Nutritional markers and proteome in patients undergoing treatment for pulmonary tuberculosis differ by geographic region
Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative...
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| Published in: | PloS one Vol. 16; no. 5; p. e0250586 |
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| Main Authors: | , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Public Library of Science
05.05.2021
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| ISSN: | 1932-6203, 1932-6203 |
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| Abstract | Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments.
We characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment).
After a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways.
We have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. |
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| AbstractList | Introduction Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments. Methods We characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment). Results After a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways. Conclusions We have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments. We characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment). After a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways. We have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. About the Authors: Leah G. Jarsberg Roles Data curation, Formal analysis, Writing – original draft, Writing – review & editing Affiliation: Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America ORCID logo https://orcid.org/0000-0001-6548-6337 Komal Kedia Roles Investigation, Methodology Affiliation: Department of Pharmacokinetics, Pharmacodynamics & Drug Metabolism (PPDM) Merck & Co., Inc., West Point, Pennsylvania, United States of America Jason Wendler Roles Data curation, Formal analysis Affiliation: Seattle Children’s Hospital, Seattle, Washington, United States of America ORCID logo https://orcid.org/0000-0003-4195-8138 Aaron T. Wright Roles Methodology Affiliations Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America, Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, United States of America Paul D. Piehowski Roles Investigation, Methodology Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Marina A. Gritsenko Roles Formal analysis, Investigation, Methodology, Writing – original draft Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Tujin Shi Roles Investigation, Methodology Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America David M. Lewinsohn Roles Conceptualization Affiliation: Pulmonary and Critical Care Medicine, Oregon Health & Science University, Portland, Oregon, United States of America George B. Sigal Roles Conceptualization, Resources Affiliation: Meso Scale Diagnostics, Rockville, Maryland, United States of America ORCID logo https://orcid.org/0000-0001-7149-6400 Marc H. Weiner Roles Conceptualization Affiliation: University of Texas Health Science Center at San Antonio and the South Texas VAMC, San Antonio, Texas, United States of America Richard D. Smith Roles Resources Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Joseph Keane Roles Methodology, Writing – review & editing Affiliation: Department of Clinical Medicine, Trinity Translational Medicine Institute, St. James’s Hospital, Dublin, Ireland Jon M. Jacobs Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing * E-mail: jon.jacobs@pnnl.gov Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America ORCID logo https://orcid.org/0000-0003-0557-7338 Payam Nahid Roles Conceptualization, Funding acquisition, Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing Affiliation: Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America ORCID logo https://orcid.org/0000-0003-2811-1311 Introduction Africa is home to 11% of the world’s population but carries 29% of the global burden of tuberculosis (TB) [1]. According to the World Health Organization (WHO), 84% of TB-related deaths worldwide occur in Africa [2]. Materials and methods Ethics statement Study 29 was approved by both CDC and local institutional review boards, and written informed consent was obtained from all study participants for collection of serum for TB-related research. Study population TBTC Study 29 (ClinicalTrials.gov Identifier NCT00694629) is a prospective, multicenter, open-label Phase 2 clinical trial comparing the antimicrobial activity and safety of a standard daily regimen containing rifampin, to that of an experimental regimen with daily rifapentine (10 mg/kg/dose), both given with isoniazid, pyrazinamide and ethambutol to adults with smear positive, culture-confirmed pulmonary TB. About the Authors: Leah G. Jarsberg Roles Data curation, Formal analysis, Writing – original draft, Writing – review & editing Affiliation: Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America ORCID logo https://orcid.org/0000-0001-6548-6337 Komal Kedia Roles Investigation, Methodology Affiliation: Department of Pharmacokinetics, Pharmacodynamics & Drug Metabolism (PPDM) Merck & Co., Inc., West Point, Pennsylvania, United States of America Jason Wendler Roles Data curation, Formal analysis Affiliation: Seattle Children’s Hospital, Seattle, Washington, United States of America ORCID logo https://orcid.org/0000-0003-4195-8138 Aaron T. Wright Roles Methodology Affiliations Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America, Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, United States of America Paul D. Piehowski Roles Investigation, Methodology Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Marina A. Gritsenko Roles Formal analysis, Investigation, Methodology, Writing – original draft Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Tujin Shi Roles Investigation, Methodology Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America David M. Lewinsohn Roles Conceptualization Affiliation: Pulmonary and Critical Care Medicine, Oregon Health & Science University, Portland, Oregon, United States of America George B. Sigal Roles Conceptualization, Resources Affiliation: Meso Scale Diagnostics, Rockville, Maryland, United States of America ORCID logo https://orcid.org/0000-0001-7149-6400 Marc H. Weiner Roles Conceptualization Affiliation: University of Texas Health Science Center at San Antonio and the South Texas VAMC, San Antonio, Texas, United States of America Richard D. Smith Roles Resources Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America Joseph Keane Roles Methodology, Writing – review & editing Affiliation: Department of Clinical Medicine, Trinity Translational Medicine Institute, St. James’s Hospital, Dublin, Ireland Jon M. Jacobs Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing * E-mail: jon.jacobs@pnnl.gov Affiliation: Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America ORCID logo https://orcid.org/0000-0003-0557-7338 Payam Nahid Roles Conceptualization, Funding acquisition, Investigation, Methodology, Resources, Writing – original draft, Writing – review & editing Affiliation: Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America ORCID logo https://orcid.org/0000-0003-2811-1311 Introduction Africa is home to 11% of the world’s population but carries 29% of the global burden of tuberculosis (TB) [1]. According to the World Health Organization (WHO), 84% of TB-related deaths worldwide occur in Africa [2]. Materials and methods Ethics statement Study 29 was approved by both CDC and local institutional review boards, and written informed consent was obtained from all study participants for collection of serum for TB-related research. Study population TBTC Study 29 (ClinicalTrials.gov Identifier NCT00694629) is a prospective, multicenter, open-label Phase 2 clinical trial comparing the antimicrobial activity and safety of a standard daily regimen containing rifampin, to that of an experimental regimen with daily rifapentine (10 mg/kg/dose), both given with isoniazid, pyrazinamide and ethambutol to adults with smear positive, culture-confirmed pulmonary TB. Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments. We characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment). After a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways. We have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments.INTRODUCTIONContemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments.We characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment).METHODSWe characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment).After a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways.RESULTSAfter a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways.We have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response.CONCLUSIONSWe have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. IntroductionContemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions, the reasons for which remain unclear. Understanding host and disease phenotypes that may vary by region is important for optimizing curative treatments.MethodsWe characterized clinical features and the serum proteome of phase 2 TB clinical trial participants undergoing treatment for smear positive, culture-confirmed TB, comparing host serum protein expression in clinical trial participants enrolled in African and Non-African regions. Serum samples were collected from 289 participants enrolled in the Centers for Disease Control and Prevention TBTC Study 29 (NCT00694629) at time of enrollment and at the end of the intensive phase (after 40 doses of TB treatment).ResultsAfter a peptide level proteome analysis utilizing a unique liquid chromatography IM-MS platform (LC-IM-MS) and subsequent statistical analysis, a total of 183 core proteins demonstrated significant differences at both baseline and at week 8 timepoints between participants enrolled from African and non-African regions. The majority of the differentially expressed proteins were upregulated in participants from the African region, and included acute phase proteins, mediators of inflammation, as well as coagulation and complement pathways. Downregulated proteins in the African population were primarily linked to nutritional status and lipid metabolism pathways.ConclusionsWe have identified differentially expressed nutrition and lipid pathway proteins by geographic region in TB patients undergoing treatment for pulmonary tuberculosis, which appear to be associated with differential treatment responses. Future TB clinical trials should collect expanded measures of nutritional status and further evaluate the relationship between nutrition and microbiologic treatment response. |
| Audience | Academic |
| Author | Gritsenko, Marina A. Keane, Joseph Kedia, Komal Lewinsohn, David M. Jacobs, Jon M. Piehowski, Paul D. Wright, Aaron T. Nahid, Payam Jarsberg, Leah G. Weiner, Marc H. Wendler, Jason Sigal, George B. Shi, Tujin Smith, Richard D. |
| AuthorAffiliation | 7 Meso Scale Diagnostics, Rockville, Maryland, United States of America 8 University of Texas Health Science Center at San Antonio and the South Texas VAMC, San Antonio, Texas, United States of America 1 Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America 3 Seattle Children’s Hospital, Seattle, Washington, United States of America 4 Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America 2 Department of Pharmacokinetics, Pharmacodynamics & Drug Metabolism (PPDM) Merck & Co., Inc., West Point, Pennsylvania, United States of America 5 Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, United States of America Rutgers Biomedical and Health Sciences, UNITED STATES 6 Pulmonary and Critical Care Medicine, Oregon Hea |
| AuthorAffiliation_xml | – name: 2 Department of Pharmacokinetics, Pharmacodynamics & Drug Metabolism (PPDM) Merck & Co., Inc., West Point, Pennsylvania, United States of America – name: 5 Voiland School of Chemical Engineering and Bioengineering, Washington State University, Pullman, Washington, United States of America – name: 8 University of Texas Health Science Center at San Antonio and the South Texas VAMC, San Antonio, Texas, United States of America – name: 6 Pulmonary and Critical Care Medicine, Oregon Health & Science University, Portland, Oregon, United States of America – name: 9 Department of Clinical Medicine, Trinity Translational Medicine Institute, St. James’s Hospital, Dublin, Ireland – name: 7 Meso Scale Diagnostics, Rockville, Maryland, United States of America – name: 3 Seattle Children’s Hospital, Seattle, Washington, United States of America – name: Rutgers Biomedical and Health Sciences, UNITED STATES – name: 1 Division of Pulmonary and Critical Care Medicine and UCSF Center for Tuberculosis, University of California San Francisco, San Francisco, California, United States of America – name: 4 Biological Sciences Division and Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, United States of America |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33951066$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1810101$$D View this record in Osti.gov |
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| CitedBy_id | crossref_primary_10_1038_s41598_023_35930_x crossref_primary_10_1371_journal_pone_0294603 crossref_primary_10_1371_journal_pone_0331721 crossref_primary_10_1002_pmic_13976 crossref_primary_10_1186_s10020_024_01052_x crossref_primary_10_3390_biomedicines10040783 crossref_primary_10_3390_pathogens14080824 |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2021 Public Library of Science 2021 Jarsberg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Jarsberg et al 2021 Jarsberg et al |
| Copyright_xml | – notice: COPYRIGHT 2021 Public Library of Science – notice: 2021 Jarsberg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2021 Jarsberg et al 2021 Jarsberg et al |
| CorporateAuthor | Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL) |
| CorporateAuthor_xml | – name: Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL) |
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| DOI | 10.1371/journal.pone.0250586 |
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| Snippet | Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus non-African regions,... Introduction Contemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus... About the Authors: Leah G. Jarsberg Roles Data curation, Formal analysis, Writing – original draft, Writing – review & editing Affiliation: Division of... IntroductionContemporary phase 2 TB disease treatment clinical trials have found that microbiologic treatment responses differ between African versus... |
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| SubjectTerms | Adult Analysis Antiinfectives and antibacterials Antimicrobial activity BASIC BIOLOGICAL SCIENCES Bioengineering Biology and Life Sciences Biomarkers Biomarkers - metabolism Blood proteins Care and treatment Chemical engineering Clinical medicine Clinical trials Critical care Data analysis Dosage Drug metabolism Editing Ethambutol Female Funding Humans Informed consent Isoniazid Laboratories Lipid Metabolism Male Medicine Medicine and Health Sciences Metabolism Methodology Middle Aged Mycobacterium tuberculosis - drug effects Mycobacterium tuberculosis - isolation & purification Mycobacterium tuberculosis - metabolism North America Nutrition Nutritional Physiological Phenomena People and Places Pharmacodynamics Pharmacokinetics Pharmacology Physical sciences Population studies Product/Service Evaluations Proteome - metabolism Proteomes Proteomics - methods Pulmonary tuberculosis Pyrazinamide Review boards Rifampin South Africa Spain Treatment Outcome Tuberculosis Tuberculosis, Pulmonary - drug therapy Tuberculosis, Pulmonary - metabolism Tuberculosis, Pulmonary - microbiology Uganda Young Adult |
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| Title | Nutritional markers and proteome in patients undergoing treatment for pulmonary tuberculosis differ by geographic region |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33951066 https://www.proquest.com/docview/2522383887 https://www.proquest.com/docview/2522615591 https://www.osti.gov/servlets/purl/1810101 https://pubmed.ncbi.nlm.nih.gov/PMC8099102 https://doaj.org/article/b9145d89909b47d4854d0bccdbebc6ef http://dx.doi.org/10.1371/journal.pone.0250586 |
| Volume | 16 |
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