MRI of Fetal and Maternal Diseases in Pregnancy 1st ed.

3. Fetal MR Imaging: Protocols and Anatomy

George Koberlein Keyanoosh Hosseinzadeh  and Evelyn Y. Anthony 

(1)

Department of Radiology, Wake Forest Baptist Medical Center, Medical Center Boulevard, Winston-Salem, NC 27157-1021, USA

George Koberlein

Email: gkoberle@wakehealth.edu

Keyanoosh Hosseinzadeh (Corresponding author)

Email: khossen@wakehealth.edu

Evelyn Y. Anthony

Email: eanthony@wakehealth.edu

Keywords

Fetal MRI protocolFetal MRI sequencesFetal MRI anatomyFetal neurodevelopmentFetal MRI indications

3.1 Introduction

Magnetic resonance imaging (MRI) of the fetus was first described in Lancet in 1983 and was used to evaluate the first trimester fetus [1]. Thus, fetal imaging by means of magnetic resonance imaging has been performed for over 30 years, without known adverse side effect on the developing fetus [23]. Early attempts at fetal imaging were hindered by long scanning times and excessive fetal motion. Concern regarding potential heat absorption, sound effects, and possible teratogenesis also hindered early studies. Over the years, improvements in image quality, scan speed, and study interpretation have advanced the field. The basic sequences used in fetal imaging have adapted and improved concurrently. Today, fetal MRI is now a common practice in obstetrical imaging.

With improvements in the hardware, software, and sequence acquisition, one imaging sequence (ultrafast T2-weighted sequences) emerged as the workhorse in fetal imaging. This base sequence is an ultrafast T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE), with variants known as single-shot fast spin echo (SSFSE) or half-Fourier acquisition single-shot turbo spin echo (HASTE), which provide rapid acquisition with high contrast resolution [4].

Gradient echo T1-weighted sequences and balanced steady-state free precession (SSFP) sequences are also traditionally acquired, with additional sequences added on a case-by-case basis [5].

3.2 Protocols

3.2.1 When To Image

To date, no deleterious effects of MRI on a developing fetus have been proven. The greatest theoretical risk on the developing fetus would be during organogenesis in the first trimester [6]. Because of this theoretical risk to the fetus, the small size of the developing fetus and current available imaging techniques, the risks, and benefits must be carefully considered prior to performing fetal MRI in the first trimester. Safe MRI practice typically allows MRI during pregnancy at any stage if the risk-to-benefit ratio warrants the study or if the data needed will affect the care of the patient or fetus during the pregnancy. Nevertheless, most institutions and practices image after 18 weeks gestation [79]. Written informed consent is usually acquired from the pregnant woman before initiation of the examination.

Prior to performing a fetal MRI study, patients have had an ultrasound (US) in the first trimester to date the pregnancy, commonly referred to as a level I examination. First trimester dating provides the most accurate estimate of fetal gestational age, which is important when assessing fetal anatomy and biometric data later in pregnancy. A level II US is typically performed between 18 and 22 weeks gestation to assess fetal anatomy. If a level II US raises concern for fetal abnormality, especially if the cause is indeterminate or the issue is associated with other significant anomalies, then a fetal MRI may be obtained. Fetal MRI is particularly useful in the setting of oligohydramnios, which can limit the diagnostic sensitivity of US. (Fig. 3.1) Fetal MRI prior to 20 weeks is uncommon, given the timing of the sonographic anatomic survey. Furthermore, the fetal anatomy is small, and a large majority of fetal landmarks that have been described by ultrasound and MRI are not present. It should be noted that current neural biometric data is only available beginning at 20 weeks gestational age, with the majority of data focused on the fetus beyond 24 weeks gestational age [10].

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Fig. 3.1

Coronal (a) and sagittal (b) SSFSE of the gravid uterus characterized by oligohydramnios. Images demonstrate reasonable resolution of the fetal brain despite the lack of amniotic fluid, which is a significant limitation for fetal ultrasound

Fetal MRI should be considered a study performed with the precise aim of clarifying a diagnostic doubt or query, not as a screening tool [11]. A sonographic anatomic survey should address the clinical questions via a tailored examination. Moreover, review of a fetal MRI should be performed in conjunction with the level II US with fetal MRI considered a level III technique.

3.2.2 MRI System

Current recommendations are for the use of a 1.5-T field strength for fetal imaging. An adequate signal-to-noise ratio (SNR) will be obtained at this field strength [11].

Lower field strengths will suffer from image noise, whereas, higher field strengths are still being validated. The coils chosen for fetal MRI can vary based on maternal size or fetal gestational age. Multichannel phased array or cardiac surface coils should grant the best signal, and the coils should be as close to the region of interest as possible. Spine coils may be needed to allow a greater field of view later in pregnancy.

Each MRI vendor will have proprietary names for specific sequences that are useful in fetal MRI. Commonly used sequences with vendor names are listed in Table 3.1.

Table 3.1

Commonly used MRI sequences used in fetal magnetic resonance imaging by vendor

 

GE

Siemens

Phillips

Toshiba

Hitachi

Sequence type

Spin echo

SE

SE

SE

SE

SE

Gradient echo

GRE

GRE

Fast field echo

GE

Field echo

Spoiled Gradient echo

SPGR

FLASH

T1 FFE

Fast FE

SARGE

Coherent Gradient echo

GRASS

FISP

FFE

Rephased SARGE

SSFP

Stead-state Free precession

SSFP

PSIF

T2 FFe

Time-reverse SARGE

 

TrueFISP

FIESTA

TrueFISP

Balanced FFE

Balanced SARGE

True SSFP

TrueFISP/dual excitation

FIESTA-C

CISS

 

Phase-balanced SARGE

 

Multi-echo data image Combination

MERGE

MEDIC

M-FFE

   

Ultrafast gradient echo

Fast SPGR

TurboFLASH

TFE

Fast FE

RGE

Ultrafast gradient echo 3D

3D fast SPGR

MPRAGE

3D TFE

3D fast FE

MPRAGE

Volume-interpolated GRE

LAVA-XV

VIBE

THRIVE

 

TIGRE

Body diffusion

 

REVEAL

DWIBS

 

Body Vision

Susceptibility-weighted imaging

SWAN

SWI

(Venous BOLD)

   

Inversion recovery

IR, MPRI, FastIR

IR, Turbo IR

IR-TSE

IR

IR

Short tau IR

STIR

STIR

STIR

Fast STIR

STIR

Long tau IR

FLAIR

Turbo Dark Fluid

FLAIR

Fast FLAIR

FLAIR

Turbo spin echo/fast spin Echo

FSE

TSE

TSE

FSE

FSE

Single-shot TSE/FSE

SSFSE

HASTE

SSTSE

FASE

SSFSE

3D TSE with variable flip angle

CUBE

SPACE

VISTA

   

Echoplanar imaging

EPI

EPI

EPI

EPI

EPI

Diffusion-weighted imaging

DWI

DWI

DWI

DWI

DWI

Apparent diffusion coefficient map

ADC

ADC

ADC

ADC

ADC map

Turbo gradient spin echo

 

TurboGSE

GRASE

Hybrid EPI

 

Adapted from Siemens at: http://www.healthcare.siemens.com/siemens_hwem-hwem_ssxa_websites-contextroot/wcm/idc/groups/public/@global/@imaging/@mri/documents/download/mdaw/mtmw/~edisp/mri_acronyms-00016934.pdf

3.2.3 Protocol

The basic sequences for performing fetal MRI are available on any vendor platform. Table 3.2 is a typical starting protocol that we use at our institution. The number of series obtained for any given sequence will vary on a case-by-case basis, as fetal motion often necessitates repeating sequences until the images are adequate. Moreover, fetal MRI protocols are often adapted during the examination depending on the clinical question. Most studies are performed in the early morning, following an overnight fast or a fasting period of at least 4–6 h, to limit postprandial motion. In addition to maternal fasting, most institutions stop maternal ingestion of prenatal vitamins for at least 1 day prior to the study, since prenatal vitamins are high in iron, which may cause localized field inhomogeneities during the time of the study. Finally, the mother should empty her bladder just prior to the start of imaging.

Table 3.2

Basic fetal MRI protocol used at our institution (protocol based on a 1.5-T GE magnet)

 

FOV (MM)

Thickness/gap (mm)

Matrix

TR (ms)

TE (ms)

Flip angle (degrees)

Number of slices

Time (s)

NSA

3-plane SSFSE survey

480

10/10

256/179

1200

94

150

24

20

1

Fetal SSFSE neural and body

360

3–4/0–4

256/179

1200

94–120

150

22

20

1

FIESTA

280

3.5/0

256/230

3.97

1.99

70

18

19

2

Fetal SSFSE neural and body

260

3/0

256/179

1200

90

150

45

56

1

Fetal neural DWI/ADC

230

5/0

192/100

6300

89

90

20

96

3

Fetal neural and body SPGR ± fat suppression

280

4–5/0.5

256/192

175

2.84

70

20

20

1

Appropriate patient positioning cannot be overstated. The mother needs to be in a position of comfort so as to limit any maternal motion. Typically, the patient is placed supine or in a left lateral position. Supine positioning may be uncomfortable in late pregnancy, as the size of the uterus may cause vena cava compression or compression of maternal organs.

Initial imaging is performed with a fast localizer sequence, typically a large field ultrafast T2-weighted single-shot sequence, in the maternal coronal, axial, and sagittal planes. These images are used to determine the placental and fetal positioning with respect to the mother. The fetus is more often than not positioned in an oblique axis to the standard maternal axis. Once fetal lie is determined, the images obtained from the localizer sequences are used as scout images for the subsequent sequences. Each additional series also serves as a scout for localization to adjust for fetal repositioning.

Just as plane selection must be made for the fetus relative to scout images of the maternal pelvis, so must plane selection of the fetus be adjusted for each fetal body region. In other words, true anatomic planes can vary by body region when the fetus is curled (Fig. 3.2). For example, the axial plane of the calvarium typically is not in the same axial plane as the fetal chest and abdomen. Thus, constant attention to image acquisition by the technologist is paramount.

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Fig. 3.2

Axial SSFSE image through the maternal pelvis shows the variability of fetal positioning. This image provides a near-coronal image through the fetal brain and an axial image of the fetal abdomen. Attention to acquisition planes is critical to confirm landmarks and normal organ configurations

To obtain high-resolution images, the field of view should be as small as possible without causing aliasing artifact. Slice thickness may be adjusted as needed to image the system or organ of interest, with an optimal range of 3–4 mm to achieve high SNR and through-plane resolution [1213]. Decreasing matrix size is another parameter influencing SNR, with smaller matrix sizes providing increased signal.

The trade-off with smaller matrix sizes is decreased in-plane resolution. Breath holding can reduce motion-related artifact, although the ultrafast sequences do allow for free-breathing acquisition [13]. Parallel imaging can be used to improve temporal resolution as long as care is exercised with selecting the field of view and with addressing SNR challenges [14]. All parameters should be chosen to keep scan time to a minimum.

3.3 Sequences and Artifacts

3.3.1 T2-Weighted Imaging

The ultrafast T2-weighted sequence is the recognized workhorse in fetal MRI [13], allowing excellent visualization of the fetal anatomy, especially cerebral anatomy. T2-weighted imaging allows optimization of tissue contrast in the fetus, due to the large volume of water in the fetus and adjacent amniotic cavity. Anatomic detail of the fetal brain, fluid-filled cavities, lungs, placenta, and fetal profile is consistently strong [15]. SSFSE allows image acquisition during a single TR interval with a total acquisition time of less than 2 s per image [16]. Images should be acquired with a 1–2 s time delay between each image to prevent saturation effects that will degrade the signal-to-noise ratio (SNR). Alternatively, the slices can be acquired in an interleaved fashion with a gap equal to the slice thickness to minimize the potential signal loss from bulk-fluid motion artifacts and cross talk. In neuroimaging, longer TEs allow better discrimination of the grey-white matter interface in the fetus since the T2 contrast increases with increasing TE times [17].

3.3.2 Steady-State Free Precession

Fast imaging with balanced steady-state free precession (SSFP) provides images with T2/T1 contrast weighting with high temporal resolution [1821]. These sequences are especially useful in demonstrating vasculature and fluid-filled cavities, specifically those surrounded by dense tissues, and these sequences can be used to visualize the fetal heart chambers [15]. Evaluation of the umbilical cord and its insertion may also be enhanced with this sequence.

SSFP sequences are obtained in a wide field of view, allowing visualization of the maternal abdominal anatomy and the uterus/placenta. Large field of view imaging limits usefulness of SSFP sequences in fetal brain imaging in early gestation [15].

SSFP provides similar image quality to SSFSE for brain imaging in the second trimester; however, axonal migration in the third trimester is best depicted with SSFSE [19]. SSFP is inferior to SSFSE in assessing the fetal lungs prior to 25 weeks gestational age since the lungs demonstrate hyperintense signal only in advanced gestation.

3.3.3 T1-Weighted Imaging

T1-weighted images are acquired using a gradient-echo sequence with breath-hold fast spoiled gradient-echo sequences used most commonly [15]. T1-weighted sequences provide little information over SSFSE sequences but can increase sensitivity for detection of fat, calcification, hemorrhage, or proteinaceous structures. Fat-suppressed T1-weighted images increase the dynamic range of fetal MRI and allow more specific detection of fat and hemorrhage [22].

T1-weighted imaging has proven beneficial when evaluating certain normal structures as well as a few common pathologies. The pituitary and thyroid glands can be seen at 20 weeks [15]. The liver is distinguished by its hyperintense T1 signal due to its high iron affinity, a fact exploited in evaluation for congenital diaphragmatic hernias or abdominal wall defects with displaced liver [2324].

Furthermore, the hyperintense T1-weighted appearance of meconium is essential to fetal abdominal imaging, both for position and caliber of the colon and for correlation with expected gestational age [2526]. T1-weighted imaging will highlight accumulating fetal adipose tissue as well.

3.3.4 DWI/DTI

Diffusion imaging is challenging in fetal MRI. Nevertheless, one important use is its sensitivity for detecting ischemic lesions, brain lesions, and regions of placental infarction [2728]. Certain diffusion sequences have been used to visualize the maturational processes of the cerebral cortex and premyelinating white matter, but this technique in fetal MRI is still in research [2932]. Diffusion anisotropy of the white matter tracts increases constantly from premyelinating to myelinating stages, revealing maturing white matter tracts before there are visualized changes on T1- and T2-weighted images [1332].

3.3.5 Advanced Imaging Techniques

Spectroscopy in fetal MRI has been applied to the older fetus whose head is relatively nonmobile within the maternal pelvis [3334]. Inversion recovery sequences may be used to obtain additional information involving the fetal brain, but these are sensitive to hemorrhage [15]. Dynamic fetal imaging allows assessment of fetal swallowing, palatal defects, diaphragm motion, peristalsis, and gross fetal motion [35].

Finally, echoplanar imaging may be considered on occasion. The speed at which echoplanar imaging (EPI) is acquired allows it to overcome typical motion artifacts seen in conventional MRI [36]. EPI has been used to produce ungated fetal cardiac movies, for volumetric measurements and for evaluating hepatic hematopoiesis [3739]. EPI is unique in depicting the fetal skeleton and cartilaginous epiphysis in the fetus before 27 weeks gestation [15]. The magnetic susceptibility of EPI makes it valuable in detecting hemosiderin and certain placental pathologies [15].

The use of 3 T field strength to perform fetal MRI is currently under investigation. The most important advantage to 3 T imaging would be the gain in SNR, which is especially important in small part imaging [40]. On the other hand, 3 T field strength exaggerates artifacts, such as large field inhomogeneity, magnetic susceptibility, and chemical shift artifacts [40]. Lastly, fetal safety at 3 T, including static field exposure, gradient field switching, and radiofrequency power deposition, is a topic of research [40].

3.3.6 Gadolinium-Based Contrast Agents

Routine use of gadolinium-based contrast agents is not a standard of care, since their biosafety in pregnancy has not been established [41]. Gadolinium-chelate agents cross the placenta, are filtered by the kidneys, are excreted into the amniotic fluid, and are resorbed by the fetus through the swallowing of amniotic fluid. With the cycle of excretion and reabsorption through swallowing, the biological half-life of gadolinium in the fetus is not known [41]. With the accumulation of gadolinium-chelate agents in the amniotic fluid, there is potential for dissociation of the toxic-free gadolinium ion, which poses a risk for the development of nephrogenic systemic fibrosis (NSF) in the mother or child. If gadolinium-based contrast agent is deemed necessary in a pregnant patient, then the agents with the lowest risk for development of NSF should be used at the lowest dose that allows for diagnosis.

3.3.7 Common Artifacts

Fetal MRI struggles with artifacts as seen with MRI in other body regions. Motion artifacts, susceptibility, aliasing, partial volume averaging, and Gibbs artifacts are issues at times. Artifact from bulk fluid motion can complicate SSFSE sequence when excited spins in fluid change position with respect to slice and/or spatial encoding gradients before the signal is acquired (Fig. 3.3). If all of the excited fluid remains stationary from excitation to the time of signal acquisition, then the fluid signal will be uniformly hyperintense. Alternatively, if all or a partial volume of the excited fluid moves out of the imaging plane by the time of image acquisition, then the fluid will become hypointense. As long as the fetus is not moving continuously, only one or two adjacent slices should be degraded during a typical SSFSE acquisition.

A330004_1_En_3_Fig3_HTML.gif

Fig. 3.3

Large field of view SSFSE image of the gravid uterus with sagittal acquisition through the fetus nicely demonstrates linear bands of dark signal (arrow) associated with bulk fluid motion from fetal shifting during image acquisition

3.4 Fetal Anatomy

Interpretation of fetal MRI requires knowledge of normal anatomy during the course of gestation, including size, configuration, position and signal changes in each organ.

The vast majority of questions brought to fetal MRI concern the central nervous system (CNS) and CNS pathology, so issues of cleavage and migration of neuronal structures are as important as gross insults of infarction or hemorrhage. In body imaging, many questions pertain to prognosis and to plans for delivery. We will review an overall approach.

3.4.1 Preparation

Fetal MRI interpretation requires correlation with available US images and/or report. The US provides a road map for tailoring the subsequent MRI examination; valuable time in the scanner should focus on specific clinical questions and on anatomy not cleared by US. Also, the US evaluates structures that are often incompletely imaged during the fetal MRI, such as the extremities or digits.

3.4.2 Situs

Determining fetal situs may not be intuitive. Confirming situs solitus eliminates numerous pathologies and allows lateralization of asymmetric findings. To determine situs, one must orient the fetus relative to the maternal axis (Fig. 3.4). In relation to the maternal long axis, the fetus can thus be vertex (head directed toward the maternal pelvis) or breech (head directed toward maternal head). If the fetus is breech, then the fetal spine is down, and the fetal abdomen is up on the image, making the fetal lie similar to that of the mother. If the fetus is vertex, the fetal spine is down, and the fetal abdomen is up on the image, creating an opposite viewing orientation of fetal and maternal anatomy. Fetal situs can subsequently be determined for any rotation about the fetal axis with regard to breech or vertex positioning.

A330004_1_En_3_Fig4_HTML.gif

Fig. 3.4

Coronal (a) and axial (b) SSFSE images through the gravid uterus with twin gestation highlight the complexity of determining fetal situs and lateralization of abnormalities. Both fetuses have left side down with respect to the mother, but fetus (a) is vertex and fetus (b) is breech. The most helpful fetal organ for lateralization is the fetal stomach (not shown), except in the case of congenital diaphragmatic hernia.

US can suggest situs ambiguity, but it may not completely describe all the anomalies that can accompany these syndromes. Furthermore, US may miss a situs abnormality, which may inadvertently be discovered on MRI by virtue of the large field of view imaging [42]. Recent work has shown that fetal MRI can demonstrate situs anomalies at least similarly to US as well as associated malformations that provide important information regarding perinatal management [42].

3.4.3 Intracranial Anatomy

The entirety of fetal embryology and neuroanatomy is beyond the scope of this chapter. Dedicated textbooks explore the magnitude of the topic, and several references on brain development are available [4351]. We will highlight key landmarks and developmental milestones in the fetal brain.

Fetal MRI is commonly used to investigate underlying etiology for ventriculomegaly and morphologic brain abnormalities that are incompletely assessed with US. The brain evolves throughout gestation, making evaluation challenging to those unaware of the normal appearance of the anatomy at a specific gestational age [6].

Beginning in the early second trimester, structures that arise from the telencephalon, mesencephalon, and rhombencephalon become visible with the gyral and sulcal pattern developing in a predictable sequence [52].

The early fetal brain is composed predominately of large ventricles with a thin layer of cerebral tissue having a smooth appearance [6]. The choroid plexus, seen as an echogenic structure filling the lateral ventricles on US, is difficult to visualize early in gestation by MRI [6]. At 14 weeks, the interhemispheric fissure separating the cerebral hemispheres is well developed [6]. At approximately 16 weeks, the Sylvian fissure begins to appear, but the cortex does not undergo infolding and opercular formation before 34 weeks gestation. Normal cortical maturation, while predictable and easily visualized on fetal MRI, often lags behind the maturation described in neuroanatomic specimens [64348]. Table 3.3 provides a list of the commonly seen and evaluated sulcal developmental landmarks, their neuropathologic appearance, and the gestational week of detectability at MRI [4353]. Note that the neuroanatomic information provided in the tables describes the gestational ages at which 25–50 % of the brains demonstrate a specific cortical landmark [654]. On a midsagittal plane, the cingular sulcus appears at 24 weeks gestation, the marginal at 27 weeks gestation, the parieto-occipital at 22 weeks gestation, and the calcarine at 24 weeks gestation. On a lateral sagittal plane, the central sulcus appears at 27 weeks gestation, the postcentral at 28 weeks gestation, and the precentral sulcus at 27 weeks gestation. On an anterior coronal plane, the superior frontal sulcus and the inferior frontal sulcus appear at the 29th week of gestation. On a coronal plane at the level of the third ventricle, the superior and inferior temporal sulci appear at 27 and 33 weeks, respectively. Sulcation continues throughout fetal life, with secondary sulci becoming evident at 32–35 weeks and tertiary sulci subsequently forming [6] (Fig. 3.5). If CNS imaging is necessary in early pregnancy, recent work is available to assess biometric data below 24 gestational weeks [55].

Table 3.3

Fetal sulcation observed on MRIa

Gestational age (week)

   

Present in more than 75 % of

Neuropathologic

appearanceb

brains in present MR study

Sulci of the vertex

Central sulcus

20

27

Precentral sulcus

24

27

Postcentral sulcus

25

28

Sulci of the medial cerebral surface

Interhemispheric fissure

10

22–23

Callosal sulcus

14

22–23

Parieto-occipital fissure

16

22–23

Cingular sulcus

18

24–25

Secondary singular sulci

32

33

Marginal sulcus

 

27

Calcarine fissure

16

24–25

Secondary occipital sulci

34

34

Sulci of the ventral cerebral surface

Hippocampic fissure

 

22–23

Collateral sulcus

23

27

Occipitotemporal sulcus

30

33

Sulci of the lateral cerebral surface

Superior frontal sulcus

25

29

Inferior frontal sulcus

28

29

Superior temporal sulcus (posterior part)

23

27

Superior temporal sulcus (anterior part)

 

32

Inferior temporal sulcus

30

33

Intraparietal sulcus

26

28

Insular sulcus

34–35

34

aAccording to Garel et al. [40]

bAccording to Chi et al. [42]

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Fig. 3.5

Coronal SSFP (a) and axial (b) SSFSE images through the fetal brain in two different patients compare the sulcation pattern at different gestational ages. (a) shows the smooth cortex and early Sylvian fissure (arrowheads) formation at 24 weeks gestation. (b) highlights the complex cortical folding pattern in a near-term fetus

In addition to parenchymal folding, the size and morphology of certain parenchymal structures should be assessed. Tables 3.43.53.63.7, and 3.8 and the associated figures can be used as a reference regarding size and location of measurement. Garel et al. provide reference data regarding additional parenchymal size landmarks [44]. Concomitant with sulcation and gyration, neural migration is occurring. At approximately 5 weeks post conception, the forebrain consists of two layers: a deep neuroepithelial layer (ventricular zone or germinal matrix) and a superficial layer (the preplate) [56]. Through complex radial migration, various layers of neural tissue are added to the developing parenchyma. The migration will give the appearance of distinct bands in the forebrain depending on the imaging time. For example, a multilayered appearance of the forebrain is typical between 23 and 28 gestational weeks [5657]. The following five distinct layers during these gestational weeks can be identified (from outside in): cortical plate, subplate zone, subventricular and intermediate zones, periventricular fiber-rich zone, and ventricular zone [57]. As neuronal migration begins, the germinal ventricular zone gradually regresses. By 29 weeks gestation, migration to the developing cortex is almost complete, and the ventricular zone disappears, resulting in the differentiation of only two layers: the cortex and the white matter. Persistent visualization of a multilayered appearance of the forebrain after 29 weeks signifies a migrational abnormality.

Table 3.4

Fronto-occipital diameter (mm)A330004_1_En_3_Figa_HTML.gif

WG

Average

SD

22–23

67.5

3.1

24–25

69.7

8.12

26

76.8

7.91

27

81.3

4.68

28

81.5

4.15

29

85.3

5.84

30

89.2

5.94

31

91

3.85

32

93.4

5.43

33

97

4.48

34

99

5.28

35–36

102.2

3.92

37–38

103

5.78

Adapted from Garel [44]

Table 3.5

Length (mm) of the corpus callosumA330004_1_En_3_Figb_HTML.gif

WG

Average

SD

22–23

30.12

1.84

24–25

30.96

3.3

26

33.4

2.6

27

35.06

4.34

28

36.2

2.57

29

35.62

3.55

30

37.06

3.05

31

37.51

3.1

32

38.63

3.6

33

40.97

3.37

34

38.89

3.09

35–36

40.9

3.54

37–38

43.12

5.87

Adapted from Garel [44]

Table 3.6

Transverse cerebellar diameter (mm)A330004_1_En_3_Figc_HTML.gif

WG

Average

SD

22–23

25.9

3.09

24–25

26.7

1.86

26

28.7

4.27

27

32.1

3.11

28

32.4

1.96

29

35.4

2.59

30

36.6

3.25

31

38.9

2.04

32

39.9

2.27

33

41.6

2.22

34

43.4

3.29

35–36

46.6

2.36

37–38

48

3.77

Adapted from Garel [44]

Table 3.7

Anteroposterior diameter (mm) of the vermisA330004_1_En_3_Figd_HTML.gif

WG

Average

SD

22–23

8.5

0.76

24–25

8.6

1.67

26

9.37

0.47

27

10.46

2.29

28

9.85

0.67

29

10.6

1.23

30

11.81

1.99

31

12.23

1.53

32

12.99

2.22

33

13.74

2.29

34

14.95

2.41

35–36

14.8

1.95

37–38

15.28

2.66

Adapted from Garel [44]

Table 3.8

Height (mm) of the vermisA330004_1_En_3_Fige_HTML.gif

WG

Average

SD

22–23

11.15

1

24–25

12.8

2.12

26

14

0.81

27

15.2

2.24

28

15.4

1.91

29

16

1.07

30

17.1

2.14

31

17.1

1.37

32

18.3

2.01

33

19.2

1.78

34

20.1

2.15

35–36

20.9

1.83

37–38

21.1

2.79

Adapted from Garel [44]

Evaluation of the cerebral ventricles should also be performed on every study. Until about 23 weeks gestation, the occipital horns are disproportionately larger than the frontal horns (Fig. 3.6); thereafter, they become smaller [658]. Prominent lateral ventricles in early pregnancy can be misdiagnosed as ventriculomegaly. Sonographic data has translated to MRI, with the standard measurement of the ventricle obtained in an axial plane through the atrium. Normal atrial width detailed by Cardoza et al. is 7.6 ± 0.6 mm, with greater than10 mm defining ventriculomegaly, but a true axial image through the atria is required [59]. Using fetal orbits as a scout landmark can aid in the acquisition of true orthogonal planes through the fetal brain [60]. In addition to the size, the margins of the ventricular walls of the ventricles should be assessed for any contour irregularity or nodularity [56]. The ventricular walls are comprised of the ventricular zone of the germinal matrix, which will appear as a smooth band of T2 dark and T1 bright signal lining the ventricles [5256]. This signal is thicker at younger gestational ages and gradually thins as term approaches [56].

A330004_1_En_3_Fig6_HTML.jpg

Fig. 3.6

Axial SSFP image of the brain in a fetus of 24 weeks gestation shows normal, symmetric fullness of the occipital horns of the lateral ventricles (arrowheads) relative to the frontal horns. This appearance should not be confused for ventriculomegaly

The corpus callosum is the largest commissural connection between the cerebral hemispheres. It develops normally between 8 and 20 weeks gestation and is detected on the midline sagittal T2-weighted image as a C-shaped hypointense structure at the superior margin of the cavum septi pellucidi [656]. The widely accepted theory for the embryogenesis of the corpus callosum suggests that the genu of the corpus callosum develops first, followed by the body and the splenium.

The exception to the orderly anterioposterior callosal development is the rostrum, which forms last, usually by 20 weeks [6162]. The corpus callosum should be uniform in thickness and should increase in length with increasing fetal age [44476162].

The cavum septi pellucidi is an important landmark in fetal neural axis evaluation and visualization of the cavum septi pellucidi by 18–20 weeks gestation reassures proper development of the central forebrain [663]. (Fig. 3.7) Nonvisualization is associated with various forebrain neuroanatomical anomalies including agenesis of the corpus callosum, holoprosencephaly (Fig. 3.8), and schizencephaly [63]. Isolated septal deficiency is a controversial entity that can be considered a normal variant [63] although, in one study, the cavum septi pellucidi was seen in 100 % of normal fetuses between 18 and 37 weeks gestation [64].

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Fig. 3.7

Axial SSFSE image through the brain of a fetus of 24 weeks gestation was performed after a level II ultrasound raised concern for holoprosencephaly. This image confirms the presence of the cavum septi pellucidi and cavum vergae (arrow), which is absent with midline cleavage anomalies

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Fig. 3.8

Coronal oblique SSFP image of the brain in a fetus of 31 weeks gestation confirms US suspicion of holoprosencephaly with large monoventricle (arrowheads) instead of separate lateral ventricles

The posterior fossa structures also undergo a predictable series of changes throughout development. Similar to forebrain development, the cerebellum arises from the neuroepithelial cells in the ventricular zone with a sparsely cellular superficial marginal layer [56]. The cerebellar hemispheres can have a multilayered appearance as early as 21 weeks, with hemisphere growth throughout gestation [6566]. The cerebellar vermis covers the fourth ventricle by 20 weeks gestation [65], but early in development there is incomplete formation of the vermis, which should not be misdiagnosed as vermian defects or hypoplasia before 20 weeks gestation [6]. Position of the tentorium cerebelli and morphology of the cerebellar vermis are best assessed on direct midline sagittal images and the cerebellar hemispheres on axial and coronal planes. AJ Robinson et al. provide normative values regarding cerebellar size and vermian development on fetal MRI with detailed description of the embryological development [67]. Brain stem morphology is best depicted on midline sagittal plane images with particular attention to the anterior pontine convexity, size of the cisterna magna, location of the cerebellar tonsils, and midbrain structures.

3.4.4 Spine

MRI evaluation of the spinal column allows evaluation for pathologies such as neural tube defects, caudal regression, and spinal tumors (Fig. 3.9). Myelomeningocele is the most common severe defect of the spine that can easily be visualized and characterized on MRI. In fact, MRI adds information where US is limited, particularly in the setting of posterior spinal positioning in utero, of oligohydramnios, and of maternal obesity [68]. Fetal MRI may also provide better characterization of the internal (intrapelvic/intra-abdominal) component of sacrococcygeal teratomas [68].

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Fig. 3.9

Sagittal SSFSE image through the body of a third trimester fetus (a) highlights several features of a normal spine, including normal alignment, intact soft tissues posteriorly (black arrowheads), and appropriate termination of the conus (white arrowhead). In contrast, sagittal SSFSE image through the body of a 26-week gestation fetus with caudal regression syndrome (b) shows marked lumbosacral kyphosis (white arrow) and open neural tube defect (black arrowheads)

Sagittal and axial imaging through the spinal column offers key images. Multiple series may be required given the inherent normal spinal curvature. Any fixed or unexpected curvature should prompt a search for associated abnormalities, such as those seen in VACTERL (vertebral anomalies, anal atresia, cardiac defects, tracheoesophageal fistula and/or esophageal atresia, renal and radial anomalies, and limb defects) and caudal regression syndrome.

Localization of the conus via MRI is usually straightforward. Postmortem MRI has reported that the conus is positioned between the L2 and L5 levels before the 35th gestational week and between the L1 and L3 levels after the 35th gestational week [69]. Recent work using SSFP sequences shows the mean conus position at L4 between the 21st and 25th gestational weeks, at L3/L4 between the 26th and 30th weeks, at L2/L3 level in fetuses between the 31st and 35th weeks, and at the L2 level in fetuses beyond the 36th gestational week [70].

3.4.5 Head and Neck

Fetal MRI is useful in evaluating normal facial structures and in defining the extent of head and neck masses. Facial structural evaluation includes the orbits for hyper- or hypotelorism (Fig. 3.10), the lip and palate for cleft (Fig. 3.11), the profile for nasal bridge and micrognathia/retrognathia (Fig. 3.12), and the ears for presence and positioning. Normative values for the interocular distance and for chin size are published [4471]. The presence of any mass will lead to discussions of prognosis and prompts plan for therapy, including delivery options. For example, the question of possible airway compromise may require ex utero intrapartum treatment (EXIT) procedure and the presence of a pediatric surgeon at delivery [68]. Pharyngeal and neck masses may also cause impairment of the swallowing mechanism, with secondary polyhydramnios. Cine imaging in the sagittal plane can assess the swallowing function of the fetus. If T1-weighted imaging is performed, the thyroid should be identified.

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Fig. 3.10

Axial SSFP images through the globes compare a fetus with normal interocular distance (a) and one with hypotelorism (b). This determination is often evident qualitatively, but published charts of normal interocular distances are available and particularly useful when assessing for certain suspected syndromes

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Fig. 3.11

Coronal SSFP image through the face in a third trimester fetus confirms an intact upper lip (arrowheads) and normal nasal configuration

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Fig. 3.12

Sagittal SSFSE through the head and body of a fetus at 36 weeks gestation shows micrognathia (arrow), which alters the shape of the lips (arrowheads) and displaces the tongue (star) posteriorly to narrow the hypopharynx. Cine images can be useful in this condition to evaluate swallowing

The airway should be screened for patency on at least one sagittal or coronal series, where it appears as a fluid-filled structure on T2-weighted images bifurcating at the level of the carina (Fig. 3.13). Patency in the setting of masses that cause extrinsic airway compression is vital information when determining possible postnatal need for emergent. Any compression of the oropharynx or nasopharynx should be documented.

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Fig. 3.13

Coronal oblique SSFP image of a 27-week gestation fetus with a large lymphangioma of the left neck (arrows), extending into the mediastinum and axilla, was performed to assess for airway compromise. This image shows normal fluid in the thoracic trachea and main stem bronchi (arrowheads) although the mass abuts the trachea at the thoracic inlet

3.4.6 Thorax

Evaluation of the fetal thorax is important when considering common pediatric pathologies such as congenital diaphragmatic hernia (CDH), the range of parenchymal lung lesions, and rare airway anomalies (Fig. 3.14). Studies have demonstrated the superior ability of MRI to differentiate congenital pulmonary airway malformation, bronchopulmonary sequestration, and CDH, a vital step in treatment planning [2472]. When one of these pathologies is suspected, careful evaluation of the lesion location, size, and any associated mass effect should be documented.

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Fig. 3.14

Coronal SSFSE images through the chest in three different early third trimester fetuses compare normal lung signal (a), compressed lung in fetus with congenital diaphragmatic hernia (CDH) (b), and abnormal lung in fetus with congenital lobar emphysema (CLE) (c), confirmed after delivery. In normal third trimester lungs (a), the signal is moderately hyperintense on fluid-sensitive sequences (arrowheads) as the lungs contain amniotic fluid. In the setting of CDH (b), ipsilateral lung is often completely compressed and indistinguishable from bowel and abdominal organs in the chest; contralateral lung may remain of moderately high signal (arrowheads) depending on degree of compression. Congenital lung masses such as CLE (c), bronchopulmonary sequestration, and congenital pulmonary airway malformation are more intense than normal lung signal (arrows)

Normative values for thoracic size, lung volumes, and mediastinal volumes should be referenced during interpretation of fetal MRI for lung lesions. The prognostic information from this step is significant given the postnatal morbidity and mortality from pulmonary hypoplasia in the setting of fetal lung lesions and/or diaphragmatic hernias [68].

The lungs should be uniform in signal and moderately hyperintense on T2-weighted images from alveolar fluid filling the lungs from the mid-second trimester. Signal heterogeneity or contour irregularity of the lungs should raise concern for a mass. The trachea and bronchi also should be seen as hyperintense tubular structures and may be resolved with appropriate slice thickness and plane selection. The diaphragm is easily visualized on sagittal and coronal images, and its integrity should be confirmed. The normal thymus may be apparent on MRI in the third trimester, where it can be seen as a homogeneous intermediate signal structure in the anterior mediastinum if the TE on the SSFSE sequence is set to an appropriate value to distinguish thymic tissue from the adjacent mediastinal tissues and lung parenchyma.

In spite of advances in MRI techniques, the fetal heart remains incompletely assessed with fetal MRI, and fetal echocardiography remains the modality of choice to exclude cardiac lesions or situs abnormalities. Nevertheless, certain pathologies, including cardiomegaly, anomalous positioning, or even tumors, may be diagnosed on fetal MRI. If fetal MRI is inconclusive regarding the heart, reporting should suggest the complementary nature of a fetal echo for completing diagnosis.

3.4.7 Abdomen

Characterization of a fetal abdominal mass is a typical indication for fetal MRI. Teratomas, neuroblastomas, hepatoblastomas, renal hydronephrosis, or a markedly distended bladder in the setting of posterior urethral valves are a few common pathologies in the fetal abdomen (Fig. 3.15). Familiarity with the normal appearance of the fetal abdomen is the critical starting point in recognizing these abnormalities. Fortunately, at the time of fetal imaging, any physiologic abdominal wall defect should not be present, and the abdominal organs should be in their final locations. Notably, the pancreas and adrenal glands are not resolved due to their small size. The normal fetal liver should be uniformly hypointense on T2-weighted sequences and intermediate to mildly hyperintense on T1-weighted images secondary to high iron content from fetal hemoglobin. The spleen is detectable by 20 weeks gestation, showing homogeneous signal slightly more intense than liver on T2-weighted images that decreases with advancing gestational age [73]. The fetal gallbladder should be visualized by 18 weeks gestational age as a hyperintense T2 structure in the typical location (Fig. 3.16). The biliary system is not visualized under normal conditions. Frequently, the portal and hepatic veins are evident as flow voids on ultrafast T2-weighted sequence and hyperintense structures on SSFP. Fetal circulation includes the ductus venosus, which may be seen.

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Fig. 3.15

Sagittal SSFE in a male fetus of approximately 20 weeks gestation demonstrates a markedly dilated bladder and prostatic urethra (arrow), most consistent with posterior urethral values. Note that amniotic fluid is present around the fetus, so obstruction is not yet complete despite the size of the bladder

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Fig. 3.16

Coronal SSFSE image of a fetus of 28-week gestation demonstrates normal abdominal situs with stomach in the left upper quadrant (star) and gallbladder in the right upper quadrant subhepatic space (arrow)

The kidneys should be assessed for location, axis, and signal, and the renal hilum should be evaluated for hydronephrosis (Fig. 3.17). Similar to obstetrical US studies, US measurements regarding hydronephrosis have translated to fetal MRI, with persistent renal pelvic dilatation above 4 mm in the second trimester and above 7 mm after 32 weeks being abnormal. MRI can demonstrate morphologic abnormalities such as cystic disease of the kidneys, obstructive uropathy, renal tumors, and urinary tract anomalies [74]. The urinary bladder is a fluid-filled structure and can occupy considerable portion of the abdomen in older fetuses (>30 weeks) [75].

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Fig. 3.17

Axial (a), coronal (b), and sagittal (c) SSFSE images through the fetal abdomen for three different patients with gestational ages of 33 weeks (a), 32 weeks (b), and 29 weeks, respectively, demonstrate normal signal, contour, and axis of the kidneys (arrows). Note that normal size is approximately 1 mm per gestational week after 20 weeks

The fetal stomach should be identified as a fluid-filled structure in the left upper quadrant. Nonvisualization of the stomach should raise concern for a possible upper gastrointestinal obstructive process, such as esophageal atresia or esophageal compression. The esophagus may not be visualized unless it is abnormal. Small bowel loops can be seen as tubular hyperintense structures, typically in the left abdomen. The colon has a hypointense T2-weighted and hyperintense T1-weighted appearance due to the presence of meconium (Fig. 3.18). Meconium should be visualized on T1-weighted imaging below the level of the urinary bladder in late gestation on sagittal sequences. Meconium is identified in the rectum typically after 20 weeks gestational age, in the left hemicolon at 24 weeks, and the right hemicolon before 31 weeks, serving as a kind of normal marker for bowel development.

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Fig. 3.18

Coronal VIBE (3D T1-weighted gradient-echo sequence) image of the abdomen in a fetus of 34 weeks gestation provides a nice example of meconium (arrows) in the colon. Meconium is hyperintense on this sequence and should be seen throughout the colon by 31 weeks gestation. Paramagnetic minerals, such as iron, manganese, and magnesium, may be responsible for the high signal since it persists even with fat-suppression techniques

Similarly, the jejunum exhibits high signal on T2-weighted sequences after 30 weeks gestational age related to the antegrade passage of swallowed amniotic fluid, and the distal small bowel becomes progressively less intense thereafter [76]. Bowel diameters increase with advancing gestational age; at 20 weeks gestation, small bowel measures 2–3 mm with large bowel 3–4 mm in diameter, increasing to 5–7 mm and 8–15 mm, respectively, by 35 weeks gestation [77].

The presence of a cystic abdominal or pelvic lesion may also prompt an MRI study. Lesions such as meconium pseudocysts, ovarian masses, mesenteric cysts, and hydrometrocolpos (Fig. 3.19) may be further characterized using MRI, given its superior contrast resolution and anatomic localization [78].

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Fig. 3.19

Coronal oblique SSFSE image of the body of an early third trimester fetus shows findings associated with cloacal anomalies. The bladder (arrow) is small and displaced anteriorly. The rounded, fluid-filled structures centrally (stars) represent dilated, septate vagina. The hydronephrotic left kidney is also in the field of view (arrowheads)

3.4.8 Extremities

The extremities are typically best evaluated with US because of the perpetual movement of the fetus complicating MRI examinations. Prenatal US is currently the method of choice for evaluating the long bones, and standardized measurements at US regarding long-bone development are performed during any fetal anatomic survey. Still, assessment of the extremities should be attempted (Figs. 3.20 and 3.21).

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Fig. 3.20

Sagittal SSFP image of a late second trimester fetus is an example of the detail of the extremities that is sometimes achieved if fetal motion is minimal. This image confirms the presence of five fingers on the left hand (arrows). Note also the normal bladder (star) in the midline of the pelvis

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Fig. 3.21

SSFSE image of the gravid uterus captures a fetal foot in the coronal plane. Five digits (arrow) are confirmed

Recent experience with echoplanar imaging enables the delineation of various epimetaphyseal structures and morphometric measurements of the fetal long bones from 18 weeks gestation until term. This information gathered from fetal MRI may be helpful in the diagnosis of isolated and complex skeletal abnormalities [79].

3.4.9 Umbilical Cord and Placenta

Evaluation of the umbilical cord, amniotic sac, and placenta complete the fetal MRI interpretive survey. Normal insertion and visualization of a three-vessel cord may exclude certain pathologies whereas the presence of a two-vessel cord should heighten awareness for additional fetal abnormalities (Fig. 3.22). The cord is defined by its flow voids on ultrafast T2-weighted sequences while the vessels are hyperintense structures on SSFP sequences. The placenta may change its appearance from a homogeneous intermediate signal intensity structure at 19–23 weeks gestation to a more heterogeneous structure with increased lobule number and T2 signal intensity later in pregnancy [80]. With placental maturation, venous stasis and/or thrombotic changes may cause areas of normal placental infarctions. Attention to placental size and positioning is also important for excluding previa and abnormal placentation.

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Fig. 3.22

SSFP sequences nicely delineate the umbilical cord. Normal cord (a) has three vessels (arrowheads)—two arteries and one larger vein. Two-vessel cord (b) (arrowhead, showing cord in cross section) can be an incidental finding or associated with various syndromes

3.5 Conclusions

MRI allows detailed visualization of the fetus as well as pregnancy structures. The specific imaging protocol used should be selected based on fetal age and suspected pathology, and each examination should be tailored to the question at hand. A systematic approach allows the recognition of developing fetal anatomy and complex lesions. Dynamic changes in fetal anatomy may alter the imaging appearance depending on the time of fetal imaging, particularly involving the intracranial structures. Knowledge of landmarks and typical appearance at any given time point should aid in the interpretation of these complex MRI examinations.

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