Originally published as JCO Early Release 10.1200/JCO.2005.05.4684 on August 8 2006

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Phase II Trial of CHOP Plus Rituximab in Patients With HIV-Associated Non-Hodgkin's Lymphoma

François Boué, Jean Gabarre, Christian Gisselbrecht, Jacques Reynes, Antoine Cheret, Fabrice Bonnet, Eric Billaud, Martine Raphael, Remi Lancar, Dominique Costagliola

From the Agence Nationale Recherche sur le Sida et les Hépatites Paris; Hôpital Antoine Béclère, Clamart; Université Paris Sud; Hôpital Salpétrière, Paris; Hôpital Saint Louis, Paris; Hòpital Gui de Chauliac, Montpellier; Hôpital Gustave Dron, Tourcoing; Hôpital Saint André, Bordeaux; Hôtel Dieu, Nantes; Hôpital Bicêtre, Le Kremlin Bicêtre; INSERM U720 and Université Pierre et Marie Curie, Paris, France

Address reprint requests to François Boué, Hopital Antoine Beclere, 157 rue de la porte de Trivaux 92140 Clamart, Clamart, France; e-mail: francois.boue{at}abc.aphp.fr

	ABSTRACT

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Purpose To evaluate the safety and efficacy of rituximab adjunction to the cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) regimen in patients with newly diagnosed AIDS-related non-Hodgkin's lymphoma.

Patients and Methods HIV-seropositive patients with high-grade lymphoma of B-cell origin were eligible if they had no more than one of the following characteristics: CD4 cell count less than 100/µL, prior AIDS, or performance status less than 2. This multicenter phase II trial evaluated the response rate and disease-free survival after six courses of rituximab plus CHOP.

Results Sixty-one patients were enrolled. All the patients were assessable for safety and 52 were assessable for the tumor response after treatment completion. Characteristics of patients were median age, 41 years; median CD4 cells, 172/µL; histology, diffuse large B-cell lymphoma (n = 42), immunoblastic (n = 2), Burkitt lymphoma (n = 16), and plasmablastic (n = 1); 42 patients with stage III to IV; International Prognostic Index 0 to 1 (n=31), and 2 to 3 (n = 27). Grade 3 or 4 toxicity consisted of febrile neutropenia in nine patients, anemia in 16 patients, and thrombocytopenia in five patients. Complete remission (CR) or unconfirmed CR was achieved in 40 of the 52 assessable patients, partial remission was achieved in five patients, and seven patients experienced progression. Forty-three patients were alive after a median follow-up of 33 months. The estimated 2-year overall survival rate was 75% (95% CI, 64% to 86%). Eighteen patients died: 16 as a result of lymphoma, one as a result of infection, and one as a result of encephalitis.

Conclusion Rituximab adjunction to CHOP produced a CR rate of 77% and a 2-year survival rate of 75% in patients with AIDS-related non-Hodgkin's lymphoma, without increasing the risk of life-threatening infections.

	INTRODUCTION

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HIV infection is associated with a high risk of lymphoma. The advent of highly active antiretroviral therapy (HAART) was accompanied by a significant improvement in the survival of HIV-infected patients. AIDS-related lymphoma (ARL) also became less frequent,¹ but remains a major cause of death in this setting² and still carries a poor prognosis.³ Trials conducted before the HAART era showed that this poor prognosis was due to both lymphoma-specific factors (histology, extranodal disease, and bone marrow involvement) and HIV-specific factors (prior opportunistic infections, poor performance status, and the CD4 lymphocyte count, which is the most important prognostic factor).^3-7 In these trials, the median survival time was 8 months, and only 10% of patients survived for at least 2 years after lymphoma onset.⁸ About half the deaths were due to lymphoma and the other half to HIV disease. Recent studies indicate that the prognosis of ARL has improved in the HAART era,¹ possibly owing to higher CD4 counts at lymphoma onset, effective antiretroviral therapy, and certain features of the lymphomas.^7,9 On the basis of preliminary results of anti-CD20 monoclonal antibody therapy^10-12 and the fact that most cases of HIV-associated non-Hodgkin's lymphoma are CD20⁺, we initiated a multicenter phase II trial in 1998 in order to evaluate the safety and efficacy of rituximab adjunction to the standard chemotherapy regimen (cyclophosphamide, doxorubicin, vincristine, and prednisone [CHOP]).

	PATIENTS AND METHODS

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Patients
Eligible patients were HIV-seropositive with high-grade (Ann Arbor stage I to IV), biopsy-confirmed, untreated non-Hodgkin's lymphoma of B-cell origin and of the following histologic types: Burkitt's lymphoma (BL) and diffuse large B-cell lymphoma (DLBCL); BL including classical BL (c-BL) and atypical Burkitt/Burkitt-like lymphoma (a-BL); and high-grade, large-cell immunoblastic lymphoma. For all patients, the expression of CD20 was positive by immunophenotyping on tumor cells. Patients with Burkitt/Burkitt-like lymphoma were excluded if they had CSF involvement and/or blood involvement or if they had CSF and bone marrow involvement. Patients between 18 and 75 years of age were eligible if they had good or intermediate prognoses, as defined in our previous study⁵ (ie, no more than one of the following prognostic factors: CD4 cell count less than 100/µL, prior history of opportunistic infections, and Karnofsky performance score less than 60 or Eastern Cooperative Oncology Group score more than 2. Patients with active viral hepatitis were ineligible. Women of reproductive age had to agree to use effective contraception. All of the patients gave their written informed consent to participate in the study. The study protocol was approved on September 2, 1998, by the Institutional Review Board of Bicêtre Hospital (Le Kremlin Bicêtre, France).

Staging
All of the patients had a detailed history taken and underwent a physical and neurologic examination. The following parameters were recorded at baseline: height, weight, WHO performance status, dimensions of all palpable lesions, CBC, blood chemistry, chest radiography, computed tomography of the thorax and abdomen, cerebral computed tomography, bone marrow aspiration and biopsy, ECG, CD4 cell count, and HIV viral load. The Ann Arbor lymphoma staging system was used. The International Prognostic Index (IPI)¹³ was also measured. Antiretroviral treatment was recorded. The biopsies were reviewed centrally by a hematopathologist (M.R.).

Treatment
All of the patients received a combination of cyclophosphamide 750 mg/m² on day 1, doxorubicin 50 mg/m² on day 1, vincristine 1.4 mg/m² (maximum 2 mg) on day 1, and prednisone 40 mg/m² per day for 5 days. The day before each CHOP course, all the patients received rituximab 375 mg/m². Rituximab infusion was interrupted if one of the following events occurred: fever, chills, edema, congestion of the head and neck mucosa, arterial hypotension, or any other serious adverse event, and was resumed when the event had resolved. After the first cycle, and as soon as rituximab was well tolerated, rituximab could be infused on the same day as CHOP. Patients were treated every 3 weeks for six cycles. No radiation therapy was scheduled or recommended at the end of treatment. Granulocyte colony-stimulating factor could be administered if grade 4 neutropenia occurred, or preventively from days 6 to 12. Antiretroviral treatment was recommended from the beginning of treatment, but administration of zidovudine and ritonavir was avoided. Pneumocystis carinii pneumonia prophylaxis with trimethoprim-sulfamethoxazole was recommended. The decision of whether to administer CNS prophylaxis was left to each participating center.

Response Assessment and Adverse Events
Tumor responses were assessed after the six cycles of chemotherapy, or at the end of prematurely interrupted treatment, and were classified as complete response (CR), unconfirmed complete (UCR), partial response, stable disease, or progressive disease, according to the International Workshop criteria.¹⁴ An independent review board reviewed all the charts and computed tomography (CT) scans to decide which patients were assessable. CR was defined as the disappearance of all lesions and of radiologic or biologic abnormalities observed at diagnosis, and the absence of new lesions. Results had to be confirmed at the second assessment 4 weeks later. A UCR was defined as a CR with the persistence of some radiologic abnormalities, which had to have regressed in size by at least 75%. Partial response was defined as the regression of any measurable lesions by more than 50%, the disappearance of nonmeasurable lesions, and the absence of new lesions. Stable disease was defined as regression of any measurable lesion by 50% or less, or no change in nonmeasurable lesions, without growth of existing lesions or the appearance of new lesions. Progressive disease was defined as the appearance of a new lesion, any growth of the initial lesion by more than 25%, or growth of any measurable lesion that had regressed during treatment by more than 50% from its smallest dimensions.

All adverse events reported by the patients or observed by the investigators were collected from the case report forms. Each event was graded according to the National Cancer Institute Common Toxicity Criteria.

Statistical Methods
The primary end point was the response rate (CRs and UCRs). When calculating the required sample size, we assumed a response rate of 70%. Enrollment of 47 assessable subjects would ensure that the response rate was significantly greater than 50%, with a two-sided significance level of 5% and 80% power. To account for nonassessable patients, it was decided to include at least 60 patients. The exact 95% CI of the response rate was estimated.

Overall survival (OS) was calculated for the 61 patients from the date chemotherapy was started to death as a result of any cause or to the last time the patient was seen. Progression-free survival (PFS) was calculated for the 52 assessable patients from the date chemotherapy was started until progression or relapse (for patients with CR or UCR), or until the last date on which the patient was known to be disease free and alive. OS and PFS were evaluated with the Kaplan-Meier method, and differences between subgroups were tested with the log-rank test. Multivariate analysis of survival was performed with the Cox proportional hazards model, including all variables that were associated significantly with outcome in univariate analysis. Hazards ratios and 95% CIs are reported.

	RESULTS

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Patient Characteristics
Sixty-one patients were enrolled in 20 centers. The main baseline characteristics of the patients are listed in Table 1. All the patients received at least one dose of treatment and were thus assessable for toxicity. The independent review board considered that 52 patients were assessable for the primary end point (tumor response after the six cycles of chemotherapy).

The median baseline CD4 count was 172/µL and the median HIV viral load was 7,895 copies/mL. Five patients had CD4 cell counts below 50/µL, and 21% of patients had previously had AIDS-defining events.

Patients were classified as untreated if HAART was started less than 3 months before the onset of lymphoma, and were classified as previously treated if they were treated for more than 3 months before onset. On this basis, 32 patients were untreated, mostly because HIV infection was diagnosed at the same time as the lymphoma.

For the centrally review of biopsies, lymphomas were classified according to the recommendations of the WHO classification into the following categories: DLBCL, 42 patients; immunoblastic lymphoma, two patients; BL, 16 patients subdivided into c-BL (six patients) and a-BL (10 patients). One patient had a plasmablastic lymphoma. Extranodal involvement was diagnosed in 78% of patients, and one third of patients had GI or hepatic involvement. The IPI score was more than 1 in 29 patients (48%).

Treatment
Forty-two (69%) of the 61 patients completed the six scheduled courses of chemotherapy, and 35 (57%) received at least 90% of the planned doses of doxorubicin and cyclophosphamide. A dose reduction or treatment delay was required for 70% of patients. Granulocyte colony-stimulating factor support was prescribed to 44% of patients during the first cycle and to 77% of patients overall. A CNS prophylaxis was performed for 22 patients. Forty-two patients received antiretroviral treatment (always including protease inhibitors) during CHOP therapy.

Clinical Outcome
At the end of treatment, 52 patients were assessable for the tumor response. Thirty-five patients had a CR and five had a UCR (CR rate, 77%; 95% CI, 63% to 87%; Table 2). Five patients had a partial response and seven experienced disease progression during treatment. After a median follow-up of 33 months, 43 patients were alive, and 34 of the 52 assessable patients were alive and disease free. The estimated 2-year OS rate was 75% (95% CI, 64% to 86%; Fig 1) and the estimated 2-year PFS rate was 69% (95% CI, 56% to 82%; Fig 2). Among the 18 patients who died, five died before the end of treatment. Sixteen deaths were related to lymphoma progression.

View larger version (8K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Overall survival.

View larger version (9K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Progression-free survival.

	DISCUSSION

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R-CHOP proved to be simple to schedule and feasible, and 42 patients (69%) completed the six courses of chemotherapy. The response rate (77%) and the estimated 2-year OS rate (75%; 95% CI, 64% to 86%) are among the most encouraging reported in this setting. If nonassessable patients are considered as not having CR, the estimated 2-year OS rate would be at 66% (95% CI, 52% to 77%). This simple-to-schedule 1-day regimen was applied in 20 different centers in France, and the results are likely to be reproducible elsewhere.

An observational study showed that the survival of patients with ARL has improved since the advent of HAART.¹ Although this study was not designed for comparison, the tumor response rate and OS observed are in the upper range of those reported in other recent studies of combination therapy with HAART and conventional CHOP-like regimens.^9,15 In contrast, they are similar to those recently obtained with infusional therapy (infusional cyclophosphamide, doxorubicin, and etoposide [CDE]) and rituximab.¹⁶ The response rate (77%) and the overall 2-year survival rate (75%) in our study are also consistent (76% and 70%, respectively) with those obtained in the R-CHOP arm of the Groupe d'Etude des Lymphomes de l'Adulte trial involving patients older than age 60 years.¹⁷

When this trial was designed in 1998, the safety of R-CHOP was uncertain in patients with advanced HIV disease, and we therefore decided to enroll only patients with no more than one of the following prognostic factors: CD4 cell count less than 100/µL, prior opportunistic infections, and poor general status (Karnofsky performance score < 60). Nevertheless, the baseline characteristics of our patients are similar to those of patients enrolled onto other trials and observational studies.^1,9,15 The characteristics of the lymphomas were similar to what was expected in the HAART era: most were DLBCL and only two were immunoblastic lymphomas.

Recent data cast doubts on the safety of R-CHOP combination therapy in HIV-infected patients. Kaplan et al¹⁸ reported that, in the AIDS-Malignancies Consortium trial (AMC) 010, 15 of the 16 infectious deaths occurred in the rituximab arm. However, in our trial only one death was possibly related to septic shock, and one other death was related to HIV encephalopathy. The other 16 deaths were all due to lymphoma progression. Episodes of febrile neutropenia occurred in 15 patients (25%), and severe sepsis was documented in two patients. In the AMC 10 trial, treatment-related infectious deaths were significantly more frequent in patients with baseline CD4 counts below 50/µL. In contrast, our inclusion criteria precluded advanced HIV infection, and only four patients had CD4 cell counts below 50/µL. Two of these four patients are in CR (despite cytomegalovirus disease in one patient), whereas the other two experienced disease progression (one with HIV encephalitis). The difference between the results of these two trials may therefore be due to the larger proportion of patients with CD4 cell counts below 50/µL in the AMC trial.

It is difficult to determine the respective roles of rituximab adjunction and better overall management of HIV-infected patients in these encouraging results. The AMC 10 trial showed no benefit of rituximab adjunction, and the CR rate (57.6%) was lower than in our study and the R-CDE trial (70%). Nevertheless, there was a trend toward a better response rate (57.6% v 47%) in the rituximab arm of the AMC 10 trial. It should be emphasized that, in contrast with other trials, our trial selected a population of patients without more than one risk factor.

When we analyzed prognostic factors for their impact on the tumor response rate and patient survival rates, it appeared that lymphoma-associated factors (ie, the IPI score) were the main determinants. The CD4 cell count at treatment initiation was also associated with the PFS rate. Thus, patients with an IPI score of 0 or 1 and a CD4 cell count greater than 100/µL seem to form a subgroup in which the results of R-CHOP are satisfactory. Conversely, patients with an IPI score greater than 1 may require more aggressive treatment, such as that recommended for patients with non-AIDS–related lymphomas.¹⁸ In our study, there were no survival differences between the main histologic subtypes BL (c-BL or a-BL) versus DLCBL, but the power of our study was not calculated for this comparison. This may be explained by the fact that patients with BL associated with CNS and bone marrow involvement and/or blood involvement were excluded from the trial. Thus, additional trials designed to investigate this issue are required.

In conclusion, this trial shows that R-CHOP is a simple to schedule and effective treatment for patients with HIV-associated B-cell lymphoma, yielding a 77% CR rate and a 75% 2-year OS rate. These results were obtained in 20 different centers, and thus may be applicable elsewhere. We observed few infectious or AIDS-related events, and most deaths were related to lymphoma progression. The best results were obtained in patients with an IPI score of 0 or 1 and a CD4 cell count greater than 100/µL at treatment initiation.

	Appendix

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The following investigators participated in the study: ANRS 085 trial investigators: François Boué, Clamart; Christian Gisselbrecht, Paris, St Louis; Eric Oksenhendler, Paris St Louis, Jean François Delfraissy, Bicetre; Yves Levy, Creteil; Jean Gabarre, Paris, Pitie; Philippe Morlat, Bordeaux; Claude Basin, Caen; Bertrand Coiffier, Lyon; Jean Yves Blay, Lyon; Noël Milpied, Nantes; Antoine Thyss, Nice; Eric Rosenthal, Nice; Jean Marie Lang, Strasbourg; François Dreyfus, Paris, Cochin; Jacques Reynes, Montpellier; Alain Devidas, Corbeil; Isabelle Plantier, Tourcoing; Xavier Lepeu, Avignon; and Frédéric Bauduer, Bayonne.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Author Contributions

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Appendix Authors' Disclosures of... Author Contributions REFERENCES

 

Conception and design: François Boué, Jean Gabarre, Christian Gisselbrecht, Martine Raphael, Dominique Costagliola Provision of study materials or patients: François Boué, Jean Gabarre, Christian Gisselbrecht, Jacques Reynes, Antoine Cheret, Fabrice Bonnet, Eric Billaud, Martine Raphael Collection and assembly of data: François Boué, Martine Raphael, Remi Lancar Data analysis and interpretation: François Boué, Jean Gabarre, Christian Gisselbrecht, Martine Raphael, Remi Lancar, Dominique Costagliola Manuscript writing: François Boué, Jean Gabarre, Christian Gisselbrecht, Martine Raphael, Dominique Costagliola Final approval of manuscript: François Boué, Jean Gabarre, Christian Gisselbrecht, Jacques Reynes, Antoine Cheret, Fabrice Bonnet, Eric Billaud, Martine Raphael, Remi Lancar, Dominique Costagliola

 

	ACKNOWLEDGMENTS

 
We thank the following colleagues for their contributions: S. Matheron, J. Dormont, and C. Riche (members of the Data Safety Monitoring Board); S. Maitre, P. Solal Celigny, and Y. Menu (members of the Response Review Board); Roche for providing rituximab and the French National Agency for Aids and Viral Hepatitis Research (ANRS) 085 trial investigators.

	NOTES

 
published online ahead of print at www.jco.org on August 7, 2006.

Supported by the French National Agency for AIDS and Viral Hepatitis Research (ANRS).

Presented in part at the 44th Annual Meeting of the American Society of Hematology, Philadelphia, PA, December 4-10, 2002, and at the 10th Conference on Retroviruses and Opportunistic Infections, Boston, MA, February 8-14, 2003.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted December 22, 2005; accepted June 29, 2006.

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