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Effects of intraabdominally insufflated carbon dioxide and elevated intraabdominal pressure on postoperative gastrointestinal transit: An experimental study in mice
Effects of Intraabdominally Insufflated Carbon Dioxide and Elevated Intraabdominal Pressure on Postoperative Gastrointestinal Transit: An Experimental Study in Mice By Joaquim
Bustorff-Silva,
Carlos
A. Perez, Los
Angeles,
Background/Purpose: Postoperative ileus after abdominal operations is thought to be related to the degree of surgical trauma, and it has been shown that the simple act of opening the peritoneum can decrease gastrointestinal motility. Accordingly, some investigators have shown a reduction in the duration of postoperative ileus after laparoscopic procedures. It is not clear, however, if this reduction is secondary to less manipulation of the viscera or to the lack of an abdominal incision. The aim of this study was to determine the effect of intraabdominal insufflation with CO2 on postoperative gastrointestinal transit. Methods:Twenty-eight male mice weighing between 25 and 30 g were divided randomly into 4 groups: Control (unoperated), Incision (conventional laparotomy), Cecal (laparotomy plus cecal manipulation), and lnsufflation (abdominal insufflation with C02). Postoperative gastrointestinal motility was assessed by weighing total fecal output over the first 15 postoperative hours.
P
ERFORMING an abdominal surgery has been shown to cause an inhibition of gastrointestinal (GI) motility known as postoperative ileus. In most cases, the duration of this disturbance is short, lasting from 12 to 24 hours. However, in some patients, extended postoperative ileus may occur, and nasogastric decompression may be needed, resulting in longer hospital stay and increased discomfort to the patient.’ The precise triggering mechanisms involved in postoperative ileus are not completely understood, and conflicting evidence exists as to whether the degree and duration of postoperative ileus are related to the degree of surgical trauma.2.3 From the Division of Pediatric Surgery and the Department of Medicine and Physiology, UCLA School of Medicine and Cure Digestive Disease Research Centen Los Angeles, CA. Supported by grants ATH DK 41004 and CURE Digestive Diseases Center Grant DK 41301 (Dr Raybould). Dr Bustotf-Silva is the recipient of postdoctorate grant #97/0927-2 from the Fundacao de Amparo a Pesquisa do Estado de Sao Paulo-FAPESP-SP Address reprint requests to James B. Atkinson, MD, Division of Pediatric Surgery, Deparhent of Surgery, Room 72-140 CHS, UCLA School of Medicine, Los Angeles, CA 90024. Copyright o 1999 by WB. Saunders Company 0022-3468/99/3410-0008$03.00/O
1482
James
B. Atkinson,
and
Helen
E. Raybould
California
Results: Fecal pellet output over 15 hours control group was 1.20 5 0.12 g. In peritoneal incision alone, fecal pellet output decreased to 0.82 IT 0.11 g (P< .05). subjected to abdominal insufflation with output was not significantly different from (1.2 % 0.05 g; not significant). Fecal pellet edly reduced by incision combined with (0.24 t 0.02 g, P < .Ol).
in the untreated mice subjected to was significantly However, in mice COP, fecal pellet untreated controls output was markcecal manipulation
Conc/usions:The current study findings show that abdominal insufflation, in a procedure similar to that used during laparoscopic surgery, had no measurable effect on gastrointestinal transit in awake mice. This suggests that the lack of an abdominal incision can contribute to a reduced postoperative ileus after abdominal surgery. J Pediatr Sorg 34:1482-1485. Copyright o 1999 by W.B. Saunders Company. INDEX
WORDS:
Postoperative
ileus,
laparoscopy,
mice.
Results of clinica14-6and experimental studies7g8have shown an earlier recovery of normal bowel function after laparoscopic procedures when compared with the same operations using the conventional route. However, it remains unclear whether the shorter ileus observed after laparoscopic procedures is secondary to a lesser degree of visceral manipulation or to the absence of the abdominal incision. In our laboratory we developed an experimental model to investigate the duration of postoperative ileus in mice by weighing the total fecal output in the first 15 hours after surgery. Using this model we were able to show a correlation between the duration of postoperative ileus and the extent of surgical manipulation of the bowel.9 Additionally, we confirmed previous observations showing that simple incision into the abdominal cavity is capable of inducing a significant, although less pronounced, delay in gastrointestinal transit.‘O Based on these findings we hypothesized that peritoneal insufflation with COZ, as performed during laparoscopic operations, would result in a lower degree of postoperative ileus than that observed after a conventional abdominal incision. In the current study, we used the mice model to
Journal
ofPediatric
Surgery,
Vol34,
No 10 (October),
1999: pp 1482-1485
POSTOPERATIVE
GASTROINTESTINAL
TRANSIT
determine the effect of peritoneal insufflation with CO;! on postoperative intestinal motility, comparing it to a conventional peritoneal incision with or without bowel manipulation. MATERIALS
AND METHODS
Study Design Procedures were performed according to a protocol reviewed and approved by the Office for Protection of Research Subjects of UCLA. fienty-eight male mice (C57BU6 strain, Harlan, San Diego, CA), weighing between 25 and 30 g were maintained in rooms with controlled temperature and light-dark cycles (lights off 6:00 PM to 690 AM) and fed ad libitum with laboratory chow. They were divided randomly into 4 study groups. In the control group (n = 7) total fecal output during 15 hours was measured in unmanipulated animals; in the incision group (n = 6) the animals were anesthetized by inhaling a mixture of 02 and halothane through a specially designed mask. A2-cm midabdominal incision was made, opening the peritoneal cavity, without touching the bowel. This incision was left open for about 10 minutes and was then closed using 2 layers of fine nonabsorbable suture. In the cecal group (n = 7), using the same anesthetic technique, a 2-cm midabdominal wall incision was made: the cecum was exteriorized and gently manipulated for 3 minutes. The cecum was then returned to the abdominal cavity and the incision closed as described previously. In the fourth group (insulYation, n = 8), using the same anesthetic technique, a small 23-gauge blunt needle was placed in the abdomen through the midline, near the umbilicus. Using a high-flow insuflator (Stryker Endoscopy, Santa Clara, CA), CO;? was injected in the abdominal cavity until an intraabdominal pressure of 6 to 8 mm Hg was achieved, which is the level used in most laparoscopic procedures performed in children. Rising the intraabdominal pressure above those levels resulted in severe respiratory discomfort. This pressure was maintained for 15 minutes. After that time, the cannula was removed. and the port site was closed using a single stitch. The duration of the combined anesthetic and surgical procedures was 15 minutes in all animals, and every procedure was performed between 400 and 600 PM. so that the animals would be studied during their normal active period of the light-dark cycle.
Evaluation
of the Postoperative
Ileus
After the surgery, mice were housed in individual wire bottom cages and offered water and food ad libitum overnight. Fifteen hours after surgery the mice were killed, the fecal pellets were harvested from the cages, allowed to dry for 2 hours under a heating lamp, and weighed. Fecal output from the control group animals was measured in the same way 15 hours after they were separated into individual cages. Mean fecal output was compared among all groups using one-way analysis of variance (ANOVA) followed by Dunnett’s Multiple Comparson test to compare the different surgical procedures to the control group. Results were considered statistically significant if P 5 .05.
RESULTS
Fecal pellet output over 15 hours in the untreated control group was 1.20 +- 0.12 g (Fig 1). In mice subjected to peritoneal incision alone, fecal pellet output was significantly decreased to 0.82 2 0.11 g (P < .05>. However, in mice subjected to abdominal insufflation with C02, fecal pellet output was not significantly different from untreated controls (1.2 + 0.05 g; not
1483
1.4 5
12
r”
T
*
1
T
.$ 3
06
2
06
g = 3I-
0.4
*
0.2 O cc3Nwa
INw=FLATloN Study
EJCISION
CKXL
groups
Fig 1. Mean f SEM of the weight (g) of the total fecal output observed in the first 15 hours after the operation in the mice of the 4 experimental groups (*P c ~35, one-way ANOVA followed by Dunnet’s test for multiple comparisons against a control.)
significant). Fecal pellet output was markedly reduced by incision combined with cecal manipulation (0.24 + 0.02 g, P < .OOl). DISCUSSION
The current study shows that in a model of experimental ileus in mice, abdominal insufflation, in a procedure similar to that used during laparoscopic surgery, had no measurable effect on gastrointestinal transit in awake mice. This is in marked contrast to the profound postoperative ileus seen in mice subjected to a conventional midline abdominal incision. Laparoscopic surgery has been said to induce less surgical trauma and result in shorter hospital stay than conventional operations. Clinical and experimental investigations have shown lower levels of circulating cytokines” and less interference with immune function12-l4 after laparoscopic procedures when compared with the same procedures using the conventional route. Experimental evidence showing an inverse correlation between the size of an abdominal incision and the degree of impairment in cell-mediated immune functioni suggests that the lower degree of surgical trauma associated with laparoscopy is at least in part related to the small size of the abdominal incisions. There is still some controversy regarding whether the shorter hospitalization associated with laparoscopic procedures is secondary to early resolution of postoperative ileus. Although this is certainly the case in procedures like cholecystectomy,16 adrenalectomy,4 or fundoplication6 data on more complex procedures like colorectal procedures remains equivocal. Although studies using experimental animals have shown an earlier onset of intestinal myoelectric activity after laparoscopic-assisted colectomy,7.17J8 clinical trials have yielded conflicting results.1g.20Reasons for this controversy may be related to a subjective and variable definition of “ileus” used by the
1484
BUSTORFF-SILVA
different investigators and also to the fact that return of myoelectric activity to isolated segments of the intestinal tract may not correlate with other parameters of normal bowel function, such as passage of flatus or stools.21 By analyzing the amount of fecal output as a measure of the duration of postoperative ileus, the model used in the current study has the advantage of reproducing the clinical setting. Previous work in rats has shown that this measurement correlates very closely with intestinal transit estimated by the time to evacuate an intragastrically placed dye.22 Data from the current experiment indicate that the degree of postoperative ileus is proportional to the extent of surgical manipulation. These results are in agreement with the observations of others’O who showed different degrees of inhibition of gastrointestinal transit associated with skin incision, laparotomy alone, or laparotomy with bowel manipulation. Taken together, these observations suggest that the abdominal incision and intestinal manipulation have an additive effect in the intensity of the postoperative ileus. This would explain why the benefits of laparoscopic surgery may be less evident in more extensive operations, especially those involving intestinal anastomosis.1g,20 In those cases, functional obstruction secondary to intestinal reconstruction may superimpose on the postoperative ileus, resulting in a delayed return to normal bowel function, regardless of the approach used. The experimental protocol used in the current study did not include performing any intestinal anastomosis making it possible to study the isolated effect of the
ET AL
peritoneal insufflation with CO2 as compared with that of a conventional abdominal incision. The data presented clearly show that the peritoneal insufflation did not result in any decrease of intestinal motility. In fact, the fecal output in the insufflation group was exactly the same as in the control group. In contrast, conventional laparotomy alone or in combination with cecal manipulation resulted in decreasing levels of intestinal motility. These results support the findings of an earlier recovery of intestinal function after laparoscopic procedures and indicates that this is, at least in part, caused by the absence of a conventional laparotomy incision. Although the current study was designed to determine the isolated role of the abdominal incision, future studies using techniques of laparoscopy and micromanipulation could help to investigate the role of laparoscopy in the prevention of postoperative ileus, in the presence of intestinal manipulation. From the clinical point of view, data from the current study confirm the beneficial aspects of the laparoscopic approach especially in operations not associated with major intestinal manipulations such as cholecystectomy and fundoplication. Data from the current study do not allow to extend those conclusions to more traumatic operations that include extensive intestinal manipulation and anastomosis. Further studies are necessary to clarify this point. Nevertheless, the absence of postoperative ileus after intraabdominal insufflation with CO2 may reflect a lesser degree of metabolic injury, which could contribute to the faster recovery of patients.
REFERENCES 1. Livingston EH, Passaro EPJ: Postoperative ileus. Dig Dis Sci 35121-132, 1990 2. Wells C, Tinnkler L, Rawlinson K: Postoperative gastrointestinal motility. Lancet 1:4-S, 1964 3. Wilson JP: Postoperative motility of the large intestine in man. Gut 16:689-692, 1915 4. Aldrighetti L, Giacomelli M, Calori G, et al: Impact of minimally invasive surgery on adrenalectomy for incidental tumors: comparison with laparotomic technique. Int Surg 82:160-164, 1997 5. Iroatulam AJ, Agachan F, Alabaz 0, et al: Laparoscopic abdominoperineal resection for anorectal cancer. Am Surg 64:12-18, 1998 6. Lame S, Rantala A, Gullichsen R, et al: Laparoscopic vs conventional Nissen fundoplication. A prospective randomized smdy. Surg Endosc 11:441-444.1997 7. Bohm B, Milsom JW, Fazio VW: Postoperative intestinal motility following conventional and laparoscopic intestinal surgery. Arch Surg 130:415-419, 1995 8. Scbippers E, Ottinger AP, Anurov M, et al: Intestinal motility after laparoscopic vs conventional cholecystectomy. An animal experiment study and clinical observation. Langenbecks Arch Chir 377: 14-18,1992 9. Bustorff-Silva J, Perez CA, Caan SA, et al: Role of mast cells in surgically-induced gastrointestinal ileus in mice. Neurogastrenterol Motil10:351,1998 10. De Winter BY, Boeckxstaens GE, De Man JG, et al: Effect of
adrenergic and nitrergic blockade on experimental ileus in rats. Br J Pharmacoll20:464-468,1997 Il. Glaser F, Sannwald GA, Buhr HJ, et al: General stress response to conventional and laparoscopic cholecystectomy. AM Surg 221:372380,1995 12. Allendorf JD, Bessler M, Whelan RL, et al: Better preservation of immune function after laparoscopic-assisted vs. open bowel resection in a murine model. Dis Colon Rectum 39:S67-S72, 1996 13. Gutt CN, Kuntz C, Schmandra T, et al: Metabolism and immunology in laparoscopy. First workshop on experimental laparoscopic surgery, Frankfurt, 1997. Surg Endosc 12:1096-1098,1998 14. Mendoza-Sagaon M, Gitzelmamr CA, Herreman-Suquet K, et al: Immune response: Effects of operative stress in a pediatric model. J Pediatr Surg 33:388-393, 1998 15. Ahendorf JD, Bessler M, Whelan RL, et al: Postoperative immune function varies inversely with the degree of surgical trauma in a murine model. Surg Endosc 11:427-430,1997 16. The Southern Surgeons Club: A prospective analysis of 1518 laparoscopic cholecystectomies. [published erratum appears in N Engl J Med 1991 Nov 21:325:1517-15181 [see comments]. N Engl J Med 324:1073-1078,199l 17. Davies W, Kollmorgen CF, Tu QM, et al: Laparoscopic colectomy shortens postoperative ileus in a canine model. Surgery 121:550555,1997 18. Hotokezaka
M, Combs
MJ, Schirmer
BD: Recovery
of gastroin-
POSTOPERATIVE
GASTROINTESTINAL
testinal motility following open versus dogs. Dig Dis Sci 41:705-710, 1996
1485
TRANSIT
laparoscopic
colon
resection
in
19. Schmitt SL, Cohen SM, Wexner SD, et al: Does laparoscopicassisted ileal pouch anal anastomosis reduce the length of hospitalization? Int J Colorectal Dis 9:134-137, 1994 20. Milsom JW, Bohm B, Hammerhofer randomized trial comparing laparoscopic
KA, et al: A prospective, versus conventional tech-
niques in colorectal cancer surgery: A preliminary report [see comments]. J Am Co11 Surg 187:46-54, 1998 21. Hotokezaka M, Mentis EP, Pate1 SP, et al: Recovery of gastrointest&l tract motility and myoelectric activity change after abdominal surgery. Arch Surg 132:410-417,1997 22. Zittel TT, Lloyd KC, Rothenhofer I, et al: Calcitonin generelated peptide and spinal afferents partly mediate postoperative colonic ileus in the rat. Surgery 123:518-527, 1998
Bustorff-Silva,
Carlos
A. Perez, Los
Angeles,
Background/Purpose: Postoperative ileus after abdominal operations is thought to be related to the degree of surgical trauma, and it has been shown that the simple act of opening the peritoneum can decrease gastrointestinal motility. Accordingly, some investigators have shown a reduction in the duration of postoperative ileus after laparoscopic procedures. It is not clear, however, if this reduction is secondary to less manipulation of the viscera or to the lack of an abdominal incision. The aim of this study was to determine the effect of intraabdominal insufflation with CO2 on postoperative gastrointestinal transit. Methods:Twenty-eight male mice weighing between 25 and 30 g were divided randomly into 4 groups: Control (unoperated), Incision (conventional laparotomy), Cecal (laparotomy plus cecal manipulation), and lnsufflation (abdominal insufflation with C02). Postoperative gastrointestinal motility was assessed by weighing total fecal output over the first 15 postoperative hours.
P
ERFORMING an abdominal surgery has been shown to cause an inhibition of gastrointestinal (GI) motility known as postoperative ileus. In most cases, the duration of this disturbance is short, lasting from 12 to 24 hours. However, in some patients, extended postoperative ileus may occur, and nasogastric decompression may be needed, resulting in longer hospital stay and increased discomfort to the patient.’ The precise triggering mechanisms involved in postoperative ileus are not completely understood, and conflicting evidence exists as to whether the degree and duration of postoperative ileus are related to the degree of surgical trauma.2.3 From the Division of Pediatric Surgery and the Department of Medicine and Physiology, UCLA School of Medicine and Cure Digestive Disease Research Centen Los Angeles, CA. Supported by grants ATH DK 41004 and CURE Digestive Diseases Center Grant DK 41301 (Dr Raybould). Dr Bustotf-Silva is the recipient of postdoctorate grant #97/0927-2 from the Fundacao de Amparo a Pesquisa do Estado de Sao Paulo-FAPESP-SP Address reprint requests to James B. Atkinson, MD, Division of Pediatric Surgery, Deparhent of Surgery, Room 72-140 CHS, UCLA School of Medicine, Los Angeles, CA 90024. Copyright o 1999 by WB. Saunders Company 0022-3468/99/3410-0008$03.00/O
1482
James
B. Atkinson,
and
Helen
E. Raybould
California
Results: Fecal pellet output over 15 hours control group was 1.20 5 0.12 g. In peritoneal incision alone, fecal pellet output decreased to 0.82 IT 0.11 g (P< .05). subjected to abdominal insufflation with output was not significantly different from (1.2 % 0.05 g; not significant). Fecal pellet edly reduced by incision combined with (0.24 t 0.02 g, P < .Ol).
in the untreated mice subjected to was significantly However, in mice COP, fecal pellet untreated controls output was markcecal manipulation
Conc/usions:The current study findings show that abdominal insufflation, in a procedure similar to that used during laparoscopic surgery, had no measurable effect on gastrointestinal transit in awake mice. This suggests that the lack of an abdominal incision can contribute to a reduced postoperative ileus after abdominal surgery. J Pediatr Sorg 34:1482-1485. Copyright o 1999 by W.B. Saunders Company. INDEX
WORDS:
Postoperative
ileus,
laparoscopy,
mice.
Results of clinica14-6and experimental studies7g8have shown an earlier recovery of normal bowel function after laparoscopic procedures when compared with the same operations using the conventional route. However, it remains unclear whether the shorter ileus observed after laparoscopic procedures is secondary to a lesser degree of visceral manipulation or to the absence of the abdominal incision. In our laboratory we developed an experimental model to investigate the duration of postoperative ileus in mice by weighing the total fecal output in the first 15 hours after surgery. Using this model we were able to show a correlation between the duration of postoperative ileus and the extent of surgical manipulation of the bowel.9 Additionally, we confirmed previous observations showing that simple incision into the abdominal cavity is capable of inducing a significant, although less pronounced, delay in gastrointestinal transit.‘O Based on these findings we hypothesized that peritoneal insufflation with COZ, as performed during laparoscopic operations, would result in a lower degree of postoperative ileus than that observed after a conventional abdominal incision. In the current study, we used the mice model to
Journal
ofPediatric
Surgery,
Vol34,
No 10 (October),
1999: pp 1482-1485
POSTOPERATIVE
GASTROINTESTINAL
TRANSIT
determine the effect of peritoneal insufflation with CO;! on postoperative intestinal motility, comparing it to a conventional peritoneal incision with or without bowel manipulation. MATERIALS
AND METHODS
Study Design Procedures were performed according to a protocol reviewed and approved by the Office for Protection of Research Subjects of UCLA. fienty-eight male mice (C57BU6 strain, Harlan, San Diego, CA), weighing between 25 and 30 g were maintained in rooms with controlled temperature and light-dark cycles (lights off 6:00 PM to 690 AM) and fed ad libitum with laboratory chow. They were divided randomly into 4 study groups. In the control group (n = 7) total fecal output during 15 hours was measured in unmanipulated animals; in the incision group (n = 6) the animals were anesthetized by inhaling a mixture of 02 and halothane through a specially designed mask. A2-cm midabdominal incision was made, opening the peritoneal cavity, without touching the bowel. This incision was left open for about 10 minutes and was then closed using 2 layers of fine nonabsorbable suture. In the cecal group (n = 7), using the same anesthetic technique, a 2-cm midabdominal wall incision was made: the cecum was exteriorized and gently manipulated for 3 minutes. The cecum was then returned to the abdominal cavity and the incision closed as described previously. In the fourth group (insulYation, n = 8), using the same anesthetic technique, a small 23-gauge blunt needle was placed in the abdomen through the midline, near the umbilicus. Using a high-flow insuflator (Stryker Endoscopy, Santa Clara, CA), CO;? was injected in the abdominal cavity until an intraabdominal pressure of 6 to 8 mm Hg was achieved, which is the level used in most laparoscopic procedures performed in children. Rising the intraabdominal pressure above those levels resulted in severe respiratory discomfort. This pressure was maintained for 15 minutes. After that time, the cannula was removed. and the port site was closed using a single stitch. The duration of the combined anesthetic and surgical procedures was 15 minutes in all animals, and every procedure was performed between 400 and 600 PM. so that the animals would be studied during their normal active period of the light-dark cycle.
Evaluation
of the Postoperative
Ileus
After the surgery, mice were housed in individual wire bottom cages and offered water and food ad libitum overnight. Fifteen hours after surgery the mice were killed, the fecal pellets were harvested from the cages, allowed to dry for 2 hours under a heating lamp, and weighed. Fecal output from the control group animals was measured in the same way 15 hours after they were separated into individual cages. Mean fecal output was compared among all groups using one-way analysis of variance (ANOVA) followed by Dunnett’s Multiple Comparson test to compare the different surgical procedures to the control group. Results were considered statistically significant if P 5 .05.
RESULTS
Fecal pellet output over 15 hours in the untreated control group was 1.20 +- 0.12 g (Fig 1). In mice subjected to peritoneal incision alone, fecal pellet output was significantly decreased to 0.82 2 0.11 g (P < .05>. However, in mice subjected to abdominal insufflation with C02, fecal pellet output was not significantly different from untreated controls (1.2 + 0.05 g; not
1483
1.4 5
12
r”
T
*
1
T
.$ 3
06
2
06
g = 3I-
0.4
*
0.2 O cc3Nwa
INw=FLATloN Study
EJCISION
CKXL
groups
Fig 1. Mean f SEM of the weight (g) of the total fecal output observed in the first 15 hours after the operation in the mice of the 4 experimental groups (*P c ~35, one-way ANOVA followed by Dunnet’s test for multiple comparisons against a control.)
significant). Fecal pellet output was markedly reduced by incision combined with cecal manipulation (0.24 + 0.02 g, P < .OOl). DISCUSSION
The current study shows that in a model of experimental ileus in mice, abdominal insufflation, in a procedure similar to that used during laparoscopic surgery, had no measurable effect on gastrointestinal transit in awake mice. This is in marked contrast to the profound postoperative ileus seen in mice subjected to a conventional midline abdominal incision. Laparoscopic surgery has been said to induce less surgical trauma and result in shorter hospital stay than conventional operations. Clinical and experimental investigations have shown lower levels of circulating cytokines” and less interference with immune function12-l4 after laparoscopic procedures when compared with the same procedures using the conventional route. Experimental evidence showing an inverse correlation between the size of an abdominal incision and the degree of impairment in cell-mediated immune functioni suggests that the lower degree of surgical trauma associated with laparoscopy is at least in part related to the small size of the abdominal incisions. There is still some controversy regarding whether the shorter hospitalization associated with laparoscopic procedures is secondary to early resolution of postoperative ileus. Although this is certainly the case in procedures like cholecystectomy,16 adrenalectomy,4 or fundoplication6 data on more complex procedures like colorectal procedures remains equivocal. Although studies using experimental animals have shown an earlier onset of intestinal myoelectric activity after laparoscopic-assisted colectomy,7.17J8 clinical trials have yielded conflicting results.1g.20Reasons for this controversy may be related to a subjective and variable definition of “ileus” used by the
1484
BUSTORFF-SILVA
different investigators and also to the fact that return of myoelectric activity to isolated segments of the intestinal tract may not correlate with other parameters of normal bowel function, such as passage of flatus or stools.21 By analyzing the amount of fecal output as a measure of the duration of postoperative ileus, the model used in the current study has the advantage of reproducing the clinical setting. Previous work in rats has shown that this measurement correlates very closely with intestinal transit estimated by the time to evacuate an intragastrically placed dye.22 Data from the current experiment indicate that the degree of postoperative ileus is proportional to the extent of surgical manipulation. These results are in agreement with the observations of others’O who showed different degrees of inhibition of gastrointestinal transit associated with skin incision, laparotomy alone, or laparotomy with bowel manipulation. Taken together, these observations suggest that the abdominal incision and intestinal manipulation have an additive effect in the intensity of the postoperative ileus. This would explain why the benefits of laparoscopic surgery may be less evident in more extensive operations, especially those involving intestinal anastomosis.1g,20 In those cases, functional obstruction secondary to intestinal reconstruction may superimpose on the postoperative ileus, resulting in a delayed return to normal bowel function, regardless of the approach used. The experimental protocol used in the current study did not include performing any intestinal anastomosis making it possible to study the isolated effect of the
ET AL
peritoneal insufflation with CO2 as compared with that of a conventional abdominal incision. The data presented clearly show that the peritoneal insufflation did not result in any decrease of intestinal motility. In fact, the fecal output in the insufflation group was exactly the same as in the control group. In contrast, conventional laparotomy alone or in combination with cecal manipulation resulted in decreasing levels of intestinal motility. These results support the findings of an earlier recovery of intestinal function after laparoscopic procedures and indicates that this is, at least in part, caused by the absence of a conventional laparotomy incision. Although the current study was designed to determine the isolated role of the abdominal incision, future studies using techniques of laparoscopy and micromanipulation could help to investigate the role of laparoscopy in the prevention of postoperative ileus, in the presence of intestinal manipulation. From the clinical point of view, data from the current study confirm the beneficial aspects of the laparoscopic approach especially in operations not associated with major intestinal manipulations such as cholecystectomy and fundoplication. Data from the current study do not allow to extend those conclusions to more traumatic operations that include extensive intestinal manipulation and anastomosis. Further studies are necessary to clarify this point. Nevertheless, the absence of postoperative ileus after intraabdominal insufflation with CO2 may reflect a lesser degree of metabolic injury, which could contribute to the faster recovery of patients.
REFERENCES 1. Livingston EH, Passaro EPJ: Postoperative ileus. Dig Dis Sci 35121-132, 1990 2. Wells C, Tinnkler L, Rawlinson K: Postoperative gastrointestinal motility. Lancet 1:4-S, 1964 3. Wilson JP: Postoperative motility of the large intestine in man. Gut 16:689-692, 1915 4. Aldrighetti L, Giacomelli M, Calori G, et al: Impact of minimally invasive surgery on adrenalectomy for incidental tumors: comparison with laparotomic technique. Int Surg 82:160-164, 1997 5. Iroatulam AJ, Agachan F, Alabaz 0, et al: Laparoscopic abdominoperineal resection for anorectal cancer. Am Surg 64:12-18, 1998 6. Lame S, Rantala A, Gullichsen R, et al: Laparoscopic vs conventional Nissen fundoplication. A prospective randomized smdy. Surg Endosc 11:441-444.1997 7. Bohm B, Milsom JW, Fazio VW: Postoperative intestinal motility following conventional and laparoscopic intestinal surgery. Arch Surg 130:415-419, 1995 8. Scbippers E, Ottinger AP, Anurov M, et al: Intestinal motility after laparoscopic vs conventional cholecystectomy. An animal experiment study and clinical observation. Langenbecks Arch Chir 377: 14-18,1992 9. Bustorff-Silva J, Perez CA, Caan SA, et al: Role of mast cells in surgically-induced gastrointestinal ileus in mice. Neurogastrenterol Motil10:351,1998 10. De Winter BY, Boeckxstaens GE, De Man JG, et al: Effect of
adrenergic and nitrergic blockade on experimental ileus in rats. Br J Pharmacoll20:464-468,1997 Il. Glaser F, Sannwald GA, Buhr HJ, et al: General stress response to conventional and laparoscopic cholecystectomy. AM Surg 221:372380,1995 12. Allendorf JD, Bessler M, Whelan RL, et al: Better preservation of immune function after laparoscopic-assisted vs. open bowel resection in a murine model. Dis Colon Rectum 39:S67-S72, 1996 13. Gutt CN, Kuntz C, Schmandra T, et al: Metabolism and immunology in laparoscopy. First workshop on experimental laparoscopic surgery, Frankfurt, 1997. Surg Endosc 12:1096-1098,1998 14. Mendoza-Sagaon M, Gitzelmamr CA, Herreman-Suquet K, et al: Immune response: Effects of operative stress in a pediatric model. J Pediatr Surg 33:388-393, 1998 15. Ahendorf JD, Bessler M, Whelan RL, et al: Postoperative immune function varies inversely with the degree of surgical trauma in a murine model. Surg Endosc 11:427-430,1997 16. The Southern Surgeons Club: A prospective analysis of 1518 laparoscopic cholecystectomies. [published erratum appears in N Engl J Med 1991 Nov 21:325:1517-15181 [see comments]. N Engl J Med 324:1073-1078,199l 17. Davies W, Kollmorgen CF, Tu QM, et al: Laparoscopic colectomy shortens postoperative ileus in a canine model. Surgery 121:550555,1997 18. Hotokezaka
M, Combs
MJ, Schirmer
BD: Recovery
of gastroin-
POSTOPERATIVE
GASTROINTESTINAL
testinal motility following open versus dogs. Dig Dis Sci 41:705-710, 1996
1485
TRANSIT
laparoscopic
colon
resection
in
19. Schmitt SL, Cohen SM, Wexner SD, et al: Does laparoscopicassisted ileal pouch anal anastomosis reduce the length of hospitalization? Int J Colorectal Dis 9:134-137, 1994 20. Milsom JW, Bohm B, Hammerhofer randomized trial comparing laparoscopic
KA, et al: A prospective, versus conventional tech-
niques in colorectal cancer surgery: A preliminary report [see comments]. J Am Co11 Surg 187:46-54, 1998 21. Hotokezaka M, Mentis EP, Pate1 SP, et al: Recovery of gastrointest&l tract motility and myoelectric activity change after abdominal surgery. Arch Surg 132:410-417,1997 22. Zittel TT, Lloyd KC, Rothenhofer I, et al: Calcitonin generelated peptide and spinal afferents partly mediate postoperative colonic ileus in the rat. Surgery 123:518-527, 1998