Vol. 277, Issue 4, G862-G866, October 1999
Measurement of upper esophageal sphincter tone and relaxation
during swallowing in premature infants
T.
Omari1,
A.
Snel2,
C.
Barnett2,
G.
Davidson1,
R.
Haslam2, and
J.
Dent3
1 Gastroenterology
Unit and
2 Neonatal Medicine
Unit, Women's and Children's
Hospital, North Adelaide, South Australia 5006; and
3 Gastrointestinal
Medicine, Royal Adelaide Hospital, Adelaide, South
Australia 5000, Australia
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ABSTRACT |
Upper esophageal sphincter (UES) motor function
has not been previously evaluated in premature infants. The motor
patterns associated with tonic activity and swallow-related relaxation of the UES were recorded for 1 h after completion of gavage feeding in
11 healthy preterm neonates (postmenstrual age 33-37 wk) with a
micromanometric assembly, which included a sleeve sensor specifically adapted for UES recordings. A clearly defined UES high-pressure zone
was observed in all premature infants studied. Resting UES pressure
ranged from 2.3 to 26.2 mmHg and was higher during periods of
irritability and apparent discomfort. During dry swallows, UES pressure
relaxed from a resting pressure of 28.2 ± 4.0 mmHg to a nadir of
1.1 ± 3.3 mmHg. The mean UES relaxation interval (the time from
relaxation onset to relaxation offset) was 0.31 ± 0.11 s. We
conclude that in premature infants 
33 wk postmenstrual age the motor
mechanisms regulating UES resting pressure and the onset of UES
relaxation are well developed.
esophageal motility; preterm infant
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INTRODUCTION |
NORMAL SWALLOWING REQUIRES the precise coordination of
lingual propulsion and pharyngeal contraction with relaxation and
opening of the upper esophageal sphincter (UES). This mechanism
facilitates the passage of a food bolus and is also the major mechanism
of pharyngeal clearance. UES resting pressure is generated
predominantly by tonic contraction of the cricopharyngeus muscle. With
swallowing, the cricopharyngeus muscle is inhibited and the UES is
opened by a combination of intrabolus pressure and the superior
excursion of the hyoid and larynx (4, 7). Studies in children have demonstrated UES pressures comparable with those of adults (40-50 mmHg) and UES relaxation in response to swallowing (5, 18, 19). In
addition, basal UES pressure is highly dependent on state of arousal,
varying from 18 mmHg during rest to 56 mmHg when crying. Abrupt changes
in the level of arousal are similarly associated with abrupt changes in
UES pressure (5).
The function of the UES of the premature neonate has not been
documented until now because of the lack of suitable micromanometric sleeve assemblies for evaluation of UES tone and relaxation. Such assemblies have now been made, and the aim of this study was to use
these to characterize UES motor function for the first time in
premature infants.
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MATERIALS AND METHODS |
Subjects.
The study protocol was approved by the Ethics Research Committee of the
Women's and Children's Hospital, and written informed parental
consent was obtained before each study. Studies were performed in 11 (5 male and 6 female) healthy preterm infants with a mean postmenstrual
age of 35 wk (range 33-37 wk). All infants were well at the time
of the study, were considered not to have reflux disease, had no
evidence of neurological dysfunction, and were not on prokinetic
medication. Mean infant weight was 1,840 g (range 1,600-2,290 g).
Four infants were receiving either theophylline or caffeine treatment
because of previous episodes of apnea and bradycardia. All 11 infants
were being gavage (tube) fed, 7 with nonfortified expressed breast milk
and 4 with infant formula (S26 low birth weight formula, Wyeth
Australia, Parramatta, NSW, Australia).
Manometric technique.
The manometric technique used allowed monitoring of
pressures from the pharynx, UES, and esophageal body with an assembly that could also be used to feed the infants. The intraluminal portion
of the manometric assembly consisted of a 2.0-mm diameter 10-lumen
extrusion that incorporated a 2-cm-long sleeve sensor for UES pressure
measurement. The UES sleeve was ovalized in cross section (Fig.
1) by "shaving" the extrusion and
building it up laterally (OD 1.8 × 4 mm) to enable consistent
anterio-posterior self orientation of the sleeve within the radially
asymmetric pressure profile of the UES high-pressure zone (6, 8). Six side-hole sensors recorded pressures from the pharynx (two), UES (one),
and esophageal body (three) (Fig. 1). The assembly was long enough to
ensure reliable delivery of feeds to the stomach via the large central
lumen. Pharyngeal side holes were air-perfused at 4 ml/min; all other
side holes were perfused with sterile degassed water at 0.04 ml/min.
The UES sleeve was perfused at 0.08 ml/min to ensure that the rate of
pressure rise at the distal margin of the sleeve was 20 mmHg/s,
sufficient for reliable recording of the onset of UES tone after
relaxation. Air/water flow rates were controlled by hydraulic resistors
(Dentsleeve, Wayville, SA, Australia). Bubble entrapment was minimized
by preflushing of manometric lines and catheters with carbon dioxide
(15).
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Fig. 1.
Schematic diagram of upper esophageal sphincter (UES) sleeve assembly
in situ alongside a manometric recording of pharyngeal, UES, and
esophageal pressures during pharyngeal swallow (sw). A diagram of UES
sleeve sensor oval cross section is also shown.
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Analog pressure transducer and pH probe signals were amplified and
filtered with a Synectics polygraph (Synectics, Stockholm, Sweden).
Data acquisition and analysis were performed on a Macintosh Quadra 700 with software based on National Instruments' Labview (M.A.D. Software,
Royal Adelaide Hospital, C. Malbert).
Protocol.
The assembly was passed transnasally and positioned
with the UES sleeve straddling the UES high-pressure zone and the UES side hole just proximal to the UES high-pressure zone on the basis of
observed pressure patterns and depth of insertion. After positioning and with the infant in the right lateral position, the feed was administered into the stomach over 10-15 min via the core channel of the assembly. Patterns of UES motor function were then recorded during the gavage feed and then for 1 h postprandially. No boluses were
administered orally. The assembly was well tolerated by infants with no
adverse effects related to the procedure.
In addition to motility, infant behavioral patterns were observed.
Behavioral patterns were characterized according to criteria established by Davidson et al. (5) and consisted of the following: A,
resting/eyes open; B, resting/eyes closed; C, moving/comfortable; D,
restless/uncomfortable; and E, irritable/crying. Patterns were scored
continuously at 30-s intervals for the duration of the study period
(i.e., 120 times over 60 min).
Analysis of manometric tracings.
The postprandial manometric recordings were analyzed to
determine resting UES pressure and the characteristics of UES
relaxation during spontaneous "dry" swallowing.
Resting UES pressure was determined for the whole study in periods of
30 s and expressed relative to basal hypopharyngeal pressure. UES
pressure drops that occurred in association with swallowing were
excluded from the analysis.
For each swallow-induced UES relaxation, the resting pressure before
relaxation, the nadir pressure at maximal relaxation, and the
relaxation interval were determined. The relaxation interval was
defined as the time from relaxation onset, recorded by the sleeve, to
relaxation offset, recorded by the side hole located just proximal to
the UES (Fig. 2). This measurement provides
the best manometrically determinable estimate of physiological UES opening and closing compared with video fluoroscopy (10). UES relaxations that were suboptimally recorded (because of incorrect sleeve position or movement/straining artifact) or occurred in response
to multiple swallowing (a sequence of two of more swallows with an
interswallow interval of <5 s) were excluded from the analyses.
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Fig. 2.
Method of analysis of UES pressure recordings for measurement of UES
relaxation characteristics. Left: example tracing of a
pharyngeal swallow. Right: expanded time scale to illustrate
the following measured parameters. a,
Resting UES pressure; b, time from
relaxation onset to maximum relaxation;
c, nadir pressure;
d, time from relaxation onset to
relaxation offset (recorded by UES side hole);
e, relaxation interval corresponding
to UES opening.
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Statistical analysis.
Grouped data were compared with an ANOVA technique
(F-test and Scheffé's test).
Correlation was determined by simple regression analysis.
P < 0.05 was considered
statistically significant. Data are expressed as means ± SD.
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RESULTS |
UES motor function.
All infants exhibited a manometrically identifiable UES high-pressure
zone that relaxed in response to pharyngeal swallow. The mean resting
UES pressure of all infants was 15.2 ± 6.9 mmHg and ranged from 2.3 ± 5.9 to 26.2 ± 6.2 mmHg. Resting UES pressure did not
correlate with postmenstrual age
[r = 0.036; not significant (ns)] or postnatal age (r = 0.045; ns). Resting UES pressure in infants having
theophylline/caffeine therapy did not differ from those not receiving
this treatment (12.8 ± 3.8 mmHg vs. 16.5 ± 8.1 mmHg,
respectively; ns). Infants receiving breast milk feeds had similar UES
pressures to those receiving formula feeds (14.8 ± 8.2 mmHg vs.
15.9 ± 4.8 mmHg).
UES relaxation characteristics were analyzed for a total of 326 dry
swallows (mean of 36 swallows per study, range 7-118). The mean
resting UES pressure at the onset of relaxation ranged from 21.5 to
32.3 mmHg (overall mean 28.2 ± 4.0 mmHg). Nadir UES pressure ranged
from 
4.4 to 5.4 mmHg (overall mean 1.1 ± 3.3 mmHg). The time
from relaxation onset to maximum relaxation ranged from 0.22 to 0.34 s
(overall mean 0.28 ± 0.04 s). The time from relaxation
onset to relaxation offset ranged from 0.45 to 0.78 s (overall mean
0.59 ± 0.10 s), and the relaxation interval ranged from 0.14 to
0.49 s (overall mean 0.31 ± 0.11 s). None of these characteristics
were altered by the presence of theophylline/caffeine therapy or feed
type, nor were these parameters influenced by postmenstrual age.
Postnatal age did not correlate with the resting pressure at relaxation
onset, the time from onset to maximal relaxation, or the nadir
pressure. However, a significant correlation was observed between older
postnatal age and a shorter time interval from UES relaxation onset to
relaxation offset (r = 0.828;
P < 0.01) and shorter UES relaxation
intervals (r = 0.785;
P < 0.05). The number of oral feeds
per day that individual infants were receiving (ranging from 1 to 5, mean 1.5) was not significantly associated with the UES relaxation
interval (r = 0.253 and 0.171, respectively; ns) or postnatal age (r = 0.476 and 0.418, respectively; ns) but did correlate with
postmenstrual age (r = 0.641;
P < 0.05).
Effect of infant behavior on resting UES pressure.
Behavioral patterns A (resting/eyes open), B (resting/eyes closed), and
C (moving/comfortable) were observed for 96% of the total time
recorded (65%, 7%, and 24%, respectively). In contrast, behavioral
patterns D (restless/uncomfortable) or E (irritable/crying) were less
frequently observed (3% and 1% of total time recorded), suggesting
that the manometric technique used in this study was well tolerated by
the infants. Infant behavioral patterns greatly influenced resting UES
pressure, with higher UES pressures recorded during periods when
behavioral patterns indicated a heightened state of arousal (Fig.
3). Mean resting UES pressure increased from 13.5 ± 11.0 mmHg for behavioral pattern A to 33.8 ± 16.7 mmHg for behavioral pattern E (P < 0.0001). Abdominal straining was also observed to transiently augment
UES pressure, although the degree of increase in UES pressure during
straining was not quantified.
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Fig. 3.
Effect of infant behavior on resting UES pressure.
A, resting/eyes open;
B, resting/eyes closed;
C, moving/comfortable;
D, restless/uncomfortable;
E, irritable/crying. *Significantly
different from A;
 significantly different from
B; §significantly different from
C (P < 0.0001) via ANOVA.
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DISCUSSION |
This study examines, for the first time, UES motor function in
premature infants by micromanometric recording techniques. In these
babies, UES motor patterns are almost identical to those recorded
previously in older infants, children, and adults with similar
techniques (4, 5, 7, 8, 10).
Premature infants exhibit UES resting tone and UES relaxation in
response to dry swallow. The magnitude of UES resting pressure is
greatly dependent on the behavioral state of the infants. The scoring
of infant behavioral patterns in real time was relatively easy to
perform. In practice, continuous behavioral scoring at 30-s intervals
proved to be sufficiently frequent to effectively monitor changes in
patterns of general behavior. Periods of apparent comfort were
associated with significantly lower UES pressures than periods of
activity and apparent discomfort or abdominal straining. These findings
are consistent with those reported in older infants and children with
the same behavioral scoring system (5, 19). Studies in adults have
shown that resting UES pressure is low during sleep and increases
during arousal (9), whereas factors such as emotional stress and
straining considerably augment UES pressure (3, 19).
On average, UES relaxation intervals associated with dry swallows in
premature infants were similar to those recorded in healthy adult
subjects. Kahrilas and colleagues (10) showed that the relaxation interval corresponds closely to the physiological opening and closing of the UES and that the presence of a food bolus during swallowing prolongs both the UES relaxation interval and the duration of UES opening. The UES relaxation interval in premature infants varied
considerably, from 0.14 to 0.49 s, and our data suggest that this
parameter became shorter as postnatal age increased. An important
distinction between the current study and previous adult studies,
however, is that we examined spontaneous swallows and not swallows
initiated on command. The variation in the UES relaxation interval may
therefore be due to differences in the volume of saliva accumulated
during the interswallow period. In addition, more premature infants may
swallow less frequently, leading to greater accumulation of saliva and
longer relaxation intervals.
Our data suggest that premature infants have manometrically normal
patterns of UES tone and dry-swallow-related UES relaxation. Previous
studies in premature infants have also shown that dry-swallow-related esophageal body peristalsis and lower esophageal sphincter relaxation are also manometrically normal (16, 17). Premature infants still,
however, experience difficulty with feeding, requiring gavage feeding
despite their apparently normal sphincter motility. One explanation for
this may be that effective passage of a food bolus past the UES depends
on the generation of sufficient intrabolus pressure to open the UES,
even though it is relaxed. Intrabolus pressure is not generated by
pharyngeal contraction, but is instead generated by the piston-like
posterior movement of the base of the tongue (7). Hypopharyngeal
contractions follow the passage of the bolus and function to clear the
pharynx of feed residues (11). This characterization of the swallowing
mechanism of adults shows clearly that, although the manometrically
recorded patterns of pharyngeal and UES function during dry swallowing
in premature babies may resemble those seen in adults, these infants
may nevertheless experience feeding difficulties if they have a
diminished capacity to generate the intrabolus pressures required to
propel the bolus beyond the UES. These pressures were not evaluated in
this study. It is certainly the case that lingual coordination and
feeding capacity is impaired in premature infants and improves as they approach term (2). Premature infants also generate 40% lower intraoral
pressures when sucking compared with full-term infants (1, 13).
Synchronization of breathing with swallowing is also usually rare in
prematurity, probably explaining the episodes of apnea, bradycardia,
and oxygen desaturation that occur during swallowing (12, 14). These
additional factors may also contribute to feeding difficulties.
This study shows that the manometric determinants of UES motor
function, such as UES tone and relaxation characteristics, can be
measured in premature infants by miniaturization of established techniques developed for use in adult humans. In premature infants, the
esophageal motor mechanisms that generate and modify UES tone appear
well developed. Pharyngeal dry swallows are well coordinated with the
onset of appropriate relaxation of the UES. Our data suggest that the
oral feeding difficulties experienced by premature infants may be due
to factors other than immaturity of the neuroregulatory mechanisms of
UES motility.
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ACKNOWLEDGEMENTS |
We thank Ros Lontis and Louise Goodchild for facilitating patient
recruitment and providing specialized nursing care at the cotside, Dr.
Charles Malbert for the computerized data acquisition and analysis
software used in this study, Rohan Williams for assistance with
analysis, and Malcolm Bakewell for providing invaluable technical support.
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FOOTNOTES |
This work was supported by grants from the National Health and Medical
Research Council of Australia and the Women's and Children's Hospital
Research Foundation.
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: T. Omari,
Gastroenterology Unit, Women's and Children's Hospital, 72 King
William Rd., North Adelaide, SA 5006, Australia (E-mail:
tomari{at}medicine.adelaide.edu.au).
Received 20 April 1999; accepted in final form 1 July 1999.
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Am J Physiol Gastroint Liver Physiol 277(4):G862-G866
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Copyright © 1999 the American Physiological Society
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ABSTRACT
INTRODUCTION
