1887

Abstract

. Severely burned patients are susceptible to bacterial infection within their burn wounds, which frequently leads to sepsis, multiple organ failure and death. The opportunistic pathogen , an organism inherently resistant to multiple antibiotics, is a common cause of sepsis in these patients.

. Development of a topical treatment unrelated to conventional antibiotics is essential for prevention of infection and sepsis, leading to a role for the direct application of probiotics or their by-products.

. We examined the effectiveness of 20× concentrated supernatant from strain 63 AM (LgCS) grown in de Man, Rogosa and Sharpe broth in inhibiting biofilms , as well as in reducing wound bioburden and sepsis .

. LgCS inhibited the growth of strain PAO1, prevented its biofilm development and eliminated partially developed PAO1 biofilms. In the murine model of thermal injury, a single injection of LgCS following injury and PAO1 infection reduced mortality to 0 % and prevented systemic spread (sepsis). Furthermore, a second injection of LgCS 24 h after the first eliminated PAO1 from the wound. In the murine dorsal excision infection model, either LgCS or ceftazidime treatment of the PAO1-infected wound significantly reduced the mortality rate among infected mice, while combining LgCS with ceftazidime eliminated mortality.

. These results suggest the potential of LgCS in preventing sepsis from infection in severely burned and other immunocompromised patients.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001066
2019-10-01
2019-10-15
Loading full text...

Full text loading...

References

  1. Argenta A, Satish L, Gallo P, Liu F, Kathju S. Local application of probiotic bacteria prophylaxes against sepsis and death resulting from burn wound infection. PLoS One 2016;11:e0165294 [CrossRef]
    [Google Scholar]
  2. Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 2007;67:351–368 [CrossRef]
    [Google Scholar]
  3. Rafla K, Tredget EE. Infection control in the burn unit. Burns 2011;37:5–15 [CrossRef]
    [Google Scholar]
  4. Worth LJ, Slavin MA. Bloodstream infections in haematology: risks and new challenges for prevention. Blood Rev 2009;23:113–122 [CrossRef]
    [Google Scholar]
  5. Pruitt BA, McManus AT, Kim SH, Goodwin CW. Burn wound infections: current status. World J Surg 1998;22:135–145
    [Google Scholar]
  6. Atiyeh BS, Gunn SW, Hayek SN. State of the art in burn treatment. World J Surg 2005;29:131–148 [CrossRef]
    [Google Scholar]
  7. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E et al. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One 2008;3:e33s6 [CrossRef]
    [Google Scholar]
  8. Fazli M, Bjarnsholt T, Kirketerp-Møller K, Jørgensen B, Andersen AS et al. Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 2009;47:4084–4089 [CrossRef]
    [Google Scholar]
  9. Martin JM, Zenilman JM, Lazarus GS. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J Invest Dermatol 2010;130:38–48 [CrossRef]
    [Google Scholar]
  10. Kirker KR, James GA. In vitro studies evaluating the effects of biofilms on wound-healing cells: a review. APMIS 2017;125:344–352 [CrossRef]
    [Google Scholar]
  11. Malone M, Bjarnsholt T, McBain AJ, James GA, Stoodley P et al. The prevalence of biofilms in chronic wounds: a systematic review and meta-analysis of published data. J Wound Care 2017;26:20–25 [CrossRef]
    [Google Scholar]
  12. Kennedy P, Brammah S, Wills E, Burns WE. Burns, biofilm and a new appraisal of burn wound sepsis. Burns 2010;36:49–56 [CrossRef]
    [Google Scholar]
  13. Malic S, Hill KE, Hayes A, Percival SL, Thomas DW et al. Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA fish). Microbiology 2009;155:2603–2611 [CrossRef]
    [Google Scholar]
  14. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002;15:167–193 [CrossRef]
    [Google Scholar]
  15. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010;35:322–332 [CrossRef]
    [Google Scholar]
  16. Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR et al. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 2005;175:7512–7518 [CrossRef]
    [Google Scholar]
  17. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318–1322 [CrossRef]
    [Google Scholar]
  18. Ammons MCB. Anti-Biofilm strategies and the need for innovations in wound care. Recent Pat Antiinfect Drug Discov 2010;5:10–17 [CrossRef]
    [Google Scholar]
  19. Wolcott RD, Cutting KF, Dowd SE, Percival SL. Types of wounds and infections In Percival S, Cutting K. (editors) Microbiology of Wounds Boca Raton: CRC Press-Taylor & Francis Group; 2010; pp219–232
    [Google Scholar]
  20. Ramos AN, Gobbato N, Rachid M, González L, Yantorno O et al. Effect of Lactobacillus plantarum and Pseudomonas aeruginosa culture supernatants on polymorphonuclear damage and inflammatory response. Int Immunopharmacol 2010;10:247–251 [CrossRef]
    [Google Scholar]
  21. Reid G, Jass J, Sebulsky MT, McCormick JK. Potential uses of probiotics in clinical practice. Clin Microbiol Rev 2003;16:658–672 [CrossRef]
    [Google Scholar]
  22. Watters C, Fleming D, Bishop D, Rumbaugh KP. Host responses to biofilm. Prog Mol Biol Transl Sci 2016;142:193–239 [CrossRef]
    [Google Scholar]
  23. Niku-Paavola ML, Laitila A, Mattila-Sandholm T, Haikara A. New types of antimicrobial compounds produced by Lactobacillus plantarum. J Appl Microbiol 1999;86:29–35 [CrossRef]
    [Google Scholar]
  24. Pridmore RD, Pittet A-C, Praplan F, Cavadini C. Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity. FEMS Microbiol Lett 2008;283:210–215 [CrossRef]
    [Google Scholar]
  25. Gan BS, Kim J, Reid G, Cadieux P, Howard JC. Lactobacillus fermentum RC-14 inhibits Staphylococcus aureus infection of surgical implants in rats. J Infect Dis 2002;185:1369–1372 [CrossRef]
    [Google Scholar]
  26. Puertollano E, Puertollano MA, Cruz-Chamorro L, de Cienfuegos GA, Ruiz-Bravo A et al. Effects of concentrated supernatants recovered from Lactobacillus plantarum on Escherichia coli growth and on the viability of a human promyelocytic cell line. J Appl Microbiol 2009;106:1194–1203 [CrossRef]
    [Google Scholar]
  27. Shokouhfard M, Kermanshahi RK, Shahandashti RV, Feizabadi MM, Teimourian S. The inhibitory effect of a Lactobacillus acidophilus derived biosurfactant on biofilm producer Serratia marcescens. Iran J Basic Med Sci 2015;18:1001–1007
    [Google Scholar]
  28. Ramos AN, Sesto Cabral ME, Noseda D, Bosch A, Yantorno OM 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;58:n/a–562 [CrossRef]
    [Google Scholar]
  29. Cannon JP, Lee TA, Bolanos JT, Danziger LH. Pathogenic relevance of Lactobacillus: a retrospective review of over 200 cases. Eur J Clin Microbiol Infect Dis 2005;24:31–40 [CrossRef]
    [Google Scholar]
  30. Gouriet F, Million M, Henri M, Fournier PE, Raoult D. Lactobacillus rhamnosus bacteremia: an emerging clinical entity. Eur J Clin Microbiol Infect Dis 2012;31:2469–2480 [CrossRef]
    [Google Scholar]
  31. Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M et al. Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 2004;38:62–69 [CrossRef]
    [Google Scholar]
  32. Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M et al. Lactobacillus bacteremia, species identification, and antimicrobial susceptibility of 85 blood isolates. Clin Infect Dis 2006;42:e35–e44 [CrossRef]
    [Google Scholar]
  33. Salminen MK, Tynkkynen S, Rautelin H, Saxelin M, Vaara M et al. Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis 2002;35:1155–1160 [CrossRef]
    [Google Scholar]
  34. Auvray F, Coddeville M, Ritzenthaler P, Dupont L. Plasmid integration in a wide range of bacteria mediated by the integrase of Lactobacillus delbrueckii bacteriophage mv4. J Bacteriol 1997;179:1837–1845 [CrossRef]
    [Google Scholar]
  35. Holloway BW, Krishnapillai V, Morgan AF. Chromosomal genetics of Pseudomonas. Microbiol Rev 1979;43:73–102
    [Google Scholar]
  36. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG et al. Common virulence factors for bacterial pathogenicity in plants and animals. Science 1995;268:1899–1902 [CrossRef]
    [Google Scholar]
  37. Lagendijk EL, Validov S, Lamers GEM, de Weert S, Bloemberg GV. Genetic tools for tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 2010;305:81–90 [CrossRef]
    [Google Scholar]
  38. Choi KH, Schweizer HP. mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 2006;1:153–161 [CrossRef]
    [Google Scholar]
  39. Rumbaugh KP, Griswold JA, Iglewski BH, Hamood AN. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 1999;67:5854–5862
    [Google Scholar]
  40. Thompson MG, Black CC, Pavlicek RL, Honnold CL, Wise MC et al. Validation of a novel murine wound model of Acinetobacter baumannii infection. Antimicrob Agents Chemother 2014;58:1332–1342 [CrossRef]
    [Google Scholar]
  41. Mokoena MP. Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: a mini-review. Molecules 2017;22:1255 [CrossRef]
    [Google Scholar]
  42. Selle K, Klaenhammer TR. Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev 2013;37:915–935 [CrossRef]
    [Google Scholar]
  43. van Heel AJ, de Jong A, Montalbán-López M, Kok J, Kuipers OP. BAGEL3: Automated identification of genes encoding bacteriocins and (non-)bactericidal posttranslationally modified peptides. Nucleic Acids Res 2013;41:W448–W453 [CrossRef]
    [Google Scholar]
  44. van Heel AJ, de Jong A, Song C, Viel JH, Kok J et al. BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res 2018;46:W278–W281 [CrossRef]
    [Google Scholar]
  45. Zouhir A, Hammami R, Fliss I, Hamida JB. A new structure-based classification of gram-positive bacteriocins. Protein J 2010;29:432–439 [CrossRef]
    [Google Scholar]
  46. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped blast and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–3402 [CrossRef]
    [Google Scholar]
  47. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 2006;103:15611–15616 [CrossRef]
    [Google Scholar]
  48. Fanci R, Paci C, Anichini P, Pecile P, Marra G et al. Incidence and molecular epidemiology of Pseudomonas aeruginosa bacteremias in patients with acute leukemia: analysis by pulsed-field gel electrophoresis. New Microbiol 2003;26:353–361
    [Google Scholar]
  49. Koh AY, Priebe GP, Pier GB. Virulence of Pseudomonas aeruginosa in a murine model of gastrointestinal colonization and dissemination in neutropenia. Infect Immun 2005;73:2262–2272 [CrossRef]
    [Google Scholar]
  50. Markou P, Apidianakis Y. Pathogenesis of intestinal Pseudomonas aeruginosa infection in patients with cancer. Front Cell Infect Microbiol 2014;3:115 [CrossRef]
    [Google Scholar]
  51. He J, Baldini RL, Déziel E, Saucier M, Zhang Q et al. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc Natl Acad Sci USA 2004;101:2530–2535 [CrossRef]
    [Google Scholar]
  52. Juárez Tomás MS, Ocaña VS, Wiese B, Nader-Macías ME. Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli. J Med Microbiol 2003;52:1117–1124 [CrossRef]
    [Google Scholar]
  53. Alexandre Y, Le Berre R, Barbier G, Le Blay G. Screening of Lactobacillus spp. for the prevention of Pseudomonas aeruginosa pulmonary infections. BMC Microbiol 2014;14:107 [CrossRef]
    [Google Scholar]
  54. Beis K, Whitfield C, Booth I, Naismith JH. Two-Step purification of outer membrane proteins. Int J Biol Macromol 2006;39:10–14 [CrossRef]
    [Google Scholar]
  55. Alakomi HL, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K et al. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 2000;66:2001–2005 [CrossRef]
    [Google Scholar]
  56. Shi H, Chen Z, Chen D, Kan J. Sublethal injury and recovery of Escherichia coli O157:H7 and K-12 after exposure to lactic acid. Food Control 2017;82:190–195 [CrossRef]
    [Google Scholar]
  57. Wesche AM, Gurtler JB, Marks BP, Ryser ET, Stress RET. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. J Food Prot 2009;72:1121–1138 [CrossRef]
    [Google Scholar]
  58. Valdéz JC, Peral MC, Rachid M, Santana M, Perdigón G. 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;11:472–479 [CrossRef]
    [Google Scholar]
  59. Cicenia A, Santangelo F, Gambardella L, Pallotta L, Iebba V et al. Protective role of postbiotic mediators secreted by Lactobacillus rhamnosus GG versus lipopolysaccharide-induced damage in human colonic smooth muscle cells. J Clin Gastroenterol 2016;50:S140–S144 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001066
Loading
/content/journal/jmm/10.1099/jmm.0.001066
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error