Pseudomonas aeruginosa biofilms perturb wound resolution and antibiotic tolerance in diabetic mice

Medical Microbiology and Immunology

Volumn 202, Issue 2, 2013, Pages 131-141

  Watters, Chase ^a   Deleon, Katrina ^a   Trivedi, Urvish ^a   Griswold, John A ^a   Lyte, Mark ^b   Hampel, Ken J ^c   Wargo, Matthew J ^c   Rumbaugh, Kendra P ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Antimicrobial tolerance; Biofilm; Chronic wounds; Diabetes; Insulin; Pseudomonas aeruginosa

Indexed keywords

GENTAMICIN; GLUCOSE; HUMAN INSULIN; INSULIN; ISOPHANE INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL LOAD; BIOFILM; BODY WEIGHT; CHRONIC WOUND; COLONY FORMING UNIT; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE COURSE; DRUG TOLERANCE; EPITHELIZATION; FLUORESCENCE IN SITU HYBRIDIZATION; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TISSUE SECTION; WEIGHT REDUCTION; WOUND CLOSURE; WOUND HEALING; WOUND HEALING IMPAIRMENT;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BIOFILMS; CHRONIC DISEASE; DIABETES MELLITUS, EXPERIMENTAL; DRUG RESISTANCE, BACTERIAL; FEMALE; GENE EXPRESSION PROFILING; INSULIN; MICE; PREVALENCE; PSEUDOMONAS AERUGINOSA; WOUND HEALING; WOUND INFECTION;

EID: 84879694104     PISSN: 03008584     EISSN: 14321831     Source Type: Journal    
DOI: 10.1007/s00430-012-0277-7     Document Type: Article

References (53)

1. Centers for Disease Control and Prevention (2011) National diabetes fact sheet: national estimates and general information on diabetes and prediabetes in the United States, 2011. US Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta
2. Reiber GE (1996) The epidemiology of diabetic foot problems. Diabet Med 13(Suppl 1):S6-11
3. Ohsawa S, Inamori Y, Fukuda K, Hirotuji M (2001) Lower limb amputation for diabetic foot. Arch Orthop Trauma Surg 121(4):186-190
4. Ebskov B, Josephsen P (1980) Incidence of reamputation and death after gangrene of the lower extremity. Prosthet Orthot Int 4(2):77-80
5. Armstrong DG, Lavery LA, Harkless LB, Van Houtum WH (1997) Amputation and reamputation of the diabetic foot. J Am Podiatr Med Assoc 87(6):255-259
6. Cunningham AB (2006) Biofilms:The Hypertextbook. Montana State University, Bozeman
7. Yoga R, Khairul A, Sunita K, Suresh C (2006) Bacteriology of diabetic foot lesions. Med J Mala 61 Suppl A:14-16
8. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318-1322
9. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167-193
10. Ehrlich GD, Veeh R, Wang X, Costerton JW, Hayes JD, Hu FZ, Daigle BJ, Ehrlich MD, Post JC (2002) Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287(13):1710-1715
11. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407(6805):762-764
12. Slusher MM, Myrvik QN, Lewis JC, Gristina AG (1987) Extended-wear lenses, biofilm, and bacterial adhesion. Arch Ophthalmol 105(1):110-115
13. Edwards R, Harding KG (2004) Bacteria and wound healing. Curr Opin Infect Dis 17(2):91-96
14. 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(1):37-44
15. Wolcott RD, Ehrlich GD (2008) Biofilms and chronic infections. JAMA 299(22):2682-2684
16. Bjarnsholt T, Kirketerp-Moller K, Jensen PO, Madsen KG, Phipps R, Krogfelt K, Hoiby N, Givskov M (2008) Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16(1):2-10. doi: 10.1111/j.1524-475X.2007.00283.x
17. Holder IA, Brown RL, Greenhalgh DG (1997) Mouse models to study wound closure and topical treatment of infected wounds in healing-impaired and normal healing hosts. Wound Repair Regen 5:198-204
18. Tesch GH, Allen TJ (2007) Rodent models of streptozotocin-induced diabetic nephropathy. Nephrology (Carlton) 12(3):261-266. doi: 10.1111/j.1440-1797.2007.00796.x
19. Schaber JA, Triffo WJ, Suh SJ, Oliver JW, Hastert MC, Griswold JA, Auer M, Hamood AN, Rumbaugh KP (2007) Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun 75(8):3715-3721
20. Wolcott RD, Rumbaugh KP, James G, Schultz G, Phillips P, Yang Q, Watters C, Stewart PS, Dowd SE (2010) Biofilm maturity studies indicate sharp debridement opens a time- dependent therapeutic window. J Wound Care 19(8):320-328
21. Lyte M, Ernst S (1992) Catecholamine induced growth of gram negative bacteria. Life Sci 50(3):203-212
22. Hammond A, Dertien J, Colmer-Hamood JA, Griswold JA, Hamood AN (2010) Serum inhibits P. aeruginosa biofilm formation on plastic surfaces and intravenous catheters. J Surg Res 159(2):735-746. doi: 10.1016/j.jss.2008.09.003
23. Shen X, Bornfeldt KE (2007) Mouse models for studies of cardiovascular complications of type 1 diabetes. Ann N Y Acad Sci 1103:202-217. doi: 10.1196/annals.1394.004
24. Spanheimer RG, Umpierrez GE, Stumpf V (1988) Decreased collagen production in diabetic rats. Diabetes 37(4):371-376
25. Covington DS, Xue H, Pizzini R, Lally KP, Andrassy RJ (1993) Streptozotocin and alloxan are comparable agents in the diabetic model of impaired wound healing. Diabetes Res 23(2):47-53
26. Jt Michaels, Churgin SS, Blechman KM, Greives MR, Aarabi S, Galiano RD, Gurtner GC (2007) db/db mice exhibit severe wound-healing impairments compared with other murine diabetic strains in a silicone-splinted excisional wound model. Wound Repair Regen 15(5):665-670. doi: 10.1111/j.1524-475X.2007.00273.x
27. Kania RE, Lamers GE, Vonk MJ, Huy PT, Hiemstra PS, Bloemberg GV, Grote JJ (2007) Demonstration of bacterial cells and glycocalyx in biofilms on human tonsils. Arch Otolaryngol Head Neck Surg 133(2):115-121. doi: 10.1001/archotol.133.2.115
28. Akiyama H, Huh WK, Yamasaki O, Oono T, Iwatsuki K (2002) Confocal laser scanning microscopic observation of glycocalyx production by Staphylococcus aureus in mouse skin: does S. aureus generally produce a biofilm on damaged skin? Br J Dermatol 147(5):879-885
29. Anderson GG, O'Toole GA (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322:85-105
30. Plotkin BJ, Viselli SM (2000) Effect of insulin on microbial growth. Curr Microbiol 41(1):60-64
31. Jeromson S, Keig P, Kerr K (1999) Interaction of insulin and Burkholderia cepacia. Clin Microbiol Infect 5(7):439-442
32. Hayford JT, Thompson RG (1982) Free and total insulin integrated concentrations in insulin dependent diabetes. Metabolism 31(4):387-397. doi: 10026-0495(82)90116-0
33. Hirose H, Takayama T, Hozawa S, Hibi T, Saito I (2011) Prediction of metabolic syndrome using artificial neural network system based on clinical data including insulin resistance index and serum adiponectin. Comput Biol Med 41(11):1051-1056. doi: 10.1016/j.compbiomed.2011.09.005
34. Yang M, Guo Q, Zhang X, Sun S, Wang Y, Zhao L, Hu E, Li C (2009) Intensive insulin therapy on infection rate, days in NICU, in-hospital mortality and neurological outcome in severe traumatic brain injury patients: a randomized controlled trial. Int J Nurs Stud 46(6):753-758. doi: 10.1016/j.ijnurstu.2009.01.004
35. Woods DE, Jones AL, Hill PJ (1993) Interaction of insulin with Pseudomonas pseudomallei. Infect Immun 61(10):4045-4050
36. Singh VA, Barbul A (2008) Bacterial biofilms in wounds. Wound Repair Regen 16(1):1. doi: 10.1111/j.1524-475X.2007.00349.x
37. Kanno E, Toriyabe S, Zhang L, Imai Y, Tachi M (2009) Biofilm formation on rat skin wounds by Pseudomonas aeruginosa carrying the green fluorescent protein gene. Exp Dermatol. doi: 10.1111/j.1600-0625.2009.00931.x
38. Schierle CF, De la Garza M, Mustoe TA, Galiano RD (2009) Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model. Wound Repair Regen 17(3):354-359. doi: 10.1111/j.1524-475X.2009.00489.x
39. Seth AK, Geringer MR, Gurjala AN, Hong SJ, Galiano RD, Leung KP, Mustoe TA (2012) 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 129(2):262e-274e. doi: 10.1097/PRS.0b013e31823aeb3b
40. 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. PLoS ONE 6(11):e27317. doi: 10.1371/journal.pone. 0027317
41. Gurjala AN, Geringer MR, Seth AK, Hong SJ, Smeltzer MS, Galiano RD, Leung KP, Mustoe TA (2011) Development of a novel, highly quantitative in vivo model for the study of biofilm-impaired cutaneous wound healing. Wound Repair Regen 19(3):400-410. doi: 10.1111/j.1524-475X.2011.00690.x
42. Zhao G, Hochwalt PC, Usui ML, Underwood RA, Singh PK, James GA, Stewart PS, Fleckman P, Olerud JE (2010) Delayed wound healing in diabetic (db/db) mice with Pseudomonas aeruginosa biofilm challenge: a model for the study of chronic wounds. Wound Repair Regen 18(5):467-477
43. Wolcott RD, Rhoads DD (2008) A study of biofilm-based wound management in subjects with critical limb ischaemia. J Wound Care 17(4):145-148, 150-142, 154-145
44. Wu K, Kah, Y. (2008) Streptozotocin-induced diabetic models in mice and rats. Curr Protoc Pharmacol UNIT 5.47 doi: 10.1002/0471141755.ph0547s40
45. Lanng S, Thorsteinsson B, Nerup J, Koch C (1994) Diabetes mellitus in cystic fibrosis: effect of insulin therapy on lung function and infections. Acta Paediatr 83(8):849-853
46. Gauglitz GG, Toliver-Kinsky TE, Williams FN, Song J, Cui W, Herndon DN, Jeschke MG (2010) Insulin increases resistance to burn wound infection-associated sepsis. Crit Care Med 38(1):202-208. doi: 10.1097/CCM.0b013e3181b43236
47. Jeschke MG, Kulp GA, Kraft R, Finnerty CC, Mlcak R, Lee JO, Herndon DN (2010) Intensive insulin therapy in severely burned pediatric patients: a prospective randomized trial. Am J Respir Crit Care Med 182(3):351-359. doi: 10.1164/rccm.201002-0190OC
48. Chai Y, Kolter R, Losick R (2009) A widely conserved gene cluster required for lactate utilization in Bacillus subtilis and its involvement in biofilm formation. J Bacteriol 191(8):2423-2430. doi: 10.1128/JB.01464-08
49. Pelegrinelli FF, Thirone AC, Gasparetti AL, Araujo EP, Velloso LA, Saad MJ (2001) Early steps of insulin action in the skin of intact rats. J Invest Dermatol 117(4):971-976. doi: 10.1046/j.0022-202x.2001.01473.x
50. Dandona P, Aljada A, Mohanty P, Ghanim H, Hamouda W, Assian E, Ahmad S (2001) Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab 86(7):3257-3265
51. Dandona P, Chaudhuri A, Mohanty P, Ghanim H (2007) Anti-inflammatory effects of insulin. Curr Opin Clin Nutr Metab Care 10(4):511-517. doi: 10.1097/MCO.0b013e3281e38774
52. Ghanim H, Mohanty P, Deopurkar R, Sia CL, Korzeniewski K, Abuaysheh S, Chaudhuri A, Dandona P (2008) Acute modulation of toll-like receptors by insulin. Diabetes Care 31(9):1827-1831. doi: 10.2337/dc08-0561
53. Kidd LB, Schabbauer GA, Luyendyk JP, Holscher TD, Tilley RE, Tencati M, Mackman N (2008) Insulin activation of the phosphatidylinositol 3-kinase/protein kinase B (Akt) pathway reduces lipopolysaccharide-induced inflammation in mice. J Pharmacol Exp Ther 326(1):348-353. doi: 10.1124/jpet.108.138891