ONCOLOGY.
No. 2
Follicular Lymphoma: Expanding Therapeutic Options
By APAR KISHOR GANTI, MD
Clinical Fellow
Section of Oncology/Hematology
Department of Internal Medicine
R. GREGORY BOCIEK, MD
Assistant Professor
Section of Oncology/Hematology
Department of Internal Medicine
PHILIP J. BIERMAN, MD
Associate Professor
Section of Oncology/Hematology
Department of Internal Medicine
CHARLES A. ENKE, MD
Professor and Chair
Department of Radiation Oncology
JULIE M. VOSE, MD
Neumann M. and
Mildred E. Harris Professor
Chief, Section of
Oncology/Hematology
Department of Internal Medicine
JAMES O. ARMITAGE, MD
Professor
Section of Oncology/Hematology
Department of Internal Medicine
University of Nebraska,
Omaha, Nebraska |
February 1, 2005
Future Directions
Vaccines
The B-cell lymphomas express a
tumor-specific clonal immunoglobulin
(idiotype). This is composed of
the unique antigenic determinants in
the variable regions of the clonal immunoglobulin
expressed by the tumor
cells. This can be recognized by
the immune system and can serve as a
target for active immunotherapy. Hsu
et al treated 41 patients with B-cell
NHL using a vaccine consisting of
tumor immunoglobulin protein coupled
to keyhole limpet hemocyanin.
In their series, 20 patients generated
specific immune responses against the
idiotypes of their tumor immunoglobulin.
Patients who mounted an
immune response had increased progression-
free survival (7.9 vs 1.3
years) and overall survival (median
survival not reached vs 7 years), as
compared to those who did not mount
an immune response.[129]
Timmerman et al vaccinated 35
patients with dendritic cells pulsed
with tumor-derived idiotype protein.
Of the 23 patients who completed the
vaccination schedule, 15 mounted an
immune response, either T-cell-
mediated or immune-mediated. At a
median of 43 months after chemotherapy,
16 of 23 patients showed no
tumor progression. Six patients who
experienced progression received
booster doses of the vaccine, and three
of them had a response.[130]
Newer Monoclonal Antibodies
The success of the monoclonal antibody
rituximab and the radioimmunoconjugates
tositumomab and
ibritumomab has spurred research into
the development of newer targeted
therapies directed toward NHL.
Epratuzumab (anti-CD22) and apolizumab
(Hu1D10) seem most promising
in this regard.
Epratuzumab is a humanized
monoclonal antibody directed against
the CD22 determinant RFB4, which is
present on 75% of B lymphocytes.[131]
In a phase I/II trial, Leonard et al
treated 55 patients with escalating doses
of epratuzumab and obtained objective
responses in 24% of patients
with follicular lymphoma. A 43% objective
response rate was seen in follicular
lymphoma patients treated at
360 mg/m2/wk, suggesting that this
dose should be explored further.[132]
Postema et al tried to determine the
maximum tolerated dose of a new radioimmunoconjugate
created by a
combination of epratuzumab with rhenium
(Re)-186 in a phase I study.
They found that Re-186 epratuzumab
at a dose of 2.0 GBq/m2 was well
tolerated. Five out of 15 patients with
NHL of diverse histology showed objective
responses following a single
dose of Re-186 epratuzumab.[133]
Apolizumab is a humanized IgG1
monoclonal antibody that binds to a
variant (likely posttranslational
modification) of the HLA-DRB
chain.[134] Apolizumab induces antibody-
dependent cellular cytoxicity
and complement-mediated lysis as
well as signaling via tyrosine phosphorylation
in lymphoma cell lines,
and hence, it is being evaluated in
NHL.[135] In a phase I study conducted
at the NCI, 20 patients were
treated at various dose levels. The
toxicity observed was mainly grade 1
and 2, and occasionally grade 3. The
investigators found clear evidence of
antitumor effects, especially in follicular
lymphoma, where four of eight
patients demonstrated an objective
response.[136]
Galiximab is a macaque-human chimeric
antibody directed against CD80.
CD80 is an immune costimulatory molecule
expressed on the surface of a
wide variety of hematologic malignancies,
including follicular lymphoma.[
137] Czuczman et al conducted a
phase I/II trial evaluating the efficacy
of galiximab in the treatment of relapsed/
refractory follicular lymphoma.
They treated 37 patients with escalating
doses of galiximab and found that
the agent was well tolerated with no
major adverse effects. They observed
two complete responses and one partial
response in 34 evaluable patients,
for an overall response rate of 9%.[137]
In another phase I study, Gordon
et al combined escalating doses of
galiximab with rituximab in patients
with relapsed/refractory follicular
lymphoma. They enrolled 12 patients
into this phase of their study, and at
50 days, they observed three complete
and four partial responses. They
also found no major adverse effects
or dose-limiting toxicities.[138] These
results show that galiximab is a
potentially safe and effective treatment
for relapsed/refractory follicular
lymphoma.
Antisense Therapy
The bcl-2 gene is commonly overexpressed
in NHL.[139] More than
85% of patients with follicular
lymphoma and t(14;18) overexpress
bcl-2.[140] This leads to resistance to
apoptosis, thereby promoting tumorigenesis.[
139] Waters et al conducted
a phase I study to evaluate the efficacy
and toxicity of an antisense oligonucleotide
targeting bcl-2 in patients
with NHL. Among the 21 patients
they treated with the oligonucleotide,
there was one complete response, two
minor responses, nine cases of stable
disease, and nine cases of progressive
disease, thereby demonstrating that
antisense therapy was feasible and
potentially effective in NHL.[141]
Proteasome Inhibitors
The proteasome is a multienzyme
complex that is present in all eukaryotic
cells. It degrades proteins that
regulate cell-cycle progression and
causes proteolysis of the endogenous
inhibitor of nuclear factor (NF)-
kappaB.[142] Bortezomib (Velcade)
is a boronic acid derivative that is a
highly selective, potent, reversible
proteasome inhibitor. The initial demonstration
of in vivo antitumor activity
of a proteasome inhibitor used a
human lymphoma xenograft model,[
143] leading to an interest in the
use of this agent in lymphoid malignancies.
O'Connor et al administered
bortezomib to 21 previously treated
patients with relapsed or refractory
indolent lymphomas (small lymphocytic
lymphoma/chronic lymphocytic
leukemia type [n = 3], follicular lymphoma
[n = 9], mantle cell lymphoma
[n = 8], and nodal marginal zone lymphoma
[n = 1]). They found that six
of the eight evaluable patients with
follicular lymphoma achieved a major
response, with one patient obtaining
a durable complete response.[144]
CpG Oligonucleotides
Bacterial DNA and synthetic oligodeoxynucleotides
containing unmethylated
cytosine-guanine dinucleotides
known as cytosine phosphorothioate
guanine (CpG) oligodeoxynucleotides
can activate immune-cell subsets, including
cells that participate in antibody-
dependent cell-mediated cytotoxicity.
Through these effects, CpG
oligonucleotides could potentially
augment the antitumor effects of monoclonal
antibodies. Indeed animal
studies have shown that CpG oligonucleotides
enhance the efficacy of
antitumor monoclonal antibody therapy
in the 38C13 murine B-cell
lymphoma.[145]
Friedberg et al conducted a phase I
study combining escalating doses of
an immunostimulatory CpG oligonucleotide
(1018 ISS) with rituximab in
16 patients with relapsed/refractory
NHL (13 patients with follicular lymphoma).
The regimen was well
tolerated with no major toxicities,
producing one complete response, five
partial responses, and two cases of
progressive disease. Interestingly,
these investigators also found an increase
in the expression of several
interferon-inducible genes. This provides
a rationale for further investigation
of combination immunotherapy
approaches in NHL.[146]
Nonmyeloablative Stem
Cell Transplantation
The biggest drawback to the routine
use of allogeneic stem cell transplantation
in the management of
follicular lymphoma is the increased
incidence of transplant-related mortality.
The success of donor lymphocyte
infusion in treating relapses following
allogeneic HSCT has led to the thinking
that a graft-vs-lymphoma (GVL)
effect, mediated by lymphocytes, is at
least partly responsible for the efficacy
of allogeneic stem cell transplantation.
Also supporting the existence of
the GVL effect is the fact that patients
who develop chronic GVHD after allogeneic
HSCT have a lower probability
of relapsing than patients who
do not develop chronic GVHD.[147]
In a study at the M. D. Anderson
Cancer Center, Khouri et al treated 20
patients with indolent NHL with the
combination of fludarabine, cyclophosphamide,
and rituximab. They
achieved a 2-year overall and relapsefree
survival rate of 84%.[148] This
study demonstrates the feasibility and
efficacy of a relatively nontoxic, nonmyeloablative
conditioning regimen for
the treatment of follicular lymphoma.
Conclusions
In conclusion, long-term diseasefree
survival is possible in select
groups of patients with follicular lymphoma.
Patients who have early-stage
disease and those who achieve a complete
response following initial chemotherapy
tend to have long-term
disease-free survival. The introduction
of newer therapeutic modalities
such as immunotherapy, radioimmunotherapy,
and advances in stem cell
transplantation has improved outcomes
in follicular lymphoma over
those seen with conventional chemotherapy
and RT alone. However, because
follicular lymphoma is an
indolent disease, watchful waiting is
still a good option in elderly asymptomatic
patients with a low tumor
burden. For patients who relapse following
a complete or partial response,
salvage chemotherapy followed by
auto-HSCT improves outcomes as
compared with conventional therapy.
For younger patients with chemoresistant
disease, allogeneic HSCT must
be considered if patients have an HLAidentical
sibling, as this strategy probably
offers the best chance for cure in
this subgroup.
There is reason for excitement
about the prospects for effective vaccine
therapies for lymphoma, as randomized
vaccine trials commence and
newer cell-based vaccine trials enter
the clinic. With such promising new
prospects on the horizon, follicular
lymphoma-long thought to be incurable-
may soon have curative options,
at least in a subset of patients.
FERNANDO CABANILLAS, MD
MICHEL VAN GELDER, MD and HARRY C. SCHOUTEN, MD
DAN L. LONGO, MD
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