Placental histopathology and pregnancy outcomes in “early” vs. “late” placental abruption
Abstract
Placenta-associated pregnancy complications (fetal growth restriction and preeclampsia) are traditionally classified as "early" and "late" due to their different pathophysiology, histopathology, and pregnancy outcomes. As placental abruption (PA) represents another placenta-associated complication, we aimed to study if this categorization can be applied to PA as well. Pregnancy and placental reports of all pregnancies complicated by PA between November 2008 and January 2019 were reviewed. Maternal background, pregnancy outcomes, and placental histopathology were compared between cases of PA < 34 weeks (early PA group) vs. > 34 weeks (late PA group). Placental lesions were classified according to the "Amsterdam" criteria. The primary outcome was severe neonatal morbidity (≥ 1 severe neonatal complications: seizures, IVH, HIE, PVL, blood transfusion, NEC, or death). Included were 305 cases of PA, 71 (23.3%) in the early group and 234 (76.7%) in the late group. The early PA group was characterized by higher rates of vaginal bleeding upon presentation (p = 0.003), DIC (p = 0.018), and severe neonatal morbidity (p < 0.001). The late PA group was characterized by a higher rate of urgent Cesarean deliveries (p < 0.001). The early PA group was characterized by higher rates of placental maternal vascular malperfusion (MVM) lesions (p < 0.001), maternal inflammatory response (MIR) lesions (p < 0.001), placental hemorrhage (p < 0.001), and a lower feto-placental ratio (p < 0.001). Using regression analysis, we found that severe neonatal morbidity was independently associated with early abruption (aOR = 5.3, 95% CI = 3.9-7.6), placental MVM (aOR = 1.5, 95% CI = 1.2-1.9), placental MIR (aOR = 1.9, 95% CI = 1.4-2.3), and inversely associated with antenatal corticosteroids (aOR = 0.9, 95% CI = 0.6-0.98). "Early" and "late" PA significantly differ in their presentation, placental pathology, and pregnancy outcomes.
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In a retrospective study of 305 cases of abruption, abruption ≥34 weeks' gestation was characterized by fewer placental maternal vascular malperfusion lesions, maternal inflammatory response lesions, and placental hemorrhages compared to abruption <34 weeks.
“A retrospective study of 305 cases of abruption that characterized placental histopathology found that abruption ≥34 week’s gestation were characterized by fewer placental maternal vascular malperfusion lesions, maternal inflammatory response lesions, and placental hemorrhages compared to abruption <34 weeks (76).”
From Placental abruption at near-term and term gestations: Pathophysiology, epidemiology, diagnosis, and management (2023) · cites this paper as [76]
Cites
Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus
The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus* (2002) · Diabetes Care · doi:10.2337/diacare.25.2007.s5 · Cited by 10,320 · see citing works
(2013) · doi:10.1097/01.aog.0000437382.03963.88 · Cited by 3,961 · see citing works
Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus
The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) · Diabetes Care · doi:10.2337/diacare.26.2007.s5 · Cited by 2,689 · see citing works
Taylor, F., Toh, C.-H., Hoots, K., Wada, H., & Levi, M. (2001) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1616068 · Cited by 2,285 · see citing works
Khong, T. Y., Mooney, E. E., Ariel, I., Balmus, N. C. M., Boyd, T. K., Bründler, M., Derricott, H., Evans, M. J., Faye-Petersen, O. M., Gillan, J., et al. (2016) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2015-0225-cc · Cited by 1,748 · see citing works
The “Great Obstetrical Syndromes” are associated with disorders of deep placentation
Brosens, I., Pijnenborg, R., Vercruysse, L., & Romero, R. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.08.009 · Cited by 1,568 · see citing works
The Two Stage Model of Preeclampsia: Variations on the Theme
Roberts, J., & Hubel, C. A. (2008) · Placenta · doi:10.1016/j.placenta.2008.11.009 · Cited by 928 · see citing works
Lisonkova, S., & Joseph, K. S. (2013) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2013.08.019 · Cited by 926 · see citing works
Figueras, F., & Gratacós, E. (2014) · Fetal Diagnosis and Therapy · doi:10.1159/000357592 · Cited by 799 · see citing works
Subclassification of Preeclampsia
von Dadelszen, P., Magee, L. A., & Roberts, J. M. (2003) · Hypertension in Pregnancy · doi:10.1081/prg-120021060 · Cited by 764 · see citing works
Valensise, H. C. C., Vasapollo, B., Gagliardi, G., & Novelli, G. P. (2008) · Hypertension · doi:10.1161/hypertensionaha.108.117358 · Cited by 598 · see citing works
Ness, R. B., & Roberts, J. M. (1996) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(96)70056-x · Cited by 568 · see citing works
Birth weight standards in the live-born population in Israel.
Dollberg, S., Haklai, Z., Mimouni, F. B., et al. (2005) · PubMed · Cited by 563 · see citing works
Oyelese, Y., & Ananth, C. V. (2006) · Obstetrics & Gynecology · doi:10.1097/01.aog.0000239439.04364.9a · Cited by 508 · see citing works
The cerebroplacental Doppler ratio revisited
Baschat, A., & Gembruch, U. (2003) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20 · Cited by 505 · see citing works
Arduini, D., & Rizzo, G. (1990) · Journal of Perinatal Medicine · doi:10.1515/jpme.1990.18.3.165 · Cited by 480 · see citing works
Classification of placental lesions
Redline, R. W. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.05.056 · Cited by 439 · see citing works
Placental abruption and adverse perinatal outcomes
Ananth, C. V. (1999) · JAMA · doi:10.1001/jama.282.17.1646 · Cited by 412 · see citing works
Placental Pathology in Early-Onset and Late-Onset Fetal Growth Restriction
Mifsud, W., & Sebire, N. J. (2014) · Fetal Diagnosis and Therapy · doi:10.1159/000359969 · Cited by 328 · see citing works
Reference Values for Singleton and Twin Placental Weights
Pınar, H., Sung, C. J., Oyer, C. E., et al. (1996) · Pediatric Pathology & Laboratory Medicine · doi:10.1080/15513819609168713 · Cited by 317 · see citing works
Placental abruption and perinatal mortality in the United States
Ananth, C. V., & Wilcox, A. J. (2001) · American Journal of Epidemiology · doi:10.1093/aje/153.4.332 · Cited by 311 · see citing works
Maternal Morbidity Associated With Early-Onset and Late-Onset Preeclampsia
Lisonkova, S., Sabr, Y., Mayer, C., Young, C. B., Skoll, A., & Joseph, K. S. (2014) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000000472 · Cited by 310 · see citing works
Veerbeek, J. H. W., Hermes, W., Breimer, A. Y., van Rijn, B. B., Koenen, S. V., Mol, B. W., Franx, A., de Groot, C. J. M., & Koster, M. P. H. (2015) · Hypertension · doi:10.1161/hypertensionaha.114.04850 · Cited by 306 · see citing works
Crispi, F., Llurba, E., Domı́nguez, C., Martı́n-Gallán, P., Cabero, L., & Gratacós, E. (2007) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.5184 · Cited by 264 · see citing works
Ananth, C. (1999) · Obstetrics & Gynecology · doi:10.1016/s0029-7844(98)00408-6 · Cited by 236 · see citing works
(2013) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000433981.36184.4e · Cited by 222 · see citing works
ACOG Practice Bulletin No. 101: Ultrasonography in Pregnancy
(2009) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31819930b0 · Cited by 214 · see citing works
Placental Abruption among Singleton and Twin Births in the United States: Risk Factor Profiles
Ananth, C. V. (2001) · American Journal of Epidemiology · doi:10.1093/aje/153.8.771 · Cited by 203 · see citing works
Wójtowicz, A., Zembala-Szczerba, M., Babczyk, D., Kołodziejczyk-Pietruszka, M., Lewaczyńska, O., & Huras, H. K. (2019) · International Journal of Hypertension · doi:10.1155/2019/4108271 · Cited by 165 · see citing works
Etiology, clinical manifestations, and prediction of placental abruption
TIKKANEN, M. (2010) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016341003686081 · Cited by 158 · see citing works
Kehl, S., Schelkle, A., Thomas, A., Puhl, A., Meqdad, K., Tuschy, B., Berlit, S., Weiss, C., Bayer, C., Heimrich, J., et al. (2016) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.14924 · Cited by 152 · see citing works
ACOG Practice Bulletin No. 98: Ultrasonography in Pregnancy
Abuhamad, A. (2008) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31818b1fba · Cited by 152 · see citing works
Tay, J., Foo, L. F., Masini, G., Bennett, P. R., McEniery, C. M., Wilkinson, I. B., & Lees, C. C. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2018.02.007 · Cited by 138 · see citing works
(1986) · PubMed · Cited by 127 · see citing works
Are Early and Late Preeclampsia Distinct Subclasses of the Disease—What Does the Placenta Reveal?
van der Merwe, J., Hall, D. R., Wright, C. A., Schubert, P. T., & Grove, D. (2010) · Hypertension in Pregnancy · doi:10.3109/10641950903572282 · Cited by 102 · see citing works
The clinical implications of placental diagnoses
Redline, R. W. (2014) · Seminars in Perinatology · doi:10.1053/j.semperi.2014.10.002 · Cited by 101 · see citing works
The placental factor in early- and late-onset normotensive fetal growth restriction
Kovo, M., Schreiber, L., Ben‐Haroush, A., Cohen, G., Weiner, E., Golan, A., & Bar, J. (2013) · Placenta · doi:10.1016/j.placenta.2012.11.010 · Cited by 99 · see citing works
Self-citationKovo, M., Schreiber, L., Ben‐Haroush, A., Gold, E., Golan, A., & Bar, J. (2012) · Prenatal Diagnosis · doi:10.1002/pd.3872 · Cited by 92 · see citing works
Self-citationThe association between placental histopathology and autism spectrum disorder
Straughen, J. K., Misra, D. P., Divine, G., Shah, R., Perez, G., VanHorn, S., Onbreyt, V., Dygulska, B., Schmitt, R., Lederman, S., et al. (2017) · Placenta · doi:10.1016/j.placenta.2017.07.006 · Cited by 91 · see citing works
Gaudineau, A. (2013) · Journal de gynécologie, obstétrique et biologie de la reproduction. Supplément/Journal de gynécologie obstétrique et biologie de la reproduction · doi:10.1016/j.jgyn.2013.09.013 · Cited by 82 · see citing works
Placental histology in spontaneous and indicated preterm birth: A case control study
Nijman, T. A. J., van Vliet, E. O. G., Benders, M. J. N. L., et al. (2016) · Placenta · doi:10.1016/j.placenta.2016.10.006 · Cited by 82 · see citing works
Impact of early- and late-onset preeclampsia on features of placental and newborn vascular health
Herzog, E. M., Eggink, A. J., Reijnierse, A., Kerkhof, M. A. M., de Krijger, R. R., Roks, A. J. M., Reiss, I. K. M., Nigg, A. L., Eilers, P. H. C., Steegers, E. A. P., et al. (2016) · Placenta · doi:10.1016/j.placenta.2016.11.014 · Cited by 81 · see citing works
Vasoactive agents for the prediction of early- and late-onset preeclampsia in a high-risk cohort
Villa, P., Hämäläinen, E. K., Mäki, A., Räikkönen, K., Pesonen, A., Taipale, P., Kajantie, E., & Laivuori, H. M. (2013) · BMC Pregnancy and Childbirth · doi:10.1186/1471-2393-13-110 · Cited by 76 · see citing works
Practice Bulletin No. 118: Antiphospholipid Syndrome
(2010) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31820a61f9 · Cited by 76 · see citing works
Mureșan, D., Rotar, I. C., & Stamatian, F. V. (2016) · Medical Ultrasonography · doi:10.11152/mu.2013.2066.181.dop · Cited by 72 · see citing works
Wikström, A., Nash, P., Eriksson, U. J., & Olovsson, M. H. (2009) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2009.06.024 · Cited by 67 · see citing works
Crovetto, F., Triunfo, S., Crispi, F., Rodríguez‐Sureda, V., Domı́nguez, C., Figueras, F., & Gratacós, E. (2016) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.15919 · Cited by 63 · see citing works
Pathologic placental lesions in early and late fetal growth restriction
Spinillo, A., Gardella, B., Adamo, L., Muscettola, G., Fiandrino, G., & Cesari, S. (2019) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.13699 · Cited by 63 · see citing works
Paulés, C., Youssef, L., Rovira, C., Crovetto, F., Nadal, A., Peguero, A., Figueras, F., Eixarch, E., Crispi, F., Miranda, J., et al. (2019) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20350 · Cited by 61 · see citing works
The placental component and obstetric outcome in severe preeclampsia with and without HELLP syndrome
Weiner, E., Schreiber, L., Grinstein, E., et al. (2016) · Placenta · doi:10.1016/j.placenta.2016.09.012 · Cited by 60 · see citing works
Self-citationDefining early vs late fetal growth restriction by placental pathology
Aviram, A., Sherman, C., Kingdom, J. C., Zaltz, A., Barrett, J. F. R., & Melamed, N. (2018) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.13499 · Cited by 54 · see citing works
Effects of Placental Inflammation on Neonatal Outcome in Preterm Infants
Liu, Z., Tang, Z., Li, J., & Yang, Y. (2013) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2013.05.007 · Cited by 52 · see citing works
Weiner, E., Feldstein, O., Tamayev, L., Grinstein, E., Barber, E., Bar, J., Schreiber, L., & Kovo, M. (2018) · Pregnancy Hypertension · doi:10.1016/j.preghy.2018.02.001 · Cited by 48 · see citing works
Self-citationRaghavan, R., Bustamante-Helfrich, B., Cerda, S. R., Ji, Y., Burd, I. D., Wang, G., Hong, X., Fu, L., Pearson, C., Fallin, M. D., et al. (2019) · Placenta · doi:10.1016/j.placenta.2019.06.374 · Cited by 47 · see citing works
The effect of immersion formaldehyde fixation on human placental weight.
Fox, G., Wesep, R. V., Resau, J., et al. (1991) · PubMed · Cited by 46 · see citing works
Matsuda, Y., Maeda, T., & Kouno, S. (2003) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(02)00219-1 · Cited by 39 · see citing works
Placental findings among newborns with hypoxic ischemic encephalopathy
Bingham, A., Gündoğan, F., Rand, K., & Laptook, A. R. (2019) · Journal of Perinatology · doi:10.1038/s41372-019-0334-9 · Cited by 32 · see citing works
Angiogenic factors and uterine Doppler velocimetry in early‐ and late‐onset preeclampsia
Tobinaga, C., Torloni, M. R., Gueuvoghlanian‐Silva, B. Y., Pendeloski, K. P. T., Akita, P. A., Sass, N., & Daher, S. (2014) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.12366 · Cited by 30 · see citing works
Vaddamani, S., Keepanasseril, A., Pillai, A. A., et al. (2017) · Pregnancy Hypertension · doi:10.1016/j.preghy.2017.10.010 · Cited by 30 · see citing works
Correlation of Placental Pathology with Perinatal Brain Injury
Redline, R. W. (2012) · Surgical pathology clinics · doi:10.1016/j.path.2012.11.005 · Cited by 27 · see citing works
Placental histopathology in preterm fetal growth restriction
Sehgal, A., Dahlstrom, J. E., Chan, Y. F., Allison, B. J., Miller, S., & Polglase, G. R. (2018) · Journal of Paediatrics and Child Health · doi:10.1111/jpc.14251 · Cited by 24 · see citing works
Levy, M., Kovo, M., Schreiber, L., Kleiner, I., Grinstein, E., Koren, L., Barda, G., Bar, J., & Weiner, E. (2019) · Placenta · doi:10.1016/j.placenta.2019.04.001 · Cited by 16 · see citing works
Self-citationSchlumpf, R. B., Marinček, B., von Schulthess, G., et al. (1989) · Diabetes · doi:10.2337/diab.38.1.s24 · Cited by 4 · see citing works
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- Authors
- Gonen, N., Levy, M., Kovo, M., Schreiber, L., Noy, L. K., Volpert, E., Bar, J., & Weiner, E.
- Affiliations
- Tel Aviv University (IL)
- Corresponding author
- Weiner, Eran
- Venue
- Reproductive Sciences
- Published
- 2020-08-18
- Volume
- 28
- Issue
- 2
- Pages
- 351-360
- ISSN
- 1933-7191 (ISSN-L)
- 1933-7205
- OpenAlex
- W3067375198
- Cited by
- 22
- References
- 63
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 3 · 2023: 3 · 2022: 4 · 2021: 3
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reproductive Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Maternal and fetal healthcare
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- placental abruption, placental pathology, Amsterdam criteria, maternal vascular malperfusion, maternal inflammatory response, antenatal corticosteroids, pregnancy outcomes, fetal growth restriction, preeclampsia, disseminated intravascular coagulation, placental hemorrhage, preterm birth
- MeSH terms
- Abruptio Placentae, Adult, Cesarean Section, Female, Gestational Age, Humans, Infant, Infant Mortality, Infant, Newborn, Infant, Newborn, Diseases, Infant, Premature, Placenta, Pregnancy, Pregnancy Outcome, Retrospective Studies, Risk Factors, Time Factors, Risk Assessment, Premature Birth
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