Anti-biofilm activity of natural honey against wound bacteria

Honey: Current Research and Clinical Applications

Volumn , Issue , 2012, Pages 83-106

  Majtan, Juraj ^a,b   Bohova, Jana ^a   Horniackova, Miroslava ^b   Majtan, Viktor ^b  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

^b SLOVAK MEDICAL UNIVERSITY   (Slovakia)

Author keywords

Biofilm; Honeydew honey; Resistance; Wound bacteria

Indexed keywords

EID: 84892443570     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (114)

1. Donlan, RM; Costerton, JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev., 2002, 15, 167-193.
2. James, GA; Swogger, E; Wolcott, R; Pulcini, E; Secor, P; Sestrich, J; Costerton, JW; Stewart, PS. Biofilms in chronic wounds. Wound Repair Regen., 2008, 16, 37-44.
3. Kirketerp-Moller, K; Jensen, PO; Fazli, M; Madsen, KG; Pedersen, J; Moser, C; Tolker-Nielsen, T; Hoiby, N; Givskov, M; Bjarnsholt, T. Distribution, organization, and ecology of bacteria in chronic wounds. J. Clin. Microbiol., 2008, 46, 2717-2722.
4. Bjarnsholt, T; Kirketerp-Moller, K; Jensen, PO; Madsen, KG; Phipps, R; Krogfelt, K; Hoiby, N; Givskov, M. Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen., 2008, 16, 2-10.
5. Bjarnsholt, T; Jensen, PO; Fiandaca, MJ; Pedersen, J; Hansen, CR; Andersen, CB; Pressler, T; Givskov, M; Hoiby, N. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr. Pulmonol., 2009, 44, 547-558.
6. Bjarnsholt, T; Tolker-Nielsen, T; Givskov, M; Janssen, M; Chrsitensen, LH. Detection of bacteria by FISH in culture-negative soft tissue filler lessions. Dermatol. Surg, 2009, 35, 1620-1624.
7. Homoe, P; Bjarnsholt, T; Wessman, M; Sorensen, HC; Johansen, HK. Morphological evidence of biofilm formation in Greenlanders with chronic suppurative otitis media. Eur. Arch. Otorhinolaryngol., 2009, 266, 1533-1538.
8. Burmolle, M; Thomsen, TR; Fazli, M; Dige, I; Christensen, L; Homoe, P; Tvede, M; Nyvad, B; Tolker-Nielsen, T; Givskov, M; Moser, C; Kirketerp-Moller, K; Johansen, HK; Hoiby, N; Jensen, PO; Sorensen, SJ; Bjarnsholt, T. Biofilms in chronic infections - a matter of opportunity - monospecies biofilms in multispecies infection. FEMS Immunol. Med. Microbiol., 2010, 59, 324-336.
9. Davis, SC; Ricotti, C; Cazzaniga, A; Welsh, E; Eagistein, WH; Mertz, PM. Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen., 2008, 16, 23-29.
10. Rhoads, DD; Wolcott, RW; Cutting, KF; Percival, SL (2007) Evidence of biofilms in wounds and potential ramifications. In: Gilbert P, Allison D, Brading M, Pratten J, Spratt D, Upton M (eds) Biofilms: coming of age. BioLine, Manchaster, pp 131-143.
11. Gottrup, F. A specialized wound-healing center concept: importance of a multidisciplinary department strcuture and surgical tretament facilities in the treatment of chronic wounds. Am. J. Surg., 2004, 187, 38S-43S.
12. Brem, H; Stojadinovic, O; Diegelmann, RF; Entero, H; Lee, B; Pastar, I; Golinko, M; Rosenberg, H; Tomic-Canic, M. Molecular markers in patients witch chronic wounds to guide surgical debridement. Mol. Med., 2007, 13, 30-39.
13. Menke, NB; Ward, KR; Witten, TM; Bonchev, DG; Diegelmann, RF. Impaired wound healing. Clin. Dermatol., 2007, 25, 19-25.
14. Walmsley, S (2002) Advances in wound management: executive summary Clinica Reports, . PJB Publications Ltd, London.
15. Dowd, SE; Sun, Y; Secor, PR; Rhoads, DD; Wolcott, BM; James, GA; Wolcott, RD. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol., 2008, 8, 43.
16. Frank, DN; Wysocki, A; Specht-Glick, DD; Rooney, A; Feldman, RA; Amand, AL; Pace, NR; Trent, JD. Microbial diversity in chronic open wounds. Wound Repair Regen., 2009, 2, 163-172.
17. Price, LB; Liu, CM; Melendez, JH; Frenkel, YM; Engelthaler, D; Aziz, M; Bowers, J; Ravel, J; Kingsley, C; Keim, PS; Lazarus, GS; Zenilman, JM. Comminity analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound bacteria microbiota. PLoS ONE, 2009, 7, e6462.
18. Martin, JM; Zenilman, JM; Lazarus, GS. Molecular microbiology: new dimensions for cutanous biology and wound healing. J. Invest. Dermatol., 2010, 1, 38-48.
19. Schaber, JA; Triffo, WJ; Suh, SJ; Oliver, JW; Hastert, MC; Griswold, JA; Auer, M; Hamood, AN; Rumbaugh, KP. Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect. Immun., 2007, 75, 715-721.
20. Davies, DG; Parsek, MR; Pearson, JP; Iglewski, BH; Costerton, JW; Greenberg, EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 1998, 280, 295-298.
21. Monroe, D. Looking for chinks in the armor of bacterial biofilm. PLoS Biol., 2007, 5, e307.
22. Winson, MK; Camara, M; Latifi, A; Foglino, M; Chhabra, SR; Daykin, M; Bally, M; Chapon, V; Salmond, GP; Bycroft, BW; Lazdunski, A; Stewart, GSAB; Williams, P. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U S A, 1995, 92, 9427-9431.
23. Gram, L; Grossart, HP; Schlingloff, A; Kiorboe, T. Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl. Environ. Microbiol., 2002, 68, 4111-4116.
24. Miller, MB; Bassler, BL. Quorum sensing in bacteria. Annu. Rev. Microbiol., 2001, 55, 165-199.
25. Fuqua, C; Winans, SC; Greenberg, EP. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol., 1996, 50, 727-751.
26. Li, YH; Tang, N; Aspiras, MB; Lau, PC; Lee, JH; Elen, RP; Cvitkovitch, DG. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol., 2002, 184, 2699-2708.
27. Costerton, JW; Stewart, PS. Battling biofilms. Sci. Am., 2001, 285, 74-81.
28. Flemming, HC; Wingender, J. Relevance of microbial extracelullar polymeric substances (EPSs) - Part I: Structural and ecological aspects. Water Sci. Technol., 2001, 43, 1-6.
29. Brady, RAL, J G; Calhoun, JH; Costerton, JW; Schirtliff, ME. Osteomyelitis and the role of biofilms in chronic infection. FEMS Immunol. Med. Microbiol,. 2008, 52, 13-22.
30. Stewart, PS; Franklin, MJ. Physiological heterogenity in biofilms. Nat. Rev. Microbiol., 2008, 6, 199-210.
31. Nickel, JC; Ruseska, I; Wright, JB; Costerton, JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob. Agents Chemother., 1985, 27, 619-624.
32. Donlan, RM. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis., 2001, 33, 1387-1392.
33. Wolcott, BM; Ehrlich, GD. Biofilms and chronic infections. JAMA, 2008, 299, 2682-2684.
34. Xu, KD; McFeters, GA; Stewart, PS. Biofilm resistance to antimicobial agents. Microbiology, 2000, 146, 547-549.
35. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov., 2003, 2, 114-122.
36. Rachid, S; Ohlsen, K; Witte, W; Hacker, J; Zeibuhr, W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercelullar adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob. Agents Chemother., 2000, 44, 3357-3363.
37. O'Toole, GA; Stewart, PS. Biofilms strike back. Nat. Biotechnol., 2005, 23, 1378-1379.
38. Spoering, AL; Lewis, K. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to kiling by antimicrobials. J. Bacteriol., 2001, 183, 6746-6751.
39. Suci, PA; Mittelman, MW; Yu, FP; Geesey, GG. Investigation of ciprofloxacin penetration into Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother., 1994, 38, 2125-2133.
40. Gordon, CAH, N A; Mrriott, C. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother., 1988, 22, 667-674.
41. Costerton, JW; Cheng, KJ; Geesey, GG; Ladd, TI; Nickel, JC; Dasgupta, M; Marrie, TJ. Bacterial biofilms in nature and disease. Annu. Rev. Microbiol., 1987, 41, 435-464.
42. Kumon, H; Tomochika, K; Matunaga, T; Ogawa, M; Ohmori, H. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol. Immunol., 1994, 38, 615-619.
43. Shigeta, M; Tanaka, G; Komatsuzawa, H; Sugai, M; Suginaka, H; Usui, T. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy, 1997, 43, 340-345.
44. Tresse, O; Jouenne, T; Junter, G. The role of oxygen in the resistance of agar-entrapped, sessile-like Escherichia coli to aminoglycoside and beta-lactam antibiotics. J. Antimicrob. Chemother., 1995, 36, 521-526.
45. Cochran, WL; McFeters, GA; Stewart, PS. Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine. J. Appl. Microbiol., 2000, 88, 22-30.
46. Yasuda, H; Ajiki, Y; Koga, T; Kawada, H; Yokota, T. Interaction between biofilms formed by Pseudomonas aeruginosa and clarithromycin. Antimicrob. Agents Chemother., 1993, 37, 1749-1755.
47. Goto, T; Nakame, Y; Nishida, M; Ohi, Y. Bacterial biofilms and catheters in experimental urinary tract infection. Int. J. Antimicrob. Agents, 1999, 11, 227-231.
48. Brooun, A; Liu, S; Lewis, K. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother., 2000, 44, 640-646.
49. Keren, I; Shah, D; Spoering, AL; Kaldalu, N; Lewis, K. Specialized persiter cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol., 2004, 186, 8172-8180.
50. Moyed, HS; Bertrand, KP. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. Journal of Bacteriology 1983, 155, 557-564.
51. RIckard, AH; Gilbert, P; High, NJ; Kolenbrander, PE; Handley, PS. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol., 2003, 11, 94-100.
52. Burmolle, M; Webb, JSR, D; Hansen, LH; Sorensen, SJ; Kjelleberg, S. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilm. Appl. Environ. Microbiol., 2006, 72, 3916-3923.
53. Ammons, CB. Anti-biofilm strategies and the need for innovations in wound care. Recent Pat. Antiinfect. Drug Discov., 2010, 5, 10-17.
54. Molan, PC. The antibacterial nature of honey. 1. The nature of the antibacterial activity. Bee World, 1992, 73, 5-28.
55. Blair, SE; Carter, DA. The potential for honey in the management of wounds and infections. J. Australian Infect. Control, 2005, 10, 24-31.
56. Allen, KL; Molan, PC; Reid, GM. A survey of the antibacterial activity of some New Zealand honeys. J. Pharm. Pharmacol., 1991, 43, 817-822.
57. Lusby, PE; Coombes, AL; Wilkinson, JM. Bactericidal activity of different honeys against pathogenic bacteria. Arch. Med. Res., 2005, 36, 464-467.
58. Molan, PC. The evidence supporting the use of honey as a wound dressing. Int. J. Low Extrem. Wounds, 2006, 5, 40-54.
59. Lin, SM; Molan, PC; Cursons, RT. The in vitro susceptibility of Campylobacter spp. to the antibacterial effect of manuka honey. Eur. J. Clin. Microbiol. Infect. Dis., 2009, 28, 339-344.
60. Tonks, AJ; Cooper, RA; Jones, KP; Blair, S; Parton, J; Tonks, A. Honey stimulates inflammatory cytokine production from monocytes. Cytokine, 2003, 21, 242-247.
61. Majtan, J; Kovacova, E; Bilikova, K; Simuth, J. The immunostimulatory effect of the recombinant apalbumin 1-major honeybee royal jelly protein-on TNFα release. Int. Immunopharmacol., 2006, 6, 269-278.
62. van den Berg, AJ; van den Worm, E; van Ufford, HC; Halkes, MJ; Hoekstra, MJ; Beukelman, CJ. An in vitro examination of the antioxidant and anti-inflammatory properties of buckwheat honey. J. Wound Care, 2008, 17, 172-178.
63. Ahmad, A; Khan, RA; Mesaik, MA. Anti inflammatory effect of natural honey on bovine thrombin-induced oxidative burst in phagocytes. Phytother. Res., 2009, 23, 801-808.
64. Majtan, J; Kumar, P; Majtan, T; Walls, AF; Klaudiny, J. Effect of honey and its major royal jelly protein 1 on cytokine and MMP-9 mRNA transcripts in human keratinocytes. Exp. Dermatol., 2010, 19, e73-e79.
65. Adams, CJ; Boult, CH; Deadman, BJ; Farr, JM; Grainger, MNC; Manley-Harris, M; Snow, MJ. Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey. Carbohydr. Res., 2008, 343, 651-659.
66. Mavric, E; Wittmann, S; Barth, G; Henle, T. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Mol. Nutr. Food Res., 2008, 52, 483-489.
67. Kwakman, PH; te Velde, AA; De Boer, L; Speijer, D; Vandenbroucke-Grauls, CM; Zaat, SA. How honey kills bacteria. FASEB J., 2010, 24, 2576-2582.
68. Estevinho, L; Pereira, AP; Moreira, L; Dias, LG; Pereira, E. Antioxidant and antimicrobial effects of phenolic compounds extracts of Northeast Portugal honey. Food Chem. Toxicol., 2008, 46, 3774-3779.
69. Aljadi, AM; Yusoff, KM. Isolation and identification of phenolic acids in Malaysian honey with antibacterial properties. Turk. J. Med. Sci., 2003, 33, 229-236.
70. Wahdan, HA. Causes of the antimicrobial activity of honey. Infection, 1998, 26, 26-31.
71. Jull, A; Rodgers, A; Walker, N. Honey as a topical treatment for wounds. Cohrane Database Syst. Rev., 2008, (4), Art. No. CD005083.
72. Jull, A; Walker, N; Parag, V; Molan, P; Rodgers, A. Randomized clinical trial of honey-impregnated dressings for venous leg ulcers. Br. J. Surg., 2008, 95, 175-182.
73. Gethin, G; Cowman, S. Manuka honey vs.hydrogel - a prospective, open label, multicentre, randomised contolled trial to compare desloughing efficacy and healing outcomes in venous ulcers. J. Clin. Nurs., 2008, 18, 466-474.
74. Robson, V; Dodd, S; Thomas, S. Standardized antibacterial honey (Medihoney) with standard therapy in wound care: randomized clinical trial. J. Adv. Nurs., 2009, 65, 565-575.
75. Weheida, SM; Nagubib, HH; El-Banna, HM; Marzouk, S. Comparing the effects of two dressing techniques on healing of low grade pressure ulcers. J. Med. Res. Inst., 1991, 12, 259-278.
76. Al-Waili, NS; Sallom, KY. Effects of topical honey on post-operative wounds infections due to gram positive and gram negative bacteria following caesarean sections and hysterectomies. Eur. J. Med. Res., 1999, 4, 126-130.
77. Subrahmanyam, M; Ugane, SP. Honey dressing beneficial in treatment of Fournier's gangrene. Indian J. Surg., 2004, 66, 75-77.
78. Shukrimi, A; Sulaiman, AR; Halim, AY; Azril, A. A comparative study between honey and povidone iodine as dressing solution for Wagner type II diabetic foot ulcers. Med. J. Malaysia, 2008, 63, 44-46.
79. Eddy, JJ; Gideonsen, MD. Topical honey for diabetic ulcers. J. Fam. Pract., 2005, 54, 533-535.
80. Merckoll, P; Jonassen, TO; Vad, ME; Jeansson, SL; Melby, KK. Bacteria, biofilm and honey: a study of the effects of honey on 'planktonic' and biofilm-embedded chronic wound bacteria. Scand. J. Infect. Dis., 2009, 41, 341-347.
81. Truchado, P; Gil-Izquierdo, A; Tomas-Barberan, FA; Allende, A. Inhibition by chestnut honey of N-acyl-L-homoserine lactones and biofilm formation in Erwinia carotova, Yersinia enterocolitica, and Aeromonas hydrophila. J. Agric. Food Chem., 2009, 57, 11186-11193.
82. Alandejani, T; Marsan, J; Ferris, W; Slinger, R; Chan, F. Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngol. Head Neck Surg., 2009, 141, 114-118.
83. Okhiria, OA; Henriques, AFM; Burton, NF; Peters, A; Cooper, RA. Honey modulates biofilms of Pseudomonas aeruginosa in a time and dose dependent manner. J. Api. Prod. Api. Med. Sci,. 2009, 1, 6-10.
84. Badet, C; Quero, F. The in vitro effect of manuka honeys on growth and adherence of oral bacteria. Anaerobe, 2011, x, xx-xx.
85. Moritz, RFA; Southwick, EE (1992) Bees as a superorganisms - an evolutionary reality. Springer Verlag, Berlin: Heidelberg.
86. Qiu, PY; Ding, HB; Tang, YK; Xu, RJ. Determination of chemical composition of commercial honey by near-infrared spectroscopy. Food Chem., 1999, 47, 2760-2765.
87. Simuth, J; Bílikova, K; Kováčova, E; Kuzmova, Z; Schroder, W. Immunochemical approach to detection of adulteration in honey: physiologically active royal jelly protein stimulating TNF-alpha is a regular component of honey. J. Agric. Food Chem., 2004, 52, 2154-2158.
88. Lerrer, B; Zinger-Yosovich, KD; Avrahami, B; Gilboa-Garber, N. Honey and royal jelly, like human milk, abrogate lectin-dependent infection-preceding Pseudomonas aeruginosa adhesion. ISME J., 2007, 1, 149-155.
89. Pasparakis, G; Alexander, C. Sweet talking double hydrophilic block copolymer vesicles. Angew Chem., 2008, 47, 4847-4850.
90. Gilboa-Garber, N; Sudakevitz, D; Sheffi, M; Sela, R; Levene, C. PA-I and PA-II lectin interactions with the ABO(H) and P blood group glycosphingolipid antigens may contribute to the broad spectrum adherence of Pseudomonas aeruginosa to human tissues in secondary infections. Glycoconj. J., 1994, 11, 414-417.
91. Moothoo, DN; Naismith, JH. Concanavalin A distorts the beta-GlcNAc-(1--2)-Man linkage of betaGlcNAc-(1--2)-alpha-Man-(1--3)-[beta-GlcNAc-(1--2)-alpha-Man-(1--6)]-Man upon binding. Glycobiology, 1998, 8, 173-181.
92. Kamakura, M; Suenobu, N; Fukushima, M. Fifty-seven-kDa protein in royal jelly enhances proliferation of primary cultured rat hepatocytes and increases albumin production in the absence of serum. Biochem. Biophys. Res. Commun., 2001, 282, 865-874.
93. Matsui, T; Yukiyoshi, A; Doi, S; Sugimoto, H; Yamada, H; Matsumoto, K. Gastrointestinal enzyme production of bioactive peptides from royal jelly protein and their antihypertensive ability in SHR. J. Nutr. Biochem., 2002, 13, 80-86.
94. Fontana, R; Mendes, MA; de Souza Monson, B; Konno, K; César, LMM; Malaspina, O. Jelleines: a family of antimicrobial peptides from the royal jelly of honeybees (Apis mellifera). Peptides, 2004, 25, 919-928.
95. Truchado, P; Lopez-Galvez, F; Gil, MI; Tomas-Barberan, FA; Allende, A. Quorum sensing inhibitory and antimicrobial activities of honeys and the relationship with individual phenolics. Food Chem., 2009, 115, 1337-1344.
96. Silici, S; Sagdic, O; Ekici, L. Total phenolic content, antiradical, antioxidant and antimicrobial activities of Rhododendron honeys. Food Chem., 2010, 121, 238-243.
97. Alvarez-Suarez, JM; Tulipani, S; Diaz, D; Estevez, Y; Romandini, S; Giampieri, F; Damiani, E; Astolfi, P; Bompadre, S; Battino, M. Antioxidant and antimicrobial capacity of several monofloral Cuban honeys and their correlation with color, polyphenol content and other chemical. Food Chem. Toxicol., 2010, 48, 2490-2499.
98. Blanco, AR; Sudano-Roccaro, A; Spoto, GC; Nostro, A; Rusciano, D. Epigallocatechin galltae inhibits biofilm formation by ocular Staphylococcal isolates. Antimicrob. Agents Chemother., 2005, 49, 4339-4343.
99. Vikram, A; Jayaprakasha, GK; Jesudhasan, PR; Pillai, SD; Patil, BS. Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J. Appl. Microbiol., 2010, 109, 515-527.
100. Rasmussen, TB; Bjarnsholt, T; Skindersoe, ME; Hentzer, M; Kristoffersen, P; Kote, M; Nielsen, J; Eberl, L; Givskov, M. Screening for quorum-sensing inhibitors (QSI) by use a novel genetic system, the QSI selector. J. Bacteriol., 2005, 187, 1799-1814.
101. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 15th informational supplement. CLSI/NCCLS M100-S15 Wayne (PA): The Institute, 2005.
102. Clinical and Laboratory Standards Institute. Methods for dilution of antimicrobial susceptibility tests for bacteria that growth aerobically, 6th edn. Approved standard M7-A6. CLSI/NCCLS M7-A6 Wayne (PA): The Institute, 2003.
103. Zaki, I; Shall L; Dalziel, KL. Bacitracin: a significant sensitizer in leg ucler patients? Contact Dermatitis, 1994, 31, 92-94.
104. Darsow, U. The European Task Force on Atopic Dermatitis: Position paper on diagnosis and treatment of atopic dermatitis. J. Eur. Acad. Dermatol. Venereol., 2005, 19, 286-295.
105. Stewart, PS; Costerton, JW. Antibiotic resistance of bacteria in biofilm. Lancet, 2001, 358, 135-138.
106. Centres for Disease Control and Prevention. Staphylococcus aureus resistant to vancomycin-United States. Morb. Mortal. Weekly Rep., 2002, 51, 565-567.
107. Centres for Disease Control and Prevention. Public health dispatch: vancomycin-resistant Staphylococcus aureus - Pennsylvania. Morb. Mortal Weekly Rep., 2002, 51, 902.
108. Majtan, J; Majtanova, L; Bohova, J; Majtan, V. Honeydew honey as a potent antibacterial agent in eradication of multi-drug resistant Stenotrophomonas maltophilia isolates from cancer patients. Phytother. Res., 2010, in press
109. Tan, HT; Rahman, RA; Gan, SH; Halim, AS; Hassan, SA; Sulaiman, SA; Kirnpal-Kaur, B. The antibacterial properties of Malaysian tualang honey against wound and enteric microorganisms in comparison to manuka honey. BMC Complement Altern. Med., 2009, 9, 34.
110. Khoo, YT; Halim, AS; Singh, KK; Mohamad, NA. Wound contraction effects and antibacterial properties of tualang honey on full-thickness burn wounds in rats in comparsion to hydrofibre. BMC Complement Altern. Med., 2010, 10, 48.
111. Nasir, NAH, A S; Singh, KK; Dorai, AA; Haneef, MN. Antibacterial properties of tualang honey and its effect in burn wound management: a comparative study. BMC Complement Altern. Med., 2010, 10, 31.
112. Sherlock, O; Dolan, A; Athman, R; Power, A; Gethin, G; Cowman, S; Humphreys, H. Comparison of the natimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complement Altern. Med., 2010, 10:47, 1-5.
113. Smith, K; Perez, A; Ramage, G; Lappin, D; Gemmell, CG; Lang, S. Biofilm formation by Scottish clinical isolates of Staphylococcus aureus. J. Med. Microbiol., 2008, 57, 1018-1023.
114. O'Neill, E; Pozzi, C; Houston, P; Smyth, D; Humphreys, H; Robinson, DA; O'Gara, JP. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus from device-related infections. J. Clin. Microbiol., 2007, 45, 1379-1388.