Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life

The first few days of life are characterized by rapid external and internal changes that require substantial immune system adaptations. Despite growing evidence of the impact of this period on lifelong immune health, this period remains largely uncharted. To identify factors that may impact the traj...

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Main Authors: Sebastiano Montante, Rym Ben-Othman, Nelly Amenyogbe, Asimenia Angelidou, Anita van den Biggelaar, Bing Cai, Yixuan Chen, Alansana Darboe, Joann Diray-Arce, Rebecca Ford, Olubukola Idoko, Amy Lee, Mandy Lo, Kerry McEnaney, Mehrnoush Malek, David Martino, Geraldine Masiria, Oludare A. Odumade, William Pomat, Casey Shannon, Kinga Smolen, The EPIC Consortium, Al Ozonoff, Peter Richmond, Scott Tebbutt, Ofer Levy, Beate Kampmann, Ryan Brinkman, Tobias Kollmann
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Journal of Immunology Research
Online Access:http://dx.doi.org/10.1155/2024/1117796
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author Sebastiano Montante
Rym Ben-Othman
Nelly Amenyogbe
Asimenia Angelidou
Anita van den Biggelaar
Bing Cai
Yixuan Chen
Alansana Darboe
Joann Diray-Arce
Rebecca Ford
Olubukola Idoko
Amy Lee
Mandy Lo
Kerry McEnaney
Mehrnoush Malek
David Martino
Geraldine Masiria
Oludare A. Odumade
William Pomat
Casey Shannon
Kinga Smolen
The EPIC Consortium
Al Ozonoff
Peter Richmond
Scott Tebbutt
Ofer Levy
Beate Kampmann
Ryan Brinkman
Tobias Kollmann
author_facet Sebastiano Montante
Rym Ben-Othman
Nelly Amenyogbe
Asimenia Angelidou
Anita van den Biggelaar
Bing Cai
Yixuan Chen
Alansana Darboe
Joann Diray-Arce
Rebecca Ford
Olubukola Idoko
Amy Lee
Mandy Lo
Kerry McEnaney
Mehrnoush Malek
David Martino
Geraldine Masiria
Oludare A. Odumade
William Pomat
Casey Shannon
Kinga Smolen
The EPIC Consortium
Al Ozonoff
Peter Richmond
Scott Tebbutt
Ofer Levy
Beate Kampmann
Ryan Brinkman
Tobias Kollmann
author_sort Sebastiano Montante
collection DOAJ
description The first few days of life are characterized by rapid external and internal changes that require substantial immune system adaptations. Despite growing evidence of the impact of this period on lifelong immune health, this period remains largely uncharted. To identify factors that may impact the trajectory of immune development, we conducted stringently standardized, high-throughput phenotyping of peripheral white blood cell (WBC) populations from 796 newborns across two distinct cohorts (The Gambia, West Africa; Papua New Guinea, Melanesia) in the framework of a Human Immunology Project Consortium (HIPC) study. Samples were collected twice from each newborn during the first week of life, first at Day of Life 0 (at birth) and then subsequently at Day of Life 1, 3, or 7 depending on the randomization group the newborn belongs to. The subsequent analysis was conducted at an unprecedented level of detail using flow cytometry and an unbiased automated gating algorithm. The results showed that WBC composition in peripheral blood changes along patterns highly conserved across populations and environments. Changes across days of life were most pronounced in the innate myeloid compartment. Breastfeeding, and at a smaller scale neonatal vaccination, were associated with changes in peripheral blood neutrophil and monocyte cell counts. Our results suggest a common trajectory of immune development in newborns and possible association with timing of breastfeeding initiation, which may contribute to immune-mediated protection from infection in early life. These data begin to outline a specific window of opportunity for interventions that could deliberately direct WBC composition, and with that, immune trajectory and thus ontogeny in early life. This trial is registered with NCT03246230.
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spelling doaj-art-3ad7341bf7814ea7b8cbe60b995dd7c02025-02-03T07:23:37ZengWileyJournal of Immunology Research2314-71562024-01-01202410.1155/2024/1117796Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human LifeSebastiano Montante0Rym Ben-Othman1Nelly Amenyogbe2Asimenia Angelidou3Anita van den Biggelaar4Bing Cai5Yixuan Chen6Alansana Darboe7Joann Diray-Arce8Rebecca Ford9Olubukola Idoko10Amy Lee11Mandy Lo12Kerry McEnaney13Mehrnoush Malek14David Martino15Geraldine Masiria16Oludare A. Odumade17William Pomat18Casey Shannon19Kinga Smolen20The EPIC Consortium21Al Ozonoff22Peter Richmond23Scott Tebbutt24Ofer Levy25Beate Kampmann26Ryan Brinkman27Tobias Kollmann28BC Cancer AgencyTelethon Kids InstituteTelethon Kids InstitutePrecision Vaccines ProgramWesfarmers Centre of Vaccines and Infectious DiseasesDepartment of PediatricsBC Cancer AgencyVaccines and Immunity ThemePrecision Vaccines ProgramPapua New Guinea Institute of Medical ResearchDepartment of Clinical ResearchDepartment of Molecular Biology and BiochemistryTelethon Kids InstitutePrecision Vaccines ProgramBC Cancer AgencyWal-yan Respiratory Research CentrePapua New Guinea Institute of Medical ResearchPrecision Vaccines ProgramPapua New Guinea Institute of Medical ResearchPROOF Centre of ExcellencePrecision Vaccines ProgramNIH, National Institute of HealthBroad Institute of MIT and HarvardDivision of PediatricsPROOF Centre of ExcellenceBroad Institute of MIT and HarvardVaccines and Immunity ThemeBC Cancer AgencyTelethon Kids InstituteThe first few days of life are characterized by rapid external and internal changes that require substantial immune system adaptations. Despite growing evidence of the impact of this period on lifelong immune health, this period remains largely uncharted. To identify factors that may impact the trajectory of immune development, we conducted stringently standardized, high-throughput phenotyping of peripheral white blood cell (WBC) populations from 796 newborns across two distinct cohorts (The Gambia, West Africa; Papua New Guinea, Melanesia) in the framework of a Human Immunology Project Consortium (HIPC) study. Samples were collected twice from each newborn during the first week of life, first at Day of Life 0 (at birth) and then subsequently at Day of Life 1, 3, or 7 depending on the randomization group the newborn belongs to. The subsequent analysis was conducted at an unprecedented level of detail using flow cytometry and an unbiased automated gating algorithm. The results showed that WBC composition in peripheral blood changes along patterns highly conserved across populations and environments. Changes across days of life were most pronounced in the innate myeloid compartment. Breastfeeding, and at a smaller scale neonatal vaccination, were associated with changes in peripheral blood neutrophil and monocyte cell counts. Our results suggest a common trajectory of immune development in newborns and possible association with timing of breastfeeding initiation, which may contribute to immune-mediated protection from infection in early life. These data begin to outline a specific window of opportunity for interventions that could deliberately direct WBC composition, and with that, immune trajectory and thus ontogeny in early life. This trial is registered with NCT03246230.http://dx.doi.org/10.1155/2024/1117796
spellingShingle Sebastiano Montante
Rym Ben-Othman
Nelly Amenyogbe
Asimenia Angelidou
Anita van den Biggelaar
Bing Cai
Yixuan Chen
Alansana Darboe
Joann Diray-Arce
Rebecca Ford
Olubukola Idoko
Amy Lee
Mandy Lo
Kerry McEnaney
Mehrnoush Malek
David Martino
Geraldine Masiria
Oludare A. Odumade
William Pomat
Casey Shannon
Kinga Smolen
The EPIC Consortium
Al Ozonoff
Peter Richmond
Scott Tebbutt
Ofer Levy
Beate Kampmann
Ryan Brinkman
Tobias Kollmann
Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
Journal of Immunology Research
title Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
title_full Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
title_fullStr Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
title_full_unstemmed Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
title_short Breastfeeding and Neonatal Age Influence Neutrophil-Driven Ontogeny of Blood Cell Populations in the First Week of Human Life
title_sort breastfeeding and neonatal age influence neutrophil driven ontogeny of blood cell populations in the first week of human life
url http://dx.doi.org/10.1155/2024/1117796
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