The role of the placenta in the development of neonatal brain lesions

1. Robbins J.R., Bakardjiev A.I. Pathogens and the placental fortress. Curr. Opin. Microbiol. 2012; 15(1): 36-43. https://dx.doi.org/10.1016/j.mib.2011.11.006.
2. DeBonis M., Torricelli M., Severi F.M., Luisi S., DeLeo V., Petraglia F. Neuroendocrine aspects of placenta and pregnancy. Gynecol. Endocrinol. 2012; 28 (Suppl. 1): 22-6. https://dx.doi.org/10.3109/09513590.2012.651933.
3. Burton G.J., Fowden A.L. The placenta: a multifaceted, transient organ. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2015; 370(1663): 20140066.https://dx.doi.org/10.1098/rstb.2014.0066.
4. Щеголев А.И., Серов В.Н. Клиническая значимость поражений плаценты. Акушерство и гинекология. 2019; 3: 54-62. [Shchegolev A.I., Serov V.N. Clinical significance of placental lesions. Obstetrics and Gynecology. 2019; (3): 54-62. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.3.54-62.
5. Щеголев А.И. Современная морфологическая классификация повреждений плаценты. Акушерство и гинекология. 2016; 4: 16-23. [Shchegolev A.I. Current morphological classification of damages to the placenta. Obstetrics and Gynecology. 2016; (4): 16-23. (in Russian)] http://dx.doi.org/10.18565/aig.2016.4.16-23.
6. Щеголев А.И., Дубова Е.А., Павлов К.А. Морфология плаценты. М.; 2010. 46c. [Shchegolev A.I., Dubova E.A., Pavlov K.A. The morphology of the placenta. Moscow; 2010. 46p. (in Russian)].
7. Meekins J.W., Pijnenborg R., Hanssens M., McFadyen I.R., vanAsshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 1994; 101(8): 669-74.https://dx.doi.org/10.1111/j.1471-0528.1994.tb13182.x.
8. Maynard S.E., Min J., Merchan J., Lim K., Li J., Mondal S. et al. Excess placental soluble fms-like tyrosine kinase (sFlt-1) may contribute to endothelial dysfunction, hypertension and proteinuria in preeclampsia. J. Clin. Invest. 2003; 111(5): 649-58. https://dx.doi.org/10.1172/JCI17189.
9. Gaffney G., Sellers S., Flave U., Squier M., Johnson A. Case-control study of intrapanum care, cerebral palsy and perinatal death. BMJ. 1994; 308(6931): 743-50. https://dx.doi.org/10.1136/bmj.308.6931.743.
10. Topp M., Langhorr-Roos J., Ulddll P., Kristensen J. Intrauterine growth and gestational age in preterm infants with cerebral palsy. Early Hum. Dev. 1996; 44(1): 27-36. https://dx.doi.org/10.1016/0378-3782(96)82791-5.
11. Walker C.K., Krakowiak P., Baker A., Hansen R.L., Ozonoff S., Hertz-Picciotto I. Preeclampsia, placental insufficiency, and autism spectrum disorder or developmental delay. JAMA Pediatr. 2015; 169(2): 154-62.https://dx.doi.org/10.1001/jamapediatrics.2014.2645.
12. Gumusoglu S.B., Chilukuri A.S.S., Santillan D.A., Santillan M.K., Stevens H.E. Neurodevelopmental outcomes of prenatal preeclampsia exposure. Trends Neurosci. 2020; 43(4): 253-68. https://dx.doi.org/10.1016/j.tins.2020.02.003.
13. Alexander B.T., Bennett W.A., Khalil R.A., Granger J.P. Preeclampsia: linking placental ischemia with cardiovascular-renal dysfunction. News Physiol. Sci. 2001; 16: 282-6. https://dx.doi.org/10.1152/physiologyonline.2001.16.6.282.
14. Murphy D.J., Sellers S., MacKenzie I.Z., Yudkin P.L., Johnson A.M. Case-control study of antenatal and intrapartum risk factors for cerebral palsy in very preterm singleton babies. Lancet. 1995; 346(8988): 1449-54. https://dx.doi.org/10.1016/s0140-6736(95)92471-x.
15. Schlapbach L.J., Ersch J., Adams M., Bernet V., Bucher H.U., Latal B. Impact of chorioamnionitis and preeclampsia on neurodevelopmental outcome in preterm infants below 32 weeks gestational age. Acta Paediatr. 2010; 99(10): 1504-9. https://dx.doi.org/10.1111/j.1651-2227.2010.01861.x.
16. Collins M., Paneth N. Preeclampsia and cerebral palsy: are they related? Dev. Med. Child Neurol. 1998; 40(3): 207-11. https://dx.doi.org/10.1111/j.1469-8749.1998.tb15449.x.
17. Shchyogolev A.I., Dubova E.A., Pavlov K.A., Lyapin V.M., Kulikova G.V., Shmakov R.G. Morphometric characteristics of terminal villi of the placenta in pre-eclampsia. Bull. Exp. Biol. Med. 2012; 154(1): 92-5. https://dx.doi.org/10.1007/s10517-012-1883-5.
18. Redline R.W., Minich N., Taylor H.G., Hack M. Placental lesions as predictors of cerebral palsy and abnormal neurocognitive function at school age in extremely low birth weight infants (<1 kg). Pediatr. Dev. Pathol. 2007; 10(4): 282-92. https://dx.doi.org/10.2350/06-12-0203.1.
19. Burke C.J., Tannenberg A.E. Prenatal brain damage and placental infarction--an autopsy study. Dev. Med. Child Neurol. 1995; 37(6): 555-62.https://dx.doi.org/10.1111/j.1469-8749.1995.tb12042.x.
20. Nielsen L., Schendel D., Grove J., Hvidtjørn D., Jacobsson B., Josiassen T. et al. Asphyxia-related risk factors and their timing in spastic cerebral palsy. BJOG. 2008; 115(12): 1518-28. https://dx.doi.org/10.1111/j.1471-0528.2008.01896.x.
21. Blair E., de Groot J., Nelson K.B. Placental infarction identified by macroscopic examination and risk of cerebral palsy in infants at 35 weeks of gestational age and over. Am. J. Obstet. Gynecol. 2011; 205(2): 124.e1-7.https://dx.doi.org/10.1016/j.ajog.2011.05.022.
22. Tikkanen M. Placental abruption: epidemiology, risk factors and consequences. Acta Obstet. Gynecol. Scand. 2011; 90(2): 140-9. https://dx.doi.org/10.1111/j.1600-0412.2010.01030.x.
23. Downes K.L., Grantz K.L., Shenassa E.D. Maternal, labor, delivery, and perinatal outcomes associated with placental abruption: a systematic review. Am. J. Perinatol. 2017; 34(10): 935-57. https://dx.doi.org/10.1055/s-0037-1599149.
24. Всемирная организация здравоохранения. Международная статистическая классификация болезней и проблем, связанных со здоровьем. 10-й пересмотр. М.: Медицина; 2003. т. 2. 180с. [World Health Organization. International Statistical Classification of Diseases and Related Health Problems. 10th revision. Moscow: Medicine; 2003. vol. 2. 180p. (in Russian)].
25. Щеголев А.И., Туманова У.Н., Шувалова М.П. Преждевременная отслойка плаценты в генезе мертворождения. Международный журнал прикладных и фундаментальных исследований. 2016; 7(4): 575-9. [Shchegolev A.I., Tumanova U.N., Shuvalova M.P. Premature abruptio placentae as the cause of stillbirth. International Journal of Applied and Basic Research. 2016;7(4): 575-9. (in Russian)].
26. Туманова У.Н., Шувалова М.П., Щеголев А.И. Отслойка плаценты и ранняя неонатальная смертность (по данным Росстата в 2010-2016 годах). Международный журнал прикладных и фундаментальных исследований. 2018; 4: 86-90. [Tumanova U.N., Shuvalova M.P., Shchegolev A.I. Abruptio placentae and early neonatal mortality (according to Rosstat in 2012–2016). International Journal of Applied and Basic Research. 2018; (4): 86-90.(in Russian)].
27. Kayani S.I., Walkinshaw S.A., Preston C. Pregnancy outcome in severe placental abruption. BJOG. 2003; 110(7): 679-83.
28. Pariente G., Wainstock T., Walfisch A., Landau D., Sheiner E. Placental abruption and long-term neurological hospitalisations in the offspring. Paediatr. Perinat. Epidemiol. 2019; 33(3): 215-22. https://dx.doi.org/10.1111/ppe.12553.
29. Ichizuka K., Toyokawa S., Ikenoue T., Satoh S., Hasegawa J., Ikeda T. et al. Risk factors for cerebral palsy in neonates due to placental abruption. J. Obstet. Gynaecol. Res. 2021; 47(1): 159-66. https://dx.doi.org/10.1111/jog.14447.
30. Nasiell J., Papadogiannakis N., Leof E., Elofsson F., Hallberg B. Hypoxic ischemic encephalopathy in newborns linked to placental and umbilical cord abnormalities. J. Matern. Fetal Neonatal Med. 2016; 29(5): 721-6.https://dx.doi.org/10.3109/14767058.2015.1015984.
31. Gonen N., Levy M., Kovo M., Schreiber L., Noy L.K., Volpert E. et al. Placental histopathology and pregnancy outcomes in "early" vs. "late" placental abruption. Reprod. Sci. 2021; 28(2): 351-60. https://dx.doi.org/10.1007/s43032-020-00287-3.
32. Spinillo A., Fazzi E., Stronati M., Ometto A., Capuzzo E., Guaschino S. Early morbidity and neurodevelopmental outcome in low-birthweight infants born after third trimester bleeding. Am. J. Perinatol. 1994; 11(2): 85-90.https://dx.doi.org/10.1055/s-2007-994562.
33. Parc E., Benin A., Lecarpentier E., Goffinet F., Lepercq J. Risk factors for hypoxic-ischemic encephalopathy or neonatal death in placental abruption. J. Gynecol. Obstet. Hum. Reprod. 2023; 52(1): 102498. https://dx.doi.org/10.1016/j.jogoh.2022.102498.
34. Furukawa S., Doi K., Furuta K., Sameshima H. The effect of placental abruption on the outcome of extremely premature infants. J. Matern. Neonatal Med. 2015; 28(6): 705-8. https://dx.doi.org/10.3109/14767058.2014.929109.
35. Oltean I., Rajaram A., Tang K., MacPherson J., Hondonga T., Rishi A. et al. The association of placental abruption and pediatric neurological outcome: a systematic review and meta-analysis. J. Clin. Med. 2022; 12(1): 205.https://dx.doi.org/10.3390/jcm12010205.
36. Redline R.W. Classification of placental lesions. Am. J. Obstet. Gynecol. 2015; 213(4, Suppl.): S21-8. https://dx.doi.org/10.1016/j.ajog.2015.05.056.
37. Gruenwald P. Abnormalities of placental vascularity in relation to intrauterine deprivation and retardation of fetal growth: Significance of avascular chorionic villi. N. Y. State J. Med. 1961; 61: 1508-13.
38. Kraus F.T., Acheen V.I. Fetal thrombotic vasculopathy in the placenta: cerebral thrombi and infarcts, coagulopathies, and cerebral palsy. Hum. Pathol. 1999; 30(7): 759-69. https://dx.doi.org/10.1016/s0046-8177(99)90136-3.
39. Cheong J.L., Cowan F.M. Neonatal arterial ischaemic stroke: obstetric issues. Semin. Fetal Neonatal Med. 2009; 14(5): 267-71. https://dx.doi.org/10.1016/j.siny.2009.07.009.
40. Geraldo A.F., Parodi A., Bertamino M., Buffelli F., Uccella S., Tortora D. et al. Perinatal arterial ischemic stroke in fetal vascular malperfusion: A case series and literature review. AJNR Am. J. Neuroradiol. 2020; 41(12): 2377-83.https://dx.doi.org/10.3174/ajnr.A6857.
41. Vik T., Redline R., Nelson K.B., Bjellmo S., Vogt C., Ng P. et al. The placenta in neonatal encephalopathy: A case-control study. J. Pediatr. 2018; 202: 77-85.e3. https://dx.doi.org/10.1016/j.jpeds.2018.06.005.
42. Redline R.W. Severe fetal placental vascular lesions in term infants with neurologic impairment. Am. J. Obstet. Gynecol. 2005; 192(2): 452-7.https://dx.doi.org/10.1016/j.ajog.2004.07.030.
43. Chen S., Shenoy A. Placental pathology and the developing brain. Semin. Pediatr. Neurol. 2022; 42: 100975. https://dx.doi.org/10.1016/j.spen.2022.100975.
44. McDonald D.G., Kelehan P., McMenamin J.B., Gorman W.A., Madden D., Tobbia I.N. et al. Placental fetal thrombotic vasculopathy is associated with neonatal encephalopathy. Hum. Pathol. 2004; 35(7): 875-80.https://dx.doi.org/10.1016/j.humpath.2004.02.014.
45. Mir I.N., Johnson-Welch S.F., Nelson D.B., Brown L.S., Rosenfeld C.R., Chalak L.F. Placental pathology is associated with severity of neonatal encephalopathy and adverse developmental outcomes following hypothermia. Am. J. Obstet. Gynecol. 2015; 213(6): 849.e1-7. https://dx.doi.org/10.1016/j.ajog.2015.09.072.
46. Grether J.K., Nelson K.B. Maternal infection and cerebral palsy in infants of normal birth weight. JAMA. 1997; 278(3): 207-11.
47. Pappas A., Kendrick D.E., Shankaran S., Stoll B.J., Bell E.F., Laptook A.R. et al. Chorioamnionitis and early childhood outcomes among extremely low-gestational-age neonates. JAMA Pediatr. 2014; 168(2): 137-47.https://dx.doi.org/10.1001/jamapediatrics.2013.4248.
48. Shatrov J.G., Birch S.C.M., Lam L.T., Quinlivan J.A., McIntyre S., Mendz G.L. Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet. Gynecol. 2010; 116(2, Pt. 1): 387-92. https://dx.doi.org/10.1097/AOG.0b013e3181e90046.
49. Salas A.A., Faye-Petersen O.M., Sims B., Peralta-Carcelen M., Reilly S.D., McGwin G. Jr. et al. Histological characteristics of the fetal inflammatory response associated with neurodevelopmental impairment and death in extremely preterm infants. J. Pediatr. 2013; 163(3): 652-7.e1-2.https://dx.doi.org/10.1016/j.jpeds.2013.03.081.
50. Alexander J.M., Gilstrap L.C., Cox S.M., McIntire D.M., Leveno K.J. Clinical chorioamnionitis and the prognosis for very low birth weight infants. Obstet. Gynecol. 1998; 91(5, Pt. 1): 725-9. https://dx.doi.org/10.1016/s0029-7844(98)00056-8.
51. Soraisham A.S., Singhal N., McMillan D.D., Sauve R.S., Lee S.K.; Canadian Neonatal Network. A multicenter study on the clinical outcome of chorioamnionitis in preterm infants. Am. J. Obstet. Gynecol. 2009; 200(4): 372.e1-6. https://dx.doi.org/10.1016/j.ajog.2008.11.034.
52. Liu Z., Tang Z., Li J., Yang Y. Effects of placental inflammation on neonatal outcome in preterm infants. Pediatr. Neonatol. 2014; 55(1): 35-40.https://dx.doi.org/10.1016/j.pedneo.2013.05.007.
53. Andrews W.W., Goldenberg R.L., Faye-Petersen O., Cliver S., Goepfert A.R., Hauth J.C. The Alabama Preterm Birth study: polymorphonuclear and mononuclear cell placental infiltrations, other markers of inflammation, and outcomes in 23- to 32-week preterm newborn infants. Am. J. Obstet. Gynecol. 2006; 195(3): 803-8. https://dx.doi.org/10.1016/j.ajog.2006.06.083.
54. Dexter S.C., Malee M.P., Pinar H., Hogan J.W., Carpenter M.W., Vohr B.R.Influence of chorioamnionitis on developmental outcome in very low birth weight infants. Obstet. Gynecol. 1999; 94(2): 267-73. https://dx.doi.org/10.1016/s0029-7844(99)00319-1.
55. Arayici S., Kadioglu Simsek G., Oncel M.Y., Eras Z., Canpolat F.E.,Oguz S.S. et al. The effect of histological chorioamnionitis on the short-term outcome of preterm infants ≤32 weeks: a single-center study. J. Matern. Fetal Neonatal Med. 2014; 27(11): 1129-33. https://dx.doi.org/10.3109/14767058.2013.850668.
56. Ylijoki M., Ekholm E., Haataja L., Lehtonen L. Is chorioamnionitis harmful for the brain of preterm infants? A clinical overview. Acta Obstet. Gynecol. Scand. 2012; 91(4): 403-19. https://dx.doi.org/10.1111/j.1600-0412.2012.01349.x.
57. Freedman A.A., Miller G.E., Ernst L.M. Chronic villitis: Refining the risk ratio of recurrence using a large placental pathology sample. Placenta. 2021; 112: 135-40. https://dx.doi.org/10.1016/j.placenta.2021.07.298.
58. Devisme L., Chauvière C., Franquet-Ansart H., Chudzinski A., Stichelbout M., Houfflin-Debarge V. et al. Perinatal outcome of placental massive perivillous fibrin deposition: a case-control study. Prenat. Diagn. 2017; 37(4): 323-8. https://dx.doi.org/10.1002/pd.5013.
59. Adams-Chapman I., Vaucher Y.E., Bejar R.F., Benirschke K., Baergen R.N., Moore T.R. Maternal floor infarction of the placenta: association with central nervous system injury and adverse neurodevelopmental outcome. J. Perinatol. 2002; 22(3): 236-41. https://dx.doi.org/10.1038/sj.jp.7210685.
60. Fuke Y., Aono T., Imai S., Suehara N., Fujita T., Nakayama M. Clinical significance and treatment of massive intervillous fibrin deposition associated with recurrent fetal growth retardation. Gynecol. Obstet. Invest. 1994; 38(1): 5-9.https://dx.doi.org/10.1159/000292434.
61. Redline R.W., O'Riordan M.A. Placental lesions associated with cerebral palsy and neurologic impairment following term birth. Arch. Pathol. Lab. Med. 2000; 124(12): 1785-91. https://dx.doi.org/10.5858/2000-124-1785-PLAWCP.
62. Cohen M.C., Peres L.C., Al-Adnani M., Zapata-Vázquez R. Increased number of fetal nucleated red blood cells in the placentas of term or near-term stillborn and neonates correlates with the presence of diffuse intradural hemorrhage in the perinatal period. Ped. Develop. Pathol. 2014; 17(1): 1-9.https://dx.doi.org/10.2350/12-02-1157-OA.1.
63. Щеголев А.И., Туманова У.Н., Ляпин В.М. Извитость пуповины: определение, классификация, клиническое значение. Акушерство и гинекология. 2019; 2: 42-50. [Shchegolev A.I., Tumanova U.N., Lyapin V.M. Umbilical cord coiling: definition, classification, clinical significance. Obstetrics and Gynecology. 2019; (2): 42-50. (in Russian)]. https://dx.doi.org/10.18565/aig.2019.2.42-50.
64. Maynard S.E., Karumanchi S.A. Angiogenic factors and preeclampsia. Semin. Nephrol. 2011; 31(1): 33-46. https://dx.doi.org/10.1016/j.semnephrol.2010.10.004.
65. Павлов К.А., Дубова Е.А., Щеголев А.И. Фетоплацентарный ангиогенез при нормальной беременности: роль плацентарного фактора роста и ангиопоэтинов. Акушерство и гинекология. 2010; 6: 10-5. [Pavlov K.A., Dubova E.A., Shchegolev A.I. Fetoplacental angiogenesis during normal pregnancy: a role of placental growth factor and angiopoietins. Obstetrics and Gynecology. 2010; (6): 10-5. (in Russian)].
66. Dubova E.A., Pavlov K.A., Lyapin V.M., Shchyogolev A.I., Sukhikh G.T. Vascular endothelial growth factor and its receptors in the placental villi of pregnant patients with pre-eclampsia. Bull. Exp. Biol. Med. 2013; 154(6): 792-5.https://dx.doi.org/10.1007/s10517-013-2058-8.
67. Dubova E.A., Pavlov K.A., Lyapin V.M., Kulikova G.V., Shchyogolev A.I., Sukhikh G.T. Expression of insulin-like growth factors in the placenta in preeclampsia. Bull. Exp. Biol. Med. 2014; 157(1): 103-7.https://dx.doi.org/10.1007/s10517-014-2502-4.
68. Щеголев А.И., Ляпин В.М., Туманова У.Н., Воднева Д.Н., Шмаков Р.Г. Гистологические изменения плаценты и васкуляризация ее ворсин при ранней и поздней преэклампсии. Архив патологии. 2016; 78(1): 13-8. [Shchegolev A.I., Lyapin V.M., Tumanova U.N., Vodneva D.N., Shmakov R.G. Histological hanges in the placenta and vascularization of its villi in early- and late-onset preeclampsia. Arkhiv Patologii. 2016; 78(1): 13-8.(in Russian)]. https://dx.doi.org/10.17116/patol201678113-18.
69. Aouache R., Biquard L., Vaiman D., Miralles F. Oxidative stress in preeclampsia and placental diseases. Int. J. Mol. Sci. 2018; 19(5): 1496.https://dx.doi.org/10.3390/ijms19051496.
70. Щеголев А.И., Туманова У.Н., Серов В.Н. Поражения плаценты у беременных с SARS-CoV-2-инфекцией. Акушерство и гинекология. 2020; 12: 44-52. [Shchegolev A.I., Tumanova U.N., Serov V.N. Placental lesions in pregnant women with SARS-CoV-2 infection. Obstetrics and Gynecology. 2020; (12): 44-52. (in Russian)]. https://dx.doi.org/10.18565/aig.2020.12.
71. Щеголев А.И., Туманова У.Н., Чаусов А.А., Шувалова М.П. Мертворождение в Российской Федерации в 2020 году (год пандемии COVID-19). Акушерство и гинекология. 2022; 11: 131-40. [Shchegolev A.I., Tumanova U.N., Chausov A.A., Shuvalova M.P. Stillbirths in the Russian Federation in 2020 (COVID-19 pandemic year). Obstetrics and Gynecology. 2022; (11): 131-40. (in Russian)]. https://dx.doi.org/10.18565/aig.2022.11.131-140.
72. Benny M., Bandstra E.S., Saad A.G., Lopez-Alberola R., Saigal G., Paidas M.J. et al. Maternal SARS-CoV-2, placental changes and brain injury in 2 neonates. Pediatrics. 2023; 151(5): e2022058271. https://dx.doi.org/10.1542/peds.2022-058271.

Received 08.08.2023

Accepted 23.08.2023