Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants

Functional gastrointestinal disorders (FGIDs) are a common concern during the first year of life. Recognized as gut-brain axis disorders by Rome IV criteria, FGIDs etiology is linked to altered gut-brain interaction, intestinal physiology, and microbiota. In this regard, probiotics have emerged as a...

Full description

Bibliographic Details
Main Authors: Erola Astó, Pol Huedo, Tatiana Altadill, Meritxell Aguiló García, Maura Sticco, Marta Perez, Jordi Espadaler-Mazo
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.741391/full
_version_ 1819282282285891584
author Erola Astó
Erola Astó
Pol Huedo
Tatiana Altadill
Tatiana Altadill
Meritxell Aguiló García
Maura Sticco
Marta Perez
Jordi Espadaler-Mazo
author_facet Erola Astó
Erola Astó
Pol Huedo
Tatiana Altadill
Tatiana Altadill
Meritxell Aguiló García
Maura Sticco
Marta Perez
Jordi Espadaler-Mazo
author_sort Erola Astó
collection DOAJ
description Functional gastrointestinal disorders (FGIDs) are a common concern during the first year of life. Recognized as gut-brain axis disorders by Rome IV criteria, FGIDs etiology is linked to altered gut-brain interaction, intestinal physiology, and microbiota. In this regard, probiotics have emerged as a promising therapy for infant FGIDs. In this study, we have investigated the probiotic potential of the strains Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041—isolated from healthy children’s feces—in the treatment of FGIDs. To this scope, genome sequences of both strains were obtained and subjected to in silico analyses. No virulence factors were detected for any strain and only the non-transferable erm(49) gene, which confers resistance to erythromycin and clindamycin, was identified in the genome of B. longum KABP042. Safety of both strains was confirmed by acute oral toxicity in rats. In vitro characterization revealed that the strains tolerate gastric and bile challenges and display a great adhesion capacity to human intestinal cells. The two strains mediate adhesion by different mechanisms and, when combined, synergically induce the expression of Caco-2 tight junction proteins. Moreover, growth inhibition experiments demonstrated the ability of the two strains alone and in combination to antagonize diverse Gram-negative and Gram-positive bacterial pathogens during sessile and planktonic growth. Pathogens’ inhibition was mostly mediated by the production of organic acids, but neutralization experiments strongly suggested the presence of additional antimicrobial compounds in probiotic culture supernatants such as the bacteriocin Lantibiotic B, whose gene was detected in the genome of B. longum KABP042. Finally, an exploratory, observational, pilot study involving 36 infants diagnosed with at least one FGID (infant colic and/or functional constipation) showed the probiotic formula was well tolerated and FGID severity was significantly reduced after 14 days of treatment with the 2 strains. Overall, this work provides evidence of the probiotic and synergic properties of strains B. longum KABP042 and P. pentosaceus KABP041, and of their potential to treat pediatric FGIDs.Clinical Trial Registration: [www.ClinicalTrials.gov], [identifier NCT04944628].
first_indexed 2024-12-24T01:13:06Z
format Article
id doaj.art-7f723398e17b4f618255922e4a3db5af
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-24T01:13:06Z
publishDate 2022-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-7f723398e17b4f618255922e4a3db5af2022-12-21T17:22:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-01-011210.3389/fmicb.2021.741391741391Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in InfantsErola Astó0Erola Astó1Pol Huedo2Tatiana Altadill3Tatiana Altadill4Meritxell Aguiló García5Maura Sticco6Marta Perez7Jordi Espadaler-Mazo8R&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainBasic Sciences Department, Universitat Internacional de Catalunya, Barcelona, SpainR&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainR&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainBasic Sciences Department, Universitat Internacional de Catalunya, Barcelona, SpainR&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainPediatric Primary Care Local Health Authority, ASL Caserta, Caserta, ItalyR&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainR&D Department, AB-Biotics S.A. (Part of Kaneka Corporation), Barcelona, SpainFunctional gastrointestinal disorders (FGIDs) are a common concern during the first year of life. Recognized as gut-brain axis disorders by Rome IV criteria, FGIDs etiology is linked to altered gut-brain interaction, intestinal physiology, and microbiota. In this regard, probiotics have emerged as a promising therapy for infant FGIDs. In this study, we have investigated the probiotic potential of the strains Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041—isolated from healthy children’s feces—in the treatment of FGIDs. To this scope, genome sequences of both strains were obtained and subjected to in silico analyses. No virulence factors were detected for any strain and only the non-transferable erm(49) gene, which confers resistance to erythromycin and clindamycin, was identified in the genome of B. longum KABP042. Safety of both strains was confirmed by acute oral toxicity in rats. In vitro characterization revealed that the strains tolerate gastric and bile challenges and display a great adhesion capacity to human intestinal cells. The two strains mediate adhesion by different mechanisms and, when combined, synergically induce the expression of Caco-2 tight junction proteins. Moreover, growth inhibition experiments demonstrated the ability of the two strains alone and in combination to antagonize diverse Gram-negative and Gram-positive bacterial pathogens during sessile and planktonic growth. Pathogens’ inhibition was mostly mediated by the production of organic acids, but neutralization experiments strongly suggested the presence of additional antimicrobial compounds in probiotic culture supernatants such as the bacteriocin Lantibiotic B, whose gene was detected in the genome of B. longum KABP042. Finally, an exploratory, observational, pilot study involving 36 infants diagnosed with at least one FGID (infant colic and/or functional constipation) showed the probiotic formula was well tolerated and FGID severity was significantly reduced after 14 days of treatment with the 2 strains. Overall, this work provides evidence of the probiotic and synergic properties of strains B. longum KABP042 and P. pentosaceus KABP041, and of their potential to treat pediatric FGIDs.Clinical Trial Registration: [www.ClinicalTrials.gov], [identifier NCT04944628].https://www.frontiersin.org/articles/10.3389/fmicb.2021.741391/fullprobioticsantimicrobial activityintestinal epitheliumtight junction proteinsFGIDconstipation
spellingShingle Erola Astó
Erola Astó
Pol Huedo
Tatiana Altadill
Tatiana Altadill
Meritxell Aguiló García
Maura Sticco
Marta Perez
Jordi Espadaler-Mazo
Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
Frontiers in Microbiology
probiotics
antimicrobial activity
intestinal epithelium
tight junction proteins
FGID
constipation
title Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
title_full Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
title_fullStr Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
title_full_unstemmed Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
title_short Probiotic Properties of Bifidobacterium longum KABP042 and Pediococcus pentosaceus KABP041 Show Potential to Counteract Functional Gastrointestinal Disorders in an Observational Pilot Trial in Infants
title_sort probiotic properties of bifidobacterium longum kabp042 and pediococcus pentosaceus kabp041 show potential to counteract functional gastrointestinal disorders in an observational pilot trial in infants
topic probiotics
antimicrobial activity
intestinal epithelium
tight junction proteins
FGID
constipation
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.741391/full
work_keys_str_mv AT erolaasto probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT erolaasto probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT polhuedo probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT tatianaaltadill probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT tatianaaltadill probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT meritxellaguilogarcia probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT maurasticco probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT martaperez probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants
AT jordiespadalermazo probioticpropertiesofbifidobacteriumlongumkabp042andpediococcuspentosaceuskabp041showpotentialtocounteractfunctionalgastrointestinaldisordersinanobservationalpilottrialininfants