Metabonomics of human fecal extracts characterize ulcerative colitis, Crohn’s disease and healthy individuals

Metabolomics

Volumn 11, Issue 1, 2015, Pages 122-133

  Bjerrum, Jacob Tveiten ^a,b   Wang, Yulan ^c,d   Hao, Fuhua ^c   Coskun, Mehmet ^b   Ludwig, Christian ^e   Günther, Ulrich ^e   Nielsen, Ole Haagen ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Wuhan National Laboratory for Optoelectronics   (China)

^d ZHEJIANG UNIVERSITY   (China)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Diagnostic tool; Dysbiosis; Inflammatory bowel disease; Metabolomics; NMR spectroscopy

Indexed keywords

EID: 84929073100     PISSN: 15733882     EISSN: 15733890     Source Type: Journal    
DOI: 10.1007/s11306-014-0677-3     Document Type: Article

References (64)

1. Ahmed, I., Greenwood, R., de Costello, B. L., Ratcliffe, N. M., & Probert, C. S. (2013). An investigation of fecal volatile organic metabolites in irritable bowel syndrome. PLoS One,8(3), e58204.
2. Balasubramanian, K., Kumar, S., Singh, R. R., et al. (2009). Metabolism of the colonic mucosa in patients with inflammatory bowel diseases: an in vitro proton magnetic resonance spectroscopy study. Magnetic Resonance Imaging,27(1), 79–86.
3. Baumgart, D. C., & Sandborn, W. J. (2012). Crohn’s disease. Lancet,380(9853), 1590–1605.
4. Bezabeh, T., Somorjai, R. L., & Smith, I. C. P. (2009). MR metabolomics of fecal extracts: applications in the study of bowel diseases. Magnetic Resonance in Chemistry,47(Suppl 1), S54–S61.
5. Bezabeh, T., Somorjai, R. L., Smith, I. C., Nikulin, A. E., Dolenko, B., & Bernstein, C. N. (2001). The use of 1H magnetic resonance spectroscopy in inflammatory bowel diseases: distinguishing ulcerative colitis from Crohn’s disease. American Journal of Gastroenterology,96(2), 442–448.
6. Bjerrum, J. T., Hansen, M., Olsen, J., & Nielsen, O. H. (2010a). Genome-wide gene expression analysis of mucosal colonic biopsies and isolated colonocytes suggests a continuous inflammatory state in the lamina propria of patients with quiescent ulcerative colitis. Inflammatory Bowel Diseases,16(6), 999–1007.
7. Bjerrum, J. T., Nielsen, O. H., Hao, F., et al. (2010b). Metabonomics in ulcerative colitis: diagnostics, biomarker identification, and insight into the pathophysiology. Journal of Proteome Research,9(2), 954–962.
8. Bjerrum, J. T., Nielsen, O. H., Wang, Y. L., & Olsen, J. (2008). Technology insight: metabonomics in gastroenterology-basic principles and potential clinical applications. Nat Clin Pract Gastroenterol Hepatol,5(6), 332–343.
9. Bjerrum, J. T., Nyberg, C., Olsen, J., & Nielsen, O. H. (2013). Assessment of the validity of a multi-gene analysis in the diagnostics of inflammatory bowel disease. Journal of Internal Medicine,275(5), 484–493.
10. Bjerrum, J. T., Rantalainen, M., Wang, Y., Olsen, J., & Nielsen, O. H. (2014). Integration of transcriptomics and metabonomics: Improving diagnostics, biomarker identification and phenotyping in ulcerative colitis. Metabolomics,10, 280–290.
11. Bylesjö, M., Rantalainen, M., Cloarec, O., Nicholson, J. K., Holmes, E., & Trygg, J. (2006). OPLS discriminant analysis: combining the strengths of PLS-DA and SIMCA classification. Journal of Chemometrics,20(8–10), 341–351.
12. Chapman, M. A., Grahn, M. F., Boyle, M. A., Hutton, M., Rogers, J., & Williams, N. S. (1994). Butyrate oxidation is impaired in the colonic mucosa of sufferers of quiescent ulcerative colitis. Gut,35(1), 73–76.
13. Cloarec, O., Dumas, M. E., Trygg, J., et al. (2005). Evaluation of the orthogonal projection on latent structure model limitations caused by chemical shift variability and improved visualization of biomarker changes in 1H NMR spectroscopic metabonomic studies. Analytical Chemistry,77(2), 517–526.
14. Dawiskiba, T., Deja, S., Mulak, A., et al. (2014). Serum and urine metabolomic fingerprinting in diagnostics of inflammatory bowel diseases. World Journal of Gastroenterology,20(1), 163–174.
15. De Preter, V., Bulteel, V., Suenaert, P., et al. (2009). Pouchitis, similar to active ulcerative colitis, is associated with impaired butyrate oxidation by intestinal mucosa. Inflammatory Bowel Diseases,15(3), 335–340.
16. De Preter, V., Rutgeerts, P., Schuit, F., Verbeke, K., & Arijs, I. (2013). Impaired expression of genes involved in the butyrate oxidation pathway in Crohn’s disease patients. Inflammatory Bowel Diseases,19(3), E43–E44.
17. Dong, F., Zhang, L., Hao, F., Tang, H., & Wang, Y. (2013). Systemic responses of mice to dextran sulfate sodium-induced acute ulcerative colitis using 1H NMR spectroscopy. Journal of Proteome Research,12(6), 2958–2966.
18. Duboc, H., Rajca, S., Rainteau, D., et al. (2013). Connecting dysbiosis, bile-acid dysmetabolism and gut inflammation in inflammatory bowel diseases. Gut,62(4), 531–539.
19. Duncan, S. H., Louis, P., & Flint, H. J. (2004). Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Applied and Environment Microbiology,70(10), 5810–5817.
20. ® models. Journal of Chemometrics,22(11–12), 594–600.
21. Etchevers, M. J., Aceituno, M., & Sans, M. (2008). Are we giving azathioprine too late? The case for early immunomodulation in inflammatory bowel disease. World Journal of Gastroenterology,14(36), 5512–5518.
22. Frank, D. N., St Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America,104(34), 13780–13785.
23. Garner, C. E., Smith, S., de Lacy Costello, B., et al. (2007). Volatile organic compounds from feces and their potential for diagnosis of gastrointestinal disease. FASEB Journal,21(8), 1675–1688.
24. Geboes, K., Colombel, J.-F., Greenstein, A., et al. (2008). Indeterminate colitis: A review of the concept—What’s in a name? Inflammatory Bowel Diseases,14(6), 850–857.
25. Harvey, R. F., & Bradshaw, J. M. (1980). A simple index of Crohn’s-disease activity. Lancet,1(8167), 514.
26. Hove, H., Nordgaard-Andersen, I., & Mortensen, P. B. (1994). Faecal DL-lactate concentration in 100 gastrointestinal patients. Scandinavian Journal of Gastroenterology,29(3), 255–259.
27. Jacobs, D. M., Deltimple, N., van Velzen, E., et al. (2008). (1)H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR in Biomedicine,21(6), 615–626.
28. Jansson, J., Willing, B., Lucio, M., et al. (2009). Metabolomics reveals metabolic biomarkers of Crohn’s disease. PLoS One,4(7), e6386.
29. Le Gall, G., Noor, S. O., Ridgway, K., et al. (2011). Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome. Journal of Proteome Research,10(9), 4208–4218.
30. Lin, H.-M., Edmunds, S. I., Helsby, N. A., Ferguson, L. R., & Rowan, D. D. (2009). Nontargeted urinary metabolite profiling of a mouse model of Crohn’s disease. Journal of Proteome Research,8(4), 2045–2057.
31. Marchesi, J. R., Holmes, E., Khan, F., et al. (2007). Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. Journal of Proteome Research,6(2), 546–551.
32. Martinez-Medina, M., Aldeguer, X., Gonzalez-Huix, F., Acero, D., & Garcia-Gil, L. J. (2006). Abnormal microbiota composition in the ileocolonic mucosa of Crohn’s disease patients as revealed by polymerase chain reaction-denaturing gradient gel electrophoresis. Inflammatory Bowel Diseases,12(12), 1136–1145.
33. Murdoch, T. B., Fu, H., MacFarlane, S., Sydora, B. C., Fedorak, R. N., & Slupsky, C. M. (2008). Urinary metabolic profiles of inflammatory bowel disease in interleukin-10 gene-deficient mice. Analytical Chemistry,80(14), 5524–5531.
34. Nikolaus, S., & Schreiber, S. (2007). Diagnostics of inflammatory bowel disease. Gastroenterology,133(5), 1670–1689.
35. Olsen, J., Gerds, T. A., Seidelin, J. B., et al. (2009). Diagnosis of ulcerative colitis before onset of inflammation by multivariate modeling of genome-wide gene expression data. Inflammatory Bowel Diseases,15(7), 1032–1038.
36. Ooi, M., Nishiumi, S., Yoshie, T., et al. (2011). GC/MS-based profiling of amino acids and TCA cycle-related molecules in ulcerative colitis. Inflammation Research,60(9), 831–840.
37. Ordás, I., Eckmann, L., Talamini, M., Baumgart, D. C., & Sandborn, W. J. (2012). Ulcerative colitis. Lancet,380(9853), 1606–1619.
38. Planell, N., Lozano, J. J., Mora-Buch, R., et al. (2013). Transcriptional analysis of the intestinal mucosa of patients with ulcerative colitis in remission reveals lasting epithelial cell alterations. Gut,62(7), 967–976.
39. Ricart, E., García-Bosch, O., Ordás, I., & Panés, J. (2008). Are we giving biologics too late? The case for early versus late use. World Journal of Gastroenterology,14(36), 5523–5527.
40. Saric, J., Wang, Y., Li, J., et al. (2008). Species variation in the fecal metabolome gives insight into differential gastrointestinal function. Journal of Proteome Research,7(1), 352–360.
41. Sartor, R. B. (2008). Microbial influences in inflammatory bowel diseases. Gastroenterology,134(2), 577–594.
42. Schicho, R., Nazyrova, A., Shaykhutdinov, R., Duggan, G., Vogel, H. J., & Storr, M. (2010). Quantitative metabolomic profiling of serum and urine in DSS-induced ulcerative colitis of mice by 1H NMR spectroscopy. Journal of Proteome Research,9(12), 6265–6273.
43. Schicho, R., Shaykhutdinov, R., Ngo, J., et al. (2012). Quantitative metabolomic profiling of serum, plasma, and urine by (1)H NMR spectroscopy discriminates between patients with inflammatory bowel disease and healthy individuals. Journal of Proteome Research,11(6), 3344–3357.
44. Schroeder, K. W., Tremaine, W. J., & Ilstrup, D. M. (1987). Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. New England Journal of Medicine,317(26), 1625–1629.
45. Segain, J. P., Raingeard de Blétière la, D., Bourreille, A., et al. (2000). Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut,47(3), 397–403.
46. Sipos, F., Galamb, O., Wichmann, B., et al. (2011). Peripheral blood based discrimination of ulcerative colitis and Crohn’s disease from non-IBD colitis by genome-wide gene expression profiling. Disease Markers,30(1), 1–17.
47. Sokol, H., Pigneur, B., Watterlot, L., et al. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proceedings of the National Academy of Sciences of the United States of America,105(43), 16731–16736.
48. Sokol, H., Seksik, P., Rigottier-Gois, L., et al. (2006). Specificities of the fecal microbiota in inflammatory bowel disease. Inflammatory Bowel Diseases,12(2), 106–111.
49. Stephens, N. S., Siffledeen, J., Su, X., Murdoch, T. B., Fedorak, R. N., & Slupsky, C. M. (2012). Urinary NMR metabolomic profiles discriminate inflammatory bowel disease from healthy. Journal of Crohn’s and Colitis,7(2), e42–e48.
50. Swidsinski, A., Loening-Baucke, V., & Herber, A. (2009). Mucosal flora in Crohn’s disease and ulcerative colitis - an overview. Journal of Physiology and Pharmacology,60(Suppl 6), 61–71.
51. Tedelind, S., Westberg, F., Kjerrulf, M., & Vidal, A. (2007). Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World Journal of Gastroenterology,13(20), 2826–2832.
52. Thibault, R., Blachier, F., Darcy-Vrillon, B., de Coppet, P., Bourreille, A., & Segain, J.-P. (2010). Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflammatory Bowel Diseases,16(4), 684–695.
53. Topping, D. L., & Clifton, P. M. (2001). Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiological Reviews,81(3), 1031–1064.
54. Trygg, J., & Wold, S. (2002). Orthogonal projections to latent structures (O-PLS). Journal of Chemometrics,16(3), 119–128.
55. Tso, V. K., Sydora, B. C., Foshaug, R. R., et al. (2013). Metabolomic profiles are gender, disease and time specific in the interleukin-10 gene-deficient mouse model of inflammatory bowel disease. PLoS One,8(7), e67654.
56. Vavricka, S. R., Spigaglia, S. M., Rogler, G., et al. (2012). Systematic evaluation of risk factors for diagnostic delay in inflammatory bowel disease. Inflammatory Bowel Diseases,18(3), 496–505.
57. Vermeiren, J., Van den Abbeele, P., Laukens, D., et al. (2012). Decreased colonization of fecal Clostridium coccoides/Eubacterium rectale species from ulcerative colitis patients in an in vitro dynamic gut model with mucin environment. FEMS Microbiology Ecology,79(3), 685–696.
58. Vernia, P., Caprilli, R., Latella, G., Barbetti, F., Magliocca, F. M., & Cittadini, M. (1988). Fecal lactate and ulcerative colitis. Gastroenterology,95(6), 1564–1568.
59. von Stein, P., Lofberg, R., Kuznetsov, N. V., et al. (2008). Multigene analysis can discriminate between ulcerative colitis, Crohn’s disease, and irritable bowel syndrome. Gastroenterology,134(7), 1869–1881.
60. Walton, C., Fowler, D. P., Turner, C., et al. (2013). Analysis of volatile organic compounds of bacterial origin in chronic gastrointestinal diseases. Inflammatory Bowel Diseases,19(10), 2069–2078.
61. Williams, H. R. T., Cox, I. J., Walker, D. G., et al. (2009). Characterization of inflammatory bowel disease with urinary metabolic profiling. American Journal of Gastroenterology,104(6), 1435–1444.
62. Williams, H. R. T., Willsmore, J. D., Cox, I. J., et al. (2012). Serum metabolic profiling in inflammatory bowel disease. Digestive Diseases and Sciences,57(8), 2157–2165.
63. Wu, F., Dassopoulos, T., Cope, L., et al. (2007). Genome-wide gene expression differences in Crohn’s disease and ulcerative colitis from endoscopic pinch biopsies: insights into distinctive pathogenesis. Inflammatory Bowel Diseases,13(7), 807–821.
64. Zhang, Y., Lin, L., Xu, Y., Lin, Y., Jin, Y., & Zheng, C. (2013). 1H NMR-based spectroscopy detects metabolic alterations in serum of patients with early-stage ulcerative colitis. Biochemical and Biophysical Research Communications,433(4), 547–551.