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Positioning Effects on Lung Function and Breathing Pattern

in Premature Newborns
Georgette Gouna, MD1, Thameur Rakza, MD1,2, Elaine Kuissi, MD1, Thomas Pennaforte, MD1, Sebastien Mur, MD1,2,
and Laurent Storme, MD1,2

Objective To compare breathing patterns and lung function in the supine, lateral, and prone positions in oxygen-
dependent preterm infants.
Study design Respiratory function in preterm infants receiving nasal continous positive airway pressure therapy
for mild respiratory failure was evaluated by respiratory inductive plethysmography. Infants were randomized to
supine, left lateral, and prone positions for 3 hours. A nest provided a semiflexed posture for the infants placed
in the left lateral position, similar to the in utero position. Tidal volume (Vt), phase angle between abdominal and tho-
racic movements, rib cage contribution to Vt, and dynamic elevation of end-expiratory lung volume were measured.
Results Fraction of inspired O2 was similar in the 3 positions for 19 infants (mean gestational age, 27  2 weeks;
mean birth weight, 950  150 g; mean postnatal age, 17  5 days). However, arterial O2 saturation and Vt were
higher in the left lateral and prone positions than in the supine position (P < .05). The phase angle between abdom-
inal and thoracic movements was lower and rib cage contribution to Vt was higher in the left lateral and prone
positions than in the supine position (P < .05). Dynamic elevation of end-expiratory lung volume was greater in
the supine position than in the left lateral and prone positions (P < .05).
Conclusion In oxygen-dependent preterm infants, both the left lateral and prone positions improve lung function
by optimizing breathing strategy. In the neonatal intensive care unit, the left lateral position can be used as an
alternative to the prone position for mild respiratory failure. (J Pediatr 2013;162:1133-7).

P
ositioning plays a critical role in pulmonary, digestive, and autonomic functions in preterm infants. Compared with the
supine position, the prone position elevates PaO2,1-3 enhances the contribution of the rib cage to tidal volume (Vt),4
improves thoracoabdominal synchrony,4 reduces obstructive apneas,5,6 promotes sucking,7 reduces stress behaviors,8,9
and increases sleep duration.5 However, prolonged prone positioning may alter postural control (dominance of the dorsal
extensor muscles) and sensorimotor organization.10,11 The tucked positions, involving gentle positioning of the infant’s
arms and legs in a flexed, midline position close to the body, is currently recommended for preterm infants to promote motor
and autonomic self-regulation, reduce stress behaviors, and enhance spontaneous movements.9,12-14 Gastroesophageal reflux is
reduced by left lateral positioning and increased by right lateral positioning.15,16 The lateral flexed position, similar to the in
utero position, facilitates tucking.9 The effects of lateral body position on pulmonary function and on breathing strategy in
preterm newborns are not known, however.
We hypothesized that in oxygen-dependent preterm infants, the left side-lying position, like the prone position, improves
lung function. To test this hypothesis, we compared breathing patterns and respiratory variables measured in the supine,
left lateral, and prone positions in preterm infants.

Methods
Our study was conducted over a 6-month period in the neonatal intensive care unit at the Regional University Hospital of Lille,
France. Inclusion criteria were preterm birth (gestational age 26-30 weeks), spontaneous breathing with nasal continuous pos-
itive airway pressure (NCPAP) therapy, and mild respiratory failure, defined as an oxygen requirement of 22%-35% to main-
tain arterial oxygen saturation (SpO2) between 88% and 95%, pH > 7.24, and PaCO2 <65 mm Hg. Exclusion criteria were
circulatory failure, receipt of vasoactive drugs, and periventricular leukomalacia or intraventricular hemorrhage. The study
was approved by the institutional Research
%RC Rib cage contribution to Vt
DEELV Dynamic elevation of end-expiratory lung volume
q Phase angle between abdominal and thoracic movements From the 1Department of Perinatology, Jeanne de
NCPAP Nasal continuous positive airway pressure Flandre Hospital, University Hospital of Lille; and
2
RIP Respiratory inductive plethysmography EA4489, Perinatal Environment and Growth, School of
Medicine, Universite Lille 2, Lille, France
SpO2 Arterial oxygen saturation
The authors declare no conflicts of interest.
Ve Expiratory flow volume
Vt Tidal volume 0022-3476/$ - see front matter. Copyright ª 2013 Mosby Inc.
All rights reserved. http://dx.doi.org/10.1016/j.jpeds.2012.11.036

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Ethics Committee. Written informed consent was obtained (q), respiratory rate, and inspiratory time. The q value was
from the parent(s) of each infant. calculated using the analysis of the Lissajous figures of the
Each infant was successively placed, in random order, in rib cage signal (y-axis) versus the abdominal signal (x-axis).
the supine, left lateral, and prone positions. The body posi- The width of the loop is related to the degree of thoracoabdo-
tions were stabilized in a nest, with the infant’s head posi- minal asynchrony. Asynchrony was assessed by calculating
tioned toward the midline in the supine and left lateral q as follows: q = [sin 1(m/s)] for q < 90 or q = [180 -
positions. The nest provided a semiflexed posture in the in- sin 1(m/s)] for q > 90 , where m is the width of the Lissajous
fants placed on the left side (tucked position) (Figure 1; figure at mid rib cage excursion and s is the width of the Lis-
available at www.jpeds.com). Respiratory variables were sajous figure at its greatest abdominal excursion. The value of
recorded for 3 hours in each body position. Special care was q can range from 0 (synchronous breathing) to 180 (para-
taken to avoid motion artifacts by minimizing external doxical breathing). Ventilatory flow was computed as the de-
stimulation. Measurements were performed after feeding to rivative of Vt. The flow-volume loops were analyzed to
ensure quiet sleep. Given that sleep state may influence estimate the dynamic elevation of end-expiratory lung vol-
breathing behavior,5 the infants’ sleep patterns were ume (DEELV), representing the difference between the
recorded. An observer remained with the infant during the end-expiratory lung volume level and the static relaxation
study to record sleep states and wake periods. Sleep states volume. The static relaxation volume was estimated from ex-
were described as active or quiet according to behavioral trapolation of the linear segment of the flow-volume curve to
criteria.17 Active sleep was defined by rapid eye movements, zero flow, as described previously.18-20 The regression line of
frequent body and facial movements, and irregular the linear part of the flow-volume loop was calculated using
breathing with paradoxical movements of the rib cage and the least squares method (Respi-Events; SensorMedics)
abdomen. Quiet sleep was defined by lack of eye (Figure 2).
movements, rare body or facial movements with occasional Preliminary tests showed that the respiratory variables sta-
startles, and regular breathing pattern. Sedation was not bilized within 30 minutes after the change in body position.
used. Each infant served as his or her own control. We analyzed the variables recorded 60-180 minutes after po-
SpO2, transcutaneous PaCO2, heart and respiratory rates, sitioning and during quiet sleep periods only, to ensure com-
and arterial blood pressure were monitored continuously plete patient stabilization and few motion artifacts. Indeed,
(IntelliVue MP70 monitor; Philips Healthcare, Suresnes, active sleep-related body movements cause motion artifacts
France), sampled at 1 Hz, and then averaged for each period on the RIP, precluding reliable RIP measurements.
(IntelliVue Information Center; Philips Healthcare). Frac- Based on our previous work indicating a mean q = 95 

tion of inspired oxygen was set to maintain SpO2 between 25 in the supine position,18,19 to detect a clinically signifi-
88% and 95%. An apneic episode was defined as a ventilatory cant difference in q, defined as 25%, with a power of 80%
pause of more than 10 seconds and/or episode of SpO2 and a 2-sided a of 0.05, at least 18 infants were required.
<80%. Breathing pattern was recorded by respiratory The variables are expressed as mean  SD or median
inductive plethysmography (RIP) (Respitrace Plus set in (IQR). The data were compared using the Friedman test
AC-coupled mode; SensorMedics, Miami, Florida). RIP for nonparametric and repeated-measures analysis. Inter-
was performed using 2 transducer bands, one around the group differences were analyzed by post hoc analysis with
thorax at the nipple line and the other around the abdomen, the Wilcoxon signed-rank test and Bonferroni correction us-
0.5 cm above the umbilicus. Special care was taken to prevent ing SPSS version 11.5.1 (IBM, Armonk, New York). A P value
RIP band displacement during nursing care or changes in po- <.05 was considered significant.
sitioning. Band positions and settings were secured and fixed
with adhesive tape. The impedance of the bands changed Results
with respiratory movements and was processed to measure
respiratory variables. Autocalibration of the device occurred All 19 preterm infants had received mechanical ventilation at
during periods of quiet breathing. The signals were recorded birth for respiratory distress syndrome and received surfac-
continuously and processed by specific software (NIMS, tant treatment within the first hour of life. Duration of the
Respi-Events software; SensorMedics, Homestead, Florida). mechanical ventilation was less than 24 hours. NCPAP
Before recording, baseline airflow was measured by face (Infant-Flow; Vyasis, CareFusion, Voisins le Bretonneux,
mask pneumotachography (Florian hot-wire pneumotacho- France) was used to wean the infants from mechanical venti-
graph, 0.7-mL dead space; Acutronic Medical Systems, Zug, lation. At the time of the study, the infants were managed
Switzerland). Vt, calculated from the integration of a series of with NCPAP and received caffeine. Mean gestational age
10 leak-free respiratory cycles, was used to calibrate the cor- was 27  2 weeks, and mean birth weight was 950  150 g.
responding RIP breaths. Calibration was performed before The infants were studied at a mean postnatal age of 17  5
the start of recording and repeated during the study period days (mean weight, 1300  275 g).
as required in the event of accidental displacement of the Heart and respiratory rates and arterial blood pressure
RIP bands. were similar in all positions. Although fraction of inspired
We recorded Vt, rib cage contribution to Vt (%RC), oxygen was similar in the 3 positions, SpO2 was higher in
phase angle between abdominal and thoracic movements the left lateral and prone positions than in the supine position
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June 2013 ORIGINAL ARTICLES

Table. Comparison of respiratory variables in the


supine, left lateral, and prone positions
Supine Left lateral Prone
Respiratory rate, breaths/minute 62  8 56  7 58  6
Vt, mL/kg 4.8  1.1 5.5  0.9* 5.7  0.9*
Ti, seconds 0.36  0.11 0.42  0.09 0.43  0.10
FiO2, % 28  5 24  3 23  2
SpO2, % 91  3 95  2* 96  1*
TcPCO2, mm Hg 57  7 52  5* 51  4*
Number of apnea episodes/3 hours 83 4  2* 5  2*

FiO2, fraction of inspired oxygen; TcPCO2, transcutaneous partial pressure of CO2.


*P < .05, compared with the value measured in the supine position.

The correlation coefficient (R2) of the regression lines cal-


culated from the linear segment of each flow-volume loop
was constantly >0.97. Flow-volume loops of a representative
infant placed in the supine, left lateral, and prone positions
are shown in Figure 2. The DEELV volume was twice as
large in the supine position than in the left lateral and
prone positions (P < .05) (Figure 3).

Discussion
We hypothesized that the left lateral position and prone po-
sition would improve lung function and breathing strategy in
our preterm infants. We found that transcutaneous SpO2 was
higher and PaCO2 was lower in the left lateral and prone
positions than in the supine position. Furthermore, the left
lateral and prone positions were associated with fewer apneic
and hypoxic episodes compared with the supine position.
Compared with the supine position, the left lateral and prone
positions increased the q and %RC values and decreased the
Figure 2. Flow-volume loops of a representative infant in DEELV value. Taken together, these results demonstrate that
supine, left lateral, and prone positions. DEELV represents the the left lateral position, as well as the prone position, improve
difference between the end-expiratory lung volume and the pulmonary function by optimizing ventilatory strategy and
static relaxation volume. The static relaxation volume can be lung volume.
estimated from the extrapolation of the linear segment of the Thoracoabdominal synchrony plays a key role in the effi-
flow-volume curve to zero flow. In the prone and left lateral ciency of lung ventilation.21,22 The Vt generated by the ab-
positions, the Ve curve fell linearly to near the zero-flow line, dominal and thoracic movements is dependent on q, the
consistent with an almost complete passive deflation; DEELV
phase angle between the chest and abdominal movement.21,22
was low. On the other hand, the expiratory time was too short
At a similar amplitude of chest wall and abdominal displace-
to achieve complete lung deflation in the supine position, in-
dicating a high DEELV. Vi, inspiratory flow; Ti, inspiratory time. ment, the resulting Vt decreases as thoracoabdominal asyn-
chrony increases. Thus, the increased Vt observed in the
left lateral and prone positions may result from better syn-
(P < .05) (Table). Transcutaneous PaCO2 was lower in the chrony of the chest wall and abdominal movements. Taken
left lateral and prone positions than in supine position together, these results indicate that the lower PaCO2 in the
(P < .05). Vt was greater in the left lateral and prone left lateral and prone positions compared with the supine po-
positions than in the supine position. Inspiratory time was sition may be related to a more efficient breathing pattern
not altered by the body position. Apneic and hypoxic through stabilization of the chest wall and increased thora-
episodes were more frequent in the supine position than in coabdominal synchrony.
the left lateral and prone positions (P < .05). The mechanisms by which left lateral and prone positions
Better synchronization of thoracoabdominal movements, improve lung function in the preterm infant remain specula-
indicated by a lower q value was seen in the prone and left lat- tive. Studies in adult patients and preterm infants have sug-
eral positions compared with the supine position (P < .05) gested that the prone position may increase lung volume
(Figure 3). The %RC value was significantly lower in the through lung expansion in the dorsal region,23-25 caused by
supine position than in the left lateral and prone positions decreased transmission of the weight of abdominal contents
(P < .05) (Figure 3). to the dorsal regions and decreased lung compression by the
Positioning Effects on Lung Function and Breathing Pattern in Premature Newborns 1135
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Figure 3. A, Phase angles, q, expressed as degree between abdominal and thoracic motions, in the supine, left lateral, and
prone positions. q was lower in the left lateral and prone positions than in the supine position, indicating better thoracoabdominal
synchrony in the left lateral and prone positions. B, Contribution of rib cage displacement to Vt (%RC to Vt), expressed in %, in
the supine, left lateral, and prone positions. The %RC to Vt was greater in the left lateral and prone positions than in the supine
position. C, Mean DEELV, expressed as % of Vt, measured in the supine, left lateral, and prone positions. Values are median
(IQR). *P < .05, compared with values measured in the supine position.

heart.26,27 In the left lateral position, expansion of the right given that we did not directly measure absolute end-
lung can be expected for the same reasons. Our finding of expiratory lung volume in this study.
decreased DEELV in the prone and left lateral positions This study has several limitations. The effect of the right
provides additional evidence supporting for this hypothesis. lateral position was not studied. In preterm infants, gastro-
Indeed, end-expiratory lung volume depends on both static esophageal reflux is increased in the right lateral posi-
and dynamic phenomena, and is maintained above the tion.15,16 In addition, with the anatomic asymmetry, we
passive resting volume during active breathing in preterm cannot estimate the impact of right lateral positioning on
infants mainly by breaking the expiratory flow.28 We previ- lung function. RIP has been used mainly to assess ventilation
ously showed that expiratory flow volume (Ve) loops provide strategies and lung volumes in preterm infants. A linear
information on the volume of trapped gas by DEELV. The relationship between pneumotachography and RIP volumes
difference between end-expiratory lung volume and relaxa- has been reported, which was not altered by sleep state,
tion volume can be estimated by extrapolating the linear position, respiratory rate, or %RC value.31 The repro-
segment of the flow-volume curve to zero flow.18-20 Our ducibility of RIP measurements in this population has not
data show that the Ve curve falls linearly to near the zero- been reported, however. In the present study, each infant
flow line in the prone and left lateral positions, consistent was his or her own control, and the order of positioning
with complete passive deflation toward the passive resting was randomized, limiting the potential bias induced by
lung volume (Figure 2). These results indicate that the interindividual reproducibility of the RIP measurements.
characteristic protective expiratory braking observed in the Our study population was limited to preterm infants with
premature infants is diminished in the prone and left mild respiratory failure managed with NCPAP; whether or
lateral positions compared with the supine position. not the effects of body position are similar in other popula-
Previous studies have shown that passive relaxation vol- tions of preterm infants remains an open question. Finally,
ume and DEELV are inversely related. NCPAP-induced pas- we did not investigate the role of body position on ventila-
sive increases in end-expiratory lung volume are associated tion distribution in this study.
with a decrease in the volume of gas actively trapped by expi- Although the prone position is largely used in neonatal
ratory braking.18,29 We speculate that the volume-preserving intensive care units, warnings regarding the potential ad-
dynamic mechanisms required to elevate end-expiratory verse impacts of prolonged prone positioning on later pos-
lung volume above the relaxation volume are no longer nec- tural control and sensorimotor organization have been
essary in both the left lateral and prone positions, suggesting reported.10,11 On the other hand, “tucked” positions are
that these positions cause a passive increase in end-expiratory currently recommended in preterm infants to promote mo-
lung volume. Results of a study showing an increase in func- tor and autonomic self-regulation,9,12 reduce stress,9,32 and
tional residual capacity in the prone position in preterm improve spontaneous movements.13 The side-lying position,
infants are in accordance with this hypothesis.30 This effect similar to the in utero position, promotes facilitated tucking
of positioning on lung volume remains speculative, however, of the preterm infant.14 Furthermore, the left lateral position
1136 Gouna et al
June 2013 ORIGINAL ARTICLES

reduces gastroesophageal reflux.15 Because left lateral and 16. Omari TI, Rommel N, Staunton E, Lontis R, Goodchild L, Haslam RR,
prone positions have similar respiratory effects, we propose et al. Paradoxical impact of body positioning on gastroesophageal
reflux and gastric emptying in the premature neonate. J Pediatr 2004;
that the left lateral position can serve as an alternative to
145:194-200.
prone position in the oxygen-dependent preterm infants 17. Prechtl HF. The behavioural states of the new born infant. Brain Res
in the neonatal intensive care unit. n 1974;76:185-212.
18. Magnenant E, Rakza T, Riou Y, Elgellab A, Matran R, Lequien P, et al.
Submitted for publication May 16, 2012; last revision received Oct 22, 2012; Dynamic behavior of respiratory system during nasal continuous posi-
accepted Nov 8, 2012. tive airway pressure in spontaneously breathing premature newborn
Reprint requests: Laurent Storme, MD, Po^ le Femme Me re Nouveau-ne, infants. Pediatr Pulmonol 2004;37:485-91.
^ pital Jeanne de Flandre, 1 Avenue Euge
Ho ne Avinee, CHRU de Lille, Lille 19. Boumecid H, Rakza T, Abazine A, Klosowski S, Matran R, Storme L.
Cedex 59035, France. E-mail: lstorme@chru-lille.fr Influence of three nasal continuous positive airway pressure devices on
breathing pattern in preterm infants. Arch Dis Child Fetal Neonatal
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Positioning Effects on Lung Function and Breathing Pattern in Premature Newborns 1137
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Figure 1. Photograph of a preterm infant placed in the left


side-lying position. A “nest” provides a gentle semiflexed
posture, similar to the in utero position, which facilitates
tucking. The arms and legs are in a flexed, midline position
close to the body.

1137.e1 Gouna et al

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