Chemical-free and synergistic interaction of ultrasound combined with plasma-activated water (PAW) to enhance microbial inactivation in chicken meat and skin

Abstract

In general, the poultry industry uses 0.5-1 ppm chlorine solution in the meat sanitization process. However, chlorine can react with organic material and produce halogenated organic compounds, notably chloroform, which causes bladder and rectal cancer in humans. For this reason, many industries try to avoid chlorine. This study investigated the efficacy of ultrasound and plasma-activated water (pAW) on the inactivation of Escherichia coli and Staphylococcus aureus in chicken muscle, rough skin, and smooth skin. Samples inoculated with bacteria suspension were treated by ultrasound alone and PAW-ultrasound. The Taguchi method and desirability function approach were used for the experimental design and optimization. Combined ultrasound and PAW inactivated up to 1.33 log CFU/ ml of E. coli K12 and 0.83 log CFU/ml of S. aureus at a sample thickness of 4 mm, at 40 °C for 60 min, while pAW alone only reduced E. coli K12 by 0.46 log CFU/ml and S. aureus by 0.33 log CFU/ml under the same condition. The muscle topography showed a porous structure, which facilitated the penetration of PAW. The color measurements of muscle treated with ultrasound and PAW-ultrasound were dramatically different from the untreated sample, as also perceived by the sensory evaluation panel. Therefore, the synergistic interaction of combined PAW-ultrasound could be used to enhance microbial inactivation in meat. In the past, sanitization by the chilling process with circulation system in the poultry industry used ice and 0.5-1 ppm chlorine to decrease the temperature of chicken carcass and lower the bacterial load in the gizzard and intestine. However, this process can cause cross-contamination because of circulated poultry water in the chiller tank. Additionally, chlorine can react with organic materials and produce halogenated organic compounds, notably, chloroform, which causes bladder and rectal cancer in humans. Various technologies have since been developed to reduce the bacteria in chicken meat, such as bacteriophage (ListShield ™) combined with UV-C light reduced Listeria monocytogenes 2.04 log CFU/ml 1 , ultrasound combined with a chemical immersion (lactic acid, sodium decanoate, and trisodium phosphate) reduced 0.73 log CFU/ml of Campylobacter jejuni, 1.02 log CFU/ml of TVC, and 1.37 log CFU/ml of total Enterobacteriaceae 2 , electrolyzed water reduced 1.0 log CFU/ml of microbial reduction 3 , non-thermal plasma jet with N 2 /O 2 gas reduced 0.66 log CFU/g of Salmonella typhimurium 4 , cold atmospheric plasma pen with He/O 2 gas reduced 3 log CFU/ml of L. innocua on muscle 5 , and dielectric barrier discharge plasma reduced 3.11 log CFU/ml of C. jejuni on skin 6. The past decade has focused on an environmentally-clean sanitizing technology called non-thermal plasma, particularly plasma-activated water (PAW). PAW can be used as a bacterial disinfection reagent in mass

Plasma‐activated water: Physicochemical properties, microbial inactivation mechanisms, factors influencing antimicrobial effectiveness, and applications in the food industry

“…The study showed that PAW ice efficiently inhibited the growth of microorganisms and slowed down the quality deterioration of shrimps, indicating a promising method to extend the shelf‐life of shrimps and other seafood products. Royintarat, Choi, Boonyawan, Seesuriyachan, and Wattanutchariya (2020) investigated the efficacy of US‐assisted PAW on the inactivation of E. coli and S. aureus on chicken muscle, rough skin, and smooth skin. Up to 1.33 and 0.83 log reduction for E. coli and S. aureus was achieved after the combined treatment, and the porous structure on chicken muscle facilitated the penetration of PAW.…”

“…Moreover, an increased lipid oxidation was reported for shrimps after PAW ice treatment (Liao et al., 2018), frozen beef after thawing by PAW (Liao et al., 2020), and fresh beef after PAW treatment (Zhao et al., 2018) due to the oxidative stress in PAW. Regarding physical parameters change after PAW treatment, less areas of blackspot in shrimps, a decreased a: value (redness) for fresh beef (Zhao et al., 2018), and distinct changes of color for chicken meat were reported (Royintarat et al., 2020). However, not all the PAW treatments resulted in remarkable quality changes.…”

“…However, not all the PAW treatments resulted in remarkable quality changes. For example, no significant difference in lipid or protein content was observed for chicken meat after PAW treatment, and it was also announced that most of the damage induced by ROS was due to the interaction of PAW with the bacterial cell wall rather than with the chicken skin (Royintarat et al., 2020).…”

Nonthermal plasma‐activated water: A comprehensive review of this new tool for enhanced food safety and quality

“…Types of working gases could influence the concentration of the reactive species produced in PAW (Lukes, Dolezalova, Sisrova, & Clupek, 2014). Several working gases, such as air, Ar, He, and Ar/O 2 , have been successfully reported to generate PAW (Lin et al., 2019; Royintarat, Choi, Boonyawan, Seesuriyachan, & Wattanutchariya, 2020; Royintarat et al., 2019; Vlad et al., 2019). Vlad et al.…”

Inactivation efficacy and mechanisms of plasma activated water on bacteria in planktonic state

“…Microbial parameters include the type and state of the micro-organism, for example, vegetative bacteria or spores, planktonic or detached state (Kamgang-Youbi et al 2008;Smet et al 2019), and the microbial community on food products may also affect the inactivation efficacy. Regarding abiotic parameters, storage temperature for PAW (Shen et al 2016;Han et al 2016b), the presence of organic materials in water (Ryu et al 2013;Xiang et al 2019;Zhao et al 2020), and the surface morphology of food products (Royintarat et al 2020) should be considered.…”