With many health benefits in mind, the consumption and demand for fresh produce continues to increase in the U.S. While most fresh produce brought to the retail market has received either no or minimal treatment, over the last 10 years, increasing volumes of produce are being further processed and brought to the consumer as a value-added, fresh-cut, ready-to-eat (RTE) product in convenient packages. However, continued recalls and high-profile outbreaks linked to foodborne pathogens keep reminding us of the potential microbial risks associated with fresh-cut produce. Consequently, the microbial safety of fresh-cut produce has become an important concern for growers, processors, retailers and consumers across the farm-to-fork continuum.

Fruits and vegetables are prone to microbial contamination from a wide range of sources, including irrigation water, soil, fertilizer, insects, animal feces and field workers during preharvest processing. After harvest, fresh produce is transported to processing facilities for further processing, which may include such steps as dump-tank washing, sanitizing, slicing, shredding, dewatering, conveying, sorting and packaging. Thereafter, these products make their way through the cold chain to foodservice or retail stores, finally reaching the consumer. Centralized production of certain fresh-cut RTE products combined with the complex nationwide distribution system can magnify a small contamination event and lead to foodborne outbreaks of epic proportions. This article focuses on the key steps impacting the microbiological safety of fresh-cut produce from commercial preparation to consumption.

Slicing and Dicing   
Commercial preparation of fresh-cut produce invariably involves shredding (e.g., lettuce, cabbage), slicing (e.g., tomatoes, onions, cucumbers) or dicing (e.g., celery, green pepper, melon) with or without prior washing, during which time both spoilage and pathogenic microorganisms, such as Salmonella, Listeria and Escherichia coli O157:H7, can be transferred from the intact outer surface of the product to multiple cut surfaces and subsequently grow, resulting in spoilage or a potentially hazardous situation. Regardless of the cutting process, contact between the product and blade as well as other food contact surfaces of the shredder, slicer or dicer will in fact lead to extended transfer of microorganisms that can seriously compromise both the quality and safety of large volumes of product generated during extended production runs. While some cross-contamination during cutting is unavoidable, the extent of microbial transfer must be better controlled, given the recent surge in foodborne outbreaks traced to an ever-widening range of products. Progress in this area can only come through a better understanding of those factors that can affect bacterial transfer during processing, with such new knowledge leading to improved equipment designs and the development of science-based transfer models for risk assessments.

One such study conducted at Michigan State University using a pilot-scale leafy green processing line tracked the transfer of E. coli O157:H7 from 20 pounds of inoculated radicchio (106 CFU/g) used as a colored surrogate for iceberg lettuce to 2,000 pounds of iceberg lettuce during shredding, conveying, flume washing without a sanitizer, shaker table dewatering and centrifugal drying.[1] Overall, the contaminated product continually spread during leafy green processing long after the contamination event. During processing, the inoculated radicchio spread to all 2,000 pounds of iceberg lettuce with 94, 1.3, 0.8 and 0.5 percent of the radicchio, respectively, recovered from pounds 1 to 500, 501 to 1,000, 1,001 to 1,500 and 1,501 to 2,000. Microbial analysis of radicchio-free iceberg lettuce showed that these same groupings contained average E. coli O157:H7 populations of 1.69-, 1.22-, 1.10- and 1.11-log CFU/g, respectively. After processing, the hundreds of radicchio pieces that still clung to the various equipment surfaces were most prevalent on the conveyor (9.8 g) (Figure 1), followed by the shredder (8.3 g), flume tank (3.5 g) and shaker table (0.1 g). Using these findings, various quantitative transfer models can be developed as shown in Figure 2, which will benefit both risk assessors and the industry in making better-informed decisions in the event of a product recall.[2] Given the multitude of sites in complex commercial leafy green processing lines where product can linger and periodically slough off, these same models also reinforce the need for more frequent cleaning and sanitizing during long processing runs and improved equipment designs that will maximize product flow-through.    

Similar to shredding, commercial slicing of fruits and vegetables also can lead to the spread of microbial contaminants to previously uncontaminated product. Unlike mechanical shredding of leafy greens, which is a relatively uniform process across the industry, commercial practices employed for slicing fresh produce vary from completely manual (e.g., hand-held knives) to semimanual (e.g., hand-operated slicers) and, in a few cases, automated, depending on the processor and the product, with much of this work being extremely repetitive and labor-intensive due to the human element. The commercial slicing of tomatoes still heavily relies upon the use of manual countertop slicers. Although many different brands of slicers are currently available, most are based on a similar design in which tomatoes are individually pushed through a stationary set of equally spaced horizontal blades. Prior to slicing, tomatoes are normally washed in a sanitizer solution to decrease the microbial load on the surface; however, the slicer won’t typically be cleaned and sanitized until the end of processing. Consequently, any foodborne pathogens surviving the sanitizer treatment can potentially transfer to the slicer, leading to cross-contamination of subsequent products.

One recently published study investigating cross-contamination of tomatoes during slicing showed that norovirus was able to spread from one inoculated tomato used to contaminate the slicer to all subsequently sliced tomatoes, with these data fitted to a logarithmic model.[3] In our laboratory, we looked at the spread of Salmonella during slicing of tomatoes and how different processing variables impact transfer.[4] Unlike the norovirus transfer study, a two-parameter exponential decay model was fitted to our data. Among the different variables assessed, only tomato variety and tomato surface wetness had a significant impact on Salmonella transfer during slicing, with the extent of cross-contamination unaffected by the other processing variables including temperature of the room during slicing, slice thickness or post-contamination hold time of the slicer before resumption of slicing. While not statistically significant, Salmonella transfer tended to be lower using an electric slicer that accumulated fewer organisms compared to the manual slicer (Figure 3). Further analysis of different tomato varieties revealed that those having a softer texture and higher water content can potentially decrease Salmonella transfer during slicing. Therefore, from an industry processing point of view, selection of proper tomato varieties and sufficient washing in an appropriate sanitizer solution are critical for minimizing potential cross-contamination during slicing.

Dicing, the last of three main unit operations for preparing fresh-cut produce, is best suited for products having a firm texture such as onions, celery, peppers and Roma tomatoes. Unlike slicing, dicing requires that the product be cut in three directions (the last two being perpendicular) as opposed to a single direction to obtain cubes. Both manual and electric dicers are inherently more complex in their design compared to slicers, raising increased concerns in regard to cross-contamination during normal operation as well as cleaning and sanitizing afterward. Our research with tomatoes, onions and celery confirmed greater and more uniform spread of Salmonella and Listeria during dicing as opposed to slicing. To evaluate the extent of pathogen transfer during mechanical dicing, one batch of Salmonella-inoculated Roma tomatoes (0.9 kg) was diced using a large-scale commercial dicer, followed by 10 batches of uninoculated tomatoes. When a two-parameter exponential decay model was fitted to the data as in the slicing study, Salmonella populations decreased significantly from 3.3- to 1.1-log CFU/g in the 10 batches of uninoculated tomatoes after dicing.[5]

In other work using L. monocytogenes-inoculated Swiss chard stems as a colored surrogate for celery, Listeria transferred to all batches of uninoculated celery during dicing, with populations decreasing from 5.2- to 2.0-log CFU/g.[6] As in the radicchio/lettuce study discussed earlier, pieces of inoculated Swiss chard were again present in all batches after dicing. However, in contrast to slicing, diced and shredded products are typically subjected to flume washing to decrease the microbial load and remove unwanted material (e.g., fines, seeds) during subsequent dewatering and conveying.  

Sanitizer Washing  
A wide range of commercial and noncommercial sanitizers have been investigated over the past decade for their ability to minimize cross-contamination of produce during washing. When used properly, many of these sanitizer treatments are capable of reducing the microbial load in commercial flume water by up to 5 logs. However, these same treatments will typically decrease microbial populations on the product being washed by no more than 2 logs.

The increased organic load in flume water as a result of soil and leached plant material is a major contributor to decreased efficacy of chlorine-based sanitizers, which are most commonly used in industry. Although fresh-cut produce processors often monitor oxygen reduction potential instead of free chlorine during flume washing as an indicator of sanitizer efficacy, this practice has proven less than ideal. In a recent pilot-plant-scale lettuce processing study, Davidson assessed the correlation between sanitizer (chlorine, peroxyacetic acid and mixed peracid) efficacy against E. coli O157:H7 and various physicochemical parameters of lettuce wash water containing an organic load of up to 10 percent.[7] As expected, an increased organic load negatively impacted efficacy of the chlorine treatment while the efficacy of peroxyacetic acid and mixed peracid remained relatively unaffected. Reduced sanitizer efficacy similarly correlated to increases in total solids, chemical oxygen demand and turbidity, and decreases in maximum filterable volume. Based on these findings, when using a chlorine-based sanitizer, every attempt should be made to minimize the organic load in the flume water and process finely shredded product near the end of production to minimize microbial cross-contamination during processing.   

All fresh-cut produce is perishable and must be properly packaged to maximize both end-product quality and safety. Some products such as fresh-cut leafy greens and baby spinach are packed in flexible pouches or bags, whereas sliced/diced tomatoes, onions, celery and berries are typically found in rigid containers. Modified atmosphere packaging and active packaging (e.g., CO2-absorbing sachets) are also used in the produce industry, particularly for those products having a high respiration rate. In addition to meeting the minimum requirements for shelf-life extension, other issues surrounding the packaging material include the permeability rates for oxygen, carbon dioxide and water, which are critical to maintaining the appropriate product-dependent in-package atmosphere as well as tensile strength, puncture resistance, sealability and eventual biodegradability of the package. Consequently, extending the freshness of fresh-cut produce is particularly complex, with different packaging strategies needed due to the wide variation in respiration rates for different products.

Working at Michigan State University, Page and Scollon investigated the effect of different modified atmospheres (99 percent O2, 15 percent CO2 plus 5 percent O2, or air) on the growth of E. coli O157:H7 and L. monocytogenes in spinach[8] and diced onions, respectively. After 10 days of refrigerated storage, E. coli O157:H7 populations decreased about 2 logs in packaged spinach containing 15 percent CO2 plus 5 percent O2 compared to less than 1 log when the same product was packaged in 99 percent O2 or air. However, the use of biodegradable polylactic acid bags in conjunction with a high-oxygen atmosphere reduced the extent of L. monocytogenes growth on diced onions during extended refrigerated storage. A wide range of packaging films coated with various antimicrobial agents also have been developed in an attempt to help prolong both the shelf life and safety of fresh-cut fruits and vegetables. Some rigid packaging systems that can generate antimicrobial gases such as ozone or chlorine dioxide within the package headspace have also been evaluated. However, the increased cost of such packages combined with nonuniform gas concentrations inside the package headspace are currently limiting their commercial adoption.

Transportation/Retail Storage/Display
After packaging, fresh-cut produce must be quickly distributed across hundreds or thousands of miles to the point of sale using temperature-controlled trucks. The U.S. Food and Drug Administration Food Code has mandated that all RTE fruits and vegetables be refrigerated at less than or equal to 5°C during transportation and retail storage/display to minimize the growth of foodborne pathogens.[9] However, maintaining this temperature during loading/unloading in the heat of summer, retail storage, retail display and at home remains an ongoing challenge. Consequently, any prolonged temperature abuse that fresh-cut produce typically encounters in the cold chain may compromise both product quality and safety.

Many studies have assessed the growth potential for foodborne pathogens in fruits and vegetables during extended storage. However, in virtually all of these reports, fixed temperatures were used that do not reflect the actual conditions that products encounter in the distribution chain. One recent study by Zeng evaluated the growth of E. coli O157:H7 and L. monocytogenes in packaged fresh-cut romaine salad mix under fluctuating temperatures collected during commercial transport, retail storage and display.[10] Over a 16-month period, a series of time-temperature profiles for bagged salads was obtained from five transportation routes covering four geographic regions (432 profiles) as well as during retail storage (4,867 profiles) and display (3,799 profiles) at 19 supermarkets. Thereafter, five time-temperature histories were duplicated in a programmable incubator to assess E. coli O157:H7 and L. monocytogenes growth in commercial bags of romaine lettuce mix. Overall, both pathogens generally increased less than 2-log CFU/g during transport, storage and display. However, the durations for temperature abuse seen at retail can significantly impact pathogen growth, with E. coli O157:H7 and L. monocytogenes populations increasing as much as 3.1- and 3.0-log CFU/g during retail storage, respectively (Figure 4). These findings from the first large-scale U.S. study will provide critical data for risk assessments related to fresh-cut fruits and vegetables. From the commercial standpoint, temperature control while the product is in the cold chain, along with proper training of retail food receivers and handlers, and continued consumer education remain among the most critical challenges for enhancing the microbial safety of fresh-cut produce. The many industry and retail guidelines that have since been put in place for proper handling of fresh fruits and vegetables during transport and retail storage/display should help further enhance both the safety and quality of fresh-cut produce reaching consumers. 

Home Storage/Handling  
After the point of purchase, fresh-cut produce will again be subjected to abuse during transport and then be either prepared or stored. Special attention must be given to fresh fruits and vegetables that are consumed raw since improper hand washing, cross-contamination from knives and cutting boards used for raw meat or poultry and other common food handling errors will all increase the likelihood of foodborne illness. In addition, the potential for temperature abuse during transport of fresh produce after purchase should also be minimized.  

In one recent study evaluating the food safety risks posed by temperature abuse in the trunks of cars, the internal car trunk temperature was as high as 41.5°C, with food product temperatures ranging from 33.5 to 38.4°C.[11] The temperature of previously refrigerated foods (e.g., eggs, milk and fresh meat) reached 20°C within 40 minutes and 30°C within 90–110 minutes. Although fresh fruits and vegetables were not included in this study, the potential risk for fresh-cut produce is obvious given these highly abusive conditions. During the hot summer months, the use of coolers for fresh produce and other temperature-sensitive products should be considered to decrease temperature fluctuations until these items can be properly refrigerated.

Similarly, proper temperature control during storage of produce at home is also critical for minimizing potential microbial risks. Based on one survey of 200 homes in the United States, 3.7 and 12.7 percent of the refrigerators had mean temperatures above 7.3°C for the bottom and door compartments, respectively, with the temperature in the door compartment exceeding 4°C for 39.3 percent of the time.[12] Hence, proper consideration must be given to where perishable foods, including fresh produce, are stored in the refrigerator. Consumers also need to be educated to deal with extreme conditions such as extended power outages.[13]

After removing fresh produce from the refrigerator, the last step prior to consumption is preparation. Rewashing of commercially washed and prepackaged fresh-cut produce such as bagged salad mixes is of little further benefit and should be avoided to minimize potential cross-contamination from the kitchen surroundings. However, washing of non-fresh-cut fruits and vegetables remains a critically important step in reducing the hazards associated with foodborne illness. Leafy greens and other delicate vegetables should be washed in clean water to which various produce sanitizers (not soaps) may be added for increased efficacy. Products with rough outer surfaces such as cantaloupe should be thoroughly scrubbed to prevent the transfer of potential pathogens from the rind to the flesh of the fruit, with the same produce sanitizers again being helpful. Alternatively, cantaloupe can be subjected to brief immersion in hot water as is being done by some commercial processors.  

Given today’s fast-paced lifestyle, the demand for fresh-cut produce has increased dramatically, with many out-of-season products being shipped across the country or from abroad. Hence, one food safety break in the fresh produce chain can lead to a product recall or outbreak that can negatively impact the entire market for months or years, with the fresh produce industry having paid a high price over the past decade. However, through these unfortunate events, many lessons have also been learned, with new strategies now continuously being developed to enhance the safety of fresh produce. In addition to the development of stricter Good Agricultural Practices, Good Manufacturing Practices and Sanitation Standard Operating Procedures, the new proposed rule for produce safety, “Standards for the Growing, Harvesting, Packing, and Holding of Produce for Human Consumption,” as part of the Food Safety Modernization Act,[14] represents a major step forward in enhancing the safety of fresh produce from farm to fork. 

Haiqiang Wang is a Ph.D. candidate in food science at Michigan State University.         

Elliot T. Ryser, Ph.D., is a professor in the department of food science and human nutrition at Michigan State University.

1. Buchholz, A.L. et al. 2010. Tracking an Escherichia coli O157:H7 contaminated batch of leafy greens through a simulated commercial processing line. Abstract T4-02. Anaheim, CA: IAFP annual meeting.
2. Pérez-Rodríguez, F. et al. 2011. A mathematical risk model for Escherichia coli O157:H7 cross-contamination of lettuce during processing. Food Microbiol 28:694–701.
3. Shieh, Y.C. et al. 2014. Tracking and modeling norovirus transmission during mechanical slicing of globe tomatoes. International Journal of Food Microbiol 180:13–18.
4. Wang, H., and E.T. Ryser. 2013. Quantitative transfer of Salmonella during commercial slicing of tomatoes as impacted by multiple processing variables. Abstract. Charlotte, NC: IAFP annual meeting.
5. Wang, H., and E.T. Ryser. 2014. Transfer and sanitizer inactivation of Salmonella during simulated commercial dicing of tomatoes. Abstract. New Orleans, LA: IFT annual meeting.
6. Kaminski, C., G. Davidson and E.T. Ryser. 2014. Listeria monocytogenes transfer during mechanical dicing of celery and growth during subsequent storage. J Food Prot 77:765–771.
7. Davidson, G.R. 2013. Impact of organic load on sanitizer efficacy against Escherichia coli O157:H7 during pilot-plant production of fresh-cut lettuce. Ph.D. dissertation, Michigan State University.
8. Page, N. et al. 2013. The effect of different packaging technologies on Escherichia coli growth in fresh spinach. Abstract. Chicago: United Fresh annual meeting.
9. www.fda.gov/Food/GuidanceRegulation/RetailFoodProtection/FoodCode/UCM2019396.htm.
10. Zeng, W. et al. 2014. Growth of Escherichia coli O157:H7 and Listeria monocytogenes in packaged fresh-cut romaine mix at fluctuating temperatures during commercial transport, retail storage, and display. J Food Prot 77:197–206.
11. Kim, S.A. et al. 2013. Temperature increase of foods in car trunk and the potential hazard for microbial growth. Food Control 29:66–70.
12. Godwin, S. et al. 2007. A comprehensive evaluation of temperatures within home refrigerators. Food Prot Trends 27:16–21.
13. Godwin, S.L. et al. 2010. Keeping food safe during an extended power outage: A consumer’s perspective. J Emerg Manag 8:44–50.
14. www.fda.gov/Food/GuidanceRegulation/FSMA/ucm334114.htm.