Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring

Abstract Influenza virus causes life-threatening infections in pregnant women and their newborns. Immunization during pregnancy is the most effective means of preventing maternal and infant mortality/morbidity; however, influenza vaccination rates of pregnant women remain under 50%. Furthermore, the...

Full description

Bibliographic Details
Main Authors: E. Stein Esser, Joanna A. Pulit-Penaloza, Haripriya Kalluri, Devin McAllister, Elena V. Vassilieva, Elizabeth Q. Littauer, Nadia Lelutiu, Mark R. Prausnitz, Richard W. Compans, Ioanna Skountzou
Format: Article
Language:English
Published: Nature Publishing Group 2017-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-05940-7
id doaj-bee56125b1cf4f40b60481bcbec9c6ab
record_format Article
spelling doaj-bee56125b1cf4f40b60481bcbec9c6ab2020-12-08T03:02:07ZengNature Publishing GroupScientific Reports2045-23222017-07-017111110.1038/s41598-017-05940-7Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspringE. Stein Esser0Joanna A. Pulit-Penaloza1Haripriya Kalluri2Devin McAllister3Elena V. Vassilieva4Elizabeth Q. Littauer5Nadia Lelutiu6Mark R. Prausnitz7Richard W. Compans8Ioanna Skountzou9Department of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineSchool of Chemical and Biomolecular Engineering, Georgia Institute of TechnologySchool of Chemical and Biomolecular Engineering, Georgia Institute of TechnologyDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineSchool of Chemical and Biomolecular Engineering, Georgia Institute of TechnologyDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineDepartment of Microbiology & Immunology and Emory Vaccine Center, Emory University School of MedicineAbstract Influenza virus causes life-threatening infections in pregnant women and their newborns. Immunization during pregnancy is the most effective means of preventing maternal and infant mortality/morbidity; however, influenza vaccination rates of pregnant women remain under 50%. Furthermore, the availability of vaccines in low-resource populations is limited. Skin immunization with microneedle patches (MN) is a novel and safe vaccination platform featuring thermostable vaccine formulations. Cold-chain independence and the potential for self-administration can expand influenza vaccination coverage in developing countries. In this study of pregnant BALB/c mice immunized with subunit H1N1 influenza vaccine, we demonstrate the advantage of skin vaccination over intramuscular delivery of a two-fold higher vaccine dose. MN vaccine induced superior humoral immune responses and conferred protective immunity against a lethal challenge dose of homologous influenza virus. Importantly, MN vaccination of mice at mid-gestation resulted in enhanced and long-lasting passive immunity of the offspring, measured by neutralizing antibody titers and survival rates after virus challenge. We conclude that skin vaccination using MN is a superior immunization approach with the potential to overcome immune tolerance observed in pregnancy, and lower vaccination costs through antigen dose-sparing, which is especially relevant in underserved countries.https://doi.org/10.1038/s41598-017-05940-7
collection DOAJ
language English
format Article
sources DOAJ
author E. Stein Esser
Joanna A. Pulit-Penaloza
Haripriya Kalluri
Devin McAllister
Elena V. Vassilieva
Elizabeth Q. Littauer
Nadia Lelutiu
Mark R. Prausnitz
Richard W. Compans
Ioanna Skountzou
spellingShingle E. Stein Esser
Joanna A. Pulit-Penaloza
Haripriya Kalluri
Devin McAllister
Elena V. Vassilieva
Elizabeth Q. Littauer
Nadia Lelutiu
Mark R. Prausnitz
Richard W. Compans
Ioanna Skountzou
Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
Scientific Reports
author_facet E. Stein Esser
Joanna A. Pulit-Penaloza
Haripriya Kalluri
Devin McAllister
Elena V. Vassilieva
Elizabeth Q. Littauer
Nadia Lelutiu
Mark R. Prausnitz
Richard W. Compans
Ioanna Skountzou
author_sort E. Stein Esser
title Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
title_short Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
title_full Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
title_fullStr Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
title_full_unstemmed Microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
title_sort microneedle patch delivery of influenza vaccine during pregnancy enhances maternal immune responses promoting survival and long-lasting passive immunity to offspring
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-07-01
description Abstract Influenza virus causes life-threatening infections in pregnant women and their newborns. Immunization during pregnancy is the most effective means of preventing maternal and infant mortality/morbidity; however, influenza vaccination rates of pregnant women remain under 50%. Furthermore, the availability of vaccines in low-resource populations is limited. Skin immunization with microneedle patches (MN) is a novel and safe vaccination platform featuring thermostable vaccine formulations. Cold-chain independence and the potential for self-administration can expand influenza vaccination coverage in developing countries. In this study of pregnant BALB/c mice immunized with subunit H1N1 influenza vaccine, we demonstrate the advantage of skin vaccination over intramuscular delivery of a two-fold higher vaccine dose. MN vaccine induced superior humoral immune responses and conferred protective immunity against a lethal challenge dose of homologous influenza virus. Importantly, MN vaccination of mice at mid-gestation resulted in enhanced and long-lasting passive immunity of the offspring, measured by neutralizing antibody titers and survival rates after virus challenge. We conclude that skin vaccination using MN is a superior immunization approach with the potential to overcome immune tolerance observed in pregnancy, and lower vaccination costs through antigen dose-sparing, which is especially relevant in underserved countries.
url https://doi.org/10.1038/s41598-017-05940-7
work_keys_str_mv AT esteinesser microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT joannaapulitpenaloza microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT haripriyakalluri microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT devinmcallister microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT elenavvassilieva microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT elizabethqlittauer microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT nadialelutiu microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT markrprausnitz microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT richardwcompans microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
AT ioannaskountzou microneedlepatchdeliveryofinfluenzavaccineduringpregnancyenhancesmaternalimmuneresponsespromotingsurvivalandlonglastingpassiveimmunitytooffspring
_version_ 1724393134658420736