Evidence-based guidelines for the investigation and medical treatment of recurrent miscarriage

Human Reproduction

Volumn 21, Issue 9, 2006, Pages 2216-2222

  Jauniaux, Eric ^a   Farquharson, Roy G ^b   Christiansen, Ole B ^c   Exalto, Niek ^d  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b LIVERPOOL WOMEN S HOSPITAL   (United Kingdom)

^c Rigshospitalet   (Denmark)

^d Infection and Immunology   (Netherlands)

Author keywords

Early pregnancy; Evidence based; Management; Recurrent miscarriage; Treatment

Indexed keywords

ACETYLSALICYLIC ACID; CARDIOLIPIN ANTIBODY; FOLIC ACID; FONDAPARINUX; GLUCOCORTICOID; HEPARIN DERIVATIVE; IMMUNOGLOBULIN; LOW MOLECULAR WEIGHT HEPARIN; LUPUS ANTICOAGULANT; MULTIVITAMIN; NONSTEROID ANTIINFLAMMATORY AGENT; PHOSPHOLIPID ANTIBODY; PREDNISONE; PROGESTERONE; TOXIN; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

AGE; ANAMNESIS; ANAPHYLAXIS; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; BLOOD CELL COUNT; BODY MASS; CHROMOSOME ABERRATION; CLINICAL PROTOCOL; CLINICAL TRIAL; CREUTZFELDT JAKOB DISEASE; DIAGNOSTIC PROCEDURE; DRUG FEVER; DRUG INDUCED HEADACHE; DRUG MEGADOSE; ECHOGRAPHY; EVIDENCE BASED MEDICINE; EXPOSURE; FAMILY HISTORY; FIRST TRIMESTER PREGNANCY; FLUSHING; GASTROSCHISIS; GRANULOMATOSIS; HEART FAILURE; HUMAN; HYPERHOMOCYSTEINEMIA; HYPOSPADIAS; HYSTEROSALPINGOGRAPHY; KARYOTYPING; LOW DRUG DOSE; LUPUS LIKE SYNDROME; LYMPHOMA; MATERNAL DISEASE; META ANALYSIS; MYALGIA; NAUSEA; OSTEOPENIA; PATHOPHYSIOLOGY; PATIENT CARE; PATIENT COUNSELING; PELVIS; PRACTICE GUIDELINE; PREECLAMPSIA; PREGNANCY DIABETES MELLITUS; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; RECURRENT ABORTION; RISK BENEFIT ANALYSIS; SKIN MANIFESTATION; SYSTEMATIC REVIEW; TERATOGENICITY; THROMBOCYTOPENIA; THROMBOPHILIA; UTERUS MALFORMATION;

EID: 33749581700     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/del150     Document Type: Article

References (80)

1. Alberman E (1992) Spontaneous abortion: Epidemiology. In Stabile S, Grudzinskas G and Chard T (eds) Spontaneous Abortion: Diagnosis and Treatment. Springer-Verlag, London, pp. 9-30.
2. Andersen AMN, Wohlfahrt J, Christens P, Olsen J and Melbye M (2000) Maternal age and fetal loss: Population based register linkage study. BMJ 320,1708-1712.
3. Backos M, Rai R, Thomas E, Murphy M, Dore C and Regan L (1999) Bone density changes in pregnant women treated with heparin: A prospective, longitudinal study. Hum Reprod 14,2876-2880.
4. Bellver J, Rossal LP, Bosch E, Zuniga A, Corona JT, Melendez F, Gomez E, Simon C, Remohi J and Pellicer A (2003) Obesity and the risk of spontaneous abortion after oocyte donation. Fertil Steril 79,1136-1140.
5. Berry CW, Bramabati B, Eskes TKAB, Exalto N, Fox H, Geraedts JPM, Gerhard I, Gomes GF, Grudzinskas JG, Hustine J et al. (1995) The Euro-Team Early Pregnancy (ETEP) protocol for recurrent miscarriage. Hum Reprod 10,1516-1520.
6. Braekeleer de M and Dao TN (1990) Cytogenetic studies in couples experiencing repeated pregnancy losses. Hum Reprod 5,519-528.
7. Bricker L and Farquharson RG (2002) Types of pregnancy loss in recurrent miscarriage: Implications for research and clinical practice. Hum Reprod 17,1345-1350.
8. Briggs S (1998) Drugs in Pregnancy and Lactation: A Reference Guide to Fetal and Neonatal Risk, 5th edn. Williams and Wilkins, Baltimore, MD, pp. 73-81.
9. Brigham SA, Conlon C and Farquharson RG (1999) A longitudinal study of pregnancy outcome following idiopathic recurrent miscarriage. Hum Reprod 14,2868-2871.
10. Carlin AJ, Farquharson RG, Quenby SM, Topping J and Fraser WD (2004) Prospective observational study of bone mineral density during pregnancy: Low molecular weight versus control. Hum Reprod 19,1211-1214.
11. Carmichael SL, Shaw GM, Laurent C, Croughan MS, Olney RS and Lammer EJ (2005) Maternal progestin intake and risk of hypospadias. Arch Pediatr Adolesc Med 159,957-962.
12. Carp H, Toder V, Aviram A, Daniely M, Mashiach S and Barkai G (2001) Karyotype of the abortus in recurrent miscarriage. Fertil Steril 75,678-682.
13. Carp H, Dolizky M, Tur-Kaspa I and Inbal A (2002) Heriditary thrombophilias are not associated with a decreased live birth rate in women with recurrent miscarriage. Fertil Steril 78,58-62.
14. Carrington B, Sacks G and Regan L (2005) Recurrent miscarriage: pathophysiology and outcome. Curr Opin Obstet Gynecol 17,591-597.
15. Christiansen OB and Nielsen HS (2005) Intravenous immunoglobulin in the prevention of recurrent miscarriage: Does it work? Chem Immunol Allergy 88,117-127.
16. Christiansen OB, Nielsen HS and Pedersen B (2004) Active or passive immunization in unexplained recurrent miscarriage. J Reprod Immunol 62,41-51.
17. Christiansen OB, Andersen AMN, Bosch E, Daya S, Delves PJ, Hviid TV, Kutteh WH, Laird SM, Li TC and van der Ven K (2005) Evidenced-based investigations and treatments of recurrent pregnancy loss. Fertil Steril 83,821-839.
18. Clark AM, Thornley B, Tomlinson L, Gattetley C and Norman RJ (1998) Weight loss in obese infertile women results in improvement in reproductive outcome for all forms of fertility treatment. Hum Reprod 13,1502-1505.
19. Claudepierre P, Deprez X, Goupille P, Hilliquim P, Pham T, Puechal X, Scaeverbeke T and Sibilia J (2005) Anti-TNF alpha therapy and safety monitoring: Clinical tool guide. Joint Bone Spine 72,S1-S5.
20. Clifford K, Rai R and Regan L (1997) Future pregnancy outcome in unexplained recurrent first trimester miscarriage. Hum Reprod 12,387-389.
21. Dawood F, Farquharson R, Quenby S and Toh CH (2003) Acquired activated protein C resistance may be a risk factor for recurrent fetal loss. Fertil Steril 80,649-650.
22. Deruelle P, Denervaud M, Hachulla E, Ducloy AS, Valat AS, Puech F, Trillot N, Hatron PY and Subti D (2005) Use of low-molecular-weight heparin from the first trimester of pregnancy: A retrospective study of 111 consecutive pregnancies. Eur J Obstet Gynecol Reprod Biol [October 19, Epub ahead of print].
23. Di Nisio M, Peters LW and Middeldorp S (2005) Anticoagulants for the treatment of recurrent pregnancy loss in women without antiphospholipid syndrome. Cochrane Database Syst Rev 2,CD004734.
24. Doss BJ, Greene MF, Hill J, Heffner LJ, Bieber FR and Genest DR (1995) Massive chronic intervillositis associated with recurrent abortions. Hum Pathol 26,1245-1251.
25. van Dunne FM, Doggen CJ, Heemskerk M, Rosendaal FR and Helmerhorst FM (2005) Factor V Leiden mutation in relation to fecundity and miscarriage in women with venous thrombosis. Hum Reprod 20,802-806.
26. Empson M, Lassere M, Craig J and Scott J (2002) Recurrent pregnancy loss with antiphospholipid antibody: A systematic review of therapeutic trials. Obstet Gynecol 99,135-144.
27. Empson M, Lassere M, Craig J and Scott J (2005) Prevention of recurrent miscarriage for women with antiphospholipid antibody or lupus anticoagulant. Cochrane Database Syst Rev 2,CD002859.
28. Farquharson RG, Quenby S and Greaves M (2002) Antiphospholipid syndrome in pregnancy: A randomized, controlled trial of treatment. Obstet Gynecol 100,408-413.
29. Fedorcsak P, Dale PO, Storeng R, Tanbo T and Abyholm T (2001) The impact of obesity and insulin resistance on the outcome of IVF or ICSI in women with polycystic ovarian syndrome. Hum Reprod 16,1086-1091.
30. Fox H (1993) Histological classification of tissue from spontaneous abortions: A valueless exercise? Histopathol 22,599-600.
31. Franssen MTM, Korevaar JC, Leschot NJ, Bossuyt PMM, Knegt AC, Gerssen-Schoorl KBJ, Wouters CH, Hansson KBM, Hochstenbach R, Madan K et al. (2005) Selective chromosome analysis in couples with two or more miscarriages: Case-control study. BMJ 331,137-139.
32. Gardella JR and Hill JA (2000) Environmental toxins associated with recurrent pregnancy loss. Semin Reprod Med 18,407-424.
33. George L, Mills JL, Johansson AL, Nordmark A, Olander B, Granath F and Cnattingius S (2002) Plasma folate levels and risk of spontaneous abortion. JAMA 288,1867-1873.
34. Greer IA and Nelson-Piercy C (2005) Low-molecular-weight heparins for thromboprophylaxis and treatment of venous thromboembolism in pregnancy: a systematic review of safety and efficacy. Blood 106,401-407.
35. Hakvoort RA, Lisman BA, Boer K, Bleker OP, van Groningen K, van Wely M and Exalto N (2006) Histological classification of chorionic villous vascularization in early pregnancy. Hum Reprod 21,1291-1294.
36. Hawkins D and Evans J (2005) Minimising the risk of heparin-induced osteoporosis during pregnancy. Expert Opin Drug Saf 4,583-590.
37. Holmberg-Marttila D, Sievanen H, Laippala P and Tuimala R (2000) Factors underlying changes in bone mineral during postpartum amenorrhea and lactation. Osteoporos Int 11,570-576.
38. Hustin J, Kadri R and Jauniaux E (1996) Spontaneous and habitual abortion: A pathologist's point of view. Early Pregnancy 2,85-95.
39. Jauniaux E, Kadri R and Hustin J (1996) Partial mole and triploidy: screening patients with first-trimester spontaneous abortion. Obstet Gynecol 88,616-619.
40. Jivraj S, Rai R, Underwood J and Regan L (2006) Genetic thrombophilic mutations among couples with recurrent miscarriage. Hum Reprod 21,1161-1165.
41. Kilpatrick DC, Bevan BH and Liston WA (1995) Association between mannan-binding-lectin protein deficiency and recurrent miscarriage. Hum Reprod 10,2501-2505.
42. Kozer E, Nikfar S, Costei A, Boskovic R, Nulman I and Koren G (2002) Aspirin consumption during the first trimester of pregnancy and congenital anomalies: A meta-analysis. Am J Obstet Gynecol 187,1623-1630.
43. Kruse C, Rosgaard A, Steffensen R, Varming K, Jensenius JC and Christiansen OB (2002) Low serum level of mannan-binding lectin is a determinant for pregnancy outcome in women with recurrent spontaneous abortion. Am J Obstet Gynecol 187,1313-1320.
44. Laird SM, Tukerman EM, Cork BA, Linjawi S, Blakemore AIF and Li TC (2003) A review of immune cells and molecules in women with recurrent miscarriage. Hum Reprod Update 9,163-174.
45. Lashen H, Fear K and Sturdee DW (2004) Obesity is associated with increased risk of first trimester and recurrent miscarriage: Matched case-control study. Hum Reprod 19,1644-1646.
46. Li DK, Liu L and Odouli R (2003) Exposure to non-steroidal anti-inflammatory drugs during pregnancy and risk of miscarriage: population based cohort study. BMJ 327,368.
47. Li TC, Makris M, Tomsu M, Tuckerman E and Laird S (2002) Recurrent miscarriage: Aetiology, management and prognosis. Hum Reprod Update 8,463-481.
48. Makris M (2000) Hyperhomocysteinemia and thrombosis. Clin Lab Haematol 22,133-143.
49. Moffett A, Regan L and Braude P (2004) Natural killer cells, miscarriage, and infertility. BMJ 329,1283-1285.
50. Morikawa M, Yamada H, Kato EH, Shimada S, Yamada T and Minakami H (2004) Embryo loss pattern is predominant in miscarriages with normal chromosome karyotype among women with repeated miscarriage. Hum Reprod 19,2644-2647.
51. Nelen WLDM, Blom HK, Steegers EAP, den Heijer M and Eskes TKAB (2000) Hyperhomocysteinemia and recurrent early pregnancy loss: A metaanalysis. Fertil Steril 74,1196-1199.
52. Nielsen GL, Sorensen HT, Larsen H and Pedersen L (2001) Risk of adverse birth outcome and miscarriage in pregnant users of non-steroidal anti-inflammatory drugs: Population based observational study and case-control study. BMJ 322,266-270.
53. Oates-Whitehead RM, Hass DM and Carrier JAK (2005) Progestogen for preventing miscarriage. Cochrane Database Syst Rev 4,CD003511.
54. Ogasawara M, Aoki K, Okada S and Suzumori K (2000) Embryonic karyotype of abortuses in relation to the number of previous miscarriages. Fertil Steril 73,300-304.
55. Pettila V, Leinonen P, Markkola A, Hiilesmaa V and Kaaja R (2002) Postpartum bone mineral density in women treated for thromboprophylaxis with unfractionated heparin or LMW heparin. Thromb Haemost 87,182-186.
56. Porter T, Lacoursiere Y and Scott Jr (2006) Immunotherapy for recurrent miscarriage. Cochrane Database Syst Rev 19,CD000112.
57. Quenby S, Vince G, Farquarson R and Aplin J (2002) Recurrent miscarriage: A defect in nature's quality control? Hum Reprod 17,1959-1963.
58. Quenby S, Kalumbi C, Bates M, Farquharson R and Vince G (2005) Prednisolone reduces preconceptual natural killer cells in women with recurrent miscarriage. Fertil Steril 84,980-984.
59. Rai R, Sacks G and Trew G (2005) Natural killer cells and reproductive failure, practice and prejudice. Hum Reprod 20,1123-1126.
60. Redline RW, Zaragoza M and Hassold T (1999) Prevalence of developmental and inflammatory lesions in nonmolar first-trimester spontaneous abortions. Hum Pathol 30,93-100.
61. Rey E, Kahn SR, David M and Shrier I (2003) Thrombophilic disorders and fetal loss: A meta-analysis. Lancet 361,901-908.
62. Robertson L, Wu O, Langhorne P, Twaddle S, Clark P, Lowe GDO, Walker ID, Greaves M, Brenkel I, Regan L et al. (2006) Thrombophilia in pregnancy: a systematic review. Br J Haematol 132,171-196.
63. Roque H, Paidas MJ, Funai EF, Kuczynski E and Lockwood CJ (2004) Maternal thrombophilias are not associated with early pregnancy loss. Thromb Haemost 91,290-295.
64. Royal College of Obstetricians and Gynaecologists (RCOG) (1998) Guideline 17: The Management of Recurrent Miscarriage. RCOG Press, London.
65. Rumbold A, Middleton P and Crowther CA (2005) Vitamin supplementation for preventing miscarriage. Cochrane Database Syst Rev 2,CD004073.
66. Salim R, Woelfer B, Backos M, Regan L and Jurkovic D (2003a) Reproducibility of three-dimension ultrasound diagnosis of congenital uterine anomalies. Ultrasound Obstet Gynecol 21,578-582.
67. Salim R, Regan L, Woelfer B, Backos M and Jurkovic D (2003b) A comparative study of the morphology of congenital uterine anomalies in women with and without a history of recurrent first trimester miscarriage. Hum Reprod 28,162-166.
68. Sapir T, Blank M and Shoenfeld Y (2005) Immunomodulatory effects of intravenous immunoglobulins as a treatment for autoimmune diseases, cancer, and recurrent pregnancy loss. Ann N Y Acad Sci 1051,743-778.
69. Scott JR (2003) Immunotherapy for recurrent miscarriage. Cochrane Database Syst Rev 1,CD000112.
70. Simpson JL, Mills JL, Lee J, Holmes JB, Kim H, Metzger B, Knopp R, Jovanovic-Peterson L, Aarons J and Conley M (1996) Infectious processes: an infrequent cause of first trimester spontaneous abortions. Hum Reprod 11,668-672.
71. Slone D, Siskind V, Heinonen OP, Monson RR, Kaufman DW and Shapiro S (1976) Aspirin and congenital malformations. Lancet 26,1373-1375.
72. Stephenson MD, Awartini KA and Robinson WP (2002) Cytogenetic analysis of miscarriages from couples with recurring miscarriage: A case-control study. Hum Reprod 17,446-451.
73. Stirrat GM (1990) Recurrent miscarriage: Definition and epidemiology. Lancet 336,673-675.
74. Stray-Pedersen B and Stray-Pedersen S (1984) Etiological factors and subsequent reproductive performance in 195 couples with a prior history of habitual abortion. Am J Obstet Gynecol 148,140-146.
75. Thum MY, Bhaskaran S, Bansal AS, Shehata H, Ford B, Sunar N and Abdalla HI (2005) Simple enumeration of peripheral blood natural killer (CD56+NK) cells, B cells and T cells have no predictive value in IVF treatment outcome. Hum Reprod 20,1272-1276.
76. Warburton D, Kline J, Stein Z, Hutzler M, Chin A and Hassold T (1987) Does the karyotype of a spontaneous abortion predict the karyotype of a subsequent abortion? Evidence from 273 women with two karyotyped spontaneous abortions. Am J Hum Genet 41,465-483.
77. Werler MM, Sheehan JE and Mitchell AA (2002) Maternal medication use and risks of gastroschisis and small intestinal atresia. Am J Epidemiol 155,26-31.
78. Wilson WA, Gharavi AE, Koike T, Lockshin MD, Branch DW, Piette JC, Brey R, Derksen R, Harris EN, Hughes GR et al. (1999) International consensus statement on preliminary classification criteria for definite antiphospholipid syndrome: Report of an international workshop. Arthritis Rheum 42,1309-1311.
79. Woelfer B, Salim R, Banerjee S, Elson J, Regan L and Jurkovic D (2001) Reproductive outcome in women with congenital uterine anomalies detected by of three-dimension ultrasound screening. Obstet Gynecol 98,1099-1103.
80. Wold AS and Arici A (2005) Natural killer cells and reproductive failure. Curr Opin Obstet Gynecol 17,237-241.