About
The Journal "Obstetrics and Gynecology"Journal HistoryAims and ScopePolicies on Conflict of Interest, Human and Animal Rights, and Informed ConsentEditorial ProcessData sharing statementAdvertising PolicyThe Process for Handling Cases Requiring Corrections, Retractions, and Editorial Expressions of ConcernEditorial BoardEditorial CounsilInformation for ProfessionalsNewsContacts
ArchiveEthical StandardsSubscription
For authors
InstructionsInformed consent policyContract offerEASE GuidelinesICJME CriteriaWAME Recommendations on ChatGPT and Chatbots in Relation to Scholarly Publications
Reviewing
About
The Journal "Obstetrics and Gynecology"Journal HistoryAims and ScopePolicies on Conflict of Interest, Human and Animal Rights, and Informed ConsentEditorial ProcessData sharing statementAdvertising PolicyThe Process for Handling Cases Requiring Corrections, Retractions, and Editorial Expressions of ConcernEditorial BoardEditorial CounsilInformation for ProfessionalsNewsContacts
ArchiveEthical StandardsSubscription
For authors
InstructionsInformed consent policyContract offerEASE GuidelinesICJME CriteriaWAME Recommendations on ChatGPT and Chatbots in Relation to Scholarly Publications
Reviewing
Logout
Obstetrics and Gynegology2024№3
COVID-19-associated placental damage

COVID-19-associated placental damage

DOI
https://dx.doi.org/10.18565/aig.2023.226

Pilkevich N.B., Markovskaya V.A., Khabibullin R.R., Yavorskaya O.V., Smirnova A.P.

1) Belgorod State National Research University, Belgorod, Russia; 2) Belgorod Pathological Anatomy Bureau, Belgorod, Russia

Modern society has faced the coronavirus disease (COVID-19), which has become a serious global threat to public health. This infection had a significant impact on the healthcare systems around the world. The article analyzes the literature sources on the pathogenesis of placentitis in COVID-19.
During the COVID-19 pandemic, the World Health Organization (WHO) identified pregnant women as a vulnerable group in terms of morbidity, and pregnancy was recognized as a risk factor for the severity of the infection.
SARS-CoV-2 placentitis is a severe and rare damage to the placenta, which is due to the infectious and immunological factors. They can cause severe and diffuse placental parenchymal destruction that can affect >75% of the placenta.
Viral particles attach to the villous trophoblast and destroy it. There is a complement activation, which contributes to the activation of hemostasis and leads to coagulopathy, as well as microvascular damage. The infected syncytiotrophoblast is damaged through complete or incomplete apoptosis. The persistent high level of the virus in the syncytiotrophoblast can lead to prolonged generation of complement fragments, cytokines of inflammatory origin and other chemotactic factors; it may cause a monocyte-macrophage inflammatory reaction, which further exacer-bates placental dysfunction.
Conclusion: COVID-19 infection can lead to the development of placental damage, pregnancy complications, including premature birth, preeclampsia, miscarriages, fetal growth retardation and stillbirth. 
SARS-CoV-2 placentitis occurs due to direct cytotoxicity after virus replication in the syncytiotrophoblast and manifests in three ways: histiocytic intervillositis, perivillous fibrin deposition and trophoblast necrosis.

Authors’ contributions: Pilkevich N.B., Markovskaya V.A., Khabibullin R.R., Yavorskaya O.V., Smirnova A.P. – developing the concept and design of the study, collecting publications, processing and analyzing material on the topic, writing the text of the article, editing the article.
Conflicts of interest: Authors declare lack of the possible conflicts of interests.
Funding: The study was conducted without sponsorship.
For citation: Pilkevich N.B., Markovskaya V.A., Khabibullin R.R., Yavorskaya O.V., Smirnova A.P. COVID-19-associated placental damage.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2024; (3): 13-19 (in Russian)
https://dx.doi.org/10.18565/aig.2023.226

Keywords

placenta
syncytiotrophoblast
pathogenesis
COVID-19
pregnancy
Full text (in Russian)

References

  1. Sekulovski M., Bogdanova-Petrova S., Peshevska-Sekulovska M., Velikova T., Georgiev T. COVID-19 related liver injuries in pregnancy. World J. Clin. Cases. 2023; 11(9): 1918-29. https://dx.doi.org/10.12998/wjcc.v11.i9.1918.
  2. Țieranu M.L., Dragoescu N.A., Zorilă G.L., Istrate-Ofițeru A.M., Rămescu C., Berbecaru E.I. et al. Addressing chronic gynecological diseases in the SARS-CoV-2 pandemic. Medicina (Kaunas). 2023; 59(4): 802. https://dx.doi.org/10.3390/medicina59040802.
  3. Rebutini P.Z., Zanchettin A.C., Stonoga E.T.S., Prá D.M.M., de Oliveira A.L.P., Dezidério F.D.S. et al. Association between COVID-19 pregnant women symptoms severity and placental morphologic features. Front. Immunol. 2021; 12: 685919. https://dx.doi.org/10.3389/fimmu.2021.685919.
  4. Cosma S., Carosso A.R., Cusato J., Borella F., Carosso M., Gervasoni F. et al. Preterm birth is not associated with asymptomatic/mild SARS-CoV-2 infection per se: pre-pregnancy state is what matters. PLoS One. 2021; 16(8): e0254875. https://dx.doi.org/10.1371/journal.pone.0254875.
  5. Balachandren N., Davies M.C., Hall J.A., Stephenson J.M., David A.L., Barrett G. et al. SARS-CoV-2 infection in the first trimester and the risk of early miscarriage: a UK population-based prospective cohort study of 3041 pregnancies conceived during the pandemic. Hum. Reprod. 2022; 37(6): 1126-33. https://dx.doi.org/10.1093/humrep/deac062.
  6. Lee J.J., Lee S.E., Kim Y., Park Y.J. Analysis of pregnant women with critically severe COVID-19 in Republic of Korea from February 2020 and December 2021. Osong Public Health Res. Perspect. 2023; 14(2): 129-37. https://dx.doi.org/10.24171/j.phrp.2023.0025.
  7. Tsikouras P., Kourti V., Gerede A., Kiosse E., Panopoulou M., Zervoudis S. et al. Impact of SARS-CoV-2 on pregnancy outcomes (review). Med. Int. (Lond). 2021; 1(5): 19. https://dx.doi.org/10.3892/mi.2021.19.
  8. Синякин И.А., Баталова Т.А., Жуковец И.В. Роль COVID-19 в развитии плацентарных нарушений у беременных пациенток. Медицина. 2023; 11(3): 42-53. [Sinyakin I.A., Batalova T.A., Zhukovets I.V. The role of COVID-19 in the development of placental abnormalities in pregnant patients. Medicine. 2023; 11(3): 42-53 (in Russian)]. https://dx.doi.org/10.29234/2308-9113-2023-11-3-42-53.
  9. Akhtar H., Patel C., Abuelgasim E., Harky A. COVID-19 (SARS-CoV-2) infection in pregnancy: a systematic review. Gynecol. Obstet. Invest. 2020; 85(4): 295-306. https://dx.doi.org/10.1159/000509290.
  10. Yang H., Wang C., Poon L.C. Novel coronavirus infection and pregnancy. Ultrasound Obstet. Gynecol. 2020; 55(4): 435-7. https://dx.doi.org/10.1002/uog.22006.
  11. Alberca R.W., Pereira N.Z., Oliveira L.M.D.S., Gozzi-Silva S.C., Sato M.N. Pregnancy, viral infection, and COVID-19. Front. Immunol. 2020; 11: 1672. https://dx.doi.org/10.3389/fimmu.2020.01672.
  12. Kreis N.N., Ritter A., Louwen F., Yuan J. A message from the human placenta: structural and immunomodulatory defense against SARS-CoV-2. Cells. 2020; 9(8): 1777. https://dx.doi.org/10.3390/cells9081777.
  13. Antoun L., Taweel N.E., Ahmed I., Patni S., Honest H. Maternal COVID-19 infection, clinical characteristics, pregnancy, and neonatal outcome: a prospective cohort study. Eur. J. Obstet. Gynecol. Reprod. Biol. 2020; 252: 559-62. https://dx.doi.org/10.1016/j.ejogrb.2020.07.008.
  14. Di Mascio D., Khalil A., Saccone G., Rizzo G., Buca D., Liberati M. et al. Outcome of coronavirus spectrum infections (SARS, MERS, COVID-19) during pregnancy: a systematic review and meta-analysis. Am. J. Obstet. Gynecol. M.F.M. 2020; 2(2): 100107. https://dx.doi.org/10.1016/j.ajogmf.2020.100107.
  15. Bahadur G., Bhat M., Acharya S., Janga D., Cambell B., Huirne J. et al. Retrospective observational RT-PCR analyses on 688 babies born to 843 SARS-CoV-2 positive mothers, placental analyses and diagnostic analyses limitations suggest vertical transmission is possible. Facts Views Vis. Obgyn. 2021; 13(1): 53-66. https://dx.doi.org/10.52054/FVVO.13.1.001.
  16. Redline R.W., Ravishankar S., Bagby C., Saab S., Zarei S. Diffuse and localized SARS-CoV-2 placentitis: prevalence and pathogenesis of an uncommon complication of COVID-19 infection during pregnancy. Am. J. Surg. Pathol. 2022; 46(8): 1036-47. https://dx.doi.org/10.1097/PAS.0000000000001889.
  17. Rauf A., Abu-Izneid T., Olatunde A., Ahmed Khalil A., Alhumaydhi F.A., Tufail T. et al. COVID-19 pandemic: epidemiology, etiology, conventional and non-conventional therapies. Int. J. Environ. Res. Public Health. 2020; 17(21): 8155. https://dx.doi.org/10.3390/ijerph17218155.
  18. Щелканов М.Ю., Колобухина Л.В., Бургасова О.А., Кружкова И.С., Малеев В.В. COVID-19: этиология, клиника, лечение. Инфекция и иммунитет. 2020; 10(3): 421-45. [Shchelkanov M.Yu., Kolobukhina L.V., Burgasova O.A., Kruzhkova I.S., Maleev V.V. COVID-19: etiology, clinical picture, treatment. Russian Journal of Infection and Immunity. 2020; 10(3): 421-45. (in Russian)]. https://dx.doi.org/10.15789/2220-7619-CEC-1473.
  19. Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. The species severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat. Microbiol. 2020; 5(4): 536-44. https://dx.doi.org/10.1038/s41564-020-0695-z.
  20. Chaudhry S., Aboudawoud O., Hardy G. A history of COVID-19 in pregnancy: a narrative review. J. Clin. Med. 2023; 12(17): 5722. https://dx.doi.org/10.3390/jcm12175722.
  21. Wastnedge E.A.N., Reynolds R.M., Van Boeckel S.R., Stock S.J., Denison F.C., Maybin J.A. et al. Pregnancy and COVID-19. Physiol. Rev. 2021; 101(1): 303-18. https://dx.doi.org/10.1152/physrev.00024.2020.
  22. Vouga M., Favre G., Martinez-Perez O., Pomar L., Acebal LF., Abascal-Saiz A. et al. Maternal outcomes and risk factors for COVID-19 severity among pregnant women. Sci. Rep. 2021; 11(1): 13898. https://dx.doi.org/10.1038/s41598-021-92357-y.
  23. Nana M., Nelson-Piercy C. COVID-19 in pregnancy. Clin. Med. (Lond). 2021; 21(5): 446-50. https://dx.doi.org/10.7861/clinmed.2021-0503.
  24. Smith E.R., Oakley E., Grandner G.W., Rukundo G., Farooq F., Ferguson K. et al. Clinical risk factors of adverse outcomes among women with COVID-19 in the pregnancy and postpartum period: a sequential, prospective meta-analysis. Am. J. Obstet. Gynecol. 2023; 228(2): 161-77. https://dx.doi.org/10.1016/j.ajog.2022.08.038.
  25. Linehan L., O'Donoghue K., Dineen S., White J., Higgins J.R., Fitzgerald B. SARS-CoV-2 placentitis: an uncommon complication of maternal COVID-19. Placenta. 2021; 15: 261-6. https://dx.doi.org/10.1016/j.placenta.2021.01.012.
  26. Huynh A., Sehn J.K., Goldfarb I.T., Watkins J., Torous V., Heerema-McKenney A. et al. SARS-CoV-2 placentitis and intraparenchymal thrombohematomas among COVID-19 infections in pregnancy. JAMA Netw. Open. 2022; 5(3): e225345. https://dx.doi.org/10.1001/jamanetworkopen.2022.5345.
  27. Watkins J.C., Torous V.F., Roberts D.J. Defining severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) placentitis. Arch. Pathol. Lab. Med. 2021; 145: 1341-9. https://dx.doi.org/10.5858/arpa.2021-0246-SA.
  28. Stenton S., McPartland J., Shukla R., Turner K., Marton T., Hargitai B. et al. SARS-COV2 placentitis and pregnancy outcome: a multicentre experience during the Alpha and early Delta waves of coronavirus pandemic in England. EClinicalMedicine. 2022; 47: 101389. https://dx.doi.org/10.1016/j.eclinm.2022.101389.
  29. Schwartz D.A., Mulkey S.B., Roberts D.J. SARS-CoV-2 placentitis, stillbirth, and maternal COVID-19 vaccination: clinical-pathologic correlations. Am. J. Obst. Gynecol. 2023; 228(3): 261-9. https://dx.doi.org/10.1016/j.ajog.2022.10.001.
  30. Delle Chiaie L., Stolpner I., Dettmer M.S., Baltz-Ghahremanpour K. Acute placental insufficiency two weeks after an asymptomatic COVID-19 maternal infection: the deleterious effects of the SARS-CoV-2 placentitis. Arch. Gynecol. Obstet. 2024; 309(2): 723-6. https://dx.doi.org/10.1007/s00404-023-06991-0.
  31. Lu-Culligan A., Chavan A.R., Vijayakumar P., Irshaid L., Courchaine E.M., Milano K.M. et al. Maternal respiratory SARS-CoV- 2 infection in pregnancy is associated with a robust inflammatory response at the maternal-fetal interface. Med. 2021; 2(5): 591-610.e10. https://dx.doi.org/10.1016/j.medj.2021.04.016.
  32. Hosier H., Farhadian S.F., Morotti R.A., Deshmukh U., Lu-Culligan A., Campbell K.H. et al. SARS-CoV-2 infection of the placenta. J. Clin. Invest. 2020; 130(9): 4947-53. https://dx.doi.org/10.1172/JCI139569.
  33. Hecht J.L., Quade B., Deshpande V., Mino-Kenudson M., Ting D.T., Desai N. et al. SARS-CoV-2 can infect the placenta and is not associated with specific placental histopathology: a series of 19 placentas from COVID-19-positive mothers. Mod. Pathol. 2020; 33(11): 2092-103. https://dx.doi.org/10.1038/s41379-020-0639-4.
  34. Shimao Y., Yamauchi A., Ohtsuka T., Terao K., Kodama Y., Yamada N. et al. C4d deposition and CD39 downregulation in the placental infection by SARS-CoV-2. Pathol. Int. 2022; 72(4): 267-9. https://dx.doi.org/10.1111/pin.13214.
  35. 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.2020.12.44-52.
  36. Debelenko L., Katsyv I., Chong A.M., Peruyero L., Szabolcs M., Uhlemann A.C. Trophoblast damage with acute and chronic intervillositis: disruption of placental barrier by SARS-CoV-2. Hum. Pathol. 2020; 109: 69-79. https://dx.doi.org/10.1016/j.humpath.2020.12.004.
  37. Song W.C., FitzGerald G.A. COVID-19, microangiopathy, hemostatic activation, and complement. J. Clin. Invest. 2020; 130(8): 3950-3. https://dx.doi.org/10.1172/JCI140183.
  38. Agostinis C., Toffoli M., Spazzapan M., Balduit A., Zito G., Mangogna A. et al. SARS-CoV-2 modulates virus receptor expression in placenta and can induce trophoblast fusion, inflammation and endothelial permeability. Front. Immunol. 2022; 13: 957224. https://dx.doi.org/10.3389/fimmu.2022.957224.
  39. Kotlyar A.M., Grechukhina O., Chen A., Popkhadze S., Grimshaw A., Tal O. et al. Vertical transmission of coronavirus disease 2019: a systematic review and meta-analysis. Am. J. Obstet. Gynecol. 2021; 224(1): 35-53. https://dx.doi.org/10.1016/j.ajog.2020.07.049.
  40. Li M., Chen L., Zhang J., Xiong C., Li X. The SARS-CoV-2 receptor ACE2 expression of maternal-fetal interface and fetal organs by single-cell transcrip-tome study. PLoS One. 2020; 15(4): e0230295. https://dx.doi.org/10.1371/journal.pone.0230295.
  41. Sayad B., Mohseni Afshar Z., Mansouri F., Salimi M., Miladi R., Rahimi S. et al. Pregnancy, preeclampsia, and COVID-19: susceptibility and mechanisms: a review study. Int. J. Fertil. Steril. 2022; 16(2): 64-9. https://dx.doi.org/10.22074/IJFS.2022.539768.1194.
  42. Jing Y., Run-Qian L., Hao-Ran W., Hao-Ran C., Ya-Bin L., Yang G. et al. Potential influence of COVID-19/ACE2 on the female reproductive system. Mol. Hum. Reprod. 2020; 26(6): 367-73. https://dx.doi.org/10.1093/molehr/gaaa030.
  43. Levy A., Yagil Y., Bursztyn M., Barkalifa R., Scharf S., Yagil C. ACE2 expression and activity are enhanced during pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008; 295(6): 1953-61. https://dx.doi.org/10.1152/ajpregu.90592.2008.
  44. Valdés G., Neves L.A., Anton L., Corthorn J., Chacón C., Germain A.M. et al. Distribution of angiotensin-(1-7) and ACE2 in human placentas of normal and pathological pregnancies. Placenta. 2006; 27(2-3): 200-7. https://dx.doi.org/10.1016/j.placenta.2005.02.015.
  45. Pique-Regi R., Romero R., Tarca A.L., Luca F., Xu Y., Alazizi A. et al. Does the human placenta express the canonical cell entry mediators for SARS-CoV-2? Elife. 2020; 9: e58716. https://dx.doi.org/10.7554/eLife.58716.
  46. Garrido-Pontnou M., Navarro A., Camacho J., Crispi F., Alguacil-Guillén M., Moreno-Baró A. Diffuse trophoblast damage is the hallmark of SARS-CoV-2-associated fetal demise. Mod. Pathol. 2021; 34(9): 1704-9. https://dx.doi.org/10.1038/s41379-021-00827-5.
  47. Raschetti R., Vivanti A.J., Vauloup-Fellous C., Loi B., Benachi A., De Luca D. Synthesis and systematic review of reported neonatal SARS-CoV-2 infections. Nat. Commun. 2020; 11(1): 5164. https://dx.doi.org/10.1038/s41467-020-18982-9.
  48. Bouachba A., Allias F., Nadaud B., Massardier J., Mekki Y., Bouscambert Duchamp M. et al. Placental lesions and SARS-Cov-2 infection: diffuse placenta damage associated to poor fetal outcome. Placenta. 2021; 112: 97-104. https://dx.doi.org/1010.1016/j.placenta.2021.07.288.
  49. Щеголев А.И., Куликова Г.В., Ляпин В.М., Шмаков Р.Г., Сухих Г.Т. Количество синцитиальных узлов и экспрессия VEGF в ворсинках плаценты у роженицы с COVID-19 зависит от тяжести заболевания. Бюллетень экспериментальной биологии и медицины. 2021; 171(3): 399-403. [Shchegolev A.I., Kulikova G.V., Lyapin V.M., Shmakov R.G., Sukhikh G.T. The number of syncytial knots and VEGF expression in placental villi in parturient woman with COVID-19 depends on the disease severity. Bulletin of Experimental Biology and Medicine. 2021; 171(3): 399-403 (in Russian)]. https://dx.doi.org/10.1007/s10517-021-05236-x.
  50. Wadman M. Studies reveal dangers of SARS-CoV-2 infection in pregnancy. Science. 2022; 375(6578): 253. https://dx.doi.org/110.1126/science.ada0233.
  51. Зазерская И.Е., Годзоева А.О., Рощина Т.Ю., Беляева О.А., Рябоконь Н.Р., Ли О.А., Осипова Н.А., Руденко К.А. Инфекция COVID-19 при беременности: гистопатология плаценты и перинатальные исходы. Анализ серии случаев. Акушерство и гинекология. 2022; 3: 156-64. [Zazerskaya I.E., Godzoeva A.O., Roshchina T.Yu., Belyaeva O.A., Ryabokon’ N.R., Li O.A., Osipova N.A., Rudenko K.A. COVID-19 infection in pregnancy: placental histopathology and perinatal outcomes. Case series analysis. Obstetrics and Gynecology. 2022; (3): 156-64. (in Russian)]. https://dx.doi.org/10.18565/aig.2022.3.156-164.
  52. 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.
  53. Marchand G., Patil A.S., Masoud A.T., Ware K., King A., Ruther S. et al. Systematic review and meta-analysis of COVID-19 maternal and neonatal clinical features and pregnancy outcomes up to June 3, 2021. AJOG Glob. Rep. 2022; 2(1): 100049. https://dx.doi.org/10.1016/j.xagr.2021.100049.
  54. Roberts D.J., Edlow A.G., Romero R.J., Coyne C.B., Ting D.T., Hornick J.L. et al.; National Institutes of Health/Eunice Kennedy Shriver National Institute of Child Health and Human Development SARS-CoV-2 Placental Infection Workshop. A standardized definition of placental infection by SARS-CoV-2, a con-sensus statement from the National Institutes of Health/Eunice Kennedy Shriver National Institute of Child Health and Human Development SARS-CoV-2 Placental Infection Workshop. Am. J. Obstet. Gynecol. 2021; 225(6): 593.e1-593.e9. https://dx.doi.org/10.1016/j.ajog.2021.07.029.
  55. Mendoza M., Garcia-Ruiz I., Maiz N., Rodo C., Garcia-Manau P., Serrano B. et al. Pre-eclampsia-like syndrome induced by severe COVID-19: a prospective observational study. BJOG. 2020; 127(11): 1374-80. https://dx.doi.org/10.1111/1471-0528.16339.
  56. Fabre M., Calvo P., Ruiz-Martinez S., Peran M., Oros D., Medel-Martinez A. et al. Frequent placental SARS-CoV-2 in patients with COVID-19-associated hypertensive disorders of pregnancy. Fetal Diagn. Ther. 2021; 48(11-12): 801-11. https://dx.doi.org/10.1159/000520179.
  57. Wu H., Liao S., Wang Y., Guo M., Lin X., Wu J. et al. Molecular evidence suggesting the persistence of residual SARS-CoV-2 and immune responses in the placentas of pregnant patients recovered from COVID-19. Cell Prolif. 2021; 54(9): e13091. https://dx.doi.org/10.1111/cpr.13091.
  58. Babal P., Krivosikova L., Sarvaicova L., Deckov I., Szemes T., Sedlackova T. et al. Intrauterine fetal demise after uncomplicated COVID-19: what can we learn from the case? Viruses. 2021; 13(12): 2545. https://dx.doi.org/10.3390/v13122545.
  59. Zhang L., Richards A., Barrasa M.I., Hughes S,H., Young R.A., Jaenisch R. Reverse-transcribed SARS-CoV-2 RNA can integrate into the genome of cultured human cells and can be expressed in patient-derived tissues. Proc. Natl. Acad. Sci. USA. 2021; 118(21): 2105968118. https://dx.doi.org/10.1073/pnas.2105968118.
  60. Zhang L., Bisht P., Flamier A., Barrasa M.I., Friesen M., Richards A. et al. LINE1-mediated reverse transcription and genomic integration of SARS-CoV-2 mRNA detected in virus-infected but not in viral mRNA-transfected cells. Viruses. 2023; 15(3): 629. https://dx.doi.org/10.3390/v15030629.

Received 28.01.2024

Accepted 04.03.2024

About the Authors

Natalya B. Pilkevich, Dr. Sci. (Med), Professor of the Department of Pathology, Belgorod State National Research University, 308015, Russia, Belgorod, Victory, str., 85,
+7(980)388-30-62, pilkevich@bsu.edu.ru, https://orcid.org/0000-0001-7260-4629, SPIN: 5422-3042, Author ID: 1191419.
Vera A. Markovskaya, PhD (Bio), Head of the Department of Pathology, Belgorod State National Research University, 308015, Russia, Belgorod, Victory, str., 85,
markovskaya @bsu.edu.ru, https://orcid.org/0000-0003-4410-9318
Ruslan R. Khabibullin, Senior Lecturer of the Department of Human Anatomy and Histology, Belgorod State National Research University, 308015, Russia, Belgorod,
Victory, str., 85; Head of the Pathological Anatomy Department of Immunohistochemistry, pathologist, Belgorod Pathological Anatomy Bureau, habibullin@bsu.edu.ru,
https://orcid.org/0000-0002-0887-2378
Olga V. Yavorskaya, teacher of the Medical College, Belgorod State National Research University, 308015, Russia, Belgorod, Victory, str., 85, yavorskaya @bsu.edu.ru
Anastasia P. Smirnova, student of the Medical Institute, Belgorod State National Research University, 308015, Russia, Belgorod, Victory, str., 85, 1330007@bsu.edu.ru,
https://orcid.org/0009-0001-3087-0037
Corresponding author: Natalya B. Pilkevich, pilkevich@bsu.edu.ru

Similar Articles

№5 / 2024
Dvoinishnikova A.O., Shebzukhova Z.R., Pronin S.M., Khabas G.N.
Early endometrial cancer in patients with congenital malformation of the genital organs
№6 / 2024
Yarygina T.A., Gasanova R.M., Marzoeva O.V., Sypchenko E.V, Leonova E.I., Lyapin V.M., Shchegolev A.I., Gus A.I.
Analysis of pathomorphological characteristics of the placental structure in cases of prenatally diagnosed fetal congenital heart disease
№10 / 2024
Keshchyan L.V., Lyalichkina N.A., Shuginin I.O.
Psychological aspects of obstetric and perinatal pathology
№7 / 2024
Lyushnina D.G., Tetruashvili N.K., Shubina Je., Rogacheva M.S., Zaretskaya N.V., Bolshakova A.S., Barkov I.Yu., Sadelov I.O., Pak V.S., Bokeriya E.L., Trofimov D.Yu.
Chromosomal abnormalities in nonimmune hydrops fetalis: diagnosis and management of pregnancy
№8 / 2024
Shabanova N.E.
Urinary tract infections in pregnant women
By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.