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CHRONIC MYELOPROLIFERATIVE NEOPLASMS

Distinct clinico-molecular arterial and venous thrombosis scores for myeloproliferative neoplasms risk stratification

Leukemia volume 38, pages 326–339 (2024)Cite this article

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Abstract

Current recommended risk scores to predict thrombotic events associated with myeloproliferative neoplasms (MPN) do not discriminate between arterial and venous thrombosis despite their different physiopathology. To define novel stratification systems, we delineated a comprehensive landscape of MPN associated thrombosis across a large long-term follow-up MPN cohort. Prior arterial thrombosis, age >60 years, cardiovascular risk factors and presence of TET2 or DNMT3A mutations were independently associated with arterial thrombosis in multivariable analysis. ARTS, an ARterial Thrombosis Score, based on these four factors, defined low- (0.37% patients-year) and high-risk (1.19% patients-year) patients. ARTS performance was superior to the two-tiered conventional risk stratification in our training cohort, across all MPN subtypes, as well as in two external validation cohorts. Prior venous thrombosis and presence of a JAK2V617F mutation with a variant allelic frequency ≥50% were independently associated with venous thrombosis. The discrimination potential of VETS, a VEnous Thrombosis Score based on these two factors, was poor, similar to the two-tiered conventional risk stratification. Our study pinpoints arterial and venous thrombosis clinico-molecular differences and proposes an arterial risk score for more accurate patients’ stratification. Further improvement of venous risk scores, accounting for additional factors and considering venous thrombosis as a heterogeneous entity is warranted.

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Fig. 1: Incidence and type of arterial and venous thrombotic events in patients diagnosed with MPN.
Fig. 2: Molecular characteristics of patients diagnosed with arterial thrombotic events during MPN follow-up.
Fig. 3: Molecular characteristics of patients diagnosed with venous thrombotic events during MPN follow-up.
Fig. 4: Clinical, biological and molecular factors associated with arterial or venous thrombotic events occurrence in MPN.
Fig. 5: Clinico-molecular arterial thrombosis risk scores in global MPN training cohort and in the two external validation cohorts.
Fig. 6: Clinico-molecular arterial risk score in MPN subtype cohorts.

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Data availability

The datasets analyzed during the current study are available from the corresponding author LB.

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Acknowledgements

The authors thank the clinical care team of the Comprehensive Myeloproliferative Neoplasms Center for samples and data collection, and the staff of the cellular biology laboratory for excellent technical assistance. The authors also thank the French Intergroup for Myeloproliferative neoplasms (FIM) for insightful discussions. This research was supported with grants from “Association Laurette Fugain”, “Féderation Leucémie Espoir”, “Fondation ARC” and “INCa PrevBio”. Lina Benajiba is a “CCA-INSERM Bettencourt” and an “ATIP-Avenir” Laureate. Graphical abstract was partially generated using Biorender.com.

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Authors and Affiliations

  1. Université Paris Cité, APHP, Hôpital Saint-Louis, Centre d’Investigations Cliniques, INSERM CIC 1427, Paris, France

    Hélène Pasquer, Rafael Daltro de Oliveira, Loic Vasseur, Juliette Soret-Dulphy, Lin-Pierre Zhao, Clémence Marcault, Marine Cazaux, Nicolas Gauthier, Jean-Jacques Kiladjian & Lina Benajiba

  2. INSERM UMR 944, Institut de Recherche Saint-Louis, Paris, France

    Hélène Pasquer & Lina Benajiba

  3. Université Paris Cité, APHP, Hôpital Saint-Louis, Laboratoire de Biologie Cellulaire, Paris, France

    Nabih Maslah, Emmanuelle Verger, Stéphane Giraudier & Bruno Cassinat

  4. INSERM UMR 1131, Institut de Recherche Saint-Louis, Paris, France

    Nabih Maslah, Emmanuelle Verger, Stéphane Giraudier, Bruno Cassinat & Jean-Jacques Kiladjian

  5. Université Paris Cité, APHP, Hôpital Saint-Louis, Département d’hématologie et d’Immunologie, Paris, France

    Nathalie Parquet & Emmanuel Raffoux

  6. APHP, Hôpital Saint-Louis, Département d’hématologie et d’Immunologie, Paris, France

    William Vainchenker

  7. Univ Angers, Nantes Université, CHU Angers, Inserm, CNRS, CRCI2NA, Angers, France

    Valérie Ugo & Damien Luque Paz

  8. Université Paris Est Créteil, APHP, Hôpital Henri Mondor, Service d’hématologie, Créteil, France

    Lydia Roy

  9. Université de Bretagne Occidentale, CHU de Brest, Service d’Hématologie Biologique, Brest, France

    Wayne-Corentin Lambert & Eric Lippert

  10. Université de Bretagne Occidentale, CHU de Brest, Service d’Hématologie et d’Hémostase Clinique, Brest, France

    Jean-Christophe Ianotto

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  1. Hélène Pasquer
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Contributions

CM, LPZ, RDO, NG, MC, EL, JCI and DLP collected the data. SG, NM, EV, BC, WCL, EL, VU and DLP performed molecular analyses. JSD, RDO, WV, NP, ER, SG, JJK, LB, LR and JCI provided patients care. LV performed statistical analysis. LB and HP analyzed the data, performed statistical analysis and wrote the manuscript. LB designed and supervised the study. All co-authors reviewed, edited and critically discussed the manuscript.

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Correspondence to Lina Benajiba.

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Competing interests

LB has received research support from Gilead and Pfizer for research projects unrelated to the current study. The remaining authors declare no competing financial interests related to this work.

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Pasquer, H., Daltro de Oliveira, R., Vasseur, L. et al. Distinct clinico-molecular arterial and venous thrombosis scores for myeloproliferative neoplasms risk stratification. Leukemia 38, 326–339 (2024). https://doi.org/10.1038/s41375-023-02114-5

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