Decidual vasculopathy and spiral artery remodeling revisited II: relations to trophoblastic dependent and independent vascular transformation

References

• Benirschke K, Burton GJ, Baergen RN. Pathology of the human placenta. 6th ed.New York (NY): Springer; 2012.
   Google Scholar
• Zeek PM, Assali NS. Vascular changes in the decidua associated with eclamptogenic toxemia of pregnancy. Am J Clin Pathol. 1950;20(12):1099–1109.
   PubMed Web of Science ®Google Scholar
• Hunt HF, Patterson WB, Nicodemus RE. Placental infarction and eclampsia. Am J Clin Pathol. 1940;10(5):319–331.
   Google Scholar
• Robertson WB, Brosens I, Dixon HG. The pathological response of the vessels of the placental bed to hypertensive pregnancy. J Pathol Bacteriol. 1967;93(2):581–592.
   PubMedGoogle Scholar
• Bartholomew RA, Kracke RR. The probable role of the hypercholesteremia of pregnancy in producing vascular changes in the placenta, predisposing to placental infarction and eclampsia. Am J Obstet Gynecol. 1936;31(4):549–562.
   Google Scholar
• 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(7):698–713.
   PubMed Web of Science ®Google Scholar
• Hertig A. Vascular pathology in the hypertensive albuminuric toxemias of pregnancy. Clinics. 1945;4:602–614.
   Google Scholar
• Khong TY, Wolf F, Robertson WB, et al. Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational age infants. BJOG. 1986;93(10):1049–1059.
   Web of Science ®Google Scholar
• Zhang P, Schmidt M, Cook L. Maternal vasculopathy and histologic diagnosis of preeclampsia: poor correlation of histologic changes and clinical manifestation. Am J Obstet Gynecol. 2006;194(4):1050–1056.
   PubMed Web of Science ®Google Scholar
• Chan JS, Heller DS, Baergen RN. Decidual vasculopathy: placental location and association with ischemic lesions. Pediatr Dev Pathol. 2017;20(1):44–48.
   PubMed Web of Science ®Google Scholar
• Taylor R, Roberts JM, Cunningham F, et al. Chesley’s hypertensive disorders in pregnancy. 4th ed. Academic Press; 2014.
   Google Scholar
• Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol. 1967;93(2):569–579.
   PubMedGoogle Scholar
• Kim YM, Chaemsaithong P, Romero R, et al. The frequency of acute atherosis in normal pregnancy and preterm labor, preeclampsia, small-for-gestational age, fetal death and midtrimester spontaneous abortion. J Matern Fetal Neonatal Med. 2015;28(17):2001–2009.
   PubMed Web of Science ®Google Scholar
• Pijnenborg R, Vercruysse L, Hanssens M, et al. Endovascular trophoblast and preeclampsia: a reassessment. Preg Hypertens. 2011;1(1):66–71.
   Web of Science ®Google Scholar
• Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. 2006;27(9–10):939–958.
   PubMed Web of Science ®Google Scholar
• Zhang P. CD56 expression of intravascular trophoblasts defines a class of vasculopathy in preeclampsia and other pregnancy complications. Fetal Pediatr Pathol. 2018. In press.
   Google Scholar
• Kam EP, Gardner L, Loke YW, et al. The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod. 1999;14(8):2131–2138.
   PubMed Web of Science ®Google Scholar
• Pröll J, Blaschitz A, Hartmann M, et al. Human first-trimester placenta intra-arterial trophoblast cells express the neural cell adhesion molecule. Early Preg. 1996;2(4):271–275.
   PubMedGoogle Scholar
• Kim YM, Chaemsaithong P, Romero R, et al. Placental lesions associated with acute atherosis. J Matern Fetal Neonatal Med. 2015;28(13):1554–1562.
   PubMed Web of Science ®Google Scholar
• Staff AC, Dechend R, Pijnenborg R. Learning from the placenta: acute atherosis and vascular remodeling in preeclampsia-novel aspects for atherosclerosis and future cardiovascular health. Hypertension. 2010;56(6):1026–1034.
   PubMed Web of Science ®Google Scholar
• Craven CM, Morgan T, Ward K. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta. 1998;19(4):241–252.
   PubMed Web of Science ®Google Scholar
• Robson A, Harris LK, Innes BA, et al. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 2012;26(12):4876–4885.
   PubMed Web of Science ®Google Scholar
• Labarrere CA, DiCarlo HL, Bammerlin E, et al. Failure of physiologic transformation of spiral arteries, endothelial and trophoblast cell activation, and acute atherosis in the basal plate of the placenta. Am J Obstet Gynecol. 2017;216(3):287.e1–287.e16.
   PubMed Web of Science ®Google Scholar
• Zhang P. Decidual vasculopathy in preeclampsia and spiral artery remodeling revisited: shallow invasion versus failure of involution. AJP Rep. 2018;8(4):e241–e246.
   PubMed Web of Science ®Google Scholar
• Roberts VHJ, Morgan TK, Bednarek P, et al. Early first trimester uteroplacental flow and the progressive disintegration of spiral artery plugs: new insights from contrast-enhanced ultrasound and tissue histopathology. Hum Reprod. 2017;32(12):2382–2393.
   PubMed Web of Science ®Google Scholar
• Whitley GS, Dash PR, Ayling LJ, et al. Increased apoptosis in first trimester extravillous trophoblasts from pregnancies at higher risk of developing preeclampsia. Am J Pathol. 2007;170(6):1903–1909.
   PubMed Web of Science ®Google Scholar
• Liu D, Shao X, Danyalov A, et al. Human placenta blood flow during early gestation with pseudocontinuous arterial spin labeling MRI. J Magn Reson Imaging. 2019. DOI:https://doi.org/10.1002/jmri.26944. [Epub ahead of print].
   Google Scholar
• Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy. N Engl J Med. 2001;345(19):1400–1408.
   PubMed Web of Science ®Google Scholar
• Guzeloglu-Kayisli O, Basar M, Arici A. Basic aspects of implantation. Reprod Biomed Online. 2007;15(6):728–739.
   PubMed Web of Science ®Google Scholar
• Damsky CH, Fitzgerald ML, Fisher SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J Clin Invest. 1992;89(1):210–222.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Fisher SJ, Janatpour M, et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J Clin Invest. 1997;99(9):2139–2151.
   PubMed Web of Science ®Google Scholar
• Ueda M, Sato Y, Horie A, et al. Endovascular trophoblast expresses CD59 to evade complement-dependent cytotoxicity. Mol Cell Endocrinol. 2019;490:57–67.
   PubMed Web of Science ®Google Scholar
• Labarrere CA. Acute atherosis. A histopathological hallmark of immune aggression? Placenta. 1988;9(1):95–108.
   PubMed Web of Science ®Google Scholar
• Smith SD, Dunk CE, Aplin JD, et al. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am J Pathol. 2009;174(5):1959–1971.
   PubMed Web of Science ®Google Scholar
• Hazan AD, Smith SD, Jones RL, et al. Vascular–leukocyte interactions: mechanisms of human decidual spiral artery remodeling in vitro. Am J Pathol. 2010;177(2):1017–1030.
   PubMed Web of Science ®Google Scholar
• Dunk C, Kwan M, Hazan A, et al. Failure of decidualization and maternal immune tolerance underlies uterovascular resistance in intra uterine growth restriction. Front Endocrinol (Lausanne). 2019;10:160.
   PubMed Web of Science ®Google Scholar
• Redline RW, Zaragoza M, Hassold T. Prevalence of developmental and inflammatory lesions in nonmolar first-trimester spontaneous abortions. Hum Pathol. 1999;30(1):93–100.
   PubMed Web of Science ®Google Scholar
• Khong TY, Liddell HS, Robertson WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. BJOG. 1987;94(7):649–655.
   Google Scholar
• Rushton DI. Simplified classification of spontaneous abortions. J Med Genet. 1978;15(1):1–9.
   PubMed Web of Science ®Google Scholar
• Winn VD, Haimov-Kochman R, Paquet AC, et al. Gene expression profiling of the human maternal-fetal interface reveals dramatic changes between midgestation and term. Endocrinology. 2007;148(3):1059–1079.
   PubMed Web of Science ®Google Scholar
• Harris LK, Smith SD, Keogh RJ, et al. Trophoblast- and vascular smooth muscle cell-derived MMP-12 mediates elastolysis during uterine spiral artery remodeling. Am J Pathol. 2010;177(4):2103–2115.
   PubMed Web of Science ®Google Scholar
• Harris LK, Benagiano M, D’Elios MM, et al. Placental bed research: II. Functional and immunological investigations of the placental bed. Am J Obstet Gynecol. 2019;221(5):457–469.
   PubMed Web of Science ®Google Scholar
• Toth P, Li X, Rao CV, et al. Expression of functional human chorionic gonadotropin/human luteinizing hormone receptor gene in human uterine arteries. J Clin Endocrinol Metab. 1994;79(1):307–315.
   PubMed Web of Science ®Google Scholar
• Toth P, Lukacs H, Gimes G, et al. Clinical importance of vascular LH/hCG receptors—a review. Reprod Biol. 2001;1(2):5–11.
   PubMedGoogle Scholar
• Lei ZM, Reshef E, Rao V. The expression of human chorionic gonadotropin/luteinizing hormone receptors in human endometrial and myometrial blood vessels. J Clin Endocrinol Metab. 1992;75(2):651–659.
   PubMed Web of Science ®Google Scholar