Skip to main content
Erschienen in: Digestive Diseases and Sciences 8/2012

01.08.2012 | Original Article

Serum Metabolic Profiling in Inflammatory Bowel Disease

verfasst von: Horace R. T. Williams, James D. Willsmore, I. Jane Cox, David G. Walker, Jeremy F. L. Cobbold, Simon D. Taylor-Robinson, Timothy R. Orchard

Erschienen in: Digestive Diseases and Sciences | Ausgabe 8/2012

Einloggen, um Zugang zu erhalten

Abstract

Background

The inflammatory bowel diseases (IBD), Crohn’s disease (CD), and ulcerative colitis (UC), are chronic inflammatory conditions of the gastrointestinal tract whose pathogenesis is not completely understood. 1H nuclear magnetic resonance (NMR) spectroscopy of serum generates comprehensive metabolic profiles, reflecting systemic metabolism, which may be altered in disease states.

Aim

The aim of this study was to use 1H NMR-based serum metabolic profiling in the investigation of CD patients, UC patients, and controls, potentially to provide insights into disordered metabolism in IBD, and into underlying mechanisms of disease.

Methods

Serum metabolic profiles were acquired from 67 individuals (24 CD patients, 20 UC patients, and 23 healthy controls). The multivariate pattern-recognition techniques of principal components analysis (PCA) and partial least squares discriminant analysis with orthogonal signal correction (OSC-PLS-DA) were used to investigate differences between cohorts.

Results

OSC-PLS-DA distinguished CD and UC cohorts with significant predictive accuracy, highlighting differences in lipid and choline metabolism. Metabolic profiles of both CD and UC cohorts, and the combined IBD cohort, differed significantly from controls: metabolites of importance in the OSC-PLS-DA models included lipoproteins (especially HDL cholesterol), choline, N-acetylglycoprotein, and amino acids.

Conclusions

1H NMR-based metabolic profiling has identified distinct differences in serum metabolic phenotype between CD and UC patients, as well as between IBD patients and controls.
Literatur
1.
Zurück zum Zitat Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573–621.PubMedCrossRef Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573–621.PubMedCrossRef
2.
Zurück zum Zitat Shih DQ, Targan SR. Insights into IBD pathogenesis. Curr Gastroenterol Rep. 2009;11:473–480.PubMedCrossRef Shih DQ, Targan SR. Insights into IBD pathogenesis. Curr Gastroenterol Rep. 2009;11:473–480.PubMedCrossRef
3.
Zurück zum Zitat Nicholson JK, Lindon JC, Holmes E. “Metabonomics”: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica. 1999;29:1181–1189.PubMedCrossRef Nicholson JK, Lindon JC, Holmes E. “Metabonomics”: understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica. 1999;29:1181–1189.PubMedCrossRef
4.
Zurück zum Zitat Nicholson JK, Holmes E, Wilson ID. Gut microorganisms, mammalian metabolism and personalized health care. Natl Rev Microbiol. 2005;3:431–438.CrossRef Nicholson JK, Holmes E, Wilson ID. Gut microorganisms, mammalian metabolism and personalized health care. Natl Rev Microbiol. 2005;3:431–438.CrossRef
5.
Zurück zum Zitat Williams HR, Cox IJ, Walker DG, et al. Characterization of inflammatory bowel disease with urinary metabolic profiling. Am J Gastroenterol. 2009;104:1435–1444.PubMedCrossRef Williams HR, Cox IJ, Walker DG, et al. Characterization of inflammatory bowel disease with urinary metabolic profiling. Am J Gastroenterol. 2009;104:1435–1444.PubMedCrossRef
6.
Zurück zum Zitat Marchesi JR, Holmes E, Khan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007;6:546–551.PubMedCrossRef Marchesi JR, Holmes E, Khan F, et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res. 2007;6:546–551.PubMedCrossRef
7.
Zurück zum Zitat Jansson J, Willing B, Lucio M, et al. Metabolomics reveals metabolic biomarkers of Crohn’s disease. PLoS ONE. 2009;4:e6386.PubMedCrossRef Jansson J, Willing B, Lucio M, et al. Metabolomics reveals metabolic biomarkers of Crohn’s disease. PLoS ONE. 2009;4:e6386.PubMedCrossRef
8.
Zurück zum Zitat Bjerrum JT, Nielsen OH, Hao F, et al. Metabonomics in ulcerative colitis: diagnostics, biomarker identification, and insight into the pathophysiology. J Proteome Res. 2010;9:954–962.PubMedCrossRef Bjerrum JT, Nielsen OH, Hao F, et al. Metabonomics in ulcerative colitis: diagnostics, biomarker identification, and insight into the pathophysiology. J Proteome Res. 2010;9:954–962.PubMedCrossRef
9.
Zurück zum Zitat Bezabeh T, Somorjai RL, Smith IC, Nikulin AE, Dolenko B, Bernstein CN. The use of 1H magnetic resonance spectroscopy in inflammatory bowel diseases: distinguishing ulcerative colitis from Crohn’s disease. Am J Gastroenterol. 2001;96:442–448.PubMedCrossRef Bezabeh T, Somorjai RL, Smith IC, Nikulin AE, Dolenko B, Bernstein CN. The use of 1H magnetic resonance spectroscopy in inflammatory bowel diseases: distinguishing ulcerative colitis from Crohn’s disease. Am J Gastroenterol. 2001;96:442–448.PubMedCrossRef
10.
Zurück zum Zitat Lin HM, Helsby NA, Rowan DD, Ferguson LR. Using metabolomic analysis to understand inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17:1021–1029.PubMedCrossRef Lin HM, Helsby NA, Rowan DD, Ferguson LR. Using metabolomic analysis to understand inflammatory bowel diseases. Inflamm Bowel Dis. 2011;17:1021–1029.PubMedCrossRef
11.
Zurück zum Zitat Nicholson JK, Foxall PJ, Spraul M, Farrant RD, Lindon JC. 750 MHz 1H and 1H–13C NMR spectroscopy of human blood plasma. Anal Chem. 1995;67:793–811.PubMedCrossRef Nicholson JK, Foxall PJ, Spraul M, Farrant RD, Lindon JC. 750 MHz 1H and 1H–13C NMR spectroscopy of human blood plasma. Anal Chem. 1995;67:793–811.PubMedCrossRef
12.
Zurück zum Zitat Teahan O, Gamble S, Holmes E, et al. Impact of analytical bias in metabonomic studies of human blood serum and plasma. Anal Chem. 2006;78:4307–4318.PubMedCrossRef Teahan O, Gamble S, Holmes E, et al. Impact of analytical bias in metabonomic studies of human blood serum and plasma. Anal Chem. 2006;78:4307–4318.PubMedCrossRef
13.
Zurück zum Zitat Bertini I, Calabro A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–177.PubMedCrossRef Bertini I, Calabro A, De Carli V, et al. The metabonomic signature of celiac disease. J Proteome Res. 2009;8:170–177.PubMedCrossRef
14.
Zurück zum Zitat Lauridsen MB, Bliddal H, Christensen R, et al. 1H NMR spectroscopy-based interventional metabolic phenotyping: a cohort study of rheumatoid arthritis patients. J Proteome Res. 2010;9:4545–4553.PubMedCrossRef Lauridsen MB, Bliddal H, Christensen R, et al. 1H NMR spectroscopy-based interventional metabolic phenotyping: a cohort study of rheumatoid arthritis patients. J Proteome Res. 2010;9:4545–4553.PubMedCrossRef
15.
Zurück zum Zitat MacIntyre DA, Jimenez B, Lewintre EJ, et al. Serum metabolome analysis by 1H-NMR reveals differences between chronic lymphocytic leukaemia molecular subgroups. Leukemia. 2010;24:788–797.PubMedCrossRef MacIntyre DA, Jimenez B, Lewintre EJ, et al. Serum metabolome analysis by 1H-NMR reveals differences between chronic lymphocytic leukaemia molecular subgroups. Leukemia. 2010;24:788–797.PubMedCrossRef
16.
Zurück zum Zitat Martin FP, Rezzi S, Philippe D, et al. Metabolic assessment of gradual development of moderate experimental colitis in IL-10-deficient mice. J Proteome Res. 2009;8:2376–2387.PubMedCrossRef Martin FP, Rezzi S, Philippe D, et al. Metabolic assessment of gradual development of moderate experimental colitis in IL-10-deficient mice. J Proteome Res. 2009;8:2376–2387.PubMedCrossRef
17.
Zurück zum Zitat Chen C, Shah YM, Morimura K, et al. Metabolomics reveals that hepatic stearoyl-CoA desaturase 1 downregulation exacerbates inflammation and acute colitis. Cell Metab. 2008;7:135–147.PubMedCrossRef Chen C, Shah YM, Morimura K, et al. Metabolomics reveals that hepatic stearoyl-CoA desaturase 1 downregulation exacerbates inflammation and acute colitis. Cell Metab. 2008;7:135–147.PubMedCrossRef
18.
Zurück zum Zitat Stange EF, Travis SP, Vermeire S, et al. European evidence-based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. Gut. 2006;55:i1–i15.PubMedCrossRef Stange EF, Travis SP, Vermeire S, et al. European evidence-based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis. Gut. 2006;55:i1–i15.PubMedCrossRef
19.
Zurück zum Zitat Stange EF, Travis SP, Vermeire S, et al. European evidence-based consensus on the diagnosis and management of ulcerative colitis: definitions and diagnosis. J Crohns Colitis. 2008;2:1–23.PubMedCrossRef Stange EF, Travis SP, Vermeire S, et al. European evidence-based consensus on the diagnosis and management of ulcerative colitis: definitions and diagnosis. J Crohns Colitis. 2008;2:1–23.PubMedCrossRef
20.
Zurück zum Zitat Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a working party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19:5–36.PubMed Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a working party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19:5–36.PubMed
21.
Zurück zum Zitat Lenz EM, Bright J, Wilson ID, et al. A 1H NMR-based metabonomic study of urine and plasma samples obtained from healthy human subjects. J Pharm Biomed Anal. 2003;33:1103–1115.PubMedCrossRef Lenz EM, Bright J, Wilson ID, et al. A 1H NMR-based metabonomic study of urine and plasma samples obtained from healthy human subjects. J Pharm Biomed Anal. 2003;33:1103–1115.PubMedCrossRef
22.
Zurück zum Zitat O’Sullivan A, Gibney MJ, Brennan L. Dietary intake patterns are reflected in metabolomic profiles: potential role in dietary assessment studies. Am J Clin Nutr. 2011;93:314–321.PubMedCrossRef O’Sullivan A, Gibney MJ, Brennan L. Dietary intake patterns are reflected in metabolomic profiles: potential role in dietary assessment studies. Am J Clin Nutr. 2011;93:314–321.PubMedCrossRef
23.
24.
Zurück zum Zitat Walmsley RS, Ayres RC, Pounder RE, Allan RN. A simple clinical colitis activity index. Gut. 1998;43:29–32.PubMedCrossRef Walmsley RS, Ayres RC, Pounder RE, Allan RN. A simple clinical colitis activity index. Gut. 1998;43:29–32.PubMedCrossRef
25.
Zurück zum Zitat Wishart DS, Tzur D, Knox C, et al. HMDB: the human metabolome database. Nucleic Acids Res. 2007;35:D521–D526.PubMedCrossRef Wishart DS, Tzur D, Knox C, et al. HMDB: the human metabolome database. Nucleic Acids Res. 2007;35:D521–D526.PubMedCrossRef
26.
Zurück zum Zitat Holmes E, Tsang TM, Huang JT, et al. Metabolic profiling of CSF: evidence that early intervention may impact on disease progression and outcome in schizophrenia. PLoS Med. 2006;3:e327.PubMedCrossRef Holmes E, Tsang TM, Huang JT, et al. Metabolic profiling of CSF: evidence that early intervention may impact on disease progression and outcome in schizophrenia. PLoS Med. 2006;3:e327.PubMedCrossRef
27.
Zurück zum Zitat Sussulini A, Prando A, Maretto DA, et al. Metabolic profiling of human blood serum from treated patients with bipolar disorder employing 1H NMR spectroscopy and chemometrics. Anal Chem. 2009;81:9755–9763.PubMedCrossRef Sussulini A, Prando A, Maretto DA, et al. Metabolic profiling of human blood serum from treated patients with bipolar disorder employing 1H NMR spectroscopy and chemometrics. Anal Chem. 2009;81:9755–9763.PubMedCrossRef
28.
Zurück zum Zitat Mao H, Wang H, Wang B, et al. Systemic metabolic changes of traumatic critically ill patients revealed by an NMR-based metabonomic approach. J Proteome Res. 2009;8:5423–5430.PubMedCrossRef Mao H, Wang H, Wang B, et al. Systemic metabolic changes of traumatic critically ill patients revealed by an NMR-based metabonomic approach. J Proteome Res. 2009;8:5423–5430.PubMedCrossRef
29.
Zurück zum Zitat Eriksson L, Trygg J, Wold S. CV-ANOVA for significance testing of PLS and OPLS® models. J Chemomet. 2008;22:594–600.CrossRef Eriksson L, Trygg J, Wold S. CV-ANOVA for significance testing of PLS and OPLS® models. J Chemomet. 2008;22:594–600.CrossRef
30.
Zurück zum Zitat Kochhar S, Jacobs DM, Ramadan Z, Berruex F, Fuerholz A, Fay LB. Probing gender-specific metabolism differences in humans by nuclear magnetic resonance-based metabonomics. Anal Biochem. 2006;352:274–281.PubMedCrossRef Kochhar S, Jacobs DM, Ramadan Z, Berruex F, Fuerholz A, Fay LB. Probing gender-specific metabolism differences in humans by nuclear magnetic resonance-based metabonomics. Anal Biochem. 2006;352:274–281.PubMedCrossRef
31.
Zurück zum Zitat Kristjansson G, Venge P, Wanders A, Loof L, Hallgren R. Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut. 2004;53:1806–1812.PubMedCrossRef Kristjansson G, Venge P, Wanders A, Loof L, Hallgren R. Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut. 2004;53:1806–1812.PubMedCrossRef
32.
Zurück zum Zitat Langhorst J, Elsenbruch S, Koelzer J, Rueffer A, Michalsen A, Dobos GJ. Noninvasive markers in the assessment of intestinal inflammation in inflammatory bowel diseases: performance of fecal lactoferrin, calprotectin, and PMN-elastase, CRP, and clinical indices. Am J Gastroenterol. 2008;103:162–169.PubMedCrossRef Langhorst J, Elsenbruch S, Koelzer J, Rueffer A, Michalsen A, Dobos GJ. Noninvasive markers in the assessment of intestinal inflammation in inflammatory bowel diseases: performance of fecal lactoferrin, calprotectin, and PMN-elastase, CRP, and clinical indices. Am J Gastroenterol. 2008;103:162–169.PubMedCrossRef
33.
Zurück zum Zitat Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427–434.PubMedCrossRef Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427–434.PubMedCrossRef
34.
Zurück zum Zitat Spoettl T, Hausmann M, Klebl F, et al. Serum soluble TNF receptor I and II levels correlate with disease activity in IBD patients. Inflamm Bowel Dis. 2007;13:727–732.PubMedCrossRef Spoettl T, Hausmann M, Klebl F, et al. Serum soluble TNF receptor I and II levels correlate with disease activity in IBD patients. Inflamm Bowel Dis. 2007;13:727–732.PubMedCrossRef
35.
Zurück zum Zitat Friedman G, Barak V, Chajek-Shaul T, et al. Recombinant human interleukin-1 suppresses lipoprotein lipase activity, but not expression of lipoprotein lipase mRNA in mesenchymal rat heart cell cultures. Biochim Biophys Acta. 1991;1089:83–87.PubMedCrossRef Friedman G, Barak V, Chajek-Shaul T, et al. Recombinant human interleukin-1 suppresses lipoprotein lipase activity, but not expression of lipoprotein lipase mRNA in mesenchymal rat heart cell cultures. Biochim Biophys Acta. 1991;1089:83–87.PubMedCrossRef
36.
Zurück zum Zitat Querfeld U, Ong JM, Prehn J, et al. Effects of cytokines on the production of lipoprotein lipase in cultured human macrophages. J Lipid Res. 1990;31:1379–1386.PubMed Querfeld U, Ong JM, Prehn J, et al. Effects of cytokines on the production of lipoprotein lipase in cultured human macrophages. J Lipid Res. 1990;31:1379–1386.PubMed
37.
Zurück zum Zitat Goldberg IJ. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res. 1996;37:693–707.PubMed Goldberg IJ. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res. 1996;37:693–707.PubMed
38.
Zurück zum Zitat Ripolles Piquer B, Nazih H, Bourreille A, et al. Altered lipid, apolipoprotein, and lipoprotein profiles in inflammatory bowel disease: consequences on the cholesterol efflux capacity of serum using Fu5AH cell system. Metabolism. 2006;55:980–988.PubMedCrossRef Ripolles Piquer B, Nazih H, Bourreille A, et al. Altered lipid, apolipoprotein, and lipoprotein profiles in inflammatory bowel disease: consequences on the cholesterol efflux capacity of serum using Fu5AH cell system. Metabolism. 2006;55:980–988.PubMedCrossRef
39.
Zurück zum Zitat Levy E, Rizwan Y, Thibault L, et al. Altered lipid profile, lipoprotein composition, and oxidant and antioxidant status in pediatric Crohn disease. Am J Clin Nutr. 2000;71:807–815.PubMed Levy E, Rizwan Y, Thibault L, et al. Altered lipid profile, lipoprotein composition, and oxidant and antioxidant status in pediatric Crohn disease. Am J Clin Nutr. 2000;71:807–815.PubMed
40.
Zurück zum Zitat Hyka N, Dayer JM, Modoux C, et al. Apolipoprotein A-I inhibits the production of interleukin-1beta and tumor necrosis factor-alpha by blocking contact-mediated activation of monocytes by T lymphocytes. Blood. 2001;97:2381–2389.PubMedCrossRef Hyka N, Dayer JM, Modoux C, et al. Apolipoprotein A-I inhibits the production of interleukin-1beta and tumor necrosis factor-alpha by blocking contact-mediated activation of monocytes by T lymphocytes. Blood. 2001;97:2381–2389.PubMedCrossRef
41.
Zurück zum Zitat Zeisel SH, Blusztajn JK. Choline and human nutrition. Ann Rev Nutr. 1994;14:269–296.CrossRef Zeisel SH, Blusztajn JK. Choline and human nutrition. Ann Rev Nutr. 1994;14:269–296.CrossRef
42.
Zurück zum Zitat Nassif A, Longo WE, Mazuski JE, Vernava AM, Kaminski DL. Role of cytokines and platelet-activating factor in inflammatory bowel disease. Implications for therapy. Dis Colon Rectum. 1996;39:217–223.PubMedCrossRef Nassif A, Longo WE, Mazuski JE, Vernava AM, Kaminski DL. Role of cytokines and platelet-activating factor in inflammatory bowel disease. Implications for therapy. Dis Colon Rectum. 1996;39:217–223.PubMedCrossRef
43.
Zurück zum Zitat Niculescu MD, Da Costa KA, Fischer LM, Zeisel SH. Lymphocyte gene expression in subjects fed a low-choline diet differs between those who develop organ dysfunction and those who do not. Am J Clin Nutr. 2007;86:230–239.PubMed Niculescu MD, Da Costa KA, Fischer LM, Zeisel SH. Lymphocyte gene expression in subjects fed a low-choline diet differs between those who develop organ dysfunction and those who do not. Am J Clin Nutr. 2007;86:230–239.PubMed
44.
Zurück zum Zitat Zeisel SH. Is there a new component of the Mediterranean diet that reduces inflammation? Am J Clin Nutr. 2008;87:277–278.PubMed Zeisel SH. Is there a new component of the Mediterranean diet that reduces inflammation? Am J Clin Nutr. 2008;87:277–278.PubMed
45.
Zurück zum Zitat Mehta AK, Singh BP, Arora N, Gaur SN. Choline attenuates immune inflammation and suppresses oxidative stress in patients with asthma. Immunobiology. 2010;215:527–534.PubMedCrossRef Mehta AK, Singh BP, Arora N, Gaur SN. Choline attenuates immune inflammation and suppresses oxidative stress in patients with asthma. Immunobiology. 2010;215:527–534.PubMedCrossRef
46.
Zurück zum Zitat Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340:448–454.PubMedCrossRef Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. 1999;340:448–454.PubMedCrossRef
47.
Zurück zum Zitat Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut. 2006;55:426–431.PubMedCrossRef Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut. 2006;55:426–431.PubMedCrossRef
48.
Zurück zum Zitat Lanfranchi GA, Brignola C, Campieri M, et al. Assessment of nutritional status in Crohn’s disease in remission or low activity. Hepatogastroenterology. 1984;31:129–132.PubMed Lanfranchi GA, Brignola C, Campieri M, et al. Assessment of nutritional status in Crohn’s disease in remission or low activity. Hepatogastroenterology. 1984;31:129–132.PubMed
49.
Zurück zum Zitat Hollander D. Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep. 1999;1:410–416.PubMedCrossRef Hollander D. Intestinal permeability, leaky gut, and intestinal disorders. Curr Gastroenterol Rep. 1999;1:410–416.PubMedCrossRef
50.
Zurück zum Zitat Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577–594.PubMedCrossRef Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008;134:577–594.PubMedCrossRef
51.
Zurück zum Zitat Velagapudi VR, Hezaveh R, Reigstad CS, et al. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res. 2010;51:1101–1112.PubMedCrossRef Velagapudi VR, Hezaveh R, Reigstad CS, et al. The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res. 2010;51:1101–1112.PubMedCrossRef
52.
Zurück zum Zitat Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.PubMedCrossRef Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–484.PubMedCrossRef
53.
Zurück zum Zitat Dumas ME, Barton RH, Toye A, et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci USA. 2006;103:12511–12516.PubMedCrossRef Dumas ME, Barton RH, Toye A, et al. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc Natl Acad Sci USA. 2006;103:12511–12516.PubMedCrossRef
Metadaten
Titel
Serum Metabolic Profiling in Inflammatory Bowel Disease
verfasst von
Horace R. T. Williams
James D. Willsmore
I. Jane Cox
David G. Walker
Jeremy F. L. Cobbold
Simon D. Taylor-Robinson
Timothy R. Orchard
Publikationsdatum
01.08.2012
Verlag
Springer US
Erschienen in
Digestive Diseases and Sciences / Ausgabe 8/2012
Print ISSN: 0163-2116
Elektronische ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-012-2127-2

Weitere Artikel der Ausgabe 8/2012

Digestive Diseases and Sciences 8/2012 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.