Comparative morphological characteristics of the uteroplacental area in abnormal placentation

The aim. To carry out a comparative morphological characteristic of the uteroplacental area with abnormal placentation – pl. accreta, pl. increta, pl. percreta.

Materials and methods. The study included 47 patients with atypical placentation; the comparison group included 10 healthy pregnant women with uterine scar after a previous caesarean section. A histological study of uteroplacental area samples was performed with hematoxylin and eosin, methylene blue staining. An immunohistochemical study with primary antibodies to cytokeratin 7 (CK7), Hif2a, vascular endothelial growth factor, α-SMA was carried out. The differences between the compared values were considered to be statistically significant at p < 0.05.

The results of the study. Pl. accreta was determined in 12 (25.5 %), pl. increta – in 30 (63.9 %), pl. percreta – in 5 (10.6 %) patients. In all patients of the main group, the decidua was completely or partially absent in the area of abnormal placentation or was replaced by an uneven layer of fetal fibrinoid. Cases when placental villi unevenly penetrated into the thickness of myometrium in the form of “tongues” or “coves” bordered by fetal fibrinoid and often located intermuscularly were defined as pl. increta (n = 26). Cases with the placental villi ingrowth to the serous membrane were considered as pl.  percreta (n  =  5). In cases with deep variants of  ingrowth (pl. increta and pl. percreta) (n = 31), the villi were visualized in the lumen of the vessels and the thinning of the lower uterine segment with the presence of stretched muscle bundles was revealed. Aseptic necrosis of  the myometrium was  found: in 2 (16.7 %) of 12 women with pl. accreta, in 26 (86.7 %) of 30 women with pl. increta and in 5 (100 %) women with pl. percreta. There were no areas of necrosis in the myometrium of the women of comparison group.

Conclusion. The appearance and increase of myometrial necrosis zones in response to an increase in the depth of placental villus ingrowth were detected. Myometrial necrosis zones could be the cause of activation of angiogenic factors and an important stimulus for the development of abnormal vascularization in placenta accreta spectrum.

1. Balayla J, Bondarenko HD. Placenta accreta and the risk of adverse maternal and neonatal outcomes. J Perinat Med. 2013; 41(2): 141-149. doi: 10.1515/jpm-2012-0219

2. Morlando M, Sarno L, Napolitano R, Capone A, Tessitore G, Maruotti G, et al. Placenta accreta: Incidence and risk factors in an area with a particularly high rate of cesarean section. Acta Obstet Gynecol Scand. 2013; 92(4): 457-460. doi: 10.1111/aogs.12080

3. Brennan K. Placental pathology: A review of placenta previa, placental abruption and placenta accretа. Update Anaest. 2019; 34: 51-55. doi: 10.1029/WFSA-D-18-00010

4. Solheim KN, Esakoff TF, Little SE, Cheng YW, Sparks TN, Caughey AB. The effect of cesarean delivery rates on the future incidence of placenta previa, placenta accreta, and maternal mortality. J Matern Fetal Neonatal Med. 2011; 24: 1341-1346. doi: 10.3109/14767058.2011.553695

5. Jauniaux E, Chantraine F, Silver RM, Langhoff‐Roos J; for the FIGO Placenta Accreta Diagnosis and Management Expert Consensus Panel. FIGO consensus guidelines on placenta accreta spectrum disorders: Epidemiology. IntJ Gynecol Obstet. 2018; 140(3): 265-273. doi: 10.1002/ijgo.12407

6. Jauniaux E, Ayres-de-Campos D, Langhoff-Roos J, Fox KA, Collins S. FIGO Placenta Accreta Diagnosis and Management Expert Consensus Panel FIGO classification for the clinical diagnosis of placenta accreta spectrum disorders. IntJ Gynecol Obstet. 2019; 146(1): 20-24. doi: 10.1002/ijgo.12761

7. Kolesnikov LL, Shevlyuk NN, Erofeeva LM. (eds). Terminologia Embriologica. International terms for human embryology with the official list of Russian equivalents. Moscow: GEOTAR-Media; 2014. (In Russ.).

8. Markaryan NM, Vandysheva RA, Nizyaeva NV, Gioeva ZV, Mikhalev SA, Khamoshina MB, et al. Clinical and morphological assessment of uterine scars after cesarean sec-tion in patients with gynecological and extragenital diseases. Clinical and Experimental Morphology. 2023; 12(1): 34-45. (In Russ.). doi: 10.31088/CEM2023.12.1.34-45

9. Milovanov AP, Aksenenko VA, Lukashevich AA, Fokina TV, Stepanova II, Tikhonova NB. The leading role of scars after the caesarian section in the pathogenesis of placenta previa accreta. Clinical and Experimental Morphology. 2019; 8(1): 10-18. (In Russ.). doi: 10.31088/2226-5988-2019-29-1-10-18

10. Benirschke K, Burton GJ, Baergen R. Pathology of the human placenta; 6th ed. Berlin, Heidelberg: Springer-Verlag; 2012.

11. Lisitsyna OI, Nizyaeva NV, Mikheeva AA. Placenta increta: Evolution of knowledge and skills. Obstetrics andGynegology. 2021; 6: 34-40. (In Russ.). doi: 10.18565/aig.2021.6.34-40

12. World Medical Association Declaration of Helsinki – Ethical principles for medical research involving human subjects. 2013. URL: https://www.wma.net/policies-post/wma-declarationof-helsinki-ethical-principles-for-medical-research-involvinghuman-subjects [date of access: 15.09.2022].

13. On the approval of the rules of clinical practice in the Russian Federation: Order No. 266 of June 19, 2003. (In Russ.). URL: https://normativ.kontur.ru/document?moduleId=1&documentId=61950 [date of access: 15.09.2022].

14. 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; 33(12): 2382-2396. doi: 10.1038/s41379-020-0569-1

15. Kulikov IA, Belousova TN, Sovaev NI, Plakhotina EN, Musaeva SV, Pavlyutina KM, et al. A method of operative delivery of patients with placenta ingrowth into a uterine scar: Patent No. 2706368 of the Russian Federation. 2019. (In Russ.).

16. Moll W. Structure adaptation and blood flow control in the uterine arterial system after hemochorial placentation. Eur J Obstet Gynecol Reprod Biol. 2003; 22(110 Suppl): S19-S27. doi: 10.1016/s0301-2115(03)00169-6

17. Jauniaux E, Ramsay B, Campbell S. Ultrasonographic investigation of placental morphologic characteristics and size during the second trimester of pregnancy. Am J Obstet Gynecol. 1994; 170(1 Pt 1): 130-137. doi: 10.1016/s0002-9378(94)70397-3

18. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta. 2009; 30(6): 473-482. doi: 10.1016/j.placenta.2009.02.009

19. Jauniaux E, Burton GJ. Pathophysiology of placenta accreta spectrum disorders: A review of current findings. Clin Obstet Gynecol. 2018; 61: 743-754. doi: 10.1097/GRF.0000000000 000392

20. Matsumoto L, Hirota Y, Saito-Fujita T, Takeda N, Tanaka T, Hiraoka T, et al. HIF2α in the uterine stroma permits embryo invasion and luminal epithelium detachment. J Clin Invest. 2018; 128(7): 3186-3197. doi: 10.1172/JCI98931

21. Tseng JJ, Chou MM, Hsieh YT, Wen MC, Ho ES, Hsu SL. Differential expression of vascular endothelial growth factor, placenta growth factor and their receptors in placentae from pregnancies complicated by placenta accreta. Placenta. 2006; 27(1): 70-78. doi: 10.1016/j.placenta.2004.12.011

22. Sokolov DI, Belyakova KL, Mikhailova VA, Shilenkova YuV, Khudinyan MM, Okorokova KS, et al. Effects of placental factors upon development of tubular structures by endothelial cells in presence of trophoblastic cells. Medical Immunology (Russia). 2017; 19(3): 285-292. (In Russ.). doi: 10.15789/1563-0625-2017-3-285-292

23. Squires R, Wu B, Tawil B. Fibrin sealant as a delivery vehicle for cells, antibiotics, growth factors, and painkillers. J Appl Biotechnol Bioeng. 2023; 10(2): 56-64. doi: 10.15406/jabb.2023.10.00328

24. Jauniaux E, Hussein AM, Elbarmelgy RM, Elbarmelgy RA, Burton GJ. Failure of placental detachment in accreta placentation is associated with excessive fibrinoid deposition at the uteroplacental interface. Am J Obstet Gynecol. 2022; 226(2): 243.e1-243.e10. doi: 10.1016/j.ajog.2021.08.026

25. Kopeina GS, Zamaraev AV, Zhivotovsky BD, Lavrik IN. Programmed necrosis and tissue regeneration. Genes & Cells. 2018; XIII(2): 35-38. (In Russ.). doi: 10.23868/201808017