Postmortem fetal magnetic resonance imaging (PMFMRI) is increasingly used thanks to its good overall concordance with histology paralleling the rising incidence of parental refusal of autopsy. The technique could become a routine clinical exami- nation but it needs to be standardized and conducted by trained radiologists. Such radiologists should be aware of not only the (congenital and acquired) anomalies that can involve the fetus, but also of the Bphysiological^ postmortem changes. In this article, we intend to focus on the contribution of PMFMRI based on the existing literature and on our own experience, as we presently perform the technique routinely in our clinical practice. Key Points � Concordance rates between PMFMRI and autopsy are high for detecting fetal pathologies. � PMFMRI is more acceptable for parents than traditional autopsy. � PMFMRI is becoming widely used as a part of the postmortem investigations. � A dedicated radiologist needs to learn to interpret correctly a PMFMRI. � PMFMRI can be easily realized in daily clinical practice. . . . . Keywords Fetus Postmortem Magnetic resonance imaging Autopsy Perinatal General considerations autopsy rates have decreased worldwide . This resulted in a loss of major information that could have been used to counsel Although contemporary prenatal testing has improved the rec- clinicians and parents regarding future pregnancies . This ognition of fetal anomalies, autopsy remains a valuable tool reduction is mainly due to parental refusal of the autopsies; the by providing diagnosis or clarification of some prenatal find- reasons for their objection are (among others): religious consid- ings in 16% of cases . Furthermore, it has been shown that erations, fear of disfiguration of the dead fetus, and delay in autopsy provides important information decisive for genetic funeral plans [6, 7]. This has brought about the development counseling in over 50% of cases . of less invasive techniques for the analysis of dead fetuses. In the past several decades, the number of terminations of Postmortem fetal magnetic resonance imaging (PMFMRI) has pregnancies has increased secondary to the development of pre- been shown to be significantly more acceptable for parents and natal diagnosis . During the same period, fetal and neonatal many healthcare professionals ; therefore, the demand for such (less invasive) imaging examinations has increased. Besides PMFMRI, other postmortem imaging modali- ties have been increasingly used or been developed, in- cluding conventional radiographs, ultrasonography (US), * E. Fred Avni and computed tomography (CT). Each of these techniques firstname.lastname@example.org has its own advantages and limitations. Still, to date, no or Department of Radiology, Hôpital Delta (CHIREC), Boulevard du little established standardized guidelines have been de- Triomphe 201, 1160 Auderghem, Belgium fined for perinatal and pediatric postmortem imaging. Department of Radiology, Hôpital Ixelles, Rue Jean Paquot 63, Across European countries, there is no unique approach 1050 Ixelles, Belgium to determine which subpopulation of postmortem fetuses Department of Neuroradiology, Hôpital Roger Salengro, Avenue du should be imaged and with what modality . This will Professeur Emile Laine, 59037 Lille, France need to be defined in the near future. 592 Insights Imaging (2018) 9:591–598 PMFMRI has an overall high negative predictive value and The procedure can be used as a first intention/screening tool. A discussion between experienced perinatal radiologists, fetal pathologists, PMFMRI should be performed as soon as possible after the and geneticists could then select which cases would require termination of the pregnancy or fetal death. In the Magnetic full or selective autopsy . This will be particularly impor- Resonance Imaging Autopsy Study (MaRIAS), all the bodies tant for central nervous system (CNS) anomalies . were stored in a mortuary at 4 °C for 1 to 6 days . It should For some authors, gestational age and body weight influence be kept in mind that there may be a delay between fetal death the diagnostic accuracy of PMFMRI. Jawad et al. usedthe and delivery in case of termination of pregnancy. This delay cut-off of 500 g. In their series, they demonstrated that could be longer after spontaneous intrauterine fetal death. PMFMRI provides diagnostic images in 90% of fetuses with a PMFMRI can be performed either at 1.5 T or 3 T. The rate body weight > 535 g, opposed to less than 50% of fetuses with a of diagnostic errors is lower using 3 T than 1.5 T MR magnets, body weight < 122 g. Therefore, they concluded that 500 g especially for low body weight fetuses and for all body parts should be the limit for PMFMRI at 1.5 T. Their experience is except for the brain and orbits . not completely confirmed by ours. We do perform second tri- The examination is usually performed in the absence of the mester PMFMRI and we almost always have diagnostic images parents. In any case, detailed explanation on the examination for fetuses with low body weight (our smallest fetus weighed is usually provided and, in some centers/countries, they may 140gat15weeksgestation) . Furthermore, the prenatal be asked to sign an informed consent . The body should be diagnosis of malformations becomes more accurate in small covered and placed supine, lying as close as possible to the fetuses and termination of second trimester pregnancies tends anatomical neutral position. The coil that will be used needs to to increase. It will, therefore, be important to further develop be adapted to the size of the body. In general, a head coil is sequences adapted to small fetuses. used for the brain and spine and a body coil for the body In order to optimize the contribution of PMFMRI, addi- imaging . Yet, in smaller fetuses, the head coil may pro- tional information from non-invasive examinations are re- vide enough coverage for both the head and the body. We quired, including detailed external examination, skeletal ra- prefer to use separate head and neck coils. diographs, placental analysis, and genetic testing . Various protocols for the examination have been proposed in The aims of the present overview are to summarize the the literature; we use a simplified protocol based on the one present (and hypothesize the future) utility of PMFMRI based reported by Norman et al. . Our protocol includes a 3D on the presently available literature and on our own experi- T2-weighted (W) volumetric acquisition [3D constructive inter- ence, as we perform it routinely in daily clinical practice. ference in steady state (CISS)], of the head and whole body with reconstructions in the three planes, T1-W sequences in the sag- ittal and coronal planes on the head and the rest of the body, and Indications of PMFMRI axial T2* of the head (Table 1). Depending on the gestational age, acquisition of the head and the body can be made at the Based on the literature gathered to date and on our own expe- same time or separately. T1-W images have poor contrast and rience, it can be stated that the main indications for PMFMRI low signal in postmortem imaging . There is a normal high are: termination of pregnancies in case of fetal malformations, T1-W signal in the normal thyroid and in the bowel (distal small late miscarriages, and intrauterine fetal deaths in every case then large bowel, depending on the gestational age) (Fig. 1). where the parents refuse autopsy. It can also be performed in High signal in the bowel is related to its meconium content the cases where the parents do accept the autopsy, as (Fig. 1). High-resolution T2-W images offer much better con- PMFMRI may orient the pathologist and potentially provide trast for PMFMRI [3, 17]. Diffusion-weighted sequences of the additional information compared to US . fetal brain has been used to estimate the degree of maceration As mentioned, in case of termination of pregnancy, whenever the exact time of death is unknown. Still, it has a poor PMFMRI can confirm the antenatal findings of obstetrical contribution in clinical routine . US and potentially provide supplementary information. In The total duration of PMFMRI in our institution is around the cases of late miscarriages and intrauterine fetal deaths, 30 min. PMFMRI may help to understand their causes. PMFMRI can be performed even in early second tri- mester fetuses. In our experience, even in these low Interpretation of PMFMRI: diagnosing weight fetuses, PMFMRI seems to be more accurate than anomalies and physiological changes obstetrical ultrasound in characterizing brain or fetal body malformations. The examination offers an easy evaluation Knowledge of the antenatal sonographic findings as well as all of the deceased fetus. The present exceptions are cardiac relevant clinical or genetic data is essential before interpreting malformations . PMFMRI, as it will increase the diagnostic accuracy. Insights Imaging (2018) 9:591–598 593 Table 1 Sequence parameters for 3D CISS T2 (sag) T1 TSE (sag) T1 TSE (cor) T2* (axial brain) postmortem fetal magnetic resonance imaging (PMFMRI) Voxel (mm) 0.8 × 0.8 × 0.8 1.4 × 0.8 × 2.5 1.4 × 0.8 × 2.5 1.1 × 0.9 × 3 Slices 96 40 40 30 Slice thickness (mm) 0.8 2.5 2.5 3 Distance factor (%) 20 25 25 15 FOV read (mm) 210 380 380 230 FOV phase (%) 68.8 75 100 100 TR (ms) 6.45 427 427 1030 TE (ms) 2.69 11 11 26 Averages 1 2 2 1 Duration of acquisition (min) 3.19 3.15 2.33 2.5 Phase oversampling (%) 13 40 100 0 FOV: field of view; CISS: constructive interference in steady state; TSE: turbo spin echo; TR: repetition time; TE: echo time; sag/cor: sagittal or coronal acquisition Evaluating the fetus should be standardized and systematic, pathological findings . The following should be men- analyzing all structures and organs from the head to toe. The tioned, among others: various findings should be correlated with fetal age. Any ab- normality should be analyzed and characterized as it would be – Fluid accumulation: Subcutaneous edema, pleural, peri- on (living) fetal MRI (for second trimester fetuses) or with cardial effusions and ascites (Fig. 2). There is often some postnatal findings in case of third trimester fetal deaths. degree of body deformation. Importantly, there are several PMFMRI changes that devel- – Head: Skull deformity (that needs to be differentiated op progressively after death (mainly because of the tissular from head molding that occurs at delivery), collapsed lysis and maceration) that should not be misinterpreted as eyeballs, brain ischemia (edema, loss of gray-white mat- ter differentiation, and low T2 signal in basal ganglia), frontal irregular cortical plate indentation , tonsillar descent, venous stasis, and small intraventricular hemor- rhage without dilatation (Fig. 3). – Chest: Dark (hyposignal) appearances of the lungs indi- cate the presence of air within the airway (when the infant has breathed before death or when cardiopulmonary Fig. 1 Coronal T1-weighted (W) image of a 24 weeks gestation fetus Fig. 2 Coronal T2-W image of a 25 weeks fetus in a case of intrauterine showing the normal T1 hypersignal of the meconium and thyroid. The death. There is bilateral pleural effusion, subcutaneous edema, ascitis, fetal liver appears relatively hypersignal, probably due to high glycogen distended bowel loops, and enlarged appearance of the normal fetal content liver. All findings are physiological postmortem changes 594 Insights Imaging (2018) 9:591–598 Fig. 3 Axial T2-W image of the brain of a 20 weeks fetus showing bilateral intraventricular hemorrhage as a normal postmortem change resuscitation methods have been used in stillbirths), whereas the lungs display an intermediate in case of ter- mination of pregnancy or late miscarriage (Fig. 4a). – Heart: Small pericardial effusions, intracardiac air, blood clots, and fluid–fluid level in the heart and major vessels are common findings (Fig. 5). The cardiac ventricles may have a pseudo-thickened appearance after death; this should not be mistaken with ventricular hypertrophy . Valves leaflets can be seen clearly when closed; they Fig. 4 Postmortem fetal magnetic resonance imaging (PMFMRI) in a term stillbirth. Physiological postmortem changes. a Coronal T2-W are more difficult to visualize if fully open. image showing dark appearance of the lungs containing air. b Axial T2- – Abdomen: Changes include gas in the hepatobiliary sys- W image showing air in the hepatobiliary system tem (Fig. 4b), small and large bowel dilatation (Fig. 2), and a pseudohepatomegaly (Fig. 2). fetusesofmore than24weeks gestation (compared with 76.4% in children) . To be noted, this study and others before have demonstrat- It should be noted that the postmortem interval cannot be ed that the diagnostic accuracy of PMFMRI varies according determined by PMFMRI even if some research has been done to the different body parts: on the influence of various factors, such as the accumulation of fluid in the lungs or the change in brain signal . – Neurological abnormalities: PMFMRI is highly accurate for the detection of cerebral malformations (sensitivity 88.4%, specificity 95.2%) (Figs. 6, 7,and 8) and intracra- nial bleedings (sensitivity 100%, specificity 99.1%), but Diagnostic accuracy of PMFMRI less sensitive for detecting ischemic injuries (sensitivity 68%, specificity 96.1%) . It seems challenging to Since the late 1990s, when Brookes et al. published the first study on non-invasive perinatal necropsy, many advances have been achieved in PMFMRI. The largest recent prospec- tive comparison of standard autopsy versus less invasive au- topsy (postmortem MRI and ancillary investigations such as examination of the placenta and postmortem blood samplings but no incision) in fetuses and children is the so-called the Magnetic Resonance Imaging Autopsy Study (MaRIAS, Lancet 2013) . In this study, the authors have analyzed 400 patients, of which 277 were fetuses. The cause of death or major pathological lesions detected by minimally invasive autopsy were concordant with conventional autopsy in 357 Fig. 5 Axial T2-W image of a 23 weeks fetus showing air and blood clots cases (89.3%). The concordance was even higher in fetuses: in the heart as a physiological postmortem change. It also shows the normal gray appearance of fetal lungs that have not been aerated 94.6% in fetuses of less than 24 weeks gestation and 95.7% in Insights Imaging (2018) 9:591–598 595 Fig. 8 PMFMRI of a 25 weeks gestation fetus in a case of late miscarriage. Sagittal T2-W image shows an occipital encephalocele Fig. 6 PMFMRI of a 21 weeks gestation fetus who died in utero. Axial T2-W image shows indirect signs of corpus callosum agenesis. Note that there is a subcutaneous edema that has to be considered as a normal differentiate between premortem ischemic injuries and postmortem change physiological postmortem changes. Furthermore, PMFMRI provides important diagnostic in- formation in 50% of fetuses in which conventional brain au- topsy is non-diagnostic due to maceration and autolysis of the brain tissues . – Abdominal abnormalities: PMFMRI is highly accurate for the detection of renal and urinary tract abnormalities (sensitivity 80%, overall concordance 97%) and for anomalies of the abdominal wall (Figs. 9 and 10). It is less accurate for adrenal, liver, and intestinal abnormali- ties (sensitivity 50%) . For instance, the adrenals may appear hemorrhagic-like on PMFMRI but normal on au- topsy. Conversely, they may appear normal on PMFMRI Fig. 7 PMFMRI of a 22 weeks gestation fetus, for which the pregnancy Fig. 9 PMFMRI of an 18 weeks gestation fetus in a case of termination of was interrupted for extensive spinal dysraphism. a Axial T2-W image pregnancy. a Sagittal T2-W image shows a megabladder and dilated shows bilateral ventriculomegaly. There is a small hemorrhage in the posterior urethra above the posterior urethral valves (arrow). b Coronal occipital horns that is considered as a postmortem change. b Sagittal T2-W image shows a right multicystic dysplastic kidney and left T2-W image shows a close spinal dysraphism (asterisk) hydronephrosis 596 Insights Imaging (2018) 9:591–598 Fig. 10 Sagittal T2-W image of a 25 weeks gestation fetus with an abdominal wall defect and a large hepatocele Fig. 11 Coronal T2-W image of a 25 weeks gestation fetus with a left congenial diaphragmatic hernia but with microscopic hemorrhage on autopsy. Intestinal anomalies, such as atresia, obstruction, and malrotation, can be difficult to diagnose, since bowel dilatation can be Interestingly, in our experience, PMFMRI is more accurate due to a postmortem change. than obstetrical ultrasound in detecting major CNS and fetal – Non-cardiac thoracic abnormalities: In the fetus, because body malformations, especially during the second trimester . there is no lung aeration, a normal thoracic PMFMRI predicts normal autopsy in over 80% of the cases . The overall sensitivity and specificity of PMFMRI for non-cardiac thoracic pathology is better in fetuses than Advantages of PMFMRI in children, with, respectively, 80% (39.5% in children) and 85.5% . Its sensitivity in detecting anatomical PMFMRI has numerous advantages: abnormalities (pleural effusion, lung or chest hypoplasia, congenital diaphragmatic hernia) is good (Fig. 11), but it – It provides immediate diagnosis in comparison with au- is poorer at detecting infection and diffuse alveolar hem- topsy, whose results can take a longer time. According to orrhage . the survey of the French society of perinatal pathology in – Cardiovascular abnormalities: The overall sensitivity 2012 (http://www.chu-clermontferrand.fr/internet/sites/ and specificity of PMFMRI are 72.7 and 96.2% for de- soffoet/default.aspx), the delay in providing a complete tecting any cardiac pathology . The technique is able histologic report is 1 month in 30% and more than to detect structural cardiac anomalies in fetuses older than 2 months in 60% of the fetuses. Noteworthy, 40% of the 24 weeks with a good negative predictive value . French pathologists in practice today will retire in less – Musculoskeletal abnormalities:PMFMRIhasahigh di- than 10 years and 80% of them will not be replaced. agnostic accuracy for the exclusion of musculoskeletal – It represents an alternative to autopsy, with at least some abnormalities (negative predictive value 93.8%) but its information provided in cases where the parents do not sensitivity is relatively poor (51.1%) . Fetal conven- agree to an invasive procedure. tional radiographs and/or fetal skeletal CT are clearly use- – It can guide the autopsy in order to have less inva- ful whenever skeletal anomalies are suspected. sive procedures. If a histological assessment of Insights Imaging (2018) 9:591–598 597 tissue is required to confirm a suspected diagnosis, Conclusion PMFMRI can be used to target samplings (transcu- taneous needle biopsies). PMFMRI may also be Advances in imaging technology along with the reduction in combined with laparoscopic examination (keyhole parental acceptance of conventional autopsy are likely to techniques) to facilitate direct organ examination change the way fetal death will be investigated. Postmortem while minimizing incisions . Both techniques fetal magnetic resonance imaging (PMFMRI) is likely to de- (percutaneous or endoscopic tissue sampling) mini- velop and become an important part of the fetal imaging. The mize the body disfiguration and can be more ac- use of fetal postmortem examination modalities should be ceptable for the parents. decided between the different specialists involved after – Images can be stored, easily sent, and used in multidisci- reviewing the full clinical history, prenatal ultrasound find- plinary meetings. ings, and external examination. PMFMRI should be per- – Precise measurements and organs volumetries can formed in all cases of parental autopsy refusal or prior to be obtained . any histopathology examination to assess if a full autopsy or, rather, a targeted biopsy is needed. Acknowledgements Geradin B. RT and Agram S. RT performed the PMFMRI examinations. Limitations of PMFMRI Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// There are some limitations to the use of PMFMRI: creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appro- – The general accessibility of MRI is a clear limitation. priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. – Radiographers trained to this type of examination are not always available. 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Scola E, Conte G, Palumbo G et al (2018) High resolution post- fetal organ volumetry using magnetic resonance imaging and com- mortem MRI of non-fixed in situ foetal brain in the second trimester parison to organ weights at conventional autopsy. Ultrasound of gestation: normal foetal brain development. Eur Radiol 28(1): Obstet Gynecol 31(2):187–193 363–371 28. Ashwin C, Hutchinson JC, Kang X et al (2017) Learning effect on 18. Papadopoulou I, Langan D, Sebire NJ, Jacques TS, Arthurs OJ perinatal post-mortem magnetic resonance imaging reporting: sin- (2016) Diffusion-weighted post-mortem magnetic resonance imag- gle reporter diagnostic accuracy of 200 cases. Prenat Diagn 37(6): ing of the human fetal brain in situ. Eur J Radiol 85(6):1167–1173 566–574 19. Arthurs OJ, Barber JL, Taylor AM, Sebire NJ (2015) Normal peri- 29. Hutchinson JC, Arthurs OJ, Sebire NJ (2016) Postmortem research: natal and paediatric postmortem magnetic resonance imaging ap- innovations and future directions for the perinatal and paediatric pearances. Pediatr Radiol 45(4):527–535 autopsy. Arch Dis Child Educ Pract Ed 101(1):54–56 20. Barber JL, Sebire NJ, Chitty LS, Taylor AM, Arthurs OJ (2015) Lung aeration on post-mortem magnetic resonance imaging is a useful marker of live birth versus stillbirth. Int J Legal Med Publisher’s Note 129(3):531–536 21. Arthurs OJ, Thayyil S, Olsen OE et al (2014) Owens CM; magnetic Springer Nature remains neutral with regard to jurisdictional claims in resonance imaging autopsy study (MaRIAS) collaborative group. published maps and institutional affiliations.
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