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. 2019 Apr 2;10:622. doi: 10.3389/fmicb.2019.00622

Table 1.

Summary of major research articles assessing the influence of processing parameters on the performance of non-thermal atmospheric plasma as a food decontamination technique.

References Treatment regime Foods/medium Microorganism Main findings
Marsili et al. (2002) 23 kV; Pulse rate: 320 pps; N2, CO2, air (10 L/min); Up to 50 s; batch 0.1% peptone solution E. coli NCTC 9001, S. aureus NCTC 4135, S. Enteritidis NCTC PT4, B. cereus NCTC KD4 Air gas facilitated a greater inactivation after a 50 s treatment. B. cereus was the most susceptible microorganism.
Deng et al. (2007) 16–25 kV; 1,000– 2,500 Hz; Air; Up to 30 s Almonds E. coli 12955 (Collection of the Dept of Food Science and Nutrition, University of Minnesota) Effectiveness increased with the applied voltage and the frequency. Cells at log growth phase were more sensitive than those at stationary phase.
Rowan et al. (2007) 23.5 kV; Pulse rate: 124 pps; N2, O2, CO2, air (10 L/min); Up to 30 s; 4°C; batch Distilled water B. cereus NCTC 11145 spores The order of effectiveness was: O2 >CO2; air >N2
Muranyi et al. (2008) 170 W; Air (0–80% RH); 20°C; For up to 7 s PET foils Bacillus subtilis DSM 4181 spores, Aspergillus niger DSM 1957 spores For A. niger, increased effectiveness at relative gas humidity of 70%; in contrast, B. subtilis spores showed slightly poorer inactivation at high gas humidity.
Miao and Jierong (2009) 13.56 MHz; 20–120 W; O2 (20–100 cm3/min); Up to 120 s Poly(vinyl chloride) (PVC) E. coli* The optimum conditions (highest efficiency) are 100 W and O2 60 cm3/min.
Song et al. (2009) 13.56 MHz; 75–150 W; Helium (10 L/min); Up to 120 s Sliced cheese and ham 3-strain cocktail of L. monocytogenes (ATCC 19114, 19115, and 19111) Increased effectiveness at high input power. Higher D values were obtained in sliced ham.
Jung et al. (2010) 13.56 MHz; 75 and 100 W; Helium and argon (6 L/min); Up to 120 s Slide glass Bacillus subtilis Spores* Helium plasma was much less efficient than argon plasma;
Increased effectiveness at high input power
Leipold et al. (2010) 10.4 kV; 21.7 kHz; 1.8 W-0.36 kW; Air; Up to 340 s Knife Listeria innocua (DMRI 0011) Increased effectiveness at high discharge power
Ragni et al. (2010) 12.7 kHz; 15 kV; Air (RH 35 and 65%); 25°C; Up to 90 min Shell eggs S. Enteritidis MB2509, S. Typhimurium T5 Increased effectiveness at high air moisture content; S. Enteritidis resulted to be more plasma sensitive
Yun et al. (2010) 13.56 MHz; 75–150 W; Helium (4 L/min); Up to 120 s Disposable plastic trays, aluminum foil, and paper cups 3-strain cocktail of L. monocytogenes (ATCC 19114, 19115, and 19111) Increased effectiveness at high input power. The lowest D values were obtained on disposable plastic trays.
Kim et al. (2011) 13.56 MHz; 75–125 W; Helium (10 L/min) and He+O2 (10 sccm); Up to 90 s Sliced bacon L. monocytogenes (KCTC 3596),
E. coli (KCTC 1682), S. Typhimurium (KCTC 1925)
Increased effectiveness at high input power and with the addition of oxygen to the working gas.
Lee et al. (2011) 2 kV; 50 kHz; He, N2 (7 L/min), He+O2, N2+O2 (0.07 L/min); Up to 2 min Agar plates, slices of cooked chicken breast and ham L. monocytogenes KCTC 3596 N2 was more effective than He. The addition of O2 to both gases improved their effectiveness, being N2 + O2 the most effective mixture. The highest and the lowest levels of inactivation were obtained on agar plates and sliced chicken breast, respectively.
Alkawareek et al. (2012) 6 kV; 20–40 kHz; 0.5% O2+ 99.5% helium (2 L/min); Up to 240 s Agar plates Pseudomonas aeruginosa PA01 (ATCC BAA-47) Increased effectiveness at high frequencies
Fröhling et al. (2012b) 27.12 MHz; 10–40 W; Argon (20 L/min); Up to 4 min Gelrite®-a polysaccharide
gel
L. innocua DSM 20649; E. coli DSM 1116 Increased effectiveness at high discharge power
Niemira (2012) 47 kHz; 549 W; Air and N2; Distance from the plasma jet: 2–6 cm; Up to 20 s Almonds S. Anatum F4317, S. Stanley H0558, S. Enteritidis PT30, E. coli O157:H7 (C9490, ATCC 35150, ATCC 43894) Air was more effective
The greatest reductions were observed for E. coli O157:H7 C9490 at a 6 cm distance
Bermúdez-Aguirre et al. (2013) 3.95–12.83 kV; 60 Hz; Argon (455.33 sccm); Up to 10 min Lettuce, baby carrots, tomatoes E. coli ATCC 11775 Effectiveness increased with voltage and decreased with increasing contamination level. Tomatoes, followed by lettuce, were easier to decontaminate than carrots.
Han et al. (2013) 56 and 70 kV; 50 Hz; Air, 90% N2 + 10% O2, 65% O2 + 30% CO2 + 5% N2; Direct and indirect exposure; Up to 120 s; batch Phosphate Buffered Saline (PBS) E. coli ATCC 25922, E. coli NCTC 12900, L. monocytogenes NCTC11994 Greater reduction of viability using higher voltage and with working gas mixtures with higher oxygen content.
Indirect mode of exposure more effective than direct exposure. L. monocytogenes resulted to be more sensitive
Ziuzina et al. (2013) 40 kV; Air; Direct and indirect exposure; Up to 300 s; batch Maximum recovery diluent (MRD) or PBS E. coli ATCC 25922 Direct exposure resulted to be more effective than indirect exposure, especially at lower plasma treatment times.
Patil et al. (2014) 50 Hz; 70 kV; Air (3–70% RH), 90% N2 + 10% O2, 65% O2 + 30% CO2 + 5% N2; 20°C; Direct and indirect exposure; Up to 120 s Sterile polystyrene Petri dish containing B. atrophaeus spore strips B.atrophaeus standard spore strips (Sportrol®_Namsa®) The gas mixture 65% O2 + 30% CO2 + 5% N2 was the most effective; Increased effectiveness at high air moisture content and after direct exposure to plasma
Edelblute et al. (2015) 24 kV; 500 Hz; Air (5, 10 L/min); Up to 3 min Brain Heart Infusion (BHI) agar plates Ecoli ATCC 25922 and S. epidermidis ATCC 12228. Effectiveness decreased with the flow rate
Takamatsu et al. (2015) 16 kHz; 9 kV; 10 W; Ar, O2, N2, CO2, air (1 L/min); 20°C; Up to 120 s; batch PBS S. aureus ATCC 25923, P. aeruginosa ATCC 27853 The greatest antimicrobial effect was obtained with N2 and CO2
Butscher et al. (2016) 6–10 kV; 5–15 kHz; Argon; Up to 60 min Wheat grains; Polypropylene granules Geobacillus stearothermophilus (ATCC 7953) spores Higher efficiency by applying faster pulse frequency or higher pulse voltage. Less decontamination effect on wheat grains than on polypropylene
Calvo et al. (2016) 1 kHz; 1 W; O2, N2 (5–15 L/min); Up to 4 min Polycarbonate membrane filters L. monocytogenes CECT 4301, L. innocua CECT 910 A higher sensitivity to plasma was observed when the treatment was performed using air; increases in flow rate from 5 to 10 L/min caused an acceleration of bacterial inactivation when air was used; gas flow rate hardly affected NTAP efficiency when nitrogen was used.
Cui et al. (2016a) 300–600 W; N2; Up to 3 min Lettuce; Stainless steel coupons Biofilms of Escherichia coli O157:H7 (CICC 21530). Significant lower inactivation was observed at 300 W; The combination of plasma and clove oil exhibited a remarkable synergistic effect
Cui et al. (2016b) 300–600 W; N2 (100 sccm); Up to 3 min Eggshell Salmonella Enteritidis (CICC 21482); Salmonella Typhimurium (CICC 22956) Significant lower inactivation was observed at 300 W; The combination of plasma and thyme oil exhibited a remarkable synergistic effect
Gabriel et al. (2016a) 2.45 GHz; 450 and 650 W; Air (5 L/min); Up to 25 min; batch Young coconut liquid endosperm Multi-strain cocktails of E. coli O157:H7 (7 strains), S. enterica (5 strains), L. monocytogenes (2 strains) and spoilage bacteria (Klebsiella spp., Staphylococcus spp., and Kluyvera spp.) Significant lower inactivation was observed at 450W; S. enterica exhibited the greatest plasma resistance, while L. monocytogenes and Staphylococcus spp. exhibited the least.
Lai et al. (2016) 4 W; Air (2–7 m/s); 52–90% RH Sterilized distilled water Micrococcus luteus ATCC 4698, Staphylococcus epidermidis ATCC 12228, E. coli
ATCC 10536, Serratia marcescens ATCC 6911, Pseudomonas. alcaligenes ATCC 14909.
The inactivation efficacy increased with flow rate and decreased with relative humidity. The inactivation efficacy at 90% R.H. dropped to 10% of the value measured at 55% R.H.
Calvo et al. (2017) 1 kHz; 1 W; O2, N2 (5–15 L/min); Up to 12 min Polycarbonate membrane filters S. Typhimurium CECT 443, S. Enteritidis CECT 4300 Microbial inactivation was higher when air was used and with increasing flow rates
*

Non-specified strain.

RH: relative humidity; pps: pulses per second; sccm: standard cubic centimeters per minute.