Part I and Part II of this series reviewed the historical background and technology of food irradiation, and the food safety implications relating to FDA’s recent approval of a new rule for use of ionizing irradiation as a processing step in fresh iceberg lettuce and spinach. This segment summarizes state-of-the art knowledge of the pros and cons (advantages and limitations) of using ionizing radiation to enhance the quality of fresh iceberg lettuce and spinach. The term “food quality” encompasses all of the objective and subjective factors that contribute to a food’s wholesomeness, nutritional value, and sensory attributes. Peri (2006) succinctly defined food quality as: “fitness for consumption,” in other words, “the requirements necessary to satisfy the needs and expectations of the consumer.”
Ionizing Radiation as a Food Preservation Technique
Irradiation is one of many food preservation techniques. As discussed in Part I, food irradiation is not new, but the application of this technology to fresh lettuce and spinach was only recently approved in the US. Before delving into the details of food quality in the context of food irradiation, it is worthwhile to consider the historical perspective of food preservation, and how food irradiation fits into this picture.
The quality of any fresh food deteriorates after harvest, in part, due to the action of spoilage organisms (e.g., bacteria, fungi). Spoilage leads to loss of nutrients and negative effects on the flavor and appearance of fresh food over time. The negative effects of deterioration could be avoided if consumers were able to prepare and eat foods almost immediately after the food leaves the farm. But, for most consumers this scenario is not practical on a year-around basis. The search for efficient and effective methods to preserve the safety, quality, and nutritional value of perishable foods during transportation and storage, while simultaneously maintaining the benefits of the original fresh product, has been an ongoing challenge across the ages of civilization.
The earliest examples of food preservation include cooking/boiling, cold storage (refrigeration/freezing), drying, and salting. To this day, these traditional methods remain a cornerstone in the prevention of food spoilage and waste, worldwide. Examples of more recent historical developments in food preservation include pasteurization and canning.
In the modern age, the food processing industry has addressed the unique food preservation challenges associated with fresh produce by introducing novel approaches such as the use of modified atmosphere packaging (MAP) and wash water disinfectants, especially for fresh-cut, minimally processed produce. Temperature control (refrigeration) continues to be the most important approach to preserving the quality and safety of fresh produce. Irradiation of fresh lettuce and spinach represents a new tool in the produce preservation toolbox. The following are examples of current approaches to achieve food quality preservation of fresh produce that may be used individually, or in combination, depending on the specific product.
• Freezing (spinach)
• Heat treatment – cooking and canning (spinach)
• Wash water sanitizers (e.g., sodium hypochlorite, hydrogen peroxide, chlorine dioxide, ozonated water, etc.)
• Modified atmosphere packaging (MAP), a procedure that packages fresh-cut lettuce/spinach in high CO2 and low O2 to control spoilage organisms
• Ionizing radiation
Irradiation and the Fresh-Cut Produce Industry
It is worth noting that many of the produce-related papers in this review address “fresh-cut” fruits and vegetables. Fresh-cut (also termed “minimally processed” or “value-added”) is defined as ready-to-eat, raw fruits and vegetables that have been peeled, chopped, shredded, or similarly processed. Fresh-cut leafy greens are usually pre-washed with a disinfectant (e.g., chlorine) and are packaged, sometimes in a modified atmosphere (reduced oxygen) to preserve the food quality. The packages range from individual containers that consumers purchase at the grocery store to institutional size packages sold to restaurants, hospitals, correctional facilities, and other facilities that serve large populations. Fresh-cut is differentiated from raw commodities such as whole lettuce heads and mature bunch spinach.
Application of Ionizing Radiation to Control Spoilage Organisms: The Shelf Test
Most retailers and consumers have experienced the disappointment of discarding spoiled fresh lettuce and spinach that was not sold or consumed, respectively, before the “use by” date. The “shelf-life,” defined as the length of time a product can be stored without becoming unsuitable for consumption, is relatively short for fresh produce (for example, 10-14 days for fresh spinach), which can lead to food waste. Plant bacterial and fungal pathogens are a major cause of lettuce and spinach spoilage during storage. Spoilage results in off-odors, “slimy” or “rotten” textures, and leaf deterioration. Because fresh-cut lettuce and spinach processing, in particular, introduces plant wounds/lesions, these products may be more vulnerable to microbial growth of spoilage organisms. The most important spoilage problems and species involved for lettuce and spinach include:
• Bacterial soft rot: Erwinia, Pseudomonas
• Watery soft rot: Sclerotinia (fungal)
• Gray mold rot: Botrytis cinerea (fungal)
Similar to foodborne pathogen reduction, the approved dosages for irradiation of lettuce and spinach significantly reduce spoilage bacterial levels (3-5 logs), and the process thereby extends shelf-life. The mechanism for control by irradiation is the same for spoilage organisms and foodborne pathogens. Thus, a major advantage to using ionizing irradiation as a microbial control step is its simultaneous impact on reducing food spoilage organisms and foodborne pathogens. However, the effectiveness of irradiation in controlling both plant and human pathogens depends on the initial quality of the iceberg lettuce or spinach coming from the field and processing plant prior to irradiation. As discussed previously, irradiation is not a replacement for good agricultural practices and good manufacturing processes; furthermore, irradiation does not “sterilize” the lettuce/spinach, and eventually the product will spoil. Everyone across the food chain, including the consumer, must still take precautions to prevent spoilage through proper handling, especially temperature control (refrigeration).
Effect of Ionizing Radiation on Nutrient Content: The Popeye Test
Popeye the Sailor is the iconic symbol of the benefits of eating spinach. The cartoon legend purportedly gains his superhero strength from iron in canned spinach. Indeed, there is no doubt that spinach (fresh, frozen, or canned) is highly nutritious, and the Reference Daily Intake (RDI) value for spinach is classified as “good” for iron (and calcium, fiber). Spinach is also considered an “excellent” source of vitamins A, C, K, and folate. In contrast, iceberg lettuce is only an “excellent” source of vitamin K.
Every food processing technique is subjected to intense scrutiny by nutritionists in the academic and regulatory world to determine the positive and negative effects on nutrient content. Food irradiation is no different, and there is an abundant amount of studies in the scientific literature describing the effect of ionizing radiation on nutrient quality of specific foods under specific conditions.
Prior to analyzing the results of these studies for any food, it is critical to consider two general key questions:
1) Is the nutrient sensitive to ionizing irradiation in the food product?
2) If so, how important is the food product as a source of the nutrient(s) in the overall diet?
Nutrients are divided into two broad categories: macronutrients (carbohydrates, protein/essential amino acids, fats/lipids, water) and micronutrients (vitamins and minerals). Notably, water is the largest component of iceberg lettuce (96%) and spinach (92%). Lettuce and spinach are not major contributors to macronutrients (carbohydrate, fat/lipid, protein) in the diet, and are therefore not significant in the nutritional evaluation of irradiation effects. Likewise, irradiation does not significantly impact minerals (including Popeye’s iron).
Vitamins are divided into two groups based on their solubility in water. The water soluble vitamins are more sensitive to destruction by irradiation. Specifically, radiation can break bonds in some vitamin molecules causing inactivation. Also, irradiation produces free radicals that can combine with antioxidant vitamins and cause the vitamin to lose its activity. Below is a summary of the impacts of ionizing radiation on the four important vitamins in fresh spinach and/or lettuce.
• Vitamin A (pro-vitamin caratenoids): this fat soluble vitamin is relatively resistant to radiation. An older study by Richardson (1961) found no significant loss at doses up to 14 times (56 kGy) the maximum approved FDA dose (4 kGy) for spinach. Evaluation of carrots, an important source of this vitamin, also showed minimal effects from radiation on this nutrient.
• Vitamin C (ascorbic acid): this water soluble vitamin is sensitive to irradiation and may undergo a reaction to produce dehydroascorbic acid; however, the reaction is reversible. Fan and Sokorai (2008) compared irradiated and non-irradiated fresh-cut iceberg lettuce and spinach and found the loss of vitamin C was similar in both groups; they concluded that most vitamin C loss related to deterioration over time during storage.
• Vitamin K: this fat-soluble vitamin is particularly resistant to radiation and studies have found no significant losses following medium-dose treatment.
• Folate: this water-soluble vitamin has some sensitivity to radiation. Muller (1996) documented a 10% loss at 2.5 kGy. Similar to vitamin C, the folate losses in spinach appear to be much more significant from storage time compared with radiation.
Overall, the vitamin losses following medium-dose irradiation of fresh iceberg lettuce and spinach are relatively insignificant, especially compared with losses due to storage time and temperature abuse. As perspective, researchers from Pennsylvania State University published a study in 2004 showing more than 50% of the folate and carotenoid (vitamin A) content of spinach was lost after 8 days of storage at refrigeration temperatures, and after only 4 days with temperature abuse.
Sensory Evaluations: The Taste Test
“Sensory science” is a field of “psychophysics.” It is the scientific study of the senses and psychological responses to stimuli, for example: taste/flavor, appearance/color, texture, and aroma/odor of food. Although consumers will differ in opinion when evaluating these subjective qualities of food, sensory science utilizes trained “panelists” and statistical analyses to quantify the sensory attributes. Additionally, qualities such as texture and color can be measured using objective criteria such as electrolyte loss (associated with “sogginess”) and chlorophyll loss (color changes) in lettuce and spinach leaves under different conditions.
Fan and his research team at the USDA ARS Eastern Regional Research Center have been on the forefront of irradiation research of fresh-cut produce and food quality. In 2002, Fan and Sokorai documented a dose-response for ionizing radiation of fresh-cut iceberg lettuce in MAP; higher radiation doses (> 2 kGy) correlated with increased sogginess. A subsequent study (2003) showed that the combination of warm water treatment and MAP could reduce the negative effects of radiation on iceberg lettuce appearance and texture. Zhang et al (2006) found a similar dose response: “experimental results showed that the number of aerobic mesophilic bacteria on fresh-cut lettuce irradiated with 1.0 kGy was reduced by 2.35 logs and sensory quality was maintained best during storage for 8 days at 4°C.” Increasing the dose to 1.5 kGy resulted in a 3 log reduction in spoilage bacteria, but also caused some damage to leaf tissue appearance.
In 2008, Fan and Sokorai describe the results of a comprehensive study of food quality effects of irradiation on 13 fresh-cut vegetables including iceberg lettuce packaged in air, iceberg lettuce in MAP, and spinach in MAP. Based on previous studies, they chose a dose of 1 kGy, and compared quality characteristics over 14 days of storage in two groups: irradiated vegetables and non-irradiated/control vegetables. They found:
• No significant differences in texture between the irradiated and control groups for iceberg lettuce and spinach during 14 days of storage.
• No significant differences in appearance for irradiated or control group spinach during 14 day storage.
• Irradiated iceberg lettuce packaged in air showed irradiation-induced enzymatic browning during storage compared with the control group
• Irradiated iceberg lettuce packaged in MAP had a better appearance score than the control group, which suggests that MAP may be an approach to mitigate the irradiation browning effect for iceberg lettuce.
• Irradiated iceberg lettuce had an off-odor due to the packaging material used in the study
Notably, there were few studies in the literature comparing different packaging materials, styles (e.g., bag, clam shell), and sizes (individual, institutional) specific for fresh iceberg lettuce and spinach. This research will be needed to fully evaluate the effects of radiation on food quality, and optimize the dose for commercial processing of fresh iceberg lettuce and spinach.
In summary, the food quality literature relating to irradiation of fresh iceberg lettuce and spinach suggests that the process has the following pros and cons:
• Reduction of spoilage microorganisms, which may translate into increased shelf-life and less food waste
• Minor to no significant loss of important nutrients in lettuce and spinach, especially compared with nutrient loss following other common food preservation techniques (e.g., boiling and freezing) and losses during storage
• At the low-end of the approved dose range for fresh lettuce and spinach (1 kGy), there was limited to no detectable problems with sensory qualities (appearance, taste, texture, and aroma)
• In general, as the dose increases, the log reduction of susceptible spoilage organisms (and foodborne pathogens) also increases, but the increased dose (especially over 2 kGy) may have negative effects on nutrients and sensory attributes
• Some packaging material may not be appropriate (or FDA approved) for irradiation processing as shown in a recent study (Fan and Sokorai, 2008) where the packaging material caused “off-odors” in fresh-cut iceberg lettuce
Taken together, the food safety and food quality literature review shows that the pros can be balanced against the cons of ionizing radiation with optimization of the process. In other words, the technology is not “one size fits all,’ and each type of product and packaging material must be evaluated to identify conditions that both promote food safety and preserve food quality. The experts frequently recommend a “hurdle approach” that employs a combination of treatments designed to minimize the radiation dose while maximizing the positive effects on microbial control and food quality.
In the final part of this series (Part IV), the costs versus the benefits for industry and consumers of implementing commercial irradiation into fresh lettuce and spinach processing will be discussed. In addition, the literature on consumer acceptance, and how irradiation of fresh lettuce and spinach may impact consumer confidence in the leafy green supply, will be analyzed.
1. Anonymous. 1994. Safety and nutritional adequacy of irradiated food. World Health Organization, Geneva.
2. Anonymous. 2008. USDA National Nutrient Database for Standard Reference. Release 21. Available at: http://www.ars.usda.gov/Services/docs.htm?docid=8964
3. Beltran, D., M. V. Selma, A. Marin, and M. I. Gil. 2005. Ozonated water extends the shelf life of fresh-cut lettuce. J Agric Food Chem 53:5654-63.
4. Brandl, M. T. 2008. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl Environ Microbiol 74:5285-9.
5. Cotton, P. A., A. F. Subar, J. E. Friday, and A. Cook. 2004. Dietary sources of nutrients among US adults. J. Am. Diet. Assoc. 104:921-30.
6. Diehl, J. F. 1995. Nutritional adequacy of irradiated foods. In: Safety of Irradiated Foods, 2nd edition. Diehl, J. F. (ed). Marcel Dekker, New York. p. 241-282.
7. Fan, X., and K. J. Sokorai. 2007. Effects of ionizing radiation on sensorial, chemical, and microbiological quality of frozen corn and peas. J Food Prot 70:1901-8.
8. Fan, X., and K. J. Sokorai. 2008. Retention of quality and nutritional value of 13 fresh-cut vegetables treated with low-dose radiation. J Food Sci 73:S367-72.
9. Fan, X., and K. J. Sokorai. 2002. Sensorial and chemical quality of gamma-irradiated fresh-cut iceberg lettuce in modified atmosphere packages. J Food Prot 65:1760-5.
10. Fan, X., P. M. Toivonen, K. T. Rajkowski, and K. J. Sokorai. 2003. Warm water treatment in combination with modified atmosphere packaging reduces undesirable effects of irradiation on the quality of fresh-cut iceberg lettuce. J Agric Food Chem 51:1231-6.
11. Farkas, J. 1989. Microbiological safety of irradiation foods. Int J Food Microbiol. 9:1-15.
12. Gomes, C., R. G. Moreira, M. E. Castell-Perez, J. Kim, P. Da Silva, and A. Castillo. 2008. E-Beam irradiation of bagged, ready-to-eat spinach leaves (Spinacea oleracea): an engineering approach. J Food Sci 73:E95-102.
13. Gomez-Lopez, V. M., P. Ragaert, V. Jeyachchandran, J. Debevere, and F. Devlieghere. 2008. Shelf-life of minimally processed lettuce and cabbage treated with gaseous chlorine dioxide and cysteine. Int J Food Microbiol 121:74-83.
14. Giusti, A. M., E. Bignetti, and C. Cannella. 2008. Exploring new frontiers in total food quality definition and assessment: from chemical to neurochemical properties. Food Bioprocess. Technol. 1:130-42.
15. Hagenmaier, R. D. and R. A. Baker. 1997. Low-dose irradiation of cut iceberg lettuce in modified atmosphere packaging. J. Agric. Food Chem. 45:2864-8.
16. Hajare, S. N., V. S. 2006. Dhokane, R. Shashidhar, S. Saroj, A. Sharms, and J. R. Bandekar. Radiation processing of minimally processed carrot (Daucus carota) and Cucumber (Cucumis sativus) to ensure safety: effect on nutritional and sensory quality. J. Food Sci. 71:198-203.
17. Kader, A. A., W. J. Lipton, and L. L. Morris. 1983. Systems for scoring quality of harvested lettuce. HortScience. 8:408-9.
18. Kader, A. A. 2002. Postharvest biology and technology: an overview. In: Postharvest Technology of Horticultural Crops. Kadar, A. A. (ed). Univ. of Calif, Oakland, CA. Spec. Publ. 3311. p. 39-48.
19. Kang, S. C., M. J. Kim, and U. K. Choi. 2007. Shelf-life extension of fresh-cut iceberg lettuce (Lactuca sativa L) by different antimicrobial films. J Microbiol Biotechnol 17:1284-90.
20. Kang, S. C., M. J. Kim, I. S. Park, and U. K. Choi. 2008. Antimicrobial (BN/PE) film combined with modified atmosphere packaging extends the shelf life of minimally processed fresh-cut iceberg lettuce. J Microbiol Biotechnol 18:568-72.
21. King, A. D., J. A. Magnuson, T. Torok, and N. Goodman. 1991. Microbial flora and storage quality of partially processed lettuce. J. Food Sci. 56:459-461.
22. Lane, R. H., Y. B. Negers, J. L. Bonner, and R. S. Stitt. Nutrient quality of selected vegetables prepared by conventional and cook-freeze methods. J. Food Qual. 9:407-14.
23. Loaiza-Velarde, J. G., M. E. Saltveit, and M. Cantwell. 1996. The visual quality of minimally processed lettuces stored in air or controlled atmosphere with emphasis on romaine and iceberg types. Postharvest. Bio. Technol. 8:179-90.
24. Murano, P. S. 1995. Quality of irradiated foods. In: Food Irradiation: A sourcebook. E. A. Murano (ed). Iowa State University Press, Ames, Iowa. p. 63-87.
25. Niemira, B. A., X. Fan, and C. H. Sommers. 2002. Irradiation temperature influences product quality factors of frozen vegetables and radiation sensitivity of inoculated Listeria monocytogenes. J Food Prot 65:1406-10.
26. Niemira, B. A. and X. Fan. 2006. Low-dose irradiation of fresh and fresh-cut produce: safety, sensory, and shelf life. In: Food Irradiation Research and Technology. C. H. Sommers and X. Fan (eds). IFT Press, Chicago, IL. p. 169-184.
27. Niemira, B. A. 2007. Relative efficacy of sodium hypochlorite wash versus irradiation to inactivate Escherichia coli O157:H7 internalized in leaves of Romaine lettuce and baby spinach. J Food Prot 70:2526-32.
28. Niemira, B. A. 2008. Irradiation compared with chlorination for elimination of Escherichia coli O157:H7 internalized in lettuce leaves: influence of lettuce variety. J Food Sci 73:M208-13.
29. Padrangi, S. and I. E. LaBorde. 2004. Retention of folate, carotenoids, and other quality characteristics in commercially packaged fresh spinach. J. Food Sci. 69:702-7.
30. Patterson, M. 2001. Combination treatments involving food irradiation. In: Food Irradiation: Principles and Applications. Molins, R. (ed). John Wiley & Sons, New York, NY. p. 313-27.
31. Peri, C. 2005. The universe of food quality. Food Quality. 17:3-8.
32. Prakash, A. and D. Foley. 2004. Improving safety and extending shelf-life of fresh-cut fruits and vegetables using irradiation. In: Irradiation of Food and Packaging: recent developments. Komolprasert, V. and K. M. Morehouse (eds). American Chemical Society, Washington D.C., p. 90-106.
33. Wood, O. B., and C. M. Bruhn. 2000. Position of the American Dietetic Association: food irradiation. J Am Diet Assoc 100:246-53.
34. Zhang, L. Z. Lu, F. Lu, and X. Bie. 2006. Effect of gamma irradiation on quality maintaining of fresh-cut iceberg lettuce in modified atmosphere packages. Food Control. 17:225-8.
35. Zhang, L., Z. Lu, and H. Wang. 2006. Effect of gamma irradiation on microbial growth and sensory quality of fresh-cut lettuce. Int J Food Microbiol 106:348-51.