Vol. 87, Issue 3, 902-909, September 1999
Influence of upper airway shunt on total respiratory impedance
in infants
K. N.
Desager1,
M.
Cauberghs2,
J.
Naudts3, and
K. P.
van de
Woestijne2
1 Department of Paediatrics,
University Hospital Antwerp, and
3 Department of Physics,
University of Antwerp, B-2650 Antwerp; and
2 Laboratorium voor
Longfunctieonderzoek, UZ Gasthuisberg, B-3000 Leuven, Belgium
 |
ABSTRACT |
When input
impedance is determined by means of the forced oscillation technique,
part of the oscillatory flow measured at the mouth is lost in the
motion of the upper airway wall acting as a shunt. This is
avoided by applying the oscillations around the subject's head (head
generator) rather than at the mouth (conventional technique). In seven
wheezing infants, we compared both techniques to estimate the
importance of the upper airway wall shunt impedance (Zuaw) for the
interpretation of the conventional technique results. Computation of
Zuaw required, in addition, estimation of nasal impedance values, which
were drawn from previous measurements (K. N. Desager, M. Willemen, H. P. Van Bever, W. De Backer, and P. A. Vermeire.
Pediatr. Pulmonol. 11: 1-7,
1991). Upper airway resistance and reactance at 12 Hz ranged from 40 to
120 and from 0 to
150
hPa · l
1 · s,
respectively. Varying nasal impedance within the range observed in
infants did not result in major changes in the estimates of Zuaw or
lung impedance (ZL), the
impedance of the respiratory system in parallel with Zuaw. The
conventional technique underestimated ZL, depending on the value of
Zuaw. The head generator technique slightly overestimated
ZL, probably because the
pressure gradient across the upper airway was not completely
suppressed. Because of the need to enclose the head in a box (which is
not required with the conventional technique), the head generator
technique is difficult to perform in infants.
forced oscillation technique; head generator; conventional
technique
 |
INTRODUCTION |
WHEN THE IMPEDANCE of the respiratory system (Zrs) is
determined by applying forced oscillations at the mouth (8), the upper
airway acts not only as an impedance in series with the lungs but also
as a shunt for the oscillatory flow. Motion of the upper airway wall
results in loss of flow (
), leading to an
underestimation of the impedance of the downstream respiratory system.
In 1956, DuBois et al. (8) already recommended support of the cheeks
with the palms of the hands to reduce the motion of the cheeks. In an
attempt to correct for upper airway wall shunt impedance (Zuaw) in
adults, Michaelson et al. (14) performed measurements during a
Valsalva maneuver and subtracted the obtained impedance value from the
Zrs. This correction overestimates the influence of the upper airway on
Zrs. Indeed, during the Valsalva maneuver the upper airway behaves as a
single shunt impedance, with the series element of the upper airway
being negligible (1, 16). Besides, performance of a Valsalva maneuver
requires good cooperation, which cannot be obtained in infants. As an
alternative, Peslin et al. (15) tried to reduce the influence of the
upper airway wall shunt on respiratory impedance measurements by using a head generator in which pressures are varied around the head rather
than directly at the mouth (conventional technique), thereby minimizing
transmural pressure across the upper airway wall. Comparison of
respiratory impedance measured with the head generator or by the
conventional technique in adults yielded values of upper airway impedance that were similar to those measured directly with a head
plethysmograph (16).
In 1989, Marchal et al. (12) compared the use of the head generator
with the conventional technique in 24 infants. Because infants are
nearly obligatory nose breathers, the assumption that upper airway wall
motion is eliminated because oscillations are applied around the head
is not entirely valid. Indeed, during nose breathing the nose induces a
pressure difference across the upper airway wall, resulting in upper
airway wall motion. This problem was recognized by the authors, and an
adaptation of their initial model was introduced in the discussion,
enabling them to simulate the influence of the upper airway in
nose-breathing infants. No attempt thus far has been made to directly
estimate Zuaw in infants.
The aim of the present study was to estimate Zuaw in infants by
means of a model combining impedance measurements obtained with the
conventional forced oscillation technique and with the head generator
and pressure measurements obtained with a head plethysmograph.
Estimation of Zuaw allowed us to evaluate the validity of results of
conventional and head generator techniques.
 |
MATERIALS AND METHODS |
Nine infants, hospitalized with bronchiolitis, were recruited for the
study. Their ages varied between 4 and 17 mo. The study was approved by
the local hospital ethics committee, and oral informed consent was
obtained from the parents.
Conventional technique combined with head plethysmograph.
A schematic representation of the experimental setup is presented in
Fig. 1. A volume-constant head
plethysmograph was made of a 35 × 20 × 24-cm wooden box.
Two walls consisted of Plexiglas to ensure visualization of the baby.
One sidewall consisted of two parts, which delimited an orifice 10 cm
in diameter. After sedation with oral choral hydrate in a dose of 80 mg/kg, the infant was nursed supine, and the two sidewall parts were
assembled around the lower part of the neck, thus closing the box. A
reasonably good seal with minimal compression of the airways was
obtained by covering the space between the orifice and the neck with a rim of silicone putty. A 90-W loudspeaker, mounted in the wall of a
chamber, generated pseudorandom noise containing all harmonics of 4 up
to 52 Hz. The oscillations were conducted to the infant through a
60-cm-long and 2-cm-bore flexible tube, and a well-fitting rigid face
mask with a silicone border was adapted to each infant individually
(5). Differential pressure across a Fleisch no. 1 pneumotachograph,
yielding
, airway opening pressure (Pao) measured
as close as possible to the face mask, and box pressure (Pbox) were
measured with identical differential pressure transducers (±2 hPa,
Validyne MP45-1). Pbox, Pao, and
were
digitized with a sampling rate of 128 Hz and fed into a computer.
The ratio of Pao to
(Pao/
)
was calibrated by using two reference loads and according to the
two-point calibration procedure (6).

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Fig. 1.
Conventional technique combined with head plethysmograph. Computer (1)
generating pseudorandom noise drives the loudspeaker (2); bias flow of
6 l/min flushes tubing between side tubes (3) and (4). See text for
details.
|
|
The impedance value, calculated from Pao/
,
corresponds to that measured with the conventional forced oscillation
technique and is called Z1
(resistance, R1; reactance,
X1). The ratio of Pbox to Pao
(Pbox/Pao) will be referred to as a "transfer function" (TF) with
a real and imaginary part.
To get information on the impedance of the box (Zbox), the face mask
was removed from the infant's face without opening the box or moving
the infant, and Pao/
was determined. The impedance values obtained were called Z3
(resistance, R3; reactance,
X3).
Head generator technique.
The experimental setup was easily changed into a head generator (15) by
disconnecting the tube from the pneumotachograph, thus allowing the
infant to breathe into the box (Fig. 2).
Oscillations produced by the loudspeaker were now applied around the
head, and the impedance values obtained were called
Z2 (resistance, R2; reactance,
X2).

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Fig. 2.
Head generator technique. Setup is similar to Fig. 1, but tube was
disconnected from pneumotachograph.
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During this procedure of changing from the conventional technique to
the head generator, the infant was not moved, the head was not tilted,
and the face mask was left in place. Measurements of
Z1,
Z2, and
Z3 were performed in a random
order, and at least four reproducible values with a coherence function
0.95 were obtained for each parameter in each infant. Because of a
lower signal-to-noise ratio, measurements <12 Hz were generally not satisfactory (coherence function < 0.95).
Estimation of Zuaw.
The experimental setup allows for the determination of four variables:
Z1,
Z2,
Z3, and TF. In the conventional
technique measuring Z1, Zuaw is
assumed to be in parallel with the impedance of the lungs, airways, and
chest wall (which will be referred to as
ZL), whereas, when
oscillations are applied around the head, yielding Z2, Zuaw is in parallel with nasal
(Zn) and pneumotachograph impedance (Zp). Figure
3 depicts electrical analogs for the three
measurement conditions, which can be described by the following
equations
|
(1)
|
|
(2)
|
|
(3)
|
Combining Eqs. 1-3, we
can solve
for
|
(4)
|
|
(5)
|
|
(6)
|
where
= (Zbox
TF · Z1)/(TF · Z1)

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Fig. 3.
Electrical circuits for the three measurement conditions:
A, conventional technique;
B, conventional technique with baby
disconnected, showing estimation of box impedance (Zbox);
C, head generator technique. Zp,
impedance of pneumotachograph; Zn, nasal impedance; Zuaw, upper airway
wall impedance; ZL, impedance of
chest, airways, and chest wall;
P1,
P2,
P3, and
P4: pressures at different points
in the circuits;
1,
2, and
3: flows at
different points in the circuits. See text for details.
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|
In addition to the values of Z1,
Z2, and TF measured directly, the
solution of Eqs. 4-6 requires an
estimate of Zbox, which was derived from the setup yielding
Z3. Initially, as a first approximation, we assumed that, in the
Z3 setup, the arm of the model
that consisted of the combination of Zn, Zuaw, and
ZL had a very high impedance
value with respect to the other arm that consisted of Zbox (Fig. 3). In
that case, Z3 was a good estimate of Zbox. ZL, Zuaw, and Zn were
then calculated from Eqs. 4-6 by using the measured values of Z1,
Z2,
Z3, and TF.
As a check for the validity of the mathematical model, loads made of
sintered glass fitted in glass tubes (5), with known impedance values,
were connected as a model of lungs, upper airway, and nose.
Because the results obtained by using the approximate expression of
Zbox did not yield satisfactory results (see
RESULTS), we decided to work out the
exact relation between Z3 and Zbox. It is
|
(7)
|
It turned out that Eqs.
1-3 and 7 are not
independent. Indeed, it can be shown that
|
(8)
|
where
It
is impossible to determine the four unknowns, Zuaw, Zn,
ZL, and Zbox, from the four
measurements from which only three are independent.
Eqs. 4-6 depend strongly on an
accurate measurement of the parameter
. It involves TF, which is
very small, because the P2
pressure point is low with respect to the
P1 pressure point (see Fig. 3 and
Table 1). Therefore, we decided not to use
Eq. 3 and to introduce into the model,
as an independent variable, values of Zn, which had been obtained
previously in 30 infants by the forced oscillation technique by
combining consecutive measurements through both nostrils and each
nostril separately (7). The mean values at 24 Hz of nasal resistance
(Rn) and reactance (Xn) in 23 asthmatic infants without nasal
obstruction were 2.5 ± 2 and
0.9 ± 3.7 hPa · l
1 · s,
respectively. These values +1 SD and
1 SD were used as representative values. This results in the following values: Rn, 0.5, 2.5, and 4.5 hPa · l
1 · s;
Xn,
4.6,
0.9, and 2.8 hPa · l
1 · s.
Zuaw, ZL, and Zbox were then
calculated from Z1,
Z2,
Z3, Zn, and Zp, as shown in the
APPENDIX.
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Table 1.
Measurements obtained with conventional technique combined with
head plethysmograph and head generator technique
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 |
RESULTS |
Measurements were extremely difficult to perform because the sedated
baby had to be nursed supine with his or her head in a tightly closed
box with minimal leakage. Reproducible impedance values for the three
experimental conditions were obtained in seven infants (Table 1). The
data of two infants were excluded: in one patient leakage of the mask
resulted in abnormally low resistance values, and in another patient
Z3 measurements showed major
variations between frequencies. Because these variations were
reproducible and the coherence function was
0.95, this phenomenon was
probably due to cross talk between frequencies because of marked
alinearities of Zrs (4). Mean SDs were lower with the conventional
technique than with the head generator, especially at higher frequencies.
When Z1,
Z2,
Z3, and TF were substituted into
Eqs. 4-6, values of Zn were
obtained nearly equal to Z1,
whereas ZL and Zuaw were close
to zero. Similar results were obtained with the physical analog. These
results are not physiologically meaningful, and thus the assumption
that Z3 = Zbox is invalid.
On the other hand, the results were different from zero and made sense
when the exact relation for Zbox was used (Figs.
4 and 5; see
DISCUSSION).

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Fig. 4.
Resistance (A) and reactance
(B) of upper airway in 7 infants
(each represented by different symbol).
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Fig. 5.
Resistance (A) and reactance
(B) of respiratory system in 7 infants (each represented by different symbol).
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Varying the values of Rn or Xn did not result in major differences in
Zuaw or ZL (Figs.
6 and 7). In
most infants, Zn did not show a frequency dependence, with the maximum
range of Rn and Xn being, respectively, 4.6 and
4.0
hPa · l
1 · s
at 12 Hz and 1.2 and 1.6 hPa · l
1 · s
at 52 Hz. Introduction of this frequency dependence of Zn in the model
did not result in marked differences in the estimates of Zuaw or
ZL.

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Fig. 6.
Influence of different values of Zn on mean values of upper airway
resistance (A) and reactance
(B). Symbols representing nasal
resistance and reactance values (in
hPa · l 1 · s),
respectively, are as follows: , 0.5 and 4.6; , 0.5 and
0.9; , 0.5 and +2.8; , 2.5 and 4.6; , 2.5 and
0.9; , 2.5 and +2.8; , 4.5 and 4.6; , 4.5 and
0.9; +, 4.5 and +2.8.
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Fig. 7.
Influence of different nasal resistance and reactance values (in
hPa · l 1 · s)
on mean values of respiratory resistance
(A) and reactance
(B). See Fig. 6 legend for
explanation of symbols.
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When estimated ZL was compared
with Z1 and
Z2, two different patterns were
observed: lung resistance (RL)
independent of frequency (n = 4) and
RL increasing with increasing
frequency (positive frequency dependence)
(n = 3). The values of lung reactance
(XL) initially increased and
then decreased at the higher frequencies. An example of both patterns
is shown for Z1,
Z2, and
ZL (Figs. 8 and 9). There
was a close parallelism between
ZL and
Z2, with the values of
RL and
XL being slightly less than the
corresponding values of R2 and
X2. The difference between
ZL and
Z1 was larger for both
RL and
XL. As shown in Fig.
10, this difference depends on the ratio
of upper airway wall resistance (Ruaw) to
RL
(Ruaw/RL).

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Fig. 8.
Pattern of respiratory resistance
(A) and reactance
(B) observed in 4 infants. ,
conventional technique; , head generator technique; , estimated
lung impedance.
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Fig. 9.
Pattern of respiratory resistance
(A) and reactance
(B) observed in 3 infants. See Fig.
8 legend for explanation of symbols.
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Fig. 10.
Difference between respiratory resistance, measured with conventional
technique, and estimated respiratory resistance as function of ratio of
upper airway resistance to estimated respiratory resistance.
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 |
DISCUSSION |
By combining measurements obtained with the conventional forced
oscillation technique, the head generator, and previously determined Zn
values, it was possible to estimate Zuaw and
ZL in infants.
Previously, consecutive measurements of the conventional (without head
plethysmograph) and head generator techniques have been performed by
Marchal et al. (12) in 24 infants, aged 2-49 mo. Data were
analyzed between 6 and 20 Hz only because the reproducibility of the
measurements was poor >20 Hz. In our measurements, a satisfactory reproducibility was obtained up to 52 Hz, although SDs were higher in
the higher frequency range with the head generator. Resistance values
obtained with the head generator were higher than with the conventional
technique, whereas reactance values were on the average less negative.
Our data are in agreement with the findings of Marchal et al. and with
the previous observations of our laboratory (5).
Several investigators have reported on the mechanical characteristics
of the upper airway in adults (1-3, 9, 11, 14). Ruaw varied
between 4 and 10 hPa · l
1 · s,
whereas upper airway wall reactance (Xuaw) ranged between
2.1
and
5.3
hPa · l
1 · s
for frequencies between 4 and 28 Hz, depending on whether or not the
cheeks were supported. Cauberghs and Van de Woestijne (1, 2) found
Ruaw values of ~20
hPa · l
1 · s
at 4 Hz, decreasing to 10 hPa · l
1 · s
at 20 Hz, with a Xuaw of
51 and
11
hPa · l
1 · s
at 4 and 20 Hz, respectively, in adults. These data were confirmed
by the measurements with the head plethysmograph (16).
In children, few data are available. In 15 children, aged 5-15 yr,
Ruaw with support of the cheeks was found to be 46 hPa · l
1 · s
at 4 Hz, decreasing to 21 hPa · l
1 · s
at 20 Hz, whereas the reactance was
65 and
20
hPa · l
1 · s
at 4 and 20 Hz, respectively (1). There are no data available on the
upper airway impedance in infants. Our data show still higher
resistance and more negative reactance values in some infants than in
children. This is to be expected from the comparison of data between
adults and children.
Because infants breathe through the nose, it seemed that the head
generator did not correctly take the upper airway shunt into account.
Marchal et al. (12) recognized this problem and estimated the error
that results from either techniques. Two assumptions were made: first,
the nose was assumed to represent 40 and 20% of total respiratory
system resistance and inertance, respectively; and, second, Ruaw and
Xuaw were chosen to be 80 and
77.1
hPa · l
1 · s,
respectively. With the use of these hypothetical values for Zn and
Zuaw, the Zrs without any shunt effects was calculated. Marchal et al.
found that, with the head generator technique, resistance was
overestimated by 6%, increasing to 8% in airway obstruction, whereas
with the conventional technique the underestimation was
13% and
was
23% in airway obstruction. In the present study, we used
previously determined Zn values to estimate the upper airway shunt.
Alternatively, one nostril was occluded, and measurements were
performed through the other. By combining these two measurements with
impedance values obtained with the unoccluded nose, Zn was calculated
(7). These measurements were performed in a group of children other
than those in the present study. Indeed, it was practically not
possible to perform these occlusions in the setup of the present study:
the infant was lying with his or her head fixed in a box, which
remained closed during the measurement of
Z1,
Z2,
Z3, and TF. However, because the
study of Zn showed that the range of values was small as long as the
nose was not obstructed by secretions, we felt that these values could
be used to solve the set of equations in the present study. This
resulted in estimations of ZL
closer to Z2 (head generator) than
to Z1 (conventional technique),
with the underestimation of Z1
being larger with smaller
Ruaw/RL. If Zuaw is high, less
flow goes to the shunt pathway and thus
Z1 reflects more closely
ZL. The overestimation of
RL with the head generator
varied between 6 and 18% (mean 10%) at 20 Hz, whereas with the
conventional technique the underestimation ranged from
13 to
57% (mean:
35%). Errors in reactances, expressed in
absolute values, were greater for the conventional than for the head
generator technique.
Comparative studies of the head generator and the conventional
technique have been performed in adults (2, 10) and in school-age
children (13). In normal adult subjects, measurements obtained with
both techniques are very similar. In patients with moderate airway
obstruction, a negative frequency dependence is observed with the
conventional technique, whereas resistance is higher without frequency
dependence with the head generator. In patients with severe
obstruction, both techniques show resistance values with negative
frequency dependence, although resistance values are higher with the
head generator. Accordingly, a negative frequency dependence of
resistance may be an artifact due to the upper airway shunt only in
patients with moderate airway obstruction. Moreover, this artifact is
not necessarily an inconvenience for diagnostic purposes, because it
allows a clear-cut separation between healthy subjects and patients
(10). In 75 children, aged 5.5-15 yr, the power of the
conventional and head generator technique vs. forced expiratory
volume in 1 s was evaluated in detecting airway response to
bronchodilators (13). The head generator technique improved specificity
of resistance at 20 Hz from 65 to 78% without a change in sensitivity
(76%). Resonant frequency had larger sensitivity with the conventional
than with the head generator technique (91 vs. 53%) but slightly lower
specificity (70 vs. 78%). Changes in reactance were more specific and
more sensitive with the conventional than with the head generator technique.
In conclusion, Zuaw was estimated by using a combination of
measurements obtained with the conventional forced oscillation and head
generator techniques and previously determined Zn values. Upper airway
resistance and reactance at 12 Hz were between 40 and 120 and 0 and
150
hPa · l
1 · s,
respectively. Head generator impedance values are closer to the
estimated ZL values than are
those of the conventional technique. Still, the head generator
technique slightly overestimates the Zrs, because it does not
completely suppress the pressure gradient across the upper airway.
Because the head of the infant has to be enclosed in a box, the
technique is unpractical and nearly impossible to perform routinely.
 |
APPENDIX |
From Eqs. 1, 2, and
7, it follows that Zuaw satisfies the
following quadratic equation
|
(A1)
|
with
Given
the largest of the two solutions of Zuaw in Eq. A1, one calculates Zbox from
|
(A2)
|
and ZL from
|
(A3)
|
Finally,
note that Eq. 8 can be written as
|
(A4)
|
Eq. A4 justifies the choice of the largest solution of
Zuaw. Indeed, the observed small values of TF require taking the
largest solution of Eq. A1 for Zuaw.
 |
ACKNOWLEDGEMENTS |
We thank Prof. J. Devreese, Dept. of Physics, Univ. of Antwerp,
for valuable advice. We gratefully acknowledge the help of Dr. J. Clément and the useful suggestions of Dr. R. Peslin.
 |
FOOTNOTES |
This study was supported by a grant from the Fonds voor
Wetenschappelijk Onderzoek.
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: K. N. Desager,
Univ. Hospital Antwerp, Dept. of Paediatrics, Wilrijkstraat 10, B-2650
Antwerp, Belgium (E-mail: desager{at}uia.ua.ac.be).
Received 25 September 1998; accepted in final form 20 May 1999.
 |
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J APPL PHYSIOL 87(3):902-909
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