akusherstvoObstetrics, Gynecology and ReproductionАкушерство, Гинекология и Репродукция2313-73472500-3194IRBIS LLC10.17749/2313-7347/ob.gyn.rep.2022.337akusherstvo-1523Research ArticleREVIEW ARTICLESНАУЧНЫЕ ОБЗОРЫStructural placental changes in women with intra-pregnancy novel coronavirus infection COVID-19 (review)Структурные изменения в плаценте женщин, перенесших во время беременности новую коронавирусную инфекцию COVID-19 (обзор литературы)https://orcid.org/0000-0001-6590-8149ЯкимоваА. В.YakimovaA. V.

Якимова Анна Валентиновна – д.м.н., профессор кафедры акушерства и гинекологии

Scopus Author ID: 26027671100.

630091 Новосибирск, Красный проспект, д. 52

Anna V. Yakimova – MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology

Scopus Author ID: 26027671100.

52 Krasny Avenue, Novosibirsk 630091

https://orcid.org/0000-0003-3114-4384БороваяС. Ю.BorovayaS. Yu.

Боровая Светлана Юрьевна – врач акушер-гинеколог

630089 Новосибирск, ул. Адриена Лежена, д. 32

Svetlana Yu. Borovaya – MD, Obstetrician-Gynecologist

32 Adriena Lezhena Str., Novosibirsk 630089

https://orcid.org/0000-0003-1054-4821МухамедшинаВ. Р.MukhamedshinaV. R.

Мухамедшина Василя Рашитовна – к.м.н., ассистент кафедры акушерства и гинекологии

630091 Новосибирск, Красный проспект, д. 52

Vasilya R. Mukhamedshina – MD, PhD, Assistant, Department of Obstetrics and Gynecology

52 Krasny Avenue, Novosibirsk 630091

Vilfahmuh@yandex.ruhttps://orcid.org/0000-0001-5200-6808ДаценкоН. С.DatsenkoN. S.

Даценко Наталья Сергеевна – ассистент кафедры акушерства и гинекологии

630091 Новосибирск, Красный проспект, д. 52

Natalya S. Datsenko – MD, Assistant, Department of Obstetrics and Gynecology

52 Krasny Avenue, Novosibirsk 630091

https://orcid.org/0000-0001-6029-8791КучеренкоС. Г.KucherenkoS. G.

Кучеренко Светлана Геннадиевна – к.м.н., доцент кафедры акушерства и гинекологии

630091 Новосибирск, Красный проспект, д. 52

Svetlana G. Kucherenko – MD, PhD, Associate Professor, Department of Obstetrics and Gynecology

52 Krasny Avenue, Novosibirsk 630091

https://orcid.org/0000-0002-4201-3665ПоздняковИ. М.PozdnyakovI. M.

Поздняков Иван Михайлович – д.м.н., профессор кафедры акушерства и гинекологии

630091 Новосибирск, Красный проспект, д. 52

Ivan M. Pozdnyakov – MD, Dr Sci Med, Professor, Department of Obstetrics and Gynecology

52 Krasny Avenue, Novosibirsk 630091

https://orcid.org/0000-0003-1356-5257НикитенкоЕ. В.NikitenkoE. V.

Никитенко Евгений Викторович – к.м.н., зав. патологоанатомическим отделением

630089 Новосибирск, ул. Адриена Лежена, д. 32

Evgeij V. Nikitenko – MD, PhD, Head of the Pathology Department

32 Adriena Lezhena Str., Novosibirsk 630089

ФГБОУ ВО «Новосибирский государственный медицинский университет» Министерства здравоохранения Российской ФедерацииРоссияNovosibirsk State Medical University, Health Ministry of Russian FederationRussian FederationГБУЗ НСО «Новосибирский государственный клинический перинатальный центр»РоссияNovosibirsk State Clinical Perinatal CenterRussian Federation202215012023166732743Copyright © Yakimova A.V., Borovaya S.Y., Mukhamedshina V.R., Datsenko N.S., Kucherenko S.G., Pozdnyakov I.M., Nikitenko E.V., 20232023Якимова А.В., Боровая С.Ю., Мухамедшина В.Р., Даценко Н.С., Кучеренко С.Г., Поздняков И.М., Никитенко Е.В.Yakimova A.V., Borovaya S.Y., Mukhamedshina V.R., Datsenko N.S., Kucherenko S.G., Pozdnyakov I.M., Nikitenko E.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.gynecology.su/jour/article/view/1523Introduction

Introduction. During the COVID-19 pandemic, the question regarding an effect of related infection on the body of pregnant women and the fetoplacental complex has emerged, with many aspects of this issue still being unknown. At the moment, it has been proven that in some cases the course of COVID-19 can be accompanied by severe systemic inflammatory reaction leading to hypercoagulable state.

Aim

Aim: to search for evidence of a direct and/or indirect effect of SARS-CoV-2 infection on human placenta structure.

Materials and Methods

Materials and Methods. Taking into account the goal, this review was compiled according to the type of a narrative review of publications on a topic of interest. A search for English-language publications dated of 01.12.2019 till 01.12.2021 in PubMed/MEDLINE, Cochrane, Web of Science databases was made. The search queries included the following keywords: combinations of «coronavirus» and «infection during pregnancy», «placental structure» and «2019-nCoV», «COVID-19 and pregnancy», «SARSCoV-2 and pregnancy». In the process of writing the article, in order to improve the reader's understanding of the essence of debated issue, there was a need to discuss some of the results with literary sources published earlier 2019 that were not directly related to the topic of the new coronavirus infection (there are 6 such sources). We analyzed full-text publications, both reports on original research and meta-analyses on relevant topics. In total, 351 full-text publications met the query criteria, of which 54 were selected as meeting the objectives of the study. The select reports were discussed by the co-authors, duplicates were excluded and 34 of them were included in this review. In those that were excluded from the review, information about the clinical course of pregnancy and its outcome during novel coronavirus infection prevailed, or isolated cases of studying insignificant placental structural changes were discussed. Studies with a small number of observations were selected only in the case of the uniqueness of the published data, the absence of scientific papers where similar studies would have been conducted in larger sample.

Results

Results. Pregnancy complicated by COVID-19 may be accompanied by placental structural changes, which represent both a manifestation of compensatory-adaptive reactions and a consequence of the damaging effect to the placenta due to infectious process. In case of late (in the III trimester) disease in pregnant woman with mild COVID-19, placental disorders are predominantly of compensatory-adaptive nature, specific cytological signs of viral cell damage are uncharacteristic. During COVID-19 infection, chronic histiocytic intervillositis and syncytiotrophoblast necrosis occur more often than in average population, and adverse fetal outcomes are characterized by additional marked increase in intervillous fibrinoid deposition. Before COVID-19 pandemic, chronic histiocytic intervillositis was described in about 6 out of 10,000 placentas (0.6 %) in II and III trimesters.

Conclusion

Conclusion. The high frequency of chronic histiocytic intervillositis, both in the placenta of paired women with live-born infants infected prenatally due to maternal virus transmission, and in the placentas of stillborn infected infants, allows us to cautiously assume that such placental structural changes are more characteristic for damage by SARS-CoV-2 rather than other infectious agents. It is necessary to study a relationship between placental structural changes occurred at different gestation ages, as well as clinical course and outcome of pregnancy during COVID-19.

Введение

Введение. Во время пандемии COVID-19 возник вопрос о влиянии данной инфекции на организм беременных и фетоплацентарный комплекс, и многие аспекты этой проблемы еще неизвестны. В настоящий момент является доказанным, что течение COVID-19 в ряде случаев может сопровождаться тяжелой системной воспалительной реакцией и приводить к состоянию гиперкоагуляции.

Цель

Цель: поиск доказательств непосредственного и/или опосредованного влияния инфекции, вызванной вирусом SARS-CoV-2, на структуру плаценты человека.

Материалы и методы

Материалы и методы. Данный обзор был составлен по типу традиционного обзора публикаций по интересующей теме с учетом поставленной цели. Проведен поиск англоязычных публикаций с 01.12.2019 по 01.12.2021 в базах PubMed/MEDLINE, Cochrane, Web of Science. Поисковые запросы включали следующие ключевые слова: сочетания «coronavirus» и «infection during pregnancy», «placental structure», «2019-nCoV», «COVID-19 and pregnancy», «SARS-CoV-2 and pregnancy». В процессе написания статьи для улучшения понимания читателем сути обсуждаемой проблемы возникала необходимость обсуждения некоторых результатов из литературных источников, опубликованных ранее 2019 г., напрямую не связанных с темой новой коронавирусной инфекции (таких источников 6). Анализировали полнотекстовые публикации, как отчеты об оригинальных исследованиях, так и метанализы по соответствующей тематике. Всего критериям запроса соответствовала 351 полнотекстовая публикация, из которых были отобраны 54 как отвечавшие цели проводимого исследования. Отобранные отчеты были обсуждены соавторами, исключены дубликаты, и в настоящий обзор были включены 34 из них. В исключенных из обзора публикациях преобладала информация о клиническом течении беременности и ее исходе на фоне новой коронавирусной инфекции или обсуждались единичные случаи изучения структурных изменений плаценты, которые не имели статистической значимости. Исследования с малым числом наблюдений были отобраны только в случае уникальности опубликованных данных, отсутствия научных работ, где были бы проведены аналогичные исследования на большем материале.

Результаты

Результаты. Беременность, осложненная COVID-19, может сопровождаться структурными изменениями плаценты, которые являются как проявлением компенсаторно-приспособительных реакций, так и следствием повреждающего воздействия инфекционного процесса на плаценту. При позднем (в III триместре) заболевании беременной COVID-19 в легкой форме плацентарные нарушения носят преимущественно компенсаторно-приспособительный характер, нехарактерны специфические цитологические признаки вирусного поражения клеток. При новой коронавирусной инфекции более часто, чем в среднем в популяции, возникает хронический гистиоцитарный интервиллузит и некроз синцитиотрофобласта, а неблагоприятные исходы для плода характеризуются дополнительно значительным увеличением отложения межворсинчатого фибриноида. До пандемии COVID-19 хронический гистиоцитарный интервиллузит описывали примерно в 6 из 10 тыс. плацент (0,6 %) во II и III триместрах.

Заключение

Заключение. Высокая частота хронического гистиоцитарного интервиллузита как в плаценте от живорожденных младенцев, заразившихся пренатально в результате передачи вируса от матери к плоду, так и в плацентах мертворожденных инфицированных младенцев позволяет с осторожностью предполагать, что такие структурные изменения плаценты характерны в большей степени для ее поражения SARS-CoV-2, а не другими инфекционными агентами. Необходимо изучение взаимосвязи структурных изменений плаценты, возникших в разные строки гестации, с клиническим течением и исходом беременности при COVID-19.

коронавирусинфекция во время беременностиструктура плаценты2019-nCoVCOVID-19 и беременностьSARS-CoV-2 и беременностьcoronavirusinfection during pregnancyplacental structure2019-nCoVCOVID-19 and pregnancySARS-CoV-2 and pregnancyReferencesSchwartz D.A. The effects of pregnancy on women with COVID-19: maternal and infant outcomes. Clin Infect Dis. 2020;71(16):2042–4. https://doi.org/10.1093/cid/ciaa559.Schwartz D.A. The effects of pregnancy on women with COVID-19: maternal and infant outcomes. Clin Infect Dis. 2020;71(16):2042–4. https://doi.org/10.1093/cid/ciaa559.Schwartz D.A. Maternal and infant death and the rVSV-ZEBOV vaccine through three recent Ebola virus epidemics – West Africa, DRC Équateur and DRC Kivu: 4 years of excluding pregnant and lactating women and their infants from immunization. Curr Trop Med Rep. 2019;6:213–22. https://doi.org/10.1007/s40475-019-00195-w.Schwartz D.A. Maternal and infant death and the rVSV-ZEBOV vaccine through three recent Ebola virus epidemics – West Africa, DRC Équateur and DRC Kivu: 4 years of excluding pregnant and lactating women and their infants from immunization. Curr Trop Med Rep. 2019;6:213–22. https://doi.org/10.1007/s40475-019-00195-w.Krauer F., Riesen M., Reveiz L. et al. Zika virus infection as a cause of congenital brain abnormalities and Guillain-Barré syndrome: systematic review PLoS Med. 2017;14(1):e1002203. https://doi.org/10.1371/journal.pmed.1002203.Krauer F., Riesen M., Reveiz L. et al. Zika virus infection as a cause of congenital brain abnormalities and Guillain-Barré syndrome: systematic review PLoS Med. 2017;14(1):e1002203. https://doi.org/10.1371/journal.pmed.1002203.Alserehi H., Wali G., Alshukairi A., Alraddadi B. Impact of Middle East Respiratory Syndrome coronavirus (MERS-CoV) on pregnancy and perinatal outcome. BMC Infect Dis. 2016;16:105. https://doi.org/10.1186/s12879-016-1437-y.Alserehi H., Wali G., Alshukairi A., Alraddadi B. Impact of Middle East Respiratory Syndrome coronavirus (MERS-CoV) on pregnancy and perinatal outcome. BMC Infect Dis. 2016;16:105. https://doi.org/10.1186/s12879-016-1437-y.Alfaraj S.H., Al-Tawfiq J.A., Memish Z.A. Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection during pregnancy: Report of two cases & review of the literature. J Microbiol Immunol Infect. 2019;52(3):501–3. https://doi.org/10.1016/j.jmii.2018.04.005.Alfaraj S.H., Al-Tawfiq J.A., Memish Z.A. Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection during pregnancy: Report of two cases & review of the literature. J Microbiol Immunol Infect. 2019;52(3):501–3. https://doi.org/10.1016/j.jmii.2018.04.005.Hammock B.D., Wang W., Gilligan M.M., Panigrahy D. The overlooked storm in coronavirus disease 2019 (COVID-19)? Am J Pathol. 2020;190(9):1782–8. https://doi.org/10.1016/j.ajpath.2020.06.01.Hammock B.D., Wang W., Gilligan M.M., Panigrahy D. The overlooked storm in coronavirus disease 2019 (COVID-19)? Am J Pathol. 2020;190(9):1782–8. https://doi.org/10.1016/j.ajpath.2020.06.01.Xu Z., Shi L., Wang Y. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420–2. https://doi.org/10.1016/S2213-2600(20)30076-X.Xu Z., Shi L., Wang Y. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. 2020;8(4):420–2. https://doi.org/10.1016/S2213-2600(20)30076-X.Mehta P., McAuley D.F., Brown M. et al., HLH Across Speciality Collaboration UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet. 2020;395(10229):1033–4. https://doi.org/10.1016/S0140-6736(20)30628-0.Mehta P., McAuley D.F., Brown M. et al., HLH Across Speciality Collaboration UK. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet. 2020;395(10229):1033–4. https://doi.org/10.1016/S0140-6736(20)30628-0.Panigrahy D., Gilligan M.M., Huang S. et al. Inflammation resolution: a dual-pronged approach to averting cytokine storms in COVID-19? Cancer Metastasis Rev. 2020;39(2):337–40. https://doi.org/10.1007/s10555-020-09889-4.Panigrahy D., Gilligan M.M., Huang S. et al. Inflammation resolution: a dual-pronged approach to averting cytokine storms in COVID-19?Cancer Metastasis Rev. 2020;39(2):337–40. https://doi.org/10.1007/s10555-020-09889-4.Connors J.M., Levy J.H. COVID-19 and its implications for thrombosis and anticoagulation. Blood. 2020;135(23):2033–40. https://doi.org/10.1182/blood.2020006000.Connors J.M., Levy J.H. COVID-19 and its implications for thrombosis and anticoagulation. Blood. 2020;135(23):2033–40. https://doi.org/10.1182/blood.2020006000.Gris J.C., Perez-Martin A., Quéré I., Sotto A. COVID-19 associated coagulopathy: The crowning glory of thrombo-inflammation concept. Anaesth Crit Care Pain Med. 2020;39(3):381–2. https://doi.org/10.1016/j.accpm.2020.04.013.Gris J.C., Perez-Martin A., Quéré I., Sotto A. COVID-19 associated coagulopathy: The crowning glory of thrombo-inflammation concept. Anaesth Crit Care Pain Med. 2020;39(3):381–2. https://doi.org/10.1016/j.accpm.2020.04.013.Algarroba G.N., Rekawek P., Vahanian S.A. et al. Visualization of severe acute respiratory syndrome coronavirus 2 invading the human placenta using electron microscopy. Am J Obstet Gynecol. 2020;223(2):275–8. https://doi.org/10.1016/j.ajog.2020.05.023.Algarroba G.N., Rekawek P., Vahanian S.A. et al. Visualization of severe acute respiratory syndrome coronavirus 2 invading the human placenta using electron microscopy. Am J Obstet Gynecol. 2020;223(2):275–8. https://doi.org/10.1016/j.ajog.2020.05.023.Vivanti A.J., Vauloup-Fellous C., Prevot S. et al. Transplacental transmission of SARS-CoV-2 infection. Nat Commun. 2020;11(1):3572. https://doi.org/10.1038/s41467-020-17436-6.Vivanti A.J., Vauloup-Fellous C., Prevot S. et al. Transplacental transmission of SARS-CoV-2 infection. Nat Commun. 2020;11(1):3572. https://doi.org/10.1038/s41467-020-17436-6.Al-Haddad B.J.S, Jacobsson B., Chabra S. et al. Long-term risk of neuropsychiatric disease after exposure to infection in utero.JAMA Psychiatry. 2019;76(6):594–602. https://doi.org/10.1001/jamapsychiatry.2019.0029.Al-Haddad B.J.S, Jacobsson B., Chabra S. et al. Long-term risk of neuropsychiatric disease after exposure to infection in utero. JAMA Psychiatry. 2019;76(6):594–602. https://doi.org/10.1001/jamapsychiatry.2019.0029.Liu H., Wang L.L., Zhao S.J. et al. Why are pregnant women susceptible to COVID-19? An immunological viewpoint. Reprod Immunol. 2020;139:103122. https://doi.org/10.1016/j.jri.2020.10312.Liu H., Wang L.L., Zhao S.J. et al. Why are pregnant women susceptible to COVID-19? An immunological viewpoint. Reprod Immunol. 2020;139:103122. https://doi.org/10.1016/j.jri.2020.10312.Wastnedge E., Reynolds R.M., van Boeckel S.R. et al. Pregnancy and COVID-19. Physiol Rev. 2021;101(1):303–18. https://doi.org/10.1152/physrev.00024.2020.Wastnedge E., Reynolds R.M., van Boeckel S.R. et al. Pregnancy and COVID-19. Physiol Rev. 2021;101(1):303–18. https://doi.org/10.1152/physrev.00024.2020.Schwartz D.A., Baldewijns M., Benachi A. et al. Chronic histiocytic intervillositis with trophoblast necrosis is a risk factor associated with placental infection from coronavirus disease 2019 (COVID-19) and intrauterine maternal-fetal severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission in live-born and stillborn infants. Arch Pathol Lab Med. 2021;145(5):517–28. https://doi.org/10.5858/arpa.2020-0771-SA.Schwartz D.A., Baldewijns M., Benachi A. et al. Chronic histiocytic intervillositis with trophoblast necrosis is a risk factor associated with placental infection from coronavirus disease 2019 (COVID-19) and intrauterine maternal-fetal severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission in live-born and stillborn infants. Arch Pathol Lab Med. 2021;145(5):517–28. https://doi.org/10.5858/arpa.2020-0771-SA.Schwartz D.A., Morotti D. Placental pathology of COVID-19 with and without fetal and neonatal infection: trophoblast necrosis and chronic histiocytic intervillositis as risk factors for transplacental transmission of SARS-CoV-2. Viruses. 2020;12(11):1308. https://doi.org/10.3390/v12111308.Schwartz D.A., Morotti D. Placental pathology of COVID-19 with and without fetal and neonatal infection: trophoblast necrosis and chronic histiocytic intervillositis as risk factors for transplacental transmission of SARS-CoV-2. Viruses. 2020;12(11):1308. https://doi.org/10.3390/v12111308.Labarrere C., Mullen E. Fibrinoid and trophoblastic necrosis with massive chronic intervillositis: an extreme variant of villitis of unknown etiology. Am J Reprod Immunol Microbiol. 1987;15(3):85–91. https://doi.org/10.1111/j.1600-0897.1987.tb00162.x.Labarrere C., Mullen E.Fibrinoid and trophoblastic necrosis with massive chronic intervillositis: an extreme variant of villitis of unknown etiology. Am J Reprod Immunol Microbiol. 1987;15(3):85–91. https://doi.org/10.1111/j.1600-0897.1987.tb00162.x.Mattuizzi A., Sauvestre F., André G. et al. Adverse perinatal outcomes of chronic intervillositis of unknown etiology: an observational retrospective study of 122 cases. Sci Rep. 2020;10(1):12611. https://doi.org/10.1038/s41598-020-69191-9.Mattuizzi A., Sauvestre F., André G. et al. Adverse perinatal outcomes of chronic intervillositis of unknown etiology: an observational retrospective study of 122 cases. Sci Rep. 2020;10(1):12611. https://doi.org/10.1038/s41598-020-69191-9.Rapkiewicz A.V., Mai X., Carsons S.E. et al. Megakaryocytes and plateletfibrin thrombi characterize multi-organ thrombosis at autopsy in COVID- 19: a case series. EClinicalMedicine. 2020;24:100434. https://doi.org/10.1016/j.eclinm.2020.100434.Rapkiewicz A.V., Mai X., Carsons S.E. et al. Megakaryocytes and plateletfibrin thrombi characterize multi-organ thrombosis at autopsy in COVID-19: a case series. EClinicalMedicine. 2020;24:100434. https://doi.org/10.1016/j.eclinm.2020.100434.Knight M., Bunch K., Vousden N. et al.; UK Obstetric Surveillance System SARS-CoV-2 Infection in Pregnancy Collaborative Group. Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: national population based cohort study. BMJ. 2020;369:m2107. https://doi.org/10.1136/bmj.m2107.Knight M., Bunch K., Vousden N. et al.; UK Obstetric Surveillance System SARS-CoV-2 Infection in Pregnancy Collaborative Group. Characteristics and outcomes of pregnant women admitted to hospital with confirmed SARS-CoV-2 infection in UK: national population based cohort study. BMJ. 2020;369:m2107. https://doi.org/10.1136/bmj.m2107.Ji H.-.L., Zhao R., Matalon S., Matthay M.A. Elevated plasmin(ogen) as a common risk factor for COVID-19 susceptibility. Physiol Rev. 2020;100(3):1065–75. https://doi.org/10.1152/physrev.00013.2020.Ji H.-.L., Zhao R., Matalon S., Matthay M.A. Elevated plasmin(ogen) as a common risk factor for COVID-19 susceptibility. Physiol Rev. 2020;100(3):1065–75. https://doi.org/10.1152/physrev.00013.2020.Di Renzo G.C., Giardina I. Coronavirus disease 2019 in pregnancy: consider thromboembolic disorders and thromboprophylaxis. Am J Obstet Gynecol. 2020;223(1):135. https://doi.org/10.1016/j.ajog.2020.04.017.Di Renzo G.C., Giardina I. Coronavirus disease 2019 in pregnancy: consider thromboembolic disorders and thromboprophylaxis. Am J Obstet Gynecol. 2020;223(1):135. https://doi.org/10.1016/j.ajog.2020.04.017.Creanga A.A., Syverson C., Seed K., Callaghan W.M. Pregnancy-related mortality in the United States, 2011–2013. Obstet Gynecol. 2017;130(2):366–73. https://doi.org/10.1097/AOG.0000000000002114.Creanga A.A., Syverson C., Seed K., Callaghan W.M. Pregnancy-related mortality in the United States, 2011–2013. Obstet Gynecol. 2017;130(2):366–73. https://doi.org/10.1097/AOG.0000000000002114.Saving Lives, Improving Mothers’ Care Lessons learned to inform maternity care from the UK and Ireland Confidential Enquiries into Maternal Deaths and Morbidity 2016–18. Maternal, Newborn and Infant Clinical Outcome Review Programme. MBRRACE-UK, 2020. 96 p. Режим доступа: https://www.npeu.ox.ac.uk/assets/downloads/mbrrace-uk/reports/maternal-report-2020/MBRRACE-UK_Maternal_Report_Dec_2020_v10_ONLINE_VERSION_1404.pdf. [Дата обращения: 25.06.2022].Saving Lives, Improving Mothers’ Care Lessons learned to inform maternity care from the UK and Ireland Confidential Enquiries into Maternal Deaths and Morbidity 2016–18. Maternal, Newborn and Infant Clinical Outcome Review Programme. MBRRACE-UK, 2020. 96 p. Available at: https://www.npeu.ox.ac.uk/assets/downloads/mbrrace-uk/reports/maternal-report-2020/MBRRACE-UK_Maternal_Report_Dec_2020_v10_ONLINE_VERSION_1404.pdf. [Accessed: 25.06.2022].Patberg E.T., Adams T., Rekawek P. et al. Coronavirus disease 2019 infection and placental histopathology in women delivering at term. Am J Obstet Gynecol. 2021;224(4):382.e1–382.e18. https://doi.org/10.1016/j.ajog.2020.10.020.Patberg E.T., Adams T., Rekawek P. et al. Coronavirus disease 2019 infection and placental histopathology in women delivering at term. Am J Obstet Gynecol. 2021;224(4):382.e1–382.e18. https://doi.org/10.1016/j.ajog.2020.10.020.Sharps M.C., Hayes D.J.L., Lee S. et al. A structured review of placental morphology and histopathological lesions associated with SARS-CoV-2 infection. Placenta. 2020;101:13–29. https://doi.org/10.1016/j.placenta.2020.08.018.Sharps M.C., Hayes D.J.L., Lee S. et al. A structured review of placental morphology and histopathological lesions associated with SARS-CoV-2 infection. Placenta. 2020;101:13–29. https://doi.org/10.1016/j.placenta.2020.08.018.Baergen R.N., Heller D.S. Placental pathology in Covid-19 positive mothers: preliminary findings. Pediatr Dev Pathol. 2020;23(3):177–80. https://doi.org/10.1177/1093526620925569.Baergen R.N., Heller D.S. Placental pathology in Covid-19 positive mothers: preliminary findings. Pediatr Dev Pathol. 2020;23(3):177–80. https://doi.org/10.1177/1093526620925569.Щеголев А.И., Куликова Г.В., Туманова У.Н. и др. Морфометрическая характеристика ворсин плаценты рожениц с COVID-19. Бюллетень экспериментальной биологии и медицины. 2021;172(7):102–7. https://doi.org/10.47056/0365-9615-2021-172-7-102-107.Shchegolev A.I., Kulikova G.V., Tumanova U.N. et al. Morphometric parameters of placental villi in parturient women with COVID-19. [Morfometricheskaya harakteristika vorsin placenty rozhenic s COVID-19]. Byulleten' eksperimental'noj biologii i mediciny. 2021;172(7):102–7. (In Russ.). https://doi.org/10.47056/0365-9615-2021-172-7-102-107.Shanes E.D., Mithal L.B., Otero S. et al. Placental pathology in COVID-19. Am J Clin Pathol. 2020;154(1):23–32. https://doi.org/10.1093/ajcp/aqaa089.Shanes E.D., Mithal L.B., Otero S. et al. Placental pathology in COVID-19. Am J Clin Pathol. 2020;154(1):23–32. https://doi.org/10.1093/ajcp/aqaa089.Щеголев А.И., Куликова Г.В., Ляпин В.М. и др. Выраженность синцитиальных узелков и экспрессии VEGF в ворсинах плаценты рожениц с COVID-19 зависит от степени ее тяжести. Бюллетень экспериментальной биологии и медицины. 2021;171(3):386–90. https://doi.org/10.47056/0365-9615-2021-171-3-386-390.Shchegolev A.I., Kulikova G.V., Lyapin V.M. et al. The number of syncytial knots and VEGF expression in placental villi in parturient woman with COVID-19 depends on the disease severity. [Vyrazhennost' sincitial'nyh uzelkov i ekspressii VEGF v vorsinah placenty rozhenic s COVID-19 zavisit ot stepeni ee tyazhesti]. Byulleten' eksperimental'noj biologii i mediciny. 2021;171(3):386–90. (In Russ.). https://doi.org/10.47056/0365-9615-2021-171-3-386-390.Mendoza M., Garcia-Ruiz I., Maiz N. et al. Pre-eclampsia-like syndrome induced by severe COVID-19: a prospective observational study. BJOG. 2020;127(11):1374–80. https://doi.org/10.1111/1471-0528.16339.Mendoza M., Garcia-Ruiz I., Maiz N. et al. Pre-eclampsia-like syndrome induced by severe COVID-19: a prospective observational study. BJOG. 2020;127(11):1374–80. https://doi.org/10.1111/1471-0528.16339.Zhao Y., Huang B., Ma H. et al. Follow-up study on the outcomes of recovered pregnant women with a history of COVID-19 in the first and second trimesters: A case series from China. Matern Fetal Med. 2020;3(1):24–32. https://doi.org/10.1097/FM9.0000000000000080.Zhao Y., Huang B., Ma H. et al. Follow-up study on the outcomes of recovered pregnant women with a history of COVID-19 in the first and second trimesters: A case series from China. Matern Fetal Med. 2020;3(1):24–32. https://doi.org/10.1097/FM9.0000000000000080.Ge X.Y., Li J.L., Yang X.L. et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature. 2013;503(7477):535–8. https://doi.org/10.1038/nature12711.Ge X.Y., Li J.L., Yang X.L. et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature. 2013;503(7477):535–8. https://doi.org/10.1038/nature12711.Kai H., Kai M. Interactions of coronaviruses with ACE2, angiotensin II, and RAS inhibitors-lessons from available evidence and insights into COVID-19. Hypertens Res. 2020;43(7):648–54. https://doi.org/10.1038/s41440-020-0455-8.Kai H., Kai M. Interactions of coronaviruses with ACE2, angiotensin II, and RAS inhibitors-lessons from available evidence and insights into COVID-19. Hypertens Res. 2020;43(7):648–54. https://doi.org/10.1038/s41440-020-0455-8.Jing Y., Run-Qian L., Hao-Ran W et al. Review. Potential influence of COVID-19/ACE2 on the female reproductive system. Mol Hum Reprod. 2020;26(6):367–73. https://doi.org/10.1093/molehr/gaaa030.Jing Y., Run-Qian L., Hao-Ran W et al. Review. Potential influence of COVID-19/ACE2 on the female reproductive system. Mol Hum Reprod. 2020;26(6):367–73. https://doi.org/10.1093/molehr/gaaa030.Weatherbee B.A.T., Glover D.M., Zernicka-Goetz M. Expression of SARSCoV-2 receptor ACE2 and the protease TMPRSS2 suggests susceptibility of the human embryo in the first trimester. Open Biol. 2020;10(8):200162. https://doi.org/10.1098/rsob.200162.Weatherbee B.A.T., Glover D.M., Zernicka-Goetz M. Expression of SARSCoV-2 receptor ACE2 and the protease TMPRSS2 suggests susceptibility of the human embryo in the first trimester. Open Biol. 2020;10(8):200162. https://doi.org/10.1098/rsob.200162.Resta L., Vimercati A., Cazzato G. et al. SARS-CoV-2 and placenta: new insights and perspectives. Viruses. 2021;13(5):723. https://doi.org/10.3390/v13050723.Resta L., Vimercati A., Cazzato G. et al. SARS-CoV-2 and placenta: new insights and perspectives. Viruses. 2021;13(5):723. https://doi.org/10.3390/v13050723.Smithgall M.C., Liu-Jarin X., Hamele-Bena D. et al. Third-trimester placentas of severe acute respiratory syndrome coronavirus 2 (SARSCoV-2)-positive women: histomorphology, including viral immunohistochemistry and in-situ hybridization. Histopathology. 2020;77(6):994–9. https://doi.org/10.1111/his.14215.Smithgall M.C., Liu-Jarin X., Hamele-Bena D. et al. Third-trimester placentas of severe acute respiratory syndrome coronavirus 2 (SARSCoV- 2)-positive women: histomorphology, including viral immunohistochemistry and in-situ hybridization. Histopathology. 2020;77(6):994–9. https://doi.org/10.1111/his.14215.

The authors declare that there are no conflicts of interest present.