Elsevier

Food Control

Volume 95, January 2019, Pages 18-26
Food Control

Review
Applications of gaseous chlorine dioxide on postharvest handling and storage of fruits and vegetables – A review

https://doi.org/10.1016/j.foodcont.2018.07.044Get rights and content

Highlights

  • Chlorine dioxide (ClO2) is a powerful sanitizer for postharvest produce use.

  • Rapid diffusion and penetration to biofilm are the advantages of gaseous ClO2.

  • Controlled-release ClO2 is applicable for control of microbial growth during storage.

  • ClO2 is effective in control of both human pathogenic and spoilage organisms.

Abstract

Foodborne illness and decay loss caused by microorganisms are primary concerns for processors and marketers of fruits and vegetables. Interest in using gaseous chlorine dioxide (ClO2) treatments for postharvest sanitation has increased in recent years due to its many advantages over other sanitizers, including its powerful antimicrobial activity, and low environmental impact. It also has low corrosivity to packing equipment at food sanitation concentrations, but can be corrosive in highly concentrated aqueous solutions. Like many water mediated sanitizers, ClO2 has been applied to various commodities. However, gaseous ClO2 has many advantages over its aqueous formulations in addition to being less corrosive, including ease of mixing with air, rapid diffusion, and the ability to penetrate permeable surfaces and biofilms. A combination of aqueous sanitizer washing and application of gaseous ClO2 will enhance decontamination of both foodborne and plant pathogens. This article compares ClO2 with other commonly used sanitizers, discusses the mechanisms of ClO2 against microorganisms, and focuses intensively on the applications of gaseous ClO2, especially controlled-release ClO2, on fruits and vegetables to reduce pathogen infection and maintain food safety and quality of fresh produce.

Introduction

Fresh fruits and vegetables are recognized as key vehicles for disease outbreaks due to their ease of contamination with various harmful microorganisms (Arango et al., 2014), and have become one of the most widespread public health problems in the world (Redmond & Griffith, 2003). It has been estimated that about 76 million Americans and 130 million Europeans are affected by foodborne illnesses annually (Mead et al., 1999, Redmond and Griffith, 2003). Historically, consumption of contaminated foods caused over 1000 deaths each year in the United States (Scallan et al., 2011) with an increasing number coming from a lack of good agricultural practices (Van Boxstael et al., 2013, Wongprawmas et al., 2015). Between 2011 and 2013 the U.S. Centers for Disease Control and Prevention (CDC) reported more than a hundred foodborne illness incidents related to the consumption of various fruits and vegetables contaminated with pathogens including, but not limited to, Salmonella enterica, Escherichia coli, and Listeria monocytogenes (Friedman et al., 2013, Sun et al., 2017, Sun et al., 2017, Sun et al., 2017).

Fruits and vegetables possess high nutritional value as they are rich in vitamins, dietary fibers, amino acids, and minerals (Gastol, Domagala-Swiatkiewicz, & Krosniak, 2011). The consumption of fruits and vegetables is recognized as conferring many health benefits, such as protection against gastric and colon cancers (Lunet, Lacerda-Vieira, & Barros, 2005), heart disease, and type 2 diabetes (Clifton, Petersen, Blanch, & Keogh, 2014). However, postharvest fruits and vegetables, especially their fresh-cut products, are highly perishable due to water and nutrient loss caused by physiological deterioration, biochemical changes, and microbial degradation, which lead to significant economic losses (Ashiq, 2015, Berg et al., 1986, Praeger et al., 2016). More than one third of fruits and vegetables spoil each year as a result of improper handling and environmental conditions. Most spoilage of fruits and vegetables is caused by microorganisms (Hammond et al., 2015). Therefore, the biosafety enhancement and quality improvement of fruits and vegetables is a constant challenge for the food industry.

The most common technology for the decontamination of fruits and vegetables is the use of sanitizers (Olanya, Annous, & Taylor, 2015). The properties of some common sanitizers are shown in Table 1. Ozone is a strong antimicrobial agent with various applications in the food industry, however, it can cause oxidation of ingredients present on food surfaces and can result in discoloration and quality deterioration (Kim, Yousef, & Dave, 1999). Some researchers have advocated the use of organic acids, including peracetic and octanoic acids, to sanitize the surfaces of vegetables (Hilgren & Salverda, 2000), due to their strong oxidizing potential, but the antimicrobial capacity of these acids relies on their low pH (Cherry, 1999). Though hydrogen peroxide has been used as a biocide to kill Cryptosporidium parvum (Kniel et al., 2003), field studies indicate that it is not an optimal disinfectant. In addition some applications reveal deposition of a hydrogen peroxide residue, which makes this treatment unfit for fresh produce (Soliva-Fortuny & Martin-Belloso, 2003). Chlorine has been applied to sterilize fresh produce, including tomatoes and apples (Abadias et al., 2011, Bartz et al., 2001), and while effective, the safe use of chlorine for the sanitization of produce can be prohibitively complicated and expensive (Soliva-Fortuny & Martin-Belloso, 2003). Chlorine may also react with nitrogen-containing compounds, including ammonia, to produce carcinogenic byproducts, such as trihalomethanes (THMs) (Richardson, Plewa, Wagner, Schoeny, & Demarini, 2007). Titanium dioxide has been evaluated in a coating with antibacterial ability for fruit storage (Lin et al., 2015). While somewhat effective under alkaline conditions, titanium dioxide is corrosive, environmentally pollutive and expensive (Schilling et al., 2010). Nitric oxide is an important signaling molecule involved in numerous plant stress responses, including infection. Treatment with nitric oxide has been demonstrated to protect peaches from infection by inducing defense enzymes and the expression of anti-pathogen related genes (Gu, Zhu, Zhou, Liu, & Shi, 2014). While nitric oxide is safe to use and non-corrosive it is only effective under acidic conditions and has a contact time ranging from minutes to hours. The safety and efficiency of nitric oxide in the preservation of fresh produce is still under investigation.

Chlorine dioxide (ClO2), a synthetic green-yellowish gas, is a water-soluble strong oxidant with an oxidation ability 2.5 times higher than that of diatomic chlorine (V. C. H. Wu & Rioux, 2010). It is extremely effective with a short treatment time at low concentrations in a large pH range without formation of THMs or other halogenated organic compounds (Benarde et al., 1967, Sun et al., 2017, Sy et al., 2005, Sy et al., 2005). It is most commonly used in the cleaning of public water treatment facilities, and paper manufacturing plants (V. M. Gomez-Lopez, Rajkovic, Ragaert, Smigic, & Devlieghere, 2009). It has also been used in both gaseous and aqueous formulations in post-harvest processes to reduce microbial populations on fruits and vegetables (V. M. Gomez-Lopez et al., 2009). Unlike other sanitizers, ClO2 does not cause the formation of excessive amounts of unwanted residues in edible fractions of fruits and vegetables (Kaur et al., 2015, Smith et al., 2015). Disadvantages of ClO2 for practical applications include its instability and the equipment requirements for on-site production (Praeger et al., 2016).

Gaseous ClO2 possess many advantages over its aqueous form. Although aqueous ClO2 treatments have been utilized for the sanitization of fruits and vegetables (Chen et al., 2011, Pao et al., 2007), its gaseous form is more effective at reaching and inactivating pathogenic cells attached to inaccessible plant parts (such as found in the peel of nettled melons) due to its high diffusivity and penetrability (Y. Lee et al., 2015, Sun et al., 2017, Sun et al., 2017, Sun et al., 2017). Han, Floros, et al. (2001) and Han, Linton, et al. (2001) evaluated the reductions of L. monocytogenes on injured and non-injured green pepper surfaces using both aqueous and gaseous ClO2. Gaseous ClO2 showed significantly higher log reduction than aqueous ClO2 treatment for both injured and uninjured food surfaces (Han, Linton, Nielsen, & Nelson, 2001). Gaseous ClO2 can also effectively penetrate the polysaccharide layer of a bacterial biofilm on the surface of fruits and vegetables without being excessively depleted due to reactions with the component sugars (Nam et al., 2014). This allows the gaseous ClO2 to react directly with the bacteria, largely bypassing the biofilm (Nam et al., 2014). Additionally, the corrosiveness and toxicity of gaseous ClO2 is minimal at concentrations used for decontamination, therefore, it is known to be an effective and generally acceptable sterilization agent for various applications (Gordon and Rosenblatt, 2005, Park and Kang, 2015a). Conversely, the high corrosivity of low pH aqueous ClO2 solutions limits its application as a sanitizer (Bohner & Bradley, 1991). An aqueous ClO2 concentration of 400 mg/L is sufficiently caustic to cause severe corrosion on A3 steel and mild corrosion on stainless steel (Kang et al., 2012). Aqueous ClO2 is however, more easily implemented into most vegetable and fruit processing lines, and does not require a sealed chamber for its application (V. C. H. Wu, 2016).

Regulations for the use of ClO2 treatment of water or fresh produce vary by country. The U.S. Environmental Protection Agency (EPA) permits maximum concentration of 0.8 mg/L of ClO2 in drinking water based on the assumption that a 70 kg adult ingests 2 L/day of water (Korn, Andrew, & Escobar, 2002). In Germany, a maximum concentration of 0.4 mg/L of ClO2 can be used for drinking water disinfection. According to the U.S. Food and Drug Administration (FDA), aqueous ClO2 can be used as an antimicrobial agent for poultry processing, and for washing fruits and vegetables that are not raw agricultural merchandises with a concentration not to exceed 3 ppm (= 3 mg/L) residual ClO2 (Praeger et al., 2016). In the U.S., a maximum of 200 ppm aqueous ClO2 concentration is also permitted for sanitizing equipment used in fruit and vegetable processing, 5 ppm maximum residual ClO2 is allowable for use in cleaning shelled beans and peas with intact cuticles and whole fresh fruits and vegetables, and only 1 ppm maximum residual ClO2 is permitted for peeled potatoes (Parish et al., 2003). For gaseous ClO2, the exposure limit is 0.1 ppm (0.28 mg/m3) for 8-h, or 0.3 ppm for 15-min time-weighted average (TWA) in the U.S., United Kingdom, and some other countries (Morino et al., 2009).

In this review, the properties of ClO2 and other commonly used sanitizers are compared, the mechanisms of ClO2 against microorganisms are illustrated, and the effects of gaseous ClO2 on the safety and quality of fruits and vegetables are discussed.

Section snippets

Mechanisms of ClO2 against microorganisms

The mechanisms of microorganism inactivation by ClO2 (Fig. 1) include destabilization of cell membranes, reaction with amino acids and interruption of protein synthesis, and possibly the oxidation of DNA/RNA/proteins (Sun et al., 2014). The antimicrobial efficacy of ClO2 is principally due to its destabilization of cell membranes: the oxygenated compounds and proteins in the cell membranes react with ClO2, causing cell metabolism disruption (Praeger et al., 2016, Vandekinderen et al., 2009).

Effect of gaseous ClO2 on microbial populations of fruits and vegetables

The efficacy of gaseous ClO2 for reducing microbial populations on fruits and vegetables has been listed in Table 2. Generally, gaseous ClO2 was less effective against Gram-positive (G+) than against Gram-negative (G-) bacteria, while molds and yeast displayed intermediate tolerance (Vandekinderen et al., 2009). Differences in tolerance between G- and G+ bacteria to gaseous ClO2 is conceivably due to the thin plate mesh peptidoglycan layer of G- bacteria, which may be more easily penetrated by

Surface color and visual appearance

Various experiments have been conducted concerning the impact of gaseous ClO2 on the visual appearance, especially the surface color, of fresh fruits and vegetables. Browning in fruits and vegetables is a major concern, because it affects appearance and organoleptic properties, and causes deterioration of nutritional quality and sensory properties (Fu, Zhang, Wang, & Du, 2007). Browning is caused by the production of melanin from the polymerization of quinones created following the oxidation of

Effect of gaseous ClO2 on chemical and physiological properties of fruits and vegetables

Gaseous ClO2 may also affect nutritional quality of fruits and vegetables, since it can react with phenolic compounds (Napolitano, Green, Nicoson, & Margerum, 2005). For example, ascorbic acid is easily oxidized by ClO2 gas. There is however little research concerning a negative effect of gaseous ClO2 treatment on nutritional quality. In contrast, ClO2 gas treatments show a tendency to slow the rate at which foods naturally lose nutritional components. The vitamin C content in the 5–50 mg/L

Effect of gaseous ClO2 on sensory properties of fruits and vegetables

Treatment with gaseous ClO2 for 20 min at 4.1 mg/L did not cause negative effects on sensory properties of cabbage, carrot, and fresh-cut lettuce stored at 23 °C (Sy, McWatters, et al., 2005). Various conducted studies have not noted a negative influence of gaseous ClO2 on the sensory qualities of blueberries and raspberries (Sy et al., 2005, Sy et al., 2005), tomatoes and onions (Sy, McWatters, et al., 2005), strawberries (V. M. Gomez-Lopez et al., 2007, Mahmoud et al., 2007), and cantaloupe (

Conclusions

Gaseous ClO2 is a highly effective biocide for use in reducing produce losses and enhancing food safety due to its strong antibacterial and antifungal activities. However, it also has some limitations, including problematic transportability, requiring expensive onsite generation or inefficient two-part powder mixing, and instability at high concentrations. The application of gaseous ClO2 is useful to improve safety, quality, and sensory properties of fruits and vegetables, even though higher

Acknowledgment

We would like to thank Drs. Jan Narciso and Christopher Ference for their help with the composition of this review.

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