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BREAST MRI
IN
PRACTICE

Edited by

Ruth Warren
Consultant Radiologist
Department of Radiology
Addenbrooke’s NHS Trust
Cambridge, UK

Alan Coulthard
Consultant Radiologist
MRI Unit
Royal Victoria Infirmary
Newcastle-upon-Tyne, UK

MARTIN DUNITZ
© 2002 Martin Dunitz Ltd, a member of the Taylor & Francis group

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Contents

Contributors vii
Foreword ix
Adrian K Dixon

1 Introduction 1
Alan Coulthard, Ruth Warren

Section I Breast MRI: Technique

2 Physical basis of magnetic resonance imaging 3
Thomas W Redpath, Carmel Hayes
3 Equipment requirements 19
Carmel Hayes, Thomas W Redpath
4 Breast MRI protocols 29
Carmel Hayes, Thomas W Redpath
5 Contrast agent dynamics in breast MRI 43
Anwar R Padhani
6 Radiographic aspects of breast MRI 55
Philip T English, Alan Coulthard
7 Reporting of the breast MRI examination 63
Alan Coulthard

Section II The Non-Operated Breast

8 Magnetic resonance imaging of the normal breast 73
Margaret Hall-Craggs, Gita Ralleigh
9 Benign breast disease 81
Sheila Rankin
10 Primary breast cancer 97
Lindsay W Turnbull, Alan Coulthard
11 The axilla 119
Alison D Murray

Section III The Operated Breast

12 Treatment-induced changes 131
Niall Moore
13 Detection of disease recurrence 139
Preminda Kessar, Anwar R Padhani
vi CONTENTS

14 Monitoring of neoadjuvant chemotherapy 155

Fiona J Gilbert
15 The augmented and reconstructed breast 161
Jane Potterton

Section IV Practical Issues in Breast MRI

16 Localization of lesions with breast MRI 177
Ruth Warren, Alan Coulthard
17 Pitfalls 189
Alan Coulthard
18 Problem-solving with breast MRI 199
Ruth Warren, Lynda Bobrow, Peter Britton and
The Cambridge Breast Unit

Section V Perspectives on Breast MRI

19 Breast MRI and screening 227
Martin O Leach, Preminda Kessar
20 A surgical perspective of breast MRI 237
Michael Douek, Michael Baum
21 Psychological aspects of MRI 247
Jennifer Anderson, Leslie Walker
22 Cost-effectiveness of breast MRI 251
Jacqueline Brown
23 Future development in breast MRI 257
David J Lomas

Index 261
Contributors

Jennifer Anderson Alan Coulthard

Health Psychologist Consultant Radiologist
Centre for Magnetic Resonance MRI Unit
Investigations Royal Victoria Infirmary
Hull Royal Infirmary Queen Victoria Road
Anlaby Road Newcastle-upon-Tyne
Hull NE1 4LP
HU3 2JZ
Michael Douek
Michael Baum Lecturer in Surgery and
Emeritus Professor of Surgery Honorary Specialist Registrar
Academic Department of Surgery Royal Free and University
University College of London College Medical School
Charles Bell House Academic Department of
67-73 Riding House Street Surgery
London 67-73 Riding House Street
W1P 7LD London
W1P 7LD
Lynda Bobrow
Lecturer in Histopathology
Philip T English
University of Cambridge
Superintendent Radiographer
Addenbrooke’s Hospital
MRI Unit
Hills Road
Victoria Wing Radiology Department
Cambridge
Royal Victoria Infirmary
CB2 2QQ
Newcastle-upon-Tyne
NE1 4LP
Peter Britton
Consultant Radiologist
Department of Radiology Fiona J Gilbert
Addenbrooke’s Hospital Professor of Radiology
Hills Road Department of Radiology
Cambridge University Medical School
CB2 2QQ Foresterhill Annex
Aberdeen
Jacqueline Brown AB9 2ZD
MRC Senior Scientist in Health Economics
MRC Health Services Research Margaret Hall-Craggs
Collaboration Consultant Radiologist
Department of Social Medicine Imaging Department
Canynge Hall UCL Hospitals NHS Trust
University of Bristol The Middlesex Hospital
Whiteladies Road London
Bristol W1N 8AA
BS8 2PR
viii CONTRIBUTORS

Carmel Hayes Jane Potterton

Study Physicist Consultant Radiologist
Section of Magnetic Resonance MRI Unit
Institute of Cancer Research Victoria Wing Radiology Department
The Royal Marsden NHS Trust Royal Victoria Infirmary
Sutton Newcastle-upon-Tyne
Surrey SM2 5PT NE1 4LP

Preminda Kessar Gita Ralleigh

Consultant Radiologist Specialist Registrar and Fellow in Breast Imaging
Section of Magnetic Resonance Imaging Kings College Hospital
Royal Marsden NHS Trust Denmark Hill
Downs Road London
Sutton SE5 9RJ
Surrey
SM2 5PT Sheila Rankin
Clinical Director
Martin O Leach Department of Radiology
Section Chairman Guy’s Hospital
CRC Magnetic Resonance Research Group St Thomas Street
Royal Marsden NHS Trust London
Downs Road, Sutton SE1 9RT
Surrey SM2 5PT
Thomas W Redpath
David J Lomas Reader, Department of
Professor of MRI Bio-Medical Physics and
University of Cambridge Bio-Engineering
Addenbrooke’s NHS Trust University of Aberdeen
Hills Road Foresterhill
Cambridge Aberdeen
CB2 2QQ AB25 2ZD

Niall Moore Lindsay W Turnbull

University Lecturer in Radiology Professor of Radiology and Scientific Director of the
and Honorary Consultant Radiologist Centre for Magnetic Resonance
University of Oxford and Oxford Radcliffe Hospital Investigations
MRI Centre, Headington Hull Royal Infirmary
Oxford OX3 9DU Anlaby Road
Hull
Alison D Murray HU3 2JZ
Senior Lecturer in Radiology
University of Aberdeen Leslie G Walker
Lillian Sutton Building Director, Institute of Rehabilitation
Foresterhill University of Hull
Aberdeen 215 Anlaby Road
AB25 2AY Hull
HU3 2PG
Anwar R Padhani
Consultant Radiologist Ruth Warren
Paul Strickland Scanner Centre Consultant Radiologist
Mount Vernon Hospital Department of Radiology
Rickmansworth Road Addenbrooke’s NHS Trust
Northwood Hills road
Middlesex Cambridge
HA6 2RN CB2 2QQ
Foreword
ADRIAN K DIXON

It is a great pleasure to prepare a foreword to this continues research into breast disease and this
practical book on breast MRI, which will prove a real includes the role of study radiologist to the Medical
asset to those entering this exciting field. The book is Research Council’s multicentre UK trial of MRI
timely for several reasons. First, many of the initial Screening for Breast Cancer (MARIBS). Both authors
technical difficulties of breast MRI have been over- are members of the study advisory group of the
come, and most manufacturers now offer appropriate MARIBS study. Alan Coulthard, a graduate with first
coils and sequences. Second, an increasing number of class honours from Newcastle University and a surg-
MRI units are starting to offer this extension to their ical background, is also a dedicated academic and
armamentarium. Hence the urgent need for a straight- research-minded radiologist. His interest in education
forward text, which should be of interest to all radi- suits him for expounding complex developing tech-
ologists and radiographers involved in the practical nology to professionals in training. Like many radi-
procedures, and to other health care professionals ologists in the UK, he has been instrumental in setting
who wish for more information about this rapidly up and then running an MRI Unit in a major teaching
evolving subject. It would appear that these various hospital. He is therefore fully aware of the pressures
needs are handsomely covered in this volume. on MRI services, particularly from the neurosciences
The editors, Ruth Warren and Alan Coulthard, have and orthopaedics.
assembled a cast of experts in the field. They have As with many other developments in MRI, breast
persuaded these contributors to keep to their remit so studies often have to be squeezed in around the
that, in a manageably sized volume, all the pertinent margins of the working day. The onerous analysis of
points of breast MRI are well covered. Even in this the images is often performed at night or at weekends.
area, where technical improvements are almost a Just consider the time taken to analyse the data from
daily occurrence, this book will remain the practical one breast MRI study, with 600 images, compared
‘Bible’ for several years to come. with that from a standard spine MR examination!
The two editors have vast experience. Ruth Warren Between them, Ruth Warren and Alan Coulthard are
has had an outstanding and varied career. As a radi- exceptionally well qualified to put together this splen-
ologist in Harlow she contributed to many major did and attractive volume, which will be so helpful to
radiological developments, including the installation all and sundry. It is not improbable, in these days of
of MRI. While managing the service, including a spell glasnost and consumerism, that informed patients
as Medical Director, she led mammographic services undergoing the procedure may buy this relatively
at Epping, from where numerous key scientific inexpensive book and may ask very pertinent ques-
papers emanated. This work on health technology tions. This is not really the reason why all involved in
assessment of screening mammography culminated in this subject should know the contents of the book,
her MD thesis, which was awarded the Ralph Noble though! They should read (and perhaps buy) Breast
prize from the University of Cambridge. Working at MRI in Practice because of a deep interest in this
Addenbrooke’s Hospital, Cambridge since 1996, she rapidly developing and important subject.
Chapter 1 Introduction
ALAN COULTHARD AND RUTH WARREN

Over the last decade we have seen breast MRI assemble some of the leading lights in UK breast MRI
develop from a technique appropriate only to a to give of their particular expertise. We have selected
limited number of research institutions, to a clinically authors not only for their excellence in particular
useful imaging tool. Breast MRI currently has an aspects of the technique, but also because we feel
established and definite role in some clinical situ- that they share our enthusiasm for the subject, as well
ations (e.g. evaluation of breast prostheses, assess- as our view of the future prospects for breast MRI.
ment of the post-surgical breast) and is rapidly It is hoped that Breast MRI in Practice may become
defining its role in others. As breast MRI passes from a practical bench book for many professionals. The
the research situation to the clinical situation, it is book is aimed primarily at radiologists and radi-
clear to us that the driving force for further develop- ographers who may be new to breast MRI (or even to
ment of the technique will lie not with researchers MRI itself). We hope that the book will offer a com-
with an interest in a particular imaging modality prehensive guide to breast MRI for radiologists in
(MRI), but with clinicians involved in the whole training. We also hope that other members of the
scope of breast diagnosis, supported by the multi- breast team, from breast clinicians to breast care
disciplinary breast team. Clearly, as the role of breast nurses, will feel able to dip into this volume to pursue
MRI expands, many more radiologists, currently particular issues. The book has been planned so that
involved in breast imaging but not necessarily expe- readers may encounter information on several levels.
rienced in MRI, will become involved with the tech- Each chapter has been written with an eye to both
nique. For those radiologists, and for all professionals ‘small print’ and ‘large print’ facts. Where appropriate,
involved in both breast imaging and the care of the latter have been organized into a series of ‘take
patients with breast disease, we hope this book will home’ points. These, combined with the illustrations
prove timely. and figures, as well as the comprehensive index
One of us (RW) is a radiologist with many years of should provide easy access for quick reference. For
experience in breast imaging, who has been drawn to those who like to trawl the original literature, the
breast MRI by the exciting possibilities of the tech- chapters are well referenced. The published literature
nique. The other (AC) is a radiologist with a primary on breast MRI is now large, and so readers may find
interest in MRI, who after many years of experience useful the list of recent review articles that follow this
in breast MRI has become involved with the wider introduction.
field of breast imaging and now participates in the There are certain inherent advantages and dis-
NHS Breast Screening Programme. We hope that our advantages to a multi-author book. The major ad-
personal approach to the subject, from diametrically vantage must be the multidisciplinary representation
opposite backgrounds, will be reflected in the scope amongst the authors, so that the subject is covered
of this book. Like our intended readership, we see from all perspectives. Undoubtedly there is some
ourselves as practical and pragmatic radiologists who overlap between chapters, but there is benefit in this.
do our utmost to keep our eye firmly on the clinical In most cases chapters are intended to be ‘stand
problem. alone’, and may be read without too many distract-
As editors of Breast MRI in Practice, we have been ing cross-references to other parts of the book,
fortunate, indeed, to be able to draw on our exten- except where major issues are more appropriately
sive personal networks of workers in the field covered elsewhere. The other advantage of the
of breast MRI. In this volume we have been able to multidisciplinary approach is that the two extremes
2 INTRODUCTION

of the subject – pragmatic problem solving of breast appearances encountered when applying the tech-
imaging dilemmas in a clinical setting and improve- nique may impair the utility of breast MRI. There is a
ment of the sensitivity and specificity of the tech- ‘problem solving’ chapter showing how MRI might be
nique using a quantitative approach in a research integrated with all the more traditional forms of breast
setting – may both be examined. This difference in diagnosis, illustrated with example cases where MRI
approach is well represented in this book. The full has been found to be helpful in achieving either the
value of breast MRI will be achieved when these two diagnosis or the information needed to treat the
approaches come together to enhance patient care in patient.
a realistic way. As this knowledge is still being devel- Breast MRI will only be used widely if it is consid-
oped, the emphasis and conclusions presented in ered to be useful by those clinicians who care for
this edition may well be subject to future changes. patients with breast disease, at an affordable and
Breast MRI in Practice is divided into five sections. justifiable price; and only then if it is acceptable to
Section I contains a group of papers covering the patients. Section V has been written by those people
science of breast MRI, along with practical guidelines best qualified to make these judgements: the clin-
on how decisions are made on the most appropriate icians, psychologists and health economists who
techniques to use. There is no ‘best method’ of con- research in the field of breast cancer. The surgical per-
ducting a breast MRI examination, and so choices spective is provided by a team who are well known
must be made. The chapters in Section I should help for challenging assumptions in the management of
with those choices, and a chapter on current thinking breast disease. The topic of screening using breast
and debate on the mode of reporting breast MRI MRI is discussed by writers who are actively involved
studies is included. in researching this topic. The impact of breast MRI on
Sections II and III carry a systematic analysis of the the patient, and the cost-effectiveness of the technique
use and findings of breast MRI in breast disease. are also discussed in this section. Finally, speculation
Section II focuses on the non-operated breast, cover- on future directions in breast MRI has been provided
ing breast MRI appearances in the normal subject, by an acknowledged expert in MRI, who understands
benign breast disease, the major topic of breast MRI the potential of the developing technology, and the
in primary breast cancer and concluding with a clinical context in which it is used.
chapter on MRI appearances in the axilla. Section III This book covers a major area of patient investiga-
covers the operated breast. In this section the issues tion in support of defeating a disease that is currently
of disease recurrence, treatment-induced changes to the major cause of death of women aged between 40
the breast, the monitoring of complex modern treat- and 65 years in the countries of the developed world.
ments currently used in women with breast cancer Although progress has been made, breast MRI has yet
and the appearances of the reconstructed breast are to find its true place in the investigation of breast
addressed. disease. The role of this book is to provide accessible
Section IV is intended to be highly practical in knowledge of the technique of breast MRI for those
content and has been illustrated freely. This section professionals who provide care to patients with dis-
demonstrates how practical issues and confusing orders of the breast.

FURTHER READING

Harms SE (1998) Breast magnetic resonance imaging. Semin Newstead GM, Weinreb JC (1995) Critical pathways for the future:
Ultrasound CT MR 19: 104–20. MR imaging and digital mammography. Radiographics
Heywang-Kobrunner SH, Heinig A, Pickuth D et al (2000) 15: 951–62.
Interventional MRI of the breast: lesion localisation and Weinreb JC, Newstead G (1995) MR imaging of the breast.
biopsy. Eur Radiol 10: 36–45. Radiology 196: 593–610.
Kuhl CK (2000) MRI of breast tumors. Eur Radiol 10: 46–58.
Section I
Breast MRI: Technique
Chapter 2 Physical basis of magnetic
resonance imaging
THOMAS W REDPATH AND CARMEL HAYES

NUCLEAR SPINS

Nuclei are positively charged. Some have a property

SPINNING TOP
termed spin and are called nuclear spins. A nuclear
spin generates a magnetic field in the same way that
a current circulating round a loop will generate a
magnetic field, rather like a tiny bar magnet. Magnetic
resonance images are normally formed from signals a
arising from hydrogen nuclei (1H), mainly because
they are so much more abundant in the body than
any other nucleus capable of undergoing nuclear
magnetic resonance (NMR) and so give a much
stronger signal.
Normally, nuclear spins do not have any preferred NUCLEAR SPIN
direction of alignment. If, however, they are placed in B0
a strong magnetic field B0, they will tend to align with
it, in much the same way as a set of compass needles
will align with the earth’s magnetic field. We do not
observe the effects of individual nuclei, we observe
b
the averaged effects of many billions of nuclei (in a
single millilitre of water, there are 3.3 × 1022 water Figure 2.1. The physics of a spinning top (a) precessing
molecules, and therefore 6.6 × 1022 hydrogen nuclei). around the vertical earth’s gravitational field is a good
The partial alignment of nuclear spins brought analogy to the Larmor precession of a nuclear spin around
about by the strong magnetic field B0 produces ‘bulk’ an applied magnetic field B0 (b).
nuclear magnetization. ‘Bulk’ means averaged over a
volume. If there were no alignment of the nuclear
spins, the bulk magnetization M would be zero and
nuclear magnetic resonance, or magnetic resonance initial alignment with the earth’s gravitational field,
imaging (MRI), would not be possible. then it precesses around a vertical axis through its
point of contact with the table. The precession is a
much slower (in terms of revolutions per second)
NUCLEAR PRECESSION motion than the spin of the top around its own axis.
Similarly, if the nuclear magnetization M is perturbed
from its alignment with B0, it precesses around the z-
The magnetization M has a preferred alignment par- axis, the direction of the static field. In NMR the pre-
allel to B0, which (by long established convention) is cession frequency f0 is often referred to as the Larmor
called the z-axis. The gyroscope, or spinning top, is a frequency and is given by:
good analogy to the behaviour of the nuclear mag-
netization (Figure 2.1). If the top is perturbed from its f0 =
B0 / 2 (2.1)
6 PHYSICAL BASIS OF MRI

where
is the gyromagnetic ratio (which has units of initially parallel to B0, it will be rotated to be anti-par-
radians per second per Tesla, hence the factor 2). allel with B0 (Figure 2.2b). M has direction as well as
The formula states that f0 is directly proportional to size and is therefore a vector.
field strength. Protons precess at 42.6 MHz in a mag-
netic field of strength 1 Tesla (T), at 63.9 MHz at
1.5 T and so on. Other nuclei have very different RELAXATION IN NMR
values for
. For instance phosphorus nuclei with an
atomic weight of 31 (31P) give an NMR signal often
used for in vivo NMR spectroscopy, and have a If the nuclear magnetization M is moved away from its
Larmor frequency of 17.2 MHz in a field of 1 T. natural alignment with B0 by applying an RF pulse, it
Whereas the spinning top can be pushed from the will begin to realign itself as soon as the RF pulse is
vertical by a tap of the finger, the magnetization M switched off. The nuclear spins do this by giving out
has to be pushed by an oscillating magnetic field the energy they have absorbed from the RF pulse.
applied at right angles to B0. This field has to be Figure 2.3 shows the recovery of the magnetization
applied at precisely the Larmor frequency for there to toward the z-axis following a 90° RF pulse. The z com-
be any effect. The oscillating magnetic field is applied ponent of magnetization Mz recovers exponentially
for only a few milliseconds, so that it is usually with time constant T1, toward its equilibrium value M0,
referred to as an RF magnetic field pulse, as imagers the value it has if left undisturbed by RF pulses. Thus,
use field strengths which give f0 values in the radio- the longer the T1 value, the longer it takes for Mz to
frequency (RF) range. The RF pulse is applied by recover. T1 is called the longitudinal relaxation time
means of a tuned RF coil surrounding the patient’s and sometimes the spin–lattice relaxation time. The
body or head, with power supplied by a radio- magnetization vectors from different groups of spins
frequency power amplifier. An RF pulse that rotates M also fan out into a cone as they precess. This effect will
through 90° from its initial position aligned with z is be discussed later in this section. Mathematically, the
called a 90° pulse. M will then precess around z, as meaning of T1 is that the difference between Mz and M0
shown in Figure 2.2a. If the amplitude of the RF mag- decreases by 63% of its value in each T1 period, pro-
netic field pulse is doubled, or alternatively, if it is left vided that no RF pulses are applied.
on for twice as long, then M is rotated by 180°. In T1 is about 3 s for protons in pure water, or for
this case we have applied a 180° pulse. Thus if M is tissues with a very high water content, such as

z z

B0 B0

M M

90°
180°

y y

x
x
a b
Figure 2.2. (a) A 90° RF pulse rotates the nuclear magnetization vector M from its initial position along the z-axis, into the
(x,y) plane at right-angles, or transverse, to z. (b) A 180° RF pulse is simply a longer or more powerful pulse, which continues
to rotate M until it has been inverted to lie along the negative z-axis, so that it now points in the opposite direction.
 RELAXATION IN NMR 7

z z

M0

90°

x x
a b

z z

M0

x x
c d
Figure 2.3. Following a 90° pulse, magnetization initially along the z-axis precesses in the transverse plane. As time
progresses, the z component becomes progressively larger, and the transverse magnetization dephases, so that the
precessing magnetization fans out into a cone, which is folding towards the z-axis.

cerebrospinal fluid (CSF). Water protons that are Table 2.1 Proton T1 relaxation times for some
bound into soft tissues have a much shorter T1 value. important tissues at 0.5, 1.0 and 1.5 T. T2 is also
Table 2.1 gives typical in vivo T1 values of various given and does not vary greatly with Larmor
tissues at 0.5, 1.0 and 1.5 T, from the data of frequency.
Henriksen et al (1993). The CSF data is from Hopkins
et al (1986). In water and CSF, where the protons Tissue T1 (0.5 T) T1 (1.0 T) T1 (1.5 T) T2
interact with their surroundings only weakly, T1 times ms ms ms ms
are long, as the nuclear spin systems take longer to
Grey matter – 1040 1140 100
give up their excess energy after an RF pulse.
White matter 450 660 720 90
Just as the value of the z-magnetization seeks to
Muscle 560 – 1160 35
recover toward the equilibrium value M0 following
CSF 4000 4000 4000 2000
any RF pulse, so the amount of any magnetization
Liver 360 – 720 60
rotated into the transverse plane (Mxy) declines as the