Behavior of Escherichia coli O157:H7 in leafy vegetables.

Leafy vegetables, including lettuce and spinach, have been implicated in several outbreaks of foodborne disease caused by Escherichia coli O157:H7, a pathogen of increasing public health significance because of the severity of the gastrointestinal illness and long-term, chronic sequelae that can result from infection. A definitive association between the consumption of leafy vegetables and human disease provides implicit evidence of transfer from animal sources to field crops and retail commodities, including minimally processed or fresh-cut products. Understanding the behavior of E. coli O157:H7 in leafy vegetables during production, after harvest, in storage, during processing, and in packaged fresh-cut products is essential for the development of effective control measures. To this end, previous research on the fate of the species at each step in the production of market-ready leafy vegetables is reviewed in this study. Several critical gaps in knowledge are identified, notably uncertainty about the location of contaminating cells on or in plant tissues, behavior in packaged products stored at low temperatures, and the influence of environmental stresses on growth and infectivity.

[1]  T. Roper,et al.  Salmonella enterica Serovar Typhimurium and Escherichia coli Contamination of Root and Leaf Vegetables Grown in Soils with Incorporated Bovine Manure , 2002, Applied and Environmental Microbiology.

[2]  M. K. Shaw,et al.  Determination of the Minimal Temperature for Growth of Escherichia coli , 1971, Journal of bacteriology.

[3]  M. Nauta,et al.  Variability in Growth Characteristics of Different E. coli O157:H7 Isolates, and its Implications for Predictive Microbiology , 1999 .

[4]  S. Bunčić,et al.  Effects of cold storage and heat–acid shocks on growth and verotoxin 2 production ofEscherichia coliO157:H7 , 1998 .

[5]  A. Charkowski,et al.  Cross-contamination of lettuce with Escherichia coli O157:H7. , 2002, Journal of food protection.

[6]  S. Palumbo,et al.  Minimum and Maximum Temperatures for Growth and Verotoxin Production by Hemorrhagic Strains of Escherichia coli. , 1995, Journal of food protection.

[7]  T. Cheasty,et al.  Transmission of Vero cytotoxin producing Escherichia coli O157 infection from farm animals to humans in Cornwall and west Devon. , 1999, Communicable disease and public health.

[8]  S. Lindow,et al.  Frequency, Size, and Localization of Bacterial Aggregates on Bean Leaf Surfaces , 2004, Applied and Environmental Microbiology.

[9]  D. O'beirne,et al.  Effects of process severity on survival and growth of Escherichia coli and Listeria innocua on minimally processed vegetables , 2005 .

[10]  A. A. Visser,et al.  Quantification of contamination of lettuce by GFP-expressing Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium. , 2007, Food microbiology.

[11]  G. Daube,et al.  Verotoxigenic Escherichia coli from animals, humans and foods: who's who? , 2005, Journal of applied microbiology.

[12]  G. Bengtsson,et al.  Potential Uptake of Escherichia coli O157:H7 from Organic Manure into Crisphead Lettuce , 2005, Applied and Environmental Microbiology.

[13]  S. Cutillo [Hemolytic-uremic syndrome]. , 1973, La Pediatria.

[14]  Lee-Ann Jaykus,et al.  A field study of the microbiological quality of fresh produce of domestic and Mexican origin. , 2006, International journal of food microbiology.

[15]  J. Marcy,et al.  Inhibition of pathogens on fresh produce by ultraviolet energy. , 2004, International journal of food microbiology.

[16]  D. Crowley,et al.  Microbial phyllosphere populations are more complex than previously realized , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  L. Beuchat,et al.  Survival and growth of Escherichia coli O157:H7 on salad vegetables , 1993, Applied and environmental microbiology.

[18]  Catherine J. Potenski,et al.  Effect of irrigation method on transmission to and persistence of Escherichia coli O157:H7 on lettuce. , 2002, Journal of food protection.

[19]  E. Solomon,et al.  Persistence of Escherichia coli O157:H7 on lettuce plants following spray irrigation with contaminated water. , 2003, Journal of food protection.

[20]  Scott A. McEwen,et al.  Associations between Indicators of Livestock Farming Intensity and Incidence of Human Shiga Toxin-Producing Escherichia Coli Infection , 2002, Emerging infectious diseases.

[21]  E. Dyck,et al.  Preharvest evaluation of coliforms, Escherichia coli, Salmonella, and Escherichia coli O157:H7 in organic and conventional produce grown by Minnesota farmers. , 2004, Journal of food protection.

[22]  R. Buchanan,et al.  pH-dependent stationary-phase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants. , 1999, Journal of food protection.

[23]  M. Drake,et al.  Stress Response of Escherichia coli , 2006 .

[24]  J F Frank,et al.  Comparison of the attachment of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella typhimurium, and Pseudomonas fluorescens to lettuce leaves. , 2000, Journal of food protection.

[25]  Arun K. Bhunia,et al.  Efficacy of Chlorine Dioxide, Ozone, and Thyme Essential Oil or a Sequential Washing in Killing Escherichia coli O157:H7 on Lettuce and Baby Carrots , 2002 .

[26]  Sheng Yang He,et al.  Plant Stomata Function in Innate Immunity against Bacterial Invasion , 2006, Cell.

[27]  A. V. Van Bruggen,et al.  Effects of Cattle Feeding Regimen and Soil Management Type on the Fate of Escherichia coli O157:H7 and Salmonella enterica Serovar Typhimurium in Manure, Manure-Amended Soil, and Lettuce , 2005, Applied and Environmental Microbiology.

[28]  T. Pennington,et al.  Long‐term survival of Escherichia coli O157 on pasture following an outbreak associated with sheep at a scout camp , 2002, Letters in applied microbiology.

[29]  J F Frank,et al.  Penetration of Escherichia coli O157:H7 into lettuce tissues as affected by inoculum size and temperature and the effect of chlorine treatment on cell viability. , 2000, Journal of food protection.

[30]  P. Gale,et al.  Land application of treated sewage sludge: quantifying pathogen risks from consumption of crops , 2005, Journal of applied microbiology.

[31]  R. Mandrell,et al.  Escherichia coli O157:H7 survival and growth on lettuce is altered by the presence of epiphytic bacteria. , 2006, Journal of food protection.

[32]  I. Capek,et al.  Possible person-to-person transmission of Escherichia coli O111 – associated hemolytic uremic syndrome , 1997, Pediatric Nephrology.

[33]  R. L. Buchanan,et al.  Fate of Escherichia coli O157:H7 on Fresh-Cut Apple Tissue and Its Potential for Transmission by Fruit Flies , 1999, Applied and Environmental Microbiology.

[34]  T. Shirahata,et al.  Does Enterohemorrhagic Escherichia coliO157:H7 Enter the Viable but Nonculturable State in Salted Salmon Roe? , 2000, Applied and Environmental Microbiology.

[35]  Franklin Park,et al.  Fresh-cut Vegetables , 2009 .

[36]  Craig S. Wong,et al.  The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. , 2000, The New England journal of medicine.

[37]  T. Whittam,et al.  Produce Isolates of the Escherichia coli Ont:H52 Serotype That Carry both Shiga Toxin 1 and Stable Toxin Genes , 2006, Applied and Environmental Microbiology.

[38]  R. Mandrell,et al.  Association of Escherichia coli O157:H7 with preharvest leaf lettuce upon exposure to contaminated irrigation water. , 2002, Journal of food protection.

[39]  J. R. Gorny,et al.  Attachment of microorganisms to fresh produce. , 2006 .

[40]  Waterborne outbreak of gastroenteritis associated with a contaminated municipal water supply, Walkerton, Ontario, May-June 2000. , 2000, Canada communicable disease report = Releve des maladies transmissibles au Canada.

[41]  Benne S. Marmer,et al.  Growth of Escherichia coli O157:H7 at Fluctuating Incubation Temperatures. , 1995, Journal of food protection.

[42]  R. Dixon Natural products and plant disease resistance , 2001, Nature.

[43]  N. Leonard,et al.  A comparison of the survival in feces and water of Escherichia coli O157:H7 grown under laboratory conditions or obtained from cattle feces. , 2006, Journal of food protection.

[44]  P. Gale Matrix effects, nonuniform reduction and dispersion in risk assessment for Escherichia coli O157 , 2005, Journal of applied microbiology.

[45]  M. Harrison,et al.  Microbial antagonists of foodborne pathogens on fresh, minimally processed vegetables. , 2002, Journal of food protection.

[46]  A. Ibekwe,et al.  Fate of Escherichia coli O157:H7 in irrigation water on soils and plants as validated by culture method and real-time PCR. , 2004, Canadian journal of microbiology.

[47]  E. Solomon,et al.  Transmission of Escherichia coli O157:H7 from Contaminated Manure and Irrigation Water to Lettuce Plant Tissue and Its Subsequent Internalization , 2002, Applied and Environmental Microbiology.

[48]  M. Drake,et al.  Impact of cold and cold-acid stress on poststress tolerance and virulence factor expression of Escherichia coli O157:H7. , 2004, Journal of food protection.

[49]  D. O'beirne,et al.  Variation among strains of Listeria monocytogenes: differences in survival on packaged vegetables and in response to heat and acid conditions , 2005 .

[50]  J. Dow,et al.  Outbreak of Escherichia coli 0157:H7 related to animal contact at a petting zoo. , 2002, The Canadian journal of infectious diseases = Journal canadien des maladies infectieuses.

[51]  E. H. Garrett,et al.  Outbreaks Associated with Fresh Produce: Incidence, Growth, and Survival of Pathogens in Fresh and Fresh‐Cut Produce , 2001 .

[52]  Larry R. Beuchat,et al.  Survival and growth of Escherichia coli O157:H7 inoculated onto cut lettuce before or after heating in chlorinated water, followed by storage at 5 or 15°C , 2001 .

[53]  L. Dipineto,et al.  Presence of Shiga toxin‐producing Escherichia coli O157:H7 in living layer hens , 2006, Letters in applied microbiology.

[54]  S. Loncarevic,et al.  Bacteriological quality of organically grown leaf lettuce in Norway , 2005, Letters in applied microbiology.

[55]  P. Feng,et al.  Influence of substrate and low temperature on growth and survival of verotoxigenicEscherichia coli , 1996 .

[56]  D. O'beirne,et al.  Effects of vegetable type, package atmosphere and storage temperature on growth and survival of Escherichia coli O157:H7 and Listeria monocytogenes , 2001, Journal of Industrial Microbiology and Biotechnology.

[57]  David L. Swerdlow,et al.  Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002 , 2005, Emerging infectious diseases.

[58]  M. Doyle,et al.  Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces , 1996, Applied and environmental microbiology.

[59]  A. King,et al.  Microbial Flora and Storage Quality of Partially Processed Lettuce , 1991 .

[60]  M. Brandl,et al.  Fitness of human enteric pathogens on plants and implications for food safety. , 2006, Annual review of phytopathology.

[61]  E. Solomon,et al.  Interaction of live and dead Escherichia coli O157:H7 and fluorescent microspheres with lettuce tissue suggests bacterial processes do not mediate adherence , 2006, Letters in applied microbiology.

[62]  Sharad C. Phatak,et al.  Survival of Escherichia coli O157:H7 in soil and on carrots and onions grown in fields treated with contaminated manure composts or irrigation water , 2005 .

[63]  H. Bolin,et al.  FACTORS AFFECTING THE STORAGE STABILITY OF SHREDDED LETTUCE , 1977 .

[64]  J. Wells,et al.  Hemorrhagic colitis associated with a rare Escherichia coli serotype. , 1983, The New England journal of medicine.

[65]  S. Phatak,et al.  Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. , 2004, Journal of food protection.

[66]  Leighton Pritchard,et al.  Comparative genomics reveals what makes an enterobacterial plant pathogen. , 2006, Annual review of phytopathology.

[67]  H. Lior,et al.  Growing Concerns and Recent Outbreaks Involving Non-O157:H7 Serotypes of Verotoxigenic Escherichia coli. , 1996, Journal of food protection.

[68]  A. Maule Survival of verocytotoxigenic Escherichia coli O157 in soil, water and on surfaces , 2000, Symposium series.

[69]  L. Harris,et al.  Survival and recovery of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes on lettuce and parsley as affected by method of inoculation, time between inoculation and analysis, and treatment with chlorinated water. , 2004, Journal of food protection.

[70]  G. Martin,et al.  Strategies used by bacterial pathogens to suppress plant defenses. , 2004, Current opinion in plant biology.

[71]  K. Seo,et al.  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. , 1999, Journal of food protection.

[72]  J. LeBlanc Implication of Virulence Factors in Escherichia coli O157:H7 Pathogenesis , 2003, Critical reviews in microbiology.

[73]  B. Swaminathan,et al.  An Outbreak of Escherichia coli O157:H7 Infection from Unpasteurized Commercial Apple Juice , 1999, Annals of Internal Medicine.

[74]  M. Griffiths,et al.  Internalization of Escherichia coli O157:H7 following biological and mechanical disruption of growing spinach plants. , 2005, Journal of food protection.

[75]  S. Lindow,et al.  Role of Leaf Surface Sugars in Colonization of Plants by Bacterial Epiphytes , 2000, Applied and Environmental Microbiology.

[76]  Y. Wasteson,et al.  Influence of bovine manure as fertilizer on the bacteriological quality of organic Iceberg lettuce , 2004, Journal of applied microbiology.

[77]  A. Jones,et al.  Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. , 2006, Journal of food protection.

[78]  S. Isobe,et al.  Prediction of pathogen growth on iceberg lettuce under real temperature history during distribution from farm to table. , 2005, International journal of food microbiology.

[79]  L. Durso,et al.  Measurements of Fitness and Competition in Commensal Escherichia coli and E. coli O157:H7 Strains , 2004, Applied and Environmental Microbiology.

[80]  Keith Warriner,et al.  Interactions of Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocytogenes plants cultivated in a gnotobiotic system. , 2005, International journal of food microbiology.

[81]  D. Law The history and evolution of Escherichia coli O157 and other Shiga toxin-producing E. coli , 2000 .

[82]  J. Hotchkiss,et al.  Comparative Growth ofEscherichia coli 0157:H7, Spoilage Organisms and Shelf-Life of Shredded Iceberg Lettuce Stored under Modified Atmospheres , 1996 .

[83]  P. Toivonen,et al.  Survival and growth of Listeria monocytogenes and Escherichia coli O157:H7 in ready-to-eat iceberg lettuce washed in warm chlorinated water. , 2002, Journal of food protection.

[84]  M. Griffiths,et al.  Effects of environmental stresses on the activities of the uspA, grpE and rpoS promoters of Escherichia coli O157:H7. , 2005, International journal of food microbiology.