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Laboratory Biofilm Reactors

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Book cover Formation and Control of Biofilm in Various Environments

Abstract

Biofilms form at the interface between different phases in nature. To investigate biofilms and to solve practical problems, we have to reproduce the phenomena in laboratories. To achieve this purpose, we need to produce biofilms in laboratories and to evaluate them properly and accurately. As for the artificial production of biofilms, we need laboratory biofilm reactors. They have to mimic natural phenomena as much as possible, while the conditions should be idealized without some unnecessary factors. However, the simplification and idealization are very often difficult. It depends on the design and production of the laboratory biofilm reactors. In this chapter, we describe some representative laboratory biofilm reactors and discuss the efficacy and also the problems.

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References

  1. Lewandowski, Z., & Beyenal, H. (2014). Fundamentals of biofilm research (2nd ed.). Boca Raton, London, New York: CRC Press.

    Google Scholar 

  2. Lebeaux, D., Chauhan, A., rendueles, O., & Beloin, C. (2013). From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens, 2, 238–356. https://doi.org/10.3390/pathogens2020288.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Anderl, J. N., Franklin, M. J., & Stewart, P. S. (2000). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrobial Agents and Chemotherapy, 44, 1818–1824.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zuroff, T. R., Bernstein, H., Lloyd-Randolfi, J., Jimenez-Taracido, L., Stewart, P. S., & Carlson, R. P. (2010). Robustness analysis of culturing perturbations on Escherichia coli colony biofilm beta-lactam and aminoglycoside antibiotic tolerance. BMC Microbiology, 10, 185.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M., et al. (1985). Adherence of coagulase-negative Staphylococci to plastic tissue culture plates: A quantitative model for the adherence of Staphylococci to medical devices. Journal of Clinical Microbiology, 22, 996–1006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Genevaux, P., Muller, S., & Bauda, P. (1996). A rapid screening procedure to identify mini-Tn10 insertion mutants of Escherichia coli K-12 with altered adhesion properties. FEMS Microbiology Letters, 142, 27–30.

    Article  CAS  PubMed  Google Scholar 

  7. Chavant, P., Gaillard-Martinie, B., Talon, R., Hébraud, M., & Bernardi, T. (2007). A new device for rapid evaluation of biofilm formation potential by bacteria. Journal of Microbiological Methods, 68, 605–612.

    Article  CAS  PubMed  Google Scholar 

  8. Ceri, H., Olson, M. E., Stremick, C., Read, R. R., Morck, D., & Buret, A. (1999). The Calgary biofilm device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. Journal of Clinical Microbiology, 37, 1771–1776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kanematsu, H., Oizumi, A., Sato, T., Kamijo, T., Honma, S., Barry, D. M., et al. (2018). Biofilm formation of a polymer brush coating with ionic liquids compared to a polymer brush coating with a non-ionic liquid. Coatings, 8(11), 398–412. https://doi.org/10.3390/coatings8110398.

    Article  CAS  Google Scholar 

  10. Kanematsu, H., Oizumi, A., Sato, T., Kamijo, T., Honma, S., Barry, D. M., et al. (2018). Polymer brush made by ionic liquids and the inhibition effects for biofilm formation. ECS Transactions, 85(13), 1089–1095. https://doi.org/10.1149/08513.1089ecst.

    Article  CAS  Google Scholar 

  11. Kanematsu, H., Sakagami, Y., Barry, D. M., Yoshitake, M., Ogawa, A., Hirai, N., et al. (2018). Evaluation for immunity of biomaterials based on Raman spectroscopy. In MS & T 2018. Columbus, Ohio, USA: The minerals, Metals and Materials Society.

    Google Scholar 

  12. Kanematsu, H., Sakagami, Y., Barry, D. M., Yoshitake, M., Ogawa, A., Hirai, N., et al. (2018). Evaluation for immunity of biomaterials based on Raman spectroscopy. Paper presented at the Materials Science and Technology 2018 (MS&T18), greater Columbus Convention Center, Columbus, Ohio, USA.

    Google Scholar 

  13. Kanematsu, H., Shindo, K., Barry, D. M., Hirai, N., Ogawa, A., Kuroda, D., et al. (2018). Electrochemical responses of graphene with biofilm formation on various metallic substrates by using laboratory biofilm reactors. ECS Transactions, 85(13), 491–498. https://doi.org/10.1149/08513.0491ecst.

    Article  CAS  Google Scholar 

  14. De Beer, D., Stoodley, P., Roe, F., & Lewandowski, Z. (1994). Effects of biofilm structures on oxygen distribution and mass transport. Biotechnology and Bioengineering, 43(11), 1131–1138.

    Article  PubMed  Google Scholar 

  15. Stoodley, P., De Beer, D., & Lewandowski, Z. (1994). Liquid flow in biofilm systems. Applied and Environmental Microbiology, 60(8), 2711–2716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Beyenal, H., & Lewandowski, Z. (2001). Mass transport dynamics, activity, and structure of sulfate reducing biofilms. AIChE Journal, 47(7), 1689–1697.

    Article  CAS  Google Scholar 

  17. Beyenal, H., Şleker, Ş., Tanyolaç, A., & Salih, B. (1997). Diffusion coefficients of phenol and oxygen in a biofilm of Pseudomonas putida. AIChE Journal, 43(1), 243–250.

    Article  CAS  Google Scholar 

  18. Beyenal, H., Yakymyshyn, C., Hyungnak, J., Davis, C. C., & Lewandowski, Z. (2004). An optical microsensor to measure fluorescent light intensity in biofilms. Journal of Microbiological Methods, 58(3), 367–374.

    Article  CAS  PubMed  Google Scholar 

  19. Groenenboom, M. D. (2000). Increase of frictional resistance in closed conduit systems fouled with biofilms. Montana State University-Bozeman, College of Engineering.

    Google Scholar 

  20. Lewandowski, Z., Altobelli, S. A., & Fukushima, E. (1993). NMR and microelectrode studies of hydrodynamics and kinetics in biofilms. Biotechnology Progress, 9(1), 40–45.

    Article  CAS  Google Scholar 

  21. Lewandowski, Z., & Beyenal, H. (2003). Mass transfer in heterogeneous biofilms. In S. Wuertz, P. L. Bishop, & P. A. Wilderer (Eds.), Biofilms in wastewater treatment (pp. 145–172). IWA Publishing, London.

    Google Scholar 

  22. Lewandowski, Z., Walser, G., & Characklis, W. G. (1991). Reaction kinetics in biofilms. Biotechnology and Bioengineering, 38(8), 877–882.

    Article  CAS  PubMed  Google Scholar 

  23. Rasmussen, K., & Lewandowski, Z. (1998). The accuracy of oxygen flux measurements using microelectrodes. Water Research, 32(12), 3747–3755.

    Article  CAS  Google Scholar 

  24. Rasmussen, K., & Lewandowski, Z. (1998). Microelectrode measurements of local mass transport rates in heterogeneous biofilms. Biotechnology and Bioengineering, 59(3), 302–309.

    Article  CAS  PubMed  Google Scholar 

  25. Schwartz, K., Stephenson, R., Hernandez, M., Jambang, N., & Boles, B. R. (2010). The use of drip flow and rotating disk reactors for Staphylococcus aureus biofilm analysis. Journal of Visualized Experiments (46), 2470. https://doi.org/10.3791/2470.

  26. Kanematsu, H., Kudara, H., Kanesaki, S., Kogo, T., Ikegai, H., Ogawa, A., et al. (2016). Application of a loop-type laboratory biofilm reactor to the evaluation of biofilm for some metallic materials and polymers such as urinary stents and catheters. Materials, 9(10), 824–834. https://doi.org/10.3390/ma9100824.

    Article  CAS  PubMed Central  Google Scholar 

  27. Kanematsu, H., Kanesaki, S., Kudara, H., Barry, D. M., Ogawa, A., & Mizunoe, Y. (2018). Biofilm formation on titanium alloy surfaces in a laboratory biofilm reactor. In M. M. Mahmoud, K. Sridharan, H. Colorado, A. S. Bhalla, J. P. Singh, S. Gupta, J. Langhorn, A. Jitianu, & N. J. Manjooran (Eds.), Ceramic Transactions—Advances in ceramics for environmental, functional, structural, and energy applications (Vol. 265, pp. 221–228). New York, the United States: Wiley, Inc.

    Google Scholar 

  28. Schaller, M., Schafer, W., Korting, H. C., & Hube, B. (1998). Differential expression of secreted aspartyl proteinases in a model of human oral candidosis and in patient samples from the oral cavity. Molecular Microbiology, 29, 605–615.

    Article  CAS  PubMed  Google Scholar 

  29. Guggenheim, B., Giertsen, E., Schüpbach, P., & Shapiro, S. (2001). Validation of an in vitro biofilm model of supragingival plaque. Journal of Dental Research, 80, 363–370.

    Article  CAS  PubMed  Google Scholar 

  30. Guggenheim, M., Thurnheer, T., Gmur, R., Giovanoli, P., & Guggenheim, B. (2011). Validation of the Zurich burn-biofilm model. Burns: Journal of the International Society for Burn Injuries, 37, 1125–1133.

    Article  Google Scholar 

  31. Grubb, S. E., Murdoch, C., Sudbery, P. E., Saville, S. P., Lopez-Ribot, J. L., & Thornhill, M. H. (2009). Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infection and Immunity, 77, 3872–3878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Woodworth, B. A., Tamashiro, E., Bhargave, G., Cohen, N. A., & Palmer, J. N. (2008). An in vitro model of Pseudomonas aeruginosa biofilms on viable airway epithelial cell monolayers. American Journal of Rhinology, 22, 235–238.

    Article  PubMed  Google Scholar 

  33. McBain, A. J., Sissons, C., Ledder, R. G., Sreenivasan, P. K., De Vizio, W., & Gilbert, P. (2005). Development and characterization of a simple perfused oral microcosm. Journal of Applied Microbiology, 98, 624–634.

    Article  CAS  PubMed  Google Scholar 

  34. Kim, J., Hegde, M., & Jayaraman, A. (2010). Microfluidic co-culture of epithelial cells and bacteria for investigating soluble signal-mediated interactions. Journal of Visualized Experiments, 38, e1749.

    Google Scholar 

  35. Huang, T. Y., Gulabivala, K., & Ng, Y. L. (2008). A bio-molecular film ex vivo model to evaluate the influence of canal dimensions and irrigation variables on the efficacy of irrigation. International Endodontic Journal, 41, 60–71.

    PubMed  Google Scholar 

  36. Chuang-Smith, O. N., Wells, C. L., Henry-Stanley, M. J., & Dunny, G. M. (2010). Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS One, 5, e15798.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Harriott, M. M., Lilly, E. A., Rodriguez, T. E., Fidel, P. L., Jr., & Noverr, M. C. (2010). Candida albicans forms biofilms on the vaginal mucosa. Microbiology, 156, 3635–3644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Carterson, A. J., Honer zu Bentrup, K., Ott, C. M., Clarke, M. S., Pierson, D. L., Vanderburg, C. R., et al. (2005). A549 lung epithelial cells grown as three-dimensional aggregates: Alternative tissue culture model for Pseudomonas aeruginosa pathogenesis. Infection and Immunity, 73, 1129–1140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nickerson, C. A., Goodwin, T. J., Terlonge, J., Ott, C. M., Buchanan, K. L., Uicker, W. C., et al. (2001). Three-dimensional tissue assemblies: Novel models for the study of Salmonella enterica serovar Typhimurium pathogenesis. Infection and Immunity, 69, 7106–7120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Smith, Y. C., Grande, K. K., Rasmussen, S. B., & O’Brien, A. D. (2006). Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infection and Immunity, 74, 750–757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kanematsu, H., Hirai, N., Miura, Y., Itoh, H., Kuroda, D., & Umeki, S. (2013). Biofilm leading to corrosion on material surface and the moderation by alternative electro-magnetic field. Paper presented at the Materials Science and Technology (MS & T), Montreal, Quebec, Canada.

    Google Scholar 

  42. Kanematsu, H., Hirai, N., Miura, Y., Tanaka, M., Kogo, T., & Itoh, H. (2013). Various metals from water by biofilm from ambient germs in a reaction container. Paper presented at the Materials Science and Technology conference, Montreal, Quebec, Canada.

    Google Scholar 

  43. Kanematsu, H., Kogo, T., Itoh, H., Wada, N., & Yoshitake, M. (2013). Fogged glass by biofilm formation and its evaluation. Paper presented at the Proceedings of MS & T’ 13, Montreal, Quebec, Canada.

    Google Scholar 

  44. Kanematsu, H., Kogo, T., Sano, K., Noda, M., Wada, N., & Yoshitake, M. (2014). Nano-composite coating on glasses for biofilm control. Journal of Materials Science & Surface Engineering, 1(2), 58–63 (in Japanese).

    Google Scholar 

  45. Nakanishi, Y., Kanematsu, H., Miura, Y., Arumugam, V., Hirai, N., & Ogawa, A. (2014). Two kinds of composites and their biofouling behavior in a LBR. CAMP-ISIJ, 27, 602–603 (in Japanese).

    Google Scholar 

  46. Nishi, N., Kanematsu, H., Miura, Y., Kito, M., Hirai, N., & Ogawa, A. (2014). Production of desktop LBR and biofilm formation behavior. CAMP-ISIJ, 27, 595–596 (in Japanese).

    Google Scholar 

  47. Sano, K., Kanematsu, H., Hirai, N., Ogawa, A., Kogo, K., Kitayabu, K., et al. (2015). Analyses of biofilm formed on various metal substrates by FT-IR and Raman spectroscopy. CAMP-ISIJ, 28, 493–494 (in Japanese).

    Google Scholar 

  48. Kanematsu, H., Sano, K., Kougo, T., Ogawa, A., & Hirai, N. (2016). Anti-biofouling surfaces produced by nano-composite films and their evaluation. IEICE Technical Report (OME2016-54–OME2016-58) Organic Molecular Electronics, 116(384), 11–15 (in Japanese).

    Google Scholar 

  49. Kanematsu, H., Saito, T., Barry, D. M., Hirai, N., Kogo, T., Ogawa, A., et al. (2017). Effects of ionic liquids on biofilm formation in a loop-type laboratory biofilm reactor. ECS Transactions, 80(10), 1147–1155. https://doi.org/10.1149/08010.1147ecst.

    Article  CAS  Google Scholar 

  50. Kanematsu, H., Maeda, S., Barry, D. M., Umeki, S., Tohji, K., Hirai, N., et al. (2018). Effects of elastic waves at several frequencies on biofilm formation in circulating types of laboratory biofilm reactors. In M. M. Mahmoud, K. Sridharan, H. Colorado, A. S. Bhalla, J. P. Singh, S. Gupta, J. Langhorn, A. Jitianu, & N. J. Manjooran (Eds.), Ceramic transactions—Advances in ceramics for environmental, functional, structural, and energy applications (Vol. 265, pp. 43–51). New York, the United States: Wiley, Inc.

    Google Scholar 

  51. Costerton, J. W. (1999). Introduction to biofilm. International Journal of Antimicrobial Agents, 11, 217–221.

    Article  CAS  PubMed  Google Scholar 

  52. Garrett, T. R., Bhakoo, M., & Zhang, Z. (2008). Bacterial adhesion and biofilms on surfaces. Progress in Natural Science, 18, 1049–1056.

    Article  CAS  Google Scholar 

  53. Pantanella, F., Valenti, P., Natalizi, T., Passeri, D., & Berlutti, F. (2013). Analytical techniques to study microbial biofilm on abiotic surfaces: Pros and cons of the main techniques currently in use. Annali di Igiene, 25, 31–42. https://doi.org/10.7416/ai.2013.1904.

    Article  CAS  PubMed  Google Scholar 

  54. Barry, D. M., & McGrath, P. B. (2015). Rotation disk process for accelerated assessment of biofilm formation on medical materials. Materials Technology: Advanced Biomaterials, 30(B1), 33–37.

    Article  CAS  Google Scholar 

  55. Photo by Dana M. Barry.

    Google Scholar 

  56. Grass, G., Rensing, C., & Solioz, M. (2011). Metallic copper as an antimicrobial surface. Applied and Environmental Microbiology, 77(5), 1541–1547.

    Article  CAS  PubMed  Google Scholar 

  57. Banerjee, J., Ghatak, P. D., Roy, S., Khanna, S., Hemann, C., Deng, B., et al. (2015) Silver-zinc redox-coupled electroceutical wound dressing disrupts bacterial biofilm. PloS ONE, 10(3). https://doi.org/10.1371/journal.pone.0119531.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. Perez-Roa, R. E., Tompkins, D. T., Paulose, M., Grimes, C. A., Anderson, M. A., & Noguera, D. R. (2006). Effects of localized, low-voltage pulsed electric fields on the development and inhibition of Pseudomonas aeruginosa biofilms. Biofouling, 22(5–6), 383–390.

    Article  PubMed  Google Scholar 

  59. Kim, Y. W., Subramanian, S., Gerasopoulos, K., Ben-Yoav, H., Wu, H.-C., Quan, D., et al. (2015). Effect of electrical energy on the efficacy of biofilm treatment using the bioelectric effect. Nature. https://doi.org/10.1038/npjbiofilms.2015.16.

  60. Sandvik, E. L., McLeod, B. R., Parker, A. E., & Stewart, P. S. (2013). Direct electric current treatment under physiologic saline conditions kills Staphylococcus epidermidis Biofilms via electrolytic generation of hypochlorous acid. PloS ONE, 8(2), e55118. https://doi.org/10.1371/journal.pone.0055118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Barry, D. M., & McGrath, P. B. (2016). Rotation disk process to assess the influence of metals and voltage on the growth of biofilm: Materials, 9(7), 568. https://doi.org/10.3390/ma9070568.

    Article  PubMed Central  CAS  Google Scholar 

  62. Carpio, I. E. M., Santos, C. M., Wei, X., & Rodrigues, D. F. (2012). Toxicity of a polymer–graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale, 4(15), 4746–4756.

    Article  CAS  Google Scholar 

  63. Subbiahdoss, G., Pidhatika, B., Coullerez, G., Charnley, M., Kuijer, R., van der Mei, H. C., et al. (2010). Bacterial biofilm formation versus mammalian cell growth on titanium-based mono-and bi-functional coating. European Cells & Materials, 19, 205–213.

    Article  CAS  Google Scholar 

  64. Sanyasi, S., Majhi, R. K., Kumar, S., Mishra, M., Ghosh, A., Suar, M., et al. (2016). Polysaccharide-capped silver nanoparticles inhibit biofilm formation and eliminate multi-drug-resistant bacteria by disrupting bacterial cytoskeleton with reduced cytotoxicity towards mammalian cells. Scientific Reports, 6, 24929.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Fan, J., Li, Y., Nguyen, H. N., Yao, Y., & Rodrigues, D. F. (2015). Toxicity of exfoliated-MoS 2 and annealed exfoliated-MoS 2 towards planktonic cells, biofilms, and mammalian cells in the presence of electron donor. Environmental Science: Nano, 2(4), 370–379.

    CAS  Google Scholar 

  66. Subbiahdoss, G., Kuijer, R., Busscher, H. J., & van der Mei, H. C. (2010). Mammalian cell growth versus biofilm formation on biomaterial surfaces in an in vitro post-operative contamination model. Microbiology, 156(10), 3073–3078.

    Article  CAS  PubMed  Google Scholar 

  67. Jurcisek, J. A., Bookwalter, J. E., Baker, B. D., Fernandez, S., Novotny, L. A., Munson, R. S., Jr., et al. (2007). The PilA protein of non typeable Haemophilus influenzae plays a role in biofilm formation, adherence to epithelial cells and colonization of the mammalian upper respiratory tract. Molecular Microbiology, 65(5), 1288–1299.

    Article  CAS  PubMed  Google Scholar 

  68. Renner, L. D., & Weibel, D. B. (2011). Physicochemical regulation of biofilm formation. MRS Bulletin, 36(5), 347–355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Alem, M. A., & Douglas, L. J. (2004). Effects of aspirin and other nonsteroidal anti-inflammatory drugs on biofilms and planktonic cells of Candida albicans. Antimicrobial Agents and Chemotherapy, 48(1), 41–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Benghezal, M., Adam, E., Lucas, A., Burn, C., Orchard, M. G., Deuschel, C., et al. (2007). Inhibitors of bacterial virulence identified in a surrogate host model. Cellular Microbiology, 9, 1336–1342.

    Article  CAS  PubMed  Google Scholar 

  71. Sandstrom, G., Saeed, A., & Abd, H. (2011). Acanthamoeba-bacteria: A model to study host interaction with human pathogens. Current Drug Targets, 12, 936–941.

    Article  PubMed  Google Scholar 

  72. Annesley, S. J., & Fisher, P. R. (2009). Dictyostelium discoideum: A model for many reasons. Molecular and Cellular Biochemistry, 329, 73–91.

    Google Scholar 

  73. Zhang, Y., Hu, Y., Yang, B., Ma, F., Lu, P., Li, L., et al. (2010). Duckweed (Lemna minor) as a model plant system for the study of human microbial pathogenesis. PLoS ONE, 5, e13527.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Silo-Suh, L., Suh, S. J., Sokol, P. A., & Ohman, D. E. (2002). A simple alfalfa seedling infection model for Pseudomonas aeruginosa strains associated with cystic fibrosis shows AlgT (sigma-22) and RhlR contribute to pathogenesis. Proceedings of the National Academy of Sciences of the United States of America 2002, 99, 15699–15704.

    Google Scholar 

  75. Schlaich, N. L. (2011). Arabidopsis thaliana: The model plant to study host-pathogen interactions. Current Drug Targets, 12, 955–966.

    Article  CAS  PubMed  Google Scholar 

  76. Graf, J. (1999). Symbiosis of Aeromonas veronii biovar sobria and Hirudo medicinalis, the medicinal leech: A novel model for digestive tract associations. Infection and Immunity, 67, 1–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Laws, T. R., Smith, S. A., Smith, M. P., Harding, S. V., Atkins, T. P., & Titball, R. W. (2005). The nematode Panagrellus redivivus is susceptible to killing by human pathogens at 37 degrees C. FEMS Microbiology Letters, 250, 77–83.

    Article  CAS  PubMed  Google Scholar 

  78. Marsh, E. K., & May, R. C. (2012). Caenorhabditis elegans, a model organism for investigating immunity. Applied and Environment Microbiology, 78, 2075–2081.

    Article  CAS  Google Scholar 

  79. Jander, G., Rahme, L. G., & Ausubel, F. M. (2000). Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. Journal of Bacteriology, 182, 3843–3845.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kounatidis, I., & Ligoxygakis, P. (2012). Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biology, 2, 120075.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Kanther, M., & Rawls, J. F. (2010). Host-microbe interactions in the developing zebrafish. Current Opinion in Immunology, 22, 10–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Cash, H. A., Woods, D. E., McCullough, B., Johanson, W. G., Jr., & Bass, J. A. (1979). A rat model of chronic respiratory infection with Pseudomonas aeruginosa. American Review of Respiratory Disease, 119, 453–459.

    CAS  Google Scholar 

  83. Bernier, S. P., Silo-Suh, L., Woods, D. E., Ohman, D. E., & Sokol, P. A. (2003). Comparative analysis of plant and animal models for characterization of Burkholderia cepacia virulence. Infection and Immunity, 71, 5306–5313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Cheung, A. T., Moss, R. B., Leong, A. B., & Novick, W. J., Jr. (1992). Chronic Pseudomonas aeruginosa endobronchitis in rhesus monkeys: I. Effects of pentoxifylline on neutrophil influx. Journal of Medical Primatology, 21, 357–362.

    CAS  PubMed  Google Scholar 

  85. Starke, J. R., Edwards, M. S., Langston, C., & Baker, C. J. (1987). A mouse model of chronic pulmonary infection with Pseudomonas aeruginosa and Pseudomonas cepacia. Pediatric Research, 22, 698–702.

    Article  CAS  PubMed  Google Scholar 

  86. Thomassen, M. J., Klinger, J. D., Winnie, G. B., Wood, R. E., Burtner, C., Tomashefski, J. F., et al. (1984). Pulmonary cellular response to chronic irritation and chronic Pseudomonas aeruginosa pneumonia in cats. Infection and Immunity, 45, 741–747.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Winnie, G. B., Klinger, J. D., Sherman, J. M., & Thomassen, M. J. (1982). Induction of phagocytic inhibitory activity in cats with chronic Pseudomonas aeruginosa pulmonary infection. Infection and Immunity, 38, 1088–1093.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Pedersen, S. S., Shand, G. H., Hansen, B. L., & Hansen, G. N. (1990). Induction of experimental chronic Pseudomonas aeruginosa lung infection with P. aeruginosa entrapped in alginate microspheres. APMIS, 98, 203–211.

    Article  CAS  PubMed  Google Scholar 

  89. Yang, L., Hengzhuang, W., Wu, H., Damkiaer, S., Jochumsen, N., Song, Z., et al. (2012). Polysaccharides serve as scaffold of biofilms formed by mucoid Pseudomonas aeruginosa. FEMS Immunology and Medical Microbiology, 65, 366–376.

    Article  CAS  PubMed  Google Scholar 

  90. Hengzhuang, W., Wu, H., Ciofu, O., Song, Z., & Hoiby, N. (2011). In vivo pharmacokinetics/pharmacodynamics of colistin and imipenem in Pseudomonas aeruginosa biofilm infection. Antimicrobial Agents and Chemotherapy, 56, 2683–2690.

    Article  CAS  Google Scholar 

  91. Yanagihara, K., Ohnishi, Y., Morinaga, Y., Nakamura, S., Kurihara, S., Seki, M., et al. (2008). Efficacy of ME1036 against meticillin-resistant Staphylococcus aureus and vancomycin- insensitive S. aureus in a model of haematogenous pulmonary infection. International Journal of Antimicrobial Agents, 32, 401–404.

    Article  CAS  PubMed  Google Scholar 

  92. Yanagihara, K., Seki, M., Izumikawa, K., Higashiyama, Y., Miyazaki, Y., Hirakata, Y., et al. (2006). Potency of DX-619, a novel des-F(6)-quinolone, in haematogenous murine bronchopneumonia caused by methicillin-resistant and vancomycin-intermediate Staphylococcus aureus. International Journal of Antimicrobial Agents, 28, 212–216.

    Article  CAS  PubMed  Google Scholar 

  93. Clarke, L. L., Grubb, B. R., Gabriel, S. E., Smithies, O., Koller, B. H., & Boucher, R. C. (1992). Defective epithelial chloride transport in a gene-targeted mouse model of cystic fibrosis. Science, 257, 1125–1128.

    Article  CAS  PubMed  Google Scholar 

  94. Keiser, N. W., & Engelhardt, J. F. (2011). New animal models of cystic fibrosis: what are they teaching us? Current Opinion in Pulmonary Medicine, 17, 478–483.

    PubMed  PubMed Central  Google Scholar 

  95. Rogers, C. S., Hao, Y., Rokhlina, T., Samuel, M., Stoltz, D. A., Li, Y., et al. (2008). Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer. Journal of Clinical Investigation, 118, 1571–1577.

    Google Scholar 

  96. Pang, B., Hong, W., West-Barnette, S. L., Kock, N. D., & Swords, W. E. (2008). Diminished ICAM-1 expression and impaired pulmonary clearance of nontypeable Haemophilus influenzae in a mouse model of chronic obstructive pulmonary disease/emphysema. Infection and Immunity, 76, 4959–4967.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Yanagihara, K., Tomono, K., Sawai, T., Hirakata, Y., Kadota, J., Koga, H., et al. (1997). Effect of clarithromycin on lymphocytes in chronic respiratory Pseudomonas aeruginosa infection. American Journal of Respiratory and Critical Care Medicine, 155, 337–342.

    Article  CAS  PubMed  Google Scholar 

  98. Nagata, T., Mukae, H., Kadota, J., Hayashi, T., Fujii, T., Kuroki, M., et al. (2004). Effect of erythromycin on chronic respiratory infection caused by Pseudomonas aeruginosa with biofilm formation in an experimental murine model. Antimicrobial Agents and Chemotherapy, 48, 2251–2259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Yanagihara, K., Tomono, K., Sawai, T., Kuroki, M., Kaneko, Y., Ohno, H., et al. (2000). Combination therapy for chronic Pseudomonas aeruginosa respiratory infection associated with biofilm formation. Journal of Antimicrobial Chemotherapy, 46, 69–72.

    Article  CAS  Google Scholar 

  100. Anderson, G. G., Palermo, J. J., Schilling, J. D., Roth, R., Heuser, J., & Hultgren, S. J. (2003). Intracellular bacterial biofilm-like pods in urinary tract infections. Science, 301, 105–107.

    Article  CAS  PubMed  Google Scholar 

  101. Justice, S. S., Hung, C., Theriot, J. A., Fletcher, D. A., Anderson, G. G., Footer, M. J., et al. (2004). Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proceedings of the National Academy of Sciences of the United States of America 2004, 101, 1333–1338.

    Article  CAS  Google Scholar 

  102. Ozok, H. U., Ekim, O., Saltas, H., Arikok, A. T., Babacan, O., Sagnak, L., et al. (2012). The preventive role of transurethral antibiotic delivery in a rat model. Drug Design, Development and Therapy, 6, 187–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Kim, H. W., Ha, U. S., Woo, J. C., Kim, S. J., Yoon, B. I., Lee, S. J., et al. (2012). Preventive effect of selenium on chronic bacterial prostatitis. Journal of Infection and Chemotherapy, 18, 30–34.

    Article  CAS  PubMed  Google Scholar 

  104. Phan, V., Belas, R., Gilmore, B. F., & Ceri, H. (2008). ZapA, a virulence factor in a rat model of Proteus mirabilis-induced acute and chronic prostatitis. Infection and Immunity, 76, 4859–4864.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kim, S. H., Ha, U. S., Lee, H. R., Sohn, D. W., Lee, S. J., Kim, H. W., et al. (2011). Do Escherichia coli extract and cranberry exert preventive effects on chronic bacterial prostatitis? Pilot study using an animal model. Journal of Infection and Chemotherapy, 17, 322–326.

    Article  PubMed  Google Scholar 

  106. Nickel, J. C., Olson, M., McLean, R. J., Grant, S. K., & Costerton, J. W. (1987). An ecological study of infected urinary stone genesis in an animal model. British Journal of Urology, 59, 21–30.

    Article  CAS  PubMed  Google Scholar 

  107. Vermeulen, C. W., & Goetz, R. (1954). Experimental urolithiasis. IX. Influence of infection on stone growth in rats. Journal of Urology, 72, 761–769.

    Article  CAS  Google Scholar 

  108. Satoh, M., Munakata, K., Kitoh, K., Takeuchi, H., & Yoshida, O. (1984). A newly designed model for infection-induced bladder stone formation in the rat. Journal of Urology, 132, 1247–1249.

    Article  CAS  Google Scholar 

  109. Clerc, M., Bebear, C., Goursolle, M., & Aparicio, M. (1984). Calculi experimentally obtained in the rat by intrarenal injection of Ureaplasma urealyticum. Annales de Biologie Clinique (Paris), 42, 277–281.

    CAS  Google Scholar 

  110. Eckmann, L. (2006). Animal models of inflammatory bowel disease: Lessons from enteric infections. Annals of the New York Academy of Sciences, 1072, 28–38.

    Article  CAS  PubMed  Google Scholar 

  111. Nell, S., Suerbaum, S., & Josenhans, C. (2010). The impact of the microbiota on the pathogenesis of IBD: Lessons from mouse infection models. Nature Reviews Microbiology, 8, 564–577.

    Article  CAS  PubMed  Google Scholar 

  112. Bohnhoff, M., Miller, C. P., & Martin, W. R. (1964). Resistance of the mouse’s intestinal tract to experimental salmonella infection. II. Factors responsible for its loss following streptomycin treatment. Journal of Experimental Medicine, 120, 817–828.

    Article  CAS  Google Scholar 

  113. Kaiser, P., Diard, M., Stecher, B., & Hardt, W. D. (2012). The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen’s virulence factors, and the host’s mucosal immune response. Immunological Reviews, 245, 56–83.

    Article  CAS  PubMed  Google Scholar 

  114. Sukupolvi, S., Edelstein, A., Rhen, M., Normark, S. J., & Pfeifer, J. D. (1997). Development of a murine model of chronic Salmonella infection. Infection and Immunity, 65, 838–842.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Monack, D. M., Bouley, D. M., & Falkow, S. (2004). Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. Journal of Experimental Medicine, 199, 231–241.

    Article  CAS  Google Scholar 

  116. Crawford, R. W., Reeve, K. E., & Gunn, J. S. (2010). Flagellated but not hyperfimbriated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. Journal of Bacteriology, 192, 2981–2990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Dai, T., Tegos, G. P., Zhiyentayev, T., Mylonakis, E., & Hamblin, M. R. (2010). Photodynamic therapy for methicillin-resistant Staphylococcus aureus infection in a mouse skin abrasion model. Lasers in Surgery and Medicine, 42, 38–44.

    Article  PubMed  PubMed Central  Google Scholar 

  118. Simonetti, O., Cirioni, O., Ghiselli, R., Goteri, G., Scalise, A., Orlando, F., et al. (2008). RNAIII-inhibiting peptide enhances healing of wounds infected with methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 52, 2205–2211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Akiyama, H., Kanzaki, H., Tada, J., & Arata, J. (1996). Staphylococcus aureus infection on cut wounds in the mouse skin: Experimental Staphylococcal botryomycosis. Journal of Dermatological Science, 11, 234–238.

    Article  CAS  PubMed  Google Scholar 

  120. Nakagami, G., Sanada, H., Sugama, J., Morohoshi, T., Ikeda, T., & Ohta, Y. (2008). Detection of Pseudomonas aeruginosa quorum sensing signals in an infected ischemic wound: An experimental study in rats. Wound Repair and Regeneration, 16, 30–36.

    Article  PubMed  Google Scholar 

  121. Gurjala, A. N., Geringer, M. R., Seth, A. K., Hong, S. J., Smeltzer, M. S., Galiano, R. D., et al. (2011). Development of a novel, highly quantitative in vivo model for the study of biofilm-impaired cutaneous wound healing. Wound Repair and Regeneration, 19, 400–410.

    Article  PubMed  Google Scholar 

  122. Mastropaolo, M. D., Evans, N. P., Byrnes, M. K., Stevens, A. M., Robertson, J. L., & Melville, S. B. (2005). Synergy in polymicrobial infections in a mouse model of type 2 diabetes. Infection and Immunity, 73, 6055–6063.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Durack, D. T., Beeson, P. B., & Petersdorf, R. G. (1973). Experimental bacterial endocarditis. 3. Production and progress of the disease in rabbits. British Journal of Experimental Pathology, 54, 142–151.

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Xiong, Y. Q., Willard, J., Yeaman, M. R., Cheung, A. L., & Bayer, A. S. (2006). Regulation of Staphylococcus aureus alpha-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. Journal of Infectious Diseases, 194, 1267–1275.

    Article  CAS  Google Scholar 

  125. Veloso, T. R., Amiguet, M., Rousson, V., Giddey, M., Vouillamoz, J., Moreillon, P., et al. (2011). Induction of experimental endocarditis by continuous low-grade bacteremia mimicking spontaneous bacteremia in humans. Infection and Immunity, 79, 2006–2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Swords, W. E., Moore, M. L., Godzicki, L., Bukofzer, G., Mitten, M. J., & VonCannon, J. (2004). Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infection and Immunity, 72, 106–113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Ehrlich, G. D., Veeh, R., Wang, X., Costerton, J. W., Hayes, J. D., Hu, F. Z., et al. (2002). Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA, 287, 1710–1715.

    Article  PubMed  Google Scholar 

  128. Byrd, M. S., Pang, B., Hong, W., Waligora, E. A., Juneau, R. A., Armbruster, C. E., et al. (2011). Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model. Infection and Immunity, 79, 3087–3095.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Dohar, J. E., Hebda, P. A., Veeh, R., Awad, M., Costerton, J. W., Hayes, J., et al. (2005). Mucosal biofilm formation on middle-ear mucosa in a nonhuman primate model of chronic suppurative otitis media. Laryngoscope, 115, 1469–1472.

    Article  PubMed  Google Scholar 

  130. Chaney, E. J., Nguyen, C. T., & Boppart, S. A. (2011). Novel method for non-invasive induction of a middle-ear biofilm in the rat. Vaccine, 29, 1628–1633.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Eriksson, P. O., Li, J., Ny, T., & Hellstrom, S. (2006). Spontaneous development of otitis media in plasminogen-deficient mice. International Journal of Medical Microbiology, 296, 501–509.

    Article  PubMed  Google Scholar 

  132. Johansson, P., Kumlien, J., Carlsoo, B., Drettner, B., & Nord, C. E. (1988). Experimental acute sinusitis in rabbits. A bacteriological and histological study. Acta Oto-Laryngologica, 105, 357–366.

    Article  CAS  PubMed  Google Scholar 

  133. Abreu, N. A., Nagalingam, N. A., Song, Y., Roediger, F. C., Pletcher, S. D., Goldberg, A. N., et al. (2012). Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Science Translational Medicine, 4, 151ra124.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. Ha, K. R., Psaltis, A. J., Tan, L., & Wormald, P. J. (2007). A sheep model for the study of biofilms in rhinosinusitis. American Journal of Rhinology, 21, 339–345.

    Article  PubMed  Google Scholar 

  135. Fitzgerald, R. J., & Keyes, P. H. (1960). Demonstration of the etiologic role of streptococci in experimental caries in the hamster. Journal of the American Dental Association, 61, 9–19.

    Article  CAS  PubMed  Google Scholar 

  136. Catalan, M. A., Scott-Anne, K., Klein, M. I., Koo, H., Bowen, W. H., & Melvin, J. E. (2011). Elevated incidence of dental caries in a mouse model of cystic fibrosis. PLoS ONE, 6, e16549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Bainbridge, B., Verma, R. K., Eastman, C., Yehia, B., Rivera, M., Moffatt, C., et al. (2010). Role of Porphyromonas gingivalis phosphoserine phosphatase enzyme SerB in inflammation, immune response, and induction of alveolar bone resorption in rats. Infection and Immunity, 78, 4560–4569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Lee, S. F., Andrian, E., Rowland, E., & Marquez, I. C. (2009). Immune response and alveolar bone resorption in a mouse model of Treponema denticola infection. Infection and Immunity, 77, 694–698.

    Article  CAS  PubMed  Google Scholar 

  139. Settem, R. P., El-Hassan, A. T., Honma, K., Stafford, G. P., & Sharma, A. (2012). Fusobacterium nucleatum and Tannerella forsythia induce synergistic alveolar bone loss in a mouse periodontitis model. Infection and Immunity, 80, 2436–2443.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Polak, D., Wilensky, A., Shapira, L., Halabi, A., Goldstein, D., Weiss, E. I., et al. (2009). Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: bone loss and host response. Journal of Clinical Periodontology, 36, 406–410.

    Article  PubMed  Google Scholar 

  141. Hasturk, H., Kantarci, A., Goguet-Surmenian, E., Blackwood, A., Andry, C., Serhan, C. N., et al. (2007). Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. Journal of Immunology, 179, 7021–7029.

    Article  CAS  Google Scholar 

  142. Pouliot, M., Clish, C. B., Petasis, N. A., Van Dyke, T. E., & Serhan, C. N. (2000). Lipoxin A(4) analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: A role for cyclooxygenase-2 and lipoxins in periodontal disease. Biochemistry, 39, 4761–4768.

    Article  CAS  PubMed  Google Scholar 

  143. Scheman, L., Janot, M., & Lewin, P. (1941). The production of experimental osteomyelitis: Preliminary report. JAMA, 117, 1525–1529.

    Article  Google Scholar 

  144. Brady, R. A., Leid, J. G., Camper, A. K., Costerton, J. W., & Shirtliff, M. E. (2006). Identification of Staphylococcus aureus proteins recognized by the antibody- mediated immune response to a biofilm infection. Infection and Immunity, 74, 3415–3426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Poeppl, W., Tobudic, S., Lingscheid, T., Plasenzotti, R., Kozakowski, N., Lagler, H., et al. (2011). Daptomycin, fosfomycin, or both for treatment of methicillin-resistant Staphylococcus aureus osteomyelitis in an experimental rat model. Antimicrobial Agents and Chemotherapy, 55, 4999–5003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Funao, H., Ishii, K., Nagai, S., Sasaki, A., Hoshikawa, T., Aizawa, M., et al. (2012). Establishment of a real-time, quantitative, and reproducible mouse model of Staphylococcus osteomyelitis using bioluminescence imaging. Infection and Immunity, 80, 733–741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Rupp, M. E., Ulphani, J. S., Fey, P. D., & Mack, D. (1999). Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infection and Immunity, 67, 2656–2659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Cirioni, O., Giacometti, A., Ghiselli, R., Dell’Acqua, G., Orlando, F., Mocchegiani, F., et al. (2006). RNAIII-inhibiting peptide significantly reduces bacterial load and enhances the effect of antibiotics in the treatment of central venous catheter-associated Staphylococcus aureus infections. Journal of Infectious Diseases, 193, 180–186.

    Article  CAS  Google Scholar 

  150. Andes, D., Nett, J., Oschel, P., Albrecht, R., Marchillo, K., & Pitula, A. (2004). Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infection and Immunity, 72, 6023–6031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Hall, L. L., DeLopez, O. H., Roberts, A., & Smith, F. A. (1974). A procedure for chronic intravenous catheterization in the rabbit. Laboratory Animal Science, 24, 79–83.

    Google Scholar 

  152. Fernandez-Hidalgo, N., Gavalda, J., Almirante, B., Martin, M. T., Onrubia, P. L., Gomis, X., et al. (2010). Evaluation of linezolid, vancomycin, gentamicin and ciprofloxacin in a rabbit model of antibiotic-lock technique for Staphylococcus aureus catheter-related infection. Journal of Antimicrobial Chemotherapy, 65, 525–530.

    Article  CAS  Google Scholar 

  153. Raad, I., Hachem, R., Tcholakian, R. K., & Sherertz, R. (2002). Efficacy of minocycline and EDTA lock solution in preventing catheter-related bacteremia, septic phlebitis, and endocarditis in rabbits. Antimicrobial Agents and Chemotherapy, 46, 327–332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Chauhan, A., Lebeaux, D., Decante, B., Kriegel, I., Escande, M. C., Ghigo, J. M., et al. (2012). A rat model of central venous catheter to study establishment of long-term bacterial biofilm and related acute and chronic infections. PLoS One, 7, e37281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Haraoka, M., Matsumoto, T., Takahashi, K., Kubo, S., Tanaka, M., & Kumazawa, J. (1995). Effect of prednisolone on ascending renal infection due to biofilm disease and lower urinary tract obstruction in rats. Urological Research, 22, 383–387.

    Article  CAS  PubMed  Google Scholar 

  156. Cirioni, O., Ghiselli, R., Silvestri, C., Minardi, D., Gabrielli, E., Orlando, F., et al. (2011). Effect of the combination of clarithromycin and amikacin on Pseudomonas aeruginosa biofilm in an animal model of ureteral stent infection. Journal of Antimicrobial Chemotherapy, 66, 1318–1323.

    Article  CAS  Google Scholar 

  157. Allison, K. R., Brynildsen, M. P., & Collins, J. J. (2011). Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature, 473, 216–220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Fung, L. C., Mittelman, M. W., Thorner, P. S., & Khoury, A. E. (2003). A novel rabbit model for the evaluation of biomaterial associated urinary tract infection. Canadian Journal of Urology, 10, 2007–2012.

    Google Scholar 

  159. Cadieux, P. A., Chew, B. H., Knudsen, B. E., Dejong, K., Rowe, E., Reid, G., et al. (2006). Triclosan loaded ureteral stents decrease Proteus mirabilis 296 infection in a rabbit urinary tract infection model. Journal of Urology, 175, 2331–2335.

    Article  Google Scholar 

  160. Kurosaka, Y., Ishida, Y., Yamamura, E., Takase, H., Otani, T., & Kumon, H. (2001). A non-surgical rat model of foreign body-associated urinary tract infection with Pseudomonas aeruginosa. Microbiology and Immunology, 45, 9–15.

    Article  CAS  PubMed  Google Scholar 

  161. Guiton, P. S., Hung, C. S., Hancock, L. E., Caparon, M. G., & Hultgren, S. J. (2010). Enterococcal biofilm formation and virulence in an optimized murine model of foreign body-associated urinary tract infections. Infection and Immunity, 78, 4166–4175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Kadurugamuwa, J. L., Modi, K., Yu, J., Francis, K. P., Purchio, T., & Contag, P. R. (2005). Noninvasive biophotonic imaging for monitoring of catheter-associated urinary tract infections and therapy in mice. Infection and Immunity, 73, 3878–3887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Olson, M. E., Nickel, J. C., Khoury, A. E., Morck, D. W., Cleeland, R., & Costerton, J. W. (1989). Amdinocillin treatment of catheter-associated bacteriuria in rabbits. Journal of Infectious Diseases, 159, 1065–1072.

    Article  CAS  Google Scholar 

  164. Hachem, R., Reitzel, R., Borne, A., Jiang, Y., Tinkey, P., Uthamanthil, R., et al. (2009). Novel antiseptic urinary catheters for prevention of urinary tract infections: correlation of in vivo and in vitro test results. Antimicrobial Agents and Chemotherapy, 53, 5145–5149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Hazan, Z., Zumeris, J., Jacob, H., Raskin, H., Kratysh, G., Vishnia, M., et al. (2006). Effective prevention of microbial biofilm formation on medical devices by low-energy surface acoustic waves. Antimicrobial Agents and Chemotherapy, 50, 4144–4152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Davis, C. P., Shirtliff, M. E., Scimeca, J. M., Hoskins, S. L., & Warren, M. M. (1995). In vivo reduction of bacterial populations in the urinary tract of catheterized sheep by iontophoresis. Journal of Urology, 154, 1948–1953.

    Article  CAS  Google Scholar 

  167. Mayberry-Carson, K. J., Tober-Meyer, B., Smith, J. K., Lambe, D. W., Jr., & Costerton, J. W. (1984). Bacterial adherence and glycocalyx formation in osteomyelitis experimentally induced with Staphylococcus aureus. Infection and Immunity, 43, 825–833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Mayberry-Carson, K. J., Tober-Meyer, B., Lambe, D. W., Jr., & Costerton, J. W. (1986). An electron microscopic study of the effect of clindamycin therapy on bacterial adherence and glycocalyx formation in experimental Staphylococcus aureus osteomyelitis. Microbios, 48, 189–206.

    CAS  PubMed  Google Scholar 

  169. Sanzen, L., & Linder, L. (1995). Infection adjacent to titanium and bone cement implants: an experimental study in rabbits. Biomaterials, 16, 1273–1277.

    Article  CAS  PubMed  Google Scholar 

  170. Eerenberg, J. P., Patka, P., Haarman, H. J., & Dwars, B. J. (1994). A new model for posttraumatic osteomyelitis in rabbits. Journal of Investigative Surgery, 7, 453–465.

    Article  CAS  PubMed  Google Scholar 

  171. Del Pozo, J. L., Rouse, M. S., Euba, G., Kang, C. I., Mandrekar, J. N., Steckelberg, J. M., et al. (2009). The electricidal effect is active in an experimental model of Staphylococcus epidermidis chronic foreign body osteomyelitis. Antimicrobial Agents and Chemotherapy, 53, 4064–4068.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  172. Evans, R. P., Nelson, C. L., & Harrison, B. H. (1993). The effect of wound environment on the incidence of acute osteomyelitis. Clinical Orthopaedics and Related Research, 289–297.

    Google Scholar 

  173. Lucke, M., Schmidmaier, G., Sadoni, S., Wildemann, B., Schiller, R., Haas, N. P., et al. (2003). Gentamicin coating of metallic implants reduces implant-related osteomyelitis in rats. Bone, 32, 521–531.

    Article  CAS  PubMed  Google Scholar 

  174. Lucke, M., Wildemann, B., Sadoni, S., Surke, C., Schiller, R., Stemberger, A., et al. (2005). Systemic versus local application of gentamicin in prophylaxis of implant-related osteomyelitis in a rat model. Bone, 36, 770–778.

    Article  CAS  PubMed  Google Scholar 

  175. Prabhakara, R., Harro, J. M., Leid, J. G., Keegan, A. D., Prior, M. L., & Shirtliff, M. E. (2011). Suppression of the inflammatory immune response prevents the development of chronic biofilm infection due to methicillin-resistant Staphylococcus aureus. Infection and Immunity, 79, 5010–5018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Li, D., Gromov, K., Soballe, K., Puzas, J. E., O’Keefe, R. J., Awad, H., et al. (2008). Quantitative mouse model of implant-associated osteomyelitis and the kinetics of microbial growth, osteolysis, and humoral immunity. Journal of Orthopaedic Research, 26, 96–105.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  177. Fitzgerald, R. H., Jr. (1983). Experimental osteomyelitis: description of a canine model and the role of depot administration of antibiotics in the prevention and treatment of sepsis. Journal of Bone and Joint Surgery. American Volume, 65, 371–380.

    Article  Google Scholar 

  178. Petty, W., Spanier, S., Shuster, J. J., & Silverthorne, C. (1985). The influence of skeletal implants on incidence of infection. Experiments in a canine model. Journal of Bone and Joint Surgery. American Volume, 67, 1236–1244.

    Article  CAS  Google Scholar 

  179. Philipov, J. P., Pascalev, M. D., Aminkov, B. Y., & Grosev, C. D. (1995). Changes in serum carboxyterminal telopeptide of type I collagen in an experimental model of canine osteomyelitis. Calcified Tissue International, 57, 152–154.

    Article  CAS  PubMed  Google Scholar 

  180. Williams, D. L., Haymond, B. S., Woodbury, K. L., Beck, J. P., Moore, D. E., Epperson, R. T., et al. (2012). Experimental model of biofilm implant- related osteomyelitis to test combination biomaterials using biofilms as initial inocula. Journal of Biomedical Materials Research Part A, 100, 1888–1900.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  181. Schurman, D. J., Trindade, C., Hirshman, H. P., Moser, K., Kajiyama, G., & Stevens, P. (1978). Antibiotic-acrylic bone cement composites. Studies of gentamicin and Palacos. Journal of Bone and Joint Surgery. American Volume, 60, 978–984.

    Article  CAS  Google Scholar 

  182. Blomgren, G., & Lindgren, U. (1981). Late hematogenous infection in total joint replacement: Studies of gentamicin and bone cement in the rabbit. Clinical Orthopaedics and Related Research, 244–248.

    Google Scholar 

  183. Southwood, R. T., Rice, J. L., McDonald, P. J., Hakendorf, P. H., & Rozenbilds, M. A. (1985). Infection in experimental hip arthroplasties. Journal of Bone and Joint Surgery. British Volume, 67, 229–231.

    Article  CAS  Google Scholar 

  184. Bernthal, N. M., Stavrakis, A. I., Billi, F., Cho, J. S., Kremen, T. J., Simon, S. I., et al. (2010). A mouse model of post-arthroplasty Staphylococcus aureus joint infection to evaluate in vivo the efficacy of antimicrobial implant coatings. PLoS One, 5, e12580.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  185. Berra, L., Curto, F., Li Bassi, G., Laquerriere, P., Baccarelli, A., & Kolobow, T. (2006). Antibacterial-coated tracheal tubes cleaned with the Mucus Shaver: A novel method to retain long-term bactericidal activity of coated tracheal tubes. Intensive Care Medicine, 32, 888–893.

    Article  PubMed  Google Scholar 

  186. Fernandez-Barat, L., Li Bassi, G., Ferrer, M., Bosch, A., Calvo, M., Vila, J., et al. (2012). Direct analysis of bacterial viability in endotracheal tube biofilm from a pig model of methicillin-resistant Staphylococcus aureus pneumonia following antimicrobial therapy. FEMS Immunology and Medical Microbiology, 65, 309–317.

    Article  CAS  PubMed  Google Scholar 

  187. Olson, M. E., Harmon, B. G., & Kollef, M. H. (2002). Silver-coated endotracheal tubes associated with reduced bacterial burden in the lungs of mechanically ventilated dogs. Chest, 121, 863–870.

    Article  PubMed  Google Scholar 

  188. Tollefson, D. F., Bandyk, D. F., Kaebnick, H. W., Seabrook, G. R., & Towne, J. B. (1987). Surface biofilm disruption. Enhanced recovery of microorganisms from vascular prostheses. Archives of Surgery, 122, 38–43.

    Article  CAS  PubMed  Google Scholar 

  189. Bergamini, T. M., Bandyk, D. F., Govostis, D., Kaebnick, H. W., & Towne, J. B. (1988). Infection of vascular prostheses caused by bacterial biofilms. Journal of Vascular Surgery, 7, 21–30.

    Article  CAS  PubMed  Google Scholar 

  190. Farooq, M., Freischlag, J., Kelly, H., Seabrook, G., Cambria, R., & Towne, J. (1999). Gelatin-sealed polyester resists Staphylococcus epidermidis biofilm infection. Journal of Surgical Research, 87, 57–61.

    Article  CAS  Google Scholar 

  191. Aboshady, I., Raad, I., Shah, A. S., Vela, D., Dvorak, T., Safi, H. J., et al. (2012). A pilot study of a triple antimicrobial-bonded Dacron graft for the prevention of aortic graft infection. Journal of Vascular Surgery, 56, 794–801.

    Article  PubMed  Google Scholar 

  192. Jacombs, A., Allan, J., Hu, H., Valente, P. M., Wessels, W. L., Deva, A. K., et al. (2012). Prevention of biofilm-induced capsular contracture with antibiotic-impregnated mesh in a porcine model. Aesthetic Surgery Journal, 32, 886–891.

    Article  PubMed  Google Scholar 

  193. Tamboto, H., Vickery, K., & Deva, A. K. (2010). Subclinical (biofilm) infection causes capsular contracture in a porcine model following augmentation mammaplasty. Plastic and Reconstructive Surgery, 126, 835–842.

    Article  CAS  PubMed  Google Scholar 

  194. Arad, E., Navon-Venezia, S., Gur, E., Kuzmenko, B., Glick, R., Frenkiel-Krispin, D., et al. (2013). Novel rat model of Methicillin- Resistant Staphylococcus aureus infected silicone breast-implants: A Study of biofilm pathogenesis. Plastic and Reconstructive Surgery, 131, 205–214.

    Article  CAS  PubMed  Google Scholar 

  195. Sun, Y., Chandra, J., Mukherjee, P., Szczotka-Flynn, L., Ghannoum, M. A., & Pearlman, E. (2010). A murine model of contact lens-associated Fusarium keratitis. Investigative Ophthalmology & Visual Science, 51, 1511–1516.

    Article  Google Scholar 

  196. Freire, M. O., Sedghizadeh, P. P., Schaudinn, C., Gorur, A., Downey, J. S., Choi, J. H., et al. (2011). Development of an animal model for Aggregatibacter actinomycetemcomitans biofilm-mediated oral osteolytic infection: a preliminary study. Journal of Periodontology, 82, 778–789.

    Article  PubMed  PubMed Central  Google Scholar 

  197. Rimondini, L., Fare, S., Brambilla, E., Felloni, A., Consonni, C., Brossa, F., et al. (1997). The effect of surface roughness on early in vivo plaque colonization on titanium. Journal of Periodontology, 68, 556–562.

    Article  CAS  PubMed  Google Scholar 

  198. Coenye, T., & Nelis, H. J. (2010). In vitro and in vivo model systems to study microbial biofilm formation. Journal of Microbiological Methods, 83, 89–105.

    Article  CAS  PubMed  Google Scholar 

  199. Ensing, G. T., Roeder, B. L., Nelson, J. L., van Horn, J. R., van der Mei, H. C., Busscher, H. J., et al. (2005). Effect of pulsed ultrasound in combination with gentamicin on bacterial viability in biofilms on bone cements in vivo. Journal of Applied Microbiology, 99, 443–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Hansen, L. K., Brown, M., Johnson, D., Palme, D. F., II, Love, C., & Darouiche, R. (2009). I n vivo model of human pathogen infection and demonstration of efficacy by an antimicrobial pouch for pacing devices. Pacing and Clinical Electrophysiology, 32, 898–907.

    Article  PubMed  Google Scholar 

  201. Illingworth, B. L., Tweden, K., Schroeder, R. F., & Cameron, J. D. (1998). In vivo efficacy of silver-coated (Silzone) infection-resistant polyester fabric against a biofilm-producing bacteria, Staphylococcus epidermidis. Journal of Heart Valve Disease, 7, 524–530.

    CAS  Google Scholar 

  202. Illingworth, B., Bianco, R. W., & Weisberg, S. (2000). In vivo efficacy of silver- coated fabric against Staphylococcus epidermidis. Journal of Heart Valve Disease, 9, 135–141.

    CAS  Google Scholar 

  203. Darouiche, R. O., Meade, R., Mansouri, M., & Raad, I. I. (1998). In vivo efficacy of antimicrobial-coated fabric from prosthetic heart valve sewing rings. Journal of Heart Valve Disease, 7, 639–646.

    CAS  Google Scholar 

  204. Nakamoto, D. A., Rosenfield, M. L., Haaga, J. R., Merritt, K., Sachs, P. B., Hutton, M. C., et al. (1994). Young investigator award. In vivo treatment of infected prosthetic graft material with urokinase: An animal model. Journal of Vascular and Interventional Radiology, 5, 549–552.

    Article  CAS  PubMed  Google Scholar 

  205. Garrison, J. R., Jr., Henke, P. K., Smith, K. R., Brittian, K. R., Lam, T. M., Peyton, J. C., et al. (1997). In vitro and in vivo effects of rifampin on Staphylococcus epidermidis graft infections. ASAIO Journal, 43, 8–12.

    Article  CAS  PubMed  Google Scholar 

  206. Chilukuri, D. M., & Shah, J. C. (2005). Local delivery of vancomycin for the prophylaxis of prosthetic device-related infections. Pharmaceutical Research, 22, 563–572.

    Article  CAS  PubMed  Google Scholar 

  207. Rediske, A. M., Roeder, B. L., Nelson, J. L., Robison, R. L., Schaalje, G. B., Robison, R. A., et al. (2000). Pulsed ultrasound enhances the killing of Escherichia coli biofilms by aminoglycoside antibiotics in vivo. Antimicrobial Agents and Chemotherapy, 44, 771–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Engelsman, A. F., van Dam, G. M., van der Mei, H. C., Busscher, H. J., & Ploeg, R. J. (2010). In vivo evaluation of bacterial infection involving morphologically different surgical meshes. Annals of Surgery, 251, 133–137.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Materials Science and Engineering, National Institute of Technology (KOSEN), Shiroko-cho, Suzuka, Mie, Japan

    Hideyuki Kanematsu

  2. Department of Electrical and Computer Engineering, Clarkson University, Potsdam, NY, USA

    Dana M. Barry

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  1. Hideyuki Kanematsu
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  2. Dana M. Barry
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Kanematsu, H., Barry, D.M. (2020). Laboratory Biofilm Reactors. In: Formation and Control of Biofilm in Various Environments. Springer, Singapore. https://doi.org/10.1007/978-981-15-2240-6_5

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