Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial

Omer Kamer; Ehud Rinott; Gal Tsaban; Alon Kaplan; Anat Yaskolka Meir; Hila Zelicha; Dan Knights; Kieran Tuohy; Francesca Fava; Matthias Uwe Scholz; Oren Ziv; Elad Rubin; Matthias Blüher; Michael Stumvoll; Uta Ceglarek; Karine Clément; Omry Koren; Frank B. Hu; Meir J. Stampfer; Dong D. Wang; Ilan Youngster; Iris Shai

doi:10.1080/19490976.2023.2264457

Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial

Omer Kamer, Ehud Rinott, Gal Tsaban, Alon Kaplan, Anat Yaskolka Meir, Hila Zelicha, Dan Knights, Kieran Tuohy, Francesca Fava, Matthias Uwe Scholz, Oren Ziv, Elad Rubin, Matthias Blüher, Michael Stumvoll, Uta Ceglarek, Karine Clément, Omry Koren, Frank B. Hu, Meir J. Stampfer, Dong D. WangIlan Youngster, Iris Shai

Bar-Ilan University - Azrieli Faculty of Medicine

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

7 Scopus citations

Abstract

We previously reported that autologous-fecal-microbiota-transplantation (aFMT), following 6 m of lifestyle intervention, attenuated subsequent weight regain and insulin rebound for participants consuming a high-polyphenol green-Mediterranean diet. Here, we explored whether specific changes in the core (abundant) vs. non-core (low-abundance) gut microbiome taxa fractions during the weight-loss phase (0–6 m) were differentially associated with weight maintenance following aFMT. Eighty-two abdominally obese/dyslipidemic participants (age = 52 years; 6 m weightloss = −8.3 kg) who provided fecal samples (0 m, 6 m) were included. Frozen 6 m’s fecal samples were processed into 1 g, opaque and odorless aFMT capsules. Participants were randomly assigned to receive 100 capsules containing their own fecal microbiota or placebo over 8 m-14 m in ten administrations (adherence rate > 90%). Gut microbiome composition was evaluated using shotgun metagenomic sequencing. Non-core taxa were defined as ≤ 66% prevalence across participants. Overall, 450 species were analyzed. At baseline, 13.3% were classified as core, and Firmicutes presented the highest core proportion by phylum. During 6 m weight-loss phase, abundance of non-core species changed more than core species (P <.0001). Subject-specific changes in core and non-core taxa fractions were strongly correlated (Jaccard Index; r = 0.54; P <.001). Following aFMT treatment, only participants with a low 6 m change in core taxa, and a high change in non-core taxa, avoided 8–14 m weight regain (aFMT = −0.58 ± 2.4 kg, corresponding placebo group = 3.18 ± 3.5 kg; P =.02). In a linear regression model, low core/high non-core 6 m change was the only combination that was significantly associated with attenuated 8–14 m weight regain (P =.038; P =.002 for taxa patterns/treatment intervention interaction). High change in non-core, low-abundance taxa during weight-loss might mediate aFMT treatment success for weight loss maintenance. ClinicalTrials.gov: NCT03020186.

Original language	English
Article number	2264457
Journal	Gut Microbes
Volume	15
Issue number	2
DOIs	https://doi.org/10.1080/19490976.2023.2264457
State	Published - Dec 2023

Bibliographical note

Publisher Copyright:
© 2023 The Author(s). Published with license by Taylor & Francis Group, LLC.

Funding

This work was supported by the Israeli Science Foundation (grant 1733/18), Israel Ministry of Health (grant no. 87472511), Israel Ministry of Science and Technology (grant 3-13604); Deutsche Forschungsgemeinschaft (DFG, German Research Foundation), Projektnummer 209933838–SFB 1052: “Obesity Mechanisms”; the Rosetrees trust (grant A2623); the Project Cabala_diet&health (http://www.cabalaproject.eu/; ERA-Net Cofund ERA-HDHL N696295), the California Walnuts Commission, and National Institutes of Health ((R01NR019992 and R00DK119412). None of the funders were involved in any stage of the design, conduct, or analysis of the study, and had no access to the study results before publication We thank Prof. Assaf Rudich for his review of the manuscript of this work.

Funders	Funder number
National Institutes of Health	R01NR019992, R00DK119412
California Walnut Commission
Rosetrees Trust	A2623, ERA-HDHL N696295
Deutsche Forschungsgemeinschaft	209933838–SFB 1052
Israel Science Foundation	1733/18
Ministry of science and technology, Israel	3-13604
Ministry of Health, State of Israel	87472511

Keywords

FMT
Low-abundance taxa
aFMT
core microbiome
lifestyle intervention
weight regain

UN SDGs

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

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10.1080/19490976.2023.2264457

Cite this

Kamer, O., Rinott, E., Tsaban, G., Kaplan, A., Yaskolka Meir, A., Zelicha, H., Knights, D., Tuohy, K., Fava, F., Uwe Scholz, M., Ziv, O., Rubin, E., Blüher, M., Stumvoll, M., Ceglarek, U., Clément, K., Koren, O., Hu, F. B., Stampfer, M. J., ... Shai, I. (2023). Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial. Gut Microbes, 15(2), Article 2264457. https://doi.org/10.1080/19490976.2023.2264457

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abstract = "We previously reported that autologous-fecal-microbiota-transplantation (aFMT), following 6 m of lifestyle intervention, attenuated subsequent weight regain and insulin rebound for participants consuming a high-polyphenol green-Mediterranean diet. Here, we explored whether specific changes in the core (abundant) vs. non-core (low-abundance) gut microbiome taxa fractions during the weight-loss phase (0–6 m) were differentially associated with weight maintenance following aFMT. Eighty-two abdominally obese/dyslipidemic participants (age = 52 years; 6 m weightloss = −8.3 kg) who provided fecal samples (0 m, 6 m) were included. Frozen 6 m{\textquoteright}s fecal samples were processed into 1 g, opaque and odorless aFMT capsules. Participants were randomly assigned to receive 100 capsules containing their own fecal microbiota or placebo over 8 m-14 m in ten administrations (adherence rate > 90%). Gut microbiome composition was evaluated using shotgun metagenomic sequencing. Non-core taxa were defined as ≤ 66% prevalence across participants. Overall, 450 species were analyzed. At baseline, 13.3% were classified as core, and Firmicutes presented the highest core proportion by phylum. During 6 m weight-loss phase, abundance of non-core species changed more than core species (P <.0001). Subject-specific changes in core and non-core taxa fractions were strongly correlated (Jaccard Index; r = 0.54; P <.001). Following aFMT treatment, only participants with a low 6 m change in core taxa, and a high change in non-core taxa, avoided 8–14 m weight regain (aFMT = −0.58 ± 2.4 kg, corresponding placebo group = 3.18 ± 3.5 kg; P =.02). In a linear regression model, low core/high non-core 6 m change was the only combination that was significantly associated with attenuated 8–14 m weight regain (P =.038; P =.002 for taxa patterns/treatment intervention interaction). High change in non-core, low-abundance taxa during weight-loss might mediate aFMT treatment success for weight loss maintenance. ClinicalTrials.gov: NCT03020186.",

keywords = "FMT, Low-abundance taxa, aFMT, core microbiome, lifestyle intervention, weight regain",

author = "Omer Kamer and Ehud Rinott and Gal Tsaban and Alon Kaplan and {Yaskolka Meir}, Anat and Hila Zelicha and Dan Knights and Kieran Tuohy and Francesca Fava and {Uwe Scholz}, Matthias and Oren Ziv and Elad Rubin and Matthias Bl{\"u}her and Michael Stumvoll and Uta Ceglarek and Karine Cl{\'e}ment and Omry Koren and Hu, {Frank B.} and Stampfer, {Meir J.} and Wang, {Dong D.} and Ilan Youngster and Iris Shai",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s). Published with license by Taylor & Francis Group, LLC.",

year = "2023",

month = dec,

doi = "10.1080/19490976.2023.2264457",

language = "אנגלית",

volume = "15",

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Kamer, O, Rinott, E, Tsaban, G, Kaplan, A, Yaskolka Meir, A, Zelicha, H, Knights, D, Tuohy, K, Fava, F, Uwe Scholz, M, Ziv, O, Rubin, E, Blüher, M, Stumvoll, M, Ceglarek, U, Clément, K, Koren, O, Hu, FB, Stampfer, MJ, Wang, DD, Youngster, I & Shai, I 2023, 'Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial', Gut Microbes, vol. 15, no. 2, 2264457. https://doi.org/10.1080/19490976.2023.2264457

TY - JOUR

T1 - Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial

AU - Kamer, Omer

AU - Rinott, Ehud

AU - Tsaban, Gal

AU - Kaplan, Alon

AU - Yaskolka Meir, Anat

AU - Zelicha, Hila

AU - Knights, Dan

AU - Tuohy, Kieran

AU - Fava, Francesca

AU - Uwe Scholz, Matthias

AU - Ziv, Oren

AU - Rubin, Elad

AU - Blüher, Matthias

AU - Stumvoll, Michael

AU - Ceglarek, Uta

AU - Clément, Karine

AU - Koren, Omry

AU - Hu, Frank B.

AU - Stampfer, Meir J.

AU - Wang, Dong D.

AU - Youngster, Ilan

AU - Shai, Iris

PY - 2023/12

Y1 - 2023/12

N2 - We previously reported that autologous-fecal-microbiota-transplantation (aFMT), following 6 m of lifestyle intervention, attenuated subsequent weight regain and insulin rebound for participants consuming a high-polyphenol green-Mediterranean diet. Here, we explored whether specific changes in the core (abundant) vs. non-core (low-abundance) gut microbiome taxa fractions during the weight-loss phase (0–6 m) were differentially associated with weight maintenance following aFMT. Eighty-two abdominally obese/dyslipidemic participants (age = 52 years; 6 m weightloss = −8.3 kg) who provided fecal samples (0 m, 6 m) were included. Frozen 6 m’s fecal samples were processed into 1 g, opaque and odorless aFMT capsules. Participants were randomly assigned to receive 100 capsules containing their own fecal microbiota or placebo over 8 m-14 m in ten administrations (adherence rate > 90%). Gut microbiome composition was evaluated using shotgun metagenomic sequencing. Non-core taxa were defined as ≤ 66% prevalence across participants. Overall, 450 species were analyzed. At baseline, 13.3% were classified as core, and Firmicutes presented the highest core proportion by phylum. During 6 m weight-loss phase, abundance of non-core species changed more than core species (P <.0001). Subject-specific changes in core and non-core taxa fractions were strongly correlated (Jaccard Index; r = 0.54; P <.001). Following aFMT treatment, only participants with a low 6 m change in core taxa, and a high change in non-core taxa, avoided 8–14 m weight regain (aFMT = −0.58 ± 2.4 kg, corresponding placebo group = 3.18 ± 3.5 kg; P =.02). In a linear regression model, low core/high non-core 6 m change was the only combination that was significantly associated with attenuated 8–14 m weight regain (P =.038; P =.002 for taxa patterns/treatment intervention interaction). High change in non-core, low-abundance taxa during weight-loss might mediate aFMT treatment success for weight loss maintenance. ClinicalTrials.gov: NCT03020186.

AB - We previously reported that autologous-fecal-microbiota-transplantation (aFMT), following 6 m of lifestyle intervention, attenuated subsequent weight regain and insulin rebound for participants consuming a high-polyphenol green-Mediterranean diet. Here, we explored whether specific changes in the core (abundant) vs. non-core (low-abundance) gut microbiome taxa fractions during the weight-loss phase (0–6 m) were differentially associated with weight maintenance following aFMT. Eighty-two abdominally obese/dyslipidemic participants (age = 52 years; 6 m weightloss = −8.3 kg) who provided fecal samples (0 m, 6 m) were included. Frozen 6 m’s fecal samples were processed into 1 g, opaque and odorless aFMT capsules. Participants were randomly assigned to receive 100 capsules containing their own fecal microbiota or placebo over 8 m-14 m in ten administrations (adherence rate > 90%). Gut microbiome composition was evaluated using shotgun metagenomic sequencing. Non-core taxa were defined as ≤ 66% prevalence across participants. Overall, 450 species were analyzed. At baseline, 13.3% were classified as core, and Firmicutes presented the highest core proportion by phylum. During 6 m weight-loss phase, abundance of non-core species changed more than core species (P <.0001). Subject-specific changes in core and non-core taxa fractions were strongly correlated (Jaccard Index; r = 0.54; P <.001). Following aFMT treatment, only participants with a low 6 m change in core taxa, and a high change in non-core taxa, avoided 8–14 m weight regain (aFMT = −0.58 ± 2.4 kg, corresponding placebo group = 3.18 ± 3.5 kg; P =.02). In a linear regression model, low core/high non-core 6 m change was the only combination that was significantly associated with attenuated 8–14 m weight regain (P =.038; P =.002 for taxa patterns/treatment intervention interaction). High change in non-core, low-abundance taxa during weight-loss might mediate aFMT treatment success for weight loss maintenance. ClinicalTrials.gov: NCT03020186.

KW - FMT

KW - Low-abundance taxa

KW - aFMT

KW - core microbiome

KW - lifestyle intervention

KW - weight regain

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Successful weight regain attenuation by autologous fecal microbiota transplantation is associated with non-core gut microbiota changes during weight loss; randomized controlled trial

Abstract

Bibliographical note

Funding

Keywords

UN SDGs

Access to Document

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