Long-Term Results of Hematopoietic Cell Transplantation (HCT) for Adults with Blood Disorders- A Systematic Review.

Introduction

Hematopoietic cell transplantation (HCT) is a procedure that transformed the treatment of hematologic malignancies, and severe non-neoplastic disorders of the hematopoietic system. Current indications for this therapy as suggested by the European Society of Blood and Marrow Transplantation (EBMT) and the American Society for Transplantation and Cellular Therapy (ASTCT) include approximately 50 diseases, the majority of which are blood disorders [ 1 , 2 ]. These diseases might be divided into: lymphoid malignancies (62.9% of HCTs), myeloid malignancies (25.6%), and non-malignant diseases of the hematopoietic system (5.9% of HCTs) [ 3 ]. Auto-HCT constitutes approximately 90% of all HCT procedures performed for lymphoid malignancies. Allo-HCT constitutes approximately 90% of all HCT procedures performed for myeloid malignancies and non-malignant disorders of the hematopoietic system [ 3 ]. According to an international registry of over 1.5 million procedures, the numbers of performed matched related donors (MRD) and matched unrelated donors (MUD) allo-HCTs are similar [ 4 ].

Vast majority of studies concerning the effects of HCT concentrate on relatively early survival (1–3 years). The proofs for the long-term efficacy of HCT, measured by OS and PFS, are based on the reports of international registries [ 3 ]. High-quality data on 5-year survival are regularly updated and published by the Center for International Blood and Marrow Transplant Research (CIBMTR) [ 5 ]. Analyses with longer follow-up are limited due to potential organizational and personnel changes in transplantation centers, difficulties in following up the survivors, and the focus on new promising therapies instead. Therefore, gathering data on 10-year, 15-year, or 20-year survival rates is a demanding task.

The data on 5-year and even shorter survival rates might be valuable in the case of novel therapies and rare indications of transplantation. However, as the procedures are around for over 50 years, it would also be important to assess the long-term survival (5, 10, or more years). This review aims to summarize up-to-date knowledge on the long-term results of HCT as an individual method of treatment for various blood disorders, which are approved indications for this therapy [ 1 ].

Methodology

The systematic review was prepared in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines. No original clinical raw data were collected for this study. The following eligibility criteria were used: 1) study types: randomized clinical trials, observational studies (both prospective and retrospective cohort studies), meta-analyses, review articles; 2) patients: adults with blood disorders treated with HCT procedures; 3) inclusion criteria: studies referring to 5-year or longer survival, values of OS and/or PFS (in months, years) and/or survival rates (in %) available to collect or estimate using the Kaplan–Meier curves included in chosen articles; 4) exclusion criteria: studies referring to survival shorter than 5 years, studies referring to pediatric patients, studies assessing the survival other than for blood disorders– data on solid tumors and autoimmune diseases; 5) language of published articles: English; 6) searched databases: PubMed and Google Scholar; 7) publication of articles: up to December 31, 2024.

The searched combinations of keywords consisted of 3 parts: 1) the name/the abbreviation of the disease of the hematopoietic system, 2) the name of the procedure (HCT) and its types (auto-HCT, allo-HCT, tandem transplantation), 3) keywords: “long-term survival”, “long-term outcomes”, “long-term results”. The examples of the searched combinations might include: “DLBCL auto-HCT long-term results”, “severe aplastic anemia allo-HCT long-term survival”, “MM tandem transplantation long-term outcomes”. We used only the combinations of keywords, which were consistent with 2022 EBMT guidelines on HCT indications [ 1 ]. In order to verify the consistency of the data from included articles, we confronted it with 2024 CIBMTR registry analyses.

Out of all 5238 records, 60 papers were included in our study. Comprehensive data regarding literature search is shown in the PRISMA 2020 flow diagram (Fig. 1 ).

The risk of bias was evaluated with the ROBINS-I V2 assessment tool for observational studies and with the ROB 2 assessment tool for randomized clinical trials. Comprehensive data regarding the risk-of-bias evaluation is shown in Fig. 2 .

Autologous Transplantation for Lymphoid Malignancies

Identified data are summarized in Table 1 and described in greater detail below.

Multiple Myeloma (MM) and Other Plasma Cell Dyscrasias

Auto-HCT is a standard of care in patients with newly-diagnosed MM younger than 70 years (biological age is decisive), in those with chemo-sensitive relapse disease, and in those with prior auto-HCT (tandem transplantation available). The procedure is also a clinical option for the patients with chemo-sensitive relapsed Waldenstrőm macroglobulinemia who achieve the second or further CR, and in patients with light-chain amyloidosis (AL) [ 1 , 2 ].

CIBMTR reports a 5-year OS of approximately 75% for MM patients and approximately 85% for AL patients [ 5 ].

The analysis of 4329 MM patients treated with auto-HCT between 1989 and 2018 showed the remarkable improvement of OS and PFS over time. The 5-year OS rates were: 47% for patients who started treatment in 1997 or earlier, 58% for 1998–2003, 62% for 2004–2008, 64% for 2009–2013, and 70% for 2014 or later. Appropriate 5-year PFS rates were: 29%, 50%, 61%, 61%, and 68% [ 6 ]. According to another study performed between 1989 and 2002, 5-year and 10-year OS rates of patients treated with auto-HCT were 46.2% and 30.8%, respectively, while 5-year and 10-year PFS rates were 32.9% and 15.2%, respectively [ 7 ]. According to the analysis of 61 725 patients from the year 2024, median OS and PFS rates were 90.2 months and 36.5 months, respectively. Non-relapse mortality (NRM) did not exceed 1–3% [ 8 ]. Tandem auto-HCT was superior to single auto-HCT in MM patients in terms of OS and PFS [ 9 ]. In the study assessing the long-term outcomes of tandem auto-HCT, the 3-year, 5-year, and 10-year OS rates are 85%, 63%, and 39%, respectively. Appropriate PFS rates were 48%, 32%, 20% [ 10 ]. Myeloablative conditioning with subsequent auto-HCT in patients with AL amyloidosis produced 5-year OS and PFS rates of 57% and 47%, respectively. Notably, the plateau effect, observed beginning from the year 3 after transplantation, was maintained up to 10 years after transplantation. Median PFS is estimated for 32 months [ 11 ]. Another analysis yielded similar results [ 12 ]. In patients with WM transplanted in CR, auto-HCT produced the 5-year OS rate of 65% and 5-year PFS rate of 46%. The results were inferior in patients who did not achieve CR before transplantation: 5-year OS rate of 56% and 5-year PFS rate of 36% [ 13 ].

Hodgkin Lymphoma (HL)

Auto-HCT is the standard of care in patients with chemo-sensitive relapsed HL. It is also a significant clinical option in patients with prior auto-HCT (tandem transplantation available), and in those with a refractory disease [ 1 , 2 ]. The role of auto-HCT in nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) is less well-defined [ 14 ].

CIBMTR reports a 5-year OS rate of approximately 90% for chemo-sensitive disease and approximately 80% for chemo-resistant disease [ 5 ].

In patients with relapsed classic HL, auto-HCT produced 5-year OS and PFS rates of 64% and 45%, respectively. Median PFS was estimated at approximately 3 years, while median OS was not reached [ 15 ]. In the long-term observational study, 10-year OS and PFS rates were 50% and 37%, respectively. Median OS and PFS were 9.0 years and 2.9 years, respectively [ 16 ]. Tandem transplantation performed in poor-risk (R/R) HL patients produced a 10-year OS rate of 47%. Single auto-HCT performed in intermediate-risk patients produced a 10-year OS rate of 70%, better than in undivided groups in other studies [ 17 ]. Auto-HCT used as the first-line treatment did not produce better long-term results compared to chemotherapy alone [ 18 ]. In NLPHL patients, the 5-year OS and PFS rates were 76% and 69%, respectively [ 19 ], or 87% and 67%, respectively [ 20 ].

Diffuse Large B-cell Lymphoma (DLBCL)

Auto-HCT is the standard of care in patients with chemo-sensitive relapsed DLBCL who achieve the second or further CR and in those with primary central nervous system lymphoma (PCNSL). It is also a significant clinical option in patients with intermediate-risk and high-risk disease who achieve CR1 [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with DLBCL.

According to the EBMT 32-year retrospective study, based on 41,148 auto-HCT procedures, 5-year and 10-year OS rates were 61.1% and 52.6%, respectively [ 21 ]. For the recipients who survived at least 2 years from auto-HCT, 5-year OS and PFS rates were estimated at 95% and 82%, respectively [ 22 ]. The divergence of results might be explained by high heterogeneity of DLBCL [ 23 ]. Moreover, while the first analysis included all patients with DLBCL who underwent transplantation in certain period, the second study included only patients who had survived at least 2 years without progression (patients with up-front superior prognosis). According to a single retrospective study, the 5-year OS rate in patients with R/R PCNSL was 62% [ 24 ]. Interestingly, auto-HCT might also provide durable remission in patients with HIV-related lymphomas, as 5-year OS and PFS rates are both 85% [ 25 ].

Follicular Lymphoma (FL)

Auto-HCT is a standard of care in patients with chemo-sensitive relapsed FL who achieved the second or further CR. It remains a clinical option in patients with FL transformed into high-grade lymphoma [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 75% for chemo-sensitive disease and approximately 55% for chemo-resistant disease [ 5 ].

Auto-HCT produced the 5-year OS and PFS rates of 78% and 60%, respectively, in patients transplanted in CR1 [ 26 ]. The results were not different for chemotherapy alone used as consolidation [ 26 , 27 ]. On the other hand, 5-year OS and PFS rates were worse in patients with R/R FL: 62% and 43%, respectively. After 10-years, survival rates were 52% and 31%, respectively [ 26 ].

T-cell Lymphomas

Auto-HCT is a clinical option in patients with peripheral T-cell lymphoma (PTCL) who achieve CR1 or in those with chemo-sensitive relapsed disease who achieve the second or further CR [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with T-cell lymphomas [ 5 ].

Available 5-year OS rates range between 37 and 87%, depending on the proportion of patients who achieved CR before transplantation [ 28 ]. In R/R PTCL patients, auto-HCT produced the 5-year OS rate of 53% and 5-year PFS rate of 40% [ 29 ]. Interestingly, in patients with anaplastic large T-cell lymphomas (ALCL), auto-HCT as front-line therapy produced 5-year OS and PFS rates of 90%, without regard to the expression of ALK kinase. Such results would imply significantly better survival than in patients with other NHLs or HL. However, the study included only 15 procedures [ 30 ].

Mantle Cell Lymphoma (MCL)

Auto-HCT is the standard of care in MCL patients who achieve CR1. It is also a significant clinical option in patients who achieve the second or further complete or partial remission (CR/PR) [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with MCL [ 5 ].

In patients who achieve CR1, if the procedure was performed early (no more than 2 lines of chemotherapy), auto-HCT produced 5-year OS rate of 61%. For the remaining patients (late procedure), it was estimated at 44%. In these cohort, 5-year PFS rates were approximated at 50% and 30%, respectively [ 31 ]. In patients with R/R disease, auto-HCT produced 5-year OS and PFS rates of only 42% and 31%, respectively. Median OS and PFS are approximately 4 and 3 years, respectively [ 32 ].

Autologous Transplantation for Myeloid Malignancies

Identified data are summarized in Table 1 and described in greater detail below.

Acute myeloid Leukemia (AML)

Auto-HCT is a clinical option in patients with favourable-risk disease and minimal residual disease who achieve CR1, in those with intermediate-risk disease who achieve CR1, and in those who achieved CR2 [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with AML [ 5 ].

In patients who achieved CR1, auto-HCT produced 5-year OS and PFS rates of 36,2% and 26,6%, respectively [ 33 ]. In R/R AML, auto-HCT produced 5-year OS and PFS rates of 32% and 30%, respectively. Notably, plateau effect was maintained after 10 years from transplantation. After 10-years, NRM was only 14%. The results were significantly better for the patients with R/R acute promyelocytic leukemia, namely 5-year OS rate of 66% [ 34 ].

Myelodysplastic Syndromes (MDS)

Auto-HCT remains a clinical option in patients with intermediate-risk disease without additional factors [ 1 , 2 ]. However, the procedure is rarely used in practice, mainly for young patients who lack suitable donor [ 35 ].

Current CIBMTR reports do not include long-term outcomes for the patents with MDS [ 5 ].

The procedure produced 5-year OS rate of approximately 45% in patients with low-risk and intermediate-risk disease, and approximately 15% in patients with high-risk disease [ 36 ].

Chronic Myeloid Leukemia (CML)

Auto-HCT is generally not recommended anymore in patients with CML [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with CML [ 5 ].

Auto-HCT used as a consolidation after treatment with interferon-α produced 5-year OS rate of approximately 70% in newly diagnosed CML patients. The result was not different for monotherapy with interferon-α [ 37 ].

Allogeneic Transplantation for Lymphoid Malignancies

Identified data are summarized in Table 2 and described in greater detail below.

Multiple Myeloma (MM) and Other Plasma Cell Dyscrasias

Allo-HCT is a standard of care in MM patients with upfront high-risk disease. It remains a significant clinical option in patients with upfront standard risk, in those with chemo-sensitive relapsed MM, and in those after prior auto-HCT. Moreover, the procedure is a clinical option in patients with poor-risk WM, AL [ 1 , 2 ], and plasma cell leukemia [ 38 ].

Current CIBMTR reports do not include long-term outcomes for allo-HCT in patents with MM and other plasma cell dyscrasias [ 5 ].

In the prospective study of patients who received allo-HCT as the first option, the 5-year and 10-year OS rates were 48,1% and 39.9%, respectively, and the 5-year and 10-year PFS rates were 33.3% and 31.4%, respectively. Median OS and PFS were approximately 3.5 years and 2 years, respectively [ 7 ]. The graft-versus-myeloma effect, which might be considered the main advantage of allo-HCT compared to auto-HCT, was not significant enough to overcome the disadvantages of allo-HCT, such as GvHD occurrence and high TRM rate [ 39 ]. In addition, in some studies investigating long-term outcomes of allo-HCT, the plateau effect in PFS was not observed [ 7 ]. Even if observed, it was associated with high TRM (16%) and high chronic GvHD incidence (66%), which deteriorated survival and quality of life [ 40 ]. In patients with WM, allo-HCT produced the results similar to auto-HCT. However, allo-HCT is associated with 30% NRM and, hence, remains even further clinical option [ 13 ].

Hodgkin Lymphoma (HL)

Allo-HCT is a standard of care in patients with chemo-sensitive relapsed HL after the failure of auto-HCT [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 70% in chemo-sensitive disease and approximately 55% in chemo-resistant disease [ 5 ].

According to the EBMT study, allo-HCT after RIC did not produce promising results in HL patients, as 5-year OS and PFS are only 43% and 24%, respectively. Median OS and PFS did not exceed 1 year [ 41 ]. Transplantation from haploidentical donors preceded by non-myeloablative conditioning produced 5-year survival rates similar to transplantations from MRD and MUD. Interestingly, after 2 years from allo-HCT the outcomes for haploidentical donors remained significantly better [ 42 ].

Diffuse Large B-cell Lymphoma (DLBCL)

Allo-HCT is a clinical option in patients with chemo-sensitive relapsed DLBCL who achieve the second or further CR, in chemo-sensitive relapsed disease after the failure of auto-HCT and in refractory disease [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with DLBCL [ 5 ].

Allo-HCT produced 5-year and 10-year OS rates of 37.8% and 30.6%, respectively, while 5-year and 10-year PFS rates were 31.4% and 24.7%, respectively. The results are similar for recipients of MRD, MUD and haploidentical transplantations [ 21 ]. In another multicenter study, which includes the patients without regard to remission status, 4-year OS and PFS rates were estimated to be only 23% and 20%, respectively. Median PFS and OS did not exceed 1 year. For patients who remained in remission before transplantation, 4-year OS and PFS rates were determined to reach 46.2% and 43.0%, respectively [ 43 ]. Notably, long-term results of allo-HCT were significantly better for de novo DLBCL patients in comparison with the transformed lymphoma group (5-year PFS of 55% vs. 28%). The plateau effect was observed only in de novo lymphoma group from 2 years after transplantation, and maintained after 15 years from transplantation [ 44 ]. The EBMT study which compared auto-HCT and MRD allo-HCT exclusively, showed a superior 5-year survival rate for the auto-HCT group and a similar relapse rate in both groups [ 45 ]. Therefore, despite higher mortality rates, allo-HCT remains a significant clinical option with potential to provide durable remissions in patients with refractory disease or those who experienced a relapse after prior auto-HCT [ 46 ].

Follicular Lymphoma (FL)

Allo-HCT is the standard of care in patients with FL who achieve the second or further CR after auto-HCT failure. It remains a significant clinical option in patients with chemo-sensitive relapsed FL who achieve the second or further CR and in refractory FL [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 70–75%, similar for both chemo-sensitive and chemo-resistant disease [ 5 ].

Allo-HCT produced 5-year OS and PFS rates both of 58% in patients with grade I-II FL and of 54% and 51%, respectively, in patients with grade III FL [ 47 ]. In most studies, survival curves reached a plateau in long-term observation, probably due to the crucial role of the graft-versus-lymphoma effect in FL. According to the EBMT study comparing the first transplantation after FL relapse, auto-HCT was associated with more relapses than allo-HCT. However, there were no differences in 5-year survival rates [ 48 ]. The other study showed a superior 5-year OS rate in auto-HCT cohort compared to allo-HCT cohort (74% to 66%) [ 49 ].

T-cell Lymphomas

Allo-HCT is the standard of care in chemo-sensitive PTCL patients who achieve the second or further CR. The procedure remains a clinical option in patients with PTCL who achieve CR1, refractory PTCL and cutaneous T-cell lymphoma (CTCL) in advanced stages (IIB to IV) [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with T-cell lymphomas [ 5 ].

In R/R PTCL patients, allo-HCT produces long-term results similar to auto-HCT, as 5-year OS rate is 54%, and 5-year PFS rate is 48%. Considering the efficacy and safety of both procedures, it is unknown which one is more beneficial [ 29 ]. In CTCL patients, the procedure produces a 4-year OS and PFS rate of 51% and 26%, respectively. Notably, PFS is significantly higher in patients with Sézary syndrome in comparison to mycosis fungoides (72.7% vs 11.5%). The plateau effect is still observable after 10 years after transplantation due to persistent graft-versus-lymphoma effect in CTCL. Similar OS is observed in both diseases. Median OS and PFS are approximately 4 years and 6 months, respectively [ 50 ].

Mantle Cell Lymphoma (MCL)

Allo-HCT remains a clinical option in patients with relapsed MCL who achieve the second or further complete or partial remission (CR/PR) or in patients with refractory disease [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with MCL [ 5 ].

Allo-HCT produced 5-year OS and PFS rates of approximately 50%. However, reported TRM rate was 29% after 1 year from transplantation [ 30 ]. Other study yielded similar results, with 5-year OS and PFS rates being 54% and 49%, respectively [ 51 ]. However, it is worth mentioning that allo-HCT is the only method with the potential to cure R/R MCL, which enables obtaining durable remissions in at least 20–30% of patients [ 52 ].

Acute Lymphoblastic Leukemia (ALL)

Allo-HCT is the standard of care in ALL patients who achieve CR2, patients in CR1 with Ph + ALL or high-risk Ph- ALL. It remains a significant clinical option in refractory ALL and patients who achieve CR1 with standard-risk Ph- ALL with positive minimal residual disease [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 60–65% for patients in CR1, similar for MRD, MUD and haploidentical donors. For the patients in CR2, the 5-year OS rate is approximately 45–50% and for R/R or never in CR patients the 5-year OS rate is 35–40% [ 5 ].

The results remain consistent with another study of Ph- CR1 patients, where 5-year OS rate is estimated at 58.3% for both MUD and MSD transplantations. The plateau effect is maintained after 10 years from transplantation. However, the survival is heavily influenced by the patients’ age, as it differs up to 20% between patients aged 15–25 years and aged 46–55 years. This topic should be examined more profoundly, because this analysis includes patients not older than 55 years, which is a crucial limitation [ 53 ]. The analysis of 7 independent studies with a follow-up ranging between 8 and 12 years estimated 5-year OS and PFS rates at 43% and 42% for MUD transplantation, respectively. Therefore, such treatment was proven a non-inferior option to MSD transplantation, which produced a 5-year OS and PFS rate of 43% and 37%, respectively [ 54 ]. Interestingly, a study with an exceptionally long follow-up showed that transplantations from MUD could be associated with significantly higher 15-year PFS rate (63.2% vs. 28.2%, p = 0.03) and lower relapse rate (30.2% vs. 64.3%; p = 0.03) compared to MSD. Interestingly, median PFS in MRD cohort was approximately 1 year, while in MUD cohort it was not reached during the 15-year observation [ 55 ].

Chronic Lymphocytic Leukemia (CLL)

Allo-HCT is a clinical option in patients with poor-risk R/R disease. It is also a standard of care in patients with Richter’s transformation [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with CLL [ 5 ].

According to EBMT study of 2589 allo-HCT recipients from the years 2000–2010, the procedure produced 5-year OS and PFS rates of 45% and 35%, respectively, and 10-year OS and PFS rates of 35% and 28%, respectively. A plateau was not reached during 10-year observation, and 5-year NRM was high– 36% [ 56 ]. Latter studies yielded slightly better results, namely 5-year OS and PFS rates of 50% and 39%, respectively. For another cohort with smaller ratio of patients with refractory disease, the results were 63% and 43%, respectively. Lower 5-year NRM of 16–23% was reported [ 57 ].

Allogeneic Transplantation for Myeloid Malignancies

Identified data are summarized in Table 2 and described in greater detail below.

Acute Myeloid Leukemia (AML)

The procedure is the standard of care in patients with intermediate and adverse risk who achieve CR1, and in all patients who achieve CR2. It is also a significant clinical option in R/R AML, and in patients with favorable risk and persisted minimal residual disease [ 1 , 2 ]. The disease is the most common indication of allo-HCT in general [ 58 ].

CIBMTR reports a 5-year OS rate of approximately 50–55% for the patients who achieved CR1, similar for MRD, MUD, mMUD and haploidentical donors. The results achieved by the patients with CR2 did not differ significantly. In patients with R/R AML or never in CR, the procedure produced 5-year OS rate of approximately 30% for all donor types [ 5 ].

According to the phase III clinical trial of the patients < 60 years of age who achieved CR1, the results are even better, as 10-year OS rate is approximately 65%. In this particular study, the conditioning regimens are carefully adjusted, as the patients aged < 50 years receive myeloablative conditioning and the patients aged 50–60 years receive RIC [ 59 ]. In refractory AML, allo-HCT produced 10-year PFS rate of 23%. However, median PFS in this study did not exceed 1 year [ 60 ]. In patients with relapsed AML this treatment option led to a median survival of 20.4 months with a 5-year OS rate of 39.3%. Notably, the OS after the procedure is durable for over 10 years [ 61 ].

Chronic Myeloid Leukemia (CML)

Allo-HCT is the standard of care after the failure of at least two lines of tyrosine kinase inhibitors (TKI) treatment in the chronic phase, or in patients in accelerated or blast phase [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with CML [ 5 ].

A multicenter analysis covering 13,416 CML patients, who accounted for over 90% of HCT recipients with CML in Europe between 1980 and 2003, enabled the assessment of long-term outcomes with a follow-up time ranging from 2 to 20 years. The OS of these patients has improved remarkably over the years. The 2-year OS rate reached 53% in 1980–1990, 59% in 1991–1999, and 63% in 2000–2003. The most remarkable reduction of TRM was observed in patients undergoing transplantation from MUD and those who had low-risk disease before the procedure. For the patients who underwent this procedure in 1980–1990, the 20-year OS rate was 34%. The cumulative TRM rate and relapse rate at 20 years were 47% and 26%, respectively [ 62 ]. Similar outcome trends have been reported in a study covering 1955 allo-HCTs performed in Japanese CML patients in 2000–2018. During this time, a 5-year OS rate significantly increased, from 46% (2000–2004 cohort) to 66% (2013–2018 cohort), which was the biggest reported difference out of all malignancies of the hematopoietic system [ 63 ].

Other Myeloproliferative Malignancies

Allo-HCT is the standard of care in patients with intermediate II or high-risk primary myelofibrosis [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 60% for MRD and approximately 50% for MUD transplants. For other myeloproliferative neoplasms, the procedure produces similar 5-year OS rate of approximately 50% for both donor types [ 5 ].

Another long-term analysis proves similar outcomes for MRDs and MUDs. Based on the results of a study including 56 patients (with primary myelofibrosis or myelofibrosis secondary to polycythemia vera or essential thrombocythemia), the 3-year OS rate is 58%. Notably, the plateau effect maintains up to after 10 years from transplantation and median PFS is not reached [ 64 ].

Myelodysplastic Syndromes (MDS)

Allo-HCT remains the standard of care for the patients with intermediate-risk with additional factors, high-risk and very high-risk MDS. It is also a significant clinical option in patients with intermediate-risk without additional factors and in low-risk and very low-risk patients [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 40–45%. The results are similar for all donor types and the disease stage (early vs. advanced disease) [ 5 ].

Other study with long follow-up has shown that allo-HCT produced higher 3-year OS rate in MUD transplant recipients (42.3%) compared to MRD (26.7%) and haploidentical donors (19.8%) with the same trend for the 3-year PFS rate (40.1%, 21.2% and 20.0%, respectively). Notably, after 2–3 years from transplantation, the Kaplan–Meier curves reach a plateau, which is maintained for up to 10 years [ 65 ].

Chronic Myelomonocytic Leukemia (CMML)

Allo-HCT is a standard of care for the patients with myeloproliferative CMML or CMML-2, and patients with CMML-1 or CMML-0 with additional risk factors [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with CMML [ 5 ].

Without regard to CMML staging, allo-HCT produced 5-year OS and PFS rates of 50% and 43%, respectively, and 10-year OS and PFS rates of 40% and 32%, respectively. The plateau effect was maintained up to 15–20 years from transplantation. However, statistically significant survival benefit compared to a cohort treated with methods other than allo-HCT, was observed only for the patients with higher-risk disease [ 66 ]. Other study even confirmed, that allo-HCT improved OS in patients with higher-risk CMML and reduced OS in patients with lower-risk CMML compared to other therapies. Reported 5-year OS rates were 42% and 27%, respectively [ 67 ].

Allogeneic Transplantation for Non-Malignant Diseases of the Hematopoietic System

Identified data are summarized in Table 2 and described in greater detail below.

Severe Aplastic Anemia (SAA)

Allo-HCT from MRD remains the standard of care in patients with acquired and constitutional SAA. The transplantations from MUD, mMUD and haploidentical donors remain significant clinical options [ 1 , 2 ].

CIBMTR reports a 5-year OS rate of approximately 90% for MRD and MUD transplantations and approximately 80% for mMUD and haploidentical transplantations [ 5 ].

In comparison to immunosuppressive therapy (cyclosporine, anti-thymocyte globulin, cyclophosphamide), allo-HCT produces a significantly better 10-year OS rate (97% vs 54%, p = 0.004), and 10-year “failure-free survival” (FFS) rate (97% vs. 40%, p = 0.0001). Failure is defined as death or transplant rejection in the HCT cohort and as death or the necessity to perform HCT in the immunosuppressive therapy cohort [ 68 ]. In another, more up-to-date trial, the cohorts does not differ significantly in terms of 10-year OS rate (92% vs 88%) and the difference is still not observable after 15 and 20 years of follow-up. However, allo-HCT produces a significantly better 10-year FFS rate than immunosuppressive therapy (87% vs. 56%, p < 0.0001). The difference remains observable after 15 and 20 years of observation [ 69 ]. The differences in results between these studies suggest that although the efficacy of immunosuppressive therapy has improved throughout the years, allo-HCT should still be considered the standard of care. However, it is worth mentioning that the procedure is not that beneficial in patients aged > 40 years, as 5-year OS rates are estimated at 67%, 58%, and 45% in patients aged 40–49, 50–59, and > = 60 years, respectively. Notably, the prognosis did not improve for patients aged over 40 in recent years [ 70 ].

Paroxysmal Nocturnal Hemoglobinuria (PNH)

Allo-HCT is the standard of care in severe PNH, similarly to SAA. However it is generally not recommended in hemolytic PNH [ 1 , 2 ].

Current CIBMTR reports do not include long-term outcomes for the patents with PNH [ 5 ].

Allo-HCT produced a 3-year OS rate of 100% in patients with classic PNH and 85,5% in patients with PNH with aplastic anemia. The plateau effect was maintained for classic PNH after 10 years of observation. Moreover, none of the patients with classic PNH developed GvHD within 10 years [ 71 ]. According to another study, the 5-year OS rate in PNH patients was 74% and the plateau effect was still observable up to 15 years after transplantation. Notably, the prognosis was significantly better (approximately 90–95%) for patients aged < 30 years at transplantation and those requiring < 20 pre-transplant transfusions of packed red cells [ 72 ]. Although allo-HCT remains the only method with the potential to cure PNH, it is not recommended as a first-line therapy due to its significant toxicity. If possible, monoclonal antibodies targeted at complement factors should be used as front-line therapy [ 73 ].

Discussion

Analyses of long-term efficacy of medical procedures have the drawback of concerning technical versions of procedures, that were used long time ago, and might have been replaced by versions producing better results. However, this simultaneously means that these long-term results, when applied to currently used technical versions, would not be worse. While the ultimate goal for any therapeutic method used for deadly disease is to achieve survival of affected patients being not different from the normal population, this is probably not achievable with HCT in vast majority of indications. However, particularly in the years when the analyzed procedures were performed (5, 10, 15, 20 years ago) they represented the main method of achieving long-term survival, at least in proportion of patients. In more recent years the situation gradually began to change with the introduction of novel treatment modalities, such as targeted drugs, monoclonal antibodies (first naked, then armed), and also bifunctional antibodies [ 74 ], and more recently CAR-T cells [ 75 ]. They may change the treatment landscape in two ways: they may either completely replace transplantation in some indications and some cases, or they may be incorporated into the treatment paradigm together with transplantation improving its overall efficacy. For all these situations, the current review aimed in providing the reference how to judge the effects in the long-term perspective. For instance, TKIs have eliminated allogeneic transplantation from use in majority of CML cases, so this is an example of situation of the first type. On the other hand, targeted drugs in AML have only been added to earlier used therapies transplantation included. This is an example of the second possibility, which would probably occur more commonly. Therefore, similar analyses carried out in future in majority of cases would not evaluate the effects of transplantation as such on long-term survival, but transplantation used in combination with or followed by other novel therapies applied as maintenance or as effective treatment in relapsed cases. It would be interesting to see whether in the future transplantation will still be used as salvage therapy in cases resistant/refractory to novel therapies. However, it is highly unlikely that in the foreseen future HCT will be completely abandoned by novel more effective and less toxic therapies.

So far these novel therapies rather add to currently available treatments particularly in cases with disease refractory to earlier therapies. However, in some cases they have already become treatment option prior transplantation. This includes CAR-T cells in ALL and DLBCL.

Long-term results of hematopoietic transplantation cannot be interpreted without considering survivals produced using other treatment methods in similar clinical situations [ 76 – 83 ]. For novel targeted therapies such results are often not available yet, due to relatively recent approval. The examples are shown in Table 3 .

Furthermore, apart from HCT procedures, post-transplantation management keeps evolving, especially regarding maintenance therapies. The examples include: lenalidomide [ 84 ], bortezomib [ 85 ], carfilzomib [ 86 ], ixazomib [ 87 ], and daratumumab [ 88 ] in MM; sorafenib [ 89 ], gilteritinib [ 90 ], and quizartinib [ 91 ] in FLT3 + AML. However, randomized clinical trials focus mainly on comparing different types of maintenance therapies, rather than comparing patients with and without maintenance therapy administered after HCT. Moreover, for most of these therapies, it is still too early to assess their influence on survival longer than 5 years. For sorafenib in FLT3 + AML, maintenance therapy was proven to increase 5-year OS rate (~ 80% vs. ~ 50%) and 5-year PFS rate (~ 70% vs. ~ 40%) compared to placebo group [ 89 ]. On the other hand, no statistically significant differences in 5-year survivals were observed in patients treated with quizartinib as maintenance therapy in allo-HCT recipients [ 91 ]. Due to rapid development of novel maintenance strategies [ 92 ], the near future is expected to yield other promising agents.

Despite the rapid development of novel treatment strategies in malignancies of the hematopoietic system, HCT remains a significant clinical option. Moreover, it is often considered a standard of care and remains the only treatment method with the potential to cure in certain situations, such as acute leukemias or SAA, as examples [ 1 , 2 , 93 ]. Moreover, it appears that the procedure’s long-term efficacy has not reached its maximum level yet. There is still an ability to optimize selection of donors, conditioning regimens, and to improve post-transplant care to reduce TRM and NRM as well as develop maintenance therapies [ 74 ].

No matter in which indication HCT has been used, it is obvious that its long-term results have improved throughout the years. It is expected that both auto-HCT and allo-HCT will still have an important role in treating blood diseases until 2050 [ 93 ]. However, the procedure’s characteristics will certainly evolve, and it will hopefully become more complex, individualized, and efficient [ 74 ]. After all, the long-term survival of transplantation recipients depends not only on hematological practice and research progress [ 94 ], but also on an interdisciplinary approach and overall development in medicine.

Limitations

Post-2010 studies were preferable in our analysis. However, pre-2010 studies have also been included. No publication date or data collection period restrictions were used. As the topic of our study implies the assessment of long-term follow-up, the only possibility is to include data collected many years ago. Moreover, HCT procedures have evolved throughout the years, and their role was more significant before the year 2010 for some diseases, for example, due to inaccessibility to novel therapies or even lack of alternative treatment methods. Sometimes, the application of HCT is limited to rare cases nowadays, unlike in the 2000’s and the 1990’s, when analyses of the longest available follow-ups were performed. For example, allo-HCT in CML is currently limited to patients refractory to numerous TKIs. A study including 20-year results [ 62 ] was published in 2000, where TKIs were not a standard of care and CML had limited options other than allo-HCT. Naturally, such a long follow-up required analyzing transplants from the 1990’s and even the 1980’s. The articles with data collected from the 2000’s and the 1990’s transplants might include significant, yet not up-to-date data. Therefore, these results should be regarded more carefully, as for current patients, long-term outcomes are probably even higher. Moreover, the results from older studies might be confronted with newer studies and confirm the prognosis improvement in HCT recipients over the years.

The other potentially confounding factor is the variability of study designs, for example, including both prospective and retrospective cohort studies. However, every study included a defined intervention– HCT procedure, not defined outcomes. Therefore, our systematic review does not technically include classic retrospective studies, but rather prospective studies based on historical cohorts. Moreover, most of registries included all HCT recipients in certain period of time, while prospective studies often had more precise inclusion criteria. It had potential impact on divergence of long-term results.

Lastly, our study relied heavily on registry data, which contain mostly heterogeneous cohorts with the same indication of transplantation. Little is still known about long-term survival within subgroups regarding minimal residual disease status, patients’ comorbidities, and genetic background. For example, the current genetic classification of AML includes numerous mutations which impact prognosis, including long-term survival after HCT [ 95 ]. Rare consideration of patients’ heterogeneity significantly impacts the divergence between included studies and registry data, for example, in FL and DLBCL. On the other hand, data inclusion periods for numerous studies occur at times when the understanding of the mentioned problems was poorer. “Personalized” long-term survival analyses are necessary to better define a relevant place for HCT procedures in the future.

Authors’ Contributions

Study concept and design– Wiesław Wiktor Jędrzejczak, Kajetan Karaszewski; literature search and data analysis– Kajetan Karaszewski, Jakub Góra, Weronika Ploch; critical revision– Wiesław Wiktor Jędrzejczak, Kajetan Karaszewski. All authors read and approved the final manuscript.

Funding

The authors did not receive support from any organization for the submitted work.

Data Availability

All articles cited in this article are available to the readers via scientific databases: Pubmed and/or Google Scholar.

Code Availability

Not applicable.

Declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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