{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T19:21:11Z","timestamp":1792351271847,"version":"4.4.0"},"reference-count":50,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T00:00:00Z","timestamp":1700092800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>The colonization of the oral cavity by potentially pathogenic antimicrobial-resistant bacteria in adolescents and its consequences is very poorly understood. The present study focused on the occurrence of oral colonization by Gram-negative bacilli (GNB) and their multidrug resistance, including the production of extended-spectrum \u03b2-lactamases (ESBLs) and carbapenemases, among healthy adolescents and risk factors associated with GNB colonization.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Materials and methods<\/jats:title>\n                    <jats:p>\n                      This study was conducted as part of \u201cA program for the early detection of risk factors for lifestyle diseases SOPKARD-Junior\u201d (SOPKARD-Junior). Oral samples were collected from 182 adolescents from four public elementary schools in Sopot, Poland, aged 13-14 years. Bacterial strains were identified by the MALDI-TOF MS method. Screening of antimicrobial resistance was performed using a disk diffusion method. The NG-Test\n                      <jats:sup>\u00ae<\/jats:sup>\n                      CARBA-5 was used to detect and differentiate the five most widely distributed carbapenemases. Demographic and clinical data were collected and statistical analysis of risk factors was performed.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      A total of 68 out of 182 (37.4%) healthy adolescents was documented oral colonization with Gram-negative bacilli, including 50\/182 (27.5%) multidrug resistant (MDR-GNB) strains. Over 60% of oral carriage concerned three main genera\n                      <jats:italic>Enterobacter<\/jats:italic>\n                      spp.,\n                      <jats:italic>Pseudomonas<\/jats:italic>\n                      spp., and\n                      <jats:italic>Serratia<\/jats:italic>\n                      spp., which were detected in 22.1%, 19.1%, and 19.1% of participants, respectively.\n                      <jats:italic>Citrobacter<\/jats:italic>\n                      spp.,\n                      <jats:italic>Escherichia coli<\/jats:italic>\n                      ,\n                      <jats:italic>Klebsiella<\/jats:italic>\n                      spp.,\n                      <jats:italic>Hafnia<\/jats:italic>\n                      spp.,\n                      <jats:italic>Aeromonas<\/jats:italic>\n                      spp.,\n                      <jats:italic>Acinetobacter<\/jats:italic>\n                      spp., and\n                      <jats:italic>Stenotrophomonas<\/jats:italic>\n                      spp. were also isolated. The antimicrobial resistance to ampicillin (100%), ceftazidime (69.1%), meropenem (60.3%), gentamycin (60.3%), piperacillin\/tazobactam (52.9%), and piperacillin (45.6%) were the most common. Among 73.5% GNB strains multidrug resistance was observed, including all\n                      <jats:italic>Pseudomonas<\/jats:italic>\n                      spp. strains. Among MDR-GNB, 30.4% were resistant to four groups of antibiotics, half of the MDR\n                      <jats:italic>Pseudomonas<\/jats:italic>\n                      spp. strains were resistant to 10 groups of antibiotics. Extended-spectrum \u03b2-lactamases were produced by\n                      <jats:italic>Enterobacter cloacae<\/jats:italic>\n                      ,\n                      <jats:italic>Klebsiella<\/jats:italic>\n                      spp., and\n                      <jats:italic>Serratia<\/jats:italic>\n                      spp. (7.4%). Colonization by ESBLs-positive GNB strains was significantly associated with recurrent respiratory infections, nasal congestion, and bronchitis (p&amp;lt;0.05).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>Our study revealed high oral carriage of multi-drug resistant Gram-negative bacilli in healthy adolescents and the association of ESBL-producing strains with respiratory infections. Further studies on oral colonization with GNB are necessary due to the possibility of distinct infections and the acquisition of antibiotic resistance by resident microbiota.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fcimb.2023.1265777","type":"journal-article","created":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T09:02:22Z","timestamp":1700125342000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["High oral carriage of multidrug resistant Gram-negative bacilli in adolescents: the SOPKARD-Junior study"],"prefix":"10.3389","volume":"13","author":[{"given":"Marta","family":"Katkowska","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarzyna","family":"Garbacz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ewa","family":"Kwapisz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Klaudia","family":"Suligowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aida","family":"Kusiak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominika","family":"Cicho\u0144ska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dariusz","family":"\u015awietlik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,11,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"29","DOI":"10.12659\/msm.881750","article-title":"Nosocomial infections and risk factors in the intensive care unit of a teaching and research hospital: a prospective cohort study","volume":"17","author":"Ak","year":"2011","journal-title":"Med. Sci. Monit."},{"key":"B2","doi-asserted-by":"publisher","first-page":"49","DOI":"10.7508\/ibj.2016.01.007","article-title":"Particular distribution of Enterobacter cloacae strains isolated from urinary tract infection within clonal complexes","volume":"20","author":"Akbari","year":"2016","journal-title":"Iran BioMed. J."},{"key":"B3","doi-asserted-by":"publisher","first-page":"4653","DOI":"10.2147\/IDR.S283488","article-title":"Multidrug-resistant and extensively drug-resistant enterobacteriaceae: prevalence, treatments, and outcomes - A retrospective cohort study","volume":"24","author":"Alkofide","year":"2020","journal-title":"Infect. Drug Resist."},{"key":"B4","first-page":"2","article-title":"Prevalence and susceptibility of Enterobacteriaceae isolated from the saliva of students from the northeast of Brazil","volume":"16","author":"Arag\u00e3o","year":"2016","journal-title":"Glob. J. Med. Res"},{"key":"B5","doi-asserted-by":"publisher","first-page":"85","DOI":"10.3329\/bjm.v36i2.45533","article-title":"Isolation and identification of gram-negative bacteria from oral cancer site infections and study of their antibiotic resistance pattern","volume":"36","author":"Ashreen","year":"2020","journal-title":"Bangladesh J. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"908","DOI":"10.3201\/eid1806.110139","article-title":"Pretransplant fecal carriage of extend-ed-spectrum beta-lactamase-producing Enterobacteriaceae and infection after liver transplant, France","volume":"18","author":"Bert","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1968","DOI":"10.7860\/JCDR\/2013\/5506.3371","article-title":"Pattern of bacterial colonization of atopic dermatitis in Saudi children","volume":"7","author":"Bilal","year":"2013","journal-title":"J. Clin. Diagn. Res."},{"key":"B8","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1111\/j.1469-0691.2007.01851.x","article-title":"Animal reservoirs for extended spectrum beta-lactamase producers","volume":"14","author":"Carattoli","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1186\/2047-2994-1-39","article-title":"The gut is the epicentre of antibiotic resistance","volume":"1","author":"Carlet","year":"2012","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.4172\/2161-0703.1000128","article-title":"Musculoskeletal Postoperative Infections due to Enterobacter cloacae complex: A New Reality","volume":"3","author":"Ceroni","year":"2013","journal-title":"J. Med. Microbiol. Diagn."},{"key":"B11","doi-asserted-by":"publisher","first-page":"812","DOI":"10.1086\/423382","article-title":"Bloodstream infections caused by enterobacter species: predictors of 30-day mortality rate and impact of broad-spectrum cephalosporin resistance on outcome","volume":"39","author":"Cheol-In","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1908","DOI":"10.1080\/07853890.2022.2092895","article-title":"Oral health and the presence of infectious microorganisms in hospitalized patients: a preliminary observational study","volume":"54","author":"Cruz","year":"2022","journal-title":"Ann. Med."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/625170","article-title":"ESBLs: A clear and present danger","volume":"2012","author":"Dhillon","year":"2012","journal-title":"Crit. Care Res. Practice."},{"key":"B14","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1086\/422002","article-title":"The role of the intestinal tract as a reservoir and source for transmission of nosocomial pathogens","volume":"39","author":"Donskey","year":"2004","journal-title":"Clin. Infect. Dis."},{"key":"B15","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1590\/S1517-838220080002000011","article-title":"Occurrence of yeasts, enterococci and other enteric bacteria in subgingival biofilm of HIV-positive patients with chronic gingivitis and necrotizing periodontitis","volume":"39","author":"Gaetti-Jardim J\u00fanior","year":"2008","journal-title":"Braz. J. Microbiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1111\/j.1469-0691.2007.01855.x","article-title":"Prevalence and clonality of extended-spectrum beta-lactamases in Asia","volume":"14","author":"Hawkey","year":"2008","journal-title":"Clin. Microbiol. Infect."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3390\/antibiotics11111459","article-title":"Risk factors and outcomes for multidrug resistant pseudomonas aeruginosa infection in immunocompromised patients","volume":"11","author":"Hern\u00e1ndez-Jim\u00e9nez","year":"2022","journal-title":"Antibiotics"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.MBP-0013-2014","article-title":"Saliva as the sole nutritional source in the development of multispecies communities in dental plaque","volume":"3","author":"Jakubovics","year":"2015","journal-title":"Microbiol. Spectr."},{"key":"B19","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1093\/cid\/ciw283","article-title":"Fecal colonization with extended-spectrum beta-lactamase-producing enterobacteriaceae and risk factors among healthy individuals: A systematic review and metaanalysis","volume":"63","author":"Karanika","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"B20","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1097\/CCM.0000000000004783","article-title":"Nosocomial infection","volume":"49","author":"Kollef","year":"2021","journal-title":"Crit. Care Med."},{"key":"B21","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1016\/j.mcna.2018.12.008","article-title":"Community-acquired pneumonia and hospital acquired pneumonia","volume":"103","author":"Lanks","year":"2019","journal-title":"Med. Clin. N. Am."},{"key":"B22","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1186\/s13756-020-0705-1","article-title":"Oral colonisation by antimicrobial-resistant Gram-negative bacteria among long-term care facility residents: prevalence, risk factors, and molecular epidemiology","volume":"4","author":"Le","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"B23","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/s00253-022-12333-y","article-title":"Pseudomonadota in the oral cavity: a glimpse into the environment-human nexus","volume":"107","author":"Le\u00e3o","year":"2023","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1093\/clinids\/7.supplement_4.s656","article-title":"Pneumonia caused by gram-negative bacilli: an overview","volume":"7","author":"Levison","year":"1985","journal-title":"Rev. Infect. Dis."},{"key":"B25","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1128\/CMR.13.4.547","article-title":"Systemic diseases caused by oral infection","volume":"13","author":"Li","year":"2000","journal-title":"Clin. Microbiol. Rev."},{"key":"B26","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1590\/S1517-83822010000100005","article-title":"Nasopharyngeal Gram-Negative bacilli colonization in Brazilian children attending day-care centers","volume":"41","author":"Lima","year":"2010","journal-title":"Braz. J. Microbiol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1111\/prd.12098","article-title":"Influence of saliva on the oral microbiota","volume":"70","author":"Marsh","year":"2016","journal-title":"Periodontol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1007\/s11033-020-06114-x","article-title":"Prevalence of Enterobacteriaceae spp. and its multidrug-resistant rates in clinical isolates: A two-center cross-sectional study","volume":"48","author":"Mirzaei","year":"2021","journal-title":"Mol. Biol. Rep."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3390\/antibiotics11091218","article-title":"ESKAPE pathogens: looking at clp ATPases as potential drug targets","volume":"11","author":"Motiwala","year":"2022","journal-title":"Antibiotics"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.00539","article-title":"Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: A review","volume":"1","author":"Mulani","year":"2019","journal-title":"Front. Microbiol."},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.3390\/ijerph191710927","article-title":"Alarming levels of multidrug resistance in aerobic gram-negative bacilli isolated from the nasopharynx of healthy under-five children in Accra, Ghana","volume":"19","author":"Osei","year":"2022","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1478","DOI":"10.1099\/mic.0.024828-0","article-title":"Identification of resistance and virulence factors in an epidemic Enterobacter hormaechei outbreak strain","volume":"155","author":"Paauw","year":"2009","journal-title":"Microbiology"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1924","DOI":"10.15562\/bmj.v11i3.3811","article-title":"Bacterial colonization in atopic dermatitis","volume":"11","author":"Paramita","year":"2022","journal-title":"Bali Med. J."},{"key":"B34","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1053\/jhin.2000.0862","article-title":"An outbreak of hospital-acquired Klebsiella pneumoniae bacteraemia, including strains producing extended-spectrum beta-lactamase","volume":"47","author":"Pena","year":"2001","journal-title":"J. Hosp Infect."},{"key":"B35","doi-asserted-by":"publisher","first-page":"846","DOI":"10.1086\/521260","article-title":"Screening for extended-spectrum beta-lactamase-producing Enterobacteriaceae among high-risk patients and rates of subsequent bacteremia","volume":"45","author":"Reddy","year":"2007","journal-title":"Clin. Infect. Dis."},{"key":"B36","doi-asserted-by":"publisher","first-page":"146","DOI":"10.22038\/rcm.2020.44468.1296","article-title":"Clinical and pathogenesis overview of Enterobacter infections","volume":"6","author":"Salimiyan Rizi","year":"2019","journal-title":"Rev. Clin. Med."},{"key":"B37","doi-asserted-by":"publisher","first-page":"R117","DOI":"10.1186\/cc7967","article-title":"A randomized trial of chlorhexidine gluconate on oral bacterial pathogens in mechanically ventilated patients","volume":"13","author":"Scannapieco","year":"2009","journal-title":"Crit. Care"},{"key":"B38","doi-asserted-by":"publisher","first-page":"819","DOI":"10.2217\/fmb.15.16","article-title":"The complex epidemiology of extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae","volume":"10","author":"Tal Jasper","year":"2015","journal-title":"Future Microbiol."},{"key":"B39","unstructured":"2021"},{"key":"B40","unstructured":"2022"},{"key":"B41","volume-title":"Bailey and Scott\u2019s Diagnostic Microbiology","author":"Tille","year":"2013"},{"key":"B42","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1186\/s12879-022-07154-3","article-title":"Multi-body-site colonization screening cultures for predicting multi-drug resistant Gram-negative and Gram-positive bacteremia in hematological patients","volume":"22","author":"Torres","year":"2022","journal-title":"BMC Infect. Dis."},{"key":"B43","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1086\/502521","article-title":"Detection and treatment of antibiotic-resistant bacterial carriage in a surgical intensive care unit: a 6-year prospective survey","volume":"26","author":"Troche","year":"2005","journal-title":"Infect. Control Hosp Epidemiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1186\/s13756-018-0344-y","article-title":"Colonization sites in carriers of ESBL-producing Gram-negative bacteria","volume":"12","author":"van Prehn","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2023.1159798","article-title":"Revisiting ESKAPE Pathogens: virulence, resistance, and combating strategies focusing on quorum sensing","volume":"13","author":"Venkateswaran","year":"2023","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B46","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1001\/jama.1995.03530080055041","article-title":"The prevalence of nosocomial infection in intensive care units in Europe. Results of the European Prevalence of Infection in Intensive Care (EPIC) Study. EPIC International Advisory Committee","volume":"274","author":"Vincent","year":"1995","journal-title":"JAMA"},{"key":"B47","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1080\/02724939992383","article-title":"Striking differences in the nasopharyngeal flora of healthy Angolan, Brazilian and Dutch children less than 5 years old","volume":"19","author":"Wolf","year":"1999","journal-title":"Ann. Trop. Paediatr."},{"key":"B48","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/s1201-9712(01)90091-8","article-title":"Carriage of gram-negative bacilli in young Brazilian children with community-acquired pneumonia","volume":"5","author":"Wolf","year":"2001","journal-title":"Int. J. Infect. Dis."},{"key":"B49","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1186\/s13613-017-0296-z","article-title":"Emergence of antimicrobial resistance to Pseudomonas aeruginosa in the intensive care unit: Association with the duration of antibiotic exposure and mode of administration","volume":"7","author":"Yusuf","year":"2017","journal-title":"Ann. Intensive Care"},{"key":"B50","doi-asserted-by":"publisher","first-page":"2747","DOI":"10.1007\/s00203-021-02300-y","article-title":"Presence of non-oral bacteria in the oral cavity","volume":"203","author":"Zaatout","year":"2021","journal-title":"Arch. Microbiol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2023.1265777\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,16]],"date-time":"2023-11-16T09:02:27Z","timestamp":1700125347000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2023.1265777\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,16]]},"references-count":50,"alternative-id":["10.3389\/fcimb.2023.1265777"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2023.1265777","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,16]]},"article-number":"1265777"}}