194 DISC

Veterinary Dermatology 2000, 11, 299304

Case report
Two cases of cutaneous T cell lymphoma in Friesian
cows in the Azores
MARIA C. PELETEIRO, 1 CARLOS PINTO, 2 JORGE J. CORREIA, 1 JOSE F. SILVA 1 and
SANDRA BRANCO 1
1

Anatomia Patologica, DEMOC, Faculdade de Medicina Veterinaria, Rua Gomes Freire 1199 Lisboa
Codex, Portugal,
2
Servico de Desenvolvimento Agrario de S. Miguel, 9500 Ponta Delgada, Azores
(Received 10 March 1997; accepted 22 July 1999)

Abstract This paper presents two cases of cutaneous neoplasia in Friesian cows, on the island of S. Miguel,
Azores. The lesions consisted of raised pink plaques, with no pruritus or signs of associated pain, that were
extensively distributed over both lateral and ventral body surfaces. The histological examination of the
material obtained by skin biopsy or post-mortem suggested a T cell lymphoma with extensive epidermal
inltration. The lymph nodes showed extensive invasion by tumour cells. The results of
immunocytochemistry, which were the same for the tumour cells in the skin and in the lymph node, were
positive for CD3, conrming the T cell origin of the tumour cells. It was concluded that these were cases of T
cell lymphoma, involving both skin and lymph nodes. Although there have been other reports of cutaneous
lymphosarcoma in the literature, these are the rst cases identied in the Azores.
Keywords: cow, histopathology, immunocytochemistry, lymphoma, skin disease.

INTRODUCTION
Cutaneous lymphoma or lymphosarcoma in cattle is
referred to in the literature as comprising two
dierent forms of the disease: skin lesions developing
as a consequence of a systemic lymphoma in animals
positive to the bovine leukaemia virus (BLV), in
which the skin is secondarily invaded, or primary
lymphomas that originate in the skin, which generally
have no involvement of the internal organs for most
of the course of the disease.14 The second situation is
very rare and is known as the `skin form' of
lymphosarcoma. It is classied as a form of sporadic
bovine leukosis, not associated with BLV, and is most
frequently found in young animals up to their third
year of life. Some authors refer to cases of apparent
recovery of skin lymphosarcoma, followed by relapse
after a few months.24
Cutaneous lymphosarcomas are described as nonepitheliotropic or epitheliotropic, according to the
degree of epidermal involvement, the second being
the rarer.5 Epitheliotropic tumours, in most species,
are usually primary to the skin and conned to it
and the supercial lymph nodes, in contrast with
nonepitheliotropic tumours, which appear more
like multicentric lymphomas eventually spreading
to the skin.5
Correspondence and reprints: Maria C. Peleteiro
# 2000 Blackwell Science Ltd

Enzootic bovine lymphomas are considered to

be of B cell origin6 but in sporadic bovine leukosis
the neoplastic cells can develop from either B or T
cells lineages.7
As far as the authors could determine, there are
few reports of attempts to characterize of the type of
lymphocyte involved in cutaneous lymphosarcoma in
cattle.8,9 In those published reports the cells identied
were T lymphocytes.
CASE REPORT
The present cases occurred in Friesian cows, in the
Island of S. Miguel, Azores. There cattle are kept
mainly for milk production and the animals stay in
the eld all year round without shelter.
The rst case was diagnosed in a two year old
heifer. The clinical history before the animal was
presented to the authors was the following: the rst
lesions were seen in August 1995 as raised pink
plaques, 45 cm in diameter, distributed all over the
body surface. The rst diagnosis was of an allergic
process or a dermatomycosis and treatment was with
a nonsteroidal anti-inammatory drug (phenylbutazone; Phenylarthrite, Vetoquinol) and a topical
fungicide and acaricide (clotrimazol formulated with
undecylenic acid and lindane; Pulsana, Cyanamid).
The animal was 8 months pregnant. No improvement
was noted following the treatment and, once the
299

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M. C. Peleteiro et al.

animal had given birth, an intramuscular systemic

treatment with dexamethasone (Dexa-Tomanol, Essex-Schering-Plough), phenylbutazone (Phenylarthrite, Vetoquinol) and an antibiotic (amoxycillin;
Clamoxyl LA, Smithkline Beecham) was applied,
again with no success. The general health of the
animal throughout this period remained good.
It was after this, in October 1995, that the animal
was referred to the Servico de Desenvolvimento
Agrario de S. Miguel.
By that time, the lesions were much more extensive,
practically covering the whole body surface, showing
in some cases supercial erosion or even ulceration.
Nodules could be seen surrounding the anus and the
vulva and in the ventral aspect of the base of the tail.
On the left shoulder was an exophytic bright red
nodule (Fig. 1). There were no signs of pruritus and
palpation appeared painless.
An excisional skin biopsy of one of the lesions was
then performed and samples were collected for fungal
identication. About one week after the biopsy was
performed, a generalized enlargement of the supercial lymph nodes was noted. Apart from this, the
general condition remained good with no signs of
weight loss.
Following the result of the biopsy it was decided to
euthanize the animal. At necropsy no lesions were

found in the organs except for a variable degree of

lymph node enlargement, especially of the supercial
ones. Further samples of skin were sent for examination, together with material from the supercial
inguinal lymph node, liver and kidney.
The second case was also in a two year old Friesian
cow that was imported from France in January 1998,
two months before the rst skin lesions were observed.
These consisted of dispersed raised plaques, a few
centimetres in diameter, distributed all over the body
surface (Fig. 2). These plaques bled easily but the
animal showed no signs of pain or obvious discomfort. There was swelling of the supercial inguinal
lymph node. On the head, some circular areas of
alopecia covered with tightly adherent greyish crust,
were present, suggesting ringworm. The general
condition was reasonably good and the appetite
normal, although there were signs of weight loss.
Skin biopsy was performed at two dierent locations and sent for histological examination. Material
from the skin of the head was collected for fungal
identication. Blood analysis was also performed.
Following the results of the biopsy that conrmed
skin lymphoma, the owners decided to euthanize the
animal, which they did without veterinary assistance.
It was therefore impossible to perform post-mortem
examination or collect more material.

Figure 1. First case. Cutaneous lesions, one of which shows as an

exophytic and bosselated bright red nodule.

Figure 2. Second case. Cutaneous lesions showing as raised

plaques

# 2000 Blackwell Science Ltd, Veterinary Dermatology, 11, 299304

194 DISC
Cutaneous T cell lymphoma in Friesian cows
Histopathology and immunocytochemistry
All the material collected for histopathological
examination was xed in 10% buered formalin,
embedded in paran wax and stained by haematoxylin/erythrosin.
The identication of the lymphoid cells, both in the
skin and in the lymph node, was made with the rabbit
polyclonal antibody antihuman T cell antigen CD3,
from Dako.
The sections were mounted on slides covered with
poly L-lysine. The immunolabelling was performed
by the streptavidin/biotin/peroxidase technique, the
material having been submitted to proteolytic digestion with trypsin (0,1% solution with 0,1% of
calcium chloride, pH 7,8, for 15 min at 37 8C).
Specicity controls were performed in the usual way,
using nonimmune rabbit serum in place of the
primary rabbit anti-CD3. For positive control of
the T cell marker, sections of normal dog lymph node
were used.
In the rst case, the histopathological examination
of the material collected by excisional biopsy,
corresponding to a nonulcerated area of the skin,
revealed the presence of multiple and extensive sheets
of neoplastic cells with a lymphoid appearance,
heavily inltrating the dermis and also the epidermis
(Fig. 3). The epidermal inltration of the lymphoid
cells was irregular, eventually reaching the stratum
corneum, but remaining contained by a thin sheet of
keratin. Sometimes the tumour cells accumulated in
bullae formed by separation of epidermal layers. The
same was found in the examination of the skin
samples sent after slaughter.
The neoplastic lymphoid cells were large, with
large pale nuclei of irregular contour, interspersed
with some small normal lymphocytes. Apart from a
high nucleus/cytoplasm ratio, they showed a variable
number of conspicuous nucleoli, sometimes up to
three, located close to the nuclear membrane. The

301

number of mitoses was high. Although packed

against each other in some areas, the tumour cells
also showed a more loose arrangement in other parts
of the aected skin.
The inguinal lymph node showed a heavy inltration of lymphoid cells with the same characteristics
identied for skin.
No signicant lesions were found in the histopathological examination of the liver or kidney.
In the second case the lesions were very similar,
although covered by a thick crust that was missing in
the rst case. The neoplastic cells invaded the deep
dermis and also showed signs of epidermal invasion
and bullae formation (Fig. 4). Their cytologic
characteristics were identical to the cells of the rst
case, showing a high nucleus/cytoplasm ratio.
The results of the immunocytochemical labelling of
the neoplastic cells in both cases were positive for
CD3, which identied them as T lymphocytes. The
staining was very marked in the cytoplasm of the
neoplastic cells in the skin in both cases (Fig. 5) and
in the inguinal lymph node in the rst case. The
results of the CD3 labelling in the dog lymph node
clearly showed brown staining of the cytoplasm of
the lymphocytes in the internodular and the deep
cortices and no labelling of the cells of the germinal
centres of the lymphoid follicles. No labelling was
identied in the specicity controls.
Microbiological results
Direct observation of the material sent for microbiological analysis revealed fungal elements in both
cases. The cultural examination identied Trichosporon cutaneum and Candida famata in the rst case
and Trichophyton verrucosum in the second one.
Haematology results
The following were obtained from the second case:
Erytrocytes, 4,4261012 L71

Figure 3. First case. Subepidermal

and epidermal inltration of
lymphoid cells, reaching the stratum
corneum. They accumulate in bullae
formed by the separation between
epidermal layers. They also show a
big nucleus/cytoplasm ratio and a
variable number of conspicuous
nucleoli (H & E, 6400).
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M. C. Peleteiro et al.

Figure 4. Second case. Subepidermal

and epidermal inltration of lymphoid
cells forming bullae between epidermal
layers (H & E, 6400).

Figure 5. First case. Neoplastic

lymphoid cells inltrating the
epidermis positive to CD3 antigen
(rabbit antihuman T cells antigen
CD3, DAB, 6400).1

Leukocytes, 15,76109 L71

Platelets, 3,986109 L71
P.C.V., 21,1%
Haemoglobin, 4,2 mmol L71
The leukocytes series was as follows (including
percentage distribution):
Neutrophils, 77%12,0896109 L71
Lymphocytes, 17%2,6696109 L71
Monocytes, 6%0,9426109 L71
Eosinophils and Basophils, 0%
DISCUSSION
Neoplasia is very frequently diagnosed in cattle in the
islands of the Azores, comparatively more than on
the Portuguese mainland.10 The explanation for this
is as yet undetermined, although the frequent presence of toxic plants like bracken fern (Pterydium
aquilinum) and lantana, together with the year round
# 2000 Blackwell Science Ltd, Veterinary Dermatology, 11, 299304

exposure to actinic radiation and the photosensitization processes that follow, might help explain the large
number of tumours. According to the same authors, in
a total of 223 neoplasms diagnosed in cattle from July
1989 to July 1994, 37 were skin tumours, representing
16.6% of the total. In the second part of the previously
mentioned study, the classication of the skin tumours
in cattle was presented, including only one case of
cutaneous lymphoma, the rst described in detail in
the present work.11
In fact, the `skin form' of lymphosarcoma in cattle,
so frequently diagnosed in companion animals,
including horses, is rarely reported in the literature.
Furthermore, the immunocytochemical identication
of the lymphoid cells involved in cutaneous lymphosarcoma in cattle has seldom been performed.
Zwahlen et al. described a case very similar to the
ones presented here.8 The lymphoma observed was
also of the epitheliotropic type and the tumour cells
were identied by immunocytochemistry as T cells of

194 DISC
Cutaneous T cell lymphoma in Friesian cows
the helper/inducer type (CD4 +). In another work
concerning the dierentiation analysis of sporadic
bovine leukosis cells, it was concluded that T cells
from the calf and skin types were more highly dierentiated cells than the ones from the thymic type.9
In the present cases, the neoplastic cells formed cell
aggregates in the epithelium identical to the microabcesses of Pautrier described in human mycosis
fungoides12 and in T cell lymphomas in the dog.1316
in human mycosis fungoides the T cell subsets
identied belong to the helper type and the same
was found in the already mentioned case of bovine
cutaneous lymphosarcoma studied by Zwahlen et al.8
In contrast, Moore et al. concluded that, in dogs,
mycosis fungoides was a proliferative disease of
suppressor/cytotoxic CD8 + cells.14
The positive CD3 staining obtained in the cytoplasm of neoplastic cells in the cases presently
described was not a surprise, due to their tendency
for epithelial invasion. According to the manufacturer's information, the rabbit antihuman CD3 antibody used is anity isolated and immunization is
performed with the synthetic peptide from the
intracellular part of the e-chain of human CD3
coupled to bovine thyroglobulin. This antibody is a
pan-cell marker and cross reacts with T-cells in many
animal species,17 which makes it particularly useful
for veterinary pathology diagnosis. The positive
control used in this work demonstrated the specicity
of the antibody for dog T cells because it positively
marked the areas where these cells concentrate in the
lymph node and, contrarily, was negative in the
typical B cell areas.18 The choice of dog lymph node
instead of cow was due to its availability, but also
because, according to the manufacturer's information, the reaction of the CD3 antibody to both cow
and dog T cells is strong.
Two types of fungi were identied on mycological
culture of the rst case (Trichosporon cutaneum and
Candida famata). However, they seem to have acted
opportunistically, probably complicating the primary
lesions, as they are yeasts normally present on skin.19
In fact, Trichosporon spp. causes minimal hair damage
and does not elicit any host reaction, except in cases of
immunosuppressed patients.20 Trichophyton verrucosum, isolated in the second case, is commonly
identied in cases of skin mycosis in cattle.21 It is the
author's belief that the neoplasia could have acted as a
factor favouring the clinical expression of the mycotic
lesions due to immunosupression.
The haematological results of the second cow
revealed some deviation from the normal blood
values,22 In particular slight anaemia and leucocytosis. Although the percentage distribution of lymphocytes is very low, the total number of these cells
does not seem to have been aected.
Concluding, both cases described above correspond to the general description of the `skin form' of
lymphosarcoma in cattle, both in respect to age of the
aected animals and to the clinical course of the

303

disease.14 Therefore, these were considered to be

cases of sporadic BLV negative bovine leukosis. Up
to the present, no cases of enzootic bovine leukosis
have ever been detected in the Azores during the
ocial campaigns undertaken by the sanitary authorities. However, cattle imports from Europe are
frequent in the islands, which makes introduction of
BLV possible. The fact that immunocytochemical
identication of T cells neoplasia is feasible in skin
biopsies, suggests it is an eective tool which could be
used to support the diagnosis of sporadic as opposed
to enzootic leukosis, not only in cases of cutaneous
lymphosarcoma, but also when applied to lymph
nodes or other tissues accessible to biopsy, in many
cases of bovine lymphosarcoma.

ACKNOWLEDGEMENTS
The authors wish to thank: Sector de Micologia do
Laboratorio de Sanidade Animal da Direccao dos
Servicos de Sanidade Animal e Higiene Publica
Veterinaria, Azores, for the mycological identication; the Servico de Patologia Morfologica, Instituto
Portugues de Oncologia Dr Francisco Gentil, Lisboa,
for the immunocytochemical identication of the
neoplastic cells in the rst case. And nally, Maria do
Rosario Lu s for her technical assistance and Prof.
Michael Pugh for the English correction of the draft.

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Resume Cet article decrit deux cas de neoplasie cutanee chez des vaches frisonnes, sur l' le de S.Miguel,
Acores. Les lesions consistaient en des plaques roses, sans prurit ou douleur, localisees au niveau des faces
laterales et ventrale du corps. L'examen histopathologique de prelevements obtenus par biopsie cutanee ou
post-mortem etait en faveur d'un lymphome T avec une inltration epidermique massive. Les noeuds
lymphatiques etaient massivement envahis par des cellules neoplasiques. Les resultats de l'examen
immunohistochimique, identiques pour les cellules tumorales cutanees et ganglionnaires, ont montre un
marquage par le CD3, qui a conrme l'origine lymphocytaire T des cellules neoplasiques. Il a donc ete conclu
qu'il s'agissait de deux cas de lymphome T, avec une atteinte de la peau et des ganglions. Bien que d'autres cas
de lymphosarcome aient deja ete rapportes dans la litterature, il s'agit des premiers cas decrits aux Acores.
[Peleteiro, M. C., Pinto, C., Correia, J. J., Silva, J. F., et Branco, S. Two cases of cutaneous T cell lymphoma
in Friesian cows in the Azores. (Deux cas de lymphome T cutane chez des vaches Frisonnes dans les Acores.)
Veterinary Dermatology 2000; 11: 299304.]
Resumen Este art culo presenta dos casos de linfoma cutaneo de celulas T en vacas Frisonas, en la isla de S.
Miguel, Azores. Las lesiones consist an en placas rosadas elevadas, sin prurito o signos de dolor asociado, que
se distribu an de forma extensa en las areas laterales y ventrales del tronco. El estudio histologico del material
obtenido por biopsia cutanea o de forma post-mortem suger an un linfoma de celulas T con inltracion
epidermica amplia. Los ganglios linfaticos mostraban una amplia invasion por celulas neoplasicas. Los
resultados de la inmunocitoqu mica, que fueron los mismos para las celulas del tumor y del ganglio linfatico,
fueron positivos para CD3, conrmando el origen en celulas T de las celulas tumorales. Se concluyo que estos
eran casos de linfoma de celulas T, involucrando tanto la piel como los ganglios linfaticos. Aunque existen
otros informes de linfosarcoma cutaneo en la bibliograf a, estos son los primeros casos identicados en las
Azores. [Peleteiro, M. C., Pinto, C., Correia, J. J., Silva, J. F., e Branco, S. Two cases of cutaneous T cell
lymphoma in Friesian cows in the Azores. (Dos casos de linfoma cutaneo de celulas T en vacas Frisonas en las
Azores.) Veterinary Dermatology 2000; 11: 299304.]
Zusammenfassung Es werden zwei Falle kutaner Neoplasie bei Friesischen Kuhen auf der Insel St. Miguel
der Azoren prasentiert. Die Eoreszenzen bestanden in erhabenen, pinkfarbenen Plaques ohne Pruritus oder
Zeichen von Schmerz, die weit verteilt uber der ventralen und den lateralen Korperoberachen vorkamen. Die
histologische Untersuchung des durch Hautbiopsie bzw. postmortalen Sektion gewonnenen Gewebes
entsprach der eines T-Zelllymphoms mit hochgradiger, epidermaler Inltration. Die Lymphknoten zeigten
eine hochgradige Inltration mit Tumorzellen. Die Immunhistochemie, die fur die Zellen in der Haut und in
den Lymphknoten identisch waren, zeigte ein CD3-positives Resultat, welches die T-Zellidentitat der
Tumorzellen bestatigte. Es wurde daraus geschlossen, da es sich hierbei um Falle von sowohl Haut als auch
Lymphknoten betreenden T-Zelllymphomen handelte. Obwohl bereits andere Berichte kutaner
Lymphosarcomata in der Literatur existieren, sind dies die ersten Falle, die in den Azoren identiziert
wurden. [Peleteiro, M. C., Pinto, C., Correia, J. J., Silva, J. F., und Branco, S. Two cases of cutaneous T cell
lymphoma in Friesian cows in the Azores. (Zwei Falle von kutanem T-Zelllymphom bei Friesischen Kuhen in
den Azoren.) Veterinary Dermatology 2000; 11: 299304.]
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