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Metabolomic Analysis in Inflammatory Bowel Disease: A Systematic Review
Abstract
Background and Aims: The inflammatory bowel diseases [IBD], Crohn’s disease and ulcerative colitis, are chronic, idiopathic gastrointestinal diseases. Although their precise aetiology is unknown, it is thought to involve a complex interaction between genetic predisposition and an abnormal host immune response to environmental exposures, probably microbial. Microbial dysbiosis has frequently been documented in IBD. Metabolomics [the study of small molecular intermediates and end products of metabolism in biological samples] provides a unique opportunity to characterize disease-associated metabolic changes and may be of particular use in quantifying gut microbial metabolism. Numerous metabolomic studies have been undertaken in IBD populations, identifying consistent alterations in a range of molecules across several biological matrices. This systematic review aims to summarize these findings. Methods: A comprehensive, systematic search was carried out using Medline and Embase. All studies were reviewed by two authors independently using predefined exclusion criteria. Sixty-four relevant papers were assessed for quality and included in the review. Results: Consistent metabolic perturbations were identified, including increases in levels of branched chain amino acids and lipid classes across stool, serum, plasma and tissue biopsy samples, and reduced levels of microbially modified metabolites in both urine [such as hippurate] and stool [such as secondary bile acids] samples. Conclusions: This review provides a summary of metabolomic research in IBD to date, highlighting underlying themes of perturbed gut microbial metabolism and mammalian–microbial co-metabolism associated with disease status.
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“BA metabolism is defective in patients with IBD, as indicated by increased levels of primary BAs (PBAs) and/or their conjugated forms, accompanied by decreased levels of second BAs (SBAs) (Lavelle and Sokol, 2020; Biagioli et al., 2021; Gallagher et al., 2021).”
From Bacteroides dorei BDX-01 alleviates DSS-induced experimental colitis in mice by regulating intestinal bile salt hydrolase activity and the FXR-NLRP3 signaling pathway (2023) · cites this paper as Gallagher et al., 2021
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Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859
Principal component analysis: A review and recent developments
Jolliffe, I. T., & Cadima, J. (2016) · Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rsta.2015.0202 · Cited by 10,117
den Besten, G., van Eunen, K., Groen, A. K., Venema, K., Reijngoud, D.-J., & Bakker, B. M. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r036012 · Cited by 5,048
Host-gut microbiota metabolic interactions
Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012) · Science · doi:10.1126/science.1223813 · Cited by 4,760
Self-citationWhiting, P., Rutjes, A. W., Reitsma, J. B., Bossuyt, P. M., & Kleijnen, J. (2003) · BMC Medical Research Methodology · doi:10.1186/1471-2288-3-25 · Cited by 3,592
Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases
Lloyd-Price, J., Arze, C., Ananthakrishnan, A. N., Schirmer, M., Avila-Pacheco, J., Poon, T. W., Andrews, E., Ajami, N. J., Bonham, K. S., Brislawn, C. J., et al. (2019) · Nature · doi:10.1038/s41586-019-1237-9 · Cited by 3,143
Gut microbiota functions: metabolism of nutrients and other food components
Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., & Tuohy, K. (2018) · European Journal of Nutrition · doi:10.1007/s00394-017-1445-8 · Cited by 2,878
Bile salt biotransformations by human intestinal bacteria
Ridlon, J. M., Kang, D.-J., & Hylemon, P. B. (2006) · Journal of Lipid Research · doi:10.1194/jlr.r500013-jlr200 · Cited by 2,829
Review article: the role of butyrate on colonic function
HAMER, H. M., JONKERS, D., VENEMA, K., VANHOUTVIN, S., TROOST, F. J., & BRUMMER, R. ‐. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2007.03562.x · Cited by 2,721
Short-chain fatty acids in control of body weight and insulin sensitivity
Canfora, E. E., Jocken, J. W., & Blaak, E. E. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.128 · Cited by 2,298
Diet–microbiota interactions as moderators of human metabolism
Sonnenburg, J. L., & Bäckhed, F. (2016) · Nature · doi:10.1038/nature18846 · Cited by 2,257
Nicholson, J. K., & Lindon, J. C. (2008) · Nature · doi:10.1038/4551054a · Cited by 1,931
Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., Ballet, V., Claes, K., Van Immerseel, F., Verbeke, K., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-304833 · Cited by 1,904
Bouatra, S., Aziat, F., Mandal, R., Guo, A. C., Wilson, M. R., Knox, C., Bjorndahl, T. C., Krishnamurthy, R., Saleem, F., Liu, P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073076 · Cited by 1,530
Eicosanoid storm in infection and inflammation
Dennis, E. A., & Norris, P. C. (2015) · Nature Reviews Immunology · doi:10.1038/nri3859 · Cited by 1,517
Gut microbiota in the pathogenesis of inflammatory bowel disease
Nishida, A., Inoüe, R., Inatomi, O., Bamba, S., Naito, Y., & Andoh, A. (2017) · Clinical Journal of Gastroenterology · doi:10.1007/s12328-017-0813-5 · Cited by 1,440
Multivariate Analysis in Metabolomics
Worley, B., & Powers, R. (2012) · Current Metabolomics · doi:10.2174/2213235x11301010092 · Cited by 1,425
Oliphant, K., & Allen-Vercoe, E. (2019) · Microbiome · doi:10.1186/s40168-019-0704-8 · Cited by 1,327
NMR Spectroscopy for Metabolomics Research
Emwas, A.-H. M., Roy, R., McKay, R. T., Tenori, L., Saccenti, E., Gowda, G. A. N., Raftery, D., Alahmari, F., Jaremko, Ł., Jaremko, M., et al. (2019) · Metabolites · doi:10.3390/metabo9070123 · Cited by 1,251
The first 1000 cultured species of the human gastrointestinal microbiota
Rajilić-Stojanović, M., & de Vos, W. M. (2014) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12075 · Cited by 1,182
The key role of anaplerosis and cataplerosis for citric acid cycle function
Owen, O. E., Kalhan, S. C., & Hanson, R. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.r200006200 · Cited by 1,172
Human metabolic phenotype diversity and its association with diet and blood pressure
Holmes, E., Loo, R. L., Stamler, J., Bictash, M., Yap, I. K. S., Chan, Q., Ebbels, T., De Iorio, M., Brown, I. J., Veselkov, K. A., et al. (2008) · Nature · doi:10.1038/nature06882 · Cited by 1,054
Self-citationHenke, M. T., Kenny, D. J., Cassilly, C. D., Vlamakis, H. C., Xavier, R. J., & Clardy, J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904099116 · Cited by 835
The gut microbiota and inflammatory bowel disease
Matsuoka, K., & Kanai, T. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-014-0454-4 · Cited by 804
Romano, K. A., Vivas, E. I., Amador-Noguez, D., & Rey, F. E. (2015) · mBio · doi:10.1128/mbio.02481-14 · Cited by 777
Holeček, M. (2018) · Nutrition & Metabolism · doi:10.1186/s12986-018-0271-1 · Cited by 773
Khan, I., Ullah, N., Zha, L., Bai, Y., Khan, A., Zhao, T., Che, T., & Zhang, C. (2019) · Pathogens · doi:10.3390/pathogens8030126 · Cited by 771
Tremaroli, V., Karlsson, F., Werling, M., Ståhlman, M., Kovatcheva-Datchary, P., Olbers, T., Fändriks, L., le Roux, C. W., Nielsen, J., & Bäckhed, F. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.07.009 · Cited by 757
Metabolomics-based methods for early disease diagnostics
Gowda, G. A. N., Zhang, S., Gu, H., Asiago, V. M., Shanaiah, N., & Raftery, D. (2008) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.8.5.617 · Cited by 705
Metabolomics: A Global Biochemical Approach to Drug Response and Disease
Kaddurah‐Daouk, R., Kristal, B. S., & Weinshilboum, R. M. (2008) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.48.113006.094715 · Cited by 685
Zhou, B., Xiao, J. F., Tuli, L., & Ressom, H. W. (2011) · Molecular BioSystems · doi:10.1039/c1mb05350g · Cited by 677
Arachidonic acid: Physiological roles and potential health benefits – A review
Tallima, H., & El Ridi, R. (2018) · Journal of Advanced Research · doi:10.1016/j.jare.2017.11.004 · Cited by 671
Gut microbiome and aging: physiological and mechanistic insights
Nagpal, R., Mainali, R., Ahmadi, S., Wang, S., Singh, R., Kavanagh, K., Kitzman, D. W., Kushugulova, A., Marotta, F., & Yadav, H. (2018) · Nutrition and Healthy Aging · doi:10.3233/nha-170030 · Cited by 670
Rapid and Noninvasive Metabonomic Characterization of Inflammatory Bowel Disease
Marchesi, J. R., Holmes, E. C., Khan, F. M. A., Kochhar, S., Scanlan, P. D., Shanahan, F., Wilson, I. D., & Wang, Y. (2007) · Journal of Proteome Research · doi:10.1021/pr060470d · Cited by 632
Self-citationIncreased Tryptophan Metabolism Is Associated With Activity of Inflammatory Bowel Diseases
Nikolaus, S., Schulte, B., Al-Massad, N., Thieme, F., Schulte, D. M., Bethge, J., Rehman, A., Tran, F., Aden, K., Häsler, R., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.08.028 · Cited by 625
Frank, D. N., Robertson, C. E., Hamm, C. M., Kpadeh, Z. Z., Zhang, T., Chen, H., Zhu, W., Sartor, R. B., Boedeker, E. C., Harpaz, N., et al. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21339 · Cited by 612
Development of a gut microbe–targeted nonlethal therapeutic to inhibit thrombosis potential
Roberts, A. B., Gu, X., Buffa, J. A., Hurd, A. G., Wang, Z., Zhu, W., Gupta, N., Skye, S. M., Cody, D. B., Levison, B. S., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0128-1 · Cited by 552
Inflammatory bowel disease: clinical aspects and treatments
Fakhoury, M., Al‐Salami, H., Negrulj, R., & Mooranian, A. (2014) · Journal of Inflammation Research · doi:10.2147/jir.s65979 · Cited by 539
Metabolomics Reveals Metabolic Biomarkers of Crohn's Disease
Jansson, J. K., Willing, B. P., Lucio, M., Fekete, A., Dicksved, J., Halfvarson, J., Tysk, C., & Schmitt‐Kopplin, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006386 · Cited by 529
Multivariate Analysis in Metabolomics
Worley, B., & Powers, R. (2012) · Current Metabolomics · doi:10.2174/2213235x130108 · Cited by 524
Wang, W., Chen, L., Zhou, R., Wang, X., Song, L., Huang, S., Wang, G., & Xia, B. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.01500-13 · Cited by 509
Bile acid nuclear receptor FXR and digestive system diseases
Ding, L., Yang, L., Wang, Z., & Huang, W. (2015) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2015.01.004 · Cited by 477
Geirnaert, A., Calatayud, M., Grootaert, C., Laukens, D., Devriese, S., Smagghe, G. J., Vos, M. D., Boon, N., & de Wiele, T. V. (2017) · Scientific Reports · doi:10.1038/s41598-017-11734-8 · Cited by 452
Microbiome–metabolome reveals the contribution of gut–kidney axis on kidney disease
Chen, Y., Chen, D., Chen, L., Liu, J., Vaziri, N. D., Guo, Y. P., & Zhao, Y. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-018-1756-4 · Cited by 430
Said, H. S., Suda, W., Nakagome, S., Chinen, H., Oshima, K., Kim, S., Kimura, R., Iraha, A., Ishida, H., Fujita, J., et al. (2013) · DNA Research · doi:10.1093/dnares/dst037 · Cited by 394
The Roles of Glutamine in the Intestine and Its Implication in Intestinal Diseases
Kim, M., & Kim, H. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18051051 · Cited by 379
Escherichia coli Pathobionts Associated with Inflammatory Bowel Disease
Mirsepasi‐Lauridsen, H. C., Vallance, B. A., Krogfelt, K. A., & Petersen, A. M. (2019) · Clinical Microbiology Reviews · doi:10.1128/cmr.00060-18 · Cited by 374
Colorectal cancer in inflammatory bowel disease: The risk, pathogenesis, prevention and diagnosis
Kim, E. R. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i29.9872 · Cited by 357
Hughes, E. R., Winter, M. G., Duerkop, B. A., Spiga, L., Furtado de Carvalho, T., Zhu, W., Gillis, C. C., Büttner, L., Smoot, M. P., Behrendt, C. L., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.01.005 · Cited by 353
Gorrochategui, E., Jaumot, J., Lacorte, S., & Tauler, R. (2016) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2016.07.004 · Cited by 352
Le Gall, G., Noor, S. O., Ridgway, K., Scovell, L., Jamieson, C., Johnson, I. T., Colquhoun, I. J., Kemsley, E. K., & Narbad, A. (2011) · Journal of Proteome Research · doi:10.1021/pr2003598 · Cited by 348
The Essential Role of Tick Salivary Glands and Saliva in Tick Feeding and Pathogen Transmission
Šimo, L., Kazimírová, M., Richardson, J. P., & Bonnet, S. I. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00281 · Cited by 341
Hippurate: The Natural History of a Mammalian–Microbial Cometabolite
Lees, H., Swann, J. R., Wilson, I. D., Nicholson, J. K., & Holmes, E. C. (2013) · Journal of Proteome Research · doi:10.1021/pr300900b · Cited by 338
Self-citationAcylcarnitines activate proinflammatory signaling pathways
Rutkowsky, J. M., Knotts, T. A., Ono‐Moore, K. D., McCoin, C. S., Huang, S., Schneider, D. A., Singh, S., Adams, S. H., & Hwang, D. H. (2014) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00656.2013 · Cited by 333
The Role of Succinate in the Regulation of Intestinal Inflammation
Connors, J., Dawe, N., & Limbergen, J. V. (2018) · Nutrients · doi:10.3390/nu11010025 · Cited by 331
Tryptophan Metabolism by Gut Microbiome and Gut-Brain-Axis: An in silico Analysis
Kaur, H., Bose, C., & Mande, S. S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01365 · Cited by 331
Pallister, T., Jackson, M. A., Martin, T. C., Zierer, J., Jennings, A., Mohney, R. P., MacGregor, A. J., Steves, C. J., Cassidy, A., Spector, T. D., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-13722-4 · Cited by 315
STATISTICAL METHODS FOR THE ANALYSIS OF HIGH-THROUGHPUT METABOLOMICS DATA
Bartel, J., Krumsiek, J., & Theis, F. J. (2013) · Computational and Structural Biotechnology Journal · doi:10.5936/csbj.201301009 · Cited by 307
Sulfide as a Mucus Barrier-Breaker in Inflammatory Bowel Disease?
Ijssennagger, N., van der Meer, R., & van Mil, S. W. C. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.01.002 · Cited by 300
Ma, N., & Ma, X. (2018) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12401 · Cited by 285
Sookoian, S. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i29.3775 · Cited by 281
The Paneth Cell: The Curator and Defender of the Immature Small Intestine
Lueschow, S. R., & McElroy, S. J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00587 · Cited by 280
Aden, K., Rehman, A., Waschina, S., Pan, W.-H., Walker, A., Lucio, M., Nunez, A. M., Bharti, R., Zimmerman, J., Bethge, J., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.07.025 · Cited by 266
Schicho, R., Shaykhutdinov, R. A., Ngo, J., Nazyrova, A., Schneider, C., Panaccione, R., Kaplan, G. G., Vogel, H. J., & Storr, M. (2012) · Journal of Proteome Research · doi:10.1021/pr300139q · Cited by 248
Effects of the intestinal microbial metabolite butyrate on the development of colorectal cancer
Wu, X., Wu, Y., He, L., Wu, L., Wang, X., & Liu, Z. (2018) · Journal of Cancer · doi:10.7150/jca.25324 · Cited by 247
Bjerrum, J. T., Wang, Y., Hao, F., Coskun, M., Ludwig, C., Günther, U. L., & Nielsen, O. H. (2014) · Metabolomics · doi:10.1007/s11306-014-0677-3 · Cited by 241
Faecal metabolite profiling identifies medium-chain fatty acids as discriminating compounds in IBD
Preter, V. D., Machiels, K., Joossens, M., Arijs, I., Matthys, C., Vermeire, S., Rutgeerts, P. J., & Verbeke, K. (2014) · Gut · doi:10.1136/gutjnl-2013-306423 · Cited by 238
Intestinal Bacteria Interplay With Bile and Cholesterol Metabolism: Implications on Host Physiology
Molinero, N., Ruíz, L., Sánchez, B., Margollés, A., & Delgado, S. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00185 · Cited by 233
Seganfredo, F. B., Blume, C. A., Moehlecke, M., Giongo, A., Casagrande, D. S., Spolidoro, J. V. N., Padoin, A. V., Schaan, B. D., & Mottin, C. C. (2017) · Obesity Reviews · doi:10.1111/obr.12541 · Cited by 228
López‐Siles, M., Enrich-Capó, N., Aldeguer, X., Sàbat, M., Duncan, S. H., Garcia-Gil, L. J., & Martínez-Medina, M. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00281 · Cited by 222
The metabolomic window into hepatobiliary disease
Beyoğlu, D., & Idle, J. R. (2013) · Journal of Hepatology · doi:10.1016/j.jhep.2013.05.030 · Cited by 219
Urinary metabolic signatures of human adiposity
Elliott, P., Posma, J. M., Chan, Q. M., García‐Pérez, I., Wijeyesekera, A., Bictash, M., Ebbels, T. M. D., Ueshima, H., Zhao, L., Horn, L. V., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa5680 · Cited by 211
Self-citationHyperketonemia and ketosis increase the risk of complications in type 1 diabetes
Marie, P. K., & Jain, S. K. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.020 · Cited by 207
Scoville, E., Allaman, M. M., Brown, C. T., Motley, A. K., Horst, S., Williams, C. S., Koyama, T., Zhao, Z., Adams, D. W., Beaulieu, D. B., et al. (2017) · Metabolomics · doi:10.1007/s11306-017-1311-y · Cited by 205
Metabolomics for the masses: The future of metabolomics in a personalized world
Trivedi, D. K., Hollywood, K. A., & Goodacre, R. (2017) · European Journal of Molecular & Clinical Medicine · doi:10.1016/j.nhtm.2017.06.001 · Cited by 201
Metabolomics of Human Brain Aging and Age-Related Neurodegenerative Diseases
Jové, M., Portero-Otín, M., Naudí, A., Ferrer, I., & Pamplona, R. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000091 · Cited by 195
Myo-Inositol and Its Derivatives: Their Emerging Role in the Treatment of Human Diseases
Chhetri, D. R. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01172 · Cited by 195
Characterization of Inflammatory Bowel Disease With Urinary Metabolic Profiling
Williams, H. R. T., Cox, I. J., Walker, D. G., North, B. V., Patel, V. M., Marshall, S. E., Jewell, D. P., Ghosh, S. K., Thomas, H. J. W., TEARE, J. P., et al. (2009) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.175 · Cited by 187
Self-citationHost-microbial Cross-talk in Inflammatory Bowel Disease
Nagao‐Kitamoto, H., & Kamada, N. (2017) · Immune Network · doi:10.4110/in.2017.17.1.1 · Cited by 185
Serum and urine metabolomic fingerprinting in diagnostics of inflammatory bowel diseases
Dawiskiba, T. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i1.163 · Cited by 182
Perna, S., Alalwan, T. A., Alaali, Z., Alnashaba, T., Gasparri, C., Infantino, V., Hammad, L., Riva, A., Petrangolini, G., Allegrini, P., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205232 · Cited by 181
Ocvirk, S., & O’Keefe, S. J. (2017) · Current Nutrition Reports · doi:10.1007/s13668-017-0219-5 · Cited by 179
GC/MS-based profiling of amino acids and TCA cycle-related molecules in ulcerative colitis
Ooi, M., Nishiumi, S., Yoshie, T., Shiomi, Y., Kohashi, M., Fukunaga, K., Nakamura, S., Matsumoto, T., Hatano, N., Shinohara, M., et al. (2011) · Inflammation Research · doi:10.1007/s00011-011-0340-7 · Cited by 173
The Role of Dietary Nutrients in Inflammatory Bowel Disease
Sugihara, K., Morhardt, T. L., & Kamada, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2018.03183 · Cited by 172
Human Metabolic Phenotypes Link Directly to Specific Dietary Preferences in Healthy Individuals
Rezzi, S., Ramadan, Z., Martin, F., Fay, L. B., van Bladeren, P., Lindon, J. C., Nicholson, J. K., & Kochhar, S. (2007) · Journal of Proteome Research · doi:10.1021/pr070431h · Cited by 165
Gut microbiome and metabolic diseases
Fukuda, S., & Ohno, H. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0399-z · Cited by 156
Bjerrum, J. T., Nielsen, O. H., Hao, F., Tang, H., Nicholson, J. K., Wang, Y., & Olsen, J. (2009) · Journal of Proteome Research · doi:10.1021/pr9008223 · Cited by 153
Determinants of the urinary and serum metabolome in children from six European populations
Lau, C. E., Siskos, A., Maître, L., Robinson, O., Athersuch, T. J., Want, E. J., Urquiza, J., Casas, M., Vafeiadi, M., Roumeliotaki, T., et al. (2018) · BMC Medicine · doi:10.1186/s12916-018-1190-8 · Cited by 153
Dark matter in host-microbiome metabolomics: Tackling the unknowns–A review
Peisl, B. Y. L., Schymanski, E., & Wilmes, P. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2017.12.034 · Cited by 152
Correlation of diet, microbiota and metabolite networks in inflammatory bowel disease
Yi, W., Gan, H. Y., Li, X., Huang, Y., Li, Z. C., Deng, H., Chen, S. Z., Zhou, Y. J., Wang, L. S., Han, Y. P., et al. (2019) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12795 · Cited by 148
Ahmed, I., Greenwood, R., Costello, B. D. L., Ratcliffe, N. A., & Probert, C. S. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13522 · Cited by 146
Sofia, M. A., Ciorba, M. A., Meckel, K. R., Lim, C. K., Guillemin, G. J., Weber, C. R., Bissonnette, M., & Pekow, J. R. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy103 · Cited by 145
Xun, Z., Zhang, Q., Xu, T., Chen, N., & Chen, F. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01136 · Cited by 139
Potential TMA-Producing Bacteria Are Ubiquitously Found in Mammalia
Rath, S., Rud, T., Pieper, D. H., & Vital, M. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02966 · Cited by 134
Urine metabolome profiling of immune-mediated inflammatory diseases
Alonso, A., Julià, A., Vinaixa, M., Domènech, E., Fernández‐Nebro, A., Cañete, J. D. D., Ferrándiz, C., Tornero, J., Gisbert, J. P., Nos, P., et al. (2016) · BMC Medicine · doi:10.1186/s12916-016-0681-8 · Cited by 132
Urinary NMR metabolomic profiles discriminate inflammatory bowel disease from healthy
Stephens, N. S., Siffledeen, J. S., Su, X., Murdoch, T. B., Fedorak, R. N., & Slupsky, C. M. (2012) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2012.04.019 · Cited by 125
Williams, H. R. T., Cox, I. J., Walker, D. G., Cobbold, J., Taylor-Robinson, S. D., Marshall, S. E., & Orchard, T. R. (2010) · BMC Gastroenterology · doi:10.1186/1471-230x-10-108 · Cited by 121
Self-citationSerum Metabolic Profiling in Inflammatory Bowel Disease
Williams, H. R. T., Willsmore, J., Cox, I. J., Walker, D. G., Cobbold, J., Taylor-Robinson, S. D., & Orchard, T. R. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2127-2 · Cited by 112
Self-citationPreter, V. D., Joossens, M., Ballet, V., Shkedy, Z., Rutgeerts, P. J., Vermeire, S., & Verbeke, K. (2013) · Clinical and Translational Gastroenterology · doi:10.1038/ctg.2012.24 · Cited by 109
Whiley, L., Nye, L. C., Grant, I., Andreas, N., Chappell, K. E., Sarafian, M. H., Misra, R., Plumb, R. S., Lewis, M. R., Nicholson, J. K., et al. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.8b05884 · Cited by 103
Self-citationBalasubramanian, K., Kumar, S., Singh, R. R., Sharma, U., Ahuja, V., Makharia, G. K., & Jagannathan, N. R. (2008) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2008.05.014 · Cited by 102
Lumbreras, B., Porta, M. S., Márquez, S., Pollán, M., Parker, L. A., & Hernández‐Aguado, I. (2008) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2008.06.018 · Cited by 101
Trimethylamine-N-oxide: A Novel Biomarker for the Identification of Inflammatory Bowel Disease
Wilson, A. S., Teft, W. A., Morse, B. L., Choi, Y., Woolsey, S., DeGorter, M. K., Hegele, R. A., Tirona, R. G., & Kim, R. B. (2015) · Digestive Diseases and Sciences · doi:10.1007/s10620-015-3797-3 · Cited by 97
Inflammatory bowel disease: An increased risk factor for neurologic complications
Morís, G. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i5.1228 · Cited by 97
Diab, J., Hansen, T., Goll, R., Stenlund, H. C., Ahnlund, M., Jensen, E., Möritz, T., Florholmen, J., & Forsdahl, G. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izz098 · Cited by 95
Qi, Y., Zang, S., Wei, J., Yu, H.-C., Yang, Z., Wu, H., Kang, Y., Tao, H., Yang, M., Jin, L., et al. (2020) · Genomics · doi:10.1016/j.ygeno.2020.09.063 · Cited by 88
Shores, D. R., Binion, D. G., Freeman, B. Α., & Baker, P. R. S. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21560 · Cited by 87
Metabolomics in cardiovascular diseases
Kordalewska, M., & Markuszewski, M. J. (2015) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2015.04.021 · Cited by 85
Lai, Y., Xue, J., Liu, C., Gao, B., Chi, L., Tu, P., Lü, K., & Ru, H. (2019) · Molecules · doi:10.3390/molecules24030449 · Cited by 81
Masoodi, M., Pearl, D. S., Eiden, M. J., Shute, J. K., Brown, J. F., Calder, P. C., & Trebble, T. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076532 · Cited by 79
Analysis of Exhaled Breath Volatile Organic Compounds in Inflammatory Bowel Disease: A Pilot Study
Hicks, L., Huang, J., Kumar, S., Powles, S., Orchard, T. R., Hanna, G. B., & Williams, H. R. T. (2015) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjv102 · Cited by 78
Self-citationPurine, Kynurenine, Neopterin and Lipid Peroxidation Levels in Inflammatory Bowel Disease
Forrest, C. M., Youd, P. L., Kennedy, A., Gould, S. R., Darlington, L. G., & Stone, T. W. (2002) · Journal of Biomedical Science · doi:10.1007/bf02256538 · Cited by 77
Tiele, A., Wicaksono, A. N., Kansara, J., Arasaradnam, R. P., & Covington, J. A. (2019) · Biosensors · doi:10.3390/bios9020055 · Cited by 77
Impact of Paneth Cell Autophagy on Inflammatory Bowel Disease
Wang, S., Shao, B., Zhao, S., Fang, J., Gu, L., Miao, C., Li, Z., & Bai, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00693 · Cited by 72
Dryahina, K., Španěl, P., Pospíšilová, V., Sovová, K., Hrdlička, L., Machková, N., Lukáš, M., & Smith, D. C. (2013) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.6660 · Cited by 71
Peng, J.-S. (2011) · Oncology Reports · doi:10.3892/or.2011.1302 · Cited by 68
Murakami, M., Iwamoto, J., Honda, A., Tsuji, T., Tamamushi, M., Ueda, H., Monma, T., Konishi, N., Yara, S., Hirayama, T. T., et al. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy022 · Cited by 67
Lipidomic Profiling in Inflammatory Bowel Disease
Fan, F., Mundra, P. A., Lu, F. Y., Galvin, A., Moore, X. L., Weir, J. M., Wong, G., White, D. A., Chin-Dusting, J. P. F., Sparrow, M., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000394 · Cited by 65
Author Correction: Gut microbiome structure and metabolic activity in inflammatory bowel disease
Franzosa, E. A., Sirota‐Madi, A., Ávila-Pacheco, J., Fornelos, N., Haiser, H. J., Reinker, S., Vatanen, T., Hall, A. B., Mallick, H., McIver, L. J., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-019-0442-5 · Cited by 65
Dryahina, K., Smith, D. C., Bortlík, M., Machková, N., Lukáš, M., & Španěl, P. (2017) · Journal of Breath Research · doi:10.1088/1752-7163/aa8468 · Cited by 64
Browning, M. G., Pessoa, B. M., Khoraki, J., & Campos, G. M. (2019) · Current Obesity Reports · doi:10.1007/s13679-019-00334-4 · Cited by 64
Volatile Organic Compounds in Exhaled Air as Novel Marker for Disease Activity in Crohnʼs Disease
Bodelier, A. G. L., Smolinska, A., Baranska, A., Dallinga, J. W., Mujagic, Z., Vanhees, K., van den Heuvel, T. R. A., Masclee, A., Jonkers, D. M. A. E., Pierik, M. J., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000436 · Cited by 62
Using metabolomic analysis to understand inflammatory bowel diseases
Lin, H., Helsby, N. A., Rowan, D. D., & Ferguson, L. R. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21426 · Cited by 61
Hisamatsu, T., Ono, N., Imaizumi, A., Mori, M., Suzuki, H., Uo, M., Hashimoto, M., Naganuma, M., Matsuoka, K., Mizuno, S., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0140716 · Cited by 60
Urinary leukotriene E4 excretion: A biomarker of inflammatory bowel disease activity
Stanke‐Labesque, F., Pofelski, J., Moreau–Gaudry, A., Bessard, G., & Bonaz, B. L. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20403 · Cited by 59
Murgia, A., Hinz, C., Liggi, S., Dénes, J., Hall, Z., West, J. A., Santoru, M. L., Piras, C., Manis, C., Usai, P., et al. (2018) · Metabolomics · doi:10.1007/s11306-018-1439-4 · Cited by 59
Self-citationTryptophan, Neurodegeneration and HIV-Associated Neurocognitive Disorder
Davies, N. W. S., Guillemin, G. J., & Brew, B. J. (2010) · International Journal of Tryptophan Research · doi:10.4137/ijtr.s4321 · Cited by 57
Probert, F., Walsh, A. J., Jagielowicz, M., Yeo, T., Claridge, T. D. W., Simmons, A., Travis, S. P. L., & Anthony, D. C. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy101 · Cited by 57
Ghonimy, A., Zhang, D., Farouk, M. H., & Wang, Q. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041008 · Cited by 53
Smolinska, A., Bodelier, A. G. L., Dallinga, J. W., Masclee, A., Jonkers, D. M. A. E., van Schooten, F., & Pierik, M. J. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14004 · Cited by 51
Combined Signature of the Fecal Microbiome and Plasma Metabolome in Patients with Ulcerative Colitis
Sun, M., Du, B., Shi, Y., Lu, Y., Zhou, Y. Y., & Liu, B.-R. (2019) · Medical Science Monitor · doi:10.12659/msm.916009 · Cited by 51
Bjerrum, J. T., Steenholdt, C., Ainsworth, M. A., Nielsen, O. H., Reed, M. A. C., Atkins, K. L., Günther, U. L., Hao, F., & Wang, Y. (2017) · BMC Medicine · doi:10.1186/s12916-017-0949-7 · Cited by 50
Diab, J., Hansen, T., Goll, R., Stenlund, H. C., Jensen, E., Möritz, T., Florholmen, J., & Forsdahl, G. (2019) · Metabolites · doi:10.3390/metabo9120291 · Cited by 48
Zhang, Y., Lin, L., Xu, Y., Lin, Y., Yu, J. H., & Zheng, C.-Q. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.03.012 · Cited by 47
Increased urinary F2-isoprostanes in patients with Crohn's disease
Cracowski, J., Bonaz, B. L., Bessard, G., Bessard, J., Anglade, C., & Fournet, J. (2002) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2002.05427.x · Cited by 45
Sharma, U., Singh, R. R., Ahuja, V., Makharia, G. K., & Jagannathan, N. R. (2010) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2010.03.039 · Cited by 44
The Lipid Status in Patients with Ulcerative Colitis: Sphingolipids are Disease-Dependent Regulated
Bazarganipour, S., Hausmann, J., Oertel, S., El-Hindi, K., Brachtendorf, S., Blumenstein, I., Kubesch, A., Sprinzl, K., Birod, K., Hahnefeld, L., et al. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8070971 · Cited by 43
Dudzińska, E., Szymona, K., Kloc, R., Gil-Kulik, P., Kocki, T., Świstowska, M., Bogucki, J., Kocki, J., & Urbańska, E. M. (2019) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284819881304 · Cited by 43
Bile Acid Malabsorption Deactivates Pregnane X Receptor in Patients with Crohn’s Disease
Iwamoto, J., Saito, Y., Honda, A., Miyazaki, T., Ikegami, T., & Matsuzaki, Y. (2013) · Inflammatory Bowel Diseases · doi:10.1097/mib.0b013e318281f423 · Cited by 40
Keshteli, A. H., van den Brand, F. F., Madsen, K. L., Mandal, R., Valcheva, R. S., Kroeker, K. I., Han, B., Bell, R. C., Cole, J. L., Hoevers, T., et al. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i21.3890 · Cited by 39
Keshteli, A. H., Tso, R., Dieleman, L. A., Park, H., Kroeker, K. I., Jovel, J., Gillevet, P. M., Sikaroodi, M., Mandal, R., Fedorak, R. N., et al. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izx070 · Cited by 39
Giovanni, N. D., Meuwis, M., Louis, E. J., & Focant, J. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00535 · Cited by 38
Kohashi, M., Nishiumi, S., Ooi, M., Yoshie, T., Matsubara, A., Suzuki, M., Hoshi, N., Kamikozuru, K., Yokoyama, Y., Fukunaga, K., et al. (2014) · Journal of Crohn s and Colitis · doi:10.1016/j.crohns.2014.01.024 · Cited by 34
Manfredi, M., Conte, E., Barberis, E., Buzzi, A., Robotti, E., Caneparo, V., Cecconi, D., Brandi, J., Vanni, E., Finocchiaro, M., et al. (2018) · Journal of Proteomics · doi:10.1016/j.jprot.2018.10.017 · Cited by 32
Schugar, R. C., Willard, B. B., Wang, Z., & Brown, J. M. (2017) · Adipocyte · doi:10.1080/21623945.2017.1398295 · Cited by 31
The potential of metabolic and lipid profiling in inflammatory bowel diseases: a pilot study
Tefas, C., Ciobanu, L., Tantau, M. V., Moraru, C., & Socaciu, C. (2019) · Bosnian Journal of Basic Medical Sciences · doi:10.17305/bjbms.2019.4235 · Cited by 29
Piešťanský, J., Olešová, D., Galba, J., Maráková, K., Parrák, V., Sečník, P., Sečník, P., Kováčech, B., Kováč, A., Zelinková, Z., et al. (2019) · Molecules · doi:10.3390/molecules24183345 · Cited by 29
1 H NMR based metabolic profiling in Crohn's disease by random forest methodology
Fathi, F., Kasmaee, L. M., Mani‐Varnosfaderani, A., Kyani, A., Rostami‐Nejad, M., Sohrabzadeh, K., Naderi, N., Zali, M. R., Rezaei–Tavirani, M., Tafazzoli, M., et al. (2014) · Magnetic Resonance in Chemistry · doi:10.1002/mrc.4074 · Cited by 27
Bene, J., Komlósi, K., Magyari, L., Talián, G. C., Horváth, K., Gasztonyi, B., Miheller, P., Figler, M., Mózsik, G., Tulassay, Z., et al. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507705020 · Cited by 27
Mojtahed, A., & Gee, M. S. (2018) · Pediatric Radiology · doi:10.1007/s00247-018-4107-y · Cited by 25
Serum Bile Acids Profiling in Inflammatory Bowel Disease Patients Treated with Anti-TNFs
Roda, G., Porru, E., Katsanos, K. H., Skamnelos, A., Kyriakidi, K., Fiorino, G., Christodoulou, D. K., Danese, S., & Roda, A. (2019) · Cells · doi:10.3390/cells8080817 · Cited by 25
Outcome after surgical resection of intraductal papillary and mucinous tumors of the pancreas.
Cuillerier, E., Cellier, C., Palazzo, L., Devière, J., Wind, P., Rickaert, F., Cugnenc, P., Cremer, M., & Barbier, J. P. (2000) · Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) · doi:10.1016/s0002-9270 · Cited by 22
Rantalainen, M., Bjerrum, J. T., Olsen, J., Nielsen, O. H., & Wang, Y. (2014) · Journal of Proteome Research · doi:10.1021/pr500699h · Cited by 17
Yau, Y. Y., Leong, R. W. L., Shin, S., Bustamante, S., Pickford, R., Hejazi, L., Campbell, B., & Wasinger, V. C. (2014) · PubMed · Cited by 15
Wang, C., Shi, J., Sun, B., Liu, D., Li, P., Gong, Y., He, Y., Liu, S., Xu, G., Li, J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044940 · Cited by 7
Alothaim, I., Gaya, D. R., & Watson, D. G. (2017) · Current Metabolomics · doi:10.2174/2213235x05666170424163105 · Cited by 6
Research works printed but not linked: 2
- Qi, 2020, High, Genomics
- Machiels, 2014, A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis, Gut, 63, 1275, 10.1136/gutjnl-2013-304833 · DOI · Paper page
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Dysbiosis in Inflammatory Bowel Disease: Pathogenic Role and Potential Therapeutic Targets
Santana, P. T., Rosas, S. L. B., Ribeiro, B. E., Marinho, Y., & de Souza, H. S. P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073464 · Cited by 359
Ning, L., Zhou, Y., Sun, H. L., Zhang, Y., Shen, C., Wang, Z., Xuan, B., Zhao, Y., Ma, Y., Yan, Y., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42788-0 · Cited by 334
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Metadata
- Authors
- Gallagher, K., Catesson, A., Griffin, J. L., Holmes, E., & Williams, H. R. T.
- Affiliations
- Imperial College London (GB)
- Murdoch University (AU)
- Imperial College Healthcare NHS Trust (GB)
- Corresponding author
- Gallagher, Kate
- Venue
- Journal of Crohn's and Colitis
- Publisher
- Oxford University Press (OUP)
- Published
- 2020-11-11
- Volume
- 15
- Issue
- 5
- Pages
- 813-826
- ISSN
- 1873-9946 (ISSN-L)
- 1876-4479
- OpenAlex
- W3102377839
- Cited by
- 133
- References
- 155
- Citations by year
- 2026: 18 · 2025: 27 · 2024: 29 · 2023: 27 · 2022: 20 · 2021: 12
- FWCI
- 1.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Journal of Crohn s and Colitis (publishedVersion)
- PubMed (publishedVersion)
- Murdoch University Research Portal (submittedVersion)
- Spiral (Imperial College London) (submittedVersion)
- Funders
- National Institute for Health Research Imperial Biomedical Research Centre
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- inflammatory bowel disease, Crohn's disease
- MeSH terms
- Gastrointestinal Microbiome, Humans, Inflammatory Bowel Diseases, Metabolomics, Dysbiosis
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