{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T04:41:33Z","timestamp":1791261693686,"version":"4.1.0"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,7,20]],"date-time":"2023-07-20T00:00:00Z","timestamp":1689811200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,7,20]],"date-time":"2023-07-20T00:00:00Z","timestamp":1689811200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Patients with cystic fibrosis are predisposed to chronic respiratory tract infections caused by <jats:italic>Pseudomonas aeruginosa<\/jats:italic>. As the disease progresses, the microorganism diversifies into genotypically and phenotypically different strains which may coexist in the patient's airways for years. Adaptation of the microorganism to the airways of patients with cystic fibrosis probably occurs in response to the host's airway environment, the elements of the immune system and antibiotic therapy. Due to the chronic persistence of the microorganism in the airways, a comprehensive molecular analysis was conducted. The analysis included 120 strains isolated from 10 adult cystic fibrosis patients with chronic <jats:italic>P. aeruginosa<\/jats:italic> infection. The aim of the study was to analyze the molecular patterns of <jats:italic>P. aeruginosa<\/jats:italic> strains and to trace their transmission in the population of cystic fibrosis patients, as well as to study a relationship of the disease with specific phenotypic features. In the research, a genotypic analysis of <jats:italic>P. aeruginosa<\/jats:italic> was performed using pulsed-field gel electrophoresis. The results of a number of phenotypic features of the strains were added to the outcomes of the molecular studies. As a result, 28 different genotypes were distinguished. The study also showed cross-transmission of strains between patients. 3 transmissible clusters were identified, including IG1 and IG2 clusters with 9 strains of <jats:italic>P. aeruginosa<\/jats:italic> each, obtained from 2 patients and IG3 cluster with 6 strains of <jats:italic>P. aeruginosa<\/jats:italic> isolated from 3 patients. Moreover, it was found that in some patients, several unrelated strains of <jats:italic>P. aeruginosa<\/jats:italic> may transiently or permanently infect the respiratory tract. A comprehensive understanding of the <jats:italic>P. aeruginosa<\/jats:italic> adaptation may help to develop more effective antimicrobial therapies and to identify new targets for future drugs in order to prevent progression of the infection to chronic stages.<\/jats:p>","DOI":"10.1038\/s41598-023-39005-9","type":"journal-article","created":{"date-parts":[[2023,7,20]],"date-time":"2023-07-20T13:02:05Z","timestamp":1689858125000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Phenotypic and genotypic characteristics of Pseudomonas aeruginosa isolated from cystic fibrosis patients with chronic infections"],"prefix":"10.1038","volume":"13","author":[{"given":"Agnieszka","family":"Iwa\u0144ska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"El\u017cbieta Anna","family":"Trafny","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u0142","family":"Czopowicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ewa","family":"Augustynowicz-Kope\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,7,20]]},"reference":[{"key":"39005_CR1","unstructured":"Marshall, B. et al. Patient Registry Annual Data Report 2020. https:\/\/www.cff.org\/sites\/default\/files\/2021-11\/Patient-Registry-Annual-Data-Report.pdf (2021)."},{"key":"39005_CR2","doi-asserted-by":"publisher","unstructured":"Allen, P., Borick, J. & Borick, J. Acute and chronic infection management in CF. In Cystic Fibrosis in Primary Care (ed. Lewis, D.) 69\u201387 (Springer International Publishing, 2020) https:\/\/doi.org\/10.1007\/978-3-030-25909-9_8.","DOI":"10.1007\/978-3-030-25909-9_8"},{"key":"39005_CR3","doi-asserted-by":"publisher","first-page":"701","DOI":"10.1055\/s-0039-1697961","volume":"40","author":"C Castellani","year":"2019","unstructured":"Castellani, C. et al. Cystic fibrosis diagnosis in newborns, children, and adults. Semin. Respir. Crit. Care Med. 40, 701\u2013714 (2019).","journal-title":"Semin. Respir. Crit. Care Med."},{"key":"39005_CR4","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1038\/s41579-020-00477-5","volume":"19","author":"E Rossi","year":"2021","unstructured":"Rossi, E. et al. Pseudomonas aeruginosa adaptation and evolution in patients with cystic fibrosis. Nat. Rev. Microbiol. 19, 331\u2013342 (2021).","journal-title":"Nat. Rev. Microbiol."},{"key":"39005_CR5","volume-title":"Mukowiscydoza choroba wielouk\u0142adowa","author":"D Sands","year":"2018","unstructured":"Sands, D. Mukowiscydoza choroba wielouk\u0142adowa (Termedia, 2018)."},{"key":"39005_CR6","unstructured":"US CF Foundation. The Clinical and Functional TRanslation of CFTR (CFTR2). https:\/\/cftr2.org (2023)."},{"key":"39005_CR7","unstructured":"Kozierkiewicz, A. et al. Opieka nad chorymi na mukowiscydoz\u0119 w Polsce. https:\/\/ptwm.org.pl\/assets\/file\/501,raport_druk.pdf (2019)."},{"key":"39005_CR8","unstructured":"Mielus, M., Walicka-Serzysko, K. & Sands, D. Rozpoznawanie i leczenie mukowiscydozy. Podsumowanie wytycznych European Cystic Fibrosis Society 2018. Med. Prakt. (2019)."},{"key":"39005_CR9","doi-asserted-by":"publisher","first-page":"303","DOI":"10.3389\/fimmu.2020.00303","volume":"11","author":"CN Ratnatunga","year":"2020","unstructured":"Ratnatunga, C. N. et al. The rise of non-tuberculosis mycobacterial lung disease. Front. Immunol. 11, 303 (2020).","journal-title":"Front. Immunol."},{"key":"39005_CR10","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1016\/j.jcf.2014.12.007","volume":"14","author":"TJ Kidd","year":"2015","unstructured":"Kidd, T. J. et al. Pseudomonas aeruginosa genotypes acquired by children with cystic fibrosis by age 5-years. J. Cyst. Fibros. 14, 361\u2013369 (2015).","journal-title":"J. Cyst. Fibros."},{"key":"39005_CR11","doi-asserted-by":"publisher","first-page":"1567","DOI":"10.1164\/rccm.201606-1107CI","volume":"195","author":"SC Ranganathan","year":"2017","unstructured":"Ranganathan, S. C., Hall, G. L., Sly, P. D., Stick, S. M. & Douglas, T. A. Early lung disease in infants and preschool children with cystic fibrosis. What have we learned and what should we do about it?. Am. J. Respir. Crit. Care Med. 195, 1567\u20131575 (2017).","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"39005_CR12","doi-asserted-by":"publisher","first-page":"680","DOI":"10.3390\/pathogens3030680","volume":"3","author":"A Sousa","year":"2014","unstructured":"Sousa, A. & Pereira, M. Pseudomonas aeruginosa diversification during infection development in cystic fibrosis lungs\u2014A review. Pathogens 3, 680\u2013703 (2014).","journal-title":"Pathogens"},{"key":"39005_CR13","doi-asserted-by":"publisher","first-page":"1603","DOI":"10.1007\/s10096-011-1483-8","volume":"31","author":"A Burkett","year":"2012","unstructured":"Burkett, A. et al. Persistency of Pseudomonas aeruginosa in sputum cultures and clinical outcomes in adult patients with cystic fibrosis. Eur. J. Clin. Microbiol. Infect. Dis. 31, 1603\u20131610 (2012).","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"39005_CR14","doi-asserted-by":"publisher","first-page":"e50731","DOI":"10.1371\/journal.pone.0050731","volume":"7","author":"N Cramer","year":"2012","unstructured":"Cramer, N. et al. Molecular epidemiology of chronic Pseudomonas aeruginosa airway infections in cystic fibrosis. PLoS ONE 7, e50731 (2012).","journal-title":"PLoS ONE"},{"key":"39005_CR15","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1183\/09031936.00204411","volume":"40","author":"JL Fothergill","year":"2012","unstructured":"Fothergill, J. L., Walshaw, M. J. & Winstanley, C. Transmissible strains of Pseudomonas aeruginosa in cystic fibrosis lung infections. Eur. Respir. J. 40, 227\u2013238 (2012).","journal-title":"Eur. Respir. J."},{"key":"39005_CR16","doi-asserted-by":"publisher","first-page":"15460","DOI":"10.1038\/s41598-021-95034-2","volume":"11","author":"D Jarych","year":"2021","unstructured":"Jarych, D., Augustynowicz-Kopec, E., Iwanska, A., Parniewski, P. & Majchrzak, M. Molecular analysis of Pseudomonas aeruginosa strains isolated from cystic fibrosis patients. Sci. Rep. 11, 15460 (2021).","journal-title":"Sci. Rep."},{"key":"39005_CR17","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1183\/09031936.00060512","volume":"41","author":"TJ Kidd","year":"2013","unstructured":"Kidd, T. J. et al. Shared Pseudomonas aeruginosa genotypes are common in Australian cystic fibrosis centres. Eur. Respir. J. 41, 1091\u20131100 (2013).","journal-title":"Eur. Respir. J."},{"key":"39005_CR18","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/S2213-2600(19)30337-6","volume":"8","author":"SC Bell","year":"2020","unstructured":"Bell, S. C. et al. The future of cystic fibrosis care: A global perspective. Lancet Respir. Med. 8, 65\u2013124 (2020).","journal-title":"Lancet Respir. Med."},{"key":"39005_CR19","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.jcf.2020.10.008","volume":"20","author":"L Jackson","year":"2021","unstructured":"Jackson, L. & Waters, V. Factors influencing the acquisition and eradication of early Pseudomonas aeruginosa infection in cystic fibrosis. J. Cyst. Fibros. 20, 8\u201316 (2021).","journal-title":"J. Cyst. Fibros."},{"key":"39005_CR20","doi-asserted-by":"publisher","first-page":"42","DOI":"10.3390\/antibiotics10010042","volume":"10","author":"P Behzadi","year":"2021","unstructured":"Behzadi, P., Bar\u00e1th, Z. & Gajd\u00e1cs, M. It\u2019s not easy being green: A narrative review on the microbiology, virulence and therapeutic prospects of multidrug-resistant Pseudomonas aeruginosa. Antibiotics 10, 42 (2021).","journal-title":"Antibiotics"},{"key":"39005_CR21","doi-asserted-by":"publisher","first-page":"665759","DOI":"10.3389\/fcimb.2021.665759","volume":"11","author":"RF Langendonk","year":"2021","unstructured":"Langendonk, R. F., Neill, D. R. & Fothergill, J. L. The building blocks of antimicrobial resistance in Pseudomonas aeruginosa: Implications for current resistance-breaking therapies. Front. Cell. Infect. Microbiol. 11, 665759 (2021).","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"39005_CR22","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1111\/nyas.14596","volume":"1496","author":"LN Yaeger","year":"2021","unstructured":"Yaeger, L. N., Coles, V. E., Chan, D. C. K. & Burrows, L. L. How to kill Pseudomonas\u2014emerging therapies for a challenging pathogen. Ann. N. Y. Acad. Sci. 1496, 59\u201381 (2021).","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"39005_CR23","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1186\/s12866-016-0760-1","volume":"16","author":"C Cigana","year":"2016","unstructured":"Cigana, C. et al. Genotypic and phenotypic relatedness of Pseudomonas aeruginosa isolates among the major cystic fibrosis patient cohort in Italy. BMC Microbiol. 16, 142 (2016).","journal-title":"BMC Microbiol."},{"key":"39005_CR24","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1016\/j.jcf.2014.09.016","volume":"14","author":"E Johansson","year":"2015","unstructured":"Johansson, E., Welinder-Olsson, C., Gilljam, M., Pourcel, C. & Lindblad, A. Genotyping of Pseudomonas aeruginosa reveals high diversity, stability over time and good outcome of eradication. J. Cyst. Fibros. 14, 353\u2013360 (2015).","journal-title":"J. Cyst. Fibros."},{"key":"39005_CR25","doi-asserted-by":"publisher","first-page":"2214","DOI":"10.1128\/IAI.01282-06","volume":"75","author":"L Jelsbak","year":"2007","unstructured":"Jelsbak, L. et al. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients. Infect. Immun. 75, 2214\u20132224 (2007).","journal-title":"Infect. Immun."},{"key":"39005_CR26","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.jhin.2015.09.010","volume":"92","author":"L Kalferstova","year":"2016","unstructured":"Kalferstova, L., VilimovskaDedeckova, K., Antuskova, M., Melter, O. & Drevinek, P. How and why to monitor Pseudomonas aeruginosa infections in the long term at a cystic fibrosis centre. J. Hosp. Infect. 92, 54\u201360 (2016).","journal-title":"J. Hosp. Infect."},{"key":"39005_CR27","doi-asserted-by":"publisher","first-page":"827","DOI":"10.1513\/AnnalsATS.201801-007OC","volume":"15","author":"MA Middleton","year":"2018","unstructured":"Middleton, M. A. et al. Epidemiology of clonal Pseudomonas aeruginosa infection in a Canadian cystic fibrosis population. Ann. Am. Thorac. Soc. 15, 827\u2013836 (2018).","journal-title":"Ann. Am. Thorac. Soc."},{"key":"39005_CR28","doi-asserted-by":"publisher","first-page":"109829","DOI":"10.1016\/j.celrep.2021.109829","volume":"37","author":"CR Armbruster","year":"2021","unstructured":"Armbruster, C. R. et al. Adaptation and genomic erosion in fragmented Pseudomonas aeruginosa populations in the sinuses of people with cystic fibrosis. Cell Rep. 37, 109829 (2021).","journal-title":"Cell Rep."},{"key":"39005_CR29","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/j.tim.2016.01.008","volume":"24","author":"C Winstanley","year":"2016","unstructured":"Winstanley, C., O\u2019Brien, S. & Brockhurst, M. A. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol. 24, 327\u2013337 (2016).","journal-title":"Trends Microbiol."},{"key":"39005_CR30","doi-asserted-by":"publisher","first-page":"3128","DOI":"10.3390\/ijms22063128","volume":"22","author":"I Jurado-Mart\u00edn","year":"2021","unstructured":"Jurado-Mart\u00edn, I., Sainz-Mej\u00edas, M. & McClean, S. Pseudomonas aeruginosa: An audacious pathogen with an adaptable arsenal of virulence factors. Int. J. Mol. Sci. 22, 3128 (2021).","journal-title":"Int. J. Mol. Sci."},{"key":"39005_CR31","doi-asserted-by":"publisher","first-page":"1697","DOI":"10.1128\/JCM.02364-06","volume":"45","author":"P Tingpej","year":"2007","unstructured":"Tingpej, P. et al. Phenotypic characterization of clonal and nonclonal Pseudomonas aeruginosa strains isolated from lungs of adults with cystic fibrosis. J. Clin. Microbiol. 45, 1697\u20131704 (2007).","journal-title":"J. Clin. Microbiol."},{"key":"39005_CR32","doi-asserted-by":"publisher","first-page":"e0143466","DOI":"10.1371\/journal.pone.0143466","volume":"10","author":"J Duong","year":"2015","unstructured":"Duong, J. et al. Phenotypic and genotypic comparison of epidemic and non-epidemic strains of Pseudomonas aeruginosa from individuals with cystic fibrosis. PLoS ONE 10, e0143466 (2015).","journal-title":"PLoS ONE"},{"key":"39005_CR33","doi-asserted-by":"publisher","first-page":"4908","DOI":"10.1128\/JB.187.14.4908-4920.2005","volume":"187","author":"P Salunkhe","year":"2005","unstructured":"Salunkhe, P. et al. A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J. Bacteriol. 187, 4908\u20134920 (2005).","journal-title":"J. Bacteriol."},{"key":"39005_CR34","doi-asserted-by":"crossref","unstructured":"Hu, H. & Manos, J. Pulsed-Field Gel Electrophoresis of Pseudomonas aeruginosa. in vol. 1301, 157\u2013171 (2015).","DOI":"10.1007\/978-1-4939-2599-5_14"},{"key":"39005_CR35","doi-asserted-by":"publisher","first-page":"2233","DOI":"10.1128\/jcm.33.9.2233-2239.1995","volume":"33","author":"FC Tenover","year":"1995","unstructured":"Tenover, F. C. et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: Criteria for bacterial strain typing. J. Clin. Microbiol. 33, 2233\u20132239 (1995).","journal-title":"J. Clin. Microbiol."},{"key":"39005_CR36","doi-asserted-by":"publisher","first-page":"10932","DOI":"10.1038\/srep10932","volume":"5","author":"ST Clark","year":"2015","unstructured":"Clark, S. T. et al. Phenotypic diversity within a Pseudomonas aeruginosa population infecting an adult with cystic fibrosis. Sci. Rep. 5, 10932 (2015).","journal-title":"Sci. Rep."},{"key":"39005_CR37","unstructured":"Pseudomonas Methods and Protocols. (Humana Press, 2014)."},{"key":"39005_CR38","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/s13568-022-01344-7","volume":"12","author":"X Cheng","year":"2022","unstructured":"Cheng, X. et al. Spontaneous quorum-sensing hierarchy reprogramming in Pseudomonas aeruginosa laboratory strain PAO1. AMB Express 12, 6 (2022).","journal-title":"AMB Express"},{"key":"39005_CR39","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1590\/S1517-83822002000200012","volume":"33","author":"D Garcia","year":"2002","unstructured":"Garcia, D. et al. Proteases (caseinase and elastase), hemolysins, adhesion and susceptibility to antimicrobials of Stenotrophomonas maltophilia isolates obtained from clinical specimens. Braz. J. Microbiol. 33, 157\u2013162 (2002).","journal-title":"Braz. J. Microbiol."},{"key":"39005_CR40","first-page":"243","volume":"61","author":"A Kalici\u0144ska","year":"2009","unstructured":"Kalici\u0144ska, A. & Tyski, S. Analysis of Pseudomonas aeruginosa biofilm production in relation to cultivation media and biofilm staining methods. Med. Dosw. Mikrobiol. 61, 243\u2013252 (2009).","journal-title":"Med. Dosw. Mikrobiol."},{"key":"39005_CR41","doi-asserted-by":"publisher","first-page":"1635","DOI":"10.1007\/s11274-013-1326-0","volume":"29","author":"EA Trafny","year":"2013","unstructured":"Trafny, E. A., Lewandowski, R., Zawistowska-Marciniak, I. & St\u0119pi\u0144ska, M. Use of MTT assay for determination of the biofilm formation capacity of microorganisms in metalworking fluids. World J. Microbiol. Biotechnol. 29, 1635\u20131643 (2013).","journal-title":"World J. Microbiol. Biotechnol."},{"key":"39005_CR42","unstructured":"EUCAST, Breakpoint Tables for bacteria, Clinical breakpoints\u2014bacteria v 12.0. https:\/\/www.eucast.org\/fileadmin\/src\/media\/PDFs\/EUCAST_files\/Breakpoint_tables\/v_13.0_Breakpoint_Tables.pdf (2022)."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-39005-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-39005-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-39005-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,20]],"date-time":"2023-07-20T13:31:20Z","timestamp":1689859880000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-023-39005-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,20]]},"references-count":42,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["39005"],"URL":"https:\/\/doi.org\/10.1038\/s41598-023-39005-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,20]]},"assertion":[{"value":"31 March 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 July 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 July 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"11741"}}