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Cited by 520Metabolomics and Mass Spectrometry StudiesNutrition, Genetics, and DiseaseNutritional Studies and Diet

The food metabolome: a window over dietary exposure

Open access
Scalbert, Augustin, Brennan, Lorraine, Manach, Claudine, Andres-Lacueva, Cristina, Dragsted, Lars O, Draper, John, Rappaport, Stephen M, van der Hooft, Justin JJ +1 more·2014·The American Journal of Clinical Nutrition
DOI 10.3945/ajcn.113.076133
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Abstract

The food metabolome is defined as the part of the human metabolome directly derived from the digestion and biotransformation of foods and their constituents. With >25,000 compounds known in various foods, the food metabolome is extremely complex, with a composition varying widely according to the diet. By its very nature it represents a considerable and still largely unexploited source of novel dietary biomarkers that could be used to measure dietary exposures with a high level of detail and precision. Most dietary biomarkers currently have been identified on the basis of our knowledge of food compositions by using hypothesis-driven approaches. However, the rapid development of metabolomics resulting from the development of highly sensitive modern analytic instruments, the availability of metabolite databases, and progress in (bio)informatics has made agnostic approaches more attractive as shown by the recent identification of novel biomarkers of intakes for fruit, vegetables, beverages, meats, or complex diets. Moreover, examples also show how the scrutiny of the food metabolome can lead to the discovery of bioactive molecules and dietary factors associated with diseases. However, researchers still face hurdles, which slow progress and need to be resolved to bring this emerging field of research to maturity. These limits were discussed during the First International Workshop on the Food Metabolome held in Glasgow. Key recommendations made during the workshop included more coordination of efforts; development of new databases, software tools, and chemical libraries for the food metabolome; and shared repositories of metabolomic data. Once achieved, major progress can be expected toward a better understanding of the complex interactions between diet and human health.

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  • Findingcitation

    About 100 dietary biomarkers have been identified in the Exposome-Explorer database.

    “Information on these biomarkers has been systematically collected in the novel Exposome-Explorer database (V Neveu, DS Wishart, and A Scalbert, unpublished data, 2014); w100 biomarkers could be identified”
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    • cites V Neveu, DS Wishart, and A Scalbert, unpublished data, 2014

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  • Findingreasoning

    Except for two studies on dietary fiber and milk protein diet, all discovery studies listed used urine samples rather than blood samples.

    “With the exception of 2 studies on dietary fiber and milk protein diet, all discovery studies were conducted on urine samples as opposed to blood samples (Table 3).”
    Quote in the paperSubstantial claim
  • Premisecitation

    Alkylresorcinols have been used as surrogate biomarkers of whole-grain cereal intake.

    “alkylresorcinols for whole-grain cereals (19,20)”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [19] Ross, 2012, Plasma alkylresorcinols as a biomarker of whole-grain food consumption in a large population: results from the WHOLEheart Intervention Study, Am J Clin Nutr source

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    • cites [20] Andersson, 2011, Plasma alkylresorcinol concentrations correlate with whole grain wheat and rye intake and show moderate reproducibility over a 2-to 3-month period in free-living Swedish adults, J Nutr source

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  • Premisecitation

    Dietary exposure has traditionally been assessed with self-reported methods such as dietary recalls or food-frequency questionnaires.

    “Dietary exposure has traditionally been measured with self-reported methods, namely dietary recalls or food-frequency questionnaires (10).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Rutishauser, 2005, Dietary intake measurements, Public Health Nutr source

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  • Premisecitation

    Biomarkers are useful when little or no food composition data exist, as is often the case for bioactive molecules such as glucosinolates or contaminants such as aflatoxins.

    “Biomarkers are also useful when little or no data exist on food composition, as is often the case for bioactive molecules such as glucosinolates or food contaminants such as aflatoxins (15,16).”
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    • cites [15] London, 2000, Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: a prospective study of men in Shanghai, China, Lancet source

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    • cites [16] Kensler, 2011, Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology, Toxicol Sci source

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    Findingreasoning

    Many proposed biomarkers in Table 3 (marked with asterisks) have not been fully validated with proper chemical standards because such standards are often not commercially available.

    “It is important to point out that the identities of many of the proposed biomarkers in Table 3 (marked with an asterisk) have not been fully validated with proper chemical standards because these standards are often not commercially available.”
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    Premisecitation

    Misclassification of subjects by dietary intake can influence observed associations between dietary exposures and disease outcomes and underlies inconsistencies in nutritional epidemiology.

    “The resulting misclassification of subjects, especially when sorting them according to dietary intake, can influence observed associations between dietary exposures and disease outcomes and underlies inconsistencies in published findings in the field of nutritional epidemiology (12).”
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    • cites [12] Marshall, 1999, Diet and health risk: risk patterns and disease-specific associations, Am J Clin Nutr source

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    Interpretationreasoning

    The food metabolome is highly complex and highly variable.

    “The food metabolome is therefore highly complex and also highly variable.”
    Quote in the paperSubstantial claim

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    Premisecitation

    Foods eaten by humans contain roughly 25,000 compounds, and most of these are further metabolized in the human body.

    “The various foods consumed by humans contain .25,000compounds, most of them being further metabolized in the human body (9).”
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    • cites [9] Wishart, 2013, HMDB 3.0—the Human Metabolome Database in 2013, Nucleic Acids Res

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    Premisecitation

    Self-reported dietary assessment methods contain random and systematic errors, including recall bias and difficulty in assessing portion sizes.

    “However, a number of random and systematic errors are inherent in such methods, including recall bias and difficulty in assessing portion sizes (11).”
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    • cites [11] Bingham, 2007, Epidemiologic assessment of sugars consumption using biomarkers: comparisons of obese and nonobese individuals in the European Prospective Investigation of Cancer Norfolk, Cancer Epidemiol Biomarkers Prev source

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    Premisecitation

    Isothiocyanates and acrylamide form adducts with blood albumin and hemoglobin, with half-lives of 3 to 8 weeks, and may be used as longer-term biomarkers.

    “Some dietary compounds such as isothiocyanates and acrylamide also form adducts with blood albumin and hemoglobin (37,38), with half-lives varying between 3 and 8 wk, and may be used as longer-term biomarkers.”
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    • cites [37] Kumar, 2010, Determination of new biomarkers to monitor the dietary consumption of isothiocyanates, Biomarkers source

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    • cites [38] Outzen, 2011, Dietary determinants for Hb-acrylamide and Hb-glycidamide adducts in Danish non-smoking women, Br J Nutr source

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    Premisecitation

    Up to 200,000 different metabolites are estimated to occur in the plant kingdom, and combinations of several hundreds of secondary metabolites generally characterize each edible plant.

    “Up to 200,000 different metabolites are estimated to occur in the plant kingdom, and combinations of several hundreds of secondary metabolites generally characterize each edible plant (6,64,65).”
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    • cites [6] Manach, 2009, The complex links between dietary phytochemicals and human health deciphered by metabolomics, Mol Nutr Food Res source

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    • cites [64] Fiehn, 2002, Metabolomics—the link between genotypes and phenotypes, Plant Mol Biol source

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    • cites [65] Iijima, 2008, Metabolite annotations based on the integration of mass spectral information, Plant J source

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    Premisecitation

    Proline betaine and lycopene are well-established biomarkers for citrus fruit and tomato products, respectively.

    “Proline betaine and lycopene are well-established biomarkers for citrus fruit and tomato products, respectively (44,45).”
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    • cites [44] Lloyd, 2011, Proline betaine and its biotransformation products in fasting urine samples are potential biomarkers of habitual citrus fruit consumption, Br J Nutr source

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    • cites [45] Al-Delaimy, 2005, Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC), Eur J Clin Nutr source

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    Premisenone given

    Essential amino acids, essential fatty acids, most vitamins, and minerals cannot be produced by humans and must originate from external dietary sources.

    “The possible exceptions are the essential amino acids, essential fatty acids along with most vitamins, and minerals, which cannot be produced by humans and must originate from external dietary sources.”
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    Premisereasoning

    Intermediary metabolites formed by digestion of lipids, polysaccharides, and proteins are common to all living organisms and identical to human endogenous metabolites, and generally cannot be used as dietary biomarkers because of their common identity and the impossibility of tracing their dietary origin.

    “Most of these compounds are common to all living organisms and identical to human endogenous metabolites.They cannot generally be used as dietary biomarkers because of their common identity and the impossibility to trace their dietary origin.”
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    Premisecitation

    The Folin assay, commonly used to estimate total polyphenols in foods, has been applied to urine to compare polyphenol intake, but such use may be inappropriate because of interfering reducing metabolites.

    “The Folin assay, commonly used to estimate total polyphenols in foods (46), has also been applied to urine samples to compare polyphenol intake (47), but such use may be inappropriate because of the presence of interfering reducing metabolites in such complex biological matrices (46).”
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    • cites [46] Scalbert, 2005, Dietary polyphenols and the prevention of diseases, Crit Rev Food Sci Nutr source

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    • cites [47] Medina-Remón, 2011, Total polyphenol excretion and blood pressure in subjects at high cardiovascular risk, Nutr Metab Cardiovasc Dis source

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    Premisecitation

    More than 300 empirical rules allow prediction of the fate of metabolites based on their chemical structure.

    “In fact, there are .300different empirical rules that allow one to predict the fate of metabolites on the basis of their chemical structure (69).”
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    • cites [69] Langowski, 2002, Computer systems for the prediction of xenobiotic metabolism, Adv Drug Deliv Rev source

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    Premisecitation

    Lipophilic markers such as carotenoids and lipids, and erythrocyte-associated biomarkers such as folate and fatty acids, have longer half-lives of weeks to months.

    “Lipophilic markers (carotenoids, lipids) (36) or biomarkers associated with erythrocytes (folate, fatty acids) (29) have longer half-lives (week to month) because of the equilibrium of biomarkers between blood and fatty tissues, or because of their integration into erythrocytes.”
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    • cites [36] Burri, 2001, Serum carotenoid depletion follows first-order kinetics in healthy adult women fed naturally low carotenoid diets, J Nutr source

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    • cites [29] Crews, 2001, A critical assessment of some biomarker approaches linked with dietary intake, Br J Nutr source

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    Premisecitation

    Dietary biomarkers include natural food constituents and also food additives such as iodine in milk and contaminants such as polychlorinated biphenyls in fatty fish.

    “Dietary biomarkers not only include natural food constituents but also certain food additives such as iodine in milk (26) or food contaminants such as polychlorinated biphenyls in fatty fish (27).”
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    • cites [26] Brantsaeter, 2009, Evaluation of urinary iodine excretion as a biomarker for intake of milk and dairy products in pregnant women in the Norwegian Mother and Child Cohort Study (MoBa), Eur J Clin Nutr source

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    • cites [27] Turunen, 2010, Dioxins, polychlorinated biphenyls, methyl mercury and omega-3 polyunsaturated fatty acids as biomarkers of fish consumption, Eur J Clin Nutr source

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    Premisecitation

    Microbial metabolites include short-chain fatty acids, secondary bile acids, protein and amino acid metabolites, and plant polyphenol metabolites.

    “These microbial metabolites include short-chain fatty acids, secondary bile acids, protein and amino acid metabolites, as well as plant polyphenol metabolites (67).”
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    • cites [67] Nicholson, 2012, Host-gut microbiota metabolic interactions, Science source

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    Premisecitation

    Polyphenols, alkylresorcinols, and amino acids have half-lives that do not exceed 24 hours.

    “Some of the biomarkers listed in Table 1 have half-lives that do not exceed 24 h [polyphenols, alkylresorcinols, and amino acids (34,35)].”
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    • cites [34] Manach, 2005, Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies, Am J Clin Nutr source

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    • cites [35] Söderholm, 2009, Plasma pharmacokinetics of alkylresorcinol metabolites: new candidate biomarkers for whole-grain rye and wheat intake, Am J Clin Nutr source

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    Premisecitation

    Noticeable differences in human metabolomes depend strongly on diet, sex, health status, genetics, kinetics, physiology, and age, with diet being most important.

    “noticeable differences in human metabolomes could be detected that appeared to depend strongly on diet, sex, health status, genetics, kinetics, physiology, and age-with diet being most important (59)(60)(61)(62).”
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    • cites (59)(60)(61)(62)

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    Premisecitation

    The yield of phase I/II reactions is often very high, and host-transformed metabolites retain many features of their parent compounds.

    “The yield of phase I/II reactions are often very high (68,71), and host-transformed metabolites retain many of the features of their parent compounds.”
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    • cites [68] Testa, 2012, Foundation review: reactions and enzymes in the metabolism of drugs and other xenobiotics, Drug Discov Today source

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    • cites [71] Silberberg, 2006, The bioavailability of polyphenols is highly governed by the capacity of the intestine and of the liver to secrete conjugated metabolites, Eur J Nutr source

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    Premisenone given

    The human body maintains a complex defense system of dozens of enzymes and membrane transporters to recognize foreign and potentially toxic chemicals and neutralize them by rapid biotransformation and/or elimination.

    “The human body maintains a complex defense system consisting of dozens of enzymes and membrane transporters to recognize these foreign and potentially toxic chemicals and to neutralize them by rapid biotransformation and/or elimination.”
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    Premisenone given

    Food compounds that are not useful for basic metabolism or that do not correspond to familiar endogenous metabolites are treated as foreign or as xenobiotics.

    “Food compounds that are not useful for basic metabolism or that do not correspond to familiar endogenous metabolites are treated as”
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    Premisecitation

    Vitamin C and selenium in erythrocyte glutathione peroxidase show saturable effects and may not be suitable at high exposure levels.

    “Biomarkers such as vitamin C or selenium in erythrocyte glutathione peroxidase show saturable effects and may not be suitable for use at high levels of exposure (29,42).”
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    • cites [29] Crews, 2001, A critical assessment of some biomarker approaches linked with dietary intake, Br J Nutr source

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    • cites [42] Levine, 1996, Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance, Proc Natl Acad Sci USA source

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  • Classified as probably not a substantial claim. May combine two claims.

    Premisenone given

    Food constituents can be metabolized in three ways: digestion in the mouth, stomach, and small intestine; transformation by host tissues; or processing by the gut microbiota.

    “Food constituents can be metabolized in 3 different ways: 1) they can be digested in the mouth, stomach, and small intestine into simple nutrients that can be absorbed through the gut barrier; 2) they can be further transformed by host tissues, especially the liver and kidney; or 3) they can be processed by the gut microbiota in the large intestine.”
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    Premisenone given

    Biotransformation consists of phase I and phase II reactions, both of which occur primarily in the liver, kidney, and intestine.

    “Classically, the biotransformation process consists of 2 types of chemical reactions, phase I and phase II transformations, both of which occur primarily in the liver, kidney, and intestine.”
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    Premisecitation

    The human gut contains more than 1000 different species of microbes, giving an enormous diversity of enzymatic processes that act on food-derived compounds.

    “Microbes have a very different set of enzymes from mammals, and given that there are .1000different species of microbes in the human gut (72) there is an enormous diversity of enzymatic processes that act on foodderived compounds.”
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    • cites [72] Peris-Bondia, 2011, The active human gut microbiota differs from the total microbiota, PLoS ONE source

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    Premisecitation

    The human metabolome contains at least 50,000 different detectable compounds.

    “Minimally, the human metabolome contains 50,000 different detectable compounds (9,63), but as instrument sensitivity and separation technologies improve, this number is expected to increase.”
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    • cites [9] Wishart, 2013, HMDB 3.0—the Human Metabolome Database in 2013, Nucleic Acids Res

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    • cites [63] Smith, 2005, METLIN—a metabolite mass spectral database, Ther Drug Monit source

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    Premisecitation

    Dietary biomarker concentrations can be altered by genetic factors, physiologic or health status, dietary factors, and lifestyle factors.

    “They may be altered because of possible interactions with genetic factors, physiologic or health status (ie, age or obesity) (30), dietary factors such as fats for lipophilic biomarkers (31), and lifestyle factors such as alcohol intake or smoking (32).”
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    • cites [30] Vioque, 2007, Plasma concentrations of carotenoids and vitamin C are better correlated with dietary intake in normal weight than overweight and obese elderly subjects, Br J Nutr source

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    • cites [31] Brown, 2004, Carotenoid bioavailability is higher from salads ingested with full-fat than with fat-reduced salad dressings as measured with electrochemical detection, Am J Clin Nutr source

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    • cites [32] Albanes, 1997, Effects of supplemental beta-carotene, cigarette smoking, and alcohol consumption on serum carotenoids in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study, Am J Clin Nutr source

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  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning

    In explorative science, there is no fixed rule for the acceptability level of the false discovery rate, and any level from 5% to 50% may be useful depending on further data analysis steps.

    “In explorative science there is no fixed rule for the acceptability level of the FDR, and any level from 5% to 50% may be useful, depending on further data analysis steps.”
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    Premisenone given

    Metabolite identification in metabolomic studies relies on comparing generated spectra with those in curated metabolite databases.

    “Metabolite identification in metabolomic studies relies on the comparison of generated spectra with those in curated metabolite databases.”
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    Premisenone given

    The gut microbiota processes indigestible carbohydrates through fermentative pathways yielding short-chain fatty acids such as butyric acid and propionic acid.

    “The gut microbiota also processes indigestible carbohydrates through a variety of fermentative pathways yielding short-chain fatty acids such as butyric acid and propionic acid.”
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    Interpretationnone given

    Multiple variables can substantially affect the final data set in any experimentally based analytic method.

    “As with any experimentally based analytic method, multiple variables can substantially affect the final data set.”
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    Interpretationnone given

    Untargeted metabolomics provides wider coverage and is likely to reveal new metabolites in biofluids and tissues.

    “In principle, untargeted metabolomics provides a wider coverage and is likely to show the presence of new metabolites in biofluids and tissues.”
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    Premisenone given

    Phenolic acids can be further conjugated to glycine as in hippurate.

    “These phenolic acids can be further conjugated to glycine as in hippurate.”
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    Premisecitation

    NMR is robust, nondestructive, and quantitative but has relatively low sensitivity, limiting its coverage of the food metabolome to predominant nutrients, sugars, and microbial metabolites at millimolar to micromolar concentrations.

    “Briefly, NMR is robust, nondestructive, and quantitative but has a relatively low sensitivity, which narrows its coverage of the food metabolome to predominant nutrients, sugars, and microbial metabolites present at millimolar to micromolar concentrations.”
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    • cites [111] Theodoridis, 2008, LC-MS-based methodology for global metabolite profiling in metabonomics/metabolomics, Trends Analyt Chem source

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    • cites [112] Scalbert, 2009, Mass-spectrometry-based metabolomics: limitations and recommendations for future progress with particular focus on nutrition research, Metabolomics source

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    • cites [113] Issaq, 2009, Analytical and statistical approaches to metabolomics research, J Sep Sci source

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    Interpretationcitation

    Supervised multivariate analysis is commonly the next step in many data analysis methods but has a strong tendency to overfit the data.

    “Supervised multivariate analysis is commonly the next step in many data analysis methods but has a strong tendency to overfit the data.”
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    Premisecitation

    There are many supervised methods, with partial least-squares discriminant analysis (PLS-DA) or its variants being the most commonly used for comparing two groups.

    “There are a large number of supervised methods (120, 127), with the most commonly used analysis for comparing 2 groups being partial least-squares discriminant analysis (PLS-DA) (132) or one of its several variants.”
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    • cites [120] Sugimoto, 2012, bioinformatics tools for mass spectroscopy-based metabolomic data processing and analysis, Current Bioinformatics source

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    • cites [127] Worley, 2013, Utilities for quantifying separation in PCA/PLS-DA scores plots, Anal Biochem source

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    • cites [132] Wold, 1983, The multivariate calibration problem in chemistry solved by the PLS methods source

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    Interpretationreasoning

    It is crucial to align different sample profiles, which do not match exactly because of small variations in retention times, masses, or chemical shifts.

    “It is crucial to align the different sample profiles, which do not match exactly because of small variations in retention times, masses, or chemical shifts.”
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    Premisecitation

    These steps include data preprocessing, alignment, normalization, and signal correction, followed by statistical analysis.

    “These include data preprocessing, data alignment, data normalization, and signal correction followed by the analysis through various statistical methods.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [119] Katajamaa, 2007, Data processing for mass spectrometry-based metabolomics, J Chromatogr A source

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    • cites [120] Sugimoto, 2012, bioinformatics tools for mass spectroscopy-based metabolomic data processing and analysis, Current Bioinformatics source

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  • May combine two claims.

    Interpretationnone given

    Features associated with a pattern can be shown by loadings in a PCA plot, but PCA is generally not well suited to identify the most prominent part of the pattern.

    “The features associated with any pattern can be shown by the loadings in a PCA plot; however, PCA is generally not well suited to identify the most prominent part of the pattern.”
    Quote in the paperNot a substantial claim

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    Premisecitation

    Certain microbial metabolites can be useful as food biomarkers, although there is a complex relation between the food source, the predominant gut microbial species, and the resulting food metabolites.

    “Certain microbial metabolites can be useful as food biomarkers, although there is a complex relation between the food source, the predominant gut microbial species, and the resulting food metabolites (73).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [73] Moco, 2012, A metabolomics view on gut microbiome modulation by polyphenol-rich foods, J Proteome Res source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given

    The food metabolome comprises much greater chemical diversity than any other part of the metabolome.

    “First, it comprises a much greater chemical diversity than any other part of the metabolome (see Food metabolome and metabolite databases section).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    The main current limitation of MS is the challenging and burdensome structural elucidation of detected ions.

    “The main current limitation of MS is the very challenging and burdensome task of the structural elucidation of the detected ions (see below).”
    Quote in the paperNot a substantial claim

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    Premisecitation

    Direct flow injection-MS has been used and offers the advantage of high-throughput analysis required for large-scale epidemiologic studies.

    “Direct flow injection-MS has also been used (82,114), which offers the advantage of high-throughput analysis, as would be required for large-scale epidemiologic studies.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [82] Lloyd, 2011, Use of mass spectrometry fingerprinting to identify urinary metabolites after consumption of specific foods, Am J Clin Nutr source

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    • cites [114] Beckmann, 2013, Hydroxylated phenylacetamides derived from bioactive benzoxazinoids are bioavailable in humans after habitual consumption of whole grain sourdough rye bread, Mol Nutr Food Res source

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  • May combine two claims.

    Premisereasoning

    MS is the most sensitive technique and the only method able to cover nonnutrient food metabolome metabolites occurring at low concentrations in biological samples.

    “MS is by far the most sensitive technique and the only method able to cover the nonnutrient metabolites of the food metabolome occurring at low concentrations in biological samples.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Interpretationnone given

    The field of metabolomics is rich with data analysis options, and the future challenge is to optimally apply these to food metabolomic studies.

    “Overall, the field of metabolomics is rich with data analysis options, and the challenge in the future will be to optimally apply these to food metabolomic studies.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    Using food-frequency questionnaires may directly identify biomarkers of habitual dietary exposure, but their lower accuracy and smaller number of documented foods may limit their usefulness for discovery studies.

    “The use of food-frequency questionnaires may directly lead to the identification of biomarkers of habitual dietary exposure, but the lower accuracy and lower number of foods documented may limit their value for such discovery studies (105).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [105] May, 2013, Metabolomic profiling of urine: response to a randomised, controlled feeding study of select fruits and vegetables, and application to an observational study, Br J Nutr source

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  • May combine two claims.

    Interpretationreasoning

    The predominance of urine samples is partly due to higher concentrations of food-derived metabolites in urine than in blood and the absence of interfering proteins.

    “The reason for this is partly technical because of the higher concentrations of food-derived metabolites in urine as compared with blood and because of the lack of interfering proteins.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Unsupervised multivariate analysis provides an objective assessment of principal patterns in the data set, such as intake or no intake of a specific food component or diet.

    “This provides an objective assessment of the principal patterns in the data set (eg, intake or no intake of a specific food component or diet).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Interpretationnone given

    Statistical analysis of untargeted metabolomic data is often an initial step in biomarker discovery and should not be confused with hypothesis testing because there is no a priori hypothesis.

    “Statistical analysis of untargeted metabolomic data is often an initial step in the biomarker discovery process that should not be confused with hypothesis testing, because there is no a priori hypothesis.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Variables affecting the final data set include sample preparation mode, chromatography method, detection mode, and choice of data reduction methods.

    “These include the mode of sample preparation, method of chromatography, mode of detection, and the choice of data reduction methods (116, 117).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [116] Barri, 2012, Metabolic fingerprinting of high-fat plasma samples processed by centrifugation- and filtration-based protein precipitation delineates significant differences in metabolite information coverage, Anal Chim Acta source

      Not checked in the free run.

    • cites [117] Gika, 2010, Does the mass spectrometer define the marker? A comparison of global metabolite profiling data generated simultaneously via UPLC-MS on two different mass spectrometers, Anal Chem source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The metabolic profile of raw data from spectrometric analysis of biological samples can be analyzed in several steps.

    “The metabolic profile of raw data generated by the spectrometric analysis of biological samples can be analyzed in several steps (119, 120).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [119] Katajamaa, 2007, Data processing for mass spectrometry-based metabolomics, J Chromatogr A source

      Not checked in the free run.

    • cites [120] Sugimoto, 2012, bioinformatics tools for mass spectroscopy-based metabolomic data processing and analysis, Current Bioinformatics source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Ion suppression effects and inability to discriminate isomers limit the use of direct flow injection-MS.

    “However, ion suppression effects, due to inefficient ionization of certain ions in complex matrices and the inability to discriminate between isomers, limit the use of this approach.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Multivariate analysis is most commonly used for explorative analysis of metabolic profiling data.

    “Multivariate analysis is most commonly used for explorative analysis of metabolic profiling data (127).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [127] Worley, 2013, Utilities for quantifying separation in PCA/PLS-DA scores plots, Anal Biochem source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    In cross-sectional studies, the large contrast seldom applies, but approximate dose-response relations from food-frequency questionnaires may help identify food intake biomarkers.

    “In cross-sectional studies this large contrast seldom applies, but approximate dose-response relations from food-frequency questionnaires may help in the identification of food intake biomarkers.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    In dietary intervention studies with single foods, the contrast for a good biomarker can be large, sometimes infinite, allowing robust work with small sample sets and discrimination of potential intake biomarkers from subtle changes in endogenous metabolites.

    “In dietary intervention studies with single foods, the contrast observed for a good biomarker can be large, sometimes even infinite, making it possible to work robustly with small sample sets and discriminate potential intake biomarkers from more subtle changes in endogenous metabolites (126).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [126] Kristensen, 2012, LC-MS metabolomics top-down approach reveals new exposure and effect biomarkers of apple and apple-pectin intake, Metabolomics source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisenone given

    Unlike univariate analysis, multivariate analysis can be performed unsupervised, without group assignment information.

    “As opposed to univariate analysis, multivariate analysis can be performed in an unsupervised manner (ie, without including information on group assignment for the analysis).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    These discriminatory biomarkers point to dietary sources, sometimes with cometabolism by gut microbiota.

    “All of these discriminatory biomarkers point to dietary sources, sometimes in combination with cometabolism by gut microbiota.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Alanine is associated with diets that emphasize animal products rather than vegetables.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Although not specific to the food metabolome, these resources are useful for metabolite identification because fragmentation data or NMR signals of known metabolites can be compared with an unknown query to gain structural information.

    “Although they are not specific to the food metabolome, these resources are useful for metabolite identification because fragmentation data or NMR signals of known metabolites can be compared with the unknown query to gain structural information.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    MWASs can be regarded as a special case of the exposome-wide association study, which investigates disease associations with all exposures to low- and high-molecular-weight compounds.

    “In fact, MWASs can be regarded as a special case of the exposome-wide association study, which investigates disease associations with all exposures to low-and high-molecular-weight compounds (167).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [167] Rappaport, 2012, Biomarkers intersect with the exposome, Biomarkers source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Recently, many food compounds have been added to the HMDB, enabling searches based on accurate masses, but it currently contains few mass fragmentation spectra useful for food metabolite identification.

    “Recently, a large number of food compounds have been added to the HMDB, which makes searches on the basis of their accurate masses possible (9); however, to date it contains few mass fragmentation spectra useful for food metabolite identification.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Wishart, 2013, HMDB 3.0—the Human Metabolome Database in 2013, Nucleic Acids Res

      Not checked in the free run.

  • May combine two claims.

    Premisereasoning

    The untargeted metabolomic approach does not presuppose which exposure sources cause a given disease; it compares comprehensive metabolomic profiles between cases and controls to find discriminating exposure biomarkers.

    “The alternative untargeted approach makes no a priori assumptions regarding sources of exposure that are causal for a particular disease but instead relies on comparisons of comprehensive profiles of metabolomic features between cases and controls to find discriminating exposure biomarkers.”
    Quote in the paperSubstantial claim

  • May combine two claims. The quote only partly states this claim.

    Premisecitation

    Three highly discriminating biomarkers were identified in the INTERMAP study: alanine was directly correlated with blood pressure, while formate and hippurate were inversely correlated with blood pressure.

    “biomarkers were identified, namely alanine, which was directly correlated with blood pressure, and formate and hippurate, both of which were inversely correlated with blood pressure.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [59] Holmes, 2008, Human metabolic phenotype diversity and its association with diet and blood pressure, Nature source

      Not checked in the free run.

    • cites [166] Bictash, 2010, Opening up the “black box”: metabolic phenotyping and metabolome-wide association studies in epidemiology, J Clin Epidemiol source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationnone given

    These associations were tentatively explained by either different amounts of dietary intake or differential fatty acid metabolism in cases and controls.

    “These associations were tentatively explained by either different amounts of dietary intake or differential fatty acid metabolism in cases and controls.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    SciFinder is currently the most comprehensive and best-curated commercial chemical database, including many food metabolome compounds collected from the literature.

    “The most comprehensive and best-curated chemical (commercial) database is currently SciFinder, which includes many food metabolome compounds collected from the literature (151).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [151] American Chemical Society. SciFinder. Available from: https://scifinder.cas.org (cited 3 September 2013).

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The Human Metabolome Database has recently expanded to include compounds found in common foods because, before metabolism, these compounds are also present in the human body.

    “The human metabolome database has recently expanded to include compounds found in common foods because these are, at least initially before metabolism, also present within the human body (9).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Wishart, 2013, HMDB 3.0—the Human Metabolome Database in 2013, Nucleic Acids Res

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Genome-wide analysis studies have identified loci associated with variations in endogenous metabolite concentrations, and many of these genes coded for metabolic enzymes.

    “A number of loci associated with variations in the concentration of endogenous metabolites could be identified in genome-wide analysis studies, and many of these genes were coding for metabolic enzymes (180-182).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [180] Suhre, 2011, Human metabolic individuality in biomedical and pharmaceutical research, Nature source

      Not checked in the free run.

    • cites [181] Illig, 2010, A genome-wide perspective of genetic variation in human metabolism, Nat Genet source

      Not checked in the free run.

    • cites [182] Kettunen, 2012, Genome-wide association study identifies multiple loci influencing human serum metabolite levels, Nat Genet source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The Metabolomics Standards Initiative launched by the Metabolomics Society has already had significant impact on reporting formats in metabolomics.

    “The Metabolomics Standards Initiative (MSI) launched by the Metabolomics Society is an example of such an initiative, and the MSI has already had significant impact on reporting formats in metabolomics (110, 188).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [110] Sumner, 2007, Proposed minimum reporting standards for chemical analysis, Metabolomics source

      Not checked in the free run.

    • cites [188] Fiehn, 2007, The Metabolomics Standards Initiative (MSI), Metabolomics source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Many studies have been conducted with oranges, but broad coverage of all citrus and many other fruits, as well as kinetic studies, were necessary to interpret proline betaine as a short-term marker of citrus dominated by orange and orange juice intake.

    “For example, many studies have been conducted with oranges (Table 3), but a broad coverage of all citrus and many other fruit as well as kinetic studies have been necessary to interpret proline betaine as a short-term marker of citrus that is dominated by orange and orange juice intake (80).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [80] Heinzmann, 2010, Metabolic profiling strategy for discovery of nutritional biomarkers: proline betaine as a marker of citrus consumption, Am J Clin Nutr source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Some commercial software exists for the pharmaceutical area and covers many phase I and II reactions.

    “Some commercial software exists for the pharmaceutical area (192,193) and covers many phase I and II reactions.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [192] T’Jollyn, 2011, Evaluation of three state-of-the-art metabolite prediction software packages (Meteor, MetaSite, and StarDrop) through independent and synergistic use, Drug Metab Dispos source

      Not checked in the free run.

    • cites [193] Piechota, 2013, pragmatic approaches to using computational methods to predict xenobiotic metabolism, J Chem Inf Model source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    These biomarkers should also significantly contribute to better understanding of the complex interactions between diet and human health.

    “They should also significantly contribute to a better understanding of the complex interactions between diet and human health.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The Metabolomics Standards Initiative has already issued several reference articles on good practice for metabolomic research.

    “The MSI, initiated by the Metabolomics Society, has already issued several reference articles on good practice for metabolomic research.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [189] Metabolomics Standards Initiative. Homepage. Available from: http://msi-workgroups.sourceforge.net/ (cited 3 September 2013).

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Metabolomic approaches could greatly expand molecular nutritional epidemiology and contribute to future progress in nutrition research.

    “Some proof-of-principle studies have established the feasibility of metabolomic approaches to identify novel dietary biomarkers and suggest that these approaches could greatly expand the field of molecular nutritional epidemiology and contribute to future progress in nutrition research.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Several training workshops on metabolomics and nutrition were supported by the Nutrigenomics Organization.

    “Several training workshops on metabolomics and nutrition were supported by the Nutrigenomics Organization (112).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [112] Scalbert, 2009, Mass-spectrometry-based metabolomics: limitations and recommendations for future progress with particular focus on nutrition research, Metabolomics source

      Not checked in the free run.

72 of 72

  • The paper relies on this without support.

    The food metabolome spans a huge range of concentrations, from picomolar or nanomolar for some contaminants or phytochemical metabolites to millimolar for nutrients such as sugars.

    “A second feature of the food metabolome is the huge range of concentrations, from picomolar or nanomolar concentrations for some contaminants or phytochemical metabolites to millimolar concentrations for nutrients such as sugars.”

  • The paper relies on this without support.

    Many components of the food metabolome are unknown.

    “Third, many components of the food metabolome are unknown.”

  • The paper relies on this without support.

    The metabolism of a large proportion of nonnutrients in humans has never been studied, and the chemical structures of their circulating metabolites have not been identified.

    “Indeed, the metabolism for a large proportion of nonnutrients in humans has never been studied and the chemical structures of their circulating metabolites have not been identified.”

  • The paper relies on this without support.

    Plasma or serum samples are more commonly available in biobanks than other biospecimens.

    “More metabolomic studies using blood samples should be carried out because of the more common availability of plasma or serum samples in biobanks.”

  • The paper relies on this without support.

    Alanine is associated with diets that emphasize animal products rather than vegetables.

    “alanine is associated with diets that emphasize animal products rather than vegetables”

  • The paper relies on this without support.

    Many compounds in foods have structures that are uncommon in pharmaceuticals.

    “many compounds in foods have structures that are uncommon in pharmaceuticals.”

  • The paper relies on this without support.

    Food constituents may be degraded by specialized enzymes and may also be extensively metabolized by gut microbiota.

    “Food constituents may be degraded by specialized enzymes and may also be extensively metabolized by the gut microbiota”

  • The paper relies on this without support.

    The large majority of components of the food metabolome are not commercially available.

    “The large majority of the components of the food metabolome are not commercially available.”

  • The paper relies on this without support.

    Definitive identification of biomarkers is often hampered by the lack of available chemical standards.

    “The definitive identification of biomarkers is often hampered by the lack of available chemical standards.”

  • The paper relies on this without support.

    The food metabolome is exceedingly complex because it encompasses metabolites derived from as many metabolomes as there are edible species.

    “The food metabolome is exceedingly complex because it encompasses metabolites derived from as many metabolomes as there are edible species.”

  • The paper relies on this without support.

    Within one group, it is difficult to cover all the techniques and methods required to perform a comprehensive metabolomic study.

    “Within one group, it is difficult to cover all the techniques and methods required to perform a comprehensive metabolomic study.”

  • The paper relies on this without support.

    For many funding agencies, data sharing is becoming a key condition of funding.

    “for many funding agencies, this is becoming a key condition of funding.”

  • The paper relies on this without support.

    There is no current standardization initiative for the food metabolome.

    “there is no current standardization initiative for the food metabolome”
13 of 13

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Cites

Flagged first, then by citations

5 of the 198 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Zamora-Ros R, Touillaud M, Rothwell JA, Romieu I, Scalbert A. Measuring exposure to the polyphenol metabolome in epidemiological studies: current tools, applications and their limits. Am J Clin Nutr (in press).

Cited by

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Related

Authors
Scalbert, A., Brennan, L., Manach, C., Andres-Lacueva, C., Dragsted, L. O., Draper, J., Rappaport, S. M., van der Hooft, J. J., & Wishart, D. S.
Affiliations
University College Dublin (IE)
ORCID
Venue
The American Journal of Clinical Nutrition
Publisher
Elsevier BV
Published
2014-06
Volume
99
Issue
6
Pages
1286-1308
ISSN
0002-9165 (ISSN-L)
DOI
10.3945/ajcn.113.076133
OpenAlex
W2169779482
Cited by
519
References
198
Citations by year
2026: 19 · 2025: 32 · 2024: 38 · 2023: 27 · 2022: 39 · 2021: 50 · 2020: 49 · 2019: 40 · 2018: 61 · 2017: 60 · 2016: 61 · 2015: 25 · 2014: 16
FWCI
5.08
Type
journal article
Language
en
Open access
Licence
Locations
  • American Journal of Clinical Nutrition (publishedVersion, other-oa)
  • PubMed (publishedVersion)
  • HAL (submittedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Funders
  • World Health Organization
  • European Commission (KBBE-2011-5, FP7-KBBE-2011–5, 289511, 260791)
  • Agence Nationale de la Recherche (ANR-10-ALIA-0007, ANR-10)
  • Medical Research Council (MR/J010308/1)
  • FP7 Food, Agriculture and Fisheries, Biotechnology
  • CHIST-ERA
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Nutrition, Genetics, and Disease
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
Keywords
dietary biomarkers, dietary exposure assessment, metabolomics, metabolomics databases, dietary bioactive compounds
MeSH terms
Animals, Diet, Digestion, Food, Humans, Models, Biological, Biomarkers, Nutritional Sciences, Metabolomics, Metabolome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-07.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-07.

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