{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,9]],"date-time":"2026-04-09T00:59:17Z","timestamp":1775696357950,"version":"3.50.1"},"reference-count":24,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,10,4]],"date-time":"2021-10-04T00:00:00Z","timestamp":1633305600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,10,4]],"date-time":"2021-10-04T00:00:00Z","timestamp":1633305600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The goal of this study was to determine the diagnostic performance of in vivo quantitative proton magnetic resonance spectroscopy (<jats:sup>1<\/jats:sup>H-MRS) to identify the presence of esophageal varices needing treatment (VNT), as well as investigate its correlation with clinical characteristics in patients with liver cirrhosis. Forty cirrhotic patients without VNT showing the negative red color sign, and 40 cirrhotic patients with VNT showing positive red color sign underwent laboratory tests, esophago-gastro-duodenoscopy, and <jats:sup>1<\/jats:sup>H-MRS with single-voxel localization in the cirrhotic liver parenchyma. The levels of lactate\u2009+\u2009triglyceride (TG) and choline in cirrhotic patients with VNT were significantly higher than those in cirrhotic patients without VNT. In multivariate analysis, spleen diameter, platelet count, and platelet count\/spleen diameter ratio, as well as lactate\u2009+\u2009TG, and choline were associated with the presence of VNT. Moreover, lactate\u2009+\u2009TG and choline levels were positively correlated with spleen diameter and negatively correlated with platelet count in the combined group of cirrhotic patients with and without VNT. Our study demonstrated that higher hepatic lactate\u2009+\u2009TG and choline levels in cirrhotic patients in conjunction with longer spleen diameter, lower platelet counts, and lower ratios of platelet count to spleen diameter were associated with the presence of esophageal VNT and the risk of developing variceal bleeding. Therefore, in vivo <jats:sup>1<\/jats:sup>H-MRS might be an effective tool for diagnosing and predicting esophageal VNT in patients with liver cirrhosis.<\/jats:p>","DOI":"10.1038\/s41598-021-99198-9","type":"journal-article","created":{"date-parts":[[2021,10,4]],"date-time":"2021-10-04T17:14:08Z","timestamp":1633367648000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Identification of potential metabolic biomarkers in predicting esophageal varices needing treatment in patients with liver cirrhosis"],"prefix":"10.1038","volume":"11","author":[{"given":"Chung-Man","family":"Moon","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yun-Young","family":"Lee","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Suk-Hee","family":"Heo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sang-Soo","family":"Shin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yong-Yeon","family":"Jeong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,10,4]]},"reference":[{"issue":"Suppl 1","key":"99198_CR1","doi-asserted-by":"publisher","first-page":"S3","DOI":"10.1016\/j.jhep.2020.11.042","volume":"75","author":"P Jepsen","year":"2021","unstructured":"Jepsen, P. & Younossi, Z. M. The global burden of cirrhosis: A review of disability-adjusted life-years lost and unmet needs. J. Hepatol. 75(Suppl 1), S3\u2013S13 (2021).","journal-title":"J. Hepatol."},{"key":"99198_CR2","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1148\/radiol.14130916","volume":"272","author":"SU Shin","year":"2014","unstructured":"Shin, S. U. et al. Prediction of esophageal varices in patients with cirrhosis: Usefulness of three-dimensional MR elastography with echo-planar imaging technique. Radiology 272, 143\u2013153 (2014).","journal-title":"Radiology"},{"key":"99198_CR3","doi-asserted-by":"publisher","first-page":"922","DOI":"10.1002\/hep.21907","volume":"46","author":"G Garcia-Tsao","year":"2007","unstructured":"Garcia-Tsao, G. et al. Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis. Hepatology 46, 922\u2013938 (2007).","journal-title":"Hepatology"},{"key":"99198_CR4","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1016\/j.jhep.2018.05.019","volume":"69","author":"S Petta","year":"2018","unstructured":"Petta, S. et al. Non-invasive prediction of esophageal varices by stiffness and platelet in non-alcoholic fatty liver disease cirrhosis. J. Hepatol. 69, 878\u2013885 (2018).","journal-title":"J. Hepatol."},{"key":"99198_CR5","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1016\/j.jhep.2015.05.022","volume":"63","author":"R de Franchis","year":"2015","unstructured":"de Franchis, R. & Baveno, V. I. F. Expanding consensus in portal hypertension: Report of the Baveno VI Consensus Workshop: Stratifying risk and individualizing care for portal hypertension. J. Hepatol. 63, 743\u2013752 (2015).","journal-title":"J. Hepatol."},{"key":"99198_CR6","doi-asserted-by":"crossref","unstructured":"Fofiu, R. et al. Assessing Baveno VI criteria using liver stiffness measured with a 2D-shear wave elastography technique. Diagnostics (Basel) 11, 1 (2021).","DOI":"10.3390\/diagnostics11050737"},{"key":"99198_CR7","unstructured":"Radda, G.K. Handbook of Magnetic resonance spectroscopy in vivo: MRS theory, practice and applications. Nmr Biomed. 30, 1 (2017)."},{"key":"99198_CR8","doi-asserted-by":"publisher","first-page":"14949","DOI":"10.18632\/aging.103554","volume":"12","author":"FF Cai","year":"2020","unstructured":"Cai, F. F. et al. Analysis of plasma metabolic profile, characteristics and enzymes in the progression from chronic hepatitis B to hepatocellular carcinoma. Aging (Albany NY) 12, 14949\u201314965 (2020).","journal-title":"Aging (Albany NY)"},{"key":"99198_CR9","first-page":"111","volume":"27","author":"B Martinez-Granados","year":"2011","unstructured":"Martinez-Granados, B. et al. Metabolic profile of chronic liver disease by NMR spectroscopy of human biopsies. Int. J. Mol. Med. 27, 111\u2013117 (2011).","journal-title":"Int. J. Mol. Med."},{"key":"99198_CR10","doi-asserted-by":"publisher","first-page":"5133","DOI":"10.3748\/wjg.v17.i47.5133","volume":"17","author":"EG ter Voert","year":"2011","unstructured":"ter Voert, E. G. et al. In vivo magnetic resonance spectroscopy of liver tumors and metastases. World J. Gastroenterol. 17, 5133\u20135149 (2011).","journal-title":"World J. Gastroenterol."},{"key":"99198_CR11","doi-asserted-by":"crossref","unstructured":"Moon, C.M. et al. Metabolic alterations associated with early-stage hepatocellular carcinoma and their correlation with aging and enzymatic activity in patients with viral hepatitis-induced liver cirrhosis: A preliminary study. J Clin Med 9, 1 (2020).","DOI":"10.3390\/jcm9030765"},{"key":"99198_CR12","doi-asserted-by":"publisher","first-page":"1298","DOI":"10.1002\/jmri.25673","volume":"46","author":"TH Kim","year":"2017","unstructured":"Kim, T. H. et al. Hepatic alanine differentiates nonalcoholic steatohepatitis from simple steatosis in humans and mice: A proton MR spectroscopy study with long echo time. J. Magn. Reson. Imaging 46, 1298\u20131310 (2017).","journal-title":"J. Magn. Reson. Imaging"},{"key":"99198_CR13","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1007\/s11307-019-01322-9","volume":"21","author":"CM Moon","year":"2019","unstructured":"Moon, C. M. et al. Metabolic changes in different stages of liver fibrosis: In vivo hyperpolarized (13)C MR spectroscopy and metabolic imaging. Mol. Imag. Biol. 21, 842\u2013851 (2019).","journal-title":"Mol. Imag. Biol."},{"key":"99198_CR14","doi-asserted-by":"publisher","first-page":"617","DOI":"10.1016\/j.jhep.2017.09.027","volume":"68","author":"AT Mazzeo","year":"2018","unstructured":"Mazzeo, A. T. & Maimone, S. Acid-base disorders in liver disease. J. Hepatol. 68, 617\u2013618 (2018).","journal-title":"J. Hepatol."},{"key":"99198_CR15","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.bbrc.2016.08.118","volume":"482","author":"CM Moon","year":"2017","unstructured":"Moon, C. M. et al. Metabolic biomarkers for non-alcoholic fatty liver disease induced by high-fat diet: In vivo magnetic resonance spectroscopy of hyperpolarized [1-(13)C] pyruvate. Biochem. Biophys. Res. Commun. 482, 112\u2013119 (2017).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"99198_CR16","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1111\/liv.13695","volume":"38","author":"CM Moon","year":"2018","unstructured":"Moon, C. M. et al. Metabolic alterations in a rat model of hepatic ischaemia reperfusion injury: In vivo hyperpolarized (13) C MRS and metabolic imaging. Liver Int. 38, 1117\u20131127 (2018).","journal-title":"Liver Int."},{"key":"99198_CR17","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1111\/liv.14054","volume":"39","author":"AA Shaheen","year":"2019","unstructured":"Shaheen, A. A. et al. Nationwide estimates and risk factors of hospital readmission in patients with cirrhosis in the United States. Liver Int. 39, 878\u2013884 (2019).","journal-title":"Liver Int."},{"key":"99198_CR18","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/S1665-2681(19)31011-7","volume":"12","author":"H Enomoto","year":"2013","unstructured":"Enomoto, H. et al. Association of amino acid imbalance with the severity of liver fibrosis and esophageal varices. Ann. Hepatol. 12, 471\u2013478 (2013).","journal-title":"Ann. Hepatol."},{"key":"99198_CR19","doi-asserted-by":"crossref","unstructured":"Sonkar, K. et al. Focus on the glycerophosphocholine pathway in choline phospholipid metabolism of cancer. Nmr Biomed 32, e4112 (2019).","DOI":"10.1002\/nbm.4112"},{"key":"99198_CR20","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1001\/jamaoncol.2016.3147","volume":"3","author":"SY Kim","year":"2017","unstructured":"Kim, S. Y. et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncol. 3, 456\u2013463 (2017).","journal-title":"JAMA Oncol."},{"key":"99198_CR21","doi-asserted-by":"publisher","first-page":"1620","DOI":"10.1053\/gast.2002.33419","volume":"122","author":"DM Jensen","year":"2002","unstructured":"Jensen, D. M. Endoscopic screening for varices in cirrhosis: findings, implications, and outcomes. Gastroenterology 122, 1620\u20131630 (2002).","journal-title":"Gastroenterology"},{"key":"99198_CR22","doi-asserted-by":"publisher","first-page":"1840","DOI":"10.21037\/qims.2019.09.18","volume":"9","author":"YXJ Wang","year":"2019","unstructured":"Wang, Y. X. J. et al. Topics on quantitative liver magnetic resonance imaging. Quant. Imaging Med. Surg. 9, 1840\u20131890 (2019).","journal-title":"Quant. Imaging Med. Surg."},{"key":"99198_CR23","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1111\/liv.14036","volume":"39","author":"HA Lee","year":"2019","unstructured":"Lee, H. A. et al. Prediction of the varices needing treatment with non-invasive tests in patients with compensated advanced chronic liver disease. Liver Int. 39, 1071\u20131079 (2019).","journal-title":"Liver Int."},{"key":"99198_CR24","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/j.aohep.2019.06.003","volume":"18","author":"AZ Mattos","year":"2019","unstructured":"Mattos, A. Z. et al. Screening for esophageal varices in cirrhotic patients - Non-invasive methods. Ann. Hepatol. 18, 673\u2013678 (2019).","journal-title":"Ann. Hepatol."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-99198-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-99198-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-99198-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T16:02:15Z","timestamp":1670083335000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-99198-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,4]]},"references-count":24,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["99198"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-99198-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,10,4]]},"assertion":[{"value":"18 February 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 September 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 October 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"19684"}}