Leon Axel, PhD, MD #{149}Lawrence Dougherty, BS

, MR Imaging of Motion with SpatialModulation of Magnetization’

841

A novel magnetic resonance imag-ing technique provides direct imag-ing of motion by spatially modulat-ing the degree of magnetization pri-or to imaging. The preimaging pulsesequence consists of a radio-fre-quency (RF) pulse to produce trans-verse magnetization, a magnetic

field gradient to “wrap” the phasealong the direction of the gradient,and a second RF pulse to mix themodulated transverse magnetiza-tion with the longitudinal magneti-zation. The resulting images showperiodic stripes due to the modula-tion. Motion between the time ofstriping and image formation is di-rectly demonstrated as a corre-sponding displacement of thestripes. This technique can be usedto study heart wall motion, to dis-tinguish slowly moving blood fromthrombus, and to study the flow ofblood and cerebrospinal fluid.

Index terms: Blood, flow dynamics #{149}Blood,

MR studies #{149}Cenebnospinal fluid, flow dynam-

ics #{149}Cerebrospinal fluid, MR studies #{149}Heart,

MR studies, 51.1214 #{149}Heart, thrombosis #{149}Mag-

netic resonance (MR), pulse sequences #{149}Mag-

netic resonance (MR), technology

Radiology 1989; 171:841-845

I From the Department of Radiology, Hospi-tal of the University of Pennsylvania. 3400Spruce St. Philadelphia. PA 19104. Received

August 18, 1988; revision requested October 11;revision received January 25, 1989; acceptedFebruary 3. L.A. supported in pant by the

American Heart Association. Address reprintrequests to L.A.

C RSNA, 1989

T HE magnetic resonance (MR) sig-

nab has long been known to besensitive to motion (1,2). One of theprincipal reasons for motion sensitiv-

ity is that when the local magnetiza-tion of a material is altered, the mate-niai maintains the altered magnetiza-tion when it moves (within the limitsof the relaxation times). For example,Morse and Singer (3) proposed mea-

suring blood flow by locally alteringthe magnetization of blood and thendetecting the passage of this “tagged”blood downstream. Analogous tech-niques have been proposed for mea-surement of blood flow with MR im-aging by detecting the passage ofblood with locally saturated or in-verted magnetization through the me-gion being imaged (4,5). A techniquehas been proposed (6) for imagingmyocardial motion within the plane

of the image by using selective exci-tation to produce a pattern of lines ofaltered magnetization, the motion ofwhich can be followed. We describeherein a novel technique for produc-ing a spatial pattern of altered mag-netization within a region to be im-aged, for the purpose of studyingmotion. We have used this techniqueto demonstrate myocardial contrac-tion and to distinguish thrombusfrom slow-moving blood. The tech-nique can also be used to demon-strate the spatial distributions ofmagnetic field inhornogeneity, radio-frequency (RF) inhomogeneity, and

gradient nonlinearity.

MATERIALS AND METHODS

This technique (Appendix) produces aperiodic spatial modulation of magnetiza-

tion (SPAMM) prior to imaging, by using

a sequence of two nonselective RF pulsesseparated by a magnetic-field-gradient

pulse (Fig 1). Starting from a condition ofuniform longitudinal magnetization (Fig2a), the first RF pulse turns some of this

magnetization (or all, in the case of a 90#{176}flip angle) into transverse magnetization.all initially with the same phase (Fig 2b).

RF-TLfL

H

E

Figure 1. Timing diagram of pulse se-

quence for SPAMM. RF radio-frequency

excitation, t = time, C wrap gradient for

production of modulation. Letters A-E mdi-

cate corresponding times in Figure 2. Thetime between A and D is assumed to be short

relative to the relaxation times.

The gradient pulse produces a periodic

spatial modulation of the phase of the

transverse magnetization (“wraps” it)

along the direction of the gradient (Fig2c). The second RF pulse mixes the modu-

lated transverse magnetization with thelongitudinal magnetization. producing

modulated longitudinal magnetization

(Fig 2d). Although the second RF pulseneed not be identical to the first, if it has

the same flip angle, the longitudinalmagnetization will be restored to its mi-tial value at the peaks of the modulation.

The phase of the second RF pulse is un-

important, except to determine the rela-

tive phase of the spatial modulation pat-

tern. An optional second gradient pulsecan be used to “spoil” the remaining

transverse magnetization. The use of gra-

dients for section selection in the subse-quent imaging sequence will also achieve

this. The net result is the production of a

stack of “planes.” or bands, of modulatedmagnetization.

The SPAMM sequence is analogous to

classical two-dimensional MR imaging (7)

with its phases of preparation, evolution,and mixing, with the subsequent imaging

sequence enabling signal detection. Lon-gitudinal relaxation between production

of the bands and imaging will reduce theamplitude of modulation (Fig 2e). The de-pendence of the amplitude of modulation

on the delay between the SPAMM se-

quence and imaging could be used to esti-

mate the local value of the longitudinal

relaxation time, Ti. The initial amplitude

of modulation of the magnetization is de-

Abbreviations: RF radio frequency. SPAMM= spatial modulation of magnetization.

M, M, M5

‘:�‘M0

a. b.

Figure 3. Magnitude of transverse magnetization. � (proportional to image intensity),

along direction of wrap gradient. r, resulting from imaging of modulated longitudinal mag-

netization, M2. (a) Different degrees of modulation of M., ranging from full inversion in

troughs (solid line) to partial saturation (dashed line). (b) Corresponding resulting�M���.

The different initial states could reflect different flip angles on different degrees of relax-ation after an initial inverting modulation.

a. b.

Figure 4. Images of a 28-cm-diameter cylindrical phantom filled with copper sulfate solu-

tion, obtained after SPAMM sequence with 90#{176}RF flip angles, producing inversion introughs of modulation. (a) Image obtained 3 msec after SPAMM sequence. Notice pairwise

convergence of stripes peripherally, due to RF inhomogeneity. (b) Series of images with 45-

msec incremental increases in delay between SPAMM and imaging, from top left (image in

Fig 4a) to top right to bottom left to bottom right. Note initial pairwise merging of stripes,

followed by fading of stripes without further motion.

M2

M� M� M�

842 #{149}Radiology June 1989

a. b. c. d. e.

Figure 2. State of magnetization (M) at different times in the pulse sequence in Figure 1. (a) Magnetization prior to initiation of the modu-

lation sequence (time A in Fig 1). Total distribution of magnetization in rotating frame is initially all polarized with value M0 along the main

magnetic field (in the z direction). (b) Magnetization after first RF pulse (time B in Fig 1). RF pulse has flip angle 0, with phase along the x

axis in rotating frame. (c) Magnetization after wrap (modulating) gradient pulse (time C in Fig 1). (d) Magnetization after second RF pulse

with same values as first (time D in Fig 1). (e) Magnetization after significant relaxation has occurred (time F in Fig 1) and after remnant

transverse magnetization has relaxed or been “spoiled.”

termined by the choice of flip angle (eg, a45#{176}flip angle produces bands of satura-tion at the troughs, while a 90#{176}flip angle

produces bands of inversion). The orien-

tation of the band is determined by the

direction of the wrap gradient. The sepa-ration of the bands is inversely propor-tional to the strength and duration of the

wrap gradient. For example, a rectangulargradient pulse of 0.6-msec duration and0.8-C/cm (0.00008-T/cm) amplitude willproduce a band spacing of 0.5 cm. The

spacing of the bands resulting from a gra-dient pulse of known shape and duration

can be used to calibrate the gradientstrength. Chemical shift differences be-tween two regions will produce a relativedisplacement in the positions of the bandpatterns. A second set of modulation

bands, for example, in a direction orthog-

onal to the first, can be produced by fob-

lowing the second RF pulse with a second

wrap gradient in an appropriate directionand then with a third RF pulse.

In the presence of magnetic field inho-mogeneities (effectively creating local

gradients), the bands of modulated mag-

netization may become nonparallel.

Keeping the time between the RF pulsesshort will reduce the evolution of phasemodulation due to field inhomogeneity

and thus minimize this effect. For studies

of cardiac motion, keeping this time short

also minimizes the delay between R-wave

detection and initiation of imaging.

Nonlinearity of the wrap gradient will

also result in nonparallel bands (or vary-

ing band spacing, if the nonlinearity is

purely one dimensional). However, inthis case, decreasing the time between theRF pulses will not reduce the effect. Thisfeature can be viewed as an advantage.rather than a problem, because it can be

used to directly display the distribution

of gradient nonlinearity. Although most

manufacturers connect the reconstructed

images for distortions due to gradientnonlinearities, the stripe pattern will stillappear distorted in the image, reflectingthe actual distorted pattern of the bandsin space.

The spatial modulation of the longitu-

dinal magnetization is made visible bythe resulting modulation of the trans-

verse magnetization in the subsequent

imaging pulse sequence, which appears

as stripes with sinusoidal variation of in-

tensity in the image. Phase alternation of

the refocusing RF pulses in the imaging

sequence can help prevent artifacts due tostimulated echoes. The stripes correspondto the intersection of the bands of modu-lation and the imaged section.

Most MR imaging systems display themagnitude but not the sign of the magne-

tization. Therefore, if the SPAMM Se-

quence produces inversion of the magne-tization (ie, RF flip angle greaten than

r

45#{176}),intensity minima will be seen in the

image at points where the longitudinal

magnetization crosses through zero im-

mediately prior to imaging (Fig 3). Thus,for modulation with inversion of magne-tization, there will be twice as many

stripes in the resulting image as theme

would be for modulation with only satu-ration. With increasing delay between theSPAMM sequence and imaging, longitu-

dinal relaxation will result in the pair-

a. b.

Volume 171 #{149}Number 3 Radiology . 843

C.

wise merging of the stripes at a timewhen the magnetization in the troughsequals zero. Further delays will result infading of the stripes but no further move-ment (for stationary tissue). The time of

merging of the stripes with initial inver-sion modulation can be used to estimate

the value of the local Ti relaxation time,in a manner analogous to the use of T

null in classic inversion-recovery mea-sumements of Ti (8).

In the case of RF strength (B1) inhomo-

geneity, the degree of inversion will con-

nespondingly vary across the image. This

variation will be reflected in varyingspacing between the pairs of stripes if in-

version has been produced in the modu-

lation, providing a means of demonstnat-ing the RF mnhomogeneity independentof image intensity. If only saturation is

produced in the modulation, the position

Figure 5. Images of a

healthy 30-year-oldwoman, acquired with

a cardiac-gatedSPAMM imaging se-quence in three or-thogonal planes withan echo time of 20

msec. The subject’s

heart rate was 56 beatsper minute. Images aredisplayed with incre-mental 45-msec in-

creases in delay be-tween SPAMM se-

quence and imaging,

as in Figure 4b.(a) Short-axis viewthrough ventricles.(b) Long-axis viewthrough left ventricle.

(c) Four-chamber view

through ventricles.

of the stripes is independent of RF

strength, making this technique insensi-

tive to RF variation when used for study-ing motion.

Due to longitudinal relaxation, thestripes produced by modulation with sat-umation at the troughs will not persist as

long as those produced by inversion.

However, if, for instance, one wishes tostudy the diastolic phase in a subject with

a slow heart rate, a delay could be intro-duced between R-wave detection andthe SPAMM sequence (eg, at the end ofsystole).

In stationary tissue, the stripes will me-

main stationary with different delays be-

tween SPAMM and imaging, except for

the merging of pairs of stripes describedabove for modulation that produces in-version. With increasing delays, thestripes will fade (assuming no inversion)

at a rate determined by the local Ti relax-

ation times (as it is the modulation of the

longitudinal magnetization that produces

the stripes). In moving tissue, the stripeswill move with the tissue. The displace-

ment of the stripes indicates the come-

sponding amount of motion at might an-

gles to the stripes between the time of tis-

sue labeling with SPAMM andsubsequent signal detection with imag-ing. The positions of the stripes in sum-rounding stationary tissues provide a

convenient visual reference for assessing

motion. More precise measurements of

motion can be made by comparing the

image with one made immediately after

labeling. If there is danger of aliasing due

to motion greater than the interstripe dis-tance, either the stripe spacing can be in-

creased by decreasing the wrap gradient

(amplitude on duration) or additional im-ages can be made at intermediate timeswhen less motion has occurred. In the

case of more complex motions, moving

the object through the imaging plane, thedegree of such motion can be assessed by

acquiring an orthogonal set of images

with stripes corresponding to the omienta-

tion of the original image plane. to pen-

mit connection for such “pull-through” ef-fects. Because the stripes are formed by anintersection of the modulated bands withthe section, if the object rotates throughthe imaging plane, the obliqueness of theintersection may decrease the visibility of

the stripes. This effect can be minimizedby minimizing the section thickness.

The SPAMM sequence in Figure 1 wasimplemented on a conventional commer-

cial 1.5-T MR imaging system (Signa; GE

Medical Systems, Milwaukee). In practice.

a separate spoil pulse is unnecessary. be-

cause the imaging gradients will perform

that function. A conventional cardiac-gat-ed imaging sequence has been modified

by adding the SPAMM sequence prior to

imaging. The total duration of the se-quence is less than 3 msec, adding a mini-

a. b.

Figure 6. Cardiac-gated images (echo time of 20 msec) of a 63-year-old woman with mitral

stenosis. The heart rate was approximately 84 beats per minute, with the patient in atnial fi-

bnillation. (a) Representative conventional image at the level of the left atrium obtained 276

msec after the R wave shows relatively high signal intensity in the left atnial cavity (arrow).

(b) Image at the same level and with the same timing as in a but with SPAMM sequence. No-

tice stripes in stationary structures and heart wall, but not within the left atrium.

Figure 7. Cardiac-gated surface-coil sagittal images (repetition time 2,770 msec, echo

time 70 msec) obtained 182 msec after the R wave in a patient with metastasis at T-4 withepidural extension. (a) Conventional image shows relatively increased signal intensity from

metastasis (M) and cerebrospinal fluid (arrow). (b) Image at the same level and timing as a

but with SPAMM sequence (5-mm stripe spacing). Note downward displacement of stripes

above tumor due to motion of cerebrospinal fluid (arrow).

844 #{149}Radiology June 1989

mal delay to the initiation of imaging af-ten R-wave detection. The SPAMM Se-quence only minimally increases the RFdose of the imaging sequence.

RESULTS

Images of a cylindrical phantom,obtained with a 90#{176}RF flip angle in

the SPAMM sequence (producing in-

version), are shown in Figure 4 for a

series of increasing delays between

modulation and imaging. Represen-

tative cardiac-gated images from amubtiplanam, mubtiphasic study of a

healthy volunteer are shown in Fig-

ure 5 (informed consent was ob-tamed).

Images of a patient with mitral ste-

nosis and strong echocardiographic

indications of intraatrial thrombus

are shown in Figure 6. ConventionalMR imaging disclosed high signal in-tensity in the left atrium, suggesting

thrombus. However, no stationary

stripes were seen on the SPAMM im-

ages, indicating that it was all slow-

moving blood and not thrombus. At

surgery for mitral valvubopbasty,

there was no thrombus in the atrium.

Images of blood vessels show dis-

placement of the stripes within the

lumen, corresponding to motion of

the blood between labeling by the

SPAMM sequence and imaging. Withturbulence or rapid flow, shearing of

the stripes within the section beingimaged can cause disappearance ofthe stripes with increasing delays be-tween SPAMM and imaging, even

though the flow may be too slow to

affect the underlying blood signal.

The application of SPAMM to thestudy of the motion of cenebrospinab

fluid is shown in Figure 7. There was

a clear difference in the amount of

motion above and below the level of

a tumor with epidurab extension, con-

responding to tumor block of the

flow of cerebrospinab fluid.

DISCUSSION

The primary function of the heart

is contraction, and it is to be expected

that diseases of the heart, such as

ischemia and infarction, would gen-

erally result in altered contraction

patterns. The direct demonstration of

the contraction of cardiac muscle has

previously been difficult. Most imag-

ing techniques show only the inner

or outer surfaces of the heart, not themotion of the muscle itself. For ex-

ample, simple fluoroscopy or kymog-

raphy shows motion of the outline of

a projected cardiac silhouette. Studiesperformed after intravascular admin-

istration of contrast medium and af-

ter radionuclide-babeled red blood

cell studies show only motion of the

endocardial surface. Conventional

MR imaging and computed tomogra-

phy can show the wall thickness but

not motion within the wall. Invasive

placement of radiopaque markers,

such as beads on screws, or ultra-

sound transducers permits tracking

of actual fixed points on the heart

wall. However, the sampling of these

points is still relatively coarse, and

the distribution of motion between

them (eg, tnansmurally) is still not

well defined.

Volume 171 #{149}Number 3 Radiology #{149}845

In contrast to these olden tech-niques, MR imaging with magneticlabeling of the myocardium permits a

direct demonstration of myocardialmotion across the thickness of thewall and at many effective locations.l3oth absolute and relative motions of

the heart can be measured. The par-ticular technique for myocandiab ba-beling presented here is flexible, fast,and easy to use and allows labelingof large regions. Although we couldalternatively use tailored RF pulses toexcite selectively (for saturation or

inversion) particular “planes”through the region to be imaged, thelabeling of multiple planes requireseither large RF power in one or a fewpulses or a series of pulses, which

may take a relatively long time. Thislimitation has two potentially badconsequences: It increases the delayafter the R wave before data can beobtained, and it may introduce sig-

nificant differences in the times atwhich different planes are labeled,potentially complicating the analysis.One relative advantage of the selec-tive-excitation technique for labelingis that relatively sharply defined

bands can be produced, while theSPAMM technique produces sinusoi-dab profiles of the labeled bands.

One problem that has affected alltomographic studies of heart wall

motion is that the motion of the heartthrough the fixed planes of imagingcan result in apparent motion andthickening of a region simply due tothe geometric effect of tangentiallycutting through the curved surfacesof the heart wall in a more peripherallocation as the heart is pulledthrough the imaging plane. Thus,

study of myocardial motion must in-

volve three-dimensional analysis tocorrect for such pull-through effects.Suitable orthogonal sets of stripedimages can provide the data neededfor such an analysis. Also, althoughpull-through effects may change the

apparent thickness of the heart wall,they will not change the spacing of

the stripes, permitting pull-througheffects to be distinguished from truecontraction even on a single set ofimages. Although it is straightfor-ward to produce a two-dimensionalarray of stripes with SPAMM, theirsinusoidal profiles result in an over-

all decrease in the signal-to-noise ra-tio of the image and make it moredifficult to appreciate the underlyinganatomy.

The other principal motion effectin MR imaging is the production of

phase shifts in excited spins movingalong magnetic-field gradients. Thus,

images that display the phase of the

signal have been used to demonstrate

effects from cardiac motion, as well

as blood flow (9). Although the phaseimages may look superficially similar

to SPAMM images, particularlywhen a strong phase shift is inducedacross the image by shifting the cen-

ten of the echo relative to the data ac-

quisition window (iO), the physics

are rather different. One potentialproblem in analysis of such images is

in calculating displacement from the

phase, because the phase shift will

generally depend not only on veboci-

ty but also on acceleration and other

higher-order variables. Other poten-

tial sources of phase shift must also

be corrected for in calculating dis-

placement.In summary, SPAMM provides a

simple and effective way to demon-

strate cardiac motion directly. It also

is useful in studying the flow of

blood or cerebrospinal fluid and indistinguishing slow-flowing blood

from thrombus. Adaptation of the

technique will permit a wide range

of other applications, including dem-onstmation of the distribution of mag-

netic field and RF field inhornogen-

eities and gradient nonbineanities,

measurement of Ti, calibration of

gradients, and demonstration of

chemical shift differences. U

Acknowledgments: We acknowledge themany helpful discussions with our colleagues,including Nathaniel Reichek, MD, Eric Hoff-man, PhD, and John Listerud, MD, PhD.

APPENDIX

The fundamental equation is the Lam-mom relationship between the resonancefrequency w and the magnetic field B:0) ‘yB, where y, the proportionality con-

stant, is the gyromagnetic ratio. The mag-

netic field experienced by a nucleus at aposition r is given by the sum of the main

magnetic field Bo(r) and any applied mag-netic-field gradients. In the case of linear

gradient fields and a homogeneous main

field, we can write B(r) = B0 + Gr, whereG is the component of the gradient along

the direction of r.

Chemical shift effects can produce a

further change in effective magnetic field

Beit for example, between fat and water,in accordance with the equation Beff

B(i - ci), where the difference in the

chemical shift parameter � is on the order

of 3 ppm for fat and water.The MR signal is detected relative to a

reference frequency, typically set equal to

that of water in the average main field.

The phase � of the transverse magnetiza-tion will evolve in time at a rate depen-dent on the difference between the localresonance frequency and the reference

frequency. In the absence of chemical

shift effects, for a uniform main field

with the reference tuned to the resonancefrequency and linear gradients, the gradi-ents will cause the phase to evolve as fol-

lows: #{231}c(r)= ‘yfG(t)rdt, where f time.This corresponds to a sinusoidal modula-

tion of the x and y components of the

transverse magnetization (with a 90#{176}

phase shift between them) along the di-

mection of the applied gradient, with a

spatial wavelength R of 2ir/’yfG(t)dt.

Thus, the spacing of the final stripes will

depend inversely on the integral of thegradient pulse. If theme are nonlinearities

of the gradients, as may be found toward

the ends of the magnet, the spacing of the

stripes will change correspondingly, withthe stripes flaring out as the gradients be-come weaken.

If two regions have chemical shift van-

ables differing by �r, the stripes will

have the same spacing in each region, butthe patterns will be offset from each otherby a distance d given by the equation

d = �yBoi�ti�n, where i�t is the time be-

tween the two RF pulses. Similarly. in thepresence of magnetic field mnhomogenei-

ty �B(r), arising either from impenfec-

tions in the magnet or from the object be-

ing imaged (eg, due to regional suscepti-bility variations), there will be a

corresponding local phase offset at the

time of the second RF pulse of �#{231}�’(r)

�y�B(r)�t. This will cause the stripes to de-

viate from parallel. Both of these effects

can be minimized by keeping �t short.

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