Serosal patching refers to the placement and suturing of 2 serosa-covered organs in direct serosal-to-serosal contact with each other to effectively create full-thickness coverage of a compromised area or defect.1–3 Serosal patches have been shown to provide mechanical support and a fibrin seal that creates early complete coverage of a visceral defect.3–5 Most veterinary reports6–10 have focused on intestine-to-intestine repairs as reinforcement of primary closures when local tissue viability was questionable or other risk factors for dehiscence, such as preoperative septic peritonitis, hypoalbuminemia, and hypotension, were present. Intestinal serosal patches have also been used in people and animals to cover and seal open intestinal defects without primary closure in both clinical and research settings2,4,6,11 and to supplement urinary bladder closures or defects in animals.6,12 In some instances, large defects of the intestinal wall cannot be repaired by primary closure without a high risk of creating a partial obstruction because of luminal narrowing.13
Numerous techniques have been described to patch large, open duodenal defects in dogs and rabbits, including jejunal serosal patch, gallbladder mucosal patch, jejunal pedicle flap, expanded polytetrafluoroethylene patch, and transverse abdominis musculoperitoneal flap.5,6,14–16 Neomucosa formation was confirmed histologically within 6 weeks after repair, and short-term survival rates were high regardless of the technique performed.4,5,14,15 However, the effectiveness of these techniques in clinical animals has not been reported. Omental patches have also been described in dogs, but these repairs are at risk of long-term stricture and loosening with subsequent leakage.13 Crowe6 included a description of a surgical technique in 12 animals that had open organ defects, including of the small intestine, that were sealed with intestinal serosal patches; however, reports that included reevaluation of this technique have not been found, and this technique is not considered a first-line treatment.
The primary objective of the study reported here was to determine whether a jejunal serosal patch could securely seal a large, open duodenal defect and prevent leakage at physiologic intraluminal pressures. The secondary objective was to compare ILPs and MIPs for duodenal segments that have been anastomosed with jejunal serosal patches and a simple continuous or simple interrupted suture pattern. Jejunal serosal patches were expected to adequately seal the duodenal defects and to withstand supraphysiologic intraluminal pressures regardless of suture pattern. Initial leakage pressures and MIPs for the repaired duodenal segments were not expected to differ significantly between suture patterns.
Materials and Methods
Specimens
The small intestines from nine 20- to 25-kg purpose-bred dogs were harvested immediately after euthanasia with IV infusion of pentobarbital.a All dogs were healthy on the basis of physical examination, were < 1 year of age, and had been euthanized for reasons unrelated to this study. Study approval by the institutional animal care and use committee was not required by our institution. Collection and subsequent testing were performed in 2 sessions; intestines were harvested from 5 dogs for the first session and 4 for the second.
The small intestine of each dog was first cut into 60-cm segments, beginning from just aboral to the pylorus to the proximal third of the jejunum. Then, from these 60-cm segments, 3 duodenal and 3 jejunal segments of approximately 10 cm each were obtained. A jejunal segment was used to repair a defect in the duodenal segment from the same dog. Segments were copiously rinsed with tap water to remove residual intraluminal content before being placed in a sterile saline (0.9% NaCl) solutionb until construct creation.
Full-thickness defects were created in 20 duodenal segments. One duodenal segment was left intact for each of the 2 sessions. Each segment designated for defect creation was placed flat on the work surface, and its diameter was measured with a ruler. A penc was used to place dots along the segment's wall to mark the defect's dimensions: a width of 50% of the diameter of the segment and length of 5 cm (Figure 1). Then, starting on the antimesenteric border, Metzenbaum scissors were used to create the defect. Because the diameter of the intestinal segments differed, defect size varied but defect width of all segments remained at 50% of the segment diameter. Twenty segments were randomly assigned by coin flip to have the defect sealed with a serosal patch with a simple continuous suture pattern or simple interrupted suture pattern. When 10 constructs were assigned to one group, the remaining constructs were assigned sequentially to the other group.
Photographs of a segment of duodenum harvested from 1 of 9 canine cadavers for intraluminal pressure testing after creation of a duodenal defect and repair with a jejunal serosal patch with 1 of 2 suture patterns. A—Intact duodenal segment prior to defect creation, with a ruler positioned perpendicular to the segment to estimate the segment's diameter (approx 2.5 cm). B—Defect created by excision of tissue approximately 50% of the segment's diameter (approx 1.25 cm). C—A ruler positioned parallel to the segment in B indicates the length (approx 5 cm) of the defect. Pen marks on the segment guided defect creation.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs of a segment of duodenum harvested from 1 of 9 canine cadavers for intraluminal pressure testing after creation of a duodenal defect and repair with a jejunal serosal patch with 1 of 2 suture patterns. A—Intact duodenal segment prior to defect creation, with a ruler positioned perpendicular to the segment to estimate the segment's diameter (approx 2.5 cm). B—Defect created by excision of tissue approximately 50% of the segment's diameter (approx 1.25 cm). C—A ruler positioned parallel to the segment in B indicates the length (approx 5 cm) of the defect. Pen marks on the segment guided defect creation.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs of a segment of duodenum harvested from 1 of 9 canine cadavers for intraluminal pressure testing after creation of a duodenal defect and repair with a jejunal serosal patch with 1 of 2 suture patterns. A—Intact duodenal segment prior to defect creation, with a ruler positioned perpendicular to the segment to estimate the segment's diameter (approx 2.5 cm). B—Defect created by excision of tissue approximately 50% of the segment's diameter (approx 1.25 cm). C—A ruler positioned parallel to the segment in B indicates the length (approx 5 cm) of the defect. Pen marks on the segment guided defect creation.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Surgical method
Serosal patch constructs were created by repairing the duodenal defects with circumferential suturing of an intact, apposed jejunal segment (Figure 2). For all constructs, the first bite of the line closure was taken at the antimesenteric border of the duodenal segment, leaving a cuff of tissue that extended approximately 2 mm from the exit point of the suture bite to the defect edge. The suture pattern was continued with full-thickness bites, intentionally incorporating the submucosa of both segments. Bites were placed every 2 to 3 mm, and the same cuff was maintained circumferentially. Each defect was completely sealed by starting a second, independent continuous suture line from the opposing antimesenteric border with a separate needle and suture or by completion of the interrupted sutures circumferentially. For the continuous pattern, the tags of each starting knot were left long and clamped with mosquito forceps that were used as anchors to stabilize the construct. The forceps were placed on the working surface, and no intentional tension was applied to them. When completed, the end of each line was tied to the suture tag of the opposite knot with square knots, so as to have only 2 knots/construct, and the suture ends were cut with Mayo scissors. In all constructs, 4-0 glycomer 631 with a swagged CV-25 half-circle, 22-mm tapered needled was used. Each construct was visually inspected after suturing, and additional simple interrupted sutures were placed in areas where spacing was judged to be > 2 to 3 mm. When completed, all constructs were placed in saline solution to avoid desiccation and refrigerated at 4°C overnight until pressure testing.17–20
Photographs showing apposition of a jejunal serosal patch onto a duodenal defect of one of the specimens in Figure 1 with a circumferential, full-thickness simple continuous (A) or simple interrupted (B) suture pattern, with a 2-mm tissue cuff and 2- to 3-mm bite spacing. A pair of mosquito forceps was used to clamp the free end of the suture knot so countertension could be applied along the suture line during suturing (panel B).
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs showing apposition of a jejunal serosal patch onto a duodenal defect of one of the specimens in Figure 1 with a circumferential, full-thickness simple continuous (A) or simple interrupted (B) suture pattern, with a 2-mm tissue cuff and 2- to 3-mm bite spacing. A pair of mosquito forceps was used to clamp the free end of the suture knot so countertension could be applied along the suture line during suturing (panel B).
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs showing apposition of a jejunal serosal patch onto a duodenal defect of one of the specimens in Figure 1 with a circumferential, full-thickness simple continuous (A) or simple interrupted (B) suture pattern, with a 2-mm tissue cuff and 2- to 3-mm bite spacing. A pair of mosquito forceps was used to clamp the free end of the suture knot so countertension could be applied along the suture line during suturing (panel B).
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Pressure testing
Pressure testing was performed with a previously described technique.17 Briefly, after purging the constructs of fluid with digital pressure, the ends of each duodenal segment were sealed with Rochester-Carmalt forceps and the ends of each jejunal segment were sealed with Kelly forceps. Forceps were attached to ring stands, such that each construct was suspended. One 14-gauge, 2-inch-long IV cathetere was inserted into each end of the duodenal lumen (Figure 3). The catheter inserted into 1 end of the duodenal lumen was connected by IV tubing to an infusion pumpf set to infuse saline solution at 900 mL/h. Dyeg was added to the saline solution (dilution 1:250) to improve detection of ILP. The catheter inserted into the other end of the duodenal lumen was attached to a 3-way connecting adapter created for the purpose of this study. A microtip pressure transducerh was introduced into the duodenal lumen through one of the ports of the adapter, extending 0.5 cm beyond the tip of the catheter. The adapter was screwed tightly to the transducer to prevent leakage around the transducer. The other end of the pressure transducer was connected to a data acquisition system.i The other ports of the connecting adapter were occluded to prevent leakage.
Photographs of a duodenal segment from one of the canine cadavers in Figure 1 without a defect or jejunal serosal patch (control segment) that was placed in the apparatus for pressure testing. A—In this view from the side, segment ends are sealed with Rochester-Carmalt forceps attached to ring stands, such that the segment is suspended. One 14-gauge, 2-inch-long IV catheter is within the lumen at each end of the duodenal segment. B—In this view from above, the catheter on the left side of the photograph was connected by IV tubing to an infusion pump set to infuse saline (0.9% NaCl) solution at a rate of 900 mL/h. The catheter on the right side of the photograph was attached to a 3-way connecting adapter. A microtip pressure transducer (asterisk) is introduced into the duodenal lumen through one of the ports of the adapter, extending 0.5 cm beyond the tip of the catheter.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs of a duodenal segment from one of the canine cadavers in Figure 1 without a defect or jejunal serosal patch (control segment) that was placed in the apparatus for pressure testing. A—In this view from the side, segment ends are sealed with Rochester-Carmalt forceps attached to ring stands, such that the segment is suspended. One 14-gauge, 2-inch-long IV catheter is within the lumen at each end of the duodenal segment. B—In this view from above, the catheter on the left side of the photograph was connected by IV tubing to an infusion pump set to infuse saline (0.9% NaCl) solution at a rate of 900 mL/h. The catheter on the right side of the photograph was attached to a 3-way connecting adapter. A microtip pressure transducer (asterisk) is introduced into the duodenal lumen through one of the ports of the adapter, extending 0.5 cm beyond the tip of the catheter.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Photographs of a duodenal segment from one of the canine cadavers in Figure 1 without a defect or jejunal serosal patch (control segment) that was placed in the apparatus for pressure testing. A—In this view from the side, segment ends are sealed with Rochester-Carmalt forceps attached to ring stands, such that the segment is suspended. One 14-gauge, 2-inch-long IV catheter is within the lumen at each end of the duodenal segment. B—In this view from above, the catheter on the left side of the photograph was connected by IV tubing to an infusion pump set to infuse saline (0.9% NaCl) solution at a rate of 900 mL/h. The catheter on the right side of the photograph was attached to a 3-way connecting adapter. A microtip pressure transducer (asterisk) is introduced into the duodenal lumen through one of the ports of the adapter, extending 0.5 cm beyond the tip of the catheter.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Immediately before pressure testing, the pressure transducer was calibrated and the recording of pressure measurements and infusion of the saline solution were initiated. Initial leakage pressure was defined as the pressure at which the saline solution was first observed to leak from the constructs. However, if leakage was noted at the needle holes where suture exited the duodenal wall or if the pressure tracing did not detect a plateau or decrease in pressure, the pressure at which this type of leakage occurred was not recorded as the ILP. After the ILP was recorded, testing continued until the serosal patch catastrophically failed, intraluminal pressure reached a plateau for 10 seconds, or the pressure transducer reached the maximum detectable pressure (250 mm Hg). Pressures at which any of the aforementioned events occurred were recorded as MIPs. All constructs were tested once in random order, regardless of group assignment. For each session, the control segment (duodenal segment without defect and serosal patch) was tested first to determine whether the pressure-testing apparatus functioned as desired and whether the harvested duodenal segment was feasible to use for pressure testing. On the basis of a previous study,21 maximum physiologic intraluminal pressure was 25 mm Hg.
Elapsed time between euthanasia and the completion of construct testing was < 17 hours for all constructs, regardless of session. One author (ML) created all defects, performed all repairs, and recorded the data. The other author (DDS) supervised the creation of the constructs for repair technique approbation.
Statistical analysis
Normality of data distribution was assessed by use of the Shapiro-Wilk test, and normally distributed data were reported as mean ± SD. The ILP and MIP data were normally distributed; therefore, a paired t test was used to compare the ILPs and MIPs between suture patterns. All analyses were performed with commercially available statistical software.j Values of P < 0.05 were considered significant.
Results
The control segments tested during each session withstood intraluminal pressures comparable to those previously published.20,22 All constructs withstood supraphysiologic pressures (> 25 mm Hg). However, 1 construct with a simple interrupted suture pattern had a suture disengage from the duodenal segment, leading to an ILP of 43 mm Hg; this result was an outlier, and therefore, it was not included in the data analysis. Therefore, data were analyzed from 10 constructs that had the jejunal serosal patch anastomosed to the duodenal segment by a simple continuous suture pattern and 9 by a simple interrupted suture pattern.
Initial leakage pressure significantly (P = 0.008) differed between the continuous (mean ± SD, 59.8 ± 20.03 mm Hg) and interrupted (68.89 ± 5.62 mm Hg) suture groups (Figure 4). All constructs, regardless of suture pattern, leaked from in between the suture holes, with mild serosal tearing from the duodenal segment. Negligible leakage was noted at the holes where suture exited the intestinal wall in 1 construct with the simple continuous suture pattern and 2 constructs with the simple interrupted suture pattern. Maximum intraluminal pressure did not significantly (P = 0.96) differ between the suture patterns (simple continuous, 90.7 ± 16.91 mm Hg; simple interrupted, 91 ± 8.27 mm Hg; Figure 5). All constructs failed with progression of the previously identified serosal tearing from the duodenal segment. In the 2 control segments, the attained intraluminal pressures were greater than that for which the pressure transducer could record (> 250 mm Hg), so specific pressures at which they failed could not be recorded. For both control segments, failure of the system occurred from catheter pullout from the duodenal lumen; serosal tearing was identified, but no leakage from those tears was observed.
Box-and-whisker plots of ILP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. The horizontal line within each box represents the median, boxes represent the interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Box-and-whisker plots of ILP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. The horizontal line within each box represents the median, boxes represent the interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Box-and-whisker plots of ILP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. The horizontal line within each box represents the median, boxes represent the interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Box-and-whisker plots of MIP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. See Figure 4 for key.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Box-and-whisker plots of MIP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. See Figure 4 for key.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Box-and-whisker plots of MIP recorded for the duodenal segments in Figure 1 after pressure testing of a duodenal segment with a defect repaired with a jejunal serosal patch anastomosed by a simple continuous or simple interrupted suture pattern. See Figure 4 for key.
Citation: American Journal of Veterinary Research 81, 12; 10.2460/ajvr.81.12.985
Discussion
The purposes of the study reported here were to determine whether a jejunal serosal patch could securely seal a large, open duodenal defect and prevent leakage at physiologic intraluminal pressures and to compare ILPs and MIPs between duodenal segments with serosal patches anastomosed to the segments’ defects with a simple continuous suture pattern and those with a simple interrupted suture pattern. The results of the present study confirmed that duodenal segments with repaired defects were able to withstand supraphysiologic intraluminal pressures (> 25 mm Hg). All constructs, regardless of suture pattern, eventually leaked, however. Although ILP and MIP were not expected to differ significantly between suture patterns, ILP did differ significantly.
Previous reports18–20 in the veterinary literature have documented intestinal leakage pressures in a similar setting as for the present study. The ILP obtained in the present study was higher than those obtained for constructs of intestine anastomosed with suture or staples.18,19 In another study,20 higher ILP was achieved in enterectomy constructs supplemented (vs not supplemented) by a jejunal serosal patch (81.8 ± 6.7 mm Hg vs 28 ± 6.7 mm Hg). Additionally, researchers have recently reported17,22 that leakage pressures of closed intestinal enterotomies in pigs and dogs are similar to those obtained in the present study. These reports17,22 also indicate that tissue processing prior to construct testing significantly impacts ILP, such that fresh and chilled tissues have higher ILPs than frozen tissues. Therefore, time elapsed from tissue collection to pressure testing in the present study was short (< 17 hours), and tissues were kept cold (4°C) and not frozen.
Initial leakage pressures differed significantly between suture patterns in the present study. Jejunal serosal patches anastomosed to duodenal defects by a simple interrupted suture pattern had higher ILP, similar to the results of another study.23 Results, however, contradicted a recent study24 that revealed a higher ILP with a simple continuous pattern versus a simple interrupted pattern in a double-layer, esophagotomy closure in a pig. Duodenal segment defect repair with a simple interrupted pattern may have leaked at higher pressures in the present study because simple interrupted (vs simple continuous) closure consistently provided a tighter seal. Knot tying at every bite may have created a tighter seal around the defect as well as more uniform spacing, especially along the curved sections of the closure. Maintaining even, firm tension on the continuous suture line was challenging, especially when suturing around the curved portion of the closure. Use of barbed suture that prevents loosening between suture bites in a continuous suture line may help to maintain firm tension and result in a tighter seal.19
One construct with simple interrupted closure leaked at a lower pressure compared with the other constructs of this group, despite that the construct was made correctly, included tissue of adequate thickness, appeared similar to the other constructs before and after testing, and was appropriately stored. Also like the other constructs, that construct leaked in between sutures; however, 1 knot disengaged from the duodenal segment as intraluminal pressure increased. Likely, the needle for at least one of the bites did not penetrate the submucosa and only included the seromuscular layer, such that the suture subsequently tore out prematurely. This occurrence highlighted the importance of including the submucosa when suturing the intestinal wall. The submucosa has been shown to provide the greatest mechanical strength in intact and anastomosed intestine.25 Despite ongoing leakage, the remainder of the construct was strong and able to reach similar MIP (75 mm Hg) as the other constructs. Although the construct otherwise withstood supraphysiologic intraluminal pressures, the data for this construct were removed from analysis because of their impact on the results (data not shown).
The purpose of a jejunal serosal patch for the repair of an open intestinal defect is to provide a strong, leakproof, autologous mechanical barrier capable of withstanding physiologic intraluminal pressures. To achieve this goal, the technique described in the present study abided by several described26,27 intestinal repair principles, including incorporating the submucosa in every bite and bite spacing at 2 to 3 mm. A circumferential 2-mm cuff was preferred over suturing within the defect because of the expected inflammatory cascade and subsequent debridement phenomenon at the wound edges in a live dog, with the latter leading to possible suture pull-through and loosening.26
Unlike human medicine, in which penetrating trauma is the leading cause for damage to the proximal portion of the duodenum,28 duodenal ulcers secondary to NSAIDs, liver disease, neoplasia (eg, mast cell tumor and gastrointestinal lymphoma), and inflammatory bowel disease are the leading causes in veterinary medicine.26 Minor duodenal defects can be closed primarily, whereas those located near the pyloroduodenal junction can be fully repaired with a Y-U pyloroplasty. However, defects of more distal portions of the duodenum with major tissue loss have limited and challenging surgical options. This situation is a prime indication for use of a serosal patch, such that more technically demanding and time-consuming duodenal diversion procedures (eg, Billroth II and Roux-en-Y) and their related serious complications can be avoided.29,30
Limitations of the present study included the use of ex vivo constructs and a nonphysiologic test method. Also, using resistance to intraluminal pressure as the sole factor to predict surgical success greatly oversimplified intestinal healing. Numerous additional factors not evaluated in the present study are also important to achieve complete intestinal defect healing.26 One clinical report6 of veterinary patients and several studies4,5,14,15 with dogs indicate that complete defect healing is possible when the defect is appropriately sealed. Intestines from cadavers will inevitably behave differently than intestines in live animals. Yet the present study's methodology was such that a short time elapsed from euthanasia to construct testing and each construct was stored cold, rather than frozen, to minimize the impact of tissue breakdown, which could have impacted pressure measurements.17,22
A jejunal serosal patch adequately sealed large, open duodenal defects and prevented leakage at supraphysiologic intraluminal pressures in duodenal segments harvested from canine cadavers. Repaired duodenal segments with simple continuous or simple interrupted suture patterns adequately withstood physiologic intraluminal pressures, although the duodenal segments repaired with a simple interrupted suture pattern withstood higher ILPs. Use of a jejunal serosal patch to repair large, open duodenal defects in canine patients is cautioned before in vivo testing has been demonstrated to yield successful outcomes.
Acknowledgments
No external funding was used in this study. Suture material was provided by Covidien.
The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| ILP | Initial leakage pressure |
| MIP | Maximum intraluminal pressure |
Footnotes
Beuthanasia-D, Schering-Plough Animal Health, Kenilworth, NJ.
Saline, Hospira Inc, Lake Forest, Ill.
Devon surgical skin marker, Covidien Animal Health, Mansfield, Mass.
Biosyn, 4-0 USP, Covidien Animal Health, Mansfield, Mass.
14-gauge IV catheter, Nipro Medical Corp, Doral, Fla.
Harvard Apparatus, Holliston, Mass.
Blue food dye, Market Pantry, Minneapolis, Minn.
Mikro-Tip catheter transducer, Millar Instruments Inc, Houston, Tex.
SonoLab, Sonometrics Corp, London, ON, Canada.
JMP, Cary, NC.
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