Laparoscopic Ovariectomy in Dogs: Comparison Between Single Portal and Two-Portal Access

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Veterinary Surgery 38:818–824, 2009

Laparoscopic Ovariectomy in Dogs: Comparison Between Single Portal and Two-Portal Access GILLES DUPRE´, DVM, Diplomate ECVS, VALENTINA FIORBIANCO, DVM, MONIKA SKALICKY, NILGU¨N GU¨LTIKEN, DVM, SERHAN SERHAT AY, DVM, and MURAT FINDIK, DVM

DTPH,

Objective: To compare surgical times and perioperative complication rates of single portal access and 2-portal laparoscopic ovariectomy (LapOVE) in dogs using a bipolar vessel sealer/divider device, and to evaluate the performance of novice laparoscopists for right ovariectomy. Study Design: Controlled clinical trial. Animals: Female dogs (n ¼ 42). Methods: Dogs were divided into groups: 1 ¼ single portal and 2 ¼ 2 portal. LapOVE was performed using a 5 mm vessel sealer/divider device and a 10 mm operating laparoscope (Group 1) or a 5 mm laparoscope (Group 2). Dog characteristics (weight, body condition score, ovarian ligament fat score), operative time, and perioperative complication rate were compared between groups. Right ovariectomy duration was evaluated for 2 novice laparoscopists. Results: No significant difference was found in mean total surgical time between group 1 (21.07 min/s) and group 2 (19.06 min/s). Factors significantly affecting times included body condition scores, ovarian ligament fat score, ovarian bleeding, and surgeon expertize. Minor complications (bleeding from ovaries or after splenic trauma) occurred and were similar in both groups. Bleeding was correlated to body condition score and ovarian ligament fat score. Interindividual differences were found among surgeons for right ovariectomy time. Conclusions: Single portal access LapOVE using vessel sealer/divider device is feasible, safe, and does not significantly increase total surgical time in comparison with 2-portal approach. Laparoscopic skills may play a role in ability to perform single portal LapOVE. Clinical Relevance: LapOVE can be performed using single portal access. r Copyright 2009 by The American College of Veterinary Surgeons

tomy,7–9 and laparoscopic-assisted ovariohysterectomy (LAOVH).10 Laparoscopic techniques are becoming widely accepted because of reported advantages, including significant decrease in postoperative pain/morbidity, and faster recovery.6,8,10–13 A wide armamentarium for achieving hemostasis during laparoscopy has been reported.14–17 Novel

INTRODUCTION

O

VARIECTOMY IS a neutering method for healthy dogs1–3 and several surgical approaches have been described.2 Numerous laparoscopic techniques have been evaluated in the bitch since 1985,4 including laparoscopic ovariectomy (LapOVE),5,6 laparoscopic ovariohysterec-

From the Clinic for Small Animal Surgery, Ophthalmology, Dentistry, Physiotherapy and Rehabilitation, Department of Small Animals and Horses, and Institute of Pathophysiology, University of Veterinary Medicine Vienna, Vienna, Austria; and the Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Ondokuz Mayis University, Samsun, Turkey This project was realized at the Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Ondokuz Mayy´ s University, 55139 Samsun, Turkey. Preliminary results were presented in part at the 5th Annual Meeting of the Veterinary Endoscopy Society, Keystone, CO, USA, March 2008. Corresponding author: Gilles Dupre´, Prof, Diplomate ECVS, Clinic for Small Animal Surgery, Ophthalmology, Dentistry, Physiotherapy and Rehabilitation, Department of Small Animals and Horses, University of Veterinary Medicine Vienna, Veterinaerplatz 1, A1210 Vienna, Austria. E-mail: [email protected]. Submitted November 2008; Accepted February 2009 r Copyright 2009 by The American College of Veterinary Surgeons 0161-3499/09 doi:10.1111/j.1532-950X.2009.00601.x

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computer-controlled bipolar electrocoagulation devices (LigaSuret, Valleylab/Tyco Healthcare, Boulder, CO; Ensealt, SurgRx, Palo Alto, CA) facilitate sealing and dividing ovarian pedicles, and are widely used for surgical procedures in people18,19 and animals.14,17,20–23 Previous clinical trials in mares and dogs have clearly demonstrated that these devices can provide an excellent hemostasis and reduce operative time in comparison with traditional ligatures and clips.17,21 In people, surgical trauma plays a critical role in determining pain and postsurgical adhesions.24 In laparoscopy, reduction of surgical trauma is achieved through a decrease either in the number or size of portals.25,26 To reduce the number of portals, different approaches have been proposed. Specific portals like double channel cannula27 or special access system,28,29 may allow entry of several instruments, or of instruments plus laparoscope. Although laparoscopic triangulation techniques usually involve the use of 3 portals, several variants including 2portal approaches26; single portal access laparoscopic techniques27,30; or laparoscopic-assisted procedures31 have been proposed. In veterinary medicine, laparoscopic surgery with a reduced number of portals has been proposed for gastropexy,32 cystopexy,33 removal of urinary calculi,34 and cryptorchidectomy.35 Use of transabdominal suspension sutures or hook to immobilize the ovary during resection has been described for 2-portal LAOVH10 and LapOVE.36 Using the above-mentioned suspension method and an operating laparoscope with an instrument channel, a single portal access for LapOVE has been reported5,37; however, no clinical trials have been published on the potential usefulness of this method. Moreover, although laparoscopic surgery requires skill and specialized training, the performance of novice laparoscopic surgeons have not been really investigated in the veterinary literature.16,17,35 Our purpose was to evaluate the feasibility of single portal access LapOVE in dogs using a bipolar vessel sealer/divider device, and to compare surgical times and perioperative complication rates with 2-portal laparoscopic techniques, and to study the influence of the operator on right ovariectomy. Our hypotheses were (1) single portal access LapOVE using a sealer/divider device is feasible in dogs; (2) surgical time and perioperative complications are comparable with 2-portal LapOVE; and (3) a significant difference in operative time for right ovary removal would be observed between experienced and novice laparoscopic surgeon. MATERIALS AND METHODS Dogs This study was performed as an interuniversity teaching cooperation project. During 1 week, 44 female stray dogs were

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admitted for LapOVE. Complete physical examination, blood count, and abdominal ultrasonography was performed before surgery. Dogs considered unfit for general anesthesia or requiring ovariohysterectomy were excluded. Information about breed, weight, pseudopregnancy or heat, and body condition scores (on a 5-grade scale)38 was collected. For organizational reasons, dogs were daily alternatively allocated to single portal LapOVE (group 1) or 2-portal LapOVE (group 2).

Methods All procedures in both study arms were performed by the same experienced surgeon (G.D.) for dogs 1–10, or partially (except right ovariectomy) for the remaining dogs. Two novice laparoscopic surgeons (X, Y) participated in the study. Before the trial, each novice had 1 session lasting 15 minutes on a pelvitrainer,39 and subsequently assisted the experienced surgeon in 5 consecutive procedures (either with the single portal or 2-portal technique). Thereafter, the novice laparoscopic surgeons performed resection of the right ovary in the same number of dogs in groups 1 and 2.

Anesthesia Acetylpromazine (0.02 mg/kg intramuscularly) was administered and 20 minutes later, anesthesia was induced by propofol (4–8 mg/kg intravenously [IV] to effect) and maintained with isoflurane in oxygen. Analgesia was achieved by epidural injection of bupivicaine (0.1–0.2 mg/kg). Electrocardiogram, capnography, pulse oximetry, esophageal temperature, noninvasive blood pressure, and respiratory rate were monitored.

Surgery Dogs were secured in dorsal recumbency without Trendelenburg positioning. Pneumoperitoneum (12 mmHg) was obtained by inserting a Verres needle in the upper right abdominal quadrant. After insertion of the 1st trocar, intraabdominal pressure was reduced to 8 mmHg. For both techniques, dogs were then positioned in right lateral recumbency for left ovariectomy, and in left lateral recumbency for right ovariectomy. Group 1: Single Portal Access Technique. A skin incision was performed at a site 1–2 cm below the umbilicus and a 12 mm trocar was inserted. A 10-mm-diameter operating laparoscope with a working channel (HOPKINS Optik 01, 10 mm, Karl Storz GMBH & Co. KG, Tuttlingen, Germany) was introduced, and thorough inspection of the abdominal cavity performed. With the dog in right lateral recumbency, the left ovary was identified and a 5-mm-grasping forceps (Click Line BABCOCK Grasping Forceps, 5 mm, 36 cm, Karl Storz GMBH & Co. KG) was introduced through the operating channel. The ovary was pulled to the abdominal wall. A polyamide monofilament transabdominal suspension suture attached to a round atraumatic needle was placed at the level of the proper ovarian ligament and held outside the abdomen by a Pean forceps. Using a 5 mm laparoscopic vessel sealer/divider device (LigaSure V, Valleylab, Covidien,

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Vienna, Austria), the proper ovarian ligament, mesovarium, and suspensory ligament were progressively sealed and transected. Bleeding from the ovarian bursa and pedicle or the uterine horn was graded and carefully controlled. The ovary still attached to the suspension suture was exteriorized through the portal, thus ensuring against inadvertent loss during exteriorization. After reinsertion of the cannula in the abdominal cavity, pneumoperitoneum was re-established and the dog was positioned in left lateral recumbency. Ovariectomy was repeated on the right side. Immediately after removal, the ovaries were checked to ensure complete removal and pneumoperitoneum was released. The abdominal portal was closed by novice surgeons or students in 2 layers using a 2/0 or 3/0 polyglycolic acid simple interrupted sutures for the abdominal musculature and skin. Group 2: 2-Portal Technique. A skin incision, 12 mm long, was made 2 cm caudal to the umbilicus. The first 12 mm trocar (Versaportt RPF, Autosuture, Covidien, Vienna, Austria or Endopath Xcel Dilatating Tip, Ethicon Endo-Surgery Inc., Cincinnati, OH) was inserted using a blind technique. A 5 mm diameter, 01 angle of vision laparoscope (HOPKINS II, Karl Storz GMBH & Co. KG) was used and thorough inspection of the abdominal cavity performed. Anomalies of the abdominal organs were recorded. After removal of the Verres needle, a 5 mm trocar (Versaportt RPF or Endopath Xcel Dilatating Tip) was placed cranial to the umbilicus and slightly paramedian while being observed through the laparoscope to avoid entering the falciform ligament. With the dog in right lateral recumbency, the laparoscope was introduced into the cranial cannula and grasping forceps into the caudal cannula. The ovarian pedicle, proper ligament, and suspensory ligament were sealed, transected as described for single portal technique. The ovary was pulled through the caudal port. After re-establishing pneumoperitoneum, and with the dog repositioned in left lateral recumbency right ovariectomy was performed and the portals closed. A single dose of carprofen (4 mg/kg IV) was administered to all dogs after surgery. After recovery, dogs were hospitalized overnight and checked the next morning before discharge. A recheck was performed 7 days after surgery at the shelter by one of the novice laparoscopic surgeons.

Recorded Data Recorded surgical times were (1) time from 1st trocar insertion to left ovary grasping; (2) left ovariectomy (fixation, resection, removal, from ovary grasping to its complete removal from abdomen); (3) right ovariectomy (fixation, resection, removal, from ovary grasping to its complete removal from abdomen); (4) total surgical time (defined as the time from Verres needle insertion until cannula/s removal); and (5) operative time (defined as the time from 1st trocar placement until cannula/s removal, with the exclusion of the 1st insufflation phase and portal/s closure). Other collected data included abnormalities in the ovaries, uterus, and other organs, fat scores of the ovarian ligament16

and perioperative complications. Bleeding coming either from the ovarian bursa, from the ovarian pedicle, or from the proper ligament was classified as minimal when there was 1 or few drops of blood that stopped immediately, moderate when bleeding did not obscure the surgical field but required the application of the vessel sealer/divider device, or severe when blood impeded a good observation of the surgical field, and required conversion to open laparotomy.

Data Analysis All analyses were performed with a statistical software package (SPSS version 14.0 for Windows, SPSS Inc., Chicago, IL). Variables are reported as mean  SD as they were normally distributed. We used an unpaired t-test to compare surgical times and other continuous variables in the 2 study arms. Categorical data was analyzed with a w2 test. Correlations between study variables (weight, body condition scores, ovarian ligament fat scores, ovarian bleeding events, and operative time) were calculated by the Pearson’s correlation coefficient. Similarly, Pearson’s correlation was used in each group to compare right ovariectomy time for each novice surgeon. One-way ANOVA and Duncan’s post hoc tests were used to evaluate the influence of the surgeon on operative time. Level of significance was set at P ¼ .05.

RESULTS Forty-two of 44 mixed-breed dogs of unknown age were included; 2 dogs were excluded because of pregnancy (1) or poor body condition (1). So there were 20 dogs in group 1 and 22 in group 2. Mean weight was 16.98  7.04 kg (range, 7.5–33 kg) for group 1, and 18.95  6.8 kg (range, 9–34.5 kg) for group 2. Twentysix dogs were classified as underweight (body condition score: 1–2), 15 dogs as normal weight (body condition score: 3), and 2 as overweight (body condition score: 4); none of the dogs was obese. The distribution of body condition score in the 2 study arms was similar. Three dogs had clinical signs of estrus characterized by vulvar swelling and serosanguinous vaginal discharge. There were no cases of pseudopregnancy. Each novice laparoscopic surgeon performed right ovariectomy in 8 dogs from each group. Single Portal LapOVE (Group 1) Versus 2-Portal LapOVE (Group 2) There was no significant difference between groups for total surgical time (from Verres needle insertion to cannula/s removal) or operative time (from 1st trocar insertion to cannula/s removal; Fig 1). Mean total surgical time was 21 minutes 7 seconds (  6 minutes 15 seconds) in group 1 and 19 minutes 6 seconds (  6 minutes 16 seconds) in group 2. Mean operative time was 17 minutes

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Fig 1.

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Single portal laparoscopic ovariectomy (LapOVE; group 1) versus 2-portal access (group 2).

57 seconds ( 5 minutes 13 seconds) in group 1 and 16 minutes 6 seconds ( 5 minutes 11 seconds) in group 2. Time from trocar insertion to the left ovary grasping was significantly longer (P ¼ .044) in group 2 (3 minutes 20 seconds  1 minute 24 seconds) than in group 1 (2 minutes 23 seconds  1 minute 34 seconds). Time required for left ovariectomy always performed by the experienced surgeon, was similar in group 1 (5 minutes 3 seconds  2 minutes 38 seconds) and group 2 (4 minutes 21 seconds  2 minutes 42 seconds). Time required for right ovariectomy was overall longer (P ¼ .034) in group 1 (8 minutes 9 seconds  4 minutes 4 seconds) than in group 2 (5 minutes 45 seconds  2 minutes 45 seconds) and significantly longer (P ¼ .008) when the intervention was performed by the novice surgeon X (Table 1). Four ovarian cysts were detected in 3 dogs (2 dogs had a cyst on the left ovary and 1 dog had cysts on both ovaries). Cysts were carefully emptied percutaneously under laparoscopic control before ovariectomy. Eight dogs in group 1 and 10 in group 2 had minimal bleeding either at the site of suspension suture or when cutting the ovarian ligament or the ovarian pedicle. They were all self-limiting and required no treatment. In 1 group, moderate bleeding occurred in 1 dog after surgeon

Table 1. Surgeon Performance for Right Ovariectomy Right Ovariectomy Time (minutes/seconds  SD) Technique

Surgeon #

Surgeon X

Surgeon Y

P-Value

Single portal Two portals P-value

4.55  0.54 4.07  1.39 .407

11.42  3.30 6.47  2.48 .008

6.11  2.41 5.58  3.03 .884

.001 .2

X punctured a vessel and this required application of the vessel-sealer device. Trocar insertion resulted in self-limiting minimal spleen bleeding in 4 dogs (2 in group 1 and 2 in group 2). Two occurred because of misplacement of Verres needle so that pneumoperitoneum was not to be obtained, so an open technique was used to insert the 1st trocar. No conversion to open surgery was required. All dogs recovered uneventfully, without any immediate (24 hours) or delayed (7 days) postoperative complications. Dogs Characteristics and Surgical Variables Body weight (P ¼ .000) and body condition scores (P ¼ .001) were associated with operative time. In particular, the association between operative time and the body condition score was evident both in group 1 (P ¼ .024) and group 2 (P ¼ .037). Regardless of the technique used, a higher amount of fat in the ovarian ligament was associated with a longer operative time (P ¼ .013). This relationship was found both for right (P ¼ .034) and left ovariectomy (P ¼ .017). The amount of fat in the ovarian ligament was found to significantly influence operative time (P ¼ .025), and left ovariectomy time in the group 1, as well as right ovariectomy time in group 2 (P ¼ .028). Bleeding significantly influenced the operative time (P ¼ .028) and time for left ovariectomy in group 1 (P ¼ .000) and was correlated with body condition score (group 1, P ¼ .031 and group 2, P ¼ .005) and with the amount of fat of ovarian ligament (group 1, P ¼ .036 and group 2, P ¼ .006). Bleeding of left side was correlated with body condition score (P ¼ .026) in group 1 and with body condition score (P ¼ .006) and ovarian ligament fat score (P ¼ .008) in group 2. Bleeding was not correlated to the surgeon.

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Surgeons (Table 1) There were significant interindividual differences in mean time required to complete right ovariectomy with the vessel sealer/divider device in the single portal group (P ¼ .001; Table 1). For surgeon X or Y, no significant difference was observed through the course of the study for right ovariectomy. DISCUSSION In veterinary surgery, numerous laparoscopic approaches with different numbers of portals have been recommended for ovariectomy.5–8,10 This study represents the first controlled clinical trial that compares operative time and perioperative complication rate of single portal access LapOVE with a 2-portal technique. We found that (1) using a vessel sealer/divider device for single portal access LapOVE is feasible in dogs and (2) surgical times and perioperative complication rates are comparable in both techniques. The operating laparoscope we used for the single portal access (group 1) allowed the introduction of 1 instrument through the working channel avoiding the need for a 2nd trocar for instruments. Moreover, as ovaries were temporarily suspended by means of transabdominal suspension sutures,10,40 use of a grasping forceps during ovarian resection could be avoided. By leaving the transabdominal suture uncut and long at time of removal, we were able to ensure protection against inadvertent loss of the ovary during extraction. To our knowledge this technique has not been suggested before. Besides reducing the number of portals, single portal access allows working within the same plane or direction of the laparoscope. This may ensure greater control of the instrument thereby preventing inadvertent motions. Another inherent advantage of single portal access is that this technique may be performed without a surgical assistant. However, compared with the 2-portal technique, some limitations of the operating laparoscope are the reduced degrees of freedom to work and impossibility bringing any instrument behind the ovary. For that reason during application of the vessel sealer/divider device, the clamp tip has to be carefully moved away from abdominal wall. Despite these apparent disadvantages, it should be noted that none of the dogs required conversion from single portal access ovariectomy to the 2-portal technique. To improve observation and access to the ovaries, either Trendelenburg6,7,9,13–16 or 15–301 lateral tilt of the table10,17,37 have been recommended. All of our dogs were positioned in true lateral recumbency without Trendelenburg. This method allowed a quick and easy exposure of both ovaries and avoided the need of addi-

tional organ manipulation. By doing so, even novice laparoscopic surgeons were able to perform right ovariectomy with 2-portal and single portal access. Although some authors suggest that tilting the table was useful in maintaining an aseptic surgical field,10 we were able to strictly adhere to principles of asepsis despite the changing side of recumbency during the procedure. Finally, another advantage is that this position can be achieved without the use of a mechanical table. We used a bipolar vessel sealer/divider device for section of the ovarian ligaments and for hemostatic sealing of the ovarian pedicle. Because of the narrow lateral thermal spread and quick drop of temperature a few seconds after stopping energy delivery,41 this device has a safer profile for vessel sealing with a reduced risk of tissue burning. These features may be especially useful when laparoscopic interventions are performed by novice surgeons and using an operating laparoscope. We considered both total surgical time (excluding closure) and operative time (excluding insufflation and closure) to eliminate confounding factors that could have influenced an adequate comparison between techniques. For example, problems during insufflation, even if related to the laparoscopic technique, have to be considered independent from the kind of access being used. Mean total surgical time (from Verres needle insertion to the removal of the cannula/s) was 21 minutes 7 seconds in group 1 and 19 minutes 6 seconds in group 2. It never exceeded 33 minutes even when right ovariectomy was performed by novice laparoscopic surgeons. These findings are in keeping with those obtained with other LapOVE or ovariohysterectomy techniques,6,9,10,13,15,16 and suggest that both single portal access or 2-portal LapOVE do not increase anesthetic-related complications linked to total surgical duration. There were no significant differences in total surgical time and operative time in the 2 study arms; however, the time from 1st trocar insertion to left ovary grasping was higher in group 2. Although the time difference might not be clinically relevant, we believe this was because of additional time needed for insertion of the 2nd trocar. The time required for right ovariectomy was 42% longer (8 minutes 9 seconds  4 minutes 4 seconds versus 5 minutes 45 seconds  2 minutes 45 seconds) in group 1 than in group 2. Surgical skills from different surgeons may explain this difference. Factors found to influence the duration of resection of the ovaries at both sites and in both study arms were the surgeons who performed the intervention, the amount of fat in the ovarian pedicle, the body condition scores and bleeding. Significant difference for right ovariectomy time in group 1 was found between expert surgeon and surgeon X and between surgeons X and Y (Table 1). This difference was not significant when experienced surgeon

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was compared with surgeon Y, suggesting that personal skills along with experience influence the ability to perform single portal access laparoscopic surgery using an operating laparoscope. In fact, the inability to manipulate the instrument out of the working channel and therefore the capacity to work in only 1 direction can be challenging for novice laparoscopic surgeons. For surgeons X and Y no time difference was identified in 8 consecutive right ovariectomies either in group 1 or group 2. Several factors may account for these observations. Firstly, the experienced surgeon remained responsible for the whole surgical intervention and the right ovariectomy was performed under his supervision. Secondly, the sample size was too small to evaluate the operating progress of the novice laparoscopic surgeons. Third, the sealer/divider device was easy to use, making further improvements of the coagulation–section–extraction phase unlikely. Recently, Mayhew and Cimino Brown17 compared 3 different methods for ovarian pedicle hemostasis and were unable to demonstrate a reduction of operative time in 10 consecutive cases when a similar device was used for LAOVH.17 On the other hand, such reduction could be observed in dogs when using knots and clips. The ovarian pedicle fat score was introduced by van Nimwegen et al16 and was associated with obesity and an increased surgical time when ovariectomy was performed by means of laser and Remorgida bipolar clamps.16 Although the device we used for resection was different, the ovarian pedicle fat score significantly influenced operative time because of the tissue thickness and by making vessels difficult to recognize. The other factor that significantly influenced operative time in both groups was body weight. The weight range in group 1 was 7–33 kg. A body weight of o7 kg may represent a potential limitation to the usefulness of the single portal access with an operating laparoscope and instruments of 37 cm of length. In these circumstances, the diameter of the operating laparoscope may be excessive and a 2-portal approach with two 5 mm trocars or even smaller may be advised. With body weight 433 kg, the length of the instrument that can be inserted through the working channel of the laparoscope may not allow to reach the ovary. Alternatively, other similar devices (Ensealt, SurgRx, Palo Alto, CA) available with a length of 45 cm can be used in bigger dogs. The only perioperative complication related to LapOVE in our dogs was minimal bleeding when the ovaries were fixed and the ovarian pedicles transected. Minimal bleeding occurred at a similar frequency in both groups and was related to the amount of fat. A large amount of fat can lead to an inadequate placement of the transfixing suture as well as to overload of the jaws of the vesselsealer electrode and therefore increase the likelihood of

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bleeding. Other factors like a dirty clamp from coagulated tissue could preclude correct vessel sealing. In 2 dogs in each group, minor complications (splenic bleeding) were caused during trocar insertion and did not required any specific treatment. None of them required conversion to open surgery. Although this complication is well-known, data are lacking in the veterinary literature. In people, although several techniques and devices have been described to avoid this complication, none of them have demonstrated to be totally sound.42 We found that single portal access LapOVE is feasible in dogs. When compared with a 2-portal technique it does not increase time or complication rate; however, further studies are needed to evaluate single portal LapOVE fully conducted by novice laparoscopic surgeons. ACKNOWLEDGMENTS The authors thank Adrien Bramoulle, Covidien, Elancourt France, and Reglind Hu¨hn Karl Storz GMBH & Co. KG for technical support, and Dr. Enzo Emanuele for editorial assistance.

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