Probabilistic Quotient Normalization as Robust Method to Account for Dilution of Complex Biological Mixtures. Application in 1H NMR MetabonomicsClick to copy article linkArticle link copied!
Abstract
For the analysis of the spectra of complex biofluids, preprocessing methods play a crucial role in rendering the subsequent data analyses more robust and accurate. Normalization is a preprocessing method, which accounts for different dilutions of samples by scaling the spectra to the same virtual overall concentration. In the field of 1H NMR metabonomics integral normalization, which scales spectra to the same total integral, is the de facto standard. In this work, it is shown that integral normalization is a suboptimal method for normalizing spectra from metabonomic studies. Especially strong metabonomic changes, evident as massive amounts of single metabolites in samples, significantly hamper the integral normalization resulting in incorrectly scaled spectra. The probabilistic quotient normalization is introduced in this work. This method is based on the calculation of a most probable dilution factor by looking at the distribution of the quotients of the amplitudes of a test spectrum by those of a reference spectrum. Simulated spectra, spectra of urine samples from a metabonomic study with cyclosporin-A as the active compound, and spectra of more than 4000 samples of control animals demonstrate that the probabilistic quotient normalization is by far more robust and more accurate than the widespread integral normalization and vector length normalization.
*
To whom correspondence should be addressed. E-mail: [email protected]. Tel: +41(0)61 6882028. Fax: +41 (0)61 6887408.
Cited By
This article is cited by 1393 publications.
- Daniel Malmodin, Anders Bay Nord, Huma Zafar, Linda Paulson, B. Göran Karlsson, Åsa Torinsson Naluai. Preanalytical (Mis)Handling of Plasma Investigated by 1H NMR Metabolomics. ACS Omega 2024, Article ASAP.
- Brian Low, Yukai Wang, Tingting Zhao, Huaxu Yu, Tao Huan. Closing the Knowledge Gap of Post-Acquisition Sample Normalization in Untargeted Metabolomics. ACS Measurement Science Au 2024, Article ASAP.
- Friederike Gutmann, Raphaela Fritsche-Guenther, Daniela B. Dias, Jennifer A. Kirwan. Comparing the Extraction Performance in Mouse Plasma of Different Biphasic Methods for Polar and Nonpolar Compounds. Journal of Proteome Research 2024, 23
(8)
, 2961-2969. https://doi.org/10.1021/acs.jproteome.3c00596
- Elena Sostare, Tara J. Bowen, Thomas N. Lawson, Anne Freier, Xiaojing Li, Gavin R. Lloyd, Lukáš Najdekr, Andris Jankevics, Thomas Smith, Dorsa Varshavi, Christian Ludwig, John K. Colbourne, Ralf J. M. Weber, David M. Crizer, Scott S. Auerbach, John R. Bucher, Mark R. Viant. Metabolomics Simultaneously Derives Benchmark Dose Estimates and Discovers Metabolic Biotransformations in a Rat Bioassay. Chemical Research in Toxicology 2024, 37
(6)
, 923-934. https://doi.org/10.1021/acs.chemrestox.4c00002
- František Sedlák, Aleš Kvasnička, Barbora Marešová, Radana Brumarová, Dana Dobešová, Kateřina Dostálová, Karolína Šrámková, Martin Pehr, Pavel Šácha, David Friedecký, Jan Konvalinka. Parallel Metabolomics and Lipidomics of a PSMA/GCPII Deficient Mouse Model Reveal Alteration of NAAG Levels and Brain Lipid Composition. ACS Chemical Neuroscience 2024, 15
(7)
, 1342-1355. https://doi.org/10.1021/acschemneuro.3c00494
- João A. Rodrigues, Evla Ferro, Rita Araújo, Ana V. Henriques, Ana M. Gomes, Marta W. Vasconcelos, Ana M. Gil. Metabolic Evaluation of Lupin-Enriched Yogurt by Nuclear Magnetic Resonance Metabolomics. Journal of Agricultural and Food Chemistry 2024, 72
(1)
, 894-903. https://doi.org/10.1021/acs.jafc.3c05837
- Fynn Brix, Tobias Demetrowitsch, Julia Jensen-Kroll, Helena U. Zacharias, Silke Szymczak, Matthias Laudes, Stefan Schreiber, Karin Schwarz. Evaluating the Effect of Data Merging and Postacquisition Normalization on Statistical Analysis of Untargeted High-Resolution Mass Spectrometry Based Urinary Metabolomics Data. Analytical Chemistry 2024, 96
(1)
, 33-40. https://doi.org/10.1021/acs.analchem.3c01380
- Yaguo Gong, Wei Ding, Panpan Wang, Qibiao Wu, Xiaojun Yao, Qingxia Yang. Evaluating Machine Learning Methods of Analyzing Multiclass Metabolomics. Journal of Chemical Information and Modeling 2023, 63
(24)
, 7628-7641. https://doi.org/10.1021/acs.jcim.3c01525
- Francesca Di Cesare, Matteo Calgaro, Veronica Ghini, Diletta Francesca Squarzanti, Annachiara De Prisco, Annalisa Visciglia, Paola Zanetta, Roberta Rolla, Paola Savoia, Angela Amoruso, Barbara Azzimonti, Nicola Vitulo, Leonardo Tenori, Claudio Luchinat, Marco Pane. Exploring the Effects of Probiotic Treatment on Urinary and Serum Metabolic Profiles in Healthy Individuals. Journal of Proteome Research 2023, 22
(12)
, 3866-3878. https://doi.org/10.1021/acs.jproteome.3c00548
- Abigail A. Sommer, Fikir B. Arega, Yael Vodovotz. Assessment of Fish Oil Oxidation Using Low-Field Proton Nuclear Magnetic Resonance Spectroscopy. ACS Food Science & Technology 2023, 3
(9)
, 1476-1483. https://doi.org/10.1021/acsfoodscitech.3c00179
- Sherin Abdelrahman, Rui Ge, Hepi H. Susapto, Yang Liu, Faris Samkari, Manola Moretti, Xinzhi Liu, Robert Hoehndorf, Abdul-Hamid Emwas, Mariusz Jaremko, Ranim H. Rawas, Charlotte A. E. Hauser. The Impact of Mechanical Cues on the Metabolomic and Transcriptomic Profiles of Human Dermal Fibroblasts Cultured in Ultrashort Self-Assembling Peptide 3D Scaffolds. ACS Nano 2023, 17
(15)
, 14508-14531. https://doi.org/10.1021/acsnano.3c01176
- Ethan Stancliffe, Michaela Schwaiger-Haber, Miriam Sindelar, Matthew J. Murphy, Mette Soerensen, Gary J. Patti. An Untargeted Metabolomics Workflow that Scales to Thousands of Samples for Population-Based Studies. Analytical Chemistry 2022, 94
(50)
, 17370-17378. https://doi.org/10.1021/acs.analchem.2c01270
- Kang Chen, Xuetao Wei, Jian Zhang, Maaria Kortesniemi, Yumei Zhang, Baoru Yang. Effect of Acylated and Nonacylated Anthocyanins on Urine Metabolic Profile during the Development of Type 2 Diabetes in Zucker Diabetic Fatty Rats. Journal of Agricultural and Food Chemistry 2022, 70
(48)
, 15143-15156. https://doi.org/10.1021/acs.jafc.2c06802
- Sara Forcisi, Franco Moritz, Christopher J. Thompson, Basem Kanawati, Jenny Uhl, Carlos Afonso, Chantal D. Bader, Aiko Barsch, Berin A. Boughton, Rosalie K. Chu, Justine Ferey, Francisco Fernandez-Lima, Céline Guéguen, Dimitri Heintz, Mario Gomez-Hernandez, Kyoung-Soon Jang, Nikolas Kessler, Vaughn Mangal, Rolf Müller, Ryo Nakabayashi, Edith Nicol, Simone Nicolardi, Magnus Palmblad, Ljiljana Paša-Tolić, Jacob Porter, Isabelle Schmitz-Afonso, Jong Bok Seo, Eduardo Sommella, Yuri E. M. van der Burgt, Claire Villette, Matthias Witt, Ashley Wittrig, Jeremy J. Wolff, Michael L. Easterling, Frank H. Laukien, Philippe Schmitt-Kopplin. Large-Scale Interlaboratory DI-FT-ICR MS Comparability Study Employing Various Systems. Journal of the American Society for Mass Spectrometry 2022, 33
(12)
, 2203-2214. https://doi.org/10.1021/jasms.2c00082
- Luiz Leonardo Saldanha, Pierre-Marie Allard, Guilherme Dilarri, Santiago Codesido, Víctor González-Ruiz, Emerson Ferreira Queiroz, Henrique Ferreira, Jean-Luc Wolfender. Metabolomic- and Molecular Networking-Based Exploration of the Chemical Responses Induced in Citrus sinensis Leaves Inoculated with Xanthomonas citri. Journal of Agricultural and Food Chemistry 2022, 70
(46)
, 14693-14705. https://doi.org/10.1021/acs.jafc.2c05156
- Da-Wei Li, Abigail Leggett, Lei Bruschweiler-Li, Rafael Brüschweiler. COLMARq: A Web Server for 2D NMR Peak Picking and Quantitative Comparative Analysis of Cohorts of Metabolomics Samples. Analytical Chemistry 2022, 94
(24)
, 8674-8682. https://doi.org/10.1021/acs.analchem.2c00891
- Huaxu Yu, Peijun Sang, Tao Huan. Adaptive Box–Cox Transformation: A Highly Flexible Feature-Specific Data Transformation to Improve Metabolomic Data Normality for Better Statistical Analysis. Analytical Chemistry 2022, 94
(23)
, 8267-8276. https://doi.org/10.1021/acs.analchem.2c00503
- Gonçalo D. S. Correia, Panteleimon G. Takis, Caroline J. Sands, Anna M. Kowalka, Tricia Tan, Lance Turtle, Antonia Ho, Malcolm G. Semple, Peter J. M. Openshaw, J. Kenneth Baillie, Zoltán Takáts, Matthew R. Lewis. 1H NMR Signals from Urine Excreted Protein Are a Source of Bias in Probabilistic Quotient Normalization. Analytical Chemistry 2022, 94
(19)
, 6919-6923. https://doi.org/10.1021/acs.analchem.2c00466
- Osvaldo Burastero, Marisol Cabrera, Elias D. Lopez, Lucas A. Defelipe, Juan Pablo Arcon, Rosario Durán, Marcelo A. Marti, Adrian G. Turjanski. Specificity and Reactivity of Mycobacterium tuberculosis Serine/Threonine Kinases PknG and PknB. Journal of Chemical Information and Modeling 2022, 62
(7)
, 1723-1733. https://doi.org/10.1021/acs.jcim.1c01358
- Petra Tomášová, Petra Procházková, Radka Roubalová, Jiří Dvořák, Helena Tlaskalová-Hogenová, Martina Čermáková, Helena Pelantová, Blanka Šedivá, Marek Vecka, Hana Papežová, Marek Kuzma. NMR- and MS-Based Untargeted Metabolomic Study of Stool and Serum Samples from Patients with Anorexia Nervosa. Journal of Proteome Research 2022, 21
(3)
, 778-787. https://doi.org/10.1021/acs.jproteome.1c00537
- Ana M. Salmerón, Ana I. Tristán, Ana C. Abreu, Ignacio Fernández. Serum Colorectal Cancer Biomarkers Unraveled by NMR Metabolomics: Past, Present, and Future. Analytical Chemistry 2022, 94
(1)
, 417-430. https://doi.org/10.1021/acs.analchem.1c04360
- Liene Bervoets, Johannes H. Ippel, Agnieszka Smolinska, Niels van Best, Paul H. M. Savelkoul, Monique A. H. Mommers, John Penders. Practical and Robust NMR-Based Metabolic Phenotyping of Gut Health in Early Life. Journal of Proteome Research 2021, 20
(11)
, 5079-5087. https://doi.org/10.1021/acs.jproteome.1c00617
- Siying Liu, Qiushi Hu, Chao Li, Fangrong Zhang, Hongjing Gu, Xinrui Wang, Shuang Li, Lei Xue, Tobias Madl, Yun Zhang, Lei Zhou. Wide-Range, Rapid, and Specific Identification of Pathogenic Bacteria by Surface-Enhanced Raman Spectroscopy. ACS Sensors 2021, 6
(8)
, 2911-2919. https://doi.org/10.1021/acssensors.1c00641
- Giorgia Manzo, Federico Gianfanti, Charlotte K. Hind, Leanne Allison, Maria Clarke, Julia Hohenbichler, Ilene Limantoro, Bethany Martin, Phoebe Do Carmo Silva, Philip M. Ferguson, Alice C. Hodgson-Casson, Roland A. Fleck, J. Mark Sutton, David A. Phoenix, A. James Mason. Impacts of Metabolism and Organic Acids on Cell Wall Composition and Pseudomonas aeruginosa Susceptibility to Membrane Active Antimicrobials. ACS Infectious Diseases 2021, 7
(8)
, 2310-2323. https://doi.org/10.1021/acsinfecdis.1c00002
- Ornuma Haonon, Zhigang Liu, Rungtiwa Dangtakot, Kitti Intuyod, Porntip Pinlaor, Anucha Puapairoj, Ubon Cha’on, Chatchawan Sengthong, Thatsanapong Pongking, Sudarat Onsurathum, Manachai Yingklang, Jutarop Phetcharaburanin, Jia V. Li, Somchai Pinlaor. Opisthorchis viverrini Infection Induces Metabolic and Fecal Microbial Disturbances in Association with Liver and Kidney Pathologies in Hamsters. Journal of Proteome Research 2021, 20
(8)
, 3940-3951. https://doi.org/10.1021/acs.jproteome.1c00246
- Reika Masuda, Samantha Lodge, Philipp Nitschke, Manfred Spraul, Hartmut Schaefer, Sze-How Bong, Torben Kimhofer, Drew Hall, Ruey Leng Loo, Maider Bizkarguenaga, Chiara Bruzzone, Rubén Gil-Redondo, Nieves Embade, José M. Mato, Elaine Holmes, Julien Wist, Oscar Millet, Jeremy K. Nicholson. Integrative Modeling of Plasma Metabolic and Lipoprotein Biomarkers of SARS-CoV-2 Infection in Spanish and Australian COVID-19 Patient Cohorts. Journal of Proteome Research 2021, 20
(8)
, 4139-4152. https://doi.org/10.1021/acs.jproteome.1c00458
- Matthew J. Smith, Delyan P. Ivanov, Ralf J. M. Weber, Jonathan Wingfield, Mark R. Viant. Acoustic Mist Ionization Mass Spectrometry for Ultrahigh-Throughput Metabolomics Screening. Analytical Chemistry 2021, 93
(26)
, 9258-9266. https://doi.org/10.1021/acs.analchem.1c01616
- Olatomiwa O. Bifarin, David A. Gaul, Samyukta Sah, Rebecca S. Arnold, Kenneth Ogan, Viraj A. Master, David L. Roberts, Sharon H. Bergquist, John A. Petros, Facundo M. Fernández, Arthur S. Edison. Machine Learning-Enabled Renal Cell Carcinoma Status Prediction Using Multiplatform Urine-Based Metabolomics. Journal of Proteome Research 2021, 20
(7)
, 3629-3641. https://doi.org/10.1021/acs.jproteome.1c00213
- Ilce G. Medina-Meza, Joshua VanderWeide, Cristobal Torres-Palacios, Paolo Sabbatini. Quantitative Metabolomics Unveils the Impact of Agricultural Practices in the Grape Metabolome. ACS Agricultural Science & Technology 2021, 1
(3)
, 253-261. https://doi.org/10.1021/acsagscitech.1c00043
- Alexandre Mallet, Roumiana Tsenkova, Jelena Muncan, Cyrille Charnier, Éric Latrille, Ryad Bendoula, Jean-Philippe Steyer, Jean-Michel Roger. Relating Near-Infrared Light Path-Length Modifications to the Water Content of Scattering Media in Near-Infrared Spectroscopy: Toward a New Bouguer–Beer–Lambert Law. Analytical Chemistry 2021, 93
(17)
, 6817-6823. https://doi.org/10.1021/acs.analchem.1c00811
- Lenka Michálková, Štěpán Horník, Jan Sýkora, Lucie Habartová, Vladimír Setnička, Bohuš Bunganič. Early Detection of Pancreatic Cancer in Type 2 Diabetes Mellitus Patients Based on 1H NMR Metabolomics. Journal of Proteome Research 2021, 20
(3)
, 1744-1753. https://doi.org/10.1021/acs.jproteome.0c00990
- Samantha Lodge, Philipp Nitschke, Ruey Leng Loo, Torben Kimhofer, Sze-How Bong, Toby Richards, Sofina Begum, Manfred Spraul, Hartmut Schaefer, John C. Lindon, Elaine Holmes, Jeremy K. Nicholson. Low Volume in Vitro Diagnostic Proton NMR Spectroscopy of Human Blood Plasma for Lipoprotein and Metabolite Analysis: Application to SARS-CoV-2 Biomarkers. Journal of Proteome Research 2021, 20
(2)
, 1415-1423. https://doi.org/10.1021/acs.jproteome.0c00815
- Samantha Lodge, Philipp Nitschke, Torben Kimhofer, Jerome D. Coudert, Sofina Begum, Sze-How Bong, Toby Richards, Dale Edgar, Edward Raby, Manfred Spraul, Hartmut Schaefer, John C. Lindon, Ruey Leng Loo, Elaine Holmes, Jeremy K. Nicholson. NMR Spectroscopic Windows on the Systemic Effects of SARS-CoV-2 Infection on Plasma Lipoproteins and Metabolites in Relation to Circulating Cytokines. Journal of Proteome Research 2021, 20
(2)
, 1382-1396. https://doi.org/10.1021/acs.jproteome.0c00876
- Ruey Leng Loo, Samantha Lodge, Torben Kimhofer, Sze-How Bong, Sofina Begum, Luke Whiley, Nicola Gray, John C. Lindon, Philipp Nitschke, Nathan G. Lawler, Hartmut Schäfer, Manfred Spraul, Toby Richards, Jeremy K. Nicholson, Elaine Holmes. Quantitative In-Vitro Diagnostic NMR Spectroscopy for Lipoprotein and Metabolite Measurements in Plasma and Serum: Recommendations for Analytical Artifact Minimization with Special Reference to COVID-19/SARS-CoV-2 Samples. Journal of Proteome Research 2020, 19
(11)
, 4428-4441. https://doi.org/10.1021/acs.jproteome.0c00537
- Nuria Gómez-Cebrián, María García-Flores, José Rubio-Briones, José Antonio López-Guerrero, Antonio Pineda-Lucena, Leonor Puchades-Carrasco. Targeted Metabolomics Analyses Reveal Specific Metabolic Alterations in High-Grade Prostate Cancer Patients. Journal of Proteome Research 2020, 19
(10)
, 4082-4092. https://doi.org/10.1021/acs.jproteome.0c00493
- James R. Anderson, Marie M. Phelan, Laura Foddy, Peter D. Clegg, Mandy J. Peffers. Ex Vivo Equine Cartilage Explant Osteoarthritis Model: A Metabolomics and Proteomics Study. Journal of Proteome Research 2020, 19
(9)
, 3652-3667. https://doi.org/10.1021/acs.jproteome.0c00143
- Kang Chen, Xuetao Wei, Jian Zhang, Raghunath Pariyani, Johanna Jokioja, Maaria Kortesniemi, Kaisa M. Linderborg, Jari Heinonen, Tuomo Sainio, Yumei Zhang, Baoru Yang. Effects of Anthocyanin Extracts from Bilberry (Vaccinium myrtillus L.) and Purple Potato (Solanum tuberosum L. var. ‘Synkeä Sakari’) on the Plasma Metabolomic Profile of Zucker Diabetic Fatty Rats. Journal of Agricultural and Food Chemistry 2020, 68
(35)
, 9436-9450. https://doi.org/10.1021/acs.jafc.0c04125
- Mengni Cui, Alessia Trimigno, Violetta Aru, Bekzod Khakimov, Søren Balling Engelsen. Human Faecal 1H NMR Metabolomics: Evaluation of Solvent and Sample Processing on Coverage and Reproducibility of Signature Metabolites. Analytical Chemistry 2020, 92
(14)
, 9546-9555. https://doi.org/10.1021/acs.analchem.0c00606
- Ahmed Mohamed, Jeffrey Molendijk, Michelle M. Hill. lipidr: A Software Tool for Data Mining and Analysis of Lipidomics Datasets. Journal of Proteome Research 2020, 19
(7)
, 2890-2897. https://doi.org/10.1021/acs.jproteome.0c00082
- Jian Gao, Peng Bai, Yuanyuan Li, Jingzhong Li, Caixia Jia, Tieshan Wang, Haibin Zhao, Yinchu Si, Jianxin Chen. Metabolomic Profiling of the Synergistic Effects of Ginsenoside Rg1 in Combination with Neural Stem Cell Transplantation in Ischemic Stroke Rats. Journal of Proteome Research 2020, 19
(7)
, 2676-2688. https://doi.org/10.1021/acs.jproteome.9b00639
- Chenglin Zhu, Luca Laghi, Zhizhong Zhang, Yongguo He, Daifu Wu, Hemin Zhang, Yan Huang, Caiwu Li, Likou Zou. First Steps toward the Giant Panda Metabolome Database: Untargeted Metabolomics of Feces, Urine, Serum, and Saliva by 1H NMR. Journal of Proteome Research 2020, 19
(3)
, 1052-1059. https://doi.org/10.1021/acs.jproteome.9b00564
- Caigui Lin, Jiyang Dong, Zhiliang Wei, Kian-Kai Cheng, Jie Li, Song You, Yueyue Liu, Xiaomin Wang, Zhong Chen. 1H NMR-Based Metabolic Profiles Delineate the Anticancer Effect of Vitamin C and Oxaliplatin on Hepatocellular Carcinoma Cells. Journal of Proteome Research 2020, 19
(2)
, 781-793. https://doi.org/10.1021/acs.jproteome.9b00635
- Emilien L. Jamin, Robin Costantino, Loïc Mervant, Jean-François Martin, Isabelle Jouanin, Florence Blas-Y-Estrada, Françoise Guéraud, Laurent Debrauwer. Global Profiling of Toxicologically Relevant Metabolites in Urine: Case Study of Reactive Aldehydes. Analytical Chemistry 2020, 92
(2)
, 1746-1754. https://doi.org/10.1021/acs.analchem.9b03146
- Alessia Vignoli, Giuseppe Santini, Leonardo Tenori, Giuseppe Macis, Nadia Mores, Francesco Macagno, Francesco Pagano, Tim Higenbottam, Claudio Luchinat, Paolo Montuschi. NMR-Based Metabolomics for the Assessment of Inhaled Pharmacotherapy in Chronic Obstructive Pulmonary Disease Patients. Journal of Proteome Research 2020, 19
(1)
, 64-74. https://doi.org/10.1021/acs.jproteome.9b00345
- Julia Debik, Leslie R. Euceda, Steinar Lundgren, Hedda von der Lippe Gythfeldt, Øystein Garred, Elin Borgen, Olav Engebraaten, Tone F. Bathen, Guro F. Giskeødegård. Assessing Treatment Response and Prognosis by Serum and Tissue Metabolomics in Breast Cancer Patients. Journal of Proteome Research 2019, 18
(10)
, 3649-3660. https://doi.org/10.1021/acs.jproteome.9b00316
- Thao Vu, Parker Siemek, Fatema Bhinderwala, Yuhang Xu, Robert Powers. Evaluation of Multivariate Classification Models for Analyzing NMR Metabolomics Data. Journal of Proteome Research 2019, 18
(9)
, 3282-3294. https://doi.org/10.1021/acs.jproteome.9b00227
- Kristina
Elisa Haslauer, Daniel Hemmler, Philippe Schmitt-Kopplin, Silke Sophie Heinzmann. Guidelines for the Use of Deuterium Oxide (D2O) in 1H NMR Metabolomics. Analytical Chemistry 2019, 91
(17)
, 11063-11069. https://doi.org/10.1021/acs.analchem.9b01580
- Christine Hinz, Sonia Liggi, Gabriele Mocciaro, Stephanie Jung, Isuru Induruwa, Milton Pereira, Clare E. Bryant, Sven W. Meckelmann, Valerie B. O’Donnell, Richard W. Farndale, John Fjeldsted, Julian L. Griffin. A Comprehensive UHPLC Ion Mobility Quadrupole Time-of-Flight Method for Profiling and Quantification of Eicosanoids, Other Oxylipins, and Fatty Acids. Analytical Chemistry 2019, 91
(13)
, 8025-8035. https://doi.org/10.1021/acs.analchem.8b04615
- Hannah J. Lees, Jonathan R. Swann, Simon Poucher, Elaine Holmes, Ian D. Wilson, Jeremy K. Nicholson. Obesity and Cage Environment Modulate Metabolism in the Zucker Rat: A Multiple Biological Matrix Approach to Characterizing Metabolic Phenomena. Journal of Proteome Research 2019, 18
(5)
, 2160-2174. https://doi.org/10.1021/acs.jproteome.9b00040
- Tharindu Fernando, Annick Sawala, Andrew P. Bailey, Alex P. Gould, Paul C. Driscoll. An Improved Method for Measuring Absolute Metabolite Concentrations in Small Biofluid or Tissue Samples. Journal of Proteome Research 2019, 18
(4)
, 1503-1512. https://doi.org/10.1021/acs.jproteome.8b00773
- Martina Čermáková, Helena Pelantová, Barbora Neprašová, Blanka Šedivá, Lenka Maletínská, Jaroslav Kuneš, Petra Tomášová, Blanka Železná, Marek Kuzma. Metabolomic Study of Obesity and Its Treatment with Palmitoylated Prolactin-Releasing Peptide Analog in Spontaneously Hypertensive and Normotensive Rats. Journal of Proteome Research 2019, 18
(4)
, 1735-1750. https://doi.org/10.1021/acs.jproteome.8b00964
- Alessia Vignoli, Beatrice Orlandini, Leonardo Tenori, Maria Rosa Biagini, Stefano Milani, Daniela Renzi, Claudio Luchinat, Antonino Salvatore Calabrò. Metabolic Signature of Primary Biliary Cholangitis and Its Comparison with Celiac Disease. Journal of Proteome Research 2019, 18
(3)
, 1228-1236. https://doi.org/10.1021/acs.jproteome.8b00849
- Covadonga Lucas-Torres, Gaspard Huber, Atsuyuki Ichikawa, Yusuke Nishiyama, Alan Wong. HR-μMAS NMR-Based Metabolomics: Localized Metabolic Profiling of a Garlic Clove with μg Tissues. Analytical Chemistry 2018, 90
(22)
, 13736-13743. https://doi.org/10.1021/acs.analchem.8b04150
- Léa Maitre, Oliver Robinson, David Martinez, Mireille B. Toledano, Jesús Ibarluzea, Loreto Santa Marina, Jordi Sunyer, Cristina M. Villanueva, Hector C. Keun, Martine Vrijheid, Muireann Coen. Urine Metabolic Signatures of Multiple Environmental Pollutants in Pregnant Women: An Exposome Approach. Environmental Science & Technology 2018, 52
(22)
, 13469-13480. https://doi.org/10.1021/acs.est.8b02215
- Francesc Puig-Castellví, Yolanda Pérez, Benjamín Piña, Romà Tauler, Ignacio Alfonso. Comparative analysis of 1H NMR and 1H–13C HSQC NMR metabolomics to understand the effects of medium composition in yeast growth. Analytical Chemistry 2018, 90
(21)
, 12422-12430. https://doi.org/10.1021/acs.analchem.8b01196
- Elena Chekmeneva, Gonçalo dos Santos Correia, María Gómez-Romero, Jeremiah Stamler, Queenie Chan, Paul Elliott, Jeremy K. Nicholson, Elaine Holmes. Ultra-Performance Liquid Chromatography–High-Resolution Mass Spectrometry and Direct Infusion–High-Resolution Mass Spectrometry for Combined Exploratory and Targeted Metabolic Profiling of Human Urine. Journal of Proteome Research 2018, 17
(10)
, 3492-3502. https://doi.org/10.1021/acs.jproteome.8b00413
- João
C. P. Silva, Marta Mota, Fátima O. Martins, Célia Nogueira, Teresa Gonçalves, Tatiana Carneiro, Joana Pinto, Daniela Duarte, António
S. Barros, John G. Jones, Ana M. Gil. Intestinal Microbial and Metabolic Profiling of Mice Fed with High-Glucose and High-Fructose Diets. Journal of Proteome Research 2018, 17
(8)
, 2880-2891. https://doi.org/10.1021/acs.jproteome.8b00354
- Francisco Madrid-Gambin, Carl Brunius, Mar Garcia-Aloy, Sheila Estruel-Amades, Rikard Landberg, Cristina Andres-Lacueva. Untargeted 1H NMR-Based Metabolomics Analysis of Urine and Serum Profiles after Consumption of Lentils, Chickpeas, and Beans: An Extended Meal Study To Discover Dietary Biomarkers of Pulses. Journal of Agricultural and Food Chemistry 2018, 66
(27)
, 6997-7005. https://doi.org/10.1021/acs.jafc.8b00047
- Francesc Puig-Castellví, Carmen Bedia, Ignacio Alfonso, Benjamin Piña, Romà Tauler. Deciphering the Underlying Metabolomic and Lipidomic Patterns Linked to Thermal Acclimation in Saccharomyces cerevisiae. Journal of Proteome Research 2018, 17
(6)
, 2034-2044. https://doi.org/10.1021/acs.jproteome.7b00921
- Yue-Xiao Xing, Ming-Hui Li, Liang Tao, Ling-Yu Ruan, Wei Hong, Cheng Chen, Wen-Long Zhao, Han Xu, Jian-Feng Chen, Jun-Song Wang. Anti-Cancer Effects of Emodin on HepG2 Cells as Revealed by 1H NMR Based Metabolic Profiling. Journal of Proteome Research 2018, 17
(5)
, 1943-1952. https://doi.org/10.1021/acs.jproteome.8b00029
- Jinping Gu, Chenyang Ji, Siqing Yue, Dan Shu, Feng Su, Yinjun Zhang, Yuanyuan Xie, Yi Zhang, Weiping Liu, Meirong Zhao. Enantioselective Effects of Metalaxyl Enantiomers in Adolescent Rat Metabolic Profiles Using NMR-Based Metabolomics. Environmental Science & Technology 2018, 52
(9)
, 5438-5447. https://doi.org/10.1021/acs.est.7b06540
- Joram M. Posma, Isabel Garcia-Perez, Timothy M. D. Ebbels, John C. Lindon, Jeremiah Stamler, Paul Elliott, Elaine Holmes, Jeremy K. Nicholson. Optimized Phenotypic Biomarker Discovery and Confounder Elimination via Covariate-Adjusted Projection to Latent Structures from Metabolic Spectroscopy Data. Journal of Proteome Research 2018, 17
(4)
, 1586-1595. https://doi.org/10.1021/acs.jproteome.7b00879
- Hyang-Gi Ji, Yeong-Ran Lee, Min-Seuk Lee, Kyeong Hwan Hwang, Clara Yongjoo Park, Eun-Hee Kim, Jun Seong Park, and Young-Shick Hong . Diverse Metabolite Variations in Tea (Camellia sinensis L.) Leaves Grown Under Various Shade Conditions Revisited: A Metabolomics Study. Journal of Agricultural and Food Chemistry 2018, 66
(8)
, 1889-1897. https://doi.org/10.1021/acs.jafc.7b04768
- Guiping Shen, Ying Huang, Jiyang Dong, Xuexi Wang, Kian-Kai Cheng, Jianghua Feng, Jingjing Xu, and Jidan Ye . Metabolic Effect of Dietary Taurine Supplementation on Nile Tilapia (Oreochromis nilotictus) Evaluated by NMR-Based Metabolomics. Journal of Agricultural and Food Chemistry 2018, 66
(1)
, 368-377. https://doi.org/10.1021/acs.jafc.7b03182
- Rhiannon Bray, Stefano Cacciatore, Beatriz Jiménez, Rufus Cartwright, Alex Digesu, Ruwan Fernando, Elaine Holmes, Jeremy K. Nicholson, Phillip R. Bennett, David A. MacIntyre, and Vik Khullar . Urinary Metabolic Phenotyping of Women with Lower Urinary Tract Symptoms. Journal of Proteome Research 2017, 16
(11)
, 4208-4216. https://doi.org/10.1021/acs.jproteome.7b00568
- Pingping Jiang, Alessia Trimigno, Jan Stanstrup, Bekzod Khakimov, Nanna Viereck, Søren Balling Engelsen, Per Torp Sangild, and Lars Ove Dragsted . Antibiotic Treatment Preventing Necrotising Enterocolitis Alters Urinary and Plasma Metabolomes in Preterm Pigs. Journal of Proteome Research 2017, 16
(10)
, 3547-3557. https://doi.org/10.1021/acs.jproteome.7b00263
- Helena U. Zacharias, Thorsten Rehberg, Sebastian Mehrl, Daniel Richtmann, Tilo Wettig, Peter J. Oefner, Rainer Spang, Wolfram Gronwald, and Michael Altenbuchinger . Scale-Invariant Biomarker Discovery in Urine and Plasma Metabolite Fingerprints. Journal of Proteome Research 2017, 16
(10)
, 3596-3605. https://doi.org/10.1021/acs.jproteome.7b00325
- Raphaële Castagné, Claire Laurence Boulangé, Ibrahim Karaman, Gianluca Campanella, Diana L. Santos Ferreira, Manuja R. Kaluarachchi, Benjamin Lehne, Alireza Moayyeri, Matthew R. Lewis, Konstantina Spagou, Anthony C. Dona, Vangelis Evangelos, Russell Tracy, Philip Greenland, John C. Lindon, David Herrington, Timothy M. D. Ebbels, Paul Elliott, Ioanna Tzoulaki, and Marc Chadeau-Hyam . Improving Visualization and Interpretation of Metabolome-Wide Association Studies: An Application in a Population-Based Cohort Using Untargeted 1H NMR Metabolic Profiling. Journal of Proteome Research 2017, 16
(10)
, 3623-3633. https://doi.org/10.1021/acs.jproteome.7b00344
- Aurélien Scalabre, Elodie Jobard, Delphine Demède, Ségolène Gaillard, Clément Pontoizeau, Pierre Mouriquand, Bénédicte Elena-Herrmann, Pierre-Yves Mure. Evolution of Newborns’ Urinary Metabolomic Profiles According to Age and Growth. Journal of Proteome Research 2017, 16
(10)
, 3732-3740. https://doi.org/10.1021/acs.jproteome.7b00421
- Linda
H. Münger, Alessia Trimigno, Gianfranco Picone, Carola Freiburghaus, Grégory Pimentel, Kathryn J. Burton, François
P. Pralong, Nathalie Vionnet, Francesco Capozzi, René Badertscher, Guy Vergères. Identification of Urinary Food Intake Biomarkers for Milk, Cheese, and Soy-Based Drink by Untargeted GC-MS and NMR in Healthy Humans. Journal of Proteome Research 2017, 16
(9)
, 3321-3335. https://doi.org/10.1021/acs.jproteome.7b00319
- Adriana N. Macedo, Stellena Mathiaparanam, Lauren Brick, Katherine Keenan, Tanja Gonska, Linda Pedder, Stephen Hill, and Philip Britz-McKibbin . The Sweat Metabolome of Screen-Positive Cystic Fibrosis Infants: Revealing Mechanisms beyond Impaired Chloride Transport. ACS Central Science 2017, 3
(8)
, 904-913. https://doi.org/10.1021/acscentsci.7b00299
- Luisa M. Ostertag, Mark Philo, Ian J. Colquhoun, Henri S. Tapp, Shikha Saha, Garry G. Duthie, E. Kate Kemsley, Baukje de Roos, Paul A. Kroon, and Gwénaëlle Le Gall . Acute Consumption of Flavan-3-ol-Enriched Dark Chocolate Affects Human Endogenous Metabolism. Journal of Proteome Research 2017, 16
(7)
, 2516-2526. https://doi.org/10.1021/acs.jproteome.7b00089
- Jiaqing Chen, Pei Zhang, Mengying Lv, Huimin Guo, Yin Huang, Zunjian Zhang, and Fengguo Xu . Influences of Normalization Method on Biomarker Discovery in Gas Chromatography–Mass Spectrometry-Based Untargeted Metabolomics: What Should Be Considered?. Analytical Chemistry 2017, 89
(10)
, 5342-5348. https://doi.org/10.1021/acs.analchem.6b05152
- Inês Lamego, M. Paula M. Marques, Iola F. Duarte, Ana S. Martins, Helena Oliveira, and Ana M. Gil . Impact of the Pd2Spermine Chelate on Osteosarcoma Metabolism: An NMR Metabolomics Study. Journal of Proteome Research 2017, 16
(4)
, 1773-1783. https://doi.org/10.1021/acs.jproteome.7b00035
- Pamela Pruski, David A. MacIntyre, Holly V. Lewis, Paolo Inglese, Gonçalo D. S. Correia, Trevor T. Hansel, Phillip R. Bennett, Elaine Holmes, and Zoltan Takats . Medical Swab Analysis Using Desorption Electrospray Ionization Mass Spectrometry: A Noninvasive Approach for Mucosal Diagnostics. Analytical Chemistry 2017, 89
(3)
, 1540-1550. https://doi.org/10.1021/acs.analchem.6b03405
- Edoardo Saccenti . Correlation Patterns in Experimental Data Are Affected by Normalization Procedures: Consequences for Data Analysis and Network Inference. Journal of Proteome Research 2017, 16
(2)
, 619-634. https://doi.org/10.1021/acs.jproteome.6b00704
- Muhammad Saeed Ahmad, Munirah Alsaleh, Torben Kimhofer, Sultan Ahmad, Wisam Jamal, Siraj Omar Wali, Jeremy Kirk Nicholson, Zoheir Abdullah Damanhouri, and Elaine Holmes . Metabolic Phenotype of Obesity in a Saudi Population. Journal of Proteome Research 2017, 16
(2)
, 635-644. https://doi.org/10.1021/acs.jproteome.6b00710
- Ibrahim Karaman, Diana L. S. Ferreira, Claire L. Boulangé, Manuja R. Kaluarachchi, David Herrington, Anthony C. Dona, Raphaële Castagné, Alireza Moayyeri, Benjamin Lehne, Marie Loh, Paul S. de Vries, Abbas Dehghan, Oscar H. Franco, Albert Hofman, Evangelos Evangelou, Ioanna Tzoulaki, Paul Elliott, John C. Lindon, and Timothy M. D. Ebbels . Workflow for Integrated Processing of Multicohort Untargeted 1H NMR Metabolomics Data in Large-Scale Metabolic Epidemiology. Journal of Proteome Research 2016, 15
(12)
, 4188-4194. https://doi.org/10.1021/acs.jproteome.6b00125
- Mun-Gwan Hong, Woojoo Lee, Peter Nilsson, Yudi Pawitan, and Jochen M. Schwenk . Multidimensional Normalization to Minimize Plate Effects of Suspension Bead Array Data. Journal of Proteome Research 2016, 15
(10)
, 3473-3480. https://doi.org/10.1021/acs.jproteome.5b01131
- Frances Jackson, Nancy Georgakopoulou, Manuja Kaluarachchi, Michael Kyriakides, Nicholas Andreas, Natalia Przysiezna, Matthew J. Hyde, Neena Modi, Jeremy K. Nicholson, Anisha Wijeyesekera, and Elaine Holmes . Development of a Pipeline for Exploratory Metabolic Profiling of Infant Urine. Journal of Proteome Research 2016, 15
(9)
, 3432-3440. https://doi.org/10.1021/acs.jproteome.6b00234
- José I. Serrano-Contreras, Isabel García-Pérez, María E. Meléndez-Camargo, and L. Gerardo Zepeda . NMR-Based Metabonomic Analysis of Physiological Responses to Starvation and Refeeding in the Rat. Journal of Proteome Research 2016, 15
(9)
, 3241-3254. https://doi.org/10.1021/acs.jproteome.6b00433
- Xin Zou, Elaine Holmes, Jeremy K Nicholson, and Ruey Leng Loo . Automatic Spectroscopic Data Categorization by Clustering Analysis (ASCLAN): A Data-Driven Approach for Distinguishing Discriminatory Metabolites for Phenotypic Subclasses. Analytical Chemistry 2016, 88
(11)
, 5670-5679. https://doi.org/10.1021/acs.analchem.5b04020
- Eun-Hye Song, Hyun-Ju Kim, Jaesik Jeong, Hyun-Jung Chung, Han-Yong Kim, Eunjung Bang, and Young-Shick Hong . A 1H HR-MAS NMR-Based Metabolomic Study for Metabolic Characterization of Rice Grain from Various Oryza sativa L. Cultivars. Journal of Agricultural and Food Chemistry 2016, 64
(15)
, 3009-3016. https://doi.org/10.1021/acs.jafc.5b05667
- Jie Hao, Manuel Liebeke, Ulf Sommer, Mark R. Viant, Jacob G. Bundy, and Timothy M. D. Ebbels . Statistical Correlations between NMR Spectroscopy and Direct Infusion FT-ICR Mass Spectrometry Aid Annotation of Unknowns in Metabolomics. Analytical Chemistry 2016, 88
(5)
, 2583-2589. https://doi.org/10.1021/acs.analchem.5b02889
- Yuka Shiokawa, Takuma Misawa, Yasuhiro Date, and Jun Kikuchi . Application of Market Basket Analysis for the Visualization of Transaction Data Based on Human Lifestyle and Spectroscopic Measurements. Analytical Chemistry 2016, 88
(5)
, 2714-2719. https://doi.org/10.1021/acs.analchem.5b04182
- Johannes Hertel, Nele Friedrich, Katharina Wittfeld, Maik Pietzner, Kathrin Budde, Sandra Van der Auwera, Tobias Lohmann, Alexander Teumer, Henry Völzke, Matthias Nauck, and Hans Jörgen Grabe . Measuring Biological Age via Metabonomics: The Metabolic Age Score. Journal of Proteome Research 2016, 15
(2)
, 400-410. https://doi.org/10.1021/acs.jproteome.5b00561
- Abdul-Hamid Emwas, Raja Roy, Ryan T. McKay, Danielle Ryan, Lorraine Brennan, Leonardo Tenori, Claudio Luchinat, Xin Gao, Ana Carolina Zeri, G. A. Nagana Gowda, Daniel Raftery, Christoph Steinbeck, Reza M. Salek, and David S. Wishart . Recommendations and Standardization of Biomarker Quantification Using NMR-Based Metabolomics with Particular Focus on Urinary Analysis. Journal of Proteome Research 2016, 15
(2)
, 360-373. https://doi.org/10.1021/acs.jproteome.5b00885
- Chongyang Huang, Qi Zhou, Shan Gao, Qingjia Bao, Fang Chen, and Chaoyang Liu . Time-Domain Nuclear Magnetic Resonance Investigation of Water Dynamics in Different Ginger Cultivars. Journal of Agricultural and Food Chemistry 2016, 64
(2)
, 470-477. https://doi.org/10.1021/acs.jafc.5b05417
- Sílvia O. Diaz, Joana Pinto, António S. Barros, Elisabete Morais, Daniela Duarte, Fátima Negrão, Cristina Pita, Maria do Céu Almeida, Isabel M. Carreira, Manfred Spraul, and Ana M. Gil . Newborn Urinary Metabolic Signatures of Prematurity and Other Disorders: A Case Control Study. Journal of Proteome Research 2016, 15
(1)
, 311-325. https://doi.org/10.1021/acs.jproteome.5b00977
- Sarah K. Davies, Jacob G. Bundy, and Armand M. Leroi . Metabolic Youth in Middle Age: Predicting Aging in Caenorhabditis elegans Using Metabolomics. Journal of Proteome Research 2015, 14
(11)
, 4603-4609. https://doi.org/10.1021/acs.jproteome.5b00442
- Guan-Yuan Chen, Hsiao-Wei Liao, I-Lin Tsai, Yufeng Jane Tseng, and Ching-Hua Kuo . Using the Matrix-Induced Ion Suppression Method for Concentration Normalization in Cellular Metabolomics Studies. Analytical Chemistry 2015, 87
(19)
, 9731-9739. https://doi.org/10.1021/acs.analchem.5b01869
- Silke S. Heinzmann, Elaine Holmes, Sunil Kochhar, Jeremy K. Nicholson, and Philippe Schmitt-Kopplin . 2-Furoylglycine as a Candidate Biomarker of Coffee Consumption. Journal of Agricultural and Food Chemistry 2015, 63
(38)
, 8615-8621. https://doi.org/10.1021/acs.jafc.5b03040
- Jochen Hochrein, Helena U. Zacharias, Franziska Taruttis, Claudia Samol, Julia C. Engelmann, Rainer Spang, Peter J. Oefner, and Wolfram Gronwald . Data Normalization of 1H NMR Metabolite Fingerprinting Data Sets in the Presence of Unbalanced Metabolite Regulation. Journal of Proteome Research 2015, 14
(8)
, 3217-3228. https://doi.org/10.1021/acs.jproteome.5b00192
- Joana Pinto, Lara M. Almeida, Ana S. Martins, Daniela Duarte, António S. Barros, Eulália Galhano, Cristina Pita, Maria do Céu Almeida, Isabel M. Carreira, and Ana M. Gil . Prediction of Gestational Diabetes through NMR Metabolomics of Maternal Blood. Journal of Proteome Research 2015, 14
(6)
, 2696-2706. https://doi.org/10.1021/acs.jproteome.5b00260
- Chaevien S. Clendinen, Christian Pasquel, Ramadan Ajredini, and Arthur S. Edison . 13C NMR Metabolomics: INADEQUATE Network Analysis. Analytical Chemistry 2015, 87
(11)
, 5698-5706. https://doi.org/10.1021/acs.analchem.5b00867
- Lyamine Hedjazi, Dominique Gauguier, Pierre A. Zalloua, Jeremy K. Nicholson, Marc-Emmanuel Dumas, and Jean-Baptiste Cazier . mQTL.NMR: An Integrated Suite for Genetic Mapping of Quantitative Variations of 1H NMR-Based Metabolic Profiles. Analytical Chemistry 2015, 87
(8)
, 4377-4384. https://doi.org/10.1021/acs.analchem.5b00145
- Joana Pinto, António S. Barros, Maria Rosário M. Domingues, Brian J. Goodfellow, Eulália Galhano, Cristina Pita, Maria do Céu Almeida, Isabel M. Carreira, and Ana M. Gil . Following Healthy Pregnancy by NMR Metabolomics of Plasma and Correlation to Urine. Journal of Proteome Research 2015, 14
(2)
, 1263-1274. https://doi.org/10.1021/pr5011982
- Mattias Rantalainen, Jacob Tveiten Bjerrum, Jørgen Olsen, Ole Haagen Nielsen, and Yulan Wang . Integrative Transcriptomic and Metabonomic Molecular Profiling of Colonic Mucosal Biopsies Indicates a Unique Molecular Phenotype for Ulcerative Colitis. Journal of Proteome Research 2015, 14
(1)
, 479-490. https://doi.org/10.1021/pr500699h
- Sabrina D. Lamour, Kirill A. Veselkov, Joram M. Posma, Emilie Giraud, Matthew E. Rogers, Simon Croft, Julian R. Marchesi, Elaine Holmes, Karin Seifert, and Jasmina Saric . Metabolic, Immune, and Gut Microbial Signals Mount a Systems Response to Leishmania major Infection. Journal of Proteome Research 2015, 14
(1)
, 318-329. https://doi.org/10.1021/pr5008202
- Alma Villaseñor, James M. Kinross, Jia V. Li, Nicholas Penney, Richard H. Barton, Jeremy K. Nicholson, Ara Darzi, Coral Barbas, and Elaine Holmes . 1H NMR Global Metabolic Phenotyping of Acute Pancreatitis in the Emergency Unit. Journal of Proteome Research 2014, 13
(12)
, 5362-5375. https://doi.org/10.1021/pr500161w
Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.
Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.
The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.