SE

M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

Available online at www.sciencedirect.com

www.elsevier.com/locate/semperi

Techniques, terminology, and indications for MRI in pregnancy

Ray O. Bahado-Singh, MD, MBAa,n, and Luis F. Goncalves, MDb
a b

Beaumont Health System, Royal Oak, MI Oakland University -William Beaumont School of Medicine, Rochester, MI

A RT I C L E IN F O

A B S T R A C T
Fetal MRI is now a well-established imaging modality for the diagnostic evaluation of fetuses

Keywords: Fetal MRI Congenital anomalies Fetal ultrasound

with congenital anomalies. In this article, the authors provide a brief overview of the physical principles involved in fetal MRI imaging, the sequences that are used in clinical practice today, current indications, and limitations. A review of current evidence supports the following indications for fetal MRI: suspected central nervous system anomalies, neck and oropharyngeal masses, diaphragmatic hernia, abdominal masses or bowel pathology not fully characterized by ultrasonography, and suspected fetal infection. Other indications should be decided on a case-by-case basis with close collaboration between the departments of maternalfetal medicine and radiology. More research is needed to determine the role of fetal MRI in functional neuroimaging at higher magnetic eld strengths (3 T). & 2013 Elsevier Inc. All rights reserved.

1.

Introduction

Magnetic resonance imaging (MRI) uses the magnetic properties of the constituent hydrogen atoms from water in the cells of tissues to produce images that can be used both for anatomical and functional evaluation. Scans can be performed using a wide range of sequences that are capable of targeting specic organs with exquisite detail. Some examples include: (1) precise characterization of the presence, extent, and timing of hemorrhage using a combination of T1-weighted (T1WI), T2-weighted (T2WI), gradient echo (GRE), and susceptibility-weighted imaging (SWI),13 (2) diagnosis of cerebral ischemic lesions using diffusion-weighted imaging (DWI),4,5 (3) mapping of white matter tracts using diffusion tensor imaging (DTI) and tractography,6 (4) functional brain mapping using blood oxygen level-dependent imaging (BOLD),710 and (5) non-invasive metabolite proling using magnetic resonance spectroscopy (MRS),1117 among many others. Clinical applications of MRI for the examination of the human fetus have evolved substantially since the rst attempts in the
n

1980s.18 Still, examination of the fetus presents specic challenges, including fetal and maternal respiratory motion, small anatomical structures, and the fact that fetal organs are in a constant state of transformation as the pregnancy evolves from conception to term.19,20 In addition, there is a technological gap between what is currently achievable in MRI imaging of fetuses compared to children and adults. In this article, we review some of the established sequences used for clinical fetal MRI, their terminology, and current accepted indications.

2.

Fetal MRI techniques

Fetal MRI is performed using magnets with eld strength of up to 1.5 Tesla. Research is currently under way to explore the potential benets of fetal imaging using stronger magnetic elds (3 T).2123 The patient is counseled regarding benets, risks, and alternative studies that can be performed to answer the clinical question. No adverse events have been

Corresponding author. Beaumont Health System, Medical Ofce Building, Suite 233, 3535 West 13 Mile Road, Royal Oak, MI 48073. E-mail address: Ray.Bahado-Singh@Beaumont.edu (R.O. Bahado-Singh).

0146-0005/13/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1053/j.semperi.2013.06.010

E M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

335

reported for fetal exposure to MRI; however, studies evaluating long-term effects are lacking. Gadolinium contrast agents are not used in fetal MRI and the exam is performed without sedation.24 The patient history is reviewed in detail for potential contra-indications for magnetic resonance imaging such as the medical insertion of metallic parts. A fetal MRI should only be performed after a high-quality fetal ultrasound has been obtained and after the images from that study have been reviewed. This recommendation is based on the fact that ultrasound and MRI are complementary imaging modalities, with MRI used as a further problemsolving tool.25 Therefore, the physician interpreting the fetal MRI should have knowledge of the prior ultrasound ndings. In addition, the technologist performing the exam and the physician who is interpreting the study should be well versed on fetal anatomy and normal developmental milestones and on how to quickly adjust the imaging planes during the study. Patients can be examined in the supine or left lateral decubitus position, with the receiving coils adjusted as necessary to improve the signal-to-noise ratio (SNR) of the region being examined.20

3. MRI signal generation, pulse sequences, and image encoding

The MRI magnet is always on and once the patient is placed within it, the hydrogen atoms of the mother and fetus align longitudinally with the static magnetic eld. The protons also precess or rotate like a spinning top about the longitudinal (vertical) axis of the magnetic eld with a precession frequency (or resonance frequency) that is proportional to the magnetic eld strength. Thus, the magnetic vector of the spinning proton has two orthogonal components: a longitudinal component that corresponds to the alignment with the static magnetic eld and a transverse or horizontal component that is related to the precessional movement about the longitudinal axis. The actual signal that generates MR images is obtained by proton excitation after application radiofrequency (RF) pulse. Once exposed to a RF pulse with the same frequency as the resonance frequency, protons change their energy state and ip, i.e. go from a longitudinal towards a horizontal position. The ip angle is determined by the strength and duration of the RF pulse. The process results in a decrease in longitudinal magnetization and appearance of transverse (horizontal) magnetization. Once the RF pulse is turned off, relaxation occurs and the stored energy is released and converted to electrical energy, which is converted to a visual image. Longitudinal relaxation results in release of RF energy to the surrounding lattice (the thermal environment through which nuclei exchange energy during longitudinal relaxation) and follows an exponential curve characterized by a tissue-specic time constant T1 that varies according to eld strength. At time T1, 63% of the longitudinal magnetization has returned to its nal value with cessation of the RF pulse. As the spinning protons go out of phase after cessation of the RF pulse, transverse relaxation occurs, with spinspin interaction between the protons and cumulative loss in phase that results in transverse magnetization decay. Transverse magnetization decay is described by an exponential

curve with a time constant T2. At time T2, transverse magnetization will have lost 63% of its original value. T2 values are unrelated to eld strength and are shorter than T1 values. Free induction decay (FID) occurs after a 901 RF pulse is applied, with exponential decay occurring at a characteristic time constant T2* that takes into account tissue-specic spinspin relaxation and static inhomogeneity in the magnetic eld that is explored for specic applications such as the detection of hemosiderin in biological tissues. MRI pulse sequences determine the characteristics of the images to be obtained and are designed to highlight specic properties of the tissues under investigation. Sequences are actually computer programs designed to control the hardware aspects of the imaging process and consist of a combination of different radiofrequency pulse angles (e.g. 901 and 1801), echo times (TE: time between the excitation RF pulse and MR signal sampling), repetition times (TR: time between two excitation pulses), and gradient pulses. Gradient pulses are used to encode the spatial information contained in the nuclear magnetic resonance signal and consist of sliceselection, phase-encoding, and frequency-encoding gradients applied at distinct time points of the MRI pulse sequence. Once the raw data is obtained, it is mapped into a data matrix called k-space and then converted into images using 2D inverse Fourier Transform.19,26

4.

Specic sequences used in clinical fetal MRI

The physics of MRI are complex and beyond the scope of this article. However, anyone who reads an MRI scan needs to understand that even though the images may look anatomically similar, there is a wealth of physiological and pathological information that can only be extracted with an understanding of the characteristics of each sequence and the specic features that the sequence was designed to highlight. The repertoire of pulse sequences used in fetal imaging is limited when compared to pediatric and adult applications. They are designed to provide both high spatial resolution and rapid image acquisition to overcome fetal and maternal breathing movements. Image quality can be improved with the use of phased-array coils with multiple elements, adjusting the position of the coil to target the specic area to be examined. Obese mothers and multiple pregnancies may result in a weaker signal if the structure is far away from the array. A small eld of view is used, with an attempt to ll as much of the eld of view with the fetal anatomy interest as possible in the absence of aliasing. The most common pulsed sequences used in clinical practice are described below. Single-shot T2-weighted sequences are the workhorses of fetal MRI. There are several acronyms depending on the equipment manufacturer, including Half Fourier Rapid Acceleration with Relaxation Enhancement (RARE), Single-Shot Fast Spin Echo (SSFSE), Single-Shot Turbo Spin Echo (singleshot TSE), extended-phase conjugate-symmetry rapid spin echo sequence (EXPRESS), Half Fourier Single-Shot Turbo Spin Echo (HASTE), and Fast Advanced Spin Echo (FASE) sequences. These sequences are capable of producing a single image

336

SE

M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

in approximately 1 s since all the phase-encoding steps necessary to form the image are collected during a single TR. Therefore, the total acquisition time for a 20-frame series is approximately 20 s. Fluid is hyperintense or bright on T2-weighted images making this sequence optimal to evaluate fetal anatomy, including amniotic uid, fetal surface, extra-axial cerebrospinal uid, developing gyrations in the fetal brain, the fetal ventricular system, umbilical cord, placental surface, nasal and oral cavities, middle and inner ear, fetal stomach, intestines, trachea, gallbladder, renal pelvis, urinary bladder, and pathological cystic structures that may develop in the fetus.19,20,26 T1-weighted images are useful in fetal imaging when evaluating for hemorrhage and for the presence of meconium in the large bowel. They also provide selective demonstration of the fetal pituitary, thyroid, and liver and are useful for the demonstration of lipoma of the corpus callosum. Acquisition is usually performed using gradient echo sequences such Spoiled Gradient Echo (SPGR), fast low-angle shot (FLASH), T1-weighted Fast Field Echo (T1-FFE), Fast Field Echo (FastFE), and Steady State Acquisition with Rewound Gradient Echo (RF spoiled SARGE). These are longer-duration acquisition sequences that require maternal breath hold during acquisition and are prone to motion artifacts.19,20,26 Echo planar imaging was more heavily used during the early phases of fetal MRI. Due to poor tissue contrast and spatial resolution compared to modern T2-weighted imaging sequences and the increased sensitivity to magnetic eld inhomogeneity, this sequence is now mainly used as a localizer or with DWI. Because of the sensitivity to magnetic susceptibility artifacts, it may be useful in the evaluation of hemorrhages.19,20 Diffusion-weighted imaging (DWI) sequences are acquired with a B-value of 700 (B-value is a parameter used during the acquisition of diffusion-weighted images that is proportional to the gradient strength squared and diffusion time interval) and using at least three phase-encoding directions. Normally, Brownian diffusion of water molecules within the tissue occurs randomly and evenly in all directions. The protons in the water molecules can be imaged and their path tracked on MRI. Since areas of infarct have restricted Brownian water motion, i.e. obstruction to the free diffusion of the water molecules, they can be depicted as areas of restricted diffusion on DWI. DWI is the basis for more advanced imaging techniques such as diffusion tensor imaging (DTI), which is used to demonstrate brain white matter tracts, with preliminary work in fetuses being recently reported.6,20 Other sequences directed at functional and metabolic imaging (including DTI briey described above) are under active investigation in fetal imaging. These include magnetic resonance spectroscopy (MRS),1117 which provides noninvasive identication of metabolites in the brain and may nd useful applications in the setting of fetal infection/ inammation and hypoxicischemic brain damage, along with blood oxygen level-dependent (BOLD)710 functional MRI, which identies areas of brain activation based on the difference in magnetic properties of oxygenated and deoxygenated hemoglobin. A change in the relative proportion of the two types of Hb occurs with changes in regional blood ow, e.g. after a neuronal discharge in the brain, and

susceptibility-weighted imaging (SWI) allows visualization of changes in regional blood ow.13

5.

MRI versus ultrasonography

The development of fetal MRI techniques predictably lead to comparisons between the accuracy of MRI versus ultrasound. Higher MRI anomaly detection rates were reported for structural defects of the CNS, thorax, abdomen, and skeletal systems in a study of 92 cases by Vimercati et al.27 A review consisting of 13 published studies comparing anomaly detection rate of ultrasound compared to MRI by Bekkar and van Vught28 found that fetal MRI provided additional anatomical information in 45.3% of the cases studied. While the majority of existing studies have found MRI to be superior, there are a few reports suggesting the quality or even marginal superiority of ultrasound.29 There are signicant potential sources of bias in many of the early studies that compared prenatal ultrasound to MRI. The majority of these studies have been retrospective and therefore at signicant risk for bias. The ultrasounds were frequently not performed in expert centers thus increasing the likelihood of additional signicant ndings being made at MRI exam. Further, the ultrasound results were previously known to the radiologist and used in MRI interpretation. Finally, signicant intervals often elapsed between ultrasound and MRI potentially allowing sufcient time for the lesions to evolve in such a way as to make them more identiable at the time of MRI. A number of recent prospective studies that directly compared prenatal ultrasound and MRI have attempted to overcome the biases of earlier publications.3032 In these prospective studies, MRI resulted in signicantly improved diagnostic accuracy compared to ultrasound in the detection of not only CNS but also other anatomical anomalies.

6.

Indications for fetal MRI

The most common clinical indication for fetal MRI is for the evaluation of suspected or proven CNS anomalies. Statistically signicant improved detection rates have been reported with the use of MRI.32 In that study, additional contribution of prenatal MRI to the ultrasound diagnosis was reported in 55% of CNS cases (p o 0.001). A diverse group of CNS abnormalities from ventriculomegaly to germinal matrix hemorrhages was considered. Prenatal differentiation between isolated versus ventriculomegaly associated with other brain anomalies is vitally important given the poor prognosis of the latter. In a large prospective multicenter study of 147 ultrasounddiagnosed cases of isolated ventriculomegaly, MRI found additional CNS abnormalities in 17 % of cases, the most frequent of which was agenesis of the corpus callosum.33 Signicant improvement in diagnostic accuracy has also been reported when MRI was performed after an ultrasound diagnosis of either mild (o15 mm) or greater degrees (415 mm) ventriculomegaly.34 In a prospective study of 185 borderline isolated ventriculomegaly (1012 mm) cases diagnosed with ultrasound, MRI was in agreement with ultrasound in only 57.3% of cases while additional abnormalities

E M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

337

were found in 5.9% of the patients. In mild unilateral ventriculomegaly, additional MRI ndings were found in 6.7% of cases.35 The reported advantages of MRI for CNS examination appear therefore to extend well beyond the assessment of ventriculomegaly. Improved detection of cortical, mid-brain, and hind-brain anomalies, hemorrhages heterotopias, and relatively common CNS pathologies such as agenesis of the corpus callosum.31,36 While diagnosable on ultrasound, MRI appears to have consistently higher sensitivity for many of these disorders. Overall, the majority of the published evidence currently available supports additional contributions of fetal MRI in the further assessment of suspected or conrmed fetal CNS defects undergoing prenatal ultrasound. We therefore recommend that the adjunctive use of fetal MRI be considered when intracranial anomalies are found or suspected on an initial targeted ultrasound. Although there is evidence of improved detection of associated spinal defects when MRI is performed for neural tube defects33 e.g., diastematomyelia, given the high sensitivity of ultrasound we do not believe that a recommendation for routine MRI is justied for this lesion. Where there is a suspicion of spina bida with suboptimal visualization of the spine (e.g., the nding of ArnoldChiari malformation) an MRI should be considered. MRI imaging prior to fetal spinal surgery appears to be a logical circumstance in which this modality may be deployed.

9.

Chest

The clinical benets of routine MRI in cases with chest anomalies have not been established. Some expert opinions suggest a value of MRI in conrming the diagnoses, clarifying tracheal anatomy, and detecting accompanying subtle anomalies.39 Indeed, prospective studies conrm improved detection of chest anomalies with fetal MRI3032 versus ultrasound. A study by Levine et al.40 evaluated 74 fetuses with chest anomalies and found that MRI provided additional information in 38% of cases compared to ultrasound, however this information only changed clinical management in 8% of cases overall. A particular benet of MRI of the fetal chest was its accuracy in determining the position of the liver in congenital diaphragmatic hernias.41 While potentially benecial, we await further evidence regarding the benets of routine prenatal MRI imaging for fetal chest anomalies in clinical practice.

10.

Abdomen

7.

Neck masses

While masses of the fetal neck are relatively easily visualized by ultrasound, MRI can provide signicant additional information. In a small study, Poutamo et al.37 reported that in 75% of cases of fetal neck masses, MRI provided additional information beyond that provided by ultrasound. Importantly, neck masses may compromise the airway leading to asphyxia at birth. MRI provides a panoramic view of the neck, pharynx, and palate and yields information on the size of location of masses and possible inltration of adjacent structures such as trachea, oropharynx, and palate.38 The clinical benets of such information include the ability to plan for and perform the ex-utero intrapartum intubation (EXIT) procedure at birth to ensure patency of the airway. Based on the available evidence, a strong recommendation can be made for the adjunctive use of prenatal MRI for the evaluation of fetal neck masses.

T1-weighted imaging is ideal for the delineation of the fetal bowel because of the hyperintense signal given by the meconium. The appearance is somewhat akin to what one sees on an abdominal lm after a barium enema. For T2weighted sequences, the signal intensity declines from stomach and proximal small bowel to the colon. Solid material including desquamated cells and meconium results in a hyperintense signal in T1 weighted images, making this technique important in the prenatal diagnosis of a range of bowel disorders.42 More precise determination of the level of bowel abnormalities including obstruction and atresia appears possible with MRI. As a consequence, we believe that it is reasonable to recommend fetal MRI for abdominal masses of uncertain signicance or unexplained bowel pathology.

11.

Others

8.

Face and palate

Three-dimensional ultrasound is an excellent tool for the evaluation of the fetal face and palate. Routine fetal MRI for anomalies of the face and palate do not appear to be justied clinically. There are, however, certain circumstances in which an MRI may provide signicant additional information. These include complex, bilateral clefts or in cleft cases in which there is signicant risk of associated brain anomalies.

The recommendations discussed above are based on an assessment of currently available published data. More limited literature suggests the potential utility of fetal MRI for imaging under other important clinical circumstances. Nonbacterial fetal infection poses a signicant risk of CNS damage and long-term neurological morbidity. In a study of 178 cases, Barkovich and Girard43 reported that fetal MRI identied brain abnormalities in 15% of toxoplasmosis infections, 39% in CMV, 18% of varicella, 25.0% of parvovirus, and a percentage of other congenital infections. These ndings suggest a possible role of MRI evaluation in cases of conrmed or strongly suspected congenital toxoplasmosis and other neurotoxic viral infections. In a smaller study of fetal CMV cases however,44 other authors found ultrasound to have superior sensitivity for brain lesions with only a small incremental benet to a subsequent MRI. Given the importance of the presence or absence of prenatal brain damage in counseling and prenatal therapy, e.g. in the case of CMV, and

338

SE

M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

the limited sensitivity of ultrasound in these circumstances, an MRI may be considered when fetal infection is conrmed or strongly suspected. A common scenario in which fetal MRI can be of clinical benet is in the evaluation of pregnancies complicated by anhydramnios or severe reduction of amniotic uid volume. The loss of the sonographic window while signicantly compromising the sensitivity of ultrasound is a perverse benet in MRI imaging since it imposes restraint on the fetal movement. Where there are uncertainties or signicant concerns about a possible fetal anomaly or the absence of a targeted ultrasound exam prior to the onset of oligohydramnios in an at risk fetus an MRI should be considered. The value of MRI for diagnoses of placental accreta has not been established in the average clinical center. Its routine use cannot therefore be recommended at this time. Finally, the issue of timing of the fetal MRI study is an area of practical interest to the obstetrician. Timing of MRI must be dictated by the specic clinical question and the need to obtain additional information at a specic point during pregnancy (e.g. before the limit of viability). For certain disorders that may be seen early by ultrasonography (e.g. ventriculomegaly), more information may obtained on later MRI, after neuronal migration has occurred and cortical development is more advanced. This approach allows a better opportunity to diagnose conditions such as lissencephaly, polymicrogyria/pachygyria, gray matter heterotopias and cortical dysplasias that may not be detectable by early MRI. Indeed, the study by Twickler et al.45 conrmed that additional information provided by prenatal MRI with advancing gestational age. For example in 43.8% of cases at o24 weeks compared to 77.8% of cases at 430 weeks, MRI provided additional information over ultrasound. While delay in imaging until the early third trimester appears to increase the diagnostic benets, it is worth also emphasizing that signicant additional information can still be derived from MRI performed before viability. Should the clinical circumstances require earlier diagnosis, MRI exam performed at o24 weeks should certainly be considered.

r e f e r e n c e s

1. Haddar D, Haacke E, Sehgal V, et al. Susceptibility weighted imaging. Theory and applications. J Radiol. 2004;85:19011908. 2. Meoded A, Poretti A, Northington FJ, Tekes A, Intrapiromkul J, Huisman TA. Susceptibility weighted imaging of the neonatal brain. Clin Radiol. 2012;67:793801. 3. Parizel PM, Makkat S, Van Miert E, Van Goethem JW, van den Hauwe L, De Schepper AM. Intracranial hemorrhage: principles of CT and MRI interpretation. Eur Radiol. 2001;11: 17701783. 4. Baldoli C, Righini A, Parazzini C, Scotti G, Triulzi F. Demonstration of acute ischemic lesions in the fetal brain by diffusion magnetic resonance imaging. Ann Neurol. 2002;52: 243246. 5. Guimiot F, Garel C, Fallet-Bianco C, et al. Contribution of diffusion-weighted imaging in the evaluation of diffuse white matter ischemic lesions in fetuses: correlations with fetopathologic ndings. AJNR Am J Neuroradiol. 2008;29:110115. 6. Kasprian G, Brugger PC, Weber M, et al. In utero tractography of fetal white matter development. Neuroimage. 2008;43:213224.

7. Huppi PS, Inder TE. Magnetic resonance techniques in the evaluation of the perinatal brain: recent advances and future directions. Semin Neonatol. 2001;6:195210. 8. Wedegartner U, Tchirikov M, Koch M, Adam G, Schroder H. Functional magnetic resonance imaging (fMRI) for fetal oxygenation during maternal hypoxia: initial results. Rofo. 2002;174:700703. 9. Wedegartner U, Tchirikov M, Schafer S, et al. Functional MR imaging: comparison of BOLD signal intensity changes in fetal organs with fetal and maternal oxyhemoglobin saturation during hypoxia in sheep. Radiology. 2006;238:872880. 10. Spadoni AD, Bazinet AD, Fryer SL, Tapert SF, Mattson SN, Riley EP. BOLD response during spatial working memory in youth with heavy prenatal alcohol exposure. Alcohol Clin Exp Res. 2009;33:20672076. 11. Girard N, Gouny SC, Viola A, et al. Assessment of normal fetal brain maturation in utero by proton magnetic resonance spectroscopy. Magn Reson Med. 2006;56:768775. 12. Fenton BW, Lin CS, Seydel F, Macedonia C. Lecithin can be detected by volume-selected proton MR spectroscopy using a 1.5 T whole body scanner: a potentially non-invasive method for the prenatal assessment of fetal lung maturity. Prenat Diagn. 1998;18:12631266. 13. Smith LM, Chang L, Yonekura ML, et al. Brain proton magnetic resonance spectroscopy and imaging in children exposed to cocaine in utero. Pediatrics. 2001;107:227231. 14. Smith LM, Chang L, Yonekura ML, Grob C, Osborn D, Ernst T. Brain proton magnetic resonance spectroscopy in children exposed to methamphetamine in utero. Neurology. 2001;57: 255260. 15. Kok RD, van den Berg PP, van den Bergh AJ, Nijland R, Heerschap A. Maturation of the human fetal brain as observed by 1H MR spectroscopy. Magn Reson Med. 2002;48: 611616. 16. Borowska-Matwiejczuk K, Lemancewicz A, Tarasow E, et al. Assessment of fetal distress based on magnetic resonance examinations: preliminary report. Acad Radiol. 2003;10:12741282. 17. Pugash D, Krssak M, Kulemann V, Prayer D. Magnetic resonance spectroscopy of the fetal brain. Prenat Diagn. 2009;29: 434441. 18. Smith FW, Adam AH, Phillips WD. NMR imaging in pregnancy. Lancet. 1983;1:6162. 19. McKenzie CA, Levine D. Current techniques and future directions for fetal MRI. In: Levine D, ed, Atlas of Fetal MRI. Boca Raton, FL: Taylor & Francis Group; 2005. p. 175193. 20. Brugger P. Methods of fetal MRI. In: Prayer D, ed, Fetal MRI. Berlin: Springer-Verlag; 2011. p. 6580. 21. Wedegartner U, Kooijman H, Andreas T, Beindorff N, Hecher K, Adam G. T2 and T2* measurements of fetal brain oxygenation during hypoxia with MRI at 3 T: correlation with fetal arterial blood oxygen saturation. Eur Radiol. 2010;20:121127. 22. Liu F, Garland M, Duan Y, et al. Study of the development of fetal baboon brain using magnetic resonance imaging at 3 Tesla. Neuroimage. 2008;40:148159. 23. Liu F, Garland M, Duan Y, et al. Techniques for in utero, longitudinal MRI of fetal brain development in baboons at 3 T. Methods. 2010;50:147156. 24. American College of Radiology (ACR), Society for Pediatric Radiology (SPR). ACR-SPR practice guideline for the safe and optimal performance of fetal magnetic resonance imaging (MRI). [online publication]. Reston (VA): American College of Radiology (ACR); 2010. 10 p. 25. Prayer D, Brugger PC, Prayer L. Fetal MRI: techniques and protocols. Pediatr Radiol. 2004;34:685693. 26. Nuclear Magnetic Resonance. IMAIOS. 2009. http://www.imaios. com/en/e-Courses/e-MRI/NMR.); 2012 Accessed 20.12.12.

E M I N A R S I N

E R I N A T O L O G Y

37 (2013) 334339

339

27. Vimercati A, Greco P, Vera L, et al. The diagnostic role of inutero magnetic resonance imaging. J Perinat Med. 1999;27: 303308. 28. Bekkar M, van Vught JM. The role of magnetic resonance imaging in the prenatal diagnosis of fetal anomalies 2001. Eur J Obstet Gynecol Reprod Biol. 2001;96:173178. 29. Malinger G, Ben-Sirer L, Lev D, et al. Fetal brain imaging: a comparison between magnetic resonance imaging and dedicated neurosonography. Ultrasound Obstet Gynecol. 2004;23:333340. 30. Rajeswaren R, Chandrasekharan A, Joseph S, et al. Ultrasound versus MRI in the diagnoses of fetal head and trunk anomalies. J Matern Fetal Neonatal Med. 2009;22:115123. 31. Amini H, Wikstrom J, Ahlstrom H, et al. Second trimester fetal magnetic resonance imaging improves diagnoses of non central nervous system anomalies. Acta Obstet Gynecol Scand. 2011;90:380389. 32. Kul S, Kormaz H, Cansu A, et al. Contribution of MRI to ultrasound in the diagnosis of fetal anomalies. J Magn Reson Imaging. 2012;35:882890. 33. Grifths PD, Reeves MJ, Morris JE, et al. A prospective study of fetuses with isolated ventriculomegaly investigated by antenatal sonography and in utero MR imaging. AJNR Am J Neuroradiol. 2010;1:106111. 34. Morris JE, Rickard S, Paley MN, et al. The value of in-utero magnetic resonance imaging in ultrasound diagnosed foetal isolated cerebral ventriculomegaly. Clin Radiol. 2007;62:140144. 35. Solomon L, Ouahba J, Delezoide A-L, et al. Third-trimester fetal MRI and isolated 10-12 mm ventriculomegaly: is it worth it. BJOG. 2006;113:942947.

36. Levine D. Ultrasound versus magnetic resonance imaging. Top Magn Reson Imaging. 2001;12:2538. 37. Poutamo J, Vanninen R, Partanen K, et al. Magnetic resonance imaging supplements ultrasonographic imaging of the posterior fossa, pharynx and neck in malformed fetuses. Ultrasound Obstet Gynecol. 1999;13:327334. 38. Sepulveda W, Ximenes R, Wong AE, et al. Fetal magnetic resonance imaging and 3-dimensional ultrasound in clinical practice: applications and prenatal diagnoses. Best Pract Res Clin Obstet Gynecol. 2012;26:593624. 39. Bulas D, Egloff AM. Fetal chest ultrasound and magnetic resonance imaging: recent advances in current clinical applications. Radiol Clin North Am. 2011;49:805823. 40. Levine D, Barnewolt CE, Mehta TS, et al. Fetal thoracic abnormalities: MR imaging. Radiology. 2003;228:379388. 41. Hubbard AM, Crumbleholme TM, Adzick NS, et al. Prenatal MRI evaluation of congenital diaphragmatic hernia. Am J Perinatol. 1999;16:407413. 42. Rubesova E. Fetal bowel abnormalities US and MRI assessment. Pediatr Radiol. 2012;42(suppl 1):S101S106. 43. Barkovich J, Girard N. Fetal brain infections. Childs Nerv Syst. 2003;19:501507. 44. Benoist G, Solomon LJ, Mohlo M, et al. Cytomegalovirusrelated fetal brain lesions: comparison between targeted ultrasound examination and magnetic resonance imaging. Ultrasound Obstet Gynecol. 2008;32:900905. 45. Twickler DM, Magee KP, Caire J, et al. Second-opinion magnetic resonance imaging for suspected fetal central nervous system fetal anomalies. Am J Obstet Gynecol. 2003;188:492496.