Abstract
Acephalous fetus in a singleton pregnancy is an extremely rare case. In twin pregnancy, it could be presumed as one type of twin reverse arterial perfusion sequence (TRAPS). In this particular case report, the situation was different. An acephalous fetus developed in a singleton pregnancy and may have been a complication of an amniotic band in the very early weeks of gestation. Nevertheless proving it is still a constraint. Despite that, motor findings in utero by using four-dimensional (4D) ultrasound were very interesting to study. Movement of the acephalous fetus is challenging thought on fetal behavior theory, as brain development and function play the central role. The Kurjak antenatal neurodevelopmental tests (KANET) was used to measure the fetal behavior of this acephalous fetus. A comparison with post natal movement findings was also done to provide a better understanding.
Introduction
Recognizing fetal behavior of the acephalous fetus in a singleton pregnancy is considered to be unique. To the best of our knowledge there has been no publication on this before. In the absence of a head and brainmade the spinal cord the only central nervous system (CNS) that control motor function. It is interesting to find how much a spinal cord could process and coordinate sensory information and respond in a motoric fashion.
The Kurjak antenatal neurodevelopment test (KANET) has been known as one of the leading tools to measure fetal behavior in correlation to the CNS structure and function. This test could be done by using a four-dimensional (4D) ultrasound. This case report has shown how the acephalous fetus neurodevelopment performance was by using KANET and also its findings after birth.
Case report
A 27-year-old patient, gravida 2, parity 1, was referred to our center at 33 weeks of gestation. Her prenatal course and family history were unremarkable. There was no relevant medical history and she was taking no other medication. She had a low standard of prenatal care, as she had no first trimester ultrasound or other proper prenatal diagnostics in early pregnancy. The patient was only seen by a midwife for her prenatal care before referral.
An absence of the head and brain was evaluated by using two- and three-dimensional (2D and 3D) transabdominal ultrasound, which confirmed the diagnosis of an acephalous fetus (Figure 1 and Figure 2). The fetal body structure and organs were normal. Fetal echocardiography also showed normal structure and function of the fetal heart. Both arms were normal but remained in the same position (in front of the chest). Although leg malformation was found with bilateral clubfeet, more complex and frequent leg movements were detected. For comparison, a computed tomography (CT)-scan and 3D CT-scan were accomplished. It showed the baby has cervical vertebrae 1 to 7 and all the fetal structures were normal except there was no cranial and facial structure (Figure 3 and Figure 4). Cardiotocography (CTG) was also performed and showed abnormal findings of low variability and no acceleration, showing no parasympathetic and sympathetic counter balance in the fetal heart rhythm.
Fetal behavior was seen by using 4D ultrasound (Voluson 730 Pro, Kretztechnik, Zipt, Austria) and was measured by using KANET. This study was performed at 33 weeks of gestational age (Figure 2). The 4D ultrasound was automatically scanned every 2 s, and 4D images were displayed on the screen. This procedure was used for the observation of fetal hands, legs and body movements (Figure 5 and Figure 6). The session was performed in 30 min and the results were demonstrated in Table 1. Limited isolated hand movement, more variable and complex leg movement, cramped and invariable finger movements were demonstrated in the acephalous fetus. Those parameters were scored 3 for KANET and concluded to be abnormal (score 0–5).
Sign | Score |
Sign score | Observation | ||
---|---|---|---|---|---|
0 | 1 | 2 | |||
Isolated head anteflexion | |||||
Cranial sutures and head circumference | |||||
Isolated eye blinking | |||||
Facial alteration | |||||
Mouth opening | |||||
Isolated hand movement | Cramped | Poor repertoire | Variable and complex | 1 | Abnormal: The movement characterized by a poor repertoire when the sequence of successive components is monotonous and movements do not occur in the complex manner. The movement characterized by cramped when it looks rigid and lack of the normal smooth and fluent character |
Isolated leg movement | Cramped | Poor repertoire | Variable and complex | 1 | |
Hand to face (cranial direction movement) |
Abrupt | Small range (0–5 times of movement) | Variable in full range, many alternation (>;6 times of movements) |
0 | Abnormal: Movement looks abrupt when marked by sudden changes in the subject with sharp transitions |
Finger movement | Unilateral or bilateral clench fist (neurological thumb) |
Cramped invariable finger movements | Smooth and complex, variable finger movements | 1 | Abnormal: Neurological sign of the thumb is demonstrated when the adduction of the thumb in a clenched fist is non reducible. Disturbance in fingers and thumb movements correlated with absence of spontaneous motor activity |
Gestalt perception of GMs | Definitely abnormal | Borderline | Normal | 0 | Abnormal: Poor amplitude, variability and fluency of the movements |
Total score | 3 | ||||
Interpretation | Score (0–5) | Abnormal |
Fetal movement after birth was documented. Prior to elective delivery, the patient came to hospital due to preterm premature rupture of membranes. An emergency C-section was performed and the baby was delivered by shoulder extraction (Figure 7). The baby had a pointed cervical vertebrae with an opened end (Figure 8). Both arms were in the front of the chest and only had few movements. Both legs showed more rigorous and frequent movement (Figure 9). Malformation of legs which were both clubfeet were noticed. Bradicardia was noted soon after delivery and the baby died 2 hours later. Placenta did not show any pathologic appearance. Amniotic membranes could not show prominent abnormality to prevail amniotic band suspicion. Even though this could not exclude this possible etiology.
Discussion
This unique case came without proper examination in the early- and mid-trimester of pregnancy. That has made tracing the etiology very difficult. An undeveloped fetal head as a solitary malformation was in correlation with chemical exposure, infection, or another environment insult has never been shown by any published journals before. There is no literature showing chromosomal anomaly or even a single gene disorder as its origin. An amniotic band in the very early beginning of pregnancy could be assumed as its cause but it is hard to be proven. The structural development of the fetal head occurs between the 3rd and 8th weeks of gestation. Mechanical disturbance from an amniotic band at neck level during this period could cause a vascular blockade, resulting in no further development of the fetal head and brain as has been shown by ultrasound. Cervical vertebra 1 to 7 were found and also confirmed after birth. The CT-scan and the 3D CT-scan examination which followed made for a better understanding for this major malformation. The anatomical structure of fetus was studied in accordance with its function. In this particular case, it is interesting to learn how the motor function was presented by the fetus.
Sporadic gene mutation that causes dysgenesis of neural crest cells might also be a cause. The embryo begins from a planar structure and prepares the development of the CNS in the 3rd week of gestation, firstly from the area of the neural plate (ectoderm). Neural folds are derived from elevation of the ectodermal tissue and the mid-sagital groove of the central ectodermal growth. The neural tube is created by neural folds fusion in beginning in the midline. Invagination of a population of ectodermal cells adjacent to the neural fold then creates the neural crest. Most connective and skeletal tissues of the cranium and face are believed to derive from neural crest cells [1]. Therefore, the dysgenesis of neural crest cells to form the head and neck may be the cause of this acephalous condition, yet it could still be entangled.
Amorphous twins with TRAPS almost always become acardiac. This case showed normal heart structure, function and rhythm in a detailed fetal echocardiography ultrasound. So it could be presumed that TRAPS was unlikely to be the cause. All other related internal organs (lung, gastrointestinal organs, kidney) showed good structure.
Almost all the body’s mechanism are controlled by the CNS which consist of brain and spinal cord. In this case the baby was born without a head and brain. As we know that the brain is needed to process and coordinate all information. It receives information from all around the body and then it process and gives instructions back to the body. A baby born without head is considered to be incompatible to live, as it has been shown in this case, the baby lived for less than 2 hours. The loss of dynamic exchange domination between the parasympathetic and sympathetic drives to the fetal heart rate was shown by poor variability in cardiotocography. This finding matches the condition of having no brain in the acephalous fetus.
The KANET scoring system was performed to assess fetal neurodevelopment that it has been established for the standardization of studies of antenatal neurobehavior on the basis of specific elements of eight behavioral parameters [2], [3]. KANET is based on the 4D ultrasonographic assessment of the fluency/frequency of six behavioral parameters, on the 4D Gestalt perception of general movements, on the appearance of cranial sutures and on one biometrical (head circumference) parameter. The scoring system differentiates normal (10–16), borderline (6–9) and abnormal (0–5) scores for evaluation. KANET was conducted in a scanning 4D ultrasound session over 30 min [4]. According to Prechtl and coworkers, any fetal brain damage will interfere with the endogenous motor activity [5]. Therefore, fetal brain status can be interpreted by spontaneous movements as an expression of neural activity [6], [7]. Sparkling and co-workers had documented the typical hand movement in fetus from 12 to 35 weeks of gestation. Many movements were shown to be straightforward and flexible to a body part or uterine wall and the hands of the fetuses moved with different frequencies and force [8]. Sparling and Wilhelm did another fetal neurobehavioral study from 14 weeks until the neonatal period, they conclude that fetal and neonatal movements appeared to be directed to specific targets to the head and face and the best predictors of neonatal movement were the observations performed at 32 weeks of gestation [9]. Deviations from typical fetal movement patterns have also been observed using 4D ultrasound in at-risk pregnancies with severe intrauterine growth restriction (IUGR) [10] and fetuses with CNS anomalies. Movement patterns in the anencephalic fetus were rigid and inconstant compared to being more flexible in normal fetus. The overall characteristic of movements showed abrubt and jerky movements as stated by Andonotopo [11].
Several parameters of KANET related to head and facial expression were scored zero in this case. Several behavior patterns were observed in the acephalous fetus. The fetal body showed no positional changes. The arms moved only in one direction and were limited in the front area of the chest, and the fingers had no movement. The leg movements also showed a lack of flexibility. The overall movement was abrupt and infrequent. The KANET score was 3 and was noted as being abnormal. This result is equal to the anencephalic case. This equality has given more credence of KANET score to represent fetal neurodevelopment in general. Poor fetal bahavior is consistently shown to be caused by a major defect of the fetal brain or loss of the fetal brain [12]. Yet the spinal cord could, in this case, be shown as having a minor role in motoric instruction. The arm and leg movements of the acephalous fetus seems to be only representing the reflex motion provided by the spinal cord after some sensory information was received by the fetus. This is in line with reflex motion as it is supposed to be: infrequent, imprecise, jerky, and not complex. This would lead to the knowledge that KANET is blend of reflex movements instructed by the spinal cord and voluntary movement instructed by the fetal brain.
No acceleration found during the cardiotocography examination also proves that the movement of arms and legs in the acephalous fetus was only a reflex motion. If it was a centrally derived voluntary movement then it would simultaneously make the fetal heart rate increase and would have shown as an acceleration in the CTG exam.
How the baby could survive for 2 hours and move for 15 minutes after delivery was an interesting question. The spinal cord and spinal nerves, as the peripheral nervous system that connect to the skin, joints, muscle, etc., allowed the transmission of efferent movements as well as afferent sensory signals and stimuli which it could make involuntary motion of muscles as well as sense perception [13].
The spinal cord performs the rhythmical and sequential activation of muscles in locomotion and the spinal locomotion resulted from complex and dynamic interactions between a central program in the lower thoracolumbar spine and proprioceptive feedback from the body in the absence of central control by the brain [14]. The central pattern generator (CPG) within the lumbosacral spinal cord segments represents an important component of the total circuitry that generates and controls posture and locomotion. The CPG provides the basic locomotor rhythm and synergies by integrating commands from various sources [15]. This spinal circuitry can function independently in the absence of input from the brain to generate stable posture and locomotion and even activity to match changing conditions (e.g. stepping over obstacles). This capability can be learned by training and therefore the spinal cord has the capability to learn and memorize [16], [17], [18], [19]. In the case of an acephalous fetus, the spinal circuit below the brain site seemed to stay active instead of became silent and worked in a modified manner [20]. So based on this theory, it explained why the baby still could move.
Conclusion
The etiology of an acephalous fetus could be intriguing although it is hard to prove. Sporadic mutation of gene disorders that causes dysgenesis of neural crest cells and also amniotic bands in very early gestation could be considered as being causal. Monotonous movement was observed in an acephalous fetus by using 4D ultrasound which was concluded as abnormal on the KANET score. The movement before and after birth was identical. There is a fact that the human body still can move even without a head and brain because there is spinal circuitary called the CPG in the lumbrosacral spinal cord segment that can function and provides movement independently. Findings of fetal behavior in this acephalous fetus case has given more credence to the KANET score as a tool for representing fetal neurodevelopment, especially as a blend of spinal and brain development.
Author’s statement
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Conflict of interest: Authors state no conflict of interest.
Material and methods
Informed consent: Informed consent has been obtained from all individuals included in this study.
Ethical approval: The research related to human subject use has complied with all the relevant national regulations, and institutional policies, and is in accordance with the tenets of the Helsinki Declaration, and has been approved by the authors’ institutional review board or equivalent committee.
References
[1] Johnston MC. Embryology of the head and neck. In: McCarthy JG, editor(s). Plastic surgery. Philadelphia, PA: WB Saunders, 1990:2451–95.Search in Google Scholar
[2] Prechtl HF. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23:151–8.10.1016/0378-3782(90)90011-7Search in Google Scholar
[3] Honemeyer A, Talic A, Therwat A, Paulose L, Patidar R. The clinical value of KANET in studying fetal neurobehavior in normal and at-risk pregnancies. J Perinat Med. 2013;41:187–97.10.1515/jpm-2011-0251Search in Google Scholar
[4] Kurjak A, Miskovic B, Stanojevic M, Amiel-Tison C, Ahmed B, Azumendi G, et al. New scoring system of fetal neurobehavior assessed by three- and four-dimensional sonography. J Perinat Med. 2008;36:73–81.10.1515/JPM.2008.007Search in Google Scholar
[5] Cioni G, Prechtl HF, Ferrari F, Paolicelli PB, Einspieler C, Roversi MF. Which better predicts later outcome in full term infants: quality of general movements or neurological examination?. Early Hum Dev. 1997;50:71–85.10.1016/S0378-3782(97)00094-7Search in Google Scholar
[6] Einspieler C, Prechtl HF, Bos AF, Ferrari F, Cioni G. Prechtl’s method on the qualitative assessment of general movements in preterm, term and young infants. London: Mac Keith Press, 2004.Search in Google Scholar
[7] Kurjak A, Andonotopo W, Hafner T, Salihagic Kadic A, Stanojevic M, Azumendi G, et al. Normal standards for fetal neurobehavioral developments – longitudinal quantification by four-dimensional sonography. J Perinat Med. 2006;34:56–65.10.1515/JPM.2006.007Search in Google Scholar
[8] Sparling JW, Van Tol J, Chescheir NC. Fetal and neonatal hand movement. Phys Ther. 1999;79:24–39.10.1093/ptj/79.1.24Search in Google Scholar
[9] Sparling JW, Wilhelm IJ. Quantitative measurement of fetal movement: fetal-posture and movement assessment (FPAM). Phys Occup Ther Pediatr. 1993;12:97.10.1080/J006v12n02_06Search in Google Scholar
[10] Andonotopo W, Kurjak A. The assessment of fetal behavior of growth restricted fetuses by 4D sonography. J Perinat Med. 2006;34:471–8.10.1515/JPM.2006.092Search in Google Scholar
[11] Andonotopo W, Kurjak A, Kosuta MI. Behavior of an encephalic fetus studied by 4D sonography. J Maternal Fetal Neonatal Med. 2005;17:165.10.1080/jmf.17.2.165.168Search in Google Scholar
[12] Visser GH, Laurini RN, de Vries JI, Bekedam DJ, Prechtl HF, et al. Abnormal motor behaviour in anencephalic fetuses. Early Hum Dev. 1985;12:173–82.10.1016/0378-3782(85)90180-XSearch in Google Scholar
[13] Kandel ER, Schwartz JH. Principles of neural science, 5th ed Appleton & Lange: McGraw Hill, 2012:338–43.Search in Google Scholar
[14] Edgerton VR, Harkema SJ, Dobkin BH. Retraining the human spinal cord. Spinal cord medicine: principles and practices Vol. 60. New York: Demos Medical Publishing, 2003:817–26.Search in Google Scholar
[15] Dietz V. Spinal cord pattern generators for locomotion. Clin Neurophysiol. 2003;114:1379–89.10.1016/S1388-2457(03)00120-2Search in Google Scholar
[16] Forssberg H, Grillner S, Rossignol S. Phase dependent reflex reversal during walking in chronic spinal cats. Brain Res. 1975;85:103–7.10.1016/0006-8993(75)91013-6Search in Google Scholar
[17] Dietz V. Spinal cord pattern generators for locomotion. Clin Neurophysiol. 2003;114:1379–89.10.1016/S1388-2457(03)00120-2Search in Google Scholar
[18] Garraway SM, Hochman S. Serotonin increases the incidence of primary afferentevoked long-term depression in rat deep dorsal horn neurons. J Neurophysiol. 2001;85:1864–72.10.1152/jn.2001.85.5.1864Search in Google Scholar PubMed
[19] Rygh LJ, Tjolsen A, Hole K, Svendsen F. Cellular memory in spinal nociceptive circuitry. Scand J Psychol. 2002;43:153–9.10.1111/1467-9450.00281Search in Google Scholar PubMed
[20] de Leon RD, Roy RR, Edgerton VR. Is the recovery of stepping following spinal cord injury mediated by modifying existing neural pathways or by generating new pathways?. Phys Ther. 2001;81:1904–11.10.1093/ptj/81.12.1904Search in Google Scholar
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