{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T15:08:55Z","timestamp":1788361735130,"version":"build-2803163510"},"reference-count":54,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2021,12,30]],"date-time":"2021-12-30T00:00:00Z","timestamp":1640822400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R61-DH105594l"],"award-info":[{"award-number":["R61-DH105594l"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01-AI103280"],"award-info":[{"award-number":["R01-AI103280"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R21-AI123808"],"award-info":[{"award-number":["R21-AI123808"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R21-AI1"],"award-info":[{"award-number":["R21-AI1"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Children\u2019s Hospital of Philadelphia Research Institute"},{"name":"Burroughs Welcome Fund"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,12,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Starkly highlighted by the current COVID-19 pandemic, infectious diseases continue to have an outsized impact on human health worldwide. Diagnostic testing for infection can be challenging due to resource limitations, time constraints, or shortcomings in the accuracy of existing diagnostics. Rapid, simple diagnostics are highly desirable. There is increasing interest in the development of diagnostics that use exhaled breath analysis as a convenient and safe diagnostic method, as breath sampling is noninvasive, secure, and easy to perform. Volatile organic compounds (VOCs) present in exhaled breath reflect the fingerprint of the underlying metabolic and biophysical processes during disease.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Content<\/jats:title>\n                  <jats:p>In this review, we overview the major biomarkers present in exhaled breath in infectious diseases. We outline the promising recent advances in breath-based diagnosis of respiratory infections, including those caused by influenza virus, SARS-CoV-2, Mycobacterium tuberculosis, Pseudomonas aeruginosa, and Aspergillus fumigatus. In addition, we review the current landscape of diagnosis of 2 other globally important infections: Helicobacter pylori gastrointestinal infection and malaria.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Summary<\/jats:title>\n                  <jats:p>Characteristic and reproducible breath VOCs are associated with several infectious diseases, suggesting breath analysis as a promising strategy for diagnostic development. Ongoing challenges include poor standardization of breath collection and analysis and lack of validation studies. Further research is required to expand the applicability of breath analysis to clinical settings.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/clinchem\/hvab218","type":"journal-article","created":{"date-parts":[[2021,10,6]],"date-time":"2021-10-06T04:17:23Z","timestamp":1633493843000},"page":"43-51","source":"Crossref","is-referenced-by-count":39,"title":["Breath Metabolites to Diagnose Infection"],"prefix":"10.1093","volume":"68","author":[{"given":"Amalia Z","family":"Berna","sequence":"first","affiliation":[{"name":"Department of Pediatrics, Children\u2019s Hospital of Philadelphia, Philadelphia, PA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8395-8537","authenticated-orcid":false,"given":"Audrey R","family":"Odom John","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, Children\u2019s Hospital of Philadelphia, Philadelphia, PA"},{"name":"Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,12,30]]},"reference":[{"key":"2021123022385425000_hvab218-B1","first-page":"371","article-title":"Hippocratic writings in the Middle Ages","volume":"18","author":"Kibre","year":"1945","journal-title":"Bull Hist Med"},{"key":"2021123022385425000_hvab218-B2","first-page":"164","article-title":"Antoine Laurent Lavoisier's contributions to medicine and public health","volume":"29","author":"Duveen","year":"1955","journal-title":"Bull Hist Med"},{"key":"2021123022385425000_hvab218-B3","doi-asserted-by":"crossref","first-page":"679","DOI":"10.2105\/AJPH.67.7.679","article-title":"Anstie's alcohol limit: Francis Edmund Anstie 1833-1874","volume":"67","author":"Baldwin","year":"1977","journal-title":"Am J Public Health"},{"key":"2021123022385425000_hvab218-B4","doi-asserted-by":"crossref","first-page":"2374","DOI":"10.1073\/pnas.68.10.2374","article-title":"Quantitative analysis of urine vapor and breath by gas-liquid partition chromatography","volume":"68","author":"Pauling","year":"1971","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021123022385425000_hvab218-B5","doi-asserted-by":"crossref","first-page":"1930","DOI":"10.1016\/S0140-6736(98)07552-7","article-title":"Volatile organic compounds in breath as markers of lung cancer: a cross-sectional study","volume":"353","author":"Phillips","year":"1999","journal-title":"Lancet"},{"key":"2021123022385425000_hvab218-B6","doi-asserted-by":"crossref","first-page":"014001","DOI":"10.1088\/1752-7155\/8\/1\/014001","article-title":"A review of the volatiles from the healthy human body","volume":"8","author":"de Lacy Costello","year":"2014","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B7","doi-asserted-by":"crossref","first-page":"e1003311","DOI":"10.1371\/journal.ppat.1003311","article-title":"Volatile metabolites of pathogens: a systematic review","volume":"9","author":"Bos","year":"2013","journal-title":"PLoS Pathog"},{"key":"2021123022385425000_hvab218-B8","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.jchromb.2012.05.038","article-title":"Bacterial volatile discovery using solid phase microextraction and comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry","volume":"901","author":"Bean","year":"2012","journal-title":"J Chromatogr B Analyt Technol Biomed Life Sci"},{"key":"2021123022385425000_hvab218-B9","first-page":"873","article-title":"Evaluation of 11 commercially available rapid influenza diagnostic tests\u2014United States, 2011-2012","volume":"61","year":"2012","journal-title":"MMWR Morb Mortal Wkly Rep"},{"key":"2021123022385425000_hvab218-B10","doi-asserted-by":"crossref","first-page":"18894","DOI":"10.1038\/s41598-019-55334-0","article-title":"Volatile scents of influenza A and S. pyogenes (co-)infected cells","volume":"9","author":"Traxler","year":"2019","journal-title":"Sci Rep"},{"key":"2021123022385425000_hvab218-B11","doi-asserted-by":"crossref","first-page":"026015","DOI":"10.1088\/1752-7163\/aa9eef","article-title":"Volatile fingerprinting of human respiratory viruses from cell culture","volume":"12","author":"Purcaro","year":"2018","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B12","doi-asserted-by":"crossref","first-page":"026001","DOI":"10.1088\/1752-7155\/4\/2\/026001","article-title":"Effect of influenza vaccination on oxidative stress products in breath","volume":"4","author":"Phillips","year":"2010","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B13","doi-asserted-by":"crossref","first-page":"037107","DOI":"10.1088\/1752-7155\/5\/3\/037107","article-title":"Effect of the influenza A (H1N1) live attenuated intranasal vaccine on nitric oxide (FE(NO)) and other volatiles in exhaled breath","volume":"5","author":"Mashir","year":"2011","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B14","doi-asserted-by":"crossref","first-page":"14857","DOI":"10.1038\/s41598-018-33061-2","article-title":"VOC breath profile in spontaneously breathing awake swine during influenza A infection","volume":"8","author":"Traxler","year":"2018","journal-title":"Sci Rep"},{"key":"2021123022385425000_hvab218-B15","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1001\/jama.2020.2648","article-title":"Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72\u202f314 cases from the Chinese Center for Disease Control and Prevention","volume":"323","author":"Wu","year":"2020","journal-title":"Jama"},{"key":"2021123022385425000_hvab218-B16","first-page":"100609","article-title":"Diagnosis of COVID-19 by analysis of breath with gas chromatography-ion mobility spectrometry\u2014a feasibility study","volume":"29","author":"Ruszkiewicz","year":"2020","journal-title":"EClin Med"},{"key":"2021123022385425000_hvab218-B17","doi-asserted-by":"crossref","first-page":"2596","DOI":"10.1021\/acsinfecdis.1c00248","article-title":"Reproducible breath metabolite changes in children with SARS-CoV-2 infection","volume":"7","author":"Berna","year":"2021","journal-title":"ACS Infect Dis"},{"key":"2021123022385425000_hvab218-B18","first-page":"103154","article-title":"Metabolomics of exhaled breath in critically ill COVID-19 patients: a pilot study","volume":"63","author":"Grassin-Delyle","year":"2021","journal-title":"EBio Med"},{"key":"2021123022385425000_hvab218-B19","doi-asserted-by":"crossref","first-page":"12125","DOI":"10.1021\/acsnano.0c05657","article-title":"Multiplexed nanomaterial-based sensor array for detection of COVID-19 in exhaled breath","volume":"14","author":"Shan","year":"2020","journal-title":"ACS Nano"},{"key":"2021123022385425000_hvab218-B20","article-title":"Ruling out SARS-CoV-2 infection using exhaled breath analysis by electronic nose in a public health setting","author":"de Vries","year":"2021.","journal-title":"medRxiv"},{"key":"2021123022385425000_hvab218-B21","year":"2020"},{"key":"2021123022385425000_hvab218-B22","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.tube.2006.03.004","article-title":"Volatile biomarkers of pulmonary tuberculosis in the breath","volume":"87","author":"Phillips","year":"2007","journal-title":"Tuberculosis (Edinb)"},{"key":"2021123022385425000_hvab218-B23","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.tube.2010.01.003","article-title":"Breath biomarkers of active pulmonary tuberculosis","volume":"90","author":"Phillips","year":"2010","journal-title":"Tuberculosis (Edinb)"},{"key":"2021123022385425000_hvab218-B24","doi-asserted-by":"crossref","first-page":"016005","DOI":"10.1088\/1752-7163\/aae80e","article-title":"Exhaled human breath analysis in active pulmonary tuberculosis diagnostics by comprehensive gas chromatography-mass spectrometry and chemometric techniques","volume":"13","author":"Beccaria","year":"2018","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B25","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.jchromb.2018.01.004","article-title":"Preliminary investigation of human exhaled breath for tuberculosis diagnosis by multidimensional gas chromatography\u2013time of flight mass spectrometry and machine learning","volume":"1074\u20131075","author":"Beccaria","year":"2018","journal-title":"J Chromatogr B Analyt Technol Biomed Life Sci"},{"key":"2021123022385425000_hvab218-B26","doi-asserted-by":"crossref","first-page":"2704","DOI":"10.1038\/s41598-021-80970-w","article-title":"Breath can discriminate tuberculosis from other lower respiratory illness in children","volume":"11","author":"Bobak","year":"2021","journal-title":"Sci Rep"},{"key":"2021123022385425000_hvab218-B27","doi-asserted-by":"crossref","first-page":"026008","DOI":"10.1088\/1752-7163\/aaa016","article-title":"Towards the use of breath for detecting mycobacterial infection: a case study in a murine model","volume":"12","author":"Franchina","year":"2018","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B28","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1152\/japplphysiol.00888.2016","article-title":"A new method to evaluate macaque health using exhaled breath: a case study of M. tuberculosis in a BSL-3 setting","volume":"122","author":"Mellors","year":"2017","journal-title":"J Appl Physiol (1985)"},{"key":"2021123022385425000_hvab218-B29","doi-asserted-by":"crossref","first-page":"016004","DOI":"10.1088\/1752-7163\/aacd18","article-title":"Identification of Mycobacterium tuberculosis using volatile biomarkers in culture and exhaled breath","volume":"13","author":"Mellors","year":"2018","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B30","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1186\/1471-2466-10-56","article-title":"2-Aminoacetophenone as a potential breath biomarker for Pseudomonas aeruginosa in the cystic fibrosis lung","volume":"10","author":"Scott-Thomas","year":"2010","journal-title":"BMC Pulm Med"},{"key":"2021123022385425000_hvab218-B31","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1128\/jcm.9.4.479-484.1979","article-title":"Use of 2-aminoacetophenone production in identification of Pseudomonas aeruginosa","volume":"9","author":"Cox","year":"1979","journal-title":"J Clin Microbiol"},{"key":"2021123022385425000_hvab218-B32","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1128\/jcm.12.4.521-526.1980","article-title":"Headspace analysis of volatile metabolites of Pseudomonas aeruginosa and related species by gas chromatography-mass spectrometry","volume":"12","author":"Labows","year":"1980","journal-title":"J Clin Microbiol"},{"key":"2021123022385425000_hvab218-B33","doi-asserted-by":"crossref","first-page":"046002","DOI":"10.1088\/1752-7155\/5\/4\/046002","article-title":"Potential sources of 2-aminoacetophenone to confound the Pseudomonas aeruginosa breath test, including analysis of a food challenge study","volume":"5","author":"Scott-Thomas","year":"2011","journal-title":"J Breath Res"},{"key":"2021123022385425000_hvab218-B34","doi-asserted-by":"crossref","first-page":"2459","DOI":"10.1002\/rcm.5146","article-title":"Quantification of methyl thiocyanate in the headspace of Pseudomonas aeruginosa cultures and in the breath of cystic fibrosis patients by selected ion flow tube mass spectrometry","volume":"25","author":"Shestivska","year":"2011","journal-title":"Rapid Commun Mass Spectrom"},{"key":"2021123022385425000_hvab218-B35","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/s12127-011-0077-6","article-title":"Detection of infectious agents in the airways by ion mobility spectrometry of exhaled breath","volume":"14","author":"Rabis","year":"2011","journal-title":"Int J Ion Mobil Spec"},{"key":"2021123022385425000_hvab218-B36","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1203\/PDR.0b013e3181df4ea0","article-title":"Metabolomics of volatile organic compounds in cystic fibrosis patients and controls","volume":"68","author":"Robroeks","year":"2010","journal-title":"Pediatr Res"},{"key":"2021123022385425000_hvab218-B37","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1080\/13693780701753800","article-title":"Investigation into the production of 2-pentylfuran by Aspergillus fumigatus and other respiratory pathogens in vitro and human breath samples","volume":"46","author":"Syhre","year":"2008","journal-title":"Med Mycol"},{"key":"2021123022385425000_hvab218-B38","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1080\/13693780802475212","article-title":"Detection of 2-pentylfuran in the breath of patients with Aspergillus fumigatus","volume":"47","author":"Chambers","year":"2009","journal-title":"Med Mycol"},{"key":"2021123022385425000_hvab218-B39","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1093\/cid\/ciu725","article-title":"A breath fungal secondary metabolite signature to diagnose invasive Aspergillosis","volume":"59","author":"Koo","year":"2014","journal-title":"Clin Infect Dis"},{"key":"2021123022385425000_hvab218-B40","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s11101-011-9216-2","article-title":"Volatile sesquiterpenes from fungi: what are they good for?","volume":"11","author":"Kramer","year":"2012","journal-title":"Phytochem Rev"},{"key":"2021123022385425000_hvab218-B41","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/B978-0-12-819967-1.00017-7","volume-title":"Breathborne biomarkers and the human volatilome.","author":"Modak","year":"2020","edition":"2nd Ed"},{"key":"2021123022385425000_hvab218-B42","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.3748\/wjg.v21.i4.1305","article-title":"Accuracy of urea breath test in Helicobacter pylori infection: meta-analysis","volume":"21","author":"Ferwana","year":"2015","journal-title":"World J Gastroenterol"},{"key":"2021123022385425000_hvab218-B43","doi-asserted-by":"crossref","first-page":"e027","DOI":"10.1097\/PG9.0000000000000027","article-title":"Overview of breath testing in clinical practice in North America","volume":"2","author":"Nichols","year":"2021","journal-title":"JPGN Rep"},{"key":"2021123022385425000_hvab218-B44","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.25008","article-title":"Modelling the drivers of the spread of Plasmodium falciparum hrp2 gene deletions in sub-Saharan Africa","volume":"6","author":"Watson","year":"2017","journal-title":"eLife"},{"key":"2021123022385425000_hvab218-B45","year":"2019"},{"key":"2021123022385425000_hvab218-B46","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1093\/infdis\/jix214","article-title":"Gametocytemia and attractiveness of Plasmodium falciparum-infected Kenyan children to Anopheles gambiae mosquitoes","volume":"216","author":"Busula","year":"2017","journal-title":"J Infect Dis"},{"key":"2021123022385425000_hvab218-B47","doi-asserted-by":"crossref","first-page":"e298","DOI":"10.1371\/journal.pbio.0030298","article-title":"Malaria infection increases attractiveness of humans to mosquitoes","volume":"3","author":"Lacroix","year":"2005","journal-title":"PLoS Biol"},{"key":"2021123022385425000_hvab218-B48","doi-asserted-by":"crossref","first-page":"e00235","DOI":"10.1128\/mBio.00235-15","article-title":"Malaria parasites produce volatile mosquito attractants","volume":"6","author":"Kelly","year":"2015","journal-title":"mBio"},{"key":"2021123022385425000_hvab218-B49","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1093\/infdis\/jiy072","article-title":"Breathprinting reveals malaria-associated biomarkers and mosquito attractants","volume":"217","author":"Schaber","year":"2018","journal-title":"J Infect Dis"},{"key":"2021123022385425000_hvab218-B50","doi-asserted-by":"crossref","first-page":"5780","DOI":"10.1073\/pnas.1801512115","article-title":"Volatile biomarkers of symptomatic and asymptomatic malaria infection in humans","volume":"115","author":"De Moraes","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021123022385425000_hvab218-B51","doi-asserted-by":"crossref","first-page":"E4209","DOI":"10.1073\/pnas.1721610115","article-title":"Plasmodium associated changes in human odor attract mosquitoes","volume":"115","author":"Robinson","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021123022385425000_hvab218-B52","doi-asserted-by":"crossref","first-page":"1120","DOI":"10.1093\/infdis\/jiv176","article-title":"Analysis of breath specimens for biomarkers of Plasmodium falciparum infection","volume":"212","author":"Berna","year":"2015","journal-title":"J Infect Dis"},{"key":"2021123022385425000_hvab218-B53","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1056\/NEJMsr2022263","article-title":"Rapid scaling up of COVID-19 diagnostic testing in the United States\u2014the NIH RADx Initiative","volume":"383","author":"Tromberg","year":"2020","journal-title":"N Engl J Med"},{"key":"2021123022385425000_hvab218-B54","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/BF03392234","article-title":"Tuberculosis detection by giant African pouched rats","volume":"34","author":"Poling","year":"2011","journal-title":"Behav Anal"}],"container-title":["Clinical Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/clinchem\/article-pdf\/68\/1\/43\/41987867\/hvab218.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/clinchem\/article-pdf\/68\/1\/43\/41987867\/hvab218.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,30]],"date-time":"2021-12-30T22:41:01Z","timestamp":1640904061000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/clinchem\/article\/68\/1\/43\/6490233"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,30]]},"references-count":54,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12,30]]},"published-print":{"date-parts":[[2021,12,30]]}},"URL":"https:\/\/doi.org\/10.1093\/clinchem\/hvab218","relation":{},"ISSN":["0009-9147","1530-8561"],"issn-type":[{"value":"0009-9147","type":"print"},{"value":"1530-8561","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,1,1]]},"published":{"date-parts":[[2021,12,30]]}}}