Research progress of bacterial biofilms for chronic wounds_West China Medical Journal

Authors：

YU Jingya ,  DAI Yan , SHI Yulan

Department of Wound Care Center, West China Hospital, Sichuan University / West China School of Nursing, Sichuan University, Chengdu, Sichuan 610041, R. P. China;

Corresponding author：

DAI Yan, Email: 1846703501@qq.com

Keywords：

Chronic wound; Biofilm; Pathogenesis; Detection; Treatment

DOI：

10.7507/1002-0179.202102198

Video：

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Abstract Full text Figures/Tables Video References Cited by

Bacterial biofilm is the key problem of chronic wound infection and difficult healing. How to prevent and control bacterial biofilm and improve the prognosis of chronic wound has become a research hotspot in the field of wound care. This paper will summarize from the following aspects: four major stages in the process of chronic wound bacteria biofilm formation (surface adhesion, formation of small colonies, biofilm maturation, and dispersion and separation); characteristics of host immune response in the presence of biofilms; morphological, microbiological, and molecular detection methods for biofilms; and progress in in vitro trials, animal trials, clinical trials, and new therapeutic methods of biofilm. The purpose of this review is to provide evidence for the treatment of biofilms for chronic wounds.

Citation： YU Jingya, DAI Yan, SHI Yulan. Research progress of bacterial biofilms for chronic wounds. West China Medical Journal, 2021, 36(5): 686-690. doi: 10.7507/1002-0179.202102198 Copy

1.	Clinton A, Carter T. Chronic wound biofilms: pathogenesis and potential therapies. Lab Med, 2015, 46(4): 277-284.
2.	董敏, 殷学利, 黄素群, 等. 专科联盟内慢性伤口患者基层医院就诊体验及卫生服务需求的质性研究. 护理学杂志, 2021, 36(5): 62-64.
3.	陈佩琴. 老年糖尿病慢性伤口患者生活质量的影响因素分析. 护理实践与研究, 2021, 18(3): 325-329.
4.	Zhao G, Usui ML, Lippman SI, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle), 2013, 2(7): 389-399.
5.	Høiby N, Bjarnsholt T, Moser C, et al. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clin Microbiol Infect, 2015, 21(Suppl 1): S1-S25.
6.	Drago F, Gariazzo L, Cioni M, et al. The microbiome and its relevance in complex wounds. Eur J Dermatol, 2019, 29(1): 6-13.
7.	Sen CK, Mathew-Steiner SS, Das A, et al. Electroceutical management of bacterial biofilms and surgical infection. Antioxid Redox Signal, 2020, 33(10): 713-724.
8.	James GA, Swogger E, Wolcott R, et al. Biofilms in chronic wounds. Wound Repair Regen, 2008, 16(1): 37-44.
9.	Omar A, Wright JB, Schultz G, et al. Microbial biofilms and chronic wounds. Microorganisms, 2017, 5(1): 9.
10.	Bjarnsholt T. The role of bacterial biofilms in chronic infections. APMIS Suppl, 2013(136): 1-51.
11.	Wu YK, Cheng NC, Cheng CM. Biofilms in chronic wounds: pathogenesis and diagnosis. Trends Biotechnol, 2019, 37(5): 505-517.
12.	Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev, 2012, 36(4): 893-916.
13.	Flemming HC, Wingender J, Szewzyk U, et al. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol, 2016, 14(9): 563-575.
14.	Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol, 2010, 8(9): 623-633.
15.	Fazli M, Bjarnsholt T, Kirketerp- Møller K, et al. Quantitative analysis of the cellular inflammatory response against biofilm bacteria in chronic wounds. Wound Repair Regen, 2011, 19(3): 387-391.
16.	Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol, 2005, 15(11): 599-607.
17.	Prabhakara R, Harro JM, Leid JG, et al. Murine immune response to a chronic Staphylococcus aureus biofilm infection. Infect Immun, 2011, 79(4): 1789-1796.
18.	Kalliolias GD, Ivashkiv LB. TNF biology, pathogenic mechanisms and emerging therapeutic strategies. Nat Rev Rheumatol, 2016, 12(1): 49-62.
19.	Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature, 1997, 385(6618): 729-733.
20.	Ashcroft GS, Jeong MJ, Ashworth JJ, et al. Tumor necrosis factor-alpha (TNF-α) is a therapeutic target for impaired cutaneous wound healing. Wound Repair Regen, 2012, 20(1): 38-49.
21.	Kennedy P, Brammah S, Wills E. Burns, biofilm and a new appraisal of burn wound sepsis. Burns, 2010, 36(1): 49-56.
22.	Lipsky BA, Berendt AR, Cornia PB, et al. 2012 infectious diseases society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis, 2012, 54(12): e132-e173.
23.	Rhoads DD, Wolcott RD, Sun Y, et al. Comparison of culture and molecular identification of bacteria in chronic wounds. Int J Mol Sci, 2012, 13(3): 2535-2550.
24.	Bjarnsholt T, Alhede M, Alhede M, et al. The in vivo biofilm. Trends Microbiol, 2013, 21(9): 466-474.
25.	Hurlow J, Blanz E, Gaddy JA. Clinical investigation of biofilm in non-healing wounds by high resolution microscopy techniques. J Wound Care, 2016, 25(Suppl 9): S11-S22.
26.	Dowd SE, Wolcott RD, Sun Y, et al. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One, 2008, 3(10): e3326.
27.	Martin JM, Zenilman JM, Lazarus GS. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J Invest Dermatol, 2010, 130(1): 38-48.
28.	Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol, 2014, 5: 258.
29.	Gião MS, Azevedo NF, Wilks SA, et al. Interaction of Legionella pneumophila and Helicobacter pylori with bacterial species isolated from drinking water biofilms. BMC Microbiol, 2011, 11: 57.
30.	Kolbert CP, Persing DH. Ribosomal DNA sequencing as a tool for identification of bacterial pathogens. Curr Opin Microbiol, 1999, 2(3): 299-305.
31.	Davies CE, Hill KE, Wilson MJ, et al. Use of 16S ribosomal DNA PCR and denaturing gradient gel electrophoresis for analysis of the microfloras of healing and nonhealing chronic venous leg ulcers. J Clin Microbiol, 2004, 42(8): 3549-3557.
32.	Dowd SE, Sun Y, Secor PR, et al. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol, 2008, 8: 43.
33.	Dowd SE, Sun Y, Wolcott RD, et al. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis, 2008, 5(4): 459-472.
34.	Johani K, Malone M, Jensen SO, et al. Evaluation of short exposure times of antimicrobial wound solutions against microbial biofilms: from in vitro to in vivo. J Antimicrob Chemother, 2018, 73(2): 494-502.
35.	O’Meara S, Al-Kurdi D, Ologun Y, et al. Antibiotics and antiseptics for venous leg ulcers. Cochrane Database Syst Rev, 2014(1): CD003557.
36.	Wolcott RD, Cook RG, Johnson E, et al. A review of iodine-based compounds, with a focus on biofilms: results of an expert panel. J Wound Care, 2020, 29(Sup7): S38-S43.
37.	Phillips PL, Yang Q, Davis S, et al. Antimicrobial dressing efficacy against mature Pseudomonas aeruginosa biofilm on porcine skin explants. Int Wound J, 2015, 12(4): 469-483.
38.	Yang Q, Larose C, Della Porta AC, et al. A surfactant-based wound dressing can reduce bacterial biofilms in a porcine skin explant model. Int Wound J, 2017, 14(2): 408-413.
39.	徐元玲, 蒋琪霞, 王建东. 慢性伤口细菌生物膜处理方法的研究进展. 中华护理杂志, 2014, 49(11): 1382-1386.
40.	徐元玲. 慢性伤口细菌生物膜临床识别及干预的初步研究. 江苏: 南京中医药大学, 2015.
41.	牛妞. 负压结合抗菌敷料用于伤口细菌生物膜感染的干预研究. 江苏: 南京大学, 2019.
42.	魏敏. 抗菌蛋白酶结合银敷料用于细菌生物膜感染的慢性伤口的效果研究. 江苏: 南京大学, 2019.
43.	吴磊, 周济宏, 汤雨佳, 等. 负压治疗结合滴注冲洗在伤口护理中的应用进展. 中华护理杂志, 2019, 54(6): 950-954.
44.	Bou Haidar N, Marais S, Dé E, et al. Chronic wound healing: a specific antibiofilm protein-asymmetric release system. Mater Sci Eng C Mater Biol Appl, 2020, 106: 110130.
45.	Silva V, Peirone C, Amaral JS, et al. High efficacy of ozonated oils on the removal of biofilms produced by methicillin-resistant Staphylococcus aureus (MRSA) from infected diabetic foot ulcers. Molecules, 2020, 25(16): 3601.
46.	Liu J, Cai M, Yan H, et al. Yunnan baiyao reduces hospital-acquired pressure ulcers via suppressing virulence gene expression and biofilm formation of Staphylococcus aureus. Int J Med Sci, 2019, 16(8): 1078-1088.

1. Clinton A, Carter T. Chronic wound biofilms: pathogenesis and potential therapies. Lab Med, 2015, 46(4): 277-284.
2. 董敏, 殷学利, 黄素群, 等. 专科联盟内慢性伤口患者基层医院就诊体验及卫生服务需求的质性研究. 护理学杂志, 2021, 36(5): 62-64.
3. 陈佩琴. 老年糖尿病慢性伤口患者生活质量的影响因素分析. 护理实践与研究, 2021, 18(3): 325-329.
4. Zhao G, Usui ML, Lippman SI, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle), 2013, 2(7): 389-399.
5. Høiby N, Bjarnsholt T, Moser C, et al. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clin Microbiol Infect, 2015, 21(Suppl 1): S1-S25.
6. Drago F, Gariazzo L, Cioni M, et al. The microbiome and its relevance in complex wounds. Eur J Dermatol, 2019, 29(1): 6-13.
7. Sen CK, Mathew-Steiner SS, Das A, et al. Electroceutical management of bacterial biofilms and surgical infection. Antioxid Redox Signal, 2020, 33(10): 713-724.
8. James GA, Swogger E, Wolcott R, et al. Biofilms in chronic wounds. Wound Repair Regen, 2008, 16(1): 37-44.
9. Omar A, Wright JB, Schultz G, et al. Microbial biofilms and chronic wounds. Microorganisms, 2017, 5(1): 9.
10. Bjarnsholt T. The role of bacterial biofilms in chronic infections. APMIS Suppl, 2013(136): 1-51.
11. Wu YK, Cheng NC, Cheng CM. Biofilms in chronic wounds: pathogenesis and diagnosis. Trends Biotechnol, 2019, 37(5): 505-517.
12. Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev, 2012, 36(4): 893-916.
13. Flemming HC, Wingender J, Szewzyk U, et al. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol, 2016, 14(9): 563-575.
14. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol, 2010, 8(9): 623-633.
15. Fazli M, Bjarnsholt T, Kirketerp- Møller K, et al. Quantitative analysis of the cellular inflammatory response against biofilm bacteria in chronic wounds. Wound Repair Regen, 2011, 19(3): 387-391.
16. Martin P, Leibovich SJ. Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol, 2005, 15(11): 599-607.
17. Prabhakara R, Harro JM, Leid JG, et al. Murine immune response to a chronic Staphylococcus aureus biofilm infection. Infect Immun, 2011, 79(4): 1789-1796.
18. Kalliolias GD, Ivashkiv LB. TNF biology, pathogenic mechanisms and emerging therapeutic strategies. Nat Rev Rheumatol, 2016, 12(1): 49-62.
19. Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature, 1997, 385(6618): 729-733.
20. Ashcroft GS, Jeong MJ, Ashworth JJ, et al. Tumor necrosis factor-alpha (TNF-α) is a therapeutic target for impaired cutaneous wound healing. Wound Repair Regen, 2012, 20(1): 38-49.
21. Kennedy P, Brammah S, Wills E. Burns, biofilm and a new appraisal of burn wound sepsis. Burns, 2010, 36(1): 49-56.
22. Lipsky BA, Berendt AR, Cornia PB, et al. 2012 infectious diseases society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis, 2012, 54(12): e132-e173.
23. Rhoads DD, Wolcott RD, Sun Y, et al. Comparison of culture and molecular identification of bacteria in chronic wounds. Int J Mol Sci, 2012, 13(3): 2535-2550.
24. Bjarnsholt T, Alhede M, Alhede M, et al. The in vivo biofilm. Trends Microbiol, 2013, 21(9): 466-474.
25. Hurlow J, Blanz E, Gaddy JA. Clinical investigation of biofilm in non-healing wounds by high resolution microscopy techniques. J Wound Care, 2016, 25(Suppl 9): S11-S22.
26. Dowd SE, Wolcott RD, Sun Y, et al. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One, 2008, 3(10): e3326.
27. Martin JM, Zenilman JM, Lazarus GS. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J Invest Dermatol, 2010, 130(1): 38-48.
28. Li L, Mendis N, Trigui H, et al. The importance of the viable but non-culturable state in human bacterial pathogens. Front Microbiol, 2014, 5: 258.
29. Gião MS, Azevedo NF, Wilks SA, et al. Interaction of Legionella pneumophila and Helicobacter pylori with bacterial species isolated from drinking water biofilms. BMC Microbiol, 2011, 11: 57.
30. Kolbert CP, Persing DH. Ribosomal DNA sequencing as a tool for identification of bacterial pathogens. Curr Opin Microbiol, 1999, 2(3): 299-305.
31. Davies CE, Hill KE, Wilson MJ, et al. Use of 16S ribosomal DNA PCR and denaturing gradient gel electrophoresis for analysis of the microfloras of healing and nonhealing chronic venous leg ulcers. J Clin Microbiol, 2004, 42(8): 3549-3557.
32. Dowd SE, Sun Y, Secor PR, et al. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol, 2008, 8: 43.
33. Dowd SE, Sun Y, Wolcott RD, et al. Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis, 2008, 5(4): 459-472.
34. Johani K, Malone M, Jensen SO, et al. Evaluation of short exposure times of antimicrobial wound solutions against microbial biofilms: from in vitro to in vivo. J Antimicrob Chemother, 2018, 73(2): 494-502.
35. O’Meara S, Al-Kurdi D, Ologun Y, et al. Antibiotics and antiseptics for venous leg ulcers. Cochrane Database Syst Rev, 2014(1): CD003557.
36. Wolcott RD, Cook RG, Johnson E, et al. A review of iodine-based compounds, with a focus on biofilms: results of an expert panel. J Wound Care, 2020, 29(Sup7): S38-S43.
37. Phillips PL, Yang Q, Davis S, et al. Antimicrobial dressing efficacy against mature Pseudomonas aeruginosa biofilm on porcine skin explants. Int Wound J, 2015, 12(4): 469-483.
38. Yang Q, Larose C, Della Porta AC, et al. A surfactant-based wound dressing can reduce bacterial biofilms in a porcine skin explant model. Int Wound J, 2017, 14(2): 408-413.
39. 徐元玲, 蒋琪霞, 王建东. 慢性伤口细菌生物膜处理方法的研究进展. 中华护理杂志, 2014, 49(11): 1382-1386.
40. 徐元玲. 慢性伤口细菌生物膜临床识别及干预的初步研究. 江苏: 南京中医药大学, 2015.
41. 牛妞. 负压结合抗菌敷料用于伤口细菌生物膜感染的干预研究. 江苏: 南京大学, 2019.
42. 魏敏. 抗菌蛋白酶结合银敷料用于细菌生物膜感染的慢性伤口的效果研究. 江苏: 南京大学, 2019.
43. 吴磊, 周济宏, 汤雨佳, 等. 负压治疗结合滴注冲洗在伤口护理中的应用进展. 中华护理杂志, 2019, 54(6): 950-954.
44. Bou Haidar N, Marais S, Dé E, et al. Chronic wound healing: a specific antibiofilm protein-asymmetric release system. Mater Sci Eng C Mater Biol Appl, 2020, 106: 110130.
45. Silva V, Peirone C, Amaral JS, et al. High efficacy of ozonated oils on the removal of biofilms produced by methicillin-resistant Staphylococcus aureus (MRSA) from infected diabetic foot ulcers. Molecules, 2020, 25(16): 3601.
46. Liu J, Cai M, Yan H, et al. Yunnan baiyao reduces hospital-acquired pressure ulcers via suppressing virulence gene expression and biofilm formation of Staphylococcus aureus. Int J Med Sci, 2019, 16(8): 1078-1088.

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