Microbiota in anorexia nervosa: The triangle between bacterial species, metabolites and psychological tests

Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. I...

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Published inPloS one Vol. 12; no. 6; p. e0179739
Main Authors Borgo, Francesca, Riva, Alessandra, Benetti, Alberto, Casiraghi, Maria Cristina, Bertelli, Sara, Garbossa, Stefania, Anselmetti, Simona, Scarone, Silvio, Pontiroli, Antonio E., Morace, Giulia, Borghi, Elisa
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 21.06.2017
Public Library of Science (PLoS)
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Abstract Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. In this study we performed a comprehensive analysis integrating data on gut microbiota with clinical, anthropometric and psychological traits to gain new insight in the pathophysiology of AN. Fifteen AN women were compared with fifteen age-, sex- and ethnicity-matched healthy controls. AN diet was characterized by a significant lower energy intake, but macronutrient analysis highlighted a restriction only in fats and carbohydrates consumption. Next generation sequencing showed that AN intestinal microbiota was significantly affected at every taxonomic level, showing a significant increase of Enterobacteriaceae, and of the archeon Methanobrevibacter smithii compared with healthy controls. On the contrary, the genera Roseburia, Ruminococcus and Clostridium, were depleted, in line with the observed reduction in AN of total short chain fatty acids, butyrate, and propionate. Butyrate concentrations inversely correlated with anxiety levels, whereas propionate directly correlated with insulin levels and with the relative abundance of Roseburia inulinivorans, a known propionate producer. BMI represented the best predictive value for gut dysbiosis and metabolic alterations, showing a negative correlation with Bacteroides uniformis (microbiota), with alanine aminotransferase (liver function), and with psychopathological scores (obsession-compulsion, anxiety, and depression), and a positive correlation with white blood cells count. In conclusion, our findings corroborate the hypothesis that the gut dysbiosis could take part in the AN neurobiology, in particular in sustaining the persistence of alterations that eventually result in relapses after renourishment and psychological therapy, but causality still needs to be proven.
AbstractList Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. In this study we performed a comprehensive analysis integrating data on gut microbiota with clinical, anthropometric and psychological traits to gain new insight in the pathophysiology of AN. Fifteen AN women were compared with fifteen age-, sex- and ethnicity-matched healthy controls. AN diet was characterized by a significant lower energy intake, but macronutrient analysis highlighted a restriction only in fats and carbohydrates consumption. Next generation sequencing showed that AN intestinal microbiota was significantly affected at every taxonomic level, showing a significant increase of Enterobacteriaceae , and of the archeon Methanobrevibacter smithii compared with healthy controls. On the contrary, the genera Roseburia , Ruminococcus and Clostridium , were depleted, in line with the observed reduction in AN of total short chain fatty acids, butyrate, and propionate. Butyrate concentrations inversely correlated with anxiety levels, whereas propionate directly correlated with insulin levels and with the relative abundance of Roseburia inulinivorans , a known propionate producer. BMI represented the best predictive value for gut dysbiosis and metabolic alterations, showing a negative correlation with Bacteroides uniformis (microbiota), with alanine aminotransferase (liver function), and with psychopathological scores (obsession-compulsion, anxiety, and depression), and a positive correlation with white blood cells count. In conclusion, our findings corroborate the hypothesis that the gut dysbiosis could take part in the AN neurobiology, in particular in sustaining the persistence of alterations that eventually result in relapses after renourishment and psychological therapy, but causality still needs to be proven.
Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. In this study we performed a comprehensive analysis integrating data on gut microbiota with clinical, anthropometric and psychological traits to gain new insight in the pathophysiology of AN. Fifteen AN women were compared with fifteen age-, sex- and ethnicity-matched healthy controls. AN diet was characterized by a significant lower energy intake, but macronutrient analysis highlighted a restriction only in fats and carbohydrates consumption. Next generation sequencing showed that AN intestinal microbiota was significantly affected at every taxonomic level, showing a significant increase of Enterobacteriaceae , and of the archeon Methanobrevibacter smithii compared with healthy controls. On the contrary, the genera Roseburia , Ruminococcus and Clostridium , were depleted, in line with the observed reduction in AN of total short chain fatty acids, butyrate, and propionate. Butyrate concentrations inversely correlated with anxiety levels, whereas propionate directly correlated with insulin levels and with the relative abundance of Roseburia inulinivorans , a known propionate producer. BMI represented the best predictive value for gut dysbiosis and metabolic alterations, showing a negative correlation with Bacteroides uniformis (microbiota), with alanine aminotransferase (liver function), and with psychopathological scores (obsession-compulsion, anxiety, and depression), and a positive correlation with white blood cells count. In conclusion, our findings corroborate the hypothesis that the gut dysbiosis could take part in the AN neurobiology, in particular in sustaining the persistence of alterations that eventually result in relapses after renourishment and psychological therapy, but causality still needs to be proven.
Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. In this study we performed a comprehensive analysis integrating data on gut microbiota with clinical, anthropometric and psychological traits to gain new insight in the pathophysiology of AN. Fifteen AN women were compared with fifteen age-, sex- and ethnicity-matched healthy controls. AN diet was characterized by a significant lower energy intake, but macronutrient analysis highlighted a restriction only in fats and carbohydrates consumption. Next generation sequencing showed that AN intestinal microbiota was significantly affected at every taxonomic level, showing a significant increase of Enterobacteriaceae, and of the archeon Methanobrevibacter smithii compared with healthy controls. On the contrary, the genera Roseburia, Ruminococcus and Clostridium, were depleted, in line with the observed reduction in AN of total short chain fatty acids, butyrate, and propionate. Butyrate concentrations inversely correlated with anxiety levels, whereas propionate directly correlated with insulin levels and with the relative abundance of Roseburia inulinivorans, a known propionate producer. BMI represented the best predictive value for gut dysbiosis and metabolic alterations, showing a negative correlation with Bacteroides uniformis (microbiota), with alanine aminotransferase (liver function), and with psychopathological scores (obsession-compulsion, anxiety, and depression), and a positive correlation with white blood cells count. In conclusion, our findings corroborate the hypothesis that the gut dysbiosis could take part in the AN neurobiology, in particular in sustaining the persistence of alterations that eventually result in relapses after renourishment and psychological therapy, but causality still needs to be proven.Anorexia nervosa (AN) is a psychiatric disease with devastating physical consequences, with a pathophysiological mechanism still to be elucidated. Metagenomic studies on anorexia nervosa have revealed profound gut microbiome perturbations as a possible environmental factor involved in the disease. In this study we performed a comprehensive analysis integrating data on gut microbiota with clinical, anthropometric and psychological traits to gain new insight in the pathophysiology of AN. Fifteen AN women were compared with fifteen age-, sex- and ethnicity-matched healthy controls. AN diet was characterized by a significant lower energy intake, but macronutrient analysis highlighted a restriction only in fats and carbohydrates consumption. Next generation sequencing showed that AN intestinal microbiota was significantly affected at every taxonomic level, showing a significant increase of Enterobacteriaceae, and of the archeon Methanobrevibacter smithii compared with healthy controls. On the contrary, the genera Roseburia, Ruminococcus and Clostridium, were depleted, in line with the observed reduction in AN of total short chain fatty acids, butyrate, and propionate. Butyrate concentrations inversely correlated with anxiety levels, whereas propionate directly correlated with insulin levels and with the relative abundance of Roseburia inulinivorans, a known propionate producer. BMI represented the best predictive value for gut dysbiosis and metabolic alterations, showing a negative correlation with Bacteroides uniformis (microbiota), with alanine aminotransferase (liver function), and with psychopathological scores (obsession-compulsion, anxiety, and depression), and a positive correlation with white blood cells count. In conclusion, our findings corroborate the hypothesis that the gut dysbiosis could take part in the AN neurobiology, in particular in sustaining the persistence of alterations that eventually result in relapses after renourishment and psychological therapy, but causality still needs to be proven.
Audience Academic
Author Garbossa, Stefania
Anselmetti, Simona
Riva, Alessandra
Scarone, Silvio
Borgo, Francesca
Morace, Giulia
Benetti, Alberto
Bertelli, Sara
Pontiroli, Antonio E.
Borghi, Elisa
Casiraghi, Maria Cristina
AuthorAffiliation 1 Department of Health Sciences, Università degli Studi di Milano, Milan, Italy
3 Department of Food, Environmental and Nutritional Sciences, Università degli Studi di Milano, Milan, Italy
Instituto de Agroquimica y Tecnologia de Alimentos, SPAIN
2 ASST Santi Paolo e Carlo, Milan, Italy
AuthorAffiliation_xml – name: 3 Department of Food, Environmental and Nutritional Sciences, Università degli Studi di Milano, Milan, Italy
– name: Instituto de Agroquimica y Tecnologia de Alimentos, SPAIN
– name: 2 ASST Santi Paolo e Carlo, Milan, Italy
– name: 1 Department of Health Sciences, Università degli Studi di Milano, Milan, Italy
Author_xml – sequence: 1
  givenname: Francesca
  surname: Borgo
  fullname: Borgo, Francesca
– sequence: 2
  givenname: Alessandra
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  fullname: Riva, Alessandra
– sequence: 3
  givenname: Alberto
  surname: Benetti
  fullname: Benetti, Alberto
– sequence: 4
  givenname: Maria Cristina
  surname: Casiraghi
  fullname: Casiraghi, Maria Cristina
– sequence: 5
  givenname: Sara
  surname: Bertelli
  fullname: Bertelli, Sara
– sequence: 6
  givenname: Stefania
  surname: Garbossa
  fullname: Garbossa, Stefania
– sequence: 7
  givenname: Simona
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– sequence: 8
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  surname: Scarone
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– sequence: 9
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– sequence: 10
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– sequence: 11
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  orcidid: 0000-0002-1893-0455
  surname: Borghi
  fullname: Borghi, Elisa
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28636668$$D View this record in MEDLINE/PubMed
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2017 Borgo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2017 Borgo et al 2017 Borgo et al
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Borgo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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SubjectTerms Abundance
Alanine
Alanine transaminase
Alanine Transaminase - blood
Anorexia
Anorexia nervosa
Anorexia Nervosa - microbiology
Anorexia Nervosa - psychology
Anthropometry
Anxiety
Anxiety Disorders - diagnosis
Aspartate Aminotransferases - blood
Bacteria
Biology and Life Sciences
Blood cells
Body mass
Body Mass Index
Bulimia
Butyrates - metabolism
Carbohydrates
Case-Control Studies
Clostridium - genetics
Clostridium - isolation & purification
Comparative analysis
Consumption
Correlation
Correlation analysis
Data processing
Depressive Disorder - diagnosis
Development and progression
Diet
Digestive tract
DNA, Bacterial - chemistry
DNA, Bacterial - isolation & purification
DNA, Bacterial - metabolism
Dysbiosis - microbiology
Eating disorders
Energy intake
Environmental factors
Fats
Fatty acids
Fatty Acids, Volatile - blood
Feces - microbiology
Gastrointestinal tract
Gastrointestinal Tract - microbiology
Genera
Humans
Insulin
Intestinal microflora
Intestine
Leukocytes
Liver
Medicine and Health Sciences
Mental depression
Metabolites
Microbiota
Microbiota (Symbiotic organisms)
Minority & ethnic groups
Nervous system
Physical Sciences
Physiological aspects
Propionates - metabolism
Propionic acid
Psychological aspects
Psychological assessment
Psychological Tests
Relative abundance
Risk factors
Ruminococcus - genetics
Ruminococcus - isolation & purification
Sequence Analysis, DNA
Social Sciences
Therapy
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Title Microbiota in anorexia nervosa: The triangle between bacterial species, metabolites and psychological tests
URI https://www.ncbi.nlm.nih.gov/pubmed/28636668
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http://dx.doi.org/10.1371/journal.pone.0179739
Volume 12
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