Application of orange essential oil as an antistaphylococcal agent in a dressing model

BMC Complementary and Alternative Medicine

Steven C Ricke²  Brian J Wilkinson¹  Philip G Crandall²  Debabrata Biswas³  Arunachalam Muthaiyan² 

[1] Microbiology Group, Department of Biological Sciences, Illinois State University, Normal, IL, 61790, USA;Center for Food Safety and Department of Food Science, University of Arkansas, Fayetteville, AR, 72701, USA;Current address: Department of Animal and Avian Sciences, University of Maryland, College Park, MD, 20742, USA

关键词: Orange essential oil;    Natural antimicrobials;    Antibiotic resistance;    S. aureus;    VISA;    MRSA;   

Others  :  1232090
DOI  :  10.1186/1472-6882-12-125

 received in 2011-11-05, accepted in 2012-08-08,  发布年份 2012

【 摘 要 】

Background

Staphylococcus aureus is the pathogen most often and prevalently involved in skin and soft tissue infections. In recent decades outbreaks of methicillin-resistant S. aureus (MRSA) have created major problems for skin therapy, and burn and wound care units. Topical antimicrobials are most important component of wound infection therapy. Alternative therapies are being sought for treatment of MRSA and one area of interest is the use of essential oils. With the increasing interest in the use and application of natural products, we screened the potential application of terpeneless cold pressed Valencia orange oil (CPV) for topical therapy against MRSA using an in vitro dressing model and skin keratinocyte cell culture model.

Methods

The inhibitory effect of CPV was determined by disc diffusion vapor assay for MRSA and vancomycin intermediate-resistant S. aureus (VISA) strains. Antistaphylococcal effect of CPV in an in vitro dressing model was tested on S. aureus inoculated tryptic soya agar plate. Bactericidal effect of CPV on MRSA and VISA infected keratinocyte cells was examined by enumeration of extra- and intra-cellular bacterial cells at different treatment time points. Cytotoxic effects on human skin cells was tested by adding CPV to the keratinocyte (HEK001) cells grown in serum free KSFM media, and observed by phase-contrast microscope.

Results

CPV vapour effectively inhibited the MRSA and VISA strains in both disc diffusion vapour assay and in vitro dressing model. Compared to untreated control addition of 0.1% CPV to MRSA infected keratinocyte decreased the viable MRSA cells by 2 log CFU/mL in 1 h and in VISA strain 3 log CFU/mL reduction was observed in 1 h. After 3 h viable S. aureus cells were not detected in the 0.2% CPV treatment. Bactericidal concentration of CPV did not show any cytotoxic effect on the human skin keratinocyte cells in vitro.

Conclusions

At lower concentration addition of CPV to keratinocytes infected with MRSA and VISA rapidly killed the bacterial cells without causing any toxic effect to the keratinocytes. Therefore, the results of this study warrant further in vivo study to evaluate the potential of CPV as a topical antistaphylococcal agent.

【 授权许可】

   
2012 Muthaiyan et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Otto M: Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu Rev Microbiol 2010, 64(1):143-162.
• [2]Chen AE, Goldstein M, Carroll K, Song X, Perl TM, Siberry GK: Evolving epidemiology of pediatric Staphylococcus aureus cutaneous infections in a Baltimore hospital. Pediatr Emerg Care 2006, 22(10):717.
• [3]Hersh AL, Chambers HF, Maselli JH, Gonzales R: National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections. Arch Intern Med 2008, 168(14):1585-1591.
• [4]Kish TD, Chang MH, Fung HB: Treatment of skin and soft tissue infections in the elderly: A review. Am J Geri Pharmacother 2010, 8(6):485-513.
• [5]Koerner R, Johnson AP: Changes in the classification and management of skin and soft tissue infections. J Antimicrob Chemother 2011, 66(2):232-234.
• [6]Edwards-Jones V, Greenwood JE: What’s new in burn microbiology?: James Laing Memorial Prize Essay 2000. Burns 2003, 29(1):15-24.
• [7]Guggenheim M, Zbinden R, Handschin AE, Gohritz A, Altintas MA, Giovanoli P: Changes in bacterial isolates from burn wounds and their antibiograms: A 20-year study (1986–2005). Burns 2009, 35(4):553-560.
• [8]Edwards-Jones V, Dawson MM, Childs C: A survey into toxic shock syndrome (TSS) in UK burns units. Burns 2000, 26(4):323-333.
• [9]Novick RP: MEDICINE: Combating Impervious Bugs. Science 2008, 319(5865):910-911.
• [10]Pirri G, Giuliani A, Nicoletto SF, Pizzuto L, Rinaldi AC: Lipopeptides as anti-infectives: a practical perspective. Centr Eur J Biol 2009, 4(3):258-273.
• [11]Stein RA: Antibiotic resistance: A global, interdisciplinary concern. The Am Biol Teacher 2011, 73(6):314-321.
• [12]Saxena S, Kumar D: Tailoring biodiversity for the development of new therapeutics. Nat Prod Rad 2002, 1:18-25.
• [13]Singh SB, Barrett JF: Empirical antibacterial drug discovery—Foundation in natural products. Biochem Pharmacol 2006, 71(7):1006-1015.
• [14]Butler MS, Buss AD: Natural products — The future scaffolds for novel antibiotics? Biochem Pharmacol 2006, 71(7):919-929.
• [15]Patwardhan B, Mashelkar RA: Traditional medicine-inspired approaches to drug discovery: can Ayurveda show the way forward? Drug Discov Today 2009, 14(15–16):804-811.
• [16]Saleem M, Nazir M, Ali MS, Hussain H, Lee YS, Riaz N, Jabbar A: Antimicrobial natural products: an update on future antibiotic drug candidates. Nat Prod Rep 2010, 27(2):238-254.
• [17]McChesney JD, Venkataraman SK, Henri JT: Plant natural products: Back to the future or into extinction? Phytochemistry 2007, 68(14):2015-2022.
• [18]Saravolatz LD, Markowitz N, Arking L, Pohlod D, Fisher E: Methicillin-resistant Staphylococcus aureus. Ann Intern Med 1982, 96(1):11-16.
• [19]Burt S: Essential oils: their antibacterial properties and potential applications in foods: a review. Inter J Food Microbiol 2004, 94:223-253.
• [20]Halcón L, Milkus K: Staphylococcus aureus and wounds: A review of tea tree oil as a promising antimicrobial. Am J Infect Con 2004, 32(7):402-408.
• [21]Fisher K, Phillips C: Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends Food Sci Technol 2008, 19(3):156-164.
• [22]Hammer KA, Carson CF, Riley TV, Nielsen JB: A review of the toxicity of Melaleuca alternifolia (tea tree) oil. Food Chem Toxicol 2006, 44(5):616-625.
• [23]Cox S, Gustafson J, Mann C, Markham J, Liew Y, Hartland R, Bell H, Warmington J, Wyllie S: Tea tree oil causes K+ leakage and inhibits respiration in Escherichia coli. Lett Appl Microbiol 1998, 26:355-358.
• [24]Elsom GKF, Hide D: Susceptibility of methicillin-resistant Staphylococcus aureus to tea tree oil and mupirocin. J Antimicrob Chemother 1999, 43(3):427-428.
• [25]Hammer KA, Carson CF, Riley TV: Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 1999, 86(6):985-990.
• [26]May J, Chan CH, King A, Williams L, French GL: Time-kill studies of tea tree oils on clinical isolates. J Antimicrob Chemother 2000, 45(5):639-643.
• [27]Takarada K, Kimizuka R, Takahashi N, Honma K, Okuda K, Kato T: A comparison of the antibacterial efficacies of essential oils against oral pathogens. Oral Microbiol Immunol 2002, 19:61-4.
• [28]Brady A, Loughlin R, Gilpin D, Kearney P, Tunney M: In vitro activity of tea-tree oil against clinical skin isolates of meticillin-resistant and -sensitive Staphylococcus aureus and coagulase-negative staphylococci growing planktonically and as biofilms. J Med Microbiol 2006, 55(10):1375-1380.
• [29]Prabuseenivasan S, Jayakumar M, Ignacimuthu S: In vitro antibacterial activity of some plant essential oils. BMC Complem Alt Med 2006, 6(1):39. BioMed Central Full Text
• [30]Chao S, Young G, Oberg C, Nakaoka K: Inhibition of methicillin-resistant Staphylococcus aureus (MRSA) by essential oils. Flavour Fragrance J 2008, 23(6):444-449.
• [31]Fisher K, Phillips CA: The effect of lemon, orange and bergamot essential oils and their components on the survival of Campylobacter jejuni, Escherichia coli O157, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus in vitro and in food systems. J Appl Microbiol 2006, 101(6):1232-1240.
• [32]O'Bryan CA, Crandall PG, Chalova VI, Ricke SC: Orange essential oils antimicrobial activities against Salmonella spp. J Food Sci 2008, 73(6):M264-M267.
• [33]Friedly EC, Crandall PG, Ricke SC, Roman M, O'Bryan C, Chalova VI: In vitro antilisterial effects of citrus oil fractions in combination with organic acids. J Food Sci 2009, 74(2):M67-M72.
• [34]Shannon EM, Milillo SR, Johnson MG, Ricke SC: Efficacy of cold-pressed terpeneless Valencia oil and its primary components on inhibition of Listeria species by direct contact and exposure to vapors. J Food Sci 2011, 76(7):M500-M503.
• [35]Nannapaneni R, Muthaiyan A, Crandall PG, Johnson MG, O'Bryan CA, Chalova VI, Callaway TR, Carroll JA, Arthington JD, Nisbet DJ: Antimicrobial activity of commercial citrus-based natural extracts against Escherichia coli O157: H7 isolates and mutant strains. Foodborne Pathog Dis 2008, 5(5):695-699.
• [36]Nannapaneni R, Chalova VI, Crandall PG, Ricke SC, Johnson MG, O'Bryan CA: Campylobacter and Arcobacter species sensitivity to commercial orange oil fractions. Int J Food Microbiol 2009, 129(1):43-49.
• [37]Muthaiyan A, Martin EM, Natesan S, Crandall PG, Wilkinson BJ, Ricke SC: Antimicrobial effect and mode of action of terpeneless cold-pressed Valencia orange essential oil on methicillin-resistant Staphylococcus aureus. J Appl Microbiol 2012, 112(5):1020-33.
• [38]Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ: sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325–4. J Bacteriol 2002, 184(19):5457-67.
• [39]Sabath LD, Wallace SJ, Byers K, Toftegaard I: Resistance of Staphylococcus aureus to penicillins and cephalosporins: reversal of intrinsic resistance with some chelating agents. Ann N Y Acad Sci 1974, 236:435-43.
• [40]Brown DF, Reynolds PE: Intrinsic resistance to beta-lactam antibiotics in Staphylococcus aureus. FEBS Lett 1980, 122(2):275-278.
• [41]Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, Cui L, Oguchi A, Aoki K, Nagai Y: Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 2001, 357(9264):1225-1240.
• [42]Pfeltz RF, Singh VK, Schmidt JL, Batten MA, Baranyk CS, Nadakavukaren MJ, Jayaswal RK, Wilkinson BJ: Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob Agents Chemother 2000, 44(2):294-303.
• [43]Braddock RJ: Handbook of citrus by-products and processing technology. Willey, New York; 1999.
• [44]Goñi P, López P, Sánchez C, Gómez-Lus R, Becerril R, Nerín C: Antimicrobial activity in the vapour phase of a combination of cinnamon and clove essential oils. Food Chem 2009, 116(4):982-989.
• [45]Edwards-Jones V, Buck R, Shawcross SG, Dawson MM, Dunn K: The effect of essential oils on methicillin-resistant Staphylococcus aureus using a dressing model. Burns 2004, 30(8):772-777.
• [46]Chung NM, Marshall CM, Leyden JJ, Lavker RM, Jensen PJ, Marsh BCR: Sodium dodecyl sulfate induces plasminogen activator inhibitor type 2 expression in epidermal keratinocytes in vivo and in vitro. J Invest Dermatol 2001, 117(3):647-653.
• [47]Harvey HA, Jennings MP, Campbell CA, Williams R, Apicella MA: Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol Microbiol 2001, 42(3):659-672.
• [48]Dorman HJD, Deans SG: Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 2000, 88(2):308-316.
• [49]Gaunt LF, Higgins SC, Hughes JF: Interaction of air ions and bactericidal vapours to control micro-organisms. J Appl Microbiol 2005, 99(6):1324-1329.
• [50]Lopez P, Sanchez C, Batlle R, Nerin C: Solid-and vapor-phase antimicrobial activities of six essential oils: susceptibility of selected foodborne bacterial and fungal strains. J Agric Food Chem 2005, 53(17):6939-6946.
• [51]Van de Sandt J, Roguet R, Cohen C, Esdaile D, Ponec M, Corsini E, Barker C, Fusenig N, Liebsch M, Benford D: The use of human keratinocytes and human skin models for predicting skin irritation. The Report and Recommendations of ECVAM Workshop. ATLA 1999, 27:723-744.
• [52]Gallo RL, Nakatsuji T: Microbial symbiosis with the innate immune defense system of the skin. J Invest Dermatol 2011, 131(October 2011):1974-1980.
• [53]Welss T, Basketter DA, Schröder KR: In vitro skin irritation: facts and future. State of the art review of mechanisms and models. Toxicol In Vitro 2004, 18(3):231-243.
• [54]Woolf AD: Herbal remedies and children: Do they work? Are they harmful? Pediatrics 2003, 112(1):240-246.
• [55]Dryden MS, Dailly S, Crouch M: A randomized, controlled trial of tea tree topical preparations versus a standard topical regimen for the clearance of MRSA colonization. J Hosp Infect 2004, 56(4):283-286.
• [56]Sherry E, Warnke PH: Successful use of an inhalational phytochemical to treat pulmonary tuberculosis: A case report. Phytomedicine 2004, 11(2–3):95-97.
• [57]Caelli M, Porteous J, Carson CF, Heller R, Riley TV: Tea tree oil as an alternative topical decolonization agent for methicillin-resistant Staphylococcus aureus. J Hosp Infect 2000, 46(3):236-237.
• [58]Sherry E, Boeck H, Warnke P: Percutaneous treatment of chronic MRSA osteomyelitis with a novel plant-derived antiseptic. BMC Surgery 2001, 1(1):1. BioMed Central Full Text
• [59]Caelli M, Porteous J, Carson CF, Heller R, Riley TV: Tea tree oil as an alternative topical decolonization agent for methicillin-resistant Staphylococcus aureus. Int J Aromather 2001, 11(2):97-99.
• [60]Sherry E, Boeck H, Warnke PH: Topical application of a new formulation of eucalyptus oil phytochemical clears methicillin-resistant Staphylococcus aureus infection. Am J Infect Control 2001, 29(5):346-346.
• [61]Palaniappan K, Holley RA: Use of natural antimicrobials to increase antibiotic susceptibility of drug resistant bacteria. Int J Food Microbiol 2010, 140(2–3):164-168.
• [62]Klein E, Smith DL, Laxminarayan R: Community-associated methicillin-resistant Staphylococcus aureus in outpatients, United States, 1999–2006. Emerg Infect Dis 2009, 15(12):1925-1930.
• [63]Mera RM, Suaya JA, Amrine-Madsen H, Hogea CS, Miller LA, Lu EP, Sahm DF, O'Hara P, Acosta CJ: Increasing role of Staphylococcus aureus and community-acquired methicillin-resistant Staphylococcus aureus infections in the United States: A 10-year trend of replacement and expansion. Microb Drug Resist 2011, 17(2):321-328.