Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field

Abstract The H9N2 subtype avian influenza virus (AIV) inactivated vaccine has been used extensively in poultry farms, but it often fails to stimulate a sufficiently high immune response in poultry in the field, although it works well in laboratory experiments; hence, the virus still causes economic...

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Main Authors: Xue Pan, Xin Su, Pingyun Ding, Jinhua Zhao, Hongrui Cui, Dawei Yan, Qiaoyang Teng, Xuesong Li, Nancy Beerens, Haitao Zhang, Qinfang Liu, Mart C. M. de Jong, Zejun Li
Format: Article
Language:English
Published: BMC 2022-05-01
Series:Animal Diseases
Subjects:
Online Access:https://doi.org/10.1186/s44149-022-00040-0
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author Xue Pan
Xin Su
Pingyun Ding
Jinhua Zhao
Hongrui Cui
Dawei Yan
Qiaoyang Teng
Xuesong Li
Nancy Beerens
Haitao Zhang
Qinfang Liu
Mart C. M. de Jong
Zejun Li
author_facet Xue Pan
Xin Su
Pingyun Ding
Jinhua Zhao
Hongrui Cui
Dawei Yan
Qiaoyang Teng
Xuesong Li
Nancy Beerens
Haitao Zhang
Qinfang Liu
Mart C. M. de Jong
Zejun Li
author_sort Xue Pan
collection DOAJ
description Abstract The H9N2 subtype avian influenza virus (AIV) inactivated vaccine has been used extensively in poultry farms, but it often fails to stimulate a sufficiently high immune response in poultry in the field, although it works well in laboratory experiments; hence, the virus still causes economic damage every year and poses a potential threat to public health. Based on surveillance data collected in the field, we found that broilers with high levels of maternal-derived antibodies (MDAs) against H9N2 virus did not produce high levels of antibodies after vaccination with a commercial H9N2 inactivated vaccine. In contrast, specific pathogen-free (SPF) chickens without MDAs responded efficiently to that vaccination. When MDAs were mimicked by administering passively transferred antibodies (PTAs) into SPF chickens in the laboratory, similar results were observed: H9N2-specific PTAs inhibited humoral immunity against the H9N2 inactivated vaccine, suggesting that H9N2-specific MDAs might hinder the generation of antibodies when H9N2 inactivated vaccine was used. After challenge with homologous H9N2 virus, the virus was detected in oropharyngeal swabs of the vaccinated and unvaccinated chickens with PTAs but not in the vaccinated chickens without PTAs, indicating that H9N2-specific MDAs were indeed one of the reasons for H9N2 inactivated vaccine failure in the field. When different titers of PTAs were used to mimic MDAs in SPF chickens, high (HI = 12 log2) and medium (HI = log 9 log2) titers of PTAs reduced the generation of H9N2-specific antibodies after the first vaccination, but a booster dose would induce a high and faster humoral immune response even of PTA interference. This study strongly suggested that high or medium titers of MDAs might explain H9N2 inactivated vaccine failure in the field.
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spelling doaj.art-99933af825674e41a3102bc0c171bcda2022-12-22T02:23:49ZengBMCAnimal Diseases2731-04422022-05-01211910.1186/s44149-022-00040-0Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the fieldXue Pan0Xin Su1Pingyun Ding2Jinhua Zhao3Hongrui Cui4Dawei Yan5Qiaoyang Teng6Xuesong Li7Nancy Beerens8Haitao Zhang9Qinfang Liu10Mart C. M. de Jong11Zejun Li12Shanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesShanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesBiotechnology Research laboratory, Jiangsu Lihua Animal Husbandry Co. Ltd.Biotechnology Research laboratory, Jiangsu Lihua Animal Husbandry Co. Ltd.Shanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesShanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesShanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesShanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesWageningen Bioveterinary Research, Wageningen University & ResearchBiotechnology Research laboratory, Jiangsu Lihua Animal Husbandry Co. Ltd.Shanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesQuantitative Veterinary Epidemiology, Animal Sciences Group, Wageningen University & ResearchShanghai Veterinary Research Institute, Chinese Academy of Agriculture SciencesAbstract The H9N2 subtype avian influenza virus (AIV) inactivated vaccine has been used extensively in poultry farms, but it often fails to stimulate a sufficiently high immune response in poultry in the field, although it works well in laboratory experiments; hence, the virus still causes economic damage every year and poses a potential threat to public health. Based on surveillance data collected in the field, we found that broilers with high levels of maternal-derived antibodies (MDAs) against H9N2 virus did not produce high levels of antibodies after vaccination with a commercial H9N2 inactivated vaccine. In contrast, specific pathogen-free (SPF) chickens without MDAs responded efficiently to that vaccination. When MDAs were mimicked by administering passively transferred antibodies (PTAs) into SPF chickens in the laboratory, similar results were observed: H9N2-specific PTAs inhibited humoral immunity against the H9N2 inactivated vaccine, suggesting that H9N2-specific MDAs might hinder the generation of antibodies when H9N2 inactivated vaccine was used. After challenge with homologous H9N2 virus, the virus was detected in oropharyngeal swabs of the vaccinated and unvaccinated chickens with PTAs but not in the vaccinated chickens without PTAs, indicating that H9N2-specific MDAs were indeed one of the reasons for H9N2 inactivated vaccine failure in the field. When different titers of PTAs were used to mimic MDAs in SPF chickens, high (HI = 12 log2) and medium (HI = log 9 log2) titers of PTAs reduced the generation of H9N2-specific antibodies after the first vaccination, but a booster dose would induce a high and faster humoral immune response even of PTA interference. This study strongly suggested that high or medium titers of MDAs might explain H9N2 inactivated vaccine failure in the field.https://doi.org/10.1186/s44149-022-00040-0Maternal-derived antibodies (MDAs)Passively transferred antibodies (PTAs)Humoral immune responseVaccination failureH9N2 avian influenza virus (AIV)
spellingShingle Xue Pan
Xin Su
Pingyun Ding
Jinhua Zhao
Hongrui Cui
Dawei Yan
Qiaoyang Teng
Xuesong Li
Nancy Beerens
Haitao Zhang
Qinfang Liu
Mart C. M. de Jong
Zejun Li
Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
Animal Diseases
Maternal-derived antibodies (MDAs)
Passively transferred antibodies (PTAs)
Humoral immune response
Vaccination failure
H9N2 avian influenza virus (AIV)
title Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
title_full Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
title_fullStr Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
title_full_unstemmed Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
title_short Maternal-derived antibodies hinder the antibody response to H9N2 AIV inactivated vaccine in the field
title_sort maternal derived antibodies hinder the antibody response to h9n2 aiv inactivated vaccine in the field
topic Maternal-derived antibodies (MDAs)
Passively transferred antibodies (PTAs)
Humoral immune response
Vaccination failure
H9N2 avian influenza virus (AIV)
url https://doi.org/10.1186/s44149-022-00040-0
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