Quantitative study of early-stage transient bacterial adhesion to bioactive glass and glass ceramics: atomic force microscopic observations.
Atomic force microscopy (AFM)
Bacterial adhesion
Bio-mineral AFM probe
Bioactive glass
Force–distance measurement
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 Sep 2024
02 Sep 2024
Historique:
received:
28
02
2024
accepted:
15
07
2024
medline:
3
9
2024
pubmed:
3
9
2024
entrez:
2
9
2024
Statut:
epublish
Résumé
Antimicrobial potential of bioactive glass (BAG) makes it promising for implant applications, specifically overcoming the toxicity concerns associated with traditional antibacterial nanoparticles. The 58S composition of BAG (with high Ca and absence of Na) has been known to exhibit excellent bioactivity and antibacterial behaviour, but the mechanisms behind have not been investigated in detail. In this pioneering study, we are using Atomic Force Microscopy (AFM) to gain insights into 58S BAG's adhesive interactions with planktonic cells of both gram-positive (Staphylococcus aureus) and gram-negative (Escherichia coli) bacteria; along with the impact of crystallinity on antibacterial properties. We have recorded greater bacterial inhibition by amorphous BAG compared to semi-crystalline glass-ceramics and stronger effect against gram-negative bacteria via conventional long-term antibacterial tests. AFM force distance curves has illustrated substantial bonding between bacteria and BAG within the initial one second (observed at a gap of 250 ms) of contact, with multiple binding events. Further, stronger adhesion of BAG with E.coli (~ 6 nN) compared to S. aureus (~ 3 nN) has been found which can be attributed to more adhesive nano-domains (size effect) distributed uniformly on E.coli surface. This study has revealed direct evidence of impact of contact time and 58S BAG's crystalline phase on bacterial adhesion and antimicrobial behaviour. Current study has successfully demonstrated the mode and mechanisms of initial bacterial adhesion with 58S BAG. The outcome can pave the way towards improving the designing of implant surfaces for a range of biomedical applications.
Identifiants
pubmed: 39223136
doi: 10.1038/s41598-024-67716-0
pii: 10.1038/s41598-024-67716-0
doi:
Substances chimiques
Glass ceramics
85422-94-2
Anti-Bacterial Agents
0
bioactive glass 58S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
20336Subventions
Organisme : Department of Science and Technology, Ministry of Science and Technology, India
ID : DST/SJF/ETA-02-2016-17
Organisme : Department of Science and Technology, Ministry of Science and Technology, India
ID : DST/SJF/ETA-02-2016-17
Organisme : Curtin University of Technology
ID : CIPRS
Informations de copyright
© 2024. The Author(s).
Références
Hu, C., Ashok, D., Nisbet, D. R. & Gautam, V. Bioinspired surface modification of orthopedic implants for bone tissue engineering. Biomaterials 219, 119366 (2019).
pubmed: 31374482
doi: 10.1016/j.biomaterials.2019.119366
Campoccia, D., Montanaro, L. & Arciola, C. R. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials 34(34), 8533–8554 (2013).
pubmed: 23953781
doi: 10.1016/j.biomaterials.2013.07.089
Drago, L., Toscano, M. & Bottagisio, M. Recent evidence on bioactive glass antimicrobial and antibiofilm activity: A mini-review. Materials (Basel, Switzerland) https://doi.org/10.3390/ma11020326 (2018).
doi: 10.3390/ma11020326
pubmed: 29495292
Hench, L. L. The story of bioglass. J. Mater. Sci. Mater. Med. 17(11), 967–978 (2006).
pubmed: 17122907
doi: 10.1007/s10856-006-0432-z
Clark, L. L. H. A. E. Adhesion to bone. In Biocompatibility of Orthopaedic Implants (ed. Winter, D. F. W. G. D.) 85–105 (CRC Press, 1982).
Jones, J. R. Review of bioactive glass: From Hench to hybrids. Acta Biomater. 9(1), 4457–4486 (2013).
pubmed: 22922331
doi: 10.1016/j.actbio.2012.08.023
Naseri, S. & Nazhat, S. N. Bioactive and soluble glasses for wound-healing applications. In Bioactive Glasses 2nd edn (ed. Ylänen, H.) 381–405 (Woodhead Publishing, 2018).
doi: 10.1016/B978-0-08-100936-9.00019-8
Begum, S., Johnson, W. E., Worthington, T. & Martin, R. A. The influence of pH and fluid dynamics on the antibacterial efficacy of 45S5 bioglass. Biomed. Mater. 11(1), 015006 (2016).
pubmed: 26836582
doi: 10.1088/1748-6041/11/1/015006
Rahaman, M. N., Bal, B. S. & Huang, W. Emerging developments in the use of bioactive glasses for treating infected prosthetic joints. Mater. Sci. Eng. C 41, 224–231 (2014).
doi: 10.1016/j.msec.2014.04.055
Waltimo, T. et al. Fine-tuning of bioactive glass for root canal disinfection. J. Dent. Res. 88(3), 235–238 (2009).
pubmed: 19329456
doi: 10.1177/0022034508330315
Hu, S., Chang, J., Liu, M. Q. & Ning, C. Q. Study on antibacterial effect of 45S5 bioglass(A (R)). J. Mater. Sci. Mater. Med. 20(1), 281–286 (2009).
pubmed: 18763024
doi: 10.1007/s10856-008-3564-5
Thomas, W. E., Trintchina, E., Forero, M., Vogel, V. & Sokurenko, E. V. Bacterial adhesion to target cells enhanced by shear force. Cell 109(7), 913–923 (2002).
pubmed: 12110187
doi: 10.1016/S0092-8674(02)00796-1
Lecuyer, S. et al. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. Biophys. J. 100(2), 341–350 (2011).
pubmed: 21244830
pmcid: 3021681
doi: 10.1016/j.bpj.2010.11.078
Thavornyutikarn, B., Feltis, B., Wright, P. F. A. & Turney, T. W. Effect of pre-treatment of crystallized bioactive glass with cell culture media on structure, degradability, and biocompatibility. Mater. Sci. Eng. C Mater. Biol. Appl. 97, 188–197 (2019).
pubmed: 30678903
doi: 10.1016/j.msec.2018.12.034
Waltimo, T., Brunner, T. J., Vollenweider, M., Stark, W. J. & Zehnder, M. Antimicrobial effect of nanometric bioactive glass 45S5. J. Dent. Res. 86(8), 754–757 (2007).
pubmed: 17652205
doi: 10.1177/154405910708600813
van Gestel, N. A. P. et al. Clinical applications of S53P4 bioactive glass in bone healing and osteomyelitic treatment: A literature review. BioMed Res. Int. https://doi.org/10.1155/2015/684826 (2015).
doi: 10.1155/2015/684826
pubmed: 26504821
pmcid: 4609389
Drago, L. et al. Bioactive glass BAG-S53P4 for the adjunctive treatment of chronic osteomyelitis of the long bones: An in vitroand prospective clinical study. BMC Infect. Dis. 13(1), 1–8 (2013).
doi: 10.1186/1471-2334-13-584
Romanò, C. et al. A comparative study of the use of bioactive glass S53P4 and antibiotic-loaded calcium-based bone substitutes in the treatment of chronic osteomyelitis: A retrospective comparative study. Bone Joint J. 96(6), 845–850 (2014).
pubmed: 24891588
doi: 10.1302/0301-620X.96B6.33014
McAndrew, J., Efrimescu, C., Sheehan, E. & Niall, D. Through the looking glass; bioactive glass S53P4 (BonAlive®) in the treatment of chronic osteomyelitis. Ir. J. Med. Sci. 182(3), 509–511 (2013).
pubmed: 23292733
doi: 10.1007/s11845-012-0895-5
Lindfors, N. et al. Bioactive glass S53P4 as bone graft substitute in treatment of osteomyelitis. Bone 47(2), 212–218 (2010).
pubmed: 20624692
doi: 10.1016/j.bone.2010.05.030
Wheeler, D. L., Eschbach, E. J., Hoellrich, R. G., Montfort, M. J. & Chamberland, D. L. Assessment of resorbable bioactive material for grafting of critical-size cancellous defects. J. Orthop. Res. 18(1), 140–148 (2000).
pubmed: 10716290
doi: 10.1002/jor.1100180120
Alam, F. & Balani, K. Adhesion force of Staphylococcus aureus on various biomaterial surfaces. J. Mech. Behav. Biomed. Mater. 65, 872–880 (2017).
pubmed: 27814559
doi: 10.1016/j.jmbbm.2016.10.009
Brady, R. A., Leid, J. G., Costerton, J. W. & Shirtliff, M. E. Osteomyelitis: Clinical overview and mechanisms of infection persistence. Clin. Microbiol. Newslett. 28(9), 65–72 (2006).
doi: 10.1016/j.clinmicnews.2006.04.001
Rohde, H. et al. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 28(9), 1711–1720 (2007).
pubmed: 17187854
doi: 10.1016/j.biomaterials.2006.11.046
Dubost, J. J. et al. No changes in the distribution of organisms responsible for septic arthritis over a 20 year period. Ann. Rheum. Dis. 61(3), 267 (2002).
pubmed: 11830437
pmcid: 1754020
doi: 10.1136/ard.61.3.267
Mortazavi, V., Nahrkhalaji, M. M., Fathi, M. H., Mousavi, S. B. & Esfahani, B. N. Antibacterial effects of sol-gel-derived bioactive glass nanoparticle on aerobic bacteria. J. Biomed. Mater. Res. Part A 94A(1), 160–168 (2010).
doi: 10.1002/jbm.a.32678
Zhang, D. et al. Antibacterial effects and dissolution behavior of six bioactive glasses. J. Biomed. Mater. Res. Part A 93A(2), 475–483 (2010).
doi: 10.1002/jbm.a.32564
Zhang, D. et al. Comparison of antibacterial effect of three bioactive glasses. In Bioceramics (eds Nakamura, T. et al.) 345–348 (Trans Tech Publications Ltd., 2006).
Gubler, M. et al. Do bioactive glasses convey a disinfecting mechanism beyond a mere increase in pH?. Int. Endod. J. 41(8), 670–678 (2008).
pubmed: 18554188
doi: 10.1111/j.1365-2591.2008.01413.x
Lepparanta, O. et al. Antibacterial effect of bioactive glasses on clinically important anaerobic bacteria in vitro. J. Mater. Sci. Mater. Med. 19(2), 547–551 (2008).
pubmed: 17619981
doi: 10.1007/s10856-007-3018-5
Elsa, M. & Moghanian, A. Comparative study of calcium content on in vitro biological and antibacterial properties of silicon-based bioglass. Int. J. Chem. Mol. Eng. 13(6), 288–295 (2019).
Kline, K. A., Fälker, S., Dahlberg, S., Normark, S. & Henriques-Normark, B. Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5(6), 580–592 (2009).
pubmed: 19527885
doi: 10.1016/j.chom.2009.05.011
Viela, F., Mathelié-Guinlet, M., Viljoen, A. & Dufrêne, Y. F. What makes bacterial pathogens so sticky?. Mol. Microbiol. 113(4), 683–690 (2020).
pubmed: 31916325
doi: 10.1111/mmi.14448
Dufrêne, Y. F., Viljoen, A., Mignolet, J. & Mathelié-Guinlet, M. AFM in cellular and molecular microbiology. Cell Microbiol. 12, e13324 (2021).
Di Martino, P. Bacterial adherence: much more than a bond. AIMS Microbiol. 4(3), 563–566 (2018).
pubmed: 31294233
pmcid: 6604948
doi: 10.3934/microbiol.2018.3.563
Dufrêne, Y. F. & Viljoen, A. Binding strength of gram-positive bacterial adhesins. Front. Microbiol. https://doi.org/10.3389/fmicb.2020.01457 (2020).
doi: 10.3389/fmicb.2020.01457
pubmed: 32670256
pmcid: 7330015
Rojas, E. R. et al. The outer membrane is an essential load-bearing element in gram-negative bacteria. Nature 559(7715), 617–621 (2018).
pubmed: 30022160
pmcid: 6089221
doi: 10.1038/s41586-018-0344-3
Harimawan, A., Rajasekar, A. & Ting, Y. P. Bacteria attachment to surfaces—AFM force spectroscopy and physicochemical analyses. J. Colloid Interface Sci. 364(1), 213–218 (2011).
pubmed: 21889162
doi: 10.1016/j.jcis.2011.08.021
Carniello, V., Peterson, B. W., van der Mei, H. C. & Busscher, H. J. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv. Colloid Interface Sci. 261, 1–14 (2018).
pubmed: 30376953
doi: 10.1016/j.cis.2018.10.005
Dunne, W. M. Jr. Bacterial adhesion: Seen any good biofilms lately?. Clin. Microbiol. Rev. 15(2), 155–166 (2002).
pubmed: 11932228
pmcid: 118072
doi: 10.1128/CMR.15.2.155-166.2002
Kuznetsova, T. G., Starodubtseva, M. N., Yegorenkov, N. I., Chizhik, S. A. & Zhdanov, R. I. Atomic force microscopy probing of cell elasticity. Micron 38(8), 824–833 (2007).
pubmed: 17709250
doi: 10.1016/j.micron.2007.06.011
Dufrêne, Y. F., Martínez-Martín, D., Medalsy, I., Alsteens, D. & Müller, D. J. Multiparametric imaging of biological systems by force–distance curve–based AFM. Nat. Methods 10(9), 847–854 (2013).
pubmed: 23985731
doi: 10.1038/nmeth.2602
Zhang, S. et al. Deciphering single-bacterium adhesion behavior modulated by extracellular electron transfer. Nano Lett. 21(12), 5105–5115 (2021).
pubmed: 34086465
doi: 10.1021/acs.nanolett.1c01062
Mignolet, J. et al. AFM unravels the unique adhesion properties of the caulobacter type IVc pilus nanomachine. Nano Lett. 21(7), 3075–3082 (2021).
pubmed: 33754731
doi: 10.1021/acs.nanolett.1c00215
Ishii, S., Yoshimoto, S. & Hori, K. Single-cell adhesion force mapping of a highly sticky bacterium in liquid. J. Colloid Interface Sci. 606, 628–634 (2022).
pubmed: 34416455
doi: 10.1016/j.jcis.2021.08.039
Mathelié-Guinlet, M. et al. Detrimental impact of silica nanoparticles on the nanomechanical properties of Escherichia coli, studied by AFM. J. Colloid Interface Sci. 529, 53–64 (2018).
pubmed: 29883930
doi: 10.1016/j.jcis.2018.05.098
Sheng, X., Ting, Y. P. & Pehkonen, S. O. Force measurements of bacterial adhesion on metals using a cell probe atomic force microscope. J. Colloid Interface Sci. 310(2), 661–669 (2007).
pubmed: 17321534
doi: 10.1016/j.jcis.2007.01.084
Alsteens, D. et al. Atomic force microscopy-based characterization and design of biointerfaces. Nat. Rev. Mater. 2(5), 17008 (2017).
doi: 10.1038/natrevmats.2017.8
Lo, Y.-S. et al. Specific interactions between biotin and avidin studied by atomic force microscopy using the Poisson statistical analysis method. Langmuir 15(4), 1373–1382 (1999).
doi: 10.1021/la981003g
Chen, Y., Busscher, H. J., van der Mei, H. C. & Norde, W. Statistical analysis of long-and short-range forces involved in bacterial adhesion to substratum surfaces as measured using atomic force microscopy. Appl. Environ. Microbiol. 77(15), 5065–5070 (2011).
pubmed: 21642399
pmcid: 3147456
doi: 10.1128/AEM.00502-11
Li, Q., Becker, T., Zhang, R., Xiao, T. & Sand, W. Investigation on adhesion of Sulfobacillus thermosulfidooxidans via atomic force microscopy equipped with mineral probes. Colloids Surf. B Biointerfaces 173, 639–646 (2019).
pubmed: 30368211
doi: 10.1016/j.colsurfb.2018.10.046
Fan, J. P., Kalia, P., Di Silvio, L. & Huang, J. In vitro response of human osteoblasts to multi-step sol–gel derived bioactive glass nanoparticles for bone tissue engineering. Mater. Sci. Eng. C 36, 206–214 (2014).
doi: 10.1016/j.msec.2013.12.009
Noeiaghaei, T., Dhami, N. & Mukherjee, A. Nanoparticles surface treatment on cemented materials for inhibition of bacterial growth. Constr. Build. Mater. 150, 880–891 (2017).
doi: 10.1016/j.conbuildmat.2017.06.046
Goss, J. W. & Volle, C. B. Using atomic force microscopy to illuminate the biophysical properties of microbes. ACS Appl. Bio Mater. 3(1), 143–155 (2019).
pubmed: 32851362
pmcid: 7447269
doi: 10.1021/acsabm.9b00973
Sepulveda, P., Jones, J. & Hench, L. In vitro dissolution of melt-derived 45S5 and sol-gel derived 58S bioactive glasses. J. Biomed. Mater. Res. Off. J. Soc. Biomater. Jpn. Soc. Biomater. Aust. Soc. Biomater. Korean Soc. Biomaterials 61(2), 301–311 (2002).
Bos, R., Van der Mei, H. C. & Busscher, H. J. Physico-chemistry of initial microbial adhesive interactions—Its mechanisms and methods for study. FEMS Microbiol. Rev. 23(2), 179–230 (1999).
pubmed: 10234844
doi: 10.1016/S0168-6445(99)00004-2
Chang, A. C. & Liu, B. H. Identification of characteristic macromolecules of Escherichia coli genotypes by atomic force microscope nanoscale mechanical mapping. Nanoscale Res. Lett. 13(1), 1–6 (2018).
doi: 10.1186/s11671-018-2452-2
Bruker Peak force QNM user guide, 2011.
Spengler, C. et al. The adhesion capability of S aureus cells is heterogeneously distributed over the cell envelope. bioRxiv 121, 1 (2021).
Katsikogianni, M. & Missirlis, Y. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur. Cell Mater. 8(3), 37–57 (2004).
pubmed: 15593018
doi: 10.22203/eCM.v008a05
Alsteens, D. et al. Atomic force microscopy-based characterization and design of biointerfaces. Nat. Rev. Mater. 2(5), 1–16 (2017).
doi: 10.1038/natrevmats.2017.8
Berne, C., Ellison, C. K., Ducret, A. & Brun, Y. V. Bacterial adhesion at the single-cell level. Nat. Rev. Microbiol. 16(10), 616–627 (2018).
pubmed: 30008468
doi: 10.1038/s41579-018-0057-5