Plasma-activated water’s potential contribution to ‘One Health’

Introduction

Foodborne pathogens cost A$2.44 billion annually in Australia due to increased mortality, healthcare costs or lost workforce.¹ The World Health Organisation reports 600 million foodborne illnesses worldwide, leading to 420,000 deaths annually.² The main pathogens responsible for these diseases include Listeria, Salmonella, Campylobacter and Escherichia coli.³

Overuse or misuse of antibiotics and chemical sanitisers in the food supply chain can cause antimicrobial resistance (AMR), which is a significant threat to public health. These resistances reduce the effectiveness of antimicrobial agents in different areas, such as commonly applied decontamination strategies and even ‘last resort’ antibiotics.⁴

The One Health approach addresses the complex interconnectedness of human, animal and environmental health, especially in the context of food safety, to reduce the risk of emerging resistance (Fig. 1). The concept encourages multidisciplinary solutions through the targeted use of antibiotics, pesticides and sanitisers, as well as general guidelines for health practitioners, veterinarians and the food industry.⁵

Fig. 1.

The One Health concept for addressing the interconnectedness of human, animal and environmental health, to reduce the risk of emerging microbial resistance.

Sanitisers are typically chemical-based and can lead to adverse effects, such as chemical residues in food and environmental pollution.⁶ Eco-friendly methods are heat or UV treatment, however, these methods are often unsuitable for low processed food as they can induce changes to sensory attributes like colour, smell or texture, leading to a demand for novel eco-friendly sanitisers. Cold plasma technology is a non-thermal solution that shows promise in addressing these challenges. Recent approaches even facilitate cold plasma to generate sanitisers based on liquids like water or aqueous solutions.

Plasma and plasma-activated water

Plasma can be generated by the application of energy to gases that then form a new state of matter. The matter is composed of myriad reactive species (ions, electrons and free radicals) including reactive oxygen and nitrogen species (RONS) that have antimicrobial properties.⁷ Thus, water treated with plasma, so-called plasma-activated water (PAW), contains short and long-lived reaction products like superoxide (O2−), nitric oxide (NO*), peroxynitrite (ONOO⁻), hydrogen peroxide (H₂O₂), ozone (O₃), nitrite (NO₂) and nitrate (NO₃).⁴ These dissolved antimicrobial species are active against foodborne pathogens like Escherichia coli, Listeria, Campylobacter and Salmonella.^3,4 This makes PAW a promising candidate for investigation in food sanitising and food safety applications. Additionally, PAW could be used as fertiliser in agriculture due to the presence of various nitrogen compounds (Fig. 2).

Fig. 2.

Combination of water and plasma. Reactions of the chemical species form reactive oxygen and nitrogen species (RONS), leading to antimicrobial and fertilising properties in plasma-activated water.

The properties of PAW are affected by the type of generator and configurations employed for plasma generation. Most important properties include the pH, oxidation–reduction potential and conductivity, which can be altered by selecting appropriate feeding gases and discharge parameters. The physicochemically diverse composition enables PAW to target multiple microbial components, including microbial membranes, enzymes and DNA.⁸ These simultaneous reactions result in rapid microbial inactivation and reduced possibility of emerging AMR.⁸

Further tailoring of the physicochemical properties allows for various applications in the food industry, including decontamination of surface contact areas and equipment, biofilm degradation and disinfection of food.^3,4 The adjustable properties of PAW additionally allow for applications in agriculture, water purification and pesticide degradation (Fig. 3).^9–11

Fig. 3.

Plasma-activated water utilisation for microbial disinfection, agriculture and other potential applications.

Applications of PAW in the food and agricultural industry

In the food industry, the antimicrobial properties of PAW have been demonstrated for foodborne pathogens like Escherichia coli, Salmonella, Listeria and Campylobacter, where log₁₀ reductions of colony forming units (CFU) for planktonic bacteria are reported as 5.4, 3.9, 5.4 and 4.2 respectively.^12–15

Bacteria survive harsh environments by forming biofilms, made from extracellular polymeric substances. The biofilm provides shelter against antibiotics and decontamination strategies and reduces the effectiveness of sanitisers and decontamination treatments drastically. Even for biofilm-forming bacteria, PAW achieves efficient decontamination, as reports show log₁₀CFU reductions of up to 5.4, 3.9 and 5.4 for E. coli, Salmonella and Listeria respectively.^15–17 Previous studies demonstrated the food sanitising capacity of PAW for fresh fruits and vegetables, nuts, meat, fish, poultry and eggs (Table 1).

PAW treatment has the benefit of minor or no effect on sensory attributes of foods, as shown for chicken breast, bean sprouts, cucamelons and beef.^8,19,20 Recent application of PAW as a nitrate rich process media for beef jerky highlighted these effects in comparison to conventional processing, while maintaining the desired red colour of the treated beef.²² The nitrogen compounds and their easier bioavailability, due to high reactivity, in PAW can additionally aid crop fertilisation. Current investigations of PAW revealed further benefits to agriculture applications for seed germination, plant growth and plant health.¹¹

Other applications utilise the incorporated reactivity of PAW or the induced modifications of treated substrates. For example, the processing of crop materials like starch and proteins with PAW results in enhanced water-binding capabilities, aggregation and gelation.²⁸

Additionally, the general reactivity of PAW allows for wastewater purification and pesticide degradation, while producing no toxic residues.¹⁰ Other applications as a thawing agent for meat and fish products to reduce bacterial contamination highlight the potential for innovative approaches for PAW besides the main use as sanitising agent.^13,24

PAW and One Health

The ‘One Health’ framework recognises that diseases affecting animals can also affect human health, and emphasises the need for a unified strategy in mitigating foodborne threats.⁵ In this context, the application of PAW as an innovative, sanitisation technology promotes food safety through potent pathogen mitigation while considering the broader effects on animal welfare and environmental sustainability.

Common food sanitisers used against foodborne pathogens often contain chemicals like chlorine, quaternary ammonium compounds, bromine or iodine, which leave residues that are harmful to both human health and the environment. Therefore, gentler and more sustainable methods are desired.²⁹ PAW is promising because its antimicrobial properties mainly derive from the action of RONS. This eliminates the need for harmful chemicals and reduces the burden on the environment resulting in improved eco-friendly food processing. Additionally, initial studies highlighted the interaction between RONS and inherent reactive species, resulting in enhanced antimicrobial properties compared to pure chemical-based sanitisers.⁸

In addition to the burden that sanitisers place on the environment, their residues and accumulation contribute to the risk of emerging resistance. Owing to shared mechanisms of action with antibiotics, this could lead to compromised effectiveness of antibiotics in human and animal health.³⁰ The evidence of increased tolerance of agricultural microbiota against common antibiotics, like ciprofloxacin and kanamycin highlights the problem of possible development of resistance caused by residuals in the environment.³⁰ Additionally, RONS are non-specific and target the membrane of bacteria, reducing the risk of emerging resistance.

Concerns of reduced agricultural output or possible pollution of soil through chemical fertilisers should be addressed regarding One Health. The demonstrated benefits of PAW’s fertilising properties related to RONS and contained nitrates could allow for the replacement of other chemical fertilisers; thereby placing less burden on soil, as well as ensuring agricultural output, while simultaneously reducing pollution in water and soil.⁵

Recent studies of PAW treatment of pesticides, like carbendazim and chlorpyrifos, have shown effective reduction by respectively 80 and 65% within 30–60 min. Furthermore, the simultaneous reduction of bacterial load and elimination of fungal spores could be proven.^9,10 The incorporation of PAW in the food supply chain could thereby reduce pesticide residues, while simultaneously decreasing the risk of forming resistance.⁹

In comparison to soil, wastewater is similarly affected by sanitisers, pesticides and fertiliser residues. Therefore, efficient wastewater treatment is needed to accomplish the vision of One Health. Recent results of PAW application for in-line water treatment showed efficient methylene-orange degradation.¹⁰ Further scale-up of this application could contribute to clean water supply and improved waste management.

As various disciplines work together for the One Health approach, effective controls pre- and post-harvest are crucial to effectively reduce the risk of contamination throughout the food supply chain. Therefore, protocols for PAW application should be developed to ensure proper use of this novel sanitiser. Furthermore, regulatory criteria should be developed for the successful application of PAW, as to our knowledge PAW is not yet approved by authorities like the World Health Organization or US Food and Drug Administration. These guidelines would ensure optimal performance for different applications.⁵

The remaining challenges are the necessary quality attributes and limitations to batch production of PAW with volumes of up to 520 L h^–1. Addressing these limitations would enable an efficient utilisation of PAW as a commercial-scale sanitiser within the food industry.^13,29

Conclusion

The application of PAW as food sanitiser, fertiliser and degradation agent for environmental pollutants could positively contribute to One Health. Besides foodborne pathogen reduction, PAW could efficiently reduce the risk of AMR within food production due to the rapid and synergistic antimicrobial reactions, addressing the unmet need for novel antimicrobials. However, further research is required to study the potential interactions of PAW with pollutants and to prove its non-toxicity before regulatory approval could enable industry application of this novel sanitiser.