Preharvest Internalization of  O157:H7 into Lettuce Leaves, as Affected by Insect and Physical Damage

Erickson, Marilyn C.; Liao, Jean; Payton, Alison S.; Riley, David G.; Webb, Cathy C.; Davey, Lindsey E.; Kimbrel, Sophia; Ma, Li; Zhang, Guodong; Flitcroft, Ian D.; Doyle, Michael P.; Beuchat, Larry R.

doi:10.4315/0362-028x-73.10.1809

Cited by 29 publications

(34 citation statements)

References 38 publications

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“…Insect honeydew is an aqueous solution consisting of various sugars and amino acids and constitutes a significant nutrient source and growth medium that could ultimately increase the survival of bacteria on the plant surface (23,46,48). In an ongoing set of replicated experiments, an approximate 2-log increase in concentrations of S. enterica was observed when the bacterial suspension was amended with honeydew collected from M. quadrilineatus and cultured overnight (J. P. Soto-Arias, unpublished data).…”

Section: Discussionmentioning

confidence: 99%

Transmission and Retention of Salmonella enterica by Phytophagous Hemipteran Insects

Soto-Arias

Groves

Barak

2014

Appl Environ Microbiol

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Several pest insects of human and livestock habitations are known as vectors of Salmonella enterica; however, the role of plantfeeding insects as vectors of S. enterica to agricultural crops remains unexamined. Using a hemipteran insect pest-lettuce system, we investigated the potential for transmission and retention of S. enterica. Specifically, Macrosteles quadrilineatus and Myzus persicae insects were fed S. enterica-inoculated lettuce leaf discs or artificial liquid diets confined in Parafilm sachets to allow physical contact or exclusively oral ingestion of the pathogen, respectively. After a 24-h acquisition access period, insects were moved onto two consecutive noninoculated leaf discs or liquid diets and allowed a 24-h inoculation access period on each of the two discs or sachets. Similar proportions of individuals from both species ingested S. enterica after a 24-h acquisition access period from inoculated leaf discs, but a significantly higher proportion of M. quadrilineatus retained the pathogen internally after a 48-h inoculation access period. S. enterica was also recovered from the honeydew of both species. After a 48-h inoculation access period, bacteria were recovered from a significantly higher proportion of honeydew samples from M. quadrilineatus than from M. persicae insects. The recovery of S. enterica from leaf discs and liquid diets postfeeding demonstrated that both species of insects were capable of transmitting the bacteria in ways that are not limited to mechanical transmission. Overall, these results suggest that phytophagous insects may serve as potential vectors of S. enterica in association with plants.

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Section: Discussionmentioning

confidence: 99%

Transmission and Retention of Salmonella enterica by Phytophagous Hemipteran Insects

Soto-Arias

Groves

Barak

2014

Appl Environ Microbiol

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“…In comparison with other studies on the survival of these pathogens on fresh produce (e.g., Aruscavage et al, 2008;Brandl and Amundson, 2008;Erickson et al, 2010a), we used growing butterhead lettuce plants cultivated under realistic northern European lettuce production conditions. The experiments were performed under the controlled conditions of a growth chamber, but in parallel an experiment in the greenhouse was made to evaluate whether the investigated factors are also important under conditions of current practice.…”

Section: Discussionmentioning

confidence: 99%

“…In other instances, Fisher's Least Significant Difference post-hoc comparisons were made with the combinations of the groups. Values below the detection limit were considered to be at the detection limit (1.3 log CFU/g) if the enrichment was positive, whereas those testing negative by enrichment culture were assigned a value of 0.0 as described by Erickson et al (2010a).…”

Section: Statistical Analysesmentioning

confidence: 99%

“…Irrigation water is considered a potentially important introduction route, and several studies have shown its potential for the transmission of enteric pathogens to lettuce plants. However, most of these studies were conducted either under laboratory or controlled conditions in growth chambers (Brandl and Mandrell, 2002;Solomon et al, 2003;Aruscavage et al, 2008;Aruscavage et al, 2010;Brandl and Amundson, 2008;Zhang et al, 2009;Erickson et al, 2010a) or field experiments (Barker-Reid et al, 2009;Erickson et al, 2010b;Harapas et al, 2010;Wood et al, 2010;Fonseca et al, 2011). Few studies have compared both types of experimental setups.…”

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confidence: 99%

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Survival of Enteric Pathogens During Butterhead Lettuce Growth: Crop Stage, Leaf Age, and Irrigation

Linden¹,

Cottyn²,

Uyttendaele

et al. 2013

Foodborne Pathogens and Disease

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The survival of Salmonella enterica serovar Thompson and Escherichia coli O157 was investigated on growing butterhead lettuce plants in the plant-growth chamber and greenhouse. All inoculation tests were made under conditions that approximate the greenhouse conditions for butterhead lettuce cultivation in Flanders (Belgium). The survival and proliferation of the pathogens on the leaves was determined at days 0, 4, and 8 after inoculation using standard plating techniques on selective medium. In the growth chamber, the extent to which both pathogens were able to multiply on the lettuce leaves was influenced by crop stage and leaf age. On young plants, the older leaves supported pathogen survival better. On nearly mature plants, pathogen population sizes were significantly higher on the old and young leaves compared with middle-aged leaves ( p < 0.001). In the greenhouse, the environmental regimen with high fluctuations in temperature and relative humidity was less conducive to the survival of E. coli O157, though its survival on nearly mature lettuce was enhanced by overhead irrigation. The moist conditions between the folded inner leaves are likely contributing to the survival of enteric pathogens in the lettuce head. Butterhead lettuce grown in greenhouses with a sprinkle irrigation system may present a potential health hazard when contaminated near harvest. Experimental design (growth chamber versus greenhouse) largely influences enteric pathogen behavior on growing lettuce plants.

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“…For example, naturally occurring mutants of E. coli O157:H7 lacking stx genes (encoding Shiga toxins) and containing a plasmid-borne green fluorescent protein have been used in field experiments to assess the effects of irrigation types and exposure to sunlight on the ability of the pathogen to colonize specific sites on plants and to persist on crops (18)(19)(20). In the United States, attenuated Salmonella strains have been used in only a few field studies (15).…”

mentioning

confidence: 99%

Development of an Avirulent Salmonella Surrogate for Modeling Pathogen Behavior in Pre- and Postharvest Environments

Moraes

Chapin

Ginn³

et al. 2016

Appl Environ Microbiol

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Recurrent outbreaks of bacterial gastroenteritis linked to the consumption of fresh fruits and vegetables highlight the paucity of understanding of the ecology of Salmonella enterica under crop production and postharvest conditions. These gaps in knowledge are due, at least in part, to the lack of suitable surrogate organisms for studies for which biosafety level 2 is problematic. Therefore, we constructed and validated an avirulent strain of Salmonella enterica serovar Typhimurium. The strain lacks major Salmonella pathogenicity islands SPI-1, SPI-2, SPI-3, SPI-4, and SPI-5 as well as the virulence plasmid pSLT. Deletions and the absence of genomic rearrangements were confirmed by genomic sequencing, and the surrogate behaved like the parental wildtype strain on selective media. A loss-of-function (phoN) selective marker allowed the differentiation of this strain from wildtype strains on a medium containing a chromogenic substrate for alkaline phosphatase. Lack of virulence was confirmed by oral infection of female BALB/c mice. The strain persisted in tomatoes, cantaloupes, leafy greens, and soil with the same kinetics as the parental wild-type and selected outbreak strains, and it reached similar final population levels. The responses of this strain to heat treatment and disinfectants were similar to those of the wild type, supporting its potential as a surrogate for future studies on the ecology and survival of Salmonella in production and processing environments. IMPORTANCEThere is significant interest in understanding the ecology of human pathogens in environments outside of their animal hosts, including the crop production environment. However, manipulative field experiments with virulent human pathogens are unlikely to receive regulatory approval due to the obvious risks. Therefore, we constructed an avirulent strain of S. enterica serovar Typhimurium and characterized it extensively. O utbreaks of human disease caused by nontyphoidal Salmonella enterica have been linked to sprouts, fruits, vegetables, and nuts that were contaminated at various points in the production cycle (1-8). Generic Escherichia coli indicator levels are currently monitored to ensure the safety of produce; however, the persistence of Salmonella on the surfaces of peaches, cantaloupes, lettuce, and bell peppers has been shown to be very different from that of E. coli (9, 10). In general, Salmonella survives better outside of its animal hosts than E. coli (11) and can persist in processed organic waste and amended soils better than fecal coliforms, although its persistence appears to be strain and/or site dependent (12-14).There is significant interest in understanding the ecology of specific pathogens in the environment outside of their animal hosts. However, field experiments with virulent human pathogens are unlikely to receive regulatory approval due to the obvious risks associated with environmental exposure. Surrogate organisms have been used to better understand how human pathogens survive in environments and respond to...

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Preharvest Internalization of O157:H7 into Lettuce Leaves, as Affected by Insect and Physical Damage

Cited by 29 publications

References 38 publications

Transmission and Retention of Salmonella enterica by Phytophagous Hemipteran Insects

Transmission and Retention of Salmonella enterica by Phytophagous Hemipteran Insects

Survival of Enteric Pathogens During Butterhead Lettuce Growth: Crop Stage, Leaf Age, and Irrigation

Development of an Avirulent Salmonella Surrogate for Modeling Pathogen Behavior in Pre- and Postharvest Environments

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