Am J Perinatol 2023; 40(12): 1328-1335
DOI: 10.1055/s-0041-1735554
Original Article

Shallow Placentation: A Distinct Category of Placental Lesions

Jerzy Stanek
1   Division of Pathology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio
› Author Affiliations

Abstract

Objective Shallow placental implantation (SPI) features placental maldistribution of extravillous trophoblasts and includes excessive amount of extravillous trophoblasts, chorionic microcysts in the membranes and chorionic disc, and decidual clusters of multinucleate trophoblasts. The histological lesions were previously and individually reported in association with various clinical and placental abnormalities. This retrospective statistical analysis of a large placental database from high-risk pregnancy statistically compares placentas with and without a composite group of features of SPI.

Study Design Twenty-four independent abnormal clinical and 44 other than SPI placental phenotypes were compared between 4,930 placentas without (group 1) and 1,283 placentas with one or more histological features of SPI (composite SPI group; group 2). Placentas were received for pathology examination at a discretion of obstetricians. Placental lesion terminology was consistent with the Amsterdam criteria, with addition of other lesions described more recently.

Results Cases of group 2 featured statistically and significantly (p < 0.001after Bonferroni's correction) more common than group 1 on the following measures: gestational hypertension, preeclampsia, oligohydramnios, polyhydramnios, abnormal Dopplers, induction of labor, cesarean section, perinatal mortality, fetal growth restriction, stay in neonatal intensive care unit (NICU), congenital malformation, deep meconium penetration, intravillous hemorrhage, villous infarction, membrane laminar necrosis, fetal blood erythroblastosis, decidual arteriopathy (hypertrophic and atherosis), chronic hypoxic injury (uterine and postuterine), intervillous thrombus, segmental and global fetal vascular malperfusion, various umbilical cord abnormalities, and basal plate myometrial fibers.

Conclusion SPI placentas were statistically and significantly associated with 48% abnormal independent clinical and 51% independent abnormal placental phenotypes such as acute and chronic hypoxic lesions, fetal vascular malperfusion, umbilical cord abnormalities, and basal plate myometrial fibers among others. Therefore, SPI should be regarded as a category of placental lesions related to maternal vascular malperfusion and the “Great Obstetrical Syndromes.”

Key Points

  • SPI reflects abnormal distribution of extravillous trophoblasts.

  • SPI features abnormal clinical and placental phenotypes.

  • SPI portends increased risk of complicated perinatal outcome.



Publication History

Received: 07 March 2021

Accepted: 05 August 2021

Article published online:
29 September 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Brosens I, Pijnenborg R, Vercruysse L, Romero R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 2011; 204 (03) 193-201
  • 2 Naicker T, Khedun SM, Moodley J, Pijnenborg R. Quantitative analysis of trophoblast invasion in preeclampsia. Acta Obstet Gynecol Scand 2003; 82 (08) 722-729
  • 3 Stanek J. Chorionic disk extravillous trophoblasts in placental diagnosis. Am J Clin Pathol 2011; 136 (04) 540-547
  • 4 Stanek J. Histological features of shallow placental implantation unify early onset and late onset preeclampsia. Pediatr Dev Pathol 2019; 22 (02) 112-122
  • 5 Stanek J, Biesiada J. Clustering of maternal/fetal clinical conditions and outcomes and placental lesions. Am J Obstet Gynecol 2012; 206 (06) 493.e1–e8
  • 6 Stanek J. Acute and chronic placental membrane hypoxic lesions. Virchows Arch 2009; 455 (04) 315-322
  • 7 Shchegolev AI, Lyapin VM, Tumanova UN, Vodneva DN, Shmakov RG. Histological hanges in the placenta and vascularization of its villi in early- and late-onset preeclampsia [in Russian]. Arkh Patol 2016; 78 (01) 13-18
  • 8 Stanek J. Decidual arteriolopathy with or without associated hypertension modifies the underlying histomorphology in placentas from diabetic mothers. J Obstet Gynaecol Res 2017; 43 (05) 839-847
  • 9 Stanek J. Patterns of placental injury in congenital anomalies in second half of pregnancy. Pediatr Dev Pathol 2019; 22 (06) 513-522
  • 10 Kingdom JC, Kaufmann P. Oxygen and placental villous development: origins of fetal hypoxia. Placenta 1997; 18 (08) 613-621 , discussion 623–626
  • 11 Stanek J. Association of coexisting morphological umbilical cord abnormality and clinical cord compromise with hypoxic and thrombotic placental histology. Virchows Arch 2016; 468 (06) 723-732
  • 12 Huppertz B. Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 2008; 51 (04) 970-975
  • 13 Levy M, Alberti D, Kovo M. et al. Placental pathology in pregnancies complicated by fetal growth restriction: recurrence vs. new onset. Arch Gynecol Obstet 2020; 301 (06) 1397-1404
  • 14 Roeca C, Little SE, Carusi DA. Pathologically diagnosed placenta accrete and hemorrhagic morbidity in a subsequent pregnancy. Obstet Gynecol 2017; 129 (02) 321-326
  • 15 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; 123 (13) 2140-2145
  • 16 Stanek J. Hypoxic patterns of placental injury: a review. Arch Pathol Lab Med 2013; 137 (05) 706-720
  • 17 Stanek J, Drummond Z. Occult placenta accreta: the missing link in the diagnosis of abnormal placentation. Pediatr Dev Pathol 2007; 10 (04) 266-273
  • 18 Khong TY, Werger AC. Myometrial fibers in the placental basal plate can confirm but do not necessarily indicate clinical placenta accreta. Am J Clin Pathol 2001; 116 (05) 703-708
  • 19 Tantbirojn P, Crum CP, Parast MM. Pathophysiology of placenta creta: the role of decidua and extravillous trophoblast. Placenta 2008; 29 (07) 639-645
  • 20 Stanek J. Placenta creta: A spectrum of lesions associated with shallow placental implantation. Obstet Gynecol Int 2020; 2020: 4230451
  • 21 Sherer DM, Salafia CM, Minior VK, Sanders M, Ernst L, Vintzileos AM. Placental basal plate myometrial fibers: clinical correlations of abnormally deep trophoblast invasion. Obstet Gynecol 1996; 87 (03) 444-449
  • 22 Kim KR, Jun SY, Kim JY, Ro JY. Implantation site intermediate trophoblasts in placenta cretas. Mod Pathol 2004; 17 (12) 1483-1490
  • 23 Khong TY, Robertson WB. Placenta creta and placenta praevia creta. Placenta 1987; 8 (04) 399-409
  • 24 Khong TY, Mooney EE, Ariel I. et al. Sampling and definitions of placental lesions. Amsterdam placental workshop group consensus statement. Arch Pathol Lab Med 2016; 140 (07) 698-713
  • 25 Stanek J, Al-Ahmadie HA. Laminar necrosis of placental membranes: a histologic sign of uteroplacental hypoxia. Pediatr Dev Pathol 2005; 8 (01) 34-42
  • 26 Stanek J, Sheridan RM, Le LD, Crombleholme TM. Placental fetal thrombotic vasculopathy in severe congenital anomalies prompting EXIT procedure. Placenta 2011; 32 (05) 373-379
  • 27 Stanek J, Weng E. Microscopic chorionic pseudocysts in placental membranes: a histologic lesion of in utero hypoxia. Pediatr Dev Pathol 2007; 10 (03) 192-198
  • 28 Stanek J. Segmental villous mineralization: a placental feature of fetal vascular malperfusion. Placenta 2019; 86: 20-27
  • 29 Stanek J, Abdaljaleel M. CD34 immunostain increases the sensitivity of placental diagnosis of fetal vascular malperfusion in stillbirth. Placenta 2019; 77: 30-38
  • 30 Stanek J. Periarterial stem villous edema is associated with hypercoiled umbilical cord and stem obliterative endarteritis. OJOG 2013; 3 (9A): 9-14
  • 31 Stanek J. Membrane microscopic chorionic pseudocysts are associated with increased amount of placental extravillous trophoblasts. Pathology 2010; 42 (02) 125-130
  • 32 Huppertz B, Gauster M, Orendi K, König J, Moser G. Oxygen as modulator of trophoblast invasion. J Anat 2009; 215 (01) 14-20
  • 33 Liu Y, Han TL, Luo X. et al. The metabolic role of LncZBTB39-1:2 in the trophoblast mobility of preeclampsia. Genes Dis 2018; 5 (03) 235-244
  • 34 Barnea ER, Vialard F, Moindjie H, Ornaghi S, Dieudonne MN, Paidas MJ. PreImplantation Factor (PIF*) endogenously prevents preeclampsia: Promotes trophoblast invasion and reduces oxidative stress. J Reprod Immunol 2016; 114: 58-64
  • 35 Fisher SJ. Why is placentation abnormal in preeclampsia?. Am J Obstet Gynecol 2015; 213 (4, Suppl) S115-S122
  • 36 Wang L, Zhang Y, Qu H. et al. Reduced ELABELA expression attenuates trophoblast invasion through the PI3K/AKT/mTOR pathway in early onset preeclampsia. Placenta 2019; 87: 38-45
  • 37 Garrido-Gómez T, Castillo-Marco N, Cordero T, Simón C. Decidualization resistance in the origin of preeclampsia. Am J Obster Gynecol 2020; S002-9378 (20) 31130-31133
  • 38 Romero R, Kim YM, Pacora P. et al. The frequency and type of placental histologic lesions in term pregnancies with normal outcome. J Perinat Med 2018; 46 (06) 613-630
  • 39 Pathak S, Sebire NJ, Hook L. et al. Relationship between placental morphology and histological findings in an unselected population near term. Virchows Arch 2011; 459 (01) 11-20
  • 40 Viscardi RM, Sun CC. Placental lesion multiplicity: risk factor for IUGR and neonatal cranial ultrasound abnormalities. Early Hum Dev 2001; 62 (01) 1-10
  • 41 Stanek J. Placental membrane and placental disc microscopic chorionic cysts share similar clinicopathologic associations. Pediatr Dev Pathol 2011; 14 (01) 1-9
  • 42 Stanek J, Biesiada J. Sensitivity and specificity of finding of multinucleate trophoblastic giant cells in decidua in placentas from high-risk pregnancies. Hum Pathol 2012; 43 (02) 261-268
  • 43 Stanek J, Biesiada J, Trzeszcz M. Clinicoplacental phenotypes vary with gestational age: an analysis by classical and clustering methods. Acta Obstet Gynecol Scand 2014; 93 (04) 392-398
  • 44 Stanek J. Comparison of placental pathology in preterm, late-preterm, near-term, and term births. Am J Obstet Gynecol 2014; 210 (03) 234.e1-234.e6
  • 45 Stanek J. Laminar necrosis, membrane chorionic microcysts, and chorion nodosum. In: Khong TY, Mooney EE, Nikkels PG, Gordijn SJ. eds. Pathology of the Placenta. A Practical Guide. Switzerland, AG: Springer Nature; 2019: 285-293
  • 46 Redline RW, Boyd T, Campbell V. et al; Society for Pediatric Pathology, Perinatal Section, Maternal Vascular Perfusion Nosology Committee. Maternal vascular underperfusion: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2004; 7 (03) 237-249
  • 47 Redline RW, Patterson P. Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum Pathol 1995; 26 (06) 594-600
  • 48 Stanek J, Biesiada J. Clustering and classical analysis of clinical and placental phenotypes in fetal growth restriction and constitutional fetal smallness. Placenta 2016; 42: 93-105
  • 49 Endler M, Saltvedt S, Papadogiannakis N. Macroscopic and histological characteristics of retained placenta: a prospectively collected case-control study. Placenta 2016; 41: 39-44
  • 50 Hecht JL, Baergen R, Ernst LM. et al. Classification and reporting guidelines for the pathology diagnosis of placenta accreta spectrum (PAS) disorders: recommendations from an expert panel. Mod Pathol 2020; 33 (12) 2382-2396
  • 51 Jacques SM, Qureshi F, Trent VS, Ramirez NC. Placenta accreta: mild cases diagnosed by placental examination. In J Gynecol Pathol 1996; 15 (01) 28-33
  • 52 Khong TY, Cramer SF, Heller DS. Chorion laeve accreta - Another manifestation of morbid adherence. Placenta 2018; 74: 32-35
  • 53 Mayhew TM. Taking tissue samples from the placenta: an illustration of principles and strategies. Placenta 2008; 29 (01) 1-14
  • 54 Baergen RN. Manual of Benirschke and Kaufmann's Pathology of the Human Placenta. New York, NY: Springer; 2005