Abstract
In recent years, due to the growing phenomenon of antimicrobial resistance, the search for alternative strategies to antibiotic treatments was increased and a considerable interest for the use of medical honey in clinical practice has emerged. Honey was used for the treatment of skin lesions, both in humans and in animals. However, knowledge concerning the use of medical honey in non-traditional companion animals is scarce. The aim of this study was to assess the antibacterial activity of a standardized medical honey (Revamil, BFactory) against bacterial strains isolated from skin lesions of non-traditional companion animals. The minimum bactericidal concentration (MBC) of Revamil honey against seventeen clinical isolates and three reference strains was established. The medical honey showed antimicrobial activity against both Gram-positive and Gram-negative bacteria. Growth was inhibited for all the strains at concentrations of medical honey ranging from 10 to 40%. Pseudomonas oryzihabitans and Alcaligenes faecalis showed the lowest MBC (10%). The reference strains Staphylococcus aureus ATCC25923 and Escherichia coli ATCC25922 showed a higher sensitivity to honey compare to the corresponding clinical isolates. The observed results suggest that Revamil could represent an effective therapeutic aid in case of pathological skin infections in non-traditional companion animals.
References
Ahmed A., Hoekstra M.J., Hage J.J. & Karim R.B. 2003. Honey-Medicated Dressing: Transformation of an Ancient Remedy Into Modern Therapy. Ann Plas Surg, 50(2), 143–48. https://doi.org/10.1097/01.SAP.0000032306.44107.C1.
Almasaudi S.B., Al-Nahari A.A.M, Abd El-Ghany E.S.M., Barbour E., Al Muhayawi S.M., Al-Jaouni S., Azhar E., Qari M., Qari Y.A. & Harakeh S. 2017. Antimicrobial Effect of Different Types of Honey on Staphylococcus Aureus. Saudi J Biol Sci, 24(6), 1255–1261. https://doi.org/10.1016/j.sjbs.2016.08.007.
Al-Waili N.S. 2004. Natural Honey Lowers Plasma Glucose, C-Reactive Protein, Homocysteine, and Blood Lipids in Healthy, Diabetic, and Hyperlipidemic Subjects: Comparison with Dextrose and Sucrose. J Med Food, 7, 100–107. https://doi.org/10.1089/109662004322984789.
Bardy J., Slevin N.J., Mais, K.L. & Molassiotis A. 2008. A systematic review of honey uses and its potential value within oncology care. J Clin Nurs, 17, 2604-2623. doi:10.1111/j.1365-2702.2008.02304.x
Basualdo C., Sgroy V.S., Finola M.S. & Marioli J.M. 2007. Comparison of the Antibacterial Activity of Honey from Different Provenance Against Bacteria Usually Isolated from Skin Wound. Vet Microbiol, 124, 375-381.
Bertocchi M., Pelizzone I., Parmigiani E., Ponzio P., Macchi E., Righi F., Di Girolamo N., Bigliardi E., Denti L., Bresciani C. & Di ianni F. 2018. Monitoring the reproductive activity in captive bred female ball pythons (P. regius) by ultrasound evaluation and noninvasive analysis of faecal reproductive hormone (progesterone and 17β-estradiol) metabolites trends. PLoS ONE, 13 (6), e0199377. DOI:10.1371/journal.pone.0199377
Biswal B.M., Zakaria A. & Ahmad N.M. 2003. Topical Application of Honey in the Management of Radiation Mucositis: A Preliminary Study. Support Care Cancer, 11(4), 242–248. https://doi.org/10.1007/s00520-003-0443-y.
Bowler P.G., Duerden B.I. & Armstrong D.G. 2001. Wound Microbiology and Associated Approaches to Wound Management. Clin Microbiol Rev, 14(2), 244-269.
Carnwath R., Graham E.M., Reynolds K. & Pollock P.J. 2014. The antimicrobial activity of honey against common equine wound bacterial isolates. Vet J, 199, 110-114. https://doi.org/10.1016/j.tvjl.2013.07.003.
Cavanagh D., Beazley J. & Ostapowicz F. 1971. Radical operation for carcinoma of the vulva. A new approach to wound healing. Obstet Gynecol Surv, 26(6), 460–461. https://doi.org/10.1097/00006254-197106000-00018.
Cooper R.A., Molan P.C. & Harding K.G. 1999. Antibacterial Activity of Honey against Strains of Staphylococcus Aureus from Infected Wounds. J Royal Soc Med, 92(6), 283–285.
Cooper R.A., Molan P.C. & Harding K.G. 2002. The Sensitivity to Honey of Gram-Positive Cocci of Clinical Significance Isolated from Wounds. J Appl Microbiol, 93(5), 857–863.
Di Ianni F., Dodi P.L., Cabassi C.S., Pelizzone I., Sala A., Cavirani S., Parmigiani E., Quintavalla F. & Taddei S. 2015a. Conjunctival flora of clinically normal and diseased turtles and tortoises. BMC Vet Res, 11, 91 DOI: 10.1186/s12917-015-0405-x
Di Ianni F., Merli E., Burtini F., Conti V., Pelizzone I., Di Lecce R., Parmigiani E., Squassino G.P., Del Bue M., Lucarelli E., Ramoni R. & Grolli S. 2015b. Preparation and application of an innovative thrombocyte/leukocyte-enriched plasma to promote tissue repair in chelonians. PLoS ONE, 10 (4), e0122595 DOI: 10.1371/journal.pone.0122595
Di Ianni F., Parmigiani E., Pelizzone I., Bresciani C., Gnudi G., Volta A., Manfredi S. & Bigliardi E. 2014. Comparison between intramuscular and intravenous administration of oxytocin in captive-bred red-eared sliders (Trachemys scripta elegans) with nonobstructive egg retention. J Exot Pet Med, 23 (1), 79-84. DOI:10.1053/j.jepm.2013.11.009
Dunford C.E. & Hanano R. 2004. Acceptability to Patients of a Honey Dressing for Non-Healing Venous Leg Ulcers. J Wound Care, 13(5), 193–197. https://doi.org/10.12968/jowc.2004.13.5.26614.
Efem S.E.1988. Clinical Observations on the Wound Healing Properties of Honey. Br J Surg, 75(7), 679–681.
Guo S. & Di Pietro L.A. 2010. Factors affecting wound healing. J Dent Res, 89(3), 219-229. DOI: 10.1177/0022034509359125
Gupta S.K., Singh H., Varshney A.C. Prakash P. & Singh S.P. 1993. Biochemical alterations during wound healing under the influence of natural honey and ampicillin in buffaloes. Indian Vet J, 70, 45–47.
Harkewicz K.A. 2001. Dermatology of reptiles: a clinical approach to diagnosis and treatment. In The Veterinary Clinics of North America: exotic animal practice. (R.E. Schmidt, Ed.) WB Saunders, Philadelphia, 441–461.
Jeddar A., Kharsany A., Ramsaroop U.G., Bhamjee A., Haffejee I.E. & Moosa A. 1985. The antibacterial action of honey. An in vitro study. S Afr Med J, 67, 257–258.
Kwakman P.H., Van den Akker J.P., Güçlü A., Aslami H., Binnekade J.M., de Boer L., Boszhard L., Paulus F., Middelhoek P., te Velde A.A., Vandenbroucke-Grauls C.M., Schultz M.J. & Zaat S.A. 2008. Medical-grade honey kills antibiotic-resistant bacteria in vitro and eradicates skin colonization. Clin Infect Dis, 46(11), 1677-1682. DOI:10.1086/587892.
Kwakman P.H., te Velde A.A., de Boer L., Speijer D., Vandenbroucke-Grauls C.M. & Zaat S.A. 2010. How honey kills bacteria. FASEB J, 24(7): 2576-2582. DOI:10.1096/fj.09-150789
Kwakman P.H.S., de Boer L., Ruyter-Spira C.P., Creemers-Molenaar T., Helsper J.P.F.G., Vandenbroucke-Grauls C.M.J.E, Zaat S.A.J. & te Velde A.A. 2011. Medical-grade honey enriched with antimicrobial peptides has enhanced activity against antibiotic-resistant pathogens. Eur J Clin Microbiol Infect Dis, 30, 251–257. DOI 10.1007/s10096-010-1077-x
Langemo D.K., Hanson D., Anderson J., Thompson P. & Hunter S. 2009. Use of honey for wound healing. Adv Skin Wound Care, 22(3): 113–118.
Lu J., Turnbull L., Burke C.M., Liu M., Carter D.A., Schlothauer R.C., Whitchurch C.B. & Harry E.J. 2014. Manuka-Type Honeys Can Eradicate Biofilms Produced by Staphylococcus Aureus Strains with Different Biofilm-Forming Abilities. PeerJ, 2, e326. https://doi.org/10.7717/peerj.326.
Majtan J. 2014. Honey: An immunomodulator in wound healing. Wound Rep Reg, 22, 187–192.
Mandal M.D. & Mandal S. 2011. Honey: its medicinal property and antibacterial activity. Asian Pac J Trop Biomed, 1(2), 154-160.
Minden-Birkenmaier B.A. & Bowlin G.L. 2018. Honey-Based Templates in Wound Healing and Tissue Engineering. Bioengineering (Basel), 5(2), E46. doi: 10.3390/bioengineering5020046.
Mitchell M.A. & Diaz-Figueroa O. 2004. Wound management in reptiles. Vet Clin North Am Exot Anim Pract, 7:123-140.
Mohapatra D.P., Thakur V. & Brar S.K. 2011. Antibacterial Efficacy of Raw and Processed Honey. Biotechnol Res Int, 917505 https://doi.org/10.4061/2011/917505.
Molan P.C. 2001. Potential of honey in the treatment of wounds and burns. Am J Clin Dermatol, 2(1), 13-19.
Molan P. & Rhodes T. 2015. Honey: A Biologic Wound Dressing. Wounds, 27(6), 141-151.
Olofsson T.C., Butler E., Lindholm C., Nilson B., Michanek P. Vasquez A. 2016. Fighting Off Wound Pathogens in Horses with Honeybee LacticAcid Bacteria. Curr Microbiol, 73, 463–473.
Pelizzone I., Di Ianni F. & Parmigiani E. 2014. Laser therapy for wound healing in chelonians: two case reports. Veterinaria (Cremona), 28, 33–38.
Prestinaci F., Pezzotti P. & Pantosti A. 2015. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health, 109(7), 309-318.
Quinn P.J., Carter M.E., Markey B.K. & Carter G.R. 1994. Bacterial pathogens: microscopy, culture and identification. In Clinical Veterinary Microbiology. Mosby-YearBook Europe, 21-66.
Rosique R.G., Rosique M.J. & Farina Junior J.A. 2015. Curbing inflammation in skin wound healing: a review. Int J Inflam, 316235 1-9. DOI 10.1155/2015/316235.
Schumacher H.H.A. 2004. Use of Medical Honey in Patients with Chronic Venous Leg Ulcers after Split-Skin Grafting. J Wound Care, 13(10), 451–452. https://doi.org/10.12968/jowc.2004.13.10.26693.
Shin H. & Ustunol Z. 2005. Carbohydrate composition of honey from different floral sources and their influence on growth of selected intestinal bacteria. Food Res Int, 38, 721–728.
Sørum H. & Sunde M. 2001. Resistance to antibiotics in the normal flora of animals. Vet Res, 32, 227–241. DOI: 10.1051/vetres:2001121
Subrahmanyam M. 1991. Topical application of honey in treatment of burns. Br J Surg, 78(4), 497-498.
Szmolka A. & Nagy B. 2013. Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol, 4, 258. DOI: 10.3389/fmicb.2013.00258
Taddei S., Dodi P.L., Di Ianni F., Cabassi C.S. & Cavirani S. 2010. Conjunctival flora of clinically normal captive green iguanas (Iguana iguana). Vet Rec, 167(1), 29-30. DOI: 10.1136/vr.b4868
Tang K.L, Caffrey N.P., Nóbrega D.B., Cork S.C., Ronksley P.E., Barkema H.W., Polachek A.J., Ganshorn H., Sharma N., Kellner J.D. & Ghali W.A. 2017. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis. Lancet Planet Health, 1(8), e316-e327. https://doi.org/10.1016/S2542-5196(17)30141-9
Vandamme L., Heneman A., Hoeksema H. Verbelen J. & Monstrey S. 2013. Honey in modern wound care: a systematic review. Burns, 39(8), 1514-1525.
Voidarou C., Alexopoulos A., Plessas S., Karapanou A., Mantzourani I., Stavropoulou E., Fotou K., Tzora A., Skoufos I. & Bezirtzoglou E. 2011. Antibacterial activity of different honeys against pathogenic bacteria. Anaerobe, 17(6), 375-379. https://doi.org/10.1016/j.anaerobe.2011.03.012.