- Pictorial Review
- Open Access
Radiological imaging of teratological fetuses: what can we learn?
© The Author(s) 2017
- Received: 23 January 2017
- Accepted: 8 March 2017
- Published: 24 April 2017
To determine the advantages of radiological imaging of a collection of full-term teratological fetuses in order to increase their scientific and educational value.
Anatomical museums around the world exhibit full-term teratological fetuses. Unfortunately, these museums are regularly considered as “morbid cabinets”. Detailed dysmorphological information concerning the exhibited specimens is often lacking. Moreover, fetuses with severe and complex congenital anomalies are frequently diagnosed incompletely, incorrectly or not at all.
In order to verify diagnoses and to enrich their educational and scientific value, we imaged 41 out of the 72 teratological specimens present in the collection of our Anatomy and Pathology Museum in Nijmegen (The Netherlands) by means of magnetic resonance imaging (MRI) and computed tomography (CT). Additionally, contemporary dysmorphological insights and 3D models are implemented in the teratology education of medical students and residents.
Full-term teratological fetuses have become increasingly rare and deserve a prominent place in every anatomical museum; they are suitable for contemporary teratological research and education. Modern radiological techniques markedly enhance their scientific and didactic value.
• To explore the scientific and educational potential of institutionalised teratological collections
• To understand the additional value of radiological imaging in diagnosing teratological specimens
• To learn about the specific settings of MRI parameters when scanning fixed specimens
• To recognise specific internal dysmorphology in several congenital anomalies
- Magnetic resonance imaging
- Computed tomography
- Congenital anomaly
Many anatomical museums around the world exhibit teratological specimens of third trimester fetuses. Among the institutionalised collections, especially noteworthy are the eighteenth century collection of the Federal Pathological Anatomy Museum in Vienna (Austria) [1, 2], the eighteenth century collection of the Hunterian Museum of the Royal College of Surgeons in London  and the nineteenth century Vrolik collection residing in the Vrolik Museum at the University Medical Centre of Amsterdam . They all contain a rich trove of teratological specimens. Although some academic institutions have abandoned their anatomical collections because of apparent legal issues, safety reasons, financial cuts or newly defined priorities, these museums are much more than time capsules with accumulations of curiosities . They can be regarded as vibrant, inspirational, instructive and interdisciplinary academic working environments with scientific and educational potentials that can be exploited in (bio)medical curricula or in resident training programs . However, one might wonder if anatomical museums should still exhibit full-grown dysmorphic fetuses as these types of anomalies are rarely occurring events in modern times. Moreover, one could question whether historical teratological specimens still have a contemporary value in a period of daily evolving medical innovations and molecular technology. These are issues anatomical museums have to deal with on a daily basis [7, 8].
Congenital anomalies have intrigued mankind since the earliest times. Already in ancient cultures terracotta ornaments were fabricated depicting congenital anomalies. These were clearly based upon existing cases, indicating that they were perceived as divinities, omens or even punishments of supernatural origin [9, 10]. Nowadays, people with very diverse backgrounds visit teratological collections residing in medical museums. Knowledge of both the normal and abnormal embryological development is important for both teachers and physicians while medical students and patients have a constantly growing medical knowledge and ask more sophisticated questions . This implies that a teratological collection can be of great value to educate people about human development. Although several anatomical museums expose teratological specimens, most institutions lack detailed external and internal (dys)morphological descriptions or imaging. Because of this, collections are often stigmatised as “morbid cabinets”.
The teratological collection of the Museum for Anatomy and Pathology in Nijmegen, The Netherlands, currently possesses 72 specimens. It was collected by Albert Verhofstad (deceased 2008), who was affiliated to the Radboud University Medical Centre in Nijmegen, between the 1950s and 1970s. The collection originates from before the ubiquitous availability and utilisation of (high-resolution) ultrasound for prenatal screening and therefore most specimens are full-grown fetuses or newborns. Nowadays full-grown fetuses with severe congenital anomalies are rarely born in well-developed countries. This implies that teratological collections become more valuable with time.
Here we report on the radiological imaging results and we describe four fetuses (cases 1–4), in which new diagnoses or interesting morphological characteristics were established. Furthermore, we discuss the scientific and educational benefits that can be gained from radiological imaging of dysmorphic fetuses. The purpose of this paper is to present an approach to create an innovative teratological exposition in order to de-stigmatise and to more profoundly educate the (bio)medical student and professional.
The entire collection of 72 teratological fetuses was visually inspected and re-described according to contemporary syndromological views by a panel of experts in 2012 (R.J.O., A.N.S.F. and L.L.B.). Verification of the identified syndromes and sequences was obtained by consulting peer groups and contemporary handbooks on clinical syndromology [12, 13]. Several anomaly groups were defined according to the classification of congenital anomalies described by the European Surveillance of Congenital Anomalies . Radiological imaging was used to generate detailed images of the internal (dys)morphology. An inclusion criterion for radiological imaging was that the specimen had not been previously subjected to autopsy in the area of interest. Furthermore, the group with neural tube defects consisted of 20 fetuses. From these fetuses, six fetuses were selected: three that displayed iniencephaly and three with a variety of other neural tube defects. This resulted in the radiological imaging of 41 specimens. Radiological imaging consisted of a total body MRI and total body CT; scanning protocols are described below. Prior to scanning, the specimens were taken out of their jars, thoroughly rinsed with demineralised water and placed in disposable plastic bags to prevent dehydration during imaging. After imaging, the specimens were replaced in a 4% formaldehyde solution. Radiological data were reviewed by three radiologists with expertise in paediatric neurological (K.K.v.U.), cardiothoracic (D.G.H.B.) and abdominal/musculoskeletal (W.M.K.) radiology, all with previous expertise in fetal post-mortem imaging.
Summary of the MRI sequence parameters
Flip angle (°)
T1w flash 3D
∼0.5 × 0.5 × 0.5
T2w TSE 3D (SPACE)
∼1.2 × 0.7 × 0.5
Scan <16 cm
Scan >16 cm
80 ∙ 0.5
Diagnostic revision in 41 scanned teratological fetuses
Diagnosis after radiology
Ventral body wall defects
- ventral body wall defect with cleft lip and encephalocele
- ventral body wall defect with neural tube defect
- ventral body wall defect (3×)
- amniotic band sequence with concomitant ectopia cordis, unilateral CLP and unilateral temporal encephalocele
- vascular disruption sequence with concomitant occipital encephalocele and gastroschisis
- OEIS complex with concomitant omphalocele
- OEIS complex with concomitant gastroschisis and ambiguous genitalia
- OEIS complex with concomitant gastroschisis and spina bifida
Skeletal dysplasias (osteochondrodysplasias)
- achondroplasia (3×)
- thanatophoric dysplasia type I (case 1)
- osteogenesis imperfecta type II (case 2)
- short-rib polydactyly syndrome; not otherwise specified
- oropharyngeal teratoma/epignathus
- conjoined twins (9×)
- thoracoileopagus tribrachius
- thoracoilieopagus tetrabrachius
- ischiopagus tripus
- ischiopagus tetrapus
- diprosopus tetrophthalmus diotis with concomitant craniorachischisis totalis
- parapagus dicephalus dibrachius dipus (case 3)
Syndromes with multiple congenital anomalies
- syndrome (2×)
- Meckel-Gruber Syndrome
- bilateral schisis (most likely trisomy 13)
- tetra-amelia syndrome (case 4)
- sirenomelia (7×)
- isolated sirenomelia type I (3×)
- isolated sirenomelia type II
- VACTERL association with concomitant sirenomelia type II
- VACTERL-H association with concomitant sirenomelia type I
- VACTERL-H association with concomitant sirenomelia type II
- cyclopia (6×)
- alobar HPE (4×)
- alobar HPE with concomitant otocephaly (2×)
Neural tube defects
- iniencephaly (3×)
- occipital encephalocele/exencephaly
- craniorachischis totalis
- iniencephaly with concomitant semi-lobar HPE and omphalocele
- iniencephaly with concomitant myelomeningocele
- occipital encephalocele/exencephaly
- craniorachischis totalis
- unknown diagnosis
- unknown diagnosis
Although many anatomical museums display teratological fetuses on a smaller or larger scale, these displays usually lack comprehensive pathogenetic storylines, additional radiological imaging of the exposed specimens, and most importantly, they often neglect their potential value in biomedical curricula. Furthermore, the diagnoses that fetuses bear are often incomplete, incorrect or outdated. As we demonstrated here, radiological imaging combined with contemporary dysmorphological knowledge was in most cases valuable or even essential to arrive at the correct diagnosis and to unveil the internal and sometimes unexpected peculiarities. Nowadays, many congenital and inherited anomalies can be diagnosed genetically. However, embalmed museological specimens frequently have fragmented and contaminated DNA, which is unsuitable for genetic exploration of candidate genes. We tried molecular inversion probe (MIP) techniques for targeted sequencing of genomic regions with potential candidate genes of multiple fetuses; unfortunately, without satisfactory results.
Cases 1 and 2 concern two distinct skeletal dysplasias, or osteochondrodysplasias, most of which originate from genetic defects that cause aberrant histological formation, growth and maturation of osseous and/or cartilaginous tissues. They usually affect all skeletal elements equally, leading to a decreased postural length (dwarfism). Therefore, skeletal dysplasias can be seen as generalised qualitative disorders of the skeleton, without primarily affecting the body plan . Although achondroplasia is a specific diagnosis among the more than 300 skeletal dysplasias presently known, it has long been used as a generic term for any type of skeletal dysplasia, as it was in the cases described here. Despite the decalcification of the skeleton, which was probably largely caused by decalcification of the bone tissue due to the acidification of formalin through time , radiological imaging made it possible to diagnose TD type I in case 1 and OI type 2 in case 2. TD is genetically related to (true) achondroplasia but it is much more severe, whereas OI is caused by a genetic defect in collagen formation, which leads to (extremely) brittle bones. The imaging results demonstrate the pathogenesis, severity and potential lethality of the conditions in these cases, which markedly adds to their didactic value.
Case 3 concerns a pair of conjoined twins. Despite being a rare congenital malformation with an incidence of 1:200,000 live births and 1:200 monozygotic twins, it is a widely known phenomenon among scientists and laymen alike . For many centuries, multiple rather enigmatic pathogenic hypotheses have been postulated, none of which satisfactorily explains their pathogenesis and conjunctional morphology. An intriguing, though not undisputed theory was postulated by Spencer in 2003 . Her model hypothesises the presence of two (instead of one) embryonic primordial discs “floating” on the surface of a shared yolk sac (resulting in ventral and lateral conjunction types) or on a shared amniotic cavity (resulting in dorsal/neural conjunction). This “spherical coalescence” theory therefore postulates a secondary, symmetrical or asymmetrical, homologous conjunction of initially separate embryonic discs and subsequent embryonic fusion. The nature and extent of the conjunction result from the initial reciprocal distance and position of the two primordial discs on the yolk sac or amniotic cavity. Case 3 concerned a parapagus dicephalus dibrachius dipus conjoined twin, which can be concluded from external dysmorphological findings. However, radiological imaging revealed the intricate internal morphology and conjunction of organs, such as the heart and liver in this specific type, which is essential to understand the pathogenesis of conjoined twinning.
Finally, case 4 presented with tetra-amelia syndrome: an extremely rare disorder characterised by the absence of all four limbs. Infants are often stillborn or die perinatally due to lung hypoplasia and concomitant anomalies such as microstomia and micrognathia. No estimates on prevalence are described due to its rarity. After radiological imaging, we found a diaphragmatic hernia in concomitance with tetra-amelia: this is only rarely found and scarcely described in the modern literature [17, 22]. Although, diaphragmatic hernia is atypical in tetra-amelia syndrome, the acquired images can be used to educate the medical students on the subjects of congenital diaphragmatic hernias and the secondary effect on thoracic organ development.
The most convincing argument for the radiological imaging of a collection of teratological fetuses is the dramatic increase of internal dysmorphological insight obtained in a non-invasive manner. Although many teratological fetuses can be diagnosed and used in an educational setting based on their external dysmorphological appearance, radiological imaging increases the diagnostic value immensely in specifying anomaly subtypes (e.g. in sirenomelia), re-diagnosing anomalies (e.g. skeletal dysplasias) or in teaching certain embryologically oriented pathogeneses (e.g. conjoined twins). Moreover, radiological findings can strengthen arguments regarding pathogenetic hypotheses and thus lead to new or improved insights.
Because of currently available prenatal screening options, pregnancies complicated by congenital anomalies are often terminated well before full-term development. Nowadays, stillborn fetuses in general, let alone fetuses with rare congenital anomalies, are almost never assigned to scientific body donation programs. This results in an absence of supplementing teratological collections, which makes historical specimens of teratological full-term fetuses increasingly valuable and irreplaceable.
We posit that when well-defined teratological specimens are displayed respectfully with additional pathognomonic storylines and radiological data, these exhibitions are educationally legitimate and instructional for any museum visitor. The acquired radiological data are essential to educate the student and the resident on the subject of teratology. Additionally, these high-resolution radiological images can be used to help the obstetrician to recognise congenital anomalies during prenatal screening. Radiological techniques transform the “old and dusty” anatomical museums into modern academic and dynamic working environments suitable to educate the student as well as the (paediatric) radiologists in training. Moreover, radiological imaging of teratological collections makes students wonder and enthusiastic about the use of radiology in their curriculum and learn to compare images with the observed (museological) specimen. Finally, radiological findings can strengthen arguments regarding embryologically oriented pathogenetic hypothesises. By imaging and re-diagnosing teratological specimens that display a similar condition congenital anomalies can be studied beyond the limitations of single case studies and the spectrum or heterogeneity of a congenital anomaly becomes more clear. Therefore, we conclude that teratological collections are a treasure chest for radiologists, paediatricians, geneticists, pathologists and embryologists, and are of interest for additional (re)describing and imaging following new imaging techniques.
Teratological specimens are becoming increasingly rare and deserve a prominent place in anatomical museums. These collections are very suitable for contemporary teratological research and can be used for public and medical education. As shown in this paper, radiological imaging is essential to reveal all the diagnostic ins and outs of old teratological specimens.
We thank the Reinier Post Foundation of the Radboud University Nijmegen (The Netherlands) for their support in the grant entitled “The anatomical museum of the future”. Furthermore, the authors are greatly indebted to Mr. Tim Rijnhout for his pictorial support.
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