International Journal of Hematology

, Volume 108, Issue 3, pp 282–289 | Cite as

Refinement of the Glasgow Prognostic Score as a pre-transplant risk assessment for allogeneic hematopoietic cell transplantation

  • Yasuhiko Shibasaki
  • Tatsuya Suwabe
  • Takayuki Katagiri
  • Tomoyuki Tanaka
  • Takashi Ushiki
  • Kyoko Fuse
  • Naoko Sato
  • Toshio Yano
  • Takashi Kuroha
  • Shigeo Hashimoto
  • Miwako Narita
  • Tatsuo Furukawa
  • Hirohito Sone
  • Masayoshi MasukoEmail author
Original Article


The Hematopoietic Cell Transplantation-specific Comorbidity Index (HCT-CI) is a widely used tool for pre-transplant risk assessment. Allogeneic hematopoietic cell transplantation (HCT) is performed on patients with diverse backgrounds, highlighting the need for other predictors to complement the HCT-CI and support bedside decision-making. There is a strong body of evidence supporting the use of pre-transplant serum ferritin (SF) in risk assessments of allogeneic HCT. We additionally found that the Glasgow Prognostic Score (GPS), which assesses inflammatory biomarkers and predicts survival of patients with solid organ malignancies, is a useful predictive marker for overall survival (OS) and non-relapse mortality (NRM) in allogeneic HCT, independent of HCT-CI and SF. In this study, we refined the GPS by adding pre-transplant SF to improve its prognostic ability and enable better stratification; we call this revised index the HCT-specific revised Glasgow Prognostic Score (HCT-GPS). We observed that the HCT-GPS more accurately predicted NRM and early-term OS than the GPS. Moreover, the HCT-GPS provides an independent prognostic factor adjusted for the HCT-CI and disease status, and stratifies patients into four risk groups by OS and NRM. Thus, the HCT-GPS is a useful index for predicting early-term complications after allogeneic HCT in patients with hematopoietic diseases.


Hematopoietic cell transplantation Risk assessment Biomarkers Predictive score 



The authors would like to thank the medical staff at each transplantation center.

Author contributions

YS performed research, TS, TK, TT, KF, TU, NS, TY, TK, SH, MN, TF, and HS performed data analysis, YS and MM wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

12185_2018_2463_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 22 KB)
12185_2018_2463_MOESM2_ESM.tif (158 kb)
Supplemental figure 1: Kaplan–Meier estimates of overall survival (a) and non-relapse mortality (b) using the Glasgow Prognostic Score (GPS). 1 year-mortality in each risk-group of the GPS was as follows, OS 0: 70.3%, 1: 50.0%, 2: 15.8% (a), NRM 0: 19.6%, 1: 28.6%, 2: 52.6% (b). (TIF 158 KB)


  1. 1.
    Miyawaki S. JSH guideline for tumors of hematopoietic and lymphoid tissues: leukemia 1. Acute myeloid leukemia (AML). Int J Hematol. 2017;106:310–25.CrossRefPubMedGoogle Scholar
  2. 2.
    Miyazaki Y. JSH guideline for tumors of hematopoietic and lymphoid tissues: leukemia: 6. Myelodysplastic syndromes (MDS). Int J Hematol. 2017;106:151–9.CrossRefPubMedGoogle Scholar
  3. 3.
    Sorror ML, Maris MB, Storb R, Baron F, Sandmaier BM, Maloney DG, et al. Hematopoietic cell transplantation (HCT)-specific comorbidity index: a new tool for risk assessment before allogeneic HCT. Blood. 2005;106:2912–9.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Sorror ML, Storb RF, Sandmaier BM, Maziarz RT, Pulsipher MA, Maris MB, et al. Comorbidity-age index: a clinical measure of biologic age before allogeneic hematopoietic cell transplantation. J Clin Oncol. 2014;32:3249–56.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Armand P, Gibson CJ, Cutler C, Ho VT, Koreth J, Alyea EP, et al. A disease risk index for patients undergoing allogeneic stem cell transplantation. Blood. 2012;120:905–13.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Armand P, Kim HT, Logan BR, Wang ZW, Alyea EP, Kalaycio ME, et al. Validation and refinement of the disease risk index for allogeneic stem cell transplantation. Blood. 2014;123:3664–71.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Gratwohl A, Stern M, Brand R, Apperley J, Baldomero H, de Witte T, et al. Risk score for outcome after allogeneic hematopoietic stem cell transplantation: a retrospective analysis. Cancer. 2009;115:4715–26.CrossRefPubMedGoogle Scholar
  8. 8.
    Parimon T, Au DH, Martin PJ, Chien JW. A risk score for mortality after allogeneic hematopoietic cell transplantation. Ann Intern Med. 2006;144:407–14.CrossRefPubMedGoogle Scholar
  9. 9.
    Kurosawa S, Yakushijin K, Yamaguchi T, Atsuta Y, Nagamura-Inoue T, Akiyama H, et al. Changes in incidence and causes of non-relapse mortality after allogeneic hematopoietic cell transplantation in patients with acute leukemia/myelodysplastic syndrome: an analysis of the Japan Transplant Outcome Registry. Bone Marrow Transplant. 2013;48:529–36.CrossRefPubMedGoogle Scholar
  10. 10.
    Kekre N, Antin JH. Hematopoietic stem cell transplantation donor sources in the 21st century: choosing the ideal donor when a perfect match does not exist. Blood. 2014;124:334–43.CrossRefPubMedGoogle Scholar
  11. 11.
    Flowers ME, Martin PJ. How we treat chronic graft-versus-host disease. Blood. 2015;125:606–15.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    El Chaer F, Shah DP, Chemaly RF. How I treat resistant cytomegalovirus infection in hematopoietic cell transplantation recipients. Blood. 2016;128:2624–36.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kerbauy DM, Chyou F, Gooley T, Sorror ML, Scott B, Pagel JM, et al. Allogeneic hematopoietic cell transplantation for chronic myelomonocytic leukemia. Biol Blood Marrow Transplant. 2005;11:713–20.CrossRefPubMedGoogle Scholar
  14. 14.
    Sorror ML, Sandmaier BM, Storer BE, Maris MB, Baron F, Maloney DG, et al. Comorbidity and disease status based risk stratification of outcomes among patients with acute myeloid leukemia or myelodysplasia receiving allogeneic hematopoietic cell transplantation. J Clin Oncol. 2007;25:4246–54.CrossRefPubMedGoogle Scholar
  15. 15.
    Boehm A, Sperr WR, Leitner G, Worel N, Oehler L, Jaeger E, et al. Comorbidity predicts survival in myelodysplastic syndromes or secondary acute myeloid leukaemia after allogeneic stem cell transplantation. Eur J Clin Invest. 2008;38:945–52.CrossRefPubMedGoogle Scholar
  16. 16.
    Sorror ML, Storer BE, Maloney DG, Sandmaier BM, Martin PJ, Storb R. Outcomes after allogeneic hematopoietic cell transplantation with nonmyeloablative or myeloablative conditioning regimens for treatment of lymphoma and chronic lymphocytic leukemia. Blood. 2008;111:446–52.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Farina L, Bruno B, Patriarca F, Spina F, Sorasio R, Morelli M, et al. The hematopoietic cell transplantation comorbidity index (HCT-CI) predicts clinical outcomes in lymphoma and myeloma patients after reduced-intensity or non-myeloablative allogeneic stem cell transplantation. Leukemia. 2009;23:1131–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Pollack SM, Steinberg SM, Odom J, Dean RM, Fowler DH, Bishop MR. Assessment of the hematopoietic cell transplantation comorbidity index in non-Hodgkin lymphoma patients receiving reduced-intensity allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2009;15:223–30.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Pavlu J, Kew AK, Taylor-Roberts B, Auner HW, Marin D, Olavarria E, et al. Optimizing patient selection for myeloablative allogeneic hematopoietic cell transplantation in chronic myeloid leukemia in chronic phase. Blood. 2010;115:4018–20.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sorror ML, Giralt S, Sandmaier BM, De Lima M, Shahjahan M, Maloney DG, et al. Hematopoietic cell transplantation specific comorbidity index as an outcome predictor for patients with acute myeloid leukemia in first remission: combined FHCRC and MDACC experiences. Blood. 2007;110:4606–13.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Atsuta Y. Introduction of Transplant Registry Unified Management Program 2 (TRUMP2): scripts for TRUMP data analyses, part I (variables other than HLA-related data). Int J Hematol. 2016;103:3–10.CrossRefPubMedGoogle Scholar
  22. 22.
    Armand P, Kim HT, Cutler CS, Ho VT, Koreth J, Alyea EP, et al. Prognostic impact of elevated pretransplantation serum ferritin in patients undergoing myeloablative stem cell transplantation. Blood. 2007;109:4586–8.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Kataoka K, Nannya Y, Hangaishi A, Imai Y, Chiba S, Takahashi T, et al. Influence of pretransplantation serum ferritin on nonrelapse mortality after myeloablative and nonmyeloablative allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2009;15:195–204.CrossRefPubMedGoogle Scholar
  24. 24.
    Maradei SC, Maiolino A, de Azevedo AM, Colares M, Bouzas LF, Nucci M. Serum ferritin as risk factor for sinusoidal obstruction syndrome of the liver in patients undergoing hematopoietic stem cell transplantation. Blood. 2009;114:1270–5.CrossRefPubMedGoogle Scholar
  25. 25.
    Tachibana T, Tanaka M, Takasaki H, Numata A, Ito S, Watanabe R, et al. Pretransplant serum ferritin is associated with bloodstream infections within 100 days of allogeneic stem cell transplantation for myeloid malignancies. Int J Hematol. 2011;93:368–74.CrossRefPubMedGoogle Scholar
  26. 26.
    Sivgin S, Baldane S, Kaynar L, Kurnaz F, Pala C, Ozturk A, et al. Pretransplant serum ferritin level may be a predictive marker for outcomes in patients having undergone allogeneic hematopoietic stem cell transplantation. Neoplasma. 2012;59:183–90.CrossRefPubMedGoogle Scholar
  27. 27.
    Grossekatthofer M, Guclu ED, Lawitschka A, Matthes-Martin S, Mann G, Minkov M, et al. Ferritin concentrations correlate to outcome of hematopoietic stem cell transplantation but do not serve as biomarker of graft-versus-host disease. Ann Hematol. 2013;92:1121–8.CrossRefPubMedGoogle Scholar
  28. 28.
    Shibasaki Y, Suwabe T, Katagiri T, Tanaka T, Kobayashi H, Fuse K, et al. The Glasgow Prognostic Score as a pre-transplant risk assessment for allogeneic hematopoietic cell transplantation. Clin Transplant. 2017. Scholar
  29. 29.
    Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dunlop DJ. Evaluation of cumulative prognostic scores based on the systemic inflammatory response in patients with inoperable non-small-cell lung cancer. Br J Cancer. 2003;89:1028–30.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Forrest LM, McMillan DC, McArdle CS, Angerson WJ, Dagg K, Scott HR. A prospective longitudinal study of performance status, an inflammation-based score (GPS) and survival in patients with inoperable non-small-cell lung cancer. Br J Cancer. 2005;92:1834–6.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Armand P, Kim HT, Virtanen JM, Parkkola RK, Itala-Remes MA, Majhail NS, et al. Iron overload in allogeneic hematopoietic cell transplantation outcome: a meta-analysis. Biol Blood Marrow Transplant. 2014;20:1248–51.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Chee L, Tacey M, Lim B, Lim A, Szer J, Ritchie D. Pre-transplant ferritin, albumin and haemoglobin are predictive of survival outcome independent of disease risk index following allogeneic stem cell transplantation. Bone Marrow Transplant. 2017;52:870–7.CrossRefPubMedGoogle Scholar
  33. 33.
    Pencina MJ, D’Agostino RB Sr, D’Agostino RB Jr, Vasan RS. Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med. 2008;27:157–72 (discussion 207–12).CrossRefPubMedGoogle Scholar
  34. 34.
    Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48:452–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Elsawy M, Sorror ML. Up-to-date tools for risk assessment before allogeneic hematopoietic cell transplantation. Bone Marrow Transplant. 2016;51:1283–300.CrossRefPubMedGoogle Scholar
  36. 36.
    Artz AS, Logan B, Zhu X, Akpek G, Bufarull RM, Gupta V, et al. The prognostic value of serum C-reactive protein, ferritin, and albumin prior to allogeneic transplantation for acute myeloid leukemia and myelodysplastic syndromes. Haematologica. 2016;101:1426–33.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Japanese Society of Hematology 2018

Authors and Affiliations

  • Yasuhiko Shibasaki
    • 1
    • 2
  • Tatsuya Suwabe
    • 2
  • Takayuki Katagiri
    • 2
  • Tomoyuki Tanaka
    • 2
  • Takashi Ushiki
    • 2
  • Kyoko Fuse
    • 2
  • Naoko Sato
    • 3
  • Toshio Yano
    • 3
  • Takashi Kuroha
    • 3
  • Shigeo Hashimoto
    • 3
  • Miwako Narita
    • 2
  • Tatsuo Furukawa
    • 3
  • Hirohito Sone
    • 2
  • Masayoshi Masuko
    • 1
    Email author
  1. 1.Department of Stem Cell TransplantationNiigata University Medical and Dental HospitalNiigataJapan
  2. 2.Department of Hematology, Endocrinology and MetabolismNiigata University Faculty of MedicineNiigataJapan
  3. 3.Department of HematologyNagaoka Red Cross HospitalNagaokaJapan

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