Noninvasive monitoring of fibre fermentation in healthy volunteers by analyzing breath volatile metabolites: lessons from the FiberTAG intervention study

Audrey M Neyrinck, Julie Rodriguez, Zhengxiao Zhang, Benjamin Seethaler, Florence Mailleux, Joeri Vercammen, Laure B Bindels, Patrice D Cani, Julie-Anne Nazare, Véronique Maquet, Martine Laville, Stephan C Bischoff, Jens Walter, Nathalie M Delzenne, Audrey M Neyrinck, Julie Rodriguez, Zhengxiao Zhang, Benjamin Seethaler, Florence Mailleux, Joeri Vercammen, Laure B Bindels, Patrice D Cani, Julie-Anne Nazare, Véronique Maquet, Martine Laville, Stephan C Bischoff, Jens Walter, Nathalie M Delzenne

Abstract

The fermentation of dietary fibre (DF) leads to the production of bioactive metabolites, the most volatile ones being excreted in the breath. The aim of this study was to analyze the profile of exhaled breath volatile metabolites (BVM) and gastrointestinal symptoms in healthy volunteers after a single ingestion of maltodextrin (placebo) versus chitin-glucan (CG), an insoluble DF previously shown to be fermented into short-chain fatty acids (SCFA) by the human microbiota in vitro. Maltodextrin (4.5 g at day 0) or CG (4.5 g at day 2) were added to a standardized breakfast in fasting healthy volunteers (n = 15). BVM were measured using selected ion flow tube mass spectrometry (SIFT-MS) throughout the day. A single ingestion of 4.5 g CG did not induce significant gastrointestinal discomfort. Untargeted metabolomics analysis of breath highlighted that 13 MS-fragments (among 408 obtained from ionizations of breath) discriminated CG versus maltodextrin acute intake in the posprandial state. The targeted analysis revealed that CG increased exhaled butyrate and 5 other BVM - including the microbial metabolites 2,3-butanedione and 3-hydroxybutanone - with a peak observed 6 h after CG intake. Correlation analyses with fecal microbiota (Illumina 16S rRNA sequencing) spotlighted Mitsuokella as a potential genus responsible for the presence of butyric acid, triethylamine and 3-hydroxybutanone in the breath. In conclusion, measuring BMV in the breath reveals the microbial signature of the fermentation of DF after a single ingestion. This protocol allows to analyze the time-course of released bioactive metabolites that could be proposed as new biomarkers of DF fermentation, potentially linked to their biological properties. Trial registration: Clinical Trials NCT03494491. Registered 11 April 2018 - Retrospectively registered, https://ichgcp.net/clinical-trials-registry/NCT03494491.

Keywords: Gut microbiota; SCFA; breath volatile metabolites; chitin-glucan; fermentation; insoluble dietary fibre.

Figures

Figure 1.
Figure 1.
Overview of the study design
Figure 1.
Figure 1.
Overview of the study design
Figure 2.
Figure 2.
Gut microbiota and short-chain fatty acids (SCFA) composition in fecal matter of 15 healthy subjects before intervention days. (a) Principal coordinate analysis (PCoA) score plot of β-diversity estimated using the using the Bray-curtis and unweighted uniFrac indexes. (b) α-diversity indexes related to bacterial richness (Observed OTU), evenness (Pielou) or both (Shannon) for each subject. (c) Bar plots of relative abundance of phylum levels accounting for more than 0.5% for each subject. (d) Bar plots of SCFA concentration for each subject
Figure 2.
Figure 2.
Gut microbiota and short-chain fatty acids (SCFA) composition in fecal matter of 15 healthy subjects before intervention days. (a) Principal coordinate analysis (PCoA) score plot of β-diversity estimated using the using the Bray-curtis and unweighted uniFrac indexes. (b) α-diversity indexes related to bacterial richness (Observed OTU), evenness (Pielou) or both (Shannon) for each subject. (c) Bar plots of relative abundance of phylum levels accounting for more than 0.5% for each subject. (d) Bar plots of SCFA concentration for each subject
Figure 3.
Figure 3.
Gastrointestinal tolerance assessed by visual analog scale of 15 healthy subjects about 8 symptoms after chitin-glucan intake of maltodextrin intake. Data are means ± SEM (p > .05; matched-pairs Wilcoxon signed-rank test on net AUC)
Figure 3.
Figure 3.
Gastrointestinal tolerance assessed by visual analog scale of 15 healthy subjects about 8 symptoms after chitin-glucan intake of maltodextrin intake. Data are means ± SEM (p > .05; matched-pairs Wilcoxon signed-rank test on net AUC)
Figure 4.
Figure 4.
Untargeted analysis of breath from 15 healthy subjects after chitin-glucan and maltodextrin intake. Principal component analysis (PCA) score plot of the MS-fragments from the SIFT-MS spectra (from H3O+, NO+ and O2+ ionizations) obtained in fasted state (time 0 h) the first test day (a) or in fasted state (time 0 h), in pre-prandial state (time 4 h) and in postprandial state (time 6 h) (b). PLS-DA (with cutoff 0.9) of 408 MS-fragments after chitin-glucan intake and maltodextrin intake at time 6 h (c). Statistical analysis was assessed by a Monte Carlo rank test
Figure 4.
Figure 4.
Untargeted analysis of breath from 15 healthy subjects after chitin-glucan and maltodextrin intake. Principal component analysis (PCA) score plot of the MS-fragments from the SIFT-MS spectra (from H3O+, NO+ and O2+ ionizations) obtained in fasted state (time 0 h) the first test day (a) or in fasted state (time 0 h), in pre-prandial state (time 4 h) and in postprandial state (time 6 h) (b). PLS-DA (with cutoff 0.9) of 408 MS-fragments after chitin-glucan intake and maltodextrin intake at time 6 h (c). Statistical analysis was assessed by a Monte Carlo rank test
Figure 5.
Figure 5.
Targeted short-chain fatty acids (SCFA) concentrations (changes from baseline) exhaled in breath of healthy subjects in response to chitin-glucan and maltodextrin intake. Data are means ± SEM (*p 

Figure 5.

Targeted short-chain fatty acids (SCFA)…

Figure 5.

Targeted short-chain fatty acids (SCFA) concentrations (changes from baseline) exhaled in breath of…

Figure 5.
Targeted short-chain fatty acids (SCFA) concentrations (changes from baseline) exhaled in breath of healthy subjects in response to chitin-glucan and maltodextrin intake. Data are means ± SEM (*p 

Figure 6.

Targeted breath volatile metabolites (BVM)…

Figure 6.

Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of…

Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 

Figure 6.

Targeted breath volatile metabolites (BVM)…

Figure 6.

Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of…

Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 
All figures (12)
Similar articles
Cited by
References
    1. Stephen AM, Champ MM, Cloran SJ, Fleith M, van Lieshout L, Mejborn H, Burley VJ.. Dietary fibre in Europe: current state of knowledge on definitions, sources, recommendations, intakes and relationships to health. Nutr Res Rev. 2017;30:149–190. doi:10.1017/S095442241700004X. - DOI - PubMed
    1. EFSA . Scientific opinion on the substantiation of health claims related to dietary fibre (ID 744, 745, 746, 748, 749, 753, 803, 810, 855, 1415, 1416, 4308, 4330) pursuant to article 13(1) of regulation (EC)No 1924/20061. EFSA Journal. 2010;8:1735. doi:10.2903/j.efsa.2010.1735. - DOI
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14:491–502. doi:10.1038/nrgastro.2017.75. - DOI - PubMed
    1. EFSA Panel on Dietetic Products NaAN . Scientific opinion on the safety of ‘Chitin-glucan’ as a novel food ingredient. EFSA Journal. 2010;8:1687. doi:10.2903/j.efsa.2010.1687. - DOI
    1. Marzorati MMV, Possemiers S. Fate of chitin-glucan in the human gastrointestinal tract as studied in a dynamic gut simulator (SHIME). J Funct Foods. 2017;30:313–320. doi:10.1016/j.jff.2017.01.030. - DOI
Show all 42 references
Publication types
MeSH terms
Associated data
Grant support
FiberTAG project was initiated from a European Joint Programming Initiative “A Healthy Diet for a Healthy Life” (JPI HDHL). This work was supported by the Service Public de Wallonie (SPW-EER, convention 1610365, Belgium). NMD is a recipient of grants from Fond de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). SCB is a recipient of a grant from the German Federal Ministry for Education and Research (BMBF, Germany, ID: 01EA1701). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no. 30770923).
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 5.
Figure 5.
Targeted short-chain fatty acids (SCFA) concentrations (changes from baseline) exhaled in breath of healthy subjects in response to chitin-glucan and maltodextrin intake. Data are means ± SEM (*p 

Figure 6.

Targeted breath volatile metabolites (BVM)…

Figure 6.

Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of…

Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 

Figure 6.

Targeted breath volatile metabolites (BVM)…

Figure 6.

Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of…

Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 
All figures (12)
Similar articles
Cited by
References
    1. Stephen AM, Champ MM, Cloran SJ, Fleith M, van Lieshout L, Mejborn H, Burley VJ.. Dietary fibre in Europe: current state of knowledge on definitions, sources, recommendations, intakes and relationships to health. Nutr Res Rev. 2017;30:149–190. doi:10.1017/S095442241700004X. - DOI - PubMed
    1. EFSA . Scientific opinion on the substantiation of health claims related to dietary fibre (ID 744, 745, 746, 748, 749, 753, 803, 810, 855, 1415, 1416, 4308, 4330) pursuant to article 13(1) of regulation (EC)No 1924/20061. EFSA Journal. 2010;8:1735. doi:10.2903/j.efsa.2010.1735. - DOI
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14:491–502. doi:10.1038/nrgastro.2017.75. - DOI - PubMed
    1. EFSA Panel on Dietetic Products NaAN . Scientific opinion on the safety of ‘Chitin-glucan’ as a novel food ingredient. EFSA Journal. 2010;8:1687. doi:10.2903/j.efsa.2010.1687. - DOI
    1. Marzorati MMV, Possemiers S. Fate of chitin-glucan in the human gastrointestinal tract as studied in a dynamic gut simulator (SHIME). J Funct Foods. 2017;30:313–320. doi:10.1016/j.jff.2017.01.030. - DOI
Show all 42 references
Publication types
MeSH terms
Associated data
Grant support
FiberTAG project was initiated from a European Joint Programming Initiative “A Healthy Diet for a Healthy Life” (JPI HDHL). This work was supported by the Service Public de Wallonie (SPW-EER, convention 1610365, Belgium). NMD is a recipient of grants from Fond de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). SCB is a recipient of a grant from the German Federal Ministry for Education and Research (BMBF, Germany, ID: 01EA1701). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no. 30770923).
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 6.
Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 

Figure 6.

Targeted breath volatile metabolites (BVM)…

Figure 6.

Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of…

Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 
All figures (12)
Similar articles
Cited by
References
    1. Stephen AM, Champ MM, Cloran SJ, Fleith M, van Lieshout L, Mejborn H, Burley VJ.. Dietary fibre in Europe: current state of knowledge on definitions, sources, recommendations, intakes and relationships to health. Nutr Res Rev. 2017;30:149–190. doi:10.1017/S095442241700004X. - DOI - PubMed
    1. EFSA . Scientific opinion on the substantiation of health claims related to dietary fibre (ID 744, 745, 746, 748, 749, 753, 803, 810, 855, 1415, 1416, 4308, 4330) pursuant to article 13(1) of regulation (EC)No 1924/20061. EFSA Journal. 2010;8:1735. doi:10.2903/j.efsa.2010.1735. - DOI
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14:491–502. doi:10.1038/nrgastro.2017.75. - DOI - PubMed
    1. EFSA Panel on Dietetic Products NaAN . Scientific opinion on the safety of ‘Chitin-glucan’ as a novel food ingredient. EFSA Journal. 2010;8:1687. doi:10.2903/j.efsa.2010.1687. - DOI
    1. Marzorati MMV, Possemiers S. Fate of chitin-glucan in the human gastrointestinal tract as studied in a dynamic gut simulator (SHIME). J Funct Foods. 2017;30:313–320. doi:10.1016/j.jff.2017.01.030. - DOI
Show all 42 references
Publication types
MeSH terms
Associated data
Grant support
FiberTAG project was initiated from a European Joint Programming Initiative “A Healthy Diet for a Healthy Life” (JPI HDHL). This work was supported by the Service Public de Wallonie (SPW-EER, convention 1610365, Belgium). NMD is a recipient of grants from Fond de la Recherche Scientifique (FRS-FNRS, convention PINT-MULTI R.8013.19 (NEURON, call 2019) and convention PDR T.0068.19) and from UCLouvain (Action de Recherche Concertée ARC18-23/092). SCB is a recipient of a grant from the German Federal Ministry for Education and Research (BMBF, Germany, ID: 01EA1701). PDC is supported by the Fonds Baillet Latour (Grant for Medical Research 2015), the Fonds de la Recherche Scientifique (FNRS, FRFS-WELBIO: WELBIO-CR-2019C-02R, and EOS program no. 30770923).
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Figure 6.
Figure 6.
Targeted breath volatile metabolites (BVM) concentrations (changes from baseline) exhaled in breath of healthy subjects significantly changed after chitin-glucan intake compared to maltodextrin intake. Data are means ± SEM (*p 
All figures (12)

References

    1. Stephen AM, Champ MM, Cloran SJ, Fleith M, van Lieshout L, Mejborn H, Burley VJ.. Dietary fibre in Europe: current state of knowledge on definitions, sources, recommendations, intakes and relationships to health. Nutr Res Rev. 2017;30:149–190. doi:10.1017/S095442241700004X.
    1. EFSA . Scientific opinion on the substantiation of health claims related to dietary fibre (ID 744, 745, 746, 748, 749, 753, 803, 810, 855, 1415, 1416, 4308, 4330) pursuant to article 13(1) of regulation (EC)No 1924/20061. EFSA Journal. 2010;8:1735. doi:10.2903/j.efsa.2010.1735.
    1. Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD, et al. Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14:491–502. doi:10.1038/nrgastro.2017.75.
    1. EFSA Panel on Dietetic Products NaAN . Scientific opinion on the safety of ‘Chitin-glucan’ as a novel food ingredient. EFSA Journal. 2010;8:1687. doi:10.2903/j.efsa.2010.1687.
    1. Marzorati MMV, Possemiers S. Fate of chitin-glucan in the human gastrointestinal tract as studied in a dynamic gut simulator (SHIME). J Funct Foods. 2017;30:313–320. doi:10.1016/j.jff.2017.01.030.
    1. Neyrinck AM, Possemiers S, Verstraete W, De Backer F, Cani PD, Delzenne NM. Dietary modulation of clostridial cluster XIVa gut bacteria (Roseburia spp.) by chitin-glucan fiber improves host metabolic alterations induced by high-fat diet in mice. J Nutr Biochem. 2012;23:51–59. doi:10.1016/j.jnutbio.2010.10.008.
    1. Berecochea-Lopez A, Decorde K, Ventura E, Godard M, Bornet A, Teissedre PL, Cristol JP, Rouanet JM. Fungal chitin-glucan from Aspergillus niger efficiently reduces aortic fatty streak accumulation in the high-fat fed hamster, an animal model of nutritionally induced atherosclerosis. J Agric Food Chem. 2009;57:1093–1098. doi:10.1021/jf803063v.
    1. Bays HE, Evans JL, Maki KC, Evans M, Maquet V, Cooper R, Anderson JW. Chitin-glucan fiber effects on oxidized low-density lipoprotein: a randomized controlled trial. Eur J Clin Nutr. 2013;67:2–7. doi:10.1038/ejcn.2012.121.
    1. Das S, Pal S, Mitra M. Significance of exhaled breath test in clinical diagnosis: a special focus on the detection of diabetes mellitus. J Med Biol Eng. 2016;36:605–624.
    1. Rieder F, Kurada S, Grove D, Cikach F, Lopez R, Patel N, Singh A, Alkhouri N, Shen B, Brzezinski A, et al. A distinct colon-derived breath metabolome is associated with inflammatory bowel disease, but not its complications. Clin Transl Gastroenterol. 2016;7:e201. doi:10.1038/ctg.2016.57.
    1. Ajibola OA, Smith D, Spanel P, Ferns GA. Effects of dietary nutrients on volatile breath metabolites. J Nutr Sci. 2013;2:e34. doi:10.1017/jns.2013.26.
    1. Raninen KJ, Lappi JE, Mukkala ML, Tuomainen TP, Mykkanen HM, Poutanen KS, Raatikainen OJ. Fiber content of diet affects exhaled breath volatiles in fasting and postprandial state in a pilot crossover study. Nutr Res. 2016;36:612–619. doi:10.1016/j.nutres.2016.02.008.
    1. Lawal O, Ahmed WM, Nijsen TME, Goodacre R, Fowler SJ. Exhaled breath analysis: a review of ‘breath-taking’ methods for off-line analysis. Metabolomics. 2017;13:110. doi:10.1007/s11306-017-1241-8.
    1. Bruderer T, Gaisl T, Gaugg MT, Nowak N, Streckenbach B, Muller S, Moeller A, Kohler M, Zenobi R. On-line analysis of exhaled breath focus review. Chem Rev. 2019;119:10803–10828. doi:10.1021/acs.chemrev.9b00005.
    1. Spanel P, Smith D. Quantification of volatile metabolites in exhaled breath by selected ion flow tube mass spectrometry, SIFT-MS. Clini Mass Spectrom. 2020;16:18–24. doi:10.1016/j.clinms.2020.02.001.
    1. Stefanuto PH, Zanella D, Vercammen J, Henket M, Schleich F, Louis R, Focant JF. Multimodal combination of GC x GC-HRTOFMS and SIFT-MS for asthma phenotyping using exhaled breath. Sci Rep. 2020;10:16159. doi:10.1038/s41598-020-73408-2.
    1. Neyrinck AM, Rodriguez J, Vinoy S, Maquet V, Walter J, Bischoff SC, Laville M, Delzenne NM. The FiberTAG project: tagging dietary fibre intake by measuring biomarkers related to the gut microbiota and their interest for health. Nutrition Bulletin. 2020;45:59–65. doi:10.1111/nbu.12416.
    1. Boshier PR, Marczin N, Hanna GB. Repeatability of the measurement of exhaled volatile metabolites using selected ion flow tube mass spectrometry. J Am Soc Mass Spectrom. 2010;21:1070–1074. doi:10.1016/j.jasms.2010.02.008.
    1. de Lacy Costello B, Amann A, Al-Kateb H, Flynn C, Filipiak W, Khalid T, Osborne D, Ratcliffe NM. A review of the volatiles from the healthy human body. J Breath Res. 2014;8:014001. doi:10.1088/1752-7155/8/1/014001.
    1. Rezaie A, Buresi M, Lembo A, Lin H, McCallum R, Rao S, Schmulson M, Valdovinos M, Zakko S, Hydrogen PM. Methane-based breath testing in gastrointestinal disorders: the North American consensus. Am J Gastroenterol. 2017;112:775–784. doi:10.1038/ajg.2017.46.
    1. Smolinska A, Tedjo DI, Blanchet L, Bodelier A, Pierik MJ, Masclee AAM, Dallinga J, Savelkoul PHM, Jonkers D, Penders J, et al. Volatile metabolites in breath strongly correlate with gut microbiome in CD patients. Anal Chim Acta. 2018;1025:1–11. doi:10.1016/j.aca.2018.03.046.
    1. Raman M, Ahmed I, Gillevet PM, Probert CS, Ratcliffe NM, Smith S, Greenwood R, Sikaroodi M, Lam V, Crotty P, et al. Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2013;11(868–75):e1–3. doi:10.1016/j.cgh.2013.02.015.
    1. Rondanelli M, Perdoni F, Infantino V, Faliva MA, Peroni G, Iannello G, Nichetti M, Alalwan TA, Perna S, Cocuzza C. Volatile organic compounds as biomarkers of gastrointestinal diseases and nutritional status. J Anal Methods Chem. 2019;2019:7247802. doi:10.1155/2019/7247802.
    1. Kistler M, Szymczak W, Fedrigo M, Fiamoncini J, Hollriegl V, Hoeschen C, Klingenspor M, Hrabe de Angelis M, Rozman J. Effects of diet-matrix on volatile organic compounds in breath in diet-induced obese mice. J Breath Res. 2014;8:016004.
    1. Baranska A, Tigchelaar E, Smolinska A, Dallinga JW, Moonen EJ, Dekens JA, Wijmenga C, Zhernakova A, van Schooten FJ. Profile of volatile organic compounds in exhaled breath changes as a result of gluten-free diet. J Breath Res. 2013;7:037104. doi:10.1088/1752-7155/7/3/037104.
    1. Barros R, Moreira A, Fonseca J, Delgado L, Castel-Branco MG, Haahtela T, Lopes C, Moreira P. Dietary intake of alpha-linolenic acid and low ratio of n-6:n-3 PUFA are associated with decreased exhaled NO and improved asthma control. Br J Nutr. 2011;106:441–450. doi:10.1017/S0007114511000328.
    1. Hageman JHJ, Nieuwenhuizen AG, van Ruth SM, Hageman JA, Keijer J. Application of volatile organic compound analysis in a nutritional intervention study: differential responses during five hours following consumption of a high- and a low-fat dairy drink. Mol Nutr Food Res. 2019;63:e1900189. doi:10.1002/mnfr.201900189.
    1. Filipiak W, Ruzsanyi V, Mochalski P, Filipiak A, Bajtarevic A, Ager C, Denz H, Hilbe W, Jamnig H, Hackl M, et al. Dependence of exhaled breath composition on exogenous factors, smoking habits and exposure to air pollutants. J Breath Res. 2012;6:036008. doi:10.1088/1752-7155/6/3/036008.
    1. Lee J, Ngo J, Blake D, Meinardi S, Pontello AM, Newcomb R, Galassetti PR. Improved predictive models for plasma glucose estimation from multi-linear regression analysis of exhaled volatile organic compounds. J Appl Physiol. 1985;2009:155–160.
    1. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–857. doi:10.1038/s41587-019-0209-9.
    1. King J, Mochalski P, Unterkofler K, Teschl G, Klieber M, Stein M, Amann A, Baumann M. Breath isoprene: muscle dystrophy patients support the concept of a pool of isoprene in the periphery of the human body. Biochem Biophys Res Commun. 2012;423:526–530. doi:10.1016/j.bbrc.2012.05.159.
    1. Smith D, Spanel P, Davies S. Trace gases in breath of healthy volunteers when fasting and after a protein-calorie meal: a preliminary study. J Appl Physiol. 1985;1999:1584–1588.
    1. Russell WR, Hoyles L, Flint HJ, Dumas ME. Colonic bacterial metabolites and human health. Curr Opin Microbiol. 2013;16:246–254. doi:10.1016/j.mib.2013.07.002.
    1. Louis P, Flint HJ. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett. 2009;294:1–8. doi:10.1111/j.1574-6968.2009.01514.x.
    1. Verbeke KA, Boobis AR, Chiodini A, Edwards CA, Franck A, Kleerebezem M, Nauta A, Raes J, van Tol EA, Tuohy KM. Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr Res Rev. 2015;28:42–66. doi:10.1017/S0954422415000037.
    1. Taucher J, Lagg A, Hansel A, Vogel W, Lindinger W. Methanol in human breath. Alcohol Clin Exp Res. 1995;19:1147–1150. doi:10.1111/j.1530-0277.1995.tb01593.x.
    1. Gelmont D, Stein RA, Mead JF. The bacterial origin of rat breath pentane. Biochem Biophys Res Commun. 1981;102:932–936. doi:10.1016/0006-291X(81)91627-2.
    1. Zalan Z, Hudacek J, Toth-Markus M, Husova E, Solichova K, Hegyi F, Plockova M, Chumchalova J, Halasz A. Sensorically and antimicrobially active metabolite production of Lactobacillus strains on Jerusalem artichoke juice. J Sci Food Agric. 2011;91:672–679. doi:10.1002/jsfa.4232.
    1. Gorham JB, Kang S, Williams BA, Grant LJ, McSweeney CS, Gidley MJ, Mikkelsen D. Addition of arabinoxylan and mixed linkage glucans in porcine diets affects the large intestinal bacterial populations. Eur J Nutr. 2017;56:2193–2206. doi:10.1007/s00394-016-1263-4.
    1. Duncan SH, Hold GL, Barcenilla A, Stewart CS, Flint HJ. Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol. 2002;52:1615–1620.
    1. Kharbach M, Kamal R, Mansouri MA, Marmouzi I, Viaene J, Cherrah Y, Alaoui K, Vercammen J, Bouklouze A, Vander Heyden Y. Selected-ion flow-tube mass-spectrometry (SIFT-MS) fingerprinting versus chemical profiling for geographic traceability of Moroccan Argan oils. Food Chem. 2018;263:8–17. doi:10.1016/j.foodchem.2018.04.059.
    1. Rodriguez J, Neyrinck AM, Zhang Z, Seethaler B, Nazare JA, Robles Sanchez C, Roumain M, Muccioli GG, Bindels LB, Cani PD, et al. Metabolite profiling reveals the interaction of chitin-glucan with the gut microbiota. Gut Microbes. 2020;12:1810530. doi:10.1080/19490976.2020.1810530.

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe