A 40-yr-old female red-eared slider (Trachemys scripta elegans) was presented for acute lethargy and anorexia of 48 h duration. A dorsoventral radiograph revealed a single hypercalcified egg within the left oviduct. Hematology and plasma biochemical values were considered normal for a gravid turtle. Administration of oxytocin failed to induce oviposition. Prefemoral salpingotomy with the aid of carbon dioxide laser facilitated removal of a necrotic egg after fragmentation of the egg in situ. Endoscopic examination of the lumen of the oviduct (salpingoscopy) through the salpingotomy incision provided direct visualization of oviductal mucosa, ruled out obstructive lesions, and confirmed complete removal of the egg and its contents. The turtle's appetite returned to normal 24 h after surgery.

A 1.17-kg, 40-yr-old female red-eared slider (Trachemys scripta elegans) was presented for acute lethargy and anorexia of 48 h duration. Husbandry was considered acceptable for this species. On the basis of a scoring system from 1 to 5, the turtle's gross body condition score was judged to be 4 (Calvert, 2004). Ballottement of the left pre-femoral fossa revealed a firm density. A dorsoventral (DV) radiograph revealed a single egg within the left oviduct. The egg possessed multiple concentric layers of radiopaque lamellae consistent with hypercalcification (Rubel et al., 1991) (Fig. 1). Skeletal density of the turtle was considered normal. The maximum widths of the egg and pelvic canal were 25 and 30 mm, respectively. Blood was collected for hematology and plasma biochemical analysis from the right jugular vein using a preheparinized syringe and 25 gauge needle. The turtle had an elevated total plasma calcium value of 22.0 mg/dl (reference value, 12.8 ± 3.0 mg/dl) (International Species Information System, 2002). A diagnosis of pathologic egg retention was made based upon excessive mineralization of the shell.

Figure 1.

Dorsoventral radiographic view of a retained egg in Trachemys scripta elegans. Note the irregular calcium deposits on the shell.

Figure 1.

Dorsoventral radiographic view of a retained egg in Trachemys scripta elegans. Note the irregular calcium deposits on the shell.

Close modal

During the previous 6 yr, the turtle had periodic incidences of anorexia lasting several days that were associated with gravidity. Normal appetite would resume after expulsion of eggs into the aquatic environment. Approximately 48 months before the current presentation, oviposition was successfully induced using calcium gluconate (20 mg/kg IM, Abraxis, Schaumburg, IL) followed 2 h later with oxytocin (Oxyject, 10 U/kg IM, Butler-Schein, Dublin, OH) and provision of a terrestrial nest site.

The turtle was released to the owner with instructions to provide a terrestrial nest site and to administer oxytocin (10 U/kg IM q8h for up to three treatments). Three weeks later, a DV radiograph revealed that the egg's width had increased to 30 mm due to continued calcium deposition from the shell gland. The egg's width was now equal to that of the pelvic canal. A prefemoral salpingotomy was recommended to remove the egg.

Carprofen (Rimadyl, 4 mg/kg IM, Pfizer, New York, NY) and piperacillin (Abraxis; 100 mg/kg IM) were administered 24 h before surgery in the right and left pectoralis major muscles, respectively. Preemptive use of a broad-spectrum bactericidal antibiotic was done to reduce the risk of possible bacteremia during surgery. Glycopyrrolate (0.01 mg/kg IM, American Regent, Shirley, NY) was administered 1 h before anesthetic induction. The turtle was maintained in an aquatic environment until 30 min before anesthetic induction. Propofol (PropoFlo, 5.0 mg/kg IV, slowly over 30 sec, Abbott Laboratories, Chicago, IL) was administered through the right jugular vein. The turtle was intubated with a 3.0 mm uncuffed endotracheal tube and connected to 1.5% isoflurane and 100% oxygen, at a flow rate of 1.0 L/min. Intermittent positive pressure ventilation was administered with a mechanical ventilator (Small Animal Ventilator, Vetronics, West Lafayette, IN) set to 8.1 cm water pressure with an expiratory length of 15 sec. The turtle was placed in dorsal recumbency on a circulating warmed water pad (T/PUMP, Gaymar Industries, Orchard Park, NY) set to 29°C (84°F). An electrocardiographic monitor display (Datascope 870, Datascope, Paramus, NJ) with leads placed bilaterally on the cervical and stifle regions revealed P and R waves with a sinus rhythm of 75–90 beats/min. Temperature of the surgical operatory was maintained at 29°C (84°F) for the duration of the procedure. The surgical area was disinfected with 2.0% chlorhexidine digluconate and quaternium-33 1.5% scrub and solution (ChlorHex-Q SCRUB, Vedco, St. Joseph, MO).

A horizontal incisional line block, approximately 2.5 cm in length, was made in the center of the left prefemoral fossa. A combination of 2% lidocaine (2 mg/kg SQ, Hospira, Lake Forest, IL) and 0.5% bupivacaine (2 mg/kg SQ, Marcaine, Hospira) diluted with sterile saline to a volume of 1 ml was used. Fifteen minutes later, the skin was incised with a carbon dioxide (CO2) laser (Shanghai Wonderful Opto- Electrics Technology, Shanghai, China) with a 0.4 mm hand piece. Power was set to 6 W with a focused continuous beam. The CO2 laser, at the same settings, was then used to incise the aponeurosis of the transverse and oblique abdominal muscles. Stay sutures (3/0 polyglycolide-co-caprolactone, Vedco) were placed through the skin and muscle layers and anchored to the surgical drape. The left oviduct was visualized immediately beneath the incised muscle layer (Fig. 2). Attempts to exteriorize the egg were unsuccessful due to size disparity between the egg and prefemoral fossa. Stay sutures were then placed through the oviduct at either end of the proposed salpingotomy site and anchored to the surgical drape. Sterile gauze pads were placed intraoperatively around the oviduct to prevent possible contamination of the coelom. An incision, parallel with the long axis of the oviduct and 2.5 cm in length, was made with CO2 laser (4 W) between the stay sutures, whereupon the egg became visible. Attempts at ovocentesis using a sterile 18 gauge needle attached to a 10 ml syringe were unsuccessful due to inspissated egg contents. An Allis tissue forceps (Misdom Frank and Sklar, West Chester, PA) was used to fragment and collapse the malodorous egg and remove it from the oviduct (Fig. 3). A sterilized 2.7 mm Hopkins rigid endoscope with 30° oblique view within a 14.5 French operating sheath (Karl Storz Veterinary Endoscopy-America, Goleta, CA) connected to a halogen light source was then inserted through the salpingotomy incision and advanced approximately 3.0 cm anterior and 4.0 cm posterior to the original location of the egg (Fig. 4). A video camera (Stryker, Santa Clara, CA) connected from the endoscope to a monitor was used to capture images. There were no shell fragments or egg contents present in the affected oviduct. No obstructive lesions such as stricture, granuloma, or neoplasia were visualized. The oviduct was sutured with an absorbable monofilament (3-0 polyglycolide-co-caprolactone, Vedco) in a simple continuous pattern. The aponeurosis of the transverse and oblique abdominal muscles was sutured in a similar manner. The skin was sutured with a nonabsorbable monofilament nylon (3-0 Monolon Blue, Vedco) in an interrupted horizontal mattress pattern. Total surgical time was 75 min. A postsurgical DV radiograph confirmed complete removal of the retained egg.

Figure 2.

Prefemoral coeliotomy incision with carbon dioxide laser. Note the absence of hemorrhage. The skin and aponeurosis of the transverse and oblique abdominal muscles have been incised revealing the oviduct.

Figure 2.

Prefemoral coeliotomy incision with carbon dioxide laser. Note the absence of hemorrhage. The skin and aponeurosis of the transverse and oblique abdominal muscles have been incised revealing the oviduct.

Close modal
Figure 3.

Retrieval of shell pieces with Allis tissue forceps after egg fragmentation in situ.

Figure 3.

Retrieval of shell pieces with Allis tissue forceps after egg fragmentation in situ.

Close modal
Figure 4.

Salpingoscopic view of oviductal mucosa anterior (A) and posterior (B) to site of the retained egg.

Figure 4.

Salpingoscopic view of oviductal mucosa anterior (A) and posterior (B) to site of the retained egg.

Close modal

Postoperatively, the turtle was administered warmed lactated Ringer's solution (Baxter, Deerfield, IL) at 25 ml/kg by intrapleuroperitoneal injection between the pectoral girdles and plastron. The turtle became ambulatory approximately 1 h after surgery and was discharged 24 h later. Treatment with piperacillin q 48 h IM for five treatments in the pectoralis major muscle was continued by the owner. The turtle's appetite returned to normal 24 h after discharge from the hospital. The turtle was maintained in water for 12 h daily and dry docked in the evening for 1 wk. There after, the turtle was returned to its aquatic habitat. Skin sutures were removed 6 wk later.

Spontaneous egg formation is relatively common in several species of captive reptiles despite the absence of con-specific males (DeNardo, 2006). In chelonians, the presence of shelled eggs in itself is not diagnostic of reproductive pathology. In fact, gravidity is commonly an incidental radiographic finding in chelonians. The use of diagnostic terms such as retained eggs, egg binding, and dystocia should be restricted to cases where there is clinical evidence, radiographic evidence, or both to support the diagnosis. Clinical symptoms commonly consist of anorexia with lethargy or excessive straining without oviposition (Johnson, 2004; McArthur, 2004). Radiographic evidence of prolonged egg retention includes severely deformed or excessively large eggs compared with normal egg size for a given taxon, excessive shell mineralization, large cystic calculi, and injuries to the vertebral column or pelvis (Johnson, 2004; McArthur, 2004; DeNardo, 2006). Under natural conditions, all chelonians normally retain shelled eggs for a variable period of time before oviposition (Ernst and Lovich, 2009).

In the United States, red-eared sliders construct nests and oviposit from mid-April to mid-July (Ernst and Lovich, 2009). Field studies have determined that ovulation and shelling of eggs occurs less than a week before nesting (Whitfield Gibbons and Greene, 1990). The longest egg retention time recorded for a red-eared slider during nesting season in South Carolina was 39 days (Buhlman et al., 1995). Photoperiod and water and air temperatures are considered to be the inducers of ovulation and nesting (Whitfield Gibbons and Greene, 1990). Under natural conditions, red-eared sliders are known to oviposit multiple clutches during the nesting season. Prolonged egg retention is considered normal for temperate turtles found at the colder limit of the species' range. For example, the North American chicken turtle (Deirochelys reticularia) may retain calcified oviductal eggs through the winter until more favorable nesting conditions the following spring (Buhlman et al., 1995). Egg retention times for this species range from 4 months (120 days) to 6.5 months (197 days) (Buhlman et al., 1995). Pathologic egg retention, as in this case, is usually associated with poor husbandry or underlying disease. Common examples of inappropriate husbandry are suboptimal temperatures, poor nutrition, and lack of a suitable nest site. Owners rarely provide appropriate nest sites because either the sex of the turtle is unknown or it is assumed that lone females are not capable of egg production. Captive red-eared sliders commonly oviposit in the water or when roaming the house.

In reptiles, anorexia can be a normal response during brumation, aestivation, courtship, folliculogenesis, and gravidity (McArthur and Divers, 2004; Funk, 2006). However, lethargy in a gravid reptile should alert the clinician to possible illness. In this case, acute lethargy and anorexia were the only symptoms of egg binding (dystocia). Straining can be symptomatic of egg binding, constipation, intestinal obstruction, and urolithiasis (Johnson, 2004; McArthur, 2004). Ballottement of eggs through the prefemoral fossae and radiography are used to diagnose gravidity in chelonians. In this case, serial radiography revealed an excessively mineralized egg due to prolonged retention in the shell gland of the oviduct. Hypercalcemia is a normal finding that is associated with ovarian activity or gravidity (Wilkenson, 2004). Gravid chelonians can also present for continued anorexia after passage of a partial clutch of eggs. This does not necessarily mean the turtle is “egg bound,” particularly if the remaining eggs are of normal size and shape. The owner should be instructed to provide a terrestrial nesting site to stimulate oviposition over a period of several weeks. It is unknown how long chelonians can retain their eggs before pathology of the reproductive system develops. In this case, it is suspected that prolonged retention time led to continued mineralization and necrosis of the egg.

The reported dosages of oxytocin used to induce oviposition in chelonians range from 1 to 20 IU/kg IM q 4–6 h for one to three treatments (Johnson, 2004; McMarthur, 2004; DeNardo, 2006). A dose of 10 IU/kg IM administered to 49 wild gravid red-eared sliders had an initial success rate of 91.8%; when it was repeated in 12 h, the overall success rate was 100% (Tucker et al., 2007). In this case, a lack of response to oxytocin may have been due to oviductal fatigue secondary to chronic distension by the retained egg. The use of parenteral calcium has been recommended to “prime” oviductal smooth muscle to make it more receptive to oxytocin (Johnson, 2004; McArthur, 2004). The author prefers to administer calcium only in cases of hypocalcemia. The use of oxytocin at excessively high doses presents potential risks such as movement of eggs into the urinary bladder (Wilkinson et al., 2004; Minter et al., 2010). If there is oviductal rupture, eggs can pass into the coelomic cavity.

There are three approaches to the chelonian reproductive tract: 1) plastron osteotomy, 2) prefemoral coeliotomy, and 3) cloacoscopy (Hernandez-Divers, 2004; Innis, 2010). An advantage of plastron osteotomy is increased surgical access to visceral organs (Hernandez-Divers, 2004; McArthur and Hernandez-Divers, 2004). Advantages of the prefemoral approach are reduced surgical time, decreased healing time, and decreased postoperative pain (Innis et al., 2007; Hernandez-Divers et al., 2009; Stahl, 1999). Prefemoral coeliotomy has been used for exposure of the reproductive, intestinal, and urinary tracts (Gould et al., 1992; Stahl, 1999; Hernandez-Divers, 2004; Innis et al., 2007; Hernandez-Divers et al., 2009; Divers et al., 2010; Innis, 2010). Examples of surgical procedures using the prefemoral approach are incisional biopsies, oophorectomy, salpingotomy, salpingectomy, cystotomy, enterotomy, and endoscopic sex determination of immature chelonians (Stahl, 1999; Hernandez-Divers, 2004; Hernandez-Divers et al., 2009). Another method to gain access to the distal urogenital tract is the use of endoscopic examination through the cloaca (cloacoscopy). Cystoscopic retrieval of ectopic eggs with a flexible endoscope and oval loop snare has been described using the cloacal approach (Minter et al., 2010).

In this case, insertion of an endoscope through the salpingotomy incision provided direct visualization of oviductal mucosa confirming complete removal of a retained necrotic egg. It also ruled out obstructive abnormalities due to stricture, granuloma, or neoplasia. In retrospect, additional diagnostics such as cytology and microbiological culture and sensitivity should have been considered. Bilateral oophorectomy was not done due to concern for the turtle's advanced age and increased surgical time. Endoscopic examination of the oviductal lumen through a salpingotomy incision is an additional technique to be considered during surgical procedures of the chelonian reproductive tract.

Buhlman
K
,
Lynch
T
,
Gibbons
J.
1995
.
Prolonged egg retention in the turtle Deirochelys reticularia in South Carolina
.
Herpetologica
,
51
(
4
):
457
462
.
Calvert
I.
2004
.
Nutrition
.
In
Girling
S
,
Raiti
P
(
eds
):
BSAVA Manual of Reptiles
.
British Small Animal Veterinary Association
,
Gloucester, UK
:
18
39
.
DeNardo
D.
2006
.
Dystocia
.
In
Mader
DR
(
ed
):
Reptile Medicine and Surgery
.
Saunders Elsevier
,
St. Louis, MO
:
787
792
.
Divers
S
,
Stahl
S
,
Camus
A.
2010
.
Evaluation of diagnostic celioscopy including liver and kidney biopsy in freshwater turtles Trachemys scripta
.
J Zoo Wildl Med
,
41
(
4
):
677
687
.
Ernst
C
,
Lovich
J.
2009
.
Turtles of the United States and Canada
.
Johns Hopkins University Press
,
Baltimore, MD
:
444
470
.
Funk
R. Anorexia
.
2006
.
In
Mader
DR
(
ed
):
Reptile Medicine and Surgery
.
Saunders Elsevier
,
St. Louis, MO
:
739
741
.
Gould
W
,
Yaeger
A
,
Glennon
J.
1992
.
Surgical correction of an intestinal obstruction in a turtle
.
J Am Vet Med Assoc
,
200
(
5
):
705
706
.
Hernandez-Divers
S.
2004
.
Diagnostic and surgical endoscopy
.
In
Girling
S
,
Raiti
P
(
eds
):
BSAVA Manual of Reptiles
.
British Small Animal Veterinary Association
,
Gloucester, UK
:
103
114
.
Hernandez-Divers
S.
2004
.
Surgery: principles and techniques
.
In
Girling
S
,
Raiti
P
(
eds
):
BSAVA Manual of Reptiles
.
British Small Animal Veterinary Association
,
Gloucester, UK
:
147
167
.
Hernandez-Divers
S
,
Stahl
S
,
Farrell
R.
2009
.
An endoscopic method for identifying sex of hatchling Chinese box turtles and comparison of general versus local anesthesia for coelioscopy
.
J Am Vet Med Assoc
,
234
(
6
):
800
804
.
Innis
C.
2010
.
Endoscopy and endosurgery of the chelonian reproductive tract
.
Vet Clin Exot Anim
,
13
(
2
):
243
254
.
Innis
C
,
Hernandez-Divers
S
,
Martinez-Jimenez
D.
2007
.
Celioscopic-assisted prefemoral oophorectomy in chelonians
.
J Am Vet Med Assoc
,
230
(
7
):
1049
1052
.
International Species Information System
.
2002
.
Physiological Data Reference Values
.
ISIS
,
Apple Valley, MN [CD Rom]
.
Johnson
J.
2004
.
Urogenital system
.
In
Girling
S
,
Raiti
P
(
eds
):
BSAVA Manual of Reptiles
.
British Small Animal Veterinary Association
,
Gloucester, UK
:
261
272
.
McArthur
S.
2004
.
Problem-solving approach to common diseases of terrestrial and semi-aquatic chelonians
.
In
McArthur
S
,
Wilkinson
R
,
Meyer
J
(
eds
):
Medicine and Surgery of Tortoises and Turtles
.
Blackwell Publishing Ltd.
,
Oxford, UK
:
309
377
.
McArthur
S
,
Hernandez-Divers
S.
2004
.
Surgery
.
In
McArthur
S
,
Wilkinson
R
,
Meyer
J
(
eds
):
Medicine and Surgery of Tortoises and Turtles
.
Blackwell Publishing
,
Oxford, UK
:
403
464
.
Minter
L
,
Wood
M
,
Hill
T
,
Lewbart
G.
2010
.
Cystoscopic guided removal of ectopic eggs from the urinary bladder of the Florida cooter turtle, Pseudemys floridana floridana
.
J Zoo Wildl Med
,
41
(
3
):
503
509
.
Rubel
G
,
Isenbugel
E
,
Wolvekamp
P.
1991
.
Atlas of Diagnostic Radiology of Exotic Pets
.
W. B. Saunders
,
Philadelphia, PA
:
194
.
Stahl
S.
1999
.
Prefemoral approach to celiotomy in chelonians
.
Proc Int Conf Exotics
,
15
19
.
Tucker
J
,
Thomas
D
,
Rose
J.
2007
.
Oxytocin dosage in turtles
.
Chel Conserv Biol
,
6
(
2
):
321
324
.
Whitfield Gibbons
J
,
Greene
J.
1990
.
Reproduction in the slider and other species of turtles
.
In
Whitfield Gibbons
J
(
ed
):
Life History and Ecology of the Slider Turtle
.
Smithsonian Institution Press
,
Washington, DC
:
124
134
.
Wilkinson
R.
Clinical pathology
.
2004
.
In
McArhur
S
,
Wilkinson
R
,
Meyer
J
(
eds
):
Medicine and Surgery of Tortoises and Turtles
.
Blackwell Publishing
,
Oxford, UK
:
141
186
.
Wilkinson
R
,
Hernandez-Divers
S
,
Lafortune
M
,
Calvert
I
,
Gumpenberger
M
,
McArthur
S.
2004
.
Diagnostic imaging techniques
.
In
McArhur
S
,
Wilkinson
R
,
Meyer
J
(
eds
):
Medicine and Surgery of Tortoises and Turtles
.
Blackwell Publishing
,
Oxford, UK
:
187
238
.