Propagation veloc ties and frequencies along canine smal intestine MARIE-LUISE SIEGLE, SABINE HEINZ-ROBERT SCHMID, AND Institute of Zoophysiology, Division of D-7000 Stuttgart, Federal Republic of
SIEGLE, MARIE-LUISE, MANN, HEINZ-ROBERT
SABINE SCHMID,
BUHNER, MICHAEL SCHEMANN, HANS-JORG EHRLEIN Gastrointestinal Physiology, University of Hohenheim, Germany
BUHNER, MICHAEL SCHEAND HANS-JORG EHRLEIN.
Propagation velocities and frequencies of contractions along canine smaZZ intestine. Am. J. Physiol. 258 (Gastrointest. Liver Physiol. 21): G738-G744, 1990.-This study was performed to clarify in detail the behavior of the propagation velocities and frequencies of contractions along the canine small intestine. In conscious dogs, duodenal, jejunal, and ileal contractions were recorded by multiple, closely spaced strain gauges and analyzed by a computerized method. During both the interdigestive and postprandial states, the propagation velocity increased from the duodenal bulb to the distal duodenum and declined aborally within the jejunum, reaching rather constant values in the ileum. The decrease was steepest in the proximal part of the jejunum. In contrast to the propagation velocities, the contraction frequencies were almost constant in the upper small intestine. In the ileum, the contraction frequencies were markedly lower than in the upper small intestine, indicating that the aboral decrease in frequency occurred in the distal parts of the jejunum. We conclude that both the propagation velocities and the frequencies of contractions decline aborally in a nonlinear fashion. However, the nonlinear patterns of the frequency and the propagation velocity gradients are different. intestinal motility; basal intercontractile tive state; postprandial state; frequency coupling
interval; interdigesgradient; electrical
INTESTINAL SLOW WAVES are thought to determine frequency, velocity, and direction of intestinal contractions (4). Both the frequency and the velocity of slow waves and of contractions decrease aborally along the small intestine. For the intact intestine, both a continuous (13) and a stepwise (6, 10) frequency gradient have been reported. The stepwise frequency gradient supports the concept of linked frequency plateaus. Previous studies have indicated that the upper small intestine is characterized by a long frequency plateau (6, 14, 18), whereas in the distal small intestine the frequency plateaus are shorter (6, 18) or even nonexistent (14, 18). There is evidence that the degree of electrical coupling of adjacent muscle cells is related to the length of the frequency plateaus (7, 14). A high degree of electrical coupling in the upper small intestine is further indicated by the high propagation velocity of slow waves commonly observed in this region (2). The propagation velocities of slow waves and, in particular, of contractions along the small intestine have been investigated less extensively than G738
0193~1857/90
$1.50
of contractions
Copyright
0 1990
the contraction frequencies. Although an aboral gradient of propagation velocities has been demonstrated, detailed information on the behavior of the propagation velocities of contractions along the small intestine is not available. Therefore, we have studied the propagation velocities of duodenal, jejunal, and ileal contractions by using multiple, closely spaced strain gauge transducers. To compare data of the propagation velocities with those of the contraction frequencies, we additionally analyzed the basal intercontractile intervals as an indication of the frequencies of contractions. MATERIALSANDMETHODS Operative Procedure Studies were done in 12 conscious beagle dogs (lo-15 kg). Four animals were used for each of three series of experiments in which the motility of the duodenum and the adjacent jejunal segment (segment l), a more distal jejunal segment (segment Z), and the ileum were investigated. Dogs were anesthetized with acepromazine (1 mg/kg) and Fentanyl (0.14 mg/kg) and were maintained on halothane (0.6-l%) during surgery. Strain gauge force transducers (final size, 12 x 6 mm) were sutured on the serosal surface of the small intestine parallel to the axis of the circular muscle. To minimize shortening of the gut as a result of handling, atropine (0.1 mg/kg) was administered intravenously during the operation. Locations of the strain gauges were marked immediately after the laparotomy. Positions of the strain gauges are illustrated in Fig. 1. After the end of the study, the intertransducer distances were checked again in each dog during a second laparotomy. The values of each intertransducer distance measured during the first and second operation were averaged. These mean values were used for calculation of the propagation velocities of contractions. Because of variations between measurements of the first and second operations, these mean values varied slightly within one study segment. The largest deviation was t10% of the values presented in Fig. 1. Experimental Procedure Before surgery, the dogs were accustomed to the laboratory and the X-ray apparatus. They were trained to the American
Physiological
Society
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stand quietly on a table and were supported by a hammock. Experiments began 10 days after surgery when the dogs had completely recovered. Before each experiment, the dogs were fasted for at least 18 h. In all dogs, studies were done during phase III of the interdigestive migrating motor complex (MMC) and in the postprandial state. The postprandial motor activity was induced by an acaloric viscous meal of cellulose gum, because in comparison with a nutrient meal the acaloric meal produced a greater number of propagated contractions and a greater number of contractions occurring at the basal intercontractile interval. Previous studies (3, 15, 17) indicated that the mean values of propagation velocities showed no significant differences between acaloric and nutrient meals. The acaloric meal was administered into the stomach by an oroesophageal tube during phase I of the MMC after an activity front had passed the duodenal, jejunal, or ileal study segment, respectively. Videofluoroscopy showed that in each study segment the acaloric meal produced a motor pattern consisting of a strong stimulation of propulsive activity. Characteristics of this motor pattern have been described previously for the duodenal, jejunal, and ileal segment (3, 15, 17). Analysis of motility was started when the characteristic motor pattern was present at the study segment. It has been previously reported (15, 17) that the onset of the characteristic motor pattern induced by a meal was delayed in the distal parts of the small intestine. The delay increased with the distance of the study segment from the pylorus. DUODENUM-JEJUNU (segment
M 1) rus
2.5cm
JEJU (segm Lig. 40.0cm 4.5cm
6.0cm [
NUM ent 2)
Jl C
32
D2
J3 22.5cm
J4
D3
24.0cm
J5
D4
J6 Lig. Treitz
24.0cm
. ’
-1
D5
m
Jl
I(
J2
m
J3
m
J4
W
J5
2.2cm[
13.2cm
I
1
-
I
m
I
-
I
I
I 1 I
2.5cm II
I
Colon
FIG. I.. Positions of strain gauge force transducers in different experimental series. Intertransducer distances were measured from center to center. On segment 1,110 strain gauges were sutured at 6-cm intervals. Length of the duodenal and jejunal segment I was 24.0 cm each. On segment 2 and the ileum, strain gauge transducers were equally spaced at 4.5-cm and 2%cm intervals, respectively. Length of segment 2 was 22.5 cm, that of the ileum 13.2 cm. Dl-D5 and 51-55, transducers on the duodenum and the adjacent jejunal segment, respectively; Jl-J6, transducers on segment 2; 11-17, transducers of the ileum.
INTESTINAL
CONTRACTIONS
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In 12 dogs, 146 phases III of the MMC were recorded (43 in the duodenal-jejunal segment 1, 33 in the jejunal segment 2, and 70 in the ileum). The total number of postprandial experiments was 121 (36 in segment 1, 19 in segment 2, and 66 in the ileum). Test Meal For preparation of the acaloric viscous meal, 12 g of hydroxyethylcellulose (Tylose H300, Hoechst, Frankfurt, FRG) was diluted in 200 ml of 0.78% saline, yielding a homogeneous (particle size, 0.1 pm) meal. The viscosity was 40,000-60,000 CP measured at 5 revolutions/min and 37°C by a rotation viscometer (Brookfield, Stoughton, MA). The osmolarity was 300 mosM. Dogs used for studies of the duodenal and jejunal motility received a volume of 200 ml. For the study of the ileal motility, a volume of 400 ml was used to obtain a sufficiently long stimulation of postprandial motility. Recording Technique and Videofluoroscopy The recording technique, the system of on-line data acquisition, and the technique of videofluoroscopy have been previously described in detail (8, 16). Data Analysis The intertransducer distances used in the present study differed according to the intestinal site of implantation. They were greater in the proximal parts of the small intestine than in the distal parts. The choice of appropriate intertransducer distances depended on two factors: the propagation velocity of contractions and the basal intercontractile interval. Propagated contractions spreading aborally occurred at adjacent recording sites with time differences reflecting their propagation velocities. Because of variations of the propagation velocities, these time differences were distributed around a mean value. The intertransducer distance was chosen adequately when the distribution was located within the basal intercontractile interval (Fig. ZA). With shorter intertransducer distances, the distribution of time differences would be shifted to the left, since time differences would be smaller (Fig. ZB). Because of reasons discussed later, a reliable evaluation of the propagation velocities would be critical. On the other hand, with greater intertransducer distances the distribution of the time differences would be shifted to the right, and time differences would become at least in part greater than the basal intercontractile interval (Fig. ZC). Consequently, slow propagated contractions would be identified either as stationary contractions or as very fast propagated contractions because of a false coordination (Fig. ZC). In the present study, stationary and propagated contractions were identified by a computerized method (16). To differentiate between stationary and propagated contractions, the time differences of the contraction maxima recorded at each of two adjacent transducers were analyzed. As described above, propagated contractions occurring at adjacent transducers produced time differences that were distributed around a mean value. The
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Intercontractile
VELOCITY
OF
INTESTINAL
Intercontractile interval
CONTRACTIONS Intercontractile interval
.... .. .. r..:...t.=...A . .. .. .. . . . .. .. . .. .
coordination !
).... . . . . t’. . .. .. .. . .. Ii r.:.:.:.:.~.:.:.:.:.~ ..... t~~~~f$+:.:.:.:.~ ‘~:~:~~~~~:*~~~~:~~ i I. . . . . . . . . . . . .
2.2
Time
(s)
2.2
Time
(s)
0
2.2
Time
(s)
FIG. 2. Choice of the appropriate intertransducer distance for a reliable evaluation of propagation velocities of contractions. Choice of the appropriate distance depended on 2 factors: propagation velocity and basal intercontractile interval. With an appropriate intertransducer distance, time differences of propagated contractions occurring at 2 adjacent transducers were distributed around a mean value (A). Time differences, even the greatest, were clearly less than basal intercontractile interval. Thin dashed lines indicate fastest and slowest propagation velocities corresponding to the limits of the distribution of time differences of propagated contractions. Thick dashed lines indicate mean propagation velocity. With a shorter intertransducer distance, distribution of time differences would be shifted to the left (B), which would complicate the differentiation between simultaneously ocurring and propagated contractions, since very fast propagation velocities would produce very small time differences. With a greater intertransducer distance, distribution of time differences would be shifted to the right. If the intertransducer distance is too large, slow propagation velocities would produce time differences greater than basal intercontractile interval (C). Consequently, slowly propagated contractions would be misinterpreted either as stationary contractions or as fast propagated contractions due to a false coordination (C).
limits of this distribution were used as limits for a time window necessary for the computerized identification of propagated contractions. Consequently, contractions occurring at two adjacent recording sites within the time window were defined as propagated contractions. Stationary contractions were those that occurred out of the time window. Videofluoroscopy confirmed that time differences occurring within the limit of the time window were caused by propagated contractions. In Fig. 3, it is illustrated for each study segment which propagation velocities were admitted by the time window. In the present study, the mean values of the time differences occurring within the defined time window were evaluated for all the adjacent recording sites in each study segment. The propagation velocities of contractions (cm/s) between two adjacent recording sites were calculated by dividing the intertransducer distance by the corresponding mean time difference. Additionally, the intercontractile intervals were analyzed for each recording site in all the study segments. The intercontractile interval was the time (in seconds) elapsed between two consecutive contraction maxima at one recording site. Analysis of the frequency distribution of the intercontractile intervals showed three peaks, which represented at least 85% of all the intercontractile intervals. Within each peak, the intercontractile inter-
vals were distributed around a mean value. In segments 1 and 2, the intercontractile intervals of peak 1 varied from 2.5 to 5.5 s. In the ileum, they varied from 3.0 to 6.5 s. In the present study, the mean values of intercontractile intervals of the first peak were calculated. The mean value ofpeak 1 represented the basal intercontractile interval when the intestine contracted at its maximal rate. The contraction frequency was calculated as the reciprocal of the basal interval in contractions per minute. In RESULTS, the data of the basal intercontractile interval are presented as frequency, indicating the maximal rate of contractions. Code et al. (4) reported that the maximal frequency of contractions is based on the rhythm of the pacesetter potential. Statistics Data are presented as mean values t SE for four dogs. A rank variance analytical test (Friedman’s test) was used to prove if data of each study segment were homogeneous. If statistical significance (P c 0.05) was obtained, values were characterized by a certain rank order. During the postprandial state, the basal intercontractile interval measured at the duodenal bulb (Dl) was excluded from the statistical analysis and from the calculation of the duodenal mean value, because the duodenal bulb exhibited a significantly smaller basal intercontract-
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FREQUENCY DUODENUM-JEJUNUM (segment Intercontractile interval
1)
1
AND JEJUNUM (segment
VELOCITY
OF
INTESTINAL ILEUM
2 1
Intercontractile interval
Intercontractile interval
1
1
cm ~-w-v
t*. ? V’ ‘1 ~~~.\.“. . Cj:::::$.& (.:.;:.:.g:j(.:.> . .. ... ... .. .. - A•.:.:.:.:.:.:~.:~~.~~ Id A
.le interval compared with the other prove if data of the interdigestive and were different, Student’s t test for used. A probability value ~0.05 was cally significant.
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duodenal sites. To postprandial states unpaired data was considered statisti-
,
/
I
/
;’
?,
A U.I. \\
\ br
FIG. 3. Propagation velocities admitted by the defined time window in the 3 different study segments. Contractions occurring within the lower and upper limit (1.1. and u.1.) of the time window at the adjacent aboral transducer were defined as propagated. Dotted areas indicate variations of propagation velocities in each study segment. Thin dashed lines indicate fastest and slowest propagation velocities admitted by the limits of the time window. Variations of the lower and upper limit of the time window because of different variations of the propagation velocity between different adjacent transducers are not indicated. Thick dashed lines represent the fastest and slowest mean propagation velocity measured between 2 adjacent transducers within 1 study segment.
significant faster propagation velocities in the postprandial state only occurred in the jejunal segment 1 (Fig. 4) . Frequencies of Contractions
Phase III of 2MIMC. The frequency of contractions did not show any trend to either increase or decrease along the duodenum (Fig. 4, Table 1). The mean frequency was Propagation Velocities of Contractions 17.8 t 0.12 contractions/min. In contrast to the duodenal Phase III of IMIMC. The propagation velocities of con- segment, contraction frequency decreased slightly (P < tractions progressively increased along the duodenum 0.05) along the jejunal and ileal segments (Fig. 4, Table (Fig. 4, Table 1). In three of four dogs, the maximal 1). The decreases along the intestinal segments were 2% propagation velocity occurred between the duodenal re- in the jejunal segment 1,4% in segment 2, and 4% in the cording sites D4 and D5 (20.5 and 26.5 cm aborad to the ileum (Table 3). pylorus). In one dog, the maximal value was observed Postprandial state. In contrast to the interdigestive between the recording sites D3 and D4 (14.5 and 20.5 cm state, contraction frequencies measured in the postaborad to the pylorus). In the jejunal segments 1 and 2, prandial state did not show any trend to either increase the propagation velocities declined aborally (Fig. 4, Table or decrease along the duodenal and jejunal segments (Fig. 1). Mean values t SE of propagation velocities between 4, Table 1). The mean values of contraction frequencies the first and last two recording sites of each study seg- measured in the duodenum, jejunal segment 1, and segment are given in Table 2. The reduction in the propa- ment 2 were 17.2 t 0.10, 17.3 t 0.11, and 17.2 t 0.17 gation velocities was stronger along the jejunal segment contractions/min, respectively. The contraction fre1 (45%) than segment 2 (20%), although the lengths of quency increased along the ileum (Fig. 4, Tables 1 and the study segments were similar (24.0 and 22.5 cm, 3) . respectively). Lowest values of the propagation velocities Compared with phase III of the MMC, the contraction of contractions were measured in the ileum (Fig. 4). frequency was diminished in each study segment postWithin this segment, the propagation velocities did not prandially (Fig. 4). The difference was significant in the show any trend to either increase or decrease (Table 1). ileum and for some recording sites in the duodenum and The mean propagation velocity of ileal contractions was proximal jejunum (Fig. 4). The difference was most pro0.76 & 0.04 cm/s. nounced in the ileum (Fig. 4). On average, contraction Postprandial state. The behavior of propagation veloc- frequency decreased by 3% in the duodenum, 1% in the ities of contractions within each study segment was jejunal segment 1, 1% in segment 2, and 8% in the ileum. postprandially similar as during phase III (Fig. 4, Table 1) DISCUSSION Compared with phase III, the propagation velocities tended to be faster in the postprandial state (11% in the This study presents for the first time a detailed analyduodenum, 20% in the jejunal segment 1,24% in segment sis of the propagation velocities of contractions in different regions along the canine small intestine. The detailed 2, and 3% in the ileum) (Fig. 4). However, statistically RESI.
LTS
l
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-
JEJUNUM (segment
JEJUNUM (segment
1)
AND
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OF
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2. Propagation velocities of contractions between the first and last two recording sites of different intestinal segments TABLE
ILEUM 2)
14.2
Propagation of Contractions,
Intestinal Segment Phase
Duodenum Dl-D2 D4-D5 Jejunum 1 51-52 54-55 Jejunum 2 51-52 55-56 Ileum 11-12 16-17
4.8 0.9
0.8 n
lg-
18.5 I\
Values
are means
III
Velocity cm/s Postprandial
6.78t0.65 11.74t1.26
7.71t0.65 14.23t1.88
8.62t0.68 4.75t0.35
9.60t0.78 5.76kO.16
3.90t0.35 3.09t0.21
5.05t0.45 3.38t0.41
0.69t0.03 0.81kO.04
0.75t0.03 0.86t0.04
k SE. Recording
sites are as listed
in Fig. 1.
3. Contraction frequencies at the first and last recording sites of different intestinal segments
TABLE
Contraction Frequency, contractions/min
Intestinal Segment Phase
13.8
12. I
!- .I’ .I”14
I,, .I,, Dl D2D3D4D5
, , , Jl J2 J3 J4 J5
I , , , Jl J2J3J4J5J6 1 22.5cm t
-11
f
24.0cm
2.5cm aborad to pylorus
f
24.0cm
Lig.Treitz
1
*
,
12.7
12.5 I
I
1
,
.
.
.
I1 12 13 14 15 I6 I7 I I 13.2cm f
I
40 cm aborad to Lig.Treitz
2.5cm
orad to ICS
FIG. 4. Propagation velocities (top) and frequencies of contractions (bottom) along 3 different study segments during phase III (solid lines) and the postprandial state (dashed lines). Values are means t SE for 4 dogs. *Statistically significant differences (P < 0.05) between the interdigestive and postprandial state. Figures indicate propagation velocities and frequencies of contractions between the first and last 2 recording sites and at the first and last recording sites, respectively, of each study segment. Abbreviations as in Fig. 1.
1. Behavior of different parameters along different intestinal segments during phase III and the postprandial state TABLE
Propagation Velocity
Intestinal Segment Phase
Duodenum Jejunum 1 Jejunum 2 Ileum
+ 0
III
Contraction Frequency
Postprandial
+ 0
Duodenum Dl D5 Jejunum 1 Jl 55 Jejunum 2 Jl J6 Ileum 11 I7
Phase
0 -
III
Postprandial
0 0 0 +
Plus and minus signs indicate significant trends (P < 0.05) of increasing and decreasing values along an intestinal segment, respectively; 0 indicates that values along an intestinal segment were homogeneous (P > 0.05, Friedman’s test).
characterization of the propagation velocities was achieved by the use of multiple, closely spaced transducers. Results indicate that during both the interdigestive and the postprandial states the propagation velocities of contractions increased from the duodenal bulb to the distal duodenum and then declined in an apparently exponen-
Values
are means
III
Postprandial
17.8t0.11 17.7kO.13
18.5t0.31 17.1t0.14
17.7t0.12 17.4kO.15
17.2t0.10 17.3t0.09
17.7t0.24 17.0t0.25
17.2t0.20 17.2t0.21
13.8t0.08 13.3t0.11
12.5t0.17 12.7kO.19
t SE. Recording
sites are as listed
in Fig. 1.
tial fashion along the jejunum, reaching smallest values in the ileum. The increasing propagation velocities of contractions in the proximal duodenum have already been reported in a previous study (11), but they were not observed by other investigators. There might be several reasons for this difference: first, by the use of only one or two widely spaced transducers one might miss the phenomenon (1, 12), and second, other investigators who used multiple, closely spaced transducers did not evaluate propagation velocities within the duodenal segment (9). The physiological significance of the increase in the propagation velocity along the duodenum remains to be clarified. Previously, McCoy and Baker (12) showed that in the upper small intestine propagation velocities of slow waves declined aborally in a linear fashion. Assuming that the linear decrease in velocity continues aborally, the velocity of slow waves would become zero at a certain region of the jejunum. Since this is unlikely, McCoy and Baker (12) suggested that the velocity might decrease only to a small but finite value. Indeed, our study indicates that propagation velocities of contractions decreased aborally in a nonlinear fashion. The decrease was steepest in the jejunal segment 1 and got smaller in segment 2. In the ileum, propagation velocity was almost
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constant. However, we cannot deduce from our study in which part of the small intestine nearly constant values of propagation velocities were reached. It is noteworthy that velocities of jejunal contractions differed markedly depending on the site of measurement, i.e., from -10 cm/s at the ligament of Treitz to -0.7 cm/s at the end of the jejunum. Propagation velocities of slow waves in the upper jejunum determined in previous studies ranged from 1.8 to 8 cm/s (1,4,X2) and those of ileal slow waves from 0.5 to 0.8 cm/s (1, 4). These values are rather consistent with our results. However, since the propagation velocity declines steeply within the proximal jejunum, values are only comparable when the sites of measurement are exactly defined. The present study shows that the frequencies of contractions were constant or changed only slightly in the proximal intestinal segments. The ileum exhibited markedly lower contraction frequencies than the proximal intestine. Values of contraction frequencies reported in this study are consistent with values (17-20 contractions/min in the duodenum and U-14 contractions/min in the ileum) summarized by Code et al. (4). The almost constant contraction frequency in the proximal small intestine and the markedly lower values in the ileum suggest that the aboral decrease of the contraction frequency occurs in the distal part of the jejunum. Previously, it has been shown that both the intestinal slowwave frequency (56) and the contraction frequency (10) decreased aborally in a stepwise fashion, with variable lengths of intestine having the same frequency. Frequency plateaus have been described to be longer in the upper small intestine than in its distal parts (5, 6, 18). In dogs, it has been found that the proximal frequency plateau was -60-70 cm in length extending through the duodenum into the proximal jejunum, whereas distal frequency plateaus were only a few centimeters in length (6). Additionally, it has been shown that the lengths and positions of the frequency plateaus varied with time (6). In the present study, determination of frequency plateaus was critical because different plateaus might be obscured by averaging values from different recording sessions and different animals. Present and previous findings (5, 6) concerning the behavior of various parameters along the small intestine are summarized schematically in Fig. 5. This figure represents a model to explain the nature of the aboral propagation velocity and frequency gradients. The internal resistance illustrated in Fig. 5 has been calculated from our data of propagation velocities according to the cable equation relating propagation velocity to internal resistance (19). Assuming that all other factors of this equation remain constant, the internal resistance is inversely related to the square of the propagation velocity. It has been suggested (2, 6) that the internal resistance determines the degree of electrical coupling of adjacent muscle cells by modification of the current flow in electrically excitable tissues. There is evidence that both the length of frequency plateaus (7, 14) and the propagation velocity (2) are related to the degree of electrical coupling. As illustrated in Fig. 5, the low internal resistance and, consequently, the high degree of electrical coupling
OF
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CONTRACTIONS Plateaus in vivo
of frequencies
I I Lig. of Treitz
I
I lleocolic junction
60 cm aborad to Lig. of Treitz
FIG. 5. Schematic model summarizing present concerning the nature of gradients of various small intestine. See text for further details.
and previous findings parameters along the
in the proximal small intestine appear to be responsible for both the long frequency plateau and the high propagation velocity in this region. On the other hand, short frequency plateaus and slow propagation velocities in the distal small intestine might be related to a low degree of electrical coupling. Figure 5 further illustrates that the propagation velocity of contractions decreases along the jejunum and ileum in a more continuous manner, whereas the frequency of contractions decreases in a discontinuous manner. It is likely that the frequency changes abruptly at the end of the plateaus where, because of the increasing internal resistance, the current is of insufficient magnitude to entrain the next slow-wave oscillator, whereas the aborally increasing internal resistance decreases the propagation velocity continuously independent of the frequency plateaus. The aboral decreases in the propagation velocity and the frequency of intestinal contractions appear to be of functional significance for the transport of intestinal content. Code et al. (4) reported that the “wavelength” of the pacesetter potential calculated from the frequency and the propagation velocity decreased from the duodenum to the ileum. Previously it has been shown that the mean length of contraction spread was characterized by a similar gradient (15, 17). It might be possible that the degree of electrical coupling that determines the length of frequency plateaus is also responsible for the length of contraction spread. It is suggested that the long plateau of high frequency, the fast propagation velocity, and the large length of contraction spread in the upper small intestine promote the propulsion of thyme evacuated from the stomach along the small intestine. Decreases in these parameters along the small intestine would then result in a delayed transport of thyme in the distal small intestine. Because the volume of luminal content decreases distally by absorption, it appears reasonable that transport of thyme slows down. The present study shows that along the small intestine the contraction frequencies tended to be shorter and the propagation velocities tended to be greater after administration of an acaloric meal compared with the interdigestive state. These results agree with previous findings
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indicating an inverse relationship between frequency and propagation velocity (2). We assume that the acaloric content of the small intestine might activate reflexes, producing a decrease in frequency. Because of the inverse relationship between frequency and propagation velocity, this would result postprandially in an increase in propagation velocity. In the proximal small intestine, this postprandial increase in propagation velocity was clearcut, whereas in the ileum a pronounced decrease in contraction frequency after the meal was accompanied only by a slight change in the propagation velocity. Previous studies (2) indicate that the relation between frequency and propagation velocity is not uniform. In the duodenum, a decrease in contraction frequency led to a more pronounced increase in the propagation velocity than in the jejunum (2). Our results support these findings and further indicate that because of the increasing internal resistance along the gut, this relation is almost nonexistent in the ileum. In the present study, different intertransducer distances were used to investigate propagation velocities at different regions of the small intestine. The choice of the appropriate intertransducer distances depended on the propagation velocities and the basal intercontractile intervals. For a reliable identification of propagated contractions and their propagation velocities, time differences of propagated contractions occurring at two adjacent recording sites should be first, shorter than the basal intercontractile interval and second, clearly distinguishable from zero. Intertransducer distances spaced very closely would result in extremely small time differences. Recently, the distribution of time differences of duodenal contractions occurring at transducers 2.5 cm apart were investigated by Engstrom et al. (9). This distribution mainly consisted of positive time differences indicating aboral propagation, but it also consisted of a few negative values; these were interpreted as orally propagated contractions. Since positive and negative time differences belonged to a homogeneous distribution, we assume that the negative time differences might be the result of the relatively small intertransducer distances used in this study. If the intertransducer distances are too small, the maximum of a contraction at the distal transducer might occur slightly earlier than that of a contraction at the oral transducer, since the contraction rise time (time from contraction onset to maximum) is variable. Consequently, negative time differences might be determined despite an aboral propagation of contractions. Because of the aboral decrease in propagation velocity of contractions, the intertransducer distances used in the present study were greater in the duodenum and the adjacent jejunal segment 1 (6 cm) than in the more distal jejunal segment 2 (4.5 cm) and the ileum (2.2 cm). On the other hand, the intertransducer distances should be kept constant within a study segment to allow the evaluation of other motility parameters like the length of contraction spread. Despite the considerable
OF
INTESTINAL
CONTRACTIONS
variations of the propagation velocities in the duodenaljejunal segment, intertransducer distances of -6 cm were appropriate to acquire both the fastest and the slowest propagation velocities occurring in this region. The authors thank Hani Sahyoun for assistance in computer analysis and Ingeborg Ehrlein and Margrit Hartmann for technical assistance. Address for reprint requests: H.-J. Ehrlein, Inst. of Zoophysiology, Div. of Gastrointestinal Physiology, Univ. of Hohenheim, Garbenstr. 30, D-7000 Stuttgart 70, FRG. Received
21 July
1989; accepted
in final
form
12 December
1989.
REFERENCES 1. ARMSTRONG, I-L I. O., G. W. MILTON, AND A. W. M. SMITH. Electropotential changes of the small intestine. J. Physiol. Land. 131: 147-153, 1956. 2. BORTOFF, A. Myogenic control of intestinal motility. Physiol. Rev. 56: 418-434, 1976. 3. BUHNER; S., AND H.-J. EHRLEIN. Characteristics of postprandial duodenal motor patterns in dogs. Dig. Dis. Sci. 34: 1873-1881,1989. 4. CODE, C. F., J. H. SZURSZEWSKI, K. A. KELLY, AND I. B. SMITH. A concept of control of gastrointestinal motility. In: Handbook of Physiology. Alimentary Canal. Washington, DC: Am. Physiol. Sot., 1968, sect. 6, vol. V, chapt. 139, p. 2881-2895. 5. DIAMANT, N. E., AND A. BORTOFF. Effects of transection on the intestinal slow-wave frequency gradient. Am. J. Physiol. 216: 734743, 1969. 6. DIAMANT, N. E., AND A. BORTOFF. Nature of the intestinal slowwave frequency gradient. Am. J. PhysioZ. 216: 301-307, 1969. 7. DIAMANT, N. E., P. K. ROSE, AND E. J. DAVISON. Computer simulation of intestinal slow-wave frequency gradient. Am. J. Physiol. 219: 1684-1690, 1970. 8. EHRLEIN, H.-J. A new technique for simultaneous radiography and recording of gastrointestinal motility in unanesthetized dogs. Lab. Anim. Sci. 30: 879-884, 1980. 9. ENGSTROM, E. R., J. G. WEBSTER, AND P. BASS. Analysis of duodenal contractility in the unanesthetized dog. IEEE Trans. Biomed. Eng. 26: 517-523,1979. 10. HASSELBRACK, R., AND J. E. THOMAS. Control of intestinal rhythmic contractions by a duodenal pacemaker. Am. J. Physiol. 201: 955-960, 1961. 11. KEINKE, O., M. SCHEMANN, AND H.-J. EHRLEIN. Mechanical factors regulating gastric emptying of viscous nutrient meals in dogs. &. J. Exp. Physiol. 69: 781-795, 1984. 12. MCCOY, E. J., AND R. D. BAKER. Intestinal slow waves: decrease in propagation velocity along upper small intestine. Am. J. Dig. Dis. 14: 9-13, 1969. 13. NELSON, T. S., AND J. C. BECKER. Simulation of the electrical and mechanical gradient of the small intestine. Am. J. PhysioZ. 217: 749-757, 1968. 14. SARNA, S. K., E. E. DANIEL, AND Y. J. KINGMA. Simulation of slow-wave electrical activity of small intestine. Am. J. Physiol. 221: 166-175,197l. 15. SCHEMANN, M., AND H.-J. EHRLEIN. Postprandial patterns of canine jejunal motility and transit of luminal content. GastroenteroZogy 90: 991-1000, 1986. 16. SCHEMANN, M., M.-L. SIEGLE, H. SAHYOUN, AND H.-J. EHRLEIN. Computer analysis of intestinal motility: effects of cholecystokinin and neurotensin on jejunal contraction patterns. 2. Gastroenterol. 24: 262-268,1986. 17. SIEGLE, M.-L., AND H.-J. EHRLEIN. Digestive motor patterns and transit of luminal contents in canine ileum. Am. J. Physiol. 254 (Gastrointest. Liver Physiol. 17): G552-G559, 1988. 18. SZURSZEWSKI, J. H., L. R. ELVEBACK, AND C. F. CODE. Configuration and frequency gradient of electric slow wave over canine small bowel. Am. J. Physiol. 218: 1468-1473, 1970. 19. TOMITA, T. Electrical properties of mammalian smooth muscle. In: Smooth Muscle, edited by E. Bulbring, A. F. Brading, A. W. Jones, and T. Tomita. London: Arnold, 1970, p. 197-243.
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SIEGLE, MARIE-LUISE, MANN, HEINZ-ROBERT
SABINE SCHMID,
BUHNER, MICHAEL SCHEMANN, HANS-JORG EHRLEIN Gastrointestinal Physiology, University of Hohenheim, Germany
BUHNER, MICHAEL SCHEAND HANS-JORG EHRLEIN.
Propagation velocities and frequencies of contractions along canine smaZZ intestine. Am. J. Physiol. 258 (Gastrointest. Liver Physiol. 21): G738-G744, 1990.-This study was performed to clarify in detail the behavior of the propagation velocities and frequencies of contractions along the canine small intestine. In conscious dogs, duodenal, jejunal, and ileal contractions were recorded by multiple, closely spaced strain gauges and analyzed by a computerized method. During both the interdigestive and postprandial states, the propagation velocity increased from the duodenal bulb to the distal duodenum and declined aborally within the jejunum, reaching rather constant values in the ileum. The decrease was steepest in the proximal part of the jejunum. In contrast to the propagation velocities, the contraction frequencies were almost constant in the upper small intestine. In the ileum, the contraction frequencies were markedly lower than in the upper small intestine, indicating that the aboral decrease in frequency occurred in the distal parts of the jejunum. We conclude that both the propagation velocities and the frequencies of contractions decline aborally in a nonlinear fashion. However, the nonlinear patterns of the frequency and the propagation velocity gradients are different. intestinal motility; basal intercontractile tive state; postprandial state; frequency coupling
interval; interdigesgradient; electrical
INTESTINAL SLOW WAVES are thought to determine frequency, velocity, and direction of intestinal contractions (4). Both the frequency and the velocity of slow waves and of contractions decrease aborally along the small intestine. For the intact intestine, both a continuous (13) and a stepwise (6, 10) frequency gradient have been reported. The stepwise frequency gradient supports the concept of linked frequency plateaus. Previous studies have indicated that the upper small intestine is characterized by a long frequency plateau (6, 14, 18), whereas in the distal small intestine the frequency plateaus are shorter (6, 18) or even nonexistent (14, 18). There is evidence that the degree of electrical coupling of adjacent muscle cells is related to the length of the frequency plateaus (7, 14). A high degree of electrical coupling in the upper small intestine is further indicated by the high propagation velocity of slow waves commonly observed in this region (2). The propagation velocities of slow waves and, in particular, of contractions along the small intestine have been investigated less extensively than G738
0193~1857/90
$1.50
of contractions
Copyright
0 1990
the contraction frequencies. Although an aboral gradient of propagation velocities has been demonstrated, detailed information on the behavior of the propagation velocities of contractions along the small intestine is not available. Therefore, we have studied the propagation velocities of duodenal, jejunal, and ileal contractions by using multiple, closely spaced strain gauge transducers. To compare data of the propagation velocities with those of the contraction frequencies, we additionally analyzed the basal intercontractile intervals as an indication of the frequencies of contractions. MATERIALSANDMETHODS Operative Procedure Studies were done in 12 conscious beagle dogs (lo-15 kg). Four animals were used for each of three series of experiments in which the motility of the duodenum and the adjacent jejunal segment (segment l), a more distal jejunal segment (segment Z), and the ileum were investigated. Dogs were anesthetized with acepromazine (1 mg/kg) and Fentanyl (0.14 mg/kg) and were maintained on halothane (0.6-l%) during surgery. Strain gauge force transducers (final size, 12 x 6 mm) were sutured on the serosal surface of the small intestine parallel to the axis of the circular muscle. To minimize shortening of the gut as a result of handling, atropine (0.1 mg/kg) was administered intravenously during the operation. Locations of the strain gauges were marked immediately after the laparotomy. Positions of the strain gauges are illustrated in Fig. 1. After the end of the study, the intertransducer distances were checked again in each dog during a second laparotomy. The values of each intertransducer distance measured during the first and second operation were averaged. These mean values were used for calculation of the propagation velocities of contractions. Because of variations between measurements of the first and second operations, these mean values varied slightly within one study segment. The largest deviation was t10% of the values presented in Fig. 1. Experimental Procedure Before surgery, the dogs were accustomed to the laboratory and the X-ray apparatus. They were trained to the American
Physiological
Society
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FREQUENCY
AND
VELOCITY
OF
stand quietly on a table and were supported by a hammock. Experiments began 10 days after surgery when the dogs had completely recovered. Before each experiment, the dogs were fasted for at least 18 h. In all dogs, studies were done during phase III of the interdigestive migrating motor complex (MMC) and in the postprandial state. The postprandial motor activity was induced by an acaloric viscous meal of cellulose gum, because in comparison with a nutrient meal the acaloric meal produced a greater number of propagated contractions and a greater number of contractions occurring at the basal intercontractile interval. Previous studies (3, 15, 17) indicated that the mean values of propagation velocities showed no significant differences between acaloric and nutrient meals. The acaloric meal was administered into the stomach by an oroesophageal tube during phase I of the MMC after an activity front had passed the duodenal, jejunal, or ileal study segment, respectively. Videofluoroscopy showed that in each study segment the acaloric meal produced a motor pattern consisting of a strong stimulation of propulsive activity. Characteristics of this motor pattern have been described previously for the duodenal, jejunal, and ileal segment (3, 15, 17). Analysis of motility was started when the characteristic motor pattern was present at the study segment. It has been previously reported (15, 17) that the onset of the characteristic motor pattern induced by a meal was delayed in the distal parts of the small intestine. The delay increased with the distance of the study segment from the pylorus. DUODENUM-JEJUNU (segment
M 1) rus
2.5cm
JEJU (segm Lig. 40.0cm 4.5cm
6.0cm [
NUM ent 2)
Jl C
32
D2
J3 22.5cm
J4
D3
24.0cm
J5
D4
J6 Lig. Treitz
24.0cm
. ’
-1
D5
m
Jl
I(
J2
m
J3
m
J4
W
J5
2.2cm[
13.2cm
I
1
-
I
m
I
-
I
I
I 1 I
2.5cm II
I
Colon
FIG. I.. Positions of strain gauge force transducers in different experimental series. Intertransducer distances were measured from center to center. On segment 1,110 strain gauges were sutured at 6-cm intervals. Length of the duodenal and jejunal segment I was 24.0 cm each. On segment 2 and the ileum, strain gauge transducers were equally spaced at 4.5-cm and 2%cm intervals, respectively. Length of segment 2 was 22.5 cm, that of the ileum 13.2 cm. Dl-D5 and 51-55, transducers on the duodenum and the adjacent jejunal segment, respectively; Jl-J6, transducers on segment 2; 11-17, transducers of the ileum.
INTESTINAL
CONTRACTIONS
G739
In 12 dogs, 146 phases III of the MMC were recorded (43 in the duodenal-jejunal segment 1, 33 in the jejunal segment 2, and 70 in the ileum). The total number of postprandial experiments was 121 (36 in segment 1, 19 in segment 2, and 66 in the ileum). Test Meal For preparation of the acaloric viscous meal, 12 g of hydroxyethylcellulose (Tylose H300, Hoechst, Frankfurt, FRG) was diluted in 200 ml of 0.78% saline, yielding a homogeneous (particle size, 0.1 pm) meal. The viscosity was 40,000-60,000 CP measured at 5 revolutions/min and 37°C by a rotation viscometer (Brookfield, Stoughton, MA). The osmolarity was 300 mosM. Dogs used for studies of the duodenal and jejunal motility received a volume of 200 ml. For the study of the ileal motility, a volume of 400 ml was used to obtain a sufficiently long stimulation of postprandial motility. Recording Technique and Videofluoroscopy The recording technique, the system of on-line data acquisition, and the technique of videofluoroscopy have been previously described in detail (8, 16). Data Analysis The intertransducer distances used in the present study differed according to the intestinal site of implantation. They were greater in the proximal parts of the small intestine than in the distal parts. The choice of appropriate intertransducer distances depended on two factors: the propagation velocity of contractions and the basal intercontractile interval. Propagated contractions spreading aborally occurred at adjacent recording sites with time differences reflecting their propagation velocities. Because of variations of the propagation velocities, these time differences were distributed around a mean value. The intertransducer distance was chosen adequately when the distribution was located within the basal intercontractile interval (Fig. ZA). With shorter intertransducer distances, the distribution of time differences would be shifted to the left, since time differences would be smaller (Fig. ZB). Because of reasons discussed later, a reliable evaluation of the propagation velocities would be critical. On the other hand, with greater intertransducer distances the distribution of the time differences would be shifted to the right, and time differences would become at least in part greater than the basal intercontractile interval (Fig. ZC). Consequently, slow propagated contractions would be identified either as stationary contractions or as very fast propagated contractions because of a false coordination (Fig. ZC). In the present study, stationary and propagated contractions were identified by a computerized method (16). To differentiate between stationary and propagated contractions, the time differences of the contraction maxima recorded at each of two adjacent transducers were analyzed. As described above, propagated contractions occurring at adjacent transducers produced time differences that were distributed around a mean value. The
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G740
FREQUENCY
AND
Intercontractile
VELOCITY
OF
INTESTINAL
Intercontractile interval
CONTRACTIONS Intercontractile interval
.... .. .. r..:...t.=...A . .. .. .. . . . .. .. . .. .
coordination !
).... . . . . t’. . .. .. .. . .. Ii r.:.:.:.:.~.:.:.:.:.~ ..... t~~~~f$+:.:.:.:.~ ‘~:~:~~~~~:*~~~~:~~ i I. . . . . . . . . . . . .
2.2
Time
(s)
2.2
Time
(s)
0
2.2
Time
(s)
FIG. 2. Choice of the appropriate intertransducer distance for a reliable evaluation of propagation velocities of contractions. Choice of the appropriate distance depended on 2 factors: propagation velocity and basal intercontractile interval. With an appropriate intertransducer distance, time differences of propagated contractions occurring at 2 adjacent transducers were distributed around a mean value (A). Time differences, even the greatest, were clearly less than basal intercontractile interval. Thin dashed lines indicate fastest and slowest propagation velocities corresponding to the limits of the distribution of time differences of propagated contractions. Thick dashed lines indicate mean propagation velocity. With a shorter intertransducer distance, distribution of time differences would be shifted to the left (B), which would complicate the differentiation between simultaneously ocurring and propagated contractions, since very fast propagation velocities would produce very small time differences. With a greater intertransducer distance, distribution of time differences would be shifted to the right. If the intertransducer distance is too large, slow propagation velocities would produce time differences greater than basal intercontractile interval (C). Consequently, slowly propagated contractions would be misinterpreted either as stationary contractions or as fast propagated contractions due to a false coordination (C).
limits of this distribution were used as limits for a time window necessary for the computerized identification of propagated contractions. Consequently, contractions occurring at two adjacent recording sites within the time window were defined as propagated contractions. Stationary contractions were those that occurred out of the time window. Videofluoroscopy confirmed that time differences occurring within the limit of the time window were caused by propagated contractions. In Fig. 3, it is illustrated for each study segment which propagation velocities were admitted by the time window. In the present study, the mean values of the time differences occurring within the defined time window were evaluated for all the adjacent recording sites in each study segment. The propagation velocities of contractions (cm/s) between two adjacent recording sites were calculated by dividing the intertransducer distance by the corresponding mean time difference. Additionally, the intercontractile intervals were analyzed for each recording site in all the study segments. The intercontractile interval was the time (in seconds) elapsed between two consecutive contraction maxima at one recording site. Analysis of the frequency distribution of the intercontractile intervals showed three peaks, which represented at least 85% of all the intercontractile intervals. Within each peak, the intercontractile inter-
vals were distributed around a mean value. In segments 1 and 2, the intercontractile intervals of peak 1 varied from 2.5 to 5.5 s. In the ileum, they varied from 3.0 to 6.5 s. In the present study, the mean values of intercontractile intervals of the first peak were calculated. The mean value ofpeak 1 represented the basal intercontractile interval when the intestine contracted at its maximal rate. The contraction frequency was calculated as the reciprocal of the basal interval in contractions per minute. In RESULTS, the data of the basal intercontractile interval are presented as frequency, indicating the maximal rate of contractions. Code et al. (4) reported that the maximal frequency of contractions is based on the rhythm of the pacesetter potential. Statistics Data are presented as mean values t SE for four dogs. A rank variance analytical test (Friedman’s test) was used to prove if data of each study segment were homogeneous. If statistical significance (P c 0.05) was obtained, values were characterized by a certain rank order. During the postprandial state, the basal intercontractile interval measured at the duodenal bulb (Dl) was excluded from the statistical analysis and from the calculation of the duodenal mean value, because the duodenal bulb exhibited a significantly smaller basal intercontract-
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FREQUENCY DUODENUM-JEJUNUM (segment Intercontractile interval
1)
1
AND JEJUNUM (segment
VELOCITY
OF
INTESTINAL ILEUM
2 1
Intercontractile interval
Intercontractile interval
1
1
cm ~-w-v
t*. ? V’ ‘1 ~~~.\.“. . Cj:::::$.& (.:.;:.:.g:j(.:.> . .. ... ... .. .. - A•.:.:.:.:.:.:~.:~~.~~ Id A
.le interval compared with the other prove if data of the interdigestive and were different, Student’s t test for used. A probability value ~0.05 was cally significant.
G741
CONTRACTIONS
duodenal sites. To postprandial states unpaired data was considered statisti-
,
/
I
/
;’
?,
A U.I. \\
\ br
FIG. 3. Propagation velocities admitted by the defined time window in the 3 different study segments. Contractions occurring within the lower and upper limit (1.1. and u.1.) of the time window at the adjacent aboral transducer were defined as propagated. Dotted areas indicate variations of propagation velocities in each study segment. Thin dashed lines indicate fastest and slowest propagation velocities admitted by the limits of the time window. Variations of the lower and upper limit of the time window because of different variations of the propagation velocity between different adjacent transducers are not indicated. Thick dashed lines represent the fastest and slowest mean propagation velocity measured between 2 adjacent transducers within 1 study segment.
significant faster propagation velocities in the postprandial state only occurred in the jejunal segment 1 (Fig. 4) . Frequencies of Contractions
Phase III of 2MIMC. The frequency of contractions did not show any trend to either increase or decrease along the duodenum (Fig. 4, Table 1). The mean frequency was Propagation Velocities of Contractions 17.8 t 0.12 contractions/min. In contrast to the duodenal Phase III of IMIMC. The propagation velocities of con- segment, contraction frequency decreased slightly (P < tractions progressively increased along the duodenum 0.05) along the jejunal and ileal segments (Fig. 4, Table (Fig. 4, Table 1). In three of four dogs, the maximal 1). The decreases along the intestinal segments were 2% propagation velocity occurred between the duodenal re- in the jejunal segment 1,4% in segment 2, and 4% in the cording sites D4 and D5 (20.5 and 26.5 cm aborad to the ileum (Table 3). pylorus). In one dog, the maximal value was observed Postprandial state. In contrast to the interdigestive between the recording sites D3 and D4 (14.5 and 20.5 cm state, contraction frequencies measured in the postaborad to the pylorus). In the jejunal segments 1 and 2, prandial state did not show any trend to either increase the propagation velocities declined aborally (Fig. 4, Table or decrease along the duodenal and jejunal segments (Fig. 1). Mean values t SE of propagation velocities between 4, Table 1). The mean values of contraction frequencies the first and last two recording sites of each study seg- measured in the duodenum, jejunal segment 1, and segment are given in Table 2. The reduction in the propa- ment 2 were 17.2 t 0.10, 17.3 t 0.11, and 17.2 t 0.17 gation velocities was stronger along the jejunal segment contractions/min, respectively. The contraction fre1 (45%) than segment 2 (20%), although the lengths of quency increased along the ileum (Fig. 4, Tables 1 and the study segments were similar (24.0 and 22.5 cm, 3) . respectively). Lowest values of the propagation velocities Compared with phase III of the MMC, the contraction of contractions were measured in the ileum (Fig. 4). frequency was diminished in each study segment postWithin this segment, the propagation velocities did not prandially (Fig. 4). The difference was significant in the show any trend to either increase or decrease (Table 1). ileum and for some recording sites in the duodenum and The mean propagation velocity of ileal contractions was proximal jejunum (Fig. 4). The difference was most pro0.76 & 0.04 cm/s. nounced in the ileum (Fig. 4). On average, contraction Postprandial state. The behavior of propagation veloc- frequency decreased by 3% in the duodenum, 1% in the ities of contractions within each study segment was jejunal segment 1, 1% in segment 2, and 8% in the ileum. postprandially similar as during phase III (Fig. 4, Table 1) DISCUSSION Compared with phase III, the propagation velocities tended to be faster in the postprandial state (11% in the This study presents for the first time a detailed analyduodenum, 20% in the jejunal segment 1,24% in segment sis of the propagation velocities of contractions in different regions along the canine small intestine. The detailed 2, and 3% in the ileum) (Fig. 4). However, statistically RESI.
LTS
l
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G742
FREQUENCY DUODENUM
-
JEJUNUM (segment
JEJUNUM (segment
1)
AND
VELOCITY
OF
INTESTINAL
CONTRACTIONS
2. Propagation velocities of contractions between the first and last two recording sites of different intestinal segments TABLE
ILEUM 2)
14.2
Propagation of Contractions,
Intestinal Segment Phase
Duodenum Dl-D2 D4-D5 Jejunum 1 51-52 54-55 Jejunum 2 51-52 55-56 Ileum 11-12 16-17
4.8 0.9
0.8 n
lg-
18.5 I\
Values
are means
III
Velocity cm/s Postprandial
6.78t0.65 11.74t1.26
7.71t0.65 14.23t1.88
8.62t0.68 4.75t0.35
9.60t0.78 5.76kO.16
3.90t0.35 3.09t0.21
5.05t0.45 3.38t0.41
0.69t0.03 0.81kO.04
0.75t0.03 0.86t0.04
k SE. Recording
sites are as listed
in Fig. 1.
3. Contraction frequencies at the first and last recording sites of different intestinal segments
TABLE
Contraction Frequency, contractions/min
Intestinal Segment Phase
13.8
12. I
!- .I’ .I”14
I,, .I,, Dl D2D3D4D5
, , , Jl J2 J3 J4 J5
I , , , Jl J2J3J4J5J6 1 22.5cm t
-11
f
24.0cm
2.5cm aborad to pylorus
f
24.0cm
Lig.Treitz
1
*
,
12.7
12.5 I
I
1
,
.
.
.
I1 12 13 14 15 I6 I7 I I 13.2cm f
I
40 cm aborad to Lig.Treitz
2.5cm
orad to ICS
FIG. 4. Propagation velocities (top) and frequencies of contractions (bottom) along 3 different study segments during phase III (solid lines) and the postprandial state (dashed lines). Values are means t SE for 4 dogs. *Statistically significant differences (P < 0.05) between the interdigestive and postprandial state. Figures indicate propagation velocities and frequencies of contractions between the first and last 2 recording sites and at the first and last recording sites, respectively, of each study segment. Abbreviations as in Fig. 1.
1. Behavior of different parameters along different intestinal segments during phase III and the postprandial state TABLE
Propagation Velocity
Intestinal Segment Phase
Duodenum Jejunum 1 Jejunum 2 Ileum
+ 0
III
Contraction Frequency
Postprandial
+ 0
Duodenum Dl D5 Jejunum 1 Jl 55 Jejunum 2 Jl J6 Ileum 11 I7
Phase
0 -
III
Postprandial
0 0 0 +
Plus and minus signs indicate significant trends (P < 0.05) of increasing and decreasing values along an intestinal segment, respectively; 0 indicates that values along an intestinal segment were homogeneous (P > 0.05, Friedman’s test).
characterization of the propagation velocities was achieved by the use of multiple, closely spaced transducers. Results indicate that during both the interdigestive and the postprandial states the propagation velocities of contractions increased from the duodenal bulb to the distal duodenum and then declined in an apparently exponen-
Values
are means
III
Postprandial
17.8t0.11 17.7kO.13
18.5t0.31 17.1t0.14
17.7t0.12 17.4kO.15
17.2t0.10 17.3t0.09
17.7t0.24 17.0t0.25
17.2t0.20 17.2t0.21
13.8t0.08 13.3t0.11
12.5t0.17 12.7kO.19
t SE. Recording
sites are as listed
in Fig. 1.
tial fashion along the jejunum, reaching smallest values in the ileum. The increasing propagation velocities of contractions in the proximal duodenum have already been reported in a previous study (11), but they were not observed by other investigators. There might be several reasons for this difference: first, by the use of only one or two widely spaced transducers one might miss the phenomenon (1, 12), and second, other investigators who used multiple, closely spaced transducers did not evaluate propagation velocities within the duodenal segment (9). The physiological significance of the increase in the propagation velocity along the duodenum remains to be clarified. Previously, McCoy and Baker (12) showed that in the upper small intestine propagation velocities of slow waves declined aborally in a linear fashion. Assuming that the linear decrease in velocity continues aborally, the velocity of slow waves would become zero at a certain region of the jejunum. Since this is unlikely, McCoy and Baker (12) suggested that the velocity might decrease only to a small but finite value. Indeed, our study indicates that propagation velocities of contractions decreased aborally in a nonlinear fashion. The decrease was steepest in the jejunal segment 1 and got smaller in segment 2. In the ileum, propagation velocity was almost
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FREQUENCY
AND
VELOCITY
constant. However, we cannot deduce from our study in which part of the small intestine nearly constant values of propagation velocities were reached. It is noteworthy that velocities of jejunal contractions differed markedly depending on the site of measurement, i.e., from -10 cm/s at the ligament of Treitz to -0.7 cm/s at the end of the jejunum. Propagation velocities of slow waves in the upper jejunum determined in previous studies ranged from 1.8 to 8 cm/s (1,4,X2) and those of ileal slow waves from 0.5 to 0.8 cm/s (1, 4). These values are rather consistent with our results. However, since the propagation velocity declines steeply within the proximal jejunum, values are only comparable when the sites of measurement are exactly defined. The present study shows that the frequencies of contractions were constant or changed only slightly in the proximal intestinal segments. The ileum exhibited markedly lower contraction frequencies than the proximal intestine. Values of contraction frequencies reported in this study are consistent with values (17-20 contractions/min in the duodenum and U-14 contractions/min in the ileum) summarized by Code et al. (4). The almost constant contraction frequency in the proximal small intestine and the markedly lower values in the ileum suggest that the aboral decrease of the contraction frequency occurs in the distal part of the jejunum. Previously, it has been shown that both the intestinal slowwave frequency (56) and the contraction frequency (10) decreased aborally in a stepwise fashion, with variable lengths of intestine having the same frequency. Frequency plateaus have been described to be longer in the upper small intestine than in its distal parts (5, 6, 18). In dogs, it has been found that the proximal frequency plateau was -60-70 cm in length extending through the duodenum into the proximal jejunum, whereas distal frequency plateaus were only a few centimeters in length (6). Additionally, it has been shown that the lengths and positions of the frequency plateaus varied with time (6). In the present study, determination of frequency plateaus was critical because different plateaus might be obscured by averaging values from different recording sessions and different animals. Present and previous findings (5, 6) concerning the behavior of various parameters along the small intestine are summarized schematically in Fig. 5. This figure represents a model to explain the nature of the aboral propagation velocity and frequency gradients. The internal resistance illustrated in Fig. 5 has been calculated from our data of propagation velocities according to the cable equation relating propagation velocity to internal resistance (19). Assuming that all other factors of this equation remain constant, the internal resistance is inversely related to the square of the propagation velocity. It has been suggested (2, 6) that the internal resistance determines the degree of electrical coupling of adjacent muscle cells by modification of the current flow in electrically excitable tissues. There is evidence that both the length of frequency plateaus (7, 14) and the propagation velocity (2) are related to the degree of electrical coupling. As illustrated in Fig. 5, the low internal resistance and, consequently, the high degree of electrical coupling
OF
INTESTINAL
G743
CONTRACTIONS Plateaus in vivo
of frequencies
I I Lig. of Treitz
I
I lleocolic junction
60 cm aborad to Lig. of Treitz
FIG. 5. Schematic model summarizing present concerning the nature of gradients of various small intestine. See text for further details.
and previous findings parameters along the
in the proximal small intestine appear to be responsible for both the long frequency plateau and the high propagation velocity in this region. On the other hand, short frequency plateaus and slow propagation velocities in the distal small intestine might be related to a low degree of electrical coupling. Figure 5 further illustrates that the propagation velocity of contractions decreases along the jejunum and ileum in a more continuous manner, whereas the frequency of contractions decreases in a discontinuous manner. It is likely that the frequency changes abruptly at the end of the plateaus where, because of the increasing internal resistance, the current is of insufficient magnitude to entrain the next slow-wave oscillator, whereas the aborally increasing internal resistance decreases the propagation velocity continuously independent of the frequency plateaus. The aboral decreases in the propagation velocity and the frequency of intestinal contractions appear to be of functional significance for the transport of intestinal content. Code et al. (4) reported that the “wavelength” of the pacesetter potential calculated from the frequency and the propagation velocity decreased from the duodenum to the ileum. Previously it has been shown that the mean length of contraction spread was characterized by a similar gradient (15, 17). It might be possible that the degree of electrical coupling that determines the length of frequency plateaus is also responsible for the length of contraction spread. It is suggested that the long plateau of high frequency, the fast propagation velocity, and the large length of contraction spread in the upper small intestine promote the propulsion of thyme evacuated from the stomach along the small intestine. Decreases in these parameters along the small intestine would then result in a delayed transport of thyme in the distal small intestine. Because the volume of luminal content decreases distally by absorption, it appears reasonable that transport of thyme slows down. The present study shows that along the small intestine the contraction frequencies tended to be shorter and the propagation velocities tended to be greater after administration of an acaloric meal compared with the interdigestive state. These results agree with previous findings
Downloaded from www.physiology.org/journal/ajpgi at Midwestern Univ Lib (132.174.254.157) on February 12, 2019.
G744
FREQUENCY
AND
VELOCITY
indicating an inverse relationship between frequency and propagation velocity (2). We assume that the acaloric content of the small intestine might activate reflexes, producing a decrease in frequency. Because of the inverse relationship between frequency and propagation velocity, this would result postprandially in an increase in propagation velocity. In the proximal small intestine, this postprandial increase in propagation velocity was clearcut, whereas in the ileum a pronounced decrease in contraction frequency after the meal was accompanied only by a slight change in the propagation velocity. Previous studies (2) indicate that the relation between frequency and propagation velocity is not uniform. In the duodenum, a decrease in contraction frequency led to a more pronounced increase in the propagation velocity than in the jejunum (2). Our results support these findings and further indicate that because of the increasing internal resistance along the gut, this relation is almost nonexistent in the ileum. In the present study, different intertransducer distances were used to investigate propagation velocities at different regions of the small intestine. The choice of the appropriate intertransducer distances depended on the propagation velocities and the basal intercontractile intervals. For a reliable identification of propagated contractions and their propagation velocities, time differences of propagated contractions occurring at two adjacent recording sites should be first, shorter than the basal intercontractile interval and second, clearly distinguishable from zero. Intertransducer distances spaced very closely would result in extremely small time differences. Recently, the distribution of time differences of duodenal contractions occurring at transducers 2.5 cm apart were investigated by Engstrom et al. (9). This distribution mainly consisted of positive time differences indicating aboral propagation, but it also consisted of a few negative values; these were interpreted as orally propagated contractions. Since positive and negative time differences belonged to a homogeneous distribution, we assume that the negative time differences might be the result of the relatively small intertransducer distances used in this study. If the intertransducer distances are too small, the maximum of a contraction at the distal transducer might occur slightly earlier than that of a contraction at the oral transducer, since the contraction rise time (time from contraction onset to maximum) is variable. Consequently, negative time differences might be determined despite an aboral propagation of contractions. Because of the aboral decrease in propagation velocity of contractions, the intertransducer distances used in the present study were greater in the duodenum and the adjacent jejunal segment 1 (6 cm) than in the more distal jejunal segment 2 (4.5 cm) and the ileum (2.2 cm). On the other hand, the intertransducer distances should be kept constant within a study segment to allow the evaluation of other motility parameters like the length of contraction spread. Despite the considerable
OF
INTESTINAL
CONTRACTIONS
variations of the propagation velocities in the duodenaljejunal segment, intertransducer distances of -6 cm were appropriate to acquire both the fastest and the slowest propagation velocities occurring in this region. The authors thank Hani Sahyoun for assistance in computer analysis and Ingeborg Ehrlein and Margrit Hartmann for technical assistance. Address for reprint requests: H.-J. Ehrlein, Inst. of Zoophysiology, Div. of Gastrointestinal Physiology, Univ. of Hohenheim, Garbenstr. 30, D-7000 Stuttgart 70, FRG. Received
21 July
1989; accepted
in final
form
12 December
1989.
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