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Electron beam processing of fresh produce – A critical review ⁎
Suresh D. Pillai , Shima Shayanfar1 National Center for Electron Beam Research, an IAEA Collaborating Centre for Electron Beam Technology, Texas A & M University, College Station, TX 77845, United States
A B S T R A C T To meet the increasing global demand for fresh produce, robust processing methods that ensures both the safety and quality of fresh produce are needed. Since fresh produce cannot withstand thermal processing conditions, most of common safety interventions used in other foods are ineffective. Electron beam (eBeam) is a non-thermal technology that can be used to extend the shelf life and ensure the microbiological safety of fresh produce. There have been studies documenting the application of eBeam to ensure both safety and quality in fresh produce, however, there are still unexplored areas that still need further research. This is a critical review on the current literature on the application of eBeam technology for fresh produce.
1. Introduction Globalization is influencing the foods we consume and when we consume these foods. A wide variety of fresh fruits and vegetables are available in grocery stores around the world, all year round. From a health perspective, this is good because consumption of fresh fruit and vegetables has documented health benefits. Between 1980 and 2001, per capita consumption of fresh fruits increased by 19% (Huang and Huang, 2007). Unlike processed foods, the transport of fresh produce across national borders has to overcome strict phytosanitary rules as well as meeting retailer mandated food safety and food quality standards. Unlike processed foods, there are special challenges confronting fresh produce. Given the fragility of produce such as berries, fresh produce in some instances are not washed. Current fresh produce packing and shipping procedures do not have a validated pathogen kill step. Since fresh produce for the most part does not undergo a validated pathogen kill step, the probability of them harboring a variety of human pathogens is quite high. It is, therefore, not surprising that there are a number of foodborne pathogen outbreaks associated with consumption of fresh produce, making them the leading cause of food borne disease at least in the US (CDC, 2013). Among foodborne pathogens, enteric viruses is the leading cause of illnesses (Painter et al., 2013). Non-thermal technologies such as ionizing radiation technology have significant value in terms of ensuring the safety, quality and phytosanitary standards of fresh produce. In the US, the treatment of fresh produce for phytosanitary applications is showing the greatest increase in the use of ionizing radiation technology in the food industry (Clemmons et al., 2015; Pillai et al., 2014). In terms of ionizing ⁎
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radiation technology, the options available are either gamma irradiation (based on cobalt-60 or cesium-137), electron beam (eBeam) irradiation (most commonly based on linear accelerator or Rhodotron™ technologies) and X-ray technology (Pillai and Shayanfar, 2015). There are commercial cobalt-60, eBeam and X-ray facilities around the world that are currently involved in treating fresh produce for phytosanitary purposes. Some of these are the National Center for Electron Beam Research at Texas A & M University, the gamma facility operated by Gateway America in Gulfport Mississippi, the Krushak gamma facility in India, the Hawaii Pride X-ray facility in Hilo, and the Benebion gamma facility in Matehuala, Mexico. There is a growing interest in the use of eBeam technology for treating foods and fresh produce specifically. This growing interest is due to the increasing cost of acquiring cobalt-60, the challenges associated with gamma facility approvals as well as the overall reduction in the cost of acquiring eBeam technology (IAEA, 2015) This literature review focuses on the peer-reviewed original research describing the efficacy of eBeam technology for fresh produce in terms of improving its overall quality i.e., shelf-life and microbiological quality i.e., eliminating or reducing microbial pathogens. This critical review focuses on fresh fruits and vegetables and focuses only on original research papers published over the past 5 years, since 2012. The following internet search engines were used namely PubMed (https:// www.ncbi.nlm.nih.gov/pubmed/), Gopubmed® (http://www. gopubmed.com/web/gopubmed), Google scholar (https://scholar. google.com/), Web of Science (http://apps.webofknowledge.com), and Scopus (https://www.elsevier.com/solutions/scopus). A variety of search terms and combinations were used to search the original
Correspondence to: Kleberg Center, Texas A & M University, Room 418B, MS 2472, College Station, TX 77843-2472, United States. E-mail address:
[email protected] (S.D. Pillai). Presently at General Mills, Minneapolis, MN, United States.
http://dx.doi.org/10.1016/j.radphyschem.2017.09.008 Received 27 April 2017; Received in revised form 29 August 2017; Accepted 11 September 2017 0969-806X/ © 2017 Published by Elsevier Ltd.
Please cite this article as: Pillai, S.D., Radiation Physics and Chemistry (2017), http://dx.doi.org/10.1016/j.radphyschem.2017.09.008
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achieved. The authors rationalize this discrepancy in pathogen inactivation at 1.1 kGy as compared to 1.5 kGy to similar inactivation trends reported by Matic et al. (1990). It is inconceivable how this discrepancy can be explained biologically. The only conclusion one can draw from these results is that there were errors in either the measured doses or in the pathogen enumeration. Nevertheless, these results do suggest that this important bacterial pathogen is sensitive to eBeam irradiation and that at least a 1-log reduction can be achieved at doses below 1 kGy. On both the 0.7 kGy and 1.5 kGy treated cantaloupe slices, the numbers of surviving S. Poona decreased over the 21 day storage. The importance of accurate experimental controls and realistic processing conditions was highlighted by Moreira et al. (2012). They report that the D-10 values can vary from 35% to 53% based on experimental factors such as dose uniformity ratio, and available oxygen. Espinosa et al. (2012) quantified the reduction of health risks if eBeam processing is adopted by determining the sensitivity of poliovirus (type 1 chat strain) and rotavirus SA-11 on lettuce and spinach. They reported that the D-10 value of poliovirus on lettuce and spinach was 2.35 ( ± 0.20) kGy and 2.32 ( ± 0.08) kGy respectively. The D-10 value of rotavirus on the other hand on lettuce and spinach was 1.29 ( ± 0.64) kGy and 1.03 ( ± 0.05) kGy respectively. A unique aspect of this study was that authors used this information to calculate the theoretical reduction in infection risks if lettuce and spinach were treated with eBeam technology at varying contamination levels. Their results showed that if a 0.8 g serving size of spinach is contaminated with 10 PFU/g of rotavirus if exposed to 3 kGy will result in infection risks being reduced from > 3 in 10 persons getting ill to approximately 5 in 100 persons. Similarly if a serving size of lettuce (~ 14 g) had a contamination level of 10 PFU/g poliovirus, treating this sample to 3 kGy will reduce infection risks from greater than 2 in 10 persons to approximately 6 in 100 persons. Shayanfar et al. (2017) using a similar quantitative microbial risk assessment (QMRA) approach quantified the reduction in infection risks from non O157 toxigenic E.coli if such pathogen-contaminated strawberries are treated using low dose (≤ 1 kGy) eBeam. They report the D-10 value of five different non O157 toxigenic E.coli strains (in buffer) to range between 0.006 kGy and 0.142 kGy but they did not report the D-10 values of the same strains in strawberry puree. Statistically, there was no significant difference in the D-10 values of the different strains. When inoculated into a strawberry “puree” and exposed to 0.95 kGy, these toxigenic strains were reduced by just over 4 logs. The QMRA analysis revealed that if strawberries of contaminated with 100,000 CFU per serving size (150 g), 2 out of every 10 susceptible individuals (20%) would get sick. However, if these same strawberries were treated with eBeam (1 kGy), the infection risks would be reduced to just 4 out of every 100,000 susceptible exposed individuals (0.004%). These results suggest that even at low eBeam doses, processing of fresh produce can result in substantial reduction in potential infection risks. One criticisms of this study is that the strawberries used in this study were made into a puree for estimating the D10 values while fresh strawberries are generally consumed as whole fruit (and not a puree). However, in order to achieve uniform eBeam doses (which is paramount for D-10 value estimations) the authors had to resort to using a puree of the strawberries.
research articles. 2. Enhancing microbiological safety of fresh produce 2.1. Viral pathogens DiCaprio et al. (2016) reported on the inactivation of human norovirus (NoV) and Tulane virus (TV) on fresh whole strawberries. They inoculated whole strawberries with defined TV and NoV using a needle and subjected the strawberries to defined doses between 4.7 kGy and 28.7 kGy. Since there was no laboratory method to enumerate surviving NoV (a method has been published since then), the inactivation of NoV was based on real-time PCR assays and a porcine gastric mucin magnetic bead (PGM-MB) binding assay. The TV viruses were enumerated using conventional tissue culture approaches. Attempting to delineate inactivation doses using intact strawberries is fraught with limitations and significant sources of error. This is because the Dmax/Dmin is never 1.0 in intact fruits. The authors should have identified the D-10 value (dose required for achieving a 1-log) reduction in the strawberries using either then slices of the fruits or a puree and then have the dose(s) required for inactivation of specific titers validated. Also, per the US FDA rules, fresh produce cannot be irradiated with doses greater than 1 kGy. So, the rationale for choosing such high doses is questionable. The authors report that 12.2 kGy was required to achieve 1-log reduction of NoV (per the PGM-MB method) and 16.3 kGy was required to achieve a 2.46 log reduction. These results suggest that there were significant experimental errors. The authors claim that 9.8 kGy was required to achieve a 1-log reduction of TV, while 12.2 kGy was required to achieve 2.09 log reduction of TV. Once again, this discrepancy in the doses required for 1-log and 2-log suggest that there were significant experimental errors in both the protocols and the data interpretation. Nevertheless, this paper is important in that they have proposed a new method of estimating the inactivation of NoV, which could be of value. However, with the recent publication of a method to enumerate human NoV in the laboratory, the value of the PGM-MB is questionable (Ettayebi et al., 2016). Predmore et al. (2015) studied the inactivation of TV and murine norovirus (MNV) on lettuce and strawberries and attempted to understand the mechanism of eBeam inactivation of viruses. Compared to the DiCaprio et al. (2016) study, these authors cut the lettuce and strawberries into 20 × 20 cm square pieces and inoculated with approximately 6-log titers of TV and MNV. The eBeam doses used were between 4 kGy and 30 kGy. Similar to the previous study, it is unclear why the authors did not report their inactivation in terms of D-10 values. Nevertheless, the authors report that it took approximately 8.7 kGy and 16.3 kGy to achieve a 6-log reduction in lettuce strawberries respectively. Based on transmission electron micrographic (TEM) analysis, the authors claim that at 32.7 kGy, the TV capsid is completely degraded. This wide variation in doses is surprising and is indicative that there were probably errors in either the dosimetry or the delivery of eBeam doses. Previous studies by Espinosa et al., have not noted such significantly different responses to eBeam based just on differences in the suspending matrix. 2.2. Bacterial pathogens
3. Enhancing quality attributes of fresh produce through inactivation of spoilage microorganisms
Palekar et al. (2015) have reported on the reduction of Salmonella enterica serotype Poona on fresh-cut cantaloupes when exposed to eBeam processing. For their experimental protocols, they peeled the melons and prepared 2.5 cm dia “melon cylinders”. They dipped these cylinders into a suspension of the bacterial pathogens and then packed these cylinders in plastic bags that had a defined atmospheric condition (9% oxygen and 3% carbon dioxide). The authors calculated the D-10 value of the pathogen using very specific experimental approaches using 4 mm thin slices which corresponded to the thickness of the alanine dosimeters. They reported that at an eBeam dose of 0.7 kGy a 1.1 log reduction is achieved and at 1.5 kGy a 3.6 log reduction is
3.1. Melons Palekar et al. (2015) reported that the indigenous yeasts and molds on cantaloupes were not significantly reduced even at 1.5 kGy. There are previous studies, which show that yeasts are more resistant than bacteria to ionizing radiation and, therefore, the resistance observed in this study is not too surprising. The indigenous lactic acid bacteria within the cantaloupes were reduced by only 0.2 log at 0.7 kGy but were reduced by > 2 logs at 1.5 kGy. However, the lactic acid bacterial 2
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compared to 39% in the untreated samples. It must be noted that no attempt was made to store the blueberries under optimized atmospheric conditions. It is possible that if the atmospheric conditions in the packages were optimized the decay percentages in the treated samples could be more pronounced. The authors also report that eBeam treatment had no adverse effect on the total monomeric anthocyanins (TMA) content among blueberries stored refrigerated for 7 days and 15 days. Similarly, the antioxidant activity in the blueberries were unaffected by eBeam doses less than 3 kGy. During storage both the treated and the untreated blueberries exhibited significant reduction in their antioxidant activity. Interestingly, there was no loss of L-ascorbic acid in blueberries treated below 3 kGy. The authors attribute this difference in results compared to previously published results which indicate that Lascorbic acid is sensitive to irradiation to differences in blueberry cultivars, quality, packaging, and storage. Overall, this study indicated that even at low eBeam doses ~ 1 kGy appreciable improvements in microbiological quality and shelf life can be expected. This paper is also noteworthy in using “% decay” as an index of shelf-life. With additional optimization of the storage conditions, one can expect enhanced value from the use of eBeam processing. Tong et al. (2015) studied the quality of blueberries and grapes after exposure to phytosanitary treatment doses of eBeam. They studied the quality and consumer acceptance attributes using 3 different varieties of blueberries (Star, Jewel, and Snowchaser) and 2 grape varieties namely, “Sugarone and Crimson Seedless”. The blueberries and grapes were irradiated at doses between 400 and 590 Gy and 400–500 Gy, respectively. The quality attributes (firmness, color, weight loss, and the ratio of soluble solids concentration to titratable acidity). The storage period (3 days and 18 days under refrigeration and 3 days at ambient conditions) were used to simulate ground and ocean shipments. The paper is noteworthy in that it describes the eBeam dosing and dosimetry to ensure uniform dosing. The consumer acceptability scores are based on 80–100 responses. Their studies showed that there were significant differences in how the different blueberry and grapes varieties respond to eBeam treatment. Among all other attributes, texture was primarily affected. There was no difference between the un-treated and eBeam treated samples in terms of consumer acceptability scores even after 3 weeks of refrigerated storage or 3 days of ambient storage.
counts increased significantly to over 7.0 logs by the end of the 21 days study. These results suggest that if the number of spoilage bacteria is reduced initially by the application of an appropriate eBeam dose, the shelf life of these cantaloupes can be extended by a specific length of time, though not indefinitely. Though microbial bioburden increases are an indication of product spoilage, the precise threshold where a certain bioburden load is indicative of undesirable quality is still elusive. Smith et al. (2017) recently reported on the value of low dose eBeam (≤ 1 kGy) treatment for preserving fresh cut watermelon cubes for use in healthy vending machines. In their studies, they monitored the microbiological quality, sensory attributes (color, texture) as well as consumer acceptability. In their study, they did not wash the watermelons cubes prior to study. However, considering the presence of natural bioburden on the outer surface of watermelon and the fact that eBeam is not a clean-up technology this approach (of not having a preliminary wash step) is unrealistic for routine use. The authors used aseptic procedures and prepared 50 g of watermelon cubes as experimental units and described in detail the steps they took to ensure reliable dosimetry. They monitored bacterial and fungal counts on watermelon cubes stored refrigerated under ambient and modified atmosphere packaging (5% oxygen, 10% carbon dioxide, and 85% nitrogen) conditions. Using Mann-Whitney statistical tests, they concluded that the bacterial and fungal populations’ levels were statistically unchanged up to 7 days of refrigerated storage under ambient conditions. Under MAP conditions, there was no statistical difference between the counts in the eBeam treated samples and prior to treatment suggesting that the combination of MAP and eBeam helped control microbial proliferation. In terms of color (redness), the eBeam treated samples by itself or in combination with MAP were significantly redder than the control samples. The eBeam treatment either under ambient or MAP conditions did not negatively influence the texture. The consumer acceptability scores of the eBeam treated samples (ambient or MAP) scored values greater than 6 out of a 9 hedonic scale in all attributes (appearance, odor, color, firmness) except flavor (between 5.14 and 5.22) (where even the control, untreated sample scored only a 6.0). Overall, there results suggest that even at doses ≤ 1 kGy, the shelf life of watermelon cubes is improved without any loss of sensory attributes thereby opening up a new avenue (i.e. healthy vending machines) for the distribution of eBeam treated fresh produce.
4. Future research needs 3.2. Blueberries
There are books, book chapters, industry articles, and review articles that in general discuss the value of using eBeam technology for fresh produce. However, the number of peer-reviewed original research publications detailing the efficacy of eBeam technology for different fresh produce commodities (especially for extending shelf-life) is extremely limited. Similarly, the number of peer-reviewed original research articles discussing the efficacy of eBeam technology to eliminate specific microbial pathogens on fresh produce is also limited. However, this body of literature is growing. The lack of original research articles related to eBeam and fresh produce could be attributed to the limited number of eBeam facilities that are available to perform this type of research. There is a need for research to develop better and realistic metrics to be used to evaluate shelf-life. For example, the USDAAgricultural Marketing Service has specific guidelines to rate the quality attributes of different commodities at point of shipping (USDAAMS, 2002). Produce quality studies with eBeam technology should at the very minimum adopt accurate dosimetry practices and the papers should include information about the minimum and maximum doses measured. Future studies that focus on microbial inactivation should ensure that the dosimetry employed is accurate and that uniform doses are employed for determining the D-10 value. The microbial inactivation should then be validated using inoculation studies or naturally contaminated samples. One area that is worthy of investigation is the potential accumulation of phytochemicals in fresh produce as a result of exposure to eBeam treatment. Whether the low eBeam doses employed
Kong et al. (2014) reported on the nutritional quality and shelf life of blueberries when inoculated with E.coli and exposed to eBeam at doses ranging between 0.5 kGy and 3.0 kGy. In this study, blueberries were inoculated with the bacterial culture in plastic bags and allowed to dry at room temperature before exposure to eBeam irradiation. The authors calculated the D-10 value of the E.coli strain on the blueberries to be 0.37 ± 0.015 kGy. The authors have recognized the importance of accurately measuring the dose uniformity ratio in their paper. The authors have expressed shelf life as a decay percentage (%) concept. The decay percentage was scored visually based on the appearance of fungal mycelium. This concept is noteworthy because measuring “shelflife” can be open to a number of interpretations. They used a n = 100 fruits to score the decay percentage. The decay percentage was calcunumberofdecayed fruit lated as totalnumberof fruits X100 . In addition to monitoring the decay percentage the authors also measured a number of parameters such as Lascorbic acid, antioxidant activity, etc. The blueberries exposed to 1.0 kGy had only a 10% decay rate compared to 40% in the untreated samples after 2 days of storage. The decay percentage was 0 in the 2.0 kGy treated blueberries after 2 days of room temperature storage. After 8 days of room temperate storage, there was a 70% decay rate in the untreated samples compared to 60% and 50% in the 1 kGy and 2 kGy treated samples. When stored refrigerated, however, even after 14 days of storage the 1 kGy treated samples exhibited only a 24% decay rate 3
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Neill, F.H., Blutt, S.E., Zeng, X., Qu, L., Kou, B., Antone, R., Burrin, D., Graham, D.Y., Ramani, S., Atmar, R.L., Mary, K., 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science 353, 1387–1393. http://dx.doi.org/10.1126/ science.aaf5211. FDA, 2017. FDA investigates multiple Salmonella outbreaks strains linked to papayas. 〈https://www.fda.gov/Food/RecallsOutbreaksEmergencies/Outbreaks/ucm568097. htm〉. (Accessed 29 August 2017). Huang, S., Huang, K., 2007. Increased U.S. Imports of Fresh Fruit and Vegetables. A Report from the Economic Research Service. USDA. FTS-328-01. . 〈http://citeseerx. ist.psu.edu/viewdoc/download?Doi=10.1.1.621.7731&rep=rep1&type=pdf〉 (Accessed in April 2017). IAEA, 2015. New IAEA Guide Helps Developing Countries Improve Food Irradiation Practices. Topical reports. . 〈https://www.iaea.org/newscenter/news/new-iaeaguide-helps-developing-countries-improve-food-irradiation-practices〉 (Accessed in April 2017). Kong, Q., Wu, A., Qi, W., Qi, R., Carter, J.M., Rasooly, R., He, X., 2014. Effects of electronbeam irradiation on blueberries inoculated with Escherichia coli and their nutritional quality and shelf life. Postharvest Biol.Technol. 95, 28–35. Matic, S., Mihokovic, V., Katusinrazem, B., Razem, D., 1990. The eradication of Salmonella in egg powder by gamma-irradiation. J. Food Prot. 53, 111–114. Moreira, R.G., Puerta‐Gomez, A.F., Kim, J., Castell‐Perez, M.E., 2012. Factors affecting radiation D‐values (D10) of an Escherichia coli cocktail and Salmonella typhimurium LT2 inoculated in fresh produce. J. Food Sci. 77 (4), E104–E111. Painter, J.A., Holekstra, R.M., Ayers, T., Taue, R.V., Braden, C.R., Angulo, F.J., Griffin, P.M., 2013. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg. Inf. Dis. http://dx.doi.org/10.3201/eid1903.1111866. Palekar, M.P., Taylor, T.M., Maxim, J.E., Castillo, A., 2015. Reduction of Salmonella enterica serotype Poona and background microbiota on fresh-cut cantaloupe by electron beam irradiation. Int. J. Food Microbiol. 202, 66–72. Pillai, S.D., 2017. Food irradiation – a technology that is moving away from photons to electrons. Spring 3 (2). Pillai, S.D., Shayanfar, S., 2015. Electron Bean Pasteurization and Complementary Food Processing Technologies. Woodhead Publishing, Cambridge, UK. Pillai, S.D., Bogran, C., Blackburn, C., 2014. Ionizing irradiation for phytosanitary applications and fresh produce safety. In: Global Safety of Fresh Produce 2013. Woodhead Publishing, Cambridge, UK, pp. 221–222. Predmore, A., Sanglay, G.C., DiCaprio, E., Li, J., Uribe, R.M., Lee, K., 2015. Electron beam inactivation of Tulane virus on fresh produce, and mechanism of inactivation of human norovirus surrogates by electron beam irradiation. Int. J. Food Microbiol. 198, 28–36. Shayanfar, S., Mena, K.D., Pillai, S.D., 2017. Quantifying the reduction in potential infection risks from non-O157 Shiga toxin producing Escherichia coli in strawberries by low dose electron beam processing. Food Cont. 72, 324–327. Smith, B., Ortega, A., Shayanfar, S., Pillai, S.D., 2017. Preserving quality of fresh cut watermelon cubes for vending distribution by low-dose electron beam processing. Food Cont. 72, 367–371. Tong, J., Rakowski, C., Prakash, A., 2015. Phytosanitary irradiation preserves the quality of fresh blueberries and grapes during storage. HortScience 50, 1666–1670. USDA-AMS, 2002. Blueberries. Shipping Point and Market Inspection Instructions. 〈https://www.ams.usda.gov/sites/default/files/media/Blueberry_Inspection_ Instructions%5B1%5D.pdf〉 (Accessed August 2017).
will actually result in detectable differences in phytochemicals is worth investigating. There is also a need for introducing other non-thermal synergistic microbial inactivation methods such as ultra-sonication or pulsed light in addition to eBeam in order to maximize the efficiency of doses < 1 kGy. The ability to further reduce molds, yeasts, spore formers and viruses is of great value to the produce industry. More detailed studies are needed to evaluate the optimal packaging conditions (ambient or modified atmosphere) to enhance shelf life and retard spoilage. As mentioned earlier, new additional metrics for calibrating shelf-life are needed. The advances in transcriptomics and metabolomics as well as in analytical methods such as GC-olfactometry should be harnessed to further our understanding of what constitutes shelf-life (Bhatia et al., 2017). There is industry interest in changing the maximum permitted dose for fresh produce beyond the current 1 kGy dose. The recent outbreaks of Salmonella in papayas (FDA, 2017) as well as the realization that fresh produce is linked to most foodborne illnesses calls for the use of eBeam technology as a pathogen kill-step (Pillai, 2017). Therefore, studies have to be published that document that there are no detrimental effects on nutrient and other beneficial attributes of fresh produce when exposed to varying eBeam doses. These research findings will be of great value to industry trade groups and others when they file petitions to the FDA to expand the applications of ionizing radiation for fresh produce. References Bhatia, S., Wall, K., Kerth, C.R., Pillai, S.D., 2017. Benchmarking the minimum electron beam (eBeam) dose required for the sterilization of space foods. Rad. Phys. Chem. http://dx.doi.org/10.1016/j.radphyschem. (2017.08.007). CDC, 2013. Available at: 〈https://wwwnc.cdc.gov/eid/article/19/3/11-1866_article〉 (Accessed in April 2017). Clemmons, H.E., Clemmons, E.J., Brown, E.J., 2015. Electron beam proessing of fresh and/or frozen raw ground beef (Chapter 14). In: Pillai, S.D., Shayanfar, S. (Eds.), Electron Beam Pasteurization and Complimentary Food Processing Technologies. Woodhead Publishing, Oxford. DiCaprio, E., Phantkankum, N., Culbertson, D., Ma, Y., Hughes, J.H., Kingsley, D., Uribe, R.M., Li, J., 2016. Inactivation of human norovirus and Tulane virus in simple media and fresh whole strawberries by ionizing radiation. Int. J. Food Microbiol. 232, 43–51. Espinosa, A.C., Jesudhasan, P., Arredondo, R., Cepeda, M., Mazari-Hiriart, M., Mena, K.D., Pillai, S.D., 2012. Quantifying the reduction in potential health risks by determining the sensitivity of poliovirus type 1 chat strain and rotavirus SA-11 to electron beam irradiation of iceberg lettuce and spinach. Appl. Environ. Microbiol. 78 (4), 988–993. Ettayebi, K., Crawford, S.E., Murakami, K., Broughman, J.R., Karandikar, U., Tenge, V.R.,
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