Allergy development is associated with consumption of breastmilk with a reduced microbial richness in the first month of life.
Asthma
/ epidemiology
Breast Feeding
Child
Child, Preschool
Female
Flow Cytometry
Food Hypersensitivity
/ epidemiology
Gastrointestinal Microbiome
Humans
Hypersensitivity
/ epidemiology
Immunoglobulin A
/ immunology
Infant
Infant, Newborn
Male
Microbiota
/ genetics
Milk, Human
/ immunology
Probiotics
/ therapeutic use
RNA, Ribosomal, 16S
IgA
allergy
breastmilk
microbiota
mother-infant transfer
Journal
Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology
ISSN: 1399-3038
Titre abrégé: Pediatr Allergy Immunol
Pays: England
ID NLM: 9106718
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
30
06
2019
revised:
08
11
2019
accepted:
12
11
2019
pubmed:
19
11
2019
medline:
5
3
2021
entrez:
19
11
2019
Statut:
ppublish
Résumé
Early colonization with a diverse microbiota seems to play a crucial role for appropriate immune maturation during childhood. Breastmilk microbiota is one important source of microbes for the infant, transferred together with maternal IgA antibodies. We previously observed that allergy development during childhood was associated with aberrant IgA responses to the gut microbiota already at 1 month of age, when the IgA antibodies are predominantly maternally derived in breastfed infants. To determine the microbial composition and IgA-coated bacteria in breastmilk in relation to allergy development in children participating in an intervention trial with pre- and post-natal Lactobacillus reuteri supplementation. A combination of flow cytometric cell sorting and 16S rRNA gene sequencing was used to characterize the bacterial recognition patterns by IgA in breastmilk samples collected one month post-partum from 40 mothers whose children did or did not develop allergic and asthmatic symptoms during the first 7 years of age. The milk fed to children developing allergic manifestations had significantly lower bacterial richness, when compared to the milk given to children that remained healthy. Probiotic treatment influenced the breastmilk microbiota composition. However, the proportions of IgA-coated bacteria, the total bacterial load and the patterns of IgA-coating were similar in breastmilk between mothers of healthy children and those developing allergies. Consumption of breastmilk with a reduced microbial richness in the first month of life may play an important role in allergy development during childhood.
Sections du résumé
BACKGROUND
Early colonization with a diverse microbiota seems to play a crucial role for appropriate immune maturation during childhood. Breastmilk microbiota is one important source of microbes for the infant, transferred together with maternal IgA antibodies. We previously observed that allergy development during childhood was associated with aberrant IgA responses to the gut microbiota already at 1 month of age, when the IgA antibodies are predominantly maternally derived in breastfed infants.
OBJECTIVE
To determine the microbial composition and IgA-coated bacteria in breastmilk in relation to allergy development in children participating in an intervention trial with pre- and post-natal Lactobacillus reuteri supplementation.
METHODS
A combination of flow cytometric cell sorting and 16S rRNA gene sequencing was used to characterize the bacterial recognition patterns by IgA in breastmilk samples collected one month post-partum from 40 mothers whose children did or did not develop allergic and asthmatic symptoms during the first 7 years of age.
RESULTS
The milk fed to children developing allergic manifestations had significantly lower bacterial richness, when compared to the milk given to children that remained healthy. Probiotic treatment influenced the breastmilk microbiota composition. However, the proportions of IgA-coated bacteria, the total bacterial load and the patterns of IgA-coating were similar in breastmilk between mothers of healthy children and those developing allergies.
CONCLUSION
Consumption of breastmilk with a reduced microbial richness in the first month of life may play an important role in allergy development during childhood.
Substances chimiques
Immunoglobulin A
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
250-257Subventions
Organisme : European Research Council
ID : 639226
Pays : International
Informations de copyright
© 2019 EAACI and John Wiley and Sons A/S. Published by John Wiley and Sons Ltd.
Références
Walker A. Breast milk as the gold standard for protective nutrients. J Pediatr. 2010;156(2):S3-7.
Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013;60(1):49-74.
Newburg DS, Walker WA. Protection of the neonate by the innate immune system of developing gut and of human milk. Pediatr Res. 2007;61(1):2-8.
West CE, Jenmalm MC, Prescott SL. The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin Exp Allergy. 2015;45(1):43-53.
West CE, Dzidic M, Prescott SL, Jenmalm MC. Bugging allergy; role of pre-, pro- and synbiotics in allergy prevention. Allergol Int. 2017;66(4):529-538.
Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2014;44(6):842-850.
Jakobsson HE, Abrahamsson TR, Jenmalm MC, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut. 2014;63(4):559-566.
Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol. 2012;129(2):434-440.
Jenmalm MC. The mother-offspring dyad: microbial transmission, immune interactions and allergy development. J Intern Med. 2017;282(6):484-495.
Dzidic M, Abrahamsson TR, Artacho A, et al. Aberrant IgA responses to the gut microbiota during infancy precede asthma and allergy development. J Allergy Clin Immunol. 2017;139(3):1017-1025.e14.
Abrahamsson TR, Jakobsson T, Böttcher MF, et al. Probiotics in prevention of IgE-associated eczema: A double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol. 2007;119(5):1174-1180.
Abrahamsson TR, Jakobsson T, Björkstén B, Oldaeus G, Jenmalm MC. No effect of probiotics on respiratory allergies: a seven-year follow-up of a randomized controlled trial in infancy. Pediatr Allergy Immunol. 2013;24(6):556-561.
Böttcher MF, Abrahamsson TR, Fredriksson M, Jakobsson T, Björkstén B. Low breast milk TGF-β2 is induced by Lactobacillus reuteri supplementation and associates with reduced risk of sensitization during infancy. Pediatr Allergy Immunol. 2008;19(6):497-504.
Simón-Soro Á, D’Auria G, Collado MC, Džunková M, Culshaw S, Mira A. Revealing microbial recognition by specific antibodies. BMC Microbiol. 2015;15(1):132.
Dzidic M, Abrahamsson T, Artacho A, Collado MC, Mira A, Jenmalm MC. Oral microbiota maturation during the first 7 years of life in relation to allergy development. Allergy. 2018;73:2000-2011.
Azad MB, Konya T, Guttman DS, et al. Infant gut microbiota and food sensitization: associations in the first year of life. Clin Exp Allergy. 2015;45(3):632-643.
Tourneur E, Chassin C. Neonatal immune adaptation of the gut and its role during infections. Clin Dev Immunol. 2013;2013:270301.
Fitzstevens JL, Smith KC, Hagadorn JI, Caimano MJ, Matson AP, Brownell EA. Systematic review of the human milk microbiota. Nutr Clin Pract. 2016;32:354-364.
Martín R, Langa S, Reviriego C, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr [Internet]. 2003;143(6):754-758.
Soto A, Martín V, Jiménez E, Mader I, Rodríguez JM, Fernández L. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J Pediatr Gastroenterol Nutr. 2014;59(1):78-88.
Martín V, Maldonado-Barragán A, Moles L, et al. Sharing of bacterial strains between breast milk and infant feces. J Hum Lact. 2012;28(1):36-44.
Benito D, Lozano C, Jiménez E, et al. Characterization of Staphylococcus aureus strains isolated from faeces of healthy neonates and potential mother-to-infant microbial transmission through breastfeeding. FEMS Microbiol Ecol. 2015;91(3):fiv007.
Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestine important to infants' and children's health? J Pediatr Gastroenterol Nutr. 2015;60(3):294-307.
Mshvildadze M, Neu J. The infant intestinal microbiome: friend or foe? Early Hum Dev. 2010;86:67-71.
Hurley WL, Theil PK. Perspectives on immunoglobulins in colostrum and milk. Nutrients. 2011;3(4):442-474.
Donaldson GP, Ladinsky MS, Yu KB, et al. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science. 2018;360(6390):795-800.
McLoughlin K, Schluter J, Rakoff-Nahoum S, Smith AL, Foster KR. Host selection of microbiota via differential adhesion. Cell Host Microbe. 2016;19(4):550-559.
Rogier EW, Frantz AL, Bruno MEC, et al. Secretory antibodies in breast milk promote long-term intestinal homeostasis by regulating the gut microbiota and host gene expression. Proc Natl Acad Sci USA. 2014;111(8):3074-3079.
Abrahamsson TR, Sinkiewicz G, Jakobsson T, Fredrikson M, Björkstén B. Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr. 2009;49:349-354.
Lundberg JO, Carlström M, Weitzberg E. Metabolic effects of dietary nitrate in health and disease. Cell Metab. 2018;28(1):9-22.