, chest length, chest volume (chest
volume in liters = chest width X chest depth X chest length), chest
circumference at rest and at maximum inspiration and expiration,
skinfolds, and skin reflectances. Skinfold measurements were made
with a Lange skinfold caliper at the upper arm, chest-juxtanipple,
chest-midaxillary, and subscapula and were added to give the sum of

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 Altitude Adaptation of Lung Function 587

skinfolds (Weiner and Lourie, 1969). Fat-free weight was cal

from a skinfolds body density equation (Pascale et al. 1956
reflectances (Lasker, 1954) were measured on the inner upp
distal to the axillary region of the arm with a photoelectric refl
meter, Model 6104. Reflectances were obtained with pure b
pure red filters. On each subject and with each filter, at lea
measurements were averaged. Skin reflectance measurements we
made on the subjects tested at 3840m.

Results

The mean and standard deviations of the anthropometric charac-

teristics are given in Table 1. All three Peruvian groups show similar
measurements of body size, with the exception of the stature of the
Peruvian sea level subjects which is significantly ( p < 0.01 ) greater
than that of altitude natives at 3840m. The U.S.A. Whites were taller
and heavier but not fatter than the other groups. The high altitude
natives at 3400m are significantly (p < 0.01) darker than the Peruvian
and U.S.A. sea level subjects. The reflectance values for the sea level
subjects acclimatized young are comparable to those reported for
White and highland Peruvian students (Mazess, 1969), and the reflec-
tance value for the highland natives is quite similar to that reported
for rural highland Indians ( Conway and Baker, 1972 ) .
Because pulmonary function is affected by body size variations,
direct inter-population comparisons in lung volumes are not adequate.
For this reason, through covariance analysis, the Forced Vital Capacity
(FVC) of each population was adjusted for age, weight, and height.
In this manner, the comparison of lung volumes are not affected by
variations in body size.
As can be seen in Table 2, at 3840m the high altitude natives at-
tained an adjusted FVC of 4830 ml. which is significantly (p <0.02)
greater than that attained by the sea level subjects acclimatized to
high altitude in the adult stage (4504 ml.). On the other hand, at
3400m the sea level subjects acclimatized to high altitude prior to
adulthood or during the developmental period attained a Forced Vital
Capacity of 5055 ml. which is equal to that attained by the high alti-
tude natives (4990 ml.). In contrast, the U.S.A. Whites who were
acclimatized at high altitude during adulthood attained a Forced Vital
Capacity of 4573 ml. which is significantly (p < 0.02) lower than the
adjusted Forced Vital Capacity of the high altitude natives (4990 ml.).

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 588 A. Roberto Frisancho et al.

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 Altitude Adaptation of Lung Function 589

Table 2

Covariance Adjustment of Forced Vital Capacity ( FVC ) among

Subjects Tested at High Altitude

Forced Vital
Capacity ( ml. )

Tested Adjusted for age,

Altitude weight, and height
(m) N Groups Mean S. E.

3840 40 High altitude natives 4830.3 69.9

3840 13 Sea level subjects acclimatized as adults 4504.6 122.1
F-Ratio 5.19 p < 0.02
3400 20 High altitude natives 4990.3 128.6
3400 21 Sea level subjects acclimatized during 5055.0 121.5
growth
F-Ratio 0.36 NS
3400 10 U.S.A. Whites1 4573.9 231.6
F-Ratio 5.53 p < 0.02

1 When compared with the h

Mean residual lung volum

natives tested at 3840m, ar
subjects reported by Wil
circuit nitrogen dilution)

Table 3

Age , Height , Weight , and Residual Lung Volumes of High Altitude

Natives Compared to Those of U.S. Sea Level Subjects

High Altitude Sea Level

Natives1 U.S.2
N = 36 N = 69
Mean S.D. Mean S.D. t p

Age (years) 21.2 2.1 22.2 3.2 1.67 NS

Height (cm) 161.3 5.7 178.0 6.9 12.47 p < 0.001
Weight (kg) 62.5 5.2 76.4 11.6 6.84 p < 0.001
Residual lung
volume (ml.) 1585.1 338.9 1301.0 289.0 4.50 p < 0.01
1 Tested at 3840m
2 From Wilmore ( 1969)

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590 A. Roberto Frisancho et al.

study. These data show that, while the high

nificantly (p < 0.001) shorter and lighter,
(p < 0.01 ) greater residual lung volumes, wh
sea level subjects.

Discussion

At 3840m and 3400m, the Forced Vital Capacity of the high altitude
natives adjusted for age and body size was significantly greater than
that of the Peruvian and U.S.A. sea level subjects acclimatized to high
altitude in the adult stage. Similarly, the residual lung volumes of the
high altitude natives tested at 3840m were significantly greater than
those reported for U.S.A. subjects of comparable age but significantly
larger body size. This is in agreement with data reported by previous
investigators (Hurtado, 1932, 1956; Frisancho, 1969; DeGraff et al
1970).
The fact that the F VC of the sea level subjects acclimatized to high
altitude in the developmental period is comparable to those attained by
the high altitude natives would suggest that the attainment of in-
creased forced expiratory lung volumes at high altitude is influenced
by developmental processes (Frisancho, 1970; Frisancho et al. 1973).
Support for this position can be discerned from experimental studies.
Burri and Weibel (1971) showed that rats raised at high altitude
(3450m), when compared to sea level controls, exhibited greater lung
volumes due to an increase in the alveolar and capillary surface area
and an increase in the pulmonary diffusing capacity. In contrast, long-
term exposure to hypoxia in adult rats did not produce differences in
lung size and morphology (Burri and Weibel, 1971). In other words,
these investigations demonstrated that exposure to high altitude hy-
poxia during the developmental period induces the formation of a
larger gas exchange system.
Studies on humans also indicate that Peruvian and U.S. high alti-
tude natives exhibit an increased pulmonary diffusing capacity and
enlarged pulmonary capillary blood volume ( Velásquez and Florentini,
1966; Remmers and Mithoefer, 1969; DeGraff et al. 1970). Further-
more, DeGraff et al. ( 1970 ) suggested that the adult sea level resident
may not acquire increased diffusing capacity at high altitude if this
requires growth of new lung tissue. In other words, the increased lung
volumes of the high altitude natives may reflect a developmental
adaptation of the organism to increase the oxygen transport and
diffusion at the level of the respiratory system. If this is the case, the

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 Altitude Adaptation of Lung Function 591

increased residual lung volume of the high altitude natives ma

be due to the influence of developmental factors. It is also impor
note that at high altitude the attainment of normal aerobic ca
(maximum oxygen intake ) has been found to be influenced by
tions acquired during the period of growth and developmen
ancho et al. 1973).
It is a well known principle that an organism is more sensit
the effects of environmental factors during the period of grow
development than during adult life. Accordingly, it is not sur
that developmental processes may influence the attainment
volumes at high altitude. Indeed, physiological and morpho
studies have demonstrated that many characteristics of the Pe
high altitude native, such as enlarged chest size, increased v
pacity, enlargement of the right ventricle of the heart, and m
nance of high peripheral temperature ( Hurtado et al. 1932; Mon
Monge, 1966; Baker et al. 1967) become apparent during t
velopmental period (Peñaloza et al. 1960; Frisancho, 1969, 1970;
et al. 1971). It should be noted that studies among Ethiopian po
tions also indicate that the increased chest size and vital capaci
the high altitude natives were acquired by lowland subjects res
at high altitude (Harrison et al. 1969). However, in this stu
on age at migration to altitude were not obtained and therefor
influence of developmental factors cannot be properly separat
that of prolonged residence.
According to current studies, population differences in s
flectance are indicative of genetic differences (Lasker, 1954; H
1971; Conway and Baker, 1972). The fact that the sea level s
acclimatized young (in the developmental period) to high a
despite their lighter skin reflectance, attained Forced Expi
Volumes comparable to those of the high altitude natives al
ports the hypothesis of developmental adaptation.
In summary, the Forced Vital Capacity of the high altitude n
when adjusted for age, height, and weight by covariance analy
significantly greater than those of the Peruvian and U.S. sea lev
jects acclimatized to high altitude as adults. In contrast, the
Vital Capacity of the sea level subjects acclimatized to high
during the developmental period was comparable to those of th
altitude natives. These findings suggest that the attainmen
creased forced expiratory lung volumes at high altitude are pr
influenced by adaptations acquired during the developmental p
It is also quite possible that the increased residual lung volu

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592 A. Roberto Frisancho et al.

the high altitude natives are due to the in

factors. However, in order to define the com
ual volume at high altitude, further resea
residing at high altitude is necessary.
In order to test the possibility of predicti
altitude natives tested at 3840m from all the functional and anthro-
pometric measurements, multiple regression techniques were em-
ployed. The statistical procedure was the same as that employed in
our previous study (Frisancho, 1969).
The results indicate that the best predictive equation for Forced
Vital Capacity (FVC) includes measurements of chest circumference
at maximum inspiration (ChCMxI), Height (Ht), Weight (Wt), and
Age (A). The multiple regression was:

FVC (ml) = -6896.7 + 71.46(ChCMxI) + 32.68(Ht) - 24.48( Wt)

+ 55.32(A). S.E. = 347.4 ml.

The best predictive equation for Total Lung Capacity (TLC) in-
cluded measurements of Forced Vital Capacity (FVC), Chest Volume
(ChV), Ponderal Index (PI), and Age (A). The multiple regression
equation was:

TLC (ml) = -6045.5 + 1.06(FVC) + 69.34(ChV) + 138.98(PI)

+ 38.52(A). S.E. = 288.3 ml.

These findings suggest that lung volume among high altitude na-
tives is a function of chest size and body size as well.

Acknowledgments

The authors express their appreciation to Danilo Pallardel of the

Department of Anthropology of the University of Cuzco, Peru, for
his technical assistance, and to Melquíades Huayna of the Instituto
de Biología Andina, Universidad Nacional Mayor de San Marcos, Lima,
Peru. We gratefully acknowledge the facilities provided by the Hos-
pital Regional of Cuzco and the Area de Salud- Hospital Regional of
Puno; the cooperation of the Peruvian Army headquarters at Puno, and
the faculty and students of the University of Cuzco, Peru.
The research was supported in part by Grant HE-13805 of the
Heart and Lung Institute of the National Institutes of Health.

Received: 2 February , 1973.

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 Altitude Adaptation of Lung Function 593

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