Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants

Edward P.K. Parker; Christina Bronowski; Kulandaipalayam Natarajan C. Sindhu; Sudhir Babji; Blossom Benny; Noelia Carmona-Vicente; Nedson Chasweka; End Chinyama; Nigel A. Cunliffe; Queen Dube; Sidhartha Giri; Nicholas C. Grassly; Annai Gunasekaran; Deborah Howarth; Sushil Immanuel; Khuzwayo C. Jere; Beate Kampmann; Jenna Lowe; Jonathan Mandolo; Ira Praharaj; Bakthavatsalam Sandya Rani; Sophia Silas; Vivek Kumar Srinivasan; Mark Turner; Srinivasan Venugopal; Valsan Philip Verghese; Alistair C. Darby; Gagandeep Kang; Miren Iturriza-Gómara

doi:10.1038/s41467-021-27074-1

Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants

Edward P.K. Parker
, Christina Bronowski
, Kulandaipalayam Natarajan C. Sindhu
, Sudhir Babji
, Blossom Benny
, Noelia Carmona-Vicente
, Nedson Chasweka
, End Chinyama
, Nigel A. Cunliffe
, Queen Dube
, Sidhartha Giri
, Nicholas C. Grassly
, Annai Gunasekaran
, Deborah Howarth
, Sushil Immanuel
, Khuzwayo C. Jere
, Beate Kampmann
, Jenna Lowe
, Jonathan Mandolo
, Ira Praharaj

Bakthavatsalam Sandya Rani, Sophia Silas, Vivek Kumar Srinivasan, Mark Turner, Srinivasan Venugopal, Valsan Philip Verghese, Alistair C. Darby, Gagandeep Kang, Miren Iturriza-Gómara

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

43 Citations (Scopus)

Abstract

Identifying risk factors for impaired oral rotavirus vaccine (ORV) efficacy in low-income countries may lead to improvements in vaccine design and delivery. In this prospective cohort study, we measure maternal rotavirus antibodies, environmental enteric dysfunction (EED), and bacterial gut microbiota development among infants receiving two doses of Rotarix in India (n = 307), Malawi (n = 119), and the UK (n = 60), using standardised methods across cohorts. We observe ORV shedding and seroconversion rates to be significantly lower in Malawi and India than the UK. Maternal rotavirus-specific antibodies in serum and breastmilk are negatively correlated with ORV response in India and Malawi, mediated partly by a reduction in ORV shedding. In the UK, ORV shedding is not inhibited despite comparable maternal antibody levels to the other cohorts. In both India and Malawi, increased microbiota diversity is negatively correlated with ORV immunogenicity, suggesting that high early-life microbial exposure may contribute to impaired vaccine efficacy.

Original language	English
Article number	7288
Journal	Nature Communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-021-27074-1
Publication status	Published - 1 Dec 2021
Externally published	Yes

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Parker, E. P. K., Bronowski, C., Sindhu, K. N. C., Babji, S., Benny, B., Carmona-Vicente, N., Chasweka, N., Chinyama, E., Cunliffe, N. A., Dube, Q., Giri, S., Grassly, N. C., Gunasekaran, A., Howarth, D., Immanuel, S., Jere, K. C., Kampmann, B., Lowe, J., Mandolo, J., ... Iturriza-Gómara, M. (2021). Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants. Nature Communications, 12(1), Article 7288. https://doi.org/10.1038/s41467-021-27074-1

@article{e2931e04faf1409193797d00bea3fb15,

title = "Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants",

abstract = "Identifying risk factors for impaired oral rotavirus vaccine (ORV) efficacy in low-income countries may lead to improvements in vaccine design and delivery. In this prospective cohort study, we measure maternal rotavirus antibodies, environmental enteric dysfunction (EED), and bacterial gut microbiota development among infants receiving two doses of Rotarix in India (n = 307), Malawi (n = 119), and the UK (n = 60), using standardised methods across cohorts. We observe ORV shedding and seroconversion rates to be significantly lower in Malawi and India than the UK. Maternal rotavirus-specific antibodies in serum and breastmilk are negatively correlated with ORV response in India and Malawi, mediated partly by a reduction in ORV shedding. In the UK, ORV shedding is not inhibited despite comparable maternal antibody levels to the other cohorts. In both India and Malawi, increased microbiota diversity is negatively correlated with ORV immunogenicity, suggesting that high early-life microbial exposure may contribute to impaired vaccine efficacy.",

author = "Parker, \{Edward P.K.\} and Christina Bronowski and Sindhu, \{Kulandaipalayam Natarajan C.\} and Sudhir Babji and Blossom Benny and Noelia Carmona-Vicente and Nedson Chasweka and End Chinyama and Cunliffe, \{Nigel A.\} and Queen Dube and Sidhartha Giri and Grassly, \{Nicholas C.\} and Annai Gunasekaran and Deborah Howarth and Sushil Immanuel and Jere, \{Khuzwayo C.\} and Beate Kampmann and Jenna Lowe and Jonathan Mandolo and Ira Praharaj and Rani, \{Bakthavatsalam Sandya\} and Sophia Silas and Srinivasan, \{Vivek Kumar\} and Mark Turner and Srinivasan Venugopal and Verghese, \{Valsan Philip\} and Darby, \{Alistair C.\} and Gagandeep Kang and Miren Iturriza-G{\'o}mara",

year = "2021",

month = dec,

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doi = "10.1038/s41467-021-27074-1",

language = "English",

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Parker, EPK, Bronowski, C, Sindhu, KNC, Babji, S, Benny, B, Carmona-Vicente, N, Chasweka, N, Chinyama, E, Cunliffe, NA, Dube, Q, Giri, S, Grassly, NC, Gunasekaran, A, Howarth, D, Immanuel, S, Jere, KC, Kampmann, B, Lowe, J, Mandolo, J, Praharaj, I, Rani, BS, Silas, S, Srinivasan, VK, Turner, M, Venugopal, S, Verghese, VP, Darby, AC, Kang, G & Iturriza-Gómara, M 2021, 'Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants', Nature Communications, vol. 12, no. 1, 7288. https://doi.org/10.1038/s41467-021-27074-1

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T1 - Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants

AU - Parker, Edward P.K.

AU - Bronowski, Christina

AU - Sindhu, Kulandaipalayam Natarajan C.

AU - Babji, Sudhir

AU - Benny, Blossom

AU - Carmona-Vicente, Noelia

AU - Chasweka, Nedson

AU - Chinyama, End

AU - Cunliffe, Nigel A.

AU - Dube, Queen

AU - Giri, Sidhartha

AU - Grassly, Nicholas C.

AU - Gunasekaran, Annai

AU - Howarth, Deborah

AU - Immanuel, Sushil

AU - Jere, Khuzwayo C.

AU - Kampmann, Beate

AU - Lowe, Jenna

AU - Mandolo, Jonathan

AU - Praharaj, Ira

AU - Rani, Bakthavatsalam Sandya

AU - Silas, Sophia

AU - Srinivasan, Vivek Kumar

AU - Turner, Mark

AU - Venugopal, Srinivasan

AU - Verghese, Valsan Philip

AU - Darby, Alistair C.

AU - Kang, Gagandeep

AU - Iturriza-Gómara, Miren

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Identifying risk factors for impaired oral rotavirus vaccine (ORV) efficacy in low-income countries may lead to improvements in vaccine design and delivery. In this prospective cohort study, we measure maternal rotavirus antibodies, environmental enteric dysfunction (EED), and bacterial gut microbiota development among infants receiving two doses of Rotarix in India (n = 307), Malawi (n = 119), and the UK (n = 60), using standardised methods across cohorts. We observe ORV shedding and seroconversion rates to be significantly lower in Malawi and India than the UK. Maternal rotavirus-specific antibodies in serum and breastmilk are negatively correlated with ORV response in India and Malawi, mediated partly by a reduction in ORV shedding. In the UK, ORV shedding is not inhibited despite comparable maternal antibody levels to the other cohorts. In both India and Malawi, increased microbiota diversity is negatively correlated with ORV immunogenicity, suggesting that high early-life microbial exposure may contribute to impaired vaccine efficacy.

AB - Identifying risk factors for impaired oral rotavirus vaccine (ORV) efficacy in low-income countries may lead to improvements in vaccine design and delivery. In this prospective cohort study, we measure maternal rotavirus antibodies, environmental enteric dysfunction (EED), and bacterial gut microbiota development among infants receiving two doses of Rotarix in India (n = 307), Malawi (n = 119), and the UK (n = 60), using standardised methods across cohorts. We observe ORV shedding and seroconversion rates to be significantly lower in Malawi and India than the UK. Maternal rotavirus-specific antibodies in serum and breastmilk are negatively correlated with ORV response in India and Malawi, mediated partly by a reduction in ORV shedding. In the UK, ORV shedding is not inhibited despite comparable maternal antibody levels to the other cohorts. In both India and Malawi, increased microbiota diversity is negatively correlated with ORV immunogenicity, suggesting that high early-life microbial exposure may contribute to impaired vaccine efficacy.

U2 - 10.1038/s41467-021-27074-1

DO - 10.1038/s41467-021-27074-1

M3 - Article

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 7288

ER -

Impact of maternal antibodies and microbiota development on the immunogenicity of oral rotavirus vaccine in African, Indian, and European infants

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