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Perinatal post-mortem ultrasound (PMUS): radiological-pathological correlation
Insights into Imaging volume 10, Article number: 81 (2019)
There has been an increasing demand and interest in post-mortem imaging techniques, either as an adjunct or replacement for the conventional invasive autopsy. Post-mortem ultrasound (PMUS) is easily accessible and more affordable than other cross-sectional imaging modalities and allows visualisation of normal anatomical structures of the brain, thorax and abdomen in perinatal cases. The lack of aeration of post-mortem foetal lungs provides a good sonographic window for assessment of the heart and normal pulmonary lobulation, in contrast to live neonates.
In a previous article within this journal, we published a practical approach to conducting a comprehensive PMUS examination. This covered the basic principles behind why post-mortem imaging is performed, helpful techniques for obtaining optimal PMUS images, and the expected normal post-mortem changes seen in perinatal deaths. In this article, we build upon this by focusing on commonly encountered pathologies on PMUS and compare these to autopsy and other post-mortem imaging modalities.
Post-mortem ultrasound can delineate the main body organs and is primarily used to identify congenital structural anomalies.
Post-mortem ultrasound is least useful in delineating congenital cardiac anomalies, likely due to the lack of foetal circulation.
Intracranial pathologies are easily identified, but maceration and overlapping cranial sutures may obscure clear sonographic views.
Without a perinatal autopsy, many parents cannot understand the cause for their child’s death, clinicians miss detailed information to counsel parents about future pregnancies, and data on epidemiological studies are incomplete [1, 2]. Parents dislike the invasive approach of traditional autopsy, , and for others, religious beliefs may preclude an autopsy . The net result of these changes in attitudes has led to an increased parental demand for alternative, non-invasive methods to aid or replace the internal examination component of a perinatal autopsy [3, 5].
Whilst a variety of advanced post-mortem imaging techniques have shown good diagnostic accuracy and reproducibility, such as post-mortem MRI (PMMR) , post-mortem CT (PMCT)  and post-mortem micro-focus CT (PMμCT) , access to these techniques may be restricted especially with limited resources or expertise. Ultrasound is a more affordable, easily accessible and adaptable imaging modality, widely used in many hospital settings. In addition, the ultrasound machinery can be easily transported to various parts of the hospital, avoiding the need to transfer bodies to clinical areas and the disruption that may ensue for other patients and members of staff.
In a recent article published within this journal , we described a practical approach to conducting a comprehensive post-mortem ultrasound (PMUS) examination. This covered the basic principles behind foetal preparation for imaging, parental consent, helpful techniques for obtaining optimal PMUS images and the expected normal post-mortem changes.
This current article builds upon our previous work by describing commonly encountered pathologies on PMUS and comparison with results at autopsy and other post-mortem imaging modalities, where available. We intend this to serve as a useful pictorial reference for radiologists, clinicians and allied healthcare professionals who wish to start providing a perinatal PMUS service.
Whilst care and thoroughness should be exercised when imaging foetuses irrespective of their prenatal history, it is important to understand the type of suspected pathology to be excluded and the clinical significance which should be placed on incidental findings. Three key considerations should therefore be taken into account—gestation, the prenatal imaging findings and the mode of foetal demise (i.e. termination of pregnancy, stillbirth or miscarriage). Gestational-dependent changes associated with foetal developmental are well recognised and not reproduced here.
Prenatal ultrasound screening is now commonplace in many developed nations, and modern imaging techniques have a high diagnostic accuracy rate in the region of 90% when compared with subsequent perinatal autopsy findings [10, 11]. It is therefore important to support or dispute prenatal diagnoses where possible with post-mortem examinations. Particular care should be taken when assessing prenatally diagnosed abdominal or musculoskeletal pathologies, as several studies have reported a lower prenatal ultrasound diagnostic accuracy rate for these body systems: approximately 60% for intra-abdominal pathologies [10, 12], and < 30% for limb anomalies . In one study of over 500 foetuses, the highest false-positive rates were given for gastrointestinal and renal tract malformations .
Regarding mode of foetal demise, a history of termination of pregnancy is particularly pertinent. This is because PMUS is able to identify congenital structural abnormalities (but less able to diagnose infection or placental aetiologies) and a high number of terminations of pregnancy will be due to antenatally detected structural abnormalities (estimated at approximately 43.8  to 85.8%  compared to only 5% of intra-uterine deaths and stillbirths ). Where a clinical indication states that a termination of pregnancy has occurred, the radiologist should be aware of the reasons behind this decision and seek to examine carefully the organs that had been suspected of significant anomalies.
Large surveys of parents and healthcare professionals have found that whilst imaging techniques for non-invasive autopsies have a high acceptability [5, 17], one barrier to uptake are concerns about ‘missed diagnoses’, potentially not reaching the same levels of certainty as an ‘invasive’ autopsy . Whilst PMMR has a more established role and its usage is widely published [7, 19,20,21,22,23,24], compared to conventional perinatal autopsy findings, the diagnostic accuracy of PMUS is still being evaluated.
Overall PMUS sensitivity and specificity rates have been reported at 75% and 83.3% for whole-body diagnoses , with abnormalities affecting the heart being particularly challenging to diagnose with lower sensitivity rates ranging between 18.2–50% [25,26,27]. These numbers may be lower than expected or acceptable, although when comparing 2-D PMUS and 3T PMMR imaging within the same cohort of 160 foetuses, Kang et al.  did not find a statistically significant difference in accuracy rates for cases where the ultrasound images were of diagnostic quality (67.8% vs 78.0% respectively, p > 0.05). This suggests that a well-performed perinatal post-mortem ultrasound study could provide a similar degree of information as PMMR without the need for further cross-sectional imaging, allowing for potential placement as a first-line technique to triage cases for PMMR. In this article, cases where PMUS was found to be non-diagnostic (i.e. unhelpful) were those that were performed in foetuses of < 20 weeks gestational age  and displaying moderate or severe maceration . Therefore, we recommend that operators are aware of the reduced likelihood of a diagnostic PMUS study in small gestational aged foetuses, those that have a known prolonged intra-uterine retention period and those with suspected cardiac anomalies.
Our approach to a comprehensive PMUS is based on a structured ‘systems review’ of the foetus. This enables a review of the main body organs for congenital anatomical variants or abnormalities. In this section, we demonstrate some of these major pathologies by body systems and describe their relative importance.
Head, neck and spine
Congenital disorders of the central nervous system (CNS) are the commonest group of structural anomalies leading to termination of pregnancy. Approximately 32–37.7% of all terminations of pregnancies may be for prenatally diagnosed CNS anomalies [14, 30], with neural tube defects accounting for the largest proportion (approximately a third of cases) .
For this reason, it is important to assess the spine in all foetuses, paying close attention for associated Chiari malformations (Fig. 1) and identifying vertebral segmental anomalies and spinal dysraphism (Fig. 2). Further characterisation with skeletal radiographs may be helpful .
The second most common CNS anomaly is lateral ventricular dilatation, or ventriculomegaly. Where prenatal ventricular dilatation is reported, cerebrospinal fluid shifts occurring after death may result in an apparent ‘resolution’ of this appearance . In those instances, PMUS cannot confirm nor refute ventriculomegaly per se but should be used to exclude other contemporaneous anomalies  such as callosal anomalies (Figs. 3 and 4), neuronal migration anomalies (Fig. 5) or cerebral aqueductal stenosis, although the latter is harder to identify at post-mortem in the presence of cerebral oedema and sutural distortion.
Congenital intracranial tumours are rare. These account for < 2% of all foetal tumours , and teratomas forming the vast majority of all subtypes (Figs. 6 and 7). As a group, congenital intracranial tumours have a poor survival rate (estimated in one study as only 7% in the first year of life ), and tumours arising from or extending into the neck are usually at high risk of airway obstruction during delivery (Fig. 8). Intracranial lesions are usually primary tumours rather than metastases, although we have imaged one neonate with multiple intracranial metastases from a congenital fibrosarcoma of the thigh (Fig. 9). Recurrence rates in future pregnancies for intracranial anomalies are fortunately low, particularly where the abnormality is isolated (which is the case for the majority) and an underlying genetic cause is not identified .
Cardiac and vascular imaging
Congenital cardiac anomalies make up a significant proportion (approximately 10% ) of all structural anomalies at termination of pregnancy, and the prevalence of such anomalies are rising. Over the last 20 years across Europe, the annual increase of cardiac anomalies has been estimated at 1.4–4.6%  with the reasons thought to be related to increased maternal risk factors such as diabetes, body mass index, assisted reproductive techniques and alcohol consumption. These are key aspects of the mother’s clinical history which should be available at post-mortem imaging.
At PMUS the detection of complex cardiac anomalies is difficult due to a combination of lack of circulating blood, intra-cardiac haemostasis and occasionally intra-cardiac gas (likely from feticide ). Some distortion of the normal anatomy at post-mortem examination can be overcome by imaging the foetus in a waterbath .
The commonest cardiac anomalies at termination of pregnancy are hypoplastic right/left heart syndrome  and uni-ventricular heart defects . Other pathologies also feature, although less commonly, and include pulmonary atresia/stenosis (Fig. 10), aortic valve atresia/stenosis, transposition of the great arteries, tetralogy of Fallot, coarctation of the aorta, anomalous pulmonary venous return and septal defects (Fig. 11).
Where cardiac imaging is non-diagnostic at PMUS, further cross-sectional imaging with PMMR may be useful, particularly if high-resolution, isovolumetric sequences for multiplanar reconstructions are acquired, given the post-mortem distortion of normal anatomy due to ‘slumping’.
Congenital pulmonary anomalies are the least common structural abnormalities seen at PMUS . Whilst congenital pulmonary malformations (including cystic malformations, bronchopulmonary sequestrations, bronchial atresia, congenital lobar emphysema and bronchogenic cysts) may all be seen in live children, these are rarely the cause for foetal demise or terminations of pregnancy [41, 42]. In our experience, we have not detected any airway or lung malformations on PMUS, although Kang et al.  report one autopsy confirmed case of a bronchopulmonary foregut malformation in their series, which was missed on PMUS. It could have been due to the subtlety of the appearances that lead to the miss on PMUS; however, the medical literature is sparse with regards to the ideal post-mortem imaging of congenital pulmonary malformations.
The commonest finding at post-mortem imaging of the lungs is lung hypoplasia, usually secondary to other intra-abdominal pathologies such as congenital diaphragmatic hernias (Fig. 12) or enlarged polycystic kidneys. Excluding pulmonary infection is not currently possible  given that the foetal and early neonatal lungs are normally fluid filled.
Abnormalities of the abdomen seen at PMUS are most commonly related to the urinary tract or abdominal wall, the latter including pathologies such as gastroschisis, omphalocele (Fig. 13) and congenital diaphragmatic hernia (Fig. 12) [25, 26, 43]. Whilst the presence of an anterior abdominal wall defect does not require ultrasound for diagnosis, the resultant distortion and shift of intra-abdominal organs may have made prenatal imaging difficult and therefore examination of the presence of internal structures is the main criteria for imaging these cases.
Congenital intra-abdominal foetal tumours are very rare but may occur in the liver (such as haemangiomas, mesenchymal hamartoma and hepatoblastomas), kidneys (mesoblastic nephroma), pelvis (sacrococcygeal teratoma) or adrenal gland (neuroblastoma) . We have previously identified splenic metastases from an aggressive primary fibrosarcoma (Fig. 14) and a suprarenal cystic mass secondary to in utero adrenal haemorrhage (Fig. 15).
Renal anomalies are common and account for approximately 6–11% of all structural abnormalities seen at terminations of pregnancy [31, 45, 46]. These are usually related to renal dilatation (Figs. 16, 17, 18, and 19), polycystic renal disease (Fig. 20) or a mixture of structural congenital renal anomalies such as renal agenesis, ectopic kidneys (Fig. 21) or cross-fused ectopia (Fig. 22). A prenatal history of oligohydramnios may be present, and non-visualisation of the urinary bladder at prenatal ultrasound has been reported as a marker for significant renal pathology and poor foetal survival [47, 48].
Musculoskeletal and soft tissue malformations
Where an underlying skeletal disorder is suspected, assessment of the whole skeleton is best performed by external examination and radiography (also known as a skeletal survey or babygram [32, 49, 50]). These are most useful over 8 weeks gestation, given the lack of skeletal ossification prior to this age . It is also important to remember that although isolated limb anomalies may be more commonly encountered in live cases , lethal skeletal dysplasias will be more prevalent in the subgroup presenting for post-mortem imaging  so an entire overview of the body is usually necessary rather than imaging of the affected limb(s). Whilst PMUS can be useful in demonstrating the non-ossified, cartilaginous anatomy which is not present on radiography (Fig. 23), it is rarely used in isolation to make a skeletal diagnosis and would be better reserved for the assessment of soft tissues.
Soft tissue lesions at PMUS may include venolymphatic (and other vascular) malformations (Fig. 24) or teratomas (as previously shown in Fig. 8) [44, 54]. In cases where a foetus is referred with a prenatal diagnosis of cystic hygroma (usually in the setting of foetal hydrops), we have also found that these cystic masses can ‘resolve’ , much like the appearances of ventriculomegaly, thus the role of PMUS is to review associated structural anomalies rather than identify the cystic hygroma itself. Associated anomalies (commonly intracranial in origin) are estimated to occur in 36–55.6% of cases, and usually related to an abnormal genetic karyotype [56, 57] which will have implications for prenatal counselling in future pregnancies .
The future of perinatal post-mortem imaging has many opportunities for further research, particularly for evidence-based studies that allow healthcare professionals and parents to understand the additional clinical yield from different imaging examinations. Combining this scientific evidence with an educational, practical approach, whilst accounting for imaging availability and affordability, will inform the future imaging protocols in this field.
At present, there are no internationally agreed guidelines outlining appropriate referral indications for PMUS or documented perinatal post-mortem imaging pathway. Given that smaller, macerated foetuses are more likely to be non-diagnostic on PMUS and that cardiac anomalies are difficult to detect, one possible referral pathway may be in prioritising PMUS for larger (> 20 weeks gestation), non-macerated foetuses [28, 29] potentially alleviating the need for PMMR and to preferentially use PMMR for prenatally suspected cardiac anomalies. Alternatively, for clinical institutions where access to PMMR is more challenging, it may be more appropriate for all perinatal deaths to be offered a PMUS in the first instance, especially if parental consent for autopsy is refused and no other imaging alternatives exist.
Where tissue samples are required for genetic analysis or histopathological correlation, PMUS-guided needle biopsies could potentially be used to reduce the invasiveness of conventional autopsy techniques. ‘Blinded’ percutaneous needle biopsies using anatomical surface landmarks have been used with varying levels of success [59, 60], and CT-guided biopsies have also been proposed in the literature . PMUS guidance may provide the optimal pragmatic solution enabling better organ visualisation (compared to ‘blinded biopsies’) and ease of access and affordability (compared with CT biopsies).
To our knowledge, there are no studies that have assessed the clinical change or additional contribution made by PMUS with respect to future pregnancy management, or whether there is any need for additional autopsy after comprehensive PMUS and prenatal imaging. More widespread use of the technique with pooling of data will allow these questions to be addressed.
Perinatal post-mortem ultrasound is an easily accessible imaging tool that allows detailed visualisation of many common congenital pathologies. This article has highlighted several examples including ventriculomegaly, congenital diaphragmatic hernias and genitourinary malformations. Whilst there may be a higher yield of non-diagnostic images in smaller (earlier gestation) and macerated foetuses, concordance rates of ultrasound with autopsy remain high and there may be a role for this technique to serve as a ‘screening’ tool prior to post-mortem MRI or in aiding image-guided biopsies.
Availability of data and materials
Data sharing is not applicable to this article as no datasets were generated or analysed during the current study
Magnetic resonance imaging
Picture archiving and communications system
Post-mortem computed tomography
Post-mortem magnetic resonance imaging
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Ethics approval and consent to participate
The imaging experience and cases reported upon are part of an ethically approved larger study investigating minimally invasive autopsy techniques and newer methods of post-mortem imaging. This has ethical approval from the National Health Service (NHS) Health Research Authority, Research Ethics Committee (REC) ID: CE13/LO/1494 and CE2015/81.
Consent for publication
All parents of children who underwent post-mortem imaging and less invasive autopsy techniques have signed consent forms agreeing for imaging to be used for educational and research purposes.
The authors declare that they have no competing interests.
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Shelmerdine, S.C., Sebire, N.J. & Arthurs, O.J. Perinatal post-mortem ultrasound (PMUS): radiological-pathological correlation. Insights Imaging 10, 81 (2019) doi:10.1186/s13244-019-0762-2
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