Download Comparison of ultrasound and magnetic resonance imaging in 100

BJOG: an International Journal of Obstetrics and Gynaecology
August 2004, Vol. 111, pp. 784 –792
DOI: 1 0 . 1 1 1 1 / j . 1 4 7 1 - 0 5 2 8 . 2 0 0 4 . 0 0 1 4 9 . x
Comparison of ultrasound and magnetic resonance imaging in
100 singleton pregnancies with suspected brain abnormalities
E.H. Whitby,a M.N.J. Paley,a A. Sprigg,b S. Rutter,c N.P. Davies,c
I.D. Wilkinson,a P.D. Griffithsa
Objective To compare the diagnostic accuracy of the current reference standard-ultrasound with in utero
magnetic resonance imaging, in a selected group of patients.
Design Prospective study.
Setting Five fetal maternal tertiary referral centres and an academic radiology unit.
Sample One hundred cases of fetuses with central nervous system abnormalities where there has been
diagnostic difficulties on ultrasound. In 48 cases the women were less than 24 weeks of gestation and in
52 cases later in pregnancy.
Methods All women were imaged on a 1.5 T clinical system using a single shot fast spin echo technique. The
results of antenatal ultrasound and in utero magnetic resonance were compared.
Main outcome measures The definitive diagnosis was made either at autopsy or by postmortem magnetic
resonance imaging, in cases that went to termination of pregnancy, or a combination of postnatal imaging
and clinical follow up in the others.
Results In 52 of cases, ultrasound and magnetic resonance gave identical results and in a further 12, magnetic
resonance provided extra information that was judged not to have had direct effects on management. In 35
of cases, magnetic resonance either changed the diagnosis (29) or gave extra information that could have
altered management (6). In 11 of the 30 cases where magnetic resonance changed the diagnosis, the brain
was described as normal on magnetic resonance.
Conclusions In utero magnetic resonance imaging is a powerful tool in investigating fetal brain abnormalities.
Our results suggest that in selected cases of brain abnormalities, detected by ultrasound, antenatal magnetic
resonance may provide additional, clinically useful information that may alter management.
INTRODUCTION
The majority of women in the United Kingdom have
detailed ultrasound imaging studies of their fetus at 18–
20 weeks after their last menstrual period. The ultrasound
has several purposes, including detection of fetal anomalies.
It follows that the information gained from imaging must
be accurate in detecting the presence of an abnormality and
must, within the limitations of the technique, be able to
define the extent of the abnormality. Ultrasonography has
many advantages over other imaging methods in as much as
it does not use ionising radiation (unlike plain films or X-ray
computed tomography), the images have high anatomical
a
Academic Unit of Radiology, University of Sheffield, UK
Department of Paediatric Radiology, Sheffield Children’s
Hospital, UK
c
Department of Obstetrics and Gynaecology, Jessop Wing,
Sheffield, UK
b
Correspondence: Dr E. H. Whitby, Academic Unit of Radiology,
University of Sheffield, Floor C, Royal Hallamshire Hospital, Glossop
Road, Sheffield S10 2JF, UK.
D RCOG 2004 BJOG: an International Journal of Obstetrics and Gynaecology
resolution and are real time, which allows dynamic assessment of the fetus. Recent work using in utero magnetic
resonance imaging has suggested that in some anatomical
systems and disease processes magnetic resonance may have
advantages over ultrasound.1 – 4 Our early work highlighted
the likely usefulness of in utero magnetic resonance imaging
in the clinical setting where there are difficulties or concerns over the antenatal ultrasound for detecting some
brain and spine abnormalities.5 There have been few large
studies, however, that have performed detailed follow up
in order to confirm or refute the antenatal diagnoses and
even fewer that have attempted to look at effects on clinical
management.
In this article, we compared the diagnostic capability of
ultrasonography and in utero magnetic resonance imaging
of 100 singleton pregnancies, referred from several tertiary centres, in which ultrasound has shown a possible
brain abnormality. We obtained the relevant combinations
of clinical investigations, postnatal imaging, autopsy and
postmortem magnetic resonance imaging in order to
produce a definitive diagnosis for the abnormality. In
addition, we have attempted to judge the effect on clinical management made by performing in utero magnetic
resonance.
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ULTRASOUND VERSUS MRI IN PREGNANCIES WITH SUSPECTED ABNORMALITIES
785
Table 1. A histogram and table showing the gestational age of 100 women at the time of in utero magnetic resonance imaging of their fetus in intervals of
two weeks.
Gestation
16/17
18/19
20/21
22/23
24/25
26/27
28/29
30/31
32/33
34/35
36/37
38/39
No. cases
1
3
18
26
15
4
7
9
7
4
7
3
METHODS
The study was undertaken with the approval of the South
Sheffield Ethics Committee. All the procedures were carried
out after fully informed, written consent was obtained from
the mother. Women were recruited from five fetal anomaly
units in the North of England but all of the magnetic
resonance studies were performed in Sheffield. All magnetic
resonance examinations were performed within four days of
referral from the obstetric ultrasonographer. In many cases,
further ultrasound examinations and other investigations
were made before referral to magnetic resonance. Fortyeight of the cases were imaged by magnetic resonance
before 24 weeks (Table 1). The remainder were cases where
the anomaly was detected by ultrasound later in pregnancy
(21 cases were referred after 31 weeks of gestation) and in
those cases the magnetic resonance examination was usually
performed within two days of referral. All of the patients had
abnormalities of the fetal brain reported or queried on the
antenatal ultrasound examinations (but normal spines) and a
provisional ultrasound report was available to the magnetic
resonance reviewers (PDG, EW) at the time of the in utero
magnetic resonance examination. All the ultrasounds were
performed in fetal maternal speciality units using ultrasound
machines used in their normal daily practise by either
specialists in fetal maternal medicine or obstetric radiologists. The ultrasound report at the time of referral was used
for comparison and no specific proforma was used.
D RCOG 2004 Br J Obstet Gynaecol 111, pp. 784 – 792
All magnetic resonance examinations were performed on
the same standard 1.5 T clinical system (Eclipse — Philips
Medical Systems, with 27 mT/m gradients) using Single
Shot Fast Spin Echo (SSFSE) sequences to produce highresolution T2-weighted images obtained in short scan
times. The protocol consisted of twenty 5-mm-thick SSFSE
images (TR 24,000 ms, TE 75 ms, echo train length 132,
field of view 25 cm, matrix 212 256, acquisition time
20 seconds) obtained in the three natural, orthogonal planes.
Those images were supplemented by twenty 3-mm-thick
SSFSE images (TR 38,000 ms, TE 156 ms, echo train
length 140, field of view 25 cm, matrix 256 256, acquisition time 30 seconds) acquired in the axial and sagittal
planes. Neither maternal sedation nor muscular blockade of
the fetus was performed in any of the cases.
A report on the magnetic resonance examination was
made within 24 hours of the magnetic resonance examination, which was prefixed by the fact that the magnetic
resonance examination had been performed as part of a research study. In cases of apparent significant disagreements
between ultrasound and magnetic resonance, the referring
ultrasonographer was contacted as soon as possible and the
in utero magnetic resonance findings were discussed.
Corroboration of the anatomical abnormalities defined
in utero was done by a variety of means appropriate to the
clinical situation. All fetuses aborted or stillborn later in
pregnancy had autopsy and/or postmortem magnetic resonance imaging. Postmortem magnetic resonance appears
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E.H. WHITBY ET AL.
Table 2. A histogram showing the number of cases falling into each of the outcome categories defined in the table below and in the text. Categories 3 and 4
include cases (35%) in which in utero magnetic resonance was judged likely to have had an effect on clinical management. In some cases, this was due to the
in utero magnetic resonance detecting abnormalities not possible to detect by ultrasound for technical reasons.
Group
No. of cases
1. Magnetic resonance ¼ ultrasound
2. Magnetic resonance additional information
3. Magnetic resonance additional information
that could have helped/altered management
4. Magnetic resonance changed the diagnosis
5. Ultrasound additional information to magnetic resonance
6. Magnetic resonance gave incorrect diagnosis
to be a robust method of obtaining information on structural fetal CNS abnormalities.6,7 In cases where the pregnancy continued to term, postnatal clinical examination was
performed along with appropriate neuroimaging. Autopsy information was obtained in the few cases that died in the neonatal period. From those definitive diagnoses, the cases were
grouped into one of five categories depending on the antenatal ultrasound and in utero magnetic resonance findings:
1. Ultrasound and magnetic resonance gave comparable
results and agreed with the final diagnosis.
2. The diagnosis was not fundamentally changed but
magnetic resonance provided extra information that
would not have affected management or counselling.
3. The diagnosis was not fundamentally changed but
magnetic resonance provided extra information that
could have affected management or counselling.
4. The diagnosis was changed on the basis of magnetic resonance imaging and found to be correct in the final analysis.
5. Any case in which ultrasound provided more information than magnetic resonance.
6. Magnetic resonance gave incorrect information.
RESULTS
The 100 fetuses reported here were taken from a group
of 101 women referred for the study. We acknowledge that
this is a selected group where there have been difficulties
52
13
6
29
0
0
establishing a definitive diagnosis at ultrasound for patient or
technical factors. However, this is the group that in utero
magnetic resonance will be used for in clinical practice
(Table 4a and b). Weight range 50 – 135 kg, mean of
73.9 kg. The position of the fetus was variable as expected
Table 3. Number of cases where the magnetic resonance and ultrasound
were in agreement (Table 3a, group 1) or the additional information obtained
from the ultrasound did not affect management (Table 3b, group 2).
Categorised by referring diagnosis.
a. Cases where the ultrasound and magnetic resonance were in
agreement (Group 1).
Suspected diagnosis or reason for referral
Hypogenesis or agenesis of the corpus callosum
Ventriculomegaly
Cerebellar or posterior fossa abnormality
Family history of previous fetal abnormality
Microcephaly
Other (includes abnormal shaped head,
PROM, midline clefts, cortical dysplasia)
No. of cases
4
19
6
8
5
10
b. Cases where magnetic resonance gave additional information,
(Group 2).
Abnormality
Hypogenesis or agenesis of the corpus callosum
Ventriculomegaly
Cerebellar abnormality or posterior fossa abnormality
Porencephalic cyst
No. of cases
7
3
2
1
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787
Table 4. Antenatal ultrasound, in utero magnetic resonance and final diagnosis for each case where the in utero magnetic resonance provided clinically
useful information (Table 4a, group 3) or changed the diagnosis (Table 4b, group 4).
Case: Gestational
age at imaging
Antenatal ultrasound diagnosis
In utero magnetic resonance diagnosis
a. Cases where magnetic resonance provided clinically useful information (Group 3).
1: 21
Parietal encephalocoele
Superficial arteriovenous malformation
2: 21
Isolated mild ventriculomegaly
Ventriculomegaly, due to a germinal
matrix haemorrhage
3: 24
Lobar Holoprosencephaly
Septo-optic dysplasia, schizencephaly
4: 22
Interhemispheric cyst
Agenesis of corpus callosum
5: 33
Calcified periventricular lesion
Haemorrhage with ventriculomegaly
6: 22
Isolated mild ventriculomegaly
Ventriculomegaly and absent septum
pellucidum
Final diagnosis: method
As in utero MR: Histology
As in utero MR: US
As
As
As
As
in
in
in
in
utero
utero
utero
utero
MR:
MR:
MR:
MR:
PM
MR
US
MR
b. Cases in which in utero magnetic resonance were judged likely to have had a direct effect on clinical management which consists of cases where
in utero magnetic resonance provided extra information to the antenatal ultrasound (Group 3, a) and cases where the diagnosis was changed by
in utero magnetic resonance (Group 4, b).
7: 22*
Isolated mild ventriculomegaly
Ventriculomegaly, ACC and
As in utero MR: PMMR, autopsy
interhemispheric cyst
8: 21*
Isolated mild ventriculomegaly
Semilobar holoprosencephaly
As in utero MR: autopsy
9: 35
Ventriculomegaly, ACC
Ventriculomegaly, and periventricular
As in utero MR: US
leukomalacia
10: 36
Asymmetric ventriculomegaly
Hemimegalencephaly
As in utero MR: MR
11: 32
Isolated mild ventriculomegaly
Ventriculomegaly and parenchymal
As in utero MR: repeat US
haemorrhage
at 33 weeks
12: 36
Isolated mild ventriculomegaly
Ventriculomegaly and Sinus thrombosis,
As in utero MR: MR
venous infarctions
13: 25*
Talipes, normal brain
Bilateral band heterotopia
As in utero MR: autopsy
14: 21
Isolated mild ventriculomegaly
Ventriculomegaly, ACC
As in utero MR: MR
15: 36
Dandy-Walker malformation
ACC, ethmoidal encephalocoele
As in utero MR: MR
16: 30
Isolated ventriculomegaly
Ventriculomegaly, Dandy-Walker
Dandy-Walker, polymicrogyria: MR
malformation
17: 24
Occipital encephalocoele
Meningocoele, normal brain
As in utero MR: clinical and MR
18: 22*
Isolated mild ventriculomegaly
Ventriculomegaly, Vein of Galen aneurysm
As in utero MR: autopsy
19: 23*
Isolated mild ventriculomegaly
Ventriculomegaly, ACC
As in utero MR: PMMR, autopsy
20: 23*
Dandy Walker variant
Dural fistula, massive torcula
As in utero MR: PMMR, autopsy
21: 33*
Isolated severe ventriculomegaly
Ventriculomegaly, Ruptured arteriovenous
As in utero MR: PMMR, autopsy
malformation
22: 25
Isolated severe ventriculomegaly
Ventriculomegaly, parenchymal
Follow up US
haemorrhage
23: 31*
Isolated mild ventriculomegaly
Ventriculomegaly, ACC
As in utero MR: PMMR, autopsy
24: 20*
Isolated severe ventriculomegaly
Al lobar holoprosencephaly
As in utero MR: PMMR, autopsy
25: 20
Isolated mild ventriculomegaly
Normal
Normal: Clinical and MR
26: 16
Isolated borderline ventriculomegaly
Normal
Normal: Clinical and MR
27: 36
Dandy-Walker malformation
Normal
Normal: Clinical and MR
28: 27
ACC
Normal
Normal: Clinical and MR
29: 29
Dandy-Walker malformation
Normal
Normal: Clinical and MR
30: 20*
Small occipital encephalocoele
Normal brain, scalp dermoid
As in utero MR: MR and histology
31: 30
Dandy-Walker malformation
Normal
Normal: Clinical and MR
32: 32
ACC
Normal
Normal: Clinical and MR
33: 23
Frontal encephalocoele, Normal brain
Normal
Normal: Clinical and MR
34: 29
ACC, interhemispheric cyst
Normal
Normal: Clinical and MR
35: 31
Small frontal encephalocoele
Normal
Normal: Clinical and MR
In these cases the in utero magnetic resonance was shown to be correct by the specified corroborative method: A ¼ autopsy; PMMR ¼ postmortem magnetic
resonance imaging; CE ¼ clinical examination; MR ¼ postnatal magnetic resonance imaging; US ¼ follow up ultrasonography (in utero or postnatal). ACC
in the diagnosis columns stands for agenesis of the corpus callosum. Mild ventriculomegaly 15 mm, severe ventriculomegaly 15 mm.
* Patients had a termination of pregnancy.
at different gestational ages. In three cases in the third
trimester the unfavourable position of the fetus was partly
responsible for the referral for magnetic resonance. In the
second trimester, repeat ultrasound was used for unfavourable position of the fetus and this did not account for any
D RCOG 2004 Br J Obstet Gynaecol 111, pp. 784 – 792
referrals for magnetic resonance unless there were additional
uncertainties.
One woman was claustrophobic and would not enter the
scanner. The gestational ages of the 100 women at the time
of magnetic resonance imaging are shown in Table 1.
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E.H. WHITBY ET AL.
Fig. 1. In utero magnetic resonance imaging of the brain at 20 weeks of gestation. (a) Ultrasound scan demonstrating the suspected occipital
encephalocele. (b) Axial section in utero magnetic resonance and (c) parasagittal section SSFSE images show that the calvarium is intact and the brain is
normal. There is a 6 mm swelling in the subcutaneous tissues in the occipital region (arrowed). At birth the region corresponded to a hairless patch on the
scalp. The swelling was removed at 12 months of age after imaging confirmed no intracranial involvement and a diagnosis of a dermoid was made on histology
(case 30, Table 4b).
In utero magnetic resonance imaging produced examinations of good diagnostic quality in all cases. The median
table occupancy time was 20 minutes; interquartile range
9 minutes (16 –25 minutes). Table 2 shows the distribution
of cases into the six categories based on comparison of the
results of antenatal ultrasound and in utero magnetic
resonance with the definitive diagnoses.
Groups 1 and 2
Table 3a and b summarises the findings of cases falling
into groups 1 and 2.
In 52 cases, the in utero magnetic resonance and antenatal
ultrasound agreed (group 1) and in 51/52 those diagnoses
agreed with the definitive diagnoses. In 1/52 both antenatal
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ultrasound and magnetic resonance demonstrated a DandyWalker malformation, confirmed ex utero, but did not detect
the bilateral frontal polymicrogyria shown on postnatal
magnetic resonance imaging (Fig. 3). In 13 cases, in utero
magnetic resonance provided extra information over the
ultrasound (all confirmed by the definitive diagnosis) but
were judged not to have had any direct influence on clinical
management (group 2).
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Groups 3 and 4
Table 4a and b summarises the findings of groups 3 and 4
in which magnetic resonance was judged to have an effect on
clinical management. Two cases are shown in Figs 1 and 2.
In six cases, in utero magnetic resonance provided
sufficient extra information to have had an effect on
clinical management (group 3, Table 4a), all of which
Fig. 2. This case is the only one of the 100 in which the in utero magnetic resonance did not show the full abnormality when compared with postnatal
imaging. The fetus was scanned at 19 weeks of gestation and was reported as normal. The mother was re-examined at 30 weeks because of reduced
movements. This showed the features of a Dandy-Walker malformation, which was confirmed on in utero magnetic resonance (a, b) and subsequently on
postnatal imaging. (Dandy-Walker malformation: cystic dilatation of the fourth ventricle, enlarged posterior fossa and hydrocephalus). However, postnatal
imaging showed bifrontal polymicrogyria (c) not shown on the antenatal ultrasound or in utero magnetic resonance.
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E.H. WHITBY ET AL.
Fig. 3. In utero magnetic resonance demonstrating agenesis of the corpus callosum. (a) Coronal section: the absence of the bridge between the two
hemispheres. (b) Sagittal section: the corpus callosum is absent.
were corroborated by the definitive diagnoses. In 29 cases,
in utero magnetic resonance imaging changed the diagnosis (group 4, Table 4b), which were confirmed by the
corroborative methods. In no cases did ultrasound show
true positives that were not shown on magnetic resonance
(group 5), or magnetic resonance provide an incorrect
diagnosis (group 6). The diagnostic ability of in utero magnetic resonance, in cases where there were difficulties with
the ultrasound, is high and in this population could
have helped clinical management in 35% (groups 3 and 4).
In 11 cases (in group 4), the ultrasound examination
suggested possible brain abnormalities that were not con-
firmed on in utero magnetic resonance or on the definitive
diagnoses (cases 25 –35). In at least two of these cases the
parents had decided on termination if the magnetic resonance confirmed the ultrasound findings. They continued
the pregnancy after the magnetic resonance.
DISCUSSION
In this article, we have described our experience in evaluating a new magnetic resonance method designed to assess
fetal brain abnormalities (in a selected group) against the
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ULTRASOUND VERSUS MRI IN PREGNANCIES WITH SUSPECTED ABNORMALITIES
current clinical reference standard — antenatal ultrasound.
We previously reported the first 20 brain and spine anomalies performed in our unit using a similar, but lower
resolution magnetic resonance method.5 In that article we
showed disagreements between the magnetic resonance
and ultrasound findings in 40% of cases and magnetic
resonance was shown to be correct on detailed postnatal
follow up. A number of criticisms could be made against
that study, significantly, the women studied were comparatively late in pregnancy at the time of magnetic resonance.
Ideally, we would like to be able to have the information
before 24 weeks. There is no doubt that a biased population
was investigated in the earlier study as the ultrasonographers referred their difficult cases that could exaggerate the
possible benefit of magnetic resonance. In the present
study, we have attempted to correct for some, but not all,
of those shortcomings as well as increase numbers and
improve our magnetic resonance methodology. Almost half
(48) of the cases in the present study were imaged earlier
than 24 weeks of gestation, one as early as 16 weeks. We
do not advocate scanning that early based on our continuing
experience and consider 20 weeks to be the earliest time
that magnetic resonance can be performed reliably. Just
over half of the cases (52) were imaged after 24 weeks in
the present study.
We have not been able to address the issue of selection
bias in this study. A completely unbiased study would consist of performing magnetic resonance on every fetus who
had a detailed anomaly ultrasound scan or at least all those
where a brain abnormality was detected. This was not the
case. The fetal anomaly experts referred cases where there
were difficulties with the antenatal ultrasound for technical
or patient related reasons. We would argue that the distribution of the problems in this study is a fair representation
of those that would be referred if in utero magnetic resonance were available in clinical practice.
The case for improved diagnostic ability in delineating
CNS abnormalities by in utero magnetic resonance is compelling in this subgroup of patients, based on our results
reported here and in the evolving related literature.8 – 10 In our
present study, we have not been able to assess the direct
effects of magnetic resonance on clinical management. The
primary reasons for this was the ethical issue concerning use
of data from a non-proven method (in utero magnetic
resonance11) in a clinical setting. In this study, we can only
report the effects the new technique might have on clinical
management as observed by the authors and this could have
introduced bias into the 35% of cases where management
could have been altered by performing new in utero magnetic resonance technique. It is possible that a prospective
study of independent fetal anomaly experts using an ‘intention-to-treat ’ basis may be the only way to eliminate this
form of bias. However, the major differences between
ultrasound and magnetic resonance reported in this study
indicate that there is a role for in utero magnetic resonance in clinical practice. There are no known risks of
D RCOG 2004 Br J Obstet Gynaecol 111, pp. 784 – 792
791
in utero magnetic resonance but it is essential that the
specific absorption ratio (a measure of heat dissipation in
the tissues) and number of sequences obtained is kept as
low as possible.
We need to further evaluate the role of in utero magnetic
resonance in detecting brain malformations. We do not advocate that magnetic resonance should become the screening
method for all pregnancies but should be reserved for further assessment of difficult suspected abnormalities defined
by ultrasound. It is likely that the ultrasound diagnosis
of isolated ventriculomegaly should be supplemented by
in utero magnetic resonance. The observation that half of
the cases listed in Table 4a and b were ultrasound diagnosed
isolated ventriculomegaly and the range of true abnormalities described in in utero magnetic resonance attest that this
is a group where in utero magnetic resonance is clinically
very helpful and often diagnoses of the cause of ventriculomegaly was not apparent on ultrasound due to the limitations of the technique. Similarly for abnormalities of the
posterior fossa or the corpus callosum (Fig. 3) as in utero
magnetic resonance allows direct visualisation of structures
in the midline in the sagittal plane. It is also likely that
in utero magnetic resonance in the later stages of pregnancy
will detect cortical abnormalities not possible to detected by
ultrasound.
In 11 of the 35 cases where magnetic resonance could
have affected clinical management were ultrasound false
positives (i.e. the brain was normal). It is not possible to
conclude what would have been the outcome in these
patients but we are aware that at least two were considering
termination. It is likely that in some of the cases the referral
was due to parental anxiety after an ultrasound abnormality
was suggested even if a further examination had failed to
confirm this, unfortunately, this information was not available to us and we have used the referring ultrasound reason
in our analysis.
Despite the bias and the above assumptions, we suggest
that in cases where there are diagnostic difficulties at
ultrasound due to patient size, gestational age, fetal lie
and technical limitations in utero magnetic resonance
should be considered.
CONCLUSION
In utero magnetic resonance is a tertiary referral centre
technique where, if the diagnosis by ultrasound is restricted
either by patient or by technical factors, additional information may be obtained that could influence patient management. In this study, we have shown that in such a subgroup of
patients with CNS anomalies, in utero magnetic resonance
provided additional information in 48%. Some of these
findings may be inferred from the ultrasound but if confirmation is obtained by in utero magnetic resonance we may
see benefits in patient management, reduction in parental
anxiety and costly medico-legal cases may be avoided.
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E.H. WHITBY ET AL.
Acknowledgements
The authors would like to thank SPARKS, Sir Jules Thorn
and The United Sheffield Hospitals Special Trustees for
financial support of EW and the project; the five referring
hospitals, Leeds General Infirmary, The City Hospital
Nottingham, Jessop Wing Sheffield, St Mary’s Hospital
Manchester and Hull; the Radiographers at the University of
Sheffield for scanning the patients; and Barbara Skevington
for arranging appointments and sorting the paper work.
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