Small Ruminant Research 121 (2014) 336–339
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A 3-portal laparoscopic ovariectomy technique in ewes Jeremiah T. Easley a,∗ , Stephen Q. Garofolo b , Dana Ruehlman a , Eileen S. Hackett a a b
Colorado State University, Department of Clinical Sciences, 300 West Drake Road, Fort Collins, CO 80523, USA University of Minnesota, Experimental Surgical Services, Minneapolis, MN, USA
a r t i c l e
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Article history: Received 12 June 2014 Received in revised form 30 July 2014 Accepted 1 August 2014 Available online 12 August 2014 Keywords: Laparoscopy Laparoscopic ovariectomy Minimally invasive surgery Sheep
a b s t r a c t The aim of this study was to describe a three-portal laparoscopic ovariectomy technique in ewes. A novel three-portal laparoscopic ovariectomy technique was utilized in 40 ewes in a research setting. Surgical time, intra-operative, and post-operative complications were recorded for each ewe. Ovaries were successfully removed utilizing the three-portal laparoscopic technique in all ewes. Median surgical time was 18 min (mean 19 min, range 12–40 min). The surgical procedure had a rapid learning curve. The laparoscopic technique provided excellent access and visualization of the female reproductive organs in the ewe. A 3-portal laparoscopic ovariectomy can be safely and rapidly performed in ewes and may improve patient outcomes, including minimizing postoperative pain and incisional morbidity. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Laparoscopy has been successfully performed in small ruminants for a variety of applications including intrauterine artificial insemination (Gourley and Riese, 1990), ovum collection (Graff et al., 1999; Baldassarre et al., 2002), nephrectomy (Sanchez-Margallo et al., 2012), cystotomy (Franz et al., 2008), and ovariectomy (Teixeira et al., 2011). Advantages include less surgical trauma, improved cosmetic results, better intra-operative visualization, and decreased surgical time, patient convalescence and pain, all of which increase efficiency and minimize medical costs (Gourley and Riese, 1990; Baldassarre et al., 2002; SanchezMargallo et al., 2012). The female reproductive anatomy of the ewe suggests that laparoscopic ovariectomy through a three-portal laparoscopic technique is possible.
∗ Corresponding author. Tel.: +1 970 682 0079>. E-mail address:
[email protected] (J.T. Easley). http://dx.doi.org/10.1016/j.smallrumres.2014.08.001 0921-4488/© 2014 Elsevier B.V. All rights reserved.
The most common indications for bilateral ovariectomy in ewes include production of females for semen collection or libido testing of rams, the removal of ovarian tumors (Pugh, 2002), and the development of translational models for the study of postmenopausal ailments in women (Thorndike and Turner, 1998; Turner, 2002). A laparoscopic ovariectomy procedure also has potential translational benefits to clinical food animal practice. Removal of the ovaries in livestock results in easier handling, suppression of estrus behavior in meat producing species improving conditioning, prevention of pregnancy and reproductive cancers, and recovery of gonadal tissue in animals of high genetic status (Garber et al., 1990; Bleul et al., 2005; Padula et al., 2002). Traditionally in ewes, an ovariectomy procedure has been performed via an open ventral midline celiotomy. Generally, ventral midline celiotomy has frequently been associated with a number of complications including difficulty in visualizing and accessing the uterus and ovaries, iatrogenic damage associated with the reproductive anatomical location, and incisional morbidity. The
J.T. Easley et al. / Small Ruminant Research 121 (2014) 336–339
uterine horns of the ewe are primarily located within the pelvic inlet adjacent to the ovarian attachments. This results in the reproductive organs residing in a significantly more caudal location when compared to other domestic species (Dyce et al., 2010). During ovariectomy via open midline celiotomy, the incision must be located cranial to the udder. The incision location in combination with the relative caudal location of the reproductive organs precipitate use of excessive traction necessary to exteriorize the ovaries and associated ovarian pedicle (Sanchez-Margallo et al., 2012). Excessive traction can then result in increased surgical hemorrhage secondary to dropped pedicle or inadequate ligation performed under traction. In comparison, laparoscopic techniques negate the need to exteriorize the ovary outside of the abdominal cavity prior to transection. Laparoscopic insufflation and the Trendelenburg position (head downward ∼15◦ ) aid in separation of the adjacent abdominal viscera, further improving visualization and ease of manipulation of the ovaries and associated structures. The reported benefits of laparoscopic techniques suggest that laparoscopic ovariectomy may be a good alternative to a ventral midline celiotomy approach (Chou et al., 1999; Lumsden et al., 2000; Leminen, 2000; Wang et al., 2001; Malur et al., 2001; Sanchez-Margallo et al., 2012). Teixeira et al. (2011) has described a two-portal laparoscopic ovariectomy approach in ewes resulting in less surgical trauma, a shorter surgical time, minimal postoperative stress and better surgical recovery. Laparoscopic ovariectomy can improve both the efficiency and quality of the ovariectomy procedure, as well as minimize the pain and stress to animals in research and clinical settings. Therefore, the purpose of this study was to develop and describe a novel three-portal laparoscopic technique for ovariectomy in ewes and evaluate efficacy, and intraoperative and post-operative complications. 2. Materials and methods 2.1. Animals and experimental design The protocol was approved by an Institutional Animal Care and Use Committee (protocol# 12-3442A). Forty mature (greater than 3+ years of age) Columbia x Rambouillet cross ewes (n = 40) weighing between 70 and 100 kgs underwent laparoscopic ovariectomy under general anesthesia as participants in an unrelated preclinical study evaluating surgical mesh implants.
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2.3. Laparoscopic ovariectomy Laparoscopic ovariectomy was performed using a three-portal (1 camera portal, 2 instrument portals) technique. A stab incision was made using a #10 scalpel blade through the skin and linea alba approximately 2 cm cranial to the udder avoiding any prominent milk veins. A teat cannula was inserted through the incision and the abdomen was insufflated with CO2 gas to a maximum pressure of 10 mmHg (Endoflator, Karl Storz GMBH & Co. KG, Tuttlingen Germany). After creation of pneumoperitoneum, the teat cannula was removed and replaced with an 11-mm cannula with a blunt trocar. The trocar was then removed and replaced with a 10-mm 30◦ laparoscope (Hopkins Optic, 10 mm × 33 cm, Karl Storz GMBH & Co. KG) with camera. Following insertion of the laparoscope, the sheep was placed in the Trendelenburg position facilitated by the use of a mechanical tilt table. The pelvic region was examined and the uterus and ovaries located. A 3.5 cm spinal needle was used to locate instrument portal sites on either side of midline to avoid any large vessels visible laparoscopically in the parainguinal region. Stab incisions were created approximately 10 cm on each side of the midline in the parainguinal region, and an 11-mm cannula and blunt trocar were inserted. The left trocar was replaced with a 10-mm laparoscopic Babcock grasping forcep, and the right trocar was replaced with a 10-mm vessel sealing device (LigaSureTM ValleyLabTM Covidien, France; Fig. 1). The right ovary was located, grasped with Babcock grasping forceps and elevated to facilitate visualization of the broad ligament, ovarian artery and vein and adjacent oviduct. The vessel sealing device was then used to coagulate the ovarian artery and vein and transect the vasculature, utero-ovarian ligament and a portion of the oviduct (Fig. 2). The ovary was then removed from the abdominal cavity by completely exteriorizing the cannula and Babcock forceps actively grasping the ovary simultaneously. The cannula and trocar were then replaced though the same stab incision on the right side. The left ovary was then removed in similar fashion using the same protocol (Fig. 3). Extension of the 10 mm stab incision was not required for ovary removal. The ovarian pedicle was observed prior to laparoscopy completion to identify adequate hemostasis. The animal was then returned to a level position and the CO2 was passively removed from the abdomen. Following cannula removal, incisions were closed routinely in two layers (rectus fascia/muscle and skin), and operative time was recorded. Operative time was defined as time from initiating surgery to discontinuation of gas anesthesia and recorded in 5-min intervals.
2.4. Aftercare and post-surgical assessment Surgical time and intra-operative complications were recorded for each sheep. After surgery the animal was transported to a recovery area and monitored until the swallowing reflex returned. At this time the animal was extubated, moved into sternal recumbency, and administered procaine G penicillin (22,000 units/kg SQ) and 1 g of oral phenylbutazone. After completion of the surgeries, the animals were moved to an indoor research barn where they were housed in groups, unrestricted in a box stall. All sheep were monitored twice daily for postoperative complications or pain.
3. Results 2.2. Pre-operative pain management and anesthetic protocol Each ewe was fasted and premedicated with 1 g of oral phenylbutazone (Bute Boluses, VEDCO, Inc., St. Joseph, MO, USA), procaine G penicillin (22,000 units/kg, SQ–PenOne ProTM , Norbrook Laboratories Limited, Newry, Ireland), and two transdermal fentanyl patches (100 mcg, 50 mcg–Fentanyl Transdemal System,Watson Pharma, Inc., Corona, CA, USA) 24 h prior to surgery. The auricular vein and artery were catheterized and anesthesia was induced using a combination of ketamine HCl (3.3 mg/kg IV–KetasetTM Boerhinger-Ingelheim, St. Joseph, MO, USA) and diazepam (0.1 mg/kg IV–Diazepam, Hospira, Inc., Lake Forest, IL, USA). Following anesthetic induction, the sheep were intubated with a cuffed endotracheal tube, placed in dorsal recumbency and maintained on isoflurane (1.5–3%—FlurisoTM , Norbrook Laboratories Limited, Newry, Ireland) with 100% oxygen using positive pressure ventilation (20 cm H2 O) for the duration of the procedure. The abdomen was clipped and prepped using povidone-iodine surgical scrub, and the caudal abdomen was draped from the cranial edge of the udder to the umbilicus.
Ovaries were successfully removed in all ewes via a three portal laparoscopic technique. The laparoscopic technique was technically simple and intuitive with a rapid learning curve. Access and visualization of the female reproductive organs was excellent in all surgeries. The mean time of the procedure was 19 min (median 18 min, range 12–40 min). There was a rapid learning curve to the procedure. No intra-operative complications were reported. All ewes returned to normal behavior within 24 h of surgery. Following surgery, one ewe developed a strangulating hernia at the left parainguinal incision within 36 hrs of surgery. The ewe was immediately taken back to surgery for reduction of GI contents and hernia repair and recovered without complication.
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Fig. 2. A high definition laparoscopic image of the uterus (D) and right ovary (black arrow) being grasped by a laparoscopic babcock forcep (A), followed by coagulation and transection of the ovarian artery, vein, utero-ovarian ligament, and adjacent oviduct (B). After coagulation and transection with the LigasureTM (C), the right ovary was removed from the abdomen.
Fig. 1. (A) Close-up view of portal placement. Black line represents the cranial most aspect of the udder. A = 10 mm rigid endoscope and camera, B = LigasureTM vessel sealing device and C = laparoscopic Babcock forceps. (B) Portal and instrument placement.
4. Discussion Laparoscopic ovariectomy utilizing the technique described in the present study can be safely and successfully performed in ewes. Surgical time is potentially decreased using the laparoscopic approach, which may precipitate a reduction in perioperative anesthetic complications such as ruminal tympany, hypoventilation, and cardiovascular collapse (Pugh, 2002). The mean surgical time in this study was 19 min (median 18 min, range 12–40 min), and the average surgical time decreased as experience increased. The median surgical time for the first 10 animals was 20 min (mean 23 min, range 15–40 min), while the median surgical time for the remaining animals was 17 min (mean 17 min, range 12–26 min). Comparatively, retrospective analysis of previous ovariectomy surgeries performed in our laboratory utilizing an open
Fig. 3. A high definition laparoscopic image showing the urinary bladder (A) and uterus (B). The black arrows show the location where the LigasureTM vessel sealing device was used to excise both ovaries.
approach had a median surgical time of 27.5 min (mean 27 min, range 20–33 min) (unpublished data). Teixeira et al. (2011) reported traditional celiotomy surgical times of 75 ± 29.5 min. A two-portal technique has been previously described with an 11-mm portal on midline, 10 cm cranial to the udder using the Hasson technique A second portal was placed 5 cm from the linea alba and 5 cm from the midline portal. This technique utilized a rigid endoscope with a working channel for instruments. Mean surgical time was 27.5 ± 2.89 min (Teixeira et al., 2011). The three portal technique described here is an alternative approach for surgeons without a rigid endoscope with a working channel and is likely to be technically easier due to improved triangulation. Single-incision laparoscopic surgery could be
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an alternative approach for ovariectomy by surgeons more familiar with this technique. Patient morbidity may be decreased when the laparoscopic technique is implemented due to a minimally invasive approach to the abdomen. The midline approach for a celiotomy typically requires a 15 cm incision. The combination of heavy ruminal contents and difficulty in restricting activity can occasionally result in hernia formation and potential gastrointestinal complications. Hernia formation typically requires a second surgery as well as additional monitoring and therapy. Although the laparoscopic technique described here resulted in hernia formation on one occasion, past experience with an open celiotomy approach results in a higher hernia formation rate. Retrospective analysis of an eight sheep study using a midline celiotomy resulted in two sheep with hernias (25% occurrence) (unpublished data). Other complications resulting from an open midline celiotomy are delayed incisional healing, seroma formation and infection, all of which can be detrimental and costly. A more invasive approach also has the potential to cause increased stress and pain to animals. In a study comparing ovariectomy by laparotomy, video-assisted laparoscopy, or complete laparoscopy, researchers evaluated the amount of postoperative pain using a behavioral scoring system (Teixeira et al., 2011). They reported that the sheep in the video–assisted and complete laparoscopy group experienced less postoperative pain than did the group that underwent a midline laparotomy. Kun et al. (2011) compared the pain and stress induced via an open abdominal abomasal fistula surgery to a laparoscopic approach in sheep by measuring interleukin-6 (IL-6), C-reactive protein (CRP) and tumor necrosis factor-␣ (TNF-␣). The study showed that IL-6, CRP and TNF-␣ all increased significantly from pre-operative values in both procedures. Laparoscopic abomasal fistula surgery resulted in a significantly smaller increase in Il-6, CRP and TNF-␣ compared to the open approach and therefore decreased pain and stress to the animals. Two potential disadvantages of the laparoscopic technique is the utilization of the peritoneal insufflation and Trendelenburg position during surgery. Peritoneal insufflation can result in physiologic abnormalities including increased partial pressure of carbon dioxide (PaCO2) , decreased partial pressure of oxygen (PaO2 ), and decreased tidal volume, which ultimately result in respiratory acidosis and hypoxemia. The presence of a pneumoperitoneum also decreases venous return and cardiac output resulting in decreased perfusion and an impairment of gas exchange. The Trendelenburg position causes cranial displacement of the abdominal viscera exacerbating these conditions (Safran and Orlando, 1994). While intraoperative gas exchange was not specifically evaluated in this study, it is important for both the surgical and anesthesia team to be cognizant of these inherent risks, administer positive pressure ventilation, and monitor the animals appropriately.
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The present study of novel laparoscopic ovariecomy in ewes highlights a number of potential advantages over an open celiotomy procedure including minimal invasiveness, better intraoperative visualization, less necessary ovarian pedicle tension during ligation, shorter surgical time, and few postoperative complications. References Baldassarre, H., Wang, B., Kafidi, N., Keefer, C., Lazaris, A., Karatzas, C.N., 2002. Advances in the production and propagation of transgenic goats using laparoscopic ovum pick-up and in vitro embryo production technologies. Theriogenology 57, 275–284. Bleul, U., Hollenstein, K., Kahn, W., 2005. Laparoscopic ovariectomy in standing cows. Anim. Reprod. Sci. 90, 193–200. Chou, D.C., Rosen, D.M., Cario, G.M., Carlton, M.A., Lam, A.M., Chapman, M., Johns, C., 1999. Home within 24 hours of laparoscopic hysterectomy. Aust. N. Z. J. Obstet. Gynaecol. 39, 234–238. Dyce, K.M., Sack, W.O., Wensing, C.J.G., 2010. Textbook of Veterinary Anatomy, fourth ed. Saunders, Philadelphia, PA. Franz, S., Dadak, A.M., Schoffmann, G., Coppens, P., Khol, J.L., Baumgartner, W., Dupre, G., 2008. Laparoscopic-assisted implantation of a urinary catheter in male sheep. J. Am. Vet. Med. Assoc. 232, 1857–1862. Garber, M.J., Roeder, R.A., Combs, J.J., 1990. Efficacy of vaginal spaying and anabolic implants on growth and carcass characteristics in beef heifers. J. Anim. Sci. 68, 1469–1475. Gourley, D.D., Riese, R.L., 1990. Laparoscopic artificial insemination in sheep. Vet. Clin. Food Anim. Pract. 6, 615–633. Graff, K.J., Meintjes, M., Dyer, V.W., Paul, J.B., Denniston, R.S., Ziomek, C., Godke, R.A., 1999. Transvaginal ultrasound-guided oocyte retrieval following FSH simulation of domestic goats. Theriogenology 51, 1099–1119. Kun, F., Jianto, Z., Dezhang, L.U., Xinyu, C., Hongbin, W., 2011. Effect of laparoscopic and open abdominal abomasal fistula surgery on stress reaction in sheep. Dongbei Nongye Daxue Xuebao 42, 117–121. Leminen, A., 2000. Comparison between personal learning curves for abdominal and laparoscopic hysterectomy. Acta. Obstet. Gynecol. Scand. 79, 1100–1104. Lumsden, M.A., Twaddle, S., Hawthorn, R., Traynor, I., Gilmore, D., Davis, J., Deeny, M., Cameron, I.T., Walker, J.J., 2000. A randomized comparison and economic evaluation of laparoscopic-assisted hysterectomy and abdominal hysterectomy. Br. J. Obstet. Gynaecol. 1107, 1386–1391. Malur, S., Possover, M., Michels, W., Schneider, A., 2001. Laparoscopicassisted vaginal versus abdominal surgery in patients with endometrial cancer—a prospective randomized trial. Gynecol. Oncol. 80, 239–244. Padula, A.M., Borman, J.M., Wright, P.J., Macmillan, K.L., 2002. Restoration of LH output and 17B-oestradiol responsiveness in acutely ovariectomised holstein dairy cows pre-treated with a GnRH agonist (deslorelin) for 10 days. Anim. Reprod. Sci. 70, 49–63. Pugh, D.G., 2002. Sheep and Goat Medicine, first ed. Saunders, Philadelphia, PA. Safran, D.B., Orlando, R., 1994. Physiologic effects of pneumoperitoneum. Am. J. Surg. 67, 281–286. Sanchez-Margallo, F.M., Perez, F.J., Sanchez, M.A., Bachiller, J., Juarez, A., Serrano, A., Ribal, M.J., Alcaraz, A., 2012. Transvaginal NOTES-assisted laparoscopic nephrectomy: a survival study in a sheep model. Surg. Endosc. 26, 926–932. Teixeira, P.M., Padilha, L.C., Motheo, T.F., Silva, M.A.M., Oliveira, M.E.F., da Silva, A.S.L., Barros, F.F.P.C., Coutinho, L.N., Flores, F.N., Lopes, M.C.S., Rodrigues, L.F.S., Vicente, W.R.R., 2011. Ovariectomy by laparotomy, a video assisted approach or a complete laparoscopic technique in Santa Ines sheep. Small Rumin. Res. 99, 199–202. Thorndike, E.A., Turner, A.S., 1998. In search of an animal model for postmenopausal diseases. Front. Biosci. 3, 17–26. Turner, A.S., 2002. The sheep as a model for osteoporosis in humans. Vet. J. 163, 232–239. Wang, P.H., Lee, W.L., Yuan, C.C., Chao, H.T., Liu, W.M., Yu, K.J., Tsai, W.Y., Wang, K.C., 2001. Major complications of operative diagnostic laparoscopy for gynecologic disease. J. Am. Assoc. Gynecol. Laparosc. 8, 68–73.