Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
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Effects and safety of COVID-19 vaccination on assisted reproductive technology and pregnancy: A comprehensive review and joint statements of the KSRM, the KSRI, and the KOSAR

  • Received : 2022.01.22
  • Accepted : 2022.02.08
  • Published : 2022.03.31
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Abstract

Humanity is in the midst of the coronavirus disease 2019 (COVID-19) pandemic, and vaccines-including mRNA vaccines-have been developed at an unprecedented speed. It is necessary to develop guidelines for vaccination for people undergoing treatment with assisted reproductive technology (ART) and for pregnancy-related situations based on the extant laboratory and clinical data. COVID-19 vaccines do not appear to adversely affect gametes, embryos, or implantation; therefore, active vaccination is recommended for women or men who are preparing for ART. The use of intravenous immunoglobulin G (IVIG) for the treatment of immune-related infertility is unlikely to impact the effectiveness of the vaccines, so COVID-19 vaccines can be administered around ART cycles in which IVIG is scheduled. Pregnant women have been proven to be at risk of severe maternal and neonatal complications from COVID-19. It does not appear that COVID-19 vaccines harm pregnant women or fetuses; instead, they have been observed to deliver antibodies against severe acute respiratory syndrome coronavirus 2 (SARSCoV-2) to the fetus. Accordingly, it is recommended that pregnant women receive COVID-19 vaccination. There is no rationale for adverse effects, or clinical cases of adverse reactions, in mothers or neonates after COVID-19 vaccination in lactating women. Instead, antibodies to SARS-CoV-2 can be delivered through breast milk. Therefore, breastfeeding mothers should consider vaccination. In summary, active administration of COVID-19 vaccines will help ensure the safe implementation of ART, pregnancy, and breastfeeding.

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References

  1. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ, et al. COVID-19: consider cytokine storm syndromes and immunosuppression. Lancet 2020;395:1033-4. https://doi.org/10.1016/s0140-6736(20)30628-0
  2. de Kretser DM, Loveland KL, Meinhardt A, Simorangkir D, Wreford N. Spermatogenesis. Hum Reprod 1998;13 Suppl 1:1-8.
  3. Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1986;1:81-7. https://doi.org/10.1093/oxfordjournals.humrep.a136365
  4. Szekeres-Bartho J, Markert UR, Varla-Leftherioti M. Immunology in reproduction. J Reprod Immunol 2015;108:1. https://doi.org/10.1016/j.jri.2015.03.003
  5. Reis FM, Bouissou DR, Pereira VM, Camargos AF, dos Reis AM, Santos RA. Angiotensin-(1-7), its receptor Mas, and the angiotensin-converting enzyme type 2 are expressed in the human ovary. Fertil Steril 2011;95:176-81. https://doi.org/10.1016/j.fertnstert.2010.06.060
  6. Vaz-Silva J, Carneiro MM, Ferreira MC, Pinheiro SV, Silva DA, Silva-Filho AL, et al. The vasoactive peptide angiotensin-(1-7), its receptor Mas and the angiotensin-converting enzyme type 2 are expressed in the human endometrium. Reprod Sci 2009;16:247-56. https://doi.org/10.1177/1933719108327593
  7. Stanley KE, Thomas E, Leaver M, Wells D. Coronavirus disease-19 and fertility: viral host entry protein expression in male and female reproductive tissues. Fertil Steril 2020;114:33-43. https://doi.org/10.1016/j.fertnstert.2020.05.001
  8. Seymen CM. The other side of COVID-19 pandemic: effects on male fertility. J Med Virol 2021;93:1396-402. https://doi.org/10.1002/jmv.26667
  9. Diaz P, Reddy P, Ramasahayam R, Kuchakulla M, Ramasamy R. COVID-19 vaccine hesitancy linked to increased internet search queries for side effects on fertility potential in the initial rollout phase following Emergency Use Authorization. Andrologia 2021;53:e14156.
  10. ESHRE COVID-19 Working Group. SARS-COV-2 and service adaptation: an update. ESHRE guidance on recommencing ART treatments [Internet]. Grimbergen: European Society of Human Reproduction and Embryology; 2021 [cited 2022 Jan 30]. Available from: https://www.eshre.eu/-/media/sitecore-files/Guidelines/COVID19/SARSCOV2-and-service-adaptation_08June2021.pdf.
  11. Ory S, Veiga A, Horton M, Gianaroli L. Joint IFFS/ESHRE statement on COVID-19 vaccination for pregnant women and those considering pregnancy. Hum Reprod Open 2021;2021:hoab016. https://doi.org/10.1093/hropen/hoab016
  12. ASRM Coronavirus/COVID-19 Task Force. Update No. 13: variants, vaccines, and vaccination [Internet]. Washington, DC: American Society for Reproductive Medicine; 2021 [cited 2021 Dec 17]. Available from: https://www.asrm.org/globalassets/asrm/asrm-content/news-and-publications/covid-19/covidtaskforceupdate13.pdf.
  13. ASRM Coronavirus/COVID-19 Task Force. Update No. 11: COVID-19 vaccination [Internet]. Washington, DC: American Society for Reproductive Medicine; 2020 [cited 2021 Dec 17]. Available from: https://www.asrm.org/globalassets/asrm/asrm-content/newsand-publications/covid-19/covidtaskforceupdate11.pdf.
  14. U.S. Food and Drug Administration. Comirnaty and pfizer-bioNTech COVID-19 vaccine [Internet]. Silver Spring: U.S. Food and Drug; 2021 [cited 2021 Dec 17]. Available from: https://www.fda.gov/media/144413/download.
  15. Orvieto R, Noach-Hirsh M, Segev-Zahav A, Haas J, Nahum R, Aizer A. Does mRNA SARS-CoV-2 vaccine influence patients' performance during IVF-ET cycle? Reprod Biol Endocrinol 2021;19:69. https://doi.org/10.1186/s12958-021-00757-6
  16. Gonzalez DC, Nassau DE, Khodamoradi K, Ibrahim E, Blachman-Braun R, Ory J, et al. Sperm parameters before and after COVID-19 mRNA vaccination. JAMA 2021;326:273-4. https://doi.org/10.1001/jama.2021.9976
  17. Safrai M, Herzberg S, Imbar T, Reubinoff B, Dior U, Ben-Meir A. The BNT162b2 mRNA Covid-19 vaccine does not impair sperm parameters. Reprod Med Online 2022 Jan 26 [Epub]. https://doi.org/10.1016/j.rbmo.2022.01.008.
  18. Sung N, Khan SA, Yiu ME, Jubiz G, Salazar MD, Skariah A, et al. Reproductive outcomes of women with recurrent pregnancy losses and repeated implantation failures are significantly improved with immunomodulatory treatment. J Reprod Immunol 2021;148:103369. https://doi.org/10.1016/j.jri.2021.103369
  19. Robertson SA, Jin M, Yu D, Moldenhauer LM, Davies MJ, Hull ML, et al. Corticosteroid therapy in assisted reproduction - immune suppression is a faulty premise. Hum Reprod 2016;31:2164-73. https://doi.org/10.1093/humrep/dew186
  20. Pirtea P, Scott RT, de Ziegler D, Ayoub JM. Recurrent implantation failure: how common is it? Curr Opin Obstet Gynecol 2021;33:207-12. https://doi.org/10.1097/GCO.0000000000000698
  21. Dimitriadis E, Menkhorst E, Saito S, Kutteh WH, Brosens JJ. Recurrent pregnancy loss. Nat Rev Dis Primers 2020;6:98. https://doi.org/10.1038/s41572-020-00228-z
  22. Centers for Disease Control and Prevention. ACIP vaccine recommendations and guidelines: Advisory Committee on Immunization Practices (ACIP) [Internet]. Atlanta: Centers for Disease Control and Prevention; 2021 [cited 2021 Dec 17]. Available from: https://www.cdc.gov/vaccines/hcp/acip-recs/index.html.
  23. UK Health Security Agency. Contraindications and special considerations: the green book, chapter 6. Information for public health professionals on immunisation [Internet]. London: UK Health Security Agency; 2017 [cited 2021 Dec 17]. Available from: https://www.gov.uk/government/publications/contraindications-andspecial-considerations-the-green-book-chapter-6.
  24. UK Health Security Agency. COVID-19: the green book, chapter 14a. Information for public health professionals on immunisation [Internet]. London: UK Health Security Agency; 2022 [cited 2021 Dec 17]. Available from: https://www.gov.uk/government/publications/covid-19-the-green-book-chapter-14a.
  25. Kearns P, Siebert S, Willicombe M, Gaskell C, Kirkham A, Pirrie S, et al. Examining the immunological effects of COVID-19 vaccination in patients with conditions potentially leading to diminished immune response capacity: The OCTAVE trial. Lancet 2021 Aug 23 [Epub]. https://doi.org/10.2139/ssrn.3910058.
  26. Woodworth KR, Olsen EO, Neelam V, Lewis EL, Galang RR, Oduyebo T, et al. Birth and infant outcomes following laboratory-confirmed SARS-CoV-2 infection in pregnancy-SET-NET, 16 jurisdictions, March 29-October 14, 2020. MMWR Morb Mortal Wkly Rep 2020;69:1635-40. https://doi.org/10.15585/mmwr.mm6944e2
  27. Zambrano LD, Ellington S, Strid P, Galang RR, Oduyebo T, Tong VT, et al. 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;69:1641-7. https://doi.org/10.15585/mmwr.mm6944e3
  28. Villar J, Ariff S, Gunier RB, Thiruvengadam R, Rauch S, Kholin A, et al. Maternal and neonatal morbidity and mortality among pregnant women with and without COVID-19 infection: the INTERCOVID multinational cohort study. JAMA Pediatr 2021;175:817-26. https://doi.org/10.1001/jamapediatrics.2021.1050
  29. Jering KS, Claggett BL, Cunningham JW, Rosenthal N, Vardeny O, Greene MF, et al. Clinical characteristics and outcomes of hospitalized women giving birth with and without COVID-19. JAMA Intern Med 2021;181:714-7. https://doi.org/10.1001/jamainternmed.2020.9241
  30. Vivanti AJ, Vauloup-Fellous C, Prevot S, Zupan V, Suffee C, Do Cao J, et al. Transplacental transmission of SARS-CoV-2 infection. Nat Commun 2020;11:3572. https://doi.org/10.1038/s41467-020-17436-6
  31. Shende P, Gaikwad P, Gandhewar M, Ukey P, Bhide A, Patel V, et al. Persistence of SARS-CoV-2 in the first trimester placenta leading to transplacental transmission and fetal demise from an asymptomatic mother. Hum Reprod 2021;36:899-906. https://doi.org/10.1093/humrep/deaa367
  32. Rubin R. Pregnant people's paradox: excluded from vaccine trials despite having a higher risk of COVID-19 complications. JAMA 2021;325:1027-8. https://doi.org/10.1001/jama.2021.2264
  33. Feldman RA, Fuhr R, Smolenov I, Mick Ribeiro A, Panther L, Watson M, et al. mRNA vaccines against H10N8 and H7N9 influenza viruses of pandemic potential are immunogenic and well tolerated in healthy adults in phase 1 randomized clinical trials. Vaccine 2019;37:3326-34. https://doi.org/10.1016/j.vaccine.2019.04.074
  34. Alberer M, Gnad-Vogt U, Hong HS, Mehr KT, Backert L, Finak G, et al. Safety and immunogenicity of a mRNA rabies vaccine in healthy adults: an open-label, non-randomised, prospective, firstin-human phase 1 clinical trial. Lancet 2017;390:1511-20. https://doi.org/10.1016/S0140-6736(17)31665-3
  35. Richner JM, Himansu S, Dowd KA, Butler SL, Salazar V, Fox JM, et al. Modified mRNA vaccines protect against Zika virus infection. Cell 2017;168:1114-25.e10. https://doi.org/10.1016/j.cell.2017.02.017
  36. Polack FP, Thomas SJ, Kitchin N, Absalon J, Gurtman A, Lockhart S, et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med 2020;383:2603-15. https://doi.org/10.1056/NEJMoa2034577
  37. Baden LR, El Sahly HM, Essink B, Kotloff K, Frey S, Novak R, et al. Efficacy and safety of the mRNA-1273 SARS-CoV-2 vaccine. N Engl J Med 2021;384:403-16. https://doi.org/10.1056/NEJMoa2035389
  38. Male V. Are COVID-19 vaccines safe in pregnancy? Nat Rev Immunol 2021;21:200-1. https://doi.org/10.1038/s41577-021-00525-y
  39. Shanes ED, Otero S, Mithal LB, Mupanomunda CA, Miller ES, Goldstein JA. Severe acute respiratory syndrome coronavirus 2 (SARSCoV-2) vaccination in pregnancy: measures of immunity and placental histopathology. Obstet Gynecol 2021;138:281-3.
  40. Shimabukuro TT, Kim SY, Myers TR, Moro PL, Oduyebo T, Panagiotakopoulos L, et al. Preliminary findings of mRNA Covid-19 vaccine safety in pregnant persons. N Engl J Med 2021;384:2273-82. https://doi.org/10.1056/NEJMoa2104983
  41. Gray KJ, Bordt EA, Atyeo C, Deriso E, Akinwunmi B, Young N, et al. Coronavirus disease 2019 vaccine response in pregnant and lactating women: a cohort study. Am J Obstet Gynecol 2021;225:303.e1-303.e17.
  42. Beharier O, Plitman Mayo R, Raz T, Nahum Sacks K, Schreiber L, Suissa-Cohen Y, et al. Efficient maternal to neonatal transfer of antibodies against SARS-CoV-2 and BNT162b2 mRNA COVID-19 vaccine. J Clin Invest 2021;131:e150319. https://doi.org/10.1172/JCI150319
  43. Golan Y, Prahl M, Cassidy A, Lin CY, Ahituv N, Flaherman VJ, et al. Evaluation of messenger RNA from COVID-19 BTN162b2 and mRNA-1273 vaccines in human milk. JAMA Pediatr 2021;175:1069-71. https://doi.org/10.1001/jamapediatrics.2021.1929
  44. Low JM, Gu Y, Ng MS, Amin Z, Lee LY, Ng YP, et al. Codominant IgG and IgA expression with minimal vaccine mRNA in milk of BNT 162b2 vaccinees. NPJ Vaccines 2021;6:105. https://doi.org/10.1038/s41541-021-00370-z
  45. Garg I, Shekhar R, Sheikh AB, Pal S. COVID-19 vaccine in pregnant and lactating women: a review of existing evidence and practice guidelines. Infect Dis Rep 2021;13:685-99. https://doi.org/10.3390/idr13030064
  46. Kelly JC, Carter EB, Raghuraman N, Nolan LS, Gong Q, Lewis AN, et al. Anti-severe acute respiratory syndrome coronavirus 2 antibodies induced in breast milk after Pfizer-BioNTech/BNT162b2 vaccination. Am J Obstet Gynecol 2021;225:101-3. https://doi.org/10.1016/j.ajog.2021.03.031
  47. P erl SH, Uzan-Yulzari A, Klainer H, Asiskovich L, Youngster M, Rinott E, et al. SARS-CoV-2-specific antibodies in breast milk after COVID-19 vaccination of breastfeeding women. JAMA 2021;325:2013-4. https://doi.org/10.1001/jama.2021.5782
  48. Collier AY, McMahan K, Yu J, Tostanoski LH, Aguayo R, Ansel J, et al. Immunogenicity of COVID-19 mRNA vaccines in pregnant and lactating women. JAMA 2021;325:2370-80. https://doi.org/10.1001/jama.2021.7563
  49. Lechosa-Muniz C, Paz-Zulueta M, Mendez-Legaza JM, Irure-Ventura J, Cuesta Gonzalez R, Calvo Montes J, et al. Induction of SARSCoV-2-Specific IgG and IgA in serum and milk with different SARS-CoV-2 vaccines in breastfeeding women: a cross-sectional study in Northern Spain. Int J Environ Res Public Health 2021;18:8831. https://doi.org/10.3390/ijerph18168831
  50. Schwartz A, Nir O, Toussia-Cohen S, Leibovich L, Strauss T, Asraf K, et al. Presence of SARS-CoV-2 antibodies in lactating women and their infants following BNT162b2 messenger RNA vaccine. Am J Obstet Gynecol 2021;225:577-9. https://doi.org/10.1016/j.ajog.2021.07.016
  51. Golan Y, Prahl M, Cassidy AG, Gay C, Wu AH, Jigmeddagva U, et al. COVID-19 mRNA vaccination in lactation: assessment of adverse effects and transfer of anti-SARS-CoV2 antibodies from mother to child. medRxiv [Preprint]. 2021 [cited 2022 Feb 20]. Available from: https://doi.org/10.1101/2021.03.09.21253241.
  52. Bertrand K, Honerkamp-Smith G, Chambers CD. Maternal and child outcomes reported by breastfeeding women following messenger RNA COVID-19 vaccination. Breastfeed Med 2021;16:697-701. https://doi.org/10.1089/bfm.2021.0169
  53. McLaurin-Jiang S, Garner CD, Krutsch K, Hale TW. Maternal and child symptoms following COVID-19 vaccination among breastfeeding mothers. Breastfeed Med 2021;16:702-9. https://doi.org/10.1089/bfm.2021.0079