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Follicular Mucinosis
A Critical Reappraisal of Clinicopathologic Features and Association With Mycosis Fungoides and Sézary Syndrome
Lorenzo Cerroni, MD;
Regina Fink-Puches, MD;
Barbara Bäck;
Helmut Kerl, MD
Arch Dermatol. 2002;138:182-189.
ABSTRACT
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Context Beginning in 1957, patients have been described with localized alopecia
characterized histopathologically by mucin deposition within hair follicles
(follicular mucinosis [FM]). At least 2 distinct diagnostic entities have
been proposed: one occurring in children and young adults without association
with other diseases ("idiopathic" FM), the other occurring in elderly patients
and associated with mycosis fungoides or Sézary syndrome ("lymphoma-associated"
FM).
Objective To determine whether idiopathic and lymphoma-associated FM are distinct
or related entities.
Design Case series.
Setting Department of Dermatology, University of Graz, Graz, Austria.
Patients Forty-four patients with FM were divided into 2 groups. Group 1 comprised
16 patients (mean age, 37.5 years) with no associated mycosis fungoides or
Sézary syndrome; group 2 was made up of the other 28 (mean age, 52.2
years), who had clinicopathologic evidence of cutaneous T-cell lymphoma.
Results Mean age was lower in patients with idiopathic FM, but a considerable
overlapping among the 2 groups was present. Location on the head and neck
region was common in both groups, but most patients with lymphoma-associated
FM had lesions also on other body sites. In fact, solitary lesions at presentation
were common in patients with idiopathic FM (11 [68.8%] of 16 patients), but
uncommon in those with lymphoma-associated FM (2 [7.1%] of 28 patients). Histopathologic
findings did not allow clear-cut differentiation of the 2 groups. Finally,
a monoclonal rearrangement of the T-cell receptor  gene was demonstrated
by polymerase chain reaction analysis in about 50% of tested cases from each
group.
Conclusions Criteria previously reported to differentiate idiopathic from lymphoma-associated
FM proved ineffective. In analogy to localized pagetoid reticulosis (Woringer-Kolopp
disease), small-plaque parapsoriasis, and so-called solitary mycosis fungoides,
idiopathic FM may represent a form of localized cutaneous T-cell lymphoma.
INTRODUCTION
IN 1957, Hermann Pinkus1 described a
group of 6 patients with localized alopecia characterized histopathologically
by mucin deposition within hair follicles. In the following years, the term follicular mucinosis (FM) proposed by Jablonska et al2 in 1959 slowly replaced alopecia
mucinosa, the designation originally coined by Pinkus himself. Subsequent
reports suggested that at least 2 distinct entities were encompassed under
this diagnosis: one occurring in children and young adults without association
with other cutaneous or extracutaneous diseases ("idiopathic" FM), the other
occurring in elderly patients and associated with mycosis fungoides or Sézary
syndrome ("lymphoma-associated" FM).3-13
In addition, progression of idiopathic FM into cutaneous T-cell lymphoma (CTCL)
has been well documented in several cases.14-18
In this study, we reviewed data from a large group of patients with
idiopathic and lymphoma-associated FM with respect to clinicopathologic presentation
and molecular features.
PATIENTS AND METHODS
Data from 44 patients with FM were retrieved from the files of the Department
of Dermatology of the University of Graz, in Austria. Patients were divided
into 2 groups according to clinicopathologic features: 16 patients had no
evidence of mycosis fungoides or Sézary syndrome at presentation and
did not develop CTCL in the follow-up time (group 1, idiopathic FM); the other
28 had clinicopathologic evidence of mycosis fungoides or Sézary syndrome
at presentation or developed CTCL in the follow-up time (group 2, lymphoma-associated
FM). Diagnosis of mycosis fungoides and Sézary syndrome was made according
to criteria published in the European Organization for Research and Treatment
of Cancer (EORTC) classification for cutaneous lymphomas.19
HISTOLOGIC CHARACTERISTICS
In all cases, one or more biopsy specimens were available for review
of histopathologic features. Hematoxylin-eosin, periodic acid–Schiff,
colloidal-iron, and Giemsa stains were available for histologic review of
biospy specimens.
IMMUNOHISTOLOGIC CHARACTERISTICS
In 30 cases where enough material was available, complete immunophenotypical
studies were performed using a standard 3-step immunoperoxidase technique.20 Antigen retrieval was performed for most of the antibodies
with a standard heat-retrieval technique.
MOLECULAR BIOLOGIC CHARACTERISTICS
Analysis of the T-cell receptor (TCR)
gene rearrangement was performed on formalin-fixed, paraffin-embedded tissue
sections in 30 cases where enough material was available. Isolation of DNA
was performed with standard methods. Briefly, five 5-µm sections were
cut from each biopsy specimen and coated on slides. To avoid cross contamination,
the blade of the microtome was changed after cutting each sample. Slides were
subsequently deparaffinized by xylene and ethanol. After air drying, sections
were scraped off the slides and resuspended in 50 to 100 µL of digestion
buffer (100mM of Tris-hydrochloride, pH 8.0; and 1 µg/µL of Proteinase
K [Boehringer Mannheim, Mannheim, Germany]), depending on the size of the
specimen. After incubation at 55°C for 24 hours, samples were heated to
94° for 15 minutes and stored at -20°C.
The TCR gene was analyzed using the
polymerase chain reaction (PCR) technique as described by McCarthy et al,21 with minor modifications. Briefly, 2% to 5% of total
template DNA was used in a 50-µL PCR reaction containing primers V11
(250 nM), V101 (250 nM), J11 (500 nM), Jp12 (500nM), dinucleotide
triphosphate (200µM each), magnesium chloride (1.5mM), potassium chloride
(50mM), Tris-hydrochloride at pH 8.3 (10mM), and AmpliTaq Gold DNA Polymerase
(Perkin Elmer, Branchburg, NJ). After initial heating at 94°C for 10 minutes,
40 cycles of the reaction were carried out (denaturation, 94°C for 60
minutes; annealing, 50°C for 30 minutes; extension, 72°C for 30 min).
A 10-µL Aliquot of the PCR products was then run on a 3.5% MetaPhor
agarose gel (FMC BioProducts, Rockland, Mass), stained with ethidium bromide,
and viewed under UV light. The  -actin gene was analyzed as internal
control in all cases.
RESULTS
IDIOPATHIC FM
Clinicopathologic and molecular features for patients with idiopathic
FM are summarized in Table 1.
Sixteen patients had FM without signs of CTCL or other cutaneous or extracutaneous
diseases (M/F, 1.3:1; mean age, 37.5 years; median age, 40 years; range, 13-61
years). Patients presented with solitary (n = 11) or multiple (n = 5) folliculotropic
patches or plaques (Figure 1). Lesions
were located on the face and neck in 15 patients and on the trunk in 1. No
patient had generalized lesions. Histologic analysis revealed mucin deposits
within the hair follicles in all cases. The amount of mucin varied in different
cases, and in different hair follicles in the same case. A varying amount
of eosinophils could be observed in 11 of 16 cases.
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Table 1. Summary of Clinicopathologic Features and Follow-up Data for
Patients With Idiopatic Follicular Mucinosis*
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Figure 1. A solitary patch of idiopathic
follicular mucinosis on the chin of patient 8.
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In 6 cases, there was a dense lymphoid infiltrate and great numbers
of lymphocytes around and within affected hair follicles (Figure 2). Some lymphocytes had hyperchromatic, folded nuclei (small
to medium-sized pleomorphic lymphocytes). Epidermotropism was not observed.
These cases were not classified as lymphoma-associated FM because of the lack
of clinicopathologic features of CTCL.
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Figure 2. Idiopathic follicular mucinosis
(FM) on patient 4. A, A dense infiltrate of lymphocytes is found within the
entire dermis, but the epidermis is spared. B, An almost completely destroyed
hair follicle shows remnants of FM with a dense perifollicular and intrafollicular
lymphoid infiltrate.
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The other 10 cases showed only a mild lymphocytic infiltrate around
hair follicles with scattered intrafollicular lymphocytes (Figure 3). Immunohistologic analysis performed in 11 cases revealed
that the great majority of the lymphocytes had a T-helper phenotype. Molecular
analysis showed the presence of a monoclonal rearrangement of the TCR gene in 6 of 11 cases analyzed (Figure 4).
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Figure 3. A, Idiopathic follicular mucinosis
(FM) in patient 12 with a mild lymphoid infiltrate. B, Detail of a hair follicle
with FM and intrafollicular lymphocytes.
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Figure 4. Results of molecular analysis
of T-cell receptor gene rearrangement in some of the cases. Lanes
1 through 5, lymphoma-associated follicular mucinosis (FM); note the monoclonal
band in lanes 3 and 4. Lanes 6 through 10, idiopathic FM; note the monoclonal
band in lanes 7 and 9. Lane 11, negative control (no DNA); lane 12, molecular
ladder; lane 13, referent.
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The mean follow-up time was 71.6 months (range, 5-242 months; median,
22 months). All patients were alive, and no one developed mycosis fungoides
or other CTCLs by the last follow-up examination. Seven patients are currently
in complete remission (mean follow-up, 148.6 months; range: 29-242 months),
whereas the other 9 show residual disease (mean follow-up, 11.7 months; range
5-25 months).
LYMPHOMA-ASSOCIATED FM
Twenty-eight patients had FM associated with mycosis fungoides (n =
26) or Sézary syndrome (n = 2) in different stages (M/F, 2.5:1; mean
age, 52.2 years; median age, 53 years; age range, 32-74 years) (Table 2). At first presentation, patients had solitary (n = 2) or
multiple (n = 20) patches or plaques covering less than 10% of the body surface
(Figure 5). Two patients with Sézary
syndrome had erythroderma, and 4 with mycosis fungoides had generalized patches
and plaques covering more than 10% of the body surface. Histopathologically,
all cases revealed varying amounts of mucin within 1 or more hair follicles.
Varying numbers of eosinophils could be observed in 19 of 28 cases. Seventeen
of 28 cases showed histopathologic features of CTCL, including the presence
of focal epidermotropism of lymphocytes within the epidermis between the hair
follicles (Figure 6). Clear-cut
Pautrier microabscesses, however, were seen only in a minority of the cases.
Some lymphocytes in the dermis had hyperchromatic, folded nuclei (small- to
medium-sized pleomorphic lymphocytes), but atypical cells never represented
the majority of the infiltrate.
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Table 2. Summary of Clinicopathologic Features and Follow-up Data for
Patients With Lymphoma-Associated Follicular Mucinosis
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Figure 5. Lymphoma-associated follicular
mucinosis in patient 29. Patches, plaques, and flat tumors appear on the face
and neck.
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Figure 6. Lymphoma-associated follicular
mucinosis (FM) in patient 40. A, Follicular mucinosis with bandlike infiltrate
in the papillary dermis. B, Detail of the epidermis showing epidermotropic
lymphocytes.
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In 2 patients (patients 22 and 33), a biopsy specimen taken at presentation
showed a dense lymphoid infiltrate around and within hair follicles, but no
evidence of epidermotropism. In 1 of these 2 patients (patient 33) a second
biopsy specimen taken at the same time showed features of mycosis fungoides
without FM. The last 9 cases revealed a histopathologic picture characterized
by mucin deposits in the hair follicles with only a mild lymphoid infiltrate
(Figure 7). In 10 of the last 11
patients, the initial diagnosis was idiopathic FM (patients 18, 22, 25, 27,
28, 31, 35, 39, 42, and 44), and the diagnosis of CTCL was made only after
analysis of specimens from repeated biopsies done over different periods of
time (mostly within a few weeks or months; in patients 25 and 39, after 2
and 15 years, respectively).
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Figure 7. Lymphoma-associated follicular
mucinosis (FM) in patient 39. This patient presented first in 1972 with multiple
patches on the trunk and upper extremities. A, Histologic findings showed
only FM with a mild lymphoid infiltrate and no feature of cutaneous lymphoma.
In 1987, 15 years after the first biopsy, the patient presented with widespread
patches and plaques with FM (B-C). The patient died in 1989 of widespread
mycosis fungoides.
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Immunohistologic analysis performed in 19 cases showed the predominance
of cells with a T-helper phenotype. Molecular analysis showed the presence
of a monoclonal population of T lymphocytes in 9 of 19 cases analyzed (Figure 4). Seven patients died of their disease
after a mean survival time of 125 months (range, 19-262 months). After a mean
follow-up of 60.9 months (range, 2-221 months; median, 48 months), 19 patients
are alive and in complete (n = 2) or partial (n = 11) remission or with progressive
disease (n = 6). Two further patients with progressive disease died of unrelated
causes after 48 and 59 months, respectively.
COMMENT
Follicular mucinosis is an epithelial reaction pattern characterized
by the accumulation of mucin within hair follicles.22
It occurs in a number of inflammatory, infectious, and neoplastic skin conditions,
and in this context cannot be considered a specific skin disease.22-34
Although it is generally accepted that the disease was first described by
Pinkus1 in 1957, in the same year Braun-Falco35 reported an identical condition, and a patient with
similar clinicopathologic features had already been observed by Lehner and
Szodoray36 in 1939.
After the report by Pinkus, several publications proposed the existence
of 2 main types of FM.3-13,37-43
The first type occurs in young patients in the absence of concomitant cutaneous
or extracutaneous disorders and shows localized lesions with a tendency to
resolve within a few years (idiopathic FM). The second type occurs in elderly
patients and is associated with mycosis fungoides or Sézary syndrome.
A third type of FM presenting with clinicopathologic features of both
of the other 2 groups has also been described (the so-called persistent or
chronic benign FM).3, 15 The existence
of this distinct third type is questionable. In fact, cases classified within
this third group probably represent examples of lymphoma-associated FM. For
example, one child described by Gibson et al44
in 1988 had widespread lesions on the trunk and extremities recurring for
17 years in spite of various treatments including systemic chemotherapy, radiotherapy,
topical nitrogen mustard, and psoralen plus UV-A therapy. Analysis of specimens
from 2 biopsies taken at presentation led to a diagnosis of lymphosarcoma,
and the clinical features were consistent with mycosis fungoides.
Classification of cases like this one as persistent FM has contributed
to the confusion existing in this field. Moreover, even the prognosis of idiopathic
FM is not well elucidated, and several cases showing "transformation" into
mycosis fungoides or other CTCLs have been reported.3-18
We have demonstrated here that no clear-cut criteria allow the differentiation
of idiopathic from lymphoma-associated FM, and we propose that idiopathic
FM may belong to the variant forms of mycosis fungoides that show a prolonged,
nonaggressive clinical course (Table 3).
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Table 3. Clinicopathologic Criteria Used in the Literature for Differentiation
of "Idiopathic" From "Lymphoma-Associated" FM and Corresponding Findings in
Our 2 Groups of Patients*
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It has been suggested that the age of the patient, location of the lesion(s),
and histopathologic features of the infiltrate may provide clues to help differentiate
idiopathic from lymphoma-associated FM.3, 8-9,45
Another criterion proposed as helpful in the differential diagnosis is the
molecular analysis of the TCR gene rearrangement.46 However, several authors have pointed out the difficulty,
or even impossibility, of clearly distinguishing the 2 groups.4, 6, 47
We shall address these proposed distinguishing features one at a time,
beginning with patient age. The mean age in our study was indeed lower in
patients with idiopathic FM than in those with lymphoma-associated FM, but
there was a considerable overlap between the 2 groups. Moreover, although
mycosis fungoides is predominantly a disease of elderly patients, several
cases have been reported in children, with or without FM.48-52
Thus, it is not possible to exclude a diagnosis of mycosis fungoides solely
on the basis of the age of the patient.
As for lesion location, lesions were present on the face and neck in
most patients from both groups, but patients with lymphoma-associated FM showed
often concomitant lesions on other areas of the body. In this context, it
should be stressed that, contrary to previous suggestions, lymphoma-associated
FM is commonly located on the face and neck region,17, 19, 53-54
and some patients presenting with isolated lesions of FM on the face afterwards
have developed clear-cut mycosis fungoides.53, 55
In short, location alone cannot be considered a valid discriminatory factor.
On the other hand, solitary vs multiple lesions might be a distinguishing
characteristic. In our series, solitary lesions at presentation were common
in patients with idiopathic FM (11 [68.8%] of 16 patients), but uncommon in
those with lymphoma-associated FM (2 [7.1%] of 28 cases). The presence of
solitary as opposed to multiple lesions, therefore, might be a distinguishing
feature between the 2 groups. However, it should be noted that mycosis fungoides
can present with solitary lesions.56-58
Moreover, a case of folliculotropic mycosis fungoides (though without clear-cut
FM) has also been documented with a solitary lesion,59
and one of idiopathic FM with generalized lesions has been reported as well,60 again underlying the overlapping clinical features
of these 2 entities.
Remarkably, in our study histopathologic analysis did not provide useful
clues to differentiate the 2 groups of patients, confirming previous observations.6, 9 In fact, in the group of lymphoma-associated
FM, 9 (32.1%) of the 28 patients showed histopathologic features suggestive
of idiopathic FM, and 2 more presented with dense lymphoid infiltrates but
without epidermotropism of lymphocytes. Conversely, in the idiopathic FM group,
6 (37.5%) of 16 patients revealed skin lesions with dense lymphoid infiltrates
unusual for this type of FM and suggestive of a cutaneous lymphoproliferative
process. Similar dense lymphoid infiltrates have been reported in patients
with idiopathic FM, which underscores the overlapping histopathologic features
between the 2 groups.1, 6, 22, 47, 61
The amount of mucin deposits within hair follicles and the presence
of eosinophils within the infiltrate were similar in the 2 groups. It is also
of interest to note that in 10 cases (35.7%) of lymphoma-associated FM, the
diagnosis of CTCL was not made at presentation, and skin lesions were originally
classified as idiopathic FM before analysis of sequential biopsy specimens
proved the nature of the infiltrate. A similar case was recently described
by Bonta et al.62 These cases would previously
have been classified as idiopathic or persistent FM with transformation into
CTCL, but we agree with Hempstead and Ackerman22
that they most likely represent examples of cases where mycosis fungoides
or Sézary syndrome was present from the beginning.
In our study, the immunophenotype was also similar in both groups, and
even PCR analysis of the infiltrate could not help differentiate the 2 types.
In fact, a monoclonal rearrangement of the TCR
gene could be identified in 6 (54.5%) of 11 and 9 (47.4%) of 19 cases of idiopathic
and lymphoma-associated FM, respectively, indicating that a monoclonal population
of T lymphocytes can be detected in about half of the cases in both groups.
These data are in contrast to those reported by Meehan et al,46
who found no monoclonality in 5 patients with idiopathic FM, but confirm previous
observations describing a monoclonal population of T lymphocytes in cases
of idiopathic FM.46, 61, 63-64
Besides mycosis fungoides and Sézary syndrome, Hodgkin disease
has also been observed in association with FM in several patients.8, 44, 65-67
However, the association of Hodgkin disease with mycosis fungoides is well
known,68 and it might be that in at least some
of these patients, cutaneous changes represented lesions of mycosis fungoides–associated
FM. Indeed, most patients showed clinical presentations uncommon for idiopathic
FM: One child described by Gibson et al44 had
a widespread skin eruption involving the upper and lower extremities as well
as the face; the child described by Kim and Winkelmann8
had multiple lesions on the arms and legs; the patient described by Stewart
and Smoller67 had lesions on both legs; and
the one described by Ramon et al65 had multiple
lesions on the chest.
One of the main problems in studying patients with FM is the bias introduced
by classifying them into one of the 2 main diagnostic groups. In fact, depending
on the definition of idiopathic and lymphoma-associated FM in the given case,
some patients may be classified into either of the groups, thus causing diagnostic
confusion. We used clinicopathologic evidence of CTCL at presentation or during
follow-up as the only distinguishing criterion to try to identify a group
of patients with benign as opposed to malignant disease. Nevertheless, there
was a considerable overlap in clinical presentation, histopathologic features,
and molecular data between the 2 groups.
It may be argued that our follow-up for some of the patients with idiopathic
FM was too short to rule out lymphoma-associated FM. However, even considering
only the 5 patients with more than 9 years of follow-up in the idiopathic
FM group (patients 4, 5, 7, 8, and 15; mean follow-up: 191.8 months; range:
111-242 months), a similar overlapping of clinicopathologic features was observed
(mean age at onset, 41.6 years; age at onset range, 21-61 years; histologic
findings suggestive of CTCL in 2 [40.0%] of 5 cases; monoclonality found in
2 [50%] of 4 tested cases).
At this point, one must question whether idiopathic and lymphoma-associated
FM are unrelated diseases (ie, represent 2 completely distinct clinicopathologic
entities) or rather different names for a single disease with a variable spectrum
of clinicopathologic presentations and outcomes. In this context, it should
be noted that several variants of mycosis fungoides with prolonged, nonaggressive
clinical course have been described, such as unilesional (solitary) mycosis
fungoides, localized pagetoid reticulosis (Woringer-Kolopp disease), and parapsoriasis
en plaques.54, 56-58
Moreover, it has also been recognized that most patients with mycosis fungoides
experience a chronic disease with prolonged survival.19, 54, 69-70
Our results, and findings from review of the literature, suggest that idiopathic
FM may represent a variant of mycosis fungoides with localized disease and
excellent prognosis, conceptually similar to the localized variant of pagetoid
reticulosis (Woringer-Kolopp disease). Regardless of the classification of
these cases as "indolent" CTCL or benign inflammatory dermatitis, patients
with so-called idiopathic FM should be observed carefully for long periods
of time.
AUTHOR INFORMATION
Accepted for publication June 18, 2001.
Corresponding author and reprints: Lorenzo Cerroni, MD, Department
of Dermatology, University of Graz, Auenbruggerplatz, 8, A-8036 Graz, Austria
(e-mail: lorenzo.cerroni{at}kfunigraz.ac.at).
From the Department of Dermatology, University of Graz, Austria.
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