International Journal of Surgery

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1 International Journal of Surgery 7 (2009) Contents lists available at ScienceDirect International Journal of Surgery journal homepage: A comparison of three single layer anastomotic techniques in the colon of the rat A. Krasniqi a,b, *, L. Gashi-Luci a,b, S. Krasniqi b, M. Jakupi b, Sh. Hashani a,b, D. Limani a,b, I.A. Dreshaj c a University Clinical Centre of Kosova, Department of Abdominal Surgery, Prishtina, Kosovo b University of Prishtina, Faculty of Medicine, Prishtina, Kosovo c Biomedical Research Center, Case Western Reserve University, Cleveland, OH, USA article info abstract Article history: Received 5 September 2008 Accepted 2 October 2008 Available online 18 October 2008 Keywords: Intestinal anastomosis Surgical technique Healing process Intraperitoneal adhesions Introduction: Although intestinal anastomoses are mainly made by staplers, manual anastomoses are still in use worldwide. In previous studies, single layer anastomosis has shown better results compared to double layer techniques. Purpose: To test experimentally some aspects of three different single layer anastomotic techniques in order to identify advantages and disadvantages of each. Material and methods: The study was done on Sprague Dawley rats. Animals were randomly divided into four groups. Three experimental groups consisted of 21 animals each, and the fourth sham group contained 10 animals. By 7 animals of each group were sacrificed on the 4th and the rest of 14 animals on the 7th postoperative day. In all groups the resected distal part of the colon was anastomosed using Halsted, Gambee and Gambee Halsted technique. To evaluate each specific technique the following were used: postoperative complication frequency, biomechanical measurements, adhesion density, condition of intestinal lumen and histological parameters of the healing process. Results: The complication frequency was not significantly different between the tested techniques. The average bursting pressure and tensile strength were higher on both the 4th and 7th postoperative days with the Gambee technique. In the colon segments removed on the 4th postoperative day 97% of pressure induced ruptures occurred in the anastomotic line, whereas on the 7th postoperative day 76% of ruptures occurred about 1 cm distal to the anastomotic line. Conclusion: The Gambee technique had significantly better biomechanical and histological results compare to the other two anastomotic techniques. Adhesion density was significantly lower in the control group (p < 0.001). Ó 2008 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved. 1. Introduction Intestinal anastomosis is a basic procedure in gastrointestinal surgery. There is still interest in research on intestinal anastomosis because failed anastomosis is associated with high morbidity and mortality rates. 1,2 Although intestinal anastomosis has been practiced for centuries, there still exist among the surgeons different opinions about the preferred type of anastomotic technique. In developed countries intestinal anastomosis is mainly performed by staplers, however, manual anastomoses are still in use worldwide. 3 * Correspondence to: Avdyl Krasniqi, University Clinical Center of Kosova, Department of Abdominal Surgery, Prishtina, Kosovo. Tel.: þ , þ , þ (mobile); fax: þ address: dr_krasniqi2001@yahoo.com (A. Krasniqi). Anastomotic technique represents an important chain of successful healing of anastomosis. 4 Although double layer anastomosis is preferred by many surgeons, in our previous studies and studies of other authors, single layer anastomosis has shown better results. 5 8 The aim of this study was to test experimentally some important aspects of three different single layer anastomotic techniques in order to identify advantages and disadvantages of each. 2. Material and methods The research was done on Sprague Dawley rats of both genders. Animals were randomly divided into four groups. The experimental (three) groups consisted of 21 animals each, whereas the fourth sham operated group contained 10 animals (Table 1). All animals underwent surgical procedure under general anaesthesia induced by intraperitoneal administration of ketamine HCl (Animal Health, /$ see front matter Ó 2008 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved. doi: /j.ijsu

2 32 A. Krasniqi et al. / International Journal of Surgery 7 (2009) Table 1 General characteristics of animals. Group Type of Anastomosis Group size Gender ratio F:M I Halsted 21 10: II Gambee 21 10: III Gambee/Halsted 21 7: IV Sham operated 10 5:5 291 Total 73 32: Average weight (gr) Fort Dodge, USA) 70 mg/kg and xylazine (The Butler Company, Columbus, Ohio) 7 mg/kg. The inferior midline laparotomy and resection of distal colon were performed in all animals of the experimental group. The continuity of colon was reestablished with end to end anastomosis according to Halsted in the first group, according to Gambee in the second group and with combined Gambee Halsted techniques in the third group (the posterior wall was anastomosed according to Gambee and the anterior wall according to Halsted). All anastomoses were done with sutures PDS II 6.0 (Ethicon, Inc.). In the sham operated animals inferior midline laparotomy and closure of abdominal wall similarly to other groups were performed without resection of colon. After surgery animals were left on ad libitum water and food. In each experimental group 7 animals were sacrificed on the 4th and, 14 others on the 7th postoperative day. Local intraperitoneal findings were checked, and adhesions dissected carefully. After the identification of anastomosis, a 5 cm segment of colon with the anastomosis in the middle was resected. To evaluate the results the following were used: postoperative complication frequency, biomechanical measurements, adhesion density, status of intestinal lumen and histological parameters of healing process. Postoperative complications included microperforation, dehiscence, stenosis of anastomosis, per secundum healing of laparotomy, incisional hernias and density of intraperitoneal adhesions. As stenotic anastomoses were arbitrarily considered those where the lumen upstream from anastomosis was twice larger than that downstream the anastomosis. The endoluminal status was evaluated by the degree of mucosal necrosis, oedema of anastomotic line and measurement of circumference of anastomotic line (Fig. 1). Adhesion density was graded from 0 to 4 according to Knightly et al. 9 (Fig. 2). To test anastomotic strength, the bursting pressure (BP) and tensile strength (TS) were measured. Bursting pressure was measured in vitro on a 5 cm segment of colon with the anastomosis in the middle. An infusion pump driven at constant speed inflated 2 ml/min of saline with methylene blue until the colonic segment ruptured. Pressure change was registered digitally and graphically by Buxco, Biosystem XA, Buxco Electronics, Inc. The BP was marked by an abrupt drop in the pressure curve as well as by the methylene blue appearance in the bathing medium. A longitudinally resected 0.7 cm wide colon strip containing the anastomotic line was used for measurement of minimal tensile strength. Minimal tensile strength was tested by dynamometer (Harvard Apparatus, Model 906, Millis, Massachusetts, USA) moving at a constant speed of 10 mm/min and measured by Validyne, Model MC (Engineering Corporation, Northridge, California, USA). The start of the drop in the tension curve (initial breakage) was marked as TS. Cellular and architectural parameters of anastomotic healing were scored according to the semi-quantitative method modified by Verhofstad et al. 10 Statistical analysis of results was done using t test and Mann-Whitney sum rank test provided in the Sigma Stat 2000 software. 3. Results The complication frequency was similar in both of the first two groups. However, in all groups complications were related to the abdominal wall rather than to the healing process of the anastomosis. There was no anastomotic dehiscence. Most often encountered complications consisted of per secundum healing of the abdominal wall, intraperitoneal adhesions and incisional hernias. The average bursting pressure and tensile strength were higher in the Gambee group (Table 2) compare to the other two groups. On the 7th postoperative day the rupture induced by increase in the intraluminal pressure in 76% of cases occurred approximately 1 cm distal to the anastomotic line, 69% of cases on the antemesocolic side. On the 4th postoperative day 97% of ruptures occurred on the anastomotic line. The biomechanical parameters (BP, TS) were significantly higher in all groups on the 7th than on the 4th postoperative day (p < 0.001). Histological evaluation showed that anastomoses done by the Gambee technique in almost all parameters such as anastomotic necrosis, polymorphonuclear cells infiltration, edema, epithelial recovery and repair of submucosal-mucosal layer demonstrated Fig. 1. Endoluminal macroscopic view of anastomotic line; Halsted, Gambee and Gambee Halsted.

3 A. Krasniqi et al. / International Journal of Surgery 7 (2009) Fig. 2. Adhesion density grades: 0 - no adhesions (a), 1-one easy dissectible adhesion (b), 2 - moderately extended adhesions without intestinal lifting (c), 3- adhesions extended between intestine and parietal peritoneum (d) and 4 extensive adhesions attached to the large and the small bowel as well as the parietal peritoneum. a better score, closer to ideal healing (Fig. 2). Also, macroscopic evaluation indicated that on the anastomotic line mucosa was abridged better with less local edema in the Gambee technique group (Fig. 3). 4. Discussion This study was undertaken to experimentally compare some aspects of the most commonly used single layer anastomotic techniques such as Halsted, Gambee and combined Gambee Table 2 Biomechanical parameters, Knightly score and overall complication frequency. Type of anastomosis Bursting Pressure (mmhg) Tensile Strength (g/mm of strip) Knightly score Halsted Gambee Gambee Halsted Overall complication frequency (%) Halsted technique. The study was focused on the following aspects: endoluminal and extra luminal macroscopic appearance of the anastomotic line, perianastomotic adhesion density, the bursting pressure and the tensile strength of the anastomosis and histological changes during the early phase of healing. There have been numerous clinical and experimental studies done on surgical techniques and the healing process of intestinal anastomosis Traditionally, two main surgical sutures have been used to perform manual intestinal anastomosis: double and single layer sutures. 1,2 Although nowadays the intestinal anastomoses are mainly made by staplers, training of surgeons on manual anastomosing is still very much needed, especially in developing countries. There are different preferences among the surgeons regarding the use of surgical techniques for creating the intestinal anastomosis. The majority of studies uniformly favor single layer in preference to double layer anastomoses. 5 9,12,13 The single layer anastomosis was first described by William. 14 Since then, different single layer anastomotic techniques have been invented. 1,12 18 Connell described his continuous inverting suture in Single layer continuous suture was reported later on by many authors

4 34 A. Krasniqi et al. / International Journal of Surgery 7 (2009) Fig. 3. Hematoxylin-eosin stained sections of anastomosis: 0 minimal necrosis and edema, normal PMN, macrophage, and lymphocytic celullarity; 3 extensive necrosis and other cellular changes. In 1951 Gambee designed a stitch that apposed both the serosa and the mucosa, forming a single layer anastomosis. 1,15 All of these techniques in essence create inverted intestinal anastomosis. They differ in using either interrupted or continuous sutures and whole intestinal wall thickness sutures or extra mucosal sutures. There are only few comparative studies that favor particular single layer anastomosis. In the present study, we focused on some aspects of the healing process of intestinal anastomosis in the period between days 3 and 7 which is characterized by restoration of the matrix accumulation and the strength. 19 Therefore, we sacrificed the animals on postoperative days 4 and 7. Endoluminally, the macroscopic appearance of anastomotic line was quite similar in specimens of all groups on the 4th postoperative day, however on the 7th postoperative day, in the Gambee group was found less edema in the anastomotic line and better mucosal coverage compared to other two groups (Fig. 1). This probably was due to, better apposition of intestinal layers, less narrowing of the lumen and a smaller amount of strangulated tissue. 20,21 Another aspect analyzed in our study was the density of intraperitoneal adhesions. The density of the intraperitoneal adhesions was quantified according to Knightly et al., 9 from grade 0to4(Fig. 2). Our results showed that there was not a significant difference in the intraperitoneal adhesion development depending on the type of anastomosis neither on the day of animal sacrifice. However, we found a statistically significant difference compared to the sham operated group (p < 0.001). DeCherney and dizerega, 22 Ellis, 23 and Holdahl et al. 24 also reported that adhesions are present more often in anastomosis and potentially are caused by the contamination of the peritoneal area, sutures as foreign material and ischemic changes of the intestine in the anastomotic region Bursting pressure and tensile strength were significantly higher in the 7th compared to the 4th postoperative day in all groups (p < 0.001, p < 0.005, p < 0.005). A significant increase of the biomechanical parameters of the anastomotic line between postoperative days 3 and 7 has been demonstrated in other studies as well. 18,19,25 Seifert et al. 19 have found a significant increase of vascular and perfusion areas in anastomotic region 7 days after surgery. They have confirmed the importance of angiogenesis and other concomitant changes that increase the strength of anastomosis after the first 3 days. The rapid increase of strength in anastomotic line on the 7th postoperative day, 19 even higher than in an intact colon, is also supported by the fact that 76% of ruptures in our experiment occurred approximately 1 cm downstream the anastomotic line, whereas, on the 4th postoperative day 97% of ruptures occurred on the anstomotic line. Cellular and architectural parameters of the anastomotic healing were evaluated on hematoxylin-eosin stained sections. We have adopted the method modified by Verhofstad et al., 10 where ideal healing is scored with 0 on the scale from 0 to 3 (Fig. 3). Analyzed changes, such as presence of necrosis, polymorphonuclear infiltration, edema, epithelial recovery and repair of submucosal-muscular layer, have shown that Gambee technique histologically was closer to the ideal healing compare to the other two techniques. The results of present study indicate that the Gambee technique has shown better biomechanical and histological parameters on both, the 4th and the 7th postoperative days compared to the two other techniques tested in this study. Conflicts of interest None declared. Funding Research was partly funded by the Department of Science, Ministry of Education, Science and Technology of Kosovo. Ethical approval Project was approved by Scientific Council and Ethical Committee of Faculty of Medicine, University of Prishtina, Prishtina Kosovo; December References 1. Ballantyne GH. The experimental basis of intestinal suturing; effect of surgical technique, inflamation, and infection on enteric healing. Dis Colon Rectum 1984;27: Thornton FJ, Barbul A. Healing in the gastrointestinal tract. Clin North Am 77:

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