Simultaneous spin-echo refocusing

Simultaneous Spin-Echo Refocusing

Matthias Gunther* and David A. Feinberg

A new approach to spin-echo imaging is presented in which the180° RF pulse refocuses two or more spin-echoes at differentpositions in the readout period. When simultaneous echo refo-cusing (SER) is implemented using multiple 180° pulses, anundesirable mixing of stimulated echoes and primary echoesfrom different slices can occur. A novel periodic gradientspoiler scheme eliminates this potential source of artifactswithout spoiling the correctly timed stimulated echoes, which,similar to RARE (TSE) sequences, add coherently to the primaryechoes. Comparisons show equivalent artifact elimination us-ing phase cycling, periodic spoiling, and a previously developedspoiling scheme for non-Carr–Purcell–Meiboom–Gill se-quences. A comparison of head images at 1.5 T acquired withSER-TSE and conventional TSE T1-weighted sequences showno degradation in image quality nor SNR. T2-weighted imagingis not achievable with the current implementation, but possiblesolutions are proposed. The proposed technique might proveespecially beneficial at higher field strengths, where the re-duced number of refocusing pulses for multislice SER-TSE de-creases RF power deposition. SER spin-echo imaging offers anapproach that is very different from low flip angle imagingto mitigate RF heating limitations in high-field clinicalimaging. Magn Reson Med 54:513–523, 2005. © 2005 Wiley-Liss, Inc.

Key words: high-field MRI; spin-echo; non-CPMG; gradientspoiling; SAR

Spin-echo-based MR imaging sequences play a key role inclinical diagnostic imaging. Their ability to produce high-resolution data and their insensitivity to inhomogeneitiesof the local magnetic field are decisive factors. Currently,both T1- and T2-weighted hybrid RARE (1) sequences, alsoknown as turbo-spin-echo (TSE) or fast-spin-echo se-quences (2), are commonly used for medical diagnosis. Forthis technique, a train of multiple radiofrequency (RF)refocusing pulses is applied after a single excitation toreuse the magnetization in order to shorten the measure-ment time compared to a conventional spin-echo (SE) (3)experiment. Since the refocusing pulses in the echo trainemploy flip angles close to 180° to collect as much mag-netization as possible, the RF energy, which is depositedin the subject’s body and generates heat, frequentlyreaches the specific absorption rate (SAR) limit set by theIEC (4).

During the past few years interest in magnetic fieldstrengths beyond the routinely used 1.5 T has grown con-tinously. MR scanners with field strengths of 3 T are nowcommercially available for clinical imaging. At these fieldstrengths the RF penetration of the human body is mark-edly reduced. To compensate for this the power of the RFpulses must be raised, which in turn leads to an increasedheating of the subject. In particular, rapid SE sequencessuch as TSE that use a large number of closely spaced highflip angle RF pulses must be slowed down considerably toprevent harming the patient.

For many implementations of TSE the SAR limitation isa significant problem, even at 1.5 T. Several approaches,including reduced flip angle refocusing pulses or timedelays between sequence iterations, have been developedto overcome this problem. Recently, a method has beenproposed, which reduces the flip angle of all refocusing RFpulses to bring down the SAR value (5) and uses noncon-stant flip angles for the first few RF pulses to approach thesteady state more smoothly (6–8). However, due to thecomplexity of the coherence pathways that are createdeven by a small number of low flip angle refocusing pulses,signal loss might occur by means of destructive interfer-ence between pathways.

More recently, Hennig and Scheffler introduced a veryinteresting and efficient technique, called hyperechoes (9).Here, RF pulse trains with an arbitrary flip angle distribu-tion are refocused by a single 180° RF pulse. All subse-quent pulses are a mirror image of the preceding RF pulsetrain. The authors show that all echo pathways will berefocused at the end of this echo train without losing anysignal (neglecting relaxation effects) to form a hyperecho.The method can be used in TSE sequences with a largenumber of refocusing pulses to reduce the flip angles formost of the refocusing pulses and, therefore, to greatlyreduce the SAR of the complete RF pulse train. Properselection of the parameters yields almost the same contrastbehavior as a standard TSE sequence. Since the echo time(TE) is chosen to be the position of the hyperecho, i.e., atthe center of the echo train, this type of modification isonly appropriate for T2-weighted imaging. In T1-weightedimaging where the TE is desired to be as short as possible,hyperechoes are not applicable.

In the following work, we present a different approachto spin-echo imaging, which provides a new solution tothe SAR limitation problem in biologic and clinical imag-ing. The novel spin-echo train sequence generates multi-ple spin-echoes instead of a single spin-echo with eachrefocusing pulse. Thus, the SAR is reduced by using fewerRF pulses rather than lower flip angles. This paper de-scribes the first experiments with simultaneous spin-echorefocusing (SER). The SER technique, formerly introduced

Advanced MRI Technologies, Sebastopol, California, USAGrant sponsor: National Center for Research Resources; Grant number: NIHR01RR13618–01A1.*Correspondence to: Matthias Gunther, Advanced MRI Technologies (AM-RIT), 652 Petaluma Avenue, Suite J, Sebastopol, CA 95472, USA. E-mail:[email protected] 5 July 2004; revised 25 March 2005; accepted 27 March 2005.DOI 10.1002/mrm.20587Published online 5 August 2005 in Wiley InterScience (www.interscience.wiley.com).

513© 2005 Wiley-Liss, Inc.

Magnetic Resonance in Medicine 54:513–523 (2005)FULL PAPERS

as simultaneous image refocusing, has proven to be usefulfor gradient-echo-based echo-planar imaging sequences(10,11). The principle of SER is to excite multiple slicesand to refocus their magnetization pathways within thesame echo train. It is shown below that the sequencetiming allows for multiple spin-echoes within each inter-val between refocusing pulses. However, the Carr–Pur-cell–Meiboom–Gill (CPMG) condition (12) is not fulfilledand, therefore, concerns might be raised regarding an arti-fact-free realization of this imaging sequence. We willshow that with the addition of a unique spoiler scheme,artifact-free SER-TSE images are generated. The SER spin-echo train sequence acquires more slices per unit timethan TSE sequences and can be used to reduce the SARdramatically.

THEORY

Standard SE sequences acquire signal from a single exci-tation by de- and rephasing the magnetization with gradi-ent pulses combined with a refocusing RF pulse. An indi-vidual acquisition of slices or volumes is mandatory sinceotherwise multiple signals originating from different sliceswould be superimposed, resulting in severe image arti-facts. In the SER method multiple slices are excited, wherethe number of slices will be denoted by the SER-factor(SERF). In the following the SERF will be included in thesequence name by naming a SER-TSE with SERF � 2 asSER2-TSE. The echo train length of the turbo spin-echosequence, i.e., the number of refocusing pulses, called theturbo factor (TF), is incorporated in the sequence name byappending the number, e.g., TSE5 for turbo factor 5.

The signals from all excited slices are separated by in-serting dephasing gradient pulses between the excitationpulses, shifting the signal of different slices to differentpositions in k-space. It has been shown for the gradientecho SER-EPI sequences that a signal will only form if allgradient moments, which were applied after excitation,are refocused. Since gradient pulses applied before anygiven excitation cannot impact an unexcited slice while allgradient pulses applied after an excitation affect all previ-ously excited slices, spin-echoes from different slices cancoexist and be refocused by a proper gradient and RF pulsearrangement in the echo train (see Fig. 1). Although thehigh-frequency regions of the slices overlap, it will be

shown below that in high-resolution imaging where thesignal energy in the outer regions of k-space is relativelysmall, the level of image artifacts is too low to be identifiedin the image. The properties of SER-GRE sequences holdtrue for SE sequences but in addition the spin-echo timingcondition must be fulfilled, i.e., the position of the refo-cusing pulse must be halfway between the excitation andthe spin-echo.

An RF refocusing pulse can be experienced simulta-neously in two or more image planes if its bandwidth issufficiently broader than the frequency separation of allexcited image planes. Under such a condition, a single,broad refocusing pulse is sufficient to create a spin-echo intwo or more (adjacent) slices. This reduces the number ofrequired refocusing pulses, which deposit RF energy andresult in heating of the subject. To meet the spin-echocondition for each slice the readout period must be at leastas long as the spacing between the excitation pulses. Infact, we will demonstrate that it should be at least twice aslong to avoid image artifacts. Figure 1 shows the SERprinciple for a simple TSE sequence with turbo-factor 4and SER-factor 2. It is obvious that problems will arise fora TSE sequence, since the CPMG condition is not fulfilled.As a consequence, many stimulated echoes resulting fromimperfect RF pulses will not fall on top of their primaryspin-echo but instead fall onto the primary echo of a dif-ferent slice. This can be seen in Fig. 2, where circles markcorrectly timed echoes, while squares mark incorrectlytimed echoes. Primary echo denotes the echo pathway,which experiences the rephasing effect of each refocusingpulse.

Periodic Spoiler Pulses

It is well known that in TSE sequences the stimulatedechoes contribute to the usable signal in addition to thespin-echoes. For the SER-TSE sequence, an optimal spoil-ing scheme should spoil only the incorrectly positionedstimulated echoes but leave the primary echoes and cor-rectly timed stimulated echoes untouched for maximumpossible image signal-to-noise ratio (SNR) and resolution.Such a spoiling scheme is optimal in terms of efficientsuppression of incorrectly positioned stimulated echoes,i.e., the avoidance of artifacts, but not in terms of utilizingthe entire signal. Previously developed spoiling schemes

FIG. 1. Sequence scheme for the simultaneousspin-echo refocusing sequence (SER2-TSE). Here,multiple slices instead of one are excited and readout with a single echo train. The signals from allexcited slices are separated by imposing dephas-ing gradient pulses between the excitation pulses(named RO1), shifting the signal of different slicesto different positions in k-space.

514 Gunther and Feinberg

of monotonically varying gradient amplitudes with chang-ing signs (13,14) eliminate all of the stimulated echoes innon-CPMG sequences. Similarly, phase cycling (15) of theexcitation pulses in SER-TSE sequences will separate thesignals of different slices and, therefore, avoid the inter-ference of incorrectly timed stimulated echoes of one slicewith those from another. However, multiple repetitions (itcan be shown that two acquisition are sufficient for arbi-trary SERF) are needed for proper slice separation.

Misregistered stimulated echoes result from echo path-ways that miss an odd number of refocusing pulses. Sincethe position of the primary echo alternates within thereadout period with every refocusing period, the destruc-tive stimulated echoes fall on top of the primary echo ofthe other slice and cause interference. On the other hand,constructive stimulated echoes miss an even number ofrefocusing pulses and fall on the correct side of the readoutperiod.

As shown in Figs. 1 and 2, the position of the primaryecho of one slice oscillates with a frequency of two refo-cusing periods. A spoiling scheme with the same oscilla-tion frequency (for a periodic spoiling scheme see (16))might preserve the correctly positioned stimulated echoes

to maintain maximum image SNR. In the following de-scription, the moment of the gradient spoilers is given inunit measures, where one unit measure generates a phasedistribution of 2� within an image voxel. Possible spoilerarrangements can be, for instance (1,2,1,2,1,2,1,2,. . . ) or(�1,1,�1,1,�1,1,. . . ), where successive numbers give therelative gradient moment for successive refocusing peri-ods.

The requirements for an optimal spoiling scheme are: (i)periodicity of 2 to coincide with the oscillation frequencyof the primary echoes; (ii) difference between moments ofspoiler pulses between refocusing periods of at least oneunit measure; (iii) complete rephasing of the primary echoduring the readout period,

The diagrams plotted in Fig. 3 show the pathways in thenew periodic spoiling scheme. The magnetization path-way of the incorrectly timed stimulated echoes is selec-tively displaced out of the read period (spoiled) while thecoherently timed stimulated echoes that fall on their re-spective primary echoes are refocused.

Signal-to-Noise Ratio

Since more than one echo is read out between successiverefocusing pulses the bandwidth and thus SNR will bedifferent in SER-TSE than in TSE.

The SNR dependence relevant for a comparison can beexpressed as

SNR � B0 � �NEXBW

, [1]

where B0 is the main magnetic field, NEX is the number ofrepetitions, and BW � 1/Tacq is the bandwidth of thereadout, i.e., the inverse of the readout period Tacq. For aconstant readout bandwidth BWTSE for the TSE sequenceEq. [1] can be written as

SNR � B0 � � NEXSERF � BWTSE

. [2]

Equation [2] illustrates that for a doubling of the band-width twice as many repetitions NEX must be performedto reach the same SNR level. This applies when, e.g., aSER2-TSE sequence is compared with a standard TSEsequence. For the same underlying echo spacing in bothtechniques, the bandwidth per image will be twice as highfor SER2-TSE as for TSE but the number of slices is alsotwice as high. To get the same slice coverage the TSEsequencemust be repeated with two different slice posi-tions, while the SER2-TSE can be repeated twice for thesame slice positions, thereby increasing the NEX by afactor of 2. Thus, the SER-TSE and TSE images wouldyield the same SNR per unit measurement time, except forminor differences in the echo timing.

MATERIALS AND METHODS

A Siemens Sonata 1.5-T scanner (Siemens, Erlangen, Ger-many) with 40 mT/m maximum gradient strength and 200mT/m/ms gradient slew rate was used in the experiments.

FIG. 2. Evolution of pathways for the SER2-TSE sequence. Theamount of dephasing due to static field inhomogeneities versus timein the sequence for both SER slices is shown. Detectable signalsoccur only when the signal pathway crosses the time axis at adephasing value of zero. The circles mark spin-echoes occurring atthe correct readout position and squares mark stimulated echoes atthe incorrect readout position. [Color figure can be viewed in theonline issue, which is available at www.interscience.wiley.com.]

Simultaneous Spin-Echo Refocusing 515

The human studies were performed with healthy volun-teers after they gave informed consent under the IRBguidelines. Phantom studies were conducted with a spher-ical phantom containing water doped with 1.25 NiSO4 �6H2O per 1000 g distilled H2O.

Avoidance of Interference of Correctly and IncorrectlyTimed Echoes

As described above, two groups of echo pathways exist butonly one can be used for image reconstruction while theother group, namely the incorrectly timed, will interferewith the correctly timed echoes of another slice. For arti-fact-free images the incorrectly timed echo signals of oneslice must be separated from the correctly timed echosignals of the other slice or discarded. This can be eitheraccomplished by phase-cycling or by application of anappropriate gradient spoiling scheme.

One way to separate primary echo and stimulatedecho components in the SER-TSE sequence is to usephase cycling (15). Let (�,�) be the phases of two exci-tation pulses whose signals might interfere. Using(0°,0°) in the first repetition and (0°,180°) in the secondallows separation of the signal from each slice by addingor subtracting the measured data, respectively. Pleasenote that only two different cycles are necessary regard-

less of the SER-factor. This is due to the fact that thecorrectly and incorrectly timed echoes will have thesame distance to the center of the refocusing period. Forexample, for a SER5-TSE sequence with excited slices(1,2,3,4,5) the signal of slice 1 interferes with the signalof slice 5 only. The signal of slice 2 interferes with thesignal of slice 4 only and the signal of slice 3 does notinterfere with any other signal since the echo is locatedin the center of each refocusing period. Drawbacks arethat an even number of repetitions is needed, whichtypically increases scan time, and that residual signalfrom the other slice might be present in the separateddata if the signal level of the images of the phase cycle isnot identical. Nevertheless, this phase-cycling tech-nique can be used for separating signals from differentslices to yield artifact-free images.

Another way to avoid interference between signals fromdifferent slices is to spoil all stimulated echo pathways.This can be done by constantly increasing the spoilingpulse amplitude (see Fig. 3). Thereby, all stimulated echopathways are suppressed efficiently but the maximumavailable gradient strength for the given scanner hardwarelimits the effectiveness of the method. Furthermore, allhigher order echo pathways are suppressed, includingthose stimulated echoes that fall on the correct side of the

FIG. 3. Comparison of the effect of different spoiling schemes. A simple sequence scheme using only three refocusing pulses illustratesthe spoiler gradient pulse arrangement along the slice-select axis. Echo pathway diagrams are shown for both slices of a SER2-TSE3sequence. The gradient moment along the slice-select axis is drawn. Circles represent correctly timed echoes and squares representincorrectly timed stimulated echoes. Detectable signals occur only when the signal pathway crosses the time axis at a moment equal tozero. Three different spoiling schemes are presented: standard constant, steadily increasing, and periodic spoiler pulses. It is obvious thatthe standard spoiling does not work, since the incorrectly timed stimulated echoes are not moved away from the centerline and thus stillcause destructive interference. The second spoiling scheme, increasing spoiler gradient pulses, works fine in that regard, but also reducesthe signal as correctly timed stimulated echoes are moved away from the centerline. Only the pure spin-echo pathway (primary echo) isrefocused properly. On the other hand, the periodic spoiling scheme dephases all undesirable stimulated echo pathways but also collectsthe complete signals from the correctly timed stimulated echo pathways. Please note that the pathway diagram of the steadily increasingspoiling scheme is cropped.


readout and would contribute to the signal without inter-ference. For the evaluation of the spoiling efficiency aSER2-TSE9 sequence was implemented using spoiler gra-dient pulses of strength (1,2,3,. . . ,9). Again, successivenumbers give the relative gradient moment for successiverefocusing periods.

All described SER-TSE sequences using the periodicspoiling are realized with the (1,2,1,2,. . . ) scheme as de-scribed above. The corresponding pathway diagram,which shows the accumulated gradient moment, is shownin Fig. 3.

All measurements for the evaluation of the spoilingschemes were performed on the spherical phantom men-tioned above. No phase encoding pulses were applied toobtain the signal evolution for each echo number sepa-rately. To distinguish between signals from different sliceswithout using phase cycling the flip angle of the excitationpulse of either slice 1 or slice 2 was set to 0. This allowedseparation of the two groups of echo pathways of one slice,e.g., slice 1, with the correctly timed signal appearing inthe image of slice 1 and the incorrectly timed in the imageof slice 2.

Slice Profile

The slice profiles of both the TSE and the SER-TSE se-quence were determined theoretically as well as experi-mentally. Optimized RF pulses were used by slightly mod-ifying sinc-shaped RF pulses (17).

The pulse profiles of the 90° and 180° pulses were cal-culated by integrating the Bloch equations. Subsequentpoint-by-point multiplication of the profile of the 90°pulse profile with that of the refocusing pulses yielded thefinal slice profile for each echo number.

The measurement was performed by applying a readgradient along the slice-select direction. For both the the-oretical and the experimental evaluation the slice param-eters were the same. Four identical slice positions werechosen for both sequence types. The slice thickness was5 mm and the spacing between adjacent slices was 2.5 mm(50%). The refocusing pulse profiles were made slightlythicker: 6 and 14 mm in the TSE and in the SER-TSEsequences, respectively.

Various methods exist to avoid interference betweensignals originating from different slices. For each of thethree approaches presented above the signal loss at eachecho number was investigated experimentally.

The amount of spoiled signal was determined by com-parison with a SER-TSE sequence with constant spoilers.The signal behavior of a TSE sequence was simulated byadding up both the correctly timed and the incorrectlytimed echoes. A total of nine RF refocusing pulses in eachecho train was used.

Estimated RF Power Deposition

In the SER-TSE technique one refocusing RF pulse is usedto refocus the magnetization in several slices. Therefore,the RF power, which is deposited in the subject’s body,will be lower than for conventional multislice SE se-quences. A rough estimate of the deposited RF power, inthe following equated with the SAR, can be made by

summing up the RF power of all RF pulses, which areapplied within unit time, i.e., a single TR cycle. This isillustrated in Appendix A in more detail. The SAR reduc-tion compared to the standard TSE sequence was calcu-lated for SER-TSE sequences with SER-factors of 2, 3,and 4.

Imaging

Brain images of three human subjects were acquired withboth TSE and SER-TSE sequences. The slice thickness of5 mm was the same for all measurements.

The standard TSE sequence used half the bandwidth perimage as the SER-TSE, resulting in almost identical timingas the SER-TSE. Parameters were chosen as follows: TR �700 ms, TE � 12 ms, BW � 130 Hz, number of slices perTR cycle � 11 for TF � 3. The TSE sequence was repeatedat different slice positions to yield the same slice coverageas the SER-TSE sequence.

Another measurement was performed with the SER-TSEsequence with periodic spoiling. In this experiment theamplitude of the second excitation pulse was set to 0 tovisualize the high-frequency artifact.

The sequence parameters for the SER2-TSE were TR �700 ms, TE � 14 ms, BW � 260 Hz per image, number ofslices per TR cycle � 22 for TF � 3, two averages. Bothimages with phase cycling (two step) and periodic spoiling(1,2,1) were acquired at the same slice position.

The overall measurement time was the same for allsequences.

SNR Measurements

To estimate SNR of the imaging techniques regions ofinterest (ROI) were drawn in white brain matter, fat, andair. SNR was calculated by dividing the mean value of theROI in tissue by the mean value of the ROI in air.

High Spatial Frequency Overlap

Images with different voxel sizes were acquired using thespherical phantom mentioned above. The second RF exci-tation pulse of a SER2-TSE was set to 0. The amount ofsignal in the high spatial frequencies was obtained bycomparing the signal at the position of slice 1 and slice 2.Since only one slice was excited the signal at the positionof the second slice signal originates from the high spatialfrequency components of the first. A ROI was selectedcontaining the sharpest edges of the phantom along read-out direction (where the highest spatial frequencies occur).The voxel size was varied from 0.5 to 6 mm.

RESULTS

Avoidance of Interference of Correctly and IncorrectlyTimed Echoes

Figure 4 shows the amount of signal lost by incorrectlytimed stimulated echoes. As expected, phase cycling andthe periodic spoiling yield almost identical results, at leastfor lower echo numbers. Here, the signal loss is 0, 2, 5, 10,and 15% for the first five echoes, respectively. At the ninthecho of the SER-TSE sequence only 67 (phase cycling) and


63% (periodic spoiling) of the simulated TSE signal areleft. The increasing spoiling scheme shows lower signal inthe first four echoes but then performs better for higherecho numbers, reaching a plateau at 88% compared toTSE. The amount of signal from incorrectly timed echoesis almost zero (�2%) for the increasing and the periodicspoiling scheme showing the efficiency of suppressinginterslice interference.

Slice Profile

The theoretical and experimental slice profiles for theSER2-TSE and the standard TSE sequence are depicted inFig. 5. While the slice profile of the TSE sequence issymmetric, the slice profile of the SER-TSE is asymmetricdue to the nature of the sequence. The profiles for adjacentslices are mirrored, with sharp edges in between. Themeasured profiles of the two slices are slightly different,since they were acquired at different echo times.

Estimated RF Power Deposition

The graph in Fig. 6 illustrates the amount of RF power,which is deposited in the subject’s body.

The estimated reduction in RF power deposition forSER-TSE sequences with SER-factors of 2, 3, and 4 iscompared to the standard TSE sequence. For typical clin-ical T1-weighted imaging turbo factors of 3 and 5 arecommonly used. With a TF � 3 typical reductions of 48,62, and 69% are achieved for SERF � 2, 3, and 4, respec-tively. For a TF � 5 the reductions are as high as 48, 63,and 71% for SERF � 2, 3, and 4, respectively. Even for aturbo factor of 1, i.e., a SER-SE sequence, a SAR reductionof 40, 53, and 60% for SERF � 2, 3, and 4, respectively, ispossible.

FIG. 4. Signal intensity of correctly timed and incorrectly timedechoes versus echo number for different spoiling schemes: Twocomponents are shown for the SER2-TSE9 sequence, the correctly(filled symbols) and the incorrectly timed (hollow symbols) echoes,for three different spoiling schemes (● standard (1,1,1,. . . ), �increasing (1,2,3, . . . ,9), and f periodic (1,2,1,2,. . . )). The amountof signal, which is lost due to incorrectly timed stimulated echoes, issmall for the first five echoes (�16%) when using the periodicspoiling scheme. The signal loss is small when using the increasingspoiling scheme. For larger turbo factors SER-TSE is getting lessefficient with periodic spoiling. Therefore, T2-weighted SER imagingwithout additional correction techniques (see Discussion) will resultin significant signal loss. All signal intensities shown in this diagramare normalized to the intensities of a standard TSE sequence, whichis calculated by adding the correctly and incorrectly timed echoeswhen using the standard spoiling method.

FIG. 5. Theoretical and experi-mental slice profiles for SER2-TSE compared to standard TSE:The slices in SER-TSE show abetter profile at the inner than atthe outer edge, since the refocus-ing pulse covers both slice posi-tions. Unfortunately, the slice pro-file is different for different slicesin SER-TSE. The same RF pulseparameters were used for SER-TSE and TSE with a slice thick-ness of 5 mm. The distance be-tween the centers of the slices inSER-TSE was 7.5 mm. The widthof the refocusing pulse was 14and 6 mm in SER-TSE and in TSE,respectively. The different ampli-tude results from different echotimes for slices 1 and 2.


Imaging

Figure 7 shows human brain images from four anatomiclocations measured with SER2-TSE3 with phase cycling(left) and the periodic spoiling scheme (middle). The twoupper and the two lower slices were acquired within thesame SER echo train. The right column shows standardTSE3 images for comparison. The SER2-TSE images ex-hibit the same image quality and image contrast as thoseacquired with the standard TSE sequences. No artifacts arevisible in the phase cycled as well as in the periodicallyspoiled SER-TSE version. Minor loss of details might beseen in Fig. 7 for SER2-TSE3 due to signal loss. SNRmeasurements were performed for white matter and fattissue.

SNR Measurements

Table 1 lists the results of the measurements in the sameorder as the images are given in Fig. 7. The SER2-TSEsequences yield almost the same SNR level as the stan-dard TSE-sequence as predicted by Eq. [2]. However,due to the different echo times for slice 1 and 2 the SNRof the SER-TSE technique for slice 1 is lower, while it ishigher in slice 2. This is especially pronounced forcompartments with a relatively short T2 relaxation timelike fat, where the SNR for slice 2 the SER-TSE tech-nique is even higher than for TSE while it is smaller forslice 1.

High Frequency Overlap

Measurements were performed to estimate the artifactload, which might be introduced by the overlap of the highfrequency components. Figure 8 shows one slice of ahealthy brain and the corresponding amount of high spa-tial frequency, which leaks into the other slice. Please notethat the image intensity for the second slice was amplified

by a factor of 5. Figure 9 displays the percentage of highfrequency overlap for different voxel sizes obtained from aphantom measurement. A small amount of less than 2% ispresent for an in-plane resolution below 1 mm.

DISCUSSION

Comparison with Existing Methods

SER-TSE is similar to the POMP method (18) in that mul-tiple slices are excited at (almost) the same time and that asingle refocusing pulse is used to rephase the magnetiza-tion in all slices. However, SER refocuses the spin echoesat distinctly different times during the readout gradient,which permits the acquisition of the entire data set with asingle average. In POMP, on the other hand, spin echoesconsist of superimposed signals that are separated alongthe phase axis of k-space. Thus, POMP needs multiplephase cycle steps to acquire an unambiguous data set.Another difference of SER-TSE compared to POMP is thereduced peak RF power (almost similar to standard TSE),which makes SER-TSE applicable for high-field imaging.

The hyperecho and the SER-TSE technique are some-what complementary for clinical scanning where T1- andT2-weighted images are desired. The optimal applicationfor SER-TSE is currently T1-weighted imaging, since forlonger TE too much signal is lost due to imperfect RF pulseprofiles, whereas hyperecho sequences benefit from alonger TE. The main field of application of hyperechosequences might therefore be T2-weighted imaging. Inprinciple, the SER-TSE technique can also be combinedwith hyperechoes to improve the SNR for T2-weightedSER-TSE imaging.

While the hyperecho sequences use lower flip angles ofthe refocusing pulses to reduce SAR, the SER-TSE tech-nique increases the spacing of those RF pulses. TheGRASE technique (19) similarly increases RF pulse spac-ing by acquiring several gradient echoes between the RFpulses. In GRASE, the CPMG condition is fulfilled at allecho times and all magnetization pathways contribute tothe measurement.

The SPLICE method, presented recently by Schick (20),uses one readout gradient to rephase two signals simulta-neously, just as in SER-TSE sequences. However, the twosignals originate in the same slice and represent the in- andout-of-phase components, which usually occur in diffusion-weighted sequences due to bulk motion during gradient ap-plication. In the SPLICE method the standard spoilingscheme with constant gradient pulses can be used becausethe in- and out-of-phase magnetization is inherently modu-lated by a period of two due to the refocusing pulses.

Some standard TSE sequences use flow compensation inone or more directions. In SER-TSE one faces the samerestriction as for TSE sequences when using flow compen-sation along slice-select and phase-encode gradient axis.However, along the read axis a more complex gradientscheme would be necessary to switch gradients betweenthe readouts of the two slices.

Image Artifacts

As shown in Fig. 4, signal loss due to incorrectly timedechoes is present especially for higher echo numbers,

FIG. 6. SAR reduction of SER-TSE compared to standard TSE. Theratio of the SAR of the SER-TSE and the standard TSE is shown fordifferent SER factors. A great reduction in SAR is present even forsmall turbo factors. SAR values were estimated as indicated in thetext and in Appendix A. The given SAR values are per slice, i.e., witha SER-factor of 2 twice as many slices as with TSE can be acquiredwith the same SAR exposure.


FIG. 7. Comparison between SER2-TSE and TSE. Two pairs of adjacent slices from a 22-slice measurement are presented for SER2-TSE3with periodic spoiling (left), SER2-TSE3 with phase-cycling (middle), and standard TSE3 (right). Measurement time was 2 min each. The twoupper slices and the two lower slices were acquired within the same SER echo train. The SER-TSE images with the periodic spoiling schemehave no visible artifacts from high spatial frequency overlap in k-space or stimulated-echo artifacts due to the novel spoiler scheme,compared to phase-cycled SER-TSE and standard TSE.


since only half of the stimulated echo magnetization canbe used for signal formation. Figure 4 demonstrates thealmost identical handling of correctly timed echoes bystandard (constant) and periodic gradient spoiling. It alsopresents evidence for the efficient suppression of incor-rectly timed echoes, which can be seen by the vanishingsignal intensity of the periodic spoiler scheme in contrastto the increasing signal intensity of the constant scheme.For T1-weighted imaging this signal loss results in a re-duction of resolution. Minor loss of details might be seenin Fig. 7 for a turbo factor of 3. By increasing the turbofactor of a SER-TSE sequence the loss of resolution mightbe significant. For T2-weighted imaging the signal drop offwill lead to decreased SNR, making the current SER-TSEimplementation not applicable. Using phase-cycling al-lows separating the correctly and incorrectly timed echoesand, therefore, enables full recovery of the magnetizationby complex summation of both echo groups. Such anexperiment would yield the same SNR as a standard TSEsequence even for T2-weighted imaging. However, thespeed advantage of the SER technique (requiring only oneacquisition) would be lost.

The novel spoiler technique designed for SER has dis-tinct advantages in SNR over other techniques in that itspoils only some of the echo pathways, while maintainingboth the primary echoes and half of the stimulated echosignals. Spoiler schemes that use gradient pulses withincreasing amplitudes acquire only the primary echo,

while all stimulated echoes are spoiled. The technicalrequirements for the increasing amplitude scheme are alsorather high, which results in a considerably increased echospacing. The signal loss in the first echoes is expected, butthe later evolution is somewhat surprising, yielding highersignal than the SER-TSE for echo numbers higher than 5.This suggests that destructive interference might occur inthe SER-TSE at those echo numbers, perhaps due to diffu-sion effects or other timing issues, which require furtherinvestigation beyond the scope of this initial report.

SER-TSE uses an asymmetric readout, where the spin-echoperiodically occurs at different relative positions within thereadout period. This leads to slightly different echo timescompared to the standard TSE and furthermore to alternatingecho spacings throughout the echo train. The difference be-tween the different echo spacings equals the length of thereadout period, which is immediately apparent. We did notidentify any image degradations or ghost artifacts resultingfrom this variation for typical T2 values. However, for veryshort T2 relaxation times this might be a source of artifacts.Nonetheless, a change in contrast between fat and tissuecould be observed. The data presented in Table 1 suggest thatthe different echo times for each slice account for the ob-served difference in contrast. Since slice 1 is excited first the

FIG. 9. Measurement of the amount of high-frequency artifacts fordifferent voxel sizes: The flip angle of the second excitation pulse wasset to 0. The signal in slice 2 therefore only consists of the high-frequency overlap of slice 1. Shown is the ratio between mean value ofartifact signal within a selected ROI and the mean value of object signalwithin the same ROI. The ROI was chosen to contain the sharpestedges of the phantom along readout direction. As expected, a smallervoxel size yields smaller high-frequency artifacts.

Table 1SNR for Images Shown in Fig. 7 for Selected ROI

SER2–TSE3 periodic SER2–TSE3 phase cycle TSE3

White matter, slice 1 36.28 1.35 36.61 1.22 42.82 1.78White matter, slice 2 40.10 1.90 37.67 1.35 47.23 2.48Fat, slice 1 77.35 2.66 77.85 2.53 84.49 4.51Fat, slice 2 106.78 4.08 102.10 4.75 97.99 3.21Fat/WM, slice 1 2.13 0.11 2.13 0.10 1.97 0.13Fat/WM, slice 2 2.66 0.16 2.71 0.16 2.07 0.13

FIG. 8. High-frequency artifact for one slice measured with SER2-TSE3 with periodic spoiling where the flip angle of the secondexcitation pulse was set to 0. Only signal arising from high-fre-quency components of the k-space of slice 1 (left) can be seen inslice 2 (right). The signal of slice 2 was amplified by a factor of 5 toshow the artifact.


signal of this slice is read out last in the first segment (i.e.,where the center of k-space is acquired), thus yielding alower SNR compared to the standard TSE sequence, espe-cially for fat, which has a shorter T2-relaxation time thanwhite matter tissue. In slice 2, which has the shorter echotime, the SNR is higher than for TSE. This effect can also beseen in the different signal amplitudes in the slice profilemeasurements (see Fig. 5).

As shown under Materials and Methods, parts of thehigh-frequency information from different slices will over-lap in SER-TSE. The higher the resolution the lower theenergy in the overlapping k-space region and the image“ghost.” Measurements show (see Fig. 8) that this energy isless than 2% for these initial clinical images. The exactdegree of high-frequency overlap depends on the actualform and structure of the imaged object. In the head im-ages, the high-frequency signal artifact was only presentfor the lipid signal of the scalp adjacent to the air interface.No other structured noise attributable to this artifact wasidentified in the brain or elsewhere in the intracranialcavity. Due to the lower resolution, the high spatial fre-quency artifact level of a recently published application ofthe SER principle using gradient echo EPI (10) is inher-ently larger.

For larger turbo-factors the amount of signal, which isspoiled by the periodic spoiling scheme, is increased con-siderably, thus producing faster signal drop off in highersegments and more pronounced edges in k-space. Thisleads to increased artifacts with a period equal to the turbofactor, referred to as a segmentation artifact, which is awell-characterized artifact in TSE sequences (21). but dueto its different nature in SER-TSE it may possibly be mit-igated through amplitude scaling using a separate mea-surement of stimulated echo amplitudes. A technique notyet explored is to use phase cycling to separate the cor-rectly timed and the incorrectly timed echoes into differ-ent data sets, without the use of any spoiler scheme. Com-plex addition of these two data sets would permit recov-ering the entire signal present in a TSE sequence. Thismight be the direction to go for T2-weighted SER-TSEimaging.

Slice Profile Improvements

Since the refocusing pulse is used with a weaker sliceselect gradient the resulting slice profile in SER2-TSE isdegraded compared to the standard TSE sequence. Thesimulated profile quality is even lower for the outer slice ofSER-TSE sequences with SER-factors higher than 2 al-though the inner slices have a better profile, which isessentially the profile of the excitation pulse. The outerside of each slice is also influenced by the sidebands of RFpulses, which excite and refocus adjacent slices groups(commonly referred to as “cross talk”). This effect is alsopresent in standard TSE measurements and can be re-duced by acquiring adjacent slices in an interleaved man-ner. While the resulting slice profile in TSE is almostsymmetrical, it will be asymmetrical in SER-TSE due tothe simultaneous refocusing of multiple adjacent slices.Furthermore, the slice profile would be different for eachindividual slice of the SER-group, which might be prob-lematic. Using tailored RF refocusing pulses could opti-

mize the slice profile but this would lead to higher energydeposition and thus higher SAR. However, the currentlyemployed RF-pulses are optimized for TSE applications.Further work is needed to optimize the RF-pulses for SER-TSE requirements.

Another possibility, at least for SERF � 2, would be tomodulate the original refocusing pulse by the frequencyoffset of both slices. This would allow slice positions thatare not necessarily adjacent. However, if the same refocus-ing pulse as for standard TSE sequences would be used theSAR of this modulated pulse would be twice as high as inthe standard case, which would negate the advantage ofSER. Again, further research is necessary to optimize theRF-pulses for SER-TSE experiments.

Measurement Time and SNR Considerations

Comparing a TSE sequence with a SER-TSE with exactlythe same timing, i.e., the same RF pulses and identicalecho spacing, it can be shown that the signal bandwidthper slice is increased by the SER factor. Thus, the SNR perrepetition of the SER-TSE will be approximately SERFsmaller than that of the TSE. Since SERF times more slicesare acquired with SER-TSE the TSE sequence must berepeated SERF times to result in the same slice coverage.Hence, for a given measurement time, the SER-TSE can berepeated SERF times resulting in an SNR increase ofSERF. Thus, a SER-TSE sequence yields the same SNRas a standard TSE sequence. However, one possible advan-tage is that since the bandwidth is increased, fewer off-resonance artifacts might occur. SER-TSE could add con-siderable benefits for situations with limited slice coverageand/or challenging SAR restrictions. The bandwidth ofstandard TSE sequences often cannot be increased anyfurther, since the refocusing RF-pulses would be spacedtoo closely in time and, therefore, the SAR limitationswould be exceeded. Since the distance between the refo-cusing RF pulses is larger in SER-TSE, higher bandwidthsper image can be used until the SAR limit is reached. Webelieve that this will be a tremendous benefit especially forhigh magnetic field scanners at 3 T and above.

Reduction in SAR

In the Results we showed that the SAR is reduced dramat-ically by the SER-TSE technique. With typical sequenceparameters (turbo factor: 3–5, SER factor 2) the SAR can beeasily reduced by a factor of 2. Adjusting the RF pulsespacing right below the SAR limitation and subsequentlychoosing the SER factor allows the measurement time to beused as optimally as possible without exceeding the SARlimitation. This will be especially important at high fieldstrengths, where the SAR limitation is even more strin-gent.

CONCLUSIONS

We have presented a new imaging pulse sequence thatgenerates multiple spin-echoes in each period between theRF refocusing pulses of a CPMG sequence. To date onlyone spin-echo per RF refocusing has been acquired inearlier CPMG measurements and in TSE (RARE) imaging


sequences. The simultaneous spin-echo refocusings usefewer RF pulses for significantly lower RF power deposi-tion than TSE sequences while producing T1-weightedimages of comparable contrast and quality. SER efficientlygenerates a larger number of spin-echoes compared to aTSE sequence. In T1-weighted imaging the periodic spoilerscheme removes only the fraction of undesirable stimu-lated echo signals, retaining many of the stimulated echoesto contribute to a higher SNR, a marked advantage overearlier spoiler schemes. In contrast to phase cycling meth-ods this allows images to be acquired within a singlerepetition. While particularly useful for T1-weighted im-aging with short echo trains, the SER principle with thecurrent periodic spoiler scheme results in significant sig-nal loss in longer echo trains. These are commonly usedfor T2-weighted imaging, where low flip angle approachesto reduce SAR would undoubtedly be more advantageousat this time.

APPENDIX A

In this section a simple estimation of the SAR value of TSEand SER-TSE sequences is presented, which allows quan-tification of the SAR reduction with SER-TSE sequences.The SAR is defined (22) at a point in the absorber, as thetime rate of change of energy transferred to charged parti-cles related to an infinitesimal volume V. A simple esti-mation of the overall SAR of the subject for a given se-quence can be made by summing up the SAR value of eachindividual RF pulse within a given time interval. For com-parison between the TSE and SER-TSE sequences, theknowledge of the actual SAR values for the 90 and the 180°RF pulses is not necessary, as long as they are the same forboth TSE and SER-TSE sequences. This holds mostly truefor the experimental setup presented in this publication. Itis further assumed that the duration of each echo train isthe same in both sequences, i.e., the bandwidth of theSER-TSE is twice that of the TSE sequence. The SAR valuerepresents the SAR per acquired slice,

with TF � turbo factor,NSLC � number of slices per TR cycle, andSERF � SER factor, number of slices, which are refo-

cused by one 180° pulse,the total SAR estimation per TR cycle for TSE sequence

yields

SARTSE � NSLC � SAR90� � NSLC � TF � SAR180�

� �SAR90� � TF � SAR180� � NSLC. [A1]

The same estimation for the SER-TSE sequence results in

SARSER-TSE � NSLC � SAR90� �NSLC � TF

SERF� SAR180�

� �SERF � SAR90� � TF � SAR180� �NSLCSERF

. [A2]

The SAR reduction for the SER-TSE is then given as

SARSER-TSE

SARTSE�

�SERF � SAR90� � TF � SAR180�

�SAR90� � TF � SAR180� � SERF.

[A3]

Assuming that SAR180° is four times the SAR90° the ratiosimplifies to

SARSER-TSE

SARTSE�

�SERF � TF � 4

�1 � TF � 4 � SERF. [A4]

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