Skip to main content
Top
Published in: Journal of Cancer Research and Clinical Oncology 3/2024

Open Access 01-03-2024 | Thyroid Cancer | Research

Distinguishing benign and malignant thyroid nodules using plasma trimethylamine N-oxide, carnitine, choline and betaine

Authors: Liang Shi, Muhong Guo, Cuixiao Shi, Gu Gao, Xianghong Xu, Chuan Zhang, Jingjing Fu, Yudan Ni, Feng Wang, Xue Xue, Fei Yu

Published in: Journal of Cancer Research and Clinical Oncology | Issue 3/2024

Login to get access

Abstract

Purpose

Trimethylamine N-oxide (TMAO), a gut microbiome–derived metabolite, and its precursors (carnitine, choline, betaine) have not been fully examined in relation to thyroid cancer (TC) risk. The aim of this study was to assess the value of TMAO and its precursors in diagnosis of benign and malignant thyroid nodules.

Methods

In this study, high-performance liquid chromatography-tandem mass spectrometry was utilized to measure the levels of plasma TMAO and its precursors (choline, carnitine, and betaine) in 215 TC patients, 63 benign thyroid nodules (BTN) patients and 148 healthy controls (HC). The distribution of levels of TMAO and its precursors among the three groups were compared by the Kruskal–Wallis test. Receiver operating characteristic curve (ROC) analysis was performed to evaluate the sensitivity, specificity, and the predictive accuracy of single and combined biomarkers.

Results

In comparison to HC, TC showed higher levels of TMAO and lower levels of its precursors (carnitine, choline, and betaine) (all P < 0.001). Plasma choline (P < 0.01) and betaine (P < 0.05) were declined in BTN than HC. The levels of carnitine (P < 0.001) and choline (P < 0.05) were significantly higher in BTN than that in TC group. Plasma TMAO showed lower levels in TC with lymph node metastasis (101.5 (73.1–144.5) ng/ml) than those without lymph node metastasis (131 (84.8–201) ng/ml, P < 0.05). Combinations of these four metabolites achieved good performance in the differential diagnosis, with the area under the ROC curve of 0.703, 0.741, 0.793 when discriminating between TC and BTN, BTN and HC, TC and HC, respectively.

Conclusion

Plasma TMAO, along with its precursors could serve as new biomarkers for the diagnosis of benign and malignant thyroid nodules.
Literature
go back to reference Alexander JL, Mullish BH, Danckert NP, Liu Z, Olbei ML, Saifuddin A, Torkizadeh M, Ibraheim H, Blanco JM, Roberts LA, Bewshea CM, Nice R, Lin S, Prabhudev H, Sands C, Horneffer-van der Sluis V, Lewis M, Sebastian S, Lees CW, Teare JP, Hart A, Goodhand JR, Kennedy NA, Korcsmaros T, Marchesi JR, Ahmad T, Powell N (2023) The gut microbiota and metabolome are associated with diminished COVID-19 vaccine-induced antibody responses in immunosuppressed inflammatory bowel disease patients. EBioMedicine 88:104430PubMedPubMedCentral Alexander JL, Mullish BH, Danckert NP, Liu Z, Olbei ML, Saifuddin A, Torkizadeh M, Ibraheim H, Blanco JM, Roberts LA, Bewshea CM, Nice R, Lin S, Prabhudev H, Sands C, Horneffer-van der Sluis V, Lewis M, Sebastian S, Lees CW, Teare JP, Hart A, Goodhand JR, Kennedy NA, Korcsmaros T, Marchesi JR, Ahmad T, Powell N (2023) The gut microbiota and metabolome are associated with diminished COVID-19 vaccine-induced antibody responses in immunosuppressed inflammatory bowel disease patients. EBioMedicine 88:104430PubMedPubMedCentral
go back to reference Backhed F (2013) Meat-metabolizing bacteria in atherosclerosis. Nat Med 19:533–534PubMed Backhed F (2013) Meat-metabolizing bacteria in atherosclerosis. Nat Med 19:533–534PubMed
go back to reference Blum M (2000) Ultrasonography of the Thyroid. In: Feingold KR, Anawalt B, Blackman MR, Boyce A, Chrousos G, Corpas E, de Herder WW, Dhatariya K, Dungan K, Hofland J, Kalra S, Kaltsas G, Kapoor N, Koch C, Kopp P, Korbonits M, Kovacs CS, Kuohung W, Laferrere B, Levy M, McGee EA, McLachlan R, New M, Purnell J, Sahay R, Shah AS, Singer F, Sperling MA, Stratakis CA, Trence DL, Wilson DP (eds) Endotext. South Dartmouth (MA) Blum M (2000) Ultrasonography of the Thyroid. In: Feingold KR, Anawalt B, Blackman MR, Boyce A, Chrousos G, Corpas E, de Herder WW, Dhatariya K, Dungan K, Hofland J, Kalra S, Kaltsas G, Kapoor N, Koch C, Kopp P, Korbonits M, Kovacs CS, Kuohung W, Laferrere B, Levy M, McGee EA, McLachlan R, New M, Purnell J, Sahay R, Shah AS, Singer F, Sperling MA, Stratakis CA, Trence DL, Wilson DP (eds) Endotext. South Dartmouth (MA)
go back to reference Bogovic Crncic T, Ilic Tomas M, Girotto N, Grbac Ivankovic S (2020) Risk factors for thyroid cancer: what do we know so far? Acta Clin Croat 59:66–72PubMedPubMedCentral Bogovic Crncic T, Ilic Tomas M, Girotto N, Grbac Ivankovic S (2020) Risk factors for thyroid cancer: what do we know so far? Acta Clin Croat 59:66–72PubMedPubMedCentral
go back to reference Chan CWH, Law BMH, Waye MMY, Chan JYW, So WKW, Chow KM (2019) Trimethylamine-N-oxide as one hypothetical link for the relationship between intestinal microbiota and cancer—where we are and where shall we go? J Cancer 10:5874–5882PubMedPubMedCentral Chan CWH, Law BMH, Waye MMY, Chan JYW, So WKW, Chow KM (2019) Trimethylamine-N-oxide as one hypothetical link for the relationship between intestinal microbiota and cancer—where we are and where shall we go? J Cancer 10:5874–5882PubMedPubMedCentral
go back to reference Dambrova M, Latkovskis G, Kuka J, Strele I, Konrade I, Grinberga S, Hartmane D, Pugovics O, Erglis A, Liepinsh E (2016) Diabetes is associated with higher trimethylamine N-oxide plasma levels. Exp Clin Endocrinol Diabetes 124:251–256PubMed Dambrova M, Latkovskis G, Kuka J, Strele I, Konrade I, Grinberga S, Hartmane D, Pugovics O, Erglis A, Liepinsh E (2016) Diabetes is associated with higher trimethylamine N-oxide plasma levels. Exp Clin Endocrinol Diabetes 124:251–256PubMed
go back to reference Deja S, Dawiskiba T, Balcerzak W, Orczyk-Pawilowicz M, Glod M, Pawelka D, Mlynarz P (2013) Follicular adenomas exhibit a unique metabolic profile. (1)H NMR studies of thyroid lesions. PLoS One 8:84637 Deja S, Dawiskiba T, Balcerzak W, Orczyk-Pawilowicz M, Glod M, Pawelka D, Mlynarz P (2013) Follicular adenomas exhibit a unique metabolic profile. (1)H NMR studies of thyroid lesions. PLoS One 8:84637
go back to reference Farrokhi Yekta R, Rezaei Tavirani M, Arefi Oskouie A, Mohajeri-Tehrani MR, Soroush AR, Akbarzadeh Baghban A (2018) Serum-based metabolic alterations in patients with papillary thyroid carcinoma unveiled by non-targeted 1H-NMR metabolomics approach. Iran J Basic Med Sci 21:1140–1147PubMedPubMedCentral Farrokhi Yekta R, Rezaei Tavirani M, Arefi Oskouie A, Mohajeri-Tehrani MR, Soroush AR, Akbarzadeh Baghban A (2018) Serum-based metabolic alterations in patients with papillary thyroid carcinoma unveiled by non-targeted 1H-NMR metabolomics approach. Iran J Basic Med Sci 21:1140–1147PubMedPubMedCentral
go back to reference Gharib H, Papini E, Garber JR, Duick DS, Harrell RM, Hegedus L, Paschke R, Valcavi R, Vitti P, Nodules AAATFoT (2016) American association of clinical endocrinologists, American college of endocrinology, and associazione medici endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules–2016 update. Endocr Pract 22:622–639PubMed Gharib H, Papini E, Garber JR, Duick DS, Harrell RM, Hegedus L, Paschke R, Valcavi R, Vitti P, Nodules AAATFoT (2016) American association of clinical endocrinologists, American college of endocrinology, and associazione medici endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules–2016 update. Endocr Pract 22:622–639PubMed
go back to reference Ha EJ, Suh CH, Baek JH (2018) Complications following ultrasound-guided core needle biopsy of thyroid nodules: a systematic review and meta-analysis. Eur Radiol 28:3848–3860PubMed Ha EJ, Suh CH, Baek JH (2018) Complications following ultrasound-guided core needle biopsy of thyroid nodules: a systematic review and meta-analysis. Eur Radiol 28:3848–3860PubMed
go back to reference Hamaya R, Ivey KL, Lee DH, Wang M, Li J, Franke A, Sun Q, Rimm EB (2020) Association of diet with circulating trimethylamine-N-oxide concentration. Am J Clin Nutr 112:1448–1455PubMedPubMedCentral Hamaya R, Ivey KL, Lee DH, Wang M, Li J, Franke A, Sun Q, Rimm EB (2020) Association of diet with circulating trimethylamine-N-oxide concentration. Am J Clin Nutr 112:1448–1455PubMedPubMedCentral
go back to reference Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L (2016) 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 26:1–133PubMedPubMedCentral Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L (2016) 2015 American thyroid association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American thyroid association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 26:1–133PubMedPubMedCentral
go back to reference Jalandra R, Dalal N, Yadav AK, Verma D, Sharma M, Singh R, Khosla A, Kumar A, Solanki PR (2021) Emerging role of trimethylamine-N-oxide (TMAO) in colorectal cancer. Appl Microbiol Biotechnol 105:7651–7660PubMed Jalandra R, Dalal N, Yadav AK, Verma D, Sharma M, Singh R, Khosla A, Kumar A, Solanki PR (2021) Emerging role of trimethylamine-N-oxide (TMAO) in colorectal cancer. Appl Microbiol Biotechnol 105:7651–7660PubMed
go back to reference Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WH, Bushman FD, Lusis AJ, Hazen SL (2013) Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19:576–585PubMedPubMedCentral Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, Smith JD, DiDonato JA, Chen J, Li H, Wu GD, Lewis JD, Warrier M, Brown JM, Krauss RM, Tang WH, Bushman FD, Lusis AJ, Hazen SL (2013) Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19:576–585PubMedPubMedCentral
go back to reference Li D, Lu Y, Yuan S, Cai X, He Y, Chen J, Wu Q, He D, Fang A, Bo Y, Song P, Bogaert D, Tsilidis K, Larsson SC, Yu H, Zhu H, Theodoratou E, Zhu Y, Li X (2022) Gut microbiota-derived metabolite trimethylamine-N-oxide and multiple health outcomes: an umbrella review and updated meta-analysis. Am J Clin Nutr 116:230–243PubMedPubMedCentral Li D, Lu Y, Yuan S, Cai X, He Y, Chen J, Wu Q, He D, Fang A, Bo Y, Song P, Bogaert D, Tsilidis K, Larsson SC, Yu H, Zhu H, Theodoratou E, Zhu Y, Li X (2022) Gut microbiota-derived metabolite trimethylamine-N-oxide and multiple health outcomes: an umbrella review and updated meta-analysis. Am J Clin Nutr 116:230–243PubMedPubMedCentral
go back to reference Liu Q, Li B, Li Y, Wei Y, Huang B, Liang J, You Z, Li Y, Qian Q, Wang R, Zhang J, Chen R, Lyu Z, Chen Y, Shi M, Xiao X, Wang Q, Miao Q, Fang JY, Gershwin ME, Lian M, Ma X, Tang R (2022a) Altered faecal microbiome and metabolome in IgG4-related sclerosing cholangitis and primary sclerosing cholangitis. Gut 71:899–909PubMed Liu Q, Li B, Li Y, Wei Y, Huang B, Liang J, You Z, Li Y, Qian Q, Wang R, Zhang J, Chen R, Lyu Z, Chen Y, Shi M, Xiao X, Wang Q, Miao Q, Fang JY, Gershwin ME, Lian M, Ma X, Tang R (2022a) Altered faecal microbiome and metabolome in IgG4-related sclerosing cholangitis and primary sclerosing cholangitis. Gut 71:899–909PubMed
go back to reference Mayers JR, Vander Heiden MG (2015) Famine versus feast: understanding the metabolism of tumors in vivo. Trends Biochem Sci 40:130–140PubMedPubMedCentral Mayers JR, Vander Heiden MG (2015) Famine versus feast: understanding the metabolism of tumors in vivo. Trends Biochem Sci 40:130–140PubMedPubMedCentral
go back to reference Miccoli P, Torregrossa L, Shintu L, Magalhaes A, Chandran J, Tintaru A, Ugolini C, Minuto MN, Miccoli M, Basolo F, Caldarelli S (2012) Metabolomics approach to thyroid nodules: a high-resolution magic-angle spinning nuclear magnetic resonance-based study. Surgery 152:1118–1124PubMed Miccoli P, Torregrossa L, Shintu L, Magalhaes A, Chandran J, Tintaru A, Ugolini C, Minuto MN, Miccoli M, Basolo F, Caldarelli S (2012) Metabolomics approach to thyroid nodules: a high-resolution magic-angle spinning nuclear magnetic resonance-based study. Surgery 152:1118–1124PubMed
go back to reference Mirji G, Worth A, Bhat SA, El Sayed M, Kannan T, Goldman AR, Tang HY, Liu Q, Auslander N, Dang CV, Abdel-Mohsen M, Kossenkov A, Stanger BZ, Shinde RS (2022) The microbiome-derived metabolite TMAO drives immune activation and boosts responses to immune checkpoint blockade in pancreatic cancer. Sci Immunol 7:0704 Mirji G, Worth A, Bhat SA, El Sayed M, Kannan T, Goldman AR, Tang HY, Liu Q, Auslander N, Dang CV, Abdel-Mohsen M, Kossenkov A, Stanger BZ, Shinde RS (2022) The microbiome-derived metabolite TMAO drives immune activation and boosts responses to immune checkpoint blockade in pancreatic cancer. Sci Immunol 7:0704
go back to reference Mondul AM, Moore SC, Weinstein SJ, Karoly ED, Sampson JN, Albanes D (2015) Metabolomic analysis of prostate cancer risk in a prospective cohort: The alpha-tocolpherol, beta-carotene cancer prevention (ATBC) study. Int J Cancer 137:2124–2132PubMedPubMedCentral Mondul AM, Moore SC, Weinstein SJ, Karoly ED, Sampson JN, Albanes D (2015) Metabolomic analysis of prostate cancer risk in a prospective cohort: The alpha-tocolpherol, beta-carotene cancer prevention (ATBC) study. Int J Cancer 137:2124–2132PubMedPubMedCentral
go back to reference Oellgaard J, Winther SA, Hansen TS, Rossing P, von Scholten BJ (2017) Trimethylamine N-oxide (TMAO) as a new potential therapeutic target for insulin resistance and cancer. Curr Pharm Des 23:3699–3712PubMed Oellgaard J, Winther SA, Hansen TS, Rossing P, von Scholten BJ (2017) Trimethylamine N-oxide (TMAO) as a new potential therapeutic target for insulin resistance and cancer. Curr Pharm Des 23:3699–3712PubMed
go back to reference Perea-Gil I, Seeger T, Bruyneel AAN, Termglinchan V, Monte E, Lim EW, Vadgama N, Furihata T, Gavidia AA, Arthur Ataam J, Bharucha N, Martinez-Amador N, Ameen M, Nair P, Serrano R, Kaur B, Feyen DAM, Diecke S, Snyder MP, Metallo CM, Mercola M, Karakikes I (2022) Serine biosynthesis as a novel therapeutic target for dilated cardiomyopathy. Eur Heart J 43:3477–3489PubMedPubMedCentral Perea-Gil I, Seeger T, Bruyneel AAN, Termglinchan V, Monte E, Lim EW, Vadgama N, Furihata T, Gavidia AA, Arthur Ataam J, Bharucha N, Martinez-Amador N, Ameen M, Nair P, Serrano R, Kaur B, Feyen DAM, Diecke S, Snyder MP, Metallo CM, Mercola M, Karakikes I (2022) Serine biosynthesis as a novel therapeutic target for dilated cardiomyopathy. Eur Heart J 43:3477–3489PubMedPubMedCentral
go back to reference Qiu S, Cai Y, Yao H, Lin C, Xie Y, Tang S, Zhang A (2023) Small molecule metabolites: discovery of biomarkers and therapeutic targets. Signal Transduct Target Ther 8:132PubMedPubMedCentral Qiu S, Cai Y, Yao H, Lin C, Xie Y, Tang S, Zhang A (2023) Small molecule metabolites: discovery of biomarkers and therapeutic targets. Signal Transduct Target Ther 8:132PubMedPubMedCentral
go back to reference Russ G, Bonnema SJ, Erdogan MF, Durante C, Ngu R, Leenhardt L (2017) European thyroid association guidelines for ultrasound malignancy risk stratification of thyroid nodules in adults: the EU-TIRADS. Eur Thyroid J 6:225–237PubMedPubMedCentral Russ G, Bonnema SJ, Erdogan MF, Durante C, Ngu R, Leenhardt L (2017) European thyroid association guidelines for ultrasound malignancy risk stratification of thyroid nodules in adults: the EU-TIRADS. Eur Thyroid J 6:225–237PubMedPubMedCentral
go back to reference Ryoo I, Kwon H, Kim SC, Jung SC, Yeom JA, Shin HS, Cho HR, Yun TJ, Choi SH, Sohn CH, Park S, Kim JH (2016) Metabolomic analysis of percutaneous fine-needle aspiration specimens of thyroid nodules: potential application for the preoperative diagnosis of thyroid cancer. Sci Rep 6:30075PubMedPubMedCentral Ryoo I, Kwon H, Kim SC, Jung SC, Yeom JA, Shin HS, Cho HR, Yun TJ, Choi SH, Sohn CH, Park S, Kim JH (2016) Metabolomic analysis of percutaneous fine-needle aspiration specimens of thyroid nodules: potential application for the preoperative diagnosis of thyroid cancer. Sci Rep 6:30075PubMedPubMedCentral
go back to reference Sakorafas GH, Mastoraki A, Lappas C, Safioleas M (2010) Small (<10 mm) thyroid nodules; how aggressively should they be managed? Onkologie 33:61–64PubMed Sakorafas GH, Mastoraki A, Lappas C, Safioleas M (2010) Small (<10 mm) thyroid nodules; how aggressively should they be managed? Onkologie 33:61–64PubMed
go back to reference Seiberling KA, Dutra JC, Gunn J (2008) Ultrasound-guided fine needle aspiration biopsy of thyroid nodules performed in the office. Laryngoscope 118:228–231PubMed Seiberling KA, Dutra JC, Gunn J (2008) Ultrasound-guided fine needle aspiration biopsy of thyroid nodules performed in the office. Laryngoscope 118:228–231PubMed
go back to reference Seo H, Na DG, Kim JH, Kim KW, Yoon JW (2015) Ultrasound-based risk stratification for malignancy in thyroid nodules: a four-tier categorization system. Eur Radiol 25:2153–2162PubMed Seo H, Na DG, Kim JH, Kim KW, Yoon JW (2015) Ultrasound-based risk stratification for malignancy in thyroid nodules: a four-tier categorization system. Eur Radiol 25:2153–2162PubMed
go back to reference Seo JW, Han K, Lee J, Kim EK, Moon HJ, Yoon JH, Park VY, Baek HM, Kwak JY (2018) Application of metabolomics in prediction of lymph node metastasis in papillary thyroid carcinoma. PLoS One 13:e0193883PubMedPubMedCentral Seo JW, Han K, Lee J, Kim EK, Moon HJ, Yoon JH, Park VY, Baek HM, Kwak JY (2018) Application of metabolomics in prediction of lymph node metastasis in papillary thyroid carcinoma. PLoS One 13:e0193883PubMedPubMedCentral
go back to reference Siegel RL, Miller KD, Fuchs HE, Jemal A (2022) Cancer statistics, 2022. CA Cancer J Clin 72:7–33PubMed Siegel RL, Miller KD, Fuchs HE, Jemal A (2022) Cancer statistics, 2022. CA Cancer J Clin 72:7–33PubMed
go back to reference Stonans I, Kuzmina J, Polaka I, Grinberga S, Sevostjanovs E, Liepins E, Aleksandravica I, Santare D, Kirsners A, Skapars R, Pcolkins A, Tolmanis I, Sivins A, Leja M, Dambrova M (2023) The association of circulating L-carnitine, gamma-butyrobetaine and trimethylamine N-oxide levels with gastric cancer. Diagnostics (basel) 13:1341PubMed Stonans I, Kuzmina J, Polaka I, Grinberga S, Sevostjanovs E, Liepins E, Aleksandravica I, Santare D, Kirsners A, Skapars R, Pcolkins A, Tolmanis I, Sivins A, Leja M, Dambrova M (2023) The association of circulating L-carnitine, gamma-butyrobetaine and trimethylamine N-oxide levels with gastric cancer. Diagnostics (basel) 13:1341PubMed
go back to reference Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA, Agatisa-Boyle B, Li XS, Levison BS, Hazen SL (2015) Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res 116:448–455PubMed Tang WH, Wang Z, Kennedy DJ, Wu Y, Buffa JA, Agatisa-Boyle B, Li XS, Levison BS, Hazen SL (2015) Gut microbiota-dependent trimethylamine N-oxide (TMAO) pathway contributes to both development of renal insufficiency and mortality risk in chronic kidney disease. Circ Res 116:448–455PubMed
go back to reference Torregrossa L, Shintu L, Nambiath Chandran J, Tintaru A, Ugolini C, Magalhaes A, Basolo F, Miccoli P, Caldarelli S (2012) Toward the reliable diagnosis of indeterminate thyroid lesions: a HRMAS NMR-based metabolomics case of study. J Proteome Res 11:3317–3325PubMed Torregrossa L, Shintu L, Nambiath Chandran J, Tintaru A, Ugolini C, Magalhaes A, Basolo F, Miccoli P, Caldarelli S (2012) Toward the reliable diagnosis of indeterminate thyroid lesions: a HRMAS NMR-based metabolomics case of study. J Proteome Res 11:3317–3325PubMed
go back to reference Tu R, Xia J (2024) Stroke and vascular cognitive impairment: the role of intestinal microbiota metabolite TMAO. CNS Neurol Disord Drug Targets 23:102–121PubMed Tu R, Xia J (2024) Stroke and vascular cognitive impairment: the role of intestinal microbiota metabolite TMAO. CNS Neurol Disord Drug Targets 23:102–121PubMed
go back to reference Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, Wu Y, Schauer P, Smith JD, Allayee H, Tang WH, DiDonato JA, Lusis AJ, Hazen SL (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:57–63PubMedPubMedCentral Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, Dugar B, Feldstein AE, Britt EB, Fu X, Chung YM, Wu Y, Schauer P, Smith JD, Allayee H, Tang WH, DiDonato JA, Lusis AJ, Hazen SL (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472:57–63PubMedPubMedCentral
go back to reference Wang H, Rong X, Zhao G, Zhou Y, Xiao Y, Ma D, Jin X, Wu Y, Yan Y, Yang H, Zhou Y, Qian M, Niu C, Hu X, Li DQ, Liu Q, Wen Y, Jiang YZ, Zhao C, Shao ZM (2022) The microbial metabolite trimethylamine N-oxide promotes antitumor immunity in triple-negative breast cancer. Cell Metab 34(581–594):e588 Wang H, Rong X, Zhao G, Zhou Y, Xiao Y, Ma D, Jin X, Wu Y, Yan Y, Yang H, Zhou Y, Qian M, Niu C, Hu X, Li DQ, Liu Q, Wen Y, Jiang YZ, Zhao C, Shao ZM (2022) The microbial metabolite trimethylamine N-oxide promotes antitumor immunity in triple-negative breast cancer. Cell Metab 34(581–594):e588
go back to reference Yang S, Dai H, Lu Y, Li R, Gao C, Pan S (2022) Trimethylamine N-oxide promotes cell proliferation and angiogenesis in colorectal cancer. J Immunol Res 2022:7043856PubMedPubMedCentral Yang S, Dai H, Lu Y, Li R, Gao C, Pan S (2022) Trimethylamine N-oxide promotes cell proliferation and angiogenesis in colorectal cancer. J Immunol Res 2022:7043856PubMedPubMedCentral
go back to reference Youn J, Cho E, Lee JE (2019) Association of choline and betaine levels with cancer incidence and survival: a meta-analysis. Clin Nutr 38:100–109PubMed Youn J, Cho E, Lee JE (2019) Association of choline and betaine levels with cancer incidence and survival: a meta-analysis. Clin Nutr 38:100–109PubMed
go back to reference Zeisel SH, da Costa KA (2009) Choline: an essential nutrient for public health. Nutr Rev 67:615–623PubMed Zeisel SH, da Costa KA (2009) Choline: an essential nutrient for public health. Nutr Rev 67:615–623PubMed
go back to reference Zhao WX, Wang B, Zhang LY, Yan SY, Yang YH (2015) Analysis on the metabolite composition of serum samples from patients with papillary thyroid carcinoma using nuclear magnetic resonance. Int J Clin Exp Med 8:18013–18022PubMedPubMedCentral Zhao WX, Wang B, Zhang LY, Yan SY, Yang YH (2015) Analysis on the metabolite composition of serum samples from patients with papillary thyroid carcinoma using nuclear magnetic resonance. Int J Clin Exp Med 8:18013–18022PubMedPubMedCentral
go back to reference Zhou J, Li Y, Chen X, Zhong L, Yin Y (2017) Development of data-independent acquisition workflows for metabolomic analysis on a quadrupole-orbitrap platform. Talanta 164:128–136PubMed Zhou J, Li Y, Chen X, Zhong L, Yin Y (2017) Development of data-independent acquisition workflows for metabolomic analysis on a quadrupole-orbitrap platform. Talanta 164:128–136PubMed
Metadata
Title
Distinguishing benign and malignant thyroid nodules using plasma trimethylamine N-oxide, carnitine, choline and betaine
Authors
Liang Shi
Muhong Guo
Cuixiao Shi
Gu Gao
Xianghong Xu
Chuan Zhang
Jingjing Fu
Yudan Ni
Feng Wang
Xue Xue
Fei Yu
Publication date
01-03-2024
Publisher
Springer Berlin Heidelberg
Published in
Journal of Cancer Research and Clinical Oncology / Issue 3/2024
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-024-05666-w

Other articles of this Issue 3/2024

Journal of Cancer Research and Clinical Oncology 3/2024 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine