JOURNAL
OF SURGICAL
Motor
RESEARCH
25,
193- 199 (1978)
Function of the Vagally Innervated Antrum following Segmental Gastric Resection in Dogs1
Y. SHIMIZU, M.D. ,2 C. L. NEUSTEIN, M.D., T. PARKER, M.D.,3 T. SEKINE, AND E. R. WOODWARD, M.D. Department
of Surgery,
College of Medicine, Submitted
University
for publication
of Florida,
October
Gainesville,
Florida
M.D.
,4
32610
16, 1977
Resection of the corpus of the stomach in the dog with preservation of the distal vagal innervation results in marked slowing of the pacesetter potential. However, the response to an ingested meal is similar in that a comparable increase in associated action potentials occurs. The segmental gastrectomy dogs indicate an increased rapidity of gastric emptying. This is explained by utilizing isolated innervated antral pouch dogs with later division of the seromuscular connection between body and antrum. Although the same slowing of PSP occurs, there’s a marked increase in contraction pressure. This latter phenomenon probably accounts for the increased rapidity of gastric emptying.
Segmental gastric resection was intro- innervation as compared to gastric transecduced for the surgical treatment of peptic tion of the wall of the stomach on the motility ulcer disease with the intent of excising most of the antrum. of the body of the stomach containing the METHOD majority of the parietal and chief cells. Thus, secretion of acid gastric juice would be reTwo experimental preparations in the dog duced with preservation of the fundus and were utilized and are described as Group 1 antrum. The operation was associated with and 2. a high incidence of recurrence as well as postoperative gastric retention. Wagensteen Group 1 -Segmental Gastrectomy and Ferguson et al. believed that gastric reTwelve mongrel dogs weighing 14.8 to tention resulted from vagal denervation of the pylorus and antrum [2-41. Maki and 21.6 kg were used. Six animals served as the control group while six underwent segassociates showed that abnormal motility developed in the antrum following gastric mental gastrectomy. This procedure was technique transection [7]. In their experiments, how- performed using the following ever, the abnormal motility was not influ- (Fig. 1): The anterior and posterior nerves enced by preservation of antral-vagal inner- of Latarjet were carefully freed from the lesser curvature of the stomach preserving vation. The present study was undertaken to investigate further the effect of vagal the branches to the antrum and pylorus. The stomach was transected at the junction of the antrum and the body of the stomach. 1 This work has been supported in part by NIH grant This point was determined by painting the #AM-13544. mucosa with Congo red dye after an anterior 2 Present address: Jikei University School of Mediwall gastrotomy and after the subcutaneous cine, Department of Surgery, Tokyo, Japan. 3 Present address: Department of Surgery, School of administration of histamine. An estimated Medicine, Vanderbilt University, 21st Avenue South 50% of the stomach was then resected proxiand Garland Avenue, Nashville, Tennessee 37232. mally, effectively removing the body of the 4 Present address: Department of Surgery, Tohoku stomach. The proximal remnant was closed University, School of Medicine, 1 - 1, Seiryo-Cho, from the lesser curvature until the aperture Sendai 980, Japan. 193
0022-4804/78/0253-0193$01.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
194
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
FIG. 1. Operative procedure of segmental gastric resection with vagally innervated antrum. (A) Anterior and posterior nerves of Latajet are freed from lesser curve and the dark area is removed. (B) Closure of the lesser curve and gastrogastrostomy performed.
approximated that of the antrum. End-to end gastrogastrostomy was then performed. In four of the control dogs and five of the experimental group, three bipolar electrodes were sutured to the anterior surface of the antrum along a longitudinal axis. The most proximal electrode (E,) was fixed immediately distal to the junction between body and antrum. The most distal electrode (E3) was placed 2 cm proximal to the pylorus, and the middle electrode (E,) was placed midway between E, and El. Each bipolar electrode consisted of two silver wires 0.7 mm in diameter fixed 0.6 cm apart. The silver wires were soldered to vinyl-insulated copper wires and the soldered junction encased within an acrylic disc. The silver wires projected 2.5 mm from the disc and silver chloride was deposited electrolytically on the tips. Two holes were drilled in the disc through which sutures were passed to anchor the disc to the seromuscular surface of the antrum. The insulated copper wires led to pins of a seven-pin connector which was embedded in a stainless steel cannula filled with dental impression material. The connector end of the cannula was exteriorized through a stab wound in the abdominal wall. Electromyographic studies were performed on the four control and the five experimental dogs which had been fitted with antral electrodes. Animals were fasted for 18hours and were fully awake and resting quietly in
Pavlov stands during each study. Electrodes were connected by leads to a Honeywell G.I. motility system, Model 3300. High and low pass filters were set at 10 and 4 kHz, respectively. The recording speed was 7.5 cm/min. Oscillographic tracings were obtained on three separate occasions in each animal: (1) early postoperatively (second to fourth day); (2) at 2 weeks; and, (3) at 1 month postoperatively. Two 30-min records were made in the fasting state in the early postoperative animal. Two weeks and one month postoperatively the basal recordings were followed by a 420-g horse meat meal and the recording continued for 1 hr postprandially. Normal peristaltic pacesetter potentials (n-PPs) were counted from the E3 lead for 15 min and expressed as the average per minute. The incidence of action potentials was calculated from the same lead as a percentage of the total n-PPs. Gastric emptying was studied in the second postoperative month in both control and experimental animals utilizing a method similar to that reported by Wilbur and Kelly [IO]. Solid plastic spheres of polypropylene measuring 7.14 mm in diameter (Orange Products, N.J.) were made radio-opaque by embedding a small lead pellet in the center. This latter procedure increased the specific gravity to 1.17. Thirty spheres were placed in the dog’s stomach by the tube gavage. X-ray films were made in supine and left
SHIMIZU
ET AL.:
ANTRAL
IAP
MOTOR
FUNCTION
195
TAP
FIG. 2. Schema of isolated antral pouch (IAP) and transected antral pouch (TAP). The IAP and TAP preparations are isolated by double mucosal bridge and by complete transection respectively. In each preparation antrum is vagally innervated. Pylorus is brought to the surface as a cutaneous fistula and gastroduodenostomy is performed.
lateral positions each hour for 4 hr and the number of spheres remaining in the stomach were counted at each interval. Group 2
Eight mongrel dogs weighing 16.5 to 21.O kg were used in this part of the experiment. In four animals an isolated, innervated antral pouch (IAP) was created utilizing a method previously described [ 111.A gastrotomy was made on the greater curvature of the junction of the antrum and body of the stomach and extended approximately onethird the width of the stomach toward the angularis incisura. The antral-corpus border was visualized by the dye technique described above. The mucosa was undermined, transected, and infolded proximally and distally to create a double layer mucosal bridge preserving both the vagal innervation and the integrity of the seromuscular layer. In the remaining four dogs the antrum was completely isolated from the corpus of the stomach to simulate the antrum after segmental gastrectomy (Fig. 2). Before complete transection at the corpus-antrum junction, the nerves of Latarjet were carefully identified and freed in the region of the incisura angularis. The proximal antrum was infolded and closed in two layers and the
divided pylorus brought to the skin as a mucous fistula in the same manner as in the first four animals. Vagal branches to the antrum were carefully preserved. In all eight animals the antrum had three bipolar electrodes placed on the anterior wall exactly as described in the Group 1 animals. After a 3-week recovery period the fasting animals were studied in the unanesthetized state resting quietly in Pavlov frames. Electromyographic tracings were recorded exactly as described in the Group 1 animals. In addition, antral contractions were recorded by inserting a latex balloon through the pyloric fistula. The balloon was inflated with air to a pressure of 50 mm H,O and connected via a low pressure transducer to a Honeywell recording oscillograph, Model 3300. The same volume of air introduced into the extracorporeal balloon resulted in no measurable pressure increase. In all animals vagal innervation of the antrum was established by inducing hypoglycemia with intravenous insulin and recording the characteristic hyperperistaltic response. Electromyography and intraluminal pressures were simultaneously recorded for 30 min in each dog on four separate days. Intraluminal contractions were correlated with the pacesetter potential and associated action potentials. The contraction pressure
196
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
SEGMENTAL
GASTRIC
TWO
DAYS POSTOPERATIVELY
ONE
MONTH
RESECTION
POSTOPERATIVELY
E3 I
1
FIG. 3. Typical electromyographic recordings of the control and segmental gastrectomy dogs in fasting state. Connected &rows show action potentials.
was determined by measuring the amplitude of a contractile wave from base to apex. The transducer-recorder system was standardized before and after each test with a water manometer, and amplitude in miliimeters was converted to contraction pressure in centimeters of water. The motility index was calculated by multiplying the mean amplitude by the frequency.
(Fig. 3) and the frequency was much slower (p < 0.001) than in the control dogs in each
of the three postoperative periods (Fig. 4). In the experimental group the mean frequency was 1.7l/min early postoperatively, increased to 3.72/min (p < 0.001) at 2 weeks, and then decreased again to 2.42lmin at 1 month. The incidence of action potential in the fasting animals appears to be higher in the experimental group during the early RESULTS postoperative study, but this difference did not persist when the two groups were tested Group 1 at 2 weeks and 1 month. Pacesetter potentials were occasionally Electromyographic recordings in the four control dogs indicated normal peristaltic observed discharging from the distal antrum pacesetter potentials which were regular in sometimes propagating distally, sometimes rhythm (Fig. 3) with a consistent frequency proximally, and occasionally in both direcbetween 4.06/min and S.ll/min (Fig. 4). In tions. There were no differences between contrast, n-PPs in the five segmental gas- the control and experimental animals and these were infrequent compared to n-PPs trectomy dogs occurred more irregularly
SHIMIZU ET AL.: ANTRAL MOTOR FUNCTION
(about 5%). These appeared similar to the abnormal PPs referred to by Sugawara as “antiperistalsis” [9]. After ingestion of the horse meat meal the intervals of n-PPs were consistently prolonged in the control dogs. However, the mean frequency of n-PPs calculated every 15 min was significantly less (p < 0.001) in the segmental gastrectomy dogs (Fig. 5). The percentage of n-PPs coupled with action potentials strikingly increased in both groups to over 90% with no significant difference between the two groups. Gastric emptying studies in the control dogs showed that the plastic spheres slowly traveled to the antrum and gradually passed through the pylorus. Approximately twothirds of the spheres remained in the stomach 4 hr after their placement by gavage (Fig. 6). In contrast the experimental group demonstrated one-half of the spheres passed through the pylorus within 1 hr; none of the spheres remained in five of the six dogs at 3 hr. The much more rapid emptying after segmental gastrectomy with vagal preservation is clearly demonstrated.
G Q30 r,
l:rc
l-30)-
0
197
15-30
O-15 TIME
30-45
45-60
(MINUTES)
FIG. 5. Influence of 420 g of horse meat ingestion on the frequency of n-PPs in the control and segmental gastrectomy dogs. Circles represent results at 2 weeks postoperatively while triangles demonstrate results at 1 month. Open figures show control dogs whereas solid figures represent segmental gastrectomy dogs. Vertical lines are SEM.
Group 2
The n-PPs in isolated antral pouches (IAP) appeared with a regular rhythm and a frequency between 3.49/min and 4.97/min (Fig. 7). The frequency of n-PPs in this preparation is similar to that observed in the control animals in Group 1. In transected antral pouches (TAP), however, the n-PPs appeared irregular in rhythm and the mean frequency very slow, between lS9/min and 3.08/min. This is very similar to the frequency observed in the fasting Group 1 animals which had had segmental gastrectomy. The mean contraction pressure measured in the antral lumen during peristaltic activity was strikingly higher (p < 0.001) in TAP as contrasted with the IAP preparation. The changes in frequency were the reverse of those observed with contraction pressure with the net result that the motility index between the two preparations was no different. DISCUSSION
Segmental gastrectomy has not been widely utilized in the surgical treatment of 2-4 DAYS 2 WEEKS 4 WEEKS peptic ulcer. Ferguson et al. demonstrated, however, that the complication of delayed FIG. 4. Mean frequencies of n-PPs during fasting state. Open circles are means of control dogs, and gastric emptying can be obviated by preservclosed circles are means of segmental gastrectomy dogs. ing the antral vagal branches [4]. In the
198
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
t,
i
i TIME
~7
3
4
(HOURS)
FIG. 6. Gastric emptying of plastic spheres. Open circles represent control animals and closed circles segmental gastrectomy dogs. Vertical bars represent SEM.
et al. found a similar slowing of the peristaltic pacesetter potentials after transverse myomectomy [ 11.It has been demonstrated that the gastric pacemaker is in the orad corpus near the greater curvature [5]. Segmental gastrectomy probably removed most if not all of the pacemaker area. The n-PPs after segmental gastrectomy are probably generated by new or ectopic pacemakers located either in the proximal antrum or distal fundus. The change in regularity and rate of the n-PPs is the apparent result. Action * potentials stimulated by food ingestion are 40readily activated even in the absence of the normal pacemaker area of the corpus. 30In the isolated antral pouch preparation complete transection of the gastric wall with 0, vagal preservation produced the same = 20. : changes in the pacesetter potential observed in the animals with segmental gastrectomy IOand vagal preservation, i.e., irregular rhythm and markedly slowed frequency. However, L , measurements of intraluminal contraction I 2 3 4 5 pressure showed a striking increase after CYCLES PER MINUTE total transection from the gastric wall. Even FIG. 7. Frequency and contraction pressure of IAP (open circle) and TAP preparation (closed though the frequency was markedly reduced circle). Horizontal and vertical bars indicate standard the very significant increase in peristaltic deviation. strength probably accounts for the more
present study resection of the body of the stomach with preservation of vagal innervation to the antrum and pylorus demonstrates that in the dog gastric emptying as measured with plastic spheres is actually faster than in control dogs. Electromyographic recordings of the antrum demonstrated that normal peristaltic pacesetter potentials had a more irregular rhythm and a much slower frequency after segmental gastrectomy. Bedi
SHIMIZU ET AL.: ANTRAL MOTOR FUNCTION
rapid emptying observed in the animals with segmental gastrectomy. This correlates well with the study of Okabayashi who reported higher contraction pressure after gastric transection in the dog [8]. The hyperistalsis occurs after gastric transection despite preservation of the vagal innervation indicating that this is not a phenomenon of vagal denervation. This appears to be a phenomenon characteristic of either separation from or removal of the normal gastric pacemaker area in the orad corpus. REFERENCES 1. Bedi, B. S., Kelly, K. A., and Holley, K. E. Pathways of propagation of the canine gastric pace63: 288, 1972. setter potential. Gastroenterology 2. Code, C. F., and Carlson, H. C. Motor activity of the stomach. In C. F. Code, (Ed.), Hundbook of Physiology, p. 1903.American Physiological Society, Washington, D.C., 1968. 3. Cooke, A. R., and Grossman, M. I. Studies on the secretion and motility of Brunner’s gland pouches. Gautroenterology 51: 506, 1966. 4. Ferguson, D. J.. Billing, H., Swensen, D., and
199
Hoover, G. Segmental gastrectomy with innervated antrum for duodenal ulcer. Surgery 47: 548, 1960. 5. Kelly, K. A., Code, C. F., and Elveback, L. R. Patterns of canine gastric electrical activity. Amer. J. Physiol. 217: 461, 1969. 6, Kelly, K. A., and La Force, R. C. Pacing the canine stomach with electric stimulation. Amer. J. Physiol.
222: 588, 1972.
7. Maki, T., Shiratori, T., Hatafuku, T., and Sugawara, K. Pylorus-preserving gastrectomy as an improved operation for gastric ulcer. Surgery 61: 838, 1967.
s, Okabayashi, T. Manometric and electromyographic studies on the effect of transection of canine stomach on the pyloric motor function. Japan. J. Smooth Muscle Revs. 3: 70, 1967. 9. Sugawara. K. An electromyographic study on the
motility of canine stomach after transection and end-to-end anastomosis. Tohoku J. Exp. Med. 84: 113, 1964.
10. Wilbur, B. G., and Kelly, K. A. Effect of proximal gastric, complete gastric, and truncal vagotomy on canine gastric electric activity, motility and emptying. Ann. Surg. 178: 295, 1973. 11. Woodward, E. R., Lyon, E. S., Landor, J., and Dragstedt, L. R. The physiology of the gastric antrum. Experimental studies on isolated antrum pouches in dogs. Gustroenterolo,gy 27: 766, 1954.
OF SURGICAL
Motor
RESEARCH
25,
193- 199 (1978)
Function of the Vagally Innervated Antrum following Segmental Gastric Resection in Dogs1
Y. SHIMIZU, M.D. ,2 C. L. NEUSTEIN, M.D., T. PARKER, M.D.,3 T. SEKINE, AND E. R. WOODWARD, M.D. Department
of Surgery,
College of Medicine, Submitted
University
for publication
of Florida,
October
Gainesville,
Florida
M.D.
,4
32610
16, 1977
Resection of the corpus of the stomach in the dog with preservation of the distal vagal innervation results in marked slowing of the pacesetter potential. However, the response to an ingested meal is similar in that a comparable increase in associated action potentials occurs. The segmental gastrectomy dogs indicate an increased rapidity of gastric emptying. This is explained by utilizing isolated innervated antral pouch dogs with later division of the seromuscular connection between body and antrum. Although the same slowing of PSP occurs, there’s a marked increase in contraction pressure. This latter phenomenon probably accounts for the increased rapidity of gastric emptying.
Segmental gastric resection was intro- innervation as compared to gastric transecduced for the surgical treatment of peptic tion of the wall of the stomach on the motility ulcer disease with the intent of excising most of the antrum. of the body of the stomach containing the METHOD majority of the parietal and chief cells. Thus, secretion of acid gastric juice would be reTwo experimental preparations in the dog duced with preservation of the fundus and were utilized and are described as Group 1 antrum. The operation was associated with and 2. a high incidence of recurrence as well as postoperative gastric retention. Wagensteen Group 1 -Segmental Gastrectomy and Ferguson et al. believed that gastric reTwelve mongrel dogs weighing 14.8 to tention resulted from vagal denervation of the pylorus and antrum [2-41. Maki and 21.6 kg were used. Six animals served as the control group while six underwent segassociates showed that abnormal motility developed in the antrum following gastric mental gastrectomy. This procedure was technique transection [7]. In their experiments, how- performed using the following ever, the abnormal motility was not influ- (Fig. 1): The anterior and posterior nerves enced by preservation of antral-vagal inner- of Latarjet were carefully freed from the lesser curvature of the stomach preserving vation. The present study was undertaken to investigate further the effect of vagal the branches to the antrum and pylorus. The stomach was transected at the junction of the antrum and the body of the stomach. 1 This work has been supported in part by NIH grant This point was determined by painting the #AM-13544. mucosa with Congo red dye after an anterior 2 Present address: Jikei University School of Mediwall gastrotomy and after the subcutaneous cine, Department of Surgery, Tokyo, Japan. 3 Present address: Department of Surgery, School of administration of histamine. An estimated Medicine, Vanderbilt University, 21st Avenue South 50% of the stomach was then resected proxiand Garland Avenue, Nashville, Tennessee 37232. mally, effectively removing the body of the 4 Present address: Department of Surgery, Tohoku stomach. The proximal remnant was closed University, School of Medicine, 1 - 1, Seiryo-Cho, from the lesser curvature until the aperture Sendai 980, Japan. 193
0022-4804/78/0253-0193$01.00/O Copyright 0 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
194
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
FIG. 1. Operative procedure of segmental gastric resection with vagally innervated antrum. (A) Anterior and posterior nerves of Latajet are freed from lesser curve and the dark area is removed. (B) Closure of the lesser curve and gastrogastrostomy performed.
approximated that of the antrum. End-to end gastrogastrostomy was then performed. In four of the control dogs and five of the experimental group, three bipolar electrodes were sutured to the anterior surface of the antrum along a longitudinal axis. The most proximal electrode (E,) was fixed immediately distal to the junction between body and antrum. The most distal electrode (E3) was placed 2 cm proximal to the pylorus, and the middle electrode (E,) was placed midway between E, and El. Each bipolar electrode consisted of two silver wires 0.7 mm in diameter fixed 0.6 cm apart. The silver wires were soldered to vinyl-insulated copper wires and the soldered junction encased within an acrylic disc. The silver wires projected 2.5 mm from the disc and silver chloride was deposited electrolytically on the tips. Two holes were drilled in the disc through which sutures were passed to anchor the disc to the seromuscular surface of the antrum. The insulated copper wires led to pins of a seven-pin connector which was embedded in a stainless steel cannula filled with dental impression material. The connector end of the cannula was exteriorized through a stab wound in the abdominal wall. Electromyographic studies were performed on the four control and the five experimental dogs which had been fitted with antral electrodes. Animals were fasted for 18hours and were fully awake and resting quietly in
Pavlov stands during each study. Electrodes were connected by leads to a Honeywell G.I. motility system, Model 3300. High and low pass filters were set at 10 and 4 kHz, respectively. The recording speed was 7.5 cm/min. Oscillographic tracings were obtained on three separate occasions in each animal: (1) early postoperatively (second to fourth day); (2) at 2 weeks; and, (3) at 1 month postoperatively. Two 30-min records were made in the fasting state in the early postoperative animal. Two weeks and one month postoperatively the basal recordings were followed by a 420-g horse meat meal and the recording continued for 1 hr postprandially. Normal peristaltic pacesetter potentials (n-PPs) were counted from the E3 lead for 15 min and expressed as the average per minute. The incidence of action potentials was calculated from the same lead as a percentage of the total n-PPs. Gastric emptying was studied in the second postoperative month in both control and experimental animals utilizing a method similar to that reported by Wilbur and Kelly [IO]. Solid plastic spheres of polypropylene measuring 7.14 mm in diameter (Orange Products, N.J.) were made radio-opaque by embedding a small lead pellet in the center. This latter procedure increased the specific gravity to 1.17. Thirty spheres were placed in the dog’s stomach by the tube gavage. X-ray films were made in supine and left
SHIMIZU
ET AL.:
ANTRAL
IAP
MOTOR
FUNCTION
195
TAP
FIG. 2. Schema of isolated antral pouch (IAP) and transected antral pouch (TAP). The IAP and TAP preparations are isolated by double mucosal bridge and by complete transection respectively. In each preparation antrum is vagally innervated. Pylorus is brought to the surface as a cutaneous fistula and gastroduodenostomy is performed.
lateral positions each hour for 4 hr and the number of spheres remaining in the stomach were counted at each interval. Group 2
Eight mongrel dogs weighing 16.5 to 21.O kg were used in this part of the experiment. In four animals an isolated, innervated antral pouch (IAP) was created utilizing a method previously described [ 111.A gastrotomy was made on the greater curvature of the junction of the antrum and body of the stomach and extended approximately onethird the width of the stomach toward the angularis incisura. The antral-corpus border was visualized by the dye technique described above. The mucosa was undermined, transected, and infolded proximally and distally to create a double layer mucosal bridge preserving both the vagal innervation and the integrity of the seromuscular layer. In the remaining four dogs the antrum was completely isolated from the corpus of the stomach to simulate the antrum after segmental gastrectomy (Fig. 2). Before complete transection at the corpus-antrum junction, the nerves of Latarjet were carefully identified and freed in the region of the incisura angularis. The proximal antrum was infolded and closed in two layers and the
divided pylorus brought to the skin as a mucous fistula in the same manner as in the first four animals. Vagal branches to the antrum were carefully preserved. In all eight animals the antrum had three bipolar electrodes placed on the anterior wall exactly as described in the Group 1 animals. After a 3-week recovery period the fasting animals were studied in the unanesthetized state resting quietly in Pavlov frames. Electromyographic tracings were recorded exactly as described in the Group 1 animals. In addition, antral contractions were recorded by inserting a latex balloon through the pyloric fistula. The balloon was inflated with air to a pressure of 50 mm H,O and connected via a low pressure transducer to a Honeywell recording oscillograph, Model 3300. The same volume of air introduced into the extracorporeal balloon resulted in no measurable pressure increase. In all animals vagal innervation of the antrum was established by inducing hypoglycemia with intravenous insulin and recording the characteristic hyperperistaltic response. Electromyography and intraluminal pressures were simultaneously recorded for 30 min in each dog on four separate days. Intraluminal contractions were correlated with the pacesetter potential and associated action potentials. The contraction pressure
196
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
SEGMENTAL
GASTRIC
TWO
DAYS POSTOPERATIVELY
ONE
MONTH
RESECTION
POSTOPERATIVELY
E3 I
1
FIG. 3. Typical electromyographic recordings of the control and segmental gastrectomy dogs in fasting state. Connected &rows show action potentials.
was determined by measuring the amplitude of a contractile wave from base to apex. The transducer-recorder system was standardized before and after each test with a water manometer, and amplitude in miliimeters was converted to contraction pressure in centimeters of water. The motility index was calculated by multiplying the mean amplitude by the frequency.
(Fig. 3) and the frequency was much slower (p < 0.001) than in the control dogs in each
of the three postoperative periods (Fig. 4). In the experimental group the mean frequency was 1.7l/min early postoperatively, increased to 3.72/min (p < 0.001) at 2 weeks, and then decreased again to 2.42lmin at 1 month. The incidence of action potential in the fasting animals appears to be higher in the experimental group during the early RESULTS postoperative study, but this difference did not persist when the two groups were tested Group 1 at 2 weeks and 1 month. Pacesetter potentials were occasionally Electromyographic recordings in the four control dogs indicated normal peristaltic observed discharging from the distal antrum pacesetter potentials which were regular in sometimes propagating distally, sometimes rhythm (Fig. 3) with a consistent frequency proximally, and occasionally in both direcbetween 4.06/min and S.ll/min (Fig. 4). In tions. There were no differences between contrast, n-PPs in the five segmental gas- the control and experimental animals and these were infrequent compared to n-PPs trectomy dogs occurred more irregularly
SHIMIZU ET AL.: ANTRAL MOTOR FUNCTION
(about 5%). These appeared similar to the abnormal PPs referred to by Sugawara as “antiperistalsis” [9]. After ingestion of the horse meat meal the intervals of n-PPs were consistently prolonged in the control dogs. However, the mean frequency of n-PPs calculated every 15 min was significantly less (p < 0.001) in the segmental gastrectomy dogs (Fig. 5). The percentage of n-PPs coupled with action potentials strikingly increased in both groups to over 90% with no significant difference between the two groups. Gastric emptying studies in the control dogs showed that the plastic spheres slowly traveled to the antrum and gradually passed through the pylorus. Approximately twothirds of the spheres remained in the stomach 4 hr after their placement by gavage (Fig. 6). In contrast the experimental group demonstrated one-half of the spheres passed through the pylorus within 1 hr; none of the spheres remained in five of the six dogs at 3 hr. The much more rapid emptying after segmental gastrectomy with vagal preservation is clearly demonstrated.
G Q30 r,
l:rc
l-30)-
0
197
15-30
O-15 TIME
30-45
45-60
(MINUTES)
FIG. 5. Influence of 420 g of horse meat ingestion on the frequency of n-PPs in the control and segmental gastrectomy dogs. Circles represent results at 2 weeks postoperatively while triangles demonstrate results at 1 month. Open figures show control dogs whereas solid figures represent segmental gastrectomy dogs. Vertical lines are SEM.
Group 2
The n-PPs in isolated antral pouches (IAP) appeared with a regular rhythm and a frequency between 3.49/min and 4.97/min (Fig. 7). The frequency of n-PPs in this preparation is similar to that observed in the control animals in Group 1. In transected antral pouches (TAP), however, the n-PPs appeared irregular in rhythm and the mean frequency very slow, between lS9/min and 3.08/min. This is very similar to the frequency observed in the fasting Group 1 animals which had had segmental gastrectomy. The mean contraction pressure measured in the antral lumen during peristaltic activity was strikingly higher (p < 0.001) in TAP as contrasted with the IAP preparation. The changes in frequency were the reverse of those observed with contraction pressure with the net result that the motility index between the two preparations was no different. DISCUSSION
Segmental gastrectomy has not been widely utilized in the surgical treatment of 2-4 DAYS 2 WEEKS 4 WEEKS peptic ulcer. Ferguson et al. demonstrated, however, that the complication of delayed FIG. 4. Mean frequencies of n-PPs during fasting state. Open circles are means of control dogs, and gastric emptying can be obviated by preservclosed circles are means of segmental gastrectomy dogs. ing the antral vagal branches [4]. In the
198
JOURNAL OF SURGICAL RESEARCH: VOL. 25, NO. 3, SEPTEMBER 1978
t,
i
i TIME
~7
3
4
(HOURS)
FIG. 6. Gastric emptying of plastic spheres. Open circles represent control animals and closed circles segmental gastrectomy dogs. Vertical bars represent SEM.
et al. found a similar slowing of the peristaltic pacesetter potentials after transverse myomectomy [ 11.It has been demonstrated that the gastric pacemaker is in the orad corpus near the greater curvature [5]. Segmental gastrectomy probably removed most if not all of the pacemaker area. The n-PPs after segmental gastrectomy are probably generated by new or ectopic pacemakers located either in the proximal antrum or distal fundus. The change in regularity and rate of the n-PPs is the apparent result. Action * potentials stimulated by food ingestion are 40readily activated even in the absence of the normal pacemaker area of the corpus. 30In the isolated antral pouch preparation complete transection of the gastric wall with 0, vagal preservation produced the same = 20. : changes in the pacesetter potential observed in the animals with segmental gastrectomy IOand vagal preservation, i.e., irregular rhythm and markedly slowed frequency. However, L , measurements of intraluminal contraction I 2 3 4 5 pressure showed a striking increase after CYCLES PER MINUTE total transection from the gastric wall. Even FIG. 7. Frequency and contraction pressure of IAP (open circle) and TAP preparation (closed though the frequency was markedly reduced circle). Horizontal and vertical bars indicate standard the very significant increase in peristaltic deviation. strength probably accounts for the more
present study resection of the body of the stomach with preservation of vagal innervation to the antrum and pylorus demonstrates that in the dog gastric emptying as measured with plastic spheres is actually faster than in control dogs. Electromyographic recordings of the antrum demonstrated that normal peristaltic pacesetter potentials had a more irregular rhythm and a much slower frequency after segmental gastrectomy. Bedi
SHIMIZU ET AL.: ANTRAL MOTOR FUNCTION
rapid emptying observed in the animals with segmental gastrectomy. This correlates well with the study of Okabayashi who reported higher contraction pressure after gastric transection in the dog [8]. The hyperistalsis occurs after gastric transection despite preservation of the vagal innervation indicating that this is not a phenomenon of vagal denervation. This appears to be a phenomenon characteristic of either separation from or removal of the normal gastric pacemaker area in the orad corpus. REFERENCES 1. Bedi, B. S., Kelly, K. A., and Holley, K. E. Pathways of propagation of the canine gastric pace63: 288, 1972. setter potential. Gastroenterology 2. Code, C. F., and Carlson, H. C. Motor activity of the stomach. In C. F. Code, (Ed.), Hundbook of Physiology, p. 1903.American Physiological Society, Washington, D.C., 1968. 3. Cooke, A. R., and Grossman, M. I. Studies on the secretion and motility of Brunner’s gland pouches. Gautroenterology 51: 506, 1966. 4. Ferguson, D. J.. Billing, H., Swensen, D., and
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Hoover, G. Segmental gastrectomy with innervated antrum for duodenal ulcer. Surgery 47: 548, 1960. 5. Kelly, K. A., Code, C. F., and Elveback, L. R. Patterns of canine gastric electrical activity. Amer. J. Physiol. 217: 461, 1969. 6, Kelly, K. A., and La Force, R. C. Pacing the canine stomach with electric stimulation. Amer. J. Physiol.
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7. Maki, T., Shiratori, T., Hatafuku, T., and Sugawara, K. Pylorus-preserving gastrectomy as an improved operation for gastric ulcer. Surgery 61: 838, 1967.
s, Okabayashi, T. Manometric and electromyographic studies on the effect of transection of canine stomach on the pyloric motor function. Japan. J. Smooth Muscle Revs. 3: 70, 1967. 9. Sugawara. K. An electromyographic study on the
motility of canine stomach after transection and end-to-end anastomosis. Tohoku J. Exp. Med. 84: 113, 1964.
10. Wilbur, B. G., and Kelly, K. A. Effect of proximal gastric, complete gastric, and truncal vagotomy on canine gastric electric activity, motility and emptying. Ann. Surg. 178: 295, 1973. 11. Woodward, E. R., Lyon, E. S., Landor, J., and Dragstedt, L. R. The physiology of the gastric antrum. Experimental studies on isolated antrum pouches in dogs. Gustroenterolo,gy 27: 766, 1954.
