Implications And Control

Many of the examples of the internalization of microorganisms by fruits and vegetables cited above involve situations occurring during crop production or harvest that cannot be controlled. Many internalization hazards can be controlled. The results of internalization can range from poor shelf life due to decay to unwholesomeness due to contamination by hazardous microorganisms. The list of human pathogens that can be internalized by fruits and vegetables is extensive [4]. For crops intended for consumption as raw products, such contamination is, at present, irreversible. With the globalization of agriculture and the consumer demand for fresh crop items all year round [61], there are nearly endless opportunities for microorganisms originating in the fields and surface waters of underdeveloped countries to end up in salad or fresh fruit items served in homes and restaurants in developed countries.

The inability of even the strongest surface disinfectants to eradicate completely human pathogens from contaminated fresh fruits and vegetables and yet be compatible with a product appearance that meets marketing requirements is well documented [4]. The failure of chlorinated water treatments, even at concentrations exceeding 5000 ppm, to eradicate plant pathogens from inoculated wounds has been known since 1945 [62]. Much conjecture has been focused on the inability of chlorine, a strong oxidizer, to disinfect contaminated wounds. Often authors suggest that active chlorine reacts with wounded tissues such that pathogen structures are not exposed to a critical dose. However, with contaminated wounds on tomato fruit, increasing doses and mechanical scrubbing of the wound surface have not led to significant increases in efficacy [63]. With contaminated cantaloupes, however, Ukuku and Fett [64] observed an increase in efficacy of 200 ppm chlorine (pH 6.4) or 5% H2O2 if the fruits were rubbed during the 2-minute immersion treatment, although not all contamination was eradicated. Based on Johnson's [43] theories on capillary movement of suspensions into leaf tissues and observations on dye movement and suspensions of soft rot bacteria into wounds on tomato fruit, Bartz et al. [50] suggested that solutions of active chlorine applied to inoculated wound surfaces on tomatoes displaced the pathogen cells further into the underlying intercellular spaces.

Internalization risks can be minimized through use of HACCP-type (hazard analysis critical control point) analyses and practices in production systems [65]. The ultimate goals of such a program are to minimize water penetration of plant tissues, crop contact with hazardous microorganisms, open wounds on plant surfaces, and situations likely to cause fluid penetration of plant surface apertures. Particularly, crops intended for raw consumption should never be treated, irrigated, washed, or cooled with poor-quality water [66]. Improperly composted manures should never be used in fields intended for production of fresh fruits and vegetables. In a recent survey of fruit and vegetable producers in Minnesota, one grower spread untreated manure throughout the growing season and 90% of the fruit and vegetable samples from that farm were positive for E. coli [67]. Fields should be fenced to keep out domestic or wild animals and should be located at least 5 miles from the nearest feed lots or other concentrations of animals [65]. Field workers should not be allowed to work with or harvest a crop if they are ill or have recently been ill. Working with water-congested plants creates a special hazard and should be avoided. Cultivars selected for production should resist the development of growth cracks or other characteristics that enable penetration by microorganisms.

Certain handling steps after harvest can reduce the internalization hazard. For example, the porosity of tomato stem scars to water is greatest immediately after harvest and then decreases over time [32]. Leaving a stem attached until just before water treatment only slightly reduces this characteristic. Studer and Kader [51] observed that tomato fruits split readily (from water uptake) if they were submerged in water immediately after harvest but did not if stored overnight before treatment. Additionally, warm fruit is more likely to absorb water than cool fruit during exposure to hydrostatic pressure as well as during exposure to water cooler than the fruit [30,31,51]. Thus, allowing tomatoes to cool overnight before packing them should decrease the likelihood of water infiltration during the unloading and washing processes at packinghouses. Although this prepacking storage would allow pathogen growth on damaged fruit (which otherwise would have been culled), small wounds would begin to heal and the stem scar would dry, thereby reducing the number of water channels. Additionally, the loss of a small amount of water from each fruit should decrease the likelihood for handling injuries to the tomato surface. With citrus, Eckert [62] noted that a standard practice in California was to "wilt" the fruit before washing and packing to reduce susceptibility to surface injuries.

The water used to handle or wash fruits and vegetables must be continually sanitized during the workday, particularly if the water is recycled. Moreover, the sanitizer must be present where the unwashed product enters the water system to minimize the chances for an internalization of hazardous microorganisms at the initial contact point. Highly reactive chemicals such as ozone [68] may be too unstable for maintenance of adequate residuals. Currently, hypochlorous acid from solutions of sodium hypochlorite, liquefied elemental chlorine, or solid powder or pellets of calcium hypochlorite best combines efficacy, speed of action, and stability for minimizing internalization hazards at packinghouses. Moreover, residues from the chlorinated water treatment either quickly dissipate from treated products or are harmless salts. Unfortunately, water chlorination cannot make badly contaminated surface waters safe to use for handling and washing produce as it is not effective against the resting stages (cysts, oocysts) of certain human parasites [68]. Additionally, where high chlorine demand exists, such as with shredded vegetables or with certain root crops, maintenance of adequate residuals is difficult.

Whether water chlorination eliminates the need to suppress completely water infiltration during postharvest handling is unclear. The infiltration of tomatoes with chlorinated water failed to prevent the development of postharvest decay when submerged fruits were treated with hydrostatic pressure at room temperature [69], but did prevent such decays when fruits were hydrocooled [34]. The presence of chlorine in the water appeared to increase the porosity of tomato stem scars [69]. The chlorination of the water used to hydrocool strawberries led to a significant reduction in botrytis fruit rot [52]. As noted above, however, chlorinated water treatments have consistently failed to eradicate completely microorganisms from fruit or vegetables likely to have internalized a portion of the contamination. For example, the washing of contaminated wounds on tomato fruit with over 500 ppm free chlorine at pH 7.0 reduced the subsequent development of soft rot by 50% in one test and had no effect in two [70]. In two separate reports on tomatoes that had been contaminated in the laboratory, washing wounds or stem scars with 100 ppm or more of free chlorine failed to eliminate Salmonella Montevideo [71,72].

When fruits or vegetables are unloaded into or washed by water, infiltration of natural apertures due to a temperature related pressure differential may be controlled by maintaining water temperatures above those of the incoming fruits and vegetables [30]. Current recommendations for water handling steps with tomato fruit are to keep water temperatures about 5°C (10°F) above those of incoming fruit and to limit fruit contact with water to 2 minutes [73]. This handling recommendation also includes provision for maintaining 100 to 150 ppm free chlorine in the water. The pH of chlorinated water should be in the range of pH 6.5 to 7.5 to ensure ample concentrations of the killing agent, HOCl, and minimal corrosion [65]. Warming the water increases chlorine's efficacy and decreases its stability [68]. In cooler weather, use of warm water to handle tomatoes has been associated with a reduction of surface injuries [74].

Selection of crop cultivars may also help reduce internalization hazards. The relative tendency of a tomato stem scar to absorb water appears to be a varietal characteristic [75]. Certain varieties consistently absorbed more water than others over different harvests of the same crop or the same cultivars in different fields and seasons. Heggestad [76] reported that leaves of certain tobacco cultivars were less likely to develop water congestion than others. In naturally occurring outbreaks of wildfire disease, lines that were less prone to water congestion had less disease. McLean and Lee [48] noted that structural differences in stomata were responsible for the resistance of mandarin orange to a bacterial disease, citrus canker. Therefore, the tendency of plant tissues to resist water intrusion and microbial internalization might be enhanced by selection and breeding.

Encouraging tissue respiration has been suggested as an internali-zation reduction treatment during preparation of fresh-cut lettuce. Takeuchi and Frank [77] reported that a high respiration rate in minimally processed lettuce produced a "counterforce" that reduced the internalization of cells of

E. coli. Thus, warming lettuce to encourage respiration during sensitive stages of fresh-cut lettuce preparation might decrease the potential for internalization of bacteria from wash water. Subsequently, a group of authors noted that reducing the O2 over the lettuce to 2.7% reduced the internalization associated with low-temperature incubation [78]. Ostensibly, the counterforce was CO2 released from respiration. The methodology used in these reports, however, raised questions about the validity of the authors' conclusions [79]. The lettuce was purchased from local stores and stored at 4°C. Tissue sections were prepared and submerged in water or an aqueous cell suspension of E. coli for 24 hours at 4, 10, 22, or 37°C [77,78]. The authors did not indicate if the tissues and fluids were equilibrated to these temperatures prior to the incubation. In fact, Takeuchi et al. [78] commented in their discussion that "... subsequent infiltration of the bacteria into the lettuce as it cooled during the inoculation period.'' If the lettuce tissues cooled during the incubation, then a pressure differential would occur in the intercellular spaces, as discussed in Section 3.6.4. This would lead to an infiltration of the bacterial suspension into the cut edges. Conversely, if the tissue sections warmed, internal gases would expand and tend to prevent infiltration. Without knowledge of tissue and fluid temperatures at the beginning of the test, it is impossible to interpret the results. Additionally, the relatively high cold-water solubility of CO2 as compared with O2 may be involved. Due to respiration, O2 in intercellular spaces would be absorbed by the lettuce cells. If CO2 production matches O2 absorption, gas pressures in the intercellular spaces should not change. However, at low temperatures, a significant portion of the CO2 released by mitochondria is likely to remain dissolved in cell sap. As such, the uptake of O2 could contribute to a reduction in internal gas pressure. (Note that this would be much like the standard laboratory exercise on measuring plant tissue respiration with a Warburg apparatus where the CO2 produced is scrubbed by an alkali solution and oxygen uptake is measured with a manometer.) In the absence of significant respiration, changes in the partial pressures of O2 and CO2 should not be factors in pressure differentials developing within the tissues.

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