Zika virus infection enhances future risk of severe dengue disease
Dengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40% homology within the envelope protein. We know that subsequent dengue infections bring a risk of antibody-dependent disease enhancement. Whereas emphasis has...
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| Published in | Science (American Association for the Advancement of Science) Vol. 369; no. 6507; pp. 1123 - 1128 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
28.08.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Dengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40% homology within the envelope protein. We know that subsequent dengue infections bring a risk of antibody-dependent disease enhancement. Whereas emphasis has been placed on how prior dengue immunity affects Zika infection, little is known about how prior Zika immunity may affect dengue disease. Katzelnick
et al.
have been following a well-characterized and established pediatric cohort in Nicaragua who were serially exposed to both flaviviruses in recent years (see the Perspective by Clapham). This study shows not only that a previous history of just one round of dengue is a problem but also that prior Zika immunity creates an increased risk for severe dengue virus sereotype 2 infection. By contrast, multiple infections raise antibodies to protective levels.
Science
, this issue p.
1123
; see also p.
1055
Prior immunity to Zika virus increases the risk of severe dengue disease via cross-reacting antibodies.
The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. |
|---|---|
| AbstractList | Dengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40% homology within the envelope protein. We know that subsequent dengue infections bring a risk of antibody-dependent disease enhancement. Whereas emphasis has been placed on how prior dengue immunity affects Zika infection, little is known about how prior Zika immunity may affect dengue disease. Katzelnick
et al.
have been following a well-characterized and established pediatric cohort in Nicaragua who were serially exposed to both flaviviruses in recent years (see the Perspective by Clapham). This study shows not only that a previous history of just one round of dengue is a problem but also that prior Zika immunity creates an increased risk for severe dengue virus sereotype 2 infection. By contrast, multiple infections raise antibodies to protective levels.
Science
, this issue p.
1123
; see also p.
1055
Prior immunity to Zika virus increases the risk of severe dengue disease via cross-reacting antibodies.
The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. The Zika pandemic sparked intense interest in whether immune interactions among dengue viruses 1–4 (DENV1–4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1–3 (2004–15), Zika (2016–17), and DENV2 (2018–20) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. In contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. Double whammyDengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40% homology within the envelope protein. We know that subsequent dengue infections bring a risk of antibody-dependent disease enhancement. Whereas emphasis has been placed on how prior dengue immunity affects Zika infection, little is known about how prior Zika immunity may affect dengue disease. Katzelnick et al. have been following a well-characterized and established pediatric cohort in Nicaragua who were serially exposed to both flaviviruses in recent years (see the Perspective by Clapham). This study shows not only that a previous history of just one round of dengue is a problem but also that prior Zika immunity creates an increased risk for severe dengue virus sereotype 2 infection. By contrast, multiple infections raise antibodies to protective levels.Science, this issue p. 1123; see also p. 1055The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines.The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika virus (ZIKV). We investigated prospective pediatric cohorts in Nicaragua that experienced sequential DENV1 to -3 (2004 to 2015), Zika (2016 to 2017), and DENV2 (2018 to 2020) epidemics. Risk of symptomatic DENV2 infection and severe disease was elevated by one prior ZIKV infection, one prior DENV infection, or one prior DENV infection followed by one ZIKV infection, compared with being flavivirus-naïve. By contrast, multiple prior DENV infections reduced dengue risk. Further, although high preexisting anti-DENV antibody titers protected against DENV1, DENV3, and ZIKV disease, intermediate titers induced by previous ZIKV or DENV infection enhanced future risk of DENV2 disease and severity, as well as DENV3 severity. The observation that prior ZIKV infection can modulate dengue disease severity like a DENV serotype poses challenges to development of dengue and Zika vaccines. |
| Author | Narvaez, César Arguello, Sonia Latta, Krista Ampie, Oscarlett Segovia-Chumbez, Bruno Katzelnick, Leah C. Lopez Mercado, Brenda Coloma, Josefina Harris, Eva Kuan, Guillermina Gordon, Aubree Premkumar, Lakshmanane Elizondo, Douglas Mercado, Juan Carlos Collado, Damaris de Silva, Aravinda M. Plazaola, Miguel Sanchez, Nery Miranda, Tatiana Halloran, M. Elizabeth Ojeda, Sergio Schiller, Amy Narvaez, Federico Bustos Carillo, Fausto Balmaseda, Angel |
| AuthorAffiliation | 2 Sustainable Sciences Institute, Managua, Nicaragua 4 Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA 7 Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA 8 Centro de Salud Sócrates Flores Vivas, Ministry of Health, Managua, Nicaragua 6 Department of Biostatistics, University of Washington, Seattle, WA, USA 1 Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA 3 Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministry of Health, Managua, Nicaragua 5 Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, NC, USA |
| AuthorAffiliation_xml | – name: 3 Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministry of Health, Managua, Nicaragua – name: 2 Sustainable Sciences Institute, Managua, Nicaragua – name: 4 Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA – name: 6 Department of Biostatistics, University of Washington, Seattle, WA, USA – name: 5 Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, NC, USA – name: 7 Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA – name: 8 Centro de Salud Sócrates Flores Vivas, Ministry of Health, Managua, Nicaragua – name: 1 Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA |
| Author_xml | – sequence: 1 givenname: Leah C. orcidid: 0000-0003-1033-6758 surname: Katzelnick fullname: Katzelnick, Leah C. organization: Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA – sequence: 2 givenname: César surname: Narvaez fullname: Narvaez, César organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 3 givenname: Sonia surname: Arguello fullname: Arguello, Sonia organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 4 givenname: Brenda orcidid: 0000-0002-9584-2571 surname: Lopez Mercado fullname: Lopez Mercado, Brenda organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 5 givenname: Damaris orcidid: 0000-0002-0878-3260 surname: Collado fullname: Collado, Damaris organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 6 givenname: Oscarlett orcidid: 0000-0002-5637-2239 surname: Ampie fullname: Ampie, Oscarlett organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 7 givenname: Douglas surname: Elizondo fullname: Elizondo, Douglas organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 8 givenname: Tatiana orcidid: 0000-0001-7358-982X surname: Miranda fullname: Miranda, Tatiana organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 9 givenname: Fausto orcidid: 0000-0002-7263-5625 surname: Bustos Carillo fullname: Bustos Carillo, Fausto organization: Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA – sequence: 10 givenname: Juan Carlos surname: Mercado fullname: Mercado, Juan Carlos organization: Sustainable Sciences Institute, Managua, Nicaragua., Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministry of Health, Managua, Nicaragua – sequence: 11 givenname: Krista orcidid: 0000-0002-5218-2702 surname: Latta fullname: Latta, Krista organization: Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA – sequence: 12 givenname: Amy orcidid: 0000-0002-1000-3665 surname: Schiller fullname: Schiller, Amy organization: Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA – sequence: 13 givenname: Bruno orcidid: 0000-0002-7730-9386 surname: Segovia-Chumbez fullname: Segovia-Chumbez, Bruno organization: Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, NC, USA – sequence: 14 givenname: Sergio orcidid: 0000-0003-2512-2306 surname: Ojeda fullname: Ojeda, Sergio organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 15 givenname: Nery surname: Sanchez fullname: Sanchez, Nery organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 16 givenname: Miguel surname: Plazaola fullname: Plazaola, Miguel organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 17 givenname: Josefina surname: Coloma fullname: Coloma, Josefina organization: Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA – sequence: 18 givenname: M. Elizabeth orcidid: 0000-0002-3127-1757 surname: Halloran fullname: Halloran, M. Elizabeth organization: Department of Biostatistics, University of Washington, Seattle, WA, USA., Vaccine and Infectious Diseases Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA – sequence: 19 givenname: Lakshmanane orcidid: 0000-0002-1736-1350 surname: Premkumar fullname: Premkumar, Lakshmanane organization: Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, NC, USA – sequence: 20 givenname: Aubree orcidid: 0000-0002-9352-7877 surname: Gordon fullname: Gordon, Aubree organization: Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA – sequence: 21 givenname: Federico surname: Narvaez fullname: Narvaez, Federico organization: Sustainable Sciences Institute, Managua, Nicaragua – sequence: 22 givenname: Aravinda M. orcidid: 0000-0003-3317-5950 surname: de Silva fullname: de Silva, Aravinda M. organization: Department of Microbiology and Immunology, University of North Carolina School of Medicine, Chapel Hill, NC, USA – sequence: 23 givenname: Guillermina surname: Kuan fullname: Kuan, Guillermina organization: Sustainable Sciences Institute, Managua, Nicaragua., Centro de Salud Sócrates Flores Vivas, Ministry of Health, Managua, Nicaragua – sequence: 24 givenname: Angel surname: Balmaseda fullname: Balmaseda, Angel organization: Sustainable Sciences Institute, Managua, Nicaragua., Laboratorio Nacional de Virología, Centro Nacional de Diagnóstico y Referencia, Ministry of Health, Managua, Nicaragua – sequence: 25 givenname: Eva orcidid: 0000-0002-7238-4037 surname: Harris fullname: Harris, Eva organization: Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32855339$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contributions: L.C.K., A.B., and E.H. conceived the project; G.K., S.O., N.S., M.P., F.N., E.H., J.C., and A.G. led and managed the clinical studies; A.B., E.H., J.C.M., L.P., and A.M.dS, designed and oversaw all laboratory analyses; D.C., O.A., T.M., and B.S.C. collected the serological data; C.N., S.A., B.L.M, D.E., K.L., A.S., and L.C.K. managed the clinical and laboratory databases and organized the data for analysis; L.C.K. E.H., A.B., A.M.dS., L.P., C.N., A.G., F.B., M.E.H. analyzed and discussed the data; L.C.K. and E.H. wrote the first draft of the manuscript and created the figures; all authors reviewed the manuscript. |
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| Snippet | Dengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40% homology within... The Zika pandemic sparked intense interest in whether immune interactions among dengue virus serotypes 1 to 4 (DENV1 to -4) extend to the closely related Zika... Double whammyDengue and Zika virus epidemics have been lapping each other around the globe. These are closely related mosquito-borne viruses with about 40%... The Zika pandemic sparked intense interest in whether immune interactions among dengue viruses 1–4 (DENV1–4) extend to the closely related Zika virus (ZIKV).... |
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| SubjectTerms | Antibodies Antibodies, Viral - blood Dengue fever Dengue hemorrhagic fever Dengue Vaccines - immunology Dengue Virus - immunology Epidemics Homology Humans Immunity Immunogenicity, Vaccine Infections Nicaragua - epidemiology Pandemics Pediatrics Risk Serogroup Serotypes Severe Dengue - epidemiology Vaccines Vector-borne diseases Viral envelope proteins Viruses Zika virus Zika Virus - immunology Zika Virus Infection - epidemiology Zika Virus Infection - immunology |
| Title | Zika virus infection enhances future risk of severe dengue disease |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/32855339 https://www.proquest.com/docview/2438014580 https://www.proquest.com/docview/2438684104 https://pubmed.ncbi.nlm.nih.gov/PMC8274975 |
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