{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T07:57:18Z","timestamp":1790409438671,"version":"4.1.0"},"reference-count":63,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,6,23]],"date-time":"2021-06-23T00:00:00Z","timestamp":1624406400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["Sonata BIS 2017\/26\/E\/ST4\/00041"],"award-info":[{"award-number":["Sonata BIS 2017\/26\/E\/ST4\/00041"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Bacteriophages (phages) are a specific type of viruses that infect bacteria. Because of growing antibiotic resistance among bacterial strains, phage-based therapies are becoming more and more attractive. The critical problem is the storage of bacteriophages. Recently, it was found that bacteriophages might adsorb on the surfaces of plastic containers, effectively decreasing the titer of phage suspensions. Here, we showed that a BOA nanocomposite (gold nanoparticles embedded in polyoxoborate matrix) deposited onto the inner walls of the containers stabilizes phage suspensions against uncontrolled adsorption and titer decrease. Additionally, BOA provides antibacterial and antifungal protection. The application of BOA assures safe and sterile means for the storage of bacteriophages.<\/jats:p>","DOI":"10.3390\/v13071206","type":"journal-article","created":{"date-parts":[[2021,6,23]],"date-time":"2021-06-23T21:14:51Z","timestamp":1624482891000},"page":"1206","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Gold\u2014Polyoxoborates Nanocomposite Prohibits Adsorption of Bacteriophages on Inner Surfaces of Polypropylene Labware and Protects Samples from Bacterial and Yeast Infections"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7822-9513","authenticated-orcid":false,"given":"Mateusz","family":"Wdowiak","sequence":"first","affiliation":[{"name":"Institute of Physical Chemistry, Polish Academy of Sciences, Kasprzaka 44\/52, 01-224 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enkhlin","family":"Ochirbat","sequence":"additional","affiliation":[{"name":"Institute of Physical Chemistry, Polish Academy of Sciences, Kasprzaka 44\/52, 01-224 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3758-3951","authenticated-orcid":false,"given":"Jan","family":"Paczesny","sequence":"additional","affiliation":[{"name":"Institute of Physical Chemistry, Polish Academy of Sciences, Kasprzaka 44\/52, 01-224 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1128\/AAC.45.3.649-659.2001","article-title":"Bacteriophage Therapy","volume":"45","author":"Sulakvelidze","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1016\/S0140-6736(05)66759-1","article-title":"Georgia: An unlikely stronghold for bacteriophage therapy","volume":"365","author":"Parfitt","year":"2005","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1749-4486.2009.01973.x","article-title":"A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; A preliminary report of efficacy","volume":"34","author":"Wright","year":"2009","journal-title":"Clin. Otolaryngol."},{"key":"ref_4","first-page":"1","article-title":"Intravesical bacteriophages for treating urinary tract infections in patients undergoing transurethral resection of the prostate: A randomised, placebo-controlled, double-blind clinical trial","volume":"3099","author":"Leitner","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_5","first-page":"1","article-title":"Safety and efficacy of phage therapy via the intravenous route","volume":"363","author":"Speck","year":"2015","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Aslam, S., Lampley, E., Wooten, D., Karris, M., Benson, C., Strathdee, S., and Schooley, R.T. (2020). Lessons learned from the first 10 consecutive cases of intravenous bacteriophage therapy to treat multidrug-resistant bacterial infections at a single center in the United States. Open Forum Infect. Dis., 7.","DOI":"10.1093\/ofid\/ofaa389"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/S1473-3099(18)30482-1","article-title":"Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): A randomised, controlled, double-blind phase 1\/2 trial","volume":"19","author":"Jault","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1346","DOI":"10.1007\/s00216-005-3289-y","article-title":"Thermostability of landscape phage probes","volume":"382","author":"Brigati","year":"2005","journal-title":"Anal. Bioanal. Chem."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep39235","article-title":"Genetically manipulated phages with improved pH resistance for oral administration in veterinary medicine","volume":"6","author":"Nobrega","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1002\/(SICI)1099-1352(199812)11:1\/6<91::AID-JMR397>3.0.CO;2-O","article-title":"Phage viability in organic media: Insights into phage stability","volume":"11","author":"Olofsson","year":"1998","journal-title":"J. Mol. Recognit."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/S1074-5521(01)00041-2","article-title":"Filamentous bacteriophage stability in non-aqueous media","volume":"8","author":"Olofsson","year":"2001","journal-title":"Chem. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1080\/14787210.2019.1646126","article-title":"Factors determining phage stability\/activity: Challenges in practical phage application","volume":"17","author":"Kula","year":"2019","journal-title":"Expert Rev. Anti. Infect. Ther."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"7387","DOI":"10.1038\/s41598-021-86571-x","article-title":"Adsorption of bacteriophages on polypropylene labware affects the reproducibility of phage research","volume":"11","author":"Richter","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.cis.2010.12.007","article-title":"Understanding protein adsorption phenomena at solid surfaces","volume":"162","author":"Rabe","year":"2011","journal-title":"Adv. Colloid Interface Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.jcis.2005.05.059","article-title":"Collagen adsorption and structure on polymer surfaces observed by atomic force microscopy","volume":"292","author":"Woodcock","year":"2005","journal-title":"J. Colloid Interface Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/0021-9797(92)90148-F","article-title":"Surface hydrophobic influences on \u03b2-lactoglobulin adsorption kinetics","volume":"154","author":"Krisdhasima","year":"1992","journal-title":"J. Colloid Interface Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.cis.2017.05.014","article-title":"Formulation, stabilisation and encapsulation of bacteriophage for phage therapy","volume":"249","author":"Malik","year":"2017","journal-title":"Adv. Colloid Interface Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.procbio.2017.09.022","article-title":"Structural and functional stabilization of bacteriophage particles within the aqueous core of a W\/O\/W multiple emulsion: A potential biotherapeutic system for the inhalational treatment of bacterial pneumonia","volume":"64","author":"Rios","year":"2018","journal-title":"Process Biochem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3802","DOI":"10.1021\/acsbiomaterials.7b00468","article-title":"Long-Term Preservation of Bacteriophage Antimicrobials Using Sugar Glasses","volume":"4","author":"Leung","year":"2018","journal-title":"ACS Biomater. Sci. Eng."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"18295","DOI":"10.1021\/acsomega.8b02679","article-title":"Long-Term Antimicrobial Activity of Phage-Sugar Glasses is Closely Tied to the Processing Conditions","volume":"3","author":"Leung","year":"2018","journal-title":"ACS Omega"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.colsurfb.2017.09.002","article-title":"Stabilization of T4 bacteriophage at acidic and basic pH by adsorption on paper","volume":"160","author":"Meyer","year":"2017","journal-title":"Colloids Surfaces B Biointerfaces"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.ijpharm.2010.01.034","article-title":"Stabilization of bacteriophage during freeze drying","volume":"389","author":"Puapermpoonsiri","year":"2010","journal-title":"Int. J. Pharm."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"27","DOI":"10.2471\/BLT.07.045096","article-title":"Estimating the costs of achieving the WHO-UNICEF Global Immunization Vision and Strategy, 2006-2015","volume":"86","author":"Wolfson","year":"2008","journal-title":"Bull. World Health Organ."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Braun, L.T.J., Jezek, J., Peterson, S., Tyagi, A., Perkins, S., Sylvester, D., Guy, M., Lal, M., Priddy, S., and Plzak, H. (2009). Characterization of a thermostable hepatitis B vaccine formulation. Vaccine.","DOI":"10.1016\/j.vaccine.2009.05.069"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.jviromet.2012.06.014","article-title":"A plate-based high-throughput assay for virus stability and vaccine formulation","volume":"185","author":"Walter","year":"2012","journal-title":"J. Virol. Methods"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1038\/sj.gt.3301527","article-title":"Development of formulations that enhance physical stability of viral vectors for gene therapy","volume":"8","author":"Croyle","year":"2001","journal-title":"Gene Ther."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Evans, R.K., Nawrocki, D.K., Isopi, L.A., Williams, D.M., Casimiro, D.R., Chin, S., Chen, M., Zhu, D.M., Shiver, J.W., and Volkin, D.B. (2004). Development of stable liquid formulations for adenovirus-based vaccines. J. Pharm. Sci.","DOI":"10.1002\/jps.20157"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Rexroad, J., Wiethoff, C.M., Green, A.P., Kierstead, T.D., Scott, M.O., and Middaugh, C.R. (2003). Structural stability of adenovirus type 5. J. Pharm. Sci.","DOI":"10.1002\/jps.10340"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Stewart, M., Ward, S.J., and Drew, J. (2014). Use of adenovirus as a model system to illustrate a simple method using standard equipment and inexpensive excipients to remove live virus dependence on the cold-chain. Vaccine.","DOI":"10.1016\/j.vaccine.2014.02.033"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"13520","DOI":"10.1038\/ncomms13520","article-title":"Additives for vaccine storage to improve thermal stability of adenoviruses from hours to months","volume":"7","author":"Pelliccia","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3931","DOI":"10.1021\/am508979y","article-title":"Gold-oxoborate nanocomposites and their biomedical applications","volume":"7","author":"Paczesny","year":"2015","journal-title":"ACS Appl. Mater. Interfaces"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"115900","DOI":"10.1016\/j.watres.2020.115900","article-title":"Evaluating the effect of silver nanoparticles on bacteriophage lytic infection cycle-a mechanistic understanding","volume":"181","author":"Gilcrease","year":"2020","journal-title":"Water Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2857","DOI":"10.2147\/IJN.S161379","article-title":"Responses of intestinal virome to silver nanoparticles: Safety assessment by classical virology, whole-genome sequencing and bioinformatics approaches","volume":"Volume 13","author":"Gokulan","year":"2018","journal-title":"Int. J. Nanomedicine"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.psep.2018.04.005","article-title":"Chick-Watson kinetics of virus inactivation with granular activated carbon modified with silver nanoparticles and\/or copper oxide","volume":"117","author":"Shimabuku","year":"2018","journal-title":"Process Saf. Environ. Prot."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1016\/j.watres.2010.12.017","article-title":"Inactivation and surface interactions of MS-2 bacteriophage in a TiO2 photoelectrocatalytic reactor","volume":"45","author":"Cho","year":"2011","journal-title":"Water Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.jcis.2017.02.059","article-title":"Inactivation of MS2 bacteriophage by titanium dioxide nanoparticles in the presence of quartz sand with and without ambient light","volume":"497","author":"Syngouna","year":"2017","journal-title":"J. Colloid Interface Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1128\/AEM.02433-09","article-title":"Biogenic Silver for Disinfection of Water Contaminated with Viruses","volume":"76","author":"Sintubin","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.1080\/09593330.2016.1245361","article-title":"Water treatment with exceptional virus inactivation using activated carbon modified with silver (Ag) and copper oxide (CuO) nanoparticles","volume":"38","author":"Shimabuku","year":"2017","journal-title":"Environ. Technol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1021\/acs.est.9b05211","article-title":"Nano-Sized Copper (Oxide) on Alumina Granules for Water Filtration: Effect of Copper Oxidation State on Virus Removal Performance","volume":"54","author":"Mazurkow","year":"2020","journal-title":"Environ. Sci. Technol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1016\/j.scitotenv.2018.08.380","article-title":"Removal of bacteriophage f2 in water by Fe\/Ni nanoparticles: Optimization of Fe\/Ni ratio and influencing factors","volume":"649","author":"Cheng","year":"2019","journal-title":"Sci. Total Environ."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"7410","DOI":"10.1021\/la100591h","article-title":"Charged gold nanoparticles in non-polar solvents: 10-min synthesis and 2D self-assembly","volume":"26","author":"Martin","year":"2010","journal-title":"Langmuir"},{"key":"ref_42","unstructured":"Sambrook, J., and Russel, D.W. (2001). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Press."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Bishop, M., Shahid, N., Yang, J., and Barron, A.R. (2004). Determination of the mode and efficacy of the cross-linking of guar by borate using MAS 11 B NMR of borate cross-linked guar in combination with solution 11 B NMR of model systems. Dalt. Trans., 2621\u20132634.","DOI":"10.1039\/B406952H"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Davidson, M.G., Wade, K., Marder, T.B., and Hughes, A.K. (2000). Contemporary Boron Chemistry, Royal Society of Chemistry. Special Publications.","DOI":"10.1039\/9781847550644"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Farafonov, V.S., and Nerukh, D. (2019). MS2 bacteriophage capsid studied using all-atom molecular dynamics. Interface Focus, 9.","DOI":"10.1098\/rsfs.2018.0081"},{"key":"ref_46","first-page":"14","article-title":"MS2 Coliphage as a Surrogate for 2009 Pandemic Influenza A (H1N1) Virus (pH1N1) in Surface Survival Studies on N95 Filtering Facepiece Respirators","volume":"21","author":"Coulliette","year":"2014","journal-title":"J. Int. Soc. Respir. Prot."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0168815","article-title":"Resistance of aerosolized bacterial viruses to four germicidal products","volume":"11","author":"Turgeon","year":"2016","journal-title":"PLoS ONE"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Turgeon, N., Toulouse, M.J., Martel, B., Moineau, S., and Duchaine, C. (2014). Comparison of five bacteriophages as models for viral aerosol studies. Appl. Environ. Microbiol.","DOI":"10.1128\/AEM.00767-14"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"271","DOI":"10.2174\/1570193X1203150429105418","article-title":"M13 Bacteriophage-Based Self-Assembly Structures and Their Functional Capabilities","volume":"12","author":"Moon","year":"2015","journal-title":"Mini. Rev. Org. Chem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/0042-6822(64)90173-4","article-title":"Some physical-chemical and biological properties of the rod-shaped coliphage M13","volume":"24","author":"Salivar","year":"1964","journal-title":"Virology"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/S1389-0344(01)00087-9","article-title":"Engineering M13 for phage display","volume":"18","author":"Sidhu","year":"2001","journal-title":"Biomol. Eng."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1007\/s00705-006-0849-1","article-title":"5500 Phages examined in the electron microscope","volume":"152","author":"Ackermann","year":"2007","journal-title":"Arch. Virol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Keen, E.C. (2015). A century of phage research: Bacteriophages and the shaping of modern biology. BioEssays.","DOI":"10.1002\/bies.201400152"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1021\/acs.est.5b04644","article-title":"Viruses at Solid-Water Interfaces: A Systematic Assessment of Interactions Driving Adsorption","volume":"50","author":"Armanious","year":"2016","journal-title":"Environ. Sci. Technol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"25385","DOI":"10.1039\/D0RA04086J","article-title":"Determination and characterisation of the surface charge properties of the bacteriophage M13 to assist bio-nanoengineering","volume":"10","author":"Passaretti","year":"2020","journal-title":"RSC Adv."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.snb.2015.09.042","article-title":"Ordering of bacteriophages in the electric field: Application for bacteria detection","volume":"224","author":"Richter","year":"2016","journal-title":"Sensors Actuators B Chem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"19622","DOI":"10.1021\/acsami.7b03497","article-title":"Dense Layer of Bacteriophages Ordered in Alternating Electric Field and Immobilized by Surface Chemical Modification as Sensing Element for Bacteria Detection","volume":"9","author":"Richter","year":"2017","journal-title":"ACS Appl. Mater. Interfaces"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jhazmat.2017.10.014","article-title":"An overview of chemical additives present in plastics: Migration, release, fate and environmental impact during their use, disposal and recycling","volume":"344","author":"Hahladakis","year":"2018","journal-title":"J. Hazard. Mater."},{"key":"ref_59","unstructured":"Grzeskowiak, R., Gerke, N., and Ag, E. (2015). Leachables: Minimizing the Influence of Plastic Consumables on the Laboratory Workflows, Eppendorf."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1128\/jb.69.4.393-398.1955","article-title":"the Growth of Escherichia Coli in Buffer Substrate and Distilled Water","volume":"69","author":"Garvie","year":"1955","journal-title":"J. Bacteriol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"6981","DOI":"10.1039\/c2ra20684f","article-title":"The toxic effect of silver ions and silver nanoparticles towards bacteria and human cells occurs in the same concentration range","volume":"2","author":"Greulich","year":"2012","journal-title":"RSC Adv."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1023\/A:1005905604043","article-title":"Laboratory contamination management: The requirement for microbiological quality assurance","volume":"52","author":"Leifert","year":"1998","journal-title":"Plant Cell. Tissue Organ Cult."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.ijfoodmicro.2018.07.031","article-title":"Spoilage yeasts: What are the sources of contamination of foods and beverages?","volume":"286","author":"Serradilla","year":"2018","journal-title":"Int. J. Food Microbiol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/7\/1206\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:21:56Z","timestamp":1760163716000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/7\/1206"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,23]]},"references-count":63,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["v13071206"],"URL":"https:\/\/doi.org\/10.3390\/v13071206","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,23]]}}}