Lung growth of pre-adolescent children M. B

Eur Respir J
1990, 3, 91-96
Lung growth of pre-adolescent children
M. Smeets, B. Brunekreef, L. Dijkstra, D. Houthuijs
Lung growth ofpre-adolescenJ children. M. Smeets, B. Brunekreef, L. Dijkstra,
D. Houthuijs.
ABSTRACT: Lung growth was studied 1n 420 Dutch children aged 6-11
yrs. J?orced vital capacity (FVC), forced expiratory volume In one second
(FEV 1), peak expiratory now (PEF) and maximal mJd-expiratory now
(MMEF) were measured four times over a 2.5 yr period with a rolling-seal
spirometer. In boys, pulmonary function Increased with approximately the
same velocity at all ages studied. ln girls, however, Ute growth velocities of
FVC and _F~~ Increased markedly at age 10 yrs, and growth velocities of
PEF and iVIMt.:F had increased already at age 9 yrs. The minimum pulmonary f11oction growth velocity could not be determined from the available
data in boys. In girls, the minimum pulmonary function growth velocities
preceded the minimum height growth velocity at the onset of the pubertal
growth spurt. All lung function growth rates were significantly associated
with the growth rate of height3 • In girls, the growth rate of FVC was also
associated wlth the weight growth rate. There was also some association
between the growth rates of PEF and MMEF and age. In boys, there was
a negative association between age and tbe growth rates of FVC and FEV1 ,
after adjustment for the growth rate of beight3•
Dept of Environmental Health, University of
Wageningen, The Netherlands.
Correspondence: Dr B. Brunekreef, Dept of
Environmental Health, University ofWageningen, P.O.
Box 238. 6700 AE Wageningen, The Netherlands.
Keywords: Children; growth; lung function.
Received: March 24, 1989; accepted for publication
July 28, 1989.
This study was supported by a grant from rhe
Netherlands Asthma Foundarion.
Eur Respir J., 1990, 3, 91-96.
Several studies have been published on pulmonary
function in childhood, often with a primary interest in
establishing reference values. Hence, most of these studies had a cross-sectional character relating the level of
respiratory function to variables such as age, height and
weight [1-5]. Information about the growth of respiratory function collected by means of longitudinal studies
is, however, limited. There have been some studies on
growth of pulmonary function in adolescence [6, 7). These
have indicated that in the pubertal growth spurt the peak
in the growth rate of forced vital capacity (FVC) and
forced expiratory volume in one second (FEV1) occurs
about 0.5-1 yr later than that in the height growth rate.
Few data have been published on lung function growth
(as opposed to level) of pre-adolescent children. A preliminary report from the Harvard Six Cities Study [8)
suggested that there is no time lag in the pre-adolescent
minimum growth rate of FEV1 relative to the minimum
height growth rate.
We have studied the development of pulmonary function in 6-11 yr old children in relation to several environmental factors. Repeated observations were made over
a period of 2.5 yrs. thus creating the possibility to assess
changes in lung function and height growth in this age
group.
The present report attempts to provide a description of
the growth of pulmonary function in relation to age and
the growth rates of height and weight in 6-11 yr old
children, with special emphasis on differences between
boys and girls.
Materials and methods
The study sample consisted of 420 children of 6-11
yrs in age. There were 206 boys and 214 girls. The
children were from a study on the relationship between
indoor air pollution and respiratory health, in which
repeated observations were made over a 2.5 yr period.
In 1984, the parents of 997 children were invited to let
their children participate. The children were 6-9 yrs old,
and the parents were contacted through ten schools
located in four small, non-industrial communities in the
south-east of The Netherlands. Of the 997 contacted. 832
(84%) were granted permission. In 1986, the parents of
702 of these children were again contacted for a followup study. Of the original 832, 88 had left the area, and
42 could not be included because their school refused to
participate. Of the 702, 614 were allowed to participate
in the follow-up study (88%).
Pulmonary fu nction of all of the children was
measured in the schools by trained technicians, using
Vicatest-5 rolling-seal spirometers coupled with a microcomputer. Forced expiratory manoeuvres were performed
whilst sitting, without a nose-clip. Each child was
required to perform at least five acceptable forced expirations from a maximum of eight attempts. PVC, FEV1 ,
92
M. SMEETS ET AL.
peak expiratory flow (PEF), maximal expiratory flow
when x% remains to be exhaled (MEF.J and maximal
mid-expiratory flow (MMEF) were recorded at each
effort. In this report, results for FYC, FEY1 , PEF and
MMEF only will be discussed. Selection of the lung
function values out of the five measurements occurred
according to the recommendations made for adults [9)
and adolescents [10]. Lung function values were
corrected to body temperature, pressure and saturation
(BTPS). Details of the protocol are given elsewhere [11].
Tests were performed in the fall of 1984, in the spring of
1985, in the fall of 1986 and again in the spring of 1987.
Acceptable data were obtained for 85-89% of all of the
children on each of the four occasions. Of the 6 14
children included in the follow-up study, 420 (68%) had
acceptable data on all four occasions. If the capacity to
perform an acceptable test were uncorrelated between
occasions, only 52% (0.854 ) to 63% (0.89 4) of the
children would have been expected to have acceptable
data on each occasion.
A respiratory symptoms questionnaire [12] was
completed by the parents of the children, and the reported
prevalence of respiratory symptoms was no different in
the 420 children with full pulmonary function data
compared to the prevalence in the total group of 614
children. The prevalence of chronic cough was 3.3% in
the group of 420 children, and 2.5% in the group of 614
children. The prevalence of chronic wheeze was 4.6 and
4.7%, respectively. The prevalence of attacks of
shortness of breath with wheeze was 3.1 and 3.0%,
respectively. The analysis was restricted to the 420
children with full data, as for them pulmonary function
growth could be calculated most reliably.
At the time of the lung function test, standing height
and weight were measured in stockinged feet. Age at
each examination was computed exactly (in yrs) by
dividing the difference between birth date and day of
measurement (days) by 365.25. Growth rates of pulmonary function, height3 and weight over the 2.5 yr period
were estimated by linear regression analysis for each child.
The mean age during the study period was calculated for
each child from the ages at examination. There were
72 children with mean age 7-8 yrs (age category 7);
131 children with mean age 8- 9 yrs (age category 8);
151 children with mean age 9- 10 yrs (age category 9);
63 children with mean age 10-11 yrs (age category 10);
and 3 children with mean age over 11 yrs.
Mean growth rates ofFVC, FEY~' PEF, MMEF, height
and weight have been tabulated according to age
category and gender. A multiple linear regression analysis was performed to investigate the relationship between
growth rates of pulmonary function, and mean age and
growth rates of height3 and weight. The analyses were
performed separately for boys and girls, as a preliminary
analysis had indicated that growth patterns in this age
group were widely different between boys and girls.
Growth rates of pulmonary function were plotted against
the height3 growth rate. There was no apparent nonlinearity (figs 1 and 2). To allow for non-linear
relationships with age, three dummy variables were
created for age, indicating the difference between age
Growth rate of FVC ml·vr1
I
450 •
400
A
A
I
i
l
t
A
A
350 •
I
A A
A
.
8
'
'
AA
I'
200
150
!
100
!
B
A
AA
AA
A
AA
A8 A
A A
A
8
A
A
A
AAA A
ABA
A A BABA AB.A
A
AA .AABB A A
8 ABBC A A AAA
AA AAB A AACA A AA
AAA ABCCASA A A A
8 BABCACB AA
BAABBA CAC
ACAS
BA
AABCA AA
A
AB
AAA
AA
A
AB
AA A AAB
A A A AA
AC
!'
..''
!
A A
AA
A
300 :
250
A A
A
I
'
'
i
..
''
I
.
A
''
'
!
so •
l
- --+- ..... --................ --- .. -- ....... ----- .. - ... -- ·--- .... --........... - ................
0.1
0.2
0.3
0.4
0.5
+---..--......... ·-..
0.6
0.7
Growth rate of helghtl m3·yr'
Fig. I. - Scauerplot of growth rates of FVC and height' in 214 Dutch
gids. FVC: forced vital capacity; A: 1 obs; B: 2 obs, etc.
Growth rate of FVC ml·yr'
I
A
450 •
I
A
400 •
A
!
A
i
A
A
A A
A
350 :
lOO
AA
l
A
AA
AA A
A 8
!
A
l
250 ;
A
A
I!
AA
150 •
i
A
A
A
A
A
A
A 8
!'
A
A
AAAAA A
A
A BAAA AB
A
AA A CAAA
AAAA ABA 8 A
A A
A
AAAACA AA A A A
BA A888
AAA A
A 8 ABBBAA
I
A
A
8
BAA ABAA
A A 8
CAB A 8
A A A ABCACAA A
A
AB A A A 88
A
A
A
A
AA AA
A
8
AAA A
A
AAAA
AAA
A
200 •
A
A A
A
A
A
100 :
I
A
so .
.I . . -+----....................... +------- '"-·- - ......... ·---- 0.1 5
0.20
0.25
0.30
0.35
t - ..... .... ·+- ......................
0.40
0.45
0.50
----+-0.55
3
Growth rate of height" m ·yr'
Fig. 2. - Scatterplot of growth rates of PVC and height' in 206 Dutch
boys. For abbreviations see legend to figure l.
LUNG GROWTH OF PRE-ADOLESCENT CHILDREN
categories 8, 9 and 10 and reference age category 7. The
three children with mean age over 11 yrs were excluded
from this analysis. Residuals from the calculations were
plotted against predicted values 1.0 check for remaining
trends in the data. Statistical analyses were performed
using the SAS system on a VAX mainframe computer.
Results
The distributions of the lung function growth rates were
generally symmetrical, and medians were closely similar
to means in all cases. As examples, the distributions of
the growth rates of FVC are shown in figs 3 and 4 for
girls and boys separately.
Table 1 shows the mean growth rates of pulmonary
function, height and weight for girls by age category.
Growth rates of FVC, FEV1 and weight were the same
at mean ages 7 and 8 yrs, and increased at ages 9 and 10
yrs. The height growth rate was greatest at ages 7 and 10
yrs, and lower in between. Growth rates of PEF and
MMEF steadily increased over the whole age range.
Growth rates at mean age 11 yrs are shown for
completeness only, as there were just two girls in this
category.
93
Table 2 shows the mean growth rates of pulmonary
function, height and weight for boys by age category.
Distributions were again generally symmetrical within
age categories. Growth rates of FVC and FEV1 were
approximately the same at all ages. The growth rate of
the PEF was variable. Growth rates of height and MMEF
decreased with increasing age, whereas the growth rate
of weight increased with age. Growth rates at mean age
11 yrs are shown for completeness only, as there was
just one boy in this category.
·
Table 3 contains the results of the regression analysis
for girls. All pulmonary function growth rates were
related to the height3 growth rate. In addition, the growth
rate of FVC was associated with the weight growth rate.
There was also some association between the growth
rates of PEF and MMEF and age.
Table 4 shows the results of the regression analyses
for boys. Again, the growth rate of height3 was significantly associated with the growth rates of all lung
function variables. After adjustment for the height3 growth
rate, there remained some negative association between
age and the growth rates of FVC and FEV1 .
Stem leaf
#
Stem leaf
44
42
40
38
36
34
32
30
28
26
24
22
20
18
16
14
12
10
8
44
42
40
38
36
34
32
30
28
26
24
22
20
18
16
14
12
10
8
4
3
21
098
2
3
1
9
44672
0014922234469
035660144889
0247045556
0222233678999000234567799
00123455677778990224455557
111223334788999901122222333357777899
1223456666777790133445677777799
136899990134466779
02227904889999
3471233889
4078
45
5
13
12
10
25
26
36
31
18
14
10
4
2
----+----+----+----+----+----+----+Fig. 3. -Stem-and-Leaf display of the distribution of growth rates of
FVC in a population of 214 Dutch girls aged 7- 11 yrs. Growth rate
of FVC in ml·yr 1• There were (e.g.) four girls with growth rates between 100 and 120 ml·yr 1; their respective values were 104, 110, 117
and 118 m1·yr·• (10 4078). FVC: Forced vital capacity.
11
8
1
1
1
3
5
6
143
61
2556
713578
047801233566699
000001267723456
01 136677833344677
0001223345600111222333344456778888
001233556788890001234556889
11233466678899122334679
1456689000222355666788899
02445501133337788
055825589
038
2
4
6
15
15
17
34
27
23
25
17
9
3
288
3
----+----+----+----+----+----+---Fig. 4. - Stem-and-Leaf display of the distribution of growth rates of
PVC in a population of 206 Dutch boys aged 7-11 yrs. Growth rate of
FVC in ml·yr·•. There were (e .g.) three boys with growth rates between
380 ana 400 ml·yr'; their respective values were 381, 384, and 393
ml·yr 1 (38 143). FVC: forced vital capacity.
Table 1. - Mean growth rates of pulmonary function, height and weight in 214 Dutch girls aged 7-11 yrs
Growth rate
of:
Age category
7
1
FVC ml·yr
FEV1 ml·yr· 1
PEF ml·s· 1·yr
MMEF ml·s·1·yr
height cm·yr·1
weight kg·yr· 1
n
210
161
419
125
6.10
3.19
36
8
(44)
(39)
(179)
(112)
(0.56)
(1.03)
209
167
459
147
5.70
3.05
67
10
9
(48)
(41)
(203)
(97)
(0.69)
(0.88)
227
185
524
164
5.78
3.48
76
(72)
(61)
(218)
(106)
(1.00)
(1.18)
252
214
581
230
6.12
3.97
33
11
(62)
(58)
(216)
(238)
(1.14)
(1.26)
291
286
683
381
7.46
5.09
2
Values are mean and standard deviation in parentheses. FVC: forced vital capacity; FEV1 : forced expiratory volume in
one second; PEF: peak expiratory flow; MMEF: maximal mid-expiratory flow.
·
·
·
M. SMEETS ET AL.
94
Table 2. - Mean growth rates of pulmonary function, height and weight in 206 Dutch boys aged 7-11 yrs
Growth rate
of
Age category
7
FVC ml·yr· 1
FEV1 ml·yr- 1
PEP ml·s· 1·yr
MMEP ml·s·'·yr
height cm·yr-1
weight kg-yr- 1
246
190
390
149
5.93
2.64
n
8
(43)
(43)
(201)
(103)
(0.55)
(0.60)
(63)
(51)
(175)
(108)
(0.56)
(1.01)
249
187
492
134
5.60
2.93
36
10
9
229
175
432
124
5.36
2.98
64
(59)
(43)
(212)
(97)
(0.61)
(0.83)
238
179
468
119
5.32
3.48
11
(81)
(73)
(204)
(108)
(0.81)
(1.56)
30
75
214
218
265
259
4.43
2.73
1
Values are mean and standard deviation in parentheses. For abbreviations see legend to table 1.
Table 3.- Association between lung function growth rates and mean age and growth rates of height and weight
in 212 Dutch girls aged 7-10 yrs
Lung
function
variable
FVC
PEV1
PEP
MMEP
Regression coefficients (SE) of:
Intercept
Age 8 yrs
11
-4
172
-19
(14)
(13)
(72)*
(38)
4
9
45
25
(8)
(8)
(42)*
(22)
Age 9 yrs
-2
8
81
25
(8)
(8)
(41)*
(22)
Age 10 yrs
-4
15
106
72
(10)
(9)
(50)*
(26)**
Growth rates of
weight
height3
7
1
7
2
(3)*
(3)
(16)
(8)
569
521
718
440
(50)***
(46)***
(251)**
(132)**
R2
0.573
0.545
0.128
0.157
Coefficients in ml·yr·1, or ml·s· 1-yr- 1 (ages 8, 9 and 10, compared to age 7); ml·yr- 1 per m'·yr·1 or ml·s· 1·yr·1 per m'·yr- 1
(height'); ml·yr· 1 per kg·yr 1 or ml·s· 1·yr·1 per kg·yr- 1 (weight);*: p<0.05; **: p<0.01; ***: p<O.OOl. For abbreviations see
legend to table 1.
Table 4. -Association between lung function rates and mean age and growth rates of height and weight in 205
Dutch boys aged 7-10 yrs
Lung
function
variable
PVC
FEV1
PEP
MMEF
Regression coefficients (sE) of:
Intercept
53
43
123
30
(22)*
(19)*
(82)
(44)
Age 8 yrs
Age 9 yrs
Age 10 yrs
Growth rates of
weight
height'
-2
-7
92
-17
-28
-23
25
-31
-30
-27
40
-41
6 (4)
2 (4)
22 (16)
-1 (8)
(11)
(9)*
(40)*
(21)
(10)**
(9)*
(39)
(21)
(13)*
(11)*
(49)
(26)
598
475
699
408
(77)***
(66)***
(290)*
(153)**
R2
0.335
0.278
0.099
0.052
Coefficients in ml·yr1 or ml·s· 1·yr· 1, (ages 8, 9 and 10, compared to age 7); ml·yr 1 per m 3 ·yr· 1 or ml·s· 1-yr 1 per m'·yr·1
(height3 ); ml-yr- 1 per kg·yr- 1 or ml·s·1-yr per kg-yr 1 (weight);*: p<0.05; **: p<O.Ol; ***: p<O.OOl. For abbreviations see legend
to table 1.
The residuals of the models were plotted against the
predicted values to check for remaining patterns in the
data. There was no indication in these plots for remaining patterns that would call for additional analyses.
Discussion
The growth rate of height decreased in boys over the
entire age range studied. In girls, there was a decrease
95
LUNG GROWTH OF PRE-ADOLESCENT CHILDREN
from mean age 7 yrs to mean age 8 yrs. followed by an
increase at mean age 10 yrs, indicating that some of the
girls had started their pubertal growth spurt. This was
also apparent from the standard deviation of the height
growth rate, which was twice as high in those 10 yrs old
than in those 7 yrs old. The growth rate of weight
increased with age in the boys over the entire age range
studied, whereas in the girls, the weight growth rates
were comparable in those 7 and 8 yrs old. There was a
clear increase from ages 8 to 9 yrs, and again from ages
9 to 10 yrs.
VENROOD-USSELMUIDEN [13) measured height and weight
growth rates in Dutch children over a one year period in
1970-1972. Height growth rates in boys were 5.4, 5.0,
4.6 and 4.8 cm·yr1 for boys in the age intervals 8-9,
9-10, 10-11 and 11-12 yrs, respectively. For girls, they
were 5.3, 5.3, 5.5 and 6.3 cm·yr1, respectively. In our
study, the time interval over which the growth rates were
calculated was about 2.5 yrs. The mean age 7, 8, 9 and
10 categories therefore included children who were up to
about 9, 10, 11 and 12 yrs of age at the end of the study.
Although this makes a direct comparison with the earlier
data impossible, it seems that the growth rates found in
1970-1972 were slightly lower than the growth rates found
in this study. The mean weight growth rates found
by VENROOU-USSELMUIDEN (13) were 3.1, 2.9, 2.9 and
3.5 kg·yr 1 for boys in the age intervals 8-9, 9-10, 10-11
and 11-12 yrs. respectively. For girls, they were 3.1 , 3.2,
3.7 and 5.0 kg·yr1, respectively. These growth rates for
weight were, therefore, very comparable to those
estimated in this study.
In boys, the growth rates of FVC and FEV1 were
somewhat higher in those 7 and 8 yrs old than in those
with mean ages 9 and 10 yrs. In girls, the pattern was
reversed. Also, the growth rates of FVC and FEV1 at age
lO yrs were clearly higher than at mean age 9 yrs. In the
boys, there was no clear variation of the growth rate of
PEF with age. The growth rate of MMEF declined slightly
with age. In the girls, on the contrary, there was a steady
increase of the growth rates of both PEF and MMEF
with mean age over the entire age range studied.
For girls, there was no indication in the data that the
minimum growth rates for FVC, FEV,, PEF and MMEF
lagged behind the minimum growth rates for height and
weight. Apparently, the time lag noted for FVC and FEV1
growth rates at the end of the growth spurt [6, 7] is not
present at the beginning. For boys, who enter their growth
spurt at a higher age than girls, the data at hand do not
permit a proper analysis of the timing of the minimum
growth rates of the different study variables.
After taking the growth rate of height3 into account,
there was not much residual effect of age and weight on
the lung function growth rates. In girls, there remained
some positive effect of age on the growth rates of PEF
and MMEF, whereas in boys there was a negative association between age and the gro wth rates of FVC and
FEV1, after adjustment for the growth rate of height3•
Apparently, the growth rates of FVC and FEV 1 are
overestimated by the growth rate of heig htl at ages 9 and
10 yrs in boys, but not in girls. A possible explanation
for these patterns is offered by TANNER [14], who noted
that there is a steady increase in the growth rates of both
chest depth and chest width in girls, but not in boys,
from age 7 yrs. These increases are not accompanied by
increases in the growth rates of standing height or sitting
height over the age range studied here. The growth patterns of lung function in children in the age categories
studied by us can be more adequately predicted from the
growth rate of height3 in girls than in boys.
Acktlowledgemerrls: The authors would like to thanlc Prof.
Ph.H. Quanjcr (Physiology Dept,
University of Leiden,
Leiden) for his helpful comments on an earlier version of
the manuscript.
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Croissance pulmoMire d' enfanls pre-adolescenls. M. Smeets,
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RESUME: La croissance pulmonaire a ete etudiee chez 420
enfants hollandais, ages de 6 a 11 ans. La capacite vitale forcee,
96
M. SMEETS ET AL.
le VEMS, le debit expiratoire de pointe et le debit expiratoire
maximum moyen on:t ete mesures a 4 reprises au cmrrs d'une
periodc de 2 ans et derni, au moyen d'un spirometre "rolling
seal". Chez les garyons !'augmentation fonctionnelle pulmonaire a approximativement la meme vitesse a tous les ages etudies. Chez les filles toutefois, la vitesse de croissance de la
capacite vitale forcee et du VEMS augmentent de fayon marquee a l'age de 10 ans alors que la vitesse de croissance du
debit expiratoire de pointe et du debit expiratoire moyen augmentent deja a l'age de 9 ans. La vitesse minimum de la croissance de la fonction pulmonaire n. a pu elre determinee apartir
des donnees disponibles chez les garyons. Chez les filles, les
vitesses de croissance fonctionnelles pulmonaires minimales
prece.dent la vitesse de croissance minimale de la taille, au
debut de la poussee de croissance pubertaire. Tous les indices
de croissance de la fonction pulmonaire sont en relation significative avec le taux de croissance de la taille. Chez lcs filles,
le taux de croissance de la capacite vitale forcee est egalement
associe au taux de croissance du poids. n y avait egalement
quelques associations entre les taux de croissance du debit
expi.ratoire maximum ou du debit expiratoi.re maximum moyen
et l'age. Chcz les gar~ons, on a note une association negative
~nlre l'age et les taux de croissance de la capacite vitale forcee
et du VEMS, apres ajustement pour le taux de croissance de la
taille.
Eur Respir J., 1990, 3 , 91-96.