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Outcomes of venous thromboembolism in patients with inherited thrombophilia treated with direct oral anticoagulants: insights from the RIETE registry

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Abstract

While direct oral anticoagulants (DOACs) are frequently used to treat venous thromboembolism (VTE), the outcomes of patients with inherited thrombophilia (IT) receiving DOACs for VTE remain understudied. We used data from the international RIETE registry to compare the rates of VTE recurrences, major bleeding, and mortality during anticoagulant treatment in VTE patients with and without IT, grouped by the use of DOACs or standard anticoagulant therapy. Among 103,818 enrolled patients, 21,089 (20.3%) were tested for IT, of whom 8422 (39.9%) tested positive: Protein C deficiency 294, Protein S deficiency 726, Antithrombin deficiency 240, Factor V Leiden 2248, Prothrombin gene mutation 1434, combined IT 3480. Overall, 14,189 RIETE patients (6.2% with IT) received DOACs, and 89,629 standard anticoagulation (8.4% with IT), mostly with heparins followed by vitamin K antagonists. Proportions of patients receiving DOACs did not differ between IT-positive and IT-negative patients. Rates of VTE recurrence on anticoagulant treatment were highest in patients with AT deficiency (P < 0.01). Rates of on-treatment major bleeding and all-cause mortality were lowest among patients with Factor V Leiden (FVL) or PT G20210A mutations, compared with patients who tested negative. Patients with IT who received DOACs had lower rates of major bleeding than those receiving standard anticoagulation. Excluding FVL and Protein S deficiency, patients with IT had lower rates of VTE recurrence with DOACs than with standard anticoagulation. DOACs are equally safe and effective in VTE patients with IT, with lower bleeding rates than those on standard anticoagulation.

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Data availability

Access to the original data of this study will be allowed through direct contact with members of the Steering Committee of the RIETE study.

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Acknowledgements

We express our gratitude to SANOFI and ROVI for supporting this Registry with an unrestricted educational grant. We also thank the RIETE Registry Coordinating Center, S&H Medical Science Service, for their quality control data, logistic and administrative support and Prof. Salvador Ortiz, Universidad Autónoma Madrid, Statistical Advisor in S&H Medical Science Service for the statistical analysis of the data presented in this paper.

Members of the RIETE Group: SPAIN: Adarraga MD, Alberich-Conesa A, Aibar J, Alda-Lozano A, Alfonso J, Amado C, Angelina-García M, Arcelus JI, Ballaz A, Barba R, Barbagelata C, Barrón M, Barrón-Andrés B, Beddar-Chaib F, Blanco-Molina A, Criado J, De Ancos C, Del Toro J, Demelo-Rodríguez P, De Juana-Izquierdo C, Díaz-Peromingo JA, Dubois-Silva A, Escribano JC, Falgá C, Farfán-Sedano AI, Fernández-Aracil C, Fernández-Capitán C, Fernández-Jiménez B, Fernández-Reyes JL, Fidalgo MA, Francisco I, Gabara C, Galeano-Valle F, García-Bragado F, García-González C, García-Ortega A, Gavín-Sebastián O, Gil-Díaz A, Gómez AM, Gómez-Cuervo C, Grau E, Guirado L, Gutiérrez J, Hernández-Blasco L, Jara-Palomares L, Jaras MJ, Jiménez D, Jiménez R, Jou I, Joya MD, Lecumberri R, León-Ramírez JM, Lobo JL, López-Jiménez L, López-Miguel P, López-Núñez JJ, López-Ruiz A, López-Sáez JB, Lorenzo A, Lumbierres M, Madridano O, Maestre A, Marchena PJ, Marcos M, Martín del Pozo M, Martín-Martos F, Maza JM, Mena E, Mercado MI, Moises J, Monreal M, Morales MV, Navas MS, Nieto JA, Núñez-Fernández MJ, Olid M, Ordieres-Ortega L, Ortiz M, Osorio J, Otálora S, Otero R, Pacheco-Gómez N, Pagán J, Palomeque AC, Paredes E, Parra P, Pedrajas JM, Pérez-Ductor C, Pérez-Jacoiste MA, Pérez-Pinar M, Peris ML, Pesce ML, Porras JA, Puchades R, Rivera-Cívico F, Rodríguez-Cobo A, Rosa V, Romero-Brugera M, Ruiz-Artacho P, Ruiz-Giménez N, Ruiz-Ruiz J, Salgueiro G, Sancho T, Sendín V, Sigüenza P, Soler S, Suárez-Fernández S, Tirado R, Tolosa C, Torrents-Vilar A, Torres MI, Trujillo-Santos J, Usandizaga E, Uresandi F, Valle R, Varona JF, Vidal G, Villalobos A, Villares P, AUSTRIA: Ay C, Nopp S, Pabinger I, BELGIUM: Vanassche T, Verhamme P, Verstraete A, BRAZIL: Yoo HHB, COLOMBIA: Montenegro AC, Morales SN, Roa J, CZECH REPUBLIC: Hirmerova J, Malý R, FRANCE: Bertoletti L, Bura-Riviere A, Catella J, Chopard R, Couturaud F, Espitia O, Grange C, Leclercq B, Le Mao R, Mahé I, Moustafa F, Plaisance L, Sarlon-Bartoli G, Suchon P, Versini E, GERMANY: Schellong S, ISRAEL: Brenner B, Dally N, Tzoran I, IRAN: Sadeghipour P, Rashidi F, ITALY: Barillari G, Basaglia M, Bilora F, Brandolin B, Ciammaichella M, Colaizzo D, Dentali F, Di Micco P, Grandone E, Imbalzano E, Marcon C, Pesavento R, Poz A, Prandoni P, Siniscalchi C, Taflaj B, Tufano A, Visonà A, Zalunardo B, LATVIA: Paluga R, Skride A, Kigitovica D, PORTUGAL: Fonseca S, Marques R, Meireles J, Pinto S, REPUBLIC OF MACEDONIA: Bosevski M, Trajkoca M, Zdraveska M, SWITZERLAND: Bounameaux H, Mazzolai L, UNITED KINGDOM: Aujayeb A, USA: Caprini JA, Weinberg I, VIETNAM: Bui HM. Coordinator of the RIETE Registry: Manuel Monreal. RIETE Steering Committee Members: Paolo Prandoni, Benjamin Brenner and Dominique Farge-Bancel. RIETE National Coordinators: Raquel Barba (Spain), Pierpaolo Di Micco (Italy), Laurent Bertoletti (France), Sebastian Schellong (Germany), Inna Tzoran (Israel), Abilio Reis (Portugal), Marijan Bosevski (R. Macedonia), Henri Bounameaux (Switzerland), Radovan Malý (Czech Republic), Peter Verhamme (Belgium), Joseph A. Caprini (USA), Hanh My Bui (Vietnam). RIETE Registry Coordinating Center: S & H Medical Science Service.

Funding

RIETE is an investigator-initiated registry. It has been previously supported by Red Respira from the Instituto Carlos III, Spain (Red Respira-ISCiii-RTIC-03/11), by Sanofi Spain in Spain and by Bayer Pharma AG for the rest of the world. None of these sponsors have had any role in the design of the registry nor do they have rights to access the database, review or comment on pre-published studies from RIETE.

Author information

Authors and Affiliations

  1. National Hemophilia Center & Institute of Thrombosis & Hemostasis, Sheba Medical Center, Tel Hashomer, Derech Sheba 2, 52621, Ramat Gan, Israel

    Omri Cohen, Gili Kenet & Sarina Levy-Mendelovich

  2. Amalia Biron Research Institute of Thrombosis and Hemostasis, School of Medicine, Tel Aviv University, Tel Aviv, Israel

    Omri Cohen, Gili Kenet & Sarina Levy-Mendelovich

  3. Department of Medicine and Surgery, University of Insubria, Varese, Italy

    Omri Cohen

  4. Department of Hematology and Bone Marrow Transplantation, Rambam Healthcare Campus, Haifa, Israel

    Inna Tzoran & Benjamin Brenner

  5. Department of Internal Medicine, Hospital Universitario de Fuenlabrada, Madrid, Spain

    Cristina De Ancos

  6. Department of Pneumonology, Hospital General Universitario de Albacete, Albacete, Spain

    Patricia López-Miguel

  7. Department of Internal Medicine, Hospital Universitario HM Montepríncipe, HM Hospitales, Boadilla del Monte, Madrid, Spain

    José F. Varona

  8. Department of Internal Medicine, Hôpital Édouard Herriot, Lyon, France

    Judith Catella

  9. Faculty of Health Sciences, Universidad Católica San Antonio de Murcia (UCAM), El Centro de Investigación Biomédica en Red Enfermedades Respiratorias (CIBERS), Madrid, Spain

    Manuel Monreal

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  1. Omri Cohen
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  2. Gili Kenet
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  3. Sarina Levy-Mendelovich
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  4. Inna Tzoran
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  5. Benjamin Brenner
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  6. Cristina De Ancos
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  7. Patricia López-Miguel
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  8. José F. Varona
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  9. Judith Catella
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  10. Manuel Monreal
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Consortia

and the RIETE investigators

  • M. D. Adarraga
  • , A. Alberich-Conesa
  • , J. Aibar
  • , A. Alda-Lozano
  • , J. Alfonso
  • , C. Amado
  • , M. Angelina-García
  • , J. I. Arcelus
  • , A. Ballaz
  • , R. Barba
  • , C. Barbagelata
  • , M. Barrón
  • , B. Barrón-Andrés
  • , F. Beddar-Chaib
  • , A. Blanco-Molina
  • , J. Criado
  • , C. De Ancos
  • , J. Del Toro
  • , P. Demelo-Rodríguez
  • , C. De Juana-Izquierdo
  • , J. A. Díaz-Peromingo
  • , A. Dubois-Silva
  • , J. C. Escribano
  • , C. Falgá
  • , A. I. Farfán-Sedano
  • , C. Fernández-Aracil
  • , C. Fernández-Capitán
  • , B. Fernández-Jiménez
  • , J. L. Fernández-Reyes
  • , M. A. Fidalgo
  • , I. Francisco
  • , C. Gabara
  • , F. Galeano-Valle
  • , F. García-Bragado
  • , C. García-González
  • , A. García-Ortega
  • , O. Gavín-Sebastián
  • , A. Gil-Díaz
  • , A. M. Gómez
  • , C. Gómez-Cuervo
  • , E. Grau
  • , L. Guirado
  • , J. Gutiérrez
  • , L. Hernández-Blasco
  • , L. Jara-Palomares
  • , M. J. Jaras
  • , D. Jiménez
  • , R. Jiménez
  • , I. Jou
  • , M. D. Joya
  • , R. Lecumberri
  • , J. M. León-Ramírez
  • , J. L. Lobo
  • , L. López-Jiménez
  • , P. López-Miguel
  • , J. J. López-Núñez
  • , A. López-Ruiz
  • , J. B. López-Sáez
  • , A. Lorenzo
  • , M. Lumbierres
  • , O. Madridano
  • , A. Maestre
  • , P. J. Marchena
  • , M. Marcos
  • , M. Martín del Pozo
  • , F. Martín-Martos
  • , J. M. Maza
  • , E. Mena
  • , M. I. Mercado
  • , J. Moises
  • , M. Monreal
  • , M. V. Morales
  • , M. S. Navas
  • , J. A. Nieto
  • , M. J. Núñez-Fernández
  • , M. Olid
  • , L. Ordieres-Ortega
  • , M. Ortiz
  • , J. Osorio
  • , S. Otálora
  • , R. Otero
  • , N. Pacheco-Gómez
  • , J. Pagán
  • , A. C. Palomeque
  • , E. Paredes
  • , P. Parra
  • , J. M. Pedrajas
  • , C. Pérez-Ductor
  • , M. A. Pérez-Jacoiste
  • , M. Pérez-Pinar
  • , M. L. Peris
  • , M. L. Pesce
  • , J. A. Porras
  • , R. Puchades
  • , F. Rivera-Cívico
  • , A. Rodríguez-Cobo
  • , V. Rosa
  • , M. Romero-Brugera
  • , P. Ruiz-Artacho
  • , N. Ruiz-Giménez
  • , J. Ruiz-Ruiz
  • , G. Salgueiro
  • , T. Sancho
  • , V. Sendín
  • , P. Sigüenza
  • , S. Soler
  • , S. Suárez-Fernández
  • , R. Tirado
  • , C. Tolosa
  • , A. Torrents-Vilar
  • , M. I. Torres
  • , J. Trujillo-Santos
  • , E. Usandizaga
  • , F. Uresandi
  • , R. Valle
  • , J. F. Varona
  • , G. Vidal
  • , A. Villalobos
  • , P. Villares
  • , C. Ay
  • , S. Nopp
  • , I. Pabinger
  • , T. Vanassche
  • , P. Verhamme
  • , A. Verstraete
  • , H. H. B. Yoo
  • , A. C. Montenegro
  • , S. N. Morales
  • , J. Roa
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  • , B. Leclercq
  • , R. Le Mao
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  • , F. Moustafa
  • , L. Plaisance
  • , G. Sarlon-Bartoli
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  • , E. Versini
  • , S. Schellong
  • , B. Brenner
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  • , I. Tzoran
  • , P. Sadeghipour
  • , F. Rashidi
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  • , M. Basaglia
  • , F. Bilora
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  • , M. Ciammaichella
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  • , F. Dentali
  • , P. Di Micco
  • , E. Grandone
  • , E. Imbalzano
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  • , R. Pesavento
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  • , C. Siniscalchi
  • , B. Taflaj
  • , A. Tufano
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  • , M. Trajkoca
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  • , H. Bounameaux
  • , L. Mazzolai
  • , A. Aujayeb
  • , J. A. Caprini
  • , I. Weinberg
  • , H. M. Bui
  • , Manuel Monreal
  • , Paolo Prandoni
  • , Benjamin Brenner
  • , Dominique Farge-Bancel
  • , Raquel Barba
  • , Pierpaolo Di Micco
  • , Laurent Bertoletti
  • , Sebastian Schellong
  • , Inna Tzoran
  • , Abilio Reis
  • , Marijan Bosevski
  • , Henri Bounameaux
  • , Radovan Malý
  • , Peter Verhamme
  • , Joseph A. Caprini
  •  & Hanh My Bui

Contributions

Study conception and design: O Cohen, S Levy-Mendelovich, M Monreal; Interpretation of the data: all authors; Drafting of the manuscript: O Cohen, G Kenet; Critical revision of the manuscript: all authors; Final approval of the manuscript: all authors.

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Correspondence to Omri Cohen.

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A full list of RIETE investigators is given in the section Acknowledgements.

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Cohen, O., Kenet, G., Levy-Mendelovich, S. et al. Outcomes of venous thromboembolism in patients with inherited thrombophilia treated with direct oral anticoagulants: insights from the RIETE registry. J Thromb Thrombolysis 57, 710–720 (2024). https://doi.org/10.1007/s11239-024-02957-4

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