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Follicular Mycosis Fungoides, a Distinct Disease Entity With or Without Associated Follicular Mucinosis
A Clinicopathologic and Follow-up Study of 51 Patients
Remco van Doorn, MD;
Erik Scheffer, MD;
Rein Willemze, MD;
for the Dutch Cutaneous Lymphoma Group
Arch Dermatol. 2002;138:191-198.
ABSTRACT
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Objective To determine the clinicopathologic features and the disease course of
patients with follicular mycosis fungoides (MF).
Design A multicenter, 14-year, retrospective cohort analysis.
Setting Dutch Cutaneous Lymphoma Group.
Patients Fifty-one patients with the clinicopathologic features of follicular
MF with (n = 49) or without (n = 2) associated follicular mucinosis. Follow-up
data were compared with those of 158 patients with the classic epidermotropic
type of MF, including 122 patients with generalized plaque-stage MF (T2 N0
M0) and 36 patients with tumor-stage MF (T3 N0 M0).
Observations Characteristic clinical features not or rarely observed in classic MF
were the preferential localization of the skin lesions in the head and neck
region (45 of 51 patients), the presence of follicular papules, alopecia,
acneiform lesions, mucinorrhoea, and often severe pruritus. Characteristic
histologic findings were the presence of perifollicular neoplastic infiltrates
with a variable degree of folliculotropism, but generally no epidermotropism,
follicular mucinosis (49 of 51 cases), and often a considerable admixture
of eosinophils and plasma cells. Response on initial treatment, risk of disease
progression (development of extracutaneous disease and/or death from lymphoma),
and disease-specific and overall survival of patients with follicular MF were
worse than in classic MF patients. The actuarial disease-specific survival
was 68% at 5 years and 26% at 10 years.
Conclusions Follicular MF shows distinctive clinicopathologic features, is more
refractory to treatment, and has a worse prognosis than the classic type of
MF; it should be considered a distinct type of cutaneous T-cell lymphoma.
Based on these results and those of other studies, we suggest the term follicular MF for cases with or without associated follicular
mucinosis.
INTRODUCTION
MYCOSIS fungoides (MF) is the most common type of cutaneous T-cell lymphoma,
characterized clinically by an indolent clinical course with the subsequent
evolution of patches, plaques, and tumors, and histologically by the infiltration
of the epidermis by medium-sized to large atypical T cells with cerebriform
nuclei.1
In the first 10 years after diagnosis, disease progression, including
development of extracutaneous disease and disease-related deaths, occurs in
only a minority of patients.2 Apart from this
so-called classic Alibert-Bazin type of MF, many clinical and histologic subtypes
have been reported, including hypopigmented, vesicular, pustular, granulomatous,
and other types of MF. Since these variant types of MF have the same clinical
course and clinical behavior and require the same therapeutic approach as
the classic type of MF, they are generally not considered separate entities.
In both the EORTC (European Organization for Research on the Treatment of
Cancer)1 classification for primary cutaneous
lymphomas and in the WHO (World Health Organization) classification,3 only pagetoid reticulosis and MF-associated follicular
mucinosis have been categorized as separate entities. Hereinafter, the latter
condition will be referred to as follicular MF, a
term also used in the WHO classification for cases with or without associated
follicular mucinosis.
Follicular MF has been classified as a separate entity because it has
distinctive clinical and histologic features, is more refractory to standard
treatment, and has a worse prognosis than classic MF. However, this observation
is particularly based on clinical experience of members of the classification
committee of the EORTC Cutaneous Lymphoma Group and is not substantiated sufficiently
in the literature. In fact, published reports on follicular MF are relatively
scarce, generally concern case reports or small series of patients, and have
mainly been focused on differentiation between MF-associated follicular mucinosis
and alopecia mucinosa, the benign idiopathic form of follicular mucinosis.4-9
In a recent study by members of our group2
on 309 patients with MF, the 32 patients with follicular MF seemed to have
significantly higher disease progression and mortality rates than the 277
patients without follicular mucinosis. These observations prompted us to review
all cases of follicular MF registered at the Dutch Cutaneous Lymphoma Group
between 1985 and 1998.
PATIENTS AND METHODS
Between October 1985 and December 1998, 57 patients with follicular
MF were included in the registry of the Dutch Cutaneous Lymphoma Group. Three
of the 57 had to be excluded from the present study, 1 because of incomplete
follow-up data and 2 because of lack of representative skin biopsy specimens.
Another 3 patients were excluded because they had a history of classic epidermotropic
MF for 4 to 7 years before they developed skin tumors on the face with the
histologic features of MF-associated follicular mucinosis. The final study
group consisted of 51 patients. In each patient the diagnosis had been made
by an expert panel of dermatologists and pathologists at one of the quarterly
meetings of the Dutch Cutaneous Lymphoma Group. The main criteria for diagnosis
and for inclusion in the study were the presence of perifollicular-to-diffuse
dermal infiltrates with variable numbers of atypical T cells with cerebriform
nuclei infiltrating the follicular epithelium and the presence of mucinous
degeneration of the follicular epithelium, as confirmed by Alcian blue staining
of the first diagnostic biopsy specimens (diagnostic specimens).6-7
Forty-nine patients met both criteria. Two cases with the same cytoarchitectural
features in the diagnostic specimen but without associated follicular mucinosis
were included as well. The time of evaluation of the first diagnostic specimen
was considered the time of diagnosis.
In all cases diagnostic evaluation at the time of diagnosis consisted
of a thorough physical examination, complete blood cell count, serum chemistry
studies, and skin specimen evaluation. Lymph node biopsies and thoracic and
abdominal computed tomographic scans were performed only in patients with
enlarged peripheral lymph nodes. Lymph node involvement was assessed using
criteria described previously.10 When indicated
clinically, additional studies to determine visceral involvement were performed.
In all cases clinical records and follow-up data, which had been collected
yearly, were evaluated. The following variables were recorded: age; sex; duration
of skin lesions before diagnosis; type of initial therapy; whether there was
a complete remission after initial therapy; the date of disease progression
if applicable; and the date of last contact (or death if applicable). Because
of difficulties in defining skin stage in patients with follicular MF, disease
progression was defined by the development of histologically documented nodal
involvement in patients with previously skin-limited disease, the development
of visceral involvement in patients with prior skin and/or lymph node involvement,
and death due to lymphoma. In all cases, one or multiple skin biopsy specimens
obtained at the time of diagnosis, and in most cases also obtained during
follow-up, were reviewed.
To evaluate differences in clinical behavior between follicular MF and
classic MF, 49 patients with follicular MF presenting with disease confined
to the skin were compared with 158 patients with classic MF included in an
earlier study.2 This latter group included
122 patients with generalized plaque-stage MF (T2 N0 M0) and 36 patients with
tumor-stage MF (T3 N0 M0) without evidence of extracutaneous disease and without
associated follicular mucinosis at the time of diagnosis.
Actuarial survival curves were calculated from the date of diagnosis
to the date of last contact (or the date of death) using the Kaplan-Meier
technique. Differences between survival and disease progression curves were
analyzed using the log-rank test. Univariate analysis of possible prognostic
factors was performed using the log-rank test and Cox proportional hazards
regression analysis. Patients lost to follow-up were considered censored at
the time of last contact. Analyses were performed using the SPSS statistical
software (SPSS Inc, Chicago, Ill).
RESULTS
CLINICAL CHARACTERISTICS
The main clinical features and relevant follow-up data have been summarized
in Table 1. Fifty-one patients,
including 42 male and 9 female, were included in this study. Four (8%) of
51 patients were younger than 40 years at the time of diagnosis. At the time
of diagnosis, 49 patients (96%) had disease confined to the skin, including
4 patients with enlarged but histologically uninvolved lymph nodes, whereas
1 patient had concurrent lymph node involvement and another, concurrent visceral
involvement.
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Table 1. Clinical Characteristics and Follow-up Data of 51 Patients
With Follicular Mycosis Fungoides*
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At the time of diagnosis, 34 of 51 patients had only patches, plaques,
or (grouped) follicular papules, often associated with alopecia; 14 had (concurrent)
nodules or tumors; and 3 had erythroderma (Figure 1). Acneiform lesions, including comedolike lesions and epidermal
cysts, were a prominent feature in 4 patients. Mucinorrhea (ie, discharge
of mucinous substance from the follicular orifices) was noted in 3 patients.
During the course of their disease, 2 patients developed a leonine face (Figure 2). In 45 of 51 patients, the skin
lesions were preferentially localized in the head and neck region at the time
of diagnosis. A characteristic finding in 25 of these 45 patients was the
presence of plaques or tumors on the head or neck, whereas the trunk and extremities
showed only patches or slightly infiltrated plaques and/or grouped follicular
papules (Figure 1A-B). Infiltrated
plaques in the eyebrows with concurrent alopecia were a common finding. Most
patients had moderate to severe pruritus.
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Figure 1. Clinical appearances of follicular
mycosis fungoides. A, Boggy infiltrates on the cheek and neck; B, concurrent
grouped follicular papules on the trunk; C, Infiltrated plaque with alopecia
and cystic lesions above the left eye; D, the same patient had numerous cysts
and comedolike lesions on the trunk; E, Diffuse erythema and alopecia of the
eyebrows (and eyelashes, not shown); F, Infiltrated plaque on the forehead
with alopecia of the left eyebrow.
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Figure 2. Sequential photographs of a 39-year-old
man with follicular mycosis fungoides. A, At the time of diagnosis; B, 26
months after diagnosis with a leonine face; C, 29 months after diagnosis;
and D, 35 months after diagnosis following total skin electron beam irradiation,
which had not resulted in complete remission. The patient died of lymphoma
42 months after diagnosis.
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HISTOLOGIC FEATURES
A total of 74 representative skin biopsy specimens from these 51 patients
were reviewed. These included the 51 diagnostic specimens, 8 prediagnostic
specimens obtained 4 to 30 months (median, 12 months) prior to diagnosis,
and 15 specimens obtained during follow-up at the time of relapse or disease
progression. Characteristically, the diagnostic specimens showed perifollicular
and perivascular-to-diffuse dermal infiltrates with variable infiltration
of the follicular epithelium by medium-sized to large atypical T cells with
cerebriform nuclei (Figure 3). Pautrier
microabscesses appeared in only a minority of specimens. Infiltration of the
interfollicular epidermis by (atypical) T cells, as in classic MF, was rare.
Only 5 of 51 specimens showed infiltration of both the epidermis (epidermotropism)
and the follicular epithelium (folliculotropism). Prominent infiltration of
the eccrine sweat glands was observed in 3 specimens. In all but 2 cases,
the skin specimens showed mucinous degeneration of the hair follicles, varying
from focal spots of mucin deposition (which had to be searched for in serial
sections) to lakes of mucin (Figure 3B).
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Figure 3. Characteristic histologic features
of follicular mycosis fungoides. Perifollicular infiltrates with marked folliculotropism
and associated follicular mucinosis. A, Note the absence of epidermal involvement.
B, Alcian blue staining of a concurrent lesion showing mucin deposits. C,
Detail of perifollicular infiltrate of part A showing atypical hyperchromatic
T cells, blast cells, and admixed histiocytes and eosinophils.
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The number of atypical T cells infiltrating the follicular epithelium
was generally low and did not correlate with the amount of mucin deposition.
The perifollicular infiltrates consisted of variable numbers of medium-sized
to large atypical T cells with cerebriform nuclei and blast cells and admixed
small lymphocytes, histiocytes, eosinophils (which were numerous in 13 of
51 specimens), and plasma cells, in particular in patients with secondary
bacterial infection (Figure 3C).
Concurrent patches on the trunk showed essentially the same histologic features,
though the number of atypical T cells was often less than in the more infiltrated
lesions in the head and neck, which made a definite diagnosis in these specimens
more difficult or even impossible.
Immunohistochemical analysis demonstrated a CD3+-CD4+-CD8-phenotype of the neoplastic T cells in all cases
studied. Small numbers of scattered CD30+ blast cells were regularly
observed, as were small clusters of admixed B cells. In the initial diagnostic
specimens of 7 of the 51 patients, we found a considerable number of blast
cells (>15%; generally a mixture of CD30+ and CD30- blast cells). Six of these 7 patients died of lymphoma 11 to 100 months
(median, 40 months) after diagnosis.
In follow-up specimens taken during disease progression, the dermal
infiltrates tended to become more diffuse, sometimes showed complete effacement
of the follicular structures, and invariably showed increasing numbers of
CD30- and/or CD30+ blast cells. In the 8 prediagnostic
specimens, the dermal infiltrates were mainly confined to the perifollicular
areas. Although some of these specimens already contained small numbers of
atypical T cells in the follicular epithelium and in the perifollicular infiltrates,
the size and morphologic characteristics of the infiltrating T cells did not
warrant a definite diagnosis of follicular MF.
THERAPY AND FOLLOW-UP
Initial therapy consisted of psoralen plus UV-A (PUVA) treatment in
22 patients and total skin electron beam irradiation (TSEBI) in 11 patients
(Table 1). Seven patients were
initially treated with local radiotherapy in combination with other therapies,
including PUVA with or without retinoids, UV-B, topical mechlorethamine, or
topical steroids. For the remaining patients treatments included topical steroids
(3 patients), topical mechlorethamine (1 patient), UV-B (1 patient), PUVA
in combination with retinoids (1 patient), prednisone (1 patient), azathioprine
in combination with topical mechlorethamine (1 patient), or polychemotherapy
(2 patients). One patient refused treatment.
Only 8 (16%) of 51 patients, each with disease confined to the skin,
achieved complete remission on initial treatment. Six of them had been treated
with TSEBI, 1 with PUVA, and 1 with a combination of PUVA, retinoids, and
local radiotherapy. Two of these 7 patients were still in complete remission
after a follow-up of 38 and 192 months, respectively, and may be considered
cured.
The follow-up period varied between 8 and 239 months (median, 48 months;
mean, 58 months). Development of lymph node or visceral involvement was documented
in 14 and 7 patients, respectively. Disease progression defined as the development
of extracutaneous disease or death from lymphoma occurred in 20 (39%) of 51
patients, and occurred 11 to 168 months (median, 45 months) after diagnosis.
The calculated risk of disease progression during the first 5 years after
diagnosis was 37%; at 10 years, 66%. At the conclusion of the study, 26 patients
had died, 20 from lymphoma. The 5- and 10-year disease-specific survival rate
was 68% and 26%, respectively. The respective overall survival rates at 5
and 10 years were 64% and 14%. Univariate analysis demonstrated no association
between disease-specific survival and age at diagnosis, sex, duration of skin
lesions before diagnosis, or response to initial treatment.
FOLLICULAR MF VS CLASSIC MF
To evaluate differences in clinical behavior and prognosis between follicular
MF and classic MF, we compared relevant clinical features of the 49 patients
with follicular MF who had disease confined to the skin with the features
of 122 patients with generalized plaque-stage MF and 36 patients with tumor-stage
MF without evidence of extracutaneous disease and without associated follicular
mucinosis (Table 2). Patients
with follicular MF showed a significantly higher male-female ratio and less
frequently achieved complete remission on initial treatment. The calculated
risk of disease progression, as defined in this study, within the first 5
years after diagnosis was 36% for follicular MF vs 12% for classic plaque-stage
MF and 24% for tumor-stage MF. Disease-specific and overall survival in patients
with follicular MF were significantly lower than in patients with generalized
plaque-stage MF, and were roughly similar to patients with tumor-stage MF
without associated follicular mucinosis (Figure 4).
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Table 2. Characteristics of Patients With Folllicular, Generalized
Plaque-Stage, and Tumor-Stage Mycosis Fungoides*
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Figure 4. Actuarial disease-related survival
of 49 patients with follicular mycosis fungoides (FMF), 122 with generalized
plaque-stage mycosis fungoides (MF) (T2 N0 M0), and 36 with tumor-stage MF
(T3 N0 M0). For FMF vs plaque-stage MF, P<.001;
for FMF vs tumor-stage MF, P = .25.
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COMMENT
The results of the present study clearly demonstrate that follicular
MF has distinctive clinicopathologic features and should be considered a distinct
disease entity. Characteristic histologic features include the primary perifollicular
localization of the dermal infiltrates, with variable infiltration of the
follicular epithelium by medium-sized to large atypical T cells with cerebriform
nuclei. In most cases the epidermis is spared (folliculotropism instead of
epidermotropism). Mucinous degeneration of the follicular epithelium occurs
in most cases, and a considerable admixture with eosinophils and plasma cells
is frequently present.
Clinical characteristics include the preferential localization of the
skin lesions in the head and neck area (45 of 51 patients), the presence of
papules (often grouped), alopecia, frequent secondary bacterial infection,
and, less commonly, the presence of acneiform lesions and mucinorrhea. Unlike
in classic MF, pruritus is often severe and may represent a good parameter
of disease activity: in several patients, a relapse after initial therapy
was preceded by the reappearance of pruritus. In addition, patients with follicular
MF proved generally more refractory to standard classic MF therapies, showed
more frequent disease progression, and had a less favorable prognosis (Table 2).
This more unfavorable prognosis suggests a true biological difference
in clinical behavior between patients with follicular MF and patients with
the classic epidermotropic type of MF, which is consistent with the conclusion
of a recent study.11 The similar duration of
skin lesions before diagnosis in patients with follicular MF and patients
with classic-type MF indicates that the difference in survival does not simply
result from a selection of patients with more advanced disease in the present
study (Table 2). Comparison of
the disease-specific and overall survival data indicate that patients with
follicular MF have a similar (at 5 years) or worse (at 10 years) survival
than patients with tumor-stage MF (Table
2). Nevertheless, under the classic MF classification systems,12-13 most of our patients with follicular
MF would have been classified as stage IA (T1 N0 M0) or IB (T2 N0 M0), and
only 14 of them had nodules or tumors at the time of diagnosis. This supports
our contention that these clinical staging systems for MF are not very useful
in patients with follicular MF. For instance, patients presenting with a solitary
patch or plaque on the face do not have stage IA or T1 N0 M0–stage disease.
Because of the perifollicular localization of the dermal infiltrates, such
patients should always be considered to have tumor-stage disease, regardless
of the clinical appearance of the skin lesion, and should be treated accordingly.
MF-ASSOCIATED FOLLICULAR MUCINOSIS VS FOLLICULAR MF
In recent years the term follicular MF or cutaneous T-cell lymphoma (also folliculocentric
MF or pilotropic MF) has been introduced for
a rare clinical variant of MF characterized by follicular papules, follicular
keratoses, comedolike lesions and epidermal cysts. Histologically, perifollicular
infiltrates are present showing marked folliculotropism, but there is generally
no epidermotropism or follicular mucinosis.14-22
Evaluation of published reports of "follicular MF" demonstrates considerable
clinical heterogeneity and suggests that this term has been used for the diagnoses
of at least 3 different groups of patients.
The largest group comprises patients with clinically and histologically
classic MF prior to or, less often, concurrent with the development of the
follicular lesions.17, 21-22
In the present study, 3 patients with 4- to 7-year histories of classic epidermotropic
MF developing skin tumors with the histologic features of follicular MF were
excluded because such cases show the clinical behavior of classic MF developing
tumor-stage disease.
The second group includes patients presenting with acneiform lesions
as the predominant or only manifestation of the disease.17, 19, 21-22
However, a similar clinical presentation may also occur in patients with associated
follicular mucinosis23-24 and
was a predominant feature in 4 of 51 patients in the present study. One of
our patients was a 16-year-old boy with a history of severely pruritic acneiform
lesions and alopecia for more than 5 years before the diagnosis MF-associated
follicular mucinosis was made. Despite radiotherapy and multiagent chemotherapy,
he died 5 years after diagnosis of systemic lymphoma. Interestingly, while
several of his acneiform lesions showed mucin deposits, others did not, even
after further sectioning.
Finally, some of the reported cases demonstrate all of the characteristic
clinical and histologic features of the cases reported herein except for the
presence of follicular mucinosis.18, 20
The present study includes 2 such cases in patients who otherwise did not
differ clinically or histologically from the 49 patients with associated follicular
mucinosis. Based on these observations, we do not believe that it is useful
to differentiate between follicular MF with and without associated follicular
mucinosis in these 2 latter groups. From a biological point of view, the most
relevant feature in follicular MF with or without follicular mucinosis is
the deep, perifollicular localization of the neoplastic infiltrates, which
makes them less accessible to skin-targeted therapies. On the basis of our
own observations and the available literature,11
we are inclined to believe that follicular MF with or without follicular mucinosis
should not be considered separately, and that cases with a preferential (peri)follicular
distribution of the neoplastic infiltrates, regardless of the presence of
mucinous degeneration, should be termed follicular MF.
DIFFERENTIAL DIAGNOSIS
Although distinctive clinical and histologic features should facilitate
an early and correct diagnosis, it is our experience over the last 15 years
that the diagnosis of follicular MF is often overlooked. Because of the preferential
involvement of the head and neck area, the absence of patches and plaques
on the trunk or buttocks, and the absence of epidermotropic atypical T cells,
the diagnosis of MF or cutaneous T-cell lymphoma is often not considered.
The following incorrect diagnoses have been made more than once prior to referral:
seborrheic dermatitis in patients presenting with erythematous lesions on
the scalp and eyebrows; atopic dermatitis, because of the severe pruritus;
and facial granuloma with eosinophilia in patients presenting with a solitary
plaque on the face and an eosinophil-rich infiltrate. Finally, it should be
noted that even when follicular MF is suspected, it may require several biopsies
to make a definite diagnosis. It is important that biopsy specimens be taken
from the most infiltrated skin lesions, generally in the face or neck, and
not only from patches with or without follicular papules on the trunk.
THERAPY
The results of the present study confirm our clinical impression and
the scattered data in literature that patients with follicular MF are generally
less responsive to standard therapies used in patients with classic MF.11, 20, 25 Our retrospective
study does not allow a meaningful comparison of the effects of the different
treatment methods because patients were treated at different institutions,
and treatment selection may have been affected by disease severity.
Because of the perifollicular localization of the dermal infiltrates,
patients with follicular MF should always be considered to have tumor-stage
disease, regardless of the clinical appearance of the skin lesions. Therefore,
in patients presenting with a single plaque or tumor or a few clustered skin
lesions, but without patches or follicular papules at other sites, radiotherapy
is the first choice for treatment. In selected cases with superficial lesions
presenting at multiple sites, PUVA treatment might be attempted first. However,
in most cases this approach will not result in complete remission. In the
present series, complete remission was achieved with PUVA therapy in only
1 of 22 patients. In patients with more infiltrated skin lesions, in particular
those who do not respond to PUVA therapy alone, TSEBI is the preferred method
of treatment. However, only 6 of 11 patients treated with TSEBI reached complete
remission, and 3 of the 6 complete responders had a relapse within 6 months.
The relative unresponsiveness of follicular MF to TSEBI has been reported.18 In some patients relapsing skin disease may be controlled
effectively by a maintenance treatment with topical nitrogen mustard. If TSEBI
is not available, PUVA in combination with interferon alfa or retinoids and
local radiotherapy for thick tumors may be an alternative. The same approach
can be used for relapsing disease following TSEBI. In our experience, multiagent
chemotherapy does not generally result in complete remission in patients with
skin-limited disease and should therefore be reserved for patients developing
extracutaneous disease.
AUTHOR INFORMATION
Accepted for publication July 2, 2001.
Corresponding author and reprints: Rein Willemze, MD, Department
of Dermatology, B1-Q-93, Leiden University Medical Center, Albinusdreef 2,
2333 ZA Leiden, the Netherlands (e-mail: willemze.dermatology{at}lumc.nl).
From the Departments of Dermatology (Dr van Doorn) and Pathology (Dr
Scheffer), Vrije Universiteit Medical Center, Amsterdam, and Department of
Dermatology (Dr Willemze), Leiden University Medical Center, the Netherlands.
A complete list of the participants in the Dutch Cutaneous Lymphoma Group
is available from the authors.
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