|Table 1. Studies conducted on the internalization, survival, or growth of microorganisms in produce and juice.
| Internalization of Microorganisms
Survival and Growth
Of Microorganisms In
Potential for Infiltration, Survival and Growth Of Human Pathogens within Fruits and Vegetables
There have only been 9 studies of human pathogens in produce and juice that FDA could find?
|(a)Value represents the number of studies performed on a given subject.
U. S. Food and Drug Administration
Center for Food Safety and Applied Nutrition
Potential for Infiltration, Survival and Growth Of Human Pathogens within Fruits and Vegetables
In the Federal Register of April 24, 1998 (63 FR 20450), FDA proposed to adopt regulations to ensure the safe and sanitary processing of fruit
and vegetable juices through implementation of Hazard Analysis Critical Control Point (HACCP) systems. In addition, in the Federal Register of
July 8, 1998 (63 FR 37030), FDA published a final rule requiring that juice products not specifically processed to destroy harmful
bacteria (i.e., processed to achieve a 5-log reduction in the most resistant pathogen of public health concern) bear a warning
statement informing consumers of the potential risk of foodborne illness associated with the product. In the HACCP proposal, the
agency proposed to require that juice processors include in their HACCP plans control measures that will produce at least a 5-log reduction in
the pertinent pathogen. Prior to the 1998 rulemakings, FDA had sought the advice of the National Advisory Committee on Microbiological Criteria
for Foods (NACMCF). In response to FDA's request, NACMCF recommended the proposed 5-log performance standard in order to ensure the
safety of juice.
Consistent with NACMCF recommendation, FDA has not proposed a specific intervention technology (e.g., pasteurization) to be used to meet
the performance standard. Instead, the agency has proposed a flexible 5-log reduction standard that theoretically could be met for some fruit (e.
g., citrus) through cumulative steps. In the April 1998 proposal, FDA stated that steps such as culling, washing, brushing, and sanitizing, followed
by extraction processes that minimize contact with the peel, could be used cumulatively to attain the 5-log reduction as long as processors could
validate bacterial reduction under their HACCP systems.
At the time of the proposal, FDA believed that such cumulative steps could be appropriate for juices produced from citrus fruit because
pathogens were not reasonably likely to be found in the interior of such fruit (63 FR 20450, April 24, 1998). The agency also stated that the
acidic nature of citrus fruits could further inactivate any pathogens that may be present in the fruit. However, comments to the proposed rule
have questioned the assumption that pathogens are not likely to be found in the interior of citrus fruit. In addition, FDA
conducted a search of the relevant published literature and has undertaken research. Both the literature and FDA research
suggest that pathogens could be internalized into citrus fruit and survive once inside the fruit.
This background document summarizes the pertinent published and unpublished information. The information contained in this document was
collected by conducting computer searches on relevant topics and contacting researchers who have done studies in related areas. These
studies were categorized as shown in Table 1.
Internalization of Microorganisms into Fruits and Vegetables
Information is available regarding internalization of plant and human pathogens into fruits and vegetables generally. Specifically, research has
been conducted regarding mechanisms by which microbes enter produce, the types of organisms that have been shown to gain entry, and the
commodities for which microbial contamination is a potential problem.
Microorganisms have been shown to enter produce through various pathways available due to the natural structure of certain produce. Bacteria
can enter leaves of plants through the stomata and enter fruit through the stem, stem scar, or calyx (Charkowski, 1999; Samish
and Etinger-Tulczynska, 1963; Samish et al., 1963; Zhuang et al., 1995). Leben (1972) showed that bacteria can be found in more
than 60 percent of the buds of field-grown commodities studied, including red clover, soybeans, cucumbers, turnips, and grapes.
In this same study, large numbers of bacteria were associated with buds, flowers, and small pods on field soybean plants. Baldwin
and Goodman (1963) found a high percentage of apple buds yielding a specific plant pathogen in midwinter, which suggested that
the buds were infected the previous growing season. Seo and Frank (1999), using confocal scanning laser microscopy, showed
that lettuce leaves dipped in a suspension of Escherichia coli O157:H7 absorbed the pathogen through the stomata and cut
surfaces on the leaves.
Microorganisms may also enter fruits and vegetables through damage to the natural structure, such as punctures, wounds, cuts,
and splits. These injuries can occur during maturation or during harvesting and processing. For example, citrus fruits may suffer
rind damage and microbial penetration as a result of creasing during growing, which may result in splits during washing or
packing; stem-end rot also facilitates microbial entry. In addition, pitting of the citrus rind can occur when fruit is exposed to
temperatures below 0° C, and stem-end rind breakdown can occur as a result of aging (Ryall and Pentzer, 1982). Hill and Faville
(1951) postulated that citrus on the tree could become infected by insect punctures, thorn injury, or hail damage, but noted that in
order for microbes to reproduce and cause infection the injury would have to penetrate the juice sacs. Subsequently, Hill and
Wenzel (1963) found that 35 percent of dropped and frost-damaged oranges had microholes too small for visual detection; half of
the fruit having microholes was contaminated with microbes.
Almed et al. (1973) found that citrus fruits could be damaged in numerous ways during harvesting and that the damage provides opportunities
for decay organisms to gain entrance to the fruit. Manually harvested fruits are subject to plugging (tearing off a portion of the peel around the
stem end of the fruit during picking), while mechanically harvested fruit is more subject to splits, punctures, and bruises. Mechanical harvesting
also results in an increased number of fruits with attached stems more than 1 cm long, which can puncture other fruits.
Ballinger and Nesbitt (1982) found that grapes with torn stem scars had 6 - 10 times more internal decay than grapes with dry stem scars. They
noted that stem scars of muscadine grapes appear to be a prime site for entrance of plant pathogens. Carballo and coworkers (1994) found that
bell peppers packaged in a packinghouse had more bruises than peppers packaged on field packing lines; however, the field-packed peppers
had more abrasions. The authors noted that volume of open skin injuries (which were more numerous on field-packed fruit) was positively
associated with greater tissue decay. Bartz and Showalter (1981) have demonstrated that tomatoes with fresh stem scars are more vulnerable to
infiltration than tomatoes with old stem scars and also showed that green and pink tomatoes are more susceptible to water infiltration and
became diseased earlier than did similarly treated red fruits. Sugar and Spotts (1993) showed that pears, when exposed to bruising and
pressure for extended periods of time in the presence of spores of Phialophora malorum, do not become infected unless they also have
Bacterial soft rot in fruits and vegetables may increase the likelihood of contamination of the fruit or vegetable with pathogens of
concern. Wells and Butterfield (1997) demonstrated that Salmonella spp. was present in 18 - 20 percent of soft-rotted samples of
vegetables, including sprouts, beans, broccoli, cantaloupe, carrots, lettuce, onions, peppers, potatoes, tomatoes and mixed
vegetables. This is nearly double the rate (9 - 10 %) found on intact, healthy samples of the same vegetables. When vegetable disks
were inoculated with Salmonella and co-inoculated with Salmonella and a soft rot bacterium, disks that were co-inoculated contained
approximately 10 times the number of Salmonella as the disks that contained only Salmonella. Many studies (Robbs et al., 1996; Sherman and
Allen, 1983; Segall et al., 1977; Bartz and Kelman, 1986; Lund and Kelman; 1977) have shown that vegetables such as celery, potatoes,
peppers, and tomatoes are particularly susceptible to bacterial soft rot. Studies have shown that packinghouse procedures such as fluming and
dump tanks can increase the incidence of soft rot (Segall et al., 1977; Lund and Kelman, 1977), while chemical treatments, including chlorination
of water, appear to reduce the incidence of soft rot (Sherman and Allen, 1983; Bartz and Kelman, 1986).
Insects, birds, and dust can act as vectors for plant and human pathogens, especially after fruits and vegetables have been injured (Beuchat,
1996). Houseflies have been found to harbor 100 different pathogens and have been shown to transmit 65 of these pathogens (Kettle, 1982).
Human pathogens that have been isolated from houseflies include Campylobacter jejuni, Entamoeba histolytica, pathogenic E.
coli, Salmonella typhimurium, Shigella spp., and Vibrio cholera O139 (Olsen, 1998). Michailides and Spotts (1990) found that
vinegar flies and nitidulid beetles in peach and nectarine orchards were contaminated with plant pathogens and transferred them
to 75 – 100 percent of injured fruit studied. Beetles were found to transfer the plant pathogens to uninjured fruit also, which
caused fruit rot on 42 – 75 percent of the uninjured fruit.
Numerous studies have shown that insects and birds can carry the human pathogen E. coli O157:H7 (Janisiewicz et al., 1999;
Iwasa et al., 1999; Shere et al., 1998; Rahn et al., 1997; Wallace et al., 1997). Iwasa et al. (1999) conducted a field study that found
contamination of wild house flies on a cattle farm with E. coli O157:H7 which persisted over a 3-month study period; a likely source
of the contamination was the cow manure that the flies were frequenting. In a controlled study, Janisiewicz and coworkers (1999) studied the
potential for fruit flies to transmit E. coli O157:H7 to wounds on apples. Contact between flies inoculated with the pathogen and apples with
surface wounds resulted in a high incidence of wounds contaminated with E. coli O157:H7.
Several studies have indicated that processing procedures may contribute to the microbial contamination of fruits and vegetables. A study on
high-pressure washing of citrus has suggested that spray washing does not generally cause visible damage to sound fruit but will rupture fruit
that has been previously physically damaged (Petracek et al., 1998). Although spray washing does not appear to compromise sound fruit, there
is suggestive evidence that microorganisms can be internalized into intact fruit in a dump tank. A team of FDA scientists performed a study to
assess the potential for intact oranges and grapefruit to internalize bacteria from contaminated water, using dye to represent bacteria (Merker et
al., 1999). This potential internalization of pathogens from contaminated water can occur if fruit is placed in a hydrocooler or a dump tank, and
also may occur on the tree during a heavy rain. The study demonstrated that infiltration of water into what appears to be intact fruit can occur. All
fruit used in this study was stringently culled prior to use so that it was representative of fruit used for juicing in operations with rigorous pre-
sorting systems. Uptake occurred most often when warm fruit was placed into cold water, so that the resulting pressure differential favored
uptake. However, there was evidence of low levels of dye uptake in grapefruit even when there was no temperature differential. Grapefruit were
generally more susceptible to infiltration than oranges. In most cases, dye was taken up through natural structures, e.g., the stem scar on fruit,
but occasionally an older puncture wound that appeared to be "healed" served as the route of entry.
Buchanan and coworkers (1999) also studied the susceptibility of apples to waterborne contamination. They found that when
warm apples were submerged in colder water contaminated with E. coli O157:H7, as might occur in processing operations where
flume water or dump tanks are not hygienically maintained, the pathogen was occasionally internalized. These results were
confirmed with dye studies in which 6 percent of warm apples immersed in cold dye solution internalized dye through open channels leading from
the blossom end into the core region. Zhuang and coworkers (1995) found that tomatoes took up higher numbers of cells of Salmonella spp.
from an aqueous environment when placed in water that was 15°C cooler than the tomatoes. Showalter (1979) and Bartz and Showalter (1981)
found that when tomatoes were dipped into water that was colder than the fruit, creating a negative temperature differential, tomatoes took up 1
to 4 percent of the fruit weight in water from the environment; most of the water uptake appeared to be in the vascular area beneath the stem
scar. In addition to the temperature differential, Bartz (1982) has shown that, with tomatoes, the amount of water uptake from the environment is
partially dependent upon the depth of submersion of the fruit. The author found that infiltration of tomatoes was influenced by both the
temperature differential phenomenon and hydrostatic pressure; there was a positive correlation between water uptake and depth of submersion.
Several studies have shown that cross contamination of products can occur from processing equipment and the processing environment.
Eisenberg and Cichowicz (1977) noted that tomato and pineapple products can become contaminated with the mold Geotrichum candidum Link,
which builds up on food contact equipment in processing plants. The authors stated that the occurrence of this mold in products can be directly
related to in-plant sanitation. A survey of citrus firms in Florida (Eisenberg, 1976) found insignificant levels of Geotrichum in orange juice and
grapefruit juice samples.
Data from studies on apples suggest that microorganisms can be spread within processing areas and can accumulate on
processing equipment. Preliminary research at the FDA Apple Cider pilot plant in Placerville, CA, has confirmed the importance of
sanitation, as one component of an overall safety strategy, in the production of quality apple juices and ciders (Keller et al., 1999). The study
was undertaken to determine the quality of juice produced when little or no clean-up or sanitation of the equipment or facilities was done. In
addition, apples used were not all of good quality and no culling was performed. Typical juices made under poor conditions with poor quality fruit
resulted in aerobic microbial populations of over 5 logs per ml, despite initial levels on incoming apples of only 3 logs per gram (Keller et al.,
Environmental sampling also was conducted as part of the FDA Apple Cider pilot study in Placerville, CA. Environmental sampling done at the
beginning and end of each day for a week repeatedly demonstrated high APC counts on the conveyor belt, floor drains, hand-wash stations, the
hammer mill, and on tubing used to pump pomace to the press. Air sampling was also done and showed that microorganisms can be distributed
throughout a plant via aerosols that occur during clean-up and processing (Keller et al., 1999).
The State of Maryland conducted a study to determine existing manufacturing and sanitation practices among cider producers (Senkel et al.,
1999). Subsequently, these cider producers were trained in safety issues, HACCP concepts and principles, sanitation procedures, and GMPs.
Microbiological evaluation of in-line apples, pomace, and cider before bottling, and cider bottled before and after training was performed to
determine the effectiveness of training. No pathogens were found in any of the samples. However, generic, non-pathogenic E. coli was found in
13% of in-line samples and 18% of cider samples, but not on the exterior of incoming apples. This suggests that E. coli was introduced during in-
plant processing and highlights the importance of appropriate sanitation practices in juice production.
Carter (1989) noted that sanitation is important in the production of fresh-squeezed orange juice because microorganisms from the peel and
equipment can instantly begin reproducing in the juice under favorable conditions. Contamination by airborne microflora can result in growth of
colonies that, after several hours of extraction operation, are sufficient to cause serious quality problems in fresh orange juice.
Pathogen Survival in Fruits and Vegetables and Juices
A pathogen that has become internalized within a fruit or vegetable must be able to survive in the product until it reaches the consumer in order
to become a public health hazard. Pathogen survival depends on many factors, including the physical and chemical characteristics of the fruit or
vegetable, the postharvest processes applied, and consumer handling. In a market basket survey, Samish et al (1963) frequently found
bacteria in tomatoes, cucumbers, peas, and beans, and less often in melons and bananas. Bacteria were rarely found in grapes, citrus
fruit, olives and peaches. Several studies have shown that human pathogens can survive and grow in tomatoes and tomato
products (Zhuang et al., 1995; Zhuang and Beuchat, 1996; Tsai and Ingham, 1997). Asplund and Nurmi (1991) have demonstrated that cut
tomatoes can be a vector of Salmonella contamination. Golden and coworkers (1993) found that Salmonella grew rapidly on cut surfaces of
cantaloupe, watermelon, and honeydew melon that were held at room temperature. Salmonella levels remained unchanged when the melons
were held at refrigerated temperatures.
Fisher and Golden (1998) studied the survival of E. coli O157:H7 in different cultivars of ground apples stored at various
temperatures. Although there were differences in population reduction, E. coli O157:H7 survived in all samples during storage. At
refrigeration temperatures, the pathogen survived in all cultivars studied for 18 days before visible mold spoilage occurred.
Survival of E. coli O157:H7 is enhanced when product is stored at refrigeration, rather than room, temperature.
Little published information is available on the natural occurrence of human pathogens in fruit. However, other microorganisms have been
studied. Hill and Faville (1951) inoculated citrus fruit on the tree with Aerobacter, Xanthomonas, and Achromobacter and found that there was a
3-log increase in bacterial numbers over 5 weeks. The authors also found that one control fruit (not inoculated) had an unusually high count of
yeast and molds (7,600,000 colony forming units (cfu)/ml). All other control fruit had an average count of yeast and molds of 50 cfu/ml over the
study period. The authors noted that all control fruits appeared to be sound, including the one with unusually high counts. If control fruit,
including the highly contaminated fruit, were used to make juice, the juice would have contained a count of 50,000 cfu/ml of yeast and molds.
The authors stressed that the external appearance of the inoculated fruit gave little indication of the high counts that were present and would
seldom be rejected by experienced graders.
Pao and Brown (1998) studied human pathogens associated with the surface of citrus. The study found no pathogenic bacteria of concern in
packed fresh citrus fruit samples from seven commercial packinghouses. They also found no generic E. coli on fruit at the end of packinghouse
procedures (dumping, washing, waxing, and hand packing), and no Salmonella at any point in the packinghouse procedure.
Several studies have demonstrated the survival of microorganisms, including human pathogens, in various juices. Miller and
Kaspar (1994), Fratamico et al (1997), and Splittstoesser and coworkers (1996) found that E. coli O157:H7 survives in apple juice
for up to 24 days at 4° C. Fisher and Golden (1998) noted that, when dropped apples were used to produce cider, the pH of the
cider was increased by mold growth enough to allow slow growth of E. coli O157:H7 at room temperature.
Studies have also been conducted on the survival of microorganisms in orange juice. In a technical manual developed for the fresh-squeezed
Florida orange juice industry, Carter (1989) noted that Lactobacillus and Leuconostoc and certain yeast and molds are considered normal
microflora for fresh orange juice and stated that the presence of microorganisms in numbers in the juice establishes the difference between
processed orange juice and fresh orange juice. Carter also stated that counts of 200,000 cfu/ml in fresh juice, as measured on orange serum
agar, at time of packaging should be considered a practical maximum at high-temperature times of the year in order to avoid quality problems in
the juice. Parish (1997) included, in a review of juice outbreaks, information on general microflora levels of orange juice made from fruit of
various qualities. Juice made from sound fruit contained an average of 500 cfu/ml of juice, from dropped fruit an average of 15,000 cfu/ml of
juice, from split fruit an average of 1,710,000 cfu/ml of juice, and from deteriorated fruit an average of 6,150,000 cfu/ml of juice. Fratamico and
coworkers (1997) found that E. coli O157:H7 survived in orange juice for 24 days at refrigeration temperatures with very little
decrease in numbers. Parish and Higgins (1989) showed that Listeria numbers declined approximately 6 logs in orange juice in 25
days at pH 3.6 and 43 days at pH 4.0 when stored at 4° C.
A May 1998 survey conducted by the Florida Department of Agriculture and Consumer Services in May 1998 of 210 small fresh juice
processors found that 4 percent of samples (383 total samples) were positive for generic E. coli, indicating recent fecal
contamination (Food and Drug Administration Docket # 97N-0511, Comment # 107). The survey included gift fruit shippers, small
markets, retail outlets, and juice bars.
Although it has been shown that pathogens can survive in orange juice, Parish (1998) has stated that Salmonella and Listeria do
not actively grow in orange juice when the pH is below 4.4. Data has been submitted to the docket of FDA's juice HACCP rule indicating
that E. coli O157:H7 and Listeria do not survive in lemon and lime juices when stored at room temperature (Food and Drug Administration
Docket # 97N-0511, Comment # 133).
Efficacy of Surface Interventions
Several studies have shown that surface treatments are ineffective in reducing microbial populations that have been internalized into produce.
Zhuang and Beuchat (1996) demonstrated that a 15 percent solution of trisodium phosphate will completely inactivate Salmonella on the surface
of tomatoes but will only result in a 2-log reduction (starting concentration = 5.5 logs) of internal populations. Pao and Davis (1999) found that
immersing inoculated oranges in hot water or various chemical solutions (200 ppm chlorine, 100 ppm chlorine dioxide, 200 ppm acid anionic
sanitizer, 80 ppm peroxyacetic acid, or 2% trisodium phosphate) was effective at reducing generic E. coli populations by 1.8 – 3.1 log cycles on
surface areas except for the stem scar. Tested treatments reduced stem scar populations by about 1.0 log.
Published and unpublished information relevant to the subject of microbial infiltration and survival in produce has demonstrated that, under
certain conditions, microorganisms can become internalized into fruits and vegetables, including citrus fruits, and can survive in that
environment. Water, insects or birds, all of which may carry human pathogens, may serve as vectors resulting in the contamination of damaged
or decayed sites on the rind. Microorganisms subsequently may infiltrate the produce through these damaged sites. In addition, fruit can become
contaminated if warm fruit is submerged into cold, contaminated water or if vulnerable external points of fruit are immersed in contaminated
water. Under certain conditions, equipment also has been shown to cross contaminate both fresh apple and orange juice during processing.
Survival of pathogens, both plant and human, has been demonstrated in both produce and juice. In laboratory studies, human
pathogens have been found in or on tomatoes, cantaloupe, watermelon, honeydew melon, and apples. There appears to be no
published information on human pathogens in citrus fruits; however, the presence of other bacteria internalized in citrus was
noted. Numerous studies have shown that human pathogens can survive in both apple and orange juice, despite their natural
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