Ovarian Teratoma in a Fiji Island Banded Iguana (Brachylophus fasciatus) and a Green Iguana (Iguana iguana) Sandra Wenger1, DMV, DECVAA, Stefka Simova-Curd1, DMV, Paula Grest2, DMV, DECVP, Hanspeter W. Steinmetz1, DMV, MS, Jean-Michel Hatt1, DMV, DACZM, DECZM (Avian)

1. Vetsuisse Faculty, Clinic for Zoo Animals, Exotic Pets and Wildlife, University of Zurich, Winterthurerstrasse 260, 8057 Zürich, Switzerland

2. Vetsuisse Faculty, Institute of Veterinary Pathology, University of Zurich, Winterthurerstrasse 260, Downloaded from http://meridian.allenpress.com/jhms/article-pdf/20/1/20/2208872/1529-9651-20_1_20.pdf by guest on 30 September 2021 8057 Zürich, Switzerland

ABSTRACT: A six-year-old female Fiji Island banded iguana, Brachylophus fasciatus, and a nine-year-old female green iguana, Iguana iguana, were presented with anorexia and coelomic distension. Exploratory coeliotomies were performed in both individuals. The left ovaries were grossly abnormal, enlarged, and contained smaller fluid-filled vesicles. The abnormal tissue was resected and examined histologically. In both cases the histological diagnosis of benign ovarian teratoma was made. Both iguanas recovered well from surgery. Ten months post-surgery, both iguanas were clinically healthy.

KEY W ORDS: Brachylophus fasciatus, Fiji Island banded iguana, green iguana, Iguana iguana ovary, teratoma.

CASE REPORT 1 unknown origin was suspected. The liver abnormalities were consistent with metabolic hepatopathy such as lipidosis or A six-year-old female Fiji Island banded iguana, Brachylo- diffuse neoplasia. phus fasciatus, was presented with anorexia of four days We decided to perform an exploratory coeliotomy. duration. It was housed together with a male in a glass Anesthesia was induced with 20 mg/kg propofol IV (Propo- terrarium. The temperature gradient was maintained fol®1%, Fresenius Kabi Ag, Stans, Switzerland). Following between 20° and 26°C (68° and 79°F) and relative humidity intubation, the patient was maintained on 2% isoflurane at 70–80%. The diet consisted of insects, fruits, and vegeta- (IsoFlo®, Abbott, Baar, Switzerland) with positive pressure bles. Four years prior to presentation, surgical removal of ventilation at a rate of 12 breaths/min (Vetronic Services four eggs had been performed because of dystocia (egg- Ventilator, Abbotskerswell, U.K.). The iguana received binding). At that time, hematology and blood chemistry 0.9 mg/kg morphine (Morphine HCl 10 mg, Sintetica S.A., were within normal limits. Reference intervals established Mendrisio, Switzerland) IM q 24 h for two treatments and by the International Species Information System (ISIS 0.25 mg/kg meloxicam (Metacam 5 mg/ml, Boehringer Physiological Data Reference Values 2002 ed., Apple Valley, Ingelheim GmbH, Basel, Switzerland) SC q 48 h for three MN) were used as comparison. Two years later, hypocalce- treatments. A heating pad was placed beneath the animal mia with tremors and somnolence had been diagnosed. The to maintain body temperature near 28–30°C (82–86°F). A animal had recovered well with calcium and fluid treatment. bolus of 40 ml/kg warm, 1:1 solution of glucose 2.5% and Since then, the patient had shown intermittent dysecdysis NaCl 0.45% (Mischinfusion für Reptilien, Kantonsapo- and multifocal blackish cutaneous discoloration over the theke, Zurich, Switzerland) was administered IV and SC. dorsal aspect of the neck and shoulder area for two years. Heart rate was monitored with a Doppler unit (Ultrascope®, Because fungal and bacteriological cultures were negative, EMS Products, Kirkland, WA) placed sternally at the level it was suspected that the dark discoloration of the skin was of the pectoral girdle. The skin was prepared for surgery secondary to bruising caused by the male. with chlorhexidine (Hibiscrub®, Globopharm AG, Zurich, On clinical examination, the Fiji Island banded iguana Switzerland). A paramedian incision was performed. The appeared alert, was in a moderate body condition, and left ovary was grossly abnormal, enlarged (2 cm × 5 cm × weighed 158 g. The coelomic cavity was enlarged, but no 4 cm), and multilobulated. The ovarian and cut surfaces obvious eggs were palpated. Ultrasonographic findings were mottled and tan-yellow to red in color. The ovary con- included an enlarged, hyperechogenic liver with otherwise tained multiple small vesicles filled with clear fluid that normal shape, smooth contours, and homogeneous echotex- comprised two thirds of its size; they were consistent with ture. Multiple round, anechoic cysts (varying between 3 mm the anechoic structures seen on the ultrasound. There were and 10 mm in diameter) and hyperechoic areas were seen on yellowish fibrinous adhesions between the mass and the the left side of the coelom (Fig. 1). The stomach and colon gastrointestinal tract, liver, and lungs. Some free fluid was appeared normal, but the rest of the gastrointestinal tract present within the coelomic cavity and was suspected to be could not be differentiated from the round structures. No a sequel to the inflammatory process present around the free coelomic fluid could be seen. A neoplastic mass of ovary. The abnormal ovary and part of the adhesions

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Figure 1. Ultrasonographic view of the coelom performed from the left side showing multiple round, anechoic (white arrow), and hyperechoic (black star) structures.

were resected. The coelom was flushed with saline (NaCl dietary intake. The iguana was force-fed with larger quanti- 0.9%, Fresenius Kabi AG, Bad Homburg, Germany) and ties, but otherwise no additional investigations regarding 30 mg/kg doxycycline (Vibravenös, Pfizer AG, Zürich, the possible liver problem were performed. Five weeks after Switzerland) was instilled into the coelom. The incision was surgery, the patient started feeding on its own and two closed in two layers with absorbable suture in an interrupted months after surgery weighed 123 g. pattern (3-0 and 4-0 Vicryl®, Ethicon, Johnson and Johnson Histologically, the normal ovarian tissue was completely Intl., Norderstedt, Germany). After surgery the animal replaced by an unencapsulated neoplasm composed of tissue weighed 118 g. A swab was taken from the yellowish adhe- from all three primordial germ lines that were arranged as sions and sent for bacteriological culture. The sample was solid and cystic areas. The solid areas were composed of incubated at 35°C (95°F) and 37°C (98.6°F) for 48 hours moderately cellular fibrous and striated muscular tissue as using blood agar and Gassner’s culture medium. The well as loosely arranged fatty tissue with interspersed vessels resected material was fixed in 10% neutral buffered forma- and nerve fibers (Fig. 2). Cysts measured up to 0.8 mm in lin, processed by routine methods to paraffin block, and diameter and were lined by a single layered, cuboidal to then reviewed as hematoxylin and eosin-stained histologic columnar epithelium resembling respiratory epithelium with sections (4 µm). multifocal presence of cilia and goblet cells. Many cysts were filled with pale amphophilic material consistent with The iguana recovered well from anesthesia. It was treated secretion products from the goblet cells within the cyst prophylactically with 25 mg/kg ceftazidime (Fortam 500 mg, lining. Because of rupture of some cysts, this material was GlaxoSmithKline, Münchenbuchsee, Switzerland) SC q released multifocally in the adjacent tissue and caused 72 h for four treatments. Fluid therapy was continued for granulomatous inflammation. Mitotic figures were not two days after surgery. No bacterial growth was evident seen in the neoplastic cells. The histological changes were from the swab taken intraoperatively from the coelomic consistent with benign ovarian teratoma. cavity. Ten months after surgery, the iguana was in good general In the following weeks, the patient was alternately force- condition and weighed 147 g. A routine ultrasonographic fed insects and a fruit/vegetable puree mixed with a recovery examination was performed, and a region consisting of food designed for carnivores (Carnivore care, Oxbow anechoic cystic and hyperechoic areas could be visualized in Animal Health, Murdock, NE), because it did not feed the midcoelom. A mass was suspected, and we decided to properly on its own. Four weeks after surgery, the iguana perform a coelioscopy under anesthesia as described above. was re-examined and found to be in poor body condition No mass could be seen in the coelomic cavity. The repro- (76 g). A blood sample was collected from the ventral ductive tract appeared normal, and four to five follicles tail vein. Hematological values were within normal limits, could be seen. It is possible that the anechoic cystic and and there was no evidence of infection. Low uric acid hyperchoic areas seen in the ultrasonographic examination (0.066 mmol/L, reference value: 0.309 ± 0.184 mmol/L) was represented normal follicles. Hematological and biochemi- seen as possibly indicating a liver problem or insufficient cal values were within normal limits at that time.

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Figure 2. Photomicrograph of the ovarian teratoma in a Fiji Island banded iguana. Multiple variably sized cysts lined by a respi- ratory epithelium (inset) are embedded in a stroma composed of fatty (*) and muscular (arrow) tissue, Hematoxylin and Eosin, bar = 100 µm.

CASE REPORT 2

The second case involved a nine-year-old female green iguana, Iguana iguana, presenting with coelomic distension. It was housed together with two male green iguanas and fed mainly vegetables. On initial presentation, the iguana weighed 3.25 kg and appeared depressed. The coelomic cavity was enlarged, painful, and had a firm consistency. Whole body radiographs revealed the presence of a moder- ate amount of free coelomic fluid and a mass (10 cm × 5 cm) of soft tissue opacity in the caudal half of the coelomic cavity. A coeliotomy was performed under anesthesia as described above. The animal received 0.6 mg/kg morphine IM q 24 h for two treatments and 0.1 mg/kg meloxicam q 48 h for three treatments. The left ovary was enlarged (10 cm × 5 cm × 8 cm), weighing 1.15 kg, had an irregular surface, and contained multiple fluid-filled cysts of varying size (Fig. 3). The right ovary and the remaining coelomic Figure 3. Gross photograph of the ovarian teratoma organs appeared normal. The abnormal ovary was resected. removed from a green iguana. The green iguana recovered uneventfully from anesthesia. The patient was treated with 20 mg/kg ceftazidime SC q 72 h for six doses, 90 mg/kg sucralfate (Ulcogant®Suspension, was alert, feeding on its own, and the wound was healing Merck AG, Zug, Switzerland) PO q 24 h for one week, and well. Ten months later, the owner reported that the iguana 0.7 mg/kg ranitidine (Zantic®, GlaxoSmithKline, München- was in good general condition and active. buchsee, Switzerland) PO q 24 h for one week. One day after Histologically, most of the ovarian tissue was replaced surgery, the animal was discharged; it was rechecked one by a mass that was composed of multiple variably sized week later. At the time of re-examination, the green iguana cysts lined by a cuboidal to flattened epithelium and were

22 Journal of Herpetological Medicine and Surgery Volume 20, No. 1, 2010 embedded within connective fibrous tissue, striated muscu- in a green iguana 18 months after surgical removal (Ander- lar tissue, and fatty tissue. Multifocally, mature cartilage son et al., 1996). The authors recommended that reptiles and glandular tissue were present, whereas neuronal tissue should be carefully monitored for recurrence of the tumor was not detected. A diagnosis of benign ovarian teratoma after surgical removal of a teratoma. In both cases reported was made. here, the teratomas were classified as benign, because there was no evidence of immature embryonal tissue. Ten months DISCUSSION after surgery, the Fiji Island banded iguana was in good general condition and showed normal ovarian activity. The Teratomas are neoplasms that arise from pluripotent germ owner of the green iguana also reported that the animal cells and have disorganized elements of at least two of the was doing well. The weights and general condition of both three embryonic germ layers (Foster, 2007). They are com- iguanas will continue to be monitored on a regular basis. posed of multiple tissues that are foreign to the part of the Teratomas are usually hormonally inactive and do not body in which they arise. Ovarian teratomas have been affect reproductive function (Catone et al., 2004). Normal reported in mammals, birds, and reptiles but are considered developing follicles and calcified eggs in the oviduct were rare (Frisk et al., 1978; Anderson et al., 1996; Basaraba seen in a red-eared slider turtle with benign ovarian tera- Downloaded from http://meridian.allenpress.com/jhms/article-pdf/20/1/20/2208872/1529-9651-20_1_20.pdf by guest on 30 September 2021 et al., 1998; Bolte and Burkhardt, 2000; Tocidlowski et al., toma (Hidalgo-Vila et al., 2006). In this case report, the Fiji 2001; Newman et al., 2003; Catone et al., 2004; Hidalgo- Island banded iguana did not produce any eggs in the year Vila et al., 2006). In reptiles, teratomas arise mainly from she was presented. Reproductive function was probably gonadal tissues; ovarian teratomas have been described indirectly affected as the tumor grew, and adhesions may in the suborders serpentes, sauria and chelonia (Anderson have caused coelomic pain and pressure symptoms. In con- et al., 1996; Frye and Randall, 1999; Hertha et al., 2000; trast, histological evidence of normal ovarian tissue with Tocidlowski et al., 2001; Newman et al., 2003; Hidalgo-Vila et al., 2006). In a retrospective study on reptile neoplasia, a follicles was found in the excised mass of the green iguana. prevalence of 1.2% was noted for teratomas in lizards, and Ovarian teratomas should be considered as a differential both cases were diagnosed in iguanids (Garner et al., 2004). in animals presenting with coelomic distension. Performing Also, teratomas have been described in two desert grassland ultrasonography or radiography was helpful in making the whiptails, which belong to the family Teiidae (Tocidlowski decision to perform exploratory surgeries in these cases. et al., 2001). Both of our cases belong to the family Iguani- dae. It is possible that there is a higher prevalence of ovarian LITERATURE CITED teratomas in the iguanids compared to other lizards; how- ever, this would need to be investigated further to confirm. Anderson N, Williams J, Sagartz J, Barnewall R. 1996. Ovar- Other ovarian neoplasia found in reptiles include ovarian ian teratoma in a green iguana (Iguana iguana). J Zoo Wildl adenocarcinoma and granulosa cell tumor (Garner et al., Med, 27:90–95. 2004). Basaraba RJ, Kraft SL, Andrews GA, Leipold HW, Small D. The clinical signs in reptiles with teratomas described 1998. An ovarian teratoma in a cat. Vet Pathol, 35:141–144. in the literature vary from none to lethargy, anorexia, Bolte AL, Burkhardt E. 2000. A teratoma in a Muscovy duck and abdominal/coelomic distension (Anderson et al., 1996; (Cairina moschata). Avian Pathol, 29:237–239. Newman et al., 2003; Hidalgo-Vila et al., 2006). Both ani- Catone G, Marino G, Mancuso R, Zangh A. 2004. Clinico- mals in this case report presented with coelomic distension, pathological features of an equine ovarian teratoma. Reprod and additionally the Fiji Island banded iguana showed Domest Anim, 39:65–69. anorexia. Rapid growth of the ovarian teratoma was seen in Foster R. 2007. Female reproductive system. In McGavin M, both patients, which is consistent with documented cases in Zachary J (eds): Pathologic Basis of Veterinary Disease. a cat and a green iguana (Anderson et al., 1996; Basaraba Mosby, St. Louis, MO:1263–1315. et al., 1998). Frisk CS, Wagner JE, Doyle RE. 1978. An ovarian teratoma in Successful surgical removal of ovarian teratomas has been a guinea pig. Lab Anim Sci, 28:199–201. described in a green iguana and domestic animals (Ander- Frye FL, Randall LS. 1999. Ovarian teratoma in a green son et al., 1996; Basaraba et al., 1998; Catone et al., 2004). iguana, Iguana iguana. Proc ARAV, 51–53. Other authors reported the intra-operative death of a Garner MM, Hernandez-Divers SM, Raymond JT. 2004. red-eared slider turtle, Trachemys scripta elegans, in which Reptile neoplasia: a retrospective study of case submissions surgical removal of a malignant ovarian teratoma was to a specialty diagnostic service. Vet Clin North Am Exot attempted (Newman et al., 2003). In the green iguana, sur- Anim Pract, 7:653–671. gical excision of the tumor was straightforward, and the Hertha DW, Giles HD, Frye FL. 2000. Ovarian teratoma in animal recovered quickly. In the Fiji Island banded iguana, a garter snake Thamnophis sirtalis. J Herpetol Med Surg, the adhesions between the teratoma and the gastrointestinal 10:22–23. tract, caused by the granulomatous inflammation, com- Hidalgo-Vila J, Martinez-Silvestre A, Diaz-Paniagua C. 2006. plicated the surgery. The Fiji Island banded iguana took Benign ovarian teratoma in a red-eared slider turtle several weeks to recover from surgery when it started (Trachemys scripta elegans). Vet Rec, 159:122–123. feeding on its own and gained weight. Newman SJ, Brown CJ, Patnaik AK. 2003. Malignant ovarian Ovarian teratomas are usually benign and composed of teratoma in a red-eared slider (Trachemys scripta elegans). well differentiated mature tissue. However, malignant forms J Vet Diagn Investig, 15:77–81. that contain immature embryonal components occur and Tocidlowski ME, Merrill CL, Loomis MR, Wright JF. 2001. have been reported in dogs and in horses (Foster, 2007). Teratoma in desert grassland whiptail lizards (Cnemido- Recurrence of an initially benign ovarian teratoma was seen phorus uniparens). J Zoo Wildl Med, 32:257–259.

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