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DISEASE IN WILDLIFE OR EXOTIC SPECIES

Facial Squamous Cell Carcinoma and Abdominal

Peripheral Nerve Sheath Tumour with
Rhabdomyoblastic Differentiation in a
Rough-toothed Dolphin (Steno bredanensis)
M. R. Alves-Motta*,†, V. Luz-Carvalho*, D. C. S. Nunes-Pinheiro†,
K. R. Groch‡, L. Gonçalves-Pereira*, A. M. S
anchez-Sarmiento‡,
an‡, J. L. Cat~
C. Sacrist
ao-Dias‡ and J. Dı́az-Delgado‡,x
*Associaç~ao de Pesquisa e Preservaç~ao de Ecossistemas Aqu
aticos, Iparana, Caucaia, † Programa de P
os-graduaç~ao em
Ci^encias Veterin
arias, Universidade Estadual do Cear
a, Fortaleza, Cear
a, ‡ Departamento de Patologia, Faculdade de
Medicina Veterin
aria e Zootecnia, Universidade de S~ao Paulo, S~ao Paulo, Brazil and x Texas A&M Veterinary Medical
Diagnostic Laboratory, College Station, Texas, USA

Summary
We report the pathological features of a facial squamous cell carcinoma (SCC) and an abdominal peripheral
nerve sheath tumour (PNST) with rhabdomyoblastic differentiation in an aged free-ranging rough-toothed
dolphin (Steno bredanensis). The animal was found stranded dead in poor body condition. On external exami-
nation, there was a 25  7  3 cm extensively ulcerated area on the right maxillary region of the rostrum,
involving the oral mucocutaneous junction with prominent nodular edges, severe soft tissue loss and extensive
maxillary and premaxillary bone lysis. On abdominal dissection, a 5  4  3.5 cm pale tan to red, raised mass
expanded the inner aspect of the right transverse abdominis muscle. Microscopically, the aggressive facial
lesion was an acantholytic SCC with extensive osteolysis; there was no evidence of metastasis in the tissues
examined. The abdominal mass had cytohistomorphological features compatible with a localized PNST,
including whorling, Antoni A and Antoni B areas and Verocay bodies intermixed with rhabdomyoblastic com-
ponents, as suggested by phosphotungstic acid haematoxylin stain. This neoplasm was locally infiltrative, yet
no metastases were observed in the tissues examined. No immunohistochemical investigations could be per-
formed due to lack of tissue availability. Total DNA from the formalin-fixed and paraffin wax-embedded
SCC was extracted and tested by polymerase chain reaction for herpesvirus and papillomavirus genetic mate-
rial. There was no amplification for either of these genera. Other pathological findings observed in this animal
were related to the ‘live-stranding stress response’. The severity and extent of the facial SCC likely related to
anorexia and poor body condition and might have played a role in the stranding and death of this dolphin.
These two tumour subtypes add to the relatively uncommon reports of neoplasia in cetaceans. Specifically,
these appear to be the first neoplasia records for rough-toothed dolphins, including the first documentation
of a PNST with features compatible with rhabdomyoblastic differentiation in a marine mammal.

Ó 2020 Elsevier Ltd. All rights reserved.

Keywords: peripheral nerve sheath tumour; rough-toothed dolphin; squamous cell carcinoma; Steno bredanensis

Correspondence to: J. Dı́az-Delgado, Texas A&M Veterinary Medical Diagnostic Laboratory, 483 Agronomy Rd, College Station, Texas, USA. (e-mail:
josue.diazdelgado@tvmdl.tamu.edu).

0021-9975/$ - see front matter Ó 2020 Elsevier Ltd. All rights reserved.
https://doi.org/10.1016/j.jcpa.2020.02.013
 Tumours in a Rough-toothed Dolphin (Steno bredanensis)
Neoplasia in cetaceans remains a relatively uncom-
mon cause of significant morbidity and mortality,
except for the St. Lawrence Estuary beluga (Delphi-
napterus leucas) population (Lair et al., 2016). Howev-
er, published cases have increased over the last 30
years (Colegrove, 2018). Overall, tumour prevalence
ranges from approximately 1% (Arbelo et al., 2013;
Dı́az-Delgado et al., 2018) to 14% (Lair et al., 2016)
for certain cetacean populations in areas with long-
term records available. A wide spectrum of tumours
has been described and the digestive, lymphoid and
reproductive systems appear to be involved most often
(Colegrove, 2018). Few comprehensive reviews on
neoplasia of cetaceans and other marine mammal spe-
cies have been published (Howard et al., 1983; Geraci
et al., 1987; Newman and Smith, 2006; Colegrove,
2018).
Cutaneous or mucocutaneous tumours (excluding
genital involvement) described in cetaceans include:
fibroma and papilloma in the fin whale (Balaenoptera
physalus) and sperm whale (Physeter macrocephalus)
(Stolk, 1952); fibroma in the Pacific white-sided dol-
phin (Lagenorhynchus obliquidens) (Howard et al., 1983);
papilloma in the orca (Orcinus orca), harbour porpoise
(Phocoena phocoena) and narwhal (Monodon monoceros)
(Geraci et al., 1987); squamous cell carcinoma
(SCC) in the Pacific white-sided dolphin (Howard
et al., 1983); SCC in Atlantic bottlenose dolphins
(Tursiops truncatus) (Bossart et al., 2005); SCC in
Indo-Pacific humpbacked dolphins (Sousa chinensis)
(Banlunara et al., 2019); and melanoma in the Sei
whale (Balaenoptera borealis) (Uys and Best, 1966). In
contrast, there are only two reports of primary muscle
tumours: a lipoma in the dorsal muscle of a fin whale
and a mediastinal ganglioma in a blue whale (Balae-
noptera musculus) (Rewell et al., 1950). Herein, we
report the pathological features of a facial SCC and
an abdominal peripheral nerve sheath tumour
(PNST) with rhabdomyoblastic differentiation in a
free-ranging rough-toothed dolphin (Steno bredanen-
sis).
A 2.44 m long adult (of advanced age as suggested
by diffuse dental wear) female rough-toothed dolphin
in poor body condition was stranded dead on Mucur-
ipe Beach, Fortaleza, Brazil (03 430 2100 S;
 0 00
38 27 57.7 W) on September 29th, 2000. The dol-
phin was subjected to necropsy examination shortly
after. Representative samples of the skin, longissimus
dorsi, rectus abdominis and transverse abdominis
muscles, peritoneum, diaphragm, brain, oesophagus,
stomach, intestine, liver, spleen, pancreas, adrenal
glands, kidneys, ureters, urinary bladder, ovaries,
uterus, vagina and vulva were collected and fixed in
10% neutral buffered formalin. The tissues were pro-
cessed routinely and embedded in paraffin wax. Sec-
123
tions (5 mm) were stained with haematoxylin and
eosin (HE). Selected sections of the muscle tumour
were stained with Masson’s trichrome (MT) and
phosphotungstic acid haematoxylin (PTAH) to high-
light collagen and muscle fibres.
Total DNA was extracted from the formalin-fixed
and paraffin wax-embedded (FFPE) SCC sample us-
ing the DNeasyÔ Blood and Tissue kit (Qiagen, Va-
lencia, California, USA), according to the
manufacturer’s protocol. Herpesvirus detection was
performed using the pan-polymerase chain reaction
(PCR) protocol described by Vandevanter et al.
(1996) targeting the DNA polymerase gene.
Regarding papillomavirus, the protocols designed
by Rector et al. (2005), using the primer combination
AR-L1F1/AR-L1R3, and Iftner et al. (2003) were fol-
lowed to amplify segments of the genes encoding the
papillomavirus late protein L1 and early protein 1
E1, respectively. Samples of lung from a
herpesvirus-positive Magellanic penguin (Spheniscus
magellanicus) and a cutaneous papilloma from a dog
positive for canine papillomavirus were selected as
positive controls. Diethylpyrocarbonate treated wa-
ter was used as no template control. PCR products
were electrophoresed with SyberÒ Safe (Invitrogen,
Carlsbad, California, USA) and positive samples
were directly sequenced by the Sanger method. Se-
quences were compared with those available in public
databases using BLAST search.
At necropsy examination, the dolphin had a
25  7  3 cm extensively ulcerated area on the right
maxillary region of the rostrum, involving the poorly
melanized oral mucocutaneous junction with promi-
nent nodular edges. There was severe soft tissue loss
and extensive maxillary and premaxillary bone lysis
(Fig. 1; Supplementary Fig. 1). On dissection of the
peritoneal cavity, a 5  4  3.5 cm pale tan to red,
raised mass expanded the inner aspect of the right
abdominal transversus muscle. Other gross findings
included live-stranding associated cutaneous erosions,
excoriations and abrasions along the rostral, ventral
and dorsolateral bodily surfaces.
Microscopically, the right maxillary soft tissues had
a poorly demarcated, unencapsulated, densely
cellular and infiltrative neoplasm comprising epithe-
lial cells arranged in nests and anastomosing fronds,
cords and pseudoglandular structures, supported by
an inflamed desmoplastic stroma (Fig. 2). Tumour
cells displayed generalized stratified squamous differ-
entiation ranging from basal-like to polygonal to ker-
atinised squamous cells (Fig. 2). Neoplastic cells had
demarcated borders with noticeable desmosomes
and central to paracentral round euchromatic nuclei
with prominent nucleoli. Anisocytosis and anisokar-
yosis were moderate to marked, and acantholysis
124 M.R. Alves-Motta et al.

Fig. 1. Facial squamous cell carcinoma in a rough-toothed dolphin. Right lateral view. Extensively ulcerated area on the right maxillary
region of the rostrum, involving the oral mucocutaneous junction with prominent nodular edges and severe soft tissue loss. Intra-
lesional barnacle (Xenobalanus sp.) is indicated with asterisk. Bar, 10 cm. Inset: Dorsal-rostral view. Bar, 5 cm.

was a prominent feature in multiple areas (Fig. 2). with features most compatible with a peripheral nerve
Mitoses averaged five per 10 high-power fields sheath tumour (PNST) with rhabdomyoblastic dif-
(HPFs; 400). Single cell necrosis/apoptosis was ferentiation were rendered. Other relevant micro-
rare, while keratin pearls were noted occasionally. scopical findings in this case were associated with
Tumour cells often traversed the basement mem- the ‘live-stranding stress response’ and included:
branes and replaced pre-existing bone trabeculae marked, diffuse pulmonary congestion, oedema and
(Fig. 2). The adjacent stroma contained abundant occasional acute haemorrhage; pulmonary
collagen fibres admixed with pleocellular inflamma-
tory infiltrates, oedema, necrotic debris and haemor-
rhage.
Microscopically, the abdominal muscle mass con-
sisted of a poorly demarcated, unencapsulated, multi-
nodular, variably dense, moderately cellular and
infiltrative neoplasm. It was largely composed of
wavy spindle cells arranged in bundles, palisades,
whorls and plexiform patterns interspersed with
larger, polygonal to elongate cells resembling rhabdo-
myoblasts, supported by a loose fibrillary matrix
(Figs. 3 and 4). Tumour cells had small amounts of
eosinophilic fibrillary cytoplasm with poorly distinct
borders and irregularly oval to elongate
normochromatic nuclei with generally a single
nucleolus. Anisocytosis and anisokaryosis were
moderate to marked, and mitoses averaged four per
10 HPFs. This neoplasm often encroached nerve Fig. 2. Microscopical features of facial squamous cell carcinoma in
structures and displayed compact Antoni A- and a rough-toothed dolphin. Neoplastic epithelial cells, ar-
loose Antoni B-like patterns, as well as Verocay ranged in nests (arrowheads) and anastomosing fronds
and cords and pseudoglandular structures (asterisks) infil-
bodies (Figs. 3 and 4). The cytoplasm of the smaller trate the inflamed desmoplastic stroma. HE, decalcified
spindle-shaped cells stained faintly red, while the specimen. Bar, 200 mm. Arrow indicates bone trabecula.
moderate to large cytoplasm of rhabdomyoblast-like Upper inset: tumour cells progress from basal (b) to polyg-
cells stained blue, highlighting rare cross striations onal (p) to keratinized squamous cells (k). HE. Bar,
(Fig. 4). No metastases were seen for either of the neo- 100 mm. Middle inset: acantholytic tumour cells. HE.
Bar, 50 mm. Lower inset: tumour cells (asterisks) and
plasms. Based on these findings, diagnoses of facial tumour stroma expansion replace pre-existing bone trabec-
acantholytic SCC and an abdominal wall sarcoma ula (arrowhead). HE. Bar, 100 mm.
 Tumours in a Rough-toothed Dolphin (Steno bredanensis)
Fig. 3. Microscopical features of PNST in a rough-toothed dol-
phin. Detail of intratumoural transition area between
compact Antoni A-like (A) and loose Antoni B areas (B).
PTAH. Bar, 200 mm. Inset: Verocay body formation.
PTAH. Bar, 50 mm.
Fig. 4. Microscopical features of PNST in a rough-toothed dol-
phin. Detail of rhabdomyoblastic cells with blue-stained
moderate to large cytoplasm and rare cross striations (ar-
row), amid loosely arranged neoplastic smaller spindle-
shaped cells stained faintly red in a loose collagenous
stroma. PTAH. Bar, 20 mm. Inset: detail of plexiform
pattern. PTAH. Bar, 50 mm.
emphysema with multifocal atelectasis; acute mono-
phasic, segmental skeletal myocyte degeneration;
and acute renal tubular degeneration. No positive
amplification was observed for herpesvirus or papillo-
mavirus DNA in the analysed tissue.
Facial and mucocutaneous SCCs are among the
most common malignant skin tumours of man and
domestic animals (Zalaudek et al., 2012;
Goldschmidt and Goldschmidt, 2016). SCC may
result from multifactorial causes such as
125
environmental, pathogens (e.g. papillomavirus,
herpesvirus) and host-related factors. Geographical
location, climate (ultraviolet [UV] light exposure)
and anatomical location (especially poorly melanized
and hairless areas) influence the incidence of SCC in
man and animals (Zalaudek et al., 2012;
Goldschmidt and Goldschmidt, 2016). In cetaceans,
there are few reports of oral SCC presumptively
associated with papillomavirus (Bossart et al., 2005).
The transition between papillomas and SCC was
documented in some of these dolphins (Bossart et al.,
2005). Recently, multicentric cutaneous SCCs were
reported in three Indo-Pacific humpback dolphins
(S. chinensis) from Thailand (Banlunara et al., 2019).
A progression from severe epithelial hyperplasia
with occasional dysplasia to neutrophilic, necroulcer-
ative dermatitis to invasive SCC was observed. While
oral SCC in the Atlantic bottlenose dolphins origi-
nated from the anterior aspect of the tongue and/or
near the lingual frenulum (Bossart et al., 2005), the
cutaneous SCC in the Indo-Pacific humpback dol-
phins originated and concentrated on the dorsal
head, with progressive involvement of the blowhole,
trunk, flipper, tail fluke and viscera (Banlunara
et al., 2019). Therefore, in both reports, SCC ap-
peared to arise in poorly melanized areas; however,
no further conclusions were drawn. In the present
case, the SCC was centred on the poorly melanized
oral mucocutaneous junction of the right maxillary
region of the rostrum. Nonetheless, UV light-
associated preneoplastic changes such as solar elasto-
sis and actinic keratosis were not readily evident histo-
logically. A potential oncopathogenic role for UV
light remains elusive. Moreover, two of the Indo-
Pacific humpback dolphins had evidence of lung
and hilar lymph node metastasis. In one of these, mo-
lecular analyses identified a novel alphaherpesvirus
(‘Sousa chinensis alphaherpesvirus’) (Banlunara et al.,
2019). Comparatively, the SCC described in those
two studies and the present case had similar cytohisto-
morphological features. The lack of readily evident
viral inclusion bodies was also a common feature in
those cases and the present case. However, in contrast
to SCC in Indo-Pacific humpback dolphins, we did
not detect any regional or distant metastasis. In this
case, molecular analysis for herpesvirus and papillo-
mavirus in a tissue sample was negative.
PNSTs may be classified as benign or malignant
and may include a number of histological subtypes
and their respective variants: schwannoma and vari-
ants; neurofibroma and variants; perineurioma; neu-
roma; hybrid nerve sheath tumours; and ‘Triton
tumours’ (TTs), among others (Fletcher et al., 2013;
Higgins et al., 2016). TTs refer to PNSTs with
intimately interposed skeletal muscle fibres or
126 M.R. Alves-Motta et al.
rhabdomyosarcomatous differentiation (Locatelli,
1925; Stasik and Tawfik, 2006; Perry, 2013). Both
benign and malignant TTs have been described;
however, the term TT has been often applied
historically to malignant variants (Fletcher et al.,
2013; Perry, 2013). In domestic species,
neurofibromas, schwannomas and perineuriomas
account for the most common PNSTs (Higgins
et al., 2006; Ochi et al., 2008; Schoniger and
Summers, 2009; Schoniger et al., 2011), while
malignant PNSTs occur most commonly in the dog,
typically involving the brachial plexus, other spinal
nerves or the trigeminal nerve (Summers et al.,
1995). Only two cases of PNST with rhabdomyosar-
comatous components have been reported in domes-
tic species; a dog (Dahme et al., 1987) and, more
recently, a cat (Stoll et al., 2018). The former
described rhabdomyosarcomatous elements in a cer-
vical (C5eC6) spinal nerve root tumour from a giant
Schnauzer dog (Dahme et al., 1987). In the latter, a
malignant TT extending from the dermis to the sub-
cutis of the ventral abdomen was diagnosed in a 12-
year-old female domestic shorthaired cat based on cy-
tohistomorphological and immunohistochemical fea-
tures. Neoplastic cells had strong vimentin
immunoexpression and occasional labelling for S100
and desmin. Furthermore, desmin-positive neoplastic
cells had strong labelling for a-sarcomeric actin and
muscle actin, weak labelling for myoglobin and occa-
sional labelling for myogenin (Stoll et al., 2018). The
present rough-toothed dolphin showed some cytohis-
tomorphological similarities with those two cases, as
all of them were characterized by a biphasic spindle
cell growth with a readily evident admixture of
compact and looser myxoid patterns with spindle-
shaped and spindle-shaped to polygonal cells, respec-
tively. In our case, however, ample areas of Antoni A
and Antoni B structure and Verocay bodies were
highly suggestive of schwannomatous differentiation.
This is in contrast to the malignant TT in the cat,
where the biphasic neoplasm appeared less differenti-
ated. A thorough immunohistochemical panel pro-
vided substantial diagnostic support (Stoll et al.,
2018). In our case, PTAH staining proved diagnosti-
cally useful. While the minimal cytoplasm of the
smaller spindle-shaped cells stained faintly red, the
cytoplasm of rhabdomyoblast-like cells stained blue
and occasional cross striations were highlighted.
Because of the lack of availability of neoplastic tissue,
we could not investigate the immunophenotypical
profile of this neoplasm. However, it is reasonable to
conclude, in light of the cytohistomorphological fea-
tures and tinctorial properties (PTAH staining) of
the tumour cells, that the neoplasm was most compat-
ible with a PNST with rhabdomyoblastic differentia-
tion. Furthermore, based on the relatively low mitotic
count, moderate to marked anisocytosis and anisokar-
yosis, ‘divergent differentiation’ and local infiltration,
it is believed that the neoplasm represented a low-
grade malignancy.
In summary, we describe a case of multiple
neoplasia in a aged, free-ranging female rough-
toothed dolphin, specifically a facial SCC and an
abdominal wall sarcoma with cytohistomorphologi-
cal and tinctorial (PTAH) features most compatible
with a PNST with rhabdomyoblastic differentiation.
No metastases were identified for either of the neo-
plasms. These appear to be the first records of
neoplasia for this species, including the first documen-
tation of a PNST with rhabdomyoblastic differentia-
tion in a marine mammal. In this case, the severity
and extent of the facial SCC likely resulted in
anorexia, poor body condition and might have played
a major role in the live-stranding event.
Acknowledgments
This research did not receive any specific grant from
funding agencies in the public, commercial or not-
for-profit sectors. JCLD is the recipient of a fellowship
from the National Research Council (CNPq; grant
#304999/2018-0). JDD is the recipient of a post-
doctoral fellowship from the S~ao Paulo Research
Foundation (FAPESP; grant #2017/02223-8). CS is
the recipient of a post-doctoral fellowship from FA-
PESP (grant# 2018/25069-7).
Supplementary data
Supplementary data to this article can be found on-
line at https://doi.org/10.1016/j.jcpa.2020.02.013.
Conflict of Interest Statement
The authors declare no potential conflicts of interest
with respect to the research, authorship and/or publi-
cation of this article.
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½ Received,
Accepted, March 1st, 2020 
October 8th, 2019