Hodgkin Lymphoma EBR
The Role of Cytotoxic Therapy with Hematopoietic Stem Cell Transplantation in the Treatment of Hodgkin
Lymphoma: An Evidence-Based Review
1. Proposed Table of Contents
I.
II.
III.
IV.
V.
VI.
VII.
VIII.
IX.
X.
Abstract
Introduction
Treatment Recommendations
Autologous SCT versus Nontransplantation Therapy
a. Autologous SCT versus Nontransplantation as first line therapy for advanced disease.
i. Autologous SCT as first line therapy for advanced disease.
b. Autologous SCT versus Nontransplantation for Patients in Partial Remission
i. Autologous SCT as first line therapy for Patients in Partial Remission
c. Autologous SCT versus Nontransplantation as Salvage Therapy
i. Chemotherapy
ii. Radiation
Autologous SCT for selected populations
a. Autologous SCT for Patients ≥ 60 Years of Age (Plan to remove this topic)
b. Autologous SCT for patients < 18 (21) years of Age
Autologous SCT
a. Comparative Studies of Autologous SCT
i. Choice of induction therapy prior to first-line autologous SCT
b. Noncomparative Studies of Autologous SCT
i. Salvage regimens prior to autologous SCT
ii. Conditioning regimens prior to autologus SCT
iii. Tandem autologous SCT
iv. Choice of stem cell mobilization and use of growth factors
c. Role of radiation, including IFRT
Allogeneic SCT
a. Regimen Intensity
b. Stem cell source
c. Donor leukocyte infusion
d. Allogeneic SCT vs. non-transplantation therapy
e. Tandem auto-allo SCT
f. Allogeneic SCT for selected populations
Autologous versus Allogeneic SCT
a. Allogeneic SCT as first line therapy
b. Salvage after failed autologous SCT
i. Second autologous SCT
ii. Allogeneic SCT
c. Front-line autologous versus allogeneic SCT
Prognostic factors
a. Clinical factors
i. At relapse
ii. At time of SCT
b. Role of Functional Imaging
c. Other factors
d. Impact of co-morbidities on outcomes
i. Autologous SCT
ii. Allogeneic SCT
Survivorship
a. Long-term toxicity
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Hodgkin Lymphoma EBR
XI.
i. Autologous SCT
ii. Allogeneic SCT
b. Guidelines for follow-up
i. Autologous SCT
ii. Allogeneic SCT
Areas of Needed Research and Ongoing Studies
a. Maintenance therapy
i. Maintenance post autologous SCT
1. Phase III Brentixumab
2. Phase III Parabinostat (study closed)
ii. Maintenance post allogeneic SCT
b. Salvage after failed SCT
c. Novel Therapies
i. Brentixumab Vedotin (pre, post SCT)
ii. Other novel agents (Bendamustine, Lenalinomide, Temsirolimus, etc)
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Hodgkin Lymphoma EBR
1. Search Methodology
Adapted from the search methodology used for the DLBCL EBR update published in BBMT in 2011, with the
following modification: Papers that included fewer than 20 HL (rather than 25 as for DLBCL) cases were
excluded because of the lower incidence of the disease. PubMed was searched, using the search terms “Hodgkin
Lymphoma” AND “transplant” limited to “human trials,” “English language,” and a publication date of January
1, 2001, or later. Papers that were published before January 2001, included fewer than 20 HL patients, or were not
peer reviewed were excluded. Also excluded were editorials, letters to the editor, Phase I (dose escalation or dose
finding) studies, reviews, consensus conference papers, practice guidelines, and laboratory studies with no clinical
correlates.
Search terms:
("hodgkin disease"[MeSH Terms] OR ("hodgkin"[All Fields] AND "disease"[All Fields]) OR "hodgkin disease"[All
Fields] OR ("hodgkin"[All Fields] AND "lymphoma"[All Fields]) OR "hodgkin lymphoma"[All Fields]) AND
("transplants"[MeSH Terms] OR "transplants"[All Fields] OR "transplant"[All Fields] OR "transplantation"[MeSH
Terms] OR "transplantation"[All Fields]) AND (("2001/01/01"[PDAT] : "3000/12/31"[PDAT]) AND
"humans"[MeSH Terms] AND English[lang])
Notes:
a. A slightly “wider net” was cast in the selection of articles to include references that also focus on toxicity and
survivorship. The list will likely need to be trimmed during a more detailed review.
b. In addition to the online database searches, a manual search of the reference lists of the included articles and
relevant reviews published since 2000 will be conducted.
c. A search of clinicaltrials.gov was also performed to identify current studies
2. Search results
Articles in search results: 2004
Articles selected for initial review: 188
Articles selected for EBR: 166 (4 artciles on SGN-35 added)
April 2013 Update (repeated the same search for 01/01/12 – 12/31/12)
Articles in search results: 172
Articles selected for initial review: 23
Articles selected for EBR: 14 additional articles
Total articles: 180
3. Grading Methodology
The ASBMT Steering Committee for EBR recommends using a standardized grading system (Harbour R, Miller
J. A new system for grading recommendations in evidence-based guidelines. Br Med J.2001;323:334-336.). This
includes grading the levels of evidence. The treatment recommendations of the expert panel also are subject to a
standardized grading system.
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Hodgkin Lymphoma EBR
Levels of Evidence
1++ High-quality meta-analyses, systematic reviews of randomized controlled trials (RCTs), or RCTs
with a very low risk of bias
1+
Well-conducted meta-analyses, systematic reviews of RCTs, or RCTs with a low risk of bias Metaanalyses, systematic reviews of RCTs, or RCTs with a high risk of bias
1–
High-quality systematic reviews of case-control or cohort studies.
2++ High quality case-control or cohort studies with a very low risk of confounding, bias, or chance, and
a high probability that the relationship is causal
2+
Well-conducted case-control or cohort studies with a low risk of confounding, bias, or chance, and a
moderate probability that the relationship is causal
2 – Case-control or cohort studies with a high risk of confounding, bias, or chance, and a significant
risk that the relationship is not causal
3
Nonanalytic studies (eg, case reports, case series)
4
Expert opinion
Grades Of Recommendation
A At least 1 meta-analysis, systematic review, or RCT rated as 1++ and directly applicable to the target
population or a systematic review of RCTs or a body of evidence consisting principally of studies
rated as 1+, directly applicable to the target population, and demonstrating overall consistency of
results.
B A body of evidence including studies rated as 2++, directly applicable to the target population, and
demonstrating overall consistency of results or extrapolated evidence from studies rated as 1++ or 1+.
C A body of evidence including studies rated as 2+, directly applicable to the target population, and
demonstrating overall consistency of results or extrapolated evidence from studies rated as 2++.
D Evidence level 3 or 4 or extrapolated evidence from studies rated as 2+.
Note: an alternative system has been used in other studies: Grading system for ranking recommendations in clinical
guidelines (Kish MA. Guide to Development of Practice Guidelines. Clin Infectious Disease. 2001; 32: 851-4):
Strength of Recommendations
A
Good evidence to support a recommendation for use
B
Moderate evidence to support a recommendation for use
C
Poor evidence to support a recommendation
D
Moderate evidence to support a recommendation against use
E
Good evidence to support a recommendation against use
Quality of Evidence
Type I
Evidence from ≥ 1 properly randomized, controlled trial
Type II
Evidence from ≥ 1 well-designed clinical trial, without randomization; from cohort or casecontrolled analytic studies (preferably from > 1 center); from multiple time-series; or from
dramatic results from uncontrolled experiments
Type III
Evidence from opinions of respected authorities, based on clinical experience, descriptive studies,
or reports of expert committees
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4. Expert Panel
Philippe Armand, DFCI
Linda Burns, UMN
Izaskun Ceberio, University of Navarra (Pamplona, Spain)/MSKCC
Robert Chen, COH
Andrew Evens, U Mass
Ginna Laport, Stanford
David Maloney, FHCRC
Craig Moskowitz, MSKCC
Miguel Perales, MSKCC
Uday Popat, MDACC
Nishita Reddy, Vanderbilt
Thomas Shea, UNC
Cindy Schwartz, Brown
Julie Vose, UNMC
5. Proposed Assignments
Section
IV
V
VI
VII
VIII
IX
X
XI
Topic
Table Reviewer Reviewer Reviewer
ASCT vs no SCT
1
Evens
Reddy
Armand
Peds
3
Schwartz
Popat
ASCT
2
Evens
Moskowitz
Vose
Allo
4
Burns
Maloney
Perales
ASCT vs. Allo
5
Armand
Shea
Perales
Prognostic Factors
6
Reddy
Vose
Laport
Survivorship
7
Burns
Shea
Research
8
Chen
Shea
Laport
Coordination/Writing: Perales/Ceberio
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Hodgkin Lymphoma EBR
Detailed Table of Contents (including references)
I.
Abstract
II.
Introduction
III.
Treatment Recommendations
IV.
Autologous SCT versus Non-transplantation Therapy
a. Autologous SCT versus Non-transplantation as first line therapy for advanced disease.
60: Carella AM, Bellei M, Brice P, Gisselbrecht C, Visani G, Colombat P, Fabbiano F, Donelli A, Luminari S, Feugier P,
Browett P, Hagberg H, Federico M. High-dose therapy and autologous stem cell transplantation versus conventional
therapy for patients with advanced Hodgkin's lymphoma responding to front-line therapy: long-term results.
Haematologica. 2009 Jan;94(1):146-8. Epub 2008 Nov 10. PubMed PMID: 19001284; PubMed Central PMCID:
PMC2625418.
61: Arakelyan N, Berthou C, Desablens B, de Guibert S, Delwail V, Moles MP, Quittet P, Jais JP, Colonna P, Andrieu
JM; Groupe Ouest-Est d'Etude des Leucémies et Autres Maladies du Sang. Early versus late intensification for patients
with high-risk Hodgkin lymphoma-3 cycles of intensive chemotherapy plus low-dose lymph node radiation therapy versus
4 cycles of combined doxorubicin, bleomycin, vinblastine, and dacarbazine plus myeloablative chemotherapy with
autologous stem cell transplantation: five-year results of a randomized trial on behalf of the GOELAMS Group. Cancer.
2008 Dec 15;113(12):3323-30. PubMed PMID: 18988286.
148: Federico M, Bellei M, Brice P, Brugiatelli M, Nagler A, Gisselbrecht C, Moretti L, Colombat P, Luminari S,
Fabbiano F, Di Renzo N, Goldstone A, Carella AM; EBMT/GISL/ANZLG/SFGM/GELA Intergroup HD01 Trial. Highdose therapy and autologous stem-cell transplantation versus conventional therapy for patients with advanced Hodgkin's
lymphoma responding to front-line therapy. J Clin Oncol. 2003 Jun 15;21(12):2320-5. PubMed PMID: 12805333.
165: Vigouroux S, Milpied N, Andrieu JM, Colonna P, Ifrah N, Colombat P, Desablens B, Abgrall JF, Casassus P,
Guilhot F, Briere J, Le Mevel A, Moreau P, Mechinaud F, Mahe B, Morineau N, Vigier M, Rapp MJ, Harousseau JL.
Front-line high-dose therapy with autologous stem cell transplantation for high risk Hodgkin's disease: comparison with
combined-modality therapy. Bone Marrow Transplant. 2002 May;29(10):833-42. PubMed PMID: 12058233.
168: Proctor SJ, Mackie M, Dawson A, White J, Prescott RJ, Lucraft HL, Angus B, Jackson GH, Lennard AL,
Hepplestone A, Taylor PR. A population-based study of intensive multi-agent chemotherapy with or without
autotransplant for the highest risk Hodgkin's disease patients identified by the Scotland and Newcastle Lymphoma Group
(SNLG) prognostic index. A Scotland and Newcastle Lymphoma Group study (SNLG HD III). Eur J Cancer. 2002
Apr;38(6):795-806. PubMed PMID: 11937314.
i. Autologous SCT as first line therapy for advanced disease.
8: Viviani S, Zinzani PL, Rambaldi A, Brusamolino E, Levis A, Bonfante V, Vitolo U, Pulsoni A, Liberati AM, Specchia
G, Valagussa P, Rossi A, Zaja F, Pogliani EM, Pregno P, Gotti M, Gallamini A, Rota Scalabrini D, Bonadonna G, Gianni
AM; Michelangelo Foundation; Gruppo Italiano di Terapie Innovative nei Linfomi; Intergruppo Italiano Linfomi. ABVD
versus BEACOPP for Hodgkin's lymphoma when high-dose salvage is planned. N Engl J Med. 2011 Jul 21;365(3):20312. PubMed PMID: 21774708.
176: Sperotto A, Zaja F, Damiani D, Patriarca F, Fanin R. High-dose therapy and autologous stem cell transplantation for
high-risk Hodgkin's lymphoma: a single center experience. Haematologica. 2001 Dec;86(12):1317-8. PubMed PMID:
11726327.
Updated 04/18/2013
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b. Autologous SCT versus Nontransplantation for Patients in Partial Remission
146: Stiff PJ, Unger JM, Forman SJ, McCall AR, LeBlanc M, Nademanee AP, Bolwell BJ, Fisher RI; Southwest
Oncology Group. The value of augmented preparative regimens combined with an autologous bone marrow transplant for
the management of relapsed or refractory Hodgkin disease: a Southwest Oncology Group phase II trial. Biol Blood
Marrow Transplant. 2003 Aug;9(8):529-39. PubMed PMID: 12931122.
165: Vigouroux S, Milpied N, Andrieu JM, Colonna P, Ifrah N, Colombat P, Desablens B, Abgrall JF, Casassus P,
Guilhot F, Briere J, Le Mevel A, Moreau P, Mechinaud F, Mahe B, Morineau N, Vigier M, Rapp MJ, Harousseau JL.
Front-line high-dose therapy with autologous stem cell transplantation for high risk Hodgkin's disease: comparison with
combined-modality therapy. Bone Marrow Transplant. 2002 May;29(10):833-42. PubMed PMID: 12058233.
171: Fermé C, Mounier N, Diviné M, Brice P, Stamatoullas A, Reman O, Voillat L, Jaubert J, Lederlin P, Colin P, Berger
F, Salles G. Intensive salvage therapy with high-dose chemotherapy for patients with advanced Hodgkin's disease in
relapse or failure after initial chemotherapy: results of the Groupe d'Etudes des Lymphomes de l'Adulte H89 Trial. J Clin
Oncol. 2002 Jan 15;20(2):467-75. PubMed PMID: 11786576.
i. Autologous SCT as first line therapy for Patients in Partial Remission
89: Akhtar S, El Weshi A, Abdelsalam M, Hussaini H, Janabi I, Rahal M, Maghfoor I. Primary refractory Hodgkin's
lymphoma: outcome after high-dose chemotherapy and autologous SCT and impact of various prognostic factors on
overall and event-free survival. A single institution result of 66 patients. Bone Marrow Transplant. 2007 Oct;40(7):651-8.
Epub 2007 Jul 30. PubMed PMID: 17660837.
124: Lavoie JC, Connors JM, Phillips GL, Reece DE, Barnett MJ, Forrest DL, Gascoyne RD, Hogge DE, Nantel SH,
Shepherd JD, Smith CA, Song KW, Sutherland HJ, Toze CL, Voss NJ, Nevill TJ. High-dose chemotherapy and
autologous stem cell transplantation for primary refractory or relapsed Hodgkin lymphoma: long-term outcome in the first
100 patients treated in Vancouver. Blood. 2005 Aug 15;106(4):1473-8. Epub 2005 May 3. PubMed PMID: 15870180.
150: Tarella C, Cuttica A, Vitolo U, Liberati M, Di Nicola M, Cortelazzo S, Rosato R, Rosanelli C, Di Renzo N, Musso
M, Pavone E, Santini G, Pescarollo A, De Crescenzo A, Federico M, Gallamini A, Pregno P, Romano R, Coser P, Gallo
E, Boccadoro M, Barbui T, Pileri A, Gianni AM, Levis A. High-dose sequential chemotherapy and peripheral blood
progenitor cell autografting in patients with refractory and/or recurrent Hodgkin lymphoma: a multicenter study of the
intergruppo Italiano Linfomi showing prolonged disease free survival in patients treated at first recurrence. Cancer. 2003
Jun 1;97(11):2748-59. PubMed PMID:12767087.
158: Holowiecki J, Giebel S, Wojnar J, Krawczyk-Kulis M, Stella-Holowiecka B, Kachel L, Wojciechowska M,
Markiewicz M, Kata D. Autologous hematopoietic stem cell transplantation for high-risk Hodgkin's disease: a singlecenter experience with the first 100 patients. Transplant Proc. 2002 Dec;34(8):3378-83. PubMed PMID: 12493478.
121: Oyan B, Koc Y, Ozdemir E, Kars A, Turker A, Tekuzman G, Kansu E. Ifosfamide, idarubicin, and etoposide in
relapsed/refractory Hodgkin disease or non-Hodgkin lymphoma: a salvage regimen with high response rates before
autologous stem cell transplantation. Biol Blood Marrow Transplant. 2005 Sep;11(9):688-97. PubMed PMID: 16125639.
140: Popat U, Hosing C, Saliba RM, Anderlini P, van Besien K, Przepiorka D, Khouri IF, Gajewski J, Claxton D, Giralt
S, Rodriguez M, Romaguera J, Hagemeister F, Ha C, Cox J, Cabanillas F, Andersson BS, Champlin RE. Prognostic
factors for disease progression after high-dose chemotherapy and autologous hematopoietic stem cell transplantation for
recurrent or refractory Hodgkin's lymphoma. Bone Marrow Transplant. 2004 May;33(10):1015-23. PubMed PMID:
15048145.
Updated 04/18/2013
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146: Stiff PJ, Unger JM, Forman SJ, McCall AR, LeBlanc M, Nademanee AP, Bolwell BJ, Fisher RI; Southwest
Oncology Group. The value of augmented preparative regimens combined with an autologous bone marrow transplant for
the management of relapsed or refractory Hodgkin disease: a Southwest Oncology Group phase II trial. Biol Blood
Marrow Transplant. 2003 Aug;9(8):529-39. PubMed PMID: 12931122.
184: Martín A, Fernández-Jiménez MC, Caballero MD, Canales MA, Pérez-Simón JA, García de Bustos J, Vázquez L,
Hernández-Navarro F, San Miguel JF. Long-term follow-up in patients treated with Mini-BEAM as salvage therapy for
relapsed or refractory Hodgkin's disease. Br J Haematol. 2001 Apr;113(1):161-71. PubMed PMID:11328296.
c. Autologous SCT versus Nontransplantation as Salvage Therapy
68: Gopal AK, Metcalfe TL, Gooley TA, Pagel JM, Petersdorf SH, Bensinger WI, Holmberg L, Maloney DG, Press OW.
High-dose therapy and autologous stem cell transplantation for chemoresistant Hodgkin lymphoma: the Seattle
experience. Cancer. 2008 Sep 15;113(6):1344-50. PubMed PMID: 18623377; PubMed Central PMCID: PMC2700660.
98: Sieniawski M, Franklin J, Nogova L, Glossmann JP, Schober T, Nisters-Backes H, Diehl V, Josting A. Outcome of
patients experiencing progression or relapse after primary treatment with two cycles of chemotherapy and radiotherapy for
early-stage favorable Hodgkin's lymphoma. J Clin Oncol. 2007 May 20;25(15):2000-5. Epub 2007 Apr 9. PubMed PMID:
17420510.
116: Morabito F, Stelitano C, Luminari S, Mammi C, Marcheselli L, Callea V, Gentile M, Polimeno G, Merli F, Molica S,
Gobbi P, Angrilli F, Brugiatelli M, Federico M. The role of high-dose therapy and autologous stem cell transplantation in
patients with primary refractory Hodgkin's lymphoma: a report from the Gruppo Italiano per lo Studio dei Linfomi
(GISL). Bone Marrow Transplant. 2006 Feb;37(3):283-8. PubMed PMID: 16327815.
120: Schellong G, Dörffel W, Claviez A, Körholz D, Mann G, Scheel-Walter HG, Bökkerink JP, Riepenhausen M, Lüders
H, Pötter R, Rühl U; DAL/GPOH. Salvage therapy of progressive and recurrent Hodgkin's disease: results from a
multicenter study of the pediatric DAL/GPOH-HD study group. J Clin Oncol. 2005 Sep 1;23(25):6181-9. PubMed PMID:
16135485.
130: Stoneham S, Ashley S, Pinkerton CR, Wallace WH, Shankar AG; United Kingdom Children's Cancer Study Group.
Outcome after autologous hemopoietic stem cell transplantation in relapsed or refractory childhood Hodgkin disease. J
Pediatr Hematol Oncol. 2004 Nov;26(11):740-5. PubMed PMID: 15543009.
139: Czyz J, Szydlo R, Knopinska-Posluszny W, Hellmann A, Gozdzik J, Hansz J, Smolewski P, Robak T, Osowiecki M,
Walewski J, Avigdor A, Nagler A, Zemelka T, Pawlicki M, Sawicki Z, Wojtukiewicz M, Kachel L, Holowiecki J,
Charlinski G, Jedrzejczak WW. Treatment for primary refractory Hodgkin's disease: a comparison of high-dose
chemotherapy followed by ASCT with conventional therapy. Bone Marrow Transplant. 2004 Jun;33(12):1225-9. PubMed
PMID: 15094747.
164: Schmitz N, Pfistner B, Sextro M, Sieber M, Carella AM, Haenel M, Boissevain F, Zschaber R, Müller P, Kirchner
H, Lohri A, Decker S, Koch B, Hasenclever D, Goldstone AH, Diehl V; German Hodgkin's Lymphoma Study Group;
Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. Aggressive conventional
chemotherapy compared with high-dose chemotherapy with autologous haemopoietic stem-cell transplantation for
relapsed chemosensitive Hodgkin's disease: a randomised trial. Lancet. 2002 Jun 15;359(9323):2065-71. PubMed PMID:
12086759.
171: Fermé C, Mounier N, Diviné M, Brice P, Stamatoullas A, Reman O, Voillat L, Jaubert J, Lederlin P, Colin P, Berger
F, Salles G. Intensive salvage therapy with high-dose chemotherapy for patients with advanced Hodgkin's disease in
relapse or failure after initial chemotherapy: results of the Groupe d'Etudes des Lymphomes de l'Adulte H89 Trial. J Clin
Oncol. 2002 Jan 15;20(2):467-75. PubMed PMID: 11786576.
Updated 04/18/2013
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Hodgkin Lymphoma EBR
V.
Autologous SCT for selected populations
a. Autologous SCT for Patients ≥ 60 Years of Age
19: Puig N, Pintilie M, Seshadri T, al-Farsi K, Franke N, Keating A, Kuruvilla J, Crump M. High-dose chemotherapy and
auto-SCT in elderly patients with Hodgkin's lymphoma. Bone Marrow Transplant. 2011 Oct;46(10):1339-44. doi:
10.1038/bmt.2010.294. Epub 2011 Jan 17. PubMed PMID: 21243027.
b. Autologous SCT for patients < 18 (21) years of Age
32: Metzger ML, Hudson MM, Krasin MJ, Wu J, Kaste SC, Kun LE, Sandlund JT, Howard SC. Initial response to
salvage therapy determines prognosis in relapsed pediatric Hodgkin lymphoma patients. Cancer. 2010 Sep
15;116(18):4376-84. PubMed PMID: 20564743; PubMed Central PMCID: PMC2936658.
47: Akhtar S, El Weshi A, Rahal M, Abdelsalam M, Al Husseini H, Maghfoor I. High-dose chemotherapy and autologous
stem cell transplant in adolescent patients with relapsed or refractory Hodgkin's lymphoma. Bone Marrow Transplant.
2010 Mar;45(3):476-82. Epub 2009 Sep 7. PubMed PMID: 19734949.
120: Schellong G, Dörffel W, Claviez A, Körholz D, Mann G, Scheel-Walter HG, Bökkerink JP, Riepenhausen M, Lüders
H, Pötter R, Rühl U; DAL/GPOH. Salvage therapy of progressive and recurrent Hodgkin's disease: results from a
multicenter study of the pediatric DAL/GPOH-HD study group. J Clin Oncol. 2005 Sep 1;23(25):6181-9. PubMed PMID:
16135485.
130: Stoneham S, Ashley S, Pinkerton CR, Wallace WH, Shankar AG; United Kingdom Children's Cancer Study Group.
Outcome after autologous hemopoietic stem cell transplantation in relapsed or refractory childhood Hodgkin disease. J
Pediatr Hematol Oncol. 2004 Nov;26(11):740-5. PubMed PMID: 15543009.
131: Lieskovsky YE, Donaldson SS, Torres MA, Wong RM, Amylon MD, Link MP, Agarwal R. High-dose therapy and
autologous hematopoietic stem-cell transplantation for recurrent or refractory pediatric Hodgkin's disease: results and
prognostic indices. J Clin Oncol. 2004 Nov 15;22(22):4532-40. PubMed PMID: 15542804.
183: Kobrinsky NL, Sposto R, Shah NR, Anderson JR, DeLaat C, Morse M, Warkentin P, Gilchrist GS, Cohen MD,
Shina D, Meadows AT. Outcomes of treatment of children and adolescents with recurrent non-Hodgkin's lymphoma and
Hodgkin's disease with dexamethasone, etoposide, cisplatin, cytarabine, and l-asparaginase, maintenance chemotherapy,
and transplantation: Children's Cancer Group Study CCG-5912. J Clin Oncol. 2001 May 1;19(9):2390-6. PubMed PMID:
11331317.
187: Frankovich J, Donaldson SS, Lee Y, Wong RM, Amylon M, Verneris MR. High-dose therapy and autologous
hematopoietic cell transplantation in children with primary refractory and relapsed Hodgkin's disease: atopy predicts
idiopathic diffuse lung injury syndromes. Biol Blood Marrow Transplant. 2001;7(1):49-57. PubMed PMID: 11215699.
197: Gorde-Grosjean S, Oberlin O, Leblanc T, Pacquement H, Donadieu J, Lambilliotte A, Schell M, Dommange F,
Munzer M, Paillard C, Schmitt C, Lutz P, Edan C, Ansoborlo S, Stephan JL, Michel G, Thomas C, Perel Y, Robert A,
Landman-Parker J. Outcome of children and adolescents with recurrent/refractory classical Hodgkin lymphoma, a study
from the Société Française de Lutte contre le Cancer des Enfants et des Adolescents (SFCE). Br J Haematol. 2012
Sep;158(5):649-56. doi: 10.1111/j.1365-2141.2012.09199.x. Epub 2012 Jul 4. PubMed PMID: 22757721.
VI.
Autologous SCT
a. Comparative Studies of Autologous SCT
i. Choice of induction therapy prior to first-line autologous SCT
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23: Josting A, Müller H, Borchmann P, Baars JW, Metzner B, Döhner H, Aurer I, Smardova L, Fischer T, Niederwieser
D, Schäfer-Eckart K, Schmitz N, Sureda A, Glossmann J, Diehl V, DeJong D, Hansmann ML, Raemaekers J, Engert A.
Dose intensity of chemotherapy in patients with relapsed Hodgkin's lymphoma. J Clin Oncol. 2010 Dec 1;28(34):5074-80.
Epub 2010 Oct 25. PubMed PMID: 20975066.
115: Kuruvilla J, Nagy T, Pintilie M, Tsang R, Keating A, Crump M. Similar response rates and superior early
progression-free survival with gemcitabine, dexamethasone, and cisplatin salvage therapy compared with carmustine,
etoposide, cytarabine, and melphalan salvage therapy prior to autologous stem cell transplantation for recurrent or
refractory Hodgkin lymphoma. Cancer. 2006 Jan 15;106(2):353-60. PubMed PMID: 16329112.
b. Noncomparative Studies of Autologous SCT
i. Salvage regimens prior to autologous SCT
1: Greaves P, Wilson A, Matthews J, Brown DL, Auer R, Montoto S, Lister TA, Gribben JG. Early relapse and refractory
disease remain risk factors in the anthracycline and autologous transplant era for patients with relapsed/refractory
classical Hodgkin lymphoma: a single centre intention-to-treat analysis. Br J Haematol. 2012 Apr;157(2):201-4. doi:
10.1111/j.1365-2141.2011.08993.x. Epub 2012 Jan 9. PubMed PMID: 22224653.
2: Moskowitz CH, Matasar MJ, Zelenetz AD, Nimer SD, Gerecitano J, Hamlin P, Horwitz S, Moskowitz AJ, Noy A,
Palomba L, Perales MA, Portlock C, Straus D, Maragulia JC, Schoder H, Yahalom J. Normalization of pre-ASCT, FDGPET imaging with second-line, non-cross-resistant, chemotherapy programs improves event-free survival in patients with
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M, Badros A, Kennedy A, Jacobs M, Hudes R, Ruehle K, Smith R, Kight L, Chambers S, MacFadden M, Cottler-Fox M,
Chen T, Phillips G, Tricot G. Autotransplantation for advanced lymphoma and Hodgkin's disease followed by posttransplant rituxan/GM-CSF or radiotherapy and consolidation chemotherapy. Bone Marrow Transplant. 2002
Feb;29(4):303-12. PubMed PMID: 11896427.
198: Goda JS, Massey C, Kuruvilla J, Gospodarowicz MK, Wells W, Hodgson DC, Sun A, Keating A, Crump M, Tsang
RW. Role of salvage radiation therapy for patients with relapsed or refractory hodgkin lymphoma who failed autologous
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VII.
Allogeneic SCT
a. Regimen Intensity
14: Ram R, Gooley TA, Maloney DG, Press OW, Pagel JM, Petersdorf SH, Shustov AR, Flowers ME, O'Donnell P,
Sandmaier BM, Storb RF, Gopal AK. Histology and time to progression predict survival for lymphoma recurring after
reduced-intensity conditioning and allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2011
Oct;17(10):1537-45. Epub 2011 Apr 12. PubMed PMID: 21536145;PubMed Central PMCID: PMC3176968.
18: Peggs KS, Kayani I, Edwards N, Kottaridis P, Goldstone AH, Linch DC, Hough R, Morris EC, Fielding A,
Chakraverty R, Thomson KJ, Mackinnon S. Donor lymphocyte infusions modulate relapse risk in mixed chimeras and
induce durable salvage in relapsed patients after T-cell-depleted allogeneic transplantation for Hodgkin's lymphoma. J
Clin Oncol. 2011 Mar 10;29(8):971-8. Epub 2011 Jan 31. PubMed PMID: 21282545.
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20: Chen R, Palmer JM, Popplewell L, Shen J, Smith E, Delioukina M, Kogut N, Rosenthal J, Forman S, Nademanee A.
Reduced intensity allogeneic hematopoietic cell transplantation can induce durable remission in heavily pretreated
relapsed Hodgkin lymphoma. Ann Hematol. 2011 Jul;90(7):803-8. Epub 2011 Jan 6. PubMed PMID: 21210120.
24: Johansson JE, Remberger M, Lazarevic VLj, Hallböök H, Wahlin A, Kimby E, Juliusson G, Omar H, Hägglund H.
Allogeneic haematopoietic stem-cell transplantation with reduced intensity conditioning for advanced stage Hodgkin's
lymphoma in Sweden: high incidence of post transplant lymphoproliferative disorder. Bone Marrow Transplant. 2011
Jun;46(6):870-5. doi: 10.1038/bmt.2010.238. Epub 2010 Oct 18. PubMed PMID: 20956959.
43: Kuruvilla J, Pintilie M, Stewart D, Lachance S, Power M, Couture F, Xenocostas A, Voralia M, Couban S, Foley R.
Outcomes of reduced-intensity conditioning allo-SCT for Hodgkin's lymphoma: a national review by the Canadian
Blood and Marrow Transplant Group. Bone Marrow Transplant. 2010 Jul;45(7):1253-5. Epub 2009 Nov 16. PubMed
PMID: 19915625.
51: Claviez A, Canals C, Dierickx D, Stein J, Badell I, Pession A, Mackinnon S, Slavin S, Dalle JH, Chacón MJ, Sarhan
M, Wynn RF, Suttorp M, Dini G, Sureda A, Schmitz N; Lymphoma and Pediatric Diseases Working Parties. Allogeneic
hematopoietic stem cell transplantation in children and adolescents with recurrent and refractory Hodgkin lymphoma: an
analysis of the European Group for Blood and Marrow Transplantation. Blood. 2009 Sep 3;114(10):2060-7. Epub 2009
Jun 4. PubMed PMID: 19498021.
57: Devetten MP, Hari PN, Carreras J, Logan BR, van Besien K, Bredeson CN, Freytes CO, Gale RP, Gibson J, Giralt
SA, Goldstein SC, Gupta V, Marks DI, Maziarz RT, Vose JM, Lazarus HM, Anderlini P. Unrelated donor reducedintensity allogeneic hematopoietic stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Biol Blood
Marrow Transplant. 2009 Jan;15(1):109-17. PubMed PMID: 19135949; PubMed Central PMCID: PMC2929570.
58: Robinson SP, Sureda A, Canals C, Russell N, Caballero D, Bacigalupo A, Iriondo A, Cook G, Pettitt A, Socie G,
Bonifazi F, Bosi A, Michallet M, Liakopoulou E, Maertens J, Passweg J, Clarke F, Martino R, Schmitz N; Lymphoma
Working Party of the EBMT. Reduced intensity conditioning allogeneic stem cell transplantation for Hodgkin's
lymphoma: identification of prognostic factors predicting outcome. Haematologica. 2009 Feb;94(2):230-8. Epub 2008
Dec 9. PubMed PMID: 19066328; PubMed Central PMCID: PMC2635413.
62: Burroughs LM, O'Donnell PV, Sandmaier BM, Storer BE, Luznik L, Symons HJ, Jones RJ, Ambinder RF, Maris MB,
Blume KG, Niederwieser DW, Bruno B, Maziarz RT, Pulsipher MA, Petersen FB, Storb R, Fuchs EJ, Maloney DG.
Comparison of outcomes of HLA-matched related, unrelated, or HLA-haploidentical related hematopoietic cell
transplantation following nonmyeloablative conditioning for relapsed or refractory Hodgkin lymphoma. Biol Blood
Marrow Transplant. 2008 Nov;14(11):1279-87. PubMed PMID: 18940683; PubMed Central PMCID: PMC2647369.
71: Tomblyn M, Brunstein C, Burns LJ, Miller JS, MacMillan M, DeFor TE, Weisdorf DJ. Similar and promising
outcomes in lymphoma patients treated with myeloablative or nonmyeloablative conditioning and allogeneic
hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2008 May;14(5):538-45. PubMed PMID: 18410896;
PubMed Central PMCID: PMC2423491.
75: Armand P, Kim HT, Ho VT, Cutler CS, Koreth J, Antin JH, LaCasce AS, Jacobsen ED, Fisher DC, Brown JR,
Canellos GP, Freedman AS, Soiffer RJ, Alyea EP. Allogeneic transplantation with reduced-intensity conditioning for
Hodgkin and non-Hodgkin lymphoma: importance of histology for outcome. Biol Blood Marrow Transplant. 2008
Apr;14(4):418-25. PubMed PMID: 18342784; PubMed Central PMCID: PMC2364453.
78: Anderlini P, Saliba R, Acholonu S, Giralt SA, Andersson B, Ueno NT, Hosing C, Khouri IF, Couriel D, de Lima M,
Qazilbash MH, Pro B, Romaguera J, Fayad L, Hagemeister F, Younes A, Munsell MF, Champlin RE. Fludarabinemelphalan as a preparative regimen for reduced-intensity conditioning allogeneic stem cell transplantation in relapsed and
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refractory Hodgkin's lymphoma: the updated M.D. Anderson Cancer Center experience. Haematologica. 2008
Feb;93(2):257-64. Epub 2008 Jan 26. PubMed PMID: 18223284.
79: Thomson KJ, Peggs KS, Smith P, Cavet J, Hunter A, Parker A, Pettengell R, Milligan D, Morris EC, Goldstone AH,
Linch DC, Mackinnon S. Superiority of reduced-intensity allogeneic transplantation over conventional treatment for
relapse of Hodgkin's lymphoma following autologous stem cell transplantation. Bone Marrow Transplant. 2008
May;41(9):765-70. Epub 2008 Jan 14. PubMed PMID: 18195684.
80: Sureda A, Robinson S, Canals C, Carella AM, Boogaerts MA, Caballero D, Hunter AE, Kanz L, Slavin S, Cornelissen
JJ, Gramatzki M, Niederwieser D, Russell NH, Schmitz N. Reduced-intensity conditioning compared with conventional
allogeneic stem-cell transplantation in relapsed or refractory Hodgkin's lymphoma: an analysis from the Lymphoma
Working Party of the European Group for Blood and Marrow Transplantation. J Clin Oncol. 2008 Jan 20;26(3):455-62.
Epub 2007 Dec 17. PubMed PMID: 18086796.
90: Kahl C, Storer BE, Sandmaier BM, Mielcarek M, Maris MB, Blume KG, Niederwieser D, Chauncey TR, Forman SJ,
Agura E, Leis JF, Bruno B, Langston A, Pulsipher MA, McSweeney PA, Wade JC, Epner E, Bo Petersen F, Bethge WA,
Maloney DG, Storb R. Relapse risk in patients with malignant diseases given allogeneic hematopoietic cell transplantation
after nonmyeloablative conditioning. Blood. 2007 Oct 1;110(7):2744-8. Epub 2007 Jun 26. PubMed PMID: 17595333;
PubMed Central PMCID: PMC1988951.
213: Sureda A, Canals C, Arranz R, Caballero D, Ribera JM, Brune M, Passweg J, Martino R, Valcárcel D, Besalduch J,
Duarte R, León A, Pascual MJ, García-Noblejas A, López Corral L, Xicoy B, Sierra J, Schmitz N. Allogeneic stem cell
transplantation after reduced intensity conditioning in patients with relapsed or refractory Hodgkin's lymphoma. Results of
the HDR-ALLO study – a prospective clinical trial by the Grupo Español de Linfomas/Trasplante de Médula Osea
(GEL/TAMO) and the Lymphoma Working Party of the European Group for Blood and Marrow Transplantation.
Haematologica. 2012 Feb;97(2):310-7. doi:10.3324/haematol.2011.045757. Epub 2011 Oct 11. PubMed PMID:
21993674; PubMed Central PMCID: PMC3269494.
b. Stem cell source
18: Peggs KS, Kayani I, Edwards N, Kottaridis P, Goldstone AH, Linch DC, Hough R, Morris EC, Fielding A,
Chakraverty R, Thomson KJ, Mackinnon S. Donor lymphocyte infusions modulate relapse risk in mixed chimeras and
induce durable salvage in relapsed patients after T-cell-depleted allogeneic transplantation for Hodgkin's lymphoma. J
Clin Oncol. 2011 Mar 10;29(8):971-8. Epub 2011 Jan 31. PubMed PMID: 21282545.
62: Burroughs LM, O'Donnell PV, Sandmaier BM, Storer BE, Luznik L, Symons HJ, Jones RJ, Ambinder RF, Maris MB,
Blume KG, Niederwieser DW, Bruno B, Maziarz RT, Pulsipher MA, Petersen FB, Storb R, Fuchs EJ, Maloney DG.
Comparison of outcomes of HLA-matched related, unrelated, or HLA-haploidentical related hematopoietic cell
transplantation following nonmyeloablative conditioning for relapsed or refractory Hodgkin lymphoma. Biol Blood
Marrow Transplant. 2008 Nov;14(11):1279-87. PubMed PMID: 18940683; PubMed Central PMCID: PMC2647369.
c. Donor leukocyte infusion
18: Peggs KS, Kayani I, Edwards N, Kottaridis P, Goldstone AH, Linch DC, Hough R, Morris EC, Fielding A,
Chakraverty R, Thomson KJ, Mackinnon S. Donor lymphocyte infusions modulate relapse risk in mixed chimeras and
induce durable salvage in relapsed patients after T-cell-depleted allogeneic transplantation for Hodgkin's lymphoma. J
Clin Oncol. 2011 Mar 10;29(8):971-8. Epub 2011 Jan 31. PubMed PMID: 21282545.
78: Anderlini P, Saliba R, Acholonu S, Giralt SA, Andersson B, Ueno NT, Hosing C, Khouri IF, Couriel D, de Lima M,
Qazilbash MH, Pro B, Romaguera J, Fayad L, Hagemeister F, Younes A, Munsell MF, Champlin RE. Fludarabinemelphalan as a preparative regimen for reduced-intensity conditioning allogeneic stem cell transplantation in relapsed and
Updated 04/18/2013
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Hodgkin Lymphoma EBR
refractory Hodgkin's lymphoma: the updated M.D. Anderson Cancer Center experience. Haematologica. 2008
Feb;93(2):257-64. Epub 2008 Jan 26. PubMed PMID: 18223284.
86: Peggs KS, Sureda A, Qian W, Caballero D, Hunter A, Urbano-Ispizua A, Cavet J, Ribera JM, Parker A, Canales M,
Mahendra P, Garcia-Conde J, Milligan D, Sanz G, Thomson K, Arranz R, Goldstone AH, Alvarez I, Linch DC, Sierra J,
Mackinnon S; UK and Spanish Collaborative Groups. Reduced-intensity conditioning for allogeneic haematopoietic stem
cell transplantation in relapsed and refractory Hodgkin lymphoma: impact of alemtuzumab and donor lymphocyte
infusions on long-term outcomes. Br J Haematol. 2007 Oct;139(1):70-80. PubMed PMID: 17854309.
112: Alvarez I, Sureda A, Caballero MD, Urbano-Ispizua A, Ribera JM, Canales M, García-Conde J, Sanz G, Arranz R,
Bernal MT, de la Serna J, Díez JL, Moraleda JM, Rubió-Félix D, Xicoy B, Martínez C, Mateos MV, Sierra J.
Nonmyeloablative stem cell transplantation is an effective therapy for refractory or relapsed Hodgkin lymphoma: results
of a spanish prospective cooperative protocol. Biol Blood Marrow Transplant. 2006 Feb;12(2):172-83. PubMed PMID:
16443515.
123: Peggs KS, Hunter A, Chopra R, Parker A, Mahendra P, Milligan D, Craddock C, Pettengell R, Dogan A, Thomson
KJ, Morris EC, Hale G, Waldmann H, Goldstone AH, Linch DC, Mackinnon S. Clinical evidence of a graft-versusHodgkin's-lymphoma effect after reduced-intensity allogeneic transplantation. Lancet. 2005 Jun 4-10;365(9475):1934-41.
PubMed PMID: 15936420.
125: Anderlini P, Saliba R, Acholonu S, Okoroji GJ, Donato M, Giralt S, Andersson B, Ueno NT, Khouri I, De Lima M,
Hosing C, Cohen A, Ippoliti C, Romaguera J, Rodriguez MA, Pro B, Fayad L, Goy A, Younes A, Champlin RE.
Reduced-intensity allogeneic stem cell transplantation in relapsed and refractory Hodgkin's disease: low transplant-related
mortality and impact of intensity of conditioning regimen. Bone Marrow Transplant. 2005 May;35(10):943-51. PubMed
PMID: 15806128.
211: Anderlini P, Saliba R, Acholonu S, Okoroji GJ, Ledesma C, Andersson BS, Jones R, Popat UR, Hosing CM, Nieto
Y, Qazilbash MH, Ueno NT, Giralt SA, de Lima MJ, Champlin RE. Donor leukocyte infusions in recurrent Hodgkin
lymphoma following allogeneic stem cell transplant: 10-year experience at the M. D. Anderson Cancer Center. Leuk
Lymphoma. 2012 Jun;53(6):1239-41. doi: 10.3109/10428194.2011.644547. Epub 2012 Jan 5. PubMed PMID: 22132837.
d. Allogeneic SCT vs. non-transplantation therapy
39: Sarina B, Castagna L, Farina L, Patriarca F, Benedetti F, Carella AM, Falda M, Guidi S, Ciceri F, Bonini A, Ferrari S,
Malagola M, Morello E, Milone G, Bruno B, Mordini N, Viviani S, Levis A, Giordano L, Santoro A, Corradini P; Gruppo
Italiano Trapianto di Midollo Osseo. Allogeneic transplantation improves the overall and progression-free survival of
Hodgkin lymphoma patients relapsing after autologous transplantation: a retrospective study based on the time of HLA
typing and donor availability. Blood. 2010 May 6;115(18):3671-7. Epub 2010 Mar 10. PubMed PMID: 20220116.
53: Castagna L, Sarina B, Todisco E, Magagnoli M, Balzarotti M, Bramanti S, Mazza R, Anastasia A, Bacigalupo A,
Aversa F, Soligo D, Giordano L, Santoro A. Allogeneic stem cell transplantation compared with chemotherapy for poorrisk Hodgkin lymphoma. Biol Blood Marrow Transplant. 2009 Apr;15(4):432-8. Epub 2009 Feb 12. PubMed PMID:
19285630.
e. Tandem auto-allo SCT
f.
Allogeneic SCT for selected populations
51: Claviez A, Canals C, Dierickx D, Stein J, Badell I, Pession A, Mackinnon S, Slavin S, Dalle JH, Chacón MJ, Sarhan
M, Wynn RF, Suttorp M, Dini G, Sureda A, Schmitz N; Lymphoma and Pediatric Diseases Working Parties. Allogeneic
Updated 04/18/2013
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Hodgkin Lymphoma EBR
hematopoietic stem cell transplantation in children and adolescents with recurrent and refractory Hodgkin lymphoma: an
analysis of the European Group for Blood and Marrow Transplantation. Blood. 2009 Sep 3;114(10):2060-7. Epub 2009
Jun 4. PubMed PMID: 19498021.
VIII.
Autologous versus Allogeneic SCT
a. Allogeneic SCT as first line therapy
18: Peggs KS, Kayani I, Edwards N, Kottaridis P, Goldstone AH, Linch DC, Hough R, Morris EC, Fielding A,
Chakraverty R, Thomson KJ, Mackinnon S. Donor lymphocyte infusions modulate relapse risk in mixed chimeras and
induce durable salvage in relapsed patients after T-cell-depleted allogeneic transplantation for Hodgkin's lymphoma. J
Clin Oncol. 2011 Mar 10;29(8):971-8. Epub 2011 Jan 31. PubMed PMID: 21282545.
114: Majhail NS, Weisdorf DJ, Wagner JE, Defor TE, Brunstein CG, Burns LJ. Comparable results of umbilical cord
blood and HLA-matched sibling donor hematopoietic stem cell transplantation after reduced-intensity preparative
regimen for advanced Hodgkin lymphoma. Blood. 2006 May 1;107(9):3804-7. Epub 2005 Dec 29. PubMed PMID:
16384924.
123: Peggs KS, Hunter A, Chopra R, Parker A, Mahendra P, Milligan D, Craddock C, Pettengell R, Dogan A, Thomson
KJ, Morris EC, Hale G, Waldmann H, Goldstone AH, Linch DC, Mackinnon S. Clinical evidence of a graft-versusHodgkin's-lymphoma effect after reduced-intensity allogeneic transplantation. Lancet. 2005 Jun 4-10;365(9475):1934-41.
PubMed PMID: 15936420.
156: Peniket AJ, Ruiz de Elvira MC, Taghipour G, Cordonnier C, Gluckman E, de Witte T, Santini G, Blaise D, Greinix
H, Ferrant A, Cornelissen J, Schmitz N, Goldstone AH; European Bone Marrow Transplantation (EBMT) Lymphoma
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associated with a lower relapse rate but a higher procedure-related mortality rate than autologous transplantation. Bone
Marrow Transplant. 2003 Apr;31(8):667-78. PubMed PMID: 12692607.
159: Robinson SP, Goldstone AH, Mackinnon S, Carella A, Russell N, de Elvira CR, Taghipour G, Schmitz N;
Lymphoma Working Party of the European Group for Blood and Bone Marrow Transplantation. Chemoresistant or
aggressive lymphoma predicts for a poor outcome following reduced-intensity allogeneic progenitor cell transplantation:
an analysis from the Lymphoma Working Party of the European Group for Blood and Bone Marrow Transplantation.
Blood. 2002 Dec 15;100(13):4310-6. Epub 2002 Aug 15. PubMed PMID: 12393626.
175: Akpek G, Ambinder RF, Piantadosi S, Abrams RA, Brodsky RA, Vogelsang GB, Zahurak ML, Fuller D, Miller CB,
Noga SJ, Fuchs E, Flinn IW, O'Donnell P, Seifter EJ, Mann RB, Jones RJ. Long-term results of blood and marrow
transplantation for Hodgkin's lymphoma. J Clin Oncol. 2001 Dec 1;19(23):4314-21. PubMed PMID: 11731514.
214: Kaloyannidis P, Voutiadou G, Baltadakis I, Tsirigotis P, Spyridonidis A, Repousis P, Balta A, Tsimberis S,
Karakasis D, Sakellari I, Dervenoulas I, Harhalakis N, Anagnostopoulos A. Outcomes of Hodgkin's lymphoma patients
with relapse or progression following autologous hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2012
Mar;18(3):451-7. doi: 10.1016/j.bbmt.2011.07.020. Epub 2011 Jul 29. PubMed PMID: 21803018.
b. Salvage after failed autologous SCT
i. Second autologous SCT
67: Smith SM, van Besien K, Carreras J, Bashey A, Cairo MS, Freytes CO, Gale RP, Hale GA, Hayes-Lattin B,
Holmberg LA, Keating A, Maziarz RT, McCarthy PL, Navarro WH, Pavlovsky S, Schouten HC, Seftel M, Wiernik PH,
Vose JM, Lazarus HM, Hari P. Second autologous stem cell transplantation for relapsed lymphoma after a prior
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Hodgkin Lymphoma EBR
autologous transplant. Biol Blood Marrow Transplant. 2008 Aug;14(8):904-12. PubMed PMID: 18640574; PubMed
Central PMCID: PMC3353768.
ii. Allogeneic SCT
39: Sarina B, Castagna L, Farina L, Patriarca F, Benedetti F, Carella AM, Falda M, Guidi S, Ciceri F, Bonini A, Ferrari S,
Malagola M, Morello E, Milone G, Bruno B, Mordini N, Viviani S, Levis A, Giordano L, Santoro A, Corradini P; Gruppo
Italiano Trapianto di Midollo Osseo. Allogeneic transplantation improves the overall and progression-free survival of
Hodgkin lymphoma patients relapsing after autologous transplantation: a retrospective study based on the time of HLA
typing and donor availability. Blood. 2010 May 6;115(18):3671-7. Epub 2010 Mar 10. PubMed PMID: 20220116.
52: Moskowitz AJ, Perales MA, Kewalramani T, Yahalom J, Castro-Malaspina H, Zhang Z, Vanak J, Zelenetz AD,
Moskowitz CH. Outcomes for patients who fail high dose chemoradiotherapy and autologous stem cell rescue for relapsed
and primary refractory Hodgkin lymphoma. Br J Haematol. 2009 Jul;146(2):158-63. Epub 2009 May 12. PubMed PMID:
19438504; PubMed Central PMCID: PMC3278667.
57: Devetten MP, Hari PN, Carreras J, Logan BR, van Besien K, Bredeson CN, Freytes CO, Gale RP, Gibson J, Giralt
SA, Goldstein SC, Gupta V, Marks DI, Maziarz RT, Vose JM, Lazarus HM, Anderlini P. Unrelated donor reducedintensity allogeneic hematopoietic stem cell transplantation for relapsed and refractory Hodgkin lymphoma. Biol Blood
Marrow Transplant. 2009 Jan;15(1):109-17. PubMed PMID: 19135949; PubMed Central PMCID: PMC2929570.
58: Robinson SP, Sureda A, Canals C, Russell N, Caballero D, Bacigalupo A, Iriondo A, Cook G, Pettitt A, Socie G,
Bonifazi F, Bosi A, Michallet M, Liakopoulou E, Maertens J, Passweg J, Clarke F, Martino R, Schmitz N; Lymphoma
Working Party of the EBMT. Reduced intensity conditioning allogeneic stem cell transplantation for Hodgkin's
lymphoma: identification of prognostic factors predicting outcome. Haematologica. 2009 Feb;94(2):230-8. Epub 2008
Dec 9. PubMed PMID: 19066328; PubMed Central PMCID: PMC2635413.
78: Anderlini P, Saliba R, Acholonu S, Giralt SA, Andersson B, Ueno NT, Hosing C, Khouri IF, Couriel D, de Lima M,
Qazilbash MH, Pro B, Romaguera J, Fayad L, Hagemeister F, Younes A, Munsell MF, Champlin RE. Fludarabinemelphalan as a preparative regimen for reduced-intensity conditioning allogeneic stem cell transplantation in relapsed and
refractory Hodgkin's lymphoma: the updated M.D. Anderson Cancer Center experience. Haematologica. 2008
Feb;93(2):257-64. Epub 2008 Jan 26. PubMed PMID: 18223284.
79: Thomson KJ, Peggs KS, Smith P, Cavet J, Hunter A, Parker A, Pettengell R, Milligan D, Morris EC, Goldstone AH,
Linch DC, Mackinnon S. Superiority of reduced-intensity allogeneic transplantation over conventional treatment for
relapse of Hodgkin's lymphoma following autologous stem cell transplantation. Bone Marrow Transplant. 2008
May;41(9):765-70. Epub 2008 Jan 14. PubMed PMID: 18195684.
86: Peggs KS, Sureda A, Qian W, Caballero D, Hunter A, Urbano-Ispizua A, Cavet J, Ribera JM, Parker A, Canales M,
Mahendra P, Garcia-Conde J, Milligan D, Sanz G, Thomson K, Arranz R, Goldstone AH, Alvarez I, Linch DC, Sierra J,
Mackinnon S; UK and Spanish Collaborative Groups. Reduced-intensity conditioning for allogeneic haematopoietic stem
cell transplantation in relapsed and refractory Hodgkin lymphoma: impact of alemtuzumab and donor lymphocyte
infusions on long-term outcomes. Br J Haematol. 2007 Oct;139(1):70-80. PubMed PMID: 17854309.
109: Baron F, Storb R, Storer BE, Maris MB, Niederwieser D, Shizuru JA, Chauncey TR, Bruno B, Forman SJ,
McSweeney PA, Maziarz RT, Pulsipher MA, Agura ED, Wade J, Sorror M, Maloney DG, Sandmaier BM. Factors
associated with outcomes in allogeneic hematopoietic cell transplantation with nonmyeloablative conditioning
after failed myeloablative hematopoietic cell transplantation. J Clin Oncol. 2006 Sep 1;24(25):4150-7. Epub 2006 Aug 8.
PubMed PMID: 16896000.
112: Alvarez I, Sureda A, Caballero MD, Urbano-Ispizua A, Ribera JM, Canales M, García-Conde J, Sanz G, Arranz R,
Bernal MT, de la Serna J, Díez JL, Moraleda JM, Rubió-Félix D, Xicoy B, Martínez C, Mateos MV, Sierra J.
Updated 04/18/2013
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Hodgkin Lymphoma EBR
Nonmyeloablative stem cell transplantation is an effective therapy for refractory or relapsed Hodgkin lymphoma: results
of a spanish prospective cooperative protocol. Biol Blood Marrow Transplant. 2006 Feb;12(2):172-83. PubMed PMID:
16443515.
114: Majhail NS, Weisdorf DJ, Wagner JE, Defor TE, Brunstein CG, Burns LJ. Comparable results of umbilical cord
blood and HLA-matched sibling donor hematopoietic stem cell transplantation after reduced-intensity preparative
regimen for advanced Hodgkin lymphoma. Blood. 2006 May 1;107(9):3804-7. Epub 2005 Dec 29. PubMed PMID:
16384924.
123: Peggs KS, Hunter A, Chopra R, Parker A, Mahendra P, Milligan D, Craddock C, Pettengell R, Dogan A, Thomson
KJ, Morris EC, Hale G, Waldmann H, Goldstone AH, Linch DC, Mackinnon S. Clinical evidence of a graft-versusHodgkin's-lymphoma effect after reduced-intensity allogeneic transplantation. Lancet. 2005 Jun 4-10;365(9475):1934-41.
PubMed PMID: 15936420.
125: Anderlini P, Saliba R, Acholonu S, Okoroji GJ, Donato M, Giralt S, Andersson B, Ueno NT, Khouri I, De Lima M,
Hosing C, Cohen A, Ippoliti C, Romaguera J, Rodriguez MA, Pro B, Fayad L, Goy A, Younes A, Champlin RE.
Reduced-intensity allogeneic stem cell transplantation in relapsed and refractory Hodgkin's disease: low transplant-related
mortality and impact of intensity of conditioning regimen. Bone Marrow Transplant. 2005 May;35(10):943-51. PubMed
PMID: 15806128.
137: Freytes CO, Loberiza FR, Rizzo JD, Bashey A, Bredeson CN, Cairo MS, Gale RP, Horowitz MM, Klumpp TR,
Martino R, McCarthy PL, Molina A, Pavlovsky S, Pecora AL, Serna DS, Tsai T, Zhang MJ, Vose JM, Lazarus HM, van
Besien K; Lymphoma Working Committee of the International Bone Marrow Transplant Registry. Myeloablative
allogeneic hematopoietic stem cell transplantation in patients who experience relapse after autologous stem cell
transplantation for lymphoma: a report of the International Bone Marrow Transplant Registry. Blood. 2004 Dec
1;104(12):3797-803. Epub 2004 Jul 27. PubMed PMID: 15280203.
159: Robinson SP, Goldstone AH, Mackinnon S, Carella A, Russell N, de Elvira CR, Taghipour G, Schmitz N;
Lymphoma Working Party of the European Group for Blood and Bone Marrow Transplantation. Chemoresistant or
aggressive lymphoma predicts for a poor outcome following reduced-intensity allogeneic progenitor cell transplantation:
an analysis from the Lymphoma Working Party of the European Group for Blood and Bone Marrow Transplantation.
Blood. 2002 Dec 15;100(13):4310-6. Epub 2002 Aug 15. PubMed PMID: 12393626.
213: Sureda A, Canals C, Arranz R, Caballero D, Ribera JM, Brune M, Passweg J, Martino R, Valcárcel D, Besalduch J,
Duarte R, León A, Pascual MJ, García-Noblejas A, López Corral L, Xicoy B, Sierra J, Schmitz N. Allogeneic stem cell
transplantation after reduced intensity conditioning in patients with relapsed or refractory Hodgkin's lymphoma. Results of
the HDR-ALLO study – a prospective clinical trial by the Grupo Español de Linfomas/Trasplante de Médula Osea
(GEL/TAMO) and the Lymphoma Working Party of the European Group for Blood and Marrow Transplantation.
Haematologica. 2012 Feb;97(2):310-7. doi:10.3324/haematol.2011.045757. Epub 2011 Oct 11. PubMed PMID:
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IX.
Prognostic factors
a. Clinical factors
i. At relapse
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disease remain risk factors in the anthracycline and autologous transplant era for patients with relapsed/refractory
classical Hodgkin lymphoma: a single centre intention-to-treat analysis. Br J Haematol. 2012 Apr;157(2):201-4. doi:
10.1111/j.1365-2141.2011.08993.x. Epub 2012 Jan 9. PubMed PMID: 22224653.
Updated 04/18/2013
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Hodgkin Lymphoma EBR
2: Moskowitz CH, Matasar MJ, Zelenetz AD, Nimer SD, Gerecitano J, Hamlin P, Horwitz S, Moskowitz AJ, Noy A,
Palomba L, Perales MA, Portlock C, Straus D, Maragulia JC, Schoder H, Yahalom J. Normalization of pre-ASCT, FDGPET imaging with second-line, non-cross-resistant, chemotherapy programs improves event-free survival in patients with
Hodgkin lymphoma. Blood. 2012 Feb 16;119(7):1665-70. Epub 2011 Dec 19. PubMed PMID: 22184409.
10: Mocikova H, Pytlik R, Markova J, Steinerova K, Kral Z, Belada D, Trnkova M, Trneny M, Koza V, Mayer J, Zak P,
Kozak T. Pre-transplant positron emission tomography in patients with relapsed Hodgkin lymphoma. Leuk Lymphoma.
2011 Sep;52(9):1668-74. Epub 2011 Jun 23. PubMed PMID: 21699377.
16: Smith SD, Moskowitz CH, Dean R, Pohlman B, Sobecks R, Copelan E, Andresen S, Bolwell B, Maragulia JC, Vanak
JM, Sweetenham J, Moskowitz AJ. Autologous stem cell transplant for early relapsed/refractory Hodgkin lymphoma:
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Epub 2011 Mar 16. PubMed PMID: 21410449.
73: Sirohi B, Cunningham D, Powles R, Murphy F, Arkenau T, Norman A, Oates J, Wotherspoon A, Horwich A. Longterm outcome of autologous stem-cell transplantation in relapsed or refractory Hodgkin's lymphoma. Ann Oncol. 2008
Jul;19(7):1312-9. Epub 2008 Mar 19. PubMed PMID: 18356139.
87: Engelhardt BG, Holland DW, Brandt SJ, Chinratanalab W, Goodman SA, Greer JP, Jagasia MH, Kassim AA,
Morgan DS, Ruffner KL, Schuening FG, Wolff S, Bitting R, Sulur P, Stein RS. High-dose chemotherapy followed by
autologous stem cell transplantation for relapsed or refractory Hodgkin lymphoma: prognostic features and outcomes.
Leuk Lymphoma. 2007 Sep;48(9):1728-35. PubMed PMID: 17786708.
89: Akhtar S, El Weshi A, Abdelsalam M, Hussaini H, Janabi I, Rahal M, Maghfoor I. Primary refractory Hodgkin's
lymphoma: outcome after high-dose chemotherapy and autologous SCT and impact of various prognostic factors on
overall and event-free survival. A single institution result of 66 patients. Bone Marrow Transplant. 2007 Oct;40(7):651-8.
Epub 2007 Jul 30. PubMed PMID: 17660837.
98: Sieniawski M, Franklin J, Nogova L, Glossmann JP, Schober T, Nisters-Backes H, Diehl V, Josting A. Outcome of
patients experiencing progression or relapse after primary treatment with two cycles of chemotherapy and radiotherapy for
early-stage favorable Hodgkin's lymphoma. J Clin Oncol. 2007 May 20;25(15):2000-5. Epub 2007 Apr 9. PubMed PMID:
17420510.
99: Evens AM, Altman JK, Mittal BB, Hou N, Rademaker A, Patton D, Kaminer L, Williams S, Duffey S, Variakojis D,
Singhal S, Tallman MS, Mehta J, Winter JN, Gordon LI. Phase I/II trial of total lymphoid irradiation and high-dose
chemotherapy with autologous stem-cell transplantation for relapsed and refractory Hodgkin's lymphoma. Ann Oncol.
2007 Apr;18(4):679-88. Epub 2007 Feb 16. PubMed PMID: 17307757.
100: Santoro A, Magagnoli M, Spina M, Pinotti G, Siracusano L, Michieli M, Nozza A, Sarina B, Morenghi E, Castagna
L, Tirelli U, Balzarotti M. Ifosfamide, gemcitabine, and vinorelbine: a new induction regimen for refractory and relapsed
Hodgkin's lymphoma. Haematologica. 2007 Jan;92(1):35-41. PubMed PMID: 17229633.
104: Majhail NS, Weisdorf DJ, Defor TE, Miller JS, McGlave PB, Slungaard A, Arora M, Ramsay NK, Orchard PJ,
MacMillan ML, Burns LJ. Long-term results of autologous stem cell transplantation for primary refractory or relapsed
Hodgkin's lymphoma. Biol Blood Marrow Transplant. 2006 Oct;12(10):1065-72. PubMed PMID: 17084370.
107: Schot BW, Zijlstra JM, Sluiter WJ, van Imhoff GW, Pruim J, Vaalburg W, Vellenga E. Early FDG-PET assessment
in combination with clinical risk scores determines prognosis in recurring lymphoma. Blood. 2007 Jan 15;109(2):486-91.
Epub 2006 Sep 26. PubMed PMID: 17003382.
112: Alvarez I, Sureda A, Caballero MD, Urbano-Ispizua A, Ribera JM, Canales M, García-Conde J, Sanz G, Arranz R,
Bernal MT, de la Serna J, Díez JL, Moraleda JM, Rubió-Félix D, Xicoy B, Martínez C, Mateos MV, Sierra J.
Updated 04/18/2013
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Nonmyeloablative stem cell transplantation is an effective therapy for refractory or relapsed Hodgkin lymphoma: results
of a spanish prospective cooperative protocol. Biol Blood Marrow Transplant. 2006 Feb;12(2):172-83. PubMed PMID:
16443515.
114: Majhail NS, Weisdorf DJ, Wagner JE, Defor TE, Brunstein CG, Burns LJ. Comparable results of umbilical cord
blood and HLA-matched sibling donor hematopoietic stem cell transplantation after reduced-intensity preparative
regimen for advanced Hodgkin lymphoma. Blood. 2006 May 1;107(9):3804-7. Epub 2005 Dec 29. PubMed PMID:
16384924.
116: Morabito F, Stelitano C, Luminari S, Mammi C, Marcheselli L, Callea V, Gentile M, Polimeno G, Merli F, Molica S,
Gobbi P, Angrilli F, Brugiatelli M, Federico M. The role of high-dose therapy and autologous stem cell transplantation in
patients with primary refractory Hodgkin's lymphoma: a report from the Gruppo Italiano per lo Studio dei Linfomi
(GISL). Bone Marrow Transplant. 2006 Feb;37(3):283-8. PubMed PMID: 16327815.
124: Lavoie JC, Connors JM, Phillips GL, Reece DE, Barnett MJ, Forrest DL, Gascoyne RD, Hogge DE, Nantel SH,
Shepherd JD, Smith CA, Song KW, Sutherland HJ, Toze CL, Voss NJ, Nevill TJ. High-dose chemotherapy and
autologous stem cell transplantation for primary refractory or relapsed Hodgkin lymphoma: long-term outcome in the first
100 patients treated in Vancouver. Blood. 2005 Aug 15;106(4):1473-8. Epub 2005 May 3. PubMed PMID: 15870180.
126: Sureda A, Constans M, Iriondo A, Arranz R, Caballero MD, Vidal MJ, Petit J, López A, Lahuerta JJ, Carreras E,
García-Conde J, García-Laraña J, Cabrera R, Jarque I, Carrera D, García-Ruiz JC, Pascual MJ, Rifón J, Moraleda JM,
Pérez-Equiza K, Albó C, Díaz-Mediavilla J, Torres A, Torres P, Besalduch J, Marín J, Mateos MV, Fernández-Rañada
JM, Sierra J, Conde E; Grupo Español de Linfomas/Trasplante Autólogo de Médula Osea Cooperative Group. Prognostic
factors affecting long-term outcome after stem cell transplantation in Hodgkin's lymphoma autografted after a first
relapse. Ann Oncol. 2005 Apr;16(4):625-33. Epub 2005 Feb 28. PubMed PMID: 15737986.
129: Josting A, Rudolph C, Mapara M, Glossmann JP, Sieniawski M, Sieber M, Kirchner HH, Dörken B, Hossfeld DK,
Kisro J, Metzner B, Berdel WE, Diehl V, Engert A. Cologne high-dose sequential chemotherapy in relapsed and
refractory Hodgkin lymphoma: results of a large multicenter study of the German Hodgkin Lymphoma Study Group
(GHSG). Ann Oncol. 2005 Jan;16(1):116-23. Erratum in: Ann Oncol. 2008 Aug;19(8):1515. Sienawski, M [corrected to
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131: Lieskovsky YE, Donaldson SS, Torres MA, Wong RM, Amylon MD, Link MP, Agarwal R. High-dose therapy and
autologous hematopoietic stem-cell transplantation for recurrent or refractory pediatric Hodgkin's disease: results and
prognostic indices. J Clin Oncol. 2004 Nov 15;22(22):4532-40. PubMed PMID: 15542804.
139: Czyz J, Szydlo R, Knopinska-Posluszny W, Hellmann A, Gozdzik J, Hansz J, Smolewski P, Robak T, Osowiecki M,
Walewski J, Avigdor A, Nagler A, Zemelka T, Pawlicki M, Sawicki Z, Wojtukiewicz M, Kachel L, Holowiecki J,
Charlinski G, Jedrzejczak WW. Treatment for primary refractory Hodgkin's disease: a comparison of high-dose
chemotherapy followed by ASCT with conventional therapy. Bone Marrow Transplant. 2004 Jun;33(12):1225-9. PubMed
PMID: 15094747.
142: Moskowitz CH, Kewalramani T, Nimer SD, Gonzalez M, Zelenetz AD, Yahalom J. Effectiveness of high dose
chemoradiotherapy and autologous stem cell transplantation for patients with biopsy-proven primary refractory Hodgkin's
disease. Br J Haematol. 2004 Mar;124(5):645-52. PubMed PMID: 14871252.
143: Qazilbash MH, Devetten MP, Abraham J, Lynch JP, Beall CL, Auber M, Weisenborn R, Bunner P, Ericson SG.
High-dose therapy and autologous stem cell transplantation in relapsed and refractory Hodgkin's disease: outcome based
on a prognostic model. Acta Haematol. 2003;110(4):173-8. PubMed PMID: 14663160.
150: Tarella C, Cuttica A, Vitolo U, Liberati M, Di Nicola M, Cortelazzo S, Rosato R, Rosanelli C, Di Renzo N, Musso
M, Pavone E, Santini G, Pescarollo A, De Crescenzo A, Federico M, Gallamini A, Pregno P, Romano R, Coser P, Gallo
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E, Boccadoro M, Barbui T, Pileri A, Gianni AM, Levis A. High-dose sequential chemotherapy and peripheral blood
progenitor cell autografting in patients with refractory and/or recurrent Hodgkin lymphoma: a multicenter study of the
intergruppo Italiano Linfomi showing prolonged disease free survival in patients treated at first recurrence. Cancer. 2003
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154: Constans M, Sureda A, Terol MJ, Arranz R, Caballero MD, Iriondo A, Jarque I, Carreras E, Moraleda JM, Carrera
D, León A, López A, Albó C, Díaz-Mediavilla J, Fernández-Abellán P, García-Ruiz JC, Hernández-Navarro F, Mataix R,
Petit J, Pascual MJ, Rifón J, García-Conde J, Fernández-Rañada JM, Mateos MV, Sierra J, Conde E; GEL/TAMO
Cooperative Group. Autologous stem cell transplantation for primary refractory Hodgkin's disease: results and clinical
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158: Holowiecki J, Giebel S, Wojnar J, Krawczyk-Kulis M, Stella-Holowiecka B, Kachel L, Wojciechowska M,
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162: Bierman PJ, Lynch JC, Bociek RG, Whalen VL, Kessinger A, Vose JM, Armitage JO. The International Prognostic
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Knopińska-Posłuszny W, Nagler A, Meder J, Walewski J, Lampka E, Sułek K, Sawicki W, Lange A, Forgacz K,
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167: Anselmo AP, Cavalieri E, Meloni G, Alimena G, Cantonetti M, Maurizi Enrici R, Tosti ME, Falchetto Osti M,
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173: Josting A, Franklin J, May M, Koch P, Beykirch MK, Heinz J, Rudolph C, Diehl V, Engert A. New prognostic score
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174: Stuart MJ, Chao NS, Horning SJ, Wong RM, Negrin RS, Johnston LJ, Shizuru JA, Long GD, Blume KG, StockerlGoldstein KE. Efficacy and toxicity of a CCNU-containing high-dose chemotherapy regimen followed by autologous
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184: Martín A, Fernández-Jiménez MC, Caballero MD, Canales MA, Pérez-Simón JA, García de Bustos J, Vázquez L,
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ii. At time of SCT
Updated 04/18/2013
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Hodgkin Lymphoma EBR
1: Greaves P, Wilson A, Matthews J, Brown DL, Auer R, Montoto S, Lister TA, Gribben JG. Early relapse and refractory
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X.
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