J. Comp. Path. 2018, Vol. 159, 31e35 Available online at www.sciencedirect.

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DISEASE IN WILDLIFE OR EXOTIC SPECIES

Ovarian Teratocarcinoma in an Emu (Dromaius

novaehollandiae): Histopathological and
Immunohistochemical Characterization
J. Leal de Araujo*, A. Perry*, J. Wild†, L. Kleinschmdit‡,
S. Hoppesx and R. R. Rech*
* Department of Veterinary Pathobiology, † College of Veterinary Medicine, Texas A&M University, College Station, Texas,
‡
Endangered Species Research Center & Veterinary Hospital, Saint Louis Zoo, St. Louis, Missouri and x Department of Small
Animal Clinical Sciences, Texas A&M University, College Station, Texas, USA

Summary
A 17-year-old female emu (Dromaius novaehollandiae) was presented for clinical evaluation due to a 3-week his-
tory of anorexia and progressive weight loss. The emu died after sedation. At necropsy examination, the ovary
and the majority of the oviduct were effaced by a multinodular cystic mass and accompanied by 6 l of coelomic
effusion. Histopathology revealed a neoplasm composed of well-differentiated, poorly organized tissues derived
from ectoderm, mesoderm and endoderm. Tissues within the neoplasm expressed glial fibrillary acidic protein,
desmin and cytokeratins AE1/AE3, respectively, confirming the diagnosis of teratocarcinoma.

Ó 2018 Elsevier Ltd. All rights reserved.

Keywords: emu; malignant teratoma; ovary; teratocarcinomatosis

A 17-year-old female emu (Dromaius novaehollandiae)
was presented to the Texas A&M University Zoolog-
ical Medical Service, College Station, Texas, USA,
for a 3-week history of anorexia. The emu had been
treated by the owner for a presumed gastrointestinal
impaction with daily oral administration of mineral
oil with no improvement of clinical signs. One day
prior to presentation the emu became recumbent.
On presentation the emu was alert, but was weak
and having difficulty standing. On initial physical ex-
amination the emu was emaciated (body condition
score: 1/5) and dehydrated. After standing on arrival,
the emu became recumbent, unable to rise and dysp-
noeic. The coelom was markedly distended with a
fluid wave appreciated on ballottement. Celiocentesis
was performed and revealed a yellow, cloudy transu-
date with no evidence of infectious organisms. Differ-
ential diagnoses included hepatic, renal, cardiac or
Correspondence to: R. R. Rech (e-mail: RRech@cvm.tamu.edu).
reproductive disease. Complete blood count, serum
biochemistry profile, abdominal fluid analysis and
computed tomography (CT) scan were recommen-
ded and the bird was sedated with ketamine (4 mg/
kg) and midazolam (0.2 mg/kg). Immediately after
sedation, the emu developed respiratory distress and
died.
Necropsy examination revealed 6 l of tan to yellow,
translucent, viscous fluid containing strands and pla-
ques of fibrin in the coelomic cavity. The ovary and
the majority of the oviduct were effaced by a
40  23  9 cm multinodular mass composed of
numerous solid, grey to light tan nodules and cysts
filled with clear, viscous fluid (Fig. 1). On cross sec-
tion, the nodules were pale tan to pink with areas of
mineralization. Numerous similar nodules and cysts
were implanted throughout the coelomic cavity.
Representative sections of all major organs and the
neoplastic nodules were fixed in 10% neutral buffered
formalin, processed routinely and embedded in

0021-9975/$ - see front matter Ó 2018 Elsevier Ltd. All rights reserved.
https://doi.org/10.1016/j.jcpa.2018.01.003
32 J. Leal de Araujo et al.

Fig. 1. Teratocarcinomatosis in an emu. Note the numerous nod-

ules and cysts throughout the coelomic cavity affecting the
ovary, oviduct, mesentery and body wall as well as the Fig. 2. Histopathological and immunohistochemical features of
coelomic effusion. tissues originating from the ectoderm in an ovarian terato-
carcinoma in an emu. HE. Bar, 20 mm. Inset: IHC for
GFAP confirms the ectodermal origin of the tissue resem-
bling brain.
paraffin wax. Sections (4 mm) were stained with hae-
matoxylin and eosin (HE). Serial sections were also
subjected to immunohistochemistry (IHC) using pri- desmin (Fig. 3) and areas of well-differentiated carti-
mary antibodies specific for glial fibrillary acidic pro- lage and bone. Endoderm-derived tissues included
tein (GFAP) (Biogen, Cambridge, Massachusetts, ciliated columnar epithelium with goblet cells resem-
USA; 1 in 4,000 dilution), cytokeratins AE1/AE3 bling respiratory or intestinal epithelium immunore-
(CellMarque, Rocklin, California, USA; ready to active for cytokeratins AE1/AE3 (Fig. 4), sometimes
use), desmin (BioCare, Pacheco, California, USA; 1 lining large cystic spaces filled with mucinous mate-
in 10 dilution), vimentin V9 (Biogen; 1 in 3,000 dilu- rial. No tissues were positive for vimentin or S100 an-
tion) and S100 (CellMarque; ready to use). The reac- tibodies. Based on the presence of tissues derived from
tivity of each antigen was ‘visualized’ following all three germ layers and the extensive spread of the
treatment with 3, 30 diaminobenzidine tetrahydro- neoplastic cells throughout the coelom, malignant
chloride and sections were counterstained with hae- teratoma with carcinomatosis (teratocarcinomatosis)
matoxylin. Sections for detection of cytokeratin, was diagnosed.
vimentin and GFAP IHC were pretreated with cit-
rate heat antigen retrieval solution (BioGenex, Fre-
mont, California, USA), while sections for detection
of desmin were pretreated with reveal heat antigen
retrieval solution (BioCare) and sections for detection
of S100 received no antigen retrieval pretreatment.
Microscopical examination revealed that the
neoplasm was composed of a mixture of well-
differentiated tissues from the three embryonic germ
cell layers: ectoderm, mesoderm and endoderm
(Supplementary Fig. 1). The majority of the tumour
was composed of ectoderm-derived tissues, primarily
disorganized, but well-differentiated neural tissue,
consisting mostly of neurons and occasional clustered
glial cells embedded in an eosinophilic fibrillary
meshwork (neuropil). Areas of neural tissue were oc-
casionally lined by ependymal cells. Astrocytic pro-
cesses of the neuropil were immunoreactive for
GFAP (Fig. 2). Other ectoderm-derived tissues Fig. 3. Histopathological and immunohistochemical features of
tissues originating from the mesoderm in an ovarian terato-
included squamous epithelium, scattered melano- carcinoma in an emu. HE. Bar, 20 mm. Inset: IHC for des-
cytes and Herbst corpuscles. Mesoderm-derived tis- min confirms the mesodermal origin of the tissue
sues included smooth muscle, which expressed resembling smooth muscle.
 Ovarian Teratocarcinoma in an Emu
Fig. 4. Histopathological and immunohistochemical features of
tissues originating from the endoderm in an ovarian terato-
carcinoma in an emu. HE. Bar, 20 mm. Inset: IHC for cy-
tokeratin confirms the endodermal origin of the tissue
resembling glandular epithelium.
Teratomas originate from totipotent cells of at least
two, and usually three, embryonic germ cell layers:
ectoderm, mesoderm and endoderm (Kusewitt and
Rush, 2016; MacLachlan and Kennedy, 2016). In
man, teratomas are usually subdivided into three
main categories: mature (cystic) teratomas,
immature teratomas and monodermal teratomas
(Outwater et al., 2001; Schmidt and Kommoss,
2007). Both mature and immature teratomas are
derived from the three germ layers. Mature
teratomas are the most common germ cell tumour in
man, are typically composed of mixed mature tissues
and have benign behaviour. Mature teratomas
occur in all life stages, but are most commonly
diagnosed in women of reproductive age (mean age
30 years) (Outwater et al., 2001). They are nearly al-
ways unilocular and always contain ectodermal tis-
sues that may include skin or hair as well as neural
tissue. Mesodermal and endodermal tissues are also
observed in the majority of cases. Immature teratomas
contain at least some embryonic tissues, are more
frequently malignant, affect younger patients (usually
during the first two decades of life) and are much less
common (<1% of ovarian teratomas) (Talerman,
1994). Immature teratomas tend to be larger than
mature teratomas and contain areas of solid tissue as
well as cystic cavities that may be filled with serous
or mucinous fluid. While one of the defining charac-
teristics of this tumour is the presence of immature/
embryonal tissue, some mature tissue is invariably
observed. Monodermal teratomas are predominately
or solely of one germ layer origin and include struma
ovarii (composed of mature thyroid tissue), carcinoid
and neural tumours (Clement et al., 1991).
33
In veterinary medicine classification of ovarian tu-
mours is less defined, potentially because ovarian ter-
atomas are rarely observed in domestic animals,
although they have been reported in the bitch, sow,
mare and cow (Schlafer and Miller, 2016). When
ovarian teratomas are diagnosed in domestic animals,
they are usually composed of well-differentiated tis-
sues and have benign behaviour, similar to the mature
teratoma classification in man. In the present case,
the ovarian teratoma was multilocular and displayed
evidence of malignancy in its spread throughout the
coelomic cavity, aligning it with the immature tera-
toma classification in man.
Teratomas have been documented in several avian
species including chickens (Helmboldt et al., 1974),
ducks (Hamir, 1985; Cullen et al., 1991; Bolte and
Burkhardt, 2000; Mutinelli and Vascellari, 2002;
Palmieri et al., 2012), geese (Reece and Lister,
1993), raptors (Ford et al., 2006; Lopez and Murcia,
2008), a heron (Schelling, 1994), a pigeon (Hooper,
2008) and turkeys (Pazdzior et al., 2012). In domestic
fowl, teratomas are rare and have been reported most
commonly in the testes (Palmieri et al., 2012). Extra-
gonadal sites of teratomas in birds include the cra-
nium, retrobulbar area, eye, brain, mediastinum
and coelom (Schelling, 1994; Mutinelli and
Vascellari, 2002; Ford et al., 2006; Hooper, 2008;
Lopez and Murcia, 2008; Palmieri et al., 2012;
Pazdzior et al., 2012). To date, teratomas in ratites
have been only reported in emus (Manasse and
Steinberg, 2015), with voluminous coelomic effusion.
While the ovarian teratoma in emus was diagnosed as
a malignant teratoma with carcinomatosis (teratocar-
cinomatosis), it is also possible that this represents a
syndrome similar to one of two conditions reported
in women with ovarian teratomas (Khan et al.,
2005). One rare condition, gliomatosis peritonei, is
associated with ovarian teratomas and involves im-
plantation or development of numerous nodules of
glial tissue throughout the abdominal cavity. Another
is pseudo-Meigs syndrome, which involves peritoneal
and pleural effusion without malignant cells and is
similar to Meigs syndrome, except for the type of
ovarian tumour associated with the effusion. In
women, neither of these syndromes negatively affects
prognosis, although glial tissue may persist after
removal of the ovarian tumour (Khan et al., 2005).
Although teratomas in animals are generally
benign, malignant teratomas or teratocarcinomas,
composed of one or more poorly differentiated tissues
(MacLachlan and Kennedy, 2016), with faster
growth and metastatic potential, can also occur. Te-
ratocarcinomas usually have a large component of
undifferentiated or embryonal tissue and areas of ne-
crosis and haemorrhage (Crum, 2010). Clinical signs
34 J. Leal de Araujo et al.
in the present case were not apparent until late in the
course of disease and in the previously reported case
(Manasse and Steinberg, 2015), the emu was found
dead with few premonitory signs. It is possible that
the tumours in these cases were present for some
time, although the timeline of disease progression is
impossible to ascertain. When teratomas are diag-
nosed ante-mortem, surgery may be attempted,
particularly in the case of single, benign teratomas.
Indeed, in women surgical removal of ovarian tera-
tomas may be attempted and be curative; however,
if there is significant associated peritoneal disease as
in the case of gliomatosis peritonei or pseudo-Meigs
syndrome (Khan et al., 2005); however, though in
the case of gliomatosis peritonei glial tissue may
persist. In the present case, apparent significant
dissemination of the tumour resulting in emaciation
would have made the emu a poor surgical candidate,
even if diagnosis of the teratoma had occurred prior to
death. In women, ruptured cystic teratomas are rare,
but can lead to peritoneal effusion (Maiti et al., 2008;
Nader et al., 2014), as seen in this emu.
In conclusion, despite the reported rarity of
neoplasia in ratites, ovarian teratoma should be
considered a differential diagnosis for this species,
particularly in cases of sudden death or rapid
decline and/or when disseminated disease is observed.
Further characterization of such cases in animals will
be required in order to determine if conditions similar
to gliomatosis peritonei or pseudo-Meigs syndrome
occur in non-human species.
Conflict of Interest Statement
The authors report no conflict of interest with respect
to publication of this manuscript.
Supplementary data
Supplementary data related to this article can be
found at https://doi.org/10.1016/j.jcpa.2018.01.003.
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