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Inactivation of Listeria monocytogenes inoculated on disposable plastic tray, aluminum foil, and paper cup by atmospheric pressure plasma
Food Control 21 (2010) 1182–1186
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Food Control journal homepage: www.elsevier.com/locate/foodcont
Inactivation of Listeria monocytogenes inoculated on disposable plastic tray, aluminum foil, and paper cup by atmospheric pressure plasma Hyejeong Yun a, Binna Kim a, Samooel Jung a, Zbigniew A. Kruk a,b, Dan Bee Kim c, Wonho Choe c, Cheorun Jo a,* a b c
Department of Animal Science and Biotechnology, Chungnam National University, Daejeon 305-764, Republic of Korea Department of Animal Science, School of Agriculture Food and Wine, The University of Adelaide, South Australia 5371, Australia Department of Physics, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Republic of Korea
a r t i c l e
i n f o
Article history: Received 21 September 2009 Received in revised form 25 January 2010 Accepted 2 February 2010
Keywords: Atmospheric pressure plasma Listeria monocytogenes Disposable plastic tray Aluminum foil Paper cup
a b s t r a c t The objective of this study was to investigate the effect of atmospheric pressure plasma (APP) on Listeria monocytogenes inoculated onto disposable food containers including disposable plastic trays, aluminum foil, and paper cups. The parameters considered in APP processing were input power (75, 100, 125, and 150 W) and exposure time (60, 90, and 120 s). The bacterial reduction in the disposable plastic trays, aluminum foil, and paper cups was associated with increased input power and exposure time of APP. The D10 values were calculated as 49.3, 47.7, 36.2, and 17.9 s in disposable plastic trays, 133, 111, 76.9, and 31.6 s in aluminum foil and 526, 65.8, 51.8, and 41.7 s in paper cups at 75, 100, 125, and 150 W of input power, respectively. There were no viable cells detected after 90 and 120 s of APP treatment at 150 W in disposable plastic trays. However, only three decimal reductions of viable cells were achieved in aluminum foil and paper cups at 150 W for 120 s. These results demonstrate that APP treatment is effective for inactivation of L. monocytogenes and applicable for disposable food containers. However, the type of material is crucial and appropriate treatment conditions should be considered for achieving satisfactory inactivation level. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Food safety is the most critical issue for both consumers and the food industry. Contamination of foods by pathogens induces an enormous social and economical burden on health care. Escherichia coli, Salmonella typhimurium, Staphylococcus aureus, Listeria monocytogenes, and Enterococcus faecalis are general food-borne pathogens that cause severe diseases and in some cases even death. It has been estimated that in the Unites States alone food-borne diseases cause 76 million illnesses, 325,000 hospitalizations and 5000 deaths each year (Mead et al., 1999). Recent reports from the World Health Organization (WHO) have also concluded that the incidence of food-borne diseases is a growing public health problem in both developed and developing countries (WHO, 2007). Several studies have suggested that various bacteria, such as E. coli, S. aureus, and Salmonella. spp., survive not only in food but also on hands, sponges, clothes, and disposable food containers (Jiang & Doyle, 1999; Kusumaningrum, Putten, Rombouts, & Beumer, 2002). In another study, survival of food-borne pathogens
* Corresponding author. Tel.: +82 42 821 5774; fax: +82 42 825 9754. E-mail address: [email protected] (C. Jo). 0956-7135/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2010.02.002
was detected at a level of 105 CFU/cm2 on stainless steel surfaces (Kusumaningrum, Ridoldi, Hazeleger, & Beumer, 2003). There are several traditional decontamination methods and they can be divided into thermal and non-thermal sterilization. Thermal sterilization can inactivate pathogens efficiently but induces side-effects in the sensory, nutritional, and functional properties of food. Therefore, it cannot be applied to some foods or materials. Moreover, food containers may be also impacted by thermal treatment. To overcome these disadvantages, non-thermal sterilization methods were developed and used including chemical treatment (Jane, Kang, Michael, Stuart, & Valgene, 2008), ultra violet (Shama, 2007), irradiation (Aziz & Moussa, 2002), high pressure (Garcia-Gonzalez et al., 2007), etc. However, these processes also have certain disadvantages which include high costs of application, requirements for specialized equipments, generation of undesirable residues, extended processing time, and lower efficiency (Brendan & Joseph, 2008). Irradiation is known as one of the best non-thermal sterilization methods to destroy pathogenic and spoilage microorganisms but may induce side-effects such as lipid oxidation, off-flavor, and loss of nutritional and sensory quality of food. In addition, this technology needs special facilities and more consumer acceptance. High pressure processing has also been successfully applied in food processing but has limitations in batch
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size processing and affects the quality of the product (Kruk et al., 2009). Plasma is an electrically energized state of matter and can be generated by electrical discharge (Bogaerts, Neyts, Gijbels, & Mullen, 2002). Utilization of non-thermal plasma discharges at pressures at or near 1 atm in the ambient condition makes the decontamination process practical and inexpensive. In addition, the fact that the gas temperature in such discharges remains relatively low makes their use suitable for heat-sensitive products. Recently, atmospheric pressure plasma (APP) has been applied to the deposition, coating, synthesis, metallurgy, and etching of thin film etc. (Gomez et al., 2009). The highly reactive free radicals (OH, H2O) and H2O2 produced during APP process are known to play a major role in the inactivation of bacteria (Gilliland & Speck, 1967; Gweon, Kim, Moon, & Choe, 2009). Reactive oxygen species affect bacterial membrane lipids by causing the formation of unsaturated fatty acid peroxides. Oxidation of amino acid and nucleic acids may also cause changes that result in microbial death or injury. Therefore, APP is introduced as a new sanitizing technology in the field of food processing. APP processing was effective to inactivate microorganisms in hard solid foods including nuts and soft foods including apples and lettuce (Brendan & Joseph, 2008). Recently, Song et al. (2009) reported that APP was effective to inactivate L. monocytogenes inoculated on sliced ham and cheese. Moon et al. (2009) suggested that APP of 4 mA conduction current and 60 °C gas temperature condition was obtained at input power 100 W using helium gas and that it could be safely applied to human skin without electrical and thermal damages. However, evidence of effectiveness on inactivation of pathogens in different foods or food containers is still very limited. The objective of this study was to investigate the inactivation effect of APP on L. monocytogenes inoculated on disposable plastic trays, aluminum foil, and paper cups, which are all commonly used for food preparation and serving. 2. Materials and methods 2.1. Samples preparation Disposable plastic trays (polystyrene), aluminum foil, and paper cups (pulp) were purchased from a local market located in Daejeon, Korea in November 2008. The samples were cut into dimensions (length x width) of 60 6 mm, then packed into a polyethylene pouch. To sterilize the samples, 35 kGy of gamma irradiation (AECL, IR-79, MDS Nordion International Co. Ltd., Ottawa, ON, Canada) was applied at the Advanced Radiation Technology Institute, Jeongeup, Korea. The source strength was approximately 320 kCi with a dose rate of 20 kGy/h at 10 ± 0.5 °C.
was uniformly and aseptically inoculated on the disposable plastic trays, aluminum foil, and paper cups, respectively. The samples were sealed in a polyethylene bag and incubated at 10 °C for 1 h to facilitate the attachment of microorganisms to the samples. 2.3. Treatment by atmospheric pressure plasma (APP) The plasma generator used in the experiment was a capacitively-coupled large area system (dimensions: 110 mm 15 mm) and consisted of a powered rod electrode covered by a dielectric material located in a grounded case, and a bottom ground electrode that was placed under the powered electrode and used as a base for material treatment (Fig. 1). The electrode was powered by a 13.56 MHz rf supply through an impedance matching network. Helium gas with a fixed flow rate of 4 lpm (liter per minute) was introduced for stable plasma generation. The input powers in this study were 75, 100, 125, and 150 W and the exposure times were 30, 60, 90, and 120 s. For plasma treatment, inoculated samples were placed on the bottom conductor and were in direct contact with the plasma at room temperature. The gap distance between the powered electrode and the treatment surface was maintained at 6 mm. Inoculated samples without plasma treatments were also prepared as a control. After plasma treatment, the samples were immediately stored at commercial storage conditions (25 °C) and microbial analysis was performed. 2.4. Microbiological analysis After APP treatment, samples were vortexed with sterile saline solution (NaCl, 0.85%) for 5 min. The samples for the microbiological count were prepared in a series of decimal dilutions utilizing sterile saline solution. The media used for L. monocytogenes was tryptic soy agar (Difco, Laboratories, Detroit, MI, USA). Each diluent (100 l) was spread in triplicate on each agar plate and the plates were incubated at 25 °C for 48 h, after which the colony formation units (CFU) per gram were calculated. 2.5. Statistical analysis Three independent trials were conducted with two samples for treatment combination per each trial in the experiment. One-way Analysis of Variance (ANOVA) was performed, and when significant differences were detected the differences among the mean values were identified by Duncan‘s multiple range test using SAS software with a confidence level of P < 0.05 (SAS, Release 8.01, SAS Institute Inc., Cary, NC). Mean values and standard errors of the mean are reported.
Dielectric
2.2. Inoculation Three strains of L. monocytogenes (ATCC 19114, 19115, and 19111) were obtained from a Korean Culture Center of Microorganisms (KCCM, Seoul, Korea). Each strain was cultured in a tryptic soy broth (Difco, Laboratories, Detroit, MI, USA) at 25 °C for 24 h. At the stationary-phase, a culture of three strains of L. monocytogenes were transferred aseptically to a 50 ml centrifuge tube and were vortexed for 10 s to ensure a homogenous cocktail. Then, L. monocytogenes were centrifuged (1950g for 10 min at 4 °C) in a refrigerated centrifuge (VS-5500, Vision Scientific Co., Seoul, Korea). The pellet was washed twice with sterile saline (0.85%), and suspended in saline to a final concentration of approximately 109 CFU/ml of the stock cocktail inoculum. The test culture suspension (100 ll)
Powered electrode
RF source
Plasma
Sample
Fig. 1. Diagrammatic representation of plasma generator.
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3. Results and discussion
3.2. Effects of APP on L. monocytogenes during storage
3.1. Effects of APP input power on L. monocytogenes survival
Table 2 shows the reduction of L. monocytogenes inoculated on disposable plastic trays, aluminum foil, and paper cups with different input power (W) and exposure time (s) during storage at 25 °C. Results show that the higher input power of APP was more effective in inactivation of L. monocytogenes at even shorter exposure times. Inactivation of L. monocytogenes was influenced more by power (W) than by exposure time (s) on disposable plastic trays. The input power of 75 W resulted in only two decimal reductions of L. monocytogenes after 120 s, but 150 W resulted in elimination of the pathogen (Table 2). APP treatment with 125 W for 60 s or longer showed approximately a two decimal reduction, but after storage for 3 days at 25 °C the viable cell number decreased to undetected levels. After 6 days, the viable cells were reduced below the detection limit with APP treatment of 100 W for 90 s (data not shown). This may be accounted for by the presence of a posttreatment effect wherein the APP damaged cells could not recover. The L. monocytogenes inoculated on aluminum foil and paper cups showed more resistance by APP treatment in this study. In aluminum foil, APP treatment with up to 100 W resulted in only one decimal reduction, and the decrease of the viable cell number was very limited after 3 days (Table 2), and even after 6 days (data not shown). APP treatment of aluminum foil with 150 W for 120 s showed three decimal reductions in L. monocytogenes. In the case of paper cups, 2–3 decimal reductions were achieved by APP at 100, 125, and 150 W for 150 s. However, APP treatment with 75 W was not effective for inactivation of microorganisms. Generally, the inactivation trend of paper cups was similar to aluminum foil. During the plasma process, the formation of an oxygen functional group occurs at the surface of treated materials through the interaction between the active species from the plasma and the surface atoms (Guruvenket, Mohan Rao, Komath, & Raichur, 2004). In plasma-solid interactions, the surface of material may be chemically and physically modified by plasma processing (Pykonen et al., 2008). The membrane surface can be changed by different functional groups. In particular the groups responsible for surface hydrophilicity such as peroxide, carboxylic acid, ketone/aldehyde and ester groups can be generated and activated by plasma on the surfaces (Lai et al., 2006; Weibel, Vilani, Habert, & Achetee, 2006). Guruvenket et al. (2004) reported that plasma-treated polystyrene increased ion density and transformed to a hydrophilic state through an increase of plasma power (Guruvenket et al., 2004). Polystyrene, the major material ingredient in disposable plastic trays, comprises of saturated hydrocarbons and can be easily attacked by the reactive species in the plasma (Araya, Yuji, Watanabe, Kashihara, & Sumida, 2007). Wang, Wu, and Li (2008) reported that the inactivation efficiency of microorganisms in polystyrene decreased with the addition of sodium carbonate, whereas it increased with the addition of ferrous sulfate. The carbonate pigment coated on paper cups may be one of the reasons for the lower efficiency of inactivation of L. monocytogenes inoculated on paper cups by APP. Recently, the inactivation of food-borne microorganisms by plasma treatment has been reported. Deng, Ruan, Mok, Huang, and Chen (2007) showed that the number of E. coli 12955 on almonds was reduced by log 5 after 30 s of non-thermal plasma at 30 kV and 2 kHz. Critzer, Kelly-Wintenberg, South, and Golden (2007) reported that reductions of 2–5 log were obtained in OAUGDP treatment of 2–5 min in E. coli O157:H7, Salmonella enteriridis, and L. monocytogenes on Red Delicious apples. Cold atmospheric plasma treatment (12 kV) reduced the number of Pantoea agglomerans and Gluconacetobacter liquefaciens on mango and melon to below the detection limit after 2.5 s. However, E. coli required 5 s to reach the same level of inactivation and Saccharomyces cerevisiae was the most resistant and required 10 and 30 s in mango
The sensitivity of APP treatment of L. monocytogenes inoculated on the surface of disposable plastic trays, aluminum foil, and paper cups are shown in Table 1. Calculated D10 values, the exposure time required to inactivate 90% of a population from the survival curves, demonstrated a decreasing trend with the increased input power in all of the materials tested. Initially, the highest D10 values with input power of 75 W were observed on paper cups followed by aluminum foil and disposable plastic trays (Table 1). The increased input power from 75 to 100 W reduced the D10 values from 49.3 and 133 s to 47.6 and 111 s on the plastic trays and aluminum foil, respectively, and from 526 to 65.8 s on the paper cups. When the input power was further raised to 150 W the D10 values for disposable plastic trays, aluminum foil and paper cups were reduced to 18.0, 31.6, and 41.7 s, respectively. These results clearly suggest that the efficiency of plasma treatment on L. monocytogenes is highly dependant on surface characteristics of the serving/storage material. Kayes et al. (2007) reported that one atmosphere uniform glow discharge plasma (OAUGDP) treatment resulted in D10 values of 22, 22, and 51 s in S. flexneri, V. parahaemolyticus, and E. coli O157:H7 at pH 7.0 agar, respectively. However, in agar with pH 5.0, D10 values were 19 and 31 s in V. parahaemolyticus and S. enteritidis, respectively. Ben Gadri et al. (2000) observed D10 values for E. coli K12 at 6, 33, and 70 s on polypropylene, glass, and agar, respectively. It seems that D10 values for these incubated agar plates depended strongly on pH among other surface characteristics. A longer plasma exposure time was also required to achieve the same inactivation level for dried cultures or cultures embedded within agar plugs (Ben Gadri et al., 2000). Bacteria in agar require a longer penetration time for the antimicrobial active species to diffuse to them in the porous medium (Montie, Kelly-Winternberg, & Roth, 2000). Recently Song et al. (2009) also pointed out the significantly different effect in inactivation of L. monocytogenes that were inoculated in ham and cheese. The authors indicated that it is possibly due to the sliced ham surface being a little rough compared with the smooth surface of the sliced cheese, so the intricate webbing on the surface of sliced ham provided numerous sites for L. monocytogenes to attach and potentially evade antimicrobial treatment. Park et al. (2008) reported that microwave-induced argon plasma treatment completely sterilized in less than 7 s the silk fabrics inoculated with various strains of either bacteria or fungi. Bacillus subtilis, Aspergillus niger, Bacillus stearothermophilus, and Saccharomyces cerevisiae with an initial spore density of 2.0 104 CFU/cm2 can easily be inactivated within less than one second of plasma treatment without forming dangerous or even toxic products that would contaminate the food packaging material, polyethylene terephthalate (PET) foils (Feichtinger, Schulz, Walker, & Schumacher, 2003).
Table 1 Calculated D10 valuesa (s) for Listeria monocytogenes inoculated on different food containers by atmospheric pressure plasma. Input power (W)
75 100 125 150
D10 value Disposable plastic tray
Aluminum foil
Paper cup
49.3 47.6 36.2 18.0
133 111 76.9 31.6
526 65.8 51.8 41.7
a D10 value is described as the time necessary to reduce the population of cells one log or 90%. The values were determined from plots of the number of survivors versus time (s).
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Table 2 Effects of atmospheric pressure plasma on Listeria monocytogenes (log CFU/g) inoculated on disposable plastic trays, aluminum foil and paper cups during storage at 25 °C. Input power (W)
Exposure time (s)
Disposable plastic tray
Aluminum foil
Paper cup
Storage (day) 0
SEMe
3 aw
bx
0
3 x
x
SEMe
0
3
SEMe
75
0 30 60 90 120 SEMf
6.79 6.07ax 5.26ay 4.49z 4.54z 0.165
5.28 5.11bxy 4.58by 4.63yz 4.47z 0.132
0.146 0.084 0.195 0.099 0.156
7.13 6.97ax 6.86axy 6.47ayz 6.26az 0.125
6.54 6.21bxy 5.92byz 5.74bz 5.61bz 0.092
0.220 0.162 0.076 0.092 0.045
6.51 6.50 6.31a 6.43a 6.23 0.291
6.04 6.32 5.34b 5.21b 5.28 0.310
0.228 0.124 0.060 0.087 0.263
100
0 30 60 90 120 SEMf
6.79aw 5.40ax 4.76ay 4.38az 4.16az 0.100
5.28bw 4.12bxy 4.31ax 3.67byz 3.50bz 0.148
0.146 0.088 0.156 0.152 0.231
7.13w 6.58x 6.19ay 6.09ayz 6.02az 0.039
6.54x 6.16xy 5.71byz 5.60bz 5.51bz 0.133
0.220 0.134 0.087 0.022 0.042
6.51x 6.02x 5.77x 5.72x 4.46y 0.276
6.04x 5.92x 5.41xy 5.46xy 4.72y 0.263
0.228 0.201 0.296 0.143 0.361
125
0 30 60 90 120 SEMf
6.79ax 4.93ay 4.37ay 3.57az 3.33az 0.173
5.28bx 3.58by NDbz NDbz NDbz 0.030
0.146 0.079 0.005 0.145 0.122
7.13w 6.56ax 6.02ay 5.66az 5.53az 0.063
6.54x 5.62by 5.54by 4.75bz 4.49bz 0.144
0.220 0.170 0.060 0.072 0.162
6.51ax 6.11axy 5.36y 4.50y 4.31y 0.292
6.04ax 5.36bxy 5.13y 4.25z 4.19z 0.181
0.228 0.092 0.045 0.420 0.074
150
0 30 60 90 120 SEMf
6.79aw 4.41ax 3.46ay NDz NDz 0.042
5.28bx NDby NDby NDy NDy 0.020
0.146 0.022 0.125 – –
7.13w 4.89x 4.77ax 4.51ay 4.04z 0.069
6.54x 4.38y 4.31byz 4.13byz 3.73z 0.158
0.220 0.190 0.090 0.110 0.120
6.51ax 6.02axy 5.20axy 4.32ay 3.66ay 0.476
6.04ax 5.15by 3.41bz 2.89az 2.15az 0.372
0.228 0.180 0.215 0.632 0.634
Values with different superscripts (a–d) within the same row and for the same material differ significantly (P < 0.05), values with different superscripts (w–z) within the same column for the same material differ significantly (P < 0.05), eStandard errors of the mean (n = 6), f(n = 15), ND = viable cells were not detected with a detection limit at < 101 CFU/g.
and melon, respectively (Perni, Liu, Shama, & Kong, 2008). Atmospheric pressure glow discharge (APGD) treatment for 10 min achieved six decimal reductions on Bacillus subtilis spores at a sporulation temperature of 22 °C and 3.5 decimal reductions at 47 °C (Deng, Shi, & Kong, 2006a, 2006b). Therefore, the microorganism inactivation by plasma treatment can be dependent on different factors including plasma type, microorganism, culture age, exposure power, temperature, pH, exposure time, composition of the media, and material type. The risk of food-borne pathogens is mainly associated with crosscontamination, level of contamination on the surfaces, and the probability of its transfer to food. Perni et al. (2008) suggested that cold atmospheric gas plasmas have potential in decontaminating the skins of soft fruits and it seems feasible when the plasmas generated are scaled up to industrial level (Shi, Liu, & Kong, 2007). In this study, it has been concluded that APP treatment has great potential for inactivation of L. monocytogenes on the surface of disposable food containers. However, different inactivation rates in different surface materials should be considered to achieve satisfactory results. Therefore, further work is required to develop an efficient APP treatment system that can be applied effectively in the food industry. Acknowledgement This work was supported by the Korea Rural Development Administration Fund. References Araya, M., Yuji, T., Watanabe, T., Kashihara, J., & Sumida, Y. (2007). Application to cleaning of waste plastic surfaces suing atmospheric non-thermal plasma jets. Thin Solid Films, 515, 4301–4307. Aziz, N. H., & Moussa, L. A. A. (2002). Influence of gamma-radiation on mycotoxin producing moulds and mycotoxins in fruits. Food Control, 13, 281–288. Ben Gadri, R., Reece Roth, J., Montie, T. C., Kelly-Wintenberg, K., Tsai, P. P. Y., Helfritch, D. J., et al. (2000). Sterilization and plasma processing of room
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Food Control journal homepage: www.elsevier.com/locate/foodcont
Inactivation of Listeria monocytogenes inoculated on disposable plastic tray, aluminum foil, and paper cup by atmospheric pressure plasma Hyejeong Yun a, Binna Kim a, Samooel Jung a, Zbigniew A. Kruk a,b, Dan Bee Kim c, Wonho Choe c, Cheorun Jo a,* a b c
Department of Animal Science and Biotechnology, Chungnam National University, Daejeon 305-764, Republic of Korea Department of Animal Science, School of Agriculture Food and Wine, The University of Adelaide, South Australia 5371, Australia Department of Physics, Korea Advanced Institute of Science and Technology, Daejeon 305-701, Republic of Korea
a r t i c l e
i n f o
Article history: Received 21 September 2009 Received in revised form 25 January 2010 Accepted 2 February 2010
Keywords: Atmospheric pressure plasma Listeria monocytogenes Disposable plastic tray Aluminum foil Paper cup
a b s t r a c t The objective of this study was to investigate the effect of atmospheric pressure plasma (APP) on Listeria monocytogenes inoculated onto disposable food containers including disposable plastic trays, aluminum foil, and paper cups. The parameters considered in APP processing were input power (75, 100, 125, and 150 W) and exposure time (60, 90, and 120 s). The bacterial reduction in the disposable plastic trays, aluminum foil, and paper cups was associated with increased input power and exposure time of APP. The D10 values were calculated as 49.3, 47.7, 36.2, and 17.9 s in disposable plastic trays, 133, 111, 76.9, and 31.6 s in aluminum foil and 526, 65.8, 51.8, and 41.7 s in paper cups at 75, 100, 125, and 150 W of input power, respectively. There were no viable cells detected after 90 and 120 s of APP treatment at 150 W in disposable plastic trays. However, only three decimal reductions of viable cells were achieved in aluminum foil and paper cups at 150 W for 120 s. These results demonstrate that APP treatment is effective for inactivation of L. monocytogenes and applicable for disposable food containers. However, the type of material is crucial and appropriate treatment conditions should be considered for achieving satisfactory inactivation level. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Food safety is the most critical issue for both consumers and the food industry. Contamination of foods by pathogens induces an enormous social and economical burden on health care. Escherichia coli, Salmonella typhimurium, Staphylococcus aureus, Listeria monocytogenes, and Enterococcus faecalis are general food-borne pathogens that cause severe diseases and in some cases even death. It has been estimated that in the Unites States alone food-borne diseases cause 76 million illnesses, 325,000 hospitalizations and 5000 deaths each year (Mead et al., 1999). Recent reports from the World Health Organization (WHO) have also concluded that the incidence of food-borne diseases is a growing public health problem in both developed and developing countries (WHO, 2007). Several studies have suggested that various bacteria, such as E. coli, S. aureus, and Salmonella. spp., survive not only in food but also on hands, sponges, clothes, and disposable food containers (Jiang & Doyle, 1999; Kusumaningrum, Putten, Rombouts, & Beumer, 2002). In another study, survival of food-borne pathogens
* Corresponding author. Tel.: +82 42 821 5774; fax: +82 42 825 9754. E-mail address: [email protected] (C. Jo). 0956-7135/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2010.02.002
was detected at a level of 105 CFU/cm2 on stainless steel surfaces (Kusumaningrum, Ridoldi, Hazeleger, & Beumer, 2003). There are several traditional decontamination methods and they can be divided into thermal and non-thermal sterilization. Thermal sterilization can inactivate pathogens efficiently but induces side-effects in the sensory, nutritional, and functional properties of food. Therefore, it cannot be applied to some foods or materials. Moreover, food containers may be also impacted by thermal treatment. To overcome these disadvantages, non-thermal sterilization methods were developed and used including chemical treatment (Jane, Kang, Michael, Stuart, & Valgene, 2008), ultra violet (Shama, 2007), irradiation (Aziz & Moussa, 2002), high pressure (Garcia-Gonzalez et al., 2007), etc. However, these processes also have certain disadvantages which include high costs of application, requirements for specialized equipments, generation of undesirable residues, extended processing time, and lower efficiency (Brendan & Joseph, 2008). Irradiation is known as one of the best non-thermal sterilization methods to destroy pathogenic and spoilage microorganisms but may induce side-effects such as lipid oxidation, off-flavor, and loss of nutritional and sensory quality of food. In addition, this technology needs special facilities and more consumer acceptance. High pressure processing has also been successfully applied in food processing but has limitations in batch
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size processing and affects the quality of the product (Kruk et al., 2009). Plasma is an electrically energized state of matter and can be generated by electrical discharge (Bogaerts, Neyts, Gijbels, & Mullen, 2002). Utilization of non-thermal plasma discharges at pressures at or near 1 atm in the ambient condition makes the decontamination process practical and inexpensive. In addition, the fact that the gas temperature in such discharges remains relatively low makes their use suitable for heat-sensitive products. Recently, atmospheric pressure plasma (APP) has been applied to the deposition, coating, synthesis, metallurgy, and etching of thin film etc. (Gomez et al., 2009). The highly reactive free radicals (OH, H2O) and H2O2 produced during APP process are known to play a major role in the inactivation of bacteria (Gilliland & Speck, 1967; Gweon, Kim, Moon, & Choe, 2009). Reactive oxygen species affect bacterial membrane lipids by causing the formation of unsaturated fatty acid peroxides. Oxidation of amino acid and nucleic acids may also cause changes that result in microbial death or injury. Therefore, APP is introduced as a new sanitizing technology in the field of food processing. APP processing was effective to inactivate microorganisms in hard solid foods including nuts and soft foods including apples and lettuce (Brendan & Joseph, 2008). Recently, Song et al. (2009) reported that APP was effective to inactivate L. monocytogenes inoculated on sliced ham and cheese. Moon et al. (2009) suggested that APP of 4 mA conduction current and 60 °C gas temperature condition was obtained at input power 100 W using helium gas and that it could be safely applied to human skin without electrical and thermal damages. However, evidence of effectiveness on inactivation of pathogens in different foods or food containers is still very limited. The objective of this study was to investigate the inactivation effect of APP on L. monocytogenes inoculated on disposable plastic trays, aluminum foil, and paper cups, which are all commonly used for food preparation and serving. 2. Materials and methods 2.1. Samples preparation Disposable plastic trays (polystyrene), aluminum foil, and paper cups (pulp) were purchased from a local market located in Daejeon, Korea in November 2008. The samples were cut into dimensions (length x width) of 60 6 mm, then packed into a polyethylene pouch. To sterilize the samples, 35 kGy of gamma irradiation (AECL, IR-79, MDS Nordion International Co. Ltd., Ottawa, ON, Canada) was applied at the Advanced Radiation Technology Institute, Jeongeup, Korea. The source strength was approximately 320 kCi with a dose rate of 20 kGy/h at 10 ± 0.5 °C.
was uniformly and aseptically inoculated on the disposable plastic trays, aluminum foil, and paper cups, respectively. The samples were sealed in a polyethylene bag and incubated at 10 °C for 1 h to facilitate the attachment of microorganisms to the samples. 2.3. Treatment by atmospheric pressure plasma (APP) The plasma generator used in the experiment was a capacitively-coupled large area system (dimensions: 110 mm 15 mm) and consisted of a powered rod electrode covered by a dielectric material located in a grounded case, and a bottom ground electrode that was placed under the powered electrode and used as a base for material treatment (Fig. 1). The electrode was powered by a 13.56 MHz rf supply through an impedance matching network. Helium gas with a fixed flow rate of 4 lpm (liter per minute) was introduced for stable plasma generation. The input powers in this study were 75, 100, 125, and 150 W and the exposure times were 30, 60, 90, and 120 s. For plasma treatment, inoculated samples were placed on the bottom conductor and were in direct contact with the plasma at room temperature. The gap distance between the powered electrode and the treatment surface was maintained at 6 mm. Inoculated samples without plasma treatments were also prepared as a control. After plasma treatment, the samples were immediately stored at commercial storage conditions (25 °C) and microbial analysis was performed. 2.4. Microbiological analysis After APP treatment, samples were vortexed with sterile saline solution (NaCl, 0.85%) for 5 min. The samples for the microbiological count were prepared in a series of decimal dilutions utilizing sterile saline solution. The media used for L. monocytogenes was tryptic soy agar (Difco, Laboratories, Detroit, MI, USA). Each diluent (100 l) was spread in triplicate on each agar plate and the plates were incubated at 25 °C for 48 h, after which the colony formation units (CFU) per gram were calculated. 2.5. Statistical analysis Three independent trials were conducted with two samples for treatment combination per each trial in the experiment. One-way Analysis of Variance (ANOVA) was performed, and when significant differences were detected the differences among the mean values were identified by Duncan‘s multiple range test using SAS software with a confidence level of P < 0.05 (SAS, Release 8.01, SAS Institute Inc., Cary, NC). Mean values and standard errors of the mean are reported.
Dielectric
2.2. Inoculation Three strains of L. monocytogenes (ATCC 19114, 19115, and 19111) were obtained from a Korean Culture Center of Microorganisms (KCCM, Seoul, Korea). Each strain was cultured in a tryptic soy broth (Difco, Laboratories, Detroit, MI, USA) at 25 °C for 24 h. At the stationary-phase, a culture of three strains of L. monocytogenes were transferred aseptically to a 50 ml centrifuge tube and were vortexed for 10 s to ensure a homogenous cocktail. Then, L. monocytogenes were centrifuged (1950g for 10 min at 4 °C) in a refrigerated centrifuge (VS-5500, Vision Scientific Co., Seoul, Korea). The pellet was washed twice with sterile saline (0.85%), and suspended in saline to a final concentration of approximately 109 CFU/ml of the stock cocktail inoculum. The test culture suspension (100 ll)
Powered electrode
RF source
Plasma
Sample
Fig. 1. Diagrammatic representation of plasma generator.
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3. Results and discussion
3.2. Effects of APP on L. monocytogenes during storage
3.1. Effects of APP input power on L. monocytogenes survival
Table 2 shows the reduction of L. monocytogenes inoculated on disposable plastic trays, aluminum foil, and paper cups with different input power (W) and exposure time (s) during storage at 25 °C. Results show that the higher input power of APP was more effective in inactivation of L. monocytogenes at even shorter exposure times. Inactivation of L. monocytogenes was influenced more by power (W) than by exposure time (s) on disposable plastic trays. The input power of 75 W resulted in only two decimal reductions of L. monocytogenes after 120 s, but 150 W resulted in elimination of the pathogen (Table 2). APP treatment with 125 W for 60 s or longer showed approximately a two decimal reduction, but after storage for 3 days at 25 °C the viable cell number decreased to undetected levels. After 6 days, the viable cells were reduced below the detection limit with APP treatment of 100 W for 90 s (data not shown). This may be accounted for by the presence of a posttreatment effect wherein the APP damaged cells could not recover. The L. monocytogenes inoculated on aluminum foil and paper cups showed more resistance by APP treatment in this study. In aluminum foil, APP treatment with up to 100 W resulted in only one decimal reduction, and the decrease of the viable cell number was very limited after 3 days (Table 2), and even after 6 days (data not shown). APP treatment of aluminum foil with 150 W for 120 s showed three decimal reductions in L. monocytogenes. In the case of paper cups, 2–3 decimal reductions were achieved by APP at 100, 125, and 150 W for 150 s. However, APP treatment with 75 W was not effective for inactivation of microorganisms. Generally, the inactivation trend of paper cups was similar to aluminum foil. During the plasma process, the formation of an oxygen functional group occurs at the surface of treated materials through the interaction between the active species from the plasma and the surface atoms (Guruvenket, Mohan Rao, Komath, & Raichur, 2004). In plasma-solid interactions, the surface of material may be chemically and physically modified by plasma processing (Pykonen et al., 2008). The membrane surface can be changed by different functional groups. In particular the groups responsible for surface hydrophilicity such as peroxide, carboxylic acid, ketone/aldehyde and ester groups can be generated and activated by plasma on the surfaces (Lai et al., 2006; Weibel, Vilani, Habert, & Achetee, 2006). Guruvenket et al. (2004) reported that plasma-treated polystyrene increased ion density and transformed to a hydrophilic state through an increase of plasma power (Guruvenket et al., 2004). Polystyrene, the major material ingredient in disposable plastic trays, comprises of saturated hydrocarbons and can be easily attacked by the reactive species in the plasma (Araya, Yuji, Watanabe, Kashihara, & Sumida, 2007). Wang, Wu, and Li (2008) reported that the inactivation efficiency of microorganisms in polystyrene decreased with the addition of sodium carbonate, whereas it increased with the addition of ferrous sulfate. The carbonate pigment coated on paper cups may be one of the reasons for the lower efficiency of inactivation of L. monocytogenes inoculated on paper cups by APP. Recently, the inactivation of food-borne microorganisms by plasma treatment has been reported. Deng, Ruan, Mok, Huang, and Chen (2007) showed that the number of E. coli 12955 on almonds was reduced by log 5 after 30 s of non-thermal plasma at 30 kV and 2 kHz. Critzer, Kelly-Wintenberg, South, and Golden (2007) reported that reductions of 2–5 log were obtained in OAUGDP treatment of 2–5 min in E. coli O157:H7, Salmonella enteriridis, and L. monocytogenes on Red Delicious apples. Cold atmospheric plasma treatment (12 kV) reduced the number of Pantoea agglomerans and Gluconacetobacter liquefaciens on mango and melon to below the detection limit after 2.5 s. However, E. coli required 5 s to reach the same level of inactivation and Saccharomyces cerevisiae was the most resistant and required 10 and 30 s in mango
The sensitivity of APP treatment of L. monocytogenes inoculated on the surface of disposable plastic trays, aluminum foil, and paper cups are shown in Table 1. Calculated D10 values, the exposure time required to inactivate 90% of a population from the survival curves, demonstrated a decreasing trend with the increased input power in all of the materials tested. Initially, the highest D10 values with input power of 75 W were observed on paper cups followed by aluminum foil and disposable plastic trays (Table 1). The increased input power from 75 to 100 W reduced the D10 values from 49.3 and 133 s to 47.6 and 111 s on the plastic trays and aluminum foil, respectively, and from 526 to 65.8 s on the paper cups. When the input power was further raised to 150 W the D10 values for disposable plastic trays, aluminum foil and paper cups were reduced to 18.0, 31.6, and 41.7 s, respectively. These results clearly suggest that the efficiency of plasma treatment on L. monocytogenes is highly dependant on surface characteristics of the serving/storage material. Kayes et al. (2007) reported that one atmosphere uniform glow discharge plasma (OAUGDP) treatment resulted in D10 values of 22, 22, and 51 s in S. flexneri, V. parahaemolyticus, and E. coli O157:H7 at pH 7.0 agar, respectively. However, in agar with pH 5.0, D10 values were 19 and 31 s in V. parahaemolyticus and S. enteritidis, respectively. Ben Gadri et al. (2000) observed D10 values for E. coli K12 at 6, 33, and 70 s on polypropylene, glass, and agar, respectively. It seems that D10 values for these incubated agar plates depended strongly on pH among other surface characteristics. A longer plasma exposure time was also required to achieve the same inactivation level for dried cultures or cultures embedded within agar plugs (Ben Gadri et al., 2000). Bacteria in agar require a longer penetration time for the antimicrobial active species to diffuse to them in the porous medium (Montie, Kelly-Winternberg, & Roth, 2000). Recently Song et al. (2009) also pointed out the significantly different effect in inactivation of L. monocytogenes that were inoculated in ham and cheese. The authors indicated that it is possibly due to the sliced ham surface being a little rough compared with the smooth surface of the sliced cheese, so the intricate webbing on the surface of sliced ham provided numerous sites for L. monocytogenes to attach and potentially evade antimicrobial treatment. Park et al. (2008) reported that microwave-induced argon plasma treatment completely sterilized in less than 7 s the silk fabrics inoculated with various strains of either bacteria or fungi. Bacillus subtilis, Aspergillus niger, Bacillus stearothermophilus, and Saccharomyces cerevisiae with an initial spore density of 2.0 104 CFU/cm2 can easily be inactivated within less than one second of plasma treatment without forming dangerous or even toxic products that would contaminate the food packaging material, polyethylene terephthalate (PET) foils (Feichtinger, Schulz, Walker, & Schumacher, 2003).
Table 1 Calculated D10 valuesa (s) for Listeria monocytogenes inoculated on different food containers by atmospheric pressure plasma. Input power (W)
75 100 125 150
D10 value Disposable plastic tray
Aluminum foil
Paper cup
49.3 47.6 36.2 18.0
133 111 76.9 31.6
526 65.8 51.8 41.7
a D10 value is described as the time necessary to reduce the population of cells one log or 90%. The values were determined from plots of the number of survivors versus time (s).
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Table 2 Effects of atmospheric pressure plasma on Listeria monocytogenes (log CFU/g) inoculated on disposable plastic trays, aluminum foil and paper cups during storage at 25 °C. Input power (W)
Exposure time (s)
Disposable plastic tray
Aluminum foil
Paper cup
Storage (day) 0
SEMe
3 aw
bx
0
3 x
x
SEMe
0
3
SEMe
75
0 30 60 90 120 SEMf
6.79 6.07ax 5.26ay 4.49z 4.54z 0.165
5.28 5.11bxy 4.58by 4.63yz 4.47z 0.132
0.146 0.084 0.195 0.099 0.156
7.13 6.97ax 6.86axy 6.47ayz 6.26az 0.125
6.54 6.21bxy 5.92byz 5.74bz 5.61bz 0.092
0.220 0.162 0.076 0.092 0.045
6.51 6.50 6.31a 6.43a 6.23 0.291
6.04 6.32 5.34b 5.21b 5.28 0.310
0.228 0.124 0.060 0.087 0.263
100
0 30 60 90 120 SEMf
6.79aw 5.40ax 4.76ay 4.38az 4.16az 0.100
5.28bw 4.12bxy 4.31ax 3.67byz 3.50bz 0.148
0.146 0.088 0.156 0.152 0.231
7.13w 6.58x 6.19ay 6.09ayz 6.02az 0.039
6.54x 6.16xy 5.71byz 5.60bz 5.51bz 0.133
0.220 0.134 0.087 0.022 0.042
6.51x 6.02x 5.77x 5.72x 4.46y 0.276
6.04x 5.92x 5.41xy 5.46xy 4.72y 0.263
0.228 0.201 0.296 0.143 0.361
125
0 30 60 90 120 SEMf
6.79ax 4.93ay 4.37ay 3.57az 3.33az 0.173
5.28bx 3.58by NDbz NDbz NDbz 0.030
0.146 0.079 0.005 0.145 0.122
7.13w 6.56ax 6.02ay 5.66az 5.53az 0.063
6.54x 5.62by 5.54by 4.75bz 4.49bz 0.144
0.220 0.170 0.060 0.072 0.162
6.51ax 6.11axy 5.36y 4.50y 4.31y 0.292
6.04ax 5.36bxy 5.13y 4.25z 4.19z 0.181
0.228 0.092 0.045 0.420 0.074
150
0 30 60 90 120 SEMf
6.79aw 4.41ax 3.46ay NDz NDz 0.042
5.28bx NDby NDby NDy NDy 0.020
0.146 0.022 0.125 – –
7.13w 4.89x 4.77ax 4.51ay 4.04z 0.069
6.54x 4.38y 4.31byz 4.13byz 3.73z 0.158
0.220 0.190 0.090 0.110 0.120
6.51ax 6.02axy 5.20axy 4.32ay 3.66ay 0.476
6.04ax 5.15by 3.41bz 2.89az 2.15az 0.372
0.228 0.180 0.215 0.632 0.634
Values with different superscripts (a–d) within the same row and for the same material differ significantly (P < 0.05), values with different superscripts (w–z) within the same column for the same material differ significantly (P < 0.05), eStandard errors of the mean (n = 6), f(n = 15), ND = viable cells were not detected with a detection limit at < 101 CFU/g.
and melon, respectively (Perni, Liu, Shama, & Kong, 2008). Atmospheric pressure glow discharge (APGD) treatment for 10 min achieved six decimal reductions on Bacillus subtilis spores at a sporulation temperature of 22 °C and 3.5 decimal reductions at 47 °C (Deng, Shi, & Kong, 2006a, 2006b). Therefore, the microorganism inactivation by plasma treatment can be dependent on different factors including plasma type, microorganism, culture age, exposure power, temperature, pH, exposure time, composition of the media, and material type. The risk of food-borne pathogens is mainly associated with crosscontamination, level of contamination on the surfaces, and the probability of its transfer to food. Perni et al. (2008) suggested that cold atmospheric gas plasmas have potential in decontaminating the skins of soft fruits and it seems feasible when the plasmas generated are scaled up to industrial level (Shi, Liu, & Kong, 2007). In this study, it has been concluded that APP treatment has great potential for inactivation of L. monocytogenes on the surface of disposable food containers. However, different inactivation rates in different surface materials should be considered to achieve satisfactory results. Therefore, further work is required to develop an efficient APP treatment system that can be applied effectively in the food industry. Acknowledgement This work was supported by the Korea Rural Development Administration Fund. References Araya, M., Yuji, T., Watanabe, T., Kashihara, J., & Sumida, Y. (2007). Application to cleaning of waste plastic surfaces suing atmospheric non-thermal plasma jets. Thin Solid Films, 515, 4301–4307. Aziz, N. H., & Moussa, L. A. A. (2002). Influence of gamma-radiation on mycotoxin producing moulds and mycotoxins in fruits. Food Control, 13, 281–288. Ben Gadri, R., Reece Roth, J., Montie, T. C., Kelly-Wintenberg, K., Tsai, P. P. Y., Helfritch, D. J., et al. (2000). Sterilization and plasma processing of room
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