Discovery and validation of urinary metabotypes for the diagnosis of hepatocellular carcinoma in West Africans

There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha‐fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Uri...

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Published inHepatology (Baltimore, Md.) Vol. 60; no. 4; pp. 1291 - 1301
Main Authors Ladep, Nimzing G., Dona, Anthony C., Lewis, Matthew R., Crossey, Mary M.E., Lemoine, Maud, Okeke, Edith, Shimakawa, Yusuke, Duguru, Mary, Njai, Harr F., Fye, Haddy K.S., Taal, Makie, Chetwood, John, Kasstan, Ben, Khan, Shahid A., Garside, Deborah A., Wijeyesekera, Anisha, Thillainayagam, Andrew V., Banwat, Edmund, Thursz, Mark R., Nicholson, Jeremy K., Njie, Ramou, Holmes, Elaine, Taylor‐Robinson, Simon D.
Format Journal Article
LanguageEnglish
Published United States Wolters Kluwer Health, Inc 01.10.2014
Wiley-Blackwell
Subjects
Online AccessGet full text
ISSN0270-9139
1527-3350
1527-3350
DOI10.1002/hep.27264

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Abstract There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha‐fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case‐control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance (1H‐NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78‐0.94), 0.93 (0.89‐0.97), and 0.89 (0.80‐0.98) in the training set and 0.81 (0.73‐0.89), 0.96 (0.94‐0.99), and 0.90 (0.85‐0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole‐3‐acetate, galactose, and an N‐acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8‐94.2]) and specificity (90.3% [74.2‐98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP = 0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1‐methylnicotinamide, methionine, acetylcarnitine, 2‐oxoglutarate, choline, and creatine. Conclusion: The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP. (Hepatology 2014;60:1291–1301)
AbstractList There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance (1H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel=0.72; AFP=0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine. Conclusion: The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP. (Hepatology 2014;60:1291-1301) [PUBLICATION ABSTRACT]
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance ((1) H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP =  0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine. The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP.
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance ( super(1)H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel=0.72; AFP=0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine. Conclusion: The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP. (Hepatology 2014; 60:1291-1301)
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance ((1) H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP = 0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine.Conclusion: The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP.
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance ((1) H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP =  0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine.UNLABELLEDThere is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case-control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance ((1) H-NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78-0.94), 0.93 (0.89-0.97), and 0.89 (0.80-0.98) in the training set and 0.81 (0.73-0.89), 0.96 (0.94-0.99), and 0.90 (0.85-0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole-3-acetate, galactose, and an N-acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8-94.2]) and specificity (90.3% [74.2-98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP =  0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1-methylnicotinamide, methionine, acetylcarnitine, 2-oxoglutarate, choline, and creatine.The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP.CONCLUSIONThe urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP.
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha‐fetoprotein (AFP) is too low for this purpose. Here, we determined the diagnostic performance of a panel of urinary metabolites of HCC patients from West Africa. Urine samples were collected from Nigerian and Gambian patients recruited on the case‐control platform of the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) program. Urinary proton nuclear magnetic resonance (1H‐NMR) spectroscopy was used to metabolically phenotype 290 subjects: 63 with HCC; 32 with cirrhosis (Cir); 107 with noncirrhotic liver disease (DC); and 88 normal control (NC) healthy volunteers. Urine samples from a further cohort of 463 subjects (141 HCC, 56 Cir, 178 DC, and 88 NC) were analyzed, the results of which validated the initial cohort. The urinary metabotype of patients with HCC was distinct from those with Cir, DC, and NC with areas under the receiver operating characteristic (AUROC) curves of 0.86 (0.78‐0.94), 0.93 (0.89‐0.97), and 0.89 (0.80‐0.98) in the training set and 0.81 (0.73‐0.89), 0.96 (0.94‐0.99), and 0.90 (0.85‐0.96), respectively, in the validation cohort. A urinary metabolite panel, comprising inosine, indole‐3‐acetate, galactose, and an N‐acetylated amino acid (NAA), showed a high sensitivity (86.9% [75.8‐94.2]) and specificity (90.3% [74.2‐98.0]) in the discrimination of HCC from cirrhosis, a finding that was corroborated in a validation cohort (AUROC: urinary panel = 0.72; AFP = 0.58). Metabolites that were significantly increased in urine of HCC patients, and which correlated with clinical stage of HCC, were NAA, dimethylglycine, 1‐methylnicotinamide, methionine, acetylcarnitine, 2‐oxoglutarate, choline, and creatine. Conclusion: The urinary metabotyping of this West African cohort identified and validated a metabolite panel that diagnostically outperforms serum AFP. (Hepatology 2014;60:1291–1301)
Author Thillainayagam, Andrew V.
Holmes, Elaine
Dona, Anthony C.
Taal, Makie
Lemoine, Maud
Njie, Ramou
Nicholson, Jeremy K.
Kasstan, Ben
Ladep, Nimzing G.
Duguru, Mary
Khan, Shahid A.
Shimakawa, Yusuke
Banwat, Edmund
Garside, Deborah A.
Fye, Haddy K.S.
Chetwood, John
Lewis, Matthew R.
Okeke, Edith
Thursz, Mark R.
Taylor‐Robinson, Simon D.
Njai, Harr F.
Wijeyesekera, Anisha
Crossey, Mary M.E.
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Cites_doi 10.1186/1746-1596-8-45
10.1016/j.cca.2012.12.024
10.1039/b820224a
10.1021/pr300502v
10.1002/hep.24199
10.4161/cc.22137
10.1053/j.gastro.2003.10.065
10.1038/nprot.2007.376
10.1021/ac00101a004
10.1016/j.aca.2011.02.038
10.1016/j.aca.2009.06.033
10.7314/APJCP.2012.13.9.4695
10.1021/ac048630x
10.1002/ijc.21731
10.1021/pr901058t
10.1007/s00216-011-5245-3
10.1055/s-2007-1007122
10.1007/s00216-012-5782-4
10.1002/(SICI)1099-1492(1998110)11:7<354::AID-NBM515>3.0.CO;2-N
10.1021/pr070063h
10.1016/S0168-8278(02)00297-0
10.1007/s10555-011-9334-8
10.1021/pr2005764
10.1016/j.ccr.2012.02.014
10.3322/canjclin.55.2.74
10.1016/j.taap.2004.06.031
10.1038/nature11708
10.1021/pr101096f
10.1053/j.gastro.2007.04.061
10.1007/s12603-009-0204-9
10.1038/nrc3162
ContentType Journal Article
Copyright 2014 by the American Association for the Study of Liver Diseases
2014 by the American Association for the Study of Liver Diseases.
Distributed under a Creative Commons Attribution 4.0 International License
Copyright_xml – notice: 2014 by the American Association for the Study of Liver Diseases
– notice: 2014 by the American Association for the Study of Liver Diseases.
– notice: Distributed under a Creative Commons Attribution 4.0 International License
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Notes This study was funded by the European Union Framework 7 programme (PROLIFICA: Prevention of Fibrosis and Liver Cancer in Africa). N.G.L. was supported by a fellowship from the Trustees of the London Clinic, London, UK and by the British Medical Research Council ICIC scheme. M.M.E.C. was supported by a fellowship (Halley Stewart Foundation, Cambridge, United Kingdom).
Potential conflict of interest: Nothing to report.
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References 2002; 37
2004; 127
2004; 126
2010; 19
2011; 53
2011; 11
2011; 10
2011; 691
2012; 13
2013; 8
2006; 118
2012; 56
2012; 403
2012; 11
2012; 31
2007; 37
2012; 491
2011; 401
2009; 13
1999; 19
2013; 418
2007; 132
1995; 67
2005; 204
2007; 6
2009; 5
2007; 2
2007; 1
2009; 648
2005; 55
2005; 77
2012; 21
1998; 11
2010; 9
Ferenci (R3-22-20250207) 2010; 19
Shariff (R31-22-20250207) 2010; 9
Heinzmann (R38-22-20250207) 2012; 11
Glunde (R33-22-20250207) 2011; 11
Nicholson (R10-22-20250207) 2012; 491
Shariff (R21-22-20250207) 2011; 10
Ye (R17-22-20250207) 2012; 11
Bollard (R25-22-20250207) 2005; 204
ElSerag (R6-22-20250207) 2004; 126
Wang (R18-22-20250207) 2013; 418
Shariff (R20-22-20250207) 2010; 9
Polanski (R28-22-20250207) 2007; 1
Khan (R4-22-20250207) 2002; 37
Wu (R16-22-20250207) 2009; 648
Chen (R13-22-20250207) 2011; 10
Macuks (R29-22-20250207) 2012; 13
Costello (R36-22-20250207) 2012; 31
Ward (R35-22-20250207) 2012; 21
Cao (R11-22-20250207) 2011; 691
Beckonert (R24-22-20250207) 2007; 2
Pahor (R37-22-20250207) 2009; 13
Bruix (R19-22-20250207) 2011; 53
Llovet (R23-22-20250207) 1999; 19
Parkin (R1-22-20250207) 2006; 118
Dong (R30-22-20250207) 2013; 8
MartinezOutschoorn (R32-22-20250207) 2012; 11
Cloarec (R27-22-20250207) 2005; 77
Chen (R12-22-20250207) 2011; 401
Yin (R14-22-20250207) 2009; 5
Zhou (R15-22-20250207) 2012; 403
ElSerag (R5-22-20250207) 2007; 132
Yang (R9-22-20250207) 2007; 6
Bell (R34-22-20250207) 1998; 11
Parkin (R2-22-20250207) 2005; 55
Nicholson (R26-22-20250207) 1995; 67
References_xml – volume: 11
  start-page: 3964
  year: 2012
  end-page: 3971
  article-title: Ketone body utilization drives tumor growth and metastasis
  publication-title: Cell Cycle
– volume: 132
  start-page: 2557
  year: 2007
  end-page: 2576
  article-title: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis
  publication-title: Gastroenterology
– volume: 10
  start-page: M110
  year: 2011
  article-title: Serum and urine metabolite profiling reveals potential biomarkers of human hepatocellular carcinoma
  publication-title: Mol Cell Proteomics
– volume: 9
  start-page: 1096
  year: 2010
  end-page: 1103
  article-title: Characterization of urinary biomarkers of hepatocellular carcinoma using magnetic resonance spectroscopy in a Nigerian population
  publication-title: J Proteome Res
– volume: 648
  start-page: 98
  year: 2009
  end-page: 104
  article-title: Metabolomic profiling of human urine in hepatocellular carcinoma patients using gas chromatography/mass spectrometry
  publication-title: Anal Chim Acta
– volume: 127
  start-page: S108
  issue: 5 Suppl. 1
  year: 2004
  end-page: S112
  article-title: Alpha‐fetoprotein and ultrasonography screening for hepatocellular carcinoma
  publication-title: Gastroenterology
– volume: 13
  start-page: 724
  year: 2009
  end-page: 728
  article-title: Sarcopenia: clinical evaluation, biological markers and other evaluation tools
  publication-title: J Nutr Health Aging
– volume: 56
  start-page: 908
  year: 2012
  end-page: 943
  article-title: management of hepatocellular carcinoma
  publication-title: J Hepatol
– volume: 13
  start-page: 4695
  year: 2012
  end-page: 4698
  article-title: Urinary concentrations of human epidydimis secretory protein 4 (He4) in the diagnosis of ovarian cancer: a case‐control study
  publication-title: Asian Pac J Cancer Prev
– volume: 55
  start-page: 74
  year: 2005
  end-page: 108
  article-title: Global cancer statistics, 2002
  publication-title: CA Cancer J Clin
– volume: 21
  start-page: 297
  year: 2012
  end-page: 308
  article-title: Metabolic reprogramming: a cancer hallmark even warburg did not anticipate
  publication-title: Cancer Cell
– volume: 53
  start-page: 1020
  year: 2011
  end-page: 1022
  article-title: Management of hepatocellular carcinoma: an update
  publication-title: Hepatology
– volume: 11
  start-page: 643
  year: 2012
  end-page: 655
  article-title: Stability and robustness of human metabolic phenotypes in response to sequential food challenges
  publication-title: J Proteome Res
– volume: 19
  start-page: 311
  year: 2010
  end-page: 317
  article-title: World Gastroenterology Organisation Guideline. Hepatocellular carcinoma (HCC): a global perspective
  publication-title: J Gastrointestin Liver Dis
– volume: 204
  start-page: 135
  year: 2005
  end-page: 151
  article-title: Comparative metabonomics of differential hydrazine toxicity in the rat and mouse
  publication-title: Toxicol Appl Pharmacol
– volume: 67
  start-page: 793
  year: 1995
  end-page: 811
  article-title: 750 MHz 1H and 1H‐13C NMR spectroscopy of human blood plasma
  publication-title: Anal Chem
– volume: 403
  start-page: 203
  year: 2012
  end-page: 213
  article-title: Serum metabolomics reveals the deregulation of fatty acids metabolism in hepatocellular carcinoma and chronic liver diseases
  publication-title: Anal Bioanal Chem
– volume: 6
  start-page: 2605
  year: 2007
  end-page: 2614
  article-title: Metabonomic studies of human hepatocellular carcinoma using high‐resolution magic‐angle spinning 1H NMR spectroscopy in conjunction with multivariate data analysis
  publication-title: J Proteome Res
– volume: 11
  start-page: 4361
  year: 2012
  end-page: 4372
  article-title: Analysis of urinary metabolic signatures of early hepatocellular carcinoma recurrence after surgical removal using gas chromatography‐mass spectrometry
  publication-title: J Proteome Res
– volume: 19
  start-page: 329
  year: 1999
  end-page: 338
  article-title: Prognosis of hepatocellular carcinoma: the BCLC staging classification
  publication-title: Semin Liver Dis
– volume: 691
  start-page: 68
  year: 2011
  end-page: 75
  article-title: Fecal metabolome profiling of liver cirrhosis and hepatocellular carcinoma patients by ultra performance liquid chromatography‐mass spectrometry
  publication-title: Anal Chim Acta
– volume: 401
  start-page: 1899
  year: 2011
  end-page: 1904
  article-title: Identification of serum biomarkers of hepatocarcinoma through liquid chromatography/mass spectrometry‐based metabonomic method
  publication-title: Anal Bioanal Chem
– volume: 37
  start-page: 806
  year: 2002
  end-page: 813
  article-title: Changing international trends in mortality rates for liver, biliary and pancreatic tumours
  publication-title: J Hepatol
– volume: 2
  start-page: 2692
  year: 2007
  end-page: 2703
  article-title: Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts
  publication-title: Nat Protoc
– volume: 77
  start-page: 1282
  year: 2005
  end-page: 1289
  article-title: Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets
  publication-title: Anal Chem
– volume: 8
  start-page: 45
  year: 2013
  article-title: The endothelial lipase protein is promising urinary biomarker for diagnosis of gastric cancer
  publication-title: Diagn Pathol
– volume: 5
  start-page: 868
  year: 2009
  end-page: 876
  article-title: A metabonomic study of hepatitis B‐induced liver cirrhosis and hepatocellular carcinoma by using RP‐LC and HILIC coupled with mass spectrometry
  publication-title: Mol Biosyst
– volume: 126
  start-page: 460
  year: 2004
  end-page: 468
  article-title: Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma
  publication-title: Gastroenterology
– volume: 418
  start-page: 86
  year: 2013
  end-page: 90
  article-title: Urinary metabolic profiling identifies a key role for glycocholic acid in human liver cancer by ultra‐performance liquid‐chromatography coupled with high‐definition mass spectrometry
  publication-title: Clin Chim Acta
– volume: 37
  start-page: S88
  issue: Suppl. 2
  year: 2007
  end-page: S94
  article-title: Epidemiology of hepatocellular carcinoma in USA
  publication-title: Hepatol Res
– volume: 1
  start-page: 1
  year: 2007
  end-page: 48
  article-title: A list of candidate cancer biomarkers for targeted proteomics
  publication-title: Biomark Insights
– volume: 118
  start-page: 3030
  year: 2006
  end-page: 3044
  article-title: The global health burden of infection‐associated cancers in the year 2002
  publication-title: Int J Cancer
– volume: 10
  start-page: 1828
  year: 2011
  end-page: 1836
  article-title: Urinary metabolic biomarkers of hepatocellular carcinoma in an egyptian population: a validation study
  publication-title: J Proteome Res
– volume: 491
  start-page: 384
  year: 2012
  end-page: 392
  article-title: Metabolic phenotyping in clinical and surgical environments
  publication-title: Nature
– volume: 11
  start-page: 835
  year: 2011
  end-page: 848
  article-title: Choline metabolism in malignant transformation
  publication-title: Nat Rev Cancer
– volume: 11
  start-page: 354
  year: 1998
  end-page: 359
  article-title: Metabolic changes underlying 31P MR spectral alterations in human hepatic tumours
  publication-title: NMR Biomed
– volume: 31
  start-page: 123
  year: 2012
  end-page: 130
  article-title: The genetic/metabolic transformation concept of carcinogenesis
  publication-title: Cancer Metastasis Rev
– volume: 8
  start-page: 45
  year: 2013
  ident: R30-22-20250207
  article-title: The endothelial lipase protein is promising urinary biomarker for diagnosis of gastric cancer.
  publication-title: Diagn Pathol
  doi: 10.1186/1746-1596-8-45
– volume: 418
  start-page: 86
  year: 2013
  ident: R18-22-20250207
  article-title: Urinary metabolic profiling identifies a key role for glycocholic acid in human liver cancer by ultraperformance liquidchromatography coupled with highdefinition mass spectrometry.
  publication-title: Clin Chim Acta
  doi: 10.1016/j.cca.2012.12.024
– volume: 5
  start-page: 868
  year: 2009
  ident: R14-22-20250207
  article-title: A metabonomic study of hepatitis Binduced liver cirrhosis and hepatocellular carcinoma by using RPLC and HILIC coupled with mass spectrometry.
  publication-title: Mol Biosyst
  doi: 10.1039/b820224a
– volume: 11
  start-page: 4361
  year: 2012
  ident: R17-22-20250207
  article-title: Analysis of urinary metabolic signatures of early hepatocellular carcinoma recurrence after surgical removal using gas chromatographymass spectrometry.
  publication-title: J Proteome Res
  doi: 10.1021/pr300502v
– volume: 53
  start-page: 1020
  year: 2011
  ident: R19-22-20250207
  article-title: Management of hepatocellular carcinoma: an update.
  publication-title: Hepatology
  doi: 10.1002/hep.24199
– volume: 11
  start-page: 3964
  year: 2012
  ident: R32-22-20250207
  article-title: Ketone body utilization drives tumor growth and metastasis.
  publication-title: Cell Cycle
  doi: 10.4161/cc.22137
– volume: 126
  start-page: 460
  year: 2004
  ident: R6-22-20250207
  article-title: Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma.
  publication-title: Gastroenterology
  doi: 10.1053/j.gastro.2003.10.065
– volume: 2
  start-page: 2692
  year: 2007
  ident: R24-22-20250207
  article-title: Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts.
  publication-title: Nat Protoc
  doi: 10.1038/nprot.2007.376
– volume: 67
  start-page: 793
  year: 1995
  ident: R26-22-20250207
  article-title: 750 MHz 1H and 1H13C NMR spectroscopy of human blood plasma.
  publication-title: Anal Chem
  doi: 10.1021/ac00101a004
– volume: 1
  start-page: 1
  year: 2007
  ident: R28-22-20250207
  article-title: A list of candidate cancer biomarkers for targeted proteomics.
  publication-title: Biomark Insights
– volume: 691
  start-page: 68
  year: 2011
  ident: R11-22-20250207
  article-title: Fecal metabolome profiling of liver cirrhosis and hepatocellular carcinoma patients by ultra performance liquid chromatographymass spectrometry.
  publication-title: Anal Chim Acta
  doi: 10.1016/j.aca.2011.02.038
– volume: 648
  start-page: 98
  year: 2009
  ident: R16-22-20250207
  article-title: Metabolomic profiling of human urine in hepatocellular carcinoma patients using gas chromatographymass spectrometry.
  publication-title: Anal Chim Acta
  doi: 10.1016/j.aca.2009.06.033
– volume: 13
  start-page: 4695
  year: 2012
  ident: R29-22-20250207
  article-title: Urinary concentrations of human epidydimis secretory protein 4 (He4) in the diagnosis of ovarian cancer: a casecontrol study.
  publication-title: Asian Pac J Cancer Prev
  doi: 10.7314/APJCP.2012.13.9.4695
– volume: 77
  start-page: 1282
  year: 2005
  ident: R27-22-20250207
  article-title: Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets.
  publication-title: Anal Chem
  doi: 10.1021/ac048630x
– volume: 118
  start-page: 3030
  year: 2006
  ident: R1-22-20250207
  article-title: The global health burden of infectionassociated cancers in the year 2002.
  publication-title: Int J Cancer
  doi: 10.1002/ijc.21731
– volume: 9
  start-page: 1096
  year: 2010
  ident: R20-22-20250207
  article-title: Characterization of urinary biomarkers of hepatocellular carcinoma using magnetic resonance spectroscopy in a Nigerian population.
  publication-title: J Proteome Res
  doi: 10.1021/pr901058t
– volume: 401
  start-page: 1899
  year: 2011
  ident: R12-22-20250207
  article-title: Identification of serum biomarkers of hepatocarcinoma through liquid chromatographymass spectrometrybased metabonomic method.
  publication-title: Anal Bioanal Chem
  doi: 10.1007/s00216-011-5245-3
– volume: 19
  start-page: 329
  year: 1999
  ident: R23-22-20250207
  article-title: Prognosis of hepatocellular carcinoma: the BCLC staging classification.
  publication-title: Semin Liver Dis
  doi: 10.1055/s-2007-1007122
– volume: 403
  start-page: 203
  year: 2012
  ident: R15-22-20250207
  article-title: Serum metabolomics reveals the deregulation of fatty acids metabolism in hepatocellular carcinoma and chronic liver diseases.
  publication-title: Anal Bioanal Chem
  doi: 10.1007/s00216-012-5782-4
– volume: 11
  start-page: 354
  year: 1998
  ident: R34-22-20250207
  article-title: Metabolic changes underlying 31P MR spectral alterations in human hepatic tumours.
  publication-title: NMR Biomed
  doi: 10.1002/(SICI)1099-1492(1998110)11:7<354::AID-NBM515>3.0.CO;2-N
– volume: 19
  start-page: 311
  year: 2010
  ident: R3-22-20250207
  article-title: World Gastroenterology Organisation Guideline. Hepatocellular carcinoma (HCC): a global perspective.
  publication-title: J Gastrointestin Liver Dis
– volume: 6
  start-page: 2605
  year: 2007
  ident: R9-22-20250207
  article-title: Metabonomic studies of human hepatocellular carcinoma using highresolution magicangle spinning 1H NMR spectroscopy in conjunction with multivariate data analysis.
  publication-title: J Proteome Res
  doi: 10.1021/pr070063h
– volume: 37
  start-page: 806
  year: 2002
  ident: R4-22-20250207
  article-title: Changing international trends in mortality rates for liver, biliary and pancreatic tumours.
  publication-title: J Hepatol
  doi: 10.1016/S0168-8278(02)00297-0
– volume: 31
  start-page: 123
  year: 2012
  ident: R36-22-20250207
  article-title: The geneticmetabolic transformation concept of carcinogenesis.
  publication-title: Cancer Metastasis Rev
  doi: 10.1007/s10555-011-9334-8
– volume: 11
  start-page: 643
  year: 2012
  ident: R38-22-20250207
  article-title: Stability and robustness of human metabolic phenotypes in response to sequential food challenges.
  publication-title: J Proteome Res
  doi: 10.1021/pr2005764
– volume: 21
  start-page: 297
  year: 2012
  ident: R35-22-20250207
  article-title: Metabolic reprogramming: a cancer hallmark even warburg did not anticipate.
  publication-title: Cancer Cell
  doi: 10.1016/j.ccr.2012.02.014
– volume: 10
  start-page: M110
  year: 2011
  ident: R13-22-20250207
  article-title: Serum and urine metabolite profiling reveals potential biomarkers of human hepatocellular carcinoma.
  publication-title: Mol Cell Proteomics
– volume: 55
  start-page: 74
  year: 2005
  ident: R2-22-20250207
  article-title: Global cancer statistics, 2002.
  publication-title: CA Cancer J Clin
  doi: 10.3322/canjclin.55.2.74
– volume: 204
  start-page: 135
  year: 2005
  ident: R25-22-20250207
  article-title: Comparative metabonomics of differential hydrazine toxicity in the rat and mouse.
  publication-title: Toxicol Appl Pharmacol
  doi: 10.1016/j.taap.2004.06.031
– volume: 491
  start-page: 384
  year: 2012
  ident: R10-22-20250207
  article-title: Metabolic phenotyping in clinical and surgical environments.
  publication-title: Nature
  doi: 10.1038/nature11708
– volume: 10
  start-page: 1828
  year: 2011
  ident: R21-22-20250207
  article-title: Urinary metabolic biomarkers of hepatocellular carcinoma in an egyptian population: a validation study.
  publication-title: J Proteome Res
  doi: 10.1021/pr101096f
– volume: 132
  start-page: 2557
  year: 2007
  ident: R5-22-20250207
  article-title: Hepatocellular carcinoma: epidemiology and molecular carcinogenesis.
  publication-title: Gastroenterology
  doi: 10.1053/j.gastro.2007.04.061
– volume: 13
  start-page: 724
  year: 2009
  ident: R37-22-20250207
  article-title: Sarcopenia: clinical evaluation, biological markers and other evaluation tools.
  publication-title: J Nutr Health Aging
  doi: 10.1007/s12603-009-0204-9
– volume: 9
  start-page: 1096
  year: 2010
  ident: R31-22-20250207
  article-title: Characterization of urinary biomarkers of hepatocellular carcinoma using magnetic resonance spectroscopy in a Nigerian population.
  publication-title: J Proteome Res
  doi: 10.1021/pr901058t
– volume: 11
  start-page: 835
  year: 2011
  ident: R33-22-20250207
  article-title: Choline metabolism in malignant transformation.
  publication-title: Nat Rev Cancer
  doi: 10.1038/nrc3162
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Snippet There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha‐fetoprotein (AFP) is too...
There is no clinically applicable biomarker for surveillance of hepatocellular carcinoma (HCC), because the sensitivity of serum alpha-fetoprotein (AFP) is too...
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SubjectTerms Acetylcarnitine - urine
Adolescent
Adult
Africa, Western - epidemiology
Aged
Aged, 80 and over
alpha-Fetoproteins - urine
Biomarkers, Tumor - urine
Carcinoma, Hepatocellular - diagnosis
Carcinoma, Hepatocellular - epidemiology
Carcinoma, Hepatocellular - urine
Case-Control Studies
Choline - urine
Creatine - urine
Female
Hepatology
Humans
Ketoglutaric Acids - urine
Life Sciences
Liver cancer
Liver cirrhosis
Liver Neoplasms - diagnosis
Liver Neoplasms - epidemiology
Liver Neoplasms - urine
Male
Metabolites
Methionine - urine
Middle Aged
Niacinamide - analogs & derivatives
Niacinamide - urine
Phenotype
Reproducibility of Results
Santé publique et épidémiologie
Sarcosine - analogs & derivatives
Sarcosine - urine
Sensitivity and Specificity
Urine
Young Adult
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Title Discovery and validation of urinary metabotypes for the diagnosis of hepatocellular carcinoma in West Africans
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhep.27264
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