Eur Radiol (2012) 22:2020–2026 DOI 10.1007/s00330-012-2455-9
MAGNETIC RESONANCE
Magnetic resonance imaging of the active second stage of labour: Proof of principle F. V. Güttler & A. Heinrich & J. Rump & M. de Bucourt & B. Schnackenburg & C. Bamberg & B. Hamm & U. K. Teichgräber
Received: 17 November 2011 / Revised: 9 February 2012 / Accepted: 23 February 2012 / Published online: 2 May 2012 # European Society of Radiology 2012
Abstract Objective To prove that magnetic resonance imaging of foetal anatomy during the active second stage of vaginal delivery is feasible. Materials and methods Initially, five pregnant volunteers around the 30th week of gestation were examined in an open MRI. Based on the findings, one vaginal delivery was acquired under real-time imaging. To monitor the birth status during image acquisition, an MR-compatible wireless cardiotocography (CTG) system was built. Single-shot sequence parameters were optimised to compensate motion artefacts during labour. Results Safety requirements to monitor the birth process under real-time MR imaging were met. High-resolution MR images were acquired immediately before and after delivery. In one patient, TSE single-shot cinematic sequences of the active second stage of labour were obtained. All sequences were adapted to tolerate movement of the mother and infant, as well as residual noise from the CTG. Furthermore, the MR imaging during labour showed only minor image artefacts. F. V. Güttler (*) : A. Heinrich : J. Rump : M. de Bucourt : B. Hamm : U. K. Teichgräber Department of Radiology, Charité University Hospital, Charitéplatz 1, 10117 Berlin, Germany e-mail:
[email protected] B. Schnackenburg Philips GmbH Unternehmensbereich Healthcare, Lübeckertordamm 5, 20099 Hamburg, Germany C. Bamberg Department of Obstetrics, Charité University Hospital, Charitéplatz 1, 10117 Berlin, Germany
Conclusion CTG-monitored acquisition of MRI series during the active second stage of delivery is feasible. Image quality should allow various further studies to improve models for birth simulation as well as potential investigation of obstructed labour and obstetric complications. Key Points • The active second stage of obstetric delivery can be followed by MRI. • Wireless cardiotocography allows monitoring of the foetus during MRI. • It has potential applications in evaluation of late obstetric problems. Keywords Parturition . Magnetic resonance imaging . Prenatal diagnosis . Pregnancy . Obstetrics Abbreviations MRI Magnetic resonance imaging bSSFP Balanced steady-state free precession CTG Cardiotocography DAQ Data acquisition FFE Fast field echo FHR Foetal heart rate FM Foetal monitor GUI Graphical user interface GRE Gradient echo toco Tocodynamometer TSE Turbo spin echo US Ultrasound
Introduction Human childbirth is a complex, three-dimensional and dynamic process in which the foetus navigates the birth canal.
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The clinician determines foetal lie and presentation by palpation of the gravid uterus. Thorough understanding of maternal and foetal anatomy and physiology is crucial for proper management of labour and delivery. Accurate models of the underlying anatomy are necessary for correct simulations of normal deliveries [1–3] and especially imperative to derive valid predictive factors for complicated deliveries. Pregnancy and vaginal birth stretch the muscles, connective tissues and nerves. These effects can cause damage to the pelvic floor, which can lead to secondary complications such as stress urinary incontinence [4, 5]. However, further investigation is necessary to objectively assess the correlation among pregnancy, birth and damage of the pelvic floor. In case of an abnormal delay in birth, a vacuum extractor or forceps can be used, increasing however the risks of birthrelated injuries [6–8]. The reason for the delay cannot always be clearly clarified. Magnetic resonance imaging (MRI) may help to increase knowledge about the maternal and foetal anatomy and dynamics during labour. Identifying potentially hazardous effects of MRI during pregnancy has been the subject of many scientific tests: The MRI noise induced does not seem to have an effect on the infant’s hearing development [9, 10]; MRI at high field strength does not seem to influence the foetal heart rate (FHR) or contractility [11]. Furthermore, studies on embryonic, foetal and human cells [12–14] showed that no cell or growth changes occurred using MRI. Besides, continuous cardiotocography (CTG) is considered crucial during the second stage of delivery [15, 16]. However, there is still no MR-compatible cardiotocograph available on the market. The objective of this technical innovation was to develop magnetic resonance imaging during human childbirth up to the end of the second stage of vaginal delivery with modern safety standards in obstetrics, to verify if this method is applicable for the amelioration of birth simulation models as well as for further research into obstructed labour and its after-effects.
Materials and methods The institutional review board approved the study. Informed consent was obtained before the examination.
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and two wirelessly connected transmitters (transducers). An ultrasound (US) transducer was used to measure the FHR, while uterine contractions were recorded with a tocodynamometer (toco) transducer. For clinical setup during birth (Fig. 1), the CTS signal output was split to allow for a connection to a foetal monitor (Philips FM50) and the custom-made CTG. The software implemented was programmed in MathWorks Matlab (v7.9.0) with Data Acquisition Toolbox (v2.1.5), and consisted of a set of real-time filters (comb and low-pass filter), calculated functions and a graphical user interface (GUI). Concerning the CTS, the signal was read by a data acquisition (DAQ) device (Northern Instruments USB–6211, Austin, TX, USA). The DAQ was connected to a standard PC (Apple MacBook, Cupertino, CA, USA). To allow the use of active CTG transducers in the isocentre of the magnet during image acquisition, various components were modified. The magnetic power switch of the transducer was replaced with a key switch. The metalcased lithium accumulator was substituted with an equivalent lithium-polymer accumulator. Moreover, ferromagnetic components (e.g. screws) were replaced. On the toco sensor board, the pressure sensor was replaced with an equivalent nonferromagnetic counterpart (custom-made by Sensetech, Fehraltorf, Switzerland). To establish MR safety conditions [17] various tests were performed. The susceptibility artefact of the active CTS transducers was assessed with a TSE sequence (TR/TE 500/20 ms, slice thickness 5 mm, NSA 3) in copper sulphate solution according to the American Society for Testing and Materials (ASTM) F2119-01 [18]. The measurements were made with MR-susceptibility artefact measurement (SAM) [19]. The occurring magnetic attraction was determined according to ASTM F2052 [20] in a Philips Gyroscan Intera (1.5 T). The susceptibility and the SNR measurements were performed with a Philips Panorama HFO MR system (1 T) and a cylindrical BodySP-M receiver coil. The signal-tonoise ratio (SNR) was determined for a TSE sequence (TR/ TE 600/10 ms, slice thickness 5 mm, NSA 1) and FFE sequence (TR/TE 12/7 ms, flip angle 15 °, slice thickness 8 mm, NSA 2). The SNR was calculated from the mean signal of the phantom divided by the standard deviation of the signal in air in a total of three MR images of each sequence [21]. Preparation of the birth process
Development of MR-compatible cardiotocography A wireless cardiotocography transducer station (Avalon CTS, Philips, Eindhoven, The Netherlands) was modified to meet MR safety standards and to allow the implementation of a custom-made CTG software to filter MR noise from the sensor signals. The CTS consists of a base receiver
All foetal MR images from preliminary experiments and from birth were acquired on a Philips Panorama HFO MR system using a cylindrical Philips BodySp-XL receiver coil. Five pregnant volunteers (around the 30th week of gestation) were examined by MRI to clarify three focal points of childbirth preparation.
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Fig. 1 Magnet room (left) and basic setup (right) during birth: in-room monitors show the MR controller (MRC) and recalculated CTG. The transducer signal (US) was transmitted to the in-room antenna
connected to the base station (CTS). The signal was split to a backup foetal monitor (FM) and the custom-made CTG
1. The first key aspect was to find a suitable positioning of the pregnant woman with good accessibility for the obstetricians and the possibility of quick evacuation of the volunteer with child from the magnet room providing medical treatment in the control room. 2. The second focal point was planned to test the MRcompatible CTG on pregnant volunteers after the successful verification of the MR safety. Not only the stability and reliability of the system were checked, but also the optimal filter setting for the sequence to be developed for point 3 was evaluated. 3. The last focal point was to develop a dynamic sequence for the birth with the aid of the pregnant women. In this process single-shot TSE and TSE sequences with a TR between 1,000-2,500 ms, as well as GRE sequences with a TR between 5-150 ms were analysed. To reduce the volume of the sequences the “SofTone mode” parameter was activated.
6 mm with 1-mm gap, voxel size 1.4×1.6 mm, FOV 300× 262 mm). Thereafter, continuous MR images were acquired from the midsagittal plane for cinematic representation of the second stage of labour using an interactive single-shot TSE sequence (TR/TE 1,600/150 ms, ETL 125, DRIVE pulse, single slice of 6 mm, pixel size 1.4×1.5 mm, FOV 380×285mm). The newborn was taken outside the magnet room for the initial medical checkup. After the placenta was expelled, the third stage of labour was recorded with a multislice bSSFP sequence (TR/TE 6/3 ms, flip angle 60 °, 26 slices of 6 mm with no gap, voxel size 2.0×2.0 mm, FOV 340×340 mm).
General MR-compatible instruments typically used in obstetrics were provided to enable interventions inside the magnet room. Furthermore, an MR-compatible blood pressure monitor was available. The MRI, the receiver coil and the gurney were covered with protective sheeting to prevent fluid leakage. Further equipment was arranged in the control room for the first visit of the newborn and for an eventual emergency.
During the development process, two prototypes were designed. The real-time filters allowed separation of the signal from the MR-induced noise during image acquisition; the GUI (Fig. 2) visualised the current heart rate and uterine contractions and their course over 15 min using a scroll function at a rate of about 1 cm/min and a resolution of 675 pixels. The artefact size of the unmodified transducers could not be determined as the MRI was not able to detect any signal. Only after the modification could the artefacts be measured. The maximum artefact size of the transducers was 7.7 cm from the device boundary to the fringe of the artefact. The magnetic attraction acting on the 107 g US transducer and of the 105 g toco-transducer was reflected in a displacement of the transducer of 21 ° and 11 ° at 2.4 T/m. In a worst case
Visualisation of the birth process For anatomical orientation sagittal, coronal and transverse MR images were acquired with a multislice single-shot TSE sequence (TR/TE 1,000/100 ms, ETL 122, 40 slices of
Results Development of MR-compatible cardiotocography
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Fig. 2 GUI of the CTG system, displaying the foetal heart rate (top), the uterine contractions (middle) and unfiltered signal of the ultrasound transducer in Fourier space as technical diagnostic information (bottom)
setting, the SNR of the active US transducer in the magnets isocenter was 8.5 in the TSE sequence and 12 in the FFE sequence. The active toco-transducer’s SNR was 15.5 in both sequences. Preparation of the birth process With an aperture of 160 cm between the two supporting pillars and a 45-cm space between the two magnet pole shoes, the MR enabled access not only via the conventional z-axis, but also from both sides of the gurney. For this reason, the supine position with the head in front proved to be the best birthing position. The CTG systems were used during all preliminary examinations in the experimental setup without malfunctioning. In a total of five pregnant women, more than 30 min were recorded with the modified CTG system. An MR-induced voltage was superimposed on foetal ultrasound data, precluding monitoring of FHR without filtering during MR image acquisition. The interfering voltage is generated by the radiofrequency field and time-varying magnetic gradient fields. Interferences induced by the single-shot pulse sequence could be identified in Fourier space because of marked clustering at multiples of 205 Hz. To eliminate these interferences, the comb filter was set accordingly. Relevant frequencies of foetal heart signals were predominantly found below about 250 Hz. Higher frequencies were suppressed with a low-pass filter. The toco signal was not filtered and was thus considered equivalent to that of the FM50. For the image acquisition of the birth, three sequences could be developed: a multislice single-shot TSE sequence
(TR/TE 1,000/100 ms, ETL 122), an interactive single-shot TSE sequence (TR/TE 1,600/150 ms, ETL 125) and a multislice bSSFP sequence (TR/TE 6/3 ms, flip angle 60 °). Preliminary findings on sequence optimisation confirmed that the foetal organs were large enough for adequate visualisation at 1 T and that the image quality was sufficient with respect to resolution and contrast. The single-shot TSE sequence was not degraded by any appreciable artefacts, and it was also less prone to susceptibility artefacts compared with the GRE sequence. Sequence optimisation also aimed at minimsing the sound pressure level, which was produced by the gradients in the range of 10.5-11.3 dB in the preliminary experiments and 10.8 dB during the active second stage of labour. Visualisation of the birth process The pregnant woman was kept in a supine position throughout the birth process (head first, Fig. 1). The single-shot TSE sequence (TR 1,000 ms) produced high-contrast anatomical images of labour. On the basis of these images, good positioning of the slices for the dynamic sequence could be carried out. The interactive singe-shot TSE sequence also allowed near real-time monitoring of the expulsion phase. During this phase, one MR image was acquired in 600 ms, and image acquisition was repeated every 1,600 ms. All through the second stage of labour, the interactive sequence could trace the foetal rotation and visualise the maternal anatomy (Fig. 3) including uterine contractions. The contractions help push the baby’s head through the birth canal, leading to a stretching and
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In the late second stage, as the foetal head protruded and the perineum distended, cinematic MRI acquisition was terminated to avoid foetal exposure to MRI noise. Immediately after childbirth, the maternal anatomy was imaged before and after expulsion of the placenta (Fig. 4) using a bSSFP sequence.
Discussion Development of MR-compatible cardiotocography
Fig. 3 Excerpt from the documented phase of expulsion: At the beginning of the expulsion phase (a) the child is pressed into the birth canal (b). Only after a rotation to the side can the head pass (c) and then finally emerge (d). MR images were acquired with an interactive TSE single-shot sequence (TR 1,600 ms, TE 150 ms, ETL 125, single slice of 6 mm, voxel size 1.4×1.5 mm, FOV 380×285 mm)
compression of the muscles. At the same time, the muscles are pressed into the tissue, which is compressed to less than half the original size. The increasing stretching and compression in the process of contractions were traced over time. After this, it became clear how extensively the rectum and adjacent muscles are pushed against the coccyx to enable the child to pass through the birth canal.
Fig. 4 Birth process: (a) beginning of the expulsion phase, (b) placenta after birth and (c) after labour and expulsion. MR images were acquired with a multislice TSE single-shot sequence (TR 1,000 ms, TE 100 ms, ETL 122, 40 slices of 6 mm with 1 mm gap, voxel size 1.4×
The presented study shows that continuous recording of CTG data during MR image acquisition is possible and that interactions between the MRI and the CTG system are manageable. It should however be noted that MRI can induce currents in the transducer, which in turn can impose upon the real measurements and thus falsify the recordings. The filtering developed here was not needed anymore as soon as the transducer of the CTG offered a conductive structure shield against induced voltage. For MR safety, it is indispensable to monitor the appliances and to check the instruments [22, 23]. If possible, a CTG system for MRI should not have any cable connection between the coil and body because the danger of fibrillation and combustion might be high [24]. To allow MR imaging at higher field strength, an extensive modification of the transducer is probably necessary. Preparation for the birth process The choice of birth position for open MR is possible to a certain extent. Even though other birth positions (upright, lateral position) require fewer episiotomies, less necessity to
1.6 mm, FOV 300×262 mm and a multislice balanced SSFP sequence; TR 6 ms, TE 3 ms, flip angle 60 °, 26 slices of 6 mm with no gap, voxel size 2.0×2.03 mm, FOV 340×340 mm)
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administer ocytocin and less epidural anaesthesia than the supine position, Bodner-Adler et al. showed that birth-related injuries, the postnatal condition of the baby and the duration of the stage of expulsion could not be influenced by the choice of birth position to a statistically significant extent [25, 26]. Filtering of the applied single shot TSE sequence during birth required only relatively simple filter methods, as the induced currents were almost equivalent during each image acquisition. This may differ for other types of sequences or vary with different parameter settings. The works of Levine et al. [27, 28] provide important information for optimal imaging of foetal organs. They recommended a single-shot TSE sequence, since such sequence designs are robust to movement artefacts of the foetus in the womb, and the foetal organs are imaged with sufficient contrast. Our findings support this recommendation and also indicate that single-shot TSE sequences are applicable to visualise labour and substantial movement during foetal expulsion. Three-dimensional imaging was not tested because of long acquisition times and likely resulting in image distortion. Visualisation of the birth process Interactive MR image acquisition is suitable for further research of unexplained obstructed labour and birth-related stress of organs and tissues. Thus, scientific statements [4, 5] that are based on presumptions or questionnaires can be substantiated experimentally and possibly corrected. The stress on muscles, connective tissues and nerves can be detected in time and level (stretching and contusion). There have been attempts [2, 3] to simulate the birth process according to the current ideas to show the interaction between the foetal head and the pelvic floor. However, there are complaints that experimental data and methods for clinical validation are missing. Birth under MR control showed that this method seems adequate to collect experimental data and therefore clarify open issues and further improve the modelling. Besides, the formability of the baby’s head and the adaptation of the mother’s pelvis can be studied with good soft tissue contrast. This study points out the potential of dynamic obstetric MRI. Further births under MRI control can probably only be justified to address specific issues since the applicability of this method and the basic requirements cannot be answered in a general way. At present, it does not appear reasonable to the authors to employ this experimental method as a regular monitoring of the birth process. However in the future, risky caesarean sections or women with high-risk pregnancies delivering vaginally might profit from real-time MRI, increasing the safety for both infant and mother. For these examinations, the use of an MR-compatible CTG would be imperative to permit continuous foetal monitoring.
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