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RESEARCH ARTICLE
Global characteristics and outcomes of autologous
hematopoietic stem cell transplantation for newly diagnosed
multiple myeloma: A study of the worldwide network for blood
and marrow transplantation (WBMT)
Laurent Garderet
1
| Luuk Gras
2
| Linda Koster
3
| Laurien Baaij
3
|
Nada Hamad
4
| Anita Dsouza
5
| Noel Estrada-Merly
6
| Parameswaran Hari
7
|
Wael Saber
5
| Andrew J. Cowan
8
| Minako Iida
9
| Shinichiro Okamoto
10
|
Hiroyuki Takamatsu
11
| Shohei Mizuno
12
| Koji Kawamura
13
|
Yoshihisa Kodera
14
| Bor-Sheng Ko
15
| Christopher Liam
16
| Kim Wah Ho
17
|
A. Sim Goh
18
| S. Keat Tan
18
| Alaa M. Elhaddad
19
| Ali Bazarbachi
20
|
Qamar un Nisa Chaudhry
21
| Rozan Alfar
22
| Mohamed-Amine Bekadja
23
|
Malek Benakli
24
| Cristobal Augusto Frutos Ortiz
25
| Eloisa Riva
26
|
Sebastian Galeano
27
| Francisca Bass
28
| Hira S. Mian
29
| Arleigh McCurdy
30
|
Feng Rong Wang
31
| Ly Meng
31
| Daniel Neumann
32
| Mickey Koh
33
|
John A. Snowden
34
| Stefan Schönland
35
| Donal P. McLornan
36
|
Patrick John Hayden
37
| Anna Sureda
38
| Hildegard T. Greinix
39
|
Mahmoud Aljurf
40
| Yoshiko Atsuta
41
| Dietger Niederwieser
42
Correspondence
Laurent Garderet, Service d'hématologie,
Hôpital Pitié Salpêtrière, 47-83 boulevard de
l'hôpital, 75013 Paris, France.
Email: laurent.garderet@aphp.fr
Abstract
Autologous hematopoietic cell transplantation (AHCT) is a commonly used treatment
in multiple myeloma (MM). However, real-world global demographic and outcome
data are scarce. We collected data on baseline characteristics and outcomes from
61 725 patients with newly diagnosed MM who underwent upfront AHCT between
2013 and 2017 from nine national/international registries. The primary endpoint was
overall survival (OS), and the secondary endpoints were progression-free survival
(PFS), relapse incidence (RI) and non-relapse mortality (NRM). Median OS amounted
to 90.2 months (95% CI 88.2–93.6) and median PFS 36.5 months (95% CI 36.1–
37.0). At 24 months, cumulative RI was 33% (95% CI 32.5%–33.4%) and NRM was
2.5% (95% CI 2.3%–2.6%). In the multivariate analysis, superior outcomes were asso-
ciated with younger age, IgG subtype, complete hematological response at auto-
For affiliations refer to page 2093
Received: 21 May 2024 Revised: 1 July 2024 Accepted: 21 July 2024
DOI: 10.1002/ajh.27451
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2024 The Author(s). American Journal of Hematology published by Wiley Periodicals LLC.
2084 Am J Hematol. 2024;99:2084–2095.
wileyonlinelibrary.com/journal/ajh
HCT, Karnofsky score of 100%, international staging scoring (ISS) stage 1, HCT-
comorbidity index (CI) 0, standard cytogenetic risk, auto-HCT in recent years, and
use of lenalidomide maintenance. There were differences in the baseline characteris-
tics and outcomes between registries. While the NRM was 1%–3% at 12 months
worldwide, the OS at 36 months was 69%–84%, RI at 12 months was 12%–24% and
PFS at 36 months was 43%–63%. The variability in these outcomes is attributable to
differences in patient and disease characteristics as well as the use of maintenance
and macroeconomic factors. In conclusion, worldwide data indicate that AHCT in
MM is a safe and effective therapy with an NRM of 1%–3% with considerable
regional differences in OS, PFS, RI, and patient characteristics. Maintenance treat-
ment post-AHCT had a beneficial effect on OS.
1|INTRODUCTION
Multiple myeloma (MM) is a plasma cell neoplasm characterized by
uncontrolled proliferation of mutated plasma cells, leading to specific
end-organ damage.
1
It was the third most common hematological
malignancy after non-Hodgkin lymphoma and leukemia in 2020, con-
tributing to 176 404 (14%) of the 1 278 362 blood cancers diagnosed
worldwide.
2
Although the cause of MM remains largely unknown, the
risk factors include male sex, Black race, older age, living in developed
countries, family clusters, radiation exposure, and obesity.
1,3
Two
additional studies confirmed a wide variation in the burden of MM,
with a higher incidence and mortality observed in men and countries
with a higher human development index.
4,5
Due to the introduction of
newly developed targeted therapies and transplantation techniques,
five-year overall survival (OS) has doubled over the past decade to
approximately 54%.
4,5
The utilization of autologous hematopoietic cell
transplantation (AHCT) plays an important role in the treatment of
MM.
6–10
The worldwide network for stem cell transplantation (WBMT)
was founded as a federation of several societies working in the field
of hematopoietic cell transplantation (HCT), with the aim of improving
HCT, stem cell donation, cellular therapy, accreditation, and access to
HCT worldwide, especially in countries with low or no activity. To this
end, the WBMT has since 2006 regularly published worldwide trans-
plant activity surveys.
11–13
Previous publications have revealed a vari-
able incidence of MM between countries, which has increased
uniformly since 1990, with the largest increase occurring in middle
and low-middle sociodemographic index countries. Access to effective
MM care is limited in many countries with low socioeconomic devel-
opment, particularly in sub-Saharan Africa.
1
AHCT activity in plasma
cell disorders, principally MM, has increased worldwide from 10 675
in 2002 to 23 701 in 2016.
2
Greater utilization has mostly been seen
in high-income regions, and it remains poorly utilized in Africa and the
Eastern Mediterranean Region (EMR). More work is needed to
improve access to AHCT in MM patients, especially in low-income to
middle-income countries.
14
The overall objective of this study was to analyze the outcomes
of AHCT in patients with MM from nine registries worldwide. The
outcomes of patients with newly diagnosed MM (NDMM) were com-
puted accounting for differences in patient and disease risk factors
between countries and country-specific macroeconomic factors.
2|PATIENTS AND METHODS
2.1 |Study design and data sources
This retrospective registry study was conducted through the WBMT,
utilizing data from their member societies and international or regional
registries on HCT for patients with NDMM aged ≥18 years between
2013 and 2017. As center-based activity reports do not contain
patient-specific information, member societies were asked to provide
patient, disease, AHCT characteristics, and outcome information. The
need for additional informed consent from patients was waived
because the study was performed by the secondary use of registry
data, and no personal information was transferred. The primary end-
point was OS and the secondary endpoints were progression-free sur-
vival (PFS), cumulative relapse incidence (RI), and non-relapse
mortality (NRM).
Outcome data were obtained through requests from the follow-
ing regional registries:
1. The Center for International Blood and Marrow Transplantation
(CIBMTR; www.cibmtr.org), the United States of America (USA),
2. The Canada registry using the Ottawa Blood Disease Center MM
Database (OBDCMMD),
3. Latin American Blood and Marrow Transplantation group
(LABMT).
4. The European Society for Blood and Marrow Transplantation
(EBMT; www.ebmt.org)
5. Australia and New Zealand Transplant & Cellular Therapies Regis-
try (ANZTCTR; www.anztct.org.au)
6. The Asian Pacific Blood and Marrow Transplant Group (APBMT;
www.apbmt.org) with reporting registries
a. Myeloma Transplant Registry, Ministry of Health, Malaysia
(MTRMOHM)
GARDERET ET AL.2085
b. Japan Society for Transplantation and Cellular Therapy/
Japanese Data Center for Hematopoietic Cell Transplantation
(JSTCT/JDCHCT)
c. Taiwan Society of Blood and Marrow Transplantation (TBMT)
d. Beijing Bone Marrow Transplant registry
7. Eastern Mediterranean Blood and Marrow Transplant Group
(EMBMT).
2.2 |Regional contributions
In 2016, 1662 teams in 86 countries across six WHO regions deliv-
ered HCT services. These included the Americas (AMR/PAHO; WHO
regions North, Middle, and South America, and Canada); Asia (SEAR/
WPR; WHO regions Southeast Asia and the Western Pacific Region,
which includes Australia and New Zealand); Europe (EUR, which
includes Turkey and Israel); and AFR/EMR [WHO regions Africa (AFR)
and Eastern Mediterranean Region (EMR)] (www.who.int/about/
regions/en/). A detailed list of organizations providing activity data
and the definitions used in the manuscript has been reported in previ-
ous publications.
4
The registries reported all AHCTs without time interval restric-
tions between diagnosis and AHCT, except for CIBMTR, which pro-
vided information on patients who underwent transplantation within
12 months of diagnosis.
2.3 |Definitions
Deletion 17p and/or t(4:14) and/or t(14:16) were considered
high-risk cytogenetic findings, with the remaining being standard
risk.
15
Hematological responses were defined according to the
IMWG criteria.
16
OS was defined as the time from AHCT to death
from any cause and PFS was defined as survival without relapse
or progression. RI was defined as the cumulative incidence of
either relapse or progression post-AHCT, and NRM as death
without evidence of relapse or progression. Transplant rate
(TR) was defined as the number of AHCTs in a country per
10 million inhabitants.
2.4 |Economic factors
Gross National Income (GNI) is defined as gross domestic product,
plus net receipts from abroad of compensation of employees, prop-
erty income, and net taxes less subsidies on production (https://
data.oecd.org/natincome/gross-national-income.htm). Current
health expenditure (HCE) includes healthcare goods and services
consumed each year without capital health expenditure. Both fac-
tors are expressed in current international dollars and converted
into purchasing power parity (PPP) per capita. Factors were
obtained from the World Bank (www.worldbank.org), WHO (www.
who.int),andUnitedNations(http://hdr.undp.org) for 2013–2017.
2.5 |Statistical analysis
Clinical, demographic, and AHCT-related characteristics at baseline were
tabulated by the year of AHCT, registry, and country. Continuous vari-
ables were expressed as median and interquartile range (IQR), and cate-
gorical variables were expressed as frequencies and proportions. Median
follow-up after baseline and 95% confidence intervals (CIs) were calcu-
lated using the reverse Kaplan–Meier (KM) method. The probabilities of
OS and PFS were estimated using the KM method, and the groups were
compared using the log-rank test. The cumulative incidence of NRM
together with RI was analyzed in a competing risk framework, and Gray's
test was used to compare the differences between the groups.
Associations between patient characteristics and outcomes were
evaluated by multivariate analysis (MVA) using Cox (cause-specific)
proportional hazard models based on complete cases. All models
included a random country effect (normally distributed) and the fol-
lowing variables: International staging scoring (ISS) at diagnosis, cyto-
genetic risk, age at AHCT, sex, year of AHCT, diagnosis and AHCT
time interval, immunoglobulin subtype, Karnofsky score (100 and
≤90%), stage at diagnosis, preparative regimen (type and dose), HCT-
comorbidity index (CI), and lenalidomide maintenance. As there was a
high degree of missing information on ISS at diagnosis, cytogenetic
risk, and HCT-CI, we analyzed the first model with all variables except
ISS, cytogenetic risk, and HCT-CI. A second analysis was performed
using a subset of patients with complete information on the three
additional aforementioned variables. The association between mainte-
nance therapy (lenalidomide, other, no maintenance) and OS, PFS, and
relapse was analyzed using landmark Cox proportional hazards models
at 3 months, including the subset of patients with available mainte-
nance data and the same two sets of confounders as described above.
All outcomes in the MVA analyses were artificially censored at
36 months. All tests were two sided. To determine the factors associ-
ated with the time-to-event outcomes, the type 1 error rate was fixed
at 0.05. No adjustments were made for the multiple comparisons. All
analyses were performed in R version 4.2.2 using “survival,”“cmprsk,”
and “prodlim”packages.
17
The methods used for the analysis of country-specific macroeco-
nomic factors are described in the Supplementary Material.
3|RESULTS
3.1 |Patient characteristics
A total of 103 847 first AHCTs for MM were reported in the WBMT
activity survey between 2013 and 2017.
3
Outcome information was
available for 61 725 NDMM patients (59.5%) from 629 transplant
centers in five WHO regions. AHCTs/year increased from 11 317 in
2013 (18.3%) to 13 498 in 2017 (21.9%). The mean number of trans-
plantations per year increased in all regions except in EMR (Table S1).
The transplant rate per 100 000 population in 2017 per region/
country is shown in Table S4. The patient, disease, and AHCT charac-
teristics are shown in Tables 1A and 1B. The median age at diagnosis
2086 GARDERET ET AL.
was 59.9 years with the lowest median age in the EMR (52.5 years)
and Malaysia (54.3 years) and highest in Ottawa, Canada (61.5 years).
The median year of diagnosis was 2014, and was well balanced
between registries. IgG (54.0%), light chain (24.4%), and IgA (18.6%)
were the predominant subtypes; however, there were significant dif-
ferences between regions. Disease stage at diagnosis was reported in
54.5% of patients (ISS I in 38.0%, ISS II in 34.8%, and ISS III in 27.1%)
and cytogenetics in 44.5% of patients (high risk 30.3%). Median age at
AHCT was 60.8 (IQR: 54.6–65.8) years, lowest in EMR (53.6 years)
and highest in Canada (62.2 years). Only 5.1% of patients were older
than 70 years at AHCT, with the lowest proportions in Malaysia (0%)
and EMR (0.6%), and the highest in the USA (9.8%). HCT-CI at AHCT
(available in 71.8%) was low in 52%, intermediate in 25%, and high in
23%. USA and Latin America reported high-risk HCT-CI scores in
42.2% and 5.5%, respectively. Karnofsky score at AHCT was ≤90% in
72.0%, lowest in Latin America (44.3%) and highest in Ottawa
(92.4%). Most patients underwent AHCT in very good partial remis-
sion (VGPR, 38.0%) and partial remission (PR, 36.2%). Complete remis-
sion (CR) was reported in 19.1% of patients, minimal remission/stable
disease (MR/SD) in 4.7%, and relapse/progression in 1.8%. The per-
centage of patients with VGPR or better ranged from 76% in Latin
America to 39% in Australia and New Zealand. The most frequently
used conditioning regimen was melphalan at a dose of 200 mg/m
2
(70% of patients). However, only 60.4% of patients received this dose
in Malaysia, as opposed to 89.6% in Ottawa, Canada. Only a minority
of patients had tandem AHCTs (6.7%): 10.1% in Europe and 1.3% in
the USA. Lenalidomide was used for posttransplant maintenance in
51% of 6801 patients for whom information was available (11.0% of
all patients).
3.2 |Outcome in the entire population
After a median follow-up of 41 months (IQR 19–60), median OS was
90.2 months (95% CI 88.2–93.6) and OS at 24 months was 88.4%
(95% CI 88.1–88.7) and 63.4% (95% CI 62.7%–64.0%) 72 months
(Figure 1A). The median PFS was 36.5 months (95% CI 36.1–37.0),
the PFS was 64.6% (95% CI 64.1%–65%) at 24 months, and 28.6%
(95% CI 28.0%–29.2%) at 72 months (Figure 1B). The cumulative RI
increased from 2.4% (95% CI 2.3–2.5) at 3 months to 33% (95% CI
32.5%–33.4%) at 24 months (Figure 1C) and 65.5% (95% CI 64.9%–
66.1%) at 72 months. In contrast, NRM was 0.6% (95% CI 0.6%–
0.7%), 2.5% (95% CI 2.3%–2.6%), and 5.9% (95% CI 5.6%–6.1%) at
3, 24, and 72 months, respectively (Figure 1D).
3.3 |Outcome according to regions
Three-year OS varied between regions, from 84.3% to 68.6% (p<.001;
Figure 2A and Table S2a). The longest median OS was observed in the
USA, and the shortest in Malaysia (Table S2a). The differences observed
within 12 months became more pronounced with longer follow-up
periods. PFS showed similar patterns (Figure 2B and Table S2a),
with the highest PFS at 36 months in Japan (62.5%) and lowest in
Malaysia (43.3%). This was reflected in the lowest cumulative
36-month RI observed in patients in Japan (31.7%) and the highest in
those from the EMR (52.3%) (Figure 2C and Table S2b). The highest
36-months NRM of 5.8% was observed in patients from Japan and the
lowest in patients from the EMR at 2.0% (Figure 2D).
3.4 |Outcome according to risk factors
Univariate analyses were performed using Karnofsky score, sex, MM
subtype, ISS Staging, cytogenetic score, HCT-CI risk score, disease
status, conditioning, graft source, age, and maintenance. All these fac-
tors were significantly associated with OS, while the interval from
diagnosis to transplant, graft source, and tandem AHCT were not.
Notably, the 36-month OS increased from 80% (95% CI 79%–81%) in
2013 to 84% (95% CI 83%–85%) in 2017.
3.5 |Multivariate analysis (MVA)
The MVA OS model (without ISS, cytogenetic risk, and HCT-CI) included
52 568 patients with complete data (Table S3). The most important risk
factors for OS and PFS were relapse at AHCT (HR 5.23 for OS and HR
3.44 for PFS), SD/MR at AHCT (HR 1.99 and 1.84), no maintenance
(HR 1.79 and 1.72), IgA subtype (HR 1.47 and 1.82), Karnofsky score
≤90% (HR 1.33 and 1.10), melphalan 140 mg/m
2
(HR 1.25 and 1.16),
VGPR at AHCT (HR 1.21 and 1.28), light chain MM (1.14 and 1.08), older
age (HR 1.1 and 1.03 per 10 years increase, respectively) as compared
with baseline (CR at AHCT, maintenance, IgG subtype, Karnofsky score
100%, melphalan 200 mg/m
2
and younger age). A more recent calendar
yearofAHCTwasassociatedwithbetterOS,PFS,andRI(TableS3). The
same factors, except for older age at AHCT (HR 0.95), were also associ-
ated with increased RI. Non-CR stage at AHCT (HR 2.5, 2.19, 1.47 for
VGPR, PR, SD/MR, and relapse/progression, respectively), melphalan
dose 140 mg/m
2
instead of 200 mg/m
2
(HR 1.64), Karnofsky score
≤90% (HR 1.40), and older age at AHCT (HR 1.36) were strongly associ-
ated with NRM. The time interval from diagnosis to AHCT was not sig-
nificantlyassociatedwithOS,PFS,riskofrelapse,orNRM.
An additional MVA was performed on a subset of 20 355 patients
for whom data on cytogenetic risk, HCT-CI risk scores, and ISS at
diagnosis were available (Tables 2A and 2B). A higher HCT-CI
(HR 1.30 and 1.15 for high and intermediate) was significantly associ-
ated with worse OS but was not significantly associated with PFS or
an increased risk of relapse. High-risk cytogenetics (HR 2.13) and a
higher ISS (HR 2.13 and 1.51 for ISS III and II, respectively) were asso-
ciated with worse OS, PFS, and RI. The point estimates of other vari-
ables in these analyses were similar to those presented in Table S3.
We then performed a three-month landmark analysis restricting
the two data sets to patients with information on post-AHCT mainte-
nance. The characteristics of the patients with and without
maintenance information were similar, except for the year of HCT.
Lenalidomide maintenance was associated with improved OS, PFS,
GARDERET ET AL.2087
TABLE 1A Characteristics of patients and diseases of global population and by region.
Characteristics
(information
available)
Group Total Europe USA Australia/New Zealand Japan EM region Taiwan Latin America Ottawa, Canada Malaysia China
All patients 61725 37 459 16 217 3164 3122 543 524 339 188 169 72
% or median (range) [IQR]
Age diagnosis
(n=61 663)
Median
years (IQR)
59.9 (17.0–82.7)
[53.6–64.9]
59.6 (17–82.7)
[53.5–64.4]
60.9 (19.7–82.5)
[54.5–66.6]
60.7 (19.7–78.7)
[54.6–65.4]
59 (24–76) [53–64] 52.5 (17.5–81.7)
[46–58.1]
57.7 (27.6–74.3)
[51.9–62.5]
55 (20–73)
[48–60]
61.5 (34.2–72.6)
[56.4–65.8]
54.3 (29.4–68.6)
[48.3–58.9]
58. (34–73)
[50–64]
Gender
(n=61 725)
Male 58.0 58.1 57.3 62.7 55.4 61.3 53.2 57.2 59.6 60.9 52.8
Race (n=28 023) Caucasian 73.1 93.4 79.9 0.2 98.3 87.9
Asian 15.7 3.1 2.1 99.7 100.0 5.3 100.0 100.0
Black 10.7 3.2 17.4 0.1 6.1
Am. Indian/Alaska 0.1 0.1 0.2 1.7 0.8
Hawaiian/Other PI 0.3 0.1 0.5
Ethnicity
(n=27 653)
No Hispanic 91.8 91.3 92.1 100 100 100 0.3 100 100 100
Year of diagnosis
(n=61 663)
Median year
(range)
2014
(1976–2017)
2014
(1976–2017)
2015
(2012–2017)
2014
(1990–2017)
2014
(1999–2017)
2014
(1995–2017)
2015
(2006–2017)
2014
(2001–2017)
2015
(2010–2017)
2014
(2000–2017)
2016
(2011–2016)
[IQR)] [2013–2016] [2013–2016] [2013–2016] [2013–2016] [2013–2015] [2013–2015] [2013–2016] [2013–2015] ]2013–2016) [2013–2015] [2013–2016]
MM classification
(n=60 429)
IgG 54.0 52.1 56.2 61.6 56.7 46.0 51.4 61.7 59.6 73.6 52.4
Light chain 24.4 27.2 20.7 16.5 19.3 37.8 21.3 16.4 14.4 4.3 17.5
IgA 18.6 17.6 20.8 18.6 19.4 13.1 23.0 16.4 23.9 20.2 25.4
Nonsecretory 1.7 1.9 11.2 1.9 1.6 1.1 0.4 3.0 1.1
Other Ig 1.3 1.1 1.1 1.4 3.0 1.9 3.9 2.4 1.1 1.8 3.2
ISS (n=33 640) I 38.0 38.8 38.9 38.8 35.7 25.3 25.7 30.5 20.6 15.7 27.9
II 34.8 34.0 34.6 37.5 38.7 36.0 36.4 24.1 47.5 41.3 41.2
III 27.1 27.2 26.6 23.7 25.7 38.7 37.9 45.4 31.9 43.0 30.9
Cytogenetic risk
(n=27 468)
High 30.3 31.3 34.8 9.9 5.2 11.8 22.3 61.9 27.4 41.4
Interval Dg—HCT
(n=61 663)
Months 7.1
(0–476)
[5.5–9.9]
7.4
(0–476)
[5.6–10.9]
6.4
(0–12)
[5.2–8.2]
6.9
(0–294)
[5.5–9.9]
7.8
(0–173)
[5.9–11.3]
8.6
(2.8–254)
[6.3–13.2]
7.7
(1.8–101)
[5.9–10.5]
13
(3–170)
[8–20]
6.4
(3–35)
[5.6–8.2]
10.8
(5–178)
[8.3–15.9]
n.a.
Abbreviations: ANZTCT, Australia and New Zealand Transplant & Cellular Therapies Registry; BM, bone marrow; BM, bone marrow; CI, confidence interval; CR, complete response; EM, Eastern Mediterranean region; HCT, hematopoietic cell
transplant; HCT-CI, hematopoietic cell transplant comorbidity index; HR, hazard ratio; IMID, immunomodulatory drug; IQR, inter quartile range; ISS, International staging scoring; NRM, non-relapse mortality; OS, overall survival; PB, peripheral
blood; PFS, progression-free survival; PI, proteasome inhibitor; PR, partial response; R/R, relapse/refractory; RI, relapse incidence; VGPR, very good partial response.
European data were provided by EBMT and included also patients from South Africa (n=142), Colombia (n=12), Singapore (n=48), Iraq (n=1), Iran (n=114), India (n=3), and Brazil (n=7).
2088 GARDERET ET AL.
TABLE 1B AHCT characteristics of the global population and according to region.
Characteristics (information
available)
Group Total Europe USA
Australia/
New Zealand Japan EM region Taiwan Latin America Ottawa, Canada Malaysia China
All patients 61 725 37 459 16 217 3164 3122 543 524 339 188 169 72
Transplant Rate
(HCT/10 million population) 138.6 213.7 226.9 53.3 5.9 31.3 22.8 37.2 17.4 3.6
% or median (range) [IQR]
Year of HCT (n=61 725) 2013/14/15 18.3/19.0/19.9 19/20/20 17/18/19 19/18/20 18/20.5/19.5 24/20/17 17/17/21 11/16/17 15/18/21 16/21/22 18/8/8
2016/17 21.0/21.9 20/21 22/23 22/21 20/21 16/23 23/23 24/32 27/19 18/22 21/44
Age at HCT (n=61 725) Years 60.8 (18.1–83.2)
[55–66]
60.7 (18.1–82.8)
(54–65)
61.5 (20–83)
(55–67)
61.6 (22.1–79.5)
[55–66]
60 (25–77)
[54–64]
53.6 (19–83)
[47–59]
58.5 (28–75.7)
[52–63]
56 (30.5–69)
[50–61]
62 (36.5–73)
[57–66]
56 (30.5–69)
[49–60]
59(34–74)
[51–65]
<60/60–65/66–70 46/30/19 47/31/19 43/26.5/20 42/31/22 46/36/17 79/16/4 58/30/10.5 67/23/9 36/35/26 73/20/8 54/28/17
>70 5.1 3.5 9.8 4.6 1.4 0.6 1.9 1.5 3.7 1
HCT-CI risk (n=44 319) Low (0) 51.8 65.2 26.8 77.3 53.0 62.9 71.3 52.8 3.8
Intermediate (1–2) 25.0 21.6 31.1 16.9 31.7 28.3 23.2 28.9 63.8
High (≥3) 23.2 13.1 42.2 5.8 15.3 8.7 5.5 18.3 32.4
Karnofsky at HCT (n=55 799) ≤90 72.2 66.9 88.1 78.2 52.5 57.9 50.6 44.3 92.4 82.6
Disease at HCT (n=60 367) CR 19.1 20.5 15.8 12.8 19.0 37.3 29.5 40.0 16.3 26.8 40.3
VGPR 38.0 39.1 39.4 26.1 31.6 26.7 41.2 35.8 4.3 27.4 29.0
PR 36.2 34.2 38.1 49.0 42.8 29.6 24.0 21.8 36.5 40.9 21.0
SD/MR 4.7 3.4 6.7 10.1 4.0 4.3 1.8 1.5 12.9 6.5
R/R 1.8 2.4 0.0 2.0 2.2 2.1 3.5 0.9 4.9 3.2
Untreated 0.2 0.3 0.1 0.4
Graft source (n=61 725) PB/BM/PB +BM 99.8/0.1/0.0 99.7/0.2/0.1 100/0/0 99.9/0.1/0 99.9/0.0/0 99.6/0.2/0.2 99.8/0.2/0 100.0/0.0/0 100/0.0/0 100.0/0.0/0 100/0/0
Non cryopreserved (n=9567) 0.7 1.2 0.0 0.0 0.0 13.6 0.0 0.0 0.0
Conditioning (n=61 355) Mel200 70.1 62.2 81.8 88.5 81.7 71.0 77.8 83.7 88.6 60.4 90.3
Mel140 12.0 9.8 18.2 10.2 8.4 4.6 20.7 7.7 5.9 29.0 9.7
Unknown dosage/ others 14.8/3.1 23.5/4.5 0.1/1.2 8.0/1.8 11.3/13.1 0.6/1.0 0.0/8.6 1.1/4.3 0.0/10.7
Tandem (n=61 663) Yes 6.7 10.1 1.3 1.1 3.7 1.5 0.6 0.6 0.0 1.2 100.0
Maintenance (n=6789) Lenalidomide 50.8 58.4 57.9 46.2 61.7 1.2 24.7 44.6 4.2 15.7
None 11.0 20.9 36.9 17.0 55.4 67.3 24.3
Other(s) 10.6 19.2 2.9 1.9 10.0 0.2 1.1
Thalidomide 9.4 9.9 0.2 15.0 30.5 38.7 21.4 44.3
Bortezomib 9.3 11.5 8.6 3.8 13.3 15.9 6.0 2.9
IMiD/PI 7.9 0.1 7.9 11.2 67.7 2.6 1.2
Carfilzomib 1.0 0.9 1.6 0.4
Abbreviations: ANZTCT, Australia and New Zealand Transplant & Cellular Therapies Registry; BM, bone marrow; BM, bone marrow; CI, confidence interval; CR, complete response; EM, Eastern Mediterranean region; HCT, hematopoietic cell
transplant; HCT-CI, hematopoietic cell transplant comorbidity index; HR, hazard ratio; IMID, immunomodulatory drug; IQR, inter quartile range; ISS, International staging scoring; NRM, non-relapse mortality; OS, overall survival; PB, peripheral
blood; PFS, progression-free survival; PI, proteasome inhibitor; PR, partial response; R/R, relapse/refractory; RI, relapse incidence; VGPR, very good partial response.
European data were provided by EBMT and included also patients from South Africa (n=142), Colombia (n=12), Singapore (n=48), Iraq (n=1), Iran (n=114), India (n=3) and Brazil (n=7).
GARDERET ET AL.2089
and lower RI, but not NRM (Figure S1). No treatment or treatment
other than lenalidomide maintenance was associated with lower OS
(HR 2.09 and 1.36), PFS (HR 1.61 and 1.39), and higher RI (HR 2.09
and 1.36) (Tables 2A,2B, and S3).
3.6 |Transplant activity and outcomes by
macroeconomic factors
Country HRs extracted from the model and country-specific health
economic variables were correlated. TR correlated strongly with HCE,
with higher AHCT activity in countries with higher HCE (r=0.67,
p< .01; Figure S2a). Furthermore, a lower risk of death after AHCT
was observed in countries with higher HCE (r=0.49, p< .01;
Figure S2b) and in countries with higher HCE/GNI (r=0.45,
p< .01; Figure S2c). Similarly, the risks of death or relapse (r=0.39,
p< .01; Figure S2d) and relapse (r=0.37, p< .01; Figure S2e) were
lower in countries with higher HCE/GNI quotients. In contrast, only a
trend was found between the HR for death without relapse and
HCE/GNI (r=0.26, p=.06; Figure S2f).
4|DISCUSSION
Information on the outcomes of patients with MM undergoing
upfront AHCT between 2013 and 2017 (inclusive) was collected from
different regions worldwide. The median OS was 90.2 months and
the median PFS 36.5 months. The cumulative RI was 15.7% at
12 months, and the NRM was 1.5% at 12 months and 3.4%
at 36 months. This confirms the safety of AHCT worldwide, indepen-
dent of the country's income. Notably, these were real-world data and
were not derived from clinical trials with defined eligibility criteria.
In MVA, older age was associated with inferior OS, primarily due to a
higher NRM. Females tended to have a slightly better OS than males as
reported previously for other hematological diseases and solid
tumors.
18–21
In recent years, outcomes have improved, most likely due to
the availability of numerous novel therapies, such as immunomodulatory
drugs (IMiDs), proteasome inhibitors, and CD38 monoclonal antibodies.
22
Interestingly, the stage of disease at AHCT was the most important prog-
nostic factor. The risk of death was higher with more advanced disease at
AHCT, underscoring the importance of utilizing a highly effective induc-
tion regimen at the outset to achieve the best response to AHCT. Achiev-
ing at least a complete remission (CR), and currently a minimal residual
disease (MRD) negative status, has a clear positive impact on posttrans-
plant outcomes.
23
With respect to the immunoglobulin subtype, our anal-
ysis confirms the detrimental outcomes seen with IgA compared with IgG
paraproteins and, to a lesser extent, light chain myeloma compared with
IgG subtype, as has also been previously reported.
24,25
The association between lower Karnofsky scores and poorer
outcomes was stronger for NRM and OS and weaker for RI. Higher
HCT-CI was only associated with worse NRM and OS, whereas poor
cytogenetic risk was associated with increased RI but had no impact
FIGURE 1 Outcome after auto-HCT: (A) probability of overall survival (OS), (B) progression-free survival (PFS), (C) cumulative relapse
incidence (RI), and (D) cumulative incidence of non-relapse mortality (NRM). Due to the large number of patients, the 95% confidence intervals
(CIs) are very narrow and cannot be distinguished from the point estimates. Numbers below the graphs show the number of patients at risk.
[Color figure can be viewed at wileyonlinelibrary.com]
2090 GARDERET ET AL.
on NRM. There was a strong association between the ISS stage and
all outcomes.
The observation that patients conditioned with a melphalan dose
of 140 mg/m
2
had poorer outcomes than those receiving 200 mg/m
2
was at odds with published data. Although we also found that the dif-
ferences in the risk of adverse outcomes between lower and standard
melphalan doses were substantially smaller in models adjusted for
cytogenic risk, ISS at diagnosis, and number of comorbidities, a signifi-
cantly higher risk of NRM remained in those who had received a
lower melphalan dose. This finding may be due to selection bias, as
patients receiving a lower dose of melphalan were older, had lower
Karnofsky scores, and had more comorbidities. Despite adjusting for
these factors, confounding by other factors that were not tested here
may be possible. For example, we could not adjust for differences in
renal function as the data were not readily available. In a previous
study, outcomes were similar following melphalan 140 mg/m
2
and
melphalan 200 mg/m
2
, with remission status at the time of transplan-
tation being the overriding determinant, that is, AHCT in less than PR
favored melphalan 200 mg/m
2
over 140 mg/m
2
in terms of OS, PFS,
and relapse risk.
26
AHCT outcomes were significantly associated with macroeco-
nomic factors. In general, a higher HCE/GNI ratio was associated with
a lower risk of death and disease recurrence but not NRM. Unsurpris-
ingly, this finding suggests that investment in healthcare services
affects the outcomes. Further healthcare services and health econom-
ics research are required to elucidate the causes of this association,
which may be due to a lack of access to maintenance therapy.
Our study has some important limitations. Reporting practices,
data collection systems, and quality checks differ between registries,
resulting in varying amounts of missing information. Despite a gener-
ally low NRM, significant differences in survival and relapse outcomes
between registries were observed in univariate analyses. Different
factors, including variations in the baseline characteristics, may be
responsible for this effect. For example, lower-income regions tend to
transplant younger patients and select patients who achieve a good
hematological response, while in other registries, a higher percentage
FIGURE 2 Outcome after auto-HCT by registry/region: (A) probability of overall survival (OS), (B) progression-free survival (PFS),
(C) cumulative relapse incidence (RI), and (D) cumulative incidence of non-relapse mortality (NRM). Numbers below the graphs show the number
of patients at risk. [Color figure can be viewed at wileyonlinelibrary.com]
GARDERET ET AL.2091
of older patients (>70 years) were transplanted, and tandem HCT was
used routinely. The percentage of patients with high HCT-CI scores
also differed between regions, with the highest percentage among
patients from the USA and Malaysia and a lower percentage of high-
risk patients in Japan and Latin America. Importantly, there were limi-
tations in data collection for post-HCT consolidation and maintenance
TABLE 2A Multivariable analysis on outcome of patients according to characteristics at diagnosis.
Clinical characteristics
OS
p
PFS
p
Relapse
p
NRM
pHR (95% CI) HR (95% CI) HR (95% CI) HR (95% CI)
Gender Male 1.00 1.00 1.00 1.00
Female 0.93 (0.87–1.01) .08 0.94 (0.90–0.98) .005 0.94 (0.90–0.99) .01 0.94 (0.80–1.10) .45
MM classification IgG 1.00 1.00 1.00 1.00
IgA 1.42 (1.30–1.56) <.0001 1.26 (1.19–1.34) <.0001 1.24 (1.17–1.31) <.0001 1.56 (1.28–1.90) <.0001
Light chain 1.10 (1.00–1.22) .06 1.12 (1.05–1.19) .0004 1.12 (1.05–1.19) .0003 1.04 (0.84–1.31) .61
Cytogenetic risk Standard 1.00 1.00 1.00 1.00
High 2.13 (1.96–2.30) <.0001 1.62 (1.55–1.70) <.0001 1.65 (1.57–1.73) <.0001 1.32 (1.11–1.58) .002
ISS at diagnosis I 1.00 1.00 1.00 1.00
II 1.51 (1.37–1.67) <.0001 1.23 (1.16–1.30) <.0001 1.22 (1.15–1.29) <.0001 1.46 (1.19–1.79) .0003
III 2.16 (1.96–2.39) <.0001 1.49 (1.41–1.58) <.0001 1.46 (1.38–1.55) <.0001 2.02 (1.64–2.49) <.0001
Interval
diagnosis-HCT
(per 6 months more) 1.02 (0.99–1.04) .14 1.00 (0.99–1.01) .99 1.00 (0.98–1.01) .54 1.04 (1.00–1.08) .04
Note: The OS model included 20 355, the PFS, relapse and NRM 19873 patients. HR > 1 is associated with an increased risk for the endpoint.
Abbreviations: CI, confidence interval; CR, complete response; HR, hazard ratio; MM, multiple myeloma; MR, minor response; NRM, non-relapse mortality;
OS, overall survival; PFS, progression-free survival; PR, partial response; SD, stable disease; VGPR, very good partial response.
The association of lenalidomide was investigated in a separate landmark model including only patients without event at 3 months and with data on
maintenance therapy available (n=2904 for OS and 2753 for PFS and relapse) but including the variables listed in this table and a random country effect.
TABLE 2B Multivariable analysis on outcome of patients according to characteristics at HCT.
Clinical characteristics
OS
p
PFS
p
Relapse
p
NRM
pHR (95% CI) HR (95% CI) HR (95% CI) HR (95% CI)
Age at HCT (per 10 year increase) 1.07 (1.02–1.12) .005 0.98 (0.96–1.01) .23 0.96 (0.94–0.99) .01 1.29 (1.16–1.44) .0004
Year of HCT (per year later) 0.92 (0.89–0.95) <.0001 0.92 (0.90–0.93) <.0001 0.91 (0.90–0.93) <.0001 0.95 (0.89–1.01) .12
Karnofsky
score at HCT
100 1.00 1.00 1.00 1.00
≤90 1.29 (1.17–1.44) <.0001 1.10 (1.05–1.15) <.0001 1.08 (1.01–1.15) .02 1.31 (1.04–1.64) .02
HCT-CI risk score Low (0) 1.00 1.00 1.00 1.00
Intermediate (1–2) 1.15 (1.04–1.27) .006 1.01 (0.96–1.08) .65 0.99 (0.93–1.05) .69 1.44 (1.15–1.80) .001
High (≥3) 1.30 (1.17–1.45) <.0001 1.05 (0.98–1.12) .15 1.00 (0.94–1.07) .93 1.92 (1.52–2.43) <.0001
Disease stage at HCT CR 1.00 1.00 1.00 1.00
VGPR 1.17 (1.04–1.32) .01 1.25 (1.16–1.34) <.0001 1.26 (1.17–1.36) <.0001 1.09 (0.84–1.40) .53
PR 1.44 (1.28–1.63) <.0001 1.55 (1.44–1.67) <.0001 1.54 (1.43–1.67) <.0001 1.58 (1.22–2.03) .0004
SD/MR 2.20 (1.84–2.62) <.0001 1.88 (1.68–2.11) <.0001 1.81 (1.61–2.04) <.0001 2.52 (1.77–3.59) <.0001
Relapse/progression 5.55 (4.36–7.06) <.0001 3.07 (2.52–3.73) <.0001 2.98 (2.42–3.67) <.0001 3.83 (2.06–7.12) <.0001
Conditioning Melphalan 200 1.00 1.00 1.00 1.00
Melphalan 140 1.07 (0.96–1.19) .21 1.09 (1.02–1.16) .01 1.06 (0.99–1.14) .09 1.36 (1.11–1.67) .003
Maintenance
a
Lenalidomide 1.00 1.00 1.00
Other 1.36 (1.04–1.78) .03 1.39 (1.20–1.60) <.0001 1.36 (1.04–1.78) .03
None 2.09 (1.53–2.87) <.0001 1.61 (1.33–1.96) <.0001 2.09 (1.53–2.87) <.0001
Note: The OS model included 20 355, the PFS, relapse and NRM 19873 patients. HR > 1 is associated with an increased risk for the endpoint.
Abbreviations: CI, confidence interval; CR, complete response; HR, hazard ratio; MM, multiple myeloma; MR, minor response; NRM, non-relapse mortality;
OS, overall survival; PFS, progression-free survival; PR, partial response; SD, stable disease; VGPR, very good partial response.
a
The association of lenalidomide was investigated in a separate landmark model including only patients without event at 3 months and with data on
maintenance therapy available (n=2904 for OS and 2753 for PFS and relapse) but including the variables listed in this table and a random country effect.
2092 GARDERET ET AL.
treatment. Maintenance therapy has been shown in prior studies to
improve PFS and OS.
27
With the caveat that the data being limited,
our analysis showed that patients with post-AHCT lenalidomide main-
tenance had a lower risk of relapse with improved OS and PFS. Access
to lenalidomide varies globally, which may partially explain the differ-
ent outcomes observed in Malaysia. We have tried to address the
important issue of drug access, but we found it more difficult than
expected. First, within the same region, country approval date varies
considerably. Second, there may be an important gap between
approval of a drug and its reimbursement. It depends very much on
the type of medical coverage whether it is state driven (“social secu-
rity system”) or through private insurance. Sometimes, within the
same country, both types of reimbursement exist, and in the end, it is
difficult to capture for a single patient whether or not the patient
actually has access to these new expensive myeloma drugs. Despite
these limitations, this study provides important insights into the use
of AHCT in NDMM and has generated useful data on its safety and
efficacy at the global level.
In conclusion, this exceptionally large study provides a high-level
overview of AHCT. Despite the reassuringly low early NRM rate, differ-
ences in patient selection, transplant procedures, and outcomes across
geographic regions have been identified. To our knowledge, this is the
first time that real-world outcome data encompassing almost 60% of
the world's transplant activity have been reported in the field of
MM. Patients with MM who underwent AHCT outside of clinical trials
between 2013 and 2017 had a RI of 15.7% in the first year, a median
PFS of 3 years, and a median OS of 7 years, and the treatment has been
increasingly utilized.
28
However, the regional differences in relapse and
survival outcomes warrant further investigation. Our new transplant
registry collaboration provides a framework for evaluating and improv-
ing MM outcomes globally. In addition, the experience gained also
paves the way for future analyses of novel non-transplant therapies and
assessment of relative global access, utilization, and outcomes.
AUTHOR CONTRIBUTIONS
LGa, LGr, MA, YA, and DN designed the study; LK, LB, AD, NEM, PH,
WS, AC, MI, SO, HT, SM, KK, YK, NH, BSK, CL, KWH, ASG, SKT,
AME, AB, QNC, RA, MAB, MB, CAFO, ER, SG, FB, HM, AMcC, FRW,
LM, MK, JS, SS, DMcL, PH, AS, and HG enrolled patients; LGa, LGr,
DNe, NH, MA, YA, and DN analyzed the data; LGa, LGr, DNe, NH,
MA, YA, and DN wrote the manuscript.
AFFILIATIONS
1
Service d'Hématologie, Sorbonne Université, Hopital Pitié Salpêtière
APHP, Paris, France
2
EBMT Statistical Unit, Leiden, Netherlands
3
EBMT Data Office, Leiden, Netherlands
4
Department of Haematology, School of Medicine, St Vincent's
Hospital Sydney, St Vincent's Clinical School, University of New
South Wales, University of Notre Dame Australia, Sydney, New South
Wales, Australia
5
Department of Medicine, Medical College of Wisconsin, Milwaukee,
Wisconsin, USA
6
CIBMTR
®
(Center for International Blood and Marrow Transplant
Research), Department of Medicine, Medical College of Wisconsin,
Milwaukee, Wisconsin, USA
7
Department of Hematology, Medical College of Wisconsin,
Milwaukee, Wisconsin, USA
8
Clinical Research Division, Fred Hutchinson Cancer Center, Seattle,
Washington, USA
9
School of Medicine, Aichi Medical University, Aichi, Japan
10
School of Medicine, Keio University, Tokyo, Japan
11
School of Entrepreneurial and Innovation Studies, Kanazawa
University, Kanazawa, Japan
12
Department of Hematology, School of Medicine, Aichi Medical
University, Nagakute, Japan
13
Division of Hematology, Jichi Medical University Saitama Medical
Center, Saitama, Japan
14
Department of Promotion for Blood and Marrow Transplantation,
School of Medicine, Aichi Medical University, Nagoya, Japan
15
Department of Hematology, National Taiwan University Hospital,
Taipei, Taiwan
16
Department of Hematology, Hospital Ampang, Ampang, Malaysia
17
Department of Hematology, Ampang Hospital, Ampang Jaya,
Malaysia
18
Penang General hospital, Penang, Malaysia
19
Department of Pediatric Oncology and Stem Cell Transplantation
Unit, National Cancer Institute, Cairo University, Cairo, Egypt
20
Bone Marrow Transplantation Program, Department of Internal
Medicine, American University of Beirut Medical Center, Beirut,
Lebanon
21
AFBMTC/NIBMT, Rawalpindi, Pakistan
22
King Hussein Cancer center, Amman, Jordan
23
Department of Hematology and Cell Therapy, EHU 1st Novembre
1954 Bir el Djir Usto, University Ahmed Benbella 1, Oran, Algeria
24
Centre Pierre et Marie Curie (CPMC), Algiers, Algeria
25
Hospital Central Del Instituto De Prevision Social, Asuncion,
Paraguay
26
Facultad de Medicina, Cátedra de Hematología, Hospital de Clínicas,
Montevideo, Uruguay
27
Hematology Department, British Hospital, Montevideo, Uruguay
28
Hospital del Salvador, Santiago, Chile
29
Department of Oncology, McMaster University, Hamilton, Canada
30
Department of Medicine, Division of Hematology, The Ottawa
Hospital, Ottawa, Canada
31
Department of Hematology, Peking University, Beijing, China
32
IMISE, University of Leipzig, Leipzig, Germany
33
Infection and Immunity Clinical Academic Group St George's,
University of London, London, UK
34
BSBMTCT, Department of Haematology, Sheffield Teaching
Hospitals NHS Trust, Sheffield, UK
35
Department of Internal Medicine V, Amyloidosis Center, Heidelberg
University Hospital, Heidelberg, Germany
36
Department of Haematology, Kings's College Hospital, London, UK
37
Department of Haematology, Trinity College Dublin, St. James's
Hospital, Dublin, Ireland
GARDERET ET AL.2093
38
Institut Català d'Oncologia, Hospital Duran i Reynals, Institut
d'Investigació Biomèdica de Bellvitge (IDIBELL), Universitat de
Barcelona, L'Hospitalet de Llobregat, Spain
39
Division of Hematology, Department of Internal Medicine, Medical
University of Graz, Graz, Austria
40
Oncology Center, King Faisal Specialist Hospital and Research
Center, Riyadh, Saudi Arabia
41
Japanese Data Center for Hematopoietic Cell Transplantation,
Department of Registry Science for Transplant and Cellular Therapy,
School of Medicine, Aichi Medical University, Nagakute, Japan
42
Department of Hematology, University of Leipzig, Leipzig, Germany
ACKNOWLEDGMENTS
We thank the patients and their family.
CONFLICT OF INTEREST STATEMENT
Laurent Garderet declares consulting fees from BMS, Janssen, Sanofi,
and Pfizer. Anita D'Souza reports institutional clinical trial support
from Abbvie, Caelum, Janssen, Novartis, Prothena, Sanofi, TeneoBio;
ad board and consulting fees from BMS/Celgene, Janssen, Kedrion,
Pfizer, and Prothena. John Snowden declares consulting fees from
Medac, Jazz and Vertex. Hira Mian is supported by an early career
award from Hamilton Health Sciences. Ad board and consulting fees:
BMS, Janssen, Sanofi, Amgen, Pfizer, and Takeda. Research funding:
Janssen and Pfizer. Yoshiko Atsuta reports consulting fees from JCR
Pharmaceuticals Co., Ltd. and Kyowa Kirin Co., Ltd.; lecture fees from
Otsuka Pharmaceutical Co., Ltd, Chugai Pharmaceutical Co., Ltd.,
Novartis Pharma KK, AbbVie GK; and honorarium from Meiji Seika
Pharma Co, Ltd. Mickey Koh: received honoraria from Gilead, KiTE
and Takeda. Other investigators have no conflict of interest.
DATA AVAILABILITY STATEMENT
Data can be obtained upon request to the corresponding author.
ORCID
Laurent Garderet https://orcid.org/0000-0002-6138-8112
Hiroyuki Takamatsu https://orcid.org/0000-0001-9515-0017
Shohei Mizuno https://orcid.org/0000-0002-4405-8808
Koji Kawamura https://orcid.org/0009-0009-9976-9787
Bor-Sheng Ko https://orcid.org/0000-0002-7965-7579
Ali Bazarbachi https://orcid.org/0000-0002-7171-4997
Eloisa Riva https://orcid.org/0000-0002-4750-034X
Hira S. Mian https://orcid.org/0000-0003-1584-1067
Ly Meng https://orcid.org/0000-0001-6625-9523
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SUPPORTING INFORMATION
Additional supporting information can be found online in the Support-
ing Information section at the end of this article.
How to cite this article: Garderet L, Gras L, Koster L, et al.
Global characteristics and outcomes of autologous
hematopoietic stem cell transplantation for newly diagnosed
multiple myeloma: A study of the worldwide network for
blood and marrow transplantation (WBMT). Am J Hematol.
2024;99(11):2084‐2095. doi:10.1002/ajh.27451
GARDERET ET AL.2095