Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability

Background: Metabolic Syndrome (MetS) is a clinical diagnosis where patients exhibit three out of the five risk factors: hypertriglyceridemia, low high-density lipoprotein (HDL) cholesterol, hyperglycemia, elevated blood pressure, or increased abdominal obesity. MetS arises due to dysregulated metab...

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Main Authors: Mia J. Coleman, Luis M. Espino, Hernan Lebensohn, Marija V. Zimkute, Negar Yaghooti, Christina L. Ling, Jessica M. Gross, Natalia Listwan, Sandra Cano, Vanessa Garcia, Debbie M. Lovato, Susan L. Tigert, Drew R. Jones, Rama R. Gullapalli, Neal E. Rakov, Euriko G. Torrazza Perez, Eliseo F. Castillo
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/12/5/431
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author Mia J. Coleman
Luis M. Espino
Hernan Lebensohn
Marija V. Zimkute
Negar Yaghooti
Christina L. Ling
Jessica M. Gross
Natalia Listwan
Sandra Cano
Vanessa Garcia
Debbie M. Lovato
Susan L. Tigert
Drew R. Jones
Rama R. Gullapalli
Neal E. Rakov
Euriko G. Torrazza Perez
Eliseo F. Castillo
author_facet Mia J. Coleman
Luis M. Espino
Hernan Lebensohn
Marija V. Zimkute
Negar Yaghooti
Christina L. Ling
Jessica M. Gross
Natalia Listwan
Sandra Cano
Vanessa Garcia
Debbie M. Lovato
Susan L. Tigert
Drew R. Jones
Rama R. Gullapalli
Neal E. Rakov
Euriko G. Torrazza Perez
Eliseo F. Castillo
author_sort Mia J. Coleman
collection DOAJ
description Background: Metabolic Syndrome (MetS) is a clinical diagnosis where patients exhibit three out of the five risk factors: hypertriglyceridemia, low high-density lipoprotein (HDL) cholesterol, hyperglycemia, elevated blood pressure, or increased abdominal obesity. MetS arises due to dysregulated metabolic pathways that culminate with insulin resistance and put individuals at risk to develop various comorbidities with far-reaching medical consequences such as non-alcoholic fatty liver disease (NAFLD) and cardiovascular disease. As it stands, the exact pathogenesis of MetS as well as the involvement of the gastrointestinal tract in MetS is not fully understood. Our study aimed to evaluate intestinal health in human subjects with MetS. Methods: We examined MetS risk factors in individuals through body measurements and clinical and biochemical blood analysis. To evaluate intestinal health, gut inflammation was measured by fecal calprotectin, intestinal permeability through the lactulose-mannitol test, and utilized fecal metabolomics to examine alterations in the host–microbiota gut metabolism. Results: No signs of intestinal inflammation or increased intestinal permeability were observed in the MetS group compared to our control group. However, we found a significant increase in 417 lipid features of the gut lipidome in our MetS cohort. An identified fecal lipid, diacyl-glycerophosphocholine, showed a strong correlation with several MetS risk factors. Although our MetS cohort showed no signs of intestinal inflammation, they presented with increased levels of serum TNFα that also correlated with increasing triglyceride and fecal diacyl-glycerophosphocholine levels and decreasing HDL cholesterol levels. Conclusion: Taken together, our main results show that MetS subjects showed major alterations in fecal lipid profiles suggesting alterations in the intestinal host–microbiota metabolism that may arise before concrete signs of gut inflammation or intestinal permeability become apparent. Lastly, we posit that fecal metabolomics could serve as a non-invasive, accurate screening method for both MetS and NAFLD.
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spelling doaj.art-a048b348431a4d2e81e28cdc42acbb6f2023-11-23T12:07:24ZengMDPI AGMetabolites2218-19892022-05-0112543110.3390/metabo12050431Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal PermeabilityMia J. Coleman0Luis M. Espino1Hernan Lebensohn2Marija V. Zimkute3Negar Yaghooti4Christina L. Ling5Jessica M. Gross6Natalia Listwan7Sandra Cano8Vanessa Garcia9Debbie M. Lovato10Susan L. Tigert11Drew R. Jones12Rama R. Gullapalli13Neal E. Rakov14Euriko G. Torrazza Perez15Eliseo F. Castillo16University of New Mexico School of Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAUniversity of New Mexico School of Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAUniversity of New Mexico School of Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USADivision of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USADivision of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAMetabolomics Core Resource Laboratory, New York University Langone Health, New York, NY 10016, USADepartment of Pathology, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USADivision of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USADivision of Gastroenterology and Hepatology, Department of Internal Medicine, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USAClinical and Translational Science Center, University of New Mexico Health Sciences Center, Albuquerque, NM 87131, USABackground: Metabolic Syndrome (MetS) is a clinical diagnosis where patients exhibit three out of the five risk factors: hypertriglyceridemia, low high-density lipoprotein (HDL) cholesterol, hyperglycemia, elevated blood pressure, or increased abdominal obesity. MetS arises due to dysregulated metabolic pathways that culminate with insulin resistance and put individuals at risk to develop various comorbidities with far-reaching medical consequences such as non-alcoholic fatty liver disease (NAFLD) and cardiovascular disease. As it stands, the exact pathogenesis of MetS as well as the involvement of the gastrointestinal tract in MetS is not fully understood. Our study aimed to evaluate intestinal health in human subjects with MetS. Methods: We examined MetS risk factors in individuals through body measurements and clinical and biochemical blood analysis. To evaluate intestinal health, gut inflammation was measured by fecal calprotectin, intestinal permeability through the lactulose-mannitol test, and utilized fecal metabolomics to examine alterations in the host–microbiota gut metabolism. Results: No signs of intestinal inflammation or increased intestinal permeability were observed in the MetS group compared to our control group. However, we found a significant increase in 417 lipid features of the gut lipidome in our MetS cohort. An identified fecal lipid, diacyl-glycerophosphocholine, showed a strong correlation with several MetS risk factors. Although our MetS cohort showed no signs of intestinal inflammation, they presented with increased levels of serum TNFα that also correlated with increasing triglyceride and fecal diacyl-glycerophosphocholine levels and decreasing HDL cholesterol levels. Conclusion: Taken together, our main results show that MetS subjects showed major alterations in fecal lipid profiles suggesting alterations in the intestinal host–microbiota metabolism that may arise before concrete signs of gut inflammation or intestinal permeability become apparent. Lastly, we posit that fecal metabolomics could serve as a non-invasive, accurate screening method for both MetS and NAFLD.https://www.mdpi.com/2218-1989/12/5/431metabolic syndromemetabolomicslipidomicsdyslipidemia
spellingShingle Mia J. Coleman
Luis M. Espino
Hernan Lebensohn
Marija V. Zimkute
Negar Yaghooti
Christina L. Ling
Jessica M. Gross
Natalia Listwan
Sandra Cano
Vanessa Garcia
Debbie M. Lovato
Susan L. Tigert
Drew R. Jones
Rama R. Gullapalli
Neal E. Rakov
Euriko G. Torrazza Perez
Eliseo F. Castillo
Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
Metabolites
metabolic syndrome
metabolomics
lipidomics
dyslipidemia
title Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
title_full Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
title_fullStr Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
title_full_unstemmed Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
title_short Individuals with Metabolic Syndrome Show Altered Fecal Lipidomic Profiles with No Signs of Intestinal Inflammation or Increased Intestinal Permeability
title_sort individuals with metabolic syndrome show altered fecal lipidomic profiles with no signs of intestinal inflammation or increased intestinal permeability
topic metabolic syndrome
metabolomics
lipidomics
dyslipidemia
url https://www.mdpi.com/2218-1989/12/5/431
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