EFFECTS OF A BASKETBALL ACTIVITY ON LUNG CAPILLARY BLOOD
VOLUME AND MEMBRANE DIFFUSING CAPACITY, MEASURED BY NO/CO TRANSFER
of Physiology and Lung Function Testing, Faculty of Medicine of Sousse,
2Department of Physiology EA 518, Victor Segalen University, Bordeaux,
3Laboratory of Physiology, Faculty of Sciences of Tunis, Tunisia
30 December 2005
Journal of Sports Science and Medicine (2006) 5, 431 - 439
Google Scholar for Citing Articles
|In both children and adults, acute exercise increases lung capillary
blood volume (Vc) and membrane factor (DmCO). We sought to determine
whether basketball training affected this adaptation to exercise in
children. The purpose of this study was to determine the effects of
two years sport activity on the components of pulmonary gas transfer
in children. Over a 2-yr period, we retested 60 nine year old boys
who were initially separated in two groups: 30 basketball players
(P) (9.0 ± 1.0 yrs; 35.0 ± 5.2 kg; 1.43 ± 0.05 m), and matched non
players controls (C) (8.9 ± 1.0 yrs; 35.0 ± 6.0 kg; 1.44 ± 0.06 m)
who did not perform any extracurricular activity, Vc and DmCO were
measured by the NO/CO transfer method at rest and during sub-maximal
exercise. Maximal aerobic power and peak power output was 12% higher
in the trained group compared to matched controls (p < 0.05). Nitric
oxide lung transfer (TLNO) per unit lung volume and thus, DmCO per
unit of lung volume (VA) were higher at rest and during exercise in
the group which had undergone regular basketball activity compared
to matched controls (p < 0.05). Neither lung capillary blood volume
nor total lung transfer for carbon monoxide (TLCO) were significantly
different between groups. These results suggest that active sport
can alter the properties of the lung alveolo-capillary membrane by
improving alveolar membrane conductance in children.
WORDS: Membrane diffusing capacity, pulmonary capillary blood
volume, alveolar volume, children, NO/CO transfer.
transfer capacity for CO (TLCO) is a widely used test
aimed at the estimation of the function of the alveolo-capillary
structure. The Roughton and Forster model (1957)
allows separating this function in two variables: membrane factor
(Dm) and pulmonary capillary blood volume (Vc). Membrane factor
(Dm) and pulmonary capillary blood volume (Vc) can be estimated
by the two-step TLCO method during which the subject
inhales O2 at different concentrations (Lewis et al.,
Membrane factor and lung capillary blood volume have also been measured
with the more recent TLCO/NO technique (Guénard et al.,
Moinard and Guénard, 1990).
This one step method has been applied to exercise in adults with
either the single breath method (Manier et al., 1993;
the rebreathing method (Tamhane et al., 2001)
or the steady state method (Borland et al., 2001).
The reaction rate of NO binding to haemoglobin (Hb) being some 280
times faster than that of carbon monoxide, the limitation of NO
transfer is due mainly to the membrane component of the transfer.
Basketball is a sport with many very fast changes in metabolic activity
requiring rapid adaptation to alterations in oxygen demand which
would implicate a specific adaptation of the lung. High-intensity
intermittent running has been shown to increase ventilatory performance
(forced vital capacity, peak flow, and forced expiratory flow) (Nourry
et al., 2005)
suggesting that intermittent exercise enhances the respiratory demand
as well as it enhances the cardiac demand (Paterson, 1979).
This prompted us to evaluate the effect of two years basketball
activity on the transfers of NO and CO in a group of basketball
playing children compared with a control group without specific
sports activity. Lung transfer components were studied in these
children using the TLCO/NO single breath method. Lung
volume, lung capillary blood volume and membrane factor were calculated
at rest and
study was conducted in a longitudinal period of two years with sixty
healthy boys (8-10 years). All were non-smokers with normal lung
volumes and flow-volume curves at rest and no history of cardiopulmonary
disease or allergy (Table 1
and Table 2). Children who
volunteered, with the agreement of the parents, to participate in
the study were allocated according to their physical activity. One
group consisted of basketball players while the other group was
children without specific sport activity. The first 30 children
who volunteered to participate in this last group were included.
Information regarding past health and activity was obtained from
a questionnaire (Ferris, 1978)
in order to obtain a socio-economically homogeneous population.
Children were selected from the city or the suburbs of Sousse (Tunisia).
This lightly industrialized area is only slightly polluted. Tunisia
is a melting pot of white populations from the Mediterranean basin.
Written informed consent was obtained from all parents and the University
approved the experimental protocol.
Before the 2-yr period, the subjects were allocated into two groups:
Players (P children): 30 children who performed basketball
training for two hours five times per week during two years, with
one month interruption in summer.
Control (C children): 30 children participated in normal
school physical activities with no extracurricular sporting activity.
Initially (test 1) anthropometric data were collected. Maximal O2
consumption (VO2max) and maximal aerobic power (MAP)
were determined by a standard protocol. Exercise was performed on
a bicycle ergometer (Monark cycle). The child performed unloaded
cycling at 60-65 revolutions/min (rpm) for the first minute after
which the work rate was increased every minute according to the
Cooper and Weiler-Ravell equation (Cooper and Weiler-Ravell, 1984)
until maximal oxygen uptake was reached. Oxygen consumption and
carbon dioxide production were measured with a MedGraphics CPX (St
Paul, MN, USA). The oxygen and carbon dioxide analyzers as well
as the flow meter were calibrated before each measurement.
On another day, the transfer of NO and CO were measured. Each child
performed three validated transfer measurements: two at rest before
exercise and one during exercise at about 75-85% of maximal aerobic
power. Exercise was performed as previously using the incremental
procedure. The validity of the manoeuvre for the transfer measurement
was checked first by looking at the child who should perform the
manoeuvre without hesitation, with his mouth tightly closed around
the mouth-piece, holding his breath steadily during the preset time.
The validity was then checked on the screen looking at the trace
depicting changes in volume during the manoeuvre. This trace should
be devoid of pause during the fast inspiration, flat during breath
hold and continuous during the fast following expiration. If these
criteria were met the results were validated. All children were
trained previously to the manoeuvre without inspiring the mixture.
If one measurement at rest was not accepted for any reason, another
measurement was made after recovery when heart rate had reached
its resting value. As the single-breath manoeuvre was difficult
to perform during exercise for some children (9/60), they were allowed
to interrupt exercise for less than one minute. Measurements were
made at the start of the pause. The results of these nine individuals
were compared to those of the remaining population. As there were
no differences in membrane factor, lung capillary blood volume and
lung volume between these individuals and the other children, their
results were included in the overall population.
NO and CO transfers, i.e. TLNO and TLCO, were measured simultaneously
during a single breath manoeuvre (SB) using an automated apparatus
(Medisoft Dinant, Belgium). The inhaled mixture was obtained by
mixing the gases of two tanks one containing 0.28% CO, 14% He, 21%
O2 balanced with N2 the other 450 ppm NO in N2 (Air Liquide
Santé, Tunisia). The final concentration of NO in the inspired bag
was 40 ppm. The apparatus was calibrated daily with the mixtures
contained in the tanks using automated procedures. Linearity of
the analyzers was factory checked. The pneumotachograph (PTG) was
calibrated with a 2L syringe.
The child breathed through a mouthpiece and a filter connected to
the PTG. When needed, he was requested to make a deep expiration.
Then at the onset of the next inspiration, a valve opened allowing
the child to inspire the mixture during a rapid deep inspiration.
An apnoea of 4 seconds was then requested followed by a deep expiration.
The first 0. 6L of expired gas was rejected as the further 0.6L
was sampled in a bag which was automatically analyzed for NO, CO
and He. The delay to analyse the sample of expired gas was constant,
35s. The lung volume during the apnoea was calculated using the
helium dilution technique. The reproducibility of the method was
tested in 12 children who performed six consecutive trials on different
Two years afterwards (test 2), the same tests (anthropometric data,
maximal O2 consumption, maximal aerobic power, and NO/CO
transfer) were repeated. All of the resting tests and exercise measurements
were performed on the same equipment, were calibrated using the
identical method, and were measured with the exact same laboratory
techniques for the initial and the follow-up tests.
protocol: DmCO vs VA
In order to check the DmCO vs VA relationship in a given individual,
12 basketball-playing children performed at rest on another day,
TLCO/NO manoeuvres at different lung volumes (about 50, 75 and 100%
of their vital capacity) (Figure
1). After the deep exhalation, they were requested to fill their
lung with the inspired mixture to a preset value indicated on the
screen by the operator.
Membrane factor (DmCO) and lung capillary blood volume (Vc) values
were derived from TLNO and TLCO values as previously described (Guénard
et al., 1987).
In brief the reactivity of NO on hemoglobin was considered very
high and its inverse negligible, therefore TLNO value was considered
equivalent to DmNO. DmCO was calculated by estimating the coefficient
of proportionality (a) of the Dm values of the
two gases to be 1.97. The reactivity of CO with hemoglobin at a
PO2 of 110 mmHg was derived from a work of Forster, 1987
in which measurements were done at physiological pH (Krawiec et
The calculation of DmCO, although not necessary, was made to allow
comparisons with previous data. Reproducibility of the method was
estimated in 12 children who performed the test six times at rest
on different days.
Statistical analyses were performed using Statistica 5. 0 software'97
edition. Student's t-test for unpaired data was used to identify
significant differences between the two groups (players and controls),
while paired data analysis was used to compare rest and exercise
data. A value of p < 0.05 was considered significant. Mean values
are given with the standard deviation (±SD).
initial subject's physical characteristics (test 1) and of the follow-up
study 2 yr later (test 2) are shown in Table
Lung volumes in comparisons with literature data (Cotes et al.,
Sylvester et al., 2005)
are shown in Table 2.
In the 12 children who performed six consecutive trials on different
days, the coefficients of variation with their standard deviations
were 2.1 ± 2.0; 1.4 ± 1.3; 7.3 ± 4.6 % for Vc, TLCO and TLNO respectively.
Initially (test 1), lung volume and lung capillary blood volume
from both groups did not differ either at rest or during exercise,
although they increased significantly in both groups during exercise
(p < 0.01) (Table 3). Two
years later (test 2), lung capillary blood volume at rest did not
differ between the two groups, but increased significantly from
rest to exercise in both groups. The increase in Vc was greater
in the control group.
Vc/VA ratios in test 1 were not different between groups either
at rest or during exercise, although they increased by 16% in the
P children and 22% in the C children from rest to exercise in test
2 (Table 4). As VA increased
significantly with age Vc at rest decrease significantly only in
P children between test 1 and test 2 and the Vc/VA ratio decreased
with age. DmCO and VA increased significantly from rest to exercise
in both groups in all conditions. P children increased their DmCO
significantly during exercise between test 1 and 2. P children had
greater DmCO at rest and during exercise in test 2 than C children.
DmCO/VA ratios were higher in the P than in the C children in all
paired conditions, however the difference was significant in test
2 between the two groups. While DmCO/VA increased from rest to exercise
in test 2 in the P children it decreased in the C children (Table
4). DmCO/Vc ratios were always higher in the P group than in
the C group, the differences were significant during exercise during
In the 12 subjects who performed measurements of transfers at different
lung volumes the relationship between membrane factor and lung volume
was linear (Figure 1), the
ratios DmCO/VA in (min·mmHg-1) were not different irrespective
of the value of VA as a percentage of its maximal value: 12.2 ±
1.1 for lung volume 54.3 ± 6.9%, 11.8 ± 0.8 for lung volume 73.1
± 13.2%, 12.4 ± 1.0 for lung volume 100%. Compared to the two lower
lung volume levels, lung capillary blood volume increased slightly
but significantly at 100% VA (Figure
study provides evidence that sporting activity has an influence
on the alveolo-capillary membrane properties of children. The main
difference was in DmCO which was higher during exercise in the P
children after a 2 year basketball training period.
Vc and Dm were calculated using a previously described method in
which reactivity of CO for hemoglobin was not taken from the early
work of Roughton and Forster, 1957
but from the more recent work of Krawiec (1983).
The reason for that choice is that the latter work was performed
at pH 7.4 as the former was performed at pH 8. As pointed elsewhere
the use of this more recent value of the reactivity of CO for hemoglobin
leads to 15 to 20% smaller Vc and 15 to 20% greater DmCO
values. Choosing the recent equation (Krawiec, 1983)
gives results in agreement with the theoretical value of the coefficient
a (a = 1.97), as using the early work of Roughton and Forster, 1957
needs to change empirically the value of "a" to 2.4 (Hsia,
Vc depends on hemoglobin (Hb) concentration which was assumed to
be normal in our subjects. This concentration was not measured for
two reasons. Firstly the University ethics committee did not permit
venous puncture in healthy children. Secondly as the children had
a similar socio-economic status, as verified by the questionnaire,
they had no reason to have great differences in their haemoglobin
concentrations. Stam et al., 1994
found in a healthy adult group that Hb concentration had no impact
on the mean CO transfer value and its standard deviation, as Hb
concentration was normally distributed within a narrow range. The
coefficients of variation for lung capillary blood volume were 25%
and 15% in the P and C groups respectively, in the range reported
in the literature.
Lung volumes: The values of lung volume at rest are in agreement
with those measured in other populations of children (Hamilton and
The P children were a few centimetres taller than the C children,
but values of lung volume did not differ between the two. This finding
is in agreement with that of Gaultier and Crapo, 1997
who found that swimming was the only physical activity leading to
a marked increase in lung volumes in children. The increase in lung
volume from rest to exercise in both groups of children was attributed
to a greater inspiratory drive resulting in a better contraction
of respiratory muscles. Changes in lung or chest mechanics could
lead to such an increase, but seems unlikely for such short exercise
durations. However, the fact that children have high thoracic compliance
(Ingimarsson et al., 2000)
would enhance the alterations in maximal lung volume due to changes
in inspiratory drive.
oxygen consumption: Maximal oxygen consumption related to body
mass in healthy children depends on age, gender and ethnicity (Turley
and Wilmore, 1997).
Eleven-year-old Negro boys (Maksud et al., 1971)
as well as 45 pre-pubertal North American children (Andreacci et
or 11-13-year-old Turkish boys (Binyildiz, 1980)
had values similar to those reported here. White pre-pubertal American
boys had values close to those of our P children (33.7 ± 6.4 vs
33.85 ± 7.6 ml·min-1·kg-1) respectively). The difference
between the group of children practicing a sport and those who did
not (12%) was greater than that reported by Mandigout et al., 2001
for boys (4.6%). The difference between these groups depends on
the physical activity of the non-practicing group as well as the
type and level of sporting activity of the practicing group.
volume: In test 2 and at rest, Vc/VA in both groups of children
was around 13 ml·L-1, a figure close to that reported by others
in young adults (16-20 years): 14 ml·L-1 by Mahajan et al., 1992.
This suggests that lung capillary growth parallels lung parenchyma
growth at least between the age of ten and young adulthood. Higher
values have been found in adults: 16.5 ml·L-1 by Manier et al.,
15.5 ml·L-1 by Zavorsky et al., 2004.
During exercise, Vc/VA increased by 16% in the player group and
22% in the control group with no significant difference between
the two. In adults, the values are dispersed: 10% for 12 professional
handball players (Manier et al., 1993),
nearly 40% for 18 young adults (Zavorsky et al., 2004)
and 70% by Hsia et al., 1995
using a rebreathing method. We will discuss below the possible implication
of cardiac blood flow in the dispersion of Vc values during exercise.
The increase in Vc during exercise has been attributed to the recruitment
of capillaries as well as their increase in diameter (Goresky et
Hsia et al., 1992;
Manier et al., 1993;
Wagner et al., 1986;
Vaughan et al., 1976).
However well correlated to cardiac blood flow, DmCO as well as Vc
are not directly dependent on blood flow as shown by Borland et
who observed in an analogue model of the lung that neither TLCO
nor TLNO were blood flow dependent. Exercise by increasing cardiac
blood flow (Q'c) increases pulmonary arterial pressure (Ppa) and
pulmonary capillary pressure (Pcap) which would induce an increase
in Vc by recruitment and distension of capillaries. The link between
the increase in Pcap and that in Vc is rather complex as suggested
by Baumgartner et al., 2003
using in vivo video microscopic observations. This type of analysis
in vivo in healthy human is impossible as Pcap can be measured only
invasively and no method exists, at this time, to estimate the microscopic
distribution of blood flow.
Alveolo capillary membrane: DmCO and VA increased significantly
from rest to exercise in both groups in all conditions. The P children
had higher DmCO/VA ratios during exercise than did C children, the
ratio was significantly different only in test 2 (Table
4), i.e. for the same lung volume, P children had 12 to 16%
more DmCO than did C children.
With the present method, DmCO was derived directly from TLNO. As
NO is highly reactive with haemoglobin, its transfer is nearly independent
of Vc but highly dependent on membrane properties. Dm is a function
of membrane thickness and lung surface area. An increase in cardiac
blood flow could decrease the thickness of the unstirred plasma
layer, close to the capillary wall, which is suspected to increase
the effective membrane thickness. However this would hold to be
true in both groups and could not explain the difference between
the two groups of children. Another attractive hypothesis is that
the alveolo-capillary membrane of trained children being submitted
to a greater stretch, owing to their greater maximal ventilation,
becomes thinner during exercise. Indeed intermittent exercise has
been shown to increase respiratory muscle force (Nourry et al.,
In this respect it has been shown that an increase in lung stretch
induces release of growth factors (Yamamoto et al., 2001)
which in turn could increase the surface of the lung.
An increase in lung surface could be due either to an increase in
the effective lung surface or to less heterogeneity in the distribution
of the perfusion of capillaries leading for a given Vc to a greater
surface of exchange. These two points will be examined successively.
An increase in the number of alveoli per unit volume would increase
the surface area, which would also increase lung mass. To our knowledge
there are no reports of lung mass in children practicing sports.
In adults, Manier et al., 1993
reported a lung mass of 1372 ± 178 g in marathon runners at rest
and Guénard et al., 1992
reported a lung mass of 997 ± 35 g in 16 healthy, non-sport-practicing
adults using the same method and material (tomodensitometry of the
lung). Mean lung densities at FRC were significantly different (0.37
± 0.044 and 0.29 ± 0.064 respectively).
As it seems that no data exists in the literature on the distribution
of perfusion within lung capillaries the fact that the ratio Dm/Vc
is significantly greater in P than C children during exercise in
test 2 suggest that the distribution of blood in capillaries is
more even in P than C children. Dm/Vc increased insignificantly
from rest to exercise in both groups during the first test as, after
a 2 yr period, this ratio decreased significantly much less in P
children than in C children from rest to exercise (Table
In conclusion, player children had greater DmCO/VA and DmCO/Vc
ratios than did control children during exercise. The mechanisms
by which basketball playing children were thought to improve lung
diffusion are speculative either via an increase in the effective
exchanging lung surface area or/and by a decrease in membrane thickness.
Further work will be required to determine the kinetics of the alteration
in Dm when children switch from non players to players status or
would like to thank Pr Youssef Féki for his comments on the manuscript,
and Dr Haythem Debbabi and Mr Mâamoun Ben Jabrallal for their technical
assistance. This work is financially supported by the Tunisian ministry
of scientific research, the technology and the development of competences.
Trained children had greater DmCO/VA and DmCO/Vc ratios compared
with control children during exercise.
mechanisms by which basketball playing children were thought to
improve lung diffusion are speculative.
work will be required to determine the kinetics of the alteration
in Dm when children switch from non players to players status
Employment: Professor of physiology at the Institute of
Sport and Physical Education of Kef, Tunisia.
Research interest: Respiratory physiology and sport sciences
Employment: Doctoral student in Respiratory Biology in the
Faculty of Medicine of Bordeaux, France.
Research interest: Respiratory physiology
E-mail: glenet firstname.lastname@example.org
Employment: Professor of physiology and head of physiology
department of faculty of medicine Ibn El Jazzar, Sousse. Tunisia.
Degree: MD, PhD.
Research interests: Respiratory physiology/Muscular exercise
Employment: Professor of physiology at the Faculty of Sciences
of Tunis, Tunisia.
Degree: MD, PhD
Research interest: Respiratory physiology
Employment: Professor of physiology at Bordeaux University
Degree: MD, PhD.
Research interest: Respiratory physiology, mainly gas
exchange and mechanics