Advanced oxidation process for the inactivation of Salmonella typhimurium on tomatoes by combination of gaseous ozone and aerosolized hydrogen peroxide

https://doi.org/10.1016/j.ijfoodmicro.2019.108387Get rights and content

Highlights

  • Gaseous ozone at up to 1600 ppm had little effect on populations of Salmonella.

  • Aerosolized hydrogen peroxide reduced Salmonella populations up to 2.1 logs.

  • AOP reduced the population by up to 5.2 logs on surface and 4.2 logs on stem scar.

  • Synergistic effects were observed between ozone and hydrogen peroxide via AOP.

Abstract

Fresh produce-associated outbreaks of foodborne illnesses continue to occur every year in the U.S., suggesting limitations of current practices and the need for effective intervention technologies. Advanced oxidation process involves production of hydrogen radicals, which are the strongest oxidant. The objective of the present study was to evaluate the effectiveness of advanced oxidation process by combining gaseous ozone and aerosolized hydrogen peroxide. Grape tomatoes were inoculated with a 2-strain cocktail of Salmonella typhimurium on both stem scar and smooth surface. Gaseous ozone (800 and 1600 ppm) and aerosolized hydrogen peroxide (2.5, 5 and 10%) were separately or simultaneously introduced into a treatment chamber where the inoculated tomatoes were placed. During the 30 min treatments, hydrogen peroxide was aerosolized using an atomizer operated in two modes: continuously or 15 s on/50 s off. After the treatments, surviving Salmonella on the smooth surface and stem scar were enumerated. Results showed that ozone alone reduced Salmonella populations by <0.6 log CFU/fruit on both the smooth surface and the stem scar area, and aerosolized hydrogen peroxide alone reduced the populations by up to 2.1 log CFU/fruit on the smooth surface and 0.8 log CFU/fruit on stem scar area. However, the combination treatments reduced the populations by up to 5.2 log CFU/fruit on smooth surface and 4.2 log CFU/fruit on the stem scar. Overall, our results demonstrate that gaseous ozone and aerosolized hydrogen peroxide have synergistic effects on the reduction of Salmonella populations on tomatoes.

Introduction

Foodborne pathogens cause 48 million illnesses, 301,000 hospitalizations, and 4300 deaths in the United States each year (CDC, 2011). Salmonella is one of the most common foodborne pathogens in the United States, causing over 1 million illnesses in the United States per year (Scallan et al., 2011). In addition, the cost of Salmonellosis is estimated to be $3.6 billion annually, which is the most expensive foodborne pathogen according to the USDA's Economic Research Service (USDA, 2014). Fresh tomatoes have been associated with multiple Salmonella outbreaks since 1998 in the United States (Greene et al., 2008; Gurtler et al., 2018). Most (80%) outbreaks associated with tomato were reported during 2000–2010 and a diversified Salmonella serovars were involved in the outbreaks including Newport, Typhimurium and Braenderup (Bennett et al., 2015; Gurtler et al., 2018). Tomatoes could be contaminated with Salmonella spp. on farms, during processing and food preparation. Although foodborne outbreaks related to tomatoes do not appear to be increasing, the risk remains (Gurtler et al., 2018). Furthermore, the proportion of all foodborne outbreaks attributable to fresh produce has been increasing (Bennett et al., 2018). Therefore, there is a need to develop intervention technologies to inactivate human pathogens on fresh produce.

Washing with chemical sanitizers, such as chlorine, is the most commonly postharvest method for minimizing cross-contamination and risk of pathogens on fresh produce. However, washing with sanitizers has limited effectiveness in alleviating the problem of pathogen contamination in produce (Balaguero et al., 2015; Gil et al., 2009; Ruiz-Cruz et al., 2007; Singh et al., 2002). Other technologies across a range of methods have been identified and evaluated. When compared to chlorine, their effectiveness are limited as well (Goodburn and Wallace, 2013). In general, aqueous sanitizers could only achieve a <2-log reduction of the population of microorganisms, although some studies reported higher reductions depending on the target microorganism, type of produce, inoculation and enumeration methods, and treatment methods. The limited effectiveness of aqueous sanitizers may be results of pathogens residing in the protective features on fresh produce such as stem scars, cracks and biofilms, which impede aqueous chemicals to access pathogen cells (Zheng et al., 2013).

Studies have also been conducted on applications of gaseous antimicrobials such as gaseous ozone (O3) and chlorine dioxide which can penetrate to the protective feathers on fresh produce. However, gaseous sanitizers have some disadvantages as well, including inconsistent results, requirement of on-site generation, and sophisticated apparatus needs for gas generation (Oh et al., 2005). Therefore, more effective and convenient decontamination methods are desirable.

Aerosolization is defined as the dispersion of a liquid into air in the form of fine mist, usually for sanitary purposes, especially for respiratory medical treatments and room disinfection (Hiom et al., 2003; Otter et al., 2010). It has been reported that aerosolization of sanitizers was effective in reducing populations of several foodborne pathogens including Bacillus cereus, Escherichia coli O157:H7, Staphylococcus aureus, and Salmonella typhimurium on agar media in the model chamber system (Oh et al., 2005). The effectiveness of aerosolized antimicrobials is dependent on type of sanitizer, concentration and exposure time of sanitizer, and location of pathogens (Jiang et al., 2017).

Advanced oxidation process (AOP) is a method involving production of hydroxyl radicals (•OH), which are among the strongest oxidants (Boczkaj and Fernandes, 2017; Misra, 2015; Oturan and Aaron, 2014). Hydroxyl radicals are commonly produced through the use of combined catalytic oxidants such as ozone-ultraviolet (O3 - UV), hydrogen peroxide-ultraviolet (H2O2 - UV) and hydrogen peroxide-ozone (H2O2 - O3). AOP has been studied for many years for waste water treatment and for degrading pesticides and other pollutants in water (Chin and Bérubé, 2005; Jin et al., 2011). There have been limited studies on the application of AOP to inactivate foodborne pathogens on food, partially due to difficulty in applying the aqueous AOP on solid food items, as well as inherent limitations of aqueous sanitizers. Applying AOP in a vaporous/aerosolized phase may be an option. When applying AOP as a gas or aerosol, two goals may be achieved: generation of hydroxyl radicals which are stronger oxidants than the parent compounds and having sanitizers in vapor/aerosolized form penetrating into small crevices and protective sites where microorganisms often preside. The objective of the present study is to evaluate the effectiveness of combining aerosolized H2O2 and gaseous O3 operated at ambient temperature to inactivate Salmonella on tomatoes in comparison with individual treatments.

Section snippets

Source of tomatoes and chemicals

Grape tomatoes were purchased via special orders through a major supermarket chain. Fruit were examined by appearance, and those without any blemish were used within two days of receiving. Fruits were brought to ambient temperature (~22 °C) before use for bacterial inoculation. H2O2 (30%) and nalidixic acid were purchased from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA). Tryptic soy broth (TSB), tryptic soy agar (TSA), and peptone water (PW) were from Difco (Becton Dickinson, Sparks, MD,

Effect of gaseous O3 alone

Results showed that fruits treated with 800 and 1600 ppm of gaseous O3 for 0.5 h had statistically (P < .05) lower populations of Salmonella on the smooth surface and stem scar area than the control, though no significant differences between 800 and 1600 ppm O3 treatments was observed regardless of inoculation location (Table 1). However, the reductions were very limited, achieving 0.6 log CFU/fruit reductions on the smooth surface and <0.5 log CFU/fruit on the stem scar area. Our earlier

Acknowledgements

We thank Louis Colaruotolo for technical assistance. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). The USDA is an equal opportunity provider and employer.

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