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REVIEW Fetal magnetic resonance imaging: jumping from 1.5 to 3 tesla (preliminary experience) Teresa Victoria & Diego Jaramillo & Timothy Paul Leslie Roberts & Deborah Zarnow & Ann Michelle Johnson & Jorge Delgado & Erika Rubesova & Arastoo Vossough Received: 12 July 2013 /Revised: 20 October 2013 /Accepted: 11 December 2013 # Springer-Verlag Berlin Heidelberg 2014 Abstract Several attempts have been made at imaging the fetus at 3 T as part of the continuous search for increased image signal and better anatomical delineation of the developing fetus. Until very recently, imaging of the fetus at 3 T has been disappointing, with numerous artifacts impeding image analysis. Better magnets and coils and improved technology now allow imaging of the fetus at greater magnetic strength, some hurdles in the shape of imaging artifacts notwithstanding. In this paper we present the preliminary experience of evaluat- ing the developing fetus at 3 T and discuss several artifacts encountered and techniques to decrease them, as well as safety concerns associated with scanning the fetus at higher magnetic strength. Keywords Magnetic resonance imaging . Fetus . 3.0 tesla . Safety . Artifacts Introduction MR imaging of the gravid patient was first reported in 1983 [1], with the initial applications primarily related to maternal and placental abnormalities [2]. In the 1990s ultrafast MR sequences evolved, decreasing fetal motion artifact and allowing the evaluation of the highly mobile fetus. Fetal MR imaging was soon shown to be complementary to US in the evaluation of multiple fetal pathologies. In parallel, improved MR imaging technology and stronger magnets allowed the transition from the 0.6-T machines first available for imaging to the currently utilized 1.5-T machines. In 2002, the U.S. Food and Drug Administration approved the use of 3-T mag- nets for human use. Since then numerous papers have praised its use for imaging of the brain [3], musculoskeletal system [4] and abdomen [5] and for various indications [6]. The search for better anatomical delineation and evaluation of the fetus warrants evaluation of the feasibility of imaging at 3 T. Another reason to consider fetal imaging at 3 T is that some imaging centers only have one magnet available for all of their imaging needs, that magnet being a 3-T system. Anecdotal presentations have been made discussing imaging of the fetus at 3 T, mostly coming from Europe and more often with disheartening results. The goal of this paper is to present the preliminary experience at the Childrens Hospital of Phil- adelphia with fetal imaging at 3 T, with a focus on one of the main impediments: the numerous artifacts encountered at 3-T MRI. These are particularly prominent in the case of the moving fetus within an environment of amniotic fluid. Gain in signal-to-noise ratio: advantages of 3-T imaging The signal created at MR imaging is the result of an excess of unpaired protons aligned in the direction of the magnetic field. The number of aligned protons is directly proportional to the CME activity This article has been selected as the CME activity for the current month. Please visit the SPR Web site at www.pedrad.org on the Education page and follow the instructions to complete this CME activity. T. Victoria (*) Radiology Department, Center for Fetal Diagnosis and Treatment, The Childrens Hospital of Philadelphia, 34th Street and Civic Center Boulevard, Philadelphia, PA 10104, USA e-mail: [email protected] D. Jaramillo : T. P. L. Roberts : D. Zarnow : A. M. Johnson : J. Delgado : A. Vossough Radiology Department, The Childrens Hospital of Philadelphia, Philadelphia, PA, USA E. Rubesova Department of Radiology, Lucile Packard Childrens Hospital, Stanford University, Stanford, CA, USA Pediatr Radiol (2014) 44:376386 DOI 10.1007/s00247-013-2857-0

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REVIEW

Fetal magnetic resonance imaging: jumping from 1.5 to 3 tesla(preliminary experience)

Teresa Victoria & Diego Jaramillo & Timothy Paul Leslie Roberts &

Deborah Zarnow & Ann Michelle Johnson & Jorge Delgado &

Erika Rubesova & Arastoo Vossough

Received: 12 July 2013 /Revised: 20 October 2013 /Accepted: 11 December 2013# Springer-Verlag Berlin Heidelberg 2014

Abstract Several attempts have been made at imagingthe fetus at 3 T as part of the continuous search forincreased image signal and better anatomical delineationof the developing fetus. Until very recently, imaging ofthe fetus at 3 T has been disappointing, with numerousartifacts impeding image analysis. Better magnets andcoils and improved technology now allow imaging ofthe fetus at greater magnetic strength, some hurdles inthe shape of imaging artifacts notwithstanding. In thispaper we present the preliminary experience of evaluat-ing the developing fetus at 3 T and discuss severalartifacts encountered and techniques to decrease them,as well as safety concerns associated with scanning thefetus at higher magnetic strength.

Keywords Magnetic resonance imaging . Fetus . 3.0 tesla .

Safety . Artifacts

Introduction

MR imaging of the gravid patient was first reported in 1983[1], with the initial applications primarily related to maternaland placental abnormalities [2]. In the 1990s ultrafast MRsequences evolved, decreasing fetal motion artifact andallowing the evaluation of the highly mobile fetus. Fetal MRimaging was soon shown to be complementary to US in theevaluation of multiple fetal pathologies. In parallel, improvedMR imaging technology and stronger magnets allowed thetransition from the 0.6-T machines first available for imagingto the currently utilized 1.5-T machines. In 2002, the U.S.Food and Drug Administration approved the use of 3-T mag-nets for human use. Since then numerous papers have praisedits use for imaging of the brain [3], musculoskeletal system [4]and abdomen [5] and for various indications [6].

The search for better anatomical delineation and evaluationof the fetus warrants evaluation of the feasibility of imaging at3 T. Another reason to consider fetal imaging at 3 T is thatsome imaging centers only have one magnet available for allof their imaging needs, that magnet being a 3-T system.Anecdotal presentations have been made discussing imagingof the fetus at 3 T, mostly coming from Europe and more oftenwith disheartening results. The goal of this paper is to presentthe preliminary experience at the Children’s Hospital of Phil-adelphia with fetal imaging at 3 T, with a focus on one of themain impediments: the numerous artifacts encountered at 3-TMRI. These are particularly prominent in the case of themoving fetus within an environment of amniotic fluid.

Gain in signal-to-noise ratio: advantages of 3-T imaging

The signal created at MR imaging is the result of an excess ofunpaired protons aligned in the direction of the magnetic field.The number of aligned protons is directly proportional to the

CME activity This article has been selected as the CME activity for thecurrent month. Please visit the SPR Web site at www.pedrad.org on theEducation page and follow the instructions to complete this CME activity.

T. Victoria (*)Radiology Department, Center for Fetal Diagnosis and Treatment,The Children’s Hospital of Philadelphia,34th Street and Civic Center Boulevard,Philadelphia, PA 10104, USAe-mail: [email protected]

D. Jaramillo : T. P. L. Roberts :D. Zarnow :A. M. Johnson :J. Delgado :A. VossoughRadiology Department, The Children’s Hospital of Philadelphia,Philadelphia, PA, USA

E. RubesovaDepartment of Radiology, Lucile Packard Children’s Hospital,Stanford University, Stanford, CA, USA

Pediatr Radiol (2014) 44:376–386DOI 10.1007/s00247-013-2857-0

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strength of the magnetic field, such that at higher strengths,more protons are available to create the MR signal withresultant increased net magnetization. The signal depends onthe square of the magnetic field strength, quadrupling at 3 T;yet the noise also doubles such that the overall theoretical gainof signal-to-noise ratio (SNR) at 3 T doubles in magnitude.Other parameters also affect the overall gain of signal, includ-ing longitudinal relaxation time (T1), transverse relaxationtime (T2) and sequence parameters. In practice, and as pub-lished inmultiple prior papers [5–7], the overall gain of signal-to-noise ratio at 3 T is more likely to be 1.7–1.8 times thesignal at 1.5 T (Fig. 1). This gain in SNR can then be exploitedto achieve higher image quality or traded for increased spatialresolution, increased temporal resolution (decreased acquisi-tion time), or a combination of both. In the case of fetalimaging, where the target is usually very small and highlymobile, this gain can theoretically represent a tremendousadvantage. The gain in signal-to-noise ratio can also allowmore streamlined implementation of SNR-hungry applica-tions such as use of parallel imaging with multichannel coilsto speed up single-shot MRI protocols, to reduce echo time onlong echo train sequences to mitigate susceptibility, and todecrease radiofrequency heating by minimizing the number ofpulses.

3-T coils and gain in signal-to-noise ratio

One crucial contributor to the SNR performance is theradiofrequency coil. Phased-array technique combinesmultiple coil elements to provide a large field of viewwhile maintaining signal. Our 3-T phased-array coilshave 32 available elements, of which, depending onthe field of view, 8 are usually used for imaging at agiven time during fetal scanning. This is in contrast tothe typical 6-channel phased-array coil configurationused at 1.5-T fetal scanning. In addition to thephased-array coil, a surface coil is placed anterior tothe mother’s abdomen; for the 3-T magnet the surfacecoil is equipped with 18 elements, whereas for the 1.5-T magnet it contains only 6 elements. An importantadvantage of utilizing phased-array coils is the potentialto employ parallel imaging. In this technique, the num-ber of samples in k-space is reduced by a factor of twoor greater, thereby significantly shortening the acquisi-tion time [8], a critical advantage in fetal imaging, whenit is difficult for the mother to hold her breath for longperiods of time and when the fetus is frequently moving(Fig. 2). Relative loss of signal-to-noise ratio is a lim-itation to the use of parallel imaging. However theoverall gain of signal while imaging at 3 T is such thatthis small loss does not detract from the gain of usingthis technique.

3-T protocol modification

Changes in T1 imaging

As the magnetic field strength increases, so does tissue T1relaxation time. For the soft tissues of the abdomen and pelvisin the adult patient T1 relaxation time has been reported to beapproximately 20–40% longer at 3 T than at 1.5 T [9] and foradult musculoskeletal tissues, approximately 15–22% greater[4]. Although no data detail exact relaxation times in fetal tissue,it is fair to assume that they are also longer at 3 T than at 1.5 T. Ifthe same signal strength is to be maintained, repetition timeshould be increased. However an increase in repetition timeresults in unwanted increased acquisition time and potentiallyworsening motion artifact of a highly mobile fetus. Our current3-T protocols (Tables 1 and 2) reflect an increase in repetitiontime at 3 T, while the matrix is held constant and the field ofview is decreased, with additional signal gain coming from theincreased number of coil elements at 3 T (see above). Theoverall acquisition time remains essentially the same for bothmagnet strengths (about 1 s per slice), such that image quality isnot compromised. The use of flip-angle characteristics can alsoaffect the T1 properties of the evaluated soft tissues, withincreasing angles resulting in increased T1 contrast (Fig. 3).

Practically speaking, there are some differences in the ex-pected T1 signal of the fetal soft tissues at higher magnetstrength, the most conspicuous being the iso- to slightly hy-perintense liver when compared to the lungs (Fig. 3). Thismight be caused by the shorter T1 time and characteristics ofthe liver compared to the lungs. At 1.5 T, the inherent T1hyperintense signal of the liver is a helpful feature in certainpathologies, including congenital diaphragmatic hernia. In thesefetuses, it is crucial to determine whether there is herniatedintrathoracic liver, because a herniated intrathoracic liver is anegative prognostic indicator of postnatal outcome [10–12].MR can be very helpful in evaluating liver position because the

�Fig. 1 Comparison between fetuses of equal gestational ages imaged at1.5 T and 3 T MRI. a, b Two fetuses at 23 weeks of gestational age.Sagittal steady-state free precession (SSFP) images at (a) 1.5 T and (b)3 T show increased soft-tissue contrast at 3 T, with increased detail of thehepatic and renal parenchyma. c, d Two different fetuses, shown at27 weeks of gestational age, who have left congenital diaphragmatichernia and herniated liver (arrow in d). In these sagittal half-acquisitionsingle-shot fast spin-echo (SSFSE) images at 1.5 T (c) and 3 T (d), theoverall conspicuity of the fetal soft tissues is increased at 3 T. e, f AxialSSFP images of the same fetuses as in (c) and (d). At 3 T (f) there is moredetail of the herniated bowel than at 1.5 T (e), and the border between theliver and bowel is better delineated. g, h SSFSE images of two fetuses at29 weeks of gestational age. Axial images at 1.5 T (g) and at 3 T (h) showthe migrational bands at 3 T (arrows in h), whereas at 1.5 T they are notvisualized. i, j Same fetuses as in (g) and (h). Sagittal images at 1.5 T (i)and at 3 T (j) show at 3 T a clear visualization of the aqueduct and opticchiasm (arrowand arrowhead, respectively, in j). kAxial image shows thefetal pancreas (arrows) in a different 28-week fetus can be seen at 3 T inthis SSFSE image; in the experience of the authors, the pancreas is neverseen at 1.5 T at this gestational age. B bowel, L liver, S stomach

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echogenicity of liver and lung at US is similar, limitingevaluation [13]. At 3 T, where the fetal liver is iso- to slightlyhyperintense with respect to lung, it can be more difficult thanat 1.5 T to unequivocally define liver position. However, whenanalyzed in conjunction with other available fluid-sensitive sequences, including echoplanar sequences

and single-shot fast spin-echo (SSFSE) and steady-statefree precession (SSFP) sequences, liver position shouldbe easily discernible.

Another difference when imaging at T1 is the improvedcontrast of the osseous structures, which remain dark againstthe intermediate signal of the surrounding soft tissues. At 3 T

Table 1 Scanning parameters for fetal body MRI

Plane Sequence FS TR/TE (ms) ETL FOV (mm) Matrix Slice/gap NEX Other imaging parameters

3-plane localizers T2 SSFSE No 1,100/80 192 250–300 265×205 3/0 1 FA-180, Pat-2, PPF-4/8, PO-63%

Sagittal T1 SGE No 180/4.76 - 250–300 256×205 4/0 1 FA-75, Pat-2, PO-25%

Coronal T1 VIGRE No 3.49/1.37 - 250–300 192×192 2/0 1 Breath hold

PPF-6/8, SPF-6/8

PO-40%, FA-10%

3 planes T2 SSFP No 4.35/1.86 - 250–300 256×256 4/0 1 PO-25%, FA-70

3 planes T2 SSFSE No 1,100/78 205 250–300 256×205 3/0 1 Pat-2

PO-63%, FA-180, PPF-4/8

ETL echo train length, FA flip angle, FOV field of view, FS fat saturation, Pat parallel acquisition technique, PO phase oversampling, PPF partial phasefourier, SGE spoiled gradient echo, SPF slice partial fourier, SSFP steady-state free precession, SSFSEhalf-acquisition single-shot fast spin echo, VIGREvolume interpolated gradient echo

Fig. 2 Twenty-four-week fetuswith omphalocele. a Sagittal 3-TSSFSE MR image of the fetuswithout parallel imaging. b Thesame fetus with parallel imaging.Note the increased conspicuity ofthe soft tissues and increasedsignal-to-noise ratio in (b)manifested as increased sharpnessof the vertebral bodies and cardiaccontour. SSFSE half-acquisitionsingle-shot fast spin echo

Table 2 Scanning parameters, neuro-fetal MRI

Plane Sequence FS TR/TE (ms) ETL FOV (mm) Matrix Slice/gap NEX Other imaging parameters

3 planes T2 SSFSE No 1,100/62 205 250–300 256×205 3/0 1 FA-150, PO-50%, Pat-2

3 planes T2 SSFSE No 1,100/78 205 250–300 256×205 3/0 1 FA-150, PO-50%, Pat-2

Axial, coronal EPI Yes 5,030/40 - 250–300 192×192 3/0 1 PPF-7/8, FA-90

EPI factor – 192, PO-25%, Pat-2

Axial, coronal EPI Yes 4,430/29 - 250–300 192×192 3/0 1 PPF-6/8, FA-90, Pat-2

EPI factor– 192, PO 25%

Axial T1 SGE No 204/4.76 - 250–300 256×166 4/0 1 FA-60, PPF-7/8, PO-25%, Pat-2

EPI echoplanar imaging, ETL echo train length, FA flip angle, FOV field of view, FS fat saturation, Pat parallel acquisition technique, PO phaseoversampling, PPF partial phase fourier, SGE spoiled gradient echo, SSFSE half-acquisition single-shot fast spin echo

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increased sharpness and spatial resolution of the osseousstructures can be achieved (Fig. 4), including those of thenotoriously difficult-to-analyze hands and feet. This mightbe helpful when evaluating the fetus with a presumed diagno-sis of skeletal dysplasia, because US has limited sensitivity inevaluating such entities and MRI at 1.5 T provides limitedbony detail [14]. Future studies could determine whether 3-Tfetal imaging helps in the prenatal evaluation of the fetus witha diagnosis of skeletal dysplasia.

Also improved is visualization of the subcutaneous fat inthe developing fetus, which can be seen as early as the mid- tolate second trimester, whereas at 1.5 T this is delayed until thethird trimester (Fig. 5).

The remaining structures that are bright at 1.5 T remain so at3 T, namely the thyroid and meconium [15]. It is worth men-tioning that in our limited experience with the second- andthird-trimester fetus (the youngest fetus had a gestational age of20 weeks), the dynamics of meconium signal, well described inprior papers [16, 17], appear unchanged between 1.5 T and 3 T.

Changes in T2 imaging

T2 relaxation time is essentially unchanged or slightly de-creased with increasing magnetic field strengths, possibly be-cause somemechanisms of T2 relaxation are prolonged, where-as others become more efficient [6]. T2* is the observed or

Fig. 3 Coronal 3-T T1-weighted spoiled gradient echo (SGE)MR imagesof a 30-week fetus at different flip angles. a 30°, (b) 60°, (c) 75°. Noteincreased T1 hyperintensity of the liver (L) and meconium (arrow) with

increasing flip angles. d, eCoronal T1-W SGE images in a 1.5-T magnetwith flip angles of 30° (d) and 75° (e). Note the increased T1 character ofboth liver and meconium at 1.5 T when compared to a 3-T magnet

Fig. 4 Evaluation of bony structures at 3 T MRI. aSagittal 3-T T1-W SGEimage of a 24-week fetus clearly demonstrates the fivemetacarpals (the handsand feet are notoriously difficult to evaluate at 1.5 T). b T1-W SGE image

shows sharp scoliosis in this 24-week fetus. c Sagittal T1-W SGE imagedemonstrates sharp visualization of the vertebral bodies in this 30-week fetus.Note the relatively hypointense liver (arrow). SGE spoiled gradient echo

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effective T2 value, a product of the intrinsic T2 value mixedwith the local field inhomogeneity. The effect of T2* is morepronounced at the greater magnet strength and results in greatermagnetic susceptibility than at 1.5 T, which is discussed below.

Artifacts encountered at 3 T

Magnetic field heterogeneity and standing wave artifact

At 3 T it is more difficult to maintain a homogeneous field,resulting in worsening of a number of artifacts. Radiofrequen-cy field inhomogeneity is one of the main challenges of fetalimaging at 3 T, particularly for echoplanar, spin-echo andsteady-state free precession sequences. The increase in mag-net strength translates into an increase in frequency and adecrease in wavelength. In water and amniotic fluid, thedecreased radiofrequency wavelength at 3 T might approxi-mate the size of the field of view. This causes the generation ofstanding waves and constructive and destructive interferencepatterns that result in heterogeneous signal, manifested asareas of hypointensity or blackout mixed with areas of bright-ening. The larger the field of view in comparison with thewavelength, the worse the artifact becomes, making the im-aging of obese and pregnant patients particularly challengingat 3 T [6, 7].

There is an additional hurdle in imaging fetuses at 3 T: thepresence of amniotic fluid. At 3 T the rapidly changingmagnetic field induces a circulating electrical current fieldthrough the highly conductive amniotic fluid. The current actsas an electromagnet that opposes the changing magnetic field,reducing the amplitude and dissipating the energy of theradiofrequency field. This radiofrequency shielding artifact,

also called “conductivity effect,” manifests as hypointenseareas in the regions of radiofrequency inhomogeneity [7,18]. In fetal imaging, these two effects, an enlarged abdomencoupled with the presence of amniotic fluid, combine toproduce particularly undesired artifacts that result in areas ofblackout centered in the field of view, where the fetus ispositioned. This artifact is particularly accentuated on thesingle-shot fast spin-echo sequences, the workhorse of fetalimaging.

Several approaches can be used to minimize standing waveartifacts or so-called dielectric resonance artifacts. One feasi-ble method to improve field homogeneity is the use of dielec-tric pads or radiofrequency cushions, given the method’ssimplicity and non-invasiveness. The cushions contain a gelencapsulated in synthetic material. The gel is mixed with agadolinium- or manganese-based medium to eliminate thesignal from the gel itself. The conducting material has a highdielectric constant and shorter wavelength than the surround-ing soft tissues, altering the magnetic field inhomogeneity bypractically changing the geometry of the imaged subject [19].There is one impediment of its use in the gravid patient: theweight of the commercially available pad, 4–6 k, cannot betolerated when placed on the anterior abdominal wall of agravid patient. One way to bypass this is to create alternative,lighter dielectric pads. In 2007 Kataoka et al. [20] showed in apreliminary study that pads filled with saline solution can beas effective as the ones filled with gel. We designed a salinecushion that acts as a dielectric pad. This pad contains four150-cc bags of saline solution placed in a pillow, which isplaced flat onto the maternal abdomen. This saline cushion,which weighs about 2 lb in total, is easily tolerated by thepregnant patient and results in partial dissipation of the dielec-tric artifact (Figs. 6 and 7).

Alternative ways to decrease the radiofrequency field in-homogeneity artifacts include use of multichannel transmis-sion body coils [21] and active radiofrequency shimmingcoupled with parallel imaging [22], although these techniquesare not widely available on all MR systems. As reported in theliterature, use of multichannel transmission body coils canprovide a more uniform radiofrequency field resulting inenhanced field homogeneity, reduced dielectric shading andimproved consistency of the images [23].

In steady-state free precession sequences, field inhomoge-neity can result in off-resonance effects, potentially aggravat-ing banding artifacts, particularly at the edge of the field ofview. Changing the orientation of scanning or the field ofview, or modifying the radiofrequency frequency or band-width might help to displace the artifact away from the areaof interest, without eliminating the artifact from the image.

When interpreting the images, the practical effect of fieldinhomogeneity results in a relatively greater time spent ma-nipulating window and level settings, even if almost invari-ably each individual fetal structure can be better seen at 3 T.

Fig. 5 Coronal 3-T T1-W SGEMRI in this 24-week fetusdemonstrates the rim of T1hyperintense fat along the surface ofthe fetus; this is not usuallyidentified until the third trimesterusing 1.5 T MRI. SGE spoiledgradient echo

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Magnetic susceptibility artifacts

Another artifact commonly encountered at 3 T fetal imaging ismagnetic susceptibility. This refers to the extent a materialbecomes magnetized in a field and occurs at the interface ofsubstances with different magnetic susceptibility. Local fieldinhomogeneity can result in intravoxel dephasing, resulting insignal attenuation, image geometric distortion and localizedregions of high or low signal intensity [18]. Susceptibilityartifacts worsen with increasing magnetic strengths, beingapproximately twice as large at 3 T as at 1.5 T [7]. This isparticularly the case with echoplanar sequences. This artifactis more conspicuous at the interface of the gas-filled colon inechoplanar imaging sequences (EPI), more so in the older,vertex-positioned fetus, where the head is in close appositionto the maternal rectum. Yet there are potential advantages tothis increased susceptibility, including increasing conspicuityof intracranial or adrenal bleeds on echoplanar imaging se-quences (Fig. 8).

A few technical modifications can minimize the degree ofdistortion of the image, including changing the readout direc-tion to alter the location of the artifact away from the field ofview, implementing parallel imaging and using shorter echo

times (TE). In brain imaging, use of a lower echo timesat 3-T imaging is often necessary compared to 1.5-Timaging in order to decrease geometric distortion of thehead and accentuated susceptibility of intracranial ves-sels seen on echoplanar imaging. The normal suscepti-bility and hypointensity of deoxyhemoglobin within theintracranial venous structures is accentuated at 3 T com-pared to 1.5 T, which can interfere with a reliablediagnosis of intracranial hemorrhage. Reduction of echotime is generally necessary at 3-T imaging to offset thisaccentuated hypointensity and conspicuity of the ves-sels. Use of a wider readout bandwidth or use of small-er voxel sizes also have a similar effect in decreasingsusceptibility, but all of these modifications need to bebalanced with the resultant decrease in signal-to-noiseratio.

Chemical shift artifact at 3 T

In general chemical shift artifacts are accentuated at 3 Tcompared to 1.5-T imaging. Yet this is not an issue in fetalimaging because the two sources of fetal fat (subcutaneous

Fig. 6 Use of saline pads. Sagittal 3-T SSFSE MRI of a 25-week fetuswith myelomeningocele. The scan was done with (a) and without (b)saline pads placed over the maternal abdomen. The dark band or standingwave artifact secondary to dielectric artifact seen along the heart in (b) isdissipated in (a). c The same imaging parameters as in (a) with the

exception of decreased slice thickness (3 mm in this image versus5 mm in a). Note the increased resolution of the soft-tissue structureswith the higher slice thickness. SSFSE half-acquisition single-shot fastspin echo

Fig. 7 Dielectric pads. Axial 3-T EPIMRI of a 23-week fetus at the level of the kidneys shows the fetus with (a) and without (b) dielectric pads over thematernal abdomen. Note the increased field homogeneity and decreased distortion of the images with the dielectric pad. EPI echoplanar imaging

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and intra-abdominal fat) appear relatively late in pregnancy,thus not contributing to artifact formation.

Magnetic resonance safety

While the benefits of signal-to-noise ratio and concomitantadvantages of spatial or temporal resolution are compellingfor fetal MRI at 3 T, several considerations should beevaluated to ensure the safety of mother and child. Apremise of this discussion is the concept that, for clinicallyindicated patients, the benefits of MRI outweigh any pro-cedure risks at 1.5 T. Two to three decades of practicegenerally support this widely held belief [24–26]. Thediscussion below outlines key safety considerations andtheir impact at 3 T MRI, in direct comparison to those at1.5 T. Issues to be addressed are:

(1) static field exposure,(2) gradient field switching, and(3) radiofrequency power deposition.

Static field exposure

There is little direct evidence of harmful effects with short-term exposure to high static magnetic fields. Although onestudy of frog embryos exposed to long durations of 16-Tmagnetic fields demonstrated a mechanistically plausible in-teraction [27], it is difficult to extrapolate from this papergiven (1) the much shorter exposure times in humans during

diagnostic imaging, (2) the lower magnetic fields (16 T vs.3 T) and (3) the fact that we are dealing with fetuses asopposed to embryos.

Gradient switching

In conventional MRI, the process of image formation requiresthe application of exogenous linear magnetic field gradients(in x- or y- or z- directions) at various short time periods, toencode spatial position across the body. Most current MRIdevices limit the maximum magnetic field gradient to approx-imately 40–50 mT/m. Given this relatively low value incontrast to the 3 T (3,000 mT) of a static field it is not likelythat the mere presence of the gradient field is contributory torisk. However because these gradient fields are pulsed on andoff at key times as dictated by the imaging pulse sequence,attention has to be paid to the changing magnetic field expe-rienced during onset and offset of a magnetic field gradientpulse. Especially in rapid imaging techniques, such asechoplanar imaging, where gradient pulses are applied andreversed extremely rapidly in order to obtain snapshot images,it is possible that high rates of change of magnetic field aretransiently experienced. By Faraday’s law of electromagneticinduction, a conducting material experiencing such a chang-ing magnetic field will experience an electrical current. Inpractice this means that exposure to magnetic field gradientswitching carries with it the risk of involuntary peripheralnerve stimulation. Most contemporary MR hardware limitsthe magnetic field gradient switching rate (slew rate) to ~200mT/m/ms. Given the length of magnetic field gradient coils(~1 m), this implies a changing magnetic field of up to 100

Fig. 8 Axial spin-echo EPIsequence (a) performed at 3 Twitha technique typically used at 1.5 T(TR/TE=4,930/94 ms, no parallelimaging) shows marked geometricdistortion and susceptibility. bDecreasing the TE to 29 ms andenabling parallel accelerationfactor of 2 markedly decreases thegeometric distortion and excessivesusceptibility artifacts. c, dAxialspin-echo EPI in a 25-week fetuswith myelomeningoceledemonstrates increased conspicuityof normal veins and germinalzones of the brain at higher echotime (TE 42 ms in image c; TE29 ms in image d). Care must beexercised not to confuse thesenormal structures with abnormalfoci of hemorrhage in the brain.EPI echoplanar imaging, TE echotime, TR repetition time

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mT/ms (or 100 T/s), 50-cm removed from the center of theimaging field of view. U.S. Food and Drug Administrationsafety limits, in fact, prevent exposure to changing magneticfields (dB/dt) of more than 60 T/s, with scanner failsafesoftware limiting these exposures. Furthermore, because thefetus is generally at or near the center of the imaging field ofview during imaging, fetal exposure changes are much lower(e.g., 1 cm from the imaging FOV center the dB/dt is only 2 T/s even at maximum slew rates). Of further note, maximumslew rates are similar at both 1.5 T and 3 T and thus incre-mental risks at 3 T vs. 1.5 T are essentially negligible. In fact,the FDA limits of exposure to changing magnetic fields areindependent of magnetic field strength.

Radiofrequency power deposition

The excitation and refocusing radiofrequency pulses ofthe MR sequences deposit energy into the subject beingimaged. The rate of energy deposition is defined by thespecific absorption rate (SAR), which is reported inW/kg and is based on approximate modeling of thesubject body.

The rate of energy deposition is dependent on the ampli-tude of the applied radiofrequency fields, which tends toincrease with increasing magnetic field strength and in factquadruples in transitioning from 1.5 T to 3 T (all other factorsbeing kept constant). Optimizing radiofrequency pulse designmight be expected to mitigate this phenomenon, for exampledecreasing the number of slices, lowering the flip angles,increasing repetition time, the use of parallel imaging tech-niques and shorter echo train lengths (in fast spin-echo se-quences) can all decrease the specific absorption rate. Al-though in general, energy deposited can lead to undesiredsubject heating, a variety of fluid and flow mechanisms mightmitigate this in practice. However these factors are not con-sidered in determining worst-case-scenario limits to specificabsorption rate. The FDA safety limits for radiofrequencyexposure are set at 4 W/kg for the maternal whole body(independent of static magnetic field strength), with scannerfailsafe controls prohibiting exposure beyond that. Of practi-cal note, typical fetal MR pulse sequences are shown inTable 3, along with their specific absorption rate loadsat 1.5 T and 3 T for approximately equivalent imagecontrasts. The values were obtained for a phantom fetus(Fig. 9), constructed with bottles of different consisten-cies (oil, water, cream-based salad dressing) that couldsimulate the soft-tissue consistencies of the fetus. Thisphantom fetus was wrapped in saline bags imitating theamniotic fluid and then placed inside an adult body-typephantom emulating the mother. Their specific absorptionrates were then obtained at 1.5 T and 3 T. Values werealso obtained for real fetuses at 1.5 T and 3 T, all of

them kept well below the whole-body exposure limit of4 W/kg required by the FDA.

Aside from the maternal whole-body specific absorptionrate limitations stipulated by the FDA, there is an additionalconsideration to the specific absorption rate received by thefetus: its inhomogeneous distribution among the imaged fetalsoft tissues [28]. Radiofrequency field inhomogeneity anddielectric and standing wave effects may produce focal SARhot spots that can be projected around or within the fetus. Thiscomplication is addressed by recent sophisticated modeling ofthe fetal environment by Hand et al. [28, 29], who suggest thatthe maximum energy deposited to the fetus is a fraction of thatreceived by the mother. In their calculations, the highest localspecific absorption rate is in the mother, with the fetus beingexposed to a peak of 50–70% of the maternal maximum SARat 3 T. They also showed that in MRI studies done undernormal-mode operating conditions set forth by the Interna-tional Electrotechnical Commission in 2008, where the ma-ternal whole-body average specific absorption rate is ≤2W/kgand the fetal whole-body specific absorption rate is 1.24W/kgand 1.14W/kg at typical 1.5-Tand 3-Tconfigurations, respec-tively [28]. They also stipulated that the average temperatureof the fetus under these conditions remains below 38OC.Care must be placed to limit the amount of time imag-ing the fetus, however, because the maximum tempera-ture predicted in the fetus can exceed 38OC followingcontinuous exposures of about 7.5 min or longer. In

Table 3 Specific absorption rate loads for MR imaging at 1.5 T and 3 T.Note that values are always kept below the 4 W/kg required by the U.S.Food and Drug Administration

SSFSE SSFP T1 EPI

1.5 T Fetus ≤2.1 ≤2.1 0.6 ≤0.71.5 T Phantom ≤0.8 0.7 ≤0.8 <0.7

3 T Fetus ≤2.8 1.4 1.6 0.2

3 T Phantom 1.6 1.4 1.1 0.2

EPI echoplanar imaging, SSFP steady-state free precession, SSFSE half-acquisition single-shot fast spin echo

Fig. 9 Fetal phantom containing fluids of different consistencies iswrapped in saline solution bags, created to measure the specific absorp-tion rates. Refer to Table 3 for further correlation

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practice, our fetal imaging protocols do not use longcontinuous exposures, with most sequences falling wellbelow the 1-min scanning time.

Alternative methods to decrease specific absorptionrate aim at minimizing dielectric and standing wave arti-facts by decreasing radiofrequency field inhomogeneity, atask that can be accomplished by the use of multichannelphased-array and parallel transmission, as discussed above[30, 31].

Taken together, although there are very real concerns aboutthe safety of the MRI procedure to the fetus at 3 T, the variousmechanisms that could theoretically have a biologically plau-sible impact are limited to the levels associated with ongoingscanning at 1.5 T.

IRB approval and informed consent prior to scanning fetusesat 3 T

The rationale for scanning at 3 T is to take advantage of theadditional signal intensity and resolution. The goal is to obtainthe best and most detailed anatomical information of the fetusto make the best informed decisions about management. Withthis in mind, after thorough discussion with the InstitutionalReview Board (IRB) department, and armed with extensiveinformation about the safety of fetal scanning at 3 T, weproceeded to scan. The reason to do so was to optimize aclinically indicated study of the fetus, done to potentiallyimprove the visualization of existing abnormalities. Becausethis was not research but a clinically indicated examination,IRB approval was not required, as agreed by the head of theIRB department.

Our institution does not require written informed consentprior to MR scanning at 1.5 T or 3 T for any anatomical part.This includes fetal imaging at 1.5 T. We extrapolated thisthinking for fetal 3-T imaging.

We also recognize that these guidelines might not apply atall institutions, and that directors at each center have to makepolicies and rules as they see fit.

Conclusion

We have presented our preliminary experience in imaging thefetus at 3 T. As expected in other fields of 3-T imaging, thesignal-to-noise ratio is superior to that at 1.5 Twhen techniqueis optimized. Yet numerous hurdles are presented along theway, mainly in the form of artifacts. These can be minimizedwith techniques discussed in this paper. Future work will bedone to further improve the available sequences with the aimof obtaining the highest-quality images to improve diagnosticaccuracy when evaluating the developing fetus.

Conflicts of interest None

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