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Irradiation could provide a kill step to enhance safety of fresh and fresh-cut produce, but

challenges remain for full commercial application.

of Fresh Fruits and VegetablesIrradIatIon

Recent research has demonstrated that irradiation effectively kills bacterial pathogens on fresh and fresh-cut produce, but retailer and consumer acceptance of this technology remains an obstacle to its commercial application.

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By Xuetong Fan, Brendan a. niemira, and anuradha Prakash

Consumption of fresh and fresh-cut fruits and vegetables in the United States has increased

every year in the past decade, because of their convenience and nutritional benefits. Unfortunately, the increasing consumption of fresh produce has been accompanied with an increase in the number of outbreaks and recalls due to con-tamination with human pathogens.

Fresh fruits and vegetables carry the potential risk of contamination because they are generally grown in open fields with potential exposure to enteric pathogens from soil, irrigation water, manure, wildlife, or other sources. Unlike meat and meat products to which a kill step (thermal treatment) is applied before

being consumed, fresh produce is often consumed without cooking or other treatments that could eliminate pathogens that may be present.

The recent Escherichia coli O157:H7 illness outbreaks and product recalls of spinach, lettuce, and other leafy greens, most notably in 2006 and 2007, have gained much media atten-tion and raised public concerns over produce safety. The fresh produce industry is in need of a kill step to ensure the safety of produce. Ionizing radiation is known to effectively eliminate human pathogens such as E. coli O157:H7 on fresh produce.

This article reviews the latest knowledge about irradiation inactivation of human pathogens on and in fresh-cut produce and its impact on the quality of produce. It also highlights current develop-ments in irradiation regulation and labeling, the challenge and opportunity for commercial application, and research needs.

Types of Ionizing RadiationRadiation is in every part of our lives, and we encounter it every day in the natural environment. Common types of radiation include radio frequency, visible light, infrared light, microwave, and ultraviolet light. More energetic forms of radiation, such as gamma-ray, X-ray, and electron beams are called ionizing radiations because they are capable of producing ions, electronically charged atoms or molecules. All three types of ionizing radiation have the same mechanisms in terms of their effects on foods and microorganisms.

Water is the principal target of ionizing radiation. The radiolysis of water generates free radicals, and these radicals, in turn, attack other

components such as DNA in micro-organisms. Each type of ionizing radiation has its own advantages and disadvantages. For example, gamma rays and X-rays have higher penetration ability than electron beams. However, gamma rays are emitted by radioactive materials, such as cobalt-60 and cesium-137, while generation of X-rays is a relatively inefficient and energy-intensive process. Most energy (about 90%) is lost to heat during the conversion of electron beams into X-rays. Electron beams have a low penetration ability, even though the electron beam generators can be switched on and off and do not involve radioactive materials.

Effectiveness in Inactivating PathogensHistorically, the high radiation doses used in attempts to produce a sterile or shelf-stable fruit or vegetable commodity have resulted in unpalatable products. Of specific interest within the context of modern produce processing is the

potential for incorporating lower irradiation doses, lower than 3 kGy, as one of several “hurdles” in an otherwise conventional produce processing system. Recent research has consistently shown that irradiation effectively kills bacterial pathogens on fresh and fresh-cut produce (Smith and Pillai, 2004; Niemira and Fan, 2005). This efficacy holds for human bacterial pathogens such as E. coli O157:H7, Salmonella, and Listeria monocytogenes, as well as for bacterial phytopathogens and spoilage organisms.

Irradiation doses that will result in a 1-log reduction in bacterial pathogens are typically in the range of 0.2–0.8 kGy. In contrast, patho-genic viruses and fungi are generally

more resistant to irradiation, often requiring 1–3 kGy to achieve 1-log reduction (Niemira and Fan, 2005). To achieve meaningful reductions of viruses and fungi, the doses required are typically above what most produce will tolerate.

In terms of food safety, it should be noted that on an annual basis, the majority of minor foodborne illnesses are caused by viruses (67%), while the majority of serious foodborne illnesses resulting in hospitaliza-tions and deaths (60% and 72%, respectively) stem from bacterial pathogens (Mead et al., 1999). As an intervention, irradiation is thus most suited for elimination of the most serious safety threats for consumers of fruits and vegetables.

The antimicrobial efficacy of irradiation is influenced by a number of factors, including the pathogen being targeted as the primary safety concern, the type of produce being treated, the condition of the fruit or vegetable

Water is the principal target of ionizing radiation. The radiolysis of water generates free radicals, and these radicals,

in turn, attack other components such as DNA in microorganisms.

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(whole vs cored, peeled, cut, chopped, etc.), the atmosphere in which it is packaged, and other commodity-specific factors (Niemira and Fan, 2005). Like any other industrial food processing technology, the methodological details of time, temperature, han-dling, and irradiation protocols must undergo process validation for the product being treated. For example, irradiation protocols developed for elimination of E. coli O157:H7 from leafy greens may not achieve the required food

safety and quality benchmarks if applied for the elimination of Salmonella from tomatoes.

One area of recent research focuses on determining the ability of irradiation to kill internalized, biofilm-associated, or otherwise protected pathogens. These protec-tive environments dramatically reduce the efficacy of chemicals and other conventional treatment options, often by orders of mag-nitude (Niemira and Fan, 2005). Initial data in this emerging field of research suggest that Salmonella

and E. coli O157:H7 in biofilms are effectively eliminated by irradia-tion, although the specific response depends on the pathogen type and maturity (Niemira, 2007).

Cells of E. coli O157:H7 that are internalized appear to be more resistant to irradiation than surface-associated cells (Table 1). At 1 kGy, pathogens such as E. coli O157:H7 on the surface of fresh-cut produce can be reduced by 3–8 logs, while internalized pathogens are only reduced by 2–3 logs. Additional research is needed to more fully understand the influence of internalization on pathogens, and on the efficacy of irradiation and other treatments.

Quality of Irradiated Fresh ProduceAt low dose levels (1 kGy or less), most fresh-cut vegetables show little change in appearance, flavor, color, and texture, although some products can lose firmness. As an example, the appearance of irradi-ated spinach was similar to that of the non-irradiated samples after 14 days storage at 4°C (Figure 1). Some vegetables such as fresh-cut cilantro can tolerate 3.85 kGy of radiation (Foley et al., 2004). In fact, the destruction of spoilage organisms increases the shelf life of most fresh and fresh-cut vegetables (Prakash and Foley, 2004; Niemira and Fan, 2005). The response to irradiation is spe-cific to product, and even similar varieties, as shown in studies on various lettuce types (Niemira et al., 2002), exhibit differences in texture and respiration rates.

• appearance and Leakage. Irradiation’s effect on permeability and functionality of cell membranes can result in electrolyte leakage and loss of tissue integrity. These effects are limited at dose levels below 1 kGy, but at higher dose levels, electrolyte leakage may cause a soggy and wilted appearance. The increase in electrolyte leakage varies among vegetables (Table 2). In a study of 13 vegetables, Fan and Sokorai (2005) observed that red cabbage, broccoli, and endive had the lowest increases in electrolyte leakage, while celery, carrot, and green onion had the most increases in leakage.

• texture. Irradiation may induce the loss of firmness (softening) in some fruits (Gunes et al., 2000; Palekar et al., 2004). Irradiation-induced loss of firmness is related to partial depolymeriza-tion of cell-wall polysaccharides, cellulose, and pectin and to changes in activity of the cell-wall enzymes pectinmethylesterase and polygalacturonase that act on pectic substrates. However, the loss of firmness can be mitigated by dipping diced tomatoes and

FiguRe 1. Appearance of spinach—non-irradiated (0 kgy, left) and irradiated (1 kgy, right)—after 14 days of storage at 4°C. The visual quality of irradiated spinach is similar to that of non-irradiated samples.

Phot

o by

Pau

l Pie

rlott

Table 1. Dose required to achieve a 1 log reduction for E. coli O157:H7 inoculated on or in fresh-cut produce, then irradiated with gamma rays. FrOm NIemIra aNd FaN (2007).

d10 value (kGy)

PrOduct ON surFace INsIde

Iceberg lettuce 0.14 0.30

boston lettuce 0.14 0.45

Red leaf lettuce 0.12 0.35

Green leaf lettuce 0.12 0.37

Romaine lettuce 0.21 0.39

baby spinach 0.24 0.45

Green onion, long cut 0.26 0.42

Green onion, short cut 0.28 0.42

irradiation’s effect on permeability and functionality of cell membranes can result in electrolyte leakage and loss of tissue integrity.

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fresh-cut apples in a calcium solution prior to irradiation (Gunes et al., 2000; Prakash et al., 2007) and by storing the products in modified-atmosphere packaging (Boynton et al., 2006).

Irradiated (1 kGy) cilantro (Fan et al., 2003a) and lettuce (Fan et al., 2003b) showed some softening, but after a few days of storage, there was no significant difference between irradiated and non-irradiated samples. Other products,

such as celery (Prakash et al., 2000), mushroom slices (Koorapati et al., 2004), and shredded carrots (Hagenmaier and Baker, 1998), also showed no change in firmness.

• Flavor and aroma. At low dose levels (≤1 kGy), few if any effects on flavor and aroma are observed in fresh and fresh-cut vegetables. A decrease in character-istic aroma of cilantro (Fan et al., 2003a) and off-flavor of

Bell peppers (Masson, 2002) has been observed at doses of ≥3 kGy. Changes in flavor and aroma of fresh vegetables are highly correlated with microbial spoilage. Thus, irradiation generally inhibits or delays development of off-flavors related to growth of spoilage organisms.

• nutritional Quality. At low dose levels (≤1 kGy), the effects on nutritional quality are minimal. Irradiation can reduce ascorbic acid

(vitamin C) in some vegetables, but the decrease is generally insignifi-cant, given the natural variation observed in fresh produce, and does not exceed the decrease seen during storage (Fan and Sokorai, 2002). Irradiation converts ascorbic acid to dehydroascorbic acid, both of which exhibit biological activity and are readily interconvertible. Irradiation can also increase phe-nolic content of certain vegetables,

thus increasing their antioxidant capacity (Fan, 2005). However, since phenolic compounds are also responsible for the browning reactions in vegetables, their increase is not a desired outcome.

In general, the effect of irradiation on quality of fresh and fresh-cut vegetables is minimal. In those cases where significant changes are seen at effective dose levels, effects on texture, color, or browning can be minimized by combining irradiation with other technologies such as calcium dips, modified-atmosphere packaging, or antibrowning agents.

Regulatory approval, labeling, and SafetyCurrently in the U.S., irradiation of whole fruits and vegetables is approved only for insect control and shelf-life extension, with a maximum allowable dose of 1 kGy (Table 3). The use of irradiation for the purpose of enhancing microbial food safety has not been approved by the Food and Drug Administration. However, FDA is evaluating a petition, filed by the Food Irradiation Coalition, asking for the use of irradiation to enhance safety of fresh-cut produce at doses up to 4.5 kGy.

Under current FDA rules, foods that have been irradiated must bear both a “Radura” logo and a statement that the food has been “treated with

radiation” or “treated by irradiation.” Earlier last year, FDA proposed a change in the labeling of irradiated foods (FDA, 2007b). Under the proposed rule, only irradiated foods in which irradiation causes a material change in the food would need to be labeled with the Radura logo and either of those statements. The term “material change” refers to a change in the organoleptic, nutritional, or functional properties of a food. In

leakaGe (%)

veGetable 0 kGy 0.5 1 1.5 2.0 2.5 3.0 lsd0.05b

broccoli 0.6 0.7 0.7 0.8 0.7 1.2 1.1 0.4

endive 1.5 1.7 1.8 2.3 2.2 3.2 3.1 0.6

Red cabbage 1.3 1.4 1.4 1.9 1.8 2.0 2.5 0.5

Green leaf lettuce 2.5 3.1 3.9 3.4 3.2 4.4 4.8 0.8

Parsley 2.1 2.1 2.6 3.0 3.7 3.7 4.7 1.1

Romaine lettuce 1.4 2.8 3.3 4.1 3.8 5.7 5.1 1.5

Iceberg lettuce 1.4 1.9 2.4 2.6 3.2 3.8 4.3 1.1

Spinach 2.8 3.4 3.3 3.8 4.1 5.4 6.2 1.2

Red leaf lettuce 3.5 3.7 4.6 5.0 5.0 6.8 8.5 1.3

Celery 2.1 3.4 3.3 4.9 6.9 8.4 9.8 1.3

Cilantro 1.4 1.8 2.1 2.4 3.1 4.3 4.1 0.9

Green onion 3.8 5.2 7.1 7.0 9.5 12.5 12.4 1.6

Carrots 2.8 3.1 3.8 4.4 5.7 6.1 8.6 1.0

Table 2. electrolyte leakage of fresh-cut vegetables as a function of radiation dosea. mOdIFIed FrOm FaN aNd sOkOraI (2005).

a Vegetables were irradiated with 0, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0 kGy of gamma radiation at 5°C in air, then electrolyte leakage was measured.

b Least significant difference at P<0.05.

At low dose levels (≤1 kgy), few if any effects on flavor and aroma are observed in fresh and fresh-cut vegetables.

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addition, FDA would allow petitions for the use of alternative labeling, such as “pasteurized” or “pasteuriza-tion,” for a food that has been treated by irradiation, where the irradiation results in the same level of pathogen reduction as thermal pasteurization. These changes are still under consideration by FDA, and a final ruling has not yet been made.

In multi-generational studies, animals fed irradiation-sterilized foods throughout their life were healthy and nutritionally satisfied, with no evidence of any negative nutritional or developmental effects. More recently, FDA has investigated the possibility that furan, a possible carcinogen present in canned meats, soups, and many other conventional thermally processed foods, might also be produced during irradiation. Studies demonstrated that irradiation at 5 kGy did not induce detectable levels of furan in most fresh-cut fruits and vegetables. In those few fruits where furan was detectable after irradiation, the levels were much lower than those in many thermally processed foods (Fan and Sokorai, 2007).

Consumer acceptanceAdoption of irradiation for food applications has been a slow process. The limited number of foods approved by regulatory agencies, cost, consumer reluctance to accept irradiated foods, and the public’s uncertainty of this technology may contribute to its minimal commercialization.

Studies on marketing of irradi-ated foods have demonstrated that consumers are more willing to buy irradiated foods after they are provided information about the process (Bhumiratana et al., 2007). Typically, fewer than half will buy the irradiated food if given a choice between an irradiated product and the non-irradiated product. If consumers are first educated about food irradiation and food safety, most of them will buy the product in these marketing tests.

In a survey conducted by The Packer (Anonymous, 2007), 63% of growers/shippers believe that the produce industry should push for irradiation or similar treatments if produce is not damaged in the process; 40% of packers think the industry should push for irradiation or similar treatments, with the same percentage undecided; more than 30% of growers/shippers think consumers are ready to buy irradiated produce, particularly leafy greens; but only 25% of retailers think consumers are ready to buy irradiated produce, leafy greens in particular—about 7% of retailers stock irradiated produce.

It seems that enthusiasm about the commercial application of irradiation on fresh produce decreases from growers/shippers, to packers, to retailers, and to consumers. Therefore, educating retailers and consumers about irradiation processing may be needed to advance the commercial applications of this technology.

PackagingPackaging is another important aspect of food irradiation. FDA has approved about 10 polymeric

packaging materials for use during irradiation of prepackaged foods. Package materials currently used by the produce industry are diversified. Most polymeric packaging materials that are used by the produce industry have been approved by FDA. The agency allows industry to submit requests for exemption from regulation if the use of the substance in the food-contact article results in a dietary concentration at or below 0.5 ppb. As a result, Proveit, on behalf of Sadex Inc., has successfully petitioned FDA to expand the packaging materials for irradiated foods (FDA, 2007a).

Specifically, FDA allows the use of all approved packaging materials to package food being irradiated, provided that the packaged food is already permitted by FDA, the packaging materials are subjected to radiation doses not exceeding 3 kGy, and the packaged food is irradiated in an oxygen-free envi-ronment or while the food is frozen and contained under vacuum.

Unfortunately, the exemptions cannot be applied for fresh-cut produce because fresh-cut produce cannot be frozen or processed

Table 3. Foods permitted to be irradiated. FrOm Fda (2007c).

tyPe OF FOOd PurPOse maxImum dOse (kGy)

Fresh, non-heated processed pork control of Trichinella spiralis 1

Fresh produce Growth and maturation inhibition 1

Fresh produce arthropod disinfection 1

Dry or dehydrated enzyme preparations microbial disinfection 10

Dry or dehydrated spices/seasonings microbial disinfection 30

Fresh or frozen, uncooked poultry products Pathogen control 3

Frozen packaged meats (solely NaSa) sterilization 44

Refrigerated, uncooked meat products Pathogen control 4.5

Frozen uncooked meat products Pathogen control 7

Fresh shell eggs control of Salmonella 3.0

Seeds for sprouting control of microbial pathogens 8.0

Fresh or frozen molluscan shellfish control of Vibrio species and other foodborne pathogens

5.5

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in an oxygen-free environment (even though nitrogen is used for flushing some packages of leafy vegetables). Fresh-cut produce is usually packaged with oxygen levels of 1–20% and therefore does not qualify under the exemption.

The majority of fresh-cut produce is packaged in polyolefin film bags, which themselves are mostly approved under 21 CFR 179.45 without any limitation on oxygen environment. However, these polyolefins may contain additives that have not been approved for use during irradiation. Therefore, packaging materials intended for irradiation of prepackaged fresh-cut produce in the presence of oxygen may still need premarket approval.

In addition, packaging materials are very complex, and emerging new packaging materials present a challenge to FDA. For example, polyethylene terephthalate (PET) films are approved by FDA under 21 CFR 179.45, but rigid and semi-rigid PET polymers are not (Komolprasert, 2007). New materials such as degradable and antimicrobial packages, adjuvants (antioxidants, stabiliz-ers, etc.), plasticizers, colorants, and adsorbent pads may need more research before being evaluated and approved by FDA (Komolprasert, 2007).

additional Research NeededMore studies on sensory analysis of irradi-ated fresh produce are needed. In addition, similar to studies on consumer acceptance of ground beef and chicken, consumer acceptance of irradiated produce needs to be evaluated, especially within the context of recent outbreaks related to produce.

Fresh produce is unique because fresh-cut fruits and vegetables are promoted as fresh and nutritious. However, it is unknown whether the word “irradiation” will affect the consumer perception of “freshness” of irradiated produce. In its recent proposal of labeling changes, FDA (2007b) expressed interest in receiving information on whether the control of foodborne pathogens changes the characteristics of food in a way outside of normal variation, which would therefore require additional labeling to inform the consumer of such changes. Thus, studies are needed to determine irradiation conditions that would

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Anonymous. 2007. Produce pulse. The Packer 114(6): A1, A4.

Bhumiratana, N., Belden, L.K., and Bruhn, C.M. 2007. Effect of an educational program on attitudes of California consumers toward food irradiation. Food Protection Trends 27: 744-748.

Boynton, B.B., Welt, B.A., Sims, C.A., Bala-ban, M.O., Brecht, J.K., and Marshall, M.R. 2006. Effects of low-dose electron beam irra-diation on respiration, microbiology, texture, color, and sensory characteristics of fresh-cut cantaloupe stored in modified-atmosphere packages. J. Food Sci. 71: S149-S155.

Fan, X. 2005. Antioxidant capacity of fresh-cut vegetables exposed to ionizing radiation. J. Sci. Food Agric. 85: 995-1000.

Fan, X. and Sokorai, K.J.B. 2002. Sensorial and chemical quality of gamma irradiated fresh-cut iceberg lettuce in modified atmosphere packages. J. Food Protect. 65: 1760-1765.

Fan, X. and Sokorai, K.J.B. 2005. Assess-ment of radiation sensitivity of fresh-cut vegetables using electrolyte leakage measure-ment. Postharvest Biol. Technol. 36: 191-197.

Fan, X. and Sokorai, K.J.B. 2007. Formation of furan from fresh fruits and vegetables due to ionizing radiation. J. Food Sci. (in press).

Fan, X., Niemira, B.A., and Sokorai, K.J.B. 2003a. Sensorial, nutritional and microbiological quality of fresh cilantro leaves as influenced by ionizing irradiation and storage. Food Res. Intl. 36: 713-719.

Fan, X., Toivonen, P.M.A., Rajkowski, K.T., and Sokorai, K.J.B. 2003b. Warm water treatment in combination with modified atmosphere packaging reduced undesirable effects or irradiation on the quality of fresh-cut iceberg lettuce. J. Agric. Food Chem. 50: 1231-1236.

FDA. 2007a. Threshold of regulation exemp-tions. Food and Drug Admin. www.cfsan.fda.gov/~dms/opa-torx.html, accessed Oct. 25.

FDA. 2007b. Irradiation in the production, processing and handling of food. Proposed rules. Fed. Reg. 72: 16291-16306. www.cfsan.fda.gov/~lrd/fr070404.html, accessed Oct. 25.

FDA, 2007c. Foods permitted to be irradiated under FDA’s regulations (21 CFR 179.26). http://www.cfsan.fda.gov/~dms/irrafood.html, accessed Oct. 25.

FDA. 2007d. Packaging materials listed in 21 CFR 179.45 for use during irradiation of prepackaged foods. http://www.cfsan.fda.gov/~dms/irrapack.html, accessed Oct. 25.

Foley, D., Euper, M., Caporaso, F., and Prakash, A. 2004. Irradiation and chlorina-tion effectively reduces Escherichia coli O157:H7 inoculated on cilantro (Coriandrum sativum) without negatively affecting quality. J. Food Protect. 67: 2092-2098.

Gunes, G., Watkins, C.B., and Hotchkiss, J.H. 2000. Effects of irradiation on respiration and ethylene production of apple slices. J. Sci. Food Agric. 80: 1169-1175.

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Koorapati, A., Foley, D., Pilling, R., and Prakash, A. 2004. Electron-beam irradiation preserves the quality of white button mushroom (Agaricus bisporus) slices. J. Food Sci. 69: S25-S29.

Masson, S. 2002. Effects of gamma irradiation on the shelf-life and quality characteristics of diced bell peppers M.S. thesis. Chapman Univ., Orange, Calif.

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minimize changes in organoleptic, nutritional, or functional properties, if any, that would constitute a material change to the consumer.

Because the response of each type (cultivar, species, whole vs fresh-cut, etc.) of fruits and vegetables to irradiation varies, process validation is required for each. While much work has been done already, it is important to prioritize future studies and products that need to be evaluated by their implication in outbreaks and/or volume of consumption.

As mentioned above, radiation resistance of pathogens is influenced by their environ-ment. More research is needed to determine radiation resistance of internalized and biofilm-associated pathogens. In addition, radiation resistance of pathogens is mostly determined by artificially inoculating fresh-cut produce to high populations before irradiation. Ideally, radiation resistance of pathogens should be determined using naturally contaminated produce and levels of pathogens similar to those found in naturally contaminated produce.

Furthermore, the effect of modified-atmosphere packaging on radiation resistance of pathogens requires more investigation. In most studies on determining radiation resistance of pathogens, the inoculated samples were irradi-ated in air, whereas many fresh-cut produce are packaged in modified atmosphere. The modified atmosphere (low O2 and high CO2 levels) may alter the radiation resistance of pathogens. Other areas, such as packaging materials, may need approval and research before irradiation is fully applied by the produce industry.

Thus, low-dose irradiation is a reliable technology capable of killing human pathogens such as E. coli O157:H7 and Salmonella by 2–8 logs without causing significant deterioration in product quality. There are many challenges ahead for commercial application of irradiation for fresh and fresh-cut produce, including regula-tory approval, packaging materials, consumer acceptance, and lack of premarket studies. FT

Xuetong Fan (xuetong.fan@ars.usda.gov) and Brendan A. Niemira (brendan.niemira@ars.usda.gov) are, respectively, Research Food Technologist and Microbiologist, U.S. Dept. of Agriculture, Agricultural Research Service, Eastern Regional Research Center, 600 E. Mermaid Ln., Wyndmoor, PA 19038. Anuradha Prakash (prakash@chapman.edu) is Professor, Chapman University, One University Dr., Orange, CA 92866. The authors are Professional Members of IFT. Send reprint requests to Xuetong Fan. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Dept. of Agriculture.