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Blood, Vol. 93 No. 11 (June 1), 1999:
pp. 3637-3642
Prognostic Factors in Primary Cutaneous Lymphomas Other Than Mycosis
Fungoides and the Sézary Syndrome
By
F. Grange,
G. Hedelin,
P. Joly,
M. Beylot-Barry,
M. D'Incan,
M. Delaunay,
L. Vaillant,
M.F. Avril,
J. Bosq,
J. Wechsler,
S. Dalac,
C. Grosieux,
N. Franck,
E. Esteve,
C. Michel,
C. Bodemer,
B. Vergier,
L. Laroche, and
M. Bagot for the French Study Group on Cutaneous
Lymphomas (FSGCL)
From the Service de Dermatologie, Hôpital Pasteur, Colmar;
Département d'Epidémiologie et de Santé Publique,
Université Louis Pasteur, Strasbourg; Clinique Dermatologique,
Hôpital Charles Nicolle, Rouen, Institut National de la Sante et
de la Recherche Medicale (INSERM) Unite 519; Service de Dermatologie,
Hôpital du Haut Lévêque, Pessac; Service de
Dermatologie, Hôtel Dieu, Clermont-Ferrand; Unité de
Dermatologie-Cancérologie, Hôpital Pellegrin, Bordeaux;
Service de Dermatologie, Hôpital Trousseau, Tours; Service de
Dermatologie, Institut Gustave Roussy, Villejuif; Département
d'Histopathologie, Institut Gustave Roussy, Villejuif; Department de
Pathologie, Hôpital Henri-Mondor, Créteil; Service de
Dermatologie, Hôpital du Bocage, Dijon; Service de Dermatologie,
Hôpital Robert Debré, Reims; Service de Dermatologie,
Hôpital Tarnier, Paris; Service de Dermatologie, Hôpital
Porte Madeleine, Orléans; Service de Dermatologie,
Hôpital du Moenschberg, Mulhouse; Service de Dermatologie,
Hôpital Necker, Paris; Service d'Anatomie Pathologique,
Hôpital du Haut Lévêque, Pessac; Service de
Dermatologie, Hôpital Avicenne, Bobigny; and Service de
Dermatologie, Hôpital Henri-Mondor, Créteil, France.
 |
ABSTRACT |
Prognostic studies of primary cutaneous lymphomas (PCL) other than
mycosis fungoides (MF) and the Sézary syndrome (SS; non-MF/SS PCL) have been mainly performed on subgroups or on small numbers of
patients by using univariate analyses. Our aim was to identify independent prognostic factors in a large series of patients with non-MF/SS PCL. We evaluated 158 patients who were registered in the
French Study Group on Cutaneous Lymphomas database from January 1, 1986 to March 1, 1997. Variables analyzed for prognostic value were: age;
sex; type of clinical lesions; maximum diameter, location, and number
of skin lesions; cutaneous distribution (ie, local, regional, or
generalized); prognostic group according to the European Organization
for Research and Treatment of Cancer (EORTC) classification for PCL; B-
or T-cell phenotype; serum lactate dehydrogenase (LDH) level; and B
symptoms. Univariate and multivariate analyses were performed using a
model of relative survival. Forty-nine patients (31%) died. The median
relative survival time was 81 months. In univariate analysis, EORTC
prognostic group, serum LDH level, B symptoms, and variables related to
tumor extension (ie, distribution, maximum diameter, and number of skin
lesions) were significantly associated with survival. When these
variables were considered together in a multivariate analysis, EORTC
prognostic group and distribution of skin lesions remained
statistically significant, independent prognostic factors. This study
confirms the good predictive value of the EORTC classification for PCL
and shows that the distribution of skin lesions at initial evaluation
is an important prognostic indicator.
© 1999 by The American Society of Hematology.
| |
INTRODUCTION |
PROGRESS IN therapeutic approach of
Non-Hodgkin lymphoma (NHL) requires an accurate estimation of
prognosis. Survival analyses have been performed in large series of
patients with NHL (mainly nodal lymphomas) to identify prognostic
factors.1-5 Main factors found to be associated with a poor
prognosis were old age, low performance status, presence of B
(systemic) symptoms, increased serum lactate dehydrogenase (LDH) level,
aggressive histological subtypes, and tumor extension. Methods to
assess the tumor extension were variable and included the Ann Arbor
classification, the evaluation of tumor bulk, largest diameter of
tumors, and number of nodal or extranodal sites of the disease.
The evaluation of overall prognosis and prognostic factors of primary
cutaneous lymphomas (PCL) other than mycosis fungoides (MF) and the
Sézary syndrome (SS) met some difficulties. First, there has been
confusion between PCL defined by the absence of extracutaneous disease
at the time of diagnosis and nodal lymphomas presenting with skin
tumors. Second, some parameters associated with a poor prognosis in
nodal lymphomas, such as B symptoms or increased LDH level, are rarely
present in PCL. Third, there is no consensus for evaluating the tumor
extension in PCL other than MF and SS (non-MF/SS PCL). Finally,
histological classification schemes used for nodal NHL seemed
inadequate to classify PCL correctly. In particular, different types of
PCL classified as "high-grade lymphomas," according to the
updated Kiel classification6 and to the Working
Formulation,7 were found to have an indolent clinical
course.8-10 These findings led the European Organization for Research and Treatment of Cancer (EORTC) Cutaneous Lymphoma Project
Group to provide precise definitions of different subtypes of PCL,
using a combination of clinical, histological, and immunophenotypic criteria, and to assign them to different prognostic
groups.11,12 This resulted in a new classification for PCL
whose validity was supported by a number of prognostic analyses in
subgroups of PCL8,10,13-17 and by survival data of patients
included in the registry of the Dutch Cutaneous Lymphoma Working
group.12 The aim of our study was to test the clinical
validity of the EORTC classification in an independent series
of patients and to identify main prognostic factors of survival in
non-MF/SS PCL.
| |
PATIENTS AND METHODS |
Patients included in the registry of the French Study Group on
Cutaneous Lymphomas (FSGCL) from January 1, 1986 to March 1, 1997 were
selected for analysis if they met the following criteria: (1) diagnosis
of cutaneous lymphoma other than classical MF, SS, and lymphomatoid
papulosis (LyP), and (2) absence of extracutaneous disease detected by
a comprehensive staging procedure at diagnosis. In each case, the
diagnosis was made by an expert panel of pathologists and
dermatologists during one of the quarterly meetings of the FSGCL and
was based on a combination of clinical, histological, and
immunophenotypical data. Classical criteria were used for the diagnosis
of MF and SS.12 Clinical and histological data of all cases
of MF undergoing transformation into a diffuse large-cell lymphoma18 were separately reviewed for distinction from
non-MF primary cutaneous large T-cell lymphomas. Primary cutaneous
pleomorphic small T-cell lymphomas were differentiated from classical
MF using criteria that have been previously reported.15,17
Primary cutaneous CD30-positive large T-cell lymphomas were
differentiated from LyP on the basis of clinical and histopathologic
data, as it was recommended.8,12,19,20 After exclusion of
patients with MF, SS, and LyP, information regarding staging at
diagnosis was reviewed for 204 cases. Staging procedure at diagnosis
included physical examination (100% of cases), blood cell count and
routine laboratory tests (100%), chest radiograph or thoracic computed tomographic (CT) scan (100%), abdominal ultrasound tomography or
thoraco-abdominal CT scan (100%), and bone-marrow biopsy (93%). Nodal
biopsies were only performed when enlarged lymph nodes were present
(14%). Forty-one patients were excluded from further analysis because
they had extracutaneous disease detected at diagnosis. Five patients
were excluded because they consulted only once for initial advice in a
reference center and were thereafter lost to follow-up. One hundred
fifty-eight patients met the inclusion criteria and were selected for analysis.
Data collection.
Variables analyzed for prognostic value were: age at diagnosis; sex;
type of clinical lesions (plaques, nodules, or tumors); anatomic site
(head and neck, upper limb, anterior aspect of the trunk, posterior
aspect of the trunk, or lower limb); largest diameter and number of
skin lesions; cutaneous distribution (namely "local" when skin
lesions involved a surface less than or equal to 100 cm2 on
one anatomic site, "regional" for a surface greater than 100 cm2 on one anatomic site, and "generalized" when
several anatomic sites were involved); prognostic group according to
the EORTC classification (ie, indolent, intermediate, aggressive, or
provisional, as defined in Table 1); B- or
T-cell phenotype; serum LDH level; and B symptoms. Information
regarding these variables was complete in all patients, except 8 cases
for whom LDH level at diagnosis was unknown. For the classification
according to diagnosis and EORTC prognostic groups, there was an
agreement among pathologists to use distinctive criteria that have been
proposed by Willemze et al.11,12 In particular,
differentiation between CD30-positive large T-cell lymphomas and
CD30-negative large T-cell lymphomas was based on the presence of more
or less than 75% CD30-positive large T cells. This distinction was
often easy because most CD30-negative large T-cell lymphomas had very
few (<20%) CD30-positive large T cells. Differentiation between
pleomorphic large T-cell lymphomas and pleomorphic small T-cell
lymphomas was based on the presence of more or less than 30% large
tumor cells. B-cell lymphomas composed of small centrocytes, large
centrocytes, centroblasts, and/or immunoblasts were classified as
follicle center-cell lymphomas, whatever the predominant cytological
feature. However, those located on the legs were classified separately,
as large B-cell lymphomas of the leg, if more than 50% of the
neoplastic B cells were large cells. B-cell lymphomas composed of
lymphocytes, lymphoplasmocytoid cells, and plasma cells with a
monotypic cytoplasmic Ig were diagnosed as immunocytomas. We did not
use the terms marginal zone B-cell lymphoma or mucosa-associated
lymphoid tissue lymphomas and classified all indolent B-cell lymphomas
either as follicle center-cell lymphomas or immunocytomas, as defined
above. Cases for whom a general agreement among pathologists was not
achieved were reviewed using a multihead microscope and finally
classified by consensus.
Follow-up.
Follow-up information was recorded until June 15, 1997 and included
initial therapy, achievement of a complete response, cutaneous relapse,
extracutaneous progression of the disease, and date and cause of death.
Ascertainment of vital status was 96% complete on June 15, 1997. For
the 6 patients (4%) lost to follow-up, the median follow-up time was
12 months (range, 3 to 26 months).
Statistical analysis.
Endpoint was death of the patient, whatever the cause. Survival
duration was calculated from diagnosis to date of death or censoring.
The study endpoint was June 15, 1997 for surviving patients with
complete follow-up and date last known alive for the 6 patients lost to
follow-up. Continuous variables were categorized for analysis as
indicated in Table 2. Univariate and
multivariate analyses were performed with the Relsurv
program,21 using a model of relative survival according to
Esteve et al,22 which provides an objective estimate of the
patients' survival corrected for the effects of causes of death
independent from lymphoma itself. The relative survival was estimated
using a table of general mortality by age and sex in France. Factors
significant at the 0.2 level in univariate analysis were included in a
stepwise regression multivariate analysis.
| |
RESULTS |
One hundred patients (63%) were men and 58 (37%) were women. Age
ranged from 12 to 95 years (mean: 61.5; median: 68). The other clinical
characteristics of patients at diagnosis are summarized in Tables 2 and
3. The distribution of cases according to
diagnostic and prognostic groups of the EORTC classification is shown
in Table 1. Initial therapies according to diagnosis are shown in Table
3. Eighteen patients (11%) did not receive any specific treatment
after initial evaluation, either because of a poor general condition or
because of spontaneous regression of skin lesions. Among 108 patients (69%) who achieved a complete response, 60 (56%) had no
relapse, whereas 48 (44%) experienced one or several relapses.
Nodal or visceral progression of the disease was documented in 30 patients (19%).
Forty-nine patients (31%) died. The proportion of death, whatever the
cause, was 6.7% among patients who achieved a complete response
without relapse, 33% among patients who experienced relapses, 58%
among patients who did not achieve a complete response, and 80% among
patients who developed extracutaneous disease. The median relative
survival time was 81 months. The 5-year overall relative survival rate
was 73%.
According to the referring physician, death was related to the lymphoma
in 31 of 49 cases (63%), to an unrelated cause in 9 cases (18%), and
to an unknown cause in 9 cases (18%). Twenty-five of 49 patients died
without evidence of extracutaneous progression of disease. The median
age of these patients was 77 years. Eight of them (32%) had a large
B-cell lymphoma of the leg. According to the referring physician, 40%
(10 of 25) of these patients died from lymphoma, most often from
cutaneous tumor progression, sepsis, or treatment-related toxicity. The
others died from unrelated (8 cases) or unknown causes (7 cases).
Univariate analysis of relative survival showed that the following
variables were related to death from lymphoma: a high number of skin
lesions (P = .05); a large maximum diameter of skin lesions (P = .03); a generalized distribution (P = .04);
the classification in the EORTC prognostic groups "intermediate"
or "aggressive" (P = .00001); an increased LDH level
(P = .0001); and the presence of B symptoms
(P = .0001). Age, sex, type of clinical lesions, anatomic
site, and immunophenotype (B or T) had no significant effect on death
from lymphoma. Relative survival curves for the different categories of
each variable significantly related to survival are shown in Fig
1. The 5-year survival rates,
according to diagnosis, are shown in Table
4. When multivariate analysis was
performed, only the classification in the EORTC groups
"intermediate" or "aggressive" (P = .0001) and a
generalized distribution (P = .03) had a significant effect
on death from lymphoma (Table 5).
View larger version (25K):
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| Fig 1.
Relative survival curves according to (A) number and (B)
maximum diameter of skin lesions, (C) distribution, (D) EORTC
prognostic group, (E) LDH level, and (F) B symptoms.
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View this table:
[in this window]
[in a new window]
|
Table 4.
Five-Year Survival Rates According to Diagnosis in
Present Study and in Patients From the Dutch Registry of PCL
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| |
DISCUSSION |
Few overall prognostic studies have been performed in non-MF/SS
PCL.15,23-26 The histological subtype was found to be
related to survival in most,15,23,24,26 but not
all25 studies. Some authors found the dissemination of
cutaneous lesions to be an adverse prognostic factor,24,26
whereas others did not.15,25 The serum LDH level was a
significant prognostic factor in 124 of 224,26
studies. Age,15,26 B- or T-cell phenotype,23,25 location of the disease,26 and maximum tumor
size26 were not found to have a significant effect on
survival. However, these studies only included univariate analyses in
about 50 patients or less and used various classification schemes and
inclusion criteria. In particular, some of them included patients with
extracutaneous disease detected at diagnosis,23,26 whereas
others excluded patients with initial15 or even subsequent
extracutaneous lesions within 324 or 625 months.
In the present study, primary cutaneous lymphomas were defined by the
absence of extracutaneous disease detected at the time of diagnosis. A
3- or 6-month survival time without extracutaneous progression was not
required, because exclusion of patients according to events occurring
within the first months after diagnosis and treatment may introduce
biases in the evaluation of prognosis. Furthermore, a pragmatic
approach of cutaneous lymphomas requires an evaluation of prognostic
parameters before the first treatment choice.
We found the classification according to EORTC prognostic groups to be
the most pertinent prognostic factor. The usefulness of this
classification has been first suggested by studies that have focused
attention on separate subgroups of PCL.8,10,13-17 CD30-positive large T-cell lymphomas8,9 and follicle
center-cell lymphomas10,14 were found to have an indolent
clinical course, whereas studies of small numbers of patients with
CD30-negative large T-cell lymphomas15 and large B-cell
lymphomas of the leg16 suggested that they had,
respectively, an aggressive and an intermediate behavior. These earlier
reports were supported by survival data of a larger number of patients
derived from the registry of the Dutch Cutaneous Lymphoma Working
Group.12 The present study performed on an independent
series of patients provides further evidence of the validity of this
classification. Five-year survival rates according to diagnosis
observed in this study were close to those of Dutch patients (Table 4),
and slight variations may have only resulted from chance. However, some
discrepancies may have been a result of variations in inclusion
criteria, because the 6-month interval without extracutaneous
progression was not required in our study as in Dutch survival
analyses. Lastly, survival rates may be affected by the hospital
selection of patients, even in a multicentric study, and
population-based studies would be required for a more accurate
estimation of survival in PCL. The largest difference in survival rates
between French and Dutch cases concerns pleomorphic small T-cell
lymphomas (Table 4). Dutch data suggests an intermediate prognosis,
whereas the present report shows a more indolent clinical course.
However, only 18 Dutch and 27 French cases were included in these
analyses. Further studies are required to better evaluate the prognosis
of this rare subtype of PCL.
A generalized distribution of skin lesions was the second adverse
prognostic factor found in multivariate analysis. To our knowledge, the
independent prognostic value of variables related to tumor extension
has not been demonstrated previously in non-MF/SS PCL. Although tumor
extension is an important prognostic parameter in nodal
lymphomas3 and seemed useful in PCL, there has been no
consensus for its evaluation in non-MF/SS PCL. Distribution, diameter,
and number of skin lesions, or a clinical index resulting from a
combination of these parameters are candidate variables for assessment
of skin tumor burden. Although they were significantly associated with
survival in univariate analysis, maximum diameter and number of skin
lesions had no independent prognostic value when the EORTC prognostic
group was taken into account. In addition, patients with skin lesions
localized on one anatomic site showed no difference in survival
according to the cutaneous surface involved. Finally, only the
involvement of more than one anatomic site was a significant,
independent indicator of a poor prognosis. This finding confirms and
extends results of previous univariate analyses in small series of
patients.24,26 Therefore, a generalized distribution at
diagnosis should be recorded as a pertinent prognostic reflect of tumor
extension when comparing survival data or evaluating the efficacy of
treatments in further studies.
In the present study, age was not a significant prognostic factor. This
result seems in contrast with studies that found age to be
significantly related to survival in many cancers, including lymphomas.4,5 However, it is noteworthy that age was
identified as a prognostic factor in studies that included a large
number of older patients4 and that most of these studies
used a Cox proportional-hazards model, which is unsatisfactory to
clarify the real impact of age in mortality, strictly because of the
disease.27 Using a Cox model in our series (data not
shown), we found an older age to be significantly related to death
(P < .0001). This and the result of the relative survival
analysis indicate that elderly patients had an increased mortality from
unrelated causes, but no increased risk of death from direct and
indirect consequences of lymphoma.
The presence of B symptoms and a high LDH level have been associated
with a poor prognosis in large series of patients with nodal
lymphomas.1,3-5 Although these parameters were strongly related to survival in univariate analysis in our study, they showed no
independent prognostic value in multivariate analysis, because many
patients with B symptoms or a high LDH level had an aggressive or
intermediate lymphoma according to the EORTC classification or a
generalized distribution of skin lesion (Table 6). However, these parameters remain useful
prognostic indicators that should be recorded at initial evaluation of
every patient with PCL.
Optimal treatments of non-MF/SS PCL are still to be determined on the
basis of appropriate clinical trials. However, preliminary guidelines
may be proposed with regard to previous reports and the present study.
Localized CD30-positive large T-cell lymphomas and localized indolent
B-cell lymphomas have a very good prognosis and are best treated with
radiation therapy alone. CD30-negative large T-cell lymphomas and
lymphomas involving more than one anatomic site should be
preferentially treated with chemotherapy. However, optimal
chemotherapeutic regimens have yet to be defined. Large B-cell
lymphomas of the leg have an intermediate prognosis that makes a
multiagent chemotherapy more suitable; however, radiotherapy may be
considered, especially in elderly patients with localized tumors.
Interferon or chemotherapy has been proposed for pleomorphic small
T-cell lymphomas,17 but a more accurate evaluation of clinical outcome and treatment is required for this subtype. Treatment of relapses represents a special challenge and should be carefully considered. Although overall 5-year relative survival in our study was
73%, death from lymphoma beyond 5 years was not rare, and relative
survival curves do not reach a plateau within a period of 10 years. New treatment modalities may be required to improve long-term
survival in PCL.
| |
ACKNOWLEDGMENT |
The authors thank Khaldoun Kuteifan for technical and linguistic
assistance, and the following clinicians, pathologists, and epidemiologists who actively participated in the study: B. Audhuy, S. Briançon, M.P. Cambie, A. Carlotti, A. Colson, P. Courville, P. Dechelotte, A. Durlach, S. Fraitag, Y. Fonck, J.C. Guillaume, F. Husseini, F. Maître, A. de Muret, T. Petrella, P. Schaffer, B. Schubert, P. Souteyrand, E. Thomine, and M.C. Tortel.
| |
FOOTNOTES |
Submitted September 11, 1998; accepted January 20, 1999.
Supported by a grant from the Société Française de Dermatologie.
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Address reprint requests to F. Grange, Service de Dermatologie,
Hôpital Pasteur, 39 avenue de la Liberté 68024 Colmar
Cedex, France.
| |
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INTRODUCTION