Delayed healing in biofilm-colonized db/db mouse wounds

Wound Repair and Regeneration

Volumn 20, Issue 3, 2012, Pages 342-352

  Zhao, Ge ^a   Usui, Marcia L ^a   Underwood, Robert A ^a   Singh, Pradeep K ^a   James, Garth A ^b   Stewart, Philip S ^b   Fleckman, Philip ^a   Olerud, John E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOFILM; CONTROLLED STUDY; FEMALE; HOST RESISTANCE; INFLAMMATION; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; TIME; WOUND HEALING IMPAIRMENT; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; GROWTH, DEVELOPMENT AND AGING; MALE; MICROBIOLOGY; NONOBESE DIABETIC MOUSE; PATHOLOGY; PSEUDOMONAS INFECTION; WOUND HEALING;

ANIMALS; BIOFILMS; DIABETES MELLITUS, EXPERIMENTAL; MALE; MICE; MICE, INBRED NOD; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; TIME FACTORS; WOUND HEALING;

EID: 84860643008     PISSN: 10671927     EISSN: 1524475X     Source Type: Journal    
DOI: 10.1111/j.1524-475X.2012.00793.x     Document Type: Article

References (37)

1. Fonder MA, Lazarus GS, Cowan DA, Aronson-Cook B, Kohli AR, Mamelak AJ,. Treating the chronic wound: a practical approach to the care of nonhealing wounds and wound care dressings. J Am Acad Dermatol 2008; 58: 185-206.
2. Fowler E,. Chronic wounds: an overview. In:, Krasner D, editor. Chronic wound care: a clinical source book for healthcare professionals. King of Prussia, PA: Health Management Publications, Inc, 1990: 12-18.
3. Singh A, Halder S, Menon GR, Chumber S, Misra MC, Sharma LK, Srivastava A,. Meta-analysis of randomized controlled trials on hydrocolloid occlusive dressing versus conventional gauze dressing in the healing of chronic wounds. Asian J Surg 2004; 27: 326-332. (Pubitemid 39424563)
4. Tomic-Canic M, Agren MS, Alvares OM,. Epidermal repair and chronic wounds. In:, Rovie DT, Maibach H, editors. The epidermis in wound healing. New York: CRS Press, 2004: 26-57.
5. Bowler PG, Davies BJ,. The microbiology of infected and noninfected leg ulcers. Int J Dermatol 1999; 38: 573-578. (Pubitemid 29404785)
6. Hansson C, Hoborn J, Moller A, Swanbeck G,. The microbial flora in venous leg ulcers without clinical signs of infection. Repeated culture using a validated standardised microbiological technique. Acta Derm Venereol 1995; 75: 24-30.
7. Gjodsbol K, Christensen JJ, Karlsmark T, Jorgensen B, Klein BM, Krogfelt KA,. Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 2006; 3: 225-231.
8. Kirketerp-Moller K, Jensen PO, Fazli M, Madsen KG, Pedersen J, Moser C, Tolker-Nielsen T, Hoiby N, Givskov M, Bjarnsholt T,. Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 2008; 46: 2717-2722.
9. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D,. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS ONE 2008; 3: e3326.
10. Price LB, Liu CM, Melendez JH, Frankel YM, Engelthaler D, Aziz M, Bowers J, Rattray R, Ravel J, Kingsley C, Keim PS, Lazarus GS, Zenilman JM,. Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS ONE 2009; 4: e6462.
11. Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA, Wolcott RD,. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 2008; 8: 43.
12. Costerton JW, Stewart PS, Greenberg EP,. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284: 1318-1322. (Pubitemid 29289651)
13. James GA, Swogger E, Wolcott R, Pulcini E, Secor P, Sestrich J, Costerton JW, Stewart PS,. Biofilms in chronic wounds. Wound Rep Reg 2008; 16: 37-44.
14. Hurlow J, Bowler PG,. Clinical experience with wound biofilm and management: a case series. Ostomy/Wound Manage 2009; 55: 38-49.
15. Kelly NM, Kluftinger JL, Pasloske BL, Paranchych W, Hancock RE,. Pseudomonas aeruginosa pili as ligands for nonopsonic phagocytosis by fibronectin-stimulated macrophages. Infect Immun 1989; 57: 3841-3845. (Pubitemid 20001257)
16. Ahn ST, Mustoe TA,. Effects of ischemia on ulcer wound healing: a new model in the rabbit ear. Ann Plast Surg 1990; 24: 17-23. (Pubitemid 20093496)
17. 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 Rep Reg 2011; 19: 400-410.
18. Gu Q, Wang D, Gao Y, Zhou J, Peng R, Cui Y, Xia G, Qing Q, Yang H, Liu J, Zhao M,. Expression of MMP1 in surgical and radiation-impaired wound healing and its effects on the healing process. J Environ Pathol Toxicol Oncol 2002; 21: 71-78. (Pubitemid 34258228)
19. Greenhalgh DG, Sprugel KH, Murray MJ, Ross R,. PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am J Pathol 1990; 136: 1235-1246. (Pubitemid 20210322)
20. Gibran NS, Jang YC, Isik FF, Greenhalgh DG, Muffley LA, Underwood RA, Usui ML, Larsen J, Smith DG, Bunnett N, Ansel JC, Olerud JE,. Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J Surg Res 2002; 108: 122-128. (Pubitemid 35373824)
21. Brown RL, Greenhalgh DG,. Mouse models to study wound closure and topical treatment of infected wounds in healing-impaired and normal healing hosts. Wound Rep Reg 1997; 5: 198-204. (Pubitemid 127686792)
22. Shi CM, Nakao H, Yamazaki M, Tsuboi R, Ogawa H,. Mixture of sugar and povidone-iodine stimulates healing of MRSA-infected skin ulcers on db/db mice. Arch Dermatol Res 2007; 299: 449-456. (Pubitemid 47546921)
23. 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 Rep Reg 2010; 18: 467-477.
24. Anderl JN, Franklin MJ, Stewart PS,. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 2000; 44: 1818-1824. (Pubitemid 30422930)
25. Fukano Y, Knowles NG, Usui ML, Underwood RA, Hauch KD, Marshall AJ, Ratner BD, Giachelli C, Carter WG, Fleckman P, Olerud JE,. Characterization of an in vitro model for evaluating the interface between skin and percutaneous biomaterials. Wound Rep Reg 2006; 14: 484-491. (Pubitemid 44266607)
26. Usui ML, Mansbridge JN, Carter WG, Fujita M, Olerud JE,. Keratinocyte migration, proliferation, and differentiation in chronic ulcers from patients with diabetes and normal wounds. J Histochem Cytochem 2008; 56: 687-696. (Pubitemid 351842422)
27. Tavakkol Z, Samuelson D, Delancey Pulcini E, Underwood RA, Usui ML, Costerton JW, James GA, Olerud JE, Fleckman P,. Resident bacterial flora in the skin of C57BL/6 mice housed under SPF conditions. J Am Assoc Lab Anim Sci 2010; 49: 588-591.
28. 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.
29. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C,. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 2003; 100: 14339-14344. (Pubitemid 37499238)
30. Eriksson G, Eklund AE, Kallings LO,. The clinical significance of bacterial growth in venous leg ulcers. Scand J Infect Dis 1984; 16: 175-180. (Pubitemid 14104153)
31. Kirker KR, Secor PR, James GA, Fleckman P, Olerud JE, Stewart PS,. Loss of viability and induction of apoptosis in human keratinocytes exposed to Staphylococcus aureus biofilms in vitro. Wound Rep Reg 2009; 17: 690-699.
32. Bjarnsholt T, Kirketerp-Moller K, Jensen PO, Madsen KG, Phipps R, Krogfelt K, Hoiby N, Givskov M,. Why chronic wounds will not heal: a novel hypothesis. Wound Rep Reg 2008; 16: 2-10.
33. Thomsen TR, Aasholm MS, Rudkjobing VB, Saunders AM, Bjarnsholt T, Givskov M, Kirketerp-Moller K, Nielsen PH,. The bacteriology of chronic venous leg ulcer examined by culture-independent molecular methods. Wound Rep Reg 2010; 18: 38-49.
34. Grice EA, Snitkin ES, Yockey LJ, Bermudez DM, Liechty KW, Segre JA,. Longitudinal shift in diabetic wound microbiota correlates with prolonged skin defense response. Proc Natl Acad Sci U S A 2010; 107: 14799-14804.
35. Mathieu D, Mani R,. A review of the clinical significance of tissue hypoxia measurements in lower extremity wound management. Int J Low Extrem Wounds 2007; 6: 273-283. (Pubitemid 350131918)
36. Biswas S, Roy S, Banerjee J, Hussain SR, Khanna S, Meenakshisundaram G, Kuppusamy P, Friedman A, Sen CK,. Hypoxia inducible microRNA 210 attenuates keratinocyte proliferation and impairs closure in a murine model of ischemic wounds. Proc Natl Acad Sci U S A 2010; 107: 6976-6981.
37. Scortegagna M, Martin RJ, Kladney RD, Neumann RG, Arbeit JM,. Hypoxia-inducible factor-1alpha suppresses squamous carcinogenic progression and epithelial-mesenchymal transition. Cancer Res 2009; 69: 2638-2646.