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© 2001 American Society for Clinical Oncology Primary Cutaneous Non-Hodgkin’s Lymphoma of Ann Arbor Stage I: Preferential Cutaneous Relapses but High Cure Rate With Doxorubicin-Based TherapyFrom the Departments of Lymphoma and Myeloma, Blood and Marrow Transplantation, Hematopathology, Dermatology, and Radiation Oncology, University of Texas M.D. Anderson Cancer Center, Houston, TX. Address reprint request to Andreas H. Sarris, MD, PhD, Department of Lymphoma-Myeloma, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 68, Houston, TX 77030; email asarris{at}mail.mdanderson.org
PURPOSE: Establish frequency, presenting features, response and relapse patterns, and outcome of primary cutaneous non-Hodgkin’s lymphoma (PCNHL). PATIENTS AND METHODS: Review of untreated patients, older than 16 years, presenting between 1971 and 1993 with cutaneous lymphoma, not mycosis fungoides, and Ann Arbor stage I. RESULTS: We identified 46 patients, 27 males, with median age of 57 years. Treatment was radiotherapy in 10 patients, doxorubicin-based therapy in 33 patients that was followed by radiotherapy in 25 patients, and other combination with radiotherapy in one patient. The complete response rate was 95%. After a median follow-up of 140 months (range, 61 to 284 months), 18 patients have relapsed, and 14 have died from lymphoma. The first failure was exclusively cutaneous in 50% of relapses. For the 44 treated patients, progression-free survival (PFS; actuarial ± SE) was 61% ± 7% and survival was 58% ± 9% at 12 years. For the 18 patients with diffuse large B-cell lymphoma, after doxorubicin-based regimens, PFS was 71% ± 12% (P = .0003) versus 0% after radiotherapy; survival was 77% ± 12% versus 25% ± 22% (P = 004), respectively. For the nine patients with follicular center-cell lymphoma treated with combined modality, the 12-year PFS was 89% ± 11% and survival 70% ± 18%. CONCLUSION: PCNHL is rare, and its first relapse is exclusively cutaneous in 50% of patients. Patients with diffuse large B-cell lymphoma are curable with doxorubicin-based regimens but not with radiotherapy. Prospective studies in PCNHL should define the cytogenetics, the basis for cutaneous tropism, the prognosis of histologic subtypes, and the role of radiotherapy.
PRIMARY CUTANEOUS non-Hodgkin’s lymphoma (PCNHL), excluding mycosis fungoides and its variants, is a heterogeneous group of lymphomas with a reported frequency in the literature of approximately 5%.1 However, the optimal treatment of PCNHL limited to skin and sufficiently localized to be classified as Ann Arbor stage IE remains controversial. The European Organization for Research and Treatment of Cancer has proposed a classification for cutaneous lymphomas based on clinical, histologic, and immunophenotypic criteria.2 The presenting clinical and laboratory characteristics as well as the results of therapy of PCNHL have been the subject of several publications before and after that proposal. Of 21 patients with stage I PCNHL of aggressive histology, 14 were treated with radiotherapy, but nine relapsed within 2 years. Only six of these 21 patients were treated with doxorubicin-based regimens, but their progression-free survival (PFS) was not reported.3 Another series analyzed 158 patients collected from a Cutaneous Lymphoma registry. However, it is unclear what was the method of accrual of the patients. In addition, 11% of them were not treated at all for lymphoma, and the treatment of the remaining patients was not described. Despite this heterogeneity, the authors reported the survival of all patients, including the untreated ones, irrespective of the cause of death.4 Another series analyzed 47 patients with CD30-positive large-cell lymphomas.5 Because spontaneous complete or partial regressions of the lymphoma were observed in seven of the patients, it is unclear whether lymphomatoid papulosis was rigorously excluded.6 In addition, therapy was diverse, including surgical excision in 23 patients, surgical excision and radiotherapy in four patients, and combination chemotherapy in six patients. However, it is unclear how many patients were treated with doxorubicin-based regimens. Relapses were observed in 27 of these 47 patients, but actuarial PFS was not presented for each different treatment group. However, it is possible that primary CD30-positive cutaneous lymphoma has good outcome because anaplastic large-cell lymphoma, even of advanced Ann Arbor stages, has been reported to have better or comparable outcome with other NHLs.7,8 Primary cutaneous B-cell lymphomas of follicle center-cell origin have been reported to have worse prognosis when localized to the lower extremity than in other sites.9 Only eight of these 55 patients had leg lymphomas, and treatment was heterogeneous; 40 patients were treated with radiotherapy, and 15 with different combination regimens, which included doxorubicin only in 11 patients. The reported end point was survival at 2 years, which is too short for indolent lymphomas. Neither survival nor PFS were reported for patient groups treated with equivalent regimens. Santucci et al10 presented an analysis of 83 patients with PCNHL of B-cell origin. These patients were identified from a pathology archive, and it is unclear how many of them were previously untreated at the time of entry onto that database. Treatment was heterogeneous, and PFS was not reported according to therapy and histologic subtype. Several questions linger, even after the publication of these data. For some investigators, the definition of PCNHL requires no progression to extracutaneous sites for 6 months after diagnosis based on adequate staging procedures.2,11-14 This would obviously introduce a positive selection bias by excluding patients with aggressive disease or with disease that does not respond to therapy. Others reported only survival but not always in an actuarial manner.2,4,5,9,12 However, survival is not an optimal end point because it can be affected by the initial and the postrelapse therapy, which were often variable or were not even specified in some series. In general, therapy is less intensive and does not include doxorubicin in older patients.15 Survival is also always limited by the immutable natural limit on life expectancy. Thus, it should not be surprising that patients with lymphomas of the leg (median age, 76 to 80 years, probably exceeding life expectancy in the parent populations) had shorter survival than patients with lymphomas arising in trunk (median age, 63 years) or head (median age, 46 to 63 years).4,9,12,15 Because the PFS of patients with PCNHL who have been treated with state-of-the-art therapy is unclear, we decided to retrospectively analyze our experience with this disease. Our objective was to define the frequency, clinical features, response to therapy, patterns of relapse, PFS, and survival of adults with PCNHL, excluding mycosis fungoides and its variants.
We searched the Institutional Lymphoma Planning Clinic Database and the Lymphoma Investigational Protocol Database for the time interval from 1971 to 1993 for patients with Ann-Arbor stage I NHL that was limited to skin. These databases contain all new, previously treated or untreated lymphoma patients presenting to the institution. Patients were included in this study only if: (1) they presented with skin lesion(s); (2) their cutaneous lesions were sufficiently localized to fulfill criteria for Ann Arbor stage I; (3) they had received no prior therapy for the lymphoma; (4) they had no prior or concurrent mycosis fungoides, Sézary Syndrome, or any prior lymphoma at any site; (5) they were older than 16 years; and (6) they did not have lymphomatoid papulosis, a CD30-positive lymphoproliferative disease of CD4-positive lymphocytes, characterized by frequent recurrences and spontaneous regressions.6 After review of all available slides, the diagnosis was revised according to the Working Formulation.16 Because tissue blocks were not always available for immunophenotyping, diagnosis according to the Revised European-American Lymphoma (REAL) classification was not possible in all cases.17 All available records were reviewed to verify presentation, staging, treatment, and outcome. Staging evaluation included physical examination, bone marrow aspirates and biopsies, and chest radiographs. Computed tomography of chest, abdomen, and pelvis were performed in 37 patients. Computed tomography of the head and neck was also performed in five patients. Bipedal lymphangiogram was performed in 41 patients. In nine patients presenting before the introduction of computed tomography, the radiographic evaluation of thoracic and abdominal involvement was based on tomograms and lymphangiograms. These findings were confirmed by negative exploratory laparotomy in five of these patients. The Ann Arbor stage18 and the treatment were determined after review of all clinical, laboratory, pathologic, and radiographic data in a multidisciplinary conference attended by hematologists, medical oncologists, radiation oncologists, hematopathologists, and diagnostic radiologists. Treatment according to standard or investigational regimens was based on risk assessment according to prognostic criteria and was administered either at the University of Texas M.D. Anderson Cancer Center (MDACC) or at the MDACC and in the community by collaborating physicians. However, all response determinations were performed at MDACC. A signed informed consent was obtained before all procedures and before all investigational therapy, as required by the investigational review board. Complete remission (CR) was defined as absence of disease for at least 1 month, as determined by physical examination and appropriate laboratory and imaging studies. Partial response (PR) was defined as more than 50% reduction of tumor area measurable in two dimensions. Progressive disease was defined as enlargement (> 25%) of an existing site of disease or the development of disease in a previously uninvolved site. Primary treatment failure was defined as failure to achieve either CR or PR during initial therapy. Relapse was defined as disease progression at least 1 month after CR or PR. PFS was measured from the beginning of treatment to the time of primary treatment failure or of relapse. All other events were censored, including deaths from toxicity or unrelated causes. Survival was measured from start of treatment to last follow-up or to death from any cause. The actuarial probability of PFS and overall survival was determined by the method of Kaplan-Meier,19 and the log-rank test was used to compare differences between groups of patients.
Clinical Features Between 1971 and 1993, a total of 2,670 previously untreated patients with non-Hodgkin’s lymphoma presented to MDACC. Forty-six patients met our criteria for stage IE PCNHL. Thus PCNHL constituted 1.7% of all untreated non-Hodgkin’s lymphomas presenting to our institution. The initial clinical and laboratory features of these 46 patients are listed in Table 1. The median size of the skin lesions in their greatest diameter was 3 cm (range, 1 to 10 cm). The median duration of skin lesions before the establishment of diagnosis was 3 months, but ranged from 1 month to 3 years.
Histology and Phenotype All slides from these 46 patients were reviewed and classified according to the Working Formulation without knowledge of presentation, treatment, or clinical course. Most patients had diffuse large-cell or diffuse large-cell immunoblastic lymphoma, although follicular lymphomas and other histologies were also observed. Because these patients presented over many years, tissue blocks were not always available for immunohistochemistry and reclassification according to the REAL classification. Immunocytochemistry was performed on 37 patients, of whom six had T-cell and 31 had B-cell phenotype. According to the REAL classification, the most common histology was diffuse large B-cell lymphoma followed by follicular center-cell lymphomas (Table 1). Of the five patients with diffuse large-cell immunoblastic lymphoma, defined according the Working Formulation, four had available immunophenotypic data and fulfilled the REAL classification criteria for diagnosis of CD30-positive anaplastic large-cell lymphoma. The remaining patient fulfilled the morphologic criteria for anaplastic large-cell lymphoma but did not have immunophenotypic data. Because spontaneous regressions had not been observed in any of our patients, including the patients with anaplastic morphology, we retrospectively excluded the diagnosis of lymphomatoid papulosis among patients with CD30-positive anaplastic large-cell lymphomas.6
Treatment Of the 44 treated patients, 33 received doxorubicin-based therapy. Combination chemotherapy regimens were assigned according the Working Formulation because the study period ended in 1993, just before the publication of the REAL classification. Regimen included cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) with bleomycin (CHOP-B)20 in 25 patients; CHOP alternating with etoposide, mitoxantrone, vincristine, and prednisone (OPEN)21 in five patients; cyclophosphamide, mitoxantrone, vincristine, and prednisone (CNOP)22 in one patient; CHOP-B alternating with cisplatin, high-dose cytarabine, and dexamethasone23 in one patient; and alternating triple therapy consisting of doxorubicin, cisplatin, cytarabine, and methylprednisolone, alternating with methotrexate, leucovorin, doxorubicin, vincristine, bleomycin, cyclophosphamide, and methylprednisolone, and with ifosfamide, mesna, mitoxantrone, and etoposide in one patient24; and cyclophosphamide, vincristine, and prednisone in one patient with indolent lymphoma.25 For the purpose of this analysis CNOP was considered a doxorubicin-based regimen. Patients with aggressive histologic types of non-Hodgkin’s lymphoma (diffuse large-cell, diffuse large-cell immunoblastic, and follicular large-cell in the Working Formulation) were treated with doxorubicin-based regimens according to the predicted risk of failure estimated from clinical prognostic models in use at the time of diagnosis.26,27 Poor-risk patients received alternating triple therapy, and good-risk patients received CHOP/OPEN or CHOP-B with or without radiotherapy. Patients with indolent histologies, defined according the Working Formulation, received CHOP-B and radiotherapy (three patients), except the one patient who received cyclophosphamide, vincristine, and prednisone and radiotherapy.28 After January 1980, radiotherapy was administered at the end of chemotherapy to 25 patients according to specific investigational protocols or at the discretion of the treating physicians. Median dose was 40 Gy (range, 30 to 50 Gy).
Response to Treatment
Failure-Free Survival and Survival
In our institution, radiotherapy was used as a curative therapy for patients with localized aggressive NHL during the 1970s. However, there was a policy change in 1980, after when chemotherapy or combined-modality therapy but not radiotherapy alone was used for the treatment of localized aggressive lymphomas. Therefore, in this series, there was no selection of patients for radiotherapy or chemotherapy. When patients were categorized according to the REAL classification, the 12-year PFS of patients with diffuse large B-cell lymphomas was significantly higher after chemotherapy or combined-modality therapy than after radiotherapy alone (actuarial ± SE, 71% ± 12% v 0%, respectively; P = .0003, Fig 2A). The overall survival for these groups was 77% ± 12% versus 25% ± 22%, respectively (P = .04, Fig 2B). According the REAL classification, there were nine patients with follicular center-cell lymphomas all of who were treated with doxorubicin-based combined-modality therapy on basis of protocols. Their 12-year PFS was 89% ± 11% (Fig 3A), and the overall survival was 70% ± 18% (Fig 3B).
There were only three patients with lymphoblastic lymphoma, two with B-cell and one with T-cell immunophenotype. They all relapsed after combined-modality therapy. There were four patients with anaplastic large-cell lymphoma; one did not receive any lymphoma therapy because of coexisting lung and prostatic carcinomas. One patient received only radiotherapy and relapsed. Two patients received doxorubicin-based therapy with added adjuvant radiotherapy in one patient, who later relapsed. There was one patient with peripheral diffuse large T-cell lymphoma who was treated with three cycles of CHOP and radiotherapy, but the patient relapsed and died of lymphoma.
Patterns of Relapse
We present our retrospective analysis of patients with Ann Arbor stage IE PCNHL, excluding mycosis fungoides and its variants. These patients were identified from a database including all patients with lymphoma presenting to our institution. We also did not require that disease remain localized for 6 months to be called PCNHL. We thus included all patients and eliminated most selection biases. In our patient population, PCNHL comprised 1.7% of all non-Hodgkin lymphomas. Histologically, most PCNHL were diffuse large B-cell lymphomas, a few were follicular center-cell, and rare cases were anaplastic large-cell or lymphoblastic lymphoma. In this study, all nine follicular center-cell lymphomas had unequivocal follicular architecture in the skin biopsy specimen. However, in a strict sense, we cannot exclude follicular center-cell derivation in all skin biopsies with a diffuse large B-cell pattern. In the years before 1980, patients with localized PCNHL were treated only with radiotherapy. However, after 1980 the treatment was changed to doxorubicin-containing regimens with adjuvant radiotherapy in many cases. This policy eliminated most biases arising from selection of patients for a specific therapy, as shown by the similar clinical presentation of patients treated with radiotherapy or doxorubicin-containing regimens. For patients with diffuse large B-cell lymphomas, doxorubicin-based therapy (with or without radiotherapy) resulted in high cure rates. These rates were comparable with the rates previously reported for doxorubicin-treated Ann Arbor stage I non-Hodgkin’s lymphomas with aggressive histologies of all sites.29-33 A recent series of PCNHL included 21 patients with Ann Arbor stage IE PCNHL, of whom only six were treated with doxorubicin-containing regimens. However, their PFS was not reported.3 Radiotherapy was not curative for diffuse large B-cell lymphomas when used as the sole therapeutic modality in our series before 1980. Our results seem comparable with reported radiotherapy outcomes; for PCNHL, nine of 14 patients treated only with radiotherapy relapsed, but actuarial PFS was not reported.3 Other series of localized PCNHL with aggressive lymphomas included untreated and variably treated patients and reported survival but not PFS.4 For aggressive PCNHL, our approach and results parallel the evolving concepts and results of therapy for early Ann-Arbor stage of all sites. Initially, these patients were treated with radiotherapy, often after exploratory laparotomy, with reported cure rates ranging from 0% to 100%.34-37 After CHOP was found to be effective in advanced-stage NHL,38 it was introduced in the treatment of early-stage NHL. The cure rate for Ann Arbor stage I ranged from 94% to 100%, and for stage II, it ranged from 72% to 78%.29-33 The benefit of radiotherapy after an abbreviated or a full course of chemotherapy was investigated by two randomized studies of non-Hodgkin lymphoma patients with Ann Arbor stages I and II. Both series demonstrated that the addition of radiotherapy to CHOP resulted in statistically superior PFS.39,40 However, it is unclear whether radiotherapy is required for all patients in the absence of bulky disease and when treatment was assigned on the basis of prognostic factors, as was done in our series. Retrospective analysis of PFS for our chemotherapy-treated patients with all aggressive histologies (according to the Working Formulation) did not reveal a benefit for adjuvant radiotherapy (data not shown). However, because of the small number of patients and the retrospective nature of the analysis, the optimal therapy of diffuse large B-cell PCNHL and the role of radiotherapy in its management should be defined by prospective studies. Our patients with follicular center-cell lymphomas had excellent PFS and survival after doxorubicin-based regimens combined with radiotherapy. This approach was used in our institution for the treatment of patients with indolent lymphoma with extranodal involvement, including skin. The PFS seen here for PCNHL is comparable with the PFS of localized disease of all sites.28 Our data cannot be easily compared with other series of variably treated patients, which only report survival3 or 2-year disease-free survival.4 Additional work is clearly required to determine the optimal therapy for patients with follicular center-cell PCNHL of Ann Arbor stage I because radiotherapy has been reported to be curative for localized follicular lymphomas. There were too few patients with anaplastic large-cell lymphoma, lymphoblastic lymphomas, or small lymphocytic lymphomas in our series to allow definitive conclusions and comparison with published data.5 The lymphoblastic lymphomas relapsed when treated with CHOP-like therapy. On the basis of their biology, they should be probably treated like acute lymphoblastic leukemia. Primary cutaneous anaplastic large-cell lymphomas have been reported to have good survival with radiotherapy. However, prospective studies would be needed to define their optimal therapy. The similarity of outcomes between PCNHL (observed in our series) and nodal diffuse large B-cell or follicular center-cell lymphomas, as reported in the literature, suggests that a separate classification system for PCNHL is not justified exclusively on the basis of this site of disease involvement. However, future work should determine whether PCNHLs are associated with unique chromosomal rearrangements not seen in their nodal counterparts, which might justify the creation of new entities.
In our series, PCNHL exhibited a remarkable predilection for cutaneous involvement during the first relapse or progression. The first relapse of PCNHL involved cutaneous sites in 72% and was exclusively cutaneous in 50% of relapsing patients. This tropism has been previously reported,10,14,41-43 but its molecular basis remains undefined. Normal B and T lymphocytes recirculate extensively in blood and tissues, but they tend to home to organs where they first encountered antigen. This recirculation is accomplished by complex interactions involving adhesion molecules expressed on lymphocytes, endothelial cells, and parenchymal cells, and chemokines secreted by nonlymphoid cells.44 Homing to skin underlies the epidermotropism of mycosis fungoides, which is characterized by multiple cutaneous relapses before eventual visceral dissemination. Interferon- We conclude that Ann Arbor stage IE PCNHL, although uncommon (1.7% of all non-Hodgkin’s lymphomas in our institution), has a unique clinical behavior characterized by cutaneous tropism; its first relapse involved the skin in 72% and was exclusively cutaneous in 50% of our relapsing patients. The PFS of patients with diffuse large B-cell or follicular center-cell PCNHL seems similar to that of similarly treated patients with nodal lymphomas of the same Ann Arbor stage and histology. Prospective studies should further define the pathologic and molecular characteristics of PCNHL, explore the mechanism for its cutaneous tropism, define the outcome of follicular, anaplastic, and other histologic subtypes after uniform therapy, and clarify the role of radiotherapy in the management of this disease.
Supported in part by Cancer Center Support grant no. CA-16672 to the University of Texas M.D. Anderson Cancer Center. We thank the nursing staff, social workers, pharmacists, and Fellows of the Lymphoma-Myeloma Department who cared for these patients over the years. We also thank Ms. Joyce Palmer for assistance with the manuscript.
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Copyright © 2001 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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TOP
ABSTRACT
INTRODUCTION
and tumor necrosis factor-
might be involved in this tropism because they induce epidermal keratinocytes to secrete interferon-inducible protein-10,
