Abstract
Fetal MR now plays an important role in the clinical work-up of pregnant females. It is performed mainly at 1.5 T. However, the desire to obtain a more precise fetal depiction or the fact that some institutions have access only to a 3.0 T scanner has resulted in a growing interest in performing fetal MR at 3.0 T. The aim of this article was to provide a reference for the use of 3.0 T MRI as a prenatal diagnostic method.
INTRODUCTION
Although fetal MRI was first described 1983,1 only with recent advances in MR technologies, including the development of fast sequences introduced in the 1990s, could fetal MR be performed without sedation. In the past decade, further improvements in MR techniques led to a broader acceptance in clinical practice and the use of fetal MR as a supplementary method for the evaluation of suspicious fetal anatomy. Fetal MRI now plays an important role in the clinical work-up of pregnant females. Currently, fetal MRI is performed mainly at 1.5 T, but, recently, a growing interest in 3.0 T examinations has emerged, not only for university and research use.2–4 The wish to perform fetal MR at 3.0 T is due to the increased signal-to-noise ratio (SNR) and probable decreased acquisition time, increased spatial resolution and ultimately a more precise fetal depiction.5,6 Another point is that some institutions may have access only to a 3.0 T scanner. However, using fetal MRI at 3.0 T at the clinical level is challenging and there is little experience with this technique.
This review article specifically concentrates on the clinical use of fetal MR at 3.0 T and attempts to assess the advantages over 1.5 T. A systematic literature review of the most recent publications relevant to fetal MR at 3.0 T was conducted.
The aim of this article was to provide a reference for the use of 3.0 T MRI as a prenatal diagnostic method.
GENERAL ASPECTS
In general, the switch from 1.5 to 3.0 T requires an optimization of sequence parameters to maintain the desired image contrast.7 Achieving T1 contrast can be challenging. T1 relaxation times (TRs) differ between the respective tissues, but are generally longer than those on 1.5 T.7 The decreased T1 tissue contrast on 3.0-T images may be compensated by a longer TR, which increases the duration of the sequence or parallel imaging, leading to a decrease in SNR.8 Another possibility to increase T1 contrast at 3.0 T is optimizing the flip angle. Ultrafast spoiled gradient-echo sequences can be used without a significant gain in time compared with 1.5 T, allowing these sequences to be performed during breath-holding. T2 TR slightly decreases with increasing magnetic field strengths.9 Owing to more pronounced local magnetic field inhomogeneities, T2 decay is shorter at 3.0 T. As a result, T2 contrast is improved but also gives rise to unwanted artefacts, which, in another point of view, increases diagnostic sensitivity, depending on the pulse sequence.8 The SNR at 3.0 T is nearly two times as high compared with 1.5 T.5–7 As a consequence, noise and random granular image appearance is reduced. The increased SNR can be used to improve image quality, invested into increased spatial and/or temporal resolution of dynamic sequences.
An important point at 3.0 T is artefacts. Inhomogeneities of the magnetic field are induced by the tissue interfaces, which lead to field distortion as a consequence of their susceptibility, shape and orientation relative to the field.10 With respect to fetal MRI, this means that shimming may become necessary during the examination, thus increasing the overall examination time. Standing wave artefacts (Figure 1) and conductivity artefacts are two effects that are particularly strong artefacts at the end stage of pregnancy or in females with multiple pregnancies. Standing wave artefacts11 represent regional brightening and signal loss, caused by constructive and destructive interference of the standing waves. This is because at 3.0 T, the wavelength of the radiofrequency (RF) field is on the same scale as the size of the field of view used in many abdominal MRI examinations and tends to be more pronounced with increasing field of view, such as that required in fetal MRI.12 A related artefact, called a conductivity artefact,13 is caused by the interaction of the RF field and highly conductive tissue or liquids in the body. As it is difficult to tackle field inhomogeneities and standing wave artefacts, a promising and more advanced technique for compensation includes multichannel transmission body coils14,15 and several manufacturer-implemented software for reducing standing wave artefacts at 3.0 T, “MultiTransmit” (Philips, Best, Netherlands), “ZOOMit” (Siemens). In our experience, which is in line with Victoria et al,6 steady-state free-precession (SSFP) sequences are more vulnerable to banding artefacts (Figure 2), which are off-resonance effects.16 One way to reduce these artefacts is to optimize shimming or to adjust TR. Susceptibility artefacts deteriorate with increasing magnetic strengths (Figure 3) and can be twice as large at 3.0 T compared with that at 1.5 T.17 Especially sensitive to these artefacts are echoplanar imaging (EPI) sequences, and this increased susceptibility brings advantage in the detection of intracranial bleed. To minimize susceptibility artefacts, readout direction can be changed, parallel imaging implemented and echo times shortened. Two other possible modifications but which lead to an SNR ratio are a wider readout bandwidth or use of smaller voxel sizes. Chemical shift artefacts are more prominent at 3.0 T than they are at 1.5 T, but owing to the fact that fetal fat is not present until later in pregnancy, it is not a significant problem in fetal imaging.3
INDICATIONS
In general, indications do not differ from those at 1.5 T.18–27
However, regarding specific clinical questions, 3.0-T fetal MRI has the potential to supply more detailed information than lower field strengths.
The increased susceptibility at 3.0 T enhances the sensitivity for deoxyhaemoglobin, haemosiderin (Figure 4) and calcifications. In addition, bony structures are more sharply delineated even on T2 weighted (T2W) and SSFP sequences (Figure 5).
Sequences that benefit from the increased SNR at 3.0 T are T1 weighted (T1W) and T2W sequences, diffusion tensor sequences and spectroscopy.8 The twofold increased chemical shift effect of 3.0 T compared with 1.5 T has a positive effect on the quality of spectroscopy8 and blood oxygen level-dependent techniques.2 These facts have an impact on especially brain imaging.
In the following, only those indications are addressed where the use of 3.0 T might be more helpful than 1.5 T.
Brain malformation
Disorders of cortical development are a common cause of neurodevelopmental delay and epilepsy. These may be very subtle and difficult to detect with ultrasound imaging. Fetal MR can depict the cerebral cortex nicely, outline abnormalities and improve the prenatal diagnosis of malformations of cortical development (Figure 6). Here, T2W sequences of good quality are very important to adequately evaluate the structure of the brain. At 3.0 T, acquisition of T2W sequences with an average slice thickness of 2–3 mm is possible, compared with 3–5 mm at 1.5 T, isovoxel (1-mm slice thickness). In addition to describing gyration and cortical sulcation, white matter development can be described by discerning the different layers of the developing brain, e.g. the ventricular/periventricular zone, intermediate zone, subplate and cortical plate28 (Figure 7), and at an earlier gestational age (Figure 8).
Diffusion tensor imaging
Diffusion tensor imaging (DTI) provides better visualization of tracts. In partial or incomplete commissural agenesis, DTI helps to differentiate which commissure is absent and what kind of fibres connect the hemispheres or in cases of a tumour, how the tracts are displaced or even absent (Figure 9). The commissures are composed of the corpus callosum and the anterior and hippocampal commissure. Agenesis of the corpus callosum can be complete or partial. In complete agenesis, there are no fibres crossing the midline, and this is often associated with interhemispheric cysts and lipomas. A perfect mid-sagittal T2W slice is important to delineate the commissures (Figure 10). At 3.0 T, DTI can be acquired with a higher SNR for fibre tracking, although it is difficult to obtain high-quality images owing to the long acquisition time required29 and movement artefacts.
Haemorrhagic lesions
In acquired brain damage, for example, the previously normally formed tissue is destroyed. There are numerous causes for this and the study of organs besides the central nervous system is important for diagnosis.30 With the different sequences available (T2W, SSFP, fluid-attenuated inversion recovery, EPI and diffusion-weighted imaging), MR can discriminate even slight differences, depict small details, characterize the extent of damage and lead to a diagnosis. At 3.0 T, higher susceptibility allows depiction of deoxyhaemoglobin/haemosiderin on T2W images. EPI can depict intra-axial or extra-axial haemorrhage (Figure 4) and calcifications. In the near future, susceptibility-weighted imaging could become a useful imaging technique to delineate fine cerebral vascular structures31 and delineate microhaemorrhages and calcifications.
Pathologies involving bones
A frequent question in fetal MR is whether there are facial defects.32 In addition to the precise evaluation of the maxillofacial anatomy and a demonstration of the extent of the defect (cleft lip, alveus, palate), associated anomalies can also be depicted. Besides T2W and SSFP sequences (Figure 5), EPI sequences (Figure 11) are best used to study the defects.33 They should be acquired in the coronal, axial and sagittal planes. Higher susceptibility at 3.0 T facilitates delineation of ossified structures, counting vertebral bodies/rips. EPI sequence at 3.0 T better delineates subtle osseus structures of the fascia, for example the nasal bone (Figure 12), and evaluates, for e.g., spinal defects and skeletal dysplasias.34 Higher susceptibility at 3.0 T also facilitates counting of vertebral bodies and ribs (Figure 5). In addition, the cartilage can be assessed with SSFP (Figure 5). In the future, susceptibility-weighted imaging might add useful information in this area. In addition, with thinner T1W images, the normal hyperintense-appearing fetal subcutaneous fat around the 27th gestational week (GW)3 (Figure 13) and fatty replacement of affected muscles in the muscular dystrophies (Figure 14) can be evaluated.
Thoracoabdominal pathologies
In addition to the normal pulmonary tissue, which is subject to a substantial maturation process and can be followed with a change in T1 and T2 signal,35 fetal MR can nicely delineate lung masses, which may be solid, cystic or mixed. The most common intrinsic lung lesions are congenital cystic adenomatoid malformations and pulmonary sequestration. Lung volumetry is an important prognostic parameter to assess pulmonary hypoplasia and may facilitate prenatal counselling and is achieved mainly with manual tracing on axial T2W slices over the thorax.35–37 Here, with thinner T2W slices, the lung tissue can be traced more exactly and the estimated lung volume will be more accurate. With thinner T2W slices, the feeding vessel in pulmonary sequestration can be visualized.
Congenital diaphragmatic hernia is an important fetal pathology, where abdominal contents enter the thoracic cavity through a defect in the diaphragm. The herniated organs compress the lungs and cause a mediastinal shift with deviation and compression of the heart. One important question in addition to the characterization of the herniated organs (Figure 15), assessment of the lung volume and pulmonary maturity is the measurement of the size and location of the defect,38 where thinner slices might be helpful. In anterior wall defects, such as gastroschisis or in omphalocele, the assessment of the extent of herniation, content and width of the abdominal wall defect in gastroschisis is important.39
In the fetal gastrointestinal tract (GIT), one of the main uses of MRI is to assess the meconium, which is of hyperintense signal on T1W sequences (Figure 16) and is a sign of maturation of the GIT. Together with the fluid content in the rest of the bowel seen on a T2W sequence, bowel function and patency can be evaluated, for example, in GIT obstruction, such as oesophageal atresia, duodenal obstruction and small and large bowel stenosis. In atresia or stenosis, dilation of the bowel proximal to the site of obstruction can be depicted. A complication of intestinal atresia may be perforation of the small bowel, which results in meconium peritonitis. At 3.0 T, thin T1W images (1.4 mm) show more details of meconium-filled bowel parts and might be helpful in evaluating complex malformations, such as cloacal dysgenesis, with a higher resolution and better contrast of the acquired images, position of the rectum in the pelvis and its position relative to the bladder. Organs such as the spleen, pancreas and uterus can be routinely delineated.6
Vascular malformations
At 3.0 T, a higher sensitivity to flow leads to a better identification of vessels.40
Whether the higher field strength might have an impact on the characterization of other pathologies that have become routine indications for fetal MRI, such as pulmonary malformations,35,41 placental imaging, heart imaging (Figure 17),42 dynamic sequences for swallowing process, fetal general movements43 or assessing residual kidney with diffusion-weighted imaging (Figure 18), has yet to be proved.
However, the use of 3.0 T also has some disadvantages compared with 1.5 T: most sequences have a longer duration (Table 1), making them more sensitive to motion-related artefacts and thus increasing the examination time, as more repetitions may be necessary than that at lower field strengths. In addition, artefacts from amniotic fluid cannot be completely avoided. As a consequence, pathologies associated with polyhydramnios, such as oesophagus atresia, should rather be examined at lower field strengths. Tissue heating is also increased at 3.0 T,44 albeit this heating is not dangerous for the fetus, it is uncomfortable for the pregnant female.
Table 1.
Sequence | FOV (mm) | Matrix | TR (ms) | TE (ms) | Flip angle (degree) | Slice thickness/gap (mm) | Number of slices | Acquisition time (s) | Main indications |
---|---|---|---|---|---|---|---|---|---|
Survey T1/TFE | 450 | 256 × 128 | 8 | 2.3 | 15 | 5–8/0 | 31 | 41 | Fetal position |
Survey T2/TSE | 400 | 268 × 200 | Shortest/3.5 | Shortest/1.75 | 60 | 6/0 | 31 | 82 | Fetal position |
T1 ultrafast GE FS | 250 | 168 × 153 | Shortest/3.12 | 1.49 | 10 | 1.5–3/0 | 31 | 21 | Brain: haemorrhage, calcifications |
T1 ultrafast GE FS | 375 | 252 × 230 | Shortest/3.32 | 1.57 | 10 | 4/0 | 27–40 | 15–21 | Body: thyroid, kidneys, digestive system (meconium) |
T1 ultrafast GE | 250 | 168 × 153 | Shortest/3.12 | 1.49 | 10 | 3/0 | 31 | 14 | Haemorrhage, calcifications, fat |
T2 single-shot ultrafast SE | 250 | 228 × 204 | Shortest/5500–9800 | 200 | 90 | 2–3/0 | 25–32 | 25–35 | Brain: anatomy, CSF |
T2 single shot ultrafast SE | 280 | 256 × 229 | Shortest/5400–8750 | 100 | 90 | 3–4/0 | 32–48 | 24–37 | Body: lung development, stomach, airway |
T2 SSFP | 250 | 168 × 125 | Shortest/3.7 | Shortest/1.83 | 90 | 6/−3 | 21 | 43 | Brain: cysts |
T2 SSFP | 400 | 268 × 200 | Shortest/3.8 | Shortest/1.90 | 90 | 4–6/0 | 21 | 38 | Body: vessels, heart |
FLAIR | 230 | 112 × 89 | 7500 | 63.1 | – | 3.5/1 | 15–25 | 45 | Brain: lamination, content of cystic lesions |
GRE EPI | 250 | 120 × 115 | 1000 | 35 | 90 | 2–3/0 | 23–31 | 8–16 | Bone/cartilage, haemorrhage |
DWI (b = 700) | 400 | 132 × 134 | 4600 | Shortest/65 | 90 | 5/0.5 | 84 | 78 | Body: kidneys, haemorrhage |
DWI (b = 700) | 230 | 152 × 106 | 2247 | Shortest/74 | 90 | 4/1.17 | 24 | 24 | Brain: ischaemia, haemorrhage |
SSFP Dynamic | 450 | 212 × 281 | 2.8 | 1.39 | 90 | 10–30/2.35 | 120 (6 fps) | 28 | Fetal movements, swallowing |
T1 FFE dynamic | 300 | 152 × 149 | Shortest/3.1 | Shortest/1.44 | 10 | 2 | 8 (6 fps) | 37 | Bowel movements |
Single-shot MRCP | 450 | 428 × 341 | 9449 | 487 | 90 | 40 | 9 | 106 | 3D fetus and surroundings |
DTI (6 directions) | 250 | 135 × 96 | Shortest/1400 | Shortest/112 | 90 | 4/0 | 15 | 106 | Tractography |
DTI (15 directions) | 250 | 135 × 96 | Shortest/856 | Shortest/112 | 90 | 4/0 | 10 | 57 | Tractography |
Spectroscopy | – | 12 × 12 | 2000 | 144 or shorter | – | – | – | 164 | Metabolite measurement |
BOLD | 230 | 96 × 94 | 907 | 35 | 90 | 4 | 15 | 50 | fMRI, placenta |
3D, three-dimensional; BOLD, blood oxygen level dependent; CSF, cerebrospinal fluid; DTI, diffusion tensor imaging; DWI, diffusion-weighted imaging; EPI, echoplanar imaging; FFE, fast field echo; FLAIR, fluid-attenuated inversion recovery; fMRI, functional MRI; FOV, field of view; FS, fat saturated; GE, gradient echo; GRE, gradient recalled echo; MRCP, magnetic resonance cholangiopancreatography; SE, spin echo; SSFP, steady-state free-precession; TE, echo time; TFE, turbo field echo; TR, relaxation time; TSE, turbo spin echo.
SAFETY CONCERNS
Of concern when scanning the fetus at a higher magnetic field strength is the energy absorbed by the fetus during MRI and measured in the form of specific absorption rate (SAR). Numerous studies conclude that there is no reason not to perform fetal MR on a 3.0 T system, although caution is suggested when performing scans without using a normal-level SAR mode, as the maximum local SAR value can be violated and may fall in the body of the fetus.45,46 According to a recent study, the SAR of a fetal MR of the brain with adapted sequences is lower at 3.0 T than that at 1.5 T,5 but contradictory to a previous publication.47 Despite no evidence supporting any actual harm to the fetus, potentially unknown risks of SAR and RF energy deposition exist. Focal hot spots caused by RF field inhomogeneity and standing wave effects, where the SAR is higher, may complicate the effects of heating. Because of this, the SAR needs to be more closely monitored during 3.0 T examinations.
As a result, the Food and Drug Administration has imposed limits for RF exposure of 4 W kg−1 for maternal whole-body exposure, independent of the magnetic field strength, and scanner fail-safe mechanisms have been put in place to ensure these exposure levels are not exceeded. The International Commission on Non-Ionizing Radiation Protection (ICNIRP) 2004 guidelines state that the body temperature of the patient who is pregnant should not rise >0.5 °C and the temperature of the fetus should not exceed 38 °C.48 With regard to the question of MR safe practices and the maximum field strength that can be applied, the report of the Canadian Task Force on Preventive Health Care concludes “Foetal magnetic resonance imaging is safe at 3.0 T or less during the second and third trimesters”.49 The practice parameter of the American College of Radiology concludes about fetal MR at 3.0 T: “At this stage, the preponderance of research studies have failed to discover any reproducible harmful effects of exposure of the mother or developing fetus to the 3.0 T or weaker magnetic fields used in the routine clinical MR imaging process. However, far less is known about the potential effects, if any, of the time varying gradient and/or RF magnetic fields used during actual scanning to potentiate image generation”. And it goes on: “These theoretical risks should be carefully balanced against the potential benefits to the patient undergoing a MR examination”.50 More conservative in its conclusion is the British Association for Perinatal Medicine: “Given that doubling field strength increases the specific absorption rate (SAR) by a factor of 4, scanning at 3.0 T is currently not performed outside a research setting”.51 These findings suggest that care should be taken to monitor both the local and whole-body SAR in patients who are pregnant and suggest that if careful monitoring is performed, scanning of the fetus can be performed safely at both 1.5 and 3.0 T. In any case, all MRI equipment have a built-in system that prohibits exposure beyond the Food and Drug Administration limits (4.0 W kg−1).
With regard to the potential risk of acoustic damage to the fetus at 3.0 T MRI, there are no data that there is a relevant effect on fetal audition. Gradient field switching produces acoustic noise, which may be detrimental to fetal auditory development.52 Reports of evidence of hearing loss, shortened gestation and low birth weight in cases where the fetus was exposed to excessive noise in utero exist,53 but this was caused by chronic maternal exposure to loud noise and not acute noise levels experienced during fetal MRI examinations. Despite the lack of evidence about the risk of acoustic damage to the fetus, some safety measures can be applied. For example, an acoustic foam, placed on the scanner table, can be used to further decrease sound transmission to the fetus. Recently, new advanced noise reduction technologies, referred to as “Quiet Suite” (Siemens) and “Silent Scan” (GE), were introduced, which act on fast gradient switches.
CONCLUSION
In general, with appropriate sequence adaptations, examinations of the fetus at 3.0 T are comparable with the images obtained at 1.5 T. Because of the higher image resolution and SNR, finer structures and lesions can be delineated at 3.0 T. A major drawback is that examinations at 3.0 T are more prone to artefacts, which complicates imaging the fetus for classic referrals (maternal obesity, polyhydramnios). It is important to decide which system might be better to address which indication (Table 2). But, is fetal MRI at 3.0 T ready for routine use? The final answer is, yes it is.
Table 2.
Indications | Reasons |
---|---|
Indications for 3.0 T | |
Brain | Intraparenchymal resolution |
Bones | Sensitivity for susceptibility effects |
Gestational age <GW 18 | Resolution |
Cartilage (joints) | Resolution |
Abdominal organs (pancreas, uterus) | Resolution |
Angiography | Background suppression |
Indications for 1.5 T | |
Polyhydramnios | Less sensitive to moving fluids |
Maternal sensitivity to heat | Less warming |
Multiplets | Shorter duration |
Large maternal habitus | Less sensitive to artefacts |
Contributor Information
Christian Weisstanner, Email: Christian.Weisstanner@insel.ch.
Gerlinde M Gruber, Email: gerlinde.gruber@meduniwien.ac.at.
Peter C Brugger, Email: peter.brugger@meduniwien.ac.at.
Christan Mitter, Email: christian.mitter@meduniwien.ac.at.
Mariana C Diogo, Email: mariana_cdiogo@hotmail.com.
Gregor Kasprian, Email: gregor.kasprian@meduniwien.ac.at.
Daniela Prayer, Email: daniela.prayer@meduniwien.ac.at.
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