Honey: a potential therapeutic agent for managing diabetic wounds

Fahmida Alam, Md Asiful Islam, Siew Hua Gan, Md Ibrahim Khalil, Fahmida Alam, Md Asiful Islam, Siew Hua Gan, Md Ibrahim Khalil

Abstract

Diabetic wounds are unlike typical wounds in that they are slower to heal, making treatment with conventional topical medications an uphill process. Among several different alternative therapies, honey is an effective choice because it provides comparatively rapid wound healing. Although honey has been used as an alternative medicine for wound healing since ancient times, the application of honey to diabetic wounds has only recently been revived. Because honey has some unique natural features as a wound healer, it works even more effectively on diabetic wounds than on normal wounds. In addition, honey is known as an "all in one" remedy for diabetic wound healing because it can combat many microorganisms that are involved in the wound process and because it possesses antioxidant activity and controls inflammation. In this review, the potential role of honey's antibacterial activity on diabetic wound-related microorganisms and honey's clinical effectiveness in treating diabetic wounds based on the most recent studies is described. Additionally, ways in which honey can be used as a safer, faster, and effective healing agent for diabetic wounds in comparison with other synthetic medications in terms of microbial resistance and treatment costs are also described to support its traditional claims.

References

    1. Bahrami M., Ataie-Jafari A., Hosseini S., Foruzanfar M. H., Rahmani M., Pajouhi M. Effects of natural honey consumption in diabetic patients: an 8-week randomized clinical trial. International Journal of Food Sciences and Nutrition. 2009;60(7):618–626. doi: 10.3109/09637480801990389.
    1. Wild S., Roglic G., Green A., Sicree R., King H. Global prevalence of diabetes estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(5):1047–1053. doi: 10.2337/diacare.27.5.1047.
    1. Maahs D. M., West N. A., Lawrence J. M., Mayer-Davis E. J. Epidemiology of type 1 diabetes. Endocrinology and Metabolism Clinics of North America. 2010;39(3):481–497. doi: 10.1016/j.ecl.2010.05.011.
    1. Cowie C. C., Rust K. F., Ford E. S., Eberhardt M. S., Byrd-Holt D. D., Li C., Williams D. E., Gregg E. W., Bainbridge K. E., Saydah S. H., Geiss L. S. Full accounting of diabetes and pre-diabetes in the U.S. population in 1988–1994 and 2005–2006. Diabetes Care. 2009;32(2):287–294. doi: 10.2337/dc08-1296.
    1. Gregg E. W., Cadwell B. L., Cheng Y. J., Cowie C. C., Williams D. E., Geiss L., Engelgau M. M., Vinicor F. Trends in the prevalence and ratio of diagnosed to undiagnosed diabetes according to obesity levels in the U.S. Diabetes Care. 2004;27(12):2806–2812. doi: 10.2337/diacare.27.12.2806.
    1. Yoon K.-H., Lee J.-H., Kim J.-W., Cho J. H., Choi Y.-H., Ko S.-H., Zimmet P., Son H.-Y. Epidemic obesity and type 2 diabetes in Asia. The Lancet. 2006;368(9548):1681–1688. doi: 10.1016/S0140-6736(06)69703-1.
    1. International Diabetes Federation World Diabetes Media Kit: every 10 seconds 1 person dies of diabetes. Brussels, Belgium, 2007, .
    1. Singh N., Armstrong D. G., Lipsky B. A. Preventing foot ulcers in patients with diabetes. The Journal of the American Medical Association. 2005;293(2):217–228. doi: 10.1001/jama.293.2.217.
    1. Lavery L. A., Higgins K. R., Lanctot D. R., Constantinides G. P., Zamorano R. G., Athanasiou K. A., Armstrong D. G., Agrawal C. M. Preventing diabetic foot ulcer recurrence in high-risk patients: use of temperature monitoring as a self-assessment tool. Diabetes Care. 2007;30(1):14–20. doi: 10.2337/dc06-1600.
    1. Pecoraro R. E., Reiber G. E., Burgess E. M. Pathways to diabetic limb amputation: basis for prevention. Diabetes Care. 1990;13(5):513–521. doi: 10.2337/diacare.13.5.513.
    1. Larsson J., Agardh C.-D., Apelqvist J., Stenström A. Long term prognosis after healed amputation in patients with diabetes. Clinical Orthopaedics and Related Research. 1998;(350):149–158.
    1. Aljadi A. M., Yusoff K. M. Isolation and identification of phenolic acids in Malaysian honey with antibacterial properties. Turkish Journal of Medical Sciences. 2003;33(4):229–236.
    1. Khanolkar M. P., Bain S. C., Stephens J. W. The diabetic foot. QJM. 2008;101(9):685–695. doi: 10.1093/qjmed/hcn027.
    1. Frykberg R. G., Veves A. Diabetic foot infections. Diabetes/Metabolism Reviews. 1996;12(3):255–270.
    1. Mayfield J. A., Reiber G. E., Sanders L. J., Janisse D., Pogach L. M. Preventive foot care in people with diabetes. Diabetes Care. 2003;26(1):S78–S79. doi: 10.2337/diacare.26.2007.S78.
    1. American Diabetes Association Consensus development conference on diabetic foot wound care: 7-8 April 1999, Boston, Massachusetts. American Diabetes Association. Diabetes Care. 1999;22(8):1354–1360. doi: 10.2337/diacare.22.8.1354.
    1. Armstrong D. G., Lipsky B. A. Diabetic foot infections: stepwise medical and surgical management. International Wound Journal. 2004;1(2):123–132. doi: 10.1111/j.1742-4801.2004.00035.x.
    1. Lavery L. A., Armstrong D. G., Wunderlich R. P., Mohler M. J., Wendel C. S., Lipsky B. A. Risk factors for foot infections in individuals with diabetes. Diabetes Care. 2006;29(6):1288–1293. doi: 10.2337/dc05-2425.
    1. Lipsky B. A., Berendt A. R., Deery H. G., Embil J. M., Joseph W. S., Karchmer A. W., LeFrock J. L., Lew D. P., Mader J. T., Norden C., Tan J. S. Diagnosis and treatment of diabetic foot infections. Clinical Infectious Diseases. 2004;39(7):885–910. doi: 10.1086/424846.
    1. Zgonis T., Stapleton J. J., Girard-Powell V. A., Hagino R. T. Surgical management of diabetic foot infections and amputations. AORN journal. 2008;87(5):935–950. doi: 10.1016/j.aorn.2008.02.014.
    1. Tentolouris N., Al-Sabbagh S., Walker M. G., Boulton A. J. M., Jude E. B. Mortality in diabetic and nondiabetic patients after amputations performed from 1990 to 1995: a 5-year follow-up study. Diabetes Care. 2004;27(7):1598–1604. doi: 10.2337/diacare.27.7.1598.
    1. Schofield C. J., Libby G., Brennan G. M., Macalpine R. R., Morris A. D., Leese G. P. Mortality and hospitalization in patients after amputation: a comparison between patients with and without diabetes. Diabetes Care. 2006;29(10):2252–2256. doi: 10.2337/dc06-0926.
    1. Boutoille D., Féraille A., Maulaz D., Krempf M. Quality of life with diabetes-associated foot complications: comparison between lower-limb amputation and chronic foot ulceration. Foot and Ankle International. 2008;29(11):1074–1078. doi: 10.3113/FAI.2008.1074.
    1. Reiber G. E., Lipsky B. A., Gibbons G. W. The burden of diabetic foot ulcers. The American Journal of Surgery. 1998;176(2):5–10. doi: 10.1016/S0002-9610(98)00181-0.
    1. Robbins J. M., Strauss G., Aron D., Long J., Kuba J., Kaplan Y. Mortality rates and diabetic foot ulcers: is it time to communicate mortality risk to patients with diabetic foot ulceration? Journal of the American Podiatric Medical Association. 2008;98(6):489–493. doi: 10.7547/0980489.
    1. Nguyen D., Orgill D., Murphy G. The Pathophysiologic Basis for Wound Healing and Cutaneous Regeneration. Elsevier; 2009.
    1. Majtan J. Methylglyoxal—a potential risk factor of manuka honey in healing of diabetic ulcers. Evidence-based Complementary and Alternative Medicine. 2011;2011 doi: 10.1093/ecam/neq013.295494
    1. Tambe S. M., Sampath L., Modak S. M. In vitro evaluation of the risk of developing bacterial resistance to antiseptics and antibiotics used in medical devices. Journal of Antimicrobial Chemotherapy. 2001;47(5):589–598. doi: 10.1093/jac/47.5.589.
    1. Appelgren P., Björnhagen V., Bragderyd K., Jonsson C. E., Ransjö U. A prospective study of infections in burn patients. Burns. 2002;28(1):39–46. doi: 10.1016/S0305-4179(01)00070-5.
    1. Abd-El Aal A., El-Hadidy M., El-Mashad N., El-Sebaie A. Antimicrobial effect of bee honey in comparison to antibiotics on organisms isolated from infected burns. Annals of Burns and Fire Disasters. 2007;20(2):83–88.
    1. Saraf R., Bowry V., Rao D., Saraf P., Molan P. The antimicrobial efficacy of Fijian honeys against clinical isolates from diabetic foot ulcers. Journal of ApiProduct and ApiMedical Science. 2009;1(3):64–71.
    1. Payne D. J., Gwynn M. N., Holmes D. J., Pompliano D. L. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nature Reviews Drug Discovery. 2007;6(1):29–40. doi: 10.1038/nrd2201.
    1. El-sound N. H. A. Honey between traditional uses and recent medicine. Macedonian Journal of Medical Sciences. 2012;5(2):205–214. doi: 10.3889/MJMS.1857-5773.2012.0213.
    1. Stephen-Haynes J., Gibson E., Greenwood M. Chitosan: a natural solution for wound healing. Journal of Community Nursing. 2014;28(1):48–53.
    1. Gethin G., Cowman S. Manuka honey vs. hydrogel—a prospective, open label, multicentre, randomised controlled trial to compare desloughing efficacy and healing outcomes in venous ulcers. Journal of Clinical Nursing. 2009;18(3):466–474. doi: 10.1111/j.1365-2702.2008.02558.x.
    1. Jull A., Walker N., Parag V., Molan P., Rodgers A. Randomized clinical trial of honey-impregnated dressings for venous leg ulcers. British Journal of Surgery. 2008;95(2):175–182. doi: 10.1002/bjs.6059.
    1. Sheckter C., van Vliet M. M., Krishnan N. M., Garner W. L. Cost-effectiveness comparison between topical silver sulfadiazine and enclosed silver dressing for partial-thickness burn treatment. Journal of Burn Care and Research. 2014;35(4):284–290. doi: 10.1097/BCR.0b013e3182a36916.
    1. Boekema B. K. H. L., Pool L., Ulrich M. M. W. The effect of a honey based gel and silver sulphadiazine on bacterial infections of in vitro burn wounds. Burns. 2013;39(4):754–759. doi: 10.1016/j.burns.2012.09.008.
    1. Oluwatosin O. M., Olabanji J. K., Oluwatosin O. A., Tijani L. A., Onyechi H. U. A comparison of topical honey and phenytoin in the treatment of chronic leg ulcers. African Journal of Medicine and Medical Sciences. 2000;29(1):31–34.
    1. Biglari B., Vd Linden P. H., Simon A., Aytac S., Gerner H. J., Moghaddam A. Use of Medihoney as a non-surgical therapy for chronic pressure ulcers in patients with spinal cord injury. Spinal Cord. 2012;50(2):165–169. doi: 10.1038/sc.2011.87.
    1. Güneş Ü. Y., Eşer I. Effectiveness of a honey dressing for healing pressure ulcers. Journal of Wound, Ostomy and Continence Nursing. 2007;34(2):184–190. doi: 10.1097/01.WON.0000264833.11108.35.
    1. Johnson D. W., Van Eps C., Mudge D. W., Wiggins K. J., Armstrong K., Hawley C. M., Campbell S. B., Isbel N. M., Nimmo G. R., Gibbs H. Randomized, controlled trial of topical exit-site application of honey (Medihoney) versus mupirocin for the prevention of catheter-associated infections in hemodialysis patients. Journal of the American Society of Nephrology. 2005;16(5):1456–1462. doi: 10.1681/ASN.2004110997.
    1. Bang L. M., Buntting C., Molan P. The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing. Journal of Alternative and Complementary Medicine. 2003;9(2):267–273. doi: 10.1089/10755530360623383.
    1. Subrahmanyam M., Sahapure A., Nagane N., Bhagwat V., Ganu J. Effects of topical application of honey on burn wound healing. Annals of Burns and fire Disasters. 2001;14:143–145.
    1. White R., Molan P. A Summary of Published Clinical Research on Honey in Wound Management. Aberdeen, UK: Wounds; 2005.
    1. Molan P. C. The evidence supporting the use of honey as a wound dressing. The International Journal of Lower Extremity Wounds. 2006;5(1):40–54. doi: 10.1177/1534734605286014.
    1. Ahmed A. K. J., Hoekstra M. J., Hage J. J., Karim R. B. Honey-medicated dressing: transformation of an ancient remedy into modern therapy. Annals of Plastic Surgery. 2003;50(2):143–148. doi: 10.1097/01.SAP.0000032306.44107.C1.
    1. Maeda Y., Loughrey A., Earle J. A. P., Millar B. C., Rao J. R., Kearns A., McConville O., Goldsmith C. E., Rooney P. J., Dooley J. S. G., Lowery C. J., Snelling W. J., McMahon A., McDowell D., Moore J. E. Antibacterial activity of honey against community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) Complementary Therapies in Clinical Practice. 2008;14(2):77–82. doi: 10.1016/j.ctcp.2007.11.004.
    1. Tandara A. A., Mustoe T. A. Oxygen in wound healing—more than a nutrient. World Journal of Surgery. 2004;28(3):294–300. doi: 10.1007/s00268-003-7400-2.
    1. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circulation Research. 2010;107(9):1058–1070. doi: 10.1161/CIRCRESAHA.110.223545.
    1. Huijberts M. S. P., Schaper N. C., Schalkwijk C. G. Advanced glycation end products and diabetic foot disease. Diabetes/Metabolism Research and Reviews. 2008;24(1):S19–S24. doi: 10.1002/dmrr.861.
    1. Sibbald R. G., Woo K. Y. The biology of chronic foot ulcers in persons with diabetes. Diabetes/Metabolism Research and Reviews. 2008;24(supplement 1):S25–S30. doi: 10.1002/dmrr.847.
    1. Tennvall G. R., Apelqvist J. Health-economic consequences of diabetic foot lesions. Clinical Infectious Diseases. 2004;39(supplement 2):S132–S139. doi: 10.1086/383275.
    1. Kanta J. The role of hydrogen peroxide and other reactive oxygen species in wound healing. Acta Medica. 2011;54(3):97–101.
    1. auf dem Keller U., Kümin A., Braun S., Werner S. Reactive oxygen species and their detoxification in healing skin wounds. Journal of Investigative Dermatology Symposium Proceedings. 2006;11(1):106–111.
    1. Islam A., Khalil I., Islam N., Moniruzzaman M., Mottalib A., Sulaiman S. A., Gan S. H. Physicochemical and antioxidant properties of Bangladeshi honeys stored for more than one year. BMC Complementary and Alternative Medicine. 2012;12, article 177 doi: 10.1186/1472-6882-12-177.
    1. Khalil M. I., Moniruzzaman M., Boukraâ L., Benhanifia M., Islam M. A., Islam M. N., Sulaiman S. A., Gan S. H. Physicochemical and antioxidant properties of algerian honey. Molecules. 2012;17(9):11199–11215. doi: 10.3390/molecules170911199.
    1. Al-Mamary M., Al-Meeri A., Al-Habori M. Antioxidant activities and total phenolics of different types of honey. Nutrition Research. 2002;22(9):1041–1047. doi: 10.1016/S0271-5317(02)00406-2.
    1. Khalil M. I., Alam N., Moniruzzaman M., Sulaiman S. A., Gan S. H. Phenolic acid composition and antioxidant properties of malaysian honeys. Journal of Food Science. 2011;76(6):C921–C928. doi: 10.1111/j.1750-3841.2011.02282.x.
    1. Cooper R. A., Molan P. C., Harding K. G. Antibacterial activity of honey against strains of Staphylococcus aureus from infected wounds. Journal of the Royal Society of Medicine. 1999;92(6):283–285.
    1. Al-Waili N. S. Investigating the antimicrobial activity of natural honey and its effects on the pathogenic bacterial infections of surgical wounds and conjunctiva. Journal of Medicinal Food. 2004;7(2):210–222. doi: 10.1089/1096620041224139.
    1. Estevinho L., Pereira A. P., Moreira L., Dias L. G., Pereira E. Antioxidant and antimicrobial effects of phenolic compounds extracts of Northeast Portugal honey. Food and Chemical Toxicology. 2008;46(12):3774–3779. doi: 10.1016/j.fct.2008.09.062.
    1. Mathews K. A., Binnington A. G. Wound management using honey. Compendium on Continuing Education for the Practicing Veterinarian. 2002;24(1):53–59.
    1. Bansal V., Medhi B., Pandhi P. Honey—a remedy rediscovered and its therapeutic utility. Kathmandu University Medical Journal. 2005;3(3):305–309.
    1. Phan T.-T., Wang L., See P., Grayer R. J., Chan S.-Y., Lee S. T. Phenolic compounds of Chromolaena adorata protect cultured skin cells from oxidative damage: implication for cutaneous wound healing. Biological and Pharmaceutical Bulletin. 2001;24(12):1373–1379. doi: 10.1248/bpb.24.1373.
    1. Molan P. C. Re-introducing honey in the management of wounds and ulcers-theory and practice. Ostomy/Wound management. 2002;48(11):28–40.
    1. Lusby P. E., Coombes A., Wilkinson J. M. Honey: a potent agent for wound healing? Journal of Wound Ostomy & Continence Nursing. 2002;29(6):295–300.
    1. Crane E. Honey. A Comprehensive Survey. Crane, Tex, USA: Russak; 1975.
    1. White J. W., Jr. Physical Characteristics of Honey. 1975.
    1. Al-Waili N. S., Saloom K. Y. Effects of topical honey on post-operative wound infections due to gram positive and gram negative bacteria following caesarean sections and hysterectomies. European Journal of Medical Research. 1999;4(3):126–130.
    1. Ryan G. B., Majno G. Acute inflammation. A review. The American Journal of Pathology. 1977;86(1):183–276.
    1. Cutting K. F. Honey and contemporary wound care: an overview. Ostomy Wound Management. 2007;53(11):49–54.
    1. Vijaya K. K., Nishteswar K. Wound healing activity of honey: a pilot study. AYU. 2012;33(3):374–377. doi: 10.4103/0974-8520.108827.
    1. Olaitan P. B., Adeleke O. E., Ola I. O. Honey: a reservoir for microorganisms and an inhibitory agent for microbes. African Health Sciences. 2007;7(3):159–165.
    1. Al-Waili N. S., Salom K., Al-Ghamdi A. A. Honey for wound healing, ulcers, and burns; data supporting its use in clinical practice. TheScientificWorldJournal. 2011;11:766–787. doi: 10.1100/tsw.2011.78.
    1. Ndayisaba G., Bazira L., Habonimana E., Muteganya D. Clinical and bacteriological outcome of wounds treated with honey. An analysis of a series of 40 cases. Revue de Chirurgie Orthopedique et Reparatrice de l'Appareil Moteur. 1993;79(2):111–113.
    1. Eddy J. J., Gideonsen M. D., Mack G. P. Practical considerations of using topical honey for neuropathic diabetic foot ulcers: a review. Wisconsin Medical Journal. 2008;107(4):187–190.
    1. Molan P. C. The role of honey in the management of wounds. Journal of wound care. 1999;8(8):415–418. doi: 10.12968/jowc.1999.8.8.25904.
    1. Archer H. G., Barnett S., Irving S., Middleton K. R., Seal D. V. A controlled model of moist wound healing: comparison between semi-permeable film, antiseptics and sugar paste. Journal of Experimental Pathology. 1990;71(2):155–170.
    1. Knutson R. A., Merbitz L. A., Creekmore M. A., Snipes H. G. Use of sugar and povidone-iodine to enhance wound healing: five years' experience. Southern Medical Journal. 1981;74(11):1329–1335. doi: 10.1097/00007611-198111000-00010.
    1. Somerfield S. D. Honey and healing. Journal of the Royal Society of Medicine. 1991;84(3):179.
    1. Green A. Wound healing properties of honey. British Journal of Surgery. 1988;75(12):1278. doi: 10.1002/bjs.1800751236.
    1. Condon R. E. Curious interaction of bugs and bees. Surgery. 1993;113(2):234–235.
    1. Seymour F. I., West K. S. Honey—its role in medicine. Medical Times. 1951;79(2):104–108.
    1. Molan P. C. The antibacterial activity of honey: 2. Variation in the potency of the antibacterial activity. Bee World. 1992;73(2):59–76.
    1. Schepartz A. I., Subers M. H. The glucose oxidase of honey I. Purification and some general properties of the enzyme. BBA—Enzymological Subjects. 1964;85(2):228–237.
    1. White J. W., Jr., Subers M. H., Schepartz A. I. The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochimica et Biophysica Acta. 1963;73(1):57–70. doi: 10.1016/0926-6569(63)90108-1.
    1. Molan P. C. The antibacterial activity of honey: 1. The nature of the antibacterial activity. Bee World. 1992;73(1):5–28.
    1. Pieper B. Honey-based dressings and wound care: an option for care in the United States. Journal of Wound, Ostomy and Continence Nursing. 2009;36(1):60–66. doi: 10.1097/01.WON.0000345177.58740.7d.
    1. Dunford C. The use of honey-derived dressings to promote effective wound management. Professional Nurse. 2005;20(8):35–38.
    1. Tur E., Bolton L., Constantine B. E. Topical hydrogen peroxide treatment of ischemic ulcers in the guinea pig: blood recruitment in multiple skin sites. Journal of the American Academy of Dermatology. 1995;33(2):217–221. doi: 10.1016/0190-9622(95)90238-4.
    1. Frankel S., Robinson G. E., Berenbaum M. R. Antioxidant capacity and correlated characteristics of 14 unifloral honeys. Journal of Apicultural Research. 1998;37(1):27–31.
    1. Yoo S. K., Huttenlocher A. Innate Immunity: Wounds Burst H2O2 Signals to Leukocytes. Current Biology. 2009;19(14):R553–R555. doi: 10.1016/j.cub.2009.06.025.
    1. Cho M., Hunt T. K., Hussain M. Z. Hydrogen peroxide stimulates macrophage vascular endothelial growth factor release. The American Journal of Physiology—Heart and Circulatory Physiology. 2001;280(5):H2357–H2363.
    1. Pruitt K. M., Tenovuo J. O. The Lactoperoxidase System. Chemistry and Biological Significance. New York, NY, USA: CRC Press; 1985.
    1. Brudzynski K. Effect of hydrogen peroxide on antibacterial activities of Canadian honeys. Canadian Journal of Microbiology. 2006;52(12):1228–1237. doi: 10.1139/W06-086.
    1. Brudzynski K., Abubaker K., St-Martin L., Castle A. Re-examining the role of hydrogen peroxide in bacteriostatic and bactericidal activities of honey. Frontiers in Microbiology. 2011;2, article 213 doi: 10.3389/fmicb.2011.00213.
    1. Childress B. B., Stechmiller J. K. Role of nitric oxide in wound healing. Biological research for nursing. 2002;4(1):5–15. doi: 10.1177/1099800402004001002.
    1. Moncada S., Palmer R. M. J., Higgs E. A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews. 1991;43(2):109–142.
    1. Schwentker A., Vodovotz Y., Weller R., Billiar T. R. Nitric oxide and wound repair: role of cytokines? Nitric Oxide—Biology and Chemistry. 2002;7(1):1–10. doi: 10.1016/S1089-8603(02)00002-2.
    1. Al-Waili N. S. Identification of nitric oxide metabolites in various honeys: effects of intravenous honey on plasma and urinary nitric oxide metabolites concentrations. Journal of Medicinal Food. 2003;6(4):359–364. doi: 10.1089/109662003772519921.
    1. Moore O. A., Smith L. A., Campbell F., Seers K., McQuay H. J., Moore R. A. Systematic review of the use of honey as a wound dressing. BMC Complementary and Alternative Medicine. 2001;1:2–10. doi: 10.1186/1472-6882-1-2.
    1. Al-Waili N., Saleeb N. Honey increased nitric oxide end product in saliva of healthy volunteer. FASEB Conference; April 2003; San Diego, Calif, USA. Abstract 236.
    1. Al-Waili N. S., Boni N. S. Honey increased saliva, plasma, and urine content of total nitrite concentrations in normal individuals. Journal of Medicinal Food. 2004;7(3):377–380. doi: 10.1089/jmf.2004.7.377.
    1. White R. The benefits of honey in wound management. Nursing Standard. 2005;20(10):57–66.
    1. Peppin G. J., Weiss S. J. Activation of the endogenous metalloproteinase, gelatinase, by triggered human neutrophils. Proceedings of the National Academy of Sciences of the United States of America. 1986;83(12):4322–4326. doi: 10.1073/pnas.83.12.4322.
    1. Ashcroft G. S., Lei K., Jin W., Longenecker G., Kulkarni A. B., Greenwell-Wild T., Hale-Donze H., McGrady G., Song X.-Y., Wahl S. M. Secretory leukocyte protease inhibitor mediates non-redundant functions necessary for normal wound healing. Nature Medicine. 2000;6(10):1147–1153. doi: 10.1038/80489.
    1. Phuapradit W., Saropala N. Topical application of honey in treatment of abdominal wound disruption. Australian and New Zealand Journal of Obstetrics and Gynaecology. 1992;32(4):381–384. doi: 10.1111/j.1479-828X.1992.tb02861.x.
    1. Topham J. Why do some cavity wounds treated with honey or sugar paste heal without scarring? Journal of wound care. 2002;11(2):53–55. doi: 10.12968/jowc.2002.11.2.26372.
    1. Viljanto J., Raekallio J. Local hyperalimentation of open wounds. British Journal of Surgery. 1976;63(6):427–430. doi: 10.1002/bjs.1800630603.
    1. Chant A. The biomechanics of leg ulceration. Annals of the Royal College of Surgeons of England. 1999;81(2):80–85.
    1. Pieper B. Honey-based dressings and wound care. Journal of Wound, Ostomy and Continence Nursing. 2009;36(6, article 589) doi: 10.1097/01.WON.0000364940.46532.9b.
    1. Halliwell B. Oxygen radicals, nitric oxide and human inflammatory joint disease. Annals of the Rheumatic Diseases. 1995;54(6):505–510. doi: 10.1136/ard.54.6.505.
    1. Flohé L., Beckmann R., Giertz H., Loschen G. Oxygen-Centred Free Radicals as Mediators of Inflammation. London, UK: Academic Press; 1985.
    1. Tonks A. J., Cooper R. A., Jones K. P., Blair S., Parton J., Tonks A. Honey stimulates inflammatory cytokine production from monocytes. Cytokine. 2003;21(5):242–247. doi: 10.1016/S1043-4666(03)00092-9.
    1. Takeuchi M., Fukuda M., Kobayashi K., Hirono Y., Miyagawa M., Ishida T., Ejiogu E. C., Sawai M., Pinkerton K. E. Jungle honey enhances immune function and antitumor activity. Evidence-Based Complementary and Alternative Medicine. 2011;2011 doi: 10.1093/ecam/nen086.908743
    1. Islam M. N., Khalil M. I., Islam M. A., Gan S. H. Toxic compounds in honey. Journal of Applied Toxicology. 2014;34(7):733–742. doi: 10.1002/jat.2952.
    1. Efem S. Clinical observations on the wound healing properties of honey. British Journal of Surgery. 1988;75(7):679–681. doi: 10.1002/bjs.1800750718.
    1. du Toit D. F., Page B. J. An in vitro evaluation of the cell toxicity of honey and silver dressings. Journal of wound care. 2009;18(9):383–389. doi: 10.12968/jowc.2009.18.9.44307.
    1. Jull A. B., Rodgers A., Walker N. Honey as a topical treatment for wounds. Cochrane Database of Systematic Reviews. 2008;(4) doi: 10.1002/14651858.CD005083.pub2.CD005083
    1. Gethin G., Cowman S. Case series of use of Manuka honey in leg ulceration. International Wound Journal. 2005;2(1):10–15. doi: 10.1111/j.1742-4801.2005.00078.x.
    1. Majno G. The Healing Hand: Man and Wound in the Ancient World. Harvard University Press; 1991.
    1. Stewart J. A., McGrane O. L., Wedmore I. S. Wound care in the wilderness: is there evidence for honey? Wilderness and Environmental Medicine. 2014;25(1):103–110. doi: 10.1016/j.wem.2013.08.006.
    1. Dunford C. E., Hanano R. Acceptability to patients of a honey dressing for non-healing venous leg ulcers. Journal of Wound Care. 2004;13(5):193–197. doi: 10.12968/jowc.2004.13.5.26614.
    1. Kamaratos A. V., Tzirogiannis K. N., Iraklianou S. A., Panoutsopoulos G. I., Kanellos I. E., Melidonis A. I. Manuka honey-impregnated dressings in the treatment of neuropathic diabetic foot ulcers. International Wound Journal. 2014;11(3):259–263. doi: 10.1111/j.1742-481X.2012.01082.x.
    1. Shukrimi A., Sulaiman A. R., Halim A. Y., Azril A. A comparative study between honey and povidone iodine as dressing solution for Wagner type II diabetic foot ulcers. Medical Journal of Malaysia. 2008;63(1):44–46.
    1. Hammouri S. K. The role of honey in the management of diabetic foot ulcers. Journal of Research in Medical Sciences. 2004;11(2):20–22.
    1. Chernev I., Liguori P. A., Senno S. L., Peters K. L., Bowers J. M. Combined noncontact, lowo-frequency ultrasound and medical honey for the treatment of chronic wounds: a case series. Journal of Wound, Ostomy and Continence Nursing. 2010;37(4):421–425. doi: 10.1097/WON.0b013e3181e39edf.
    1. Alzahrani H. A., Bakhotmah B. A., Boukraâ L. In Vitro susceptibility of diabetic wound bacteria to mixtures of honey, Commiphora molmol and Nigella sativa. Open Nutraceuticals Journal. 2011;4:172–175. doi: 10.2174/1876396001104010172.
    1. Al Saeed M. Therapeutic efficacy of conventional treatment combined with Manuka honey in the treatment of patients with diabetic foot ulcers: a randomized controlled study. Egyptian Journal of Hospital Medicine. 2013;53:1064–1071.
    1. Lotfy M., Badra G., Burham W., Alenzi F. Q. Combined use of honey, bee propolis and myrrh in healing a deep, infected wound in a patient with diabetes mellitus. British Journal of Biomedical Science. 2006;63(4):171–173.
    1. Majno G. The Healing Hand: Man and Wound in the Ancient World. Cambridge, Mass, USA: Harvard University Press; 1975.
    1. Nawfar S. A., Han C. S., Paiman M., Iskandar M. A randomized control trial comparing the effects of manuka honey and tualang honey on wound granulation of post debridement diabetic foot wounds. Journal of ApiProduct & ApiMedical Science. 2011;3(1):18–25.
    1. Freeman A., May K., Wraight P. Honey: the bees' knees for diabetic foot ulcers? Wound Practice & Research. 2010;18(3):144.
    1. Nurul Syazana M. S., Gan S. H., Halim A. S., Shah N. S. M., Sukari H. A. Analysis of volatile compounds of Malaysian Tualang (Koompassia excelsa) honey using gas chromatography mass spectrometry. African Journal of Traditional, Complementary and Alternative Medicines. 2013;10(2):180–188.
    1. van der Weyden E. A. The use of honey for the treatment of two patients with pressure ulcers. British Journal of Community Nursing. 2003;8(12):S14–S20.
    1. Molan P. C. Potential of honey in the treatment of wounds and burns. The American Journal of Clinical Dermatology. 2001;2(1):13–19. doi: 10.2165/00128071-200102010-00003.
    1. Molan P. C., Betts J. A. Clinical usage of honey as a wound dressing: an update. Journal of Wound Care. 2004;13(9):353–356. doi: 10.12968/jowc.2004.13.9.26708.
    1. Mohamed H., Salma M. A., Al Lenjawi B., et al. Enhancing primary healing post ray amputation in a diabetic patient: efficacy of natural honey. Journal of Diabetic Foot Complications. 2014;6(1):13–18.
    1. Mohamed H., Abu Salma M., Allenjawi B., et al. Natural honey as an adjunctive alternative in the management of diabetic foot ulcers. Wound Practice & Research. 2012;20(4):212.
    1. Candeias N., Cardoso M. Management of diabetic foot ulceration with honey. Wounds UK. 2011;7(3):84–86.
    1. Moghazy A. M., Shams M. E., Adly O. A., Abbas A. H., El-Badawy M. A., Elsakka D. M., Hassan S. A., Abdelmohsen W. S., Ali O. S., Mohamed B. A. The clinical and cost effectiveness of bee honey dressing in the treatment of diabetic foot ulcers. Diabetes Research and Clinical Practice. 2010;89(3):276–281. doi: 10.1016/j.diabres.2010.05.021.
    1. Makhdoom A., Khan M. S., Lagahari M. A., Rahopoto M. Q., Tahir S. M., Siddiqui K. A. Management of diabetic foot by natural honey. Journal of Ayub Medical College, Abbottabad. 2009;21(1):103–105.
    1. Eddy J. J., Gideonsen M. D. Topical honey for diabetic foot ulcers. The Journal of Family Practice. 2005;54(6):533–535.
    1. Xu L., McLennan S. V., Lo L., Natfaji A., Bolton T., Liu Y., Twigg S. M., Yue D. K. Bacterial load predicts healing rate in neuropathic diabetic foot ulcers. Diabetes Care. 2007;30(2):378–380. doi: 10.2337/dc06-1383.
    1. Bader M. S. Diabetic foot infection. The American Family Physician. 2008;78(1):71–82.
    1. Louie T. J., Bartlett J. G., Tally F. P., Gorbach S. L. Aerobic and anaerobic bacteria in diabetic foot ulcers. Annals of Internal Medicine. 1976;85(4):461–463. doi: 10.7326/0003-4819-85-4-461.
    1. Bowler P. G., Duerden B. I., Armstrong D. G. Wound microbiology and associated approaches to wound management. Clinical Microbiology Reviews. 2001;14(2):244–269. doi: 10.1128/CMR.14.2.244-269.2001.
    1. Bansal E., Garg A., Bhatia S., Attri A., Chander J. Spectrum of microbial flora in diabetic foot ulcers. Indian Journal of Pathology and Microbiology. 2008;51(2):204–208. doi: 10.4103/0377-4929.41685.
    1. Chincholikar D. A., Pal R. B. Study of fungal and bacterial infections of the diabetic foot. Indian Journal of Pathology and Microbiology. 2002;45(1):15–22.
    1. Caputo G. M., Cavanagh P. R., Ulbrecht J. S., Gibbons G. W., Karchmer A. W. Assessment and management of foot disease in patients with diabetes. The New England Journal of Medicine. 1994;331(13):854–860. doi: 10.1056/NEJM199409293311307.
    1. Lipsky B. A., Pecoraro R. E., Larson S. A., Hanley M. E., Ahroni J. H. Outpatient management of uncomplicated lower-extremity infections in diabetic patients. Archives of Internal Medicine. 1990;150(4):790–797. doi: 10.1001/archinte.150.4.790.
    1. El-Tahawy A. T. Bacteriology of diabetic foot infections. Saudi Medical Journal. 2000;21(4):344–347.
    1. Efem S. E. E., Udoh K. T., Iwara C. I. The antimicrobial spectrum of honey and its clinical significance. Infection. 1992;20(4):227–229. doi: 10.1007/BF02033065.
    1. Al-Waili N. S., Akmal M., Al-Waili F. S., Saloom K. Y., Ali A. The antimicrobial potential of honey from United Arab Emirates on some microbial isolates. Medical Science Monitor. 2005;11(12):BR433–BR438.
    1. Nzeako B., Hamdi J. Antimicrobial potential of honey on some microbial isolates. Medical Sciences. 2000;2(2):75–79.
    1. Taormina P. J., Niemira B. A., Beuchat L. R. Inhibitory activity of honey against foodborne pathogens as influenced by the presence of hydrogen peroxide and level of antioxidant power. International Journal of Food Microbiology. 2001;69(3):217–225. doi: 10.1016/S0168-1605(01)00505-0.
    1. Sherlock O., Dolan A., Athman R., Power A., Gethin G., Cowman S., Humphreys H. Comparison of the antimicrobial activity of Ulmo honey from Chile and Manuka honey against methicillin-resistant Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa. BMC Complementary and Alternative Medicine. 2010;10, article 47 doi: 10.1186/1472-6882-10-47.
    1. George N. M., Cutting K. F. Antibacterial honey (Medihoney): in-vitro activity against clinical isolates of MRSA, VRE, and other multiresistant gram-negative organisms including Pseudomonas aeruginosa. Wounds. 2007;19(9):231.
    1. Chauhan A., Pandey V., Chacko K., Khandal R. Antibacterial activity of raw and processed honey. Electronic Journal of Biology. 2010;6(3):58–66.
    1. Hegazi A. G. Antimicrobial activity of different Egyptian honeys as comparison of Saudi Arabia honey. Research Journal of Microbiology. 2011;6(5):488–495. doi: 10.3923/jm.2011.488.495.
    1. Ramani A., Ramani R., Shivananda R., Shivananda P. G., Kundaje G. N. Bacteriology of diabetic foot ulcers. Indian Journal of Pathology and Microbiology. 1991;34(2):81–87.
    1. Sevgi K., Rezzan A., Esra U., Sengül K. Antioxidant and antimicrobial activities of selected Turkish honeys. Hacettepe Journal of Biology and Chemistry. 2008;36(2):163–172.
    1. Mulu A., Tessema B., Derbie F. In vitro assessment of the antimicrobial potential of honey on common human pathogens. Ethiopian Journal of Health Development. 2004;18(2):107–111.
    1. Mullai V., Menon T. Bactericidal activity of different types of honey against clinical and environmental isolates of Pseudomonas aeruginosa. Journal of Alternative and Complementary Medicine. 2007;13(4):439–442. doi: 10.1089/acm.2007.6366.
    1. Santos F. A., Bastos E. M. A., Rodrigues P. H., De Uzeda M., De Carvalho M. A. R., De Macedo Farias L., Andrade Moreira E. S. Susceptibility of Prevotella intermedia/Prevotella nigrescens (and Porphyromonas gingivalis) to propolis (bee glue) and other antimicrobial agents. Anaerobe. 2002;8(1):9–15. doi: 10.1006/anae.2002.0411.
    1. Eick S., Schäfer G., Kwieciński J., Atrott J., Henle T., Pfister W. Honey—a potential agent against Porphyromonas gingivalis: an in vitro study. BMC Oral Health. 2014;14(1, article 24) doi: 10.1186/1472-6831-14-24.
    1. Khosravi A. R., Shokri H., Katiraee F., Ziglari T., Forsi M. Fungicidal potential of different Iranian honeys against some pathogenic Candida species. Journal of Apicultural Research. 2008;47(4):256–260. doi: 10.3896/IBRA.1.47.4.04.
    1. Lansdown A. B. Silver. 2: toxicity in mammals and how its products aid wound repair. Journal of Wound Care. 2002;11(5):173–177. doi: 10.12968/jowc.2002.11.5.26398.
    1. Smoot E. C., III, Kucan J. O., Roth A., Mody N., Debs N. In vitro toxicity testing for antibacterials against human keratinocytes. Plastic and Reconstructive Surgery. 1991;87(5):917–924. doi: 10.1097/00006534-199105000-00017.
    1. Moyer C. A., Brentano D. L., Gravens D. L., Margraf H. W., Monafo W. W., Jr. Treatment of large human burns with 0.5% silver nitrate solution. Archives of Surgery. 1965;90(6):812–867. doi: 10.1001/archsurg.1965.01320120014002.
    1. Boateng J. S., Matthews K. H., Stevens H. N. E., Eccleston G. M. Wound healing dressings and drug delivery systems: a review. Journal of Pharmaceutical Sciences. 2008;97(8):2892–2923. doi: 10.1002/jps.21210.
    1. Iwamoto Y., Ferguson L. R., Pearson A., Baguley B. C. Photo-enhancement of the mutagenicity of 9-anilinoacridine derivatives related to the antitumour agent amsacrine. Mutation Research: Fundamental and Molecular Mechanisms of Mutagenesis. 1992;268(1):35–41. doi: 10.1016/0027-5107(92)90080-L.
    1. Dela Cruz F., Brown D. H., Leikin J. B., Franklin C., Hryhorczuk D. O. Iodine absorption after topical administration. Western Journal of Medicine. 1987;146(1):43–45.
    1. Drosou A., Falabella A., Kirsner R. S. Antiseptics on wounds: an area of controversy. Wounds. 2003;15(5):149–166.
    1. Hansbrough J. F., Zapata-Sirvent R. L., Cooper M. L. Effects of topical antimicrobial agents on the human neutrophil respiratory burst. Archives of Surgery. 1991;126(5):603–608. doi: 10.1001/archsurg.1991.01410290079016.
    1. Monafo W. W., West M. A. Current treatment recommendations for topical burn therapy. Drugs. 1990;40(3):364–373. doi: 10.2165/00003495-199040030-00004.
    1. Ward R. S., Saffle J. R. Topical agents in burn and wound care. Physical Therapy. 1995;75(6):526–538.
    1. Steen M. Review of the use of povidone-iodine (PVP-I) in the treatment of burns. Postgraduate Medical Journal. 1993;69(3):S84–S92.
    1. Sleigh J. W., Linter S. P. K. Hazards of hydrogen peroxide. The British Medical Journal. 1985;291(6510):1706. doi: 10.1136/bmj.291.6510.1706.
    1. Brown C. D., Zitelli J. A. A review of topical agents for wounds and methods of wounding: guidelines for wound management. Journal of Dermatologic Surgery and Oncology. 1993;19(8):732–737. doi: 10.1111/j.1524-4725.1993.tb00417.x.
    1. Shelanski H. A., Shelanski M. V. PVP-iodine: history, toxicity and therapeutic uses. The Journal of the International College of Surgeons. 1956;25(6):727–734.
    1. Tatnall F. M., Leigh I. M., Gibson J. R. Comparative study of antiseptic toxicity on basal keratinocytes, transformed human keratinocytes and fibroblasts. Skin Pharmacology. 1990;3(3):157–163. doi: 10.1159/000210865.
    1. Jacobs M. R., Zanowiak P. Handbook of Nonprescriptive Drugs. 9th. Washington, D.C., USA: American Pharmaceutical Association; 1990.
    1. Marks J. G., Jr. Allergic contact dermatitis to povidone-iodine. Journal of the American Academy of Dermatology. 1982;6(4):473–475. doi: 10.1016/S0190-9622(82)80363-0.
    1. Cookson B. D., Bolton M. C., Platt J. H. Chlorhexidine resistance in methicillin-resistant Staphylococcus aureus or just an elevated MIC? An in vitro and in vivo assessment. Antimicrobial Agents and Chemotherapy. 1991;35(10):1997–2002. doi: 10.1128/AAC.35.10.1997.
    1. Greener Y., McCartney M., Jordan L. Assessment of the systemic effects, primary dermal irritation, and ocular irritation of chlorhexidine acetate solutions. Journal of the American College of Toxicology. 1985;4(6):309–319.
    1. Lineaweaver W., McMorris S., Soucy D., Howard R. Cellular and bacterial toxicities of topical antimicrobials. Plastic and Reconstructive Surgery. 1985;75(3):394–396. doi: 10.1097/00006534-198503000-00016.
    1. Cooper M. L., Boyce S. T., Hansbrough J. F., Foreman T. J., Frank D. H. Cytotoxicity to cultured human keratinocytes of topical antimicrobial agents. Journal of Surgical Research. 1990;48(3):190–195. doi: 10.1016/0022-4804(90)90212-K.
    1. Gallico G. G., O'Connor N. E., Compton C. C., Remensnyder J. P., Kehinde O., Green H. Cultured epithelial autografts for giant congenital nevi. Plastic and Reconstructive Surgery. 1989;84(1):1–9. doi: 10.1097/00006534-198907000-00001.
    1. Hudspith J., Rayatt S. ABC of burns: first aid and treatment of minor burns. The British Medical Journal. 2004;328(7454):1487–1489. doi: 10.1136/bmj.328.7454.1487.
    1. Montvale N. J. Physicians' Desk Reference. 49th. Medical Economics Data Production Co; 1995.
    1. Gilman A. G., Goodman L. S., Rall T. W., Murad F. The Pharmacological Basis of Therapeutics. New York, NY, USA: Macmillan; 1985.
    1. Moncrief J. A., Haynes B. W., Jr., Fox C. L. Topical therapy for control of bacteria in the burn wound. World Journal of Surgery. 1978;2(2):151–165. doi: 10.1007/BF01553539.
    1. Harrison H. N., Shuck J. M., Caldwell E. Studies of the pain produced by mafenide acetate preparations in burns. Archives of Surgery. 1975;110(12):1446–1449. doi: 10.1001/archsurg.1975.01360180016003.
    1. Gette M. T., Marks J. G., Jr., Maloney M. E. Frequency of postoperative allergic contact dermatitis to topical antibiotics. Archives of Dermatology. 1992;128(3):365–367. doi: 10.1001/archderm.128.3.365.

Source: PubMed

3
Iratkozz fel