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Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP001

2nd Edition
The Comet Assay in Toxicology
 View Online

Issues in Toxicology

Series Editors:
Professor Diana Anderson, University of Bradford, UK
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP001

Dr Michael D. Waters, Michael Waters Consulting, N. Carolina, USA

Dr Timothy C. Marrs, Edentox Associates, Kent, UK

Advisor to the Board:

Professor Alok Dhawan, CSIR-Indian Institute of Toxicology Research,
Lucknow, India

Titles in the Series:

1: Hair in Toxicology: An Important Bio-Monitor
2: Male-mediated Developmental Toxicity
3: Cytochrome P450: Role in the Metabolism and Toxicity of Drugs and
other Xenobiotics
4: Bile Acids: Toxicology and Bioactivity
5: The Comet Assay in Toxicology
6: Silver in Healthcare
7: In Silico Toxicology: Principles and Applications
8: Environmental Cardiology
9: Biomarkers and Human Biomonitoring, Volume 1: Ongoing Programs
and Exposures
10: Biomarkers and Human Biomonitoring, Volume 2: Selected Biomarkers
of Current Interest
11: Hormone-Disruptive Chemical Contaminants in Food
12: Mammalian Toxicology of Insecticides
13: The Cellular Response to the Genotoxic Insult: The Question of
Threshold for Genotoxic Carcinogens
14: Toxicological Effects of Veterinary Medicinal Products in Humans:
Volume 1
15: Toxicological Effects of Veterinary Medicinal Products in Humans:
Volume 2
16: Aging and Vulnerability to Environmental Chemicals: Age-related
Disorders and their Origins in Environmental Exposures
17: Chemical Toxicity Prediction: Category Formation and Read-Across
18: The Carcinogenicity of Metals: Human Risk Through Occupational and
Environmental Exposure
19: Reducing, Refining and Replacing the Use of Animals in Toxicity Testing
20: Advances in Dermatological Sciences
21: Metabolic Profiling: Disease and Xenobiotics
22: Manganese in Health and Disease
23: Toxicology, Survival and Health Hazards of Combustion Products
24: Masked Mycotoxins in Food: Formation, Occurrence and Toxicological
Relevance
 View Online

25: Aerobiology: The Toxicology of Airborne Pathogens and Toxins

26: Chemical Warfare Toxicology, Volume 1: Fundamental Aspects
27: Chemical Warfare Toxicology, Volume 2: Management of Poisoning
28: Toxicogenomics in Predictive Carcinogenicity
29: Human Stem Cell Toxicology
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30: The Comet Assay in Toxicology, 2nd Edition

How to obtain future titles on publication:

A standing order plan is available for this series. A standing order will bring
delivery of each new volume immediately on publication.

For further information please contact:

Book Sales Department, Royal Society of Chemistry, Thomas Graham House,
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 View Online

The Comet Assay in Toxicology

2nd Edition
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP001

Edited by

Alok Dhawan
CSIR-Indian Institute of Toxicology Research, Lucknow, India
Email: [email protected]

Diana Anderson
University of Bradford, UK
Email: [email protected]
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP001 View Online

Issues in Toxicology No. 30

Print ISBN: 978-1-78262-287-1

PDF eISBN: 978-1-78262-289-5
EPUB eISBN: 978-1-78262-915-3
ISSN: 1757-7179

A catalogue record for this book is available from the British Library

r The Royal Society of Chemistry 2017

All rights reserved

Apart from fair dealing for the purposes of research for non-commercial purposes or for
private study, criticism or review, as permitted under the Copyright, Designs and Patents
Act 1988 and the Copyright and Related Rights Regulations 2003, this publication may not
be reproduced, stored or transmitted, in any form or by any means, without the prior
permission in writing of The Royal Society of Chemistry or the copyright owner, or in the
case of reproduction in accordance with the terms of licences issued by the Copyright
Licensing Agency in the UK, or in accordance with the terms of the licences issued by
the appropriate Reproduction Rights Organization outside the UK. Enquiries concerning
reproduction outside the terms stated here should be sent to The Royal Society of
Chemistry at the address printed on this page.

The RSC is not responsible for individual opinions expressed in this work.

The authors have sought to locate owners of all reproduced material not in their own
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Published by The Royal Society of Chemistry,

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Printed in the United Kingdom by CPI Group (UK) Ltd, Croydon, CR0 4YY, UK
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP007

Preface

This book is the first of its kind to be devoted exclusively to the Comet assay
and its applications as an important tool in current toxicology. This multi-
author book will serve as both a reference and a guide for investigators in
the biomedical, biochemical and pharmaceutical sciences. Specialists from
the fields of genetic toxicology and human epidemiology, with first-hand
knowledge of their chosen sub-specialities, have contributed to this peer-
reviewed scientific venture.
The simplicity, rapidity, versatility and ease of application of the Comet
assay have made it a favourite amongst researchers and it is now also
gaining acceptance amongst regulators. It can be used with all single cells
from prokaryotes and eukaryotes, plants and animals, including humans,
both somatic and germ cells. It is also a relatively inexpensive assay to
perform.
The book is divided into different sections, reflecting the range of interest
in the exploitation of this assay. It begins with an introductory section
reviewing the genesis of the assay for those new to the technique, and details
the various fields in which it finds wide acceptance. This sets the scene by
explaining why the assay has become the most sensitive and sought after
assay in modern toxicology.
There is a section that describes the protocols being followed to assess
various types of DNA damage in different cell types. The third section brings
together the specific applications of the assay in diverse areas ranging from
genetic toxicity testing to human monitoring and environmental toxicology.
The last section considers strategies for the conduct of the assay using
in vitro and in vivo systems, based on internationally accepted guidelines.
The book draws to be a close with an assessment of image-analysis
principles and the statistics used for evaluating the data generated by
the assay.

Issues in Toxicology No. 30

The Comet Assay in Toxicology, 2nd Edition
Edited by Alok Dhawan and Diana Anderson
r The Royal Society of Chemistry 2017
Published by the Royal Society of Chemistry, www.rsc.org

vii
 View Online

viii Preface

This book is a culmination of over fifteen years of active collaboration

and friendship between the editors and provides a good basic understanding
of issues relating to the assay.

Alok Dhawan
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP007

Diana Anderson
Published on 07 October 2016 on http://pubs.rsc.org | doi:10.1039/9781782622895-FP009

Contents

Section I: Genesis of Comet Assay

Chapter 1 The Comet Assay: A Versatile Tool for Assessing DNA

Damage 3
Mahima Bajpayee, Ashutosh Kumar and Alok Dhawan

1.1 Introduction 3
1.1.1 Bacteria 5
1.2 Plant Models 5
1.2.1 The Comet Assay in Lower Plants and Fungi 5
1.2.2 The Comet Assay in Higher Plants 8
1.3 Animal Models 10
1.3.1 Lower Animals 10
1.4 Higher Animals 18
1.4.1 Vertebrates 18
1.5 The Specificity, Sensitivity and Limitations of the
Comet Assay 32
1.6 Conclusions 34
References 35

Section II: Various Procedures for the Comet Assay

Chapter 2 High-throughput Measurement of DNA Breaks and

Oxidised Bases with the Comet Assay 67
Amaya Azqueta, Isabele Campos Costa-Amaral and
Andrew R. Collins

2.1 Introduction 67

Issues in Toxicology No. 30

The Comet Assay in Toxicology, 2nd Edition
Edited by Alok Dhawan and Diana Anderson
r The Royal Society of Chemistry 2017
Published by the Royal Society of Chemistry, www.rsc.org

ix
 View Online

x Contents

2.2 Methods for Measuring DNA Oxidation Damage 69

2.3 Enzyme Specificity 71
2.4 Applications 73
2.5 Protocol 76
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2.5.1 Equipment 76
2.5.2 Supplies 76
2.5.3 Reagents, Buffers and Enzymes 77
2.5.4 Procedure 78
Acknowledgements 87
References 87

Chapter 3 Microplate-based Comet Assay 93

Elizabeth D. Wagner and Michael J. Plewa

3.1 Introduction 93
3.2 Microplate Comet Assay 94
3.3 Drinking-water Disinfection Byproducts 94
3.4 Chinese Hamster Ovary Cells 96
3.5 CHO Cell Microplate Comet Assay Protocol 96
3.5.1 CHO Cell Treatment 96
3.5.2 Preparation of Comet Microgels 97
3.5.3 Comet Microscopic Examination 98
3.5.4 Normalisation of CHO Cell Comet Data and
Statistical Analysis 99
3.6 Utility of the Microplate Comet Assay in Comparing
Classes of DBPs 101
3.6.1 Microplate Comet Analysis of the
Haloacetonitriles 102
3.6.2 Microplate Comet Analysis of the
Haloacetamides 103
3.6.3 Comparison of SCGE Genotoxic Potency
Values of the Haloacetonitriles and
Haloacetamides 105
3.7 Advantages of the Mammalian Cell Microplate
Comet Assay 105
Acknowledgements 106
References 106

Chapter 4 The Use of Higher Plants in the Comet Assay 112

Tomas Gichner, Irena Znidar, Elizabeth D. Wagner and
Michael J. Plewa

4.1 Introduction 112

 View Online

Contents xi

4.2 Differences between the Animal and Plant

Comet Assay 113
4.3 Cultivation and Treatment of Plants for the
Comet Assay 113
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4.3.1 Onion (Allium cepa) 113

4.3.2 Tobacco (Nicotiana tabacum) 114
4.3.3 Broad Bean (Vicia faba) 114
4.3.4 Plants Used for In situ Studies 114
4.4 Isolation of Nuclei from Plant Tissues 115
4.4.1 Isolation of Nuclei via Protoplast
Formation 115
4.4.2 Isolation of Nuclei by Mechanical
Destruction of the Cell Wall 115
4.5 Preparation of Comet Assay Slides 115
4.6 DNA Unwinding and Electrophoresis 116
4.7 DNA Staining 117
4.8 Reading the Slides, Expressing DNA Damage,
Statistics 117
4.9 Comet Assay Procedure 118
4.10 Reagents, Media, Buffers 119
4.11 Equipment and Software 121
4.12 Determination of Toxicity 121
4.13 Correlation between the DNA Damage Evaluated
by the Comet Assay and Other Genetic Endpoints
in Plants 122
4.14 The Utility of the Comet Assay for Genotoxic
Studies in the Laboratory 122
4.15 The Utility of the Comet Assay as an In situ Marker 126
4.16 Comet Assay with Irradiated Food of Plant Origin 127
4.17 Recommendations for Plant Comet Assay Users 127
Abbreviations 128
References 128

Chapter 5 Methods for Freezing Blood Samples at 80 1C for DNA

Damage Analysis in Human Leukocytes 134
Narendra P. Singh and Henry C. Lai

5.1 Introduction 134

5.2 Materials and Methods 135
5.2.1 Protocol I 135
5.2.2 Protocol II 136
5.2.3 Fresh Blood 136
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xii Contents

5.2.4 Fresh Blood Stored on Ice Prior to Freezing 136

5.2.5 Image and Data Analysis 137
5.3 Results and Discussion 137
References 141
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Chapter 6 Development and Applications of the Comet-FISH Assay

for the Study of DNA Damage and Repair 143
Valerie J. Mckelvey-Martin and Declan J. Mckenna

6.1 Introduction 143

6.2 The Comet-FISH Assay Procedure 144
6.3 Applications of the Comet-FISH Assay 149
6.3.1 Discovery of the Comet-FISH Assay 149
6.3.2 Using Comet-FISH to Measure DNA Damage 149
6.3.3 Using Comet-FISH to Quantify DNA Repair 155
6.3.4 Summary of Studies 156
6.4 Limitations of Comet-FISH Assay 157
6.4.1 Practical Difficulties 157
6.4.2 Imaging Difficulties 157
6.4.3 Interpretation of Results 158
6.5 Conclusion 159
References 159

Chapter 7 Detection of DNA Damage in Different Organs

of the Mouse 164
Ritesh Kumar Shukla, Mahima Bajpayee and Alok Dhawan

7.1 Introduction 164

7.2 The Alkaline Comet Assay in Multiple Organs of Mice 165
7.2.1 Chemicals and Materials 166
7.2.2 Methodology 169
7.3 Conclusions 172
Acknowledgements 173
References 173

Chapter 8 Detection of DNA Damage in Drosophila 177

Ashutosh Kumar, Mahima Bajpayee and Alok Dhawan

8.1 Introduction 177

8.2 General Protocol for the Assessment of DNA
Damage Using the Alkaline Comet Assay 178
8.2.1 Chemicals and Materials 178
8.2.2 Preparation of Reagents 180
 View Online

Contents xiii

8.2.3 Preparation of Agarose Coated (Base) Slides

for the Comet Assay 181
8.2.4 Preparation of Microgel Slides for the
Comet Assay 181
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8.2.5 Electrophoresis of Microgel Slides 182

8.2.6 Evaluation of DNA Damage 183
8.3 The Alkaline Comet Assay in Drosophila
melanogaster 183
8.3.1 Chemicals and Materials 184
8.3.2 Methodology 184
8.4 Conclusion 187
Acknowledgements 188
References 188

Section III: Applications of Comet Assay

Chapter 9 The Comet Assay: Clinical Applications 195

M. M. Piperakis, K. Kontogianni and S. M. Piperakis

9.1 Introduction 195

9.2 The Comet Assay Methodology 196
9.3 Clinical Studies 197
9.4 Discussion and Conclusions 229
References 230

Chapter 10 Applications of the Comet Assay in Human

Biomonitoring 238
Andrew R. Collins and Maria Dusinska

10.1 Biomonitoring and Biomarkers – An Introduction 238

10.2 The (Modified) Comet Assay 239
10.3 Guidelines for Biomonitoring Studies 240
10.4 Biomonitoring with the Comet Assay: Special
Considerations 241
10.4.1 Surrogate and Target Cells; The Use of
White Blood Cells 242
10.4.2 Sampling Time and Transport 242
10.4.3 Reference Standards 243
10.4.4 What Affects the Background Level of
DNA Damage? 244
10.5 DNA Damage as a Marker of Environmental
Exposure and Risk 244
10.6 DNA Repair as a Biomarker of Individual
Susceptibility 245
 View Online

xiv Contents

10.7 Protocols 246

10.7.1 Protocol for Blood Sample Collection and
Long-term Storage of Lymphocytes for
the Measurement of DNA Damage and
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Repair 246
10.7.2 Comet Assay – Determination of DNA
Damage (Strand Breaks and Oxidised
Bases) 249
10.7.3 In vitro Assays for DNA Repair 252
10.8 Solutions, etc. 254
10.8.1 Lysis Solution 254
10.8.2 Buffer F (Enzyme Reaction Buffer for
FPG, Endonuclease III, and In vitro
BER Assay) 254
10.8.3 Buffer F þ Mg (Used for In vitro
NER Assay) 254
10.8.4 Buffer A (Used in In vitro
Repair Assays) 254
10.8.5 Triton Solution 255
10.8.6 Ro 19-8022 (Photosensitiser) 255
10.8.7 Electrophoresis Solution 255
10.8.8 Neutralising Buffer 255
10.8.9 Agarose 255
10.8.10 Enzymes 255
10.9 Analysis and Interpretation of Results 256
10.9.1 Quantitation 256
10.9.2 Calculation of Net Enzyme-sensitive Sites 257
10.9.3 Calibration 257
10.9.4 How to Deal with Comet Assay Data
Statistically 257
10.10 Conclusions 258
Acknowledgements 258
References 259

Chapter 11 Comet Assay in Human Biomonitoring 264

Mahara Valverde and Emilio Rojas

11.1 Introduction 264

11.2 Human Monitoring 265
11.3 Environmental Exposure 268
11.4 Lifestyle Exposure 273
11.5 Occupational Exposure 276
 View Online

Contents xv

11.6 Reviews 288

11.7 Usefulness of the Comet Assay in Human
Monitoring 291
11.8 Conclusions 292
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References 293

Chapter 12 Use of Single-cell Gel Electrophoresis Assays in Dietary

Intervention Trials 314
Armen Nersesyan, Christine Hoelzl, Franziska Ferk,
Miroslav Mišı́k, Halh Al-Serori, Tahereh Setayesh and
Siegfried Knasmueller

12.1 Introduction 314

12.2 Different Endpoints 315
12.3 Experimental Design of Human Studies 315
12.4 Indicator Cells and Media 318
12.5 Conventional SCGE Trials With Complex Foods
and Individual Components—The Current State of
Knowledge 319
12.5.1 Definition of the Quality Score (QS) 319
12.6 Use of SCGE Trials to Detect Protection Against
DNA-reactive Carcinogens 319
12.7 Use of SCGE-experiments to Monitor Alterations of
the DNA-repair Capacity (Base- and
Nucleotide-excision Repair) 333
12.8 What Have We Learned From Intervention Studies
So Far? 333
12.9 Future Perspectives 337
12.9.1 Hot Topics 337
12.9.2 Detection of Antioxidants 338
12.9.3 Standardization 338
12.9.4 Search for Mechanistic Explanations 339
12.9.5 Interpretation Problems 339
References 341

Chapter 13 The Application of the Comet Assay in Aquatic

Environments 354
G. Frenzilli, T. P. Bean and B. P. Lyons

13.1 Introduction 354

13.2 Protocols, Cell Types and Target Organs 356
 View Online

xvi Contents

13.3 Application of the Comet Assay to Invertebrate

Species 357
13.3.1 Freshwater Invertebrates 357
13.3.2 Marine Invertebrates 358
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13.4 Application of the Comet Assay to Vertebrate

Species 359
13.4.1 Freshwater Vertebrates 359
13.4.2 Marine Vertebrates 360
13.5 Conclusions 361
References 361

Chapter 14 The Alkaline Comet Assay in Prognostic Tests for Male

Infertility and Assisted Reproductive Technology
Outcomes 369
Sheena E. M. Lewis and Ishola M. Agbaje

14.1 Introduction 369

14.2 Sites of DNA Damage in Sperm 370
14.2.1 Oxidative Stress, a Major Cause of DNA
Damage 371
14.2.2 Oxidative Stress, Antioxidant Therapies 372
14.2.3 Sperm DNA Damage Tests 372
14.2.4 Modifications to the Alkaline Comet Assay
for Use with Sperm 373
14.2.5 Sperm DNA Adducts and their
Relationship with DNA Fragmentation 375
14.3 Can Sperm DNA Integrity Predict Success?
Relationships with Assisted Conception Outcomes 376
14.4 Clinically Induced DNA Damage 377
14.4.1 Cryopreservation 378
14.4.2 Vasectomy 379
14.5 A Major Barrier to Progress 379
14.6 Opportunities and Challenges – The
Establishment of Clinical Thresholds and the
Integration of DNA Testing into Clinical Practice 379
Acknowledgements 380
References 380

Chapter 15 The Comet Assay in Sperm—Assessing Genotoxins in Male

Germ Cells 390
Adolf Baumgartner, Aftab Ali, Charmaine Normington and
Diana Anderson

15.1 Introduction 390

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