Longitudinal Trends of Prevalence of Neutralizing Antibody against Human Cytomegalovirus over the Past 30 Years in Japanese Women
Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women. The IgG-positivity rate to HCMV determined by enzyme immunoassay (EIA) or indirect immunofluorescence assay has decreased from approximately 10...
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| Published in | Japanese Journal of Infectious Diseases Vol. 75; no. 5; pp. 496 - 503 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Tokyo
National Institute of Infectious Diseases, Japanese Journal of Infectious Diseases Editorial Committee
30.09.2022
Japan Science and Technology Agency |
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| Abstract | Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women. The IgG-positivity rate to HCMV determined by enzyme immunoassay (EIA) or indirect immunofluorescence assay has decreased from approximately 100% to 70% over the past 30 years in Japan. We tested serum samples from 630 Japanese women aged 20–49 years whose blood samples were obtained between 1980 and 2015. IgG titer was measured using an EIA-based assay. HCMV-NAb titer was measured using a neutralization test assay with an HCMV isolate on human retinal epithelial cells. Longitudinal transitions in HCMV-NAb prevalence were clarified. The prevalence of HCMV-EIA-IgG, and HCMV-NAb at a titer of 16-fold, and HCMV-NAb at a titer of 100-fold, changed from 96.7% to 78.9%, 93.3% to 85.6%, and 35.5% to 41.1%, respectively, between 1980–1990 and 2010–2015. Prevalence of HCMV-NAb at a titer of 16-fold decreased by 7.7%, whereas that at a titer of 100-fold increased by 5.6%. A high titer of HCMV-NAb in pregnant women is expected to reduce the risk of intrauterine HCMV transmission from the mother to the fetus. The association between the risk of congenital HCMV infection and the prevalence of HCMV-NAb remains to be addressed. |
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| AbstractList | Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women. The IgG-positivity rate to HCMV determined by enzyme immunoassay (EIA) or indirect immunofluorescence assay has decreased from approximately 100% to 70% over the past 30 years in Japan. We tested serum samples from 630 Japanese women aged 20–49 years whose blood samples were obtained between 1980 and 2015. IgG titer was measured using an EIA-based assay. HCMV-NAb titer was measured using a neutralization test assay with an HCMV isolate on human retinal epithelial cells. Longitudinal transitions in HCMV-NAb prevalence were clarified. The prevalence of HCMV-EIA-IgG, and HCMV-NAb at a titer of 16-fold, and HCMV-NAb at a titer of 100-fold, changed from 96.7% to 78.9%, 93.3% to 85.6%, and 35.5% to 41.1%, respectively, between 1980–1990 and 2010–2015. Prevalence of HCMV-NAb at a titer of 16-fold decreased by 7.7%, whereas that at a titer of 100-fold increased by 5.6%. A high titer of HCMV-NAb in pregnant women is expected to reduce the risk of intrauterine HCMV transmission from the mother to the fetus. The association between the risk of congenital HCMV infection and the prevalence of HCMV-NAb remains to be addressed. Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women. The IgG-positivity rate to HCMV determined by enzyme immunoassay (EIA) or indirect immunofluorescence assay has decreased from approximately 100% to 70% over the past 30 years in Japan. We tested serum samples from 630 Japanese women aged 20-49 years whose blood samples were obtained between 1980 and 2015. IgG titer was measured using an EIA-based assay. HCMV-NAb titer was measured using a neutralization test assay with an HCMV isolate on human retinal epithelial cells. Longitudinal transitions in HCMV-NAb prevalence were clarified. The prevalence of HCMV-EIA-IgG, and HCMV-NAb at a titer of 16-fold, and HCMV-NAb at a titer of 100-fold, changed from 96.7% to 78.9%, 93.3% to 85.6%, and 35.5% to 41.1%, respectively, between 1980-1990 and 2010-2015. Prevalence of HCMV-NAb at a titer of 16-fold decreased by 7.7%, whereas that at a titer of 100-fold increased by 5.6%. A high titer of HCMV-NAb in pregnant women is expected to reduce the risk of intrauterine HCMV transmission from the mother to the fetus. The association between the risk of congenital HCMV infection and the prevalence of HCMV-NAb remains to be addressed.Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women. The IgG-positivity rate to HCMV determined by enzyme immunoassay (EIA) or indirect immunofluorescence assay has decreased from approximately 100% to 70% over the past 30 years in Japan. We tested serum samples from 630 Japanese women aged 20-49 years whose blood samples were obtained between 1980 and 2015. IgG titer was measured using an EIA-based assay. HCMV-NAb titer was measured using a neutralization test assay with an HCMV isolate on human retinal epithelial cells. Longitudinal transitions in HCMV-NAb prevalence were clarified. The prevalence of HCMV-EIA-IgG, and HCMV-NAb at a titer of 16-fold, and HCMV-NAb at a titer of 100-fold, changed from 96.7% to 78.9%, 93.3% to 85.6%, and 35.5% to 41.1%, respectively, between 1980-1990 and 2010-2015. Prevalence of HCMV-NAb at a titer of 16-fold decreased by 7.7%, whereas that at a titer of 100-fold increased by 5.6%. A high titer of HCMV-NAb in pregnant women is expected to reduce the risk of intrauterine HCMV transmission from the mother to the fetus. The association between the risk of congenital HCMV infection and the prevalence of HCMV-NAb remains to be addressed. |
| ArticleNumber | JJID.2021.726 |
| Author | Fujii, Hikaru Harada, Shizuko Saijo, Masayuki Inagaki, Takuya Yamada, Souichi Fukushi, Shuetsu Nguyen, Phu Hoang Anh Oka, Akira Yoshikawa, Tomoki Mizuguchi, Masashi Shibamura, Miho |
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| Cites_doi | 10.1093/cid/cix621 10.1097/INF.0b013e3182897c36 10.1056/NEJM200105033441804 10.1093/cid/ciq085 10.1001/jama.289.8.1008 10.1097/TP.0b013e318224115e 10.1111/trf.12390 10.1093/infdis/jiz464 10.1016/j.ajog.2009.11.018 10.1016/j.vaccine.2018.02.089 10.1056/NEJMoa043337 10.1016/j.jcv.2013.12.013 10.1128/JVI.02392-16 10.1093/cid/cit586 10.1136/bmjopen-2011-000118 10.1186/s12985-020-01390-2 10.3389/fmicb.2015.01016 10.1086/649903 10.1093/infdis/171.1.26 10.1002/rmv.535 10.2353/ajpath.2006.050482 10.1016/j.jcv.2013.07.004 10.1515/jpm-2011-0257 10.1093/cid/cis423 10.1080/21645515.2019.1593729 10.1016/j.jiac.2020.03.009 10.3390/v7082828 10.1093/cid/cis425 10.1016/j.jcv.2009.10.004 10.1093/cid/cit018 |
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| References | 9. Yamamoto AY, Mussi-Pinhata MM, Boppana SB, et al. Human cytomegalovirus reinfection is associated with intrauterine transmission in a highly cytomegalovirus-immune maternal population. Am J Obstet Gynecol. 2010;202:297.e1-297.e8. 19. Nigro G, Adler SP, La Torre R, et al. Passive immunization during pregnancy for congenital cytomegalovirus infection. N Engl J Med. 2005;353:1350-1362. 10. Wang C, Zhang X, Bialek S, et al. Attribution of congenital cytomegalovirus infection to primary versus non-primary maternal infection. Clin Infect Dis. 2011;52:e11-e13. 25. Azuma H, Takanashi M, Kohsaki M, et al. Cytomegalovirus seropositivity in pregnant women in Japan during 1996-2009. J Jpn Soc Perin Neon Med. 2010;46:1273-1279. Japanese. 2. Koyano S, Inoue N, Oka A, et al. Screening for congenital cytomegalovirus infection using newborn urine samples collected on filter paper: feasibility and outcomes from a multicentre study. BMJ Open. 2011;1:e000118. 8. Plotkin SA, Boppana SB. Vaccination against the human cytomegalovirus. Vaccine. 2019;37:7437-7442. 24. Adler SP. Primary maternal cytomegalovirus infection during pregnancy: Do we have a treatment option? Clin Infect Dis. 2012;55:504-506. 28. Cui X, Snapper CM. Development of novel vaccines against human cytomegalovirus. Hum Vaccin Immunother. 2019;15:2673-2683. 26. Taniguchi K, Watanabe N, Sato A, et al. Changes in cytomegalovirus seroprevalence in pregnant Japanese women—A 10-year single center study. J Clin Virol. 2014;59:192-194. 29. Wunsch M, Zhang W, Hanson J, et al. Characterization of the HCMV-specific CD4 T cell responses that are associated with protective immunity. Viruses. 2015;7:4414-4437. 32. Boppana SB, Rivera LB, Fowler KB, et al. Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N Engl J Med. 2001;344:1366-1371. 14. Maidji E, McDonagh S, Genbacev O, et al. Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol. 2006;168:1210-1226. 16. Shibamura M, Yoshikawa T, Yamada S, et al. Association of human cytomegalovirus (HCMV) neutralizing antibodies with antibodies to the HCMV glycoprotein complexes. Virol J. 2020;17:120. 13. Adler SP, Starr SE, Plotkin SA, et al. Immunity induced by primary human cytomegalovirus infection protects against secondary infection among women of childbearing age. J Infect Dis. 1995;171:26-32. 22. Buxmann H, Stackelberg OM, Schlößer RL, et al. Use of cytomegalovirus hyperimmunoglobulin for prevention of congenital cytomegalovirus disease: a retrospective analysis. J Perinat Med. 2012;40:439-446. 30. Britt WJ. Human cytomegalovirus infection in women with preexisting immunity: sources of infection and mechanisms of infection in the presence of antiviral immunity. J Infect Dis. 2020;221:S1-S8. 4. Adland E, Klenerman P, Goulder P, et al. Ongoing burden of disease and mortality from HIV/CMV coinfection in Africa in the antiretroviral therapy era. Front Microbiol. 2015;6:1016. 17. Torii Y, Kimura H, Ito Y, et al. et al. Clinicoepidemiologic status of mother-to-child infections: a nationwide survey in Japan. Pediatr Infect Dis J. 2013;32:699-701. 20. Planitzer CB, Saemann MD, Gajek H, et al. Cytomegalovirus neutralization by hyperimmune and standard intravenous immunoglobulin preparations. Transplantation. 2011;92:267-270. 18. Yamada H, Tanimura K, Fukushima S, et al. A cohort study of the universal neonatal urine screening for congenital cytomegalovirus infection. J Infect Chemother. 2020;26:790-794. 15. Nozawa N, Fang-Hoover J, Tabata T, et al. Cytomegalovirus-specific, high-avidity IgG with neutralizing activity in maternal circulation enriched in the fetal bloodstream. J Clin Virol. 2009;46:S58-S63. 12. Fowler KB, Stagno S, Pass RF. Maternal immunity and prevention of congenital cytomegalovirus infection. JAMA. 2003;289:1008-1011. 23. Nigro G, Adler SP. Hyperimmunoglobulin for prevention of congenital cytomegalovirus disease. Clin Infect Dis. 2013;57:S193-S195. 7. Britt WJ. Congenital human cytomegalovirus infection and the enigma of maternal immunity. J Virol. 2017;91:e02392-16. 6. Townsend CL, Forsgren M, Ahlfors K, et al. Long-term outcomes of congenital cytomegalovirus infection in Sweden and the United Kingdom. Clin Infect Dis. 2013;56:1232-1239. 33. Ikuta K, Minematsu T, Inoue N, et al. Cytomegalovirus (CMV) glycoprotein H-based serological analysis in Japanese healthy pregnant women, and in neonates with congenital CMV infection and their mothers. J Clin Virol. 2013;58:474-478. 5. Ishibashi M, Moriuchi H. Chronological change of seroprevalence for cytomegalovirus –Future direction of prenatal and perinatal management–. Jpn J Obstet Gynecol Neonatal Hematol. 2017;26:29-34. Japanese. 1. Mocarski ES Jr, Shenk T, Griffiths PD, et al. Cytomegaloviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 6th ed. Philadelphia, PA, USA: Wolters Kluwer / Lippincott Williams & Wilkins; 2013. p.1960-2014. 27. Furui Y, Satake M, Hoshi Y, et al. Cytomegalovirus (CMV) seroprevalence in Japanese blood donors and high detection frequency of CMV DNA in elderly donors. Transfusion. 2013;53:2190-2197. 31. Ross SA, Arora N, Novak Z, et al. Cytomegalovirus reinfections in healthy seroimmune women. J Infect Dis. 2010;201:386-389. 21. Visentin S, Manara R, Milanese L, et al. Early primary cytomegalovirus infection in pregnancy: maternal hyperimmunoglobulin therapy improves outcomes among infants at 1 year of age. Clin Infect Dis. 2012;55:497-503. 3. Kenneson A, Cannon MJ. Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol. 2007;17:253-276. 11. Tanimura K, Tairaku S, Morioka I, et al. Universal screening with use of immunoglobulin G avidity for congenital cytomegalovirus infection. Clin Infect Dis. 2017;65:1652-1658. 22 23 24 25 26 27 28 29 30 31 10 32 11 33 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: 1. Mocarski ES Jr, Shenk T, Griffiths PD, et al. Cytomegaloviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 6th ed. Philadelphia, PA, USA: Wolters Kluwer / Lippincott Williams & Wilkins; 2013. p.1960-2014. – reference: 16. Shibamura M, Yoshikawa T, Yamada S, et al. Association of human cytomegalovirus (HCMV) neutralizing antibodies with antibodies to the HCMV glycoprotein complexes. Virol J. 2020;17:120. – reference: 17. Torii Y, Kimura H, Ito Y, et al. et al. Clinicoepidemiologic status of mother-to-child infections: a nationwide survey in Japan. Pediatr Infect Dis J. 2013;32:699-701. – reference: 24. Adler SP. Primary maternal cytomegalovirus infection during pregnancy: Do we have a treatment option? Clin Infect Dis. 2012;55:504-506. – reference: 21. Visentin S, Manara R, Milanese L, et al. Early primary cytomegalovirus infection in pregnancy: maternal hyperimmunoglobulin therapy improves outcomes among infants at 1 year of age. Clin Infect Dis. 2012;55:497-503. – reference: 5. Ishibashi M, Moriuchi H. Chronological change of seroprevalence for cytomegalovirus –Future direction of prenatal and perinatal management–. Jpn J Obstet Gynecol Neonatal Hematol. 2017;26:29-34. Japanese. – reference: 2. Koyano S, Inoue N, Oka A, et al. Screening for congenital cytomegalovirus infection using newborn urine samples collected on filter paper: feasibility and outcomes from a multicentre study. BMJ Open. 2011;1:e000118. – reference: 32. Boppana SB, Rivera LB, Fowler KB, et al. Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N Engl J Med. 2001;344:1366-1371. – reference: 13. Adler SP, Starr SE, Plotkin SA, et al. Immunity induced by primary human cytomegalovirus infection protects against secondary infection among women of childbearing age. J Infect Dis. 1995;171:26-32. – reference: 7. Britt WJ. Congenital human cytomegalovirus infection and the enigma of maternal immunity. J Virol. 2017;91:e02392-16. – reference: 20. Planitzer CB, Saemann MD, Gajek H, et al. Cytomegalovirus neutralization by hyperimmune and standard intravenous immunoglobulin preparations. Transplantation. 2011;92:267-270. – reference: 4. Adland E, Klenerman P, Goulder P, et al. Ongoing burden of disease and mortality from HIV/CMV coinfection in Africa in the antiretroviral therapy era. Front Microbiol. 2015;6:1016. – reference: 22. Buxmann H, Stackelberg OM, Schlößer RL, et al. Use of cytomegalovirus hyperimmunoglobulin for prevention of congenital cytomegalovirus disease: a retrospective analysis. J Perinat Med. 2012;40:439-446. – reference: 33. Ikuta K, Minematsu T, Inoue N, et al. Cytomegalovirus (CMV) glycoprotein H-based serological analysis in Japanese healthy pregnant women, and in neonates with congenital CMV infection and their mothers. J Clin Virol. 2013;58:474-478. – reference: 19. Nigro G, Adler SP, La Torre R, et al. Passive immunization during pregnancy for congenital cytomegalovirus infection. N Engl J Med. 2005;353:1350-1362. – reference: 18. Yamada H, Tanimura K, Fukushima S, et al. A cohort study of the universal neonatal urine screening for congenital cytomegalovirus infection. J Infect Chemother. 2020;26:790-794. – reference: 30. Britt WJ. Human cytomegalovirus infection in women with preexisting immunity: sources of infection and mechanisms of infection in the presence of antiviral immunity. J Infect Dis. 2020;221:S1-S8. – reference: 28. Cui X, Snapper CM. Development of novel vaccines against human cytomegalovirus. Hum Vaccin Immunother. 2019;15:2673-2683. – reference: 14. Maidji E, McDonagh S, Genbacev O, et al. Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol. 2006;168:1210-1226. – reference: 25. Azuma H, Takanashi M, Kohsaki M, et al. Cytomegalovirus seropositivity in pregnant women in Japan during 1996-2009. J Jpn Soc Perin Neon Med. 2010;46:1273-1279. Japanese. – reference: 29. Wunsch M, Zhang W, Hanson J, et al. Characterization of the HCMV-specific CD4 T cell responses that are associated with protective immunity. Viruses. 2015;7:4414-4437. – reference: 31. Ross SA, Arora N, Novak Z, et al. Cytomegalovirus reinfections in healthy seroimmune women. J Infect Dis. 2010;201:386-389. – reference: 8. Plotkin SA, Boppana SB. Vaccination against the human cytomegalovirus. Vaccine. 2019;37:7437-7442. – reference: 9. Yamamoto AY, Mussi-Pinhata MM, Boppana SB, et al. Human cytomegalovirus reinfection is associated with intrauterine transmission in a highly cytomegalovirus-immune maternal population. Am J Obstet Gynecol. 2010;202:297.e1-297.e8. – reference: 27. Furui Y, Satake M, Hoshi Y, et al. Cytomegalovirus (CMV) seroprevalence in Japanese blood donors and high detection frequency of CMV DNA in elderly donors. Transfusion. 2013;53:2190-2197. – reference: 11. Tanimura K, Tairaku S, Morioka I, et al. Universal screening with use of immunoglobulin G avidity for congenital cytomegalovirus infection. Clin Infect Dis. 2017;65:1652-1658. – reference: 3. Kenneson A, Cannon MJ. Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol. 2007;17:253-276. – reference: 6. Townsend CL, Forsgren M, Ahlfors K, et al. Long-term outcomes of congenital cytomegalovirus infection in Sweden and the United Kingdom. Clin Infect Dis. 2013;56:1232-1239. – reference: 10. Wang C, Zhang X, Bialek S, et al. Attribution of congenital cytomegalovirus infection to primary versus non-primary maternal infection. Clin Infect Dis. 2011;52:e11-e13. – reference: 15. Nozawa N, Fang-Hoover J, Tabata T, et al. Cytomegalovirus-specific, high-avidity IgG with neutralizing activity in maternal circulation enriched in the fetal bloodstream. J Clin Virol. 2009;46:S58-S63. – reference: 12. Fowler KB, Stagno S, Pass RF. Maternal immunity and prevention of congenital cytomegalovirus infection. JAMA. 2003;289:1008-1011. – reference: 23. Nigro G, Adler SP. Hyperimmunoglobulin for prevention of congenital cytomegalovirus disease. Clin Infect Dis. 2013;57:S193-S195. – reference: 26. Taniguchi K, Watanabe N, Sato A, et al. Changes in cytomegalovirus seroprevalence in pregnant Japanese women—A 10-year single center study. J Clin Virol. 2014;59:192-194. – ident: 11 doi: 10.1093/cid/cix621 – ident: 17 doi: 10.1097/INF.0b013e3182897c36 – ident: 32 doi: 10.1056/NEJM200105033441804 – ident: 10 doi: 10.1093/cid/ciq085 – ident: 12 doi: 10.1001/jama.289.8.1008 – ident: 20 doi: 10.1097/TP.0b013e318224115e – ident: 27 doi: 10.1111/trf.12390 – ident: 30 doi: 10.1093/infdis/jiz464 – ident: 9 doi: 10.1016/j.ajog.2009.11.018 – ident: 8 doi: 10.1016/j.vaccine.2018.02.089 – ident: 19 doi: 10.1056/NEJMoa043337 – ident: 26 doi: 10.1016/j.jcv.2013.12.013 – ident: 7 doi: 10.1128/JVI.02392-16 – ident: 23 doi: 10.1093/cid/cit586 – ident: 2 doi: 10.1136/bmjopen-2011-000118 – ident: 5 – ident: 1 – ident: 16 doi: 10.1186/s12985-020-01390-2 – ident: 4 doi: 10.3389/fmicb.2015.01016 – ident: 31 doi: 10.1086/649903 – ident: 13 doi: 10.1093/infdis/171.1.26 – ident: 3 doi: 10.1002/rmv.535 – ident: 14 doi: 10.2353/ajpath.2006.050482 – ident: 33 doi: 10.1016/j.jcv.2013.07.004 – ident: 22 doi: 10.1515/jpm-2011-0257 – ident: 21 doi: 10.1093/cid/cis423 – ident: 28 doi: 10.1080/21645515.2019.1593729 – ident: 18 doi: 10.1016/j.jiac.2020.03.009 – ident: 29 doi: 10.3390/v7082828 – ident: 24 doi: 10.1093/cid/cis425 – ident: 15 doi: 10.1016/j.jcv.2009.10.004 – ident: 6 doi: 10.1093/cid/cit018 – ident: 25 |
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| Snippet | Neutralizing antibodies (NAbs) to human cytomegalovirus (HCMV) are associated with the risk of transplacental HCMV infection of the fetus in pregnant women.... |
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| SubjectTerms | Antibodies congenital cytomegalovirus infection Cytomegalovirus Enzyme immunoassay Epithelial cells Epithelium Fetuses human cytomegalovirus Immunoassay Immunofluorescence Immunoglobulin G Japan Neutralization Neutralizing neutralizing antibody Pregnancy Risk seroprevalence |
| Title | Longitudinal Trends of Prevalence of Neutralizing Antibody against Human Cytomegalovirus over the Past 30 Years in Japanese Women |
| URI | https://www.jstage.jst.go.jp/article/yoken/75/5/75_JJID.2021.726/_article/-char/en https://www.proquest.com/docview/2720113065 https://www.proquest.com/docview/2658644217 |
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| ispartofPNX | Japanese Journal of Infectious Diseases, 2022/09/30, Vol.75(5), pp.496-503 |
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