A longitudinal analysis of paroxysmal nocturnal haemoglobinuria-type cells in patients with bone marrow failure: Results of a prospective multi-centre study in Japan.

aplastic anaemia bone marrow failure flow cytometry myelodysplastic syndrome paroxysmal nocturnal haemoglobinuria-type cell

Journal

British journal of haematology
ISSN: 1365-2141
Titre abrégé: Br J Haematol
Pays: England
ID NLM: 0372544

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 31 07 2023
received: 26 04 2023
accepted: 07 08 2023
pubmed: 1 9 2023
medline: 1 9 2023
entrez: 1 9 2023
Statut: ppublish

Résumé

To determine the prevalence and clinical relevance of glycosylphosphatidylinositol-anchored protein-deficient (GPI[-]) cell populations (paroxysmal nocturnal haemoglobinuria [PNH]-type cells) in patients with acquired aplastic anaemia (AA) or myelodysplastic syndrome (MDS), we prospectively studied peripheral blood samples of 2402 patients (1075 with AA, 900 with MDS, 144 with PNH, and 283 with other anaemia) using a high-sensitivity flow cytometry assay in a nationwide multi-centre observational study. PNH-type cells were detected in 52.6% of AA and 13.7% of MDS patients. None of the 35 patients with refractory anaemia (RA) with ringed sideroblasts or the 86 patients with RA with excess of blasts carried PNH-type cells. Among the 317 patients possessing PNH-type granulocytes, the percentage of PNH-type granulocytes increased by ≥10% in 47 patients (14.8%), remained unchanged in 240 patients (75.7%), and decreased by ≥10% in 30 patients (9.5%) during 3 years of follow-up. PNH-type granulocyte expansion occurred more frequently (27.1%) in the 144 patients who originally carried PNH-type granulocytes ≥1% than in the 173 patients with PNH-type granulocytes <1% (4.6%). This study confirmed that PNH-type cells are undetectable in authentic clonal MDS patients, and the presence of ≥1% PNH-type granulocytes predicts a higher likelihood of PNH-type cell expansion than with <1% PNH-type granulocytes.

Identifiants

pubmed: 37654088
doi: 10.1111/bjh.19048
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

468-476

Informations de copyright

© 2023 British Society for Haematology and John Wiley & Sons Ltd.

Références

Schrezenmeier H, Hertenstein B, Wagner B, Raghavachar A, Heimpel H. A pathogenetic link between aplastic anemia and paroxysmal nocturnal hemoglobinuria is suggested by a high frequency of aplastic anemia patients with a deficiency of phosphatidylinositol glycan anchored proteins. Exp Hematol. 1995;23(1):81-87. https://www.ncbi.nlm.nih.gov/pubmed/7995374
Dunn DE, Tanawattanacharoen P, Boccuni P, Nagakura S, Green SW, Kirby MR, et al. Paroxysmal nocturnal hemoglobinuria cells in patients with bone marrow failure syndromes. Ann Intern Med. 1999;131(6):401-408. https://doi.org/10.7326/0003-4819-131-6-199909210-00002
Wang H, Chuhjo T, Yasue S, Omine M, Nakao S. Clinical significance of a minor population of paroxysmal nocturnal hemoglobinuria-type cells in bone marrow failure syndrome. Blood. 2002;100(12):3897-3902. https://doi.org/10.1182/blood-2002-03-0799
Sugimori C, Mochizuki K, Qi Z, Sugimori N, Ishiyama K, Kondo Y, et al. Origin and fate of blood cells deficient in glycosylphosphatidylinositol-anchored protein among patients with bone marrow failure. Br J Haematol. 2009;147(1):102-112. https://doi.org/10.1111/j.1365-2141.2009.07822.x
Scheinberg P, Marte M, Nunez O, Young NS. Paroxysmal nocturnal hemoglobinuria clones in severe aplastic anemia patients treated with horse anti-thymocyte globulin plus cyclosporine. Haematologica. 2010;95(7):1075-1080. https://doi.org/10.3324/haematol.2009.017889
Kulagin A, Lisukov I, Ivanova M, Golubovskaya I, Kruchkova I, Bondarenko S, et al. Prognostic value of paroxysmal nocturnal haemoglobinuria clone presence in aplastic anaemia patients treated with combined immunosuppression: results of two-centre prospective study. Br J Haematol. 2014;164(4):546-554. https://doi.org/10.1111/bjh.12661
Raza A, Ravandi F, Rastogi A, Bubis J, Lim SH, Weitz I, et al. A prospective multicenter study of paroxysmal nocturnal hemoglobinuria cells in patients with bone marrow failure. Cytometry B Clin Cytom. 2014;86(3):175-182. https://doi.org/10.1002/cyto.b.21139
Morado M, Freire Sandes A, Colado E, Subirá D, Isusi P, Soledad Noya M, et al. Diagnostic screening of paroxysmal nocturnal hemoglobinuria: prospective multicentric evaluation of the current medical indications. Cytometry B Clin Cytom. 2017;92(5):361-370. https://doi.org/10.1002/cyto.b.21480
Nakao S, Sugimori C, Yamazaki H. Clinical significance of a small population of paroxysmal nocturnal hemoglobinuria-type cells in the management of bone marrow failure. Int J Hematol. 2006;84(2):118-122. https://doi.org/10.1532/IJH97.06077
Fattizzo B, Ireland R, Dunlop A, Yallop D, Kassam S, Large J, et al. Clinical and prognostic significance of small paroxysmal nocturnal hemoglobinuria clones in myelodysplastic syndrome and aplastic anemia. Leukemia. 2021;35(11):3223-3231. https://doi.org/10.1038/s41375-021-01190-9
Sugimori C, Chuhjo T, Feng X, Yamazaki H, Takami A, Teramura M, et al. Minor population of CD55-CD59- blood cells predicts response to immunosuppressive therapy and prognosis in patients with aplastic anemia. Blood. 2006;107(4):1308-1314. https://doi.org/10.1182/blood-2005-06-2485
Zhao X, Zhang L, Jing L, Zhou K, Li Y, Peng G, et al. The role of paroxysmal nocturnal hemoglobinuria clones in response to immunosuppressive therapy of patients with severe aplastic anemia. Ann Hematol. 2015;94(7):1105-1110. https://doi.org/10.1007/s00277-015-2348-5
Narita A, Muramatsu H, Sekiya Y, Okuno Y, Sakaguchi H, Nishio N, et al. Paroxysmal nocturnal hemoglobinuria and telomere length predicts response to immunosuppressive therapy in pediatric aplastic anemia. Haematologica. 2015;100(12):1546-1552. https://doi.org/10.3324/haematol.2015.132530
Brodsky RA, Mukhina GL, Li S, Nelson KL, Chiurazzi PL, Buckley JT, et al. Improved detection and characterization of paroxysmal nocturnal hemoglobinuria using fluorescent aerolysin. Am J Clin Pathol. 2000;114(3):459-466. https://doi.org/10.1093/ajcp/114.3.459
Hosokawa K, Sugimori C, Ishiyama K, Takamatsu H, Noji H, Shichishima T, et al. Establishment of a flow cytometry assay for detecting paroxysmal nocturnal hemoglobinuria-type cells specific to patients with bone marrow failure. Ann Hematol. 2018;97(12):2289-2297. https://doi.org/10.1007/s00277-018-3443-1
Rondelli T, Berardi M, Peruzzi B, Boni L, Caporale R, Dolara P, et al. The frequency of granulocytes with spontaneous somatic mutations: a wide distribution in a normal human population. PloS One. 2013;8(1):e54046. https://doi.org/10.1371/journal.pone.0054046
Camitta BM. Criteria for severe aplastic anaemia. Lancet. 1988;1(8580):303-304. https://doi.org/10.1016/s0140-6736(88)90388-1
Cheson BD, Greenberg PL, Bennett JM, Lowenberg B, Wijermans PW, Nimer SD, et al. Clinical application and proposal for modification of the International Working Group (IWG) response criteria in myelodysplasia. Blood. 2006;108(2):419-425. https://doi.org/10.1182/blood-2005-10-4149
Wang SA, Pozdnyakova O, Jorgensen JL, Medeiros LJ, Stachurski D, Anderson M, et al. Detection of paroxysmal nocturnal hemoglobinuria clones in patients with myelodysplastic syndromes and related bone marrow diseases, with emphasis on diagnostic pitfalls and caveats. Haematologica. 2009;94(1):29-37. https://doi.org/10.3324/haematol.13601
Bessler M, Mason PJ, Hillmen P, Miyata T, Yamada N, Takeda J, et al. Paroxysmal nocturnal haemoglobinuria (PNH) is caused by somatic mutations in the PIG-A gene. EMBO J. 1994;13(1):110-117. https://www.ncbi.nlm.nih.gov/pubmed/8306954
Sutherland DR, Illingworth A, Marinov I, Ortiz F, Andreasen J, Payne D, et al. ICCS/ESCCA consensus guidelines to detect GPI-deficient cells in paroxysmal nocturnal hemoglobinuria (PNH) and related disorders part 2-reagent selection and assay optimization for high-sensitivity testing. Cytometry B Clin Cytom. 2018;94(1):23-48. https://doi.org/10.1002/cyto.b.21610
Ishiyama K, Chuhjo T, Wang H, Yachie A, Omine M, Nakao S. Polyclonal hematopoiesis maintained in patients with bone marrow failure harboring a minor population of paroxysmal nocturnal hemoglobinuria-type cells. Blood. 2003;102(4):1211-1216. https://doi.org/10.1182/blood-2002-12-3706
Yoshizato T, Dumitriu B, Hosokawa K, Makishima H, Yoshida K, Townsley D, et al. Somatic mutations and clonal hematopoiesis in aplastic anemia. N Engl J Med. 2015;373(1):35-47. https://doi.org/10.1056/NEJMoa1414799
Pu JJ, Mukhina G, Wang H, Savage WJ, Brodsky RA. Natural history of paroxysmal nocturnal hemoglobinuria clones in patients presenting as aplastic anemia. Eur J Haematol. 2011;87(1):37-45. https://doi.org/10.1111/j.1600-0609.2011.01615.x
Luzzatto L, Risitano AM. Advances in understanding the pathogenesis of acquired aplastic anaemia. Br J Haematol. 2018;182(6):758-776. https://doi.org/10.1111/bjh.15443

Auteurs

Ken Ishiyama (K)

Department of Hematology, Faculty of Medicine, Institute of Medical Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan.
Department of Hematology, National Center for Global Health and Medicine, Tokyo, Japan.
Japan PNH Study Group, Tokyo, Japan.

Yuji Yonemura (Y)

Japan PNH Study Group, Tokyo, Japan.
Department of Transfusion Medicine and Cell Therapy, Kumamoto University, Kumamoto, Japan.

Tatsuya Kawaguchi (T)

Japan PNH Study Group, Tokyo, Japan.
Department of Medical Technology, Kumamoto Health Science University, Kumamoto, Japan.

Kohei Hosokawa (K)

Department of Hematology, Faculty of Medicine, Institute of Medical Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan.
Japan PNH Study Group, Tokyo, Japan.

Chiharu Sugimori (C)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology, Ishikawa Prefectural Central Hospital, Kanazawa, Japan.

Yasutaka Ueda (Y)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Hiroyuki Takamori (H)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Naoshi Obara (N)

Japan PNH Study Group, Tokyo, Japan.
Department of Medical Sciences, Hematology, Tsukuba University, Tsukuba, Japan.

Hideyoshi Noji (H)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology, Fukushima Medical University, Fukushima, Japan.

Yukari Shirasugi (Y)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Tokai University, Tokyo, Japan.

Kiyoshi Ando (K)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Tokai University, Tokyo, Japan.

Tsutomu Shichishima (T)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology, Fukushima Medical University, Fukushima, Japan.

Haruhiko Ninomiya (H)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology, Tsukuba University, Tsukuba, Japan.

Shigeru Chiba (S)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology, Tsukuba University, Tsukuba, Japan.

Jun-Ichi Nishimura (JI)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Yuzuru Kanakura (Y)

Japan PNH Study Group, Tokyo, Japan.
Department of Hematology and Oncology, Osaka University Graduate School of Medicine, Suita, Japan.

Shinji Nakao (S)

Department of Hematology, Faculty of Medicine, Institute of Medical Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan.
Japan PNH Study Group, Tokyo, Japan.

Classifications MeSH