Challenges in linking preclinical anti-microbial research strategies with clinical outcomes for device-associated infections

European Cells and Materials

Volumn 28, Issue , 2014, Pages 112-128

  Moriarty, T F ^a   Grainger, D W ^b   Richards, R G ^a  

^a AO RESEARCH INSTITUTE   (Switzerland)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Antibiotic resistance; Clinical translational research; In vitro in vivo correlations; Infection strategy; Medical implants

Indexed keywords

ANTIBIOTIC AGENT; ANTIBIOTIC BONE CEMENT; ANTIINFECTIVE AGENT; BIOMATERIAL;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM DETECTION; BIOFILM; BIOLUMINESCENCE; BIOMATERIAL ASSOCIATED INFECTION; CLINICAL EFFECTIVENESS; CLINICAL RESEARCH; DEVICE INFECTION; DEVICE SAFETY; DRUG CHOICE; DRUG RESEARCH; DRUG SCREENING; EX VIVO STUDY; FLUORESCENCE IMAGING; FOREIGN BODY; HOST RANGE; HUMAN; IMPLANTATION; IN VITRO STUDY; IN VIVO STUDY; INSTRUMENT STERILIZATION; MEDICAL DEVICE; MEDICAL DEVICE CONTAMINATION; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; TRANSLATIONAL RESEARCH; VACCINE FAILURE; ANIMAL; CLINICAL TRIAL (TOPIC); MICROBIOLOGY; PROCEDURES; PROSTHESIS-RELATED INFECTIONS;

ANIMALS; ANTI-BACTERIAL AGENTS; CLINICAL TRIALS AS TOPIC; DRUG EVALUATION, PRECLINICAL; HUMANS; PROSTHESIS-RELATED INFECTIONS;

EID: 84907816559     PISSN: 14732262     EISSN: None     Source Type: Journal    
DOI: 10.22203/eCM.v028a09     Document Type: Article

References (135)

1. Aaron SD, Vandemheen KL, Ferris W, Fergusson D, Tullis E, Haase D, Berthiaume Y, Brown N, Wilcox P, Yozghatlian V, Bye P, Bell S, Chan F, Rose B, Jeanneret A, Stephenson A, Noseworthy M, Freitag A, Paterson N, Doucette S, Harbour C, Ruel M, MacDonald N (2005) Combination antibiotic susceptibility testing to treat exacerbations of cystic fibrosis associated with multiresistant bacteria: a randomised, double-blind, controlled clinical trial. Lancet 366: 463-471.
2. Alexander JW, Van SH, Vanoss K, Hooker EA, Edwards MJ (2013) Surveillance of bacterial colonization in operating rooms. Surg Infect (Larchmt) 14: 345-351.
3. Allo MD, Tedesco M (2005) Operating room management: operative suite considerations, infection control. Surg Clin North Am 85: 1291-1297, xii.
4. An YH, Friedman RJ (1998) Animal models of orthopedic implant infection. J Invest Surg 11: 139-146.
5. Berkes M, Obremskey WT, Scannell B, Ellington JK, Hymes RA, Bosse M, Southeast Fracture C (2010) Maintenance of hardware after early postoperative infection following fracture internal fixation. J Bone Joint Surg Am 92: 823-828.
6. Botelho-Nevers E, Verhoeven P, Paul S, Grattard F, Pozzetto B, Berthelot P, Lucht F (2013) Staphylococcal vaccine development: review of past failures and plea for a future evaluation of vaccine efficacy not only on staphylococcal infections but also on mucosal carriage. Expert Rev Vaccines 12: 1249-1259.
7. Brooks B, Brooks A, Grainger D (2013)Antimicrobial medical devices in preclinical development and clinical use. In: Biomaterials Associated Infection (Moriarty TF, Zaat SAJ, Busscher HJ, eds), Springer New York, pp 307- 354.
8. Brown M, Kowalski R, Zorman J, Wang XM, Towne V, Zhao Q, Secore S, Finnefrock AC, Ebert T, Pancari G, Isett K, Zhang Y, Anderson AS, Montgomery D, Cope L, McNeely T (2009) Selection and characterization of murine monoclonal antibodies to Staphylococcus aureus iron-regulated surface determinant B with functional activity in vitro and in vivo. Clin Vaccine Immunol 16: 1095-1104.
9. Bubeck WJ, Bae T, Otto M, Deleo FR, Schneewind O (2007) Poring over pores: alpha-hemolysin and Panton- Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13: 1405-1406.
10. Busscher HJ, van der Mei HC (2012) How do bacteria know they are on a surface and regulate their response to an adhering state? PLoS Pathog 8: e1002440.
11. Busscher HJ, van der Mei HC, Subbiahdoss G, Jutte PC, van den Dungen JJ, Zaat SA, Schultz MJ, Grainger DW (2012) Biomaterial-associated infection: locating the finish line in the race for the surface. Sci Transl Med 4: 153rv110.
12. Calabro L, Lutton C, Din A, Richards RG, Moriarty TF (2013)Animal models of orthopedic implant-related infection. In: Biomaterials Associated Infection (Moriarty TF, Zaat SAJ, Busscher HJ, eds), Springer New York, pp 273-304.
13. Campoccia D, Montanaro L, Moriarty TF, Richards RG, Ravaioli S, Arciola CR (2008) The selection of appropriate bacterial strains in preclinical evaluation of infection-resistant biomaterials. Int J Artif Organs 31: 841-847.
14. Chaffin DO, Taylor D, Skerrett SJ, Rubens CE (2012) Changes in the Staphylococcus aureus transcriptome during early adaptation to the lung. PLoSOne 7: e41329.
15. Chagnot C, Zorgani MA, Astruc T, Desvaux M (2013) Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 4: 303.
16. Chan PF, Foster SJ (1998) The role of environmental factors in the regulation of virulence-determinant expression in Staphylococcus aureus 8325-4. Microbiology 144: 2469-2479.
17. Clarke SR, Foster SJ (2006) Surface adhesins of Staphylococcus aureus. Adv Microb Physiol 51: 187-224.
18. Collins J, Rudkin J, Recker M, Pozzi C, O'Gara JP, Massey RC (2010) Offsetting virulence and antibiotic resistance costs by MRSA. ISMEJ 4: 577-584.
19. Cremieux AC, Dumitrescu O, Lina G, Vallee C, Cote JF, Muffat-Joly M, Lilin T, Etienne J, Vandenesch F, Saleh- Mghir A (2009) Panton-valentine leukocidin enhances the severity of community-associated methicillin-resistant Staphylococcus aureus rabbit osteomyelitis. PLoSOne 4: e7204.
20. Daghighi S, Sjollema J, Dijkstra RJ, Jaspers V, Zaat SA, van der Mei HC, Busscher HJ (2014) Real-time quantification of matrix metalloproteinase and integrin alphavbeta3 expression during biomaterial-associated infection in a murine model. Eur Cell Mater 27: 26-37.
21. Dalstrom DJ, Venkatarayappa I, Manternach AL, Palcic MS, Heyse BA, Prayson MJ (2008) Time-dependent contamination of opened sterile operating-room trays. J Bone Joint Surg Am 90: 1022-1025.
22. Dalton T, Dowd SE, Wolcott RD, Sun Y, Watters C, Griswold JA, Rumbaugh KP (2011) An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoSOne 6: e27317.
23. Darouiche R (2013)Antimicrobial-modified vascular catheters. In: Biomaterials Associated Infection (Moriarty TF, Zaat SAJ, Busscher HJ, eds), Springer New York, pp 485-503.
24. Deleo FR, Otto M, Kreiswirth BN, Chambers HF (2010) Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557-1568.
25. Diep BA, Palazzolo-Ballance AM, Tattevin P, Basuino L, Braughton KR, Whitney AR, Chen L, Kreiswirth BN, Otto M, Deleo FR, Chambers HF (2008) Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoSOne 3: e3198.
26. Duan K, Dammel C, Stein J, Rabin H, Surette MG (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
27. Ecker DJ, Sampath R, Massire C, Blyn LB, Hall TA, Eshoo MW, Hofstadler SA (2008) Ibis T5000: a universal biosensor approach for microbiology. Nat Rev Microbiol 6: 553-558.
28. Elasri MO, Thomas JR, Skinner RA, Blevins JS, Beenken KE, Nelson CL, Smeltzer MS (2002) Staphylococcus aureus collagen adhesin contributes to the pathogenesis of osteomyelitis. Bone 30: 275-280.
29. Elek SD, Conen PE (1957) The virulence of Staphylococcus pyogenes for man; a study of the problems of wound infection. Br J Exp Pathol 38: 573-586.
30. Fazli M, Bjarnsholt T, Kirketerp-Moller K, Jorgensen B, Andersen AS, Krogfelt KA, Givskov M, Tolker-Nielsen T (2009) Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47: 4084-4089.
31. Fisher CJ, Jr., Agosti JM, Opal SM, Lowry SF, Balk RA, Sadoff JC, Abraham E, Schein RM, Benjamin E (1996) Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. N Engl J Med 334: 1697-1702.
32. Fitzgerald RH, Jr. (1979) Microbiologic environment of the conventional operating room. Arch Surg 114: 772-775.
33. Fluckiger U, Ulrich M, Steinhuber A, Doring G, Mack D, Landmann R, Goerke C, Wolz C (2005) Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect Immun 73: 1811- 1819.
34. Fowler VG, Allen KB, Moreira ED, Moustafa M, Isgro F, Boucher HW, Corey GR, Carmeli Y, Betts R, Hartzel JS, Chan IS, McNeely TB, Kartsonis NA, Guris D, Onorato MT, Smugar SS, DiNubile MJ, Sobanjo-ter Meulen A (2013) Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: a randomized trial. JAMA 309: 1368-1378.
35. Fuchs T, Stange R, Schmidmaier G, Raschke MJ (2011) The use of gentamicin-coated nails in the tibia: preliminary results of a prospective study. Arch Orthop Trauma Surg 131: 1419-1425.
36. Garzoni C, Francois P, Huyghe A, Couzinet S, Tapparel C, Charbonnier Y, Renzoni A, Lucchini S, Lew DP, Vaudaux P, Kelley WL, Schrenzel J (2007) A global view of Staphylococcus aureus whole genome expression upon internalization in human epithelial cells. BMC Genomics 8: 171.
37. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Vandenesch F, Piemont Y, Brousse N, Floret D, Etienne J (2002) Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 359: 753-759.
38. Goerke C, Wolz C (2004) Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. Int J Med Microbiol 294: 195- 202.
39. Goerke C, Campana S, Bayer MG, Doring G, Botzenhart K, Wolz C (2000) Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun 68: 1304-1311.
40. Goerke C, Fluckiger U, Steinhuber A, Zimmerli W, Wolz C (2001) Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infection resolved by direct quantitative transcript analysis. Mol Microbiol 40: 1439- 1447.
41. Goerke C, Fluckiger U, Steinhuber A, Bisanzio V, Ulrich M, Bischoff M, Patti JM, Wolz C (2005) Role of Staphylococcus aureus global regulators sae and sigmaB in virulence gene expression during device-related infection. Infect Immun 73: 3415-3421.
42. Gottenbos B, van der Mei HC, Busscher HJ (1999) Models for studying initial adhesion and surface growth in biofilm formation on surfaces. Methods Enzymol 310: 523-534.
43. Grainger DW, van der Mei HC, Jutte PC, van den Dungen JJ, Schultz MJ, van der Laan BF, Zaat SA, Busscher HJ (2013) Critical factors in the translation of improved antimicrobial strategies for medical implants and devices. Biomaterials 34: 9237-9243.
44. Gristina AG, Naylor P, Myrvik Q (1988) Infections from biomaterials and implants: a race for the surface. Med Prog Technol 14: 205-224.
45. Gristina AG, Naylor PT, Myrvik QN (1991) Mechanisms of musculoskeletal sepsis. Orthop Clin North Am 22: 363- 371.
46. Guillou PJ (1993) Biological variation in the development of sepsis after surgery or trauma. Lancet 342: 217-220.
47. Gustilo RB, Anderson JT (1976) Prevention of infection in the treatment of one thousand and twenty-five open fractures of long bones: retrospective and prospective analyses. J Bone Joint Surg Am 58: 453-458.
48. Haja MH, Corris PA, Nicholson A, Perry JD, Meachery G, Marrs EC, Peart S, Fagan C, Lordan JL, Fisher AJ, Gould FK (2012) Targeted antibiotic prophylaxis for lung transplantation in cystic fibrosis patients colonised with Pseudomonas aeruginosa using multiple combination bactericidal testing. J Transplant 2012: 135738.
49. Hanssen AD, Osmon DR, Nelson CL (1997) Prevention of deep periprosthetic joint infection. Instr Course Lect 46: 555-567.
50. Hardes J, Ahrens H, Gebert C, Streitbuerger A, Buerger H, Erren M, Gunsel A, Wedemeyer C, Saxler G, Winkelmann W, Gosheger G (2007) Lack of toxicological side-effects in silver-coated megaprostheses in humans. Biomaterials 28: 2869-2875.
51. Hendricks KJ, Burd TA, Anglen JO, Simpson AW, Christensen GD, Gainor BJ (2001) Synergy between Staphylococcus aureus and Pseudomonas aeruginosa in a rat model of complex orthopaedic wounds. J Bone Joint Surg Am 83-A: 855-861.
52. Hoch RC, Rodriguez R, Manning T, Bishop M, Mead P, Shoemaker WC, Abraham E (1993) Effects of accidental trauma on cytokine and endotoxin production. Crit Care Med 21: 839-845.
53. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35: 322-332.
54. Holtfreter S, Kolata J, Broker BM (2010) Towards the immune proteome of Staphylococcus aureus - The anti-S. aureus antibody response. Int J Med Microbiol 300: 176- 192.
55. Howard JL, Hanssen AD (2007) Principles of a clean operating room environment. J Arthroplasty 22: 6-11.
56. Howe TS, Erlich G, Koh JS, Ng AC, Costerton W (2013) A case of an atypical femoral fracture associated with bacterial biofilm - pathogen or bystander? Osteoporos Int 24: 1765-1766.
57. Hudson MC, Ramp WK, Frankenburg KP (1999) Staphylococcus aureus adhesion to bone matrix and bone-associated biomaterials. FEMS Microbiol Lett 173: 279-284.
58. James GA, Swogger E, Wolcott R, Pulcini E, Secor P, Sestrich J, Costerton JW, Stewart PS (2008) Biofilms in chronic wounds. Wound Repair Regen 16: 37-44.
59. James RC, MacLeod CJ (1961) Induction of staphylococcal infections in mice with small inocula introduced on sutures. Br J Exp Pathol 42: 266-277.
60. Kadurugamuwa JL, Sin L, Albert E, Yu J, Francis K, DeBoer M, Rubin M, Bellinger-Kawahara C, Parr TRJ Jr, Contag PR (2003) Direct continuous method for monitoring biofilm infection in a mouse model. Infect Immun 71: 882-890.
61. Kalicke T, Schlegel U, Printzen G, Schneider E, Muhr G, Arens S (2003) Influence of a standardized closed soft tissue trauma on resistance to local infection. An experimental study in rats. J Orthop Res 21: 373-378.
62. Kasemo B, Lausmaa J (1994) Material-tissue interfaces: the role of surface properties and processes. Environ Health Perspect 102 Suppl 5: 41-45.
63. Katsikogianni M, Missirlis YF (2004) Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. Eur Cell Mater 8: 37-57.
64. Keays T, Ferris W, Vandemheen KL, Chan F, Yeung SW, Mah TF, Ramotar K, Saginur R, Aaron SD (2009) A retrospective analysis of biofilm antibiotic susceptibility testing: a better predictor of clinical response in cystic fibrosis exacerbations. J Cyst Fibros 8: 122-127.
65. Kim A, Kuti JL, Nicolau DP (2009) Probability of pharmacodynamic target attainment with standard and prolonged-infusion antibiotic regimens for empiric therapy in adults with hospital-acquired pneumonia. Clin Ther 31: 2765-2778.
66. Kim KS, Anthony BF (1981) Importance of bacterial growth phase in determining minimal bactericidal concentrations of penicillin and methicillin. Antimicrob Agents Chemother 19: 1075-1077.
67. Kollef M (2013) Preventive strategies in VAP: Focus on silver-coated endotracheal tubes. In: Biomaterials Associated Infection (Moriarty TF, Zaat SAJ, Busscher HJ, eds), Springer New York, pp 531-555.
68. Korgaonkar A, Trivedi U, Rumbaugh KP, Whiteley M (2013) Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proc Natl Acad Sci USA 110: 1059-1064.
69. Krettek C (1998) [Fracture and soft tissue damage]. Chirurg 69: 684-700.
70. Kuijer R, Jansen EJ, Emans PJ, Bulstra SK, Riesle J, Pieper J, Grainger DW, Busscher HJ (2007) Assessing infection risk in implanted tissue-engineered devices. Biomaterials 28: 5148-5154.
71. Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, McNeely T, Noble L, Brown MJ, Zorman JK, Wang XM, Pancari G, Fan H, Isett K, Burgess B, Bryan J, Brownlow M, George H, Meinz M, Liddell ME, Kelly R, Schultz L, Montgomery D, Onishi J, Losada M, Martin M, Ebert T, Tan CY, Schofield TL, Nagy E, Meineke A, Joyce JG, Kurtz MB, Caulfield MJ, Jansen KU, McClements W, Anderson AS (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 74: 2215- 2223.
72. Lammers A, Kruijt E, van de Kuijt C, Nuijten PJ, Smith HE (2000) Identification of Staphylococcus aureus genes expressed during growth in milk: a useful model for selection of genes important in bovine mastitis? Microbiology 146: 981-987.
73. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29: 1128-1132.
74. Lindsay JA, Holden MT (2006) Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct Integr Genomics 6: 186-201.
75. Lipinska U, Hermans K, Meulemans L, Dumitrescu O, Badiou C, Duchateau L, Haesebrouck F, Etienne J, Lina G (2011) Panton-Valentine leukocidin does play a role in the early stage of Staphylococcus aureus skin infections: a rabbit model. PLoSOne 6: e22864.
76. Livermore DM (2011) Discovery research: the scientific challenge of finding new antibiotics. J Antimicrob Chemother 66: 1941-1944.
77. Loffler B, Hussain M, Grundmeier M, Bruck M, Holzinger D, Varga G, Roth J, Kahl BC, Proctor RA, Peters G (2010) Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog 6: e1000715.
78. Lynch RJ, Englesbe MJ, Sturm L, Bitar A, Budhiraj K, Kolla S, Polyachenko Y, Duck MG, Campbell DA, Jr. (2009) Measurement of foot traffic in the operating room: implications for infection control. Am J Med Qual 24: 45-52.
79. Massey RC, Dissanayeke SR, Cameron B, Ferguson D, Foster TJ, Peacock SJ (2002) Functional blocking of Staphylococcus aureus adhesins following growth in ex vivo media. Infect Immun 70: 5339-5345.
80. Mastropaolo MD, Evans NP, Byrnes MK, Stevens AM, Robertson JL, Melville SB (2005) Synergy in polymicrobial infections in a mouse model of type 2 diabetes. Infect Immun 73: 6055-6063.
81. Matsukawa M, Kunishima Y, Takahashi S, Takeyama K, Tsukamoto T (2005) Bacterial colonization on intraluminal surface of urethral catheter. Urology 65: 440-444.
82. McAleese FM, Walsh EJ, Sieprawska M, Potempa J, Foster TJ (2001) Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J Biol Chem 276: 29969-29978.
83. Mohler KM, Torrance DS, Smith CA, Goodwin RG, Stremler KE, Fung VP, Madani H, Widmer MB (1993) Soluble tumor necrosis factor (TNF) receptors are effective therapeutic agents in lethal endotoxemia and function simultaneously as both TNF carriers and TNF antagonists. J Immunol 151: 1548-1561.
84. Molina-Manso D, del PG, Ortiz-Perez A, Manrubia- Cobo M, Gomez-Barrena E, Cordero-Ampuero J, Esteban J (2013) In vitro susceptibility to antibiotics of staphylococci in biofilms isolated from orthopaedic infections. Int J Antimicrob Agents 41: 521-523.
85. Montanaro L, Campoccia D, Arciola CR (2008) Nanostructured materials for inhibition of bacterial adhesion in orthopedic implants: a minireview. Int J Artif Organs 31: 771-776.
86. Moriarty TF, Elborn JS, Tunney MM (2007) Effect of pH on the antimicrobial susceptibility of planktonic and biofilm-grown clinical Pseudomonas aeruginosa isolates. Br J Biomed Sci 64: 101-104.
87. Moriarty TF, Poulsson AHC, Rochford ETJ, Richards RG (2011) Bacterial adhesion and biomaterial surfaces. In: Comprehensive Biomaterials (Paul D, ed), Elsevier, Oxford, pp 75-100.
88. Moskowitz SM, Emerson JC, McNamara S, Shell RD, Orenstein DM, Rosenbluth D, Katz MF, Ahrens R, Hornick D, Joseph PM, Gibson RL, Aitken ML, Benton WW, Burns JL (2011) Randomized trial of biofilm testing to select antibiotics for cystic fibrosis airway infection. Pediatr Pulmonol 46: 184-192.
89. Neut D, Kluin OS, Thompson J, van der Mei HC, Busscher HJ (2010) Gentamicin release from commercially-available gentamicin-loaded PMMA bone cements in a prosthesis-related interfacial gap model and their antibacterial efficacy. BMC Musculoskelet Disord 11: 258.
90. Norden CW (1970) Experimental osteomyelitis. I. A description of the model. J Infect Dis 122: 410-418.
91. Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34: 415-425.
92. Otto M (2010) Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu Rev Microbiol 64: 143-162.
93. Palmer M, Costerton W, Sewecke J, Altman D (2011) Molecular techniques to detect biofilm bacteria in long bone nonunion: a case report. Clin Orthop Relat Res 469: 3037-3042.
94. Panahi P, Stroh M, Casper DS, Parvizi J, Austin MS (2012) Operating room traffic is a major concern during total joint arthroplasty. Clin Orthop Relat Res 470: 2690- 2694.
95. Perl TM, Cullen JJ, Wenzel RP, Zimmerman MB, Pfaller MA, Sheppard D, Twombley J, French PP, Herwaldt LA (2002) Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 346: 1871-1877.
96. Peters BM, Jabra-Rizk MA, O'May GA, Costerton JW, Shirtliff ME (2012) Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev 25: 193-213.
97. Pittet D, Simon A, Hugonnet S, Pessoa-Silva CL, Sauvan V, Perneger TV (2004) Hand hygiene among physicians: performance, beliefs, and perceptions. Ann Intern Med 141: 1-8.
98. Poelstra KA, Barekzi NA, Slunt JB, Schuler TC, Grainger DW (2000) Surgical irrigation with pooled human immunoglobulin G to reduce post-operative spinal implant infection. Tissue Eng 6: 401-411.
99. Poelstra KA, Barekzi NA, Rediske AM, Felts AG, Slunt JB, Grainger DW (2002) Prophylactic treatment of gram-positive and gram-negative abdominal implant infections using locally delivered polyclonal antibodies. J Biomed Mater Res 60: 206-215.
100. Pribaz JR, Bernthal NM, Billi F, Cho JS, Ramos RI, Guo Y, Cheung AL, Francis KP, Miller LS (2012) Mouse model of chronic post-arthroplasty infection: noninvasive in vivo bioluminescence imaging to monitor bacterial burden for long-term study. J Orthop Res 30: 335-340.
101. Proctor RA (2012) Is there a future for a Staphylococcus aureus vaccine? Vaccine 30: 2921-2927.
102. Que YA, Haefliger JA, Piroth L, Francois P, Widmer E, Entenza JM, Sinha B, Herrmann M, Francioli P, Vaudaux P, Moreillon P (2005) Fibrinogen and fibronectin binding cooperate for valve infection and invasion in Staphylococcus aureus experimental endocarditis. J Exp Med 201: 1627-1635.
103. Ramos ER, Reitzel R, Jiang Y, Hachem RY, Chaftari AM, Chemaly RF, Hackett B, Pravinkumar SE, Nates J, Tarrand JJ, Raad II (2011) Clinical effectiveness and risk of emerging resistance associated with prolonged use of antibiotic-impregnated catheters: more than 0.5 million catheter days and 7 years of clinical experience. Crit Care Med 39: 245-251.
104. Rogasch K, Ruhmling V, Pane-Farre J, Hoper D, Weinberg C, Fuchs S, Schmudde M, Broker BM, Wolz C, Hecker M, Engelmann S (2006) Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J Bacteriol 188: 7742-7758.
105. Rooijakkers SH, van Kessel KP, van Strijp JA (2005) Staphylococcal innate immune evasion. Trends Microbiol 13: 596-601.
106. Rudkin JK, Edwards AM, Bowden MG, Brown EL, Pozzi C, Waters EM, Chan WC, Williams P, O'Gara JP, Massey RC (2012) Methicillin resistance reduces the virulence of healthcare-associated methicillin-resistant Staphylococcus aureus by interfering with the agr quorum sensing system. J Infect Dis 205: 798-806.
107. Schafer P, Fink B, Sandow D, Margull A, Berger I, Frommelt L (2008) Prolonged bacterial culture to identify late periprosthetic joint infection: a promising strategy. Clin Infect Dis 47: 1403-1409.
108. Scheman L, Janota M, Lewin P (1941) The Production of Experimental Osteomyelitis. JAMA 117: 1525-1529.
109. Scully IL, Liberator PA, Jansen KU, Anderson AS (2014) Covering all the bases: Preclinical development of an effective vaccine. Front Immunol 5: 109.
110. Sellman BR, Timofeyeva Y, Nanra J, Scott A, Fulginiti JP, Matsuka YV, Baker SM (2008) Expression of Staphylococcus epidermidis SdrG increases following exposure to an in vivo environment. Infect Immun 76: 2950-2957.
111. Sepandj F, Ceri H, Gibb A, Read R, Olson M (2004) Minimum inhibitory concentration (MIC) versus minimum biofilm eliminating concentration (MBEC) in evaluation of antibiotic sensitivity of gram-negative bacilli causing peritonitis. Perit Dial Int 24: 65-67.
112. Sjollema J, Sharma PK, Dijkstra RJ, van Dam GM, van der Mei HC, Engelsman AF, Busscher HJ (2010) The potential for bio-optical imaging of biomaterial-associated infection in vivo. Biomaterials 31: 1984-1995.
113. Smith AL, Fiel SB, Mayer-Hamblett N, Ramsey B, Burns JL (2003) Susceptibility testing of Pseudomonas aeruginosa isolates and clinical response to parenteral antibiotic administration: lack of association in cystic fibrosis. Chest 123: 1495-1502.
114. Stone PW, Larson E, Kawar LN (2002) A systematic audit of economic evidence linking nosocomial infections and infection control interventions: 1990-2000. Am J Infect Control 30: 145-152.
115. Stone PW, Glied SA, McNair PD, Matthes N, Cohen B, Landers TF, Larson EL (2010) CMS changes in reimbursement for HAIs: setting a research agenda. Med Care 48: 433-439.
116. Subbiahdoss G, Kuijer R, Grijpma DW, van der Mei HC, Busscher HJ (2009) Microbial biofilm growth vs. tissue integration: "the race for the surface" experimentally studied. Acta Biomater 5: 1399-1404.
117. Subbiahdoss G, Grijpma DW, van der Mei HC, Busscher HJ, Kuijer R (2010a) Microbial biofilm growth versus tissue integration on biomaterials with different wettabilities and a polymer-brush coating. J Biomed Mater Res A 94: 533-538.
118. Subbiahdoss G, Pidhatika B, Coullerez G, Charnley M, Kuijer R, van der Mei HC, Textor M, Busscher HJ (2010b) Bacterial biofilm formation versus mammalian cell growth on titanium-based mono- and bi-functional coating. Eur Cell Mater 19: 205-213.
119. Subbiahdoss G, Fernandez IC, Domingues JF, Kuijer R, van der Mei HC, Busscher HJ (2011) In vitro interactions between bacteria, osteoblast-like cells and macrophages in the pathogenesis of biomaterial-associated infections. PLoSOne 6: e24827.
120. Sun Y, Dowd SE, Smith E, Rhoads DD, Wolcott RD (2008) In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen 16: 805-813.
121. Trampuz A, Widmer AF (2004) Hand hygiene: a frequently missed lifesaving opportunity during patient care. Mayo Clin Proc 79: 109-116.
122. Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R (2007) Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 357: 654-663.
123. Tunney MM, Patrick S, Curran MD, Ramage G, Hanna D, Nixon JR, Gorman SP, Davis RI, Anderson N (1999) Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene. J Clin Microbiol 37: 3281-3290.
124. Uckay I, Harbarth S, Peter R, Lew D, Hoffmeyer P, Pittet D (2010) Preventing surgical site infections. Expert Rev Anti Infect Ther 8: 657-670.
125. Uckay I, Hoffmeyer P, Lew D, Pittet D (2013) Prevention of surgical site infections in orthopaedic surgery and bone trauma: state-of-the-art update. J Hosp Infect 84: 5-12.
126. Van Oosten M, Schafer T, Gazendam JA, Ohlsen K, Tsompanidou E, de Goffau MC, Harmsen HJ, Crane LM, Lim E, Francis KP, Cheung L, Olive M, Ntziachristos V, van Dijl JM, van Dam GM (2013) Real-time in vivo imaging of invasive- and biomaterial-associated bacterial infections using fluorescently labelled vancomycin. Nat Commun 4: 2584.
127. Von Eiff C, Becker K, Machka K, Stammer H, Peters G (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344: 11-16.
128. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, Welty D, Long RD, Dorward DW, Gardner DJ, Lina G, Kreiswirth BN, Deleo FR (2006) Is Panton- Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194: 1761-1770.
129. Vriesema AJ, Beekhuizen H, Hamdi M, Soufan A, Lammers A, Willekens B, Bakker O, Welten AG, Veltrop MH, van De Gevel JS, Dankert J, Zaat SA (2000) Altered gene expression in Staphylococcus aureus upon interaction with human endothelial cells. Infect Immun 68: 1765-1772.
130. Wichmann MW, Zellweger R, DeMaso CM, Ayala A, Williams C, Chaudry IH (1996) Immune function is more compromised after closed bone fracture and hemorrhagic shock than hemorrhage alone. Arch Surg 131: 995-1000.
131. Widmer AF, Frei R, Rajacic Z, Zimmerli W (1990) Correlation between in vivo and in vitro efficacy of antimicrobial agents against foreign body infections. J Infect Dis 162: 96-102.
132. Wiltshire MD, Foster SJ (2001) Identification and analysis of Staphylococcus aureus components expressed by a model system of growth in serum. Infect Immun 69: 5198-5202.
133. Xiong YQ, Willard J, Yeaman MR, Cheung AL, Bayer AS (2006) Regulation of Staphylococcus aureus alpha-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. J Infect Dis 194: 1267-1275.
134. Yarwood JM, McCormick JK, Paustian ML, Kapur V, Schlievert PM (2002) Repression of the Staphylococcus aureus accessory gene regulator in serum and in vivo. J Bacteriol 184: 1095-1101.
135. Zimmerli W, Waldvogel FA, Vaudaux P, Nydegger UE (1982) Pathogenesis of foreign body infection: description and characteristics of an animal model. J Infect Dis 146: 487-497.