Skip to main content
Top
Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Probiotics | Research

Impact of probiotics on pathogen survival in an innovative human plasma biofilm model (hpBIOM)

Authors: M. Besser, J. Terberger, L. Weber, B. Ghebremedhin, E. A. Naumova, W. H. Arnold, E. K. Stuermer

Published in: Journal of Translational Medicine | Issue 1/2019

Login to get access

Abstract

Background

Despite of medical advances, the number of patients suffering on non-healing chronic wounds is still increasing. This fact is attended by physical and emotional distress and an economic load. The majority of chronic wounds are infected of harmful microbials in a protecting extracellular matrix. These biofilms inhibit wound healing. Biofilm-growing bacteria developed unique survival properties, which still challenge the appropriate wound therapy. The present in-vitro biofilm models are not suitable for translational research. By means of a novel in-vivo like human plasma biofilm model (hpBIOM), this study systematically analysed the influence of 3 probiotics on the survival of five clinically relevant pathogenic microorganisms.

Methods

Human plasma was used to produce the innovate biofilm. Pathogenic microorganisms were administered to the plasma. By stimulating the production of a fibrin scaffold, stable coagula-like discs with integrated pathogens were produced. The five clinically relevant pathogens P. aeruginosa, S. aureus, S. epidermidis, E. faecium and C. albicans were challenged to the probiotics L. plantarum, B. lactis and S. cerevisiae. The probiotics were administered on top of the biofilm and the survival was quantified after 4 h and 24 h of incubation. For statistics, two-way ANOVA with post-hoc Tukey’s HSD test was applied. P-value > 0.05 was considered to be significant.

Results

SEM micrographs depicted the pathogens on the surface of the fibrin scaffold, arranged in close proximity and produced the glycocalyx. The application of probiotics induced different growth-reducing capacities towards the pathogens. B. lactis and S. cerevisiae showed slight bacteria-reducing properties. The survival of C. albicans was not affected at all. The most antimicrobial activity was detected after the treatment with L. plantarum.

Conclusions

This study successfully reproduced a novel human biofilm model, which provides a human wound milieu and individual immune competence. The success of bacteriotherapy is dependent on the strain combination, the number of probiotics and the activity of the immune cells. The eradicating effect of L. plantarum on P. aeruginosa should be emphasized.
Literature
1.
go back to reference Dissemond J, et al. Diagnosis and treatment of chronic wounds: current standards of Germany's Initiative for Chronic Wounds e V. J Wound Care. 2017;26(12):727–32.PubMedCrossRef Dissemond J, et al. Diagnosis and treatment of chronic wounds: current standards of Germany's Initiative for Chronic Wounds e V. J Wound Care. 2017;26(12):727–32.PubMedCrossRef
2.
go back to reference Krech T, Traber JÜ. Bakterien in chronischen Wunden. Ars Medici. 2010;23:960–4. Krech T, Traber JÜ. Bakterien in chronischen Wunden. Ars Medici. 2010;23:960–4.
3.
go back to reference Siddiqui AR, Bernstein JM. Chronic wound infection: facts and controversies. Clin Dermatol. 2010;28(5):519–26.PubMedCrossRef Siddiqui AR, Bernstein JM. Chronic wound infection: facts and controversies. Clin Dermatol. 2010;28(5):519–26.PubMedCrossRef
5.
go back to reference Costerton JW. Introduction to biofilm. Int J Antimicrob Agents. 1999;11(3–4):217–21 (discussion 237–9).PubMedCrossRef Costerton JW. Introduction to biofilm. Int J Antimicrob Agents. 1999;11(3–4):217–21 (discussion 237–9).PubMedCrossRef
6.
go back to reference Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22.PubMedCrossRef Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22.PubMedCrossRef
7.
go back to reference Zhao G, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle). 2013;2(7):389–99.CrossRef Zhao G, et al. Biofilms and inflammation in chronic wounds. Adv Wound Care (New Rochelle). 2013;2(7):389–99.CrossRef
8.
go back to reference Spiliopoulou AI, et al. Bacterial adhesion, intracellular survival and cytokine induction upon stimulation of mononuclear cells with planktonic or biofilm phase Staphylococcus epidermidis. FEMS Microbiol Lett. 2012;330(1):56–655.PubMedCrossRef Spiliopoulou AI, et al. Bacterial adhesion, intracellular survival and cytokine induction upon stimulation of mononuclear cells with planktonic or biofilm phase Staphylococcus epidermidis. FEMS Microbiol Lett. 2012;330(1):56–655.PubMedCrossRef
9.
go back to reference Tzaneva V, et al. Antibiotic treatment and resistance in chronic wounds of vascular origin. Clujul Med. 2016;89(3):365–70.PubMedPubMedCentral Tzaneva V, et al. Antibiotic treatment and resistance in chronic wounds of vascular origin. Clujul Med. 2016;89(3):365–70.PubMedPubMedCentral
11.
go back to reference Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8.PubMedCrossRef Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8.PubMedCrossRef
12.
go back to reference Stewart PS, et al. Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol. 2001;91(3):525–32.PubMedCrossRef Stewart PS, et al. Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. J Appl Microbiol. 2001;91(3):525–32.PubMedCrossRef
13.
go back to reference Schultz GS, et al. Wound bed preparation: a systematic approach to wound management. Wound Repair Regen. 2003;11(Suppl 1):1–28.CrossRef Schultz GS, et al. Wound bed preparation: a systematic approach to wound management. Wound Repair Regen. 2003;11(Suppl 1):1–28.CrossRef
14.
go back to reference Tacconelli E, et al. Surveillance for control of antimicrobial resistance. Lancet Infect Dis. 2018;18(3):e99–e106.PubMedCrossRef Tacconelli E, et al. Surveillance for control of antimicrobial resistance. Lancet Infect Dis. 2018;18(3):e99–e106.PubMedCrossRef
15.
go back to reference Tacconelli E, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318–27.CrossRef Tacconelli E, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318–27.CrossRef
16.
go back to reference Vuotto C, Longo F, Donelli G. Probiotics to counteract biofilm-associated infections: promising and conflicting data. Int J Oral Sci. 2014;6(4):189–94.PubMedPubMedCentralCrossRef Vuotto C, Longo F, Donelli G. Probiotics to counteract biofilm-associated infections: promising and conflicting data. Int J Oral Sci. 2014;6(4):189–94.PubMedPubMedCentralCrossRef
17.
go back to reference Argenta A, et al. Local application of probiotic bacteria prophylaxes against sepsis and death resulting from burn wound infection. PLoS ONE. 2016;11(10):e0165294.PubMedPubMedCentralCrossRef Argenta A, et al. Local application of probiotic bacteria prophylaxes against sepsis and death resulting from burn wound infection. PLoS ONE. 2016;11(10):e0165294.PubMedPubMedCentralCrossRef
18.
go back to reference Satish L, et al. Local probiotic therapy with Lactobacillus plantarum mitigates scar formation in rabbits after burn injury and infection. Surg Infect (Larchmt). 2017;18(2):119–27.CrossRef Satish L, et al. Local probiotic therapy with Lactobacillus plantarum mitigates scar formation in rabbits after burn injury and infection. Surg Infect (Larchmt). 2017;18(2):119–27.CrossRef
19.
go back to reference Lukic J, et al. Probiotics or pro-healers: the role of beneficial bacteria in tissue repair. Wound Repair Regen. 2017;25(6):912–22.PubMedCrossRef Lukic J, et al. Probiotics or pro-healers: the role of beneficial bacteria in tissue repair. Wound Repair Regen. 2017;25(6):912–22.PubMedCrossRef
20.
go back to reference Sonal Sekhar M, et al. Topical application/formulation of probiotics: will it be a novel treatment approach for diabetic foot ulcer? Med Hypotheses. 2014;82(1):86–8.PubMedCrossRef Sonal Sekhar M, et al. Topical application/formulation of probiotics: will it be a novel treatment approach for diabetic foot ulcer? Med Hypotheses. 2014;82(1):86–8.PubMedCrossRef
21.
go back to reference Zipperer A, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 2016;535(7613):511–6.PubMedCrossRef Zipperer A, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 2016;535(7613):511–6.PubMedCrossRef
22.
go back to reference Francolini I, et al. Antifouling polyurethanes to fight device-related staphylococcal infections: synthesis, characterization, and antibiofilm efficacy. Pathog Dis. 2014;70(3):401–7.PubMedCrossRef Francolini I, et al. Antifouling polyurethanes to fight device-related staphylococcal infections: synthesis, characterization, and antibiofilm efficacy. Pathog Dis. 2014;70(3):401–7.PubMedCrossRef
23.
go back to reference Francolini I, et al. Antifouling and antimicrobial biomaterials: an overview. APMIS. 2017;125(4):392–417.PubMedCrossRef Francolini I, et al. Antifouling and antimicrobial biomaterials: an overview. APMIS. 2017;125(4):392–417.PubMedCrossRef
24.
go back to reference Besser M, Stuermer EK. Efficiency of antiseptics in a novel 3-dimensional human plasma biofilm model (hpBIOM). NPJ Biofilms and Microbiomes. 2019 Besser M, Stuermer EK. Efficiency of antiseptics in a novel 3-dimensional human plasma biofilm model (hpBIOM). NPJ Biofilms and Microbiomes. 2019
25.
go back to reference Purwins S, et al. Cost-of-illness of chronic leg ulcers in Germany. Int Wound J. 2010;7(2):97–102.PubMedCrossRef Purwins S, et al. Cost-of-illness of chronic leg ulcers in Germany. Int Wound J. 2010;7(2):97–102.PubMedCrossRef
26.
go back to reference Misic AM, Gardner SE, Grice EA. The wound microbiome: modern approaches to examining the role of microorganisms in impaired chronic wound healing. Adv Wound Care (New Rochelle). 2014;3(7):502–10.CrossRef Misic AM, Gardner SE, Grice EA. The wound microbiome: modern approaches to examining the role of microorganisms in impaired chronic wound healing. Adv Wound Care (New Rochelle). 2014;3(7):502–10.CrossRef
27.
go back to reference Velnar T, Bailey T, Smrkolj V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res. 2009;37(5):1528–42.PubMedCrossRef Velnar T, Bailey T, Smrkolj V. The wound healing process: an overview of the cellular and molecular mechanisms. J Int Med Res. 2009;37(5):1528–42.PubMedCrossRef
28.
go back to reference Demidova-Rice TN, Hamblin MR, Herman IM. Acute and impaired wound healing: pathophysiology and current methods for drug delivery, part 1: normal and chronic wounds: biology, causes, and approaches to care. Adv Skin Wound Care. 2012;25(7):304–14.PubMedPubMedCentralCrossRef Demidova-Rice TN, Hamblin MR, Herman IM. Acute and impaired wound healing: pathophysiology and current methods for drug delivery, part 1: normal and chronic wounds: biology, causes, and approaches to care. Adv Skin Wound Care. 2012;25(7):304–14.PubMedPubMedCentralCrossRef
30.
go back to reference Baquerizo Nole, K.L., E. Yim, J.E. Keri, Probiotics and prebiotics in dermatology. J Am Acad Dermatol, 2014; 71(4): 814–21.PubMedCrossRef Baquerizo Nole, K.L., E. Yim, J.E. Keri, Probiotics and prebiotics in dermatology. J Am Acad Dermatol, 2014; 71(4): 814–21.PubMedCrossRef
31.
go back to reference Comelli EM, et al. Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci. 2002;110(3):218–24.PubMedCrossRef Comelli EM, et al. Selection of dairy bacterial strains as probiotics for oral health. Eur J Oral Sci. 2002;110(3):218–24.PubMedCrossRef
33.
34.
go back to reference Butler E, et al. A pilot study investigating lactic acid bacterial symbionts from the honeybee in inhibiting human chronic wound pathogens. Int Wound J. 2016;13(5):729–37.PubMedCrossRef Butler E, et al. A pilot study investigating lactic acid bacterial symbionts from the honeybee in inhibiting human chronic wound pathogens. Int Wound J. 2016;13(5):729–37.PubMedCrossRef
35.
go back to reference Valdez JC, et al. Interference of Lactobacillus plantarum with Pseudomonas aeruginosa in vitro and in infected burns: the potential use of probiotics in wound treatment. Clin Microbiol Infect. 2005;11(6):472–9.PubMedCrossRef Valdez JC, et al. Interference of Lactobacillus plantarum with Pseudomonas aeruginosa in vitro and in infected burns: the potential use of probiotics in wound treatment. Clin Microbiol Infect. 2005;11(6):472–9.PubMedCrossRef
36.
go back to reference Ramos AN, 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):552–62.PubMed Ramos AN, 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):552–62.PubMed
37.
go back to reference Ramos AN, et al. Effect of Lactobacillus plantarum and Pseudomonas aeruginosa culture supernatants on polymorphonuclear damage and inflammatory response. Int Immunopharmacol. 2010;10(2):247–51.PubMedCrossRef Ramos AN, et al. Effect of Lactobacillus plantarum and Pseudomonas aeruginosa culture supernatants on polymorphonuclear damage and inflammatory response. Int Immunopharmacol. 2010;10(2):247–51.PubMedCrossRef
38.
go back to reference Ramos AN, et al. Compounds from Lactobacillus plantarum culture supernatants with potential pro-healing and anti-pathogenic properties in skin chronic wounds. Pharm Biol. 2015;53(3):350–8.PubMedCrossRef Ramos AN, et al. Compounds from Lactobacillus plantarum culture supernatants with potential pro-healing and anti-pathogenic properties in skin chronic wounds. Pharm Biol. 2015;53(3):350–8.PubMedCrossRef
39.
go back to reference Tsiouris CG, et al. The efficacy of probiotics as pharmacological treatment of cutaneous wounds: meta-analysis of animal studies. Eur J Pharm Sci. 2017;104:230–9.PubMedCrossRef Tsiouris CG, et al. The efficacy of probiotics as pharmacological treatment of cutaneous wounds: meta-analysis of animal studies. Eur J Pharm Sci. 2017;104:230–9.PubMedCrossRef
Metadata
Title
Impact of probiotics on pathogen survival in an innovative human plasma biofilm model (hpBIOM)
Authors
M. Besser
J. Terberger
L. Weber
B. Ghebremedhin
E. A. Naumova
W. H. Arnold
E. K. Stuermer
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-1990-4

Other articles of this Issue 1/2019

Journal of Translational Medicine 1/2019 Go to the issue