International salmonellosis outbreaks associated with fresh produce.
Abstract
Fruits and vegetables are important for a healthy diet. However, when eaten raw and contaminated with human pathogens (HPs) they may cause a disease outbreak. Contamination with HPs can occur along the entire farm-to-fork production chain and Salmonella enterica is one of the most common foodborne pathogens. A range of biotic and abiotic environmental factors can influence the complex interactions between Salmonella and plants. Moreover, the outcome of experiments largely depends on the experimental design and parameters or methods employed, and on top, on the accompanying plant microbiome and the genetic equipment of the plant and the Salmonella strain. Particularly mobile genetic elements contribute to the diversification and adaptation of Salmonella to the plant environment. So far, little is known about the key processes and factors influencing the attachment and potential internalization of Salmonella in plants and the plant specific responses. It is therefore important to better understand the ecology of Salmonella in the soil and plant environment, in order to propose practicable recommendations for prevention of foodborne diseases. This also requires improved sensitivity and specificity of detection methods. In this chapter, we present the current knowledge, research needs, and methodology regarding the complex interactions between Salmonella and plants.
Keywords
- Salmonella enterica
- plant
- biofilm
- colonization mechanisms
- interaction
1. Introduction
The natural microbiome of plants includes a wide diversity of microorganisms and is a key determinant of plant health and productivity, e.g., by supporting the uptake of mineral nutrients in roots or suppressing pathogen growth and inducing the host‐immune system [1–3]. Due to its relevance, the plant microbiome (totality of microorganisms associated with the plant) is even called the second plant genome. Because of the tight interplay between plants and their epiphytic and endophytic microorganisms the terms holobiont and meta‐organisms are used as well. The plant microbiome is important not only for plant growth and health, but is also positively influencing human health [4]. However, besides positive effects on human health plants can also be carriers of bacterial HPs.
2. Contamination of fresh produce
Besides contaminated animal products,
Organic fertilizers like manure, biogas plant digestates and sewage sludge offer an additional route for contamination of fresh produce. Similarly, animals like birds, game, mice, or insects can contribute to the contamination of fresh produce directly or indirectly via feces or irrigation water [7, 14, 20]. Often underestimated are soil particles, which can be carried by the wind over long distances and contribute to the transient of microbiome between plants [8]. Hence, wind‐caused spread of HPs should also be considered. Contaminated plant residues might constitute additional risk if incorporated into soil before the planting of next crop. The infection of plants is essentially dependent on the ability of HPs to survive and persist in the agricultural environment.
Contamination of fresh produce with HPs like
3. Epidemiology of Salmonella in agricultural systems
Fresh produce contaminated with
Vector | Year | Country | Cases/serovar confirmed | Reference | |
---|---|---|---|---|---|
Tomatoes | 2015 | USA | 115/81 | [112] | |
Cucumbers | 2015‐16 | USA | 907/907 | [113] | |
Unknown | Onions, tomatoes | 2015 | USA | 200/0 | [114] |
Sprouts, beans |
2014 | USA | 115/0 | [113] | |
Cucumbers | 2014 | USA | 275/0 | [113] | |
Cantaloupe | 2012 | USA | 261/261 | [115] | |
Mangoes | 2012 | USA, Canada | 127/0 | [113] | |
Mung beans | 2011 | Germany Netherlands | 106/32 | [116] | |
Unknown | Produce‐based salads, broccoli salad | 2011 | Japan | 1500/0 | [117] |
Fruit, papaya | 2011 | USA | 106/0 | [113] | |
Vegetables, sprouts, alfalfa sprouts | 2010 | USA | 140/0 | [118] | |
Vegetables, leafy greens, lettuce fruit, tomatoes, olives | 2010 | USA | 114/108 | [119] |
Although fruits and vegetables were identified as source of human pathogens, it is not clear whether the plants were colonized in the field or during processing.
4. Factors influencing the survival of Salmonella in soil
Successful establishment of human pathogenic bacteria in soil depends on a variety of biotic and abiotic factors (see Figure 1 for an overview). Numerous studies, carried out under different conditions, showed that among them are weather or atmospheric conditions like temperature, UV radiation, and moisture content of the soil [7, 35]. In general, temperature has an important effect on growth and decay rates of bacteria. Most studies examined the influence of temperature on survival of enteric bacteria under isothermal conditions, showing a generally reduced survival of
The soil microbial community and its composition have a great influence on the survival of
In addition to the environment in which
In conclusion, studies analyzing the survival of
5. Attachment to plant surfaces and biofilm formation
Attachment and adhesion of
Several other studies provided evidence for biofilm formation by
Although many factors influencing the colonization of plants were identified by
6. Internalization of Salmonella into plant tissues
An increasing number of salmonellosis outbreaks associated with plants shows that human pathogenic bacteria use plants as a niche for replication or as hosts and vectors for animal and human infection (Table 1). For a long time it was assumed that
From the consumers’ point of view, not only the internalization into leaves but also the translocation within the plant, e.g., toward fruits is important. In some crop plants, e.g., tomato, such translocation was detected [81]. The authors showed internalization into the tomato fruits when the entire plant was systemically colonized. Still, the colonization rates seemed rather low [81]. Nonetheless, in light of the persistent pathogenicity in animals after the passage through a plant host [84], the internalization mechanisms are of high interest. Some detailed mechanisms were already suggested. Erlacher and coworkers proposed one of those possible mechanisms: colonization of the niche below the cuticle layer of the epidermis [9]. Obviously such a behavior protects bacteria from the harsh conditions on the leaf surface (UV light, drought, and quick changes in temperature) but also from surface sterilization agents. Another strategy would be an intracellular lifestyle, which would resemble the strategy in the animal infection model. Until now, this possibility remains unverified, two reports postulated internalization into plant cells using
Many row eaten crop plants plants associated with salmonellosis outbreaks or food poisoning are usually grown in soil (lettuce, basil, parsley, etc.). In such cases the translocation from the potentially contaminated soil (through manure or irrigation water) via roots into the harvested and consumed plant parts is of enormous importance. Several reports assessed already this possibility and pointed at a very diverse picture with regard to pathogenic
7. The function of T3SS and the role of plant immune system during the interactions between plant and Salmonella
Bacterial pathogens use T3SS and T4SS to inject so‐called effector proteins directly into the cytoplasm of host cells. Those effectors are able to manipulate the host immune system and suppress the otherwise negative effects of defense responses.
8. Salmonella changes its physiology in contact with plant host
During the interaction between
9. Detection, characterization and quantification of Salmonella in environmental samples
Traditional methods for the detection and identification of HPs often rely on cultivation‐dependent techniques followed by biochemical and serological identification, which is typically time‐consuming and laborious [104]. Furthermore, in response to environmental stresses
So far, knowledge is scarce regarding the specific and reliable detection of
Microarrays and next‐generation sequencing technologies offer intriguing possibilities regarding the rapid and accurate detection as well as genetic characterization of
10. Conclusions
Today the notion that human pathogenic bacteria such as
Acknowledgments
The authors would like to apologize to all colleagues whose work was not cited due to space limitation. This work was supported by the German Federal Environment Agency (Umweltbundesamt; 371271209), the JKI, and the Federal Office for Agriculture and Food (Bundesanstalt für Landwirtschaft und Ernährung, BLE), Grants 13HS026 and 13HS029.
References
- 1.
Berendsen RL, Pieterse CM & Bakker PA. The rhizosphere microbiome and plant health. Trends Plant Sci 2012;17 :478–486. - 2.
Buee M, De Boer W, Martin F et al . The rhizosphere zoo: An overview of plant‐associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors.Plant Soil 2009;321 :189–212. - 3.
Turner TR, James EK & Poole PS. The plant microbiome. Genome Biol 2013;14 :10. - 4.
Berg G, Grube M, Schloter M et al . The plant microbiome and its importance for plant and human health.Front Microbiol 2014;5:491 . - 5.
Majowicz SE, Musto J, Scallan E et al . The global burden of nontyphoidalSalmonella gastroenteritis.Clin Infect Dis 2010;50 :882–889. - 6.
Brandl MT, Cox CE & Teplitski M. Salmonella interactions with plants and their associated microbiota. Phytopathology 2013;103 :316–325. - 7.
Brandl MT. Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 2006;44 :367–392. - 8.
Rastogi G, Sbodio A, Tech JJ et al . Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field‐grown lettuce.Isme Journal 2012;6 :1812–1822. - 9.
Erlacher A, Cardinale M, Grube M et al . Biotic stress shifted structure and abundance ofEnterobacteriaceae in the lettuce microbiome.PLoS ONE 2015;10 :e0118068. - 10.
van Overbeek LS, van Doorn J, Wichers JH et al . The arable ecosystem as battleground for emergence of new human pathogens.Front Microbiol 2014;5 :17. - 11.
Olaimat AN & Holley RA. Factors influencing the microbial safety of fresh produce: A review. Food Microbiol 2012;32 :1–19. - 12.
Allende A & Monaghan J. Irrigation water quality for leafy crops: A perspective of risks and potential solutions. Int J Environ Res Public Health 2015;12 :7457–7477. - 13.
Li B, Jackson SA, Gangiredla J et al . Genomic evidence reveals numerous Salmonella enterica serovar Newport reintroduction events in suwannee watershed irrigation ponds.Appl Environ Microbiol 2015;81 :8243–8253. - 14.
Jacobsen CS & Bech TB. Soil survival of Salmonella and transfer to freshwater and fresh produce.Food Res Int 2012;45 :557–566. - 15.
Barak JD & Liang AS. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS One 2008;3 :e1657. - 16.
Duffy EA, Lucia LM, Kells JM et al . Concentrations ofEscherichia coli and genetic diversity and antibiotic resistance profiling of salmonella isolated from irrigation water, packing shed equipment, and fresh produce in texas.J Food Protect 2005;1 :70–79. - 17.
Miles JM, Sumner SS, Boyer RR et al . Internalization ofSalmonella enterica serovar montevideo into greenhouse tomato plants through contaminated irrigation water or seed stock.J Food Protect 2009;4 :696–914. - 18.
Fonseca JM, Fallon SD, Sanchez CA et al . Escherichia coli survival in lettuce fields following its introduction through different irrigation systems.J Appl Microbiol 2011;110 :893–902. - 19.
Monaghan JM & Hutchison ML. Distribution and decline of human pathogenic bacteria in soil after application in irrigation water and the potential for soil‐splash‐mediated dispersal onto fresh produce. J Appl Microbiol 2012;112 :1007–1019. - 20.
Semenov AM, Kuprianov AA & van Bruggen AH. Transfer of enteric pathogens to successive habitats as part of microbial cycles. Microb Ecol 2010;60 :239–249. - 21.
Islam M, Morgan J, Doyle MP et al . Persistence of salmonella enterica serovar Typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water.Foodborne Pathog Dis 2004;1 :27–35. - 22.
You Y, Rankin SC, Aceto HW et al . Survival ofSalmonella enterica serovar Newport in manure and manure‐amended soils.Appl Environ Microbiol 2006;72 :5777–5783. - 23.
Acea MJ, Moore CR & Alexander M. Survival and growth of bacteria introduced into soil. Soil Biol Biochem 1988;20 :509–515. - 24.
Mallon CA, Elsas JD & Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol 2015;23 :719–729. - 25.
Mallon CA, Poly F, Le Roux X et al . Resource pulses can alleviate the biodiversity–invasion relationship in soil microbial communities.Ecol Soc Am 2015;96 :915–926. - 26.
Fierer N & Jackson RB. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 2006;103 :626–631. - 27.
Martiny JB, Bohannan BJM, Brown JH et al . Microbial biogeography: Putting microorganisms on the map.Nat Rev Microbiol 2006;4 :102–112. - 28.
Horner‐Devine MC, Lage M, Hughes JB et al . A taxa–area relationship for bacteria.Nature 2004;432 :750–753. - 29.
Suslow TV, Oria MP, Beuchat LR et al . Production practices as risk factors in microbial food safety of fresh and fresh‐cut produce.Compr Rev Food Sci Food Saf 2003;2 :38–77. - 30.
Hanning IB, Nutt JD & Ricke SC. Salmonellosis outbreaks in the united states due to fresh produce: Sources and potential intervention measures. Foodborne Pathog Dis 2009;6 :635–648. - 31.
Gu G, Cevallos‐Cevallos JM & van Bruggen AH. Ingress of Salmonella enterica Typhimurium into tomato leaves through hydathodes.PLoS One 2013;8 :e53470. - 32.
Guo X, Chen J, Brackett RE et al . Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening.Appl Environ Microbiol 2001;67 :4760–4764. - 33.
WBG. The economic impact of ebola on sub‐Saharan Africa: Updated estimates for 2015. 2015;1–17. - 34.
Butler D. The next time the world is ill‐prepared for the next epidemic or pandemic. But the horror of the ebola outbreak in West Africa may drive change. Nature 2015;524 :22–25. - 35.
Santamaría J & Toranzos GA. Enteric pathogens and soil: a short review. Int Microbiol 2003;6 :5–9. - 36.
Arrus KM, Holley RA, Ominski KH et al . Influence of temperature onSalmonella survival in hog manure slurry and seasonal temperature profiles in farm manure storage reservoirs.Livest Sci 2006;102 :226–236. - 37.
García R, Baelum J, Fredslund L et al . Influence of temperature and predation on survival ofSalmonella enterica serovar Typhimurium and expression ofinvA in soil and manure‐amended soil.Appl Environ Microbiol 2010;76 :5025–5031. - 38.
Semenov AV, van Bruggen AH, van Overbeek L et al . Influence of temperature fluctuations onEscherichia coli O157:H7 andSalmonella enterica serovar Typhimurium in cow manure.FEMS Microbiol Ecol 2007;60 :419–428. - 39.
Bernstein N, Sela S & Neder‐Lavon S. Effect of irrigation regimes on persistence of Salmonella enterica serovar Newport in small experimental pots designed for plant cultivation.Irrigation Sci 2007;26 :1–8. - 40.
Or D, Smets BF, Wraith JM et al . Physical constraints affecting bacterial habitats and activity in unsaturated porous media—a review.Adv Water Resour 2007;30 :1505–1527. - 41.
Holley RA, Arrus KM, Ominski KH et al . Salmonella survival in manure‐treated soils during simulated seasonal temperature exposure.J Environ Qual 2006;35 :1170–1180. - 42.
Bech TB, Johnsen K, Dalsgaard A et al . Transport and distribution ofSalmonella enterica serovar Typhimurium in loamy and sandy soil monoliths with applied liquid manure.Appl Environ Microbiol 2010;76 :710–714. - 43.
Horswell J, Hewitt J, Prosser J et al . Mobility and survival ofSalmonella Typhimurium and human adenovirus from spiked sewage sludge applied to soil columns.J Appl Microbiol 2010;108 :104–114. - 44.
Semenov AV, van Overbeek L & van Bruggen AH. Percolation and survival of Escherichia coli O157:H7 andSalmonella enterica serovar Typhimurium in soil amended with contaminated dairy manure or slurry.Appl Environ Microbiol 2009;75 :3206–3215. - 45.
Hutchison ML, Walters LD, Moore T et al . Fate of pathogens present in livestock wastes spread onto fescue plots.Appl Environ Microbiol 2005;71 :691–696. - 46.
Nicholson FA, Groves SJ & Chambers BJ. Pathogen survival during livestock manure storage and following land application. Bioresour Technol 2005;96 :135–143. - 47.
Hruby CE, Soupir ML, Moorman TB et al . Effects of tillage and poultry manure application rates onSalmonella and fecal indicator bacteria concentrations in tiles draining Des Moines Lobe soils.J Environ Manage 2016;171 :60–69. - 48.
Semenov AV, van Overbeek L, Termorshuizen AJ et al . Influence of aerobic and anaerobic conditions on survival ofEscherichia coli O157:H7 andSalmonella enterica serovar Typhimurium in Luria‐Bertani broth, farm‐yard manure and slurry.J Environ Manage 2011;92 :780–787. - 49.
Bennett DD, Higgins SE, Moore RW et al . Effects of lime onSalmonella enteritidis survival in vitro.J Appl Poult Res 2003;12 :65–68. - 50.
Ding GC, Radl V, Schloter‐Hai B et al . Dynamics of soil bacterial communities in response to repeated application of manure containing sulfadiazine.Plos One 2014;9 (3):e92958. - 51.
Franz E, van Diepeningen AD, de Vos OJ et al . Effects of cattle feeding regimen and soil management type on the fate ofEscherichia coli O157:H7 andSalmonella enterica serovar Typhimurium in manure, manure‐amended soil, and lettuce.Appl Environ Microbiol 2005;71 :6165–6174. - 52.
Moynihan EL, Richards KG, Brennan FP et al . Enteropathogen survival in soil from different land‐uses is predominantly regulated by microbial community composition.Appl Soil Ecol 2015;89 :76–84. - 53.
Goberna M, Podmirseg SM, Waldhuber S et al . Pathogenic bacteria and mineral N in soils following the land spreading of biogas digestates and fresh manure.Appl Soil Ecol 2011;49 :18–25. - 54.
Ge C, Lee C, Nangle E et al . Impact o f phytopathogen infection and extreme weather stress on internalization ofSalmonella Typhimurium in lettuce.Int J Food Microbiol 2014;168 –169 :24–31. - 55.
Caldwell KN, Anderson GL, Williams PL et al . Attraction of a free‐living nematode,Caenorhabditis elegans , to foodborne pathogenic bacteria and its potential as a vector ofSalmonella Poona for preharvest contamination of cantaloupe.J Food Protect 2003;66 :1964–1971. - 56.
Brandl MT, Rosenthal BM, Haxo AF et al . Enhanced survival ofSalmonella enterica in vesicles released by a soilborneTetrahymena species.Appl Environ Microbiol 2005;71 :1562–1569. - 57.
Cooley MB, Miller WG & Mandrell RE. Colonization of Arabidopsis thaliana withSalmonella enterica and enterohemorrhagicEscherichia coli O157:H7 and competition byEnterobacter asburiae .Appl Environ Microbiol 2003;69 :4915–4926. - 58.
Kroupitski Y, Golberg D, Belausov E et al . Internalization ofSalmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata.Appl Environ Microbiol 2009;75 :6076–6086. - 59.
Schikora M, Neupane B, Madhogaria S et al . An image classification approach to analyze the suppression of plant immunity by the human pathogenSalmonella Typhimurium .BMC Bioinformatics 2012;13 . - 60.
Gibson DL, White AP, Snyder SD et al . Salmonella produces an O‐antigen capsule regulated by AgfD and important for environmental persistence.J Bacteriol 2006;188 :7722–7730. - 61.
Vestby LK, Moretro T, Langsrud S et al . Biofilm forming abilities ofSalmonella are correlated with persistence in fish meal and feed factories.BMC Vet Res 2009;5 . - 62.
Lapidot A, Romling U & Yaron S. Biofilm formation and the survival of Salmonella Typhimurium on parsley.Int J Food Microbiol 2006;109 :229–233. - 63.
Wiedemann A, Virlogeux‐Payant I, Chausse AM et al . Interactions ofSalmonella with animals and plants.Front Microbiol 2014;5 :791. - 64.
Tan MSF, White AP, Rahman S et al . Role of fimbriae, flagella and cellulose on the attachment ofSalmonella Typhimurium ATCC 14028 to plant cell wall models.PLos One 2016;11 :13. - 65.
Yaron S & Romling U. Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol 2014;7 :496–516. - 66.
Ongeng D, Geeraerd AH, Springael D et al . Fate ofEscherichia coli O157:H7 andSalmonella enterica in the manure‐amended soil‐plant ecosystem of fresh vegetable crops: a review.Crit Rev Microbiol 2015;41 :273–294. - 67.
Berger CN, Shaw RK, Brown DJ et al . Interaction ofSalmonella enterica with basil and other salad leaves.ISME J 2009;3 :261–265. - 68.
Kroupitski Y, Pinto R, Belausov E et al . Distribution ofSalmonella Typhimurium in romaine lettuce leaves.Food Microbiol 2011;28 :990–997. - 69.
Klerks MM, Franz E, van Gent‐Pelzer M et al . Differential interaction ofSalmonella enterica serovars with lettuce cultivars and plant‐microbe factors influencing the colonization efficiency.ISME J 2007;1 :620–631. - 70.
Barak JD, Gorski L, Naraghi‐Arani P et al . Salmonella enterica virulence genes are required for bacterial attachment to plant tissue.Appl Environ Microbiol 2005;71 :5685–5691. - 71.
Klerks MM, van Gent‐Pelzer M, Franz E et al . Physiological and molecular responses ofLactuca sativa to colonization bySalmonella enterica serovar Dublin.Appl Environ Microbiol 2007;73 :4905–4914. - 72.
Steenackers H, Hermans K, Vanderleyden J et al . Salmonella biofilms: An overview on occurrence, structure, regulation and eradication.Food Res Int 2012;45 :502–531. - 73.
Gerstel U & Romling U. The csgD promoter, a control unit for biofilm formation inSalmonella Typhimurium.Res Microbiol 2003;154 :659–667. - 74.
Cevallos‐Cevallos JM, Gu G, Danyluk MD et al . Adhesion and splash dispersal ofSalmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density.Int J Food Microbiol 2012;160 :58–64. - 75.
Cevallos‐Cevallos JM, Gu G, Danyluk MD et al . Salmonella can reach tomato fruits on plants exposed to aerosols formed by rain.Int J Food Microbiol 2012;158 :140–146. - 76.
Barak JD, Gorski L, Liang AS et al . Previously uncharacterizedSalmonella enterica genes required for swarming play a role in seedling colonization.Microbiology 2009;155 :3701–3709. - 77.
Lapidot A & Yaron S. Transfer of Salmonella enterica serovar Typhimurium from contaminated irrigation water to parsley is dependent on curli and cellulose, the biofilm matrix components.J Food Prot 2009;72 :618–623. - 78.
Holmes A, Birse L, Jackson RW et al . An optimized method for the extraction of bacterial mRNA from plant roots infected withEscherichia coli O157:H7.Front Microbiol 2014;5 :286. - 79.
Golberg D, Kroupitski Y, Belausov E et al . Salmonella Typhimurium internalization is variable in leafy vegetables and fresh herbs.Int J Food Microbiol 2011;145 :250–257. - 80.
Barak JD, Kramer LC & Hao LY. Colonization of tomato plants by Salmonella enterica is cultivar dependent, and type 1 trichomes are preferred colonization sites.Appl Environ Microbiol 2011;77 :498–504. - 81.
Gu G, Hu J, Cevallos‐Cevallos JM et al . Internal colonization ofSalmonella enterica serovar Typhimurium in tomato plants.PLoS One 2011;6 :e27340. - 82.
Berg G, Erlacher A, Smalla K et al . Vegetable microbiomes: Is there a connection among opportunistic infections, human health and our ‘gut feeling’?Microb Biotechnol 2014;7 :487–495. - 83.
Erlacher A, Cardinale M, Grosch R et al . The impact of the pathogenRhizoctonia solani and its beneficial counterpartBacillus amyloliquefaciens on the indigenous lettuce microbiome.Front Microbiol 2014;5 :175. - 84.
Schikora A, Carreri A, Charpentier E et al . The dark side of the salad:Salmonella Typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle.PLoS One 2008;3 :e2279. - 85.
Shirron N & Yaron S. Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium .PLoS One 2011;6 :e18855. - 86.
Garcia AV, Charrier A, Schikora A et al . Salmonella enterica flagellin is recognized via FLS2 and activates PAMP‐triggered immunity inArabidopsis thaliana .Molecular Plant 2014;7 :657–674. - 87.
Gorbatsevich E, Sela Saldinger S, Pinto R et al . Root internalization, transport and in‐planta survival ofSalmonella enterica serovar Newport in sweet basil.Environ Microbiol Rep 2013;5 :151–159. - 88.
Erickson MC, Webb CC, Diaz‐Perez JC et al . Infrequent internalization ofEscherichia coli O157:H7 into field‐grown leafy greens.J Food Prot 2010;73 :500–506. - 89.
Bernstein N, Sela S & Neder‐Lavon S. Assessment of contamination potential of lettuce by Salmonella enterica serovar Newport added to the plant growing medium.J Food Prot 2007;70 :1717–1722. - 90.
Franz E, Visser AA, Van Diepeningen AD et al . Quantification of contamination of lettuce by GFP‐expressingEscherichia coli O157:H7 andSalmonella enterica serovar Typhimurium.Food Microbiol 2007;24 :106–112. - 91.
Niemann GS, Brown RN, Gustin JK et al . Discovery of novel secreted virulence factors fromSalmonella enterica serovar Typhimurium by proteomic analysis of culture supernatants.Infect Immun 2011;79 :33–43. - 92.
Hernandez‐Reyes C & Schikora A. Salmonella , a cross‐kingdom pathogen infecting humans and plants.FEMS Microbiol Lett 2013; 343(1):1–7. - 93.
Schikora A, Virlogeux‐Payant I, Bueso E et al . Conservation ofSalmonella infection mechanisms in plants and animals.PLoS One 2011;6 :e24112. - 94.
Ustun S, Muller P, Palmisano R et al . SseF, a type III effector protein from the mammalian pathogenSalmonella enterica , requires resistance‐gene‐mediated signalling to activate cell death in the model plantNicotiana benthamiana .New Phytol 2012;194 :1046–1060. - 95.
Neumann C, Fraiture M, Hernandez‐Reyes C et al . TheSalmonella effector protein SpvC, a phosphothreonine lyase is functional in plant cells.Front Microbiol 2014;5 :548. - 96.
Deiwick J, Salcedo SP, Boucrot E et al . The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche.Infect Immun 2006;74 :6965–6972. - 97.
Pitzschke A, Schikora A & Hirt H. MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 2009;12 :421–426. - 98.
Melotto M, Panchal S & Roy D. Plant innate immunity against human bacterial pathogens. Front Microbiol 2014;5 :411. - 99.
Deng X, Li Z & Zhang W. Transcriptome sequencing of Salmonella enterica serovar Enteritidis under desiccation and starvation stress in peanut oil.Food Microbiol 2012;30 :311–315. - 100.
Goudeau DM, Parker CT, Zhou Y et al . TheSalmonella transcriptome in lettuce and cilantro soft rot reveals a niche overlap with the animal host intestine.Appl Environ Microbiol 2013;79 :250–262. - 101.
Kyle JL, Parker CT, Goudeau D et al . Transcriptome analysis ofEscherichia coli O157:H7 exposed to lysates of lettuce leaves.Appl Environ Microbiol 2010;76 :1375–1387. - 102.
Crozier L, Hedley PE, Morris J et al . Whole‐transcriptome analysis of verocytotoxigenicEscherichia coli O157:H7 (Sakai) suggests plant‐species‐specific metabolic responses on exposure to spinach and lettuce extracts.Front Microbiol 2016;7: 1088. - 103.
Micallef SA, Rosenberg Goldstein RE, George A et al . Occurrence and antibiotic resistance of multiple Salmonella serotypes recovered from water, sediment and soil on mid‐Atlantic tomato farms.Environ Res 2012;114 :31–39. - 104.
Hein I, Flekna G, Krassnig M et al . Real‐time PCR for the detection ofSalmonella spp. in food: An alternative approach to a conventional PCR system suggested by the FOOD‐PCR project.J Microbiol Methods 2006;66 :538–547. - 105.
Park SH, Aydin M, Khatiwara A et al . Current and emerging technologies for rapid detection and characterization ofSalmonella in poultry and poultry products.Food Microbiol 2014;38 :250–262. - 106.
Mandal PK, Biswas AK, Choi K et al . Methods for rapid detection of foodborne pathogens: an overview.Am J Food Technol 2011;6 :87–102. - 107.
Law JWF, Ab Mutalib NS, Chan KG et al . Rapid methods for the detection of foodborne bacterial pathogens: principles, applications, advantages and limitations.Front Microbiol 2015;5 :19. - 108.
Zhao X, Lin CW, Wang J et al . Advances in rapid detection methods for foodborne pathogens.J Microbiol Biotechnol 2014;24 :297–312. - 109.
Vojkovska H, Kubikova I & Kralik P. Evaluation of DNA extraction methods for PCR‐based detection of Listeria monocytogenes from vegetables.Lett Appl Microbiol 2015;60 :265–272. - 110.
Blaser MJ & Newman LS. A review of human salmonellosis: I. Infective dose. Rev Infect Dis 1982;4 :1096–1106. - 111.
Nastasi A, Mammina C & Mioni R. Detection of Salmonella spp. in food by a rapid PCR‐hybridization procedure.Microbiologica 1999;22 :195–202. - 112.
MDH. Update: Tomatoes identified as source of Salmonella outbreak in restaurant chain. 2015. - 113.
CDC. Salmonella outbreaks. Available athttp://www.cdc.gov/Salmonella/outbreaks.html . Accessed July 2016:177–188. - 114.
CDHD. Health department investigating recent salmonella cases. 2015. - 115.
ISDH. Chamberlain farm produce, inc. 2012. - 116.
RKI. Salmonella Newport‐Ausbruch in Deutschland und den Niederlanden, 2011. Epidemiologisches Bulletin 2012;20 :177–188. - 117.
TJP. Available at http://www.japantimes.co.jp/news/2011/02/24/news/salads‐caused‐hokkaido‐food‐scare . Accessed July 2016. 2011. - 118.
FDH. Fei number 1000515256. 2011. - 119.
IDPH. Summary of S . ser. Hvittingfoss outbreak April‐June 2010. 2010.