Three mature, female, red-eared slider turtles (Trachemys scripta elegans) were individually, and separately, diagnosed with different forms of oviductal disease. Case 1 presented with acute cloacal bleeding and was diagnosed with acute oviductal rupture and ectopic eggs in the coelom. Case 2 presented for repeated scratching in the direction of the cloaca and was diagnosed with chronic oviductal impaction and coelomitis. Both cases were treated successfully by endoscopy-assisted complete ovariosalpingectomy via a bilateral prefemoral approach. Case 3 presented with a reduced appetite and signs of nesting behaviour and was diagnosed with obstructive dystocia associated with bacterial salpingitis. Successful treatment consisted of transcloacal egg removal and systemic antibiotics. Complete recovery was achieved in all three turtles, which remained disease-free 23 to 33 months later. Oviductal disease can present with a variety of clinical signs, and an accurate diagnosis can be made based on a thorough history, physical examination and appropriate diagnostic techniques.
The diagnosis and treatment of reproductive pathology in chelonia requires knowledge of the normal reproductive cycle of the species under consideration. Ovulation in chelonia is not dependent on copulation, or the presence of a mate, and oviposition of non-fertilised eggs and female reproductive tract disorders are common problems in captive female freshwater turtles (Innis and Boyer 2002). During its passage through the convoluted oviduct, albumin is added to the ovum in the uterine tube, followed by the formation of shell membranes and shell in the isthmus segment and the distal uterus, respectively (Innis and Boyer 2002, Jacobson 2007). In chelonia, eggs are held in the vagina, which is the most distal part of the oviduct, until oviposition. The vagina enters the urodeum of the cloaca (Johnson 2004, Jacobson 2007). In free-ranging, red-eared slider turtles, oviposition occurs between April and June, and mean clutch size is 11·5 eggs (Perez-Santigosa and others 2008).
Dystocia or pathological egg retention in chelonia has been defined as “a failure to deposit eggs within a time considered usual for the species of concern” (McArthur 2004). Mineralised eggs are often incidental findings in female chelonia, and the presence of mineralised eggs does not necessarily support a diagnosis of reproductive pathology (McArthur 2004). Physiologic egg retention in chelonia has been reported to be 1 to 2 months but can be as long as 4 to 6 months (Innis and Boyer 2002, McArthur 2004). Therefore, a thorough history, physical examination and appropriate diagnostics are necessary to differentiate physiologic from pathologic egg retention, but a clear diagnosis may remain difficult (Johnson 2004, McArthur 2004).
Case 1 (oviductal rupture)
A 17-year-old female, red-eared slider turtle (Trachemys scripta elegans), weighing 1·28 kg, was presented for cloacal bleeding of 4 days duration. The turtle was fed an unspecified brand of turtle pellets and was housed in a glass aquarium (60×35×30 cm), filled with shallow water. No light or heat source was provided. No medical or reproductive history was reported. During the physical examination, the turtle was bright, alert and responsive. Frank and clotted blood was observed originating from the cloacal opening. Multiple, mineralised eggs were palpable via the prefemoral fossae. Dorsoventral, whole body radiographs revealed the presence of seven mineralised eggs (Fig 1A). Two of the eggs were partially collapsed. One egg was located at the midline of the body and two eggs were located left of midline, suggesting that all three eggs were not localised within either oviduct but probably free in the coelomic cavity. A blood sample was collected from the jugular vein for a complete blood cell count and a plasma biochemical profile (VetScan Avian Reptilian Profile Plus; Abaxis Inc). The turtle was mildly anaemic [packed cell volume (PCV), 24%; reference range 25 to 33%], but all other parameters were within reference range. On the basis of the significant amount of frank blood from the cloaca and presence of mineralised eggs, which were suspected to be outside of the oviducts, acute oviductal rupture with associated cloacal haemorrhage and ectopic eggs was the presumptive diagnosis. The owner agreed to an exploratory coeliotomy. The turtle was premedicated with 2 mg/kg, sc, morphine (Baxter Healthcare Corp.) and was anaesthetically induced using 10 mg/kg, iv, propofol (Abbott Laboratories) administered in the jugular vein. After endotracheal intubation, the turtle was maintained on isoflurane (1 to 2%) (Abbott Laboratories) delivered in 100% oxygen (1 L/min). Initially, a cloacoscopy was performed to identify the source of haemorrhage, but results were non-diagnostic. For the subsequent exploratory coeliotomy, a bilateral, prefemoral surgical approach was used. Under endoscopic guidance, five eggs, free within the coelom, were identified and removed. Two eggs remained in the oviducts. A perforation of the right oviduct was identified (Fig 2). A complete bilateral ovariosalpingectomy was performed, using an endoscopy-assisted prefemoral technique as described previously (Innis and others 2007). Under endoscopic visualisation, both ovaries and oviducts were carefully grasped, using non-traumatic grasping forceps, and exteriorised through each ipislateral prefemoral incision. The vasculature of the mesovaria and mesosalpinx were ligated using stainless steel ligation clips (Hemoclip®, Teleflex Inc), before transection. Each oviduct was ligated at the level of the vagina and transected.
The coelom was lavaged with 50 mL of warm, lactated Ringer's solution. The straight and oblique abdominal muscles were closed using 3-0 polydioxanone (PDS®, Ethicon Inc) in a simple continuous pattern, and the skin was closed using 3-0 nylon in a horizontal mattress pattern. The turtle received 0·15 mg/kg, sc, meloxicam and 20 mg/kg, sc, ceftazidime, and she recovered from anaesthesia without complications. The turtle was discharged to the client the next day, and treatment with 20 mg/kg, sc, ceftazidime every 72 hours was continued for five additional doses. The turtle was allowed to soak in shallow water for 10 minutes, twice daily for the first 14 days after surgery. In a follow-up phone call 23 months after the ovariosalpingectomy, the owner reported that the turtle was alive and had experienced no further problems.
Case 2 (oviductal impaction)
A 14-year-old female, red-eared slider turtle, weighing 2·49 kg, was presented for reduced activity and appetite of approximately 5 days duration. This turtle had a history of cessation of annual egg production 3 to 4 years before presentation. For the past 12 months prior to presentation, the owner noticed intermittent occurrence of white-to-clear discharge from the cloaca, as well as intermittent repetitive kicking and scratching with the hindlimbs in the direction of the cloaca. The turtle was housed in a glass aquarium (120×50×30 cm), filled with approximately 10 cm of water. The turtle's diet consisted of turtle pellets of unknown brand and dried shrimp. During the physical examination, the turtle was bright, alert and responsive. Coelomic palpation revealed mineralised structures, which were suspected to be mineralised eggs.
Results of dorsoventral radiographs were consistent with mineralised material bilaterally in the location of the oviducts, which was more prominent on the left side (Fig 1B). Coelomic ultrasonography confirmed mineralised material in both oviducts, as well as the presence of multiple large ovarian follicles (average diameter of 2·0 cm). A blood sample was collected from the jugular vein for a complete blood cell count and a plasma biochemical profile. Results of the plasma biochemical profile were consistent with severe lipaemia (3+), hypercalcaemia (>5 mmol/L; reference range 2·08 to 4·5 mmol/L) and mild hyperphosphataemia (2·68 mmol/L; reference range 0·87 to 2·49 mmol/L). Bilateral oviductal impaction with associated mineralised material was diagnosed. An ovariosalpingectomy was recommended and elected by the owner.
Before induction of general anaesthesia, the turtle received 20 mg/kg, sc, ceftazidime (Hospira, Inc.) and 2 mg/kg, sc, morphine. General anaesthesia was induced using a combination of 1 mg/kg, sc, midazolam (Baxter Healthcare Corp.), 0·1 mg/kg, sc, medetomidine (Pfizer, Inc.) and 5 mg/kg, sc, ketamine (Fort Dodge, Inc.). The turtle was intubated, intermittently ventilated and maintained on isoflurane at 0·5 to 1% delivered in 100% oxygen (1 L/min). Before coeliotomy, a prefemoral coelioscopy was performed revealing moderate amounts of opaque fluid with lipid droplets (Fig 3A and 3B), mature ovarian follicles (Fig 3A) and generalised opacity and adhesions of the coelomic serosa. These findings were consistent with yolk coelomitis. The liver capsule appeared pale, and the liver margins rounded (Fig 3C). Following coelioscopy, a bilateral, prefemoral coeliotomy was performed. The left oviduct contained three mineralised eggs, which were desiccated and partially collapsed (Fig 4A and 4B). The right oviduct contained one large, misshapened, mineralised egg and a smaller mineralised egg. A complete bilateral prefemoral ovariosalpingectomy was performed as in case 1, and the coelom was lavaged using 60 mL warmed physiological saline solution (0·9%). Closure of muscle layers and skin was performed as described in case 1. The turtle received 0·05 mg/kg, sc, flumazenil, 0·5, sc, mg/kg atipamezole (Pfizer, Inc.) and 0·2 mg/kg, sc, meloxicam (Boehringer Ingelheim Vetmedica, Inc.) for every 48 hours continued for two doses and recovered without complications. The turtle was discharged to the client 2 days after surgery. During a follow-up phone call, 23 months after ovariosalpingectomy, the owner reported that the turtle was clinically normal.
Case 3 (salpingitis)
A 10-year-old female, red-eared slider turtle, weighing 0·69 kg, was presented with a history of reduced appetite, increased activity and nesting behaviour. The diet consisted of dried shrimp and an unspecified brand of commercial turtle pellet. The turtle was housed in a glass aquarium (50×50×30 cm), with shallow water, and had access to a dry dock area. During the physical examination, the turtle was bright and alert. Multiple mineralised eggs could be palpated in the coelomic cavity. The result of whole body radiographs revealed six mineralised eggs of normal size (Fig 1C). One egg was located within the pelvic canal. The cranial pole of this egg was partially compressed, which was apparently caused by compression of two eggs just cranial to the egg in the pelvic canal. A blood sample was collected from the jugular vein for a complete blood cell count and plasma biochemical profile. All parameters were within reference range. On the basis of these radiographic and normal blood parameters, dystocia secondary to an egg wedged in the uterus or pelvic canal was the presumptive diagnosis. The primary cause for the dystocia remained unclear, as the eggs appeared normal in size and shape. The turtle received 4 IU/kg, sc, oxytocin (Bimeda Inc) once and 12 mL, sc, lactated Ringer's solution (Abbott Laboratories) and was hospitalised to monitor for oviposition. However, no eggs were passed within 18 hours after oxytocin administration. Therefore, the turtle was anesthetised for cloacoscopy using 2 mg/kg, sc, midazolam, 0·1 mg/kg, sc, medetomidine, 1 mg/kg, sc, butorphanol (Fort Dodge, Inc.) and 3 mg/kg, iv, propofol. During an endoscopy-guided cloacoscopy, the caudal pole of the most caudal egg was visualised within the vaginal opening, partially protruding into the urodeum of the cloaca. The egg was partially adhered to the vaginal wall, making it difficult to remove the egg in toto. As a result of continued manipulation, the egg partially collapsed and was removed in a piecemeal fashion. Some shell fragments remained adhered to the vaginal wall but were not removed to avoid vaginal trauma and possible haemorrhage. A relatively large volume of dark, flocculent fluid discharged from the vaginal opening after egg removal. A sample of the fluid was collected for cytology and aerobic bacterial culture and antibiotic sensitivity. The turtle received 0·2 mg/kg, sc, meloxicam, 0·5 mg/kg, sc, atipamezole and 0·05 mg/kg, sc, flumazenil (West-Ward Pharmaceutical Corp.) and recovered without complications. Cytological examination of the vaginal fluid revealed high numbers of Gram-negative, rod-shaped bacteria. Pending aerobic bacterial culture results, the turtle was prescribed 35 mg/kg, sc, ceftazidime for every 72 hours and 10 mg/kg, sc, enrofloxacin (Bayer Healthcare LLC), diluted in 0·9% saline, for every 24 hours. A final diagnosis of severe, bacterial salpingitis and associated obstructive dystocia was established based on the radiographic, cloacoscopic and cytological findings. Results of aerobic bacterial culture revealed heavy growth of Escherichia coli and Proteus mirabilis. Both organisms were sensitive to enrofloxacin and ceftazidime. The turtle was re-presented 9 days later, and the owner reported that the turtle had passed three eggs within the 48 hours before the recheck appointment. The owner reported that the turtle was bright and active at home, and its appetite had returned to normal. The turtle eventually passed the remaining two eggs within the following 4 weeks. Treatment with enrofloxacin and ceftazidime was discontinued after a total course of 4 and 5 weeks, respectively. A follow-up phone call to the owner, 33 months after treatment of dystocia and salpingitis, revealed that the turtle was clinically normal. The turtle had laid two to three eggs the year following the treatment of dystocia and salpingitis, and an unknown number of eggs the year following.
This manuscript describes three cases of oviductal disease in female, captive red-eared slider turtles, and the subsequent medical and surgical management associated with each case. Oviductal disease and dystocia can present with a variety of clinical signs and duration and typically requires an individualised treatment approach to ensure a successful outcome.
Clinical signs of oviductal disease and pathological egg retention vary greatly because of the variety of underlying causes and duration of the disorder. Turtles can be bright and alert, or depressed and lethargic. Similarly, appetite can remain normal or the turtle may become hyporexic or anorexic (Innis and Boyer 2002, Johnson 2004). In the three cases presented here, there was good historical and physical evidence that egg retention was pathologic and required therapeutic intervention. Cloacal bleeding (case 1) or discharge (case 2), as well as behaviour consistent with straining (case 2), are of concern and likely indicate a underlying oviductal disease process (Innis and Boyer 2002). If, in addition, mineralised eggs are radiographically evident, pathologic egg retention should be strongly suspected.
Dystocia in chelonia rarely presents as a life-threatening emergency, as chelonia can retain eggs for extended periods of time (Innis and Boyer 2002, McArthur and Hernandez-Divers 2004). In the three cases presented here, there was good historical and physical evidence that egg retention was pathologic and required therapeutic intervention. Treatment options include surgical and non-surgical intervention. Non-obstructive dystocia should be initially treated by correcting and treating possible underlying infectious or metabolic disorders, by providing a suitable nesting site and substrate and by ensuring appropriate environmental temperatures and humidity (McArthur 2004). Oxytocin is reported as a successful medical treatment option to induce oviposition in chelonia (Johnson 2004, DeNardo 2006). In case 3 of this report, oxytocin was administered for this indication. However, in retrospect, the use of oxytocin in this case may not have been appropriate, since oxytocin administration should be limited to cases in which an obstructive cause for dystocia has been ruled out. Possible complications associated with oxytocin administration in obstructive dystocias include oviductal spasms and rupture and ectopic eggs in the urinary bladder in chelonia (Wilkinson 2004, Minter and others 2010).
Immediate surgical intervention is rarely beneficial, particularly in chelonia with non-obstructive dystocia, or with underlying systemic or infectious disease, which should be corrected first. However, in cases of obstructive dystocia (case 3) or other disorders, such as oviductal rupture associated with haemorrhage (case 1), delaying surgical intervention can potentially contribute to further deterioration of the patients’ condition. The transcloacal approach, under endoscopic guidance, allows removal of retained eggs from the vagina, cloaca and urinary bladder (Knotek and others 2009, Minter and others 2010). This technique was used in case 3, to successfully remove the caudal-most egg, which facilitated normal oviposition of the remaining eggs. This approach also facilitated visualisation of adhesions between the caudal-most egg and the vaginal wall, as well as diagnosis of severe bacterial salpingitis.
Salpingotomy and ovariosalpingectomy were reported for treatment of obstructive and non-obstructive dystocia in captive and wild chelonia with varied success (Hernandez-Divers 2004, DeNardo 2006, Innis and others 2007, Sykes 2010). Salpingotomy may be necessary for those chelonians in which breeding viability must be maintained (Innis and Boyer 2002). For captive chelonians not intended for breeding, ovariosalpingectomy is preferred to salpingotomy to eliminate the risk of dystocia recurrence in cases diagnosed with oviductal disease (Hernandez-Divers 2004). Both surgical procedures can be performed via the prefemoral approach or central plastron osteotomy (Hernandez-Divers 2004). The prefemoral approach into the coelomic cavity was chosen in cases 1 and 2 because of the previously described safety and efficacy of this procedure for ovariectomy and unilateral salpingectomy in red-eared slider turtles (Innis and others 2007). It has been previously suggested that salpingectomy of a diseased oviduct, and egg removal via the prefemoral approach, can potentially be more difficult compared to a central plastron osteotomy (DeNardo 2006). In cases 1 and 2, the bilateral prefemoral approach to the coelom was sufficient for complete removal of both ovaries and oviducts without any associated short-, or long-term complications. In addition, the prefemoral approach was suitable for removal of ectopic eggs from the coelom (case 1), and lavage of the coelom for treatment of yolk coelomitis (case 2). Bilateral ovariosalpingectomy, by a bilateral prefemoral approach, for the treatment of oviductal disease in chelonia, has not been reported in the literature.
By using a bilateral prefemoral approach to the coelom in case 1 and 2, the more invasive central plastron osteotomy technique was avoided, which is associated with prolonged surgical procedure time, an increased risk of postsurgical complications, and is thought to be significantly more painful compared to the prefemoral soft tissue approach (Innis and others 2007). Most importantly, the healing times after prefemoral coeliotomy (approximately 4 weeks) are substantially shorter than after a plastron osteotomy (approximately 1 to 2 years) (Mader and others 2006). In aquatic and semi-aquatic chelonia, early return to the aquatic environment is critical to allow normal behaviour, food intake and defecation. The prefemoral approach significantly shortens the post-surgical duration, during which time the turtle must be maintained out of water. Therefore, the prefemoral approach should be considered the preferred surgical approach to the coelom in aquatic and semi-aquatic chelonian species.
In conclusion, oviductal disease in captive red-eared slider turtles can be reliably diagnosed based on a thorough history, physical examination and appropriate diagnostic testing. Treatment of oviductal disease should be based on the underlying cause. In the absence of concurrent disease, the long-term prognosis for red-eared slider turtles diagnosed with oviductal disease appears to be good, following appropriate treatment. In the three cases described here, no complications or disease recurrence were reported, 23 to 33 months later after successful treatment.
Conflict of interest
None of the authors of this article has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper.