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Evaluation of Combined Antibacterial Effects of Eugenol, Cinnamaldehyde, Thymol, and Carvacrol Against E. Coli with an Improved Method

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Evaluation of Combined Antibacterial Effects of Eugenol, Cinnamaldehyde, Thymol, and Carvacrol Against E. Coli with an Improved Method See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/38072806 Evaluation of Combined Antibacterial Effects of Eugenol, Cinnamaldehyde, Thymol, and Carvacrol against E. coli with an Improved Method ARTICLE in JOURNAL OF FOOD SCIENCE · SEPTEMBER 2009 Impact Factor: 1.7 · DOI: 10.1111/j.1750-3841.2009.01287.x · Source: PubMed CITATIONS READS 82 443 4 AUTHORS, INCLUDING: Ruisong Pei Bao-Ping Ji University of Wisconsin–Madison China Agricultural University 12 PUBLICATIONS 232 CITATIONS 18 PUBLICATIONS 244 CITATIONS SEE PROFILE SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Ruisong Pei letting you access and read them immediately. Retrieved on: 20 February 2016 JFS M: Food Microbiology and Safety Evaluation of Combined Antibacterial Effects of Eugenol, Cinnamaldehyde, Thymol, and Carvacrol against E. coli with an Improved Method RUI-SONG PEI,FENG ZHOU,BAO-PING JI, AND JING XU ABSTRACT: In this study, the antibacterial activities of eugenol, cinnamaldehyde, thymol, carvacrol, and their combinations against E. coli were investigated separately. First, broth macro-dilution assay was adopted to deter- mine the minimal inhibitory concentration (MIC) of the 4 components. Second, the combination testing was per- formed using chequerboard method. Finally, the combined effects were evaluated with an improved method, which was based on the indices of fractional inhibitory concentration (FIC) and Effect of the Combination (EC) jointly. The results indicated that MICs of the 4 components were 1600, 400, 400, and 400 mg/L, respectively; treatments with cinnamaldehyde/eugenol, thymol/eugenol, carvacrol/eugenol, and thymol/carvacrol revealed synergistic ef- fects according to the 2 indices. By means of combination, MICs of eugenol, cinnamaldehyde, thymol, and carvacrol decreased to 400, 100, 100, and 100 mg/L, respectively. Consequently, the negative impacts of unpleasant smell of these 4 components could be minimized, making it possible to add them to foods as preservatives. In addition, this improved evaluation method provided a more accurate and comprehensive way to evaluate combined effects. Keywords: antibacterial activity, E. coli, essential oils component, evaluation method, synergism & Safety M: Food Microbiology Introduction EOs in semiskimmed milk (Karatzas and others 2001) and tenfold he antibacterial effects of essential oils (EOs) and their compo- more in pork liver sausage (Pandit and Shelef 1994). T nents have been examined recently. It has been reported that To enhance the antimicrobial activities, the EOs components the essential oils of the oregano and thyme were effective against have been used in combination with other antibacterial agents and strains of E. coli (Dorman and Deans 2000). The major antibacte- a variety of treatments. Karatzas and others (2000) reported that the rial components of these oils are carvacrol and its isomer thymol combined effects of carvacrol, cinnamaldehyde, and thymol with (Burt and others 2005). Studies have shown that the essential oils of mild heat treatment could reduce the viability of L. monocytogenes. thyme and clove are effective against Listeria monocytogenes (Singh Ettayebi and others (2000) found that the combination of nisin and and others 2003). The inhibitory effects of thyme and basil EOs, car- thymol could effectively control the foodborne pathogenic bacte- vacrol, and thymol toward Shigella sonnei and Shigella flexneri were ria, so that the required concentration of nisin and tymol would investigated (Bagamboula and others 2004). Other researchers re- be decreased. Other methods were also reported in previous stud- ported the antimicrobial effects of carvacrol, cinnamaldehyde, and ies, including combined with modified atmosphere (Chouliara and thymol on growth of Bacillus cereus (Valero and Giner 2005). others 2007), sodium citrate and monolaurin (Blaszyk and Holley An increasing number of people prefer natural and minimal 1998), and nisin and diglycerol fatty acid ester (Solomakos and oth- processed food products, which are regarded as safe and more ers 2008). However, it is hard to compare the results of these re- nutritional. Many EOs and their components, including eugenol, ports because researchers choose different methods to perform the cinnamaldehyde, thymol, and carvacrol, have been registered by combination testing and adopt various indices to evaluate the re- the European Commission and are considered to present no risk sults, which leads to nonstandard outcomes (Fyfe and others 1998; to the health of customers (Burt 2004). Therefore, it is possible to Ettayebi and others 2000; Delaquis and others 2002). Thus, there is use them as preservatives to extend the shelf life of selected foods a clear need to develop an effective and standardized way to evalu- considering their safety and antimicrobial activities. However, the ate and quantify the synergistic effects of EOs combination. organoleptic quality of foods could be affected by the taste of these The chequerboard method combined with fractional inhibitory components; besides, even greater addition is needed to achieve concentration (FIC) index is commonly used to test the antimicro- the same effect in foods, because the antimicrobial effects would bial abilities of drugs in medicine. Many researchers have also used be weakened in some particular situations (Shelef 1983; Smid and this method to study the antimicrobial abilities of EOs (Shin and Gorris 1999). For instance, it would need more than twofold more Kang 2003; Filoche and others 2005; Si and others 2008). In our previous studies, we tested the combined effects of components themselves or with chelator and organic acids against Salmonella MS 20090150 Submitted 2/19/2009, Accepted 6/17/2009. Authors are with typhimurium using the EC index (Zhou and others 2007a, 2007b). College of Food Science and Nutritional Engineering, China Agricultural Therefore, based on the previous reports, we tried to use these 2 in- Univ., 17 Qinghua Donglu, Haidian District, Beijing, China. Direct in- quiries to author Zhou (E-mail: [email protected]). dices jointly to develop a more comprehensive way to quantify the synergistic effects of EOs combination. C 2009 Institute of Food Technologists R Vol. 74, Nr. 7, 2009—JOURNAL OF FOOD SCIENCE M379 doi: 10.1111/j.1750-3841.2009.01287.x Further reproduction without permission is prohibited An improved evaluation method of combination effects . Eugenol, cinnamaldehyde, thymol, and carvacrol were 4 com- suspensions and aliquots of 1 mL of each component at a concen- monly used antibacterial components of the EOs of clove, tration of 4 times the targeted final concentration were dispensed cinnamon, oregano, and thyme (Demo and others 2001; Kwon and in the tubes. One tube with 4 mL of MHB without adding any com- others 2003; Valero and Giner 2005). The major objective of this ponents was set as control. The experiment was carried out at least study was to investigate the separate and combined antibacterial thrice. The MICs were determined as described previously. activities of these 4 components against E. coli; furthermore, an im- Two kinds of indices were adopted to evaluate the interactions. proved method was developed to evaluate and quantify synergistic The FIC, which is the sum of the FICs for each component; and combinations. the FIC is calculated as follows: for component A the FIC equals the MIC of component A in combination divided by the MIC of compo- Materials and Methods nent A alone. The interactions are considered synergistic if the FIC index is less than 1, additive if the FIC is equal to 1, indifferent if the Bacterial strains and growing conditions FIC index is between 1 and 2, and antagonistic if the FIC index is E. coli CGMCC 1.487 (obtained from China General Microbio- greater than 2 (Franzot and Casadevall 1997). logical Culture Collection Center, Beijing, China) was maintained The EC, which was described in our previous studies (Zhou and on Mueller–Hinton agar (MHA) (Beijing Chemical Corp., Beijing, others 2007a) and the EC is calculated using the following formula: ◦ China) slants at 4 C. Cells were prepared by 16-h culture in Mueller ◦ –Hinton broth (MHB) (Beijing Chemical Corp.) at 37 C. EC = Log DPI − Log DPII A 16-h culture was diluted with MHB to achieve an inoculum of 6 1 × 10 CFU/mL approximately. The number of cells in the suspen- The Log DPI and Log DPII represented the Log DP of the combina- sions was estimated by duplicate plating from tenfold serial dilu- tion system and the single agent, respectively. tion on MHA and counting the colonies after incubation at 37 ◦C The synergistic effects of the combinations were determined for 24 h. based on 3 principles. (1) The decrease in populations (>90%): linked with the defini- < < − M: Food Microbiology EO components tion of DP,it was concluded that only when DP 0.1 (log DP 1) Cinnamaldehyde (≥98%) and eugenol (≥98%) were obtained that the combinations of various reagents had significant antibac- & Safety from Fluka (Buchs, Switzerland). Carvacrol (≥98%) and thymol terial activity. (≥99%) were obtained from Sigma (St. Louis, Mo., U.S.A.). Certain (2) When there was significant difference (analyzed by the one- amount of each component filter-sterilized (0.22-μm-pore filter; way analysis of variance [ANOVA]) between the antibacterial ac- Millipore Corp, Bedford, Mass., U.S.A.) was added to MHB to ob- tivity of the combination and
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