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December 2013, Supplement to Volume 17, Number
6
Article
Autologous Hematopoietic Stem Cell Transplantation for Multiple
Myeloma: Frequently Asked Questions
Patricia A. Mangan, MSN, APRN-BC, Charise L.
Gleason, MSN, ANP-C, AOCNP®, and Teresa Miceli, RN, BSN, OCN®
When caring for patients with multiple myeloma,
questions often arise about the role and timing of autologous hematopoietic
stem cell transplantation. As a complement to the other articles in this
supplement, as well as to ensure that readers are provided with the insight
needed to feel comfortable speaking to patients and other practitioners about
this topic, the authors address eight frequently asked questions about common
decision points in the process of autologous hematopoietic stem cell
transplantation as a treatment for patients with multiple myeloma.
Who are the best
candidates for transplantation?
Multiple myeloma is the leading indication for
autologous hematopoietic stem cell transplantation (AHSCT) in North America,
which has become the standard of care for patients aged 65 years and younger (Gertz, Ghobrial, & Luc-Harousseau, 2009; Giralt et al.,
2009; Moreau, Avet-Loiseau, Harousseau,
& Attal, 2011; Palumbo & Anderson, 2011;
Palumbo, Attal, & Roussel,
2011; Pasquini & Wang, 2012). Several randomized
clinical trials demonstrated a superior survival outcome for patients who
underwent high-dose melphalan and AHSCT when compared
to those who received standard-dose chemotherapeutic agents (Attal et al., 1996; Matsui, Borrello,
& Mitsiades, 2012; Palumbo, Attal,
et al., 2011). Although most of those trials were conducted before newer agents
such as lenalidomide, bortezomib,
and thalidomide were available, more recent comparative trials using lenalidomide-containing initial regimens, with or without
AHSCT, continue to demonstrate superiority of survival. One study stated that
progression-free survival (PFS) at two years is 73% with transplantation
compared to 43% without transplantation (Palumbo, Cavallo,
et al., 2011). With that in mind, AHSCT should at least be considered for all
patients with active multiple myeloma who have
adequate organ function and performance status (Palumbo & Rajkumar, 2010).
AHSCT is not without risk and results in morbidity
and mortality for 1%–2% of patients, usually from infection, bleeding, or organ
toxicity (Hari & McCarthy, 2013). Patients with
poor performance status are at a higher risk for these complications. Organ
dysfunction, including compromised cardiac or liver function, as well as renal
insufficiency, also predict a higher risk of toxicity and may lead to poor
outcomes (Cavo et al., 2011; Palumbo & Anderson,
2011). Patients older than 70 years can undergo transplantation, but the
incremental benefit of transplantation in this age group has not been
demonstrated in randomized, prospective clinical trials. In addition, the
standard dose of melphalan (200 mg/m2) has
been shown to be of increased toxicity in patients older than 70 years with
poor performance status and other comorbidities. A risk-adapted dosing of melphalan for patients older than aged 70 years (e.g., 140
mg/m2) and patients with renal insufficiency (100 mg/m2)
has allowed patients to successfully undergo transplantation with acceptable
toxicities (Gertz et al., 2009). Therefore, the use
of AHSCT in these populations should be conducted cautiously and with
risk-adapted dose modification of melphalan.
Patients with poor risk biology, defined by
cytogenetic abnormalities such as t(4;14), del (17p),
as well as high b2 microglobulin, have
shorter remission duration after AHSCT. Although this varies widely, median
overall survival in the poor risk group can range from 18–36 months (Chang et
al., 2004; Neben et al., 2010). This group of patients is
the subject of clinical trials incorporating newer agents, including
next-generation immunomodulatory medications and
proteasome inhibitors that may improve overall results (Bladé, Rosiñol, Cibeira, Rovira, & Carreras,
2010; Palumbo & Rajkumar, 2010). Participation in
clinical trials should be encouraged whenever possible.
What is the optimal
timing for transplantation?
The role of initial therapy for patients with symptomatic
myeloma is to stabilize the patient, improve any organ dysfunction, and obtain
a tumor response prior to transplantation. Patients who attain deep remissions
and reversal of organ dysfunction have the best success following AHSCT.
Whether attempting to deepen the response by extending induction therapy is
beneficial prior to stem cell transplantation is unclear. In fact, continued
initial therapy for months after attaining a response may cause toxicity as
well as decrease the stem cell yield, particularly if the initial therapy
includes alkylating agents or prolonged use of immunomodulatory
agents (Giralt et al., 2009). Although a complete
remission is obviously favorable, treatment beyond six cycles of therapy in an
attempt to achieve a deeper remission does not definitively improve outcome (Cavo et al., 2011).
Data comparing the benefit of induction therapy
followed by high-dose melphalan and AHSCT to up-front
chemotherapy alone as initial therapy for active myeloma demonstrate
improvement in PFS, response rates, and overall survival (OS) (Attal et al., 1996; Child et al., 2003). High-dose
chemotherapy and stem cell transplantation as part of first-line therapy after
initial response has resulted in median survival of more than five years
compared to response without AHSCT (Attal et al.,
1996; Child et al., 2003). Patients undergoing transplantation as part
of their initial line of therapy have experienced longer event-free survival
and better quality of life than patients who undergo stem cell transplantation
as a late therapy, but early transplantation has not been shown to improve
overall survival (Cavo et al., 2011; Fermand et al., 1998; Palumbo & Anderson, 2011;
Palumbo, Attal, et al., 2011). On the other hand,
retrospective analyses of series of patients treated with AHSCT during their
first line of therapy have reported similar outcomes as patients treated with
transplantation as part of second-line therapy (Gertz
et al., 2009; Palumbo, Attal, et al., 2011). The
optimal timing for transplantation continues to be an area of investigation. An
international, prospective comparison of transplantation as first-line therapy
versus second-line therapy is underway to help clarify this issue
(ClinicalTrials.gov, n.d.a.; Moreau et al., 2011).
Despite the success of high-dose melphalan
and AHSCT, the regimen is not a curative treatment, and the majority of
patients will relapse. Many strategies have been used to improve survival for
patients with multiple myeloma who have undergone AHSCT, such as tandem transplantation,
second transplantation, and using newer agents (e.g., lenalidomide,
bortezomib, thalidomide) as consolidation therapy or
maintenance therapy after stem cell transplantation.
What is the role of
tandem transplantation?
Tandem autologous transplantation occurs when two
auto-logous transplantations are performed within a
period of no more than six months. For more than two decades, patients with
multiple myeloma have successfully been treated with tandem stem cell
transplantation using high-dose melphalan. One trial
showed improved PFS and OS with tandem transplantation compared to single
transplantation (Attal et al., 2003). That study
suggests that patients who either progress after the first transplantation or
are in complete remission are less likely to benefit from the second
transplantation. Patients who achieve less than a very good partial response
(VGPR) but are responding and have tolerated the first transplantation well may
be the best candidates for a second transplantation (Bladé
et al., 2010; Cavo et al., 2011; Moreau et al.,
2011). A large national trial is underway to prospectively compare single AHSCT
with tandem AHSCT, which should help clarify this issue (ClinicalTrials.gov, n.d.b.).
What is the role of
salvage transplantation?
Mobilization techniques have improved and stem cells
now can be stored for more than a decade. Salvage AHSCT has been used for
patients who have relapsed after a prior stem cell
transplantation, or who had stem cells harvested and did not initially proceed
to stem cell transplantation. Response rates in the setting of relapsed and
refractory myeloma are high, although the toxicity is increased (as high as 10%
mortality versus 1%–2% mortality when AHSCT is conducted in the initial line of
therapy) (Olin et al., 2009). Response durations also tend to be shorter
(measured in months rather than years) with a second stem cell transplantation,
or one conducted in the setting of refractory disease (Cook et al., 2011; Olin
et al., 2009). Frequently, the remission induced by a stem cell transplantation
acts as a bridge to another therapy for which the patient was not eligible
because of rapid progression of disease or organ dysfunction. An intermediate
dose of melphalan (100–140 mg/m2) usually
is used in this setting, keeping in mind the patient’s performance status and
organ function and implementing the same risk-adapted approaches used for
initial therapy.
What is the role of
consolidation therapy after stem cell transplantation?
Despite the improvement in survival after AHSCT, a
high likelihood of disease progression remains. Interest is increasing in the
role of post-transplantation consolidation using lenalidomide,
bortezomib, and alkylating agents as consolidation
therapy. A number of trials (Cavo et al., 2011; Hari & McCarthy, 2013) have demonstrated the
feasibility of this approach, and regimens such as bortezomib,
lenalidomide, and dexamethasone and bortezomib, thalidomide, and dexamethasone for two to four
cycles following AHSCT and prior to initiation of maintenance therapy have been
well tolerated with suggestion of improved duration of response. Preliminary
results show increasing rates of complete remission following consolidation
therapy. Once again, a number of clinical trials are prospectively analyzing
the incorporation of these regimens after stem cell transplantation.
What is the role of
maintenance therapy after autologous hematopoietic stem cell transplantation?
Although AHSCT is associated with improved remission
rates and PFS, relapse is inevitable for almost all patients. The goal of
maintenance therapy is to prolong the duration of remission, extend OS,
maintain quality of life, and reduce toxicities (Matsui et al., 2012; Moreau et al., 2011).
Maintenance therapy has been investigated since the 1990s, and a number of
approaches have been used. Alpha interferon given subcutaneously initially
showed benefit, but prospective randomized trials demonstrated increased
toxicity without a clear survival advantage (Attal et
al., 1996; Cunningham et al., 1998). Oral thalidomide also has been used in the
maintenance setting, with several randomized trials demonstrating improved
remission rates, PFS, and OS. However, the use of thalidomide in this setting
is limited because of cumulative toxicities including neurotoxicity and the
development of resistance with prolonged exposure (Cavo
et al., 2011; Gertz et al., 2009). Pulse doses of
corticosteroids (prednisone or dexamethasone) also have been used after stem
cell transplantation, showing improved PFS and tolerability with intermittent
administration (Berenson et al., 2002).
A number of prospective trials have assessed
low-dose lenalidomide as a maintenance therapy after
AHSCT. McCarthy et al. (2012) showed significant PFS benefit in patients who
received low-dose lenalidomide (86%) versus those who
did not (58%), in addition to an OS advantage at three years of 88% versus 80%,
respectively. Attal et al. (2012) showed a PFS
benefit for the lenalidomide maintenance group at
four years of 43% compared to 22% for those who did not receive lenalidomide. In those trials, lenalidomide
was given until either progression or toxicity precluded additional use.
Maintenance lenalidomide was well tolerated with a
low incidence of neurotoxicity. However, the risk of second cancers, including
solid tumor and hematologic malignancies, increased (Attal
et al., 2012; McCarthy et al., 2012). Second cancers have been observed in
patients with multiple myeloma; however, the risk has been less than 5% in
previous studies (McCarthy et al., 2012). Most recent analyses report that the
incidence of second cancers increases to 8% for patients on lenalidomide
(McCarthy et al., 2012). When compared to the risks of progressive myeloma, the
consensus remains supportive of the use of lenalidomide
as maintenance therapy. However, research is ongoing. Efforts are now underway
to identify the mechanisms for secondary malignancies and to determine risk
factors that might reduce the likelihood of carcinogenesis (Cavo
et al., 2011).
Bortezomib as
part of initial and maintenance therapy has been shown to improve outcomes when
compared to a similar regimen containing thalidomide instead of bortezomib (PFS median survival = 13 months versus 30
months; median OS = 21 months versus 54 months, respectively) (Sonneveld et al., 2012). When given on a weekly or biweekly
schedule, bortezomib is well tolerated, although
neurotoxicity remains a potential side effect. The relative benefit of
proteasome inhibitors to immunomodulatory agents as
single-agent maintenance therapy as well as in combination continues to be an
area of active investigation (Palumbo & Anderson, 2011; Sonneveld
et al., 2012). The combination of thalidomide and bortezomib,
for instance, has been shown to be well tolerated and may result in improved
disease-free outcomes (Mateos et al., 2012).
Maintenance therapy prolongs duration of remission,
particularly for those who have achieved less than a VGPR. The ultimate benefit
of maintenance therapy for those who have achieved complete remission after
transplantation remains to be determined. However, increasing knowledge
suggests that continued exposure may be advantageous even for patients in
complete remission by preventing proliferation of malignant plasma cells and by
maintaining a hostile bone marrow microenvironment (Giralt,
Landau, & Palumbo, 2012; Matsui et al., 2012; McCarthy et al., 2012).
Additional evaluation may clarify the use of maintenance in the
post-transplantation setting (ClinicalTrials.gov, n.d.b).
Is there a role for
transplantation in the era of novel therapies?
Since 2000, the survival of patients with multiple
myeloma has substantially improved. The median OS for patients with multiple
myeloma in 1996 was three years; in 2012, patients had a median OS of eight
years (McCarthy et al., 2012). That is a result of the incorporation of newer
agents (e.g., thalidomide, lenalidomide, bortezomib) and the use of high-dose melphalan
and AHSCT. Given that information, the timing of high-dose melphalan
and stem cell transplantation should be considered. As noted earlier, despite
the use of lenalidomide and dexamethasone in both
groups of patients, the incorporation of high-dose therapy and AHSCT continues
to improve the survival of patients compared to those who did not receive transplantation
(Bladé et al., 2010). That finding may be explained
by the heterogeneous nature of myeloma cells and the complementary nature of
the use of high-dose alkylating agents, such as melphalan,
to overcome the resistance mechanisms in cells that are otherwise resistant to immunomodulatory agents and bortezomib.
In particular, melphalan may have a greater effect
against the myeloma stem cell. Additional studies investigating high-dose melphalan and autologous transplantation in the era of
newer agents are ongoing.
What needs to be
considered when choosing a transplantation center?
Healthcare insurance coverage should be considered
when choosing a transplantation center. The cost of transplantation can be
prohibitive and requires insurance approval. Patients without insurance will
require assistance from resourceful social workers and financial counselors to
successfully undergo transplantation. Insurance carriers frequently contract
with a select group of “centers of excellence” or other transplantation
networks that they direct their patients to for evaluation; these may or may
not be geographically close to where the patient lives. If the third-party
payer does not direct the patient to a particular transplantation center, the
primary hematologist may refer the patient to a center with which he or she has
had prior success. Geographic location and resources available within that
community also are important factors in choice of centers. Fortunately, most
regions of the country have one or more experienced centers within close
proximity of the patient in need. Ultimately, patients and their primary
oncologists need to feel comfortable with the treatment philosophy and care
approach of their transplantation team. A listing of available transplantation
centers by location, disease, and statistical review can be found
at www.CIBMTR.org or www.HRSA.gov.
Summary
Since 1998, high-dose melphalan
and AHSCT have been a standard of care for patients with multiple myeloma,
particularly when administered early in the course of disease. The willingness
of patients to participate in the randomized comparative trials has been
essential to the development of successful treatment approaches. The current
practice of combining an initial (or induction) course of chemotherapy to
autologous stem cell harvest and one or two cycles of high-dose melphalan and AHSCT followed by maintenance therapy with lenalidomide or bortezomib has
resulted in unprecedented survival for this disease. A number of questions
concerning the optimal timing, best initial therapy, post-transplantation
consolidation, and maintenance therapy still remain. Ongoing clinical trials of
innovative approaches hold great promise that these questions will be answered
soon. The ultimate result will be improved survival and quality of life for
patients with multiple myeloma.
The authors gratefully acknowledge Brian G.M. Durie, MD, and Diane P. Moran, RN, MA, EdM,
senior vice president of strategic planning at the International Myeloma
Foundation, for their critical review of the manuscript.
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Patricia
A. Mangan, MSN, APRN-BC, is the nurse lead in the
Department of Hematologic Malignancies and Bone Marrow and Stem Cell Transplant
Programs in the Abramson Cancer Center at the University of Pennsylvania in
Philadelphia; Charise L. Gleason, MSN, ANP-C, AOCNP®, is a nurse practitioner
in the Winship Cancer Institute at Emory University
in Atlanta, GA; and Teresa Miceli, RN, BSN, OCN®, is a bone marrow
transplantation nurse coordinator and assistant professor of nursing in the
College of Medicine in the William von Liebig Transplant Center at the Mayo
Clinic in Rochester, MN. The authors received editorial support from Alita Anderson, MD, with Eubio
Medical Communications in preparation of this article supported by Sanofi Oncology. The authors are fully responsible for
content and editorial decisions about this article. Mangan
is on the speakers bureaus of Celgene Corporation,
Millennium: The Takeda Oncology Company, and Onyx Pharmaceuticals, and serves
as a consultant for Sanofi Oncology; and Gleason
serves a consultant for Celgene Corporation. Miceli has no financial relationships to disclose. The
content of this article has been reviewed by independent peer reviewers to ensure
that it is balanced, objective, and free from commercial bias. No financial
relationships relevant to the content of this article have been disclosed by
the independent peer reviewers or editorial staff. Mangan
can be reached at patricia.mangan@uphs.upenn.edu,
with copy to editor at CJONEditor@ons.org.
(Submitted July 2013. Revision submitted September
2013. Accepted for publication September 8, 2013.)
http://dx.doi.org/10.1188/13.CJON.43-47