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UROGENITAL

Magnetic resonance imaging of clinically stable late


pregnancy bleeding: beyond ultrasound
Gabriele Masselli & Roberto Brunelli &
Tiziana Parasassi & Giuseppina Perrone &
Gianfranco Gualdi
Received: 28 December 2010 / Accepted: 23 February 2011 / Published online: 12 April 2011
# European Society of Radiology 2011
Abstract
Objectives To compare the accuracy of magnetic resonance
(MRI) and colour Doppler-ultrasound (US) in the diagnosis
of late pregnancy bleeding and to assess the accuracy of the
different MR sequences in visualizing the origin of
haemorrhage.
Methods 42 patients in the third trimester of pregnancy
underwent to US and MRI for the evaluation of painless
vaginal bleeding. Multiplanar HASTE, True Fisp, 3D T1
GRE and sagittal DWI sequences were acquired. Two
radiologists, blinded to the results of US, reviewed each
case, resolving by consensus any discrepancy. Reference
standards were surgical and pathological findings.
Results The reference standards identified 22 placenta
previa, 11 placental abruptions (1 coincident with a
placental chorioangioma), 1 thrombohaematoma and 1
fibroma with haemorrhagic degeneration. MRI identified
correctly all these condition with an interobserver agree-
ment of 0.955. DWI and T1 weighted sequences were
statistically superior to Haste and True Fisp sequences in
detecting the cause of bleeding (p<.001). US had 6 false
negatives and 2 false positive results, its diagnostic
accuracy resulting lower than MRI (p=.001).
Conclusions MRI accurately evaluates pregnancy bleeding
with an excellent interobserver agreement and can grant
new and additional data when US is negative.
Keywords Late pregnancy bleeding
.
Magnetic resonance
.
Obstetric hemorrhage
.
Placental abnormalities
.
Placenta
hematoma
Introduction
Obstetric haemorrhage is still one of the leading causes of
maternal mortality and morbidity and causes many diag-
nostic and management dilemmas for the obstetrician [1].
Of note, optimal management of late pregnancy bleeding
relies on an accurate identification of the cause and a
specific and timely intervention [2].
Placental abnormalities are major contributors to
obstetric haemorrhage [3]; common abnormalities in-
clude placenta previa, placental abruption, placenta
adhesive disorders (accreta, increta, percreta) and vasa
previa [4].
Ultrasound (US) is the mainstay of fetal and placental
imaging in the antepartum period [5]; however, despite
constant improvements in US technology over last years,
the diagnostic US sensitivity for detecting bleeding is still
low and has not significantly improved [6].
Magnetic resonance imaging (MRI/MR) is increas-
ingly considered after negative US in several maternal
disease during pregnancy [711]. MRI offers multiplanar
imaging capabilities, a wide field of view, a high soft
G. Masselli (*)
:
G. Gualdi
Radiology Dea Department, Umberto I Hospital,
Sapienza University,
Viale del Policlinico 155,
00161 Rome, Italy
e-mail: gabrielemasselli@libero.it
R. Brunelli
:
G. Perrone
Department of Gynecology and Obstetrics, Umberto I Hospital,
Sapienza University,
Viale del Policlinico 155,
00161 Rome, Italy
T. Parasassi
Institute of Neurobiology and Molecular Medicine,
National Research Council, Via del Fosso del Fiorano 64,
Viale del Policlinico 155,
00143 Rome, Italy
Eur Radiol (2011) 21:18411849
DOI 10.1007/s00330-011-2120-8
tissue contrast and the ability to highlight blood and
therefore may be superior to US in detecting intrauterine
haemorrhage.
The purpose of this study was to evaluate accuracy of
MRI and colour Doppler US in diagnosing late pregnancy
bleeding and to assess the accuracy of the different MR
sequences in visualizing intrauterine clots.
Materials and methods
This study protocol was approved by our institutional
review board. Written informed consent was obtained from
all patients included in the study.
Inclusion Criteria was the evidence of grade 1 painless
vaginal bleeding (normal haemodynamic status of the
mother and normal fetal heart rate) without uterine tetany
and tenderness in patients with a gestational age between
23 and 38 weeks. Exclusion Criteria were the presence of
common contraindications to MR imaging (pacemaker,
metallic foreign bodies, and claustrophobia).
Between May 2009 and December 2010, 44 patients were
referred by the department of perinatal medicine to undergo
colour Doppler US and MR examinations with the targeted
purpose of identifying the cause of painless vaginal bleeding.
In 2/44 patients MRI was not performed due to
claustrophobia.
42 patients [mean gestational age 30.3 weeks (SD
3.3 weeks; median, 30.8 weeks; range, 2437 weeks)
(mean age 31 years; range 2238 years)] were ultimately
included in the study.
In all patients, US and MRI studies were completed
within 24 h from admission.
In all patients, both transabdominal and transvaginal US
were performed using a Siemens Sonoline Elegra (Siemens,
Issaqua, WA, USA) ultrasound equipment. Patients were
asked to void before the examinations.
In all cases, both grey scale B mode and colour Doppler
flow were used; Doppler power settings were at the level
approved for fetal use.
Magnetic resonance imaging was performed at 1.5 T
(Magnetom Avanto. Siemens Medical Solution, Malvern,
PA, USA) equipped with high-performance gradients and
phase array coils.
Patients were supine, with their feet entering the magnet
bore first to minimize feelings of claustrophobia. Breath-
holding by the mother was utilized to minimize respiratory
motion artifact. Sagittal, coronal and axial Steady State
precession, T2-weighted single-shot fast spin-echo sequen-
ces and T1-3D GRE with Fat Sat were acquired. T1-
weighted sequences were acquired using fat-suppression
technique to increase contrast and reduce artifacts caused
by respiration and other motion. DW images were obtained
in the sagittal plane by using a multisection fast spin-echo
echoplanar sequence (Table 1).
Imaging sequences with high temporal resolution and
good contrast-to-noise ratios, such as SSFSE and steady-
state free-precession gradient-echo sequences, were
Table 1 Magnetic resonance imaging parameters
Parameter True fast-imaging sequence
(True FISP)
a
T2 Half-Fourier sequence (HASTE)
b
T1 3D sequence (VIBE)
c
DWI
d
Axial Coronal/Sagittal Axial Coronal/Sagittal Sagittal/Axial/Coronal Sagittal
Repetition time/echo
time (msec)
4.3/2.2 4.3/2.2 1000/90 1000/90 4.1/1.1 3200/75
Flip angle (degrees) 50 50 150 150 10 10
Field of view (mm) 320400 320400 320400 320400 320400 320400
Matrix 256224 256224 256224 256224 256224 256192
Parallel imaging factor 2 2 2 2 3 2
Section thickness (mm) 5 5 4 4 2.5 5
Intersection gap (mm) 0 0 0 0 0 0
NEX 1 1 1 1 1 6
Receiver Bandwith 125 125 200 200 310 1930
Acquisition Time (sec) 19 21 1520 1520 1518 180
a
The true fast imaging sequence is the true fast imaging with steady-state free precession sequence
b
The T2 half-Fourier sequence is the T2-weighted half-Fourier acquisition single-shot turbo spin-echo
c
The T1 three-dimensional (3D) fat-saturated sequence is the T1-weighted dynamic volumetric interpolated breath-hold examination (VIBE) with
fat saturation sequence. Fat saturation was achieved with the chemical shift-selective fat suppression technique
d
DWI was acquired with b values of 50, 400 and 800 s/mm
1842 Eur Radiol (2011) 21:18411849
acquired. Parallel Imaging reconstruction algorithms
GRAPPA with iPAT factor 2 were used to decrease the
MR data acquisition time of the sequences therefore
reduce foetal and maternal motion artefact.
To minimize the deposition of radiofrequency energy in the
pregnant patient and optimize temporal resolution, a 256224
matrix is used with a partial-phase field of view of 0.75 in
applicable rectangular geometries, such as the axial plane.
Imaging analysis
All US examinations were performed by an obstetrician with
20 years of experience in obstetrical US, who was aware that
the examination was dictated by the presence of vaginal
bleeding. Placenta previa, assessed by transvaginal examina-
tion, was categorized as complete partial, marginal or low
lying [12]. Abruption was diagnosed when in presence of
preplacental fluid collection between the placenta and
amniotic fluid, Jello- like movement of the chorionic plate
induced by fetal activity, presence of marginal, subchorionic,
or intraamniotic haematoma(s) and increased heterogeneous
placental thickness (>5 cm in a perpendicular plane) [13].
Other pathological conditions such as vasa previa or
placental adhesive disorders were also assessed [14, 15].
For MR image analysis, two radiologists assessed the
data during two separate imaging analysis by using a
Table 2 Summary of diagnostic performance of US and MR (two independent readers and consensus) for detecting the correct diagnosis of
pregnancy bleeding
US Reader 1 MR Reader 2 MR Consensus MR
True positive - n 29 35 34 35
False negative - n 6 0 1 0
True negative - n 5 7 7 7
False positive - n 2 0 0 0
Sensitivity-%(95%CI) 82 (30.175.1) 100 (100100) 97 (84.6100) 100 (100100)
Specificity-%(95%CI) 71 (69.4100) 100 (100100) 100 (100100) 100 (100100)
PPV -% (95% CI) 93 (54.099.8) 100 (100100) 100 (100100) 100 (100100)
NPV -% (95% CI) 45 (42.183.7) 100 (100100) 87 (86.1100) 100 (100100)
Inter-observer agreement for MR detection of uterin bleeding was 0.955 k (0.8731.000 95% CI)
95% CI 95% Confidence Interval
PPV Positive predictive value
NPV Negative predictive value
k Cohens kappa statistic
Table 3 Overview of the imaging findings in 13 patients with intrauterine haematomas, thrombohaematoma and Choriangioma
Pts G age Placenta MRI US Doppler
30 Posterior Corpus Subcorionic Haematoma covering the
internal cervical os
No Haematoma
31 Anterior, fundal Subcorionic Haematoma Equal findings
31 Anterior fundal Subcorionic Haematoma Equal findings
29 Posterior fundal Subcorionic Haematoma covering the
internal cervical os
Equal findings
33 Posterior fundal Retroplacental Haematoma No Haematoma
35 Anterior fundal Subcorionic Haematoma No Haematoma
33 Posterior fundal Subcorionic Haematoma Equal findings
31 Posterior fundal Retroplacental Haematoma No Haematoma
35 Anterior fundal Subcorionic Haematoma Equal findings
35 Posterior fundal Retroplacental Haematoma No Haematoma
34 Anterior Marginal Large Fibroid with endocervical extension with
Haemorrhage and bleeding into the OUI
Large Fibroid with no evidence
of Haemorrhage and bleeding
into the OUI
35 Posterior previa thrombohaematoma Retroplacental Haematoma
24 Posterior fundal Choriangioma Preplacental Haematoma
Eur Radiol (2011) 21:18411849 1843
picture archiving and communication system (Care-
stream PACS System 5.3 sp1.1; Kodak, Rochester, NY,
USA). Both readers were blinded to all clinical data and
ultrasound imaging findings but were aware that MR
imaging had been indicated by the presence of vaginal
bleeding.
During each imaging analysis, haematomas resulting
from abruptions were diagnosed on the basis of identifica-
tion of a well marginated blood collection and classified
according to their predominant location as subchorionic
(when only the margin of the placenta was separeted),
retroplacental (when the bleeding was behind the placenta),
and preplacental (bleeding was anterior to the placenta and
limited by the umbilical cord) [16].
During the first analysis, performed promptly after the
acquisition, the two radiologists independently reviewed all
images relative to each case and assigned a diagnosis by
consensus.
During the second analysis, performed at the end of the
study, a radiology technologist presented images fromdifferent
cases in random order, and the two readers independently
reviewed the different sequences, assessing one by one their
accuracy in detecting the intrauterine origin of bleeding.
Differences in assessment were resolved by consensus.
To further reduce recall bias, this second analysis was
performed in two different reading sessions separated by a
4-week intervals, with the half of the data sets analyzed at
each session.
a
b
c
d
Fig. 1 Placental abruption in a
35 year old woman at 32 weeks
of gestational age presenting
with history of vaginal bleeding
and unremarkable US findings.
Sagittal gradient echo T1-
weighted image (a) shows a
marginal anterior haematoma
(long arrows) with blood
extending into the cervix; the
haematoma appears hyperin-
tense with respect to the pla-
centa (short arrow). Sagittal
DWI image (b) shows the
markedly hyperintense anterior
haematoma (long arrows) and
an hypointense haemorrhage
(short arrow) along the posterior
uterine surface. On sagittal T2-
weighted HASTE (c) the anteri-
or haematoma signal intensity
(long arrow) is similar to that of
the placenta, while the posterior
blood collection is hypointense
(short arrow). Axial true-FISP
sequence (d) well delineates the
posterior bleeding (long arrow)
with a low intensity peripheric
rim (short arrow). Therefore, the
different MR sequences are
complementary and are all use-
ful for a complete characteriza-
tion of existing haemorrhage
1844 Eur Radiol (2011) 21:18411849
Diagnostic accuracy of both MR and US was calculated
with reference to clinical findings at delivery or to
pathology reports.
Statistical analysis
The sensitivity (Se), specificity (Sp), positive predictive
value (PPV), negative predictive value (NPV), and
diagnostic accuracy (DA) of US Doppler and MRI in
the identification of the source of bleeding were
calculated.
The interobserver strength of agreement in the detection
of various pathologies, as well as the inter-rater agreement
between each MRI sequence (T1, Haste, True Fisp, and
DWI) were calculated by using the Cohens k pairwise
inter-test for nominal scales [17]. The strength of agreement
was considered poor for k <0.20, fair for 0.21k0.40,
moderate for 0.41 k0.60, good for 0.61k0.80, and
very good for 0.81k1.00.
All statistical evaluations were carried out by using
MedCalc Software (version 11.2.1, Mariakerke, Belgium).
Results
Among the 42 patients in our study group, 22 placenta
previa (16 complete and 6 marginal), 11 placental abrupt-
ions (7 with a subchorionic location and 4 with a
retroplacental location; of these latter 1 was coincident
with a placental chorioangioma) 1 retroplacental thrombo-
heamatoma and 1 massive fibroma with haemorrhagic
degeneration were identified. 7 patients with no abnormal
findings received a final post partum diagnosis of abnormal
bleeding of undetermined origin (ABUO).
All placenta previa were confirmed by clinical findings
during surgery. In 7 patients placental abruption was confirmed
by the clinical evidence of adherent blood clots with fibrin
deposits after the obstetricians, with more than 15 years of
experience in operative obstetrics, performed a careful
inspection of the placenta after delivery [18]. 4 abruptions
were confirmed microscopically by an experienced (more
than 25 years) pathologist, according to recognized criteria of
diagnosis [19]. Thromboematoma was scored when in
presence of a large subchorionic laminated thrombosis [20].
The reported chorioangioma showed degenerative changes
including infarction and extensive thromboses.
Time interval between the MR examination and delivery
was 7 days (range, 125 days; SD 8 days).
The diagnostic performance of US and MR imaging for
detecting the origin of bleeding is reported in Table 2.
US had 6 false negatives and 2 false positive results, its
diagnostic accuracy resulting lower than that of MRI (p=.001).
US failed to identify the origin of bleeding in 1 case
presenting with a haemorrhagic degeneration of a large
a
b
c
d
Fig. 2 Placental choriangioma
in patient at 24 weeks of gesta-
tional age and profuse vaginal
bleeding. US (a) showed the
presence of a well defined
hypoecogenic mass (arrow) on
the fetal surface of the placenta
with no evidence of significant
vascularization on Doppler; Us
findings were suggestive of pre-
placental haematoma. Axial
T2-weighted HASTE (b) and
sagittal TRUE-FISP (c) images
showed an intrauterine mass
peripherally located and pro-
truding from the fetal surface of
the placenta. Note the posterior
hypointense retroplacental
haematoma (short arrows in c).
Coronal T1 GRE (d) sequence
showed the retroplacental blood
extending to the cervix (short
arrows) and the placental
vascular lesion (long arrow)
with a central hyperintense area
Eur Radiol (2011) 21:18411849 1845
fibroma and in 5 of haematomas (2 subchorionic, 3
retroplacental) resulting from placental abruptions. US also
had 2 false positives, scoring as retroplacental and
preplacental haematomas 1 case of thrombohaematoma
and 1 chorioangioma, respectively (Table 3).
MR consensus review led to the correct identification
of all the identified origins of bleeding as well as of all
cases of ABUO. Sensitivity of MR examination was
100% and 97% for readers 1 and 2, respectively, the
second reviewer missing the presence of one placental
abruption.
In particular, MR allowed the detection of vaginal
bleeding due to placental abruptions, either isolated
(Fig. 1) or concomitant with chorioangioma (Fig. 2), and
to thrombohaematoma (Fig. 3).
US and MRI showed the same accuracy in detecting
patients with placenta previa. However, with reference to
these cases of previa, MR showed the presence of
subplacental haemorrhage in 13/22 cases of placenta previa
(Fig. 4); only 5 of these 13 haemorrhagic processes were
pointed out by US.
Of note, new episodes of vaginal bleeding occurred more
frequently in cases with a visualized haemorrhages (8/13)
than in those where this evidence was absent (3/9).
During the second reading session, DWI and T1-
weighted sequences were more accurate than Haste and
True Fisp sequences in detecting the presence of bleeding
(p<00.1), as they allowed the identification of the origin of
vaginal bleeding in 35 (100%) and 32 (91%) cases,
respectively (Table 4).
Discussion
Antepartum haemorrhage remains an important cause of
maternal and fetal morbidity and mortality [3]. Placenta
a b
c
Fig. 3 Thrombohaematoma in a
35 year old woman at 34 weeks of
gestational age with vaginal
bleeding. Sagittal HASTE (a) and
Sagittal True FISP (b) sequences
showed an area (arrows) with a
heterogeneous signal and layered
appearance below to the placen-
ta. c Sagittal T1- image showed
an area (arrow) hyso-intense to
the placenta and a hyperintense
signal collection (short arrow)
into the cervix due to small
haemorrhage. Massive
thrombohaematoma was found
at delivery
1846 Eur Radiol (2011) 21:18411849
previa and placental abruption account for more than one
half of cases of antepartum haemorrhage and are increasing
in prevalence as the rate of cesarean section increases [2].
Additionally, differential diagnosis of rare causes of
bleeding (vasa previa, fibroid degeneration, cervical abnor-
malities and placental tumours) is important to select the
optimal management, representing an invaluable informa-
tion for the clinician.
Diagnostic imaging should be performed with minimal
risk for to both the mother and the developing fetus;
therefore, US represents the mainstay of ante partum
diagnosis [5, 6].
a
b c d
Fig. 4 Placenta previa in a
32 year old woman at 33 weeks
of gestational age presenting
with vaginal bleeding. Sagittal
US (a) shows symmetric com-
plete placenta previa. The pla-
centa is implanted in the lower
uterus. Sagittal T2-weighted
True-FISP (b) show the placenta
(long arrows) centered over the
internal os (short arrow), a
location consistent with a diag-
nosis of complete placenta pre-
via. Sagittal T1 GRE (c) and
DWI sequence (d) show a small
amount of haemorrage (short
arrows) between the placenta
and the internal os. The placenta
shows normal signal intensity
(long arrows)
Table 4 Diagnostic efficacy of the different MR sequences in identifying the cause of late pregnancy bleeding
SeSE (95% CI) SpSE (95% CI) PPVSE (95% CI) NPVSE (95% CI)
MR T1-w 91.46.5 (83.2105.0) 100.00.0 (100.0100.0) 100.00.0 (100.0100.0) 70.24.7 (86.1104.3)
MR Haste T2-w 82.811.4 (61.595.8) 100.00.0 (100.0100.0) 100.00.0 (100.0100.0) 53.37.6 (68.498.2)
MR True Fisp sequence 85.710.3 (69.8100.5) 100.00.0 (100.0100.0) 100.00.0 (100.0100.0) 58.07.0 (73.3100.7)
MR DWI sequence 100.00.0 (95.0100.0) 100.00.0 (100.0100.0) 100.00.0 (100.0100.0) 100.00.0 (100.0100.0)
All values in table are expressed as percentages (%)
Se sensitivity; Sp specificity; PPV positive predictive value; NPV negative predictive value; SE standard error; 95% CI, 95% confidence interval
Eur Radiol (2011) 21:18411849 1847
However, since the haemorrhage echo texture is frequently
similar to that of the adjacent placenta [13] and blood often
drains through the cervix [21], it is often difficult, regardless
the use of colour Doppler, to identify both the source and the
extent of bleeding when using ultrasound.
MR imaging might well have a pivotal role in the
diagnosis of intrauterine bleeding thanks to its high
spatial resolution, improved soft tissue contrast and to
the known high sensitivity and specificity in distinguish-
ing blood from other fluid collections [2224]. More-
over, MR has a larger FOV and is less operator dependent
than US; however, it is limited by cost, patient claustro-
phobia, and limited availability.
In our study, we confirmed the poor sonographic
detection of abruption [13] and corroborated previous
evidence, obtained in a short series of 5 patients, of the
value of MR in assessing intrauterine bleeding in patients
with abruption and ultrasound negative findings [25].
Interestingly, in one case, not only was the retroplacental
haematoma missed by US but a coexistent chorioangioma
was scored as preplacental haematoma. A reasonable
explanation of the misinterpretation was offered by the
pathology report of extensive thromboses within the
tumour. Thromboses of the capillary and sinusoidal vessels
hindered the typical US evidence of substantial internal
vascularity or of a large feeding vessel within the tumor
[26] and could also explain the lack of development of any
feto-maternal symptomatology including hydramnios, fetal
growth restriction and cardiogenic hydrops [27]. The
occurrence of abruptio placentae with chorioangioma has
long been known and interpreted as dependent upon a
disruption of the decidual plate by a turbolent maternal
blood flow in the intervillous space due to the displacement
of functioning chorionic villi by the inert tissue of the
tumor [28]. In our case, confirmation that bleeding was of
maternal origin was obtained by a Kleihauer Betke that did
not show any feto-maternal transplacental haemorrhage.
In another case, an incorrect US diagnosis of massive
retroplacental haematoma was amended by MR to that of
thrombohaematoma, due to the evidence of an area with
heterogeneous signal and layered appearance below the
placenta; in this case bleeding was only observed in the
cervical canal.
The occurrence of new episodes of bleeding in
patients with previa is unpredictable, In this regard,
the evidence that MR identified many haemorrhages
missed by US that look associated to a higher risk of
recurrent bleeding seems particularly intriguing and
deserves validation on a larger scale. A possible
explanation could refer to the reported stimulatory
action of thrombin on myometrium contractility [29].
The finding that MR imaging is an extremely accurate
modality to identify intrauterine haemorrhage, modified our
management protocol of patients with late pregnancy bleed-
ing. Indeed, clinically stable patients with very pretermfetuses
are nowdischarged fromhospital after a negative US and MR,
with an assigned putative diagnosis of ABUO.
In our study the DWI and T1-weighted sequences were
extremely accurate in identifying intrauterine bleeding, well
in agreement with previously reported evidence [24, 30]
and with the notion that blood breakdown products cause
susceptibility effects accurately demonstrated by DWI [23].
Nevertheless, Haste and True Fisp sequences also showed a
very good diagnostic efficacy; this was probably due to the
coexistence of phases of haemorrhage and ischemia in
many cases of bleeding [18].
Need of a skilled image interpretation is a theoretical
limit of MR. Therefore, our reported excellent interobserver
agreement between two readers with different feto-placental
MRI expertise is an important additional finding.
In summary, MRI is an extremely accurate investiga-
tion that identifies, with an excellent inter-observer
agreement, the origin of second and third trimester
uterine bleeding: with respect to US, it grants new and
additional data that can influence the clinical manage-
ment of these patients.
Acknowledgements Scientific oral communication presented at
ECR 2010.
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