{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T14:34:55Z","timestamp":1790433295359,"version":"4.1.0"},"reference-count":58,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T00:00:00Z","timestamp":1712707200000},"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. Microbiol."],"abstract":"<jats:p>Finding strategies for decolonizing gut carriers of multidrug-resistant <jats:italic>Escherichia coli<\/jats:italic> (MDR-<jats:italic>Ec<\/jats:italic>) is a public-health priority. In this context, novel approaches should be validated in preclinical <jats:italic>in vivo<\/jats:italic> gut colonization models before being translated to humans. However, the use of mice presents limitations. Here, we used for the first time <jats:italic>Zophobas morio<\/jats:italic> larvae to design a new model of intestinal colonization (28-days duration, T28). Three hyperepidemic MDR-<jats:italic>Ec<\/jats:italic> producing extended-spectrum \u03b2-lactamases (ESBLs) or carbapenemases were administered via contaminated food to larvae for the first 7\u2009days (T7): <jats:italic>Ec<\/jats:italic>-4901.28 (ST131, CTX-M-15), <jats:italic>Ec<\/jats:italic>-042 (ST410, OXA-181) and <jats:italic>Ec<\/jats:italic>-050 (ST167, NDM-5). Growth curve analyses showed that larvae became rapidly colonized with all strains (T7, ~10<jats:sup>6\u20137<\/jats:sup> CFU\/mL), but bacterial load remained high after the removal of contaminated food only in <jats:italic>Ec<\/jats:italic>-4901.28 and <jats:italic>Ec<\/jats:italic>-042 (T28, ~10<jats:sup>3\u20134<\/jats:sup> CFU\/mL). Moreover, larvae receiving a force-feeding treatment with <jats:italic>INTESTI bacteriophage<\/jats:italic> cocktail (on T7 and T10 via gauge needle) were decolonized by <jats:italic>Ec<\/jats:italic>-4901.28 (<jats:italic>INTESTI<\/jats:italic>-susceptible); however, <jats:italic>Ec<\/jats:italic>-042 and <jats:italic>Ec<\/jats:italic>-050 (<jats:italic>INTESTI<\/jats:italic>-resistant) did not. Initial microbiota (before administering contaminated food) was very rich of bacterial genera (e.g., <jats:italic>Lactococcus<\/jats:italic>, <jats:italic>Enterococcus, Spiroplasma<\/jats:italic>), but patterns were heterogeneous (Shannon diversity index: range 1.1\u20132.7) and diverse to each other (Bray\u2013Curtis dissimilarity index \u226530%). However, when larvae were challenged with the MDR-<jats:italic>Ec<\/jats:italic> with or without administering bacteriophages the microbiota showed a non-significant reduction of the diversity during the 28-day experiments. In conclusion, the <jats:italic>Z. morio<\/jats:italic> larvae model promises to be a feasible and high-throughput approach to study novel gut decolonization strategies for MDR-<jats:italic>Ec<\/jats:italic> reducing the number of subsequent confirmatory mammalian experiments.<\/jats:p>","DOI":"10.3389\/fmicb.2024.1381051","type":"journal-article","created":{"date-parts":[[2024,4,10]],"date-time":"2024-04-10T04:42:07Z","timestamp":1712724127000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":12,"title":["A new in vivo model of intestinal colonization using Zophobas morio larvae: testing hyperepidemic ESBL- and carbapenemase-producing Escherichia coli clones"],"prefix":"10.3389","volume":"15","author":[{"given":"Yasmine","family":"Eddoubaji","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Aldeia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edgar I.","family":"Campos-Madueno","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aline I.","family":"Moser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cindy","family":"Kundlacz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincent","family":"Perreten","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Markus","family":"Hilty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Endimiani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,4,10]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/s42523-019-0010-6","article-title":"The microbiome of the invertebrate model host Galleria mellonella is dominated by Enterococcus","volume":"1","author":"Allonsius","year":"2019","journal-title":"Anim. 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Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"4555","DOI":"10.1128\/AEM.66.10.4555-4558.2000","article-title":"Rapid and simple determination of the Escherichia coli phylogenetic group","volume":"66","author":"Clermont","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref13","volume-title":"Bacteriophages: Methods and protocols, vol 1. Isolation, characterization, and interactions","author":"Clockie","year":"2009"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"311","DOI":"10.3389\/fmicb.2019.00311","article-title":"Optimization and characterization of a galleria mellonella larval infection model for virulence studies and the evaluation of therapeutics against Streptococcus pneumoniae","volume":"10","author":"Cools","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"6686","DOI":"10.1038\/s41467-021-26963-9","article-title":"A standardized gnotobiotic mouse model harboring a minimal 15-member mouse gut microbiota recapitulates SOPF\/SPF phenotypes","volume":"12","author":"Darnaud","year":"2021","journal-title":"Nat. Commun."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"766","DOI":"10.1093\/jac\/dkz470","article-title":"Employees of Swiss veterinary clinics colonized with epidemic clones of carbapenemase-producing E. coli","volume":"75","author":"Endimiani","year":"2020","journal-title":"J. Antimicrob. 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Biol."},{"key":"ref20","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1186\/s40168-021-01137-3","article-title":"Gut microbiota regulation of P-glycoprotein in the intestinal epithelium in maintenance of homeostasis","volume":"9","author":"Foley","year":"2021","journal-title":"Microbiome"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1007\/s11095-016-2069-z","article-title":"Alternative animal and non-animal models for drug discovery and development: Bonus or burden?","volume":"34","author":"Freires","year":"2017","journal-title":"Pharm. Res."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"604","DOI":"10.3390\/insects11090604","article-title":"Evaluation of organic wastes as substrates for rearing Zophobas morio, Tenebrio molitor, and Acheta domesticus larvae as alternative feed supplements","volume":"11","author":"Harsanyi","year":"2020","journal-title":"Insects"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"967","DOI":"10.1093\/cid\/cis581","article-title":"Transmission dynamics of extended-spectrum \u03b2-lactamase-producing Enterobacteriaceae in the tertiary care hospital and the household setting","volume":"55","author":"Hilty","year":"2012","journal-title":"Clin. Infect. 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Biotechnol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"e0227621","DOI":"10.1128\/aem.02276-21","article-title":"In vitro demonstration of targeted phage therapy and competitive exclusion as a novel strategy for decolonization of extended-Spectrum-cephalosporin-resistant Escherichia coli","volume":"88","author":"Laird","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"key":"ref28","doi-asserted-by":"publisher","DOI":"10.3791\/59270-v","article-title":"A Galleria mellonella oral administration model to study commensal-induced innate immune responses","author":"Lange","year":"2019","journal-title":"J. Vis. Exp."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"162","DOI":"10.4292\/wjgpt.v8.i3.162","article-title":"Phage therapy: an alternative to antibiotics in the age of multi-drug resistance","volume":"8","author":"Lin","year":"2017","journal-title":"World J. Gastrointest. Pharmacol. Ther."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"dlab068","DOI":"10.1093\/jacamr\/dlab068","article-title":"Adverse clinical outcomes associated with infections by Enterobacterales producing ESBL (ESBL-E): a systematic review and meta-analysis","volume":"3","author":"Ling","year":"2021","journal-title":"JAC Antimicrob. Resist."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"2300209","DOI":"10.2807\/1560-7917.ES.2023.28.19.2300209","article-title":"Rapid cross-border emergence of NDM-5-producing Escherichia coli in the European Union\/European economic area, 2012 to June 2022","volume":"28","author":"Linkevicius","year":"2023","journal-title":"Euro Surveill."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"131006","DOI":"10.1016\/j.chemosphere.2021.131006","article-title":"Biodegradation of foam plastics by Zophobas atratus larvae (Coleoptera: Tenebrionidae) associated with changes of gut digestive enzymes activities and microbiome","volume":"282","author":"Luo","year":"2021","journal-title":"Chemosphere"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"e0229848","DOI":"10.1371\/journal.pone.0229848","article-title":"Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae","volume":"15","author":"Mason","year":"2020","journal-title":"PLoS One"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","article-title":"Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data","volume":"8","author":"Mcmurdie","year":"2013","journal-title":"PLoS One"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1038\/s41598-023-50823-9","article-title":"Bacteriophage-mediated decolonization of Klebsiella pneumoniae in a novel Galleria mellonella gut colonization model with Enterobacteriaceae","volume":"14","author":"Mirza","year":"2024","journal-title":"Sci. Rep."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1080\/19490976.2021.1927634","article-title":"Influence of pig farming on human gut microbiota: role of airborne microbial communities","volume":"13","author":"Moor","year":"2021","journal-title":"Gut Microbes"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.jgar.2022.08.014","article-title":"Genome stability during serial subculturing in hyperepidemic multidrug-resistant Klebsiella pneumoniae and Escherichia coli","volume":"31","author":"Moser","year":"2022","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.jgar.2021.10.012","article-title":"Repatriation of a patient with COVID-19 contributed to the importation of an emerging carbapenemase producer","volume":"27","author":"Moser","year":"2021","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"24","DOI":"10.2807\/1560-7917.ES.2019.24.39.1900071","article-title":"Shedding of OXA-181 carbapenemase-producing E. coli from companion animals after hospitalisation in Switzerland: an outbreak in 2018","author":"Nigg","year":"2019","journal-title":"Euro Surveill."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"e723","DOI":"10.1016\/j.chom.2022.03.002","article-title":"Dynamics of the normal gut microbiota: a longitudinal one-year population study in Sweden","volume":"30","author":"Olsson","year":"2022","journal-title":"Cell Host Microbe"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"1529","DOI":"10.1007\/s40265-019-01180-3","article-title":"Extended-Spectrum \u03b2-lactamase-producing Enterobacteriaceae: update on molecular epidemiology and treatment options","volume":"79","author":"Peirano","year":"2019","journal-title":"Drugs"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"2585","DOI":"10.1128\/AAC.00891-10","article-title":"Effect of antibiotic treatment on establishment and elimination of intestinal colonization by KPC-producing Klebsiella pneumoniae in mice","volume":"55","author":"Perez","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"104265","DOI":"10.1016\/j.meegid.2020.104265","article-title":"The evolutionary puzzle of Escherichia coli ST131","volume":"81","author":"Pitout","year":"2020","journal-title":"Infect. Genet. Evol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"e0133923","DOI":"10.1128\/aac.01339-23","article-title":"Escherichia coli sequence type 410 with carbapenemases: a paradigm shift within E. coli toward multidrug resistance","volume":"68","author":"Pitout","year":"2024","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"14","DOI":"10.3390\/microorganisms7010014","article-title":"What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases","volume":"7","author":"Rinninella","year":"2019","journal-title":"Microorganisms"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"e00337","DOI":"10.1128\/mSphere.00337-18","article-title":"Escherichia coli sequence type 410 is causing new international high-risk clones","volume":"3","author":"Roer","year":"2018","journal-title":"mSphere"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1093\/jisesa\/ieab014","article-title":"The Superworm, Zophobas morio (Coleoptera:Tenebrionidae): a 'Sleeping Giant' in nutrient sources","volume":"21","author":"Rumbos","year":"2021","journal-title":"J. Insect Sci."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1186\/s13756-020-00742-5","article-title":"Poor infection prevention and control standards are associated with environmental contamination with carbapenemase-producing Enterobacterales and other multidrug-resistant bacteria in Swiss companion animal clinics","volume":"9","author":"Schmidt","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"2249","DOI":"10.1093\/jac\/dkt208","article-title":"Extended-spectrum cephalosporin-resistant Escherichia coli in community, specialized outpatient clinic and hospital settings in Switzerland","volume":"68","author":"Seiffert","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1061","DOI":"10.3390\/antibiotics12061061","article-title":"Antimicrobial resistance and clonal lineages of Escherichia coli from food-producing animals","volume":"12","author":"Silva","year":"2023","journal-title":"Antibiotics (Basel)"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1556\/030.66.2019.001","article-title":"A powerful in vivo alternative model in scientific research: Galleria mellonella","volume":"66","author":"Singkum","year":"2019","journal-title":"Acta Microbiol. Immunol. Hung."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"3007","DOI":"10.1242\/jeb.147058","article-title":"Considering aspects of the 3Rs principles within experimental animal biology","volume":"220","author":"Sneddon","year":"2017","journal-title":"J. Exp. Biol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"6335","DOI":"10.1038\/s41598-021-85766-6","article-title":"The influence of antibiotics on transitory resistome during gut colonization with CTX-M-15 and OXA-162 producing K. pneumoniae ST15","volume":"11","author":"Stercz","year":"2021","journal-title":"Sci. Rep."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1258142","DOI":"10.3389\/fcimb.2023.1258142","article-title":"Differential expression of immunity-related genes in larval Manduca sexta tissues in response to gut and systemic infection","volume":"13","author":"Von Bredow","year":"2023","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"e00009","DOI":"10.1128\/mSystems.00009-15","article-title":"Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys","volume":"1","author":"Walters","year":"2016","journal-title":"mSystems"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"2296603","DOI":"10.1080\/19490976.2023.2296603","article-title":"Microbial collaborations and conflicts: unraveling interactions in the gut ecosystem","volume":"16","author":"Wang","year":"2024","journal-title":"Gut Microbes"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"2750","DOI":"10.3389\/fmicb.2019.02750","article-title":"Zebrafish and Galleria mellonella: models to identify the subsequent infection and evaluate the immunological differences in different Klebsiella pneumoniae intestinal colonization strains","volume":"10","author":"Zhang","year":"2019","journal-title":"Front. 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