Arteriovenous Haemangioma

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J. Comp. Path. 2008, Vol. 139, 130e136 Available online at www.sciencedirect.com
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SHORT PAPER
Arteriovenous Haemangioma
in Two Dogs and a Cat
Cor
002
doi
S. Schöniger*, M. S. Tivers†, S. J. Baines† and B. A. Summers*
*Department of Pathology and Infectious Diseases and †Department of Veterinary Clinical Sciences, The Royal Veterinary
College, Hawkshead Lane, North Mymms, Hatfield, Herts AL9 7TA, UK
resp
1-99
:10.1
Summary
Haemangiomas are benign vascular tumours and several types can be distinguished based on microscopical
features. Capillary and cavernous haemangiomas are most commonly reported in man and domestic animals.
Arteriovenous haemangiomas are rare variants in man and herein we describe this subtype in two dogs and one
cat. One dog and the cat presented with a cutaneous vascular lesion, the other dog with a bleeding mass in the
tongue. Surgically excised masses comprised non-encapsulated proliferations of variably sized arterial- and
venous-like vessels, accompanied by clusters of capillaries and immature vascular structures in the feline cuta-
neous tumour and the canine lingual neoplasm. All vasoformative elements had vonWillebrand factor-positive
endothelia enclosed by a smooth muscle actin-positive tunica media or by pericytes. The results of this study
expand the range of differential diagnoses for vascular neoplasms in the dog and cat.
� 2008 Elsevier Ltd. All rights reserved.
Keywords: arteriovenous haemangioma; cat; dog
Haemangiomas are benign tumours of vascular endo-
thelial cells or their progenitors. In man, they are
most frequently located in the skin, but have also
been described in other tissues and organs (Weiss
and Goldblum, 2001). Haemangiomas are common
in dogs and rare in cats, horses and other domestic
animals (Goldschmidt and Hendrick, 2002). Canine
haemangiomas are also most commonly located in
the skin (Schultheiss, 2004) but in addition are
recorded in the tongue (Van der Gaag et al., 1989;
Schoofs, 1997), spleen (Day et al., 1995; Schultheiss,
2004), synovia (Miller et al., 2007), conjunctiva (Pirie
et al., 2006), liver (Rallis et al., 1998), kidney (Eddle-
stone et al., 1999) and spinal cord (Cordy, 1979).
Feline haemangiomas have also been reported in
the skin (Miller et al., 1992), tongue (Crow et al.,
1981) and conjunctiva (Pirie and Dubielzig, 2006).
Cutaneous haemangiomas are also described in the
horse (Johnson et al., 1996).
ondence to: Dr. S. Schöniger (e-mail: sschoeniger@rvc.ac.uk).
75/$ - see front matter
016/j.jcpa.2008.05.005
Microscopically, haemangiomas are characterized
by proliferating, vasoformative mesenchymal tissue
forming capillary and cavernous vessels and, less often,
arterial and venous structures. Endothelial cells in
these tumours may be surrounded by pericytes and
fibroblasts (Calonje and Fletcher, 2007; Gross et al.,
2007a). Haemangiomas may be classified histologi-
cally as capillary, cavernous, arteriovenous, lobular,
spindle cell or epithelioid subtypes (Vos et al., 1986;
Calonje and Fletcher, 2007; Gross et al., 2007a; War-
ren and Summers, 2007). Most haemangiomas in
dogs and cats are capillary, cavernous or combined
capillaryecavernous (Van der Gaag et al., 1989;
Hargis et al., 1992; Miller et al., 1992; Goldschmidt
and Hendrick, 2002).
In man, arteriovenous haemangiomas are rare tu-
mours that have been diagnosed in the head and
neck area, limbs and oral cavity including the tongue.
They contain a mixture of thick- and thinner-walled
arterial and venous vessels sometimes also with capil-
laries (Barrett and Speight, 2000; Calonje and
Fletcher, 2007). Arteriovenous haemangiomas have
been described in a textbook as rare variants of hae-
mangioma in dogs and cats (Gross et al., 2007a).
� 2008 Elsevier Ltd. All rights reserved.
mailto:sschoeniger@rvc.ac.uk
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Arteriovenous Haemangioma in Two Dogs and a Cat 131
The present communication is the first description of
this tumour in the primary literature.
Case 1 was a 7-year-old, neutered male Belgian
Tervuren dog which developed a small, exophytic
dermal mass on the right dorsal antebrachium over
the cephalic vein. The mass (0.6 cm in diameter)
was dark red and fluctuant on palpation. The mass
was noted after a cephalic venipuncture had resulted
in venous thrombosis and formation of a perivenous
haematoma. Initially, the mass was clinically silent,
but it began to bleed 18 months after the venipunc-
ture. A complete blood count, serum biochemistry
analysis and a coagulation panel were within normal
limits. The mass was removed together with the over-
lying skin. No connection was noted to the underlying
cephalic vein.
The second case occurred in a 10-year-old, female
Domestic Longhair cat, which reportedly presented
with a 1 cm diameter vascular mass located at
the base of the right ear. This mass was surgically
excised.
A 4.5-year-old, neutered male Greyhound (case 3)
was presented for investigation of a 2 cm diameter,
red, ulcerated, bulging mass on the right ventral as-
pect of the tongue. This had been present for approx-
imately 10 weeks (Fig. 1). The regional lymph nodes
were unremarkable on palpation. Whilst the dog was
hospitalized there was intermittent profuse haemor-
rhage from the mass. Routine serum biochemistry,
haematology and clotting times were within normal
limits and no pulmonary metastases were identified
on thoracic radiographs. An excisional biopsy was
performed with 5 mm margins, followed by primary
closure. The dogmade a good recovery and no further
lingual haemorrhage was noted. Telephone follow-up
18 months after excision revealed that there had been
Fig. 1. Canine lingual arteriovenous haemangioma (case 3). Par-
tial rotation of the tongue reveals a raised, ulcerated, red
mass located on the right ventral aspect near the lateral
margin (arrow). Bar, 1 cm.
no recurrence of the lesion or of lingual haemorrhage
and that the dog was well.
The excised masses were fixed in 10% neutral buff-
ered formalin and submitted for microscopical evalu-
ation. Tissue specimens were processed by routine
methods, embedded in paraffin wax, sectioned and
stainedwith haematoxylin and eosin (HE). AnElastic
vanGieson stainwas applied to sections of the tumours
from cases 1 and 3. Immunohistochemistry (IHC) for
the detection of von Willebrand factor (vWF; clone
A0082, diluted 1 in 4000;DakoCytomation,Glostrup,
Denmark), vimentin (clone V9, diluted 1 in 500;
Sigma Biosciences, Poole, Dorset), cytokeratin (clone
5D3+LP34, diluted 1 in100; Vector Laboratories,
Burlingame, USA), smooth muscle actin (clone
aSMA, diluted 1 in 50;Vector Laboratories) and lyso-
zyme (Clone A0099, diluted 1 in1500; DakoCytoma-
tion) was performed on sections of the tumours from
cases 1 and 3. The avidinebiotineperoxidase (ABC)
method with 3,30-diaminobenzidine tetrahydrochlor-
ide as chromogen was used.
Microscopically, all of the masses were composed
of non-encapsulated clusters of small- and medium-
sized, thick- and thin-walled vascular structures
resembling arteries and veins, respectively (Figs. 2e4).
Many vessels appeared malformed because of their
size, irregular shape and variation in thickness of the
vesselwall.Vesselswere linedbya single layer of atten-
uated to plump, monomorphic endothelia. Thick-
walled and most thin-walled vascular structures had
a variably developed mural smooth muscle layer. In
Fig. 2. Canine cutaneous arteriovenous haemangioma (case 1).
The tumour is composed of irregular small- and medium-
sized, thick- and thin-walled vascular structures separated
by collagen fibres and sheets of adipocytes. Thin-walled
vessels often branch and some have a partial muscular
wall. The contiguity (asterisk) of an arterial-type vessel
(arrow) with a venous-type vessel (arrowhead) resembles
an arteriovenous anastomosis. HE. Bar, 200 mm.
Fig. 4. Canine lingual arteriovenous haemangioma (case 3). Pro-
liferating vascular elements expand the endo- and perimy-
sium of tongue musculature and surround myofibres(asterisks). Vascular elements include thick-walled arte-
rial-type (thick arrows), thin-walled venous-type (thin ar-
rows) and capillary structures and slit-like vascular spaces
(arrowheads). HE. Bar, 120 mm.
132 S. Schöniger et al.
case 1 there were occasional connections between
arterial-type and venous-type vascular structures
that resembled arteriovenous anastomoses (Fig. 2).
Lumina of vascular structures were often filled with
red blood cells and proteinaceous fluid. In two cases,
many arterial- and venous-type vascular structures
were surrounded by dense clusters of tiny capillary
vessels (cases 2 and 3) and slit-like vascular spaces
(case 3; Figs. 3e5). Capillary proliferations and slit-
like vascular spaces were formed by uniform plump
spindle-shaped endothelial cells with a single elongate
hyperchromatic to vesicular nucleus and a mild
amount of eosinophilic cytoplasm (Fig. 5). Mitoses
were not a feature of the arterial and venous vessels
in any tumour or of the capillary clusters in the feline
cutaneous tumour (case 2). By contrast, sparsemitotic
figures (1e2 per occasional �40 objective field) were
noted in cells lining the capillary vessels and slit-like
vascular spaces in the canine lingual tumour (case 3).
In the cutaneous masses (cases 1 and 2), the vascu-
lar proliferations were well-demarcated, restricted
to the dermis, effaced adnexa and separated by
collagen bundles (cases 1 and 2) and small sheets of
adipocytes (case 2). The vascular nodule in the
tongue (case 3) was poorly demarcated and involved
the mucosa, submucosa and underlying musculature.
Within the lingual muscle, vascular elements ex-
panded the endomysium and perimysium and sur-
rounded muscle fibre bundles and individual muscle
fibres (Fig. 4). The overlying epithelium was focally
ulcerated in all cases and the exposed superficial der-
mis or lamina propria was infiltrated by neutrophils
(cases 1 and 2) and partially replaced by granulation
Fig. 3. Feline cutaneous arteriovenous haemangioma (case 2).
The dermis is expanded by small- and medium-sized arte-
rial- and venous-type vascular structures, some of which
are surrounded by closely packed proliferating capillaries
(asterisks). HE. Bar, 300 mm. The inset shows detail of
the region of capillary proliferation. HE. Bar, 70 mm.
tissue with histiocytic infiltration (case 3). In the
ulcerated areas, some vascular channels opened to
the surface of the skin and tongue (case 1 and 3),
resulting in haemorrhage.
Similar to normal arteries, numerous thick-walled
vascular structures contained an internal elastic
lamina demonstrated by Elastic van Gieson stain.
IHC demonstrated expression of vWF antigen and
vimentin by endothelial cells and expression of
smooth muscle actin and vimentin by smooth muscle
cells and pericytes. IHC confirmed that arterial- and
venous-type vascular structures were lined by a single
layered endothelium (Fig. 6) and contained a mural
Fig. 5. Canine lingual arteriovenous haemangioma (case 3). Arte-
rial- and venous-type vascular structures (arrowheads) are
surrounded by proliferating capillaries and slit-like vascu-
lar spaces (arrows). HE. Bar, 70 mm.
Fig. 6. Canine lingual arteriovenous haemangioma (case 3). Expression of vWF antigen. (A) Vascular structures (arrowheads) and pro-
liferating capillaries and slit-like vascular spaces (asterisk) are lined by a singular layer of endothelial cells expressing vWF. (B)
Higher magnification indicating positive immunolabelling (arrows). IHC. Bar, (A) 200 mm, (B) 45 mm.
Arteriovenous Haemangioma in Two Dogs and a Cat 133
layer of concentrically arranged smooth muscle cells
(Fig. 7). Capillary buds and slit-like vascular spaces
were also lined by a singular layer of endothelial cells
(Fig. 6) that were often surrounded by pericytes
(Fig. 7). Cells forming vascular elements did not
express cytokeratin or lysozyme. Histiocytic cells
associated with the ulcerated mucosal surface of the
tongue (case 3) labelled positively for lysozyme.
Fig. 7. Canine lingual arteriovenous haemangioma (case 3). Expressio
type (thin arrow) vascular structures have smoothmuscle withi
vessel (thick arrow). The endothelial cells lining capillary buds
surrounded by a single layer of pericytes expressing smooth m
buds and slit-like vascular spaces. (C) Higher magnification of
tion. IHC. Bars, (A) 150 mm, (B) 30 mm, (C) 35 mm.
The present series represents the first primary
documentation of canine and feline arteriovenous
haemangioma and demonstrates the similarity of
these lesions to those of man with respect to prev-
alence, location, clinical presentation and microscop-
ical features (Barrett and Speight, 2000; Calonje
and Fletcher, 2007). Marked intermittent haemor-
rhage without an obvious initiating cause is often
n of smooth muscle actin. (A) Arterial- (thick arrow) and venous-
n their wall. Note the irregular thickness of the muscle of the largest
(two arrowheads) and slit-like vascular spaces (one arrowhead) are
uscle actin. (B) Higher magnification of the aggregate of capillary
the vascular wall of the venous-type structure and capillary forma-
134 S. Schöniger et al.
associated with human arteriovenous haemangiomas
(Barrett and Speight, 2000; Calonje and Fletcher,
2007) and was also observed in cases 1 and 3 of this
series.
The microscopical hallmark of arteriovenous
haemangioma is the proliferation of thick- and thin-
walled vascular structures with occasional arteriove-
nous anastomoses (Requena and Sangueza, 1997;
Barrett and Speight, 2000; Calonje and Fletcher,
2007). Arteriovenous haemangiomas may also con-
tain additional vascular elements such as capillary
and cavernous formations (Barrett and Speight,
2000; Calonje and Fletcher, 2007). The tumours of
this series generally lacked mitotic activity, with the
exception of occasional mitoses associated with the en-
dothelial cells forming capillary structures and slit-
like vascular spaces in case 3. Scattered mitoses may
also be observed in capillary haemangiomas in cats
and dogs (Gross et al., 2007a) and man (Calonje
and Fletcher, 2007).
The canine lingual tumour (case 3) reported here
involved themusculature of the tongue. This distribu-
tion is comparable with the variant of human hae-
mangioma termed intramuscular haemangioma
(Weiss and Goldblum, 2001; Calonje and Fletcher,
2007). These tumours are considered benign, as they
are well-delineated and lack morphological and cyto-
logical features of malignancy (Weiss and Goldblum,
2001). Although in case 3 the tumour had separated
muscle fibres, this was not considered indicative of
malignancy and the lesion was diagnosed as an arte-
riovenous haemangioma partially involving the lin-
gual musculature.
Some authors classify human arteriovenous hae-
mangiomas according to the depth of tissue involve-
ment as superficial and deep variants (Calonje and
Fletcher, 2007). Superficial arteriovenous haeman-
giomas usually arise in older adults and may be
associated with chronic liver diseases such as chronic-
active hepatitis and hepatic cirrhosis (Akiyama and
Inamoto, 2001). The deep variant commonly affects
adolescents and young adults, is located in the head
and neck area and at the extremities, and likely
represents a congenital vascular malformation
(Calonje and Fletcher, 2007). Although haemangio-
mas are classified as benign neoplasms, some types
of haemangiomas likely represent reactive vascular
hyperplasia or vascular malformations (Gross et al.,
2007a). Thus the distinction between neoplastic
and non-neoplastic vasoformative proliferations of
this type is blurred. Arteriovenous malformations
commonly show an initial quiescent phase followed
by a progressive growth phase, which is related to
the onset of the clinical symptoms (Garzon et al.,
2007).
The canine and feline cutaneous arteriovenous hae-
mangiomas of the present series (cases 1 and 2) were
located superficially within the dermis and affected
animals were older adults without evidence of liver
disease. The clinical history of case 1 was particularlyinteresting due to the possible association between tu-
mour development and thrombosis of the cephalic
vein. An association between repeated episodes of in-
travascular thrombosis and recanalization and the
development of spindle cell haemangioma in man
has been noted (Gross et al., 2007a). In addition,
trauma or arterial embolism can trigger the progres-
sive phase of clinically silent arteriovenous malforma-
tion (Garzon et al., 2007).
The lingual tumour (case 3) was diagnosed in
a middle aged Greyhound and involved the muscula-
ture of the tongue. Such deep tissue involvement may
suggest a congenital lesion; however, invasion of deep
tissue during the progressive phase of human arterio-
venousmalformation is reported (Garzon et al., 2007).
Lingual haemangioma has been reported previously
in a 7-month-old Jack Russell Terrier (Schoofs,
1997), an 11-year-old Spaniel (Van der Gaag et al.,
1989) and a 2.5-year-old Siamese cat (Crow et al.,
1981). Similar to case 3 from this series, the Jack Rus-
sell Terrier and the Siamese cat presented with recur-
rent oral haemorrhage. In the Jack Russell Terrier,
the lingual haemangioma was composed of cystic
spaces lined by endothelium (Schoofs, 1997). The tu-
mour in the Spaniel was identified as capillary hae-
mangioma (Van der Gaag et al., 1989) and the
feline tumour was consistent with a combined cavern-
ous and capillary haemangioma (Crow et al., 1981).
The present series, therefore, provides the first de-
scription of canine lingual arteriovenous haeman-
gioma.
The main differential diagnoses for the three cases
reported here were arteriovenous malformation and
glomangioma, a subtype of glomus tumours. As indi-
cated, the designations arteriovenous haemangioma
and malformation are often used for similar lesions,
since the precise differentiation between an acquired
and congenital arteriovenous tumour-like lesion is dif-
ficult (Calonje and Fletcher, 2007; Garzon et al.,
2007). Whilst the microscopical appearance of the
present lesions may have suggested a vascular malfor-
mation, the presentation of these three cases as focal
masses in mature animals would favour the interpre-
tation that they were benign neoplasms. An arteriove-
nous malformation has been reported in the spinal
cord of an 8-year-old German Shepherd dog charac-
terized by the presence of arterial- and venous-type
structures together with smaller vessels including
capillaries (Hayashida et al., 1999). Despite the simi-
lar appearance of the lesions described in the present
Arteriovenous Haemangioma in Two Dogs and a Cat 135
series, these have been classified as arteriovenous hae-
mangiomas in accordance with current literature
(Calonje and Fletcher, 2007; Gross et al., 2007a).
Glomus cells are bland, rounded cells that cluster in
association with the vascular wall. Glomus tumours
arise from modified smooth muscle cells that form
the glomus body, which represents a specialized
type of arteriovenous anastomosis. Gomangiomas
are variants of glomus tumours in which neoplastic
glomus cells surround vascular structures (Galofaro
et al., 2006; Calonje and Fletcher, 2007). Glomus
tumours are rare neoplasms of man (Calonje and
Fletcher, 2007) and dogs and cats (Galofaro et al.,
2006; Gross et al., 2007b). The vascular proliferations
described in the present series lacked glomus cells and
comprised vascular structures with somewhat aber-
rant features.
In conclusion, this communication reports three ar-
teriovenous haemangiomas located in the skin of one
dog and one cat and in the tongue of a dog. Although
these tumours are rare in dogs and cats, they should
be included as a differential diagnosis for vascular
proliferations in these species.
Acknowledgements
The authors thank the histopathology laboratories at
the Royal Veterinary College, London and Cornell
University, Ithaca for their excellent technical sup-
port.
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½ RA
eceived, January 11th, 2008ccepted, May 16th, 2008
 �
	Arteriovenous Haemangioma in Two Dogs and a Cat
	References