Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis

Abstract Background Relationships between gut microbiomes and airway immunity have been established in murine and human studies of allergy and asthma. Early life Lactobacillus supplementation alters the composition and metabolic productivity of the gut microbiome. However, little is known of how Lac...

Full description

Bibliographic Details
Main Authors: Kathryn J. Ray, Clark Santee, Kathryn McCauley, Ariane R. Panzer, Susan V. Lynch
Format: Article
Language:English
Published: BMC 2022-07-01
Series:BMC Pulmonary Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12890-022-02078-9
_version_ 1811222878752866304
author Kathryn J. Ray
Clark Santee
Kathryn McCauley
Ariane R. Panzer
Susan V. Lynch
author_facet Kathryn J. Ray
Clark Santee
Kathryn McCauley
Ariane R. Panzer
Susan V. Lynch
author_sort Kathryn J. Ray
collection DOAJ
description Abstract Background Relationships between gut microbiomes and airway immunity have been established in murine and human studies of allergy and asthma. Early life Lactobacillus supplementation alters the composition and metabolic productivity of the gut microbiome. However, little is known of how Lactobacillus supplementation impacts the gut microbiota in children with cystic fibrosis (CF) and whether specific microbiota states that arise following gut microbiome manipulation relate to pulmonary outcomes. Methods Stool samples were collected from CF patients enrolled in a multi-center, double-blind, randomized placebo-controlled trial of daily Lactobacillus rhamnosus strain GG (LGG) probiotic supplementation over a 12-month period. Fecal 16S rRNA biomarker sequencing was used to profile fecal bacterial microbiota and analyses were performed in QiiME. Results Bifidobacteria-dominated fecal microbiota were more likely to arise in LGG-treated children with CF (P = 0.04). Children with Bifidobacteria-dominated gut microbiota had a reduced rate of pulmonary exacerbations (IRR = 0.55; 95% CI 0.25 to 0.82; P = 0.01), improved pulmonary function (+ 20.00% of predicted value FEV1; 95% CI 8.05 to 31.92; P = 0.001), lower intestinal inflammation (Calprotectin; Coef =  − 16.53 μg g−1 feces; 95% CI − 26.80 to − 6.26; P = 0.002) and required fewer antibiotics (IRR = 0.43; 95% CI 0.22 to 0.69; P = 0.04) compared to children with Bacteroides-dominated microbiota who were less likely to have received LGG. Conclusions The majority of pediatric CF patients in this study possessed a Bacteroides- or Bifidobacteria-dominated gut microbiota. Bifidobacteria-dominated gut microbiota were more likely to be associated with LGG-supplementation and with better clinical outcomes.
first_indexed 2024-04-12T08:23:16Z
format Article
id doaj.art-9cd90028955640fdbad3f8890cd423d9
institution Directory Open Access Journal
issn 1471-2466
language English
last_indexed 2024-04-12T08:23:16Z
publishDate 2022-07-01
publisher BMC
record_format Article
series BMC Pulmonary Medicine
spelling doaj.art-9cd90028955640fdbad3f8890cd423d92022-12-22T03:40:30ZengBMCBMC Pulmonary Medicine1471-24662022-07-012211910.1186/s12890-022-02078-9Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosisKathryn J. Ray0Clark Santee1Kathryn McCauley2Ariane R. Panzer3Susan V. Lynch4Department of Epidemiology and Biostatistics, University of California San Francisco (UCSF)Division of Gastroenterology, Department of Medicine, University of California San Francisco (UCSF)Division of Gastroenterology, Department of Medicine, University of California San Francisco (UCSF)Division of Gastroenterology, Department of Medicine, University of California San Francisco (UCSF)Division of Gastroenterology, Department of Medicine, University of California San Francisco (UCSF)Abstract Background Relationships between gut microbiomes and airway immunity have been established in murine and human studies of allergy and asthma. Early life Lactobacillus supplementation alters the composition and metabolic productivity of the gut microbiome. However, little is known of how Lactobacillus supplementation impacts the gut microbiota in children with cystic fibrosis (CF) and whether specific microbiota states that arise following gut microbiome manipulation relate to pulmonary outcomes. Methods Stool samples were collected from CF patients enrolled in a multi-center, double-blind, randomized placebo-controlled trial of daily Lactobacillus rhamnosus strain GG (LGG) probiotic supplementation over a 12-month period. Fecal 16S rRNA biomarker sequencing was used to profile fecal bacterial microbiota and analyses were performed in QiiME. Results Bifidobacteria-dominated fecal microbiota were more likely to arise in LGG-treated children with CF (P = 0.04). Children with Bifidobacteria-dominated gut microbiota had a reduced rate of pulmonary exacerbations (IRR = 0.55; 95% CI 0.25 to 0.82; P = 0.01), improved pulmonary function (+ 20.00% of predicted value FEV1; 95% CI 8.05 to 31.92; P = 0.001), lower intestinal inflammation (Calprotectin; Coef =  − 16.53 μg g−1 feces; 95% CI − 26.80 to − 6.26; P = 0.002) and required fewer antibiotics (IRR = 0.43; 95% CI 0.22 to 0.69; P = 0.04) compared to children with Bacteroides-dominated microbiota who were less likely to have received LGG. Conclusions The majority of pediatric CF patients in this study possessed a Bacteroides- or Bifidobacteria-dominated gut microbiota. Bifidobacteria-dominated gut microbiota were more likely to be associated with LGG-supplementation and with better clinical outcomes.https://doi.org/10.1186/s12890-022-02078-9Cystic fibrosismicrobiomeLactobacillus rhamnosus GG
spellingShingle Kathryn J. Ray
Clark Santee
Kathryn McCauley
Ariane R. Panzer
Susan V. Lynch
Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
BMC Pulmonary Medicine
Cystic fibrosis
microbiome
Lactobacillus rhamnosus GG
title Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
title_full Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
title_fullStr Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
title_full_unstemmed Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
title_short Gut Bifidobacteria enrichment following oral Lactobacillus-supplementation is associated with clinical improvements in children with cystic fibrosis
title_sort gut bifidobacteria enrichment following oral lactobacillus supplementation is associated with clinical improvements in children with cystic fibrosis
topic Cystic fibrosis
microbiome
Lactobacillus rhamnosus GG
url https://doi.org/10.1186/s12890-022-02078-9
work_keys_str_mv AT kathrynjray gutbifidobacteriaenrichmentfollowingorallactobacillussupplementationisassociatedwithclinicalimprovementsinchildrenwithcysticfibrosis
AT clarksantee gutbifidobacteriaenrichmentfollowingorallactobacillussupplementationisassociatedwithclinicalimprovementsinchildrenwithcysticfibrosis
AT kathrynmccauley gutbifidobacteriaenrichmentfollowingorallactobacillussupplementationisassociatedwithclinicalimprovementsinchildrenwithcysticfibrosis
AT arianerpanzer gutbifidobacteriaenrichmentfollowingorallactobacillussupplementationisassociatedwithclinicalimprovementsinchildrenwithcysticfibrosis
AT susanvlynch gutbifidobacteriaenrichmentfollowingorallactobacillussupplementationisassociatedwithclinicalimprovementsinchildrenwithcysticfibrosis