{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T15:35:08Z","timestamp":1772120108270,"version":"3.50.1"},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2023,8,14]],"date-time":"2023-08-14T00:00:00Z","timestamp":1691971200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2023,8,14]],"date-time":"2023-08-14T00:00:00Z","timestamp":1691971200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Appl Genetics"],"published-print":{"date-parts":[[2023,9]]},"DOI":"10.1007\/s13353-023-00776-6","type":"journal-article","created":{"date-parts":[[2023,8,13]],"date-time":"2023-08-13T21:01:47Z","timestamp":1691960507000},"page":"591-597","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Relationship between antibiotic resistance with class 1 integron and SmeDEF efflux pump encoding genes in clinical isolates of Stenotrophomonas maltophilia"],"prefix":"10.1007","volume":"64","author":[{"given":"Soheila","family":"Bafandeh Zamanpour","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rasoul","family":"Yousefi Mashouf","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Himen","family":"Salimizand","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mohsen","family":"Nazari","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4577-4029","authenticated-orcid":false,"given":"Mohammad Yousef","family":"Alikhani","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6087-9147","authenticated-orcid":false,"given":"Safar","family":"Farajnia","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2023,8,14]]},"reference":[{"issue":"11","key":"776_CR1","doi-asserted-by":"publisher","first-page":"3079","DOI":"10.1128\/AAC.44.11.3079-3086.2000","volume":"44","author":"A Alonso","year":"2000","unstructured":"Alonso A, Martinez JL (2000) Cloning and characterization of SmeDEF, a novel multidrug efflux pump from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 44(11):3079\u20133086","journal-title":"Antimicrob Agents Chemother"},{"issue":"1","key":"776_CR2","doi-asserted-by":"publisher","first-page":"9582","DOI":"10.1038\/s41598-021-88977-z","volume":"11","author":"A Azimi","year":"2021","unstructured":"Azimi A et al (2021) Emergence of fluoroquinolone resistance and possible mechanisms in clinical isolates of Stenotrophomonas maltophilia from Iran. Sci Rep 11(1):9582","journal-title":"Sci Rep"},{"issue":"2","key":"776_CR3","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1128\/AAC.48.2.666-669.2004","volume":"48","author":"R Barbolla","year":"2004","unstructured":"Barbolla R et al (2004) Class 1 integrons increase trimethoprim-sulfamethoxazole MICs against epidemiologically unrelated Stenotrophomonas maltophilia isolates. Antimicrob Agents Chemother 48(2):666\u2013669","journal-title":"Antimicrob Agents Chemother"},{"key":"776_CR4","doi-asserted-by":"publisher","first-page":"100943","DOI":"10.1016\/j.nmni.2021.100943","volume":"44","author":"Z Baseri","year":"2021","unstructured":"Baseri Z et al (2021) Prevalence of resistance genes and antibiotic resistance profile among Stenotrophomonas maltophilia isolates from hospitalized patients in Iran. New Microbes New Infect 44:100943","journal-title":"New Microbes New Infect"},{"issue":"9","key":"776_CR5","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1007\/s10096-014-2101-3","volume":"33","author":"J Betts","year":"2014","unstructured":"Betts J et al (2014) Activity of colistin in combination with tigecycline or rifampicin against multidrug-resistant Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis 33(9):1565\u20131572","journal-title":"Eur J Clin Microbiol Infect Dis"},{"key":"776_CR6","doi-asserted-by":"publisher","unstructured":"Bostanghadiri N et al (2019) Characterization of phenotypic and genotypic diversity of Stenotrophomonas maltophilia strains isolated from selected hospitals in Iran. Front Microbiol 10:1191. https:\/\/doi.org\/10.3389\/fmicb.2019.0119110","DOI":"10.3389\/fmicb.2019.0119110"},{"issue":"2","key":"776_CR7","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1089\/mdr.2015.0228","volume":"23","author":"SY Chong","year":"2017","unstructured":"Chong SY et al (2017) Levofloxacin efflux and smeD in clinical isolates of Stenotrophomonas maltophilia. Microb Drug Resist 23(2):163\u2013168","journal-title":"Microb Drug Resist"},{"issue":"2","key":"776_CR8","doi-asserted-by":"publisher","first-page":"246","DOI":"10.3343\/alm.2015.35.2.246","volume":"35","author":"HS Chung","year":"2015","unstructured":"Chung HS et al (2015b) The sul1 gene in Stenotrophomonas maltophilia with high-level resistance to trimethoprim\/sulfamethoxazole. Ann Lab Med 35(2):246\u2013249","journal-title":"Ann Lab Med"},{"issue":"2","key":"776_CR9","doi-asserted-by":"publisher","first-page":"246","DOI":"10.3343\/alm.2015.35.2.246","volume":"35","author":"H-S Chung","year":"2015","unstructured":"Chung H-S et al (2015a) The sul1 gene in Stenotrophomonas maltophilia with high-level resistance to trimethoprim\/sulfamethoxazole. Ann Lab Med 35(2):246","journal-title":"Ann Lab Med"},{"issue":"4","key":"776_CR10","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 et al (2008) The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 9(4):R74","journal-title":"Genome Biol"},{"issue":"1","key":"776_CR11","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1128\/CMR.11.1.57","volume":"11","author":"M Denton","year":"1998","unstructured":"Denton M, Kerr KG (1998) Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev 11(1):57\u201380","journal-title":"Clin Microbiol Rev"},{"issue":"8","key":"776_CR12","first-page":"872","volume":"22","author":"HS Ebrahim-Saraie","year":"2019","unstructured":"Ebrahim-Saraie HS et al (2019) Prevalence of antibiotic resistance and integrons, sul and Smqnr genes in clinical isolates of Stenotrophomonas maltophilia from a tertiary care hospital in Southwest Iran. Iran J Basic Med Sci 22(8):872","journal-title":"Iran J Basic Med Sci"},{"key":"776_CR13","unstructured":"EUCAST (2015) The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, Version 5.0. http:\/\/www.eucast.org"},{"key":"776_CR14","unstructured":"Fu et al (2022) Characteristics and influencing factors for Stenotrophomonas maltophilia infection in a tertiary general hospital of Sanya City and drug resistance from 2016 to 2020. Chin J Nosocomiology 32(10):1464\u20131467"},{"issue":"3","key":"776_CR15","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1093\/jac\/dkp476","volume":"65","author":"N Gordon","year":"2010","unstructured":"Gordon N, Wareham D (2010) Novel variants of the Sm qnr family of quinolone resistance genes in clinical isolates of Stenotrophomonas maltophilia. J Antimicrob Chemother 65(3):483\u2013489","journal-title":"J Antimicrob Chemother"},{"issue":"6","key":"776_CR16","doi-asserted-by":"publisher","first-page":"1070","DOI":"10.1093\/jac\/dkl106","volume":"57","author":"VC Gould","year":"2006","unstructured":"Gould VC, Avison MB (2006) SmeDEF-mediated antimicrobial drug resistance in Stenotrophomonas maltophilia clinical isolates having defined phylogenetic relationships. J Antimicrob Chemother 57(6):1070\u20131076","journal-title":"J Antimicrob Chemother"},{"key":"776_CR17","doi-asserted-by":"crossref","unstructured":"Gozel MG, Celik C, Elaldi N (2015) Stenotrophomonas maltophilia infections in adults: primary bacteremia and pneumonia. Jundishapur J Microbiol 8(8):e23569","DOI":"10.5812\/jjm.2356"},{"issue":"3","key":"776_CR18","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ijantimicag.2010.10.025","volume":"37","author":"LF Hu","year":"2011","unstructured":"Hu LF et al (2011a) Stenotrophomonas maltophilia resistance to trimethoprim\/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37(3):230\u2013234","journal-title":"Int J Antimicrob Agents"},{"issue":"3","key":"776_CR19","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ijantimicag.2010.10.025","volume":"37","author":"L-F Hu","year":"2011","unstructured":"Hu L-F et al (2011b) Stenotrophomonas maltophilia resistance to trimethoprim\/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 37(3):230\u2013234","journal-title":"Int J Antimicrob Agents"},{"issue":"6","key":"776_CR20","doi-asserted-by":"publisher","first-page":"e0157693","DOI":"10.1371\/journal.pone.0157693","volume":"11","author":"L-F Hu","year":"2016","unstructured":"Hu L-F et al (2016) Increase in the prevalence of resistance determinants to trimethoprim\/sulfamethoxazole in clinical Stenotrophomonas maltophilia isolates in China. PloS One 11(6):e0157693","journal-title":"PloS One"},{"issue":"1","key":"776_CR21","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1089\/mdr.2014.0072","volume":"21","author":"Y-W Huang","year":"2015","unstructured":"Huang Y-W et al (2015) The contribution of class 1 integron to antimicrobial resistance in Stenotrophomonas maltophilia. Microb Drug Resist 21(1):90\u201396","journal-title":"Microb Drug Resist"},{"issue":"5","key":"776_CR22","doi-asserted-by":"publisher","first-page":"e02685","DOI":"10.1128\/AAC.02685-16","volume":"61","author":"Y-W Huang","year":"2017","unstructured":"Huang Y-W et al (2017) Overexpression of SmeDEF efflux pump decreases aminoglycoside resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 61(5):e02685\u2013e02616","journal-title":"Antimicrob Agents Chemother"},{"issue":"3","key":"776_CR23","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.4314\/ahs.v20i3.13","volume":"20","author":"N Ince","year":"2020","unstructured":"Ince N et al (2020) An evaluation of six-year Stenotrophomonas maltophilia infections in a university hospital. Afr Health Sci 20(3):1118\u20131123","journal-title":"Afr Health Sci"},{"key":"776_CR24","doi-asserted-by":"crossref","unstructured":"Insuwanno W, Kiratisin P, Jitmuang A (2020) Stenotrophomonas maltophilia infections: clinical characteristics and factors associated with mortality of hospitalized patients. Infect Drug Resist 13:1559\u20131566","DOI":"10.2147\/IDR.S253949"},{"issue":"3","key":"776_CR25","doi-asserted-by":"publisher","first-page":"254","DOI":"10.4103\/0974-777X.83531","volume":"3","author":"F Jamali","year":"2011","unstructured":"Jamali F et al (2011) Minimal inhibitory concentration of ceftazidime and co-trimoxazole for Stenotrophomonas maltophilia using E-test. J Glob Infect 3(3):254","journal-title":"J Glob Infect"},{"issue":"5","key":"776_CR26","doi-asserted-by":"publisher","first-page":"5177","DOI":"10.3390\/ijerph120505177","volume":"12","author":"W Jia","year":"2015","unstructured":"Jia W et al (2015) Resistance of Stenotrophomonas maltophilia to fluoroquinolones: prevalence in a university hospital and possible mechanisms. Int J Environ Res Public Health 12(5):5177\u20135195","journal-title":"Int J Environ Res Public Health"},{"issue":"4","key":"776_CR27","doi-asserted-by":"publisher","first-page":"1200","DOI":"10.1128\/AEM.03408-14","volume":"81","author":"X-M Kang","year":"2015","unstructured":"Kang X-M et al (2015) Genome-wide identification of genes necessary for biofilm formation by nosocomial pathogen Stenotrophomonas maltophilia reveals that orphan response regulator FsnR is a critical modulator. Appl Environ Microbiol 81(4):1200\u20131209","journal-title":"Appl Environ Microbiol"},{"issue":"2","key":"776_CR28","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1016\/j.ijantimicag.2009.09.015","volume":"35","author":"SJ Liaw","year":"2010","unstructured":"Liaw SJ, Lee YL, Hsueh PR (2010) Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 35(2):126\u2013130","journal-title":"Int J Antimicrob Agents"},{"issue":"5","key":"776_CR29","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, M\u00fchlemann K (2009a) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9(5):312\u2013323","journal-title":"Lancet Infect Dis"},{"issue":"5","key":"776_CR30","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, Muhlemann K (2009b) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9(5):312\u2013323","journal-title":"Lancet Infect Dis"},{"issue":"2","key":"776_CR31","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/S0167-7012(00)00174-3","volume":"42","author":"BC Millar","year":"2000","unstructured":"Millar BC et al (2000) A simple and sensitive method to extract bacterial, yeast and fungal DNA from blood culture material. J Microbiol Methods 42(2):139\u2013147","journal-title":"J Microbiol Methods"},{"issue":"4","key":"776_CR32","first-page":"470","volume":"13","author":"MH Namaei","year":"2021","unstructured":"Namaei MH et al (2021) High prevalence of multidrug-resistant non-fermentative Gram-negative bacilli harboring blaIMP-1 and blaVIM-1 metallo-beta-lactamase genes in Birjand, south-east Iran. Iran J Microbiol 13(4):470","journal-title":"Iran J Microbiol"},{"issue":"11","key":"776_CR33","doi-asserted-by":"publisher","first-page":"7117","DOI":"10.1128\/AAC.01723-15","volume":"59","author":"TR Pak","year":"2015","unstructured":"Pak TR et al (2015) Whole-genome sequencing identifies emergence of a quinolone resistance mutation in a case of Stenotrophomonas maltophilia bacteremia. Antimicrob Agents Chemother 59(11):7117\u20137120","journal-title":"Antimicrob Agents Chemother"},{"issue":"3","key":"776_CR34","doi-asserted-by":"publisher","first-page":"292","DOI":"10.3934\/microbiol.2022021","volume":"8","author":"M Papadimitriou-Olivgeris","year":"2022","unstructured":"Papadimitriou-Olivgeris M et al (2022) Clonal dissemination and resistance genes among Stenotrophomonas maltophilia in a Greek University Hospital during a four-year period. AIMS Microbiology 8(3):292","journal-title":"AIMS Microbiology"},{"key":"776_CR35","first-page":"29","volume":"M100","author":"C Performance","year":"2017","unstructured":"Performance C (2017) Standards for antimicrobial susceptibility testing. CLSI Supplement M100:29","journal-title":"CLSI Supplement"},{"issue":"5","key":"776_CR36","doi-asserted-by":"publisher","first-page":"1185","DOI":"10.1111\/j.1365-2672.2011.05120.x","volume":"111","author":"C Pinot","year":"2011","unstructured":"Pinot C et al (2011) Identification of Stenotrophomonas maltophilia strains isolated from environmental and clinical samples: a rapid and efficient procedure. J Appl Microbiol 111(5):1185\u20131193","journal-title":"J Appl Microbiol"},{"issue":"6","key":"776_CR37","doi-asserted-by":"publisher","first-page":"655","DOI":"10.2217\/fmb.09.45","volume":"4","author":"MB Sanchez","year":"2009","unstructured":"Sanchez MB, Hernandez A, Martinez JL (2009) Stenotrophomonas maltophilia drug resistance. Future Microbiol 4(6):655\u2013660","journal-title":"Future Microbiol"},{"key":"776_CR38","doi-asserted-by":"publisher","unstructured":"S\u00e1nchez MB et al (2016) Antimicrobial drug efflux pumps in Stenotrophomonas maltophilia. In: Xian-Zhi L (ed) Efflux-mediated antimicrobial resistance in bacteria, 1st edn. Springer, pp 401\u2013416. https:\/\/doi.org\/10.1007\/978-3-319-39658-3","DOI":"10.1007\/978-3-319-39658-3"},{"key":"776_CR39","doi-asserted-by":"publisher","unstructured":"Srivastava S et al (2022) Infection trends, susceptibility pattern, and treatment options for Stenotrophomonas maltophilia infections in trauma patients: a retrospective study. J Lab Physicians 15(1):106\u2013109. https:\/\/doi.org\/10.1055\/s-0042-1757413","DOI":"10.1055\/s-0042-1757413"},{"issue":"2","key":"776_CR40","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.diagmicrobio.2007.09.007","volume":"60","author":"C-K Tan","year":"2008","unstructured":"Tan C-K et al (2008) Extensively drug-resistant Stenotrophomonas maltophilia in a tertiary care hospital in Taiwan: microbiologic characteristics, clinical features, and outcomes. Diagn Microbiol Infect Dis 60(2):205\u2013210","journal-title":"Diagn Microbiol Infect Dis"},{"issue":"4","key":"776_CR41","doi-asserted-by":"publisher","first-page":"559","DOI":"10.3201\/eid1304.061378","volume":"13","author":"MA Toleman","year":"2007","unstructured":"Toleman MA et al (2007) Global emergence of trimethoprim\/sulfamethoxazole resistance in Stenotrophomonas maltophilia mediated by acquisition of sul genes. Emerg Infect Dis 13(4):559","journal-title":"Emerg Infect Dis"},{"key":"776_CR42","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.jgar.2017.09.015","volume":"12","author":"L Watson","year":"2018","unstructured":"Watson L et al (2018) Sulfamethoxazole\/trimethoprim versus fluoroquinolones for the treatment of Stenotrophomonas maltophilia bloodstream infections. J Glob Antimicrob Resist 12:104\u2013106","journal-title":"J Glob Antimicrob Resist"},{"issue":"12","key":"776_CR43","doi-asserted-by":"publisher","first-page":"3497","DOI":"10.1128\/AAC.45.12.3497-3503.2001","volume":"45","author":"L Zhang","year":"2001","unstructured":"Zhang L, Li XZ, Poole K (2001) SmeDEF multidrug efflux pump contributes to intrinsic multidrug resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 45(12):3497\u20133503","journal-title":"Antimicrob Agents Chemother"}],"container-title":["Journal of Applied Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s13353-023-00776-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s13353-023-00776-6\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s13353-023-00776-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,25]],"date-time":"2023-08-25T21:06:07Z","timestamp":1692997567000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s13353-023-00776-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,14]]},"references-count":43,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2023,9]]}},"alternative-id":["776"],"URL":"https:\/\/doi.org\/10.1007\/s13353-023-00776-6","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-2681762\/v1","asserted-by":"object"}]},"ISSN":["1234-1983","2190-3883"],"issn-type":[{"value":"1234-1983","type":"print"},{"value":"2190-3883","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,14]]},"assertion":[{"value":"14 March 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 July 2023","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 August 2023","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 August 2023","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Consent to participate was not applicable to this study because the isolates in the study were obtained from existing clinical collections routinely collected as part of tertiary hospital laboratory practices. Clinical strains of <i>S. maltophilia<\/i> were obtained with the permission of the head of the hospital laboratory.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The current study was approved by the research ethics committee of Hamadan University of Medical Sciences, Hamadan, Iran (ID: IR.UMSHA. REC.1396.918).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}