This is the second part of a series on Food Safety and irradiation. Here was the first installlment. The new FDA rule approves the use of ionizing radiation (also termed irradiation, irradiation pasteurization, cold pasteurization) of fresh iceberg lettuce and fresh spinach for control of foodborne pathogens, and extension of shelf-life. Molins (2001) and other experts agree that food irradiation fits the definition of a “critical control point” in a comprehensive farm-to-table approach (e.g., HACCP) to prevent foodborne illnesses and outbreaks. But, implementing irradiation into fresh lettuce and spinach processing poses some challenges. In the second part of this series, the pros and cons (advantages and limitations) of irradiation relative to food safety are reviewed.
The Problem of Foodborne Pathogens in Fresh Lettuce and Spinach
Before embracing a potentially expensive and controversial new control method in processing such as irradiation, it is imperative to consider the scope of the problem being addressed. Consumer confidence in the safety of fresh fruits and vegetables has been shaken in recent years due to high-profile and sometimes deadly outbreaks linked to produce contaminated with foodborne pathogens. Experts in nutrition agree unanimously that fresh produce is an important component of a healthy diet; therefore, production of safe produce free of harmful pathogens is critical.
Outbreaks associated with fresh leafy green vegetables including iceberg lettuce and spinach are increasing. Herman (2008) presented data at the International Conference on Emerging Infectious Diseases showing a 9% increase in consumption of leafy green vegetables from 1996-2005, compared with a 38.6% increase in leafy green-associated outbreaks during the same time period. These results suggest that the proportion of foodborne disease outbreaks due to leafy greens cannot be explained by increases in consumption alone. Unfortunately, there is evidence that consumers may be at risk from produce that is contaminated prior to purchase, and recommendations to “wash” their fruits and vegetables before consumption may not always be adequate to prevent foodborne illness. In a study of E. coli O157:H7 outbreaks from 1982-2002, the authors estimated that half of the produce-associated outbreaks were due to produce already contaminated with E. coli O157 before purchase by the retail store or consumer (Rangel et al, 2005).
Examples of foodborne disease outbreaks and recent recalls linked to salad greens are shown in the Table below. The table includes only outbreaks/recalls believed to be due to contamination before the produce reached the retail level (e.g., grocery store, restaurant, kitchen). The fact that lettuce, spinach and other raw or minimally-processed produce can be contaminated with foodborne pathogens on the farm, or during harvest, transportation, or processing is a daunting problem for public health and industry. The risk is increased because fresh lettuce, and often spinach, is not subjected to a “kill” step such as cooking prior to consumption. Other unique challenges with microbial contamination of lettuce and spinach have been documented in the literature.
• The purpose of sanitizers used to wash leafy greens (for example, chlorine solutions) is to eliminate microbial contamination of the wash water, not the plant leaves. Many studies have shown the limitations of routine protocols for chemical washing of lettuce and other leafy greens in reducing pathogen levels. The low infectious dose (very few bacteria) of pathogens such as E. coli O157:H7, other STECs, and Shigella increase the threat.
• Researchers have found that plant lesions (such as those caused by harvesting and processing, including “fresh-cut” processing) can promote the rapid multiplication of E. coli O157:H7 (Brandl, 2008)
• Bacteria may internalize into the plant tissue and be protected from chemical sanitizers. Giron from the University of Arizona described preliminary results from high-resolution electron microscopy showing E. coli O157 internalized within the “stomata” of spinach leaves, and the bacteria were not destroyed by chlorine wash solutions
See Table of Outbreaks from 1995 to present.
The Pros (Advantages) of Food Irradiation for Fresh Lettuce and Spinach
Could any of these outbreaks or recalls have been prevented by use of irradiation as a control step during processing in the US and other countries?
An analysis by Tauxe (2001) suggests that the answer to this question would be “yes.” He analyzed the potential benefit of irradiated meat and poultry and estimated that 900,000 cases of infection, 8,500 hospitalizations, over 6,000 catastrophic illnesses, and 350 deaths could have been prevented each year. A similar analysis of the potential impact of irradiation in preventing illnesses due to contamination of lettuce, spinach, and other leafy greens would be interesting. Nine of the outbreaks and 1 recall (Table) were from contaminated fresh iceberg lettuce or spinach. Additionally, several outbreaks involved institutional settings such as hospitals, children’s camp, and nursing homes, which serve populations that are especially vulnerable to severe illness or death from foodborne pathogens.
Notably, the pathogens most commonly implicated in leafy green-related outbreaks and recalls are bacteria and parasites; these organisms are also the most susceptible to control using medium (1-10 kGy) dosage of irradiation. For example, research indicates that Campylobacter, Cyclospora, E. coli O157/STECs, Listeria, Salmonella, and Shigella are reduced by 3-5 logs. Additionally, raw or “minimally processed” fresh-cut, pre-washed leafy greens have unique risks that irradiation as a control step could potentially address. Specifically, an advantage of irradiation is its ability to penetrate the leaf tissue and reach bacteria internalized in the lettuce or spinach tissue. For example, Niemira (2007) showed that “ionizing radiation but not chemical sanitizers effectively reduced viable E. coli O157:H7 cells internalized in leafy green vegetables.”
The Cons (Limitations) of Food Irradiation for Fresh Lettuce and Spinach
The irradiation dose (up to 4 kGy) approved by FDA is not meant to sterilize (kill all living organisms) iceberg lettuce or spinach. Thus, irradiation is not a replacement for good agricultural practices and management practices on the farm and during harvest, transportation, and processing. Use of irradiation also does not prevent post-processing contamination during transport or by the retailer or consumer during food preparation and handling. Murano summarizes the issue in her chapter on microbiology of irradiated foods:
“Irradiation, however, should not be used to make “dirty” products (those heavily contaminated with microorganisms) clean again. To attempt to do so would require doses much higher than those needed to eliminate normal background levels. This would result in significant damage to the quality of the product, and in high costs to the processor in terms of energy.”
Additionally, at the approved dose for iceberg lettuce and spinach, irradiation may not effectively reduce viruses (e.g., norovirus, hepatitis A), spore forming bacteria such as Clostridium botulinum, and it does not eliminate toxins. However, it is worth noting that these causes of foodborne illness and intoxication are rarely linked to fresh lettuce and spinach. All forms of food processing including ionizing radiation may introduce “resistance” into the microbial pathogen. Likewise, processing techniques may lead to mutations in bacteria. There is a theoretical risk of irradiation-induced mutations leading to increased virulence in a bacterial population, but no evidence of this phenomenon with food irradiation could be found in the literature.
Food Irradiation and Toxicology
Considerable debate about the safety of irradiated food products in terms of potential “side effects” has ensued since the inception of this technology. The primary concerns raised include: 1) potential for “radioactivity” of the food or packaging, and 2) production of toxic elements or “unique radiolytic products” in the food or packaging that may have long-term health consequences for consumers such as cancer or reproductive problems.
An extensive review of the literature revealed no significant health risks for consumers at the irradiation doses approved for food processing. Indeed, the research by preeminent scientists in the fields of physics, biology, nutrition, and medicine overwhelmingly provide data that refutes concerns about food irradiation leading to long-term negative health outcomes. Additionally, respected public health organizations worldwide have reviewed the data, and every major group has stated that food irradiation is a potential tool to protect the public health. In addition to FDA, these groups include but are not limited to: American Academy of Pediatrics, American Dietetics Association, American Medical Association, Centers for Disease Control and Prevention, and the World Health Organization.
Given the massive amount of work by experts already dedicated to addressing the two questions above, only a brief summary and selected citations are provided in this review.
First, it is physically impossible to create radioactivity in food or packaging at the approved food irradiation dosages using gamma ray technology; as discussed in the previous part of this series, gamma rays are the only food irradiation technique that require a radioactive substance (Cobalt 60). X-ray and electronic beam (E-beam) technology do not use radioactive substances, and therefore cannot create “radioactivity” in food or packaging.
The second concern about potential toxic substances created by irradiation, and subsequent effects on human health, has been the subject of intense research for four decades. A few preliminary studies suggested possible risks that prompted more research; the original findings could not be reproduced in later studies, which lead experts to conclude that food irradiation is safe.
One substance is worth mentioning as it is the only chemical described as a potential “unique radiolytic product” in food following irradiation: 2-alkylcyclobutanones (2-ACBs). Scientific evidence indicates that 2-ACBs do not pose a health risk for consumers. The substance is created by a chemical reaction with lipids (fats), and most research has focused on food with fat content (e.g., meat, poultry). Since iceberg lettuce and spinach contain virtually no fat content, 2-ACBs are not relevant in the discussion of food safety and use of irradiation to reduce foodborne pathogens..
In summary, food irradiation is not a “silver bullet” for food safety. However, the increasing problem of illnesses and deaths associated with consumption of fresh produce, including lettuce and spinach, emphasizes the need for an intervention. It is critical that scientists, policy makers, industry, and the public consider carefully the implications of this technology, and its potential role in food safety.
In the next part of this series, the effect of food irradiation on food quality, including sensory and nutritional properties, will be explored.
1. Ackers, M. L., B. E. Mahon, E. Leahy, B. Goode, T. Damrow, P. S. Hayes, W. F. Bibb, D. H. Rice, T. J. Barrett, L. Hutwagner, P. M. Griffin, and L. Slutsker. 1998. An outbreak of Escherichia coli O157:H7 infections associated with leaf lettuce consumption. J Infect Dis 177:1588-93.
2. Anonymous. 1994. Safety and nutritional adequacy of irradiated food. World Health Organization, Geneva.
3. Anonymous. 1997. Hospital outbreak of Escherichia coli O157:H7 associated with a rare phage type – Ontario. Canada Communicable Disease Report. 23-05:
4. Anonymous. 2002. E. coli O157:H7 Illnesses in Washington. California Department of Public Health, Sacramento, CA.
5. Anonymous. 2004. Investigation of E. coli O157:H7 Illnesses in San Diego and Orange Counties California Department of Public Health. Sacramento, CA.
6. Anonymous. 2007. Investigation of an E. coli O157 H7 Outbreak Associated with Consumption of Dole Brand Pre Packaged Salads. California Department of Public Health, Sacramento, CA.
7. Anonymous. 2007. Investigation of an Escherichia coli O157:H7 outbreak associated with Dole pre-packaged spinach. California Department of Public Health, Sacramento, CA.
8. Anoymous. CDPH. 2007. Investigation of a 2006 E. coli O157: H7 Outbreak Associated with Taco Bell Restaurants in the Northeastern United States. California Department of Public Health, Sacramento, California.
9. Anonymous. 2008. Investigation of the Taco John’s Escherichia coli O157:H7 Outbreak Associated with Iceberg Lettuce. California Department of Public Health, Sacramento, California.
10. Barna, J. 1979. Compliation of bioassay data on wholesomeness of irradiated food items. Acta Alimentaria. 8:205-315.
11. Brandl, M. T. 2008. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl Environ Microbiol 74:5285-9.
12. Davies, R. and A. J. Sinskey. 1973. Radiation-resistant mutants of Salmonella typhimurium LT2: development and characterization. J Bacteriol. 113: 133-44.
13. Crook, P. D., J. F. Aguilera, E. J. Threlfall, S. J. O’Brien, G. Sigmundsdottir, D. Wilson, I. S. Fisher, A. Ammon, H. Briem, J. M. Cowden, M. E. Locking, H. Tschape, W. van Pelt, L. R. Ward, and M. A. Widdowson. 2003. A European outbreak of Salmonella enterica serotype Typhimurium definitive phage type 204b in 2000. Clin Microbiol Infect 9:839-45.
14. Dhokane, V. S., S. Hajare, R. Shashidhar, A. Sharma, and J. R. Bandekar. 2006. Radiation processing to ensure safety of minimally processed carrot (Daucus carota) and cucumber (Cucumis sativus): optimization of dose for the elimination of Salmonella Typhimurium and Listeria monocytogenes. J Food Prot 69:444-8.
15. Doorduyn, Y., C. M. de Jager, W. K. van der Zwaluw, I. H. Friesema, A. E. Heuvelink, E. de Boer, W. J. Wannet, and Y. T. van Duynhoven. 2006. Shiga toxin-producing Escherichia coli (STEC) O157 outbreak, The Netherlands, September-October 2005. Euro Surveill 11:182-5.
16. Farkas, J. 1989. Microbiological safety of irradiation foods. Int J Food Microbiol. 9:1-15.
17. Franz, E., and A. H. van Bruggen. 2008. Ecology of E. coli O157:H7 and Salmonella enterica in the Primary Vegetable Production Chain. Crit Rev Microbiol. 34:1-19.
18. Friesema, I., B. Schimmer, O. Stenvers, A. Heuvelink, E. de Boer, K. van der Zwaluw, C. de Jager, D. Notermans, I. van Ouwerkerk, R. de Jonge, and W. van Pelt. 2007. STEC O157 outbreak in the Netherlands, September-October 2007. Euro Surveill 12:E071101 1.
19. Giron, J. A., J. Xicohtencatl, E. Sanchez, and J. M. Leong. 2008. Interaction of Escherichia coli O157:H7 with fresh leafy green produce. Fresh Express Fresh Produce Safety Research Conference Synopses. Monterey, CA. p. 6-8.
20. 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.
21. Anonymous. 2004. Investigation of an E. coli O157:H7 outbreak at a San Mateo Retirement Facility. California Department of Public Health, Sacramento, CA.
22. Herman, K. M. 2008. Foodborne disease outbreaks associated with leafy greens, 1973-2006. International Conference on Emerging Infectious Diseases 2008. slide sessions and poster abstracts. Emerg Infect Dis. Available from http://www.cdc.gov/eid/content/14/3/ICEID2008.pdf
23. Hilborn E. D., J. H. Mermin, P. A. Mshar, J. L. Hadler, A. Voetsch, C. Wojtkunski, M. Swartz, R. Mshar, M. A. Lambert-Fair, J. A. Farrar, M. K. Glynn, and L. Slutsker. 1999. A multistate outbreak of Escherichia coli O157:H7 infections associated with consumption of mesclun lettuce. Arch. Intern. Med. 159:1758-64.
24. Molins, R. A, Y. Motarjemi, F. K. Kaferstein. 2001. Irradiation: a critical control point in ensuring the microbiological safety of raw foods. Food Control 12:347-56.
25. Murano, E. A. 1995. Microbiology of irradiated foods. In: Food Irradiation: A sourcebook. E. A. Murano (ed). Iowa State University Press, Ames, Iowa. p. 29-61.
26. Niemira, B. A., C. H. Sommers, and X. Fan. 2002. Suspending lettuce type influences recoverability and radiation sensitivity of Escherichia coli O157:H7. J Food Prot 65:1388-93.
27. Niemira, B. A. 2003. Radiation sensitivity and recoverability of Listeria monocytogenes and Salmonella on four lettuce types. J Food Science. 63:2784-7.
28. Niemira, B. A. and X. Fan. 2006. Low-dose irradiation of fresh an 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.
29. 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.
30. 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.
31. Osterholm, M. T., and A. P. Norgan. 2004. The role of irradiation in food safety. N Engl J Med 350:1898-901.
32. Preston, M., A. Borczyk, and R. Davidson. 1997. Hospital outbreak of Escherichia coli O157:H7 associated with a rare phage type–Ontario. Can Commun Dis Rep 23:33-6; discussion 36-7.
33. Raiden, R. M., S. S. Sumner, J. D. Eifert, and M. D. Pierson. 2003. Efficacy of detergents in removing Salmonella and Shigella spp. from the surface of fresh produce. J Food Prot 66:2210-5.
34. Rangel, J. M., P. H. Sparling, C. Crowe, P. M. Griffin, and D. L. Swerdlow. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 11:603-9.
35. Raul, F., F. Gosse, H. Delincee, A. Hartwig, E. Marchioni, M. Miesch, D. Werner, and D. Burnouf. 2002. Food-borne radiolytic compounds (2-alkylcyclobutanones)may promote experimental colon carcinogenesis. Nutr Cancer 44:189-91.
36. Shea, K. M. 2000. Technical report: irradiation of food. Committee on Environmental Health. Pediatrics 106:1505-10.
37. Soderstrom, A., P. Osterberg, A. Lindqvist, B. Jonsson, A. Lindberg, S. Blide Ulander, C. Welinder-Olsson, S. Lofdahl, B. Kaijser, B. De Jong, S. Kuhlmann-Berenzon, S. Boqvist, E. Eriksson, E. Szanto, S. Andersson, G. Allestam, I. Hedenstrom, L. Ledet Muller, and Y. Andersson. 2008. A large Escherichia coli O157 outbreak in Sweden associated with locally produced lettuce. Foodborne Pathog Dis 5:339-49.
38. Sommers, C. H., H. Delincee, J. S. Smith, and E. Marchioni. 2006. Toxicological safety of irradiated foods. In: Food Irradiation Research and Technology. Sommers, C. H. and X. Fan (eds). IFT Press, Ames, IA. p.. 43-61.
39. Stewart, E. M. 2001. Food irradiation chemistry. In: Food Irradiation: Principles and Applications. Molins, R. (ed). John Wiley & Sons, New York, NY. p. 37-76.
40. Takkinen, J., U. M. Nakari, T. Johansson, T. Niskanen, A. Siitonen, and M. Kuusi. 2005. A nationwide outbreak of multiresistant Salmonella Typhimurium in Finland due to contaminated lettuce from Spain, May 2005. Euro Surveill 10:E050630 1.
41. Tauxe, R. V. 2001. Food safety and irradiation: protecting the public from foodborne infections. Emerg Infect Dis 7:516-21.
42. Thayer, D. W. 1990. Food irradiation: benefits and concerns. J Food Quality. 13:147-69.
43. Welinder-Olsson, C., K. Stenqvist, M. Badenfors, A. Brandberg, K. Floren, M. Holm, L. Holmberg, E. Kjellin, S. Marild, A. Studahl, and B. Kaijser. 2004. EHEC outbreak among staff at a children’s hospital–use of PCR for verocytotoxin detection and PFGE for epidemiological investigation. Epidemiol Infect 132:43-9.
44. Wood, O. B., and C. M. Bruhn. 2000. Position of the American Dietetic Association: food irradiation. J Am Diet Assoc 100:246-53.
45. 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.
46. See California Department of Health Environmental Investigations.