Vol. 284, Issue 4, G575-G582, April 2003
Deglutitive inhibition affects both esophageal peristaltic
amplitude and shortening
Guoxiang
Shi1,
John E.
Pandolfino1,
Qing
Zhang1,
Ikuo
Hirano1,
Raymond J.
Joehl2, and
Peter J.
Kahrilas1
Departments of 1 Medicine and 2 Surgery, Northwestern
University, The Feinberg School of Medicine, Chicago, Illinois
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ABSTRACT |
Deglutitive inhibition attenuates ongoing
esophageal contractions if swallows are separated by short time
intervals. This study aimed to determine whether esophageal shortening,
mediated by longitudinal muscle, was similarly affected. Eight healthy subjects with two distal esophageal segments demarcated by mucosal clips and manometric recording sites positioned within those segments underwent concurrent manometry and fluoroscopy. Peristaltic amplitude and change in distal segment lengths were quantified during single swallows, paired swallows separated by progressively prolonged intervals, and a series of rapid repetitive swallows. During grouped swallows, deglutitive inhibition with complete attenuation of both the
manometric contraction and segment shortening was evident with
short-interval swallows and rapid-sequence swallows. No inhibition of
either was evident with long-interval pairs. With intermediate interswallow intervals, the occurrence and degree of deglutitive inhibition between peristaltic amplitude and segment shortening were
closely correlated. Deglutitive inhibition affects both the longitudinal and circular muscle layers of the esophageal wall, and the
occurrence of inhibition evident in one layer is strongly correlated
with the other.
peristalsis; swallowing
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INTRODUCTION |
DEGLUTITIVE
INHIBITION is a fundamental property of primary esophageal
peristalsis. The peristaltic activity resultant from a swallow is
rapidly and completely inhibited by a second swallow if the interval
between swallows is inadequate for the first contraction to traverse
the striated muscle (proximal) esophagus. Once the peristaltic
contraction associated with the first swallow reaches the distal
esophagus, a second swallow cannot totally inhibit the contraction but
can abort its distal propagation. Deglutitive inhibition can be
directly demonstrated experimentally by creating an artificial
high-pressure zone in the distal esophagus by wedging a manometric
catheter between the wall of the esophagus and a small intraesophageal
balloon (10-12). The resultant artificial high-pressure zone is inhibited with swallowing such that the period of
inhibition is inversely proportional to the propagation rate of the
peristaltic contraction. If a second swallow follows the first by only
a short interval, the associated peristaltic contraction may also be
attenuated or incomplete as a result of muscle refractoriness (1,
6, 14). Thus the interaction of a second swallow with an earlier
swallow is dependent on the interval between the two swallows and can
result in attenuation or complete inhibition of either peristaltic sequence.
Note that all of the experiments described above relate to the
contraction amplitude of peristalsis as recorded by esophageal manometry. Because contraction amplitude is mainly a function of
esophageal circular muscle contraction, it is reasonable to attribute
these observations to deglutitive inhibition of the circular muscle
layer of the muscularis propria. However, peristalsis also involves a
sequenced contraction of esophageal longitudinal muscle. Esophageal
shortening (a consequence of contraction of the longitudinal muscle
layer of the muscularis propria) has been studied with several
techniques: fluoroscopic observation of radiopaque markers sewn to the
esophageal muscle (2), fluoroscopic observation of
mucosally attached metal clips (3, 4, 8, 9), or observation of dynamic changes in the thickness of the longitudinal muscle layer during intraluminal high-frequency ultrasonograpy (7, 15). Such studies have demonstrated that both layers of esophageal muscle exhibit a coordinated contraction during peristalsis. However, it has yet to be ascertained as to whether or not
deglutitive inhibition affects the esophageal longitudinal muscle
contraction (esophageal shortening) in the same way that it affects the
circular muscle contraction. Thus the aim of this study was to
determine whether or not deglutitive inhibition also affects the
esophageal longitudinal muscle and, if so, how this correlates with
inhibition of the circular muscle.
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METHODS |
Eight healthy volunteers (3 males, 5 females) free of
gastrointestinal symptoms and without a history of upper
gastrointestinal surgery were studied. The mean age of participants was
26 ± 1 yr. The study protocol was approved by the Northwestern
University Institutional Review Board and informed consent was obtained
from each subject. No subjects were taking any medications that could affect esophageal motility. Tobacco use was not permitted on the day of
the study.
Endoscopic marking of the esophageal segments by mucosal
clipping.
Subjects fasted overnight before undergoing an esophagoscopy under
sedation with 1-3 mg of intravenous midazolam. During this procedure, three 11-mm stainless steel clips were attached to the
esophageal mucosa using an endoscopic clip-fixing device (HX-3L, Olympus America, Lake Success, NY). Clip 1 was fixed at the
squamocolumnar junction (SCJ), and clips 2 and 3 were placed ~3 and 6 cm proximal, respectively. Clips 1 and 2 thus delineated the distal esophageal segment, whereas
clips 2 and 3 delineated the proximal esophageal segment in the subsequent analysis (Fig.
1). After completion of the clipping
procedure, subjects were allowed to recover from sedation for at least
1 h before proceeding with the remainder of the experimental
protocol. The esophagus was again imaged fluoroscopically 1 mo after
the completion of the study, and mucosal clips that had not
spontaneously dislodged were removed endoscopically.
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Fig. 1.
Tracing of a fluoroscopic image of the lower esophagus
illustrating the experimental setup. The distal clip (Clip
1) was attached at the squamocolumanar junction. Clip 2 was attached ~3 cm proximal, and Clip 3 was attached 6 cm
proximal. Clip 1 and Clip 2 delineated the distal
esophageal segment; Clip 2 and Clip 3 delineated
the proximal esophageal segment. The sleeve sensor straddled the
esophagogastric junction.
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Manometric and fluoroscopic evaluation.
Manometric recording was performed with a 9-lumen silicone catheter,
3.5-mm outer diameter (Dentsleeve, Bowden, South Australia). A 6-cm
sleeve was used to monitor the esophagogastric junction pressures.
Side-hole recording sites were spaced 3 cm apart proximal to the sleeve
center, with an additional site 27 cm above the sleeve center that was
used as a swallow marker and another 4 cm distal to the sleeve center
used to monitor intragastric pressure (Fig. 1). Manometric recording
channels were connected to external pressure transducers that were, in
turn, connected to a 16-channel computerized polygraph (Neomedix
Systems, Warriewood, New South Wales, Australia) set at a sampling
frequency of 40 Hz. The manometric assembly was passed transnasally,
positioned such that the sleeve sensor straddled the lower esophageal
sphincter, and taped securely to the subject's nose. Subjects laid in
a supine posture and were allowed to adapt to the recording apparatus
for at least 15 min before experimentation. This was followed by a
15-min baseline recording period. Manometric data were processed using
Gastromac software (Version 3.5, Neomedix).
The subject was then positioned under a fluoroscope centered on the
lower chest and upper abdomen. Two swallows of 5 ml room-temperature water were imaged fluoroscopically. Thereafter, six to eight paired swallows separated by short, intermediate, or long intervals were tested. The intended separations between the short-, intermediate-, and
long-interval paired swallows were 3, 6, and 9 s, respectively. Finally, a series of 10-14 rapid repetitive swallows was done with
the subject swallowing as rapidly as possible. Each element of the
swallow protocol was separated by at least 30 s. Fluoroscopic images were recorded with a videotape recorder (VO 9800 model; Sony,
Tokyo, Japan) at 30 frames/s while the signals detailed in the
preceding paragraph were displayed and stored concurrently on the
polygraph. Video images and tracings recorded on the polygraph were
synchronized using a video timer (model VC 436; Thalner Electronics Laboratories, Ann Arbor, MI) that encoded time in hundredths of a
second on each video frame and sent a 1-V, 10-ms pulse to an instrumentation channel of the polygraph at whole second intervals.
Data analysis.
Fluoroscopic images were analyzed to determine the time course and
extent of clip movement. Images recorded during swallow protocols were
digitized at 0.5-s intervals and analyzed using image-analysis software
to correct for fluoroscopic magnification and to track the movement of
each clip. The lengths of the two esophageal segments between the three
clips were calculated on each digitized image. Segment lengths were
normalized among individuals by establishing the baseline separation as
100% and expressing the separation at subsequent times as a percentage
of that value. Maximal shortening of each segment was determined. A
shortening index was then calculated to normalize data among subjects.
The shortening index was equal to the fractional value of a test
swallow over the mean shortening observed with single swallows. For
example, if a subject exhibited two single swallows with segmental
shortening of 25 and 29% and a paired swallow with shortening of 27%,
the shortening index of the paired swallow was {27%/[(25% + 29%)/2]} = 1.
The amplitude of the peristaltic contraction corresponding to segment
shortening during swallows was measured from the side-hole recording
sites positioned within the limits of each esophageal segment. The mean
amplitude was calculated for single swallows for each subject from
within each esophageal segment. A contraction index was then calculated
to normalize data among subjects. The contraction index was equal to
the fractional value of a test swallow over the mean peristaltic
amplitude of single swallows. This contraction index was used to
correlate contractile amplitude with the percentage of shortening or
shortening index.
Data were summarized as means ± SE unless otherwise specified.
Averaged data were compared using Student's t-test. The
Pearson test was used to correlate the percentage of shortening with
the contraction index; P < 0.05 was considered
significant throughout.
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RESULTS |
All subjects completed the protocol without unforeseen problems;
clip attachment was easily accomplished, and the procedures were well
tolerated. The clips and sites of mucosal attachment were readily
identified fluoroscopically.
The intervals between two swallows measured from the pharyngeal
recording site on the manometric tracing were 3.2 ± 0.2, 6.2 ± 0.3, and 9.3 ± 0.3 s for short-, intermediate-, and
long-interval pairs, respectively. The interval between the first and
second swallows during swallowing at maximal rate was 1.4 ± 0.1 s, and the number of swallows was 12 ± 2.
Interactions between swallows.
Normally propagated peristalsis was observed in all subjects during the
single swallow. In synchrony with the propagated contraction, the two
esophageal segments exhibited an immediate initial lengthening (6-9% of baseline length) and subsequent shortening. The segments began to shorten 1-2 s before the arrival of the contractile wave within each segment. Maximal shortening ranged from 15 to 25%. After
segment shortening, they regained their initial length before the
termination of the propagated contraction within that segment.
With paired swallows, complex interactions were observed between the
swallows. Figures 2 and
3 illustrate examples of manometric tracing and esophageal segment shortening from two of the subjects selected because of the clarity with which one exhibited deglutitive inhibition (Fig. 2) and the other exhibited muscle refractoriness (Fig.
3). Note that in both cases during the multiple swallow sequence, only
the final swallow was associated with a propagated contractile sequence
and an accompanying sequence of esophageal shortening. In Fig. 2, four
paired swallows with different intervals are illustrated. When the
interval between two swallows was very short (1.9 s), the first swallow
was totally inhibited and the second was completely propagated, similar
to a single swallow as evident by the manometrically recorded
contraction and the sequenced esophageal shortening of both segments.
When the interval between swallows was long (8.9 s), each resulted in a
completely propagated manometrically recorded contraction and sequenced
shortening, although the peristaltic amplitude was slightly lower than
that of a single swallow. With paired swallows with intermediate
intervals (4.3 and 4.6 s), the first contractile sequence was
partially inhibited, evidenced by lower contraction amplitude and early termination of the manometrically recorded contraction in the distal
segment. Analogous to this, only the proximal, not distal, segment
exhibited slight shortening. On the other hand, the second swallow of
the pairs appeared relatively normal, both manometrically and in terms
of sequenced shortening.
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Fig. 2.
Manometric tracing and segmental esophageal shortening during a
single swallow, 4 paired swallows with different intervals, and a
series (11) of swallows in 10 s in a representative
subject demonstrating deglutitive inhibition of both the manometric
contraction and segment shortening. In each swallow or swallow
sequence, the top shows the manometric tracing,
including swallow (SW) marker, and representative manometric
recording sites 3, 6, and 15 cm proximal to the lower esophageal
sphincter (LES). Latencies between the swallow and the onset of
contraction at each site are L1, L2, and L3, equal to 4.2, 7.4, and
9.5 s in this instance. Other manometric channels are omitted for
simplification. The bottom illustrates the change in length
of the proximal ( ) and distal ( )
segments. A length >100% indicated that the segment lengthened, and a
percentage <100% indicates shortening. See text for further
explanation.
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Fig. 3.
Another example of manometric tracings and segmental shortening, in
this case illustrating muscle refractoriness. Details of the figure are
the same as in Fig. 2. See text for further explanation.
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Figure 3 illustrates a series of single, paired, and multiple swallows
in another subject who best exhibited muscle refractoriness. The
manometric and shortening activity associated with the single swallow,
short-interval swallow, long-interval swallow, and multiple swallows is
similar to those illustrated in Fig. 2. However, the intermediate
interval swallows exhibited a distinct pattern. In the paired swallows
separated by 4.8 s, the first swallow was relatively intact,
whereas the second swallow was almost completely inhibited with only a
low-amplitude simultaneous contraction evident in the two distal
channels, and no significant esophageal shortening was observed.
Similarly, in the paired swallows with an interval of 7.5 s, the
first peristaltic sequence was relatively intact and, although the
second was associated with a propagated contraction, this was of low
amplitude. Similarly, the degree of shortening was minimal. Thus,
rather than the second swallow attenuating the contractile activity of
the first, as illustrated in Fig. 2 (deglutitive inhibition), the first
attenuated the second (muscle refractoriness). Of the eight subjects
studied, five exhibited only deglutitive inhibition and three showed
some degree of muscle refractoriness. Of the three, the example
illustrated in Fig. 3 was by far the most illustrative.
Duration of deglutitive inhibition.
Figure 4 summarizes the contraction
amplitudes and the associated percentages of shortening observed during
all single swallows; paired swallows of short, intermediate, and long
intervals; and rapidly sequenced swallows for all subjects. The
contraction amplitude and the extent of shortening observed for a
single swallow, the second swallow of a pair, or the last of a series
of multiple swallows was very similar within both esophageal segments.
However, both peristaltic amplitude and the extent of segmental
shortening were strongly influenced by the duration of the time
interval between the paired swallows. With short intervals, there was
nearly complete inhibition of the first peristaltic contraction both in
terms of peristaltic amplitude and segmental shortening. Conversely, with long-interval swallows, there was no significant inhibition of
peristaltic amplitude or segmental shortening within either esophageal
segment. However, for paired swallows separated by intermediate time
intervals, both segments exhibited significantly lower amplitude and a
reduced extent of shortening (limited to the distal segment). Note that
because deglutitive inhibition was by far the dominant pattern of
interaction observed, the influence of muscle refractoriness is not
evident in Fig. 4.
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Fig. 4.
The amplitude of esophageal contractions (A)
and the degree of esophageal shortening (B) during single
swallows; paired swallows separated by short (<4 s), intermediate
(4-8 s), or long intervals (>8 s); and a series of repetitive
swallows. Peristaltic amplitude is expressed as the peristaltic index:
the fractional value of the observed swallow divided by the mean value
for single swallows. Note that both peristaltic amplitude and segment
shortening are completely inhibited with multiple swallows, very
substantially inhibited with short-interval pairs, usually inhibited
with intermediate interval pairs and unaffected by long-interval pairs.
There is no significant effect on the second swallow in terms of
peristaltic amplitude or segment shortening.  P < 0.05, *P < 0.001 vs. single swallow.
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In Figs. 2 and 3, the intervals between the onset of the
pharyngeal swallow and the onset of the manometric contraction are labeled L1, L2, and L3 for the channels 15, 6, and 3 cm proximal to the
SCJ, respectively. These latencies approximate the period of inhibition
before the onset of the manometric contraction at each esophageal
locus. Thus, if deglutitive inhibition is simply a consequence of the
normal period of inhibition associated with peristalsis, it should be
evident at each esophageal location (SCJ + 15, SCJ + 6, and
SCJ + 3 cm) for a period closely related to L1, L2, and L3 after
the first swallow, respectively. Figure 5
tests this hypothesis for the manometrically recorded contractions 15 and 6 cm proximal to the SCJ. In the Fig. 5A,
time 0 for each pair of swallows is equal to L1 for the
subject in question, and the contractile index is equal to the
peristaltic amplitude of the first swallow divided by that of the
single swallow for that subject. Thus, if there were no change in
amplitude, the contractile index would be 1, and if there was complete
inhibition of the first swallow, it was 0. Quite clearly, at 15 cm
proximal to the SCJ, there was complete inhibition of the first swallow
until time 
1.0 (s) and partial inhibition until time
0, after which no consistent effect was observed. Figure
5B illustrates the analogous analysis for the recording site
6 cm proximal to the SCJ; in this case, time 0 was equal to
L2 for each subject. Note that there is complete inhibition until 3.0
s, partial inhibition until 0.0 s, and no consistent inhibition of
the first swallow after 0.0 s.
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Fig. 5.
The effect of the separation interval between 2 swallows
on peristaltic amplitude at 2 esophageal sites: 15 cm above the sleeve
center (A; striated muscle esophagus) and 6 cm above the
sleeve center (B; smooth muscle esophagus). The latency
between the contraction in the pharyngeal channel and that at 15 and 6 cm above the LES (L1 and L2 in Figs. 2 and 3) was used as time
0 in A and B, respectively. The observed
time interval between swallows was then referenced to these values;
e.g., if the observed interval was 4 s and L1 was 5 s, the
data point coordinate was 1.0 s. All values within a 1-s interval
were then grouped, and each circle represents the mean ± SE for
all swallow pairs within that 1-s range of separation intervals. Note
that the period of complete inhibition extends up to time 1.0 s in
A and 3.0 s in the distal channel, whereas partial
inhibition is evident until time 0 at both loci.
*P < 0.05 vs. single-swallow amplitude.
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Figure 6 illustrates an analysis of the
persistence of deglutitive inhibition of segment shortening that is
analogous to that of inhibition of the manometric contraction
illustrated in Fig. 5. Figure 5A pertains to the proximal
segment, and Fig. 5B pertains to the distal segment.
Time 0 is equal to L2 in A and L3 in B for each subject. For both segments, significant inhibition is evident
until 2.0 s and partial (although not statistically significant) inhibition is evident until 1.0 s. Thereafter, no consistent effect
is seen in either segment.
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Fig. 6.
The effect of the separation interval between paired
swallows on segment shortening during the first swallow for the
proximal (A) and distal (B) esophageal segments.
The time axis and data grouping were computed as in Fig. 5 with the
caveat that L2 and L3 were used as 0 reference for A
and B, respectively. Note that the period of complete
inhibition extends up to time 3.0 s in A and 4.0 s in
B, whereas partial inhibition is evident until time 1.0 s
in A and 2.0 s B. Comparing these data to Fig.
4 suggests that inhibition of the longitudinal muscle precedes that of
the circular muscle by 1-2 s in the distal esophagus.
*P < 0.05 vs. single-swallow amplitude.
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Correlation between manometric amplitude and the extent of segment
shortening.
A case-by-case correlation of the contraction index with the shortening
index for the first swallow of every pair is illustrated in Fig.
7. In every instance, the occurrence of a
manometric contraction was accompanied by some degree of segment
shortening. Quantitatively, a highly significant correlation was found
between the contraction index and the percentage of shortening during
the first of the paired swallows (r = 0.6, P 
0.001 for the proximal segment, r = 0.66, P 0.001 for the distal segment).
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Fig. 7.
Correlation between peristaltic amplitude and segment
shortening for the proximal (A) and distal esophageal
segments (B). Each data point depicts the %shortening and
corresponding amplitude index for the first swallow of 1 pair in 1 subject. Highly significant correlation was observed in both esophageal
segments.
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DISCUSSION |
The major aims of this study were to determine whether or not
deglutitive inhibition affected the longitudinal muscle of the esophageal muscularis propria in a similar manner to the circular muscle and, if so, to determine how the two correlated. Experiments were done using concurrent manometry and fluoroscopy after having demarcated two distal esophageal segments by placement of mucosal clips
and situating side-hole recording sites within each segment. The major
findings of the investigation were that longitudinal muscle does
exhibit deglutitive inhibition, that the degree of attenuation of
segment shortening observed strongly correlated with the degree of
attenuation of peristaltic amplitude, and that the period of inhibition
of segment shortening was 1-2 s less than the inhibition of
contractile amplitude within that segment.
The manometric contractions associated with two closely spaced swallows
observed in the current study closely parallel the earlier description
of Vanek and Diamant (14): with short interswallow intervals (<4 s) or a rapid sequence of swallows, only the final swallow was associated with a propagated contraction; with interswallow intervals >8 s, there were two normal-appearing propagated
contractions; with interswallow intervals between 4 and 8 s, there
was either significant or complete inhibition of the first propagated
contraction. We also observed that in every case, complete inhibition
of the manometric contraction was matched by inhibition of shortening in the corresponding segment, and in cases of partial inhibition, the
degree of inhibition evident manometrically was closely correlated with
the degree to which segment shortening was attenuated. These observations suggest that the property of deglutitive inhibition affects both the longitudinal and circular muscle contractile patterns
that are integral to esophageal peristalsis and that if one component
is subject to partial or complete deglutitive inhibition, the other is
similarly affected.
An elegant investigation by Sifrim et al. (11) used an
artificial high-pressure zone in the distal esophagus to demonstrate that normal peristalsis was comprised of a wave of inhibition followed
by a sequenced contraction. That investigation uniquely focused on
manometric recordings, presumably indicative of circular muscle
contractility. In the current study, we tested the hypothesis that
deglutitive inhibition is another manifestation of the initial wave of
inhibition that precedes the sequenced esophageal contraction. We
reasoned that if this were the case, the latency between swallowing and
manometrically recorded contraction at a given esophageal locus would
closely parallel the period of deglutitive inhibition operational at
that locus. As evident by the analysis illustrated in Fig. 5, this
relationship is highly significant; deglutitive inhibition persisted in
both the proximal and distal esophagus for time periods equal to the
respective latencies observed during normal peristalsis. We then tested
the hypothesis that deglutitive inhibition of segment shortening,
indicative of longitudinal muscle activity, should exhibit similar
temporal characteristics. Figure 6 illustrates the findings from that
analysis. Note that although there is a clear relationship between the
degree of inhibition of shortening and the time reference, inhibition
does not persist to time 0 as was the case with the
manometric (circular muscle) contraction. In the case of shortening,
deglutitive inhibition ends 1-2 s before the time references that
were equal to the respective latencies of circular muscle contraction
observed during peristalsis. In fact, owing to an inherent
methodological limitation of our study, we probably somewhat
underestimated the magnitude of the delay between the end of
longitudinal and circular muscle inhibition. The methodological
limitation in question is that segmental shortening was measured along
a 3-cm segment of esophagus, whereas circular muscle contraction was
measured at the proximal margin of that segment. Thus, if circular and
longitudinal muscle contractions were simultaneous, the inherent error
in our measurement would make it appear that the circular muscle
contraction preceded the longitudinal muscle contraction, which is the
opposite of what was observed. Intraluminal high-frequency
ultrasound would overcome this limitation because it can quantify
muscle thickness and hence contraction of both layers of esophageal
muscle at a given location (7, 15). However, our
observation is consistent with earlier observations relating to the
relative timing of contraction of the longitudinal and circular muscle
during peristalsis. Analysis using methods similar to the current
investigation (4, 8, 9), external markers placed directly
on the muscularis propria (2), or intraluminal
high-frequency ultrasound (7) have all concluded that the
onset of longitudinal muscle contraction precedes that of circular
muscle contraction.
Swallow-evoked peristaltic sequences are mediated via vagal efferent
nerves. Neurophysiological studies in animals support the hypothesis
that peristalsis is comprised of active inhibition followed by a
sequenced esophageal contraction and that both esophageal inhibition
and contraction are centrally mediated (14). Vagal efferent fiber recordings have demonstrated populations of short- and
long-latency neurons whose activity temporally corresponds with
inhibition and contraction, respectively. Furthermore, the long-latency
neurons to the striated and smooth muscles are sequentially activated.
Peripheral mechanisms can also mediate sequential esophageal contractions as evidenced by the persistence of secondary peristalsis after thoracic vagotomy (5). No direct neurophysiological
data exist regarding the mechanism of deglutitive inhibition of
esophageal longitudinal muscle. However, on the basis of the
similarities of deglutitive inhibition of the propagated contraction
and segment shortening observed in the current investigation, we
suspect that the mechanisms are similar, and both likely involve
centrally mediated vagal inhibition. Furthermore, centrally mediated
vagal inhibition may be the only mechanism operational for longitudinal muscle, because the peripheral mechanism of sequential contraction was
not demonstrated in longitudinal muscle (13).
In conclusion, esophageal shortening is affected by deglutitive
inhibition in a similar manner to manometrically recorded esophageal
contractions. The presence and degree of inhibition evident in
peristaltic amplitude closely correlates with those observed in
segmental shortening, indicative of longitudinal muscle activity. The
deglutitive inhibition evident in both muscle layers is likely
attributable to the same vagally mediated inhibition that is an
integral component of normal peristalsis, with the caveat that just as
the onset of longitudinal muscle contraction precedes circular muscle
contraction, the period of deglutitive inhibition of the longitudinal
muscle is 1-2 s shorter than that of circular muscle.
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ACKNOWLEDGEMENTS |
This work was supported by National Institute of Diabetes and
Digestive and Kidney Diseases Grant RO1-DK-56033 (to P. J. Kahrilas and R. J. Joehl).
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FOOTNOTES |
Address for reprint requests and other correspondence:
P. J. Kahrilas, Northwestern Univ., Feinberg School of
Medicine, Dept. of Medicine, Div. of Gastroenterology and Hepatology,
676 St. Claire St., Suite 1400, Chicago, IL 60611 (E-mail:
p-kahrilas{at}northwestern.edu).
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. Section 1734 solely to indicate this fact.
10.1152/ajpgi.00311.2002
Received 29 July 2002; accepted in final form 2 December 2002.
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REFERENCES |
1.
Ask, P,
and
Tibbling L.
Effect of time interval between swallows on esophageal peristalsis.
Am J Physiol Gastrointest Liver Physiol
238:
G485-G490,
1980[Abstract/Free Full Text].
2.
Dodds, WJ,
Stewart ET,
Hodges D,
and
Zboralske FF.
Movement of the feline esophagus associated with respiration and peristalsis. An evaluation using tantalum markers.
J Clin Invest
52:
1-13,
1973[ISI][Medline].
3.
Edmundowicz, SA,
and
Clouse RE.
Shortening of the esophagus in response to swallowing.
Am J Physiol Gastrointest Liver Physiol
260:
G512-G516,
1991[Abstract/Free Full Text].
4.
Kahrilas, PJ,
Wu S,
Lin S,
and
Pouderoux P.
Attenuation of esophageal shortening during peristalsis with hiatus hernia.
Gastroenterology
109:
1818-1825,
1995[ISI][Medline].
5.
Kravitz, JJ,
Sanpe WJ, Jr,
and
Cohen S.
Effect of thoracic vagotomy and vagal stimulation on esophageal function.
Am J Physiol Endocrinol Metab Gastrointest Physiol
234:
E359-E364,
1978[Abstract].
6.
Meyer, GW,
Gerhardt DC,
and
Castell DO.
Human esophageal response to rapid swallowing: muscle refractory period or neural inhibition?
Am J Physiol Gastrointest Liver Physiol
241:
G129-G136,
1981[Abstract/Free Full Text].
7.
Nicosia, MA,
Brasseur JG,
Liu JB,
and
Miller LS.
Local longitudinal muscle shortening of the human esophagus from high-frequency ultrasonography.
Am J Physiol Gastrointest Liver Physiol
281:
G1022-G1033,
2001[Abstract/Free Full Text].
8.
Pouderoux, P,
Lin S,
and
Kahrilas PJ.
Timing, propagation, coordination, and effect of esophageal shortening during peristalsis.
Gastroenterology
112:
1147-1154,
1997[ISI][Medline].
9.
Shi, G,
Pandolfino JE,
Joehl RJ,
Brasseur JG,
and
Kahrilas PJ.
Distinct patterns of esophageal shortening during primary peristalsis, secondary peristalsis and transient lower esophageal sphincter relaxation.
Neurogastr Motil.
14:
505-512,
2002.
10.
Sifrim, D,
and
Janssens J.
Secondary peristaltic contractions, like primary peristalsis, are preceded by inhibition in the human esophageal body.
Digestion
57:
73-78,
1996[Medline].
11.
Sifrim, D,
Janssens J,
and
Vantrappen G.
A wave of inhibition precedes primary peristaltic contractions in the human esophagus.
Gastroenterology
103:
876-82,
1992[ISI][Medline].
12.
Sifrim, D,
Janssens J,
and
Vantrappen G.
Failing deglutitive inhibition in primary esophageal motility disorders.
Gastroenterology
106:
875-882,
1994[ISI][Medline].
13.
Sugarbaker, DJ,
Rattan S,
and
Goyal RK.
Swallowing induces sequential activation of esophageal longitudinal smooth muscle.
Am J Physiol Gastrointest Liver Physiol
247:
G515-G519,
1984[Abstract/Free Full Text].
14.
Vanek, AW,
and
Diamant NE.
Responses of the human esophagus to paired swallows.
Gastroenterology
92:
643-650,
1987[ISI][Medline].
15.
Yamamoto, Y,
Liu J,
Smith TK,
and
Mittal RK.
Distension-related responses in circular and longitudinal muscle of the human esophagus: an ultrasonographic study.
Am J Physiol Gastrointest Liver Physiol
275:
G805-G811,
1998[Abstract/Free Full Text].
Am J Physiol Gastrointest Liver Physiol 284(4):G575-G582
0193-1857/03 $5.00
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