Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood

Josh M. Colston; Ruthly Francois; Nora Pisanic; Pablo Peñataro Yori; Benjamin J.J. Mccormick; Maribel Paredes Olortegui; Md Amran Gazi; Erling Svensen; Mondar Maruf Moin Ahmed; Esto Mduma; Jie Liu; Eric R. Houpt; Robert Klapheke; Julia W. Schwarz; Robert L. Atmar; Robert E. Black; Margaret N. Kosek

doi:10.1093/infdis/jiz072

Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood

Josh M. Colston, Ruthly Francois, Nora Pisanic, Pablo Peñataro Yori, Benjamin J.J. Mccormick, Maribel Paredes Olortegui, Md Amran Gazi, Erling Svensen, Mondar Maruf Moin Ahmed, Esto Mduma, Jie Liu, Eric R. Houpt, Robert Klapheke, Julia W. Schwarz, Robert L. Atmar, Robert E. Black, Margaret N. Kosek^* (Corresponding Author)

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

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

37 Citations (Scopus)

Abstract

Background: Histo-blood group antigens (HBGAs) such as fucosyltransferase (FUT)2 and 3 may act as innate host factors that differentially influence susceptibility of individuals and their offspring to pediatric enteric infections. Methods: In 3 community-based birth cohorts, FUT2 and FUT3 statuses were ascertained for mother-child dyads. Quantitative polymerase chain reaction panels tested 3663 diarrheal and 18 148 asymptomatic stool samples for 29 enteropathogens. Cumulative diarrhea and infection incidence were compared by child (n = 520) and mothers' (n = 519) HBGA status and hazard ratios (HRs) derived for all-cause diarrhea and specific enteropathogens. Results: Children of secretor (FUT2 positive) mothers had a 38% increased adjusted risk of all-cause diarrhea (HR = 1.38; 95% confidence interval (CI), 1.15-1.66) and significantly reduced time to first diarrheal episode. Child FUT2 and FUT3 positivity reduced the risk for all-cause diarrhea by 29% (HR = 0.81; 95% CI, 0.71-0.93) and 27% (HR = 0.83; 95% CI, 0.74-0.92), respectively. Strong associations between HBGAs and pathogen-specific infection and diarrhea were observed, particularly for noroviruses, rotaviruses, enterotoxigenic Escherichia coli, and Campylobacter jejuni/coli. Conclusions: Histo-blood group antigens affect incidence of all-cause diarrhea and enteric infections at magnitudes comparable to many common disease control interventions. Studies measuring impacts of interventions on childhood enteric disease should account for both child and mothers' HBGA status.

Original language	English
Pages (from-to)	151-162
Number of pages	12
Journal	Journal of Infectious Diseases
Volume	220
Issue number	1
Early online date	15 Feb 2019
DOIs	https://doi.org/10.1093/infdis/jiz072
Publication status	Published - 1 Jul 2019

Bibliographical note

Funding Information:
Financial support. This work was funded by the Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development Project (MAL-ED) is carried out as a collaborative project funded by the Bill & Melinda Gates Foundation (BMGF) (BMGF-47075), the Foundation for the National Institutes of Health, and the National Institutes of Health, Fogarty International Center, whereas additional support was obtained from BMGF for the examination of host innate factors on enteric disease risk and enteropathy (Grants OPP1066146 and OPP1152146; to M. N. K.). Additional funding was obtained from teh Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases, Johns Hopkins School of Medicine (to M. N. K) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institues of health 1UL1TR001079.

Acknowledgments. We thank the participants, their families, and the study community for their dedicated time and effort to better the understanding the transmission and more enduring impact of enteric infections in early childhood. We also thank the following: Jan Vinje (Centers for Disease Control and Prevention) for critical input and manuscript review; Dr. Leah Jager for consultation regarding the statistical analysis; Dr. Ben Jann (University of Bern, Switzerland) for guidance in generating the figures; Christine Szymanski for insight and encouragement, particularly regarding Campylobacter infection and disease patency; Chris Damman and Anita Zaidi for input on early iterations of the analysis; and Dick Guerrant for final reflections.

Keywords

antibodies, bacterial
bacterial vaccines
colonization factor antigens
controlled human infection model
diarrhea, prevention and control
Escherichia coli infections
fimbriae proteins
immunization, passive
milk proteins, immunology
randomized controlled clinical trial

UN SDGs

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

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Colston, J. M., Francois, R., Pisanic, N., Peñataro Yori, P., Mccormick, B. J. J., Olortegui, M. P., Gazi, M. A., Svensen, E., Ahmed, M. M. M., Mduma, E., Liu, J., Houpt, E. R., Klapheke, R., Schwarz, J. W., Atmar, R. L., Black, R. E., & Kosek, M. N. (2019). Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood. Journal of Infectious Diseases, 220(1), 151-162. https://doi.org/10.1093/infdis/jiz072

Colston, JM, Francois, R, Pisanic, N, Peñataro Yori, P, Mccormick, BJJ, Olortegui, MP, Gazi, MA, Svensen, E, Ahmed, MMM, Mduma, E, Liu, J, Houpt, ER, Klapheke, R, Schwarz, JW, Atmar, RL, Black, RE & Kosek, MN 2019, 'Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood', Journal of Infectious Diseases, vol. 220, no. 1, pp. 151-162. https://doi.org/10.1093/infdis/jiz072

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title = "Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood",

abstract = "Background: Histo-blood group antigens (HBGAs) such as fucosyltransferase (FUT)2 and 3 may act as innate host factors that differentially influence susceptibility of individuals and their offspring to pediatric enteric infections. Methods: In 3 community-based birth cohorts, FUT2 and FUT3 statuses were ascertained for mother-child dyads. Quantitative polymerase chain reaction panels tested 3663 diarrheal and 18 148 asymptomatic stool samples for 29 enteropathogens. Cumulative diarrhea and infection incidence were compared by child (n = 520) and mothers' (n = 519) HBGA status and hazard ratios (HRs) derived for all-cause diarrhea and specific enteropathogens. Results: Children of secretor (FUT2 positive) mothers had a 38% increased adjusted risk of all-cause diarrhea (HR = 1.38; 95% confidence interval (CI), 1.15-1.66) and significantly reduced time to first diarrheal episode. Child FUT2 and FUT3 positivity reduced the risk for all-cause diarrhea by 29% (HR = 0.81; 95% CI, 0.71-0.93) and 27% (HR = 0.83; 95% CI, 0.74-0.92), respectively. Strong associations between HBGAs and pathogen-specific infection and diarrhea were observed, particularly for noroviruses, rotaviruses, enterotoxigenic Escherichia coli, and Campylobacter jejuni/coli. Conclusions: Histo-blood group antigens affect incidence of all-cause diarrhea and enteric infections at magnitudes comparable to many common disease control interventions. Studies measuring impacts of interventions on childhood enteric disease should account for both child and mothers' HBGA status.",

keywords = "antibodies, bacterial, bacterial vaccines, colonization factor antigens, controlled human infection model, diarrhea, prevention and control, Escherichia coli infections, fimbriae proteins, immunization, passive, milk proteins, immunology, randomized controlled clinical trial",

author = "Colston, {Josh M.} and Ruthly Francois and Nora Pisanic and {Pe{\~n}ataro Yori}, Pablo and Mccormick, {Benjamin J.J.} and Olortegui, {Maribel Paredes} and Gazi, {Md Amran} and Erling Svensen and Ahmed, {Mondar Maruf Moin} and Esto Mduma and Jie Liu and Houpt, {Eric R.} and Robert Klapheke and Schwarz, {Julia W.} and Atmar, {Robert L.} and Black, {Robert E.} and Kosek, {Margaret N.}",

note = "Funding Information: Financial support. This work was funded by the Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development Project (MAL-ED) is carried out as a collaborative project funded by the Bill & Melinda Gates Foundation (BMGF) (BMGF-47075), the Foundation for the National Institutes of Health, and the National Institutes of Health, Fogarty International Center, whereas additional support was obtained from BMGF for the examination of host innate factors on enteric disease risk and enteropathy (Grants OPP1066146 and OPP1152146; to M. N. K.). Additional funding was obtained from teh Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases, Johns Hopkins School of Medicine (to M. N. K) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institues of health 1UL1TR001079. Acknowledgments. We thank the participants, their families, and the study community for their dedicated time and effort to better the understanding the transmission and more enduring impact of enteric infections in early childhood. We also thank the following: Jan Vinje (Centers for Disease Control and Prevention) for critical input and manuscript review; Dr. Leah Jager for consultation regarding the statistical analysis; Dr. Ben Jann (University of Bern, Switzerland) for guidance in generating the figures; Christine Szymanski for insight and encouragement, particularly regarding Campylobacter infection and disease patency; Chris Damman and Anita Zaidi for input on early iterations of the analysis; and Dick Guerrant for final reflections.",

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doi = "10.1093/infdis/jiz072",

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T1 - Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood

AU - Colston, Josh M.

AU - Francois, Ruthly

AU - Pisanic, Nora

AU - Peñataro Yori, Pablo

AU - Mccormick, Benjamin J.J.

AU - Olortegui, Maribel Paredes

AU - Gazi, Md Amran

AU - Svensen, Erling

AU - Ahmed, Mondar Maruf Moin

AU - Mduma, Esto

AU - Liu, Jie

AU - Houpt, Eric R.

AU - Klapheke, Robert

AU - Schwarz, Julia W.

AU - Atmar, Robert L.

AU - Black, Robert E.

AU - Kosek, Margaret N.

N1 - Funding Information: Financial support. This work was funded by the Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health and Development Project (MAL-ED) is carried out as a collaborative project funded by the Bill & Melinda Gates Foundation (BMGF) (BMGF-47075), the Foundation for the National Institutes of Health, and the National Institutes of Health, Fogarty International Center, whereas additional support was obtained from BMGF for the examination of host innate factors on enteric disease risk and enteropathy (Grants OPP1066146 and OPP1152146; to M. N. K.). Additional funding was obtained from teh Sherrilyn and Ken Fisher Center for Environmental Infectious Diseases, Johns Hopkins School of Medicine (to M. N. K) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institues of health 1UL1TR001079. Acknowledgments. We thank the participants, their families, and the study community for their dedicated time and effort to better the understanding the transmission and more enduring impact of enteric infections in early childhood. We also thank the following: Jan Vinje (Centers for Disease Control and Prevention) for critical input and manuscript review; Dr. Leah Jager for consultation regarding the statistical analysis; Dr. Ben Jann (University of Bern, Switzerland) for guidance in generating the figures; Christine Szymanski for insight and encouragement, particularly regarding Campylobacter infection and disease patency; Chris Damman and Anita Zaidi for input on early iterations of the analysis; and Dick Guerrant for final reflections.

PY - 2019/7/1

Y1 - 2019/7/1

N2 - Background: Histo-blood group antigens (HBGAs) such as fucosyltransferase (FUT)2 and 3 may act as innate host factors that differentially influence susceptibility of individuals and their offspring to pediatric enteric infections. Methods: In 3 community-based birth cohorts, FUT2 and FUT3 statuses were ascertained for mother-child dyads. Quantitative polymerase chain reaction panels tested 3663 diarrheal and 18 148 asymptomatic stool samples for 29 enteropathogens. Cumulative diarrhea and infection incidence were compared by child (n = 520) and mothers' (n = 519) HBGA status and hazard ratios (HRs) derived for all-cause diarrhea and specific enteropathogens. Results: Children of secretor (FUT2 positive) mothers had a 38% increased adjusted risk of all-cause diarrhea (HR = 1.38; 95% confidence interval (CI), 1.15-1.66) and significantly reduced time to first diarrheal episode. Child FUT2 and FUT3 positivity reduced the risk for all-cause diarrhea by 29% (HR = 0.81; 95% CI, 0.71-0.93) and 27% (HR = 0.83; 95% CI, 0.74-0.92), respectively. Strong associations between HBGAs and pathogen-specific infection and diarrhea were observed, particularly for noroviruses, rotaviruses, enterotoxigenic Escherichia coli, and Campylobacter jejuni/coli. Conclusions: Histo-blood group antigens affect incidence of all-cause diarrhea and enteric infections at magnitudes comparable to many common disease control interventions. Studies measuring impacts of interventions on childhood enteric disease should account for both child and mothers' HBGA status.

AB - Background: Histo-blood group antigens (HBGAs) such as fucosyltransferase (FUT)2 and 3 may act as innate host factors that differentially influence susceptibility of individuals and their offspring to pediatric enteric infections. Methods: In 3 community-based birth cohorts, FUT2 and FUT3 statuses were ascertained for mother-child dyads. Quantitative polymerase chain reaction panels tested 3663 diarrheal and 18 148 asymptomatic stool samples for 29 enteropathogens. Cumulative diarrhea and infection incidence were compared by child (n = 520) and mothers' (n = 519) HBGA status and hazard ratios (HRs) derived for all-cause diarrhea and specific enteropathogens. Results: Children of secretor (FUT2 positive) mothers had a 38% increased adjusted risk of all-cause diarrhea (HR = 1.38; 95% confidence interval (CI), 1.15-1.66) and significantly reduced time to first diarrheal episode. Child FUT2 and FUT3 positivity reduced the risk for all-cause diarrhea by 29% (HR = 0.81; 95% CI, 0.71-0.93) and 27% (HR = 0.83; 95% CI, 0.74-0.92), respectively. Strong associations between HBGAs and pathogen-specific infection and diarrhea were observed, particularly for noroviruses, rotaviruses, enterotoxigenic Escherichia coli, and Campylobacter jejuni/coli. Conclusions: Histo-blood group antigens affect incidence of all-cause diarrhea and enteric infections at magnitudes comparable to many common disease control interventions. Studies measuring impacts of interventions on childhood enteric disease should account for both child and mothers' HBGA status.

KW - antibodies, bacterial

KW - bacterial vaccines

KW - colonization factor antigens

KW - controlled human infection model

KW - diarrhea, prevention and control

KW - Escherichia coli infections

KW - fimbriae proteins

KW - immunization, passive

KW - milk proteins, immunology

KW - randomized controlled clinical trial

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DO - 10.1093/infdis/jiz072

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AN - SCOPUS:85067494577

SN - 0022-1899

VL - 220

SP - 151

EP - 162

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 1

ER -

Effects of Child and Maternal Histo-Blood Group Antigen Status on Symptomatic and Asymptomatic Enteric Infections in Early Childhood

Abstract

Bibliographical note

Keywords

UN SDGs

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