Medical-grade honey enriched with antimicrobial peptides has enhanced activity against antibiotic-resistant pathogens

European Journal of Clinical Microbiology and Infectious Diseases

Volumn 30, Issue 2, 2011, Pages 251-257

  Kwakman, P H S ^a   De Boer, L ^a   Ruyter Spira, C P ^b   Creemers Molenaar, T ^c   Helsper, J P F G ^b   Vandenbroucke Grauls, C M J E ^a,d   Zaat, S A J ^a   Te Velde, A A ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c Bfactory Health Products   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERICIDAL PEPTIDE 2; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BURKHOLDERIA CEPACIA; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; HONEY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS EPIDERMIDIS;

ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIA; HONEY; HUMANS; MICROBIAL VIABILITY;

EID: 78751569697     PISSN: 09349723     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10096-010-1077-x     Document Type: Article

References (45)

1. Walsh C (2003) Antibiotics: actions, origins, resistance. American Society for Microbiology (ASM) Press, Washington
2. SB Levy B Marshall 2004 Antibacterial resistance worldwide: causes, challenges and responses Nat Med 10 S122 S129 1:CAS:528:DC%2BD2cXhtVeht7fF 10.1038/nm1145 15577930 (Pubitemid 40018235)
3. MA Fischbach CT Walsh 2009 Antibiotics for emerging pathogens Science 325 1089 1093 1:CAS:528:DC%2BD1MXhtVersrzK 10.1126/science.1176667 19713519
4. RA Cooper PC Molan KG Harding 2002 The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds J. Appl Microbiol 93 857 863 1:STN:280:DC%2BD38notFClsw%3D%3D 10.1046/j.1365-2672.2002. 01761.x 12392533 (Pubitemid 35340889)
5. SEE Efem 1988 Clinical observations on the wound healing properties of honey Br J Surg 75 679 681 1:STN:280:DyaL1czislaqsQ%3D%3D 10.1002/bjs.1800750718 3416123
6. D Bonn 2003 Sweet solution to superbug infections? Lancet Infect Dis 3 608 10.1016/S1473-3099(03)00794-1 14558506
7. B Dixon 2003 Bacteria can't resist honey Lancet Infect Dis 3 116 10.1016/S1473-3099(03)00524-3 12560201 (Pubitemid 36164209)
8. PE Lusby A Coombes JM Wilkinson 2002 Honey: a potent agent for wound healing? J Wound Ostomy Continence Nurs 29 295 300 1:STN:280: DC%2BD38nnvVOiuw%3D%3D 12439453
9. A Simon K Traynor K Santos G Blaser U Bode P Molan 2009 Medical honey for wound care-still the 'latest resort'? Evid Based Complement Alternat Med 6 165 173 10.1093/ecam/nem175 18955301
10. PC Molan 1992 The antibacterial activity of honey. 2. Variation in the potency of the antibacterial activity Bee World 73 59 76
11. KL Allen PC Molan GM Reid 1991 A survey of the antibacterial activity of some New Zealand honeys J Pharm Pharmacol 43 817 822 1:STN:280: DyaK383mtVeltA%3D%3D 1687577
12. CJ Adams CH Boult BJ Deadman JM Farr MN Grainger M Manley-Harris MJ Snow 2008 Isolation by HPLC and characterisation of the bioactive fraction of New Zealand manuka (Leptospermum scoparium) honey Carbohydr Res 343 651 659 1:CAS:528:DC%2BD1cXis1CgtLo%3D 10.1016/j.carres.2007.12.011 18194804
13. E Mavric S Wittmann G Barth T Henle 2008 Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand Mol Nutr Food Res 52 483 489 1:CAS:528:DC%2BD1cXltlensr0%3D 10.1002/mnfr.200700282 18210383
14. T Postmes AE van den Bogaard M Hazen 1995 The sterilization of honey with cobalt 60 gamma radiation: a study of honey spiked with spores of Clostridium botulinum and Bacillus subtilis Experientia 51 986 989 1:CAS:528: DyaK2MXovVyqt7w%3D 10.1007/BF01921753 7556583
15. PHS Kwakman JPC Van den Akker A Güçlü H Aslami JM Binnekade L de Boer L Boszhard F Paulus P Middelhoek AA te Velde CMJE Vandenbroucke-Grauls MJ Schultz SAJ Zaat 2008 Medical-grade honey kills antibiotic-resistant bacteria in vitro and eradicates skin colonization Clin Infect Dis 46 1677 1682 1:CAS:528:DC%2BD1cXnsVOhtLY%3D 10.1086/587892 18433338 (Pubitemid 351706764)
16. PHS Kwakman AA te Velde L de Boer D Speijer CMJE Vandenbroucke-Grauls SAJ Zaat 2010 How honey kills bacteria FASEB J 24 2576 2582 1:CAS:528: DC%2BC3cXptV2ku7Y%3D 10.1096/fj.09-150789 20228250
17. HW Huang 2000 Action of antimicrobial peptides: two-state model Biochemistry 39 8347 8352 1:CAS:528:DC%2BD3cXktlOrt7c%3D 10.1021/bi000946l 10913240 (Pubitemid 30489931)
18. Y Shai 2002 Mode of action of membrane active antimicrobial peptides Biopolymers 66 236 248 1:CAS:528:DC%2BD3sXitlOrsA%3D%3D 10.1002/bip.10260 12491537 (Pubitemid 36098316)
19. S Kobayashi K Takeshima CB Park SC Kim K Matsuzaki 2000 Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor Biochemistry 39 8648 8654 1:CAS:528: DC%2BD3cXktlOrt7s%3D 10.1021/bi0004549 10913273 (Pubitemid 30489964)
20. RM Epand HJ Vogel 1999 Diversity of antimicrobial peptides and their mechanisms of action Biochim Biophys Acta 1462 11 28 1:CAS:528: DyaK1MXnslymurg%3D 10.1016/S0005-2736(99)00198-4 10590300
21. K Matsuzaki 1999 Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes Biochim Biophys Acta 1462 1 10 1:CAS:528:DyaK1MXnslymuro%3D 10.1016/S0005-2736(99)00197-2 10590299
22. DA Devine RE Hancock 2002 Cationic peptides: distribution and mechanisms of resistance Curr Pharm Des 8 703 714 1:CAS:528:DC%2BD38XjtlWktr4%3D 10.2174/1381612023395501 11945166 (Pubitemid 34498560)
23. N Al Naiemi B Duim PH Savelkoul L Spanjaard E de Jonge A Bart CM Vandenbroucke-Grauls MD de Jong 2005 Widespread transfer of resistance genes between bacterial species in an intensive care unit: implications for hospital epidemiology J Clin Microbiol 43 4862 4864 1:CAS:528:DC%2BD2MXhtVOrtb7E 10.1128/JCM.43.9.4862-4864.2005 (Pubitemid 41298296)
24. JW White Jr MH Subers 1963 Studies on honey inhibine. 2. A chemical assay J Apic Res 2 93 100
25. J Dankert J van der Werff SAJ Zaat W Joldersma D Klein J Hess 1995 Involvement of bactericidal factors from thrombin-stimulated platelets in clearance of adherent viridans streptococci in experimental infective endocarditis Infect Immun 63 663 671 1:CAS:528:DyaK2MXjt1Kmurw%3D 7822036
26. O Sørensen K Arnljots JB Cowland DF Bainton N Borregaard 1997 The human antibacterial cathelicidin, hCAP-18, is synthesized in myelocytes and metamyelocytes and localized to specific granules in neutrophils Blood 90 2796 2803 9326247
27. M Frohm Nilsson B Sandstedt O Sørensen G Weber N Borregaard M Ståhle-Bäckdahl 1999 The human cationic antimicrobial protein (hCAP18), a peptide antibiotic, is widely expressed in human squamous epithelia and colocalizes with interleukin-6 Infect Immun 67 2561 2566 1:CAS:528:DyaK1MXivFWhsLo%3D 10225921
28. PHS Kwakman AA te Velde CMJE Vandenbroucke-Grauls SJH van Deventer SAJ Zaat 2006 Treatment and prevention of Staphylococcus epidermidis experimental biomaterial-associated infection by bactericidal peptide 2 Antimicrob Agents Chemother 50 3977 3983 1:CAS:528:DC%2BD28XhtlWksrrL 10.1128/AAC.00575-06 17000746 (Pubitemid 44865138)
29. LM Bang C Buntting P Molan 2003 The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing J Altern Complement Med 9 267 273 10.1089/10755530360623383 12804080
30. W Lineaweaver S Mcmorris D Soucy R Howard 1985 Cellular and bacterial toxicities of topical antimicrobials Plast Reconstr Surg 75 394 396 1:STN:280:DyaL2M7ktVGquw%3D%3D 10.1097/00006534-198503000-00016 3975287
31. JR Wilson JG Mills ID Prather SD Dimitrijevich 2005 A toxicity index of skin and wound cleansers used on in vitro fibroblasts and keratinocytes Adv Skin Wound Care 18 373 378 10.1097/00129334-200509000-00011 16160464
32. BE Watt AT Proudfoot JA Vale 2004 Hydrogen peroxide poisoning Toxicol Rev 23 51 57 1:CAS:528:DC%2BD2MXitFyksA%3D%3D 10.2165/00139709-200423010-00006 15298493 (Pubitemid 40484572)
33. S Fujiwara J Imai M Fujiwara T Yaeshima T Kawashima K Kobayashi 1990 A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin J Biol Chem 265 11333 11337 1:CAS:528:DyaK3cXkvFemsLo%3D 2358464
34. K Casteels-Josson W Zhang T Capaci P Casteels P Tempst 1994 Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures J Biol Chem 269 28569 28575 1:CAS:528:DyaK2cXmsVyqtrY%3D 7961803
35. MP Kalapos 2008 The tandem of free radicals and methylglyoxal Chem Biol Interact 171 251 271 1:CAS:528:DC%2BD1cXhsVSiurs%3D 10.1016/j.cbi.2007.11.009 18164697
36. M Brownlee 2001 Biochemistry and molecular cell biology of diabetic complications Nature 414 813 820 1:CAS:528:DC%2BD38Xhtlyltg%3D%3D 10.1038/414813a 11742414 (Pubitemid 34000785)
37. AW Stitt 2003 The role of advanced glycation in the pathogenesis of diabetic retinopathy Exp Mol Pathol 75 95 108 1:CAS:528:DC%2BD3sXlt1altLo%3D 10.1016/S0014-4800(03)00035-2 12834631 (Pubitemid 36798117)
38. M Zanetti R Gennaro D Romeo 1995 Cathelicidins: a novel protein family with a common proregion and a variable C-terminal antimicrobial domain FEBS Lett 374 1 5 1:CAS:528:DyaK2MXovVynsr0%3D 10.1016/0014-5793(95)01050-O 7589491
39. RI Lehrer T Ganz 2002 Cathelicidins: a family of endogenous antimicrobial peptides Curr Opin Hematol 9 18 22 10.1097/00062752-200201000-00004 11753073 (Pubitemid 34025307)
40. F Niyonsaba H Ogawa 2005 Protective roles of the skin against infection: Implication of naturally occurring human antimicrobial agents beta-defensins, cathelicidin LL-37 and lysozyme J Dermatol Sci 40 157 168 1:CAS:528: DC%2BD2MXht1Omsr%2FM 10.1016/j.jdermsci.2005.07.009 16150577 (Pubitemid 41728963)
41. K Pütsep G Carlsson HG Boman M Andersson 2002 Deficiency of antibacterial peptides in patients with morbus Kostmann: an observation study Lancet 360 1144 1149 10.1016/S0140-6736(02)11201-3 12387964 (Pubitemid 35246490)
42. JR Govan V Deretic 1996 Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia Microbiol Rev 60 539 574 1:STN:280:DyaK28vjvVemug%3D%3D 8840786
43. GM Clore E Appella M Yamada K Matsushima AM Gronenborn 1990 Three-dimensional structure of interleukin 8 in solution Biochemistry 29 1689 1696 1:CAS:528:DyaK3cXps1Klsw%3D%3D 10.1021/bi00459a004 2184886
44. J Turner Y Cho NN Dinh AJ Waring RI Lehrer 1998 Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils Antimicrob Agents Chemother 42 2206 2214 1:CAS:528:DyaK1cXmtVWqs78%3D 9736536
45. RA Cooper P Wigley NF Burton 2000 Susceptibility of multiresistant strains of Burkholderia cepacia to honey Lett Appl Microbiol 31 20 24 1:STN:280:DC%2BD3cvhslejtA%3D%3D 10.1046/j.1472-765x.2000.00756.x 10886608