1887

Abstract

Microbial species can act in synergy to circumvent environmental stress conditions and survive. In addition, biofilms are a serious public-health issue globally and constitute a clinical emergency. Infection persistence, increased morbidity and mortality, and antibiotic resistance are consequences of poly-microbial synergy. Due to inherited complexity and synergy between numerous species, newer antimicrobial agents of increased efficacy and tolerability are needed. In this unique medical case, a chronic (9 year) multi-bacterial scalp infection was differentially diagnosed from other inflammatory skin disorders by prolonged microbiological culture. The bacterial species found seem to have caused lesions of visible biofilm not documented previously in the medical literature. This complicated infection was treated successfully and rapidly with the combined topical application of the active halogen compounds -chlorotaurine, -bromotaurine and bromamine T, which is in contrast to the previous failed systemic and topical therapeutic approaches. This study strengthens the case for the use of active halogen compounds against multi-bacterial infections of the skin in the future, without the occurrence of resistance.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. The Microbiology Society waived the open access fees for this article.
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2020-04-24
2024-03-29
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References

  1. Murray JL, Connell JL, Stacy A, Turner KH, Whiteley M. Mechanisms of synergy in polymicrobial infections. J Microbiol 2014; 52:188–199 [View Article]
    [Google Scholar]
  2. Björkqvist M, Liljedahl M, Zimmermann J, Schollin J, Söderquist B. Colonization pattern of coagulase-negative staphylococci in preterm neonates and the relation to bacteremia. Eur J Clin Microbiol Infect Dis 2010; 29:1085–1093 [View Article][PubMed]
    [Google Scholar]
  3. Barsoumian AE, Mende K, Sanchez CJ, Beckius ML, Wenke JC et al. Clinical infectious outcomes associated with biofilm-related bacterial infections: a retrospective chart review. BMC Infect Dis 2015; 15:223 [View Article]
    [Google Scholar]
  4. Nobile CJ, Johnson AD. Candida albicans biofilms and human disease. Annu Rev Microbiol 2015; 69:71–92. [View Article][PubMed]
    [Google Scholar]
  5. Krause J, Geginat G, Tammer I. Prostaglandin E2 from Candida albicans stimulates the growth of Staphylococcus aureus in mixed biofilms. PLoS One 2015; 10:e0135404. [View Article][PubMed]
    [Google Scholar]
  6. van der Gast CJ, Walker AW, Stressmann FA, Rogers GB, Scott P et al. Partitioning core and satellite taxa from within cystic fibrosis lung bacterial communities. Isme J 2011; 5:780–791 [View Article][PubMed]
    [Google Scholar]
  7. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA 2012; 109:5809–5814 [View Article][PubMed]
    [Google Scholar]
  8. Rogers GB, Hart CA, Mason JR, Hughes M, Walshaw MJ et al. Bacterial diversity in cases of lung infection in cystic fibrosis patients: 16S ribosomal DNA (rDNA) length heterogeneity PCR and 16S rDNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 2003; 41:3548–3558 [View Article][PubMed]
    [Google Scholar]
  9. Barsoumian AE, Mende K, Sanchez CJ, Beckius ML, Wenke JC et al. Clinical infectious outcomes associated with biofilm-related bacterial infections: a retrospective chart review. BMC Infect Dis 2015; 15:223 [View Article][PubMed]
    [Google Scholar]
  10. Akers KS, Mende K, Cheatle KA, Zera WC, Yu X et al. Biofilms and persistent wound infections in United States military trauma patients: a case-control analysis. BMC Infect Dis 2014; 14:190. [View Article][PubMed]
    [Google Scholar]
  11. Price LB, Liu CM, Melendez JH, Frankel YM, Engelthaler D et al. Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS One 2009; 4:e6462 [View Article][PubMed]
    [Google Scholar]
  12. Brook I. Secondary bacterial infections complicating skin lesions. J Med Microbiol 2002; 51:808–812 [View Article][PubMed]
    [Google Scholar]
  13. Olesen BA. Chronic skin disease and risk of infection. Open Infect Dis J 2012; 6:60–64 [View Article]
    [Google Scholar]
  14. Murray JL, Connell JL, Stacy A, Turner KH, Whiteley M. Mechanisms of synergy in polymicrobial infections. J Microbiol 2014; 52:188–199 [View Article][PubMed]
    [Google Scholar]
  15. Bjarnsholt T. The role of bacterial biofilms in chronic infections. APMIS 2013; 121:1–58 [View Article][PubMed]
    [Google Scholar]
  16. Sanchez CJ, Mende K, Beckius ML, Akers KS, Romano DR et al. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 2013; 13:47 [View Article][PubMed]
    [Google Scholar]
  17. Gottardi W, Nagl M. N-Chlorotaurine, a natural antiseptic with outstanding tolerability. J Antimicrob Chemother 2010; 65:399–409. [View Article][PubMed]
    [Google Scholar]
  18. Marcinkiewicz J. Taurine bromamine (TauBr) – its role in immunity and new perspectives for clinical use. J Biomed Sci 2010; 17 (Suppl 1):S3 [View Article][PubMed]
    [Google Scholar]
  19. Kyriakopoulos AM, Logotheti S, Marcinkiewicz J, Nagl M. N-Chlorotaurine and N-bromotaurine combination regimen for the cure of valacyclovir-unresponsive herpes zoster comorbidity in a multiple sclerosis patient. IJMPCR 2016; 7:1–6 [View Article]
    [Google Scholar]
  20. Kyriakopoulos AM, Grapsa E, Marcinkiewicz J, Nagl M. Swift cure of a chronic wound infected with multiresistant Staphylococcus aureus in an elderly patient with stage 5 renal disease. Int J Low Extrem Wounds 2019; 18:192–196 [View Article][PubMed]
    [Google Scholar]
  21. Marcinkiewicz J, Strus M, Walczewska M, Machul A, Mikołajczyk D. Influence of taurine haloamines (TauCl and TauBr) on the development of Pseudomonas aeruginosa biofilm: a preliminary study. Adv Exp Med Biol 2013; 775:269–283 [View Article][PubMed]
    [Google Scholar]
  22. Walczewska M, Peruń A, Białecka A, Śróttek M, Jamróz W et al. Comparative analysis of microbicidal and anti-inflammatory properties of novel taurine bromamine derivatives and bromamine T. Adv Exp Med Biol 2017; 975:515–534 [View Article][PubMed]
    [Google Scholar]
  23. Clark AE, Kaleta EJ, Arora A, Wolk DM. Matrix-assisted laser desorption ionization-time of flight mass spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin Microbiol Rev 2013; 26:547–603 [View Article][PubMed]
    [Google Scholar]
  24. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters, version 9.0; 2019
  25. Böttcher B, Sarg B, Lindner HH, Nagl M. Inactivation of microbicidal active halogen compounds by sodium thiosulphate and histidine/methionine for time-kill assays. J Microbiol Methods 2017; 141:42–47. [View Article][PubMed]
    [Google Scholar]
  26. Ramirez GA, Yacoub MR, Ripa M, Mannina D, Cariddi A et al. Eosinophils from physiology to disease: a comprehensive review. Biomed Res Int 2018; 2018:9095275
    [Google Scholar]
  27. Panuncialman J, Falanga V. Unusual causes of cutaneous ulceration. Surg Clin North Am 2010; 90:1161–1180. [View Article][PubMed]
    [Google Scholar]
  28. Jay SM, Skokos EA, Zeng J, Knox K, Kyriakides TR. Macrophage fusion leading to foreign body giant cell formation persists under phagocytic stimulation by microspheres in vitro and in vivo in mouse models. J Biomed Mater Res A 2010; 93:189–199. [View Article][PubMed]
    [Google Scholar]
  29. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999; 284:1318–1322.
    [Google Scholar]
  30. Biaggini K, Barbey C, Borrel V, Feuilloley M, Déchelotte P et al. The pathogenic potential of Pseudomonas fluorescens MFN1032 on enterocytes can be modulated by serotonin, substance P and epinephrine. Arch Microbiol 2015; 197:983–990. [View Article][PubMed]
    [Google Scholar]
  31. Scales BS, Dickson RP, LiPuma JJ, Huffnagle GB. Microbiology, genomics, and clinical significance of the Pseudomonas fluorescens species complex, an unappreciated colonizer of humans. Clin Microbiol Rev 2014; 27:927–948. [View Article][PubMed]
    [Google Scholar]
  32. Kim M, Christley S, Khodarev NN, Fleming I, Huang Y et al. Pseudomonas aeruginosa wound infection involves activation of its iron acquisition system in response to fascial contact. J Trauma Acute Care Surg 2015; 78:823–829. [View Article][PubMed]
    [Google Scholar]
  33. Heldt Manica LA, Cohen PR. Staphylococcus lugdunensis infections of the skin and soft tissue: a case series and review. Dermatol Ther 2017; 7:555–562. [View Article][PubMed]
    [Google Scholar]
  34. Missineo A, Di Poto A, Geoghegan JA, Rindi S, Heilbronner S et al. IsdC from Staphylococcus lugdunensis induces biofilm formation under low-iron growth conditions. Infect Immun 2014; 82:2448–2459. [View Article][PubMed]
    [Google Scholar]
  35. Facklam R, Elliott JA. Identification, classification, and clinical relevance of catalase-negative, gram-positive cocci, excluding the streptococci and enterococci. Clin Microbiol Rev 1995; 8:479–495. [View Article][PubMed]
    [Google Scholar]
  36. Parrey AH, Sofi F, Ahmad M, Kuchay A. Aerococcus viridans infection presenting as cutaneous vasculitis in an immunocompetent patient. Reumatologia 2016; 54:318–320. [View Article][PubMed]
    [Google Scholar]
  37. Tena D, Martinez-Torres JA, Perez-Pomata MT, Sáez-Nieto JA, Rubio V et al. Cutaneous infection due to Bacillus pumilus: report of 3 cases. Clin Infect Dis 2007; 44:e40–e42. [View Article][PubMed]
    [Google Scholar]
  38. Kimouli M, Vrioni G, Papadopoulou M, Koumaki V, Petropoulou D et al. Two cases of severe sepsis caused by Bacillus pumilus in neonatal infants. J Med Microbiol 2012; 61:596–599. [View Article][PubMed]
    [Google Scholar]
  39. Clemente L, Dragovic D, Milocco C, Fontana F. Report of a rare case of sepsis caused by Bacillus pumilus in an immunocompetent child with the involvement of soft tissues cellulitis. Microbiologia Medica 2016; 31:6289 [View Article]
    [Google Scholar]
  40. Falagas ME, Vouloumanou EK, Samonis G, Vardakas KZ. Fosfomycin. Clin Microbiol Rev 2016; 29:321–347. [View Article][PubMed]
    [Google Scholar]
  41. dos Ramos Almeida CJL, da Silva SM, Napoleão TH, da Silva MV, de Oliveira MBM. Biofilm formation in Bacillus cereus, B. licheniformis and B. pumilus: an alternative for survival in impacted environments. Int J Sci 2017; 3:73–78 [View Article]
    [Google Scholar]
  42. Cairns LS, Hobley L, Stanley-Wall NR. Biofilm formation by Bacillus subtilis: new insights into regulatory strategies and assembly mechanisms. Mol Microbiol 2014; 93:587–598. [View Article][PubMed]
    [Google Scholar]
  43. Kandi V, Palange P, Vaish R, Bhatti AB, Kale V et al. Emerging bacterial infection: identification and clinical significance of Kocuria species. Cureus 2016; 8:e731. [View Article][PubMed]
    [Google Scholar]
  44. Pulcrano G, Balzaretti M, Grosini A, Piacentini V, Poddighe D. First report of Kocuria marina bloodstream infection unrelated to a central venous catheter: a mini-review on an emerging and under-recognized opportunistic pathogen. Infez Med 2017; 25:71–74[PubMed]
    [Google Scholar]
  45. Ananieva M, Nazarchuk O, Faustova M, Basarab Y, Loban G. Pathogenicity factors of Kocuria kristinae contributing to the development of peri-implant mucositis. Malaysian J Med Health Sci 2018; 14:34–38
    [Google Scholar]
  46. Cui B, Smooker PM, Rouch DA, Daley AJ, Deighton MA. Differences between two clinical Staphylococcus capitis subspecies as revealed by biofilm, antibiotic resistance, and pulsed-field gel electrophoresis profiling. J Clin Microbiol 2013; 51:9–14 [View Article][PubMed]
    [Google Scholar]
  47. Møretrø T, Hermansen L, Holck AL, Sidhu MS, Rudi K et al. Biofilm formation and the presence of the intercellular adhesion locus ICA among staphylococci from food and food processing environments. Appl Environ Microbiol 2003; 69:5648–5655. [View Article][PubMed]
    [Google Scholar]
  48. Raghupathi PK, Liu W, Sabbe K, Houf K, Burmølle M et al. Synergistic interactions within a multispecies biofilm enhance individual species protection against grazing by a pelagic protozoan. Front Microbiol 2017; 8:2649 [View Article][PubMed]
    [Google Scholar]
  49. Hook EW, Sande MA. Role of the vegetation in experimental Streptococcus viridans endocarditis. Infect Immun 1974; 10:1433–1438. [View Article][PubMed]
    [Google Scholar]
  50. Sonesson A, Przybyszewska K, Eriksson S, Mörgelin M, Kjellström S et al. Identification of bacterial biofilm and the Staphylococcus aureus derived protease, staphopain, on the skin surface of patients with atopic dermatitis. Sci Rep 2017; 7:8689. [View Article][PubMed]
    [Google Scholar]
  51. Tett A, Pasolli E, Farina S, Truong DT, Asnicar F et al. Unexplored diversity and strain-level structure of the skin microbiome associated with psoriasis. NPJ Biofilms Microbiomes 2017; 3:14 [View Article][PubMed]
    [Google Scholar]
  52. Ehrlich GD, Hu FZ, Shen K, Stoodley P, Post JC. Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin Orthop Relat Res 2005; 437:20–24. [View Article][PubMed]
    [Google Scholar]
  53. Wu H, Moser C, Wang H-Z, Høiby N, Song Z-J. Strategies for combating bacterial biofilm infections. Int J Oral Sci 2015; 7:1–7. [View Article][PubMed]
    [Google Scholar]
  54. Chu EK, Kilic O, Cho H, Groisman A, Levchenko A. Self-induced mechanical stress can trigger biofilm formation in uropathogenic Escherichia coli . Nat Commun 2018; 9:4087. [View Article][PubMed]
    [Google Scholar]
  55. Senpuku H, Sogame A, Inoshita E, Tsuha Y, Miyazaki H et al. Systemic diseases in association with microbial species in oral biofilm from elderly requiring care. Gerontology 2003; 49:301–309. [View Article][PubMed]
    [Google Scholar]
  56. Walczewska M, Ciszek-Lenda M, Peruń A, Kiecka A, Nazimek K et al. Combined biological effects of N-bromotaurine analogs and ibuprofen. Part I: influence on inflammatory properties of macrophages. Adv Exp Med Biol 2019; 1155:1015–1031. [View Article][PubMed]
    [Google Scholar]
  57. Coraça-Huber DC, Ammann CG, Fille M, Hausdorfer J, Nogler M et al. Bactericidal activity of N-chlorotaurine against biofilm-forming bacteria grown on metal disks. Antimicrob Agents Chemother 2014; 58:2235–2239 [View Article][PubMed]
    [Google Scholar]
  58. Ammann CG, Fille M, Hausdorfer J, Nogler M, Nagl M et al. Influence of poly-N-acetylglucosamine in the extracellular matrix on N-chlorotaurine mediated killing of Staphylococcus epidermidis . New Microbiol 2014; 37:383–386.[PubMed]
    [Google Scholar]
  59. Gottardi W, Klotz S, Nagl M. Superior bactericidal activity of N-bromine compounds compared to their N-chlorine analogues can be reversed under protein load. J Appl Microbiol 2014; 116:1427–1437. [View Article][PubMed]
    [Google Scholar]
  60. Marcinkiewicz J, Wojas-Pelc A, Walczewska M, Lipko-Godlewska S, Jachowicz R et al. Topical taurine bromamine, a new candidate in the treatment of moderate inflammatory acne vulgaris: a pilot study. Eur J Dermatol 2008; 18:433–439. [View Article][PubMed]
    [Google Scholar]
  61. Arnitz R, Stein M, Bauer P, Lanthaler B, Jamnig H et al. Tolerability of inhaled N-chlorotaurine in humans: a double-blind randomized phase I clinical study. Ther Adv Respir Dis 2018; 12:1753466618778955. [View Article][PubMed]
    [Google Scholar]
  62. 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. [View Article][PubMed]
    [Google Scholar]
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