Gut microbiome shifts in adolescents after sleeve gastrectomy with increased oral-associated taxa and pro-inflammatory potential

Cynthia O. Akagbosu
Kathryn E Mccauley
Sivaranjani Namasivayam
Hector N Romero-Soto
Wade O'Brien
Mickayla Bacorn
Eric Bohrnsen
Benjamin Schwarz
Shreni Mistry
Andrew S. Burns
P. Juliana Perez-Chaparro
Qing Chen
Phoebe Lapoint
Anal Patel
Lauren E. Krausfeldt
Poorani Subramanian
Brian A Sellers
Foo Cheung
Richard Apps
Iyadh Douagi
Shira Levy
Evan P. Nadler
Suchitra K. Hourigan
Publication typePosted Content
Publication date2024-09-16
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Abstract
ABSTRACT
Background

Bariatric surgery is highly effective in achieving weight loss in children and adolescents with severe obesity, however the underlying mechanisms are incompletely understood, and gut microbiome changes are unknown.

Objectives

1) To comprehensively examine gut microbiome and metabolome changes after laparoscopic vertical sleeve gastrectomy (VSG) in adolescents and 2) to assess whether the microbiome/metabolome changes observed with VSG influence phenotype using germ-free murine models.

Design

1) A longitudinal observational study in adolescents undergoing VSG with serial stool samples undergoing shotgun metagenomic microbiome sequencing and metabolomics (polar metabolites, bile acids and short chain fatty acids) and 2) a human-to-mouse fecal transplant study.

Results

We show adolescents exhibit significant gut microbiome and metabolome shifts several months after VSG, with increased alpha diversity and notably with enrichment of oral-associated taxa. To assess causality of the microbiome/metabolome changes in phenotype, pre-VSG and post-VSG stool was transplanted into germ-free mice. Post-VSG stool was not associated with any beneficial outcomes such as adiposity reduction compared pre-VSG stool. However, post-VSG stool exhibited an inflammatory phenotype with increased intestinal Th17 and decreased regulatory T cells. Concomitantly, we found elevated fecal calprotectin and an enrichment of proinflammatory pathways in a subset of adolescents post-VSG.

Conclusion

We show that in some adolescents, microbiome changes post-VSG may have inflammatory potential, which may be of importance considering the increased incidence of inflammatory bowel disease post-VSG.

What is already known on this topic

Bariatric surgery is highly effective in achieving weight loss in children and adolescents with severe obesity, however the underlying mechanisms are incompletely understood, and gut microbiome changes are unknown.

What this study adds

Significant gut microbiome and metabolome shifts were found several months after vertical sleeve gastrectomy in adolescents, notably with enrichment of oral-associated taxa. Using human to germ-free mice fecal transplant studies, the post-surgery changes in the gut microbiome/metabolome were shown to have inflammatory potential. Furthermore, raised fecal calprotectin and inflammatory systemic pathways were seen in a subset of adolescents post-surgery.

How this study might affect research, practice or policy

These findings may be of importance given the growing recognition of an increased incidence of inflammatory bowel disease after bariatric surgery and warrants further investigation.

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GOST Copy
Akagbosu C. O. et al. Gut microbiome shifts in adolescents after sleeve gastrectomy with increased oral-associated taxa and pro-inflammatory potential // medRxiv : the preprint server for health sciences. 2024.
GOST all authors (up to 50) Copy
Akagbosu C. O., Mccauley K. E., Namasivayam S., Romero-Soto H. N., O'Brien W., Bacorn M., Bohrnsen E., Schwarz B., Mistry S., Burns A. S., Perez-Chaparro P. J., Chen Q., Lapoint P., Patel A., Krausfeldt L. E., Subramanian P., Sellers B. A., Cheung F., Apps R., Douagi I., Levy S., Nadler E. P., Hourigan S. K. Gut microbiome shifts in adolescents after sleeve gastrectomy with increased oral-associated taxa and pro-inflammatory potential // medRxiv : the preprint server for health sciences. 2024.
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RIS Copy
TY - GENERIC
DO - 10.1101/2024.09.16.24313738
UR - http://medrxiv.org/lookup/doi/10.1101/2024.09.16.24313738
TI - Gut microbiome shifts in adolescents after sleeve gastrectomy with increased oral-associated taxa and pro-inflammatory potential
T2 - medRxiv : the preprint server for health sciences
AU - Akagbosu, Cynthia O.
AU - Mccauley, Kathryn E
AU - Namasivayam, Sivaranjani
AU - Romero-Soto, Hector N
AU - O'Brien, Wade
AU - Bacorn, Mickayla
AU - Bohrnsen, Eric
AU - Schwarz, Benjamin
AU - Mistry, Shreni
AU - Burns, Andrew S.
AU - Perez-Chaparro, P. Juliana
AU - Chen, Qing
AU - Lapoint, Phoebe
AU - Patel, Anal
AU - Krausfeldt, Lauren E.
AU - Subramanian, Poorani
AU - Sellers, Brian A
AU - Cheung, Foo
AU - Apps, Richard
AU - Douagi, Iyadh
AU - Levy, Shira
AU - Nadler, Evan P.
AU - Hourigan, Suchitra K.
PY - 2024
DA - 2024/09/16
PB - Cold Spring Harbor Laboratory
PMID - 39371172
ER -
BibTex
Cite this
BibTex (up to 50 authors) Copy
@article{2024_Akagbosu,
author = {Cynthia O. Akagbosu and Kathryn E Mccauley and Sivaranjani Namasivayam and Hector N Romero-Soto and Wade O'Brien and Mickayla Bacorn and Eric Bohrnsen and Benjamin Schwarz and Shreni Mistry and Andrew S. Burns and P. Juliana Perez-Chaparro and Qing Chen and Phoebe Lapoint and Anal Patel and Lauren E. Krausfeldt and Poorani Subramanian and Brian A Sellers and Foo Cheung and Richard Apps and Iyadh Douagi and Shira Levy and Evan P. Nadler and Suchitra K. Hourigan},
title = {Gut microbiome shifts in adolescents after sleeve gastrectomy with increased oral-associated taxa and pro-inflammatory potential},
journal = {medRxiv : the preprint server for health sciences},
year = {2024},
publisher = {Cold Spring Harbor Laboratory},
month = {sep},
url = {http://medrxiv.org/lookup/doi/10.1101/2024.09.16.24313738},
doi = {10.1101/2024.09.16.24313738}
}