A review of hematopoietic cell transplantation in China: data and trends during 2008–2016

Abstract

Hematopoietic cell transplantation (HCT) activity in China was surveyed to assess its current status. A record number of HCTs (21 884: 16 631 allogeneic (76%) and 5253 autologous (24%)) were reported by 76 centers in China between 1 January 2008 and 30 June 2016. HCT trends included continued growth in transplant activity, a continued rapid increase in haploidentical donors (HID), and slower growth for unrelated donors, matched-related donors (MRD) and cord blood transplantation (CBT). The proportion of HID HCT among allogeneic HCTs increased from 29.6% (313/1062) in 2008 to 48.8% (1939/3975) in 2015, even 51.7% (1157/2237) in the first half of 2016. During this time frame, the proportion of MRD HCTs among allogeneic HCTs decreased from 48.1% (511/1062) to 33.0% (332/3975). The proportion of unrelated donor HCTs among allogeneic HCTs decreased from 20.4 (216/1062) to 13.6% (540/3975). The proportion of CBTs among allogeneic HCTs was increased from 2.1% (22/1062) to 4.2% (184/3975). HCTs have been increasing continuously for all indications except chronic myelogenous leukemia. Severe aplastic anemia is a common HCT indication among non-malignant diseases in China. The number of cases of allogeneic HCT for this disorder has increased annually, from 59 (5.6%) in 2008 to 569 (14.3%) in 2015, even 334 (14.9%) in the first half year in 2016. This survey clearly shows recent trends for HCTs in China.

Introduction

Hematopoietic cell transplantation (HCT) is a curative treatment for a broad spectrum of hematopoietic diseases including acute and chronic leukemias, myelodysplastic syndromes (MDS), lymphomas, aplastic anemia, immune disorders and other congenital disorders of metabolism.1, 2, 3, 4 International data on HCT activity are collected by a number of registries including the Center for International Blood and Marrow Transplant Research (CIBMTR), the European Group for Blood and Marrow Transplantation (EBMT) and the Asia-Pacific Blood and Marrow Transplantation Group (APBMT).1, 2, 3 The CIBMTR collects HCT data from over 1566 participating centers worldwide.1 The EBMT collects HCT data from more than 550 centers in Europe2 and also runs an annual activity survey.2, 3 The APBMT collects allogeneic HCT data from over 432 participating centers in the Asia–Pacific region.4 Data from these registries indicate that there are regional differences in transplant indications and donor availability.

There is a survey from pediatric patients in China,5 but no nationwide survey of the entire population of transplant patients. The Chinese Blood and Marrow Transplantation Registry Group (CBMTRG) was established in 2007 and collects data every 6 months. In China, increasing numbers of haploidentical donor (HID) HCT are performed. To understand the patient and donor pools, we performed a survey of trends and highlighted differences from Western reports. Our survey of HCT activity in China involves an 8-year period and is based on available databases to provide an overview of the current state of HCT in China.

Materials and methods

Data collection

From January 2008, the Stem Cell Application Section of the Hematology Branch of the Chinese Medical Association organized a nationwide registration of HCT. Participating HCT teams were required to report their data by Excel form to the CBMTRG every 6 months. The data included transplant numbers, disease, patients’ gender and age, conditioning regimen, donor type and stem cell source. This was a retrospective study focusing on data collected from HCT centers in China during the period from January 2008 to June 2016. The teams involved in this study are listed in the Supplementary Appendix in alphabetical order by the name of the hospital.

Results

Numbers of participating teams and transplants

Over the survey period, additional centers joined the CBMTR. There were 27 participating transplant teams in the first half of 2008 and 76 in the first half of 2016. The 76 teams were located in 24 provinces excluding Tibet, Qing Hai province, the Nei Monggol Autonomous Region and Guizhou province. There were significant differences in HCT numbers among the centers. For example, during 2015, 1 center (Peking University People’s Hospital, Peking University Institute of Hematology) undertook 703 HCTs, 1 center (The First Affiliated Hospital of Soochow University) 406, 12 centers 101–300, 22 centers 50–100 and 39 centers under 50. When limited to allogeneic HCTs, 1 center (Peking University People’s Hospital, Peking University Institute of Hematology) undertook 689, 1 center 316, 9 centers 101–300, 15 centers 50–100 and 49 centers <50. HID HCT was reported by 93.4% (71/76) of the centers. Transplants were performed on both adult and pediatric patients in 94% of the centers, and only on pediatric patients in 6% of the centers. The mean HCT activity per team increased from 39 to 69 from 2008 to 2016.

Of the 21 884 HCTs (allogeneic: 16 631 (76%); autologous: 5253 (24%)) performed between 1 January 2008 and 30 June 2016, 39% were female and 61% were male. The numbers of autologous and allogeneic HCTs increased continually during the study period (Figure 1a). Twenty-five centers provided data during the first half year in 2008 and first half year in 2016. These data provided by these 25 centers showed an increase in autologous HCT from 574 to 1664, and allogeneic HCT from 485 to 1394 during this time period.

Figure 1
figure1

HCT in China during 2008–2015. (a) Numbers of HCT patients based on donor type and graft source. (b) Annual trend of donor type for allogeneic HCT. (c) Annual trend of absolute numbers of disease indications for allogeneic HCT. (d) Annual trend of absolute number of HCT for severe aplastic anemia based on donor type.

Autologous HCT trends

The number of autologous HCTs was smaller than the number of allogeneic HCTs, although the relative proportion of autologous HCTs increased (Figure 2a). There were 121 (10.5%) autologous HCTs performed in 2008 and 1142 (24.3%) in 2015 (Figure 1a). Disease indications for autologous HCT were: lymphoma 45%, multiple myeloma 27%, AML 14%, ALL 4% and POEMS syndrome 4% (Figure 2b).

Figure 2
figure2

Proportions of patients in China undergoing HCT during 2008–2015. (a) Proportions of donor types among HCTs. (b) Proportions of disease indications among autologous HCTs. (c) Proportions of disease indications among allogeneic HCTs. (d) Distribution of ages when patients received allogeneic HCT.

Allogeneic HCT trends

Patients’ age and gender

Forty percent of the allogeneic HCT patients were female and 60% were male. The number of pediatric patients (18 years of age) was 4826 (29.0%) and elderly patients (>50 years of age) 916 (5.5%) (Figure 2d). There were 72 patients >60 years of age (0.4%). The ratio of pediatric and elderly patients increased annually (Figure 3).

Figure 3
figure3

Annual trend of relative proportions of patients’ age among allogeneic hematopoietic cell transplants in China during 2008–2016.

Related vs unrelated donors

The total number of allogeneic HCTs increased continually with time. The number and relative proportion of related donors among allogeneic HCT patients exhibited a notable increase. The number of cord blood transplants (CBT) increased. The number and relative proportions of unrelated donor (URD) HCTs had a different trend. The ratios of related donor HCT to URD–HCT/CBT increased from 3.46 (824/238) in 2008 to 4.49 (3251/724) in 2015.

In the latest report, TBI-based conditioning was applied in 11.4% of allogeneic HCT patients, non-TBI conditioning was applied in 89.6%.

Disease indications

HCT centers performed allogeneic HCTs for both malignant and non-malignant diseases. There were more transplants performed for malignant (~82%) compared to non-malignant (~8%) conditions (Figure 2c). The distributions of diseases leading to allogeneic HCT between January 2008 and June 2016 were: AML (34%), ALL (26%), severe aplastic anemia (SAA) (11%), MDS (9%), CML (8%), non-Hodgkin’s lymphoma (3%) and other diseases (2%) (Figure 2c). In the latest registry, among allogeneic HCTs, AML was the most common reason (35%), followed by ALL (25%), MDS (9%) and CML (3%). For non-malignant conditions, allogeneic HCT was performed most for SAA (15%), followed by hemoglobinopathy (4%).

The number of allogeneic HCTs for most types of hematological malignancies, including AML, ALL and MDS, has been increasing. The number of cases of allogeneic HCT for SAA has also increased annually, from 59 cases (5.6%) in 2008 to 569 cases (14.3%) in 2015, and 334 (14.9%) in the first half year of 2016. The relative numbers of allogeneic HCTs for AML, ALL and MDS remained nearly stable over time, whereas the total number increased. However, CML showed a different trend. The number of transplants for CML has decreased since 2012. The absolute number and relative proportion of allogeneic HCTs for CML decreased continuously from 241 cases (22.7%) in 2008 to 166 cases (3.4%) in 2015 (Figure 1c).

Stem cell source: matched-related donor, URD, cord blood and HID

HCT centers carried out allogeneic HCTs from MRD, HID, URD and cord blood. Although the CMDP bank has 2 20 4 432 volunteers, of the 55 106 cases searched up to 30 June 2016, there were only seven bank offers of cord blood to patients. URD and CBT among allogeneic HCT accounted for only about 20% (3591/18 030) (URD 17.3%, CBT 3.7%) of the total transplants. During 2008–2015, 80% of the allogeneic HCTs involved related donors: HID 40.7% (7358/18 030) and MRD 38.3% (7081/18 030) (Figures 1b and 2a). In 2015, there were 2.7% (36/1312) bone marrow (BM), 73.1% (959/1312) PBSC and 24.1% (316/1312) G-CSF-primed BM and PBSC among the MRD HCTs. There were 2.7% (35/1939) BM, 21.3% (413/1939) PBSC and 76.0% (1474/1939) G-CSF-primed BM and PBSC among HID HCT. There was 99.6% (538/540) PBSC among URD-HCT.

The total number of HCTs from HID donors increased during the study period and exceeded the number of HCTs from related donors in 2013 (Figure 1b). The proportion of HID out of the allogeneic HCTs increased continuously from 29.5% (313/1062) to 48.8% (1939/3975) from 2008 to 2015. The first half of 2016 showed a further increase to 51.7% (1157/2237). Conversely, the proportion of MSD cases among allogeneic HCT decreased annually, from 48.1% (95/1062) in 2008 to 33.0% (332/3975) in 2015. The proportion of URDs among allogeneic HCTs decreased slightly from 20.4% (216/1062) to 13.6% (540/3975), and CBT increased from 2.1% (22/1062) to 4.2% (184/3975) (Figure 1c).

The annual proportion of cases of HID allogeneic HCT for SAA, relative to total allogeneic HCT for SAA, has increased rapidly in China, from 32.1% (18 cases) in 2008 to 47.2% (268 cases) in 2015 (Figure 1d). HID HCT for SAA is characterized by a combination of G-CSF-mobilized BM and peripheral blood.

Discussion

This paper reflects current practice and development of HCT in China. Our activity survey shows a continual increase in the use of HCT across China since 2008, with an especially notable increase in HID HCT. We also found that the number of HIDs for SAA increased. There are more allogeneic than autologous HCTs in the database. This is similar to a report from the American Society for Blood and Marrow Transplantation, but differs from reports from EBMT and CIBMTR that found more autologous HCT.1, 2, 3, 4

There are many reasons contributing to the increased number of allogeneic HCTs. One was an increase in the number of reporting teams and mean transplant activity per team (from 39 to 69 HCTs per team). A second reason is expansion of the donor pools because the unrelated volunteer donor bank and cord blood bank were enlarged. The success of HID HCT has brought in a new era of 'everyone has a donor' to the real world. The third reason is that patients eligible for HCT increased because older patients could receive a reduced intensity conditioning regimen and the list of disease indications for HCT increased.

In a consensus statement on allogeneic HCT in China published in 2014, the indications include HID HCT for selected subgroups of low-risk AML in CR1, intermediate-risk AML in CR1, Philadelphia (Ph)+ ALL, adult standard risk ALL-CR1/MDS/CML-AP, as well as high-risk leukemia and CML-BC.6 These indications for HCT differ markedly from those in the National Comprehensive Cancer Network guidelines.7, 8, 9, 10 However, current clinical practice is supported by the results of HID HCT and clinical trials organized by Huang et al. (some trials are listed in Table 1).11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25

Table 1 The clinical outcome of HID HCT and trials comparing HCT with chemotherapy or TKI

The AML patient subgroup classified in the low-risk karyotype by the World Health Organization stratification system, obtained benefit from allogeneic HCT in CR1 status following re-stratification by applying risk-directed therapy based on MRD. In a trial registered at http://www.chictr.org.cn/enIndex.aspx as #ChiCTR-OCH-12002406,13 the high-risk group was defined as those patients not achieving major molecular remission (MMR) after the second consolidation therapy or those exhibiting the loss of MMR within 6 months of achieving MMR. The low-risk group was defined as patients who achieved MMR after the second consolidation therapy and maintained MMR for 6 months. Risk-directed therapy included recommending allogeneic HCT for high-risk patients and chemotherapy/autologous stem cell therapy for low-risk patients. Similar results were observed with inv(16) AML.14 A CBFB–MYH11 level of 0.2% after course 2 consolidation was used to define a poor molecular response. Compared with chemotherapy/autologous stem cell therapy, allogeneic stem cell therapy decreased the 3-year cumulative incidence of relapse and improved the disease-free survival and overall survival of patients with a poor molecular response, but did not improve the outcome of patients with good molecular response. Treatment based on minimal residual disease-directed risk stratification may improve the outcome of t(8;21) AML or inv(16) AML in CR1 and is recommended in practice.13, 14 Adult Ph(−) ALL patients with high- or low-risk can obtain benefit from HID HCT in CR1.16, 17, 18, 19, 20 Thus, Ph(+) ALL remains an important indication for allogeneic HCT in the era of treatment with tyrosine kinase inhibitors. Allogeneic HCT, combined with tyrosine kinase inhibitor maintenance therapy after HCT, can reduce the relapse rate and improve disease-free survival time.21 Overall, allogeneic HCT is recommended for all ALL patients except standard risk pediatric patients.6

There has been a notable decrease in HCT for CML in the chronic phase in Europe since 2000 due to the use of tyrosine kinase inhibitors.26 This trend has been delayed several years in China, as CML was 22.7% among allogeneic HCT in 2008. Tyrosine kinase inhibitors are expensive and need to be given to patients for a long period. The consideration of cost effectiveness between these two highly expensive treatments, and the desire for a cure, affected the trends for HCT.

On the basis of results from a cohort study demonstrating that allogeneic HCT is superior to first- and second-generation tyrosine kinase inhibitors for accelerated phase and blastic crisis patients,22, 23, 24, 25 the consensus statement in China published in 2014 recommends these patients, as well as T315i-mutated patients in the chronic or accelerated phases, receive allogeneic HCT.6 HID HCT is standard care for advanced CML patients in China. Therefore, the overall number of HCTs for CML is stable, whereas the proportion of CML patients receiving allogeneic HCT is decreasing continuously.

Another notable trend is that the number of SAA cases undergoing HCT is growing due to new strategies being developed. HID HCT has been considered a potential option in patients with SAA in the absence of an identical sibling donor or URD.6, 27, 28 The feasibility of HID transplantation was evaluated for treating SAA patients following the failure of previous immunosuppressant therapy in a prospective multicenter clinical trial registered as ChiCTR-ONC-12002107 at http://www.chictr.org.cn/enIndex.aspx.27 HID HCT, as an upfront therapy, was an effective and safe option for SAA patients with favorable outcomes in experienced centers in a registry-based comparison study.28 The consideration of cost effectiveness between these two highly expensive treatments, immunosuppressive therapy and HCT, may have a great effect on the future trends.

An important finding in this study was that there were marked differences in donor and stem cell selections from CIBMTR and EBMT with rapid growth of URD or cord blood PBSCs is a priority. In China, HID is the most rapidly growing donor pool, and G-CSF-primed BM combined with PBSCs is popular for use in HID HCT. HID HCT was studied intensively because of the decreasing family size in China. The optimization of protocols and pre-transplant risk stratification has helped improve the results of HID HCT. In the new era of 'everyone has a donor', we look for the best among many HID candidates. On the basis of a large sample size and relative consistency of transplant variables, Wang et al.29 proposed an algorithm for donor selection. This algorithm ranks haplo donor characteristics in the following order: young, male, non-inherited maternal antigen mismatch. Transplants from older mothers and non-inherited paternal antigen-mismatched donors should be avoided. Recently, the relationship between donor-specific anti-HLA antibodies and primary graft failure after un-manipulated HID HCT was investigated in a prospective randomly assigned training and validation sets study.30 The results suggested that incorporating donor-specific antibodies in the algorithm improved HID selection.30

The increased numbers of allogeneic HCTs using HID reflect the greater availability of donors and the recognition that HID transplantation provides equivalent safety to related donor transplantation and URD in many conditions including AML, ALL, CML, MDS and SAA. The conclusion that HID HCT can give similar clinical outcomes with MRD and URD is supported by a series of comparative studies listed in Table 2.18, 21, 27, 28, 31, 32, 33, 34, 35, 36, 37 The use of HID continues to increase due to its convenience and ready availability without delay. A dramatic increase in the number of HID HCTs performed was observed in 2013, but only a slower increase in MRD, URD and CBT. This was compensated for by an increase in the use of HIDs who are, in some sense, competition for URD and CBT.

Table 2 Clinical results of haploidentical donors and comparisons with matched-related donor, unrelated donor and cord blood transplantation

The current study has some limitations. Primarily, the survey did not include patient demographics or outcomes, and many other factors. Thus, detailed data are not available. Nevertheless, this survey did highlight trends both in HCT activity and registry in China. The results provide reasonably comprehensive information about the current state of HCT in China, and could be the basis for multicenter retrospective studies of HCT practice and outcomes. The survey results also suggest that clinical decisions could be made based on local experience from clinical trials. Further efforts should be made to obtain detailed information from all centers to create a complete data set.

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Acknowledgements

We sincerely thank all participating centers and their staff. All participating teams are listed in the Appendix. This work was supported by the Key Program of the National Natural Science Foundation of China (Grant No. 81230013), the National Natural Science Foundation of China (Grant No. 81400145), Project TG-2015-003 supported by the Health Science Promotion Project of Beijing and the Beijing Talent fund (No. 2015000021223ZK39).

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Correspondence to X-J Huang.

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Xu, LP., Wu, DP., Han, MZ. et al. A review of hematopoietic cell transplantation in China: data and trends during 2008–2016. Bone Marrow Transplant 52, 1512–1518 (2017). https://doi.org/10.1038/bmt.2017.59

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