Reproductive disorders, such as oophoritis, salpingitis, follicular stasis, retained eggs, dystocia, and ectopic eggs, are common in captive female chelonians.1–4 Surgical access to the reproductive tract in chelonians has traditionally been achieved via plastron osteotomy, resulting in creation of a bone flap.5,6 Although this technique has been successfully used for many years, it is associated with prolonged healing times and may be complicated by sequestration of the bone flap. As an alternative to plastron osteotomy, coeliotomy via the prefemoral region has been recommended.7–9
In some chelonian species, such as sea turtles, the prefemoral region is relatively large, and prefemoral coeliotomy provides adequate exposure of and access to the coelomic viscera. In most species, however, the prefemoral region is relatively small, so that exposure of and access to the viscera are limited. Endoscopic-assisted techniques have been used to improve tissue visualization and manipulation10,11 and likely would be beneficial in chelonians undergoing oophorectomy. The purpose of the present report was to describe a coelioscopic-assisted prefemoral oophorectomy technique for use in chelonians.
Technique
Routine preoperative examination, diagnostic imaging, and laboratory testing were performed as indicated, and food was withheld for 24 hours prior to surgery. Anesthesia was induced, and a 1.5- or 2.0-mm uncuffed endotracheal tube was inserted. Anesthesia was maintained with isoflurane in oxygen delivered through a nonrebreathing circuit. Positive-pressure ventilation (1 to 4 breaths/min at peak inspiratory pressure of 4 to 10 mm Hg) was provided manually or by use of an electric pressure-cycle ventilator.a Heart rate was monitored with a Doppler ultrasonic flow detector placed over the carotid artery, oxygen saturation was monitored with a pulse oximeter probe placed in the esophagus, and end-tidal partial pressure of CO2 was monitored with a capnograph.
Once a surgical plane of anesthesia was achieved, the turtle was placed in dorsal recumbency on a heated surgical table (28° to 30°C), and 1 hind limb was restrained in extension to expose the prefemoral region. The prefemoral region and surrounding shell were aseptically prepared and surgically draped. A 1- to 2-cm-long craniocaudal skin incision was made in the center of the prefemoral fossa, and subcutaneous connective tissue and fat were bluntly dissected to expose the tendinous aponeurosis of the transverse and oblique abdominal muscles. The aponeurosis was incised to expose the coelomic viscera, and a ring retractor with elastic staysb was used to provide exposure. Coelomic insufflation was not required.
Coelioscopy was performed with a 30°, 18-cm X 2.7-mm rigid endoscopec inserted through a 3.5-mm or 14.5-F sheath and connected to a xenon light source. The liver, gall bladder, heart, stomach, intestines, urinary bladder, ovaries, and oviducts were identified and examined. A 5-mm Babcock forceps or 3-mm fenestrated atraumatic forceps inserted into the coelomic cavity alongside the endoscope was used for manipulation (Figure 1).
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. Prefemoral skin and muscle incisions have been retracted with elastic stays and a ring retractor, and an endoscope and forceps have been introduced into the coelomic cavity.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. Prefemoral skin and muscle incisions have been retracted with elastic stays and a ring retractor, and an endoscope and forceps have been introduced into the coelomic cavity.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. Prefemoral skin and muscle incisions have been retracted with elastic stays and a ring retractor, and an endoscope and forceps have been introduced into the coelomic cavity.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
After examination of the coelomic cavity, an avascular area of ovarian interfollicular connective tissue was selected for placement of grasping forceps, taking care to avoid perforation of any ovarian follicles (Figure 2). Gentle traction was applied under endoscopic visualization, and the ovary was gently retracted toward the incision. With the ovary held just deep to the prefemoral incision, the endoscope was removed. The ovarian follicles were then gently exteriorized. If numerous large ovarian follicles that could not be easily exteriorized were present, the coelomic incision was extended as necessary. Rarely, fine-needle aspiration of individual follicles was used to reduce follicle diameter.
Coelioscopic views of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The endoscope is used to identify the ovary (a), and a forceps is used to grasp the ovarian interfollicular connective tissue (b). The ovary is retracted toward the prefemoral fossa (c) and elevated to the incision made in the prefemoral fossa (d).
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Coelioscopic views of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The endoscope is used to identify the ovary (a), and a forceps is used to grasp the ovarian interfollicular connective tissue (b). The ovary is retracted toward the prefemoral fossa (c) and elevated to the incision made in the prefemoral fossa (d).
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Coelioscopic views of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The endoscope is used to identify the ovary (a), and a forceps is used to grasp the ovarian interfollicular connective tissue (b). The ovary is retracted toward the prefemoral fossa (c) and elevated to the incision made in the prefemoral fossa (d).
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Exteriorization was continued until all follicles were visible, along with clear cranial and caudal borders of the mesovarium. The ovarian vasculature was ligated with stainless steel surgical ligation clips,d and the mesovarium was transected with scissors or a radiosurgery unite (Figure 3). Coelioscopic examination of the ligation site was performed to verify hemostasis and to verify complete excision of all ovarian tissue. In cases in which bilateral oophorectomy was desired, the second ovary was exteriorized and resected through the same prefemoral incision.
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The ovary has been exteriorized through the incision in the prefemoral fossa, vascular clips have been applied to vessels in the mesovarium, and a bipolar radiosurgery unit is used to dissect the ovary free.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The ovary has been exteriorized through the incision in the prefemoral fossa, vascular clips have been applied to vessels in the mesovarium, and a bipolar radiosurgery unit is used to dissect the ovary free.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
Photograph of a method for coelioscopic-assisted prefemoral oophorectomy in a turtle. The ovary has been exteriorized through the incision in the prefemoral fossa, vascular clips have been applied to vessels in the mesovarium, and a bipolar radiosurgery unit is used to dissect the ovary free.
Citation: Journal of the American Veterinary Medical Association 230, 7; 10.2460/javma.230.7.1049
The coelomic aponeurosis was closed with 3-0 polydioxanone in a simple continuous pattern. Skin was closed with 3-0 nylon or polydioxanone in a horizontal mattress pattern or with skin staples. Analgesics were administered upon return of spontaneous respiration. Patients with evidence of tissue necrosis or infection were treated with cefotaxime (20 mg/kg [9 mg/lb], IM) or amikacin (5 mg/kg [2.3 mg/lb], IM) during surgery. Antimicrobial treatment was adjusted on the basis of results of bacterial culture and continued for 4 weeks after surgery.
Results
Coelioscopic-assisted prefemoral oophorectomy was performed on 11 privately owned adult female turtles belonging to 4 species (6 red-eared sliders [Trachemys scripta elegans], 2 box turtles [Terrapene carolina], 1 painted turtle [Chrysemys picta], 1 four-eyed turtle [Sacalia bealei], and 1 Chinese red-necked pond turtle
[Chinemys kwangtungensis]). Five turtles required oophorectomy because of reproductive tract disease; the remaining 6 underwent elective oophorectomy. The exact age of the turtles was unknown, as all had been obtained through the pet trade as mature animals. Mean ± SD weight was 806 ± 489 g; mean straight carapace length was 15.7 ± 3.7 cm.
Preoperative physical examination revealed a 2-cm-long portion of necrotic prolapsed oviduct in the four-eyed turtle and in the red-necked pond turtle; a 3-cm-diameter soft tissue mass was identified in the left caudal portion of the coelomic cavity in 1 of the box turtles. In the remaining turtles, results of pre-operative physical examination were unremarkable.
Results of preoperative hematologic and plasma biochemical testing in 4 redeared sliders were within reference limits. One box turtle with an ovarian remnant had high plasma calcium (19.1 mg/dL) and triglycerides (670 mg/dL) concentrations consistent with reproductive activity and hepatic lipidosis. In this turtle, coelomic ultrasonography revealed several large, fluid-filled cystic structures on the right side that resembled ovarian follicles. Radiography revealed a single abnormally small, shelled egg in the left caudal portion of the coelomic cavity in 1 box turtle; a normal-appearing egg in the left caudal portion of the coelomic cavity in the four-eyed turtle; and 3 normal-appearing eggs in the mid portion of the coelomic cavity in 1 slider. The remaining turtles either were not radiographed or did not have radiographic abnormalities.
In 8 cases, bilateral oophorectomy was performed through a single incision. In 4 of these cases, surgical time was accurately recorded. Mean ± SD surgery time was 36 ± 6 minutes. In 2 cases, unilateral oophorosalpingectomy was performed because of unilateral oviduct damage, with the goal of maintaining future reproductive potential. Ectopic eggs were easily removed from the coelomic cavity, and the oviducts were easily exteriorized for salpingectomy or salpingotomy. One box turtle was examined because of a right ovarian remnant following incomplete oophorectomy performed via plastron osteotomy 3 years previously. This remnant was successfully removed via a right prefemoral approach. During coelioscopy, the liver appeared swollen and pale, and histologic examination of an endoscopic biopsy specimen revealed severe hepatic lipidosis. Although the turtle recovered from surgery and received supportive care, including placement of an esophagostomy tube to allow for fluid therapy, provision of nutritional support, and administration of medication, the turtle died a week after surgery. Necropsy was declined by the owner. In a second box turtle, a large retrocoelomic granuloma was resected following oophorectomy. Histologic examination of the mass revealed a broad core coagulum of necrotic cellular debris admixed with bacteria surrounded by a zone of epithelioid macrophages and multinucleated giant cells. This turtle died 2 days after surgery; necropsy was declined by the owner.
No complications associated with coelioscopic-assisted oophorectomy were identified, and all 11 turtles recovered from anesthesia. Full access to water was provided for aquatic species within 24 hours after surgery. In the 9 turtles that survived, skin healing appeared complete by 4 to 8 weeks after surgery. These 9 turtles appeared healthy at the time of final follow-up 6 to 26 months after surgery.
Discussion
Results for the 11 turtles described in the present report suggest that coelioscopic-assisted prefemoral oophorectomy is a practical and safe method for treating reproductive disorders and performing elective oophorectomy. Importantly, healing time in these turtles (4 to 8 weeks) was substantially shorter than healing times reported for turtles that have undergone plastron osteotomy (1 to 2 years).6 In addition, although controlled studies are lacking, it is likely that this approach is less painful than plastron osteotomy.6 One of the main benefits of plastron osteotomy over prefemoral coeliotomy is improved visualization of the coelomic viscera. In the turtles described in the present report, coelioscopic-assisted prefemoral coeliotomy provided greater visualization of the coelomic viscera than did prefemoral coeliotomy and allowed for examination of the coelomic viscera, biopsy of various tissues, and verification of hemostasis and complete ovarian excision. In this regard, coelioscopic-assisted prefemoral coeliotomy may permit some surgical procedures that previously were only possible via plastron osteotomy.
Prefemoral unilateral oophorosalpingectomy has previously been described in a loggerhead sea turtle (Carretta caretta) with a prolapsed oviduct.9 In this large, mature turtle, the prefemoral region was large enough to permit access to the ovary and oviduct through standard surgical techniques. Importantly, reproductive potential was preserved, and successful nesting was noted in subsequent years. Unilateral oophorosalpingectomy was performed on 2 turtles described in the present report to allow them to continue to be part of a captive breeding program. It remains unclear whether unilateral oophorectomy is necessary if an ipsilateral oviduct is removed. Follicles from 1 ovary have been documented to ovulate and enter the contralateral oviduct in some turtle species.12–14 Until this phenomenon is better understood, the decision to remove an ipsilateral ovary when salpingectomy is required is left to the discretion of the surgeon.
Although insufflation is often used for coelioscopic procedures in reptiles, visualization of the ovaries in turtles generally does not require insufflation.10,11,15 Additionally, our technique did not require placement of endosurgical cannulae. Although cannulae may be used successfully in chelonians, especially when instruments are placed through both prefemoral fossae, we found them unnecessary for the technique described in the present report. The prefemoral incision needed to be large enough to allow exteriorization of the ovary and was, therefore, sufficient to allow introduction of the endoscope and forceps through a single surgical incision without the need for separate cannulae.
Selection of turtles for coelioscopic-assisted prefemoral oophorectomy should be limited to mature females. The ovaries of immature females are involuted, and the mesovarium may not have enough laxity to allow exteriorization. In these patients, intracorporeal coelioscopic oophorectomy would be required, with the ovaries being isolated and excised within the coelomic cavity through the use of endosurgical techniques. Given the common risk of reproductive tract disease and the relative simplicity of the described technique, the authors recommend prophylactic coelioscopic-assisted oophorectomy as a practical and safe method of sterilizing mature female chelonians that are not required for breeding purposes.
Small animal ventilator VT-5000, BAS Vetronics, Bioanalytical Systems Inc, West Lafayette, Ind.
Lonestar retractor, Lone Star Medical Products Inc, Stafford, Tex.
Karl Storz Veterinary Endoscopy, Goleta, Calif.
Hemoclips, Weck Closure Systems, Teleflex Medical, Research Triangle Park, NC.
4.0-MHz dual-frequency radiosurgery unit, Ellman International Inc, Oceanside, NY.
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