Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India

Ira Praharaj; Edward P.K. Parker; Sidhartha Giri; David J. Allen; Sophia Silas; R. Revathi; Saravanakumar Puthupalayam Kaliappan; Jacob John; Jasmine Helan Prasad; Beate Kampmann; Miren Iturriza-Go'Mara; Nicholas C. Grassly; Gagandeep Kang

doi:10.1093/infdis/jiy568

Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India

Ira Praharaj^*, Edward P.K. Parker, Sidhartha Giri, David J. Allen, Sophia Silas, R. Revathi, Saravanakumar Puthupalayam Kaliappan, Jacob John, Jasmine Helan Prasad, Beate Kampmann, Miren Iturriza-Go'Mara, Nicholas C. Grassly, Gagandeep Kang

^*Corresponding author for this work

Virus Reference Department General

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

38 Citations (Scopus)

Abstract

Background. Oral poliovirus vaccine (OPV) is less immunogenic in low-or middle-income than in high-income countries. We tested whether bacterial and viral components of the intestinal microbiota are associated with this phenomenon. Methods. We assessed the prevalence of enteropathogens using TaqMan array cards 14 days before and at vaccination in 704 Indian infants (aged 6-11 months) receiving monovalent type 3 OPV (CTRI/2014/05/004588). Nonpolio enterovirus (NPEV) serotypes were identifed by means of VP1 sequencing. In 120 infants, the prevaccination bacterial microbiota was characterized using 16S ribosomal RNA sequencing. Results. We detected 56 NPEV serotypes on the day of vaccination. Concurrent NPEVs were associated with a reduction in OPV seroconversion, consistent across species (odds ratio [95% confdence interval], 0.57 [.36-.90], 0.61 [.43-.86], and 0.69 [.41-1.16] for species A, B, and C, respectively). Recently acquired enterovirus infections, detected at vaccination but not 14 days earlier, had a greater interfering effect on monovalent type 3 OPV seroresponse than did persistent infections, with enterovirus detected at both time points (seroconversion in 44 of 127 infants [35%] vs 63 of 129 [49%]; P =.02). Te abundance of specifc bacterial taxa did not differ signifcantly according to OPV response, although the microbiota was more diverse in nonresponders at the time of vaccination. Conclusion. Enteric viruses have a greater impact on OPV response than the bacterial microbiota, with recent enterovirus infections having a greater inhibitory effect than persistent infections.

Original language	English
Pages (from-to)	1178-1186
Number of pages	9
Journal	Journal of Infectious Diseases
Volume	219
Issue number	8
DOIs	https://doi.org/10.1093/infdis/jiy568
Publication status	Published - 8 Apr 2019

Bibliographical note

Funding Information:
Potential conflicts of interests. M. I. G. received support from an Institutional Strategic Support Fund Wellcome Trust grant awarded to the University of Liverpool and the Health Protection Research Unit in Gastrointestinal Infections, National Institute for Health Research at the University of Liverpool (grant NIHR HPRU 2012-10038). All other authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

Funding Information:
Disclaimer. The views expressed are those of the authors and do not necessarily represent those of the National Institute for Health Research or Public Health England. The funder had no role in the study design, data collection, data analysis, data interpretation, or writing of the report. Financial support. This study was funded by the Bill and Melinda Gates Foundation (grant OPP1039135 to N. C. G. and G. K.).

Keywords

16S rRNA
Bacterial microbiota
Next generation sequencing
Nonpolio enteroviruses
OPV

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1093/infdis/jiy568

Cite this

Praharaj, I., Parker, E. P. K., Giri, S., Allen, D. J., Silas, S., Revathi, R., Kaliappan, S. P., John, J., Prasad, J. H., Kampmann, B., Iturriza-Go'Mara, M., Grassly, N. C., & Kang, G. (2019). Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India. Journal of Infectious Diseases, 219(8), 1178-1186. https://doi.org/10.1093/infdis/jiy568

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title = "Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India",

abstract = "Background. Oral poliovirus vaccine (OPV) is less immunogenic in low-or middle-income than in high-income countries. We tested whether bacterial and viral components of the intestinal microbiota are associated with this phenomenon. Methods. We assessed the prevalence of enteropathogens using TaqMan array cards 14 days before and at vaccination in 704 Indian infants (aged 6-11 months) receiving monovalent type 3 OPV (CTRI/2014/05/004588). Nonpolio enterovirus (NPEV) serotypes were identifed by means of VP1 sequencing. In 120 infants, the prevaccination bacterial microbiota was characterized using 16S ribosomal RNA sequencing. Results. We detected 56 NPEV serotypes on the day of vaccination. Concurrent NPEVs were associated with a reduction in OPV seroconversion, consistent across species (odds ratio [95% confdence interval], 0.57 [.36-.90], 0.61 [.43-.86], and 0.69 [.41-1.16] for species A, B, and C, respectively). Recently acquired enterovirus infections, detected at vaccination but not 14 days earlier, had a greater interfering effect on monovalent type 3 OPV seroresponse than did persistent infections, with enterovirus detected at both time points (seroconversion in 44 of 127 infants [35%] vs 63 of 129 [49%]; P =.02). Te abundance of specifc bacterial taxa did not differ signifcantly according to OPV response, although the microbiota was more diverse in nonresponders at the time of vaccination. Conclusion. Enteric viruses have a greater impact on OPV response than the bacterial microbiota, with recent enterovirus infections having a greater inhibitory effect than persistent infections.",

keywords = "16S rRNA, Bacterial microbiota, Next generation sequencing, Nonpolio enteroviruses, OPV",

author = "Ira Praharaj and Parker, {Edward P.K.} and Sidhartha Giri and Allen, {David J.} and Sophia Silas and R. Revathi and Kaliappan, {Saravanakumar Puthupalayam} and Jacob John and Prasad, {Jasmine Helan} and Beate Kampmann and Miren Iturriza-Go'Mara and Grassly, {Nicholas C.} and Gagandeep Kang",

note = "Funding Information: Potential conflicts of interests. M. I. G. received support from an Institutional Strategic Support Fund Wellcome Trust grant awarded to the University of Liverpool and the Health Protection Research Unit in Gastrointestinal Infections, National Institute for Health Research at the University of Liverpool (grant NIHR HPRU 2012-10038). All other authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. Funding Information: Disclaimer. The views expressed are those of the authors and do not necessarily represent those of the National Institute for Health Research or Public Health England. The funder had no role in the study design, data collection, data analysis, data interpretation, or writing of the report. Financial support. This study was funded by the Bill and Melinda Gates Foundation (grant OPP1039135 to N. C. G. and G. K.).",

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Praharaj, I, Parker, EPK, Giri, S, Allen, DJ, Silas, S, Revathi, R, Kaliappan, SP, John, J, Prasad, JH, Kampmann, B, Iturriza-Go'Mara, M, Grassly, NC & Kang, G 2019, 'Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India', Journal of Infectious Diseases, vol. 219, no. 8, pp. 1178-1186. https://doi.org/10.1093/infdis/jiy568

TY - JOUR

T1 - Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response

T2 - A study from south India

AU - Praharaj, Ira

AU - Parker, Edward P.K.

AU - Giri, Sidhartha

AU - Allen, David J.

AU - Silas, Sophia

AU - Revathi, R.

AU - Kaliappan, Saravanakumar Puthupalayam

AU - John, Jacob

AU - Prasad, Jasmine Helan

AU - Kampmann, Beate

AU - Iturriza-Go'Mara, Miren

AU - Grassly, Nicholas C.

AU - Kang, Gagandeep

N1 - Funding Information: Potential conflicts of interests. M. I. G. received support from an Institutional Strategic Support Fund Wellcome Trust grant awarded to the University of Liverpool and the Health Protection Research Unit in Gastrointestinal Infections, National Institute for Health Research at the University of Liverpool (grant NIHR HPRU 2012-10038). All other authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. Funding Information: Disclaimer. The views expressed are those of the authors and do not necessarily represent those of the National Institute for Health Research or Public Health England. The funder had no role in the study design, data collection, data analysis, data interpretation, or writing of the report. Financial support. This study was funded by the Bill and Melinda Gates Foundation (grant OPP1039135 to N. C. G. and G. K.).

PY - 2019/4/8

Y1 - 2019/4/8

N2 - Background. Oral poliovirus vaccine (OPV) is less immunogenic in low-or middle-income than in high-income countries. We tested whether bacterial and viral components of the intestinal microbiota are associated with this phenomenon. Methods. We assessed the prevalence of enteropathogens using TaqMan array cards 14 days before and at vaccination in 704 Indian infants (aged 6-11 months) receiving monovalent type 3 OPV (CTRI/2014/05/004588). Nonpolio enterovirus (NPEV) serotypes were identifed by means of VP1 sequencing. In 120 infants, the prevaccination bacterial microbiota was characterized using 16S ribosomal RNA sequencing. Results. We detected 56 NPEV serotypes on the day of vaccination. Concurrent NPEVs were associated with a reduction in OPV seroconversion, consistent across species (odds ratio [95% confdence interval], 0.57 [.36-.90], 0.61 [.43-.86], and 0.69 [.41-1.16] for species A, B, and C, respectively). Recently acquired enterovirus infections, detected at vaccination but not 14 days earlier, had a greater interfering effect on monovalent type 3 OPV seroresponse than did persistent infections, with enterovirus detected at both time points (seroconversion in 44 of 127 infants [35%] vs 63 of 129 [49%]; P =.02). Te abundance of specifc bacterial taxa did not differ signifcantly according to OPV response, although the microbiota was more diverse in nonresponders at the time of vaccination. Conclusion. Enteric viruses have a greater impact on OPV response than the bacterial microbiota, with recent enterovirus infections having a greater inhibitory effect than persistent infections.

AB - Background. Oral poliovirus vaccine (OPV) is less immunogenic in low-or middle-income than in high-income countries. We tested whether bacterial and viral components of the intestinal microbiota are associated with this phenomenon. Methods. We assessed the prevalence of enteropathogens using TaqMan array cards 14 days before and at vaccination in 704 Indian infants (aged 6-11 months) receiving monovalent type 3 OPV (CTRI/2014/05/004588). Nonpolio enterovirus (NPEV) serotypes were identifed by means of VP1 sequencing. In 120 infants, the prevaccination bacterial microbiota was characterized using 16S ribosomal RNA sequencing. Results. We detected 56 NPEV serotypes on the day of vaccination. Concurrent NPEVs were associated with a reduction in OPV seroconversion, consistent across species (odds ratio [95% confdence interval], 0.57 [.36-.90], 0.61 [.43-.86], and 0.69 [.41-1.16] for species A, B, and C, respectively). Recently acquired enterovirus infections, detected at vaccination but not 14 days earlier, had a greater interfering effect on monovalent type 3 OPV seroresponse than did persistent infections, with enterovirus detected at both time points (seroconversion in 44 of 127 infants [35%] vs 63 of 129 [49%]; P =.02). Te abundance of specifc bacterial taxa did not differ signifcantly according to OPV response, although the microbiota was more diverse in nonresponders at the time of vaccination. Conclusion. Enteric viruses have a greater impact on OPV response than the bacterial microbiota, with recent enterovirus infections having a greater inhibitory effect than persistent infections.

KW - 16S rRNA

KW - Bacterial microbiota

KW - Next generation sequencing

KW - Nonpolio enteroviruses

KW - OPV

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U2 - 10.1093/infdis/jiy568

DO - 10.1093/infdis/jiy568

M3 - Article

C2 - 30247561

AN - SCOPUS:85064498064

SN - 0022-1899

VL - 219

SP - 1178

EP - 1186

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 8

ER -

Influence of nonpolio enteroviruses and the bacterial gut microbiota on oral poliovirus vaccine response: A study from south India

Abstract

Bibliographical note

Keywords

UN SDGs

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