Massive uterine lipoleiomyoma and leiomyoma in a miniature poodle bitch

Abstract

A 15-year-old, intact, female miniature poodle was presented for further evaluation of a large abdominal mass. Computed tomography was conducted to determine the origin of the mass and 2 large uterine masses were discovered. Ovariohysterectomy was performed and histopathological evaluation revealed a massive uterine lipoleiomyoma (27 × 17 × 15 cm), the largest recorded in the veterinary literature, and a smaller leiomyoma (7 × 5 × 4 cm).

Neoplasia of the canine uterus is a rare occurrence in veterinary medicine, accounting for 0.3% to 0.4% of all canine tumors (1). The most common canine uterine tumors are leiomyomas, which are benign mesenchymal tumors most frequently observed in the vaginal tract of dogs (2). Leiomyomas are characteristically noninvasive, slow-growing tumors which can be difficult to distinguish from their malignant epithelial counterparts (leiomyosarcoma) without histological evaluation (2). Lipoleiomyomas are a rare variant of leiomyomas characterized by well-differentiated neoplastic smooth muscle cells and mature adipocytes (3,4). Only 1 case of canine uterine lipoleiomyoma has been reported (5); however, there are several reports in the human literature (6–9). The histogenesis of lipoleiomyomas is controversial, as adipose tissue is not native to the myometrium (4,10). In the human medical literature, several studies have shown that lipoleiomyomas may arise from metaplasia of pluripotent mesenchymal cells or by a direct metaplasia of smooth muscle cells (4,10).

Clinical signs reported in dogs related to uterine tumors include abnormal estrus cycles, tenesmus, stranguria, and abdominal distension from large space occupying lesions (5,11,12). Given their benign nature, lipoleiomyomas and leiomyomas offer a good long-term prognosis with successful surgical excision (2).

Diagnostic imaging is an important step in determining the tissue of origin of abdominal masses and subsequent planning for treatment. However, the size and nature of large uterine masses can make interpretation of abdominal radiographs and ultrasonography challenging. Large uterine masses may be seen as poorly demarcated, soft-tissue opacities in the caudal abdomen, whereas smaller masses may not be seen at all radiographically (13). Ultrasonography has successfully determined the tissue of origin in smaller uterine masses (up to 11 cm × 7 cm in 1 report) (13). However, with increasing size of a soft-tissue mass, the ability to locate the tissue of origin can become more difficult with radiography and ultrasound (6,13). Cross-sectional imaging such as computed tomography (CT) provides additional imaging options for diagnosis of uterine tumors. These modalities can provide further detail into the tissue of origin and assist in clinical decision-making.

This report details a case of a 15-year-old poodle with a massive uterine lipoleiomyoma and leiomyoma. To the authors’ knowledge, this report describes the largest lipoleiomyoma reported in the veterinary literature.

Case description

A 15-year-old, 8.3-kg, intact, miniature poodle bitch was presented to the referring veterinarian for complaints of a distended abdomen of 4 days’ duration and loss of the ability to jump. The dog had its last estrus cycle 2 mo earlier and became pseudopregnant. Physical examination revealed a markedly distended abdomen and abdominal palpation discovered a large mass occupying the entire abdomen. The remainder of the physical examination was unremarkable. Abdominal radiographs and ultrasonography as well as a complete blood (cell) count (CBC) and serum biochemical profile were performed. Blood analysis revealed a mildly elevated blood urea nitrogen [BUN; 13.8 mmol/L, reference range (RR): 2.1 to 11.1 mmol/L] and a mild leukocytosis (16 × 10⁹/L, RR: 4 to 15.5 × 10⁹/L) with mild neutrophilia (13.3 × 10⁹/L, RR: 2.06 to 10.6 × 10⁹/L). No other blood abnormalities were observed. Abdominal radiographs revealed a large, soft-tissue opacity mass (~26 × 12 cm) in the abdomen extending from the liver to the pubis, and displacing the bowel dorsally (Figure 1). Prominent teats were also noted. Cursory abdominal ultrasound examination revealed a large fluid-filled mass, the origin of which could not be ascertained.

Figure 1.

Left lateral (A) and ventral dorsal (B) abdominal radiographs of a 15-year-old intact female poodle. Note the large soft tissue opaque mass in the ventral aspect of the peritoneum extending from the liver to the pubis and displacing the intestines dorsally and to the right.

Based on the findings of a large abdominal mass from an unknown location, exploratory laparotomy was recommended by the referring veterinarian. The following day, the patient was routinely anesthetized and a ventral midline laparotomy was performed. A large, cystic mass was discovered; however, its tissue of origin could not be ascertained. The dog was hypotensive under general anesthesia, and, for this reason, the laparotomy incision was closed and the patient was recovered without attempting removal. The dog recovered uneventfully from anesthesia and was referred to the Ontario Veterinary College Health Sciences Centre (OVCHSC).

Upon presentation to the OVCHSC the dog was bright, alert, and responsive, weighing 8.3 kg, with all vital parameters within normal limits. Cardiothoracic auscultation revealed a grade 1–2/6 left systolic heart murmur; no other abnormalities were observed. Abdominal palpation revealed a large mass in the entirety of the abdomen. All palpable lymph nodes were soft and symmetric. A 6-cm ventral midline incision was present from the prior exploratory laparotomy. The remainder of the physical examination was unremarkable.

In order to further characterize the large abdominal mass and plan for surgery, CT of the abdomen was performed. The following day the dog was routinely anesthetized and an abdominal CT revealed a large, fluid-filled (10 Hounsfield units, HU) mass with soft tissue septations, occupying approximately 60% of the abdomen and extending from the liver to the pubis along the ventral abdomen (Figure 2). A small soft tissue dense mass (35 HU) was present in the left lateral abdomen that exhibited contrast enhancement (64 HU), and arose from the cranial extremity of the right uterine horn (Figure 2). A large blood vessel extended from this smaller soft tissue mass into the center of the larger fluid dense mass. The dog had stable cardiorespiratory function under anesthesia and surgical removal of the mass via ovariohysterectomy was recommended and carried out with the owner’s consent.

Figure 2.

Abdominal computed tomography (CT) images following intravenous administration of contrast medium. A — Reformatted sagittal plane image of the mid-abdomen, demonstrating the extent of the large cystic mass (#). B — Reformatted sagittal plane image of the left side of the abdomen depicting the smaller solid mass (*). C, D — Transverse plane images at the level of the smaller solid mass (*). C — A connection of the smaller mass to the right uterine horn (arrowhead) can be seen and a vessel extends into the larger cystic mass from the uterus (arrow). E — Dorsal plane reformatted image, depicting a large vessel extending from the uterus into the large cystic mass (arrow). # — lipoleiomeyoma; * — leiomyoma.

The prior ventral midline incision was enlarged and Balfour retractors were applied to improve abdominal exposure. A large, multi-lobulated cystic mass associated with the uterine body (Figure 3) was present and occupied most of the abdominal cavity. Both ovarian pedicles were sealed and divided using a vessel-sealing device (Ligasure PRECISE; Medtronic-Covidien, Mansfield, Massachusetts, USA). The uterine body was double ligated with 2 circumferential sutures (PDS; Ethicon, Edison, New Jersey, USA) and removed. The entire structure (mass and reproductive tract) weighed 2 kg. The remainder of the reproductive tract and the abdominal contents were unremarkable at the time of exploration. The reproductive tract was submitted for histopathology and the dog recovered from anesthesia.

Figure 3.

Intra-operative image of the uterine mass exteriorized through a laparotomy incision. The surgeon is elevating the right and left ovary. # — large cystic mass (lipoleiomyoma); * — small solid mass (leiomyoma).

Following surgery, the dog was allowed to recover in the intensive care unit on a fentanyl continuous rate infusion [2 to 6 μg/kg body weight (BW) per hour], IV and was discharged from hospital 1 d after surgery, weighing 6.5 kg. The dog was discharged with gabapentin (Auro Gabapentin; Aurolindo, Woodbridge, Ontario), 100 mg, PO, q8h, and received a sustained-release injection of buprenorphine (Vetergesic; Champion Alstoe Animal Health, Whitby, Onatrio), 0.2 mg, before discharge.

Histopathology

Gross examination of the submitted tissue revealed a large 27 × 17 × 15 cm soft, ovoid, tan, fluctuant mass. Upon examination of the cut section, several cavities containing serous fluids were observed. The smaller 7 × 5 × 4 cm firm, tan, ovoid mass was associated with the uterine horn 3 cm distal to the larger mass. Samples of the remaining uterine tissue and the ovaries were also taken.

Histologic examination showed that both masses were located within the myometrium. The larger mass was surrounded by 100 μm of a thick, loose, fibrous connective tissue capsule. The spindle cell sheets contained within them mature adipose tissue and regions in which spindle cells were widely separated by clear spaces or myxoid intercellular matrix accounting for up to 20% of the mass. The neoplastic cells were well-differentiated, the nuclei were oval to elongate with small, distinct nucleoli without the presence of mitotic figures and negligible anisocytosis and anisokaryosis. This mass was diagnosed as lipoleiomyoma with myxoid features due to the adipose and myxoid tissue components (Figure 4). The smaller mass had similar neoplastic features, but lacked the adipocyte and myxoid characteristics. This mass was diagnosed as a leiomyoma.

Figure 4.

A low power photomicrograph (200× magnification) of a section of the mass showing details of the neoplastic morphology. Bundles of well-differentiated smooth muscle cells are separated by sheets of mature adipose tissue or myxoid intercellular matrix (each making up approximately 20% of the mass). Hematoxylin and eosin (H&E). Scale bar = 100 μm.

Discussion

Canine uterine tumors are a rare finding, especially with the routine practice of early ovariohysterectomy (1). Lipoleiomyomas are characterized by well-differentiated neoplastic smooth muscle cells and mature adipocytes, and are considered a variant of leiomyoma which is the most common canine uterine neoplasia (3,4). Other reported canine uterine tumors include angiolipoleiomyoma, hemangiosarcoma, fibroma, fibroleiomyoma, fibromyoma, adenoma, endometrial polyp, adenocarcinoma, and plasmacytoma as well as other variants of leiomyoma (14–19). This report details a massive lipoleiomyoma (27 × 17 × 15 cm) as well as a smaller leiomyoma (7 × 5 × 4 cm), that together with the reproductive tract weighed 2 kg. The signalment of this dog is consistent with the typical presentation of a middle-aged to older intact female animal (1). However, the size of the lipoleiomyoma is considerably larger than what has been reported in previous cases (3,5,13). As in dogs, giant lipoleiomyoma in humans are uncommon with ~140 cases reported in the medical literature. Leiomyomas (also termed fibroids) are common uterine tumors with a high incidence in reproductive women (7). A benign variant, lipoleiomyomas, are histologically characterized by variable amounts of adiopocytes and smooth muscle cells. Similar to the dog in this report, in human lipoleiomyoma, the adipocytes do not have abnormal cytological characteristics and immunohistochemical staining is often performed to rule out well-differentiated liposarcoma (7). Several theories have been proposed as to the source of the adipose portion of the uterus during histogenesis. In early reports, the adipose tissue was thought to arise from degeneration of lipoleiomyoma, however, more recently, it has been considered that the adipose tissue results from direct metaplasia of the smooth muscle cells of leiomyoma, or due to abnormally located remnants of adipocytes in the embryo, or from multipotential undifferentiated mesenchymal cells (6–10). In women, uterine lipoleiomyomas are associated with vaginal bleeding, abdominal pain, and a palpable abdominal mass (6–10).

The effects of repeated exposure to steroid hormones produced during estrous cycles on the development of mammary carcinoma has been well-described in the veterinary literature (20,21). It is believed in the human and veterinary literature that steroid hormones (particularly estrogen) play a role in the formation of uterine leiomyomas (11,22–24). Miniature potbellied pigs have been shown to develop uterine leiomyomas with similar frequency, presentation, lesions, and effects of parity as in humans (25). Although miniature pigs have not been shown to develop lipoleiomyomas, they provide a promising model for the study of hormonal influence on formation of uterine tumors (25). In the human literature, it is suggested that giant lipoleiomyomas may be linked to altered lipid metabolism such as in diabetes mellitus, hypothyroidism, and menopause (7–10). The dog of this report did not have any co-morbidities or metabolic abnormalities; however, further research into the formation of leiomyomas and their transformation into lipoleiomyomas may shed light on the influence of prolonged exposure to sex hormones in the development of canine uterine tumors.

This case demonstrates the difficultly of diagnosing uterine masses through abdominal radiographs, ultrasonography, and physical examination alone. A large uterine mass may be seen radiographically as a soft-tissue opaque abdominal mass with an unknown tissue of origin (26,27). Main radiographical differential diagnoses in a geriatric dog include neoplasia originating from the liver, spleen, lymphoid tissue, gastrointestinal tract, or reproductive tract. These differential diagnoses may lead an owner to believe that their animal’s prognosis is far graver than if a uterine leiomyoma is suspected, which emphasizes the importance of obtaining a definitive diagnosis. While ultrasound may be able to further characterize the origin of the mass, a diagnosis of leiomyoma/lipoleiomyoma can only be made following histopathological evaluation as many other uterine abnormalities may have a similar appearance (6,13).

Cross-sectional imaging is the next step in identifying the origin of the mass, should ultrasonography be inconclusive. As demonstrated by this case, cross-sectional imaging was imperative in helping to determine the tissue of origin of the mass and surgical resectability. Abdominal radiographs and ultrasound were ineffective in this regard. Once CT imaging was conducted, the 2 masses were traced to the uterus and successful surgical removal was performed following routine ovariohysterectomy. With definitive diagnosis only possible through histology, large uterine lipoleiomyomas present a clinical conundrum for owners with limited financial ability to pursue advanced diagnostic imaging. Biopsy or fine-needle aspiration may assist in diagnosis of uterine tumors and in clinical decision-making, especially as the diagnosis of leiomyoma would lead to a more positive prognosis (11,28,29). Misdiagnosis of these tumors may lead to euthanasia based on differential diagnoses with a poor long-term prognosis.

In conclusion, uterine leiomyomas and lipoleiomyomas are rare benign uterine tumors typically seen in middle-aged to older dogs. This is the first report describing a bitch with a uterine leiomyoma and myxoid lipoleiomyoma, as well as the largest lipoleiomyoma reported in the veterinary literature. Practitioners should consider benign uterine neoplasia in intact bitches presenting with large abdominal masses. Computed tomography is a superior diagnostic imaging choice in dogs with large abdominal masses. CVJ