Evaluation of the effect of low molecular weight heparin in unexplained recurrent pregnancy loss: a meta-analysis of randomized controlled trials

References

• Rai R, Regan L. Recurrent miscarriage. Lancet. 2006;368(9535):601–611.
   PubMed Web of Science ®Google Scholar
• The Practice Committee of the American Society for Reproductive Medicine. Evaluation and treatment of recurrent pregnancy loss: a committee opinion. Fertil Steril. 2012;98(5):1103–1111.
   PubMed Web of Science ®Google Scholar
• Coomarasamy A, Williams H, Truchanowicz E, et al. A randomized trial of progesterone in women with recurrent miscarriages. N Engl J Med. 2015;373(22):2141–2148.
   PubMed Web of Science ®Google Scholar
• Genetic aspects of female reproduction. Hum Reprod Update. 2008;14(4):293–307.
   PubMed Web of Science ®Google Scholar
• Regan L, Rai R. Epidemiology and the medical causes of miscarriage. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14(5):839–854.
   PubMed Web of Science ®Google Scholar
• de Jong PG, Kaandorp S, Di Nisio M, et al. Aspirin and/or heparin for women with unexplained recurrent miscarriage with or without inherited thrombophilia. Cochrane Database Syst Rev. 2014;7:CD004734.
   PubMed Web of Science ®Google Scholar
• Malassiné A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9(6):531–539.
   PubMed Web of Science ®Google Scholar
• Tempfer CB, Kurz C, Bentz E-K, et al. A combination treatment of prednisone, aspirin, folate, and progesterone in women with idiopathic recurrent miscarriage: a matched-pair study. Fertil Steril. 2006;86(1):145–148.
   PubMed Web of Science ®Google Scholar
• Abbattista M, Gianniello F, Novembrino C, et al. Risk of pregnancy-related venous thromboembolism and obstetrical complications in women with inherited type I antithrombin deficiency: a retrospective, single-centre, cohort study. Lancet Haematol. 2020;7(4):e320–e328.
   PubMed Web of Science ®Google Scholar
• Li J-P, Vlodavsky I. Heparin, heparan sulfate and heparanase in inflammatory reactions. Thromb Haemost. 2009;102(5):823–828.
   PubMed Web of Science ®Google Scholar
• Gris J-C, Mercier E, Quéré I, et al. Low-molecular-weight heparin versus low-dose aspirin in women with one fetal loss and a constitutional thrombophilic disorder. Blood. 2004;103(10):3695–3699.
   PubMed Web of Science ®Google Scholar
• Laskin CA, Spitzer KA, Clark CA, et al. Low molecular weight heparin and aspirin for recurrent pregnancy loss: results from the randomized, controlled HepASA Trial. J Rheumatol. 2009;36(2):279–287.
   PubMed Web of Science ®Google Scholar
• Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009;339:b2535.
   PubMed Web of Science ®Google Scholar
• Higgins J, Wells G. Cochrane handbook for systematic reviews of interventions of interventions. version 5.1.0 [updated March 2011]. Oxford (UK): The Cochrane Collaboration; 2011.
   Google Scholar
• Higgins JPT, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560.
   PubMed Web of Science ®Google Scholar
• Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–1558.
   PubMed Web of Science ®Google Scholar
• Shaaban OM, Abbas AM, Zahran KM, et al. Low-molecular-weight heparin for the treatment of unexplained recurrent miscarriage with negative antiphospholipid antibodies: a randomized controlled trial. Clin Appl Thromb Hemost. 2017;23(6):567–572.
   PubMed Web of Science ®Google Scholar
• Schleussner E, Kamin G, Seliger G, et al. Low-molecular-weight heparin for women with unexplained recurrent pregnancy loss: a multicenter trial with a minimization randomization scheme. Ann Intern Med. 2015;162(9):601–609.
   PubMed Web of Science ®Google Scholar
• Pasquier E, de Saint Martin L, Bohec C, et al. Enoxaparin for prevention of unexplained recurrent miscarriage: a multicenter randomized double-blind placebo-controlled trial. Blood. 2015;125(14):2200–2205.
   PubMed Web of Science ®Google Scholar
• Fawzy M, Shokeir T, El-Tatongy M, et al. Treatment options and pregnancy outcome in women with idiopathic recurrent miscarriage: a randomized placebo-controlled study. Arch Gynecol Obstet. 2008;278(1):33–38.
   PubMed Web of Science ®Google Scholar
• Badawy AM, Khiary M, Sherif LS, et al. Low-molecular weight heparin in patients with recurrent early miscarriages of unknown aetiology. J Obstet Gynaecol. 2008;28(3):280–284.
   PubMedGoogle Scholar
• World Health Organization. World Health Organization manual of the international statistical classification of diseases, injuries and causes of death, ninth revision. Geneva (Switzerland): WHO; 1992.
   Google Scholar
• Pandey MK, Rani R, Agrawal S. An update in recurrent spontaneous abortion. Arch Gynecol Obstet. 2005;272(2):95–108.
   PubMedGoogle Scholar
• Nybo Andersen AM, Wohlfahrt J, Christens P, et al. Maternal age and fetal loss: population based register linkage study. BMJ. 2000;320(7251):1708–1712.
   PubMed Web of Science ®Google Scholar
• ACOG practice bulletin. Management of recurrent pregnancy loss. Number 24. American College of Obstetricians and Gynecologists. Int J Gynaecol Obstet. 2002;78(2):179–190.
   PubMed Web of Science ®Google Scholar
• American Society for Reproductive Medicine. Patient’s fact sheet-recurrent pregnancy loss. Washington (DC): ASRM; 2008.
   Google Scholar
• Branch DW, Gibson M, Silver RM. Clinical practice. Recurrent miscarriage. N Engl J Med. 2010;363(18):1740–1747.
   PubMed Web of Science ®Google Scholar
• Coomarasamy A, Truchanowicz EG, Rai R. Does first trimester progesterone prophylaxis increase the live birth rate in women with unexplained recurrent miscarriages? BMJ. 2011;342:d1914.
   PubMedGoogle Scholar
• Ou H, Yu Q. Efficacy of aspirin, prednisone, and multivitamin triple therapy in treating unexplained recurrent spontaneous abortion: a cohort study. Int J Gynecol Obstet. 2020;148(1):21–26.
   PubMed Web of Science ®Google Scholar
• Christiansen OB, Nybo Andersen A-M, Bosch E, et al. Evidence-based investigations and treatments of recurrent pregnancy loss. Fertil Steril. 2005;83(4):821–839.
   PubMed Web of Science ®Google Scholar
• Fouda UM, Sayed AM, Abdou A-MA, et al. Enoxaparin versus unfractionated heparin in the management of recurrent abortion secondary to antiphospholipid syndrome. Int J Gynaecol Obstet. 2011;112(3):211–215.
   PubMed Web of Science ®Google Scholar
• Walport MJ. Complement. First of two parts. N Engl J Med. 2001;344(14):1058–1066.
   PubMed Web of Science ®Google Scholar
• Oberkersch R, Attorresi AI, Calabrese GC. Low-molecular-weight heparin inhibition in classical complement activation pathway during pregnancy. Thromb Res. 2010;125(5):e240–e245.
   PubMed Web of Science ®Google Scholar
• Van Horn JT, Craven C, Ward K, et al. Histologic features of placentas and abortion specimens from women with antiphospholipid and antiphospholipid-like syndromes. Placenta. 2004;25(7):642–648.
   PubMed Web of Science ®Google Scholar
• Clark P, Walker ID, Langhorne P, et al. SPIN (Scottish Pregnancy Intervention) study: a multicenter, randomized controlled trial of low-molecular-weight heparin and low-dose aspirin in women with recurrent miscarriage. Blood. 2010;115(21):4162–4167.
   PubMed Web of Science ®Google Scholar
• Kaandorp SP, Goddijn M, van der Post JAM, et al. Aspirin plus heparin or aspirin alone in women with recurrent miscarriage. N Engl J Med. 2010;362(17):1586–1596.
   PubMed Web of Science ®Google Scholar
• Edlow AG, Srinivas SK, Elovitz MA. Second-trimester loss and subsequent pregnancy outcomes: what is the real risk? Am J Obstet Gynecol. 2007;197(6):581.e1–581–e6.
   PubMed Web of Science ®Google Scholar
• Daya S, Gunby J. The effectiveness of allogeneic leukocyte immunization in unexplained primary recurrent spontaneous abortion. Am J Reprod Immunol. 1994;32(4):294–302.
   PubMed Web of Science ®Google Scholar
• Saccone G, Schoen C, Franasiak JM, et al. Supplementation with progestogens in the first trimester of pregnancy to prevent miscarriage in women with unexplained recurrent miscarriage: a systematic review and meta-analysis of randomized, controlled trials. Fertil Steril. 2017;107(2):430–438.
   PubMed Web of Science ®Google Scholar
• Javert CT. Repeated abortion; results of treatment in 100 patients. Obstet Gynecol. 1954;3(4):420–434.
   PubMed Web of Science ®Google Scholar
• Brigham SA, Conlon C, Farquharson RG. A longitudinal study of pregnancy outcome following idiopathic recurrent miscarriage. Hum Reprod. 1999;14(11):2868–2871.
   PubMed Web of Science ®Google Scholar
• Bricker L, Farquharson RG. Types of pregnancy loss in recurrent miscarriage: implications for research and clinical practice. Hum Reprod. 2002;17(5):1345–1350.
   PubMed Web of Science ®Google Scholar
• Lee C, Slade P. Miscarriage as a traumatic event: a review of the literature and new implications for intervention. J Psychosom Res. 1996;40(3):235–244.
   PubMed Web of Science ®Google Scholar
• Blomqvist L, Hellgren M, Strandell A. Acetylsalicylic acid does not prevent first-trimester unexplained recurrent pregnancy loss: a randomized controlled trial. Acta Obstet Gynecol Scand. 2018;97(11):1365–1372.
   PubMed Web of Science ®Google Scholar
• Musters AM, Koot YEM, van den Boogaard NM, et al. Supportive care for women with recurrent miscarriage: a survey to quantify women’s preferences. Hum Reprod. 2013;28(2):398–340.
   PubMed Web of Science ®Google Scholar