Intestinal tumors account for approximately 3% to 10% of all canine tumors. Rectal neoplasia, although a small subset of this population, can present a significant treatment challenge.1–4 The primary treatment option for benign and malignant rectal tumors is surgical excision, especially for solitary lesions. Surgical options for rectal mass excision in canines are largely dependent on location and rectal wall invasiveness. Historical techniques include endoscopic resection, electrosurgery, cryosurgery, rectal pull-through, and pelvic osteotomy via laparotomy.5–7 These techniques are associated with potentially severe complications such as stricture, dehiscence, and fecal incontinence.7,8 Due to the high morbidity associated with these complications, there is a need to explore minimally invasive options to obtain either a diagnosis, palliation, or curative intent with benign or slowly growing masses.1,9
Cantatore et al10 have shown that submucosal resection of both benign and malignant rectal masses was associated with a low rate of severe complications and prolonged survival in their patient population. There was no difference in disease-free survival between benign tumors and carcinomas in situ, benign tumors and carcinomas, or carcinomas in situ and carcinomas. There was also no difference in overall survival when comparing benign tumors and carcinomas in situ, but overall survival was longer for benign tumors over carcinomas.
Transanal minimally invasive surgery (TAMIS) was first described in human colorectal surgery in 2010 by Atallah et al11 with the use of a single-incision access port (SILS port; Medtronic). Transanal minimally invasive surgery is defined as the use of any multichannel port transanally, combined with the use of routine laparoscopic instruments, a laparoscopic camera, and a standard laparoscopic CO2 insufflator to perform endoluminal surgery.12 This novel technique requires minimal setup duration, low equipment cost, and the use of existing laparoscopic instruments.11 Since its inception it has become the most common technique for local excision of rectal neoplasia in human colorectal surgery.12
Transanal minimally invasive surgery has been recently described in the veterinary literature as a feasible minimally invasive alternative for rectal surgery in canines.9 The single access port from Medtronic (SILS port; Medtronic) has been approved for transanal surgery in humans12 and has been reported as an option for transanal access for canine colonoscopy.13 It provides adequate visualization of the rectal and colonic mucosa, constant insufflation of the colon, and is easier to perform with fewer personnel compared with other transanal endoscopic approaches.13 Benefits of the SILS port include economic feasibility and resterilization ability.14 The thermoplastic elastomer material allows for safe and atraumatic transanal access in dogs. The pliability of the port allows for its quick removal and reintroduction as needed.11
Previous studies have investigated the feasibility of TAMIS in humans and canines with insufflation pressures ranging from 2 mmHg to 25 mmHg and 8 mmHg to 10 mmHg, respectively.9,13,15 To the authors’ knowledge, however, no studies have documented which insufflation pressures provide the optimal working environment for TAMIS in dogs. To optimize visualization, ease of dissection, and suturing during TAMIS in dogs different insufflation pressures need to be tested to guide an optimal laparoscopic working environment within the rectum.
The purpose of this study was to determine the ideal insufflation pressures during TAMIS in canine cadavers for submucosal rectal resection and suturing as they relate to visualization, ease of technique, and complications. It was hypothesized that the insufflation pressure would have no effect on the submucosal dissection, duration of incisional closure, or rate of full-thickness perforation.
Materials and Methods
Medium to large breed canine cadavers were entered in the study. All cadavers were donated for research purposes to the James L. Voss Veterinary Teaching Hospital at Colorado State University (CSU VTH; Colorado State University IACUC No. 17-7102A) after being euthanized or dying from unrelated causes. For animals who were euthanized, they were first given a sedative combination of ketamine and xylazine intramuscularly. Once they were deemed sedated to the level of unconsciousness, this was followed by Fatal-Plus intracardiac or intravenously. All cadavers were equilibrated to room temperature before procedural testing. Dogs were excluded if they weighed less than 10 kg, or had known or suspected gastrointestinal pathology.
Dogs were randomly entered into a low-pressure group (6 mmHg to 8 mmHg; group 1), medium-pressure group (10 mmHg to 12 mmHg; group 2), or high-pressure group (14 mmHg to 16 mmHg; group 3). Randomization was performed using an online random number generator (randomizer.org). The cadavers were numbered and then divided into the 3 insufflation groups based on the order determined by the generator. The procedures were then performed in order of their initial number identification.
Surgical technique
The cadavers were placed in lateral recumbency to allow measurement of intravesical pressure with their tail tied cranially to facilitate rectal access. Bowel preparation was performed with the digital removal of feces followed by the digital placement of 4 X 4-inch gauze intrarectally to prevent further fecal contamination. To monitor for changes in intra-abdominal pressures (IAP), which could be seen secondary to a leak in the rectal wall with perforation or insufflation of the colon cranial to the gauze, intravesical pressure was measured with a urinary catheter advanced into the bladder and connected to a water manometer. The water manometer was zeroed at the level of the midline of the pubis, and a volume of 1 mL/kg of saline was instilled into the bladder to establish baseline IAP.16 Baseline IAP readings were taken before insufflation, monitored throughout the procedure, and recorded at the completion of the procedure.
A single access port (SILS; Medtronic) was introduced into the rectum. Three, 5 mm cannulas were placed into the single access port with the associated obturators (Figure 1). The distal colon and rectum were then insufflated with CO2 (Endoflator; Karl Storz) to the predetermined pressure according to their group with a flow of CO2 at 5 L/min. Pressure recordings were monitored every 30 seconds to ensure insufflation pressure did not vary from the desired group range.
Image of the single access port placed transanally for rectal access with three 5 mm cannulas in place. Cadavers were placed in lateral recumbency with the tail tied cranially. The cadaver in this image is in left lateral recumbency with the tail base denoted by the asterisk. Five mm and 12 mm cannulas were placed with ease into the single access port.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Image of the single access port placed transanally for rectal access with three 5 mm cannulas in place. Cadavers were placed in lateral recumbency with the tail tied cranially. The cadaver in this image is in left lateral recumbency with the tail base denoted by the asterisk. Five mm and 12 mm cannulas were placed with ease into the single access port.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Image of the single access port placed transanally for rectal access with three 5 mm cannulas in place. Cadavers were placed in lateral recumbency with the tail tied cranially. The cadaver in this image is in left lateral recumbency with the tail base denoted by the asterisk. Five mm and 12 mm cannulas were placed with ease into the single access port.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
A 5-mm 0° telescope (Hopkins telescope; Karl Storz) was introduced into 1 of the 5 mm cannulas. The gauze was moved further cranially at this point with a laparoscopic palpation probe if the initial digital placement was insufficient. Using 5-mm markers on a laparoscopic probe, 6 cm to 9 cm from the anocutaneous junction was measured. At this location, a 2 X 2 cm area of resection was determined in a similar fashion for resection at the ventral aspect of the rectal wall. This area was at the 6 o’clock position based on the cadaver’s lateral recumbency. The rectal submucosa was transected using 5 mm laparoscopic grasping forceps (Fine teeth grasping forceps; Karl Storz) and laparoscopic Metzenbaum scissors (Metzenbaum scissors; Karl Storz). One 5 mm cannula was then replaced with a 12 mm cannula to introduce the suture. After the introduction of the suture into the rectal lumen, the 12 mm cannula was replaced by a 5 mm cannula to reduce the clashing of the cannulas during suturing. The defect was closed with a single strand of 6-inch 4-0 or 3-0 unidirectional barbed suture made of glycomer 631 on a CV 23 needle (Vloc 90, Medtronic) in a simple continuous pattern in an orad to aborad fashion with 5 mm laparoscopic needle holders (Needle Holders, Karl Storz). The suture line was completed by taking 2 additional bites of rectal submucosa beyond the incision aborad, perpendicular to the previous bites.
The duration for transection was recorded from the time of the first incision to the completion of the resection. The duration for incisional closure was recorded from when the first suture bite was taken and concluded following the completion of the additional bites beyond defect closure. Total surgery time was defined as the combination of duration for transection and duration for incisional closure. The ease of visualization for transection and of performing incisional closure was graded immediately upon procedural completion. The grading scheme was created for this study, as outlined (Tables 1 and 2). All procedures and grading were performed by a single board-certified surgeon (EM) with extensive experience with intracorporeal suturing. A rectal pull-through procedure was performed to assess for full-thickness suture penetration.
Subjective scoring system to describe feasibility for visualizing the distinction between the submucosal and muscularis layers to perform dissection.
| Grade of visualization for plane of dissection |
|---|
| Grade 1: Able to differentiate rectal submucosa and muscularis layers at initiation of transection |
| Grade 2: Able to differentiate rectal submucosa and muscularis layers after extended transection |
| Grade 3: Unable or difficult to differentiate rectal submucosa and muscularis layers during transection |
Subjective scoring system to describe feasibility of performing closure of submucosal resection.
| Grade of ease of performing incisional closure |
|---|
| Grade 1: Able to perform without difficulty |
| Grade 2: Able to perform with some difficulty |
| Grade 3: Able to perform with significant difficulty |
Statistical analysis
A Wilcoxon/Kruskal-Wallis (Rank Sums) test was used to compare the procedural durations between insufflation groups. A Wilcoxon signed-rank test was used to compare the before and after insufflation IAP as paired data. A Chi-square was used to compare the distribution of the visualization score and the ease to complete the procedure score across the groups. A value of P < .05 was considered significant. Medians and ranges were reported because data was not normally distributed. All statistical analyses were performed using commercially available statistical software (JMP version 15.0.0; SAS Institute).17
Results
Fifteen canine cadavers were entered into this study and subdivided into 5 dogs per group. One dog in group 3 was excluded from statistical analysis, other than signalment and complication rate because the rectal wall was perforated at the start of dissection. This dog was replaced by another dog to maintain 5 cases in group 3. Cadavers consisted of mostly mixed breeds (n = 14), 1 of each of an Australian Shepherd and a German Shepherd. The median weight was 29.9 kg (range = 22.7–48 kg). Ages were estimated with the majority being between 6–9 years of age (n = 11), greater than 10 years (n = 2), and less than 5 years (n = 3).
The single access port was placed with ease in all patients and the rectal seal maintained the desired level of insufflation for each group with a flow of CO2 set at 5 L/min. No cadavers included in the study had evidence of macroscopic colorectal disease. Duration for transection, duration for closure, scoring grades for visualization and closure, and IAP are reported for groups 1, 2, and 3 elsewhere (Supplementary Table S1).
The time for transection, incisional closure, and procedural completion was not significantly different between each insufflation group (Figure 2). The medians and ranges of time for the duration to complete transection, incisional closure, and the procedure are outlined elsewhere (Supplementary Table S2). The visualization score was not affected by the pressure of insufflation (P = .260). Defining the plane of dissection in group 3 was challenging and led to perforation in 2 cadavers. Cadaver 5 in group 3 was excluded from statistical analysis because the rectal wall was perforated as soon as the dissection began leading to significant rectal wall collapse and the IAP increased by 6.5 cmH2O, which did not allow for continued dissection. The procedure could be completed in the second cadaver with a rectal perforation since the rectum did not collapse. The IAP raised to 3 cmH2O in this dog.
Box-plot graph showing the time taken in each group for transection (A), closure (B), and the entire surgery (C).
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Box-plot graph showing the time taken in each group for transection (A), closure (B), and the entire surgery (C).
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Box-plot graph showing the time taken in each group for transection (A), closure (B), and the entire surgery (C).
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
The ease of closure was not significantly affected by the pressure of insufflation (P = .676). The cadaver in group 2 with a grade 3 had a more caudally placed defect, which created a tight working space when suturing aborad. Triangulation became subjectively more challenging at the end of the incisional closure for all groups due to the decrease in working space. It was perceived that the greater the distance from the anocutaneous junction, the easier the procedure was to complete. One cadaver in group 1 also had a grade 3 for incisional closure. This was the first cadaver tested and suspected to be associated with a learning curve. In cadaver 5 of group 2 luminal narrowing developed aborad to the incision line following closure. This resulted in the narrowing of the rectal lumen by approximately 50%.
The pressure of insufflation affected the IAP (P = .007; Figure 3). Perforation through the rectal muscularis layer occurred following the initial transection for 1 cadaver in group 3. This was recognized grossly and with a change in IAP; however, the rectum did not collapse. No sutures were identified in the wall of the rectum following procedural completion, except for the dog in group 3 who had known rectal wall perforation.
Box-plot graph showing the intra-abdominal pressure changes for each group from the start of the procedure to completion.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Box-plot graph showing the intra-abdominal pressure changes for each group from the start of the procedure to completion.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Box-plot graph showing the intra-abdominal pressure changes for each group from the start of the procedure to completion.
Citation: American Journal of Veterinary Research 84, 7; 10.2460/ajvr.23.02.0033
Discussion
The insufflation pressure did not affect the duration of transection or the duration of suturing of the rectal submucosa during a transanal approach in this cadaveric canine study. The visualization of the rectal lumen, the plane of dissection, and the ease of suturing were also not affected by the insufflation pressure. However, the insufflation pressure affected the IAP.
The cadavers in our study were similar to the canine population which typically presents for rectal tumors.6,8,10 Mayhew et al,9 in a study on the canine transanal approach, used cadavers with a weight range similar to the canine cadavers used in this study. We only used dogs weighing greater than 10 kg to eliminate potential problems associated with small breed dogs, such as single access port placement and maintenance.
The insufflation pressure did not significantly affect the duration of the dissection or closure of the rectal submucosa defect. To the authors’ knowledge, there are currently no guidelines on the maximal insufflation pressure to use in dogs during colonoscopy or TAMIS. McLemore et al15 described establishing a pneumorectum with the lowest pressure needed to achieve adequate visualization with a range of 5 mmHg to 25 mmHg in humans and then decreasing the intraluminal pressure to 2 mmHg to 5 mmHg to facilitate defect closure. Mayhew et al9 successfully used an insufflation pressure from 8 mmHg to 10 mmHg to complete rectal mucosa resection and suturing with a transanal approach in 6 canine cadavers. Since the rectum and the sigmoid colon dilates more than any other segments of the colon at similar pressures, a low pressure of insufflation should be used during TAMIS.18,19 The insufflation pressures used in this study are within a safe range to avoid iatrogenic trauma to the wall of the rectum and colon.19 Higher pressures can be used to create better distension of the rectum and the sigmoid colon. However, severe distention has been shown to induce short-term discomfort and the long-term effect of over-distension is not known. Additionally, the diameter of the rectum and sigmoid colon is more likely limited by the pelvic canal in dogs.
Carbon dioxide was used for insufflation instead of air because it has been shown to reduce discomfort in patients after colonoscopy.19 Carbon dioxide insufflation reduces discomfort during flexible sigmoidoscopy in colorectal cancer screening.20 An automatic insufflator was used to maintain adequate and constant pressure during the experiment. Automatic insufflators have been shown to provide better distension of the colon and rectum compared with manual insufflation.19 Carbon dioxide has also been recommended for insufflation of the rectum and colon because it interferes less than air with blood flow within the wall of the colon.21
Visualization and the ability to complete defect closure were deemed adequate in all groups and were not affected by the insufflation pressure. These were graded by the surgeon who was not blinded to the insufflation pressure during the procedure. The time to perform each step of the procedure was used as another indicator of visualization and procedure feasibility. Only a cadaveric population without macroscopic colorectal pathology was used. In a patient population with intraluminal masses, a higher insufflation pressure may be required to improve visualization and increase working space to complete tumor resection. Additionally, the increased distance of the defect from the anocutaneous junction made suturing subjectively easier. In cases where the caudal aspect of the defect was closer to the anocutaneous junction, as noted in cadaver 2 of group 2, there was increased interference between the laparoscope, laparoscopic needle holders, and the tips of the cannulas. An alternative option in these cases would be mucosal eversion as described by Cantatore et al.10 Mayhew et al9 reported their defect to be a median of 35 mm from the aborad edge to the anocutaneous junction with no discussion on the ease of suturing when the defect was close to the anocutaneous junction. A 30° telescope was used in their study that may have facilitated the completion of the procedure with the lesion close to the anocutaneous junction. Resection of cranially located lesions in the rectum is limited by the length of the instruments. Because the instruments are 30 cm long, lesions localized in the pelvic canal that are difficult to reach with traditional surgical approaches could then be reached with TAMIS.
The plane deep to the rectal submucosa was very superficial and full-thickness rectal perforation could occur easily during resection and suturing. Because the rectum is not covered by a serosal layer, the risk of full-thickness perforation is more likely increased. Mayhew et al9 reported the placement of suture bites through the full thickness of the rectum in 2 dogs. Once the plane was defined, however, the remainder of the dissection was subjectively easy. At the higher pressure of insufflation, it was more difficult to separate the plane of dissection but this difficulty did not translate into longer surgical time. One dog in the highest insufflation pressure group experienced a perforation of the rectal wall that resulted in a transient IAP increase. In another dog, the perforation resulted in the collapse of the rectum and the procedure could not be completed. Contrary to human patients, full-thickness resection will likely not be feasible in dogs because of the caudal extent of the peritoneal reflection. The peritoneal reflection extends further caudally in dogs with only 2 cm to 3 cm of rectum located retroperitoneal. It has been described to extend to the level of the third coccygeal vertebrae in male dogs.22 Therefore, full-thickness resection would result in penetration of the abdominal cavity. In humans, full-thickness resection with TAMIS has been reported with 1 cm full-thickness margins because the peritoneal reflection does not extend toward the rectum.23
Unidirectional barbed sutures were used in this study because it does not require knot tying which could be challenging in a limited space. Based on experience with laparoscopic gastropexy, the strand of sutures was 15.2 cm long (6 inches) to facilitate its manipulation in the rectum.24 This was long enough to complete each procedure. The main difficulty encountered with suturing was manipulating the needle and creating tension to bring tissue into apposition since the working space was limited. A small needle and cranial traction were used to help facilitate suturing and tissue apposition, respectively. None of the sutures tore through the submucosal layer. Alternatively, an endoscopic suturing device could be used because it has been designed to facilitate suturing in difficult locations.25,26 A narrowing of the rectal diameter was observed in only 1 case in the study. More likely, it was the result of obtaining wider bites of submucosa during closure. During the necropsy, none of the sutures were placed at full thickness.
Intravesicular pressure was used as an indicator of IAP following the technique described by Way et al.16 Intra-abdominal pressure increased only in the 2 groups with higher insufflation pressures. This is an indication that the colon was likely being insufflated while sponges were placed in the descending colon. When the rectum was perforated, in the case eliminated from the study, the IAP increased to 11 cmH2O as soon as the perforation occurred. Way et al16 used laparoscopic insufflation during their experiment to validate IAP as a technique to document increased intra-abdominal pressure. Based on this study, we considered IAP as a valid technique to detect either leakage of CO2 into the peritoneal cavity or insufflation of the colon. Because the peritoneal reflections are extended caudally in dogs, any perforation of the rectal wall during our procedure, 6 cm from anocutaneous junction, would have resulted in leakage of CO2 into the peritoneal cavity. Some canine cadavers had a resting IAP below zero more likely due to the absence of bladder wall tone and because the bladder was sitting below the level of the midline of the pubis.
Gauze sponges were packed in the distal colon and proximal rectum to maintain feces away from the surgical site and to minimize CO2 insufflation to the entire colon. Because the IAP significantly changed we can assume the colon was getting some insufflation during the procedure, however, none of the insufflation pressures used would increase the risk of colonic rupture. Radiographs were not taken to rule out a pneumocolon in our study. Placement of the surgical sponges might not be feasible when a mass is present in the rectum and could induce bleeding that would interfere with visualization.
For our study, each cadaver was placed in lateral recumbency for consistency and to facilitate the excision of tumors that would be present along the lateral aspect of the rectal wall. When performing TAMIS in humans, the patients are positioned dependent on the anatomic location of the tumor so that the tumor is located in the 6 o’clock position.11 Lateral recumbency was also chosen in this study to facilitate the measurement of IAP.
Several single-access ports are available for minimally invasive surgery.27 The single access port used in this study has been approved for transanal surgery in human patients and is the most common technique used for local excision of rectal neoplasia in colorectal surgery.12 Howard et al13 also described the utilization of the same single access port as a transanal access technique for canine colonoscopy. Mayhew et al9 used a different transanal access platform (GET-TAP; Applied Medical) to conduct their study in canine cadavers. This platform requires a dilator to dilate the anus and rectum to allow full deployment of the access sheath. The access sheath can then be sutured to the skin to prevent dislodgment. The single access port used in our study was made out of foam that can be compressed to facilitate its placement. It can be decreased to approximately 60% of its original diameter and could be used in a broader canine weight range. The port could be easily placed in each dog in this study but, only canine cadavers above 10 kg were used. The port did not require suturing and none of the ports were dislodged during the procedure. However, even with a tight fit against the anocutaneous junction, CO2 could escape. The foam in between the cannulas permits independent movement of the laparoscopic instruments, which allows for more manageable instrument interference. The single access port used in this study allows placement of three 5 mm cannulas, or two 5 mm cannulas and one 12 mm cannula at the same time. The 5 mm cannulas were used during the resection of the submucosal layer. The 12 mm cannula was only used to introduce the suture with the needle into the rectum, it was then switched to a 5 mm cannula to complete the suturing. The head of the 12 mm cannula would have interfered with the other cannulas during suturing. A 12 mm cannula permits the seamless introduction of sutures and would allow for the use of a linear stapler, a vessel sealing device, or an endoscopic suturing device. Because the single access port used in this study does not require a dilator or suturing, its introduction and removal during the procedure facilitated the removal of the resected tissue with ease.
This study has several limitations. As a cadaveric study, this study cannot accurately represent the practical difficulties associated with live patients such as bleeding, peristalsis, anesthetic plane, and the presence of an intraluminal mass impacting visualization. Insufflation may be more challenging to maintain with rectal vault collapse. If this were to occur, Attalah et al11 found that maintaining a deeper plane of anesthesia and muscle paralytics can assist with maintaining insufflation. After the initial submucosal incision with the 5 mm Metzenbaum scissors, a 5 mm vessel sealant device or a 5 mm ultrasound dissector could be used to complete the dissection and minimize bleeding. We were also unable to objectively standardize the measurement of CO2 insufflation as CO2 could escape from the anus around the single access port. To compensate for this leakage, the flow of CO2 was maintained at 5 L/min. Insufflation and urinary catheter pressures were continuously monitored to account for a leakage into the abdomen or the proximal colon. Due to the nature of the study, post-operative patient comfort and peri- and post-operative complications such as stress to the rectal sphincter tissue after surgery could not be evaluated. Although the single access port compressibility allows its placement in smaller animals, there is the potential for secondary discomfort post-operatively depending on their rectal diameter. Only 1 surgeon performed all the procedures to avoid a confounding effect related to the experience of the surgeon performing intracorporeal suturing. The surgeon performing the procedures was not blinded to insufflation pressures used during the procedure because the rectal distension made it fairly obvious which pressures were used with each cadaver. The lack of blinding could have placed bias in the ranking of the ease of performing each step of the procedure. However, time was used as a more objective measurement for ease to complete each step.
The insufflation pressure range of 6 mmHg to 12 mmHg provided adequate visualization for transection and defect closure in this cadaver population without the colorectal disease. The pressure range of 14 mmHg to 16 mmHg provided excellent visualization of the rectal lumen and increased instrument working space, however, made the visualization of the plane of dissection more challenging with an increased incidence of rectal wall perforation. The complications noted in this study were rectal lumen narrowing in 1 cadaver and rectal wall perforation in 2 cadavers. Insufflation pressure can be modified during surgery to assist with different steps of the procedure. This study has favorable results for TAMIS with the SILS port and a broad insufflation pressure range to provide an alternative minimally invasive option for rectal tumor resection with guided case selection.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript.
The authors declare that there were no conflicts of interest.
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