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Cortical Maturation in Normal and Abnormal Fetuses as Assessed with Prenatal MR Imaging

¹ Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215 (D.L.)
² Department of Radiology, Children's Hospital, Boston, Mass (P.D.B.).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To establish the appearance of normal fetal cortical development in utero and compare it with the appearance of abnormal cortical development.

MATERIALS AND METHODS: Magnetic resonance (MR) images of the brain in 53 normal and 40 abnormal fetuses at 14–38 weeks gestational age (GA) were reviewed. The GAs at the time of MR imaging visualization of the fissures or sulci were compared with the GA guidelines based on neuroanatomic studies.

RESULTS: In normal fetuses, the sulcation landmarks appeared on MR images in the order predicted by using anatomic studies, with a 0–8-week lag in the MR imaging visualization of the sulci compared with the reported time of visualization of the sulci in anatomic specimens. When landmarks were grouped by range of GAs, the expected MR imaging sulcation landmarks in the group with younger GAs than the actual GA were seen in 50 of 53 (94%) normal fetuses, in five of nine fetuses (56%, P < .05) with isolated mild ventriculomegaly, and in 24 of 31 fetuses (77%, P < .05) with other CNS anomalies.

CONCLUSION: Normal fetal cortical maturation at MR imaging follows a predictable course that is slightly delayed compared with that described in neuroanatomic specimens. This maturation is often further delayed in fetuses with CNS abnormalities.

Index terms: Fetus, abnormalities, 856.8743, 856.87442, 856.8745, 856.8748 • Fetus, central nervous system, 856.8743, 856.87442, 856.8745, 856.8748 • Fetus, MR, 856.121416 • Magnetic resonance (MR), rapid imaging, 856.121416

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Sulcal development is one of the markers of cortical maturation and is used as an indicator of cortical development. The patterns of cortical development in the neonate and in autopsy specimens from fetuses have been described in anatomic (1–4), ultrasonographic (US) (3,5–8), and magnetic resonance (MR) imaging (3,9,10) studies. However, the description of the pattern of development in fetuses in vivo has been limited by the inability to visualize the majority of the fetal cortex.

In a recent study of transvaginal US imaging of the fetal brain by Monteagudo and Timor-Tritsch (11), it was reported that the first visualization of the cingulate gyrus lagged behind that reported in neuroanatomic studies by at least 8 weeks. It is likely that the lag in the entire population is longer than 8 weeks, because only the first visualization in only those brains in which the target sulci were seen was reported. The time lag between neuroanatomic and imaging studies is important because neuroanatomic assessment of cortical maturation in normal fetuses is a reliable indicator of fetal maturity (2,8).

Because fetal MR imaging is increasingly used to assess fetal central nervous system (CNS) anomalies (12–19), it is important to establish the normal appearance of the fetal brain with respect to gestational age (GA) and to evaluate whether this normal appearance is altered in fetuses with CNS anomalies. We hypothesize that in the abnormal brain, development may not proceed normally and that cortical maturation may be affected as well. The purpose of the present study was to establish the appearance of normal fetal cortical development in utero and to compare it with the patterns of abnormal fetal cortical development.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Ninety-three fetal MR imaging examinations were reviewed. The GA range was 14–38 weeks. The numbers of normal fetuses in each GA group are listed in Table 1. Fifty-three fetuses had normal CNS MR images, nine had isolated mild ventriculomegaly, and 31 had other CNS anomalies. MR imaging was performed by using a 1.5-T superconducting system (Vision; Siemens, Erlangen, Germany) and a four-element, phased-array body coil. MR images were acquired by using a half-Fourier rapid acquisition with relaxation enhancement (RARE) technique with an echo spacing of 4.2 msec, echo time (TE) of 60 msec, echo train length of 72, section thickness of 3–5 mm, field of view of 26 x 35 cm, acquisition matrix of 128 x 256, and refocusing flip angle of 130°, for a total acquisition time of 19 seconds (ie, 420 msec per section)(9). All studies were performed either for clinical indications (ie, pelvic masses) or under protocols that were approved by the internal review board of Beth Israel Deaconess Medical Center. Written informed consent was obtained from all patients prior to the MR imaging examinations.

Two reviewers (D.L., P.D.B.) together identified cortical landmarks on each study. The GA at the time of visualization of each sulcus was tallied for each fetus. In cases of agenesis of the corpus callosum, the cingulate sulcus was not included in the assessment of the sulcus. Differences of opinion were discussed, and a final assessment as to whether a sulcus or fissure was depicted was made.

Fetuses were classified as having (a) a normal CNS, (b) isolated mild ventriculomegaly with no other morphologic abnormality other than a ventricular diameter of less than 15 mm at the atrium, or (c) another type of CNS anomaly. Repeat MR imaging examinations were performed in three fetuses with CNS anomalies. In the 46 fetuses in which MR imaging examinations were performed for a suspected fetal CNS abnormality (40 examinations performed in 37 abnormal fetuses and nine normal fetuses), the classification of normal or abnormal CNS was based on the results of postnatal follow-up at autopsy (n = 3), results of surgery (n = 7), findings at postnatal imaging (n = 23), and prenatal MR imaging appearance (n = 13) when postnatal follow-up was not available or the pregnancy was ongoing. The "other CNS anomalies" are listed in Table 2.

The GAs according to visualization of the cerebral fissures or sulci were compared with the GAs determined in anatomic specimens by Chi et al (1). These guidelines describe GAs at which 25%–50% of brain specimens demonstrate particular cortical landmarks, with an interval of approximately 2 weeks between the earliest appearance of a particular landmark and its occurrence in 75%–100% of the brains. The appearances of sulci or fissures according to GA in the fetuses with normal brain MR images are listed in Table 1.

Anticipating that an individual fissure or sulcus would be difficult to image, we also compared the following grouped appearances of fissures or sulci, as suggested in the article by Chi et al (1): sylvian, interhemispheric (10–15 weeks); circular, calcarine, parieto-occipital, cingulate (16–19 weeks); central, superior temporal (20–23 weeks); precentral, postcentral, superior frontal (24–27 weeks); inferior frontal, inferior temporal (28–31 weeks); insular, parietal, superior occipital, secondary frontal, secondary parietal, secondary temporal (32–35 weeks); and inferior occipital, tertiary frontal, and tertiary parietal (36–39 weeks) (1). Landmarks of GA were considered to have been achieved when greater than or equal to one-half of the expected fissures or sulci were seen in that particular menstrual age group. The statistical methods used included the Student t test and the Fisher exact test.

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
On all the normal fetal brain MR imaging examinations, the sulcation landmarks appeared in the order predicted by using anatomic studies (Table 1, Figs 1–5). However, there was a 0–8-week lag (mean time ± SD, 1.9 weeks ± 2.2) between the MR imaging depiction of the sulci or fissures and the reported visualization of the sulci or fissures in anatomic specimens. The greatest lags were at 20–32 weeks GA. The sulci of which there were the greatest lags in time of appearance were the calcarine and cingulate sulci; there was an 8-week time lag with each. When comparing the fetuses in the normal brain MR imaging examination group with those with isolated mild ventriculomegaly and with those with other CNS anomalies, there was a 2-week mean lag in the time of appearance of the fissures or sulci in the abnormal groups (P < .01) (Table 3).

View larger version (166K): [in this window] [in a new window]   Figure 1. Coronal half-Fourier RARE MR image (TE, 60 msec) of a fetal brain at 18 weeks gestation. A cavum septum pellucidum (arrow) is seen. Note the wide sylvian fissures (arrowheads). The sylvian fissure begins as a shallow depression at 14 weeks gestation and subsequently becomes grooved.

View larger version (131K): [in this window] [in a new window]   Figure 5a. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain at 37 weeks gestation. (a) Just lateral to the midline, the pons (p) and cerebellum (c) are well seen. This image demonstrates secondary frontal sulci (arrowheads) and gyri (arrows), which are landmarks of 32–35 weeks gestation. (b) Lateral to a, the temporal sulci (arrows) are seen separating the superior (s), middle (m), and inferior (i) temporal gyri.

View larger version (122K): [in this window] [in a new window]   Figure 5b. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain at 37 weeks gestation. (a) Just lateral to the midline, the pons (p) and cerebellum (c) are well seen. This image demonstrates secondary frontal sulci (arrowheads) and gyri (arrows), which are landmarks of 32–35 weeks gestation. (b) Lateral to a, the temporal sulci (arrows) are seen separating the superior (s), middle (m), and inferior (i) temporal gyri.

View larger version (154K): [in this window] [in a new window]   Figure 6a. (a) Axial and (b) sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain with mild ventriculomegaly (V) at 22 weeks gestation. The interhemispheric (long arrow in a) and sylvian (short arrow in a) fissures are seen, but the sulcal landmarks of 16–19 weeks gestation (ie, the circular, calcarine, parieto-occipital, and cingulate sulci) and of 20–23 weeks gestation (ie, the central and superior temporal sulci) are not seen.

View larger version (148K): [in this window] [in a new window]   Figure 6b. (a) Axial and (b) sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain with mild ventriculomegaly (V) at 22 weeks gestation. The interhemispheric (long arrow in a) and sylvian (short arrow in a) fissures are seen, but the sulcal landmarks of 16–19 weeks gestation (ie, the circular, calcarine, parieto-occipital, and cingulate sulci) and of 20–23 weeks gestation (ie, the central and superior temporal sulci) are not seen.

View larger version (142K): [in this window] [in a new window]   Figure 7. Sagittal half-Fourier RARE MR image (TE, 60 msec) of a fetus with a large encephalocele (solid arrow) at 22 weeks gestation. None of the normal fissures or sulci are seen. The open arrow indicates pleural effusion.

In the normal fetuses, the expected MR imaging sulcation landmarks in the group with younger GAs than the actual GA were seen in 50 (94%) of 53 fetuses, and the landmarks of the actual GA were seen in 35 (66%) of the 53 fetuses. The corresponding percentages were 56% (five of nine fetuses, P < .05) and 33% (three of nine fetuses, not significant), respectively, with isolated mild ventriculomegaly and 77% (24 of 31 fetuses, P < .05) and 35% (11 of 31 fetuses, P < .05), respectively, with other CNS anomalies.

Three of the fetuses classified as having a normal CNS, two at 20 weeks gestation and one at 24 weeks gestation, did not achieve the landmarks of sulcation of the group younger than their expected GA.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
This work serves as a baseline for the MR imaging appearance of the normal fetal brain in vivo that can be used to detect abnormal maturation in fetuses with morphologic abnormalities. Further studies are needed to substantiate the results of our study. We found that cortical development follows a predictable pattern, as suggested by the results of anatomic studies. It is reasonable that the MR imaging findings of sulcation should lag behind those of anatomic specimens, because the MR imaging section thickness is much greater than that used in the anatomic studies of Chi et al (1). In the study by Chi et al (1), 15–30-µm-thick brain sections were examined visually for early sulcal development. Shallow indentations were considered to be sufficient to indicate the presence of a particular sulcus or fissure. Obviously, MR imaging of the shallow indentations in early sulcal development is more difficult than direct visualization because of not only the degradation inherent with the imaging process itself but also the 1,000-fold increase in section thickness. In addition, the guidelines described by Chi et al document the appearance according to GA at which 25%–50% of brains demonstrate the structure, with an interval of approximately 2 weeks between the earliest appearance of a particular structure in the brain and its occurrence in 75%–100% of brains.

One other factor that possibly contributed to the time lag is that the majority of the MR imaging studies of normal fetal brains in our series were performed for maternal rather than fetal indications. Therefore, section acquisitions frequently were nonorthogonal to the brain. This bias may have had the effect of "delaying" the appearance of sulci or fissures in the normal fetuses, because orthogonal imaging planes were used to examine the fetuses with abnormal brain morphologies.

Another factor that possibly contributed to a lag in the depiction of sulci or fissures is the inclusion of twin fetuses in our study population. Chi et al (1) reported a 2–3-week lag in the appearance of sulci or fissures in twins compared with that in singleton fetuses. The number of twin fetuses in our study was too small to confirm that a similar trend exists when sulci or fissures are evaluated by using MR imaging.

In neonatal studies, Huang (5) found an 8–9-week lag in the US appearance of sulci compared with the appearance of sulci before 28 weeks gestation in anatomic studies, and a 1–3-week lag in the US appearance of sulci at 28–31 weeks gestation. Huang concluded that the younger the brains, the larger the differences in time of sulcal appearance between US studies and neuroanatomic studies. Our MR imaging results did not demonstrate that younger brains have greater time lags. For example, all of the normal brains at 18 weeks gestation demonstrated the calcarine fissure at MR imaging. The greatest time lags in our studies were those of the fetuses at 26–27 weeks gestation and at 32–33 weeks gestation. However, some of the results in our study were similar to those in the Huang study (5) in that the calcarine sulcus was seen in all normal fetuses by 26–27 weeks gestation; the cingulate sulcus, by 27 weeks gestation; the postcentral sulcus, by 28 weeks gestation; the inferior temporal sulcus, by 32 weeks gestation; and the insular sulcus, by 35 weeks gestation.

When examining fetuses with an abnormal brain at MR imaging, we found a mean 2-week lag in cortical development compared with the cortical development in normal fetuses. The results of the study by Slagle et al (22) demonstrated that infants with intraventricular hemorrhage and ventricular dilatation, parenchymal hemorrhage, or cystic periventricular leukomalacia had local delays in convolutional maturation. They hypothesized that alterations in local nutrients and associated decreases in cellular proliferation might result in delayed sulcal development. Similarly, in our series, mild ventriculomegaly was associated with delays in the appearance of the sulci or fissures. It is not certain whether this delay is real, or the lack of sulcal appearance at MR imaging is related to sulcal deformation.

Fetuses with mild ventriculomegaly are at risk for developmental delay (23–26). When the ventriculomegaly is isolated, it is associated with lower morbidity and mortality relative to that in nonisolated cases. Many children with mild ventriculomegaly are judged to be completely healthy at birth (23). Further studies are necessary to identify whether those fetuses with delayed cortical maturation in addition to mild ventriculomegaly are those who eventually demonstrate developmental delay.

In our study, the fetuses with CNS anomalies other than mild ventriculomegaly showed wide variations in cortical development, as expected given the wide variation in the types of anomalies evaluated. The fetuses with the more severe developmental abnormalities had delays in cortical development that depended on the GA at the time of the MR imaging examination. For example, the fetus with holoprosencephaly was examined at 16 weeks gestation and had no interhemispheric fissure. This represented a 6-week delay according to our scoring method. A fetus with a frontal encephalocele was examined at 33 weeks gestation and had no sylvian fissure; this indicated a delay of 21 weeks according to our scoring method. The delay in weeks is rather arbitrary in these two cases; it demonstrates that the markers of cortical development are unreliable in the grossly malformed or deformed brain. However, this is unlikely to be problematic in the evaluation of severe fetal brain anomalies, because an assessment of cortical development is unlikely to change the prognosis.

One potential false-positive case with a long delay was a fetus with a lumbar neural tube defect and ventriculomegaly that was examined at 26 weeks gestation. The interhemispheric fissure, along with portions of the sylvian fissure and superior temporal sulcus, was present; these findings suggested normal cortical development. However, the calcarine and parietooccipital fissures were not depicted, and no extracerebral cerebrospinal fluid could be identified. The nondepiction of the fissures was probably related to effacement caused by obstructive hydrocephalus.

There is up to an 8-week delay in the appearance of the sulci or fissures in normal fetal brains as visualized by using MR imaging. In addition, by using the "grouped" appearance of sulci or fissures, it is expected that normal fetuses will have attained the landmarks of the group with younger GAs than the actual GA. If a delay of 10 weeks or longer is indicated on an otherwise normal-appearing image, or if the grouped landmarks of the GA younger than that of the actual GA have not developed, the results should be interpreted as potentially abnormal. Further studies are needed to substantiate these results and to perform postnatal follow-up of the development of infants with in utero cortical development delays before patients can be adequately counseled on the importance of these abnormal results.

However, detailed knowledge of the appearance of normal fetal cortical development on MR images will be useful in screening patients at risk for abnormal cortical development—for example, in pregnant patients with a family history of lissencephaly. Lissencephaly (ie, agyria-pachygyria spectrum) is one expression of various genetic and nongenetic conditions (27) that are important causes of mental retardation and epilepsy. In cases of known chromosome abnormalities, a diagnosis can be made with chorionic villous sampling or amniocentesis. However, many cases are of unknown cause, but they can still be inherited as an autosomal recessive trait (27,28). In lissencephaly, the cerebral gyri are almost completely absent. The surface of the brain is smooth, similar to that of fetuses before 20 weeks gestation. The prenatal US-based diagnosis cannot be made with confidence, because the cortical sulci typically are not depicted. It is our expectation that MR imaging will aid in screening for this disease.

In conclusion, cortical maturation, as manifested by the progressive appearance of cerebral fissures and sulci, is clearly demonstrated by using fetal MR imaging. Normal maturation as depicted at MR imaging follows a predictable course that is slightly delayed compared with that described in neuroanatomic specimens. This maturation is delayed in many fetuses with CNS abnormalities. Further studies are needed to substantiate the results of our study and to evaluate how the abnormal sulcal appearance correlates with postnatal cognitive and motor development.

View larger version (87K): [in this window] [in a new window]   Figure 2a. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetus at 26 weeks gestation. (a) Slightly oblique and off-midline view shows the corpus callosum (arrows), massa intermedia (m), and parieto-occipital fissure (arrowhead). (b) Slightly lateral to a, a smooth cerebral surface, along with the early appearance of the precentral (arrow 1) and central (arrow 2) sulci, is depicted. The central sulcus is a landmark of 20 weeks gestation, and the precentral sulcus is a landmark of 24 weeks gestation. (Reprinted, with permission, from reference 20.)

View larger version (80K): [in this window] [in a new window]   Figure 2b. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetus at 26 weeks gestation. (a) Slightly oblique and off-midline view shows the corpus callosum (arrows), massa intermedia (m), and parieto-occipital fissure (arrowhead). (b) Slightly lateral to a, a smooth cerebral surface, along with the early appearance of the precentral (arrow 1) and central (arrow 2) sulci, is depicted. The central sulcus is a landmark of 20 weeks gestation, and the precentral sulcus is a landmark of 24 weeks gestation. (Reprinted, with permission, from reference 20.)

View larger version (146K): [in this window] [in a new window]   Figure 3a. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain at 30 weeks gestation. (a) The cingulate sulcus (white arrows), parieto-occipital fissure (thin black arrow), and calcarine fissure (thick black arrow) are seen. p = pons. (Reprinted, with permission, from reference 21.) (b) Slightly lateral to a, the precentral (arrow 1), central (arrow 2), and postcentral (arrow 3) sulci are seen. (c) Further lateral to a, the superior temporal sulcus (arrowhead) is seen.

View larger version (144K): [in this window] [in a new window]   Figure 3b. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain at 30 weeks gestation. (a) The cingulate sulcus (white arrows), parieto-occipital fissure (thin black arrow), and calcarine fissure (thick black arrow) are seen. p = pons. (Reprinted, with permission, from reference 21.) (b) Slightly lateral to a, the precentral (arrow 1), central (arrow 2), and postcentral (arrow 3) sulci are seen. (c) Further lateral to a, the superior temporal sulcus (arrowhead) is seen.

View larger version (142K): [in this window] [in a new window]   Figure 3c. Sagittal half-Fourier RARE MR images (TE, 60 msec) of a fetal brain at 30 weeks gestation. (a) The cingulate sulcus (white arrows), parieto-occipital fissure (thin black arrow), and calcarine fissure (thick black arrow) are seen. p = pons. (Reprinted, with permission, from reference 21.) (b) Slightly lateral to a, the precentral (arrow 1), central (arrow 2), and postcentral (arrow 3) sulci are seen. (c) Further lateral to a, the superior temporal sulcus (arrowhead) is seen.

View larger version (156K): [in this window] [in a new window]   Figure 4. Coronal half-Fourier RARE MR image (TE, 60 msec) of a fetal brain at 35 weeks gestation. The corpus callosum (arrowheads) is seen as a dark band above the cavum septum pellucidum (c). The insular cortex (arrows) is still relatively smooth. In histopathologic specimens, insular gyri are seen at 32–35 weeks gestation.

	Footnotes

 
Supported in part by National Institutes of Health grant NS 37945.

Address reprint requests to D.L.

From the 1997 RSNA scientific assembly.

Abbreviations: GA = gestational age CNS = central nervous system RARE = rapid acquisition with relaxation enhancement

Author contributions: Guarantor of integrity of entire study, D.L.; study concepts and design, D.L., P.D.B.; definition of intellectual content, D.L., P.D.B.; literature research, D.L., P.D.B.; clinical and experimental studies, D.L.; data acquisition, D.L., P.D.B.; data and statistical analyses, D.L.; manuscript preparation, D.L.; manuscript editing and review, P.D.B.

Received February 17, 1998; revision requested April 27, 1998; revision received August 7, 1998; accepted October 13, 1998.

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