User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Oral vancomycin treatment does not alter markers of postprandial inflammation in lean and obese subjects.

Primary tabs

download
  • Open access
  • PDF
  • 589.96 K
Bakker, Guido J Schnitzler, Johan G Bekkering, Siroon de Clercq, Nicolien C Koopen, Annefleur M Cani, Patrice D. [UCL] Nieuwdorp, Max

Intake of a high-fat meal induces a systemic inflammatory response in the postprandial which is augmented in obese subjects. However, the underlying mechanisms of this response have not been fully elucidated. We aimed to assess the effect of gut microbiota modulation on postprandial inflammatory response in lean and obese subjects. Ten lean and ten obese subjects with metabolic syndrome received oral vancomycin 500 mg four times per day for 7 days. Oral high-fat meal tests (50 g fat/m body surface area) were performed before and after vancomycin intervention. Gut microbiota composition, leukocyte counts, plasma lipopolysaccharides (LPS), LPS-binding protein (LBP), IL-6 and MCP-1 concentrations and monocyte CCR2 and cytokine expression were determined before and after the high-fat meal. Oral vancomycin treatment resulted in profound changes in gut microbiota composition and significantly decreased bacterial diversity in both groups (phylogenetic diversity pre- versus post-intervention: lean, 56.9 ± 7.8 vs. 21.4 ± 6.6, P < 0.001; obese, 53.9 ± 7.8 vs. 21.0 ± 5.9, P < 0.001). After intervention, fasting plasma LPS significantly increased (lean, median [IQR] 0.81 [0.63-1.45] EU/mL vs. 2.23 [1.33-3.83] EU/mL, P = 0.017; obese, median [IQR] 0.76 [0.45-1.03] EU/mL vs. 1.44 [1.11-4.24], P = 0.014). However, postprandial increases in leukocytes and plasma LPS were unaffected by vancomycin in both groups. Moreover, we found no changes in plasma LBP, IL-6 and MCP-1 or in monocyte CCR2 expression. Despite major vancomycin-induced disruption of the gut microbiota and increased fasting plasma LPS, the postprandial inflammatory phenotype in lean and obese subjects was unaffected in this study.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2019
Language Anglais
Journal information "Physiological reports" - Vol. 7, no.16, p. e14199 [1-13] (2019)
Publisher Wiley Periodicals, Inc. ((United States) Malden, MA)
e-issn 2051-817X
Publication status Publié
Affiliation UCL - SSS/LDRI - Louvain Drug Research Institute
Keywords Bacterial endotoxins ; Bacterial translocation ; Inflammation ; Obesity
Links
  1. Alipour Arash, van Oostrom Antonie J.H. H.M, Izraeljan Alisa, Verseyden Caroline, Collins Jennifer M., Frayn Keith N., Plokker Thijs W.M., Elte Jan Willem F., Castro Cabezas Manuel, Leukocyte Activation by Triglyceride-Rich Lipoproteins, 10.1161/atvbaha.107.159749
  2. Amar Jacques, Chabo Chantal, Waget Aurélie, Klopp Pascale, Vachoux Christelle, Bermúdez‐Humarán Luis G., Smirnova Natalia, Bergé Mathieu, Sulpice Thierry, Lahtinen Sampo, Ouwehand Arthur, Langella Philippe, Rautonen Nina, Sansonetti Philippe J., Burcelin Rémy, Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment, 10.1002/emmm.201100159
  3. Basu Subhabrata, Haghiac Maricela, Surace Peter, Challier Jean-Claude, Guerre-Millo Michele, Singh Katherine, Waters Thaddeus, Minium Judi, Presley Larraine, Catalano Patrick M., Hauguel-de Mouzon Sylvie, Pregravid Obesity Associates With Increased Maternal Endotoxemia and Metabolic Inflammation, 10.1038/oby.2010.215
  4. Béaslas Olivier, Cueille Carine, Delers François, Chateau Danielle, Chambaz Jean, Rousset Monique, Carrière Véronique, Sensing of Dietary Lipids by Enterocytes: A New Role for SR-BI/CLA-1, 10.1371/journal.pone.0004278
  5. Bernelot Moens Sophie J., Neele Annette E., Kroon Jeffrey, van der Valk Fleur M., Van den Bossche Jan, Hoeksema Marten A., Hoogeveen Renate M., Schnitzler Johan G., Baccara-Dinet Marie T., Manvelian Garen, de Winther Menno P.J., Stroes Erik S.G., PCSK9 monoclonal antibodies reverse the pro-inflammatory profile of monocytes in familial hypercholesterolaemia, 10.1093/eurheartj/ehx002
  6. Blackburn Patricia, Després Jean-Pierre, Lamarche Benoît, Tremblay Angelo, Bergeron Jean, Lemieux Isabelle, Couillard Charles, Postprandial Variations of Plasma Inflammatory Markers in Abdominally Obese Men*, 10.1038/oby.2006.201
  7. Callahan Benjamin J, McMurdie Paul J, Rosen Michael J, Han Andrew W, Johnson Amy Jo A, Holmes Susan P, DADA2: High-resolution sample inference from Illumina amplicon data, 10.1038/nmeth.3869
  8. Cani P. D., Amar J., Iglesias M. A., Poggi M., Knauf C., Bastelica D., Neyrinck A. M., Fava F., Tuohy K. M., Chabo C., Waget A., Delmee E., Cousin B., Sulpice T., Chamontin B., Ferrieres J., Tanti J.-F., Gibson G. R., Casteilla L., Delzenne N. M., Alessi M. C., Burcelin R., Metabolic Endotoxemia Initiates Obesity and Insulin Resistance, 10.2337/db06-1491
  9. Cani P. D., Bibiloni R., Knauf C., Waget A., Neyrinck A. M., Delzenne N. M., Burcelin R., Changes in Gut Microbiota Control Metabolic Endotoxemia-Induced Inflammation in High-Fat Diet-Induced Obesity and Diabetes in Mice, 10.2337/db07-1403
  10. Chawla Ajay, Nguyen Khoa D., Goh Y. P. Sharon, Macrophage-mediated inflammation in metabolic disease, 10.1038/nri3071
  11. Clemente-Postigo M., Queipo-Ortuño M. I., Murri M., Boto-Ordoñez M., Perez-Martinez P., Andres-Lacueva C., Cardona F., Tinahones F. J., Endotoxin increase after fat overload is related to postprandial hypertriglyceridemia in morbidly obese patients, 10.1194/jlr.p020909
  12. Deopurkar R., Ghanim H., Friedman J., Abuaysheh S., Sia C. L., Mohanty P., Viswanathan P., Chaudhuri A., Dandona P., Differential Effects of Cream, Glucose, and Orange Juice on Inflammation, Endotoxin, and the Expression of Toll-Like Receptor-4 and Suppressor of Cytokine Signaling-3, 10.2337/dc09-1630
  13. van Dijk Susan J., Mensink Marco, Esser Diederik, Feskens Edith J. M., Müller Michael, Afman Lydia A., Responses to High-Fat Challenges Varying in Fat Type in Subjects with Different Metabolic Risk Phenotypes: A Randomized Trial, 10.1371/journal.pone.0041388
  14. Erridge Clett, Attina Teresa, Spickett Corinne M, Webb David J, A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation, 10.1093/ajcn/86.5.1286
  15. Esser Diederik, van Dijk Susan J., Oosterink Els, Müller Michael, Afman Lydia A., A High-Fat SFA, MUFA, or n3 PUFA Challenge Affects the Vascular Response and Initiates an Activated State of Cellular Adherence in Lean and Obese Middle-Aged Men, 10.3945/jn.113.174540
  16. Everard A., Belzer C., Geurts L., Ouwerkerk J. P., Druart C., Bindels L. B., Guiot Y., Derrien M., Muccioli G. G., Delzenne N. M., de Vos W. M., Cani P. D., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity, 10.1073/pnas.1219451110
  17. Fogarty Christopher L., Nieminen Janne K., Peräneva Lina, Lassenius Mariann I., Ahola Aila J., Taskinen Marja-Riitta, Jauhiainen Matti, Kirveskari Juha, Pussinen Pirkko, Hörkkö Sohvi, Mäkinen Ville-Petteri, Gordin Daniel, Forsblom Carol, Groop Per-Henrik, Vaarala Outi, Lehto Markku, High-fat meals induce systemic cytokine release without evidence of endotoxemia-mediated cytokine production from circulating monocytes or myeloid dendritic cells, 10.1007/s00592-014-0641-8
  18. Ghanim H., Abuaysheh S., Sia C. L., Korzeniewski K., Chaudhuri A., Fernandez-Real J. M., Dandona P., Increase in Plasma Endotoxin Concentrations and the Expression of Toll-Like Receptors and Suppressor of Cytokine Signaling-3 in Mononuclear Cells After a High-Fat, High-Carbohydrate Meal: Implications for insulin resistance, 10.2337/dc09-0979
  19. Gower R. Michael, Wu Huaizhu, Foster Greg A., Devaraj Sridevi, Jialal Ishwarlal, Ballantyne Christie M., Knowlton Anne A., Simon Scott I., CD11c/CD18 Expression Is Upregulated on Blood Monocytes During Hypertriglyceridemia and Enhances Adhesion to Vascular Cell Adhesion Molecule-1, 10.1161/atvbaha.110.215434
  20. Gregor Margaret F., Hotamisligil Gökhan S., Inflammatory Mechanisms in Obesity, 10.1146/annurev-immunol-031210-101322
  21. Gutsmann T., Muller M., Carroll S. F., MacKenzie R. C., Wiese A., Seydel U., Dual Role of Lipopolysaccharide (LPS)-Binding Protein in Neutralization of LPS and Enhancement of LPS-Induced Activation of Mononuclear Cells, 10.1128/iai.69.11.6942-6950.2001
  22. Harte A. L., Varma M. C., Tripathi G., McGee K. C., Al-Daghri N. M., Al-Attas O. S., Sabico S., O'Hare J. P., Ceriello A., Saravanan P., Kumar S., McTernan P. G., High Fat Intake Leads to Acute Postprandial Exposure to Circulating Endotoxin in Type 2 Diabetic Subjects, 10.2337/dc11-1593
  23. Karlsson Fredrik H., Tremaroli Valentina, Nookaew Intawat, Bergström Göran, Behre Carl Johan, Fagerberg Björn, Nielsen Jens, Bäckhed Fredrik, Gut metagenome in European women with normal, impaired and diabetic glucose control, 10.1038/nature12198
  24. Kembel S. W. D. D.Ackerly S. P.Blomberg W. K.Cornwell P. D.Cowan M. R.Helmus et al.2014.Package Picante: R tools for integrating phylogenies and ecology. Version 1.7.
  25. Khoury Dalia El, Hwalla Nahla, Frochot Vincent, Lacorte Jean-Marc, Chabert Michèle, Kalopissis Athina D., Postprandial metabolic and hormonal responses of obese dyslipidemic subjects with metabolic syndrome to test meals, rich in carbohydrate, fat or protein, 10.1016/j.atherosclerosis.2009.11.017
  26. Kim Dorothy, Hofstaedter Casey E., Zhao Chunyu, Mattei Lisa, Tanes Ceylan, Clarke Erik, Lauder Abigail, Sherrill-Mix Scott, Chehoud Christel, Kelsen Judith, Conrad Máire, Collman Ronald G., Baldassano Robert, Bushman Frederic D., Bittinger Kyle, Optimizing methods and dodging pitfalls in microbiome research, 10.1186/s40168-017-0267-5
  27. Klop B., van de Geijn G.-J. M., Njo T. L., Janssen H. W., Rietveld A. P., van Miltenburg A., Fernández-Sender L., Elte J. W. F., Castro Cabezas M., Leukocyte cell population data (volume conductivity scatter) in postprandial leukocyte activation, 10.1111/ijlh.12103
  28. Kozich James J., Westcott Sarah L., Baxter Nielson T., Highlander Sarah K., Schloss Patrick D., Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform, 10.1128/aem.01043-13
  29. Lankelma Jacqueline M, Belzer Clara, Hoogendijk Arie J, de Vos Alex F, de Vos Willem M, van der Poll Tom, Wiersinga Joost W, Antibiotic-Induced Gut Microbiota Disruption Decreases TNF-α Release by Mononuclear Cells in Healthy Adults : , 10.1038/ctg.2016.43
  30. Laugerette Fabienne, Vors Cécile, Géloën Alain, Chauvin Marie-Agnès, Soulage Christophe, Lambert-Porcheron Stéphanie, Peretti Noël, Alligier Maud, Burcelin Rémy, Laville Martine, Vidal Hubert, Michalski Marie-Caroline, Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation, 10.1016/j.jnutbio.2009.11.011
  31. Laugerette Fabienne, Alligier Maud, Bastard Jean‐Philippe, Drai Jocelyne, Chanséaume Emilie, Lambert‐Porcheron Stéphanie, Laville Martine, Morio Béatrice, Vidal Hubert, Michalski Marie‐Caroline, Overfeeding increases postprandial endotoxemia in men: Inflammatory outcome may depend on LPS transporters LBP and sCD14, 10.1002/mnfr.201400044
  32. Lozupone C., Knight R., UniFrac: a New Phylogenetic Method for Comparing Microbial Communities, 10.1128/aem.71.12.8228-8235.2005
  33. Lundman Pia, Boquist Susanna, Samnegård Ann, Bennermo Marie, Held Claes, Ericsson Carl-Göran, Silveira Angela, Hamsten Anders, Tornvall Per, A high-fat meal is accompanied by increased plasma interleukin-6 concentrations, 10.1016/j.numecd.2005.11.009
  34. McMurdie Paul J., Holmes Susan, phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data, 10.1371/journal.pone.0061217
  35. Meher Dayanidhi, Dutta Deep, Ghosh Sujoy, Mukhopadhyay Pradip, Chowdhury Subhankar, Mukhopadhyay Satinath, Effect of a mixed meal on plasma lipids, insulin resistance and systemic inflammation in non-obese Indian adults with normal glucose tolerance and treatment naïve type-2 diabetes, 10.1016/j.diabres.2013.12.047
  36. Milan Amber M., Pundir Shikha, Pileggi Chantal A., Markworth James F., Lewandowski Paul A., Cameron-Smith David, Comparisons of the Postprandial Inflammatory and Endotoxaemic Responses to Mixed Meals in Young and Older Individuals: A Randomised Trial, 10.3390/nu9040354
  37. Moreno-Navarrete J M, Ortega F, Serino M, Luche E, Waget A, Pardo G, Salvador J, Ricart W, Frühbeck G, Burcelin R, Fernández-Real J M, Circulating lipopolysaccharide-binding protein (LBP) as a marker of obesity-related insulin resistance, 10.1038/ijo.2011.256
  38. Simplified Calculation of Body-Surface Area, 10.1056/nejm198710223171717
  39. Nappo Francesco, Esposito Katherine, Cioffi Michele, Giugliano Giovanni, Molinari Anna Maria, Paolisso Giuseppe, Marfella Raffaele, Giugliano Dario, Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: Role of fat and carbohydrate meals, 10.1016/s0735-1097(02)01741-2
  40. Oksanen J. F.Guillaume Blanchet M. K.Friendly R.Kindt P.Legendre D.McGlinn et al.2018.Package Vegan: Community Ecology Package. Version 2.5‐2.
  41. Opal Steven M., Scannon Patrick J., Vincent Jean‐Louis, White Mark, Carroll Stephen F., Palardy John E., Parejo Nicolas A., Pribble John P., Lemke Jon H., Relationship between Plasma Levels of Lipopolysaccharide (LPS) and LPS‐Binding Protein in Patients with Severe Sepsis and Septic Shock, 10.1086/315093
  42. Pussinen Pirkko J., Tuomisto Karolina, Jousilahti Pekka, Havulinna Aki S., Sundvall Jouko, Salomaa Veikko, Endotoxemia, Immune Response to Periodontal Pathogens, and Systemic Inflammation Associate With Incident Cardiovascular Disease Events, 10.1161/atvbaha.106.138743
  43. Pussinen P. J., Havulinna A. S., Lehto M., Sundvall J., Salomaa V., Endotoxemia Is Associated With an Increased Risk of Incident Diabetes, 10.2337/dc10-1676
  44. Qin Junjie, Li Yingrui, Cai Zhiming, Li Shenghui, Zhu Jianfeng, Zhang Fan, Liang Suisha, Zhang Wenwei, Guan Yuanlin, Shen Dongqian, Peng Yangqing, Zhang Dongya, Jie Zhuye, Wu Wenxian, Qin Youwen, Xue Wenbin, Li Junhua, Han Lingchuan, Lu Donghui, Wu Peixian, Dai Yali, Sun Xiaojuan, Li Zesong, Tang Aifa, Zhong Shilong, Li Xiaoping, Chen Weineng, Xu Ran, Wang Mingbang, Feng Qiang, Gong Meihua, Yu Jing, Zhang Yanyan, Zhang Ming, Hansen Torben, Sanchez Gaston, Raes Jeroen, Falony Gwen, Okuda Shujiro, Almeida Mathieu, LeChatelier Emmanuelle, Renault Pierre, Pons Nicolas, Batto Jean-Michel, Zhang Zhaoxi, Chen Hua, Yang Ruifu, Zheng Weimou, Li Songgang, Yang Huanming, Wang Jian, Ehrlich S. Dusko, Nielsen Rasmus, Pedersen Oluf, Kristiansen Karsten, Wang Jun, A metagenome-wide association study of gut microbiota in type 2 diabetes, 10.1038/nature11450
  45. Quast Christian, Pruesse Elmar, Yilmaz Pelin, Gerken Jan, Schweer Timmy, Yarza Pablo, Peplies Jörg, Glöckner Frank Oliver, The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, 10.1093/nar/gks1219
  46. Reijnders Dorien, Goossens Gijs H., Hermes Gerben D.A., Neis Evelien P.J.G., van der Beek Christina M., Most Jasper, Holst Jens J., Lenaerts Kaatje, Kootte Ruud S., Nieuwdorp Max, Groen Albert K., Olde Damink Steven W.M., Boekschoten Mark V., Smidt Hauke, Zoetendal Erwin G., Dejong Cornelis H.C., Blaak Ellen E., Effects of Gut Microbiota Manipulation by Antibiotics on Host Metabolism in Obese Humans: A Randomized Double-Blind Placebo-Controlled Trial, 10.1016/j.cmet.2016.06.016
  47. Salonen Anne, Nikkilä Janne, Jalanka-Tuovinen Jonna, Immonen Outi, Rajilić-Stojanović Mirjana, Kekkonen Riina A., Palva Airi, de Vos Willem M., Comparative analysis of fecal DNA extraction methods with phylogenetic microarray: Effective recovery of bacterial and archaeal DNA using mechanical cell lysis, 10.1016/j.mimet.2010.02.007
  48. Schromm A. B., J. Immunol., 161, 5464 (1998)
  49. Schwander Flurina, Kopf-Bolanz Katrin A., Buri Caroline, Portmann Reto, Egger Lotti, Chollet Magali, McTernan Philip G., Piya Milan K., Gijs Martin A. M., Vionnet Nathalie, Pralong François, Laederach Kurt, Vergères Guy, A Dose-Response Strategy Reveals Differences between Normal-Weight and Obese Men in Their Metabolic and Inflammatory Responses to a High-Fat Meal, 10.3945/jn.114.193565
  50. Sun L., Yu Z., Ye X., Zou S., Li H., Yu D., Wu H., Chen Y., Dore J., Clement K., Hu F. B., Lin X., A Marker of Endotoxemia Is Associated With Obesity and Related Metabolic Disorders in Apparently Healthy Chinese, 10.2337/dc10-0340
  51. Thompson Patricia A., Kitchens Richard L., Native High-Density Lipoprotein Augments Monocyte Responses to Lipopolysaccharide (LPS) by Suppressing the Inhibitory Activity of LPS-Binding Protein, 10.4049/jimmunol.177.7.4880
  52. Thompson Patricia A., Berbée Jimmy F.P., Rensen Patrick C.N., Kitchens Richard L., Apolipoprotein A-II augments monocyte responses to LPS by suppressing the inhibitory activity of LPS-binding protein, 10.1177/1753425908099171
  53. Tremaroli Valentina, Bäckhed Fredrik, Functional interactions between the gut microbiota and host metabolism, 10.1038/nature11552
  54. Turnbaugh Peter J., Hamady Micah, Yatsunenko Tanya, Cantarel Brandi L., Duncan Alexis, Ley Ruth E., Sogin Mitchell L., Jones William J., Roe Bruce A., Affourtit Jason P., Egholm Michael, Henrissat Bernard, Heath Andrew C., Knight Rob, Gordon Jeffrey I., A core gut microbiome in obese and lean twins, 10.1038/nature07540
  55. Verweij Simone L, Duivenvoorden Raphaël, Stiekema Lotte C A, Nurmohamed Nick S, van der Valk Fleur M, Versloot Miranda, Verberne Hein J, Stroes Erik S G, Nahrendorf Matthias, Bekkering Siroon, Bernelot Moens Sophie J, CCR2 expression on circulating monocytes is associated with arterial wall inflammation assessed by 18F-FDG PET/CT in patients at risk for cardiovascular disease, 10.1093/cvr/cvx224
  56. Vishnyakova Tatyana G., Bocharov Alexander V., Baranova Irina N., Chen Zhigang, Remaley Alan T., Csako Gyorgy, Eggerman Thomas L., Patterson Amy P., Binding and Internalization of Lipopolysaccharide by Cla-1, a Human Orthologue of Rodent Scavenger Receptor B1, 10.1074/jbc.m211032200
  57. Vors Cécile, Pineau Gaëlle, Drai Jocelyne, Meugnier Emmanuelle, Pesenti Sandra, Laville Martine, Laugerette Fabienne, Malpuech-Brugère Corinne, Vidal Hubert, Michalski Marie-Caroline, Postprandial Endotoxemia Linked With Chylomicrons and Lipopolysaccharides Handling in Obese Versus Lean Men: A Lipid Dose-Effect Trial, 10.1210/jc.2015-2518
  58. Vrieze Anne, Out Carolien, Fuentes Susana, Jonker Lisanne, Reuling Isaie, Kootte Ruud S., van Nood Els, Holleman Frits, Knaapen Max, Romijn Johannes A., Soeters Maarten R., Blaak Ellen E., Dallinga-Thie Geesje M., Reijnders Dorien, Ackermans Mariëtte T., Serlie Mireille J., Knop Filip K., Holst Jenst J., van der Ley Claude, Kema Ido P., Zoetendal Erwin G., de Vos Willem M., Hoekstra Joost B.L., Stroes Erik S., Groen Albert K., Nieuwdorp Max, Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity, 10.1016/j.jhep.2013.11.034
  59. Wang Q., Garrity G. M., Tiedje J. M., Cole J. R., Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy, 10.1128/aem.00062-07
  60. Zweigner J., High concentrations of lipopolysaccharide-binding protein in serum of patients with severe sepsis or septic shock inhibit the lipopolysaccharide response in human monocytes, 10.1182/blood.v98.13.3800
Bibliographic reference Bakker, Guido J ; Schnitzler, Johan G ; Bekkering, Siroon ; de Clercq, Nicolien C ; Koopen, Annefleur M ; et. al. Oral vancomycin treatment does not alter markers of postprandial inflammation in lean and obese subjects.. In: Physiological reports, Vol. 7, no.16, p. e14199 [1-13] (2019)
Permanent URL http://hdl.handle.net/2078.1/218910