Abstract
A wound is damage of a tissue usually caused by laceration of a membrane, generally the skin. Wound healing is accomplished in three stages in healthy individuals, including inflammatory, proliferative, and remodeling stages. Healing of wounds normally starts from the inflammatory phase and ends up in the remodeling phase, but chronic wounds remain in an inflammatory stage and do not show progression due to some specific reasons. Chronic wounds are classified in different categories, such as diabetic foot ulcer (DFU), venous leg ulcers (VLU) and pressure ulcer (PU), surgical site infection (SSI), abscess, or trauma ulcers. Globally, the incidence rate of DFU is 1–4 % and prevalence rate is 5.3–10.5 %. However, colonization of pathogenic bacteria at the wound site is associated with wound chronicity. Most chronic wounds contain more than one bacterial species and produce a synergetic effect that results in previously non-virulent bacterial species becoming virulent and causing damage to the host. While investigating bacterial diversity in chronic wounds, Staphylococcus, Pseudomonas, Peptoniphilus, Enterobacter, Stenotrophomonas, Finegoldia, and Serratia were found most frequently in chronic wounds. Recently, it has been observed that bacteria in chronic wounds develop biofilms that contribute to a delay in healing. In a mature biofilm, bacteria grow slowly due to deficiency of nutrients that results in the resistance of bacteria to antibiotics. The present review reflects the reasons why acute wounds become chronic. Interesting findings include the bacterial load, which forms biofilms and shows high-level resistance toward antibiotics, which is a threat to human health in general and particularly to some patients who have acute wounds.
Similar content being viewed by others
References
Bygott JD, Bertram BCR, Hanby JP (1979) Male lions in large coalitions gain reproductive advantages. Nature 282:839–841
Fallouh HB, Venugopal PS, Newton A (2009) Occult gunshot wounds in the emergency department. Lancet 373:631–632
Dombradi Z, Bodnar F, Orosi P, Dombrádi V, Szabo J (2009) A case report of vancomycin-resistant Enterococcus faecalis colonization of a femoral wound in central Europe. Cent Eur J Med 4:259–261
Nasser S, Mabrouk A, Maher A (2003) Colonization of burn wounds in Ain Shams University Burn Unit. J Int Soc Burn Inj 29:229–233
Quinn JV (1998) Tissue adhesives in wound care. BC Decker
Reiber GE, Ledoux WR (2002) Epidemiology of diabetic foot ulcers and amputations: evidence for prevention. Evid Base Diabetes Care 641–665
Ramachandran A (2004) Specific problems of the diabetic foot in developing countries. Diabetes Metab Res Rev 20:123–133
Gloviczki P, Gloviczki ML (2009) Evidence on efficacy of treatments of venous ulcers and on prevention of ulcer recurrence. Perspect Vasc Surg Endovasc Ther 21:259–268
Bergan JJ, Schmid-Schönbein GW, Smith PD, Nicolaides AN, Boisseau MR, Eklof B (2006) Chronic venous disease. N Engl J Med 355:488–498
Smyth ET, McIlvenny G, Enstone JE, Emmerson AM, Humphreys H, Fitzpatrick F, Davies E, Newcombe RG, Spencer RC (2008) Hospital Infection Society Prevalence Survey Steering Group. Four country healthcare associated infection prevalence survey 2006: overview of the results. J Hosp Infect 69:230–48
Armour-Burton T, Fields W, Outlaw L, Deleon E (2013) The healthy skin project: changing nursing practice to prevent and treat hospital-acquired pressure ulcers. Crit Care Nurse 33:32–40
Chicano S, Drolshagen C (2009) Wound care: reducing hospital-acquired pressure ulcers. J Wound Ostomy Cont Nurs 36:45–50
Cuddigan J, Berlowitz DR, Ayello EA (2001) Pressure ulcers in America: prevalence, incidence, and implications for the future. Adv Skin Wound Care 14:208
Bessa LJ, Fazii P, Giulio M, Cellini L (2015) Bacterial isolates from infected wounds and their antibiotic susceptibility pattern: some remarks about wound infection. Int Wound J 12:47–52
Olszewski WL (2016) Role of bacteria in pathogenesis of lower leg ulcers. In ulcers of the lower extremity 125–140. Springer, India
Lewis K (2012) Persister cells: molecular mechanisms related to antibiotic tolerance. In Antibiotic resistance 121–133. Springer Berlin Heidelberg
Ghannoum M, O’Toole GA (2008) Microbial biofi lms. ASM Press, Washington, DC
Dowd SE, Sun Y, Secor PR, Rhoads DD, Wolcott BM, James GA, Wolcott RD (2008) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8:1
Hassan M, Kjos M, Nes IF, Diep DB, Lotfipour F (2012) Natural antimicrobial peptides from bacteria: characteristics and potential applications to fight against antibiotic resistance. J App Microbiol 23:1365–2672
Mah MW, Memish ZA, Cummingam G, Bannyamm RM (2001) Outbreak of acenetobacter baumanii in intensice care unit associated with trechostaumi. Am J Infect Control 29:284–288
Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358:135–138
Davis SC, Ricotti C, Cazzaniga A (2008) Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 16:23–29
Mustoe TA, Shaughnessy KO, Kloeters O (2006) Chronic wound pathogenesis and current treatment strategies: a unifying hypothesis. Plast Reconstr Surg 117:35–41
Doughty MJ, Laiquzzaman M, Muller A, Oblak E, Button NF (2007) Central corneal thickness in European (white) individuals, especially children and the elderly, and assessment of its possible importance in clinical measures of intra-ocular pressure. Ophthalmic Physiol Opt 22:491–504
Evans E (2005) Nutritional assessment in chronic wound care. J Wound Ostomy Cont Nurs 32:317–320
Kane DP (2007) Chronic wound healing and chronic wound management. J Wound Regen 78:123–138
Singh N, Armstrong DG (2005) Preventing foot ulcers in patients with diabetes. J Acquir Manag 293:217–228
Bakker K, Riley PH (2005) The year of the diabetic foot. Diabetes Voice 50:11–14
Bahler K, Riley PH (2005) The year of the diabetic foot. Diabetes Voice 51:15–18
Reiber GE (2001) Epidemiology of foot ulcers and amputations in the diabetic foot. Diabet Foot 9:13–19
Reiber GE, Ledoux WR (2002) Epidemiology of diabetic foot ulcers and amputations: evidence for prevention. Evide Base Diabetes Care Wiley 641–665
McInnes AD (2012) Diabetic foot disease in the United Kingdom: about time to put feet first. J Foot Ankle Res 5:1146–1186
Kung HS, Hoyer DL, Xu J (2005) Deaths: final data for national vital statistics. Braz J Microbiol 58:2004–2041
Margolis DJ, Malay DS, Hoffstad OJ, Leonard CE, MaCurdy T, Tan Y, Molina T, de Nava KL, Siegel KL (2011) Economic burden of diabetic foot ulcers and amputations
International Diabetes Federation (2014) Diabetes Atlas http://www.eatlas.idf.org/media
Pittet D, Harbarth S, Sudan R (2011) Andreas Voss International Conference on Prevention & Infection Control (ICPIC 2011). BMC Proc 5
Pendsey S, Abbas ZG (2007) The step-by-step program for reducing diabetic foot problems: a model for the developing world. Curr Diab Rep 7:425–428
Ali SM, Basit A, Shaikh T, Mumtaz S, Hydrie MZ (2001) Diabetic foot ulcer-a prospective study. J Pak Med Assoc 51:78–81
Reiber GE, Vileikyte L (1999) Causal pathways for incident lower-extremity ulcers in patients with diabetes from two settings. Diabetes Care 22:157–176
Wieman TJ (2003) Principles of management: the diabetic foot. Am J Surg 9:190–295
Marston WA (2003) Infection in daibetic foot ulcer. Diabetes Care 26:1701–1705
Brem H, Sheehan P, Rosenberg HJ, Schneider JS, Boulton AJ (2006) Evidence-based protocol for diabetic foot ulcers. Plast Reconstr Surg 117:193–209
Deribe B, Woldemichael K, Nemera G (2014) Prevalence and factors influencing diabetic foot ulcer among diabetic patients attending Arbaminch Hospital South Ethiopia. J Diabetes Metab 5:4172–6156
Ahmad W, Khan IA, Salma G, Farhan KAS, Khan I (2013) Risk factors for diabetic foot ulcer. J Ayub Med Coll Abbottabad 25:1–2
Rathur HM, Boulton AJ (2007) The diabetic foot. Clin Dermatol 25:109–120
Viswanathan V (2007) The diabetic foot: perspectives from Chennai, South India. Int J Extrem Wounds 6:34–6
Spentzouris G, Labropoulos N (2009) The evaluation of lower-extremity ulcers seminar. Int Radiol 26:286–295
Baker R, Fraser RC (1995) Development of review criteria: linking guidelines and assessment of quality. Bio Med J 311:370–373
Mark H (2005) Lower extremity venous anatomy. Semin Interv Radiol 22:147–156
Nelson EA, Bell-Syer SE, Cullum NA, Webster J (2000) Compression for preventing recurrence of venous ulcers. Cochrane Database Syst Rev 4:CD002303
Simon LS, Mills JA (2009) Nonsteroidal anti-inflammatory drugs. New Eng J Med 302:1179–1185
Agale SV (2013) Chronic leg ulcers: epidemiology, aetiopathogenesis, and management. Ulcers
Abbade LP, Lastoria S, Almeida HR, Stolf HO (2005) A sociodemographic, clinical study of patients with venous ulcer. Int J Dermatol 44:989–992
Margolis DJ, Bilker W, Santanna J, Baumgarten M (2002) Venous leg ulcer: incidence and prevalence in the elderly. J Am Acad Dermatol 46:381–392
Khan AF, Chaudhri R, Ashraf MA, Mazaffar MS, Zawar-ul-Imam S, Tanveer M (2013) Prevalence and presentation of chronic venous disease in Pakistan: a multicentre study. Phlebology 28:74–79
Rayner RCK, Keaton J, Prentice J, Santamaria N (2009) Leg ulcers: atypical presentations and associated comorbidities. Wound Pract Res 17:168–185
Sasanka CS (2012) Venous ulcers of the lower limb: where do we stand. Ind J Plast Surg 45:266–274
Fu X (1998) Skin ulcers in lower extremities: the epidemiology and management in China. Int J Low r Extrem Wounds 4:4–6
Shukla A, Rasik AM, Patnaik GK (2005) Depletion of reduced glutathione, ascorbic acid, vitamin E and antioxidant defence enzymes in a healing cutaneous wound. Free Radic Res 26:93–101
Baker SE, Hopkinson SB, Fitchmun M, Andreason GL, Frasier F, Plopper G, Quaranta V, Jones JC (1996) Laminin-5 and hemidesmosomes: role of the alpha 3 chain subunit in hemidesmosome stability and assembly. J Cell Sci 109:2509–2520
Faria E, Blanes L, Hochman B, Filho MM, Ferreira L (2011) Health-related quality of life, self-esteem, and functional status of patients with leg ulcers. Wounds UK 23:4–10
Lyder CH (2003) Pressure ulcer prevention and management. JAMA 289:223–226
Fogerty MD, Abumrad NN, Nanney L, Arbogast PG, Poulose B, Barbul A (2008) Risk factors for pressure ulcers in acute care hospitals. Wound Repair Regen 16:11–18
Lyder C, Ayello E (2008) Pressure ulcers: a patient safety issue. Agency Healthcare Res Qual 8:1–33
Bluestien D, Jawaheri A (2008) Pressure ulcers: prevention, evaluation, and management. Am Fam Physician 78:1186–1194
European Pressure Ulcer Advisory Panel (2009) Prevention and treatment of pressure ulcers. http://www.npuap.org/wp-content/uploads/2012/03/Final-2009-Treatment-Technical-Report1
Brown G (2003) Long-term outcomes of full-thickness pressure ulcers: healing and mortality. Ostomy Wound Manage 49:42–50
Horn SD, Bender SA, Ferguson ML, Smout RJ, Bergstrom N, Taler G, Cook AS, Sharkey SS, Voss AC (2004) The national pressure ulcer long‐term care study: pressure ulcer development in long‐term care residents. J Am Geriatr Soc 52:359–367
Grey JE, Harding KG, Enoch S (2006) Pressure ulcers. Braz Med J 332:472–475
Gunningberg L, Lindholm C, Carlsson M, Sjoden PO (2000) Effect of visco-elastic foam mattresses on the development of pressure ulcers in patients with hip fractures. J Wound Care 9:455–460
Vanderwee K, Clark M, Dealey C, Gunningberg L, Defloor T (2007) Pressure ulcer prevalence in Europe: a pilot study. J Eval Clin Pract 13:227–235
Shahin S, Jafari A, Mobli H, Rafiee S, Karimi M (2008) Effect of farm size on energy ratio for wheat production: a case study from Ardabil province of Iran American. Eurasian J Agric Environ Sci 3:604–608
Ballard N (2008) How our ICU decreased the rate of hospital acquired pressure ulcers. J Nurs Care Qual 23:92–96
Elliot R, Mckinley S, Fox V (2008) Quality improvement program to reduce the prevelence of pressure ulcer in intensive care unit (ICU). Am J Crit Care 17:328–324
Tubaishata A, Anthonyb D, Salehc M (2011) Pressure ulcers in Jordan: a point prevalence study. J Tissue Viability 20:14–19
Tannen A, Dassen T, Halfens R (2009) Differences in prevalence of pressure ulcers between the Netherlands and Germany associations between risk, prevention and occurrence of pressure ulcers in hospitals and nursing homes. J Clin Nurs 18:304–305
Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR (1999) Guideline for prevention of surgical site infection. Am J Infect Control 27:97–132
Weigelt JA, Lipsky BA, Tabak YP, Derby KG, Kim M, Gupta V (2010) Surgical site infections: causative pathogens and associated outcomes. Am J Infect Control 38:112–120
Graham JC, Pedler SJ (2003) Surgical antibiotic prophylaxis, 3rd edn. Walker R and Edwards C, London, pp 569–581
John WD, Salmaan K, Stephen WT (2002) Antimicrobial prophylaxis in surgery, 5th edn. McGraw Hill Publications, New York, pp 2111–2122
Ameh EA, Mshelbwala PM, Nasir AA, Lukong CS, Jabo BA, Anumah MA, Nmadu PT (2009) Surgical site infection in children: prospective analysis of the burden and risk factors in a sub-Saharan African setting. Surg Infect (Larchmt) 10:105–109
Boni L, Benevento A, Rovera F, Dionigi G, Giuseppe MD, Bertoglio C, Dionigi R (2006) Infective complications in laparoscopic surgery. Surg Infect (Larchmt) 7:101–109
Gastmeier P, Sohr D, Rath A, Forster DH, Wischnewski N, Lacour M, Daschnerand F (2000) Repeated prevalence investigations on nosocomial infections for continuous surveillance. J Hosp Infect 45:47–53
Santos KR, Fonseca L, Bravo NGP, Filho GPP (1997) Surgical site infection: rates, etiology and resistance patterns to antimicrobials among strains isolated at Rio de Janeiro University Hospital. Infection 25:217–220
Sohn AH, Tien NP, Mai VT, Van Nho V, Hanh TN, Ewald B, Dibley M (2006) Microbiology of surgical site infections and associated antimicrobial use among Vietnamese orthopedic and neurosurgical patients. Infect Control 27:855–862
Tiberi S, Nsubuga S, Muzaale C, Lazzarin A, Scarpellini P (2010) Impact of preoperative antibiotic prophylaxis on the incidence of surgical site infection in a Ugandan Hospital. Int Conference on Healthcare Associated Infections, Fifth Decennial
Khan M, Khalil J, Rooh-ul-Muqim MZ, Hassan TU, Ahmed N, Salman M, Muhammad G (2011) Rate and risk factors for surgical site infection at a tertiary care facility in Peshawar, Pakistan. J Ayub Med Coll Abbottabad 23
Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR (1999) Guideline for prevention of surgical site infection. Am J Infect Control 27:97–134
Mayhall CG (1993) Surgical infections including burns. Prevention and control of nosocomial infections, 2nd edn. Williams & Wilkins, Baltimore, pp 614–624
Weiss CA, Statz CL, Dahms RA, Remucal MJ, Dunn DL, Beilman GJ (1999) Six years of surgical wound infection surveillance at a tertiary care center: review of the microbiologic and epidemiological aspects of 20,007 wounds. Arch Surg 134:1041–1048
Haycock C, Laser C, Keuth J, Montefour K, Wilson M, Austin K, Coulen C, Boyle D (2005) Implementing evidence‐based practice findings to decrease postoperative sternal wound infections following open heart surgery. J Cardiovasc Nurs 20:299–305
Dellinger EP, Hausmann SM, Bratzler DW, Johnson RM, Daniel DM, Bunt KM, Baumgardner GA, Sugarman JR (2005) Hospitals collaborate to decrease surgical site infections. Am J Surg 190:9–15
Tanner J, Woodings D, Moncaster K (2006) Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev 3:1465–1478
Amábile-Cuevas CF, Byarugaba DK, Hsueh PR, Kariuki S, Okeke IN (2010) Antimicrobial resistance in developing countries. Springer, New York
Bowler PG, Duerden BI, Armstrong DG (2001) Wound microbiology and associated approaches to wound management. Clin Microbiol Rev 14:244–269
Howell-Jones MJ, Wilson KEH (2005) A review of the microbiology, antibiotic usage and resistance in chronic skin wounds. J Antimicrob Chemother 55:143–149
Stephens P (2001) Skin and oral fibroblasts exhibit phenotypic differences in extracellular matrix reorganization and matrix metalloproteinase activity. Br J Dermatol 144:229–237
Madsen SM, Westh H, Danielsen L, Rosdahl VT (1996) Bacterial colonization and healing of venous leg ulcers. Apmis 104:895–899
Dow G, Browne A, Sibbald RG (1999) Infection in chronic wounds: controversies in diagnosis and treatment. Ostomy Wound Manag 45:23–24
Wolcott RD, Dowd SE, Sun Y, McKeehan T, Smith E, Rhoads D (2008) Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 3:3326
Shin YW, Rishya M, Sekaran M (2015) Prevalence and antibiotic susceptibility of bacteria from acute and chronic wounds in Malaysian subjects. J Infect Dev Ctries 9:936–944
Thomas S (2008) Hydrocolloid dressings in the management of acute wounds: a review of the literature. Int Wound J 5:602–613
Schmidt K, Debus ES, Jessberger ST, Ziegler U, Thiede A (2000) Bacterial population of chronic crural ulcers: is there a difference between the diabetic, the venous, and the arterial ulcer. J Microbiol 29:62–70
Fazli M, Bjarnsholt T, Kirketerp-Møller K, Jørgensen 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
Daxboeck F, Goerzer E, Apfalter (2004) Isolation of Bordetella trematum from a diabetic leg ulcer. Diabet Med 21:1247–8
Bowling FL, Stickings DS, Edwards-Jones V, Armstrong DG, Boulton AJ (2009) Hydrodebridement of wounds: effectiveness in reducing wound bacterial contamination and potential for air bacterial contamination. J Foot Ankle Res 2:1–8
Ahmad M, Khan TH, Ansari MN, Ahmad SF (2014) Enhanced wound healing by topical administration of d-limonene in alloxan induced diabetic mice through reduction of pro-inflammatory markers and chemokine expression. Biomed Central Genomics 15:10–29
Wysocki M, Delatour F, Faurisson F (2013) Continuous versus intermittent infusion of vancomycin in severe staphylococcal infections: prospective multicenter randomized study. Antimicrob Agents Chemother 45:2460–2467
Doerler M, Eming S, Dissemond J, Wolter A, Stoffels-Weindorf M, Reich-Schupke S, Altmeyer P, Stücker M (2014) A novel epidermal growth factor–containing wound dressing for the treatment of hard-to-heal venous leg ulcers. Adv Skin Wound Care 27:456–460
Kariyama R, Mitsuhata R, Chow JW, Clewell DB, Kumon H (2000) Simple and reliable multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. J Clin Microbiol 38:3092–3095
Braga L, Renner JB, Schwartz TA, Woodard J, Helmick CG, Hochberg MC, Jordan JM (2009) Differences in radiographic features of knee osteoarthritis in African-Americans and Caucasians: the Johnston County Osteoarthritis Project. Osteoarthritis Cartilage 17:1554–1561
Paju S, Scannapieco F (2007) Oral biofilms, periodontitis, and pulmonary infections. Oral Dis 13:508–512
Niels H, Oana C, Bjarnsholt T (2010) Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 11:1663–1674
Barbara WT, Rabih OD (2004) Role of biofilm in catheter-associated urinary tract infection. Am J Infect Control 3:177–183
James GA, Swogger E, Wolcott R, Ed P, Secor P, Sestrich J, Costerton JW, Stewart PS (2008) Biofilms in chronic wounds. Wound Repair Regen 16:37–44
Robert D. Kaplan. (2011) American interest: the wounded home front American interest: http://www.cfr.org/world/american-interest-wounded-home-front/p23550.Accessed 1 June 2015
Ghafoor A, Hay ID, Rehm HAB (2011) Role of Exopolysaccharides in Pseudomonas aeruginosa Biofilm Formation and Architecture. Appl Environ Microbiol 77:5238–5246
Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Ann Rev Microbiol 56:187–209
McDougald D, Rice SA, Weichart D (2011) Non culturability: adaptation or debilitation. Microb Ecol 25:1–9
Mah T, Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39
Fazli M, Bjarnsholt T, Moller K (2011) Quantitative analysis of the cellular inflammatory response against biofilm bacteria in chronic wounds. Wound Repair Regen 19:387–391
Taj Y, Essa F, Aziz F, Kazmi SU (2012) Study on biofilm-forming properties of clinical isolates of Staphylococcus aureus. J Inf Dev Ctries 5:403–409
Attinger C, Wolcott R (2012) Clinically addressing biofilm in chronic wounds. Adv Wound Care 1:127–132
Carlos J et al (2013) Biofilm formation by clinical isolates and the implications in chronic infections. Biomed Cent Inf Dis 13:47
Schaber JA et al (2004) Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 53:841–853
Harris LG, Murray S, Pascoe B, Bray J, Meric G, Mageiros L et al (2016) Correction: biofilm morphotypes and population structure among Staphylococcus epidermidis from commensal and clinical samples. PLoS ONE 11(4)
Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (1991) Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567
Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK et al (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395–2407
Murga R, Stewart PS, Daly D (1995) Quantitative analysis of biofilm thickness variability. Biotechnol Bioeng 45:503–510
Beyenal H, Donovan C, Lewandowski Z, Harkin G (2004) Three-dimensional biofilm structure quantification. J Microbiol Methods 59:395–413
Wolcott RD, Rhoads DD (2008) A study of biofilm-based management in subjects with critical limb ischaemia. J Wound Care 17:145–155
Costerton JW, Stewart PS (2001) Antibiotic resistance of bacteria in biofilms. Lancet 58:135–138
Donlan RM, Costerton W (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
Stewart PS, Davison WM, Steenbergen JN (2009) Daptomycin rapidly penetrates a Staphylococcus epidermidis biofilm. Antimicrob Agents Chemother 53:3505–3507
Lewis K (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999–1007
Gilbert S, Loranger A, Daigle N, Marceau N (2002) Simple epithelium keratins 8 and 18 provide resistance to Fas-mediated apoptosis. The protection occurs through a receptor-targeting modulation. J Cell Biol 154:763–774
Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. J Immunol 175:7512–7518
Rani SA, Pitts B, Beyenal H, Veluchamy RA, Lewandowski Z, Davison WM, Buckingham-Meyer K, Stewart PS (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189:4223–4233
Hennequin C, Robin F, Cabrolier N, Bonnet R, Forestier C (2012) Characterization of a DHA-1-producing Klebsiella pneumoniae strain involved in an outbreak and role of the AmpR regulator in virulence. Antimicrob Agents Chemother 56:288–294
Keren I, Shah D, Spoering A, Kaldalu N, Lewis K (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172–8180
Roberts ME, Stewart PS (2005) Modeling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiologyl 151:75–80
Akinobu I, Asami T, Thithiwat M, Kawata K, Okabe S (2009) Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microbiol 34:4093–4100
http://www.whasa.org/C_Region_ECapeNewsletter. Accessed 20 June 2016
Acknowledgments
This work was granted by CAPES, CNPq, FUNDECT, and FAPDF.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rahim, K., Saleha, S., Zhu, X. et al. Bacterial Contribution in Chronicity of Wounds. Microb Ecol 73, 710–721 (2017). https://doi.org/10.1007/s00248-016-0867-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-016-0867-9