There are a variety of methods used to reduce populations of microorganisms on whole and fresh-cut produce. Each method has distinct advantages and disadvantages depending upon the type of produce, mitigation protocol, and other variables. The best method to eliminate pathogens from produce is to prevent contamination in the first place. However, this is not always possible and the need to wash and sanitize many types of produce remains of paramount importance to prevent disease outbreaks. It should be noted that washing and sanitizing are unlikely to totally eliminate all pathogens after the produce is contaminated. Therefore, it is important to use washing and sanitizing protocols that are efficient. Another important point to consider is that some produce, such as certain berries, cannot be washed due to their delicate structure and problems with mold proliferation. These and some other produce items are often packaged in the field with minimal postharvest handling or washing.
In reference to food contact surfaces, 21 CFR 110.3(o) (CFR 2000b) defines the word sanitize: "to adequately treat food-contact surfaces by a process that is effective in destroying vegetative cells of microorganisms of public health significance." An additional definition of "sanitize" is found in the FDA Guide to Minimize Microbial Food Safety Hazards for Fresh Fruits and Vegetables (FDA 1998): "to treat clean produce by a process that is effective in destroying or substantially reducing the numbers of microorganisms of public health concern, as well as other undesirable microorganisms, without adversely affecting the quality of the product or its safety for the consumer." This definition addresses the need to maintain produce quality while enhancing safety by reducing populations of pathogenic microorganisms of public health significance that might theoretically exist on the produce.
Traditional methods of reducing microbial populations on produce involve chemical and physical treatments. Control of contamination requires that these treatments be applied to equipment and facilities as well as to produce. Methods of cleaning and sanitizing produce surfaces usually involve the application of water, cleaning chemicals (for example, detergent), and mechanical treatment of the surface by brush or spray washers, followed by rinsing with potable water. The rinse step may include a sanitizer treatment. It is important to ensure that water used for washing and sanitizing purposes is clean so that it does not become a vehicle for contamination.
Efficacy of the method used to reduce microbial populations is usually dependent upon the type of treatment, type and physiology of the target microorganisms, characteristics of produce surfaces (cracks, crevices, hydrophobic tendency, texture), exposure time and concentration of cleaner/sanitizer, pH, and temperature. It should be noted that the concentration/level of sanitizers or other intervention methods may be limited by unacceptable sensory impact on the produce. Infiltration of microorganisms into points below the surface of produce is problematic. While it is known that microorganisms can infiltrate into produce under certain handling conditions, the significance of any such infiltration to public health requires further study.
The relationship between human pathogens and the native microflora, including postharvest spoilage organisms, on produce is of interest for at least two reasons. First, it has been suggested that reducing/controlling the native microbial populations by washing and sanitizing or by controlled atmosphere storage can allow human pathogens to flourish on produce surfaces (Brackett 1992). Concern has been expressed that reductions in surface populations reduces competition for space and nutrients thereby providing growth potential for pathogenic contaminants. In theory, this scenario can result in an unspoiled product that is unsafe for consumption. Berrang and others (1989ab) showed that pathogens grow to higher levels on produce stored under controlled atmosphere for extended shelf life than traditionally stored produce. While the cut salad industry traditionally uses natural spoilage as a food safety control measure, lengthening product shelf life would not be desirable if it increases the risk that pathogens would grow before spoilage is detectable. Secondly, a proliferation of postharvest spoilage organisms may compromise peel integrity and alter product pH thereby enhancing the survival and growth of human pathogens (Conway and others 2000).
These issues, along with primary methods of pathogen control for whole and fresh-cut produce are described in more detail below. Although the intent of this report is to describe methods to reduce or eliminate pathogens from produce, information regarding mitigation against non-pathogenic microorganisms is included in the text to illustrate the overall effectiveness of certain intervention technologies.
The concept of using multiple intervention methods is analogous to hurdle technology where two or more preservation technologies are used to prevent growth of microorganisms in or on foods (Leistner and Gorris 1995; Leistner 2000; Howard and Gonzalez 2001)
Hot water is used as a mitigation treatment of some fruits to control insects and postharvest plant pathogens that cause product spoilage. Fruits investigated for hot water treatment include apple, cherry, grapefruit, lemon, mango, melon, papaya, pear, or tomato (Breidt and others 2000; Puerta and Suslow 2001, personal communication, unreferenced ). Although adverse effects on color, texture, and flavor limit the usefulness of this treatment, hot water may have application as a sanitizer of produce, especially for fresh-cut products or unpasteurized juices where inedible outer rinds, skins or peels are discarded during processing. Pao and Davis (1999) determined that immersion of oranges in hot water (70 °C [158 °F] for 2 min, or 80 °C [176 °F] for 1 min) effectively reduced Escherichia coli on overall fruit surfaces by 5 log CFU/cm2, although reductions on the stem-end tissue were not as great. One disadvantage is that thermally treated produce might not be considered "fresh" by FDA based on 21 CFR part 101.95 (CFR 2000a).
The hygiene and temperature of water used during the handling of produce are of primary importance. Immersion of warm whole or fresh-cut produce in cool process solutions may induce infiltration of the solution (including contaminating microorganisms) into the product through openings in the peel such as stem-end vascular tissue, lenticels, stomata, puncture wounds, or other physical disruptions. Research by Bartz (1982), Bartz and Showalter (1981) and Showalter (1979) showed that bacteria in a cool (20 to 22 °C) (68 to 71.6 °F) aqueous suspension penetrate into stem tissue of warm tomatoes after a 10 min exposure. A negative temperature differential of 15 °C (77°F) allowed the infiltration of Salmonella Montevideo into the core of tomatoes at significantly higher rates than without a temperature differential (Zhuang and others 1995). The issue of infiltration is of special concern during hydrocooling where water is used to cool the product. It is imperative that water used for this purpose be sanitary and free of human pathogens.
Buchanan, Edelson, Miller and others (1999) determined that E. coli O157:H7 can penetrate into the core of warm apples placed in a cool suspension of the pathogen. Results of Burnett and others (2000) suggest that this same pathogen may infiltrate through apple floral tubes regardless of temperature differences although infiltration was greater for apples under a negative temperature differential. These studies point out the importance of maintaining adequate disinfectant levels to eliminate pathogens in water from dump tanks or other handling procedures before they have the opportunity to penetrate into the produce interior. It should be noted that temperatures in hot water dump tanks that are used to kill insect pests might aid survival of some pathogens. In a recent salmonellosis outbreak from Brazilian mangoes, the hot water treatment to kill fruit flies was at 46 to 47 °C (114.8 to 116.6 °F) for 65 to 90 min (Anonymous 2000). This was followed by a cooling procedure that could have caused internalization of the salmonellae into the fruit. Alternatively, the salmonellae could have simply attached to structures on the peel surface and not crossed the peel barrier into the fruit interior.
It is well documented that microorganisms, including some human pathogens, are capable of crossing peel barriers to enter the interior of produce (Bartz, 1982, 1988, 1991; Bartz and Showalter 1981; Buchanan, Edelson, Miller and others 1999; Burnett and others 2000; Showalter 1979; Zhuang and others 1995). This internalization phenomenon deserves closer scrutiny since it is a viable hypothesis that could explain some disease outbreaks. Studies on possible infiltration under commercial handling conditions are warranted. It is important to reproduce field, handling, packing, and storage conditions during infiltration experiments. Also, mechanisms by which microorganisms cross peel barriers to enter the interior portions of produce are an obvious focal point for research. It should be noted that the usefulness of dye penetration as a model for bacterial internalization may be limited since dyes can readily penetrate through tissue fissures too small for the passage of microbial cells (Pao and others 2001).
Upon soaking cut lettuce in suspensions (109 CFU/mL) of E. coli O157:H7 for 24 h at various temperatures, the pathogen penetrated into cut edges to a greater degree at 4 °C (39.2 °F) than at higher temperatures (Takeuchi and Frank 2000). Cells penetrated the cut lettuce tissue to an average depth of 74 µm at 4 °C (39.2 °F) and were unaffected by treatment with chlorine. Penetration was lower at higher incubation temperatures. In a study on apples, Burnett and others (2000) determined that E. coli O157:H7 penetrated damaged tissue around puncture wounds to a depth of 70 µm. It has also been reported that produce affected by postharvest soft rot may harbor human pathogens at a higher frequency than healthy produce (Wells and Butterfield 1997). The mechanism by which this harborage occurs is not clearly understood, although compromised peel integrity and pH changes may each play a role.
Washing efficiency varies with commodity, type of washing system, type of soil, contact time, detergent, and water temperature. In one study, brushwashing of oranges in plain water reduced the surface microbial population approximately 60 to 70% compared to 90% reduction when a sanitizer was included (Winniczuk 1994). In several studies on chemical sanitizers, simple rinsing of produce in plain water reduces the surface populations although the reduction is usually well less than 1 log. A concern regarding washing system efficiency is the quality of wash water, especially if the water is recycled and not treated prior to reuse. The use of disinfectant chemicals in wash water provides a barrier to cross contamination of produce. Research on new or more efficient methods to physically remove microorganisms from produce surfaces may be warranted.
The most common forms of free chlorine include liquid chlorine and hypochlorites. (Chlorine dioxide and acidified sodium chlorite will be discussed in the next section.) Liquid chlorine and hypochlorites are generally used in the 50 to 200 ppm concentration range with a contact time of 1 to 2 min to sanitize produce surfaces and processing equipment. Higher concentrations have been investigated for use on seeds for sprout production. Hypochlorous acid (HOCl) is the form of free available chlorine that has the highest bactericidal activity against a broad range of microorganisms. In aqueous solutions, the equilibrium between hypochlorous acid (HOCl) and the hypochlorite ion (OCl¯) is pH dependent with the concentration of HOCl increasing as pH decreases. Typically, pH values between 6.0 and 7.5 are used in sanitizer solutions to minimize corrosion of equipment while yielding acceptable chlorine efficacy. HOCl concentration is also significantly affected by temperature, presence of organic matter, light, air, and metals. For example, increasing levels of organic matter decreases HOCl concentration and overall antimicrobial activity. Maximum solubility in water is observed near 4 °C (39.2 °F); however, it has been suggested that the temperature of processing water should be maintained at least 10 °C (50 °F) higher than that of produce items in order to reduce the possibility of microbial infiltration caused by a temperature-generated pressure differential. The opportunity for infiltration of microorganisms is also minimized when the sanitary condition of the water is maintained. There are readily available commercial systems for inline monitoring and application of chlorine to maintain water cleanliness. This is particularly applicable to water used in dump tanks or for cleaning or cooling purposes.
Effects of chlorine on bacterial pathogens inoculated onto produce have been investigated with mixed results. Studies indicate those chlorine concentrations traditionally used with produce (<200 ppm) are not particularly effective at reducing microbial populations on lettuce. Survival of E. coli O157:H7 on cut lettuce pieces after submersion for 90 s in a solution of 20 ppm chlorine at 20 or 50 °C (68 or 122 °F) was not significantly different from the non chlorine treatment (Li and others 2001). Spray treatment of lettuce with 200 ppm chlorine was no more effective at removing E. coli O157:H7 than treatment with deionized water (Beuchat 1999). Increasing the exposure time from 1 to 5 min did not result in an increased kill. Likewise, Adams and others (1989) indicated that a standardized washing procedure for lettuce leaves was only slightly improved with inclusion of 100 ppm chlorine over tap water alone. Although a reduction of pH of the chlorine solution to between 4.5 and 5.0 increased lethality up to 4-fold, longer wash times (from 5 to 30 min) did not result in increased removal of microorganisms.
Research reported by Nguyen-the and Carlin (1994) suggests that inactivation of L. monocytogenes on vegetables by chlorine is limited. Zhang and Farber (1996) showed that treatment of shredded lettuce and cabbage with 200 ppm chlorine for 10 min reduced the population of L. monocytogenes by 1.7 and 1.2 log CFU/g, respectively. Reductions were only marginally greater when exposure time was increased from 1 to 10 min. Similarly, 10-minute exposures of Yersinia enterocolitica on shredded lettuce to 100 and 300 ppm chlorine resulted in population reductions of roughly 2 to 3 log (Escudero and others 1999). Results at 4 °C (39.2 °F) and 22 °C (71.6 °F) were not significantly different (P<0.05). In this same study, a combination of 100 ppm chlorine and 0.5% lactic acid inactivated Y. enterocolitica by greater than 6 log. These results suggest that Y. enterocolitica may be more sensitive to chlorine than some other pathogens. Brackett (1987) reported that the reduction in numbers of L. monocytogenes on Brussels sprouts changed from 90% (dipped 10 s in sterile water without chlorine) to 99% with the addition of 200 ppm chlorine. When inoculated into cracks of mature green tomatoes, Salmonella Montevideo survived treatment with 100 ppm chlorine (Wei and others 1995).
Treatment of produce with higher concentrations of chlorine (>500 ppm) has been studied. For example, sprouts have unique attributes and microbiological issues that have required investigations of non-traditional sanitation regimens. Treatment of alfalfa seeds and sprouts with chlorine to control salmonellae and E. coli O157:H7 has been studied (Jaquette and others 1996; Beuchat and Ryu 1997; Taormina and Beuchat 1999a, 1999b). Chlorine concentrations up to 100 ppm reduced populations of pathogens on alfalfa seeds; however, concentrations between 100 and 1000 ppm were not more effective (Jaquette and others 1996). Treatment of alfalfa sprouts for 2 min with a 500 ppm chlorine dip reduced salmonellae populations by 3.4 log per gram, and, after treatment with 2000 ppm chlorine, salmonellae populations were undetectable (<1 CFU/g) (Beuchat and Ryu 1997). The effect of chlorine treatment on sensory aspects of the sprouts was not reported. Escherichia coli O157:H7 populations were reduced significantly after exposure to Ca(OCl)2 at 500 and 1000 ppm; however, treatment with 20,000 ppm Ca(OCl)2 did not eliminate this microorganism from seeds (Taormina and Beuchat 1999a). Application of 2000 ppm sodium or calcium hypochlorite significantly reduced the population of E. coli O157:H7 on germinated alfalfa seeds but did not control growth of the pathogen on sprouts during the sprouting process (Taormina and Beuchat 1999b).
Beuchat and others (1998) showed that the maximum reduction in human pathogen populations on apples, tomatoes, and lettuce was 2.3 log CFU/cm2 after dipping in solutions of 2000 ppm chlorine for 1 min. On fresh-cut cantaloupe cubes, 2000 ppm chlorine resulted in less than a 90% reduction in viable cells of several strains of salmonellae (Beuchat and Ryu 1997). Populations of salmonellae or E. coli O157:H7 inoculated onto the surfaces of cantaloupes and honeydew melons were reduced between 2.6 and 3.8 log CFU (as compared to a water wash control) when treated for 3 min with 2000 ppm sodium hypochlorite or 1200 ppm acidified sodium chlorite (Park and Beuchat 1999). These treatments were less effective when applied to asparagus spears, thereby indicating that it may be necessary to customize sanitation treatments for different types of produce. Populations of Shigella sonnei inoculated onto whole parsley leaves were reduced more than 7 log CFU/g after treatment for 5 min with 250 ppm free chlorine (Wu and others 2000).
Reduction in populations of microflora on whole and fresh-cut produce is dependent upon the type of produce and the type of natural microflora present. Senter and others (1985) determined that total plate counts and Enterobacteriaceae populations on tomato surfaces decreased when chlorine levels of process water were raised from about 115 to 225 ppm. Pao and Davis (1999) showed that populations of E. coli inoculated onto orange surfaces were reduced more than 2 log CFU/cm2 after immersion in 200 ppm chlorine at 30 °C (86 °F) for 8 min. This reduction was only slightly higher than that resulting from immersion in deionized water alone. Murdock and Brokaw (1958) used water containing 20 to 50 ppm free chlorine to reduce total microbial populations on the surface of oranges by 92 to 99%, as compared to 79% for oranges washed in water. Winniczuk (1994) determined that dipping washed oranges in 1000 ppm HOCl for 15 s reduced the microbial population on the surface by about 90%, as compared to 60% for control oranges dipped in plain water. Populations of E. coli inoculated onto lettuce leaves and broccoli florets were generally reduced <1 log CFU/g after a 5 min dip in 100 ppm free chlorine compared to a plain water dip (Behrsing and others 2000).
Results of Mazollier (1988) indicated that microbial reductions on leafy salad greens were essentially the same when treated with 50 or 200 ppm chlorine. Total microbial populations were reduced about 1000-fold when lettuce was dipped in water containing 300 ppm total chlorine, but no effect was seen against microbial populations on red cabbage or carrots (Garg and others 1990). Coliform bacteria were reduced by 81% on parsley, 93% on lettuce, 98% on strawberries, and 85% on coriander after a 10-min contact time in a solution of 300 ppm chlorine (Lopez and others 1988). Microbial populations of cut potato strips were not effectively controlled by dips in 300 ppm hypochlorite (Gunes and others 1997). Treatment of honeydew melons and cantaloupes with 200 ppm hypochlorite significantly (P<0.05) reduced surface microbial populations compared to water-washed controls (Ayhan and others 1998).
Since chlorine reacts with organic matter, components leaching from tissues of cut produce surfaces may neutralize some of the chlorine before it reaches microbial cells, thereby reducing its effectiveness. Additionally, crevices, cracks, and small fissures in produce, along with the hydrophobic nature of the waxy cuticle on the surface of many fruit and vegetables, may prevent chlorine and other sanitizers from reaching the microorganisms. Surfactants, detergents, and solvents, alone or coupled with physical manipulation such as brushing, may be used to reduce hydrophobicity or remove part of the wax to increase exposure of microorganisms to sanitizers. However, such treatments may cause deterioration of sensory quality, thereby limiting their usefulness to applications just prior to consumption (Adams and others 1989; Zhang and Farber 1996).
There is less information about the effectiveness of ClO2 than HOCl as a sanitizer for produce. As with HOCl, microbial susceptibility to ClO2 differs with strain and environmental conditions of application. A population of L. monocytogenes inoculated onto shredded lettuce and cabbage leaves was reduced an additional 1.1 and 0.8 log at 4 and 22 °C (39.2 and 71.6 °F), respectively, after treatment with 5 ppm ClO2 for 10 min when compared to washing in tap water (Zhang and Farber 1996). Use of ClO2 gas reduced the numbers of E. coli O157:H7 on injured green pepper surfaces (Han and others 2000). Treatment of surface-injured green peppers with 0.6 and 1.2 ppm ClO2 gas reduced populations of E. coli O157:H7 by 3.0 and 6.4 log cycles, respectively. These researchers noted that no significant growth of E. coli O157:H7 was observed on uninjured pepper surfaces, but significant growth occurred on injured pepper surfaces within 24 h at 37 °C (98.6 °F). The use of ClO2 in a gaseous state, as opposed to an aqueous solution, warrants further study.
Roberts and Reymond (1994) demonstrated mortality of postharvest spoilage fungi to ClO2. Greater than 99% kill of conidia or sporangiophores was observed after 1 min in water containing 3 or 5 ppm ClO2. Fungal populations on conveying equipment were reduced upon treatment with foam containing 14 to 18 ppm ClO2. Costilow and others (1984) reported that 2.5 ppm ClO2 was effective against microorganisms in wash water, but concentrations as high as 105 ppm did not reduce the microflora in or on cucumbers. Similar results were reported by Reina and others (1995). Immersion of oranges in 100 ppm chlorine dioxide at 30 °C (86 °F) for 8 min produced a 3-log reduction of non-pathogenic E. coli compared to about a 2-log reduction when immersed in deionized water only (Pao and Davis 1999).
Acidified sodium chlorite has been approved for use on certain meats, seafood, poultry, and raw fruits and vegetables as either a spray or dip in the range of 500 to 1200 ppm (CFR 2000d). Reactive intermediates of this compound are highly oxidative with broad spectrum germicidal activity. Applications of 500 ppm acidified ClO2 significantly reduced populations of E. coli O157:H7 (>1 log) on germinated alfalfa seeds, but did not control the growth of the pathogen during the sprouting process (Taormina and Beuchat 1999b). Park and Beuchat (1999) showed that acidified sodium chlorite has a substantial antimicrobial effect against E. coli O157:H7 and salmonellae inoculated onto cantaloupes, honeydew melons and asparagus spears. Pathogen reductions were in the range of 3 log. There is a need for more published information on the general usefulness of acidified sodium chlorite for produce.
As with most sanitizers, iodophors are more active against vegetative cells than bacterial spores. Decimal reduction values for vegetative bacterial cells are between 3 and 15 s at 6 to 13 ppm available iodine at neutral pH (Hays and others 1967; Mosley and others 1976; Gray and Hsu 1979). D values for spores of Bacilllus cereus, Bacillus subtilis, and C. botulinum Type A treated with 10 to 100 ppm of iodophor are 10- to 1000-fold greater than for vegetative cells (Odlaug 1981). Although iodophors are not approved for direct food contact, they might have some usefulness for treatment of produce items that are peeled before consumption. This type of use would require regulatory approval and a demonstration that produce treated by these compounds are safe for consumption.
Quat sanitizers form a residual antimicrobial film when applied to most hard surfaces and are relatively stable to organic compounds. They are most effective when used at pH 6 to 10, and are not compatible with acidic environments, soaps or anionic detergents. Although they are not approved for direct food contact, quats may have some limited usefulness with whole produce that must be peeled prior to consumption. As with iodine compounds, direct food contact would require regulatory approval and a demonstration that produce treated by quats is safe for consumption.
Brown and Schubert (1987) determined that a 30 s exposure of oranges to a 500 ppm quat solution reduced Xanthomonas campestris pv. vesicatoria as effectively as 150 - 250 ppm chlorine for 2 min. The surface microflora of oranges brushwashed in water and dipped in 200 ppm quat for 15 s was reduced about 95% compared to 60% for washed oranges dipped in plain water (Winniczuk 1994).
In contrast to their use as preservatives, organic acids, primarily lactic acid, are also successfully used as sanitizers on food animal carcasses and may have potential for application to produce surfaces for the purpose of reducing populations of microorganisms. Treatment with citric acid in the form of lemon juice has been shown to reduce populations of Salmonella Typhi inoculated onto cubes of papaya and jicama (Fernandez Escartin and others 1989). Castillo and Escartin (1994) investigated survival of C. jejuni on cubes of watermelon and papaya treated at room temperature with lemon juice. Six hours after treatment, populations of Campylobacter jejuni ranged from 0 to 14.3% of the original inoculum on cubes treated with lemon juice, and from 7.7 to 61.8% on cubes not treated with lemon juice. The antimicrobial activity was more pronounced on papaya than watermelon.
Use of acetic acid to inactivate pathogenic bacteria on fresh parsley was studied by Karapinar and Gonul (1992). Populations of Y. enterocolitica inoculated onto parsley leaves were reduced > 7 log cycles after washing for 15 min in solutions of 2% acetic acid or 40% vinegar. Treatment in 5% acetic acid for 30 min did not result in any recovery of aerobic bacteria, while treatment with vinegar gave a 3 to 6 log decrease in aerobic counts, depending upon vinegar concentration and exposure time. Treatment of whole parsley leaves for 5 min at 21 °C (69.8 °F) with vinegar (7.6% acetic acid) reduced populations of S. sonnei more than 7 log per gram (Wu and others 2000). Vinegar and lemon juice have potential as inexpensive, simple household sanitizers; however, possible negative sensory effects when used on produce would be a disadvantage.
Various combinations of acetic acid, lactic acid and chlorine were observed to reduce populations of L. monocytogenes on shredded lettuce (Zhang and Farber 1996). Lactic or acetic acids in combination with 100 ppm chlorine were slightly more antagonistic toward L. monocytogenes than either acid or chlorine alone; however, the increased antagonism might be due to an additive effect of the combined compounds or due to an increase in hypochlorous acid at the reduced pH levels of the acid combinations. A 2 min dip in 5% acetic acid at room temperature was the most effective treatment of several investigated for reducing populations of E. coli O157:H7 inoculated onto apple surfaces (Wright and others 2000). The 5% acetic acid treatment reduced the population more than 3 log CFU/cm2 as compared to less than a 3 log reduction by a commercial preparation with 80 ppm peroxyacetic acid. It was noteworthy that the 2 min dip treatment with a commercial 0.3% phosphoric acid-based fruit wash caused sublethal injury to E. coli O157:H7 as measured by a comparison of counts on selective and non-selective media.
Antimicrobial activity varies among the organic acids. Citric acid was much less effective than tartaric acid in preventing growth of microorganisms on salad vegetables (Shapiro and Holder 1960). A concentration of 1500 ppm citric acid did not affect bacterial growth, while treatment with 1500 ppm tartaric acid resulted in a 10-fold reduction in counts after 4 d at 10 °C (50 °F). Priepke and others (1976) reported that microbial populations of cut lettuce, endive, carrots, celery, radishes, and green onions treated with 2000 ppm sorbate and/or 10,000 ppm ascorbate, then stored 10 d at 4.4 °C (40 °F), were not effectively controlled. Coliforms and fecal coliforms were reduced about 2 and 1 log/g, respectively, on mixed salad vegetables treated with 1% lactic acid (Torriani and others 1997). In the same study, treatment of the mixed vegetables with a 3% sterile permeate from a culture of Lactobacillus casei reduced the total mesophilic count about 5 log/g and prevented growth of coliforms, enterococci, and Aeromonas hydrophila after 6 d at 8 °C (46.4 °F).
Orthophosphoric acid with added surfactants is commonly used in the citrus processing industry for both cleaning and sanitizing purposes. Pao and Davis (1999) demonstrated that immersion of oranges in a 200 ppm phosphoric acid/surfactant solution decreased E. coli populations only slightly better than immersion in deionized water alone. Winniczuk (1994) determined that dipping oranges for 15 s in 500 ppm of a commercial phosphoric acid surfactant solution after brushwashing in water reduced surface populations approximately 85%, as compared to 60% for brushwashing alone.
Nearly 100-fold reductions in total counts and fecal coliforms on cut-salad mixtures were observed after treatment with 90 ppm peroxyacetic (peracetic) acid or with 100 ppm chlorine (Masson 1990). The subsequent inhibition of microbial growth during storage of salads was attributed to residual peracetic activity. Microbial populations on the surface of oranges were reduced about 85% after brushwashing in water followed with a 15 s dip in 200 ppm peracetic acid, compared to a 60% reduction on oranges that were brushwashed and dipped in plain water (Winniczuk 1994).
Confidential research results from one company indicated that a static 2-min treatment of inoculated tomatoes with a sanitizer formulation containing 60 ppm peracetic acid in combination with surfactants reduced populations of Salmonella Javiana, L. monocytogenes, and E. coli O157:H7 by 96%, 99.96% and 99.5%, respectively, compared with treatment in sterile water. Similar results were obtained with a second sanitizer formulation containing 40 ppm peracetic and surfactants.
Use of H2O2 on whole and fresh-cut produce has been investigated in recent years. Salmonella populations on alfalfa sprouts were reduced approximately 2 log CFU/g after treatment for 2 min with 2% H2O2 or 200 ppm chlorine (Beuchat and Ryu 1997). Less than 1 log CFU/g reduction was observed on cantaloupe cubes under similar test conditions. Treatment with 5% H2O2 bleached sprouts and cantaloupe cubes. Treatment of whole cantaloupes, honeydew melons, and asparagus spears with 1% H2O2 was less effective at reducing levels of inoculated salmonellae and E. coli O157:H7 than hypochlorite, acidified sodium chlorite or a peracetic acid-containing sanitizer (Park and Beuchat 1999). Use of a 1% H2O2 spray on alfalfa seeds and sprouts did not control growth of E. coli O157:H7 (Taormina and Beuchat 1999b). H2O2 (3%), alone or in combination with 2 or 5% acetic acid sprayed onto green peppers, reduced Shigella populations approximately 5 log cycles, compared to less than a 1-log reduction by water alone (Peters 1995). In the same study, Shigella inoculated onto lettuce was reduced approximately 4 log after dipping in H2O2 combined with either 2 or 5% acetic acid; however, obvious visual defects were noted on the treated lettuce. The same treatment gave similar results for E. coli O157:H7 inoculated onto broccoli florets or tomatoes with minimal visual defects.
Microbial populations on whole cantaloupes, grapes, prunes, raisins, walnuts, and pistachios were significantly reduced upon treatment with H2O2 vapor (Sapers and Simmons 1998). Treatment by dipping in H2O2 solution reduced microbial populations on fresh-cut bell peppers, cucumber, zucchini, cantaloupe, and honeydew melon, but did not alter sensory characteristics. Treatment of other produce was not as successful. H2O2 vapor concentrations necessary to control Pseudomonas tolaasii caused mushrooms to turn brown, while anthocyanin-bleaching occurred in strawberries and raspberries. Shredded lettuce was severely browned upon dipping in a solution of H2O2. Combinations of 5% H2O2 with acidic surfactants at 50 °C (122 °F ) produced a 3 to 4 log reduction of non-pathogenic E. coli inoculated onto the surfaces of unwaxed Golden Delicious apples (Sapers and others 1999). Further research is necessary to determine the usefulness of H2O2 treatment on other fruits and vegetables.
Ozone is an effective treatment for drinking water and will inactivate bacteria, fungi, viruses, and protozoa (Peeters and others 1989; Korich and others 1990; Finch and Fairbairn 1991; Restaino and others 1995). According to Restaino and others (1995), bacterial pathogens such as Salmonella Typhimurium, Y. enterocolitica, S. aureus, and L. monocytogenes are sensitive to treatment with 20 ppm ozone in water. Finch and Fairbairn (1991) investigated the sensitivity of enteric viruses to ozone, while Korich and others (1990) reported on the ozone inactivation of protozoa such as Cryptosporidium parvum. Treatment of C. parvum oocysts with 1 ppm ozone for 5 min resulted in < 1 log inactivation. In the same study, Giardia spp. cysts were more sensitive than C. parvum to ozone treatment. Peeters and others (1989) reported that 2.27 ppm ozone treatment for 8 min eliminated the infectivity of 5x105 C. parvum oocysts in water.
Treatment with ozonated water can extend the shelf life of apples, grapes, oranges, pears, raspberries, and strawberries by reducing microbial populations and by oxidation of ethylene to retard ripening (Beuchat 1998). Microbial populations on berries and oranges were reduced by treatment with 2-3 ppm and 40 ppm, respectively. Kim and others (1999a) reported a 2 log/g reduction in total counts for shredded lettuce suspended in water ozonated with 1.3 mM ozone at a flow rate of 0.5 L/min.
In contrast to the use of ozone as an initial treatment to reduce microbial populations on produce surfaces, ozone gas has also been investigated for use during storage of various foods, including fish (Haraguchi and others 1969), poultry (Sheldon and Brown 1986), peanuts and cottonseed meal (Dwankanath and others 1968), pork, beef, dairy products, eggs, mushrooms, potatoes, and fruits (Kaess and Weidemann 1968; Gammon and Kerelak 1973). Apples stored in an atmosphere containing ozone had reduced incidents of spoilage (Bazarova 1982). Fungal growth during storage of blackberries was inhibited by 0.1 to 0.3 ppm ozone (Barth and others 1995). Treatment of grapes by ozone increased shelf life and reduced fungal growth (Sarig and others 1996). Spoilage of vegetables such as onions, potatoes, and sugar beets was reduced upon storage in an ozone containing atmosphere (Kim and others 1999b).
Due to its strong oxidizing activity, ozone may cause physiological injury of produce (Horvath and others 1985). Bananas treated with ozone developed black spots after 8 d of exposure to 25 to 30 ppm gaseous ozone. Carrots exposed to ozone gas during storage had a lighter, less intense color than untreated carrots (Liew and Prange 1994). Ozone can also cause corrosion of metals and other materials in processing equipment. It is capital intensive and may be difficult to monitor and control in situations where highly variable organic loads are likely to occur. As with other sanitizers, employee safety and health issues must be addressed and appropriate safeguards must be in place when using ozone as a sanitizing agent. Since ozone produces toxic vapors, adequate ventilation is necessary for employee safety. However, since it has excellent ability to penetrate and does not leave a residue, ozone may have usefulness for treatment of process water, food contact surfaces, or whole produce. Industry representatives indicate that the postharvest use of ozone for treatment of produce is increasing.
In a review on irradiation and produce, Thayer and Rajkowski (1999) state, "To date, relatively little effort has been applied to the control of foodborne pathogens on fresh foods. However, ionizing irradiation has recently been used to eliminate Escherichia coli O157:H7 from apple juice, Toxoplasma gondii and/or Cyclospora cayetanensis from raspberries, and E. coli O157:H7 and salmonellae from seed and sprouts." Research on the effectiveness of irradiation against human pathogens has been conducted mostly on food products of animal origin (Mossel and Stegeman 1985; Farkas 1989; Monk and others 1995); however, Rajkowski and Thayer (2000) reported that salmonellae were not recovered from alfalfa sprouts irradiated with 0.5 kGy even though the seeds used to produce the sprouts contained detectable levels of the pathogen. These researchers concluded that ionizing radiation can be used to reduce pathogen populations on sprouts. Buchanan and others (1998) determined that 1.8 kGy will produce a 5-log reduction of E. coli O157:H7 in apple juice. These same researchers reported that acid-resistant stationary phase cells of enterohemorrhagic E. coli are more resistant to irradiation than non-acid-resistant cells (Buchanan, Edelson, and Boyd 1999).
Doses in the range of <1 to 3 kGy have been shown to reduce or eliminate populations of foodborne pathogens, postharvest spoilage organisms, and other microorganisms on produce (Moy 1983; Urbain 1986; Farkas 1997). Most medium and high level doses are not appropriate for produce because they can cause sensory defects (visual, texture, and flavor) and/or accelerated senescence due to irreparable damage to DNA and proteins (Thomas 1986; Barkai-Golan 1992). Treatment of unpasteurized orange juice with 3 kGy electron-beam irradiation reduced E. coli populations inoculated into the juice by at least 5 log, but had unacceptable sensory consequences (Parish and Goodrich 2000; personal communication; unreferenced). Strawberry shelf life can be extended with treatments in the range of 2 to 3 kGy (Sommer and Maxie 1966; Zegota 1988; Marcotte 1992; Diehl 1995). Maxie and others (1971) asserted that strawberry is the only domestic fruit or vegetable with adequate potential to utilize irradiation for shelf life extension, since other commodities do not tolerate dosage levels needed to control spoilage. Research conducted since that time suggests that irradiation can be an important treatment to enhance safety of other types of produce. Postharvest disease incidence in apples and Bosc pears was reduced after 0.3 to 0.9 kGy irradiation treatment (Drake and others 1999). Disease incidence of Anjou pears was not reduced.
Use of ionizing radiation to eliminate insect pests, and to control postharvest spoilage organisms on fresh produce has been reviewed (Clarke 1959; Willison 1963; Staden 1973; Moy 1983; CAST 1986, 1989; Barkai-Golan 1992; Wilkinson and Gould 1996) and guidelines for treatment have been issued (Anonymous 1991a, 1991b, 1993). Combinations of ionizing radiation with other treatments have been studied. A combination of 0.75 kGy irradiation with a 10 min dip in 50 °C (122°F) water provided much better control of postharvest spoilage organisms of papayas and mangoes than either treatment alone (Brodrick and van der Linde 1981). Neither irradiation (0.3 to 0.6 kGy), hot fungicide treatment, nor a combination of the two, satisfactorily prevented postharvest spoilage of mangoes (Johnson and others 1990). Higher doses of irradiation caused unacceptable peel blemishes. A combination of UV and gamma radiation was not more effective than either treatment alone at preventing storage rot of peaches (Lu and others 1993). Irradiation (0.43 kGy average dose) of segments from cut and peeled citrus fruits was not as effective as chemical preservatives at preventing spoilage during chilled storage (Hagenmaier and Baker 1998a).
The shelf life of packaged leaf vegetables stored at 10 °C (50 °F) was extended by treatment with 1 kGy (Langerak 1978). In this study, Enterobacteriaceae were eliminated on endive and the shelf life was extended from 1 (for nonirradiated) to 5 d. Chervin and Boisseau (1994) concluded that irradiation of shredded carrots was superior to chlorination and spin-drying. Microbial populations (measured as total plate counts) of shredded carrots treated with 0.5 kGy or chlorine and stored 9 d under refrigeration were 1300 and 87,000 CFU/g, respectively (Hagenmaier and Baker 1998b). The same authors reported a similar reduction of microbial populations on cut iceberg lettuce treated with 0.19 kGy (Hagenmaier and Baker 1997). A combination of hot water dips and 1.0 kGy irradiation doubled the shelf life of mangoes from 25 to 50 d (El-Samahy and others 2000).
As discussed in the recent FDA report, "Kinetics of microbial inactivation for alternative food processing technologies" (FDA 2000), high intensity pulsed X-rays have been shown to reduce E. coli O157:H7 populations in ground beef by 3 log cycles, and to decrease Salmonella Senftenberg on turkey carcasses. Studies on the use of X-rays to inactivate pathogens on/in produce may be warranted.
Consumer acceptance of irradiated food remains questionable. A publication by USDA-ERS suggests that the number of consumers likely to purchase irradiated food has decreased in recent years from about 70% in 1996 to 50% in 2000 (Frenzen and others 2000). Additionally, there is a need to ensure that research on irradiation addresses sensory aspects, such as taste, appearance and texture, of produce.
The use of bacteriophage to reduce populations of Salmonella on fresh-cut fruit was recently reported (Leverentz and others 2001). Application of Salmonella-specific phages reduced populations about 3.5 log on honeydew melon slices (pH 5.8) stored at 5 or 10 °C (41 or 50 °F). Salmonellae were not reduced on apple slices possibly due to the fruit's lower pH (4.2). Use of phage for pathogen control deserves further investigation.
The concept of "induced resistance" of plants to microorganisms that cause pathologies in plant systems is worth noting (Hammerschmidt 1999). In recent years groups of researchers have begun to focus efforts on the mechanisms and signaling pathways plants use to resist disease. Additionally, biotech companies are engineering plants to resist pests. While speculative, it is conceivable that research on biocontrol efforts through induced resistance or genetic engineering could lead to plants that resist human pathogens in addition to plant pathogens.
| Mitigation Method | Advantages | Limitations | Comments on current use | Comments on research |
|---|---|---|---|---|
| Hypochlorite |
|
|||
| Acidified sodium chlorite | ||||
| Chlorine dioxide | ||||
| Bromine | ||||
| Iodine | ||||
| Trisodium phosphate | ||||
| Quaternary ammonium compounds | ||||
| Acids | ||||
| Hydrogen peroxide | ||||
| Ozone | ||||
| Irradiation | ||||
| Biocontrol |
[Anonymous]. 1991a. Code of good irradiation practice for insect disinfestation of fresh fruits (as a quarantine treatment) [ICGFI Document No. 7]. International Consultative Group on Food Irradiation. <http://www.iaea.or.at/programmes/rifa/icgfi/documents/publications.htm>. Accessed 2001 Sept 6.
[Anonymous]. 1991b. Irradiation as a quarantine treatment of fresh fruits and vegetables: report of a task force [ICGFI Document 13]. International Consultative Group on Food Irradiation. <http://www.iaea.or.at/programmes/rifa/icgfi/documents/publications.htm>. Accessed 2001 Sept 6.
[Anonymous]. 1993. F1355 - Guideline for the irradiation of fresh fruits for insect disinfestation as a quarantine treatment. [unknown]: Annual Year Book of the American Society for Testing and Materials (ASTM) Standards. Vol. 15.07.
[Anonymous]. 2000. DBMD traces Salmonella outbreak to mangoes. CDC/NCID Focus 9(4):1-2. <http://www.cdc.gov/ncidod/focus/index.htm> Accessed 2001 Sept 6.
Austin JW, Dodds KL, Blanchfield B, Farber JM. 1998. Growth and toxin production by Clostridium botulinum on inoculated fresh-cut packaged vegetables. J Food Prot 61(3):324-8.
Ayhan Z, Chism GW, Richter ER. 1998. The shelf life of minimally processed fresh cut melons. J Food Qual 21:29-40.
Barkai-Golan R. 1992. Suppression of postharvest pathogens of fresh fruits and vegetables by ionizing radiation. In: Rosenthal, editor. Electromagnetic Radiations in Food Science, I. Berlin: Springer-Verlag. p 155-94.
Barth MM, Zhou C, Mercier M, Payne FA. 1995. Ozone storage effects on anthocyanin content and fungal growth in blackberries. J Food Sci 60:1286-7.
Bartlett PG, Schmidt W. 1957. Surface-iodine complexes as germicides. Appl Microbiol 5:355-9.
Bartz JA, Showalter RK. 1981. Infiltration of tomatoes by aqueous bacterial suspensions. Phytopathology 71(5):515-8.
Bartz JA. 1982. Infiltration of tomatoes immersed at different temperatures to different depths in suspensions of Erwinia carotovora subsp. carotovora. Plant Disease 66(4):302-6.
Bartz JA. 1988. Potential for postharvest disease in tomato fruit infiltrated with chlorinated water. Plant Dis 72(1):9-13.
Bartz JA. 1991. Relation between resistance of tomato fruit to infiltration by Erwinia carotovora subsp. carotovora and bacterial soft rot. Plant Dis 75(2):152-5.
Bazarova VI. 1982. Use of ozone in storage of apples. Food Sci Technol Abstr 14(11):J1653.
Behrsing J, Winkler S, Franz P, Premier R. 2000. Efficacy of chlorine for inactivation of Escherichia coli on vegetables. Postharv Biol Technol 19:187-92.
Benarde MA, Snow WB, Olivieri OP, Davidson B. 1967. Kinetics and mechanism of bacterial disinfection by chlorine dioxide. Appl Microbiol 15:257-65.
Bennik MHJ, Van Overbeek W, Smid EJ, Gorris LGM. 1999. Biopreservation in modified atmosphere stored mungbean sprouts: the use of vegetable-associated bacteriocinogenic lactic acid bacteria to control the growth of Listeria monocytogenes. Lett Appl Microbiol 28:226-32.
Berrang ME, Brackett RE, Beuchat LR. 1989a. Growth of Listeria monocytogenes on fresh vegetables stored under controlled atmosphere. J Food Prot 52(10):702-5.
Berrang ME, Brackett RE, Beuchat LR. 1989b. Growth of Aeromonas hydrophila on fresh vegetables stored under a controlled atmosphere. Appl Environ Microbiol 55(9):2167-71.
Beuchat LR, Ryu J-H. 1997 Oct-Dec. Produce handling and processing practices: special issue. Emerg Infect Dis 3(4):459-65.
Beuchat LR. 1998. Surface decontamination of fruits and vegetables eaten raw: a review. World Health Organization, Food Safety Unit WHO/FSF/FOS/98.2. <www.who.int/fsf/fos982~1.pdf>. Accessed 2001 July 25.
Beuchat LR, Nail BV, Adler BB, Clavero MRS. 1998. Efficacy of spray application of chlorinated water in killing pathogenic bacteria on raw apples, tomatoes, and lettuce. J Food Prot 61(10):1305-11.
Beuchat LR. 1999. Survival of Enterohemorrhagic Escherichia coli O157:H7 in bovine feces applied to lettuce and the effectiveness of chlorinated water as a disinfectant. J Food Prot 62(8):845-9.
Beuchat LR. 2000. Use of sanitizers in raw fruit and vegetable processing. In: Alzamora SM, Tapia MS, Lopez-Malo A, editors. Minimally Processed Fruits and Vegetables: Fundamental Aspects and Applications. Gaithersburg [MD]: Aspen.
Bianchi A, Ricke SC, Cartwright AL, Gardner FA. 1994. A peroxidase catalyzed chemical dip for the reduction of Salmonella on chicken breast skin. J Food Prot 57:301-4.
Bowles BL, Sackitey SK, Williams AC. 1995. Inhibitory effects of flavor compounds on Staphylococcus aureus WRRC B124. J Food Safety 15:337-47.
Bowles BL, Juneja VK. 1998. Inhibition of food-borne bacterial pathogens by naturally occurring food additives. J Food Safety 18:101-12.
Brackett RE. 1987. Antimicrobial effect of chlorine on Listeria monocytogenes. J Food Prot 50(12):999-1003.
Brackett RE. 1992. Shelf stability and safety of fresh produce as influenced by sanitation and disinfection. J Food Prot 55(10):804-14.
Breidt R, Hayes JS, Fleming HP. 2000. Reduction of microflora on whole pickling cucumbers by blanching. J Food Sci 65:1354-8.
Brodrick HT, van der Linde HJ. 1981. Technological feasibility studies on combination treatments for subtropical fruits. Combination Processes in Food Irradiation, Proceedings Series. Vienna: International Atomic Energy Agency. p 141-52.
Brown GE, Schubert TS. 1987. Use of Xanthamonas campestris pv. vesicatoria to evaluate surface disinfectants for canker quarantine treatment of citrus fruit. Plant Dis 4:319-23.
Buchanan RL, Edelson SG, Snipes K, Boyd G. 1998. Inactivation of Escherichia coli O157:H7 in apple juice by irradiation. Appl Environ Microbiol 64(11):4533-5.
Buchanan RL, Edelson SG, Boyd G. 1999. Effects of pH and acid resistance on the radiation resistance of enterohemorrhagic Escherichia coli. J Food Prot 62:219-28.
Buchanan RL, Edelson SG, Miller RL, Sapers GM. 1999. Contamination of intact apples after immersion in an aqueous environment containing Escherichia coli O157:H7. J Food Prot 62(5):444-50.
Burnett SL, Chen J, Beuchat LR. 2000. Attachment of Escherichia coli 0157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl Environ Microbiol 66(11):4679-87.
Buta JG, Moline HE. 1998. Methyl jasmonate extends shelf life and reduces microbial contamination of fresh-cut celery and peppers. J Agric Food Chem 46:1253-6.
Calvente V, Benuzzi D, deTosetti MIS. 1999. Antagonistic action of siderophores from Rhodotorula glutinis upon the postharvest pathogen Penicillium expansum. Int Biodeter Biodeg 43:167-72.
Carlin F, Nguyen C, Morris CE. 1996. Influence of background microflora on Listeria monocytogenes on minimally processed fresh broad-leaved endive (Cichorium endivia var. latifolia). J Food Prot 59:698-703.
[CAST] Council for Agricultural Science and Technology. 1986. Ionizing energy in food processing and pest control: I. Wholesomeness of food treated with ionizing energy. Ames (IA): CAST. Report nr 109. 50 p.
[CAST] Council for Agricultural Science and Technology. 1989. Ionizing energy in food processing and pest control: II. Applications. Ames (IA): CAST. Report nr 115. 98 p.
Castillo A, Escartin EF. 1994. Survival of Campylobacter jejuni on sliced watermelon and papaya [a research note]. J Food Prot 57(2):166-8.
Cerrutti P, Alzamora SM, Vidales SL. 1997. Vanillin as an antimicrobial for producing shelf stable strawberry puree. J Food Sci 62:608-10.
[CFR] Code of Federal Regulations. 2000a. Title 21, Part 101.95. Food Labelling: "Fresh," "freshly frozen," "fresh frozen," "frozen fresh." Available from: <http://www.access.gpo.gov/nara/cfr/index.html>. Accessed 2001 Sept 6.
[CFR] Code of Federal Regulations. 2000b. Title 21, Part 110.3(o). Current Good Manufacturing Practice in Manufacturing, Packing, or Holding Human Food: Definitions. Available from: <http://www.access.gpo.gov/nara/cfr/index.html>. Accessed 2001 Sept 6.
[CFR] Code of Federal Regulations. 2000c. Title 21, Part 173.300. Secondary Direct Food Additives Permitted in Food for Human Consumption: Chlorine dioxide. Available from: <http://www.access.gpo.gov/nara/cfr/index.html>. Accessed 2001 Sept 6.
[CFR] Code of Federal Regulations. 2000d. Title 21, Part 173.325. Secondary Direct Food Additives Permitted in Food for Human Consumption: Acidified sodium chlorite solutions. Available from: <http://www.access.gpo.gov/nara/cfr/index.html>. Accessed 2001 Sept 6.
Chantaysakorn P, Richter RL. 2000. Antimicrobial properties of Pepsin-digested Lactoferrin added to carrot juice and filtrates of carrot juice. J Food Prot 63(3):376-80.
Cherry JP. 1999. Improving the safety of fresh produce with antimicrobials. Food Technol 53(11):54-7.
Chervin C, Boisseau P. 1994. Quality maintenance of "ready-to-eat" shredded carrots by gamma-irradiation. J Food Sci 59:359-61.
Clarke ID. 1959. Possible applications of ionizing radiations in the fruit, vegetable and related industries. Int J Appl Radiat Isot 6:175.
Conway WS, Leverentz B, Saftner RA. 2000. Survival and growth of Listeria monocytogenes on fresh-cut apple slices and its interaction with Glomerella cingulata and Penicillium expansum. Plant Dis 84:177-81.
Costilow RN, Uebersax MA, Ward PJ. 1984. Use of chlorine dioxide for controlling microorganisms during handling and storage of fresh cucumbers. J Food Sci 49:396-401.
Cousins CM, Allan CD. 1967. Sporicidal properties of some halogens. J Appl Bacteriol 30:168-74.
Delaquis PJ, Mazza G. 1995. Antimicrobial properties of isothiocyanates in food preservation. Food Technol 49(11):73-84.
Diehl JF. 1995. Safety of irradiated foods. 2nd revised ed. New York: Marcel Dekker, Inc.
Drake SR, Sanderson PG, Neven LG. 1999. Response of apple and winter pear fruit quality to irradiation as a quarantine treatment. J Food Proc Preserv 23:203-16.
Dwankanath CT, Rayner ET, Mann GE, Dollar FG. 1968. Reduction of aflatoxin levels in cottonseed and peanut meals by ozonation. J Am Oil Chem Soc 45:93-5.
El-Ghaouth A, Smilanick JL, Brown GE, Ippolito A, Wisniewski M, Wilson CL. 2000. Application of Candida saitoana and glycochitosan for the control of postharvest diseases of apple and citrus fruit under semi-commercial conditions. Plant Dis 84:243-8.
El-Samahy SK, Youssef BM, Askar AA, Swailam HMM. 2000. Microbiological and chemical properties of irradiated mango. J Food Safety 20:139-56.
Escudero ME, Velazquez L, Di Genaro MS, De Guzman AS. 1999. Effectiveness of various disinfectants in the elimination of Yersinia enterocolitica on fresh lettuce. J Food Prot 62:665-9.
Farber JM, Wang SL, Cai Y, Zhang S. 1998. Changes in populations of Listeria monocytogenes inoculated on packaged fresh-cut vegetables. J Food Prot 61(2):192-5.
Farkas J. 1989. Microbiological safety of irradiated foods. Int J Food Microbiol 9:1-15.
Farkas J. 1997. Physical methods of food preservation. In: Doyle MP, Beuchat LR, Monteville TJ, editors. Food microbiology: fundamentals and frontiers. Washington, DC: American Society for Microbiology. p 497-519.
Fatemi P, Frank JF. 1999. Inactivation of Listeria monocytogenes/Pseudomonas biofilms by peracid sanitizers. J Food Prot 62:761-5.
[FDA] Food and Drug Administration, Center for Food Safety and Applied Nutrition. 1998 Oct 26. Guide to minimize microbial food safety hazards for fresh fruits and vegetables [Guidance for Industry]. <http://www.foodsafety.gov/~dms/prodguid.html>. Accessed 2001 Aug 10.
[FDA] Food and Drug Administration, Center for Food Safety and Applied Nutrition. 2000. Kinetics of microbial inactivation for alternative food processing technologies. <http://vm.cfsan.fda.gov/~comm/ift-toc.html>. Accessed 2001 Aug 15.
Fernandez Escartin EF, Castillo Ayala A, Saldana Lozano J. 1989. Survival and growth of Salmonella and Shigella on sliced fresh fruit. J Food Prot 52(7):471-2.
Finch GR, Fairbairn N. 1991. Comparative inactivation of poliovirus type 3 and MS2 coliphage in demand-free phosphate buffer by using ozone. Appl Environ Microbiol 57(11):3121-6.
Foegeding PM, Busta FF. 1991. Chemical food preservatives. In: Block SE, editor. Disinfection, sterilization and preservation. 4th ed. Philadelphia (PA): Lea & Febiger.
Francis GA, Thomas C, O'Beirne D. 1999. The microbiological safety of minimally processed vegetables [review article]. Int J Food Sci Technol 34:1-22.
Frenzen PD, Majchrowicz A, Buzby JC, Imhoff B. 2000. Consumer acceptance of irradiated meat and poultry products. Ag Info Bull 757.
Fukao T, Sawada H, Ohta Y. 2000. Combined effect of hop resins and sodium hexametaphosphate against certain strains of Escherichia coli. J Food Prot 63:735-40.
Gammon R, Kerelak K. 1973. Gaseous sterilization of foods. Am Inst Chem Engr Symp Ser 69:91.
Garg N, Churey JJ, Splittstoesser DF. 1990. Effect of processing conditions on the microflora of fresh-cut vegetables. J Food Prot 53:701-3.
Gershenfeld L, Witlin B. 1949. Evaluation of the antibacterial efficiency of dilute solutions of free halogens. J Am Pharm Assoc, Sci Ed. 38:411-4.
Gray RJ, Hsu D. 1979. Effectiveness of iodophor in the destruction of Vibrio parahaemolyticus. J Food Sci 44:1097-100.
Gunes G, Splittstoesser DL, Lee CY. 1997. Microbial quality of fresh potatoes: effect of minimal processing. J Food Prot 60:863-6.
Hagenmaier RD, Baker RA. 1997. Low-dose irradiation of cut iceberg lettuce in modified atmosphere packaging. J Ag Food Chem 45:2864-8.
Hagenmaier RD, Baker RA. 1998a. An evaluation of gamma irradiation for preservation of citrus salads in flexible packaging. Proc Florida State Hort Soc 110:243-5.
Hagenmaier RD, Baker RA. 1998b. Microbial population of shredded carrot in modified atmosphere packaging as related to irradiation treatment. J Food Sci 63:162-4.
Hammerschmidt R. 1999. Induced disease resistance: how do induced plants stop pathogens? Physiol Mol Plant Pathol 55:77-84.
Han Y, Sherman DM, Linton RH, Nielsen SS, Nelson PE. 2000. The effects of washing and chlorine dioxide gas on survival and attachment of Escherichia coli O157:H7 to green pepper surfaces. Food Microbiol 17:521-33.
Haraguchi T, Slimidu U, Aiso K. 1969. Preserving effect of ozone on fish. Bull Jpn Soc Sci Fish 35(915-20).
Hays H, Elliker PR, Sandine WE. 1967. Microbial destruction by low concentrations of hypochlorite and iodophor germicides in alkaline and acidified water. Appl Microbiol 15:575-81.
Horvath M, Bilitzky L, Huttner J. 1985. Ozone. Amsterdam: Elsevier. 68-74, 304-31 p.
Howard LR, Gonzalez AR. 2001. Food safety and produce operations: What is the future? Hort Sci 36:33-9.
Isshiki K, Tokuoka K, Mori R, Chiba S. 1992. Preliminary examination of allyl isothiocyanate vapor for food preservation. Biosci Biotech Biochem 56:1476-7.
Janisiewicz WJ, Bors B. 1995. Development of a microbial community of bacterial and yeast antagonists to control wound-invading postharvest pathogens of fruit. Appl Environ Microbiol 61:3261-7.
Janisiewicz WJ, Conway WS, Leverentz B. 1999. Biological control of postharvest decays of apple can prevent growth of
Escherichia coli O157:H7 in apple wounds. J Food Prot 62:1372-5.
Jaquette CB, Beuchat LR, Mahon BE. 1996. Efficacy of chlorine and heat treatment in killing Salmonella stanley
inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl Environ
Microbiol 62(6):2212-5.
Jilbert WR. 1988. Quality control and sanitation aspects of fresh squeezed citrus juice processing. In: Matthews RF, editor. Food industry short course proceedings. Gainesville (FL): Florida IFT and University of Florida Extension Service.
Johnson GI, Boag TS, Cooke AW, Izard M, Panitz M, Sangchote S. 1990. Interaction of post harvest disease control treatments and gamma irradiation on mangoes. Ann Appl Biol 116:245-57.
Juven BJ, Pierson MD. 1996. Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation. J Food Prot 59(11):1233-41.
Kaess G, Weidemann JF. 1968. Ozone treatment of chilled beef. J Food Technol 3:325-33.
Karapinar M, Gonul SA. 1992. Removal of Yersinia enterocolitica from fresh parsley by washing with acetic acid or vinegar. Int J Food Microbiol 16:261-4.
Kenney SJ, Burnett SL, Beuchat LR. 2001. Location of Escherichia coli 0157:H7 on and in apples as affected by bruising, washing, and rubbing. J Food Prot 64(9):1328-33.
Kim JG, Yousef AE, Chism GW. 1999a. Use of ozone to inactivate microorganisms on lettuce. J Food Safety 19:17-34.
Kim JG, Yousef AE, Dave S. 1999b. Application of ozone for enhancing the microbiological safety and quality of foods: a review. J Food Prot 62(9):1071-87.
Korich DG, Mead JR, Madore MS, Sinclair NA, Sterling CR. 1990. Effects of ozone, chlorine dioxide, chlorine, and monochloramine on Cryptosporidium parvum oocyst viability. Appl Environ Microbiol 56(5):1423-8.
Korsten L, De Jager ES, De Villiers EE, Lourens A, Kotze JM, Wehner FC. 1995. Evaluation of bacterial epiphytes isolated from avocado leaf and fruit surfaces for biocontrol of avocado postharvest disease. Plant Dis 79:1149-56.
Kristofferson T. 1958. Mode of action of hypochlorite sanitizers with and without sodium bromide. J Dairy Sci 41:942-9.
Lacey RW. 1979. Antibacterial activity of providone iodine towards non-sporing bacteria. J Appl Bacteriol 46:443-9.
Langerak DI. 1978. The influence of irradiation and packaging on the quality of prepacked vegetables. Ann Nutr Aliment 32:569-86.
Lawrence CA, Carpenter CM, Naylor-Foote AWC. 1957. Iodophors as disinfectants. J Am Pharm Assoc 46:500-5.
Leibinger W, Breuker B, Hahn M, Mendgen K. 1997. Control of postharvest pathogens and colonization of the apple surface by antagonistic microorganisms in the field. Phytopathology 87(11):1103-10.
Leistner L, Gorris LGM. 1995. Food preservation by hurdle technology. Trends Food Sci Technol 6:41-6.
Leistner L. 2000. Basic aspects of food preservation by hurdle technology. Intl J Food Microbiol 55:181-6.
Leverentz B, Conway WS, Alavidze Z, Janisiewicz WJ, Fuchs Y, Camp MJ, Chighladze E, Sulakvelidze A. 2001. Examination of bacteriophage as a biocontrol method for Salmonella on fresh-cut fruit: a model study. J Food Prot 64(8):1116-21.
Li Y, Brackett RE, Chen J, Beuchat LR. 2001. Survival and growth of Escherichia coli 0157:H7 inoculated onto cut lettuce before or after heating in chlorinated water, followed by storage at 5 °C or 15 °C. J Food Prot 64(3):305-9.
Liao CH. 1989. Antagonism of Pseudomonas putida strain PP22 to phytopathogenic bacteria and its potential use as a biocontrol agent. Plant Dis 73:223-6.
Liao C-H, Sapers GM. 2000. Attachment and growth of Salmonella chester on apple fruit and in vivo response of attached bacteria to sanitizer treatments. J Food Prot 63(7):876-83.
Liew CL, Prange RK. 1994. Effect of ozone and storage temperature on postharvest diseases and physiology of carrots (Caucus carota L.). J Am Soc Hortic Sci 119:563-7.
Lis-Balchin M, Hart S, Deans SG, Eaglesham E. 1996. Comparison of the pharmacological and antimicrobial action of commercial plant essential oils. J Herbs Spices Medic Plants 4:69-86.
Lopez LV, Romero JR, Urbina J. 1988. Eficiencia de desinfectantes en vegetales y frutas. Alimentos 13:25-30.
Lu JY, Lukombo SM, Stevens C, Khan VA, Wilson CL, Pusey PL, Chaultz E. 1993. Low dose UV and gamma radiation on storage
rot and physiochemical changes in peaches. J Food Qual 16:301-9.
Marcotte M. 1992. Irradiated strawberries enter the U.S. market. Food Technol 46(5):80-6.
Marriott NG. 1999. Principles of Food Sanitation. 4th ed. Gaithersburg (MD): Aspen. p 147-9.
Masson RB. 1990. Recherche de nouveax disinfectants pour les produits de 4eme gamme. In: Proc Congress Produits de 4eme Gamme et de 5eme Gamme; Brussels. C.E.R.I.A. p 101.
Maxie EC, Sommer NF, Mitchell FG. 1971. Infeasibility of irradiating fresh fruits and vegetables. Hort Sci 6:202-4.
Mazollier Jr. 1988. IVe gamme. Lavage-desinfection des salades. Infros-Ctifl 41:19.
Monk JD, Beuchat LR, Doyle MP. 1995. Irradiation inactivation of food-borne microorganisms. J Food Prot 58:197-208.
Mosley EB, Elliker PR, Hays H. 1976. Destruction of food spoilage indicator and pathogenic organisms by various germicides in solution and on a stainless steel surface. J Milk Food Technol 39:830-6.
Mossel DAA, Stegeman H. 1985. Irradiation: An effective mode of processing food for safety. In: Food Irradiation Processing. Proc Int Symp on Food Irrad Processing; 1985 March 4-8; Washington. International Atomic agency for Food and Agriculture Organization of the United Nations. p 251-79.
Moy JH. 1983. Radurization and radication: fruits and vegetables. In: Josephson ES, Peterson MS, editors. Preservation of food by ionizing radiation. Boca Raton (FL): CRC Pr. p 83-108.
Murdock DI, Brokaw CH. 1958. Sanitary control in processing citrus concentrates: some specific sources of microbial contamination from fruit bins to extractors. Food Technol 12:573-6.
[NACMCF] National Advisory Committee on Microbiological Criteria for Foods. 1999. Microbiological safety evaluations and recommendations on fresh produce. Food Control 10:117-43.
Nguyen-the C, Carlin F. 1994. The microbiology of minimally processed fresh fruits and vegetables. Crit Rev Food Sci Nutr 34(4):371-401.
Odlaug TE. 1981. Antimicrobial activity of halogens. J Food Prot 44(8):608-13.
Ortenzio LF, Stuart LS. 1964. A standard test for efficacy of germicides and acceptability of residual disinfecting activity in swimming pool water. J Assoc Off Agric Chem 47:540-7.
Pao S, Davis CL. 1999. Enhancing microbiological safety of fresh orange juice by fruit immersion in hot water and chemical sanitizers. J Food Prot 62(7):756-60.
Pao S, Davis CL, Kelsey DF, Petracek PD. 1999. Sanitizing effects of fruit waxes at high pH and temperature on orange surfaces inoculated with Escherichia coli. J Food Sci 64(2):359-62.
Pao S, Davis CL, Kelsey DF. 2000. Efficacy of alkaline washing for the decontamination of orange fruit surfaces inoculated with Escherichia coli. J Food Prot 63(7):961-4.
Pao S, Davis CL, Parish ME. 2001. Microscopic observation and processing validation of fruit sanitizing treatments for the enhanced microbiological safety of fresh orange juice. J Food Prot 64:310-4.
Parish ME, Davidson PM. 1993. Methods for evaluation. In: Davidson PM, Branen AL, editors. Antimicrobials in Foods. New York: Marcel Dekker.
Parish ME, Narciso JA, Friedrich LM. 1997. Survival of Salmonellae in orange juice. J Food Safety 17:273-81.
Park CM, Beuchat LR. 1999. Evaluation of sanitizers for killing Escherichia coli O157:H7, Salmonella and naturally occurring microorganisms on cantaloupes, honeydew melons, and asparagus. Dairy Food Environ Sanit 19:842-7.
Peeters JE, Ares Mazas E, Masschelein WJ, Villacorta Martinez de Maturana I, Debacker E. 1989. Effect of disinfection of drinking water with ozone or chlorine dioxide on survival of Cryposporidium parvum oocysts. Appl Environ Microbiol 55(6):1519-22.
Peters DL. 1995. Control of enteric pathogenic bacteria on fresh produce [Master of Science]. Lincoln: Univ of Nebraska Graduate College.
Piagentini AM, Pirovani ME, Guemes DR, Di Pentima JH, Tessi MA. 1997. Survival and growth of Salmonella hadar on minimally processed cabbage as influenced by storage abuse conditions. J Food Sci 62:616-8.
Priepke PE, Wei LS, Nelson AI. 1976. Refrigerated storage of prepackaged salad vegetables. J Food Sci 41:379-82.
Rajkowski KT, Thayer DW. 2000. Reduction of Salmonella spp. and strains of Escherichia coli O157:H7 by gamma radiation of inoculated sprouts. J Food Prot 63(7):871-5.
Reina LD, Fleming HP, Humphries EG. 1995. Microbiological control of cucumber hydrocooling water with chlorine dioxide. J Food Prot 58(5):541-6.
Restaino L, Frampton EW, Hemphill JB, Palnikar P. 1995. Efficacy of ozonated water against against various food-related microorganisms. Appl Environ Microbiol 61(9):3471-5.
Roberts RG, Reymond ST. 1994. Chlorine dioxide for reduction of postharvest pathogen inoculum during handling of tree fruits. Appl Environ Microbiol 60(8):2864-8.
Sapers GM, Simmons GF. 1998. Hydrogen peroxide disinfection of minimally processed fruits and vegetables. Food Technol 52(2):48-52.
Sapers GM, Miller RL, Mattrazzo AM. 1999. Effectiveness of sanitizing agents in inactivating Escherichia coli in golden delicious apples. J Food Sci 64(4):734-7.
Sarig P, Zahavi T, Zutkhi Y, Yannai S, Lisker N, Ben-Arie R. 1996. Ozone for control of postharvest decay of table grapes caused by Rhizopus stolonifer. Physiol Mol Plant Pathol 48:403-15.
Senter SD, Cox NA, Bailey JS, Forbus Jr. WR. 1985. Microbiological changes in fresh market tomatoes during packing operations [a research note]. J Food Sci 50:254-5.
Seymour IJ. 1999. Review of current industry practice on fruit and vegetable decontamination [review no. 14]. Gloucestershire (UK): Campden & Chorleywood Food Research Association. 1-38 p.
Shapiro JE, Holder IA. 1960. Effect of antibiotic and chemical dips on the microflora of packaged salad mix. Appl Microbiol 8:341.
Sheldon BW, Brown AL. 1986. Efficacy of ozone as a disinfectant for poultry carcasses and chill water. J Food Sci 51(2):305-9.
Shere L, Kelley MJ, Richardson JH. 1962. Effect of bromide hypochlorite bactericides on microorganisms. Appl Microbiol 10:538-41.
Showalter RK. 1979. Postharvest water intake by tomatoes. Hort Sci 14(2):125.
Smilanick JL, Denis-Arrue R. 1992. Control of green mold of lemons with Pseudomonas species. Plant Dis 76:481-5.
Somers EB, Schoeni JL, Wong ACL. 1994. Effect of trisodium phosphate on biofilm and planktonic cells of Campylobacter jejuni, Escherichia coli O157:H7, Listeria monocytogenes and Salmonella typhimurium. Int J Food Microbiol 22:269-76.
Sommer NF, Maxie EG. 1966. Recent research on the irradiation of fruits and vegetables. Food Irradiation. Vienna: International Atomic Energy Agency. p 571.
Staden OL. 1973. A review of the potential of fruit and vegetable irradiation. Sci Hortic 1:291-308.
Stanley D. 1994. Yeasts and bacteria battle decay. Agric Res 42(5):8-9.
Takeuchi K, Frank JF. 2000. Penetration of Escherichia coli O157:H7 into lettuce tissues as affected by inoculum size and temperature and the effect of chlorine treatment on cell viability. J Food Prot 63(4):434-40.
Taormina PJ, Beuchat LR. 1999a. Behavior of enterohemorrhagic Escherichia coli O157:H7 on alfalfa sprouts during the sprouting process as influenced by treatments with various chemicals. J Food Prot 62(8):850-6.
Taormina PJ, Beuchat LR. 1999b. Comparison of chemical treatments to eliminate enterohemorrhagic Escherichia coli O157:H7 on alfalfa seeds. J Food Prot 62(4):318-24.
Teo AY-L, Ravishankar S, Sizer CE. 2001. Effect of low-temperature, high-pressure treatment on the survival of Escherichia coli 0157:H7 and Salmonella in unpasteurized fruit juices. J Food Prot 64(8):1122-7.
Thayer DW, Josephson ES, Brynjolfsson A, Giddings GG. 1996. Radiation pasteurization of food. Council for Agricultural Science and Technology Issue Paper Nr. 7(Apr):1-12.
Thayer DW, Rajkowski KT. 1999. Developments in irradiation of fresh fruits and vegetables. Food Technol 53(11):62-5.
Thomas P. 1986. Radiation preservation of foods of plant origin. V. Temperate fruits: pome fruits, stone fruits, and berries. Crit Rev Fd Sci Technol 24:357-400.
Tokuoka K, Isshiki K. 1994. Possibility of application of Allylisothiocyanate vapor for food preservation. Nippon Shokuhin Kogyo Gakkaishi 41(9):595-9.
Torriani S, Orsi C, Vescovo M. 1997. Potential of Lactobacillus casei, culture permeate, and lactic acid to control microorganisms in ready-to-use vegetables. J Food Prot 60:1564-7.
Ulate-Rodriguez J, Schafer HW, Zottola EA, Davidson PM. 1997. Inhibition of Listeria monocytogenes, Escherichia coli 0157:H7, and Micrococcus lutens by linear furanocoumarins in a model food system. J Food Prot 60:1050-4.
Urbain WM. 1986. Fruits, vegetables, and nuts. In: Schweigert BS, editor. Food Irradiation. Orlando (FL): Academic Pr. p 170-216. (Food Science and Technology, A series of monographs).
Usall J, Teixido N, Fons E, Vinas I. 2000. Biological control of blue mould on apple by a strain of Candida sake under several controlled atmosphere conditions. Int J Food Microbiol 58:83-92.
Vescovo M, Torriani S, Orsi C, Macchiarolo F, Scolari G. 1996. Application of antimicrobial-producing lactic acid bacteria to control pathogens in ready-to-use vegetables. J Appl Bacteriol 81:113-9.
Walker HW, LaGrange WS. 1991. Sanitation in food manufacturing operations. In: Block SE, editor. Disinfection, sterilization, and preservation. 4th ed. Philadelphia (PA): Lea & Febiger.
Wan J, Wilcock A, Coventry MJ. 1998. The effect of essential oils of basil on the growth of Aeromonas hydrophila and Pseudomonas fluorescens. J Appl Microbiol 84:152-8.
Wei CI, Huang TS, Kim JM, Lin WF, Tamplin ML, Bartz JA. 1995. Growth and survival of Salmonella montevideo on tomatoes and disinfection with chlorinated water. J Food Prot 58(8):829-36.
Wells JM, Butterfield JE. 1997. Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Dis 81(8):867-72.
Wilkinson VM, Gould GW. 1996. Food Irradiation: a reference guide. Oxford (UK): Butterworth - Heinemann.
Willison SR. 1963. Ionizing radiation for the control of plant pathogens: a review. Can Plant Dis (Survey) 43:39.
Winniczuk PP. 1994. Effects of sanitizing compounds on the microflora of orange fruit surfaces and orange juice [M.S.]. Gainesville (FL): Univ of Florida Graduate School.
Wright JR, Sumner SS, Hackney CR, Pierson MD, Zoecklein BW. 2000. Reduction of Escherichia coli O157:H7 on apples using wash and chemical sanitizer treatments. Dairy Food Environ Sanit:120-6.
Wu FM, Doyle MP, Beuchat LR, Wells JG, Mintz ED, Swaminathan B. 2000. Fate of Shigella sonnei on parsley and methods of disinfection. J Food Prot 63(5):568-72.
Xu L. 1999. Use of ozone to improve the safety of fresh fruits and vegetables. Food Technol 53(10):58-61, 3.
Zegota H. 1988. Suitability of Dukat strawberries for studying effects on shelf life of irradiation combined with cold storage. Z Levensm Unters Forsch 187:111-4.
Zhang S, Farber JM. 1996. The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiol 13:311-21.
Zhao T, Doyle MP, Besser RE. 1993. Fate of enterohemorrhagic Escherichia coli O157:H7 in apple cider with and without preservatives. Appl Environ Microbiol 59(8):2526-30.
Zhao J, Cranston PM. 1995. Microbial decontamination of black pepper by ozone and the effect of the treatment on volatile oil constituents of the spice. J Sci Food Agric 68:11-8.
Zhuang R-Y, Beuchat LR, Angulo FJ. 1995. Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Appl Environ Microbiol 61(6):2127-31.
Zhuang R-Y, Beuchat LR. 1996. Effectiveness of trisodium phosphate for killing Salmonella montevideo on tomatoes. Lett Appl Microbiol 22:97-100.
Hypertext updated by dav 2001-DEC-31