Skip to main content
NCBI home page
Journal of Food Science and Technology logoLink to Journal of Food Science and Technology
. 2019 Jul 29;56(11):4938–4945. doi: 10.1007/s13197-019-03964-7

Inactivation of Pseudomonas deceptionensis CM2 on chicken breasts using plasma-activated water

Chaodi Kang 1,2,3,#, Qisen Xiang 1,2,3,#, Dianbo Zhao 1,2,3, Wenjie Wang 1,2,3, Liyuan Niu 1,2,3, Yanhong Bai 1,2,3,✉
PMCID: PMC6828889  PMID: 31741517

Abstract

The aim of this study was to examine the effectiveness of plasma-activated water (PAW) for inactivating Pseudomonas deceptionensis CM2 on chicken breasts. Sterile distilled water (SDW) was activated by gliding arc discharge plasma for 60 s, which was defined as PAW60. The chicken breast samples inoculated P. deceptionensis CM2 were dipped in PAW60 or SDW for the indicated time intervals, respectively. After the treatment of PAW60 for 12 min, the population of P. deceptionensis CM2 on chicken breast was significantly reduced by 1.05 log10 CFU/g (p < 0.05), which was higher than that of SDW-treated samples for the same time intervals (p < 0.05). The L* value of chicken breasts were increased whereas a* and b* values were decreased following PAW60 treatment, while there was no significant differences in the values of a* and b* between PAW60- and SDW-treated samples for the same time intervals (p > 0.05). As compared with SDW, PAW60 caused no significant changes in the texture characteristics (e.g. hardness, springiness, cohesiveness and gumminess) and sensory properties (e.g. appearance, color, odor, texture, acceptability). Thus, PAW can be very effective to improve microbiological safety of chicken breasts with resulting slight changes to the sensory qualities. This synergistic treatment of PAW with other non-thermal technologies should be well investigated in order to improve inactivation efficacy of PAW.

Keywords: Plasma-activated water, Pseudomonas deceptionensis CM2, Chicken breast, Quality

Introduction

Meat and meat products are rich in nutrients (e.g. proteins, fats, vitamins, and minerals) and provide an ideal medium for growth of microorganisms. Therefore, meat and meat products are potentially susceptible to contamination by a range of spoilage and pathogenic microorganisms during production, processing, and storage (Remenant et al. 2017). Spoilage caused by microbial growth, oxidation and enzymatic autolysis has remained a serious challenge for the meat industry (Doulgeraki et al. 2012). Bacteria are the dominant spoilage microorganisms in meat and meat products, including Pseudomonas spp., Carnobacterium spp., Leuconostoc spp., Lactococcus spp., Enterobacterales spp., Serratia spp., and Brochothrix thermosphacta and so on (Borch et al. 1996). The growth and metabolism of spoilage microorganisms can adversely affect the nutritional and sensory properties of meat products, such as the development of unattractive odors and flavors, discoloration, oxidative rancidity, gas production, slime production, and decrease in pH (Borch et al. 1996). In addition, meat and meat products are easily contaminated with various foodborne pathogens such as Campylobacter spp., Salmonella spp., Shiga toxin-producing strains of Escherichia coli, and Listeria monocytogenes, which may cause considerable disease burden and economic loss (Omer et al. 2018).

Hence, it is essential to apply to ensure the safety and maintain high quality of meat and meat products. Various thermal preservation techniques such as pasteurization, ultrahigh-temperature (UHT) sterilization, and ohmic heating, can effectively kill microbial contaminants in food products with an extended shelf life (De Halleux et al. 2005). On the other hand, conventional thermal sterilization methods usually adversely affect nutritional and sensory quality of the final food products, such as losses of certain nutrients, undesirable texture, off-flavors, and surface discoloration (van Boekel et al. 2010). Meanwhile, some unpleasant toxic compounds are formed during the thermal processing of foods, including furan, acrylamide, 5-hydroxymethylfurfural (HMF), and acrolein (Koszucka and Nowak 2018; van Boekel et al. 2010). In order to satisfy consumers’ rising demands for fresh and safe foods, various non-thermal technologies have been well developed as alternatives to traditional thermal processing, such as ultra-high pressure, pulsed electric field, dense phase carbon dioxide, electrolyzed water, and cold plasma (Bhat et al. 2019; Xiang et al. 2018b; Zhou et al. 2010). These innovative non-thermal sterilization technologies can effectively ensure microbial stability and safety of foods with less impact on the nutritional and sensory properties of foods.

Recently, plasma-activated water (PAW), as a novel non-thermal processing technology, has attracted a great deal of attention for potential application in the food industry with good safety (Kim et al. 2016) and storage stability (Shen et al. 2016). PAW exhibits excellent antimicrobial activity against bacteria, molds, and yeasts and shows great potential for the preservation of fresh fruit and vegetables (e.g. grapes, Chinese bayberries, mung bean sprouts, and button mushrooms) (Guo et al. 2017; Ma et al. 2016; Xiang et al. 2019b; Xu et al. 2016). As an alternative source of nitrite, PAW has been successfully used to cure meat products (Jung et al. 2015; Yong et al. 2018). In addition, Liao et al. (2018) reported that PAW ice could extend the storage time of fresh shrimps by 4–8 days, showing great application potential in the preservation of some seafood products. However, the influence of PAW on the microbial load and sensory attributes of meat products has not been well examined.

Based on this scenario, the aim of this study was to investigate the effects of PAW treatment on the inactivation of Pseudomonas deceptionensis CM2 in raw chicken breasts. In addition, the influences of PAW treatment on the physicochemical, texture, and sensory attributes of fresh chicken breast meat were also evaluated.

Materials and methods

Chemicals and strain

The strain P. deceptionensis CM2 was used in the present study, which was previously isolated from spoiling chicken meat samples collected from Zhengzhou (Henan Province, China). This isolate shares 97.5% 16S rRNA gene sequence similarity with P. deceptionensis DSM 26521. Nutrient agar (NA) and nutrient broth (NB) were purchased from Beijing Aoboxing Biotechnology Co., Ltd. (Beijing, China).

Preparation of inoculum

P. deceptionensis CM2 was cultivated in NB medium for 12 h with mild shaking (150 rpm) at 25 °C. The cells were harvested by centrifugation (8000 × g, 4 °C, 10 min) and washed twice with sterile 0.85% (w/v) NaCl solution. The final cell pellet was resuspended gently in sterile saline (0.85%) to yield a prepared cell suspension of 8 to 9 log10 colony forming units (CFU)/mL.

Preparation of PAW and treatments

In this study, PAW was prepared using a gliding arc discharge plasma jet under atmospheric pressure (Tonson Automation Equipment Co., LTD, Shenzhen, China) (Xiang et al. 2019b). The distance between the atmospheric-pressure plasma jet nozzle and the water surface was 5 mm. The electrical power is supplied to the electrodes by a high voltage generator (5 kV, 40 kHz). The input power was set at 750 W. Compressed air (approximately 0.18 MPa) was used as the working gas. The flow rate of compressed air was 30 L/min at the jet outlet (Xiang et al. 2019b). Every 200 mL of sterile distilled water (SDW) was activated by plasma for 30, 60, and 90 s to obtain PAW, which were defined as PAW30, PAW60, and PAW90, respectively.

Fresh chicken breast samples were purchased from a local supermarket (Zhengzhou, China) and stored at 4 °C until use. Sample portions were separately cut into equal-sized pieces (2 × 2 × 1 cm) using a sterile knife, each weighing 8.00 ± 0.05 g. To destroy the background microflora, the surfaces of chicken breast fillets were wiped with 75% ethanol and exposed to UV light by turning every 10 min for up to 30 min (Rahman et al. 2013). The prepared P. deceptionensis CM2 suspension (0.1 mL, more than 108 CFU/mL) was inoculated onto the external surfaces of UV-treated chicken breasts in a biological safety hood. The chicken breast samples were kept in a laminar flow hood for 30 min to allow for bacterial attachment. Finally, the chicken breast samples were placed individually in sterile containers with 200 mL of SDW or PAW at room temperature for 3, 6, 9, and 12 min, respectively (Fig. 1).

Fig. 1.

Fig. 1

Open in a new tab

Schematic diagram of the experimental arrangement, including PAW generation and treatments of fresh chicken breasts with SDW or PAW

Enumeration of bacteria

After being treated with PAW or SDW for indicated time periods, each meat sample was transferred to a sterile bag with 72 mL of 0.85% sterile saline and then homogenized for 2 min using a stomacher (Scientz-04, Ningbo Scientz Biotechnology Co., Ltd., Ningbo, China). The homogenates were serially diluted in sterile 0.85% saline solution. Then, 0.1 mL of the diluted bacterial suspension was plated onto Pseudomonas selective agar supplemented with cephaloridine, fucidin, and cetrimide (Beijing Bridge Technology Co., Ltd., Beijing, China). After 48 h of incubation at 25 °C, the number of colonies per plate was counted and the results were expressed as log10 CFU/g meat. The unwashed meat samples inoculated with P. deceptionensis CM2 cells were used as control throughout the experiment.

pH determination

Following the different treatments, the pH values of chicken breasts were measured according to a previously reported method (Duan et al. 2017). In brief, each meat sample (approximately 8.0 g) was homogenized in 72 mL of distilled water at 10,000 rpm for 2 × 30 s, and the pH value of the obtained homogenate was measured using a Delta 320 pH meter (Mettler-Toledo, Schwerzenbach, Switzerland).

Color measurement

After being dipped in each 200 mL of PAW60 or SDW for 3, 6, 9, and 12 min, respectively, the color of meat samples was measured using a Ci64UV portable sphere spectrophotometer (X-Rite Inc., Grand Rapids, MI, USA). Color characteristics were expressed by the CIE L*a*b* system (L*—lightness/darkness, a*—redness/greenness, and b*—yellowness/blueness).

Texture profile analysis

Texture characteristics of PAW60 or SDW-treated chicken breast samples were determined using a texture analyser (TA-XT Plus, Stable Micro Systems Ltd., Surry, UK) equipped with a 50-kg load cell (Jayasena et al. 2015). A double compression cycle test was performed up to 60% strain compression of the original height using an aluminum cylinder probe (SMP P/50, flat bottom, diameter 50 mm). The samples were measured with a 5 g trigger force with a pretest speed of 2.0 mm/s, a test speed of 1.0 mm/s, and a post-test speed of 1 mm/s. A time of 5 s was allowed to elapse between the first and second stroke. The recorded force–time plots were used for the calculation of TPA parameters values including hardness, springiness, cohesiveness, and gumminess. Fifteen replicate samples were used for each treatment.

Sensory evaluation

Sensory properties (color, appearance, odor, texture, and overall acceptability) of PAW60 or SDW-treated chicken breast samples were determined using a method described previously (Lee et al. 2016; Yang et al. 2017). Sensory qualities of the samples were evaluated by sensory panelists who were all staff of the laboratory using a 9-point hedonic scale, where “1” is extreme dislike, and “9” is highly acceptable.

Statistical analysis

All analyses were performed in triplicate and the results were presented as the mean ± standard deviation (SD). Data were analyzed using SPSS for Windows (version 21.0, IBM, Chicago, IL, USA). Statistical differences were analyzed using a one-way analysis of variance (ANOVA) followed by Duncan’s multiple range tests. A value of p < 0.05 was considered significant.

Results and discussions

PAW induced the inactivation of P. deceptionensis CM2

The effectiveness of PAW for the inactivation of P. deceptionensis CM2 on the surface of raw chicken breasts is summarized in Fig. 2. As shown in Fig. 2a, PAW60 showed stronger bactericidal activity against P. deceptionensis CM2 than PAW30 (p < 0.05). However, the treatment of PAW90 did not result in a significant reduction of P. deceptionensis CM2 cells compared with that of PAW60 (p > 0.05). Therefore, PAW60 was chosen for the next work. The dipping time also remarkably affected the bactericidal efficiency of PAW against P. deceptionensis CM2 incubated onto chicken breasts. As shown in Fig. 2b, significant reduction of P. deceptionensis CM2 was observed after being treated with PAW60 or SDW for 3 to 12 min. The bacterial inactivation efficiency of PAW60 was significantly higher than that of SDW for the same time intervals (p < 0.05). As compared with the control group, the number of P. deceptionensis CM2 was reduced nearly by 1.05 log10 CFU/g after being treated with PAW60 for 12 min. The antibacterial mechanism of PAW is not fully understood, but may result from the synergistic effect of long-lived chemical species (e.g. nitrites, nitrates, hydrogen peroxide, and peroxynitrous acid) and acidic pH (Naïtali et al. 2010).

Fig. 2.

Fig. 2

Open in a new tab

Inactivation of P. deceptionensis CM2 inoculated on fresh chicken breasts after treatments with PAW or SDW. a The meat samples were treated with PAW30, PAW60, PAW90, and SDW for 6 min as described in the Materials and Methods section. b The meat samples were treated with PAW60 or SDW for the indicated time intervals. All experiments were performed in triplicate. Different letters indicate significant differences between groups (p < 0.05)

The antibacterial activity of PAW against P. deceptionensis CM2 incubated onto chicken breasts was lower than that in 0.85% sterile saline (Xiang et al. 2018a). According to our previous study, some organic matters in chicken breasts may cause decrease in the antibacterial efficiency of PAW (Xiang et al. 2019a). Therefore, the PAW should be combined with other non-thermal technologies such as UV and ultrasound in order to strengthen its inactivation efficiency against pathogenic and spoiling microorganisms.

Effect of PAW treatment on the pH value of chicken breasts

pH value has been shown to be a key factor in determining the quality of poultry meat, such as water-holding capacity, tenderness, color, flavor, and shelf life (Huff-Lonergan and Lonergan 2005; Ismail and Joo 2017). The pH values for all samples are shown in Table 1 with the initial pH being 5.77 for the control samples. As shown in Table 1, no significant changes in the pH values of fresh chicken breasts were observed after SDW treatment for 3 to 12 min (p > 0.05). The PAW60 treatment for 3 to 9 min also resulted in no significant changes in the pH values of chicken breast samples. Nevertheless, the pH of chicken breasts subjected to PAW60 treatment for 12 min was significantly lower than that of the control group (p < 0.05). These results are consistent with previous research of Jung et al. (2017), in which the pH of meat batter subjected to plasma treatment for 25 and 30 min was significantly lower than that of the untreated samples (p < 0.05).

Table 1.

pH values of chicken breasts treated with SDW or PAW60

Treatment time (min) SDW PAW60
0 5.77 ± 0.06a 5.77 ± 0.06a
3 5.75 ± 0.01a 5.75 ± 0.04a
6 5.75 ± 0.05a 5.73 ± 0.06a
9 5.74 ± 0.02a 5.72 ± 0.05a
12 5.76 ± 0.05a 5.70 ± 0.02b
Open in a new tab

The results are expressed as the mean ± standard deviation (n = 6). Values with different letters in the same column are significantly different (p < 0.05)

The decrease in pH values of chicken breasts may due to the acidification of PAW during plasma activation. The pH of PAW60 was found to be 2.80 in our previous work, which might be related to the high levels of acidogenic molecules (e.g., NOx) generated during plasma discharge in water (Xiang et al. 2018a).

Effect of PAW treatment on the texture properties of chicken breasts

The texture profile of chicken breasts after being washed with PAW60 or SDW are shown in Table 2. The treatment of PAW60 or SDW for 3 to 12 min did not result in significant changes in the hardness and springiness values of chicken breasts (p > 0.05). On the contrary, the washing treatments with PAW60 or SDW caused obvious decreases in the values of cohesiveness and gumminess. However, there was no statistically significant difference between the values for cohesiveness and gumminess of PAW60-treated samples and those of SDW-treated samples (p > 0.05). In summary, the treatment of PAW60 did not result in significant changes in the texture parameters of chicken breasts as compared with SDW.

Table 2.

Texture profile analysis of chicken breasts treated with SDW or PAW60

Group Treatment time (min) Hardness (kg) Springiness (mm) Cohesiveness (%) Gumminess (kg)
Control – 11.57a 0.46a 0.38a 4.45a
SDW 3 10.98a 0.41a 0.34ab 3.98ab
SDW 6 10.58a 0.45a 0.37ab 3.83ab
SDW 9 10.98a 0.41a 0.36ab 3.88ab
SDW 12 9.84a 0.42a 0.30ab 2.88b
PAW60 3 11.30a 0.42a 0.30ab 3.40ab
PAW60 6 10.63a 0.41a 0.31ab 3.31ab
PAW60 9 11.13a 0.42a 0.33ab 3.71ab
PAW60 12 9.82a 0.41a 0.29b 2.76b
Open in a new tab

The results are expressed as the mean ± standard deviation (n = 15). Values with different letters in the same column are significantly different (p < 0.05)

Effect of PAW treatment on the color of chicken breasts

Color is the most common quality indicator used by consumers to judge the eating quality of fresh meat. The surface color of PAW60- or SDW-treated chicken breasts is presented in Table 3. There was no significant difference in the values for L* of SDW-treated samples (p > 0.05). On the contrary, significant increases in the lightness values (L*) were observed in chicken breasts treated by PAW60 for 9 or 12 min (p < 0.05). In addition, the treatment of SDW and PAW60 also resulted in significant decreases in the redness (a*) and yellowness (b*) values, but no significant differences in the values of a* and b* were observed between PAW60- and SDW-treated samples for the same time intervals (p > 0.05). These findings are in accordance with Yang and Froning (1992), who found the L* values of chicken meat increased and a* values decreased after washing treatment. Similarly, brightness values of chicken breasts were also increased following the treatment with alkaline and acidic electrolyzed water (Shimamura et al. 2016).

Table 3.

Surface color of chicken breasts treated with SDW or PAW60

Group Treatment time (min) L* a* b*
Control – 60.76 ± 1.92b 7.56 ± 1.20a 20.37 ± 2.32a
SDW 3 61.36 ± 1.78b 6.58 ± 1.34ab 16.45 ± 2.32b
SDW 6 62.25 ± 1.48b 6.13 ± 1.57bc 15.52 ± 2.67b
SDW 9 61.79 ± 1.39b 6.06 ± 1.75bc 16.32 ± 2.93b
SDW 12 61.16 ± 1.71b 5.28 ± 1.00c 14.09 ± 2.49b
PAW60 3 61.98 ± 2.62b 6.56 ± 1.48ab 16.21 ± 2.67b
PAW60 6 61.07 ± 3.24b 6.11 ± 1.46bc 16.38 ± 3.61b
PAW60 9 63.99 ± 1.70a 5.30 ± 1.15c 15.18 ± 2.43b
PAW60 12 65.15 ± 1.87a 5.16 ± 1.55c 16.11 ± 4.01b
Open in a new tab

The results are expressed as the mean ± standard deviation (n = 15). Values with different letters in the same column are significantly different (p < 0.05)

The changes in the surface color of chicken breasts induced by PAW may be due to reactive oxygen species and reactive nitrogen species in PAW, which are generated during plasma activation (Choi et al. 2016; Lee et al. 2016; Yong et al. 2017). High levels of hydrogen peroxide (H2O2), nitrite (NO3−), and nitrate (NO2−) are determined in PAW in our previous works (Xiang et al. 2018a, 2019b). The generated hydrogen peroxide in PAW can react with myoglobin, causing the color of meat to appear greener (Fröhling et al. 2012).

As an alternative to synthetic sodium nitrite, PAW has been used for meat curing (Jung et al. 2015). Yong et al. (2018) found out that the a* value of PAW-cured loin ham was significantly increased as compared with that of samples injected with sodium nitrite. However, PAW causes no remarkable changes in the b* value and L* value of loin ham (Yong et al. 2018). The mechanism of meat product discoloration by PAW should be elucidated in further study.

Influences of PAW treatment on the sensory qualities of chicken breasts

The effect of PAW or SDW treatments on the sensory properties of chicken breasts is shown in Table 4. The color of chicken breasts was not significantly affected by PAW60 or SDW (p > 0.05). On the contrary, the appearance, odor, texture, and acceptability of chicken breasts immersed in SDW or PAW60 were significantly decreased as compared with untreated samples (p < 0.05). However, no significant differences in the appearance, odor, texture, and acceptability of chicken breasts were observed between PAW60- and SDW-treated samples for the same time intervals (p > 0.05). PAW-induced changes in the sensory acceptance may be attributed to the reactive oxygen species (ROS) and reactive nitrogen species (RNS) generated during plasma discharge, such as hydroxyl radical (OH·), hydrogen radical (·H), oxygen (1O2), nitrite (NO2−), and nitrate (NO3−) (Arjunan et al. 2015). In agreement with previous studies, ROS and RNS have slightly reduced the scores of overall acceptability, odor, and texture on pork (Choi et al. 2016; Jayasena et al. 2015) and beef (Yong et al. 2017).

Table 4.

Sensory acceptance of chicken breasts treated with SDW or PAW60

Group Treatment time (min) Appearance Color Odor Texture Acceptability
Control – 7.83 ± 0.41a 7.58 ± 0.80a 7.67 ± 0.82a 7.67 ± 0.52a 7.72 ± 0.25a
SDW 3 6.67 ± 1.21b 7.15 ± 0.52a 6.58 ± 1.11b 6.33 ± 0.75b 6.62 ± 0.45b
SDW 6 6.20 ± 0.84b 7.20 ± 0.57a 6.52 ± 0.67b 6.30 ± 1.20b 6.50 ± 0.50b
SDW 9 6.10 ± 0.74b 7.00 ± 0.01a 6.50 ± 0.50b 6.40 ± 0.55b 6.52 ± 0.36b
SDW 12 6.50 ± 1.00b 7.10 ± 0.22a 6.60 ± 0.55b 6.30 ± 0.67b 6.48 ± 0.40b
PAW60 3 6.33 ± 0.52b 7.33 ± 0.52a 6.42 ± 0.66b 6.43 ± 0.59b 6.75 ± 0.16b
PAW60 6 6.00 ± 0.01b 6.88 ± 0.25a 6.50 ± 1.00b 6.50 ± 0.91b 6.55 ± 0.60b
PAW60 9 6.56 ± 0.52b 6.80 ± 0.84a 6.46 ± 0.68b 6.42 ± 0.43b 6.60 ± 0.44b
PAW60 12 6.40 ± 0.82b 7.06 ± 0.75a 6.50 ± 0.71b 6.36 ± 0.47b 6.52 ± 0.48b
Open in a new tab

The results are expressed as the mean ± standard deviation (n = 15). Values with different letters in the same column are significantly different (p < 0.05)

Conclusion

The present research focused on the effect of PAW on inactivation of P. deceptionensis CM2 and quality of chicken breast. The results showed that PAW could significantly inactivate P. deceptionensis CM2 incubated on the surface of chicken breasts. At the same time, PAW60 caused no significant changes in the physicochemical and sensory properties of chicken breast than that of SDW-treated samples. In future studies, the combination of PAW with other non-thermal technologies should be well investigated in order to improve inactivation efficacy and minimize negative effects on sensory and nutritional qualities of fresh meat. On the other hand, the scientific assessment of efficacy and safety of PAW should be carried out before its application in the food industry.

Acknowledgements

This work was financially supported by the National Key R & D Program of China (No. 2018YFD0401204), the China Postdoctoral Science Foundation (No. 2018M632765), the Fundamental Research Funds for the Universities in Henna Province (No. 18KYYWF0404), and the Foundation for University Young Key Teachers of Henan Province (No. 2017GGJS095).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Chaodi Kang and Qisen Xiang have contributed equally to this work.

References

  1. Arjunan KP, Sharma VK, Ptasinska S. Effects of atmospheric pressure plasmas on isolated and cellular DNA—a review. Int J Mol Sci. 2015;16(2):2971–3016. doi: 10.3390/ijms16022971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bhat ZF, Morton JD, Mason SL, Bekhit AEA. Current and future prospects for the use of pulsed electric field in the meat industry. Crit Rev Food Sci Nutr. 2019;59(10):1660–1674. doi: 10.1080/10408398.2018.1425825. [DOI] [PubMed] [Google Scholar]
  3. Borch E, Kant-Muermans ML, Blixt Y. Bacterial spoilage of meat and cured meat products. Int J Food Microbiol. 1996;33(1):103–120. doi: 10.1016/0168-1605(96)01135-X. [DOI] [PubMed] [Google Scholar]
  4. Choi S, Puligundla P, Mok C. Corona discharge plasma jet for inactivation of Escherichia coli O157:H7 and Listeria monocytogenes on inoculated pork and its impact on meat quality attributes. Ann Microbiol. 2016;66(2):685–694. doi: 10.1007/s13213-015-1147-5. [DOI] [Google Scholar]
  5. De Halleux D, Piette G, Buteau ML, Dostie M. Ohmic cooking of processed meats: energy evaluation and food safety considerations. Can Biosyst Eng. 2005;47:341–347. [Google Scholar]
  6. Doulgeraki AI, Ercolini D, Villani F, Nychas GJE. Spoilage microbiota associated to the storage of raw meat in different conditions. Int J Food Microbiol. 2012;157(2):130–141. doi: 10.1016/j.ijfoodmicro.2012.05.020. [DOI] [PubMed] [Google Scholar]
  7. Duan DB, Wang HH, Xue SW, et al. Application of disinfectant sprays after chilling to reduce the initial microbial load and extend the shelf-life of chilled chicken carcasses. Food Control. 2017;75:70–77. doi: 10.1016/j.foodcont.2016.12.017. [DOI] [Google Scholar]
  8. Fröhling A, Durek J, Schnabel U, et al. Indirect plasma treatment of fresh pork: decontamination efficiency and effects on quality attributes. Innov Food Sci Emerg Technol. 2012;16:381–390. doi: 10.1016/j.ifset.2012.09.001. [DOI] [Google Scholar]
  9. Guo J, Huang K, Wang X, et al. Inactivation of Yeast on grapes by plasma-activated water and its effects on quality attributes. J Food Prot. 2017;80(2):225–230. doi: 10.4315/0362-028X.JFP-16-116. [DOI] [PubMed] [Google Scholar]
  10. Huff-Lonergan E, Lonergan SM. Mechanisms of water-holding capacity of meat: the role of postmortem biochemical and structural changes. Meat Sci. 2005;71(1):194–204. doi: 10.1016/j.meatsci.2005.04.022. [DOI] [PubMed] [Google Scholar]
  11. Ismail I, Joo ST. Poultry meat quality in relation to muscle growth and muscle fiber characteristics. Korean J Food Sci Anim Resour. 2017;37(6):873–883. doi: 10.5851/kosfa.2017.37.6.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jayasena DD, Kim HJ, Yong HI, et al. Flexible thin-layer dielectric barrier discharge plasma treatment of pork butt and beef loin: effects on pathogen inactivation and meat-quality attributes. Food Microbiol. 2015;46:51–57. doi: 10.1016/j.fm.2014.07.009. [DOI] [PubMed] [Google Scholar]
  13. Jung S, Kim HJ, Park S, et al. The use of atmospheric pressure plasma-treated water as a source of nitrite for emulsion-type sausage. Meat Sci. 2015;108:132–137. doi: 10.1016/j.meatsci.2015.06.009. [DOI] [PubMed] [Google Scholar]
  14. Jung S, Lee J, Lim Y, et al. Direct infusion of nitrite into meat batter by atmospheric pressure plasma treatment. Innov Food Sci Emerg Technol. 2017;39:113–118. doi: 10.1016/j.ifset.2016.11.010. [DOI] [Google Scholar]
  15. Kim HJ, Sung NY, Yong HI, et al. Mutagenicity and immune toxicity of emulsion-type sausage cured with plasma-treated water. Food Sci Anim Resour. 2016;36(4):494–498. doi: 10.5851/kosfa.2016.36.4.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Koszucka A, Nowak A. Thermal processing food-related toxicants: a review. Crit Rev Food Sci Nutr. 2018 doi: 10.1080/10408398.2018.1500440. [DOI] [PubMed] [Google Scholar]
  17. Lee H, Yong HI, Kim HJ, et al. Evaluation of the microbiological safety, quality changes, and genotoxicity of chicken breast treated with flexible thin-layer dielectric barrier discharge plasma. Food Sci Biotechnol. 2016;25(4):1189–1195. doi: 10.1007/s10068-016-0189-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liao XY, Su Y, Liu DH, et al. Application of atmospheric cold plasma-activated water (PAW) ice for preservation of shrimps (Metapenaeus ensis) Food Control. 2018;94:307–314. doi: 10.1016/j.foodcont.2018.07.026. [DOI] [Google Scholar]
  19. Ma RN, Yu S, Tian Y, et al. Effect of non-thermal plasma-activated water on fruit decay and quality in postharvest Chinese Bayberries. Food Bioprocess Technol. 2016;9(11):1825–1834. doi: 10.1007/s11947-016-1761-7. [DOI] [Google Scholar]
  20. Naïtali M, Kamgang-Youbi G, Herry JM, et al. Combined effects of long-living chemical species during microbial inactivation using atmospheric plasma-treated water. Appl Environ Microbiol. 2010;76:7662–7664. doi: 10.1128/AEM.01615-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Omer MK, Alvarez-Ordonez A, Prieto M, et al. A systematic review of bacterial foodborne outbreaks related to red meat and meat products. Foodborne Pathog Dis. 2018;15(10):598–611. doi: 10.1089/fpd.2017.2393. [DOI] [PubMed] [Google Scholar]
  22. Rahman SME, Wang J, Oh DH. Synergistic effect of low concentration electrolyzed water and calcium lactate to ensure microbial safety, shelf life and sensory quality of fresh pork. Food Control. 2013;30(1):176–183. doi: 10.1016/j.foodcont.2012.06.041. [DOI] [Google Scholar]
  23. Remenant B, Jaffres E, Dousset X, et al. Bacterial spoilers of food: behavior, fitness and functional properties. Food Microbiol. 2017;45(PrA):45–53. doi: 10.1016/j.fm.2014.03.009. [DOI] [PubMed] [Google Scholar]
  24. Shen J, Tian Y, Li YL, et al. Bactericidal effects against S. aureus and physicochemical properties of plasma activated water stored at different temperatures. Sci Rep. 2016;6:28505. doi: 10.1038/srep28505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shimamura Y, Shinke M, Hiraishi M, et al. The application of alkaline and acidic electrolyzed water in the sterilization of chicken breasts and beef liver. Food Sci Nutr. 2016;4(3):431–440. doi: 10.1002/fsn3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. van Boekel M, Fogliano V, Pellegrini N, et al. A review on the beneficial aspects of food processing. Mol Nutr Food Res. 2010;54(9):1215–1247. doi: 10.1002/mnfr.200900608. [DOI] [PubMed] [Google Scholar]
  27. Xiang QS, Kang CD, Niu LY, et al. Antibacterial activity and a membrane damage mechanism of plasma-activated water against Pseudomonas deceptionensis CM2. LWT Food Sci Technol. 2018;96:395–401. doi: 10.1016/j.lwt.2018.05.059. [DOI] [Google Scholar]
  28. Xiang QS, Liu XF, Li JG, et al. Influences of cold atmospheric plasma on microbial safety, physicochemical and sensorial qualities of meat products. J Food Sci Technol. 2018;55(3):846–857. doi: 10.1007/s13197-017-3020-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Xiang QS, Kang CD, Zhao DB, et al. Influence of organic matters on the inactivation efficacy of plasma-activated water against E. coli O157:H7 and S. aureus. Food Control. 2019;99:28–33. doi: 10.1016/j.foodcont.2018.12.019. [DOI] [Google Scholar]
  30. Xiang QS, Liu XF, Liu SN, et al. Effect of plasma-activated water on microbial quality and physicochemical characteristics of mung bean sprouts. Innov Food Sci Emerg Technol. 2019;52:49–56. doi: 10.1016/j.ifset.2018.11.012. [DOI] [Google Scholar]
  31. Xu YY, Tian Y, Ma RN, et al. Effect of plasma activated water on the postharvest quality of button mushrooms, Agaricus bisporus. Food Chem. 2016;197(PtA):436–444. doi: 10.1016/j.foodchem.2015.10.144. [DOI] [PubMed] [Google Scholar]
  32. Yang TS, Froning GW. Selected washing processes affect thermal gelation properties and microstructure of mechanically deboned chicken meat. J Food Sci. 1992;57(2):325–326. doi: 10.1111/j.1365-2621.1992.tb05486.x. [DOI] [Google Scholar]
  33. Yang S, Sadekuzzaman M, Ha SD. Treatment with lauric arginate ethyl ester and commercial bacteriophage, alone or in combination, inhibits Listeria monocytogenes in chicken breast tissue. Food Control. 2017;78:57–63. doi: 10.1016/j.foodcont.2017.02.021. [DOI] [Google Scholar]
  34. Yong HI, Lee H, Park S, et al. Flexible thin-layer plasma inactivation of bacteria and mold survival in beef jerky packaging and its effects on the meat’s physicochemical properties. Meat Sci. 2017;123:151–156. doi: 10.1016/j.meatsci.2016.09.016. [DOI] [PubMed] [Google Scholar]
  35. Yong HI, Park J, Kim HJ, et al. An innovative curing process with plasma-treated water for production of loin ham and for its quality and safety. Plasma Process Polym. 2018;15(2):e1700050. doi: 10.1002/ppap.201700050. [DOI] [Google Scholar]
  36. Zhou GH, Xu XL, Liu Y. Preservation technologies for fresh meat-a review. Meat Sci. 2010;86(1):119–128. doi: 10.1016/j.meatsci.2010.04.033. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Food Science and Technology are provided here courtesy of Springer

RESOURCES