Incomplete ovariosalpingectomy and subsequent malignant granulosa cell tumor in a female green iguana (Iguana iguana)

Janice A. Cruz Cardona Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Kenneth J. Conley Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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James F. X. Wellehan Jr Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Lisa L. Farina Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Francesco C. Origgi Center for Fish and Wildlife Health, Department of Pathology, College of Veterinary Medicine, University of Bern, 3012 Bern-CH, Switzerland.

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Heather L. Wamsley Department of Physiological Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Abstract

Case Description—A 9-year-old spayed female green iguana (Iguana iguana) was evaluated because of a distended coelom and weight loss. History included a single episode of egg binding and subsequent bilateral ovariosalpingectomy.

Clinical Findings—Physical examination revealed a mass within the coelomic cavity. Ultrasonography revealed a large, irregular mass with hypoechoic regions and coelomic effusion. Clinicopathologic derangements included heterophilia, monocytosis, lymphopenia, basophilia, hypocholesterolemia, hypoproteinemia, and hypercalcemia. Results of cytologic evaluation of the mass were suggestive of malignant epithelial neoplasia, but neoplastic cells were not found in the effusion. An ovarian tumor was suspected on the basis of clinical signs, clinicopathologic findings, and results of cytologic evaluation of the mass.

Treatment and Outcome—Surgical exploration revealed a large left ovary, a normal-appearing contralateral ovary, and a mass in the fat body, all of which were removed and submitted for histologic examination. The histologic diagnosis was granulosa cell tumor with metastasis to the fat body. The patient died 11 months after evaluation, and disseminated granulosa cell tumor was confirmed at necropsy; histologic examination at that time also identified systemic mastocytosis.

Clinical Relevance—Granulosa cell tumors are uncommon in reptiles, and this was the first granulosa cell tumor described antemortem cytologically, histologically, and ultrastructurally in an iguana. Findings in this iguana underscored concerns associated with incomplete oophorectomy of iguanas; cytologic and histopathologic findings were similar to those observed in other domestic animals. Oophorectomy should be considered as an alternative to standard ovariosalpingectomy to avoid potential complications in pet reptiles, and use of microsurgical instruments and vascular clips is advised.

Abstract

Case Description—A 9-year-old spayed female green iguana (Iguana iguana) was evaluated because of a distended coelom and weight loss. History included a single episode of egg binding and subsequent bilateral ovariosalpingectomy.

Clinical Findings—Physical examination revealed a mass within the coelomic cavity. Ultrasonography revealed a large, irregular mass with hypoechoic regions and coelomic effusion. Clinicopathologic derangements included heterophilia, monocytosis, lymphopenia, basophilia, hypocholesterolemia, hypoproteinemia, and hypercalcemia. Results of cytologic evaluation of the mass were suggestive of malignant epithelial neoplasia, but neoplastic cells were not found in the effusion. An ovarian tumor was suspected on the basis of clinical signs, clinicopathologic findings, and results of cytologic evaluation of the mass.

Treatment and Outcome—Surgical exploration revealed a large left ovary, a normal-appearing contralateral ovary, and a mass in the fat body, all of which were removed and submitted for histologic examination. The histologic diagnosis was granulosa cell tumor with metastasis to the fat body. The patient died 11 months after evaluation, and disseminated granulosa cell tumor was confirmed at necropsy; histologic examination at that time also identified systemic mastocytosis.

Clinical Relevance—Granulosa cell tumors are uncommon in reptiles, and this was the first granulosa cell tumor described antemortem cytologically, histologically, and ultrastructurally in an iguana. Findings in this iguana underscored concerns associated with incomplete oophorectomy of iguanas; cytologic and histopathologic findings were similar to those observed in other domestic animals. Oophorectomy should be considered as an alternative to standard ovariosalpingectomy to avoid potential complications in pet reptiles, and use of microsurgical instruments and vascular clips is advised.

A 9-year-old spayed female green iguana (Iguana iguana) with a 3-week history of an enlarged coelom and progressive weight loss was evaluated at the University of Florida Veterinary Medical Center. Pertinent history included a single episode of egg binding and subsequent bilateral ovariosalpingectomy at least 2 years previously. No behavior abnormalities had been noted by the owners. On evaluation, the iguana had generalized muscle wasting, and a large mass was palpable in the mid coelomic region on the left side. Ultrasonographic evaluation revealed a body cavity effusion and a large, irregular mass with multiple hypoechoic regions in the mid coelomic region. The mass could not be localized to a particular organ. A CBC and serum biochemical analysis were performed, and ultrasound-guided fine-needle aspirates of the mass and the effusion were submitted for cytologic examination. The CBC revealed heterophilia (6,620 cells/μL; reference interval, 600 to 6,400 cells/μL1), lymphopenia (3,720 cells/μL; reference interval, 5,200 to 14,400 cells/μL1), monocytosis (4,760 cells/μL; reference interval, 400 to 2,300 cells/μL1), and basophilia (5,380 cells/μL; reference interval, 200 to 1,200 cells/μL1). These results were suggestive of chronic inflammation, although stress may have contributed to the lymphopenia.2,3 Serum biochemical analysis indicated moderate hypoproteinemia (3.9 g/dL; reference interval, 4.9 to 7.6 g/dL1), moderate hypocholesterolemia (105 mg/dL; reference interval, 204 to 347 mg/dL1), and mild hypernatremia (176 mEq/L; reference interval, 156 to 172 mEq/L1). The hypoproteinemia and hypocholesterolemia were suggestive of decreased food intake or a catabolic state, while the hypernatremia was consistent with mild dehydration. In addition, the iguana had moderate hypercalcemia (16.8 mg/dL; reference interval, 10.8 to 14.0 mg/dL1). Folliculogenesis was a primary consideration, although serum calcium concentrations may be much higher (values up to 40 mg/dL3 and 32.5 ± 13.2 mg/dL1 have been reported). Other considerations for hypercalcemia included excess vitamin D intake and calcium supplementation, but these were considered unlikely given the dietary history and a serum phosphorus concentration that was within the reference interval. Renal failure was considered less likely given that other markers of renal disease, such as serum phosphorus and uric acid concentrations, were within reference intervals. Moreover, renal failure in lizards is more commonly associated with mild hypocalcemia and an inverted calcium-to-phosphorus ratio.4

Cytologic evaluation of the coelomic mass by use of Wright-Giemsa stain revealed a well-stained, well-preserved, and moderately hemodilute tissue aspirate that contained a moderate amount of amorphous dark eosinophilic material. Pleomorphic cells were present in large, dense, cohesive sheets (Figure 1) and, occasionally, in loose acinar structures. These cells had marked anisocytosis, anisokaryosis, and a moderately high nuclear-to-cytoplasmic ratio. They were polygonal or oval with distinct cell borders and a small to moderate amount of cytoplasm that was pale basophilic, often containing a moderate number of small round vacuoles and infrequent eosinophilic granules. Nuclei were oval or round with finely reticular to coarse chromatin and prominent round or oval, typically single nucleoli. However, more than 1 nucleolus as well as anisonucleoliosis was occasionally seen. Mitotic figures, nuclear molding, and karyomegaly were also rarely noted. An inflammatory cell population was present in moderate numbers, including heterophils, well-granulated mast cells, and rare eosinophils. In addition, a large number of heavily vacuolated macrophages were also present, many arranged in large, loosely cohesive clumps and individually. Capillaries were rarely noted in association with neoplastic cell clusters. No infectious agents were identified. The cytologic features observed were most consistent with an epithelial tumor, particularly adenocarcinoma, given the clinical signs. Ovarian neoplasia was suspected despite the history of ovariosalpingectomy because of the ultrasonographic appearance and location of the mass and its cytologic features and high serum calcium concentrations. Other secretory epithelial cell neoplasms remained diagnostic considerations.

Figure 1—
Figure 1—

Photomicrographs of a cytologic specimen of a coelomic mass in a female green iguana (Iguana iguana) evaluated because of a distended coelom and weight loss. A—Neoplastic cells are present in variably sized cohesive sheets. B—Occasionally, acinar structures (solid arrowhead) are identified in addition to clusters of heterophils (arrow) within cell clumps. C—Cells have various criteria of malignancy, including multinucleation, anisokaryosis, anisocytosis, pleomorphism, and coarse chromatin. Large, prominent pleomorphic nucleoli are also present (arrowheads). D—Notice the population of large, heavily vacuolated epithelioid macrophages. Wright-Giemsa stain; bars = 100, 50, 20, and 100 μm for panels A, B, C, and D, respectively.

Citation: Journal of the American Veterinary Medical Association 239, 2; 10.2460/javma.239.2.237

The fluid collected from the body cavity effusion was medium yellow and had low protein content (< 2.0 g/dL) and cellularity (82 cells/μL). A 200-cell differential count revealed that heterophils predominated (70%), followed by fewer numbers of eosinophils (13%), lymphocytes (8%), heavily vacuolated macrophages (6%), and basophils (3%). No infectious agents were identified. The effusion was classified as a transudate.

The iguana was anesthetized, and an exploratory celiotomy was performed. A 13 × 11 × 7.5-cm firm, tan mass was identified in the mid coelomic region and appeared to arise from the normal location of the left ovary. The mass contained several cystic structures separated by areas of soft tissue consistent with ovarian tissue. Full exploration of the coelom revealed a grossly normal right ovary that contained several follicles. A 2-cm-diameter raised soft mass was identified in the left fat body. Additionally, yolk material was found coating coelomic viscera. No other abnormalities were noted. Bilateral oophorectomy was performed by use of 4-mm stainless steel ligature clips,a and the section of the fat body containing the mass was excised. The coelomic cavity was lavaged extensively with saline (0.9% NaCl) solution, and all excised tissues were placed in neutral-buffered 10% formalin in preparation for histologic evaluation. A multilobular, unencapsulated, and poorly demarcated mass effaced ovarian tissue and was composed of solid sheets of polygonal cells separated by fibrocollagenous trabeculae (Figure 2). Neoplastic cells occasionally palisaded around vessels, forming pseudorosettes, and had similar cytoplasmic and nuclear features to those observed cytologically with moderate numbers of bizarre mitotic figures, vacuolated cells, and marked anisocytosis. Occasional neoplastic cells containing cytoplasmic eosinophilic globular material were also seen. Areas of cystic degeneration and of necrosis were scattered in the sections and were frequently infiltrated by a low number of heterophils. Multifocal infiltration of lymphocytes, plasma cells, and mast cells was also observed within the interstitium, and there was often a thin rim of mast cells at the periphery of the neoplasm. The neoplastic cells were noted to invade vessels and the fat body. The histologic diagnosis was a malignant GCT with vascular invasion and metastasis to the fat body.

Figure 2—
Figure 2—

Photomicrographs of sections of the fat body (A) and the affected ovary (ie, GCT; B, C, and D) of the same iguana as in Figure 1. Notice that the fat body (A) has solid sheets of polygonal cells separated by fibrous trabeculae and infiltrated by rare heterophils. In the affected ovary (B, C, and D), neoplastic cells have marked anisokaryosis and anisocytosis, with bizarre mitotic figures and prominent nucleoli; few infiltrating heterophils are also observed (B). Neoplastic cells containing cytoplasmic eosinophilic globular material were occasionally observed (C). Mast cells are occasionally associated with the neoplasm (D). Inset—Mast cell granules exhibit metachromasia (Giemsa stain). M = Mast cell population. N = Neoplastic tissue. H&E stain; bars = 200, 100, 100, and 200 μm for panels A, B, C, and D, respectively.

Citation: Journal of the American Veterinary Medical Association 239, 2; 10.2460/javma.239.2.237

The patient recovered without complications and was discharged 2 days following surgery. Ultrasonography performed 4 months following surgery revealed multiple irregular hypoechoic nodules on serosal surfaces throughout the coelomic cavity. At this time, therapeutic coelomocentesis was performed, and chemotherapy, antimicrobials, antiemetics, appetite stimulants, and fluid therapy were administered. Chemotherapy consisted of intracoelomic administration of carboplatin (10 mg/kg [4.5 mg/lb]) every 3 weeks. Although initial reduction in mass size was noted, the coelomic nodules slowly grew in size over time despite treatment. The patient died 11 months after initial evaluation and was in poor body condition at necropsy. Within the coelomic cavity, there was approximately 175 mL of brown, slightly opaque fluid that contained tan, flocculent debris. There was a large, soft, friable mass within the cranioventral portion of the coelom, and the kidneys and the caudal coelomic fat bodies contained multiple raised, friable nodules.

Histologically, the cranial coelomic mass was composed of 3 cell populations. The predominant cell type was similar to the neoplastic cells identified in the original biopsy specimen. The second cell population was composed of large, well-differentiated mast cells that contained numerous metachromatic cytoplasmic granules as detected via Giemsa staining; these cells formed nodules and occasionally encircled neoplastic tissue (Figure 2). Finally, cords of atrophic adipocytes characterized by multiple small clear cytoplasmic vacuoles made up the final population of cells. Necrosis, which mainly affected the neoplastic population, composed approximately 15% to 25% of the sections examined. Similar neoplastic cells and associated mast cells were present in the coelomic fat bodies, kidneys, liver, duodenal serosa, and visceral coelomic membrane overlying the lungs. Mast cell infiltrates not associated with neoplastic tissue were present in the gastric serosa, adrenal glands, hepatic and renal parenchyma, tunica adventitia of the great vessels, pancreas, bone marrow, uveal tract, and choroid plexus and were found diffusely replacing the normal splenic architecture.

Ultrastructurally, granulosa cells from the non-neoplastic ovary contained a variable amount of cytoplasmic lipid and euchromatic nuclei with prominent nucleoli (Figure 3). Neoplastic cells from the initial submission had a high nuclear-to-cytoplasmic ratio and an irregular to indented nucleus with mainly heterochromatic and prominent nucleoli. They also contained cytoplasmic lipid and phospholipid vacuoles, and there were rare intercellular desmosomes. Electron microscopic examination of splenic tissue revealed numerous mast cells and rare leukocytes of other lineages. The mast cells had an irregular, heterochromatic nucleus and numerous, variably condensed granules.

Figure 3—
Figure 3—

Transmission electron photomicrographs of sections of the grossly normal ovary (A), affected ovary (ie, GCT; B), and spleen of the same iguana as in Figure 1. In the grossly normal ovary (A), granulosa cells contain variable amounts of cytoplasmic lipid (arrows). Euchromatic nuclei with prominent nucleoli are present. Notice the zona pellucida on the left of the image (arrowheads) and the granulosa cell layer basement membrane in the upper right corner (star). In the GCT (B), notice that cytoplasmic lipid is present in most neoplastic cells (arrows). In the spleen (C), mast cells are present; notice the irregular heterochromatic nuclei and numerous, variably dense cytoplasmic granules. Bars = 20, 6, and 1 μm for panels A, B, and C, respectively.

Citation: Journal of the American Veterinary Medical Association 239, 2; 10.2460/javma.239.2.237

Discussion

Neutering of pet reptiles is commonly performed for treatment and prophylaxis of dystocia.5 Dystocia is a common and potentially fatal problem in female reptiles, with reported incidences of up to 10% annually in some collections.5 Unlike the ovaries of cats and dogs, iguana ovarian tissue is diffuse and intimately associated with the vena cava and adrenal gland. This makes oophorectomy in iguanas technically challenging. If the procedure is incomplete, even small remnants will regrow and folliculogenesis will develop. Furthermore, if the oviduct has been removed, normal oviposition is no longer possible, which may cause considerable problems. Authors (HLW and JFXW) of the present report have previously evaluated another green iguana with incomplete ovariosalpingectomy for septic yolk peritonitis.b In the iguana of the present report, the ovarian tumor and the normal-appearing contralateral ovary represent regrowth of ovarian tissue following incomplete surgical excision and the development of subsequent neoplasia. Use of hemostatic clips and microsurgical instruments has been recommended, and this may aid in complete ovarian removal.5 Because of the risk of ovarian regrowth, it may be advisable to only remove the ovaries and leave the oviducts unless they are diseased. For surgical treatment of dystocia, one of the authors (JFXW) recommends bilateral ovariectomy and removal of eggs, if present, by salpingotomy.

In domestic mammals, primary ovarian tumors are typically classified into 3 broad categories on the basis of the embryological cell of origin of the predominating neoplastic cell: epithelial tumors (adenocarcinoma and adenoma), germ cell tumors (dysgerminomas and teratomas), and sex cord tumors (GCT, thecoma, granulosa-theca cell, and luteoma).6 The last category is usually associated with excessive sex hormone production and related clinical signs, such as irregular estrus, aggression, masculine behavior, nymphomania, and infertility.7,8 Granulosa cell tumors compose 5% of all ovarian neoplasia in women,9 85% of reproductive tract tumors in mares (2.5% of all tumors in horses),8 and 0.5% to 1.2% of all tumors in dogs.10,11 In horses, these tumors usually develop in middle-aged mares and are usually unilateral and benign. However, cases of bilateral GCTs,12 metastasis,13 and development in young animals14 have also been documented. Reptilian ovarian tumors are uncommonly reported in the literature.15–29,c To date, GCTs have been identified in some snake species and rarely in lizards; these have been benign.15–17,26 Specifically in green iguanas, previously reported ovarian tumors include 5 teratomas, a dysgerminoma, an adenocarcinoma, and a papillary cystadenocarcinoma.18–21 The present report is the first of a malignant GCT in a green iguana and of a metastatic GCT in a reptile.

The cytologic features of GCTs in dogs have been described.30 Fine-needle aspirates of GCTs in dogs have a high number of moderately pleomorphic cells that are arranged in sheets and loose acinar structures, have a polygonal shape, and contain variable cytoplasmic vacuolation. Call-Exner bodies, which are composed of a round, eosinophilic center of proteinaceous material rimmed by an acinar-like aggregate of tumor cells, are also occasionally seen along with capillaries that appear as linear structures containing erythrocytes lined by endothelial cells with elongated nuclei. Histologically, the neoplastic cells of GCTs may be arranged in follicles, trabeculae, cords, solid sheets, and nests. Vacuolated cells with abundant eosinophilic cytoplasm can be observed in areas of luteinization. Although they are not observed in every case, Call-Exner bodies are a histologic hallmark of GCTs.6 Although these were not documented, all other cytologic and histologic features were identified in the GCT from this iguana.

The influx of mast cells associated with the neoplastic tissue and the systemic mastocytosis in this patient are findings not previously reported with reptilian neoplastic disease. Increased tissue mast cells have been observed in lizards (Podarcis sicula) administered estradiol via IP injection.31 In reptiles, tissue mast cell numbers have been shown to fluctuate on the basis of hormonal, seasonal, and thermal variations.31 Because normal granulosa cells in mammals, birds, and reptiles are known to be hormonogenic, as are mammalian GCTs, it is possible that in reptiles, a functional GCT may cause hyperestrogenism, stimulating systemic mastocytosis. In the iguana of the present report, the systemic mastocytosis may also represent an inflammatory response or development of additional concurrent neoplasia. An attempt to document hyperestrogenism was unsuccessful; measurement of other sex hormones and genetic analysis of the tumor and mast cells were not performed.

To the authors' knowledge, this is the first GCT described antemortem cytologically, histologically, and ultrastructurally in reptiles. Signs that may be associated with this neoplasm include presence of a coelomic mass, ascites, catabolic state, and hypercalcemia. Cytologic evaluation of fine-needle aspirates can be a valuable tool in diagnosis when used in concert with data from physical examination, ultrasonography, CBC, and serum biochemical analysis. Findings in the iguana of the present report underscore the possible serious consequences of incomplete ovariosalpingectomy. Variations in neutering procedures, such as oophorectomy without oviduct removal and the use of ligature clips and microsurgical instruments, should be considered to avoid potential complications in neutered pet reptiles.

ABBREVIATION

GCT

Granulosa cell tumor

a.

Hemoclips, Pilling Weck Inc, Research Triangle Park, NC.

b.

Wamsley HL, Bischoff K, Wellehan JFX. Egg yolk peritonitis in an ovariosalpingectomized green iguana (abstr), in Proceedings. 39th Am Coll Vet Pathol Am Soc Vet Pathol Joint Annu Meet 2004;13.

c.

Registry of Tumors in Lower Animals (RTLA), Experimental Pathology Laboratories, Sterling, Va.

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  • Figure 1—

    Photomicrographs of a cytologic specimen of a coelomic mass in a female green iguana (Iguana iguana) evaluated because of a distended coelom and weight loss. A—Neoplastic cells are present in variably sized cohesive sheets. B—Occasionally, acinar structures (solid arrowhead) are identified in addition to clusters of heterophils (arrow) within cell clumps. C—Cells have various criteria of malignancy, including multinucleation, anisokaryosis, anisocytosis, pleomorphism, and coarse chromatin. Large, prominent pleomorphic nucleoli are also present (arrowheads). D—Notice the population of large, heavily vacuolated epithelioid macrophages. Wright-Giemsa stain; bars = 100, 50, 20, and 100 μm for panels A, B, C, and D, respectively.

  • Figure 2—

    Photomicrographs of sections of the fat body (A) and the affected ovary (ie, GCT; B, C, and D) of the same iguana as in Figure 1. Notice that the fat body (A) has solid sheets of polygonal cells separated by fibrous trabeculae and infiltrated by rare heterophils. In the affected ovary (B, C, and D), neoplastic cells have marked anisokaryosis and anisocytosis, with bizarre mitotic figures and prominent nucleoli; few infiltrating heterophils are also observed (B). Neoplastic cells containing cytoplasmic eosinophilic globular material were occasionally observed (C). Mast cells are occasionally associated with the neoplasm (D). Inset—Mast cell granules exhibit metachromasia (Giemsa stain). M = Mast cell population. N = Neoplastic tissue. H&E stain; bars = 200, 100, 100, and 200 μm for panels A, B, C, and D, respectively.

  • Figure 3—

    Transmission electron photomicrographs of sections of the grossly normal ovary (A), affected ovary (ie, GCT; B), and spleen of the same iguana as in Figure 1. In the grossly normal ovary (A), granulosa cells contain variable amounts of cytoplasmic lipid (arrows). Euchromatic nuclei with prominent nucleoli are present. Notice the zona pellucida on the left of the image (arrowheads) and the granulosa cell layer basement membrane in the upper right corner (star). In the GCT (B), notice that cytoplasmic lipid is present in most neoplastic cells (arrows). In the spleen (C), mast cells are present; notice the irregular heterochromatic nuclei and numerous, variably dense cytoplasmic granules. Bars = 20, 6, and 1 μm for panels A, B, and C, respectively.

  • 1.

    Harr KE, Alleman AR, Dennis PM, et al. Morphologic and cytochemical characteristics of blood cells and hematologic and plasma biochemical reference ranges in green iguanas. J Am Vet Med Assoc 2001; 218: 915921.

    • Crossref
    • Search Google Scholar
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