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Multiple Infiltrative Intraosseous Lipomas in the Appendicular Skeleton of a Rose-breasted Cockatoo (Eolophus roseicapilla) with a Humeral Fracture.

Abstract: A 9-year-old female rose-breasted cockatoo (Eolophus roseicapilla) was presented for a humeral fracture. At presentation, the bird was severely lethargic and obese. On physical examination, an open right humeral fracture, healed left ulnar fracture, and intertarsal joint swelling were present. Results of hematologic testing and biochemical analysis revealed severe leukocytosis with heterophilia and increased creatine kinase and aspartate aminotransferase activities consistent with musculoskeletal lesions. Radiographs confirmed a right humeral fracture and showed severe polyostotic lytic and expansile lesions of the appendicular skeleton, as well as an enlarged hepatic silhouette. Surgical repair of the fracture was attempted, but the bird died during the procedure. Postmortem examination revealed severe bone deformities involving the fractured humerus, both ulnas, and the left tibiotarsus. Histologic findings were consistent with multiple intraosseous lipomas of the long bones and severe hepatic lipidosis. To our knowledge, this is the first report of multiple intraosseous lipomas in a bird.

Key words: neoplasia, lipoma, intraosseous, bone, fracture, avian, rose-breasted cockatoo, Eolophus roseicapilla

Clinical Report

A 9-year-old female rose-breasted cockatoo (Eolophus roseicapilla) was referred to the Centre Hospitalier Veterinaire Fregis because of an open humeral fracture noticed an hour before presentation after the bird apparently fell off its perch. It was fed a ration composed of pellets (Medium Daily Select, Pretty Bird, Stacy, MN, USA), hazelnuts, vegetables, and fruits. The bird had been adopted 2 years previously, and its medical history included a subcutaneous lipoma and a left ulnar fracture diagnosed 1 and 2 years before presentation, respectively. Persistent lameness of the left leg was also reported. On presentation, the bird was severely depressed and markedly obese, with a body condition score of 6/7 and a body weight of 430 grams. (1) A right humeral open fracture associated with soft tissue swelling was palpated. The left wing was dropped, and swelling of the left intertarsal joint was noticed. Abundant subcutaneous adipose tissue was observed ventral to the coelomic cavity. The remainder of the clinical examination was unremarkable.

Whole-body survey radiographs were obtained with the cockatoo under general anesthesia with 3% isoflurane. Severe soft tissue swelling was noticed surrounding the tibiotarsal and tarsophalangeal joints and appeared more marked on the left side. Severe bone lesions were observed in all bones of the wings and tibiotarsi. Lesions comprised a moth-eaten pattern of lysis affecting mainly the medullary cavities; expansion and irregular contour of the cortex of the diaphysis and the metaphysis of the left radius and ulna, as well as, to a minor degree, the distal right ulna; irregular thinning with multifocal areas of subperiosteal scalloping and lysis of the cortex of both radiuses, ulnas, and tibiotarsi, as well as digits; irregular and poorly mineralized periosteal reaction on the medial aspect of the distal metaphysis and distal diaphysis of the left tibiotarsus; medullary sclerosis, geographic lysis, and multifocal subperiosteal scalloping without cortical expansion of both humeri; and an oblique, simple, and proximomedially displaced right humeral fracture (Fig 1). The main findings were summarized as severe, polyostotic long bone lesions with a lytic, expansile, and sclerotic component affecting the wings and, to a minor degree, the legs. These findings suggested bone tumor or infection.

A blood sample was collected from the jugular vein for a complete blood count and a plasma biochemical analysis. Results showed a marked leukocytosis (white blood cells, 69 000 cells/[micro]L; reference interval, 5000-13 000 cells/[micro]L) and heterophilia (60 000 cells/[micro]L; reference interval, 22509360 cells/[micro]L) with no sign of toxicosis, a normal lymphocyte count, and monocytosis (3450 cells/ [micro]L; reference interval, 0-260 cells/[micro]L)." Results of the plasma biochemical analysis revealed moderate increased activity of creatine kinase (15 532 U/L; reference interval, 147-418 U/L) and aspartate aminotransferase (645 U/L; reference interval, 140-360 U/L), as well as mild hypercholesterolemia (2.39 g/L; reference interval, 0.96-2.12 g/L). (2) Biochemical and hematologic results were consistent with severe inflammation and muscular trauma associated with the fracture. Triglycerides and bile acid concentrations were within reference intervals.

The bird was hospitalized and stabilized over a 12-hour period. A 26-gauge intravenous catheter was placed into the left ulnar vein and secured with sutures. Feathers on the dorsal aspect of the right scapula and the right wing, with the exception of the secondary flight feathers, were plucked, and the open wound was cleaned with chlorhexidine digluconate. A figure-of-eight bandage was applied with a cohesive bandage associated with a body wrap. The bird was hospitalized in an incubator supplemented with oxygen, and colloid fluid therapy (1 mL IV bolus, q12h; Voluven HEA 130/0.4, Fresenius Kabi, Louviers, France) was initiated as a therapy for shock. Marbofloxacin (10 mg/kg IM q12h) was initiated empirically. Because the fracture was very unstable and a potential source of pain, analgesia was provided with meloxicam (1 mg/kg IM q12h for 2 days) and butorphanol (1 mg/kg IM) at admission. Butorphanol was then replaced

by tramadol (30 mg/kg PO q8h) to reduce stress and pain associated with frequent intramuscular administration of butorphanol. A fine-needle aspiration of the bone marrow in the left ulna and right tibiotarsus was performed, but results were nondiagnostic because of the very low cellularity of the sample. After a 12-hour period of initial stabilization, the demeanor of the bird improved.

Several treatment options were presented to the owners, including wing amputation, which was denied. A surgical reduction of the fracture was attempted to alleviate pain, knowing that the fracture could be pathologic. The bird was premedicated with butorphanol (1 mg/kg IM) and meloxicam (1 mg/kg IM), and anesthesia was induced with 3% isoflurane delivered via facemask. The bird was intubated with a 2.5-mm uncuffed endotracheal silicone tube and maintained under anesthesia with 1.8%-2.5% isoflurane during the procedure. The bird was monitored during anesthesia with capnography, cloacal temperature probe, and electrocardiography. Thermal support and crystalloid fluid therapy (10 mL/kg per hour IV) was provided throughout the procedure. Intermittent positive pressure ventilation was provided to support respiration. During the surgical procedure, a bone biopsy was harvested because the medullary cavity appeared abnormally rich in adipose tissue. Unfortunately, the bird went into cardiorespiratory arrest at the end of the procedure, and resuscitation was unsuccessful. The cause of death was not clearly identified, but the severe obesity possibly predisposed the bird to hypoventilation and potential ischemic heart disease.

At necropsy, a large amount of subcutaneous fat was apparent, and abundant yellow adipose tissue was present in the coelomic cavity. The liver was enlarged with rounded edges and diffusely discolored yellow brown (Fig 2). The kidneys were pale red-brown. The duodenum was mildly distended with a brown pasty content. The lungs were mildly congested and edematous. Most long bones were severely deformed, including the fractured humerus, both ulnas, and the left tibiotarsus (Fig 3). The left tibiotarsal and right humeral medullary cavities were opened, which showed yellow, fatty tissue. All other organs, including the thyroid and parathyroid glands, heart, crop, proventriculus, and ventriculus, appeared grossly unremarkable.

Tissue samples were collected from major organs, as well as the fractured humerus, both ulnas, and the left intertarsal joint, and fixed in 10% neutral buffered formalin for 24 hours. Bone samples were then incubated with 8% hydrochloric acid. Once soft enough for sectioning, bone samples were washed in tap water for 24 hours, then sectioned transversally with a microtome blade. Tissue samples were processed routinely for histopathologic examination.

Histologically, the diaphysis and metaphysis of all the examined bones were severely infiltrated by a nonencapsulated population of well-differentiated adipocytes replacing the medullary trabeculae, compressing and multifocally disrupting the cortex and deeply extending through the adjacent muscular and subcutaneous tissues (Figs 4 and 5). Adipocytes were supported by very thin collagenous bands of stroma. Anisocytosis, anisokaryosis, and mitotic figures were absent. Focally extensive osseous necrosis, fibrin deposition, and acute hemorrhages were observed in the right humerus, consistent with an acute focal osseous fracture. Histologic examination of the liver revealed diffuse hepatic lipidosis. The heart, proventriculus, ventriculus, jejunum, and pancreas showed no significant histologic anomalies.


This report describes the first documented case of multiple intraosseous lipomas in a bird. (3-5) The neoplastic process was associated with previous and recent bone fractures, and diagnostic imaging revealed unusual aggressive polyostotic radiographic lesions. In this case, multiple intraosseous infiltrative lipomas and benign subcutaneous encapsulated lipomas were diagnosed.

Lipocytic tumors are neoplastic processes originating from lipocytes. They are classified by their location, benign or malignant behavior, and encapsulated or infiltrative nature. (6) Infiltrative lipomas are benign and locally aggressive lipocytic tumors invading adjacent tissues, such as muscle, fascia, nerve, joint capsule, and bone. They are composed of well-differentiated lipocytes and therefore cannot be distinguished from simple lipomas by cytologic or small biopsy samples. (7) Infiltrative lipomas have been reported in avian medicine, invading the body wall musculature in a conure (Aratinga acuticaudata) and the lumbosacral vertebrae in a Canada goose (Branta canadensis). (8,9) However, in these reports, the infiltrative lipomas were isolated and not multifocal. Intraosseous lipomas are rare tumors constituting up to 0.1% of bone neoplasia in human medicine. They have been reported in 2 dogs, with invasion of the radius in one case and cervical bones in the other case. (10-12) In people, they usually appear between the fourth and fifth decade of life and affect the lower extremities in up to 71% of the cases. (13)

Infiltrative intraosseous lipomas in birds should be distinguished from other lytic bone tumors, including giant cell tumors, (14) air sac cystadenocarcinoma, (15) soft tissue sarcoma, (16) osteoma aneurysmal bone cyst, (18) traumatic bone cyst, (4) and ossifying fibromas, (19) as well as infectious conditions including mycobacteriosis or salmonellosis (20) and metabolic conditions such as nutritional hyperparathyroidism. (20) Several pathogeneses have been suspected in people, including posttraumatic bone reaction, healing of bone infarct, and a true benign tumor. (21) The absence of malignancy combined with multifocal localization suggests multiple traumas or a systemic disorder, such as a metabolic disorder or a choristomatous lesion secondary to abnormal tissue migration during development. (3,22)

Benign subcutaneous lipomas were also diagnosed in this parrot. Lipomas represent the most commonly diagnosed neoplasia in people (23) and the second most frequent neoplasia in dogs. (6) A study reveals lipomas are also the most frequently diagnosed neoplasia in psittacine birds, (24) and they occur most often in species such as budgerigars (Melopsittacus undulatus), Amazon parrots (Amazona species), cockatiels (Nymphicus hollandicus), and rose-breasted cockatoos. (3,25,26) In birds, they usually appear as masses with a diffuse base in the subcutis of the sternum, abdomen, and inner thighs, (4,25) although intracranial lipomas have also been described in ducks (Anas platyrhynchos f dom). (27)

Genetic diseases, abnormal embryo development, endocrine disorders (eg, hypothyroidism), viral infection (eg, polyomavirus), or dietary imbalances have all been implicated as playing a role in the development of lipomas in birds. (22,27-29) The underlying cause of neoplastic transformation in this cockatoo is unclear, because thorough examination of histologic slides revealed no evidence of viral inclusions, and nutritional assessment revealed the diet comprised low-fat pellets (5% fat) and vegetables. However, the diagnosis of hepatic lipidosis could support an abnormal lipid metabolism and endocrine influence in this case. Macroscopic examination of the thyroid gland was normal, and thyroxine levels were not available at the time of presentation. Because the diagnosis of hypothyroidism relies on thyrotropin stimulation testing, the endocrine influence in the present case remains undetermined. The subcutaneous and intraosseous lipomas possibly shared a similar pathogenesis in this case.

Intraosseous lipomas are often asymptomatic in people, but pain as well as pathologic fractures have been occasionally described, as in this case. One of the cases described in a dog was a 2-year-old Leonberger that presented with lameness. (12) In the cockatoo we describe, persistent lameness was observed involving the left leg, which had the tibiotarsal intraosseous lipoma. Chronic microtrauma or cortical destruction secondary to neoplastic infiltration possibly resulted in weakening of the bone associated with pain and fracture. In human medicine, diagnostic imaging of the bones with intraosseous lipomas reveals an increased signal intensity in some cases, which could be related to overload and microfractures of bone trabeculae. (13)

The radiographic lesions of the bones seen in this cockatoo appeared unusually polyostotic and diffuse compared with previous radiographic descriptions of avian bone neoplasia. (20) In human medicine, intraosseous lipomas have a variable appearance based on their stage, but none were similar to the radiographic skeletal lesion observed in this case. Stage 1 tumors consist of viable fat cells and typically appear as sharply delineated cystic lesions with an increased radiolucency. Stage 2 tumors consist of viable cells with a variable amount of central necrosis or calcification and appear as the cockade sign, which describes a well-defined lytic lesion with a central calcification. Finally, stage 3 tumors consist of fat necrosis, cyst formation, and wall sclerosis, which appear as areas of bone loss and increased radiodensity centrally and along the periphery of the region. (13,30,31) Computed tomography and magnetic resonance imaging could be valuable in the diagnosis of intraosseous lipomas in birds, because these imaging methods have a sufficient contrast resolution to allow determination of the amount of adipose tissue within a lesion, which provides a definitive diagnosis in human medicine. (32-34)

Treatment of lipomas in birds usually involves a combination of dietary management and surgery. (24) In the present case, surgical repair was elected despite the risks of nonhealing of the potentially pathologic fracture and anesthetizing a morbidly obese bird. In human medicine, surgical stabilization of pathologic fractures has been recommended to provide pain relief and conservative treatment. (35,36) Retrospectively, amputation of the fractured limb may have been preferred because the neoplastic lesions were diffuse, and debulking would not have been achievable. Surgical management of noninfiltrative intraosseous lipomas is sometimes required in human medicine, but spontaneous involution has been described, making conservative treatment a "gold standard." (10,30) In the case of infiltrative lipomas, surgical excision is usually required, but local recurrence has been reported in 36% to up to 50% of canine cases. (37,38) Radiotherapy is often recommended to limit the risk of recurrence. (19) Alternatively, use of dietary carnitine could be considered in birds. Carnitine is an amino acid derivative implicated in the metabolism of fat for energy production, which has been shown to decrease the size of naturally occurring lipomas in budgerigars. Efficiency of L-carnitine to control lipomas has not been evaluated in other species. (40) Similarly, in a case of lipomas associated with hypothyroidism, complete remission of the neoplasia in a budgerigar has been observed after thyroxine supplementation. (41)

In summary, this report describes multiple infiltrative intraosseous lipomas in a cockatoo with a humerus fracture. Although intraosseous lipomas are uncommon, they should be included in the differential diagnosis for diffuse heterogeneous bone remodeling in rose-breasted cockatoos. Their potential association with pathologic fractures could justify screening morbidly obese birds for bony abnormalities.

Graham Zoller, DVM, IPSAV, Jerome Cavoizy, DVM, Lauriane Devaux, DVM, Harriet Hahn, DVM, Alexandra Nicolier, DVM, and Minh Huynh, DVM, MRCVS, Dipl ECZM (Avian)

From the Centre Hospitalier Veterinaire Fregis, 43 avenue Aristide Briand 94110 Arcueil, France (Zoller. Devaux. Hahn. Huynh): Exovet. 17 Rue de la Bergerie 77181 Coutry, France (Cavoizy): and Vetdiagnostics. 14 avenue Rockefeller 69008 Lyon. France (Nicolier).


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Caption: Figure 1. Ventrodorsal radiographic view of a rose-breasted cockatoo with a moth-eaten pattern of lysis (asterisks) in all bones of the wings and both tibiotarsi, cortical expansion and irregular contour of the left ulna (circle), area of subperiosteal scalloping and lysis (large arrowheads), and irregular periosteal reaction (small arrowhead) of the tarsi. Medullary sclerosis (diamond) and geographic lysis is visible on both humeri as well as a fracture (arrow) of the right humerus.

Caption: Figure 2. Coelomic cavity of the rose-breasted cockatoo described in Figure 1 showing diffusely enlarged liver (arrows), abundant subcutaneous adipose tissue (dotted arrow), and intracoelomic adipose tissue (dashed arrow). Abbrev: Cd, caudal; Cr, cranial; L. left; R. right.

Caption: Figure 3. Left intertarsal joint of the rose-breasted cockatoo described in Figure 1. Note the severe soft tissue swelling (arrows).

Caption: Figure 4. Left ulna of the rose-breasted cockatoo described in Figure 1 showing thinning of the cortex (arrow) and invasion of the surrounding soft tissues and medulla by well-differentiated adipocytes (asterisks) (hematoxylin and eosin stain; bar = 500 nm).

Caption: Figure 5. Left ulna of the rose-breasted cockatoo described in Figure 1 with multifocal disruption of the cortex (arrows) and invasion of the medulla by well-differentiated adipocytes (asterisks) (hematoxylin and eosin stain, bar= 100 ([micro]m).
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Author:Zoller, Graham; Cavoizy, Jerome; Devaux, Lauriane; Hahn, Harriet; Nicolier, Alexandra; Huynh, Minh
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2019
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