Following this morning's report of a new European study demonstrating the potential for internalization of Salmonella in produce, Ben Chapman pulled together the following notes on the topic.

Irrigation water containing raw sewage or improperly treated effluents from sewage treatment plants may contain hepatitis A, Norwalk viruses, or enteroviruses in addition to bacterial pathogens such as E.coli O157:H7, Salmonella spp. and Shigella spp. (Beuchat, 1998).

Produce can also be contaminated with pathogens due to internalization of pathogens both through the root system and flesh or stem scars. Evidence of infiltration of bacteria into vegetables is reported in several articles (Bartz 1982; Bartz and Showalter 1981; Burnett et al., 2000; Seo and Frank 1999; Zhuang et al., 1995). Clear evidence exists to conclude that pathogens can be incorporated into fresh produce. So far, this evidence is based on laboratory experiments, not actual real world situations. Past research suggests that pathogens can enter lettuce plants through its roots and end up in the edible leaves. Small gaps in growing roots through which plant pathogens infect tissue may also allow E. coli entry (Solomon et al, 2002b; Warriner et al., 2003a, Warriner et al., 2003b).

The uptake of Salmonella spp. by roots of hydroponically grown tomato plants has been shown. Within one day of exposure to a high concentration mixture of Salmonella spp. pathogen cells were found in the hypocotyls, cotyledons, stems and leaves of young plants; though whether fruit is affected is not known at this time (Guo et al., 2002).

Solomon and colleagues (2002a) discovered that the transmission of E.coli O157:H7 to lettuce was possible through both spray and drip irrigation. They also found that the pathogen persisted on the plants for 20 days following application and submerging the lettuce in a solution of 200ppm chlorine did not eliminate all viable E.coli O157:H7 cells. This suggests that irrigation water of unknown microbial quality should be avoided in lettuce production (Solomon et al., 2002a).  In a follow-up experiment, Solomon and colleagues (2002b) explored the transmission of E. coli O157:H7 from manure-contaminated soil and irrigation water to lettuce plants. The researchers recovered viable cells from the inner tissues of the lettuce plants and found that the cells migrated to internal locations in plant tissue and were thus protected from the action of sanitizing agents These experiments demonstrated that E. coli O157:H7 can enter the lettuce plant through the root system and migrate throughout the edible portion of the plant (Solomon et al., 2002b).

The risk of contamination of produce due to Salmonella spp. was found to be increased when soil and water were present, and that soil and water actually act as reservoirs of the pathogen. Xuan and colleagues (2002) found that soil and water were factors in the infiltration of salmonella into the tissues of tomato. This supports the theory that preharvest contact with contaminated soil or water increased the contamination potential by certain pathogens and can lead to problems in pathogen removal and the efficacy of sanitizers.

Flesh scarring can provide a suitable environment for pathogen growth, and decreases the value of employing sanitizers, either in the packing shed or by consumers (Xuan et al., 2002).

The uptake of Salmonella spp. by roots of hydroponically grown tomato plants has also been shown. Within one day of exposure to a high concentration mixture of Salmonella spp. pathogen cells were found in the hypocotyls, cotyledons, stems and leaves of young plants; though whether fruit is affected is not known at this time (Guo et al., 2002).

In a 2006 review, Vectors and conditions for preharvest contamination of fruits and vegetables with  pathogens capable of causing enteric diseases,  Larry Beuchat of the Center for Food Safety and Department of Food Science and Technology at the University of Georgia, concluded:

"Manure, manure compost, sewage, sludge, irrigation water, and runoff water represent
avenues for introduction of pathogenic bacteria, parasites, and viruses to soil in which
fruits and vegetables intended to be eaten raw are grown. Pathogens vary in their
ability to survive in soil amendments and in soil. Inactivation rates and persistence in
soil are also influenced by soil type, rainfall, temperature, and agronomic practices.
Some pathogens can survive in soil for periods of time exceeding those needed to grow
plants from seeds or seedlings to the point of harvest. Pathogens originating from
preharvest environments may contaminate the surface of produce and evidence is
mounting that contamination of internal tissues can also occur. Prevention of
preharvest contamination of fruits and vegetables is an essential part of a systems
approach focused on applying interventions designed to achieve delivery of
microbiologically safe produce to the consumer."

References

Bartz, J.A. 1982. Infiltration of tomatoes immersed at different temperatures to different depths in suspensions of Erwinia carotovora subsp. carotovora. Plant Disease. 66:302-305.

Bartz, J.A., and R.K. Showalter. 1981. Infiltration of tomatoes by aqueous bacterial suspensions. Phytopathology. 71: 515-518.

Beuchat, 2006. Vectors and conditions for preharvest contamination of fruits and vegetables with  pathogens capable of causing enteric diseases. British Food Journal 108 (1): 38-53.

Beuchat, L.R. 1998. Surface decontamination of fruits and vegetables eaten raw: a review. WHO/FSF/FOS/Publication 98.2. World Health Organization. Geneva. 49pp.

Burnett, S.L., Chen. J. and Beuchat, L.R. 2000. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Applied and Environmental Microbiology. 66: 4679-4687.

Guo, X., van Iersel, M. W., Chen, J., Brackett, R. E. and Beuchat, L. R. 2002. Evidence of association of salmonellae with tomato plants grown hydroponically in inoculated nutrient solution. Applied  Environmental Microbiology. 68: 3639-3643.

Hedberg, C.W., Angulo, F.J., White, K.E., Langkop, C.W., Schell, W.L., Stobierski M.G., Schuchat, A., Besser, J.M., Dietrich, S., Helsel, L., Griffin, P.M., McFarland J.W. and Osterholm M.T. 1999. Outbreaks of salmonellosis associated with eating uncooked tomatoes: implications for public health. Epidemiology and Infection 122: 385-93.

Seo, K. H., and J. F. Frank. 1999. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. Journal of Food Protection.  62: 3-9.

Solomon, E. B., Yaron, S., and Matthews, K.R. 2002b. Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Applied Environmental Microbiology. 68: 397-400.

Solomon, E.B., ,Potenski, C.J. and Matthews, K.R. 2002a. Effect of irrigation method on transmission to and persistence of Escherichia coli O157:H7 on lettuce. Journal of Food Protection. 65: 673–676.

Warriner K., Ibrahim F., Dickinson M,. Wright C. and Waites W.M. 2003a. Internalization of human pathogens within growing salad vegetables. Biotechnology & Genetic Engineering Reviews.  20: 117-134.

Warriner K., Ibrahim F., Dickinson M,. Wright C. and Waites W.M. 2003b. Interaction of Escherichia coli with growing salad spinach plants. Journal of Food Protection. 66: 1790-1797.

Xuan, G., Jinru, C., Brackett, R.E., Beuchat, L.R. 2002. Survival of salmonella on tomatoes stored at high relative humidity, in soil, and on tomatoes in contact with soil. Journal of Food Protection. 65: 274-279.

Zhuang, R.-Y., Beuchat, L.R. and Angulo. F.J. 1995. Fate of Salmonella montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Applied Environmental Microbiolology. 61: 2127-2131.

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