A 15-month-old 66-kg (145-lb) African lion (Panthera leo; lion 1) was examined before undergoing elective ovariectomy to prevent breeding. The lion was privately owned, had been bred for public exhibition, and was housed in an outdoor pen. Surgical sterilization by means of single-incision laparoscopic ovariectomy was elected.
Food was withheld for 12 hours prior to surgery. On the day of surgery, results of visual examination of the animal were unremarkable, and immobilization was achieved by means of remote IM injection of butorphanol (0.3 mg/kg [0.14 mg/lb]), midazolam (0.2 mg/kg [0.09 mg/lb]), and dexmedetomidine (50 μg/kg [23 μg/lb]), with doses calculated on the basis of an estimated body weight of 80 kg (176 lb). After suitable immobilization was achieved, the lion was weighed, an IV catheter was placed in a cephalic vein, and propofol (4 mg/kg [1.8 mg/lb], IV, titrated to effect) was administered. An endotracheal tube was placed, and general anesthesia was maintained with sevoflurane in oxygen. A physical examination (auscultation of the heart and lungs; evaluation of pulse quality, mucous membrane color, and capillary refill time; measurement of rectal temperature; and examination of the external ear canals and skin) was then performed, and results were unremarkable. A BCS of 3 (on a scale from 1 to 5, with 1 = cachectic and 5 = obese)1 was assigned on the basis of results of visual examination and palpation.
Heart rate and rhythm (measured with a lead II ECG), end-tidal partial pressure of carbon dioxide (measured by means of capnography), arterial oxygen saturation (measured by means of pulse oximetry), esophageal temperature, blood pressure (measured noninvasively with an oscillometric method and blood pressure cuff), and respiratory rate were monitored and lactated Ringer solution (10 mL/kg/h [4.5 mL/lb/h]) was administered throughout the anesthetic procedure. The lion was mechanically ventilated throughout the surgical procedure to maintain end-tidal partial pressure of carbon dioxide between 35 and 40 mm Hg, with a maximum airway pressure of 20 cm H2O. Amoxicillin (20 mg/kg [9.1 mg/lb], IV, once) was administered prophylactically at the time of anesthetic induction.
The lion was positioned in dorsal recumbency, and the abdominal area was aseptically prepared. A 2- to 3-cm-long skin incision was made just caudal to the umbilicus. Because of the depth of subcutaneous fat2 and larger amount of adipose tissue than expected, extensive dissection of the subcutaneous tissues was necessary to reach the peritoneum. Margins of the incised linea alba were grasped, and stay sutures (size-0 polyglactin 910) were placed to evert the muscular edges. A single-port multiple-access devicea was folded at the lower ridge with 2 curved forceps that clamped the device in a staggered fashion, as previously described,3 allowing insertion into the peritoneal cavity under visual control to avoid iatrogenic injury to the abdominal organs.4 Only half of the device was introduced, making sure that the lower ridge was completely inside the abdomen, and the forceps were then released. Traction on the stay sutures was maintained to provide counterpressure, and three 5-mm-diameter cannulae were introduced through the access channels with a blunt trocar, which was subsequently withdrawn. The abdomen was insufflated to a pressure of 12 mm Hg with CO2. A 29-cm-long, 30° telescopeb was inserted via a cannula, and a brief scan of the abdominal cavity was performed to rule out iatrogenic injury during placement of the multiple-access device and cannulae.
The lion was then placed in a 10° Trendelenburg position, and the operating table was tilted approximately 15° to the right and left to improve exposure of the left and right ovaries. Left ovariectomy was performed first. The proper ligament was grasped and suspended with a standard 36-cm-long laparoscopic grasperc (Figure 1), and the proper ovarian ligament, mesovarium, and suspensory ligament were progressively sealed and transected with a 37-cm-long vessel sealer and divider deviced (Figures 2 and 3). The fat content in the mesovarium was subjectively minimal. The ovarian pedicle remnant was checked for hemorrhage, and with the transected left ovary held with the laparoscopic grasper, the vessel sealer and divider device and telescope and their associated cannulae were removed. The last cannula was subsequently withdrawn over the laparoscopic grasper, which remained inside the abdominal cavity and in the access channel of the multiple-access device. Removal of the cannulae allowed the abdomen to deflate, which relieved pressure on the muscular edges of the laparotomy incision and facilitated removal of the multiple-access device from the incision. Care was taken to ensure that the laparoscopic grasper remained closed to prevent inadvertent ovary release. Once the multiple-access device was fully outside the abdominal cavity, the laparoscopic grasper was withdrawn, and the ovary was extracted. Excised tissues were checked to ensure the ovary was completely removed. The multiple-access device was then reintroduced as described, and right ovariectomy was performed in the same manner. Once the right ovary was removed, the abdomen was fully exsufflated by manual external compression. No technical difficulties were recorded.
Laparoscopic view of the ovary (O) and uterus (U) in a 15-month-old 66-kg (145-lb) lion (Panthera leo; lion 1). Notice that fat content in the mesovarium is minimal, the ovary is easily accessible, and the long mesovarium allows the ovary to be easily manipulated. Cd = Caudal. Cr = Cranial.
Citation: Journal of the American Veterinary Medical Association 252, 12; 10.2460/javma.252.12.1548
Laparoscopic view of transection of the ovarian vessels (A) and mesovarium (B) with a vessel sealer and divider device (asterisk) in lion 1. Cd = Caudal. Cr = Cranial. M = Mesovarium. O = Ovary.
Citation: Journal of the American Veterinary Medical Association 252, 12; 10.2460/javma.252.12.1548
Laparoscopic view during transection of the proper ligament in lion 1. Notice the triangulation limitations, because the 2 instruments are in the same operative axis. See Figure 1 for key.
Citation: Journal of the American Veterinary Medical Association 252, 12; 10.2460/javma.252.12.1548
The abdominal incision was closed in a routine manner, with size-0 polyglactin 910 in a continuous suture pattern for the abdominal musculature, 2-0 polyglactin 910 in a continuous suture pattern for the subcutaneous tissues, and 3-0 polydioxanone in an intradermal continuous suture pattern for the skin. Surgery time (ie, time from initial incision to closure) was 43 minutes. The lion was weaned off the ventilator and moved back to its transport cage. A single dose of meloxicam (0.1 mg/kg [0.045 mg/lb], IM) was administered for postoperative analgesia. Following extubation, immobilization was reversed by administration of atipamezole (0.25 mg/kg [0.11 mg/lb], IM) and flumazenil (0.003 mg/kg [0.0014 mg/lb], IM). Recovery time (ie, time from administration of atipamezole and flumazenil until the lion was standing) was 16 minutes, and total anesthesia time (ie, time from the immobilization injection until the lion was again standing) was 146 minutes. Recovery was uneventful, and no apparent postoperative complications occurred. The lion was confined to a small indoor pen and monitored closely for 14 days after surgery. Two weeks after surgery, the lion was returned to its normal group housing. No signs of estrus were reported during the year after surgery.
Six other lions belonging to the same owner as lion 1 also underwent elective ovariectomy to prevent breeding.
Lion 2 was a 15-month-old African lion from the same litter as lion 1. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1. No difficulties or complications were encountered. Estimated body weight (used to calculate doses of immobilization drugs) was 80 kg. Actual body weight was 71 kg (157 lb), and BCS was 3. Surgery time was 29 minutes, recovery time was 13 minutes, and anesthesia time was 162 minutes.
Lion 3 was a 15-month-old African lion from the same litter as lion 1. Estimated body weight was 80 kg, and actual body weight was 64 kg (141 lb); BCS was 3. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1, except that after the left ovary was transected, it was placed in the right rectovaginal recess while right ovariectomy was performed. After both pedicles were checked for hemorrhage, the left ovary was grasped with the laparoscopic grasper and the right ovary was grasped with the vessel sealer and divider device. The multiple-access device, vessel sealer and divider device, and laparoscopic grasper were then removed from the abdominal cavity. To accomplish this, the telescope was removed, and the cannulae were subsequently withdrawn over the instruments, which remained inside the abdominal cavity and in the access channel of the multiple-access device. Once the multiple-access device was fully outside the abdominal cavity, the 2 instruments were withdrawn and the ovaries were extracted. Excised tissues were checked to ensure the ovaries were completely removed. No perioperative or postoperative complications were encountered. Surgery time was 35 minutes, recovery time was 17 minutes, and anesthesia time was 135 minutes.
Lion 4 was a 22-month-old African lion. Estimated body weight was 90 kg (198 lb), and actual body weight was 88 kg (194 lb); BCS was 3. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1. No difficulties or complications were encountered. Surgery time was 28 minutes, recovery time was 30 minutes, and anesthesia time was 130 minutes.
Lion 5 was a 26-month-old African lion. Estimated body weight was 100 kg (220 lb), and actual body weight was 105 kg (231 lb); BCS was 2. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1. No difficulties or complications were encountered. Surgery time was 24 minutes, recovery time was 26 minutes, and anesthesia time was 146 minutes.
Lion 6 was a 9-month-old African lion. Estimated body weight was 50 kg (110 lb), and actual body weight was 48 kg (106 lb); BCS was 2. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1. No difficulties or complications were encountered. Surgery time was 21 minutes, recovery time was 21 minutes, and anesthesia time was 130 minutes.
Lion 7 was a 34-month-old African lion. Estimated body weight was 150 kg (330 lb), and actual body weight was 145 kg (320 lb); BCS was 4. Immobilization, anesthetic induction, single-incision laparoscopic ovariectomy, and postoperative care were as described for lion 1, except that lion 7 was not sufficiently sedated following immobilization to allow catheter placement. Two additional injections of butorphanol (10 mg), midazolam (15 mg), and dexmedetomidine (2.5 mg) were needed to obtain suitable sedation. In addition, the ovaries were not easily accessible in lion 7, and extensive retraction of the viscera was necessary to uncover and expose the ovaries and pedicles. Laparoscopic maneuverability was subjectively more difficult than with the other lions. Surgery time was 49 minutes, recovery time was 960 minutes, and anesthesia time was 1,200 minutes. No perioperative or postoperative complications were noted, except for the prolonged recovery time.
Discussion
African lions are classified as a vulnerable species by the International Union for the Conservation of Nature, and the population of African lions in the wild decreased approximately 43% between 1993 and 2014, with an inferred rate of decline > 50%.5 However, African lions are also commonly kept in reserves and zoological parks, with a population of 750 animals in European zoos.6 Thus, population control is still indicated for captive lions.
Elective sterilization has been advised for lions that will not be bred or that have behavioral problems.7 In addition, the European Association of Zoos and Aquaria has suggested that elective sterilization be performed to ensure that offspring are not produced if they cannot be kept in-house or placed in other suitable conditions.8 Male castration (although it results in the undesirable loss of the mane) or vasectomy can be performed for elective sterilization; however, sterilization of females is sometimes preferred because it allows for removal of the hormonal stimulus that may lead to pyometra, an important cause of morbidity in captive felids.9 Elective sterilization of female lions is performed medically by means of chemical contraception or surgically by means of ovariectomy, ovariohysterectomy, or salpingectomy.2,7 Medical contraception can be effective, but practitioners should educate themselves on the reversibility, current recommendations, and potential adverse effects before choosing a medical option.10–13 Surgical sterilization is typically a reliable and permanent sterilization technique.
The lions described in the present report were young, trained females. Safety precautions are important when anesthetizing nondomestic felids,14 and anesthetic protocols for large felids generally include IM administration of a dissociative agent, often by means of remote injection, before the animal is approached.14–17 The combination of butorphanol, medetomidine, and midazolam has been reported to be safe and effective in immobilizing free-ranging lions.18 This combination was used in the present report because of the tame nature of the animals, the lack of dissociative agent-related adverse effects, and the potential reversibility of the combination, leading to rapid recovery.18 Notably, recovery time (ie, time from administration of atipamezole and flumazenil until the lion was standing) was substantially longer for lion 7 (960 minutes) than for the 6 other lions in the present report. This could have been a result of the additional drug doses required for sedation. Other possible explanations include the higher fat content (as indicated by the higher BCS), longer surgery time, and possible SC rather than IM injection of the initial drug doses.
Any surgical procedure carries some inherent risks in terms of surgical and postsurgical management. Traditional open surgical ovariectomy has been performed on lions but has several potential disadvantages, including risks of incisional infection or dehiscence, self-induced trauma, and prolonged recovery.19 Moreover, lions, like tigers, have a very deep and large abdominal cavity, and even with a long ventral midline incision, it can be difficult to visualize and ligate the mesovarium.20 In addition, lions are commonly returned to an outdoor environment after the surgical procedure, which can increase the risk of incision site infection because wound cleaning and bandaging cannot be easily performed.
Laparoscopic procedures are being increasingly performed in both human and veterinary surgery,21–25 and laparoscopic ovariectomy is now routinely performed in dogs26–30 and cats31–34 and has been described for lions,2 tigers,35 and cheetahs.36 Several reports suggest decreased postoperative pain and surgical stress in dogs26,37-39 and cats33 undergoing laparoscopic ovariectomy, compared with traditional open procedures. For these reasons, laparoscopic ovariectomy, which provides excellent visibility by means of a minimally invasive approach, appears to be a valuable option for sterilization of female lions.2
Although laparoscopic procedures may be associated with lower morbidity rates, compared with open surgical techniques, they typically still require several incisions. Each incision has potentially negative sequelae, including pain, hemorrhage, internal organ damage, infection, and herniation of abdominal content.27,37,40-43 For these reasons, less invasive options are being explored, such as single-incision laparoscopic surgery, an approach that has been described for several procedures, including ovariectomy in dogs,3,4,44-46 cats,32 cheetahs,36 and tigers35 and salpingectomy in leopards.47 Multiple studies have shown that the single-incision approach minimizes soft tissue trauma in human patients42,48-50 and decreases surgical time and intraoperative complications in dogs undergoing elective procedures,51 compared with standard multiple-access laparoscopic surgery. For these reasons, single-incision laparoscopic methods could be valuable in large wild animals.
In the present report, 7 lions underwent elective ovariectomy by means of single-incision laparoscopic surgery. From a technical point of view, single-incision laparoscopic ovariectomy appeared to offer certain advantages. First, the single-port multiple-access device that was used housed 2 instrument channels and a telescope portal in a flexible cylinder that could be inserted through a single incision. The 2 instrument channels and telescope portal obviated the need for a transabdominal suspension suture or hook, which is required when performing laparoscopic ovariectomy with 2 cannulae or an operating telescope.27,46 In fact, the size of these lions, compared with that of dogs and cats, and their well-developed abdominal musculature would likely have precluded the use of a transabdominal suspension suture or hook.2,35 A second advantage was that only a single 3-cm-long incision was needed. This was similar to the overall incision length reported previously for lions in which three 10- to 12-mm-diameter cannulae were used,2 but presented several benefits. First, the device could be placed relatively easily despite the abundant subcutaneous fat, which would have made establishment of pneumoperitoneum with a Veress needle or modified Hasson technique more complicated.2 Second, the device could be placed under visual control, thus minimizing the risk of iatrogenic trauma to the abdominal organs, as previously described.4 Finally, the 3-cm-long incision facilitated ovary extraction at the end of the procedure, and if the ovaries had been dropped during extraction, they could likely have been easily retrieved.
In the present report, surgery time ranged from 21 to 49 minutes, which was similar to surgery times reported for dogs4 and cheetahs36 but shorter than those reported for tigers.35 Notably, we did not see the expected decrease in surgery time as the surgical team gained experience with the use of the single-port multiple-access device in lions.35,52 This was possibly because the sample size was too small to evaluate the learning curve or because the surgical team already had extensive experience with single-incision laparoscopic surgery in dogs. The shortest surgery time was for the lion that weighed the least (lion 6), and the longest surgery time was for the lion that weighed the most (lion 7). In view of this, we suggest that even if the surgical time could improve with experience, it could be negatively impacted by heavier body weight. This requires further investigation.
Whereas there may be a number of advantages of single-incision laparoscopic ovariectomy in lions, some drawbacks should be noted. First, the instruments are introduced adjacent and parallel to each other, and maneuverability is thereby more difficult than during conventional laparoscopic procedures. For this reason, the device used for the lions of the present report was designed to be used with articulated instruments. However, the soft-foam nature of this device and its flexible capabilities also allow the use of standard straight laparoscopic instruments, which partially compensates for the loss of triangulation. Moreover, the range of instrument movement required during laparoscopic ovariectomy is limited, and triangulation is not mandatory.4 In fact, in a previous report35 of single-incision laparoscopic ovariectomy in tigers, no obvious advantages of using bent or articulated instruments were observed. In the present report, no technical difficulties were encountered, and ovariectomies were relatively easily performed by experienced laparoscopic surgeons. Furthermore, ovarian and uterine surgical anatomy and topography in lions are similar to those found in cats, and compared with dogs, there was almost no fat in the pedicles and the long mesovaria allowed the ovaries to be easily manipulated. Such observations could in part explain why no technical difficulties were encountered in the present report. However, the long surgery time experienced with the heaviest lion (lion 7) could have been attributable to limited triangulation and maneuverability. It is possible that when performing more technically demanding procedures through a single-port multiple-access device in larger or obese animals, bent or articulated instruments could be necessary.
A second drawback of single-incision laparoscopic ovariectomy is the high cost of the laparoscopic equipment and single-port multiple-access device. However, we believe that these costs are outweighed by the benefits of the procedure in lions.
Findings for lions in the present report suggested that ovariectomy with the single-port multiple-access device may be an acceptable, minimally invasive option for ovariectomy in large felids. Even though laparoscopic procedures are less invasive than open surgical approaches, there is still potential for pain and complications. Additional studies directly comparing single-incision laparoscopic ovariectomy to other surgical techniques would be valuable.
Acknowledgments
Lions were treated at the Clinique Vétérinaire Vet'Arenes.
The authors received no specific grant from any funding agency in the public, commercial, or not-for-profit sector for the preparation of this article. The authors declare that they had no conflicts of interest.
ABBREVIATIONS
| BCS | Body condition score |
Footnotes
SILS Port, Covidien, Norwalk, Conn.
Hopkins, Karl Storz-Endoscopy, Guyancourt, France.
Bowel grasper, fenestrated, Karl Storz Endoscopy, Guyancourt, France.
Valleylab LigaSure V, Covidien, Vetoquinol, Paris, France.
References
1. Burkholder WJ. Use of body condition scores in clinical assessment of the provision of optimal nutrition. J Am Vet Med Assoc 2000;217:650–654.
2. Hartman MJ, Monnet E, Kirberger RM, et al. Laparoscopic sterilization of the African lioness (Panthera leo). Vet Surg 2013;42:559–564.
3. Runge JJ, Mayhew PD. Evaluation of single port access gastropexy and ovariectomy using articulating instruments and angled telescopes in dogs. Vet Surg 2013;42:807–813.
4. Manassero M, Leperlier D, Vallefuoco R, et al. Laparoscopic ovariectomy in dogs using a single-port multiple-access device. Vet Rec 2012;171:69.
5. Bauer H, Packer C, Funston P, et al. The IUCN red list of threatened species. Panthera leo. Available at: www.iucnredlist.org/details/15951/0. Accessed Apr 25, 2018.
6. Simonsen K, Králová K. African lion (Panthera leo) monitor studbook. Give, Denmark: Givskud Zoo, Zootopia, 2014.
7. Association of Zoos and Aquariums Lion Species Survival Plan. Lion (Panthera leo) care manual. Silver Spring, Md: Association of Zoos and Aquariums, 2012.
8. European Association of Zoos and Aquaria. Standards for the Accommodation and Care of Animals in Zoos and Aquaria. Available at: www.eaza.net/assets/Uploads/Standards-and-policies/Standards-for-the-Accommodation-and-Care-of-Animals-2014.pdf. Accessed Apr 25, 2018.
9. McCain S, Ramsay E, Allender MC, et al. Pyometra in captive large felids: a review of eleven cases. J Zoo Wildl Med 2009;40:147–151.
10. Bertschinger HJ, de Barros Vaz Guimaráes MA, Trigg TE, et al. The use of deslorelin implants for the long-term contraception of lionesses and tigers. Wildl Res 2008;35:525–530.
11. Harrenstien LA, Munson L, Chassy LM, et al. Effects of porcine zona pellucida immunocontraceptives in zoo felids. J Zoo Wildl Med 2004;35:271–279.
12. McAloose D, Munson L, Naydan DK. Histologic features of mammary carcinomas in zoo felids treated with melengestrol acetate (MGA) contraceptives. Vet Pathol 2007;44:320–326.
13. Moresco A, Dadone L, Arble J, et al. Location and removal of deslorelin acetate implants in female African lions (Panthera leo). J Zoo Wildl Med 2014;45:397–401.
14. Gunkel C, Lafortune M. Felids. In: West G, Heard D, Caulkett N, eds. Zoo animal and wildlife immobilization and anesthesia. 2nd ed. Ames, Iowa: Wiley Blackwell Publishing, 2014;635–646.
15. Herbst LH, Packer C, Seal US. Immobilization of free-ranging African lions (Panthera leo) with a combination of xylazine hydrochloride and ketamine hydrochloride. J Wildl Dis 1985;21:401–404.
16. Jacquier M, Aarhaug P, Arnemo JM, et al. Reversible immobilization of free-ranging African lions (Panthera leo) with medetomidine-tiletamine-zolazepam and atipamezole. J Wildl Dis 2006;42:432–436.
17. Lamberski N. Felidae. In: Miller R, Fowler M, eds. Zoo and wild animal medicine. St Louis: Elsevier Saunders, 2015;467–476.
18. Wenger S, Buss P, Joubert J, et al. Evaluation of butorphanol, medetomidine and midazolam as a reversible narcotic combination in free-ranging African lions (Panthera leo). Vet Anaesth Analg 2010;37:491–500.
19. Gass H. Felidae, Viverridae, Mustelidae. In: Klos H, Lang E, eds. Handbook of zoo medicine. New York: Van Nostrand Reinhold Co, 1982;119–120.
20. Steeil JC, Sura PA, Ramsay EC, et al. Laparoscopic-assisted ovariectomy of tigers (Panthera tigris) with the use of the LigaSure device. J Zoo Wildl Med 2012;43:566–572.
21. Freeman LJ, Rahmani EY, Sherman S, et al. Oophorectomy by natural orifice transluminal endoscopic surgery: feasibility study in dogs. Gastrointest Endosc 2009;69:1321–1332.
22. Mayhew PD. Advanced laparoscopic procedures (hepatobiliary, endocrine) in dogs and cats. Vet Clin North Am Small Anim Pract 2009;39:925–939.
23. Monnet E, Twedt DC. Laparoscopy. Vet Clin North Am Small Anim Pract 2003;33:1147–1163.
24. Richter KP. Laparoscopy in dogs and cats. Vet Clin North Am Small Anim Pract 2001;31:707–727.
25. Twedt DC, Monnet E. Laparoscopy: technique and clinical experience. In: McCarthy TC, ed. Veterinary endoscopy for the small animal practitioner. St Louis: Elsevier Saunders, 2005;357–385.
26. Culp WT, Mayhew PD, Brown DC. The effect of laparoscopic versus open ovariectomy on postsurgical activity in small dogs. Vet Surg 2009;38:811–817.
27. Dupré G, Fiorbianco V, Skalicky M, et al. Laparoscopic ovariectomy in dogs: comparison between single portal and two-portal access. Vet Surg 2009;38:818–824.
28. Fiorbianco V, Dupré G, Skalicky M, et al. Laparoscopic ovariectomy in dogs: comparison between single-hole and two-hole approaches, in Proceedings. 18th Annu Sci Meet Eur Coll Vet Surg 2009;299–301.
29. Van Goethem BE, Rosenveldt KW, Kirpensteijn J. Monopolar versus bipolar electrocoagulation in canine laparoscopic ovariectomy: a nonrandomized, prospective, clinical trial. Vet Surg 2003;32:464–470.
30. Van Nimwegen SA, Kirpensteijn J. Comparison of Nd:YAG surgical laser and Remorgida bipolar electrosurgery forceps for canine laparoscopic ovariectomy. Vet Surg 2007;36:533–540.
31. Case JB, Boscan PL, Monnet EL, et al. Comparison of surgical variables and pain in cats undergoing ovariohysterectomy, laparoscopic-assisted ovariohysterectomy, and laparoscopic ovariectomy. J Am Anim Hosp Assoc 2015;51:1–7.
32. Coisman JG, Case JB, Shih A, et al. Comparison of surgical variables in cats undergoing single-incision laparoscopic ovariectomy using a LigaSure or extracorporeal suture versus open ovariectomy. Vet Surg 2014;43:38–44.
33. Gauthier O, Holopherne-Doran D, Gendarme T, et al. Assessment of postoperative pain in cats after ovariectomy by laparoscopy, median celiotomy, or flank laparotomy. Vet Surg 2015;44(suppl 1):23–30.
34. van Nimwegen SA, Kirpensteijn J. Laparoscopic ovariectomy in cats: comparison of laser and bipolar electrocoagulation. J Feline Med Surg 2007;9:397–403.
35. Emerson JA, Case JB, Brock AP, et al. Single-incision, multicannulated, laparoscopic ovariectomy in two tigers (Panthera tigris). Vet Q 2013;33:108–111.
36. Hartman MJ, Monnet E, Kirberger RM, et al. Single-incision laparoscopic sterilization of the cheetah (Acinonyx jubatus). Vet Surg 2015;44(suppl 1):76–82.
37. Austin B, Lanz OI, Hamilton SM, et al. Laparoscopic ovariohysterectomy in nine dogs. J Am Anim Hosp Assoc 2003;39:391–396.
38. Davidson EB, Moll HD, Payton ME. Comparison of laparoscopic ovariohysterectomy and ovariohysterectomy in dogs. Vet Surg 2004;33:62–69.
39. Gower S, Mayhew PD. Canine laparoscopic and laparoscopic-assisted ovariohysterectomy and ovariectomy. Compend Contin Educ Vet 2008;30:430–440.
40. McClaran JK, Buote NJ. Complications and need for conversion to laparotomy in small animals. Vet Clin North Am Small Anim Pract 2009;39:941–951.
41. Raman JD, Bagrodia A, Cadeddu JA. Single-incision, umbilical laparoscopic versus conventional laparoscopic nephrectomy: a comparison of perioperative outcomes and short-term measures of convalescence. Eur Urol 2009;55:1198–1204.
42. Raman JD, Cadeddu JA, Rao P, et al. Single-incision laparoscopic surgery: initial urological experience and comparison with natural-orifice transluminal endoscopic surgery. BJU Int 2008;101:1493–1496.
43. Yerdel MA, Karayalcin K, Koyuncu A, et al. Direct trocar insertion versus Veress needle insertion in laparoscopic cholecystectomy. Am J Surg 1999;177:247–249.
44. Runge JJ, Curcillo PG II, King SA, et al. Initial application of reduced port surgery using the single port access technique for laparoscopic canine ovariectomy. Vet Surg 2012;41:803–806.
45. Runge JJ, Mayhew PD, Case JB, et al. Single-port laparoscopic cryptorchidectomy in dogs and cats: 25 cases (2009–2014). J Am Vet Med Assoc 2014;245:1258–1265.
46. Case JB, Marvel SJ, Boscan P, et al. Surgical time and severity of postoperative pain in dogs undergoing laparoscopic ovariectomy with one, two, or three instrument cannulas. J Am Vet Med Assoc 2011;239:203–208.
47. Hartman MJ, Monnet E, Kirberger RM, et al. Laparoscopic salpingectomy in two captive leopards (Panthera pardus) using a single portal access system. J Zoo Wildl Med 2015;46:945–948.
48. Chamberlain RS, Sakpal SV. A comprehensive review of single-incision laparoscopic surgery (SILS) and natural orifice transluminal endoscopic surgery (NOTES) techniques for cholecystectomy. J Gastrointest Surg 2009;13:1733–1740.
49. Kommu SS, Chakravarti A, Luscombe CJ, et al. Laparoendoscopic single-site surgery (LESS) and NOTES; standardised platforms in nomenclature. BJU Int 2009;103:701–702.
50. Kommu SS, Kaouk JH, Rane A. Laparo-endoscopic single-site surgery: preliminary advances in renal surgery. BJU Int 2009;103:1034–1037.
51. Gonzalez-Gasch E, Monnet E. Comparison of single port access versus multiple port access systems in elective laparoscopy: 98 dogs (2005–2014). Vet Surg 2015;44:895–899.
52. Runge JJ, Boston RC, Ross SB, et al. Evaluation of the learning curve for a board-certified veterinary surgeon performing laparoendoscopic single-site ovariectomy in dogs. J Am Vet Med Assoc 2014;245:828–835.
