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. 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