{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T07:44:43Z","timestamp":1791531883274,"version":"4.3.4"},"reference-count":20,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T00:00:00Z","timestamp":1613952000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T00:00:00Z","timestamp":1613952000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Science and Technology Research Program of Chongqing Municipal Education Commission","award":["KJ1500235"],"award-info":[{"award-number":["KJ1500235"]}]},{"name":"Science and Technology Research Program of Chongqing Municipal Education Commission","award":["KJ1702022"],"award-info":[{"award-number":["KJ1702022"]}]},{"name":"Medical Research Program of Chongqing Health and Family Planning Commission","award":["2018MSXM009"],"award-info":[{"award-number":["2018MSXM009"]}]},{"DOI":"10.13039\/501100005230","name":"Natural Science Foundation of Chongqing","doi-asserted-by":"publisher","award":["cstc2020jcyj-msxmX0519"],"award-info":[{"award-number":["cstc2020jcyj-msxmX0519"]}],"id":[{"id":"10.13039\/501100005230","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Microbiol"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      Treatment options for\n                      <jats:italic>Stenotrophomonas maltophilia (S. maltophilia)<\/jats:italic>\n                      infections were limited. We assessed the efficacy of ceftazidime (CAZ), ceftazidime-avibactam (CAZ-AVI), aztreonam (ATM), and aztreonam-avibactam (ATM-AVI) against a selection of 76\u2009\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      out of the 1179 strains isolated from the First Affiliated Hospital of Chongqing Medical University during 2011\u20132018.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      We investigated the antimicrobial resistance profiles of the 1179\u2009\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      clinical isolates from the first affiliated hospital of Chongqing Medical University during 2011\u20132018, a collection of 76 isolates were selected for further study of microbiological characterization. Minimum inhibitory concentrations (MICs) of CAZ, CAZ-AVI, ATM and ATM-AVI were determined via the broth microdilution method. We deemed that CAZ-AVI or ATM-AVI was more active in vitro than CAZ or ATM alone when CAZ-AVI or ATM-AVI led to a category change from \u201cResistant\u201d or \u201cIntermediate\u201d with CAZ or ATM alone to \u201cSusceptible\u201d with CAZ-AVI or ATM-AVI, or if the MIC of CAZ-AVI or ATM-AVI was at least 4-fold lower than the MIC of CAZ or ATM alone.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      For the 76 clinical isolates included in the study, MICs of CAZ, ATM, CAZ-AVI and ATM-AVI ranged from 0.03\u201364, 1\u20131024, 0.016\u201364, and 0.06\u201364\u2009\u03bcg\/mL, respectively. In combined therapy, AVI was active at restoring the activity of 48.48% (16\/33) and 89.71% (61\/68) of\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      to CAZ and ATM, respectively. Furthermore, CAZ-AVI showed better results in terms of the proportion of susceptible isolates (77.63% vs. 56.58%,\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001), and MIC50 (2\u2009\u03bcg\/mL vs. 8\u2009\u03bcg\/mL,\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.05) when compared to CAZ. According to our definition, CAZ-AVI was more active in vitro than CAZ alone for 81.58% (62\/76) of the isolates. Similarly, ATM-AVI also showed better results in terms of the proportion of susceptible isolates (90.79% vs.10.53%,\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001) and MIC50 (2\u2009\u03bcg\/mL vs. 64\u2009\u03bcg\/mL,\n                      <jats:italic>P<\/jats:italic>\n                      \u2009&lt;\u20090.001) when compared to ATM. According to our definition, ATM-AVI was also more active in vitro than ATM alone for 94.74% (72\/76) of the isolates.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>\n                      AVI potentiated the activity of both CAZ and ATM against\n                      <jats:italic>S. maltophilia<\/jats:italic>\n                      clinical isolates in vitro. We demonstrated that CAZ-AVI and ATM-AVI are both useful therapeutic options to treat infections caused by\n                      <jats:italic>S. maltophilia.<\/jats:italic>\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s12866-021-02108-2","type":"journal-article","created":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T08:04:45Z","timestamp":1613981085000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":29,"title":["Avibactam potentiated the activity of both ceftazidime and aztreonam against S. maltophilia clinical isolates in vitro"],"prefix":"10.1186","volume":"21","author":[{"given":"Qiuxia","family":"Lin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Zou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xian","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Menglu","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Deyu","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanbing","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Siqiang","family":"Niu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7641-8823","authenticated-orcid":false,"given":"Shifeng","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,2,22]]},"reference":[{"key":"2108_CR1","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1128\/CMR.00019-11","volume":"25","author":"JS Brooke","year":"2012","unstructured":"Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev. 2012;25:2\u201341. https:\/\/doi.org\/10.1128\/CMR.00019-11.","journal-title":"Clin Microbiol Rev"},{"key":"2108_CR2","doi-asserted-by":"publisher","first-page":"893","DOI":"10.3389\/fmicb.2015.00893","volume":"6","author":"YT Chang","year":"2015","unstructured":"Chang YT, Lin CY, et al. Update on infections caused by Stenotrophomonas maltophilia with particular attention to resistance mechanisms and therapeutic options. Front Microbiol. 2015;6:893. https:\/\/doi.org\/10.3389\/fmicb.2015.00893.","journal-title":"Front Microbiol"},{"key":"2108_CR3","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1016\/S1473-3099(09)70083-0","volume":"9","author":"WJ Looney","year":"2009","unstructured":"Looney WJ, Narita M, et al. Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis. 2009;9:312\u201323. https:\/\/doi.org\/10.1016\/S1473-3099(09)70083-0.","journal-title":"Lancet Infect Dis"},{"key":"2108_CR4","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1007\/s10096-009-0709-5","volume":"28","author":"ME Falagas","year":"2009","unstructured":"Falagas ME, Kastoris AC, et al. Community-acquired Stenotrophomonas maltophilia infections: a systematic review. Eur J Clin Microbiol Infect Dis. 2009;28:719\u201330. https:\/\/doi.org\/10.1007\/s10096-009-0709-5.","journal-title":"Eur J Clin Microbiol Infect Dis"},{"issue":"12","key":"2108_CR5","first-page":"1170","volume":"91","author":"TN Jang","year":"1992","unstructured":"Jang TN, Wang FD, et al. Xanthomonas maltophilia bacteremia: an analysis of 32 cases. J Formos Med Assoc. 1992;91(12):1170\u20136.","journal-title":"J Formos Med Assoc"},{"issue":"3","key":"2108_CR6","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1017\/s0950268898008735","volume":"120","author":"PE Verweij","year":"1998","unstructured":"Verweij PE, Meis JF, et al. Nosocomial outbreak of colonization and infection with Stenotrophomonas maltophilia in preterm infants associated with contaminated tap water. Epidemiol Infect. 1998;120(3):251\u20136. https:\/\/doi.org\/10.1017\/s0950268898008735.","journal-title":"Epidemiol Infect"},{"key":"2108_CR7","unstructured":"World Health Organization. 2018. Public health importance of antimicrobial resistance. https:\/\/www.who.int\/drugresistance\/AMR_Importance\/en\/. Accessed 20 Feb 2020."},{"key":"2108_CR8","doi-asserted-by":"publisher","first-page":"R74","DOI":"10.1186\/gb-2008-9-4-r74","volume":"9","author":"LC Crossman","year":"2008","unstructured":"Crossman LC, Gould VC, et al. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol. 2008;9:R74. https:\/\/doi.org\/10.1186\/gb-2008-9-4-r74.","journal-title":"Genome Biol"},{"key":"2108_CR9","doi-asserted-by":"publisher","first-page":"1525","DOI":"10.1128\/AAC.01485-07","volume":"52","author":"A Okazaki","year":"2008","unstructured":"Okazaki A, Avison MB. Induction of L1 and L2 \u03b2-lactamase production in Stenotrophomonas maltophilia is dependent on an AmpR-type regulator. Antimicrob Agents Chemother. 2008;52:1525\u20138. https:\/\/doi.org\/10.1128\/AAC.01485-07.","journal-title":"Antimicrob Agents Chemother"},{"key":"2108_CR10","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1016\/j.ijantimicag.2014.01.007","volume":"43","author":"HS Sader","year":"2014","unstructured":"Sader HS, Farrell DJ, et al. Antimicrobial susceptibility of gram-negative organisms isolated from patients hospitalized with pneumonia in US and European hospitals: results from the SENTRY antimicrobial surveillance program, 2009\u20132012. Int J Antimicrob Agents. 2014;43:328\u201334. https:\/\/doi.org\/10.1016\/j.ijantimicag.2014.01.007.","journal-title":"Int J Antimicrob Agents"},{"issue":"10","key":"2108_CR11","doi-asserted-by":"publisher","first-page":"e00777","DOI":"10.1128\/AAC.00777-17","volume":"61","author":"MF Mojica","year":"2017","unstructured":"Mojica MF, Papp-Wallace KM, et al. Avibactam restores the susceptibility of aztreonam against clinical isolates of Stenotrophomonas maltophilia. Antimicrob Agents Chemother. 2017;61(10):e00777\u201317. https:\/\/doi.org\/10.1128\/AAC.00777-17.","journal-title":"Antimicrob Agents Chemother"},{"key":"2108_CR12","doi-asserted-by":"publisher","first-page":"5130","DOI":"10.1128\/AAC.00264-16","volume":"60","author":"MF Mojica","year":"2016","unstructured":"Mojica MF, Ouellette CP, et al. Successful treatment of bloodstream infection due to metallo-beta-lactamase-producing Stenotrophomonas maltophilia in a renal transplant patient. Antimicrob Agents Chemother. 2016;60:5130\u20134. https:\/\/doi.org\/10.1128\/AAC.00264-16.","journal-title":"Antimicrob Agents Chemother"},{"issue":"6","key":"2108_CR13","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1007\/s40265-017-0725-1","volume":"77","author":"D Wong","year":"2017","unstructured":"Wong D, van Duin D. Novel beta-lactamase inhibitors: unlocking their potential in therapy. Drugs. 2017;77(6):615\u201328. https:\/\/doi.org\/10.1007\/s40265-017-0725-1.","journal-title":"Drugs"},{"issue":"Suppl 7","key":"2108_CR14","doi-asserted-by":"publisher","first-page":"S565","DOI":"10.1093\/cid\/ciz830","volume":"69","author":"Y Doi","year":"2019","unstructured":"Doi Y. Treatment options for Carbapenem-resistant gram-negative bacterial infections. Clin Infect Dis. 2019;69(Suppl 7):S565. https:\/\/doi.org\/10.1093\/cid\/ciz830.","journal-title":"Clin Infect Dis"},{"key":"2108_CR15","doi-asserted-by":"publisher","unstructured":"Farfour E, Trochu E, et al. Trends in ceftazidime-avibactam activity against multidrug-resistant organisms recovered from respiratory samples of cystic fibrosis patients. Transpl Infect Dis:e12955\u2013018. https:\/\/doi.org\/10.1111\/tid.12955.","DOI":"10.1111\/tid.12955"},{"issue":"3","key":"2108_CR16","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/j.medmal.2020.01.003","volume":"50","author":"C Moriceau","year":"2020","unstructured":"Moriceau C, Eveillard M, et al. Stenotrophomonas maltophilia susceptibility to ceftazidime-avibactam combination versus ceftazidime alone. Med Mal Infect. 2020;50(3):305\u20137. https:\/\/doi.org\/10.1016\/j.medmal.2020.01.003.","journal-title":"Med Mal Infect"},{"issue":"1","key":"2108_CR17","doi-asserted-by":"publisher","first-page":"e01595","DOI":"10.1128\/AAC.01595-19","volume":"64","author":"LJ Caverly","year":"2019","unstructured":"Caverly LJ, Spilker T, et al. In vitro activities of \u03b2-lactam-\u03b2-lactamase inhibitor antimicrobial agents against cystic fibrosis respiratory pathogens. Antimicrob Agents Chemother. 2019;64(1):e01595\u201319. https:\/\/doi.org\/10.1128\/AAC.01595-19.","journal-title":"Antimicrob Agents Chemother"},{"key":"2108_CR18","doi-asserted-by":"publisher","first-page":"3017","DOI":"10.2147\/IDR.S219635","volume":"12","author":"H Zou","year":"2019","unstructured":"Zou H, Xiong SJ, et al. CP-CRE\/non-CP-CRE stratification and CRE resistance mechanism determination help in better managing CRE bacteremia using ceftazidime-avibactam and aztreonam-avibactam. Infect Drug Resist. 2019;12:3017\u201327. https:\/\/doi.org\/10.2147\/IDR.S219635.","journal-title":"Infect Drug Resist"},{"key":"2108_CR19","volume-title":"Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard M07, 11th ed","author":"Clinical and Laboratory Standards Institute (CLSI)","year":"2018","unstructured":"Clinical and Laboratory Standards Institute (CLSI). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard M07, 11th ed. Wayne: Clinical and Laboratory Standards Institute; 2018."},{"key":"2108_CR20","volume-title":"CLSI supplement M100 (ISBN 978\u20131\u201368440-032-4 [Print]; ISBN 978\u20131\u201368440-033-1 [Electronic])","author":"Clinical and Laboratory Standards Institute (CLSI)","year":"2019","unstructured":"Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. In: CLSI supplement M100 (ISBN 978\u20131\u201368440-032-4 [Print]; ISBN 978\u20131\u201368440-033-1 [Electronic]). 29th ed. Wayne: Clinical and Laboratory Standards Institute; 2019.","edition":"29"}],"container-title":["BMC Microbiology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-021-02108-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12866-021-02108-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12866-021-02108-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,22]],"date-time":"2021-02-22T08:06:30Z","timestamp":1613981190000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcmicrobiol.biomedcentral.com\/articles\/10.1186\/s12866-021-02108-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,22]]},"references-count":20,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["2108"],"URL":"https:\/\/doi.org\/10.1186\/s12866-021-02108-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-80713\/v1","asserted-by":"object"}]},"ISSN":["1471-2180"],"issn-type":[{"value":"1471-2180","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,22]]},"assertion":[{"value":"20 September 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 February 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 February 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The data and samples analyzed in the present study were obtained in accordance with the standards and approved by the Chongqing Medical University Institutional Review Board and Biomedical Ethics Committee. For this study, samples were collected at the microbiology laboratory of our hospital, with no contact with the patients. This study was retrospective and there was no patient identification performed during data collection. Therefore, the ethics committee determined that informed consent was not required.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"60"}}