Characterization of silk sutures coated with propolis and biogenic silver nanoparticles (AgNPs); an eco-friendly solution with wound healing potential against surgical site infections (SSIs)

Background/aim: Bacterial adherence to a suture material is one of the main causes of surgical site infections. An antibacterialsuture material with enhanced wound healing function may protect the surgical site from infections. Thus, the present study aimed toinvestigate the synergistic effect of propolis and biogenic metallic nanoparticles when combined with silk sutures for biomedical use.Materials and methods: Silver nanoparticle (AgNP) synthesis was carried out via a microbial-mediated biological route andimpregnated on propolis-loaded silk sutures using an in situ process. Silk sutures fabricated with propolis and biosynthesized AgNPs(bioAgNP-propolis-coated sutures) were intensively characterized using scanning electron microscopy (SEM), energy dispersive X-rayspectroscopy (EDS), thermogravimetric analysis (TGA), and differential scanning calorimetry (DSC). The antibacterial characteristicsof the bioAgNP-propolis-coated sutures were evaluated using the agar plate method. The biocompatibility of the bioAgNP-propoliscoatedsutures was evaluated using 3T3 fibroblast cells, and their wound-healing potential was also investigated.Results: BioAgNP-propolis-coated sutures displayed potent antibacterial activity against pathogenic gram-negative and gram-positivebacteria, Escherichia coli and Staphylococcus aureus, respectively. BioAgNP-propolis-coated silk sutures were found to be biocompatiblewith 3T3 fibroblast cell culture. In vitro wound healing scratch assay also demonstrated that the extract of bioAgNP-propolis-coatedsutures stimulated the 3T3 fibroblasts’ cell proliferation.Conclusion: Coating the silk sutures with propolis and biogenic AgNPs gave an effective antibacterial capacity to surgical suturesbesides providing biocompatibility and wound healing activity.

PDF

___

1. Edmiston CE, Seabrook GR, Goheen MP, Krepel CJ, Johnson CP et al. Bacterial adherence to surgical sutures: can antibacterial-coated sutures reduce the risk of microbial contamination?. Journal of the American College of Surgeons 2006; 203 (4): 481-489. doi: 10.1016/j.jamcollsurg.2006.06.026
2. Katz S, Izhar M, Mirelman D. Bacterial adherence to surgical sutures. A possible factor in suture induced infection. Annals of Surgery 1981; 194: 35-41.
3. Justinger C, Moussavian MR, Schlueter C, Kopp B, Kollmar O et al. Antibiotic coating of abdominal closure sutures and wound infection. Surgery 2009; 145: 330-334. doi: 10.1016/j. surg.2008.11.007
4. Grigg TR, Liewehr FR, Patton WR, Buxton TB, McPherson JC. Effect of the wicking behavior of multifilament sutures. Journal of Endodontics 2004; 30: 649-652. doi: 10.1097/01. DON.0000121617.67923.05
5. Mingmalairak C, Ungbhakorn P, Paocharoen V. Efficacy of antimicrobial coating suture coated polyglactin 910 with tricosan (Vicryl plus) compared with polyglactin 910 (Vicryl) in reduced surgical site infection of appendicitis, double blind randomized control trial, preliminary safety report. Journal of the Medical Association of Thailand 2009; 92 (6): 770-775.
6. van Duin D, Paterson DL. Multidrug-resistant bacteria in the community: trends and lessons learned. Infectious Disease Clinics of North America 2016; 30 (2): 377-390. doi: 10.1016/j. idc.2016.02.004
7. Stepanović S, Antić N, Dakić I, Švabić-Vlahović M. In vitro antimicrobial activity of propolis and synergism between propolis and antimicrobial drugs. Microbiological Research 2003; 158 (4): 353-357. doi: 10.1078/0944-5013- 00215
8. Ramos AFN, Miranda JD. Propolis: a review of its antiinflammatory and healing actions. Journal of Venomous Animals and Toxins including Tropical Diseases 2007; 13 (4): 697-710. doi: 10.1590/S1678-91992007000400002
9. do Nascimento TG, Silva ADS, Lessa Constant PB, da Silva SAS, Fidelis de Moura MAB et al. Phytochemical screening, antioxidant and antibacterial activities of some commercial extract of propolis. Journal of Apicultural Research 2018; 57 (2): 246-254. doi: 10.1080/00218839.2017.1412563
10. Airen B, Sarkar PA, Tomar U, Bishen KA. Antibacterial effect of propolis derived from tribal region on Streptococcus mutans and Lactobacillus acidophilus: An in vitro study. Journal of Indian Society of Pedodontics and Preventive Dentistry 2018; 36 (1): 48-52. doi: 10.4103/JISPPD.JISPPD_1128_17
11. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ et al. Antimicrobial effects of silver nanoparticles. Nanomedicine 2007; 3 (1): 95- 101. doi: 10.1016/j.nano.2006.12.001
12. Paladini F, Pollin, M, Sannino A, Ambrosio L. Metal-based antibacterial substrates for biomedical applications. Biomacromolecules 2015; 16 (7): 1873-1885. doi: 10.1021/acs.biomac.5b00773
13. Rai M, Yadav A, Gade A. Silver nanoparticles as a new generation of antimicrobials. Biotechnology Advances 2009; 27 (1): 76-83. doi: 10.1016/j.biotechadv.2008.09.002
14. Mooranian A, Negrulj R, Mathavan S, Martinez J, Sciarretta J et al. An advanced microencapsulated system: a platform for optimized oral delivery of antidiabetic drug-bile acid formulations. Pharmaceutical Development and Technology 2015; 20 (6): 702-709. doi: 10.3109/10837450.2014.915570
15. Verma VC, Kharwar RN, Gange AC. Biosynthesis of noble metal nanoparticles and their application. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2009; 4 (026): 1-17. doi: 10.1079/PAVSNNR20094026
16. Obermeier A, Schneider J, Harrasser N, Tübel J, Mühlhofer H et al. Viable adhered Staphylococcus aureus highly reduced on novel antimicrobial sutures using chlorhexidine and octenidine to avoid surgical site infection (SSI). PloS one 2018; 13 (1): e0190912. doi: 10.1371/journal.pone.0190912
17. Baygar T, Ugur A. Biosynthesis of silver nanoparticles by Streptomyces griseorubens isolated from soil and their antioxidant activity. IET Nanobiotechnology 2016; 11 (3): 286- 291. doi: 10.1049/iet-nbt.2015.0127
18. Baygar T, Sarac N, Ugur A, Karaca IR. Antimicrobial characteristics and biocompatibility of the surgical sutures coated with biosynthesized silver nanoparticles. Bioorganic Chemistry 2019; 86: 254-258. doi: 10.1016/j.bioorg.2018.12.034
19. National Committee for Clinical Laboratory Standards (NCCLS): ‘Approval standard M7-A3, Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically’, Villanova, PA, USA 1993
20. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 1983; 65: 55-63. doi: 10.1016/0022-1759(83)90303-4
21. Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nature Protocols 2007; 2 (2): 329-333. doi: 10.1038/ nprot.2007.30
22. Dhas SP, Anbarasan S, Mukherjee A. Chandrasekaran N. Biobased silver nanocolloid coating on silk fibers for prevention of post-surgical wound infections. International Journal of Nanomedicine 2015; 10 (Suppl 1): 159-170. doi:10.2147/IJN. S82211
23. Ho MP, Wang H, Lau KT. Thermal properties and structure conformation on silkworm silk fibre. In: Proceedings of the Composites Australia and CRC-ACS Conference: Diversity in Composite, Leura, Australia, 2012, pp. 1-8.
24. Elakkiya T, Malarvizhi G, Rajiv S, Natarajan TS. Curcumin loaded electrospun Bombyx mori silk nanofibers for drug delivery. Polymer International 2014; 63 (1): 100–105. doi: 10.1002/pi.4499
25. Mohanpuria P, Rana NK, Yadav SK. Biosynthesis of nanoparticles: technological concepts and future applications. Journal of Nanoparticle Research 2008; 10 (3): 507-517. doi: 10.1007/s11051-007-9275-x
26. Pollini M, Russo M, Licciulli A, Sannino A, Maffezzoli A. Characterization of antibacterial silver coated yarns. Journal of Materials Science: Materials in Medicine 2009; 20 (11): 2361- 2366. doi: 10.1007/s10856-009-3796-z
27. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP et al. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clinical Infectious Diseases 2004; 39 (3): 309-317. doi: 10.1086/421946
28. Ugur A, Barlas M, Ceyhan N, Turkmen V. Antimicrobial effects of propolis extracts on Escherichia coli and Staphylococcus aureus strains resistant to various antibiotics and some microorganisms. Journal of Medicinal Food 2000; 3 (4): 173- 180. doi: 10.1089/jmf.2000.3.173
29. Uzel A, Önçağ Ö, Çoğulu D, Gençay Ö. Chemical compositions and antimicrobial activities of four different Anatolian propolis samples. Microbiological Research 2005; 160 (2): 189-195. doi: 10.1016/j.micres.2005.01.002
30. Tosi EA, Re E, Ortega ME. Cazzoli AF. Food preservative based on propolis: Bacteriostatic activity of propolis polyphenols and flavonoids upon Escherichia coli. Food Chemistry 2007; 104 (3): 1025-1029. doi: 10.1016/j.foodchem.2007.01.011
31. Pratten J, Nazhat SN, Blaker JJ, Boccaccini AR. In vitro attachment of Staphylococcus epidermidis to surgical sutures with and without Ag-containing bioactive glass coating. Journal of Biomaterials Applications 2004; 19 (1): 47-57. doi: 10.1177/0885328204043200
32. De Simone S, Gallo AL, Paladini F, Sannino A, Pollini M. Development of silver nano-coatings on silk sutures as a novel approach against surgical infections. Journal of Materials Science: Materials in Medicine 2014; 25 (9): 2205-2214. doi: 10.1007/s10856-014-5262-9
33. Yan X, He B, Liu L, Qu G, Shi J et al. Antibacterial mechanism of silver nanoparticles in pseudomonas aeruginosa: Proteomics approach. Metallomics 2018; 10: 557–564. doi: 10.1039/ C7MT00328E
34. Hendi A. Silver nanoparticles mediate differential responses in some of liver and kidney functions during skin wound healing. Journal of King Saud University-Science 2011; 23: 47–52. doi: 10.1016/j.jksus.2010.06.006
35. Gong CP, Li SC, Wang RY. Development of biosynthesized silver nanoparticles based formulation for treating wounds during nursing care in hospitals. Journal of Photochemistry and Photobiology B: Biology 2018; 183: 137–141. doi: 10.1016/j.jphotobiol.2018.04.030
36. Burdușel AC, Gherasim O, Grumezescu A, Mogoantă L, Ficai A et al. Biomedical applications of silver nanoparticles: An upto- date overview. Nanomaterials 2018; 8 (9): 681. doi: 10.3390/ nano8090681
37. Kumar SSD, Rajendran NK, Houreld NN, Abrahamse H. Recent advances on silver nanoparticle and biopolymer based biomaterials for wound healing applications. International Journal of Biological Macromolecules 2018; 115: 165-175. doi: 10.1016/j.ijbiomac.2018.04.003
38. Tian J, Wong KK, Ho CM, Lok CN, Yu WY et al. Topical delivery of silver nanoparticles promotes wound healing. ChemMedChem 2007; 2 (1): 129-136. doi: 10.1002/ cmdc.200600171
39. Gallo AL, Paladini F, Romano A, Verri T, Quattrini A et al. Efficacy of silver coated surgical sutures on bacterial contamination, cellular response and wound healing. Materials Science and Engineering: C 2016; 69: 884-893. doi: 10.1016/j. msec.2016.07.074
40. Gallo AL, Pollini M, Paladini F. A combined approach for the development of novel sutures with antibacterial and regenerative properties: the role of silver and silk sericin functionalization. Journal of Materials Science: Materials in Medicine 2018; 29: 133. doi: 10.1007/s10856-018-6142-5