Pseudomonas aeruginosa biofilm aggravates skin inflammatory response in BALB/c mice in a novel chronic wound model

Wound Repair and Regeneration

Volumn 21, Issue 2, 2013, Pages 292-299

  Trøstrup, Hannah ^a   Thomsen, Kim ^a   Christophersen, Lars J ^a   Hougen, Hans P ^b   Bjarnsholt, Thomas ^a   Jensen, Peter Ø ^a   Kirkby, Nikolai ^a   Calum, Henrik ^a   Høiby, Niels ^a   Moser, Claus ^a  

^a International Center for Research and Research Training in Endocrine Disruption of Male Reproduction and Child Health   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; ALGINIC ACID; INTERLEUKIN 1BETA; PEPTIDE NUCLEIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIOLOGY; BACTERIUM CULTURE; BIOFILM; CONTROLLED STUDY; DISEASE MODEL; FLUORESCENCE IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SKIN NECROSIS; STAINING; WOUND INFECTION;

ALGINATES; ANIMALS; ANTI-INFECTIVE AGENTS; BIOFILMS; BURNS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; FEMALE; INTERLEUKIN-1BETA; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SKIN; WOUND HEALING; WOUND INFECTION;

EID: 84874859968     PISSN: 10671927     EISSN: 1524475X     Source Type: Journal    
DOI: 10.1111/wrr.12016     Document Type: Article

References (42)

1. Gottrup F,. A specialized wound-healing center concept: importance of a multidisciplinary department structure and surgical treatment facilities in the treatment of chronic wounds. Am J Surg 2004; 187 (5A): 38S-43S.
2. Gottrup F, Holstein P, Jorgensen B, Lohmann M, Karlsmar T,. A new concept of a multidisciplinary wound healing center and a national expert function of wound healing. Arch Surg 2001; 136: 765-772.
3. Meaume S, Perez J, Rethore V, Sebbane G, Dompmartin A, Bressieux JM, Leguyadec T, Tacca O, Bohbot S,. Management of chronic wounds with an innovative absorbent wound dressing. J Wound Care 2012; 21: 315-316. 8, 20-2.
4. Manizate F, Fuller A, Gendics C, Lantis JC, 2nd,. A prospective, single-center, nonblinded, comparative, postmarket clinical evaluation of a bovine-derived collagen with ionic silver dressing versus a carboxymethylcellulose and ionic silver dressing for the reduction of bioburden in variable-etiology, bilateral lower-extremity wounds. Adv Skin Wound Care 2012; 25: 220-225.
5. Kranke P, Bennett MH, Martyn-St James M, Schnabel A, Debus SE,. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst Rev 2012; (4): CD004123.
6. Stadelmann WK, Digenis AG, Tobin GR,. Physiology and healing dynamics of chronic cutaneous wounds. Am J Surg 1998; 176 (2A Suppl.): 26S-38S.
7. Moor AN, Vachon DJ, Gould LJ,. Proteolytic activity in wound fluids and tissues derived from chronic venous leg ulcers. Wound Repair Regen 2009; 17: 832-839.
8. Trøstrup H, Lundquist R, Christensen LH, Jorgensen LN, Karlsmark T, Haab BB, Ågren MS,. S100A8/A9 deficiency in nonhealing venous leg ulcers uncovered by multiplexed antibody microarray profiling. Br J Dermatol 2011; 165: 292-301.
9. Zillmer R, Trøstrup H, Karlsmark T, Ifversen P, Agren MS,. Duration of wound fluid secretion from chronic venous leg ulcers is critical for interleukin-1alpha, interleukin-1beta, interleukin-8 levels and fibroblast activation. Arch Dermatol Res 2011; 303: 601-606.
10. Gjødsbøl K, Christensen JJ, Karlsmark T, Jørgensen B, Klein BM, Krogfelt KA,. Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 2006; 3: 225-231.
11. Høgsberg T, Bjarnsholt T, Thomsen JS, Kirketerp-Møller K,. Success rate of split-thickness skin grafting of chronic venous leg ulcers depends on the presence of Pseudomonas aeruginosa: a retrospective study. PLoS One 2011; 6: e20492.
12. Hoiby N, Ciofu O, Johansen HK, Song ZJ, Moser C, Jensen PO, Molin S, Givskov M, Tolker-Nielsen T, Bjarnsholt T,. The clinical impact of bacterial biofilms. Int J Oral Sci 2011; 3: 55-65.
13. Bjarnsholt T, Østrup Jensen P, Moser C, Høiby N,. Biofilm infections, 1st ed. New York: Springer, 2010.
14. Dalton T, Dowd SE, Wolcott RD, Sun Y, Watters C, Griswold JA, Rumbaugh KP,. An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoS One 2011; 6: e27317.
15. Davis SC, Ricotti C, Cazzaniga A, Welsh E, Eaglstein WH, Mertz PM,. Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 2008; 16: 23-29.
16. James GA, Swogger E, Wolcott R, Pulcini E, Secor P, Sestrich J, Costerton JW, Stewart PS,. Biofilms in chronic wounds. Wound Repair Regen 2008; 16: 37-44.
17. Kirketerp-Møller K, Jensen PO, Fazli M, Madsen KG, Pedersen J, Moser C, Tolker-Nielsen T, Høiby N, Givskov M, Bjarnsholt T,. Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 2008; 46: 2717-2722.
18. Kirketerp-Møller K, Gottrup F,. [Bacterial biofilm in chronic wounds]. Ugeskr Laeger 2009; 171: 1097.
19. Fazli M, Bjarnsholt T, Kirketerp-Moller K, Jorgensen B, Andersen AS, Krogfelt KA, Givskov M, Tolker-Nielsen T,. Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 2009; 47: 4084-4089.
20. Baffoni M, Bessa LJ, Grande R, Di Giulio M, Mongelli M, Ciarelli A, Cellini L,. Laser irradiation effect on Staphylococcus aureus and Pseudomonas aeruginosa biofilms isolated from venous leg ulcer. Int Wound J 2012; 5: 517-524.
21. Birch M, Tomlinson A, Ferguson MW,. Animal models for adult dermal wound healing. Methods Mol Med 2005; 117: 223-235.
22. Seth AK, Geringer MR, Gurjala AN, Hong SJ, Galiano RD, Leung KP, Mustoe TA,. Treatment of Pseudomonas aeruginosa biofilm-infected wounds with clinical wound care strategies: a quantitative study using an in vivo rabbit ear model. Plast Reconstr Surg 2012; 129: 262e-274.
23. Donlan RM,. Biofilms: microbial life on surfaces. Emerg Infect Dis 2002; 8: 881-890.
24. Moser C, Hougen HP, Song Z, Rygaard J, Kharazmi A, Hoiby N,. Early immune response in susceptible and resistant mice strains with chronic Pseudomonas aeruginosa lung infection determines the type of T-helper cell response. APMIS 1999; 107: 1093-1100.
25. Cash HA, Woods DE, McCullough B, Johanson WG, Jr, Bass JA,. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 1979; 119: 453-459.
26. Calum H, Moser C, Jensen PO, Christophersen L, Maling DS, van, Gennip M, Bjarnsholt T, Hougen HP, Givskov M, Jacobsen GK, Høiby,. Thermal injury induces impaired function in polymorphonuclear neutrophil granulocytes and reduced control of burn wound infection. Clin Exp Immunol 2009; 156: 102-110.
27. Pedersen SS, Shand GH, Hansen BL, Hansen GN,. Induction of experimental chronic Pseudomonas aeruginosa lung infection with P. aeruginosa entrapped in alginate microspheres. APMIS 1990; 98: 203-211.
28. Moser C, Van Gennip M, Bjarnsholt T, Jensen PO, Lee B, Hougen HP, Calum H, Ciofu O, Givskov M, Molin S, Høiby N,. Novel experimental Pseudomonas aeruginosa lung infection model mimicking long-term host-pathogen interactions in cystic fibrosis. APMIS 2009; 117: 95-107.
29. Bozic CR, Kolakowski LF, Jr, Gerard NP, Garcia-Rodriguez C, von, Uexkull-Guldenband C, Conklyn MJ, Breslow R, Showell HJ, Gerard C,. Expression and biologic characterization of the murine chemokine KC. J Immunol 1995; 154: 6048-6057.
30. Boxman IL, Ruwhof C, Boerman OC, Lowik CW, Ponec M,. Role of fibroblasts in the regulation of proinflammatory interleukin IL-1, IL-6 and IL-8 levels induced by keratinocyte-derived IL-1. Arch Dermatol Res 1996; 288: 391-398.
31. Petreaca ML, Do D, Dhall S, McLelland D, Serafino A, Lyubovitsky J, Schiller N, Martins-Green MM,. Deletion of a tumor necrosis superfamily gene in mice leads to impaired healing that mimics chronic wounds in humans. Wound Repair Regen 2012; 20: 353-366.
32. Byrd MS, Pang B, Hong W, Waligora EA, Juneau RA, Armbruster CE, Weimer KE, Murrah K, Mann EE, Lu H, Sprinkle A, Parsek M, Kock ND, Wozniak DJ, Swords WE,. Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model. Infect Immun 2011; 79: 3087-3095.
33. Schaber JA, Triffo WJ, Suh SJ, Oliver JW, Hastert MC, Griswold JA, Auer M, Hamood AN, Rumbaugh KP,. Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun 2007; 75: 3715-3721.
34. Zhao G, Hochwalt PC, Usui ML, Underwood RA, Singh PK, James GA, Stewart PS, Fleckman P, Olerud JE,. Delayed wound healing in diabetic (db/db) mice with Pseudomonas aeruginosa biofilm challenge: a model for the study of chronic wounds. Wound Repair Regen 2010; 18: 467-477.
35. Zhao G, Usui ML, Underwood RA, Singh PK, James GA, Stewart PS, Fleckman P, Olerud JE,. Time course study of delayed wound healing in a biofilm-challenged diabetic mouse model. Wound Repair Regen 2012; 20: 342-352.
36. Gurjala AN, Geringer MR, Seth AK, Hong SJ, Smeltzer MS, Galiano RD, Leung KP, Mustoe TA,. Development of a novel, highly quantitative in vivo model for the study of biofilm-impaired cutaneous wound healing. Wound Repair Regen 2011; 19: 400-410.
37. Høiby N, Krogh Johansen H, Moser C, Song Z, Ciofu O, Kharazmi A,. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 2001; 3: 23-35.
38. Jensen PO, Givskov M, Bjarnsholt T, Moser C,. The immune system vs. Pseudomonas aeruginosa biofilms. FEMS Immunol Med Microbiol 2010; 59: 292-305.
39. Moser C, Jensen PO, Kobayashi O, Hougen HP, Song Z, Rygaard J, Kharazmi A, Høiby N,. Improved outcome of chronic Pseudomonas aeruginosa lung infection is associated with induction of a Th1-dominated cytokine response. Clin Exp Immunol 2002; 127: 206-213.
40. Calum H, Moser C, Jensen PO, Shirai R, Hoiby N,. Cytokine and surface receptor diversity of NK cells in resistant C3H/HeN and susceptible BALB/c mice with chronic Pseudomonas aeruginosa lung infection. APMIS 2003; 111: 891-897.
41. Jensen PO, Moser C, Kobayashi O, Hougen HP, Kharazmi A, Hoiby N,. Faster activation of polymorphonuclear neutrophils in resistant mice during early innate response to Pseudomonas aeruginosa lung infection. Clin Exp Immunol 2004; 137: 478-485.
42. Wysocki AB,. Wound fluids and the pathogenesis of chronic wounds. J Wound Ostomy Continence Nurs 1996; 23: 283-290.