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Introduction

Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis [1-4]. Historically, the best outcomes of allo-HSCT were obtained in cases when a donor was an HLA-matched sibling [5]. The probability of having an HLA-matched sibling donor is approximately thirty percent [6]. For patients who lack an HLA-matched sibling, alternative sources of donor grafts can be found in suitable HLA-matched adult unrelated donors (MUD), unrelated umbilical cord blood (UCB) donors, and partially HLA-mismatched-unrelated donors (mMUD) or HLA-haploidentical related donors (haplo-HSCT) [1, 8]. Despite the increasing number of volunteers in unrelated donor registries, the likelihood of finding a suitable matched unrelated donor is modest [6, 7]. However, haploidentical donor can be found for nearly every patient. The use of haploidentical donors is not limited by racial/ethnic HLA diversity or unusual HLA phenotypes due to mixed racial ancestry [6]. The benefits of haplo-HSCT include immediate donor availability for patients who need the transplant as soon as possible. Besides, post-transplant donor-derived cellular therapy is more easily accessible with the use of a related donor. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. However, this method was historically associated with poor engraftment, high risk of early death, and severe graft-versus-host disease (GVHD).

Earlier attempts at using unmanipulated haploidentical transplant were associated with an unacceptably high rate of GVHD related mortality. Several strategies have been evolved over the past decade to avoid these disadvantages. The advent of T-cell depleted haplo-SCT has allowed better control of the severe GVHD risk [9]. However, this approach was associated with a high rate of graft failure due to host T-lymphocytes that survived the conditioning regimen [10-12]. Later studies have shown that murine and human hematopoietic stem cells have veto cell activity and infusion of a large number of donor hematopoietic stem cells can overcome the MHC barrier and promote engraftment [13-15]. Megadose human CD34+ stem cells (on average >10×10⁶ CD34+ cells/kg body weight) with minimal T cell contamination (a median of 1×10⁴/kg weight) have been successfully used in haploidentical transplantation, which results in high-level engraftment of MHC disparate stem cells. The use of intensive conditioning without additional GVHD prophylaxis led to the result that nearly 80% of patients achieved primary engraftment and only 18% of the patients developed grade II-IV acute GVHD [16, 17]. The major disadvantages of T-cell depleted grafts are both high rate of relapse and nonrelapse mortality (NRM) due to slow immune reconstitution and, thus, infectious complications [18].

Another method to manipulate the T-cell depleted graft is co-infusion of donor-derived regulatory T-cells (Tregs). CD4+CD25+ regulatory T-cells have been shown to suppress proliferative responses of CD4+CD25− T-cells to allo-antigenic stimulation in vitro and are required for ex vivo tolerization of donor T-cells, which results in their reduced potential to induce aGVHD [19, 20]. Despite promising results, this approach is costly and technically demanding, which limits its application to experienced centers.

Another innovative approach is to selectively deplete T-cells responsible for GVHD (TCR alpha-beta) while sparing gamma-delta T-cells (γδ T-cells). Gamma-delta T-cells account for 1% to 10% of peripheral T-cells and have MHC-unrestricted innate cytotoxic activity against tumor cells [21-23]. The use of TCRαβ/CD19-depleted stem cells essentially accelerated immune recovery.

A more recent strategy is to selectively deplete naive T-cells to separate GVHD and the GVL effect. Naive T-cells with CD45RA expression demonstrate to be the most allo-reactive among the T-cell subsets. Ex vivo depletion of CD45RA T-cells and adoptive transfer of CD45RA-memory T-cells accelerate the immune reconstitution, increase the GVL effect while abrogating GVHD [24].

A group of Chinese researchers used a method based on G-CSF-stimulation of the donor, intensified immunosuppression, antithymocyte globulin as in vivo T-cell depletion, and combination of peripheral blood stem cell and bone marrow allografts. Despite satisfactory relapse-free survival rates, acceptable NRM and engraftment, relatively high incidence of severe acute and chronic GVHD was observed. In addition, the standard-risk patients often suffered with opportunistic infections [25, 26].

Trying to improve these results, Italian research team modified this approach through using only BM allografts and adding basiliximab which allowed them to achieve a lower rate of chronic GVHD that included both forms, limited and extensive [27].
Another approach to allo-HSCT was developed in Baltimore (USA) based on non-manipulated graft followed by post-transplant cyclophosphamide injection (PtCy) [28, 29]. This approach has overcome most obstacles historically connected with haplo-HSCT. Thus, recent changes in haplo- HSCT methodology have allowed to improve its results.

The aim of this study was to compare the efficiency of various haplo-HSCT approaches used in our HSCT center.

Patients and methods

The study included 119 patients transplanted from a haploidentical donor (haplo-HSCT) between 2006 and 2018 at the R. M. Gorbacheva Institute of Children Oncology (CIC 725). Their clinical parameters are shown in Table 1. Nine patients received second haplo-HSCT, due to graft failure in 8 cases and relapse in one patient. Eight patients were transplanted from the same donor and one patient from the other donor. Median age was 26 years (18-63), 61 patients were males (51%). Most frequent diagnosis in transplanted patients was acute leukemia (77%, n=92). Primary diagnoses were ALL (31%, n=37), AML (45%, n=53), ABL (2%, n=2), myeloproliferative neoplasms (8%, n=9), lymphoproliferative disorders (13%, n=16), severe aplastic anemia (1%, n=2). Median follow-up was 371 days (1-2219). A total of 46 patients with acute leukemia (38%) had complete remission at the time of HSCT (the first complete remission – 80%, n=37, the 2d or greater remission – 20%, n=9), 33% patients (n=30) had relapse, 15% patients (n=14) had refractory disease. Thus, 67 (56%) patients in the general group received haplo-HSCT as salvage therapy. Non-myeloablative, or reduced-intensity conditioning (RIC) was employed in 81% (n=96) and the myeloablative treatment (MAC) was used in 19% (n=23). Seventy-seven patients (65%) received busulfan, 14 patients (12%), melphalan, and 28 patients (23%) were administered other alkylating agents. Bone marrow was the graft source for 61% patients (n=73), peripheral blood (PBSC) – 39% patients (n=46). Mean transplant CD34+cell and CD3+cell dose was 5×10⁶/kg (1.5-10) and 10×10⁷/kg (2-44) respectively for bone marrow as a graft source, whereas it was 5.1×10⁶/kg (1-16.6) and 10×10⁷/kg (3-47) respectively for recipients who received PBSC as a source of graft.

GVHD prophylaxis based on рost-transplant cyclophosphamide (PTCY-based GVHD prophylaxis) 50 mg/kg at day+3, +4 was employed in 78 patients (66%), also these recipients received tacrolimus 0.03 mg/kg/day and MMF 30-45 mg/kg starting from day +5. Eleven patients (9%) received a T-cell manipulated transplant. The protocol of depletion and HSCT included conditioning according to the GIAC protocol, depleted PBSC in combination with native BM and ATGAM, tacrolimus, MMF.

A total of 30 patients (25%) received GVHD prophylaxis with ATGAM- 31 (26%) and alemtuzumab in 5 patients (4%). Tacrolimus was used for GVHD prophylaxis in 93 patients (72%), cyclosporin A – in 18 patients (14%). Clinical characteristics of the study group are presented in Table 1.

Table 1. Clinical characteristics of the study group

Clinical diagnosis of acute (aGVHD) and chronic GVHD (cGVHD) was based on standard criteria and confirmed by histological analysis of skin and/or rectal biopsy specimens. First-line and second-line therapy for GVHD was provided according to institutional protocols. For statistical evaluation, SPSS Statistics v.17 was used. Two-year time frame was selected for all outcomes. In the group description overall survival (OS), event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) were calculated using Kaplan-Meier methodology.

The comparisons were made using the log-rank test. The difference levels of p<0.05 were considered significant. Cumulative incidence analysis was used for aGVHD, cGVHD, relapse incidence and NRM. The comparisons were made using Gray test. The parameters with p.value <0.1 were selected for further Fyne-Gray regression analysis.

Results

Hematopoietic recovery

Stem cell engraftment after haplo-HSCT was documented in 61% of total group of patients (n=72). CD34+cell level less than 3×106/kg significantly reduced the engraftment rate (p=0.02). Median neutrophil engraftment time (absolute neutrophil count reached ≥0.5×10⁹/L for 3 consecutive days) was day +22 (11-58) and median platelet engraftment time (platelet count reached ≥20×10⁹/L for 7 consecutive days without transfusion) was day +23 (11-60). In group PTCY-based GVHD prophylaxis the engraftment time was delayed (Fig. 1). 21 recipient (18%) had primary graft failure, including resistant relapse in 6 patients.

Figure 1. Engraftment terms for the patients with different GvHD prophylaxis. Abscissa, observation terms, days; ordinate, graft failure probability. Red graphs, recovery in cyclophosphamide-based GvHD prophylaxis; blue graphs, Cy-free regimens.
Box A, platelet engraftment time; Box B, neutrophil engraftment time

Survival data

Two-year overall survival (OS) in general group proved to be 40.3% after haplo-HSCT (Fig. 2). Particularly, the two-year OS in patients transplanted in remission of ALL and AML was 57% and 46% respectively as compared to 22% and 19% for the patients transplanted in adverse disease status (р=0.07). Overall survival for patients with lymphoproliferative disorders, acute leukemia and other diseases proved to be 82%, 31%, and 54% respectively (p=0.002, Fig. 2). For patients who received haplo-HSCT as salvage therapy two-year OS was 29% as compared to 57% for patients transplanted in remissions of diseases (р=0.001). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively (Fig. 3). Event-free survival for patients with lymphoproliferative disorders was significant higher compared with other groups: 76% vs 26% for patient with acute leukemia and 54% for patients with the other diseases (p=0.01, Fig. 2). With the current sample size GVHD prophylaxis based on рost-transplant cyclophosphamide had no significant impact for two-year OS and EFS (p=0.15 for OS and p=0.28 for EFS, Fig. 2).

Figure 2. Clinical outcomes of haplo-HSCT. Abscissa, observation terms, days; ordinate, survival probability

Note: A, B, two-year overall survival and event-free survival in general group; C, D, two-year overall survival and event-free survival depending on the GVHD prophylaxis (PTCY, post-transplant cyclophosphamide; TCD, T-cell depleted, ATG-based GVHD prophylaxis with ATGAM); E, F, two-year overall survival and event-free survival among patients with different disorders.

Figure 3. GVHD-free/relapse-free survival in general group.
Abscissa, observation terms, days; ordinate, survival probability

In the multivariate analysis, we found that advanced disease phase (p=0.03, 95%CI HR 1.074-4.286), acute GVHD (p=0.0039, 95%CI HR 0.145-0.69), and the earlier terms after transplantation (p=0.0042, 95%CI HR 0.711-0.938) were negative predictors of survival
(Fig. 4).

Figure 4. Subgroup analysis of event- free survival post-HSCT and relative risk factors (a Forest plot)

Posttransplant complications

Out of the 72 patients with engraftment, the cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. Use of manipulated transplants and PBSC as a source of graft significantly increased the incidence of aGVHD. However, in regression analysis these parameters had no significant impact. The cumulative incidence of chronic GVHD (cGVHD) was 16%. The only factor that significantly increased the risk of cGVHD was the preceeding aGVHD (p=0.03).

The cumulative incidence of relapse was 21%. In multivariate analysis, we found that BM as a source of graft (p=0.003, 95%CI HR 0.10-0.64), high/very high DRI group (p=0.04, 95%CI HR 1.02-2.72) were associated with a significantly increased incidence of relapse.

The overall transplant-associated mortality was 43% in the studied group. For patients who received haplo-HSCT as salvage therapy (47% vs 36%, p=0.03) and also in the group of patients with acute leukemia (48% vs 38% for patients with the other diseases, p=0.04) overall transplant-associated mortality was significantly higher. In multivariate analysis only advanced disease status did significantly impact the transplant-associated mortality (p=0.03, 95%CI HR 1.03-3.1).

Eighty-four recipients (65%) developed clinically significant complications. The main complications were as follows: grade II-III mucositis (53 recipients, 63%); hemorrhagic cystitis (20 recipients, 24%); sepsis (41 recipients, 49%); severe sepsis with septic shock (30 recipients, 36%); invasive fungal disease (17 recipients, 20%); clinically significant CMV reactivation (27 recipients, 32%).

The main cause of death up to day +100 (n=48) were infectious complications (n=32, 67%). Clinical and molecular relapses up to 100 days were observed in 7 recipients (15%).

Causes of death at later post-transplant period (n=28) were presented by infectious complications (n=13, 46%) and progression of primary disease (n=15, 54%).

Discussion

Allo-HSCT of the non-manipulated primed bone marrow from a haploidentical donor proved to be an effective approach to achieve clinical remission in children and adolescents with malignant disorders of hematopoiesis [30]. However, the role of this type of transplantation in the treatment of adult patients is still not completely determined. Immediate availability of a haploidentical donor makes this approach an attractive treatment option for patients who lack an HLA-identical donor or those for whom a MUD cannot be found in a timely manner. In recent years, use of post-transplant cyclophosphamide for GVHD prophylaxis after T-cell repleted haploidentical HSCT has yielded encouraging results in adults. In terms of survival, the outcomes following haploidentical HSCT with post-transplant cyclophosphamide have been comparable to MRD or MUD transplant in several non-randomized studies. Particularly, in cases where an HLA-identical sibling donor is not available for an AML patient with adverse disease a haploidentical donor may be used with the expectation of similar results, compared with those achieved with 10/10 matched and 9/10 mismatched UD unrelated donors. In our study, in a group of patients with acute leukemia, both in remission and in relapse, we obtained results comparable to the results of multicenter studies.

PTCy-based haplo-HSCT is associated with similar results with respect to NRM, OS, and EFS with those of conventional transplantations for patients with Hodgkin lymphoma. In a recent study by Martínez С et al, overall survival, relapse incidences and non-relapse mortality were 67%, 39% and 17% [31]. In the group of patients transplanted in our BMT center, these results were as follows: OS was 79%, relapse incidences – 15% and non-relapse mortality was 14%. In addition, several studies demonstrated the advantages for haplo-HSCT compared with the conventional transplantations for patients with r/r Hodgkin lymphoma allowing long-term remissions with limited toxicity, low GVHD incidence and early immune reconstitution to be achieved [32]. The data obtained allow of considering haplo-HSCT to be an acceptable option for patients with refractory/resistant (R/R) Hodgkin lymphoma.

The main causes of death according to our results were infectious complications in the pre-engraftment period and due to slow immune reconstitution after HSCT. The majority of patients were patients with relapsed/refractory acute leukemia who previously received significant number of chemotherapy courses. It is known, that the risk for colonization resistant bacteria is highest among patients with acute leukemia or high-risk MDS. Importantly, the treatment of these diseases prior to allo-HSCT typically requires one or more hospital admissions for high-dose chemotherapy and broad-spectrum antibiotics for fever and neutropenia, which presumably increases the risk of colonization multidrug resistant bacteria. Bacterial colonization in the setting of allo-HSCT confers an extraordinarily high risk for bloodstream infection in the early post-transplant period, with a considerable decrement in survival [33]. An additional adverse factor for patients with refractory disease was iron overload due to multiple blood transfusions. In accordance with our previous findings, we observed that the baseline increase of serum ferritin contents is associated with higher risk of febrile episodes, infectious conditions, and slower recovery of myeloid cells [34].

Post-transplant relapses represent the major problem for these patients. High percentage of relapses in our group of patients (39%) may be explained by the disease status at the time of haplo-HSCT. The majority of the patients (56%, n=67) received haplo-HSCT as a salvage therapy. According to the data published by Italian group, the relapse rates may reach 50% in this subset of patients [35, 36]. A strong graft-versus-leukemia effect mediated by alloreactive NK cells, resulting in reduced risk for relapse, was documented in adult patients with acute myeloid leukemia, undergoing T-cell-depleted HLA-haploidentical HSCT. Among receptors influencing NK cell function, the killer-cell immunoglobulin-like receptors (KIRs) are of particular importance. Two basic KIR haplotypes can be found in humans: the group A and the group B haplotypes [37]. Noteworthy, in a recent study by Michaelis et al, 57 adults with hematological malignancies given T-cell-depleted haploidentical HSCT were found to have a reduced risk for relapse when transplanted from a KIR haplotype B donor [38]. The presence of activating KIR, as seen in KIR haplotype B might reduce relapse in myeloid malignancies [39]. In our study, KIR genotyping was not carried out.

Graft failure remains a serious obstacle to the success of haplo-HSCT. Our haplo-HSCT data show unsatisfactory primary graft failure rate (18%). Most commonly, graft failure mediated by residual cellular immunity (recipient T-cells or NK-mediated allograft rejection) or humoral immunity (HLA-specific antibodies). In our study, we did not screen HLA -antibodies. Patients sensitized by blood transfusions, but also by pregnancy are at increased risk of rejection. The question of effective depletion of NK- cells still remains unresolved. Another major status for graft failure which may explain the observed results is the advanced disease status [40]. This might have significantly contributed to our results. The approach to dealing with the graft failure is the implementation of novel bridge therapies.

Conclusion

In summary, our results show that unmanipulated haplo-HSCT is a reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. The major advantage of haploidentical HSCT is the almost universal availability of highly motivated donors who can be mobilized in a short time at a relatively low cost. However, the problematic issue is the higher rate of graft failure, increased non-relapse mortality (NRM) and post-transplant relapses. To improve the results of haplo-HSCT, the appropriate multicenter studies are required.

Conflict of interest

The authors report no conflicts of interest.

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33. Marasco V, Forcina A, Lorentino F, Greco R. Pre-transplant colonization by a multidrug-resistant Gram negative bacteria has no impact on overall survival and mortality after hematopoietic stem cell transplantation: A single-center experience in 362 patients. J. Blood 2016 128:5743.
34. Mostafa Shaheen, Maria O. Ivanova, Ivan S. Moiseev, Sergey V. Bondarchuk, Boris V.Afanasyev. Impact of initial serum ferritin on early post-HSCT complications: a single- center study. Cell Ther Transplant. 2016;5(2): 40-49.
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36. Aversa F, Terenzi A, Tabilio A et al. Full haplotype mismatched hematopoietic stem-cell transplantation: a phase II study in patients with acute leukemia at high risk of relapse. J Clin Oncol. 2005; 23(15):3447-3454.
37. Oevermann L, Michaelis SU, Mezger M et al. KIR B haplotype donors confer a reduced risk for relapse after haploidentical transplantation in children with ALL. Blood. 2014;124(17):2744-2747.
38. Michaelis SU, Mezger M, Bornhäuser M, Trenschel R, Stuhler G, Federmann B, Oevermann L, Kanz L, Handgretinger R, Bethge WA. KIR haplotype B donors but not KIR-ligand mismatch result in a reduced incidence of relapse after haploidentical transplantation using reduced intensity conditioning and CD3/CD19-depleted grafts. Ann Hematol. 2014;93(9):1579-1586.
39. Heidenreich S, Kröger N. Reduction of relapse after unrelated donor stem cell transplantation by KIR-based graft selection. Front Immunol. 2017; 8:41. Published 2017 Feb 8. doi:10.3389/fimmu.2017.00041.
40. Mattsson J, Ringdén O, Storb R. Graft failure after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2008;14(1 Suppl 1):165-170.

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Introduction

Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis [1-4]. Historically, the best outcomes of allo-HSCT were obtained in cases when a donor was an HLA-matched sibling [5]. The probability of having an HLA-matched sibling donor is approximately thirty percent [6]. For patients who lack an HLA-matched sibling, alternative sources of donor grafts can be found in suitable HLA-matched adult unrelated donors (MUD), unrelated umbilical cord blood (UCB) donors, and partially HLA-mismatched-unrelated donors (mMUD) or HLA-haploidentical related donors (haplo-HSCT) [1, 8]. Despite the increasing number of volunteers in unrelated donor registries, the likelihood of finding a suitable matched unrelated donor is modest [6, 7]. However, haploidentical donor can be found for nearly every patient. The use of haploidentical donors is not limited by racial/ethnic HLA diversity or unusual HLA phenotypes due to mixed racial ancestry [6]. The benefits of haplo-HSCT include immediate donor availability for patients who need the transplant as soon as possible. Besides, post-transplant donor-derived cellular therapy is more easily accessible with the use of a related donor. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. However, this method was historically associated with poor engraftment, high risk of early death, and severe graft-versus-host disease (GVHD).

Earlier attempts at using unmanipulated haploidentical transplant were associated with an unacceptably high rate of GVHD related mortality. Several strategies have been evolved over the past decade to avoid these disadvantages. The advent of T-cell depleted haplo-SCT has allowed better control of the severe GVHD risk [9]. However, this approach was associated with a high rate of graft failure due to host T-lymphocytes that survived the conditioning regimen [10-12]. Later studies have shown that murine and human hematopoietic stem cells have veto cell activity and infusion of a large number of donor hematopoietic stem cells can overcome the MHC barrier and promote engraftment [13-15]. Megadose human CD34+ stem cells (on average >10×10⁶ CD34+ cells/kg body weight) with minimal T cell contamination (a median of 1×10⁴/kg weight) have been successfully used in haploidentical transplantation, which results in high-level engraftment of MHC disparate stem cells. The use of intensive conditioning without additional GVHD prophylaxis led to the result that nearly 80% of patients achieved primary engraftment and only 18% of the patients developed grade II-IV acute GVHD [16, 17]. The major disadvantages of T-cell depleted grafts are both high rate of relapse and nonrelapse mortality (NRM) due to slow immune reconstitution and, thus, infectious complications [18].

Another method to manipulate the T-cell depleted graft is co-infusion of donor-derived regulatory T-cells (Tregs). CD4+CD25+ regulatory T-cells have been shown to suppress proliferative responses of CD4+CD25− T-cells to allo-antigenic stimulation in vitro and are required for ex vivo tolerization of donor T-cells, which results in their reduced potential to induce aGVHD [19, 20]. Despite promising results, this approach is costly and technically demanding, which limits its application to experienced centers.

Another innovative approach is to selectively deplete T-cells responsible for GVHD (TCR alpha-beta) while sparing gamma-delta T-cells (γδ T-cells). Gamma-delta T-cells account for 1% to 10% of peripheral T-cells and have MHC-unrestricted innate cytotoxic activity against tumor cells [21-23]. The use of TCRαβ/CD19-depleted stem cells essentially accelerated immune recovery.

A more recent strategy is to selectively deplete naive T-cells to separate GVHD and the GVL effect. Naive T-cells with CD45RA expression demonstrate to be the most allo-reactive among the T-cell subsets. Ex vivo depletion of CD45RA T-cells and adoptive transfer of CD45RA-memory T-cells accelerate the immune reconstitution, increase the GVL effect while abrogating GVHD [24].

A group of Chinese researchers used a method based on G-CSF-stimulation of the donor, intensified immunosuppression, antithymocyte globulin as in vivo T-cell depletion, and combination of peripheral blood stem cell and bone marrow allografts. Despite satisfactory relapse-free survival rates, acceptable NRM and engraftment, relatively high incidence of severe acute and chronic GVHD was observed. In addition, the standard-risk patients often suffered with opportunistic infections [25, 26].

Trying to improve these results, Italian research team modified this approach through using only BM allografts and adding basiliximab which allowed them to achieve a lower rate of chronic GVHD that included both forms, limited and extensive [27].
Another approach to allo-HSCT was developed in Baltimore (USA) based on non-manipulated graft followed by post-transplant cyclophosphamide injection (PtCy) [28, 29]. This approach has overcome most obstacles historically connected with haplo-HSCT. Thus, recent changes in haplo- HSCT methodology have allowed to improve its results.

The aim of this study was to compare the efficiency of various haplo-HSCT approaches used in our HSCT center.

Patients and methods

The study included 119 patients transplanted from a haploidentical donor (haplo-HSCT) between 2006 and 2018 at the R. M. Gorbacheva Institute of Children Oncology (CIC 725). Their clinical parameters are shown in Table 1. Nine patients received second haplo-HSCT, due to graft failure in 8 cases and relapse in one patient. Eight patients were transplanted from the same donor and one patient from the other donor. Median age was 26 years (18-63), 61 patients were males (51%). Most frequent diagnosis in transplanted patients was acute leukemia (77%, n=92). Primary diagnoses were ALL (31%, n=37), AML (45%, n=53), ABL (2%, n=2), myeloproliferative neoplasms (8%, n=9), lymphoproliferative disorders (13%, n=16), severe aplastic anemia (1%, n=2). Median follow-up was 371 days (1-2219). A total of 46 patients with acute leukemia (38%) had complete remission at the time of HSCT (the first complete remission – 80%, n=37, the 2d or greater remission – 20%, n=9), 33% patients (n=30) had relapse, 15% patients (n=14) had refractory disease. Thus, 67 (56%) patients in the general group received haplo-HSCT as salvage therapy. Non-myeloablative, or reduced-intensity conditioning (RIC) was employed in 81% (n=96) and the myeloablative treatment (MAC) was used in 19% (n=23). Seventy-seven patients (65%) received busulfan, 14 patients (12%), melphalan, and 28 patients (23%) were administered other alkylating agents. Bone marrow was the graft source for 61% patients (n=73), peripheral blood (PBSC) – 39% patients (n=46). Mean transplant CD34+cell and CD3+cell dose was 5×10⁶/kg (1.5-10) and 10×10⁷/kg (2-44) respectively for bone marrow as a graft source, whereas it was 5.1×10⁶/kg (1-16.6) and 10×10⁷/kg (3-47) respectively for recipients who received PBSC as a source of graft.

GVHD prophylaxis based on рost-transplant cyclophosphamide (PTCY-based GVHD prophylaxis) 50 mg/kg at day+3, +4 was employed in 78 patients (66%), also these recipients received tacrolimus 0.03 mg/kg/day and MMF 30-45 mg/kg starting from day +5. Eleven patients (9%) received a T-cell manipulated transplant. The protocol of depletion and HSCT included conditioning according to the GIAC protocol, depleted PBSC in combination with native BM and ATGAM, tacrolimus, MMF.

A total of 30 patients (25%) received GVHD prophylaxis with ATGAM- 31 (26%) and alemtuzumab in 5 patients (4%). Tacrolimus was used for GVHD prophylaxis in 93 patients (72%), cyclosporin A – in 18 patients (14%). Clinical characteristics of the study group are presented in Table 1.

Table 1. Clinical characteristics of the study group

Clinical diagnosis of acute (aGVHD) and chronic GVHD (cGVHD) was based on standard criteria and confirmed by histological analysis of skin and/or rectal biopsy specimens. First-line and second-line therapy for GVHD was provided according to institutional protocols. For statistical evaluation, SPSS Statistics v.17 was used. Two-year time frame was selected for all outcomes. In the group description overall survival (OS), event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) were calculated using Kaplan-Meier methodology.

The comparisons were made using the log-rank test. The difference levels of p<0.05 were considered significant. Cumulative incidence analysis was used for aGVHD, cGVHD, relapse incidence and NRM. The comparisons were made using Gray test. The parameters with p.value <0.1 were selected for further Fyne-Gray regression analysis.

Results

Hematopoietic recovery

Stem cell engraftment after haplo-HSCT was documented in 61% of total group of patients (n=72). CD34+cell level less than 3×106/kg significantly reduced the engraftment rate (p=0.02). Median neutrophil engraftment time (absolute neutrophil count reached ≥0.5×10⁹/L for 3 consecutive days) was day +22 (11-58) and median platelet engraftment time (platelet count reached ≥20×10⁹/L for 7 consecutive days without transfusion) was day +23 (11-60). In group PTCY-based GVHD prophylaxis the engraftment time was delayed (Fig. 1). 21 recipient (18%) had primary graft failure, including resistant relapse in 6 patients.

Figure 1. Engraftment terms for the patients with different GvHD prophylaxis. Abscissa, observation terms, days; ordinate, graft failure probability. Red graphs, recovery in cyclophosphamide-based GvHD prophylaxis; blue graphs, Cy-free regimens.
Box A, platelet engraftment time; Box B, neutrophil engraftment time

Survival data

Two-year overall survival (OS) in general group proved to be 40.3% after haplo-HSCT (Fig. 2). Particularly, the two-year OS in patients transplanted in remission of ALL and AML was 57% and 46% respectively as compared to 22% and 19% for the patients transplanted in adverse disease status (р=0.07). Overall survival for patients with lymphoproliferative disorders, acute leukemia and other diseases proved to be 82%, 31%, and 54% respectively (p=0.002, Fig. 2). For patients who received haplo-HSCT as salvage therapy two-year OS was 29% as compared to 57% for patients transplanted in remissions of diseases (р=0.001). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively (Fig. 3). Event-free survival for patients with lymphoproliferative disorders was significant higher compared with other groups: 76% vs 26% for patient with acute leukemia and 54% for patients with the other diseases (p=0.01, Fig. 2). With the current sample size GVHD prophylaxis based on рost-transplant cyclophosphamide had no significant impact for two-year OS and EFS (p=0.15 for OS and p=0.28 for EFS, Fig. 2).

Figure 2. Clinical outcomes of haplo-HSCT. Abscissa, observation terms, days; ordinate, survival probability

Note: A, B, two-year overall survival and event-free survival in general group; C, D, two-year overall survival and event-free survival depending on the GVHD prophylaxis (PTCY, post-transplant cyclophosphamide; TCD, T-cell depleted, ATG-based GVHD prophylaxis with ATGAM); E, F, two-year overall survival and event-free survival among patients with different disorders.

Figure 3. GVHD-free/relapse-free survival in general group.
Abscissa, observation terms, days; ordinate, survival probability

In the multivariate analysis, we found that advanced disease phase (p=0.03, 95%CI HR 1.074-4.286), acute GVHD (p=0.0039, 95%CI HR 0.145-0.69), and the earlier terms after transplantation (p=0.0042, 95%CI HR 0.711-0.938) were negative predictors of survival
(Fig. 4).

Figure 4. Subgroup analysis of event- free survival post-HSCT and relative risk factors (a Forest plot)

Posttransplant complications

Out of the 72 patients with engraftment, the cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. Use of manipulated transplants and PBSC as a source of graft significantly increased the incidence of aGVHD. However, in regression analysis these parameters had no significant impact. The cumulative incidence of chronic GVHD (cGVHD) was 16%. The only factor that significantly increased the risk of cGVHD was the preceeding aGVHD (p=0.03).

The cumulative incidence of relapse was 21%. In multivariate analysis, we found that BM as a source of graft (p=0.003, 95%CI HR 0.10-0.64), high/very high DRI group (p=0.04, 95%CI HR 1.02-2.72) were associated with a significantly increased incidence of relapse.

The overall transplant-associated mortality was 43% in the studied group. For patients who received haplo-HSCT as salvage therapy (47% vs 36%, p=0.03) and also in the group of patients with acute leukemia (48% vs 38% for patients with the other diseases, p=0.04) overall transplant-associated mortality was significantly higher. In multivariate analysis only advanced disease status did significantly impact the transplant-associated mortality (p=0.03, 95%CI HR 1.03-3.1).

Eighty-four recipients (65%) developed clinically significant complications. The main complications were as follows: grade II-III mucositis (53 recipients, 63%); hemorrhagic cystitis (20 recipients, 24%); sepsis (41 recipients, 49%); severe sepsis with septic shock (30 recipients, 36%); invasive fungal disease (17 recipients, 20%); clinically significant CMV reactivation (27 recipients, 32%).

The main cause of death up to day +100 (n=48) were infectious complications (n=32, 67%). Clinical and molecular relapses up to 100 days were observed in 7 recipients (15%).

Causes of death at later post-transplant period (n=28) were presented by infectious complications (n=13, 46%) and progression of primary disease (n=15, 54%).

Discussion

Allo-HSCT of the non-manipulated primed bone marrow from a haploidentical donor proved to be an effective approach to achieve clinical remission in children and adolescents with malignant disorders of hematopoiesis [30]. However, the role of this type of transplantation in the treatment of adult patients is still not completely determined. Immediate availability of a haploidentical donor makes this approach an attractive treatment option for patients who lack an HLA-identical donor or those for whom a MUD cannot be found in a timely manner. In recent years, use of post-transplant cyclophosphamide for GVHD prophylaxis after T-cell repleted haploidentical HSCT has yielded encouraging results in adults. In terms of survival, the outcomes following haploidentical HSCT with post-transplant cyclophosphamide have been comparable to MRD or MUD transplant in several non-randomized studies. Particularly, in cases where an HLA-identical sibling donor is not available for an AML patient with adverse disease a haploidentical donor may be used with the expectation of similar results, compared with those achieved with 10/10 matched and 9/10 mismatched UD unrelated donors. In our study, in a group of patients with acute leukemia, both in remission and in relapse, we obtained results comparable to the results of multicenter studies.

PTCy-based haplo-HSCT is associated with similar results with respect to NRM, OS, and EFS with those of conventional transplantations for patients with Hodgkin lymphoma. In a recent study by Martínez С et al, overall survival, relapse incidences and non-relapse mortality were 67%, 39% and 17% [31]. In the group of patients transplanted in our BMT center, these results were as follows: OS was 79%, relapse incidences – 15% and non-relapse mortality was 14%. In addition, several studies demonstrated the advantages for haplo-HSCT compared with the conventional transplantations for patients with r/r Hodgkin lymphoma allowing long-term remissions with limited toxicity, low GVHD incidence and early immune reconstitution to be achieved [32]. The data obtained allow of considering haplo-HSCT to be an acceptable option for patients with refractory/resistant (R/R) Hodgkin lymphoma.

The main causes of death according to our results were infectious complications in the pre-engraftment period and due to slow immune reconstitution after HSCT. The majority of patients were patients with relapsed/refractory acute leukemia who previously received significant number of chemotherapy courses. It is known, that the risk for colonization resistant bacteria is highest among patients with acute leukemia or high-risk MDS. Importantly, the treatment of these diseases prior to allo-HSCT typically requires one or more hospital admissions for high-dose chemotherapy and broad-spectrum antibiotics for fever and neutropenia, which presumably increases the risk of colonization multidrug resistant bacteria. Bacterial colonization in the setting of allo-HSCT confers an extraordinarily high risk for bloodstream infection in the early post-transplant period, with a considerable decrement in survival [33]. An additional adverse factor for patients with refractory disease was iron overload due to multiple blood transfusions. In accordance with our previous findings, we observed that the baseline increase of serum ferritin contents is associated with higher risk of febrile episodes, infectious conditions, and slower recovery of myeloid cells [34].

Post-transplant relapses represent the major problem for these patients. High percentage of relapses in our group of patients (39%) may be explained by the disease status at the time of haplo-HSCT. The majority of the patients (56%, n=67) received haplo-HSCT as a salvage therapy. According to the data published by Italian group, the relapse rates may reach 50% in this subset of patients [35, 36]. A strong graft-versus-leukemia effect mediated by alloreactive NK cells, resulting in reduced risk for relapse, was documented in adult patients with acute myeloid leukemia, undergoing T-cell-depleted HLA-haploidentical HSCT. Among receptors influencing NK cell function, the killer-cell immunoglobulin-like receptors (KIRs) are of particular importance. Two basic KIR haplotypes can be found in humans: the group A and the group B haplotypes [37]. Noteworthy, in a recent study by Michaelis et al, 57 adults with hematological malignancies given T-cell-depleted haploidentical HSCT were found to have a reduced risk for relapse when transplanted from a KIR haplotype B donor [38]. The presence of activating KIR, as seen in KIR haplotype B might reduce relapse in myeloid malignancies [39]. In our study, KIR genotyping was not carried out.

Graft failure remains a serious obstacle to the success of haplo-HSCT. Our haplo-HSCT data show unsatisfactory primary graft failure rate (18%). Most commonly, graft failure mediated by residual cellular immunity (recipient T-cells or NK-mediated allograft rejection) or humoral immunity (HLA-specific antibodies). In our study, we did not screen HLA -antibodies. Patients sensitized by blood transfusions, but also by pregnancy are at increased risk of rejection. The question of effective depletion of NK- cells still remains unresolved. Another major status for graft failure which may explain the observed results is the advanced disease status [40]. This might have significantly contributed to our results. The approach to dealing with the graft failure is the implementation of novel bridge therapies.

Conclusion

In summary, our results show that unmanipulated haplo-HSCT is a reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. The major advantage of haploidentical HSCT is the almost universal availability of highly motivated donors who can be mobilized in a short time at a relatively low cost. However, the problematic issue is the higher rate of graft failure, increased non-relapse mortality (NRM) and post-transplant relapses. To improve the results of haplo-HSCT, the appropriate multicenter studies are required.

Conflict of interest

The authors report no conflicts of interest.

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31. Martinez C, Gayoso J, Channels C, Finel H, Peggs K, Dominietto A, Castagna L, Afanasyev B, Robinson S, Blaise D, Corradini P, Itälä-Remes M, Bermúdez A, Forcade E, Russo D, Potter M, McQuaker G, Yakoub-Agha I, Scheid C, Bloor A, Montoto S, Dreger P, Sureda A. Post-transplantation cyclophosphamide-based haploidentical transplantation as alternative to matched sibling or unrelated donor transplantation for Hodgkin lymphoma: A registry study of the Lymphoma Working Party of the European Society for Blood and Marrow Transplantation. J Clin Oncol. 2017;35(30):3425-3432.
32. 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;14(11):1279-1287.
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Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. 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Бейнарович, Елена В. Бабенко, Иван С. Моисеев, Олеся В. Паина, Ольга В. Пирогова, Татьяна А. Рудакова, Татьяна Л. Гиндина, Елена И. Дарская, Елена В. Морозова, Сергей Н. Бондаренко, Людмила С. Зубаровская, Борис В. Афанасьев</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(425) "

Анастасия В. Бейнарович, Елена В. Бабенко, Иван С. Моисеев, Олеся В. Паина, Ольга В. Пирогова, Татьяна А. Рудакова, Татьяна Л. Гиндина, Елена И. Дарская, Елена В. Морозова, Сергей Н. Бондаренко, Людмила С. Зубаровская, Борис В. Афанасьев

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НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета, Санкт-Петербург, Россия

" ["TYPE"]=> string(4) "HTML" } ["~DESCRIPTION"]=> string(0) "" ["~NAME"]=> string(22) "Организации" ["~DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } } ["SUMMARY_RU"]=> array(36) { ["ID"]=> string(2) "27" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(29) "Описание/Резюме" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(10) "SUMMARY_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "27" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21342" ["VALUE"]=> array(2) { ["TEXT"]=> string(4755) "<p style="text-align: justify;">Аллогенная трансплантация костного мозга (алло- ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными. </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид. </p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(4699) "

Аллогенная трансплантация костного мозга (алло- ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными.

Ключевые слова

Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид.

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Anastasia V. Beynarovich, Elena V. Babenko, Ivan S. Moiseev, Olesya V. Paina, Olga V. Pirogova, Tatiana A. Rudakova, Tatyana L. Gindina, Elena I. Darskaya, Elena V. Morozova, Sergey N. Bondarenko, Ludmila S. Zubarovskaya, Boris V. Afanasyev

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R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantology at the First St. Petersburg State I. Pavlov Medical University

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Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis. For patients who lack an HLA-matched sibling, HLA-haploidentical related donors (haplo-HSCT) can be considered as alternative sources of donor grafts. The benefits of haplo-HSCT include immediate donor availability for patients who are in urgent need of the transplant. Besides, an availability of a related donor makes post-transplant donor-derived cellular therapy more easily accessible. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. The aim of our study was to summarize our single-center experience of haplo-HSCT performed with non-manipulated grafts in adult patients with different malignant diseases. The study included a total of 119 patients with different hematological disorders subjected to haplo-HSCT. At the time of analysis, median follow-up was 371 days (1-2219). Most frequent diagnosis in transplanted patients was acute leukemia. 67 (56%) patients received haplo-HSCT as salvage therapy.
Overall survival with an observation term of 2 years was 40.3% for the general group. In particular, the two-year OS in patients transplanted in remissions of ALL and AML was 57% and 46% respectively as compared to 22% and 15% for the patients transplanted in adverse disease status). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively. The cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. The cumulative incidence of chronic GVHD (cGVHD) was 16%.The cumulative incidence of relapse was 21%. The overall transplant-associated mortality was 43% in the studied group. In conclusion, our results show that unmanipulated haplo-HSCT is reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. However, such problems as higher rate graft failure, increased nonrelapse mortality (NRM) and post-transplant relapses remain extremely relevant.

Keywords

Allogeneic hematopoietic stem cell transplantation, haploidentical, adult patients, overall survival, post-transplant relapse, graft-versus-host disease, graft failure, post-transplant cyclophosphamide.

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Beynarovich, Elena V. Babenko, Ivan S. Moiseev, Olesya V. Paina, Olga V. Pirogova, Tatiana A. Rudakova, Tatyana L. Gindina, Elena I. Darskaya, Elena V. Morozova, Sergey N. Bondarenko, Ludmila S. Zubarovskaya, Boris V. Afanasyev</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(248) "

Anastasia V. Beynarovich, Elena V. Babenko, Ivan S. Moiseev, Olesya V. Paina, Olga V. Pirogova, Tatiana A. Rudakova, Tatyana L. Gindina, Elena I. Darskaya, Elena V. Morozova, Sergey N. Bondarenko, Ludmila S. Zubarovskaya, Boris V. Afanasyev

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Anastasia V. Beynarovich, Elena V. Babenko, Ivan S. Moiseev, Olesya V. Paina, Olga V. Pirogova, Tatiana A. Rudakova, Tatyana L. Gindina, Elena I. Darskaya, Elena V. Morozova, Sergey N. Bondarenko, Ludmila S. Zubarovskaya, Boris V. Afanasyev

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Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis. For patients who lack an HLA-matched sibling, HLA-haploidentical related donors (haplo-HSCT) can be considered as alternative sources of donor grafts. The benefits of haplo-HSCT include immediate donor availability for patients who are in urgent need of the transplant. Besides, an availability of a related donor makes post-transplant donor-derived cellular therapy more easily accessible. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. The aim of our study was to summarize our single-center experience of haplo-HSCT performed with non-manipulated grafts in adult patients with different malignant diseases. The study included a total of 119 patients with different hematological disorders subjected to haplo-HSCT. At the time of analysis, median follow-up was 371 days (1-2219). Most frequent diagnosis in transplanted patients was acute leukemia. 67 (56%) patients received haplo-HSCT as salvage therapy.
Overall survival with an observation term of 2 years was 40.3% for the general group. In particular, the two-year OS in patients transplanted in remissions of ALL and AML was 57% and 46% respectively as compared to 22% and 15% for the patients transplanted in adverse disease status). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively. The cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. The cumulative incidence of chronic GVHD (cGVHD) was 16%.The cumulative incidence of relapse was 21%. The overall transplant-associated mortality was 43% in the studied group. In conclusion, our results show that unmanipulated haplo-HSCT is reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. However, such problems as higher rate graft failure, increased nonrelapse mortality (NRM) and post-transplant relapses remain extremely relevant.

Keywords

Allogeneic hematopoietic stem cell transplantation, haploidentical, adult patients, overall survival, post-transplant relapse, graft-versus-host disease, graft failure, post-transplant cyclophosphamide.

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Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis. For patients who lack an HLA-matched sibling, HLA-haploidentical related donors (haplo-HSCT) can be considered as alternative sources of donor grafts. The benefits of haplo-HSCT include immediate donor availability for patients who are in urgent need of the transplant. Besides, an availability of a related donor makes post-transplant donor-derived cellular therapy more easily accessible. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. The aim of our study was to summarize our single-center experience of haplo-HSCT performed with non-manipulated grafts in adult patients with different malignant diseases. The study included a total of 119 patients with different hematological disorders subjected to haplo-HSCT. At the time of analysis, median follow-up was 371 days (1-2219). Most frequent diagnosis in transplanted patients was acute leukemia. 67 (56%) patients received haplo-HSCT as salvage therapy.
Overall survival with an observation term of 2 years was 40.3% for the general group. In particular, the two-year OS in patients transplanted in remissions of ALL and AML was 57% and 46% respectively as compared to 22% and 15% for the patients transplanted in adverse disease status). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively. The cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. The cumulative incidence of chronic GVHD (cGVHD) was 16%.The cumulative incidence of relapse was 21%. The overall transplant-associated mortality was 43% in the studied group. In conclusion, our results show that unmanipulated haplo-HSCT is reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. However, such problems as higher rate graft failure, increased nonrelapse mortality (NRM) and post-transplant relapses remain extremely relevant.

Keywords

Allogeneic hematopoietic stem cell transplantation, haploidentical, adult patients, overall survival, post-transplant relapse, graft-versus-host disease, graft failure, post-transplant cyclophosphamide.

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R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantology at the First St. Petersburg State I. Pavlov Medical University

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R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantology at the First St. Petersburg State I. Pavlov Medical University

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Beynarovich" ["LINK_ELEMENT_VALUE"]=> bool(false) } ["SUMMARY_RU"]=> array(37) { ["ID"]=> string(2) "27" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(29) "Описание/Резюме" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(10) "SUMMARY_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "27" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21342" ["VALUE"]=> array(2) { ["TEXT"]=> string(4755) "<p style="text-align: justify;">Аллогенная трансплантация костного мозга (алло- ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными. </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид. </p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(4699) "

Аллогенная трансплантация костного мозга (алло- ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными.

Ключевые слова

Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид.

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Аллогенная трансплантация костного мозга (алло- ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными.

Ключевые слова

Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид.

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НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета, Санкт-Петербург, Россия

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НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета, Санкт-Петербург, Россия

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Introduction

One of the urgent problems of modern otorhinolaryngology and clinical medicine are inflammatory lesions of the paranasal sinuses (PS). Over the past decade, the incidence of sinusitis has increased 3 times [1]. According to different authors, acute or chronic sinusitis suffer from 5 to 15% of the adult population and about 5-13% of children [2, 3]. In the structure of stationary pathology acute sinusitis is 15-36% [4]. Every year, the number of hospitalizations for this reason increases by 1.5-2% [1].

Infections are a relevant problem for hematopoietic stem cell transplantation (HSCT) and cause of failure in the treatment of patients after transplantation. At the same time, there has been an increase in the number of immunocompromised patients, due to increased usage of HSCT for various oncological, hematological and hereditary diseases [5]. As a result, the risk of bacterial, viral, fungal infections increases at various sites, including the defeat clinically significant lesions of paranasal sinuses (PS) in such patients [6-14]. According to the published studies, the incidence of sinusitis among adult patients subjected to HSCT ranges from 21% to 36% [11, 15, 16]. Appropriate data on children and adolescents are absent in available literature.

Currently we know about several retrospective studies of the factors associated with allo-HSCT procedure which increase the risk of PS affection in adults. Such studies are lacking in children and adolescents undergoing HSCT.

The patients with post-transplant leukocytopenia do not exhibit a typical inflammatory response, unlike immunocompetent patients. In this regard, the symptoms of PS lesions may be absent, or mildly expressed [11], thus making it difficult to diagnose these conditions. In addition, invasive procedures in HSCT recipients, e.g., diagnostic and therapeutic punctures of maxillary sinuses or mucosal biopsy in invasive PS mycosis, or PS lesion, as a manifestation of the underlying disease, may be associated with development of severe complications that aggravate general condition of the patient [17]. Meanwhile, X-ray diagnostics of PS at the specialized radiological units for detection of sinusitis at early terms after allo-HSCT is difficult due to limited access for the patients over the aplastic period since they have to be isolated in the wards equipped with laminar air flow and HEPA filtration.

Evolving sinusitis may be a factor contributing to development of other infectious complications (bronchitis, pneumonia) at the early and late terms after allo-HSCT [18].

Thus, the study of risk factors, diagnostic issues and therapy of inflammatory PS lesions in children and adolescents is a necessary condition preventing infectious complications after HSCT and, ultimately, providing a clinical success.

The aim of our study was to improve diagnosis and treatment of sinusitis in children and adolescents after allogeneic transplantation of hematopoietic stem cells. We have identified a subgroup of patients with increased risk for infectious complications after allo-HSCT, in particular, sinusitis, thus allowing to develop methods of its prevention and diagnosis, as well as early therapy of this condition.

Patients and Methods

The work was performed on the basis of retrospective and prospective analysis of medical records on the patients 0 to 21 years of age after autologous or allogeneic hematopoietic stem cell transplantation (HSCT), performed in R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantation at the First St. Petersburg State I. Pavlov Medical University over the period of 2008 to 2013.

The main group of the study consisted of 352 recipients (67% of total) subjected to allo-HSCT at the age ranging from 4 months to 21 years (median, 12 years; gender ratio: 213 males and 139 females). The comparison group consisted of 172 recipients (33%) who underwent autologous HSCT (auto- HSCT), 1 to 21 years old (median of 12 years, the group included 101 males and 71 females). The spectrum of underlying disorders in HSCT recipients is presented in Table 1.

Table 1. Clinical characteristics of primary disease in the patients subjected to allo- or auto-HSCT

Remission of the underlying disease was observed in 195 patients with allo-HSCT, relapse, in 157 patients. At the auto-HSCT, 147 patients were in complete remission; 25 patients were in partial remission. Bone marrow (BM) was used as a stem cell source in 244 patients (69%) allo-HSCT; peripheral blood stem cells (PBSC) were applied in 108 cases (31%). For auto-HSCT, BM was used in 139 patients (81%); PBSC were transfused to 33 recipients (19%). The conditioning regimen for ALLO-HSCT was chosen with respect to the patient's age, primary diagnosis, previous treatment, complications associated with therapy, and somatic status at the time of HSCT. Myeloablative regimens (MR) were used in 148 patient (42%)s scheduled for allo-HSCT, and in 172 cases (100%) intended for auto-HSCT. Non-myeloablative regimens and reduced-intensity doses (NR/RID) were applied to 204 (58%) patients for allo-HSCT.

Allo-HSCT was performed from related or unrelated donors that were completely or partially compatible for HLA antigens. Related donors were used for 166 patients (47%) including 51 patients (31%) transplanted from HLA-compatible donors, and 115 patients (69%) with haploidentical stem cells. Matched unrelated donors were used in 186 patients (53%), including 166 patients (89%) with HLA-compatible genes (11%) and 20 patients with HLA – partially compatible genes (89%).

The patients with sinusitis as an infectious complication after allo-HSCT were considered a separate clinical subgroup. The group of patients with sinusitis consisted of 78 recipients of allo-HSCT at the age of 2 to 21 years (median of 13 years; the M/F ratio was 51:27). Forty-three patients were classified as children (2 – 13 years, median age – 9 years), and 35 patients were considered adolescents and young adults (14 – 21 years, median age – 18 years). The primary diagnoses in the group of patients with sinusitis after allo-HSCT are shown in Table 2.

Table 2. Spectrum of underlying diseases in the group of patients with sinusitis after allo-HSCT (n=78)

Diagnostic criteria of sinusitis in children and adolescents were based on the common recommendations [19]. The main research methods were as follows: collection of the patients’ medical history and complaints to assess overall severity of sinusitis manifestations in the post-transplant patients. A visual analogue scale was graded from 0 (minimal symptomatics) to 10 (maximal severity of symptoms) [19, 20]. Routine otorhinolaryngological examination was also performed, i.e., anterior and posterior rhinoscopy, pharyngoscopy, otoscopy, indirect laryngoscopy. Endoscopic inspection of nasal cavity was performed using a rigid endoscope with a viewing angle of 0° (Karl Storz, Germany). Visible changes in mucous membrane of the nasal cavity and nature of secretions the discharge in the nasal passages were evaluated by the endoscopy. The results of this study were recorded on digital media for subsequent analysis. Rigid endoscopes with different angles (Karl Storz, Germany) were also used for endovideoscopy and functional surgery of paranasal sinuses.

The cases of sinusitis were confirmed by X-ray examination, computed tomography (CT) or magnetic resonance imaging (MRI) of the area. PS alterations revealed with CT and MRI techniques were classified by a modified version of Lund method [21]. The degree of PS lesions was scored from 0 to 2. A score of 0 corresponded to absence of the PS disease; 1, partial shading or thickening of the PS mucous membrane; 2, total shading or fluid levels in PS. Ostiomeatal complexes on the PS images obtained by CT and MRI were evaluated as 0 or 2 points, respectively, free or blocked.

Taking material from the paranasal sinuses for bacteriological and mycological studies was performed by aspiration of the contents of maxillary sinuses during a diagnostic puncture.

Biopsy material was obtained intraoperatively under the control of rigid endoscopes with a viewing angle of 0°, 45°, 30°. Prevention of infectious complications was commenced from the first day of conditioning treatment, using the second-generation fluoroquinolones (ciprofloxacin) at a daily dose of 10-15 mg/kg in 2 injections. To prevent pneumonias, trimethoprim/sulfamethoxazole (Biseptol) was used at a dose of 10 mg/kg/day (trimethoprim), depending on age, twice a day, 3 times a week. Acyclovir was used at a dose of 200 mg 3 times a day as antiviral prophylaxis, starting from the day of hematopoietic restoration.

Primary prophylaxis of fungal infection was performed with drugs from the azole group (triazoles) of different generations (e.g., Fluсonazole), at a dose of 1-2 mg/kg/day. Secondary prevention proceeded with Voriconazole at a dose of 100-200 mg every 12 hours; Posaconazole at a dose of 600-800 mg/day, or a drug from the group of echinocandins (Сaspofungin), 50-70 mg/day, starting on the first day of conditioning and continuing until ceasing the immunosuppressive therapy in the absence of invasive mycoses.

All the patients underwent routine blood and differential leukocyte counts, serum biochemical analysis. Engraftment of donor hematopoietic cells was controlled by the results of clinical blood cell counts, and molecular biology methods (donor chimerism assays). The day of engraftment was defined as achieving neutrophil levels of >0.5×10⁹/l without prior stimulation by G-CSF for 3 days, reaching platelet counts of >25.0×10⁹/l without prior transfusion of platelet concentrate for 3 days. Severity of thrombocytopenia and neutropenia was assessed in accordance with the World Health Organization classification.

Statistical analysis was performed in Statistica version 10.0 (StatSoft, USA) using nonparametric methods for comparing groups by the quantitative Mann-Whitney criteria, the groups with qualitative characteristics were compared using conjugated tables, t-test, Chi-square and Fisher exact tests. Correlation analysis was performed with Spearman method, log-linear multifactorial analysis. The differences were considered significant by р<0.05.

Results

Occurrence and severity of sinusitis post-transplant

The incidence of sinusitis after allo-HSCT was 22.2% among our patients. It was found that the frequency of sinusitis after allo-HSCT (22.2%) was significantly higher than after auto-HSCT (1.7%, p <0.001). Over recent years, the number of performed allo-HSCT has increased by 33%. Meanwhile, the frequency of sinusitis after allo-HSCT has significantly decreased, i.e., from 39.2% in 2010 to 10.8% in 2013 (p=0.001), as shown in Fig. 1.

Figure 1. Annual numbers of allo-HSCTs and relative frequencies of sinusitis in the cohorts studied

The largest incidence of sinusitis among children and adolescents was observed in 2010 (respectively, 40.5% and 36.8%). In 2013, the sinusitis occurence is progressively reduced to 14.8% (p=0.018) in the groups of children, and to 6.8% among adolescents (p=0.026).

The frequency of sinusitis proved to be higher at later terms (>100 days after allo-HSCT). Incidence of sinusitis within 100 days post-transplant was 9.6%, as compared to 17.7% after D+100 (p=0.006).

Distribution of the PS lesions by their volume in patients after allo-HSCT was as follows: the maxillary sinus (MS) was involved in 24 patients (30.8%) including unilateral MS affection in 1 case; the MS lesions combined with other PS were detected in 51 cases (65.4%), including 13 patients with all the sinuses affected (16.7%). Isolated lesion of the main sinus was observed in 2 cases (2.5%). Inflammation of PS without MS affection was documented in 3 cases (3.8%).

A decrease in the number of clinical symptoms of sinusitis (p=0.008), and an increase in cases of mild sinusitis on a visual analog scale (p=0.032) was registered since 100 days post-transplant (Fig. 2).

Figure 2. Time-dependent dynamics of clinical sinusitis manifestations according to visual analogue scale period after allo-HSCT

In the patients with neutropenia of I–IV degree at several weeks post-HSCT, severe changes in paranasal sinuses were more often noted by means of CT technique (p=0.018). However, in 50% of cases (24/48). In view of clinical severity of PS affection detected by CT, there were changes in severe-grade cases, and such changes in PS were more common after >100 days post-transplant (p=0.014) (Fig. 3).

Figure 3. Dynamics of changes in the sinuses detected by computer tomography, depending on the time period after allo-HSCT

Infectious agents in sinusitis

In the course of this study, 41 bacteriological and mycological analyses of the samples from maxillary sinuses were performed. The specimens were obtained during diagnostic and therapeutic puncture. Briefly, any pathogen growth was not detected in 10 cases (24.4%), bacterial monocultures were isolated in 15 cases (36.6%); fungal monocultures were obtained from two samples (4.9%). The results concerning maxillary sinus aspirate were as follows: inflammation associated with bacteria in 51.2% of cases (n=21), fungal cultures were obtained in 19.5% of cases (n=8), and mixed infection was revealed in 2 cases (4.9%), as shown in Fig. 5.

Figure 5. Results of microbiological cultures of maxillary sinus aspirate from the sinusitis patients

The main sinusitis-associated pathogens in allo-HSCT recipients were Gram-positive bacteria: Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). The frequency of fungal sinusitis after allo-HSCT was 5%; association of bacteria and fungi was observed in 20% of cases. Aspergillus moulds proved to be the main causative agents in fungal sinusitis (80% of positive samples).

After 100 days from allo-HSCT, a larger proportion of sinus secretions showed the absence of microflora growth (p=0.022). It should be noted that the bacterial monocultures predominated up to 100 days from allo-HSCT (p=0.011). Incidence of bacterial sinusitis up to 100 days from allo-HSCT was 74% (14/19); after 100 days from allo-HSCT it was 32% (7/22) (p=0.018).

A comparative analysis of children and adolescent groups has revealed that combined infections were more often observed in adolescent patients with sinusitis (p=0.042).

Treatment of sinusitis

When assessing duration of sinusitis treatment, we have noted that the patients after auto-HSCs recovered faster than the patients after allo-HSCT (p=0.007). In our study, a recovery from sinusitis occurred within 15 days in 5% of patients after allo-HSCT, whereas 92.5% of such patients received therapy for >30 days. In 2.5% of cases, the treatment period was more than 100 days. Terms of treatment and methods of therapy for different age groups are presented in Table 3.

Table 3. Duration of treatment of sinusitis in groups and with different methods of therapy

The sinusitis treatment in pediatric patients was longer than in adolescent group (p=0.018). Usage of MS puncture in combination with antimicrobial therapy significantly reduces the duration of sinusitis treatment (p=0.024), especially in severe changes in the sinuses on CT (p=0.035).

Diagnostic and treatment punctures were performed in 41 (52.6%) patients with mandatory sampling of biomaterial for bacteriological and mycological examinations. Age of patients at the time of puncture ranged from 4 years to 21 years. In the children under 7 years, the procedure was carried out under the endotracheal anesthesia in the operating room.

At the time of the puncture, 26/41 (63.4%) patients had a blood platelet level <100.0×10⁹/L. Of them, 20/26 (77%) patients did not exceed the level of 50.0×10⁹/L (p=0.0001). We have not confirmed a relationship between the frequency of bleeding after the procedure and platelet levels (p=0.935).

Pneumonia and bronchitis after a sinus infection in recipients of HSCT was observed in 70.5% of cases (55/78). When analyzing the incidence of lung lesions due to sinusitis in HSCT recipients, depending on the period after allo-HSCT, we have revealed that the pulmonary lesions were observed more often before D+100 after allo-HSCT (28/34, 82%) than after 100 days (27/44, 61%, p=0.049).

The endoscopic sinus surgery was performed in 4 patients (5%) under general anaesthesia, indications for the operation were: orbital complications (reactive edema of the eyelids and local face areas), invasive fungal infection. At the time of surgical treatment, the blood platelet levels in patients ranged from 15.0 to 50.0×10⁹/L, complications after surgery were not observed.

The mono- and multifactorial analysis have revealed several risk factors for sinusitis after allo-HSCT: a story of sinusitis before allo-HSCT (p <0.001), acute (p=0.022) or chronic graft-versus-host disease (p <0.001). In unifactorial analysis, the duration of neutropenia more than 10 days was also associated with sinusitis risk (p=0.054).

Discussion

According to different studies, the frequency of sinusitis in adult patients after allo-HSCT ranges from 11 to 51% [3, 8, 15, 16, 18]. In our group of patients, the frequency of sinusitis after allo-HSCT was 22.2%. Our study has also shown that the sinusitis frequency after allo-HSCT is higher than after auto-HSCT (p <0.001), which coincides with results from other groups [8, 11, 18].

Previous studies have noted that the presence of acute or chronic graft-versus-host reaction (GVHD) comprises a risk factor for sinusitis after allo-HSCT [18]. In our study, we found a correlation between these factors and sinusitis occurrence. Presence of acute (p=0.022) or chronic GVHD (p <0.001) was associated with significant increase of paranasal sinus pathology after allo-HSCT.

In the patients with immunodeficiency of either origin (neutropenia, HSC recipients, HIV infection) nosocomial infections were more common associated with Gram-negative bacteria (Pseudomonas aeruginosa, Klebsiella pneumoniae, Escherichia coli, Proteus spp., Enterobacter spp., Citrobacter), as well as Gram-positive bacteria such as Staphylococcus aureus (15.3%), Streptococcus pneumoniae, Enterococcus faecalis [18, 22]. In our study, the main local causative agents of sinusitis revealed in allo-HSCT recipients were Gram-positive bacteria Staphylococcus epidermidis (30%), Streptococcus viridans (30%), or Gram-negative bacteria, e.g., Klebsiella pneumoniae (17.5%). It was found that the proportion of negative cultures from the sinuses was higher at the terms of >100 days after allo-HSCT (p=0.022). It should be noted that the monocultures of bacteria prevailed up to 100 days from allo-HSCT (p=0.011). The findings for combined sinusitis-associated infections were more often observed in adolescent patients, in comparison with children group (p=0.042).

In assessing the duration of sinusitis treatment, we have noted that the patients after auto-HSCT recovered faster than patients after allo-HSCT (p=0.007). This fact may be associated with a faster recovery of the body's defense mechanisms after auto-HSCT than following allo-HSCT, as well as the lack of immunosuppressive therapy in autologous transplants. In our study, recovery from sinusitis occurred within 15 days in 5% of patients after allo-HSCT; 92.5% of patients received therapy for 30 days or more. In 2.5% of patients, the treatment period exceeded 100 days post-transplant. The use of PPP puncture in combination with antimicrobial therapy significantly reduces the duration of sinusitis treatment (p=0.024), especially in cases with severe changes in paranasal sinuses registered by CT and MRI (p=0.035). In pediatric patients, sinusitis treatment was longer than in the adolescent group (p=0.018).

Conclusion

1. Sinusitis folowing allogeneic HSCT occurs more frequently than in auto-transplants;
2. The significant factors for the post-transplant sinusitis are: sufficient immunosuppression, e.g., associated to acute or chronic GVHD;
3. Opportunistic microflora in local samples from the sinusitis patients was found in a half of microbiological cultures.

Conflict of interest

The authors report no conflicts of interest.

References

1. Ivanchenko OA, Lopatin AS. Chronic rhinosinusitis: epidemiology, classification, etiology, pathogenesis. Mo-dern view on the problem. Vestn Otorhinolaryngol. 2012; 2: 91-96 (In Russian).
2. Pluzhnikov MS, Lavrenova GV, Katinas EB. Basic prin- ciples of immunocorrecting therapy in otorhinolaryngology. Vestn Otorhinolaryngol. 2008. № 4:7-12 (In Russian).
3. Arulrajah S, Symons H, Cahoon EK, Tekes A, Thierry A, Huisman G M, Izbudak I. Relationship between clinical sinusitis symptoms and sinus CT severity in pediatric post bone marrow transplant and immunocompetent patients. Eur J Pediatr. 2012; 171(2): 375-381.
4. Slavsky AN, Pshonkina DM, Svistushkin VM. Bacteriophages in the complex treatment of acute bacterial rhinosinusitis. Rus Med J. 2014; 2:1925-1928 (In Russian).
5. Bento LR, Ortiz E, Nicola EM, Vigorito AC. Sinonasal disorders in hematopoietic stem cell transplantation. Braz J Otorhinolaryngol. 2014; 80(4): 285-289.
6. Afanasyev BV, Volkova OY, Ganapiev AA. In: Afanasyev, BV (Ed). Hematology: A Guide for Doctors. St.Petersburg: Speclit. 2008. - 238 p (In Russian).
7. Weinberg К, Blazar BR, Wagner JE, Agura E, Hill BJ, Smogorzewska M, Koup RA, Betts MR, Collins RH, Douek DC. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood. 2001; 97(5): 1458-1466.
8. Thompson AM, Couch M, Zahurak ML, Johnson C, Vogelsang GB. Risk factors for post-stem cell transplant sinusitis. Bone Marrow Transplant. 2002; 29(3): 257-261.
9. Appelbaum FR. Hematopoietic-cell transplantation at 50. New Engl J Med. 2007; 357(15):1472-1475.
10. Gratwohl A, Baldomero H, Aljurf M, Pasquini MC. Hematopoietic stem cell transplantation. A global perspective. J Am Med Ass. 2010;303(16):1617-1624.
11. Won YW, Yi SY, Jang JH, Kim K, Kim SJ, Kim WS, Jung CW, Kim DH. Retrospective analysis of paranasal sinusitis in patients receiving hematopoietic stem cell transplantation. Int J Hematol. 2011; 93(3):383-388.
12. Inaba H, Hartford CM, Pei D, Posner MJ, Yang J, Hayden RT, Srinivasan A, Triplett BM, McCulllers JA, Pui CH, Leung W. Longitudinal analysis of antibody response to immunization in paediatric survivors after allogeneic haematopoietic stem cell transplantation. Br J Haematol. 2012; 156(1): 109-117.
13. Meng L, Huang XJ. Allogeneic hematopoietic stem cell transplantation in China: where we are and where to go. J Hematol Oncol. 2012. 5(1):10.
14. Mortellaro C, Mortellaro C, Barat V, Nesi F, L. Bello, G. Bologna, D. Farronato, A. G. Lucchina, A. Linari. Intercurrent infectious diseases in post-stem cell transplant patients: paranasal sinusitis. J Craniofac Surg. 2012; 23(1):153-157. 
15. Meyers JD. Infection in bone marrow transplant recipients Am J Med. 1986; 81(1):27-38.
16. Shibuya TY, Momin F, Abella E, Jacobs JR, Karanes C, Ratanatharathorn V, Sensenbrenner LL, Lum LG. Sinus disease in the bone marrow transplant population: incidence, risk factors, and complications. Otolaryngol Head Neck Surg. 1995; 113(6):705-711.
17. Deutsch JH, Hudgins PA, Siegel JL, Peterman SB, Devine SM, York R, Wingard JR. The paranasal sinuses of patients with acute graft-versus-host disease. Am J Neuroradiol. 1995; 16(6):1287-1291.
18. Savage DG, Taylor P, Blackwel J, Chen F, Szydlo RM, Rule SAJ, Spencer A, Apperley JF, Goldman JM. Paranasal sinusitis following allogeneic bone marrow transplant. Bone Marrow Transplant. 1997; 19(1):55-59.
19. Fokkens WJ, Lund VJ, Mullol J, Bachert C, Alobid I, Baroody F, Cohen N, Cervin A, Douglas R, Gevaert P, Georgalas C, Goossens H, Harvey R, Hellings P, Hopkins C, Jones N, Joos G, et al. European Position Paper on Rhinosinusitis and Nasal Polyps Group: European position paper on rhinosinusitis and nasal polyps 2012. Rhinology. 2012; 50 (Suppl 23): 1-329.
20. Lim М, Lew Gor S, Darby Y. The relationship between subjective assessment instruments in chronic rhinosinusitis. Rhinology. 2007; 45(2):144-147.
21. Lund VJ, Kennedy DW. Staging for chronic rhinosinusitis. Otolaryngol Head Neck Surg. 1997: 117(1):35-40.
22. Imamura R, Voegels R, Sperandio F. Microbiology of sinusitis in patients undergoing bone marrow transplantation. Otolaryngol Head Neck Surg. 1999; 120(2): 279-282.

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Introduction

One of the urgent problems of modern otorhinolaryngology and clinical medicine are inflammatory lesions of the paranasal sinuses (PS). Over the past decade, the incidence of sinusitis has increased 3 times [1]. According to different authors, acute or chronic sinusitis suffer from 5 to 15% of the adult population and about 5-13% of children [2, 3]. In the structure of stationary pathology acute sinusitis is 15-36% [4]. Every year, the number of hospitalizations for this reason increases by 1.5-2% [1].

Infections are a relevant problem for hematopoietic stem cell transplantation (HSCT) and cause of failure in the treatment of patients after transplantation. At the same time, there has been an increase in the number of immunocompromised patients, due to increased usage of HSCT for various oncological, hematological and hereditary diseases [5]. As a result, the risk of bacterial, viral, fungal infections increases at various sites, including the defeat clinically significant lesions of paranasal sinuses (PS) in such patients [6-14]. According to the published studies, the incidence of sinusitis among adult patients subjected to HSCT ranges from 21% to 36% [11, 15, 16]. Appropriate data on children and adolescents are absent in available literature.

Currently we know about several retrospective studies of the factors associated with allo-HSCT procedure which increase the risk of PS affection in adults. Such studies are lacking in children and adolescents undergoing HSCT.

The patients with post-transplant leukocytopenia do not exhibit a typical inflammatory response, unlike immunocompetent patients. In this regard, the symptoms of PS lesions may be absent, or mildly expressed [11], thus making it difficult to diagnose these conditions. In addition, invasive procedures in HSCT recipients, e.g., diagnostic and therapeutic punctures of maxillary sinuses or mucosal biopsy in invasive PS mycosis, or PS lesion, as a manifestation of the underlying disease, may be associated with development of severe complications that aggravate general condition of the patient [17]. Meanwhile, X-ray diagnostics of PS at the specialized radiological units for detection of sinusitis at early terms after allo-HSCT is difficult due to limited access for the patients over the aplastic period since they have to be isolated in the wards equipped with laminar air flow and HEPA filtration.

Evolving sinusitis may be a factor contributing to development of other infectious complications (bronchitis, pneumonia) at the early and late terms after allo-HSCT [18].

Thus, the study of risk factors, diagnostic issues and therapy of inflammatory PS lesions in children and adolescents is a necessary condition preventing infectious complications after HSCT and, ultimately, providing a clinical success.

The aim of our study was to improve diagnosis and treatment of sinusitis in children and adolescents after allogeneic transplantation of hematopoietic stem cells. We have identified a subgroup of patients with increased risk for infectious complications after allo-HSCT, in particular, sinusitis, thus allowing to develop methods of its prevention and diagnosis, as well as early therapy of this condition.

Patients and Methods

The work was performed on the basis of retrospective and prospective analysis of medical records on the patients 0 to 21 years of age after autologous or allogeneic hematopoietic stem cell transplantation (HSCT), performed in R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantation at the First St. Petersburg State I. Pavlov Medical University over the period of 2008 to 2013.

The main group of the study consisted of 352 recipients (67% of total) subjected to allo-HSCT at the age ranging from 4 months to 21 years (median, 12 years; gender ratio: 213 males and 139 females). The comparison group consisted of 172 recipients (33%) who underwent autologous HSCT (auto- HSCT), 1 to 21 years old (median of 12 years, the group included 101 males and 71 females). The spectrum of underlying disorders in HSCT recipients is presented in Table 1.

Table 1. Clinical characteristics of primary disease in the patients subjected to allo- or auto-HSCT

Remission of the underlying disease was observed in 195 patients with allo-HSCT, relapse, in 157 patients. At the auto-HSCT, 147 patients were in complete remission; 25 patients were in partial remission. Bone marrow (BM) was used as a stem cell source in 244 patients (69%) allo-HSCT; peripheral blood stem cells (PBSC) were applied in 108 cases (31%). For auto-HSCT, BM was used in 139 patients (81%); PBSC were transfused to 33 recipients (19%). The conditioning regimen for ALLO-HSCT was chosen with respect to the patient's age, primary diagnosis, previous treatment, complications associated with therapy, and somatic status at the time of HSCT. Myeloablative regimens (MR) were used in 148 patient (42%)s scheduled for allo-HSCT, and in 172 cases (100%) intended for auto-HSCT. Non-myeloablative regimens and reduced-intensity doses (NR/RID) were applied to 204 (58%) patients for allo-HSCT.

Allo-HSCT was performed from related or unrelated donors that were completely or partially compatible for HLA antigens. Related donors were used for 166 patients (47%) including 51 patients (31%) transplanted from HLA-compatible donors, and 115 patients (69%) with haploidentical stem cells. Matched unrelated donors were used in 186 patients (53%), including 166 patients (89%) with HLA-compatible genes (11%) and 20 patients with HLA – partially compatible genes (89%).

The patients with sinusitis as an infectious complication after allo-HSCT were considered a separate clinical subgroup. The group of patients with sinusitis consisted of 78 recipients of allo-HSCT at the age of 2 to 21 years (median of 13 years; the M/F ratio was 51:27). Forty-three patients were classified as children (2 – 13 years, median age – 9 years), and 35 patients were considered adolescents and young adults (14 – 21 years, median age – 18 years). The primary diagnoses in the group of patients with sinusitis after allo-HSCT are shown in Table 2.

Table 2. Spectrum of underlying diseases in the group of patients with sinusitis after allo-HSCT (n=78)

Diagnostic criteria of sinusitis in children and adolescents were based on the common recommendations [19]. The main research methods were as follows: collection of the patients’ medical history and complaints to assess overall severity of sinusitis manifestations in the post-transplant patients. A visual analogue scale was graded from 0 (minimal symptomatics) to 10 (maximal severity of symptoms) [19, 20]. Routine otorhinolaryngological examination was also performed, i.e., anterior and posterior rhinoscopy, pharyngoscopy, otoscopy, indirect laryngoscopy. Endoscopic inspection of nasal cavity was performed using a rigid endoscope with a viewing angle of 0° (Karl Storz, Germany). Visible changes in mucous membrane of the nasal cavity and nature of secretions the discharge in the nasal passages were evaluated by the endoscopy. The results of this study were recorded on digital media for subsequent analysis. Rigid endoscopes with different angles (Karl Storz, Germany) were also used for endovideoscopy and functional surgery of paranasal sinuses.

The cases of sinusitis were confirmed by X-ray examination, computed tomography (CT) or magnetic resonance imaging (MRI) of the area. PS alterations revealed with CT and MRI techniques were classified by a modified version of Lund method [21]. The degree of PS lesions was scored from 0 to 2. A score of 0 corresponded to absence of the PS disease; 1, partial shading or thickening of the PS mucous membrane; 2, total shading or fluid levels in PS. Ostiomeatal complexes on the PS images obtained by CT and MRI were evaluated as 0 or 2 points, respectively, free or blocked.

Taking material from the paranasal sinuses for bacteriological and mycological studies was performed by aspiration of the contents of maxillary sinuses during a diagnostic puncture.

Biopsy material was obtained intraoperatively under the control of rigid endoscopes with a viewing angle of 0°, 45°, 30°. Prevention of infectious complications was commenced from the first day of conditioning treatment, using the second-generation fluoroquinolones (ciprofloxacin) at a daily dose of 10-15 mg/kg in 2 injections. To prevent pneumonias, trimethoprim/sulfamethoxazole (Biseptol) was used at a dose of 10 mg/kg/day (trimethoprim), depending on age, twice a day, 3 times a week. Acyclovir was used at a dose of 200 mg 3 times a day as antiviral prophylaxis, starting from the day of hematopoietic restoration.

Primary prophylaxis of fungal infection was performed with drugs from the azole group (triazoles) of different generations (e.g., Fluсonazole), at a dose of 1-2 mg/kg/day. Secondary prevention proceeded with Voriconazole at a dose of 100-200 mg every 12 hours; Posaconazole at a dose of 600-800 mg/day, or a drug from the group of echinocandins (Сaspofungin), 50-70 mg/day, starting on the first day of conditioning and continuing until ceasing the immunosuppressive therapy in the absence of invasive mycoses.

All the patients underwent routine blood and differential leukocyte counts, serum biochemical analysis. Engraftment of donor hematopoietic cells was controlled by the results of clinical blood cell counts, and molecular biology methods (donor chimerism assays). The day of engraftment was defined as achieving neutrophil levels of >0.5×10⁹/l without prior stimulation by G-CSF for 3 days, reaching platelet counts of >25.0×10⁹/l without prior transfusion of platelet concentrate for 3 days. Severity of thrombocytopenia and neutropenia was assessed in accordance with the World Health Organization classification.

Statistical analysis was performed in Statistica version 10.0 (StatSoft, USA) using nonparametric methods for comparing groups by the quantitative Mann-Whitney criteria, the groups with qualitative characteristics were compared using conjugated tables, t-test, Chi-square and Fisher exact tests. Correlation analysis was performed with Spearman method, log-linear multifactorial analysis. The differences were considered significant by р<0.05.

Results

Occurrence and severity of sinusitis post-transplant

The incidence of sinusitis after allo-HSCT was 22.2% among our patients. It was found that the frequency of sinusitis after allo-HSCT (22.2%) was significantly higher than after auto-HSCT (1.7%, p <0.001). Over recent years, the number of performed allo-HSCT has increased by 33%. Meanwhile, the frequency of sinusitis after allo-HSCT has significantly decreased, i.e., from 39.2% in 2010 to 10.8% in 2013 (p=0.001), as shown in Fig. 1.

Figure 1. Annual numbers of allo-HSCTs and relative frequencies of sinusitis in the cohorts studied

The largest incidence of sinusitis among children and adolescents was observed in 2010 (respectively, 40.5% and 36.8%). In 2013, the sinusitis occurence is progressively reduced to 14.8% (p=0.018) in the groups of children, and to 6.8% among adolescents (p=0.026).

The frequency of sinusitis proved to be higher at later terms (>100 days after allo-HSCT). Incidence of sinusitis within 100 days post-transplant was 9.6%, as compared to 17.7% after D+100 (p=0.006).

Distribution of the PS lesions by their volume in patients after allo-HSCT was as follows: the maxillary sinus (MS) was involved in 24 patients (30.8%) including unilateral MS affection in 1 case; the MS lesions combined with other PS were detected in 51 cases (65.4%), including 13 patients with all the sinuses affected (16.7%). Isolated lesion of the main sinus was observed in 2 cases (2.5%). Inflammation of PS without MS affection was documented in 3 cases (3.8%).

A decrease in the number of clinical symptoms of sinusitis (p=0.008), and an increase in cases of mild sinusitis on a visual analog scale (p=0.032) was registered since 100 days post-transplant (Fig. 2).

Figure 2. Time-dependent dynamics of clinical sinusitis manifestations according to visual analogue scale period after allo-HSCT

In the patients with neutropenia of I–IV degree at several weeks post-HSCT, severe changes in paranasal sinuses were more often noted by means of CT technique (p=0.018). However, in 50% of cases (24/48). In view of clinical severity of PS affection detected by CT, there were changes in severe-grade cases, and such changes in PS were more common after >100 days post-transplant (p=0.014) (Fig. 3).

Figure 3. Dynamics of changes in the sinuses detected by computer tomography, depending on the time period after allo-HSCT

Infectious agents in sinusitis

In the course of this study, 41 bacteriological and mycological analyses of the samples from maxillary sinuses were performed. The specimens were obtained during diagnostic and therapeutic puncture. Briefly, any pathogen growth was not detected in 10 cases (24.4%), bacterial monocultures were isolated in 15 cases (36.6%); fungal monocultures were obtained from two samples (4.9%). The results concerning maxillary sinus aspirate were as follows: inflammation associated with bacteria in 51.2% of cases (n=21), fungal cultures were obtained in 19.5% of cases (n=8), and mixed infection was revealed in 2 cases (4.9%), as shown in Fig. 5.

Figure 5. Results of microbiological cultures of maxillary sinus aspirate from the sinusitis patients

The main sinusitis-associated pathogens in allo-HSCT recipients were Gram-positive bacteria: Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). The frequency of fungal sinusitis after allo-HSCT was 5%; association of bacteria and fungi was observed in 20% of cases. Aspergillus moulds proved to be the main causative agents in fungal sinusitis (80% of positive samples).

After 100 days from allo-HSCT, a larger proportion of sinus secretions showed the absence of microflora growth (p=0.022). It should be noted that the bacterial monocultures predominated up to 100 days from allo-HSCT (p=0.011). Incidence of bacterial sinusitis up to 100 days from allo-HSCT was 74% (14/19); after 100 days from allo-HSCT it was 32% (7/22) (p=0.018).

A comparative analysis of children and adolescent groups has revealed that combined infections were more often observed in adolescent patients with sinusitis (p=0.042).

Treatment of sinusitis

When assessing duration of sinusitis treatment, we have noted that the patients after auto-HSCs recovered faster than the patients after allo-HSCT (p=0.007). In our study, a recovery from sinusitis occurred within 15 days in 5% of patients after allo-HSCT, whereas 92.5% of such patients received therapy for >30 days. In 2.5% of cases, the treatment period was more than 100 days. Terms of treatment and methods of therapy for different age groups are presented in Table 3.

Table 3. Duration of treatment of sinusitis in groups and with different methods of therapy

The sinusitis treatment in pediatric patients was longer than in adolescent group (p=0.018). Usage of MS puncture in combination with antimicrobial therapy significantly reduces the duration of sinusitis treatment (p=0.024), especially in severe changes in the sinuses on CT (p=0.035).

Diagnostic and treatment punctures were performed in 41 (52.6%) patients with mandatory sampling of biomaterial for bacteriological and mycological examinations. Age of patients at the time of puncture ranged from 4 years to 21 years. In the children under 7 years, the procedure was carried out under the endotracheal anesthesia in the operating room.

At the time of the puncture, 26/41 (63.4%) patients had a blood platelet level <100.0×10⁹/L. Of them, 20/26 (77%) patients did not exceed the level of 50.0×10⁹/L (p=0.0001). We have not confirmed a relationship between the frequency of bleeding after the procedure and platelet levels (p=0.935).

Pneumonia and bronchitis after a sinus infection in recipients of HSCT was observed in 70.5% of cases (55/78). When analyzing the incidence of lung lesions due to sinusitis in HSCT recipients, depending on the period after allo-HSCT, we have revealed that the pulmonary lesions were observed more often before D+100 after allo-HSCT (28/34, 82%) than after 100 days (27/44, 61%, p=0.049).

The endoscopic sinus surgery was performed in 4 patients (5%) under general anaesthesia, indications for the operation were: orbital complications (reactive edema of the eyelids and local face areas), invasive fungal infection. At the time of surgical treatment, the blood platelet levels in patients ranged from 15.0 to 50.0×10⁹/L, complications after surgery were not observed.

The mono- and multifactorial analysis have revealed several risk factors for sinusitis after allo-HSCT: a story of sinusitis before allo-HSCT (p <0.001), acute (p=0.022) or chronic graft-versus-host disease (p <0.001). In unifactorial analysis, the duration of neutropenia more than 10 days was also associated with sinusitis risk (p=0.054).

Discussion

According to different studies, the frequency of sinusitis in adult patients after allo-HSCT ranges from 11 to 51% [3, 8, 15, 16, 18]. In our group of patients, the frequency of sinusitis after allo-HSCT was 22.2%. Our study has also shown that the sinusitis frequency after allo-HSCT is higher than after auto-HSCT (p <0.001), which coincides with results from other groups [8, 11, 18].

Previous studies have noted that the presence of acute or chronic graft-versus-host reaction (GVHD) comprises a risk factor for sinusitis after allo-HSCT [18]. In our study, we found a correlation between these factors and sinusitis occurrence. Presence of acute (p=0.022) or chronic GVHD (p <0.001) was associated with significant increase of paranasal sinus pathology after allo-HSCT.

In the patients with immunodeficiency of either origin (neutropenia, HSC recipients, HIV infection) nosocomial infections were more common associated with Gram-negative bacteria (Pseudomonas aeruginosa, Klebsiella pneumoniae, Escherichia coli, Proteus spp., Enterobacter spp., Citrobacter), as well as Gram-positive bacteria such as Staphylococcus aureus (15.3%), Streptococcus pneumoniae, Enterococcus faecalis [18, 22]. In our study, the main local causative agents of sinusitis revealed in allo-HSCT recipients were Gram-positive bacteria Staphylococcus epidermidis (30%), Streptococcus viridans (30%), or Gram-negative bacteria, e.g., Klebsiella pneumoniae (17.5%). It was found that the proportion of negative cultures from the sinuses was higher at the terms of >100 days after allo-HSCT (p=0.022). It should be noted that the monocultures of bacteria prevailed up to 100 days from allo-HSCT (p=0.011). The findings for combined sinusitis-associated infections were more often observed in adolescent patients, in comparison with children group (p=0.042).

In assessing the duration of sinusitis treatment, we have noted that the patients after auto-HSCT recovered faster than patients after allo-HSCT (p=0.007). This fact may be associated with a faster recovery of the body's defense mechanisms after auto-HSCT than following allo-HSCT, as well as the lack of immunosuppressive therapy in autologous transplants. In our study, recovery from sinusitis occurred within 15 days in 5% of patients after allo-HSCT; 92.5% of patients received therapy for 30 days or more. In 2.5% of patients, the treatment period exceeded 100 days post-transplant. The use of PPP puncture in combination with antimicrobial therapy significantly reduces the duration of sinusitis treatment (p=0.024), especially in cases with severe changes in paranasal sinuses registered by CT and MRI (p=0.035). In pediatric patients, sinusitis treatment was longer than in the adolescent group (p=0.018).

Conclusion

1. Sinusitis folowing allogeneic HSCT occurs more frequently than in auto-transplants;
2. The significant factors for the post-transplant sinusitis are: sufficient immunosuppression, e.g., associated to acute or chronic GVHD;
3. Opportunistic microflora in local samples from the sinusitis patients was found in a half of microbiological cultures.

Conflict of interest

The authors report no conflicts of interest.

References

1. Ivanchenko OA, Lopatin AS. Chronic rhinosinusitis: epidemiology, classification, etiology, pathogenesis. Mo-dern view on the problem. Vestn Otorhinolaryngol. 2012; 2: 91-96 (In Russian).
2. Pluzhnikov MS, Lavrenova GV, Katinas EB. Basic prin- ciples of immunocorrecting therapy in otorhinolaryngology. Vestn Otorhinolaryngol. 2008. № 4:7-12 (In Russian).
3. Arulrajah S, Symons H, Cahoon EK, Tekes A, Thierry A, Huisman G M, Izbudak I. Relationship between clinical sinusitis symptoms and sinus CT severity in pediatric post bone marrow transplant and immunocompetent patients. Eur J Pediatr. 2012; 171(2): 375-381.
4. Slavsky AN, Pshonkina DM, Svistushkin VM. Bacteriophages in the complex treatment of acute bacterial rhinosinusitis. Rus Med J. 2014; 2:1925-1928 (In Russian).
5. Bento LR, Ortiz E, Nicola EM, Vigorito AC. Sinonasal disorders in hematopoietic stem cell transplantation. Braz J Otorhinolaryngol. 2014; 80(4): 285-289.
6. Afanasyev BV, Volkova OY, Ganapiev AA. In: Afanasyev, BV (Ed). Hematology: A Guide for Doctors. St.Petersburg: Speclit. 2008. - 238 p (In Russian).
7. Weinberg К, Blazar BR, Wagner JE, Agura E, Hill BJ, Smogorzewska M, Koup RA, Betts MR, Collins RH, Douek DC. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood. 2001; 97(5): 1458-1466.
8. Thompson AM, Couch M, Zahurak ML, Johnson C, Vogelsang GB. Risk factors for post-stem cell transplant sinusitis. Bone Marrow Transplant. 2002; 29(3): 257-261.
9. Appelbaum FR. Hematopoietic-cell transplantation at 50. New Engl J Med. 2007; 357(15):1472-1475.
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12. Inaba H, Hartford CM, Pei D, Posner MJ, Yang J, Hayden RT, Srinivasan A, Triplett BM, McCulllers JA, Pui CH, Leung W. Longitudinal analysis of antibody response to immunization in paediatric survivors after allogeneic haematopoietic stem cell transplantation. Br J Haematol. 2012; 156(1): 109-117.
13. Meng L, Huang XJ. Allogeneic hematopoietic stem cell transplantation in China: where we are and where to go. J Hematol Oncol. 2012. 5(1):10.
14. Mortellaro C, Mortellaro C, Barat V, Nesi F, L. Bello, G. Bologna, D. Farronato, A. G. Lucchina, A. Linari. Intercurrent infectious diseases in post-stem cell transplant patients: paranasal sinusitis. J Craniofac Surg. 2012; 23(1):153-157. 
15. Meyers JD. Infection in bone marrow transplant recipients Am J Med. 1986; 81(1):27-38.
16. Shibuya TY, Momin F, Abella E, Jacobs JR, Karanes C, Ratanatharathorn V, Sensenbrenner LL, Lum LG. Sinus disease in the bone marrow transplant population: incidence, risk factors, and complications. Otolaryngol Head Neck Surg. 1995; 113(6):705-711.
17. Deutsch JH, Hudgins PA, Siegel JL, Peterman SB, Devine SM, York R, Wingard JR. The paranasal sinuses of patients with acute graft-versus-host disease. Am J Neuroradiol. 1995; 16(6):1287-1291.
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19. Fokkens WJ, Lund VJ, Mullol J, Bachert C, Alobid I, Baroody F, Cohen N, Cervin A, Douglas R, Gevaert P, Georgalas C, Goossens H, Harvey R, Hellings P, Hopkins C, Jones N, Joos G, et al. European Position Paper on Rhinosinusitis and Nasal Polyps Group: European position paper on rhinosinusitis and nasal polyps 2012. Rhinology. 2012; 50 (Suppl 23): 1-329.
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Утимишева¹, Олег И. Долгов¹, Олеся В. Паина¹, Кирилл А. Екушов¹, Алина А. Витрищак¹, Борис И. Смирнов², Людмила С. Зубаровская ¹, Сергей А. Карпищенко¹, Борис В. Афанасьев¹</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(423) "

Екатерина С. Утимишева¹, Олег И. Долгов¹, Олеся В. Паина¹, Кирилл А. Екушов¹, Алина А. Витрищак¹, Борис И. Смирнов², Людмила С. Зубаровская ¹, Сергей А. Карпищенко¹, Борис В. Афанасьев¹

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¹ Первый Санкт-Петербургский государственный медицинский университет им. академика И. П. Павлова, Россия
² Санкт-Петербургский государственный электротехнический университет «ЛЭТИ», Россия

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Синусит после аллогенной трансплантации гемопоэтических стволовых клеток возникает в 22,2% случаев с более высокой частотой после 100 дня от алло-ТГСК, чем до 100 (р=0,006). Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина» (р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии Staphylococcus epidermidis (30%), Streptococcus viridans (30%), грамотрицательные бактерии Klebsiella pneumoniae (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024).

Ключевые слова

Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.

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Ekaterina S. Utimisheva¹, Oleg I. Dolgov¹, Olesya V. Paina¹, Kirill A. Ekushov¹, Alina A. Vitrischak¹, Boris I. Smirnov², Ludmila S. Zubarovskaya¹, Sergey A. Karpischenko¹, Boris V. Afanasyev¹

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¹ Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia
² St. Petersburg State Electrotechnical University LETI, St. Petersburg, Russia

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Sinusitis after allogeneic transplantation of hematopoietic stem cells occurs in 22.2% of cases being more frequent at >100 days following allo-HSCT, than at earlier terms (p=0.006). The main risk factors for sinusitis after allogeneic stem cell transplantation were as follows: sinusitis before allo-HSCT (p <0.001), neutropenia duration for more than 10 days (p=0.054), acute (p=0.022) or chronic graft-versus-host disease (p <0.001) in the patients. The main pathogens of sinusitis revealed in allo-HSCT recipients during the study were: Gram-positive Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). A monoculture of bacteria predominated within 100 days posttransplant (p=0.011). Poly-etiological origin of the causative bacterial agents in sinusitis was more likely in adolescent patients, in comparison to the younger children group. The severity of changes in paranasal sinuses, as registered with computed tomography after 100 days after allo-HSCT, was more pronounced (p=0.014) than at earlier terms, thus being discordant with less common clinical signs of sinusitis (p=0.008), and milder clinical course of sinusitis assessed by a visual analogue scale (p=0.032) during this period. Punctures of maxillary sinuses combined with antimicrobial therapy proved to shorten the duration of sinusitis treatment in these patients (p=0.024).

Keywords

Sinusitis, children, hematopoietic stem cell transplantation.

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Utimisheva¹, Oleg I. Dolgov¹, Olesya V. Paina¹, Kirill A. Ekushov¹, Alina A. Vitrischak¹, Boris I. Smirnov², Ludmila S. Zubarovskaya¹, Sergey A. Karpischenko¹, Boris V. Afanasyev¹</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(298) "

Ekaterina S. Utimisheva¹, Oleg I. Dolgov¹, Olesya V. Paina¹, Kirill A. Ekushov¹, Alina A. Vitrischak¹, Boris I. Smirnov², Ludmila S. Zubarovskaya¹, Sergey A. Karpischenko¹, Boris V. Afanasyev¹

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Ekaterina S. Utimisheva¹, Oleg I. Dolgov¹, Olesya V. Paina¹, Kirill A. Ekushov¹, Alina A. Vitrischak¹, Boris I. Smirnov², Ludmila S. Zubarovskaya¹, Sergey A. Karpischenko¹, Boris V. Afanasyev¹

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Sinusitis after allogeneic transplantation of hematopoietic stem cells occurs in 22.2% of cases being more frequent at >100 days following allo-HSCT, than at earlier terms (p=0.006). The main risk factors for sinusitis after allogeneic stem cell transplantation were as follows: sinusitis before allo-HSCT (p <0.001), neutropenia duration for more than 10 days (p=0.054), acute (p=0.022) or chronic graft-versus-host disease (p <0.001) in the patients. The main pathogens of sinusitis revealed in allo-HSCT recipients during the study were: Gram-positive Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). A monoculture of bacteria predominated within 100 days posttransplant (p=0.011). Poly-etiological origin of the causative bacterial agents in sinusitis was more likely in adolescent patients, in comparison to the younger children group. The severity of changes in paranasal sinuses, as registered with computed tomography after 100 days after allo-HSCT, was more pronounced (p=0.014) than at earlier terms, thus being discordant with less common clinical signs of sinusitis (p=0.008), and milder clinical course of sinusitis assessed by a visual analogue scale (p=0.032) during this period. Punctures of maxillary sinuses combined with antimicrobial therapy proved to shorten the duration of sinusitis treatment in these patients (p=0.024).

Keywords

Sinusitis, children, hematopoietic stem cell transplantation.

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Sinusitis after allogeneic transplantation of hematopoietic stem cells occurs in 22.2% of cases being more frequent at >100 days following allo-HSCT, than at earlier terms (p=0.006). The main risk factors for sinusitis after allogeneic stem cell transplantation were as follows: sinusitis before allo-HSCT (p <0.001), neutropenia duration for more than 10 days (p=0.054), acute (p=0.022) or chronic graft-versus-host disease (p <0.001) in the patients. The main pathogens of sinusitis revealed in allo-HSCT recipients during the study were: Gram-positive Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). A monoculture of bacteria predominated within 100 days posttransplant (p=0.011). Poly-etiological origin of the causative bacterial agents in sinusitis was more likely in adolescent patients, in comparison to the younger children group. The severity of changes in paranasal sinuses, as registered with computed tomography after 100 days after allo-HSCT, was more pronounced (p=0.014) than at earlier terms, thus being discordant with less common clinical signs of sinusitis (p=0.008), and milder clinical course of sinusitis assessed by a visual analogue scale (p=0.032) during this period. Punctures of maxillary sinuses combined with antimicrobial therapy proved to shorten the duration of sinusitis treatment in these patients (p=0.024).

Keywords

Sinusitis, children, hematopoietic stem cell transplantation.

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¹ Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia
² St. Petersburg State Electrotechnical University LETI, St. Petersburg, Russia

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¹ Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia
² St. Petersburg State Electrotechnical University LETI, St. Petersburg, Russia

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Екатерина С. Утимишева¹, Олег И. Долгов¹, Олеся В. Паина¹, Кирилл А. Екушов¹, Алина А. Витрищак¹, Борис И. Смирнов², Людмила С. Зубаровская ¹, Сергей А. Карпищенко¹, Борис В. Афанасьев¹

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Екатерина С. Утимишева¹, Олег И. Долгов¹, Олеся В. Паина¹, Кирилл А. Екушов¹, Алина А. Витрищак¹, Борис И. Смирнов², Людмила С. Зубаровская ¹, Сергей А. Карпищенко¹, Борис В. Афанасьев¹

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Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина» (р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии <i>Staphylococcus epidermidis </i>(30%), <i>Streptococcus viridans</i> (30%), грамотрицательные бактерии <i>Klebsiella pneumoniae</i> (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024). </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(2701) "

Синусит после аллогенной трансплантации гемопоэтических стволовых клеток возникает в 22,2% случаев с более высокой частотой после 100 дня от алло-ТГСК, чем до 100 (р=0,006). Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина» (р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии Staphylococcus epidermidis (30%), Streptococcus viridans (30%), грамотрицательные бактерии Klebsiella pneumoniae (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024).

Ключевые слова

Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.

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Синусит после аллогенной трансплантации гемопоэтических стволовых клеток возникает в 22,2% случаев с более высокой частотой после 100 дня от алло-ТГСК, чем до 100 (р=0,006). Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина» (р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии Staphylococcus epidermidis (30%), Streptococcus viridans (30%), грамотрицательные бактерии Klebsiella pneumoniae (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024).

Ключевые слова

Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.

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¹ Первый Санкт-Петербургский государственный медицинский университет им. академика И. П. Павлова, Россия
² Санкт-Петербургский государственный электротехнический университет «ЛЭТИ», Россия

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¹ Первый Санкт-Петербургский государственный медицинский университет им. академика И. П. Павлова, Россия
² Санкт-Петербургский государственный электротехнический университет «ЛЭТИ», Россия

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Introduction

Myelodysplastic syndrome (MDS) is a heterogeneous group of clonal bone marrow disorders characterized by ineffective hematopoiesis, and increased propensity to evolve to acute myeloid leukemia (AML). Currently allogeneic hematopoietic stem cell transplantation (allo-HSCT) is the only treatment option with curative potential in MDS patients. However, allo-HSCT is associated with risk of significant toxicity – 1-year non-relapse mortality (NRM) is reaching 17% to 25% [1, 2]. Thereby transplant- and disease-related risks should be carefully weighed against the benefits of transplantation. Several prognostic scoring indexes such as International prognostic scoring system (IPSS) [3], revised IPSS [4], WHO-classification-based IPSS (WPSS) [5] are widely used to predict MDS disease course and optimize timing of allo-HSCT according to disease related factors. Allo-HSCT is indicated in patients with high/very high and even in very low/ low or intermediate IPSS-R risk with poor features (poor risk cytogenetics, life-threatening cytopenias, severe transfusion dependence and persistently increasing blast count) [6]. Multiparametric prognostic models IPSS, WPSS and IPSS-R were developed to assess disease risk at diagnosis. In contrast disease related index (DRI) [7] and prognostic models defined by Kroeger et al. [8] and Armand et al. [9] were designed directly for the posttransplant outcome evaluation. Patient-related risk factors such as comorbidities and age should be also taken into consideration. They are included in several prognostic scoring systems such as EBMT score [10], Pretransplant Assessment of Mortality score (PAM) [11] or Hematopoietic Cell Transplantation-specific Comorbidity Index HCT-CI [12]. Here we evaluate aforementioned disease- and transplant-related prognostic indexes in MDS patients treated with allo-HSCT in one center.

Patients and methods

All consecutive primary allogeneic transplants performed for the diagnosis MDS in the time period 2002-2018 and complete information to calculate all of the prognostic indexes were included in the analysis. Pediatric patients and patients transformed to AML were excluded. Main patient characteristics, transplantation parameters, outcomes and complications are summarized in Table 1.

Median of age was 44 years (range 18-67). Twenty four percent of patients were grafted from a matched related donor, and 73% were transplanted from the 9-10/10 HLA-matched unrelated donors. MDS with excess blasts I or II was documented in seventy-six percent of the patients. Twenty-two percent were treated with hypomethylating drugs before transplant. Conditioning regimen was myeloablative in 1/4 of patients, and consisted of oral busulfan 16 mg/kg and cyclophosphamide 120 mg/kg. Reduced-intensity conditioning comprised fludarabine 180 mg/m² and oral busulfan 8-10 mg/kg. The reduced-intensity conditioning was used in all the patients after first analysis of the RICMAC trial [2] in 2012. Graft-versus-host disease (GVHD) prophylaxis included posttransplant cyclophosphamide in 37% of patients, while the rest of them received calcineurin-based prophylaxis with short-course methotrexate, or mycophenolate mofetil and antithymocyte globulin in case of unrelated grafts.

Table 1. Patient characteristics and overall transplantation outcomes

Clinical outcomes

Time-to-disease relapse, acute GVHD (aGVHD), moderate to severe GVHD (chGVHD), non-relapse mortality (NRM), overall survival (OS), event-free survival (EFS), and GVHD-relapse free survival (GRFS) were defined as the time from transplantation to the event. Graft failure without evidence of the disease after transplantation was not considered an event. Patients were censored at the time of last contact or a second transplantation for all outcomes. The disease relapse was defined as morphologic or cytogenetic evidence of disease with pre-transplant characteristics. Disease staging, including bone marrow aspirate, was routinely performed on days +30,+60,+100, +180, +365 post-transplant. Primary graft failure was defined as the complete absence of donor chimerism in bone marrow aspirate by day +40. Time to engraftment was calculated as time from HSCT to unsupported neutrophil count >500/ul and white blood cell count >1000/ul for 3 consecutive days. Toxicity was assessed with CTCAE ver. 4.03. Sepsis and severe sepsis were diagnosed based on International Guidelines for Management of Severe Sepsis and Septic Shock [13]. Invasive mycosis was diagnosed in case of probable or proven infection according to EORTC/MSG guidelines [14]. HCT-CI [12], DRI [7], IPSS [3], IPSS-R [4], WPSS [5], PAM [11], Armand et al. risk score [9], Kroeger et al. risk score [8] were calculated based on the published scoring systems.

Statistical Analysis

All tests were two-sided, and differences with p values less than 0.05 were considered significant. The difference in grading between indexes was accessed using Friedman test. The survival distributions for OS, EFS, GRFS were calculated using Kaplan-Meier methodology with 95% confidence intervals. Appropriate survival curves are provided in Supplementary files (see online version) Cumulative incidence analysis with competing risks was used for relapse and NRM. Five-year OS was used as an outcome to test all prognostic systems, because most of them were created based overall survival with follow up for 5 years and more [3, 4, 5, 9]. The univariate comparisons were made using the log-rank test. Proportional hazard modeling was used for the multivariate analysis. Based on the number of events 3 most significant factors from univariate analysis were included in the model. The MDS risk indexes were added in the series of tests. The final multivariate confidence intervals are the result of meta-analysis with fixed effect modeling. The heterogeneity of confidence intervals was tested with Cochran Q test. The C-statistic for the predictive factors was produced from logistic regression with death during five years after transplantation as an outcome. The predictive values were presented as area under the curve (AUC) with confidence intervals. Analyses were conducted in R 3.4.1 and SAS 9.3 (SAS Institute, Inc.).

Results

Distribution of patients by different scoring systems

We analyzed the distribution of patients by disease specific scoring systems such as IPSS, WPSS and IPSS-R and MDS prognostic indexes for patients undergoing allo-HSCT developed by Kroeger et al. and Armand et al. (Fig. 1). Fifty-four percent of patients were transplanted in high or very high IPSS-R risk. Forty-eight percent of patients with high/very high WPSS or IPSS-R risk were reclassified into intermediate risk according to pretransplant Kroeger et al. MDS score and 60% into intermediate risk, according to pretransplant Armand et al. score. There was a difference between disease- and pretransplant prognostic systems especially in distinction between high/very high and intermediate risk (p<0.001).

Figure 1. Distribution of patients by different prognostic scoring systems

Clinical outcomes

Platelet and leukocyte engraftment was documented in 48 (81%) of patients. Primary graft failure was observed in six cases (10%). Four patients out of them died (in one case, due to disease progression, and three patients deceased due to infections). The median time to leukocyte engraftment was 18 days (range 11-30), neutrophil engraftment, 20 days (range 10-30), platelet engraftment, 17 days (range 11-130). Overall, 50% of patients developed aGVHD with severe aGVHD grade 3-4 registered only in 15% of cases. The rate of chronic GVHD was 30%, which proved to be extensive in 28% of the patients (Table 1).

Cumulative incidence of relapse at 5 years was 37% (95% CI 25-57%). The cumulative incidence of non-relapse mortality (NRM) at 1 year was 25% (95% CI 16-40%). Thirty patients died during the follow-up study. The main reasons of death were disease progression or relapse in 26%; GVHD, 26%; infections, 37%; hemorrhagic events, 7%; acute myocardial infarction, in 4% of cases.

With a median follow-up of 36 months (range 3 to 135), the 5-year OS, EFS and GRFS was 34%, 33% and 29%, respectively. In univariate analysis, the significant factors for prolonged OS were as follows: aGVHD grade 1-2 (62% vs 18% p=0.004), quantities of donor СD34+ cells (p=0.006), and absence of septic episodes before engraftment (44 % vs 17%, p=0.003). The disease-specific prognostic indexes (IPSS, WPSS, IPSS-R), and transplant comorbidity indexes (PAM, EBMT, HCT-CI) did not predict OS . However, differences in OS rates between the risk groups according to disease-related prognostic systems such as Disease-Related Index, DRI (p=0.049), and risk score by Kroeger et al. (p=0.071) have shown a trend towards statistical significance (Supplement, Fig. 1-7. The supplemental files could be found in electronic version of this paper at www.cttjournal.com). The 5-year OS in low risk group, according to transplant risk score proposed by Kroeger et al. was 61%, thus being significantly higher compared to intermediate and high/very high risk – 26% (p=0.041). Surprisingly, we found no difference in OS between intermediate and high/very high risk groups (28% and 22%, respectively). This might be a reason for the failure of the index used by Kroeger et al. to achieve statistical significance. Interestingly, that the causes of death were nearly the same in both risk groups, i.e., ca. 50% of patients died due to transplant related factors.

ROC analysis shows influence of different prognostic systems and factors upon OS in the MDS patients. Amount of transplanted CD34+ donor cells proved to be the only factor which significantly affected transplant outcome (p=0.006) in this analysis (Fig. 2).

Figure 2. Influence of different prognostic systems and factors on OS in MDS patients, receiver-operating-curve (ROC) analysis

Note: C-statistics for the potential predictors of overall survival. Results of the ROC analysis treated in logistic regression with 5-year overall survival as an outcome. The non-significant parameters (p>0.05) are shown in grey. The significant (p<0.05) parameters are shown in black. The 95% confidence intervals of sensitivity and specificity are produced from individual results of all the parameters tested. C-statistic values of the variables were: CD34 positive cells in the graft 0.7080 (95% CI 0.5740-0.8421), Kroger et al. 0.5862 (95% CI 0.4391-0.7333), Armand et al. 0.5339 (95% CI 0.3850-0.6828), IPSS 0.5534 (95% CI 0.4121-0.6948), WPSS 0.5672 (95% CI 0.4354-0.6991), IPSS-R 0.5885 (0.4430-0.7340), DRI 0.5747 (0.4429-0.7065), EBMT 0.5230 (0.3758-0.6702), serum ferritin 0.4500 (0.2861-0.6139), PAM index 0.5584 (0.4037-0.7131), CRP before conditioning 0.4845 (0.3234-0.6456).

However, only presence of aGVHD grade 1-2 (p=0.013), absence of septic episodes (p=0.006), and DRI (p=0.037) retained their statistical significance in the multivariate analysis (Fig. 3). Other prognostic scores, except of DRI, did not show a statistical significance.

Figure 3. Analysis of the prognostic value of risk indexes in the multivariate model

Note: Multivariate analysis of overall survival. Acute GVHD, graft CD34+ cells and sepsis in aplasia were included based on univariate selection of the most predictive variables. The indexes were added as the fourth co-variable separately in a series of tests. The cumulative confidence intervals for the clinical variables were produced with fixed effect model from the individual hazards in the series.

Discussion

The major question in every MDS patient with currently existing treatments is whether he will benefit from allo-HSCT. Despite the fact that all existing treatments in most cases lead to only temporary responses, the results of allo-HSCT in MDS unfortunately are also one of the most disappointing compared to other diseases [15]. According to our 5-year observation data, the OS level in allotransplanted MDS patients is 34%. The other studies are showing nearly the same results: from 45% to 37% [1, 16]. This is due to relatively high NRM [3], but also due to high relapse rate [2, 17]. Currently used indexes of the natural course of the disease such as IPSS, WPSS, IPSS-R are established to evaluate risk of death and transformation to acute myeloid leukemia in untreated MDS patients [3, 4, 5]. All of these indexes are well validated in large patient cohorts [17]. However, their role in predicting the outcome after allo-HSCT is not so well defined.

Lee et al. [18] evaluated prognostic impact of IPSS before allo-HSCT. The authors showed significant differences in OS after allo-HSCT between low/intermediate and intermediate/high groups. Further it was shown that WPSS has a relevant prognostic value in posttransplant outcome of patients with MDS [19]. Modified prognostic model IPSS-R was assessed pre-transplant as a predictor of transplant outcome by C. Scheid et al. [20]. In that study, IPSS-R significantly influenced OS after allo-HSCT, but OS in high and intermediate groups were comparable: 47% and 44%, respectively. This was due to high and comparable NRM in these groups. In our study we have also observed high NRM in the favorable prognostic groups based on IPSS or IPSS-R.

The potential causes for early mortality in this group are relatively well discussed in the literature. They include primary graft failure [21], iron overload which results in higher incidence of liver veno-occlusive disease [22] and infectious complications [23]. It should be noted that, according to our data, the rate of primary graft failure is 10% being considered relatively high. The incidence of graft failure varies from 2 to 13% [2, 16, 24]. We didn’t find any correlation between rate of graft failure and type of stem cell source or rate of СD34+ cells in the graft, as reported in previous studies [21]. According to the results of large study by Olsson et al. [21], MDS diagnosis itself is associated with increased risk of graft failure, along with other hematologic malignancies, e.g., myeloproliferative disorders and chronic lymphocytic leukemia. Poor graft function may be another documented cause of NRM that leads to increased incidence of opportunistic infections and hemorrhagic complications [25]. Thus, high NRM rate was the main reason of non-significant predictive value of classical indexes after allo-HSCT found in our study.

A number of indexes accounting for NRM based on previous treatment burden, like as duration of the disease in EBMT index, or comorbidity burden, like in HCT-CI, or prediction of viral reactivations based on serological markers, like in PAM. However, there are conflicting results about influence of the comorbidity indexes on OS in MDS patients. Guilfoyle et al. did not find associations between HCT-CI and OS in MDS patients [26]. On the other hand, a large retrospective study showed that EBMT score accurately predicted OS and NRM [27]. In the present study, we have not observed any predictive impact of these indexes on the disease outcome. The published data and results of our study indicate that biological mechanisms behind NRM might be in certain cases different in MDS compared to the other diseases [28].

Several new prognostic indexes have been recently developed aiming for precise evaluation of transplant outcome in MDS patients. Kroeger et al. have combined the disease-related factors (cytogenetics, blood blasts, and platelets) and patient-related factors (performance status and age) into a common prognostic system [8]. Armand et al. added ferritin level and type of a conditioning regimen to the disease-related risk factors [9]. The disease risk index was another prognostic system evaluated in our study. It includes cytogenetics and remission status of MDS patients at transplant [7]. These indexes, except of DRI, were assessed in large data sets to specifically account for the risk of relapse and the risk of NRM. There is only a limited number of studies validating these indexes [29]. Interestingly, about half of IPSS-R high/very high risk patients were reclassified as more favorable category, the intermediate-1, according to risk score by Kroeger et al. and Armand et al. [8, 9]. Thereby, the disease- and transplant-specific scoring systems determine the transplant outcome in different ways. According to our data, only DRI significantly influenced OS values among all the mentioned prognostic scores. In our study, these transplant-specific indexes were shown to define well the group with good prognosis and adverse prognosis. However, we observed that clinical prognosis for the intermediate group proved to be as adverse as for the high-risk patients.

Thus, our study indicates that current prognostic indexes do not well define the intermediate prognosis. It is likely that most of the heterogeneity of the disease fall into this category, including patients with stromal and miRNA signaling deficiency [30], pyroptosis of hematopoietic stem cells [31], certain mutations without cytogenetic abnormalities [32]. Any of these pathogenetic variants might manifest in different mechanisms of NRM and relapse risk. Pooling the patients into large cohorts alleviate these differences by creation of risk indexes. However, small-group or individual prediction might not be so accurate, due to the causes mentioned above. Thus, future development of indexes and predictive systems for allo-HSCT should incorporate molecular data, at least, for the intermediate risk groups in MDS.

Conclusion

our relatively small single-center study, we have observed little predictive value of currently existing scoring systems, particularly due to adverse results in the intermediate risk patients. Further characterization of this “intermediate” patents is required to broaden the clinical application of the scoring systems for individual treatment planning.

Acknowledgments

We thank our patients, research and medical staff for making this study possible. This work was done as part of Russian Science Foundation grant №17-75-20145.

Disclosure statement

Authors confirm the absence of any conflicts of interests.

References

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Introduction

Myelodysplastic syndrome (MDS) is a heterogeneous group of clonal bone marrow disorders characterized by ineffective hematopoiesis, and increased propensity to evolve to acute myeloid leukemia (AML). Currently allogeneic hematopoietic stem cell transplantation (allo-HSCT) is the only treatment option with curative potential in MDS patients. However, allo-HSCT is associated with risk of significant toxicity – 1-year non-relapse mortality (NRM) is reaching 17% to 25% [1, 2]. Thereby transplant- and disease-related risks should be carefully weighed against the benefits of transplantation. Several prognostic scoring indexes such as International prognostic scoring system (IPSS) [3], revised IPSS [4], WHO-classification-based IPSS (WPSS) [5] are widely used to predict MDS disease course and optimize timing of allo-HSCT according to disease related factors. Allo-HSCT is indicated in patients with high/very high and even in very low/ low or intermediate IPSS-R risk with poor features (poor risk cytogenetics, life-threatening cytopenias, severe transfusion dependence and persistently increasing blast count) [6]. Multiparametric prognostic models IPSS, WPSS and IPSS-R were developed to assess disease risk at diagnosis. In contrast disease related index (DRI) [7] and prognostic models defined by Kroeger et al. [8] and Armand et al. [9] were designed directly for the posttransplant outcome evaluation. Patient-related risk factors such as comorbidities and age should be also taken into consideration. They are included in several prognostic scoring systems such as EBMT score [10], Pretransplant Assessment of Mortality score (PAM) [11] or Hematopoietic Cell Transplantation-specific Comorbidity Index HCT-CI [12]. Here we evaluate aforementioned disease- and transplant-related prognostic indexes in MDS patients treated with allo-HSCT in one center.

Patients and methods

All consecutive primary allogeneic transplants performed for the diagnosis MDS in the time period 2002-2018 and complete information to calculate all of the prognostic indexes were included in the analysis. Pediatric patients and patients transformed to AML were excluded. Main patient characteristics, transplantation parameters, outcomes and complications are summarized in Table 1.

Median of age was 44 years (range 18-67). Twenty four percent of patients were grafted from a matched related donor, and 73% were transplanted from the 9-10/10 HLA-matched unrelated donors. MDS with excess blasts I or II was documented in seventy-six percent of the patients. Twenty-two percent were treated with hypomethylating drugs before transplant. Conditioning regimen was myeloablative in 1/4 of patients, and consisted of oral busulfan 16 mg/kg and cyclophosphamide 120 mg/kg. Reduced-intensity conditioning comprised fludarabine 180 mg/m² and oral busulfan 8-10 mg/kg. The reduced-intensity conditioning was used in all the patients after first analysis of the RICMAC trial [2] in 2012. Graft-versus-host disease (GVHD) prophylaxis included posttransplant cyclophosphamide in 37% of patients, while the rest of them received calcineurin-based prophylaxis with short-course methotrexate, or mycophenolate mofetil and antithymocyte globulin in case of unrelated grafts.

Table 1. Patient characteristics and overall transplantation outcomes

Clinical outcomes

Time-to-disease relapse, acute GVHD (aGVHD), moderate to severe GVHD (chGVHD), non-relapse mortality (NRM), overall survival (OS), event-free survival (EFS), and GVHD-relapse free survival (GRFS) were defined as the time from transplantation to the event. Graft failure without evidence of the disease after transplantation was not considered an event. Patients were censored at the time of last contact or a second transplantation for all outcomes. The disease relapse was defined as morphologic or cytogenetic evidence of disease with pre-transplant characteristics. Disease staging, including bone marrow aspirate, was routinely performed on days +30,+60,+100, +180, +365 post-transplant. Primary graft failure was defined as the complete absence of donor chimerism in bone marrow aspirate by day +40. Time to engraftment was calculated as time from HSCT to unsupported neutrophil count >500/ul and white blood cell count >1000/ul for 3 consecutive days. Toxicity was assessed with CTCAE ver. 4.03. Sepsis and severe sepsis were diagnosed based on International Guidelines for Management of Severe Sepsis and Septic Shock [13]. Invasive mycosis was diagnosed in case of probable or proven infection according to EORTC/MSG guidelines [14]. HCT-CI [12], DRI [7], IPSS [3], IPSS-R [4], WPSS [5], PAM [11], Armand et al. risk score [9], Kroeger et al. risk score [8] were calculated based on the published scoring systems.

Statistical Analysis

All tests were two-sided, and differences with p values less than 0.05 were considered significant. The difference in grading between indexes was accessed using Friedman test. The survival distributions for OS, EFS, GRFS were calculated using Kaplan-Meier methodology with 95% confidence intervals. Appropriate survival curves are provided in Supplementary files (see online version) Cumulative incidence analysis with competing risks was used for relapse and NRM. Five-year OS was used as an outcome to test all prognostic systems, because most of them were created based overall survival with follow up for 5 years and more [3, 4, 5, 9]. The univariate comparisons were made using the log-rank test. Proportional hazard modeling was used for the multivariate analysis. Based on the number of events 3 most significant factors from univariate analysis were included in the model. The MDS risk indexes were added in the series of tests. The final multivariate confidence intervals are the result of meta-analysis with fixed effect modeling. The heterogeneity of confidence intervals was tested with Cochran Q test. The C-statistic for the predictive factors was produced from logistic regression with death during five years after transplantation as an outcome. The predictive values were presented as area under the curve (AUC) with confidence intervals. Analyses were conducted in R 3.4.1 and SAS 9.3 (SAS Institute, Inc.).

Results

Distribution of patients by different scoring systems

We analyzed the distribution of patients by disease specific scoring systems such as IPSS, WPSS and IPSS-R and MDS prognostic indexes for patients undergoing allo-HSCT developed by Kroeger et al. and Armand et al. (Fig. 1). Fifty-four percent of patients were transplanted in high or very high IPSS-R risk. Forty-eight percent of patients with high/very high WPSS or IPSS-R risk were reclassified into intermediate risk according to pretransplant Kroeger et al. MDS score and 60% into intermediate risk, according to pretransplant Armand et al. score. There was a difference between disease- and pretransplant prognostic systems especially in distinction between high/very high and intermediate risk (p<0.001).

Figure 1. Distribution of patients by different prognostic scoring systems

Clinical outcomes

Platelet and leukocyte engraftment was documented in 48 (81%) of patients. Primary graft failure was observed in six cases (10%). Four patients out of them died (in one case, due to disease progression, and three patients deceased due to infections). The median time to leukocyte engraftment was 18 days (range 11-30), neutrophil engraftment, 20 days (range 10-30), platelet engraftment, 17 days (range 11-130). Overall, 50% of patients developed aGVHD with severe aGVHD grade 3-4 registered only in 15% of cases. The rate of chronic GVHD was 30%, which proved to be extensive in 28% of the patients (Table 1).

Cumulative incidence of relapse at 5 years was 37% (95% CI 25-57%). The cumulative incidence of non-relapse mortality (NRM) at 1 year was 25% (95% CI 16-40%). Thirty patients died during the follow-up study. The main reasons of death were disease progression or relapse in 26%; GVHD, 26%; infections, 37%; hemorrhagic events, 7%; acute myocardial infarction, in 4% of cases.

With a median follow-up of 36 months (range 3 to 135), the 5-year OS, EFS and GRFS was 34%, 33% and 29%, respectively. In univariate analysis, the significant factors for prolonged OS were as follows: aGVHD grade 1-2 (62% vs 18% p=0.004), quantities of donor СD34+ cells (p=0.006), and absence of septic episodes before engraftment (44 % vs 17%, p=0.003). The disease-specific prognostic indexes (IPSS, WPSS, IPSS-R), and transplant comorbidity indexes (PAM, EBMT, HCT-CI) did not predict OS . However, differences in OS rates between the risk groups according to disease-related prognostic systems such as Disease-Related Index, DRI (p=0.049), and risk score by Kroeger et al. (p=0.071) have shown a trend towards statistical significance (Supplement, Fig. 1-7. The supplemental files could be found in electronic version of this paper at www.cttjournal.com). The 5-year OS in low risk group, according to transplant risk score proposed by Kroeger et al. was 61%, thus being significantly higher compared to intermediate and high/very high risk – 26% (p=0.041). Surprisingly, we found no difference in OS between intermediate and high/very high risk groups (28% and 22%, respectively). This might be a reason for the failure of the index used by Kroeger et al. to achieve statistical significance. Interestingly, that the causes of death were nearly the same in both risk groups, i.e., ca. 50% of patients died due to transplant related factors.

ROC analysis shows influence of different prognostic systems and factors upon OS in the MDS patients. Amount of transplanted CD34+ donor cells proved to be the only factor which significantly affected transplant outcome (p=0.006) in this analysis (Fig. 2).

Figure 2. Influence of different prognostic systems and factors on OS in MDS patients, receiver-operating-curve (ROC) analysis

Note: C-statistics for the potential predictors of overall survival. Results of the ROC analysis treated in logistic regression with 5-year overall survival as an outcome. The non-significant parameters (p>0.05) are shown in grey. The significant (p<0.05) parameters are shown in black. The 95% confidence intervals of sensitivity and specificity are produced from individual results of all the parameters tested. C-statistic values of the variables were: CD34 positive cells in the graft 0.7080 (95% CI 0.5740-0.8421), Kroger et al. 0.5862 (95% CI 0.4391-0.7333), Armand et al. 0.5339 (95% CI 0.3850-0.6828), IPSS 0.5534 (95% CI 0.4121-0.6948), WPSS 0.5672 (95% CI 0.4354-0.6991), IPSS-R 0.5885 (0.4430-0.7340), DRI 0.5747 (0.4429-0.7065), EBMT 0.5230 (0.3758-0.6702), serum ferritin 0.4500 (0.2861-0.6139), PAM index 0.5584 (0.4037-0.7131), CRP before conditioning 0.4845 (0.3234-0.6456).

However, only presence of aGVHD grade 1-2 (p=0.013), absence of septic episodes (p=0.006), and DRI (p=0.037) retained their statistical significance in the multivariate analysis (Fig. 3). Other prognostic scores, except of DRI, did not show a statistical significance.

Figure 3. Analysis of the prognostic value of risk indexes in the multivariate model

Note: Multivariate analysis of overall survival. Acute GVHD, graft CD34+ cells and sepsis in aplasia were included based on univariate selection of the most predictive variables. The indexes were added as the fourth co-variable separately in a series of tests. The cumulative confidence intervals for the clinical variables were produced with fixed effect model from the individual hazards in the series.

Discussion

The major question in every MDS patient with currently existing treatments is whether he will benefit from allo-HSCT. Despite the fact that all existing treatments in most cases lead to only temporary responses, the results of allo-HSCT in MDS unfortunately are also one of the most disappointing compared to other diseases [15]. According to our 5-year observation data, the OS level in allotransplanted MDS patients is 34%. The other studies are showing nearly the same results: from 45% to 37% [1, 16]. This is due to relatively high NRM [3], but also due to high relapse rate [2, 17]. Currently used indexes of the natural course of the disease such as IPSS, WPSS, IPSS-R are established to evaluate risk of death and transformation to acute myeloid leukemia in untreated MDS patients [3, 4, 5]. All of these indexes are well validated in large patient cohorts [17]. However, their role in predicting the outcome after allo-HSCT is not so well defined.

Lee et al. [18] evaluated prognostic impact of IPSS before allo-HSCT. The authors showed significant differences in OS after allo-HSCT between low/intermediate and intermediate/high groups. Further it was shown that WPSS has a relevant prognostic value in posttransplant outcome of patients with MDS [19]. Modified prognostic model IPSS-R was assessed pre-transplant as a predictor of transplant outcome by C. Scheid et al. [20]. In that study, IPSS-R significantly influenced OS after allo-HSCT, but OS in high and intermediate groups were comparable: 47% and 44%, respectively. This was due to high and comparable NRM in these groups. In our study we have also observed high NRM in the favorable prognostic groups based on IPSS or IPSS-R.

The potential causes for early mortality in this group are relatively well discussed in the literature. They include primary graft failure [21], iron overload which results in higher incidence of liver veno-occlusive disease [22] and infectious complications [23]. It should be noted that, according to our data, the rate of primary graft failure is 10% being considered relatively high. The incidence of graft failure varies from 2 to 13% [2, 16, 24]. We didn’t find any correlation between rate of graft failure and type of stem cell source or rate of СD34+ cells in the graft, as reported in previous studies [21]. According to the results of large study by Olsson et al. [21], MDS diagnosis itself is associated with increased risk of graft failure, along with other hematologic malignancies, e.g., myeloproliferative disorders and chronic lymphocytic leukemia. Poor graft function may be another documented cause of NRM that leads to increased incidence of opportunistic infections and hemorrhagic complications [25]. Thus, high NRM rate was the main reason of non-significant predictive value of classical indexes after allo-HSCT found in our study.

A number of indexes accounting for NRM based on previous treatment burden, like as duration of the disease in EBMT index, or comorbidity burden, like in HCT-CI, or prediction of viral reactivations based on serological markers, like in PAM. However, there are conflicting results about influence of the comorbidity indexes on OS in MDS patients. Guilfoyle et al. did not find associations between HCT-CI and OS in MDS patients [26]. On the other hand, a large retrospective study showed that EBMT score accurately predicted OS and NRM [27]. In the present study, we have not observed any predictive impact of these indexes on the disease outcome. The published data and results of our study indicate that biological mechanisms behind NRM might be in certain cases different in MDS compared to the other diseases [28].

Several new prognostic indexes have been recently developed aiming for precise evaluation of transplant outcome in MDS patients. Kroeger et al. have combined the disease-related factors (cytogenetics, blood blasts, and platelets) and patient-related factors (performance status and age) into a common prognostic system [8]. Armand et al. added ferritin level and type of a conditioning regimen to the disease-related risk factors [9]. The disease risk index was another prognostic system evaluated in our study. It includes cytogenetics and remission status of MDS patients at transplant [7]. These indexes, except of DRI, were assessed in large data sets to specifically account for the risk of relapse and the risk of NRM. There is only a limited number of studies validating these indexes [29]. Interestingly, about half of IPSS-R high/very high risk patients were reclassified as more favorable category, the intermediate-1, according to risk score by Kroeger et al. and Armand et al. [8, 9]. Thereby, the disease- and transplant-specific scoring systems determine the transplant outcome in different ways. According to our data, only DRI significantly influenced OS values among all the mentioned prognostic scores. In our study, these transplant-specific indexes were shown to define well the group with good prognosis and adverse prognosis. However, we observed that clinical prognosis for the intermediate group proved to be as adverse as for the high-risk patients.

Thus, our study indicates that current prognostic indexes do not well define the intermediate prognosis. It is likely that most of the heterogeneity of the disease fall into this category, including patients with stromal and miRNA signaling deficiency [30], pyroptosis of hematopoietic stem cells [31], certain mutations without cytogenetic abnormalities [32]. Any of these pathogenetic variants might manifest in different mechanisms of NRM and relapse risk. Pooling the patients into large cohorts alleviate these differences by creation of risk indexes. However, small-group or individual prediction might not be so accurate, due to the causes mentioned above. Thus, future development of indexes and predictive systems for allo-HSCT should incorporate molecular data, at least, for the intermediate risk groups in MDS.

Conclusion

our relatively small single-center study, we have observed little predictive value of currently existing scoring systems, particularly due to adverse results in the intermediate risk patients. Further characterization of this “intermediate” patents is required to broaden the clinical application of the scoring systems for individual treatment planning.

Acknowledgments

We thank our patients, research and medical staff for making this study possible. This work was done as part of Russian Science Foundation grant №17-75-20145.

Disclosure statement

Authors confirm the absence of any conflicts of interests.

References

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Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.</p> <h3>Пациенты и методы</h3> <p style="text-align: justify;">В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).</p> <h3>Результаты</h3> <p style="text-align: justify;">В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения. </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.</p>" ["ELEMENT_PREVIEW_PICTURE_FILE_TITLE"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["ELEMENT_DETAIL_PICTURE_FILE_ALT"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["ELEMENT_DETAIL_PICTURE_FILE_TITLE"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_META_TITLE"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_META_KEYWORDS"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_META_DESCRIPTION"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_PICTURE_FILE_ALT"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_PICTURE_FILE_TITLE"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_PICTURE_FILE_NAME"]=> string(100) "primenenie-standartnykh-i-novykh-prognosticheskikh-sistem-u-bolnykh-s-mielodisplasticheskim-sindromo" ["SECTION_DETAIL_PICTURE_FILE_ALT"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_DETAIL_PICTURE_FILE_TITLE"]=> string(317) "Применение стандартных и новых прогностических систем у больных с миелодиспластическим синдромом, подлежащих аллогенной трансплантации гемопоэтических стволовых клеток" ["SECTION_DETAIL_PICTURE_FILE_NAME"]=> string(100) "primenenie-standartnykh-i-novykh-prognosticheskikh-sistem-u-bolnykh-s-mielodisplasticheskim-sindromo" ["ELEMENT_PREVIEW_PICTURE_FILE_NAME"]=> string(100) "primenenie-standartnykh-i-novykh-prognosticheskikh-sistem-u-bolnykh-s-mielodisplasticheskim-sindromo" ["ELEMENT_DETAIL_PICTURE_FILE_NAME"]=> string(100) "primenenie-standartnykh-i-novykh-prognosticheskikh-sistem-u-bolnykh-s-mielodisplasticheskim-sindromo" } ["FIELDS"]=> array(1) { ["IBLOCK_SECTION_ID"]=> string(3) "121" } ["PROPERTIES"]=> array(18) { ["KEYWORDS"]=> array(36) { ["ID"]=> string(2) "19" ["TIMESTAMP_X"]=> string(19) "2015-09-03 10:46:01" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(27) "Ключевые слова" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(8) "KEYWORDS" ["DEFAULT_VALUE"]=> string(0) "" ["PROPERTY_TYPE"]=> string(1) "E" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "Y" ["XML_ID"]=> string(2) "19" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "4" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "Y" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" 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string(3) "285" [6]=> string(4) "1631" [7]=> string(2) "60" [8]=> string(2) "34" } ["DESCRIPTION"]=> array(9) { [0]=> string(0) "" [1]=> string(0) "" [2]=> string(0) "" [3]=> string(0) "" [4]=> string(0) "" [5]=> string(0) "" [6]=> string(0) "" [7]=> string(0) "" [8]=> string(0) "" } ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(9) { [0]=> string(3) "147" [1]=> string(3) "146" [2]=> string(4) "1633" [3]=> string(4) "1634" [4]=> string(4) "1635" [5]=> string(3) "285" [6]=> string(4) "1631" [7]=> string(2) "60" [8]=> string(2) "34" } ["~DESCRIPTION"]=> array(9) { [0]=> string(0) "" [1]=> string(0) "" [2]=> string(0) "" [3]=> string(0) "" [4]=> string(0) "" [5]=> string(0) "" [6]=> string(0) "" [7]=> string(0) "" [8]=> string(0) "" } ["~NAME"]=> string(12) "Авторы" ["~DEFAULT_VALUE"]=> string(0) "" } ["AUTHOR_RU"]=> array(36) { ["ID"]=> string(2) "25" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(12) "Авторы" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(9) "AUTHOR_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "25" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21571" ["VALUE"]=> array(2) { ["TEXT"]=> string(334) "<p>Елена В. Морозова, Мария В. Барабанщикова, Николай Ю. Цветков, Ксения В. Мельситова, Юлия В. Рудницкая, Елена И. Дарская, Сергей Н. Бондаренко, Иван С. Моисеев, Борис В. Афанасьев</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(322) "

Елена В. Морозова, Мария В. Барабанщикова, Николай Ю. Цветков, Ксения В. Мельситова, Юлия В. Рудницкая, Елена И. Дарская, Сергей Н. Бондаренко, Иван С. Моисеев, Борис В. Афанасьев

" ["TYPE"]=> string(4) "HTML" } ["~DESCRIPTION"]=> string(0) "" ["~NAME"]=> string(12) "Авторы" ["~DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } } ["ORGANIZATION_RU"]=> array(36) { ["ID"]=> string(2) "26" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(22) "Организации" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(15) "ORGANIZATION_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "26" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21572" ["VALUE"]=> array(2) { ["TEXT"]=> string(366) "<p>НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета им. И. П. Павлова, Санкт-Петербург, Россия</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(354) "

НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета им. И. П. Павлова, Санкт-Петербург, Россия

" ["TYPE"]=> string(4) "HTML" } ["~DESCRIPTION"]=> string(0) "" ["~NAME"]=> string(22) "Организации" ["~DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } } ["SUMMARY_RU"]=> array(36) { ["ID"]=> string(2) "27" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(29) "Описание/Резюме" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(10) "SUMMARY_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "27" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21573" ["VALUE"]=> array(2) { ["TEXT"]=> string(3764) "<p style="text-align: justify;">Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.</p> <h3>Пациенты и методы</h3> <p style="text-align: justify;">В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).</p> <h3>Результаты</h3> <p style="text-align: justify;">В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения. </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(3637) "

Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.

Пациенты и методы

В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).

Результаты

В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения.

Ключевые слова

Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.

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Elena V. Morozova, Maria V. Barabanshikova, Nikolai Yu. Tcvetkov, Ksenia V. Melsitova, Julia V. Rudnitskaya, Elena I. Darskaya, Sergey N. Bondarenko, Ivan S. Moiseev, Boris V. Afanasyev

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R. Gorbacheva Memorial Research Institute for Pediatric Oncology, Hematology and Transplantation, The First Pavlov St. Petersburg State Medical University, St. Petersburg, Russian Federation

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Several prognostic indexes were developed to predict outcome in patients with myelodysplastic syndrome (MDS). The aim of our study was to evaluate prognostic impact of disease- and transplant-specific indexes on the results of allogeneic hematopoietic stem cell transplantation (allo-HSCT) in MDS patients.

Patients and methods

A retrospective cohort of fifty-nine MDS patients (excluding secondary acute myeloid leukemia) and treated with allo-HSCT was used to evaluate the predictive value of the following prognostic indexes: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), prognostic systems developed by Kroeger et al., Armand et al., Pretransplant Assessment of Mortality Score (PAM), EBMT risk score and Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI).

Results

There was a significant difference in risk estimation between indexes (p<0.001). Clinical factors significant for overall survival (OS) in the univariate and multivariate analyses were as follows: acute graft-versus-host disease (GVHD) grade I-II (HR 0.223, 95% CI 0.059-0.721, p=0.0134) and occurrence of sepsis during aplasia (HR 3.636, 95% CI 1.438-8.673, p=0.0059). Despite significant impact of CD34+ cell contents in hematopoietic graft (p=0.006) revealed in ROC analysis, only DRI remained a significant predictor of 5-year OS in the multivariate model (HR 1.857, 95% CI 1.036-3.328, p=0.037). Inferiority of other MDS-specific indexes to predict the outcome for allo-HSCT seems to be associated with adverse results in the intermediate risk group. In conclusion, we presume a need for further characterization of the intermediate risk patients when predicting the therapy outcomes.

Keywords

Myelodysplastic syndrome, allogeneic hematopoietic stem cell transplantation, prognostic indexes, risk estimation.

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"37" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21584" ["VALUE"]=> array(2) { ["TEXT"]=> string(204) "<p>Elena V. Morozova, Maria V. Barabanshikova, Nikolai Yu. Tcvetkov, Ksenia V. Melsitova, Julia V. Rudnitskaya, Elena I. Darskaya, Sergey N. Bondarenko, Ivan S. Moiseev, Boris V. Afanasyev</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(192) "

Elena V. Morozova, Maria V. Barabanshikova, Nikolai Yu. Tcvetkov, Ksenia V. Melsitova, Julia V. Rudnitskaya, Elena I. Darskaya, Sergey N. Bondarenko, Ivan S. Moiseev, Boris V. Afanasyev

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Elena V. Morozova, Maria V. Barabanshikova, Nikolai Yu. Tcvetkov, Ksenia V. Melsitova, Julia V. Rudnitskaya, Elena I. Darskaya, Sergey N. Bondarenko, Ivan S. Moiseev, Boris V. Afanasyev

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Several prognostic indexes were developed to predict outcome in patients with myelodysplastic syndrome (MDS). The aim of our study was to evaluate prognostic impact of disease- and transplant-specific indexes on the results of allogeneic hematopoietic stem cell transplantation (allo-HSCT) in MDS patients.

Patients and methods

A retrospective cohort of fifty-nine MDS patients (excluding secondary acute myeloid leukemia) and treated with allo-HSCT was used to evaluate the predictive value of the following prognostic indexes: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), prognostic systems developed by Kroeger et al., Armand et al., Pretransplant Assessment of Mortality Score (PAM), EBMT risk score and Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI).

Results

There was a significant difference in risk estimation between indexes (p<0.001). Clinical factors significant for overall survival (OS) in the univariate and multivariate analyses were as follows: acute graft-versus-host disease (GVHD) grade I-II (HR 0.223, 95% CI 0.059-0.721, p=0.0134) and occurrence of sepsis during aplasia (HR 3.636, 95% CI 1.438-8.673, p=0.0059). Despite significant impact of CD34+ cell contents in hematopoietic graft (p=0.006) revealed in ROC analysis, only DRI remained a significant predictor of 5-year OS in the multivariate model (HR 1.857, 95% CI 1.036-3.328, p=0.037). Inferiority of other MDS-specific indexes to predict the outcome for allo-HSCT seems to be associated with adverse results in the intermediate risk group. In conclusion, we presume a need for further characterization of the intermediate risk patients when predicting the therapy outcomes.

Keywords

Myelodysplastic syndrome, allogeneic hematopoietic stem cell transplantation, prognostic indexes, risk estimation.

" ["TYPE"]=> string(4) "HTML" } ["~DESCRIPTION"]=> string(0) "" ["~NAME"]=> string(21) "Description / Summary" ["~DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["DISPLAY_VALUE"]=> string(1982) "

Several prognostic indexes were developed to predict outcome in patients with myelodysplastic syndrome (MDS). The aim of our study was to evaluate prognostic impact of disease- and transplant-specific indexes on the results of allogeneic hematopoietic stem cell transplantation (allo-HSCT) in MDS patients.

Patients and methods

A retrospective cohort of fifty-nine MDS patients (excluding secondary acute myeloid leukemia) and treated with allo-HSCT was used to evaluate the predictive value of the following prognostic indexes: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), prognostic systems developed by Kroeger et al., Armand et al., Pretransplant Assessment of Mortality Score (PAM), EBMT risk score and Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI).

Results

There was a significant difference in risk estimation between indexes (p<0.001). Clinical factors significant for overall survival (OS) in the univariate and multivariate analyses were as follows: acute graft-versus-host disease (GVHD) grade I-II (HR 0.223, 95% CI 0.059-0.721, p=0.0134) and occurrence of sepsis during aplasia (HR 3.636, 95% CI 1.438-8.673, p=0.0059). Despite significant impact of CD34+ cell contents in hematopoietic graft (p=0.006) revealed in ROC analysis, only DRI remained a significant predictor of 5-year OS in the multivariate model (HR 1.857, 95% CI 1.036-3.328, p=0.037). Inferiority of other MDS-specific indexes to predict the outcome for allo-HSCT seems to be associated with adverse results in the intermediate risk group. In conclusion, we presume a need for further characterization of the intermediate risk patients when predicting the therapy outcomes.

Keywords

Myelodysplastic syndrome, allogeneic hematopoietic stem cell transplantation, prognostic indexes, risk estimation.

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R. Gorbacheva Memorial Research Institute for Pediatric Oncology, Hematology and Transplantation, The First Pavlov St. Petersburg State Medical University, St. Petersburg, Russian Federation

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R. Gorbacheva Memorial Research Institute for Pediatric Oncology, Hematology and Transplantation, The First Pavlov St. Petersburg State Medical University, St. Petersburg, Russian Federation

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Елена В. Морозова, Мария В. Барабанщикова, Николай Ю. Цветков, Ксения В. Мельситова, Юлия В. Рудницкая, Елена И. Дарская, Сергей Н. Бондаренко, Иван С. Моисеев, Борис В. Афанасьев

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Елена В. Морозова, Мария В. Барабанщикова, Николай Ю. Цветков, Ксения В. Мельситова, Юлия В. Рудницкая, Елена И. Дарская, Сергей Н. Бондаренко, Иван С. Моисеев, Борис В. Афанасьев

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Barabanshikova" ["LINK_ELEMENT_VALUE"]=> bool(false) } ["SUMMARY_RU"]=> array(37) { ["ID"]=> string(2) "27" ["TIMESTAMP_X"]=> string(19) "2015-09-02 18:01:20" ["IBLOCK_ID"]=> string(1) "2" ["NAME"]=> string(29) "Описание/Резюме" ["ACTIVE"]=> string(1) "Y" ["SORT"]=> string(3) "500" ["CODE"]=> string(10) "SUMMARY_RU" ["DEFAULT_VALUE"]=> array(2) { ["TEXT"]=> string(0) "" ["TYPE"]=> string(4) "HTML" } ["PROPERTY_TYPE"]=> string(1) "S" ["ROW_COUNT"]=> string(1) "1" ["COL_COUNT"]=> string(2) "30" ["LIST_TYPE"]=> string(1) "L" ["MULTIPLE"]=> string(1) "N" ["XML_ID"]=> string(2) "27" ["FILE_TYPE"]=> string(0) "" ["MULTIPLE_CNT"]=> string(1) "5" ["TMP_ID"]=> NULL ["LINK_IBLOCK_ID"]=> string(1) "0" ["WITH_DESCRIPTION"]=> string(1) "N" ["SEARCHABLE"]=> string(1) "N" ["FILTRABLE"]=> string(1) "N" ["IS_REQUIRED"]=> string(1) "N" ["VERSION"]=> string(1) "1" ["USER_TYPE"]=> string(4) "HTML" ["USER_TYPE_SETTINGS"]=> array(1) { ["height"]=> int(200) } ["HINT"]=> string(0) "" ["PROPERTY_VALUE_ID"]=> string(5) "21573" ["VALUE"]=> array(2) { ["TEXT"]=> string(3764) "<p style="text-align: justify;">Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.</p> <h3>Пациенты и методы</h3> <p style="text-align: justify;">В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).</p> <h3>Результаты</h3> <p style="text-align: justify;">В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения. </p> <h2>Ключевые слова</h2> <p style="text-align: justify;">Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.</p>" ["TYPE"]=> string(4) "HTML" } ["DESCRIPTION"]=> string(0) "" ["VALUE_ENUM"]=> NULL ["VALUE_XML_ID"]=> NULL ["VALUE_SORT"]=> NULL ["~VALUE"]=> array(2) { ["TEXT"]=> string(3637) "

Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.

Пациенты и методы

В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).

Результаты

В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения.

Ключевые слова

Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.

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Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.

Пациенты и методы

В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).

Результаты

В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения.

Ключевые слова

Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.

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                    [TEXT] => <p style="text-align: justify;">Аллогенная трансплантация костного мозга (алло-
ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными. </p>
<h2>Ключевые слова</h2>
<p style="text-align: justify;">Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид. </p>
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ТГСК) является потенциальной возможностью излечения злокачественных и незлокачественных заболеваний кроветворения. Для пациентов, у которых отсутствует HLA-совместимый сиблинг, можно использовать HLA-гаплоидентичного донора (гапло-ТГСК) в качестве альтернативного источника трансплантата. Преимуществом гапло-ТГСК является немедленная доступность донора для пациентов, которым необходимо выполнение трансплантации в короткие сроки. Кроме того, наличие родственного донора делает более доступной клеточную терапию после трансплантации. Также, большее несоответствие по генам HLA-системы в случае гаплоидентичной трансплантации, может потенциировать эффект «трансплантат против опухоли». В этом отчете представлен анализ результатов гапло-ТГСК, выполненных в нашем центре взрослым пациентам с различными злокачественными заболеваниями, при использовании неманипулированного трансплантата. На момент анализа медиана наблюдения составила 371 день (1-2219). Основным диагонозом был острый лейкоз. Шестидесяти семи пациентам (56%) гапло-ТГСК была выполнена в качестве терапии спасения. Общая выживаемость в течении 2 лет в исследуемой группе составила 40,3%. В частности, двухлетняя общая выживаемость у пациентов с ОЛЛ и ОМЛ в ремиссии заболевания, составила 57% и 46% соответственно в сравнении с 22% и 15% у пациентов с продвинутыми стадиями заболеваний. Безрецидивная выживаемость в течение 2 лет, а также выживаемость без проявлений оРТПХ и рецидива заболевания в общей группе составили 35,7% и 21% соответственно. Частота возникновения острой РТПХ II-IV степени и тяжелой РТПХ III-IV степени составили 19% и 10% соответственно. Частота хронической РТПХ составила 16%. Частота возникновения рецидива заболевания составила 21%. Трансплантационная летальность исследуемой группе 43%. В заключение необходимо отметить, что наши результаты показывают, что гапло-ТГСК с использованием неманипулированного трансплантата является приемлемым методом лечения взрослых пациентов с различными злокачественными заболеваниями кроветворения. Однако такие проблемы, как высокая частота неприживления, высокая трансплантационная летальность, а также посттрасплантационные рецидивы остаются чрезвычайно актуальными. 
Ключевые слова
Аллогенная трансплантация гемопоэтических стволовых клеток, гаплоидентичная, взрослые пациенты, общая выживаемость, рецидив после трансплантации, реакция «трансплантат против хозяина», неприживление трансплантатата, посттрансплантационный циклофосфамид. 
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Anastasia V. Beynarovich, Elena V. Babenko, Ivan S. Moiseev, Olesya V. Paina, Olga V. Pirogova, Tatiana A. Rudakova, Tatyana L. Gindina, Elena I. Darskaya, Elena V. Morozova, Sergey N. Bondarenko, Ludmila S. Zubarovskaya,
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R. Gorbacheva Memorial Research Institute of Children Oncology, Hematology and Transplantology at the First St. Petersburg State I. Pavlov Medical University
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                    [TEXT] => <p style="text-align: justify;">Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis. For patients who lack an HLA-matched sibling, HLA-haploidentical related donors (haplo-HSCT) can be considered as alternative sources of donor grafts. The benefits of haplo-HSCT include immediate donor availability for patients who are in urgent need of the transplant. Besides, an availability of a related donor makes post-transplant donor-derived cellular therapy more easily accessible. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. The aim of our study was to summarize our single-center experience of haplo-HSCT performed with non-manipulated grafts in adult patients with different malignant diseases. The study included a total of 119 patients with different hematological disorders subjected to haplo-HSCT. At the time of analysis, median follow-up was 371 days (1-2219). Most frequent diagnosis in transplanted patients was acute leukemia. 67 (56%) patients received haplo-HSCT as salvage therapy.<br>
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<h2>Keywords</h2>
<p style="text-align: justify;">Allogeneic hematopoietic stem cell transplantation, haploidentical, adult patients, overall survival, post-transplant relapse, graft-versus-host disease, graft failure, post-transplant cyclophosphamide.</p>

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Allogeneic HSCT (allo-HSCT) is potentially curative option for a wide variety of malignant and nonmalignant disorders of hematopoiesis. For patients who lack an HLA-matched sibling, HLA-haploidentical related donors (haplo-HSCT) can be considered as alternative sources of donor grafts. The benefits of haplo-HSCT include immediate donor availability for patients who are in urgent need of the transplant. Besides, an availability of a related donor makes post-transplant donor-derived cellular therapy more easily accessible. In addition, the greater HLA mismatch associated with haploidentical HSCT (haplo-HSCT) may potentiate graft-versus-tumor (GVT) effects. The aim of our study was to summarize our single-center experience of haplo-HSCT performed with non-manipulated grafts in adult patients with different malignant diseases. The study included a total of 119 patients with different hematological disorders subjected to haplo-HSCT. At the time of analysis, median follow-up was 371 days (1-2219). Most frequent diagnosis in transplanted patients was acute leukemia. 67 (56%) patients received haplo-HSCT as salvage therapy.

Overall survival with an observation term of 2 years was 40.3% for the general group. In particular, the two-year OS in patients transplanted in remissions of ALL and AML was 57% and 46% respectively as compared to 22% and 15% for the patients transplanted in adverse disease status). Two-year event-free survival (EFS) and GVHD-free/relapse-free survival (GRFS) group proved to be 35.7% and 21% respectively. The cumulative incidence of acute GVHD grade II-IV and severe aGVHD grade III-IV was 19% and 10% respectively. The cumulative incidence of chronic GVHD (cGVHD) was 16%.The cumulative incidence of relapse was 21%. The overall transplant-associated mortality was 43% in the studied group. In conclusion, our results show that unmanipulated haplo-HSCT is reasonable treatment option for adult patients with different malignant disorders of hematopoiesis. However, such problems as higher rate graft failure, increased nonrelapse mortality (NRM) and post-transplant relapses remain extremely relevant. 
Keywords
Allogeneic hematopoietic stem cell transplantation, haploidentical, adult patients, overall survival, post-transplant relapse, graft-versus-host disease, graft failure, post-transplant cyclophosphamide.

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<sup>2</sup> Санкт-Петербургский государственный электротехнический университет «ЛЭТИ», Россия</p>
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1 Первый Санкт-Петербургский государственный медицинский университет им. академика И. П. Павлова, Россия

2 Санкт-Петербургский государственный электротехнический университет «ЛЭТИ», Россия
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                    [TEXT] => <p style="text-align: justify;">Синусит после аллогенной трансплантации гемопоэтических стволовых клеток возникает в 22,2% случаев с более высокой частотой после 100 дня от алло-ТГСК, чем до 100 (р=0,006). Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина»
(р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии <i>Staphylococcus epidermidis </i>(30%), <i>Streptococcus viridans</i> (30%), грамотрицательные бактерии <i>Klebsiella pneumoniae</i> (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024).  </p>
<h2>Ключевые слова</h2>
<p style="text-align: justify;">Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.</p>
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Синусит после аллогенной трансплантации гемопоэтических стволовых клеток возникает в 22,2% случаев с более высокой частотой после 100 дня от алло-ТГСК, чем до 100 (р=0,006). Основными факторами риска возникновения синусита после аллогенной трансплантации гемопоэтических стволовых клеток являлись: синусит до алло-ТГСК (р <0,001), длительность нейтропении более 10 дней (р=0,054), наличие у пациентов острой (р=0,022) или хронической «реакции трансплантат против хозяина»
(р <0,001). Основными возбудителями острых синуситов у реципиентов алло-ТГСК в исследовании являлись грамположительные бактерии Staphylococcus epidermidis (30%), Streptococcus viridans (30%), грамотрицательные бактерии Klebsiella pneumoniae (17,5%). Монокультура бактерий преобладала до 100 дня от алло-ТГСК (р=0,011). У пациентов подросткового возраста чаще наблюдался полиэтиологичный характер возбудителей синусита по сравнению с группой «дети». Степень тяжести изменений околоносовых пазух на компьютерной томографии после 100 дня от алло-ТГСК более выражена (р=0,014), что находится в дисбалансе с меньшим количеством клинических симптомов синусита (р=0,008) и более частым течением синусита в легкой степени при оценке по визуальной аналоговой шкале (р=0,032) в этот период. Применение пункций верхнечелюстных пазух в сочетании с противомикробной терапией сокращает сроки лечения синусита у этих пациентов (р=0,024).  
Ключевые слова
Синусит, дети, трансплантация гемопоэтических клеток, клинические особенности.
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<sup>2</sup> St. Petersburg State Electrotechnical University LETI, St. Petersburg, Russia</p>
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1 Pavlov First St. Petersburg State Medical University, St. Petersburg, Russia

2 St. Petersburg State Electrotechnical University LETI, St. Petersburg, Russia
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                    [TEXT] => <p style="text-align: justify;">Sinusitis after allogeneic transplantation of hematopoietic stem cells occurs in 22.2% of cases being more frequent at >100 days following allo-HSCT, than at earlier terms (p=0.006). The main risk factors for sinusitis after allogeneic stem cell transplantation were as follows: sinusitis before allo-HSCT (p <0.001), neutropenia duration for more than 10 days (p=0.054), acute (p=0.022) or chronic graft-versus-host disease (p <0.001) in the patients. The main pathogens of sinusitis revealed in allo-HSCT recipients during the study were: Gram-positive <i>Staphylococcus epidermidis</i> (30%), <i>Streptococcus viridans</i> (30%); Gram-negative <i>Klebsiella pneumoniae</i> (17.5%). A monoculture of bacteria predominated within 100 days posttransplant (p=0.011). Poly-etiological origin of the causative bacterial agents in sinusitis was more likely in adolescent patients, in comparison to the younger children group. The severity of changes in paranasal sinuses, as registered with computed tomography after 100 days after allo-HSCT, was more pronounced (p=0.014) than at earlier terms, thus being discordant with less common clinical signs of sinusitis (p=0.008), and milder clinical course of sinusitis assessed by a visual analogue scale (p=0.032) during this period. Punctures of maxillary sinuses combined with antimicrobial therapy proved to shorten the duration of sinusitis treatment in these patients (p=0.024).</p>
<h2>Keywords</h2>
<p style="text-align: justify;">Sinusitis, children, hematopoietic stem cell transplantation.</p>
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Sinusitis after allogeneic transplantation of hematopoietic stem cells occurs in 22.2% of cases being more frequent at >100 days following allo-HSCT, than at earlier terms (p=0.006). The main risk factors for sinusitis after allogeneic stem cell transplantation were as follows: sinusitis before allo-HSCT (p <0.001), neutropenia duration for more than 10 days (p=0.054), acute (p=0.022) or chronic graft-versus-host disease (p <0.001) in the patients. The main pathogens of sinusitis revealed in allo-HSCT recipients during the study were: Gram-positive Staphylococcus epidermidis (30%), Streptococcus viridans (30%); Gram-negative Klebsiella pneumoniae (17.5%). A monoculture of bacteria predominated within 100 days posttransplant (p=0.011). Poly-etiological origin of the causative bacterial agents in sinusitis was more likely in adolescent patients, in comparison to the younger children group. The severity of changes in paranasal sinuses, as registered with computed tomography after 100 days after allo-HSCT, was more pronounced (p=0.014) than at earlier terms, thus being discordant with less common clinical signs of sinusitis (p=0.008), and milder clinical course of sinusitis assessed by a visual analogue scale (p=0.032) during this period. Punctures of maxillary sinuses combined with antimicrobial therapy proved to shorten the duration of sinusitis treatment in these patients (p=0.024).
Keywords
Sinusitis, children, hematopoietic stem cell transplantation.
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НИИ детской онкологии, гематологии и трансплантологии им. Р. М. Горбачевой Первого Санкт-Петербургского государственного медицинского университета им. И. П. Павлова, Санкт-Петербург, Россия
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                    [TEXT] => <p style="text-align: justify;">Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.</p>
<h3>Пациенты и методы</h3>
<p style="text-align: justify;">В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).</p>
<h3>Результаты</h3>
<p style="text-align: justify;">В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения.  </p>
<h2>Ключевые слова</h2>
<p style="text-align: justify;">Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.</p>
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Разработан ряд предиктивных индексов для прогнозирования исхода у пациентов с миелодиспластическим синдромом (МДС). Целью нашего исследования была оценка прогностического вклада показателей заболевания и трансплантации в результаты аллогенной трансплантации гемопоэтических клеток (ТГСК) пациентам с МДС.
Пациенты и методы
В ретроспективное исследование была включена группа из 53 пациентов с МДС (за исключением вторичного острого миелобластного лейкоза), леченных с применением алло-ТГСК. Целью работы была оценка предиктивной значимости следующих прогностических индексов: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), а также прогностической системы, предложенной Kroeger et al., Armand et al., индекса претрансплантационной оценки смертности (PAM), оценки риска по EBMT и ТГСК-специфичного индекса коморбидности (HCT-CI).
Результаты
В результате работы показана достоверная разница в оценке риска при сравнении отдельных индексов (p <0,001). Были отмечены следующие клинические факторы, значимые для общей выживаемости (ОВ) в одно- и многофакторном анализе: острая реакция «трансплантат против хозяина» (ОРТПХ) I-II степени (HR 0,.223; 95% CI 0.059-0,721; p=0,0134) и возникновение сепсиса в период аплазии (HR 3,636; 95% CI 1,438-8,673; p=0,0059). Несмотря на значительный вклад числа CD34+ клеток в трансплантате, (p=0,006), выявленного посредством ROC-анализа, только индекс DRI являлся существенным средством прогноза 5-летней выживаемости в многофакторной модели (HR 1,857; 95% CI 1,036-3,328; p=0,037). Более низкая эффективность других МДС-специфичных индексов в прогнозировании исходов алло-ТГСК связана, по-видимому, с неблагоприятными исходами в группе промежуточного риска. В заключение мы должны отметить необходимость дальнейшей характеризации пациентов промежуточной группы риска при прогнозировании исхода лечения.  
Ключевые слова
Миелодиспластический синдром, аллогенная трансплантация гемопоэтических стволовых клеток, прогностические индексы, оценка риска.
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Elena V. Morozova, Maria V. Barabanshikova, Nikolai Yu. Tcvetkov, Ksenia V. Melsitova, Julia V. Rudnitskaya, Elena I. Darskaya, Sergey N. Bondarenko, Ivan S. Moiseev, Boris V. Afanasyev
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R. Gorbacheva Memorial Research Institute for Pediatric Oncology, Hematology and Transplantation, The First Pavlov St. Petersburg State Medical University, St. Petersburg, Russian Federation
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                    [TEXT] => <p style="text-align: justify;">Several prognostic indexes were developed to predict outcome in patients with myelodysplastic syndrome (MDS). The aim of our study was to evaluate prognostic impact of disease- and transplant-specific indexes on the results of allogeneic hematopoietic stem cell transplantation (allo-HSCT) in MDS patients.</p>
<h3>Patients and methods</h3>
<p style="text-align: justify;">A retrospective cohort of fifty-nine MDS patients (excluding secondary acute myeloid leukemia) and treated with allo-HSCT was used to evaluate the predictive value of the following prognostic indexes: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), prognostic systems developed by Kroeger et al., Armand et al., Pretransplant Assessment of Mortality Score (PAM), EBMT risk score and Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI).</p>
<h3>Results</h3>
<p style="text-align: justify;">There was a significant difference in risk estimation between indexes (p<0.001). Clinical factors significant for overall survival (OS) in the univariate and multivariate analyses were as follows: acute graft-versus-host disease (GVHD) grade I-II (HR 0.223, 95% CI 0.059-0.721, p=0.0134) and occurrence of sepsis during aplasia (HR 3.636, 95% CI 1.438-8.673, p=0.0059). Despite significant impact of CD34+ cell contents in hematopoietic graft (p=0.006) revealed in ROC analysis, only DRI remained a significant predictor of 5-year OS in the multivariate model (HR 1.857, 95% CI 1.036-3.328, p=0.037). Inferiority of other MDS-specific indexes to predict the outcome for allo-HSCT seems to be associated with adverse results in the intermediate risk group. In conclusion, we presume a need for further characterization of the intermediate risk patients when predicting the therapy outcomes. </p>
<h2>Keywords</h2>
<p style="text-align: justify;">Myelodysplastic syndrome, allogeneic hematopoietic stem cell transplantation, prognostic indexes, risk estimation.  </p>
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Several prognostic indexes were developed to predict outcome in patients with myelodysplastic syndrome (MDS). The aim of our study was to evaluate prognostic impact of disease- and transplant-specific indexes on the results of allogeneic hematopoietic stem cell transplantation (allo-HSCT) in MDS patients.
Patients and methods
A retrospective cohort of fifty-nine MDS patients (excluding secondary acute myeloid leukemia) and treated with allo-HSCT was used to evaluate the predictive value of the following prognostic indexes: IPSS, IPSS-R, WPSS, Disease Risk Index (DRI), prognostic systems developed by Kroeger et al., Armand et al., Pretransplant Assessment of Mortality Score (PAM), EBMT risk score and Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI).
Results
There was a significant difference in risk estimation between indexes (p<0.001). Clinical factors significant for overall survival (OS) in the univariate and multivariate analyses were as follows: acute graft-versus-host disease (GVHD) grade I-II (HR 0.223, 95% CI 0.059-0.721, p=0.0134) and occurrence of sepsis during aplasia (HR 3.636, 95% CI 1.438-8.673, p=0.0059). Despite significant impact of CD34+ cell contents in hematopoietic graft (p=0.006) revealed in ROC analysis, only DRI remained a significant predictor of 5-year OS in the multivariate model (HR 1.857, 95% CI 1.036-3.328, p=0.037). Inferiority of other MDS-specific indexes to predict the outcome for allo-HSCT seems to be associated with adverse results in the intermediate risk group. In conclusion, we presume a need for further characterization of the intermediate risk patients when predicting the therapy outcomes. 
Keywords
Myelodysplastic syndrome, allogeneic hematopoietic stem cell transplantation, prognostic indexes, risk estimation.  
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