Thrombosis Update (Dec 2023)
A prognostic score to identify women at increased risk for abnormal uterine bleeding during anticoagulation for venous thromboembolism
- Gabrielle Sarlon-Bartoli,
- Juan Criado,
- Saskia Middeldorp,
- José Antonio Nieto,
- María del Carmen Díaz-Pedroche,
- Farès Moustafa,
- Nuria Ruiz-Giménez,
- Benjamin Brenner,
- Manuel Monreal,
- Pierpaolo DI Micco,
- 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,
- M.D. Adarraga,
- P. Agudo,
- C. Amado,
- J.I. Arcelus,
- A. Ballaz,
- J. Bascuñana,
- R. Barba,
- C. Barbagelata,
- M. Barrón,
- B. Barrón-Andrés,
- A. Blanco-Molina,
- F. Beddar Chaib,
- E. Botella,
- I. Cañas,
- R. Carrero-Arribas,
- I. Casado,
- P. Cerdá,
- L. Chasco,
- J. Criado,
- C. de Ancos,
- J. de Miguel,
- J. del Toro,
- P. Demelo-Rodríguez,
- A.M. Díaz-Brasero,
- M.C. Díaz-Pedroche,
- J.A. Díaz-Peromingo,
- I.M. Domínguez,
- A. Dubois-Silva,
- J.C. Escribano,
- F. Espósito,
- A.I. Farfán-Sedano,
- C. Falgá,
- C. Fernández-Capitán,
- B. Fernández-Jiménez,
- J. Fernández-Muixi,
- J.L. Fernández-Reyes,
- C. Font,
- I. Francisco,
- F. Galeano-Valle,
- M.A. García,
- F. García-Bragado,
- M. García de Herreros,
- O. Gavín-Blanco,
- A. Gil-Díaz,
- C. Gómez-Cuervo,
- A.M. Gómez-Mosquera,
- M. Gonzalez-Moreno,
- E. Grau,
- L. Guirado,
- J. Gutiérrez,
- L. Hernández-Blasco,
- L. Jara-Palomares,
- M.J. Jaras,
- D. Jiménez,
- I. Jou,
- M.D. Joya,
- B. Lacruz,
- S. Lainez-Justo,
- Latorre A,
- Lima J,
- Lobo Jl,
- M. López-De la Fuente,
- L. López-Jiménez,
- M. López-Meseguer,
- P. López-Miguel,
- J.J. López-Núñez,
- R. López-Reyes,
- J.B. López-Sáez,
- M.A. Lorente,
- A. Lorenzo,
- O. Madridano,
- A. Maestre,
- P.J. Marchena,
- J.M. Martín-Guerra,
- F. Martín-Martos,
- M. Mellado,
- E. Mena,
- J. Moisés,
- M.I. Mercado,
- M. Monreal,
- A. Muñoz-Blanco,
- G. Muñoz-Gamito,
- M.V. Morales,
- J.A. Nieto,
- E. Noguera-Gras,
- M.J. Núñez-Fernández,
- M. Olid-Velilla,
- J. Osorio,
- S. Otalora,
- R. Otero,
- D. Paredes-Ruiz,
- P. Parra,
- V. Parra,
- J.M. Pedrajas,
- M. Pérez-López,
- M.L. Peris,
- M.L. Pesce,
- J.A. Porras,
- J. Poyo-Molina,
- R. Puchades,
- A. Riera-Mestre,
- F. Rivera-Civico,
- A. Rivera-Gallego,
- M. Roca,
- V. Rosa,
- A. Rodríguez-Cobo,
- C. Rodríguez-Matute,
- P. Ruiz-Artacho,
- N. Ruiz-Giménez,
- J. Ruiz-Ruiz,
- G. Salgueiro,
- T. Sancho,
- V. Sendín,
- P. Sigüenza,
- S. Soler,
- B. Suárez-Rodríguez,
- J.M. Suriñach,
- G. Tiberio,
- M.I. Torres,
- A. Torres-Sánchez,
- J. Trujillo-Santos,
- F. Uresandi,
- E. Usandizaga,
- R. Valle,
- J.F. Varona,
- L. Vela,
- J.R. Vela,
- A. Villalobos,
- P. Villares,
- C. Ay,
- S. Nopp,
- I. Pabinger,
- M.M. Engelen,
- C. Martens,
- P. Verhamme,
- H.H.B. Yoo,
- J.D. Arguello,
- A.C. Montenegro,
- J. Roa,
- J. Hirmerova,
- R. Malý,
- S. Accassat,
- L. Bertoletti,
- A. Bura-Riviere,
- J. Catella,
- R. Chopard,
- F. Couturaud,
- O. Espitia,
- S. El Harake,
- R. Le Mao,
- I. Mahé,
- F. Moustafa,
- L. Plaisance,
- G. Sarlon-Bartoli,
- P. Suchon,
- E. Versini,
- S. Schellong,
- A. Braester,
- B. Brenner,
- G. Kenet,
- I. Tzoran,
- P. Sadeghipour,
- M. Basaglia,
- F. Bilora,
- C. Bortoluzzi,
- B. Brandolin,
- M. Ciammaichella,
- A. De Angelis,
- F. Dentali,
- P. Di Micco,
- E. Imbalzano,
- S. Merla,
- R. Pesavento,
- P. Prandoni,
- C. Siniscalchi,
- A. Tufano,
- A. Visonà,
- N. Vo Hong,
- B. Zalunardo,
- D. Kigitovica,
- E. Rusa,
- A. Skride,
- S. Fonseca,
- M. Manuel,
- J. Meireles,
- M. Bosevski,
- A. Eftimova,
- M. Zdraveska,
- H. Bounameaux,
- L. Mazzolai,
- A. Aujayeb,
- J.A. Caprini,
- I. Weinberg,
- H.M. Bui
Affiliations
- Gabrielle Sarlon-Bartoli
- Department of Vascular Medicine and Arterial Hypertension, Hôpital de la Timone, Marseille, France; Corresponding author. Department of Vascular Medicine and Arterial Hypertension. Aix-Marseille Université, Assistance Publique Hôpitaux de Marseille - Hôpital de la Timone, 264, rue Saint-Pierre, 13385, Marseille cedex 05, France.
- Juan Criado
- Department of Internal Medicine, Hospital Universitario Reina Sofía, Córdoba, Spain
- Saskia Middeldorp
- Department of Internal Medicine & Research Institute of Health Sciences (RIHS), Radboud University Medical Center, Nijmegen, the Netherlands
- José Antonio Nieto
- Department of Internal Medicine, Hospital General Virgen de la Luz, Cuenca, Spain
- María del Carmen Díaz-Pedroche
- Department of Internal Medicine, Hospital Universitario 12 de Octubre, Madrid, Spain
- Farès Moustafa
- Department of Emergency, Clermont-Ferrand University Hospital, Clermont-Ferrand, France
- Nuria Ruiz-Giménez
- Department of Internal Medicine, Hospital Universitario de La Princesa, Madrid, Spain
- Benjamin Brenner
- Department of Haematology and Bone Marrow Transplantation, Rambam Health Care Campus, Haifa, Israel
- Manuel Monreal
- Chair for the Study of Thromboembolic Disease, Faculty of Health Sciences, UCAM - Universidad Católica San Antonio de Murcia, Spain
- Pierpaolo DI Micco
- Department of Internal Medicine and Emergency Room, Ospedale Buon Consiglio Fatebenefratelli, Naples, Italy
- Manuel Monreal
- Paolo Prandoni
- Benjamin Brenner
- Dominique Farge-Bancel
- Raquel Barba
- Spain
- Pierpaolo Di Micco
- Italy
- Laurent Bertoletti
- France
- Sebastian Schellong
- Germany
- Inna Tzoran
- Israel
- Abilio Reis
- Portugal
- Marijan Bosevski
- Macedonia
- Henri Bounameaux
- Switzerland
- Radovan Malý
- Czech Republic
- Peter Verhamme
- Belgium
- Joseph A. Caprini
- USA
- Hanh My Bui
- Viet Nam
- M.D. Adarraga
- Spain
- P. Agudo
- Spain
- C. Amado
- Spain
- J.I. Arcelus
- Spain
- A. Ballaz
- Spain
- J. Bascuñana
- Spain
- R. Barba
- Spain
- C. Barbagelata
- Spain
- M. Barrón
- Spain
- B. Barrón-Andrés
- Spain
- A. Blanco-Molina
- Spain
- F. Beddar Chaib
- Spain
- E. Botella
- Spain
- I. Cañas
- Spain
- R. Carrero-Arribas
- Spain
- I. Casado
- Spain
- P. Cerdá
- Spain
- L. Chasco
- Spain
- J. Criado
- Spain
- C. de Ancos
- Spain
- J. de Miguel
- Spain
- J. del Toro
- Spain
- P. Demelo-Rodríguez
- Spain
- A.M. Díaz-Brasero
- Spain
- M.C. Díaz-Pedroche
- Spain
- J.A. Díaz-Peromingo
- Spain
- I.M. Domínguez
- Spain
- A. Dubois-Silva
- Spain
- J.C. Escribano
- Spain
- F. Espósito
- Spain
- A.I. Farfán-Sedano
- Spain
- C. Falgá
- Spain
- C. Fernández-Capitán
- Spain
- B. Fernández-Jiménez
- Spain
- J. Fernández-Muixi
- Spain
- J.L. Fernández-Reyes
- Spain
- C. Font
- Spain
- I. Francisco
- Spain
- F. Galeano-Valle
- Spain
- M.A. García
- Spain
- F. García-Bragado
- Spain
- M. García de Herreros
- Spain
- O. Gavín-Blanco
- Spain
- A. Gil-Díaz
- Spain
- C. Gómez-Cuervo
- Spain
- A.M. Gómez-Mosquera
- Spain
- M. Gonzalez-Moreno
- Spain
- E. Grau
- Spain
- L. Guirado
- Spain
- J. Gutiérrez
- Spain
- L. Hernández-Blasco
- Spain
- L. Jara-Palomares
- Spain
- M.J. Jaras
- Spain
- D. Jiménez
- Spain
- I. Jou
- Spain
- M.D. Joya
- Spain
- B. Lacruz
- Spain
- S. Lainez-Justo
- Spain
- Latorre A
- Spain
- Lima J
- Spain
- Lobo Jl
- Spain
- M. López-De la Fuente
- Spain
- L. López-Jiménez
- Spain
- M. López-Meseguer
- Spain
- P. López-Miguel
- Spain
- J.J. López-Núñez
- Spain
- R. López-Reyes
- Spain
- J.B. López-Sáez
- Spain
- M.A. Lorente
- Spain
- A. Lorenzo
- Spain
- O. Madridano
- Spain
- A. Maestre
- Spain
- P.J. Marchena
- Spain
- J.M. Martín-Guerra
- Spain
- F. Martín-Martos
- Spain
- M. Mellado
- Spain
- E. Mena
- Spain
- J. Moisés
- Spain
- M.I. Mercado
- Spain
- M. Monreal
- Spain
- A. Muñoz-Blanco
- Spain
- G. Muñoz-Gamito
- Spain
- M.V. Morales
- Spain
- J.A. Nieto
- Spain
- E. Noguera-Gras
- Spain
- M.J. Núñez-Fernández
- Spain
- M. Olid-Velilla
- Spain
- J. Osorio
- Spain
- S. Otalora
- Spain
- R. Otero
- Spain
- D. Paredes-Ruiz
- Spain
- P. Parra
- Spain
- V. Parra
- Spain
- J.M. Pedrajas
- Spain
- M. Pérez-López
- Spain
- M.L. Peris
- Spain
- M.L. Pesce
- Spain
- J.A. Porras
- Spain
- J. Poyo-Molina
- Spain
- R. Puchades
- Spain
- A. Riera-Mestre
- Spain
- F. Rivera-Civico
- Spain
- A. Rivera-Gallego
- Spain
- M. Roca
- Spain
- V. Rosa
- Spain
- A. Rodríguez-Cobo
- Spain
- C. Rodríguez-Matute
- Spain
- P. Ruiz-Artacho
- Spain
- N. Ruiz-Giménez
- Spain
- J. Ruiz-Ruiz
- Spain
- G. Salgueiro
- Spain
- T. Sancho
- Spain
- V. Sendín
- Spain
- P. Sigüenza
- Spain
- S. Soler
- Spain
- B. Suárez-Rodríguez
- Spain
- J.M. Suriñach
- Spain
- G. Tiberio
- Spain
- M.I. Torres
- Spain
- A. Torres-Sánchez
- Spain
- J. Trujillo-Santos
- Spain
- F. Uresandi
- Spain
- E. Usandizaga
- Spain
- R. Valle
- Spain
- J.F. Varona
- Spain
- L. Vela
- Spain
- J.R. Vela
- Spain
- A. Villalobos
- Spain
- P. Villares
- Spain
- C. Ay
- Austria
- S. Nopp
- Austria
- I. Pabinger
- Austria
- M.M. Engelen
- Belgium
- C. Martens
- Belgium
- P. Verhamme
- Belgium
- H.H.B. Yoo
- Brazil
- J.D. Arguello
- Colombia
- A.C. Montenegro
- Colombia
- J. Roa
- Colombia
- J. Hirmerova
- Czech Republic
- R. Malý
- Czech Republic
- S. Accassat
- France
- L. Bertoletti
- France
- A. Bura-Riviere
- France
- J. Catella
- France
- R. Chopard
- France
- F. Couturaud
- France
- O. Espitia
- France
- S. El Harake
- France
- R. Le Mao
- France
- I. Mahé
- France
- F. Moustafa
- France
- L. Plaisance
- France
- G. Sarlon-Bartoli
- France
- P. Suchon
- France
- E. Versini
- France
- S. Schellong
- Germany
- A. Braester
- Israel
- B. Brenner
- Israel
- G. Kenet
- Israel
- I. Tzoran
- Israel
- P. Sadeghipour
- Iran
- M. Basaglia
- Italy
- F. Bilora
- Italy
- C. Bortoluzzi
- Italy
- B. Brandolin
- Italy
- M. Ciammaichella
- Italy
- A. De Angelis
- Italy
- F. Dentali
- Italy
- P. Di Micco
- Italy
- E. Imbalzano
- Italy
- S. Merla
- Italy
- R. Pesavento
- Italy
- P. Prandoni
- Italy
- C. Siniscalchi
- Italy
- A. Tufano
- Italy
- A. Visonà
- Italy
- N. Vo Hong
- Italy
- B. Zalunardo
- Italy
- D. Kigitovica
- Latvia
- E. Rusa
- Latvia
- A. Skride
- Latvia
- S. Fonseca
- Portugal
- M. Manuel
- Portugal
- J. Meireles
- Portugal
- M. Bosevski
- Macedonia
- A. Eftimova
- Macedonia
- M. Zdraveska
- Macedonia
- H. Bounameaux
- Switzerland
- L. Mazzolai
- Switzerland
- A. Aujayeb
- United Kingdom
- J.A. Caprini
- USA
- I. Weinberg
- USA
- H.M. Bui
- Viet Nam
- Journal volume & issue
-
Vol. 13
p. 100148
Abstract
Introduction: Little is known about the clinical characteristics of women at increased risk for abnormal uterine bleeding (UB) during anticoagulation for venous thromboembolism (VTE). Methods: We used the RIETE registry to identify the baseline characteristics of women developing abnormal UB during anticoagulation. We used logistic regression analysis to identify independent predictors for abnormal UB. Then, we built a prognostic score to identify at-risk women. Results: From March 2001 through October 2022, there were 54,372 women with VTE. During anticoagulation (median, 181 days), 318 (0.6%) developed abnormal UB (major bleeding = 88, clinically relevant non-major (CRNM) = 230). On multivariable analysis, women aged 70 kg, with uterine cancer, recent UB, anemia, estrogen-related VTE, or receiving rivaroxaban or apixaban were at increased risk for abnormal UB. Using the prognostic score, 42,273 women (78%) were at low-risk, 8,828 (16%) intermediate-, and 3,271 (6.1%) at high-risk for abnormal UB. Their rates of abnormal UB were: 0.28 (95%CI: 0.23–0.35), 1.32 (95%CI: 1.07–1.61) and 7.12 (95%CI: 5.98–8.41) bleeds per 100 patient-years, respectively. The c-statistic was 0.80 (95%CI: 0.77–0.83). The rates of major UB were: 0.06 (95%CI: 0.04–0.09), 0.43 (95%CI: 0.30–0.60) and 1.85 (95%CI: 1.31–2.53) per 100 patient-years, respectively (c-statistic: 0.84; 95%CI: 0.80–0.89). The rates of CRNM uterine bleeding were: 0.21 (95%CI: 0.17–0.26), 0.85 (95%CI: 0.65–1.08), and 5.02 (95%CI: 4.09–6.10) bleeds per 100 patient-years, respectively (c-statistic: 0.78; 95%CI: 0.75–0.82). Conclusions: Using 7 variables easily available at admission, we built a prognostic score that reliably identified women with VTE at increased risk for abnormal UB during anticoagulation.