ReviewApplications of gaseous chlorine dioxide on postharvest handling and storage of fruits and vegetables – A review☆
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.
References (106)
- et al.
Evaluation of alternative sanitizers to chlorine disinfection for reducing foodborne pathogens in fresh-cut apple
Postharvest Biology and Technology
(2011) - et al.
In situ quantification of chlorine dioxide gas consumption by fresh produce using UV-visible spectroscopy
Journal of Food Engineering
(2014) - et al.
Sustainable sanitation techniques for keeping quality and safety of fresh-cut plant commodities
Postharvest Biology and Technology
(2009) - et al.
Corrosivity of chlorine dioxide used as sanitizer in ultrafiltration systems
Journal of Dairy Science
(1991) - et al.
Combined effects of aqueous chlorine dioxide and ultrasonic treatments on postharvest storage quality of plum fruit (Prunus salicina L.)
Postharvest Biology and Technology
(2011) - et al.
Effects of aqueous chlorine dioxide treatment on nutritional components and shelf-life of mulberry fruit (Morus alba L.)
Journal of Bioscience and Bioengineering
(2011) - et al.
Mechanisms of Escherichia coli inactivation by several disinfectants
Water Research
(2010) - et al.
The efficacy of the combined use of chlorine dioxide and passive modified atmosphere packaging on sweet cherry quality
Postharvest Biology and Technology
(2015) - et al.
Inactivation by chlorine dioxide gas (ClO2) of Listeria monocytogenes spotted onto different apple surfaces
Food Microbiology
(2002) - et al.
Efficacy of chlorine dioxide gas in reducing Escherichia coli O157: H7 on apple surfaces
Food Microbiology
(2003)
Effects of aqueous chlorine dioxide treatment on polyphenol oxidases from Golden Delicious apple
Lwt-Food Science and Technology
Shelf-life extension of minimally processed carrots by gaseous chlorine dioxide
International Journal of Food Microbiology
Shelf-life of minimally processed lettuce and cabbage treated with gaseous chlorine dioxide and cysteine
International Journal of Food Microbiology
Chlorine dioxide for minimally processed produce preservation: A review
Trends in Food Science & Technology
Effects of chlorine dioxide treatment on respiration rate and ethylene synthesis of postharvest tomato fruit
Postharvest Biology and Technology
Response surface modeling for the inactivation of Escherichia coli O157: H7 on green peppers (Capsicum annuum L.) by chlorine dioxide gas treatments
Journal of Food Protection
Reduction of Listeria monocytogenes on green peppers (Capsicum annuum L.) by gaseous and aqueous chlorine dioxide and water washing and its growth at 7 degrees C
Journal of Food Protection
Decontamination of strawberries using batch and continuous chlorine dioxide gas treatments
Journal of Food Protection
The effects of washing and chlorine dioxide gas on survival and attachment of Escherichia coli O157: H7 to green pepper surfaces
Food Microbiology
Disinfection effect of chlorine dioxide on bacteria in water
Water Research
Primary mutagenicity screening of food-additives currently used in Japan
Food and Chemical Toxicology
Chloroxyanion residue quantification in cantaloupes treated with chlorine dioxide gas
Journal of Food Protection
Application of ozone for enhancing the microbiological safety and quality of foods: A review
Journal of Food Protection
Evaluation of gaseous chlorine dioxide for the inactivation of Tulane virus on blueberries
International Journal of Food Microbiology
Effect of organic acids and hydrogen peroxide on Cryptosporidium parvum viability in fruit juices
Journal of Food Protection
Development of chlorine dioxide-related by-product models for drinking water treatment
Water Research
Reaction and diffusion of chlorine dioxide gas under dark and light conditions at different temperatures
Journal of Food Engineering
Efficacy of chlorine dioxide gas against Alicyclobacillus acidoterrestris spores on apple surfaces
International Journal of Food Microbiology
Development of silver/titanium dioxide/chitosan adipate nanocomposite as an antibacterial coating for fruit storage
Lwt-Food Science and Technology
Inactivation kinetics of inoculated Escherichia coli O157: H7, Listeria monocytogenes and Salmonella enterica on strawberries by chlorine dioxide gas
Food Microbiology
Inactivation kinetics of inoculated Escherichia coli O157:H7 and Salmonella enterica on lettuce by chlorine dioxide gas
Food Microbiology
Inactivation kinetics of inoculated Escherichia coli O157: H7, Listeria monocytogenes and Salmonella Poona on whole cantaloupe by chlorine dioxide gas
Food Microbiology
Efficacy of gaseous chlorine dioxide in inactivating Bacillus cereus spores attached to and in a biofilm on stainless steel
International Journal of Food Microbiology
Moisture loss is the major cause of firmness change during postharvest storage of blueberry
Postharvest Biology and Technology
Using aqueous chlorine dioxide to prevent contamination of tomatoes with Salmonella enterica and Erwinia carotovora during fruit washing
Journal of Food Protection
Antimicrobial effect of chlorine dioxide gas against foodborne pathogens under differing conditions of relative humidity
Lwt-Food Science and Technology
Combination treatment of chlorine dioxide gas and aerosolized sanitizer for inactivating foodborne pathogens on spinach leaves and tomatoes
International Journal of Food Microbiology
Effect of temperature on chlorine dioxide inactivation of Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on spinach, tomatoes, stainless steel, and glass surfaces
International Journal of Food Microbiology
Efficacy of chlorine dioxide gas sachets for enhancing the microbiological quality and safety of blueberries
Journal of Food Protection
Evaluation of chlorine dioxide gas treatment to inactivate Salmonella enterica on mungbean sprouts
Journal of Food Protection
Consumer food handling in the home: A review of food safety studies
Journal of Food Protection
Occurrence, genotoxicity, and carcinogenicity of regulated and emerging disinfection by-products in drinking water: A review and roadmap for research
Mutation Research
Use of chlorine dioxide fumigation to alleviate enzymatic browning of harvested 'Daw' longan pericarp during storage under ambient conditions
Postharvest Biology and Technology
Efficacy of chlorine dioxide, ozone, and thyme essential oil or a sequential washing in killing Escherichia coli O157: H7 on lettuce and baby carrots
Lebensmittel-Wissenschaft Und-Technologie-Food Science and Technology
New advances in extending the shelf-life of fresh-cut fruits: A review
Trends in Food Science & Technology
Antimicrobial activity of controlled-release chlorine dioxide gas on fresh blueberries
Journal of Food Protection
Effect of controlled-release chlorine dioxide on the quality and safety of cherry/grape tomatoes
Food Control
Efficacy of gaseous chlorine dioxide as a sanitizer for killing Salmonella, yeasts, and molds on blueberries, strawberries, and raspberries
Journal of Food Protection
Evaluation of gaseous chlorine dioxide as a sanitizer for killing Salmonella, Escherichia coli O157: H7, Listeria monocytogenes, and yeasts and molds on fresh and fresh-cut produce
Journal of Food Protection
Use of high-concentration-short-time chlorine dioxide gas treatments for the inactivation of Salmonella enterica spp. inoculated onto Roma tomatoes
Food Microbiology
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