{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:13:33Z","timestamp":1790799213341,"version":"4.1.0"},"reference-count":41,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T00:00:00Z","timestamp":1663200000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81872679"],"award-info":[{"award-number":["81872679"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100018625","name":"Science and Technology Innovation Plan Of Shanghai Science and Technology Commission","doi-asserted-by":"publisher","award":["21DZ2202400"],"award-info":[{"award-number":["21DZ2202400"]}],"id":[{"id":"10.13039\/501100018625","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Public Health"],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Fluoroquinolones (FQs) are the most important second-line anti-tuberculosis (anti-TB) drugs, primarily used for the treatment of multidrug- or rifampicin-resistant TB (MDR\/RR-TB). However, FQs are also commonly used to treat other bacterial infections. There are few published data on the rates of FQ resistance among rifampicin-susceptible TB.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We used whole-genome sequencing (WGS) to determine the prevalence of FQ resistance among rifampicin-susceptible TB in a rural district of Shanghai. This was a population-based retrospective study of all culture-positive pulmonary TB patients diagnosed in the Chongming district of Shanghai, China during 2009\u20132018.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>The rate of FQ resistance was 8.4% (29\/345) among TB, 6.2% (20\/324) among rifampicin-susceptible TB, and 42.9% (9\/21) among MDR\/RR-TB. Transmission of FQ-resistant strains was defined as strains differing within 12 single-nucleotide polymorphisms (SNPs) based on WGS. Among the rifampicin-susceptible TB, 20% (4\/20) of FQ resistance was caused by the transmission of FQ-resistant strains and 45% (9\/20) of FQ resistance was identified as hetero-resistance.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>The prevalence of FQ resistance in rifampicin-susceptible TB was higher than expected in Shanghai. Both the transmission and the selection of drug-resistant strains drive the emergence of FQ resistance in rifampicin-susceptible TB isolates. Therefore, the WGS-based surveillance system for TB should be urgently established and the clinical awareness of the rational use of FQs for respiratory infections should be enhanced to prevent the premature occurrence of FQ resistance.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fpubh.2022.990894","type":"journal-article","created":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T15:29:53Z","timestamp":1663255793000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Whole-genome sequencing for surveillance of fluoroquinolone resistance in rifampicin-susceptible tuberculosis in a rural district of Shanghai: A 10-year retrospective study"],"prefix":"10.3389","volume":"10","author":[{"given":"Yangyi","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenlei","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xuhui","family":"Shen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qichao","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Shen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,9,15]]},"reference":[{"key":"B1","volume-title":"WHO Consolidated Guidelines on Tuberculosis, Module 4: Treatment - Drug-Resistant Tuberculosis Treatment","year":"2020"},{"key":"B2","doi-asserted-by":"publisher","first-page":"1705","DOI":"10.1056\/NEJMoa2033400","article-title":"Four-month rifapentine regimens with or without moxifloxacin for tuberculosis","volume":"384","author":"Dorman","year":"2021","journal-title":"N Engl J Med."},{"key":"B3","volume-title":"Treatment of Drug-Susceptible Tuberculosis: Rapid Communication","year":"2021"},{"key":"B4","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.ijid.2014.03.1388","article-title":"Fluoroquinolone resistance in non-multidrug-resistant tuberculosis-a surveillance study in New South Wales, Australia, and a review of global resistance rates","volume":"26","author":"Ho","year":"2014","journal-title":"Int J Infect Dis."},{"key":"B5","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1186\/s13104-021-05832-0","article-title":"Fluoroquinolone Susceptibility in First-Line Drug-Susceptible M. Tuberculosis Isolates in Lima, Peru","volume":"14","author":"Schwalb","year":"2021","journal-title":"BMC Res Notes."},{"key":"B6","doi-asserted-by":"publisher","first-page":"S113","DOI":"10.1086\/428051","article-title":"The quinolones: past, present, and future","volume":"41","author":"Andriole","year":"2005","journal-title":"Clin Infect Dis."},{"key":"B7","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1136\/thx.2005.056887","article-title":"Empirical treatment with a fluoroquinolone delays the treatment for tuberculosis and is associated with a poor prognosis in endemic areas","volume":"61","author":"Wang","year":"2006","journal-title":"Thorax."},{"key":"B8","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1016\/j.tube.2011.03.001","article-title":"Population-based investigation of fluoroquinolones resistant tuberculosis in rural eastern China","volume":"91","author":"Hu","year":"2011","journal-title":"Tuberculosis (Edinb)."},{"key":"B9","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1038\/s41579-019-0214-5","article-title":"Whole genome sequencing of mycobacterium tuberculosis: current standards and open issues","volume":"17","author":"Meehan","year":"2019","journal-title":"Nat Rev Microbiol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1910","DOI":"10.1093\/cid\/ciaa496","article-title":"Resistance-conferring mutations on whole-genome sequencing of fluoroquinolone-resistant and -susceptible mycobacterium tuberculosis isolates: a proposed threshold for identifying resistance","volume":"72","author":"Maruri","year":"2021","journal-title":"Clin Infect Dis."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1364","DOI":"10.1093\/cid\/cix556","article-title":"Fluoroquinolone resistance mutation detection is equivalent to culture-based drug sensitivity testing for predicting multidrug-resistant tuberculosis treatment outcome: a retrospective cohort study","volume":"65","author":"Farhat","year":"2017","journal-title":"Clin Infect Dis."},{"key":"B12","doi-asserted-by":"publisher","first-page":"3270","DOI":"10.1128\/AAC.02066-13","article-title":"High Proportion of Heteroresistance in Gyra and Gyrb in Fluoroquinolone-Resistant Mycobacterium Tuberculosis Clinical Isolates","volume":"58","author":"Eilertson","year":"2014","journal-title":"Antimicrob Agents Chemother."},{"key":"B13","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1186\/s13073-019-0650-x","article-title":"Integrating informatics tools and portable sequencing technology for rapid detection of resistance to anti-tuberculous drugs","volume":"11","author":"Phelan","year":"2019","journal-title":"Genome Med."},{"key":"B14","doi-asserted-by":"publisher","first-page":"1193","DOI":"10.1016\/S1473-3099(15)00062-6","article-title":"Whole-genome sequencing for prediction of mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study","volume":"15","author":"Walker","year":"2015","journal-title":"Lancet Infect Dis."},{"key":"B15","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1186\/s13073-021-00953-4","article-title":"Gentb: a user-friendly genome-based predictor for tuberculosis resistance powered by machine learning","volume":"13","author":"Gr\u00f6schel","year":"2021","journal-title":"Genome Med."},{"key":"B16","doi-asserted-by":"publisher","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"Fastp: an ultra-fast all-in-one fastq preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics."},{"key":"B17","doi-asserted-by":"publisher","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","article-title":"Twelve Years of Samtools and Bcftools","volume":"10","author":"Danecek","year":"2021","journal-title":"GigaScience"},{"key":"B18","doi-asserted-by":"publisher","first-page":"e1002137","DOI":"10.1371\/journal.pmed.1002137","article-title":"Whole genome sequence analysis of a large isoniazid-resistant tuberculosis outbreak in london: a retrospective observational study","volume":"13","author":"Casali","year":"2016","journal-title":"PLoS Med."},{"key":"B19","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1016\/S1473-3099(16)30418-2","article-title":"Transmission of multidrug-resistant mycobacterium tuberculosis in Shanghai, China: a retrospective observational study using whole-genome sequencing and epidemiological investigation","volume":"17","author":"Yang","year":"2017","journal-title":"Lancet Infect Dis."},{"key":"B20","doi-asserted-by":"publisher","first-page":"4812","DOI":"10.1038\/ncomms5812","article-title":"A robust Snp barcode for typing mycobacterium tuberculosis complex strains","volume":"5","author":"Coll","year":"2014","journal-title":"Nat Commun."},{"key":"B21","doi-asserted-by":"publisher","first-page":"8136","DOI":"10.1073\/pnas.1424063112","article-title":"Southern East Asian origin and coexpansion of mycobacterium tuberculosis Beijing family with han Chinese","volume":"112","author":"Luo","year":"2015","journal-title":"Proc Natl Acad Sci U S A."},{"key":"B22","doi-asserted-by":"publisher","first-page":"4453","DOI":"10.1093\/bioinformatics\/btz305","article-title":"Raxml-Ng: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference","volume":"35","author":"Kozlov","year":"2019","journal-title":"Bioinformatics."},{"key":"B23","doi-asserted-by":"publisher","first-page":"2002272","DOI":"10.1183\/13993003.02272-2020","article-title":"Use of a whole genome sequencing-based approach for mycobacterium tuberculosis surveillance in Europe in 2017-2019: an ecdc pilot study","volume":"57","author":"Tagliani","year":"2021","journal-title":"Eur Respir J"},{"key":"B24","doi-asserted-by":"publisher","first-page":"1448","DOI":"10.1086\/379328","article-title":"Fluoroquinolone resistance in patients with newly diagnosed tuberculosis","volume":"37","author":"Ginsburg","year":"2003","journal-title":"Clin Infect Dis."},{"key":"B25","doi-asserted-by":"publisher","first-page":"45","DOI":"10.5152\/TurkThoracJ.2021.19128","article-title":"The relation between the emergence of fluoroquinolone resistance and fluoroquinolone exposure in new cases of active pulmonary tuberculosis","volume":"22","author":"Aydin Kayali","year":"2021","journal-title":"Turk Thorac J."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1723","DOI":"10.1093\/jac\/dkw013","article-title":"Trends and patterns of antibiotic consumption in shanghai municipality, China: a 6 year surveillance with sales records, 2009-14","volume":"71","author":"Lin","year":"2016","journal-title":"J Antimicrob Chemother."},{"key":"B27","doi-asserted-by":"publisher","first-page":"3857","DOI":"10.1128\/AAC.00102-13","article-title":"Prevalence and genetic characterization of second-line drug-resistant and extensively drug-resistant mycobacterium tuberculosis in rural China","volume":"57","author":"Hu","year":"2013","journal-title":"Antimicrob Agents Chemother."},{"key":"B28","doi-asserted-by":"publisher","first-page":"e19","DOI":"10.1038\/emi.2014.21","article-title":"Association of Gyra\/B mutations and resistance levels to fluoroquinolones in clinical isolates of mycobacterium tuberculosis","volume":"3","author":"Li","year":"2014","journal-title":"Emerg Microbes Infect."},{"key":"B29","doi-asserted-by":"publisher","first-page":"e0120470","DOI":"10.1371\/journal.pone.0120470","article-title":"Frequency and geographic distribution of gyra and gyrb mutations associated with fluoroquinolone resistance in clinical mycobacterium tuberculosis isolates: a systematic review","volume":"10","author":"Avalos","year":"2015","journal-title":"PLoS ONE."},{"key":"B30","doi-asserted-by":"publisher","first-page":"E839","DOI":"10.1073\/pnas.1525055113","article-title":"Fluoroquinolone Interactions with mycobacterium tuberculosis gyrase: enhancing drug activity against wild-type and resistant gyrase","volume":"113","author":"Aldred","year":"2016","journal-title":"Proc Natl Acad Sci U S A."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1093\/molbev\/msx052","article-title":"Mutation supply and relative fitness shape the genotypes of ciprofloxacin-resistant Escherichia Coli","volume":"34","author":"Huseby","year":"2017","journal-title":"Mol Biol Evol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1093\/molbev\/msz214","article-title":"The genetic background modulates the evolution of fluoroquinolone-resistance in mycobacterium tuberculosis","volume":"37","author":"Castro","year":"2020","journal-title":"Mol Biol Evol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.drup.2012.03.005","article-title":"Evolution of antibiotic resistance at non-lethal drug concentrations","volume":"15","author":"Andersson","year":"2012","journal-title":"Drug Resist Updat."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1164\/rccm.201711-2333OC","article-title":"Drug-penetration gradients associated with acquired drug resistance in patients with tuberculosis","volume":"198","author":"Dheda","year":"2018","journal-title":"Am J Respir Crit Care Med."},{"key":"B35","doi-asserted-by":"publisher","first-page":"e211","DOI":"10.1016\/j.ijid.2010.11.008","article-title":"Fluoroquinolones are associated with delayed treatment and resistance in tuberculosis: a systematic review and meta-analysis","volume":"15","author":"Chen","year":"2011","journal-title":"Int J Infect Dis."},{"key":"B36","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1183\/09031936.00036812","article-title":"Protecting the tuberculosis drug pipeline: stating the case for the rational use of fluoroquinolones","volume":"40","author":"Migliori","year":"2012","journal-title":"Eur Respir J."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1308","DOI":"10.1093\/cid\/civ076","article-title":"Us outpatient antibiotic prescribing variation according to geography, patient population, and provider specialty in 2011","volume":"60","author":"Hicks","year":"2015","journal-title":"Clin Infect Dis."},{"key":"B38","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1164\/rccm.200901-0146OC","article-title":"Fluoroquinolone resistance in mycobacterium tuberculosis: the effect of duration and timing of fluoroquinolone exposure","volume":"180","author":"Devasia","year":"2009","journal-title":"Am J Respir Crit Care Med."},{"key":"B39","doi-asserted-by":"publisher","first-page":"3977","DOI":"10.1128\/AAC.49.9.3977-3979.2005","article-title":"Emergence of fluoroquinolone resistance in mycobacterium tuberculosis during continuously dosed moxifloxacin monotherapy in a mouse model","volume":"49","author":"Ginsburg","year":"2005","journal-title":"Antimicrob Agents Chemother."},{"key":"B40","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1093\/cid\/civ255","article-title":"Transmission of mycobacterium tuberculosis in China: a population-based molecular epidemiologic study","volume":"61","author":"Yang","year":"2015","journal-title":"Clin Infect Dis."},{"key":"B41","doi-asserted-by":"publisher","first-page":"2334","DOI":"10.1016\/S0140-6736(15)00322-0","article-title":"Turning off the tap: stopping tuberculosis transmission through active case-finding and prompt effective treatment","volume":"386","author":"Yuen","year":"2015","journal-title":"Lancet."}],"container-title":["Frontiers in Public Health"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2022.990894\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,15]],"date-time":"2022-09-15T15:29:59Z","timestamp":1663255799000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpubh.2022.990894\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,15]]},"references-count":41,"alternative-id":["10.3389\/fpubh.2022.990894"],"URL":"https:\/\/doi.org\/10.3389\/fpubh.2022.990894","relation":{},"ISSN":["2296-2565"],"issn-type":[{"value":"2296-2565","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,15]]},"article-number":"990894"}}