Cover
Title Page
List of Contributors
Preface to the Technical Series
Preface
1 Microbial Toxins – An Overview
1. 1.1 Introduction
2. 1.2 Microbial toxins: modes of action
3. 1.3 Bacterial toxins
4. 1.4 Mycotoxins
5. 1.5 Biogenic amines (BAs)
6. 1.6 Conclusions
7. References
2 Incidences of Mould and Bacterial Toxins in Dairy Products
1. 2.1 Background
2. 2.2 Bacterial toxins
3. 2.3 Mould toxins (mycotoxins)
4. 2.4 Other mycotoxins
5. 2.5 Conclusion
6. References
3 Bacterial Toxins – Structure, Properties and Mode of Action
1. 3.1 Background
2. 3.2 Bacillus cereus toxins
3. 3.3 Botulinum neurotoxin
4. 3.4 Staphylococcus aureus enterotoxin
5. 3.5 Conclusions
6. References
4 Biogenic Amines in Dairy Products
1. 4.1 Introduction
2. 4.2 Biochemistry: biosynthesis pathways, enzymes and transporters
3. 4.3 Biogenic amine‐producing micro‐organisms
4. 4.4 Toxicological effects
5. 4.5 Factors affecting BAs accumulation in dairy products
6. 4.6 Other preventive methods
7. 4.7 Conclusions
8. Acknowledgements
9. References
5 Contamination of Raw Milk
1. 5.1 Introduction
2. 5.2 The concept of contamination
3. 5.3 Sources of contamination
4. 5.4 Conclusion
5. References
6 Milk Product Contamination After the Farm Gate
1. 6.1 Introduction
2. 6.2 The significance of microbial contamination
3. 6.3 Factories, processes and people
4. 6.4 Raw milk handling
5. 6.5 Milk‐processing and dairy products manufacture
6. 6.6 Buttermaking
7. 6.7 Cheesemaking
8. 6.8 Yoghurt
9. 6.9 Milk powders
10. 6.10 Evaporated milk and sweetened condensed milk
11. 6.11 Ice‐cream
12. 6.12 Hygiene, food safety management and cleaning‐in‐place (CIP)
13. 6.13 Packaging, storage, distribution and the retail environment
14. 6.14 Conclusions
15. References
7 Techniques for Detection, Quantification and Control of Bacterial Toxins
1. 7.1 Introduction
2. 7.2 Bacterial toxins
3. 7.3 Control of toxins
4. 7.4 Methods for identification and detection of microbial toxins
5. 7.5 Conclusion
6. References
8 Techniques for Detection, Quantification and Control of Mycotoxins in Dairy Products
1. 8.1 Introduction
2. 8.2 Methods for detection and quantification of mycotoxins
3. 8.3 Separation methods
4. 8.4 Mathematical model (exposure assessment of mycotoxins in dairy milk)
5. 8.5 Control of mycotoxin
6. 8.6 Conclusion
7. References
9 Approaches to Assess the Risks/Modelling of Microbial Growth and Toxin Production
1. 9.1 Background on risk analysis
2. 9.2 Focus on cheese risk assessment
3. 9.3 Staphylococcus aureus
4. 9.4 Escherichia coli
5. 9.5 Listeria monocytogenes
6. 9.6 Cheese ‐ chemical risk assessment
7. 9.7 Modelling of growth and inactivation: kinetic approaches
8. 9.8 Conclusions
9. References
10 Regulatory Measures for Microbial Toxins
1. 10.1 Introduction and background
2. 10.2 The evolution and economic significance of heat‐treated milk and milk products
3. 10.3 Bacterial toxins
4. 10.4 Regulatory provisions on bacterial toxins in milk and milk products
5. 10.5 Mycotoxins
6. 10.6 Conclusions
7. References
Index
End User License Agreement

List of Tables

Chapter 01
1. Table 1.1 Some general characteristics of mycotoxins detected in dairy products.
2. Table 1.2 Some physical characteristics of biogenic amine (BAs) that have been identified in dairy products, mainly cheeses that are potential health risks to humans.
Chapter 02
1. Table 2.1 Growth and toxin production by Bacillus cereus nc7401 in various food samples at 30°C for 24 h.
2. Table 2.2 Emetic toxin production of Bacillus cereus isolates from infant food formulas.
3. Table 2.3 Growth and toxin production of groups I and II of Clostridium botulinum in dairy foods.
4. Table 2.4 Dairy products associated with outbreaks of botulism in humans.
5. Table 2.5 Incidence and level of aflatoxin M₁ in cow’s milk (unless specified) and dairy products.
6. Table 2.6 Incidence and level of aflatoxin M₁ in different variety of cheeses.
7. Table 2.7 Incidence and level of aflatoxin M₁ in different dairy products.
8. Table 2.8 Incidence and level of ochratoxin a in milk and infant formulas.
9. Table 2.9 Incidence and level of ochratoxin a in different cheeses varieties.
10. Table 2.10 Incidence and levels of mycotoxins in different cheeses.
Chapter 04
1. Table 4.1 Average and maximum contents (mg L^–1 or mg kg^–1) of biogenic amines (BAs) compounds in different foods as reported by many researchers.
Chapter 05
1. Table 5.1 Main source of micro‐organisms occurring in milk and associated spoilage and safety issues in dairy products.
2. Table 5.2 Possible routes of contamination by toxic producing organism on the farm.
3. Table 5.3 The 2001 Stockholm Convention on persistent organic pollutants.
Chapter 06
1. Table 6.1 Condensed milks regulations in the United Kingdom (UK).
Chapter 08
1. Table 8.1 Detection and quantification of mycotoxin by liquid chromatography (LC) and fluorescent/ultraviolet (UV) detector.
2. Table 8.2 Detection and quantification of mycotoxin by liquid chromatography (LC) and mass spectroscopy (MS) detector.
3. Table 8.3 Detection and quantification of mycotoxin by enzyme‐linked immunosorbent assay (ELISA) method.
Chapter 09
1. Table 9.1 Genus Staphylococcus – coagulase‐positive species.
2. Table 9.2 Types of staphylococcal enterotoxins (SEs) that have been identified.
3. Table 9.3 Factors influencing Staphylococcus aureus growth and staphylococcal enterotoxins (SEs) production.
4. Table 9.4 Effect of the minimum thermisation (62°C for 15 s) and minimum storage/maturation of cheese (2°C for 90 days).
5. Table 9.5 Consequences of exposure determinations after pathogen infection.
6. Table 9.6 Hazard characterisation and infective dose.
7. Table 9.7 Prevalence of confirmed food poisoning cases in European countries from 2007 to 2012.
8. Table 9.8 Prevalence of confirmed Escherichia Coli food poisoning in European countries from 2007 to 2012 of the most important serogroups.
9. Table 9.9 Some selected studies reporting on the occurrence of verotoxigenic Escherichia coli (VTEC) and prevalence of Stx genes in dairy products.
10. Table 9.10 Human outbreaks of food‐borne listeriosis associated with dairy products.
11. Table 9.11 Dose‐response (mg kg⁻¹) for humans and alimentary histamine in different cheeses.
Chapter 10
1. Table 10.1 Heat treatment requirements under European Union hygiene legislation.
2. Table 10.2 Criteria for raw milk supply in European Union legislation.
3. Table 10.3 Microbiological criteria for milk and milk products in European Union legislation.
4. Table 10.4 Standards for grade “A” raw milk and milk products for pasteurisation, ultra‐pasteurisation and aseptic processing supply in the US legislation (PMO).
5. Table 10.5 Heat treatment requirements specified in the US legislation (PMO and CFR).
6. Table 10.6 Standards for grade “A” pasteurised milk and milk products in the US legislation (PMO).
7. Table 10.7 Microbiological standards for certain grade “A” milk products in the US legislation (PMO).
8. Table 10.8 List of the Codex Alimentarius Commission (CAC) standards, guidelines, codes of practice and principles related to food hygiene and microbiological food safety most relevant to milk and milk products.
9. Table 10.9 Section headings of Codex Alimentarius Commission (CAC) codes of hygiene.
10. Table 10.10 List of the Codex Alimentarius Commission (CAC) standards, guidelines, codes of practice and principles related to contaminants, including mycotoxins in food and feed most relevant to milk and milk products.

List of Illustrations

Chapter 04
1. Fig. 4.1 An illustration showing the classification of biogenic amines (BAs). Top: According to the number of amino groups present, BAs can be classified as mono‐, di‐ or poly‐amines. Right: According to the chemical structure, BAs can be classified as cyclic or aliphatic.
2. Fig. 4.2 Tyramine biosynthesis.
3. Fig. 4.3 Histamine biosynthesis.
4. Fig. 4.4 Putrescine biosynthesis.
5. Fig. 4.5 Cadaverine biosynthesis.
6. Fig. 4.6 An illustration of the typical genetic organisation of gene clusters involved in biogenic amines (BAs) production from different bacteria isolated from dairy products.
Chapter 07
1. Fig. 7.1 Common sources of food contamination.
2. Fig. 7.2 Industrial sectors that require control of toxin production.
3. Fig. 7.3 Common methods in pathogen detection. Abbreviation: DNA – deoxyribonucleic acid.
4. Fig. 7.4 Bacterial toxins – traditional and upcoming methods for their detection. Abbreviations: RPLA = reverse passive latex agglutination; ELISA = enzyme‐linked immonosorbent assay; ELIFA = enzyme‐linked immunofiltration assay; PCR = polymerase chain reaction; LOC = lab‐on‐a‐chip; SPR = surface plasmon resonance.
5. Fig. 7.5 Enzyme‐linked immunosorbent assay (ELISA) for detection of microbial toxins.
6. Fig. 7.6 A lateral flow assay (LFA) system for detection of bacterial toxins.
7. Fig. 7.7 The principle of surface plasmon resonance (SPR) for detection of bacterial toxins.
Chapter 08
1. Fig. 8.1 Chemical structures of some mycotoxin compounds.
2. Fig. 8.2 Flow‐injection immunoassay set‐up.
3. Fig. 8.3 Use of the polymerase chain reaction (PCR) for detection of mycotoxigenic fungi.

Society of Dairy Technology Series

Series Editor(s): A.Y. Tamime.

The Society of Dairy Technology has joined with Wiley‐Blackwell to produce a series of technical dairy‐related handbooks providing an invaluable resource for all those involved in the dairy industry; from practitioners to technologists working in both traditional and modern large‐scale dairy operations.

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by Koon Hoong Teh, Steve Flint, John Brooks, and Geoff Knight (Editors)

Milk and Dairy Products as Functional Foods
by Ara Kanekanian (Editor)

Membrane Processing: Dairy and Beverage Applications
by Adnan Y. Tamime (Editor)

Processed Cheese and Analogues
by Adnan Y. Tamime (Editor)

Technology of Cheesemaking, 2nd Edition
by Barry A. Law and Adnan Y. Tamime (Editors)

Dairy Fats and Related Products
by Adnan Y. Tamime (Editor)

Dairy Powders and Concentrated Products
by Adnan Y. Tamime (Editor)

Milk Processing and Quality Management
by Adnan Y. Tamime (Editor)

Cleaning‐in‐Place: Dairy, Food and Beverage Operations, 3rd Edition
by Adnan Y. Tamime (Editor)

Structure of Dairy Products
by Adnan Y. Tamime (Editor)

Brined Cheeses
by Adnan Y. Tamime (Editor)

Fermented Milks
by Adnan Y. Tamime (Editor)

Probiotic Dairy Products
by Adnan Y. Tamime (Editor)

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Library of Congress Cataloging‐in‐Publication Data

Names: Tamime, A. Y., editor.
Title: Microbial toxins in dairy products / edited by Adnan Y. Tamime.
Other titles: Society of Dairy Technology series.
Description: Chichester, West Sussex, UK ; Hoboken, NJ : John Wiley & Sons, Inc., 2017. |
Series: Society of Dairy Technology series | Includes bibliographical references and index.
Identifiers: LCCN 2016032565 (print) | LCCN 2016033156 (ebook) | ISBN 9781118756430 (cloth) | ISBN 9781118823651 (pdf) | ISBN 9781118823149 (epub)
Subjects: | MESH: Dairy Products–microbiology | Bacterial Toxins–toxicity | Dairy Products–toxicity
Classification: LCC QR121 (print) | LCC QR121 (ebook) | NLM QW 85 | DDC 579.3/7–dc23
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Cover image: Dr O. Donkor

List of Contributors

Editor

Dr A.Y. Tamime
Dairy Science & Technology Consultant
Ayr
Scotland ‐ United Kingdom
Tel. +44 (0)1292 265498
Fax +44 (0)1292 265498
Mobile +44 (0)7980 278950
E‐mail: adnan@tamime.fsnet.co.uk

Contributors

Dr M.A. Alvarez
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Head of the Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985893418
Fax +34 985892233
E‐mail: maag@ipla.csic.es.

Dr J.W. Austin
Health Canada
Food Directorate
Health Products and Food Branch
Ottawa
Ontario
Canada
Tel. + 1 613 957‐0902
Fax +1 613 941‐0280
E‐mail: John.Austin@hc‐sc.gc.ca

Dr R. Condoleo
Istituto Zooprofilattico Sperimentale Lazio e Toscana
M. Aleandri
Roma
Italy
Tel. +39 06 79099360
Fax +39 06 79099312
E‐mail: roberto.condoleo@izslt.it

Dr M.‐L. Cortesi
Research Group of Food Inspection of Department of Veterinary Medicine and Animal Production
Napoli
Italy
Tel. +39 081 2536469
Fax +39 081 458683
E‐mail: cortesi@unina.it

Dr O. Donkor
Victoria University
Advanced Food Systems Research Unit
College of Health and Biomedicine
Werribee Campus
Melbourne
Victoria
Australia
Tel. + 61 (0)3 9919 8062
Fax + 61 (0)3 9919 8284
E‐mail: osaana.donkor@vu.edu.au

Dr R. Early
Harper Adams University
Department of Food Science and Agri‐Food Supply Chain Management
Newport
Shropshire
England – United Kingdom
Tel. +44 (0) 1952 815365
Mobile +44 (0) 7792 453319
Fax +44 (0) 1952 814783
E‐mail: rearly@harper‐adams.ac.uk & early818@btinternet.com

Dr M. Fernández
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985893352
Fax +34 985892233
E‐mail: mfernandez@ipla.csic.es

M. Hickey
Michael Hickey Associates Food Consultancy, Derryreigh
Creggane
Charleville
Co. Cork
Ireland
Tel. +353 (0)63 89392
Mobile +353 (0)87 2385653
E‐mail: hickeymfg@eircom.net

Dr V. Ladero
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985892131
Fax +34 985892233
E‐mail: ladero@ipla.csic.es

Dr F. Leroy
Vrije Universiteit
Research Group of Industrial Microbiology and Food Biotechnology (IMDO)
Faculty of Sciences and Bio‐engineering Sciences
Brussels
Belgium
Tel. +32 (0)2 6293612
Fax +32 (0)2 6292720
E‐mail: fleroy@vub.ac.be

Dr D.M. Linares
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985892131
Fax +34 985892233
E‐mail: daniml@ipla.csic.es

Dr R. Mercogliano
Research Group of Food Inspection of Department of Veterinary Medicine and Animal Production
Napoli
Italy
Tel. +39 081 2536062
Fax +39 081 458683
E‐mail: raffaella.mercogliano@unina.it

Dr N. Murru
Research Group of Food Inspection of Department of Veterinary Medicine and Animal Production
Napoli
ItalyTel. +39 081 2536062
Fax +39 081 458683
E‐mail: murru@unina.it

Dr H.I. El‐Nezami
University of Hong Kong
5S‐13 Kadoorie Biological Sciences Building
Hong Kong
Tel. +852 2299 0835
Fax +852 22990364
E‐mail: elnezami@hku.hk

Dr M.F. Peruzy
Research Group of Food Inspection of Department of Veterinary Medicine and Animal Production
Naples
Italy
Tel. + 0039 03 391884980
E‐mail: mariafrancesca.peruzy@gmail.com

Dr M. Pérez
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985892131
Fax +34 985892233
E‐mail: mpgarcia@ipla.csic.es

Dr L. Ramchandran
Victoria University
Advanced Food Systems Research Unit
College of Health and Biomedicine
Werribee Campus
Melbourne
Victoria
Australia
Tel. + 61 (0)3 9919 8062
Fax + 61 (0)3 9919 8284
E‐mail: lata.ramchandran@vu.edu.au

Dr B. del Rio
Spanish National Research Council (CSIC)
Dairy Research Institute (IPLA‐CSIC)
Department of Biotechnology of Dairy Products
Villaviciosa
Asturias
Spain
Tel. +34 985892131
Fax +34 985892233
E‐mail: beadelrio@ipla.csic.es

Dr N.P. Shah
University of Hong Kong
6N‐08, Kadoorie Biological Sciences Building
Dairy and Probiotic Unit
Food and Nutritional Science Programme
Hong Kong
Tel. +852 2299 0836
Fax +852 2559 9114E
E‐mail: npshah@hku.hk

Dr T. Vasiljevic
Victoria University
Advanced Food Systems Research Unit
College of Health and Biomedicine
Werribee Campus
Melbourne
Victoria
Australia
Tel. + 61 (0)3 9919 8062
Fax + 61 (0)3 9919 8284
E‐mail: todor.vasiljevic@vu.edu.au

Dr M.L.Y. Wan
University of Hong Kong
5S‐12 Kadoorie Biological Sciences Building
Hong Kong
Tel. +852 2299 0835
Fax +852 2299 0364
E‐mail: murphyly@connect.hku.hk

Dr A. Warnakulasuriya
Victoria University
Advanced Food Systems Research Unit
College of Health and Biomedicine
Werribee Campus
Melbourne
Victoria
Australia
Tel. + 61 (0)3 9919 8062
Fax + 61 (0)3 9919 8284
E‐mail: asalangika.warnakulasuriya@vu.edu.au

Preface

Food‐borne diseases, including dairy products, have been recognised as major threats to human health and can affect the national economies of both industrialised and developing countries worldwide. It can be argued that some of the causes associated with dairy food‐borne diseases are the use of raw milk in the manufacture of dairy products, faulty processing conditions during the heat treatment of milk, contamination of products after post‐processing, failure in due‐diligence (i.e. adding processed food to dairy products, for example, the case of botulism in hazel nut yoghurt in the United Kingdom), in‐adequate clean water supply, and so on. Primarily, dairy food‐borne diseases affecting human health are associated with certain strains of bacteria (e.g. belonging to the genera of Clostridium, Bacillus, Escherichia, Staphylococcus and Listeria) that are capable of producing toxins, plus moulds that are similarly capable of producing mycotoxins, such as aflatoxins, sterigmatocytin and ochratoxin. In addition, biogenic amines can accumulate in dairy products through microbial activity (e.g. starter cultures in cheeses), where the ingestion of high concentrations can be dangerous to human health.

Incidences of human illnesses associated with dairy products are relatively low compared with foodborne illnesses in general. The purpose of this book, which is written by a team of well‐known international scientists, is to review the latest scientific knowledge/developments in these fields, such as surveying the incidences of human illnesses caused by the consumption of dairy products, updating the analytical techniques required to examine bacterial and mould toxins, and the potential for contamination of milk as it passes along the food chain (i.e. from ‘farm‐to‐fork’). This is complemented by a review of current approaches used to model microbial growth and toxin production plus the associated risks, and the regulatory measures available in different countries for control of microbial toxins in dairy products. It is anticipated that this up‐dated information will help to further minimise the incidences of dairy food‐borne illnesses in humans.

I would like to acknowledge the time and effort that the expert contributors have given to make this edition possible. Although some overlap of scientific data have occurred in some chapters, I have felt justified in allowing this overlap because it has resulted in making the chapter(s) easier to read and understand.

Adnan Y. Tamime
October 2015