Pathologic findings of the placenta and clinical implications – recommendations for placental examination (original) (raw)
Review article: Medical guidelines
- Elisabeth Bruder+−
- Irene Hösli+−
- Olav Lapaire+−
- Luigi Raio+−
- Henning Schneider+−
- Sylvia Höller+−
- Roland Hentschel+−
- Simone Brandt+−
- Peter Bode+−
- Sven Schultzke+−
- Gero Drack+−
Summary
The placenta is a unique and complex organ that combines the circulatory systems of two or more individuals within a single dynamic organ with a set, short lifespan. A diverse spectrum of disorders, including infections as well as metabolic, genetic, circulatory, and maturation defects, may affect its function. Pathology investigation of the placenta is key for identifying several pathogenic processes in both the mother and the foetus. Aberrant placentation, maternal and foetal vascular compromise, infection, inflammatory immunologic conditions, and disorders of maturation are elements of newly proposed classification schemes.
The clinical impact of placental examination consists of diagnosing maternal and foetal disease, identifying the potential for recurrence, correlating clinical pathological findings with distinct morphologic features, and identifying the aetiology responsible for growth restriction or foetal death.
Gestational trophoblastic disease occurs more frequently in the first trimester; however, in very rare cases, it can affect the term or third-trimester placenta.
The application of reproducible nomenclature is expected to facilitate progress in the diagnosis and treatment of obstetric and foetal disorders with placental manifestation.
Therefore, this review aims to facilitate communication between obstetricians, neonatologists, and pathologists involved in this diagnostic process.
References
- Langston C, Kaplan C, Macpherson T, Manci E, Peevy K, Clark B, et al. Practice guideline for examination of the placenta: developed by the Placental Pathology Practice Guideline Development Task Force of the College of American Pathologists. Arch Pathol Lab Med. 1997 May;121(5):449–76.
- Roberts DJ, Baergen RN, Boyd TK, Carreon CK, Duncan VE, Ernst LM, et al. Criteria for placental examination for obstetrical and neonatal providers. Am J Obstet Gynecol. 2023 May;228(5):497–508.e4. doi: https://doi.org/10.1016/j.ajog.2022.12.017DOI: https://doi.org/10.1016/j.ajog.2022.12.017
- S2k-Leitlinie Pathomorphologische Untersuchung der Plazenta. 2022. AWMF Registriernummer 035/005. available from: https://register.awmf.org/de/leitlinien/detail/035-005
- Evans, C., et al., Tissue pathway for histological examination of the placenta. The Royal college of pathologists. G 108, 2022.
- Polnaszek BE, Clark SL, Rouse DJ. Pathologic Assessment of the Placenta: Evidence Compared With Tradition. Obstet Gynecol. 2022 Apr;139(4):660–7. doi: https://doi.org/10.1097/AOG.0000000000004719DOI: https://doi.org/10.1097/AOG.0000000000004719
- Khong TY, Mooney EE, Ariel I, Balmus NC, Boyd TK, Brundler MA, et al. Sampling and Definitions of Placental Lesions: Amsterdam Placental Workshop Group Consensus Statement. Arch Pathol Lab Med. 2016 Jul;140(7):698–713. doi: https://doi.org/10.5858/arpa.2015-0225-CCDOI: https://doi.org/10.5858/arpa.2015-0225-CC
- Slack JC, Parra-Herran C. Life After Amsterdam: Placental Pathology Consensus Recommendations and Beyond. Surg Pathol Clin. 2022 Jun;15(2):175–96. doi: https://doi.org/10.1016/j.path.2022.02.001DOI: https://doi.org/10.1016/j.path.2022.02.001
- Zhou YY, Ravishankar S, Luo G, Redline RW. Predictors of High Grade and Other Clinically Significant Placental Findings by Indication for Submission in Singleton Placentas From Term Births. Pediatr Dev Pathol. 2020 Aug;23(4):274–84. doi: https://doi.org/10.1177/1093526620904801DOI: https://doi.org/10.1177/1093526620904801
- Guttmacher AE, Maddox YT, Spong CY. The Human Placenta Project: placental structure, development, and function in real time. Placenta. 2014 May;35(5):303–4. doi: https://doi.org/10.1016/j.placenta.2014.02.012DOI: https://doi.org/10.1016/j.placenta.2014.02.012
- Roberts JM, Hansson SR, Vaiman D, Redman CW; Global Pregnancy Collaboration. Global Pregnancy Collaboration symposium on placental health: summary and recommendations. Placenta. 2017 Apr;52:116–21. doi: https://doi.org/10.1016/j.placenta.2017.01.115DOI: https://doi.org/10.1016/j.placenta.2017.01.115
- Odibo I, Gehlot A, Ounpraseuth ST, Magann EF. Pathologic examination of the placenta and its clinical utility: a survey of obstetrics and gynecology providers. J Matern Fetal Neonatal Med. 2016;29(2):197–201. doi: https://doi.org/10.3109/14767058.2014.998192DOI: https://doi.org/10.3109/14767058.2014.998192
- Sebire NJ. Implications of placental pathology for disease mechanisms; methods, issues and future approaches. Placenta. 2017 Apr;52:122–6. doi: https://doi.org/10.1016/j.placenta.2016.05.006DOI: https://doi.org/10.1016/j.placenta.2016.05.006
- Redline RW, Roberts DJ, Parast MM, Ernst LM, Morgan TK, Greene MF, et al. Placental pathology is necessary to understand common pregnancy complications and achieve an improved taxonomy of obstetrical disease. Am J Obstet Gynecol. 2023 Feb;228(2):187–202. doi: https://doi.org/10.1016/j.ajog.2022.08.010DOI: https://doi.org/10.1016/j.ajog.2022.08.010
- Redline RW. The clinical implications of placental diagnoses. Semin Perinatol. 2015 Feb;39(1):2–8. doi: https://doi.org/10.1053/j.semperi.2014.10.002DOI: https://doi.org/10.1053/j.semperi.2014.10.002
- Redline RW. Classification of placental lesions. Am J Obstet Gynecol. 2015 Oct;213(4 Suppl):S21–8. doi: https://doi.org/10.1016/j.ajog.2015.05.056DOI: https://doi.org/10.1016/j.ajog.2015.05.056
- Gabriel H, Korinth D, Ritthaler M, Schulte B, Battke F, von Kaisenberg C, et al. Trio exome sequencing is highly relevant in prenatal diagnostics. Prenat Diagn. 2022 Jun;42(7):845–51. doi: https://doi.org/10.1002/pd.6081DOI: https://doi.org/10.1002/pd.6081
- Redline RW. Placental pathology: is it time to get serious? Contemp Ob Gyn. 2014;59(2):41–8.
- Khong TY. Evidence-based pathology: umbilical cord coiling. Pathology. 2010 Dec;42(7):618–22. doi: https://doi.org/10.3109/00313025.2010.520309DOI: https://doi.org/10.3109/00313025.2010.520309
- Cromb D, et al. Clinical value of placental examination for paediatricians. Arch Dis Child Fetal Neonatal Ed. 2023. DOI: https://doi.org/10.1136/archdischild-2023-325674
- de Laat MW, Franx A, van Alderen ED, Nikkels PG, Visser GH. The umbilical coiling index, a review of the literature. J Matern Fetal Neonatal Med. 2005 Feb;17(2):93–100. doi: https://doi.org/10.1080/jmf.17.2.93.100DOI: https://doi.org/10.1080/14767050400028899
- Dirnhofer S, B.L., Lehr HA, Landau B, Zenklusen HR, Qualitätsrichtlinien SGPath. 2011.
- Avagliano L, Locatelli A, Danti L, Felis S, Mecacci F, Bulfamante GP. Placental histology in clinically unexpected severe fetal acidemia at term. Early Hum Dev. 2015 May;91(5):339–43. doi: https://doi.org/10.1016/j.earlhumdev.2015.03.004DOI: https://doi.org/10.1016/j.earlhumdev.2015.03.004
- Chen A, Roberts DJ. Placental pathologic lesions with a significant recurrence risk - what not to miss! APMIS. 2018 Jul;126(7):589–601. doi: https://doi.org/10.1111/apm.12796DOI: https://doi.org/10.1111/apm.12796
- Kaspar HG, Abu-Musa A, Hannoun A, Seoud M, Shammas M, Usta I, et al. The placenta in meconium staining: lesions and early neonatal outcome. Clin Exp Obstet Gynecol. 2000;27(1):63–6.
- Spong CY, Mercer BM, D’Alton M, Kilpatrick S, Blackwell S, Saade G. Timing of indicated late-preterm and early-term birth. Obstet Gynecol. 2011 Aug;118(2 Pt 1):323–33. doi: https://doi.org/10.1097/AOG.0b013e3182255999DOI: https://doi.org/10.1097/AOG.0b013e3182255999
- Abdulghani S, Moretti F, Gruslin A, Grynspan D. Recurrent Massive Perivillous Fibrin Deposition and Chronic Intervillositis Treated With Heparin and Intravenous Immunoglobulin: A Case Report. J Obstet Gynaecol Can. 2017 Aug;39(8):676–81. doi: https://doi.org/10.1016/j.jogc.2017.03.089DOI: https://doi.org/10.1016/j.jogc.2017.03.089
- Dubruc E, Lebreton F, Giannoli C, Rabilloud M, Huissoud C, Devouassoux-Shisheboran M, et al. Placental histological lesions in fetal and neonatal alloimmune thrombocytopenia: A retrospective cohort study of 21 cases. Placenta. 2016 Dec;48:104–9. doi: https://doi.org/10.1016/j.placenta.2016.10.009DOI: https://doi.org/10.1016/j.placenta.2016.10.009
- Nedberg NH, Turowski G, Guz K, Przytuła E, Uhrynowska M, Roald B, et al. Platelet alloimmunization is associated with low grade chronic histiocytic intervillositis - A new link to a rare placental lesion? Placenta. 2021 Sep;112:89–96. doi: https://doi.org/10.1016/j.placenta.2021.07.291DOI: https://doi.org/10.1016/j.placenta.2021.07.291
- Romero R, Whitten A, Korzeniewski SJ, Than NG, Chaemsaithong P, Miranda J, et al. Maternal floor infarction/massive perivillous fibrin deposition: a manifestation of maternal antifetal rejection? Am J Reprod Immunol. 2013 Oct;70(4):285–98. doi: https://doi.org/10.1111/aji.12143DOI: https://doi.org/10.1111/aji.12143
- Redline RW. Severe fetal placental vascular lesions in term infants with neurologic impairment. Am J Obstet Gynecol. 2005 Feb;192(2):452–7. doi: https://doi.org/10.1016/j.ajog.2004.07.030DOI: https://doi.org/10.1016/j.ajog.2004.07.030
- Hösli I, et al. Gestationsdiabetes. Schweiz Arzteztg. 2023;103(38):88–90. DOI: https://doi.org/10.4414/saez.2023.22112
- Redline RW. Disorders of placental circulation and the fetal brain. Clin Perinatol. 2009 Sep;36(3):549–59. doi: https://doi.org/10.1016/j.clp.2009.06.003DOI: https://doi.org/10.1016/j.clp.2009.06.003
- Clapp JF 3rd, Lopez B, Simonean S. Nuchal cord and neurodevelopmental performance at 1 year. J Soc Gynecol Investig. 1999;6(5):268–72. DOI: https://doi.org/10.1016/S1071-5576(99)00020-9
- Myers RE. Fetal asphyxia due to umbilical cord compression. Metabolic and brain pathologic consequences. Biol Neonate. 1975;26(1-2):21–43. doi: https://doi.org/10.1159/000240714DOI: https://doi.org/10.1159/000240714
- Guzick DS, Winn K. The association of chorioamnionitis with preterm delivery. Obstet Gynecol. 1985 Jan;65(1):11–6.
- Redline RW. Inflammatory response in acute chorioamnionitis. Semin Fetal Neonatal Med. 2012 Feb;17(1):20–5. doi: https://doi.org/10.1016/j.siny.2011.08.003DOI: https://doi.org/10.1016/j.siny.2011.08.003
- Leviton A, Allred EN, Kuban KC, Hecht JL, Onderdonk AB, O’shea TM, et al. Microbiologic and histologic characteristics of the extremely preterm infant’s placenta predict white matter damage and later cerebral palsy. the ELGAN study. Pediatr Res. 2010 Jan;67(1):95–101. doi: https://doi.org/10.1203/PDR.0b013e3181bf5fabDOI: https://doi.org/10.1203/PDR.0b013e3181bf5fab
- Blanc WA. Pathology of the placenta and cord in ascending and in haematogenous infection. Ciba Found Symp. 1979;(77):17–38. DOI: https://doi.org/10.1002/9780470720608.ch3
- Kraus FT. R.R., Gersell DJ, Nelson DM, Dicke JM., Placental Pathology. Washington (DC): American Registry of Pathology; 2004. DOI: https://doi.org/10.55418/1881041891
- Keenan WJ, Steichen JJ, Mahmood K, Altshuler G. Placental pathology compared with clinical outcome: a retrospective blind review. Am J Dis Child. 1977 Nov;131(11):1224–7. doi: https://doi.org/10.1001/archpedi.1977.02120240042009DOI: https://doi.org/10.1001/archpedi.1977.02120240042009
- Rogers BB, Alexander JM, Head J, McIntire D, Leveno KJ. Umbilical vein interleukin-6 levels correlate with the severity of placental inflammation and gestational age. Hum Pathol. 2002 Mar;33(3):335–40. doi: https://doi.org/10.1053/hupa.2002.32214DOI: https://doi.org/10.1053/hupa.2002.32214
- Fahmi A, Brügger M, Démoulins T, Zumkehr B, Oliveira Esteves BI, Bracher L, et al. SARS-CoV-2 can infect and propagate in human placenta explants. Cell Rep Med. 2021 Dec;2(12):100456. doi: https://doi.org/10.1016/j.xcrm.2021.100456DOI: https://doi.org/10.1016/j.xcrm.2021.100456
- Stenton S, McPartland J, Shukla R, Turner K, Marton T, Hargitai B, et al. SARS-COV2 placentitis and pregnancy outcome: A multicentre experience during the Alpha and early Delta waves of coronavirus pandemic in England. EClinicalMedicine. 2022 May;47:101389. doi: https://doi.org/10.1016/j.eclinm.2022.101389DOI: https://doi.org/10.1016/j.eclinm.2022.101389
- Schwartz DA, Avvad-Portari E, Babál P, Baldewijns M, Blomberg M, Bouachba A, et al. Placental Tissue Destruction and Insufficiency From COVID-19 Causes Stillbirth and Neonatal Death From Hypoxic-Ischemic Injury. Arch Pathol Lab Med. 2022 Jun;146(6):660–76. doi: https://doi.org/10.5858/arpa.2022-0029-SADOI: https://doi.org/10.5858/arpa.2022-0029-SA
- Boyd TK, Redline RW. Chronic histiocytic intervillositis: a placental lesion associated with recurrent reproductive loss. Hum Pathol. 2000 Nov;31(11):1389–96. doi: https://doi.org/10.1016/S0046-8177(00)80009-XDOI: https://doi.org/10.1053/hupa.2000.19454
- Bos M, Harris-Mostert ET, van der Meeren LE, Baelde JJ, Williams DJ, Nikkels PG, et al. Clinical outcomes in chronic intervillositis of unknown etiology. Placenta. 2020 Feb;91:19–23. doi: https://doi.org/10.1016/j.placenta.2020.01.001DOI: https://doi.org/10.1016/j.placenta.2020.01.001
- Redline RW. Villitis of unknown etiology: noninfectious chronic villitis in the placenta. Hum Pathol. 2007 Oct;38(10):1439–46. doi: https://doi.org/10.1016/j.humpath.2007.05.025DOI: https://doi.org/10.1016/j.humpath.2007.05.025
- Sentilhes L, Kayem G, Ambroselli C, Provansal M, Fernandez H, Perrotin F, et al. Fertility and pregnancy outcomes following conservative treatment for placenta accreta. Hum Reprod. 2010 Nov;25(11):2803–10. doi: https://doi.org/10.1093/humrep/deq239DOI: https://doi.org/10.1093/humrep/deq239
- Lausman A, McCarthy FP, Walker M, Kingdom J. Screening, diagnosis, and management of intrauterine growth restriction. J Obstet Gynaecol Can. 2012 Jan;34(1):17–28. doi: https://doi.org/10.1016/S1701-2163(16)35129-5DOI: https://doi.org/10.1016/S1701-2163(16)35129-5
- Himes KP, Simhan HN. Risk of recurrent preterm birth and placental pathology. Obstet Gynecol. 2008 Jul;112(1):121–6. doi: https://doi.org/10.1097/AOG.0b013e318179f024DOI: https://doi.org/10.1097/AOG.0b013e318179f024
- Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016 Sep;48(3):333–9. doi: https://doi.org/10.1002/uog.15884DOI: https://doi.org/10.1002/uog.15884
- DGGG, O., SGGG, Intrauterine growth restriction. Guideline of the German Society of Gynecology and Obstetrics. 2016.
- Burton GJ, Jauniaux E. Pathophysiology of placental-derived fetal growth restriction. Am J Obstet Gynecol. 2018 Feb;218(2S 2s):S745–61. doi: https://doi.org/10.1016/j.ajog.2017.11.577DOI: https://doi.org/10.1016/j.ajog.2017.11.577
- Sun C, Groom KM, Oyston C, Chamley LW, Clark AR, James JL. The placenta in fetal growth restriction: what is going wrong? Placenta. 2020 Jul;96:10–8. doi: https://doi.org/10.1016/j.placenta.2020.05.003DOI: https://doi.org/10.1016/j.placenta.2020.05.003
- Vounzoulaki E, Khunti K, Abner SC, Tan BK, Davies MJ, Gillies CL. Progression to type 2 diabetes in women with a known history of gestational diabetes: systematic review and meta-analysis. BMJ. 2020 May;369:m1361. doi: https://doi.org/10.1136/bmj.m1361DOI: https://doi.org/10.1136/bmj.m1361
- Correa A, Gilboa SM, Besser LM, Botto LD, Moore CA, Hobbs CA, et al. Diabetes mellitus and birth defects. Am J Obstet Gynecol. 2008 Sep;199(3):237.e1–9. doi: https://doi.org/10.1016/j.ajog.2008.06.028DOI: https://doi.org/10.1016/j.ajog.2008.06.028
- Parra-Herran C, Djordjevic B. Histopathology of Placenta Creta: Chorionic Villi Intrusion into Myometrial Vascular Spaces and Extravillous Trophoblast Proliferation are Frequent and Specific Findings With Implications for Diagnosis and Pathogenesis. Int J Gynecol Pathol. 2016 Nov;35(6):497–508. doi: https://doi.org/10.1097/PGP.0000000000000250DOI: https://doi.org/10.1097/PGP.0000000000000250
- Evers IM, Nikkels PG, Sikkema JM, Visser GH. Placental pathology in women with type 1 diabetes and in a control group with normal and large-for-gestational-age infants. Placenta. 2003;24(8-9):819–25. doi: https://doi.org/10.1016/S0143-4004(03)00128-0DOI: https://doi.org/10.1016/S0143-4004(03)00128-0
- Asmussen I. Ultrastructure of the villi and fetal capillaries of the placentas delivered by non-smoking diabetic women (White group D). Acta Pathol Microbiol Immunol Scand [A]. 1982 Mar;90(2):95–101. doi: https://doi.org/10.1111/j.1699-0463.1982.tb00069_90A.xDOI: https://doi.org/10.1111/j.1699-0463.1982.tb00069_90A.x
- Björk O, Persson B. Placental changes in relation to the degree of metabolic control in diabetes mellitus. Placenta. 1982;3(4):367–78. doi: https://doi.org/10.1016/S0143-4004(82)80030-1DOI: https://doi.org/10.1016/S0143-4004(82)80030-1
- Teasdale F. Histomorphometry of the human placenta in Class B diabetes mellitus. Placenta. 1983;4(1):1–12. doi: https://doi.org/10.1016/S0143-4004(83)80012-5DOI: https://doi.org/10.1016/S0143-4004(83)80012-5
- Jauniaux E, Burton GJ. Villous histomorphometry and placental bed biopsy investigation in Type I diabetic pregnancies. Placenta. 2006;27(4-5):468–74. doi: https://doi.org/10.1016/j.placenta.2005.04.010DOI: https://doi.org/10.1016/j.placenta.2005.04.010
- Nelson SM, Coan PM, Burton GJ, Lindsay RS. Placental structure in type 1 diabetes: relation to fetal insulin, leptin, and IGF-I. Diabetes. 2009 Nov;58(11):2634–41. doi: https://doi.org/10.2337/db09-0739DOI: https://doi.org/10.2337/db09-0739
- Daskalakis G, Marinopoulos S, Krielesi V, Papapanagiotou A, Papantoniou N, Mesogitis S, et al. Placental pathology in women with gestational diabetes. Acta Obstet Gynecol Scand. 2008;87(4):403–7. doi: https://doi.org/10.1080/00016340801908783DOI: https://doi.org/10.1080/00016340801908783
- Huynh J, Dawson D, Roberts D, Bentley-Lewis R. A systematic review of placental pathology in maternal diabetes mellitus. Placenta. 2015 Feb;36(2):101–14. doi: https://doi.org/10.1016/j.placenta.2014.11.021DOI: https://doi.org/10.1016/j.placenta.2014.11.021
- Dubova EA, Pavlov KA, Yesayan RM, Nagovitsyna MN, Tkacheva ON, Shestakova MV, et al. Morphometric characteristics of placental villi in pregnant women with diabetes. Bull Exp Biol Med. 2011 Sep;151(5):650–4. doi: https://doi.org/10.1007/s10517-011-1406-9DOI: https://doi.org/10.1007/s10517-011-1406-9
- Huynh J, Yamada J, Beauharnais C, Wenger JB, Thadhani RI, Wexler D, et al. Type 1, type 2 and gestational diabetes mellitus differentially impact placental pathologic characteristics of uteroplacental malperfusion. Placenta. 2015 Oct;36(10):1161–6. doi: https://doi.org/10.1016/j.placenta.2015.08.004DOI: https://doi.org/10.1016/j.placenta.2015.08.004
- Makhseed M, Musini VM, Ahmed MA, Al-Harmi J. Placental pathology in relation to the White’s classification of diabetes mellitus. Arch Gynecol Obstet. 2002 Jul;266(3):136–40. doi: https://doi.org/10.1007/s004040100232DOI: https://doi.org/10.1007/s004040100232
- Alwasel SH, Abotalib Z, Aljarallah JS, Osmond C, Al Omar SY, Harrath A, et al. The breadth of the placental surface but not the length is associated with body size at birth. Placenta. 2012 Aug;33(8):619–22. doi: https://doi.org/10.1016/j.placenta.2012.04.015DOI: https://doi.org/10.1016/j.placenta.2012.04.015
- Yampolsky M, Salafia CM, Shlakhter O, Haas D, Eucker B, Thorp J. Centrality of the umbilical cord insertion in a human placenta influences the placental efficiency. Placenta. 2009 Dec;30(12):1058–64. doi: https://doi.org/10.1016/j.placenta.2009.10.001DOI: https://doi.org/10.1016/j.placenta.2009.10.001
- Schwartz N, Mandel D, Shlakhter O, Coletta J, Pessel C, Timor-Tritsch IE, et al. Placental morphologic features and chorionic surface vasculature at term are highly correlated with 3-dimensional sonographic measurements at 11 to 14 weeks. J Ultrasound Med. 2011 Sep;30(9):1171–8. doi: https://doi.org/10.7863/jum.2011.30.9.1171DOI: https://doi.org/10.7863/jum.2011.30.9.1171
- Hecht JL, Baergen R, Ernst LM, Katzman PJ, Jacques SM, Jauniaux E, et al. Classification and reporting guidelines for the pathology diagnosis of placenta accreta spectrum (PAS) disorders: recommendations from an expert panel. Mod Pathol. 2020 Dec;33(12):2382–96. doi: https://doi.org/10.1038/s41379-020-0569-1DOI: https://doi.org/10.1038/s41379-020-0569-1
- Benirschke K. B.G., Baergen RN., Pathology of the human placenta. 6th edition. 2012. DOI: https://doi.org/10.1007/978-3-642-23941-0
- Linn RL, Miller ES, Lim G, Ernst LM. Adherent basal plate myometrial fibers in the delivered placenta as a risk factor for development of subsequent placenta accreta. Placenta. 2015 Dec;36(12):1419–24. doi: https://doi.org/10.1016/j.placenta.2015.10.004DOI: https://doi.org/10.1016/j.placenta.2015.10.004
- Miller ES, Linn RL, Ernst LM. Does the presence of placental basal plate myometrial fibres increase the risk of subsequent morbidly adherent placenta: a case-control study. BJOG. 2016 Dec;123(13):2140–5. doi: https://doi.org/10.1111/1471-0528.13579DOI: https://doi.org/10.1111/1471-0528.13579
- Jauniaux E, Jurkovic D. Placenta accreta: pathogenesis of a 20th century iatrogenic uterine disease. Placenta. 2012 Apr;33(4):244–51. doi: https://doi.org/10.1016/j.placenta.2011.11.010DOI: https://doi.org/10.1016/j.placenta.2011.11.010
- Vinograd A, Wainstock T, Mazor M, Mastrolia SA, Beer-Weisel R, Klaitman V, et al. A prior placenta accreta is an independent risk factor for post-partum hemorrhage in subsequent gestations. Eur J Obstet Gynecol Reprod Biol. 2015 Apr;187:20–4. doi: https://doi.org/10.1016/j.ejogrb.2015.01.014DOI: https://doi.org/10.1016/j.ejogrb.2015.01.014
- Roeca C, Little SE, Carusi DA. Pathologically Diagnosed Placenta Accreta and Hemorrhagic Morbidity in a Subsequent Pregnancy. Obstet Gynecol. 2017 Feb;129(2):321–6. doi: https://doi.org/10.1097/AOG.0000000000001843DOI: https://doi.org/10.1097/AOG.0000000000001843
- Kingdom JC, Audette MC, Hobson SR, Windrim RC, Morgen E. A placenta clinic approach to the diagnosis and management of fetal growth restriction. Am J Obstet Gynecol. 2018 Feb;218(2S 2s):S803–17. doi: https://doi.org/10.1016/j.ajog.2017.11.575DOI: https://doi.org/10.1016/j.ajog.2017.11.575
- Thompson JM, Irgens LM, Skjaerven R, Rasmussen S. Placenta weight percentile curves for singleton deliveries. BJOG. 2007 Jun;114(6):715–20. 10.1111/j.1471-0528.2007.01327.x DOI: https://doi.org/10.1111/j.1471-0528.2007.01327.x
- Vogel M, Turowski G, eds. Clinical Pathology of the Placenta. Berlin: De Gruyter; 2019. 10.1515/9783110452600 DOI: https://doi.org/10.1515/9783110452600
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- Francesca Compagno, Klaudia Naegele, Christian R. Kahlert, Irene Hösli, Karoline Aebi-Popp, Begona Martinez de Tejada, Paolo Paioni, Sabine Yerly, Jürg Böni, Manuel Battegay, Christoph Rudin, Hans H. Hirsch, the Swiss HIV Cohort Study, The rate of mother-to-child transmission of antiretroviral drug-resistant HIV strains is low in the Swiss Mother and Child HIV Cohort Study, Swiss Medical Weekly: Vol. 149 No. 1314 (2019)
- Jarmila A. Zdanowicz, Eliane Sommer, Luigi Raio, Mathias Nelle, Roland Gerull, Do late preterm twins face an increased neonatal morbidity compared with singletons?, Swiss Medical Weekly: Vol. 148 No. 0102 (2018)
- Christian De Geyter, Oliver Sterthaus, Peter Miny, Friedel Wenzel, Olav Lapaire, Maria De Geyter, Gideon Sartorius, First successful pregnancy in Switzerland after prospective sex determination of the embryo through the separation of X-chromosome bearing spermatozoa, Swiss Medical Weekly: Vol. 143 No. 0708 (2013)
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