Polymicrobial wound infections: Pathophysiology and current therapeutic approaches

International Journal of Pharmaceutics

Volumn 463, Issue 2, 2014, Pages 119-126

  Bertesteanu, Serban ^a   Triaridis, Stefanos ^b   Stankovic, Milan ^c   Lazar, Veronica ^d   Chifiriuc, Mariana Carmen ^d   Vlad, Mihaela ^e   Grigore, Raluca ^a  

^a CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^c UNIVERSITY OF NI   (Serbia)

^d UNIVERSITY OF BUCHAREST   (Romania)

^e UNIVERSITY POLITEHNICA OF BUCHAREST   (Romania)

Author keywords

Biofilm; Infection; Polymicrobial; Therapy; Vaccination; Wound

Indexed keywords

BIOFILM; INFECTION; POLYMICROBIAL; THERAPY; VACCINATION; WOUND;

ANIMALS; BIOFILMS; HUMANS; WOUND INFECTION;

EID: 84894225530     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2013.12.012     Document Type: Article

References (151)

1. K.G. Alberti, and P.Z. Zimmet Definition, diagnosis and classification of diabetes mellitus and its complications: Part 1: Diagnosis and classification of diabetes mellitus provisional report of a WHO consultation Diabet. Med. 15 1998 539 553 (Pubitemid 28319935)
2. I. Anghel, A.M. Grumezescu, A.M. Holban, A. Ficai, A.G. Anghel, and M.C. Chifiriuc Biohybrid nanostructured iron oxide nanoparticles and Satureja hortensis to prevent fungal biofilm development Int. J. Mol. Sci. 14 2013 18110 18123
3. D.G. Armstrong, L.A. Lavery, and A.J. Boulton Negative pressure wound therapy via vacuum-assisted closure following partial foot amputation: what is the role of wound chronicity? Int. Wound J. 4 2007 79 86
4. C.E. Attinger, J.E. Janis, J. Steinberg, J. Schwartz, A. Al-Attar, and K. Couch Clinical approach to wounds: debridement and wound bed preparation including the use of dressings and wound-healing adjuvants Plast. Reconstr. Surg. 117 2006 72S 109S (Pubitemid 44317773)
5. E.A. Ayello, and J.E. Cuddigan Debridement: controlling the necrotic/cellular burden Adv. Skin Wound 17 2004 66 75
6. P.C. Balaure, E. Andronescu, A.M. Grumezescu, A. Ficai, K.S. Huang, C.H. Yang, Y.S. Lin, and C.M. Chifiriuc Fabrication, characterization and in vitro profile based interaction with eukaryotic and prokaryotic cells of alginate-chitosan-silica biocomposite Int. J. Pharm. 441 2013 555 561
7. L.M. Bariar, S.M. Vasenwala, A. Malik, G.H. Ansari, and T.E. Chowdhury A clinicopathological study of infections in burn patients and importance of biopsy J. Indian Med. Soc. 95 1997 573 575
8. R.C. Barnes Hyperbaric oxygen is beneficial for diabetic foot wounds Clin. Infect. Dis. 43 2006 188 192
9. C.E. Black, and J.W. Costerton Current concepts regarding the effect of wound microbial ecology and biofilms on wound healing Surg. Clin. North Am. 90 2010 1147 1160
10. T.J. Blokhuis Formulations and delivery vehicles for bone morphogenetic proteins: latest advances and future directions Injury 40 2009 S8 S11
11. A.J. Boulton What you can't feel can hurt you J. Vasc. Surg. 52 2010 28S 30S
12. P.G. Bowler The anaerobic and aerobic microbiology of wounds: a review Wounds 10 1998 170 178
13. P.G. Bowler, and B.J. Davies The microbiology of infected and noninfected leg ulcers Int. J. Dermatol. 38 1999 101 106
14. P.G. Bowler, B.I. Duerden, and D.G. Armstrong Wound microbiology and associated approaches to wound management Clin. Microbiol. Rev. 14 2001 244 269 (Pubitemid 32294670)
15. F.L. Bowling, E.B. Jude, and A.J. Boulton MRSA and diabetic foot wounds: contaminating or infecting organisms? Curr. Diab. Rep. 9 2009 440 444
16. R.A. Brady, J.G. Leid, A.K. Camper, J.W. Costerton, and M.E. Shirtliff Identification of Staphylococcus aureus proteins recognized by the antibody-mediated immune response to a biofilm infection Infect. Immun. 74 2006 3415 3426 (Pubitemid 43794532)
17. L.K. Branski, G.G. Gauglitz, D.N. Herndon, and M.G. Jeschke A review of gene and stem cell therapy in cutaneous wound healing Burns 35 2009 171 180
18. W.C. Breidenbach, and S. Trager Quantitative culture technique and infection in complex wounds of the extremities closed with free flaps Plast. Reconstr. Surg. 95 1995 860 865
19. B.M. Peters, M.A. Jabra-Rizk, G.A. O'May, J. William Costerton, and M.E. Shirtliff Polymicrobial interactions: impact on pathogenesis and human disease Clin. Microbiol. Rev. 25 2012 193 213
20. K.A. Brogden, J.M. Guthmiller, and C.E. Taylor Human polymicrobial infections Lancet 365 2005 253 255 (Pubitemid 40138019)
21. I. Brook Aerobic and anaerobic microbiology of necrotising fasciitis in children Pediatr. Dermatol. 13 1996 281 284 (Pubitemid 26260471)
22. I. Brook Aerobic and anaerobic microbiology of infections after trauma in children J. Accid. Emerg. Med. 15 1998 162 167
23. I. Brook, and S.M. Finegold Aerobic and anaerobic bacteriology of cutaneous abscesses in children Pediatrics 67 1981 891 895 (Pubitemid 11005278)
24. I. Brook, and E.H. Frazier Aerobic and anaerobic bacteriology of wounds and cutaneous abscesses Arch. Surg. 125 1990 1445 1451 (Pubitemid 20375707)
25. I. Brook, and E.H. Frazier The aerobic and anaerobic bacteriology of perirectal abscesses J. Clin. Microbiol. 35 1997 2974 2976 (Pubitemid 27452447)
26. I. Brook, and E.H. Frazier Aerobic and anaerobic microbiology of infection after trauma Am. J. Emerg. Med. 16 1998 585 591 (Pubitemid 28465584)
27. I. Brook, and E.H. Frazier Aerobic and anaerobic microbiology of chronic venous ulcers Int. J. Dermatol. 137 1998 426 428 (Pubitemid 28284869)
28. I. Brook, and J.G. Randolph Aerobic and anaerobic bacterial flora of burns in children J. Trauma 21 1981 313 318 (Pubitemid 11099158)
29. A. Casadevall, and L.J. Pirofski Host-pathogen interactions: the attributes of virulence J. Infect. Dis. 184 2001 37 44
30. G. Cazander, J.S. Pawiroredjo, C.M. Vandenbroucke-Grauls, M.W. Schreurs, and G.N. Jukema Synergism between maggot excretions and antibiotics Wound Repair Regen. 18 2010 637 642
31. L. Cen, W. Liu, L. Cui, W. Zhang, and Y. Cao Collagen tissue engineering: development of novel biomaterials and applications Pediatr. Res. 63 2008 492 496 (Pubitemid 351572218)
32. M.C. Chifiriuc, A.M. Grumezescu, C. Saviuc, C. Croitoru, D.E. Mihaiescu, and V. Lazar Improved antibacterial activity of cephalosporins loaded in magnetic chitosan microspheres Int. J. Pharm. 436 2012 201 205
33. M.C. Chifiriuc, A.M. Grumezescu, E. Andronescu, A. Ficai, A.I. Cotar, V. Grumezescu, E. Bezirtzoglou, V. Lazar, and R. Radulescu Water dispersible magnetite nanoparticles influence the efficacy of antibiotics against planktonic and biofilm embedded Enterococcus faecalis cells Anaerobe 22 2013 14 19
34. M.E. Ciaravino, M.L. Friedell, and T.C. Kammerlocher Is hyperbaric oxygen a useful adjunct in the management of problem lower extremity wounds? Ann. Vasc. Surg. 10 1996 558 562 (Pubitemid 27021385)
35. M.A. Cohen, and W.H. Eaglstein Recombinant human platelet-derived growth factor gel speeds healing of acute full-thickness punch biopsy wounds J. Am. Acad. Dermatol. 45 2001 857 862 (Pubitemid 33096625)
36. R.A. Cooper, and P.C. Molan Honey in wound care J. Wound Care 8 1999 340
37. A.I. Cotar, A.M. Grumezescu, K.S. Huang, M.C. Chifiriuc, and R. Radulescu Magnetite nanoparticles influence the efficacy of antibiotics against biofilm embedded Staphylococcus aureus cells Biointerface Res. Appl. Chem. 3 2013 559 565
38. B. Cullen, P.W. Watt, and C. Lundqvist The role of oxidized regenerated cellulose/collagen in chronic wound repair and its potential mechanism of action Int. J. Biochem. Cell Biol. 34 2002 1544 1556
39. T. Dai, G.P. Tegos, M. Burkatovskaya, A.P. Castano, and M.R. Hamblin Chitosan acetate bandage as a topical antimicrobial dressing for infected burns Antimicrob. Agents Chemother. 53 2009 393 400
40. T. Dai, M. Tanaka, Y.Y. Huang, and M.R. Hamblin Chitosan preparations for wounds and burns: antimicrobial and wound-healing effects Expert Rev. Anti Infect. Ther. 9 2011 857 879
41. T.N. Demidova-Rice, M.R. Hamblin, and I.M. Herman Acute and impaired wound healing: pathophysiology and current methods for drug delivery: Part 1: Normal and chronic wounds: biology, causes, and approaches to care Adv. Skin Wound Care 25 2012 304 314
42. A. Di Poto, M.S. Sbarra, G. Provenza, L. Visai, and P. Speziale The effect of photodynamic treatment combined with antibiotic action or host defense mechanisms on Staphylococcus aureus biofilms Biomaterials 30 2009 3158 3166
43. L.N. Diebel, D.M. Liberati, C.A. Diglio, S.A. Dulchavsky, and W.J. Brown Synergistic effects of Candida and Escherichia coli on gut barrier function J. Trauma 47 1999 1045 1050
44. R.M. Donlan Preventing biofilms of clinically relevant organisms using bacteriophage Trends Microbiol. 17 2009 66 72
45. B.I. Duerden Virulence factors in anaerobes Clin. Infect. Dis. 18 1994 S253 S259
46. S.A. Eming, T. Krieg, and J.M. Davidson Inflammation in wound repair: molecular and cellular mechanisms J. Invest. Dermatol. 127 2007 514 525
47. V. Falanga Wound healing and its impairment in the diabetic foot Lancet 366 2005 1736 1743 (Pubitemid 41587454)
48. D.N. Frank, A. Wysocki, D.D. Specht-Glick, A. Rooney, R.A. Feldman, A.L. Amand, N.R. Pace, and J.D. Trent Microbial diversity in chronic open wounds Wound Repair Regen. 17 2009 163 172
49. H. Galkowska, U. Wojewodzka, and W.L. Olszewski Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers Wound Repair Regen. 14 2006 558 565 (Pubitemid 44470072)
50. S.E. Gardner, and R.A. Frantz Wound bioburden and infection-related complications in diabetic foot ulcers Biol. Res. Nurs. 10 2008 44 53
51. D.N. Gerding Foot infections in diabetic patients: the role of anaerobes Clin. Infect. Dis. 20 1995 S283 S288
52. D.W. Gilroy, T. Lawrence, M. Perretti, and A.G. Rossi Inflammatory resolution: new opportunities for drug discovery Nat. Rev. Drug Discov. 3 2004 401 416 (Pubitemid 38618123)
53. K. Gjødsbøl, J.J. Christensen, T. Karlsmark, B. Jørgensen, B.M. Klein, and K.A. Krogfelt Multiple bacterial species reside in chronic wounds: a longitudinal study Int. Wound J. 3 2006 225 231
54. V. Gontcharova, E. Youn, Y. Sun, R.D. Wolcott, and S.E. Dowd A comparison of bacterial composition in diabetic ulcers and contralateral intact skin Open Microbiol. J. 4 2010 8 19
55. M. Greener The fifty year war against infection Pharm. Times 1998 34 37
56. A.M. Grumezescu, C. Saviuc, A. Holban, R. Hristu, G. Stanciu, C. Chifiriuc, D. Mihaiescu, P. Balaure, and V. Lazar Magnetic chitosan for drug targeting and in vitro drug delivery response Biointerface Res. Appl. Chem. 1 2011 160
57. A.M. Grumezescu, E. Andronescu, A. Ficai, C. Bleotu, D.E. Mihaiescu, and M.C. Chifiriuc Synthesis, characterization and in vitro assessment of the magnetic chitosan-carboxymethylcellulose biocomposite interactions with the prokaryotic and eukaryotic cells Int. J. Pharm. 436 2012 771 777
58. A.M. Grumezescu, C.M. Chifiriuc, C. Saviuc, V. Grumezescu, R. Hristu, D. Mihaiescu, G.A. Stanciu, and E. Andronescu Hybrid nanomaterial for stabilizing the antibiofilm activity of Eugenia carryophyllata essential oil IEEE T. NanoBioSci. 11 2012 360 365
59. A.M. Grumezescu, E. Andronescu, M.G. Albu, A. Ficai, and D. Dragu Wound dressing based collagen biomaterials containing usnic acid as quorum sensing inhibitor agent: synthesis, characterization and bioevaluation Curr. Org. Chem. 17 2013 125 131
60. A.M. Grumezescu, E. Andronescu, A.M. Holban, A. Ficai, D. Ficai, G. Voicu, V. Grumezescu, P.C. Balaure, and M.C. Chifiriuc Water dispersible cross-linked magnetic chitosan beads for increasing the antimicrobial efficiency of different therapeutic agents Int. J. Pharm. 454 2013 233 240
61. 2 network Dig. J. Nanomater. Biostruct. 8 2013 869 876
62. V. Grumezescu, G. Socol, A.M. Grumezescu, A.M. Holban, A. Ficai, R. TruşcÇ, C. Bleotu, P.C. Balaure, R. Cristescu, and M.C. Chifiriuc Functionalized antibiofilm thin coatings based on PLA-PVA microspheres loaded with usnic acid natural compounds fabricated by MAPLE Appl. Surf. Sci. 2013 (in press)
63. S.E. Handfield-Jones, C.E.H. Grattan, R.A. Simpson, and C.T.C. Kennedy Comparison of a hydrocolloid dressing and paraffin gauze in the treatment of venous ulcers Br. J. Dermatol. 118 1988 425 427
64. M.M. Harriott, and M.C. Noverr Importance of Candida-bacterial polymicrobial biofilms in disease Trends Microbiol. 19 2011 557 563
65. T. Hashimoto, Y. Suzuki, M. Tanihara, Y. Kakimaru, and K. Suzuki Development of alginate wound dressings linked with hybrid peptides derived from laminin and elastin Biomaterials 25 2004 1407 1414 (Pubitemid 37476214)
66. B. Hinz Formation and function of the myofibroblast during tissue repair J. Invest. Dermatol. 127 2007 526 537
67. D.A. Hogan Talking to themselves: autoregulation and quorum sensing in fungi Eukaryot. Cell 5 2006 613 619
68. 4@C18-carvone to prevent Candida tropicalis biofilm development Rom. J. Mater. 2013 (in press)
69. K.S. Huang, C.Y. Wang, C.H. Yang, A.M. Grumezescu, Y.S. Lin, C.P. Kung, I.Y. Lin, Y.C. Chang, W.J. Weng, and W.T. Wang Synthesis and characterization of oil-chitosan composite spheres Molecules 18 2013 5749 5760
70. K.S. Huang, Y.S. Lin, C.H. Yang, A.M. Grumezescu, and C.I. Wang Synthesis of uniform core-shell gelatin-alginate microparticles as intestine-released oral delivery drug carrier Electrophoresis 2013 (in press)
71. K.A. Hughes, I.W. Sutherland, and M.V. Jones Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase Microbiology 144 1998 3039 3047 (Pubitemid 28515582)
72. R. Humar, F.N. Kiefer, H. Berns, T.J. Resink, and E.J. Battegay Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling FASEB J. 16 2002 771 780 (Pubitemid 34615125)
73. J.J. Hutchinson, and J.C. Lawrence Wound infection under occlusive dressings J. Hosp. Infect. 17 1991 83 94
74. H.R. Ingham, D. Tharagonnet, P.R. Sisson, and J.B. Selkon Inhibition of phagocytosis in vitro by obligate anaerobes Lancet 2 1977 1252 1254 (Pubitemid 8285408)
75. G.A. James, E. Swogger, R. Wolcott, E. Pulcini, P. Secor, J. Sestrich, J.W. Costerton, and P.S. Stewart Biofilms in chronic wound Wound Repair Regen. 16 2008 37 44
76. P.A. Janmey, J.P. Winer, and J.W. Weisel Fibrin gels and their clinical and bioengineering applications J. R. Soc. Interface 6 2009 1 10
77. J.T. Johnson, and V.L. Yu Role of anaerobic bacteria in postoperative wound infections following oncologic surgery of the head and neck Ann. Otol. Rhinol. Laryngol. Suppl. 154 1991 46 48
78. I. Joint, K. Tait, and M.E. Callow Cell-to-cell communication across the prokaryote-eukaryote boundary Science 298 2002 1207 (Pubitemid 35285481)
79. D.D. Kakagia, K.J. Kazakos, and K.C. Xarchas Synergistic action of protease-modulating matrix and autologous growth factors in healing of diabetic foot ulcers: a prospective randomized trial J. Diabetes Complications 21 2007 387 391 (Pubitemid 47633241)
80. D. Kingston, and D.V. Seal Current hypotheses on synergistic microbial gangrene Br. J. Surg. 77 1990 260 264 (Pubitemid 20103756)
81. M.A. Kuhn, L. Page, K.K.F. Nguyen, X. Wang, T.L. Wachtel, and M.C. Robson Basic fibroblast growth factor in a carboxymethylcellulose vehicle reverses the bacterial retardation of wound contraction Wounds 13 2001 73 80 (Pubitemid 33691809)
82. M.N. Kumar, R.A. Muzzarelli, C. Muzzarelli, H. Sashiwa, and A.J. Domb Chitosan chemistry and pharmaceutical perspectives Chem. Rev. 104 2004 6017 6084 (Pubitemid 40025733)
83. D. Ladin Becaplermin gel (PDGF-BB) as topical wound therapy. Plastic Surgery Educational Foundation DATA Committee Plast. Reconstr. Surg. 105 2000 1230 1231
84. P.J. Leahy, and W.T. Lawrence Biologic enhancement of wound healing Clin. Plast. Surg. 34 2007 659 671 (Pubitemid 47632764)
85. D. Leaper, A.J. McBain, A. Kramer, O. Assadian, J.L.A. Sanchez, J. Lumio, and M. Kiernan Healthcare associated infection: novel strategies and antimicrobial implants to prevent surgical site infection Ann. R. Coll. Surg. Engl. 92 2010 453 458
86. S.S. Lee, C.Y. Chen, Y.S. Chan, C.Y. Yen, E.K. Chao, and S.W.N. Ueng Hyperbaric oxygen in the treatment of diabetic foot infection Chang Keng I Hsueh 20 1997 17 22
87. W.R. Lee, J.H. Park, and K.H. Kim The biological effects of topical alginate treatment in an animal model of skin wound healing Wound Repair Regen. 17 2009 505 510
88. N.S. Levine, R.B. Lindberg, A.D. Mason, and B.A. Pruitt The quantitative swab culture and smear: a quick simple method for determining the number of viable bacteria on open wounds J. Trauma 16 1976 89 94
89. C.C. Lin, and K.S. Anseth PEG hydrogels for the controlled release of biomolecules in regenerative medicine Pharm. Res. 26 2009 631 643
90. Y.S. Lin, C.H. Yang, C.T. Wu, A.M. Grumezescu, C.Y. Wang, S.Y. Chen, and K.S. Huang A microfluidic chip using phenol formaldehyde resin for uniform-sized polycaprolactone and chitosan microparticles generation Molecules 18 2013 6521 6531
91. Z.J. Liu, and O.C. Velazquez Hyperoxia, endothelial progenitor cell mobilization, and diabetic wound healing Antioxid. Redox Signal. 10 2008 1869 1882
92. A.J. Mangram, T.C. Horan, M.L. Pearson, L.C. Silver, and W.R. Jarvis Guideline for prevention of surgical site infection Am. J. Infect. Control 27 1999 97 134
93. L. Margolin, and P. Gialanella Assessment of the antimicrobial properties of maggots Int. Wound J. 7 2010 202 204
94. J.M. Martin, J.M. Zenilman, and G.S. Lazarus Molecular microbiology: new dimensions for cutaneous biology and wound healing J. Invest. Dermatol. 130 2010 38 48
95. K. Maruyama Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing Am. J. Pathol. 170 2007 1178 1191 (Pubitemid 47339326)
96. M.D. Mastropaolo Synergy in polymicrobial infections in a mouse model of type 2 diabetes Infect. Immun. 73 2005 6055 6063 (Pubitemid 41193044)
97. D. Mayrand, and B.C. McBride Ecological relationships of bacteria involved in a simple, mixed anaerobic infection Infect. Immun. 27 1980 44 50 (Pubitemid 10211932)
98. A.S. McKee, A.S. McDermaid, A.R. Baskerville, A.B. Dowsett, D.C. Ellwood, and P.D. Marsh Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50 Infect. Immun. 52 1986 249 355
99. X. Ming, M. Nichols, and S. Rothenburger In vivo antibacterial efficacy of MONOCRYL plus antibacterial suture (poliglecaprone 25 with triclosan) Surg. Infect. (Larchmt) 8 2007 209 214
100. P.C. Molan The role of honey in the management of wounds J. Wound Care 8 1999 415 418
101. A. Nelson, A. De Soyza, J.D. Perry, I.C. Sutcliffe, and S.P. Cummings Polymicrobial challenges to Koch's postulates: ecological lessons from the bacterial vaginosis and cystic fibrosis microbiomes Innate Immun. 18 2012 774 783
102. C. Nucci, M. Artini, M. Pasmore, F. Missiroli, J.W. Costerton, and L. Selan A microbiological and confocal microscopy study documenting a slime-producing Staphylococcus epidermidis isolated from a nylon corneal suture of a patient with antibiotic-resistant endophthalmitis Graefes Arch. Clin. Exp. Ophthalmol. 243 2005 951 954 (Pubitemid 41386722)
103. A.G. Nusbaum, J. Gil, M.K. Rippy, B. Warne, J. Valdes, A. Claro, and S.C. Davis Effective method to remove wound bacteria: comparison of various debridement modalities in an in vivo porcine model J. Surg. Res. 176 2012 701 707
104. K. Obara, M. Ishihara, and T. Ishizuka Photocrosslinkable chitosan hydrogel containing fibroblast growth factor-2 stimulates wound healing in healing-impaired db/db mice Biomaterials 24 2003 3437 3444 (Pubitemid 36703118)
105. J. O'Connor, A. Kells, S. Henry, and T. Scalea Vacuum-assisted closure for the treatment of complex chest wounds Ann. Thorac. Surg. 79 2005 1196 1200 (Pubitemid 40431838)
106. L. Ovington Bacterial toxins and wound healing Ostomy Wound Manage. 49 2003 8 12
107. C.J. Park, S.G. Clark, C.A. Lichtensteiger, R.D. Jamison, and A.J. Johnson Accelerated wound closure of pressure ulcers in aged mice by chitosan scaffolds with and without bFGF Acta Biomater. 5 2009 1926 1936
108. I. Pastar, I. Pastar, A.G. Nusbaum, J. Gil, S.B. Patel, J. Chen, J. Valdes, S. Olivera, L.R. Plano, M. Tomic-Canic, and S.C. Davis Interactions of methicillin resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in polymicrobial wound Infection 8 2013 e56846
109. A.L.G. Peel Definition of infection E.W. Taylor, Infection in Surgical Practice 1992 Oxford University Press Oxford, United Kingdom 82 87
110. A.Y. Peleg, D.A. Hogan, and E. Mylonakis Medically important bacterial-fungal interactions Nat. Rev. Microbiol. 8 2010 340 349
111. P.E. Prete Growth effects of Phaenicia sericata larval extracts on fibroblasts: mechanism for wound healing by maggot therapy Life Sci. 60 1997 505 510 (Pubitemid 27099797)
112. D. Raahave, A. Friis-Moller, K. Bjerre-Jespen, J. Thiis-Knudsen, and L.B. Rasmussen The infective dose of aerobic and anaerobic bacteria in postoperative wound sepsis Arch. Surg. 121 1986 924 929 (Pubitemid 16039340)
113. N.K. Rai, K. Tripathi, D. Sharma, and V.K. Shukla Apoptosis: a basic physiologic process in wound healing Int. J. Low Extrem. Wounds 4 2005 138 144 (Pubitemid 41437580)
114. S.A. Rani Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states J. Bacteriol. 189 2007 4223 4233 (Pubitemid 46847371)
115. M.C. Robson Wound infection: a failure of wound healing caused by an imbalance of bacteria Surg. Clin. North Am. 77 1997 637 650 (Pubitemid 27256038)
116. G.T. Rodeheaver, L.D. Kurtz, W.T. Bellamy, S.L. Smith, H. Farris, and R.F. Edlich Biocidal braided sutures Arch. Surg. 118 1983 322 327 (Pubitemid 13195794)
117. C. Rollenhagen, M. Sorensen, K. Rizos, R. Hurvitz, and D. Bumann Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen Proc. Natl. Acad. Sci. U.S.A. 101 2004 8739 8744 (Pubitemid 38745841)
118. A. Rubinstein, and C.E. Pierce Rapid healing of diabetic foot ulcers with meticulous blood glucose control Acta Diabetol. 25 1988 25 32
119. A. Rubinstein, C.E. Pierce, and Z. Bloomgarden Rapid healing of diabetic foot ulcers with subcutaneous insulin infusion Am. J. Med. 75 1983 161 166
120. C. Saviuc, A.M. Grumezescu, M.C. Chifiriuc, C. Bleotu, G. Stanciu, R. Hristu, D.E. Mihaiescu, and V. Lazar In vitro methods for the study of microbial biofilms Biointerface Res. Appl. Chem. 1 2011 31
121. C.F. Schierle, M. De la Garza, T.A. Mustoe, and R.D. Galiano Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model Wound Repair Regen. 17 2009 354 359
122. G.S. Schultz, R.G. Sibbald, and V. Falanga Wound bed preparation: a systematic approach to wound management Wound Repair Regen. 11 2003 S1 S28
123. G. Seneviratne, J.S. Zavahir, W.M.M.S. Bandara, and M.L.M.A.W. Weerasekara Fungal-bacterial biofilms: their development for novel biotechnological applications World J. Microbiol. Biotechnol. 24 2008 739 743 (Pubitemid 351585252)
124. A.K. Seth, M.R. Geringer, R.D. Galiano, K.P. Leung, and T.A. Mustoe Quantitative comparison and analysis of species-specific wound biofilm virulence using an in vivo, rabbit-ear model J. Am. Coll. Surg. 15 2012 388 399
125. M.E. Shirtliff, B.M. Peters, and M.A. Jabra-Rizk Cross-kingdom interactions: Candida albicans and bacteria FEMS Microbiol. Lett. 299 2009 1 8
126. C.D. Sibley Discerning the complexity of community interactions using a Drosophila model of polymicrobial infections PLoS Pathog. 4 2008 e1000184
127. P. Simamora, and W. Chern Poly-l-lactic acid: an overview J. Drugs Dermatol. 5 2006 436 440
128. A.J. Singer, and R.A. Clark Cutaneous wound healing N. Engl. J. Med. 341 1999 738 746 (Pubitemid 29407375)
129. M. Sokolsky-Papkov, K. Agashi, A. Olaye, K. Shakesheff, and A.J. Domb Polymer carriers for drug delivery in tissue engineering Adv. Drug Deliv. Rev. 59 2007 187 206 (Pubitemid 46887622)
130. W.D. Spotnitz Fibrin sealant: past, present, and future: a brief review World J. Surg. 34 2010 632 634
131. B.E. Stompro, J.F. Hansbrough, and S.T. Boyce Attachment of peptide growth factors to implantable collagen J. Surg. Res. 46 1989 413 421 (Pubitemid 19148966)
132. M.L. Storch, S.J. Rothenburger, and G. Jacinto Experimental efficacy study of coated Vicryl plus antibacterial suture in guinea pigs challenged with Staphylococcus aureus Surg. Infect. (Larchmt) 5 2004 281 288 (Pubitemid 39462171)
133. M. Tanihara, Y. Suzuki, E. Yamamoto, A. Noguchi, and Y. Mizushima Sustained release of basic fibroblast growth factor and angiogenesis in a novel covalently crosslinked gel of heparin and alginate J. Biomed. Mater. Res. 56 2001 216 221 (Pubitemid 32520696)
134. N. Tatiana, D. Rice, M.R. Hamblin, and I.M. Herman Acute and impaired wound healing: pathophysiology and current methods for drug delivery: Part 2: Role of growth factors in normal and pathological wound healing: therapeutic potential and methods of delivery Adv. Skin Wound Care 25 2012 349 370
135. J.K. Tessmar, and A.M. Gopferich Matrices and scaffolds for protein delivery in tissue engineering Adv. Drug Deliv. Rev. 59 2007 274 291 (Pubitemid 46879975)
136. M. Tomic-Canic, E.A. Ayello, O. Stojadinovic, M.S. Golinko, and H. Brem Using gene transcription patterns (bar coding scans) to guide wound debridement and healing Adv. Skin Wound Care 21 2008 487 492
137. N.J. Trengove, M.C. Stacey, D.F. McGechie, and S. Mata Qualitative bacteriology and leg ulcer healing J. Wound Care 5 1996 277 280
138. A. Turkmen, K. Graham, and D.A. McGrouther Therapeutic applications of the larvae for wound debridement J. Plast. Reconstr. Aesthet. Surg. 63 2009 184 188
139. H. Ueno, T. Mori, and T. Fujinaga Topical formulations and wound healing applications of chitosan Adv. Drug Deliv. Rev. 52 2001 105 115 (Pubitemid 33079166)
140. United States Patent and Trademark Office (USPTO) Patent Application 20070010856, Antimicrobial sutures and methods of making them.
141. G. Voicu, R.E. Geanaliu, C.D. Ghitulica, A. Ficai, A.M. Grumezescu, and C. Bleotu Synthesis, characterization and bioevaluation of irinotecan-collagen hybrid materials for biomedical applications as drug delivery systems in tumoral treatments Cent. Eur. J. Chem. 11 2013 2134 2143
142. R.D. Waite Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles BMC Genomics 7 2006 162
143. A.S. Weyrich, and G.A. Zimmerman Platelets: signaling cells in the immune continuum Trends Immunol. 254 2004 89 95
144. R.L. Williams Hyperbaric oxygen therapy and the diabetic foot J. Am. Podiatr. Med. Assoc. 87 1997 279 292 (Pubitemid 127686436)
145. G.E. Wnek, and G.L. Bowlin Encyclopedia of Biomaterials and Biomedical Engineering vol. 2 2008 Informa Healthcare New York, USA
146. R.D. Wolcott, D.D. Rhoads, and S.E. Dowd Biofilms and chronic wound inflammation J. Wound Care 17 2008 333 341
147. R.D. Wolcott, J.P. Kennedy, and S.E. Dowd Regular debridement is the main tool for maintaining a healthy wound bed in most chronic wounds J. Wound Care 18 2009 54 56
148. S.C. Wu, V.R. Driver, J.S. Wrobel, and D.G. Armstrong Foot ulcers in the diabetic patient, prevention and treatment Vasc. Health Risk Manage. 3 2007 65 76 (Pubitemid 46860717)
149. W.A. Zamboni, H.P. Wong, L.L. Stephenson, and M.A. Pfeifer Evaluation of hyperbaric oxygen for diabetic wounds: a prospective study Undersea Hyperb. Med. 24 1997 175 179 (Pubitemid 127460661)
150. G. Zhao, M.L. Usui, R.A. Underwood, P.K. Singh, and G.A. James Time course study of delayed wound healing in a biofilm-challenged diabetic mouse model Wound Repair Regen. 20 2012 342 352
151. D. Zoutman, S. McDonald, and D. Vethanayagan Total and attributable costs of surgical-wound infections at a Canadian tertiary-care center Infect. Control Hosp. Epidemiol. 19 1998 254 259 (Pubitemid 128472672)