The site of the Media Sphera Publishers contains materials intended solely for healthcare professionals.
By closing this message, you confirm that you are a certified medical professional or a student of a medical educational institution.

Sakhautdinova I.V.

Bashkir State Medical University

Zasyadkin I.S.

Bashkir State Medical University

Khamad’yanova A.U.

Bashkir State Medical University

Tayupova I.M.

Bashkir State Medical University

Kuleshova T.P.

Bashkir State Medical University

Perinatal outcomes and immunological changes in pregnant women with new COVID-19 coronavirus infection

Authors:

Sakhautdinova I.V., Zasyadkin I.S., Khamad’yanova A.U., Tayupova I.M., Kuleshova T.P.

More about the authors

Read: 1332 times


To cite this article:

Sakhautdinova IV, Zasyadkin IS, Khamad’yanova AU, Tayupova IM, Kuleshova TP. Perinatal outcomes and immunological changes in pregnant women with new COVID-19 coronavirus infection. Russian Bulletin of Obstetrician-Gynecologist. 2023;23(5):38‑44. (In Russ.)
https://doi.org/10.17116/rosakush20232305138

Recommended articles:
The practice of using medi­cal abortion in the world. Russian Bulletin of Obstetrician-Gynecologist. 2025;(1):19-24
Acute kidney injury during pregnancy with favo­rable obstetric and nephrological outcome. Russian Bulletin of Obstetrician-Gynecologist. 2025;(1):65-70
Asplenia — a new cause of thro­mbosis in pregnant women?. Russian Bulletin of Obstetrician-Gynecologist. 2025;(1):71-76
Modern aspe­cts of gestational diabetes mellitus: defi­nition, risk factors. Russian Bulletin of Obstetrician-Gynecologist. 2025;(2):35-41
Hormonal contraception methods and multiple scle­rosis. S.S. Korsakov Journal of Neurology and Psychiatry. 2025;(1):24-30
Reproductive health of women with hepa­titis C (literature review and own data). Russian Journal of Human Reproduction. 2025;(1):12-20

References:

  1. WHO Coronavirus (COVID-19) Dashboard https://covid19.who.int/
  2. Merad M, Blish CA, Sallusto F, Iwasaki A. The immunology and immunopathology of COVID-19. Science. 2022;375:6585:1122-1127. https://doi.org/10.1126/science.abm8108
  3. Wang Y, Shi L, Que J, Lu Q, Liu L, Lu Z, Xu Y, Liu J, Sun Y, Meng S, Yuan K, Ran M, Lu L, Bao Y, Shi J. The impact of quarantine on mental health status among general population in China during the COVID-19 pandemic. Mol Psychiatry. 2021;26:9:4813-4822. https://doi.org/10.1038/s41380-021-01019-y
  4. Aghaeepour N, Ganio EA, Mcilwain D, Tsai AS, Tingle M, Van Gassen S, Gaudilliere DK, Baca Q, McNeil L, Okada R, Ghaemi MS, Furman D, Wong RJ, Winn VD, Druzin ML, El-Sayed YY, Quaintance C, Gibbs R, Darmstadt GL, Shaw GM, Stevenson DK, Tibshirani R, Nolan GP, Lewis DB, Angst MS, Gaudilliere B. An immune clock of human pregnancy. Sci Immunol. 2017;2:15:eaan2946. https://doi.org/10.1126/sciimmunol.aan2946
  5. Mor G, Aldo P, Alvero AB. The unique immunological and microbial aspects of pregnancy. Nat Rev Immunol. 2017;17:8:469-482.  https://doi.org/10.1038/nri.2017.64
  6. Jamieson DJ, Rasmussen SA. An update on COVID-19 and pregnancy. Am J Obstet Gynecol. 2022;226:2:177-186.  https://doi.org/10.1016/j.ajog.2021.08.054
  7. Wastnedge EAN, Reynolds RM, van Boeckel SR, Stock SJ, Denison FC, Maybin JA, Critchley HOD. Pregnancy and COVID-19. Physiol Rev. 2021;101:1:303-318.  https://doi.org/10.1152/physrev.00024.2020
  8. Gil-Etayo FJ, Suàrez-Fernández P, Cabrera-Marante O, Arroyo D, Garcinuño S, Naranjo L, Pleguezuelo DE, Allende LM, Mancebo E, Lalueza A, Díaz-Simón R, Paz-Artal E, Serrano A. T-Helper cell subset response is a determining factor in COVID-19 progression. Front Cell Infect Microbiol. 2021;11:624483. https://doi.org/10.3389/fcimb.2021.624483
  9. Chen Z, John Wherry E. T cell responses in patients with COVID-19. Nat Rev Immunol. 2020;20:9:529-536.  https://doi.org/10.1038/s41577-020-0402-6
  10. Alberca RW, Pereira NZ, Oliveira L, Gozzi-Silva SC, Sato MN. Pregnancy, Viral Infection, and COVID-19. Front Immunol. 2020;11:1672. https://doi.org/10.3389/fimmu.2020.01672
  11. Pavel AB, Glickman JW, Michels JR, Kim-Schulze S, Miller RL, Guttman-Yassky E. Th2/Th1 cytokine imbalance is associated with higher COVID-19 risk mortality. Front Genet. 2021;12:706902. https://doi.org/10.3389/fgene.2021.706902
  12. Hsieh W-C, Lai E-Y, Liu Y-T, Wang Y-F, Tzeng Y-S, Cui L, Lai Y-J, Huang H-C, Huang J-H, Ni H-C, Tsai D-Y, Liang J-J, Liao C-C, Lu Y-T, Jiang L, Liu M-T, Wang J-T, Chang S-Y, Chen C-Y, Tsai H-C, Chang Y-M, Wernig G, Li C-W, Lin K-I, Lin Y-L, Tsai H-K, Huang Y-T, Chen S-Y. NK cell receptor and ligand composition influences the clearance of SARS-CoV-2. J Clin Invest. 2021;131:21:e146408. https://doi.org/10.1172/JCI146408
  13. Lampé R, Kövér Á, Szűcs S, Pál L, Árnyas E, Ádány R, Póka R. Phagocytic index of neutrophil granulocytes and monocytes in healthy and preeclamptic pregnancy. J Reprod Immunol. 2015;107:26-30.  https://doi.org/10.1016/j.jri.2014.11.001
  14. Siiteri PK, Febres F, Clemens LE, Chang RJ, Gondos B, Stites D. Progesterone and maintenance of pregnancy: is progesterone nature’s immunosuppressant? Ann New York Academy of Sciences. 1977;286:384-397.  https://doi.org/10.1111/j.1749-6632.1977.tb29431.x
  15. Hall OJ, Nachbagauer R, Vermillion MS, Fink AL, Phuong V, Krammer F, Klein SL. Progesterone-based Contraceptives reduce adaptive immune responses and protection against sequential influenza a virus infections. J Virol. 2017;91:8:e02160-16.  https://doi.org/10.1128/JVI.02160-16
  16. Wei R, Lai N, Zhao L, Zhang Z, Zhu X, Guo Q, Chu C, Fu X, Li X. Dendritic cells in pregnancy and pregnancy-associated diseases. Biomed Pharmacother. 2021;133:110921. https://doi.org/10.1016/j.biopha.2020.110921
  17. Reizis B. Plasmacytoid dendritic cells. Development, regulation, and function. Immunity. 2019;50:1:37-50.  https://doi.org/10.1016/j.immuni.2018.12.027
  18. Vanders RL, Gibson PG, Murphy VE, Wark PA. Plasmacytoid dendritic cells and CD8 T cells from pregnant women show altered phenotype and function following H1N1/09 infection. J Infect Dis. 2013;208:7:1062-1070. https://doi.org/10.1093/infdis/jit296
  19. Lee JS, Shin EC. The type I interferon response in COVID-19: implications for treatment. Nat Rev Immunol. 2020;20:10:585-586.  https://doi.org/10.1038/s41577-020-00429-3
  20. Khanmohammadi S, Rezaei N. Role of Toll-like receptors in the pathogenesis of COVID-19. J Med Virol. 2021;93:5:2735-2739. https://doi.org/10.1002/jmv.26826
  21. Abu-Raya B, Michalski C, Sadarangani M, Lavoie PM. Maternal immunological adaptation during normal pregnancy. Front Immunol. 2020;11:575197. https://doi.org/10.3389/fimmu.2020.575197
  22. Mor G, Cardenas I, Abrahams V, Guller S. Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci. 2011;1221:1:80-87.  https://doi.org/10.1111/j.1749-6632.2010.05938.x
  23. Richani K, Soto E, Romero R, Espinoza J, Chaiworapongsa T, Nien JK, Edwin S, Kim YM, Hong JS, Mazor M. Normal pregnancy is characterized by systemic activation of the complement system. J Matern Fetal Neonatal Med. 2005;17:4:239-245.  https://doi.org/10.1080/14767050500072722
  24. Derzsy Z, Prohászka Z, Rigó J Jr, Füst G, Molvarec A. Activation of the complement system in normal pregnancy and preeclampsia. Mol Immunol. 2010;47;7-8:1500-1506. https://doi.org/10.1016/j.molimm.2010.01.021
  25. Java A, Apicelli AJ, Liszewski MK, Coler-Reilly A, Atkinson JP, Kim AH, Kulkarni HS. The complement system in COVID-19: friend and foe? JCI Insight. 2020;5:15:e140711. https://doi.org/10.1172/jci.insight.140711
  26. Gralinski LE, Sheahan TP, Morrison TE, Gralinski LE, Sheahan TP, Morrison TE, Menachery VD, Jensen K, Leist SR, Whitmore A, Heise MT, Baric RS. Complement activation contributes to severe acute respiratory syndrome coronavirus pathogenesis. mBio. 2018;9:5:e01753-18.  https://doi.org/10.1128/mBio.01753-18
  27. Fodil S, Annane D. Complement inhibition and COVID-19: The Story so far. Immunotargets Ther. 2021;10:273-284.  https://doi.org/10.2147/ITT.S284830
  28. Potere N, Batticciotto A, Vecchié A, Porreca E, Cappelli A, Abbate A, Dentali F, Bonaventura A. The role of IL-6 and IL-6 blockade in COVID-19. Expert Rev Clin Immunol. 2021;17:6:601-618.  https://doi.org/10.1080/1744666X.2021.1919086
  29. Young BC, Stanic AK, Panda B, Rueda BR, Panda A. Longitudinal expression of Toll-like receptors on dendritic cells in uncomplicated pregnancy and postpartum. Am J Obstet Gynecol. 2014;210:5:445.e1-445.e4456. https://doi.org/10.1016/j.ajog.2013.11.037
  30. Patra R, Chandra Das N, Mukherjee S. Targeting human TLRs to combat COVID-19: A solution? J Med Virol. 2021;93:2:615-617.  https://doi.org/10.1002/jmv.26387
  31. Petes C, Odoardi N, Gee K. The Toll for trafficking: Toll-like receptor 7 delivery to the endosome. Front Immunol. 2017;8:1075. https://doi.org/10.3389/fimmu.2017.01075
  32. Moreno-Eutimio MA, López-Macías C, Pastelin-Palacios R. Bioinformatic analysis and identification of single-stranded RNA sequences recognized by TLR7/8 in the SARS-CoV-2, SARS-CoV, and MERS-CoV genomes. Microbes Infect. 2020;22:4-5:226-229.  https://doi.org/10.1016/j.micinf.2020.04.009
  33. Yazdanpanah F, Hamblin MR, Rezaei N. The immune system and COVID-19: Friend or foe? Life Sci. 2020;256:117900. https://doi.org/10.1016/j.lfs.2020.117900
  34. Overton EE, Goffman D, Friedman AM. The Epidemiology of COVID-19 in Pregnancy. Clin Obstet Gynecol. 2022;65:1:110-122.  https://doi.org/10.1097/GRF.0000000000000674
  35. Zambrano LD, Ellington S, Strid P, Galang RR, Oduyebo T, Tong VT, Woodworth KR, Nahabedian JF 3rd, Azziz-Baumgartner E, Gilboa SM, Meaney-Delman D. Update: Characteristics of symptomatic women of reproductive age with laboratory-confirmed SARS-CoV-2 infection by pregnancy status — United States, January 22-October 3, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:44:1641-1647. https://doi.org/10.15585/mmwr.mm6944e3
  36. Badr DA, Mattern J, Carlin A, Cordier AG, Maillart E, El Hachem L, El Kenz H, Andronikof M, De Bels D, Damoisel C, Preseau T, Vignes D, Cannie MM, Vauloup-Fellous C, Fils JF, Benachi A, Jani JC, Vivanti AJ. Are clinical outcomes worse for pregnant women at ≥20 weeks’ gestation infected with coronavirus disease 2019? A multicenter case-control study with propensity score matching. Am J Obstet Gynecol. 2020;223:5:764-768.  https://doi.org/10.1016/j.ajog.2020.07.045
  37. Lokken EM, Huebner EM, Taylor GG, Hendrickson S, Vanderhoeven J, Kachikis A, Coler B, Walker CL, Sheng JS, Al-Haddad B, McCartney SA, Kretzer NM, Resnick R, Barnhart N, Schulte V, Bergam B, Ma KK, Albright C, Larios V, Kelley L. Disease severity, pregnancy outcomes, and maternal deaths among pregnant patients with severe acute respiratory syndrome coronavirus 2 infection in Washington State. Am J Obstet Gynecol. 2021;225:1:77.e1-77.e14.  https://doi.org/10.1016/j.ajog.2020.12.1221
  38. Kotlyar AM, Grechukhina O, Chen A, Popkhadze S, Grimshaw A, Tal O, Taylor HS, Tal R. Vertical transmission of coronavirus disease 2019: a systematic review and meta-analysis. Am J Obstet Gynecol. 2021;224:1:35-53.e3.  https://doi.org/10.1016/j.ajog.2020.07.049
  39. Wei SQ, Bilodeau-Bertrand M, Liu S, Auger N. The impact of COVID-19 on pregnancy outcomes: a systematic review and meta-analysis. CMAJ. 2021;193:16:540-548.  https://doi.org/10.1503/cmaj.202604
  40. Pérez-López FR, Savirón-Cornudella R, Chedraui P, López-Baena MT, Pérez-Roncero G, Sanz-Arenal A, Narváez-Salazar M, Dieste-Pérez P, Tajada M. Obstetric and perinatal outcomes of pregnancies with COVID 19: a systematic review and meta-analysis. J Matern Fetal Neonatal Med. 2022;35:25:9742-9758. https://doi.org/10.1080/14767058.2022.2051008
  41. Adhikari EH, Moreno W, Zofkie AC, MacDonald L, McIntire DD, Collins RRJ, Spong CY. Pregnancy outcomes among women with and without severe acute respiratory syndrome Coronavirus 2 infection. JAMA Netw Open. 2020;3:11:e2029256. Published 2020 Nov 2.  https://doi.org/10.1001/jamanetworkopen.2020.29256
  42. Villar J, Ariff S, Gunier RB, Thiruvengadam R, Rauch S, Kholin A, Roggero P, Prefumo F, do Vale MS, Cardona-Perez JA, Maiz N, Cetin I, Savasi V, Deruelle P, Easter SR, Sichitiu J, Soto Conti CP, Ernawati E, Mhatre M, Teji JS, Papageorghiou AT. Maternal and neonatal morbidity and mortality among pregnant women with and without COVID-19 infection: The INTERCOVID Multinational Cohort Study. JAMA Pediatr. 2021;175:8:817-826.  https://doi.org/10.1001/jamapediatrics.2021.1050
  43. Charles CM, Osman NB, Arijama D, Matingane B, Sitoé T, Kenga D, Lorenzoni C, Luís E, de Carvalho Pacagnella R, Sacarlal J. Clinical and epidemiological aspects of SARS-CoV-2 infection among pregnant and postpartum women in Mozambique: a prospective cohort study. Reprod Health. 2022;19:1:164.  https://doi.org/10.1186/s12978-022-01469-9
  44. Angelidou A, Sullivan K, Melvin PR, Shui JE, Goldfarb IT, Bartolome R, Chaudhary N, Vaidya R, Culic I, Singh R, Yanni D, Patrizi S, Hudak ML, Parker MG, Belfort MB. Association of maternal perinatal SARS-CoV-2 infection with neonatal outcomes during the COVID-19 pandemic in Massachusetts. JAMA Netw Open. 2021;4:4:e217523. https://doi.org/10.1001/jamanetworkopen.2021.7523
  45. Metz TD, Clifton RG, Hughes BL, Sandoval G, Saade GR, Grobman WA, Manuck TA, Miodovnik M, Sowles A, Clark K, Gyamfi-Bannerman C, Mendez-Figueroa H, Sehdev HM, Rouse DJ, Tita A, Bailit J, Costantine MM, Simhan HN, Macones GA. Disease severity and perinatal outcomes of pregnant patients with coronavirus disease 2019 (COVID-19). Obstet Gynecol. 2021;137:4:571-580.  https://doi.org/10.1097/AOG.0000000000004339
  46. Katz D, Bateman BT, Kjaer K, Turner DP, Spence NZ, Habib AS, George RB, Toledano RD, Grant G, Madden HE, Butwick AJ, Lynde G, Minehart RD, Beilin Y, Houle TT, Sharpe EE, Kodali B, Bharadwaj S, Farber MK, Palanisamy A, Prabhu M, Gonzales NY, Landau R, Leffert L. The Society for obstetric anesthesia and perinatology coronavirus disease 2019 Registry: An analysis of outcomes among pregnant women delivering during the initial severe acute respiratory syndrome Coronavirus-2 outbreak in the United States. Anesth Analg. 2021;133:2:462-473.  https://doi.org/10.1213/ANE.0000000000005592
  47. Kotlyar AM, Grechukhina O, Chen A, Popkhadze S, Grimshaw A, Tal O, Taylor HS, Tal R. Vertical transmission of coronavirus disease 2019: a systematic review and meta-analysis. Am J Obstet Gynecol. 2021;224:1:35-53.  https://doi.org/10.1016/j.ajog.2020.07.049
  48. Mullins E, Hudak ML, Banerjee J, Getzlaff T, Townson J, Barnette K, Playle R, Perry A, Bourne T, Lees CC. Pregnancy and neonatal outcomes of COVID-19: coreporting of common outcomes from PAN-COVID and AAP-SONPM registries. Ultrasound Obstet Gynecol. 2021;57:4:573-581.  https://doi.org/10.1002/uog.23619
  49. Dhir SK, Kumar J, Meena J, Kumar P. Clinical features and outcome of SARS-CoV-2 infection in neonates: A Systematic review. J Trop Pediatr. 2021;67:3:fmaa059. https://doi.org/10.1093/tropej/fmaa059
  50. Jafari M, Pormohammad A, Sheikh Neshin SA, Ghorbani S, Bose D, Alimohammadi S, Basirjafari S, Mohammadi M, Rasmussen-Ivey C, Razizadeh MH, Nouri-Vaskeh M, Zarei M. Clinical characteristics and outcomes of pregnant women with COVID-19 and comparison with control patients: A systematic review and meta-analysis. Rev Med Virol. 2021;31:5:1-16.  https://doi.org/10.1002/rmv.2208
  51. Chmielewska B, Barratt I, Townsend R, Kalafat E, van der Meulen J, Gurol-Urganci I, O’Brien P, Morris E, Draycott T, Thangaratinam S, Le Doare K, Ladhani S, von Dadelszen P, Magee L, Khalil A. Effects of the COVID-19 pandemic on maternal and perinatal outcomes: a systematic review and meta-analysis. Lancet Glob Health. 2021;9:6:759-772.  https://doi.org/10.1016/S2214-109X(21)00079-6
  52. Chmielewska B, Barratt I, Townsend R, Kalafat E, van der Meulen J, Gurol-Urganci I, O’Brien P, Morris E, Draycott T, Thangaratinam S, Doare KL, Ladhani S, von Dadelszen P, Magee L, Khalil A. Effects of the COVID-19 pandemic on maternal and perinatal outcomes: a systematic review and meta-analysis. Lancet Glob Health. 2021;9:6:e758. https://doi.org/10.1016/S2214-109X(21)00079-6
  53. Prasad S, Kalafat E, Blakeway H, Townsend R, O’Brien P, Morris E, Draycott T, Thangaratinam S, Le Doare K, Ladhani S, von Dadelszen P, Magee LA, Heath P, Khalil A. Systematic review and meta-analysis of the effectiveness and perinatal outcomes of COVID-19 vaccination in pregnancy. Nat Commun. 2022;13:1:2414. https://doi.org/10.1038/s41467-022-30052-w
  54. Kalafat E, Heath P, Prasad S, O Brien P, Khalil A. COVID-19 vaccination in pregnancy. Am J Obstet Gynecol. 2022;227:2:136-147.  https://doi.org/10.1016/j.ajog.2022.05.020
  55. Shafiee A, Kohandel Gargari O, Teymouri Athar MM, Fathi H, Ghaemi M, Mozhgani SH. COVID-19 vaccination during pregnancy: a systematic review and meta-analysis. BMC Pregnancy Childbirth. 2023;23:1:45.  https://doi.org/10.1186/s12884-023-05374-2

Email Confirmation

An email was sent to test@gmail.com with a confirmation link. Follow the link from the letter to complete the registration on the site.

Email Confirmation

We use cооkies to improve the performance of the site. By staying on our site, you agree to the terms of use of cооkies. To view our Privacy and Cookie Policy, please. click here.