Chapter IV. Outbreaks Associated with Fresh and Fresh-Cut Produce. Incidence, Growth, and Survival of Pathogens in Fresh and Fresh-Cut Produce
Analysis and Evaluation of Preventive Control Measures for the Control and Reduction/Elimination of Microbial Hazards on Fresh and Fresh-Cut Produce
An important consideration when addressing safety issues is the incidence of pathogens and outbreaks associated with particular food products. This chapter addresses outbreaks that have been associated with the consumption of fresh and fresh-cut produce. In addition, studies that investigate the incidence of pathogens and factors contributing to the survival and growth of pathogens are reviewed. Although they may not be exhaustive, the tables at the end of the chapter include highlights of incidence studies from industry and published literature sources (Tables I1-I7), outbreaks (Tables O1-O10), and growth/survival studies related to fresh produce (Tables G/S1-G/S8).
1. Foodborne pathogens associated with fresh produce
The minimum processing required for fresh and fresh-cut produce, which omits any effective microbial elimination step, results in food products that naturally would carry microorganisms, some of which may be potentially hazardous to human health. When investigating possible control methods, a vital step is to examine the nature of the human pathogenic microorganisms present in produce throughout the production process. However, incidence studies are time-consuming and expensive. For this reason, sample sizes are often too small to be of statistical relevance, especially if the probability of detection is low. Most researchers do not collect sufficient information regarding the source of the sample other than perhaps the country of origin or sample location (for example, retail outlets, farmers' markets). There has been little consistency in sample collection, treatment, laboratory test methods, or data analysis. Controls are often missing and techniques for isolating pathogens from produce items are often not optimized. In many cases, identification of the pathogen has not been verified. Most published articles stress the detection of pathogens in incidence surveys; negative data may not be reported or their significance is minimized. However, these negative data are important in evaluating the risks associated with consumption of fresh fruits and vegetables and should be considered in risk assessments. Table IV-1 outlines some of the factors that should be considered when designing a study to determine the frequency of isolation of pathogens from produce.
Because of the extremely large number of variables that might influence contamination of raw fruits or vegetables, it is difficult to design well-controlled experiments that would address risk factors for contamination. While incidence studies can provide a snapshot assessment of contamination at a particular location on a particular produce item at a particular time of year, they rarely provide information on the source of contamination. For these reasons, caution must be used when interpreting data from these types of studies, and overly broad conclusions should be avoided. Nevertheless, numerous pathogenic microorganisms have been isolated from a wide variety of fresh fruits and vegetables, sometimes at relatively high frequencies (Table I1-I7). Not all of the microorganisms listed in these tables have been linked to produce-associated illnesses. Under the right conditions, however, all of these microorganisms have the potential to cause produce-associated illness. Isolation rates are not consistent. Percentage of samples contaminated ranges from 0 to greater than 50%, depending upon the target pathogen and produce item. Data provided by Wells and Butterfield (1997) indicate that Salmonella is more readily isolated from decaying fruits and vegetables. Whether this applies to other pathogens is not known.
Table IV-1. Considerations when examining raw fruits and vegetables for the presence and populations of pathogenic microorganisms
Procedure for sampling
Location of source (field, packing shed, processing plant, retail location, food service, home)
Number and size of samples
Distribution of samples in test lot
Protection of samples for transport to laboratory
Handling samples between collection and analysis
Protection against cross-contamination
Temperature between selection and analysis of sample
Time between selection and analysis of samples
Weight or number of pieces to represent samples
Area or portion to be tested (whole piece, skin only, diced, cut)
Selection of wash fluid or diluent
Ratio of produce to wash fluid or diluent
Temperature of produce and wash fluid or diluent
Soaked or not soaked before processing
Type of processing (washing, rubbing, stomaching, homogenizing, macerating, blending)
Time of processing
Enrichment and/or direct plating
Composition and volume of enrichment broth
Composition of direct plating medium
Pour-plate or surface plate
Incubation temperature and time
2. Outbreaks of foodborne illness associated with the consumption of raw fruits and vegetables
The number of foodborne illness outbreaks linked to fresh produce and reported to the United States Centers for Disease Control and Prevention (CDC) has increased in the last years (Bean and Griffin 1990; CDC 1990; CDC 2000). Some of this increase is due to improved surveillance, but other factors may also come into play. A number of reasons have been proposed for this increased association of foodborne illness with fresh produce. Since the early 1970's, a significant increase in the consumption of fresh produce has been observed in the United States, presumably due, in part, to active promotion of fruits and vegetables as an important part of a healthy diet. From 1982 to 1997, per capita consumption of fresh fruits and vegetables increased from 91.6 to 121.1 kg, an increase of 32% (Table IV-2). If contamination levels were consistent, increased consumption of these foods should be expected to lead to greater numbers of illnesses over this time. During this same period, there has been a trend toward greater consumption of foods not prepared in the home and an increase in the popularity of salad bars (buffets). Greater volumes of intact and chopped, sliced or prepared fruits and vegetables are being shipped from central locations and distributed over much larger geographical areas to many more people (see Chapter I). This, coupled with increased global trade, potentially increases human exposure to a wide variety of foodborne pathogens and also increases the chances that an outbreak will be detected. Reasons for increases in foodborne illness in the summertime are not fully understood, although abusive temperatures and a higher consumption of fresh produce during the summer months are likely to play a role.
Table IV-2. Per capita (kg) consumption of raw fruits and vegetables in the US. Source: Fruit and Tree Nut Situation and Outlook Report (USDA 1999).
The perishability of produce and a complex distribution system have made it difficult to effectively investigate many produce-related outbreaks. Trace-back has been particularly difficult because of the complexity of the distribution system and the practice of co-mingling produce in packing houses. Epidemiological investigations often take weeks before detecting a link between reported illnesses and a produce item. As a result, there is little or no product available for testing. However, improvements in outbreak investigations and pathogen detection methods have contributed to an increase in documentation of produce-borne illnesses.
Foodborne illness resulting from the consumption of any food is dependent upon a number of factors. The produce must first be contaminated with a pathogen and the pathogen must survive until the time of consumption at levels sufficient to cause illness. The infective dose (minimum numbers of organisms necessary to cause illness) is very low in many cases (Table IV-3), which means that the microorganism needs only to contaminate the food to survive without reproducing. For example, pathogenic parasites and viruses are unable to multiply outside of a human or animal host and only need to survive in sufficient numbers to cause illness.
Table IV-3. Characteristics of some microbial pathogens that have been linked to outbreaks of produce-associated illness.
|Microorganism||Typical Incubation Period||Symptoms||Infectious Dose (Number of cells)||Source|
|Clostridium botulinum||Nausea, vomiting, fatigue, dizziness, dryness of mouth and throat, muscle paralysis, difficulty swallowing, double or blurred vision, drooping eyelids, and breathing difficulties||soil, lakes, streams, decaying vegetation, reptiles|
|Escherichia coli O157:H7||Bloody diarrhea, abdominal pain. Can lead to hemolytic uremic syndrome and kidney failure especially in children and the elderly||animal feces, especially cattle, deer and human; cross contamination from raw meat|
|Salmonella spp.||Abdominal pain, diarrhea, chills, fever, nausea, vomiting||animal and human feces; cross contamination from raw meat, poultry, or eggs|
|Shigella spp.||Abdominal pain, diarrhea, fever, vomiting||human feces|
|Listeria monocytogenes||Febrile gastroenteritis in healthy adults; may lead to spontaneous abortion or stillbirth in pregnant women; severe septicemia and meningitis in neonates and immunocompromised adults; mortality may be 20 to 40%||soil, food processing environments|
|Cryptosporidium spp.||Profuse watery diarrhea, abdominal pain, anorexia, vomiting||Animal and human feces|
|Cyclospora spp.||Watery diarrhea, nausea, anorexia, abdominal cramps (duration 7 to 40 d)||others? specific environmental sources unknown at this time|
|Hepatitis A||Fever, malaise, anorexia, nausea, abdominal pain, jaundice, dark urine||human feces and urine|
|Norwalk/Norwalk-like virus||Vomiting diarrhea, malaise, fever, nausea, abdominal cramps||human feces, vomitus|
In other cases, however, multiplication of the pathogen is also essential. Some microorganisms cause illness only when ingested in high numbers (for example, Clostridium perfringens), while in other cases, the infectious dose is thought to be dependent upon the susceptibility of the individual (most infectious agents). Illness due to Staphylococcus aureus, Bacillus cereus, or Clostridium botulinum is a result of the production of toxins in the food, and it is the toxins that are responsible (sometimes in the absence of viable cells) for symptoms of the disease. These toxins are only produced by multiplying cells. This requires favorable growth conditions. In summary, while enhancing the likelihood of illness, temperature abuse and multiplication of pathogenic bacteria is not always necessary for foodborne illness to occur. Although raw produce is often spoiled by other microorganisms prior to detection of toxin, one should not rely on this fact to prevent the development of disease (for example, botulism).
A wide variety of bacteria, viruses, and parasites have been linked to outbreaks of illness associated with fresh produce (Table O1-O10). Although these microorganisms are physiologically diverse, they share some common features (Table IV-3). Foodborne pathogens that are frequently associated with fresh produce originate, for the most part, from enteric environments - that is, they are found in the intestinal tract and fecal material of humans or animals. Exceptions include C. botulinum, which is usually isolated from soils, water and decaying plant or animal material, and Listeria monocytogenes, which can be readily isolated from human and animal feces, as well as from many other environments including soil, agricultural irrigation sources, decaying plant residue on equipment or bins, cull piles, packing sheds and food processing facilities.
Produce can become contaminated with microbial pathogens by a wide variety of mechanisms. Contamination leading to foodborne illness has occurred during production, harvest, processing, and transporting, as well as in retail and foodservice establishments and in the home kitchen (Table IV-4). Contamination at any point in the food handling chain can be exacerbated by improper handling and storage of produce prior to consumption (Table O10). The point of contamination is important because control measures will be most effective if geared towards reducing contamination at the source. For example, Good Agricultural Practices will not prevent illness due to post-harvest cross-contamination at any point, including foodservice environments or in the home (Table O9).
Contamination of raw fruits and vegetables with pathogenic organisms of human health significance can occur directly or indirectly via animals or insects, soil, water, dirty equipment, and human handling. For example, fruit flies have been shown to transfer Escherichia coli O157:H7 to damaged apples under laboratory conditions (Janisiewicz and others 1999). This may have implications during harvesting and in packing sheds or processing facilities, where damaged produce is inevitable and flies may be difficult to control. Humans and animals can shed foodborne pathogens in the absence of signs of illness. While domestic animals may be separated from fruit and vegetable growing operations, wild animals and birds can only be controlled to a limited extent. Human hygiene, including hand washing all along the food chain, is critical in reducing or eliminating contamination with fecal pathogens.
Table IV-4. Sources of pathogenic microorganisms on fresh produce and conditions that influence their survival and growth
Green or inadequately composted manure
Wild and domestic animals
Water for other uses (for example, pesticides, foliar treatments, growth hormones)
Human handling (workers, consumers)
Transport containers (field to packing shed)
Wild and domestic animals
Wash and rinse water
Sorting, packing, cutting and further-processing equipment
Improper storage (temperature, physical environment)
Improper packaging (includes new packaging technologies)
Cross contamination (other foods in storage, preparation and display areas)
Improper display temperature
Improper handling after wholesale or retail purchase
Cooling water (for example, hydrocooling)
3. Survival and multiplication of pathogens on raw produce
The survival and/or growth of pathogens on fresh produce is influenced by the organism, produce item, and environmental conditions in the field and thereafter, including storage conditions. In general, pathogens will survive but not grow on the uninjured outer surface of fresh fruits or vegetables, due in part to the protective character of the plant's natural barriers (for example, cell walls and wax layers). In some cases pathogen levels will decline on the outer surface.
In the field, the physical environment of leaf surfaces is considered to be inhospitable for the growth and survival of bacteria (for example, lack of nutrients and free moisture, temperature and humidity fluctuations, and ultraviolet light) (Dickinson 1986). Environmental conditions, however, can greatly influence bacterial populations; the presence of free moisture on leaves from precipitation, dew, or irrigation may promote survival and growth of bacterial populations (Blakeman 1981; Andrews 1992; Beattie and Lindow 1995, 1999). Certain conditions, such as sunlight, particularly the shorter ultraviolet wavelengths, can damage bacterial cells (Webb 1976; Jagger 1981; Sundin and others 1996; Sundin and Jacobs 1999). Consequently, nature may select for bacteria with adaptations to these stressful conditions. Although most of the body of research has been done with stress adaptation of microorganisms other than human pathogens (high ultraviolet tolerance in Pseudomonas syringae or high osmotic potentials in Escherichia herbicola) preliminary results suggest that humans pathogens are less likely to develop stress resistance (O'Brien and Lindow 1988). Many of the human pathogens have an enteric source, and therefore may be unsuccessful as plant colonists relative to the more suited plant microbial populations. The relative fitness of human pathogens and common epiphytes (microbes that grow and persist on plant surfaces) and the interaction between bacterial pathogens and indigenous microflora needs further research.
Similarly, after harvest, pathogens will survive but not grow on the outer surface of fresh fruits and vegetables, especially if the humidity is high. In some cases, pathogen levels will decline on the outer surface. The rate of decline is dependent upon the produce type, humidity, and temperature, as well as the atmosphere and type of packaging used. Growth on intact surfaces is not common because foodborne pathogens do not produce the enzymes necessary to break down the protective outer barriers on most produce. This restricts the availability of nutrients and moisture. One exception is the reported growth of E. coli O157:H7 on the surface of watermelon and cantaloupe rinds (Table G/S1).
Survival of foodborne pathogens on produce is significantly enhanced once the protective epidermal barrier has been broken either by physical damage, such as punctures or bruising, or by degradation by plant pathogens (bacteria or fungi). These conditions can also promote the multiplication of pathogens, especially at nonrefrigerated temperatures. Microorganisms often survive at refrigerated temperatures even though these conditions reduce or eliminate the ability of the organisms to multiply. Exceptions to this are the psychrotrophic pathogens including non-proteolytic C. botulinum, L. monocytogenes, Y. enterocolitica, and the presumptive pathogen Aeromonas hydrophila. Various enteric pathogens have been shown to multiply on the surface of cut melons, on shredded lettuce, and on chopped parsley and under acidic conditions, such chopped tomatoes and wounded apple tissue (Tables G/S1 Â– G/S8). Temperature control becomes critical for preventing bacterial reproduction on any cut produce item. Fresh-cut produce, by definition, has been injured through peeling, cutting, slicing, or shredding. These same operations can transfer pathogenic microorganisms, if present, from the surface of the intact fruit or vegetable to the internal tissues. Injured cells and released cell fluids provide a nourishing environment for microbial growth.
A vigorous population of nonpathogenic bacteria is potentially another barrier to reduce the risk of foodborne illness from fresh-cut products. These bacteria do not necessarily prevent the growth of pathogens but they do provide indicators of temperature abuse and age of the produce by causing detectable spoilage. Most pathogens do not cause produce to spoil, even at relatively high populations. In the absence of spoilage, high populations of pathogens may be achieved and the item may be consumed because it is not perceived as spoiled. For this reason, specifications requiring very low microbial counts may, in some cases, compromise produce safety.
Infiltration of wash-water into intact fruit has been demonstrated with several fruits and vegetables, and is thought to have contributed to an outbreak of salmonellosis associated with fresh market tomatoes (Table O8). Wash-water contaminated with microorganisms, including pathogens, can infiltrate the intercellular spaces through pores when conditions are right. Internal gas pressures and surface hydrophobicity usually prevent uptake of water. However, when the produce temperature is much higher than the water temperature, the pressure difference created may be sufficient to draw water into the fruit (Bartz 1999). Adding detergents to the water appears to enhance infiltration, likely due to reduced surface tension. Under some circumstances, wash water may enter an intact fruit through the stem scar or other opening, such as the blossom or stem end of an apple. Conditions that reduce infiltration of plant pathogens should also prevent infiltration of human pathogens.
3.1. Influence of packaging
Fresh produce packaged in gas-permeable films can modify its own atmosphere, thereby creating more favorable conditions for storage. Three mutually interacting processes determine the course of this modification: 1) respiration by the fruit or vegetable, 2) gas diffusion through the produce item, and 3) temperature, and 4) gas transmission through the film. As a result of produce respiration, the oxygen (O2) concentration in the package is decreased and the carbon dioxide (CO2) concentration is increased. Growth and toxin production by C. botulinum is of particular concern in this instance. This subject has been reviewed in depth (see Chapter VI).
3.2. Specific foods - Examples
Raw raspberries and possibly blackberries imported from Guatemala have been associated with several large Cyclospora cayetanensis outbreaks (Table O2). The natural host for this parasite has not been identified; however, contaminated water used for pesticide application and poor harvester hygiene has been suggested as the most likely routes of contamination. Frozen raspberries or frozen strawberries have been linked to two or three outbreaks of hepatitis A, respectively (Table O3). Hepatitis A, a virus spread by human feces, is thought to have contaminated the berries by contact with infected harvesters or contaminated irrigation water. Frozen raspberries have also been associated with illness due to calicivirus, also spread through human feces.
Raw berries destined for the fresh market are harvested by hand and field packed into retail containers without being washed. Strawberries destined for freezing are destemmed in the field, either using a metal device or a thumbnail. Berries which are to be processed are transported, usually at ambient temperature, to a processing facility where they are washed with potable water or water containing an antimicrobial (for example, chlorine), sometimes sliced, and often mixed with up to 30% sucrose before freezing. The extra human handling during harvesting and co-mingling in the processing facility may explain the greater association of outbreaks with frozen berries. Also, virus and parasites may actually be preserved by the freezing step.
To date, bacterial foodborne illnesses have not been linked to consumption of berries. However, reservoirs for enteric organisms such as Salmonella and E. coli O157:H7 are similar to that of hepatitis A virus, suggesting that bacterial pathogens may also be occasional contaminants of berries. A recent FDA survey of imported produce found Salmonella in one of 143 samples of strawberries (Table I1).
3.2.2. Seed sprouts.
Over the past several years, seed sprouts have become a fresh produce item commonly linked to foodborne illness. Seed sprouts are a special problem because bacterial pathogens that may be present at very low levels on sprout seeds at the time of sprouting can multiply to very high levels during the 3 to 10 d sprouting process and can survive through the typical refrigerated shelf life of the products (Table G/S 7). Also, seed sprouts are produced as agricultural commodities, not subject to sanitation requirements because they are not regarded as foods. A wide variety of pathogens have been isolated from sprouted seeds (Table I2). Outbreaks have been associated primarily with Salmonella serotypes but have also been attributed to B. cereus, E. coli O157:H7, and Y. enterocolitica (Table O4).
Most sprout outbreaks have been due to seed contaminated with a bacterial pathogen before the sprouting process begins, presumably during production or harvest (Table O4). Many pathogens can survive for months under the dry conditions used for seed storage. Populations in the seeds are exceptionally low, making it difficult to detect pathogens in routine seed screening programs (Table I2). Although contaminated alfalfa sprouts have been identified as the source of pathogens in many outbreaks, clover, radish, and mung bean sprouts have also been associated with outbreaks. The association with alfalfa sprouts may be due to the volume consumed, as these are the most popular type of seed sprouts that are commonly eaten raw. Mung bean sprouts, while sold in relatively large quantities are often stir-fried or otherwise heated prior to consumption. This would reduce the risk and likelihood of illness from mung bean sprouts. However, any type of sprout seed may potentially be contaminated with bacterial pathogens before it is sprouted.
Cut cantaloupe is considered a potentially hazardous food in the FDA Food Code because it is capable of supporting the growth of pathogens due to low acidity (pH 5.2 to 6.7) and high water activity (0.97 to 0.99). The FDA investigated the frequency of Salmonella isolated from cantaloupe imported from Mexico (Table I1). In 1990, 11 of 1,440 (0.76%) cantaloupe were positive for eight different Salmonella serotypes. In 1991, 24 of 2,220 (1.08%) were positive with 12 different Salmonella serotypes isolated. More recently, the FDA isolated Salmonella from eight (5.3%) and Shigella from three (2.0%) of 151 cantaloupe samples collected from nine countries exporting to the United States (FDA 2001). These results suggest that melons may be naturally contaminated with Salmonella.
Outbreaks of salmonellosis have been associated with the consumption of cut cantaloupe and watermelon (Table O1). At least two of these outbreaks have been relatively large and have involved multiple states and/or provinces. For most outbreaks, it has been assumed that Salmonella was present on the rind, presumably contaminated in the field or during washing in a packinghouse, and that the edible surface became contaminated during final preparation. Improper storage temperature combined with the favorable conditions for growth on the surface of cut melons were factors that likely contributed to the outbreak (Table O10). Some outbreaks associated with melons have resulted from contamination during final preparation either through an infected food handler (with, for example, Norwalk virus) or cross-contamination from raw beef to the melon (with, for example, E. coli O157:H7) via knives, cutting boards, or hands.
Escherichia coli O157:H7 and Salmonella, can survive and grow readily on improperly stored (non-refrigerated) cut melons (Table G/S1). When initial populations were between 2.0 and 3.0 log CFU/g, final levels reached 7.0 or 8.0 log CFU/g after 24 h at 23 °C (73.4°F). At 5 °C (41 °F), both Salmonella and E. coli O157:H7 populations did not increase.
Cut melons are subject to time/temperature requirements of the U. S. FDA model food code criteria for potentially hazardous food. Recommendations made by the FDA to retail establishments that prepare or sell fresh cantaloupe are that melons should be washed before cutting, clean, sanitized utensils and surfaces should be used when preparing cut melons, cut melons should be kept at or below 7 °C (44.6 °F), and they should be displayed for no longer than 4 h if they are not refrigerated (Golden and others 1993).
3.2.4. Unpasteurized juices.
Approximately 2% of all juices sold in the United States are unpasteurized. Parish (1997) provides an excellent review of the safety of unpasteurized fruit juices. Unpasteurized juices are made from fruits and vegetables that are ground and/or pressed or squeezed to extract the juice. Unpasteurized juices are included here because they have not been thermally processed and an evaluation of outbreaks associated with these products might contribute to an understanding of risk factors for contamination of the raw fruits.
There have been very few surveys of retail juices for the presence of pathogens, probably because of the very low probability of finding pathogens in these products. Sado and others (1998) used rapid test kits to survey retail juices for the presence of L. monocytogenes, E. coli O157:H7, Salmonella, coliforms, and fecal coliforms. Only L. monocytogenes was isolated from two of 50 juices, an apple juice (pH 3.78) and an apple raspberry blend (pH 3.75) (Table I1).
Although there is a long history of juice-related outbreaks, they have been relatively infrequent and, until 1995, were generally associated with very small commercial processors or home-prepared products (Table O5). While the acidity of most fruit juices prevents the multiplication of pathogens, survival is much better than has been traditionally assumed (Table G/S 6). Pathogen viability decreases with increasing temperature due to the rapid growth of yeasts and other spoilage organisms at the higher temperatures. This also leads to a decrease in shelf life.
While pathogen contamination routes have not been definitively confirmed in any juice outbreak, the use of dropped fruit, the use of non-potable water, and the presence of cattle, deer, or, in one case, amphibians, in or near the orchards or groves does appear to be a reoccurring theme. Of five documented outbreaks associated with reconstituted orange juice, three have been the result of contamination by an infected handler preparing the juice (Table O6). In another outbreak the water source used to reconstitute the juice was thought to be a factor.
3.3. Pathogens of concern Â– Bacteria
3.3.1. Aeromonas species
Aeromonas species were first recognized as pathogens of cold-blooded animals. The ability of Aeromonas hydrophila and Aeromonas sobria to cause human infection has not been fully confirmed, however, their potential as infectious agents exists (Wadstrom and Ljungh 1991). The presence of Aeromonas in drinking water, fresh and saline waters, brackish water and sewage has been demonstrated on a global scale. Cytotoxic strains have been isolated from a wide range of seafoods, meats and poultry as well as from seed sprouts, lettuce or salad greens, mixed raw vegetables, parsley, and carrots (Table I4, I5, I7); however, outbreaks associated with this organism have not been reported. The pathogen can grow rapidly on raw vegetables and seed sprouts at refrigeration temperature (Tables G/S4 and G/S7). Controlled or modified atmosphere storage does not significantly affect the growth of A. hydrophila.
3.3.2. Campylobacter species
Campylobacter jejuni and Campylobacter coli are a leading cause of bacterial enteritis. Campylobacter has been isolated from a variety of produce items sampled from farmer's markets in Canada and from mushrooms sampled from retail markets in the United States (Tables I4 and I6). While consumption of contaminated food of animal origin, particularly poultry, is largely responsible for infection, Campylobacter enteritis has also been associated with lettuce or salads (Table O7). Cross-contamination during food preparation was thought to be possible or probable, in one case with raw chicken juices (Table O7). Cross-contamination of fresh produce with Campylobacter from poultry and other meats is a distinct possibility in delicatessen and other foodservice operations. Therefore, the linkage of C. enteritis to uncooked produce should not be viewed as improbable; control should focus on reducing cross-contamination during food storage and preparation. Studies reported by Castillo and Escartin (1994) indicate that C. jejuni can survive on sliced watermelon and papaya for sufficient time to be a risk to the consumer (Tables G/S1 and G/S2).
3.3.3. Escherichia coli
Enterotoxigenic E. coli is a common cause of travelers' diarrhea, an illness sometimes experienced when visiting developing countries. Raw vegetables are thought to be a common cause of travelers' diarrhea. A prospective study of 73 physicians and 48 family members attending a conference in Mexico City in 1974 revealed that enterotoxigenic E. coli was the most common cause of illness (Merson and others 1976). Fifty-nine participants became ill from eating salads containing raw vegetables.
Outbreaks of illness determined to be caused by enterotoxigenic E. coli in persons who had not traveled outside the United States are not uncommon. In one outbreak, 47 airline passengers suffered from illness strongly associated with eating garden salad made from iceberg and romaine lettuce, endive, and shredded carrots (see Beuchat 1996b). In another outbreak, 78 lodge guests became ill after consuming tossed salad as part of a buffet dinner. The salad contained several ingredients, including onions, carrots, zucchini, peppers, broccoli, mushrooms, and tomatoes (see Beuchat 1996b).
Enterohemorrhagic E. coli O157:H7 is recognized as an important foodborne pathogen. The infectious dose is very low and sequelae to gastroenteritis can include bloody diarrhea (hemmorrhagic colitis) and hemolytic uremic syndrome. The latter is most common in young children (<5 years) and in the elderly. There have been very few surveys for the presence of the organism in raw produce. Surveys of lettuce or salad mixes in the United Kingdom and United States did not isolate the organism and, although originally included in an FDA imported produce study, it was later deleted because positive samples had not been identified (FDA 2001). However, a single survey in Mexico revealed very high isolation rates (19%) for this organism in mixed vegetables, cilantro, coriander, and celery (Table I5). This single study was published as an abstract in 1995 and, to our knowledge, has not been published as a peer reviewed manuscript. Therefore, we were unable to review their methodology.
Since cattle appear to be a primary reservoir, the vast majority of outbreaks of illness associated with E. coli O157:H7 have been associated with consuming undercooked beef and dairy products. However, outbreaks have also been linked to lettuce (Table O7), unpasteurized apple cider (Table O5), cantaloupe (Table O1), and sprouts (Table O4). In outbreaks associated with cantaloupe and in some cases lettuce, contamination, particularly with raw beef juices, occurred during final preparation (Table 09).
Escherichia coli O157:H7 grows rapidly in several types of raw fruits and vegetables, particularly when stored at 12°C (53.6°F) or above (Tables G/S1, G/S2, G/S4, G/S5, G/S7). Packaging under modified atmosphere has little or no effect on the survival or growth of E. coli O157:H7. In addition, the infection dose of E. coli O157:H7 is low and can develop acid-resistance.
3.3.4. Listeria monocytogenes
While L. monocytogenes causes relatively mild gastroenteritis in healthy adults, the illness can be severe in susceptible individuals including pregnant women, neonates, and immune compromised individuals. The infective dose for this organism has not been clearly established, although it is thought to be relatively low among susceptible individuals. Listeria monocytogenes is widely distributed on raw fruits and vegetables (Tables I2 and I4) and on plant material (Beuchat 1996b). However several studies with relatively large sample sizes failed to detect the organism (Table I4). Factors affecting its presence or persistence have yet to be determined. Plants and plant parts used as salad vegetables play a role in disseminating the pathogen from natural habitats to the human food supply. This role may be indirect, for example by contaminating milk via forage or silage, or direct in the form of raw contaminated produce. In 1967, Blenden and Szatalowicz (1967) reported that 731 cases of human listeriosis had been documented between 1933 and 1966 in the United States. They stated that produce such as lettuce or other fresh vegetables contaminated with L. monocytogenes may have been responsible for some of these cases. However, documented outbreaks associated with this organism and linked to fresh produce have been limited. Ho and others (1986), (Table O8), reported an outbreak of L. monocytogenes infection that involved 23 patients from eight Boston hospitals in 1979. Three foods (tuna fish, chicken salad and cheese) were preferred by case patients more frequently than by control patients. However, the only common foods served with these foods were raw celery, tomatoes, and lettuce. It was concluded that consumption of these vegetables may have caused the listeriosis outbreak. No attempt was made to isolate L. monocytogenes from vegetables at the time of the outbreak.
An outbreak of human infection due to L. monocytogenes occurred in 1981 in the Maritine provinces (Prince Edward Island, Nova Scotia and New Brunswick) in Canada (Table O8). A case-control survey revealed that cases were more likely than controls to have consumed coleslaw during the three months before onset of illness. Ingestion of radishes was associated with coleslaw consumption but not with illness. Coleslaw obtained from the refrigerator of a patient was positive for L. monocytogenes serotype 4b, which was the epidemic strain and the strain isolated from the patient's blood. The coleslaw was commercially prepared with cabbage and carrots obtained from wholesalers and local farmers. Two unopened packages of coleslaw purchased from two different Halifax, Nova Scotia supermarkets yielded L. monocytogenes serotype 4b. Both packages of coleslaw were produced by the same processor. An investigation of the sources of cabbage revealed one farmer who, in addition to raising cabbage, maintained a flock of sheep. Two of his sheep had died of listeriosis in 1979 and 1981. The farmer used composted and fresh sheep manure in fields in which cabbage were grown. From the last harvest in October through the winter and early spring, cabbage was kept in a cold-storage shed. A shipment of cabbage from that shed during the period of the outbreak was traced to the implicated coleslaw processor. This information strongly suggests that the vehicle of the 1981 Canadian outbreak of listerosis was coleslaw.
Listeria monocytogenes can grow on fresh produce stored at refrigerated temperature. Growth on fresh-cut fruit as well as asparagus, broccoli, butternut squash, coleslaw and cauliflower, rutabaga stored at 4°C (39.2°F) (Table G/S4), lettuce at 5°C (41°F) (Table G/S5) and chicory endive at 6.5°C (43.7°F) (Table G/S4) has been reported. Controlled atmosphere storage does not appear to influence growth rates. Carrot juice appears to be inhibitory towards this organism (Beuchat and Brackett 1990a; Nguyen-the and Lund 1991, 1992; Beuchat and others 1994; Beuchat and Doyle 1995). The antimicrobial properties are attributed to phytoalexins naturally present in carrots. The addition of carrot juice as a natural antimicrobial in other food products has been relatively unsuccessful (Beuchat and Doyle 1995).
The genus Salmonella has over 2700 serotypes. Animals and birds are the natural reservoirs. Surveys of fresh produce have revealed the presence of several Salmonella serotypes capable of causing human infection (Table I1-I7).
Poultry and other meat products, eggs and dairy products, are the most commonly implicated sources in salmonellosis outbreaks. Fresh fruits and vegetables are implicated less frequently, although outbreaks have been documented most notably in cantaloupe and sprouts. Several additional large outbreaks of salmonellosis have been attributed to fresh produce. Among them are three multi-state outbreaks traced to the consumption of raw tomatoes; one involved Salmonella Javiana in 1992, another involved Salmonella Montevideo in 1993, and a third in 2000 involved Salmonella Baildon (Table O8). Subsequent laboratory studies revealed that the pathogen can grow in damaged, chopped, or sliced tomatoes (pH 4.1 Â– 4.5) stored at 20 to 30°C (68 to 86°F ) (Table G/S3).
3.3.6. Shigella species
The genus Shigella is composed of four species, Shigella dysenteriae, Shigella boydii, Shigella sonnei, and Shigella flexneri. All species are pathogenic to humans at a low dose of infection. Shigellosis is usually transmitted from person-to-person but may also occur by consumption of contaminated water and foods, including foods such as fruits or vegetables that have received little or no heat treatment. Several large outbreaks of shigellosis have been attributed to the consumption of contaminated raw vegetables. A lettuce processing facility was the common source of product responsible for outbreaks caused by S. sonnei that occurred simultaneously on two university campuses in Texas (Table O7). Ill students on both campuses had eaten salads from self-serve salad bars. Lettuce was the only produce item used in salads consumed by all students who became ill.
In another outbreak of S. sonnei gastroenteritis was associated with eating shredded lettuce (Table O7). All implicated restaurants received shredded lettuce from the same produce facility. An investigation suggested that a worker in the plant was the source of contamination and that the method of processing allowed contamination of the lettuce.
Two midwestern United States outbreaks of S. flexneri infection have been linked to the consumption of fresh green onions (see Beuchat, 1996b). The onions were traced to shippers in California who obtained most of their green onions from a single farm in Mexico. It was concluded that contamination may have occurred in Mexico at harvest or during packing.
Shigella sonnei can survive on lettuce at 5°C (41°F ) for 3 days without decreasing in number, and increased by more than 1000-fold at 22°C (71.6°F) (Table G/S5). Shigella can grow in shredded cabbage and chopped parsley stored at 24°C (75.2°F) (Table G/S4). Populations of S. sonnei, S. flexneri, and S. dysenteriae inoculated onto the surface of freshly cut cubes of papaya, jicama, and watermelon increased substantially within 4-6 h at 22-27°C (71.6-80.6°F) (Table G/S2, G/S4, and G/S1). The pH values of the three fruits were 5.69, 5.97 and 6.81, respectively.
3.3.7. Staphylococcus aureus
Staphylococcus aureus has been detected on fresh produce and ready-to-eat vegetable salads (Table I2 and I6), and is known to be carried by food handlers. However, enterotoxigenic S. aureus does not compete well with other microorganisms normally present on fresh produce, so incipient spoilage caused by nonpathogenic microbiota would likely precede the development of high populations of this pathogen. An outbreak of staphylococcal foodborne illness was linked to canned mushrooms. Growth and toxin production occurred prior to processing the mushrooms, without significant visual degradation, possibly because the mushrooms were held under ambient conditions in plastic bags and with salt. Conditions within the bags rapidly became anaerobic and the normal spoilage microbiota may have been inhibited and S. aureus selected. Because the toxin is heat stable, it survived the thermal process. This suggests that raw produce-associated outbreaks due to S. aureus could potentially occur given the right conditions. S. aureus has been shown to grow on peeled Hamlin oranges (Table G/S2) stored at 24°C (75.2°F) or survived up to 14 d when stored at 4-8°C (39.2-46.4°F).
3.3.8. Yersinia enterocolitica
Although animals, particularly swine, are the predominant natural reservoir for Y. enterocolitica, the pathogen has also been isolated from several raw vegetables. Yersinia enterocolitica infection has been associated with the consumption of mung bean sprouts contaminated with well-water containing the organism (Table O4). Catteau and others (1985) analyzed 58 samples of grated carrots obtained from eating establishments in France and found that 27% were contaminated with Yersinia. Seven percent of the samples contained Y. enterocolitica serotypes that may be pathogenic to humans. Darbas and others (1985) examined prepared raw vegetables destined for school meals that had been held for up to 5 days in cold storage. Fifty percent of 30 samples of raw vegetables analyzed contained Yersinia species. The incidence was higher in root and leafy vegetables than for tomatoes or cucumbers. Yersinia enterocolitica was the only species isolated from grated carrots, whereas Yersinia intermedia and Yersinia kristensenii were mainly isolated from lettuce. Cross-contamination between vegetables was observed in some cases. No pathogenic strains were isolated from raw vegetables analyzed in this study. The pathogen can grow at refrigeration temperatures commonly used during transport and storage of fresh produce.
3.4. Spore-forming pathogenic bacteria
Contamination of vegetables and fruits with spores of pathogenic bacteria such as B. cereus, C. botulinum, or C. perfringens present in soil is common (Tables I2, I4, I5, and I7). However, only when produce is handled in a manner that enables germination of spores and growth of vegetative cells is there a threat to public health from these spore-forming bacteria. Of particular concern are vegetables packaged under modified atmosphere (see Chapter VI).
Botulism has been linked more to consumption of cooked vegetables than to fresh produce. The organism requires relatively high water activity, a pH of greater than 4.6, relatively warm temperatures, and anaerobic conditions to grow and produce toxin. Growth and toxin production often lag behind spoilage in fresh vegetables. Of greatest concern are those products that will support growth and toxin production prior to visible signs of spoilage.
Outbreaks implicating cabbage and garlic in oil have been documented (Table O8-10). The garlic was likely dried and rehydrated prior to mixing with oil, but subsequent studies have shown that the organism will grow in fresh garlic. Botulism has been linked to eating coleslaw prepared from packaged, shredded cabbage mixed with coleslaw dressing (Solomon and others 1990). Since the pH of the dressing was 3.5, C. botulinum had apparently grown in the shredded cabbage that was suspected to have been packed in a modified atmosphere. A survey subsequently revealed that 12 of 88 cabbages obtained from supermarkets contained C. botulinum spores, and that botulinum toxin can be formed in shredded cabbage when the cabbage is packaged under an atmosphere containing reduced oxygen and stored at 22-25°C (71.7-77°F) for 4-6 d. The appearance and color of the stored cabbage was acceptable when toxin was present. Other vegetables that appear to support growth and toxin production of C. botulinum before spoilage is detected are cubed butternut squash and sliced onions (Table G/S4).
The high rate of respiration of mushrooms can create an anaerobic environment within film-wrapped packages, thus favoring botulinal toxin production. Botulinal toxin was produced in polyvinyl chloride film-packaged mushrooms held at 20°C (68°F) for 3-4 d, and the toxic mushrooms appeared to be edible (Sugiyama and Yang 1975). Although placing holes in film reduces the shelf life of mushrooms, this practice is encouraged so as to prevent C. botulinum growth. Proteolytic strains of C. botulinum grew and produced toxin in vacuum-packaged Enoki mushrooms held at 15-27°C (59-80.6°F), but the mushrooms were visibly spoiled at the time toxin was detected (Malizio and Johnson 1991).
Bacillus cereus has been associated with one outbreak related to the consumption of mixed seed sprouts (Table O4). The organism was subsequently shown to be present at relatively high levels in a variety of seeds sold for sprouting (Table I2). Clostridium perfringens was associated with one outbreak epidemiologically linked to the consumption of salad. Illness caused by this organism is usually associated with gravies and meat dishes. Large numbers of the organism are required to cause illness and anaerobic conditions and a nutrient-rich environment are essential for growth of the organism. It is not clear how salad (presumably lettuce salad) would provide these conditions.
3.5. Pathogens of greatest concern - Viruses
Outbreaks caused by hepatitis A virus, calicivirus, and Norwalk-like viruses have been associated with the consumption of produce (Table O1, O6, O7, O8). These outbreaks have been associated with frozen raspberries or frozen strawberries, lettuce, melons, salads, watercress, diced tomatoes, and fresh-cut fruit. A number of these outbreaks were the result of contamination via an infected food handler during final preparation (Table O9). Hepatitis A and Norwalk-like viruses are the most commonly documented viral food contaminants. Viruses can be excreted in large numbers by infected individuals and have been isolated from sewage and untreated waste-water used for crop irrigation. Although viruses cannot grow in or on foods, their presence on fresh produce, which may serve as vehicles for infection, is of concern. Of 14 reports of viral gastroenteritis outbreaks cited by Hedberg and Osterholm (1993), a food handler who was ill before or while handling the implicated food was identified as the source of infection in eight outbreaks. Salads were the implicated vehicle in five outbreaks (36%), and cold food items or ice were implicated in all but one outbreak.
The survival of viruses on vegetables has been studied. Several enteroviruses (poliomyelitis, enteroviruses, hepatitis A, rotavirus, and Coxsackie viruses) can survive in a variety of raw vegetables for periods exceeding the normal shelf life of salad vegetables (Table G/S8). Survival appears to be dependent upon the pH, moisture content, and temperature. These observations indicate that salad vegetables can serve as vehicles for the transmission of viral pathogens to humans.
3.6. Pathogens of greatest concern - Protozoan parasites
Reliable and sensitive detection methods for parasites in raw produce are lacking and therefore, incidence studies are not available with the exception of one Costa Rican survey. In Costa Rica, Monge and Chinchilla (1996) surveyed a total of 640 samples from eight different vegetables for the presence of Cryptosporidium oocysts, fecal coliforms, and generic E. coli. Escharichia coli was found at populations of 101 (tomato) to 105/106 MPN/g (cilantro leaves/cilantro roots). Cryptosporidium oocysts were found in at least one of 80 samples of each vegetable except cabbage. Highest isolation rates were seen for cilantro leaves (5 of 80 samples positive) and cilantro roots (7 of 80 samples positive). Highest contamination rates were observed in the rainy season and the probable contamination route was thought to be the use of contaminated irrigation water. No correlation was observed between the presence of Cryptosoridium oocysts and populations of fecal coliforms or generic E. coli.
3.6.1. Cryptosporidium parvum
Cryptosporidium parvum is an obligate intracellular parasite. It is currently thought that the form infecting humans is the same species that causes disease in young calves. The forms that infect avian hosts and those that infect mice are not thought capable of infecting humans. Cryptosporidium sp. infects many herd animals (cows, goats, and sheep among domesticated animals, and deer and elk among wild animals). The infective stage of the organism is the oocyst. The sporocysts are resistant to most chemical disinfectants, but are susceptible to drying and the ultraviolet portion of sunlight.
Intestinal cryptosporidiosis is characterized by severe watery diarrhea that is particularly severe in immune compromised individuals. Healthy adults may be asymptomatic. The infectious dose is less than 10 organisms and, presumably, one organism can initiate an infection. Oocysts are shed in the infected individual's feces. Cryptosporidium sp. could occur, theoretically, on any food touched by a contaminated food handler. The incidence is higher in child day care centers that serve food. Fertilizing salad vegetables with manure is another possible source of human infection. Large outbreaks have been associated with contaminated water supplies suggesting that contaminated irrigation water could be another route of contamination. Produce- and juice-associated outbreaks of cryptosporidiosis have occurred (Table O-5, O-8).
3.6.2. Cyclospora cayetanensis
Cyclospora cayetanensis is a unicellular parasite previously known as cyanobacterium-like or coccidia-like body (CLB). The first known human cases of illness caused by Cyclospora infection (for example, cyclosporiasis) were reported in the medical literature in 1979. Cases have been reported with increased frequency from various countries since the mid 1980s, in part because of the availability of better techniques for detecting the parasite in stool specimens.
Infected persons excrete the oocyst stage of Cyclospora in their feces. When excreted, oocysts are not infectious and may require days to weeks to become infectious (for example, to sporulate). Therefore, transmission of Cyclospora directly from an infected person to someone else is unlikely. However, indirect transmission can occur if an infected person contaminates the environment and oocysts have sufficient time, under appropriate conditions, to become infectious. For example, Cyclospora may be transmitted by ingestion of water or food contaminated with oocysts. Outbreaks linked to contaminated water, as well as outbreaks linked to various types of fresh produce, have been reported in recent years. Raspberries and possibly blackberries imported from Guatamala have been implicated in at least five outbreaks, two involving numerous states and Canadian provinces (Table O2). The route of contamination was not conclusively determined, but was suspected to be related to contaminated water used for irrigation or pesticide application. Berries imported in the spring but not in the fall were associated with illnesses suggesting a seasonality to the illness. In addition, fresh basil and products made from the basil were implicated in an outbreak in 1997 (Table O8). The source of contamination for this outbreak was not determined. How common the various modes of transmission and sources of infection are is not yet known, nor is it known whether animals can be infected and serve as sources of infection for humans. The incubation period between acquisition of infection and onset of symptoms averages 1 week. Cyclospora infects the small intestine and typically causes watery diarrhea, with frequent, sometimes explosive, stools. Other symptoms can include loss of appetite, substantial loss of weight, bloating, increased flatus, stomach cramps, nausea, vomiting, muscle aches, low-grade fever, and fatigue. If untreated, illness may last for a few days to a month or longer, and may follow a remitting-relapsing course. Some infected persons are asymptomatic.
3.6.3. Giardia lamblia
Organisms that appear identical to those that cause human illness have been isolated from domestic animals (dogs and cats) and wild animals (beavers and bears). A related but morphologically distinct organism infects rodents, although rodents may be infected with human isolates in the laboratory. Human giardiasis may involve diarrhea within 1 week of ingestion of the cyst, which is the environmental survival form and infective stage of the organism. Normally, illness lasts for 1 to 2 weeks, but there are cases of chronic infections lasting months to years. Chronic cases, both those with defined immune deficiencies and those without, are difficult to treat. Different individuals show various degrees of symptoms when infected with the same strain, and the symptoms of an individual may vary during the course of the disease.
Ingestion of one or more cysts may cause disease. Giardiasis is most frequently associated with the consumption of contaminated water. Cool moist conditions favor the survival of the organism. Produce-related outbreaks have been linked to lettuce, tomatoes, and onions (Table O7, O8).
- Numerous microorganisms, most of them from enteric environments (for example, Salmonella spp., E. coli O157:H7, C.jejuni) but also from other sources (for example, C. botulinum and L. monocytogenes) have been isolated from a variety of fresh fruits and vegetables.
Although isolation rates can be high, they are not consistent. The percentage of samples contaminated ranges from 0 to 50%, depending upon the product and target pathogen. Because of differences in their production systems, surface morphology, or other factors, produce items, such as lettuce, berries, seed sprouts, melons, seem to provide conditions for pathogen survival and/or growth.
The number of foodborne illness outbreaks linked to fresh produce and reported to the United States Centers for Disease Control and Prevention (CDC) has increased in the last years. Some of this increase is due to improved surveillance, but other factors may also come into play, such as increase in consumption, change in consumers' habits, and complex distribution systems.
Foodborne illness resulting from the consumption of any food is dependant upon a several factors. For example, the produce must be contaminated with a pathogen that survives or grows to infective level doses at the time of consumption. Temperature abuse and growth is not always necessary for foodborne illness to occur.
Conditions for survival and/or growth of pathogens on fresh produce necessary for illness are influenced by the type of microorganism, produce item, and environmental conditions in the field and subsequent handling and storage. For example, free moisture resulting from condensation rain or irrigation may promote survival and growth of microbial populations in an otherwise inhospitable environment.
After harvest, pathogens will survive but not grow on the outer surface of most fresh fruits and vegetables, especially if the humidity is high. In some cases, pathogen levels will decline on the outer surface. The rate of decline is dependent upon the produce type, humidity, and temperature, as well as the atmosphere and type of packaging used.
Survival and multiplication of foodborne pathogens on produce is significantly enhanced once the protective epidermal barrier has been broken either by physical damage, such as punctures or bruising, or by degradation by plant pathogens.
Physically damage produce and fresh cut produce can promote the multiplication of pathogens, especially at nonrefrigerated temperatures. At refrigerated temperatures the ability of the microorganisms to multiply is reduced with the exceptions of psychrotrophic pathogens (for example, non-proteolytic C. botulinum, L. monocytogenes, Y. enterocolitica).
Specifications requiring very low microbial counts may, in some cases, compromise produce safety because the population of nonpathogenic bacteria is potentially a barrier that reduces the risk of illness associated with fresh-cut products.
Under some circumstances (for example, pressure differentials) wash water may enter an intact fruit through the stem scar or other opening, promoting pathogen infiltration. Access to nutrients inside the product may induce pathogen multiplication to hazardous levels. Conditions that reduce infiltration of plant pathogens should also prevent infiltration of human pathogens.
- Packaging of the product under modified atmospheres changes the growth rate of pathogens which may become a concern (for example, growth and toxin production by C. botulinum).
5. Research needs
Continue and increase the number of well-designed incidence studies of pathogens in fresh produce. Isolation studies should be designed considering their statistical relevance, consistency (for example, consistent sample collection, treatment, laboratory test methods, and data analysis) and including testing of control samples. Negative results should also be reported.
Increase surveillance and investigation of fresh produce related outbreaks.
Investigate the relative fitness of human pathogens and common epiphytes (microbes that grow and persist on plant surfaces) and the interaction between bacterial pathogens and indigenous microorganisms.
Determine the effects of various environmental factors (for example, ultraviolet irradiation) on the survival and growth of pathogens of concern.
- Investigate the factors affecting produce infiltration of microorganisms and assess the risk of foodborne disease due to infiltration of pathogen inside produce.
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