Polymers are currently widely used to replace a variety of natural materials with respect to their favourable physical and chemical properties, and due to their economic advantage. One of the most important branches of application of polymers is the production of different products for medical use. In this case, it is necessary to face a significant disadvantage of polymer products due to possible and very common colonization of the surface by various microorganisms that can pose a potential danger to the patient. One of the possible solutions is to prepare polymer with antibacterial/antimicrobial properties that is resistant to bacterial colonization. The aim of this study was to contribute to the development of antimicrobial polymeric material ideal for covering vascular implants with subsequent use in transplant surgery. Therefore, the complexes of polymeric substances (hyaluronic acid and chitosan) with silver nitrate or silver phosphate nanoparticles were created, and their effects on gram-positive bacterial culture of Staphylococcus aureus were monitored. Stages of formation of complexes of silver nitrate and silver phosphate nanoparticles with polymeric compounds were characterized using electrochemical and spectrophotometric methods. Furthermore, the antimicrobial activity of complexes was determined using the methods of determination of growth curves and zones of inhibition. The results of this study revealed that the complex of chitosan, with silver phosphate nanoparticles, was the most suitable in order to have an antibacterial effect on bacterial culture of Staphylococcus aureus. Formation of this complex was under way at low concentrations of chitosan. The results of electrochemical determination corresponded with the results of spectrophotometric methods and verified good interaction and formation of the complex. The complex has an outstanding antibacterial effect and this effect was of several orders higher compared to other investigated complexes.

Department of Chemistry and Biochemistry Faculty of Agronomy Mendel University in Brno Zemedelska 1 CZ 613 00 Brno Czech Republic

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Perl T.M., Cullen J.J., Wenzel R.P., Zimmerman M.B., Pfaller M.A., Sheppard D., Twombley J., French P.P., Herwaldt L.A. the Mupirocin and the Risk of Staphylococcus aureus Study Team. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N. Engl. J. Med. 2002;346:1871–1877. PubMed

Ginalska G., Osinska M., Uryniak A., Urbanik-Sypniewska T., Belcarz A., Rzeski W., Wolski A. Antibacterial activity of gentamicin-bonded gelatin-sealed polyethylene terephthalate vascular prostheses. Eur. J. Vasc. Endovasc. Surg. 2005;29:419–424. PubMed

Bandyk D.F. Vascular surgical site infection: Risk factors and preventive measures. Semin. Vasc. Surg. 2008;21:119–123. PubMed

Teebken O.E., Bisdas T., Assadian O., Ricco J.B. Recommendations for reporting treatment of aortic graft infections. Eur. J. Vasc. Endovasc. Surg. 2012;43:174–181. PubMed

Homer-Vanniasinkam S. Surgical site and vascular infections: Treatment and prophylaxis. Int. J. Infect. Dis. 2007;11:S17–S22. PubMed

O’Brien R., Pocock N., Torella F. Wound infection after reconstructive arterial surgery of the lower limbs: Risk factors and consequences. Surg. J. R. Coll. Surg. Edinb. Irel. 2011;9:245–248. PubMed

Tatterton M.R., Homer-Vanniasinkam S. Infections in vascular surgery. Injury-Int. J. Care Inj. 2011;42:S35–S41. PubMed

Nasim A., Thompson M.M., Naylor A.R., Bell P.R.F., London N.J.M. The impact of MRSA on vascular surgery. Eur. J. Vasc. Endovasc. Surg. 2001;22:211–214. PubMed

Young M.H., Upchurch G.R., Malani P.N. Vascular graft infections. Infect. Dis. Clin. N. Am. 2012;26:41–56. PubMed

Anderson D.J., Sexton D.J., Kanafani Z.A., Auten G., Kaye K.S. Severe surgical site infection in community hospitals: Epidemiology, key procedures, and the changing prevalence of methicillin-resistant staphylococcus aureus. Infect. Control Hosp. Epidemiol. 2007;28:1047–1053. PubMed

Earnshaw J.J. Methicillin-resistant Staphylococcus aureus: Vascular surgeons should fight back. Eur. J. Vasc. Endovasc. Surg. 2002;24:283–286. PubMed

Driscoll A.J., Bhat N., Karron R.A., O’Brien K.L., Murdoch D.R. Disk diffusion bioassays for the detection of antibiotic activity in body fluids: Applications for the pneumonia etiology research for child health project. Clin. Infect. Dis. 2012;54:S159–S164. PubMed

Lew W., Moore W. Antibiotic-impregnated grafts for aortic reconstruction. Semin. Vasc. Surg. 2011;24:211–219. PubMed

Ricco J.B., Assadian O. Antimicrobial silver grafts for prevention and treatment of vascular graft infection. Semin. Vasc. Surg. 2011;24:234–241. PubMed

Green J.B.D., Fulghum T., Nordhaus M.A. Review of immobilized antimicrobial agents and methods for testing. Biointerphases. 2011;6:MR13–MR28. PubMed

Osinska-Jaroszuk M., Ginalska G., Belcarz A., Uryniak A. Vascular prostheses with covalently bound gentamicin and amikacin reveal superior antibacterial properties than silver-impregnated ones—An in vitro study. Eur. J. Vasc. Endovasc. Surg. 2009;38:697–706. PubMed

Rai M.K., Deshmukh S.D., Ingle A.P., Gade A.K. Silver nanoparticles: The powerful nanoweapon against multidrug-resistant bacteria. J. Appl. Microbiol. 2012;112:841–852. PubMed

Unger C., Luck C. Inhibitory effects of silver ions on Legionella pneumophila grown on agar, intracellular in Acanthamoeba castellanii and in artificial biofilms. J. Appl. Microbiol. 2012;112:1212–1219. PubMed

Xu H.Y., Qu F., Xu H., Lai W.H., Wang Y.A., Aguilar Z.P., Wei H. Role of reactive oxygen species in the antibacterial mechanism of silver nanoparticles on Escherichia coli O157:H7. Biometals. 2012;25:45–53. PubMed

Park H.J., Kim J.Y., Kim J., Lee J.H., Hahn J.S., Gu M.B., Yoon J. Silver-ion-mediated reactive oxygen species generation affecting bactericidal activity. Water Res. 2009;43:1027–1032. PubMed

Kwakye-Awuah B., Williams C., Kenward M.A., Radecka I. Antimicrobial action and efficiency of silver-loaded zeolite X. J. Appl. Microbiol. 2008;104:1516–1524. PubMed

Li W.R., Xie X.B., Shi Q.S., Duan S.S., Ouyang Y.S., Chen Y.B. Antibacterial effect of silver nanoparticles on Staphylococcus aureus. Biometals. 2011;24:135–141. PubMed

Limbach L.K., Wick P., Manser P., Grass R.N., Bruinink A., Stark W.J. Exposure of engineered nanoparticles to human lung epithelial cells: Influence of chemical composition and catalytic activity on oxidative stress. Environ. Sci. Technol. 2007;41:4158–4163. PubMed

Choi O., Deng K.K., Kim N.J., Ross L., Surampalli R.Y., Hu Z.Q. The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res. 2008;42:3066–3074. PubMed

Chen Y.G., Chen H., Zheng X., Mu H. The impacts of silver nanoparticles and silver ions on wastewater biological phosphorous removal and the mechanisms. J. Hazard. Mater. 2012;239:88–94. PubMed

Jo H.J., Choi J.W., Lee S.H., Hong S.W. Acute toxicity of Ag and CuO nanoparticle suspensions against Daphnia magna: The importance of their dissolved fraction varying with preparation methods. J. Hazard. Mater. 2012;227:301–308. PubMed

Joshi N., Ngwenya B.T., French C.E. Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances. J. Hazard. Mater. 2012;241:363–370. PubMed

Pallavicini P., Taglietti A., Dacarro G., Diaz-Fernandez Y.A., Galli M., Grisoli P., Patrini M., de Magistris G.S., Zanoni R. Self-assembled monolayers of silver nanoparticles firmly grafted on glass surfaces: Low Ag+ release for an efficient antibacterial activity. J. Colloid Interface Sci. 2010;350:110–116. PubMed

Taglietti A., Fernandez Y.A.D., Amato E., Cucca L., Dacarro G., Grisoli P., Necchi V., Pallavicini P., Pasotti L., Patrini M. Antibacterial activity of glutathione-coated silver nanoparticles against gram positive and gram negative bacteria. Langmuir. 2012;28:8140–8148. PubMed

Dowling D.P., Betts A.J., Pope C., McConnell M.L., Eloy R., Arnaud M.N. Anti-bacterial silver coatings exhibiting enhanced activity through the addition of platinum. Surf. Coat. Technol. 2003;163:637–640.

Ruden S., Hilpert K., Berditsch M., Wadhwani P., Ulrich A.S. Synergistic interaction between silver nanoparticles and membrane-permeabilizing antimicrobial peptides. Antimicrob. Agents Chemother. 2009;53:3538–3540. PubMed PMC

Zitka O., Sobrova P., Adam V., Hubalek J., Provaznik I., Zizkova V., Kizek R. Nanotechnology for more efficient blood vessel replacements. Chem. Listy. 2013;107:24–29.

Evanko S.P., Wight T.N. Intracellular localization of hyaluronan in proliferating cells. J. Histochem. Cytochem. 1999;47:1331–1341. PubMed

Kogan G., Soltes L., Stern R., Gemeiner P. Hyaluronic acid: A natural biopolymer with a broad range of biomedical and industrial applications. Biotechnol. Lett. 2007;29:17–25. PubMed

Guibal E. Interactions of metal ions with chitosan-based sorbents: A review. Sep. Purif. Technol. 2004;38:43–74.

Pires N.R., Cunha P.L.R., Maciel J.S., Angelim A.L., Melo V.M.M., de Paula R.C.M., Feitosa J.P.A. Sulfated chitosan as tear substitute with no antimicrobial activity. Carbohydr. Polym. 2013;91:92–99. PubMed

Madhumathi K., Kumar P.T.S., Abhilash S., Sreeja V., Tamura H., Manzoor K., Nair S.V., Jayakumar R. Development of novel chitin/nanosilver composite scaffolds for wound dressing applications. J. Mater. Sci. 2010;21:807–813. PubMed

Jayakumar R., Menon D., Manzoor K., Nair S.V., Tamura H. Biomedical applications of chitin and chitosan based nanomaterials—A short review. Carbohydr. Polym. 2010;82:227–232.

Huang G.Q., Sun Y.T., Xiao J.X., Yang J. Complex coacervation of soybean protein isolate and chitosan. Food Chem. 2012;135:534–539. PubMed

Lee S.B., Kim Y.H., Chong M.S., Lee Y.M. Preparation and characteristics of hybrid scaffolds composed of beta-chitin and collagen. Biomaterials. 2004;25:2309–2317. PubMed

Abdel-Mohsen A.M., Hrdina R., Burgert L., Krylova G., Abdel-Rahman R.M., Krejcova A., Steinhart M., Benes L. Green synthesis of hyaluronan fibers with silver nanoparticles. Carbohydr. Polym. 2012;89:411–422. PubMed

Wan Y., Guo Z.R., Jiang X.L., Fang K., Lu X., Zhang Y., Gu N. Quasi-spherical silver nanoparticles: Aqueous synthesis and size control by the seed-mediated Lee-Meisel method. J. Colloid Interface Sci. 2013;394:263–268. PubMed

Jiang J., Chae B., Jeong S.K., Min B.K., Kim S.H., Piao L., Yoon S. Assembling Ag nanoparticles into morphology controlled secondary structures on loosely packed self-assembled monolayers. J. Colloid Interface Sci. 2013;394:639–642. PubMed

Boomi P., Prabu H.G., Mathiyarasu J. Synthesis and characterization of polyaniline/Ag-Pt nanocomposite for improved antibacterial activity. Colloid Surf. B. 2013;103:9–14. PubMed

Li G.Y., Wen Q.W., Zhang T., Ju Y.Y. Synthesis and properties of silver nanoparticles in chitosan-based thermosensitive semi-interpenetrating hydrogels. J. Appl. Polym. Sci. 2013;127:2690–2697.

Li X., Lenhart J.J. Aggregation and dissolution of silver nanoparticles in natural surface water. Environ. Sci. Technol. 2012;46:5378–5386. PubMed

Khan A., Qamar M., Muneer M. Synthesis of highly active visible-light-driven colloidal silver orthophosphate. Chem. Phys. Lett. 2012;519–520:54–58.

Bin Ahmad M., Lim J.J., Shameli K., Ibrahim N.A., Tay M.Y. Synthesis of silver nanoparticles in chitosan, gelatin and chitosan/gelatin bionanocomposites by a chemical reducing agent and their characterization. Molecules. 2011;16:7237–7248. PubMed PMC

Dospivova D., Hynek D., Kopel P., Bezdekova A., Sochor J., Krizkova S., Adam V., Trnkova L., Hubalek J., Babula P., et al. Electrochemical behaviour of apoferritin encapsulating of silver(i) ions and its application for treatment of Staphylococcus aureus. Int. J. Electrochem. Sci. 2012;7:6378–6395.

Trnkova L., Krizkova S., Adam V., Hubalek J., Kizek R. Immobilization of metallothionein to carbon paste electrode surface via anti-MT antibodies and its use for biosensing of silver. Biosens. Bioelectron. 2011;26:2201–2207. PubMed

Zitka O., Huska D., Adam V., Horna A., Beklova M., Svobodova Z., Kizek R. CoulArray detector as a tool for estimation of acute toxicity of silver(I) ions. Int. J. Electrochem. Sci. 2010;5:1082–1089.

Chekin F., Raoof J.B., Bagheri S., Abd Hamid S.B. The porous chitosan-sodium dodecyl sulfate-carbon nanotube nanocomposite: Direct electrochemistry and electrocatalysis of hemoglobin. Anal. Methods. 2012;4:2977–2981.

Ma L.P., Yuan R., Chai Y.Q., Chen S.H. Amperometric hydrogen peroxide biosensor based on the immobilization of HRP on DNA-silver nanohybrids and PDDA-protected gold nanoparticles. J. Mol. Catal. B. 2009;56:215–220.

An J., Luo Q.Z., Yuan X.Y., Wang D.S., Li X.Y. Preparation and characterization of silver-chitosan nanocomposite particles with antimicrobial activity. J. Appl. Polym. Sci. 2011;120:3180–3189.

Sharma S., Sanpui P., Chattopadhyay A., Ghosh S.S. Fabrication of antibacterial silver nanoparticle-sodium alginate-chitosan composite films. RSC Adv. 2012;2:5837–5843.

Rodriguez-Arguelles M.C., Sieiro C., Cao R., Nasi L. Chitosan and silver nanoparticles as pudding with raisins with antimicrobial properties. J. Colloid Interface Sci. 2011;364:80–84. PubMed

Murray P.R. What is new in clinical microbiology microbial identification by MALDI-TOF mass spectrometry a paper from the 2011 William Beaumont Hospital Symposium on molecular pathology. J. Mol. Diagn. 2012;14:419–423. PubMed PMC

Welker M. Proteomics for routine identification of microorganisms. Proteomics. 2011;11:3143–3153. PubMed

Jordana-Lluch E., Catala E.M., Ruiz V.A. Mass spectrometry in the clinical microbiology laboratory. Enferm. Infec. Microbiol. Clin. 2012;30:635–644. PubMed PMC

Kok J., Chen S.C.A., Dwyer D.E., Iredell J.R. Current status of matrix-assisted laser desorption ionisation-time of flight mass spectrometry in the clinical microbiology laboratory. Pathology. 2013;45:4–17. PubMed

Lu J.J., Tsai F.J., Ho C.M., Liu Y.C., Chen C.J. Peptide biomarker discovery for identification of methicillin-resistant and vancomycin-intermediate Staphylococcus aureus strains by MALDI-TOF. Anal. Chem. 2012;84:5685–5692. PubMed

Ouedraogo R., Daumas A., Ghigo E., Capo C., Mege J.L., Textoris J. Whole-cell MALDI-TOF MS: A new tool to assess the multifaceted activation of macrophages. J. Proteomics. 2012;75:5523–5532. PubMed

Van Veen S.Q., Claas E.C.J., Kuijper E.J. High-throughput identification of bacteria and yeast by matrix-assisted laser desorption ionization-time of flight mass spectrometry in conventional medical microbiology laboratories. J. Clin. Microbiol. 2010;48:900–907. PubMed PMC

Szabados F., Woloszyn J., Richter C., Kaase M., Gatermann S. Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J. Med. Microbiol. 2010;59:787–790. PubMed

Charyulu E.M., Gnanamani A., Mandal A.B. Identification and Discrimination of methicillin resistant Staphylococcus aureus strains isolated from burn wound sites using pcr and authentication with MALDI-TOF-MS. Indian J. Microbiol. 2012;52:337–345. PubMed PMC

Bohme K., Morandi S., Cremonesi P., No I.C.F., Barros-Velazquez J., Castiglioni B., Brasca M., Canas B., Calo-Mata P. Characterization of Staphylococcus aureus strains isolated from Italian dairy products by MALDI-TOF mass fingerprinting. Electrophoresis. 2012;33:2355–2364. PubMed

Verma V.C., Kharwar R.N., Gange A.C. Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus. Nanomedicine. 2010;5:33–40. PubMed

Dar M.A., Ingle A., Rai M. Enhanced antimicrobial activity of silver nanoparticles synthesized by Cryphonectria sp. evaluated singly and in combination with antibiotics. Nanomedicine. 2013;9:105–110. PubMed

Mohanty S., Mishra S., Jena P., Jacob B., Sarkar B., Sonawane A. An investigation on the antibacterial, cytotoxic, and antibiofilm efficacy of starch-stabilized silver nanoparticles. Nanomedicine. 2012;8:916–924. PubMed

Martinez-Gutierrez F., Thi E.P., Silverman J.M., de Oliveira C.C., Svensson S.L., Hoek A.V., Sanchez E.M., Reiner N.E., Gaynor E.C., Pryzdial E.L.G., et al. Antibacterial activity, inflammatory response, coagulation and cytotoxicity effects of silver nanoparticles. Nanomedicine. 2012;8:328–336. PubMed

Martinez-Gutierrez F., Olive P.L., Banuelos A., Orrantia E., Nino N., Sanchez E.M., Ruiz F., Bach H., Av-Gay Y. Synthesis, characterization, and evaluation of antimicrobial and cytotoxic effect of silver and titanium nanoparticles. Nanomedicine. 2010;6:681–688. PubMed

Hrabarova E., Valachova K., Rychly J., Rapta P., Sasinkova V., Malikova M., Soltes L. High-molar-mass hyaluronan degradation by Weissberger’s system: Pro- and anti-oxidative effects of some thiol compounds. Polym. Degrad. Stabil. 2009;94:1867–1875.

Sintzel M.B., Bernatchez S.F., Tabatabay C., Gurny R. Biomaterials in ophthalmic drug delivery. Eur. J. Pharm. Biopharm. 1996;42:358–374.

Stern R. Devising a pathway for hyaluronan catabolism: Are we there yet? Glycobiology. 2003;13:105R–115R. PubMed

Teh B.M., Shen Y., Friedland P.L., Atlas M.D., Marano R.J. A review on the use of hyaluronic acid in tympanic membrane wound healing. Expert Opin. Biol. Ther. 2012;12:23–36. PubMed

Fernandez-Saiz P., Soler C., Lagaron J.M., Ocio M.J. Effects of chitosan films on the growth of Listeria monocytogenes, Staphylococcus aureus and Salmonella spp. in laboratory media and in fish soup. Int. J. Food Microbiol. 2010;137:287–294. PubMed

Borneman D.L., Ingham S.C., Ane C. Mathematical approaches to estimating lag-phase duration and growth rate for predicting growth of Salmonella serovars, Escherichia coli O157:H7, and Staphylococcus aureus in raw beef, bratwurst, and poultry. J. Food Prot. 2009;72:1190–1200. PubMed

Rufian-Henares J.A., Morales F.J. Microtiter plate-based assay for screening antimicrobial activity of melanoidins against E-coli and S-aureus. Food Chem. 2008;111:1069–1074.

Mahdavi B., Yaacob W.A., Din L.B., Nazlina I. Antimicrobial activity of consecutive extracts of Etlingera brevilabrum. Sains Malays. 2012;41:1233–1237.

Joray M.B., Gonzalez M.L., Palacios S.M., Carpinella M.C. Antibacterial activity of the plant-derived compounds 23-Methyl-6-O-desmethylauricepyrone and (Z,Z)-5-(Trideca-4,7- dienyl)resorcinol and their synergy with antibiotics against methicillin-susceptible and -resistant Staphylococcus aureus. J. Agric. Food Chem. 2011;59:11534–11542. PubMed

Tawiah A.A., Gbedema S.Y., Adu F., Boamah V.E., Annan K. Antibiotic producing microorganisms from River Wiwi, Lake Bosomtwe and the Gulf of Guinea at Doakor Sea Beach, Ghana. BMC Microbiol. 2012;12:1–8. PubMed PMC

Moussa A., Noureddine D., Mohamed H.S., Abdelmelek M., Saad A. Antibacterial activity of various honey types of Algeria against Staphylococcus aureus and Streptococcus pyogenes. Asian Pac. J. Trop. Med. 2012;5:773–776. PubMed

Lokendrajit N., Indira S., Swapana N., Singh C.B. Antioxidant and antimicrobial activity of Croton caudatus Geisel. Asian J. Chem. 2012;24:4418–4420.

Zaremba M., Borowski J., Polejczuk E., Jakubicz P. Evaluation of Staphytest, A New System for Identification of Staphylococci. Vol. 21. Gustav Fischer Verlag; Stuttgart, Germany: 1991. p. 87.

Sedlacek I., Kocur M. Identification of Staphylococcus and Micrococcus species with the Staphytest system. Folia Microbiol. 1991;36:401–405. PubMed

Radulescu M.C., Chira A., Radulescu M., Bucur B., Bucur M.P., Radu G.L. Determination of silver(i) by differential pulse voltammetry using a glassy carbon electrode modified with synthesized N-(2-Aminoethyl)-4,4′-Bipyridine. Sensors. 2010;10:11340–11351. PubMed PMC

Peverly A.A., Peters D.G. Electrochemical determination of trihalomethanes in water by means of stripping analysis. Anal. Chem. 2012;84:6110–6115. PubMed

Yan G.P., Wang Y.H., He X.X., Wang K.M., Su J., Chen Z.F., Qing Z.H. A highly sensitive electrochemical assay for silver ion detection based on un-labeled C-rich ssDNA probe and controlled assembly of MWCNTs. Talanta. 2012;94:178–183. PubMed

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