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Streptococcus pneumoniae and Staphylococcus aureus Pneumonia Induce Distinct Metabolic Responses

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Department of Medicine, and Magnetic Resonance Diagnostics Centre, 550A HMRC, University of Alberta, Edmonton, Alberta, Canada T6G 2S2
* Corresponding author: Carolyn Slupsky, Department of Medicine, 550A Heritage Medical Research Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2S2. Phone: (780) 492 - 8919. Fax: (780) 492 - 5329.
†Department of Medicine, University of Alberta.
#Contributed equally to this work.
‡Magnetic Resonance Diagnostics Centre, University of Alberta.
Cite this: J. Proteome Res. 2009, 8, 6, 3029–3036
Publication Date (Web):April 15, 2009
https://doi.org/10.1021/pr900103y
Copyright © 2009 American Chemical Society
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Abstract

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Pneumonia is an infection of the lower respiratory tract caused by microbial pathogens. Two such pathogens, Streptococcus pneumoniae and Staphylococcus aureus, are the most common causes of community-acquired and hospital-acquired pneumonia respectively. Each expresses strains highly resistant to penicillin and other antibiotics, and a significant number of people succumb to infection by these pathogens every year. Urinary metabolite changes in a C57Bl/6 mouse model with lung infection from either S. pneumoniae or S. aureus were characterized using multivariate targeted profiling data obtained from 1H NMR spectra. Marked changes in the urinary metabolite profile occurred within 24 h after infection with either pathogen. Specifically, significant decreases in TCA cycle intermediates, coupled with increases in fucose, creatine, and taurine were observed in the urine of S. pneumoniae-treated mice. Infection with S. aureus resulted in the decrease of a number of urinary metabolites including 1-methylnicotinamide, 3-methyl-2-oxovalerate, 2-oxoisocaproate, N-isovaleroylglycine and others. Disturbances in gut-derived microbial metabolites were also observed. Analysis of metabolic trajectory data indicated that, as the mice recovered from infection, their urinary metabolic profile became similar to that of the preinfected state. These results underline the potential of metabolomics as a tool for diagnosis, health monitoring, and drug development, and show its usefulness for understanding microbial-host interactions.

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  2. Khalid Muzaffar Banday, Kishore Kumar Pasikanti, Eric Chun Yong Chan, Rupak Singla, Kanury Venkata Subba Rao, Virander Singh Chauhan, and Ranjan Kumar Nanda . Use of Urine Volatile Organic Compounds To Discriminate Tuberculosis Patients from Healthy Subjects. Analytical Chemistry 2011, 83 (14) , 5526-5534. https://doi.org/10.1021/ac200265g
  3. Ji-Hyun Shin, Ji-Young Yang, Bo-Young Jeon, Yoo Jeong Yoon, Sang-Nae Cho, Yeon-Ho Kang, Do Hyun Ryu, and Geum-Sook Hwang . 1H NMR-based Metabolomic Profiling in Mice Infected with Mycobacterium tuberculosis. Journal of Proteome Research 2011, 10 (5) , 2238-2247. https://doi.org/10.1021/pr101054m
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  5. Xiang-Min Lin, Jun-Ning Yang, Xuan-Xian Peng, and Hui Li. A Novel Negative Regulation Mechanism of Bacterial Outer Membrane Proteins in Response to Antibiotic Resistance. Journal of Proteome Research 2010, 9 (11) , 5952-5959. https://doi.org/10.1021/pr100740w
  6. Carolyn M. Slupsky, Kathryn N. Rankin, Hao Fu, David Chang, Brian H. Rowe, Patrick G. P. Charles, Allison McGeer, Donald Low, Richard Long, Dennis Kunimoto, Michael B. Sawyer, Richard N. Fedorak, Darryl J. Adamko, Erik J. Saude, Sirish L. Shah and Thomas J. Marrie . Pneumococcal Pneumonia: Potential for Diagnosis through a Urinary Metabolic Profile. Journal of Proteome Research 2009, 8 (12) , 5550-5558. https://doi.org/10.1021/pr9006427
  7. Xiaoguang Li, Juan Du, Jing Chen, Fei Lin, Wei Wang, Ting-Ting Wei, Jie Xu, Qing-Bin Lu. Metabolic profile of exhaled breath condensate from the pneumonia patients. Experimental Lung Research 2022, 48 (4-6) , 149-157. https://doi.org/10.1080/01902148.2022.2078019
  8. Emily Wildman, Beata Mickiewicz, Hans J. Vogel, Graham C. Thompson. Metabolomics in pediatric lower respiratory tract infections and sepsis: a literature review. Pediatric Research 2022, 17 https://doi.org/10.1038/s41390-022-02162-0
  9. Zoran Stojanovic, Filipe Gonçalves-Carvalho, Alicia Marín, Jorge Abad Capa, Jose Domínguez, Irene Latorre, Alicia Lacoma, Cristina Prat-Aymerich. Advances in diagnostic tools for respiratory tract infections: from tuberculosis to COVID-19 – changing paradigms?. ERJ Open Research 2022, 8 (3) , 00113-2022. https://doi.org/10.1183/23120541.00113-2022
  10. Yu-Hsuan Liao, Chung-Hung Shih, Maysam F. Abbod, Jiann-Shing Shieh, Yu-Jen Hsiao. Development of an E-nose system using machine learning methods to predict ventilator-associated pneumonia. Microsystem Technologies 2022, 28 (1) , 341-351. https://doi.org/10.1007/s00542-020-04782-0
  11. Bart’s Jongers, An Hotterbeekx, Kenny Bielen, Philippe Vervliet, Jan Boddaert, Christine Lammens, Erik Fransen, Geert Baggerman, Adrian Covaci, Herman Goossens, Surbhi Malhotra-Kumar, Philippe G Jorens, Samir Kumar-Singh. Identification of Potential Urinary Metabolite Biomarkers of Pseudomonas aeruginosa Ventilator-Associated Pneumonia. Biomarker Insights 2022, 17 , 117727192210991. https://doi.org/10.1177/11772719221099131
  12. Lilliam Ambroggio, Todd A. Florin, Kayla Williamson, Cory Pfefferman, Brandie D. Wagner, Larisa Yeomans, Jae Hyun Kim, Heidi Sucharew, Maurizio Macaluso, Richard M. Ruddy, Samir S. Shah, Kathleen A. Stringer. Respiratory Colonization and Short-Term Temporal Changes in the Urinary Metabolome of Children. Metabolites 2021, 11 (8) , 500. https://doi.org/10.3390/metabo11080500
  13. Britney L. Hardy, D. Scott Merrell, . Friend or Foe: Interbacterial Competition in the Nasal Cavity. Journal of Bacteriology 2021, 203 (5) https://doi.org/10.1128/JB.00480-20
  14. , M. Drobot. INDICATORS OF PROTEIN METABOLISM IN CALVES WITH BRONCHOPNEUMONIA UNDER INDIVIDUAL THERAPY. Ukrainian journal of veterinary sciences 2020, 11 (4) https://doi.org/10.31548/ujvs2020.04.007
  15. C. Blakebrough-Hall, A. Dona, M. J. D’occhio, J. McMeniman, L. A González. Diagnosis of Bovine Respiratory Disease in feedlot cattle using blood 1H NMR metabolomics. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-019-56809-w
  16. Nirmal S. Sharma, Grant Vestal, Keith Wille, Kapil N. Patel, Feng Cheng, Srinivas Tipparaju, Sultan Tousif, Mudassir M. Banday, Xin Xu, Landon Wilson, Viswam S. Nair, Casey Morrow, Don Hayes, Andreas Seyfang, Stephen Barnes, Jessy S. Deshane, Amit Gaggar. Differences in airway microbiome and metabolome of single lung transplant recipients. Respiratory Research 2020, 21 (1) https://doi.org/10.1186/s12931-020-01367-3
  17. Joseph F. Pierre, Oguz Akbilgic, Heather Smallwood, Xueyuan Cao, Elizabeth A. Fitzpatrick, Senen Pena, Stephen P. Furmanek, Julio A. Ramirez, Colleen B. Jonsson. Discovery and predictive modeling of urine microbiome, metabolite and cytokine biomarkers in hospitalized patients with community acquired pneumonia. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-020-70461-9
  18. Jelle Vlaeminck, Dina Raafat, Kristin Surmann, Leen Timbermont, Nicole Normann, Bret Sellman, Willem J. B. van Wamel, Surbhi Malhotra-Kumar. Exploring Virulence Factors and Alternative Therapies against Staphylococcus aureus Pneumonia. Toxins 2020, 12 (11) , 721. https://doi.org/10.3390/toxins12110721
  19. Lingling Zheng, Fangqin Lin, Changxi Zhu, Guangjian Liu, Xiaohui Wu, Zhiyuan Wu, Jianbin Zheng, Huimin Xia, Yi Cai, Huiying Liang. Machine Learning Algorithms Identify Pathogen-Specific Biomarkers of Clinical and Metabolomic Characteristics in Septic Patients with Bacterial Infections. BioMed Research International 2020, 2020 , 1-11. https://doi.org/10.1155/2020/6950576
  20. David S. Wishart. Metabolomics for Investigating Physiological and Pathophysiological Processes. Physiological Reviews 2019, 99 (4) , 1819-1875. https://doi.org/10.1152/physrev.00035.2018
  21. Helen E. Rich, Collin C. McCourt, Wen Quan Zheng, Kevin J. McHugh, Keven M. Robinson, Jieru Wang, John F. Alcorn, . Interferon Lambda Inhibits Bacterial Uptake during Influenza Superinfection. Infection and Immunity 2019, 87 (5) https://doi.org/10.1128/IAI.00114-19
  22. Britney L. Hardy, Seth W. Dickey, Roger D. Plaut, Daniel P. Riggins, Scott Stibitz, Michael Otto, D. Scott Merrell, . Corynebacterium pseudodiphtheriticum Exploits Staphylococcus aureus Virulence Components in a Novel Polymicrobial Defense Strategy. mBio 2019, 10 (1) https://doi.org/10.1128/mBio.02491-18
  23. January Weiner, Robert P. Mohney, Stefan H.E. Kaufmann. The potential of metabolic profiling for vaccine development. Seminars in Immunology 2018, 39 , 44-51. https://doi.org/10.1016/j.smim.2018.07.002
  24. Sayed Metwaly, Andreanne Cote, Sarah J. Donnelly, Mohammad M. Banoei, Ahmed I. Mourad, Brent W. Winston. Evolution of ARDS biomarkers: Will metabolomics be the answer?. American Journal of Physiology-Lung Cellular and Molecular Physiology 2018, 315 (4) , L526-L534. https://doi.org/10.1152/ajplung.00074.2018
  25. Hans J. Vogel, Mauricio Arias, James M. Aramini, Subrata Paul, Zhihong Liu, Hiroaki Ishida. Characterization of Antimicrobial and Host-Defense Peptides by NMR Spectroscopy. 2018,,, 2055-2079. https://doi.org/10.1007/978-3-319-28388-3_119
  26. , Mohammad M. Banoei, Hans J. Vogel, Aalim M. Weljie, Anand Kumar, Sachin Yende, Derek C. Angus, Brent W. Winston. Plasma metabolomics for the diagnosis and prognosis of H1N1 influenza pneumonia. Critical Care 2017, 21 (1) https://doi.org/10.1186/s13054-017-1672-7
  27. Lilliam Ambroggio, Todd A. Florin, Samir S. Shah, Richard Ruddy, Larisa Yeomans, Julie Trexel, Kathleen A. Stringer. Emerging Biomarkers of Illness Severity: Urinary Metabolites Associated with Sepsis and Necrotizing Methicillin-Resistant Staphylococcus aureus Pneumonia. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy 2017, 37 (9) , 1033-1042. https://doi.org/10.1002/phar.1973
  28. David Antcliffe, Beatriz Jiménez, Kirill Veselkov, Elaine Holmes, Anthony C. Gordon. Metabolic Profiling in Patients with Pneumonia on Intensive Care. EBioMedicine 2017, 18 , 244-253. https://doi.org/10.1016/j.ebiom.2017.03.034
  29. Pouline van Oort, Sanne de Bruin, Hans Weda, Hugo Knobel, Marcus Schultz, Lieuwe Bos, . Exhaled Breath Metabolomics for the Diagnosis of Pneumonia in Intubated and Mechanically-Ventilated Intensive Care Unit (ICU)-Patients. International Journal of Molecular Sciences 2017, 18 (2) , 449. https://doi.org/10.3390/ijms18020449
  30. Hans J. Vogel, Mauricio Arias, James M. Aramini, Subrata Paul, Zhihong Liu, Hiroaki Ishida. Characterization of Antimicrobial and Host-Defense Peptides by NMR Spectroscopy. 2017,,, 1-25. https://doi.org/10.1007/978-3-319-28275-6_119-1
  31. Nikolaos Evangelatos, Pia Bauer, Matthias Reumann, Kapaettu Satyamoorthy, Hans Lehrach, Angela Brand. Metabolomics in Sepsis and Its Impact on Public Health. Public Health Genomics 2017, 20 (5) , 274-285. https://doi.org/10.1159/000486362
  32. Darryl J. Adamko, Erik Saude, Matthew Bear, Shana Regush, Joan L. Robinson. Urine metabolomic profiling of children with respiratory tract infections in the emergency department: a pilot study. BMC Infectious Diseases 2016, 16 (1) https://doi.org/10.1186/s12879-016-1709-6
  33. David Antcliffe, Anthony C. Gordon. Metabonomics and intensive care. Critical Care 2016, 20 (1) https://doi.org/10.1186/s13054-016-1222-8
  34. Mohamed I.F. Shariff, Jin U. Kim, Nimzing G. Ladep, Mary M.E. Crossey, Larry K. Koomson, Abigail Zabron, Helen Reeves, Matthew Cramp, Stephen Ryder, Shaun Greer, I. Jane Cox, Roger Williams, Elaine Holmes, Kathryn Nash, Simon D. Taylor-Robinson. Urinary Metabotyping of Hepatocellular Carcinoma in a UK Cohort Using Proton Nuclear Magnetic Resonance Spectroscopy. Journal of Clinical and Experimental Hepatology 2016, 6 (3) , 186-194. https://doi.org/10.1016/j.jceh.2016.03.003
  35. Silva Holtfreter, Julia Kolata, Sebastian Stentzel, Stephanie Bauerfeind, Frank Schmidt, Nandakumar Sundaramoorthy, Barbara Bröker. Omics Approaches for the Study of Adaptive Immunity to Staphylococcus aureus and the Selection of Vaccine Candidates. Proteomes 2016, 4 (1) , 11. https://doi.org/10.3390/proteomes4010011
  36. Kathleen A. Stringer, Ryan T. McKay, Alla Karnovsky, Bernadette Quémerais, Paige Lacy. Metabolomics and Its Application to Acute Lung Diseases. Frontiers in Immunology 2016, 7 https://doi.org/10.3389/fimmu.2016.00044
  37. D. Antcliffe, A. C. Gordon. Metabonomics and Intensive Care. 2016,,, 353-363. https://doi.org/10.1007/978-3-319-27349-5_28
  38. Melissa S. Webster, James S. Cooper, Edith Chow, Lee J. Hubble, Andrea Sosa-Pintos, Lech Wieczorek, Burkhard Raguse. Detection of bacterial metabolites for the discrimination of bacteria utilizing gold nanoparticle chemiresistor sensors. Sensors and Actuators B: Chemical 2015, 220 , 895-902. https://doi.org/10.1016/j.snb.2015.06.024
  39. Li-na Du, Tong Xie, Jian-ya Xu, An Kang, Liu-qing Di, Jin-jun Shan, Shou-chuan Wang. A metabolomics approach to studying the effects of Jinxin oral liquid on RSV-infected mice using UPLC/LTQ-Orbitrap mass spectrometry. Journal of Ethnopharmacology 2015, 174 , 25-36. https://doi.org/10.1016/j.jep.2015.07.040
  40. Aiping Zhou, Jinjing Ni, Zhihong Xu, Ying Wang, Haomin Zhang, Wenjuan Wu, Shuihua Lu, Petros C. Karakousis, Yu-Feng Yao. Metabolomics specificity of tuberculosis plasma revealed by 1H NMR spectroscopy. Tuberculosis 2015, 95 (3) , 294-302. https://doi.org/10.1016/j.tube.2015.02.038
  41. B. Fatemeh Nobakht M. Gh., Rasoul Aliannejad, Mostafa Rezaei-Tavirani, Salman Taheri, Afsaneh Arefi Oskouie. The metabolomics of airway diseases, including COPD, asthma and cystic fibrosis. Biomarkers 2015, 20 (1) , 5-16. https://doi.org/10.3109/1354750X.2014.983167
  42. Shih-Chin Cheng, Leo A.B. Joosten, Mihai G. Netea. The interplay between central metabolism and innate immune responses. Cytokine & Growth Factor Reviews 2014, 25 (6) , 707-713. https://doi.org/10.1016/j.cytogfr.2014.06.008
  43. Angelica Dessì, Barbara Liori, Pierluigi Caboni, Giovanni Corsello, Mario Giuffrè, Antonio Noto, Francesca Serraino, Mauro Stronati, Marco Zaffanello, Vassilios Fanos. Monitoring neonatal fungal infection with metabolomics. The Journal of Maternal-Fetal & Neonatal Medicine 2014, 27 (sup2) , 34-38. https://doi.org/10.3109/14767058.2014.954787
  44. Rosa Vázquez-Fresno, Rafael Llorach, Jelena Marinic, Sara Tulipani, Mar Garcia-Aloy, Irene Espinosa-Martos, Esther Jiménez, Juan Miguel Rodríguez, Cristina Andres-Lacueva. Urinary metabolomic fingerprinting after consumption of a probiotic strain in women with mastitis. Pharmacological Research 2014, 87 , 160-165. https://doi.org/10.1016/j.phrs.2014.05.010
  45. Sushma K. Cribbs, Youngja Park, David M. Guidot, Greg S. Martin, Lou Ann Brown, Jeffrey Lennox, Dean P. Jones. Metabolomics of Bronchoalveolar Lavage Differentiate Healthy HIV-1-Infected Subjects from Controls. AIDS Research and Human Retroviruses 2014, 30 (6) , 579-585. https://doi.org/10.1089/aid.2013.0198
  46. Craig H. Warden, Carolyn Slupsky, Stephen M. Griffey, Ahmed Bettaieb, Esther Min, Anh Le, Janis S. Fisler, Susan Hansen, Fawaz Haj, Judith S. Stern, . Brown Norway Chromosome 1 Congenic Reduces Symptoms of Renal Disease in Fatty Zucker Rats. PLoS ONE 2014, 9 (1) , e87770. https://doi.org/10.1371/journal.pone.0087770
  47. Paige Lacy, Ryan T. McKay, Michael Finkel, Alla Karnovsky, Scott Woehler, Michael J. Lewis, David Chang, Kathleen A. Stringer, . Signal Intensities Derived from Different NMR Probes and Parameters Contribute to Variations in Quantification of Metabolites. PLoS ONE 2014, 9 (1) , e85732. https://doi.org/10.1371/journal.pone.0085732
  48. Karl Burgess, Naomi Rankin, Stefan Weidt. Metabolomics. 2014,,, 181-205. https://doi.org/10.1016/B978-0-12-386882-4.00010-4
  49. Natalie J Serkova, Tessa Little. Metabolomics in infections (HIV). 2014,,, 182-191. https://doi.org/10.4155/ebo.13.614
  50. Zhangjian Jiang, Feng Liu, Eng Shi Ong, Sam Fong Yau Li. Metabolic profile associated with glucose and cholesterol lowering effects of berberine in Sprague–Dawley rats. Metabolomics 2012, 8 (6) , 1052-1068. https://doi.org/10.1007/s11306-012-0407-7
  51. Li-Feng Wang, Xiang-Jun Hu, Rui-Yun Peng, Shui-Ming Wang, Ya-Bing Gao, Ji Dong, Li Zhao, Xiang Li, Hong-Yan Zuo, Chang-Zhen Wang, Rong-Lian Gao, Zhen-Tao Su, Xin-Xing Feng. Application of 1H-NMR-based metabolomics for detecting injury induced by long-term microwave exposure in Wistar rats’ urine. Analytical and Bioanalytical Chemistry 2012, 404 (1) , 69-78. https://doi.org/10.1007/s00216-012-6115-3
  52. Reza Mirnezami, James M. Kinross, Panagiotis A. Vorkas, Robert Goldin, Elaine Holmes, Jeremy Nicholson, Ara Darzi. Implementation of Molecular Phenotyping Approaches in the Personalized Surgical Patient Journey. Annals of Surgery 2012, 255 (5) , 881-889. https://doi.org/10.1097/SLA.0b013e31823e3c43
  53. Thilo M. Fuchs, Wolfgang Eisenreich, Jürgen Heesemann, Werner Goebel. Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats. FEMS Microbiology Reviews 2012, 36 (2) , 435-462. https://doi.org/10.1111/j.1574-6976.2011.00301.x
  54. Betsy Foxman. Molecular Tools. 2012,,, 79-97. https://doi.org/10.1016/B978-0-12-374133-2.00006-X
  55. Elizabeth M.S. McNiven, J. Bruce German, Carolyn M. Slupsky. Analytical metabolomics: nutritional opportunities for personalized health. The Journal of Nutritional Biochemistry 2011, 22 (11) , 995-1002. https://doi.org/10.1016/j.jnutbio.2011.05.016
  56. Thomas J Marrie. Primary Care Management of Community-Acquired Pneumonia. 2011,,https://doi.org/10.2217/9781780840185
  57. Thomas J Marrie. Community-acquired pneumonia: a common illness that continues to evolve. 2011,,, 2-8. https://doi.org/10.2217/ebo.11.104
  58. Natalie J. Serkova, Theodore J. Standiford, Kathleen A. Stringer. The Emerging Field of Quantitative Blood Metabolomics for Biomarker Discovery in Critical Illnesses. American Journal of Respiratory and Critical Care Medicine 2011, 184 (6) , 647-655. https://doi.org/10.1164/rccm.201103-0474CI
  59. Viswanathan Lakshmanan, Kyu Y. Rhee, Johanna P. Daily. Metabolomics and malaria biology. Molecular and Biochemical Parasitology 2011, 175 (2) , 104-111. https://doi.org/10.1016/j.molbiopara.2010.09.008
  60. Sean C. Booth, Matthew L. Workentine, Aalim M. Weljie, Raymond J. Turner. Metabolomics and its application to studying metal toxicity. Metallomics 2011, 3 (11) , 1142. https://doi.org/10.1039/c1mt00070e
  61. Paige Lacy. Metabolomics of sepsis-induced acute lung injury: a new approach for biomarkers. American Journal of Physiology-Lung Cellular and Molecular Physiology 2011, 300 (1) , L1-L3. https://doi.org/10.1152/ajplung.00375.2010
  62. Matteo Sofia, Mauro Maniscalco, Guglielmo de Laurentiis, Debora Paris, Dominique Melck, Andrea Motta. Exploring Airway Diseases by NMR-Based Metabonomics: A Review of Application to Exhaled Breath Condensate. Journal of Biomedicine and Biotechnology 2011, 2011 , 1-7. https://doi.org/10.1155/2011/403260
  63. Carolyn M Slupsky. Nuclear magnetic resonance-based analysis of urine for the rapid etiological diagnosis of pneumonia. Expert Opinion on Medical Diagnostics 2011, 5 (1) , 63-73. https://doi.org/10.1517/17530059.2011.537653
  64. Carolyn M. Slupsky, Helen Steed, Tiffany H. Wells, Kelly Dabbs, Alexandra Schepansky, Valerie Capstick, Wylam Faught, Michael B. Sawyer. Urine Metabolite Analysis Offers Potential Early Diagnosis of Ovarian and Breast Cancers. Clinical Cancer Research 2010, 16 (23) , 5835-5841. https://doi.org/10.1158/1078-0432.CCR-10-1434
  65. Dimitris Argyropoulos, Daina Avizonis. Electronic Referencing in Quantitative NMR. 2010,,https://doi.org/10.1002/9780470034590.emrstm1168
  66. Evagelia C. Laiakis, Gerard A. J. Morris, Albert J. Fornace, Stephen R. C. Howie, . Metabolomic Analysis in Severe Childhood Pneumonia in The Gambia, West Africa: Findings from a Pilot Study. PLoS ONE 2010, 5 (9) , e12655. https://doi.org/10.1371/journal.pone.0012655
  67. Carolyn M Slupsky. NMR-based analysis of metabolites in urine provides rapid diagnosis and etiology of pneumonia. Biomarkers in Medicine 2010, 4 (2) , 195-197. https://doi.org/10.2217/bmm.10.11
  68. Geum-Sook Hwang, Ji-Young Yang, Do Hyun Ryu, Tae-Hwan Kwon. Metabolic profiling of kidney and urine in rats with lithium-induced nephrogenic diabetes insipidus by 1 H-NMR-based metabonomics. American Journal of Physiology-Renal Physiology 2010, 298 (2) , F461-F470. https://doi.org/10.1152/ajprenal.00389.2009
  69. Jun Han, L Caetano M Antunes, B Brett Finlay, Christoph H Borchers. Metabolomics: towards understanding host–microbe interactions. Future Microbiology 2010, 5 (2) , 153-161. https://doi.org/10.2217/fmb.09.132
  70. Angika Basant, Mayuri Rege, Shobhona Sharma, Haripalsingh M Sonawat. Alterations in urine, serum and brain metabolomic profiles exhibit sexual dimorphism during malaria disease progression. Malaria Journal 2010, 9 (1) , 110. https://doi.org/10.1186/1475-2875-9-110

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