Journal of Veterinary Diagnostic Investigation Vol. 18 Issue 6, 605-607
Copyright © 2006 by the American Association of Veterinary Laboratory Diagnosticians
Hyperandrogenism from an ovarian interstitial-cell tumor in an alpaca
Rosanne Gilbert,
Michelle Kutzler1,
Beth A. Valentine and
Stacy Semevolos
Correspondence: 1Corresponding Author: Dr. Michelle Kutzler, 105 Magruder Hall, Oregon State University, Corvallis, OR 97331
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Abstract
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An 8-year-old intact female Huacaya alpaca (Lama pacos) was presented for recent development of male behavior. Serum testosterone concentration was determined to be 969.1 pg/ml by using radioimmunoassay, while the range in 33 healthy female adult intact alpacas was 11.7–62.1 pg/ml. An ovarian mass was suspected, and an exploratory laparotomy was performed. A tan mass was present on the left ovary. Histologically, the mass was composed of closely packed, plump, polygonal cells with central round nuclei with granular chromatin and abundant eosinophilic finely granular to vesiculate cytoplasm. An ovarian benign interstitial (Leydig) cell tumor was diagnosed.
Key Words: Alpaca • hyperandrogenism • ovary • testosterone • tumor
An 8-year-old intact female Huacaya alpaca (Lama pacos) was presented to the veterinary teaching hospital at Oregon State University with long-standing infertility and recent development of male behavior. From 2 to 5 years of age, the alpaca had been bred on several occasions to proven males, but pregnancy never resulted. Results of serum progesterone analysisa during this time suggested ovulation occurred after breeding (progesterone concentration >1.0 ng/ml). Six months before presentation, the owner observed changes in behavior, including mounting other females and aggression toward males. Physical examination was unremarkable except for a slightly enlarged clitoris. Transrectal ultrasound examination revealed a uterine shadow; however, the ovaries were not visualized. Vaginoscopic examination was performed by using a video endoscopeb and showed multiple vaginal adhesions, and the cervical canal was impenetrable. Results of a complete blood count and a serum chemistry panel were within normal limits. Serum progesterone and testosterone concentrations were determined to be 0.3 ng/ml and 969.1 pg/ml, respectively.c The progesterone concentration was consistent with the nonluteal phase (<0.5 ng/ml).1 However, the testosterone concentration was several-fold greater than the female equine reference range (113–133 pg/ml).9 Reference ranges for testosterone have not been reported for female alpacas. To establish a reference range for testosterone in female alpacas, serum samples were collected from 33 healthy adult intact animals. By using radioimmunoassay,c testosterone concentration in healthy females ranged from 11.7 to 62.1 pg/ml (mean ±SD: 27.4 ± 1.8 pg/ml).
Based on the male-like behavior and the markedly increased serum testosterone concentration, a secretory ovarian or adrenal tumor was suspected. With the alpaca under general anesthesia, it was placed in dorsal recumbency, and a ventral midline incision was made. Exploratory laparotomy revealed follicular development in both ovaries (Fig. 1). The right ovary (2 x 2 x 2 cm3) and the left ovary (2 x 1 x 1 cm3) were within the expected range for size. A tan mass that resembled a corpus luteum was present at 1 pole of the left ovary. Both ovaries appeared grossly unremarkable, so an adrenal cortical tumor was suspected and the animal was euthanized because of the poor prognosis for reproductive soundness.
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Figure 1 Exteriorized reproductive tract during abdominal surgery appears to have 2 ovaries with follicles. A tan mass, consistent with the appearance of a corpus luteum, was present on the caudal pole of the left ovary.
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Postmortem examination indicated there was a round mass in the left ovary 1.5 cm in diameter; it was discrete, soft, and dark tan (Fig. 2). There were no significant findings in the adrenal glands or other organs examined. Samples of ovary and adrenal gland were fixed in 10% buffered formalin, processed routinely, and stained with hematoxylin and eosin (HE). The mass in the left ovary was highly vascular and demarcated by a fibrous capsule (Fig. 3). The mass was composed of sheets of closely packed, plump, polygonal cells with central round nuclei that contained granular chromatin and abundant eosinophilic finely granular to vesiculate cytoplasm (Fig. 4). Mitotic figures were not seen. Based on the gross and histologic appearance, an ovarian benign interstitial (Leydig) cell tumor was diagnosed.
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Figure 2 At necropsy, the sectioned left ovary had a 1.5-cm diameter, round, discrete, soft, dark tan mass.
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Figure 3 Photomicrograph of the left ovary with a discrete tumor (T) separated from ovarian tissue by a fibrous capsule (C). A developing follicle (F) is present in the ovarian tissue. HE stain. Bar = 200 µm.
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Figure 4 Photomicrograph of the tumor indicated it was composed of plump polygonal cells, with central heterochromatic nuclei and abundant eosinophilic finely granular to vesiculate cytoplasm. HE stain. Bar = 20 µm.
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Hormonally active gonadal tumors (sex-cord stromal tumors) are classified according to differentiation of cellular elements; they include granulosa-cell tumor, luteoma, thecoma, interstitial-cell tumor, and mixed sex-cord stromal tumors.4 Ovarian neoplasia is uncommon in camelids, comprising approximately 2.6% of ovarian lesions in alpacas.10 Teratoma is the most common ovarian tumor in alpacas, followed by granulosa cell tumor.10 Females with sex-cord stromal tumors may exhibit abnormal behavior or masculinization.4 Interstitial-cell tumors are relatively more common in males in the testes. Ovarian interstitial-cell tumors are rare in all species.1,8,9,11 An interstitial-cell tumor of the ovary resembles a corpus luteum both grossly and histologically.4 In women, ovarian interstitial-cell tumors may cause masculinization, clitoromegaly, androgenic alopecia, and increased serum testosterone concentration.6,7,8,11 Interstitial-cell tumors in mares are associated with hyperandrogenism and stallion-like behavior.8 Congenital interstitial-cell masses within the ovary of foals are considered to be hamartomas rather than neoplasms.2 Ovarian interstitial-cell tumors have also been reported in cattle,5 dogs,5 and cats,3 but no details of clinical signs or endocrinologic findings were provided. To the authors' knowledge, an ovarian interstitial-cell tumor has not been previously reported in a camelid.
The history of infertility in this alpaca was considered to be likely related to vaginal and cervical scarring, as progesterone analyses after breeding indicated ovulation had occurred. Male-like behavior did not develop until 6 months before presentation. Hyperandrogenism was attributed to the presence of a hormonally active ovarian interstitial-cell tumor. Serum testosterone concentration in this alpaca was confirmed to be several times higher than the range of values determined from 33 adult female alpacas. Results of this study provide a reference range for serum testosterone in adult female alpacas (11.7–62.1 pg/ml) and indicate that a diagnosis of ovarian interstitial-cell tumor should be considered in female camelids with male-like behavior.
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Acknowledgments
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The authors thank Jermey Becker for photography and technical assistance and Fern Hill Alpacas for her support.
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Sources and manufacturers
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From the Departments of Clinical Sciences (Gilbert, Kutzler, Semevolos) and Biomedical Sciences and Veterinary Diagnostic Laboratory (Valentine), Oregon State University, Corvallis, OR 97331. 
a. M & M Veterinary Laboratory, Milan, MI.
b. Pentax EG 2930, PENTAX Medical Company, A Division of PENTAX of America, Inc., Montvale, NJ.
c. University of California Endocrinology Laboratory, Davis, CA.
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References
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