Breastfeeding Is Associated with Lower Likelihood of Helicobacter Pylori Colonization in Babies, Based on a Prospective USA Maternal-Infant Cohort.
Antibiotics
Breastfeeding
Cytokines
Helicobacter pylori
Immunomodulation
Infectious diseases
Journal
Digestive diseases and sciences
ISSN: 1573-2568
Titre abrégé: Dig Dis Sci
Pays: United States
ID NLM: 7902782
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
31
05
2021
accepted:
20
12
2021
pubmed:
5
2
2022
medline:
26
10
2022
entrez:
4
2
2022
Statut:
ppublish
Résumé
Mother-to-child transmission of Helicobacter pylori (H. pylori) is the primary source of intrafamilial spread in early childhood in regions of high H. pylori prevalence. However, early-in-life H. pylori colonization and associated protective or risk factors have not been fully evaluated in lower prevalence regions, such as the USA. Therefore, from a well-characterized prospective US cohort, we selected women who provided fecal samples during pregnancy and had paired fecal samples from their babies up to 24 months postpartum. We evaluated maternal and baby factors associated with likelihood of H. pylori colonization in the babies. Fecal antigen testing was used to determine H. pylori status. We also evaluated the association between maternal breastmilk cytokines and H. pylori colonization in breastfed babies. Among included mother-baby pairs (n = 66), H. pylori prevalence was 31.8% in mothers and 19.7% in their babies. Dominant breastfeeding (adjusted odds ratio [aOR] 0.17, 95% CI 0.03-0.98) and maternal IBD (aOR 0.05, 95% CI 0.01-0.27) were associated with significantly lower likelihood of H. pylori colonization among babies; no other clinical factors were associated with H. pylori colonization in the babies. Matrix metalloproteinase-10 (MMP-10) and tumor necrosis factor-related activation-induced cytokine expression were significantly higher in breastmilk of mothers with H. pylori positive vs negative babies. Consistent with data from high H. pylori prevalence regions, our findings suggest dominant breastfeeding may protect against early H. pylori colonization. Downregulation of pro-inflammatory cytokines such as MMP-10 may be relevant in mediating this protection among breastfed babies, but more data are needed.
Sections du résumé
BACKGROUND
Mother-to-child transmission of Helicobacter pylori (H. pylori) is the primary source of intrafamilial spread in early childhood in regions of high H. pylori prevalence. However, early-in-life H. pylori colonization and associated protective or risk factors have not been fully evaluated in lower prevalence regions, such as the USA.
AIMS
Therefore, from a well-characterized prospective US cohort, we selected women who provided fecal samples during pregnancy and had paired fecal samples from their babies up to 24 months postpartum. We evaluated maternal and baby factors associated with likelihood of H. pylori colonization in the babies. Fecal antigen testing was used to determine H. pylori status. We also evaluated the association between maternal breastmilk cytokines and H. pylori colonization in breastfed babies.
RESULTS
Among included mother-baby pairs (n = 66), H. pylori prevalence was 31.8% in mothers and 19.7% in their babies. Dominant breastfeeding (adjusted odds ratio [aOR] 0.17, 95% CI 0.03-0.98) and maternal IBD (aOR 0.05, 95% CI 0.01-0.27) were associated with significantly lower likelihood of H. pylori colonization among babies; no other clinical factors were associated with H. pylori colonization in the babies. Matrix metalloproteinase-10 (MMP-10) and tumor necrosis factor-related activation-induced cytokine expression were significantly higher in breastmilk of mothers with H. pylori positive vs negative babies.
CONCLUSIONS
Consistent with data from high H. pylori prevalence regions, our findings suggest dominant breastfeeding may protect against early H. pylori colonization. Downregulation of pro-inflammatory cytokines such as MMP-10 may be relevant in mediating this protection among breastfed babies, but more data are needed.
Identifiants
pubmed: 35119598
doi: 10.1007/s10620-021-07371-x
pii: 10.1007/s10620-021-07371-x
pmc: PMC9349469
mid: NIHMS1778073
doi:
Substances chimiques
Matrix Metalloproteinase 10
EC 3.4.24.22
RANK Ligand
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
5149-5157Subventions
Organisme : CSRD VA
ID : IK2 CX002027
Pays : United States
Organisme : AHRQ HHS
ID : K12 HS026395
Pays : United States
Organisme : NIDDK NIH HHS
ID : K23 DK129762
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA116087
Pays : United States
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Hooi JKY, Lai WY, Ng WK, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017. https://doi.org/10.1053/j.gastro.2017.04.022.
Amedei A, Codolo G, Del Prete G, de Bernard M, D’Elios MM. The effect of Helicobacter pylori on asthma and allergy. J Asthma Allergy. 2010. https://doi.org/10.2147/JAA.S8971.
Papamichael K, Konstantopoulos P, Mantzaris GJ. Helicobacter pylori infection and inflammatory bowel disease: is there a link? World J Gastroenterol. 2014;20:6374-6385. https://doi.org/10.3748/wjg.v20.i21.6374.
Shah SC, Tepler A, Peek RM, Colombel JF, Hirano I, Narula N. Association Between Helicobacter pylori Exposure and Decreased Odds of Eosinophilic Esophagitis—A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2019. https://doi.org/10.1016/j.cgh.2019.01.013.
Gold BD. New approaches to Helicobacter pylori infection in children. Curr Gastroenterol Rep. 2001;3:235-247. https://doi.org/10.1007/s11894-001-0028-1.
Malaty HM, Logan ND, Graham DY, Ramchatesingh JE. Helicobacter pylori infection in preschool and school-aged minority children: Effect of socioeconomic indicators and breast-feeding practices. Clin Infect Dis. 2001. https://doi.org/10.1086/320148.
Malaty HM, El-Kasabany A, Graham DY, et al. Age at acquisition of Helicobacter pylori infection: A follow-up study from infancy to adulthood. Lancet. 2002. https://doi.org/10.1016/S0140-6736(02)08025-X.
Rothenbacher D, Bodeb G, Brenner H. History of breastfeeding and Helicobacter pylori infection in pre-school children: Results of a population-based study from Germany. Int J Epidemiol. 2002. https://doi.org/10.1093/ije/31.3.632.
Weyermann M, Borowski C, Bode G, et al. Helicobacter pylori-specific immune response in maternal serum, cord blood, and human milk among mothers with and without current Helicobacter pylori infection. Pediatr Res. 2005. https://doi.org/10.1203/01.PDR.0000181370.67474.FD.
Weyermann M, Rothenbacher D, Brenner H. Acquisition of helicobacter pylori infection in early childhood: Independent contributions of infected mothers, fathers, and siblings. Am J Gastroenterol. 2009. https://doi.org/10.1038/ajg.2008.61.
Chak E, Rutherford GW, Steinmaus C. The role of breast-feeding in the prevention of Helicobacter pylori infection: A systematic review. Clin Infect Dis. 2009. https://doi.org/10.1086/596499.
Okuda M, Miyashiro E, Koike M, Okuda S, Minami K, Yoshikawa N. Breast-feeding prevents Helicobacter pylori infection in early childhood. Pediatr Int. 2001. https://doi.org/10.1046/j.1442-200X.2001.01481.x.
Peter I, Maldonado-Contreras A, Eisele C, et al. A dietary intervention to improve the microbiome composition of pregnant women with Crohn’s disease and their offspring: The MELODY (Modulating Early Life Microbiome through Dietary Intervention in Pregnancy) trial design. Contemp Clin Trials Commun. 2020. https://doi.org/10.1016/j.conctc.2020.100573.
Assarsson E, Lundberg M, Holmquist G, et al. Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability. PLoS One. 2014. https://doi.org/10.1371/journal.pone.0095192.
Fredriksson S, Gullberg M, Jarvius J, et al. Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol. 2002. https://doi.org/10.1038/nbt0502-473.
Huang J, Khademi M, Fugger L, et al. Inflammation-related plasma and CSF biomarkers for multiple sclerosis. Proc Natl Acad Sci U S A. 2020. https://doi.org/10.1073/pnas.1912839117.
Santaella A, Kuiperij HB, Van Rumund A, et al. Inflammation biomarker discovery in Parkinson’s disease and atypical parkinsonisms. BMC Neurol. 2020. https://doi.org/10.1186/s12883-020-1608-8.
Chiu CY, Yeh KW, Lin G, et al. Metabolomics reveals dynamic metabolic changes associated with age in early childhood. PLoS One. 2016. https://doi.org/10.1371/journal.pone.0149823.
Monteleone P, Monteleone AM, Troisi J, et al. Metabolomics signatures of acutely ill and short-term weight recovered women with anorexia nervosa. Mol Psychiatry. 2019. https://doi.org/10.1038/s41380-019-0573-3.
Perez-Perez GI, Olivares AZ, Foo FY, et al. Seroprevalence of Helicobacter pylori in New York City populations originating in East Asia. J Urban Heal. 2005. https://doi.org/10.1093/jurban/jti093.
Everhart JE, Kruszon-Moran D, Perez-Perez GI, Tralka TS, McQuillan G. Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis. 2000. https://doi.org/10.1086/315384.
Malaty HM, Graham DY, Klein DG, Adam EE, Evans DJ. Transmission of helicobacter pylori infection studies in families of healthy individuals. Scand J Gastroenterol. 1991. https://doi.org/10.3109/00365529108996244.
AXON ATR. Review article Is Helicobacter pylori transmitted by the gastro‐oral route? Aliment Pharmacol Ther. 1995. https://doi.org/10.1111/j.1365-2036.1995.tb00426.x.
Konno M, Fujii N, Yokota SI, et al. Five-year follow-up study of mother-to-child transmission of Helicobacter pylori infection detected by a random amplified polymorphic DNA fingerprinting method. J Clin Microbiol. 2005. https://doi.org/10.1128/JCM.43.5.2246-2250.2005.
Ashorn M, Mäki M, Hällström M, et al. Helicobacter pylori infection in finnish children and adolescents a serologic Cross-sectional and follow-up study. Scand J Gastroenterol. 1995. https://doi.org/10.3109/00365529509101594.
Rotbenbacher D, Inceoglu J, Bode G, Brenner H. Acquisition of Helicobacter pylori infection in a high-risk population occurs within the first 2 years of life. J Pediatr. 2000. https://doi.org/10.1016/s0022-3476(00)77103-4.
Kienesberger S, Perez-Perez GI, Olivares AZ, et al. When is Helicobacter pylori acquired in populations in developing countries? A birth-cohort study in Bangladeshi children. Gut Microbes. 2018. https://doi.org/10.1080/19490976.2017.1421887.
Thai JD, Gregory KE. Bioactive factors in human breast milk attenuate intestinal inflammation during early life. Nutrients. 2020. https://doi.org/10.3390/nu12020581.
Weaver LT. Helicobacter pylori infection, nutrition and growth of West African infants. Trans R Soc Trop Med Hyg. 1995;89:347-350. https://doi.org/10.1016/0035-9203(95)90002-0.
Thomas JE, Austin S, Dale A, et al. Protection by human milk IgA against Helicobacter pylori infection in infancy. Lancet. 1993. https://doi.org/10.1016/0140-6736(93)91327-I
Clyne M, Thomas J, Weaver L, Drumm B. In vitro evaluation of the role of antibodies against Helicobacter pylori in inhibiting adherence of the organism to gastric cells. Gut. 1997. https://doi.org/10.1136/gut.40.6.731.
Costa AM, Ferreira RM, Pinto-Ribeiro I, et al. Helicobacter pylori activates matrix metalloproteinase 10 in gastric epithelial cells via EGFR and ERK-mediated pathways. J Infect Dis. 2016. https://doi.org/10.1093/infdis/jiw031.
Lv Y pin, Cheng P, Zhang J yu, et al. Helicobacter pylori-induced matrix metallopeptidase-10 promotes gastric bacterial colonization and gastritis. Sci Adv. 2019. https://doi.org/10.1126/sciadv.aau6547.
.Kronsteiner B, Bassaganya-Riera J, Philipson N, Hontecillas R. Novel insights on the role of CD8+ T cells and cytotoxic responses during Helicobacter pylori infection. Gut Microbes. 2014. https://doi.org/10.4161/gmic.28899.
Perri F, Pastore M, Leandro G, et al. Helicobacter pylori infection and growth delay in older children. Arch Dis Child. 1997. https://doi.org/10.1136/adc.77.1.46.
Thomas JE, Dale A, Bunn JEG, et al. Early Helicobacter pylori colonisation: the association with growth faltering in The Gambia. Arch Dis Child, 2004. https://doi.org/10.1136/adc.2002.015313.
Fall CHD, Goggin PM, Hawtin P, Fine D, Duggleby S. Growth in infancy, infant feeding, childhood living conditions, and Helicobacter pylori infection at age 70. Arch Dis Child. 1997. https://doi.org/10.1136/adc.77.4.310.
George S, Mamani N, Lucero Y, et al. Detection of Helicobacter pylori by real-time PCR for 16s rRNA in Stools of noninfected healthy children, using ELISA antigen stool test as the gold standard. Helicobacter. 2016. https://doi.org/10.1111/hel.12318.
Tepler A, Narula N, Peek RM, et al. Systematic review with meta-analysis: association between Helicobacter pylori CagA seropositivity and odds of inflammatory bowel disease. Aliment Pharmacol Ther. 2019. https://doi.org/10.1111/apt.15306.