https://doi.org/10.4081/itjm.2024.1749
Retrospective analysis on clinical characteristics and venous thromboembolism outcomes using bridging prophylaxis with low molecular weight heparin for thrombophilic women performing oocyte retrieval for assisted reproductive procedures: 15 years of experience
Published: 17 June 2024
Abstract Views: 353
PDF: 222
HTML: 22
HTML: 22
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
In vitro fertilization (IVF) procedures have been frequently associated with antithrombotic treatment, particularly aspirin or low molecular weight heparin. Historically, this type of treatment has been intended to increase the success rate of IVF with embryo transfer (IVF-ET) and live births after the procedure, as well as to prevent thrombotic disorders during pharmacological ovarian stimulation. Recurrent IVF failures and venous thromboembolism (VTE) complications during IVF-ET may be related to inherited thrombophilia. However, there aren't many studies in the literature on the frequency of VTE or bleeding in women undergoing thromboprophylaxis for IVF-ET, and reports on the caliber of clinical data vary. Thus, in this report, we describe our clinical experience with early antithrombotic prophylaxis with enoxaparin in women who have had thrombophilic defects and are undergoing IVF-ET over a period of years.
Downloads
Download data is not yet available.
PlumX Metrics
PlumX Metrics provide insights into the ways people interact with individual pieces of research output (articles, conference proceedings, book chapters, and many more) in the online environment. Examples include, when research is mentioned in the news or is tweeted about. Collectively known as PlumX Metrics, these metrics are divided into five categories to help make sense of the huge amounts of data involved and to enable analysis by comparing like with like.
Citations
Simon A, Laufer N. Repeated implantation failure: clinical approach. Fertil Steril 2012;97:1039-43.
DOI: https://doi.org/10.1016/j.fertnstert.2012.03.010
Lodigiani C, Di Micco P, Ferrazzi P, et al. Low-molecular-weight heparin in women with repeated implantation failure. Womens Health 2011;7:425-31.
DOI: https://doi.org/10.2217/WHE.11.38
Qublan HS, Eid SS, Ababneh HA, et al. Acquired and inherited thrombophilia: implication in recurrent IVF and embryo transfer failure. Hum Reprod 2006;21:2694-8.
DOI: https://doi.org/10.1093/humrep/del203
Simur A, Ozdemir S, Acar H, et al. Repeated in vitro fertilization failure and its relation with thrombophilia. Gynecol Obstet Invest 2009;67:109-12.
Di Micco P, Russo V, Mastroiacovo D, et al. In vitro fertilization procedures with embryo transfer and their association with thrombophilia, thrombosis and early antithrombotic treatments. J Blood Med 2020;11:185-90.
DOI: https://doi.org/10.2147/JBM.S248988
Di Micco P, D’Uva M, Lodigiani C, Rota LL. Thrombophilia and repeated in vitro fertilization and embryo transfer failure: an open issue. Thromb Haemost 2010;103:472-3.
DOI: https://doi.org/10.1160/TH09-09-0674
Bates SM, Greer IA, Middeldorp S, et al. VTE, thrombophilia, antithrombotic therapy, and pregnancy. Chest 2012;141:e691S-e736S.
DOI: https://doi.org/10.1378/chest.11-2300
Wang L, Huang X, Li X, et al. Efficacy evaluation of low-dose aspirin in IVF/ICSI patients evidence from 13 RCTs: a systematic review and meta-analysis. Medicine 2017;96:e7720.
DOI: https://doi.org/10.1097/MD.0000000000007720
Jahromi BN, Parsanezhad ME, Shomali Z, et al. Ovarian hyperstimulation syndrome: a narrative review of its pathophysiology, risk factors, prevention, classification, and management. Iran J Med Sci 2018;43:248-60.
Cramer ACM, McLean AW, Ahari J. Upper extremity deep venous thrombosis and pulmonary embolus after ovarian hyperstimulation. BMJ Case Rep 2016;2016:bcr2016216719
DOI: https://doi.org/10.1136/bcr-2016-216719
Jang YG, Kim HK, Choi BC, et al. Expression of tissue factor and tissue factor pathway inhibitors during ovulation in rats: a relevance to the ovarian hyperstimulation syndrome. Reprod Biol Endocrinol 2021;19:52.
DOI: https://doi.org/10.1186/s12958-021-00708-1
Mor YS, Schenker JG. Ovarian hyperstimulation syndrome and thrombotic events. Am J Reprod Immunol 2014;72:541-8.
Villani M, Dentali F, Colaizzo D, et al. Pregnancy-related venous thrombosis: comparison between spontaneous and ART conception in an Italian cohort. BMJ Open 2015;5:e008213
DOI: https://doi.org/10.1136/bmjopen-2015-008213
Levy G, Lucidi RS. Thrombophilia and ovarian hyperstimulation syndrome: a case report. Hawaii Med J 2011;70:97-8.
Henriksson P, Westerlund E, Wallen H, et al. Incidence of pulmonary and venous thromboembolism in pregnancies after in vitro fertilisation: cross sectional study. BMJ 2013;346:e8632.
DOI: https://doi.org/10.1136/bmj.e8632
Grandone E, Colaizzo D, Vergura P, et al. Age and homocysteine plasma levels are risk factors for thrombotic complications after ovarian stimulation. Hum Reprod 2004;19:1796-9.
DOI: https://doi.org/10.1093/humrep/deh346
Rogolino A, Coccia ME, Fedi S, et al. Hypercoagulability, high tissue factor and low tissue factor pathway inhibitor levels in severe ovarian hyperstimulation syndrome: possible association with clinical outcome. Blood Coagul Fibrinolysis 2003;14:277-82.
DOI: https://doi.org/10.1097/01.mbc.0000061296.28953.d0
Barbar S, Noventa F, Rossetto V, et al. A risk assessment model for the identification of hospitalized medical patients at risk for venous thromboembolism: the Padua prediction score. J Thrombosis Haemostasis 2010;8:2450-7.
DOI: https://doi.org/10.1111/j.1538-7836.2010.04044.x
Gerotziafas GT, Van Dreden P, d’Argent EM, et al. Impact of blood hypercoagulability on in vitro fertilization outcomes: a prospective longitudinal observational study. Thromb J 2017;15:9.
DOI: https://doi.org/10.1186/s12959-017-0131-7
Grandone E, Villani M, Dentali F, et al. Low-molecular weight heparin in pregnancies after ART. A retrospective study. Thromb Res 2014;134:336-9.
DOI: https://doi.org/10.1016/j.thromres.2014.06.004
Lodigiani C, Dentali F, Banfi E, et al. The effect of parnaparin sodium on in vitro fertilization outcome: a prospective randomized controlled trial. Thromb Res 2017;159:116-21.
DOI: https://doi.org/10.1016/j.thromres.2017.08.006
Devreese KMJ, Ortel TL, Pengo V, de Laat B; Subcommittee on Lupus Anticoagulant/Antiphospholipid Antibodies. Laboratory criteria for antiphospholipid syndrome: communication from the SSC of the ISTH. J Thromb Haemost 2018;16:809-13.
DOI: https://doi.org/10.1111/jth.13976
Schulman S, Kearon C; Subcommittee on Control of Anticoagulation of the Scientific and Standardization Committee of the International Society on Thrombosis and Haemostasis. Definition of major bleeding in clinical investigations of antihemostatic medicinal products in nonsurgical patients. J Thromb Haemost 2005;3:692-4.
DOI: https://doi.org/10.1111/j.1538-7836.2005.01204.x
Jacobson B, Rambiritich V, Paek D, et al. Safety and efficacy of enoxaparin in pregnancy: a systematic review and meta-analysis. Adv Ther 2020;37:27-40.
DOI: https://doi.org/10.1007/s12325-019-01124-z
Stojnic J, Bila J, Tulic L, et al. Severe hemoperitoneum due to ovarian bleeding after transvaginal oocyte retrieval with surgical management: a retrospective analysis and comprehensive review of the literature. Medicina 2023;59:307.
DOI: https://doi.org/10.3390/medicina59020307
Sennström M, Rova K, Hellgren M, et al. Thromboembolism and in vitro fertilization - a systematic review. Acta Obstet Gynecol Scand 2017;96:1045-52.
Rubinstein M, Marazzi A, de Fried EP. Low-dose aspirin treatment improves ovarian responsiveness, uterine and ovarian blood flow velocity, implantation, and pregnancy rates in patients undergoing in vitro fertilization: a prospective, randomized, double-blind placebo-controlled assay. Fertil Steril 1999;71:825-9.
DOI: https://doi.org/10.1016/S0015-0282(99)00088-6
D’Uva M, Di Micco P, Strina I, et al. Hyperhomocysteinemia in women with unexplained sterility or recurrent early pregnancy loss from Southern Italy: a preliminary report. Thromb J 2007;11:10.
DOI: https://doi.org/10.1186/1477-9560-5-10
Coulam CB, Jeyendran RS, Fishel LA, Roussev R. Multiple thrombophilic gene mutations are risk factors for implantation failure. Reprod Biomed Online 2006;12:322-7.
DOI: https://doi.org/10.1016/S1472-6483(10)61004-8
Simur A, Ozdemir S, Acar H, et al. Repeated in vitro fertilization failure and its relation with thrombophilia. Gynecol Obstet Invest 2009;67:109-112.
DOI: https://doi.org/10.1159/000165776
Vaquero E, Lazzarin N, Caserta D, et al. Diagnostic evaluation of women experiencing repeated in vitro fertilization failure. Eur J Obstet Gynecol Reprod Biol 2006;125:79-84.
DOI: https://doi.org/10.1016/j.ejogrb.2005.08.001
Altmäe S, Stavreus-Evers A, Ruiz JR, et al. Variations in folate pathway genes are associated with unexplained female infertility. Fertil Steril 2010;94:130-7.
DOI: https://doi.org/10.1016/j.fertnstert.2009.02.025
Candeloro M, Di Nisio M, Ponzano A, et al. Effects of obesity and thrombophilia on the risk of abortion in women undergoing in vitro fertilization. Front Endocrinol (Lausanne) 2020;11:594867.
DOI: https://doi.org/10.3389/fendo.2020.594867
Potdar N, Gelbaya TA, Konje JC, Nardo LG. Adjunct-low-molecular-weight heparin to improve live birth rate after recurrent implantation failure: a systematic review and meta-analysis. Hum Reprod 2013;19:674-84.
DOI: https://doi.org/10.1093/humupd/dmt032
Dirckx K, Cabri P, Merien A, et al. Does low-dose aspirin improve pregnancy rate in IVF/ICSI? A randomized double-blind placebo-controlled trial. Hum Reprod 2009;24:856-60.
DOI: https://doi.org/10.1093/humrep/den476
Dentali F, Ageno W, Rezoagli E, et al. Low-dose aspirin for in vitro fertilization or intracytoplasmic sperm injection: a systematic review and a meta-analysis of the literature. J Thromb Haemost 2012;10:2075-85.
DOI: https://doi.org/10.1111/j.1538-7836.2012.04886.x
Mahajan N, Naidu P, Gupta S, et al. Deep venous thrombosis in a patient undergoing in-vitro fertilization with oocyte donation. J Hum Reprod Sci 2015;8:182-5.
DOI: https://doi.org/10.4103/0974-1208.165150
Grandone E, Di Micco P, Villani M, et al. Monreal M; RIETE Investigators. Venous thromboembolism in women undergoing assisted reproductive technologies: data from the RIETE registry. Thromb Haemost 2018;118:1962-8.
DOI: https://doi.org/10.1055/s-0038-1673402
Mor YS, Schenker JG. Ovarian hyperstimulation syndrome and thrombotic events. Am J Reprod Immunol 2014;72:541-8.
DOI: https://doi.org/10.1111/aji.12310
Filipovic-Pierucci A, Gabet A, Deneux-Tharaux C, et al. Arterial and venous complications after fertility treatment: a French nationwide cohort study. Eur J Obstet Gynecol Reprod Biol 2019;237:57-63.
DOI: https://doi.org/10.1016/j.ejogrb.2019.02.034
Sennström M, Rova K, Hellgren M, et al. Thromboembolism and in vitro fertilization - a systematic review. Acta Obstet Gynecol Scand 2017;96:1045-52.
DOI: https://doi.org/10.1111/aogs.13147
Rova K, Passmark H, Lindqvist PG. Venous thromboembolism in relation to in vitro fertilization: an approach to determining the incidence and increase in risk in successful cycles. Fertil Steril 2012;97:95-100.
DOI: https://doi.org/10.1016/j.fertnstert.2011.10.038
Yang XL, Chen F, Yang XY, et al. Efficacy of low molecular weight heparin on the outcomes of in vitro fertilization/ intracytoplasmic sperm injection pregnancy in non-thrombophilic women: a meta-analysis. Acta Obstet Gynecol Scand 2018;97:1061-72.
DOI: https://doi.org/10.1111/aogs.13359
Allahbadia GN. Low-molecular-weight heparin (LMWH) in women with repeated implantation failure. J Obstet Gynecol India 2012;62:381-3.
DOI: https://doi.org/10.1007/s13224-012-0308-8
Siristatidis C, Dafopoulos K, El-Khayat W, et al. Administration of prednisolone and low molecular weight heparin in patients with repeated implantation failures: a cohort study. Gynecol Endocrinol 2018;34:136-9.
DOI: https://doi.org/10.1080/09513590.2017.1380182
Urman B, Ata B, Yakin K, et al. Luteal phase empirical low molecular weight heparin administration in patients with failed ICSI embryo transfer cycles: a randomized open-labeled pilot trial. Hum Reprod 2009;24:1640-7.
DOI: https://doi.org/10.1093/humrep/dep086
Berker B, Taşkin S, Kahraman K, et al. The role of low-molecular-weight heparin in recurrent implantation failure: a prospective, quasi-randomized, controlled study. Fertil Steril 2011;95:2499-502.
DOI: https://doi.org/10.1016/j.fertnstert.2010.12.033
Butwick A, Hass C, Wong J, et al. Anticoagulant prescribing practices and anesthetic interventions among anticoagulated pregnant patients: a retrospective study. Int J Obstet Anesth 2014;23:238-45.
DOI: https://doi.org/10.1016/j.ijoa.2014.03.007
Rosencher N, Noack H, Feuring M, et al. Type of anaesthesia and the safety and efficacy of thromboprophylaxis with enoxaparin or dabigatran etexilate in major orthopaedic surgery: pooled analysis of three randomized controlled trials. Thromb J 2012;10:9.
DOI: https://doi.org/10.1186/1477-9560-10-9
How to Cite
Di Micco, P., Lodigiani, C., Rota, L. L., Camporese, G., Strina, I., & Alviggi, C. (2024). Retrospective analysis on clinical characteristics and venous thromboembolism outcomes using bridging prophylaxis with low molecular weight heparin for thrombophilic women performing oocyte retrieval for assisted reproductive procedures: 15 years of experience. Italian Journal of Medicine, 18(2). https://doi.org/10.4081/itjm.2024.1749
Copyright (c) 2024 the Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.