<scp>ISUOG</scp> Practice Guidelines: performance of fetal magnetic resonance imaging

Abstract

The International Society of Ultrasound in Obstetrics and Gynecology (ISUOG) is a scientific organization that encourages sound clinical practice, and high-quality teaching and research related to diagnostic imaging in women's healthcare. The ISUOG Clinical Standards Committee (CSC) has a remit to develop Practice Guidelines and Consensus Statements as educational recommendations that provide healthcare practitioners with a consensus-based approach, from experts, for diagnostic imaging. They are intended to reflect what is considered by ISUOG to be the best practice at the time at which they are issued. Although ISUOG has made every effort to ensure that Guidelines are accurate when issued, neither the Society nor any of its employees or members accepts any liability for the consequences of any inaccurate or misleading data, opinions or statements issued by the CSC. The ISUOG CSC documents are not intended to establish a legal standard of care because interpretation of the evidence that underpins the Guidelines may be influenced by individual circumstances, local protocol and available resources. Approved Guidelines can be distributed freely with the permission of ISUOG ([email protected]). These guidelines are based on consensus reached between participants following a survey of current practices, conducted by ISUOG in 2014 (Appendix S1). Fetal magnetic resonance imaging (MRI) is an important diagnostic imaging adjunct to ultrasonography1, particularly for the assessment of fetal brain development2. A survey conducted by ISUOG in 2014 (Appendix S1), in which 60 international perinatal centers participated, showed that fetal MRI is being performed in one or more centers in at least 27 countries worldwide. However, the quality of imaging, sequences used and operator experience appear to differ widely between centers3. The impact of such differences should be reduced by development of guidelines to define better the role of fetal MRI in relation to prenatal diagnostic ultrasound. The aim of this document is to provide information on state-of-the-art fetal MRI for those performing the examination, as well as for clinicians interpreting the results. The purpose of fetal MRI is to complement an expert ultrasound examination4, 5, either by confirmation of the ultrasound findings or through the acquisition of additional information6. MRI is not currently used as a primary screening tool in prenatal care, although standardized and complete assessment of the fetal anatomy is probably feasible. Figure 1 presents the survey participants' opinions regarding indications for which MRI can provide useful information. MRI is not associated with known adverse fetal effects at any point in pregnancy, when performed without administration of contrast media7. There are no reported adverse effects of MRI performed at 1.5 Tesla (1.5 T)8. However, there have been no human studies of possible adverse effects at higher field strength, such as 3.0 T7, 9, 10, although recent data show that it may be safe in a porcine model11. There is general consensus that fetal MRI is indicated following an expert ultrasound examination in which the diagnostic information about an abnormality is incomplete. Under these circumstances, MRI may provide important information that may confirm or complement the ultrasound findings and alter or modify patient management. Presently, factors influencing the decision to perform fetal MRI include, but are not limited to: experience/equipment of the ultrasound and MRI facilities, accessibility to MRI, maternal conditions, gestational age, safety concerns, legal consideration regarding termination of pregnancy (TOP) and parental wishes after appropriate counseling3, 10, 12, 13. The ISUOG survey addressed the necessity of MRI for selected indications and used a 7-point rating scale to weight the responses from 0 (not at all indicated) to 7 (definitely indicated) (Figure 1). The variety of responses is likely to reflect the divergence seen between various specialties and the spectrum of pathologies seen at each center. The opinions may also reflect different levels of experience when performing fetal ultrasound and MRI. In general, performance of an ultrasound examination following only the minimum recommendations for second-trimester ultrasound/basic brain examination, as proposed by ISUOG5, is insufficient prior to requesting MRI. Additional views, such as orthogonal views, higher frequency probes and/or transvaginal imaging are required to detail the specific abnormality14, 15. The practice of TOP and associated medicolegal implications may influence the use of fetal MRI at local institutions. In countries in which the decision about TOP has to be made before 24 weeks, the performance of MRI prior to this time may help an individual couple decide on the future of their pregnancy; however, in general, MRI is better reserved for later in the second or third trimester13. Although available data are still inconclusive, MRI for parental reassurance regarding the absence of associated pathologies in fetuses with apparently isolated conditions may be recommended in fetuses with isolated ventriculomegaly16, agenesis of the corpus callosum17, absent septum pellucidum and cerebellar or vermian anomalies18. In addition, fetal MRI has been found to be helpful in monochorionic twin pregnancies after iatrogenic or natural demise of a cotwin to find pathological changes in the surviving twin19, 20. Fetal MRI performed before 18 weeks does not usually provide information additional to that obtained on ultrasound examination. In some cases, additional information can be obtained before 22 weeks13 but MRI becomes increasingly helpful thereafter. Specific examples of pathologies that can be evaluated in the third trimester include, but are not limited to, those of cortical development and neck masses that may cause airway compromise21. Most organs can be visualized in detail between 26 and 32 weeks of pregnancy, when pathologies related to abnormal development are more fully evolved, but each pregnancy and each fetus will differ. It may become more difficult for the woman to stay comfortable in the scanner with advancing gestation and consideration of left-lateral offset is recommended. When indicated, performed properly and interpreted correctly, MRI not only contributes to diagnosis but may be an important component of treatment choice, delivery planning and counseling. Practitioners who interpret fetal MRI should be familiar with fetal diagnosis, as it differs from diagnosis in other patient populations. Choice of appropriate protocols and techniques requires extensive training; thus, the performance of fetal MRI should be limited to individuals with specific training and expertise. The same applies to interpretation of the examination. In many centers this will require a multispecialty collaborative approach, including experts in the field of prenatal diagnosis, perinatology, neonatology, pediatric neurology and neuroradiology, genetics and other related specialties (Table 1), in order to integrate the clinical and family histories and the ultrasound and MRI findings, to optimize patient care. Consultation with a geneticist and other pediatric subspecialists may be required in order to provide the patient with the best counseling and management options. Although at present we are unaware of the existence of a recognized fetal MRI specialization, individuals who perform fetal MRI should have undergone specialized training in collaboration with a teaching center, enabling them to perform a state-of-the-art fetal MRI examination after a sufficient amount of cases (GOOD PRACTICE POINT; i.e. recommended best practice based on the clinical experience of the guideline development group). Performance of fetal MRI according to standardized criteria (Table 2) will improve the management of pregnancies complicated by a fetal malformation or acquired condition (GOOD PRACTICE POINT). At present, 1.5 T is the most commonly used field strength, providing acceptable resolution even as early as 18 weeks22. 3 T has the potential to provide images with higher resolution and better signal-to-noise ratio than does 1.5 T, while maintaining a comparable or lower energy deposition22. Nonetheless, higher field strength is currently not recommended for in-vivo fetal imaging10. In all cases, the field-of-view should be adjusted to the region of interest. A slice thickness of 3–5 mm with a 10–15% intersection gap will be appropriate in most cases. The examination should include at least T2 information in three orthogonal planes of the fetal brain and body, and T1- and GRE-EP sequences in one or two planes, preferably frontal and sagittal. This ‘minimum’ protocol should be executable in less than 30 min, even allowing for fetal movement and sequence repetition. Only examinations that are performed following this protocol should be regarded as ‘state of the art’ (GOOD PRACTICE POINT). Although usually measurements will already have been made with ultrasound, measuring certain structures at the MRI examination may be of benefit in particular cases12. When measuring fluid-containing structures, it is important to remember that MRI measurements are usually around 10% greater than the corresponding ultrasound measurements. In lung volumetry, normal gestational-age related MRI measurements correlate with fetal body volume29 and are considered predictive of outcome in cases of lung pathology30. The whole examination should be stored according to local practice, preferably in electronic format. CDs of the examinations can be produced for the patient to enable second-opinion assessment (GOOD PRACTICE POINT). Fetal situs, stomach and gallbladder (fluid filling), fluid and meconium signals of bowels (Figure 7c,d), kidneys, urinary bladder (fluid filling); on request: female/male external genitals (in case of latter: descent of testes) (Figure 8) Standardized reports should follow the suggested structure outlined in Table 3 (GOOD PRACTICE POINT). As MRI is usually not a first-line examination, but a complementary examination following an ultrasound examination performed in the second trimester31, the emphasis of the examination and report should be on structures that are more difficult to assess with ultrasound. A detailed anatomical assessment may be performed on demand. D. Prayer*, Division of Neuroradiology and Musculoskeletal Radiology, Department of Radiology, Medical University of Vienna, Vienna, Austria G. Malinger*, Division of Ultrasound in Obstetrics & Gynecology, Lis Maternity Hospital, Sourasky Medical Center and Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel P. C. Brugger, Division of Anatomy, Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria C. Cassady, Texas Children's Hospital and Fetal Center, Houston, TX, USA L. De Catte, Department of Obstetrics & Gynecology, University Hospitals Leuven, Leuven, Belgium B. De Keersmaecker, Department of Obstetrics & Gynecology, University Hospitals Leuven, Leuven, Belgium G. L. Fernandes, Fetal Medicine Unit, Department of Obstetrics, ABC Medicine University, Santo Andre, Brazil P. Glanc, Departments of Radiology and Obstetrics & Gynecology, University of Toronto and Sunnybrook Research Institute, Obstetrical Ultrasound Center, Department of Medical Imaging, Body Division, Sunnybrook Health Sciences Centre, Toronto, Canada L. F. Gonçalves, Fetal Imaging, William Beaumont Hospital, Royal Oak and Oakland University William Beaumont School of Medicine, Rochester, MI, USA G. M. Gruber, Division of Anatomy, Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria S. Laifer-Narin, Division of Ultrasound and Fetal MRI, Columbia University Medical Center - New York Presbyterian Hospital, New York, NY, USA W. Lee, Department of Obstetrics and Gynecology, Baylor College of Medicine and Texas Children's Pavilion for Women, Houston, TX, USA A.-E. Millischer, Radiodiagnostics Department, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, Université Paris Descartes, Paris, France M. Molho, Diagnostique Ante Natal, Service de Neuroradiologie, CHU Sud Réunion, St Pierre, La Réunion, France J. Neelavalli, Department of Radiology, Wayne State University School of Medicine, Detroit, MI, USA L. Platt, Department of Obstetrics and Gynecology, David Geffen School of Medicine, Los Angeles, CA, USA D. Pugash, Department of Radiology, University of British Columbia and Department of Obstetrics and Gynecology, BC Women's Hospital, Vancouver, Canada P. Ramaekers, Prenatal Diagnosis, Department of Obstetrics and Gynecology, Ghent University Hospital, Ghent, Belgium L. J. Salomon, Department of Obstetrics, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, Université Paris Descartes, Paris, France M. Sanz, Department of Obstetrics and Gynecology, Baylor College of Medicine and Texas Children's Pavilion for Women, Houston, TX, USA I. E. Timor-Tritsch, Division of Obstetrical & Gynecological Ultrasound, NYU School of Medicine, New York, NY, USA B. Tutschek, Department of Obstetrics & Gynecology, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany and Prenatal Zurich, Zürich, Switzerland D. Twickler, University of Texas Southwestern Medical Center, Dallas, TX, USA M. Weber, Division of Neuroradiology and Musculoskeletal Radiology, Department of Radiology, Medical University of Vienna, Vienna, Austria R. Ximenes, Fetal Medicine Foundation Latin America, Centrus, Campinas, Brazil N. Raine-Fenning, Department of Child Health, Obstetrics & Gynaecology, School of Medicine, University of Nottingham and Nurture Fertility, The Fertility Partnership, Nottingham, UK *D. P. and G. M. contributed equally to this article. These Guidelines should be cited as: ‘Prayer D, Malinger G, Brugger PC, Cassady C, De Catte L, De Keersmaecker B, Fernandes GL, Glanc P, Gonçalves LF, Gruber GM, Laifer-Narin S, Lee W, Millischer A-E, Molho M, Neelavalli J, Platt L, Pugash D, Ramaekers P, Salomon LJ, Sanz M, Timor-Tritsch IE, Tutschek B, Twickler D, Weber M, Ximenes R, Raine-Fenning N. ISUOG Practice Guidelines: performance of fetal magnetic resonance imaging. Ultrasound Obstet Gynecol 2017; 49: 671–680.’ Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.