ArticleCancer research2014
Noninvasive urinary metabolomic profiling identifies diagnostic and prognostic markers in lung cancer.
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Article in Cancer research, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 114 papers, 1 of them a synthesis that pooled it.
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114citing papers in PubMed, 1 pooled it
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Who cites it
114 citing papers in PubMed, 1 synthesis or guideline pooled it, 195 citations in OpenAlex.
- Metabolomics and metabolites in cancer diagnosis and treatment.Molecular biomedicine · 2025Pooled it
- Urinary 27-nor-5β-cholestane-3α,7α,12α,24medRxiv : the preprint server for health sciences · 2026Article
- The urinary-metabolite-based lung cancer index (uLCI): an interpretable machine-learning risk model for early-stage disease.medRxiv : the preprint server for health sciences · 2026Article
- miR-4513 promotes the proliferation and metastasis of non-small cell lung cancer cells by targeting VIPR1.Hereditas · 2026Article
- Application of untargeted plasma metabolomics and machine learning to construct a diagnostic model for hypertrophic cardiomyopathy: a case-control study.Metabolomics : Official journal of the Metabolomic Society · 2026Article
- Ensemble learning on serum metabolic fingerprints for early detection of lung adenocarcinoma.NPJ precision oncology · 2026Article
- Identification of High-Performing Blood Metabolite Biomarkers of Lung Cancer in a Chinese Population.Phenomics (Cham, Switzerland) · 2026Article
- The Omics Molecule Extractor: A Web Application for the Selection of Potential Biomarker Panels.Journal of proteome research · 2026Article
- 2,3-Pyridinedicarboxylate Is Associated with Shorter Recurrence-Free Survival in Patients with Hypopharyngeal Squamous Cell Carcinoma.Pathobiology : journal of immunopathology, molecular and cellular biology · 2026Article
- Prospective proteomics for discovering biomarkers in lung adenocarcinoma: a literature review.Translational cancer research · 2025Review
- Metabolite biomarkers in lung cancer: unlocking the potential of body fluid analysis for early detection and prognosis-a narrative review.Translational lung cancer research · 2025Review
- Urinary Metabolites and Survival in Malignant Mesothelioma.medRxiv : the preprint server for health sciences · 2025Article
- All-flexible chronoepifluidic nanoplasmonic patch for label-free metabolite profiling in sweat.Nature communications · 2025Article
- Identification of urinary metabolic biomarkers for histone 3 lysine27-to-methionine mutation diagnosis in brainstem gliomas.Neuro-oncology · 2025Article
- Semi-Supervised Learned Autoencoder for Classification of Events in Distributed Fibre Acoustic Sensors.Sensors (Basel, Switzerland) · 2025Article
- Rapid and Noninvasive Early Detection of Lung Cancer by Integration of Machine Learning and Salivary Metabolic Fingerprints Using MS LOC Platform: A Large-Scale Multicenter Study.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Article
- Mass-spectrometry based metabolomics: an overview of workflows, strategies, data analysis and applications.Proteome science · 2025Review
- Analysis of time-fractional cancer-tumor immunotherapy model using modified He-Laplace algorithm.Scientific reports · 2025Article
- Metabolomic Profiling of Disease Progression Following Radiotherapy for Breast Cancer.Cancers · 2025Article
- Clinical metabolomics in type 2 diabetes mellitus: from pathogenesis to biomarkers.Frontiers in endocrinology · 2025Review
54 more citing papers are in PubMed but not listed here.
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Authors and funding
14 authors at 4 institutions in 2 countries.
Ewy A MathéAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, SwitzerlandAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Andrew D PattersonAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Majda HaznadarAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Soumen K MannaAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Kristopher W KrauszAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Elise D BowmanAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Peter G ShieldsAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Jeffrey R IdleAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Philip B SmithAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Katsuhiro AnamiAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Dickran G KazandjianAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Emmanuel HatzakisAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Frank J GonzalezAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland.
Curtis C HarrisAuthors' Affiliations: Laboratory of Molecular Immunogenomics, Genomic and Immunity Section, NIAMS/NIH; Laboratories of Human Carcinogenesis, and Metabolism, National Cancer Institute, NIH, Bethesda, Maryland; Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis; Metabolomics Core Facility; Nuclear Magnetic Resonance Spectroscopy, The Pennsylvania State University, University Park, Pennsylvania; Ohio State University Comprehensive Cancer Center, Columbus, Ohio; and Department of Clinical Research, University of Bern, Bern, Switzerland Curtis_Harris@nih.gov.
National Cancer Institute · USUniversity of Bern · CHThe Ohio State University · USPennsylvania State University · US
Funding
Translational Therapeutics Research Program (TT)P30CA016058 · NCI · OHIO STATE UNIVERSITY · PI Tasleem J Padamsee · 1985 to 2026
$132.3MPrecision Medicine of CancerZIABC011492 · NCI · DIVISION OF BASIC SCIENCES - NCI · PI HARRIS, CURTIS · 2013 to 2025
$23.2MOptimized Metabolite Extraction, Separation, and Identification for MetabolomicsR01ES022186 · NIEHS · PENNSYLVANIA STATE UNIVERSITY, THE · PI PATTERSON, ANDREW · 2012 to 2016
$2.0MIntramural NIH HHS Z99 CA999999NCI NIH HHS P30 CA016058NIEHS NIH HHS ES022186NIEHS NIH HHS R01 ES022186
Abstract
Lung cancer remains the most common cause of cancer deaths worldwide, yet there is currently a lack of diagnostic noninvasive biomarkers that could guide treatment decisions. Small molecules (<1,500 Da) were measured in urine collected from 469 patients with lung cancer and 536 population controls using unbiased liquid chromatography/mass spectrometry. Clinical putative diagnostic and prognostic biomarkers were validated by quantitation and normalized to creatinine levels at two different time points and further confirmed in an independent sample set, which comprises 80 cases and 78 population controls, with similar demographic and clinical characteristics when compared with the training set. Creatine riboside (IUPAC name: 2-{2-[(2R,3R,4S,5R)-3,4-dihydroxy-5-(hydroxymethyl)-oxolan-2-yl]-1-methylcarbamimidamido}acetic acid), a novel molecule identified in this study, and N-acetylneuraminic acid (NANA) were each significantly (P < 0.00001) elevated in non-small cell lung cancer and associated with worse prognosis [HR = 1.81 (P = 0.0002), and 1.54 (P = 0.025), respectively]. Creatine riboside was the strongest classifier of lung cancer status in all and stage I-II cases, important for early detection, and also associated with worse prognosis in stage I-II lung cancer (HR = 1.71, P = 0.048). All measurements were highly reproducible with intraclass correlation coefficients ranging from 0.82 to 0.99. Both metabolites were significantly (P < 0.03) enriched in tumor tissue compared with adjacent nontumor tissue (N = 48), thus revealing their direct association with tumor metabolism. Creatine riboside and NANA may be robust urinary clinical metabolomic markers that are elevated in tumor tissue and associated with early lung cancer diagnosis and worse prognosis.
Indexed as
AgedBiomarkers, TumorCarcinoma, Non-Small-Cell LungCase-Control StudiesCreatineFemaleHumansKaplan-Meier EstimateLung NeoplasmsMaleMetabolomeMiddle AgedN-Acetylneuraminic AcidPrognosisProportional Hazards ModelsRibonucleosides2-(2-(3,4-dihydroxy-5-(hydroxymethyl)oxolan-2-yl)-1-methylcarbamimidamido)acetic acidBiomarkers, TumorCreatineN-Acetylneuraminic AcidRibonucleosides
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