Suppression of Staphylococcus aureus biofilm formation under a short-term impact of low-intensity direct current in vitro and in a rat model of implant-associated osteomyelitis

Document Type : Original Article

Authors

1 Experimental Laboratory, National Ilizarov Medical Research Centre for Traumatology and Ortopaedics, Kurgan, Russia

2 Laboratory of Morphology, National Ilizarov Medical Research Centre for Traumatology and Ortopaedics, Kurgan, Russia

3 Department of preclinical and laboratory research, National Ilizarov Medical Research Centre for Traumatology and Ortopaedics, Kurgan, Russia

Abstract

Objective(s): We investigated the effect of short-term low-intensity direct current (LIDC) on Staphylococcus aureus.
Materials and Methods: The reference strain of S. aureus was used. Experiments were performed in agar culture and on a model of rat’s femur osteomyelitis. K-wires were used as electrodes. The exposure to LIDC of 150 μA continued for one minute. In vitro exposure was performed once. In vivo group 1 was a control group. Osteomyelitis was modeled in three groups but only groups 3 and 4 were exposed to LIDC four times: either from day 1 or from day 7 post-surgery. The effect was evaluated on day 21. Microbiological, histological, scanning electron, and light microscopy methods were used for evaluation of  the LIDC effect. 
Results: Bacteria diameter, oblongness, and division increased 15 min after LIDC exposure in the culture around the cathode. After 24 hr, the amount of exomatrix was lower than in the control test, and the cell diameter and roundness increased. Similar changes around the anode were less pronounced. In vivo, biofilm formation on the intramedullary wire cathode was suppressed in group 3. In group 4, detachment and destruction of the biofilm were observed. The formation of S. aureus microcolonies was suppressed, and the adhesion of fibroblasts and immune cells was activated. LIDC did not stop the development of the osteomyelitis process.
Conclusion: Short-term exposure to LIDC suppresses S. aureus biofilm formation on the implant cathode surface in the acute and early postoperative period but does not have an impact on the development of osteomyelitis.

Keywords

Main Subjects

References

1. Huang K, Lin B, Liu Y, Ren H, Guo Q. Correlation analysis between chronic osteomyelitis and bacterial biofilm. Stem Cells Int 2022;2022:9433847-2022:9433854.
2. Tryapichnikov AS, Ermakov AM, Silantieva TA, Burtsev AV. Efficiency of surgical debridement and implant retaining in treatment of early postoperative and acute hematogenous periprosthetic infections of hip. Travmatologiya I Ortopediya Rossii 2021;27:23-33.
3. van der Borden AJ, van der Mei HC, Busscher HJ. Electric-current-induced detachment of Staphylococcus epidermidis strains from surgical stainless steel. J Biomed Mater Res B Appl Biomater 2004;68:160-164.
4. Gayuk VD, Kliushin NM, Burnashov SI. Pin site soft tissue infection and osteomyelitis: literature review. Genij Ortopedii 2019;25:407-412.
5. van der Borden AJ, Maathuis PG, Engels E, Rakhorst G, van der Mei HC, Busscher HJ et al. Prevention of pin tract infection in external stainless steel fixator frames using electric current in a goat model. Biomaterials 2007;28:2122-2126. 
6. Mirani ZA, Urooj S, Khan MN, Khan AB, Shaikh IA, Siddiqui A. An effective weapon against biofilm consortia and small colony variants of MRSA. Iran J Basic Med Sci 2020;23:1494-1498.
7. Lister JL, Horswill AR. Staphylococcus aureus biofilms: Recent developments in biofilm dispersal. Front Cell Infect Microbiol. 2014;4:178-186.
8. Ermakov AM, Silanteva TA, Naumenko ZS, Kliushin NM, Malkova TA, Burtsev A.V. Complex diagnostic study of twenty-nine patients revised for periprosthetic hip joint reinfection and the role of the histological method in detection of osteomyelitis. Genij Ortopedii 2021;27:540-547.
9. KliushinNM, Ermakov AM, Naumenko ZS, Ababkov IuV, Triapichnikov AS, Koiushkov AN. Etiology of acute periprosthetic joint infection and the results of its surgical treatment. Genij Ortopedii 2017;23:417-422.
10. Zalipour M, Sedigh Ebrahim-Saraie H, Sarvari J, Khashei R. Detection of biofilm production capability and icaA/D genes among staphylococci isolates from Shiraz, Iran. Jundishapur J Microbiol 2016;9:e41431-41437.
11. Shivaee A, Sadeghi Kalani B, Talebi M, Darban-Sarokhalil D. Does biofilm formation have different pathways in Staphylococcus aureus? Iran J Basic Med Sci 2019;22:1147-1152.
12. Haghi Ghahremanloi Olia A, Ghahremani M, Ahmadi A, Sharifi Y. Comparison of biofilm production and virulence gene distribution among community- and hospital-acquired Staphylococcus aureus isolates from northwestern Iran. Infect Genet Evol. 2020;81:104262.
13. Schmidt-Malan SM, Brinkman CL, Greenwood-Quaintance KE, Karau MJ, Mandrekar JN, Patel R. Activity of fixed direct electrical current in experimental Staphylococcus aureus foreign-body osteomyelitis. Diagn Microbiol Infect Dis 2019;93:92-95.
14. Fahmide F, Ehsani P, Atyabi SM. Time-dependent behavior of the Staphylococcus aureus biofilm following exposure to cold atmospheric pressure plasma. Iran J Basic Med Sci 2021;24:744-751.
15. Sedarat Z, Taylor-Robinson AW. Biofilm formation by pathogenic bacteria: Applying a Staphylococcus aureus model to appraise potential targets for therapeutic intervention. Pathogens 2022;11:388-408.
16. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev 2015;28:603-661.
17. Ovchinnikov EN, Godovykh NV, Dyuryagina OV, Stogov MV. Antimicrobial efficacy of exposure of medical metal implants to direct electric current. Biomed Eng 2022;55:323–327.
18. del Pozo JL, Rouse MS, Mandrekar JN, Steckelberg JM, Patel R. The electricidal effect: Reduction of Staphylococcus and pseudomonas biofilms by prolonged exposure to low-intensity electrical current. Antimicrob Agents Chemother 2009;53:41-45.
19. Ovchinnikov EN, Dyuryagina OV, Stogov MV, Silanteva TA, Kireeva EA. Model of osteomyelitis in rats. Bull Exp Biol Med 2022;173:394-397.
20. Silant’eva TA, Gorbach EN, Ir’janov JuM, Stupina TA, Vorsegova TN. Method of preparing biological tissue samples for analysis in scanning electron microscope. Patent RF 2397472. 2010:5. https://pubchem.ncbi.nlm.nih.gov/patent/RU-2397472-C1#section=Full-Text.
21. Naumenko ZS Ocheretina RJu. Method to prepare samples of microorganisms biofilms for survey in scanning electronic microscope. Patent RF 2484446, 2013:6. https://pubchem.ncbi.nlm.nih.gov/patent/RU-2484446-C1.
22. Hryhorovskyi V. Aspects of pathomorphology and nomenclature in the modern classification of nonspecific osteomyelitis. Orthopaedics Traumatology and Prosthetics 2013; 3: 77-87
23. Sybenga AB, Jupiter DC, Speights VO, Rao A. Diagnosing osteomyelitis: A histology guide for pathologists. J Foot Ankle Surg 2020;59:75-85.
24. Tiemann A, Hofmann GO, Krukemeyer MG, Krenn V, Langwald S. Histopathological osteomyelitis evaluation score (HOES) - an innovative approach to histopathological diagnostics and scoring of osteomyelitis. GMS Interdiscip Plast Reconstr Surg DGPW 2014;3:1-12.
25. Boudjemaa R, Steenkeste K, Canette A, Briandet R, Fontaine-Aupart MP, Marlière C. Direct observation of the cell-wall remodeling in adhering Staphylococcus aureus 27217: An AFM study supported by SEM and TEM. Cell Surf 2019;5:100018-100026.
26. Andryukov BG, Timchenko NF, Lyapun IN, Bynina MP, Matosova EV. Heterogeneity in isogenic bacteria populations and modern technologies of cell phenotyping. J Microbiol Epidemiol Immunobiol 2021;98:73-83.
27. Monteiro JM, Fernandes PB, Vaz F, Pereira AR, Tavares AC, Ferreira MT et al. Cell shape dynamics during the staphylococcal cell cycle. Nat Commun 2015;6:8055-8066.
28. Szafrańska AK, Junker V, Steglich M, Nübel U. Rapid cell division of Staphylococcus aureus during colonization of the human nose. BMC Genomics 2019;20:229-241.
29. Amalou H, Negussie AH, Ranjan A, Chow L, Xu S, Kroeger C et al. Electrically conductive catheter inhibits bacterial colonization. J Vasc Interv Radiol 2014;25:797-802.
30. Liu WK, Brown MR, Elliott TS. Mechanisms of the bactericidal activity of low amperage electric current (DC). J Antimicrob Chemother 1997;39:687-95.
31. Wang H, Ren D. Controlling Streptococcus mutans and Staphylococcus aureus biofilms with direct current and chlorhexidine. AMB Express 2017;7:204-212.
32. Zhang J, Neoh KG, Hu X, Kang ET. Mechanistic insights into response of Staphylococcus aureus to bioelectric effect on polypyrrole/chitosan film. Biomaterials 2014;35:7690-7698.
33. Voegele P, Badiola J, Schmidt-Malan SM, Karau MJ, Greenwood-Quaintance KE, Mandrekar JN et al. Antibiofilm activity of electrical current in a catheter model. Antimicrob Agents Chemother 2015;60:1476-1480.
34. Ruiz-Ruigomez M, Badiola J, Schmidt-Malan SM, Greenwood-Quaintance K, Karau MJ, Brinkman CL et al. Direct electrical current reduces bacterial and yeast biofilm formation. Int J Bacteriol 2016;2016:9727810-9727815.
35. Merriman HL, Hegyi CA, Albright-Overton CR, Carlos J Jr, Putnam RW, Mulcare JA. A comparison of four electrical stimulation types on Staphylococcus aureus growth in vitro. J Rehabil Res Dev 2004;41:139-146.
36. del Pozo JL, Rouse MS, Mandrekar JN, Sampedro MF, Steckelberg JM, Patel R. Effect of electrical current on the activities of antimicrobial agents against Pseudomonas aeruginosa, Staphylococcus aureus, and Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 2009;53:35-40.
37. Ehrensberger MT, Tobias ME, Nodzo SR, Hansen LA, Luke-Marshall NR, Cole RF et al. Cathodic voltage-controlled electrical stimulation of titanium implants as treatment for methicillin-resistant Staphylococcus aureus periprosthetic infections. Biomaterials 2015;41:97-105.
38. Minkiewicz-Zochniak A, Strom K, Jarzynka S, Iwańczyk B, Koryszewska-Bagińska A, Olędzka G. Effect of low amperage electric current on Staphylococcus aureus-strategy for combating bacterial biofilms formation on dental implants in cystic fibrosis patients, in vitro study. Materials (Basel) 2021;14:6117-6133.
39. Ovchinnikov EN, Stogov MV. Stimulation of osteogenesis by direct electric current (Review). Travmatologiya I Ortopediya Rossii 2019;25:185-191.
40. Nicksic PJ, Donnelly DT, Hesse M, Bedi S, Verma N, Seitz AJ et al. Electronic bone growth stimulators for augmentation of osteogenesis in in vitro and in vivo models: A narrative review of electrical stimulation mechanisms and device specifications. Front Bioeng Biotechnol 2022;10:793945-793961.
41. Balakatounis KC, Angoules AG. Low-intensity electrical stimulation in wound healing: Review of the efficacy of externally applied currents resembling the current of injury. Eplasty 2008;8:e28-36.
Iranian Journal of Basic Medical Sciences
Volume 27, Issue 2
February 2024
Pages 247-255

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