Human Stool Metabolome Differs upon 24 h Blood Pressure Levels and Blood Pressure Dipping Status: A Prospective Longitudinal Study

HUART, Justine; Cirillo, Arianna; Taminiau, Bernard; DESCY, Julie; SAINT-REMY, Annie; Daube, Georges; KRZESINSKI, Jean-Marie; MELIN, Pierrette; De Tullio, Pascal; JOURET, François

doi:10.3390/metabo11050282

Article (Scientific journals)

Human Stool Metabolome Differs upon 24 h Blood Pressure Levels and Blood Pressure Dipping Status: A Prospective Longitudinal Study

HUART, Justine; Cirillo, Arianna; Taminiau, Bernard et al.

2021 • In Metabolites, 11 (5), p. 282

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/262357

DOI
10.3390/metabo11050282

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

metabolites-11-00282-1.pdf

Author postprint (1.36 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Metabolomics; hypertension; micribiome

Abstract :

[en] Dysbiosis of gut microbiota (GM) has been involved in the pathophysiology of arterial hypertension (HT), via a putative role of short chain fatty acids (SCFAs). Its role in the circadian regulation of blood pressure (BP), also called "the dipping profile", has been poorly investigated. Sixteen male volunteers and 10 female partners were subjected to 24 h ambulatory BP monitoring and were categorized in normotensive (NT) versus HT, as well as in dippers versus non-dippers. Nuclear magnetic resonance (NMR)-based metabolomics was performed on stool samples. A 5-year comparative follow-up of BP profiles and stool metabolomes was done in men. Significant correlations between stool metabolome and 24 h mean BP levels were found in both male and female cohorts and in the entire cohort (R2 = 0.72, R2 = 0.79, and R2 = 0.45, respectively). Multivariate analysis discriminated dippers versus non-dippers in both male and female cohorts and in the entire cohort (Q2 = 0.87, Q2 = 0.98, and Q2 = 0.68, respectively). Fecal amounts of acetate, propionate, and butyrate were higher in HT versus NT patients (p = 0.027; p = 0.015 and p = 0.015, respectively), as well as in non-dippers versus dippers (p = 0.027, p = 0.038, and p = 0.036, respectively) in the entire cohort. SCFA levels were significantly different in patients changing of dipping status over the 5-year follow-up. In conclusion, stool metabolome changes upon global and circadian BP profiles in both genders.

Disciplines :

Pharmacy, pharmacology & toxicology

Author, co-author :

HUART, Justine ^✱; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Service de néphrologie

Cirillo, Arianna ^✱; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique

Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires

DESCY, Julie ; Centre Hospitalier Universitaire de Liège - CHU > Unilab > Laboratoire mycobactérie

SAINT-REMY, Annie ; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Service de néphrologie

Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires

KRZESINSKI, Jean-Marie ; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Service de néphrologie

MELIN, Pierrette ; Centre Hospitalier Universitaire de Liège - CHU > Unilab > Service de microbiologie clinique

De Tullio, Pascal ^✱; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique

JOURET, François ^✱; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Service de néphrologie

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Human Stool Metabolome Differs upon 24 h Blood Pressure Levels and Blood Pressure Dipping Status: A Prospective Longitudinal Study

Publication date :

29 April 2021

Journal title :

Metabolites

eISSN :

2218-1989

Publisher :

MDPI AG

Volume :

Issue :

Pages :

282

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 01 August 2021

Statistics

Number of views

237 (34 by ULiège)

Number of downloads

172 (16 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Yang, T.; Santisteban, M.M.; Rodriguez, V.; Vermali, R.; Ahmari, N.; Carvajal, J.M.; Zadeh, M.; Gong, M.; Qi, Y.; Zubcevic, J.; et al. Gut Dysbiosis Is Linked to Hypertension. Hypertension 2015, 65, 1331-1340.
Yan, Q.; Gu, Y.; Li, X.; Yang,W.; Jia, L.; Chen, C.; Han, X.; Huang, Y.; Zhao, L.; Li, P.; et al. Alterations of the Gut Microbiome in Hypertension. Front. Cell. Infect. Microbiol. 2017, 7, 381.
Li, J.; Zhao, F.; Wang, Y.; Chen, J.; Tao, J.; Tian, G.; Wu, S.; Liu, W.; Cui, Q.; Geng, B.; et al. Gut microbiota dysbiosis contributes to the development of hypertension. Microbiome 2017, 5, 14.
Kim, S.; Goel, R.; Kumar, A.; Qi, Y.; Lobaton, G.; Hosaka, K.; Mohammed, M.; Handberg, E.M.; Richards, E.M.; Pepine, C.J.; et al. Imbalance of gut microbiome and intestinal epithelial barrier dysfunction in patients with high blood pressure. Clin. Sci. 2018, 132, 701-718.
Meijers, B.; Jouret, F.; Evenepoel, P. Linking gut microbiota to cardiovascular disease and hypertension: Lessons from chronic kidney disease. Pharmacol. Res. 2018, 133, 101-107.
Butel, M.-J. Probiotics, gut microbiota and health. Méd. Mal. Infect. 2014, 44, 1-8.
Alonso, V.R.; Guarner, F. Linking the gut microbiota to human health. Br. J. Nutr. 2013, 109, S21-S26.
Raizada, M.K.; Joe, B.; Bryan, N.S.; Chang, E.B.; Dewhirst, F.E.; Borisy, G.G.; Galis, Z.S.; Henderson, W.; Jose, P.A.; Ketchum, C.J.; et al. Report of the National Heart, Lung, and Blood InstituteWorking Group on the Role of Microbiota in Blood Pressure Regulation. Hypertension 2017, 70, 479-485.
Van Hul, M.; Geurts, L.; Plovier, H.; Druart, C.; Everard, A.; Ståhlman, M.; Rhimi, M.; Chira, K.; Teissedre, P.-L.; Delzenne, N.M.; et al. Reduced obesity, diabetes, and steatosis upon cinnamon and grape pomace are associated with changes in gut microbiota and markers of gut barrier. Am. J. Physiol. Metab. 2018, 314, E334-E352.
Duparc, T.; Plovier, H.; Marrachelli, V.G.; Van Hul, M.; Essaghir, A.; Ståhlman, M.; Matamoros, S.; Geurts, L.; Pardo-Tendero, M.M.; Druart, C.; et al. Hepatocyte MyD88 affects bile acids, gut microbiota and metabolome contributing to regulate glucose and lipid metabolism. Gut 2016, 66, 620-632.
Genest, J. Progress in Hypertension Research. Hypertension 2001, 38, E13-E18.
Krzesinski, J.-M.; Saint-Remy, A. Essential hypertension, a complex trait. Rev. Med. Liege 2012, 67, 279-285.
Davidson, M.B.; Hix, J.K.; Vidt, D.G.; Brotman, D.J. Association of Impaired Diurnal Blood Pressure Variation with a Subsequent Decline in Glomerular Filtration Rate. Arch. Intern. Med. 2006, 166, 846-852.
Zweiker, R.; Eber, B.; Schumacher, M.; Toplak, H.; Klein, W. “Non-dipping” related to cardiovascular events in essential hypertensive patients. Acta Med. Austriaca 1994, 21, 86-89.
Bartolomaeus, H.; Markó, L.; Wilck, N.; Luft, F.C.; Forslund, S.K.; Muller, M.N. Precarious Symbiosis Between Host and Microbiome in Cardiovascular Health. Hypertension 2019, 73, 926-935.
Miyamoto, J.; Kasubuchi, M.; Nakajima, A.; Irie, J.; Itoh, H.; Kimura, I. The role of short-chain fatty acid on blood pressure regulation. Curr. Opin. Nephrol. Hypertens. 2016, 25, 379-383.
De La Cuesta-Zuluaga, J.; Mueller, N.T.; Álvarez-Quintero, R.; Velásquez-Mejía, E.P.; Sierra, J.A.; Corrales-Agudelo, V.; Carmona, J.A.; Abad, J.M.; Escobar, J.S. Higher Fecal Short-Chain Fatty Acid Levels Are Associated with Gut Microbiome Dysbiosis, Obesity, Hypertension and Cardiometabolic Disease Risk Factors. Nutrients 2018, 11, 51.
Pluznick, J.L. Microbial Short-Chain Fatty Acids and Blood Pressure Regulation. Curr. Hypertens. Rep. 2017, 19, 25.
Bugaut,M. Occurrence, absorption andmetabolismof short chain fatty acids in the digestive tract ofmammals. Comp. Biochem. Physiol. Part B Comp. Biochem. 1987, 86, 439-472.
Pluznick, J.L. Gut microbiota in renal physiology: Focus on short-chain fatty acids and their receptors. Kidney Int. 2016, 90, 1191-1198.
Ríos-Covián, D.; Ruas-Madiedo, P.; Margolles, A.; Gueimonde, M.; Reyes-Gavilán, C.G.D.L.; Salazar, N. Intestinal Short Chain Fatty Acids and their Link with Diet and Human Health. Front. Microbiol. 2016, 7, 185.
Koh, A.; De Vadder, F.; Kovatcheva-Datchary, P.; Bäckhed, F. From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites. Cell 2016, 165, 1332-1345.
Nilsson, N.E.; Kotarsky, K.; Owman, C.; Olde, B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem. Biophys. Res. Commun. 2003, 303, 1047-1052.
Brown, A.J.; Goldsworthy, S.M.; Barnes, A.A.; Eilert, M.M.; Tcheang, L.; Daniels, D.; Muir, A.I.; Wigglesworth, M.J.; Kinghorn, I.; Fraser, N.J.; et al. The Orphan G Protein-coupled Receptors GPR41 and GPR43 Are Activated by Propionate and Other Short Chain Carboxylic Acids. J. Biol. Chem. 2003, 278, 11312-11319.
Huart, J.; Leenders, J.; Taminiau, B.; Descy, J.; Saint-Remy, A.; Daube, G.; Krzesinski, J.-M.; Melin, P.; De Tullio, P.; Jouret, F. Gut Microbiota and Fecal Levels of Short-Chain Fatty Acids Differ Upon 24-Hour Blood Pressure Levels in Men. Hypertension 2019, 74, 1005-1013.
Sun, S.; Lulla, A.; Sioda, M.; Winglee, K.; Wu, M.C.; Jacobs, D.R.; Shikany, J.M.; Lloyd-Jones, D.M.; Launer, L.J.; Fodor, A.A.; et al. Gut Microbiota Composition and Blood Pressure. Hypertension 2019, 73, 998-1006.
Caporaso, J.G.; Lauber, C.L.; Walters, W.A.; Berg-Lyons, D.; Lozupone, C.A.; Turnbaugh, P.J.; Fierer, N.; Knight, R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 2011, 108 (Suppl. 1), 4516-4522.
Verhaar, B.J.H.; Collard, D.; Prodan, A.; Levels, J.H.M.; Zwinderman, A.H.; Bäckhed, F.; Vogt, L.; Peters, M.J.L.; Muller, M.; Nieuwdorp, M.; et al. Associations between gut microbiota, faecal short-chain fatty acids, and blood pressure across ethnic groups: The HELIUS study. Eur. Hear. J. 2020, 41, 4259-4267.
Bier, A.; Braun, T.; Khasbab, R.; Di Segni, A.; Grossman, E.; Haberman, Y.; Leibowitz, A. A High Salt Diet Modulates the Gut Microbiota and Short Chain Fatty Acids Production in a Salt-Sensitive Hypertension Rat Model. Nutrients 2018, 10, 1154.
Chakraborty, S.; Mandal, J.; Cheng, X.; Galla, S.; Hindupur, A.; Saha, P.; Yeoh, B.S.; Mell, B.; Yeo, J.-Y.; Vijay-Kumar, M.; et al. Diurnal Timing Dependent Alterations in Gut Microbial Composition Are Synchronously Linked to Salt-Sensitive Hypertension and Renal Damage. Hypertension 2020, 76, 59-72.
Huart, J.; Cirillo, A.; Saint-Remy, A.; Krzesinski, J.-M.; de Tullio, P.; Jouret, F. The faecal abundance of short chain fatty acids is increased in men with a non-dipping blood pressure profile. Acta Cardiol. 2021, 1-4.
Rahman, A.; Hasan, A.U.; Nishiyama, A.; Kobori, H. Altered Circadian Timing System-Mediated Non-Dipping Pattern of Blood Pressure and Associated Cardiovascular Disorders in Metabolic and Kidney Diseases. Int. J. Mol. Sci. 2018, 19, 400.
Agarwal, R. Regulation of circadian blood pressure: From mice to astronauts. Curr. Opin. Nephrol. Hypertens. 2010, 19, 51-58.
Paschos, G.K.; FitzGerald, G.A. Circadian Clocks and Metabolism: Implications for Microbiome and Aging. Trends Genet. 2017, 33, 760-769.
Voigt, R.M.; Forsyth, C.B.; Green, S.J.; Mutlu, E.; Engen, P.; Vitaterna, M.H.; Turek, F.W.; Keshavarzian, A. Circadian Disorganization Alters Intestinal Microbiota. PLoS ONE 2014, 9, e97500.
Leone, V.; Gibbons, S.M.; Martinez, K.; Hutchison, A.L.; Huang, E.Y.; Cham, C.M.; Pierre, J.F.; Heneghan, A.F.; Nadimpalli, A.; Hubert, N.; et al. Effects of Diurnal Variation of Gut Microbes and High-Fat Feeding on Host Circadian Clock Function and Metabolism. Cell Host Microbe 2015, 17, 681-689.
Mukherji, A.; Kobiita, A.; Ye, T.; Chambon, P. Homeostasis in Intestinal Epithelium Is Orchestrated by the Circadian Clock and Microbiota Cues Transduced by TLRs. Cell 2013, 153, 812-827.
Thaiss, C.A.; Zeevi, D.; Levy, M.; Zilberman-Schapira, G.; Suez, J.; Tengeler, A.C.; Abramson, L.; Katz, M.N.; Korem, T.; Zmora, N.; et al. Transkingdom Control of Microbiota Diurnal Oscillations Promotes Metabolic Homeostasis. Cell 2014, 159, 514-529.
Pickering, T.G.; Kario, K. Nocturnal non-dipping: What does it augur? Curr. Opin. Nephrol. Hypertens. 2001, 10, 611-616.
Pioli, M.R.; Ritter, A.M.V.; De Faria, A.P.; Modolo, R. White coat syndrome and its variations: Differences and clinical impact. Integr. Blood Press. Control 2018, 11, 73-79.
Bo, Y.; Kwok, K.-O.; Chung, V.C.-H.; Yu, C.-P.; Tsoi, K.K.-F.;Wong, S.Y.-S.; Lee, E.K.-P. Short-term reproducibility of ambulatory blood pressure measurements: A systematic review and meta-analysis of 35 observational studies. J. Hypertens. 2020, 38, 2095-2109.
Haug, K.; Cochrane, K.; Nainala, V.C.; Williams, M.; Chang, J.; Jayaseelan, K.V.; O’Donovan, C. MetaboLights: A resource evolving in response to the needs of its scientific community. Nucleic Acids Res. 2019, 48, D440-D444.
Mancia, G.; Fagard, R.; Narkiewicz, K.; Redon, J.; Zanchetti, A.; Böhm, M.; Christiaens, T.; Cifkova, R.; De Backer, G.; Dominiczak, A.; et al. 2013 ESH/ESC Guidelines for the management of arterial hypertension: The task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur. Heart J. 2013, 34, 2159-2219.
Fagard, R.H. Dipping pattern of nocturnal blood pressure in patients with hypertension. Expert Rev. Cardiovasc. Ther. 2009, 7, 599-605.
Cardona, S.; Eck, A.; Cassellas, M.; Gallart, M.; Alastrue, C.; Dore, J.; Azpiroz, F.; Roca, J.; Guarner, F.; Manichanh, C. Storage conditions of intestinal microbiota matter in metagenomic analysis. BMC Microbiol. 2012, 12, 158.
Rodriguez, C.; Taminiau, B.; Korsak, N.; Avesani, V.; Van Broeck, J.; Brach, P.; Delmée, M.; Daube, G. Longitudinal survey of Clostridium difficile presence and gut microbiota composition in a Belgian nursing home. BMC Microbiol. 2016, 16, 229.
Schloss, P.D.; Westcott, S.L.; Ryabin, T.; Hall, J.R.; Hartmann, M.; Hollister, E.B.; Lesniewski, R.A.; Oakley, B.B.; Parks, D.H.; Robinson, C.J.; et al. Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Appl. Environ. Microbiol. 2009, 75, 7537-7541.
Edgar, R.C.; Haas, B.J.; Clemente, J.C.; Quince, C.; Knight, R. UCHIME Improves Sensitivity and Speed of Chimera Detection. Bioinformatics 2011, 27, 2194-2200.
Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016, 4, e2584.
Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glöckner, F.O. The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. Nucleic Acids Res. 2012, 41, D590-D596.
Bray, J.R.; Curtis, J.T. An Ordination of the Upland Forest Communities of SouthernWisconsin. Ecol. Monogr. 1957, 27, 325-349.
Martin, A.P. Phylogenetic Approaches for Describing and Comparing the Diversity of Microbial Communities. Appl. Environ. Microbiol. 2002, 68, 3673-3682.