Indications expand for fetal MR imaging

May 15, 2006

Fetal MRI has become established in clinical practice over the past decade. MRI is indicated when conditions do not favor fetal ultrasound such as cases of maternal obesity or anhydramnios.1 It has also been shown that fetal MRI may discriminate among tissue components that do not display impedance differences on ultrasound; for instance, laminae in the developing brain.2 These advantages, along with MR's ability to delineate small structures, such as cranial nerves, has furthered its use as an adjunct to ultrasound in fetal imaging.1 Applications for fetal MRI are growing. The development of improved methods for fetal imaging, including availability of ultrafast sequences,3 has also furthered adoption.

Fetal MRI has become established in clinical practice over the past decade. MRI is indicated when conditions do not favor fetal ultrasound such as cases of maternal obesity or anhydramnios.1 It has also been shown that fetal MRI may discriminate among tissue components that do not display impedance differences on ultrasound; for instance, laminae in the developing brain.2 These advantages, along with MR's ability to delineate small structures, such as cranial nerves, has furthered its use as an adjunct to ultrasound in fetal imaging.1 Applications for fetal MRI are growing. The development of improved methods for fetal imaging, including availability of ultrafast sequences,3 has also furthered adoption.

Doctors performing fetal MRI face two main challenges. The first is to visualize very small structures within a constantly moving subject. The second involves early detection of impaired development. Certain anomalies present with subtle signs that are quite different from postnatal symptoms. Lissencephalies, for instance, may be recognized before onset of gyration by a disturbed lamination of the brain parenchyma.2 Other pathologies may be undetectable in early stages but become obvious later. For example, it is difficult to detect the course of the bowels before they become filled with fluid and meconium during the 23rd and 24th weeks of gestation. This means that bowel malrotation will remain undetectable until that time.4

Clinicians should meet with patients before they undergo fetal MRI to gain detailed information on relevant indications. They should also explain the implications and consequences of possible results. Radiologists and radiographers should explain details of the scanning procedure and ensure that the patient is positioned comfortably with coil-receptor elements close to the fetus. The presence of an assistant during the examination may be helpful; for instance, if coils need to be repositioned. This can be necessary if the fetus is large or if there are multiple fetuses. An assistant can also encourage better patient cooperation, which is a prerequisite to optimal image quality.

Image quality is additionally affected by the availability of MR hardware and sequences suitable for fetal imaging and an appropriate imaging protocol. The protocol should be adjusted to suit gestational age, organs being imaged, and the clinical question being addressed.3 Producing a suitable protocol means selecting the highest possible matrix and smallest field-of-view that will permit imaging during a defined time window (usually not longer than 30 seconds) but without producing infolding artifacts.

Ultrafast sequences originally designed for abdominal imaging have proven useful for fetal MRI, primarily where T2-weighted contrast is used.5,6 Ultrafast T2-weighted steady-state free precession (SSFP) and single-shot fast spin-echo (SSFSE) sequences remain the mainstay of prenatal MRI. Conventional half-Fourier acquisition single-shot turbo spin-echo (HASTE) and SSFSE sequences are both excellent at depicting fetal organs at all gestational ages. Ultrafast sequences can supply additional information (see table).

SSFP sequences may provide extra information on vessels and the fetal heart (Figure 1). Acquisitions planned as a dynamic sequence can demonstrate intrinsic movement of fetal organs and gross fetal movement. Acquisitions involving a heavily T2-weighted thick slab (up to 40 mm) can provide an overview of the whole fetus within seconds (Figure 2).

T2-weighted echo-planar imaging (EPI) is used to assess the placenta and to gain information about susceptibility effects. EPI-based diffusion-weighted sequences may be performed to demonstrate ultrastructural details in various organs (Figure 3B). T1-weighted sequences are used to demonstrate cell density, protein and lipids, and methemoglobin (Figure 4). Increasing experience has shown that fine-tuning these sequences with respect to gestational age, respective organ, and clinical question may improve the accuracy of MR findings.7

POTENTIAL PITFALLS

Certain fetomaternal conditions may complicate the MR examination. Polyhydramnios, for instance, is often associated with increased fetal motility. Imaging is best scheduled immediately after therapeutic reduction of amniotic fluid in these circumstances. Artifacts from maternal breathing may be overcome by performing breath-hold sequences. These are usually well tolerated if no longer than 15 seconds.

Artifacts caused by maternal or fetal motion may be mitigated by shortening the sequence. This is done by using parallel imaging and reducing the matrix or echo time. If the echo time is reduced, and the relaxation time is set on "shortest," the acquisition time of the respective sequences will decrease by a factor of 10 to 20 seconds.7 Thick- slab single-shot T2-weighted MR sequences, which provide an overview of intrauterine contents, may be helpful in cases of increased fetal movement.

Bad positioning of the region of interest with respect to the coil's receptor elements can result in pathologies being disguised or misinterpreted. Repositioning the coil will help in these cases. Inappropriate sequence choice may additionally prevent delineation of certain structures.

It is important to remember that a single morphological anomaly is often just the tip of the iceberg. An accurate estimation of overall prognosis requires examination of the whole fetus, including extrafetal intrauterine structures. Imaging planes should also be oriented orthogonally to the organ of interest.

CLINICAL APPLICATIONS

By far, the most experience with fetal MRI has been gathered in the brain.2,8,9 Normal development is demonstrated by visualizing the cortical folding and maturation states of the parenchyma.7,10 The cerebral cortex can be delineated easily against surrounding cerebrospinal fluid on T2-weighted SSFSE sequences. These also show lamination of the brain parenchyma between gestational weeks 18 and 28.

Good tissue contrast and high spatial resolution make T2-weighted sequences (Figure 3A) the method of choice for depicting brain malformations that include small structural changes such as heterotopia. Information from T1-weighted and diffusion-weighted MRI will be required in cases of suspect acquired pathologies.11 T1-weighted hyperintensity may indicate methemoglobin-containing hemorrhagic lesions (rare) or calcifications that are caused by hemorrhage or infection (more common). Diffusion-weighted sequences may reveal acute ischemic lesions at a time when these appear isointense on other sequences. Movement studies provide further clues on the developmental state of the fetal central nervous system.12

Evidence gathered during the past few years has shown that MRI may contribute valuable information to assessments of fetal lung maturity.13 This can be accomplished through accurate volumetry studies and measurements of T2-weighted signal intensities.14 The degree of lung maturity is one of the main life-limiting factors in congenital diaphragmatic hernia, intrauterine growth restriction, and premature birth. Information from MRI is thus important for prognosis.

Visualization of the fetal esophagus may be important in cases of suspected atresia, where ultrasound has shown polyhydramnios but failed to demonstrate a fluid-filled stomach. MRI will reveal fluid-filled parts of the esophagus on T2-weighted images (Figure 1). Transportation of a fluid-bolus, in case of stenosis, may be followed on dynamic SSFP sequences.

Fetal abdominal organs change their size, shape, position, and signal properties during the second and third trimesters.4 This is especially true for the bowels. Bowel abnormalities caused by rotation, stenoses, and displacement may be recognized with a combination of T2- and T1-weighted sequences. The former will show the fluid-filled parts, and the latter meconium-filled bowel (Figure 4).

Both the liver and spleen display relatively constant T1- and T2-weighted signals, although the appearance of T2*-weighted images and EPI studies change with increasing content of blood cells.4 The position, form, and signal intensities of these organs, coupled with the presence/absence and number of spleens, may add prognostic information. Renal development is mirrored by an increase in growth and definition of parenchymal structure. Signals from diffusion-weighted MRI may allow identification of displaced kidneys (e.g., pelvic kidney) and can indicate the presence or absence of functional parenchyma.15

Assessment of the fetal skeleton is generally performed with ultrasound.16 Use of EPI sequences that depict bones, however, has made it possible to define spina bifida defects and to characterize skeletal malformations.3 Thick-slab T2-weighted sequences provide a quick overview of muscle relief (Figure 2).

Extrafetal intrauterine structures should not be left out of a fetal MR examination. The integrity of the placenta, umbilical cord, and amniotic fluid are mandatory for normal fetal development. The placenta undergoes characteristic morphological changes as gestation progresses.17 Irregularities in these presentations may be associated with acute or chronic insufficiencies in placental function.18

Acute venous congestion leads to changes on diffusion-weighted images. Chronic impairment may be visualized morphologically as premature aging and/or a lumpy placental surface. The length, thickness, number of vessels, configuration of Wharton's jelly, and insertion of the umbilical cord can be demonstrated on T2-weighted MRI. MR-based volumetry will calculate the amount of amniotic fluid. T1-weighted sequences may reveal hemorrhage into the amniotic cavity.1

Several factors have been responsible for the upturn in fetal MRI. First and foremost, it is no longer necessary to immobilize the fetus by curarization via the umbilical vein or to sedate pregnant patients in order to overcome fetal movement. The availability of ultrafast sequences allows good images to be generated even with a moving fetus. Fetal MRI has become a completely noninvasive method and one that could be considered more often in pregnancy.

Radiologists' experience in this area continues to increase. Obstetricians working in the field of prenatal diagnostics and neonatologists have also come to accept this method of assessment and diagnosis.

Future improvement in fetal MRI should include development of tailored sequences, the advent of dedicated coils, devices that permit optimal patient positioning within the magnet, and MR systems that cater to patient comfort as well as technical progress.

References

1. Prayer D, Brugger PC, Krampl E, et al. Indications for fetal magnetic resonance imaging (MRI). Radiologe 2006 Feb;46(2):98-104. [In German]

2. Prayer D, Kasprian G, Krampl E, et al. MRI of normal fetal brain development. Eur J Radiol 2006;57(2):199-216.

3. Brugger PC, Stuhr F, Lindner C, et al. Methods of fetal MR: beyond T2-weighted imaging. Europ J Radiol 2006;57(2):172-181.

4. Brugger PC, Prayer D. Fetal abdominal magnetic resonance imaging. Europ J Radiol 2006 Feb;57(2):278-93.

5. Semelka RC, Kelekis NL, Thomasson D, et al. HASTE MR imaging: description of technique and preliminary results in the abdomen. J Mag Res 1996;6(4):698-699.

6. Levine D, Barnes PD, Madsen JR, et al. Central nervous system abnormalities assessed with prenatal magnetic resonance imaging. Obstet Gynecol 1999;94(6):1011-1019.

7. Prayer D, Brugger PC, Prayer L. Fetal MRI: techniques and protocols. Pedtr Radiol 2004 Sep;34(9):685-693.

8. Garel C CE, Brisse H, Elmaleh M, et al. Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJNR 2001;22(1):184-189.

9. Levine D, Barnes PD. Cortical maturation in normal and abnormal fetuses as assessed with prenatal MR imaging. Radiology 1999;210(3):751-758.

10. Garel C. Fetal cerebral biometry: normal parenchymal findings and ventricular size. Europ Radiol 2005;15(4):809-813.

11. Prayer D, Brugger PC, Kasprian G, et al. MRI of fetal acquired brain lesions. Europ J Radiol 2006;57(2):233-249.

12. Prechtl HF, Einspieler C. Is neurological assessment of the fetus possible? Eur J Obstet Gynecol Reprod Biol 1997;75(1):81-84.

13. Osada H, Kaku K, Masuda K, et al. Quantitative and qualitative evaluations of fetal lung with MR imaging. Radiology 2004;231(3):887-892.

14. Kasprian G, Balassy C, Brugger PC, Prayer D. MRI of normal and pathological fetal lung development. Europ J Radiol 2006;57(2):261-270.

15. Witzani L, Brugger PC, Hormann M, et al. Normal renal development investigated with fetal MRI. Europ J Radiol 2006;57(2):233-249.

16. Blaicher W, Mittermayer C, Messerschmidt A, et al. Fetal skeletal deformities - the diagnostic accuracy of prenatal ultrasonography and fetal magnetic resonance imaging. Ultraschall Med 2004;25(3):195-199.

17. Blaicher W, Brugger PC, Mittermayer C, et al. Magnetic resonance imaging of the normal placenta. Europ J Radiol 2006;57(2):256-260.

18. Ong SS, Tyler DJ, Moore RJ, et al. Functional magnetic resonance imaging (magnetization transfer) and stereological analysis of human placentae in normal pregnancy and in pre-eclampsia and intrauterine growth restriction. Placenta 2004;25(5):408-412.

DR. PRAYER is an associate professor of radiology at the Medical University of Vienna. DR. BRUGGER is an assistant professor at the Center of Anatomy and Cell Biology at the Medical University of Vienna.