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Intestinal transit time is delayed by artificial sphincters after massive enterectomy in dogs
Intestinal Transit Time is Delayed by Artificial Sphincters After Massive Enterectomy in Dogs
Aldo Stacchini, MD, PhD, SGo Paulo, Brazil Liberato J. A. DiDio, MD, PhD, Toledo, Ohio A. John Christoforidis, MD, PhD, Columbus, Ohio Vicente Borelli, DVM, PhD, S2o Paulo, Brazil
The first successful extensive resection of the small intestine was performed by Koeberle in 1881, and pioneering experimental work in intestinal surgery aimed at treatment of obstructions was accomplished by Senn in 1888. In order to decelerate rapid intestinal transit as a result of massive resection, investigators have created several techniques, such as reversed jejunal segments that are interposed between the remaining stumps [l-6]. Numerous investigations have followed to test reversed segments of the small intestine, colon, and even of the stomach in varied numbers, lengths, and locations, and have produced conflicting results [7,8]. At one point, the use of recirculation loops attracted the attention of surgeons [g-11]; however, the need for an adequate amount of residual loops and the excessive number of anastomoses necessary were limiting factors, and the results did not meet reasonable expectations. The idea of slowing intestinal transit to allow a longer period of contact between absorbable nutrients and the residual intestine after massive resection of the small intestine led to the utilization of artificial sphincters. For the same reason, partial blockage of the intestinal flow by sutures, jejunal wall pleating, inward folding, or by a Teflon@ collar around the gut have been investigated [IZ]. The use of artificial sphincters and the creation of a jejunocolic valve and of an experimental sphincter have also been studied [13-161. From the Department of Anatomy, School of Medicine of Santos, SHo Paulo, Brazil. the Department of Anatomy, Medical College of Ohio, Toledo, Ohio, the Department of Radiology, Ohio State University College of Medicine, Columbus, Ohio, and the Department of Topographic Anatomy, Faculty of Veterinary Medicine, University of SHo Paulo, SHo Paulo, Brazil. Requests for reprints should be addressed to A. John Christoforidis, MD, Department of Radiology, Ohio State University College of Medicine, 410 West 10th Avenue, Columbus, Ohio 43210-1228.
480
In order to evaluate findings from a recent investigation [11] in which the feasibility of artificial sphincters was clearly demonstrated, we decided to measure the transit time of radiopaque medium in the intestine. We attempted to accomplish our goal by comparing the time of the radiologic transit between the duodenum and the rectum; that is, from the moment the radiopaque medium passed the gastroduodenal pylorus to the moment it reached the rectum. The animals used were enterectomized dogs with and without one or two artificial sphincters. The objective was to remove a 1 cm long segment of the longitudinal muscular layer of the intestinal wall while leaving intact the circular muscular layer. With this surgical maneuver, the circular layer could contract without the opposition of the removed longitudinal layer. Material and Methods We used 18 clinically normal mongrel adult dogs (9 male and 9 female) ranging in weight from 11 to 19.6 kg. They were distributed into Groups A, B, and C, each comprising six dogs (three males and three females). All animals underwent resection of 87.5 percent of the small intestine followed by an end-to-end duodenum to ileum anastomosis 10 cm orally to the ileocecal junction. Each group was treated as follows: (1) Group A dogs received an artificial sphincter 1 cm long constructed 5 cm orally from the anastomosis. (2) Group B dogs received two artificial sphincters 1 cm long created 5 cm and 10 cm orally from the anastomosis (Figure 1). (3) Group C dogs served as control animals and no artificial sphincters were created after the massive enterectomy. According to the technique of Stacchini et al [17], sphincters were created by moving circumferentially 1 cm long segments of the longitudinal musculature. This included the mesenteric border of the perimeter and entirely denuded the circular muscular layer. This was per-
The American Journal of Surgery
Delayed Intestinal Transit Time in Dogs
Figure 1. The creation of two artificial sphincters ( S, and S,). The iongitudinaimuscuiar iayer has been removed in two sites so that the circular iayer can contract without opposition.
formed so that ablation of the outer longitudinal muscular layer of the intestine would permit unopposed contraction of the inner circular layer. The longitudinal muscular layer represents the dilating component and the inner circular layer the closing or sphincteric component, thus creating a mechanism similar to a sphincter with the aim of reducing the rate of intestinal flow [13]. At the end of the sixth postoperative week, the dogs were studied radiologically. An image amplification fluoroscopic unit was used to monitor the progress of the contrast medium in the intestinal tract at frequent intervals as necessary. After a 12 hour fast, each animal was initially given 100 ml of barium sulfate by means of an esophageal probe and was immediately observed by fluoroscopy. The duration of radiologic transit was measured from the moment the radiopaque substance passed through the pylorus until its arrival in the rectum, monitored by successive observations made at 5 minute intervals. Radiographs were obtained during the initial and final stages of transit (Figures 2 and 3). The results were tested with the one-way analysis of variance by rank to compare the intestinal transit times in the three groups of dogs [18,19]. This was complemented by the Mann-Whitney test for independent groups [19]. p SO.05 was considered significant.
Figure 2. Radiograph obtained immediate/y after passage of the contrast medium through the pyiorus andinto the duodenum. D = duodenum; P = pyiorus; St = stomach.
To test the homogeneity of the groups with respect to the mean intestinal lengths, the small intestine of the dogs was measured before resection. The results are given in Table II. Using the analysis of variance, homogeneity of the mean intestinal length was confirmed, since the data indicated no statistically significant differences among the groups.
Results We evaluated the intestinal transit time from the pylorus to the rectum in 15 dogs (5 in each group) after resection of 87.5 percent of the length of the small intestine (Table I). The creation of two sphincters significantly delayed the intestinal transit time under the experimental conditions to which the dogs were submitted. The average transit time in Group A was 52 minutes; in Group B, 160 minutes; and in Group C, 50 minutes. One-way analysis of variance by rank demonstrated that the mean transit times of the three groups were significantly different. Group B was significantly different from Groups A and C by the Mann-Whitney U test, whereas the latter two groups did not differ from each other.
Volume 151, April 1966
CDtTltn@tltS The time of intestinal transit, measured from the moment the radiopaque contrast medium passed through the gastroduodenal pylorus until it reached the rectum, was not influenced by variations in the length of the residual intestine, since there were no statistically significant differences among the groups initially. Since resection of 87.5 percent of the total length of the small intestine from all animals was carried out, it is legitimate to consider the residual intestinal segments of the three groups equally homogenous. No deaths occurred during operation, and the median survival of the dogs with two artificial sphincters was longer than the other two groups of animals. When data from the three
481
Stacchini et al
TABLE I
lntestlnal Transit Time After Resection’ Transit Time (min)
Dogs Group A 1 2 3 5 Group B 7 8 9 10 11 Group C 13 14 15 16 17
30 37 52 75 146 214 183 87 172 43 46 54 52 58
Dogs 4, 12, and 18 were excluded because they died before the sixth postoperative week. l
Figure 3. Radlograph obtained at the @aI stage of transit showing arrival of the contrast medium at the rectum. D = duodenum; P = pylorus; Sl, SII = artfflcial sphincters; St = stomach.
TABLE II
Preoperative Lengths of the Small lntestlne In the Experlmental Groups
Dogs Group A 1 2 3 4 5 6 Group B
i 8 9 10 11 12 Group C 13 14 15 16 17 18
482
Length of Intestine (cm)
280 224 234.5 300 340 284 296 236 264 264 296 276 272.8 284 288 280.8 240 272
groups were compared, the intestinal transit time showed a statistically significant increase only in those dogs in which two artificial sphincters had been created. Thus, a minimum of two artificial sphincters (at least in the location selected for our experiments) were needed to protect the animals against the massive intestinal resection carried out. Further investigations are needed to determine whether a single artificial sphincter in another location may sufficiently slow the accelerated intestinal transit to provide survival. Perhaps a single, longer artificial sphincter will be as protective as the two sphincters that proved so efficient in the experiment just described. It remains to be ascertained whether only the double interruption of the myenteric plexus causes delay of transit time or also sphincteric length or location. Despite the difficulty of comparing our results and those of other investigators [20,21] because of the substantial differences in the surgical techniques used, we can nevertheless confirm their ultimate conclusion: namely, that intestinal transit time increases with the performance of sufficiently complete myectomies. Summary Artificial sphincters were created in three groups of dogs after the resection of 87.5 percent of the intestine in each animal. Intestinal transit time was measured after 6 weeks by observing the passage of a radiopaque medium through the animals’ intestinal tracts. No statistically significant differences were found between the intestinal transit times of dogs with one artificial sphincter and control animals. In dogs with two artificial sphincters there was
Ths American Journal of Surgery
Delayed Intestinal Transit Time in Dogs
a delay in the radiologically monitored intestinal transit time that was statistically significant compared with that of the control group. References 1. Singleton A0 Jr, Kurris FD, Donegan DW. Increasing absorption following massive resections of the bowel by means of antiperistaltic bowel segments as measured by radioiodine fat absorption studies. Ann Surg 1961;154(suppl):130-2. 2. Martiscelli F, Muritano VM, Spinelli P. Sulle es&se resezioni intestinali sperimentali. Minerva Chir 1963;20:943-6. 3. Baldwin-Price HK, Copp D, Singleton AD. Reversed intestinal segments in the management of anenteric malabsorption syndrome. Ann Surg 1965;161:225-30. 4. Concalves EL, Bevilacqua RG, Machado MCC, et al. Absorcao intestinal apos enterectomias amplas e inversai de segmento de intestino delgado. AMB 1965;11:492-5. 5. Sadowsky J. Experimental investigations on improvement of intestinal absorption in dogs subjected to massive resection of the small intestine combined with use of the onlay reversed segment of the intestine. Bull Pol Med Sci Hist 1967;10:85-92. 6. Tolosa EMC. Utilizacao de segmentos anisoperistalticos de alca intestinal nas enterectomies extensas. Estudo experimental em caes. Thesis, Faculdade de Medlcina da Universidad SHo Paulo, 5&o Paulo, 197 1. Shapiro M. lnterposicao de urn segment0 de cola distal entre cotos remanescentes de intestino delgado apos reseccao de 90 percent do jejuno-ileo. Estudo experimental no cao. Thesis, Escola Paulista de Medicina, SHo Paulo, 1974. Gerwig WHG, Ghaphery A. Experimental attempt to delay alimentary transit after small bowel exclusion. Arch Surg 1963;87:34-41. Altman DP, Ellison EH. Massive intestinal resection: inadequa-
Volume151,April la88
ties of the recirculating loop. Surg Forum 1965;16:365-7. 10. Mackby MI, Richards V, Gilfillan RS, Floridia R. Methods of increasing the efficiency of residual small bowel segments. A preliminary study. Am J Surg 1965;109:32-8. 11. Budding J, Smith CC. Role of recirculating loops in the management of massive resection of the small intestine. Surg Gynecol Obstet 1987;125:243-9. 12. Stahlgren W, Roy RH, Umana G. A mechanical impediment to intestinal flow. Physiological effects on intestinal absorption. JAMA 1964;187:141-4. 13. Schiller WR, DiDio WA, Anderson MC. Production of artificial sphincters. Ablation of the longitudinal layer of the intestine. Arch Surg 1987;95:436-42. 14. DiDio WA, Anderson MC. The sphincters of the digestive system. Baltimore: Williams & Wilkins, 1968. 15. Waddell WR, Kern F, Halgrimson CC, Woodbury JJ. A simple jejunocolic valve for relief of rapid transit and the shortbowel syndrome. Arch Surg 1970;100:434-44. 16. Grier RL. Nelson AW. Lumb WV. Experimental sphincter for short-bowel syndrome. Arch Surg 1971;102:203-8. 17. Stacchini A, DiDlo WA, Primo MLS, Borelli V. Andretto R. Artificial sphincters as surgical treatment for experimental massive resection of small intestine. Am J Surg 1962; 143: 721-6. 18. Kruskal WH, Wallis WA. Use of ranks in one-criterion variance analysis. J Am Stat Assoc 1952;47:583-621. 19. Siegel S. Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill, 1956. 20. Blamer A, Dux A, Sobbe A, Lenz H, Wessel W. Operative Eingriffe zur Verlangsamung der Dunndarmpassage. Tierexperimentelle Untersuchungen. Langenbecks Arch Chir 1972;330:285-306. 21. Hidalgo F, Lopet-Cortes M, Salas SJ, Zavala J. Intestinal muscular layer ablation in short-bowel syndrome in puppies with 90 percent small intestinal resection. Surgery 1971; 70: 189-97.
483
Aldo Stacchini, MD, PhD, SGo Paulo, Brazil Liberato J. A. DiDio, MD, PhD, Toledo, Ohio A. John Christoforidis, MD, PhD, Columbus, Ohio Vicente Borelli, DVM, PhD, S2o Paulo, Brazil
The first successful extensive resection of the small intestine was performed by Koeberle in 1881, and pioneering experimental work in intestinal surgery aimed at treatment of obstructions was accomplished by Senn in 1888. In order to decelerate rapid intestinal transit as a result of massive resection, investigators have created several techniques, such as reversed jejunal segments that are interposed between the remaining stumps [l-6]. Numerous investigations have followed to test reversed segments of the small intestine, colon, and even of the stomach in varied numbers, lengths, and locations, and have produced conflicting results [7,8]. At one point, the use of recirculation loops attracted the attention of surgeons [g-11]; however, the need for an adequate amount of residual loops and the excessive number of anastomoses necessary were limiting factors, and the results did not meet reasonable expectations. The idea of slowing intestinal transit to allow a longer period of contact between absorbable nutrients and the residual intestine after massive resection of the small intestine led to the utilization of artificial sphincters. For the same reason, partial blockage of the intestinal flow by sutures, jejunal wall pleating, inward folding, or by a Teflon@ collar around the gut have been investigated [IZ]. The use of artificial sphincters and the creation of a jejunocolic valve and of an experimental sphincter have also been studied [13-161. From the Department of Anatomy, School of Medicine of Santos, SHo Paulo, Brazil. the Department of Anatomy, Medical College of Ohio, Toledo, Ohio, the Department of Radiology, Ohio State University College of Medicine, Columbus, Ohio, and the Department of Topographic Anatomy, Faculty of Veterinary Medicine, University of SHo Paulo, SHo Paulo, Brazil. Requests for reprints should be addressed to A. John Christoforidis, MD, Department of Radiology, Ohio State University College of Medicine, 410 West 10th Avenue, Columbus, Ohio 43210-1228.
480
In order to evaluate findings from a recent investigation [11] in which the feasibility of artificial sphincters was clearly demonstrated, we decided to measure the transit time of radiopaque medium in the intestine. We attempted to accomplish our goal by comparing the time of the radiologic transit between the duodenum and the rectum; that is, from the moment the radiopaque medium passed the gastroduodenal pylorus to the moment it reached the rectum. The animals used were enterectomized dogs with and without one or two artificial sphincters. The objective was to remove a 1 cm long segment of the longitudinal muscular layer of the intestinal wall while leaving intact the circular muscular layer. With this surgical maneuver, the circular layer could contract without the opposition of the removed longitudinal layer. Material and Methods We used 18 clinically normal mongrel adult dogs (9 male and 9 female) ranging in weight from 11 to 19.6 kg. They were distributed into Groups A, B, and C, each comprising six dogs (three males and three females). All animals underwent resection of 87.5 percent of the small intestine followed by an end-to-end duodenum to ileum anastomosis 10 cm orally to the ileocecal junction. Each group was treated as follows: (1) Group A dogs received an artificial sphincter 1 cm long constructed 5 cm orally from the anastomosis. (2) Group B dogs received two artificial sphincters 1 cm long created 5 cm and 10 cm orally from the anastomosis (Figure 1). (3) Group C dogs served as control animals and no artificial sphincters were created after the massive enterectomy. According to the technique of Stacchini et al [17], sphincters were created by moving circumferentially 1 cm long segments of the longitudinal musculature. This included the mesenteric border of the perimeter and entirely denuded the circular muscular layer. This was per-
The American Journal of Surgery
Delayed Intestinal Transit Time in Dogs
Figure 1. The creation of two artificial sphincters ( S, and S,). The iongitudinaimuscuiar iayer has been removed in two sites so that the circular iayer can contract without opposition.
formed so that ablation of the outer longitudinal muscular layer of the intestine would permit unopposed contraction of the inner circular layer. The longitudinal muscular layer represents the dilating component and the inner circular layer the closing or sphincteric component, thus creating a mechanism similar to a sphincter with the aim of reducing the rate of intestinal flow [13]. At the end of the sixth postoperative week, the dogs were studied radiologically. An image amplification fluoroscopic unit was used to monitor the progress of the contrast medium in the intestinal tract at frequent intervals as necessary. After a 12 hour fast, each animal was initially given 100 ml of barium sulfate by means of an esophageal probe and was immediately observed by fluoroscopy. The duration of radiologic transit was measured from the moment the radiopaque substance passed through the pylorus until its arrival in the rectum, monitored by successive observations made at 5 minute intervals. Radiographs were obtained during the initial and final stages of transit (Figures 2 and 3). The results were tested with the one-way analysis of variance by rank to compare the intestinal transit times in the three groups of dogs [18,19]. This was complemented by the Mann-Whitney test for independent groups [19]. p SO.05 was considered significant.
Figure 2. Radiograph obtained immediate/y after passage of the contrast medium through the pyiorus andinto the duodenum. D = duodenum; P = pyiorus; St = stomach.
To test the homogeneity of the groups with respect to the mean intestinal lengths, the small intestine of the dogs was measured before resection. The results are given in Table II. Using the analysis of variance, homogeneity of the mean intestinal length was confirmed, since the data indicated no statistically significant differences among the groups.
Results We evaluated the intestinal transit time from the pylorus to the rectum in 15 dogs (5 in each group) after resection of 87.5 percent of the length of the small intestine (Table I). The creation of two sphincters significantly delayed the intestinal transit time under the experimental conditions to which the dogs were submitted. The average transit time in Group A was 52 minutes; in Group B, 160 minutes; and in Group C, 50 minutes. One-way analysis of variance by rank demonstrated that the mean transit times of the three groups were significantly different. Group B was significantly different from Groups A and C by the Mann-Whitney U test, whereas the latter two groups did not differ from each other.
Volume 151, April 1966
CDtTltn@tltS The time of intestinal transit, measured from the moment the radiopaque contrast medium passed through the gastroduodenal pylorus until it reached the rectum, was not influenced by variations in the length of the residual intestine, since there were no statistically significant differences among the groups initially. Since resection of 87.5 percent of the total length of the small intestine from all animals was carried out, it is legitimate to consider the residual intestinal segments of the three groups equally homogenous. No deaths occurred during operation, and the median survival of the dogs with two artificial sphincters was longer than the other two groups of animals. When data from the three
481
Stacchini et al
TABLE I
lntestlnal Transit Time After Resection’ Transit Time (min)
Dogs Group A 1 2 3 5 Group B 7 8 9 10 11 Group C 13 14 15 16 17
30 37 52 75 146 214 183 87 172 43 46 54 52 58
Dogs 4, 12, and 18 were excluded because they died before the sixth postoperative week. l
Figure 3. Radlograph obtained at the @aI stage of transit showing arrival of the contrast medium at the rectum. D = duodenum; P = pylorus; Sl, SII = artfflcial sphincters; St = stomach.
TABLE II
Preoperative Lengths of the Small lntestlne In the Experlmental Groups
Dogs Group A 1 2 3 4 5 6 Group B
i 8 9 10 11 12 Group C 13 14 15 16 17 18
482
Length of Intestine (cm)
280 224 234.5 300 340 284 296 236 264 264 296 276 272.8 284 288 280.8 240 272
groups were compared, the intestinal transit time showed a statistically significant increase only in those dogs in which two artificial sphincters had been created. Thus, a minimum of two artificial sphincters (at least in the location selected for our experiments) were needed to protect the animals against the massive intestinal resection carried out. Further investigations are needed to determine whether a single artificial sphincter in another location may sufficiently slow the accelerated intestinal transit to provide survival. Perhaps a single, longer artificial sphincter will be as protective as the two sphincters that proved so efficient in the experiment just described. It remains to be ascertained whether only the double interruption of the myenteric plexus causes delay of transit time or also sphincteric length or location. Despite the difficulty of comparing our results and those of other investigators [20,21] because of the substantial differences in the surgical techniques used, we can nevertheless confirm their ultimate conclusion: namely, that intestinal transit time increases with the performance of sufficiently complete myectomies. Summary Artificial sphincters were created in three groups of dogs after the resection of 87.5 percent of the intestine in each animal. Intestinal transit time was measured after 6 weeks by observing the passage of a radiopaque medium through the animals’ intestinal tracts. No statistically significant differences were found between the intestinal transit times of dogs with one artificial sphincter and control animals. In dogs with two artificial sphincters there was
Ths American Journal of Surgery
Delayed Intestinal Transit Time in Dogs
a delay in the radiologically monitored intestinal transit time that was statistically significant compared with that of the control group. References 1. Singleton A0 Jr, Kurris FD, Donegan DW. Increasing absorption following massive resections of the bowel by means of antiperistaltic bowel segments as measured by radioiodine fat absorption studies. Ann Surg 1961;154(suppl):130-2. 2. Martiscelli F, Muritano VM, Spinelli P. Sulle es&se resezioni intestinali sperimentali. Minerva Chir 1963;20:943-6. 3. Baldwin-Price HK, Copp D, Singleton AD. Reversed intestinal segments in the management of anenteric malabsorption syndrome. Ann Surg 1965;161:225-30. 4. Concalves EL, Bevilacqua RG, Machado MCC, et al. Absorcao intestinal apos enterectomias amplas e inversai de segmento de intestino delgado. AMB 1965;11:492-5. 5. Sadowsky J. Experimental investigations on improvement of intestinal absorption in dogs subjected to massive resection of the small intestine combined with use of the onlay reversed segment of the intestine. Bull Pol Med Sci Hist 1967;10:85-92. 6. Tolosa EMC. Utilizacao de segmentos anisoperistalticos de alca intestinal nas enterectomies extensas. Estudo experimental em caes. Thesis, Faculdade de Medlcina da Universidad SHo Paulo, 5&o Paulo, 197 1. Shapiro M. lnterposicao de urn segment0 de cola distal entre cotos remanescentes de intestino delgado apos reseccao de 90 percent do jejuno-ileo. Estudo experimental no cao. Thesis, Escola Paulista de Medicina, SHo Paulo, 1974. Gerwig WHG, Ghaphery A. Experimental attempt to delay alimentary transit after small bowel exclusion. Arch Surg 1963;87:34-41. Altman DP, Ellison EH. Massive intestinal resection: inadequa-
Volume151,April la88
ties of the recirculating loop. Surg Forum 1965;16:365-7. 10. Mackby MI, Richards V, Gilfillan RS, Floridia R. Methods of increasing the efficiency of residual small bowel segments. A preliminary study. Am J Surg 1965;109:32-8. 11. Budding J, Smith CC. Role of recirculating loops in the management of massive resection of the small intestine. Surg Gynecol Obstet 1987;125:243-9. 12. Stahlgren W, Roy RH, Umana G. A mechanical impediment to intestinal flow. Physiological effects on intestinal absorption. JAMA 1964;187:141-4. 13. Schiller WR, DiDio WA, Anderson MC. Production of artificial sphincters. Ablation of the longitudinal layer of the intestine. Arch Surg 1987;95:436-42. 14. DiDio WA, Anderson MC. The sphincters of the digestive system. Baltimore: Williams & Wilkins, 1968. 15. Waddell WR, Kern F, Halgrimson CC, Woodbury JJ. A simple jejunocolic valve for relief of rapid transit and the shortbowel syndrome. Arch Surg 1970;100:434-44. 16. Grier RL. Nelson AW. Lumb WV. Experimental sphincter for short-bowel syndrome. Arch Surg 1971;102:203-8. 17. Stacchini A, DiDlo WA, Primo MLS, Borelli V. Andretto R. Artificial sphincters as surgical treatment for experimental massive resection of small intestine. Am J Surg 1962; 143: 721-6. 18. Kruskal WH, Wallis WA. Use of ranks in one-criterion variance analysis. J Am Stat Assoc 1952;47:583-621. 19. Siegel S. Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill, 1956. 20. Blamer A, Dux A, Sobbe A, Lenz H, Wessel W. Operative Eingriffe zur Verlangsamung der Dunndarmpassage. Tierexperimentelle Untersuchungen. Langenbecks Arch Chir 1972;330:285-306. 21. Hidalgo F, Lopet-Cortes M, Salas SJ, Zavala J. Intestinal muscular layer ablation in short-bowel syndrome in puppies with 90 percent small intestinal resection. Surgery 1971; 70: 189-97.
483