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LYMPHOMA FOUNDATION  NEWSLETTER  
                      DECEMBER 2008


THE LYMPHOMA FOUNDATION SUPPORTS  RESEARCH OF THE LYMPHOMAS AND ALLIED DISEASES

ON THE CUTTING EDGE OF NEW APPROACHES TO CANCER CURES

The Lymphoma Foundation has awarded research grants to Marcel van den Brink, M.D., Ph.D. and his group of research scientists at the Memorial Sloan Kettering Cancer Center. (Dr. van den Brink is the Head, Division of Hematologic Oncology and the Immunology of Bone Marrow Transplantation Laboratory). His laboratory team is studying clinically important problems in allogeneic Human Stem Cell Tranplantation (HSCT)including graft-versus-host disease (GVHD), graft-versus-tumor (GVT) activity and post-transplant immune reconstitution. [Allogeneic stem cell transplants refer to stem cells that are taken from one person and given to another]. Allogeneic hematopoietic stem cell transplantation (HSCT) is a curative therapy for many hematopoietic malignancies including leukemias and lymphomas, but is associated with significant post-transplant T cell deficiency. This results in an increased susceptibility to viral and fungal infections and increased risks for graft failure and malignant relapse. In seeking ways to improve T cell immunity Dr. van den Brink and his colleagues have performed a series of preclinical studies focused on T cell recovery in recipients of an allogeneic T cell-depleted (TCD) HSCT and they have developed a strategy for adoptive immunotherapy with ex vivo generated T cell precursors [ex vivo refers to experimentation or measurements done in or on living tissue in an artificial environment outside the organism with the minimum alteration of the natural conditions]. T cell precursors were generated using a so-called “Notch-based” culture system and their administration resulted in an early ‘wave’ of T cell reconstitution from thymic and extrathymic sites, enhancing T cell immunity after allogeneic HSCT. 

The goal of this research is the perfection of these strategies extending them beyond the laboratory and into clinical practice that will enhance T cell recovery after Human Stem Cell Tranplantation (HSCT)... as this will improve the overall outcome for patients receiving this therapy.

MORE BASIC RESEARCH

At the Duke University Medical Center in Durham, NC… Dr. Christopher Counter, PhD is also receiving research grant support from the Lymphoma Foundation to fund a pilot project dealing with the oncogenic Ras protein. This will expand their studies of eNOS in relation to cancer development. Dr. Counter wrote to the Lymphoma Foundation: “Specifically, we propose to compare Ras-mediated lymphomagenesis or leukemogenesis in eNOS +/+ versus eNOS-/-mice. If genetic ablation of eNOS reduces cancer in these mice, we would next address whether the NOS small molecular inhibitor L-NAME inhibits such cancers in mouse genetic models. These studies dovetail nicely with our current work on NOS inhibitors in pancreatic cancer.”

ABOUT RAS and eNOS proteins: 1) Signaling pathways are indispensable for cellular communications that control proper development of multicellular organisms. Cancer cells undergo active proliferation. The central importance of the RAS signal transduction in promoting cell proliferation, neoplastic transformation, and oncogenesis is well established. Oncogenic RAS proteins, which are hyperactived forms of RAS, are among the most common genetic alterations detected in human cancer. 2) The protein eNOS mediates Ras oncogenesis in solid tumors. Small molecular inhibitors against NOS proteins have been tested in phase III clinical trials for septic and cardiac shock, but not cancer. Dr. Counter will be studying the role of the eNOS protein to control Ras-mediated cancers.

Further assessment of novel monoclonal antibodies in B-cell malignancies

John Leonard, M.D. and his colleagues at the Weill Cornell Lymphoma Myeloma Cancer Center in New York City reported to the Lymphoma Foundation their current research and future plans supported in part by Lymphoma Foundation grants:
“We are extensively evaluating epratuzumab, an anti-CD22 monoclonal antibody, and our studies have  demonstrated evidence of clinical activity and manageable toxicity.  We are continuing to evaluate patients treated with single-agent epratuzumab, repeated courses (at relapse) as well as in combination with rituximab.  These results have been published in the Journal of Clinical Oncology, and a follow-up international multi-center study [in Cancer Oct. 2008].  This work has led to a recently initiated trial using rituximab + epratuzumab (combination biologic therapy without chemotherapy) as initial therapy for follicular lymphoma which we are conducting with the Cancer and Leukemia Group B of the National Cancer Institute.  Additionally, we are currently conducting several studies with novel human and humanized CD20 monoclonal antibodies which offer several potential advantages over rituximab.  One of these is the first study of subcutaneous anti-CD20 therapy in lymphoma, and initial results are quite promising.   Finally, we have recently initiated a  new phase I trial in lymphoma and CLL with a novel anti-CD74 antibody.  This has been well tolerated in the initial patient groups that have received it, with dose-escalation and efficacy analysis ongoing.  Our group is the first to test this agent in lymphoma patients, and this project has benefited from Lymphoma Foundation support.”
 

Studies of radioimmunotherapy as part of initial therapy for lymphoma.  We have  reported exciting data on fludarabine + I-131 tositumomab (JCO), and are currently evaluating CVP and CHOP in sequential combination with I-131 tositumomab as upfront treatment.  Initial results have been promising, with significant numbers of patients remaining in continuous multi-year remissions.  We have also analyzed outcomes by prognostic group (identified by the follicular lymphoma international prognostic index, or FLIPI), and are looking at this approach to support the idea of a “risk-adapted” treatment approach for follicular lymphoma based on reliable prognostic indicators.  We are participating in an ongoing SWOG/CALGB study to compare CHOP-R versus CHOP-Bexxar as initial treatment in indolent lymphoma.  While this approach may fall into the “intensive” category, early results suggest a potential survival benefit relative to a historical comparison group.”   

Novel chemotherapy regimens. “We have been a leading center in the ongoing pivotal trial of bendamustine, a chemotherapeutic agent that has demonstrated activity in patients with chemo-resistant and rituximab-resistant disease.  This offers a new option for patients with disease resistant to standard agents.  Additionally, we have ongoing studies of oral, low-dose metronomic chemotherapy with PEP-C [Prednisone, Etoposide, Procarbazine, Cyclophosphamide]”   “We will also further expand our efforts to assess novel chemotherapeutic agents and regimens, including the evaluation of new and emerging agents and combinations such as histone deacetylase inhibitors and other compounds in development such as specific cell cycle inhibitors in mantle cell and other lymphoma cell types.”

 


LYMPHOMA FOUNDATION  NEWSLETTER          SEPTEMBER 2008


THE LYMPHOMA FOUNDATION GRANT SUPPORT FOR PATIENT ORIENTED RESEARCH HELPED RESULT IN A MAJOR CHANGE IN HODGKIN’S DISEASE TREATMENT

SPEARHEADED BY THE RESEARCH “Results of a prospective randomized clinical trial of doxorubicin, bleomycin, vinblastine, and dacarbazine (ABVD) followed by radiation therapy (RT) versus ABVD alone for stages I, II, and IIIA nonbulky Hodgkin disease” published in the journal Blood, 1 December 2004, Vol. 104, No. 12, pp. 3483-3489, a major change of treatment by many medical oncologists occurred. Chemotherapy alone is now used for the initial treatment of most patients with early stage non-bulky Hodgkin lymphoma… avoiding the use of radiation that has a high incidence of late serious side-effects.  And Dr. David Straus the leader of this Memorial Sloan Kettering research project wrote to the Lymphoma Foundation: “I am very grateful for your [the Lymphoma Foundation] support of this study.”

ANOTHER HODGKIN’S STUDY UPDATE: Dr. Straus reported that as of August 1, 2008 “We have also made progress in our long-term Hodgkin’s survivor study.  Jennifer Ford, a clinical psychologist in the Department of Psychology and Behavioral Sciences, Kevin Oeffinger, a cancer survivor expert in the Department of Pediatrics, and Matt Matasar, one of our medical oncology fellows with an epidemiology back ground, are helping me with this project.  Matt will be joining the staff of the Lymphoma Service. Our protocol, “A Global Assessment of Medical Morbidities and Quality of Life Among Survivors of Hodgkin Lymphoma” (IRB #05-041), is nearing completion of enrollment.” And once again, Dr. Straus noted: “The support of the Lymphoma Foundation has been invaluable in moving forward these efforts to improve the outcome for patients with Hodgkin lymphoma, and I am deeply grateful for your … support.”

UPDATE REGARDING A VACCINE AGAINST LYMPHOMA The CD20 DNA vaccine developed by the Sloan Kettering research team headed by Dr. Alan Houghton and assisted by Dr. M. Lia Palomba and many other members of the Houghton laboratory staff… after over ten years of support by annual Lymphoma Foundation grants... is finally leaving the laboratory phase and is entering a clinical patient oriented phase.  This clinical phase is proving to be more difficult than initially anticipated as the need to protect the patients from any possible untoward effect of the vaccine has led to extremely stringent and narrow criteria for entry into the clinical trial and follow-up care. In this regard… Dr. Palomba informed the Lymphoma Foundation in August 2008 that “…The FDA has requested that the first enrolled patient be followed until completion of all vaccinations and his/her circulating B cells and quantitative serum immunoglobulins be serially monitored before enrolling patient number 2. This will delay accrual of the second patient of about 3-4 months.” Patient accrual for safety reasons, therefore, will be very slow and the ultimate test of the value of the vaccine will not be known for many months to come.

MORE RESEARCH NEWS

Suresh C. Jhanwar, PhD is the director of the Cytogenetics Laboratory at the Memorial Sloan Ketteing Cancer Center and with support [in part] from Lymphoma Foundation research grants Dr. Jhanwar and his research associates are achieving important advances in understanding Neurofibromatosis (NF-1):

“… we have fully characterized MPNST [Malignant Peripheral Nerve Sheath Tumor] cell lines derived from a patient with metastatic and recurrent disease with NF1 disorder, and also identified a gene associated with metastatic potential which is amenable to various therapeutic and chemo preventative approaches. These cell lines with extensive characterization of genetic abnormalities, therefore, are likely to provide important reagents for various biochemical, molecular, and pharmacological studies related to MPNST.”  Molecular characterization of Permanent Cell Lines from Primary, Metastatic and Recurrent Malignant Peripheral Nerve Sheath Tumors (MPNST) with Underlying Neurofibromatosis-1 by Fang Yuqiang, Abul Elahi, Ryan Denley, Pulivarthi H. Rao, Murray F. Brennan, and Suresh C. Jhanwar 

And there is further Lymphoma Foundation grant support for ongoing research of Neurofibromatosis by Dr. Jhanwar and his associates: The expression profiling and array-based CGH data is currently being analyzed to identify specific genes altered in metastatic and recurrent cell lines. We have identified several recognized genes namely ITGA4, PDGFRB, PDGFA, CDK1C, and CDKN2D which are differentially regulated in these cell lines. The studies are in progress to validate this data both by RT-PCR and Western blotting. Future plans: Study of (1) Methylation inhibitor, 5-AZA CdR and Lycopene mediated re-expression of Nm23-H1 in metastatic cell line and its impact on motility and invasion, characteristic features of metastatic tumor and (2) Investigation of NF-1 interaction with the Ras and PI3K,  pathways involved in deregulation of cell growth and tumorigenesis and  modulation of the metastasis, following chemotherapeutic drugs as well as chemo-preventive agents. Such studies are expected to provide molecular mechanism of the metastasis, a major cause of mortality in these tumors, and also expected to provide information relating to targets of chemo-preventive strategies  in patients with underlying NF-1.

OLDER NEWSLETTERS

LYMPHOMA FOUNDATION NEWSLETTER DECEMBER 2005
THE DILEMMA POSED IN CHOOSING TREATMENT OF ‘LOW GRADE’ FOLLICULAR LYMPHOMAS

SUMMARIES OF RESEARCH IN PROGRESS

 LYMPHOMA FOUNDATION NEWSLETTER  SEPTEMBER 2005
SEEKING SOLUTIONS TO SERIOUS  LATE OCCURRING COMPLICATIONS OF RADIATION THERAPY

THE IDEAL CHOLESTEROL: LOWER IS BETTER: ‘STATIN’ ANTI-CHOLESTEROL MEDICATION

THE ROLE OF MAMMOGRAPHY TO ACHIEVE AN EARLY DIAGNOSIS OF BREAST CANCER

THE LYMPHOMA FOUNDATION CONTINUES TO DISTRIBUTE ITS GRANT SUPPORT FOR A BROAD SPECTRUM OF BASIC AND CLINICAL RESEARCH OF THE LYMPHOMAS AND ALLIED DISEASES
 

 


LYMPHOMA FOUNDATION NEWSLETTERS


SEEKING SOLUTIONS TO SERIOUS  LATE OCCURRING COMPLICATIONS OF RADIATION THERAPY

Use of the radiation therapy to a 'mantle field' was responsible for effectively limiting the chances of early relapses and helped introduce long survival in many patients with Hodgkin's disease. Now it is understood that this treatment has its own unique limitations.


THE PROBLEM: In Hodgkin’s patients treated with radiation therapy to the chest and neck areas a shortened life expectancy is caused by an increased late occurring incidence of coronary heart disease and stroke.



THE POSSIBLE SOLUTIONS: Consider stopping the routine use of Radiation Therapy for patients with Hodgkin’s disease and treat primarily with chemotherapy [**Reference a research study supported in part with Lymphoma Foundation grants by Dr. D. J. Straus, et al at Memorial Sloan Kettering Cancer Center published in Blood, 1 December 2004, Vol. 104, No. 12, pp. 3483-3489 with a supporting commentary by Dr. D. L. Longo of the National Institute of Aging p. 3418:

 ”ABVD chemotherapy alone is as effective as ABVD plus radiation therapy in early-stage Hodgkin disease; thus, the majority of patients are curable without being exposed to the life-long, life-threatening risks of therapeutic radiation.”

¨ Because the use of Radiation therapy may not be stopped but only modified it will continue to be a significant risk factor for the development of coronary heart disease. Therefore cardiologists and oncologists should unite to consider and initiate a study of the value of adding long term use of a statin to the radiation treatment.

¨ Advise the American College of Cardiology (ACC) and the American Heart Association (AHA)  that radiation therapy to the chest and neck in lymphoma patients should be added as a serious risk factor for the development of acute coronary syndromes and stroke and the already treated surviving patients post-radiation should consider starting statin medication and be sure to lower the LDL cholesterol levels to the lowest levels now expected to achieve the best results.

    In this regard an Editorial appeared in the Journal of the American Medical Association entitled
 

The IDEAL Cholesterol

Lower Is Better

by Christopher P. Cannon, MD

JAMA. November 16, 2005;Volume 294:page 2492

“… patients should know their cholesterol numbers, for both LDL-C and HDL-C, to enable them to see how much lowering is needed to reach targets of an LDL-C level of less than 100 mg/dL for patients with risk factors or less than 70 mg/dL for patients with heart disease  … any drug treatment should be taken together with an appropriate diet and exercise program to lower cholesterol and overall vascular risk. … The amount of LDL-C lowering with diet is only in the range of 7% to 12%. Clearly, diet is a central part of the treatment, but to get the benefits of very low cholesterol levels, drug treatment is often necessary. ...Optimal use of diet and appropriate use of medications will dramatically reduce the risk of MI, stroke, and death from heart disease. These new data should help motivate any patients who have been hesitating about treating their cholesterol to talk with their physician to get the benefits of intensive cholesterol lowering”

 And... in the August 2, 2005 issue of the Annals of Internal Medicine of the American College of Physicians Dr. John V.L. Sheffield and Dr. Eric B. Larson reviewed data regarding Cardiovascular Disease and Statin Use and they noted the following:

This year's trial results [2004] indicate a real change in our understanding of indications for the use of statins.

In type 2 diabetic patients with at least 1 additional risk factor for coronary heart disease, lipid-lowering treatment with statins is effective for primary prevention of cardiovascular disease (CVD). In patients with acute coronary syndromes, early initiation of intensive lipid-lowering treatment to achieve serum low-density lipoprotein (LDL) cholesterol levels below 1.80 mmol/L (<70 mg/dL) prevents major cardiovascular events more effectively than moderate lipid lowering.

Intensive lipid lowering is also beneficial for patients with stable coronary disease.

These results indicate that statin treatment could benefit a greater number of patients and that target LDL cholesterol levels for treatment of patients at highest risk should be lower than previously recommended. 

Because these findings indicate that patients are now more likely to be using statins for many years, we are reassured to learn that treatment for as long as 10 years appears to be safe.”

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ATTENTION  ALL  LYMPHOMA PATIENTS AND ALL PERSONS  —- BE INFORMED AND INFORM YOUR PHYSICIANS AND YOUR FRIENDS ABOUT THE DATA REGARDING ‘STATIN’ ANTI-CHOLESTEROL MEDICATION and THE ROLE OF MAMMOGRAPHY TO ACHIEVE AN EARLY DIAGNOSIS OF BREAST CANCER —-

GO TO THE ‘HEART' AND ‘BREAST CANCER’ PAGES OF THE LYMPHOMA FOUNDATION WEBSITE TO REVIEW THIS INFORMATION

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THE LYMPHOMA FOUNDATION'S CURRENT AND PREVIOUS DISTRIBUTION OF GRANT SUPPORT TO MAJOR CANCER CENTERS FOR A BROAD SPECTRUM OF BASIC AND CLINICAL RESEARCH OF THE LYMPHOMAS AND ALLIED DISEASES


UNIVERSITY OF UTAH — HEMATOLOGY DIVISION — SCHOOL OF MEDICINE—
SALT LAKE CITY, UTAH
Studies of the early stages of lymphoid development, using a novel culture model that provides a differentiation signal crucial to specification of the T lymphocyte lineage at the stage of the lymphoid progenitor.

DUKE UNIVERSITY MEDICAL CENTER — DURHAM, NORTH CAROLINA
Studies in aging regarding the relationship of hPot1 and cellular senescence, a biomarker of aging. The objective will be to determine which proteins hPot1 interacts with to keep the telomere in a closed state, and hence protect telomeres from eliciting a senescence signal.

YALE UNIVERSITY CANCER CENTER — NEW HAVEN, CONNECTICUT
Clinical management of patients with Hodgkin’s disease and the non-Hodgkin’s lymphomas

TUFTS MEDICAL CENTER --- BOSTON, MASSACHUSETTS
Studies in new approaches to the treatment of multiple myeloma and allied disorders

CORNELL NEW YORK-PRESBYTERIAN HOSPITALS — NEW YORK, NEW YORK
▪ Further assessment of the anti-CD22 antibody epratuzumab and other monoclonal antibodies in B-cell malignancies. 
▪ Evaluation of combination regimens with rituximab and biologic agents (including IL-2, anti-CD80, revlimid and CpG immunostimulatory oligonucleotides).

MEMORIAL SLOAN KETTERING CANCER CENTER —NEW YORK, NEW YORK
▪ Targeting the ubiquitin proteasome pathway  in indolent and mantle cell lymphoma.
▪ Alpha-particle immunotherapy by targeted Alpha-emitters or Alpha-emitting isotope generators.
Seeking genetic modifiers that are protective against cancer in a subset of elderly individuals.
Analysis of cancer prevention data in children of families affected by hereditary cancer syndromes.
▪ I
ntensity-modulated radiotherapy for lymphoma involving the mediastinum.
▪ Methods to overcome platinum resistance, consolidation strategies in patients with ovarian cancer and immune directed strategies directed towards CA-125.
▪ New approaches to the treatment of multiple myeloma.
▪ Treatment of patients with low grade lymphoma and chronic lymphocytic leukemia.
▪ Analysis of Schwann cell origin: the role of tumor environment of Neurofibromas in NF1.
High-dose chemotherapy and stem cell transplantation for Large Cell Lymphoma and relapsed and refractory Hodgkin’s disease.
▪ Continuing development of DNA vaccines against CD20 antigen expressed by lymphoma cells.

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SUMMARIES OF RESEARCH IN PROGRESS

Monoclonal antibody, Anti-sense BC-2 and Bortezomib therapy JOHN P. LEONARD, M.D.,  Joan and Sanford Weill Medical College of Cornell University “The assistance of the Lymphoma Foundation [will] be used to support the following efforts at our center in very meaningful ways…”  “Novel initial therapies for aggressive lymphoma.  We continue to explore ways to improve outcomes with chemotherapy, particularly combinations of CHOP chemotherapy and rituximab along with agents such as Bcl-2 antisense, idiotype vaccines, and bortezomib (Velcade).  Trials with these are ongoing, and initial phase I results of the CHOP-R-Velcade study have been submitted to ASH.  We are excited about these preliminary findings, and the support from the Lymphoma Foundation will help us to continue this trial as well as to conduct correlative studies on tumor tissue that will allow us to characterize tumors from the molecular standpoint in the patients on the study.  We also plan additional future trials with other novel agents.” “Further assessment of the anti-CD22 antibody epratuzumab and other antibodies in B-cell malignancies.  We continue to study this agent, with which we have demonstrated evidence of clinical activity and manageable toxicity.  We are evaluating patients treated with single-agent epratuzumab, repeated courses (at relapse) as well as in combination with rituximab.  Substantial numbers of these patients remain in remission years later (initial results from one study recently reported in the JCO).  Our initial efforts are encouraging in this regard, and we are currently conducting a pilot study in lymphoplasmacytic lymphoma (which highly expresses CD22).  We are also attempting to identify clinical, laboratory, and pathologic parameters, which may correlate with response and therefore allow us to better target appropriate patient populations.  Further trials in combination with CHOP-R and with rituximab are being planned.  Additionally, we are currently conducting phase I studies with anti-CD40 and anti-interleukin 6 monoclonal antibodies.”

Is there a genetic (inherited) component that protects against the development of cancer? KENNETH OFFIT, M.D., MPH, Memorial Sloan Kettering Cancer Center: As a result of the “genetic revolution” it is now possible to look for genetic variations between individuals and to learn if these are associated with disease.  The goal of one aspect of our genetic research  at the Memorial Sloan Kettering Cancer Center has been to use “whole genome” technologies to look for genetic markers that will predict resistance to disease in the elderly.  Our initial research paper soon to be published demonstrated that it is possible to do “whole genome” analysis to “rediscover” known genes.  As preliminary data we performed low density genomic scans and we have been able to resolve two significant regions: one on chromosome 12 and one on chromosome 22 that may be associated with the resistance to breast cancer in this elderly population.  As we continue our research we hope to better map these regions and to discover other genetic regions that confer cancer resistance in the elderly.

How is cell senescence (aging) controlled
CHRISTOPHER M. COUNTER, PhD, Duke University Medical School Human cells can continue to divide up to a time when they stop growing and enter a period termed senescence.  It is thought that this hard-wiring of cell lifespan may be related to the process of aging.  One of the 'clocks' that keeps track of how long a cell can continue to divide is the end of the chromosomes, or telomeres.  Telomeres shorten every round of cell division, ticking off the number of divisions a cell has left.  When telomeres reach a short length associated with senescence it is proposed that they signal the cell to stop dividing, perhaps because the telomeres become recognized as damaged DNA.  We have shown that reducing the amount of the telomere-binding protein, hPot1, achieves the same fate, namely that cells stop dividing and enter what appears to be senescence.  We are now very interested in determining how this occurs, and are currently testing what functions of hPot1 can stop this senescence.  Understanding how loss of hPot1 function induces senescence may shed light on this process, and aging.

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THE DILEMMA POSED IN CHOOSING TREATMENT OF ‘LOW GRADE’ FOLLICULAR LYMPHOMAS
The ‘indolent’ follicular lymphomas are not usually aggressive early in their course and may be ‘observed’ for many years without any  treatment as noted in a COMMENTARY by Craig H. Moskowitz, M.D. (in BLOOD February 15, 2005, Vol.105, Number 4)
“Follicular lymphoma is a chronic disease with a variable course; many patients can be monitored for years without therapy yet others need to be treated aggressively at the onset. Median survival in 2004 approaches 14 years…”  

New approaches to treatment are being studied in order to secure the much needed improved longer-term survival. 
1)
Human clinical trials are underway with an ‘auto’ vaccine (a vaccine developed from the patients’ own lymph node cells) added to primary forms of chemotherapy with or without monoclonal antibody treatments. Uniquely different trials are outlined on the National Cancer Institute Clinical Trials website. There are no conclusions yet and much time will have to pass before it is determined whether or not this approach improves survival. [GO TO HOME PAGE TO REVIEW HOW TO LOG ON TO THE CLINICAL TRIALS SITE AND ACCESS THE LYMPHOMA VACCINE TRIALS]

2) Some of the latest clinical human research implies that the best current approach to treatment for Follicular Lymphoma
is a combination of chemotherapy plus the monoclonal antibody rituximab in sequence… and possibly with long term intermittent maintenance treatment with rituximab

Frontline therapy with rituximab added to the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) significantly improves the outcome for patients with advanced-stage follicular lymphoma compared with therapy with CHOP alone: results of a prospective randomized study of the German Low-Grade Lymphoma Study Group” Hindemann, et al in BLOOD December 1, 2005 Vol.106, Number 12, pp 3725-3732: 

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