1887

Chapter 12 : Shiga Toxin-Producing in Fresh Produce: A Food Safety Dilemma

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Shiga Toxin-Producing in Fresh Produce: A Food Safety Dilemma, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818791/9781555818784_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555818791/9781555818784_Chap12-2.gif

Abstract:

The worldwide trends for healthier lifestyles to reduce obesity and other complications arising from unhealthy diets have greatly increased the consumption of fresh fruits and vegetables. This increased demand, coupled with ever busier consumer lifestyles, also stimulated the growth of a “convenience” food industry and popularized the concept of bagged salad vegetables and fruits. It has been estimated that several millions of bags of fresh produce are sold daily in the United States. Bagged produce, also referred to as “fresh cut” or “precut,” is often regarded as ready-to-eat (RTE) and consumed without further intervention steps. However, because produce is predominantly cultivated in soil in open fields, it is susceptible to contamination and can contain high levels of complex microbial populations, occasionally including bacterial pathogens. As a result, increases in fresh produce demand and consumption coupled with changes in production practices have also contributed to increases in incidents of food-borne illness. In the United States, about 0.7% of the infections in the 1970s were attributed to fresh produce, but this increased to 6% in the 1990s ( ). Since “fresh cut” products are often mass produced, broadly distributed, and marketed worldwide, a single pathogen contamination event can have broadly impacting consequences, and several large, produce-related outbreaks have occurred in many countries ( ). In 2006, a large multistate outbreak in the United States that infected more than 200 persons was traced to bagged spinach contaminated with O157:H7 ( ). Several months later, another O157:H7 outbreak in a fast-food restaurant chain had initially implicated green onions but appeared to have been due to bagged lettuce. At about the same time, bagged lettuce was implicated in another O157:H7 outbreak that affected three states ( ). Likewise, increased consumption of sprouts caused several outbreaks of sp., O157:H7, and other Shigatoxin-producing (STEC) strains. STEC serotype O26:H11 strains caused an outbreak with alfalfa sprouts and, more recently, with clover sprouts, and the large outbreak of O104:H4 in 2011 in the European Union also implicated the consumption of sprouts ( ). These large produce-related outbreak incidents worldwide have greatly raised concerns about the safety of fresh produce and about the microbiological and sanitary quality of fresh produce.

Citation: Feng P. 2015. Shiga Toxin-Producing in Fresh Produce: A Food Safety Dilemma, p 245-259. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0010-2013
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555818791.chap12
1. Sivapalasingam S,, Friedman CR,, Cohen L,, Tauxe RV . 2004. Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67 : 23422353.[PubMed]
2. Lynch MF,, Tauxe RV,, Hedberg CW . 2009. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 137 : 307315.[PubMed] [CrossRef]
3. Berger CN,, Sodha SV,, Shaw RK,, Griffin PM,, Pink D,, Hand P,, Frankel G . 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 12 : 23852397.[PubMed] [CrossRef]
4. Centers for Disease Control and Prevention . 2006. Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach—United States, September 2006. Morb Mortal Wkly Rep 55 : 10451046.[PubMed]
5. Doyle MP,, Erickson MC . 2008. Summer meeting 2007—the problem with fresh produce: an overview. J Appl Microbiol 105 : 317330.[PubMed] [CrossRef]
6. Beutin L,, Martin A . 2012. Outbreak of Shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J Food Prot 75 : 408418.[PubMed] [CrossRef]
7. Johnston LM,, Jaykus LA,, Moll D,, Martinez MC,, Anciso J,, Mora B,, Moe CL . 2005. A field study of the microbiological quality of fresh produce. J Food Prot 68 : 18401847.[PubMed]
8. Johnston LM,, Jaykus LA,, Moll D,, Anciso J,, Mora B,, Moe CL . 2006. A field study of the microbiological quality of fresh produce of domestic and Mexican origin. Int J Food Microbiol 112 : 8395.[PubMed] [CrossRef]
9. Mukherjee A,, Speh D,, Jones AT,, Buesing KM,, Diez-Gonzalez F . 2006. Longitudinal microbiological survey of fresh produce grown by farmers in the upper Midwest. J Food Prot 69 : 19281936.[PubMed]
10. Soriano JM,, Rico H,, Moltó JC,, Mañes J . 2006. Assessment of the microbiological quality and wash treatments of lettuce served in University restaurants. Int J Food Microbiol 58 : 123128.[PubMed] [CrossRef]
11. Abadias M,, Usall J,, Anguera M,, Solsona C,, Viñas I . 2008. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 123 : 121129.[PubMed] [CrossRef]
12. Caponigro V,, Ventura M,, Chiancone I,, Amato L,, Parente E,, Piro F . 2010. Variation of microbial load and visual quality of ready-to-eat salads by vegetable type, season, processor and retailer. Food Microbiol 27 : 10711077.[PubMed] [CrossRef]
13. Fröder H,, Martins CG,, De Souza KL,, Landgraf M,, Franco BD,, Destro MT . 2007. Minimally processed vegetable salads: microbial quality evaluation. J Food Prot 70 : 12771280.[PubMed]
14. Hagenmeaier RD,, Baker RA . 1998. A survey of the microbial population and ethanol content of bagged salad. J Food Prot 61 : 357359.[PubMed]
15. Valentin-Bon I,, Jacobson A,, Monday S,, Feng P . 2008. Microbiological quality of bagged cut spinach and lettuce mixes. Appl Environ Microbiol 74 : 12401242.[PubMed] [CrossRef]
16. Kase JA,, Borenstein S,, Feng PCH . 2012. Microbial quality of bagged baby spinach and romaine lettuce—effects of top vs. bottom sampling. J Food Prot 75 : 132136.[PubMed] [CrossRef]
17. Sagoo SK,, Little CL,, Mitchell RT . 2003. Microbiological quality of open ready-to-eat salad vegetables: effectiveness of food hygiene training of management. J Food Prot 66 : 15811586.[PubMed]
18. Sospedra I,, Rubert J,, Soriano JM,, Mañes J . 2013. Survey of microbial quality of plant-based foods served in restaurants. Food Control 30 : 418422.[CrossRef]
19. Sagoo SK,, Little CL,, Mitchell RT . 2001. The microbiological examination of ready-to-eat organic vegetables from retail establishments in the United Kingdom. Lett Appl Microbiol 33 : 434439.[PubMed] [CrossRef]
20. Sagoo SK,, Little CL,, Ward L,, Gillespie IA,, Mitchell RT . 2003. Microbiological study of ready-to-eat salad vegetables from retail establishments uncovers a national outbreak of salmonellosis. J Food Prot 66 : 403409.[PubMed]
21. Feng P,, Strockbine N,, Fratamico P . 2012. Methods of detection and characterization of pathogenic Escherichia coli . In UNESCO-EOLSS Joint Committee (ed), Food Quality and Standards, in Encyclopedia of Life Support Systems (EOLSS). Developed under the Auspices of the UNESCO. Eolss Publishers, Oxford, UK. (http://www.eolss.net)
22. Lopez-Saucedo C,, Cerna JF,, Estrada-Garcia T . 2010. Non-O157 Shiga toxin-producing Escherichia coli is the most prevalent diarrheagenic E. coli pathotype in street-vended taco dressings in Mexico City. Clin Infect Dis 50 : 450451.[PubMed] [CrossRef]
23. Feng PCH,, Reddy SP . 2014. Prevalence and diversity of enterotoxigenic Escherichia coli strains in fresh produce. J Food Prot 77 : 820823.[PubMed] [CrossRef]
24. Monday SR,, Keys C,, Hansen P,, Shen Y,, Whittam TS,, Feng P . 2006. Produce isolates of Escherichia coli Ont:H52 serotype that carry both Shiga toxin 1 and StableToxin genes. Appl Environ Microbiol 72 : 30623065.[PubMed] [CrossRef]
25. Scheutz F,, Teel LD,, Beutin L,, Piérard D,, Buvens G,, Karch H,, Mellmann A,, Caprioli A,, Tozzoli R,, Morabito S,, Strockbine NA,, Melton-Celsa AR,, Sanchez M,, Persson S,, O’Brien AD . 2012. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 50 : 29512963.[PubMed] [CrossRef]
26. Martin A,, Beutin L . 2011. Characteristics of Shiga toxin-producing Escherichia coli from meat and milk products of different origins and association with food producing animals as main contamination sources. Int J Food Microbiol 146 : 99104.[PubMed] [CrossRef]
27. Monaghan A,, Byrne B,, Fanning S,, Sweeney T,, McDowell D,, Bolton DJ . 2011. Serotypes and virulence profiles of non-O157 Shiga toxin-producing Escherichia coli isolates from bovine farms. Appl Environ Microbiol 77 : 86628668.[PubMed] [CrossRef]
28. Mora A,, López C,, Dhabi G,, López-Beceiro AM,, Fidalgo LE,, Díaz EA,, Martínez-Carrasco C,, Mamani R,, Herrera A,, Blanco JE,, Blanco M,, Blanco J . 2012. Seropathotypes, phylogroups, Stx subtypes, and intimin types of wildlife-carried, Shiga toxin-producing Escherichia coli strains with same characteristics as human-pathogenic isolates. Appl Environ Microbiol 78 : 25782585.[PubMed] [CrossRef]
29. García-Aljaro C,, Muniesa M,, Blanco JE,, Blanco M,, Blanco J,, Jofre J,, Blanch AR . 2005. Characterization of Shiga toxin-producing Escherichia coli isolated from aquatic environments. FEMS Microbiol Lett 246 : 5565.[PubMed] [CrossRef]
30. Feng PCH,, Reddy S . 2013. Prevalences of Shiga toxin subtypes and selected other virulence factors among Shiga-toxigenic Escherichia coli strains isolated from fresh produce. Appl Environ Microbiol 79 : 69176923.[PubMed] [CrossRef]
31. Hussein HS . 2007. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J Anim Sci 85(13 Suppl):E63E72.[PubMed] [CrossRef]
32. Newton HJ,, Sloan J,, Bulach DM,, Seemann T,, Allison CC,, Tauschek M,, Robins-Browne RM,, Paton JC,, Whittam TS,, Paton AW,, Hartland EL . 2009. Shiga toxin producing Escherichia coli strains negative for locus of enterocyte effacement. Emerg Infect Dis 15 : 372380.[PubMed] [CrossRef]
33. Friedrich AW,, Borell J,, Bielaszewska M,, Fruth A,, Tschape H,, Karch H . 2003. Shiga toxin 1c-producing Escherichia coli strains: phenotypic and genetic characterization and association with human disease. J Clin Microbiol 41 : 22482453.[CrossRef]
34. Ethelberg S,, Olsen KE,, Scheutz F,, Jensen C,, Schiellerup P,, Enberg J,, Olesen B,, Gerner-Smidt P,, Mølbak K . 2004. Virulence factors for hemolytic uremic syndrome, Denmark. Emerg Infect Dis 10 : 842847.[PubMed] [CrossRef]
35. Karmali MA,, Petric M,, Lim C,, Fleming PC,, Arbus GS,, Lior H . 1985. The association between idiopathic hemolytic uremic syndrome and infection by verocytotoxin-producing Escherichia coli . J Infect Dis 151 : 775782.[PubMed] [CrossRef]
36. Paton AW,, Woodrow MC,, Doyle RM,, Lanser JA,, Paton JC . 1999. Molecular characterization of a Shiga toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J Clin Microbiol 37 : 33573361.[PubMed]
37. Paton AW,, Srimanote P,, Woodrow MC,, Paton JC . 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect Immun 69 : 69997009.[PubMed] [CrossRef]
38. Galli L,, Miliwebsky E,, Irino K,, Leotta G,, Rivas M . 2010. Virulence profile comparison between LEE-negative Shiga toxin-producing Escherichia coli (STEC) strains isolated from cattle and humans. Vet Microbiol 143 : 307313.[PubMed] [CrossRef]
39. Jenkins C,, Perry NT,, Cheasty T,, Shaw DJ,, Frankel G,, Dougan G,, Gunn GJ,, Smith HR,, Paton AW,, Paton JC . 2003. Distribution of the saa gene in strains of Shiga toxin-producing Escherichia coli of human and bovine origins. J Clin Microbiol 41 : 17751778.[PubMed] [CrossRef]
40. Bosilevac JM,, Koohmaraie M . 2011. Prevalence and characterization of non-O157 Shiga toxin producing Escherichia coli isolated from commercial ground beef in the United States. Appl Environ Microbiol 77 : 21032112.[PubMed] [CrossRef]
41. Boczek LA,, Johnson CH,, Rice EW,, Kinkle BK . 2006. The widespread occurrence of the enterohemolysin gene ehlyA among environmental strains of Escherichia coli . FEMS Microbiol Lett 254 : 281284.[PubMed] [CrossRef]
42. Karch H,, Bielaszewska M . 2001. Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157:H- strains: epidemiology, phenotypic and molecular characteristic, and microbiological diagnosis. J Clin Microbiol 39 : 20432049.[PubMed] [CrossRef]
43. Paton AW,, Beddoe T,, Thorpe CM,, Whisstock JC,, Wilce MC,, Rossjohn J,, Talbot UM,, Paton JC . 2006. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443 : 548552.[PubMed] [CrossRef]
44. Michelacci V,, Tozzoli R,, Caprioli A,, Martínez R,, Scheutz F,, Grande L,, Sánchez S,, Morabito S . 2013. A new pathogenicity island carrying an allelic variant of the Subtilase cytotoxin is common among Shiga toxin producing Escherichia coli of human and ovine origin. Clin Microbiol Infect 19 : E149E156.[PubMed] [CrossRef]
45. Johnson KE,, Thorpe CM,, Sears CL . 2006. The emerging clinical importance of non-O157 Shiga toxin-producing Escherichia coli . Clin Infect Dis. 43 : 15871595.[PubMed] [CrossRef]
46. Beutin L,, Montenegro MA,, Orskov I,, Prada J,, Zimmerman S,, Stephan R . 1989. Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli . J Clin Microbiol 27 : 25592564.[PubMed]
47. Sugiyama K,, Inoue K,, Sakazaki R . 2001. Mitomycin-supplemented washed blood agar for the isolation of Shiga toxin-producing Escherichia coli other than O157:H7. Lett Appl Microbiol 33 : 193195.[PubMed] [CrossRef]
48. Feng PCH,, Councell T,, Key C,, Monday SR . 2011. Virulence characterization of Shigatoxigenic Escherichia coli serotypes isolated from wholesale produce. Appl Environ Microbiol 77 : 343345.[PubMed] [CrossRef]
49. Feng PCH,, Delannoy S,, Lacher DW,, dos Santos LF,, Beutin L,, Fach P,, Rivas M,, Hartland EL,, Paton AW,, Guth BEC . 2014. Genetic diversity and virulence potential of Shiga toxin-producing Escherichia coli O113:H21 strains isolated from clinical, environmental, and food sources. Appl Environ Microbiol 80 : 47574763.[PubMed] [CrossRef]
50. Lacher DW,, Gangiredla J,, Jackson SA,, Elkins CA,, Feng PCH . 2014. A novel microarray design for molecular serotyping of Shiga toxin-producing Escherichia coli isolated from fresh produce. Appl Environ Microbiol 80 : 46774682.[PubMed] [CrossRef]

Tables

Generic image for table
TABLE 1

Selected STEC strains and serotypes isolated from various produce commodities

Citation: Feng P. 2015. Shiga Toxin-Producing in Fresh Produce: A Food Safety Dilemma, p 245-259. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0010-2013
Generic image for table
TABLE 2

Serotype and pathotype of selected produce STEC strains

Citation: Feng P. 2015. Shiga Toxin-Producing in Fresh Produce: A Food Safety Dilemma, p 245-259. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0010-2013

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error