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The Effect of Body Positioning on Gastroesophageal Reflux in Premature
Infants: Evaluation by Combined Impedance and pH Monitoring
LUIGI CORVAGLIA, MD, RAFFAELLA ROTATORI, MD, MARIANNA FERLINI, MD, ARIANNA ACETI, MD,
GINA ANCORA, MD, AND GIACOMO FALDELLA, MD

Objective To evaluate the pattern of acid and nonacid gastroesophageal reflux (GER) in different body positions in preterm
infants with reflux symptoms by a combined multichannel intraluminal impedance (MII)–pH monitoring, which identifies both
acid and nonacid GER.
Study design Premature infants with frequent regurgitation and postprandial desaturation (n ⴝ 22) underwent a 24-hour
recording of MII-pH. In a within-subjects design, reflux indexes were analyzed with the infants in 4 different positions: supine
(S), prone (P), on the right side (RS), and on the left side (LS).
Results All infants were analyzed for 20 hours. The mean number of recorded GER episodes was 109.7. The mean
esophageal exposure to acid and nonacid GER was lower in positions P (4.4% and 0.3%, respectively) and LS (7.5% and 0.7%,
respectively) than in positions RS (21.4% and 1.2%, respectively) and S (17.6% and 1.3%, respectively). The number of
postprandial nonacid GER episodes decreased but the number of acid GER episodes increased over time. The LS position
showed the lowest esophageal acid exposure (0.8%) in the early postprandial period, and the P position showed the lowest
esophageal acid exposure (5.1%) in the late postprandial period.
Conclusion Placing premature infants in the prone or left lateral position in the postprandial period is a simple intervention
to limit GER. (J Pediatr 2007;151:591-6)
astroesophageal reflux (GER) is common in premature infants. Because it may be linked to serious clinical consequences, it is cause for concern in neonatologists and parents and necessitates prolongation of hospitalization.1,2 As in
term infants,3 a conservative approach based on postural treatment has been suggested in preterm infants with GER.1
However, few studies have been performed to investigate the best body position for this approach to GER treatment in
premature infants, and results are not conclusive. Using pH monitoring, Ewer et al4 found that prone and left lateral positioning
was more effective in preventing GER. Omari et al,5 using combined manometry and multichannel intraluminal impedance
(MII) recording in preterm infants asymptomatic for GER, found that left lateral positioning was more advantageous than right
lateral positioning. These authors analyzed the mechanisms triggering GER and observed an increased number of transient lower
esophageal sphincter relaxations (TLESRs) in the right lateral position, despite a gastric
emptying rate twice that in the left lateral position. Despite these important findings, this
study was unable to differentiate acid and nonacid GER.5
The effect of positioning is predictable based on previous work, but it is important
See editorial, p 560 and
to describe this effect using the current state-of-the-art methods for GER measurement.
Consequently, the aim of our study was to evaluate the affect of body position on GER
related article, p 585
in symptomatic premature infants using combining intraluminal impedance and pH
monitoring.
From the Institute of Preventive Pediatrics
and Neonatology, St. Orsola Malpighi GenMII is based on the intraluminal electrical impedance changes occurring during
eral Hospital, University of Bologna, Bolothe passage of a bolus through the esophagus. It is measured by electrodes incorpogna, Italy (L.C., R.R., M.F., A.A., G.A., G.F.).
rated along a catheter. Impedance is decreased if the bolus is liquid and is increased
Submitted for publication Feb 1, 2007; last
revision received Apr 27, 2007; accepted
if it is air. The direction of the bolus is determined by evaluating changes in
Jun 6, 2007.
intraluminal impedance at various levels over time.6 MII can detect gas, mixed, and

G

BEI
GER
LES
LS
MACT
MII

Bolus exposure index
Gastroesophageal reflux
Lower esophageal sphincter
Left side
Mean acidic clearing time
Multichannel intraluminal impedance

P
RIpH
RS
S
TLESR

Prone
Reflux index
Right side
Supine
Transient lower esophageal sphincter
relaxation

Reprint requests: Luigi Corvaglia, MD, Istituto
di Pediatria Preventiva e Neonatologia, Via
Massarenti 11, 40138 Bologna, Italy. E-mail:
[email protected]
0022-3476/$ - see front matter
Copyright © 2007 Mosby Inc. All rights
reserved.
10.1016/j.jpeds.2007.06.014

591

liquid GER episodes but cannot differentiate acid and
non-acid episodes; for this reason, it is essential to combine
MII and pH monitoring to evaluate the role of acid and
nonacid GER episodes.

METHODS
A total of 22 (16 male) symptomatic premature infants
with a median gestational age at birth of 31 weeks (range, 24
to 32 weeks) and a median birth weight of 1220 g (range, 630
to 2250 g) were enrolled in the study at a median age of 29
days (range, 12 to 83 days) and a median weight of 1747 g
(range, 1150 to 3215 g). The infants exhibited frequent regurgitation and postprandial desaturation; in addition, 7 infants had postprandial apnea, 4 had failure to thrive, 1 had
bradycardia, and 1 had both postprandial apnea and bradycardia. All were otherwise healthy at the time of examination.
None had malformation or major gastrointestinal problems or
was taking drugs influencing gastrointestinal motility or gastric acidity. Seven infants were fed extracted human milk
fortified with 3% FM85 (Nestlé, Vevey, Switzerland), 3 were
fed a standard preterm formula, and the remaining 12 received both. All 22 infants tolerated at least 100 ml/kg per day
of milk.
The effect of postural intervention on GER was evaluated in a within-subjects design, taking for each subject
measurement of GER in different postural conditions. In a
within-subjects design, the same subjects are tested in each
condition; therefore, differences among subjects can be separated from error, increasing the power of significance tests. A
possible drawback of this method is the “carry-over” effect—a
persistent effect in a subsequent treatment period from treatment in the previous period. In our study, this could be
represented by the effect on GER of each position on the
subsequent position. To limit this effect, we randomly assigned to each enrolled infant a different sequence of the
possible postural combinations.

Postural Intervention
In the 24-hour examination, 4 positions—supine (S),
prone (P), right side (RS), and left side (LS)—were studied.
Each position was maintained for 6 hours, except for 2
periods of 30 minutes each for feeding. The order of different
positions was assigned randomly and was not known by the
data analysts. Each infant received 8 meals (1 every 3 hours)
through a feeding bottle or an orogastric tube, inserted and
removed at each meal. This approach allowed us to include 2
meals and 2 150-minute postprandial periods in each body
position.
GER Monitoring
Each patient underwent a 24-hour, continuous, simultaneous measurement of intraesophageal pH and multichannel electrical impedance. The system was calibrated before
each measurement using pH buffer solutions of pH 4.0 and
pH 7.0. A single-use combined MII–pH probe (Comfortec
592

Corvaglia et al

MII-pH, 2.1 mm in diameter; Sandhill Scientific, Highlands
Ranch, CO) was used. The flexible catheter contained seven
impedance electrodes representing 6 bipolar impedance channels and 1 antimony electrode for pH detection. The distance
between each impedance electrode was 1.5 cm, except for the
distal couple spaced at 2 cm. The pH sensor was located 1 cm
above the distal impedance ring, in the middle of the most
distal impedance-measurement segment. The catheter was
inserted through a nostril without sedation and placed under
fluoroscopic guidance. The tip was fixed 1 to 1.5 cm above the
gastroesophageal junction. Before removal, the position of the
catheter was compared with the initial position by checking
the depth mark on the catheter, to exclude possible displacement. Data were acquired on a portable Sleuth system (Sandhill Scientific), stored at the end of each test in a personal
computer, and analyzed by BioVIEW Analysis software, version 5.0.9 (Sandhill Scientific) and by direct visual evaluation
of each event.
During each GER episode, we recorded the minimum
pH value; the height (in cm), calculated by the distance from
the lower esophageal sphincter (LES) of the most proximal
electrode that detected the reflux; and the duration (in seconds), defined as the time between the onset of GER and the
recovery of 50% of the initial impedance value, measured at
the level of the distal impedance bipolar channel (ie, 1.5 cm).
To be detected as MII-GER, the bolus, moving in a retrograde direction, had to contact at least 3 impedance electrodes, reaching a height of at least 4 to 4.5 cm above the
gastroesophageal junction. An MII-GER episode was defined as acid (aMII-GER) if the pH was ⬍4 and as nonacid
(NaMII-GER) if the pH was ⱖ4.7 The total percentage of
time with a MII-GER in the esophagus was indicated as
bolus exposure index (BEI) and further separated into acid
(aMII-GER-BEI) and nonacid (NaMII-GER-BEI) reflux
indexes.
The number of all acid GERs, including those detected
only by pH electrode and those detected by MII as well, was
classified as pH-acid-GER. The total percent time of esophageal exposure to a pH ⬍ 4 was designated as the reflux index
(RIpH). This latter measurement substantially represents a
traditional pH monitoring and includes periods of acid
esophageal exposure associated with retrograde movement
detected by MII and periods with acid esophageal exposure
not associated with retrograde movement detected by MII.
The mean time (in seconds) required for pH to return to 4
after a GER episode was designated the mean acidic clearing time (MACT).
Because the features of GER change during postprandial hours,8 we further analyzed and compared GER indexes
measured during the first 75 postprandial minutes (first period) with those measured during the second 75 postprandial
minutes (second period).
The study design was approved by the hospital’s Institutional Ethics Committee. Written informed consent was
obtained from a parent of each infant enrolled in the study.
The Journal of Pediatrics • December 2007

Table I. Reflux parameters measured in the 22 patients
Total

Left side

Right side

Supine

Prone

P

Liquid GER (n)

40.5 (20.5)
0-87

7.9 (4.8)
0-20

13.6 (8.8)
0-30

15.9 (9.7)
0-39

3.1 (2.6)
0-10

Gaseous GER (n)

4.8 (5.2)
0-19
7.4 (5.9)
0-22
11.7 (9.1)
1-35

1.7 (2.1)
0-8
2.3 (2.6)
0-11
1.9 (2.1)
0-8

1.1 (1.4)
0-5
2.5 (2.9)
0-13
4.2 (4.4)
0-18

0.9 (1.2)
0-4
1.7 (1.9)
0-7
4.3 (3.5)
0-12

1.1 (2)
0-8
0.8 (1.4)
0-6
1.1 (1.2)
0-3

LS vs RS: .012
LS vs S: .002
P vs RS, S, LS: .001
NS

35.9 (22)
2-91
73.7 (44.3)
3-149
0.3 (0.2)
0-0.7

8.3 (5.8)
0-21
17.9 (15.7)
0-56
0.2 (0.3)
0-1

11.9 (8.9)
0-36
27.1 (18.1)
3-66
0.5 (0.5)
0-1.7

12.9 (9.1)
1-35
21.9 (15.3)
0-56
0.5 (0.5)
0-1.7

2.8 (2.6)
0-8
6.8 (5.3)
0-17
0.1 (0.1)
0-0.4

0.9 (0.5)
0-1.8
12.7 (10.5)
1.6-37.9

0.7 (0.6)
0-2.1
7.5 (8.2)
0-32.2

1.2 (0.9)
0-2.6
21.4 (19.4)
0.4-68.4

1.3 (1)
0.11-3.3
17.6 (16.1)
0-48.6

0.3 (0.3)
0-1
4.4 (5.8)
0-19.8

119.8 (116.1)
26.4-582.6
3.5 (1.2)
1.8-7.2

93.2 (143.9)
0-701.8
3.9 (1.7)
1.7-9

176.4 (245.6)
26.4-1216.9
3.4 (1.2)
1.5-7

162.7 (103)
17.1-282.9
3.8 (1.3)
1.7-7.3

94.9 (91.1)
0-257.1
3 (1.4)
0-7

Mixed GER (n)
aMII-GER (n)

NaMII-GER (n)
pH-acid-GER (n)
aMII-GER-BEI (%)

NaMII-GER-BEI (%)
RipH (%)

MACT (sec)
Mean MII-GER
height (cm)

NS
P vs S: .001
P vs RS: .019
LS vs S: .029
P vs RS, S, LS: .001
P vs S, RS: .001
P vs LS: .006
P vs RS: .001
P vs S: .006
RS vs LS: .015
P vs S, RS: .0001
LS vs S: .011
P vs RS: .001
P vs S: .002
LS vs RS: .004
LS vs S: .014
P vs S: .016
LS vs RS: .021
NS

NS, not significant.
Values are expressed as mean (standard deviation) and range.

Statistical Analysis
All statistical analyses were performed with SPSS 13.0
for Windows (SPSS Inc, Chicago IL). Normal distribution
was first evaluated by the Kolmogorov-Smirnov test. Reflux
variables in each position were analyzed using generalized
likelihood model repeated-measures design (1 within-subjects
factor) and Bonferroni post hoc pairwise comparison; differences between the first and second postprandial periods were
tested by paired-sample t tests. A P value ⬍ .05 was considered statistically significant.

percent times of esophageal exposure to reflux of 0.3%, 0.9%,
and 12.7%.

RESULTS

Effect of Position on the Physical Composition
of Refluxate
GER episodes were first analyzed regarding physical
composition of the refluxate. In each position, most of the
GER refluxate was liquid, although some was gaseous or
mixed. Liquid refluxate was significantly less frequent in the
LS and P positions compared with the RS and S positions
(P ⬍ .01) (Table I). There were no significant differences
among positions regarding gaseous and mixed episodes.

The test was well tolerated by all of the patients, and
their clinical status remained stable. No probe position
changes were detected during any examination. We analyzed
a total of 176 postprandial periods (44 periods for each
position), with a mean duration of 149 minutes (range, 145 to
157 minutes).
RIpH measurements in the 22 patients are given in
Table I. During the 20-hour monitoring (24 hours minus 4
feeding hours), the mean total number of recorded GER
episodes was 109.7 (5.5 per hour). The mean numbers of
aMII-GER, NaMII-GER, and pH-acid-GER episodes were
11.7, 35.9, and 73.7, respectively, with corresponding mean

Effect of Position on Impedance-Detected and
pH-Detected Reflux
When values were analyzed by different positions, we
observed a reduction of each type of MII-pH– detected GER
in the LS and P positions compared with the RS and S
positions (Figures 1 and 2). In particular, acid exposure time
(RIpH) and MACT were significantly lower in both the P
and LS positions compared with the S and RS positions. We
found no difference between the P and LS positions. The P
position exhibited significantly fewer Na-MII-GER episodes
than the other 3 positions.

The Effect of Body Positioning on Gastroesophageal Reflux in Premature Infants: Evaluation by Combined Impedance
and pH Monitoring

593

all of the other positions (P ⬍ .01) (Figure 4; available at
www.jpeds.com).

DISCUSSION

Figure 1. RIpH in different body positions (—, median; ---, 95th
percentile).

Improvement in all GER indexes in the P and LS
positions was seen in all patients except 1, who showed better
GER indexes in the S and RS positions than in the P and LS
positions. In this patient, an upper radiograph study with a
barium swallow performed after MII-pH monitoring demonstrated a gastric malrotation. We decided not to exclude
this patient from the analysis, because the inclusion criteria
were fulfilled, and the diagnosis of malrotation was made after
the MII-pH monitoring had been performed. Moreover, we
verified that the exclusion of this patient would not have
affected the global results; in fact, in an analysis performed
excluding this patient, all statistical significances did not vary
(data not showed).

Influence of Position on the Height of GER Episodes
No difference among positions was found in mean
height reached by GER episodes.
Changes in the Composition of Postprandial
Refluxate Over Time
Comparison of the 2 postprandial periods (Table II)
revealed that acid GER indexes (RIpH and aMII-GER-BEI)
were significantly higher in the second postprandial period
than in the first postprandial period in all of the positions
studied except P. In the first postprandial period, the P and
LS positions were associated with a significantly lower RIpH
compared with the S and RS positions (P ⬍ .01). RIpH was
the lowest in the LS position (with 12 of the 22 patients
having a RipH of 0%), significantly lower than in the P
position (LS ⫽ 0.8% vs P ⫽ 3.6%; P ⬍ .05) (Figure 3;
available at www.jpeds.com).
During the second postprandial period, the P position
was associated with strongly reduced esophageal acid exposure
compared with the other 3 positions (P ⬍ .01). RIpH was
lower in the LS than in the S and RS position (P ⬍ .01);
however, RIpH was significantly higher in the LS position
than in the P position (14.3% vs 5%; P ⫽ .016). In the first
postprandial period, Na-MII-GER-BEI was significantly
lower in the P position compared with the RS and S positions
(P ⬍ .05); in the second postprandial period, Na-MII-GERBEI was significantly lower in the P position compared with
594

Corvaglia et al

In this study, we found fewer GER episodes when
infants were placed in the LS and P positions compared with
the RS and S positions. Body position had no influence on the
proximal extent of MII-detected GER episodes. In each body
position, we noticed a decrease in the number of postprandial
nonacid GER episodes and an increase in the number of
postprandial acid GER episodes over time.
GER is common in preterm infants; the almost fixed
lying position promotes the entry of liquid gastric contents
into the esophagus when TLESR occurs. Additional risk
factors associated with preterm birth include high total fluid
enteral intake, frequent handling by nurses, and the use of
permanent feeding tubes.9
A study in asymptomatic preterm neonates found a
median of 71 reflux episodes in 24 hours.10 Although GER is
asymptomatic in most preterm infants, in some it may cause
such symptoms as desaturation, regurgitation, and bradycardia or can lead to such complications as apnea, recurrent
desaturation and/or aspiration, difficulties in oral feeding,
vomiting, and failure to thrive.1 Although acid reflux episodes
are considered more likely associated with symptoms in preterm infants,11 recent studies indicate that nonacid reflux can
produce these symptoms as well.12
For preterm infants with symptomatic GER, a stepwise
approach, based mainly on conservative interventions, is the
best therapeutic choice. Drugs should be the last option,
considering that cisapride was withdrawn from the market
because of its possible cardiac side effects,13 and treatment
with gastric acid inhibitors is not without risk.14,15
In a previous study, we found no reduction of GER
from thickening human milk with precooked starch.16 Moreover, a possible relationship between milk thickening and the
development of necrotizing enterocolitis has been described
in 2 preterm infants.17
Few studies have evaluated the influence of body position on acid GER in preterm newborns, and, to the best of
our knowledge, none have investigated the influence of body
position on nonacid GER. Omari et al5 evaluated the incidence of GER in 10 newborns with mild prematurity and
without GER symptoms using a combined MII and manometry catheter and found an advantage of LS over RS positioning in terms of a reduced number of GER episodes. Although
that study provided important data concerning GER pathological mechanisms, the presence of a trans-LES catheter
could have increased the number of GER episodes, and the
absence of a pH sensor did not allow the authors to differentiate acid and nonacid episodes. Another study confirmed
these findings in 18 premature babies with GER symptoms
using pH monitoring and comparing the P position with the
RS and LS positions.4 But that study evaluated only acid
episodes with no information about the S position, the most
frequently used position in both term and in preterm newThe Journal of Pediatrics • December 2007

Figure 2. aMII-BEI and NaMII-BEI in different body positions (—, median; ---, 95th percentile). (aMII-BEI: P vs RS P ⫽ .001, P vs S ⫽ P ⫽ .006,
RS vs LS P ⫽ .015; NaMII-BEI: P vs RS P ⫽ .0001, P vs S ⫽ P ⫽ .0001, RS vs LS P ⫽ .011.)

Table II. Variation of acid and nonacid GER during postprandial periods
RIpH
Left side
First period
Second period
Right side
First period
Second period
Supine
First period
Second period
Prone
First period
Second period
Total
First period
Second period

P

aMII-GER-BEI

P

NaMII-GER-BEI

P

0.8 (1.5) 0-5.5
14.3 (16) 0-64.4

.001

0 (0.1) 0-0.3
0.2 (0.5) 0-2

.03

1.2 (1) 0-3.7
0.2 (0.2) 0-0.6

.0001

9.9 (21) 0-92.1
32.9 (26.1) 0.7-84.3

.001

0.3 (0.5) 0-2.2
0.8 (0.9) 0-2.5

.01

2.2 (1.7) 0-5.2
0.2 (0.3) 0-0.8

.0001

5.4 (13.4) 0-54.9
29.7 (25.6) 0-72.6

.0001

0.1 (0.2) 0-0.6
0.9 (0.9) 0-3.1

.0001

2.2 (1.7) 0.2-5.5
0.4 (0.8) 0-3.1

.0001

3.6 (8.7) 0-37.3
5.1 (7.3) 0-33.7

NS

0 (0.1) 0-0.4
0.1 (0.2) 0-0.9

.04

0.7 (0.6) 0-2.0
0 (0.1) 0-0.5

.0001

.0001

0.1 (0.1) 0-0.5
0.5 (0.4) 0-1.4

.001

1.6 (0.9) 0.1-3.5
0.21 (0.3) 0-1.0

.0001

4.9 (9.3) 0-34.3
20.5 (14.3) 0.2-47.8

Values are expressed as mean (standard deviation) and range.

borns. Recognizing that nonacid reflux episodes are common
in premature infants, we believe that combined MII-pH
monitoring is the most appropriate method for evaluating
GER in preterm newborns.
In our study, RIpH was mostly measured only by a pH
electrode (placed 1.5 to 2 cm above the diaphragm), not by
MII (with the most distal 2 electrodes placed at about 4.5 cm
above diaphragm). Thus, GER episodes were detected in 2
different esophageal sites 3 cm apart; this distance is particularly relevant considering the total esophageal length of
about 6 to 10 cm. For this reason, we can state that in
symptomatic preterm infants, most GER occurs in the distal
half of the esophagus. Even in adults, a 6-fold increase in acid
exposure (mean RipH, 11.7% vs 1.8%) was found between the
more distal and proximal pH measurements.18

Our data are not comparable with those from previous
studies, due to methodological differences. Wenzl,6 Skopnik
et al,19 and others reported that most GER episodes reached
the proximal esophagus because they considered as GER
episodes only those detectable by both MII and pH probes. In
comparison, we also considered numerous short-segment episodes detected only by the pH probe. Omari et al11 characterized most GER episodes as nonacid, because they first
detected all GER episodes by manometry just above the LES
and then classified them as acid or nonacid by a pH electrode.
In contrast, we were able to detect GER episodes just above
the LES only by the pH probe.
We found that the P and LS positions significantly
decreased the number of acid and nonacid GER episodes
compared with the S and RS positions. The effect of the LS

The Effect of Body Positioning on Gastroesophageal Reflux in Premature Infants: Evaluation by Combined Impedance
and pH Monitoring

595

position in reducing GER is due mainly to a functional
factor—reduced TLESR episodes— by laying the gastric contents on the gastric body and greater curvature, which together act as a reservoir.5 The effect of the P position is
related mainly to an anatomic factor. In this position, the
LES is above the gastric body, far from the gastric contents;4
thus, when a TLESR occurs, the gastric contents are farther
from the LES and are less likely to go back into the esophagus.
Our separate analysis of the incidence of acid and nonacid GER episodes and the relationship with different body
positions in the first and second postprandial periods revealed
that in the first period, the degree of acid esophageal exposure
was 4-fold higher in the P position compared with the LS
position (percent time, 3.6% vs 0.8%; P ⬍ .05). In dyspeptic
adults, after meals in upright position, a pocket of unbuffered
acid juice forms near the gastroesophageal junction; it seems
to escape the buffering effects of meals, remaining highly acid
compared with the body of the stomach.20 The presence of a
similar pocket in preterm infants lying in the P position could
explain the higher esophageal acid exposure in the P position
than in the LS position during the first postprandial period.
In contrast, in the second postprandial period, esophageal
acid exposure was higher in the LS position than in the P
position (P ⫽ .016). These findings suggest that acid exposure
can be optimally reduced by keeping the newborn on the left
side during the early postprandial period and in the prone
position thereafter.
In conclusion, our study suggests that placing premature infants in a prone or left lateral position during the
postprandial period is a simple intervention to limit GER.
Our findings do not provide any information on clinical
improvement, because the study was not designed to monitor
the effect of postural intervention on GER symptoms. Further studies are needed to evaluate the effective correlation
between postural intervention and improvement of GER
symptoms.

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The Journal of Pediatrics • December 2007

Figure 3. RIpH in the first and second postprandial periods in the LS
and P positions (—, median; ---, 95th percentile).

Figure 4. aMII-BEI and NaMII-BEI in the first and second
postprandial periods in the LS and P positions (—, median; ---, 95th
percentile).

The Effect of Body Positioning on Gastroesophageal Reflux in Premature Infants: Evaluation by Combined Impedance
and pH Monitoring

596.e1

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