Role of flow cytometry in myelodysplastic syndromes: diagnosis, classification, prognosis and response assessment

References

• Fenaux P. Myelodysplastic syndromes: from pathogenesis and prognosis to treatment. Semin Hematol 2004;41:6–12.
   PubMed Web of Science ®Google Scholar
• Bennett JM, Brunning RD, Vardiman JW. Myelodysplastic syndromes:from French-American-British to World Health Organization: a commentary. Blood 2002;99:3074–3075.
   PubMed Web of Science ®Google Scholar
• Bennett JM, Komrokji RS. The myelodysplastic syndromes: diagnosis, molecular biology and risk assessment. Hematology 2005;10(Suppl. 1):258–269.
   PubMed Web of Science ®Google Scholar
• Greenberg P, Cox C, LeBeau MM, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood 1997;89:2079–2088.
   PubMed Web of Science ®Google Scholar
• Valent P, Horny HP, Bennett JM, et al. Definitions and standards in the diagnosis and treatment of the myelodysplastic syndromes:Consensus statements and report from a working conference. Leuk Res 2007;31:727–736.
   PubMed Web of Science ®Google Scholar
• Cheson BD, Bennett JM, Kantarjian H, et al. Report of an international working group to standardize response criteria for myelodysplastic syndromes. Blood 2000;96:3671–3674.
   PubMed Web of Science ®Google Scholar
• Malcovati L, Germing U, Kuendgen A, et al. Time-dependent prognostic scoring system for predicting survival and leukemic evolution in myelodysplastic syndromes. J Clin Oncol 2007;25:3503–3510.
   PubMed Web of Science ®Google Scholar
• Parmentier S, Schetelig J, Lorenz K, et al. Assessment of dysplastic hematopoiesis: lessons from healthy bone marrow donors. Haematologica 2012;97:723–730.
   PubMed Web of Science ®Google Scholar
• Mufti GJ, Bennett JM, Goasguen J, et al. Diagnosis and classification of myelodysplastic syndrome: International Working Group on Morphology of myelodysplastic syndrome (IWGM-MDS) consensus proposals for the definition and enumeration of myeloblasts and ring sideroblasts. Haematologica 2008;93:1712–1717.
   PubMed Web of Science ®Google Scholar
• Ramos F, Fernandez-Ferrero S, Suarez D, et al. Myelodysplastic syndrome: a search for minimal diagnostic criteria. Leuk Res 1999;23:283–290.
   PubMed Web of Science ®Google Scholar
• Valent P, Horny HP. Minimal diagnostic criteria for myelodysplastic syndromes and separation from ICUS and IDUS: update and open questions. Eur J Clin Invest 2009;39:548–553.
   PubMed Web of Science ®Google Scholar
• Sole F, Espinet B, Sanz GF, et al. Incidence, characterization and prognostic significance of chromosomal abnormalities in 640 patients with primary myelodysplastic syndromes. Grupo Cooperativo Espanol de Citogenetica Hematologica. Br J Haematol 2000;108:346–356.
   Google Scholar
• Chun K, Hagemeijer A, Iqbal A, et al. Implementation of standardized international karyotype scoring practices is needed to provide uniform and systematic evaluation for patients with myelodysplastic syndrome using IPSS criteria: an International Working Group on MDS Cytogenetics Study. Leuk Res 2010;34:160–165.
   PubMed Web of Science ®Google Scholar
• Bacher U, Kern W, Alpermann T, et al. Prognoses of MDS subtypes RARS, RCMD and RCMD-RS are comparable but cytogenetics separates a subgroup with inferior clinical course. Leuk Res 2012;36:826–831.
   PubMed Web of Science ®Google Scholar
• Ossenkoppele GJ, van de Loosdrecht AA, Schuurhuis GJ. Review of the relevance of aberrant antigen expression by flow cytometry in myeloid neoplasms. Br J Haematol 2011;153:421–436.
   PubMed Web of Science ®Google Scholar
• Mach WJ, Thimmesch AR, Orr JA, et al. Flow cytometry and laser scanning cytometry, a comparison of techniques. J Clin Monit Comput 2010;24:251–259.
   PubMedGoogle Scholar
• Wood BL, Arroz M, Barnett D, et al. 2006 Bethesda International Consensus recommendations on the immunophenotypic analysis of hematolymphoid neoplasia by flow cytometry: optimal reagents and reporting for the flow cytometric diagnosis of hematopoietic neoplasia. Cytometry B Clin Cytom 2007;72(Suppl. 1):S14–S22.
   PubMed Web of Science ®Google Scholar
• Loken MR, van de Loosdrecht A, Ogata K, et al. Flow cytometry in myelodysplastic syndromes:report from a working conference. Leuk Res 2008;32:5–17.
   PubMed Web of Science ®Google Scholar
• van de Loosdrecht AA, Ireland R, Kern W, et al. Rationale for the clinical application of flow cytometry in patients with myelodysplastic syndromes: position paper of an International Consortium and the European LeukemiaNet Working Group. Leuk Lymphoma 2013;54: 472–475.
   PubMed Web of Science ®Google Scholar
• Kern W, Haferlach C, Schnittger S, et al. Clinical utility of multiparameter flow cytometry in the diagnosis of 1013 patients with suspected myelodysplastic syndrome: correlation to cytomorphology, cytogenetics, and clinical data. Cancer 2010;116:4549–4563.
   PubMed Web of Science ®Google Scholar
• Kussick SJ, Fromm JR, Rossini A, et al. Four-color flow cytometry shows strong concordance with bone marrow morphology and cytogenetics in the evaluation for myelodysplasia. Am J Clin Pathol 2005;124:170–181.
   PubMed Web of Science ®Google Scholar
• Malcovati L, Della Porta MG, Lunghi M, et al. Flow cytometry evaluation of erythroid and myeloid dysplasia in patients with myelodysplastic syndrome. Leukemia 2005;19:776–783.
   PubMed Web of Science ®Google Scholar
• Ogata K, Della Porta MG, Malcovati L, et al. Diagnostic utility of flow cytometry in low-grade myelodysplastic syndromes:a prospective validation study. Haematologica 2009;94:1066–1074.
   PubMed Web of Science ®Google Scholar
• van de Loosdrecht AA, Westers TM, Westra AH, et al. Identification of distinct prognostic subgroups in low- and intermediate-1-risk myelodysplastic syndromes by flow cytometry. Blood 2008;111: 1067–1077.
   PubMed Web of Science ®Google Scholar
• Wells DA, Benesch M, Loken MR, et al. Myeloid and monocytic dyspoiesis as determined by flow cytometric scoring in myelodysplastic syndrome correlates with the IPSS and with outcome after hematopoietic stem cell transplantation. Blood 2003;102:394–403.
   PubMed Web of Science ®Google Scholar
• Della Porta MG, Malcovati L, Invernizzi R, et al. Flow cytometry evaluation of erythroid dysplasia in patients with myelodysplastic syndrome. Leukemia 2006;20:549–555.
   PubMed Web of Science ®Google Scholar
• Truong F, Smith BR, Stachurski D, et al. The utility of flow cytometric immunophenotyping in cytopenic patients with a non-diagnostic bone marrow: a prospective study. Leuk Res 2009;33: 1039–1046.
   PubMed Web of Science ®Google Scholar
• Westers TM, Ireland R, Kern W, et al. Standardization of flow cytometry in myelodysplastic syndromes: a report from an international consortium and the European LeukemiaNet Working Group. Leukemia 2012;26:1730–1741.
   PubMed Web of Science ®Google Scholar
• van de Loosdrecht AA, Westers TM. Flow cytometry in myelodysplastic syndromes: ready for translation into clinical practice. Leuk Res 2011;35:850–852.
   PubMed Web of Science ®Google Scholar
• Ogata K. Flow cytometry will be a routine tool in clinical practice in myelodysplastic syndromes:a real story. Leuk Res 2011;35:848–849.
   PubMed Web of Science ®Google Scholar
• van de Loosdrecht AA, Alhan C, Bene MC, et al. Standardization of flow cytometry in myelodysplastic syndromes: report from the first European LeukemiaNet working conference on flow cytometry in myelodysplastic syndromes. Haematologica 2009;94:1124–1134.
   PubMed Web of Science ®Google Scholar
• Wood BL. Myeloid malignancies: myelodysplastic syndromes, myeloproliferative disorders, and acute myeloid leukemia. Clin Lab Med 2007;27:551–575, vii.
   PubMed Web of Science ®Google Scholar
• Westers TM, van der Velden VH, Alhan C, et al. Implementation of flow cytometry in the diagnostic work-up of myelodysplastic syndromes in a multicenter approach: report from the Dutch Working Party on Flow Cytometry in MDS. Leuk Res 2012;36:422–430.
   PubMed Web of Science ®Google Scholar
• Wood B. 9-color and 10-color flow cytometry in the clinical laboratory. Arch Pathol Lab Med 2006;130:680–690.
   PubMed Web of Science ®Google Scholar
• De Rosa SC, Brenchley JM, Roederer M. Beyond six colors: a new era in flow cytometry. Nat Med 2003;9:112–117.
   PubMed Web of Science ®Google Scholar
• van Dongen JJ, Lhermitte L, Bottcher S, et al. EuroFlow antibody panels for standardized n-dimensional flow cytometric immunophenotyping of normal, reactive and malignant leukocytes. Leukemia 2012;26:1908–1975.
   PubMed Web of Science ®Google Scholar
• Wells DA, Sale GE, Shulman HM, et al. Multidimensional flow cytometry of marrow can differentiate leukemic from normal lymphoblasts and myeloblasts after chemotherapy and bone marrow transplantation. Am J Clin Pathol 1998;110:84–94.
   PubMed Web of Science ®Google Scholar
• van Lochem EG, van der Velden VH, Wind HK, et al. Immunophenotypic differentiation patterns of normal hematopoiesis in human bone marrow: reference patterns for age-related changes and disease-induced shifts. Cytometry B Clin Cytom 2004;60:1–13.
   PubMed Web of Science ®Google Scholar
• Arnoulet C, Bene MC, Durrieu F, et al. Four- and five-color flow cytometry analysis of leukocyte differentiation pathways in normal bone marrow: a reference document based on a systematic approach by the GTLLF and GEIL. Cytometry B Clin Cytom 2010;78:4–10.
   PubMedGoogle Scholar
• Civin CI, Loken MR. Cell surface antigens on human marrow cells: dissection of hematopoietic development using monoclonal antibodies and multiparameter flow cytometry. Int J Cell Cloning 1987;5:267–288.
   PubMedGoogle Scholar
• Stetler-Stevenson M, Arthur DC, Jabbour N, et al. Diagnostic utility of flow cytometric immunophenotyping in myelodysplastic syndrome. Blood 2001;98:979–987.
   PubMed Web of Science ®Google Scholar
• Stachurski D, Smith BR, Pozdnyakova O, et al. Flow cytometric analysis of myelomonocytic cells by a pattern recognition approach is sensitive and specific in diagnosing myelodysplastic syndrome and related marrow diseases: emphasis on a global evaluation and recognition of diagnostic pitfalls. Leuk Res 2008;32:215–224.
   PubMed Web of Science ®Google Scholar
• Lorand-Metze I, Ribeiro E, Lima CS, et al. Detection of hematopoietic maturation abnormalities by flow cytometry in myelodysplastic syndromes and its utility for the differential diagnosis with non-clonal disorders. Leuk Res 2007;31:147–155.
   PubMed Web of Science ®Google Scholar
• Della Porta MG, Lanza F, Del Vecchio L. Flow cytometry immunophenotyping for the evaluation of bone marrow dysplasia. Cytometry B Clin Cytom 2011;80:201–211.
   PubMed Web of Science ®Google Scholar
• Loken MR, Chu SC, Fritschle W, et al. Normalization of bone marrow aspirates for hemodilution in flow cytometric analyses. Cytometry B Clin Cytom 2009;76:27–36.
   PubMed Web of Science ®Google Scholar
• Kern W, Haferlach C, Schnittger S, et al. Serial assessment of suspected myelodysplastic syndromes: significance of flow cytometric findings validated by cytomorphology, cytogenetics, and molecular genetics. Haematologica 2013;98:201–207.
   PubMed Web of Science ®Google Scholar
• Ogata K, Nakamura K, Yokose N, et al. Clinical significance of phenotypic features of blasts in patients with myelodysplastic syndrome. Blood 2002;100:3887–3896.
   PubMed Web of Science ®Google Scholar
• Matarraz S, Lopez A, Barrena S, et al. The immunophenotype of different immature, myeloid and B-cell lineage-committed CD34 + hematopoietic cells allows discrimination between normal/reactive and myelodysplastic syndrome precursors. Leukemia 2008;22:1175–1183.
   PubMed Web of Science ®Google Scholar
• Maftoun-Banankhah S, Maleki A, Karandikar NJ, et al. Multiparameter flow cytometric analysis reveals low percentage of bone marrow hematogones in myelodysplastic syndromes. Am J Clin Pathol 2008;129:300–308.
   PubMed Web of Science ®Google Scholar
• Kussick SJ, Wood BL. Using 4-color flow cytometry to identify abnormal myeloid populations. Arch Pathol Lab Med 2003;127: 1140–1147.
   PubMed Web of Science ®Google Scholar
• Elghetany MT, Ge Y, Patel J, et al. Flow cytometric study of neutrophilic granulopoiesis in normal bone marrow using an expanded panel of antibodies: correlation with morphologic assessments. J Clin Lab Anal 2004;18:36–41.
   PubMed Web of Science ®Google Scholar
• Zini G, Bain B, Bettelheim P, et al. A European consensus report on blood cell identification: terminology utilized and morphological diagnosis concordance among 28 experts from 17 countries within the European LeukemiaNet network WP10, on behalf of the ELN Morphology Faculty. Br J Haematol 2010;151:359–364.
   PubMed Web of Science ®Google Scholar
• Bain BJ. Morphology in the diagnosis of red cell disorders. Hematology 2005;10(Suppl. 1):178–181.
   PubMed Web of Science ®Google Scholar
• Westers TM, Ireland R, Kern W, et al. Standardization of flow cytometry in myelodysplastic syndromes: a report from an international consortium and the European LeukemiaNet Working Group. Leukemia 2012;26:1730–1741.
   PubMed Web of Science ®Google Scholar
• Briggs RC, Briggs JA, Ozer J, et al. The human myeloid cell nuclear differentiation antigen gene is one of at least two related interferon-inducible genes located on chromosome 1q that are expressed specifically in hematopoietic cells. Blood 1994;83:2153–2162.
   PubMed Web of Science ®Google Scholar
• Burrus GR, Briggs JA, Briggs RC. Characterization of the human myeloid cell nuclear differentiation antigen:relationship to interferon-inducible proteins. J Cell Biochem 1992;48:190–202.
   PubMed Web of Science ®Google Scholar
• Briggs RC, Kao WY, Dworkin LL, et al. Regulation and specificity of MNDA expression in monocytes, macrophages, and leukemia/B lymphoma cell lines. J Cell Biochem 1994;56:559–567.
   PubMed Web of Science ®Google Scholar
• Briggs RC, Shults KE, Flye LA, et al. Dysregulated human myeloid nuclear differentiation antigen expression in myelodysplastic syndromes: evidence for a role in apoptosis. Cancer Res 2006;66:4645–4651.
   PubMed Web of Science ®Google Scholar
• Hofmann WK, de Vos S, Komor M, et al. Characterization of gene expression of CD34 + cells from normal and myelodysplastic bone marrow. Blood 2002;100:3553–3560.
   PubMed Web of Science ®Google Scholar
• Cousar JB, Briggs RC. Expression of human myeloid cell nuclear differentiation antigen (MNDA) in acute leukemias. Leuk Res 1990;14:915–920.
   PubMed Web of Science ®Google Scholar
• Miranda RN, Briggs RC, Shults K, et al. Immunocytochemical analysis of MNDA in tissue sections and sorted normal bone marrow cells documents expression only in maturing normal and neoplastic myelomonocytic cells and a subset of normal and neoplastic B lymphocytes. Hum Pathol 1999;30:1040–1049.
   PubMed Web of Science ®Google Scholar
• McClintock-Treep SA, Briggs RC, Shults KE, et al. Quantitative assessment of myeloid nuclear differentiation antigen distinguishes myelodysplastic syndrome from normal bone marrow. Am J Clin Pathol 2011;135:380–385.
   PubMed Web of Science ®Google Scholar
• Bellos F, Alpermann T, Gouberman E, et al. Evaluation of flow cytometric assessment of myeloid nuclear differentiation antigen expression as a diagnostic marker for myelodysplastic syndromes in a series of 269 patients. Cytometry B Clin Cytom 2012;82:295–304.
   PubMed Web of Science ®Google Scholar
• Leveque C, Grafte S, Paysant J, et al. Regulation of interleukin 3 receptor alpha chain (IL-3R alpha) on human monocytes by interleukin (IL)-4, IL-10, IL-13, and transforming growth factor beta (TGF-beta). Cytokine 1998;10:487–494.
   PubMed Web of Science ®Google Scholar
• Munoz L, Nomdedeu JF, Lopez O, et al. Interleukin-3 receptor alpha chain (CD123) is widely expressed in hematologic malignancies. Haematologica 2001;86:1261–1269.
   PubMed Web of Science ®Google Scholar
• Hauswirth AW, Florian S, Printz D, et al. Expression of the target receptor CD33 in CD34+/CD38-/CD123 + AML stem cells. Eur J Clin Invest 2007;37:73–82.
   PubMed Web of Science ®Google Scholar
• Jordan CT, Upchurch D, Szilvassy SJ, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000;14:1777–1784.
   PubMed Web of Science ®Google Scholar
• Hassanein NM, Alcancia F, Perkinson KR, et al. Distinct expression patterns of CD123 and CD34 on normal bone marrow B-cell precursors (“hematogones”) and B lymphoblastic leukemia blasts. Am J Clin Pathol 2009;132:573–580.
   PubMed Web of Science ®Google Scholar
• Jin L, Lee EM, Ramshaw HS, et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009;5:31–42.
   PubMed Web of Science ®Google Scholar
• Vardiman JW. The World Health Organization (WHO) classification of tumors of the hematopoietic and lymphoid tissues: an overview with emphasis on the myeloid neoplasms. Chem Biol Interact 2010;184: 16–20.
   PubMed Web of Science ®Google Scholar
• Benesch M, Deeg HJ, Wells D, et al. Flow cytometry for diagnosis and assessment of prognosis in patients with myelodysplastic syndromes. Hematology 2004;9:171–177.
   PubMedGoogle Scholar
• Huang J, Lai P, Zhou M, et al. A multiparametric flow cytometry immunophenotypic scoring system for the diagnosis and prognosis of myelodysplastic syndromes. Clin Lab 2012;58:1241–1251.
   PubMed Web of Science ®Google Scholar
• Scott BL, Wells DA, Loken MR, et al. Validation of a flow cytometric scoring system as a prognostic indicator for posttransplantation outcome in patients with myelodysplastic syndrome. Blood 2008;112:2681–2686.
   PubMed Web of Science ®Google Scholar
• Ogata K. Diagnostic flow cytometry for low-grade myelodysplastic syndromes. Hematol Oncol 2008;26:193–198.
   PubMed Web of Science ®Google Scholar
• Della Porta MG, Picone C, Pascutto C, et al. Multicentre validation of a reproducible flow cytometric score for the diagnosis of low-risk myelodysplastic syndromes: results of a European LeukemiaNET study. Haematologica 2012;97:1209–1217.
   PubMed Web of Science ®Google Scholar
• Valent P, Hofmann WK, Busche G, et al. Meeting report: Vienna 2008 Workshop of the German-Austrian Working Group for Studying Prognostic Factors in Myelodysplastic Syndromes. Ann Hematol 2009;88:607–611.
   PubMed Web of Science ®Google Scholar
• Bennett JM. World Health Organization classification of the acute leukemias and myelodysplastic syndrome. Int J Hematol 2000;72: 131–133.
   PubMed Web of Science ®Google Scholar
• Dawson MA, Davis A, Elliott P, et al. Linezolid-induced dyserythropoiesis: chloramphenicol toxicity revisited. Intern Med J 2005;35:626–628.
   PubMed Web of Science ®Google Scholar
• Fong T, Vij R, Vijayan A, et al. Copper deficiency: an important consideration in the differential diagnosis of myelodysplastic syndrome. Haematologica 2007;92:1429–1430.
   PubMed Web of Science ®Google Scholar
• Amos RJ, Deane M, Ferguson C, et al. Observations on the haemopoietic response to critical illness. J Clin Pathol 1990;43: 850–856.
   PubMed Web of Science ®Google Scholar
• Haase D, Germing U, Schanz J, et al. New insights into the prognostic impact of the karyotype in MDS and correlation with subtypes: evidence from a core dataset of 2124 patients. Blood 2007;110:4385–4395.
   PubMed Web of Science ®Google Scholar
• Fenaux P. Chromosome and molecular abnormalities in myelodysplastic syndromes. Int J Hematol 2001;73:429–437.
   PubMed Web of Science ®Google Scholar
• Germing U, Strupp C, Kuendgen A, et al. Prospective validation of the WHO proposals for the classification of myelodysplastic syndromes. Haematologica 2006;91:1596–1604.
   PubMed Web of Science ®Google Scholar
• Malcovati L, Porta MG, Pascutto C, et al. Prognostic factors and life expectancy in myelodysplastic syndromes classified according to WHO criteria: a basis for clinical decision making. J Clin Oncol 2005;23:7594–7603.
   PubMed Web of Science ®Google Scholar
• Kern W, Haferlach C, Alpermann T, et al. Multiparameter flow cytometry in patients with suspected myelodysplastic syndromes adds significant prognostic information: a study on 1,013 patients. Blood 2011;118(Suppl. 1): Abstract 1722.
   Google Scholar
• Chu SC, Wang TF, Li CC, et al. Flow cytometric scoring system as a diagnostic and prognostic tool in myelodysplastic syndromes. Leuk Res 2011;35:868–873.
   PubMed Web of Science ®Google Scholar
• Westers TM, Alhan C, Chamuleau ME, et al. Aberrant immunophenotype of blasts in myelodysplastic syndromes is a clinically relevant biomarker in predicting response to growth factor treatment. Blood 2010;115:1779–1784.
   PubMed Web of Science ®Google Scholar
• Hellstrom-Lindberg E, Gulbrandsen N, Lindberg G, et al. A validated decision model for treating the anaemia of myelodysplastic syndromes with erythropoietin + granulocyte colony-stimulating factor:significant effects on quality of life. Br J Haematol 2003;120: 1037–1046.
   PubMed Web of Science ®Google Scholar
• Silverman LR, Fenaux P, Mufti GJ, et al. Continued azacitidine therapy beyond time of first response improves quality of response in patients with higher-risk myelodysplastic syndromes. Cancer 2011;117:2697–2702.
   PubMed Web of Science ®Google Scholar
• Fenaux P. Response assessments in low-risk and high-risk myelodysplastic syndromes (MDS). Semin Oncol 2005;32:S11–S115.
   Web of Science ®Google Scholar
• Balleisen S, Kuendgen A, Hildebrandt B, et al. Prognostic relevance of achieving cytogenetic remission in patients with acute myelogenous leukemia or high-risk myelodysplastic syndrome following induction chemotherapy. Leuk Res 2009;33:1189–1193.
   PubMed Web of Science ®Google Scholar
• Gangatharan SA, Carney DA, Campbell LJ, et al. Cytogenetic response is not a prerequisite for clinical response in patients with myelodysplastic syndromes treated with azacitidine. Eur J Haematol 2011;87:186–188.
   PubMed Web of Science ®Google Scholar
• Burbury K, Gambell P, Came N, et al. Utility of flow cytometry in the assessment of therapeutic efficacy in myelodysplastic syndromes after intervention. Blood 2009;114(Suppl. 1): Abstract 2767.
   Google Scholar