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Blood, Vol. 95 No. 12 (June 15), 2000:
pp. 3653-3661
PLENARY PAPER
From the Department of Dermatology, Leiden University Medical
Center, Leiden; the Departments of Pathology and Dermatology, Free
University Hospital, Amsterdam; the Department of Dermatology,
University Hospital Groningen; the Department of Dermatology,
University Hospital Rotterdam; the Department of Dermatology,
University Hospital Gent; and the Department of Dermatology, University
Hospital Utrecht, The Netherlands.
To evaluate our diagnostic and therapeutic guidelines, clinical and
long-term follow-up data of 219 patients with primary or secondary
cutaneous CD30+ lymphoproliferative disorders were
evaluated. The study group included 118 patients with lymphomatoid
papulosis (LyP; group 1), 79 patients with primary cutaneous
CD30+ large T-cell lymphoma (LTCL; group 2), 11 patients
with CD30+ LTCL and skin and regional lymph node
involvement (group 3), and 11 patients with secondary cutaneous
CD30+ LTCL (group 4). Patients with LyP often did not
receive any specific treatment, whereas most patients with primary
cutaneous CD30+ LTCL were treated with radiotherapy or
excision. All patients with skin-limited disease from groups 1 and 2 who were treated with multiagent chemotherapy had 1 or more skin
relapses. The calculated risk for systemic disease within 10 years of
diagnosis was 4% for group 1, 16% for group 2, and 20% for group 3 (after initial therapy). Disease-related 5-year-survival rates were
100% (group 1), 96% (group 2), 91% (group 3), and 24% (group 4),
respectively. The results confirm the favorable prognoses of these
primary cutaneous CD30+ lymphoproliferative disorders and
underscore that LyP and primary cutaneous CD30+ lymphomas
are closely related conditions. They also indicate that
CD30+ LTCL on the skin and in 1 draining lymph node
station has a good prognosis similar to that for primary cutaneous
CD30+ LTCL without concurrent lymph node involvement.
Multiagent chemotherapy is only indicated for patients with full-blown
or developing extracutaneous disease; it is never or rarely indicated
for patients with skin-limited CD30+ lymphomas.
(Blood. 2000;95:3653-3661)
Primary cutaneous T-cell lymphomas (CTCL) represent a
heterogeneous group of neoplasms derived from skin-homing T cells.
Apart from mycosis fungoides (MF), primary cutaneous CD30+
lymphoproliferative disorders are the most common group, accounting for
approximately 25% of all CTCL. This group includes primary cutaneous
CD30+ (anaplastic) large T-cell lymphomas (LTCL) and
lymphomatoid papulosis (LyP), a chronic recurrent, self-healing
papulonodular skin eruption with histologic features of a
(CD30+) CTCL.1-3 Because of
overlapping clinical, histologic, and immunophenotypical characteristics, these conditions are considered to represent a
spectrum of primary cutaneous CD30+
lymphoproliferations.4,5 It is well established that these primary cutaneous CD30+ lymphoproliferations have favorable
prognoses in most patients.6-12 Previous studies by our
group demonstrated significant differences between primary cutaneous
CD30+ (anaplastic) LTCL and morphologically similar
systemic CD30+ anaplastic large-cell
lymphomas.13 In contrast to these systemic lymphomas,
primary cutaneous CD30+ LTCL are rare in children; they
generally express the cutaneous lymphocyte antigen (CLA) characteristic
of skin-homing T cells but usually not the epithelial membrane antigen
(EMA). They are not associated with Epstein-Barr virus or, according
to most studies,14-17 with the t(2;5) translocation
(ALK/p80-negative), and they have a significantly better prognosis. For
these reasons, primary CD30+ CTCL is included as a separate
group in the revised European-American classification for non-Hodgkin
lymphomas (REAL classification)18 and in the proposed World
Health Organization classification.19 Notwithstanding the
many publications describing the characteristic features of these
primary cutaneous CD30+ lymphomas and emphasizing their
favorable prognosis, referral centers for cutaneous lymphomas are
confronted regularly with patients who have been misdiagnosed or who
have been treated with unnecessarily aggressive treatment
regimens.20-22 In particular, the diagnosis LyP is often
overlooked. Based on the histologic diagnosis of a CD30+
(anaplastic) LTCL and the presence of multifocal skin lesions, patients
with LyP are routinely treated with multiagent chemotherapy by
physicians unaware of the spectrum of LyP. Unfortunately, skin relapses
during or shortly after systemic chemotherapy are almost the rule and
give the false impression of a highly aggressive T-cell lymphoma
requiring even more aggressive therapy.
The current report describes the results of a recent evaluation of 219 patients with cutaneous CD30+ lymphoproliferation who were
included in the Dutch registry for cutaneous lymphomas between 1983 and
1998. This study was conducted to evaluate our current diagnostic and
therapeutic approaches for these patients and to define potential risk
factors for tumor progression. Detailed clinical and long-term
follow-up data of well-defined groups of primary and secondary
cutaneous CD30+ lymphoproliferations are presented. Based
on these data, practical guidelines for proper diagnosis, management,
and treatment are presented.
Patients
Risk factors for tumor progression
Statistical analysis
The main clinical characteristics for the 4 groups studied are
summarized in Table 2. Additional
information for these groups is given separately below.
Lymphomatoid papulosis Group 1 consisted of 69 males and 49 females with a median age of 45.5 years at diagnosis (range, 4 to 88 years). Patients initially sought treatment for papular, papulonecrotic, or nodular skin lesions, and 8 patients (7%) also sought it for additional plaques or tumors. Characteristically, skin lesions in different stages of evolution were found next to each another (Figure 1). There was no preferential anatomic site of involvement. The group included 12 patients (10%) younger than 20 years of age at the time of diagnosis (median, 12 years; range, 4 to 19 years). Interestingly, 3 of these children (6, 13, and 16 years of age) had papules and rapidly growing ulcerating nodules or tumors. Despite this alarming clinical presentation, the lesions slowly subsided within 6 to 10 weeks without any specific treatment. None of the 12 children had extracutaneous disease or died of lymphoma after a median follow-up of 52 months (range, 25 to 131 months).
Primary cutaneous CD30+ large cell lymphoma
CD30+ LTCL with skin and draining lymph node
involvement
Secondary cutaneous CD30+ large T-cell lymphoma
In the current study, clinical and histologic variables of a major
group of 219 cutaneous CD30+ lymphoproliferations were
evaluated. The primary goals of this analysis were a critical
evaluation of our current diagnostic and therapeutic approaches and a
definition of potential risk factors for tumor progression. Relevant
features of the different groups of cutaneous
CD30+ lymphomas are discussed, and guidelines for
correct diagnosis and treatment are presented.
Primary cutaneous CD30+ large T-cell lymphoma
Therapy. In patients with a solitary or few localized nodules or tumors, local radiotherapy is the first choice of treatment. However, follow-up data indicate that if the lesion has been excised completely or has disappeared spontaneously, no further therapy is required. If a skin lesion relapses, spontaneous resolution can be awaited for some weeks or the patient can undergo radiotherapy or surgical excision. According to our existing guidelines formulated in 1991, patients with multifocal skin lesions should be treated with doxorubicin-based multiagent chemotherapy. However, only 7 of 17 patients with multifocal skin lesions in this study had ever been treated with systemic chemotherapy. More important, all patients who were treated with CHOP courses because of multifocal skin lesions (6 of 7 patients) had 1 or several skin relapses afterward. Moreover, in 3 of these 17 patients, all initial skin lesions disappeared spontaneously. Unlike LyP lesions, however, relapse did not occur during the 32- to 72-month follow-up. These observations suggest that multifocal skin-restricted CD30+ LTCL should not be treated routinely with multiagent chemotherapy. If spontaneous regression does not occur, these patients can best be treated with radiotherapy for a few lesions or with low-dose methotrexate as for LyP.20,27 In patients with full-blown or developing regional lymph node involvement, multiagent chemotherapy is still considered the safest option. However, skin relapses after chemotherapy are common, but they are not associated with an aggressive clinical behavior and therefore do not require an aggressive approach. Moreover, complete spontaneous resolution of skin and lymph node localizations may occur. In such patients an expectative approach seems justified. Lymphomatoid papulosis In this very large group of patients with LyP with a median follow-up of 77 months and of 29 patients with a follow-up of more than 10 years, 23 of 118 patients (19%) had associated malignant lymphoma either before, after, or concurrent with LyP. However, only 7 of 118 had extracutaneous disease, and only 2 of 118 patients died of systemic lymphoma. The calculated risk for systemic lymphoma within the first 10 or 15 years after diagnosis was 4% and 12%, respectively, in contrast with the 80% at 15 years in a study of Cabanillas et al.21 However, in that study, only patients with LyP who had initially been misdiagnosed or had another type of malignant lymphoma were included, suggesting that the striking difference between both studies results from differences in patient selection. As in earlier studies on smaller groups of patients,25,28,29 risk factors for disease progression could not be found.Therapy. Because a curative therapy is unavailable and none of the available treatment modalities affects the natural course of the disease, the short-term benefits of active treatment should be balanced carefully against the potential side effects.5,20 We believe that in patients with relatively few and nonscarring lesions, active treatment is not necessary. In patients with cosmetically disturbing lesions (eg, scarring lesions or many lesions), low-dose oral methotrexate (5 to 20 mg/wk) or PUVA therapy can be administered to reduce skin lesions.20,27,30 When larger skin tumors develop in the course of LyP, spontaneous remission can be awaited for 4 to 6 weeks. If spontaneous resolution does not occur, such lesions can be excised or treated with radiotherapy. Whether such isolated skin tumors developing in the course of LyP should be considered progression to CD30+ LTCL is debatable. Primary cutaneous CD30+ lymphoproliferations in children. Of the 12 children with LyP in this study, 3 had large, rapidly growing ulcerating lesions in addition to papular lesions. Because of this distressing clinical presentation suggesting aggressive lymphoma, multiagent chemotherapy was first considered in all 3 children. However, because the histologic appearance was highly suggestive of LyP and staging procedures did not show any evidence of extracutaneous disease, it was decided to wait for several weeks. In all 3 patients the larger skin lesions disappeared completely within 2 to 3 months, whereas the papular lesions continued to develop. This illustrates that the physician should be cautious before using aggressive chemotherapy to treat children with skin-limited CD30+ lymphoproliferations because they often simply have LyP (12 of 13 patients younger than 20 in this study). A short period of watchful waiting is warranted and may avert unnecessary treatment. Previous studies also report an indolent course for children with LyP.28,31,32 Guidelines for diagnosis, management, and treatment The central problem in the correct diagnosis and classification of this group of diseases is that there are no reliable histologic criteria to differentiate between the different types of primary and secondary cutaneous CD30+ lymphoproliferations. Patients with cutaneous CD30+ LTCL may show an LyP-like histology, whereas patients with the characteristic clinical presentation and clinical behavior of LyP may show large sheets of CD30+ cells with only few infiltrating reactive cells (LyP, type C). Consequently, the histologic diagnosis should always be considered as a differential diagnosis and should never serve as a basis for therapeutic decisions. The definite diagnosis should always be based on a combination of histological and clinical criteria. This diagnostic process involves 2 steps (Figure 7). The first and most important question is whether it is a primary or a secondary cutaneous CD30+ lymphoproliferation. The second question is whether it is LyP or primary cutaneous CD30+ LTCL.
Step 1: primary or secondary cutaneous CD30+ lymphoma? Confronted with a patient with the histologic diagnosis of a cutaneous CD30+ lymphoproliferation, distinctions should first be made among primary cutaneous CD30+ lymphoproliferation, cutaneous CD30+ lymphoma secondary to MF (or another type of CTCL), and skin localizations of a systemic CD30+ (anaplastic) LTCL. Cutaneous CD30+ lymphomas secondary to MF can generally be recognized easily because of the presence of prior or concurrent patches or plaques with the typical histology of MF. If no extracutaneous disease can be demonstrated, patients can be treated routinely as for tumor-stage MF, primarily with skin-directed therapies such as local radiotherapy or total skin electron beam irradiation. Patients with skin and extracutaneous localizations require multiagent chemotherapy and generally have an unfavorable prognosis. MF with transformation into a CD30+ LTCL should not be confused with MF with concurrent LyP, a combination observed in 9% of patients with LyP (current study) and in approximately 3% of patients with MF33 and carrying, almost without exception, a very good prognosis.25,33,34 Step 2: management of primary cutaneous CD30+ lymphoproliferations. Previous studies emphasize the many similarities between primary cutaneous CD30+ LTCL and LyP, suggesting that these are closely related conditions within a continuous spectrum.4,5 Distinction between these 2 ends of the spectrum was considered important because patients with CD30+ LTCL were thought to be at much higher risk for extracutaneous disease than patients with LyP and, unlike patients with LyP, always required adequate staging and even systemic chemotherapy if they had multifocal skin lesions.5,11 However, the results of the current study suggest that the differences in disease progression and survival between both groups are smaller than anticipated previously (Table 2). In addition, skin relapses after systemic chemotherapy were not only observed in patients with LyP but also in all patients with skin-limited CD30+ LTCL,22 which argues against the use of systemic chemotherapy for patients with only skin lesions. Taken together, our observations indicate that the choice of treatment should be based above all on the size, the extent, and the clinical behavior of the skin lesions and not as much on the diagnosis of CD30+ LTCL or LyP (Figure 6).
Submitted November 29, 1999; accepted February 8, 2000.
Reprints: Rein Willemze, Leiden University Medical Center, Department of Dermatology, B1-Q-93, P.O. Box 9600, 2300 RC Leiden, The Netherlands; e-mail: willemze.dermatology{at}lumc.nl or rein.willemze{at}planet.nl.
The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked "advertisement" in accordance with 18 U.S.C. section 1734.
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R. Willemze, E. S. Jaffe, G. Burg, L. Cerroni, E. Berti, S. H. Swerdlow, E. Ralfkiaer, S. Chimenti, J. L. Diaz-Perez, L. M. Duncan, et al. WHO-EORTC classification for cutaneous lymphomas Blood, May 15, 2005; 105(10): 3768 - 3785. [Abstract] [Full Text] [PDF]
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J. E. Janik, J. C. Morris, S. Pittaluga, K. McDonald, M. Raffeld, E. S. Jaffe, N. Grant, M. Gutierrez, T. A. Waldmann, and W. H. Wilson Elevated serum-soluble interleukin-2 receptor levels in patients with anaplastic large cell lymphoma Blood, November 15, 2004; 104(10): 3355 - 3357. [Abstract] [Full Text] [PDF]
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Lymphomatoid Papulosis: Reappraisal of Clinicopathologic Presentation and Classification Into Subtypes A, B, and C Arch Dermatol, April 1, 2004; 140(4): 441 - 447.
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T. Nijsten, C. Curiel-Lewandrowski, and M. E. Kadin Lymphomatoid Papulosis in Children: A Retrospective Cohort Study of 35 Cases Arch Dermatol, March 1, 2004; 140(3): 306 - 312. [Abstract] [Full Text] [PDF]
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M. E. Kadin Extracutaneous origin of lymphomatoid papulosis Blood, November 15, 2003; 102(10): 3468 - 3468. [Full Text] [PDF]
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Pruritic Plaque in a 46-Year-Old Woman--Diagnosis Arch Dermatol, August 1, 2003; 139(8): 1075 - 1080. [Full Text] [PDF]
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J. Willers, R. Dummer, W. Kempf, T. Kundig, G. Burg, and M. E. Kadin Proliferation of CD30+ T-Helper 2 Lymphoma Cells Can Be Inhibited by CD30 Receptor Cross-Linking with Recombinant CD30 Ligand Clin. Cancer Res., July 1, 2003; 9(7): 2744 - 2754. [Abstract] [Full Text] [PDF]
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M. Kleinhans, A. Tun-Kyi, M. Gilliet, M. E. Kadin, R. Dummer, G. Burg, and F. O. Nestle Functional expression of the eotaxin receptor CCR3 in CD30+ cutaneous T-cell lymphoma Blood, February 15, 2003; 101(4): 1487 - 1493. [Abstract] [Full Text] [PDF]
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 I N Farstad, F-E Johansen, L Vlatkovic, J Jahnsen, H Scott, O Fausa, A Bjorneklett, P Brandtzaeg, and T S Halstensen Heterogeneity of intraepithelial lymphocytes in refractory sprue: potential implications of CD30 expression Gut, September 1, 2002; 51(3): 372 - 378. [Abstract] [Full Text]
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J. L. Kutok and J. C. Aster Molecular Biology of Anaplastic Lymphoma Kinase-Positive Anaplastic Large-Cell Lymphoma J. Clin. Oncol., September 1, 2002; 20(17): 3691 - 3702. [Abstract] [Full Text] [PDF]
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M. E. Kadin T-Cell Clonality in Pityriasis Lichenoides: Evidence for a Premalignant or Reactive Immune Disorder? Arch Dermatol, August 1, 2002; 138(8): 1089 - 1090. [Full Text] [PDF]
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M. Steinhoff, M. Hummel, I. Anagnostopoulos, P. Kaudewitz, V. Seitz, C. Assaf, C. Sander, and H. Stein Single-cell analysis of CD30+ cells in lymphomatoid papulosis demonstrates a common clonal T-cell origin Blood, June 28, 2002; 100(2): 578 - 584. [Abstract] [Full Text] [PDF]
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Top
Abstract
Introduction
,
EMA
suggesting that the
appearance of skin lesions in CD30+ ALCL is a poor
prognostic sign.