1,013
Views
3
CrossRef citations to date
0
Altmetric
Review

Early Pregnancy Losses: Review of Nomenclature, Histopathology, and Possible Etiologies

ORCID Icon, , , &
Pages 191-209 | Received 12 Dec 2017, Accepted 05 Mar 2018, Published online: 08 May 2018

References

  • Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy. N Eng J Med. 2001;345(19):1400–8. doi:10.1056/NEJMra000763.
  • Jauniaux E, Burton GJ. Pathophysiology of histological changes in early pregnancy loss. Placenta. 2005;26:1142–3. doi:10.1016/j.placenta.2004.05.011.
  • Pandya P, Snijders RJM, Psara N, Hibert L, Nicolaides KH. The prevalence of non-viable pregnancy at 101–3 weeks of gestation. Ultrasound Obstet Gynecol. 1996;7:1703. doi:10.1046/j.1469-0705.1996.07030170.x.
  • Casikar I, Reid S, Rippey J, Condous G. Redefining first trimester miscarriage. Aust N Z J Obstet Gynaecol. 2012 Dec;52(6):5978. doi:10.1111/ajo.12022.
  • Jurkovic D, Overton C, Bender-Atik R. Diagnosis and management of first trimester miscarriage. BMJ. 2013 Jun;19;346:f3676. doi:10.1136/bmj.f3676.
  • De Braekeleer M, Dao TN. Cytogenetic studies in couples experiencing repeated pregnancy losses. Hum Reprod. 1990;5:519–28. doi:10.1093/oxfordjournals.humrep.a137135. PMID:2203803.
  • ACOG practice bulletin: management of recurrent early pregnancy loss. No. 24. Washington, DC: American College of Obstetricians and Gynecologists; 2001.
  • Goddijn M, Leschot NJ. Genetic aspects of miscarriage. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14(5):855–65. Review. doi:10.1053/beog.2000.0124. PMID:11023805.
  • Jenderny J. Chromosome aberrations in a large series of spontaneous miscarriages in the German population and review of the literature. Mol Cytogenet. 2014;5(7):38. doi:10.1186/1755-8166-7-38.
  • Massalska D, Zimowski JG, Bijok J, Pawelec M, Czubak-Barlik M, Jakiel G, Roszkowski T. First trimester pregnancy loss: clinical implications of genetic testing. J Obstet Gynaecol Res. 2017;43(1):23–29. doi:10.1111/jog.13179. PMID:27928862.
  • Sahoo T, Dzidic N, Strecker MN, Commander S, Travis MK, Doherty C, Hovanes K. Comprehensive genetic analysis of pregnancy loss by chromosomal microarrays: outcomes, benefits, and challenges. Genet Med. 2017;19(1):83–89. doi:10.1038/gim.2016.69. PMID:27337029.
  • Roszkowski T. First trimester pregnancy loss: clinical implications of genetic testing. J Obstet Gynaecol Res. 2017;43(1):23–29. doi:10.1111/jog.13179. PMID:27928862.
  • Stephenson MD, Awartani KA, Robinson WP. Cytogenetic analysis of miscarriages from couples with recurrent miscarriage: a case-control study. Hum Reprod. 2002 Feb;17(2):446–51. doi:10.1093/humrep/17.2.446.
  • Zloposa G, Skrablin S, Kalafatic D, Banovic V, Lesin J. Uterine anomalies and pregnancy outcome following resectoscope metroplasty. Int J Gynecol Obstet. 2007;98:1291.
  • Larsen EC, Christiansen OB, Kolte AM, Macklon N. New insights into mechanisms behind miscarriage. BMC Med. 2013;11(1):154. doi:10.1186/1741-7015-11-154. PMID:23803387.
  • García-Enguídanos A, Calle ME, Valero J, Luna S, Domínguez-Rojas V. Risk factors in miscarriage: a review. Eur J Obstet Gynecol Reprod Biol. 2002;102(2):111–19. doi:10.1016/S0301-2115(01)00613-3. PMID:11950476.
  • Lathi RB, Gray Hazard FK, Heerema-McKenney A, Taylor J, Chueh JT. First trimester miscarriage evaluation. Semin Reprod Med. 2011;29(6):463–9. doi:10.1055/s-0031-1293200. PMID:22161459.
  • Sierra S, Stephenson M. Genetics of recurrent pregnancy loss. Semin Reprod Med. 2006 Feb;24(1):172–4. Review. doi:10.1055/s-2006-931797.
  • Doubilet PM, Benson CB, Bourne T, Blaivas M. Diagnostic criteria for nonviable pregnancy early in the first trimester. Ultrasound Q. 2014;30(1):39. doi:10.1097/RUQ.0000000000000060.
  • Genest DR, Roberts D, Boyd T, Bieber FR. Fetoplacental histology as a predictor of karyotype: a controlled study of spontaneous first trimester abortions. Hum Pathol. 1995;26(2):2019. doi:10.1016/0046-8177(95)90038-1.
  • Jauniaux E, Johns J, Burton GJ. The role of ultrasound imaging in diagnosing and investigating early pregnancy failure. Ultrasound Obstet Gynecol. 2005;25(6):613–24. doi:10.1002/uog.1892. PMID:15861413.
  • Jeve Y, Rana R, Bhide A, Thangaratinam S. Accuracy of first-trimester ultrasound in the diagnosis of early embryonic demise: a systematic review. Ultrasound Obstet Gynecol. 2011;38(5):489–96. doi:10.1002/uog.10108. PMID:21997875.
  • Papaioannou GI, Syngelaki A, Maiz N, Ross JA, Nicolaides KH. Ultrasonographic prediction of early miscarriage. Hum Reprod. 2011;26(7):1685–92. doi:10.1093/humrep/der130. PMID:21531997.
  • Royal College of Obstetricians and Gynaecologists. Management of early pregnancy loss. London: RCOG Press; c2006.
  • Sebire NJ, Sepulveda W. Correlation of placental pathology with prenatal ultrasound findings. J Clin Pathol. 2008;61(12):1276–84. doi:10.1136/jcp.2008.055251. PMID:18682416.
  • Barnhart KT, Benacerraf BR, Brown DL, Filly RA, Fox JC, Goldstein SR, Kendall JL, Lyons EA, Porter MB, Pretorius DH, Timor-Tritsch IE. Diagnostic criteria for nonviable pregnancy early in the first trimester. N Engl J Med. 2013;369(15):1443–51. doi:10.1056/NEJMra1302417. PMID:24106937.
  • Farquharson RG, Jauniaux E, Exalto N. Updated and revised nomenclature for description of early pregnancy events. Hum Reprod. 2005;20(11):3008–11. doi:10.1093/humrep/dei167. PMID:16006453.
  • Silver RM, Branch DW, Goldenberg R, Iams JD, Klebanoff MA. Nomenclature for pregnancy outcomes: time for a change. Obstet Gynecol. 2011;118(6):14028. doi:10.1097/AOG.0b013e3182392977.
  • Houwert–De Jong MH, Bruinse HW, Eskes TKAB, Mantingh A, Termijklen A, Kooyman CD. Early recurrent miscarriage: histology of conception products. Br J Obstet Gynaecol. 1990;97:5335.
  • Kohut KG, Anthony MN, Salafia CM. Decidual and placental histologic findings in patients experiencing spontaneous abortions in relation to pregnancy order. Am J Reprod Immunol. 1997 Mar;37(3):257–61. doi:10.1111/j.1600-0897.1997.tb00224.x.
  • Novak RW, Malone JM, Robinson HB. The role of the pathologist in the evaluation of first trimester abortions. Pathol Annu. 1990;25:297–311. PMID:2404247.
  • Ernst LM, Gawron L, Fritsch MK. Pathologic examination of fetal and placental tissue obtained by dilation and evacuation. Arch Pathol Lab Med. 2013;137(3):326–37. doi:10.5858/arpa.2012-0090-RA. PMID:23451744.
  • Hardy K, Hardy PJ. 1st trimester miscarriage: four decades of study. Transl Pediatr. 2015;4(2):189–200. PMID:26835373.
  • Hustin J, Jauniaux E, Schaaps JP. Histological study of the materno-embryonic interface in spontaneous abortion. Placenta. 1990;11(6):477–86. doi:10.1016/S0143-4004(05)80193-6. PMID:2290799.
  • Jindal P, Regan L, Fourkala EO, Rai R, Moore G, Goldin RD, Sebire NJ. Placental pathology of recurrent spontaneous abortion: the role of histopathological examination of products of conception in routine clinical practice: a mini review. Hum Reprod. 2007;22(2):313–16. doi:10.1093/humrep/del128. PMID:17008326.
  • Redline RW, Hassold T, Zaragoza M. Determinants of villous trophoblastic hyperplasia in spontaneous abortions. Mod Pathol. 1998;11(8):762–8. PMID:9720505.
  • Lapinsky SE. Obstetric infections. Crit Care Clin. 2013 Jul;29(3):509–20. doi:10.1016/j.ccc.2013.03.006.
  • Szulman AE. Examination of the early conceptus. Arch Pathol Lab Med. 1991;115:696–700. PMID:2064529.
  • Branch DW, Gibson M, Silver R. Recurrent miscarriage. New Engl J Med. 2010;363(18):1740–7. doi:10.1056/NEJMcp1005330. PMID:20979474.
  • Conway DA, Patel SS, Liem J, Fan KJ, Jalian R, Williams J, Pisarska MD. The risk of cytogenetic abnormalities in the late first trimester of pregnancies conceived through assisted reproduction. Fertil Steril. 2011;95(2):503–6. doi:10.1016/j.fertnstert.2010.09.019. PMID:20947075.
  • Dukhovny S, Zutshi P, Abbott JF. Recurrent second trimester pregnancy loss: evaluation and management. Curr Opin Endocrinol Diabetes Obesity. 2009;16(6):451–8. doi:10.1097/MED.0b013e328332b808.
  • Filges I, Friedman JM. Exome sequencing for gene discovery in lethal fetal disorders—harnessing the value of extreme phenotypes. Prenatal Diag. 2015;35(10):1005–9. doi:10.1002/pd.4464. PMID:25046514.
  • Lathi RB, Mark SD, Westphal LM, Milki AA. Cytogenetic testing of anembryonic pregnancies compared to embryonic missed abortions. J Assisted Reprod Genet. 2007;24(11):521–4. doi:10.1007/s10815-007-9166-1.
  • Greenwold N, Jauniaux E. Collection of villous tissue under ultrasound guidance to improve the cytogenetic study of early pregnancy failure. Hum Reprod. 2002;17:4526. doi:10.1093/humrep/17.2.452.
  • Levy B, Sigurjonsson S, Pettersen B, Maisenbacher MK, Hall MP, Demko Z, Lathi RB, Tao R, Aggarwal V, Rabinowitz M. Genomic imbalance in products of conception: single-nucleotide polymorphism chromosomal microarray analysis. Obstet Gynecol. 2014;124(2 Pt 1):2029.
  • Wohlfahrt J, Andersen AM, Melbye M. Interval between pregnancies and risk of spontaneous abortion. Epidemiology. 2000;11(1):923. doi:10.1097/00001648-200001000-00021.
  • van den Berg MM, van Maarle MC, van Wely M, Goddijn M. Genetics of early miscarriage. Biochim Biophys Acta. 2012;1822(12):19519.
  • Carr DH. Cytogenetics and the pathologist. Pathol Ann. 1975;10:931–44.
  • Grinschgl I, Mannweiler S, Holzapfel-Bauer M, Pferschy U, Hoefler G, Guertl B. The role of morphology in combination with ploidy analysis in characterizing early gestational abortion. Virchow's Arch. 2013;462(2):1758–62.
  • Kalousek DK, Vekemans M. Confined placental mosaicism. J Med Genet. 1996;33:5295–333. [Review] doi:10.1136/jmg.33.7.529.
  • Hui P, Martel M, Parkash V. Gestational trophoblastic diseases: recent advances in histopathologic diagnosis and related genetic aspects. Adv Anat Pathol. 2005;12:116–25. doi:10.1097/01.pap.0000163960.11107.73. PMID:15900112.
  • Lurain JR. Gestational trophoblastic disease I: epidemiology, pathology, clinical presentation and diagnosis of gestational trophoblastic disease, and management of hydatidiform mole. Am J Obstet Gynecol. 2010;203(6):5319. doi:10.1016/j.ajog.2010.06.073.
  • Hoffner L, Surti U. The genetics of gestational trophoblastic disease: a rare complication of pregnancy. Cancer Genet. 2012;205(3):63–77. doi:10.1016/j.cancergen.2012.01.004. PMID:22469506.
  • Horn LC, Kowalzik J, Bilek K, Richter CE, Einenkel J. Clinicopathologic characteristics and subsequent pregnancy outcome in complete hydatidiform moles. Eur J Obstet Gynecol Reprod Biol. 2006;128:101–4. doi:10.1016/j.ejogrb.2006.01.024.
  • Nguyen NM, Slim R. Genetics and epigenetics of recurrent hydatidiform moles: basic science and genetic counselling. Curr Obstet Gynecol Rep. 2014;3:55–64. doi:10.1007/s13669-013-0076-1. PMID:24533231.
  • Golubovsky MD. Postzygotic diploidization of triploids as a source of unusual cases of mosaicism, chimerism and twinning. Hum Reprod. 2003;18:236e242. doi:10.1093/humrep/deg060.
  • Dekel N, Gnainsky Y, Granot I, Mor G. Inflammation and implantation. Am J Reprod Immunol. 2009;63(1):17–21. doi:10.1111/j.1600-0897.2009.00792.x.
  • Spinillo A, Iacobone AD, Calvino IG, Alberi I, Gardella B. The role of the placenta in feto-neonatal infections. Early Hum Dev. 2014;90(Suppl 1):S79.
  • Syridou G, Spanakis N, Konstantinidou A, Piperaki E, Kafetzis D, Patsouris E, Tsakris A. Detection of cytomegalovirus, parvovirus B19 and herpes simplex viruses in cases of intrauterine fetal death: association with pathological findings. J Med Virol. 2008;80(10):1776–82. doi:10.1002/jmv.21293. PMID:18712818.
  • Guarner J, Southwick K, Greer P, Bartlett J, Fears M, Santander A, Zaki S. Testing umbilical cords for funisitis due to Treponema pallidum infection, Bolivia. Emerg Infect Dis. 2000;6(5):487–92. doi:10.3201/eid0605.000507. PMID:10998379.
  • Lee K, Kim YW, Shim J-Y, Won H-S, Lee PR, Kim A, Kim CJ. Distinct patterns of C4d immunoreactivity in placentas with villitis of unknown etiology, cytomegalovirus placentitis, and infarct. Placenta. 2013;34(5):432–5. doi:10.1016/j.placenta.2013.02.003. PMID:23481222.
  • Zhou Y, Bian G, Zhou Q, Gao Z, Liao P, Liu Y, He M. Detection of cytomegalovirus, human parvovirus B19, and herpes simplex virus-1/2 in women with first-trimester spontaneous abortions. J Med Virol. 2015;87:1749–53. doi:10.1002/jmv.24218. PMID:25976377.
  • Nuovo GJ, Cooper LD, Bartholomew D. Histologic, infectious, and molecular correlates of idiopathic spontaneous abortion and perinatal mortality. Diag Mol Pathol. 2005;14(3):152–8. doi:10.1097/01.pas.0000176769.18423.37.
  • Craven CM, Chedwick LR, Ward K. Placental basal plate formation is associated with fibrin deposition in decidual veins at sites of trophoblast cell invasion. Am J Obstet Gynecol. 2002;186(2):291–6. doi:10.1067/mob.2002.119717. PMID:11854653.
  • Zhou Y, Genbacev O, Damsky CH, Fisher SJ. Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J Reprod Immunol. 1998;39(1–2):197–213. doi:10.1016/S0165-0378(98)00022-9. PMID:9786462.
  • Boyd TK, Redline RW. Chronic histiocytic intervillositis: a placental lesion associated with recurrent reproductive loss. Hum Pathol. 2000;31(11):1389–96. doi:10.1016/S0046-8177(00)80009-X. PMID:11112214.
  • Avagliano L, Bulfamante GP, Morabito A, Marconi AM. Abnormal spiral artery remodelling in the decidual segment during pregnancy: from histology to clinical correlation. J Clin Pathol. 2011;64(12):1064–8. doi:10.1136/jclinpath-2011-200092. PMID:21836040.
  • Brosens JJ, Pijnenborg R, Brosens IA. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies. Am J Obstet Gynecol. 2002;187(5):1416–23. doi:10.1067/mob.2002.127305. PMID:12439541.
  • Cartwright JE, Fraser R, Leslie K, Wallace AE, James JL. Remodelling at the maternal–fetal interface: relevance to human pregnancy disorders. Reproduction. 2010;140(6):803–13. doi:10.1530/REP-10-0294. PMID:20837731.
  • Charnock-Jones DS, Burton GJ. Placental vascular morphogenesis. Baillières Best Pract Res Clin Obstet Gynaecol. 2000;14(6):953–68. doi:10.1053/beog.2000.0137. PMID:11141343.
  • Lyall F. Priming and remodelling of human placental bed spiral arteries during pregnancy—a review. Placenta. 2005;26:S31–6. doi:10.1016/j.placenta.2005.02.010. PMID:15837064.
  • Musizzano Y, Fulcheri E. Decidual vascular patterns in first-trimester abortions. Virchows Archiv. 2010;456(5):543–60. doi:10.1007/s00428-010-0883-y. PMID:20157826.
  • Chan YY, Jayaprakasan K, Tan A, Thornton JG, Coomarasamy A, Raine-Fenning NJ. Reproductive outcomes in women with congenital uterine anomalies: a systematic review. Ultrasound Obstet Gynecol. 2011;38(4):371–82. doi:10.1002/uog.10056. PMID:21830244.
  • Jaslow CR. Uterine factors. Obstet Gynecol Clin North Am. 2014;41(1):57–86. doi:10.1016/j.ogc.2013.10.002. PMID:24491984.
  • Twig G, Shina A, Amital H, Shoenfeld Y. Pathogenesis of infertility and recurrent pregnancy loss in thyroid autoimmunity. J Autoimmune. 2012;38:J275–81. doi:10.1016/j.jaut.2011.11.014.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.