Advertisement

Targeting Biofilms in Orthopedic Infection

  • Karan Goswami
  • Javad Parvizi
Chapter

Abstract

While the use of orthopedic implants has transformed the treatment of chronic musculoskeletal diseases such as osteoarthritis, the introduction of foreign materials increases the ability of microbes to cause infection more than 100,000-fold (Elek, Annals of the New York Academy of Sciences. 65:85–90, 1956; Parvizi et al. J Am Acad Orthop Surg. 23:S32-43, 2015). Even when implants are successfully placed without infection, their continued presence predisposes patients to infection years after implantation. The annual cost of infected revision total joint arthroplasty to US hospitals, an example of one of the most common device-associated infections, is projected to exceed $1.62 billion by the year 2020 (Kurtz et al. J Arthroplasty. 27:61–65.e1, 2012). Treatment of prosthesis-associated infections is complex as implants serve as a surface for microbial growth into a resistant biofilm layer. This biofilm layer makes bacteria more difficult to eradicate, facilitates host immune evasion, propagates antimicrobial resistance, and reduces the efficacy of standard antibiotic therapy. Over recent years, numerous strategies have been investigated to prevent, target, and disrupt biofilm on orthopedic implants. We describe the main modes of biofilm-disrupting technology pertinent to orthopedics that have been examined over the last decade – including biofilm localization techniques, implant material modification, bioactive antibacterial coatings, vaccines, bacteriophages, electrical stimulation, and inhibition of quorum sensing. Of note, the success of these novel antibiofilm approaches is currently largely limited to the preclinical setting or early clinical stages. Collaborative efforts between industry, academia, and regulatory authorities are required to fuel translation of this innovation into the clinical arena and ultimately lead to improved patient outcomes.

Keywords

Orthopedic Implants Biofilm Translational research Therapies Development Testing 

References

  1. 1.
    Elek, S. D. (1956). Experimental staphylococcal infections in the skin of man. Annals of the New York Academy of Sciences, 65, 85–90.CrossRefGoogle Scholar
  2. 2.
    Parvizi, J., Alijanipour, P., Barberi, E. F., Hickok, N. J., Phillips, K. S., Shapiro, I. M., et al. (2015). Novel developments in the prevention, diagnosis, and treatment of periprosthetic joint infections. The Journal of the American Academy of Orthopaedic Surgeons, 23(Suppl), S32–S43.CrossRefGoogle Scholar
  3. 3.
    Kurtz, S. M., Lau, E., Watson, H., Schmier, J. K., & Parvizi, J. (2012). Economic burden of periprosthetic joint infection in the United States. The Journal of Arthroplasty, 27, 61–65.e1.CrossRefGoogle Scholar
  4. 4.
    Urish, K. L., DeMuth, P. W., Kwan, B. W., Craft, D. W., Ma, D., Haider, H., et al. (2016). Antibiotic-tolerant Staphylococcus aureus biofilm persists on arthroplasty materials. Clinical Orthopaedics and Related Research, 474, 1649–1656.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Ma, D., Shanks, R. M. Q., Davis, C. M., Craft, D. W., Wood, T. K., Hamlin, B. R., et al. (2017). Viable bacteria persist on antibiotic spacers following two-stage revision for periprosthetic joint infection. Journal of Orthopaedic Research, 36, 452–458.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Tzeng, A., Tzeng, T. H., Vasdev, S., Korth, K., Healey, T., Parvizi, J., et al. (2015). Treating periprosthetic joint infections as biofilms: Key diagnosis and management strategies. Diagnostic Microbiology and Infectious Disease, 81, 192–200.CrossRefGoogle Scholar
  7. 7.
    Gbejuade, H. O., Lovering, A. M., & Webb, J. C. (2015). The role of microbial biofilms in prosthetic joint infections. Acta Orthopaedica, 86, 147–158.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Tande, A. J., & Patel, R. (2014). Prosthetic joint infection. Clinical Microbiology Reviews, 27, 302–345.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995). Microbial biofilms. Annual Review of Microbiology, 49, 711–745.CrossRefGoogle Scholar
  10. 10.
    Zimmerli, W., Trampuz, A., & Ochsner, P. E. (2004). Prosthetic-joint infections. The New England Journal of Medicine, 351, 1645–1654.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Tan, T. L., Goswami, K., Fillingham, Y. A., Shohat, N., Rondon, A. J., & Parvizi, J. (2018). Defining treatment success after 2-stage exchange arthroplasty for Periprosthetic joint infection. The Journal of Arthroplasty, 33, 3541–3546.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    George, D. A., Gant, V., & Haddad, F. S. (2015). The management of periprosthetic infections in the future. The Bone & Joint Journal, 97-B, 1162–1169.CrossRefGoogle Scholar
  13. 13.
    Duque, A. F., Post, Z. D., Lutz, R. W., Orozco, F. R., Pulido, S. H., & Ong, A. C. (2017). Is there still a role for irrigation and debridement with liner exchange in acute periprosthetic total knee infection? The Journal of Arthroplasty, 32, 1280–1284.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Parry, J. A., Karau, M. J., Kakar, S., Hanssen, A. D., Patel, R., & Abdel, M. P. (2017). Disclosing agents for the intraoperative identification of biofilms on orthopedic implants. The Journal of Arthroplasty, 32, 2501–2504.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Stoodley, P., Kathju, S., Hu, F. Z., Erdos, G., Levenson, J. E., Mehta, N., et al. (2005). Molecular and imaging techniques for bacterial biofilms in joint arthroplasty infections. Clinical Orthopaedics and Related Research, 437, 31–40.CrossRefGoogle Scholar
  16. 16.
    Stoodley, P., Nistico, L., Johnson, S., Lasko, L.-A., Baratz, M., Gahlot, V., et al. (2008). Direct demonstration of viable Staphylococcus aureus biofilms in an infected total joint arthroplasty. A case report. The Journal of Bone and Joint Surgery. American Volume, 90, 1751–1758.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kobayashi, N., Bauer, T. W., Tuohy, M. J., Fujishiro, T., & Procop, G. W. (2007). Brief ultrasonication improves detection of biofilm-formative bacteria around a metal implant. Clinical Orthopaedics and Related Research, 457, 210–213.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Nguyen, L. L., Nelson, C. L., Saccente, M., Smeltzer, M. S., Wassell, D. L., & McLaren, S. G. (2002). Detecting bacterial colonization of implanted orthopaedic devices by ultrasonication. Clinical Orthopaedics and Related Research, 403, 29–37.CrossRefGoogle Scholar
  19. 19.
    Gad, G. F. M., Aziz, A., & Aly Ibrahem, R. (2012). In-vitro adhesion of Staphylococcus spp. to certain orthopedic biomaterials and expression of adhesion genes. Journal of Applied Pharmaceutical Science, 2, 145–149.Google Scholar
  20. 20.
    Lauderdale, K. J., Malone, C. L., Boles, B. R., Morcuende, J., & Horswill, A. R. (2010). Biofilm dispersal of community-associated methicillin-resistant Staphylococcus aureus on orthopedic implant material. Journal of Orthopaedic Research, 28, 55–61.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Sheehan, E., McKenna, J., Mulhall, K. J., Marks, P., & McCormack, D. (2004). Adhesion of Staphylococcus to orthopaedic metals, an in vivo study. Journal of Orthopaedic Research, 22, 39–43.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Walkowiak-Przybyło, M., Klimek, L., Okrój, W., Jakubowski, W., Chwiłka, M., Czajka, A., et al. (2012). Adhesion, activation, and aggregation of blood platelets and biofilm formation on the surfaces of titanium alloys Ti6Al4V and Ti6Al7Nb. Journal of Biomedical Materials Research. Part A, 100, 768–775.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Campoccia, D., Montanaro, L., & Arciola, C. R. (2013). A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials, 34, 8533–8554.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Clement, J. L., & Jarrett, P. S. (1994). Antibacterial silver. Metal Based Drugs, 1, 467–482.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Nair, L. S., & Laurencin, C. T. (2008). Nanofibers and nanoparticles for orthopaedic surgery applications. The Journal of Bone and Joint Surgery. American Volume, 90(Suppl 1), 128–131.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Brennan, S. A., Ní Fhoghlú, C., Devitt, B. M., O’Mahony, F. J., Brabazon, D., & Walsh, A. (2015). Silver nanoparticles and their orthopaedic applications. The Bone & Joint Journal, 97-B, 582–589.CrossRefGoogle Scholar
  27. 27.
    Harrasser, N., Jüssen, S., Banke, I. J., Kmeth, R., von Eisenhart-Rothe, R., Stritzker, B., et al. (2015). Antibacterial efficacy of titanium-containing alloy with silver-nanoparticles enriched diamond-like carbon coatings. AMB Express, 5, 77.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Shimazaki, T., Miyamoto, H., Ando, Y., Noda, I., Yonekura, Y., Kawano, S., et al. (2010). In vivo antibacterial and silver-releasing properties of novel thermal sprayed silver-containing hydroxyapatite coating. Journal of Biomedical Materials Research Part B Applied Biomaterials, 92, 386–389.Google Scholar
  29. 29.
    Hobman, J. L., & Crossman, L. C. (2015). Bacterial antimicrobial metal ion resistance. Journal of Medical Microbiology, 64, 471–497.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Huang, Q., Yu, H.-J., Liu, G.-D., Huang, X.-K., Zhang, L.-Y., Zhou, Y.-G., et al. (2012). Comparison of the effects of human β-defensin 3, vancomycin, and clindamycin on Staphylococcus aureus biofilm formation. Orthopedics, 35, e53–e60.CrossRefGoogle Scholar
  31. 31.
    Zhu, C., Tan, H., Cheng, T., Shen, H., Shao, J., Guo, Y., et al. (2013). Human β-defensin 3 inhibits antibiotic-resistant Staphylococcus biofilm formation. The Journal of Surgical Research, 183, 204–213.CrossRefGoogle Scholar
  32. 32.
    Nablo, B. J., Prichard, H. L., Butler, R. D., Klitzman, B., & Schoenfisch, M. H. (2005). Inhibition of implant-associated infections via nitric oxide release. Biomaterials, 26, 6984–6990.CrossRefGoogle Scholar
  33. 33.
    Hickok, N. J., & Shapiro, I. M. (2012). Immobilized antibiotics to prevent orthopaedic implant infections. Advanced Drug Delivery Reviews, 64, 1165–1176.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lawson, M. C., Bowman, C. N., & Anseth, K. S. (2007). Vancomycin derivative photopolymerized to titanium kills S. epidermidis. Clinical Orthopaedics and Related Research, 461, 96–105.PubMedGoogle Scholar
  35. 35.
    Edin, M. L., Miclau, T., Lester, G. E., Lindsey, R. W., & Dahners, L. E. (1996). Effect of cefazolin and vancomycin on osteoblasts in vitro. Clinical Orthopaedics and Related Research, 333, 245–251.CrossRefGoogle Scholar
  36. 36.
    Parvizi, J., Wickstrom, E., Zeiger, A. R., Adams, C. S., Shapiro, I. M., Purtill, J. J., et al. (2004). Frank Stinchfield Award. Titanium surface with biologic activity against infection. Clinical Orthopaedics and Related Research, 429, 33–38.CrossRefGoogle Scholar
  37. 37.
    Lawson, M. C., Hoth, K. C., Deforest, C. A., Bowman, C. N., & Anseth, K. S. (2010). Inhibition of Staphylococcus epidermidis biofilms using polymerizable vancomycin derivatives. Clinical Orthopaedics and Related Research, 468, 2081–2091.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Hart, E., Azzopardi, K., Taing, H., Graichen, F., Jeffery, J., Mayadunne, R., et al. (2010). Efficacy of antimicrobial polymer coatings in an animal model of bacterial infection associated with foreign body implants. The Journal of Antimicrobial Chemotherapy, 65, 974–980.CrossRefGoogle Scholar
  39. 39.
    Moskowitz, J. S., Blaisse, M. R., Samuel, R. E., Hsu, H.-P., Harris, M. B., Martin, S. D., et al. (2010). The effectiveness of the controlled release of gentamicin from polyelectrolyte multilayers in the treatment of Staphylococcus aureus infection in a rabbit bone model. Biomaterials, 31, 6019–6030.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Ooi, N., Miller, K., Randall, C., Rhys-Williams, W., Love, W., & Chopra, I. (2010). XF-70 and XF-73, novel antibacterial agents active against slow-growing and non-dividing cultures of Staphylococcus aureus including biofilms. The Journal of Antimicrobial Chemotherapy, 65, 72–78.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Sinclair, K. D., Pham, T. X., Farnsworth, R. W., Williams, D. L., Loc-Carrillo, C., Horne, L. A., et al. (2012). Development of a broad spectrum polymer-released antimicrobial coating for the prevention of resistant strain bacterial infections. Journal of Biomedical Materials Research. Part A, 100, 2732–2738.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Stewart, S., Barr, S., Engiles, J., Hickok, N. J., Shapiro, I. M., Richardson, D. W., et al. (2012). Vancomycin-modified implant surface inhibits biofilm formation and supports bone-healing in an infected osteotomy model in sheep: A proof-of-concept study. The Journal of Bone and Joint Surgery. American Volume, 94, 1406–1415.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Romanò, C. L., Toscano, M., Romanò, D., & Drago, L. (2013). Antibiofilm agents and implant-related infections in orthopaedics: Where are we? Journal of Chemotherapy, 25, 67–80.CrossRefGoogle Scholar
  44. 44.
    Secinti, K. D., Özalp, H., Attar, A., & Sargon, M. F. (2011). Nanoparticle silver ion coatings inhibit biofilm formation on titanium implants. Journal of Clinical Neuroscience, 18, 391–395.CrossRefGoogle Scholar
  45. 45.
    Gallo, J., Havranek, V., & Zapletalova, J. (2010). Risk factors for accelerated polyethylene wear and osteolysis in ABG I total hip arthroplasty. International Orthopaedics, 34, 19–26.CrossRefGoogle Scholar
  46. 46.
    Romanò, C. L., Gala, L., Logoluso, N., Romanò, D., & Drago, L. (2012). Two-stage revision of septic knee prosthesis with articulating knee spacers yields better infection eradication rate than one-stage or two-stage revision with static spacers. Knee Surgery, Sports Traumatology, Arthroscopy, 20, 2445–2453.CrossRefGoogle Scholar
  47. 47.
    Ionita, D., Grecu, M., Ungureanu, C., & Demetrescu, I. (2011). Antimicrobial activity of the surface coatings on TiAlZr implant biomaterial. Journal of Bioscience and Bioengineering, 112, 630–634.CrossRefGoogle Scholar
  48. 48.
    Darouiche, R. O. (1999). Anti-infective efficacy of silver-coated medical prostheses. Clinical Infectious Diseases, 29, 1371–1377; quiz 1378.CrossRefGoogle Scholar
  49. 49.
    Slane, J., Vivanco, J., Rose, W., Ploeg, H.-L., & Squire, M. (2015). Mechanical, material, and antimicrobial properties of acrylic bone cement impregnated with silver nanoparticles. Materials Science & Engineering. C, Materials for Biological Applications, 48, 188–196.CrossRefGoogle Scholar
  50. 50.
    Aurore, V., Caldana, F., Blanchard, M., Kharoubi Hess, S., Lannes, N., Mantel, P.-Y., et al. (2018). Silver-nanoparticles increase bactericidal activity and radical oxygen responses against bacterial pathogens in human osteoclasts. Nanomedicine, 14, 601–607.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Qin, H., Cao, H., Zhao, Y., Zhu, C., Cheng, T., Wang, Q., et al. (2014). In vitro and in vivo anti-biofilm effects of silver nanoparticles immobilized on titanium. Biomaterials, 35, 9114–9125.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Kalishwaralal, K., BarathManiKanth, S., Pandian, S. R. K., Deepak, V., & Gurunathan, S. (2010). Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids and Surfaces. B, Biointerfaces, 79, 340–344.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Wang, J., Li, J., Qian, S., Guo, G., Wang, Q., Tang, J., et al. (2016). Antibacterial surface design of titanium-based biomaterials for enhanced bacteria-killing and cell-assisting functions against periprosthetic joint infection. ACS Applied Materials & Interfaces, 8, 11162–11178.CrossRefGoogle Scholar
  54. 54.
    Fayaz, A. M., Balaji, K., Girilal, M., Yadav, R., Kalaichelvan, P. T., & Venketesan, R. (2010). Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: A study against gram-positive and gram-negative bacteria. Nanomedicine, 6, 103–109.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Naqvi, S. Z. H., Kiran, U., Ali, M. I., Jamal, A., Hameed, A., Ahmed, S., et al. (2013). Combined efficacy of biologically synthesized silver nanoparticles and different antibiotics against multidrug-resistant bacteria. International Journal of Nanomedicine, 8, 3187–3195.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Inoue, D., Kabata, T., Ohtani, K., Kajino, Y., Shirai, T., & Tsuchiya, H. (2017). Inhibition of biofilm formation on iodine-supported titanium implants. International Orthopaedics (SICOT), 41, 1093–1099.CrossRefGoogle Scholar
  57. 57.
    Tsuchiya, H., Shirai, T., Nishida, H., Murakami, H., Kabata, T., Yamamoto, N., et al. (2012). Innovative antimicrobial coating of titanium implants with iodine. Journal of Orthopaedic Science, 17, 595–604.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Shirai, T., Watanabe, K., Matsubara, H., Nomura, I., Fujiwara, H., Arai, Y., et al. (2014). Prevention of pin tract infection with iodine-supported titanium pins. Journal of Orthopaedic Science, 19, 598–602.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Kabata, T., Maeda, T., Kajino, Y., Hasegawa, K., Inoue, D., Yamamoto, T., et al. (2015). Iodine-supported hip implants: Short term clinical results. BioMed Research International, 2015, 368124.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Søe, N. H., Jensen, N. V., Jensen, A. L., Koch, J., Poulsen, S. S., Pier, G. B., et al. (2017). Active and passive immunization against Staphylococcus aureus periprosthetic osteomyelitis in rats. In Vivo, 31, 45–50.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Gustin, M.-P., Ohannessian, R., Giard, M., Caillat-Vallet, E., Savey, A., Vanhems, P., et al. (2017). Use of surveillance data to calculate the sample size and the statistical power of randomized clinical trials testing Staphylococcus aureus vaccine efficacy in orthopedic surgery. Vaccine, 35, 6934–6937.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Shinefield, H., Black, S., Fattom, A., Horwith, G., Rasgon, S., Ordonez, J., et al. (2002). Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. The New England Journal of Medicine, 346, 491–496.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Brady, R. A., O’May, G. A., Leid, J. G., Prior, M. L., Costerton, J. W., & Shirtliff, M. E. (2011). Resolution of Staphylococcus aureus biofilm infection using vaccination and antibiotic treatment. Infection and Immunity, 79, 1797–1803.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Levy, J., Licini, L., Haelterman, E., Moris, P., Lestrate, P., Damaso, S., et al. (2015). Safety and immunogenicity of an investigational 4-component Staphylococcus aureus vaccine with or without AS03B adjuvant: Results of a randomized phase I trial. Human Vaccines & Immunotherapeutics, 11, 620–631.CrossRefGoogle Scholar
  65. 65.
    Frenck, R. W., Creech, C. B., Sheldon, E. A., Seiden, D. J., Kankam, M. K., Baber, J., et al. (2017). Safety, tolerability, and immunogenicity of a 4-antigen Staphylococcus aureus vaccine (SA4Ag): Results from a first-in-human randomised, placebo-controlled phase 1/2 study. Vaccine, 35, 375–384.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    de Bruyn, G., Saleh, J., Workman, D., Pollak, R., Elinoff, V., Fraser, N. J., et al. (2016). Defining the optimal formulation and schedule of a candidate toxoid vaccine against Clostridium difficile infection: A randomized Phase 2 clinical trial. Vaccine, 34, 2170–2178.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Döring, G., Meisner, C., Stern, M., & Flagella Vaccine Trial Study Group. (2007). A double-blind randomized placebo-controlled phase III study of a Pseudomonas aeruginosa flagella vaccine in cystic fibrosis patients. Proceedings of the National Academy of Sciences of the United States of America, 104, 11020–11025.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Akanda, Z. Z., Taha, M., & Abdelbary, H. (2018). Current review-The rise of bacteriophage as a unique therapeutic platform in treating peri-prosthetic joint infections. Journal of Orthopaedic Research, 36, 1051–1060.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Chhibber, S., Kaur, T., & null, S. K. (2013). Co-therapy using lytic bacteriophage and linezolid: Effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One, 8, e56022.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Yilmaz, C., Colak, M., Yilmaz, B. C., Ersoz, G., Kutateladze, M., & Gozlugol, M. (2013). Bacteriophage therapy in implant-related infections: An experimental study. The Journal of Bone and Joint Surgery. American Volume, 95, 117–125.CrossRefGoogle Scholar
  71. 71.
    Ferry, T., Leboucher, G., Fevre, C., Herry, Y., Conrad, A., Josse, J., et al. Salvage debridement, antibiotics and implant retention (“DAIR”) with local injection of a selected cocktail of bacteriophages: Is it an option for an elderly patient with relapsing Staphylococcus aureus prosthetic-joint infection? Open Forum Infectious Diseases, 5, ofy269. [Internet]. 2018 [cited 2019 Jan 5]; Available from: http://academic.oup.com/ofid/article/5/11/ofy269/5144083.
  72. 72.
    Gasiunas, G., Sinkunas, T., & Siksnys, V. (2014). Molecular mechanisms of CRISPR-mediated microbial immunity. Cellular and Molecular Life Sciences, 71, 449–465.CrossRefGoogle Scholar
  73. 73.
    Kaplan, J. B., LoVetri, K., Cardona, S. T., Madhyastha, S., Sadovskaya, I., Jabbouri, S., et al. (2012). Recombinant human DNase I decreases biofilm and increases antimicrobial susceptibility in staphylococci. The Journal of Antibiotics, 65, 73–77.CrossRefGoogle Scholar
  74. 74.
    Pavlukhina, S. V., Kaplan, J. B., Xu, L., Chang, W., Yu, X., Madhyastha, S., et al. (2012). Noneluting enzymatic Antibiofilm coatings. ACS Applied Materials & Interfaces, 4, 4708–4716.CrossRefGoogle Scholar
  75. 75.
    Darouiche, R. O., Mansouri, M. D., Gawande, P. V., & Madhyastha, S. (2009). Antimicrobial and antibiofilm efficacy of triclosan and DispersinB combination. The Journal of Antimicrobial Chemotherapy, 64, 88–93.CrossRefGoogle Scholar
  76. 76.
    Ntrouka, V. I., Slot, D. E., Louropoulou, A., & Van der Weijden, F. (2011). The effect of chemotherapeutic agents on contaminated titanium surfaces: A systematic review. Clinical Oral Implants Research, 22, 681–690.CrossRefGoogle Scholar
  77. 77.
    Kizhner, V., Krespi, Y. P., Hall-Stoodley, L., & Stoodley, P. (2011). Laser-generated shockwave for clearing medical device biofilms. Photomedicine and Laser Surgery, 29, 277–282.CrossRefGoogle Scholar
  78. 78.
    Rediske, A. M., Roeder, B. L., Brown, M. K., Nelson, J. L., Robison, R. L., Draper, D. O., et al. (1999). Ultrasonic enhancement of antibiotic action on Escherichia coli biofilms: An in vivo model. Antimicrobial Agents and Chemotherapy, 43, 1211–1214.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Pickering, S. A., Bayston, R., & Scammell, B. E. (2003). Electromagnetic augmentation of antibiotic efficacy in infection of orthopaedic implants. Journal of Bone and Joint Surgery. British Volume (London), 85, 588–593.CrossRefGoogle Scholar
  80. 80.
    Ercan, B., Kummer, K. M., Tarquinio, K. M., & Webster, T. J. (2011). Decreased Staphylococcus aureus biofilm growth on anodized nanotubular titanium and the effect of electrical stimulation. Acta Biomaterialia, 7, 3003–3012.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Ueshima, M., Tanaka, S., Nakamura, S., & Yamashita, K. (2002). Manipulation of bacterial adhesion and proliferation by surface charges of electrically polarized hydroxyapatite. Journal of Biomedical Materials Research, 60, 578–584.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Chatterjee, M., D’Morris, S., Paul, V., Warrier, S., Vasudevan, A. K., Vanuopadath, M., et al. (2017). Mechanistic understanding of Phenyllactic acid mediated inhibition of quorum sensing and biofilm development in Pseudomonas aeruginosa. Applied Microbiology and Biotechnology, 101, 8223–8236.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Cho, Y.-J., Song, H. Y., Ben Amara, H., Choi, B.-K., Eunju, R., Cho, Y.-A., et al. (2016). In vivo inhibition of porphyromonas gingivalis growth and prevention of periodontitis with quorum-sensing inhibitors. Journal of Periodontology, 87, 1075–1082.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Durai, S., Vigneshwari, L., & Balamurugan, K. (2013). Caenorhabditis elegans-based in vivo screening of bioactives from marine sponge-associated bacteria against Vibrio alginolyticus. Journal of Applied Microbiology, 115, 1329–1342.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Husain, F. M., Ahmad, I., Baig, M. H., Khan, M. S., Khan, M. S., Hassan, I., et al. (2016). Broad-spectrum inhibition of AHL-regulated virulence factors and biofilms by sub-inhibitory concentrations of ceftazidime. RSC Advances, 6, 27952–27962.CrossRefGoogle Scholar
  86. 86.
    Ivanova, K., Fernandes, M. M., Francesko, A., Mendoza, E., Guezguez, J., Burnet, M., et al. (2015). Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS Applied Materials & Interfaces, 7, 27066–27077.CrossRefGoogle Scholar
  87. 87.
    Rowley D., Zhao W., Yuan T., Dao C., Sohn S., Gomez Chiarri M., et al. Mechanisms of microbe-microbe-host interactions in a probiont-pathogen-bivalve model. Planta Medica[Internet], 2015; 81. Available from: http://www.embase.com/search/results?subaction=viewrecord&from=export&id=L71958553.
  88. 88.
    Srinivasan, R., Mohankumar, R., Kannappan, A., Karthick Raja, V., Archunan, G., Karutha Pandian, S., et al. (2017). Exploring the anti-quorum sensing and antibiofilm efficacy of phytol against Serratia marcescens associated acute pyelonephritis infection in Wistar rats. Frontiers in Cellular and Infection Microbiology, 7, 498.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Piewngam, P., Zheng, Y., Nguyen, T. H., Dickey, S. W., Joo, H.-S., Villaruz, A. E., et al. (2018). Pathogen elimination by probiotic Bacillus via signalling interference. Nature, 562, 532.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Karan Goswami
    • 1
  • Javad Parvizi
    • 1
  1. 1.Rothman Institute of Orthopedics at Thomas Jefferson UniversityPhiladelphiaUSA

Personalised recommendations