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Effects of post-processing handling and packaging on microbial populations
Postharvest Biology and Technology 15 (1999) 313 – 321
Effects of post-processing handling and packaging on microbial populations Devon Zagory * De6on Zagory and Associates, 759 North Campus Way, Da6is, CA 95616, USA Received 30 June 1998; accepted 11 November 1998
Abstract The type of produce, process conditions, and prior temperature management will all affect the mix of microorganisms found on fresh produce. Normally, fresh produce will be covered by a complex mix of bacteria, fungi and yeasts that are characteristic of that fruit or vegetable. For example, carrots typically have large numbers of Lactobacillus and other lactic acid bacteria while apples may have relatively large numbers of yeasts. Which of these microorganisms will come to dominate the population will be a function of the make-up of the original population on the product in the field, distribution time, distribution temperature and the atmosphere within the package. Another chief determinant of microbial populations will be the physiological condition of the product. Factors that injure or weaken the plant tissues may be expected to encourage microbial growth while conditions that maintain the physiological integrity of the tissues may be expected to discourage microbial growth. Each of these factors can be expected to affect the make-up of the microbial population in characteristic ways but always constrained by the initial condition of original population makeup. This paper describes which microorganisms are favored by given conditions in order to develop a concept of microbial management designed to favor desirable microbes at the expense of undesirable ones. Particular emphasis will be placed on the effects of modified atmospheres on microorganisms, especially human pathogens. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Fresh-cut; Bacteria; Fungi; Pathogen; Modified atmosphere; Packaging; Irradiation; Sanitation
1. Introduction
Manuscript from presentation at Beltsville Agricultural Symposium, May 3 – 6, 1998. * Corresponding author.
The subject of this paper will not be a comprehensive review of the research literature regarding microbial population dynamics on fresh produce. The literature is large and disperse and, often times, contradictory. Results have been generated
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under different experimental systems and evaluated according to different criteria and seldom make up a coherent whole. Little of the research has been incorporated into commercial practice, and that which has, has often been misunderstood and misapplied. Commercial experience has led to certain assumptions about produce microbiology. Those assumptions have led to the assignment of causality and this presumptive causality has evolved into conventional wisdom. Examples of commercial conventional wisdom include: high microbial populations result in shortened shelf-life; the lower the initial bacterial counts on produce the better the produce quality and the longer the shelf-life; modified atmospheres reduce microbial populations; the purpose of wash water sanitizing chemicals is to remove bacteria from produce; irradiation of fresh produce can remove human pathogens and ensure safety. Much of the conventional wisdom may be inaccurate and may lead to misguided or even unsafe sanitation practices. This attempt to address some of the conventional wisdom will be not as a typical hypothesis paper but rather more as an antithesis paper that will explore some research results that reflect on some of the conventional wisdom about microbial populations on fresh-cut produce as affected by processing, post processing handling and packaging.
2. Microbial populations on fresh produce The numbers and kinds of microorganisms found on fresh produce, and specifically on freshcut (minimally processed) produce, are highly variable. Mesophilic bacteria from plate count studies typically range from 103 to 109 CFU g − 1. Total counts on products after processing range from 103 to 106 CFU g − 1 (Nguyen-the and Carlin, 1994). The bacteria normally found on freshcut products are the same as those normally found on produce in the field. The microflora of vegetables and fruits is made up largely of Pseudomonas spp., Erwinia herbicola, Fla6obacterium,
Xanthomonas, and Enterobacter agglomerans as well as various molds. Lactic acid bacteria, such as Leuconostoc mesenteroides and Lactobacillus spp., are also commonly found, as are several species of yeasts (primarily on fruits). Pseudomonas normally dominates and may make up 50–90% of the microbial population on many vegetables (Zagory and Hurst, 1996). Typically these microorganisms are not harmful to humans. In fact many different genera of microorganisms can be found on fresh produce and what is found largely reflects the conditions and media used for isolation. Many of the most common media and growth conditions select for mesophillic bacteria that grow rapidly at temperatures of 25–35°C. Other common media select for coliform or fecal coliform bacteria that also grow well at higher temperatures. Few studies have directly assayed for the psychrotrophic microbes that would be expected to dominate at the refrigeration temperatures recommended for fresh-cut produce. For this reason, our views of microbial population dynamics on fresh-cut produce may be incomplete and imprecise.
3. Microbial populations and shelf life Many of the concepts regarding the microbiology of fresh produce have come from concerns with spoilage microorganisms, plant pathogens and extension of shelf life. The correlation of development of large populations of microorganisms with the end of shelf life has led to the assignment of causality, that is, that proliferation of microorganisms is a primary cause of the end of shelf life. This assignment of causality has led to strategies to reduce total bacterial counts as a way to maintain quality and extend shelf life. However, a weight of published research does not support this view. In many cases total bacterial numbers bear little or no relationship to product quality or to shelf life. In Fig. 1, spoilage is associated with injurious levels of carbon dioxide, but not with populations of aerobic bacteria. Total numbers of psychrotrophic microorganisms of 106 or 107 have been associated with high visual quality ratings (Barriga et al., 1991). Again,
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Fig. 1. Effects of CO2 + 10% O on spoilage and populations of aerobic bacteria of cut endive at 3C. Data received from: Carlin et al., 1996.
there was very little correlation between bacterial populations and product quality. Deterioration of cabbage in coleslaw was similar at 7 and 14°C, but microbial growth was much greater at the higher temperature (King et al., 1976). Spoilage of fresh-cut kiwifruit, papaya, and pineapple stored at 4°C was not a consequence of microbial growth (O’Connor-Shaw et al., 1994). Many other published studies report a similar lack of linkage between spoilage and bacterial populations. Of course, in some instances, specific bacteria or plant pathogenic fungi may be associated with particular forms of spoilage. Pectinolytic bacteria and fungi may lead to breakdown of tissues and subsequent spoilage. In addition, lactic acid bacteria may be associated with spoilage of specific commodities, such as carrots. Spoilage of shredded carrots after 14 days at 10°C was always associated with large populations of L. mesenteroides, though not with mesophilic bacterial populations (Carlin et al., 1989). However, even in these instances, there is little evidence for causality. Pectinolytic plant pathogens tend to be opportunistic and will only effectively invade through wounded or senescent tissues. A temperature of 10°C is well above the optimal for carrots and can be considered an abusive temperature.
If bacterial populations are not directly associated with quality or shelf life in a causal way, with what do they have a causal relationship? The available evidence suggests that microbial growth and populations depend primarily upon the morphological and physiological condition of the plant tissues. Intact, healthy tissues may be expected to be a poor substrate for growth of opportunistic microorganisms. Damaged, physiologically compromised tissues would deteriorate faster and provide a better substrate for microbial growth. The conclusions from a study by Bolin et al. (1977) describe some of the factors that have a significant effect on quality and shelf life of freshcut produce: marketable quality was retained 2.5 times longer at 2°C than at 10°C. Temperature is a controlling factor for shelf life and quality; a sharp blade slicing was superior to either a sharp blade chopping or a dull blade slicing or chopping; smaller shred size reduced storage life. Physical damage of the shredded lettuce reduced its storage life; presence of free moisture or cellular fluids on the lettuce surface reduced storage life. It appears that rather than high microbial populations being responsible for deterioration of
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fresh produce, deterioration may be responsible for high microbial populations. Those operations that reduce injury and preserve the physiological integrity of fresh produce are associated with low populations of microorganisms while those measures that damage or abuse the tissues are associated with high populations. Scanning electron micrographs showed that microorganisms were not present on the surface of healthy unbroken leaves of fresh-cut spinach. Large numbers of bacteria were found in areas where the cuticle was broken and could be seen infecting the internal palisade parenchyma. Most of the bacteria were reported to be in the genus Pseudomonas (Babic et al., 1996). Other workers (Seo and Frank, 1999) have found that pathogenic Escherichia coli O157:H7 accumulate within the cut edges of lettuce and are protected from chlorine wash treatments. Nguyen-the and Carlin (1994) concluded that ‘‘Some products are more likely to undergo microbial fermentation (e.g. shredded carrots, shredded butterhead lettuce), whereas others develop soft rot symptoms (e.g. chicory salads), although in many cases spoilage cannot be related to any particular microorganism’’.
4. Microbial populations and modified atmosphere packaging Another area of assumed causality and conventional wisdom is the belief that modified atmospheres suppress microbial growth and in that way extend shelf life. There is ample evidence that elevated CO2 extends the lag phase of bacterial growth and can slow the propagation of bacteria. However, much of this evidence comes from the meat and poultry literature where concentrations of 50–100% were used in experimental studies. Fruits and vegetables sustain physiological injury at much lower levels of CO2 and these high levels would be inappropriate for all but the shortest treatments. Elevated CO2 and/or reduced O2 can favor or select for certain classes of microorganisms. Low O2 is likely to favor microaerophillic microbes such as Listeria and lactic acid bacteria. Elevated
CO2 may favor gram positive over gram negative bacteria, esp. coryneforms and lactic acid bacteria (Brackett, 1987). Other workers have reported that storage in reduced O2 and elevated CO2 increased the edible shelf life of several products from 14 days to 21 days (Berrang et al., 1990). However, for asparagus and cauliflower there were only small effects on the microorganisms when compared to controls. For broccoli, there was a larger effect on the general microbial population. Again, extension of shelf life appeared to be independent of effects on microorganisms, at least for some products. Beuchat and Brackett (1990a) found that after packaging shredded lettuce in 3% O2 + 97% N2 or in air no significant differences could be found in populations of mesophilic bacteria. Packaging under modified atmosphere had no effect on survival or growth of E. coli O157:H7 on shredded lettuce or cucumber (Abdul-Raouf et al., 1993). Beuchat and Brackett (1991) concluded that ‘‘growth patterns of mesophilic aerobic microorganisms, psychrotrophic microorganisms, and yeasts and molds on whole and chopped tomatoes were essentially unaffected by chlorine and modified atmosphere packaging treatments’’. Hao and Brackett (1993) studied bell peppers inoculated with suspensions of individual decay bacteria (Erwinia, Pseudomonas, and Xanthomonas) and held in bags at 25°C either in air or in 5% O2 + 10% CO2. The MA neither enhanced nor reduced the bacterial deterioration of the bell peppers. Uninoculated control peppers deteriorated at about the same rate as inoculated peppers. Bacteria isolated from developing lesions were not those used for inoculations. Most peppers deteriorated in the peduncle area though the researchers took care not to inoculate the peduncle. Lesions were likely caused by preexisting microorganisms on the peppers or physiological changes in the peppers. Color of the peppers stored in MA did not change during the 2-week test period. Most of the peppers stored in air started to change color in one week. None of the gas mixtures tested (CO2/O2/N2: 0/5/95; 0/10/90; 5/10/85; 5/20/75; 10/5/85; 10/20/70, air) significantly affected growth of bacteria (Erwinia, Pseudomonas, and Xanthomonas) in vitro at 5, 10, and
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20°C. Incubation temperature, rather than gas composition, was the major factor controlling bacterial growth. They concluded that ‘‘Therefore, it appears that the extension of shelf life of fresh produce may be due to the physiological state of vegetables rather than by simply inhibiting microbial growth’’. For fresh-cut spinach leaves at 5°C, 0.8% O2 +10% CO2 reduced microbial growth between 10- and 100-fold, except for lactic acid bacteria and yeasts. At 10°C populations increased regardless of atmospheric composition to 10–100 times those at the lower temperature. Yeasts remained at low levels (103 – 104 CFU g − 1) during the entire storage period in air or under CA at both temperatures. Low O2, rather than high CO2, seemed to be the limiting factor on the growth of aerobic microorganisms on spinach leaves at 5°C, but not at 10°C (Babic and Watada, 1996). A great deal of work has been done on the effects of MAP on the growth of human pathogens, particularly Listeria monocytongenes, on fresh-cut produce. For example MAP conditions that were favorable for the produce quality retarded growth of spoilage microorganisms during storage at low temperature (Bennik et al., 1996). However, L. monocytogenes inoculated onto the product was not inhibited by MAP. The extent to which L. monocytogenes grew depended on its initial population, type of chicory endive and size of the population of competitive spoilage microflora. Experiments conducted for 9 days at 8°C used atmospheres of 0, 1.5, or 21% O2 combined with 0, 5, or 20% CO2 in a flow through system. In general, Pseudomonas counts were lower under 0% O2 than under 21% O2, irrespective of CO2. Pseudomonas were the predominant spoilage microflora under 21% O2, whereas Enterobacter predominated under 0% O2. Subpopulations under 1.5% O2 were similar to those under 21% O2. Epiphytic bacteria were significantly reduced by 30 and 50% CO2, but there was no effect on L. monocytogenes. Growth for all bacteria was greatly reduced at 3°C compared to 10°C, but with no differences among populations. For CO2 levels up to 20%, in vitro, growth of spoilage microorganisms, in-
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cluding P. flourescens, showed a slight reduction in the rate of growth. More substantial growth reduction occurred under 50% CO2, though final population densities were reduced by B 1 log unit as compared to growth under lower CO2 concentrations. P. 6iridifla6a was more sensitive to increased CO2 than other spoilage microorganisms (Bennik et al., 1996). It may be that under conditions that support the physiology of the host plant tissues, some reduction in microbial growth can be attributed to MAP. Under conditions of temperature abuse or physiological deterioration the reduction due to MAP is overcome by enhancement of microbial growth on the compromised tissues.
5. Wash water sanitation and microbial populations Fresh-cut processors often rely on wash water sanitizers to reduce initial bacterial populations on their products in the belief that such reductions lead to improved quality and extended shelf life. Most of the evidence does not support this. Reducing the initial microbial load on chicory by disinfection for 2 min with 10% hydrogen peroxide minimized produce spoilage. Populations were reduced by 1–2 logs compared to water rinse only. However, L. monocytogenes grew better on disinfected produce than on nondisinfected or water-rinsed produce (Bennik et al., 1996). Disinfected and non-disinfected chicory had different populations of epiphytes at day 0 but there were no differences on days 4 or 7. After post-disinfection inoculation with L. monocytogenes there were higher populations of L. monocytogenes on days 4 and 7 for disinfected compared to water washed chicory. When L. monocytogenes was inoculated onto chicory before disinfection, the numbers of L. monocytogenes and epiphytic bacteria were reduced to similar extents. During subsequent storage at 10°C, epiphytic bacteria grew rapidly on the disinfected leaves whereas L. monocytogenes survived but did not multiply. Treatment with disinfectant before contamination with L. mono-
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cytogenes occurs may increase the growth potential of the pathogen. This seems to be mainly due to the fact that disinfection diminishes the epiphytic microflora. When the pathogen is on the produce before disinfection, the treatment reduces its growth potential (Bennik et al., 1996). A survey of commercial processing lines and microbe counts on product taken after various processing steps found that chlorinated water dips only partially removed microbes from vegetables. Shredders were major sources of in-plant contamination with bacteria, with Pseudomonas spp. being the main contaminating bacteria found (Garg et al., 1990). Beuchat and Brackett (1990b) found that a chlorine wash reduced the initial population of bacteria on lettuce, but that after 4 days at 5°C no significant differences could be found in populations on chlorine washed or water washed lettuce. A 30 min soak in sodium dichloroisocyanurate (40 – 320 ppm free chlorine) reduced initial microbial load on various vegetables by 1.69 – 2.42 log compared to water washed controls. After storage for 11 days at 5°C the differences in microbial load were 0.62–0.98 log (Nicholl and Prendergast, 1998). Microbial populations increased most rapidly, and reached the highest numbers, on water cress after washing in high concentrations of chlorine, up to 1000 ppm, compared to water controls (Park and Lee, 1995). While wash water sanitizers, such as chlorine compounds, are essential to maintain clean wash water, their long term effects on microbial populations of fresh-cut vegetables are problematic. The effects of wash water sanitizers are likely to be different on populations of different target microorganisms. Epiphytic bacteria may be more accessible to chemical treatment than pathogenic bacteria that may be hidden within plant issues or protected by damaged tissues. L. monocytogenes appears to be little affected by chlorine washes and may grow faster after competing epiphytic bacteria have been partially removed. Evidence for this reinforces the importance of preventing pathogens from infesting produce before or during processing since wash water chemistry may be ineffective at reducing pathogens.
6. Postprocessing treatments in the management of microbial populations Various treatments and strategies have been evaluated to aid in the management of post-processing microbial populations. Among them, irradiation with a gamma source, such as cobalt 60, has been looked at by many workers. In the 30 years proceeding 1983 as many as 1152 published reports had addressed irradiation of fruits and vegetables (Kader and Heintz, 1983). The accumulated data suggest that irradiation may have some applications for the disinfestation of fruits and vegetables but that irradiation, alone, will not resolve most microbiological issues. Different organisms vary in their sensitivity to ionizing radiation (Table 1) and many microbes will not be killed at the maximum allowable dose of 1 kGy. Different fruits and vegetables differ in the maximum dose that they will tolerate without unacceptable softening or loss of other quality parameters. In addition, temperature at treatment, atmospheric composition during treatment and physiological state of the produce are all contributing variables making the outcome less than straight forward. For example, chlorine washed shredded carrots were irradiated at 0.5 kGy and stored at 2 and 22°C. After 9 days irradiated carrots had total plate counts of 1300 CFU g − 1 while non-irradiated carrots had mean populations of 87 000 CFU g − 1, representing : 1.5 log reduction. Oxygen and ethanol in package headspace were not sig-
Table 1 Approximate lethal doses of ionizing radiation for various organismsa Organism
Dose (kGy)
Higher animals and man Insects Gram-negative bacteria Gram-positive bacteria Bacterial spores Molds Yeasts Viruses
0.005–0.01 0.01–1.0 0.05–7.5 0.05–7.5 10–50 1.5–5 3–20 \30
a
From: Brackett, 1987.
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nificantly affected by the irradiation treatment (Hagenmaier and Baker, 1998). The 1994 review by Nguyen-the and Carlin (1994) concludes that, in general, differences in bacterial counts disinfected with chemicals disappear rapidly while lower counts achieved through irradiation persist during storage. In contrast, Kader and Gorny (1998, personnel communication) recently irradiated shredded carrots and cubed cantaloupe with 1 kGy from a gamma source. They measured total plate counts after 1 and 7 days at 10°C. There were significant reductions in bacterial populations after 1 day, up to 3.5 logs in the case of carrots. However, after 7 days bacterial populations were the same on irradiated and non-irradiated carrots and cantaloupe. Color of cantaloupe, measured as ‘L’ value, was significantly lower for irradiated cantaloupe cubes as was firmness. Another potential management strategy relies on antimicrobial substances produced by some vegetables or by selected microorganisms (Beuchat and Brackett 1990b). For example, carrots have been shown to be inhibitory to the growth of L. monocytogenes. Populations of viable L. monocytogenes decreased upon contact with whole and shredded raw carrots but not cooked carrots. Viable populations of L. monocytogenes decreased in cell suspensions in which carrots were dipped. Small populations of L. monocytogenes detected on whole carrots immediately after dipping were essentially nondetectable after 7 days of storage at 5 or 15°C. Carrots stored at 5 or 15°C spoiled before L. monocytogenes grew. Populations of mesophilic aerobes, psychrophiles, and yeasts and molds increased throughout storage at 5 and 15°C. Cutting treatment (whole or shredded), chlorine treatment (200 –260 ppm free chlorine), and MAP (3% O2 + 97% N2) had no effect on the survival or growth of L. monocytogenes or naturally occurring microflora. Populations of mesophilic aerobic microorganisms on whole carrots remained the same or increased by B 100-fold during 18 days of storage at 5°C. Much greater increases were noted for shredded carrots; populations increased 100fold within 3 days. Chlorine treatment reduced the initial population by at lest 90%, but neither
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chlorine treatment nor MA conditions substantially influenced growth patterns of mesophilic aerobes on carrots stored at 5°C. Freeze-dried spinach powder had an inhibitory effect on the growth of L. monocytogenes. The inhibitory effect was greatly decreased when the native microorganisms were almost eliminated by heating or irradiation. These results indicate that if L. monocytogenes is present as a contaminant on fresh-cut spinach, its growth probably will be restricted by native microorganisms. Pseudomonas flourescens has been shown to be an inhibitor of L. monocytogenes due to production of iron chelating siderophores (Babic et al., 1997). Red chicory, though not green chicory, appeared to be antagonistic to certain Pseudomonas bacteria as well as to the human pathogen Aeromonas hydrophylla (Guerzoni et al., 1996). Lactic acid bacteria have also been the subjects of research as possible inhibitors of gram positive pathogenic bacteria.
7. Observations and conclusions The concept that spoilage microorganisms are the primary cause of the end of shelf life, and that reducing initial microbial populations is a strategy to extend shelf life, does not appear to be supported by the available literature. Rather, the conditions that favor growth of microorganisms, such as high temperature, mechanically damaged product, overmature product, injurious levels of CO2, and time, lead to spoilage of the product as well as to the proliferation of microorganisms. If this is so, then reduction of initial micro counts will do little to extend shelf life or limit growth of microorganisms. If fruits or vegetables are handled roughly or held at abusive temperatures, it matters little if they started with 102 or 106 CFU g − 1. Conditions that injure the product are conditions that favor microbial growth and high populations of microbes will result. Irradiation dosages that cause injury to produce may initially reduce populations of bacteria and fungi, but those populations will regenerate very quickly because an appropriate substrate for growth, weakened plant tissues, is available.
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While high concentrations of CO2 are known to suppress the growth of many, though not all, bacteria and fungi, the CO2 concentrations that are effective, typically \10%, are injurious to many fruits and vegetables. Similarly, very low O2 concentrations that can suppress the growth of many spoilage bacteria can induce fermentation in plant tissues and make them more suitable for growth of other groups of bacteria. Yet appropriate modified atmosphere packaging is associated with maintenance of quality and extension of shelf life for many fresh-cut fruits and vegetables. It seems likely that these benefits are realized largely through indirect effects, such as the prevention of moisture loss due to the plastic bags, and the reduction of ethylene effects through reduced O2 and elevated CO2. Reduction of ethylene sensitivity alone can slow ripening and senescence and thus extend shelf life. Through maintaining fruits and vegetables in a less ripe condition, growth of most opportunistic microorganisms would also be expected to be retarded since they tend to grow most rapidly on aging tissues. Several direct benefits can ensue from the proper use of modified atmospheres, such as reduction of browning reactions and maintenance of firmness for some fruits. Direct reduction of microbial growth may occur for those commodities, such as strawberries, that are tolerant of 10 – 20% CO2. For many other commodities the primary benefit of MAP is maintenance of quality, which helps resist microbial growth. The expectation that wash water sanitizers are an effective kill step in produce processing is unfounded. At best, microbial populations can be reduced 1–2 log cycles. If product is then mishandled, contaminated during subsequent processing steps or temperature abused, microbial levels will go right back up to pre-wash levels or higher. Wash water sanitizers are important to prevent the wash water itself from becoming a contaminating step in the processing operation. If the water should become a reservoir for human pathogens introduced on product contaminated in the field, the wash water sanitizer should ensure that the pathogens are rapidly killed and cannot contaminate subsequent product. Similarly, irradiation at allowable dosages (up
to 1 kGy) can reduce, but not eliminate, microorganisms. If the dosage used also damages the product, again microbial levels will go right back up to pre-irradiation levels or higher. For these reasons, irradiation should be seen as a potentially useful supplement to good sanitation practices and temperature management, not as a substitute for careful handling. The widely expressed sentiment that bacteria are bad and need to be eliminated from fresh-cut produce obscures several important issues. Bacteria make up a diverse and important part of fresh-cut produce. Treatments to reduce bacterial populations that also do injury to the product are likely to be counter productive. Furthermore, viable populations of aerobic spoilage bacteria may be a hurdle to the growth of dangerous human pathogens. At the very least, the spoilage bacteria serve as a warning system that the quality and shelf life of the product have been depleted and the product should be disposed of rather than consumed. Attempting to suppress the warning system is analogous to disconnecting a smoke alarm in the belief that fire is thereby prevented. A more sensible approach would be to focus on treatments and handling steps that support the natural resistance of the product to microbial growth and thereby manage, rather than simply try to reduce, microbial populations. By focusing on the three mainstays of produce quality, ‘‘keep it cold, keep it clean, and move it fast’’, microbial populations will work in our favor rather than against us.
References Abdul-Raouf, U.M., Beuchat, L.R., Ammar, M.S., 1993. Appl. Environ. Microbiol. Survival and growth of E. coli O157:H7 on salad vegetables 59, 1999 – 2006. Babic, I., Watada, A.E., 1996. Microbial populations of freshcut spinach leaves affected by controlled atmospheres. Postharvest Biol. Technol. 9, 187 – 193. Babic, I., Roy, S., Watada, A.E., Wergin, W.P., 1996. Changes in microbial populations on fresh-cut spinach. Int. J. Food Microbiol. 31, 107 – 119. Babic, I., Watada, A.E., Buta, J.G., 1997. Growth of Listeria monocytogenes restricted by native microorganisms and other properties of fresh-cut spinach. J. Food Prot. 60 (8), 912 – 917.
D. Zagory / Posthar6est Biology and Technology 15 (1999) 313–321 Barriga, M.I., Trachy, G., Willemot, C., Simard, R.E., 1991. Microbial changes in shredded iceberg lettuce stored under controlled atmospheres. J. Food Sci. 56 (6), 1586–1599. Bennik, M.H.J., Peppelenbos, H.W., Nguyen-the, C., Carlin, F., Smid, E.J., Gorris, L.G.M., 1996. Microbiology of minimally processed, modified-atmosphere packaged chicory endive. Postharvest Biol. Technol. 9, 209–221. Berrang, M.E., Brackett, R.E., Beuchat, L.R., 1990. Microbial, color and textural qualities of fresh asparagus, broccoli and cauliflower stored under controlled atmosphere. J. Food Prot. 53, 391 – 395. Beuchat, L.R., Brackett, R.E., 1990. Survival and growth of Listeria monocytogenes on lettuce as influenced by shredding, chlorine treatment, modified atmosphere packaging and temperature. J. Food Sci. 55, 755–758. Beuchat, L.R., Brackett, R.E., 1990. Inhibitory effect of raw carrots on Listeria monocytogenes. Appl. Env. Microbiol. 56, 1734. Beuchat, L.R., Brackett, R.E., 1991. Behavior of Listeria monocytogenes inoculated into raw tomatoes and processed tomato products. Appl. Env. Microbiol. 57 (5), 1367–1371. Bolin, H.R., Stafford, A.E., King Jr., A.D., Huxsoll, C.C., 1977. Factors affecting the storage stability of shredded lettuce, J. Food Sci. 42 (5), 1319–1321. Brackett, R.E., 1987. Microbiological consequences of minimally processed fruits and vegetables. J. Food Quality 10, 195 – 206. Carlin, F., Nguyen-the, C., Cudennec, P., Reich, M., 1989. Microbiological spoilage of fresh, ready-to-use grated carrots. Sci. Alim. 9, 371–386. Carlin, F., Nguyen-the, C., Da Silva, A.A., Cochet, C., 1996. Effects of carbon dioxide on the fate of Listeria monocytogenes, of aerobic bacteria and on the development of spoilage in minimally processed fresh endive. Int. J. Food Microbiol. 32, 159 – 172.
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Effects of post-processing handling and packaging on microbial populations Devon Zagory * De6on Zagory and Associates, 759 North Campus Way, Da6is, CA 95616, USA Received 30 June 1998; accepted 11 November 1998
Abstract The type of produce, process conditions, and prior temperature management will all affect the mix of microorganisms found on fresh produce. Normally, fresh produce will be covered by a complex mix of bacteria, fungi and yeasts that are characteristic of that fruit or vegetable. For example, carrots typically have large numbers of Lactobacillus and other lactic acid bacteria while apples may have relatively large numbers of yeasts. Which of these microorganisms will come to dominate the population will be a function of the make-up of the original population on the product in the field, distribution time, distribution temperature and the atmosphere within the package. Another chief determinant of microbial populations will be the physiological condition of the product. Factors that injure or weaken the plant tissues may be expected to encourage microbial growth while conditions that maintain the physiological integrity of the tissues may be expected to discourage microbial growth. Each of these factors can be expected to affect the make-up of the microbial population in characteristic ways but always constrained by the initial condition of original population makeup. This paper describes which microorganisms are favored by given conditions in order to develop a concept of microbial management designed to favor desirable microbes at the expense of undesirable ones. Particular emphasis will be placed on the effects of modified atmospheres on microorganisms, especially human pathogens. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Fresh-cut; Bacteria; Fungi; Pathogen; Modified atmosphere; Packaging; Irradiation; Sanitation
1. Introduction
Manuscript from presentation at Beltsville Agricultural Symposium, May 3 – 6, 1998. * Corresponding author.
The subject of this paper will not be a comprehensive review of the research literature regarding microbial population dynamics on fresh produce. The literature is large and disperse and, often times, contradictory. Results have been generated
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under different experimental systems and evaluated according to different criteria and seldom make up a coherent whole. Little of the research has been incorporated into commercial practice, and that which has, has often been misunderstood and misapplied. Commercial experience has led to certain assumptions about produce microbiology. Those assumptions have led to the assignment of causality and this presumptive causality has evolved into conventional wisdom. Examples of commercial conventional wisdom include: high microbial populations result in shortened shelf-life; the lower the initial bacterial counts on produce the better the produce quality and the longer the shelf-life; modified atmospheres reduce microbial populations; the purpose of wash water sanitizing chemicals is to remove bacteria from produce; irradiation of fresh produce can remove human pathogens and ensure safety. Much of the conventional wisdom may be inaccurate and may lead to misguided or even unsafe sanitation practices. This attempt to address some of the conventional wisdom will be not as a typical hypothesis paper but rather more as an antithesis paper that will explore some research results that reflect on some of the conventional wisdom about microbial populations on fresh-cut produce as affected by processing, post processing handling and packaging.
2. Microbial populations on fresh produce The numbers and kinds of microorganisms found on fresh produce, and specifically on freshcut (minimally processed) produce, are highly variable. Mesophilic bacteria from plate count studies typically range from 103 to 109 CFU g − 1. Total counts on products after processing range from 103 to 106 CFU g − 1 (Nguyen-the and Carlin, 1994). The bacteria normally found on freshcut products are the same as those normally found on produce in the field. The microflora of vegetables and fruits is made up largely of Pseudomonas spp., Erwinia herbicola, Fla6obacterium,
Xanthomonas, and Enterobacter agglomerans as well as various molds. Lactic acid bacteria, such as Leuconostoc mesenteroides and Lactobacillus spp., are also commonly found, as are several species of yeasts (primarily on fruits). Pseudomonas normally dominates and may make up 50–90% of the microbial population on many vegetables (Zagory and Hurst, 1996). Typically these microorganisms are not harmful to humans. In fact many different genera of microorganisms can be found on fresh produce and what is found largely reflects the conditions and media used for isolation. Many of the most common media and growth conditions select for mesophillic bacteria that grow rapidly at temperatures of 25–35°C. Other common media select for coliform or fecal coliform bacteria that also grow well at higher temperatures. Few studies have directly assayed for the psychrotrophic microbes that would be expected to dominate at the refrigeration temperatures recommended for fresh-cut produce. For this reason, our views of microbial population dynamics on fresh-cut produce may be incomplete and imprecise.
3. Microbial populations and shelf life Many of the concepts regarding the microbiology of fresh produce have come from concerns with spoilage microorganisms, plant pathogens and extension of shelf life. The correlation of development of large populations of microorganisms with the end of shelf life has led to the assignment of causality, that is, that proliferation of microorganisms is a primary cause of the end of shelf life. This assignment of causality has led to strategies to reduce total bacterial counts as a way to maintain quality and extend shelf life. However, a weight of published research does not support this view. In many cases total bacterial numbers bear little or no relationship to product quality or to shelf life. In Fig. 1, spoilage is associated with injurious levels of carbon dioxide, but not with populations of aerobic bacteria. Total numbers of psychrotrophic microorganisms of 106 or 107 have been associated with high visual quality ratings (Barriga et al., 1991). Again,
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Fig. 1. Effects of CO2 + 10% O on spoilage and populations of aerobic bacteria of cut endive at 3C. Data received from: Carlin et al., 1996.
there was very little correlation between bacterial populations and product quality. Deterioration of cabbage in coleslaw was similar at 7 and 14°C, but microbial growth was much greater at the higher temperature (King et al., 1976). Spoilage of fresh-cut kiwifruit, papaya, and pineapple stored at 4°C was not a consequence of microbial growth (O’Connor-Shaw et al., 1994). Many other published studies report a similar lack of linkage between spoilage and bacterial populations. Of course, in some instances, specific bacteria or plant pathogenic fungi may be associated with particular forms of spoilage. Pectinolytic bacteria and fungi may lead to breakdown of tissues and subsequent spoilage. In addition, lactic acid bacteria may be associated with spoilage of specific commodities, such as carrots. Spoilage of shredded carrots after 14 days at 10°C was always associated with large populations of L. mesenteroides, though not with mesophilic bacterial populations (Carlin et al., 1989). However, even in these instances, there is little evidence for causality. Pectinolytic plant pathogens tend to be opportunistic and will only effectively invade through wounded or senescent tissues. A temperature of 10°C is well above the optimal for carrots and can be considered an abusive temperature.
If bacterial populations are not directly associated with quality or shelf life in a causal way, with what do they have a causal relationship? The available evidence suggests that microbial growth and populations depend primarily upon the morphological and physiological condition of the plant tissues. Intact, healthy tissues may be expected to be a poor substrate for growth of opportunistic microorganisms. Damaged, physiologically compromised tissues would deteriorate faster and provide a better substrate for microbial growth. The conclusions from a study by Bolin et al. (1977) describe some of the factors that have a significant effect on quality and shelf life of freshcut produce: marketable quality was retained 2.5 times longer at 2°C than at 10°C. Temperature is a controlling factor for shelf life and quality; a sharp blade slicing was superior to either a sharp blade chopping or a dull blade slicing or chopping; smaller shred size reduced storage life. Physical damage of the shredded lettuce reduced its storage life; presence of free moisture or cellular fluids on the lettuce surface reduced storage life. It appears that rather than high microbial populations being responsible for deterioration of
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fresh produce, deterioration may be responsible for high microbial populations. Those operations that reduce injury and preserve the physiological integrity of fresh produce are associated with low populations of microorganisms while those measures that damage or abuse the tissues are associated with high populations. Scanning electron micrographs showed that microorganisms were not present on the surface of healthy unbroken leaves of fresh-cut spinach. Large numbers of bacteria were found in areas where the cuticle was broken and could be seen infecting the internal palisade parenchyma. Most of the bacteria were reported to be in the genus Pseudomonas (Babic et al., 1996). Other workers (Seo and Frank, 1999) have found that pathogenic Escherichia coli O157:H7 accumulate within the cut edges of lettuce and are protected from chlorine wash treatments. Nguyen-the and Carlin (1994) concluded that ‘‘Some products are more likely to undergo microbial fermentation (e.g. shredded carrots, shredded butterhead lettuce), whereas others develop soft rot symptoms (e.g. chicory salads), although in many cases spoilage cannot be related to any particular microorganism’’.
4. Microbial populations and modified atmosphere packaging Another area of assumed causality and conventional wisdom is the belief that modified atmospheres suppress microbial growth and in that way extend shelf life. There is ample evidence that elevated CO2 extends the lag phase of bacterial growth and can slow the propagation of bacteria. However, much of this evidence comes from the meat and poultry literature where concentrations of 50–100% were used in experimental studies. Fruits and vegetables sustain physiological injury at much lower levels of CO2 and these high levels would be inappropriate for all but the shortest treatments. Elevated CO2 and/or reduced O2 can favor or select for certain classes of microorganisms. Low O2 is likely to favor microaerophillic microbes such as Listeria and lactic acid bacteria. Elevated
CO2 may favor gram positive over gram negative bacteria, esp. coryneforms and lactic acid bacteria (Brackett, 1987). Other workers have reported that storage in reduced O2 and elevated CO2 increased the edible shelf life of several products from 14 days to 21 days (Berrang et al., 1990). However, for asparagus and cauliflower there were only small effects on the microorganisms when compared to controls. For broccoli, there was a larger effect on the general microbial population. Again, extension of shelf life appeared to be independent of effects on microorganisms, at least for some products. Beuchat and Brackett (1990a) found that after packaging shredded lettuce in 3% O2 + 97% N2 or in air no significant differences could be found in populations of mesophilic bacteria. Packaging under modified atmosphere had no effect on survival or growth of E. coli O157:H7 on shredded lettuce or cucumber (Abdul-Raouf et al., 1993). Beuchat and Brackett (1991) concluded that ‘‘growth patterns of mesophilic aerobic microorganisms, psychrotrophic microorganisms, and yeasts and molds on whole and chopped tomatoes were essentially unaffected by chlorine and modified atmosphere packaging treatments’’. Hao and Brackett (1993) studied bell peppers inoculated with suspensions of individual decay bacteria (Erwinia, Pseudomonas, and Xanthomonas) and held in bags at 25°C either in air or in 5% O2 + 10% CO2. The MA neither enhanced nor reduced the bacterial deterioration of the bell peppers. Uninoculated control peppers deteriorated at about the same rate as inoculated peppers. Bacteria isolated from developing lesions were not those used for inoculations. Most peppers deteriorated in the peduncle area though the researchers took care not to inoculate the peduncle. Lesions were likely caused by preexisting microorganisms on the peppers or physiological changes in the peppers. Color of the peppers stored in MA did not change during the 2-week test period. Most of the peppers stored in air started to change color in one week. None of the gas mixtures tested (CO2/O2/N2: 0/5/95; 0/10/90; 5/10/85; 5/20/75; 10/5/85; 10/20/70, air) significantly affected growth of bacteria (Erwinia, Pseudomonas, and Xanthomonas) in vitro at 5, 10, and
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20°C. Incubation temperature, rather than gas composition, was the major factor controlling bacterial growth. They concluded that ‘‘Therefore, it appears that the extension of shelf life of fresh produce may be due to the physiological state of vegetables rather than by simply inhibiting microbial growth’’. For fresh-cut spinach leaves at 5°C, 0.8% O2 +10% CO2 reduced microbial growth between 10- and 100-fold, except for lactic acid bacteria and yeasts. At 10°C populations increased regardless of atmospheric composition to 10–100 times those at the lower temperature. Yeasts remained at low levels (103 – 104 CFU g − 1) during the entire storage period in air or under CA at both temperatures. Low O2, rather than high CO2, seemed to be the limiting factor on the growth of aerobic microorganisms on spinach leaves at 5°C, but not at 10°C (Babic and Watada, 1996). A great deal of work has been done on the effects of MAP on the growth of human pathogens, particularly Listeria monocytongenes, on fresh-cut produce. For example MAP conditions that were favorable for the produce quality retarded growth of spoilage microorganisms during storage at low temperature (Bennik et al., 1996). However, L. monocytogenes inoculated onto the product was not inhibited by MAP. The extent to which L. monocytogenes grew depended on its initial population, type of chicory endive and size of the population of competitive spoilage microflora. Experiments conducted for 9 days at 8°C used atmospheres of 0, 1.5, or 21% O2 combined with 0, 5, or 20% CO2 in a flow through system. In general, Pseudomonas counts were lower under 0% O2 than under 21% O2, irrespective of CO2. Pseudomonas were the predominant spoilage microflora under 21% O2, whereas Enterobacter predominated under 0% O2. Subpopulations under 1.5% O2 were similar to those under 21% O2. Epiphytic bacteria were significantly reduced by 30 and 50% CO2, but there was no effect on L. monocytogenes. Growth for all bacteria was greatly reduced at 3°C compared to 10°C, but with no differences among populations. For CO2 levels up to 20%, in vitro, growth of spoilage microorganisms, in-
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cluding P. flourescens, showed a slight reduction in the rate of growth. More substantial growth reduction occurred under 50% CO2, though final population densities were reduced by B 1 log unit as compared to growth under lower CO2 concentrations. P. 6iridifla6a was more sensitive to increased CO2 than other spoilage microorganisms (Bennik et al., 1996). It may be that under conditions that support the physiology of the host plant tissues, some reduction in microbial growth can be attributed to MAP. Under conditions of temperature abuse or physiological deterioration the reduction due to MAP is overcome by enhancement of microbial growth on the compromised tissues.
5. Wash water sanitation and microbial populations Fresh-cut processors often rely on wash water sanitizers to reduce initial bacterial populations on their products in the belief that such reductions lead to improved quality and extended shelf life. Most of the evidence does not support this. Reducing the initial microbial load on chicory by disinfection for 2 min with 10% hydrogen peroxide minimized produce spoilage. Populations were reduced by 1–2 logs compared to water rinse only. However, L. monocytogenes grew better on disinfected produce than on nondisinfected or water-rinsed produce (Bennik et al., 1996). Disinfected and non-disinfected chicory had different populations of epiphytes at day 0 but there were no differences on days 4 or 7. After post-disinfection inoculation with L. monocytogenes there were higher populations of L. monocytogenes on days 4 and 7 for disinfected compared to water washed chicory. When L. monocytogenes was inoculated onto chicory before disinfection, the numbers of L. monocytogenes and epiphytic bacteria were reduced to similar extents. During subsequent storage at 10°C, epiphytic bacteria grew rapidly on the disinfected leaves whereas L. monocytogenes survived but did not multiply. Treatment with disinfectant before contamination with L. mono-
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cytogenes occurs may increase the growth potential of the pathogen. This seems to be mainly due to the fact that disinfection diminishes the epiphytic microflora. When the pathogen is on the produce before disinfection, the treatment reduces its growth potential (Bennik et al., 1996). A survey of commercial processing lines and microbe counts on product taken after various processing steps found that chlorinated water dips only partially removed microbes from vegetables. Shredders were major sources of in-plant contamination with bacteria, with Pseudomonas spp. being the main contaminating bacteria found (Garg et al., 1990). Beuchat and Brackett (1990b) found that a chlorine wash reduced the initial population of bacteria on lettuce, but that after 4 days at 5°C no significant differences could be found in populations on chlorine washed or water washed lettuce. A 30 min soak in sodium dichloroisocyanurate (40 – 320 ppm free chlorine) reduced initial microbial load on various vegetables by 1.69 – 2.42 log compared to water washed controls. After storage for 11 days at 5°C the differences in microbial load were 0.62–0.98 log (Nicholl and Prendergast, 1998). Microbial populations increased most rapidly, and reached the highest numbers, on water cress after washing in high concentrations of chlorine, up to 1000 ppm, compared to water controls (Park and Lee, 1995). While wash water sanitizers, such as chlorine compounds, are essential to maintain clean wash water, their long term effects on microbial populations of fresh-cut vegetables are problematic. The effects of wash water sanitizers are likely to be different on populations of different target microorganisms. Epiphytic bacteria may be more accessible to chemical treatment than pathogenic bacteria that may be hidden within plant issues or protected by damaged tissues. L. monocytogenes appears to be little affected by chlorine washes and may grow faster after competing epiphytic bacteria have been partially removed. Evidence for this reinforces the importance of preventing pathogens from infesting produce before or during processing since wash water chemistry may be ineffective at reducing pathogens.
6. Postprocessing treatments in the management of microbial populations Various treatments and strategies have been evaluated to aid in the management of post-processing microbial populations. Among them, irradiation with a gamma source, such as cobalt 60, has been looked at by many workers. In the 30 years proceeding 1983 as many as 1152 published reports had addressed irradiation of fruits and vegetables (Kader and Heintz, 1983). The accumulated data suggest that irradiation may have some applications for the disinfestation of fruits and vegetables but that irradiation, alone, will not resolve most microbiological issues. Different organisms vary in their sensitivity to ionizing radiation (Table 1) and many microbes will not be killed at the maximum allowable dose of 1 kGy. Different fruits and vegetables differ in the maximum dose that they will tolerate without unacceptable softening or loss of other quality parameters. In addition, temperature at treatment, atmospheric composition during treatment and physiological state of the produce are all contributing variables making the outcome less than straight forward. For example, chlorine washed shredded carrots were irradiated at 0.5 kGy and stored at 2 and 22°C. After 9 days irradiated carrots had total plate counts of 1300 CFU g − 1 while non-irradiated carrots had mean populations of 87 000 CFU g − 1, representing : 1.5 log reduction. Oxygen and ethanol in package headspace were not sig-
Table 1 Approximate lethal doses of ionizing radiation for various organismsa Organism
Dose (kGy)
Higher animals and man Insects Gram-negative bacteria Gram-positive bacteria Bacterial spores Molds Yeasts Viruses
0.005–0.01 0.01–1.0 0.05–7.5 0.05–7.5 10–50 1.5–5 3–20 \30
a
From: Brackett, 1987.
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nificantly affected by the irradiation treatment (Hagenmaier and Baker, 1998). The 1994 review by Nguyen-the and Carlin (1994) concludes that, in general, differences in bacterial counts disinfected with chemicals disappear rapidly while lower counts achieved through irradiation persist during storage. In contrast, Kader and Gorny (1998, personnel communication) recently irradiated shredded carrots and cubed cantaloupe with 1 kGy from a gamma source. They measured total plate counts after 1 and 7 days at 10°C. There were significant reductions in bacterial populations after 1 day, up to 3.5 logs in the case of carrots. However, after 7 days bacterial populations were the same on irradiated and non-irradiated carrots and cantaloupe. Color of cantaloupe, measured as ‘L’ value, was significantly lower for irradiated cantaloupe cubes as was firmness. Another potential management strategy relies on antimicrobial substances produced by some vegetables or by selected microorganisms (Beuchat and Brackett 1990b). For example, carrots have been shown to be inhibitory to the growth of L. monocytogenes. Populations of viable L. monocytogenes decreased upon contact with whole and shredded raw carrots but not cooked carrots. Viable populations of L. monocytogenes decreased in cell suspensions in which carrots were dipped. Small populations of L. monocytogenes detected on whole carrots immediately after dipping were essentially nondetectable after 7 days of storage at 5 or 15°C. Carrots stored at 5 or 15°C spoiled before L. monocytogenes grew. Populations of mesophilic aerobes, psychrophiles, and yeasts and molds increased throughout storage at 5 and 15°C. Cutting treatment (whole or shredded), chlorine treatment (200 –260 ppm free chlorine), and MAP (3% O2 + 97% N2) had no effect on the survival or growth of L. monocytogenes or naturally occurring microflora. Populations of mesophilic aerobic microorganisms on whole carrots remained the same or increased by B 100-fold during 18 days of storage at 5°C. Much greater increases were noted for shredded carrots; populations increased 100fold within 3 days. Chlorine treatment reduced the initial population by at lest 90%, but neither
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chlorine treatment nor MA conditions substantially influenced growth patterns of mesophilic aerobes on carrots stored at 5°C. Freeze-dried spinach powder had an inhibitory effect on the growth of L. monocytogenes. The inhibitory effect was greatly decreased when the native microorganisms were almost eliminated by heating or irradiation. These results indicate that if L. monocytogenes is present as a contaminant on fresh-cut spinach, its growth probably will be restricted by native microorganisms. Pseudomonas flourescens has been shown to be an inhibitor of L. monocytogenes due to production of iron chelating siderophores (Babic et al., 1997). Red chicory, though not green chicory, appeared to be antagonistic to certain Pseudomonas bacteria as well as to the human pathogen Aeromonas hydrophylla (Guerzoni et al., 1996). Lactic acid bacteria have also been the subjects of research as possible inhibitors of gram positive pathogenic bacteria.
7. Observations and conclusions The concept that spoilage microorganisms are the primary cause of the end of shelf life, and that reducing initial microbial populations is a strategy to extend shelf life, does not appear to be supported by the available literature. Rather, the conditions that favor growth of microorganisms, such as high temperature, mechanically damaged product, overmature product, injurious levels of CO2, and time, lead to spoilage of the product as well as to the proliferation of microorganisms. If this is so, then reduction of initial micro counts will do little to extend shelf life or limit growth of microorganisms. If fruits or vegetables are handled roughly or held at abusive temperatures, it matters little if they started with 102 or 106 CFU g − 1. Conditions that injure the product are conditions that favor microbial growth and high populations of microbes will result. Irradiation dosages that cause injury to produce may initially reduce populations of bacteria and fungi, but those populations will regenerate very quickly because an appropriate substrate for growth, weakened plant tissues, is available.
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While high concentrations of CO2 are known to suppress the growth of many, though not all, bacteria and fungi, the CO2 concentrations that are effective, typically \10%, are injurious to many fruits and vegetables. Similarly, very low O2 concentrations that can suppress the growth of many spoilage bacteria can induce fermentation in plant tissues and make them more suitable for growth of other groups of bacteria. Yet appropriate modified atmosphere packaging is associated with maintenance of quality and extension of shelf life for many fresh-cut fruits and vegetables. It seems likely that these benefits are realized largely through indirect effects, such as the prevention of moisture loss due to the plastic bags, and the reduction of ethylene effects through reduced O2 and elevated CO2. Reduction of ethylene sensitivity alone can slow ripening and senescence and thus extend shelf life. Through maintaining fruits and vegetables in a less ripe condition, growth of most opportunistic microorganisms would also be expected to be retarded since they tend to grow most rapidly on aging tissues. Several direct benefits can ensue from the proper use of modified atmospheres, such as reduction of browning reactions and maintenance of firmness for some fruits. Direct reduction of microbial growth may occur for those commodities, such as strawberries, that are tolerant of 10 – 20% CO2. For many other commodities the primary benefit of MAP is maintenance of quality, which helps resist microbial growth. The expectation that wash water sanitizers are an effective kill step in produce processing is unfounded. At best, microbial populations can be reduced 1–2 log cycles. If product is then mishandled, contaminated during subsequent processing steps or temperature abused, microbial levels will go right back up to pre-wash levels or higher. Wash water sanitizers are important to prevent the wash water itself from becoming a contaminating step in the processing operation. If the water should become a reservoir for human pathogens introduced on product contaminated in the field, the wash water sanitizer should ensure that the pathogens are rapidly killed and cannot contaminate subsequent product. Similarly, irradiation at allowable dosages (up
to 1 kGy) can reduce, but not eliminate, microorganisms. If the dosage used also damages the product, again microbial levels will go right back up to pre-irradiation levels or higher. For these reasons, irradiation should be seen as a potentially useful supplement to good sanitation practices and temperature management, not as a substitute for careful handling. The widely expressed sentiment that bacteria are bad and need to be eliminated from fresh-cut produce obscures several important issues. Bacteria make up a diverse and important part of fresh-cut produce. Treatments to reduce bacterial populations that also do injury to the product are likely to be counter productive. Furthermore, viable populations of aerobic spoilage bacteria may be a hurdle to the growth of dangerous human pathogens. At the very least, the spoilage bacteria serve as a warning system that the quality and shelf life of the product have been depleted and the product should be disposed of rather than consumed. Attempting to suppress the warning system is analogous to disconnecting a smoke alarm in the belief that fire is thereby prevented. A more sensible approach would be to focus on treatments and handling steps that support the natural resistance of the product to microbial growth and thereby manage, rather than simply try to reduce, microbial populations. By focusing on the three mainstays of produce quality, ‘‘keep it cold, keep it clean, and move it fast’’, microbial populations will work in our favor rather than against us.
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