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(Radiology. 2000;214:421-425.)
© RSNA, 2000

Radiation Oncology

Hematologic Toxic Reaction to Radiation Therapy Adjuvant to Autologous Peripheral Blood Stem Cell Transplantation for Recurrent or Refractory Hodgkin Disease1

Jeffrey A. Bogart, MD, Carmen Ungureanu, MD, Samuel Ryu, MD, Chung T. Chung, MD and Kenneth W. Zamkoff, MD

1 From the Departments of Radiation Oncology (J.A.B., C.U., S.R., C.T.C.) and Medicine (K.W.Z.), State University of New York Health Science Center, 750 E Adams St, Syracuse, NY 13210. From the 1998 RSNA scientific assembly. Received March 5, 1999; revision requested April 28; revision received May 24; accepted June 14. Address reprint requests to J.A.B. (e-mail: bogartj@mailbox.hscsyr.edu).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the hematologic toxic reaction to external-beam radiation therapy after high-dose chemotherapy with peripheral blood stem cell (PBSC) support in patients with Hodgkin disease.

MATERIALS AND METHODS: A retrospective study of 30 cases of Hodgkin disease in patients who underwent high-dose carmustine, etoposide, and cyclophosphamide chemotherapy with PBSC support was performed. Thirteen patients underwent radiation therapy (28.8–39.0 Gy) a median of 45 days after PBSC repeat infusion.

RESULTS: Radiation therapy was delivered as planned, without interruption, in all patients. Five patients developed thrombocytopenia (one with grade 1 thrombocytopenia; two, grade 2; and two, grade 3) and included three with progressive disease prior to radiation therapy and two with a history of prior irradiation. None developed a bleeding complication or required transfusion support. Five patients who underwent irradiation had thrombocytopenia (three with grade 1 and two with grade 2) 100 days after PBSC repeat infusion, compared with three patients (two with grade 1 and one with grade 3) who did not undergo posttransplantation irradiation. At the most recent follow-up, no patient without evidence of disease had a platelet count of less than 100 x 109/L.

CONCLUSION: External-beam radiation therapy was well tolerated in the posttransplantation setting in patients with Hodgkin disease. Thrombocytopenia was common but was not related to clinical complications.

Index terms: Blood, platelets, 57.458, 57.47, 57.65 • Bone marrow, transplantation, 40.455 • Hodgkin disease, 99.8342 • Hodgkin disease, therapeutic radiology, 99.1299, 99.8342 • Hodgkin disease, therapy, 99.1299, 99.8342 • Stem cells


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
High-dose chemotherapy followed by autologous bone marrow or peripheral blood stem cell (PBSC) transplantation has become a routine treatment option for patients with relapsing or refractory Hodgkin disease (1–9). Even with increasingly aggressive therapy, greater than 50% of patients may experience tumor recurrence (2,3,5,10). Relapses are most often at sites of gross involvement prior to transplantation, and local radiation therapy is effective in reducing the risk of tumor relapse (10–14).

However, a survival benefit is difficult to demonstrate for patients who undergo adjuvant irradiation (12); this may be in part due to treatment-related toxic reactions. One concern has been the acute hematologic tolerance of local radiation therapy after bone marrow reconstitution in patients who often have been pretreated heavily with chemotherapy. This may compromise the ability to administer a timely, adequate radiation therapy dose (11,13).

The purpose of this study was to evaluate the hematologic toxic reaction to external-beam radiation therapy after high-dose chemotherapy in patients treated for Hodgkin disease in whom PBSCs were used to reconstitute the bone marrow.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Thirty patients with relapsing or refractory Hodgkin disease were treated at our institution with high-dose chemotherapy with PBSC support between September 1992 and September 1997. Patient, treatment, and tumor characteristics are shown in Table 1. The median age for all patients was 28 years (age range, 16–63 years). Thirteen patients were female and 17 were male.


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  		TABLE 1. Patient, Tumor, and Treatment Characteristics
 
The histologic findings were nodular sclerosis in 27 patients, lymphocyte-predominant disease in two, and mixed cellularity in one. All but one patient underwent chemotherapy as part of prior therapy for Hodgkin disease, and 13 patients underwent prior radiation therapy. Twenty-one patients underwent transplantation for relapsing disease after a complete remission, and nine patients had disease refractory to chemotherapy and never achieved a complete remission.

Twenty-seven patients underwent two or three cycles of repeat induction chemotherapy with vincristine sulfate (Oncovin; Lilly, Indianapolis, Ind) ifosfamide (Ifex; BMS Oncology, Princeton, NJ), and methotrexate sodium (Immunex, Seattle, Wash), or VIM, prior to the transplantation preparatory regimen. One patient underwent no repeat induction therapy; one received etoposide (VePesid; BMS Oncology), vincristine sulfate, and doxorubicin hydrochloride (Adriamycin; Pharmacia & Upjohn, Kalamazoo, Mich); and one received dexamethasone acetate (Decadron-LA; Merck & Co, West Point, Pa), cytarabine (Ara-Cytidine; Pharmacia & Upjohn), and cisplatin (Platinol AQ; BMS Oncology), or DHAP.

The treatment regiment prior to PBSC reinfusion was BiCNU sterile carmustine (BCNU; BMS Oncology, 450 mg/m2), etoposide (VePesid; BMS Oncology, 2,400 mg/m2 over 34 hours), and cyclophosphamide (Cytoxan; BMS Oncology, 1,800 mg/m2 per day x 4 days) in all patients. No patient received total-body irradiation.

Autologous peripheral blood hematopoietic stem cells were reinfused in all cases for bone marrow reconstitution, and nine patients also underwent autologous bone marrow repeat infusion. Filgrastim (Neupogen [5 µg/m2]; Amgen, Thousand Oaks, Calif) was administered daily after stem cell repeat infusion until bone marrow engraftment. The median time to engraftment was 11 days.

A decision regarding the delivery of adjuvant irradiation was made after patient consultation with a radiation oncologist (J.A.B. or C.T.C.). Thirteen patients underwent adjuvant radiation therapy (Clinac 2100C; Varian Oncology Services, Palo Alto, Calif); 17 patients did not undergo irradiation because of a history of prior radiation therapy in 11 patients, patient refusal in two patients, and physician preference in four patients.

The doses ranged from 28.8 to 39.0 Gy (median, 33.0 Gy) in 1.5–1.8-Gy fractions. Custom immobilization devices (Alpha Cradle; Smithers Medical Products, North Canton, Ohio) were routinely employed, and computed tomography (CT)-based planning was used, when possible, to shield as much normal tissue as possible. Treatment was delivered with 6- or 15-MV photons, depending on the tumor location, and fields were shaped by using custom Cerrobend blocks (Cerro de Pasco, New York, NY).

Patients were examined by an attending physician (J.A.B. or C.T.C.) weekly during radiation therapy to monitor reactions to the radiation. At this time, a directed history was obtained and a physical examination was performed. A complete blood cell count was performed weekly or biweekly during radiation therapy. Patients underwent follow-up examinations at 1 month after radiation therapy, every 2–3 months for 2 years, and subsequently at 4–6-month intervals. Results of blood cell counts performed approximately 100 days after stem cell repeat infusion were used to compare hematologic toxic reactions in patients who did and in patients who did not undergo irradiation.

The criteria proposed by the Radiation Therapy Oncology Group (RTOG) (15), were used for assessing the toxic reaction (Table 2). One of two authors (J.A.B. or C.U.) reviewed the platelet count data to accomplish the toxic reaction assessment. Survival and follow-up times were measured from the time of stem cell repeat infusion. The diagnosis of disease recurrence was based on clinical and radiologic findings, and histologic documentation was obtained in nine of 10 patients with relapse after stem cell transplant.


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  		TABLE 2. RTOG Acute Radiation Morbidity Grading Criteria
 

   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Adjuvant radiation therapy was delivered 40–88 days (median, 45 days) after stem cell repeat infusion in 13 patients, as planned. Two patients underwent subtotal nodal irradiation, which included whole-lung irradiation in one patient; one, mantle-field irradiation; one, whole-abdomen irradiation; and the remaining nine, supradiaphragmatic involved–field irradiation.

The extent of radiation therapy was dependent on the sites of disease relapse and the response to repeat induction therapy and to conditioning chemotherapy; the planned dose of radiation therapy likewise was based on disease response to pretransplantation and to therapies at the time of transplantation.

Irradiation was generally initiated after the recovery of blood cell counts. At the start of radiation therapy, the median white blood cell count was 4.3 x 109/L (range, 1.9–14.4 x 109/L), the median hematocrit level was 0.341 (range, 0.274–0.421), and the median platelet count was 233 x 109/L (range, 66–394 x 109/L).

Radiation therapy was tolerated well. There were no treatment interruptions, and no patient had treatment terminated early. During the radiation therapy course, the white blood cell count and hematocrit level remained stable or increased. The platelet count declined in seven patients and stabilized or improved in the remaining six patients.

Thrombocytopenia (per RTOG toxic reaction criteria) developed in five patients: one patient with grade 1 and two patients each with grades 2 and 3. All patients were asymptomatic, without clinical evidence of bleeding abnormalities. No platelet transfusions were required.

Comparison of blood cell counts performed approximately 100 days after stem cell repeat infusion (Table 3) showed that five patients who underwent irradiation continued to have thrombocytopenia (three with grade 1 and two with grade 2), compared with three patients (two with grade 1 and one with grade 3) who did not undergo posttransplantation irradiation. Three patients with thrombocytopenia at day 100 who underwent irradiation were known to have progression of disease and died of progression of disease within 6 months of radiation therapy completion. The remaining two patients, both with a history of prior radiation therapy, recovered their platelet counts (>100 x 109/L) within 3 months of completion of radiation therapy and were disease free at the end of this study, with normal platelet counts 2–31/2 years after transplantation.


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  		TABLE 3. Characteristics of Patients with Hematologic Toxic Reactions
 
One patient with thrombocytopenia in the group who had not undergone irradiation died of complications 4 months after transplantation, without evidence of disease recurrence; the other two patients recovered from thrombocytopenia, without complications. Median white blood cell counts and hematocrit levels at day 100 were similar in patients who underwent irradiation and in those who did not.

Both patients who underwent posttransplantation radiation therapy with a history of prior external-beam irradiation developed transient grade 1 thrombocytopenia. In addition, both patients who had histologic results of lymphocyte depletion developed thrombocytopenia, but they also had disease progression shortly after radiation therapy. Due to the limited number of patients in this study, it was not possible to correlate hematologic toxic reactions with patient, tumor, or treatment variables.

No severe nonhematologic toxic reactions were observed. Mild fatigue was common after transplantation and during radiation therapy. Symptomatic pulmonary injury, including radiation pneumonitis, did not occur in any patient who underwent posttransplantation radiation therapy. There were no fatalities related to adjuvant irradiation.

Median follow-up was 42 months (range, 12–72 months) in living patients. Relapse occurred in three patients who underwent irradiation and in seven patients who did not. Actuarial 3-year overall survival and relapse-free survival rates were 75% and 60%, respectively, for all patients.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Although radiation therapy is to our knowledge the single most effective agent in the treatment of Hodgkin disease, the role of consolidation irradiation adjuvant to bone marrow and PBSC transplantation remains unclear. While retrospective analyses (10–14) have shown a reduction in the risk of local tumor relapse with the addition of local radiation therapy, to our knowledge, results of randomized studies have not been reported, and the routine use of adjuvant radiation therapy remains controversial.

The majority of relapses are at sites of previous disease (11), and an argument can be made for the use of adjuvant radiation therapy if the accompanying toxic reaction is acceptable. The effect on overall toxic reaction has been difficult to discern, as findings of early studies (4,14,16–18) of both allogenic and autologous bone marrow transplantations showed high treatment-related mortality and morbidity, but local peritransplantation radiation therapy has been implicated as a contributing factor to mortality in up to 7%–14% (10,12,14) of patients. With advances in supportive care and the shift to autologous PBSC support, overall mortality and morbidity have decreased (6,7,19,20), and this provides a more optimal scenario to assess the effects of adjuvant irradiation.

In the present series, the toxicity of consolidation radiation therapy did not contribute to any deaths.

The main purpose of this study was to assess the hematologic feasibility of routine, adjuvant external-beam irradiation. Few studies have focused on this topic, and to our knowledge this is the first study in which the hematologic toxic reaction to high-dose chemotherapy with PBSC support in patients with Hodgkin disease who do and in those who do not undergo irradiation has been evaluated. Authors of other reviews (13,14) have noted more difficulty in the delivery of adjuvant irradiation after bone marrow transplantation.

Price and colleagues (13) reported on 17 patients who underwent posttransplantation radiation therapy for Hodgkin disease. Severe hematologic morbidity was seen in four patients and was correlated with the pre–radiation therapy white blood cell and platelet counts and initial disease stage. However, patients underwent irradiation at the time of relapse (1–23 months) after autologous transplantation, and disease progression may have contributed to hematologic toxic reactions in this patient population.

Abrams et al (14), reporting on posttransplantation radiation therapy in 21 patients with lymphoma, also correlated severe hematologic toxic reactions with the pre–radiation therapy platelet count. However, the patient population was not uniform, as autologous and allogenic bone marrow reconstitutions were used, patients with Hodgkin and patients with non-Hodgkin lymphoma were included, and total-body irradiation was sometimes part of the preparatory regimen.

Despite the use of necessarily large radiation therapy fields in certain patients, who included those who underwent subtotal nodal irradiation and whole-lung irradiation, the hematologic tolerance of the newly reconstituted bone marrow was good.

This contrasts with the experience of Price and colleagues (13), in which extended-field irradiation correlated with grade 3 or grade 4 hematologic toxic reactions, although this difference may be related partly to patient selection.

As was expected, in our study, patients known to have active disease were likely to have hematologic toxic reactions after radiation therapy, and three of five patients who developed hematologic toxic reactions after undergoing adjuvant irradiation had progression of disease. In addition, both patients who underwent prior irradiation developed mild, transient thrombocytopenia. The low overall toxic reaction rate may be explained partially by the routine use of PBSCs as the source for hematologic reconstitution. Comparisons of autologous bone marrow and PBSC transplantations demonstrate faster hematologic recovery, shorter hospital stays, and fewer toxic reactions that lead to death in patients who receive PBSC support (6,7,18,19).

In addition, CT-based conformal radiation therapy was used when possible to limit the amount of normal tissue irradiated, and radiation therapy fractions were generally limited to 1.5 Gy.

To our knowledge, the optimal timing for radiation therapy in conjunction with bone marrow or stem cell transplantation is not known. Radiation therapy prior to conditioning therapy has been advocated in an effort to minimize the tumor burden at the time of transplantation (18). This approach also helps to avoid irradiation of the newly reconstituted bone marrow, which, in addition to sparing acute morbidity, might be less likely to contribute to subsequent myelodysplasia or to secondary leukemia than radiation therapy after transplantation.

While these concerns may have some theoretic validity, to our knowledge there is no practical evidence in the literature that radiation therapy prior to transplantation is associated with improved results or fewer side effects than irradiation after transplantation. In fact, recent pretransplantation mediastinal irradiation has been associated with severe pulmonary toxic reaction and mortality (21,22), although other treatment-related factors including chemotherapy dose need to be considered (23).

Interpretation of the effect of radiation therapy timing is further complicated, as studies may include patients who undergo irradiation both before and after transplantation, and often those selected for posttransplantation radiation therapy already have evidence of disease relapse (11,12).

Posttransplantation radiation therapy has been adopted at our institution, as it does not delay the timing of the conditioning regimen and the patient does not face the combined acute toxicity of local radiation therapy and high-dose conditioning chemotherapy. In addition, the radiation therapy field may be reduced in size for tumors that respond to the transplantation regimen. Local tumor control in the present series was comparable to that in studies (12,18,22) in which researchers used pretransplantion irradiation; hence, there was no evidence of a deleterious effect of delay of radiation therapy.

The purpose of this review was not to compare treatment outcome but to assess the hematologic tolerance of adjuvant irradiation after high-dose chemotherapy with PBSC support in patients treated for Hodgkin disease. Because of differences in patient selection and prior therapy and due to the retrospective nature of this study, no conclusions can be drawn with regard to relapse or survival. However, the 3-year actuarial overall and relapse-free survival rates, 75% and 60%, respectively, are in line with other results documented in the literature (1–7).

External-beam radiation therapy was well tolerated after high-dose chemotherapy with PBSC support in patients with Hodgkin disease. Transient hematologic toxic reactions were common but were not related to clinical complications. While we were able to deliver local radiation therapy safely in this patient population, larger comparative trials are needed to determine its utility and effect on acute and long-term transplantation-related toxicity.


   Footnotes
 
Abbreviations: PBSC = peripheral blood stem cell RTOG = Radiation Therapy Oncology Group

Author contributions: Guarantor of integrity of entire study, J.A.B.; study concepts and design, J.A.B., K.W.Z.; definition of intellectual content, J.A.B., K.W.Z., C.U.; literature research, J.A.B., C.U.; clinical studies, J.A.B.; data acquisition and analysis, J.A.B., C.U.; manuscript preparation, J.A.B., S.R., C.U.; manuscript editing, J.A.B., S.R.; manuscript review, C.T.C., J.A.B., K.W.Z.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Reece DE, Phillips GL. Intensive therapy and autologous stem cell transplantation for Hodgkin's disease in first relapse after combination chemotherapy. Leuk Lymphoma 1996; 21:245-253.[Medline]
  2. Horning SJ, Chao NJ, Negrin RS, et al. High-dose therapy and autologous hematopoietic progenitor cell transplantation for recurrent or refractory Hodgkin's disease: analysis of the Stanford University results and prognostic indices. Blood 1997; 89:801-813.[Abstract/Free Full Text]
  3. Armitage JO, Bierman PJ, Vose JM, et al. Autologous bone marrow transplantation for patients with relapsed Hodgkin's disease. Am J Med 1991; 91:605-611.[Medline]
  4. Nademanee A, O'Donnell MR, Snyder DS, et al. High-dose chemotherapy with or without total body irradiation followed by autologous bone marrow and/or peripheral blood stem cell transplantation for patients with relapsed and refractory Hodgkin's disease: results in 85 patients with analysis of prognostic factors. Blood 1995; 85:1381-1390.[Abstract/Free Full Text]
  5. Sweetenham JW, Taghipour G, Milligan D, et al. High-dose therapy and autologous stem cell rescue for patients with Hodgkin's disease in first relapse after chemotherapy: results from the EBMT—Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant 1997; 20:745-752.[Medline]
  6. Caballero MD, Rubio V, Rifon J, et al. BEAM chemotherapy followed by autologous stem cell support in lymphoma patients: analysis of efficacy, toxicity and prognostic factors. Bone Marrow Transplant 1997; 20:451-458.[Medline]
  7. Geisler CH, Hansen MM, Andersen NS, et al. BEAM + autologous stem cell transplantation in malignant lymphoma: 100 consecutive transplants in a single centre—efficacy, toxicity and engraftment in relation to stem-cell source and previous treatment. Eur J Haemat 1998; 61:173-182.
  8. Bierman PJ, Anderson JR, Freeman MB, et al. High-dose chemotherapy followed by autologous hematopoietic rescue for Hodgkin's disease patients following first relapse after chemotherapy. Ann Oncol 1996; 7:151-156.[Abstract/Free Full Text]
  9. Moreau P, Fleury J, Brice P, et al. Early intensive therapy with autologous stem cell transplantation in advance Hodgkin's disease: retrospective analysis of 158 cases from the French registry. Bone Marrow Transplant 1998; 21:787-793.[Medline]
  10. Pezner RD, Nademanee A, Niland JC, Vora N, Forman SJ. Involved field radiation therapy for Hodgkin's disease autologous bone marrow transplantation regimens. Radiother Oncol 1995; 34:23-29.[Medline]
  11. Mundt AJ, Sibley G, Williams S, Hallahan D, Nautiyal J, Weichselbaum RR. Patterns of failure following high-dose chemotherapy and autologous bone marrow transplantation with involved field radiotherapy for relapsed/refractory Hodgkin's disease. Int J Radiat Oncol Biol Phys 1995; 33:261-270.[Medline]
  12. Poen JC, Hoppe RT, Horning SJ. High-dose therapy and autologous bone marrow transplantation for relapsed/refractory Hodgkin's disease: the impact of involved field radiotherapy on patterns of failure and survival. Int J Radiat Oncol Biol Phys 1996; 36:3-12.[Medline]
  13. Price A, Cunningham D, Horwich A, Brada M. Haematological toxicity of radiotherapy following high-dose chemotherapy and autologous bone marrow transplantation in patients with recurrent Hodgkin's disease. Eur J Cancer 1994; 30:903-907.
  14. Abrams RA, Liu PJ, Ambinder RF, et al. Hodgkin and non-Hodgkin lymphoma: local-regional radiation therapy after bone marrow transplantation. Radiology 1997; 203:865-870.[Abstract/Free Full Text]
  15. Radiation Therapy Oncology Group (RTOG). RTOG Procedure Manual Philadelphia, Pa: RTOG Headquarters, 1998.
  16. Anderson JE, Litzow MR, Appelbaum FR, et al. Allogeneic, syngeneic, and autologous marrow transplantation for Hodgkin's disease: the 21-year Seattle experience. Clin Oncol 1993; 11:2342-2350.
  17. Bierman PJ. Update of results of autologous bone marrow transplantation in lymphoma. Med Oncol 1994; 11:35-41.[Medline]
  18. Yahalom J, Gulati SC, Toia M, et al. Accelerated hyperfractionated total-lymphoid irradiation, high-dose chemotherapy, and autologous bone marrow transplantation for refractory and relapsing patients with Hodgkin's disease. J Clin Oncol 1993; 11:1062-1070.[Abstract/Free Full Text]
  19. Majolino I, Pearce R, Taghipour G, Goldstone AH. Peripheral-blood stem-cell transplantation versus autologous bone marrow transplantation in Hodgkin's and non-Hodgkin's lymphomas: a new matched-pair analysis of the European Group for Blood and Marrow Transplantation Registry Data—Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. J Clin Oncol 1997; 15:509-517.[Abstract/Free Full Text]
  20. Deliliers GL, Tagliaferri E, Annaloro C, et al. G-CSF after autologous hemopoietic stem cell transplantation in malignant lymphoma. Prostaglandins Other Lipid Mediat 1998; 56:33-42.[Medline]
  21. Jones RJ, Piantadosi S, Mann RB, et al. High-dose cytotoxic therapy and bone marrow transplantation for relapsed Hodgkin's disease. J Clin Oncol 1990; 8:527-537.[Abstract]
  22. Phillips GL, Wolff SN, Herzig RH, et al. Treatment of progressive Hodgkin's disease with intensive chemoradiotherapy and autologous bone marrow transplantation. Blood 1989; 73:2086-2092.[Abstract/Free Full Text]
  23. Weaver CH, Appelbaum FR, Petersen FB, et al. High-dose cyclophosphamide, carmustine, and etoposide followed by autologous bone marrow transplantation in patients with lymphoid malignancies who have received dose-limiting radiation therapy. Clin Oncol 1993; 11:1329-1335.




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