{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,27]],"date-time":"2026-05-27T11:56:27Z","timestamp":1779882987198,"version":"3.53.1"},"reference-count":37,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2019,8,11]],"date-time":"2019-08-11T00:00:00Z","timestamp":1565481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Vitamin C has antimicrobial activity and is often used as an oral supplement accompanying antibiotic treatment in urinary tract infections (UTI). Proteus mirabilis is the third common species responsible for UTIs that are mostly treated with fluoroquinolones or aminoglycosides. Treatment of the UTI caused by P. mirabilis is problematic due to the ability to form biofilm on the urinary catheters. The aim of the study was to evaluate the influence of ascorbic acid in combination with antibiotics on P. mirabilis abilities to form biofilm. The susceptibility of P. mirabilis reference strain ATCC\u00ae 29906\u2122 and four clinical strains isolated from the urine samples of patients with urinary catheter were evaluated according to EUCAST recommendations. The influence of ascorbic acid (0.4 mg \u00d7 mL\u22121) in combination with antibiotics on biofilm formation was evaluated spectrophotometrically. Aminoglycosides at sub-inhibitory concentrations more successfully limited biofilm formation by P. mirabilis strains without ascorbic acid addition. Inhibition rate differences at the lowest concentrations of gentamicin and amikacin were statistically significant (p \u2264 0.05). Ascorbic acid addition to the culture medium limited the inhibitory effect of fluoroquinolones, facilitating biofilm formation by P. mirabilis strains. The addition of ascorbic acid during aminoglycosides therapy may disturb treatment of urinary tract infections related to the presence of P. mirabilis biofilm.<\/jats:p>","DOI":"10.3390\/antibiotics8030116","type":"journal-article","created":{"date-parts":[[2019,8,12]],"date-time":"2019-08-12T06:38:02Z","timestamp":1565591882000},"page":"116","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Vitamin C in the Presence of Sub-Inhibitory Concentration of Aminoglycosides and Fluoroquinolones Alters Proteus mirabilis Biofilm Inhibitory Rate"],"prefix":"10.3390","volume":"8","author":[{"given":"Joanna","family":"Kwieci\u0144ska-Pir\u00f3g","sequence":"first","affiliation":[{"name":"Department of Microbiology, Nicolaus Copernicus University in Toru\u0144, L. Rydygier Collegium Medicum in Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0868-864X","authenticated-orcid":false,"given":"Krzysztof","family":"Skowron","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Nicolaus Copernicus University in Toru\u0144, L. Rydygier Collegium Medicum in Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6787-1378","authenticated-orcid":false,"given":"Tomasz","family":"Bogiel","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Nicolaus Copernicus University in Toru\u0144, L. Rydygier Collegium Medicum in Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agata","family":"Bia\u0142ucha","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Nicolaus Copernicus University in Toru\u0144, L. Rydygier Collegium Medicum in Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jana","family":"Przekwas","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology, Antoni Jurasz University Hospital No. 1, Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eugenia","family":"Gospodarek-Komkowska","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Nicolaus Copernicus University in Toru\u0144, L. Rydygier Collegium Medicum in Bydgoszcz, 9 M. Sk\u0142odowska-Curie St., 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,8,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"89","DOI":"10.31989\/ffhd.v5i3.174","article-title":"Vitamin C: Optimal dosages, supplementation and use in disease prevention","volume":"5","author":"Pacier","year":"2015","journal-title":"FFHD"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1111\/odi.12446","article-title":"Vitamin C: The known and the unknown and Goldilocks","volume":"22","author":"Padayatty","year":"2016","journal-title":"Oral Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"198","DOI":"10.7762\/cnr.2017.6.3.198","article-title":"Effects of vitamin C supplementation on plasma and urinary vitamin C concentration in Korean women","volume":"6","author":"Choi","year":"2017","journal-title":"Clin. Nutr. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"319","DOI":"10.3177\/jnsv.51.319","article-title":"Values of water-soluble vitamins in blood and urine of Japanese young men and women consuming a semi-purified diet based on the Japanese Dietary Reference Intakes","volume":"51","author":"Shibata","year":"2005","journal-title":"J. Nutr. Sci. Vitaminol. (Tokyo)"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"477","DOI":"10.3389\/fphys.2018.00477","article-title":"Role of ROS and nutritional antioxidants in human diseases","volume":"9","author":"Liu","year":"2018","journal-title":"Front Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Hemil\u00e4, H. (2017). Vitamin C and infections. Nutrients, 9.","DOI":"10.3390\/nu9040339"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"88","DOI":"10.4103\/jcrsm.jcrsm_35_17","article-title":"Antimicrobial activity of vitamin C demonstrated on pathogenic Escherichia coli and Klebsiella pneumoniae","volume":"3","author":"Verghese","year":"2017","journal-title":"J. Curr. Res. Sci. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.jgar.2018.01.005","article-title":"Evaluation of synergistic antimicrobial effect of vitamins (A, B1, B2, B6, B12, C, D, E and K) with antibiotics against resistant bacterial strains","volume":"13","author":"Shahzad","year":"2018","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2352","DOI":"10.1128\/AAC.49.6.2352-2355.2005","article-title":"Intravesical nitric oxide delivery for prevention of catheter-associated urinary tract infections","volume":"49","author":"Carlsson","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_10","first-page":"1","article-title":"Efficacy of anti-microbial agents with ascorbic acid in catheter associated urinary tract infection","volume":"5","author":"Afzal","year":"2017","journal-title":"J. Infect. Dis. Prev. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1139\/w99-065","article-title":"The effect of water, ascorbic acid, and cranberry derived supplementation on human urine and uropathogen adhesion to silicone rubber","volume":"45","author":"Habash","year":"1999","journal-title":"Can. J. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1086\/501964","article-title":"The direct costs of nosocomial catheter-associated urinary tract infection in the era of managed care","volume":"23","author":"Tambyah","year":"2002","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.jhin.2006.12.013","article-title":"Prevalence of hospital infection and antibiotic use at a university medical center in Hong Kong","volume":"65","author":"Lee","year":"2007","journal-title":"J. Hosp. Infect."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1177\/1757177408098265","article-title":"The pathogenesis of catheter-associated urinary tract infection","volume":"10","author":"Barford","year":"2009","journal-title":"J. Infect. Prev."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1497","DOI":"10.1016\/S1286-4579(00)01304-6","article-title":"Pathogenesis of Proteus mirabilis urinary tract infection","volume":"2","author":"Coker","year":"2000","journal-title":"Microbes Infect."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.jmii.2011.11.007","article-title":"Proteus mirabilis urinary tract infection and bacteremia: Risk factors, clinical presentation, and outcomes","volume":"45","author":"Chen","year":"2012","journal-title":"J. Microbiol. Immunol. Infect."},{"key":"ref_17","unstructured":"(1996, October 18). National Center for Biotechnology Information, Available online: https:\/\/www.ncbi.nlm.nih.gov\/."},{"key":"ref_18","first-page":"204","article-title":"Proteus bacilli: Features and virulence factors","volume":"61","author":"Kwil","year":"2007","journal-title":"Post. Hig. Med. Do\u015bw."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1111\/j.1574-6968.2006.00587.x","article-title":"Structure of Proteus mirabilis biofilms grown in artificial urine and standard laboratory media","volume":"268","author":"Jones","year":"2007","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1002\/jbm.820241005","article-title":"The effect of protein and urine on uropathogen adhesion to polymer substrata","volume":"24","author":"Hawthorn","year":"1990","journal-title":"J. Biomed. Mater. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1078\/1438-4221-00196","article-title":"Mechanisms of antibiotic resistance in bacterial biofilms","volume":"292","author":"Stewart","year":"2002","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1046\/j.1464-410X.1997.00185.x","article-title":"Which indwelling urethral catheters resist encrustation by Proteus mirabilis biofilms?","volume":"80","author":"Morris","year":"1997","journal-title":"Br. J. Urol."},{"key":"ref_23","first-page":"5","article-title":"Biological Significance of Ascorbic Acid (Vitamin C) in Human Health\u2014A Review","volume":"3","author":"Iqbal","year":"2004","journal-title":"Pak. J. Nutr."},{"key":"ref_24","first-page":"131","article-title":"Effect of levofloxacin and vitamin C on bacterial adherence and preformed biofilm on urethral catheter surfaces","volume":"4","author":"Essam","year":"2012","journal-title":"J. MicrobBiochem. Technol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"76","DOI":"10.4103\/0255-0857.93044","article-title":"Antimicrobial activities against biofilm formed by Proteus mirabilis isolates from wound and urinary tract infections","volume":"30","author":"Wasfi","year":"2012","journal-title":"Indian J. Med. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1007\/s00284-012-0094-7","article-title":"Ciprofloxacin-induced antibacterial activity is reversed by vitamin E and vitamin C","volume":"64","author":"Masadeh","year":"2012","journal-title":"Curr. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/j.1574-6968.2011.02453.x","article-title":"Sublethal ciprofloxacin treatment leads to resistance via antioxidant systems in Proteus mirabilis","volume":"327","author":"Aiassa","year":"2012","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_28","first-page":"107","article-title":"The pharmacokinetic and biopharmaceutical effect of ascorbic acid (vitamin C) on pefloxacin on concurrent administration in human","volume":"2","author":"Awofisayo","year":"2012","journal-title":"J. Appl. Pharm. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2599","DOI":"10.3389\/fmicb.2017.02599","article-title":"Low concentration of vitamin C reduce the synthesis of extracellular polymers and destabilize bacterial biofilms","volume":"8","author":"Pandit","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_30","unstructured":"Yassein, M.A.M. (2019, August 10). Studies on the Prevention of Adherence of Biofilm Associated Bacteria to Human Cells and Implanted Medical Devices. Available online: https:\/\/dsr.kau.edu.sa\/Show_Res.aspx?Site_ID=305&LNG=EN&RN=53934."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1111\/j.1365-2621.2004.tb13374.x","article-title":"Evaluation of ascorbic acid as a quorum-sensing analogue to control growth, sporulation, and enterotoxin production in Clostridium perfringens","volume":"69","author":"Novak","year":"2004","journal-title":"J. Food Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1590\/S1516-89132005000300007","article-title":"Synergic interaction between ascorbic acid and antibiotics against Pseudomnas aeruginosa","volume":"48","author":"Cursino","year":"2005","journal-title":"Braz. Arch. Biol. Technol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1128\/AAC.00779-06","article-title":"Effects of glutathione and ascorbic acid on streptomycin sensitivity of Escherichia coli","volume":"51","author":"Goswami","year":"2007","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1016\/j.biopha.2014.10.011","article-title":"Enhancement of the antibiotic activity of aminoglycosides by alpha-tocopherol and other cholesterol derivates","volume":"68","author":"Andrade","year":"2014","journal-title":"Biomed. Pharmacother."},{"key":"ref_35","unstructured":"European Committee on Antimicrobial Susceptibility Testing (2018, September 03). Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 8.0. Available online: http:\/\/www.eucast.org."},{"key":"ref_36","unstructured":"(2001, November 30). Clinical Laboratory Standards Institute. Available online: https:\/\/clsi.org\/."},{"key":"ref_37","first-page":"930876","article-title":"The assessment of Proteus mirabilis susceptibility to ceftazidime and ciprofloxacin and the impact of these antibiotics at subinhibitory concentrations on Proteus mirabilis biofilms","volume":"2013","author":"Skowron","year":"2013","journal-title":"BioMed Res. Int."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/8\/3\/116\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:10:19Z","timestamp":1760188219000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/8\/3\/116"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8,11]]},"references-count":37,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2019,9]]}},"alternative-id":["antibiotics8030116"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics8030116","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,8,11]]}}}