Research progress on the mechanisms of probiotics promoting wound healing_Journal of Biomedical Engineering

Authors：

DONG Jiali ¹ ,  WANG Xuejing ² , BAI Geyan ¹ , WANG Dong ³

1. Department of Clinical Medicine, Shaanxi University of Traditional Chinese Medicine, Xianyang, Shaanxi 712046, P. R. China;
2. Medical Experiment Center, Shaanxi University of Traditional Chinese Medicine, Xianyang, Shaanxi 712046, P. R. China;
3. Department of Medicine, Xizang Minzu University, Xianyang, Shaanxi 712082, P.R. China;

Corresponding author：

WANG Xuejing, Email: snowy921@163.com

Keywords：

Probiotics; Chronic wound; Wound healing; Intestinal probiotics; Mechanism of action

DOI：

10.7507/1001-5515.202208003

Video：

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Slow wound healing has been a troublesome problem in clinic. In China, traditional methods such as antibiotics and silver sulfadiazine are used to treat skin wound, but the abuse use has many disadvantages, such as chronic wounds and pathogen resistance. Studies have shown that the microorganisms with symbiotic relationship with organisms have benefits on skin wound. Therefore, the way to develop and utilize probiotics to promote wound healing has become a new research direction. In this paper, we reviewed the studies on the bacteriotherapy in the world, described how the probiotics can play a role in promoting wound healing through local wound and intestine, and introduced some mature probiotics products and clinical trials, aiming to provide foundations for further development of bacteriotherapy and products.

Citation： DONG Jiali, WANG Xuejing, BAI Geyan, WANG Dong. Research progress on the mechanisms of probiotics promoting wound healing. Journal of Biomedical Engineering, 2024, 41(3): 635-640. doi: 10.7507/1001-5515.202208003 Copy

1.	高金梅. 伤口分期治疗及辅料的使用. 甘肃科技, 2017, 33(17): 113-114.
2.	中华医学会创伤学分会组织修复专业委员会(组). 慢性伤口诊疗指导意见(2011版)第4讲创伤性溃疡. 中国临床医生, 2011, 39(12): 55-57.
3.	钟果玉, 谭惠仪, 叶雪梅, 等. 慢性伤口细菌生物膜管理的研究进展. 护理实践与研究, 2021, 18(12): 1790-1794.
4.	Attinger C, Wolcott R. Clinically addressing biofilm in chronic wounds. Adv Wound Care (New Rochelle), 2012, 1(3): 127-132.
5.	Zhao G, Usui M L, Lippman S I, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle), 2013, 2(7): 389-399.
6.	Tejero-sarinena S, Barlow J, Costabile A, et al. In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe, 2012, 18(5): 530-538.
7.	Rainer B M, Thompson K G, Antonescu C, et al. Characterization and analysis of the skin microbiota in rosacea: a case-control study. Am J Clin Dermatol, 2020, 21(1): 139-147.
8.	Zipperer A, Konnerth M C, Laux C, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature, 2016, 535(7613): 511-516.
9.	Xu H, Jeong H S, Lee H Y, et al. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett Appl Microbiol, 2009, 49(4): 434-442.
10.	Zakaria Gomaa E. Antimicrobial and anti-adhesive properties of biosurfactant produced by lactobacilli isolates, biofilm formation and aggregation ability. J Gen Appl Microbiol, 2013, 59(6): 425-436.
11.	Živković M, Miljković M S, Ruas-Madiedo P, et al. EPS-SJ exopolisaccharide produced by the strain lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front Microbiol, 2016, 7: 286.
12.	Scheffold A, Bacher P, LeibundGut-Landmann S. T cell immunity to commensal fungi. Curr Opin Microbiol, 2020, 8: 116-123.
13.	Claudel J P, Auffret N, Leccia M T, et al. Staphylococcus epidermidis: a potential new player in the physiopathology of acne?. Dermatology, 2019, 235(4): 287-294.
14.	Sultana R, McBain A J, O'Neill C A. Strain-dependent augmentation of tight-junction barrier function in human primary epidermal keratinocytes by lactobacillus and bifidobacterium lysates. Appl Environ Microbiol, 2013, 79(16): 4887-4894.
15.	Park Y J, Lee H K. The role of skin and orogenital microbiota in protective immunity and chronic immune-mediated inflammatory disease. Front Immunol, 2018, 8: 1955.
16.	Fijan S, Frauwallner A, Langerholc T, et al. Efficacy of using probiotics with antagonistic activity against pathogens of wound infections: an integrative review of literature. Biomed Res Int, 2019, 2019: 7585486.
17.	Rutherford S T, Bassler B L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med, 2012, 2(11): a012427.
18.	Ramos A N, Cabral M E, Noseda D, et al. Antipathogenic properties of lactobacillus plantarum on pseudomonas aeruginosa: the potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair Regen, 2012, 20(4): 552-562.
19.	Paharik A E, Parlet C P, Chung N, et al. Coagulase-negative staphylococcal strain prevents staphylococcus aureus colonization and skin infection by blocking quorum sensing. Cell Host Microbe, 2017, 22(6): 746-756.
20.	Monnappa A K, Dwidar M, Seo J K, et al. Bdellovibrio bacteriovorus inhibits staphylococcus aureus biofilm formation and invasion into human epithelial cells. Sci Rep, 2014, 4: 3811.
21.	Naseri S, Lepry W C, Nazhat S N. Bioactive glasses in wound healing: hope or hype?. J Mater Chem B, 2017, 5(31): 6167-6174.
22.	Duan T, Du Y, Xing C, et al. Toll-like receptor signaling and its role in cell-mediated immunity. Front Immunol, 2022, 13: 812774.
23.	Lai Y, Di Nardo A, Nakatsuji T, et al. Commensal bacteria regulate toll-like receptor 3-dependent inflammation after skin injury. Nat Med, 2009, 15(12): 1377-1382.
24.	Kim C K, Karau M J, Greenwood-Quaintance K E, et al. Superantigen-producing staphylococcus aureus elicits systemic immune activation in a murine wound colonization model. Toxins (Basel), 2015, 7(12): 5308-5319.
25.	Tsai W H, Chou C H, Huang T Y, et al. Heat-killed lactobacilli preparations promote healing in the experimental cutaneous wounds. Cells, 2021, 10(11): 3264.
26.	Linehan J L, Harrison O J, Han S J, et al. Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell, 2018, 172(4): 784-796.
27.	Luqman A, Nega M, Nguyen M T, et al. SadA-expressing staphylococci in the human gut show increased cell adherence and internalization. Cell Rep, 2018, 22(2): 535-545.
28.	Pullar C E, Isseroff R R. The beta 2-adrenergic receptor activates pro-migratory and pro-proliferative pathways in dermal fibroblasts via divergent mechanisms. J Cell Sci, 2006, 119(Pt 3): 592-602.
29.	Luqman A, Muttaqin M Z, Yulaipi S, et al. Trace amines produced by skin bacteria accelerate wound healing in mice. Commun Biol, 2020, 3(1): 277.
30.	Mohammedsaeed W, Cruickshank S, McBain A J, et al. Lactobacillus rhamnosus GG lysate increases re-epithelialization of keratinocyte scratch assays by promoting migration. Sci Rep, 2015, 5: 16147.
31.	Poutahidis T, Kearney S M, Levkovich T, et al. Microbial symbionts accelerate wound healing via the neuropeptide hormone oxytocin. PLoS One, 2013, 8(10): e78898.
32.	Varian B J, Poutahidis T, DiBenedictis B T, et al. Microbial lysate upregulates host oxytocin. Brain Behav Immun, 2017, 61: 36-49.
33.	Alves E, Gregório J, Baby A R, et al. Homemade kefir consumption improves skin condition-a study conducted in healthy and atopic volunteers. Foods, 2021, 10(11): 2794.
34.	Benyacoub J, Bosco N, Blanchard C, et al. Immune modulation property of lactobacillus paracasei NCC2461 (ST11) strain and impact on skin defences. Benef Microbes, 2014, 5(2): 129-136.
35.	Erdman S E, Poutahidis T. Probiotic 'glow of health': it's more than skin deep. Benef Microbes, 2014, 5(2): 109-119.
36.	Rooj A K, Kimura Y, Buddington R K. Metabolites produced by probiotic lactobacilli rapidly increase glucose uptake by Caco-2 cells. BMC Microbiol, 2010, 10: 16.
37.	Jones M L, Martoni C J, Prakash S. Oral supplementation with probiotic L. reuteri NCIMB 30242 increases mean circulating 25-hydroxyvitamin D: a post hoc analysis of a randomized controlled trial. J Clin Endocrinol Metab, 2013, 98(7): 2944-2951.
38.	De Angelis M, Bottacini F, Fosso B, et al. Lactobacillus rossiae, a vitamin B12 producer, represents a metabolically versatile species within the genus lactobacillus. PLoS One, 2014, 9(9): e107232.
39.	Ming Z, Han L, Bao M, et al. Living bacterial hydrogels for accelerated infected wound healing. Adv Sci (Weinh), 2021, 8(24): e2102545.
40.	潘杉, 张玉彬. 慢性伤口的益生菌疗法. 药物生物技术, 2020, 27(3): 281-285.
41.	Peral M C, Rachid M M, Gobbato N M, et al. Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with lactobacillus plantarum. Clin Microbiol Infect, 2010, 16(3): 281-286.
42.	Peral M C, Martinez M A, Valdez J C. Bacteriotherapy with lactobacillus plantarum in burns. Int Wound J, 2009, 6(1): 73-81.
43.	Mohseni S, Bayani M, Bahmani F, et al. The beneficial effects of probiotic administration on wound healing and metabolic status in patients with diabetic foot ulcer: a randomized, double-blind, placebo-controlled trial. Diabetes Metab Res Rev, 2018, 34(3). DOI: 10. 1002/dmrr. 2970.
44.	Kasatpibal N, Whitney J D, Saokaew S, et al. Effectiveness of probiotic, prebiotic, and synbiotic therapies in reducing postoperative complications: a systematic review and network meta-analysis. Clin Infect Dis, 2017, 64(suppl_2): S153-S160.

1. 高金梅. 伤口分期治疗及辅料的使用. 甘肃科技, 2017, 33(17): 113-114.
2. 中华医学会创伤学分会组织修复专业委员会(组). 慢性伤口诊疗指导意见(2011版)第4讲创伤性溃疡. 中国临床医生, 2011, 39(12): 55-57.
3. 钟果玉, 谭惠仪, 叶雪梅, 等. 慢性伤口细菌生物膜管理的研究进展. 护理实践与研究, 2021, 18(12): 1790-1794.
4. Attinger C, Wolcott R. Clinically addressing biofilm in chronic wounds. Adv Wound Care (New Rochelle), 2012, 1(3): 127-132.
5. Zhao G, Usui M L, Lippman S I, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle), 2013, 2(7): 389-399.
6. Tejero-sarinena S, Barlow J, Costabile A, et al. In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe, 2012, 18(5): 530-538.
7. Rainer B M, Thompson K G, Antonescu C, et al. Characterization and analysis of the skin microbiota in rosacea: a case-control study. Am J Clin Dermatol, 2020, 21(1): 139-147.
8. Zipperer A, Konnerth M C, Laux C, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature, 2016, 535(7613): 511-516.
9. Xu H, Jeong H S, Lee H Y, et al. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett Appl Microbiol, 2009, 49(4): 434-442.
10. Zakaria Gomaa E. Antimicrobial and anti-adhesive properties of biosurfactant produced by lactobacilli isolates, biofilm formation and aggregation ability. J Gen Appl Microbiol, 2013, 59(6): 425-436.
11. Živković M, Miljković M S, Ruas-Madiedo P, et al. EPS-SJ exopolisaccharide produced by the strain lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front Microbiol, 2016, 7: 286.
12. Scheffold A, Bacher P, LeibundGut-Landmann S. T cell immunity to commensal fungi. Curr Opin Microbiol, 2020, 8: 116-123.
13. Claudel J P, Auffret N, Leccia M T, et al. Staphylococcus epidermidis: a potential new player in the physiopathology of acne?. Dermatology, 2019, 235(4): 287-294.
14. Sultana R, McBain A J, O'Neill C A. Strain-dependent augmentation of tight-junction barrier function in human primary epidermal keratinocytes by lactobacillus and bifidobacterium lysates. Appl Environ Microbiol, 2013, 79(16): 4887-4894.
15. Park Y J, Lee H K. The role of skin and orogenital microbiota in protective immunity and chronic immune-mediated inflammatory disease. Front Immunol, 2018, 8: 1955.
16. Fijan S, Frauwallner A, Langerholc T, et al. Efficacy of using probiotics with antagonistic activity against pathogens of wound infections: an integrative review of literature. Biomed Res Int, 2019, 2019: 7585486.
17. Rutherford S T, Bassler B L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med, 2012, 2(11): a012427.
18. Ramos A N, Cabral M E, Noseda D, et al. Antipathogenic properties of lactobacillus plantarum on pseudomonas aeruginosa: the potential use of its supernatants in the treatment of infected chronic wounds. Wound Repair Regen, 2012, 20(4): 552-562.
19. Paharik A E, Parlet C P, Chung N, et al. Coagulase-negative staphylococcal strain prevents staphylococcus aureus colonization and skin infection by blocking quorum sensing. Cell Host Microbe, 2017, 22(6): 746-756.
20. Monnappa A K, Dwidar M, Seo J K, et al. Bdellovibrio bacteriovorus inhibits staphylococcus aureus biofilm formation and invasion into human epithelial cells. Sci Rep, 2014, 4: 3811.
21. Naseri S, Lepry W C, Nazhat S N. Bioactive glasses in wound healing: hope or hype?. J Mater Chem B, 2017, 5(31): 6167-6174.
22. Duan T, Du Y, Xing C, et al. Toll-like receptor signaling and its role in cell-mediated immunity. Front Immunol, 2022, 13: 812774.
23. Lai Y, Di Nardo A, Nakatsuji T, et al. Commensal bacteria regulate toll-like receptor 3-dependent inflammation after skin injury. Nat Med, 2009, 15(12): 1377-1382.
24. Kim C K, Karau M J, Greenwood-Quaintance K E, et al. Superantigen-producing staphylococcus aureus elicits systemic immune activation in a murine wound colonization model. Toxins (Basel), 2015, 7(12): 5308-5319.
25. Tsai W H, Chou C H, Huang T Y, et al. Heat-killed lactobacilli preparations promote healing in the experimental cutaneous wounds. Cells, 2021, 10(11): 3264.
26. Linehan J L, Harrison O J, Han S J, et al. Non-classical immunity controls microbiota impact on skin immunity and tissue repair. Cell, 2018, 172(4): 784-796.
27. Luqman A, Nega M, Nguyen M T, et al. SadA-expressing staphylococci in the human gut show increased cell adherence and internalization. Cell Rep, 2018, 22(2): 535-545.
28. Pullar C E, Isseroff R R. The beta 2-adrenergic receptor activates pro-migratory and pro-proliferative pathways in dermal fibroblasts via divergent mechanisms. J Cell Sci, 2006, 119(Pt 3): 592-602.
29. Luqman A, Muttaqin M Z, Yulaipi S, et al. Trace amines produced by skin bacteria accelerate wound healing in mice. Commun Biol, 2020, 3(1): 277.
30. Mohammedsaeed W, Cruickshank S, McBain A J, et al. Lactobacillus rhamnosus GG lysate increases re-epithelialization of keratinocyte scratch assays by promoting migration. Sci Rep, 2015, 5: 16147.
31. Poutahidis T, Kearney S M, Levkovich T, et al. Microbial symbionts accelerate wound healing via the neuropeptide hormone oxytocin. PLoS One, 2013, 8(10): e78898.
32. Varian B J, Poutahidis T, DiBenedictis B T, et al. Microbial lysate upregulates host oxytocin. Brain Behav Immun, 2017, 61: 36-49.
33. Alves E, Gregório J, Baby A R, et al. Homemade kefir consumption improves skin condition-a study conducted in healthy and atopic volunteers. Foods, 2021, 10(11): 2794.
34. Benyacoub J, Bosco N, Blanchard C, et al. Immune modulation property of lactobacillus paracasei NCC2461 (ST11) strain and impact on skin defences. Benef Microbes, 2014, 5(2): 129-136.
35. Erdman S E, Poutahidis T. Probiotic 'glow of health': it's more than skin deep. Benef Microbes, 2014, 5(2): 109-119.
36. Rooj A K, Kimura Y, Buddington R K. Metabolites produced by probiotic lactobacilli rapidly increase glucose uptake by Caco-2 cells. BMC Microbiol, 2010, 10: 16.
37. Jones M L, Martoni C J, Prakash S. Oral supplementation with probiotic L. reuteri NCIMB 30242 increases mean circulating 25-hydroxyvitamin D: a post hoc analysis of a randomized controlled trial. J Clin Endocrinol Metab, 2013, 98(7): 2944-2951.
38. De Angelis M, Bottacini F, Fosso B, et al. Lactobacillus rossiae, a vitamin B12 producer, represents a metabolically versatile species within the genus lactobacillus. PLoS One, 2014, 9(9): e107232.
39. Ming Z, Han L, Bao M, et al. Living bacterial hydrogels for accelerated infected wound healing. Adv Sci (Weinh), 2021, 8(24): e2102545.
40. 潘杉, 张玉彬. 慢性伤口的益生菌疗法. 药物生物技术, 2020, 27(3): 281-285.
41. Peral M C, Rachid M M, Gobbato N M, et al. Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with lactobacillus plantarum. Clin Microbiol Infect, 2010, 16(3): 281-286.
42. Peral M C, Martinez M A, Valdez J C. Bacteriotherapy with lactobacillus plantarum in burns. Int Wound J, 2009, 6(1): 73-81.
43. Mohseni S, Bayani M, Bahmani F, et al. The beneficial effects of probiotic administration on wound healing and metabolic status in patients with diabetic foot ulcer: a randomized, double-blind, placebo-controlled trial. Diabetes Metab Res Rev, 2018, 34(3). DOI: 10. 1002/dmrr. 2970.
44. Kasatpibal N, Whitney J D, Saokaew S, et al. Effectiveness of probiotic, prebiotic, and synbiotic therapies in reducing postoperative complications: a systematic review and network meta-analysis. Clin Infect Dis, 2017, 64(suppl_2): S153-S160.

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