Ultrasonically enhanced rifampin activity against internalized Staphylococcus aureus

Shi,Si-Feng; Zhang,Xian-Long; Zhu,Chen; Chen,De-Sheng; Guo,Yong-Yuan

doi:10.3892/etm.2012.758

Ultrasonically enhanced rifampin activity against internalized Staphylococcus aureus

Authors:
- Si-Feng Shi
- Xian-Long Zhang
- Chen Zhu
- De-Sheng Chen
- Yong-Yuan Guo
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Affiliations: Department of Orthopaedic Surgery, Shanghai Sixth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200233, P.R. China
Published online on: October 22, 2012 https://doi.org/10.3892/etm.2012.758
Pages: 257-262

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Abstract

Staphylococcus aureus (S. aureus) is the principle causative agent of osteomyelitis, accounting for 80% of all human cases. S. aureus internalized in osteoblasts escapes immune response, including engulfment by phagocytes. It also escapes the action of a number of antibiotics. Ultrasound increases cell membrane permeability to a number of drugs. Following an internalization assay, we used low-frequency, low-power ultrasound combined with the antibiotic rifampin to target S. aureus internalized in human osteoblasts. Tryptic soy agar (TSA) was used to quantitate the antibacterial effect of rifampin combined with low-frequency ultrasound. A Cell Counting Kit-8 (CCK-8) assay was used to evaluate cell viability following exposure to ultrasound. Our data revealed that rifampin successfully penetrates into osteoblasts and kills internalized S. aureus in osteoblasts, while low-frequency ultrasound promotes this process. Ultrasound had a negative impact on the cell viability of osteoblasts; however, this damage was slight and reversible. Ultrasound-enhanced antibiotic efficiency to bacteria internalized in the osteoblasts may contribute to the control of chronic infection to reduce recurrence.

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1	Ellington JK, Harris M, Webb L, et al: Intracellular Staphylococcus aureus. A mechanism for the indolence of osteomyelitis. J Bone Joint Surg Br. 85:918–921. 2003.
2	Wright JA and Nair SP: Interaction of staphylococci with bone. Int J Med Microbiol. 300:193–204. 2010. View Article : Google Scholar : PubMed/NCBI
3	Ellington JK, Harris M, Hudson MC, Vishin S, Webb LX and Sherertz R: Intracellular Staphylococcus aureus and antibiotic resistance: implications for treatment of staphylococcal osteomyelitis. J Orthop Res. 24:87–93. 2006.PubMed/NCBI
4	Ning R, Zhang X, Guo X and Li Q: Attachment of Staphylococcus aureus is required for activation of nuclear factor kappa B in human osteoblasts. Acta Biochim Biophys Sin. 42:883–892. 2010.
5	Chihara S and Segreti J: Osteomyelitis. Disease-a-Month. 56:6–31. 2010. View Article : Google Scholar
6	Ishida I, Kohda C, Yanagawa Y, Miyaoka H and Shimamura T: Epigallocatechin gallate suppresses expression of receptor activator of NF-kappaB ligand (RANKL) in Staphylococcus aureus infection in osteoblast-like NRG cells. J Med Microbiol. 56:1042–1046. 2007. View Article : Google Scholar : PubMed/NCBI
7	Jin C and Flavell RA: Molecular mechanism of NLRP3 inflammasome activation. J Clin Immunol. 30:628–631. 2010. View Article : Google Scholar : PubMed/NCBI
8	Chauhan VS and Marriott I: Differential roles for NOD2 in osteoblast inflammatory immune responses to bacterial pathogens of bone tissue. J Med Microbiol. 59:755–762. 2010. View Article : Google Scholar : PubMed/NCBI
9	Webb LX, Wagner W, Carroll D, Tyler H, Coldren F and Martin E: Osteomyelitis and intraosteoblastic Staphylococcus aureus. J Surg Orthop Adv. 16:73–78. 2007.
10	Reilly SS: In vivo internalization of Staphylococcus aureus by embryonic chick osteoblasts. Bone. 26:63–70. 2000.
11	Shi S and Zhang X: Interaction of Staphylococcus aureus with osteoblasts (Review). Exp Ther Med. 3:367–370. 2012.
12	Lefebvre M, Jacqueline C, Amador G, et al: Efficacy of daptomycin combined with rifampicin for the treatment of experimental meticillin-resistant Staphylococcus aureus (MRSA) acute osteomyelitis. Int J Antimicrob Agents. 36:542–544. 2010. View Article : Google Scholar : PubMed/NCBI
13	Khanlari B, Elzi L, Estermann L, et al: A rifampicin-containing antibiotic treatment improves outcome of staphylococcal deep sternal wound infections. J Antimicrob Chemother. 65:1799–1806. 2010. View Article : Google Scholar
14	Garrigos C, Murillo O, Euba G, et al: Efficacy of usual and high doses of daptomycin in combination with rifampin versus alternative therapies in experimental foreign-body infection by methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 54:5251–5256. 2010. View Article : Google Scholar : PubMed/NCBI
15	El Helou OC, Berbari EF, Lahr BD, et al: Efficacy and safety of rifampin containing regimen for staphylococcal prosthetic joint infections treated with debridement and retention. Eur J Clin Microbiol Infect Dis. 29:961–967. 2010.PubMed/NCBI
16	Rediske AM, Hymas WC, Wilkinson R and Pitt WG: Ultrasonic enhancement of antibiotic action on several species of bacteria. J Gen Appl Microbiol. 44:283–288. 1998. View Article : Google Scholar : PubMed/NCBI
17	Carmen JC, Roeder BL, Nelson JL, et al: Ultrasonically enhanced vancomycin activity against Staphylococcus epidermidis biofilms in vivo. J Biomater Appl. 18:237–245. 2004. View Article : Google Scholar : PubMed/NCBI
18	Carmen JC, Nelson JL, Beckstead BL, et al: Ultrasonic-enhanced gentamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. J Infect Chemother. 10:193–199. 2004. View Article : Google Scholar : PubMed/NCBI
19	Runyan CM, Carmen JC, Beckstead BL, Nelson JL, Robison RA and Pitt WG: Low-frequency ultrasound increases outer membrane permeability of Pseudomonas aeruginosa. J Gen Appl Microbiol. 25:295–301. 2006. View Article : Google Scholar : PubMed/NCBI
20	Wang L, Wang ZH, Shen CY, You ML, Xiao JF and Chen GQ: Differentiation of human bone marrow mesenchymal stem cells grown in terpolyesters of 3-hydroxyalkanoates scaffolds into nerve cells. Biomaterials. 31:1691–1698. 2010. View Article : Google Scholar : PubMed/NCBI
21	Williams RG and Pitt WG: In vitro response of Escherichia coli to antibiotics and ultrasound at various insonation intensities. J Biomater Appl. 12:20–30. 1997.
22	Rediske AM, Roeder BL, Brown MK, et al: Ultrasonic enhancement of antibiotic action on Escherichia coli biofilms: an in vivo model. Antimicrob Agents Chemother. 43:1211–1214. 1999.
23	Carmen JC, Roeder BL, Nelson JL, et al: Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. Am J Infect Control. 33:78–82. 2005. View Article : Google Scholar : PubMed/NCBI
24	Rapoport N, Smirnov AI, Timoshin A, Pratt AM and Pitt WG: Factors affecting the permeability of Pseudomonas aeruginosa cell walls toward lipophilic compounds: effects of ultrasound and cell age. Arch Biochem Biophys. 344:114–124. 1997.PubMed/NCBI
25	Rediske AM, Rapoport N and Pitt WG: Reducing bacterial resistance to antibiotics with ultrasound. Lett Appl Microbiol. 28:81–84. 1999. View Article : Google Scholar : PubMed/NCBI
26	Mitragotri S, Blankschtein D and Langer R: Transdermal drug delivery using low-frequency sonophoresis. Pharm Res. 13:411–420. 1996. View Article : Google Scholar : PubMed/NCBI
27	Wyber JA, Andrews J and D’Emanuele A: The use of sonication for the efficient delivery of plasmid DNA into cells. Pharm Res. 14:750–756. 1997. View Article : Google Scholar : PubMed/NCBI
28	Tachibana K, Uchida T, Tamura K, Eguchi H, Yamashita N and Ogawa K: Enhanced cytotoxic effect of Ara-C by low intensity ultrasound to HL-60 cells. Cancer Lett. 149:189–194. 2000. View Article : Google Scholar : PubMed/NCBI
29	Li YS, Reid CN and McHale AP: Enhancing ultrasound-mediated cell membrane permeabilisation (sonoporation) using a high frequency pulse regime and implications for ultrasound-aided cancer chemotherapy. Cancer Lett. 266:156–162. 2008. View Article : Google Scholar
30	Iwanaga K, Tominaga K, Yamamoto K, et al: Local delivery system of cytotoxic agents to tumors by focused sonoporation. Cancer Gene Ther. 14:354–363. 2007. View Article : Google Scholar : PubMed/NCBI
31	Kinoshita M and Hynynen K: Key factors that affect sonoporation efficiency in in vitro settings: the importance of standing wave in sonoporation. Biochem Biophys Res Commun. 359:860–865. 2007. View Article : Google Scholar : PubMed/NCBI
32	Mehier-Humbert S, Bettinger T, Yan F and Guy RH: Plasma membrane poration induced by ultrasound exposure: implication for drug delivery. J Control Release. 104:213–222. 2005. View Article : Google Scholar : PubMed/NCBI
33	Qian Z, Sagers RD and Pitt WG: Investigation of the mechanism of the bioacoustic effect. J Biomed Mater Res. 44:198–205. 1999. View Article : Google Scholar : PubMed/NCBI
34	Liu J, Lewis TN and Prausnitz MR: Non-invasive assessment and control of ultrasound-mediated membrane permeabilization. Pharm Res. 15:918–924. 1998. View Article : Google Scholar : PubMed/NCBI
35	Ananta E, Voigt D, Zenker M, Heinz V and Knorr D: Cellular injuries upon exposure of Escherichia coli and Lactobacillus rhamnosus to high-intensity ultrasound. J Appl Microbiol. 99:271–278. 2005.PubMed/NCBI
36	Saito K, Miyake K, McNeil PL, Kato K, Yago K and Sugai N: Plasma membrane disruption underlies injury of the corneal endothelium by ultrasound. Exp Eye Res. 68:431–437. 1999. View Article : Google Scholar : PubMed/NCBI
37	Guzman HR, McNamara AJ, Nguyen DX and Prausnitz MR: Bioeffects caused by changes in acoustic cavitation bubble density and cell concentration: a unified explanation based on cell-to-bubble ratio and blast radius. Ultrasound Med Biol. 29:1211–1222. 2003. View Article : Google Scholar
38	Pitt WG and Ross SA: Ultrasound increases the rate of bacterial cell growth. Biotechnol Prog. 19:1038–1044. 2003. View Article : Google Scholar : PubMed/NCBI
39	Gracewski SM, Miao H and Dalecki D: Ultrasonic excitation of a bubble near a rigid or deformable sphere: implications for ultrasonically induced hemolysis. J Acoust Soc Am. 117:1440–1447. 2005. View Article : Google Scholar : PubMed/NCBI
40	Huber PE and Pfisterer P: In vitro and in vivo transfection of plasmid DNA in the Dunning prostate tumor R3327-AT1 is enhanced by focused ultrasound. Gene Ther. 7:1516–1525. 2000. View Article : Google Scholar : PubMed/NCBI
41	Chang DC: Structure and dynamics of electric field-induced membrane pores as revealed by rapid-freezing electron microscopy. Guide to Electroporation and Electrofusion. Academic Press, Inc; San Diego: pp. 9–27. 1992
42	Lee EK, Gallagher RJ, Campbell AM and Prausnitz MR: Prediction of ultrasound-mediated disruption of cell membranes using machine learning techniques and statistical analysis of acoustic spectra. IEEE Trans Biomed Eng. 51:82–89. 2004. View Article : Google Scholar : PubMed/NCBI
43	Guzman HR, Nguyen DX, Khan S and Prausnitz MR: Ultrasound-mediated disruption of cell membranes. II. Heterogeneous effects on cells. J Acoust Soc Am. 110:597–606. 2001. View Article : Google Scholar : PubMed/NCBI
44	Guzman HR, Nguyen DX, Khan S and Prausnitz MR: Ultrasound-mediated disruption of cell membranes. I. Quantification of molecular uptake and cell viability. J Acoust Soc Am. 110:588–596. 2001. View Article : Google Scholar : PubMed/NCBI