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DOI: 10.1148/radiol.2383041283
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(Radiology 2006;238:997-1003.)
© RSNA, 2006

Obstetric Imaging

Fetal Posterior Fossa Volume: Assessment with MR Imaging1

Sara C. Chen, MD, Erin M. Simon, MD, John C. Haselgrove, PhD{dagger}, Larissa T. Bilaniuk, MD, Leslie N. Sutton, MD, Mark P. Johnson, MD, David M. Shera, PhD and Robert A. Zimmerman, MD

1 From the Department of Radiology, University of Pennsylvania School of Medicine, Philadelphia, Pa (S.C.C., E.M.S., L.T.B., L.N.S., M.P.J., R.A.Z.); and Department of Radiology, the Children's Hospital of Philadelphia, 34th St and Civic Center Blvd, Philadelphia, PA 19104-4399 (E.M.S., J.C.H., L.T.B., L.N.S., M.P.J., D.M.S., R.A.Z.). Received July 27, 2004; revision requested October 5; revision received March 21, 2005; accepted April 18; final version accepted, May 25. Address correspondence to E.M.S. (e-mail: Simon{at}email.chop.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Purpose: To retrospectively determine the relationship between posterior fossa volume (PFV) and estimated gestational age (EGA) and/or femur length (FL) during pregnancy for the purpose of developing a normal growth curve.

Materials and Methods: Advance institutional review board approval was obtained for this HIPAA-compliant study, and the need for parent informed consent was waived. A cross-sectional retrospective study was performed to measure PFV on in vivo magnetic resonance (MR) images obtained in 76 fetuses of 18–36 weeks gestation who had a morphologically normal CNS. Because this was a retrospective series, MR imaging techniques varied slightly, but all fetuses underwent imaging at contiguous 3–5-mm intervals in at least two orthogonal planes, with repetition time msec/echo time msec, 5–12/62–95; number of signals acquired, one; flip angle, 150°–180°; and matrix, 128–192 x 256. Posterior fossa areas were manually traced on half-Fourier rapid acquisition with relaxation enhancement in utero fetal MR images by one observer. PFVs were then calculated by manually summing areas from the contiguous sections and multiplying the total area by the section thickness. An average PFV (APFV) across orthogonal planes was calculated for each fetus, and the relationship between APFV and EGA was mathematically modeled. Coronal, transverse, and sagittal views were compared with correlations and Bland-Altman plots. Two additional observers repeated the measurements for a small subset of fetuses (n = 5). Paired t test analyses were also performed to determine significant differences between sagittal, transverse, and coronal measurements, as well as to determine preliminary intraobserver and interobserver variability of measurements in a subset of cases.

Results: The relationship between APFV (in cubic centimeters) and EGA (in weeks) was well described by a single exponential function [APFV = 0.689 exp(EGA/9.10)]. APFV doubling time was 6.31 weeks. Root-mean-square variation of values around the model line was 1.63 cm3. There was no statistically significant intra- or interobserver variation (P > .16 for all fetuses) at preliminary analysis. No correlation between APFV and FL could be found.

Conclusion: The normal fetal PFV growth curve generated in this study may have potential as a model for clinical application.

© RSNA, 2006


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Normal ranges for fetal posterior fossa volume (PFV) throughout the second and third trimesters of pregnancy may have the ability to provide valuable prognostic information for fetuses with central nervous system (CNS) conditions in which the posterior fossa is abnormal. In the Chiari II malformation with myelomeningocele, PFV is known to be small, while in the Dandy-Walker spectrum of malformations, it often subjectively appears to be large. To our knowledge, no literature documents the normal size of the fetal posterior fossa alone, relative to gestational age, or relative to established biometric parameters throughout this time period.

Standards of fetal cerebellar growth during the second and third trimesters have been generated on the basis of transverse cerebellar diameters measured at conventional two-dimensional ultrasonography (US) (1–3). These data, however, do not quantitate PFV and are only an indirect measure of the entire posterior fossa. Similarly, relatively recent studies that focused on the development of the fetal cerebellar vermis alone did not involve assessment of the posterior fossa and its contents as a whole (4,5). Studies in which three-dimensional US was used have focused on structural assessment but not measurement of the entire fetal brain (6,7). Fetal head circumference as determined by using three-dimensional US is a clinically valuable parameter but does not address the posterior fossa (8). In addition, diagnostic US of the fetal brain does not routinely yield the image clarity or accuracy possible with magnetic resonance (MR) imaging, especially during the second and third trimesters (9–13).

Other studies have involved the use of stereologic techniques on MR images to evaluate total fetal brain volume in the third trimester (14,15). However, these measures do not allow for discrete PFV determination. Therefore, there is a strong research and clinical need for the development of a standard curve that describes the normal volume of the fetal posterior fossa in the second and third trimesters of pregnancy.

Available postnatal methods of evaluation of the posterior fossa are dependent on ionizing radiation and are not applicable to a fetal population. For example, the "posterior fossa ratio" developed by Krogness (16) and Krogness and Nyland (17,18) in the 1970s was based on an area ratio derived with two-dimensional postnatal skull radiography. Variations in the third (transverse) dimension, which are not visible on lateral radiographs, could not be taken into account. Badie et al (19) have applied this posterior fossa ratio to MR imaging. However, their internal standard of reference was the supratentorial compartment. Clearly, the use of the supratentorial compartment as a standard of reference has substantial potential to introduce inaccuracy because many primary and secondary conditions that affect the posterior fossa involve associated supratentorial anomalies, and posterior fossa anomalies can affect the supratentorial volume.

Work performed by Nishikawa et al (20) in adults involved comparing the volume of the posterior fossa neural tissue as measured with MR imaging with the volume of the osseous confines of the posterior fossa as measured with computed tomography (CT). This "volume ratio" was specifically tailored for the assessment of the adult posterior fossa in the setting of the Chiari I malformation, did not take age into account, and would not be applicable to a fetal population.

With the advent of rapid acquisition MR imaging as a complement to US, more precise assessment of the fetal CNS has become possible. In particular, the fetal posterior cranial fossa and its contents can now be visualized more precisely (9–13,21). Thus, the purpose of our study was to retrospectively determine the relationship between PFV and estimated gestational age (EGA) and/or femur length during pregnancy for the purpose of creating a normal growth curve.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study Fetuses
Institutional review board approval was obtained in advance for this cross-sectional retrospective study, which was compliant with the terms of the Health Insurance Portability and Accountability Act. The need to obtain informed consent from the parents was waived. Data in 76 fetuses imaged between January 1999 and August 2001 were available for review. Inclusion criteria were as follows: singleton intrauterine gestation with absence of a documented fetal chromosomal abnormality, absence of diagnosed maternal conditions known to affect the normal growth of the fetus (ie, maternal diabetes or hypertension), and documented MR imaging report of an anatomically normal and developmentally appropriate fetal CNS between 18 and 36 weeks gestation.

In all fetuses, MR imaging was clinically indicated for isolated non-CNS anomalies (Table 1). Each fetus was measured at one time point. All images were reviewed by one or more pediatric neuroradiologists (E.M.S., L.T.B., and/or R.A.Z., all of whom had at least 3 years of experience in fetal brain imaging) to confirm normal morphologic features of the fetal CNS.


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  		Table 1. MR Imaging Diagnoses for 76 Fetuses

 
Fetal sex was known for 68 (89%) of the 76 fetuses. Sex was determined with chromosomal analysis for 38 (56%) of the 68 fetuses and through postnatal follow-up for 30 (44%) fetuses. Thirty-eight (50%) of the 76 fetuses were male, and 30 (39%) were female.

EGA at the time of MR imaging was determined on the basis of standard clinical criteria. Thus, if gestational age as determined by reference to the first day of the last menstrual period and average US age were discordant by 14 or fewer days, the EGA was based on the first day of the last menstrual period. If they were discordant by more than 14 days, the average US age was used. In 68 (89%) of the 76 fetuses, the first day of the last menstrual period was used for EGA determination. In 61 of these 68 fetuses, the average US age was based on that observed at a second- or third-trimester US examination (the 2-week discrepancy is well within the margin of error for "dating" US examinations during these periods of gestation). For two of the eight fetuses in whom EGA was based on the average US age, only the average US age was available and was thus used for dating. In the remaining six fetuses in whom EGA was based on the average US age, the EGA based on the first day of the last menstrual period and the average US age were discordant by an average of 3 weeks, which is minimally outside the accuracy range of later trimester "dating" US examinations.

If the US examination whose results were used for EGA determination had been performed at the Department of Radiology at the Hospital of the University of Pennsylvania (n = 19), the interval between US and MR imaging was 0–1 day. If US had been performed at a nonaffiliated institution (n = 54), the interval between US and MR imaging ranged from 10 days to 3 months (depending on the EGA at the time of MR imaging). In three fetuses, the US examination for EGA determination was performed by the Department of Obstetrics and Gynecology at the Hospital of the University of Pennsylvania, with a 10–30-day interval between US and MR imaging.

MR Imaging and Image Analysis
Because this was a retrospective series, MR imaging techniques varied slightly; however, all fetuses were imaged with a 1.5-T MR imaging unit (Vision or Sonata; Siemens, Erlangen, Germany) at contiguous 3–5-mm intervals in at least two orthogonal planes with a repetition time msec/echo time msec of 5–12/62–95, one signal acquired, a flip angle of 150°–180°, and a matrix of 128–192 x 256. For 16 of the 76 study fetuses, motion-degraded or off-axis images acquired during an otherwise acceptable imaging study were excluded. Posterior fossa areas in the sagittal, coronal, and transverse planes (when available) were manually traced by one observer (S.C.C.) on half-Fourier rapid acquisition with relaxation enhancement in utero fetal MR images. Posterior fossa subarachnoid spaces, but not deep venous sinuses, were included in these measurements. The confines of the posterior fossa were traced in each plane (Fig 1). The superior margin was defined as follows: The anterior half consisted of a line from the dorsal clivus to the tentorium cerebelli (traversing the diencephalic-mesencephalic junction), and the posterior half consisted of the undersurface of the tentorium cerebelli. The foramen magnum delineated the inferior margin.


Figure 1
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  		Figure 1a: Half-Fourier rapid acquisition with relaxation enhancement MR images (62/5) of brain in representative 21-week-old fetus in (a) sagittal, (b) coronal, and (c) transverse planes. Outlined in white are the boundaries of the posterior fossa, which include the entire cerebellum, brainstem, and extraaxial spaces.

 

Figure 1
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  		Figure 1b: Half-Fourier rapid acquisition with relaxation enhancement MR images (62/5) of brain in representative 21-week-old fetus in (a) sagittal, (b) coronal, and (c) transverse planes. Outlined in white are the boundaries of the posterior fossa, which include the entire cerebellum, brainstem, and extraaxial spaces.

 

Figure 1
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  		Figure 1c: Half-Fourier rapid acquisition with relaxation enhancement MR images (62/5) of brain in representative 21-week-old fetus in (a) sagittal, (b) coronal, and (c) transverse planes. Outlined in white are the boundaries of the posterior fossa, which include the entire cerebellum, brainstem, and extraaxial spaces.

 
The number of sections per plane per fetus was dependent on section thickness (range, 3–5 mm; no intersection gap) and EGA. Section thickness was not determined by EGA or by imaging plane, and there were typically seven to nine sections per plane.

Manual tracing of the defined region on each section was performed by using a picture archiving and communication system (PACS; Siemens) that calculated the area for the region of interest. Volumes were then calculated by manually summing areas from the contiguous sections and multiplying the total area by the section thickness. An average PFV (APFV) value across orthogonal planes was calculated for each fetus, and the relationship between APFV and EGA was mathematically modeled. The relationship between APFV and exact EGA (in weeks and days) was modeled as a single exponential growth curve by using the following equation: APFV = Ao · exp(EGA/T). The constants Ao and T were calculated from the intercept and the slope of the straight line regression between ln(APFV) and EGA.

APFV was also independently correlated (S.C.C.) with femur length as measured at US performed on the same day as the MR imaging examination in 73 fetuses.

Record Review
When available, postnatal medical records were reviewed (S.C.C., E.M.S.) for brain imaging and/or neurologic examination findings.

Statistical Analysis
Coronal, transverse, and sagittal views were compared with correlations and Bland-Altman plots. Given the assumption of an exponential growth model, the log volumes were fit with a linear model to provide a mean and 95% confidence intervals for an additional observation at each EGA. In addition, for those fetuses in whom EGA was derived at a US examination performed after the first trimester (US examinations performed after the first trimester may be less accurate for pregnancy dating purposes), a weighted regression analysis was performed in which data were given a weight of one-half instead of one. Finally, the log volumes were fit with a linear model (J.C.H., D.M.S.) after the data in the above-mentioned fetuses were excluded—the equivalent of giving these data a weight of zero. Analyses were performed by using statistical software (SAS, version 9.1; SAS Institute, Cary, NC).

Paired t test analyses were also performed (J.C.H., D.M.S.) to determine significant differences between sagittal, transverse, and coronal measurements. P = .05 was considered to indicate a significant difference.

So that we could preliminarily assess intraobserver variability, APFV was remeasured by the original observer (S.C.C.) in a sample set of three fetuses whose EGAs spanned the gestational age period being evaluated. These measurements were then compared with the original data set by using the paired t test. APFV was also remeasured by two additional observers (E.M.S., L.T.B.) in another subset of five fetuses (one fetus had an EGA of 19 weeks 1 day, one had an EGA of 23 weeks 4 days, one had an EGA of 27 weeks 4 days, one had an EGA of 29 weeks 3 days, and one had an EGA of 34 weeks 0 days). Paired t test analyses were then performed with these data and the original data for a limited assessment of interobserver variability.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
APFV Results
Student t testing and Bland-Altman plots (Fig 2) indicated that there were no significant differences in APFV value between coronal, transverse, and sagittal images (P > .2 for all comparisons), suggesting that the three measurements could be averaged. The mean difference in the AFPV value between coronal and transverse images was –0.14 cm3 ± 0.88 (standard deviation) (P = .23), the mean difference between coronal and sagittal images was –0.03 cm3 ± 0.84 (P = .78), and the mean difference between sagittal and transverse images was –0.06 cm3 ± 0.86 (P = .59). Correlations among coronal, transverse, and sagittal measurements were all extremely high, with all estimates greater than 0.99.


Figure 2
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  		Figure 2: Bland-Altman plots for PFV measurements on transverse, coronal, and sagittal MR images. Numbers on x-axis indicate the average value of PFV in cubic centimeters obtained from the two planes listed. On the y-axis, for example, Coronal – Axial in mm3 indicates the difference (in cubic millimeters) between the APFV values obtained from these two planes. Dashed lines represent 95% confidence intervals.

 
The relationship between APFV in cubic centimeters and EGA in weeks (calculated with reference to the first day of the last menstrual period for 68 [89%] of 76 fetuses) was well described by a single exponential growth curve [APFV = 0.689 exp(EGA/9.10)] (Fig 3). APFV doubling time was 6.31 weeks. The root-mean-square variation of values around the model line was 1.63 cm3.


Figure 3
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  		Figure 3: APFV versus EGA. Graph shows APFV in cubic centimeters as a function of EGA in weeks. Each symbol represents the APFV for a single study fetus. Exact EGA was calculated and plotted as a decimal number (eg, 20 weeks 4 days = 20 weeks 4/7 days = 20.57 weeks). The central dark line represents the mathematical model of the data, which is the exponential function [APFV = 0.689 exp(EGA/9.10)]. APFV doubling time is 6.31 weeks, and the root-mean-square value is 1.63 cm3. The outer dark lines represent twice the root-mean-square value calculated without the fetuses older than 30 weeks gestation. The outer light lines represent twice the root-mean-square value calculated with the fetuses older than 30 weeks gestation. There is no significant difference.

 
All three methods of weighting observations with various determinants of EGA yielded similar results; the predicted confidence intervals were nearly identical (Table 2). Preliminary intraobserver variability (observer 1: mean difference, –0.86 cm3 ± 1.03 [P = .29]) and interobserver variability (observer 1 vs observer 2: mean difference, –0.60 cm3 ± 0.28 [P = .16]; observer 1 vs observer 3: mean difference, –0.06 cm3 ± 1.54 [P = .93]; observer 2 vs observer 3: mean difference, 0.54 cm3 ± 1.06 [P = .31]) appeared grossly acceptable.


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  		Table 2. Confidence Bounds Yielded by Weighted Model

 
Calculation of ratios of APFV to femur length (range, 1.79–4.94) failed to reveal any EGA-independent value.

Record Review
Postnatal follow-up records and/or imaging data were available for 26 fetuses (mean age, 9.8 months; range, 1 day to 25 months). Nine fetuses (five at US, one at CT, and three at MR imaging) had normal postnatal brain imaging results. Fifteen fetuses, including three of the fetuses with normal postnatal brain imaging results, had unremarkable postnatal neurologic examination results. In five fetuses, including one fetus born at 33 weeks gestation who had seizures and periventricular leukomalacia and hydrocephalus also documented with postnatal MR imaging, US revealed periventricular leukomalacia or grade I germinal matrix hemorrhage that was attributed to prematurity.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
MR imaging is a useful way of measuring the volume of the fetal posterior fossa between 18 and 36 weeks gestation and may prove valuable in assessing fetal anomalies in the future.

The modeled growth curve generated by our results, with normal ranges for each EGA, can be considered as a model for clinical application.

Measurements from the single plane in which the fetal posterior fossa is most readily visualized appear to be adequate for practical evaluation. In our experience, measuring the volume in the sagittal plane was easiest. This is in contrast to US, where the transverse plane is usually considered best for visualization and quantitative measurements.

Possible methodologic issues that could have affected the accuracy and precision of the results were addressed as follows:

1. Although the selected patient population did not have appreciable CNS abnormalities, there was a theoretical possibility that an undetected CNS anomaly existed. The presence of normal chromosome study results and normal CNS morphologic findings in the study fetuses argues against the presence of any important undetected CNS anomaly in these fetuses, as do the follow-up results available for more than one-third of the fetuses.

2. Relative to the sample size in other fetal biometry studies, the sample size of 76 fetuses in this study was relatively small. However, additional measurements would have been statistically unlikely to alter the shape of the defined exponential curve, as demonstrated by the close fitting of the model curve and predicted confidence intervals with the actual data points.

3. Accurate gestational dating is crucial for the development of an accurate measurement tool. The criteria for determining EGA for this study were established on the basis of clinical practice guidelines, as well as on criteria previously used by groups studying fetal biometry (22,23). We are highly confident in the level of accuracy of EGA determination for the fetuses in this study. Results of our repeated statistical analyses, with various weightings of the gestational age determinants, also indicated that the modeled curve was not affected by these potential discrepancies. Thus, we can safely say that including those data points for which EGA had been determined at second- or third-trimester US did not bias our results.

4. Our sample suffered from a relative lack of data points at the extremes of gestational ages. This reflects the clinical indications for the MR imaging examinations and the clinical applicability of MR imaging for decision making in pregnancy management. The close fitting of the model, however, suggests that the addition of such data points would be unlikely to significantly alter the curve itself.

5. Poorly acquired CNS MR imaging studies may have the potential to introduce systematic errors in measurement because suboptimal visualization of the fetal CNS and posterior fossa landmarks may be present. Measurement precision was strengthened in part by eliminating the studies that yielded images whose planes were degraded by substantial fetal motion, head rotation, and/or off-axis imaging. We anticipate that the same criteria would be used in clinical practice.

Future investigations may involve evaluating immediate postnatal APFV values to determine the shape and most appropriate model for the posterior fossa growth curve after birth.

A secondary, long-term goal of this project is to use the model curve to evaluate PFV in fetuses with CNS malformations. The posterior fossa is abnormally small in the Chiari II malformation and in myelomeningocele. Relatively recent reports (24–26), however, have indicated that there is a reduction in the qualitative severity of posterior fossa malformations after in utero myelomeningocele repair. The quantitative measurement instrument developed in this study could be used to assess the effect on PFV of repair of the myelomeningocele in such fetuses and to follow up these fetuses prospectively because anecdotal experience indicates a marked improvement postoperatively.

These PFV measurements could potentially be correlated with neurologic outcomes and the need for ventricular shunting, as well as used in a predictive manner analogous to the current use of the lung-head ratio for the stratification of outcome for fetuses with congenital diaphragmatic hernia. Because the reduced volume of the posterior fossa leads to neurologic morbidity in children with myelomeningocele (27,28) and fetal surgery is not without risk to the mother and the fetus, the usefulness of a tool for objectively evaluating the posterior fossa in this population cannot be underestimated. This measurement instrument also has the potential to be applied to other conditions in which assessment of PFV may be important, such as the Dandy-Walker spectrum of anomalies, which often involve an enlarged posterior fossa.


   FOOTNOTES
 

Abbreviations: APFV = average PFV • CNS = central nervous system • EGA = estimated gestational age • PFV = posterior fossa volume

{dagger} Deceased Back

Author contributions: Guarantor of integrity of entire study, E.M.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, S.C.C., E.M.S., J.C.H.; clinical studies, S.C.C., E.M.S., L.T.B., M.P.J., R.A.Z.; experimental studies, S.C.C., J.C.H.; statistical analysis, S.C.C., E.M.S., J.C.H., D.M.S.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE