Transverse limb deficiency of the upper extremities

In the final months of the year 2023, a ruling of the Austrian Supreme Court of Justice (OGH) caused concern and uncertainty among many colleagues specialized in prenatal ultrasound examinations. In short, an Austrian gynecologist was found liable for damages and is required to assume all child maintenance costs because he failed to detect the complete absence of the fetusʼs left arm (amelia) during multiple ultrasound examinations conducted in 2018 including first-trimester screening and second trimester anomaly scan (OGH 3 Ob 9/23 d dated 11/21/2023).

The circumstances of the failure to detect the malformation are not known to the author and will not be discussed further. However, the case is used as an example for investigating the following questions:

• Classification, etiology, and prevalence of transverse limb deficiency of the upper extremities

• Ability to visualize the extremities with ultrasound and detection rates of transverse limb deficiency of the upper extremities

• Quality criteria for sonographic screening examinations affecting the extremities

• Current legal approaches

• Consequences for physicians performing prenatal ultrasound examinations

Transverse limb deficiency

Classification

Malformations of individual extremity sections can be systematically classified according to Swanson. More complex classifications have also been proposed [1] [2] [3].

The term peromelia refers to transverse limb deficiency, particularly of the upper limbs [4]. The upper limb is truncated with the level of the defect being variable and being able to affect, for example, the hand, the forearm, or the entire arm, with the latter being referred to as amelia ([Fig. 1]).

Fig. 1 Terminal transverse limb deficiency, data according to Girsch et al. [4].

Prevalence

In the European network of population-based registries for the epidemiological surveillance of congenital anomalies (EUROCAT), transverse limb deficiency occurred at a rate of 0.41–0.99 per 10 000 births in the years 2011–2021 ([Table 1]).

Table 1 Prevalence of transverse limb deficiency of the extremities per 10 000 births in the period 2011 to 2021 (without genetic anomalies), data from EUROCAT (https://eu-rd-platform.jrc.ec.europa.eu/eurocat/eurocat-data_en).

	2011	2012	2013	2014	2015	2016	2017	2018	2019	2020	2021
All cases	0.64	0.48	0.58	0.41	0.54	0.64	0.46	0.47	0.64	0.41	0.99
Live births and stillbirths ≥ 20 gestational weeks	0.37	0.26	0.37	0.18	0.36	0.35	0.23	0.22	0.34	0.16	0.54
Pregnancy termination	0.27	0.22	0.21	0.23	0.19	0.29	0.24	0.25	0.3	0.25	0.45

A search specifically for amelia yields a prevalence of 0.14–0.24 per 10 000 and 0.063 per 10 000 live births [5] [6]. Therefore, these are rare malformations.

Etiology

The limb buds of the upper extremities form approximately in the 4^th gestational week and develop from proximal to distal [7]. The limb bud contains mesodermal cells that later differentiate to form muscles, nerves, blood vessels, and bones. The apical ectodermal ridge (AER) forms at the distal tip of the pair of primordial limb buds. The AER continues the extension of the limb buds in the proximodistal direction in that fibroblast growth factors (FGF) are continuously produced with a plurality of additional genes also being involved in the development of the extremities [8] [9]. Near the end of the 8^th gestational week, the entire upper extremity is formed and contains all relevant anatomical structures like cartilage, joints, and soft tissues [10] ([Fig. 2]).

Fig. 2 Development of the extremities in the a) 5^th, b) 6^th, and c) 8^th gestational week according to [10].

The cause of peromelia has not yet been fully clarified. However, it is assumed that hypoperfusion disrupts AER development [11]. This can be attributed to vaso-occlusive events and vascular causes like thromboses, vasospasms, and embolisms [12] [13] [14]. Other etiologies include maternal thrombophilia [15], alpha thalassemia [16], and cocaine abuse [17].

Another rare cause of reduction defects is the amniotic band syndrome in which amniotic strands wrap around and constrict a normally developing body part (e. g. lower arm, hand, or foot), resulting in amputation [18]. Secondary amputations due to amniotic bands with amniotic bands can usually be clearly differentiated from the primary causes postnatally.

Ability to visualize the extremities on ultrasound

High-resolution ultrasound devices and transvaginal ultrasound probes make it possible to track and document the development of the extremities in early pregnancy. In the early fifth week of embryogenesis, the buds of the upper and lower extremities are visible as protuberances from the ventrolateral body wall. The limb buds continue to grow between the fifth and the eighth week until the extremities assume their final form [10].

Fetal extremities can be effectively visualized in the first trimester via transvaginal ultrasound, with three-dimensional imaging allowing visualization of the presence of all 4 extremities on 1 image ([Fig. 3]).

Fig. 3 Transvaginal 3D-imaging of the entire fetus at a) 10 + 3 gestational weeks and b) 12 + 2 gestational weeks.

During detailed first-trimester anatomy screening between 11 + 0 and 13 + 6 gestational weeks, the extremities can typically be effectively evaluated to ensure that they are fully developed, since the arms and legs of the fetus can be visualized on ultrasound based on the slight flexion of the proximal joints and extension of the distal joints. The presence of the 3 segments of each extremity can and should be documented [19] [20]. The hands are usually open so that in some cases even the shape and number of fingers can be examined. However, this is not required for screening. Even in the case of suboptimal scanning conditions, a sufficient check for the presence of the 3 segments of the upper extremities can typically be performed in the first and the early second trimester ([Fig. 4]).

Fig. 4 Image of a fetal upper extremity at a) 11 + 6 gestational weeks, b) 13 + 5 gestational weeks, and c) 16 + 6 gestational weeks with slightly limited visibility. Image c) shows only one forearm bone due to the angle of the probe. However, both bones should ideally be able to be visualized as in images a) and b). If this is not possible, additional planes showing the presence of both bones should be documented.

In this way primarily terminal transverse reduction defects, like the various forms of peromelia, can be effectively detected in the first or early second trimester ([Fig. 5]).

Fig. 5 Peromelia of the left forearm at 13 + 5 gestational weeks on a) 2-dimensional and b) 3-dimensional ultrasound images. The upper arm bone is completely formed while the ulna and radius are only rudimentary. The yellow stars show the location of transverse limb deficiency (source: Prof. Oliver Kagan, University Hospital for Women, Tübingen).

The extremities can usually also be sufficiently visualized during detailed ultrasound scans in the second trimester so that reduction defects can be detected, particularly when they affect large parts of the arms or legs.

Detection rates of transverse limb deficiency of the upper extremities

If malformations of the extremities occur in combination with other severe physical and genetic anomalies, these can often be detected prenatally during routine examinations [21]. Reduction defects of the extremities without associated anomalies are detected significantly less frequently in routine ultrasound examinations since smaller defects or the addition or absence of individual fingers and toes is often present. Depending on the local conditions of the regions participating in the registry, reduction defects are detected prenatally in only approximately slightly more than half of cases according to the data of the EUROCAT registry, with regions with organized screening achieving rates of 80–90 % ([Fig. 6]).

Fig. 6 Prenatal detection rates of limb reduction defects (without genetic anomalies) in the various regions of the European malformation registry EUROCAT in the period 2017–2021.

In studies with systematic screening protocols, the detection rates for transverse limb deficiency in terms of complete absence of a hand, arm, leg, or foot is 100 %, with 75 % of cases already being detected in the first trimester and 25 % in the second trimester [22] [23] [24].

Quality criteria for sonographic screening examinations of the extremities

Recommendations and guidelines regarding the content, processes, and documentation of sonographic screening examinations in pregnancy have been published by national and international societies [25] [26] [27]. The German Society for Ultrasound in Medicine (DEGUM) last published updated quality specifications for performing secondary detailed prenatal ultrasound examinations in the first and second trimester in this journal in the years 2012 and 2016 [19] [28].

The S2e guidelines (085-002) of the Association of the Scientific Medical Societies in Germany (AWMF) on “first-trimester diagnosis and treatment @ 11–13 + 6 gestational weeks” were recently completed and will be published as a short version in one of the upcoming editions of this journal (https://register.awmf.org/assets/guidelines/085-002l_S2e_Ersttrimester-Diagnostik-Therapie@11-13_6_Schwangerschaftswochen_2024-01_1.pdf) [20].

According to the DEGUM recommendations as well as the AWMF guidelines, sonographic visualization of the arms ([Fig. 7]) and legs is obligatory in first-trimester screening, while visualization of the hands and feet is optional ([Table 2]) [19] [20]. A detailed image of the fingers and toes is not required.

Fig. 7 Visualization of extremities during first-trimester screening at 13 + 0 gestational weeks. Image a) shows details of the hand and the forearm and image b) shows both upper extremities.

Table 2 Standard sonographic requirements for fetal anatomy screening and optional parameters for detailed first-trimester screening between 11 + 0 and 13 + 6 gestational weeks [19].

	Standard views	Optional parameters
Skull/brain	Bone of the skull, falx cerebri, chorioid plexus	Intracranial translucency (IT) Brainstem
Face	Profile	Eyes, maxillary and mandible, lips
Neck	Nuchal translucency (NT)[1]	Nasal bone (NB)[1]
Spine		Outline
Heart/thorax	Position, contour Four-chamber view Lungs	Outflow tracts (color) Three-vessel-trachea view Tricuspid flow (TR)[1]
Abdomen	Stomach Abdominal wall	Diaphragm Ductus venosus flow (DV)1 Umbilical arteries and urinary bladder
Extremities	Arms and legs	Hands and feet (Femur, tibia, fibula, humerus, radius, ulna)
Urogenital tract	Urinary bladder	Kidneys
Placenta	Chorionicity, amnionicity (multiples), structure	Position, Insertion of umbilical cord Uterine arteries[1]

The purpose of detailed ultrasound screening in the period between 18 and 22 gestational weeks is to largely rule out or detect anomalies that are visible on ultrasound and indicate a congenital disease or fetal developmental disorder [28]. The fetal body structures visible on ultrasound (= sonoanatomy) are systematically examined. To ensure appropriate quality, guidelines and recommendations have been published. They define the conditions under which these examinations should be conducted, what needs to be documented, and how pregnant women should be counseled [25] [26] [28] [29] [30].

In 2009 in Austria, the Austrian Society for Ultrasound in Medicine (ÖGUM), the Austrian Society for Gynecology and Obstetrics (OEGGG), and the Austrian Society for Prenatal and Perinatal Medicine (ÖGPPM) published criteria listing the parameters to be examined during organ screening [30]. These match with DEGUM recommendations that were published in this journal as well as with recommendations of the ISUOG [25] [26] [28].

In all of these recommendations, examination of the fetal arms and legs with the long bones as well as of the hands and feet is obligatory. However, detailed visualization of the fingers and toes is not considered necessary ([Table 3]).

Table 3 Sonographic parameters to be examined during second trimester screening according to DEGUM and ÖGUM [28] [30].

Head	Outline: Outer contour (cranial bones) at the level of the fronto-occipital plane Internal structures: Cerebral lateral ventricles, chorioid plexus, cavum septi pellucidi, outline of the cerebellum, Cisterna magna Face: Profile including the nasal bone, orbits (optionally, lenses), lips/nose viewed from above
Neck/throat	Outline
Spine	Sagittal longitudinal view + skin contour over the spine, possibly additional transverse views
Thorax	Lungs: Structure Heart: Heart rate and rhythm, qualitative evaluation of size, shape, and position of the heart, 4-chamber view, left and right ventricular outflow tract Diaphragm: Sagittal section of the dome contour
Abdomen	Abdominal wall: Umbilical cord insertion Liver: Position and structure Stomach: Position and size Bowel: Echogenicity, dilation
Urogenital tract	Kidneys: Position and structure, renal pelvis Bladder: Position and shape
Extremities	Arms and legs, hands and feet (without detailed visualization of the fingers and toes), detection of the long bones of the extremities: Femur, tibia, fibula, humerus, radius, ulna

Exact reporting and sufficient image documentation are important for further prenatal care. They are the foundation of quality assurance and control and provide a performance record and forensic validation for the examiner. DEGUM defined which structures need to be documented as images [28] ([Table 4]).

Table 4 Sonographic parameters to be documented as images during second trimester screening according to DEGUM and ÖGUM [28] [30].

1. Skull in the fronto-occipital plane

2. Cerebellum

3. Facial profile with nasal bone

4. Orbits

5. Lips/nose viewed from above

6. Sagittal view of the spine including skin contour

7. Heart: 4-chamber view

8. Heart: Left ventricular outflow tract

9. Heart: Right ventricular outflow tract

10. Sagittal and front views of the diaphragm

11. Transverse section of the abdomen (biometry plane) including the stomach

12. Fetal umbilical cord insertion

13. Kidneys, bilateral

14. Bladder

15. Femur and humerus

16. Tibia and fibula

17. Radius and ulna

18. Hands and feet

19. Location of the placenta

Current legal approaches (primarily in relation to Austria)

The concern was not that damages were awarded but rather the fact that the plaintiff was awarded not only compensation for the additional expenditure resulting from the affected child's disability but also compensation for all maintenance costs for the child. The mother of the affected child argued that she would have terminated the pregnancy if she had been given the corresponding information prenatally, even if that meant receiving treatment outside of Austria. Based on this argument, the OGH concluded that no child would be present if the pregnancy had been terminated in which case there would also be no child maintenance costs. Since termination of the pregnancy was impeded as a result of the negligent examinations by the gynecologist, the court ruled that the child's mother was owed complete compensation for all maintenance costs. The claim to compensation of maintenance costs does not expire until the child becomes financially independent at which point the liability to pay damages will also end.

This interpretation of the law is not new and can be found in comparable “wrongful birth” verdicts. Case law fundamentally assumes that the goal of prenatal screening is to detect developmental disorders and malformations of an unborn child with a further goal of these examinations in prenatal care being to allow the mother (parents) to make a decision about a legally permissible termination of pregnancy in the case of an identified risk of severe impairment of the child. The fact that the decision to terminate a pregnancy in such a case could also be based on the substantial financial costs of caring for a disabled child is “objectively foreseeable so that under these circumstances the financial interests of the mother (parents) are included in the protective purpose of the medical treatment contract” (from OGH 3 Ob 9/23 d). It is, therefore, clear that if proper diagnosis and counseling had been provided, the pregnancy would have been terminated and the plaintiff would not have had to assume maintenance costs for the child. In terms of damages, only the situation with and without the child can be compared. Therefore, the claim to damages cannot be limited to the increase in maintenance costs resulting from the childʼs disability. Such an amount could “only be determined by comparing the disabled child to a fictional healthy child and such a comparison would not only be incorrect in terms of the right to damages but would also represent an approach that is focused on the childʼs disability and is thus discriminatory” (from OGH 3 Ob 9/23 d).

Based on these causality considerations, “the awarding of all maintenance costs is not only consistent but also mandatory: The basis for liability in the ‘wrongful birth’ cases is the failure to detect the impairment of the fetus or the lack of corresponding parental counseling and not causation of the disability. The physician’s actions do not prevent the birth of a healthy child. Instead, the parents’ options in the case of a diagnosed and confirmed fetal impairment – excluding a condition that can be treated in utero – are limited to giving birth to a disabled child or terminating the pregnancy. As a result of the unlawful and negligent actions of the physician, the parents were denied the opportunity to make a decision in favor of the second option” (from OGH 3 Ob 9/23 d).

In the present scenario, the reasoning of the OGH relates “neither to the ‘right of parents to a healthy child’ nor to denying disabled people the ‘right to life’. Instead, the rights of the parents to make an autonomous decision firstly whether they even want a child and secondly whether they, in light of their circumstances, are prepared and able to raise a disabled child and meet its needs” (from OGH 3 Ob 9/23 d).

The OGH also includes the following sentence in the reasons for the judgment: “Special legal solutions to a specific, particularly sociopolitical area of the law – like the present case – must be reserved for the legislative authority. The legislative authority has not yet been able to determine special legal treatment of the legal questions to be answered here” (from OGH 3 Ob 9/23 d). Therefore, it remains to be seen whether corresponding political pressure can change the current legal situation.

Consequences for physicians performing prenatal ultrasound examinations

In light of the judgments and the high payments of damages prominently featured in the media, affected parents will increasingly wonder if their child’s congenital malformation could have been detected prenatally and if they could be legally eligible for financial compensation. This trend can already be seen – at least in Austria – and the author is familiar with multiple similar claims. Although these claims are often unfounded and are ultimately rejected, they are still unpleasant for the affected physicians. However, some claims are understandable from an expert standpoint since the performed examinations did not fulfill the high professional requirements listed above (corresponding to DEGUM level II) and also did not meet with the other quality criteria of a second trimester screening. A significant lack of care and negligent handling of documentation and counseling was discovered in some cases. The fetuses were either not examined systematically and fully in compliance with guidelines or no image documentation was available, no written reports were available, or the person performing the examination did not have the appropriate qualifications. Courts are highly dependent on medical experts, who are tasked with evaluating whether a congenital malformation would have been able to be detected prenatally, whether the examinations were performed with the required care and in compliance with the relevant standards, and whether there would have been a medical indication for termination of the pregnancy. However, such an evaluation requires complete medical documentation. An expert cannot write an expert opinion exonerating the examiner without images or other documents verifying the completeness and technical correctness of the examination. Image archiving should no longer present a technical or financial challenge given the availability of digitalization.

As mentioned above, the legal position is clear. If the required professional and technical criteria cannot be fulfilled, detailed screening examinations should not be offered. Anyone performing ultrasound and claiming to evaluate fetal anatomy is legally liable for the completeness of the examination and for ensuring that the examination is performed lege artis. The days of some doctors using terms like “organ check” and “organ scan” to differentiate from detailed second trimester screening and performing inadequate examinations for commercial reasons are over. If the required standards cannot be met, the pregnant woman must be referred to an examiner who can meet the standards [28] [29] [31] [32]. The 3-level concept of ÖGUM-DEGUM-SGUM allows for these differences in quality.

Of course, there is a risk of failure to detect fetal anomalies even in the case of careful completion of an examination by an appropriately trained and qualified examiner. This requires a separate discussion and written informed consent [28]. To avoid failure to detect missing extremities or parts of extremities, a careful bilateral examination must be performed. A cross-sectional view or a video clip sweeping from one side to the other can be useful here so that both arms or legs can be viewed on one plane in order to show that both upper and both lower extremities were present at the time of the examination ([Fig. 7b]). Especially in the first trimester, 3D-imaging can show the presence of all 4 complete extremities on one image. It is essential to proceed systematically and to work through the corresponding checklists in order to avoid mistakes – even on long days with many consecutive examinations. It is helpful to regularly review all stored images before completing the examination, to check off (in writing) structures that have already been seen or to have an assistant check that the examination is complete. Modern ultrasound devices offer the option of performing this directly on the device or even semi-automatically. A screening examination can only be considered concluded if all structures to be examined have been clearly seen and documented. If needed, the pregnant woman must return at a later date to repeat the examination.

Conclusion:

• Transverse limb deficiency of the upper extremities is rare.

• The presence of arms, legs, hands, and feet is to be documented in detailed systematic examinations performed in the first and second trimester.

• Complete absence of arms, legs, hands, or feet is almost always able to be detected with careful screening examinations. Detailed examination of fingers or toes is not required. Therefore, failure to detect finger or toe anomalies (e. g., polydactyly or the absence of individual fingers) cannot be considered negligent.

• Physicians performing screening examinations, are subject to high liability pressure. The following points must be taken into consideration to address this pressure and meet the requirements:

  • High level of ultrasound examination quality, regular continuing education, recertification of qualifications in accordance with DEGUM level II, updating of devices, documentation,

  • Guideline-compliant examinations with exact photodocumentation of all anatomical structures required in first-trimester and second trimester screening,

  • Counseling of pregnant women about the capabilities and limitations of the particular examination method and about possible causes of suspicion during an examination that could require a repeat of the examination or a referral.

Disclaimer: The author is a court-certified expert but was not involved in any way in the described case.

Prof. Dr. Philipp Klaritsch.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Publication History

Article published online:
04 June 2024