The ideal post-gastrectomy reconstruction procedure should maintain the normal digestive function and restore intestinal transit to improve the patient quality of life. Creating a gastric reservoir has been found to keep a low speed of the food passage in the upper intestinal tract and retain the food storage volume, and increasing evidence from randomized controlled clinical studies reveals that establishing a jejunal reservoir improves the post-operation food capacity and nutritional status.1,2
Several studies have shown that the presence of post-prandial hyperglycemia may indicate an abnormal glucose metabolism, possibly representing glucose intolerance or an early stage of diabetes.3 Post-challenge hyperglycemia after an oral glucose tolerance test (OGTT) is an appropriate model of post-prandial hyperglycemia, and it represents a phenotype of early-stage overt diabetes.4 After a subtotal or total gastrectomy, a liquid diet flows promptly from the stomach or the esophagus into the duodenum or the jejunum, resulting in the immediate absorption of glucose from the intestine and the development of postprandial hyperglycemia. A previous study demonstrated significantly higher blood glucose and insulin levels after the OGTT in distal gastrectomy patients compared with those in a control group.5
Gastric motility is controlled by gastric electrical activity (GEA); alterations in GEA synchronization can cause various abnormalities in the gastric motor function.6,7 The myoelectric and transit abnormalities that can occur during restorative operations are caused by a variety of factors, including altered propagation of more than 50% of the time,8 a loss of myoneural continuity between the duodenal pacemaker and the limb, and a decreased frequency of the pacesetter potentials (PPs) in the Roux limb and distally.9 Interestingly, the myoelectric irregularities observed in conventional Roux patients were caused by the jejunal transaction, not by the gastrectomy or vagotomy.10
In our previous studies, we developed a reconstruction procedure, the continual jejunal interposition, for digestive tract reconstruction after subtotal distal gastrectomy. Our data demonstrated that continual jejunal interposition after subtotal distal gastrectomy can recover the physiological continuity of the digestive tract and improve the quality of life without reflux gastritis.11 We previously assessed the clinical utility of jejunal pouch interposition from the standpoint of postoperative symptoms, changes in body weight, and changes in the prognosis nutrition index (PNI), and we confirmed its high utility.12 However, no detailed analysis has been published concerning the physiological changes of the jejunal pouch reconstructed after subtotal distal gastrectomy. Therefore, we evaluated the effects of currently used alimentary reconstruction procedures (integral continual jejunal interposition, Billroth I, Billroth II, and isolated jejunal interposition) after subtotal gastrectomy on the postoperative myoelectrical activity and nutritional parameters, including the blood glucose, insulin responses, routine blood parameters, liver function, and myoelectrical activity, in Beagle dogs.
Thirty-two beagle dogs weighing 7.5–9.5 kg were randomly divided into four groups that underwent subtotal distal gastrectomy combined with one of four reconstruction procedures. After fasting for 24 hours, anesthesia was induced by venous injection of 0.3 ml/kg of 5% pentobarbital and intramuscular injection of 10 mg/kg of ketamine and was maintained by inhalation of 1%–2% isoflurane gas in 100% oxygen. Venous access was obtained, and then the operation was performed aseptically under general anesthesia with tracheal intubation.
The transection line of the stomach connected the bifurcating point of the right side of the first descending branch of the left gastric artery on the lesser curvature and that of the left side of first vertical branch of the left gastroepiploic artery on the greater curvature. Four alimentary reconstruction procedures were performed after subtotal distal gastrectomy. For the integral continual jejunal interposition (n
=9; Figure 1), the procedure was as follows. First, an end-to-side gastrojejunostomy was performed at 20 cm anal to Treitz’s ligament. Then an end-to-side duodenojejunostomy was created at the efferent limb 30 cm distal to the gastrojejunostomy, followed by a side-to-side jejunostomy at 10 cm distal to the duodenojejunostomy and 15 cm distal to Treitz’s ligament. Finally, two jejunal proper ligations were made at 2 cm oral to the gastrojejunostomy and 5 cm distal to the duodenojejunostomy. The two ligations blockade food and liquid through the jejunum, but supply of blood was normal. For the Billroth I procedure (n
=7), an end-to-end gastrojejunostomy was performed. In the Billroth II procedure (n
=7), the duodenal stump was closed, and an antecolic end-to-side gastrojejunostomy was performed at 25–30 cm anal from Treitz’s ligament. In the isolated jejunal interposition
=9), a pedicled jejunal strip of approximately 25-cm long was collected from approximately 30 cm distal to the ligament of Treitz to prepare a jejunal pouch, while attention was paid to the artery supplying blood to the ligament. The pedicled jejunal strip was elevated before the colon, and an end-to-end gastrojejunostomy was first performed at 30 cm anal to Treitz’s ligament. Then an end-to-end duodenojejunostomy was created at the efferent limb 25 cm distal to the gastrojejunostomy, followed by an end-to-end jejunostomy.
After the integral continual jejunal interposition and the isolated jejunal interposition, bipolar electrical leads were placed on the serosal surface of the remnant stomach (3 cm from the gastrojejunostomy anastomosis), on the jejunal interposition (3 cm from the duodenojejunostomy anastomosis and the gastrojejunostomy anastomosis) and on the duodenal stump (3 cm from the duodeno- jejunostomy anastomosis; Figure 1). After the Billroth II procedure, bipolar electrical leads were placed on the serosal surface of the remnant stomach (3 cm from the gastrojejunostomy anastomosis), on the afferent loop and efferent loop (3 cm from the duodenojejunostomy anastomosis and the gastrojejunostomy anastomosis, respectively) and on the duodenal stump (3 cm from the duodenojejunostomy anastomosis). After the Billroth I procedure, bipolar electrical leads were placed on the serosal surface of the remnant stomach and duodenal stump (3 cm from the gastroduodenal anastomosis). The ends of the electrodes in all groups were covered with a Teflon patch to insulate them from the adjacent loops of bowel. The distance between the two electrodes was 5 mm. The free ends were extracted in a transcutaneous fashion through the flanks of the animals.
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Figure 1. Integral continual jejunal interposition. Gastrojejunostomy (A), duodenojejunostomy (B), side-to-side jejunostomy (C), Treitz’s ligament (D), and (E) and (F) the ligation sites. a: bipolar electrical leads were placed on the serosal surface of the remnant stomach (3 cm from the gastrojejunostomy anastomosis); b and c: bipolar electrical leads were placed at the jejunal interposition (3 cm from the duodenojejunostomy anastomosis and the gastrojejunostomy anastomosis); d: bipolar electrical leads were placed at the duodenal stump (3 cm from the duodenojejunostomy anastomosis).
The animals were fasted (no food and water) for 72 hours postoperatively. During this period, they received a maintenance infusion of 5% glucose and sodium chloride brine (40 ml/kg) containing antibiotics. After 72 hours, dogs were permitted water and liquid food, and the amount was increased depending on the animal’s condition. It became possible for all animals to eat a normal meal (commercially available dog food, 120 g/day) by approximately two weeks after surgery. Two dogs in the isolated jejunal interposition group died from peritonitis after 1 week.
The body weights of the dogs were measured before the operation and at 1, 4, 8, and 12 weeks after operation. Routine blood parameters (white blood cell, red blood cell, hemoglobin, and absolute lymphocyte counts, among others) and liver function (total protein, albumin, cholesterol, and triglyceride concentrations, among others) were analyzed before the operation and at 2, 4, and 8 weeks after operation. Animals were fasted for 16 hours before each experiment. The routine blood parameters were determined using a completely automatic blood cell count analyzer (Beckman-Coulter MAXM, USA). Liver function was determined using a completely automatic biochemistry analyzer (Beckman-Coulter SYNCHRON LX 20). The PNI was calculated as follows: PNI
= 10 ´ serum albumin (g/100 ml) + 0.005 ´ total lymphocyte count/mm3
of peripheral blood.13
OGTT and the detection of insulin
OGTT was performed on eight animals before the operation and on each animal at 6 weeks after operation. Animals were fasted for 16 hours before the experiment. Fifty-percent glucose (2.5 g/kg body weight) was delivered via gavage, which was placed in each animal’s mouth to ensure the uniformity of the delivered dose. The samples for the glucose and insulin were taken at 0, 30, 60, 90, 120, 150, and 180 minutes were drawn. Sera from these animals were analyzed for serum glucose values and insulin levels. The resulting glucose levels were used as the baseline value for the fasting blood glucose and insulin in the study. The plasma glucose concentration was determined by the glucose dehydrogenase method using a completely automatic biochemistry analyzer (Beckman-Coulter SYNCHRON LX 20). The plasma insulin level was determined by enzyme-linked immunosorbent assay with chemiluminescence using a chemiluminescence instrument (ADVIA Centaur, USA).
A 6-week recovery period was allowed after the completion of each operative procedure. The animals were fasted for 16 hours and then placed in a canvas sling. Electrical activity was recorded using an amplifier and pen recorder Medlab6 (Nanjing, China). The fasting myoelectric activity was recorded for 60 minutes to determine the baseline pattern of PPs, and postprandial recordings of electrical activity were continued for 60 minutes.
The PPs were examined for frequency, and the aboral propagation percentage was estimated by a visual analysis of the 1-minute sample taken every ten minutes during fasting and postprandially. Aboral propagation was considered to be present if the appearance of PPs between adjacent electrodes occurred at time reported previously.14,15 Each 1-minute period analyzed represented the corresponding 10-minute period. The direction of PP propagation was then noted to be aboral, oral, or indeterminate. Indeterminate propagation was deemed as present when less than two thirds of the PPs showed consistent propagation across all electrodes. A postmortem examination was performed on each dog after the completion of all tests.
The SPSS 12.0 software (SPSS Inc., IL, USA) was used for data comparisons. Statistical significance was analyzed by a factorial analysis of variance (ANOVA) for the series of blood glucose and insulin values over time and by a one-way ANOVA for the integrated secretions. The integrated secretions were calculated as the area under the hormone concentration curve. The myoelectric factors were obtained for each experimental condition. The Student’s t-test for paired samples was used. The results are expressed as the means ± standard error. Differences with P values less than 0.05 were considered significant.
The dogs in the Billroth I, Billroth II, integral continual jejunal interposition, and isolated jejunal interposition groups recovered to a normal diet after (8.13±0.99), (8.88±0.64), (9.38±0.92), and (10.50±1.20) days post-operation, respectively. The times required for the recovery to a normal diet for the integral continual jejunal interposition and isolated jejunal interposition groups were longer than those for the Billroth I and II groups, and there were significant differences among the four groups (P <0.05).
The weight of the dogs decreased during the first post-operative weeks; however, dogs in the integral continual jejunal interposition, Billroth I, and Billroth II groups gained significantly more weight by 8 weeks compared to the isolated jejunal interposition group (P <0.05). Dogs in the integral continual jejunal interposition group gained significantly more weight by 12 weeks compared to the Billroth I, Billroth II, and isolated jejunal interposition groups (P <0.05; Figure 2).
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Figure 2. Comparison of the weights of dogs after the four digestive tract reconstruction procedures following subtotal gastrectomy.
The PNI of the dogs decreased during the first 2 post-operative weeks and then increased significantly by four weeks in the integral continual jejunal interposition (P <0.05) and Billroth I groups compared to the Billroth II and isolated jejunal interposition groups. However, the PNI of the dogs decreased during the first 4 post-operative weeks and then increased in the isolated jejunal interposition and Billroth II groups (Figure 3).
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Figure 3. Comparison of the prognosis nutrition index (PNI) among four digestive tract reconstruction procedures after subtotal gastrectomy.
Glucose levels after the four digestive tract reconstruction procedures following subtotal gastrectomy
Figure 4 demonstrates the blood glucose levels in the five groups during the meal provocation test. The glucose curve for the controls was flat, while for the operated dogs, it reached higher values. The curves look diabetoid, most prominently for the Billroth II group. The factorial analysis of variance found a significant difference between the four groups and the normal control group. The group with the duodenal exclusion (Billroth II) had significantly higher glucose levels compared to the normal control group (P <0.05). There were no significant differences between the integral continual jejunal interposition and Billroth I groups and the control group.
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Figure 4. The glucose levels after the four digestive tract reconstruction procedures following subtotal gastrectomy.
Insulin level after the four digestive tract reconstruction procedures following subtotal gastrectomy
The insulin level increased to abnormally high values in all four gastrectomized groups in response to food stimulus compared to the healthy controls (Figure 5). The basal values did not differ among the five groups. The insulin curve was much higher in the dogs with a preserved duodenal passage (Billroth I, continual jejunal interposition, and isolated jejunal interposition). The factorial ANOVA showed that the curves differed significantly according to the type of groups. The results were significantly different between the normal and preserved duodenal passage groups (P <0.05; Billroth I, continual jejunal interposition, and isolated jejunal interposition) and between the normal and the Billroth II group (P <0.05).
Fasting myoelectric activity
In all groups, the electrical control activity with a frequency of approximately 5 cycles/min was recorded from the electrodes on the gastric remnant. The frequencies of fasting jejunal PPs were greater in the integral continual jejunal interposition ((15.0±0.5) cycles/min) and Billroth I ((14.5±0.6) cycles/min) groups than in the isolated jejunal interposition ((10.3±0.7) cycles/min) and Billroth II ((11.0±0.4) cycles/min) groups (P <0.05). The percentage of aboral propagation of PPs was greater in the integral continual jejunal interposition group than in the Billroth I, isolated jejunal interposition, and Billroth II groups ((90.0±1.5)%, (84.1±1.4)%, (60.2±1.2)%, and (49.1±1.6)%, respectively; P <0.01).
Post-prandial myoelectric activity
The post-prandial frequencies of PPs were greater in the integral continual jejunal interposition ((19.1±0.9) cycles/min) and Billroth I ((18.5±0.7) cycles/min) groups than in the isolated jejunal interposition ((15.3±0.8) cycles/min) and Billroth II ((16.0±0.5) cycles/min) groups (P <0.05). The percentage of aboral propagation of PPs was greater in the integral continual jejunal interposition group than in the Billroth I, isolated jejunal interposition, and Billroth II groups ((91.0±1.6)%, (82.1±1.5)%, (52.2±1.2)%, and (50.5±1.6)%, respectively; P <0.01).
To reduce complications and improve nutritional status after subtotal gastrectomy, it is important to find a proper reconstruction technique for future clinical application. Creating a gastric reservoir has been found to maintain a low speed of food passage in the upper intestinal tract and retain the food storage volume, and increasing evidence from randomized controlled clinical studies reveals that establishing a jejunal reservoir improves the post-operation food capacity and nutritional status.1,2,16-18 Our study showed that nutritional parameters, including the average weight and PNI, were significantly greater in the integral continual jejunal interposition and Billroth I groups and suggested that jejunal continuity and duodenal food passage exerted beneficial effects on the dogs’ quality of life after subtotal gastrectomy. Methods that avoid jejunal transection and the maintenance of the duodenal passage have been performed with good results after subtotal gastrectomy.15,19
Total or subtotal gastrectomy, by removing the hormone producing mucosa of the stomach and rearranging the gastrointestinal route for the passage of food, inevitably alters the gastrointestinal hormone production. Different types of surgical reconstructions (exclusion or preservation of the duodenal passage) may result in a different magnitude of this disturbance. The altered production of gastrointestinal hormones may lead to an altered experience of hunger and satiety resulting in decreased caloric intake and reduced quality of life in patients after total or subtotal gastrectomy. Blood sugar regulation has long been described to be disturbed after gastrectomy, with early hyperglycemia and late hypoglycemia during the oral glucose tolerance test.20 There were significantly higher glucose levels in the Roux-en-Y patients and in patients with pouch construction and duodenal exclusion, while the pathological glucose tolerance did not develop when the duodenal route was preserved.21 In patients with total gastrectomy and a preserved duodenal passage, there were significantly higher glucose levels in the first 45 minutes after a liquid test meal.22 In our study, the postprandial glucose curves were higher in dogs in the four operative groups compared to the controls, and the group with duodenal exclusion (Billroth II) had significantly higher glucose levels compared to the normal control group. There were no significant differences between the integral continual jejunal interposition and Billroth I groups. Duodenal exclusion disturbs glucose homeostasis more than reconstructions with a preserved duodenal passage.23
The current study demonstrates that insulin secretion is altered during the hyperglycemic phase in post-operative OGTT. Previous studies on subjects after total gastrectomy regarding endogenous insulin production also found higher postprandial levels.22 Regarding the duodenal passage preservation, Schwarz et al found that the insulin level was elevated only in the jejunum interposition cases and not in cases where the duodenum was excluded.21 Post-prandial insulin curves reached significantly higher levels in all operated groups compared to controls, and a disturbed glucose homeostasis was observed in gastrectomized patients, most prominently in the Roux-en-Y group.23 In our experiment, the insulin level increased to abnormally high values in all four gastrectomized groups in response to food stimulus compared to the healthy control. The insulin curve was highest in groups with a preserved duodenal passage (Billroth I, continual jejunal interposition, and isolated jejunal interposition group). The OGTT evaluates a more physiological response to ingested glucose by virtue of its dependence on the enteric modulation of the insulin release. It is well known that the gut affects the overall response to glucose by stimulating the release of insulin via separate enteric hormonal mechanisms. Gastric inhibitory peptide (GIP) belongs to the secretin and glucagon family and is produced by the K cells of the small intestine. The concentration of GIP is the highest in the jejunum, and the duodenum and ileum also secrete a small amount; GIP might stimulate insulin release. GIP has more recently come to be known as glucose-dependent insulinotropic polypeptide; after the ingestion of glucose or a mixed meal, the insulin and GIP levels increase rapidly and simultaneously.24,25 Oral glucose resulted in a greater insulin response than the same amount of intravenous glucose.26 Insulin secretion is stimulated by the high blood glucose peak as a result of the early and quick intestinal absorption of glucose due to the rapid intestinal transit in the gastrectomized state.
The continuity of the gastrointestinal tract plays a key role in the coordination of intestinal motility. Emerging evidence has shown that the surgical manipulation of the gastrointestinal tract, such as resection followed by reanastomosis, results in the disruption of intestinal motility.27 Furthermore, several studies suggested that the disruption of motility by the gastrointestinal resection was due to damage to the pacemakers for the gastrointestinal tract, the interstitial cells of Cajal (ICCs). ICCs are responsible for generating and propagating electrical slow waves that coordinate the phasic contractions.28,29 In our study, the fasting myoelectric activity with a frequency of approximately 5 cycles/min was recorded from the electrodes on the gastric remnant. The frequencies of fasting and postprandial jejunal PPs were greater in the integral continual jejunal interposition and Billroth I groups than in the isolated jejunal interposition and Billroth II groups. The percentage of aboral propagation of PPs was greater in the integral continual jejunal interposition group than in the Billroth I, isolated jejunal interposition, and Billroth II groups. Jejunal transection from the duodenal pacemaker disrupts the propagation of PPs, which leads to ectopic pacemaker formation and an increase in the oral PP propagation.
The “uncut Roux” reconstructive technique has been duplicated and found to be successful in promoting myoelectric continuity in the aboral direction and in preventing the formation of ectopic pacemakers.14,15 Tu’s experiments confirmed that restoring the jejunal continuity with a hand-sewn jejunojejunostomy and constructing an uncut Roux limb with the gastrojejunostomy distal to the segment used for the original Roux limb increased the percentage of aborally propagating PPs in the new Roux limb.30 The aboral propagation occurred more frequently in the uncut Roux-en-Y with a jejunal pouch (URYJP) group during fasting and after feeding. The myoelectric data indicated that the URYJP technique promotes the maintenance of the PP frequency and an increased percentage of aboral propagation of PPs, while the conventional Roux-en-Y technique might cause an abnormal propagation of the PPs and decrease the frequency of PPs. The combination of the jejunal pouch and uncut Roux limb improved the overall nutritional parameters compared to the traditional Roux-en-Y while preserving the aboral propagation of jejunal pacesetter potentials.31 Electrophysiologically, a significant difference was noted between the jejunal pouch interposition (JP) and esophagogastrostomy (EG) groups in the number of action potentials per unit time, the mean amplitude, and the length of the resting period in the preprandial state. All parameters tended to be normalized sooner after surgery in the JP group. The clinical superiority of the JP was suggested experimentally to the same extent based on the electromyograms.32
Continual jejunal interposition after subtotal gastrectomy avoids jejunal transection, maintains the duodenal passage and food storage bags, and reduces the influence of blood glucose and insulin after the reconstruction of the digestive tract. The continuity of the gastrointestinal tract plays a key role in the coordination of intestinal motility. If an alimentary reconstruction using the Billroth I procedure cannot be performed, priority should be given to the continual jejunal interposition after subtotal gastrectomy.
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