First trimester cerebral appearance in the presence of closed spina bifida with myelomeningocele, part of the oeis complex
- Delia Roxana Ungureanu 1,
- Lucian George Zorila 1 , 2,
- Razvan Grigoras Capitanescu 2 , 3 and
- Dominic Gabriel Iliescu 2 , 3
- 1 Obstetrics and Gynecology, University of Medicine and Pharmacy of Craiova Faculty of Medicine, Craiova, Romania
- 2 Obstetrics and Gynecology, Medgin Prenatal Diagnostic Unit, Craiova, Dolj, Romania
- 3 Obstetrics and Gynecology, University of Medicine and Pharmacy of Craiova, Craiova, Romania
- Correspondence to Dr Lucian George Zorila; zorilalucian@gmail.com
Abstract
Our communication presents a prenatally detected case with severe spinal defect detected in the first trimester of pregnancy, accompanied by a large skin-covered myelomeningocele but normal cranio-cerebral structural appearance.
These findings suggest that in the first trimester, the extent of the spinal defect, the cerebrospinal fluid leakage to a large, but skin-covered, meningocele and fixation of the spinal cord at the lesion are not sufficient to determine downward hindbrain displacement and the development of secondary signs for open spina bifida.
Therefore, we suggest a careful evaluation of the fetal cerebral features if a meningocele is detected. The presence of the skin covering the lesion may not be evident in the first trimester, but the absence of intracranial open spina bifida markers may indicate a ‘closed’ spinal defect, which generally associates a good neurological outcome. Also, studies aimed to investigate the accuracy of the intracranial features for open spina bifida detection should consider the possibility of ‘closed’ myelomeningoceles to avoid incorrect correlations.
Background
Spina bifida (SB) malformation is classified as either closed or open defects. The presence of a meningocele sac is associated with open spinal cord defects and significant developmental impairment, while in closed SB cases the clinical manifestations are minor, because the nerve tissue is covered by skin and not exposed outside the body.
A reliable prenatal diagnosis of open SB is feasible as early as the end of the first trimester, by means of direct or indirect signs. Spinal deformation (U-shaped of kyphoscoliosis) and the presence of myelomeningocele represent the direct signs of open SB, indifferently to the gestational age. The indirect signs represent the consequence of developing Chiari type II malformation, that in the first trimester consist in a significantly reduced intracranial collection of cerebrospinal fluid, as an early sign of cerebrospinal fluid leakage. The so-called ‘dried-up brain’ is associated with a decrease in the area of lateral ventricles, roof of the third ventricle and aqueduct of Sylvius in the axial view of the fetal head.1 Scalloping of the frontal bones (the so-called ‘lemon-sign’) may be present in the first trimester, similar with what is seen later in pregnancy.2 Still, the first trimester ‘dried-up brain’ is the opposite of the second and third trimester hydrocephaly detected in open SB cases. Consequently, a BPD (biparietal diameter) below the 5th percentile is present in about half of the first trimester fetuses and a ratio between the BPD and the transverse abdominal diameter lower than 1, in two-thirds of cases.3–5
Posterior fossa abnormalities due to reduced fluid-filled sonolucent spaces represent another useful method for open SB screening in the first trimester of pregnancy, similarly to the second trimester omniprevalent ‘banana sign’. Non-visualisation of the fourth ventricle or intracranial translucency has the potential to detect more than half of the fetuses for a 99% specificity6 while a reduced cisterna magna, below the 5th percentile detects up to three-quarters of the cases.7 Moreover, in the midsagittal nuchal translucency plane, a reduced fluid area,8 abnormal four-line view,9 the absence of one of the three posterior brain spaces10 or abnormal posterior brain biometry regarding measurements of the brainstem, brainstem to occipital bone distance and their ratio11–14 detects nearly all open SB first trimester cases.
As a result of cerebrospinal fluid leakage, the posterior displacement and deformation of the mesencephalon may lead to cerebral peduncles migration close to occipital bone (‘crash sign’).15
The severity of open SB disease is associated with the size of the spinal defect and its early manifestation.16
Closed SB associated with a skin-covered myelomeningocele, also called terminal myelocystocele represents a neural tube defect where an ependyma lined sac herniates through a dorsal spinal defect and constitutes approximately 4%–6.5% of skin-covered lower spine masses.17 18 They are often found in association with omphalocele, exstrophy of the bladder, imperforate anus and sacral agenesis. The presence of abdominal wall defects is associated with higher risk of neurological deficits.17
Our communication presents a case with severe spinal defect detected in the first trimester, accompanied by a large skin-covered myelomeningocele, without indirect cranio-cerebral signs.
Case presentation
A 24-year-old, gravida 2 para 1 woman was referred to our centre for open SB suspected in a 13 weeks of pregnancy fetus. The patient’s medical history was unremarkable. The first trimester combined test yelled a low genetic risk. We decided to perform a detailed ultrasound structural evaluation of the fetus.
Investigations: ultrasound scan
The scan confirmed a spinal lumbosacral defect accompanied by a large myelomeningocele (figure 1A–C). We furthermore suspected body stalk anomaly (BSA) based on the short umbilical cord appearance, embedded in amniotic sheets, infraumbilical abdominal defect with gut herniation and limb anomalies: pelvic asymmetry, fixed adduction deformity of the thighs and bilateral clubfoot with talipes eqinus and varus (figure 2A–F, video 1). However, despite the presence of obvious meningocele, we did not detect the rest of the open SB direct signs, regarding spine deformation. Also, the secondary intracranial signs were absent figure 1D–F, videos 2 and 3). We noted a normal appearance of the skull, cerebral ventricles, Sylvian aqueduct, choroid plexus and thalamus, and normal measurements of biparietal diameter and posterior brain morphometry (brainstem, intracranial translucency and cisterna magna). We further tried to enhance the spine assessment using transvaginal scan. The normalcy of the cranial features was confirmed, but due to the longitudinal fetal ‘stuck’ position with the cephalic extremity close to the cervix, we were unable to properly explore the spinal defect. The only spinal feature confirmed during transvaginal scan was the continuity of the skin underlying the mass protruding in the lumbosacral area.
(A) Spinal defect (*) with absent kyphoscoliosis. (B, C) Lumbosacral thick-walled cyst suggestive for myelomeningocele (arrow). The underlying skin is visible and the abdominal defect (arrow). (D) Normal aspect of the lateral ventricles (lv) and third ventricle (arrow) between the choroid plexus (p). (E) Thalamus (t) in normal place and Sylvian aqueduct with normal appearance (arrow). (F) Posterior brain with normal relations (bs, brainstem; IT, intracranial translucency—fourth ventricle; cm, cisterna magna). (G, H) Transvaginal scan, with evaluation of the brain median and parasagittal structures: t, bs, lv, p, falx cerebri (f). (I) Poor visualisation of the lumbosacral spine, because of the fixed vertical position of the fetus with the caudal part far from the probe. The continuity and integrity of the skin is well seen underlying the lumbosacral bulging mass (arrow). NT, nuchal translucency.
Body-stalk anomaly features. (A) Short umbilical cord evidenced using directional power Doppler, accompanied by omphalocele (O). (B) 3D rendering of the umbilical cord, showing the placental insertion embedded in amniotic sheets, indicated with arrows. (C) Axial pelvic view showing fixed adduction deformity of the thighs with a wide angle between the femurs (F) and the protruding omphalocele (O). (D, E) Bilateral limb anomalies with fixed flexed legs and bilateral clubfoot with talipes eqinus and varus.
Outcome and follow-up
Termination of pregnancy was offered and accepted by parents. Fetuses with SB and intact skin over the myelomeningocele might have a good neurological prognosis,19 but the counselling also provided information regarding the ethicunfavourable BSA prognosis. Although our case lacked many of the major anomalies associated to BSA, such as cardiac disorders or craniofacial defects, several other malformations were present (abdominal wall hernia, spinal defect and limb anomalies). BSA is usually incompatible with life, progressing to miscarriages or stillborn fetuses with only few reports of survival during the neonatal period.20
Medical termination of pregnancy was performed at 14 gestational weeks, according to hospital protocol regarding the investigation of fetal major anomalies. All suspected abnormalities were confirmed at the pathology examination (figures 3 and 4). The large myelomeningocele sac was covered by skin, protruding through a widespread lumbosacral spinal defect and with the spinal cord attached to the sac.
Spinal defect investigation at the pathology examination. (A) Abdominal wall defect with gut herniation (open arrow). (A, B) Lumbosacral bulging (solid arrow) covered with skin. (C, D) Large lumbosacral spinal defect (*) and the continuity of the myelomeningocele (solid arrow) with spinal cord (open arrow).
Features of body-stalk anomaly associated with omphalocele, exstrophy of the bladder, imperforate anus and sacral agenesis complex at the pathology examination. (A, B) Large ventral abdominal defect extended from the umbilical insertion region to the pubic symphysis. (C, D) Absent anus in the perineal area, suggesting imperforate anus. (E) Placenta and umbilical cord aspect, with short umbilical cord embedded in amniotic sheets.
As expected, genetic analysis by means of quantitative fluorescence-PCR and karyotype did not reveal chromosomal anomalies. The literature regarding BSA fetuses reported generally normal genetic findings with few exceptions.21
Discussion
Careful examination of the fetal spine should be part of the routine first-trimester scan for SB screening, as recommended by international guidelines.22 Open SB is difficult to diagnose in the first trimester of pregnancy, as the spine is not yet fully ossified and the ultrasound findings are more subtle, because the secondary Chiari malformation will not have fully developed. However, the understanding of the neurodevelopment in early pregnancy and systematic investigation of secondary cerebral features improve the potential to diagnose neural tube defects.
These findings show that the large extent of the spinal defect, the fixation of the spinal cord at the lesion with secondary traction of the posterior brain and the cerebrospinal fluid leakage to a large meningocele, were not enough to determine downward hindbrain displacement. Apparently, the ‘open’ characteristic, meaning the lack of skin covering the defect is essential for Chiari type II early pathophysiology and manifestations. The features of our case are in line with the hypotheses of a previous ‘closed’ meningocele case report, diagnosed in the second trimester, that did not associate intracranial signs.23 However, in that case, the meningocele was not apparent in the first trimester and the lesion was secondary to a small sacral spinal defect.
The manifestation of cerebral features should not be influenced by the presence of associated malformations as in our case, since they do not interfere with Chiari malformation pathogenic mechanism and there is no evidence in the literature in this direction.
Sonographers should keep in mind that the indirect or secondary cerebral features, which are critical for myelomeningocele detection, are likely to be absent in the advent of skin-covered, or so-called ‘closed’ lesions. This is important, because ‘closed’ SB cases generally associate a good neurological outcome. However, the accurate identification of the skin covering the meningocele may not be possible in the first trimester. Thus, the evaluation of the cerebro-cranial features could indicate the ‘open’ or ‘closed’ type of the spinal defect. Still, the prognosis of prenatally documented ‘closed’ myelomeningoceles was communicated only in few case reports,19 24 therefore more data are needed for proper parental counselling.
Another application of this finding is for research purposes. The studies aimed to investigate the accuracy of the intracranial features to detect open SB should consider the possibility of ‘closed’ myelomeningoceles. The pathology examination is not routinely performed even in research settings and the overlying skin may be damaged during the termination of pregnancy. Thus, the investigators should evaluate carefully the defect type in SB cases in order to avoid incorrect correlations. Some of the myelomeningocele cases reported in the first trimester with normal cerebral ventricular features may be due to the ‘closed’ type of the spinal defect.
Learning points
-
Downward displacement of the hindbrain is not present in closed spina bifida, even in the event of large spinal defects, associated with significant meningocele and the spinal cord fixed at the lesion. Apparently, the lack of skin covering the defect is mandatory for Chiari type II early pathophysiology development and manifestations.
-
The evaluation of the cerebro-cranial features could indicate the ‘open’ or ‘closed’ type of the spinal defect in the first trimester, which is important for parents’ counselling regarding the outcome.
-
Studies aimed to investigate the accuracy of the intracranial features for open spina bifida detection should consider the possibility of ‘closed’ myelomeningoceles to avoid incorrect correlations.
Acknowledgments
The Pathology Laboratory of the University Emergency County Hospital, conducted by Professor Cristiana Simionescu provided the conditions for an appropriate pathology examination for the fetus. Medgin Centre from Craiova provided high resolution equipment for better representation of the fetal anomalies.
Footnotes
-
Contributors DRU and LGZ have a substantial contribution to the design and implementation of the study that takes place in our unit regarding the early detection of fetal CNS abnormalities and their pathology confirmation. RGC contributed to the initial acquisition and analysis of the data. LGZ drafted the manuscript. DGI has a substantial contribution to the interpretation of the data and revised the paper.
-
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
-
Competing interests None declared.
-
Patient consent for publication Obtained.
-
Ethics approval The research comply with the guidelines for human studies and was conducted ethically in accordance with the World Medical Association Declaration of Helsinki. The study protocol was approved by the University’s Committee on Human Research.
-
Provenance and peer review Not commissioned; externally peer reviewed.
- © BMJ Publishing Group Limited 2020. No commercial re-use. See rights and permissions. Published by BMJ.
References
Use of this content is subject to our disclaimer