DOI: 10.1111/j.1365-3164.2009.00793.
Canine cutaneous epitheliotropic T-cell lymphoma:
a review of 30 cases
Jacques Fontaine*, Marianne Heimann† and
Michael J. Day‡
*Faculté Vétérinaire de l’Université de Liège, Service de Médecine
Interne des Petits Animaux – Dermatologie, Batiment 44, 20 Bd de
Colonster, B-4000 Liège, Belgium
†
Institut de Pathologie et Génétique ⁄ Bio.be, 25 av Georges Lemaı̂tre
6041, Gosselies, Belgium
‡
Division of Veterinary Pathology, Infection and Immunity, School of
Clinical Veterinary Science, University of Bristol, Langford BS40 5DU,
UK
Correspondence: Jacques Fontaine, Faculté Vétérinaire de l’Univer-
sité de Liège, Service de Médecine Interne des Petits Animaux – Der-
matologie, Batiment 44, 20 Bd de Colonster, B-4000 Liège, Belgium.
E-mail: jacques.fontaine@ulg.ac.be
Conflict of Interest
No conflicts of interest have been declared.
Sources of Funding
We thank the Institut de Recherche Scientifique and the Institut de
Pathologie et Génétique that provided funding for the immunohisto-
chemical study.
Abstract
This retrospective study reviewed the clinical,
histological and immunohistochemical features of 30
European cases of canine cutaneous epitheliotropic
T-cell lymphoma (CETL). The clinical presentation
was highly variable and was not associated with the
disease subtype. Diffuse erythema (86.6%) with scal-
ing (60%) and focal hypopigmentation (50%) were
the most common lesions. The skin was uniformly
involved but muco-cutaneous junctions or mucosae
were affected in 50% of cases. The median age at
diagnosis was 10 years (SD 2.79, range 4–15) and the
median time between onset and final diagnosis was
5 months (SD 3.79, range 0–12). Five cases occurred
in Bichon Frises. There was no evidence of a previous
history of chronic dermatitis in any cases. Histologi-
cally, the follicular epithelium was affected in 86.7%
of cases. One case with mainly follicular disease was
considered folliculotropic mycosis fungoides (MF),
but no follicular mucinosis was observed. Epidermal
Pautrier’s microabscesses were uncommon (23.3%).
Sweat glands were infiltrated in 70% of cases. Immu-
nohistochemistry confirmed T-cell neoplasia in all
cases. B cells infiltrated as individual cells or formed
linear bands or ectopic follicles at the base of the neo-
plasm. Ki67 labelling revealed a range of proliferation
indices but did not correlate with severity. A final
diagnosis of classical MF was made in 40% of the
dogs, MF d’emblé in 36.7%, generalized Pagetoid reti-
culosis in 20% and localized Pagetoid reticulosis in
one case (Woringer–Kolopp Pagetoid reticulosis). The
median survival time after diagnosis was 6 months
ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.
and this did not change appreciably with therapy
(lomustine or prednisolone).
Accepted 13 May 2009
Introduction
Canine cutaneous epitheliotropic T-cell lymphoma
(CETL) is an uncommon neoplastic condition of
unknown aetiology.1–3 It is characterized by infiltration
of neoplastic T lymphocytes with a tropism specific to
the epidermis and adnexal structures.1,2,4 Using criteria
described in humans,5–7 canine CETL can be divided
into two types: mycosis fungoides (MF) and the Sézary
syndrome. Using the latest human classification, MF
may be divided into several subtypes: classical Alibert–
Bazin MF, folliculotropic MF and Pagetoid reticulosis
(PR). Although two clinical forms of Pagetoid reticulosis
have been described [a localized form (Woringer–Kolopp
type) and a generalized form (Ketron–Goodman type)],
the European Organization for Research and Treatment
of Cancer (EORTC) has recently recommended that the
term Pagetoid reticulosis be used only for the localized
form.5,6 The generalized form has distinct clinical behav-
iour and should be classified as aggressive epidermo-
tropic CETL or a tumour stage of MF. Folliculotropic
MF is characterized by the presence of follicular epithe-
lial infiltrates, usually with sparing of the epidermis.5,6
Most cases also show mucinous degeneration of the
hair follicles. The previous subtype MF ‘d’emblé’ is no
longer recognized by the EORTC.5,6 Using immunophe-
notypic markers, many of these cases can be classified
as various types of non-MF T-cell lymphoma or even B-
cell lymphoma. The recognition of these subtypes is
important, as their behaviour can vary from indolent
(localized PR), to intermediate (classical MF) to aggres-
sive (Sézary).
In dogs, the clinical presentation of CETL is highly
variable and the disease can mimic many dermato-
ses.1,2,8,9 Dogs usually present with a recent history of
chronic dermatitis10 and muco-cutaneous junctions or the
oral mucosa may sometimes be affected. Involvement of
other organs can be observed in the late stages of the
disease. English cocker spaniels and boxers appear to be
predisposed.9,11–18 It has proved difficult to characterize
CETL subtypes based on cutaneous signs, and Pagetoid
reticulosis and Sézary syndrome are very rarely
documented in the veterinary literature.12,19 The classifi-
cation scheme proposed by Scott et al.2 may be a better
approach to describing the clinical presentation of CETL
in the dog. This scheme defines the following clinical
267
Fontaine et al.

subtypes: exfoliative erythroderma, plaque(s) ⁄ nodule(s), immunolabelling and the slides were then counter-stained with hae-
ulcerative disease of the oral mucosa and a muco-cutane- matoxylin. The 30 cases were finally categorized as to subtype of
CETL. The proliferation index was evaluated by counting the posi-
ous form. In general, the prognosis for dogs with CETL is
tively labelled cells per 1000 stromal cells within the area of the
poor. The mean survival time after diagnosis is reported tumour that contained the highest number of Ki67 positive cells on
to range from a few months to 2 years.2,5,16,20 light microscopic examination.
The diagnosis must always be confirmed by histopath- The statistical analysis of the results was performed by the
ological examination of skin biopsy specimens. Histology Department of Biostatistics at the University of Liège veterinary
also permits the pathologist to subtype the CETL. During school. A Kruskal–Wallis test was chosen to analyse the treatment
early stages of the disease, the histological differentiation efficacy (abnormal distribution of three samples but having the same
distribution).
from non-neoplastic lymphocytic dermatoses can be diffi-
cult.1,12,20,21 CETL is characterized by cutaneous infiltra-
tion of neoplastic lymphocytes showing a variable degree Results
of epitheliotropism that may involve the epidermis and ad-
Clinical presentation
nexae. The lymphocytes are of variable size (ranging from
Thirty cases were collected from the files. The estimated
20 to 30 lm) and often have an indented nucleus or irreg-
prevalence of CETL over a 5-year period in one referral
ular nuclear contour. There is generally scant eosinophilic
practice (JF) was seven per 1000 dogs referred for der-
cytoplasm, although rare cases may display abundant
matological disease. For cases observed at the veterinary
pale amphophilic cytoplasm. In contrast to inflammatory
faculty at the University of Liège the prevalence was two
processes, there is no destruction of the adnexae,
per 1000 dermatological consultations.
although progressive obliteration may be seen. A range of
Cutaneous epitheliotropic T-cell lymphoma was
secondary changes including hyperkeratosis, spongiosis,
observed in 18 different pure breeds and seven cross-
apoptosis, acanthosis or melanosis may be observed.
bred dogs. The disease was observed in five Bichon fries
The dermis, despite the presence of a severe leukocytic
and two Bouvier des Flandres, but the remaining pure
infiltrate, does not show fibrosis or the neoangiogenesis
breeds were represented only once. Fourteen cases
that may accompany chronic lymphocytic dermatitis.1
were male (two neutered) and 16 female (eight neutered)
The aim of the present study was to retrospectively
and the median age at the time of diagnosis was 10 years
review the clinical and histological aspects of 30 cases of
(SD 2.79, range 4–15). The median time between the
CETL to add to the relatively sparse European data on this
onset of first lesions until the final diagnosis of CETL was
disease and to define further the diagnostic features of
3.8 months (range 0–12 months). For 25 cases, a long
this neoplasm.
clinical history was available and in no case was chronic
dermatitis reported prior to the earliest onset of CETL.
Materials and methods The types of lesions observed (Figures 1–5) were ery-
Cases of CETL were retrospectively selected from the files of four
thema (86.6%, n = 26), plaques (73.3%, n = 22) erosions
dermatology referral practices. These cases were selected on the (60%, n = 18), scales (60%, n = 18), nodules (53.3%,
basis of the classical clinical presentation, clear supportive histologi- n = 16), hypopigmentation (50%, n = 15), crusts (46.6%,
cal findings and long-term clinical follow-up (in the majority of cases n = 14) and alopecia (33.3%, n = 10). Involvement of the
until death). A range of historical data was collected, including time mucosa was observed in 50% (n = 15) of the cases
between the first onset of lesions and the diagnosis of CETL, pres-
(Table 1). Using Scott et al.’s classification,2 pure exfolia-
ence of pruritus (graded as 1 = mild, 2 = moderate and 3 = intense)
tive erythroderma was observed in 6.6% (n = 2), pure
and interaction with other skin diseases. Characterization and distri-
bution of clinical lesions were studied. The treatments administered patch ⁄ plaque presentation in 13.3% (n = 4), pure nodular
and responses to therapy were reviewed, including the survival time form in 6.6% (n = 2), pure muco-cutaneous form (muco-
if available. cutaneous junction) in 10% (n = 3) and ulcerative disease
For all cases, the original skin biopsies [stained by haematoxylin of mucosa (without any skin lesion) in 3.3% (n = 1). Over-
and eosin (H&E), periodic acid Schiff (PAS) and Giemsa] were lap of different stages was frequently noted: a mixed
reviewed microscopically by the same pathologist (MH), using crite-
ria reported in the veterinary literature1,2,8,11,15,17 modified according
to the current model used in human medicine (Table 4).22–24 Serial
sections were also subjected to immunohistochemistry in order to
phenotype the neoplastic lymphoid cells. Primary antisera specific to
the T-cell marker CD3 (clone F7.2.38, dilution 1 ⁄ 50; Dako Belgium
Interleuvenlaan, Heverlee, Belgium) and for the B-cell marker CD79a
(clone HM57, dilution 1 ⁄ 200; Dako) were employed. Immunolabelling
for expression of the proliferation marker Ki67 (clone MIB-1, dilution
1 ⁄ 100; Dako) was also performed to allow a better evaluation of the
proliferative activity of the neoplastic cells. These cross-reactive anti-
sera have been widely validated for the dog and are now routinely
used for pathological diagnosis in this species and in our laboratory.15
Briefly, sections were pretreated with citrate buffer (pH 6.0) for
40 min at 90 C. The slides were then treated according to the manu- Figure 1. Epitheliotropic lymphoma in a Bichon fries dog (case 30).
facturer’s data sheets. For the detection of the CD3 and CD79a mole- This breed was over-represented in the present study and exfoliative
cules, the slides were incubated for 30 min at room temperature erythroderma was the predominant presentation in these dogs. The
with Envision Polymer reagent (Dako) and, for Ki67, the Streptavidin– right panel shows a close-up view of the dorsal aspect of the
Biotin 2 system (LSAB2; Dako) was used. The chromogen 3,3¢-diam- head. The inset shows focal loss of pigmentation associated with
inobenzidine (DAB; Dako) was used for the visualization of the erythroderma of the planum nasale.

268 ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.

Figure 2. Ventral abdomen of a 10.5-year-old Bouvier des Flandres
dog (case 14) showing the formation of plaques ⁄ patches characteris-
tic of epitheliotropic lymphoma. The inset shows the lesions
observed at the genital muco-cutaneous junction.
Figure 3. 8-year-old mongrel dog (case 23) with localized Pagetoid
reticulosis (Woringer–Kolopp form) showing hypopigmentation and
erythema of the muzzle at the time of diagnosis (right) and
36 months later (left). There is minimal progression of the lesions
over that time.
presentation of exfoliative erythroderma and patches ⁄ pla-
ques was observed in 6.6% (n = 2); patches ⁄ plaques and
nodules were observed in 6.6% (n = 2). Association of
exfoliative erythroderma and nodular forms was never
observed. The remaining 14 cases (46.6%) had more
complex clinical presentations with concurrent presence
of all lesion types (Table 2). These complex clinical pre-
sentations did not correlate with the duration of disease
or the prognosis (no reduction in the survival time).
Muco-cutaneous lesions (Table 3) were frequently
observed (15 of 30 dogs). In seven cases, only a single
muco-cutaneous junction was affected, and this was
most often the naso-buccal junction (six cases). Overall,
the naso-buccal junction was affected in 13 of 30 dogs.
Lesions of the oral cavity were observed affecting the gin-
giva, the tongue or the hard and ⁄ or soft palate (macula to
plaques, diffuse infiltration to ulcerations).
The majority of the cutaneous lesions were dissemi-
nated over the trunk (83.3%; n = 25) or localized to the
ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.
Epitheliotropic T-cell lymphoma in dogs
Figure 4. Erosion and haemorrhage of the oral mucosa and muco-
cutaneous junction in a 12-year-old Bichon fries dog (case 6) with
epitheliotropic lymphoma.
Figure 5. A 12-year-old, cross-bred dog (case 1) with the Pagetoid
form of epitheliotropic lymphoma. The dog has extensive truncal
alopecia that correlates with the marked tropism of neoplastic
lymphocytes for follicular epithelium seen histologically.
head (63%; n = 19), especially the nasal region (43%;
n = 13). The footpad (often at the junction of the footpad
and the skin) was affected in 26.6% of the cases (n = 8),
with presence of crusts, depigmentation and sometimes
ulceration.
Pruritus was observed in 40% of the cases. If present,
the mean pruritus intensity (graded from 1 to 3) was 1.83
(SD 0.94, range 1–3).
Lymph node enlargement was observed in six cases.
Nodal involvement did not correlate with a more chronic
stage of the disease as the mean time of onset of the
lesions until the diagnosis of lymph node enlargement
was 4.2 months (SD 2.73, range 1–8). These enlarged
lymph nodes were not aspirated or biopsied; so, the
nature of the enlargement was not further characterized.
Routine haematological and serum biochemical exam-
inations were performed in 12 dogs (by three different
laboratories), and in none was any significant abnormality
noted. No additional data concerning other diagnostic pro-
cedures that may have been performed were available.
Therapy was attempted in 14 of 30 cases. In six dogs,
prednisolone (1 mg ⁄ kg per day until reduction in the signs
and then classical alternate day therapy) was prescribed.
CCNU or lomustine [1-(2-chloroethyl)-3-cyclohexyl-1-nitr-
osoure] chemotherapy was employed in eight cases at
60–70 mg ⁄ m2 every 3 weeks25,26 (median 64.4 mg ⁄ m2).
The survival time was difficult to determine accurately
because of lack of precise information, but for the 18
dogs evaluated a median survival time of 6 months was
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Fontaine et al.

Table 1. Summary of clinical lesions (%) documented in comparison epithelial infiltration with minimal dermal reaction) was
with a published case series diagnosed in 23.3% of cases (n = 7) (Figure 6a,c). On the
Fontaine et al.3 Beale et al.9 basis of the normal haematological results, we consider
(Belgium) (USA) that none of the dogs in the present series had Sézary
Erythema 86.6 80.8 syndrome. One case (case 28) was considered as a follic-
Plaques 73.3 61.5 ulotropic subtype of MF.
Erosion ⁄ ulceration 60 42.3 The lymphocytes were of variable size, ranging from
Scaling 60 61.5 small (<20 lm) to medium (20–30 lm) or large (>30 lm),
Nodules 53.3 57.7
and often had a convoluted nucleus. Most neoplastic cells
Hypopigmentation 50 Not available
had scant eosinophilic cytoplasm, although rare cases
Crusting 46 38.5
Mucosal lesions 50 38.5 had abundant pale amphophilic cytoplasm. There was no
Pruritus 40 38.5 destruction of the adnexa, although progressive oblitera-
tion was seen in some biopsies. Secondary changes
including hyperkeratosis, spongiosis, apoptosis, acantho-
Table 2. Distribution of clinical forms of CETL in the dogs of this sis or melanosis of the epithelium were sometimes
series observed. There was no evidence of dermal neo-
Pure forms Mixed forms
angiogenesis. Dermal fibrosis was rarely observed and
always associated with localized inflammation and B-cell
Exfoliative 2 Exfoliative erythroderma + 2
infiltration.
erythroderma patches ⁄ plaques
Patches ⁄ plaques 4 Patches ⁄ plaques + Nodules 2
The neoplastic lymphocytes were CD3+ in all cases
Nodule(s) 2 Exfoliative erythroderma + 0 (Figures 6b and 7b). There was infiltration of CD79a+ B
nodule(s) lymphocytes at the base of the T-cell infiltrates in nine
Muco-cutaneous form 3 All forms concurrently 14 cases (30%). The number of B cells varied greatly
Ulcerative disease of 1 amongst the cases and within different biopsies taken
mucosa from any one case. The B cells showed no morphological
atypia and were of small mature lymphocyte type. The
reported (SD 5.22, range 1–24 months). Most dogs were presence of these B lymphocytes correlated mostly with
euthanized, but this took place at different stages nodular or plaque tumour lesions. B lymphocytes had ten-
depending on the tolerance of the owners. The median dency to concentrate at the base of the neoplastic infil-
survival times after diagnosis for dogs treated with trate, forming linear bands or occasionally ectopic
lomustine (n = 7), with prednisolone (n = 6) or without lymphoid follicles. Rare cells infiltrated the neoplasm, but
treatment (n = 5) were 6 (SD 1.82, range: 6–10); 4.25 (SD none were observed within the epidermis or adnexae.
8.69, range 1–24) and 3 months (SD 3.43, range 2–10) Plasma cells accompanied the B cells in variable propor-
respectively. One case of localized Pagetoid reticulosis tions. In four cases (cases 2, 17, 19 and 21), the B cells
was still alive at the time of writing. This dog was treated predominated at the periphery of the tumour forming a
with five cycles of lomustine at two different treatment lichenoid infiltrate within the superficial dermis surround-
intervals (10 total cycles) with no evidence of disease ing the mass. In those areas, mild cicatricial fibrosis was
progression 2.5 years after the initial diagnosis. occasionally observed.
The proliferating cells labelled by the Ki67 antiserum
Histopathological and immunohistochemical varied in number and pattern from case to case. Cases
findings with a low proliferative index (up to 9%) with a diffuse dis-
The microscopical changes noted within biopsies of tribution of proliferating cells throughout the lesion were
lesional tissue from these dogs are summarized in observed (Figure 6d). These cases had a mild cellular infil-
Table 4. Epitheliotropism was observed in all cases. The tration, often limited to the epidermis, or sometimes a
follicular epithelium was generally affected in 86.7% of Pagetoid distribution (cases 1, 2, 6, 8, 10, 16, 26, 28 and
cases (n = 26). In 46.7% of cases (n = 14), there was 29). In cases with high proliferative index (30–61%) the
greater infiltration of the dermis than the epithelium. In positively labelled cells were diffusely distributed within
40% of samples (n = 12), the epithelium was more the neoplastic infiltrate (Figure 7a). These cases had intra-
affected than the dermis. In 13.3% of cases (n = 4), the epithelial or intradermal neoplastic infiltration (cases 3, 9,
lymphocytic infiltrate was strictly intraepithelial. 12–15, 18–20, 23 and 27). Another specific pattern was
The most frequent pattern observed, in 40% of cases characterized by proliferation at the base of the tumour
(n = 12), was that of classical MF (resembling human (cases 5, 12, 17, 22 and 30) or multifocal proliferation
Alibert–Bazin MF). Cases with a dominant dermal infiltra- (cases 7, 11 and 25) with a variable proliferation index.
tion are often described as having ‘mycosis fungoides Some animals showed variation in the pattern of Ki67
d’emblé’, and this histological presentation was observed labelling that was dependent upon the lesion biopsied or
in 36.7% (n = 11). Pagetoid reticulosis (Pagetoid the type of infiltration observed (mild intraepithelial or

Table 3. Lesions affecting the muco-cutaneous junction(s)

Number of muco-cutaneous junctions 1 2 3 4
affected in the same dog 23.3% (n = 7) 13.3% (n = 4) 10% (n = 3) (3 .3% (n = 1)
Muco-cutaneous junctions affected Lips ⁄ nasal junction (n = 13) Anal junction (n = 5) Genital junction (n = 6) Eyelids (n = 4)

270 ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.
 Epitheliotropic T-cell lymphoma in dogs

Table 4. Summary of major histopathological features

Epidermis Dermal involvement
Lymphocytic infiltration: single cell ⁄ diffuse 93.3 Involvement of apocrine sweat glands 70.0
Lymphocytic aggregation 66.7 Apocrine sweat glands obliterated 26.7
Pautrier’s microabcessation 23.3 Involvement of sebaceous glands 56.7
Localization to basal epidermis 50.0 Sebaceous glands obliterated 23.3
Panepidermal localization 33.3 Dermal fibrosis 3.3
Pagetoid infiltration 23.3

Size of epidermal lymphocytes Size of dermal lymphocytes

Large >30 lm 26.7 Large >30 lm 30.0

Medium 20–30 lm 80.0 Medium 20–30 lm 60.0
Small <20 lm 43.3 Small <20 lm 33.3
Mixed large ⁄ medium 23.3 Mixed large ⁄ medium 20.0
Mixed medium ⁄ small 26.7 Mixed medium ⁄ small 23.3
Mixed large ⁄ medium ⁄ small 3.3 Mixed large ⁄ medium ⁄ small 6.7

Other epidermal changes Follicular involvement

Spongiosis 43.3 Focal involvement of isthmus 80.0

Apoptosis 6.7 Pan-folliclular (nodular effect) 6.7
Acanthosis 70.0
Dermo-epidermal obliteration 26.7
Pigmentary incontinence 10.0
All values are given as percentage. Pautrier’s microabscess is defined as at least four atypical lymphocytes in a single intraepidermal space.36

plaque or nodular). Often the B-cell population that
accompanied the T-cell lymphoma was also proliferative
and this was taken into account when evaluating the
proliferation index.
Discussion
The prevalence of CETL described in the northern Euro-
pean patient populations in this study (0.2–0.7%) is
greater than that reported in published investigations
elsewhere, but may reflect the fact that this study was of
referral populations.3 The number of dogs of the Bichon
fries breed affected was also unexpected, despite the
fact that this breed is well represented in the local
canine population (Bichons born in Belgium during 2007
comprised 0.88% of the newly registered canine popula-
tion, data from LOSRH [livre des origines Société Royal
St Hubert (Belgian Kennel Club)]; Bichons in France
comprise 3.6% of the canine population, data from the
LOF [livre des origines Française (French Kennel Club)]).
For case series documented in the literature,9–18 it would
appear that the English cocker spaniel and boxer may be
predisposed to CETL, but there was only one cocker
spaniel and one boxer in our study population.
As is also reported in the literature, no gender predispo-
sition was observed in this series. The mean age at the
time of diagnosis (9.8 years) was similar to that derived
from the published data (8.6 years). 3 The fact that this
disease is difficult to diagnose is also confirmed by the
fact that the mean time between first onset of lesions
until final diagnosis was 5.4 months (from 0 to
12 months). One case was diagnosed very early during a
routine vaccination consultation. The dog had a small
plaque localized on the lip and the owners had noted that
this had been present for only a few weeks.
A relationship between previous chronic dermatitis
(especially atopic dermatitis; AD) and CETL has been
suggested to occur in humans and dogs.9,10,13,27,28
Recently, Santoro et al. suggested a possible association
between AD and CETL in dogs.29 In that study, the odds
of developing CETL were 12 times higher in dogs with
AD than in dogs without AD. In our study, the complete
clinical history was available in 25 cases and in none of
those dogs was there a previous report of chronic derma-
titis.
The clinical presentation of CETL is highly variable and
the disease can mimic many inflammatory dermatoses.
The most challenging aspect of diagnosis is identification
of the disease at an early stage. Diffuse erythema
(86.6%) with scales (60%) and focal hypopigmentation
(50%) are the most suggestive lesions.
This highly variable clinical presentation in dogs sug-
gests that this disease in dogs does not closely mimic the
human counterpart. For example, generalized erythroder-
ma, which is common as an early manifestation in dogs,
is considered as a hallmark of late-stage presentation in
affected humans.5,6 Another distinct difference between
the canine and human disease is the frequent involve-
ment of muco-cutaneous junctions or mucosae in dogs
(50% of the cases).3
The clinical classification system proposed by Scott et
al.2 (outlined above) was not readily applicable to many
animals in the present study because in the majority of
cases, several or all of the individual forms were observed
in the same animal. Some clinical patterns may neverthe-
less be breed associated, as we observed in the Bichon
fries in which exfoliative erythroderma was predominant.
The final diagnosis and the subtype identification must
always be based on microscopic examination of skin
biopsy specimens. The most characteristic lesion,
common to all forms of CETL, is the tropism of neoplastic
cells for epithelium. The follicular epithelium was often
affected in dogs of this series (86.7%). The classical
aggregation of T lymphocytes forming microabscesses
(Pautrier’s microabscesses Figure 7b) was uncommon
(23.3% of cases). Reduced epitheliotropism with progres-

ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275. 271
Fontaine et al.
(a) (b)
(c) (d)
(a) (b)
sive invasion of the dermis was not observed as it is usu-
ally reported in the human disease.22
A range of other cutaneous changes was observed
microscopically. Spongiosis was often present (43%) but
is difficult to interpret as this is also a prominent feature
of most other types of nonspecific inflammatory dermati-
tis.1 Individual keratinocyte apoptosis was rarely
observed (6.7%). This observation could help to distin-
guish between CETL and erythema multiforme (EM) in
which keratinocyte apoptosis is a hallmark feature.
Involvement of adnexal glands was often observed in
the dogs of this series, with involvement of apocrine
sweat glands in 70% and of sebaceous glands in 56.7%.
Complete obliteration of apocrine sweat glands (26.7%)
and sebaceous glands (23.3%) was also recorded.
The size of lymphocytes infiltrating the epithelium var-
ied between cases. Lymphocytes of medium size were
observed in 80% of cases as has been previously
reported,1,4,13,17,26,30 but in more than 50% of cases the
population was not homogenous with a mixture of cell
sizes recorded. Fewer cases had a dominance of
272 ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.
Figure 6. Skin from case 1 showing
changes consistent with the Pagetoid form
of epitheliotropic lymphoma. Quadrant (a)
(H&E, bar = 175 lm) and (c) (H&E, bar =
75 lm): the infiltration of neoplastic lym-
phocytes is restricted to the epidermis and
follicular epithelium; there is prominent
hyperkeratosis. Quadrant (b) (CD3, bar =
50 lm): the lymphocytes show cytoplasmic
labelling with the T-cell marker. Quadrant
(d) (Ki67, bar = 80 lm): a low number of
neoplastic cells have positive nuclear label-
ling (arrows) with Ki67, illustrating a low-
to-moderate mitotic activity.
Figure 7. Skin from case 25 with epithelio-
tropic lymphoma. Quadrant (a) (bar =
75 lm): immunohistochemical labelling for
expression of Ki67 demonstrates the high
mitotic activity of epitheliotropic lympho-
cytes. Quadrant (b) (bar = 50 lm): labelling
for CD3 expression confirms that these are
epitheliotropic T cells forming Pautrier’s
microabscesses (arrowed).
medium-sized lymphocytes within the dermal infiltrates
(60%). This variation in lymphocyte size impedes the abil-
ity of the pathologist to differentiate between a clonal pro-
liferation of neoplastic T cells and a reactive lymphoid
population. The use of the pan-T-cell marker CD3 facili-
tates the analysis of lymphoid infiltration but does not
help in the differentiation between neoplastic and reac-
tive cells. Such discrimination may have been assisted by
polymerase chain reaction assessment of T-cell receptor
clonality, but such testing is currently unavailable in
Europe and was not employed at the time of diagnosis of
these cases.
As observed in human patients,31 in nine of our cases,
a B-cell population was present as individual cells within
the tumour or as a linear band at the base of the neoplas-
tic T-lymphocyte infiltrate within the dermis. Follicular for-
mation was also sometimes seen and a variable number
of plasma cells were associated with the infiltrating B
cells. Such a reaction is believed to be due to the produc-
tion of cytokines such as interleukin-4 and B-cell stimulat-
ing factor-2 by the neoplastic T lymphocytes.31 There was

no significant difference in the behaviour of the tumour
when there was an accompanying B-cell infiltrate, but the
B-cell infiltrate was only observed in cases with nodule
and plaque formation.
The study of the proliferation index of the neoplastic
cells revealed several distinct patterns. Some tumours
had a low proliferation index (<9%), while others were
characterized by a high proliferative activity (30–61%).
The remainder (between 9% and 30%) was considered
as having intermediate proliferative activity.
Most cases with low proliferation index were poorly
cellular MF with infiltration of the neoplastic cells limited
to the epithelia. Some exclusively intraepithelial tumours
had high mitotic index.
The distribution of the proliferating cells could be diffuse
throughout the tumour, intra-epithelial and intradermal, or
multifocal. In five cases, the proliferating cells were
located at the base of the tumour. This pattern varied
between different biopsies taken from the same patient.
As detailed above, the Ki67 index in these cases was
determined by evaluation of areas of each biopsy in which
the greatest amount of labelling was observed. The pur-
pose of this approach was to ensure that the most consis-
tent measurement was made between individual tissue
samples. Despite this, no correlation between the KI 67
index and time to diagnosis was observed. The KI 67 index
was not, furthermore, predictive of the survival time.
A final diagnosis of classical MF was made in 40% of
cases (n = 12) cases in the present series. Surprisingly,
MF d’emblé was commonly observed (36.7%; n = 11).
This presentation could be a late stage of MF (tumour
form) or a specific form (spontaneous form dermal-
oriented recognized as an aggressive lymphoma in
humans). For the MF d’emblé cases, the median time
before diagnosis was 4.3 months. In comparison with
the overall median time before diagnosis (5 months), it
appears that these cases do not take a longer time to
develop. The mean survival time (7 months) was only
available for five of these d’emblé cases but did not sig-
nificantly differ from the overall survival time for the
entire series (6.3 months). It would therefore appear that
canine MF d’emblé is not a late stage of MF (tumour
form) nor a more aggressive subtype as it is now consid-
ered to be the case in humans.
Generalized Pagetoid reticulosis (Ketron–Goodman
form) was diagnosed in six of 30 cases and localized
Pagetoid reticulosis (Woringer–Kolopp Pagetoid reticulo-
sis) in one case. In human Pagetoid reticulosis, the
lesions typically affect the distal extremities.23,32 It has
been suggested that in canine Pagetoid reticulosis, the
footpad may be more commonly affected, with the pres-
ence of crusts, hypopigmentation and ulceration.1,2 In
the present series it was not possible to clinically distin-
guish PR from MF. Pedal lesions appeared not to be
specific to canine Pagetoid reticulosis. Canine Pagetoid
reticulosis is rarely documented in the literature,10,11,33
but when reported, it seems similar to the human vari-
ant of disseminated Pagetoid reticulosis or Ketron–Good-
man Pagetoid reticulosis.1,11 If we were to adopt the
recent EORTC classification,5,6 we would suggest using
the term PR only for the localized form and Ketron–
Goodman CETL for the other forms. Only one case with
ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275.
Epitheliotropic T-cell lymphoma in dogs
a single, isolated, slowly progressing plaque has been
described in the dog.11 We report here a second case of
Woringer–Kolopp Pagetoid reticulosis. As it is in
humans, these localized cases could reflect the pres-
ence of a distinct disease process.32 In our case, there
was no apparent progression of the signs more than
36 months after the diagnosis was made.
One case was considered as a folliculotropic subtype
of MF and in all other cases follicular infiltration was a
continuation of infiltration of the epidermis. Follicular
mucinosis was not observed in these cases. Systemic
involvement appears to be very rare in the dog, and in this
series we only observed lymph node enlargement in six
cases. No case of Sézary syndrome was recorded in our
dogs, but only a single case of canine Sézary syndrome
has been clearly documented in the literature.12
The prognosis for dogs with CETL is generally consid-
ered to be poor. In our series the median survival time
after diagnosis in 18 cases was 6 months (range 1–
24 months). The case of localized PR was not considered
in determining this survival time because the affected
dog was still alive at the time of writing. The mean sur-
vival time after diagnosis of CETL reported in the litera-
ture ranges from a few months to 2 years.2,9,20 The
prognosis for canine MF is surprisingly different to that
for the human disease. In humans, the 5-year survival for
MF is 88% and for PR is 100%.5,6 These observations
could be related to the type of T lymphocytes involved in
the disease. In human MF, 90% of the tumour cells are
CD4+, but in the canine disease 80% of the cells are
CD8+. The prognosis for canine CETL is similar to that of
human Ketron–Goodman CETL, which is also a CD8+
T-cell proliferation. Unfortunately, as this was a retro-
spective study, we had no fresh-frozen tissue samples to
permit immunolabelling for canine CD4 and CD8.
Many treatment protocols for CETL have been
reported,34 with the large number attesting to the fact
that none has good efficacy.2,34 In our cases, treatment
was only documented in 14 of 30 cases. Although this
number is relatively low for a statistical analysis, a Krusk-
all–Wallis test revealed that the survival time after diag-
nosis was not significantly (P = 0.209) different between
treated and untreated dogs, or between different treat-
ment modalities. In two recent retrospective studies of
dogs with CETL, an overall response rate of 78–83%
was quoted,26,35 although survival times were not
reported. Despite the absence of significant improve-
ment in survival time in our cases there was always a
clinical improvement which improved the quality of life.
Conclusion
The present study confirmed that the clinical presentation
of CETL is highly variable. The classification proposed by
Scott et al.2 may be used to characterize the signs pres-
ent but not to define a specific type of disease as, in the
majority of cases, several or all forms can be present in
the same animal. Despite this, the present series
included six dogs with Ketron–Goodman CETL and one
dog with Woringer–Kolopp PR. The histological diagnosis
may be challenging in early cases, but the key feature is
single cell or diffuse lymphocytic infiltration of the epithe-
273
Fontaine et al.

lium. In this series, the follicular epithelium was often
affected but epidermal Pautrier’s microabscesses were
uncommon. Apocrine sweat glands were also frequently
involved. The prognosis for canine CETL is poor. The
median survival time after diagnosis was 6 months and
this did not change appreciably with therapy. Labelling
with the pan-T-cell marker CD3 facilitates the analysis of
lymphoid infiltration. CD79a and Ki67 are not helpful as
predictive factors of clinical severity or survival time.
Acknowledgements
We express our gratitude to Jean-Louis D’argent for his
help in reviewing some slides, and helping with us to
understand the human counterpart of this complex
disease. D’argent also kindly reviewed the manuscript.
We also thank Frederic Farnir for his assistance in the
statistical analysis of our data. This work has been made
possible, thanks to Hill’s Pet Nutrition who supported
the position of J. Fontaine at the Faculty of Veterinary
Medicine of the University of Liège, Belgium.
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Résumé Cette étude rétrospective a passé en revue les dispositifs cliniques, histopathologiques et
immuno-histochimiques de 30 cas européens de lymphome cutané épithéliotrope canin (CETL). La présen-
tation clinique était hautement variable et n’était pas associée au sous-type de la maladie. Erythème diffus
(86.6%), squamosis (60%) et hypopigmentation focale (50%) étaient les lésions les plus fréquentes. La
peau était uniformément atteinte mais les jonctions cutanéo-muqueuses et les muqueuses étaient
atteintes dans 50% des cas. L’age moyen de diagnostic était de 10 ans (SD 2.79, range 4 – 15) et la durée
moyenne entre le début et le diagnostic final était de 5 mois (SD 3.79, range 0 – 12). Cinq cas ont touchés
des bichons frisés. Dans aucun des cas il n’y avait d’anamnèse de dermatite chronique. Histologiquement,
l’épithélium folliculaire était atteint dans 86.7% des cas. Un cas avec une maladie essentiellement follicu-
laire a été considéré comme un mycosis fongoı̈des (MF) folliculotrope mais aucune mucinose folliculaire
n’a été observée. Les microabcès de Pautrier épidermiques étaient rares (23.3%). Les glandes sudoripares
étaient infiltrées dans 70% des cas. Les lymphocytes T néoplasiques ont été confirmés par immunohisto-
chimie dans tous les cas. Les cellules B infiltraient en tant que cellules isolées ou formaient des bandes
linéaires ou des follicules ectopiques à l’origine de la tumeur. Le marquage Ki67 révélait une gamme
d’index de prolifération mais pas de corrélation pas avec la sévérité. Un diagnostic final de MF classique a
été posé pour 40% des chiens, de MF d’emblée dans 36.7% des cas, de réticulose pagétoı̈de dans 20% et
de réticulose pagétoı̈de localisée dans un cas (Woringer-Kolopp Pagetoid reticulosis). La durée de survie
moyenne après diagnostic était de 6 mois et ne changeait pas avec la thérapie (lomustine ou prednisolone).

Resumen Este estudio retrospectivo revisa las caracterı́sticas clı́nicas, histológicas e inmunohistoquı́mi-
cas de 30 casos de linfoma epiteliotrópico cutáneo canino (CETL). La presentación clı́nica fue variada y no
estaba asociada con el subtipo de la enfermedad. Eritema difuso (86,6%), con descamación (60%) e
hipopigmentación focal (50%) fueron las lesiones mas comunes. La piel estaba siempre afectada, pero las
uniones mucocutáneas y las mucosas solo se afectaron en un 50% de los casos. La edad media al tiempo
de diagnostico fue de 10 años (desviación estándar 2.79, rango 4-15) y el tiempo medio entre la aparición de
lesiones y diagnostico final fue de cinco meses (desviación estándar 3,79, rango 0-12). Cinco casos ocurrier-
on en perros de raza Bichon Frise. No habı́a evidencia de historia previa de dermatitis crónica en ninguno de
los casos. Histológicamente el epitelio folicular se afecto en un 86,7% de los casos. Un caso con enferme-
dad fundamentalmente folicular fue considerado micosis fungoides foliculotropica (MF) pero no se observo
mucinosis folicular. Microabscesos epidermales de Pautrier fueron poco comunes (23,3%). Las glándulas
apocrinas estaban infiltradas en un 70% de los casos. La inmunohistoquı́mica confirmó que eran linfocitos
T en todos los casos. Linfocitos B infiltraban como células individuales o formando bandas o folı́culos ectóp-
icos en la parte basal de la neoplasia. El marcaje con ki-67 reveló un rango variado de ı́ndices proliferativos
que no se correlacionó con la severidad. Un diagnostico final de MF clásica fue dado en un 40% de los per-
ros, MF d’emblé en un 36,7%, reticulosis generalizada Pagetoide en un 20% y reticulosis Pagetoide localiz-
ada en un caso (reticulosis Pagetoide de Woringer-Kolopp). El tiempo medio de supervivencia tras el
diagnostico fue de 6 meses y no cambió apreciablemente con el tratamiento (lomustina o prednisolona).

Zusammenfassung Diese retrospektive Studie stellt eine Review der klinischen, histologischen und
immunhistochemischen Charakteristika bei 30 europäischen Fällen von caninem kutanem epitheliotropen
Lymphom (CETL) dar. Die klinische Präsentation war sehr variabel und wurde nicht mit dem Subtyp der
Krankheit in Verbindung gebracht. Ein diffuses Erythem (86,6%) mit Schuppenbildung (60%) und fokaler
Hypopigmentierung (50%) waren die häufigsten Veränderungen. Die Haut war immer betroffen, während
die mukokutanen Übergänge oder die Schleimhäute in 50% der Fälle betroffen waren. Das mediane Alter
zum Zeitpunkt der Diagnose war 10 Jahre (SD 2,79; Range 4-15) und die mediane Zeit vom Beginn bis zur
endgültigen Diagnose betrug 5 Monate (SD 3,79; Range 0-12). Fünf Fälle betrafen Bichon Frises. Bei kei-
nem der Fälle bestand die Anamnese einer chronischen Dermatitis. Histologisch war bei 86,7% der Fälle
das follikuläre Epithel betroffen. Ein Fall mit hauptsächlich follikulärer Erkrankung wurde als follikulotrope
Mycosis fungoides (MF) bezeichnet, wobei keine follikuläre Muzinose beobachtet wurde. Epidermale
Pautrier¢s Mikroabszesse waren selten (23,3%). In 70% der Fälle waren die Schweißdrüsen infiltriert.
Mittels Immunhistochemie wurde in allen Fällen eine T-Zell Neoplasie bestätigt. B-Zellen infiltrierten als
individuelle Zellen oder formten lineare Bänder oder ektopische Follikel an der Basis der Neoplasmen. Die
Markierung von Ki67 zeigte eine Spannweite an Proliferationsindizes, stimmte aber nicht mit der Schwere
überein. Bei 40% der Hunde wurde klassische MF als endgültige Diagnose gestellt. MF d¢emblé wurde bei
36,7% der Hunde, eine generalisierte Pagetoide Retikulose bei 20% und eine lokalisierte Pagetoide Retiku-
lose (Woringer-Kolopp Pagetoide Retikulose) in einem Fall diagnostiziert. Die mediane Überlebenszeit nach
der Diagnose betrug 6 Monate und wurde durch Therapie (Lomustine oder Prednisolon) nicht erheblich
beeinflusst.

ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 267–275. 275