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Cutaneous Mast Cell Tumor and Mastocytosis in a Black-masked Lovebird


(Agapornis personata)

Article  in  Journal of Avian Medicine and Surgery · March 2012


DOI: 10.2307/41497487 · Source: PubMed

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Cutaneous Mast Cell Tumor and Mastocytosis in a Black-masked Lovebird
(Agapornis personata)
Author(s) :Rebecca K. Dallwig, DVM, Julia K. Whittington, DVM, Karen Terio, DVM, PhD, Dipl
ACVP, and Ann Barger, MS, DVM, Dipl ACVP
Source: Journal of Avian Medicine and Surgery, 26(1):29-35. 2012.
Published By: Association of Avian Veterinarians
DOI: http://dx.doi.org/10.1647/2011-019.1
URL: http://www.bioone.org/doi/full/10.1647/2011-019.1

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Journal of Avian Medicine and Surgery 26(1):29–35, 2012
’ 2012 by the Association of Avian Veterinarians

Cutaneous Mast Cell Tumor and Mastocytosis in a


Black-masked Lovebird (Agapornis personata)
Rebecca K. Dallwig, DVM, Julia K. Whittington, DVM,
Karen Terio, DVM, PhD, Dipl ACVP, and Ann Barger, MS, DVM, Dipl ACVP

Abstract: A 12-year-old female black-masked lovebird (Agapornis personata) with a cobalt


color mutation was presented for self-mutilation of a mass located on the right lateral neck.
Cytologic evaluation of the soft tissue mass revealed a predominance of poorly stained mast cells
with metachromatic intracytoplasmic granules. The presumptive diagnosis was cutaneous mast
cell tumor. Clinical evaluation, results of a complete blood cell count and biochemical analysis,
and radiographs did not reveal systemic manifestation of mast cell disease. The mass was
surgically resected, but surgical margins were limited because of the location of the mass and the
small size of the patient. The lovebird died the day after surgery. Gross postmortem examination
revealed splenomegaly, multifocal pinpoint white nodules throughout the liver parenchyma,
severe thickening and yellow coloration of the great vessels, and pale pink swelling of the caudal
right kidney. Histopathologic analysis of the resected mass revealed sheets of round cells that
contain metachromatic granules, defined as neoplastic mast cells, within a fine fibrovascular
stroma. Similar neoplastic cells were seen in the right kidney, hepatic sinusoids, splenic pulp,
periovarian connective tissue, and bone marrow. The histopathologic diagnosis was a cutaneous
mast cell tumor and disseminated mast cell disease, or mastocytosis. To the authors’ knowledge,
this is the first reported case of a cutaneous mast cell tumor and mastocytosis in a psittacine bird.
Key words: mast cell, mastocytosis, neoplasia, self-mutilation, avian, psittacine bird, lovebird,
Agapornis personata

Clinical Report score of 2/5. An ulcerated soft tissue mass that


measured 15 mm 3 22 mm and 5 mm in thickness
A 12-year-old female intact black-masked
was visible on the right lateral aspect of the neck
lovebird (Agapornis personata) with a cobalt color
immediately cranial to the thoracic inlet (Fig 1).
mutation was presented to the University of
The mass involved the underlying musculature,
Illinois Veterinary Teaching Hospital because of
but passage of a gavage feeding tube confirmed
a 4-day history of self-mutilation. The lovebird
that it did not communicate with the crop. The
had no history of self-trauma and was reported to
surface of the mass contained a mild serosan-
be otherwise healthy. The bird was housed alone
guineous discharge, and a small amount of dried
in a household with exposure to cigarette smoke
blood was evident on the bird’s beak.
and was fed a diet that consisted of commercial
The owner initially declined extensive diagnos-
psittacine pellets and a cockatiel/parrot seed
tic testing or anesthesia and opted for simple
mix (brands unknown by the owner). No recent
wound management. Butorphanol (2.0 mg/kg
changes to the environment were reported. On
IM; Torbugesic, Fort Dodge Animal Health,
physical examination, the bird weighed 52 g
Fort Dodge, IA, USA) was administered for
and was bright and alert, with a body condition
analgesia, and the ulcerated mass was swabbed
for cytologic evaluation. Feathers on the wound
From the Zoological Medicine Service (Dallwig), Depart- periphery were plucked, and the ulcerated tissue
ment of Veterinary Clinical Medicine (Whittington), Zoolog-
ical Pathology Program (Terio), and Veterinary Diagnostic
was cleansed with sterile saline solution. An aloe
Laboratory (Barger), University of Illinois, College of vera preparation (Soother Plus cream, Harrisons’
Veterinary Medicine, Urbana, IL 61802, USA. Pet Products, Lake Worth, FL, USA) was applied

29
30 JOURNAL OF AVIAN MEDICINE AND SURGERY

2.0–2.8 g/dL [20–28 g/L]), and a high concentra-


tion of creatine kinase (925 U/L; reference range,
52–245 U/L).1 Hematogenous mast cells were not
observed. The anemia and hypoproteinemia in
conjunction with hypoalbuminemia were attrib-
uted to recent blood loss associated with self-
mutilation. Whole-body radiographs demonstrat-
ed the expansile nature of the soft-tissue mass,
which was causing tracheal deviation to the right.
No evidence of gross metastatic disease was seen.
The wound was cleaned and rebandaged as
previously described. Treatment with oral enro-
floxacin and meloxicam was continued, and
diphenhydramine (2 mg/kg PO q12h; Benadryl,
Pfizer Consumer Healthcare, Morris Plains, NJ,
USA) was added.
Three days after staging, the lovebird was
admitted for surgical resection of the mass. The
bird had remained bright and alert, and no
Figure 1. Raised ulcerated soft-tissue mass, measuring changes were revealed during physical exami-
approximately 15 3 22 3 5 mm, on the right lateral nation. Before surgery, butorphanol (2.5 mg/kg
neck of a 12-year-old female black-masked lovebird. IM once) was administered for analgesia. Gen-
eral anesthesia was induced with 5% isoflurane
to the ulcerated area, and the neck was bandaged (Minrad Inc, Orchard Park, NY, USA) delivered
with a film dressing (Telfa pad, Tyco Health Care by face mask. The lovebird was intubated with a
Group LP, Mansfield, MA, USA), cast padding, modified 8-Fr red rubber tube (Tyco Health Care
and flexible bandaging material (Vetrap, 3M Group LP, Mansfield, MA, USA), and anesthesia
Animal Care Products, St Paul, MN, USA). was maintained with 1.5%–3% isoflurane.
The bird was discharged with meloxicam (0.5 The soft tissue surrounding the mass was
mg/kg PO q24h; Metacam, Boehringer Ingelheim circumferentially incised with a scalpel blade,
Vetmedica Inc, St Joseph, MO, USA) and and the tumor was bluntly dissected from the
enrofloxacin (15 mg/kg PO q12h; Baytril, Bayer underlying tissue. The mass did not appear to
Health Care, Shawnee Mission, KS, USA). A extend through the underlying fascial plane.
commercial Romanowsky stain (Diff-Quik, Jor- Because of the location and size of the mass
gensen Laboratories Inc, Loveland, CO, USA) relative to the size of the bird, minimal margins
applied to the tissue sample revealed a highly (2–3 mm) were obtained. The skin was closed
cellular infiltrate composed primarily of presump- with 4–0 Vicryl (Ethicon Inc, Somerville, NJ,
tive mast cells and background erythrocytes USA) in a Ford interlocking pattern. The mass
(Fig 2A). The presence of mast cells was con- was submitted for histopathology. The bird had
firmed by Wright-Giemsa stain (Fig 2B). The an uneventful recovery from anesthesia and was
presumptive diagnosis was a cutaneous mast cell discharged that night.
tumor. The following day, the bird was found dead in
Twelve hours later, the lovebird was returned its cage at home. A postmortem evaluation was
for a scheduled bandage change. Because of the performed, and tissue samples were submitted for
presumptive diagnosis, the owner elected to histopathology. On gross examination, the spleen
pursue staging for neoplasia. A complete blood was enlarged (5-mm diameter) and dark red, the
cell count (CBC), whole blood biochemical analy- liver parenchyma contained multiple pinpoint
sis, and radiographic evaluation were performed. white nodules, and the caudal pole of the right
Results of the CBC showed a decreased packed kidney was enlarged and pale pink. The great ves-
cell volume (26%; reference range, 39%–51%) and sels at the heart base were thickened and yellow.
leukopenia (3.5 103/mL; reference range, 4.5–9 3 On histologic examination, the mass excised from
103/mL), and results of the biochemical analysis the neck was well demarcated but unencapsulated
revealed hypoproteinemia (0.9 g/dL [9 g/L]; and composed of sheets of round cells within a
reference range, 2.8–4.0 g/dL [28–40 g/L]), hypo- fine fibrovascular stroma. Neoplastic cells con-
albuminemia (0.7 g/dL [7g/L]; reference range, tained a moderate amount of slightly granular
DALLWIG ET AL—CUTANEOUS MAST CELL TUMOR AND MASTOCYTOSIS IN A BLACK-MASKED LOVEBIRD 31

Figure 2. Photomicrographs of cytologic preparations and histopathologic sections from a soft-tissue mass on the
right lateral neck of a black-masked lovebird; (A) cytologic preparation, showing a predominance of poorly stained
granular mast cells (small arrows) and background erythrocytes (Romanowsky stain, bar 5 10 mm); (B) cytologic
preparation, demonstrating characteristic dark metachromatic intracytoplasmic cell granules (white arrows) (Wright-
Giemsa stain, bar 5 10 mm); (C) section of trachea (lumen denoted by an asterisk), showing neoplastic cells in
syringeal marrow spaces and extending through bone into surrounding tissues (large arrow) (hematoxylin and eosin
stain, bar 5 50 mm); and (D) section of trachea, demonstrating metachromatic granules in neoplastic cells (toluidine
blue stain, bar 5 20 mm).
32 JOURNAL OF AVIAN MEDICINE AND SURGERY

basophilic cytoplasm and a large round-to-oval intracytoplasmic granules.18,34 Mast cell tumors
nucleus that contained clumped chromatin and a can be identified via cytology by using a
single prominent nucleolus. Giemsa and toluidine commercially available Romanowsky stain; how-
stains revealed metachromatic granules in neo- ever, the staining quality is variable, and mast
plastic cells (Fig 2D). Mitoses were rare. Small cells may go unidentified. Mast cells can be
numbers of eosinophils and fewer heterophils cytologically confirmed by using a Wright-Giem-
were scattered throughout the mass. Neoplastic sa stain, which demonstrates the characteristic
cells of similar morphology also were found dark metachromatic intracytoplasmic granules.18
within the syringeal marrow (Fig 2C), extending On histologic examination, mast cell granules can
into the adjacent tissue of the neck, and be better identified by using Giemsa or toluidine
infiltrating the marrow of the long bones. Similar blue stains.18 Techniques used to diagnose avian
neoplastic cells also effaced the right kidney and mast cell tumors have not been well described,
infiltrated the hepatic sinusoids, splenic red pulp, and the methodology used is often extrapolated
and periovarian connective tissue. Other lesions from mammals. In this case report, a cutaneous
included atherosclerosis and retention of the mast cell tumor was suspected based on a
superficial esophageal mucosa, suggestive of commercial Romanowsky stain used for cytologic
inanition. evaluation. However, as depicted in Figure 2A
and B, the avian mast cells were not as readily
Discussion apparent with this stain as with a Wright-Giemsa
stain. On histologic examination, granules exhib-
This case report describes the presentation of ited a typical, although faint, metachromasia with
a cutaneous mast cell tumor with secondary toluidine blue and Giemsa stains (Fig 2D).
self-mutilation and disseminated mastocytosis in Scant literature is available that describes the
an adult female lovebird. Mast cell disease is distribution and function of avian mast cells,
uncommon in birds, and, to our knowledge, this especially with regard to psittacine birds. Mast
is the first reported case of a cutaneous mast cell cells in domestic chickens have been found in
tumor and mastocytosis in a psittacine bird. highest numbers in the connective tissues of the
Various types of cutaneous and subcutaneous oviduct, proventriculus, small intestine, peritone-
neoplasia have been reported in psittacine birds, um, crop, thyroid glands, and peripheral nerves.35
including basal cell carcinoma,2 lymphosarcoma,3 In cockerels, large numbers of mast cells were
lipoma,4 malignant melanoma,5–7 metastatic renal reported in the dermis, subcutaneous tissues,
carcinoma,8 sarcoma,9 squamous cell carcino- lung, spleen, and thymus. Relative numbers of
ma,10,11 nonepitheliotropic B-cell lymphoma,12 mast cells vary among avian species, with larger
hemangiosarcoma,13 and granular cell tumors.14 counts found in chickens than in turkeys,
Mast cell disease has been documented in pheasants, or Japanese quail.36
numerous small domestic mammals and occa- Mast cell tumors in domestic mammalian
sional reptilian species, including dogs,15–20 species are highly variable. In dogs, mast cell
cats,15,16,21,22 ferrets,23–26 hedgehogs,27 a snake,28 tumors are common, which represents 7%–20%
and a chelonian.29 Mast cell tumors in birds are of all cutaneous tumors,18–20,37 and approximately
rare. Cutaneous mast cell tumors have previously 50% of these tumors are malignant. Cutaneous
been documented in owls30,31 and gallinaceous mast cell tumors in dogs are graded on a scale of
birds.32,33 Disseminated or metastatic mast cell 1–3 based on the degree of mast cell differentia-
disease has very rarely been reported in birds, tion. This grading scale in dogs has been
with cases documented in 2 chickens.32,33 correlated to the biologic behavior of the tumors
Mast cells in mammals arise from a heteroge- and, therefore, the prognosis.15,16,18,38 A grade I
nous myelomonocytic cell population originating (well differentiated) cutaneous mast cell tumor
in the bone marrow. Mature mast cells are normal is likely to be completely excised by using the
components of the dermis/subdermis, lungs, liver, recommended 2- to 3-cm lateral margins and
and gastrointestinal tract, and have important one fascial plane for a deep margin, whereas a
roles in the mediation of inflammatory responses, grade III (poorly differentiated) tumor is more
promoting hypersensitivity reactions, stimulating likely to have metastasized.19,20,39 In addition to
T cells in immune responses, and defending the grading, staging of mast cell disease is important
host against tissue parasites.15,18 Mammalian mast to determine the extent of the neoplasia. The
cells are round with a centrally located round-to- World Health Organization has established the
oval nucleus and contain varying numbers of Clinical Staging System for canine mast cell
DALLWIG ET AL—CUTANEOUS MAST CELL TUMOR AND MASTOCYTOSIS IN A BLACK-MASKED LOVEBIRD 33

tumors: stage I, a single tumor confined to the Previously documented mast cell tumors in
dermis; stage II, a single tumor confined to the birds have been confined to the head: cutaneous
dermis with regional lymph node involvement; mast cell tumors in a great horned owl (Bubo
stage III, multiple dermal tumors with local virginianus) were located adjacent to the right
infiltration and regional lymph node involvement; orbit and near the left auditory meatus,30 a mast
and stage IV, any tumor with distant metastasis cell tumor in a burrowing owl (Athene cunicularia)
or recurrence with metastasis.15,18,37,38 In dogs, the involved the oral mucosa,31 a lump on the margin
most common sites for cutaneous mast cell tumor of the right upper eyelid in Hawaiian owl (Asio
metastasis are the regional lymph nodes, spleen, flammeus sandwichensis) was later confirmed to be
and liver.18 As with other neoplastic conditions, a mast cell tumor,31 and a periocular mast cell
clinical staging is accomplished by evaluating tumor was reported in a white leghorn cock.32 The
bloodwork results, bone marrow cytology, radio- mast cell tumor found on the neck of the lovebird
graphs, regional lymph node cytology or histo- described in this case report mirrored the
pathology, and advanced diagnostics, for exam- distribution documented in cats.
ple, an abdominal ultrasound.15,18,37,40 Circulating Complications of mast cell disease in domestic
mast cells are concentrated in the buffy coat, animals include gastroduodenal ulceration sec-
which should be evaluated when performing a ondary to histamine release and subsequent
CBC. However, cytologic evaluation of a bone stimulation of gastric H2 receptors, excessive acid
marrow aspirate provides a more accurate assess- secretion, and hypermotility. Additional compli-
ment of possible mastocythemia than does a cations include pruritus, prolonged coagulation
CBC.15,18 times, and delayed healing of surgical sites.15,18,37,38
Although the behavior of mast cell disease and The lovebird described here originally presented
mastocytosis in avian species is poorly described, for self-mutilation, which may have been induced
the lovebird in this case report was staged by by pruritus.
extrapolating most of the recommendations used Treatment for mast cell disease in small animals
in dogs. Hematologic analysis and radiographic involves surgical removal of the tumor and/or a
examination were performed; however, the lack combination of radiation therapy and chemo-
of peripheral lymph nodes in birds precluded the therapy. Surgical margins recommended for mast
evaluation of lymph tissue. In addition, because cell tumor removal are 3 cm laterally and a deep
of case constraints, coelomic ultrasound and bone margin of one fascial plane.15,16,18 A study in dogs
marrow aspirates were not performed. In this reported complete excision of grade I and II
lovebird, the postmortem discovery of neoplastic cutaneous mast cell tumors by using 2-cm lateral
cells in tissues surrounding the mass as well as in margins in conjunction with a deep margin of
the bone marrow and multiple other sites led to a one fascial plane.20 Adjunct radiation therapy
presumptive assessment of grade III mast cell is recommended if the location of the tumor
disease with advanced stage III–IV neoplasia. prevents complete surgical excision. Radiation
Cutaneous mast cell tumors are not reported therapy for grade I and II mast cell tumors
as frequently in cats as in dogs; however, they reportedly achieves a 1- to 2-year disease-free
still comprise 12%–20% of all feline skin interval in 79%–97% and 77%–85% of cases,15
tumors.15,21 Cutaneous mast cell tumors in cats respectively, or 85%–95% of cases with low- or
are most often located on the head and neck,15,16 intermediate-grade mast cell differentiation.16 In
with one paper citing these locations in 43% of cases of poorly differentiated mast cell disease or
cats with mast cell tumors.21 Currently, the documented dissemination, surgical excision and
histologic grading system used to evaluate radiation therapy may only be palliative, and
canine mast cell tumors is not recommended additional treatment with chemotherapy may be
for cats because the correlation of histologic warranted. However, the prognosis is poor in
findings with prognosis differs in cats.16,21,22 many of these cases, because mast cell disease
Unlike dogs, cats have a higher propensity to appears to be fairly resistant to chemotherapy.15,18
develop mastocytosis, which is the visceral or In the case of the lovebird, disseminated disease
systemic form of the disease.16 Mastocytosis in was not suspected when the tumor was excised.
domestic mammals has a predilection for the Because of the patient’s small size, as well as the
spleen, liver, and abdominal lymph nodes.16,22 By location of the tumor on the lateral aspect of the
using these same criteria in the lovebird, the neck in close proximity to the trachea, esophagus,
discovery of mast cells in the liver and spleen and jugular vein, complete surgical resection
confirmed the presence of mastocytosis. with recommended margins was not possible.
34 JOURNAL OF AVIAN MEDICINE AND SURGERY

Although mastocytosis was not revealed until carcinoma in a peach-faced lovebird (Agapornis
postmortem examination, local adjunct radiation roseicollis). Avian Pathol. 2002;31(1):101–104.
therapy may have been an option. Treatment for 10. Klaphake E, Beazley-Keane SL, Jones M, Shoieb
mastocytosis has not been documented in birds. A. Multisite integumentary squamous cell carcino-
ma in an African grey parrot (Psittacus erithacus
In spite of radiation therapy and possible
erithacus). Vet Rec. 2006;158(17):593–596.
chemotherapy, the extent of disease described in
11. Suedmeyer WK, Henry C, McCaw D, Boucher M.
this lovebird relative to the prognosis for masto- Attempted photodynamic therapy against patagial
cytosis in domestic mammals was not likely to squamous cell carcinoma in an African rose-ringed
have resulted in a good prognosis. parakeet (Psittacula krameri). J Zoo Wildl Med.
This case report describes both a cutaneous 2007;38(4):597–600.
mast cell tumor and disseminated mastocytosis in 12. Rivera S, McClearen JR, Reavill DR. Treatment
a lovebird. Because this bird presented for self- of nonepitheliotropic cutaneous B-cell lymphoma
mutilation, a diagnostic workup, including cytol- in an umbrella cockatoo (Cacatua alba). J Avian
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Subcutaneous haemangiosarcoma in a cockatiel
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Dipl ACVR, Avery Bennett, MS, DVM, Dipl ACVS, 14. Quist CF, Latimer KS, Goldade SL, et al.
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