PHYTOTHERAPY RESEARCH Phytother. Res. 28: 1867–1872 (2014) Published online 15 September 2014 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/ptr.5219
Chemical Composition and Antimicrobial Activity of the Essential Oil of Apricot Seed Hyun-hee Lee,1 Jeong-Hyun Ahn,1 Ae-Ran Kwon,1 Eun Sook Lee,1 Jin-Hwan Kwak2 and Yu-Hong Min1* 1
Department of Herbal Skin Care, College of Herbal Bio-Industry, Daegu Haany University, Gyeongsan, 712-715, Korea School of Life and Food Sciences, Handong Global University, Pohang, 791-708, Korea
2
In traditional oriental medicine, apricot (Prunus armeniaca L.) seed has been used to treat skin diseases such as furuncle, acne vulgaris and dandruff, as well as coughing, asthma and constipation. This study describes the phytochemical profile and antimicrobial potential of the essential oil obtained from apricot seeds (Armeniacae Semen). The essential oil isolated by hydrodistillation was analysed by gas chromatography–mass spectroscopy. Benzaldehyde (90.6%), mandelonitrile (5.2%) and benzoic acid (4.1%) were identified. Disc diffusion, agar dilution and gaseous contact methods were performed to determine the antimicrobial activity against 16 bacteria and two yeast species. The minimum inhibitory concentrations ranged from 250 to 4000, 500 to 2000 and 250 to 1000 μg/mL for Gram-positive bacteria, Gram-negative bacteria and yeast strains, respectively. The minimum inhibitory doses by gaseous contact ranged from 12.5 to 50, 12.5 to 50 and 3.13 to 12.5 mg/L air for Gram-positive bacteria, Gram-negative bacteria and yeast strains, respectively. The essential oil exhibited a variable degree of antimicrobial activity against a range of bacteria and yeasts tested. Copyright © 2014 John Wiley & Sons, Ltd. Keywords: Prunus armeniaca L.; apricot seeds; essential oil; antimicrobial.
INTRODUCTION The apricot tree (Prunus armeniaca L.) belongs to the Prunus genus of the Rosaceae family. It is thought to have origin in China, Korea and Japan (Lim, 2012). It is cultivated mainly in Asia, Europe and America. The apricot seed (Armeniacae Semen) is commonly used for the production of oil, benzaldehyde and chemicals for cosmetic purposes (Lim, 2012). The apricot seed is rich in nutrients such as oils, proteins, soluble sugars and fibres (Femenia et al., 1995). The oil consists mainly of unsaturated fatty acids, such as oleic and linoleic acid (Femenia et al., 1995). Amygdalin is a poisonous substance found in the seed and tissue of apricot. Amygdalin is hydrolyzed by β-glucosidase to yield glucose, benzaldehyde and hydrogen cyanide (Haisman and Knight, 1967). In traditional oriental medicine, apricot seed has been widely used to treat respiratory symptoms and diseases such as coughing, wheeze, asthma, emphysema and bronchitis (Bensky et al., 2004). Moreover, it has been used for treating skin diseases such as furuncle, acne vulgaris and dandruff, as well as constipation (Ju et al., 2004). Pharmacological studies demonstrated antiasthmatic, antiinflammatory, analgesic, antimutagenic, anticancer, antioxidant and antimicrobial effects of the apricot seed (Yamamoto et al., 1992; Chang et al., 2005; Do et al., 2006; Chang et al., 2006; Ghazavi et al., 2008; Yiğit et al., 2009; Korekar et al., 2011). In the case of the antimicrobial activities, both water and methanol extracts exhibited * Correspondence to: Yu-Hong Min, PhD, Department of Herbal Skin Care, College of Herbal Bio-Industry, Daegu Haany University, 1 Haanydaero, Gyeongsan, 712-715, Korea. E-mail: [email protected]
Copyright © 2014 John Wiley & Sons, Ltd.
inhibitory activities against Staphylococcus aureus, Escherichia coli, Proteus mirabilis, Salmonella typhi and Candida albicans (Ghazavi et al., 2008; Yiğit et al., 2009). However, antimicrobial activity was not reported for the fixed seed oil (Hammer et al., 1999). Benzaldehyde is an aromatic molecule widely used as a flavour in foods and cosmetics and a precursor to pharmaceutical compounds (Brühne and Wright, 2007). It was also shown to have antitumor activity (Ariyoshi-Kishino et al., 2010). It is mainly found in Prunus species. The kernel oil of plum (Prunus domestica) contains benzaldehyde as a major volatile component (Pićurić-Jovanović and Milovanović, 1993). Benzaldehyde is also known to be present in the seeds of peach and cherry (Chandra and Nair, 1993; Mezzomo et al., 2010). The essential oil of cherry laurel leaves has a high content of benzaldehyde (Lazić et al., 2009). However, to the best of our knowledge, the specific concentration of benzaldehyde has never been reported in the essential oil from the seeds of Prunus species. The increasing resistance to antimicrobial agents has necessitated the search for therapeutic alternatives. Essential oils are today considered as the important sources for the natural antimicrobials. As the apricot seed is used for the treatment of skin diseases, it is reasonable to investigate the ability of the essential oil as an antimicrobial. To our knowledge, there are no published reports on the antimicrobial activity of the essential oil from Prunus species such as apricot seed. In the present study, we determined the constituents of the essential oil by a gas chromatography–mass spectroscopy (GC–MS) method and then evaluated antimicrobial properties of the essential oil and its major component using disc diffusion, agar dilution and gaseous contact methods. Received 28 January 2014 Revised 31 July 2014 Accepted 9 August 2014
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MATERIALS AND METHODS Plant material. Essential oil. The apricot fruits (P. armeniaca L. var. ansu Maxim.) were harvested from Gyeongju, Korea. Identification was confirmed by Prof. Seong-Soo Roh from the Department of Herbology, Daegu Haany University, Korea. A voucher specimen (no. AS12YM) has been deposited there. The air-dried and grounded seeds (300 g) were subjected to hydrodistillation in 1.5 L of water for 3 h in a Clevenger-type apparatus (Goheung Glass, Daegu, Korea; yield 0.27% w/w). Composition. The chemical composition of the apricot seed essential oil was determined by GC–MS using an Agilent 7890A GC in combination with an Agilent 5975C mass selective detector (Agilent Technologies, Santa Clara, CA, USA). The GC column was a DB-1 model (J&W Scientific, Folsom, CA, USA) with a length of 30 m, a diameter of 250 μm and film thickness of 0.25 μm. The carrier gas was helium at a flow rate of 1 mL/min. The oven temperature was programmed as follows: initial temperature of 50 °C for 2 min, then gradually increased to 280 °C at 10 °C/min and held for 5 min. The injector temperature was 250 °C, and the diluted sample (1/100, in CH2Cl2) was injected using a split mode (10:1). The components were identified by comparing their relative retention times and mass spectra with those of the standards and W9N08 library data of the GC–MS system. Benzaldehyde standard was purchased from Sigma-Aldrich (St. Louis, MO, USA).
Microbial strains. The essential oil and component were tested against 18 microorganisms of clinical importance. Reference strains were Bacillus cereus ATCC 27348, Enterococcus faecalis ATCC 29212, S. aureus ATCC 29213, Staphylococcus epidermidis ATCC 12228, Citrobacter freundii ATCC 6750, Enterobacter aerogenes ATCC 13048, Enterobacter cloacae ATCC 27508, E. coli ATCC 25922, Klebsiella pneumoniae ATCC 10031, P. mirabilis ATCC 25933, Pseudomonas aeruginosa ATCC 27853, Salmonella typhimurium ATCC 14028, Serratia marcescens ATCC 27117, Shigella sonnei ATCC 11060, C. albicans ATCC 10231 and Malassezia furfur ATCC 14521. Clinical strains were methicillin-resistant S. aureus (MRSA) P15 and P. aeruginosa D24 isolated from the Severance Hospital in Seoul.
Culture agar media. Mueller Hinton agar (Difco, Detroit, MI, USA), Sabouraud dextrose agar (Oxoid, Basingstoke, UK) and modified Dixon agar were used for bacteria, C. albicans and M. furfur, respectively. Antimicrobial activities for bacteria were determined after incubation at 35 °C for 24 h, at 30 °C for 48 h for C. albicans and at 32 °C for 72 h for M. furfur.
and 106 CFU/mL of yeast was spread on the agar plates. Sterile paper discs (8 mm in diameter; Advantec Toyo, Tokyo, Japan) were impregnated with 3 mg of the oil or component and placed on the inoculated agar surface (one disc per Petri dish). The diameter of the inhibition zones was measured after incubation. The positive controls (10 μg) were gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. All tests were repeated independently at least three times. Determination of the minimum inhibitory concentration and minimum bactericidal/fungicidal concentration by agar dilution. The agar dilution method was carried out as described previously (Hammer et al., 1999) with certain modifications. Mueller Hinton agar and Sabouraud dextrose agar were supplemented with 0.5% (v/v) Tween 20 (Sigma-Aldrich) to enhance the solubility of the oil or component. The agar plates were inoculated with the suspensions of bacteria and C. albicans (104 CFU/spot) and M. furfur (103 CFU/spot) using a microinoculator (Sakuma, Tokyo, Japan). The minimum inhibitory concentration (MIC) (μg/mL) was defined as the lowest concentration within the range of 125–16 000 μg/mL at which no growth was visible. To determine the minimum bactericidal/fungicidal concentration (MBC/MFC), a sample swab was taken from the inoculation spots having no visible growth and streaked on the growth agar without any inhibitory substance. The MBC/MFC (μg/mL) represents the lowest concentration at which the inoculated organism was completely killed. All of the assays were repeated independently at least three times. The inoculated plates without oil or compound were used as negative controls. The positive controls were gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively.
Determination of the minimum inhibitory dose by gaseous contact. The antimicrobial activity of the essential oil vapour phase was estimated by the method of Inouye et al. (2001). The plates were inoculated as described in MIC determination and then placed in 1.1-L airtight stainless-steel boxes (Carnation Co., Kimpo, Korea). Serial two-fold dilutions of the oil or component ranging from 1.65 to 846 mg/mL were made in ethyl acetate, and 260 μL of each dilution was soaked on filter paper (90 mm in diameter) to give final concentrations of 0.39 to 200 mg/L air space. After incubation, the minimum inhibitory dose (MID) (mg/L air space) was defined as the lowest inhibitory dose of the oil or component inhibiting visible growth.
RESULTS AND DISCUSSION Chemical composition of the essential oil
Disc diffusion method. The agar disc diffusion test was performed on the basis of the methods from the literature (Hernández et al., 2005). Briefly, plates were prepared in Petri dishes (with an inner diameter of 85.6 mm). Then, 0.1 mL from a cell suspension containing 108 colony-forming units (CFU)/mL of bacteria Copyright © 2014 John Wiley & Sons, Ltd.
Gas chromatography–mass spectroscopy analysis resulted in the identification of three compounds accounting for 99.9% of the total oil. Benzaldehyde was the predominant compound (90.6%), followed by mandelonitrile (5.2%) and benzoic acid (4.1%) (Fig. 1). Phytother. Res. 28: 1867–1872 (2014)
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Figure 1. Gas chromatography–mass spectroscopy chromatogram of the apricot seed essential oil.
Similar results were previously reported for the essential oil of cherry laurel (Prunus laurocerasus) leaves, which consisted of benzaldehyde (82.1%), mandelonitrile (15.4%), benzoic acid (1.12%) and 2-hexenal (0.63%) (Lazić et al., 2009). The plum seed (P. domestica) oil had benzaldehyde as a major volatile component but consisted of 50 or more volatile compounds (PićurićJovanović and Milovanović, 1993). Benzaldehyde was
also found in the pulp and skin of P. armeniaca (Takeoka et al., 1990; Guillot et al., 2006). The high benzaldehyde content in apricot seed essential oil is probably due to an increase in the contact between amygdalin and β-glucosidase that was caused by disruption of the seed cell wall that occurred in the course of sample grinding (Tunçel et al., 1998). The essential oil of the apricot seed could serve as a source of benzaldehyde. Mandelonitrile
Table 1. In vitro antimicrobial activity of apricot seed essential oil and its major component, benzaldehyde, by disc diffusion method Inhibition zone diameter (mm)a Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15c Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24c Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Benzaldehyde (3 mg)
Positive controlb (10 μg)
9.6 8.8 ti ti ti
9.9 15.4 ti ti 11.9
23.9 10.1 0.0 21.2 29.4
0.0 0.0 0.0 ti 9.5 0.0 ti ti ti 15.8 ti
0.0 0.0 0.0 11.7 9.1 0.0 38.6 21.8 10.1 9.0 11.5
19.3 18.0 21.1 21.5 23.1 20.8 20.6 11.7 19.1 22.7 19.2
ti ti
13.8 ti
13.6 19.7
Apricot seed essential oil (3 mg)
ti, total growth inhibition (see Materials and methods). The diameter of paper discs (8 mm) is included. b Gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. c Gentamicin-resistant clinical isolates. a
Copyright © 2014 John Wiley & Sons, Ltd.
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Table 2. MIC and MBC/MFC (μg/mL) of apricot seed essential oil and its major component, benzaldehyde Apricot seed essential oil Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15b Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24b Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Benzaldehyde
Positive controla
MIC
MBC/MFC
MIC
MBC/MFC
MIC
MBC/MFC
2000 4000 500 500 250
4000 8000 1000 1000 250
2000 4000 1000 1000 1000
4000 16 000 1000 1000 2000
0.25 8 32 0.25 0.13
0.25 8 32 0.25 0.13
2000 2000 1000 500 2000 2000 500 500 500 1000 500
4000 4000 2000 2000 4000 4000 1000 1000 2000 2000 2000
2000 2000 1000 1000 2000 4000 1000 1000 2000 2000 1000
4000 4000 2000 1000 2000 4000 2000 2000 8000 4000 2000
0.5 0.5 0.25 0.5 0.25 0.25 1 16 0.5 0.5 0.5
0.5 0.5 0.25 0.5 0.25 0.25 1 16 0.5 0.5 0.5
1000 250
2000 1000
2000 500
4000 2000
0.5 2
0.5 2
The MICs of gentamicin for E. faecalis ATCC 29212, S. aureus ATCC 29213, E. coli ATCC 25922 and P. aeruginosa ATCC 27853 were within the quality control ranges established by Clinical and Laboratory Standards Institute (2013). MIC, minimum inhibitory concentration; MBC/MFC, minimum bactericidal/fungicidal concentration. a Gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. b Gentamicin-resistant clinical isolates.
and benzoic acid were also detected as minor components of the oil. Although these compounds have been found in the seeds and stones of several Prunus species (Chandra and Nair, 1993; Pićurić-Jovanović and Milovanović, 1993; Khallouki et al., 2012), the specific content has not been established in the seed essential oil. Mandelonitrile is the reaction intermediate in the decomposition of amygdalin to benzaldehyde and hydrogen cyanide. Benzoic acid is generated by the oxidation of benzaldehyde. Other volatile compounds, such as linalool, which were previously shown to present in the pulp and skin of the apricot (Takeoka et al., 1990), were not detected in the seed essential oil. Benzyl alcohol, a major volatile component in the plum seed oil (Pićurić-Jovanović and Milovanović, 1993), was also not detected. Antimicrobial activity The results of the disc diffusion assay are presented in Table 1. The essential oil of the apricot seed exhibited a variable degree of antimicrobial activity against the 16 bacteria and two yeast species tested. Interestingly, complete inhibition of growth (a clear plate) was observed in three of the five Gram-positive bacteria, five of the 11 Gram-negative bacteria and both of the two yeast species (total inhibition). Weak activity or inactivity was observed against the other strains tested (≤15.8 mm). No obvious difference in susceptibility was found between Gram-positive and Gram-negative bacteria. Benzaldehyde, the major component of the oil, exhibited maximum activity against S. aureus strains including gentamicin-resistant MRSA (total inhibition). Copyright © 2014 John Wiley & Sons, Ltd.
Table 3. In vitro antimicrobial activity of apricot seed essential oil and its major component, benzaldehyde, by gaseous contact MID (mg/L air)
Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15a Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24a Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Apricot seed essential oil
25 50 12.5 12.5 25
Benzaldehyde
12.5 25 25 25 50
25 25 25 12.5 50 25 12.5 12.5 12.5 25 12.5
50 50 50 50 50 100 25 25 100 100 50
12.5 3.13
100 25
MIDs of ≤6.25, 12.5–50 and ≥100 mg/L air were regarded as high, moderate and weak activities, respectively (Inouye et al., 2001). MID, minimum inhibitory dose. a Gentamicin-resistant clinical isolates. Phytother. Res. 28: 1867–1872 (2014)
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The remaining strains were less susceptible to benzaldehyde (≤38.6 mm). For essential oils, the result of the disc diffusion method does not exactly reflect the antimicrobial effectiveness owing to the differences in the diffusion ability of the oils through the agar and the evaporation (Hernández et al., 2005). Thus, the MIC and MBC/MFC values of the essential oil were also determined. The MIC ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 250–4000, 500–2000 and 250–1000 μg/mL, respectively (Table 2). The MBC/MFC ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 250–8000, 1000–4000 and 1000–2000 μg/mL, respectively. The results of MIC and MBC/MFC indicated that the essential oil had low antimicrobial activity, as judged by the criteria suggested previously (Ríos and Recio, 2005). The MIC and MBC/MFC values of the oil were equal to or lower than those of benzaldehyde. The MIC range of benzaldehyde was 1000–4000 μg/mL, except M. furfur. Several studies previously reported comparable levels of MIC (>1000 μg/mL) against Bacillus subtilis, E. faecalis, S. aureus, E. coli and P. aeruginosa, among others (Kang et al., 1992; Chang et al., 2001). It is noticeable that the essential oil of apricot seed showed the same activity against gentamicin- and methicillin-susceptible S. aureus and gentamicin-resistant MRSA strains. It also showed the same activity against gentamicin-resistant P. aeruginosa and gentamicinsusceptible P. aeruginosa strains. The essential oils exert antimicrobial activity through gaseous contact as well as direct contact with microorganisms.
The antimicrobial activity of the apricot seed essential oil by gaseous contact is shown in Table 3. The MID ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 12.5–50, 12.5–50 and 3.13-12.5 mg/L air, respectively. E. faecalis and K. pneumoniae displayed the weakest susceptibility (MID 50 mg/L air). M. furfur was the most susceptible among the microorganisms tested (MID 3.13 mg/L air). The essential oil of apricot seed showed the highest activity against M. furfur and moderate activity against the other species, as judged by the values defined previously (Inouye et al., 2001). The MID values of benzaldehyde were comparable with or higher than those of the apricot seed essential oil.
CONCLUSION The results of this study suggest that the essential oil of the apricot seed could be a source of benzaldehyde. The essential oil of apricot seed possesses antimicrobial activity against a range of bacteria and yeasts. The essential oil has potential usage as an air disinfectant, preservative and antimicrobial agent. Additional study will be needed to assess the potential toxicity.
Conflict of Interest The authors declare that there is no conflict of interest.
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Takeoka GR, Flath RA, Mon TR, Teranishi R, Guentert M. 1990. Volatile constituents of apricot (Prunus armeniaca). J Agric Food Chem 38: 471–477. Tunçel G, Nout MJR, Brimer L. 1998. Degradation of cyanogenic glycosides of bitter apricot seeds (Prunus armeniaca) by endogenous and added enzymes as affected by heat treatments and particle size. Food Chem 63: 65–69. Yamamoto K, Osaki Y, Kato T, Miyazaki T. 1992. Antimutagenic substances in the Armeniacae semen and Persicae semen. Yakugaku Zasshi 112: 934–939. Yiğit D, Yiğit N, Mavi A. 2009. Antioxidant and antimicrobial activities of bitter and sweet apricot (Prunus armeniaca L.) kernels. Braz J Med Biol Res 42: 346–352.
Phytother. Res. 28: 1867–1872 (2014)
Chemical Composition and Antimicrobial Activity of the Essential Oil of Apricot Seed Hyun-hee Lee,1 Jeong-Hyun Ahn,1 Ae-Ran Kwon,1 Eun Sook Lee,1 Jin-Hwan Kwak2 and Yu-Hong Min1* 1
Department of Herbal Skin Care, College of Herbal Bio-Industry, Daegu Haany University, Gyeongsan, 712-715, Korea School of Life and Food Sciences, Handong Global University, Pohang, 791-708, Korea
2
In traditional oriental medicine, apricot (Prunus armeniaca L.) seed has been used to treat skin diseases such as furuncle, acne vulgaris and dandruff, as well as coughing, asthma and constipation. This study describes the phytochemical profile and antimicrobial potential of the essential oil obtained from apricot seeds (Armeniacae Semen). The essential oil isolated by hydrodistillation was analysed by gas chromatography–mass spectroscopy. Benzaldehyde (90.6%), mandelonitrile (5.2%) and benzoic acid (4.1%) were identified. Disc diffusion, agar dilution and gaseous contact methods were performed to determine the antimicrobial activity against 16 bacteria and two yeast species. The minimum inhibitory concentrations ranged from 250 to 4000, 500 to 2000 and 250 to 1000 μg/mL for Gram-positive bacteria, Gram-negative bacteria and yeast strains, respectively. The minimum inhibitory doses by gaseous contact ranged from 12.5 to 50, 12.5 to 50 and 3.13 to 12.5 mg/L air for Gram-positive bacteria, Gram-negative bacteria and yeast strains, respectively. The essential oil exhibited a variable degree of antimicrobial activity against a range of bacteria and yeasts tested. Copyright © 2014 John Wiley & Sons, Ltd. Keywords: Prunus armeniaca L.; apricot seeds; essential oil; antimicrobial.
INTRODUCTION The apricot tree (Prunus armeniaca L.) belongs to the Prunus genus of the Rosaceae family. It is thought to have origin in China, Korea and Japan (Lim, 2012). It is cultivated mainly in Asia, Europe and America. The apricot seed (Armeniacae Semen) is commonly used for the production of oil, benzaldehyde and chemicals for cosmetic purposes (Lim, 2012). The apricot seed is rich in nutrients such as oils, proteins, soluble sugars and fibres (Femenia et al., 1995). The oil consists mainly of unsaturated fatty acids, such as oleic and linoleic acid (Femenia et al., 1995). Amygdalin is a poisonous substance found in the seed and tissue of apricot. Amygdalin is hydrolyzed by β-glucosidase to yield glucose, benzaldehyde and hydrogen cyanide (Haisman and Knight, 1967). In traditional oriental medicine, apricot seed has been widely used to treat respiratory symptoms and diseases such as coughing, wheeze, asthma, emphysema and bronchitis (Bensky et al., 2004). Moreover, it has been used for treating skin diseases such as furuncle, acne vulgaris and dandruff, as well as constipation (Ju et al., 2004). Pharmacological studies demonstrated antiasthmatic, antiinflammatory, analgesic, antimutagenic, anticancer, antioxidant and antimicrobial effects of the apricot seed (Yamamoto et al., 1992; Chang et al., 2005; Do et al., 2006; Chang et al., 2006; Ghazavi et al., 2008; Yiğit et al., 2009; Korekar et al., 2011). In the case of the antimicrobial activities, both water and methanol extracts exhibited * Correspondence to: Yu-Hong Min, PhD, Department of Herbal Skin Care, College of Herbal Bio-Industry, Daegu Haany University, 1 Haanydaero, Gyeongsan, 712-715, Korea. E-mail: [email protected]
Copyright © 2014 John Wiley & Sons, Ltd.
inhibitory activities against Staphylococcus aureus, Escherichia coli, Proteus mirabilis, Salmonella typhi and Candida albicans (Ghazavi et al., 2008; Yiğit et al., 2009). However, antimicrobial activity was not reported for the fixed seed oil (Hammer et al., 1999). Benzaldehyde is an aromatic molecule widely used as a flavour in foods and cosmetics and a precursor to pharmaceutical compounds (Brühne and Wright, 2007). It was also shown to have antitumor activity (Ariyoshi-Kishino et al., 2010). It is mainly found in Prunus species. The kernel oil of plum (Prunus domestica) contains benzaldehyde as a major volatile component (Pićurić-Jovanović and Milovanović, 1993). Benzaldehyde is also known to be present in the seeds of peach and cherry (Chandra and Nair, 1993; Mezzomo et al., 2010). The essential oil of cherry laurel leaves has a high content of benzaldehyde (Lazić et al., 2009). However, to the best of our knowledge, the specific concentration of benzaldehyde has never been reported in the essential oil from the seeds of Prunus species. The increasing resistance to antimicrobial agents has necessitated the search for therapeutic alternatives. Essential oils are today considered as the important sources for the natural antimicrobials. As the apricot seed is used for the treatment of skin diseases, it is reasonable to investigate the ability of the essential oil as an antimicrobial. To our knowledge, there are no published reports on the antimicrobial activity of the essential oil from Prunus species such as apricot seed. In the present study, we determined the constituents of the essential oil by a gas chromatography–mass spectroscopy (GC–MS) method and then evaluated antimicrobial properties of the essential oil and its major component using disc diffusion, agar dilution and gaseous contact methods. Received 28 January 2014 Revised 31 July 2014 Accepted 9 August 2014
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MATERIALS AND METHODS Plant material. Essential oil. The apricot fruits (P. armeniaca L. var. ansu Maxim.) were harvested from Gyeongju, Korea. Identification was confirmed by Prof. Seong-Soo Roh from the Department of Herbology, Daegu Haany University, Korea. A voucher specimen (no. AS12YM) has been deposited there. The air-dried and grounded seeds (300 g) were subjected to hydrodistillation in 1.5 L of water for 3 h in a Clevenger-type apparatus (Goheung Glass, Daegu, Korea; yield 0.27% w/w). Composition. The chemical composition of the apricot seed essential oil was determined by GC–MS using an Agilent 7890A GC in combination with an Agilent 5975C mass selective detector (Agilent Technologies, Santa Clara, CA, USA). The GC column was a DB-1 model (J&W Scientific, Folsom, CA, USA) with a length of 30 m, a diameter of 250 μm and film thickness of 0.25 μm. The carrier gas was helium at a flow rate of 1 mL/min. The oven temperature was programmed as follows: initial temperature of 50 °C for 2 min, then gradually increased to 280 °C at 10 °C/min and held for 5 min. The injector temperature was 250 °C, and the diluted sample (1/100, in CH2Cl2) was injected using a split mode (10:1). The components were identified by comparing their relative retention times and mass spectra with those of the standards and W9N08 library data of the GC–MS system. Benzaldehyde standard was purchased from Sigma-Aldrich (St. Louis, MO, USA).
Microbial strains. The essential oil and component were tested against 18 microorganisms of clinical importance. Reference strains were Bacillus cereus ATCC 27348, Enterococcus faecalis ATCC 29212, S. aureus ATCC 29213, Staphylococcus epidermidis ATCC 12228, Citrobacter freundii ATCC 6750, Enterobacter aerogenes ATCC 13048, Enterobacter cloacae ATCC 27508, E. coli ATCC 25922, Klebsiella pneumoniae ATCC 10031, P. mirabilis ATCC 25933, Pseudomonas aeruginosa ATCC 27853, Salmonella typhimurium ATCC 14028, Serratia marcescens ATCC 27117, Shigella sonnei ATCC 11060, C. albicans ATCC 10231 and Malassezia furfur ATCC 14521. Clinical strains were methicillin-resistant S. aureus (MRSA) P15 and P. aeruginosa D24 isolated from the Severance Hospital in Seoul.
Culture agar media. Mueller Hinton agar (Difco, Detroit, MI, USA), Sabouraud dextrose agar (Oxoid, Basingstoke, UK) and modified Dixon agar were used for bacteria, C. albicans and M. furfur, respectively. Antimicrobial activities for bacteria were determined after incubation at 35 °C for 24 h, at 30 °C for 48 h for C. albicans and at 32 °C for 72 h for M. furfur.
and 106 CFU/mL of yeast was spread on the agar plates. Sterile paper discs (8 mm in diameter; Advantec Toyo, Tokyo, Japan) were impregnated with 3 mg of the oil or component and placed on the inoculated agar surface (one disc per Petri dish). The diameter of the inhibition zones was measured after incubation. The positive controls (10 μg) were gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. All tests were repeated independently at least three times. Determination of the minimum inhibitory concentration and minimum bactericidal/fungicidal concentration by agar dilution. The agar dilution method was carried out as described previously (Hammer et al., 1999) with certain modifications. Mueller Hinton agar and Sabouraud dextrose agar were supplemented with 0.5% (v/v) Tween 20 (Sigma-Aldrich) to enhance the solubility of the oil or component. The agar plates were inoculated with the suspensions of bacteria and C. albicans (104 CFU/spot) and M. furfur (103 CFU/spot) using a microinoculator (Sakuma, Tokyo, Japan). The minimum inhibitory concentration (MIC) (μg/mL) was defined as the lowest concentration within the range of 125–16 000 μg/mL at which no growth was visible. To determine the minimum bactericidal/fungicidal concentration (MBC/MFC), a sample swab was taken from the inoculation spots having no visible growth and streaked on the growth agar without any inhibitory substance. The MBC/MFC (μg/mL) represents the lowest concentration at which the inoculated organism was completely killed. All of the assays were repeated independently at least three times. The inoculated plates without oil or compound were used as negative controls. The positive controls were gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively.
Determination of the minimum inhibitory dose by gaseous contact. The antimicrobial activity of the essential oil vapour phase was estimated by the method of Inouye et al. (2001). The plates were inoculated as described in MIC determination and then placed in 1.1-L airtight stainless-steel boxes (Carnation Co., Kimpo, Korea). Serial two-fold dilutions of the oil or component ranging from 1.65 to 846 mg/mL were made in ethyl acetate, and 260 μL of each dilution was soaked on filter paper (90 mm in diameter) to give final concentrations of 0.39 to 200 mg/L air space. After incubation, the minimum inhibitory dose (MID) (mg/L air space) was defined as the lowest inhibitory dose of the oil or component inhibiting visible growth.
RESULTS AND DISCUSSION Chemical composition of the essential oil
Disc diffusion method. The agar disc diffusion test was performed on the basis of the methods from the literature (Hernández et al., 2005). Briefly, plates were prepared in Petri dishes (with an inner diameter of 85.6 mm). Then, 0.1 mL from a cell suspension containing 108 colony-forming units (CFU)/mL of bacteria Copyright © 2014 John Wiley & Sons, Ltd.
Gas chromatography–mass spectroscopy analysis resulted in the identification of three compounds accounting for 99.9% of the total oil. Benzaldehyde was the predominant compound (90.6%), followed by mandelonitrile (5.2%) and benzoic acid (4.1%) (Fig. 1). Phytother. Res. 28: 1867–1872 (2014)
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Figure 1. Gas chromatography–mass spectroscopy chromatogram of the apricot seed essential oil.
Similar results were previously reported for the essential oil of cherry laurel (Prunus laurocerasus) leaves, which consisted of benzaldehyde (82.1%), mandelonitrile (15.4%), benzoic acid (1.12%) and 2-hexenal (0.63%) (Lazić et al., 2009). The plum seed (P. domestica) oil had benzaldehyde as a major volatile component but consisted of 50 or more volatile compounds (PićurićJovanović and Milovanović, 1993). Benzaldehyde was
also found in the pulp and skin of P. armeniaca (Takeoka et al., 1990; Guillot et al., 2006). The high benzaldehyde content in apricot seed essential oil is probably due to an increase in the contact between amygdalin and β-glucosidase that was caused by disruption of the seed cell wall that occurred in the course of sample grinding (Tunçel et al., 1998). The essential oil of the apricot seed could serve as a source of benzaldehyde. Mandelonitrile
Table 1. In vitro antimicrobial activity of apricot seed essential oil and its major component, benzaldehyde, by disc diffusion method Inhibition zone diameter (mm)a Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15c Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24c Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Benzaldehyde (3 mg)
Positive controlb (10 μg)
9.6 8.8 ti ti ti
9.9 15.4 ti ti 11.9
23.9 10.1 0.0 21.2 29.4
0.0 0.0 0.0 ti 9.5 0.0 ti ti ti 15.8 ti
0.0 0.0 0.0 11.7 9.1 0.0 38.6 21.8 10.1 9.0 11.5
19.3 18.0 21.1 21.5 23.1 20.8 20.6 11.7 19.1 22.7 19.2
ti ti
13.8 ti
13.6 19.7
Apricot seed essential oil (3 mg)
ti, total growth inhibition (see Materials and methods). The diameter of paper discs (8 mm) is included. b Gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. c Gentamicin-resistant clinical isolates. a
Copyright © 2014 John Wiley & Sons, Ltd.
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Table 2. MIC and MBC/MFC (μg/mL) of apricot seed essential oil and its major component, benzaldehyde Apricot seed essential oil Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15b Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24b Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Benzaldehyde
Positive controla
MIC
MBC/MFC
MIC
MBC/MFC
MIC
MBC/MFC
2000 4000 500 500 250
4000 8000 1000 1000 250
2000 4000 1000 1000 1000
4000 16 000 1000 1000 2000
0.25 8 32 0.25 0.13
0.25 8 32 0.25 0.13
2000 2000 1000 500 2000 2000 500 500 500 1000 500
4000 4000 2000 2000 4000 4000 1000 1000 2000 2000 2000
2000 2000 1000 1000 2000 4000 1000 1000 2000 2000 1000
4000 4000 2000 1000 2000 4000 2000 2000 8000 4000 2000
0.5 0.5 0.25 0.5 0.25 0.25 1 16 0.5 0.5 0.5
0.5 0.5 0.25 0.5 0.25 0.25 1 16 0.5 0.5 0.5
1000 250
2000 1000
2000 500
4000 2000
0.5 2
0.5 2
The MICs of gentamicin for E. faecalis ATCC 29212, S. aureus ATCC 29213, E. coli ATCC 25922 and P. aeruginosa ATCC 27853 were within the quality control ranges established by Clinical and Laboratory Standards Institute (2013). MIC, minimum inhibitory concentration; MBC/MFC, minimum bactericidal/fungicidal concentration. a Gentamicin, amphotericin B and ketoconazole for bacteria, C. albicans and M. furfur, respectively. b Gentamicin-resistant clinical isolates.
and benzoic acid were also detected as minor components of the oil. Although these compounds have been found in the seeds and stones of several Prunus species (Chandra and Nair, 1993; Pićurić-Jovanović and Milovanović, 1993; Khallouki et al., 2012), the specific content has not been established in the seed essential oil. Mandelonitrile is the reaction intermediate in the decomposition of amygdalin to benzaldehyde and hydrogen cyanide. Benzoic acid is generated by the oxidation of benzaldehyde. Other volatile compounds, such as linalool, which were previously shown to present in the pulp and skin of the apricot (Takeoka et al., 1990), were not detected in the seed essential oil. Benzyl alcohol, a major volatile component in the plum seed oil (Pićurić-Jovanović and Milovanović, 1993), was also not detected. Antimicrobial activity The results of the disc diffusion assay are presented in Table 1. The essential oil of the apricot seed exhibited a variable degree of antimicrobial activity against the 16 bacteria and two yeast species tested. Interestingly, complete inhibition of growth (a clear plate) was observed in three of the five Gram-positive bacteria, five of the 11 Gram-negative bacteria and both of the two yeast species (total inhibition). Weak activity or inactivity was observed against the other strains tested (≤15.8 mm). No obvious difference in susceptibility was found between Gram-positive and Gram-negative bacteria. Benzaldehyde, the major component of the oil, exhibited maximum activity against S. aureus strains including gentamicin-resistant MRSA (total inhibition). Copyright © 2014 John Wiley & Sons, Ltd.
Table 3. In vitro antimicrobial activity of apricot seed essential oil and its major component, benzaldehyde, by gaseous contact MID (mg/L air)
Organism Gram-positive Bacillus cereus Enterococcus faecalis MRSA P15a Staphylococcus aureus Staphylococcus epidermidis Gram-negative Citrobacter freundii Enterobacter aerogenes Enterobacter cloacae Escherichia coli Klebsiella pneumoniae Proteus mirabilis Pseudomonas aeruginosa P. aeruginosa D24a Salmonella typhimurium Serratia marcescens Shigella sonnei Yeast Candida albicans Malassezia furfur
Apricot seed essential oil
25 50 12.5 12.5 25
Benzaldehyde
12.5 25 25 25 50
25 25 25 12.5 50 25 12.5 12.5 12.5 25 12.5
50 50 50 50 50 100 25 25 100 100 50
12.5 3.13
100 25
MIDs of ≤6.25, 12.5–50 and ≥100 mg/L air were regarded as high, moderate and weak activities, respectively (Inouye et al., 2001). MID, minimum inhibitory dose. a Gentamicin-resistant clinical isolates. Phytother. Res. 28: 1867–1872 (2014)
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The remaining strains were less susceptible to benzaldehyde (≤38.6 mm). For essential oils, the result of the disc diffusion method does not exactly reflect the antimicrobial effectiveness owing to the differences in the diffusion ability of the oils through the agar and the evaporation (Hernández et al., 2005). Thus, the MIC and MBC/MFC values of the essential oil were also determined. The MIC ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 250–4000, 500–2000 and 250–1000 μg/mL, respectively (Table 2). The MBC/MFC ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 250–8000, 1000–4000 and 1000–2000 μg/mL, respectively. The results of MIC and MBC/MFC indicated that the essential oil had low antimicrobial activity, as judged by the criteria suggested previously (Ríos and Recio, 2005). The MIC and MBC/MFC values of the oil were equal to or lower than those of benzaldehyde. The MIC range of benzaldehyde was 1000–4000 μg/mL, except M. furfur. Several studies previously reported comparable levels of MIC (>1000 μg/mL) against Bacillus subtilis, E. faecalis, S. aureus, E. coli and P. aeruginosa, among others (Kang et al., 1992; Chang et al., 2001). It is noticeable that the essential oil of apricot seed showed the same activity against gentamicin- and methicillin-susceptible S. aureus and gentamicin-resistant MRSA strains. It also showed the same activity against gentamicin-resistant P. aeruginosa and gentamicinsusceptible P. aeruginosa strains. The essential oils exert antimicrobial activity through gaseous contact as well as direct contact with microorganisms.
The antimicrobial activity of the apricot seed essential oil by gaseous contact is shown in Table 3. The MID ranges for the Gram-positive bacteria, Gram-negative bacteria and yeast strains were 12.5–50, 12.5–50 and 3.13-12.5 mg/L air, respectively. E. faecalis and K. pneumoniae displayed the weakest susceptibility (MID 50 mg/L air). M. furfur was the most susceptible among the microorganisms tested (MID 3.13 mg/L air). The essential oil of apricot seed showed the highest activity against M. furfur and moderate activity against the other species, as judged by the values defined previously (Inouye et al., 2001). The MID values of benzaldehyde were comparable with or higher than those of the apricot seed essential oil.
CONCLUSION The results of this study suggest that the essential oil of the apricot seed could be a source of benzaldehyde. The essential oil of apricot seed possesses antimicrobial activity against a range of bacteria and yeasts. The essential oil has potential usage as an air disinfectant, preservative and antimicrobial agent. Additional study will be needed to assess the potential toxicity.
Conflict of Interest The authors declare that there is no conflict of interest.
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