A number of essential oils from citrus peels are claimed to have biological activities. Citrus peel, called ‘Jin-Pi’, is used in traditional medicine for digestion, severe cold, and fever. However, the antibacterial activities against skin pathogens and anti-inflammatory effects of the essential oils of Citrus sunki (JinGyul) and Fortunella japonica var. margarita (GumGyul) have not yet been described. Therefore, in this study, the essential oils of the citrus species C. sunki (CSE) and F. japonica var. margarita (FJE), both native to the island of Jeju, Korea, were examined for their anti-inflammatory and antimicrobial activities against skin pathogens. Four human skin pathogenic microorganisms, Staphylococcus epidermidis CCARM 3709, Propionibacterium acnes CCARM 0081, Malassezia furfur KCCM 12679, and Candida albicans KCCM 11282, were studied. CSE and FJE exhibited strong antimicrobial activity against most of the pathogenic bacteria and yeast strains that were tested. Interestingly, CSE and FJE even showed antimicrobial activity against antibiotic-resistant S. epidermidis CCARM 3710, S. epidermidis CCARM 3711, P. acnes CCARM9009, and P. acnes CCARM9010 strains. In addition, CSE and FJE reduced the lipopolysaccharide (LPS)-induced secretion of nitric oxide (NO) in RAW 264.7 cells, indicating that they have anti-inflammatory effects. We also analysed the chemical composition of the oils by gas chromatography-mass spectrometry (GC-MS) and identified several major components, including dl-limonene (68.18%) and β-myrcene (4.36%) for CSE, and dl-limonene (61.58%) and carvone (6.36%) for FJE. Taken together, these findings indicate that CSE and FJE have great potential to be used in human skin health applications.
Bakkali, F., Averbeck, S., Averbeck, D., Idaomar, M.: Biological effects of essential oils — a review. Food Chem. Toxicol. 46 , 446–475 (2008).
Idaomar M. , 'Biological effects of essential oils — a review ' (2008 ) 46 Food Chem. Toxicol. : 446 -475.
Kim, J. Y., Oh, T. H., Kim, B. J., Kim, S. S., Lee, N. H., Hyun, C. G.: Chemical composition and anti-inflammatory effects of essential oil from Farfugium japonicum flower. J. Oleo Sci. 57 , 623–628 (2008).
Hyun C. G. , 'Chemical composition and anti-inflammatory effects of essential oil from Farfugium japonicum flower ' (2008 ) 57 J. Oleo Sci. : 623 -628.
Yoon, W. J., Kim, S. S., Oh, T. H., Lee, N. H., Hyun, C. G.: Cryptomeria japonica essential oil inhibits the growth of drug-resistant skin pathogens and LPS-induced nitric oxide and pro-inflammatory cytokine production. Pol. J. Microbiol. 58 , 61–68 (2009).
Hyun C. G. , 'Cryptomeria japonica essential oil inhibits the growth of drug-resistant skin pathogens and LPS-induced nitric oxide and pro-inflammatory cytokine production ' (2009 ) 58 Pol. J. Microbiol. : 61 -68.
Nannapaneni, R., Muthaiyan, A., Crandall, P. G., Johnson, M. G., O’Bryan, C. A., Chalova, V. I., Callaway, T. R., Carroll, J. A., Arthington, J. D., Nisbet, D. J., Ricke, S. C.: Antimicrobial activity of commercial citrus-based natural extracts against Escherichia coli O157:H7 isolates and mutant strains. Foodborne Pathog. Dis. 5 , 695–699 (2008).
Ricke S. C. , 'Antimicrobial activity of commercial citrus-based natural extracts against Escherichia coli O157:H7 isolates and mutant strains ' (2008 ) 5 Foodborne Pathog. Dis. : 695 -699.
Oh, T. H., Kim, S. S., Yoon, W. J., Kim, J. Y., Yang, E. J., Lee, N. H., Hyun, C. G.: Chemical composition and biological activities of jeju Thymus quinquecostatus essential oils against Propionibacterium species inducing acne. J. Gen. Appl. Microbiol. 55 , 63–68 (2009).
Hyun C. G. , 'Chemical composition and biological activities of jeju Thymus quinquecostatus essential oils against Propionibacterium species inducing acne ' (2009 ) 55 J. Gen. Appl. Microbiol. : 63 -68.
Barbosa, L. N., Rall, V. L., Fernandes, A. A., Ushimaru, P. I., da Silva Probst, I., Fernandes, A. Jr.: Essential oils against foodborne pathogens and spoilage bacteria in minced meat. Foodborne Pathog. Dis. 6 , 725–728 (2009).
Fernandes A. , 'Essential oils against foodborne pathogens and spoilage bacteria in minced meat ' (2009 ) 6 Foodborne Pathog. Dis. : 725 -728.
Vukovic, N., Milosevic, T., Sukdolak, S., Solujic, S.: Antimicrobial activities of essential oil and methanol extract of Teucrium montanum . Evid. Based Complement. Alternat. Med. 4 , 17–20 (2007).
Solujic S. , 'Antimicrobial activities of essential oil and methanol extract of Teucrium montanum ' (2007 ) 4 Evid. Based Complement. Alternat. Med. : 17 -20.
Choi, S. Y., Hwang, J. H., Ko, H. C., Park, J. G., Kim, S. J.: Nobiletin from citrus fruit peel inhibits the DNA-binding activity of NF-kappaB and ROS production in LPS-activated RAW 264.7 cells. J. Ethnopharmacol. 113 , 149–155 (2007).
Kim S. J. , 'Nobiletin from citrus fruit peel inhibits the DNA-binding activity of NF-kappaB and ROS production in LPS-activated RAW 264.7 cells ' (2007 ) 113 J. Ethnopharmacol. : 149 -155.
Ghasemia, K., Ghasemia, Y., Ebrahimzadehb, M. A.: Antioxidant activity, phenol and flavonoid contents of 13 citrus species peels and tissues. Pak. J. Pharm. Sci. 22 , 277–281 (2009).
Ebrahimzadehb M. A. , 'Antioxidant activity, phenol and flavonoid contents of 13 citrus species peels and tissues ' (2009 ) 22 Pak. J. Pharm. Sci. : 277 -281.
Itoh, K., Hirata, N., Masuda, M., Naruto, S., Murata, K., Wakabayashi, K., Matsuda, H.: Inhibitory effects of Citrus hassaku extract and its flavanone glycosides on melanogenesis. Biol. Pharm. Bull. 32 , 410–415 (2009).
Matsuda H. , 'Inhibitory effects of Citrus hassaku extract and its flavanone glycosides on melanogenesis ' (2009 ) 32 Biol. Pharm. Bull. : 410 -415.
Parmar, H. S., Kar, A.: Antidiabetic potential of Citrus sinensis and Punica granatum peel extracts in alloxan treated male mice. Biofactors 31 , 17–24 (2007).
Kar A. , 'Antidiabetic potential of Citrus sinensis and Punica granatum peel extracts in alloxan treated male mice ' (2007 ) 31 Biofactors : 17 -24.
Ho, S. C., Lin, C. C.: Investigation of heat treating conditions for enhancing the anti-inflammatory activity of citrus fruit (Citrus reticulata) peels. J. Agric. Food Chem. 56 , 7976–7982 (2008).
Lin C. C. , 'Investigation of heat treating conditions for enhancing the anti-inflammatory activity of citrus fruit (Citrus reticulata) peels ' (2008 ) 56 J. Agric. Food Chem. : 7976 -7982.
Parmar, H. S., Kar, A.: Antiperoxidative, antithyroidal, antihyperglycemic and cardioprotective role of Citrus sinensis peel extract in male mice. Phytother. Res. 22 , 791–795 (2008).
Kar A. , 'Antiperoxidative, antithyroidal, antihyperglycemic and cardioprotective role of Citrus sinensis peel extract in male mice ' (2008 ) 22 Phytother. Res. : 791 -795.
Orallo, F., Camiña, M., Alvarez, E., Basaran, H., Lugnier, C.: Implication of cyclic nucleotide phosphodiesterase inhibition in the vasorelaxant activity of the citrus-fruits flavonoid (+/−)-naringenin. Planta Med. 71 , 99–107 (2005).
Lugnier C. , 'Implication of cyclic nucleotide phosphodiesterase inhibition in the vasorelaxant activity of the citrus-fruits flavonoid (+/−)-naringenin ' (2005 ) 71 Planta Med. : 99 -107.
Reverberi, M., Betti, C., Fabbri, A. A., Zjalic, S., Spadoni, S., Mattei, B., Fanelli, C.: A role for oxidative stress in the Citrus limon/Phoma tracheiphila interaction. Plant Pathol. 57 , 92–102 (2008).
Fanelli C. , 'A role for oxidative stress in the Citrus limon/Phoma tracheiphila interaction ' (2008 ) 57 Plant Pathol. : 92 -102.
Yang, E. J., Kim, S. S., Oh, T. H., Baik, J. S., Lee, N. H., Hyun, C. G.: Essential oil of citrus fruit waste attenuates LPS-induced nitric oxide production and inhibits the growth of skin pathogens. Int. J. Agric. Biol. 11 , 791–794 (2009).
Hyun C. G. , 'Essential oil of citrus fruit waste attenuates LPS-induced nitric oxide production and inhibits the growth of skin pathogens ' (2009 ) 11 Int. J. Agric. Biol. : 791 -794.
Malhotra, S., Suri, S., Tuli, R.: Antioxidant activity of citrus cultivars and chemical composition of Citrus karna essential oil. Planta Med. 75 , 62–44 (2009).
Tuli R. , 'Antioxidant activity of citrus cultivars and chemical composition of Citrus karna essential oil ' (2009 ) 75 Planta Med. : 62 -44.
Lan Phi, N. T., Nishiyama, C., Choi, H. S, Sawamura, M.: Evaluation of characteristic aroma compounds of Citrus natsudaidai Hayata (Natsudaidai) cold-pressed peel oil. Biosci. Biotechnol. Biochem. 70 , 1832–1838 (2006).
Sawamura M. , 'Evaluation of characteristic aroma compounds of Citrus natsudaidai Hayata (Natsudaidai) cold-pressed peel oil ' (2006 ) 70 Biosci. Biotechnol. Biochem. : 1832 -1838.
Quijano, C. E., Pino, J. A.: Volatile compounds of round kumquat ( Fortunella japonica Swingle) peel oil from Colombia. J. Essent. Oil Res. 21 , 483–485 (2009).
Pino J. A. , 'Volatile compounds of round kumquat (Fortunella japonica Swingle) peel oil from Colombia ' (2009 ) 21 J. Essent. Oil Res. : 483 -485.
Choi, H. S.: Characteristic odor components of kumquat ( Fortunella japonica Swingle) peel oil. J. Agric. Food Chem. 53 , 1642–1647 (2005).
Choi H. S. , 'Characteristic odor components of kumquat (Fortunella japonica Swingle) peel oil ' (2005 ) 53 J. Agric. Food Chem. : 1642 -1647.
Umano, K., Hagi, Y., Tamura, T., Shoji, A., Shibamoto, T.: Identification of volatile compounds isolated from round kumquat ( Fortunella japonica Swingle). J. Agric. Food Chem. 42 , 1888–1890 (1994).
Shibamoto T. , 'Identification of volatile compounds isolated from round kumquat (Fortunella japonica Swingle) ' (1994 ) 42 J. Agric. Food Chem. : 1888 -1890.
Alviano, D. S., Alviano, C. S.: Plant extracts: Search for new alternatives to treat microbial diseases. Curr. Pharm. Biotechnol. 10 , 106–121 (2009).
Alviano C. S. , 'Plant extracts: Search for new alternatives to treat microbial diseases ' (2009 ) 10 Curr. Pharm. Biotechnol. : 106 -121.
Raja, S. B., Murali, M. R., Devaraj, S. N.: Differential expression of ompC and ompF in multidrug-resistant Shigella dysenteriae and Shigella flexneri by aqueous extract of Aegle marmelos, altering its susceptibility toward beta-lactam antibiotics. Diagn. Microbiol. Infect. Dis. 61 , 321–328 (2008).
Devaraj S. N. , 'Differential expression of ompC and ompF in multidrug-resistant Shigella dysenteriae and Shigella flexneri by aqueous extract of Aegle marmelos, altering its susceptibility toward beta-lactam antibiotics ' (2008 ) 61 Diagn. Microbiol. Infect. Dis. : 321 -328.
Simonart, T., Dramaix, M.: Treatment of acne with topical antibiotics: Lessons from clinical studies. Br. J. Dermatol. 153 , 395–403 (2005).
Dramaix M. , 'Treatment of acne with topical antibiotics: Lessons from clinical studies ' (2005 ) 153 Br. J. Dermatol. : 395 -403.
Ross, J. I., Snelling, A. M., Carnegie, E., Coates, P., Cunliffe, W. J., Bettoli, V., Tosti, G., Katsambas, A., Galvan Peréz Del Pulgar, J. I., Rollman, O., Török, L., Eady, E. A., Cove, J. H.: Antibiotic-resistant acne: Lessons from Europe. Br. J. Dermatol. 148 , 467–478 (2003).
Cove J. H. , 'Antibiotic-resistant acne: Lessons from Europe ' (2003 ) 148 Br. J. Dermatol. : 467 -478.
Tan, A. W., Tan, H. H.: Acne vulgaris: A review of antibiotic therapy. Exp. Opin. Pharmacother. 6 , 409–418 (2005).
Tan H. H. , 'Acne vulgaris: A review of antibiotic therapy ' (2005 ) 6 Exp. Opin. Pharmacother. : 409 -418.
Yoon, W. J., Kim, S. S., Oh, T. H., Lee, N. H., Hyun, C. G.: Abies koreana essential oil inhibits drug-resistant skin pathogen growth and LPS-induced inflammatory effects of murine macrophage. Lipids 44 , 471–476 (2009).
Hyun C. G. , 'Abies koreana essential oil inhibits drug-resistant skin pathogen growth and LPS-induced inflammatory effects of murine macrophage ' (2009 ) 44 Lipids : 471 -476.
Raman, A., Weir, U., Bloomfield, S. F.; Antimicrobial effects of tea-tree oil and its major components on Staphylococcus aureus, Staph. epidermidis and Propionibacterium acnes . Lett. Appl. Microbiol. 21 , 242–245 (1995).
Bloomfield S. F. , 'Antimicrobial effects of tea-tree oil and its major components on Staphylococcus aureus, Staph. epidermidis and Propionibacterium acnes ' (1995 ) 21 Lett. Appl. Microbiol. : 242 -245.
Demirci, F., Noma, Y., Kirimer, N., Can Baper, K. H.: Microbial transformation of (−)-carvone. Z. Naturforsch. C. 59 , 389–392 (2004).
Can Baper K. H. , 'Microbial transformation of (−)-carvone ' (2004 ) 59 Z. Naturforsch. C. : 389 -392.
Kotan, R., Kordali, S., Cakir, A.: Screening of antibacterial activities of twenty-one oxygenated monoterpenes. Z. Naturforsch. C. 62 , 507–513 (2007).
Cakir A. , 'Screening of antibacterial activities of twenty-one oxygenated monoterpenes ' (2007 ) 62 Z. Naturforsch. C. : 507 -513.
van Vuuren, S. F., Viljoen, A. M.: Antimicrobial activity of limonene enantiomers and 1,8-cineole alone and in combination. Flav. Frag. J. 22 , 540–544 (2007).
Viljoen A. M. , 'Antimicrobial activity of limonene enantiomers and 1,8-cineole alone and in combination ' (2007 ) 22 Flav. Frag. J. : 540 -544.
Dorman, H. J., Deans, S. G.: Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. J. Appl. Microbiol. 88 , 308–316 (2000).
Deans S. G. , 'Antimicrobial agents from plants: Antibacterial activity of plant volatile oils ' (2000 ) 88 J. Appl. Microbiol. : 308 -316.
Tripathi, P.: Nitric oxide and immune response. Indian J. Biochem. Biophys. 44 , 310–319 (2007).
Tripathi P. , 'Nitric oxide and immune response ' (2007 ) 44 Indian J. Biochem. Biophys. : 310 -319.
Sharma, J. N., Al-Omran, A., Parvathy, S. S.: Role of nitric oxide in inflammatory diseases. Inflammopharmacol. 15 , 252–259 (2007).
Parvathy S. S. , 'Role of nitric oxide in inflammatory diseases ' (2007 ) 15 Inflammopharmacol : 252 -259.
Murakami, A.: Chemoprevention with phytochemicals targeting inducible nitric oxide synthase. Forum Nutr. 61 , 193–203 (2009).
Murakami A. , 'Chemoprevention with phytochemicals targeting inducible nitric oxide synthase ' (2009 ) 61 Forum Nutr. : 193 -203.
Murakami, A., Ohigashi, H.: Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int. J. Cancer 121 , 2357–2363 (2007).
Ohigashi H. , 'Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals ' (2007 ) 121 Int. J. Cancer : 2357 -2363.