Local longitudinal muscle shortening of the human esophagus
from high-frequency ultrasonography
Mark A.
Nicosia1,
James
G.
Brasseur1,
Ji-Bin
Liu2, and
Larry S.
Miller3
1 Department of Mechanical Engineering, Pennsylvania State
University, University Park 16802; 2 Department of Radiology,
Thomas Jefferson University Hospital, and 3 Division of
Gastroenterology, Temple University Hospital, Philadelphia,
Pennsylvania 19140
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ABSTRACT |
We analyzed local
longitudinal shortening by combining concurrent ultrasonography and
manometry with basic principles of mechanics. We applied the law of
mass conservation to quantify local axial shortening of the esophageal
wall from ultrasonically measured cross-sectional area concurrently
with measured intraluminal pressure, from which correlations between
local contraction of longitudinal and circular muscle are inferred. Two
clear phases of local longitudinal shortening were observed during
bolus transport. During luminal filling by bolus fluid, the muscle
layer distends and the muscle thickness decreases in the absence of
circular or longitudinal muscle contraction. This is followed by local
contraction, first in longitudinal muscle, then in circular muscle.
Maximal longitudinal shortening occurs nearly coincidently with peak
intraluminal pressure. Longitudinal muscle contraction begins before
and ends after circular muscle contraction. Larger longitudinal
shortening is correlated with higher pressure amplitude, suggesting
that circumferential contractile forces are enhanced by longitudinal
muscle shortening. We conclude that a peristaltic wave of longitudinal
muscle contraction envelops the wave of circular muscle contraction as
it passes through the middle esophagus, with peak longitudinal
contraction aligned with peak circular muscular contraction. Our
results suggest that the coordination of the two waves may be a
physiological response to the mechanical influence of longitudinal
shortening, which increases contractile force while reducing average
muscle fiber tension by increasing circular muscle fiber density
locally near the bolus tail.
muscle contraction; ultrasound; mechanics
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INTRODUCTION |
WHEREAS CONTRACTION OF
ESOPHAGEAL circular muscle during a swallow can be quantified
with manometric measurement of intraluminal pressure, contraction of
longitudinal muscle is difficult to measure precisely in humans.
Consequently, the role of longitudinal muscle in bolus transport
remains poorly understood. In a classic study by Dodds et al.
(5), four metal markers were inserted into the muscle wall
of a feline esophagus to measure longitudinal motions during normal
bolus transport. Their data suggested the existence of a wave of
localized longitudinal shortening that appeared to traverse the distal
esophagus in concert with the bolus tail. Qualitatively similar
characteristics have been observed in the human esophagus with widely
spaced metal clips endoscopically attached to the mucosa (6,
16). In this study, we analyze the relationship between circular
and longitudinal muscle contraction near the bolus tail by directly
measuring local shortening of the esophagus concurrently with
intraluminal pressure during normal bolus transport. This is done by
coupling concurrent endoscopic ultrasonography and intraluminal
manometry with a basic conservation law from mechanics.
A consequence of contraction of longitudinal muscle is shortening in
the axial direction. For this reason, longitudinal muscle contraction
of the human esophagus has been inferred from longitudinal shortening
measured by using widely spaced metal clips attached to the esophageal
mucosa (6, 9, 13, 16). The change in spacing between
adjacent clips gives a relatively crude measure of longitudinal
shortening over esophageal segments 3-10 cm in length. A
characteristic of these studies, however, is that the motion of widely
spaced mucosal clips measures global rather than local shortening. To
illustrate this point, imagine a segment of the esophagus of initial
length L* = 1 cm shortening to length L = 0.5 cm
in the absence of any other shortening of the esophagus. Local
longitudinal shortening is given by L/L* = 0.5. However, if
the same isolated local contraction were measured by using clips spaced
3 cm apart, for example, global longitudinal shortening would be
calculated as L/L* = (3
0.5)/3 = 0.83. Similarly, 5-cm spaced clips measure L/L* = 0.9. Thus
mucosal clips spaced outside a localized contracting segment
underestimate longitudinal shortening (larger L/L*
implies less shortening), and the estimate varies with clip spacing.
Furthermore, the relative motion between a clip on the mucosal surface
and the underlying muscle layer (from shear distortion of the mucosa)
introduces additional unknown error in the estimate of local
longitudinal shortening.
To avoid the uncertainty associated with mucosal clips, we developed a
new procedure for accurately measuring local longitudinal shortening of
the esophageal wall using a high-frequency ultrasound transducer at
fixed locations within the lumen. As discussed in METHODS,
application of the law of mass conservation (a fundamental law of
physics) to the incompressible matter within esophageal muscle implies
that a local increase in cross-sectional area of the muscle wall is
inversely proportional to longitudinal shortening of the muscle layer
locally at the same cross-section. Thus measurement of cross-sectional
area of the muscle layer(s) can be related quantitatively to local
shortening (or lengthening) of the same muscle layer(s). Furthermore,
we shall show that measuring only changes in esophageal muscle wall
thickness (1, 14, 24), as during luminal filling, for
example, is generally insufficient to deduce local longitudinal shortening.
In this study, cross-sectional area was measured during bolus transport
at a point in the middle esophagus from ultrasound images generated
from a high-frequency transducer. Placement of the ultrasound probe
within an endoscope adjacent to a single manometric sidehole allowed
concurrent measurement of intraluminal pressure with local longitudinal
shortening at the same luminal location. From these data we infer a
correlation between longitudinal and circular muscle contraction from
concurrent measurement of muscle cross-sectional area and intraluminal pressure.
 |
METHODS |
The principle of mass conservation applied to muscle.
Mass conservation is a basic law of physics that underlies the
deformation of all matter. In context with muscle, the law can be
understood by imagining a volume within the muscle where each material
particle along the surface of the volume is tagged by a marker (a
material particle may be thought of as extremely large numbers of
molecules within a submicroscopic volume much smaller than any volume
of interest). As the muscle deforms, so does the surface defined by
these same mass particles. Mass conservation states that at all times,
before, during, and after its change in shape, the mass within the
volume defined by the same tagged material particles cannot change
(23).
Whereas the mass within the material volume cannot change, the density
of the material (mass divided by volume) can change if the size of the
material volume changes during deformation. This is the case, for
example, when air within a closed cylinder is compressed by a piston.
Indeed, a fundamental characteristic of a gas is that when pressure is
applied to the enclosing surface of a material gas volume, the relative
change in volume is as large as the relative change in pressure. By
contrast, when pressure is applied to liquids or solids, the
change in volume is negligible. Liquids and solids are described as
"incompressible," meaning that the density of the substance and
material volumes do not change with changes in pressure (to a high
degree of accuracy).
At the microscopic level, muscle is a matrix of liquid (e.g.,
intracellular and interstitial water) and deformable solid (e.g., cellular material). Therefore, muscle is incompressible, and a predefined macroscopic segment of the esophageal wall can only change
its volume during deformation if either vapor pockets of significant
size exist within the muscle or significant liquid content were to
leave the muscle volume during contraction and be taken up again after
contraction. There is no evidence to suggest that either of these
scenarios is relevant during esophageal muscle contraction, and the
incompressibility of muscle (including esophageal muscle) has been
verified experimentally by several investigators (7, 8,
22). Furthermore, any fluid that might be speculated to leave
the muscle layer during contraction will lead to an underestimate of
muscle cross-section and, as we show next, local longitudinal shortening. Thus any observations made from measurements of local longitudinal shortening can be enhanced only if fluid exchange existed.
Measuring local longitudinal shortening.
Incompressibility is tacitly assumed in muscle clip studies when global
longitudinal muscle contraction is inferred from relative displacement
of two clips. Here we explicitly apply the principle to quantify local
shortening from measurement of change in cross-sectional area from
ultrasound images.
Consider the schematic in Fig. 1, a short
material segment of esophageal wall muscle at two instants in time, in
the resting state and after longitudinal contraction. Because this
axial muscle segment contains the same incompressible material
components within and between cells before and after contraction (i.e.,
the surfaces of the segment are always attached to the same material
particles), the volume of this muscle segment must also be the same
before and after contraction. It follows that a contraction of the
muscle segment in the longitudinal direction must be accompanied by an increase in cross-sectional area according to the equation
LA=L*A*, where L*A* and LA are the
volumes of the muscle segments before and after contraction. Thus
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(1)
|
where the precontractile (resting) state is denoted by *. This
formula states that a local increase in muscle cross-sectional area
(A/A* > 1) is inversely proportional to local longitudinal shortening (L/L* < 1) at the same axial location along the
esophagus.

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Fig. 1.
Schematic showing the relationship between longitudinal
shortening and changes in the cross-sectional area of esophageal
muscle. The dotted line is the outer wall of an esophageal muscle
layer; a cross-sectional material surface of the muscle layer is
illustrated by the cross-hatched surface. A local longitudinal slice of
esophageal muscle has shortened from length L* to length
L as a result of local longitudinal contraction. For
convenience, only one muscle layer is shown. To conserve volume, the
longitudinal contraction must be accompanied by an increase in
cross-sectional area according to the relationship L/L*
=A*/A, where A* and A are the
cross-sectional areas in the resting and contracted states,
respectively.
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Using Eq. 1, we can measure A/A* from ultrasound
images to unambiguously infer L/L*. In doing so, we
recognize that, because the muscle surface moves 1-2 cm relative
to the transducer during local longitudinal shortening, the material
elements within area A in Eq. 1 measured at one
time likely originated a short distance above or below the ultrasound
transducer. However, the potential error in the measurement of
A/A* associated with axial wall motion is very small, given
quantitatively by the percent variation in A* over a
1-2 cm segment of middle esophagus.
Note that the method can, in principal, be applied to any layer or
groups of layers of the esophageal wall. Whereas we primarily analyze
the two muscle layers as a unit (longitudinal/circular muscle layers
plus intermuscular connective tissue), we also present a separate
analysis of the longitudinal muscle layer alone.
Concurrent ultrasonography with manometry.
Concurrent ultrasound and water-perfused manometry data from Miller et
al. (14) were analyzed from four healthy subjects with no
swallowing disorders (ages 23-25 years), lying supine (at 30°
inclination) and for 24 swallows. The subjects were asked to swallow
10-ml boluses of water or gelatin mix. The gelatin bolus was designed
to reduce the level of air bubbles within the bolus, which disrupt the
ultrasound waves and render many images unsuitable for analysis. The
resulting liquid was roughly the thickness of honey at room temperature.
Images were digitized from VHS videotape at 5 frames/s, corresponding
to 50-60 images/swallow. Because of the time-consuming nature of
the image analysis (see Image processing) and the
inability to fully analyze some swallows due to significant image loss
from air swallowed with the bolus (which is quite common and interferes with ultrasound), time-resolved image analysis and curve fitting for
complete swallows were feasible in eight swallows from two subjects
from which the changes in muscle cross-sectional area and local
longitudinal shortening were deduced during entire bolus transport
sequences. The time-resolved data analyzed in detail were chosen by the
quality of the ultrasound images and the extent of air-induced image
degradation. However, 16 additional swallows were analyzed over fewer
images to determine the resting state geometry, maximum local
longitudinal shortening (i.e., maximum cross-sectional area ratio
Amus/A*mus), and maximum
intraluminal pressure (Pamp). The details of swallows from each subject are shown in Table
1. Further data collection details are
given in Ref. 14.
The esophageal wall was imaged using a 20-MHz ultrasonographic
transducer housed in a 4.8-Fr catheter (1.52 mm outer diameter) with an axial resolution of 0.1 mm and a penetration depth of 2.0 cm.
The 4.8-F catheter was glued to a 3-F manometric catheter (0.95 mm
outer diameter), and the combined assembly was passed transnasally
through a 16-F nasogastric tube (5.09 mm outer diameter) with the
manometric sidehole and ultrasound transducer extending ~2 cm from
the proximal margin of the tube. The ultrasonic transducer and
manometric sidehole were placed at the same axial location, ~10 cm
proximal to the lower esophageal sphincter. The baseline of
manometrically measured intraluminal pressure (P) was
approximately atmospheric.
Image processing.
Figure 2, a, b, and c, shows
typical ultrasound images of the esophageal cross-section obtained at
three different times during a swallow: the relaxed state
(a; i.e., before a swallow), the esophagus distended by the
bolus (b), and the maximally contracted state
(c). The inner wall of the circular muscle and the outer wall of the longitudinal muscle are shown by dashed lines on the same
images in Fig. 2, a', b', and c',
respectively. The white annulus in the middle of each image is the
catheter, inside of which the ultrasound transducer is housed. Because
the transducer spins to obtain the image, the concentric circular bands
that appear in the image are artifacts and do not correspond to any anatomic structure.

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Fig. 2.
Typical ultrasound images obtained at 3 different times during a
swallow: resting state (a), esophagus distended by the bolus
(b), and maximally contracted state (c). In
a', b', and c', the inner wall of the
circular muscle and the outer wall of the longitudinal muscle are
outlined on the same images as per the method described in Image
processing.
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To compute the cross-sectional area of the circular and longitudinal
muscle layers, it was necessary to extract three contours from each
image: the inner wall of the circular muscle, the intermuscular connective tissue (between circular and longitudinal muscle layers), and the outer wall of the longitudinal muscle. To this end, we developed an in-house interactive image processing system using a
Silicon Graphics Indigo 4000 workstation (Silicon Graphics, Mountain
View, CA). Digitized images were converted to grayscale and imported
into our analysis system.
The quality of ultrasound images is degraded by high (spatial)
frequency noise known as "speckle" (12), which results
from interference among signals scattered from sources smaller than the
resolution of the imaging system. To smooth this noise we applied an
Olympic filter (18): a moving window of M × M pixels was placed at each pixel of the image, and the
average grayscale intensity of the pixels within the window was
computed, ignoring the highest and lowest grayscale values. The pixel
at the center of the window was then replaced with this average value
and the other pixels within the window were left unchanged. We found
the Olympic filter with M = 5 to be most effective at
reducing speckle noise and enhancing contrast at esophageal muscle boundaries.
Having filtered the images, we designed software to extract the edges
of the circular and longitudinal muscle layers using a
"knowledge-based" edge detection method (19), whereby
knowledge of the image structure was used in the edge detection
algorithm. We applied the knowledge obtained in the study of Miller et
al. (15), which related ultrasonically imaged esophageal
cross-section to histologically defined muscle layers. (M. A. Nicosia was extensively trained by L. S. Miller, an experienced
sonographer, in identifying muscle layer boundaries in these ultrasound
images.)
To detect the muscle layers in as automated a way as possible, the
catheter was used as a point of reference, because it was at the same
location in every image and always located within the esophageal
contours. The computer program first searched for the outer wall of the
longitudinal muscle. Because the adventitia appears white and muscle
appears black, there is an abrupt change in grayscale intensity moving
from the longitudinal muscle to the adventitia (see Fig.
2), which the computer was often able to
find automatically. Once the outer wall was detected, the program moved inward (toward the catheter) to search for the inner margin of
the circular muscle, which appears as a transition from the darker
muscle layer to the lighter submucosa. The intermuscular connective
tissue appears as a slight increase in grayscale intensity within the
dark band of the muscle layers and is difficult to extract automatically.
After allowing the computer to identify edges automatically, the edges
were superimposed on the raw image and presented to the user, who added
and/or deleted points as appropriate to correct and complete the
computer-detected edges. The user always made the final decision about
the location of the muscle boundary. The purpose of the initial
automatic detection phase was to speed up the very time-consuming edge
detection process. In portions of the image in which the muscle edge
was not clearly visible, the edge was interpolated by passing a smooth
curve from adjoining regions where the edge could be clearly
identified. In most images, however, interpolation was only required
over a small percentage of the edge (<10%). Images of the maximally
distended esophagus were the most difficult to analyze, since the
esophageal walls were farthest away from the transducer and the signal
was correspondingly weaker. In these images it was generally necessary
to interpolate ~35% of the edge. To aid in the interpolations,
however, the location of the edge in previous and following images was
used to guide the choice of interpolation control points.
From the detected edges, the cross-sectional areas of the circular
muscle (Acirc), longitudinal muscle
(Along), and lumen (Alumen) were determined, as illustrated in Fig.
3. The total muscle area was given by
Amus = Acirc + Along.

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Fig. 3.
A schematic describing the effective radii of the muscle
layers. The three cross-sectional areas of the lumen
(Alumen), circular muscle
(Acirc), and longitudinal muscle
(Along), measured from the ultrasound images
(A), were placed concentrically within an effective circle
with the same total area (B). The effective radii to the
inner circular muscle (Rin), intermuscular
connective tissue (Rmid), and outer longitudinal
muscle (Rout) were defined from this effective
circle (see Eq. 2). The total muscle area is
Amus = Acirc + Along.
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Analysis.
Effective radii to the inner circular muscle
(Rin), to the intermuscular
connective tissue (Rmid), and to the outer
longitudinal muscle (Rout) were defined as shown
in Fig. 3, where the measured areas Alumen,
Acirc, and Along were
placed in concentric circles. Thus the effective radii were defined by
|
(2)
|
and the average muscle thicknesses (
) by
|
(3)
|
The resting state (*) was measured before initiation of a
swallow. The time corresponding to the maximum total muscle area in
each sequence
[(Amus/A*mus)max]
was defined as t = 0. The different sequences were aligned
relative to this reference time, and mean values and standard
deviations were computed.
As per Eq. 1, longitudinal shortening (a decrease
in L/L* to values <1) was given equivalently by an increase
in A/A* to values >1, where A* is the muscle
cross-sectional area in the resting state and A can be
Acirc, Along, or
Amus. Equation 1 was applied separately to Amus and
Along, and longitudinal shortening in the muscle
wall was compared with the longitudinal layer alone.
The onsets and offsets of circular and longitudinal muscle contractions
were subjectively defined as the times when manometric pressure and
cross-sectional area initiated a rapid increase in and returned to
their baseline values (see RESULTS). Defining the onset
times as tC,1 and tL,1,
the delay between the onset of circular and longitudinal muscle
contractions is given by
|
(4)
|
The Pearson coefficient was computed to test for correlation.
Significance was analyzed by Student's t-test.
 |
RESULTS |
The wall muscle layer.
The resting state was measured before the initiation of a swallow.
Averaged over eight swallows, the resting state in the middle esophagus
was characterized by wall muscle layer area and thickness
A*mus = 0.40 ± 0.03 cm2 and
*mus = 0.138 ± 0.007 cm; longitudinal muscle area and thickness A*long = 0.218 ± 0.013 cm2 and
*long =
0.069 ± 0.005 cm; radius to circular muscle
R*in = 0.40 ± 0.05 cm; and
intraluminal pressure P* =
0.12 ± 0.80 mmHg
(means ± SD).
Recall from Eq. 1 that local longitudinal
shortening relative to the rest state (L/L*) is given by the
inverse of A/A*, so that the larger is the deviation of
A/A* > 1, the greater is the relative shortening in the
longitudinal direction. Similarly, A/A* < 1 implies
longitudinal lengthening. Figures 4 and
5 give the time variation in longitudinal shortening of the wall muscle layers
(Amus/A*mus and
Along/A*long) and wall
muscle thicknesses (
mus and
long) and intraluminal pressure and inner
muscle radius (Rin) at a fixed point in the middle esophagus averaged over eight swallows and centered on the time
of maximum total muscle cross-sectional area
(Amus/A*mus). These figures
contain a great deal of information that shall be interpreted in terms
of muscle contractile physiology in the DISCUSSION. We
focus first on the characteristics of the total muscle layer (Fig. 4).

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Fig. 4.
Temporal variation in total muscle area
Amus/A*mus and
intraluminal pressure (A), and average radius to circular
muscle and total muscle thickness (B), averaged over 8 swallows. The average resting muscle area,
A*mus, is 0.40 cm2. The bars
indicate SD. The horizontal dotted lines indicate the resting state
values A*mus and P*
(A), and R*in and
*mus (B). The vertical
dotted lines are chosen to match features in the 2 panels.
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Fig. 5.
Temporal variation in total muscle area
Along/A*mus and
intraluminal pressure (A) and average radius to circular
muscle and total muscle thickness (B), averaged over 8 swallows. The average resting muscle area,
A*mus, is 0.218 cm2. The
bars indicate SD. The horizontal dotted lines indicate the resting
state values A*mus and P*
(A), and R*in and
*long (B). The vertical
dotted lines are chosen to match features in the 2 panels.
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A general characteristic that appears when the four curves in Fig. 4
are compared is the existence of two overall phases of muscle activity
during bolus transport through the middle esophagus. Initially, the
esophageal lumen distended, as indicated by the rise in
Rin from its resting state to a peak at about
2 s. During most of this period, until about
3 s, the thickness of
muscle layer decreased in approximate inverse proportion to
Rin, but with
Amus/A*mus hovering close to
1 (the slight increase in
Amus/A*mus during this
period is only marginally significant). Intraluminal pressure rose to a
plateau of 4.4 mmHg during this period, which reflects intrabolus
pressure preceding the arrival of the circular muscle contraction wave
(3). During this distension phase (roughly
7 to
3 s),
the bolus fills the lumen and the muscle layer thickness decreases in
the absence of significant longitudinal shortening or circular muscle
contractile activity.
A local longitudinal shortening phase followed as both the thickness
and cross-sectional area of the muscle increased above their resting
state values, beginning their rise at about the same time (
3 s) and
reaching coincident maxima at t = 0. The increase in
Amus/A*mus > 1 necessarily
implies increasing local longitudinal shortening, with maximum relative
reduction in longitudinal length of L/L* = 0.36 having
occurred ~0.25 s before maximum luminal pressure. The maximum muscle
area was 1.11 ± 0.10 cm2, significantly greater than
the resting area 0.40 ± 0.03 cm2 (P < 0.001).
Whereas average Amus/A*mus > 1 implies local longitudinal shortening, the rapid increase in
intraluminal pressure above the slightly elevated intrabolus pressure
implies circular muscle contraction, luminal narrowing, and subsequent
luminal closure (3). We estimate from Fig. 4A
that this rise in average intrabolus pressure began at about
2.0 s.
The upstroke in local longitudinal shortening, by contrast, was
estimated subjectively from Fig. 4A to begin at
3 s,
roughly 1 s before the upstroke in pressure. Indeed, Fig.
4A shows that a wave of local longitudinal shortening enveloped the wave of circular muscle contraction:
Amus/A*mus began a rapid
increase before the upstroke in intraluminal pressure and returned to
its resting state level well after intraluminal pressure had returned
approximately to its resting state (t > 4.6 s).
In Fig. 4A, the difference in duration between the waves of
circular muscle contraction and local longitudinal shortening waves is
indicated qualitatively by defining subjectively the downstrokes in
pressure and longitudinal shortening as the times when pressure and
Amus/A*mus reached plateaus
after an initially rapid drop. Defined in this way, the duration of the
longitudinal shortening wave was 1.45 times longer than the duration of
the circular muscle contraction wave. A more precise ratio of
durations, defined by the periods at which pressure and
Amus/A*mus are above their
half-maxima, gives the same ratio of durations to within the accuracy
of the data.
The distension phase is heralded by an increase in radius
Rin concurrent with a decrease in muscle
thickness
mus in the absence of significant
change in Amus/A*mus.
Circular muscle contraction is heralded by a sudden rise in
intraluminal pressure coincident with a decrease in
Rin at about
2 s. In contrast, longitudinal
shortening begins with a rapid increase in
Amus/A*mus, which, in Fig.
4, is coincident with an increase in
mus at
t
3 s, reaching its peak at the time of peak
Amus/A*mus (i.e., peak local
longitudinal shortening). Maximum local longitudinal shortening
preceded the peak in intraluminal pressure by only 0.25 s; they
were very nearly coincident. At the times of maximal longitudinal
shortening and intraluminal pressure, the average radius
Rin had reached a plateau of ~0.46 cm, above the resting state value R*in = 0.40 cm.
The plateau in average Rin, which began at peak
longitudinal shortening and circular muscle contraction, remained in
the range 0.44-0.46 cm until longitudinal shortening and
intraluminal pressure had reduced to low levels and reached plateaus at
~3.7 s, after which Rin decreased to its
resting state value together with intraluminal pressure. During this
reduction, however,
Amus/A*mus and
mus remained above their resting state values
(Amus/A*mus
1.1-1.2), suggesting a persistence of lower-level longitudinal shortening beyond the period of circular muscle contraction.
The longitudinal muscle layer.
Figure 5 shows the variation in longitudinal shortening of the isolated
longitudinal muscle layer
(Along/A*mus) together with
intraluminal pressure, inner muscle radius Rin,
and longitudinal muscle thickness
long, with
t = 0 defined at peak total muscle cross-sectional area
(Amus/A*mus). Comparison of
Fig. 5 with Fig. 4 shows that the temporal variations in longitudinal
shortening of the longitudinal muscle layer were the same as
longitudinal shortening of the entire muscle layer, to within the
precision of the data. In particular, a wave of local longitudinal
shortening enveloped the pressure wave, with upstroke, downstroke, and
duration essentially the same as longitudinal shortening of the entire
muscle layer. Note that it is more difficult to identify and measure
accurately the cross-sectional area and thickness of the longitudinal
muscle layer from ultrasound images than to measure the total muscle
layer, so the precisions of Along and
long are less than that of
Amus/A*mus and
mus. The difference between peak
Along/A*mus (Fig.
5A) and peak
Amus/A*mus (Fig.
4A), for example, is not statistically significant
(P = 0.25).
Cross-sectional shape of the lumen.
To illustrate the change in cross-sectional shape of the lumen during
the passage of the bolus and contraction wave, Fig. 6 shows three-dimensional reconstructions
(two space and one time coordinates) of the cross-sectional shape of
the inner wall of the esophagus over time during a representative
swallow. To evaluate the correlation between the change in shape of the
luminal cross-section and the waves of local longitudinal shortening
and circular muscle contraction, we have shaded the surfaces of the
figures so that the gray level is proportional to the magnitude of
Amus (i.e., local longitudinal shortening) in
Fig. 6A and to the magnitude of intraluminal pressure in
Fig. 6B.

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Fig. 6.
Three-dimensional (space-time) reconstructions of the
inner wall of the circular muscle for a representative swallow. The
lateral cross-sectional shape of the lumen (to the circular muscle) is
shown as a function of time at the transducer location, and the large
tickmarks in time imply seconds. The resulting surfaces are shaded so
that the grayscale value is proportional in A to the
magnitude of Amus and in B to the
magnitude of intraluminal pressure for this swallow. Lighter gray color
in A implies greater local longitudinal shortening, whereas
in B lighter tone implies higher intraluminal pressure (and
circular muscle contraction), as shown. Like the average result in Fig.
4, the wave of longitudinal shortening envelops the wave of circular
muscle contraction. The reconstructions also show that the noncircular
lumen cross-section becomes circular at maximal circular muscle
contraction.
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The distension of the lumen during esophageal filling is apparent in
the images by the increase in luminal cross-sectional area during the
first few seconds. During most of this distension phase, neither
longitudinal shortening nor circular muscle contraction had occurred.
The change in cross-sectional shape with time indicates that the
esophageal lumen had a noncircular cross-section in the resting and
distended states, whereas the lumen became circular during the period
of strong circular and longitudinal muscle contraction. These changes
in cross-sectional shape are apparent also in the ultrasound images of
Fig. 2. At the final time shown in the images, the bolus is fully
cleared from the lumen and the luminal cross-section apparently
returned to its resting state geometry. The muscle physiology, however,
had not fully returned to its resting state at the final time, as is
apparent by the lighter shade of Amus indicating
that Amus > A*mus.
Figure 6 shows clearly the envelopment of the wave of circular muscle
contraction (Fig. 6B) by a wave of local longitudinal shortening (Fig. 6A). Also apparent is the axially
nonsymmetric nature of longitudinal shortening: local longitudinal
shortening extended much farther from the time of maximal shortening in
the direction of advancing time than in the reverse time direction. This structure is in contrast with intraluminal pressure, which was
relatively symmetrical in time about peak pressure. Note also that,
whereas the luminal cross-section became circular under the action of
circular muscle squeeze, longitudinal shortening extended in time in
both directions into periods when the cross-section was highly noncircular.
Correlations.
As discussed in METHODS, the process of carefully done
image analysis required for Figs. 4 and 5 was highly time intensive, limiting the full-wave analysis to eight swallows. However, to establish statistically the correlation between levels of circular muscle contraction and local longitudinal shortening, peak
cross-sectional areas were quantified for 24 swallows. Figure
7 shows that larger peak longitudinal
shortening
(Amus/A*mus)max
was correlated with larger maximum intraluminal pressure (i.e.,
pressure amplitude Pamp), on average (r
= 0.61, P < 0.001, N = 24). That is, stronger closure force near the bolus tail tended
to be accompanied by greater local longitudinal shortening in the same
local area. Furthermore, from Fig. 8, a
shorter delay between the onset of circular muscle contraction and
onset of longitudinal shortening (
t) was negatively
correlated with larger Pamp (r =
0.85, P < 0.01, N = 8). Thus the
strength of the luminal closure force was altered both by the magnitude
of longitudinal shortening and by the closeness of temporal
coordination between longitudinal and circular muscle contraction.

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|
Fig. 7.
Correlation between maximum longitudinal shortening
[(Amus/A*mus)max]
and maximum intraluminal pressure (Pamp) for 24 individual swallows (r = 0.61; P < 0.001).
|
|

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Fig. 8.
Correlation between the delay in onset of local
longitudinal shortening and circular muscle contractions
( t) and Pamp for 8 individual
swallows (r = 0.85; P < 0.01).
|
|
 |
DISCUSSION |
Measurement of longitudinal shortening.
In this study, we have quantified shortening of longitudinal muscle
locally in the middle human esophagus during bolus transport. The
method combines explicit measurement of circular, longitudinal, and
total muscle layer cross-sectional geometry with the incompressibility of the muscle layer to unambiguously deduce shortening (or lengthening) in the longitudinal direction within an axially thin segment of the
esophageal wall segment at the location of the transducer. Whereas a
single-point measurement using the method introduced here does not
provide the motion of material points on the esophageal wall, the
approach yields a purely local measurement of longitudinal shortening
without inaccuracies inherent in the use of widely spaced clips placed
on the mucosa.
Incompressibility of muscle layers has been confirmed experimentally
(7, 8, 22), and the accuracy of the method is limited
primarily by the accuracy with which the cross-sectional area of the
muscle layer under consideration can be measured from endoscopic
ultrasound images (or other imaging techniques). The method is
applicable throughout the gastrointestinal tract wherever it is
possible to image the cross-section with sufficient resolution to
quantify muscle cross-sectional area. However, practical application of
the method is limited by the time-intensive nature of interactive edge
detection and analysis of the hundreds of images which underlie the
data, for example, in Figs. 4-8.
The two phases of muscle activity in the middle esophagus.
Whereas one might anticipate that shortening of the esophageal wall
muscle implies a change in muscle layer thickness, Figs. 4 and 5 make
it clear that muscle thickness cannot be used alone as an indicator of
longitudinal shortening. This is because, in the absence of
longitudinal shortening, the muscle layer thickness
mus varies approximately in inverse
proportion to the luminal radius Rin. Thus
mus is sensitive to change in luminal radius, particularly to distension of the esophageal lumen by filling, as is
apparent in Figs. 4 and 5. Relative change in muscle layer cross-sectional area, on the other hand, unambiguously reflects local
relative change in the longitudinal dimension of the muscle layer,
through Eq. 1. We conclude from Figs. 4 and 5, therefore, that the changes in geometry at the middle esophagus in response to
bolus transport occur in two broad parts: 1) a "distension phase," which occurs in the absence of longitudinal shortening or
circular muscle contraction, but during which muscle wall thickness decreases while luminal radius increases as the esophagus is filled, followed by 2) a "contraction phase," whereby
longitudinal shortening and circular muscle contraction act in concert;
local longitudinal shortening increases cross-sectional area and muscle
layer thickness while circular muscle contraction decreases luminal
radius and raises intraluminal pressure.
Whereas active circular muscle contraction began ~1 s after the
initiation of local longitudinal shortening and circular muscle contraction was nearly coincident (within ~0.25 s) with longitudinal shortening, circular muscle tone decreases more rapidly than does longitudinal shortening. We conclude that longitudinal shortening envelops circular muscle contraction as the peristaltic wave moves through the middle esophagus. Defining the durations of the waves of
circular muscle contraction and local longitudinal shortening either
with upstrokes and downstrokes or in terms of half-maxima of the
excursions in Figs. 4 and 5 (see RESULTS), we find that the
duration of local longitudinal shortening in the middle esophagus is
~1.5 times that of circular muscle contraction. However, we also find
that the variation of local longitudinal shortening in time is very
much more asymmetric around its peak than is intraluminal pressure
(especially obvious in Fig. 6). Our results show no significant longitudinal shortening from the initiation of a swallow to ~1 s
before circular muscle contraction. However, as intraluminal pressure
returns toward its resting state value, local longitudinal shortening
and muscle layer thickness, L/L* and
/
*,
reach plateaus 10-15% different from 1, suggesting that the
esophageal wall remains in a state of mild longitudinal shortening for
some period after the passage of waves of circular muscle contraction
and local longitudinal shortening. Whereas the lumen is noncircular in
general, the circular geometry of the lumen during contraction (Fig. 6) suggests relatively uniform circumferential active fiber tension in the
circular muscle layer during peristalsis.
Comparisons with mucosal clip studies.
Dodds et al. (5) measured the axial motion of four
tantalum wires inserted into the in vivo longitudinal muscle over the distal half of the feline esophagus. Although coarser in resolution than the current study, their results suggested the progression of a
wave of longitudinal shortening into the lower esophagus roughly
coincident with the bolus tail. Pouderoux et al. (16) placed three clips at ~4-cm intervals in the distal 8-10 cm of the human esophagus and concluded, consistent with the current study,
that the "contracting longitudinal segment was advancing ahead of the
contracting circular muscle segment." An earlier study with mucosal
clips by Edmundowicz and Clouse (6) measured change in
length of upper and lower halves of the human esophagus and observed
that early in the swallow the lower half lengthened while the upper
half shortened, consistent with the clip motions in the cat esophagus
measured by Dodds et al. (5). Their coarse measurements
are also consistent with the later clip data of Pouderoux et al.
(16), who observed that two adjacent 4-cm segments of the
distal esophagus initially lengthen and later shorten in
peristalsis-like fashion. In the current study, the wave of
longitudinal shortening is preceded by negligible change in esophageal
length locally, indicating that the middle-esophageal ultrasound
transducer was located above the more distal esophageal segments that
initially lengthen and later shorten.
In the introduction, we pointed out that the quantification of
longitudinal shortening using mucosal clips will change with the
distance between the clips; the more widely spaced the clips, the more
underpredicted will be the measurement of longitudinal shortening. Thus
it is not surprising that we measure significantly greater local
shortening than previous clip studies. Figure 4 gives maximal local
longitudinal shortening of the muscle wall layers in the middle
esophagus to be L/L*
0.34 ± 0.02. Kahrilas et al.
(9) and Pouderoux et al. (16) give rough
estimates of minimum L/L* between 0.6 and 0.8 over
esophageal segments 3-5 cm in length, whereas Edmundowicz and
Clouse (6) measure much lower levels of shortening,
maximum L/L*
0.92 and 0.98 over the distal and proximal
halves of the esophagus roughly 10-14 cm in length (remember that
lower values of L/L* imply greater longitudinal shortening).
The lower levels of longitudinal shortening measured in the clip
studies no doubt reflect the global nature of the measurement.
In fact, whereas the cross-sectional area-based method introduced here
arguably yields the most precise measurement of local longitudinal
shortening, clip-based measurements are complementary in that the
relative change in length of the segment between mucosal clips
(ignoring potential error in measured clip position from mucosal
deformation) may be shown to give the average of the local longitudinal
shortening over that segment. The results in Figs. 4 and 5 show that
local shortening varies strongly along the esophagus, with a peak
nearly coincident with the circular muscle contraction wave. Thus
average longitudinal shortening measured with clips will always
underestimate maximum local shortening in the segment between the
clips, and the underestimate will depend on the distance over which the
average is taken (i.e., the distance between the clips).
Coordinated waves of local longitudinal and circular muscle
contraction.
The data in Figs. 4 and 5 are presented as time changes in a variable
at a fixed location in the middle esophagus. However, Figs. 4 and 5 may
also be interpreted qualitatively as variations along the esophagus at
a fixed time by imagining the peaks in intraluminal pressure and local
longitudinal shortening in these figures to be at the transducer
location in the middle esophagus and assuming that the spatial wave
forms change only slowly as they propagate distally. The data to the
left of these peaks in the figures, then, represents the esophagus
distal to the transducer (note that the bolus arrives in advance of the
pressure peak), whereas the data to the right of the peaks represents
the esophagus proximal (3). Applied to Fig. 6, where the
time axis is reversed, this interpretation places the distal esophagus
on the right and the proximal esophagus on the left of the
three-dimensional images. The time axes can be converted roughly to
distance along the esophageal lumen by multiplying time by the
peristaltic wave speed, typically ~2 cm/s in the middle esophagus.
The resulting image is an approximation to the spatial structure along
the esophageal lumen of coordinated waves of circular muscle
contraction and local longitudinal shortening as they propagate
distally through the middle esophagus. The clip studies discussed above
indicate that, although the spatial structure of these peristaltic
waves likely changes slowly as the waves move into the distal
esophagus, the peaks in the circular muscle and local longitudinal
shortening waves remain closely aligned.
Previous studies using mucosal clips have implicitly assumed that
measured longitudinal shortening may be interpreted as indicating contraction of longitudinal muscle (note, for example, the reference to
the "contracting longitudinal segment" in the quote above from Ref.
16). Recognizing that studies of longitudinal shortening, using either mucosal clips or the method introduced here, are ultimately directed at the contractile activity of longitudinal muscle,
it is of interest to consider possible interpretations of longitudinal
shortening in context with circular and longitudinal muscle contraction
and the law of mass conservation.
To interpret the observed longitudinal shortening in terms of
longitudinal muscle contraction, consider the possibility that longitudinal shortening within a segment might occur in the absence of
longitudinal muscle contraction within the same segment. In this case,
the observed longitudinal shortening at peak intraluminal pressure is
possible only if the longitudinal muscle in segments proximal or distal
to the shortened segment were to extend. Because muscle has the
property that it can only contract (or relax from a previous
contraction), it is difficult to imagine a physiologically consistent
scenario in which the longitudinal shortening measured in this study
(and previous studies) could result from other than contraction of
longitudinal muscle fibers. It has been remarked that contraction of
circular muscle fibers concentrated within a narrow axial segment
could, in principle, create a bulge in area, and consequently local
longitudinal shortening, in adjacent esophageal segments as a result of
local deformation of the muscle layer from compression by the
contracting circular muscles. Although this effect is, in principle, a
possible contributor to longitudinal shortening, the relative magnitude
of the effect is undoubtedly minimal, given the material stiffness of
muscle. Nevertheless, if the effect were measurable, it could serve
only to reduce the peaks in A/A* in Figs. 4 and 5, implying
a slight underprediction of maximal local longitudinal shortening, and
the conclusions from this study, and related clip studies, remain unaffected.
We conclude that the local longitudinal shortening measured in this
study may be interpreted as indicating contraction of longitudinally
aligned muscle fibers either within the esophageal wall or within the
muscularis mucosa. Inferring the existence of circular muscle
contraction by deviations from baseline of intrabolus intraluminal
pressure, Figs. 4-6 indicate that a longitudinal muscle
contraction wave (LMCW) accompanies the peristaltic circular muscle
contraction wave (CMCW) as it traverses the esophagus, with peak
longitudinal contraction well coordinated with peak circular muscular
contraction. The LMCW envelops the CMCW, extending axially over a
broader region of the esophagus. In particular, whereas longitudinal
muscle contraction extends perhaps 2 cm distal to circular muscle
contraction in the middle esophagus (assuming a wave speed of 2 cm/s),
low-level contraction of longitudinal muscle appears to extend at least
twice that distance proximally from the CMCW (especially apparent in
Fig. 6). It may be that this low-level longitudinal shortening that
persists in the proximal esophagus after passage of the circular muscle
contraction wave reflects establishment of global shortening of the
esophagus that persists until the contraction waves have passed through
the lower esophageal sphincter and the esophagus has returned
to its resting state.
A physiological interpretation of local longitudinal shortening.
The observation that longitudinal shortening envelops circular muscle
contraction as the peristaltic wave traverses the esophagus was made in
excised opossum esophagi by Sugarbaker et al. (21), leading them to suggest a physiological role for longitudinal muscle
contraction. Sugarbaker et al. hypothesized that longitudinal shortening leads to local increases in circular muscle fiber number density within axial segments, which in turn increases the closure force generated by circular muscle contraction in that segment. Our
observation that local longitudinal shortening peaks close to the peak
in luminal pressure is consistent with this hypothesis.
Defining the force acting to close a segment of the esophagus of length
L as Fclosure, an approximate
relationship between average circular muscle fiber tension
Tfiber and the closure force Fclosure can be developed from a force balance
called the "Laplace equation"
|
(5)
|
where
circ is the thickness of the
circular muscle layer and const = 1/(2
) is a constant.
This expression states that for given closure force
Fclosure, the average circular muscle fiber tension Tfiber can be reduced by increasing the
thickness of the muscle layer
circ.
Alternatively, for given muscle fiber tension Tfiber, closure force
Fclosure is enhanced by increasing muscle layer
thickness
circ. Figs. 4 and 5 show that
circ increases under local longitudinal
shortening, thus reducing the average circular muscle fiber tension for
given closure force, or increasing closure force for given fiber tension.
Closure force Fclosure, it may be shown, is
directly proportional to intraluminal pressure P. Thus if
the Sugarbaker et al. hypothesis is valid, one should expect to find a
correlation between peak intraluminal pressure
Pamp and maximum local longitudinal shortening
(Amus/A*mus)max.
This is, in fact, the result in Fig. 7, where the correlation
coefficient is r = 0.61. [The correlation would be
significantly higher if the two lower points at
(Amus/A*mus)max
2.6 were missing.] This conclusion is potentially significant for
the transport of solid boluses, for which clearance typically requires
multiple circular muscle contraction waves, each contraction wave
moving the bolus partially along the esophagus before passing over. The
correlation in Fig. 7 between closure force and longitudinal shortening
implies the generation of higher axial propulsive force on solid
boluses compared with no longitudinal shortening. This conjecture might
explain the in vitro result of Ren and Schulze-Delrieu
(17), who found that the transport of a solid bolus
through an excised opossum esophagus was enhanced if the esophagus was
allowed to shorten globally.
Figure 8 indicates a strong correlation between a lower delay
t between onset of circular and longitudinal muscle
contraction and higher pressure amplitude Pamp,
or closure force. The following speculative scenario is offered as a
possible explanation for this observation in terms of bolus transport.
Maximal longitudinal shortening occurs nearly coincident with peak
intraluminal pressure (Figs. 4-6). If, in addition, the rate of
increase in pressure is approximately the same from swallow to swallow,
then a shorter time delay
t between the initiation of
circular and longitudinal muscle contraction would allow intraluminal
pressure to reach higher amplitude. In this way, the physiological
system could modulate the degree of contractile force required to
maintain closure for a given swallow by controlling the delay between
onset of circular and longitudinal muscle contraction.
Esophageal wall dimensions.
We have measured the thicknesses of the muscle layers in the middle
esophagus from the ultrasound images in the resting state to be
mus = 1.38 ± 0.07 mm
(
long
circ =
0.69 ± 0.05 mm) and
mucosa
3.0 mm.
These data likely represent the most accurate measurements to date of
in vivo esophageal muscle layer thicknesses. Others' data include
dimensions from surgically removed esophagi from cadavers (2, 10,
20) in which the excised esophagus has shortened by
30-50%, and three other ultrasound studies, one of which is from
the same data set used in the current study (14), and a
related data set other from the same group (11). The one independent ultrasound study (4) quoted only an
approximate estimate of 3 mm (no precision bounds), presumably over the
middle-to-distal esophagus in achalasics and apparently including part
or all of the mucosa. Furthermore, whereas Biancani et al.
(2) did quote dimensions allowing for estimates of mucosal
thickness in the middle esophagus that match those in this study, they
did not quote surgically obtained dimensions of muscle wall thickness directly, and it was necessary to deduce these from their plots and
equations. Nevertheless, taking into account shortening of excised
esophagi, their measurements were within range of the more careful
ultrasound studies presented here and in Refs. 11 and 14.
In summary, our results indicate that a wave of longitudinal muscle
contraction envelops the peristaltic wave of circular muscle
contraction as it passes through the middle esophagus, with peak
longitudinal contraction aligned with peak circular muscular
contraction. Our results support the hypothesis proposed by Sugarbaker
et al. (21) that the spatial and temporal coordination of
longitudinal and circular muscle contraction may be a physiological response to the mechanical influence of longitudinal shortening on
increasing contractile force while reducing average muscle fiber
tension. It follows, therefore, that mechanical advantage results by
physiologically maintaining close coordination between peak local
longitudinal shortening and maximal circular muscle contraction force.
 |
ACKNOWLEDGEMENTS |
This work was supported by National Institute of Diabetes and
Digestive and Kidney Diseases Grant R01-DK-41436.
 |
FOOTNOTES |
Address for reprint requests and other correspondence:
J. G. Brasseur, Dept. of Mechanical Engineering, The Pennsylvania
State Univ., University Park, PA 16802 (E-mail:
brasseur{at}jazz.me.psu.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.
Received 30 June 2000; accepted in final form 20 June 2001.
 |
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