Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine

Michael Eschbaumer; Carolina Stenfeldt; Steven I. Rekant; Juan M. Pacheco; Ethan J. Hartwig; George R. Smoliga; Mary A. Kenney; William T. Golde; Luis L. Rodriguez; Jonathan Arzt

doi:10.1186/s12917-016-0838-x

Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine

Michael Eschbaumer, Carolina Stenfeldt, Steven I. Rekant, Juan M. Pacheco, Ethan J. Hartwig, George R. Smoliga, Mary A. Kenney, William T. Golde, Luis L. Rodriguez, Jonathan Arzt

Veterinary Population Medicine

Research output: Contribution to journal › Article › peer-review

26 Scopus citations

Abstract

Background: In order to investigate host factors associated with the establishment of persistent foot-and-mouth disease virus (FMDV) infection, the systemic response to vaccination and challenge was studied in 47 steers. Eighteen steers that had received a recombinant FMDV A vaccine 2 weeks earlier and 29 non-vaccinated steers were challenged by intra-nasopharyngeal deposition of FMDV A24. For up to 35 days after challenge, host factors including complete blood counts with T lymphocyte subsets, type I/III interferon (IFN) activity, neutralizing and total FMDV-specific antibody titers in serum, as well as antibody-secreting cells (in 6 non-vaccinated animals) were characterized in the context of viral infection dynamics. Results: Vaccination generally induced a strong antibody response. There was a transient peak of FMDV-specific serum IgM in non-vaccinated animals after challenge, while IgM levels in vaccinated animals did not increase further. Both groups had a lasting increase of specific IgG and neutralizing antibody after challenge. Substantial systemic IFN activity in non-vaccinated animals coincided with viremia, and no IFN or viremia was detected in vaccinated animals. After challenge, circulating lymphocytes decreased in non-vaccinated animals, coincident with viremia, IFN activity, and clinical disease, whereas lymphocyte and monocyte counts in vaccinated animals were unaffected by vaccination but transiently increased after challenge. The CD4⁺/CD8⁺ T cell ratio in non-vaccinated animals increased during acute infection, driven by an absolute decrease of CD8⁺ cells. Conclusions: The incidence of FMDV persistence was 61.5 % in non-vaccinated and 54.5 % in vaccinated animals. Overall, the systemic factors examined were not associated with the FMDV carrier/non-carrier divergence; however, significant differences were identified between responses of non-vaccinated and vaccinated cattle.

Original language	English (US)
Article number	205
Journal	BMC Veterinary Research
Volume	12
Issue number	1
DOIs	https://doi.org/10.1186/s12917-016-0838-x
State	Published - Sep 15 2016

Bibliographical note

Funding Information:
This work was funded in part by CRIS project 1940-32000-057-00D (USDA, Agricultural Research Service), as well as through an interagency agreement with the Science and Technology Directorate of the U.S. Department of Homeland Security under Award Number HSHQPM-13-X-00131. ME, CS, and SIR are recipients of PIADC Research Participation Program fellowships, administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement with the U.S. Department of Energy. The sponsors had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication.

Publisher Copyright:
© 2016 The Author(s).

Keywords

Carrier
ELISA
ELISPOT
FMDV
Flow cytometry
Interferon
Lymphopenia
Persistence
Vaccination

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Eschbaumer, M., Stenfeldt, C., Rekant, S. I., Pacheco, J. M., Hartwig, E. J., Smoliga, G. R., Kenney, M. A., Golde, W. T., Rodriguez, L. L., & Arzt, J. (2016). Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine. BMC Veterinary Research, 12(1), Article 205. https://doi.org/10.1186/s12917-016-0838-x

Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine. / Eschbaumer, Michael; Stenfeldt, Carolina; Rekant, Steven I. et al.
In: BMC Veterinary Research, Vol. 12, No. 1, 205, 15.09.2016.

Research output: Contribution to journal › Article › peer-review

Eschbaumer, M, Stenfeldt, C, Rekant, SI, Pacheco, JM, Hartwig, EJ, Smoliga, GR, Kenney, MA, Golde, WT, Rodriguez, LL & Arzt, J 2016, 'Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine', BMC Veterinary Research, vol. 12, no. 1, 205. https://doi.org/10.1186/s12917-016-0838-x

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abstract = "Background: In order to investigate host factors associated with the establishment of persistent foot-and-mouth disease virus (FMDV) infection, the systemic response to vaccination and challenge was studied in 47 steers. Eighteen steers that had received a recombinant FMDV A vaccine 2 weeks earlier and 29 non-vaccinated steers were challenged by intra-nasopharyngeal deposition of FMDV A24. For up to 35 days after challenge, host factors including complete blood counts with T lymphocyte subsets, type I/III interferon (IFN) activity, neutralizing and total FMDV-specific antibody titers in serum, as well as antibody-secreting cells (in 6 non-vaccinated animals) were characterized in the context of viral infection dynamics. Results: Vaccination generally induced a strong antibody response. There was a transient peak of FMDV-specific serum IgM in non-vaccinated animals after challenge, while IgM levels in vaccinated animals did not increase further. Both groups had a lasting increase of specific IgG and neutralizing antibody after challenge. Substantial systemic IFN activity in non-vaccinated animals coincided with viremia, and no IFN or viremia was detected in vaccinated animals. After challenge, circulating lymphocytes decreased in non-vaccinated animals, coincident with viremia, IFN activity, and clinical disease, whereas lymphocyte and monocyte counts in vaccinated animals were unaffected by vaccination but transiently increased after challenge. The CD4+/CD8+ T cell ratio in non-vaccinated animals increased during acute infection, driven by an absolute decrease of CD8+ cells. Conclusions: The incidence of FMDV persistence was 61.5 % in non-vaccinated and 54.5 % in vaccinated animals. Overall, the systemic factors examined were not associated with the FMDV carrier/non-carrier divergence; however, significant differences were identified between responses of non-vaccinated and vaccinated cattle.",

keywords = "Carrier, ELISA, ELISPOT, FMDV, Flow cytometry, Interferon, Lymphopenia, Persistence, Vaccination",

author = "Michael Eschbaumer and Carolina Stenfeldt and Rekant, {Steven I.} and Pacheco, {Juan M.} and Hartwig, {Ethan J.} and Smoliga, {George R.} and Kenney, {Mary A.} and Golde, {William T.} and Rodriguez, {Luis L.} and Jonathan Arzt",

note = "Funding Information: This work was funded in part by CRIS project 1940-32000-057-00D (USDA, Agricultural Research Service), as well as through an interagency agreement with the Science and Technology Directorate of the U.S. Department of Homeland Security under Award Number HSHQPM-13-X-00131. ME, CS, and SIR are recipients of PIADC Research Participation Program fellowships, administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement with the U.S. Department of Energy. The sponsors had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication. Publisher Copyright: {\textcopyright} 2016 The Author(s).",

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doi = "10.1186/s12917-016-0838-x",

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T1 - Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine

AU - Eschbaumer, Michael

AU - Stenfeldt, Carolina

AU - Rekant, Steven I.

AU - Pacheco, Juan M.

AU - Hartwig, Ethan J.

AU - Smoliga, George R.

AU - Kenney, Mary A.

AU - Golde, William T.

AU - Rodriguez, Luis L.

AU - Arzt, Jonathan

N1 - Funding Information: This work was funded in part by CRIS project 1940-32000-057-00D (USDA, Agricultural Research Service), as well as through an interagency agreement with the Science and Technology Directorate of the U.S. Department of Homeland Security under Award Number HSHQPM-13-X-00131. ME, CS, and SIR are recipients of PIADC Research Participation Program fellowships, administered by the Oak Ridge Institute for Science and Education (ORISE) through an interagency agreement with the U.S. Department of Energy. The sponsors had no involvement in the study design, in the collection, analysis and interpretation of data, in the writing of the manuscript, or in the decision to submit the manuscript for publication. Publisher Copyright: © 2016 The Author(s).

PY - 2016/9/15

Y1 - 2016/9/15

N2 - Background: In order to investigate host factors associated with the establishment of persistent foot-and-mouth disease virus (FMDV) infection, the systemic response to vaccination and challenge was studied in 47 steers. Eighteen steers that had received a recombinant FMDV A vaccine 2 weeks earlier and 29 non-vaccinated steers were challenged by intra-nasopharyngeal deposition of FMDV A24. For up to 35 days after challenge, host factors including complete blood counts with T lymphocyte subsets, type I/III interferon (IFN) activity, neutralizing and total FMDV-specific antibody titers in serum, as well as antibody-secreting cells (in 6 non-vaccinated animals) were characterized in the context of viral infection dynamics. Results: Vaccination generally induced a strong antibody response. There was a transient peak of FMDV-specific serum IgM in non-vaccinated animals after challenge, while IgM levels in vaccinated animals did not increase further. Both groups had a lasting increase of specific IgG and neutralizing antibody after challenge. Substantial systemic IFN activity in non-vaccinated animals coincided with viremia, and no IFN or viremia was detected in vaccinated animals. After challenge, circulating lymphocytes decreased in non-vaccinated animals, coincident with viremia, IFN activity, and clinical disease, whereas lymphocyte and monocyte counts in vaccinated animals were unaffected by vaccination but transiently increased after challenge. The CD4+/CD8+ T cell ratio in non-vaccinated animals increased during acute infection, driven by an absolute decrease of CD8+ cells. Conclusions: The incidence of FMDV persistence was 61.5 % in non-vaccinated and 54.5 % in vaccinated animals. Overall, the systemic factors examined were not associated with the FMDV carrier/non-carrier divergence; however, significant differences were identified between responses of non-vaccinated and vaccinated cattle.

AB - Background: In order to investigate host factors associated with the establishment of persistent foot-and-mouth disease virus (FMDV) infection, the systemic response to vaccination and challenge was studied in 47 steers. Eighteen steers that had received a recombinant FMDV A vaccine 2 weeks earlier and 29 non-vaccinated steers were challenged by intra-nasopharyngeal deposition of FMDV A24. For up to 35 days after challenge, host factors including complete blood counts with T lymphocyte subsets, type I/III interferon (IFN) activity, neutralizing and total FMDV-specific antibody titers in serum, as well as antibody-secreting cells (in 6 non-vaccinated animals) were characterized in the context of viral infection dynamics. Results: Vaccination generally induced a strong antibody response. There was a transient peak of FMDV-specific serum IgM in non-vaccinated animals after challenge, while IgM levels in vaccinated animals did not increase further. Both groups had a lasting increase of specific IgG and neutralizing antibody after challenge. Substantial systemic IFN activity in non-vaccinated animals coincided with viremia, and no IFN or viremia was detected in vaccinated animals. After challenge, circulating lymphocytes decreased in non-vaccinated animals, coincident with viremia, IFN activity, and clinical disease, whereas lymphocyte and monocyte counts in vaccinated animals were unaffected by vaccination but transiently increased after challenge. The CD4+/CD8+ T cell ratio in non-vaccinated animals increased during acute infection, driven by an absolute decrease of CD8+ cells. Conclusions: The incidence of FMDV persistence was 61.5 % in non-vaccinated and 54.5 % in vaccinated animals. Overall, the systemic factors examined were not associated with the FMDV carrier/non-carrier divergence; however, significant differences were identified between responses of non-vaccinated and vaccinated cattle.

KW - Carrier

KW - ELISA

KW - ELISPOT

KW - FMDV

KW - Flow cytometry

KW - Interferon

KW - Lymphopenia

KW - Persistence

KW - Vaccination

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DO - 10.1186/s12917-016-0838-x

M3 - Article

C2 - 27634113

AN - SCOPUS:84987858722

SN - 1746-6148

VL - 12

JO - BMC Veterinary Research

JF - BMC Veterinary Research

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ER -

Systemic immune response and virus persistence after foot-and-mouth disease virus infection of naïve cattle and cattle vaccinated with a homologous adenovirus-vectored vaccine

Abstract

Bibliographical note

Keywords

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