Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease

Charlotte R Hedin; Neil E McCarthy; Petra Louis; Freda Farquharson; Sara McCartney; Andrew J Stagg; James O Lindsay; Kevin Whelan

doi:10.1016/j.clnu.2021.05.033

Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease

Charlotte R Hedin
, Neil E McCarthy
, Petra Louis
, Freda Farquharson
, Sara McCartney
, Andrew J Stagg
, James O Lindsay
, Kevin Whelan^* (Corresponding Author)

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

Queen Mary University of London
Karolinska University Hospital
Karolinska Institutet
University College London Hospitals NHS Foundation Trust
Rowett Institute, University of Aberdeen
King's College London

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

22 Citations (Scopus)

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Abstract

Background & Aims Siblings of people with Crohn’s disease (CD) share aspects of the disease phenotype (raised faecal calprotectin, altered microbiota), which are markers of risk for their own development of CD. The aim was to determine whether supplementation with prebiotic oligofructose/inulin induces a prebiotic response and impacts the risk phenotype in CD patients and siblings.MethodsPatients with inactive CD (n=19, CD activity index <150) and 12 of their unaffected siblings (with calprotectin >50μg/g) ingested oligofructose/inulin (15g/day) for three weeks. Faecal microbiota (qPCR), intestinal permeability (lactulose-rhamnose test), blood T cells (flowcytometry) and calprotectin (ELISA) were measured at baseline and follow-up.ResultsFollowing oligofructose/inulin, calprotectin did not significantly change in patients (baseline mean 537 SD 535µg/g; follow-up mean 974 SD 1318µg/g, p=0.08) or siblings (baseline mean 73 SD 90µg/g: follow up mean 58 SD 72µg/g, p=0.62). Faecal Bifidobacteria and Bifidobacterium longum increased in patients and siblings; Bifidobacterium adolescentis and Roseburia spp. increased only in siblings. Compared with patients, siblings had a greater magnitude change in Bifidobacteria (+14.6% vs +0.4%, p=0.028), B. adolescentis (+1.1% vs 0.0% p=0.006) and Roseburia spp. (+1.5% vs -0.1% p=0.004). Intestinal permeability decreased significantly in patients after oligofructose/inulin to a level that was similar to siblings. Blood T cell abundance reduced in siblings but not patients following oligofructose/inulin.ConclusionsOligofructose/inulin supplementation did not significantly impact calprotectin, but theprebiotic effect was more marked in healthy siblings compared with patients with inactive CD and was associated with alterations in other CD risk markers. Future research should focus on dietary intervention, including with prebiotics, in the primary prevention of CD.

Original language	English
Pages (from-to)	5009-5019
Number of pages	11
Journal	Clinical Nutrition
Volume	40
Issue number	8
Early online date	23 Jun 2021
DOIs	https://doi.org/10.1016/j.clnu.2021.05.033
Publication status	Published - Aug 2021

Bibliographical note

Funding
This work was supported by a clinical research fellowship granted by the charity Core (Guts UK) (CRH). FMF and PL received financial support from the Scottish Government Rural and Environment Science and Analytical Services.
Acknowledgments
The authors would like to acknowledge BENEO-Orafti, Teinen, Belgium who provided the oligofructose-enriched inulin. The authors would like to thank the patients and the siblings who generously participated in this study.

Funding

This work was supported by a clinical research fellowship granted by the charity Core (Guts UK) (CRH) . FMF and PL received financial support from the Scottish Government Rural and Environment Science and Analytical Services .

UN SDGs

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

SDG 3 Good Health and Well-being

Keywords

Prebiotics
Crohn’s disease
microbiota
Pre-disease
first-degree relative
prevention

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Hedin, C. R., McCarthy, N. E., Louis, P., Farquharson, F., McCartney, S., Stagg, A. J., Lindsay, J. O., & Whelan, K. (2021). Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease. Clinical Nutrition, 40(8), 5009-5019. https://doi.org/10.1016/j.clnu.2021.05.033

Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease. / Hedin, Charlotte R; McCarthy, Neil E; Louis, Petra et al.
In: Clinical Nutrition, Vol. 40, No. 8, 08.2021, p. 5009-5019.

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

Hedin, CR, McCarthy, NE, Louis, P, Farquharson, F, McCartney, S, Stagg, AJ, Lindsay, JO & Whelan, K 2021, 'Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease', Clinical Nutrition, vol. 40, no. 8, pp. 5009-5019. https://doi.org/10.1016/j.clnu.2021.05.033

Hedin CR, McCarthy NE, Louis P, Farquharson F, McCartney S, Stagg AJ et al. Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease. Clinical Nutrition. 2021 Aug;40(8):5009-5019. Epub 2021 Jun 23. doi: 10.1016/j.clnu.2021.05.033

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title = "Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn{\textquoteright}s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease",

abstract = "Background \& Aims Siblings of people with Crohn{\textquoteright}s disease (CD) share aspects of the disease phenotype (raised faecal calprotectin, altered microbiota), which are markers of risk for their own development of CD. The aim was to determine whether supplementation with prebiotic oligofructose/inulin induces a prebiotic response and impacts the risk phenotype in CD patients and siblings.MethodsPatients with inactive CD (n=19, CD activity index <150) and 12 of their unaffected siblings (with calprotectin >50μg/g) ingested oligofructose/inulin (15g/day) for three weeks. Faecal microbiota (qPCR), intestinal permeability (lactulose-rhamnose test), blood T cells (flowcytometry) and calprotectin (ELISA) were measured at baseline and follow-up.ResultsFollowing oligofructose/inulin, calprotectin did not significantly change in patients (baseline mean 537 SD 535µg/g; follow-up mean 974 SD 1318µg/g, p=0.08) or siblings (baseline mean 73 SD 90µg/g: follow up mean 58 SD 72µg/g, p=0.62). Faecal Bifidobacteria and Bifidobacterium longum increased in patients and siblings; Bifidobacterium adolescentis and Roseburia spp. increased only in siblings. Compared with patients, siblings had a greater magnitude change in Bifidobacteria (+14.6\% vs +0.4\%, p=0.028), B. adolescentis (+1.1\% vs 0.0\% p=0.006) and Roseburia spp. (+1.5\% vs -0.1\% p=0.004). Intestinal permeability decreased significantly in patients after oligofructose/inulin to a level that was similar to siblings. Blood T cell abundance reduced in siblings but not patients following oligofructose/inulin.ConclusionsOligofructose/inulin supplementation did not significantly impact calprotectin, but theprebiotic effect was more marked in healthy siblings compared with patients with inactive CD and was associated with alterations in other CD risk markers. Future research should focus on dietary intervention, including with prebiotics, in the primary prevention of CD.",

keywords = "Prebiotics, Crohn{\textquoteright}s disease, microbiota, Pre-disease, first-degree relative, prevention",

author = "Hedin, \{Charlotte R\} and McCarthy, \{Neil E\} and Petra Louis and Freda Farquharson and Sara McCartney and Stagg, \{Andrew J\} and Lindsay, \{James O\} and Kevin Whelan",

note = "Funding This work was supported by a clinical research fellowship granted by the charity Core (Guts UK) (CRH). FMF and PL received financial support from the Scottish Government Rural and Environment Science and Analytical Services. Acknowledgments The authors would like to acknowledge BENEO-Orafti, Teinen, Belgium who provided the oligofructose-enriched inulin. The authors would like to thank the patients and the siblings who generously participated in this study. ",

year = "2021",

month = aug,

doi = "10.1016/j.clnu.2021.05.033",

language = "English",

volume = "40",

pages = "5009--5019",

journal = "Clinical Nutrition",

issn = "0261-5614",

publisher = "Churchill Livingstone",

number = "8",

}

TY - JOUR

T1 - Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease

T2 - a pilot study investigating the potential for primary prevention of inflammatory bowel disease

AU - Hedin, Charlotte R

AU - McCarthy, Neil E

AU - Louis, Petra

AU - Farquharson, Freda

AU - McCartney, Sara

AU - Stagg, Andrew J

AU - Lindsay, James O

AU - Whelan, Kevin

N1 - Funding This work was supported by a clinical research fellowship granted by the charity Core (Guts UK) (CRH). FMF and PL received financial support from the Scottish Government Rural and Environment Science and Analytical Services. Acknowledgments The authors would like to acknowledge BENEO-Orafti, Teinen, Belgium who provided the oligofructose-enriched inulin. The authors would like to thank the patients and the siblings who generously participated in this study.

PY - 2021/8

Y1 - 2021/8

N2 - Background & Aims Siblings of people with Crohn’s disease (CD) share aspects of the disease phenotype (raised faecal calprotectin, altered microbiota), which are markers of risk for their own development of CD. The aim was to determine whether supplementation with prebiotic oligofructose/inulin induces a prebiotic response and impacts the risk phenotype in CD patients and siblings.MethodsPatients with inactive CD (n=19, CD activity index <150) and 12 of their unaffected siblings (with calprotectin >50μg/g) ingested oligofructose/inulin (15g/day) for three weeks. Faecal microbiota (qPCR), intestinal permeability (lactulose-rhamnose test), blood T cells (flowcytometry) and calprotectin (ELISA) were measured at baseline and follow-up.ResultsFollowing oligofructose/inulin, calprotectin did not significantly change in patients (baseline mean 537 SD 535µg/g; follow-up mean 974 SD 1318µg/g, p=0.08) or siblings (baseline mean 73 SD 90µg/g: follow up mean 58 SD 72µg/g, p=0.62). Faecal Bifidobacteria and Bifidobacterium longum increased in patients and siblings; Bifidobacterium adolescentis and Roseburia spp. increased only in siblings. Compared with patients, siblings had a greater magnitude change in Bifidobacteria (+14.6% vs +0.4%, p=0.028), B. adolescentis (+1.1% vs 0.0% p=0.006) and Roseburia spp. (+1.5% vs -0.1% p=0.004). Intestinal permeability decreased significantly in patients after oligofructose/inulin to a level that was similar to siblings. Blood T cell abundance reduced in siblings but not patients following oligofructose/inulin.ConclusionsOligofructose/inulin supplementation did not significantly impact calprotectin, but theprebiotic effect was more marked in healthy siblings compared with patients with inactive CD and was associated with alterations in other CD risk markers. Future research should focus on dietary intervention, including with prebiotics, in the primary prevention of CD.

AB - Background & Aims Siblings of people with Crohn’s disease (CD) share aspects of the disease phenotype (raised faecal calprotectin, altered microbiota), which are markers of risk for their own development of CD. The aim was to determine whether supplementation with prebiotic oligofructose/inulin induces a prebiotic response and impacts the risk phenotype in CD patients and siblings.MethodsPatients with inactive CD (n=19, CD activity index <150) and 12 of their unaffected siblings (with calprotectin >50μg/g) ingested oligofructose/inulin (15g/day) for three weeks. Faecal microbiota (qPCR), intestinal permeability (lactulose-rhamnose test), blood T cells (flowcytometry) and calprotectin (ELISA) were measured at baseline and follow-up.ResultsFollowing oligofructose/inulin, calprotectin did not significantly change in patients (baseline mean 537 SD 535µg/g; follow-up mean 974 SD 1318µg/g, p=0.08) or siblings (baseline mean 73 SD 90µg/g: follow up mean 58 SD 72µg/g, p=0.62). Faecal Bifidobacteria and Bifidobacterium longum increased in patients and siblings; Bifidobacterium adolescentis and Roseburia spp. increased only in siblings. Compared with patients, siblings had a greater magnitude change in Bifidobacteria (+14.6% vs +0.4%, p=0.028), B. adolescentis (+1.1% vs 0.0% p=0.006) and Roseburia spp. (+1.5% vs -0.1% p=0.004). Intestinal permeability decreased significantly in patients after oligofructose/inulin to a level that was similar to siblings. Blood T cell abundance reduced in siblings but not patients following oligofructose/inulin.ConclusionsOligofructose/inulin supplementation did not significantly impact calprotectin, but theprebiotic effect was more marked in healthy siblings compared with patients with inactive CD and was associated with alterations in other CD risk markers. Future research should focus on dietary intervention, including with prebiotics, in the primary prevention of CD.

KW - Prebiotics

KW - Crohn’s disease

KW - microbiota

KW - Pre-disease

KW - first-degree relative

KW - prevention

UR - https://www.scopus.com/pages/publications/85111883698

U2 - 10.1016/j.clnu.2021.05.033

DO - 10.1016/j.clnu.2021.05.033

M3 - Article

C2 - 34364241

AN - SCOPUS:85111883698

SN - 0261-5614

VL - 40

SP - 5009

EP - 5019

JO - Clinical Nutrition

JF - Clinical Nutrition

IS - 8

ER -

Prebiotic fructans have greater impact on luminal microbiology and CD3+ T cells in healthy siblings than patients with Crohn’s disease: a pilot study investigating the potential for primary prevention of inflammatory bowel disease

Abstract

Bibliographical note

Funding

UN SDGs

Keywords

Access to Document

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Cite this