Pathogenetic parallels of tumor growth and placental pathological invasion

Kayumova A.V., Melkozerova O.A., Bashmakova N.V., Malgina G.B., Chistyakova G.N.

Ural Research Institute of Maternal and Infant Care, Ministry of Health of the Russian Federation, Yekaterinburg, Russia
Objective: To study current ideas about the pathogenesis of placental pathological invasion according to Russian and foreign literature and to identify parallels between some pathogenetic mechanisms of tumor growth and placental abnormal invasion.
Materials and methods: The keywords “placenta”, “deep placental invasion”, “placenta accreta”, “implantation”, “apoptosis”, “neoangiogenesis”, “mitochondrial dysfunction”, “placenta accreta spectrum”, “placenta percreta”, “placenta increta”, “placenta accreta”, and “epithelial-mesenchymal transition” were used to search for literature sources in the Russian and foreign databases eLibrary, Medline/PubMed, Embase, and Crossref.
Results: Placental pathological invasion is considered as a multifactorial complication of gestation, which has the features of tumor growth, including abnormal neoangiogenesis, apoptosis, uncontrolled proteolysis, and escape from immunological control. The basis for these pathophysiological parallels is the phenomenon of epithelial-mesenchymal transition. The paper presents recent studies demonstrating the role of placental mitochondrial dysfunction in changing the expression of promoter genes that regulate the depth of placental invasion.
Conclusion: The parallels between some pathogenetic mechanisms of tumor growth and placental abnormal invasion, which are identified in this article, can give rise to further in-depth studies of the pathogenesis of this pregnancy complication in order to expand science knowledge of the pathophysiology of deep placenta accreta and to improve models for predicting this pathology to prevent maternal morbidity and mortality.

Keywords

deep placental invasion
placenta accreta
epithelial-mesenchymal transition
implantation
apoptosis
neoangiogenesis
mitochondrial dysfunction

References

  1. Shainker S., Shamshirsaz A., Haviland M., O'Brien K., Redhunt A., Bateni Z. et al. Utilization and outcomes of massive transfusion protocols in women with and without invasive placentation. J. Matern. Fetal Neonatal Med. 2020; 33(21): 3614-8. https://dx.doi.org/10.1080/14767058.2019.1581168.
  2. Лисицына О.И., Низяева Н.В., Михеева А.А. Врастание плаценты. Эволюция знаний и умений. Акушерство и гинекология. 2021; 6: 34-40. [Lisitsyna O.I., Nizyaeva N.V., Mikheeva A.A. Placenta increta: Evolution of knowledge and skills. Obstetrics and Gynecology. 2021; 6: 34-40 (in Russian)]. https://dx.doi.org/10.18565/aig.2021.6.34-40.
  3. D'Antonio F., Palacios-Jaraquemada J., Timor-Trisch I., Cali G. Placenta accreta spectrum disorders: Prenatal diagnosis still lacks clinical correlation. Acta Obstet. Gynecol. Scand. 2018; 97(7): 773-5. https://dx.doi.org/10.1111/aogs.13374.
  4. Гуменюк Е.Г., Рудакова И.С. Врастание плаценты: обзор литературы с обсуждением клинического случая «near miss». Медико-фармацевтический журнал «Пульс». 2020; 22(1): 21-33. [Gumeniuk E.G., Rudakova I.S. Placenta accreta: literature review with discussion of the clinical case «near miss». Medical & pharmaceytical journal «Pulse». 2020; 22(1): 21-33. (in Russian)]. https://dx.doi.org/10.26787/nydha-2686-6838-2020-22-1-21-33.
  5. Баринов С.В., Медянникова И.В., Тирская Ю.И., Безнощенко Г.Б., Кадцына Т.В., Лазарева О.В., Биндюк А.В., Неустроева Т.Н., Степанов С.С. Прогнозирование приращения плаценты при ее предлежании. Акушерство и гинекология. 2021; 1: 61-9. [Barinov S.V., Medyannikova I.V., Tirskaya Yu.I., Beznoshchenko G.B., Kadtsyna T.V., Lazareva O.V., Bindyuk A.V., Neustroeva T.N., Stepanov S.S. Prediction of placenta accreta associated with placenta previa. Obstetrics and Gynecology. 2021; 1: 61-9. (in Russian)]. https://dx.doi.org/10.18565/aig.2021.1.61-69.
  6. Шмаков Р.Г., Пирогова М.М., Васильченко О.Н., Чупрынин В.Д., Ежова Л.С. Хирургическая тактика при врастании плаценты с различной глубиной инвазии. Акушерство и гинекология. 2020; 1: 78-82. [Shmakov R.G., Pirogova M.M., Vasilchenko O.N., Chuprynin V.D., Ezhova L.S. Surgery tactics for placenta increta with different depths of invasion. Obstetrics and Gynecology. 2020; 1: 78-82 (in Russian)]. https:/dx.doi.org/10.18565/aig.2020.1.78-82.
  7. Михеева А.А., Шмаков Р.Г., Рогачевский О.В. Возможности сохранения репродуктивной функции у женщин после органосохраняющих операций при врастании плаценты. Акушерство и гинекология. 2022; 1: 90-6. [Mikheeva A.A., Shmakov R.G., Rogachevskiy O.V., Yarygina T.A., Nizyaeva N.V., Amiraslanov E.Yu. Fertility preservation in women with placenta accrete spectrum undergoing organ-sparing surgery. Obstetrics and Gynecology. 2022; 1: 90-6 (in Russian)]. https://dx.doi.org/10.18565/aig.2022.1.90-96.
  8. Irving C., Hertig A.T. A study of placenta accreta. Surg. Gynecol. Obstet. 1937; 64: 178-200.
  9. Luke R.K., Sharpe J.W., Greene R.R. Placenta accreta: The adherent or invasive placena. Am. J. Obstet. Gynecol. 1966; 95: 660-8.
  10. Silver R.M., Landon M.B., Rouse D.J., Leveno K.J., Spong C.Y., Thom E.A. et al. Maternal morbidity associated with multiple repeat cesarean deliveries. Obstet. Gynecol. 2006; 107(6): 1226-32. https://dx.doi.org/10.1097/01.AOG.0000219750.79480.8432.
  11. Miller W.G. A clinical and pathology study of placenta accrete. J. Obstet. Gynaecol. Br. Emp. 1959; 66: 353-64. https://dx.doi.org/10.1111/j.1471-0528.1959.tb02043.x.
  12. Khong T.Y., Robertson W.B. Placenta creta and placenta praevia creta. Placenta. 1987; 8(4): 399-409. https://dx.doi.org/1010.1016/0143-4004(87)90067-1.
  13. Fox H. Pathology of the placenta. 2nd ed. London: Saunders; 1997. 488p.
  14. Strickland S., Richards W.G. Invasion of the trophoblasts Cell. 1992; 71: 355-7. https://dx.doi.org/10.1016/0092-8674(92)90503-5.
  15. Tantbirojn P., Crum CD., Parast M.M. Pathophysiology of placenta creta: the role of deciduas and extravillous cytotrophoblast. Placenta. 2008; 29(7): 639-45. https://dx.doi.org/10.1016/j.placenta.2008.04.008.
  16. Benirschke K., Kaufmann P. Pathology of the human placenta. 4th ed. New York: Springer; 2000. 947p.
  17. Wehrum M.J., Buhimschi I.A., Salafia C., Thung S., Bahtiyar M.O., Werner E.F. et al. Accreta complicating complete placenta previa is characterized by reduced systemic levels of vascular endothelial growth factor and by epithelial-to-mesenchymal transition of the invasive trophoblast. Am. J. Obstet. Gynecol. 2011; 204(5): 411.e1-411.e11. https://dx.doi.org/10.1016/j.ajog.2010.12.027.
  18. Jauniaux E., Burton G.J. Pathophysiology of placenta accreta spectrum disorders: A review of current findings. Clin. Obstet. Gynecol. 2018; 61(4): 743-54. https://dx.doi.org/10.1097/GRF.0000000000000392.
  19. Kim S.M., Kim J.S. A review of mechanisms of implantation. Dev. Reprod. 2017; 21(4): 351-9. https://dx.doi.org/10.12717/DR.2017.21.4.351.
  20. Governini L., Luongo F.P., Haxhiu A., Piomboni P., Luddi A. Main actors behind the endometrial receptivity and successful implantation. Tissue Cell. 2021; 73: 101656. https://dx.doi.org/10.1016/j.tice.2021.101656.
  21. Jansen C.H.J.R., Kastelein A.W., Kleinrouweler C.E., Leeuwen E.V., Jong K.H., Pajkrt E., Noorden C.J.F., Van Noorden C.J.F. Development of abnormalities in the location and anatomy of the placenta. Acta Obstet. Gynecol. Scand. 2020; 99(8): 983-93. https://dx.doi.org/10.1111/aogs.13834.
  22. Fournier S.B., D'Errico J.N., Stapleton P.A. Uterine vascular control preconception and during pregnancy. Compr. Physiol. 2021; 11(3): 1871-93. https://dx.doi.org/10.1002/cphy.c190015.
  23. Allerkamp H.H., Clark A.R., Lee T.C., Morgan T.K., Burton G.J., James J.L. Something old, something new: digital quantification of uterine vascular remodelling and trophoblast plugging in historical collections provides new insight into adaptation of the utero-placental circulation. Hum. Reprod. 2021; 36(3): 571-86. https://dx.doi.org/10.1093/humrep/deaa303.
  24. James J.L., Saghian R., Perwick R., Clark A.R. Trophoblast plugs: impact on utero-placental haemodynamics and spiral artery remodelling. Hum. Reprod. 2018; 33(8):1430-41. https://dx.doi.org/10.1093/humrep/dey225.
  25. Jauniaux E., Collins S., Burton G.J. Placenta accreta spectrum: pathophysiology and evidence-based anatomy for prenatal ultrasound imaging. Am. J. Obstet. Gynecol. 2018; 218(1): 75-87. https://dx.doi.org/10.1016/j.ajog.2017.05.067.
  26. Liu X., Wang Y., Wu Y., Zeng J., Yuan X., Tong C., Qi H. What we know about placenta accreta spectrum (PAS). Eur. J. Obstet. Gynecol. Reprod. Biol. 2021; 259: 81-9. https://dx.doi.org/10.1016/j.ejogrb.2021.02.001.
  27. Nik-Ahmad-Zuky N.L., Seoparjoo A., Husna E.I.E. Placenta increta presenting with threatened miscarriage during the first trimester in rhesus-negative mother: a case report. J. Med. Case Rep. 2021; 15(1): 448. https://dx.doi.org/10.1186/s13256-021-03030-x.
  28. El-Hussieny M., Mohammed E.M., Zenhom N.M., Refaie M.M., Okasha A.M., Tawab M.A.E. Possible role of TGF- β 1, MMP-2, E-CAD, β-Catenin and antioxidants in pathogenesis of placenta accreta. Fetal Pediatr. Pathol. 2021; 40(3): 222-32. https://dx.doi.org/10.1080/15513815.2020.1843574.
  29. Cabral-Pacheco G.A., Garza-Veloz I., Castruita-De la Rosa C., Ramirez-Acuña J.M., Perez-Romero B.A., Guerrero-Rodriguez J.F. et al. The roles of matrix metalloproteinases and their inhibitors in human diseases. Int. J. Mol. Sci. 2020; 21(24): 9739. https://dx.doi.org/10.3390/ijms21249739.
  30. DaSilva-Arnold S.C., Zamudio S., Al-Khan A., Alvarez-Perez J., Mannion C., Koenig C. et al. Human trophoblast epithelial-mesenchymal transition in abnormally invasive placenta. Biol. Reprod. 2018; 99(2): 409-21. https://dx.doi.org/10.1093/biolre/ioy042.
  31. Carlino C., Rippo M.R., Lazzarini R., Monsurrò V., Morrone S., Angelini S. et al. Differential microRNA expression between decidual and peripheral blood natural killer cells in early pregnancy. Hum. Reprod. 2018; 33(12): 2184-95. https://dx.doi.org/10.1093/humrep/dey323.
  32. Díaz-Hernández I., Alecsandru D., García-Velasco J.A., Domínguez F. Uterine natural killer cells: from foe to friend in reproduction. Hum. Reprod. Update. 2021; 27(4): 720-46. https://dx.doi.org/10.1093/humupd/dmaa062.
  33. Bulmer J.N., Lash G.E. Uterine natural killer cells: Time for a re-appraisal? F1000Res. 2019; 8: 999-1000. https://dx.doi.org/10.12688/f1000research.19132.1.
  34. Carvajal L., Gutiérrez J., Morselli E., Leiva A. Autophagy process in trophoblast cells invasion and differentiation: similitude and differences with cancer cells. Front. Oncol. 2021; 11: 637594. https://dx.doi.org/ 10.3389/fonc.2021.637594.
  35. Verbovsek U., Van Noorden C.J., Lah T.T. Complexity of cancer protease biology: Cathepsin K expression and function in cancer progression. Semin. Cancer Biol. 2015; 35: 71-84. https://dx.doi.org/10.1016/j.semcancer.2015.08.010.
  36. Lala P.K., Nandi P., Hadi A., Halari C. Placenta; 2021; 116: 12-30. https://dx.doi.org/10.1016/j.placenta.2021.03.003.
  37. Wang N., Shi D., Li N., Qi H. Clinical value of serum VEGF and sFlt-1 in pernicious placenta previa. Ann. Med. 2021; 53(1): 2041-9. https://dx.doi.org/ 10.1080/07853890.2021.1999492.
  38. Shainker S.A., Dannheim K., Gerson K.D., Neo D., Zsengeller Z.K., Pernicone E. et al. Down-regulation of soluble fms-like tyrosine kinase 1 expression in invasive placentation. Arch. Gynecol. Obstet. 2017; 296(2): 257-62. https://dx.doi.org/10.1007/s00404-017-4432-7.
  39. Bartels H.C., Postle J.D., Downey P., Brennan D.J. Placenta accreta spectrum: A review of pathology, molecular biology, and biomarkers. Dis. Markers. 2018; 2018: 1507674. https://dx.doi.org/10.1155/2018/1507674.
  40. Goh W., Yamamoto S.Y., Thompson K.S., Bryant-Greenwood G.D. Relaxin, its receptor (RXFP1), and insulin-like peptide 4 expression through gestation and in placenta accreta. Reprod. Sci. 2013; 20(8): 968-80. https://dx.doi.org/10.1177/1933719112472735.
  41. Brabletz T., Kalluri R., Nieto M.A., Weinberg R.A. EMT in cancer. Nat. Rev. Cancer. 2018; 18(2): 128-34. https://dx.doi.org/10.1038/nrc.2017.118.
  42. Поздняков Д.Ю., Шувалов О.Ю., Барлев Н.А., Миттенберг А.Г. Транскрипционный фактор ZEB1: посттранскрипционная регуляция его активности в карциномах молочной железы человека. Цитология. 2020; 62(1): 3-15. [Pozdnyakov D.Y., Shuvalova O.Y., Barlev N.A., Mittenberg A.G. Transcription factor ZEB1 and post-transcriptional regulation of its activity in human breast carcinomae. Citology. 2020; 62(1): 3-15 (in Russian)]. https://dx.doi.org/10.31857/S0041377120010071.
  43. Imani S., Hosseinifard H., Cheng J., Wei C., Fu J. Prognostic value of EMT-inducing transcription factors (EMT-TFs) in metastatic breast cancer: A systematic review and meta-analysis. Sci. Rep. 2016; 6: 28587. https://dx.doi.org/10.1038/srep28587.
  44. Li N., Yang T., Yu W., Liu H., Qiao C., Liu C. The role of Zeb1 in the pathogenesis of morbidly adherent placenta. Mol. Med. Rep. 2019; 20(3):2812-22. https://dx.doi.org/10.3892/mmr.2019.10490.
  45. Wu W.S., You R.I., Cheng C.C., Lee M.C., Lin T.Y., Hu C.T. Snail collaborates with EGR-1 and SP-1 to directly activate tran- scription of MMP 9 and ZEB1. Sci. Rep. 2017; 7: 17753. https://dx.doi.org/10.1038/s41598-017-18101-7.
  46. Soyama H., Miyamoto M., Ishibashi H., Iwahashi H., Matsuura H., Kakimoto S. et al. Placenta previa may acquire invasive nature by factors associated with epithelial-mesenchymal transition and matrix metalloproteinases. J. Obstet. Gynaecol. Res. 2020; 46(12): 2526-33. https://dx.doi.org/10.1111/jog.14485.
  47. Hayder H., O'Brien J., Nadeem U., Peng C. MicroRNAs: crucial regulators of placental development. Reproduction. 2018; 155(6): 259-71. https://dx.doi.org/10.1530/REP-17-0603.
  48. Liao G., Wang R., Rezey A.C., Gerlach B.D., Tang D.D. Micro-RNA miR-509 regulates ERK1/2, the vimentin network, and focal adhesions by targeting Plk1. Sci. Rep. 2018; 8: 12635. https://dx.doi.org/10.1038/s41598-018-30895-8.
  49. Кугаевская Е.В., Гуреева Т.А., Тимошенко О.С., Соловьева Н.И. Система активатора плазминогена урокиназного типа и ее роль в прогрессировании опухоли. Биомедицинская химия. 2018; 64(6), 472-86. [Kugaevskaya E.V., Gureeva T.A., Timoshenko O.S., Solovyeva N.I. The urokinase-type plasminogen activator system and its role in tumor progression. Biomeditsinskaya khimiya/ Biomedical Chemistry. 2018; 64(6): 472-86. (in Russian)]. https://dx.doi.org/10.18097/PBMC20186406472.
  50. Gu Y., Meng J., Zuo C., Wang S., Li H., Zhao S. et al. Downregulation of MicroRNA-125a in placenta accreta spectrum disorders contributes antiapoptosis of implantation site intermediate trophoblasts by targeting MCL1. Reprod. Sci. 2019; 26(12): 1582-9. https://dx.doi.org/10.1177/1933719119828040.
  51. Чистякова Г.Н., Ремизова И.И., Гришкина А.А., Каюмова А.В., Нестеров В.Ф. Морфологические и иммуногистохимические особенности плацентарной ткани при аномалиях прикрепления плаценты. Российский вестник акушера-гинеколога. 2019; 19(2): 34-41. [Chistiakova G.N., Remizova I.I., Grishkina A.A., Kayumova A.V., Nesterov V.F. The morphological and immunohistochemical features of placental tissue in placentation abnormalities. Russian Bulletin of Obstetrician-Gynecologist. 2019; 19(2): 34 41. (in Russian)]. https://dx.doi.org/10. 17116/rosakush20191902134.
  52. Humaira A., Edwin C. Etiopathogenesis and risk factors for placental accreta spectrum disorders. Best Pract. Res. Clin. Obstet. Gynaecol. 2021; 72: 4-12. https://dx.doi.org/10.1016/j.bpobgyn.2020.07.006.
  53. Ernst L.M., Linn R.L., Minturn L., Miller E.S. Placental pathologic associations with morbidly adherent placenta: potential insights into pathogenesis. Pediatr. Dev. Pathol. 2017; 20(5): 387-93. https://dx.doi.org/10.1177/1093526617698600.
  54. Jabrane-Ferrat N., Siewiera J. The up side of decidual natural killer cells: new developments in immunology of pregnancy. Immunology. 2014; 141(4): 490-7. https://dx.doi.org/10.1111/imm.12218.
  55. Judge A., Dodd M.S. Metabolism. Essays Biochem. 2020; 64(4): 607-47. https://dx.doi.org/10.1042/EBC20190041.
  56. Holland O., Dekker Nitert M., Gallo L.A., Vejzovic M., Fisher J.J., Perkins A.V. Review: Placental mitochondrial function and structure in gestational disorders. Placenta. 2017; 54: 2-9. https://dx.doi.org/10.1016/j.placenta.2016.12.012.
  57. Egan G., Khan D.H., Lee J.B., Mirali S., Zhang L., Schimmer A.D. Mitochondrial and metabolic pathways regulate nuclear gene expression to control differentiation, stem cell function, and immune response in leukemia. Cancer Discov. 2021; 11(5): 1052-66. https://dx.doi.org/10.1158/2159-8290.CD-20-1227.
  58. Liu S., Diao L., Huang C., Li Y., Zeng Y., Kwak-Kim J.Y.H. The role of decidual immune cells on human pregnancy. J. Reprod. Immunol. 2017; 124: 44-53. https://dx.doi.org/10.1016/j.jri.2017.10.045.
  59. Cartwright J.E., James-Allan L., Buckley R.J., Wallace A.E. The role of decidual NK cells in pregnancies with impaired vascular remodelling. J. Reprod. Immunol. 2017;119: 81-4. https://dx.doi.org/10.1016/j.jri.2016.09.002.
  60. Ander S.E., Diamond M.S., Coyne C.B. Immune responses at the maternal-fetal interface. Sci. Immunol. 2019; 4(31): eaat6114. https://dx.doi.org/10.1126/ sciimmunol.aat6114.
  61. Ning F., Liu H., Lash G.E. The role of decidual macrophages during normal and pathological pregnancy. Am. J. Reprod. Immunol. 2016; 75(3): 298-309. https://dx.doi.org/10.1111/aji.12477.
  62. Wu K., Lin K., Li X., Yuan X., Xu P., Ni P. et al. Redefining tumor-associated macrophage subpopulations and functions in the tumor microenvironment. Front. Immunol. 2020; 11: 1731. https://dx.doi.org/10.3389/fimmu.2020.01731.
  63. Fernández-Cortés M., Delgado-Bellido D., Oliver F.J. Vasculogenic mimicry: become an endothelial cell ‘But Not So Much’. Front. Oncol. 2019; 9: 803. https://dx.doi.org/10.3389/fonc.2019.00803.
  64. West R.C., Bouma G.J., Winger Q.A. Shifting perspectives from "oncogenic" to oncofetal proteins; how these factors drive placental development. Reprod. Biol. Endocrinol. 2018; 16(1): 1-12. https://dx.doi.org/10.1186/s12958-018-0421-3.
  65. Murray M.J., Lessey B.A. Embryo implantation and tumor metastasis: Common pathways of invasion and angiogenesis. Semin. Reprod. Endocrinol. 1999; 17(3): 275-90. https://dx.doi.org/10.1055/s-2007-1016235 110.
  66. Li X., Sun X., Carmeliet P. Hallmarks of endothelial cell metabolism in health and disease. Cell Metab. 2019; 30(3): 414-33. https://dx.doi.org/10.1016/j.cmet.2019.08.011.
  67. Zecchin A., Kalucka J., Dubois C., Carmeliet P. How endothelial cells adapt their metabolism to form vessels in tumors. Front. Immunol. 2017; 8: 1750. https://dx.doi.org/10.3389/fimmu.2017.01750.
  68. Macklin P.S., McAuliffe J., Pugh C.W., Yamamoto A. Hypoxia and HIF pathway in cancer and the placenta. Placenta. 2017; 56: 8-13. https://dx.doi.org/10.1016/ j.placenta.2017.03.010.

Received 15.02.2022

Accepted 28.04.2022

About the Authors

Alena V. Kayumova, PhD, Leading Researcher, Head of the Medical Care Quality Control Department, Ural Research Institute of Maternity and Child Care,
Ministry of Health of the Russian Federation, +7-982-62-32-047, kaum-doc@mail.ru, https://orcid.org/0000-0003-2685-4285, 620028, Russia, Ekaterinburg, Repin str., 1.
Oksana A. Melkozerova, Dr. Med. Sci., Deputy Director for Science, Ural Research Institute of Maternity and Child Care, Ministry of Health of the Russian Federation, abolmed1@mail.ru, https://orcid.org/0000-0002-4090-0578, 620028, Russia, Ekaterinburg, Repin str., 1.
Nadezhda V. Bashmakova, Dr. Med. Sci., Professor, Chief Researcher, Ural Research Institute of Maternity and Child Care, Ministry of Health of the Russian Federation, bashmakovanv@niiomm.ru, https://orcid.org/0000-0001-5746-316X, 620028, Russia, Ekaterinburg, Repin str., 1.
Galina B. Malgina, Dr. Med. Sci., Director of the Ural Research Institute of Maternity and Child Care, Ministry of Health of Russia, galinamalgina@mail.ru,
https://orcid.org/0000-0002-5500-6296, 620028, Russia, Ekaterinburg, Repin str., 1.
Guzal N. Chistyakova, Dr. Med. Sci., Professor, Head of Research Department of Immunology and Microbiology, Ural Research Institute of Maternity and Child Care,
Ministry of Health of the Russian Federation, guzel@niiomm.ru, https://orcid.org/0000-0002-0852-6766, 620028, Russia, Ekaterinburg, Repin str., 1.
Corresponding author: Alena V. Kayumova, kaum-doc@mail.ru

Authors' contributions: Kayumova A.V., Melkozerova O.A. – concept and design of the investigation, material collection and procession; Kayumova A.V. – writing the text; Bashmakova N.V., Melkozerova O.A., Malgina G.B., Chistyakova G.N. – editing.
Conflicts of interest: The authors declare that there are no possible conflicts of interest.
Funding: State research assignment No. 056-00121-22-00.
For citation: Kayumova A.V., Melkozerova O.A.,
Bashmakova N.V., Malgina G.B., Chistyakova G.N. Pathogenetic parallels
of tumor growth and placental pathological invasion.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 5: 14-22 (in Russian)
https://dx.doi.org/10.18565/aig.2022.5.14-22

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.