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Pediatric Pulmonology 49:764771 (2014)

Challenging a Paradigm: Positional Changes in


Ventilation Distribution Are Highly Variable in Healthy
Infants and Children
Alison R. Lupton-Smith, BSc (Physio),1* Andrew C. Argent, FCPaeds (SA), MD,1,2
Peter C. Rimensberger, MD,3 and Brenda M. Morrow, PhD1,2
Summary. Rationale: Current understanding is that infants and children preferentially ventilate
non-dependent lungs, a reversal of that of adults, based on studies using krypton-81m ventilation
scanning. Participants in these studies had lung disease and were either sedated or ventilated.
There is little understanding of the distribution of ventilation in spontaneous breathing healthy
infants and children. Objectives: This study aimed to determine the effects of side lying on the
distribution of ventilation in healthy, spontaneously breathing infants and children between the
ages of 6 months and 9 years. Methods and Measurements: Measurements were taken using
electrical impedance tomography (EIT) in supine, left and right side lying. Distribution of ventilation
was described using end-expiratory to end-inspiratory relative impedance change. Results: Fifty-
six (31, 55% male) participants were studied. Nineteen (35%) participants consistently showed
greater ventilation in the non-dependent lung, eight (15%) consistently showed greater ventilation
in the dependent lung and 28 (51%) showed a varied pattern between left and right side lying.
Overall, left side lying resulted in significantly better mean ventilation of the right (non-dependent)
lung (P < 0.01). Distribution of ventilation in right side lying was relatively equal between left and
right lungs. Conclusions: This study demonstrates that the distribution of ventilation in
spontaneously breathing infants and children is not as straightforward as previously described.
The distribution of ventilation was variably affected by body position with no clear reversal of the
adult pattern evident. Pediatr Pulmonol. 2014; 49:764771. 2013 Wiley Periodicals, Inc.

Key words: electrical impedance tomography; body position; infants and children;
ventilation distribution.

Funding source: Medical Research Council of South Africa; Institute of Child Health, UCT;
Research Foundation of the South African Society of Physiotherapy

INTRODUCTION lungs, in healthy subjects, with respect to gravity thereby


affecting the distribution of ventilation.2 The distribution
Positioning is commonly used in ill and critically ill of ventilation in response to different body positions in
patients in order to optimize ventilation and ventilation/ adults has been well established, with greater ventilation
perfusion matching.1 Positioning is therefore, an impor- occurring in the dependent (lower) lung.3 Studies using
tant component of the management of respiratory disease. 81-m krypton scanning,4,5 where majority of the
Different body positions change the orientation of the participants had lung disease and were mechanically

1
School of Child and Adolescent Health, University of Cape Town, Cape Conflict of Interest: None.
Town, South Africa.

Correspondence to: Alison Lupton-Smith, BSc (Physio), UCT School of
2
Paediatric Intensive Care Unit, Red Cross War Memorial Childrens Child and Adolescent Health, 5th Floor, Institute of Child Health Building,
Hospital, Cape Town, South Africa. Red Cross War Memorial Childrens Hospital, Klipfontein Road,
Rondebosch 7700, Cape Town, South Africa.
3
Department of Paediatrics, University Hospital of Geneva, Pediatric and E-mail: alison.lupton-smith@uct.ac.za
Neonatal Intensive Care Unit, Geneva, Switzerland.
Received 23 January 2013; Revised 17 July 2013; Accepted 17 July 2013.
Presentations: Abstract presented at Critical4Africa, Combined meeting of
the Critical Care Society of Southern Africa (CCSSA), South African DOI 10.1002/ppul.22893
Thoracic Society (SATS), South African Society for Parenteral and Enteral Published online 5 September 2013 in Wiley Online Library
Nutrition (SASPEN) and Trauma Society of South Africa (TSSA). S Afr J (wileyonlinelibrary.com).
Crit Care 2012;28(1):2836.

2013 Wiley Periodicals, Inc.


Effects of Side Lying on Ventilation in Children 765

ventilated, described greater ventilation occurring in the were to determine the effects of left and right side lying on
non-dependent (upper) lung in the pediatric population, the distribution of ventilation in healthy, spontaneously
opposite to that of adults. This is often described as the breathing infants and children using EIT and to establish
pediatric pattern of ventilation and is thought to whether there are age related differences in this
continue into the second decade of life.6 These studies distribution.
currently guide clinical practice in the pediatric popula-
tion. However, recent studies in healthy, spontaneously METHODS
breathing neonates and infants under 6 months of age79
have questioned these previously reported findings. Two A cross-sectional observational study was conducted of
of these studies reported that in neonates9 and infants up healthy, spontaneously breathing, unsedated infants and
to 6 months of age8 the distribution of ventilation in children between the ages of 6 months and 9 years
supine and prone positions was similar to that found in attending out-patient clinics and day wards at Red Cross
adults. Frerichs et al.7 also reported that neonates showed War Memorial Childrens Hospital, Cape Town, South
greater ventilation of the dependent lung in right side Africa. Subjects were excluded if they had any respiratory
lying during spontaneous sighs. In order to correctly disease or other factors impacting on respiratory
understand how ventilation is distributed in different mechanics.
disease states or during mechanical ventilation, and to A sample size of 40 subjects (10 in each age group: 6
inform clinical practice; an understanding of what occurs 12 months; 13 years; 46 years; 79 years) was
under normal circumstances is imperative. However, calculated as being required in order to detect a mean
there are no studies investigating the normal distribution difference in relative impedance change (DZ), in large
of ventilation in spontaneously breathing, healthy infants lung regions, of four with a standard deviation (SD) of 3.5
and children beyond neonatal age. (alpha 0.5, power 0.8). A total of 56 subjects were
Previous methods of determining the distribution of recruited in order to allow for the possibility of poor
ventilation in infants and children have proved difficult, quality data if participants did not cooperate fully. Ethical
given the limited ability of children to co-operate with approval was obtained from the Human Research Ethics
testing procedures, as well as the lack of suitable testing Committee of the University of Cape Town. Written
procedures that do not require sedation, radiation informed consent was obtained from the parent or legal
exposure or invasive procedures. This makes baseline guardian of all participants and verbal or written assent
studies on healthy infants and children difficult. Electrical was obtained from participants where age-appropriate.
impedance tomography (EIT), however, allows for non-
invasive, radiation-free imaging, which may be particu- Procedure
larly suited to this population. EIT has been well validated EIT measurements were taken in the following three
and has repeatedly been found to reliably detect changes body positions: supine with the head midline, left and right
in ventilation within the lungs.1020 EIT can be used for side lying. The order chosen was one of convenience owing
extended periods of time with no known harmful effects to co-operation challenges in young, active children.
or the need for sedation.7,13,21 Measurements can be Sixteen neonatal sized electrodes (Blue Sensor
obtained at up to 40 scans per second,22 which is BR-50-K, Ambu, Ballerup, Denmark), connected to the
particularly useful for the pediatric population where EIT device (Goettingen Goe-MF II EIT System; Viasys/
irregular breathing is common. EIT measures changes in Carefusion, Hochberg, Germany), were placed around the
impedance (resistance of biological tissues to alternating thorax at the level of the nipple line. Recordings were
current) in the lungs, by applying a small alternating taken for approximately 1 min in each position, EIT scans
current through 16 electrodes around the thorax and were generated at 13 scans/sec. Positioning was standard-
measuring the resulting potential differences.15,22 Imped- ized, as far as possible, with the head supported on a
ance increases during inspiration as a result of stretching pillow in side lying, the upper limbs relaxed (with no
of the lung tissue as air flows into the lungs.11,15,22 The movement); the shoulders flexed forward, perpendicular
reverse is true for expiration. Changes in impedance are, to the trunk and the lower limbs relaxed with hips and
therefore, closely related to tidal volume.23 knees flexed to ensure a stable pelvis. In supine, the arms
Given the current lack of understanding of the were dependent at the sides.
distribution of ventilation in the pediatric population in
response to different body positions, the aims of this study
Off-Line Analysis

ABBREVIATIONS:
Analysis was performed off-line using Auspex Version
EIT electrical impedance tomography 1.6 software (Viasys Healthcare, Amsterdam, Netherlands).
SD standard deviation The data was filtered to eliminate the effect of the heart.21,24
A series of five reproducible tidal breaths, of similar
Pediatric Pulmonology
766 Lupton-Smith et al.

amplitude with no inspiratory or expiratory pauses, were Pattern of Ventilation


selected for analysis (Fig. 1a). Functional EIT (fEIT)
Nineteen (35%) subjects demonstrated greater ventila-
images (Fig. 2) were generated using the average of the end-
tion in the non-dependent lung and eight (15%)
expiratory to end-inspiratory DZ (Fig. 1b). Calculations
demonstrated greater ventilation in the dependent lung
were performed using the sum of pixel values of the fEIT
in both left and right side lying, whilst 28 (51%) followed
images for global DZ and regional DZ for regions of interest
different patterns in left and right side lying.
(ROI). ROI were determined as described by Pulletz et al.25
with 20% of the regression coefficient being used to
Distribution of Ventilation in Left and Right Lungs
determine the contour. In this case, ROI were the entire left
and right lung, respectively. The global and regional DZ changes in supine and side
Mean DZ change was used to compare left and right lying positions are presented in Table 2. There was no
ROI, as well as globally, in different positions. The significant difference in global ventilation between the
difference in mean DZ change between non-dependent different positions. There was no difference in DZ
and dependent positions in left and right lungs, between left and right lungs in supine. Overall ventilation
respectively, was calculated to determine the pattern of the right lung was greater than the left when lying on
of ventilation and between- age group comparisons. In the left side, while mean ventilation of both lungs was
addition, the proportion (%) of ventilation occurring in equal in right side lying (Table 2).
each lung region relative to the global ventilation was The right lung showed greater ventilation when non-
calculated for between- age group comparisons. dependent in 36 (65%) of the participants, whereas the left
lung showed better ventilation when non-dependent in 30
Statistical Analysis (55%) of participants.
Both left and right lungs showed greater ventilation
Analysis was performed using Statistica version 10
when non-dependent compared to dependent in side lying
(StatSoft, Tulsa, Oklahoma, USA). Data were tested for
(Table 2), although this was only significant in the right
normality using the Shapiro Wilks W-test and were found
lung. The difference between left and right lungs when
to be normally distributed. Results are shown as means 
non-dependent approached significance (P 0.06; Ta-
SD and 95% CI. Multi-way ANOVAs were used to
ble 2). There was a significant decrease in ventilation in
determine differences between age groups and ROI,
both left (P 0.004) and right (P 0.02) lungs when
respectively in different positions. T-tests for dependent
moving from supine position to side lying with that lung
and independent variables were used to determine
dependent (Table 2). In left side lying there was a
significant differences within and between groups.
significant difference in ventilation between left and right
P-values 0.05 were considered significant.
lungs, with the right (non-dependent) lung being better
ventilated, whilst no difference was noted between left
RESULTS
and right lungs in right side lying (Table 2). The right lung
Fifty-six participants (31, 55.4% male) were included was better ventilated in left side lying when compared to
in the study. Population characteristics are presented in right side lying (P 0.02).
Table 1. Complete measurements were obtained in 55 Comparison of the proportion of ventilation relative to
subjects. global ventilation, between left and right lungs, revealed

Fig. 1. Selection of reproducible tidal breaths (A) used for analysis indicated by vertical lines.
fEIT images were generated for the end-expiration and end-inspiration points are marked with
arrows (B) and are an indication of tidal volume.

Pediatric Pulmonology
Effects of Side Lying on Ventilation in Children 767

Fig. 2. fEIT images in right side lying from two different participants (both between the ages of 4
and 6 years). Lighter portions indicate areas of greater ventilation. (A) Indicates greater
ventilation in the non-dependent (left) lung and (B) indicates greater ventilation in the dependent
(right) lung.

that the right lung had a significantly greater proportion of 13 years age group had a greater proportion of
ventilation (P < 0.001) than the left lung in left side lying, ventilation in the right (dependent) lung. The 46 years
whilst there was no difference in right side lying (P 0.9). and 79 years age groups demonstrated relatively equal
ventilation between left and right lungs in right side lying
The Effect of Age (Fig. 4).
The distribution of ventilation in the left and right
DISCUSSION
lungs, as well as globally, was similar between age groups
in the different positions (Fig. 3); however, significant This study examined the regional distribution of
age-related changes were found in the proportion of ventilation in spontaneously breathing, healthy infants
ventilation in the left and right lungs (Fig. 4) in side lying. and children in response to side lying positions, using EIT.
Significant age-related differences were found when Our results show that the distribution of ventilation in
comparing the DZ change in the left lung between side healthy, spontaneously breathing, nonsedated infants and
lying positions. The 612 months group favourably children is complex, with the pattern of ventilation not
ventilated the left lung when non-dependent, whereas the being uniform as previously reported.4,5 A high degree of
older age groups (13 and 79 years) favourably variability was found between participants with approxi-
ventilated the left lung when dependent. No age-related mately half showing a different pattern of ventilation
differences were found in the right lung (Table 3 and distribution between right and left lungs in side lying
Fig. 5). positions. Only about one-third of the children conformed
A significantly greater proportion of ventilation to the previously described pattern of consistently greater
occurred in the right (nondependent) lung compared to ventilation in the non-dependent lung.4,5,26 Age related
the left lung in left side lying, amongst all age groups differences were primarily noted in the left lung, and
(Fig. 4). In right side lying, the 612 months age group between those younger and older than 12 months, with
demonstrated a significantly greater proportion of those under 12 months demonstrating better ventilation in
ventilation in the left (non-dependent) lung, while the the non-dependent lung.

TABLE 1 Population Characteristics (Mean  SD)


TABLE 2 Mean DZ  SD of Lung Regions in Different
Gender Positions
(male: Respiratory rate
Age group Number female) Age (years) (breath per minute) Lung region Supine Left side lying Right side lying
  ,
612 months 10 6:4 0.85  0.11 47.00  7.42 Left 16.8  9.0 14.1  7.3 15.6  9.3ll
13 years 18 11:7 2.76  0.94 26.78  5.34 Right 17.8  7.9 18.4  7.5,,ll 15.7  7.0,
46 years 18 7:11 5.59  0.94 21.94  3.62 Global 34.6  16.3 32.6  13.5 31.5  14.3
79 years 10 7:3 8.72  0.85 19.90  2.85
Total 56 31:25 Comparisons are marked as significant.

P 0.004; P 0.02; P 0.002; P 0.02; llP 0.06.

Pediatric Pulmonology
768 Lupton-Smith et al.

Fig. 3. Mean relative tidal impedance change (DZ) in left (A) and right (B) lungs between age
groups in left side lying (sd ly), supine and right side lying. Points represent means and vertical
bars denote 95% CI.

This is the first study of postural effects on ventilation there was a trend towards greater ventilation in the non-
distribution in normal, healthy children. The majority of dependent lung. These findings are in keeping with those
participants in previous studies4,5 displayed abnormal of Frerichs et al.7
chest radiographs and were either mechanically ventilat- The marked difference between left and right side lying
ed or most likely required sedation. These factors may all is not unexpected given the asymmetry of the chest and
affect respiratory mechanics and may predispose to related organs, particularly the heart, which occupies the
favourable ventilation of the non-dependent lung,7,9,27 left ventral compartment.28 In left side lying the
accounting for the difference between our findings. gravitational effect on the heart, the heaviest structure
The most notable effect of position on the distribution in the thorax, would likely limit left lung expansion. This
of ventilation was in left side lying, with a significantly is supported by the suggestion that changes in the
larger proportion of ventilation in the non-dependent distribution of ventilation in different positions are
(right) lung. This is in keeping with the pattern described primarily attributed to movement of thoracic tissue in
by Davies et al.4 In right side lying, however, both the response to gravity.2931 To our knowledge, there are no
distribution and proportion of ventilation remained reports on the effect of left side lying on the distribution of
relatively equal between the left and right lungs, although ventilation in infants and children.

Fig. 4. Proportion of ventilation (relative to global ventilation) in left and right lungs, depicted as
means, 95% CI and minmax values, in left (A) and right (B) side lying. Comparisons marked as
significant  P 0.03 between left and right lungs; P < 0.001 between left and right lungs;

P 0.003 between left and right lungs; P < 0.001;  P 0.02 between left and right lungs.
ll
P 0.01 within left and right lungs, respectively between age groups; P 0.01 within left and
right lungs, respectively, between age groups; P 0.02 within left and right lungs, respectively
between age groups.

Pediatric Pulmonology
Effects of Side Lying on Ventilation in Children 769
TABLE 3 Mean  SD Difference in DZ in Left and Right in dependent lung portions and therefore, greater
Lungs, Respectively, When Moving From Non-Dependent to ventilation in the non-dependent lung. Most of the
Dependent
changes in the chest wall and respiratory musculature
Age group Left lung Right lung occur up to the age of 2 years, coinciding with motor
 , development where a more upright posture is as-
612 months 4.9  5.9 1.3  9.0
13 years 0.3  4.7 5.0  5.3 sumed.37,38 After about 2 years of age the chest wall
46 years 2.8  15.0 0.4  9.3 and respiratory musculature are similar to that of adults.37
79 years 2.0  4.8 4.6  8.5 Heaf et al.5 also postulated that the side lying position
places the dependent hemidiaphragm at a mechanical
A positive value indicates greater ventilation of the non-dependent
lung, whilst a negative value indicates greater ventilation of the
disadvantage. Contractility of the diaphragm is governed,
dependent lung. Comparisons are marked as significant. in part, by the resting length of the muscle fibres (preload).
 The longer the resting length, the better the contraction
P 0.04; P 0.01.
and therefore greater ventilation to the lung.39 In adults, in
side lying, there is greater preload on the dependent
Authors of previous studies4,5 attributed the difference hemidiaphragm as a result of pressure from the abdominal
between ventilation distribution in adults towards the contents, hence better ventilation of the dependent lung.
dependent lung3 and the trend towards better ventilation Davies et al.4 and Heaf et al.5 postulated that due to the
of the non-dependent lung in infants and children to narrower abdomen in infants, the difference in preload of
differences in respiratory mechanics. Ventilation is the dependent and non-dependent diaphragm is less,
determined by a complex interplay between chest wall, resulting in greater ventilation of the non-dependent lung5
lung, respiratory muscle and pleural dynamics. In adults or a smaller difference between lungs.4 These factors may
the changes in the distribution of ventilation are primarily explain the overall trend to greater ventilation in the non-
due to differences in pleural pressure, which become dependent lung in our study, particularly in infants under
progressively more positive down the vertical axis of the 12 months of age.
thorax as a result of gravity.32,33 These changes in pleural The variability found amongst different children is
pressures result from increased superimposed pressures difficult to explain, although it may relate in part to
on the dependent lung by the weight of the lung above normal physiological principles in which energy is likely
it.31,34 Consequently, the dependent lung has lower to be conserved by varying patterns of respiratory muscle
resting volumes and expands more during inspiration use.40 Irregular respiratory rates and patterns may also
than the non-dependent lung.31 Children differ from contribute to this variability. The lack of variability
adults in that they have higher chest wall compliance35; as described in earlier studies of mostly ventilated children
a result the resting pleural pressure is more positive. This with lung pathology,4,5 may reflect a diseased state in
results in a lower functional residual capacity which nears which normal fluctuations of breathing pattern are not
closing volumes.4,5,35,36 The higher resting pleural possible. Intersubject variability may also be due, in part,
pressure, in addition to the gravitational effects on the to differences in developmental levels given that the chest
intrapleural pressure,32 is likely to result in airway closure wall is similar to that of adults by the age of 2 years and
may result in a similar distribution of ventilation to that of
adults. Coinciding with the changes in the chest wall are
changes in respiratory muscle strength and function38 and
chest wall compliance.35 The vertical height of the lungs
(size of the child) may also affect the distribution of
ventilation, and possibly explain some of the variability
found in our study, based on findings of Agostoni and
DAngelo41 that the vertical pleural pressure gradient
decreases with increasing size (height of the lung). These
suggestions require further investigation, particularly
considering that we were unable to show clear age-
related differences in ventilation distribution.
It is possible that the relative impedance measured also
reflected changes in perfusion, which is known to be
affected by gravity. However, it has been noted that changes
Fig. 5. The proportion of participants in different age groups in perfusion account for <5% of the recorded relative
demonstrating better ventilation of the left and right lungs when
either dependent or non-dependent. The left lung is dependent
impedance.42 Perfusion is related to cardiac frequency. By
in left side lying and non-dependent in right side lying. This is filtering the data to exclude the heart noise,24 effects of
reversed for the right lung. perfusion on the readings were likely reduced.
Pediatric Pulmonology
770 Lupton-Smith et al.

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