Download Nuclear Magnetic Resonance Imaging

123
Clinical Science (1984) 66,123-127
EDITORIAL REVIEW
Nuclear magnetic resonance imaging
R . E. STEINER A N D G . M . BYDDER
Department of Diagnostic Radiology, Royal Postgraduate Medical School, Hammersmith Hospital, London
Introduction
Nuclear magnetic resonance is the latest addition
to medical imaging technology. Clinical experience
so far has been very limited, with a total of little
more than 2000 patient studies worldwide. Most
of these patients have been examined with research
prototype imaging machines and the examinations
have generally been slow with clinical evaluation
running in parallel with machine development. In
spite of these difficulties it now appears likely that
n.m.r. may play a significant role in neurological
diagnosis in the future, and possibly in other areas
of medicine as well.
Historical development
The phenomenon of nuclear magnetic resonance
(nm.r.), whereby nuclei respond to the application of particular magnetic fields by absorbing or
emitting electromagnetic waves, was first demonstrated independently by Blochetul. [ 11 and hrcell
et ul. [2] in 1946. N.m.r. spectra representing
absorption and emission at different frequencies
have been used extensively as a basic technique in
analytical chemistry since this time, but the
medical application of nm.r. began in the 1950s.
In an extensive body of work Erik Odeblad, a
Swedish obstetrician and gynaecologist, used
n.m.r. spectroscopy to study the properties of
human erythrocytes, cervical mucus, myometrium,
human milk, saliva, gingival tissue and fluids of the
eye as well as ovulation [3-51. Later work in vitro
with spectroscopy by Damadian in 1971 [5] and
Weisman et ul. [6] in 1972 demonstrated an
increase in the relaxation time of tumours in
animals and this finding was also demonstrated in
human tumours by Parrish el ul. in 1974 [7].
The production of images with n.m.r. required
the application of graduated magnetic fields to the
area of interest, a technique which was proposed
by Damadian [a], Mansfield [9] and Lauterbur
[ 101. The first published image was produced by
Lauterbur in 1973. Human images in vivo were
produced in 1977 [Il-131 and the first images in
vivo demonstrating pathology were published by
Hawkes et ul. in 1980 [ 141. There are now about a
dozen groups involved in the evaluation of n m r .
imaging systems and most regions of the body are
now being studied.
Instrumentation
All n.m.r. machines are constructed around a large
magnet which provides a uniform static magnetic
field. In the presence of this field protons behave
like tiny bar magnets. Their magnetization is
aligned with the static magnetic field producing a
net proton magnetization in the long axis of the
patient. Additional perpendicular magnetic pulses
are applied by means of a coil surrounding the
patient. These pulses are used to rotate the nuclear
magnetization into the transverse plane, after
which it recovers or relaxes back to its original
magnitude and direction in the longitudinal axis
of the patient. During the recovery or relaxation
period the component of the magnetization in the
long axis of the patient recovers to its original
magnitude in an exponential way. This recovery is
called longitudinal or spin-lattice relaxation and is
characterized by the time constant Tl. Relaxation
of the magnetization in the transverse direction
back to its original value of zero is termed transverse
relaxation or spin-spin relaxation and is characterized by the time constant T2.As the magnetization
recovers it induces an electrical signal in a receiver
coil which surrounds the patient. The electrical
signal detected by this coil after such a 90" pulse is
known as the free induction decay (FID) and it is
this signal which is used to reconstruct the image.
Longitudinal relaxation ( T I ) depends on the
interaction of protons with surrounding nuclei and
molecules (the 'lattice') and transverse relaxation
depends on the interaction of protons with each
other. Both T1and T1 are sensitive indices of the
124
R. E. Steiner and G.M.Bydder
local nuclear and molecular environment. By using
a variety of pulse sequences it is possible to produce
images with varying dependence on proton density
(p), Tl and T2.More detailed description of n.m.r.
imaging systems are available elsewhere [ 15, 161.
Image interpretation
Image interpretation has largely proceeded on an
empirical basis. Increases in Tl and Tz are seen in a
variety of pathological processes in which the water
content of the lesion is increased, e.g. inflammation, oedema and many tumours, whereas a relative
decrease in Tl is seen in such conditions as acute
haemorrhage, fatty lesions, fibrosis and pleural
thickening. The change in Tl or T2 may be 200300% but is relatively non-specific. Specificity is
usually derived from localization and the clinical
context.
Empirical rules have evolved for optimizing
contrast and avoiding difficulties in image interpretation due to the n.m.r. properties of cerebrospinal
fluid and intra-abdominal fat, although much more
work will be required in this area.
FIG. 1. Multiple sclerosis: 2'2 dependent scan. The
lesions have a long T2 and appear light (arrows).
Vascular disease of the brain
Cerebral infarction produces an increase in Tl and
T2 and a loss of grey-white matter contrast with
Tl dependent scans [17, 181. There may also be a
small associated mass effect with large areas of infarction. N.m.r. is of most value in showing brainstem and cerebellar infarction, where abnormalities
on CT scans are frequently obscured by the
presence of artifact from bone. Acute intracerebral
haemorrhage displays a short Tl and a long T2. In
addition central areas of liquefaction or clot
dissolution are seen. Haemorrhages evolve and may
eventually leave residual cysts. During these
changes TI and T2 increase. Both the medial and
lateral margins of subdural haemorrhages are seen
unobscured b y bone. In addition, displacement of
intracranial structures is well seen because of the
series of grey-white matter interfaces present on
the Tl dependent scans, which define gross
anatomical boundaries within the brain.
White matter disease of the brain
The lesions of multiple sclerosis are well demonstrated with n.m.r. [19]. They are characteristically
periventricular and have an increased Tl and T2
(Fig. 1).
Small lesions and lesions in the posterior fossa
are frequently shown with n.m.r. when they are
not evident on CT scans.
In leucodystrophy the normal white matter is
highlighted on the n.m.r. scans because of the
increased relaxation time. The characteristic
distribution of lesions has been seen in adrenoleucodystrophy, together with loss of grey-white
matter contrast in the adjacent occipital lobes.
Cerebral tumours
Most tumours have an increase in Tl and T2but
lipid-containing tumours and recent haemorrhage
may display a short Tl (Fig. 2).
Oedema displays an increase in TI and T2 and
in a proportion of cases there is difficulty in
defining the margin between tumour and oedema.
In these instances contrast-enhanced CT is often
superior to n.m.r. The development of n.m.r.
contrast agents, which will mark blood-brain
barrier breakdown, is now in progress and may be
very important in resolving this problem.
Mass effects are well demonstrated with TI dependent scans, particularly with sagittal and
coronal imaging planes.
Paediatric neurological disease
The high level of grey-white matter contrast
available with Tl dependent sequences provides a
Nuclear magnetic resonance imaging
125
demonstrating obstruction or occlusion of vessels
and in allowing the demonstration of atheromatous
plaque in major vessels. As with cardiac imaging
the clinical usefulness of this remains to be determined.
The development of Echoplanar imaging by
Mansfield and others offers the potential of real
time imaging of the heart. Data acquisition only
requires milliseconds and the process can be
repeated rapidly [21]. Initial results have been
obtained in animals and the spatial resolution has
been limited, but the technique is improving.
Abdomen
FIG. 2. Intrinsic tumour of the brainstem: sagittal
Tl dependent scan. The tumour (arrow) has a long
Tl and appears dark.
basis for the demonstration of the normal process
of myelination in infants in vivo [20]. There is a
rapid phase of myelination in the first 2 years of
life followed by a slower phase extending into the
second decade of life.
Delays in this development are seen after intraventricular haemorrhage and a variety of other
conditions. Cerebral tumours, hydrocephalus infarction and infective changes have been seen with
n.m.r.
In spite of respiratory movement during the 24 min scan time causing blurring, the high level of
soft tissue contrast on inversion-recovery images
enables the liver to be seen with considerable
clarity. Intrahepatic blood vessels and bile ducts
appear dark against the grey of normal liver
parenchyma.
In a study of 30 patients Smith et al. 1221
compared n.m.r. favourably with isotope scanning
and ultrasonography and first drew attention to
the value of Tiin the diagnosis of liver disease.
Metastases are well seen with both CT and
n.m.r. (Fig. 3) and studies by Moss et al. on metastases have shown a sensitivity similar to that of
CT [23].
In diffuse disease the pattern is more varied. In
steatosis CT is usually diagnostic although Tl
dependent scans show no change. This may be of
value in distinguishing focal fatty infdtration from
Heart
Saturation-recovery images (which largely reflect
proton density) show little contrast between blood
and myocardium but these structures are clearly
distinguished by using Tl weighted sequences.
Experimental infarction produced by occlusion
of the left anterior descending artery can be
demonstrated. In patients abnormal ventricular
contours have been seen in ventricular hypertrophy
and hypertrophic obstructive cardiomyopathy, but
the clinical role of this technique remains uncertain.
Gating of the n.m.r. image can be performed
either by using the peripheral pulse with a pressure
transducer or the ECG. The sensitivity of the
nm.r. images to changes in flow is of value both in
FIG. 3. Metastasis in the liver: Tl dependent scan.
The tumour is dark and the liver vessels are also
seen.
126
R. E. Steiner and G. M. Bydder
tumour, which can be a problem with CT. In other
conditions information of varying specificity is
contributed by both CT and n.m.r.
Retropentoneum and pelvis
The pancreas has a Tl value similar to that of liver
and disease processes such as tumour and pancreatitis have the effect of lengthening this. As a result,
these conditions may be difficult to visualize
because the pancreatic relaxation time becomes
similar to that of adjacent fluid-filled loops of
bowel.
The most striking feature about the kidney
images is the differentiation of cortex and medulla
seen with TI dependent sequences. Perirenal fat is
clearly seen around the kidney.
Focal changes in tumours and cysts have been
observed with n.m.r. [24,25] but these conditions
are well seen with other techniques. If n.m.r. is t o
have a specific role in renal disease it appears likely
to be in diffuse parenchymal disease rather than
focal diseases, which are already well demonstrated
with existing techniques.
Future developments
There is little doubt that improvements in n.m.r.
image quality will continue in the next few years,
although probably at a slower rate than over the
last 2 years. In particular increased spatial resolution in the body may result in a significant role for
n.m.r.
Other nuclei besides protons are also of interest
and S . K. Hilal et al. (unpublished work) have
successfully imaged 23 Na in rats after experimental
cerebral infarction. Although the natural abundance
of 23 Na in the body is much less than protons, the
relative changes in concentration in diseases such
as infarction are much greater so that this technique
may have clinical applications. 31 P is another
nucleus of interest in this context although it has
not yet been successfully imaged. "F images of
gaseous fluorocarbons in the lung have been
demonstrated and "F may prove useful in the
form of contrast agents.
Another field of interest has been the possibility
of obtaining clinically useful images and 31 P
spectra on the same machine. This requires the use
of high magnetic fields (e.g. 15 kilogauss). At these
fields it is expected that absorption of electromagnetic radiation may become a problem with
larger objects and more complex pulse sequences.
The high field also restricts the magnet choice t o
cryogenic systems and increases the expense.
Although the clinical advantages of such a system
are uncertain, research in this direction is being
actively pursued at several centres.
Acknowledgments
We are very grateful to Dr Ian Young and his team
from Picker International and the General Electric
Company, who designed and built the n.m.r.
machine from which the above images were
obtained.
References
1. Block, F., Hansen, W.W. & Packard, M.E. (1946)
Nuclear induction. Physics Review, 63, 127.
2.Purcell, E.M., Torrey, H.C. & Pound, R.V. (1946)
Resonance absorption by nuclear magnetic movements
in a solid. Physics Review, 69, 37.
3. Odeblad, E. & Lindstrom, G. (1955) Some preliminary
observations on the proton magnetic resonance in
biologic samples.Acta Radiologica, 43,469-475.
4.Odeblad, E. (1966) Micro-NMR in high permanent
magnetic fields. Acta Obstetrica et Gynaecologica
Scandinavica, 45 (Suppl. 2), 1-88.
5.Damadian, R. (1971) Tumor detection by nuclear
magnetic resonance. Science, 171, 1151-1153.
6. Weisman, I.D., Bennett, L.H.,Maxwell, L.R., Woods,
M.W. & Burk, D. (1972) Recognition of cancer in
vivo by nuclear magnetic resonance. Science, 179,
1288-1290.
7. Parrish, R.G., Kurrland, R. J., Janese, W.W. & Bakey, L.
(1974) Proton relaxation rates of water in brain and
brain tumours. Science, 183,438-439.
8.Damadian, R. (1972) Apparatus and method for
detecting cancer in tissue. US. Patent no.3789832.
U.S. Patents Office.
9. Mansfield, P. &Grannell,P.K. (1973) NMR 'diffraction'
in solids. Journal of Physics C Solid State Physics, 6,
L422.
10. Lauterbur, P.C. (1973) Image formation by induced
local interactions: examples employing NMR. Nature
(London), 242,190-191.
11. Mansfield, P. & Maudsley, A.A. (1977) Medical
imaging by NMR. British Journal of Radiology, 60,
188-194.
12. Damadian, R., Goldsmith, M. & Minkoff, L. (1977)
NMR in cancer: XVI. Fonar image of the live human
body. Physiological Chemistry and Physics, 9, 97-100.
13.Hinshaw, W.S., Bottomley, P.A. & Holland, G.N.
(1977) Radiographic thin section image of the human
wrist by nuclear magnetic resonance. Nature (London),
270, 722-723.
14. Hawkes, R.C., Holland, G.N., Moore, W.S.&Worthington, B.S. (1980) NMR tomography of the brain: a
preliminary clinical assessment with demonstration of
pathology. Journal of Computer Assisted Tomography,
4, 577-586.
15. Pykett, I.L., Newhouse, J.H., Buonanno, F.S., Brady,
T.J., Goldman, M.R., Kistler, J.P. & Pohost, G.M.
(1982) Principles of nuclear magnetic resonance
imaging.Radiology, 143, 157-168.
16. Bradley, W.G. & Tostetan, H. (1982) Basic physics of
NMR. In: Nuclear Magnetic Resonance Imaging in
Medicine, pp. 11-29. Ed. Kaufman, L., Crooks, L.E.
& Margulis, A.R. Igaku-Sloin Ltd, Tokyo.
17. Bailes, D.R., Young, I.R., Thomas, D.J., Straughan,
K., Bydder, G.M. & Steiner, R.E. (1982)NMRimaging
of the brain using spin-echo sequences. Clinical
Radiology, 33, 395-414.
18. Bydder, G.M., Steiner, R.E., Young, I.R., Hall,A.S.,
Thomas, D.J., Marshall, J., Pallis, C.A. & Legg, N. J.
Nuclear magnetic resonance imaging
(1982) Clinical NMR imaging of the brain: 140 cases.
American Journal of Roentgenology, 139,215-236.
19.Young, I.R., Hall, A.S., Pallis, C.A., L e g , N.J.,
Bydder, G.M. & Steiner, R.E. (1981) Nuclear magnetic
resonance imaging of the brain in multiple sclerosis.
Lancet, ii, 1063-1066.
20. Levene, M.I., Whitelaw, A., Dubowitz, V., Bydder,
G.M., Steiner, R.E., Randell, C.P. & Young, I.R.
(1982) Nuclear magnetic (NMR) imaging of the brain
in children. British Medical Journal, 285,114-116.
21. Ordidge, R.J., Mansfield, P., Doyle, M. & Coupland,
RE. (1982) Real time movie images by NMR. British
Journal of Radiology, 55,129-133.
22. Smith, F.W., Mallard, J.R., Reid, A. & Hutchinson,
J.M.S. (1981) Nuclear magnetic resonance tomographic
127
imaging in liver diwase. Lancet, i, 963-966.
23. Moss, A.A., Davis, P.L., Goldberg, H.I.,Margulis, A.R.,
Stark, D. & Kaufman, L. (1983) NMR scanning of
hepatic tumors. Evaluation of various imaging techniques. Journal of Magnetic Resonance in Medicine,
Suppl. 1 (In press).
24. Smith, F.W., Hutchinson, J.M.S., Mallard, J.R., Reid,
A., Johnson, G., Redpath, T.W. & Selbie, R.D. (1981)
Renal cyst or tumour-differentiation by whole-body
nuclear magnetic resonance imaging. Diagnostic
Imaging, 50,61-65.
25.Hricak, H., Kaufman, L., Crooks, L., Davis, P. &
Sheldon, P. (1983) NMR imaging of the kidney.
Journal of Magnetic Resonance in Medicine, Suppl. 1
(In press).