Low-frequency sonication may alter surface topography of endoprosthetic components and damage articular cartilage without eradicating biofilms completely
Gurpal Singh
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
University Orthopaedics, Hand and Reconstructive Microsurgery Cluster, National University Health System, Singapore, Singapore
Search for more papers by this authorRita Hameister
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorBernd Feuerstein
Department of Mechanical Engineering, Magdeburg-Stendal University of Applied Sciences, Magdeburg, Germany
Search for more papers by this authorFriedemann Awiszus
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorHeiko Meyer
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorCorresponding Author
Christoph H. Lohmann
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Correspondence to: C. H. Lohmann (e-mail: [email protected])Search for more papers by this authorGurpal Singh
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
University Orthopaedics, Hand and Reconstructive Microsurgery Cluster, National University Health System, Singapore, Singapore
Search for more papers by this authorRita Hameister
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorBernd Feuerstein
Department of Mechanical Engineering, Magdeburg-Stendal University of Applied Sciences, Magdeburg, Germany
Search for more papers by this authorFriedemann Awiszus
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorHeiko Meyer
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Search for more papers by this authorCorresponding Author
Christoph H. Lohmann
Department of Orthopaedic Surgery, Otto-von-Guericke University, Magdeburg, Germany
Correspondence to: C. H. Lohmann (e-mail: [email protected])Search for more papers by this authorAbstract
Two-stage exchange arthroplasty is the current standard of care for arthroplasty-related infections. Reinfection rates up to 30% are reported, and there is significant morbidity for the patient. In cases of failure, arthrodesis or amputation may result. Ultrasonic treatment has the potential to eradicate biofilms and avoid two-stage exchange arthroplasty. Data in the specific context of arthroplasty infections is scant, and there is debate regarding optimal frequency and intensity of treatment. Surface topography alterations of the endoprosthetic components and damage to adjacent bone and cartilage have not been investigated. We found incomplete biofilm eradication and significant increase in surface roughness (maximum peak-to-valley height) of cobalt-chrome unicondylar knee components as well as reduction in articular cartilage thickness area from 10 retrieved femoral heads after low-frequency sonication treatment according to manufacturer-specified recommendations. Our data collectively suggest that sonication treatment for biofilm eradication in arthroplasty infections may not be effective and surface topography alterations may potentially reduce implant longevity. © 2014 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 102B: 1835–1846, 2014.
REFERENCES
- 1 Bozic KJ, Kurtz SM, Lau E, Ong K, Vail TP, Berry DJ. The epidemiology of revision total hip arthroplasty in the United States. J Bone Joint Surg Am 2009; 91: 128–133.
- 2 Widmer AF. New developments in diagnosis and treatment of infection in orthopedic implants. Clin Infect Dis 2001; 33: S94–106.
- 3 Leone JM, Hanssen AD. Management of infection at the site of a total knee arthroplasty. J Bone Joint Surg Am 2005; 87: 2335–2348.
- 4 Cuckler JM. The infected total knee: Management options. J Arthroplasty 2005; 20: 33–36.
- 5 Haleem AA, Berry DJ, Hanssen AD. Mid-term to long-term followup of two-stage reimplantation for infected total knee arthro plasty. Clin Orthop Relat Res 2004; 428: 35–39.
- 6 Mortazavi SMJ, Vegari D, Ho A, Zmistowski B, Parvizi J. Two-stage exchange arthroplasty for infected total knee arthroplasty: Predictors of failure. Clin Orthop Relat Res 2011; 469: 3049–3054.
- 7 Lentino JR. Prosthetic joint infections: Bane of orthopedists, challenge for infectious disease specialists. Clin Infect Dis 2003; 36: 1157–1161.
- 8 Uçkay I, Pittet D, Vaudaux P, Sax H, Lew D, Waldvogel F. Foreign body infections due to Staphylococcus epidermidis. Ann Med 2009; 41: 109–119.
- 9 Høiby N, Ciofu O, Johansen HK, Song Z, Moser C, Jensen PØ, Molin S, Givskov M, Tolker-Nielsen T, Bjarnsholt T. The clinical impact of bacterial biofilms. Int J Oral Sci 2011; 3: 55–65.
- 10 Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. The Calgary biofilm device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 1999; 37: 1771–1776.
- 11 Barth E, Myrvik QM, Wagner W, Gristina AG. In vitro and in vivo comparative colonization of Staphylococcus aureus and Staphylococcus epidermidis on orthopaedic implant materials. Biomaterials 1989; 10: 325–328.
- 12 Fitzgerald SJ, Hanssen AD. Surgical techniques for staged revision of the chronically infected total knee arthroplasty. Surg Technol Int 2011; XXI: 204–211.
- 13 Cui Q, Mihalko WM, Shields JS, Ries M, Saleh KJ. Antibiotic-impregnated cement spacers for the treatment of infection associated with total hip or knee arthroplasty. J Bone Joint Surg Am 2007; 89: 871–882.
- 14 Vlasak R, Gearen PF, Petty W. Knee arthrodesis in the treatment of failed total knee replacement. Clin Orthop Relat Res 1995; 321: 138–144.
- 15 Butcher GPL. Wound bed preparation: Ultrasonic-assisted debridement. Br J Nurs 2013; 22: S36–S43.
- 16 Breuing KH, Bayer L, Neuwalder J, Orgill DP. Early experience using low-frequency ultrasound in chronic wounds. Ann Plast Surg 2005; 55: 183–187.
- 17 De Paolis G, Vincenti V, Prencipe M, Milana V, Plotino G. Ultrasonics in endodontic surgery: A review of the literature. Ann Stomatol (Roma) 2010; 1: 6–10.
- 18 Oda S, Nitta H, Setoguchi T, Izumi Y, Ishikawa I. Current concepts and advances in manual and power-driven instrumentation. Periodontol 2000 2004; 36: 45–58.
- 19 Greenstein G. Nonsurgical periodontal therapy in 2000: A literature review. J Am Dent Assoc 2000; 131: 1580–1592.
- 20 Bigelow TA, Northagen T, Hill TM, Sailer FC. The destruction of Escherichia coli biofilms using high-intensity focused ultrasound. Ultrasound Med Biol 2009; 35: 1026–1031.
- 21 Ioannou I, Dimitriadis N, Papadimitriou K, Sakellari D, Vouros I, Konstantinidis A. Hand instrumentation versus ultrasonic debridement in the treatment of chronic periodontitis: A randomized clinical and microbiological trial. J Clin Periodontol 2009; 36: 132–141.
- 22 Bigelow TA, Northagen T, Hill TM, Sailer FC. Ultrasound histotripsy and the destruction of Escherichia coli biofilms. Conf Proc IEEE Eng Med Biol Soc 2008; 2008: 4467–4470.
- 23 Walmsley AD, Laird WR, Williams AR. Dental plaque removal by cavitational activity during ultrasonic scaling. J Clin Periodontol 1988; 15: 539–543.
- 24 Oulahal-Lagsir N, Martial-Gros A, Boistier E, Blum LJ, Bonneau M. The development of an ultrasonic apparatus for the noninvasive and repeatable removal of fouling in food processing equipment. Lett Appl Microbiol 2000; 30: 47–52.
- 25 Kirzhner F, Zimmels Y, Malkovskaja A, Starosvetsky J. Removal of microbial biofilm on water hyacinth plants roots by ultrasonic treatment. Ultrasonics 2009; 49: 153–158.
- 26 Patel JD, Ebert M, Ward R, Anderson JM. S. epidermidis biofilm formation: Effects of biomaterial surface chemistry and serum proteins. J Biomed Mater Res Part A 2007; 80: 742–751.
- 27 Arnold JW, Bailey GW. Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: Scanning electron and atomic force microscopy study. Poult Sci 2000; 79: 1839–1845.
- 28 Schoenbach SF, Song IC. Ultasonic debridement: A new approach in the treatment of burn wounds. Plast Reconstr Surg 1980; 66: 34–37.
- 29 Serena T, Lee SK, Lam K, Attar P, Meneses P, Ennis W. The impact of noncontact, nonthermal, low-frequency ultrasound on bacterial counts in experimental and chronic wounds. Ostomy Wound Manage 2009; 55: 22–30.
- 30 Phull SS, Newman AP, Lorimer JP, Pollet B, Mason TJ. The development and evaluation of ultrasound in the biocidal treatment of water. Ultrason Sonochem 1997; 4: 157–164.
- 31 Nishikawa T, Yoshida A, Khanal A, Habu M, Yoshioka I, Toyoshima K, Takehara T, Nishihara T, Tachibana K, Tominaga K. A study of the efficacy of ultrasonic waves in removing biofilms. Gerodontology 2010; 27: 199–206.
- 32 Xu J, Bigelow TA, Halverson LJ, Middendorf JM, Rusk B. Minimization of treatment time for in vitro 1.1 MHz destruction of Pseudomonas aeruginosa biofilms by high-intensity focused ultrasound. Ultrasonics 2012; 52: 668–675.
- 33 Ensing GT, Neut D, van Horn JR, van der Mei HC, Busscher HJ. The combination of ultrasound with antibiotics released from bone cement decreases the viability of planktonic and biofilm bacteria: An in vitro study with clinical strains. J Antimicrob Chemother 2006; 58: 1287–1290.
- 34 Pitt WG, Ross SA. Ultrasound increases the rate of bacterial cell growth. Biotechnol Prog 2003; 19: 1038–1044.
- 35 Pitt WG, McBride MO, Lunceford JK, Roper RJ, Sagers RD. Ultrasonic enhancement of antibiotic action on gram-negative bacteria. Antimicrob Agents Chemother 1994; 38: 2577–2582.
- 36 Qian Z, Stoodley P, Pitt WG. Effect of low-intensity ultrasound upon biofilm structure from confocal scanning laser microscopy observation. Biomaterials 1996; 17: 1975–1980.
- 37 Rediske AM, Roeder BL, Nelson JL, Robison RL, Schaalje GB, Robison RA, Pitt WG. Pulsed ultrasound enhances the killing of Escherichia coli biofilms by aminoglycoside antibiotics in vivo. Antimicrob Agents Chemother 2000; 44: 771–772.
- 38 Peterson R, Pitt WG. The effect of frequency and power density on the ultrasonically-enhanced killing of biofilm-sequestered Escherichia coli. Colloids Surf B 2000; 17: 219–227.
- 39 Carmen JC, Roeder BL, Nelson JL, Beckstead BL, Runyan CM, Schaalje GB, Robison RA, Pitt WG. Ultrasonically enhanced vancomycin activity against Staphylococcus epidermidis biofilms in vivo. J Biomater Appl 2004; 18: 237–245.
- 40 Dong Y, Chen S, Wang Z, Peng N, Yu J. Synergy of ultrasound microbubbles and vancomycin against Staphylococcus epidermidis biofilm. J Antimicrob Chemother 2013; 68: 816–826.
- 41 Nithila SR, Anandkumar B, Vanithakumari S, George R, Mudali UK, Dayal R. Studies to control biofilm formation by coupling ultrasonication of natural waters and anodization of titanium. Ultrason Sonochem 2014; 21: 189–199.
- 42 Torlak E, Sert D. Combined effect of benzalkonium chloride and ultrasound against Listeria monocytogenes biofilm on plastic surface. Lett Appl Microbiol 2013; 57: 220–226.
- 43 Iqbal K, Ohl S, Khoo B, Neo J, Fawzy AS. Effect of High-Intensity Focused Ultrasound on Enterococcus Faecalis Planktonic Suspensions and Biofilms. Ultrasound in Medicine & Biology 2013; 39: 825–833.
- 44 Seth AK, Nguyen KT, Geringer MR, Hong SJ, Leung KP, Mustoe TA, Galiano RD. Noncontact, low-frequency ultrasound as an effective therapy against Pseudomonas aeruginosa-infected biofilm wounds. Wound Repair Regen 2013; 21: 266–274.
- 45 He N, Hu J, Liu H, Zhu T, Huang B, Wang X, Wu Y, Wang W, Qu D. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrob Agents Chemother 2011; 55: 5331–5337.
- 46 Carmen JC, Nelson JL, Beckstead BL, Runyan CM, Robison RA, Schaalje GB, Pitt WG. Ultrasonic-enhanced gentamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. J Infect Chemother 2004; 10: 193-199.
- 47 Carmen JC, Roeder BL, Nelson JL, Ogilvie RLR, Robison RA, Schaalje GB, Pitt WG. Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. Am J Infect Control 2005; 33: 78–82.
- 48 Rediske AM, Rapoport N, Pitt WG. Reducing bacterial resistance to antibiotics with ultrasound. Lett Appl Microbiol 1999; 28: 81–84.
- 49 Rediske AM, Hymas WC, Wilkinson R, Pitt WG. Ultrasonic enhancement of antibiotic action on several species of bacteria. J Gen Appl Microbiol 1998; 44: 283–288.
- 50 Johnson LL, Vaughn Peterson R, Pitt WG. Treatment of bacterial biofilms on polymeric biomaterials using antibiotics and ultrasound. J Biomater Sci Polym Ed 1998; 9: 1177–1185.
- 51 Dowson D, El-Hady Diab MM, Gillis BJ, Atkinson JR. Influence of counterface topography on the wear of ultra high molecular weight polyethylene under wet or dry conditions. conference paper;1985: 171–187.
- 52 McGloughlin TM, Kavanagh AG. Wear of ultra-high molecular weight polyethylene (UHMWPE) in total knee prostheses: A review of key influences. Proc Inst Mech Eng H 2000; 214: 349–359.
- 53 Price GJ, White AJ, Clifton AA. The effect of high-intensity ultrasound on solid polymers. Polymer 1995; 247: 4919–4925.
- 54 Walmsley AD, Williams AR. Measurement of cavitational activity within ultrasonic baths. J Dent 1991; 19: 62–66.
- 55 Cook SD, Salkeld SL, Patron LP, Doughty ES, Jones DG. The effect of low-intensity pulsed ultrasound on autologous osteochondral plugs in a canine model. Am J Sports Med 2008; 36: 1733–1741.
- 56 Huang MH, Ding HJ, Chai CY, Huang YF, Yang RC. Effects of sonication on articular cartilage in experimental osteoarthritis. J Rheumatol 1997; 24: 1978–1984.
- 57 Loyola-Sanchez A, Richardson J, Beattie KA, Otero-Fuentes C, Adachi JD, MacIntyre NJ. Effect of low-intensity pulsed ultrasound on the cartilage repair in people with mild to moderate knee osteoarthritis: A double-blinded, randomized, placebocontrolled pilot study. Arch Phys Med Rehabil 2012; 93: 35–42.
- 58 Watson P, Kernohan WG, Mollan RA. The effect of ultrasonically induced cavitation on articular cartilage. Clin Orthop Relat Res 1989: 288–296.