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Advances in Microbial Food Safety: Volume 2

Advances in Microbial Food Safety: Volume 2

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Advances in Microbial Food Safety: Volume 2

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Nov 25, 2014


Research and legislation in food microbiology continue to evolve, and outbreaks of foodborne disease place further pressure on the industry to provide microbiologically safe products. This second volume in the series Advances in Microbial Food Safety summarises major recent advances in this field, and complements volume 1 to provide an essential overview of developments in food microbiology. Part one opens the book with an interview with a food safety expert. Part two provides updates on single pathogens, and part three looks at pathogen detection, identification and surveillance. Part four covers pathogen control and food preservation. Finally, part five focuses on pathogen control management.
  • Extends the breadth and coverage of the first volume in the series
  • Includes updates on specific pathogens and safety for specific foods
  • Reviews both detection and management of foodborne pathogens
Lançado em:
Nov 25, 2014

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Advances in Microbial Food Safety - Elsevier Science

Advances in microbial food safety

First Edition

John Sofos

Woodhead Publishing Series in Food Science, Technology and Nutrition: Number 275

Volume 2

Table of Contents

Cover image

Title page

Copyright page

Contributor contact details

Editorial advisors

Woodhead Publishing Series in Food Science, Technology and Nutrition

Part I: Hazards

1: Update on non-O157 Shiga toxin-producing E. coli as a foodborne pathogen: analysis and control


1.1 Introduction

1.2 Virulence of non-O157 Shiga toxin-producing E. coli (STEC)

1.3 Animal reservoirs of non-O157 STEC

1.4 Outbreaks caused by non-O157 STEC

1.5 Transmission of non-O157 STEC to humans

1.6 Interventions for control of non-O157 STEC in produce

1.7 Interventions for control of STEC in cattle

1.8 Resistance of non-O157 STEC to stress

1.9 Detection of non-O157 STEC

1.10 Conclusions

2: Update on Yersinia as a foodborne pathogen: analysis and control


2.1 Introduction

2.2 History and background

2.3 Evolution, genome, taxonomy and pathogenicity

2.4 Detection and identification methods

2.5 Epidemiology

2.6 Control

2.7 Future trends

3: Update on Toxoplasma gondii as a parasite in food: analysis and control


3.1 Introduction

3.2 Morphology, structure and life cycle

3.3 Biology, genetics and genomics

3.4 Diagnosis

3.5 Epidemiology

3.6 Pathogenesis and clinical features

3.7 Treatment and prevention

3.8 Future trends

4: The role of free-living protozoa in protecting foodborne pathogens


4.1 Introduction

4.2 Protozoa

4.3 Free-living protozoa in food-related environments

4.4 Free-living protozoa in drinking water and food

4.5 Interactions between bacteria and free-living protozoa

4.6 Significance of bacteria–protozoa interactions for food safety

4.7 Conclusions and future trends

5: Update on foodborne viruses: types, concentration and sampling methods


5.1 Introduction

5.2 Challenges in detecting foodborne viruses

5.3 Types of virus

5.4 Methodologies for sampling and concentration

5.5 Conclusions

6: Update on foodborne viruses: molecular-based detection methods


6.1 Introduction

6.2 Methods for detection of foodborne viruses

6.3 RNA extraction and purification

6.4 Molecular amplification and detection

6.5 Confirmation of RNA-amplified products

6.6 Real-time reverse-transcriptase polymerase chain reaction (RT-PCR) approaches

6.7 Nucleic acid sequence-based amplification (NASBA) assay

6.8 Reverse transcription loop-mediated isothermal amplification (RT-LAMP) assay

6.9 Biosensors

6.10 Microarrays

6.11 Next-generation sequencing approaches

6.12 Detection of infectious versus noninfectious viruses using molecular-based assays

6.13 Conclusions

7: Update on Listeria monocytogenes: reducing cross-contamination in food retail operations


7.1 Introduction to the food safety issue

7.2 L. monocytogenes and listeriosis

7.3 Presence and prevalence of L. monocytogenes in retail operations

7.4 Transfer dynamics of L. monocytogenes at retail

7.5 The role of food workers in L. monocytogenes cross-contamination at retail

7.6 Risk assessment of L. monocytogenes in retail delicatessen

7.7 Mitigation options to control cross-contamination with L. monocytogenes at retail

7.8 Future trends

Part II: Hazard management and control

8: Developments in food disease surveillance: using source attribution to inform risk management


8.1 Introduction

8.2 Foodborne disease surveillance

8.3 Surveillance and the role of typing of foodborne pathogens

8.4 Producing evidence to inform policy to prevent and control foodborne diseases

8.5 Usefulness and applicability of source attribution methods for foodborne hazards

8.6 Future trends

9: Modelling the spread of pathogen contamination in fresh produce


9.1 Introduction

9.2 Contamination of fresh produce: modelling pathogen growth behaviour

9.3 Case study: predicting pathogen growth on lettuce

9.4 Case study: modelling Listeria monocytogenes contamination of minced tuna

9.5 Summary

10: Developments in validation and verification methods for hazard analysis and critical control points (HACCP) and other food safety systems


10.1 Introduction

10.2 Validating food safety systems

10.3 eassessment or revalidation of food safety controls

10.4 Validation of food controls: case studies

10.5 Verification of food safety management system activities

10.6 Validation and verification: a Global Food Safety Initiative (GFSI) perspective

10.7 Future trends

10.10 Appendix: Comparison of critical control points (CCPs) and prerequisite programs (PRPs)

Part III: Particular foods

11: Developments in sampling and test methods for pathogens in fresh meat


11.1 Introduction

11.2 Sampling plans

11.3 Testing for pathogens: hazard analysis critical control point (HACCP) systems

11.4 Principles and limitations of sample testing

11.5 Current US and EU methods of sample testing

11.6 Future trends

12: Developments in Salmonella control in eggs


12.1 Introduction

12.2 Salmonella in laying flocks and eggs

12.3 Monitoring and controls in Europe before the EU baseline survey

12.4 The current situation in Europe

12.5 Human salmonellosis outbreaks in Europe

12.6 Incidence and control of egg-borne salmonellosis outside of Europe

12.7 Potential for eradication of Salmonella Enteritidis from laying farms

12.8 Potential treatments for eggs

12.9 Future trends

13: The role of animal manure in the contamination of fresh food


13.1 Introduction

13.2 Animal manure

13.3 Foodborne pathogens associated with animal manure

13.4 Common practices in applying animal manure to agricultural fields

13.5 Persistence and transmission of human pathogens after land application of animal manure

13.6 Contamination of produce on farms originating from animal manure

13.7 Animal waste treatments to minimize contamination

13.8 Guidelines on direct application of raw animal manure or composted products to cropland

13.9 Conclusions

14: Developments in improving the safety of sprouts


14.1 Introduction

14.2 Trends in the consumption of raw vegetables

14.3 Microbiological hazards in seeds and sprouts

14.4 Bacterial pathogens contaminating seeds and sprouts

14.5 Outbreaks of foodborne illness associated with the consumption of sprouts

14.6 Measures to control hazards associated with sprouts

14.7 Conclusions and future trends

15: Food safety standards in the fresh produce supply chain: advantages and disadvantages


15.1 Introduction

15.2 Benefits and concerns relating to the implementation of food safety standards

15.3 Improving food safety management systems in the fresh produce supply chain

15.4 Future trends in food safety standards

15.5 Conclusions: the importance of training and risk communication for well-accepted and functional food safety standards

15.6 Sources of further information

15.7 Acknowledgements



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Contributor contact details

(* = main contact)


Prof. J. Sofos, john.sofos@colostate.edu     Department of Animal Sciences, Center for Meat Safety and Quality, Colorado State University Fort Collins, CO 80523-1171, USA

Chapter 1

P.M. Fratamico, pina.fratamico@ars.usda.gov     USDA, Agricultural Research Service, Eastern Regional Research Center 600 East Mermaid Lane, Wyndmoor, PA 19038, USA

Chapter 2

Prof. T. Nesbakken, truls.nesbakken@nmbu.no     Faculty of Veterinary Medicine and Biosciences, Dept. of Food Safety and Infection Biology, Section for Food Safety Norwegian University of Life Sciences, P. O. Box 8146 Dep., 0033 Oslo, Norway

Chapter 3

D.E. Hill*, dolores.hill@ars.usda.gov; J.P. Dubey, jitender.dubey@ars.usda.gov     USDA, ARS, BARC, APDL BLDG 307-C & 1001, BARC-EAST, Beltsville, MD 20705, USA,

Chapter 4

M. Vaerewijck; K. Houf*, Kurt.Houf@UGent.be     Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine Ghent University, Salisburylaan 133 9820 Merelbeke, Belgium

Chapters 5 and 6

D.H. D’Souza, ddsouza@utk.edu     Department of Food Science and Technology, University of Tennessee-Knoxville 2600 River Drive, Room 102 FSPB Knoxville, TN 37996-4591, USA

Chapter 7

K. Hoelzer*, Karin.Hoelzer@fda.hhs.gov     S. Dennis, US Food and Drug Administration Center for Food Safety and Applied Nutrition, 5100 Paint Branch Parkway College Park, MD 20740, USA

J. Kause     US Department of Agriculture Food Safety and Inspection Service Office of Public Health Science Washington, DC 20250, USA

Chapter 8

S.M. Pires, smpi@food.dtu.dk     National Food Institute, Technical University of Denmark Mørkhøj Byfgade 19, Building H 2860 Søborg, Denmark

Chapter 9

S. Koseki, koseki@bpe.agr.hokudai.ac.jp     Research Faculty of Agriculture Hokkaido University, Kita 9, Nishi 9, Kita-ku Sapporo 060-8589, Japan

Chapter 10

J.G. Surak, jgsurak@yahoo.com     Surak and Associates, 108 Lakeview Circle, Clemson, SC 29631, USA

Chapter 11

C.O. Gill*, colin.gill@agr.gc.ca     Agriculture and Agri-food Canada Lacombe Research Centre, 6000 C & E Trail, Lacombe, Alberta, T4L 1 W1, Canada

A.O. Gill, alex.gill@hc-sc.gc.ca     Health Canada, Bureau of Microbial Hazards, 251 Sir Frederick Banting Driveway, P.L. 2204E, Ottawa, Ontario, K1A 0 K9, Canada

Chapter 12

R.H. Davies, rob.davies@ahvla.gsi.gov.uk; A.D. Wales*, andywales@fastmail.co.uk     Bacteriology Department, Animal Health and Veterinary Laboratories Agency (AHVLA) Woodham Lane, New Haw, Addlestone, Surrey KT15 3NB, UK

Chapter 13

X. Jiang*, xiuping@clemson.edu; Z. Chen; M. Dharmasena     Department of Food, Nutrition, and Packaging Sciences, Clemson University Clemson, SC 29634, USA

Chapter 14

S. Morabito, stefano.morabito@iss.it     EU Reference Laboratory for Escherichia coli including VTEC, Istituto Superiore di Sanità Veterinary Public Health and Food Safety Department Viale Regina Elena 299 00161 Rome, Italy

Chapter 15

M. Uyttendaele*, mieke.uyttendaele@UGent.be; S. Van Boxstael; L. Jacxsens, Liesbeth.Jacxsens@UGent.be     Department Food Safety and Food Quality, Faculty of Bio-Science Engineering Ghent University, Coupure Links 653 Ghent, 9000, Belgium

K. Kirezieva, klementina.kirezieva@wur.nl; P. Luning, pieternel.luning@wur.nl     Food Quality and Design Group, Department of Agrotechnology and Food Sciences, Wageningen University, P.O. Box 17, 6700AA Wageningen The Netherlands

Editorial advisors

Prof. Stanley Brul, University of Amsterdam, The Netherlands

Prof. Robert Buchanan, University of Maryland, USA

Prof. Mansel Griffiths, University of Guelph, Canada

Dr Peter McClure, Unilever, UK

Assoc. Prof. Tom Ross, University of Tasmania, Australia

Woodhead Publishing Series in Food Science, Technology and Nutrition

Chilled foods: A comprehensive guide Edited by C. Dennis and M. Stringer

Yoghurt: Science and technology A. Y. Tamime and R. K. Robinson

Food processing technology: Principles and practice P. J. Fellows

Bender’s dictionary of nutrition and food technology Sixth edition D. A. Bender

Determination of veterinary residues in food Edited by N. T. Crosby

Food contaminants: Sources and surveillance Edited by C. Creaser and R. Purchase

Nitrates and nitrites in food and water Edited by M. J. Hill

Pesticide chemistry and bioscience: The food-environment challenge Edited by G. T. Brooks and T. Roberts

Pesticides: Developments, impacts and controls Edited by G. A. Best and A. D. Ruthven

10 Dietary fibre: Chemical and biological aspects Edited by D. A. T. Southgate, K. W. Waldron, I. T. Johnson and G. R. Fenwick

11 Vitamins and minerals in health and nutrition M. Tolonen

12 Technology of biscuits, crackers and cookies Second edition D. Manley

13 Instrumentation and sensors for the food industry Edited by E. Kress-Rogers

14 Food and cancer prevention: Chemical and biological aspects Edited by K. W. Waldron, I. T. Johnson and G. R. Fenwick

15 Food colloids: Proteins, lipids and polysaccharides Edited by E. Dickinson and B. Bergenstahl

16 Food emulsions and foams Edited by E. Dickinson

17 Maillard reactions in chemistry, food and health Edited by T. P. Labuza, V. Monnier, J. Baynes and J. O’Brien

18 The Maillard reaction in foods and medicine Edited by J. O’Brien, H. E. Nursten, M. J. Crabbe and J. M. Ames

19 Encapsulation and controlled release Edited by D. R. Karsa and R. A. Stephenson

20 Flavours and fragrances Edited by A. D. Swift

21 Feta and related cheeses Edited by A. Y. Tamime and R. K. Robinson

22 Biochemistry of milk products Edited by A. T. Andrews and J. R. Varley

23 Physical properties of foods and food processing systems M. J. Lewis

24 Food irradiation: A reference guide V. M. Wilkinson and G. Gould

25 Kent’s technology of cereals: An introduction for students of food science and agriculture Fourth edition N. L. Kent and A. D. Evers

26 Biosensors for food analysis Edited by A. O. Scott

27 Separation processes in the food and biotechnology industries: Principles and applications Edited by A. S. Grandison and M. J. Lewis

28 Handbook of indices of food quality and authenticity R. S. Singhal, P. K. Kulkarni and D. V. Rege

29 Principles and practices for the safe processing of foods D. A. Shapton and N. F. Shapton

30 Biscuit, cookie and cracker manufacturing manuals Volume 1: Ingredients D. Manley

31 Biscuit, cookie and cracker manufacturing manuals Volume 2: Biscuit doughs D. Manley

32 Biscuit, cookie and cracker manufacturing manuals Volume 3: Biscuit dough piece forming D. Manley

33 Biscuit, cookie and cracker manufacturing manuals Volume 4: Baking and cooling of biscuits D. Manley

34 Biscuit, cookie and cracker manufacturing manuals Volume 5: Secondary processing in biscuit manufacturing D. Manley

35 Biscuit, cookie and cracker manufacturing manuals Volume 6: Biscuit packaging and storage D. Manley

36 Practical dehydration Second edition M. Greensmith

37 Lawrie’s meat science Sixth edition R. A. Lawrie

38 Yoghurt: Science and technology Second edition A. Y. Tamime and R. K. Robinson

39 New ingredients in food processing: Biochemistry and agriculture G. Linden and D. Lorient

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41 Technology of biscuits, crackers and cookies Third edition D. Manley

42 Food processing technology: Principles and practice Second edition P. J. Fellows

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44 Handbook of hydrocolloids Edited by G. O. Phillips and P. A. Williams

45 Food labelling Edited by J. R. Blanchfield

46 Cereal biotechnology Edited by P. C. Morris and J. H. Bryce

47 Food intolerance and the food industry Edited by T. Dean

48 The stability and shelf-life of food Edited by D. Kilcast and P. Subramaniam

49 Functional foods: Concept to product Edited by G. R. Gibson and C. M. Williams

50 Chilled foods: A comprehensive guide Second edition Edited by M. Stringer and C. Dennis

51 HACCP in the meat industry Edited by M. Brown

52 Biscuit, cracker and cookie recipes for the food industry D. Manley

53 Cereals processing technology Edited by G. Owens

54 Baking problems solved S. P. Cauvain and L. S. Young

55 Thermal technologies in food processing Edited by P. Richardson

56 Frying: Improving quality Edited by J. B. Rossell

57 Food chemical safety Volume 1: Contaminants Edited by D. Watson

58 Making the most of HACCP: Learning from others’ experience Edited by T. Mayes and S. Mortimore

59 Food process modelling Edited by L. M. M. Tijskens, M. L. A. T. M. Hertog and B. M. Nicolaï

60 EU food law: A practical guide Edited by K. Goodburn

61 Extrusion cooking: Technologies and applications Edited by R. Guy

62 Auditing in the food industry: From safety and quality to environmental and other audits Edited by M. Dillon and C. Griffith

63 Handbook of herbs and spices Volume 1 Edited by K. V. Peter

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66 Food chemical safety Volume 2: Additives Edited by D. Watson

67 Fruit and vegetable biotechnology Edited by V. Valpuesta

68 Foodborne pathogens: Hazards, risk analysis and control Edited by C. de W. Blackburn and P. J. McClure

69 Meat refrigeration S. J. James and C. James

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72 Minimal processing technologies in the food industries Edited by T. Ohlsson and N. Bengtsson

73 Fruit and vegetable processing: Improving quality Edited by W. Jongen

74 The nutrition handbook for food processors Edited by C. J. K. Henry and C. Chapman

75 Colour in food: Improving quality Edited by D. MacDougall

76 Meat processing: Improving quality Edited by J. P. Kerry, J. F. Kerry and D. A. Ledward

77 Microbiological risk assessment in food processing Edited by M. Brown and M. Stringer

78 Performance functional foods Edited by D. Watson

79 Functional dairy products Volume 1 Edited by T. Mattila-Sandholm and M. Saarela

80 Taints and off-flavours in foods Edited by B. Baigrie

81 Yeasts in food Edited by T. Boekhout and V. Robert

82 Phytochemical functional foods Edited by I. T. Johnson and G. Williamson

83 Novel food packaging techniques Edited by R. Ahvenainen

84 Detecting pathogens in food Edited by T. A. McMeekin

85 Natural antimicrobials for the minimal processing of foods Edited by S. Roller

86 Texture in food Volume 1: Semi-solid foods Edited by B. M. McKenna

87 Dairy processing: Improving quality Edited by G. Smit

88 Hygiene in food processing: Principles and practice Edited by H. L. M. Lelieveld, M. A. Mostert, B. White and J. Holah

89 Rapid and on-line instrumentation for food quality assurance Edited by I. Tothill

90 Sausage manufacture: Principles and practice E. Essien

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92 Bread making: Improving quality Edited by S. P. Cauvain

93 Food preservation techniques Edited by P. Zeuthen and L. Bøgh-Sørensen

94 Food authenticity and traceability Edited by M. Lees

95 Analytical methods for food additives R. Wood, L. Foster, A. Damant and P. Key

96 Handbook of herbs and spices Volume 2 Edited by K. V. Peter

97 Texture in food Volume 2: Solid foods Edited by D. Kilcast

98 Proteins in food processing Edited by R. Yada

99 Detecting foreign bodies in food Edited by M. Edwards

100 Understanding and measuring the shelf-life of food Edited by R. Steele

101 Poultry meat processing and quality Edited by G. Mead

102 Functional foods, ageing and degenerative disease Edited by C. Remacle and B. Reusens

103 Mycotoxins in food: Detection and control Edited by N. Magan and M. Olsen

104 Improving the thermal processing of foods Edited by P. Richardson

105 Pesticide, veterinary and other residues in food Edited by D. Watson

106 Starch in food: Structure, functions and applications Edited by A.-C. Eliasson

107 Functional foods, cardiovascular disease and diabetes Edited by A. Arnoldi

108 Brewing: Science and practice D. E. Briggs, P. A. Brookes, R. Stevens and C. A. Boulton

109 Using cereal science and technology for the benefit of consumers: Proceedings of the 12th International ICC Cereal and Bread Congress, 24–26th May, 2004, Harrogate, UK Edited by S. P. Cauvain, L. S. Young and S. Salmon

110 Improving the safety of fresh meat Edited by J. Sofos

111 Understanding pathogen behaviour: Virulence, stress response and resistance Edited by M. Griffiths

112 The microwave processing of foods Edited by H. Schubert and M. Regier

113 Food safety control in the poultry industry Edited by G. Mead

114 Improving the safety of fresh fruit and vegetables Edited by W. Jongen

115 Food, diet and obesity Edited by D. Mela

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117 Detecting allergens in food Edited by S. Koppelman and S. Hefle

118 Improving the fat content of foods Edited by C. Williams and J. Buttriss

119 Improving traceability in food processing and distribution Edited by I. Smith and A. Furness

120 Flavour in food Edited by A. Voilley and P. Etievant

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123 Emerging foodborne pathogens Edited by Y. Motarjemi and M. Adams

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130 Meat products handbook: Practical science and technology G. Feiner

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135 Maximising the value of marine by-products Edited by F. Shahidi

136 Chemical migration and food contact materials Edited by K. Barnes, R. Sinclair and D. Watson

137 Understanding consumers of food products Edited by L. Frewer and H. van Trijp

138 Reducing salt in foods: Practical strategies Edited by D. Kilcast and F. Angus

139 Modelling microorganisms in food Edited by S. Brul, S. Van Gerwen and M. Zwietering

140 Tamime and Robinson’s Yoghurt: Science and technology Third edition A. Y. Tamime and R. K. Robinson

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142 Improving the flavour of cheese Edited by B. Weimer

143 Novel food ingredients for weight control Edited by C. J. K. Henry

144 Consumer-led food product development Edited by H. MacFie

145 Functional dairy products Volume 2 Edited by M. Saarela

146 Modifying flavour in food Edited by A. J. Taylor and J. Hort

147 Cheese problems solved Edited by P. L. H. McSweeney

148 Handbook of organic food safety and quality Edited by J. Cooper, C. Leifert and U. Niggli

149 Understanding and controlling the microstructure of complex foods Edited by D. J. McClements

150 Novel enzyme technology for food applications Edited by R. Rastall

151 Food preservation by pulsed electric fields: From research to application Edited by H. L. M. Lelieveld and S. W. H. de Haan

152 Technology of functional cereal products Edited by B. R. Hamaker

153 Case studies in food product development Edited by M. Earle and R. Earle

154 Delivery and controlled release of bioactives in foods and nutraceuticals Edited by N. Garti

155 Fruit and vegetable flavour: Recent advances and future prospects Edited by B. Brückner and S. G. Wyllie

156 Food fortification and supplementation: Technological, safety and regulatory aspects Edited by P. Berry Ottaway

157 Improving the health-promoting properties of fruit and vegetable products Edited by F. A. Tomás-Barberán and M. I. Gil

158 Improving seafood products for the consumer Edited by T. Børresen

159 In-pack processed foods: Improving quality Edited by P. Richardson

160 Handbook of water and energy management in food processing Edited by J. Klemeš, R. Smith and J.-K. Kim

161 Environmentally compatible food packaging Edited by E. Chiellini

162 Improving farmed fish quality and safety Edited by Ø. Lie

163 Carbohydrate-active enzymes Edited by K.-H. Park

164 Chilled foods: A comprehensive guide Third edition Edited by M. Brown

165 Food for the ageing population Edited by M. M. Raats, C. P. G. M. de Groot and W. A Van Staveren

166 Improving the sensory and nutritional quality of fresh meat Edited by J. P. Kerry and D. A. Ledward

167 Shellfish safety and quality Edited by S. E. Shumway and G. E. Rodrick

168 Functional and speciality beverage technology Edited by P. Paquin

169 Functional foods: Principles and technology M. Guo

170 Endocrine-disrupting chemicals in food Edited by I. Shaw

171 Meals in science and practice: Interdisciplinary research and business applications Edited by H. L. Meiselman

172 Food constituents and oral health: Current status and future prospects Edited by M. Wilson

173 Handbook of hydrocolloids Second edition Edited by G. O. Phillips and P. A. Williams

174 Food processing technology: Principles and practice Third edition P. J. Fellows

175 Science and technology of enrobed and filled chocolate, confectionery and bakery products Edited by G. Talbot

176 Foodborne pathogens: Hazards, risk analysis and control Second edition Edited by C. de W. Blackburn and P. J. McClure

177 Designing functional foods: Measuring and controlling food structure breakdown and absorption Edited by D. J. McClements and E. A. Decker

178 New technologies in aquaculture: Improving production efficiency, quality and environmental management Edited by G. Burnell and G. Allan

179 More baking problems solved S. P. Cauvain and L. S. Young

180 Soft drink and fruit juice problems solved P. Ashurst and R. Hargitt

181 Biofilms in the food and beverage industries Edited by P. M. Fratamico, B. A. Annous and N. W. Gunther

182 Dairy-derived ingredients: Food and neutraceutical uses Edited by M. Corredig

183 Handbook of waste management and co-product recovery in food processing Volume 2 Edited by K. W. Waldron

184 Innovations in food labelling Edited by J. Albert

185 Delivering performance in food supply chains Edited by C. Mena and G. Stevens

186 Chemical deterioration and physical instability of food and beverages Edited by L. H. Skibsted, J. Risbo and M. L. Andersen

187 Managing wine quality Volume 1: Viticulture and wine quality Edited by A. G. Reynolds

188 Improving the safety and quality of milk Volume 1: Milk production and processing Edited by M. Griffiths

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191 Sensory analysis for food and beverage quality control: A practical guide Edited by D. Kilcast

192 Managing wine quality Volume 2: Oenology and wine quality Edited by A. G. Reynolds

193 Winemaking problems solved Edited by C. E. Butzke

194 Environmental assessment and management in the food industry Edited by U. Sonesson, J. Berlin and F. Ziegler

195 Consumer-driven innovation in food and personal care products Edited by S. R. Jaeger and H. MacFie

196 Tracing pathogens in the food chain Edited by S. Brul, P. M. Fratamico and T. A. McMeekin

197 Case studies in novel food processing technologies: Innovations in processing, packaging, and predictive modelling Edited by C. J. Doona, K. Kustin and F. E. Feeherry

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200 Oxidation in foods and beverages and antioxidant applications Volume 2: Management in different industry sectors Edited by E. A. Decker, R. J. Elias and D. J. McClements

201 Protective cultures, antimicrobial metabolites and bacteriophages for food and beverage biopreservation Edited by C. Lacroix

202 Separation, extraction and concentration processes in the food, beverage and nutraceutical industries Edited by S. S. H. Rizvi

203 Determining mycotoxins and mycotoxigenic fungi in food and feed Edited by S. De Saeger

204 Developing children’s food products Edited by D. Kilcast and F. Angus

205 Functional foods: Concept to product Second edition Edited by M. Saarela

206 Postharvest biology and technology of tropical and subtropical fruits Volume 1: Fundamental issues Edited by E. M. Yahia

207 Postharvest biology and technology of tropical and subtropical fruits Volume 2: Açai to citrus Edited by E. M. Yahia

208 Postharvest biology and technology of tropical and subtropical fruits Volume 3: Cocona to mango Edited by E. M. Yahia

209 Postharvest biology and technology of tropical and subtropical fruits Volume 4: Mangosteen to white sapote Edited by E. M. Yahia

210 Food and beverage stability and shelf life Edited by D. Kilcast and P. Subramaniam

211 Processed Meats: Improving safety, nutrition and quality Edited by J. P. Kerry and J. F. Kerry

212 Food chain integrity: A holistic approach to food traceability, safety, quality and authenticity Edited by J. Hoorfar, K. Jordan, F. Butler and R. Prugger

213 Improving the safety and quality of eggs and egg products Volume 1 Edited by Y. Nys, M. Bain and F. Van Immerseel

214 Improving the safety and quality of eggs and egg products Volume 2 Edited by F. Van Immerseel, Y. Nys and M. Bain

215 Animal feed contamination: Effects on livestock and food safety Edited by J. Fink-Gremmels

216 Hygienic design of food factories Edited by J. Holah and H. L. M. Lelieveld

217 Manley’s technology of biscuits, crackers and cookies Fourth edition Edited by D. Manley

218 Nanotechnology in the food, beverage and nutraceutical industries Edited by Q. Huang

219 Rice quality: A guide to rice properties and analysis K. R. Bhattacharya

220 Advances in meat, poultry and seafood packaging Edited by J. P. Kerry

221 Reducing saturated fats in foods Edited by G. Talbot

222 Handbook of food proteins Edited by G. O. Phillips and P. A. Williams

223 Lifetime nutritional influences on cognition, behaviour and psychiatric illness Edited by D. Benton

224 Food machinery for the production of cereal foods, snack foods and confectionery L.-M. Cheng

225 Alcoholic beverages: Sensory evaluation and consumer research Edited by J. Piggott

226 Extrusion problems solved: Food, pet food and feed M. N. Riaz and G. J. Rokey

227 Handbook of herbs and spices Second edition Volume 1 Edited by K. V. Peter

228 Handbook of herbs and spices Second edition Volume 2 Edited by K. V. Peter

229 Breadmaking: Improving quality Second edition Edited by S. P. Cauvain

230 Emerging food packaging technologies: Principles and practice Edited by K. L. Yam and D. S. Lee

231 Infectious disease in aquaculture: Prevention and control Edited by B. Austin

232 Diet, immunity and inflammation Edited by P. C. Calder and P. Yaqoob

233 Natural food additives, ingredients and flavourings Edited by D. Baines and R. Seal

234 Microbial decontamination in the food industry: Novel methods and applications Edited by A. Demirci and M.O. Ngadi

235 Chemical contaminants and residues in foods Edited by D. Schrenk

236 Robotics and automation in the food industry: Current and future technologies Edited by D. G. Caldwell

237 Fibre-rich and wholegrain foods: Improving quality Edited by J. A. Delcour and K. Poutanen

238 Computer vision technology in the food and beverage industries Edited by D.-W. Sun

239 Encapsulation technologies and delivery systems for food ingredients and nutraceuticals Edited by N. Garti and D. J. McClements

240 Case studies in food safety and authenticity Edited by J. Hoorfar

241 Heat treatment for insect control: Developments and applications D. Hammond

242 Advances in aquaculture hatchery technology Edited by G. Allan and G. Burnell

243 Open innovation in the food and beverage industry Edited by M. Garcia Martinez

244 Trends in packaging of food, beverages and other fast-moving consumer goods (FMCG) Edited by N. Farmer

245 New analytical approaches for verifying the origin of food Edited by P. Brereton

246 Microbial production of food ingredients, enzymes and nutraceuticals Edited by B. McNeil, D. Archer, I. Giavasis and L. Harvey

247 Persistent organic pollutants and toxic metals in foods Edited by M. Rose and A. Fernandes

248 Cereal grains for the food and beverage industries E. Arendt and E. Zannini

249 Viruses in food and water: Risks, surveillance and control Edited by N. Cook

250 Improving the safety and quality of nuts Edited by L. J. Harris

251 Metabolomics in food and nutrition Edited by B. C. Weimer and C. Slupsky

252 Food enrichment with omega-3 fatty acids Edited by C. Jacobsen, N. S. Nielsen, A. F. Horn and A.-D. M. Sørensen

253 Instrumental assessment of food sensory quality: A practical guide Edited by D. Kilcast

254 Food microstructures: Microscopy, measurement and modelling Edited by V. J. Morris and K. Groves

255 Handbook of food powders: Processes and properties Edited by B. R. Bhandari, N. Bansal, M. Zhang and P. Schuck

256 Functional ingredients from algae for foods and nutraceuticals Edited by H. Domínguez

257 Satiation, satiety and the control of food intake: Theory and practice Edited by J. E. Blundell and F. Bellisle

258 Hygiene in food processing: Principles and practice Second edition Edited by H. L. M. Lelieveld, J. Holah and D. Napper

259 Advances in microbial food safety Volume 1 Edited by J. Sofos

260 Global safety of fresh produce: A handbook of best practice, innovative commercial solutions and case studies Edited by J. Hoorfar

261 Human milk biochemistry and infant formula manufacturing technology Edited by M. Guo

262 High throughput screening for food safety assessment: Biosensor technologies, hyperspectral imaging and practical applications Edited by A. K. Bhunia, M. S. Kim and C. R. Taitt

263 Foods, nutrients and food ingredients with authorised EU health claims: Volume 1 Edited by M. J. Sadler

264 Handbook of food allergen detection and control Edited by S. Flanagan

265 Advances in fermented foods and beverages: Improving quality, technologies and health benefits Edited by W. Holzapfel

266 Metabolomics as a tool in nutrition research Edited by J.-L. Sébédio and L. Brennan

267 Dietary supplements: Safety, efficacy and quality Edited by K. Berginc and S. Kreft

268 Grapevine breeding programs for the wine industry: Traditional and molecular technologies Edited by A. G. Reynolds

269 Handbook of antimicrobials for food safety and quality Edited by M. Taylor

270 Managing and preventing obesity: Behavioural factors and dietary interventions Edited by T. P. Gill

271 Electron beam pasteurization and complementary food processing technologies Edited by S. D. Pillai and S. Shayanfar

272 Advances in food and beverage labelling: Information and regulations Edited by P. Berryman

273 Flavour development, analysis and perception in food and beverages Edited by J. K. Parker, S. Elmore and L. Methven

274 Rapid sensory profiling techniques and related methods: Applications in new product development and consumer research, Edited by J. Delarue, J. B. Lawlor and M. Rogeaux

275 Advances in microbial food safety: Volume 2 Edited by J. Sofos

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277 Lockhart and Wiseman’s crop husbandry including grassland: Ninth edition H. J. S. Finch, A. M. Samuel and G. P. F. Lane

278 Global legislation for food contact materials: Processing, storage and packaging Edited by J. S. Baughan

279 Colour additives for food and beverages Edited by M. Scotter

280 A complete course in canning and related processes 14th Edition: Volume 1 Revised by S. Featherstone

281 A complete course in canning and related processes 14th Edition: Volume 2 Revised by S. Featherstone

282 A complete course in canning and related processes 14th Edition: Volume 3 Revised by S. Featherstone

Part I



Update on non-O157 Shiga toxin-producing E. coli as a foodborne pathogen: analysis and control*

J.L. Smith; P.M. Fratamico; N.R. Launchi    United States Department of Agriculture, USA


Although Shiga toxin-producing Escherichia coli (STEC) O157:H7 is a leading cause of foodborne illness worldwide, non-O157 STEC serogroups may cause more illnesses than O157:H7, and information on transmission and outbreaks is presented. The role of ruminants as a major reservoir for both O157 and non-O157 STEC is explored, and how ingestion of contaminated animal products or produce contaminated by animal feces can lead to illness is discussed. Intervention strategies that control STEC O157:H7 and also inactivate non-O157 STEC are identified. Methods for detection of highly virulent non-O157 STEC are described and the need for additional research to understand the prevalence, epidemiology, and virulence of these pathogens is emphasized for their effective control.

Key words

non-O157 Shiga toxin-producing Escherichia coli

foodborne pathogens

Shiga toxin

virulence genes

animal reservoirs

1.1 Introduction

Shiga toxin-producing Escherichia coli (STEC) are diarrheic foodborne pathogens that are the major causative agents of hemorrhagic colitis (HC) and postdiarrheal hemolytic uremic syndrome (HUS) leading to severe kidney disease and even death. E. coli O157:H7 has, for many years, been the major STEC strain causing HUS. Use of improved methods for the detection and identification of non-O157 STEC have revealed that the number of non-O157 STEC infections is overtaking O157:H7 as the main cause of STEC-associated illness (Gould et al., 2013; Scallan et al., 2011). In general, the non-O157 STEC do not cause as severe disease as the O157 STEC but some non-O157 STEC strains have caused HUS (Gould et al., 2013).

The intestinal tracts of animals used as a food source, particularly cattle and other ruminants, are reservoirs of both O157 and non-O157 STEC; therefore, during slaughtering operations, the carcass may become contaminated, leading to meat products containing the pathogens. Surveys of cattle (feces, hides, and pre- and post-intervention carcasses) showed similar levels of E. coli O157:H7 and non-O157 STEC. Produce and vegetables may be contaminated with STEC strains because fecal excretion by animals can contaminate soil and water sources (Kaspar et al., 2010). Other animal reservoirs for STEC include goats, sheep, guanaco, deer, and elk. There was an outbreak associated with deer meat contaminated with STEC O103:H2 in high school students in Minnesota in 2010 (Rounds et al., 2012). Non-ruminants, including cats, dogs, pigs, horses, rabbits, and poultry, as well as transport hosts, including birds, rodents, flies, and beetles can also carry STEC.

An awareness of the importance of the non-O157 STEC as foodborne pathogens is critical for food microbiologists, food processors, food regulators, and clinicians; however, there is, overall, less known about this heterogeneous group of pathogens than about STEC O157:H7. This chapter provides information on transmission and outbreaks caused by non-O157 STEC, virulence factors, reservoirs, ecology, control strategies, and detection.

1.2 Virulence of non-O157 Shiga toxin-producing E. coli (STEC)

1.2.1 Non-O157 STEC serogroups and serotypes associated with human disease

Based on data from US FoodNet sites for the period of 2000 to 2010, Gould et al. (2013) found that the non-O157 STEC serogroups caused a total of 2006 infections, and serogroup O157 was responsible for 5688 infections. Over 70% of the total non-O157 infections were caused by serogroup O26, O45, O103, O111, O121, and O145. Overall, 7.5% of non-O157 STEC infections were linked to outbreaks, whereas 19.5% of O157 STEC infections were outbreak-associated. Infections caused by non-O157 STEC were more commonly associated with international travel (16.2%) than O157 (2.7%). In addition to the six non-O157 serogroups listed above, Gould et al. (2013) list 66 other non-O157 serogroups responsible for illness in the United States. For the period 2007 to 2010, the European Union (EU) reported 2140 cases of STEC-induced illness. STEC O157:H7/H − was responsible for 1047/2140 (49.0%) cases, and 1093/2140 (51%) cases were attributable to non-O157 STEC (EFSA, 2013). Serogroups O26, O63, O91, O103, O111, O117, O121, O128, O145, and O146 accounted for 48.5% (530/1093) of non-O157 STEC cases in the EU. Non-O157 STEC serotypes associated with confirmed HUS cases in the EU during 2007 to 2010 include: O1:H42, O7:H6, O26:H11, O76:H19, O80:H2, O86:H27, O91:H10, O104:H21, O105:H18, O111:H −/H8, O121:H19/H2, O123:H2, O128:H2, O145:H −/H28, and O174:H2/H21 (EFSA, 2013 [their table 13]). Although there are some STEC serotypes such as O26:H11, O111:H −, O121:H19, and O145:H − that are important causes of serious illness both in the USA and in Europe, there are other serotypes that are more common in Europe than in the USA and vice versa.

1.2.2 Diseases caused by non-O157 STEC

In general, non-O157 STEC infections are not as severe as O157 infections. The median hospital stay is 3 days with both types of STEC infections; however, during the period of 2000 to 2010 in the USA, only 13.7% of patients infected with non-O157 STEC were hospitalized compared with 43.4% for O157 cases (Gould et al., 2013). During that period, 33 deaths were reported for O157 STEC but only two were due to non-O157 STEC. Data from cases reported in 2008 to 2009 indicated that diarrhea was common with both types of STEC but 85.5% of O157 STEC cases presented with bloody diarrhea compared with 54.8% of non-O157 STEC cases. Only 1.3% (4/301) of non-O157 cases developed HUS whereas 10.7% (83/773) of O157 cases contracted HUS. The four cases of HUS associated with non-O157 infection were attributable to serogroups O111 (two cases) and one case each by O103 and O121 (Gould et al., 2013). In 2012, STEC O157 accounted for 531 foodborne infections whereas non-O157 accounted for 551 infections. Reports indicated that O157 and non-O157 STEC caused 187 and 88 hospitalizations, respectively (CDC, 2013). Long-term consequences may occur in some patients with diarrhea-associated HUS. HUS occurs more often in children and the elderly, and it is the most common cause of acute renal failure in children. Shiga toxin causes glomerular damage with development of anemia, thrombocytopenia, and renal failure. Extrarenal lesions may involve the gastrointestinal tract, pancreas, liver, cardiovascular system, and central nervous system (Gallo and Gianantonio, 1995). Extrarenal lesions are rarer today because of early intervention by dialysis of the affected patient.

1.2.3 Non-O157 STEC virulence genes

Some genes that may be necessary for virulence in O157:H7 and non-O157 STEC are presented in Table 1.1. The production of Shiga toxin (Stx) by STEC strains is the most critical virulence factor responsible for HC and HUS. There are two types of Stx: Stx1 and Stx2; and several variants of both are known. Stx2 is ca. 1000 times more toxic than Stx1 toward renal micro-vascular endothelial cells (Gyles, 2007). The toxins are encoded by genes carried on lysogenic phages located in the STEC chromosome. Both toxins have an A1B5 structure; the B moiety binds to globotriaosylceramide (Gb3) present on host microvascular endothelial cell surfaces (kidney, intestine, and brain) followed by endocytosis of the toxin (Ivarsson et al., 2012). The A subunit is released from the B moiety and enters the cytosol via chaper-one-mediated transfer. The A subunit acts as a 28S RNA N-glycosidase, blocking protein synthesis and inducing apoptosis of endothelial cells, particularly those of the kidneys (Ivarsson et al., 2012; Khan and Naim, 2011). The renal glomerular endothelial cells swell and detach from the basement membrane, fibrin thrombi form, and there is narrowing of the capillary lumen leading to a reduced blood supply to the glomeruli causing a loss of kidney function (Gyles, 2007).

Table 1.1

Virulence genes present in O157 and non-O157 STEC. Values are number of isolates positive by PCR with percentages given in parentheses

Modified from Buvens and Piérard (2012)

Genes on the 35-kb chromosomal pathogenicity island, LEE (locus of enterocyte effacement), encode important STEC virulence factors. There are three distinct factors of LEE: the adhesin known as intimin and the translocatedintimin receptor (Tir), the type III protein secretion system (TTSS), and the secreted proteins EspA, EspB, and EspD (Khan and Naim, 2011). Intimin (encoded by eae) enables the STEC cell to attach to the intestinal epithelial cells and induce attaching and effacing (A/E) lesions. Tir (encoded by tir) passes through the host cell membrane via TTSS to form a transmembrane structure with one terminal located in the cytoplasm and the other terminal binding to intimin (Khan and Naim, 2011). Thus, the binding action of Tir produces an intimate attachment of the microorganisms to the host cell. The genes espADB encode the translocator proteins EspA, EspB, and EspD, which form the conduit through which the TTSS delivers effector proteins to the host cell. The LEE-encoded proteins induce efficient bacterial colonization, dissemination, and multiplication in the intestinal tract. In addition, these proteins induce A/E lesions with resultant microvillus destruction and actin reorganization to form a cup-like structure around the micro-organism attached to the enterocyte (pedestal formation). Pedestal formation allows STEC to remain extracellular while enabling the cells to avoid immune consequences (Lara-Ochoa et al., 2010). Individuals infected with STEC producing Stx2 have an increased risk of developing HUS and the presence of both the stx2 and eae genes is a strong predictor of HUS induction (Gyles, 2007). The data presented in Table 1.1 indicate that a higher percentage of non-O157 STEC strains associated with HUS were more likely to carry the stx2, ehxA, and eae genes, as well as some O-island 122 (OI-122)-associated genes than strains not associated with HUS.

Additionally, other genes postulated to be associated with virulence are found on large plasmids present in STEC strains. For example, pO157, present in O157:H7 STEC carries the ehx operon responsible for synthesis and transport of enterohemolysin, katP, and espP genes encoding a biofunctional catalase peroxidase and serine protease, respectively, as well as the etpD gene, which is involved in type II secretion (Caprioli et al., 2005; Khan and Naim, 2011). The katP, espP, and ehx operon genes are present on the large plasmid present in LEE-positive O26:H11 and O145:NM STEC indicating that the plasmids from these STEC strains are closely related (Fratamico et al., 2011b; Yan et al., 2012). Non-O157 STEC lacking LEE (i.e., eae negative), also have similar large plasmids which carry genes such as ehxA and espP (Newton et al., 2009). In addition, LEE-negative non-O157 STEC strains may have plasmid-associated subAB and saa genes, which encode for the subtilasecytotoxin and autoagglutinating adhesion proteins, respectively (Irino et al., 2010; Paton et al., 2001). The saa and subAB genes appear to be limited to eae-negative STEC.

The STEC strains have been divided into seropathotypes (SPT): STEC in SPT-A are HUS- and outbreak-associated (O157:H7); STEC in SPT-B are less commonly associated with outbreaks but can cause severe disease (O26:H11, O103:H2, O111:H8/NM, O121:H19, O145:NM), SPT-C can cause severe illness, but rarely causes outbreaks (O91:H21, O104:H21, O113:H21, as well as other serotypes), SPT-D is diarrhea-associated and rarely outbreak-associated, and serotypes in SPT-E are not associated with illness. Multiple serotypes are found in SPT-D and SPT-E (Karmali et al., 2003; Mora et al., 2012). In addition to the LEE pathogenicity island (PAI), several other PAIs (n = 11) are found in seropathotypes A and B; PAIs are rarer in strains within seropathotypes C, D, and E (Imamovic et al., 2010). Important PAIs associated with HUS present in SPT-A, -B, and -C strains include OI-122 and OI-57. OI-122 was present in 19/34 (55.9%) of SPT-A and -B strains but in only 17.2% (11/64) of SPT-C,D,E strains. HUS was induced by 26/56 (46.4%) strains of SPT-A, -B, and -C strains containing OI-122 but in only 4/42 (9.5%) of SPT-D and -E strains (Ju et al., 2013). Genes present on OI-122 include pagC (encodes a virulence factor required for survival in macrophages), sen (encodes an enterotoxin), efa1/2 (encode adherence factors), and nleB/E (encode proteins that inhibit host cell inflammatory responses). OI-57 was present in 28/34 (82.3%) SPT-A and -B but in only 14 of 64 (21.9%) of SPT-C,D,E strains. HUS was induced by 60.7% (34/56) of SPT-A,B,C strains whereas only 19.0% (8/42) of SPT-D,E strains containing OI-57 induced HUS. OI-57 genes include nleG genes whose functions are unknown (Ju et al., 2013). The presence of OI-122 and OI-57 is strongly associated with the presence of LEE in STEC strains (Ju et al., 2012). The data presented in Table 1.1 suggest that a number of genes may be associated with severe illness (HC and HUS), but Gyles (2007) and Konczy et al. (2008) indicate that the eae and stx2 genes are the most important virulence genes.

1.2.4 Impact of diet on O157 and non-O157 STEC virulence

Fermentation of dietary fiber in the colon results in the formation of short-chain fatty acids including butyrate. Butyrate leads to the increased expression of Gb3. Binding of Stx to Gb3 is an important part of the disease process induced by STEC (Zumbrun et al., 2013). Utilizing mice fed a high fiber diet, Zumbrun et al. (2013) found that this diet increased the intestinal colonization of E. coli O157:H7 86-24 and led to a 25% greater mortality than in mice fed a low fiber diet. They further demonstrated that binding of Stx to colonocytes and renal tissue of the mice fed a high fiber diet was greater than that of mice fed a low fiber diet. In addition, mice fed a high fiber diet had a reduced level of commensal E. coli that may promote enhanced colonization of STEC. The experiments in mice suggest that a high fiber diet with resultant increased binding of Stx may result in a higher incidence of severe disease induced by O157 and non-O157 STEC.

1.3 Animal reservoirs of non-O157 STEC

Non-O157 STEC have been isolated from the feces of a variety of animals, both domestic and wild. However, ruminants, particularly beef and dairy cattle, are the most important reservoirs of both O157 and non-O157 STEC (Hussein and Bollinger, 2005; Hussein and Sakuma, 2005).

1.3.1 Cattle

Surveying published studies from a number of countries (1989–2004), Hussein and Bollinger (2005) found that testing of beef cattle feces for O157 STEC showed a prevalence rate ranging from 0.2 to 27.8%, whereas the prevalence rate for non-O157 STEC was 2.1 to 70.1%. Hussein and Sakuma (2005) did a similar survey (1991–2004) to examine fecal shedding of STEC in dairy cattle. The prevalence rate for shedding O157 STEC was 0.2 to 48.8%, whereas the prevalence rate for non-O157 STEC serogroups was 0.4 to 74.0%.

Jeon et al., (2006) obtained 809 fecal samples from beef and dairy cattle located on 209 farms in Korea and found that 54 fecal samples were positive for E. coli serogroup O26 (49 of these strains were positive for stx) and 77 samples contained serogroup O111 (28 strains were positive for stx). Pearce et al., (2006) determined the fecal shedding prevalence of E. coli serogroups O26, O103, O111, and O145 in Scottish beef cattle. They investigated 6086 fecal pats from 338 farms. Serogroup O26 was present in 279 fecal pats, serogroup O103 was present in 164, and serogroup O145 was present in 43 fecal pats. Serogroups O103 and O145 rarely carried the stx gene; however, 49.0% of the serogroup O26 isolates were positive for stx. The stx, eae, and ehxA genes were present in 28.9% of the O26 isolates (Pearce et al., 2006). In a survey of 20 Irish cattle farms (both dairy and beef), 107 of 1200 fecal samples and 600 soil samples contained STEC strains (Monaghan et al., 2011). The most common isolate was serotype O113:H4 (n = 31); other serotypes were O26:H11 (n = 14), O2:H27 (n = 13), and O168:H2 (n = 10) (Monaghan et al., 2011).

Tanaro et al. (2012) studied the STEC prevalence in 292 fecal swabs obtained on an Argentinian beef farm between September 2005 and November 2006. The prevalence of STEC in the fecal samples was 37.7% (110/292). The STEC strains consisted of 24 serotypes and included O103:H2 (n = 12), O136:H12 (n = 8), O178:H19 (n = 8), and O103:NM (n = 5) (Tanaro et al., 2012). Fecal samples obtained from beef cattle in 21 feedlots from four US states were tested by PCR for seven STEC serogroups (Dargatz et al., 2013).

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