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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

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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.

REFERENCES 1. Poets CF. Gastroesophageal reflux: a critical review of its role in preterm infants. Pediatrics 2004;113:128-32. 2. Frakaloss G, Burke G, Sanders MR. Impact of gastroesophageal reflux on growth and hospital stay in premature infants. J Pediatr Gastroenterol Nutr 1998;26:146-50.

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3. Tobin JM, McCloud P, Cameron DJS. Posture and gastro-oesophageal reflux: a case for left lateral positioning. Arch Dis Child 1997;76:254-8. 4. Ewer AK, James ME, Tobin JM. Prone and left lateral positioning reduce gastro-oesophageal reflux in preterm infants. Arch Dis Child Fetal Neonatal Ed 1999;81:F201-5. 5. Omari TI, Rommel N, Staunton E, Lontis R, Goodchild L, Haslam RR, et al. Paradoxical impact of body positioning on gastroesophageal reflux and gastric emptying in the premature neonate. J Pediatr 2004;145:194-200. 6. Wenzl TG. Investigating esophageal reflux with the intraluminal impedance technique. J Pediatr Gastroenterol Nutr 2002;34:261-8. 7. Sifrim D, Castell D, Dent J, Kahrilas PJ. Gastro-esophageal reflux monitoring: review and consensus report on detection and definitions of acid, nonacid, and gas reflux. Gut 2004;53:1024-31. 8. Wildi SM, Tutuian R, Castell DO. The influence of rapid food intake on postprandial reflux: studies in healthy volunteers. Am J Gastroenterol 2004;99:1645-51. 9. Peter CS, Wiechers C, Bohnhorst B, Silny J, Poets C. Influence of nasogastric tubes on gastroesophageal reflux in preterm infants: a multiple intraluminal impedance study. J Pediatr 2002;14:277-9. 10. Lòpez-Alonso M, Moya MJ, Cabo JA, Ribas J, Macias MdC, Silny J, et al. Twenty-four-hour esophageal impedance-pH monitoring in healthy preterm neonates: rate and characteristics of acidic, weakly acidic, and weakly alkaline gastroesophageal reflux. Pediatrics 2006;118:e299-308. 11. Omari TI, Barnett CP, Benninga MA, Lontis R, Goodchild L, Haslam RR, et al. Mechanism of gastro-oesophageal reflux in preterm and term infants with reflux disease. Gut 2002;51:475-9. 12. Wenzl TG, Silny J, Schenke S, Peschgens T, Heimann G, Skopnik H. Gastroesophageal reflux and respiratory phenomena in infants: status of the intraluminal impedance technique. J Pediatr Gastroenterol Nutr 1999;28:423-8. 13. Corvaglia L, Faldella G, Rotatori R, Lanari M, Capretti MG, Salvioli GP. Intrauterine growth retardation is a risk factor for cisapride-induced QT prolongation in preterm infants. Cardiovasc Drug Ther 2004;18:371-5. 14. Guillet R, Stoll BJ, Cotten CM, Gantz M, McDonald S, Poole WK, Phelps DL, National Institute of Child Health and Human Development Research Network. Association of H2-blocker therapy and higher incidence of necrotizing enterocolitis in very low birth weight infants. Pediatrics 2006;117:e137-42. 15. Canani RB, Cirillo P, Roggero P, Romano C, Malamisura B, Terrin G, et al, Working Group on Intestinal Infections of the Italian Society of Pediatric Gastroenterology, Hepatology and Nutrition. Therapy with gastric acidity inhibitors increases the risk of acute gastroenteritis and community-acquired pneumonia in children. Pediatrics 2006;117:e817-20. 16. Corvaglia L, Ferlini M, Rotatori R, Paoletti V, Alessandroni R, Cocchi G, et al. Starch thickening of human milk is ineffective in reducing the gastroesophageal reflux in preterm infants: a crossover study using intraluminal impedance. J Pediatr 2006; 148:265-8. 17. Clarke P, Robinson MJ. Thickening milk feeds may cause necrotizing enterocolitis. Arch Dis Child Fetal Neonatal Ed 2004;89:F280. 18. Fletcher J, Wirz A, Henry E, McColl KEL. Studies of acid exposure immediately above the gastro-oesophageal squamocolumnar junction: evidence of short segment reflux. Gut 2004;53:168-73. 19. Skopnik H, Silny J, Heiber O, Schulz J, Rau G, Heimann G. Gastroesophageal reflux in infants: evaluation of a new intraluminal impedance technique. J Pediatr Gastroenterol Nutr 1996;23:591-8. 20. Fletcher J, Wirz A, Young J, Vallance R, McColl KEL. Unbuffered highly acidic gastric juice exists at the esophageal junction after a meal. Gastroenterology 2001; 121:775-83.

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

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