Donor metabolic characteristics drive effects of faecal microbiota transplantation on recipient insulin sensitivity, energy expenditure and intestinal transit time
ObjectiveBariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FM...
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| Published in | Gut Vol. 69; no. 3; pp. 502 - 512 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BMJ Publishing Group Ltd and British Society of Gastroenterology
01.03.2020
BMJ Publishing Group LTD BMJ Publishing Group |
| Series | Original research |
| Subjects | |
| Online Access | Get full text |
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| Abstract | ObjectiveBariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects.DesignSubjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope (2H2-glucose and 2H5-glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks.ResultsWe observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 µmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa.ConclusionAllogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects.Trial registration numberNTR4327. |
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| AbstractList | ObjectiveBariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects.DesignSubjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope (2H2-glucose and 2H5-glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks.ResultsWe observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 µmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa.ConclusionAllogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects.Trial registration numberNTR4327. Bariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects.OBJECTIVEBariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects.Subjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope (2H2-glucose and 2H5-glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks.DESIGNSubjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope (2H2-glucose and 2H5-glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks.We observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 µmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa.RESULTSWe observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 µmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa.Allogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects.CONCLUSIONAllogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects.NTR4327.TRIAL REGISTRATION NUMBERNTR4327. Objective: Bariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects. Design: Subjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope (2H2-glucose and 2H5-glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks. Results: We observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 μmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa. Conclusion: Allogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects. Trial registration number: NTR4327. Bariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery diet-induced obese mice in germ-free mice improves glucose metabolism and intestinal homeostasis. We here investigated whether allogenic FMT using faeces from post-Roux-en-Y gastric bypass donors (RYGB-D) compared with using faeces from metabolic syndrome donors (METS-D) has short-term effects on glucose metabolism, intestinal transit time and adipose tissue inflammation in treatment-naïve, obese, insulin-resistant male subjects. Subjects with metabolic syndrome (n=22) received allogenic FMT either from RYGB-D or METS-D. Hepatic and peripheral insulin sensitivity as well as lipolysis were measured at baseline and 2 weeks after FMT by hyperinsulinaemic euglycaemic stable isotope ( H -glucose and H -glycerol) clamp. Secondary outcome parameters were changes in resting energy expenditure, intestinal transit time, faecal short-chain fatty acids (SCFA) and bile acids, and inflammatory markers in subcutaneous adipose tissue related to intestinal microbiota composition. Faecal SCFA, bile acids, glycaemic control and inflammatory parameters were also evaluated at 8 weeks. We observed a significant decrease in insulin sensitivity 2 weeks after allogenic METS-D FMT (median rate of glucose disappearance: from 40.6 to 34.0 µmol/kg/min; p<0.01). Moreover, a trend (p=0.052) towards faster intestinal transit time following RYGB-D FMT was seen. Finally, we observed changes in faecal bile acids (increased lithocholic, deoxycholic and (iso)lithocholic acid after METS-D FMT), inflammatory markers (decreased adipose tissue chemokine ligand 2 (CCL2) gene expression and plasma CCL2 after RYGB-D FMT) and changes in several intestinal microbiota taxa. Allogenic FMT using METS-D decreases insulin sensitivity in metabolic syndrome recipients when compared with using post-RYGB-D. Further research is needed to delineate the role of donor characteristics in FMT efficacy in human insulin-resistant subjects. NTR4327. |
| Author | Khan, Muhammad Tanweer de Groot, Pieter Scheithauer, Torsten Bergman, Jacques JGHM Hoekstra, Joost B L de Brauw, Maurits Holleman, Frits Gerdes, Victor E Schimmel, Alinda W M Levels, Johannes H M Bäckhed, Fredrik Serlie, Mireille J M Groen, Albert Prodan, Andrei Sales, Amber Nieuwdorp, Max Herrema, Hilde Levin, Evgeni Ackermans, Mariette Ståhlman, Marcus Dallinga-Thie, Geesje Bakker, Guido J |
| AuthorAffiliation | 1 Department of Internal and Vascular Medicine , Amsterdam University Medical Centres , Amsterdam , The Netherlands 3 Department of Surgery , Spaarne Gasthuis , Haarlem , The Netherlands 4 Department of Gastroenterology , Amsterdam University Medical Centres , Amsterdam , The Netherlands 2 Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy , Goteborgs Universitet , Gothenburg , Sweden |
| AuthorAffiliation_xml | – name: 4 Department of Gastroenterology , Amsterdam University Medical Centres , Amsterdam , The Netherlands – name: 1 Department of Internal and Vascular Medicine , Amsterdam University Medical Centres , Amsterdam , The Netherlands – name: 2 Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy , Goteborgs Universitet , Gothenburg , Sweden – name: 3 Department of Surgery , Spaarne Gasthuis , Haarlem , The Netherlands |
| Author_xml | – sequence: 1 givenname: Pieter orcidid: 0000-0003-3559-0138 surname: de Groot fullname: de Groot, Pieter organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 2 givenname: Torsten surname: Scheithauer fullname: Scheithauer, Torsten organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 3 givenname: Guido J surname: Bakker fullname: Bakker, Guido J organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 4 givenname: Andrei orcidid: 0000-0003-2789-7789 surname: Prodan fullname: Prodan, Andrei organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 5 givenname: Evgeni surname: Levin fullname: Levin, Evgeni organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 6 givenname: Muhammad Tanweer surname: Khan fullname: Khan, Muhammad Tanweer organization: Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy, Goteborgs Universitet, Gothenburg, Sweden – sequence: 7 givenname: Hilde surname: Herrema fullname: Herrema, Hilde organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 8 givenname: Mariette surname: Ackermans fullname: Ackermans, Mariette organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 9 givenname: Mireille J M surname: Serlie fullname: Serlie, Mireille J M organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 10 givenname: Maurits surname: de Brauw fullname: de Brauw, Maurits organization: Department of Surgery, Spaarne Gasthuis, Haarlem, The Netherlands – sequence: 11 givenname: Johannes H M surname: Levels fullname: Levels, Johannes H M organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 12 givenname: Amber surname: Sales fullname: Sales, Amber organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 13 givenname: Victor E surname: Gerdes fullname: Gerdes, Victor E organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 14 givenname: Marcus surname: Ståhlman fullname: Ståhlman, Marcus organization: Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy, Goteborgs Universitet, Gothenburg, Sweden – sequence: 15 givenname: Alinda W M surname: Schimmel fullname: Schimmel, Alinda W M organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 16 givenname: Geesje surname: Dallinga-Thie fullname: Dallinga-Thie, Geesje organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 17 givenname: Jacques JGHM surname: Bergman fullname: Bergman, Jacques JGHM organization: Department of Gastroenterology, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 18 givenname: Frits surname: Holleman fullname: Holleman, Frits organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 19 givenname: Joost B L surname: Hoekstra fullname: Hoekstra, Joost B L organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 20 givenname: Albert surname: Groen fullname: Groen, Albert organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands – sequence: 21 givenname: Fredrik surname: Bäckhed fullname: Bäckhed, Fredrik organization: Wallenberg Laboratory, Department of Molecular and Clinical Medicine, Sahlgrenska Academy, Goteborgs Universitet, Gothenburg, Sweden – sequence: 22 givenname: Max surname: Nieuwdorp fullname: Nieuwdorp, Max organization: Department of Internal and Vascular Medicine, Amsterdam University Medical Centres, Amsterdam, The Netherlands |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31147381$$D View this record in MEDLINE/PubMed https://gup.ub.gu.se/publication/282512$$DView record from Swedish Publication Index |
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| Keywords | intestinal microbiology bile acid metabolism diabetes mellitus gastrointestinal transit |
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| Snippet | ObjectiveBariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric... Bariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric surgery... Objective: Bariatric surgery improves glucose metabolism. Recent data suggest that faecal microbiota transplantation (FMT) using faeces from postbariatric... |
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| SubjectTerms | Adipose tissue Adult Aged Bile bile acid metabolism Bile acids Bile Acids and Salts - analysis Chemokine CCL2 - blood Chemokine CCL2 - genetics Chemokines Chromatography Diabetes diabetes mellitus Diet Donors Endocrinology and Diabetes Endokrinologi och diabetes Energy expenditure Energy Metabolism Fatty acids Fatty Acids, Volatile - analysis Fecal Microbiota Transplantation Feces Feces - chemistry Gastric Bypass Gastroenterologi och hepatologi Gastroenterology and Hepatology Gastrointestinal Microbiome Gastrointestinal surgery Gastrointestinal Transit Gene Expression Germfree Glucose Glucose - metabolism Glycerol Gut Microbiota Homeostasis Humans Inflammation Insulin Insulin Resistance intestinal microbiology Intestinal microflora Intestinal transit time Intestine Lipolysis Male Metabolic syndrome Metabolic Syndrome - metabolism Metabolic Syndrome - physiopathology Metabolic Syndrome - therapy Metabolites Metabolomics Microbiota Middle Aged Monocyte chemoattractant protein 1 Probiotics Studies Subcutaneous Fat - metabolism Surgery Tissue Donors Transplantation Transplants & implants Weight control Young Adult |
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| Title | Donor metabolic characteristics drive effects of faecal microbiota transplantation on recipient insulin sensitivity, energy expenditure and intestinal transit time |
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