Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets

Natural planned exposure (NPE) remains one of the most common methods in swine herds to boost lactogenic immunity against rotaviruses. However, the efficacy of NPE protocols in generating lactogenic immunity has not been investigated before. A longitudinal study was conducted to investigate the dyna...

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Main Authors: Deepak Kumar, Amanda V. Anderson Reever, Jeremy S. Pittman, Nora L. Springer, Kylynn Mallen, Gleyder Roman-Sosa, Neha Sangewar, Mary C. Casey-Moore, Michael D. Bowen, Waithaka Mwangi, Douglas G. Marthaler
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Vaccines
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Online Access:https://www.mdpi.com/2076-393X/11/12/1866
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author Deepak Kumar
Amanda V. Anderson Reever
Jeremy S. Pittman
Nora L. Springer
Kylynn Mallen
Gleyder Roman-Sosa
Neha Sangewar
Mary C. Casey-Moore
Michael D. Bowen
Waithaka Mwangi
Douglas G. Marthaler
author_facet Deepak Kumar
Amanda V. Anderson Reever
Jeremy S. Pittman
Nora L. Springer
Kylynn Mallen
Gleyder Roman-Sosa
Neha Sangewar
Mary C. Casey-Moore
Michael D. Bowen
Waithaka Mwangi
Douglas G. Marthaler
author_sort Deepak Kumar
collection DOAJ
description Natural planned exposure (NPE) remains one of the most common methods in swine herds to boost lactogenic immunity against rotaviruses. However, the efficacy of NPE protocols in generating lactogenic immunity has not been investigated before. A longitudinal study was conducted to investigate the dynamics of genotype-specific antibody responses to different doses (3, 2 and 1) of Rotavirus A (RVA) NPE (genotypes G4, G5, P[7] and P[23]) in gilts and the transfer of lactogenic immunity to their piglets. Group 1 gilts received three doses of NPE at 5, 4 and 3 weeks pre-farrow (WPF), group 2 received two doses at 5 and 3 WPF, group 3 received one dose at 5 WPF, and group 4 received no NPE (control group). VP7 (G4 and G5) and truncated VP4* (P[7] and P[23]) antigens of RVA were expressed in mammalian and bacterial expression systems, respectively, and used to optimize indirect ELISAs to determine antibody levels against RVA in gilts and piglets. In day-0 colostrum samples, group 1 had significantly higher IgG titers compared to the control group for all four antigens, and either significantly or numerically higher IgG titers than groups 2 and 3. Group 1 also had significantly higher colostrum IgA levels than the control group for all antigens (except G4), and either significantly or numerically higher IgA levels compared to groups 2 and 3. In piglet serum, group 1 piglets had higher IgG titers for all four antigens at day 0 than the other groups. Importantly, RVA NPE stimulated antibodies in all groups regardless of the treatment doses and prevented G4, G5, P[7] and P[23] RVA fecal shedding prior to weaning in piglets in the absence of viral challenge. The G11 and P[34] RVA genotypes detected from pre-weaning piglets differed at multiple amino acid positions with parent NPE strains. In conclusion, the results of this study suggest that the group 1 NPE regimen (three doses of NPE) resulted in the highest anti-RVA antibody (IgG and IgA) levels in the colostrum/milk, and the highest IgG levels in piglet serum.
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spelling doaj.art-a4a760bead3f4722bdb0e036734c0d602023-12-22T14:47:41ZengMDPI AGVaccines2076-393X2023-12-011112186610.3390/vaccines11121866Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in PigletsDeepak Kumar0Amanda V. Anderson Reever1Jeremy S. Pittman2Nora L. Springer3Kylynn Mallen4Gleyder Roman-Sosa5Neha Sangewar6Mary C. Casey-Moore7Michael D. Bowen8Waithaka Mwangi9Douglas G. Marthaler10Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USADepartment of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USASmithfield Foods, 434 E Main St., Waverly, VA 23890, USAClinical Pathology, Biomedical and Diagnostic Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996, USADepartment of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USAInstitute of Virology, University of Veterinary Medicine Hannover, Foundation, 30559 Hannover, GermanyDepartment of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USAViral Gastroenteritis Branch, Division of Viral Diseases, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention, 1600 Clifton Rd NE, Atlanta, GA 30329, USAViral Gastroenteritis Branch, Division of Viral Diseases, National Center for Immunization and Respiratory Diseases (NCIRD), Centers for Disease Control and Prevention, 1600 Clifton Rd NE, Atlanta, GA 30329, USADepartment of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USAScience and Technology, Indical Inc., Orlando, FL 32804, USANatural planned exposure (NPE) remains one of the most common methods in swine herds to boost lactogenic immunity against rotaviruses. However, the efficacy of NPE protocols in generating lactogenic immunity has not been investigated before. A longitudinal study was conducted to investigate the dynamics of genotype-specific antibody responses to different doses (3, 2 and 1) of Rotavirus A (RVA) NPE (genotypes G4, G5, P[7] and P[23]) in gilts and the transfer of lactogenic immunity to their piglets. Group 1 gilts received three doses of NPE at 5, 4 and 3 weeks pre-farrow (WPF), group 2 received two doses at 5 and 3 WPF, group 3 received one dose at 5 WPF, and group 4 received no NPE (control group). VP7 (G4 and G5) and truncated VP4* (P[7] and P[23]) antigens of RVA were expressed in mammalian and bacterial expression systems, respectively, and used to optimize indirect ELISAs to determine antibody levels against RVA in gilts and piglets. In day-0 colostrum samples, group 1 had significantly higher IgG titers compared to the control group for all four antigens, and either significantly or numerically higher IgG titers than groups 2 and 3. Group 1 also had significantly higher colostrum IgA levels than the control group for all antigens (except G4), and either significantly or numerically higher IgA levels compared to groups 2 and 3. In piglet serum, group 1 piglets had higher IgG titers for all four antigens at day 0 than the other groups. Importantly, RVA NPE stimulated antibodies in all groups regardless of the treatment doses and prevented G4, G5, P[7] and P[23] RVA fecal shedding prior to weaning in piglets in the absence of viral challenge. The G11 and P[34] RVA genotypes detected from pre-weaning piglets differed at multiple amino acid positions with parent NPE strains. In conclusion, the results of this study suggest that the group 1 NPE regimen (three doses of NPE) resulted in the highest anti-RVA antibody (IgG and IgA) levels in the colostrum/milk, and the highest IgG levels in piglet serum.https://www.mdpi.com/2076-393X/11/12/1866antibodyELISAnatural planned exposurerotavirus Asequencingswine
spellingShingle Deepak Kumar
Amanda V. Anderson Reever
Jeremy S. Pittman
Nora L. Springer
Kylynn Mallen
Gleyder Roman-Sosa
Neha Sangewar
Mary C. Casey-Moore
Michael D. Bowen
Waithaka Mwangi
Douglas G. Marthaler
Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
Vaccines
antibody
ELISA
natural planned exposure
rotavirus A
sequencing
swine
title Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
title_full Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
title_fullStr Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
title_full_unstemmed Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
title_short Role of Pre-Farrow Natural Planned Exposure of Gilts in Shaping the Passive Antibody Response to Rotavirus A in Piglets
title_sort role of pre farrow natural planned exposure of gilts in shaping the passive antibody response to rotavirus a in piglets
topic antibody
ELISA
natural planned exposure
rotavirus A
sequencing
swine
url https://www.mdpi.com/2076-393X/11/12/1866
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