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. 2024 Jul 9;10(4):e1520. doi: 10.1002/vms3.1520

Myxoid leiomyosarcoma of the oviduct and uterus in a Cockatiel (Nymphicus hollandicus)

Diba Golchin 1,✉, Ali Borhanikiya 2,3
PMCID: PMC11231927  PMID: 38979745

Abstract

An 11‐year‐old female cinnamon cockatiel (Nymphicus hollandicus) was presented with a coelomic distention. Dystocia was suspected, given its previous history of a calcium‐deficient diet and multiple instances of nonobstructive dystocia. Exploratory coeliotomy revealed a large intraluminal mass extending through the magnum to the uterus (shell gland). Metastasis and multiorgan involvement were not seen. Histopathologically, malignant and invasive fascicles of spindle cells were associated with abundant myxoid matrix and hypocellular areas. Multinucleation, bizarre cells and atypical mitotic figures were prominent. Masson's trichrome staining verified the muscular origin, and the myxoid matrix was demonstrated utilizing Alcian blue. The neoplastic cells exhibited alpha‐smooth muscle actin and desmin immunoreactivity and were negative for vimentin. Thus, the patient was diagnosed with oviductal and uterine myxoid leiomyosarcoma (LMS). The patient survived 34 days post‐surgery before death associated with suspected enteritis. Myxoid LMS is an extremely rare neoplasm in animals. To our knowledge, myxoid LMS has not been reported previously in pet birds.

Keywords: cockatiel, histopathology, immunohistochemistry, myxoid leiomyosarcoma, uterus

An 11‐year‐old female Cinnamon Cockatiel (Nymphicus hollandicus) was presented with an abdominal bulge. Exploratory celiotomy revealed a large intraluminal mass extending through the magnum to the uterus. Histopathological features of the mass, coupled with Masson's trichrome and Alcian blue special staining, and immunohistochemistry for α‐SMA, desmin, vimentin and Ki67, lead to the diagnosis of myxoid leiomyosarcoma, a neoplasm never reported previously in pet birds.

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1. INTRODUCTION

Neoplastic diseases are common in pet birds (Robat et al., 2017). Coeliotomy and surgical excision are accepted as routine treatments for intracoelomic neoplasms (Filippich, 2004). Various neoplasms have been diagnosed in pet and aviary birds affecting different organ systems (Nemeth et al., 2016; Robat et al., 2017; Sutherland et al., 2023). Leiomyosarcoma (LMS) is a malignant neoplasm of smooth muscle origin and is the most common sarcoma affecting the uterine tissue in humans (Verta et al., 2023). Myxoid LMS (mLMS) is characterized by the presence of an abundant myxoid matrix, separating the malignant smooth muscle cells and leaving hypocellular aggregates of neoplastic spindle cells. Dense hypercellular areas of neoplastic cells are also present. Uterine mLMSs rarely occur in humans. However, despite few published reports, mLMSs are known to exhibit more aggressive behaviour compared to LMSs (Cooper et al., 2006; Parra‐Herran et al., 2016). These tumours were typically large upon diagnosis (Cooper et al., 2006). Reports of mLMS are extremely limited in the veterinary literature. The entity has been diagnosed in the subcutaneous tissue of a female Sarus crane (Grus antigone) (Frazier et al., 1993), in the ventriculus of a female broiler (Gallus gallus domesticus) (Sato et al., 2002), and in the uterus of a domestic cat (Felis catus) (Cooper et al., 2006). Here, we highlight the occurrence of mLMS in the reproductive tract of a female cockatiel (Nymphicus hollandicus) and describe its histopathological and immunohistological features. We retrieved no cases of mLMS in a search of Google, PubMed, CAB Direct, Web of Science and Scopus, using search terms ‘myxoid leiomyosarcoma’, ‘pet bird’, ‘ornamental bird’ and ‘cockatiel’, suggesting that this condition has not been reported in pet birds or specifically in a cockatiel.

2. CASE REPORT

An 11‐year‐old female cockatiel was presented to Avin Pet Clinic (Tehran, Iran) for anorexia and lethargy of several‐day duration. The patient had been treated for several incidences of nonobstructive dystocia (egg‐binding secondary to normal‐sized thin‐shelled eggs). The condition was first identified by physical examination and radiography at 2 years of age. Episodes recurred every 8–14 months, occurring with the final egg of each clutch. The average clutch size was four. Previously, the condition was successfully treated by applying gentle pressure on the coelom cranial to the egg. The cockatiel's diet was mainly composed of grains and mixed seeds, with occasional parsley, lettuce, apple, dried berries and figs. The bird was reluctant to consume mineral supplements and balanced pellets; hence, physical signs of nutritional deficiencies were apparent from an early age. At this presentation, physical examination revealed coelomic distension with a palpable mass in the coelomic cavity (Figure 1). Given the signalment, chronic dietary calcium deficiency, history of nonobstructive dystocia (with the previous incident occurring 5 months prior) and the palpable coelomic mass, a recurrence of dystocia was suspected. Hepatomegaly, herniation, enteritis, splenomegaly, ascites or coelomic organ neoplasia were considered differential diagnoses. It was elected to manage the bird as an outpatient, and the following treatments were administered for supportive care: lactated Ringer's solution (2 mL SC; I.P.P.C), Duphalyte (0.2 mL SC; Zoetis Manufacturing and Research Spain), injectable calcium gluconate (70 mg/kg SC; Caltrex, Sina Darou), injectable meloxicam (0.1 mg/kg IM; Melovem, Pantex Holland) and injectable tramadol (5 mg/kg SC; Texidol, Tehran Chemie). Meloxicam (0.1 mg/kg PO q24 h × 1 day; Meloxib 7.5, Samisaz Pharmaceutical Co.) and tramadol (10 mg/kg PO q12 h × 1 day; Tramadol 100, Pharma Chemie Pharmaceutical Co.) were prescribed for the following day, and the patient was discharged. The next day, the patient re‐presented having failed to respond to treatments. Mild digital pressure was applied under inhalant isoflurane (5% for induction, 2% for maintenance; IsoFlo, Zoetis) anaesthesia. The presence of a neoplasm affecting one of the coelomic organs was suspected due to the unusually large size (larger than a normal egg) and firm consistency of the palpated mass, and the bird was scheduled for an exploratory coeliotomy. Injectable lincomycin‐spectinomycin (50 mg/kg IM; LincojectS, Rooyan Darou) was administered, and the patient was premedicated (injectable Meloxicam and injectable Tramadol). Anaesthesia was induced and maintained by a face mask using isoflurane in oxygen. Exploratory coeliotomy was performed through a ventral midline incision. Enlarged uterus and oviduct were seen displacing other visceral organs. A prominent intraluminal mass was discovered extending through the magnum to the uterus (shell gland), occupying a significant portion of the coelomic cavity. The entire reproductive tract was removed by ligating the uterus as distal as possible adjacent to the cloaca and ligation of the cranial oviduct at the level of the ovarian artery/vein using absorbable suture material (polyglycolate 3/0 USP/2 metric; Supabon, Supa). There were no visible signs of metastasis or multiorgan involvement, and the liver, intestines and other visceral organs were macroscopically normal. The excised tissues were placed in 10% neutral buffered formalin and referred to the pathology service. Electrocautery was used for hemostasis, and the midline coelomic and skin incisions were sutured by a simple continuous pattern using absorbable suture material polydioxanone 5/0 and 6/0, respectively (Surgicryl, SMI AG). Post‐operatively, meloxicam (0.1 mg/kg PO q24 h × 3 days), tramadol (10 mg/kg PO q12 h × 3 days) and lincomycin (50 mg/kg PO q12 h × 3 days; Lincopec, Razak Laboratories, Tehran, Iran) were prescribed. Recovery from surgery was uneventful, and the bird was discharged into the owner's care. On the first day post‐surgery, medicines were administered in the clinic. Re‐examination on days 4 and 8 post‐surgery showed proper healing and normal clinical presentation.

FIGURE 1.

FIGURE 1

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Anaesthesia is induced and maintained by a mask. The caudal coelomic area is bulged by an intracoelomic mass (arrow).

Grossly, the excised ovoid and intraluminal mass appeared cream, glistening, smooth to mucoid and gelatinous to soft, weighed 9 g and measured 3.4 × 2.5 × 2.4 cm3 (Figure 2A). The cut surface appeared cream to yellow, hyperemic, haemorrhagic and myxoid (Figure 2B). Following fixation, representative sections were obtained and routinely processed. Paraffin‐embedded blocks were sectioned at 5 µm thickness and stained with haematoxylin and eosin. Histopathologic examination revealed an unencapsulated neoplastic mass partially covered by ciliated simple columnar epithelium (Figure 3A). The neoplasm was composed of islands of dense whorls and bundles of malignant pleomorphic spindle cells with abundant eosinophilic cytoplasm and cigar‐shaped or oval nuclei, mimicking smooth muscle fibres. These fascicles were coupled with clusters of loosely arranged spindle cells within a slightly basophilic myxoid matrix (Figure 3B). Invasion of neoplastic cells into the uterine tunica muscularis was evident. Moderate‐to‐severe anisokaryosis, anisocytosis, bizarre cells and atypical mitotic figures (14 mitoses per 10 high‐power fields) were prominent in the neoplastic cells (Figure 3C). Occasional multinucleation was also noted (Figure 3D). Masson's trichrome staining was utilized and validated the muscular origin of both densely packed and loosely arranged neoplastic cells (Figure 4A). Alcian blue special staining (pH = 2.5) demonstrated the myxoid matrix (Figure 4B). Alpha‐smooth muscle actin (α‐SMA), desmin, vimentin and Ki67 immunostainings were performed (Table 1). The neoplastic cells displayed diffuse moderate to strong cytoplasmic immunoreactivity for α‐SMA (Figure 4C) and desmin (Figure 4D), confirming their smooth muscle origin, whereas anti‐vimentin antibodies failed to demonstrate immunoreactivity. Ki67 expression was observed in 10% of neoplastic cells. Based on these results, a diagnosis of mLMS was made. The patient was followed up for 34 days, and there was no evidence of tumour recurrence or metastasis. On day 40 post‐surgery, the cockatiel returned with weight loss and anorexia. Coelomic radiographs revealed moderate diffuse ileus and hepatosplenomegaly, as well as a generalized decreased opacity of the skeletal system, attributed to the patient's long‐standing calcium deficiency. The remainder of the radiographs was unremarkable. Cefixime in liquid suspension (30 mg/kg PO q8 h × 3 days; Maxime, Mascot Health Series Pvt. Ltd) was prescribed, but regretfully, the animal died from complications associated with suspected enteritis/ileus, and the owner declined a necropsy.

FIGURE 2.

FIGURE 2

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(a) The neoplastic mass appears cream, congested, glistening and ovoid. (b) The cut surface reveals soft and myxoid tissue affected by hyperemia and haemorrhage.

FIGURE 3.

FIGURE 3

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(a) The mass is partially covered by simple columnar ciliated epithelium of the ovarian/uterine mucosa (arrow) (haematoxylin and eosin [H&E]). (b) The neoplasm is composed of dense bundles and fascicles (asterisk) coupled with loosely arranged spindle cells within a myxoid matrix (arrowhead) (H&E). (c) The neoplastic cells exhibit remarkable pleomorphism, vesicular nuclei, eosinophilic cytoplasm and mitotic activity (arrowheads) (H&E). (d) A multinucleated tumour cell (arrow) and mitotic figures (arrowheads) are depicted in the hypocellular area (H&E).

FIGURE 4.

FIGURE 4

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(a) The neoplastic cells are diffusely stained red (Masson's trichrome). (b) The myxoid content (asterisk) is stained blue (Alcian blue). (c) The neoplastic cells exhibit diffuse cytoplasmic immunostaining with alpha‐smooth muscle actin (α‐SMA) (immunohistochemistry (IHC)). (d) The neoplastic cells exhibit diffuse cytoplasmic immunostaining with desmin (IHC).

TABLE 1.

Details of immunohistochemical stains performed on sections of suspected myxoid leiomyosarcoma in the cockatiel.

Antibody Source Antigen retrieval Dilution Secondary polymer
α‐SMA ScyTek, A00002 Heat‐induced epitope retrieval for 15 min at 120°C in citrate buffer (pH 6.0) Ready to use BioGenex, supersensitive polymer‐HRP
Desmin Zytomed, BMS007 Heat‐induced epitope retrieval for 15 min at 120°C in citrate buffer (pH 6.0) Ready to use BioGenex, supersensitive polymer‐HRP
Vimentin Zytomed, BMS012 Heat‐induced epitope retrieval for 15 min at 120°C in citrate buffer (pH 6.0) BioGenex, supersensitive polymer‐HRP
Ki67 Zytomed, BRB040 Heat‐induced epitope retrieval for 15 min at 120°C in citrate buffer (pH 6.0) Ready to use BioGenex, supersensitive polymer‐HRP
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Abbreviation: α‐SMA, Alpha‐smooth muscle actin.

3. DISCUSSION

Despite the prevalence of neoplastic diseases in pet birds, diagnosis and treatment of neoplasia are considered difficult in clinical practice, attributed to the small size of the companion birds, difficult venipuncture, increased risk of anaesthesia and limited clinical reports regarding diagnosis, care and treatment of neoplastic diseases in these patients (Robat et al., 2017). Exploratory coeliotomy and surgical removal of coelomic neoplastic masses are often essential for controlling such tumours (Filippich, 2004). In addition to surgery, radiation therapy, chemotherapy, photodynamic therapy, cryotherapy and antihormonal therapy have been described in various avian patients with mixed and contradictory results. Definitive diagnosis and assessment of surgical margins can be achieved by histopathology of biopsied or excised samples. Immunohistochemistry can also be employed for a more precise diagnosis; however, cross‐reactions may be limited in avian tissues when utilizing routine mammalian antibodies (Robat et al., 2017). Previous investigations have shown varying rates of neoplastic involvement in different organs and systems. A study of 141 solid neoplastic lesions of pet and aviary birds revealed higher incidences of neoplasms in the gastrointestinal and reproductive systems (Sutherland et al., 2023). In a pathological study of 827 tissue samples obtained from various avian species, neoplasia was diagnosed in 9.2% of birds, with the majority (79%) being diagnosed as malignancy. Lymphoma was the most commonly diagnosed neoplasm among avian tumour patients, with Psittaciformes being overrepresented that was attributed to the longevity of this order (Nemeth et al., 2016). In another study of pet birds, the skin and urogenital tract had the highest rates of neoplasia compared to other organ systems (Robat et al., 2017). The incidence of genitourinary tumours was higher in cockatiels compared to other species (Filippich, 2004).

Neoplasms originating from the oviduct are less common compared to ovarian tumours (Echols & Speer, 2022). Adenoma, adenomatous hyperplasia (Echols & Speer, 2022), adenocarcinoma (Carleton & Garner, 2002; Schmidt et al., 2015), hemangiosarcoma (Rosen, 2012), lymphoid leukosis (Greenacre, 2015), carcinomatosis (Rosen, 2012), granulosa cell tumour (Robat et al., 2017), dysgerminoma (Strunk et al., 2011), leiomyoma (Anjum et al., 1988; Tunca et al., 2014) and rarely LMS (Antinoff et al., 1997) have been reported in the reproductive tract of female birds. Conventional LMS has also been reported in the skin and subcutis (Nemeth et al., 2016; Timurkaan et al., 2016), large intestine (Cardoso & Levy, 2014), jejunum (Steinberg, 1988) and anterior limb (Bonel et al., 2019) of pet birds. However, mLMS has never been reported in pet birds and avian urogenital tract. All cases of mLMSs in veterinary literature were associated with metastases (Cooper et al., 2006; Frazier et al., 1993; Sato et al., 2002), whereas in the present case, metastasis was not grossly evident at the time of diagnosis. There are no long‐term follow‐ups in veterinary patients with mLMS, as the patients were either immediately euthanized and necropsied (Frazier et al., 1993; Sato et al., 2002), or euthanized and necropsied 1 month after the removal of the primary tumour with widespread mesenteric metastases (Cooper et al., 2006). In mLMS, the neoplastic cells are sparsely scattered within myxoid areas; therefore, low mitotic counts do not refute malignancy (Parra‐Herran et al., 2016). Thus, mitotic figures are most expected in dense and hypercellular areas, which is in‐line with the findings of the current and the aforementioned reports (Cooper et al., 2006). In addition to infiltrative tumour margins, the presence of either remarkable mitotic count (>2 per 10 high‐power fields), moderate‐to‐severe nuclear atypia, or coagulative necrosis has been proposed as criteria for the diagnosis of malignancy in this tumour. A cutoff of 50% has also been suggested for the myxoid matrix to establish a myxoid tumour (Parra‐Herran et al., 2016). In the present case, the tumour's large size and histopathologic findings were consistent with those diagnosed in human and animal cases of mLMS, except for the presence of coagulative necrosis. In a study conducted on 30 women with uterine mLMSs, patients with >10 mitoses in 10 high‐power fields died of the disease. Additionally, their ≥5 years of follow‐up revealed that the overall survival of mLMS patients was significantly worse than that of conventional LMSs (Parra‐Herran et al., 2016). The index cockatiel remained clinically disease‐free for 34 days after the surgery but unfortunately died from complications associated with suspected enteritis. This patient had undergone surgery and received no other curative interventions. Precise clinical examination, obtaining a good clinical history, and a complete imaging assessment (such as radiography and ultrasound examination) of any coelomic swelling/enlargement are recommended before exploratory coeliotomy. In the present case, the patient's gender, clinical history, shape of the bulging mass and signalment mimicked previous episodes of dystocia. Furthermore, imaging was overlooked because of the shortcomings of radiography (in identifying a soft tissue mass or a thin‐shelled egg) and ultrasound (in distinguishing the origin and nature of this large mass).

Generally, the differential diagnoses of mLMS include myxoid leiomyoma (Cooper et al., 2006), myxosarcoma (Frazier et al., 1993) and inflammatory myofibroblastic tumour (Parra‐Herran et al., 2016). Utilization of trichrome staining and α‐SMA and desmin as smooth muscle immunomarkers, along with histopathological features of the neoplasm, led to the precise diagnosis of myxoid LMS in this patient.

4. CONCLUSION

Inflammatory, infectious, traumatic and neoplastic lesions are common in pet birds, and the reproductive tract is frequently diagnosed with such diseases (Konicek et al., 2020; Nemeth et al., 2016). This is the first documentation of mLMS in a pet bird. The pleomorphism, mitotic activity and invasive manner of the neoplastic cells readily differentiated the tumour from myxoid leiomyoma. Desmin and α‐SMA immunoreactivity of the neoplastic cells confirmed the smooth muscle origin of the neoplasm. Notably, inflammatory myofibroblastic tumour was ruled out due to lack of mixed inflammatory cell infiltrates.

AUTHOR CONTRIBUTIONS

Diba Golchin: Investigation; project administration; resources; visualization; writing – original draft; writing – review and editing. Ali Borhanikiya: Investigation; resources; visualization; writing – review and editing.

CONFLICT OF INTEREST STATEMENT

The authors declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

FUNDING INFORMATION

None

PEER REVIEW

The peer review history for this article is available at https://www.webofscience.com/api/gateway/wos/peer-review/10.1002/vms3.1520.

ETHICS STATEMENT

The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to and the appropriate ethical review committee approval has been received.

ACKNOWLEDGEMENTS

The authors would like to express their sincere gratitude to ArenaPath Comparative Pathology Laboratory and Fahimeh Babaahmadi Milani for their support and assistance in histologic preparations, special staining and immunohistochemistry.

Golchin, D. , & Borhanikiya, A. (2024). Myxoid leiomyosarcoma of the oviduct and uterus in a Cockatiel (Nymphicus hollandicus). Veterinary Medicine and Science, 10, e1520. 10.1002/vms3.1520

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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