The cardiovascular risk of healthy individuals studied by NMR metabonomics of plasma samples

Journal of Proteome Research

Volumn 10, Issue 11, 2011, Pages 4983-4992

  Bernini, Patrizia ^a,b   Bertini, Ivano ^a,b   Luchinat, Claudio ^a   Tenori, Leonardo ^b   Tognaccini, Adriana ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b FiorGen Foundation   (Italy)

^c PISTOIA HOSPITAL   (Italy)

Author keywords

atherosclerosis; cardiovascular diseases; metabolites; metabolomics; metabonomics; NMR spectroscopy; oxidative stress

Indexed keywords

2 OXOGLUTARIC ACID; 3 HYDROXYBUTYRIC ACID; DIMETHYLGLYCINE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; THREONINE; TRIACYLGLYCEROL;

ADULT; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; CLINICAL ASSESSMENT; CONTROLLED STUDY; DIABETES MELLITUS; FEMALE; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; IMMOBILIZATION; MAJOR CLINICAL STUDY; MALE; METABOLITE; METABOLOMICS; MORBIDITY; MORTALITY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; OXIDATIVE STRESS; PREDICTOR VARIABLE; PRIORITY JOURNAL; RISK REDUCTION; SMOKING;

ADULT; AGED; CARDIOVASCULAR DISEASES; CHOLESTEROL; FEMALE; HUMANS; LIPOPROTEINS, HDL; LIPOPROTEINS, LDL; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; MIDDLE AGED; RISK FACTORS; YOUNG ADULT;

EID: 80655131103     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200452j     Document Type: Article

References (62)

1. D'Agostino, R. B.; Russell, M. W.; Huse, D. M.; Ellison, R. C.; Silbershatz, H.; Wilson, P. W.; Hartz, S. C. Primary and subsequent coronary risk appraisal: new results from the Framingham study Am. Heart J. 2000, 139 (2 Pt. 1) 272-281 (Pubitemid 30090804)
2. McMahan, C. A.; Gidding, S. S.; Viikari, J. S.; Juonala, M.; Kahonen, M.; Hutri-Kahonen, N.; Jokinen, E.; Taittonen, L.; Pietikainen, M.; McGill, H. C.; Raitakari, O. T. Association of Pathobiologic Determinants of Atherosclerosis in Youth risk score and 15-year change in risk score with carotid artery intima-media thickness in young adults (from the Cardiovascular Risk in Young Finns Study) Am. J. Cardiol. 2007, 100 (7) 1124-1129 (Pubitemid 47404470)
3. Gidding, S. S.; McMahan, C. A.; McGill, H. C.; Colangelo, L. A.; Schreiner, P. J.; Williams, O. D.; Liu, K. Prediction of coronary artery calcium in young adults using the Pathobiological Determinants of Atherosclerosis in Youth (PDAY) risk score: the CARDIA study Arch. Intern. Med. 2006, 166 (21) 2341-2347 (Pubitemid 44833359)
4. McMahan, C. A.; Gidding, S. S.; Malcom, G. T.; Tracy, R. E.; Strong, J. P.; McGill, H. C. Pathobiological determinants of atherosclerosis in youth risk scores are associated with early and advanced atherosclerosis Pediatrics 2006, 118 (4) 1447-1455 (Pubitemid 46393790)
5. Friedmann, P. D.; Brett, A. S.; Mayo-Smith, M. F. Differences in generalists' and cardiologists' perceptions of cardiovascular risk and the outcomes of preventive therapy in cardiovascular disease Ann. Intern. Med. 1996, 124 (4) 414-421 (Pubitemid 26065073)
6. Grover, S. A.; Lowensteyn, I.; Esrey, K. L.; Steinert, Y.; Joseph, L.; Abrahamowicz, M. Do doctors accurately assess coronary risk in their patients? Preliminary results of the coronary health assessment study BMJ [Br. Med. J.] 1995, 310 (6985) 975-978
7. McManus, R. J.; Mant, J.; Meulendijks, C. F.; Salter, R. A.; Pattison, H. M.; Roalfe, A. K.; Hobbs, F. D. Comparison of estimates and calculations of risk of coronary heart disease by doctors and nurses using different calculation tools in general practice: cross sectional study BMJ [Br. Med. J.] 2002, 324 (7335) 459-464 (Pubitemid 34169462)
8. Montgomery, A. A.; Fahey, T.; Mackintosh, C.; Sharp, D. J.; Peters, T. J. Estimation of cardiovascular risk in hypertensive patients in primary care Br. J. Gen. Pract. 2000, 50 (451) 127-128 (Pubitemid 30076681)
9. D'Agostino, R. B.; Grundy, S.; Sullivan, L. M.; Wilson, P. Validation of the Framingham coronary heart disease prediction scores: results of a multiple ethnic groups investigation JAMA, J. Am. Med. Assoc. 2001, 286 (2) 180-187 (Pubitemid 32640849)
10. Anderson, K. M.; Wilson, P. W.; Odell, P. M.; Kannel, W. B. An updated coronary risk profile. A statement for health professionals Circulation 1991, 83 (1) 356-362
11. Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III) JAMA, J. Am. Med. Assoc. 2001, 285 (19) 2486-2497
12. Wilson, P. W.; D'Agostino, R. B.; Levy, D.; Belanger, A. M.; Silbershatz, H.; Kannel, W. B. Prediction of coronary heart disease using risk factor categories Circulation 1998, 97 (18) 1837-1847 (Pubitemid 28213628)
13. Topol, E. J.; Lauer, M. S. The rudimentary phase of personalised medicine: coronary risk scores Lancet. 2003, 362 (9398) 1776-1777 (Pubitemid 37494752)
14. Lauer, M. S. Clinical practice. Aspirin for primary prevention of coronary events N. Engl. J. Med. 2002, 346 (19) 1468-1474 (Pubitemid 34755716)
15. Nicholson, J. K.; Lindon, J. C.; 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 (11) 1181-1189
16. Nicholson, J. K. Global systems biology, personalized medicine and molecular epidemiology Mol. Syst. Biol. 2006, 2, 52
17. Shockcor, J. P.; Holmes, E. Metabonomic applications in toxicity screening and disease diagnosis Curr. Top. Med. Chem. 2002, 2 (1) 35-51
18. Nicholson, J. K.; Lindon, J. C. Systems biology: Metabonomics Nature 2008, 455 (7216) 1054-1056
19. Serkova, N. J.; Niemann, C. U. Pattern recognition and biomarker validation using quantitative 1H-NMR-based metabolomics Expert Rev. Mol. Diagn. 2006, 6 (5) 717-731 (Pubitemid 44525597)
20. Wishart, D. S.; Tzur, D.; Knox, C.; Eisner, R.; Guo, A. C.; Young, N.; Cheng, D.; Jewell, K.; Arndt, D.; Sawhney, S.; Fung, C.; Nikolai, L.; Lewis, M.; Coutouly, M. A.; Forsythe, I.; Tang, P.; Shrivastava, S.; Jeroncic, K.; Stothard, P.; Amegbey, G.; Block, D.; Hau, D. D.; Wagner, J.; Miniaci, J.; Clements, M.; Gebremedhin, M.; Guo, N.; Zhang, Y.; Duggan, G. E.; Macinnis, G. D.; Weljie, A. M.; Dowlatabadi, R.; Bamforth, F.; Clive, D.; Greiner, R.; Li, L.; Marrie, T.; Sykes, B. D.; Vogel, H. J.; Querengesser, L. HMDB: the Human Metabolome Database Nucleic Acids Res. 2007, 35 (Database issue) D521-D526
21. Aranjbar, N.; Ott, K. H.; Roongta, V.; Mueller, L. Metabolomic analysis using optimized NMR and statistical methods Anal. Biochem. 2006, 355 (1) 62-70 (Pubitemid 44041397)
22. Raamsdonk, L. M.; Teusink, B.; Broadhurst, D.; Zhang, N.; Hayes, A.; Walsh, M. C.; Berden, J. A.; Brindle, K. M.; Kell, D. B.; Rowland, J. J.; Westerhoff, H. V.; van Dam, K.; Oliver, S. G. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations Nat. Biotechnol. 2001, 19 (1) 45-50 (Pubitemid 32051955)
23. Urbanczyk-Wochniak, E.; Luedemann, A.; Kopka, J.; Selbig, J.; Roessner-Tunali, U.; Willmitzer, L.; Fernie, A. R. Parallel analysis of transcript and metabolic profiles: a new approach in systems biology EMBO Rep. 2003, 4 (10) 989-993 (Pubitemid 37407468)
24. Mendes, P.; Kell, D. B.; Westerhoff, H. V. Why and when channelling can decrease pool size at constant net flux in a simple dynamic channel Biochim. Biophys. Acta 1996, 1289 (2) 175-186 (Pubitemid 26088677)
25. Sreekumar, A.; Poisson, L. M.; Rajendiran, T. M.; Khan, A. P.; Cao, Q.; Yu, J. D.; Laxman, B.; Mehra, R.; Lonigro, R. J.; Li, Y.; Nyati, M. K.; Ahsan, A.; Kalyana-Sundaram, S.; Han, B.; Cao, X. H.; Byun, J.; Omenn, G. S.; Ghosh, D.; Pennathur, S.; Alexander, D. C.; Berger, A.; Shuster, J. R.; Wei, J. T.; Varambally, S.; Beecher, C.; Chinnaiyan, A. M. Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression Nature 2009, 457 (7231) 910-914
26. Oakman, C.; Tenori, L.; Biganzoli, L.; Santarpia, L.; Cappadona, S.; Luchinat, C.; Di Leo, A. Uncovering the metabolomic fingerprint of breast cancer Int. J. Biochem. Cell Biol. 2011, 43 (7) 1010-1020
27. Lanza, I. R.; Zhang, S.; Ward, L. E.; Karakelides, H.; Raftery, D.; Nair, K. S. Quantitative metabolomics by H-NMR and LC-MS/MS confirms altered metabolic pathways in diabetes PLoS One 2010, 5 (5 e10538
28. Bertini, I.; Calabro, A.; De Carli, V.; Luchinat, C.; Nepi, S.; Porfirio, B.; Renzi, D.; Saccenti, E.; Tenori, L. The metabonomic signature of celiac disease J. Proteome Res. 2009, 1, 170-177
29. Wilson, P. W. Progressing from risk factors to omics Circ. Cardiovasc. Genet. 2008, 1 (2) 141-146
30. Mayr, M. Metabolomics: ready for the prime time? Circ. Cardiovasc. Genet. 2008, 1 (1) 58-65
31. Holmes, E.; Loo, R. L.; Stamler, J.; Bictash, M.; Yap, I. K.; Chan, Q.; Ebbels, T.; De Iorio, M.; Brown, I. J.; Veselkov, K. A.; Daviglus, M. L.; Kesteloot, H.; Ueshima, H.; Zhao, L.; Nicholson, J. K.; Elliott, P. Human metabolic phenotype diversity and its association with diet and blood pressure Nature 2008, 453 (7193) 396-400 (Pubitemid 351693125)
32. Shah, S. H.; Sun, J. L.; Pieper, K.; Crosslin, D. R.; Haynes, C.; Bain, J. R.; Muehlbauer, M.; Stevens, R. D.; Hauser, E. R.; Kraus, W. E.; Newgard, C. B.; Granger, C. B.; Califf, R. M.; Newby, L. K. Abstract 1261: Plasma Metabolomic Profiles Predict Future Cardiovascular Events Circulation 2009, 120 (18 Meeting Abstracts) S466-S46d
33. Shah, S. H.; Bain, J. R.; Muehlbauer, M. J.; Stevens, R. D.; Crosslin, D. R.; Haynes, C.; Dungan, J.; Newby, L. K.; Hauser, E. R.; Ginsburg, G. S.; Newgard, C. B.; Kraus, W. E. Association of a peripheral blood metabolic profile with coronary artery disease and risk of subsequent cardiovascular events Circ. Cardiovasc. Genet. 2010, 3 (2) 207-214
34. Sabatine, M. S.; Liu, E.; Morrow, D. A.; Heller, E.; McCarroll, R.; Wiegand, R.; Berriz, G. F.; Roth, F. P.; Gerszten, R. E. Metabolomic identification of novel biomarkers of myocardial ischemia Circulation 2005, 112 (25) 3868-3875 (Pubitemid 43739484)
35. Brindle, J. T.; Antti, H.; Holmes, E.; Tranter, G.; Nicholson, J. K.; Bethell, H. W.; Clarke, S.; Schofield, P. M.; McKilligin, E.; Mosedale, D. E.; Grainger, D. J. Rapid and noninvasive diagnosis of the presence and severity of coronary heart disease using 1H-NMR-based metabonomics Nat. Med. 2002, 8 (12) 1439-1444 (Pubitemid 36019430)
36. Kirschenlohr, H. L.; Griffin, J. L.; Clarke, S. C.; Rhydwen, R.; Grace, A. A.; Schofield, P. M.; Brindle, K. M.; Metcalfe, J. C. Proton NMR analysis of plasma is a weak predictor of coronary artery disease Nat. Med. 2006, 12 (6) 705-710 (Pubitemid 43865242)
37. Barton, R. H.; Waterman, D.; Bonner, F. W.; Holmes, E.; Clarke, R.; the PROCARDIS Consortium; Nicholson, J. K.; Lindon, J. C. The influence of EDTA and citrate anticoagulant addition to human plasma on information recovery from NMR-based metabolic profiling studies Mol. BioSyst. 2010, 6 (1) 215-224
38. Allain, C. C.; Poon, L. S.; Chan, C. S.; Richmond, W.; Fu, P. C. Enzymatic determination of total serum cholesterol Clin. Chem. 1974, 20 (4) 470-475
39. Bucolo, G.; David, H. Quantitative determination of serum triglycerides by the use of enzymes Clin Chem. 1973, 19 (5) 476-482
40. Friedewald, W. T.; Levy, R. I.; Fredrickson, D. S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge Clin. Chem. 1972, 18 (6) 499-502
41. Westerhuis, J.; Hoefsloot, H.; Smit, S.; Vis, D.; Smilde, A.; van Velzen, E.; van Duijnhoven, J.; van Dorsten, F. Assessment of PLSDA cross validation Metabolomics 2008, 4 (1) 81-89 (Pubitemid 351217591)
42. Szymanska, E.; Saccenti, E.; Smilde, A.; Westerhuis, J. Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies Metabolomics 2011, 1-14
43. Bonferroni, C. E. Il calcolo delle assicurazioni su gruppi di teste. In Studi in Onore del Professore Salvatore Ortu Carboni; Carboni, S.O., Ed.; Tipografia del Senato: Rome, Italy, 1935.
44. Broadhurst, D.; Kell, D. Statistical strategies for avoiding false discoveries in metabolomics and related experiments Metabolomics 2006, 2 (4) 171-196 (Pubitemid 46099798)
45. Ihaka, R.; Gentleman, R. R A language for data analysis and graphics J. Comput. Stat. Graph. 1996, 5 (3) 299-314
46. Bellodi, G.; Bernini, G.; Manicardi, V.; Veneri, L.; Muratori, L.; Magnanini, G.; Rossi, G.; Bossini, P.; Descovich, G. Arterial hypertension in relation to life style and other cardiovascular risk factors. Epidemiologic study of a population of blood donors. Project AVIS Minerva Cardioangiol. 1994, 42 (3) 73-84 (Pubitemid 24165288)
47. Beckwith-Hall, B. M.; Thompson, N. A.; Nicholson, J. K.; Lindon, J. C.; Holmes, E. A metabonomic investigation of hepatotoxicity using diffusion-edited 1H NMR spectroscopy of blood serum Analyst 2003, 128 (7) 814-818 (Pubitemid 36897867)
48. Hageman, J. A.; Hendriks, M. M.; Westerhuis, J. A.; van der Werf, M. J.; Berger, R.; Smilde, A. K. Simplivariate models: ideas and first examples PLoS One 2008, 3 (9) e3259
49. Kashiwaya, Y.; Takeshima, T.; Mori, N.; Nakashima, K.; Clarke, K.; Veech, R. L. D-beta-hydroxybutyrate protects neurons in models of Alzheimer's and Parkinson's disease Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (10) 5440-5444 (Pubitemid 30313737)
50. Tani, T.; Taki, Y.; Aoyama, H.; Jikkoh, A.; Arii, S.; Ozawa, K.; Tobe, T. Changes in acetoacetate/beta-hydroxybutyrate ratio in arterial blood following hepatic artery embolization in man Life Sci. 1984, 35 (11) 1177-1182 (Pubitemid 14065465)
51. Saibara, T.; Maeda, T.; Onishi, S.; Yamamoto, Y. Plasma exchange and the arterial blood ketone body ratio in patients with acute hepatic failure J. Hepatol. 1994, 20 (5) 617-622 (Pubitemid 24149021)
52. Tunaru, S.; Kero, J.; Schaub, A.; Wufka, C.; Blaukat, A.; Pfeffer, K.; Offermanns, S. PUMA-G and HM74 are receptors for nicotinic acid and mediate its anti-lipolytic effect Nat. Med. 2003, 9 (3) 352-355 (Pubitemid 36362793)
53. Soudijn, W.; van, W., I; Ijzerman, A. P. Nicotinic acid receptor subtypes and their ligands Med. Res. Rev. 2007, 27 (3) 417-433 (Pubitemid 46668940)
54. Bazzano, G.; Bazzano, G. S. Hypocholesterolemic effect of -ketoglutarate in the Mongolian gerbil Proc. Soc. Exp. Biol. Med. 1972, 140 (1) 36-39
55. He, W.; Miao, F. J.; Lin, D. C.; Schwandner, R. T.; Wang, Z.; Gao, J.; Chen, J. L.; Tian, H.; Ling, L. Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors Nature 2004, 429 (6988) 188-193 (Pubitemid 38656195)
56. Guerranti, R.; Pagani, R.; Neri, S.; Errico, S. V.; Leoncini, R.; Marinello, E. Inhibition and regulation of rat liver L-threonine dehydrogenase by different fatty acids and their derivatives Biochim. Biophys. Acta 2001, 1568 (1) 45-52 (Pubitemid 33145383)
57. Friesen, R. W.; Novak, E. M.; Hasman, D.; Innis, S. M. Relationship of dimethylglycine, choline, and betaine with oxoproline in plasma of pregnant women and their newborn infants J. Nutr. 2007, 137 (12) 2641-2646 (Pubitemid 350255291)
58. MacKenzie, C. G.; Frisell, W. R. The metabolism of dimethylglycine by liver mitochondria J. Biol. Chem. 1958, 232 (1) 417-427
59. Slow, S.; McGregor, D. O.; Lever, M.; Lee, M. B.; George, P. M.; Chambers, S. T. Dimethylglycine supplementation does not affect plasma homocysteine concentrations in pre-dialysis chronic renal failure patients Clin. Biochem. 2004, 37 (11) 974-976 (Pubitemid 39388658)
60. Kalmar, I. D.; Cools, A.; Verstegen, M. W.; Huyghebaert, G.; Buyse, J.; Roose, P.; Janssens, G. P. Dietary supplementation with dimethylglycine affects broiler performance and plasma metabolites depending on dose and dietary fatty acid profile J. Anim. Physiol. Anim. Nutr. 2011, 95 (2) 146-153
61. Befroy, D. E.; Petersen, K. F.; Dufour, S.; Mason, G. F.; de Graaf, R. A.; Rothman, D. L.; Shulman, G. I. Impaired mitochondrial substrate oxidation in muscle of insulin-resistant offspring of type 2 diabetic patients Diabetes 2007, 56 (5) 1376-1381 (Pubitemid 46715630)
62. Fiorgen Foundation. AVIS Project Datasets. http://www.fiorgen.net/ Downloads.html (accessed September 30, 2011).