Proposed minimal diagnostic criteria for myelodysplastic syndromes (MDS) and potential pre-MDS conditions

Oncotarget

Volumn 8, Issue 43, 2017, Pages 73483-73500

  Valent, Peter ^a   Orazi, Attilio ^b   Steensma, David P ^c   Ebert, Benjamin L ^d   Haase, Detlef ^e   Malcovati, Luca ^f   van de Loosdrecht, Arjan A ^g   Haferlach, Torsten ^h   Westers, Theresia M ^g   Wells, Denise A ⁱ   Giagounidis, Aristoteles ^j   Loken, Michael ⁱ   Orfao, Alberto ^k   Lübbert, Michael ^l   Ganser, Arnold ^m   Hofmann, Wolf Karsten ⁿ   Ogata, Kiyoyuki ^o   Schanz, Julie ^e   Béné, Marie C ^p   Hoermann, Gregor ^a   Sperr, Wolfgang R ^a   Sotlar, Karl ^q   Bettelheim, Peter ^r   Stauder, Reinhard ^s   Pfeilstöcker, Michael ^t   Horny, Hans Peter ^u   Germing, Ulrich ^v   Greenberg, Peter ^w   Bennett, John M ^x   more..

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^f UNIVERSITY OF PAVIA   (Italy)

^g University of Amsterdam   (Netherlands)

^h MLL MUNICH LEUKEMIA LABORATORY   (Germany)

ⁱ HEMATOLOGICS INC   (United States)

^j MARIEN HOSPITAL DÜSSELDORF   (Germany)

^k CSIC   (Spain)

^l UNIVERSITY OF FREIBURG   (Germany)

^m HANNOVER MEDICAL SCHOOL   (Germany)

ⁿ UNIVERSITY OF HEIDELBERG   (Germany)

^o Metropolitan Research and Treatment Center for Blood Disorders (MRTC Japan)   (Japan)

^p NANTES UNIVERSITY HOSPITAL   (France)

^q PARACELSUS MEDICAL UNIVERSITY   (Austria)

^r ELISABETHINEN HOSPITAL   (Austria)

^s INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^t HANUSCH HOSPITAL   (Austria)

^u UNIVERSITY OF MUNICH   (Germany)

^v HEINRICH HEINE UNIVERSITY   (Germany)

^w STANFORD UNIVERSITY   (United States)

^x UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

more..

Author keywords

Diagnostic criteria; Myelodysplasia; pre MDS conditions; Standardization

Indexed keywords

BLOOD SMEAR; BONE MARROW BIOPSY; CLINICAL FEATURE; CLINICAL PRACTICE; CONSENSUS; CYTOPENIA; DIAGNOSTIC PROCEDURE; DIFFERENTIAL DIAGNOSIS; DISEASE CLASSIFICATION; DISEASE MARKER; FLOW CYTOMETRY; GENE MUTATION; HEMATOPOIESIS; HUMAN; IDIOPATHIC DISEASE; IMMUNOHISTOCHEMISTRY; KARYOTYPING; MINIMAL DIAGNOSTIC CRITERIA; MUTATIONAL ANALYSIS; MYELODYSPLASTIC SYNDROME; PROGNOSIS; REVIEW; SCORING SYSTEM; STANDARD;

EID: 85030105932     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.19008     Document Type: Review

References (103)

1. Hofmann WK, Koeffler HP. Myelodysplastic syndrome. Annu Rev Med. 2005; 56:1-16.
2. Nimer SD. Myelodysplastic syndromes. Blood. 2008; 111:4841-4851.
3. Bejar R, Levine R, Ebert BL. Unraveling the molecular pathophysiology of myelodysplastic syndromes. J Clin Oncol. 2011; 29:504-515.
4. Giagounidis A, Haase D. Morphology, cytogenetics and classification of MDS. Best Pract Res Clin Haematol. 2013; 26:337-353.
5. Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR, Sultan C. Proposals for the classification of the myelodysplastic syndromes. Br J Haematol. 1982; 51:189-199.
6. Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR, Sultan C, Cox C. The chronic myeloid leukaemias: guidelines for distinguishing chronic granulocytic, atypical chronic myeloid, and chronic myelomonocytic leukaemia. Proposals by the French-American-British Cooperative Leukaemia Group. Br J Haematol. 1994; 87:746-754.
7. Brunning RD, Bennett JM, Flandrin G, Matutes E, Head D, Vardiman JW, Harris NL. Myelodysplastic Syndromes. in: World Health Organization Classification of Tumours. Pathology & Genetics. Tumours of Haematopoietic and Lymphoid Tissues. Jaffe ES, Harris NL, Stein H, Vardiman JW (eds). IARC Press Lyon, 2001; 1:62-73.
8. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, Harris NL, Le Beau MM, Hellström Lindberg E, Tefferi A, Bloomfield CD. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood. 2009; 114:937-951.
9. Arber DA, Hasserjian RP. Reclassifying myelodysplastic syndromes: What's where in the new WHO and why. Hematology (Am Soc Hematol Educ Program). 2015; 294-298.
10. Stauder R, Nösslinger T, Pfeilstöcker M, Sperr WR, Wimazal F, Krieger O, Valent P. Impact of age and comorbidity in myelodysplastic syndromes. J Natl Compr Canc Netw. 2008; 6:927-934.
11. Itzykson R, Kosmider O, Fenaux P. Somatic mutations and epigenetic abnormalities in myelodysplastic syndromes. Best Pract Res Clin Haematol. 2013; 26:355-364.
12. Zeidan AM, Gore SD, Padron E, Komrokji RS. Current state of prognostication and risk stratification in myelodysplastic syndromes. Curr Opin Hematol. 2015; 22:146-154.
13. Busque L, Patel JP, Figueroa ME, Vasanthakumar A, Provost S, Hamilou Z, Mollica L, Li J, Viale A, Heguy A, Hassimi M, Socci N, Bhatt PK, et al. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat Genet. 2012; 44:1179-1181.
14. Genovese G, Kähler AK, Handsaker RE, Lindberg J, Rose SA, Bakhoum SF, Chambert K, Mick E, Neale BM, Fromer M, Purcell SM, Svantesson O, Landén M, et al. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N Engl J Med. 2014; 371:2477-2487.
15. Steensma DP, Bejar R, Jaiswal S, Lindsley RC, Sekeres MA, Hasserjian RP, Ebert BL. Clonal hematopoiesis of indeterminate potential and its distinction from myelodysplastic syndromes. Blood. 2015; 126:9-16.
16. Valent P, Horny HP, Bennett JM, Fonatsch C, Germing U, Greenberg P, Haferlach T, Haase D, Kolb HJ, Krieger O, Loken M, van de Loosdrecht A, Ogata K, 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.
17. 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.
18. Schroeder T, Ruf L, Bernhardt A, Hildebrandt B, Aivado M, Aul C, Gattermann N, Haas R, Germing U. Distinguishing myelodysplastic syndromes (MDS) from idiopathic cytopenia of undetermined significance (ICUS): HUMARA unravels clonality in a subgroup of patients. Ann Oncol. 2010; 21:2267-2271.
19. Valent P, Bain BJ, Bennett JM, Wimazal F, Sperr WR, Mufti G, Horny HP. Idiopathic cytopenia of undetermined significance (ICUS) and idiopathic dysplasia of uncertain significance (IDUS), and their distinction from low risk MDS. Leuk Res. 2012; 36:1-5.
20. Steensma DP. Dysplasia has a differential diagnosis: distinguishing genuine myelodysplastic syndromes (MDS) from mimics, imitators, copycats and impostors. Curr Hematol Malig Rep. 2012; 7:310-320.
21. Valent P. Low blood counts: immune mediated, idiopathic, or myelodysplasia. Hematology Am Soc Hematol Educ Program. 2012; 2012:485-491.
22. Greenberg PL, Tuechler H, Schanz J, Sanz G, Garcia-Manero G, Solé F, Bennett JM, Bowen D, Fenaux P, Dreyfus F, Kantarjian H, Kuendgen A, Levis A, et al. Cytopenia levels for aiding establishment of the diagnosis of myelodysplastic syndromes. Blood. 2016; 128:2096-2097.
23. Horny HP, Sotlar K, Valent P. Diagnostic value of histology and immunohistochemistry in myelodysplastic syndromes. Leuk Res. 2007; 31:1609-1616.
24. Orazi A, Czader MB. Myelodysplastic syndromes. Am J Clin Pathol. 2009; 132:290-305.
25. Valent P, Orazi A, Büsche G, Schmitt-Gräff A, George TI, Sotlar K, Streubel B, Beham-Schmid C, Cerny-Reiterer S, Krieger O, van de Loosdrecht A, Kern W, Ogata K, et al. Standards and impact of hematopathology in myelodysplastic syndromes (MDS). Oncotarget. 2010; 1:483-496. doi: 10.18632/oncotarget.101104.
26. Auner HW, Klintschar M, Crevenna R, Beham-Schmid C, Hoefler G, Mitterbauer G, Linkesch W, Sill H. Two case studies of chronic idiopathic neutropenia preceding acute myeloid leukaemia. Br J Haematol. 1999; 105:431-433.
27. Wimazal F, Fonatsch C, Thalhammer R, Schwarzinger I, Müllauer L, Sperr WR, Bennett JM, Valent P. Idiopathic cytopenia of undetermined significance (ICUS) versus low risk MDS: the diagnostic interface. Leuk Res. 2007; 31:1461-1468.
28. Malcovati L, Cazzola M. The shadowlands of MDS: idiopathic cytopenias of undetermined significance (ICUS) and clonal hematopoiesis of indeterminate potential (CHIP). Hematology Am Soc Hematol Educ Program. 2015; 2015:299-307.
29. Petrova-Drus K, Hasserjian R, Pozdnyakova O, Dal Cin P, Mathew S, Margolskee E, Orazi A, Geyer JT. Clinicopathologic evaluation of cytopenic patients with isolated trisomy 8: a detailed comparison between idiopathic cytopenia of unknown significance and lowgrade myelodysplastic syndrome. Leuk Lymphoma. 2016; 7:1-9.
30. Valent P, Jäger E, Mitterbauer-Hohendanner G, Müllauer L, Schwarzinger I, Sperr WR, Thalhammer R, Wimazal F. Idiopathic bone marrow dysplasia of unknown significance (IDUS): definition, pathogenesis, follow up, and prognosis. Am J Cancer Res. 2011; 1:531-541.
31. Hahn WC, Weinberg RA. Modelling the molecular circuitry of cancer. Nat Rev Cancer. 2002; 2:331-241.
32. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, Chomienne C, Ishikawa F, Schuringa JJ, Stassi G, Huntly B, Herrmann H, Soulier J, et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer. 2012; 12:767-775.
33. Jaiswal S, Fontanillas P, Flannick J, Manning A, Grauman PV, Mar BG, Lindsley RC, Mermel CH, Burtt N, Chavez A, Higgins JM, Moltchanov V, Kuo FC, et al. Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med. 2014; 371:2488-2498.
34. Gillis NK, Ball M, Zhang Q, Ma Z, Zhao Y, Yoder SJ, Balasis ME, Mesa TE, Sallman DA, Lancet JE, Komrokji RS, List AF, McLeod HL, et al. Clonal haemopoiesis and therapy-related myeloid malignancies in elderly patients: a proof-of-concept, case-control study. Lancet Oncol. 2017; 18:112-121.
35. Takahashi K, Wang F, Kantarjian H, Doss D, Khanna K, Thompson E, Zhao L, Patel K, Neelapu S, Gumbs C, Bueso-Ramos C, DiNardo CD, Colla S, et al. Preleukaemic clonal haemopoiesis and risk of therapy-related myeloid neoplasms: a case-control study. Lancet Oncol. 2017; 18:100-111.
36. Gibson CJ, Lindsley RC, Tchekmedyian V, Mar BG, Shi J, Jaiswal S, Bosworth A, Francisco L, He J, Bansal A, Morgan EA, Lacasce AS, Freedman AS, et al. Clonal Hematopoiesis Associated With Adverse Outcomes After Autologous Stem-Cell Transplantation for Lymphoma. J Clin Oncol. 2017; 35:1598-1605.
37. Steensma DP, Abedi M, Bejar R, Cogle CR, Foucar K, Garcia-Manero G, George TI, Grinblatt D, Komrokji R, Ma X, Maciejewski J, Pollyea DA, Savona MR, et al. Connect MDS/AML: design of the myelodysplastic syndromes and acute myeloid leukemia disease registry, a prospective observational cohort study. BMC Cancer. 2016; 16:652.
38. Bennett JM, Kouides PA, Forman SJ. The myelodysplastic syndromes: morphology, risk assessment, and clinical management (2002). Int J Hematol. 2002; 76:228-238.
39. Mufti GJ, Bennett JM, Goasguen J, Bain BJ, Baumann I, Brunning R, Cazzola M, Fenaux P, Germing U, Hellström-Lindberg E, Jinnai I, Manabe A, Matsuda A, 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.
40. Della Porta MG, Travaglino E, Boveri E, Ponzoni M, Malcovati L, Papaemmanuil E, Rigolin GM, Pascutto C, Croci G, Gianelli U, Milani R, Ambaglio I, Elena C, et al. Minimal morphological criteria for defining bone marrow dysplasia: a basis for clinical implementation of WHO classification of myelodysplastic syndromes. Leukemia. 2015; 29:66-75.
41. Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016; 127:2391-2405.
42. Germing U, Strupp C, Giagounidis A, Haas R, Gattermann N, Starke C, Aul C. Evaluation of dysplasia through detailed cytomorphology in 3156 patients from the Düsseldorf Registry on myelodysplastic syndromes. Leuk Res. 2012; 36:727-734.
43. Bennett JM, Tuechler H, Aul C, Strupp C, Germing U. Dysplastic erythroid precursors in the myelodysplastic syndromes and the acute myeloid leukemias: Is there biologic significance? (How should blasts be counted?). Leuk Res. 2016; 47:63-69.
44. Tuzuner N, Bennett JM. Reference standards for bone marrow cellularity. Leuk Res. 1994; 18:645-647.
45. Tuzuner N, Cox C, Rowe JM, Bennett JM. Bone marrow cellularity in myeloid stem cell disorders: impact of age correction. Leuk Res. 1994; 18:559-564.
46. Schemenau J, Baldus S, Anlauf M, Reinecke P, Braunstein S, Blum S, Nachtkamp K, Neukirchen J, Strup C, Aul C, Haas R, Gattermann N, Germing U. Cellularity, characteristics of hematopoietic parameters and prognosis in myelodysplastic syndromes. Eur J Haematol. 2015; 95:181-189.
47. Horny HP, Wehrmann M, Schlicker HU, Eichstaedt A, Clemens MR, Kaiserling E. QBEND10 for the diagnosis of myelodysplastic syndromes in routinely processed bone marrow biopsy specimens. J Clin Pathol. 1995; 48:291-294.
48. Orazi A, Albitar M, Heerema NA, Haskins S, Neiman RS. Hypoplastic myelodysplastic syndromes can be distinguished from acquired aplastic anemia by CD34 and PCNA immunostaining of bone marrow biopsy specimens. Am J Clin Pathol. 1997; 107:268-274.
49. Thiele J, Quitmann H, Wagner S, Fischer R. Dysmegakaryopoiesis in myelodysplastic syndromes (MDS): an immunomorphometric study of bone marrow trephine biopsy specimens. J Clin Pathol. 1991; 44:300-305.
50. Horny HP, Sotlar K, Valent P. Differential diagnoses of systemic mastocytosis in routinely processed bone marrow biopsy specimens: a review. Pathobiology. 2010; 77:169-180.
51. Steidl C, Steffens R, Gassmann W, Hildebrandt B, Hilgers R, Germing U, Trumper L, Haase D. Adequate cytogenetic examination in myelodysplastic syndromes: analysis of 529 patients. Leuk Res. 2005; 29:987-993.
52. ISCN: an international system for human cytogenetic nomenclature (2016). Editors: Jean McGowan-Jordan, Annet Simons, Michael Schmid. Karger Basel, New York, 2016.
53. Romeo M, Chauffaille Mde L, Silva MR, Bahia DM, Kerbauy J. Comparison of cytogenetics with FISH in 40 myelodysplastic syndrome patients. Leuk Res. 2002; 26:993-996.
54. Bernasconi P, Cavigliano PM, Boni M, Calatroni S, Klersy C, Giardini I, Rocca B, Crosetto N, Caresana M, Lazzarino M, Bernasconi C. Is FISH a relevant prognostic tool in myelodysplastic syndromes with a normal chromosome pattern on conventional cytogenetics? A study on 57 patients. Leukemia. 2003; 17:2107-2112.
55. Braulke F, Jung K, Schanz J, Götze K, Müller-Thomas C, Platzbecker U, Germing U, Brümmendorf TH, Bug G, Ottmann O, Giagounidis AA, Stadler M, Hofmann WK, et al. Molecular cytogenetic monitoring from CD34+ peripheral blood cells in myelodysplastic syndromes: First results from a prospective multicenter German diagnostic study. Leuk Res. 2013; 37:900-906.
56. Cherry AM, Slovak ML, Campbell LJ, Chun K, Eclache V, Haase D, Haferlach C, Hildebrandt B, Iqbal AM, Jhanwar SC, Ohyashiki K, Sole F, Vandenberghe P, et al. Will a peripheral blood (PB) sample yield the same diagnostic and prognostic cytogenetic data as the concomitant bone marrow (BM) in myelodysplasia? Leuk Res. 2012; 36:832-840.
57. Braulke F, Platzbecker U, Müller-Thomas C, Götze K, Germing U, Brümmendorf TH, Nolte F, Hofmann WK, Giagounidis AA, Lübbert M, Greenberg PL, Bennett JM, Solé F, et al. Validation of cytogenetic risk groups according to International Prognostic Scoring Systems by peripheral blood CD34+FISH: results from a German diagnostic study in comparison with an international control group. Haematologica. 2015; 100:205-213.
58. Babicka L, Ransdorfova S, Brezinova J, Zemanova Z, Sindelarova L, Siskova M, Maaloufova J, Cermak J, Michalova K. Analysis of complex chromosomal rearrangements in adult patients with MDS and AML by multicolor FISH. Leuk Res. 2007; 31:39-47.
59. Tricot G, Boogaerts MA, De Wolf-Peeters C, Van den Berghe H, Verwilghen RL. The myelodysplastic syndromes: different evolution patterns based on sequential morphological and cytogenetic investigations. Br J Haematol. 1985; 59:659-670.
60. Horiike S, Taniwaki M, Misawa S, Abe T. Chromosome abnormalities and karyotypic evolution in 83 patients with myelodysplastic syndrome and predictive value for prognosis. Cancer. 1988; 62:1129-1138.
61. Jabbour E, Takahashi K, Wang X, Cornelison AM, Abruzzo L, Kadia T, Borthakur G, Estrov Z, O'Brien S, Mallo M, Wierda W, Pierce S, Wei Y, et al. Acquisition of cytogenetic abnormalities in patients with IPSS defined lower-risk myelodysplastic syndrome is associated with poor prognosis and transformation to acute myelogenous leukemia. Am J Hematol. 2013; 88:831-837.
62. Haase D. Cytogenetic features in myelodysplastic syndromes. Ann Hematol. 2008; 87:515-526.
63. Schanz J, Steidl C, Fonatsch C, Pfeilstöcker M, Nösslinger T, Tuechler H, Valent P, Hildebrandt B, Giagounidis A, Aul C, Lübbert M, Stauder R, Krieger O, et al. Coalesced multicentric analysis of 2,351 patients with myelodysplastic syndromes indicates an underestimation of poor-risk cytogenetics of myelodysplastic syndromes in the international prognostic scoring system. J Clin Oncol. 2011; 29:1963-1970.
64. Schanz J, Tüchler H, Solé F, Mallo M, Luño E, Cervera J, Granada I, Hildebrandt B, Slovak ML, Ohyashiki K, Steidl C, Fonatsch C, Pfeilstöcker M, et al. New comprehensive cytogenetic scoring system for primary myelodysplastic syndromes (MDS) and oligoblastic acute myeloid leukemia after MDS derived from an international database merge. J Clin Oncol. 2012; 30:820-829.
65. Greaves M, Maley CC. Clonal evolution in cancer. Nature. 2012; 481:306-313.
66. Yates LR, Campbell PJ. Evolution of the cancer genome. Nat Rev Genet. 2012; 13:795-806.
67. Hofmann WK, de Vos S, Komor M, Hoelzer D, Wachsman W, Koeffler HP. Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow. Blood. 2002; 100:3553-3560.
68. Ueda M, Ota J, Yamashita Y, Choi YL, Ohki R, Wada T, Koinuma K, Kano Y, Ozawa K, Mano H. DNA microarray analysis of stage progression mechanism in myelodysplastic syndrome. Br J Haematol. 2003; 123:288-296.
69. Pellagatti A, Esoof N, Watkins F, Langford CF, Vetrie D, Campbell LJ, Fidler C, Cavenagh JD, Eagleton H, Gordon P, Woodcock B, Pushkaran B, Kwan M, et al. Gene expression profiling in the myelodysplastic syndromes using cDNA microarray technology. Br J Haematol. 2004; 125:576-583.
70. Chen G, Zeng W, Miyazato A, Billings E, Maciejewski JP, Kajigaya S, Sloand EM, Young NS. Distinctive gene expression profiles of CD34 cells from patients with myelodysplastic syndrome characterized by specific chromosomal abnormalities. Blood. 2004; 104:4210-4218.
71. Bejar R, Stevenson K, Abdel-Wahab O, Galili N, Nilsson B, Garcia-Manero G, Kantarjian H, Raza A, Levine RL, Neuberg D, Ebert BL. Clinical effect of point mutations in myelodysplastic syndromes. N Engl J Med. 2011; 364:2496-2506.
72. Papaemmanuil E, Gerstung M, Malcovati L, Tauro S, Gundem G, Van Loo P, Yoon CJ, Ellis P, Wedge DC, Pellagatti A, Shlien A, Groves MJ, Forbes SA, et al. Clinical and biological implications of driver mutations in myelodysplastic syndromes. Blood. 2013; 122:3616-3627.
73. Haferlach T, Nagata Y, Grossmann V, Okuno Y, Bacher U, Nagae G, Schnittger S, Sanada M, Kon A, Alpermann T, Yoshida K, Roller A, Nadarajah N, et al. Landscape of genetic lesions in 944 patients with myelodysplastic syndromes. Leukemia. 2014; 28:241-247.
74. Duncavage EJ, Tandon B. The utility of next-generation sequencing in diagnosis and monitoring of acute myeloid leukemia and myelodysplastic syndromes. Int J Lab Hematol. 2015; 37:115-121.
75. Bacher U, Kohlmann A, Haferlach T. Mutational profiling in patients with MDS: ready for every-day use in the clinic? Best Pract Res Clin Haematol. 2015; 28:32-42.
76. Reinig E, Yang F, Traer E, Arora R, Brown S, Rattray R, Braziel R, Fan G, Press R, Dunlap J. Targeted next generation sequencing in myelodysplastic syndrome and chronic myelomonocytic leukemia aids diagnosis in challenging cases and identifies frequent spliceosome mutations in transformed acute myeloid leukemia. Am J Clin Pathol. 2016; 145:497-506.
77. Albitar F, Ma W, Diep K, De Dios I, Agersborg S, Thangavelu M, Brodie S, Albitar M. Deep Sequencing of Cell-Free Peripheral Blood DNA as a Reliable Method for Confirming the Diagnosis of Myelodysplastic Syndrome. Genet Test Mol Biomarkers. 2016; 20:341-345.
78. Ohyashiki K, Aota Y, Akahane D, Gotoh A, Miyazawa K, Kimura Y, Ohyashiki JH. The JAK2 V617F tyrosine kinase mutation in myelodysplastic syndromes (MDS) developing myelofibrosis indicates the myeloproliferative nature in a subset of MDS patients. Leukemia. 2005; 19:2359-2360.
79. Ingram W, Lea NC, Cervera J, Germing U, Fenaux P, Cassinat B, Kiladjian JJ, Varkonyi J, Antunovic P, Westwood NB, Arno MJ, Mohamedali A, Gaken J, et al. The JAK2 V617F mutation identifies a subgroup of MDS patients with isolated deletion 5q and a proliferative bone marrow. Leukemia. 2006; 20:1319-1321.
80. Ogata K, Nakamura K, Yokose N, Tamura H, Tachibana M, Taniguchi O, Iwakiri R, Hayashi T, Sakamaki H, Murai Y, Tohyama K, Tomoyasu S, Nonaka Y, et al. Clinical significance of phenotypic features of blasts in patients with myelodysplastic syndrome. Blood. 2002; 100:3887-3896.
81. Malcovati L, Della Porta MG, Lunghi M, Pascutto C, Vanelli L, Travaglino E, Maffioli M, Bernasconi P, Lazzarino M, Invernizzi R, Cazzola M. Flow cytometry evaluation of erythroid and myeloid dysplasia in patients with myelodysplastic syndrome. Leukemia. 2005; 19:776-783.
82. Westers TM, Cremers EM, Oelschlaegel U, Johansson U, Bettelheim P, Matarraz S, Orfao A, Moshaver B, Brodersen LE, Loken MR, Wells DA, Subirá D, Cullen M, et al. Immunophenotypic analysis of erythroid dysplasia in myelodysplastic syndromes. A report from the IMDSFlow working group. Haematologica. 2017; 102:308-319.
83. Ogata K, Kishikawa Y, Satoh C, Tamura H, Dan K, Hayashi A. Diagnostic application of flow cytometric characteristics of CD34+ cells in low-grade myelodysplastic syndromes. Blood. 2006; 108:1037-1044.
84. Eidenschink Brodersen L, Menssen AJ, Wangen JR, Stephenson CF, de Baca ME, Zehentner BK, Wells DA, Loken MR. Assessment of erythroid dysplasia by "difference from normal" in routine clinical flow cytometry workup. Cytometry B Clin Cytom. 2015; 88:125-135.
85. Cremers EM, Westers TM, Alhan C, Cali C, Wondergem MJ, Poddighe PJ, Ossenkoppele GJ, van de Loosdrecht AA. Multiparameter flow cytometry is instrumental to distinguish myelodysplastic syndromes from non-neoplastic cytopenias. Eur J Cancer. 2016; 54:49-56.
86. Wells DA, Benesch M, Loken MR, Vallejo C, Myerson D, Leisenring WM, Deeg HJ. 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.
87. Benesch M, Deeg HJ, Wells D, Loken M. Flow cytometry for diagnosis and assessment of prognosis in patients with myelodysplastic syndromes. Hematology. 2004; 9:171-177.
88. Porwit A, van de Loosdrecht AA, Bettelheim P, Brodersen LE, Burbury K, Cremers E, Della Porta MG, Ireland R, Johansson U, Matarraz S, Ogata K, Orfao A, Preijers F, et al. Revisiting guidelines for integration of flow cytometry results in the WHO classification of myelodysplastic syndromes-proposal from the International/European LeukemiaNet Working Group for Flow Cytometry in MDS. Leukemia. 2014; 28:1793-1798.
89. Arroyo JL, Fernandez ME, Hernandez JM, Orfao A, San Miguel JF, del Canizo MC. Impact of immunophenotype on prognosis of patients with myelodysplastic syndromes. Its value in patients without karyotypic abnormalities. Hematol J. 2004; 5:227-233.
90. Cremers EM, Westers TM, Alhan C, Cali C, Visser-Wisselaar HA, Chitu DA, van der Velden VH, Te Marvelde JG, Klein SK, Muus P, Vellenga E, de Greef GE, Legdeur MC, et al. Implementation of erythroid lineage analysis by flow cytometry in diagnostic models for myelodysplastic syndromes. Haematologica. 2017; 102:320-326.
91. Kern W, Bacher U, Haferlach C, Alpermann T, Schnittger S, Haferlach T. Multiparameter flow cytometry provides independent prognostic information in patients with suspected myelodysplastic syndromes: A study on 804 patients. Cytometry B Clin Cytom. 2015; 88:154-164.
92. Alhan C, Westers TM, Cremers EM, Cali C, Witte BI, Ossenkoppele GJ, van de Loosdrecht AA. High flow cytometric scores identify adverse prognostic subgroups within the revised international prognostic scoring system for myelodysplastic syndromes. Br J Haematol. 2014; 167:100-109.
93. Alhan C, Westers TM, Cremers EM, Cali C, Witte BI, Ossenkoppele GJ, van de Loosdrecht AA. The myelodysplastic syndromes flow cytometric score: a threeparameter prognostic flow cytometric scoring system. Leukemia. 2016; 30:658-665.
94. Kahn JD, Chamuleau ME, Westers TM, Van de Ven PM, van Dreunen L, van Spronsen M, Ossenkoppele GJ, van de Loosdrecht AA. Regulatory T cells and progenitor B cells are independent prognostic predictors in lower risk myelodysplastic syndromes. Haematologica. 2015; 100:e220-e222.
95. Oelschlaegel U, Westers TM, Mohr B, Kramer M, Parmentier S, Sockel K, Thiede C, Bornhäuser M, Ehninger G, van de Loosdrecht AA, Platzbecker U. Myelodysplastic syndromes with a deletion 5q display a characteristic immunophenotypic profile suitable for diagnostics and response monitoring. Haematologica. 2015; 100:e93-e96.
96. Westers TM, Ireland R, Kern W, Alhan C, Balleisen JS, Bettelheim P, Burbury K, Cullen M, Cutler JA, Della Porta MG, Dräger AM, Feuillard J, Font P, 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.
97. Alhan C, Westers TM, van der Helm LH, Eeltink C, Huls G, Witte BI, Buchi F, Santini V, Ossenkoppele GJ, van de Loosdrecht AA. Absence of aberrant myeloid progenitors by flow cytometry is associated with favorable response to azacitidine in higher risk myelodysplastic syndromes. Cytometry B Clin Cytom. 2014; 86:207-215.
98. Westers TM, Alhan C, Chamuleau ME, van der Vorst MJ, Eeltink C, Ossenkoppele GJ, van de Loosdrecht AA. Aberrant immunophenotype of blasts in myelodysplastic syndromes is a clinically relevant biomarker in predicting response to growth factor treatment. Blood. 2010; 115:1779-1784.
99. Strupp C, Nachtkamp K, Hildebrandt B, Giagounidis A, Haas R, Gattermann N, Bennett JM, Aul C, Germing U. New proposals of the WHO working group (2016) for the diagnosis of myelodysplastic syndromes (MDS): Characteristics of refined MDS types. Leuk Res. 2017; 57:78-84.
100. Greenberg P, Cox C, LeBeau MM, Fenaux P, Morel P, Sanz G, Sanz M, Vallespi T, Hamblin T, Oscier D, Ohyashiki K, Toyama K, Aul C, et al. J.International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood. 1997; 89:2079-2088.
101. Malcovati L, Della Porta MG, Pascutto C, Invernizzi R, Boni M, Travaglino E, Passamonti F, Arcaini L, Maffioli M, Bernasconi P, Lazzarino M, Cazzola M. 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.
102. Bennett JM, Komrokji RS. The myelodysplastic syndromes: diagnosis, molecular biology and risk assessment. Hematology. 2005; 10:258-269.
103. Greenberg PL, Tuechler H, Schanz J, Sanz G, Garcia-Manero G, Solé F, Bennett JM, Bowen D, Fenaux P, Dreyfus F, Kantarjian H, Kuendgen A, Levis A, et al. Revised international prognostic scoring system for myelodysplastic syndromes. Blood. 2012; 120:2454-2465.