2021 年 8 巻 1 号 p. 739-746
Saccular limited dorsal myeloschisis (LDM) is characterized by a fibroneural stalk linking the saccular skin lesion to the underlying spinal cord. Since untethering surgery during the early postnatal period is often indicated to prevent sac rupture, saccular LDM should be distinguished from myelomeningocele (MMC) during the perinatal period. We treated two patients with the spinal cord deviation from the spinal canal to the sac, which mimicked a prolapse of the neural placode into the MMC sac. In patient 1, pre- and postnatal magnetic resonance imaging (MRI) revealed that the spinal cord was strongly tethered to the thick stalk. During surgery, the dorsally bent cord and stalk were united, and the border between these two was determined with intraoperative neurophysiological mapping (IONM). In patient 2, the spinal cord was tethered to two slender stalks close to each other, which was visible with the combined use of sagittal and axial postnatal three-dimensional heavily T2-weighted imaging (3D-hT2WI). The preoperative MRI hallmark of saccular LDM is the visualization of a stalk that links the bending cord and sac. Complete untethering surgery to return the cord into the spinal canal and correct its dorsal bending is recommended.
The term limited dorsal myeloschisis (LDM) was first described as a distinct clinicopathological entity of spinal dysraphism by Pang et al.1–4) LDM is thought to originate from a small segmental failure of the dorsal closure of the neural folds during primary neurulation. At the focal limited non-closure site, the disjunction between the cutaneous and neural ectoderms is impaired. This results in a retained fibroneural stalk linking the skin lesion and the dorsal spinal cord, which results in the tethering of the cord.1–4) The recommended treatment consists of a prophylactic untethering of the stalk from the cord.1–4)
Based on the skin manifestation, LDMs were originally categorized as saccular and non-saccular (flat).1,2) Saccular LDM consists of a skin-based cerebrospinal fluid (CSF) sac topped by a squamous epithelial dome, whereas the flat LDM has a squamous epithelial flat surface or a sunken crater or pit typically called a “cigarette-burn” skin lesion.1–6) Recently, we reported a human tail-like cutaneous appendage as an additional morphological type of skin lesion.7–10) Between April 2015 and December 2020, 23 Japanese LDM patients underwent initial untethering surgery at our hospitals. The external skin lesions were flat in 13 patients, saccular in 5, and tail-like in 5.
The preoperative diagnosis could be made based on the presence of the stalk that connects the skin lesions and the dorsal spinal cord on magnetic resonance image (MRI).1–4) However, in infants with slender stalk, it is often difficult to diagnose with MRI.4–6,11) Although the central histopathological feature of an LDM stalk is the presence of a glial fibrillary acidic protein (GFAP)-immunopositive neuroglial tissue in the fibrocollagenous stalk, a hallmark of the stalk’s origin from the non-dysjunctioned neuroectoderm,1–4) immunopositivity for GFAP was observed in approximately 50% of pathologically examined cases.4–6) Thus, the clinical diagnosis of LDM should be based on comprehensive analysis of clinical, neuroradiological, operative, and histopathological findings.4–6)
For the saccular LDM, untethering surgery during the early postnatal period is often indicated, unlike for flat and tail-like LDM, because it prevents rupture of the sac or a major hindrance to proper handling of the baby.1–6,11–13) Therefore, saccular LDM should be distinguished from open spinal dysraphism centered on a myelomeningocele (MMC) during the perinatal period.11,13–15) MMCs generally have poor functional outcome; however, LDMs can have good outcomes with appropriate untethering surgery.1–3,11,13–15) Among the five saccular LDMs, two patients had spinal cord deviation from the spinal canal to the sac, probably due to the fairly strong tethering effect, which mimicked a prolapse of the neural placode into the MMC sac. We, herein, describe these cases and discuss the diagnostic and surgical strategies.
A 19-year-old primigravida was referred to us at 32+2 weeks of gestation, following the detection of a CSF-filled mass in the lumbar region on ultrasound (US) examination. Prenatal MRI at 33+3 weeks, including half-Fourier acquisition single-shot turbo spin-echo sequence (HASTE) image, demonstrated severe dorsal bending and deviation of the cord to the sac out of the spinal canal due to the tethering effect of the thick stalk attached to the sac. The spinal cord bent approximately at right angles and ran dorsally to attach to the inner wall of the sac before running ventrally back into the spinal canal (Fig. 1a). However, the bending cord and stalk were united and the boundary was not determined. No hydrocephalus or Chiari malformation was observed.
The baby boy weighing 2760 g was delivered, with Apgar scores of 8 and 8, via a scheduled cesarean section at 37+3 weeks. Physical examination revealed a dorsal midline sac measuring 42 × 35 mm in the upper lumbar region, which was torn during delivery (Fig. 1b). He had no neurological deficits. Postnatal MRI examination, including three-dimensional heavily T2-weighted imaging (3D-hT2WI) confirmed a severe dorsal bending and deviation of the cord to the sac, and out of the spinal canal, at the L1-L2 vertebral level (Fig. 1c) while the sac was collapsed. The bending cord and stalk were united, similar to the findings of prenatal MRI.
On the next day after birth, untethering and repair surgery for the sac were performed. Opening the sac with a widening of the tear, a thick stalk and tethered cord, which measured 8–9 mm in diameter and 15 mm in length together, emerged from the orifice of the spinal canal and attached to the wall of the sac (Fig. 1d, e-1). A skin erosion was noted on the outer surface of the sac where the stalk was attached. The border between the spinal cord and stalk could not be distinguished, and nerve root-like structures were found near the orifice of the spinal canal (Fig. 1e-2). This border was neurophysiologically determined by tracing the evoked compound muscle action potentials (CMAPs) of the external anal sphincter muscle, hamstring, and gastrocnemius with direct bipolar stimulation with 2 mA intensity starting from the functional cord and continuing to the non-functional stalk. The CMAPs were evoked following stimulation at 0–5 mm from the orifice of the spinal canal; no CMAPs were evoked following stimulation at 10 mm or more peripheral from the orifice (Fig. 1f). The stalk was severed at 10 mm from the orifice. The cut edge was approximated with a pial suture and returned to the spinal canal. Due to the small size of the orifice, the anatomical relationship between the cord and stalk was not determined.
Postoperatively, de novo neurological abnormalities were not observed. MRI performed on the postoperative 25th day demonstrated that the dorsal bending of the cord markedly improved due to the successful untethering of the cord, although 5 mm of the stalk persisted (Fig. 1g). Hydromyelic central canal distended the remnant stalk. Histopathologically, the resected stalk included a fibrocollagenous tissue embedded with GFAP-immunopositive neuroglial tissues (Fig. 1h and 1i). The sac was covered with finely jagged squamous epithelium, except for the attachment of the stalk.
During the patient’s 11-month postoperative follow-up, his development was normal, without neurological deficits.
Patient 2A 32-year-old, gravida 3, para 2 woman was referred to us at 29+2 weeks of gestation, following the detection of a CSF-filled mass in the lower thoracic region, ventriculomegaly, and Chiari malformation on US examination. Prenatal MRI at 31+1 weeks did not reveal the anatomical relationship involving the cord, stalk, and sac, although the dorsal tenting of the subarachnoid space continuous with the sac was demonstrated (Fig. 2a). Hydrocephalus and Chiari malformation were also observed (Fig. 2b and 2c).
At 37+2 weeks, labor was pharmacologically induced because of planned delivery. The mother vaginally delivered a male neonate weighing 2882 g with Apgar scores of 9 and 9. Physical examination revealed a dorsal midline sac measuring 42 × 33 mm, with small blood vessels on the surface at the lower thoracic level (Fig. 2d). He had no neurological deficit. Sagittal 3D-hT2WI images showed severe dorsal bending and deviation of the spinal cord to the sac out of the spinal canal at the T8–T10 vertebral levels, but it did not show the stalk (Fig. 2e). Serial axial 3D-hT2WI images demonstrated that the stalk was attached to the rostral part of the sac (Fig. 2f-1) and the tethered cord deviated to the sac (Fig. 2f-2, 3, 4). The existence of another slender stalk was suspected (Fig. 2f-5), and the caudal cord returned to the spinal canal (Fig. 2f-4, 5, 6). Type II split cord malformation (SCM) was observed at the caudal cord to the dorsally bending site (Fig. 2g). Cranial MRI showed ventriculomegaly with subependymal nodular heterotopias on the both sides (Fig. 2h) and Chiari malformation (Fig. 2i).
On the next day after birth, following the placement of Ommaya’s reservoir, untethering and repair surgery for the sac were performed. Opening the sac (Fig. 2d), two stalks linking the bending cord, protruding from the orifice of the spinal canal, and inner wall of the sac were observed after dissecting the surrounding connective tissue (Fig. 2j and k). The rostral and caudal stalk had the following diameters; 1.6–2.0 mm and 0.4–0.8 mm, respectively. Each stalk was severed at the attachment with the cord, and the cord was returned to the spinal canal.
Postoperatively, de novo neurological abnormalities were not observed. MRI performed on the postoperative 39th day demonstrated that the cord returned to the spinal canal after successful untethering surgery (Fig. 2l, m-1, 2). The dorsal bending of the cord improved to an extent, but it persisted. The hydromyelic central canal was observed at the stalk attachment. Ommaya’s reservoir was replaced by a ventriculoperitoneal shunt on the postoperative 77th day.
Histopathologically, the rostral stalk included a fibrocollagenous tissue embedded with GFAP-immunopositive neuroglial tissues (Fig. 3a) containing several neurons (Fig. 3b). The attachment of the rostral stalk to the sac had a partial ependymal lining and was densely infiltrated with neutrophils (Fig. 3c). The caudal stalk also included a fibrocollagenous tissue embedded with GFAP-immunopositive neuroglial tissues, an endodermal cyst lined by bronchial epithelium (Fig. 3d), peripheral nerve bundles, and arachnoid villi-like structures (Fig. 3e). The sac to which the caudal stalk attached was covered by keratinizing stratified squamous epithelium with angiomatous dilated blood vessels (Fig. 3f).
During the patient’s 10-month postoperative follow-up, his development was normal, without neurological deficits.
According to the original description by Pang et al,1,2) some LDM stalks are stout, and their tethering effects on the spinal cord are obvious. The tension in the stalk is illustrated by a dorsally tented thecal sac at the point of dural penetration, and the cord is also tented dorsally at the stalk-cord union. However, there are no reports of cases with the spinal cord deviations from the spinal canal into the sac. In this report, the spinal cord was strongly tethered to a thick stalk in patient 1 and two slender stalks that were close to each other in patient 2.
The prenatal imaging hallmark of saccular LDM is the visualization of a stalk that links the cord and sac,11,14,15) while that of MMC is the presence of neural placode in the sac continuous from the cord.16–19) Although prenatal MRI sequences such as HASTE or fast imaging with steady precession allow the acquisition of diagnostic images within a reasonably short time, their shortcoming is the necessity to increase the slice thickness.11,19) The 3- to 5-mm-thick sections obtained by prenatal MRI in the present study provided sufficient image of the thick stalk in patient 1 and the prenatal diagnosis of LDM was possible; however, the details of the slender stalks in patient 2 were insufficient.11) Complication of hydrocephalus and Chiari malformation are common in patients with MMC16–19) but rare in those with LDM.11) However, the complications of these pathologies on prenatal MRI do not deny the diagnosis of LDM, as demonstrated in patient 2 who had subependymal nodular heterotopias in addition to these anomalies.
We previously reported the utility of postnatal 3D-hT2WI in demonstrating a slender stalk in saccular LDM patients.5,11,12) However, we could not observe the two slender stalks on sagittal 3D-hT2WI for patient 2. This is probably because 1.25-mm-thick sections in the present study are still insufficient to demonstrate the details of a slender stalk, which could be overcome with the additional use of axial 3D-hT2WI,5,11) as was demonstrated in patient 2. Thus, the postnatal diagnosis of LDM was possible in patient 2.
Since the diagnosis of LDM was made based on the preoperative MRI (prenatal MRI in patient 1 and postnatal MRI in patient 2), the primary purpose of surgery was cord untethering. During surgery, it is recommended to sever the LDM stalk at the cord attachment and resect the entire length of the stalk,1–4,20,21) which could be performed in patient 2. However, in patient 1, we could not morphologically distinguish the border between dorsally bended cord and the LDM stalk under an operative microscope, and this border was determined by intraoperative neurophysiological mapping (IONM). However, postoperative MRI demonstrated that the cord–stalk attachment was located 5 mm farther to the central side. To prevent the current spread through the CSF during IONM, which could result in false-positive findings, we ensured that the operative field was dry. We think that it could not be completely prevented because the tissue itself contains water.
Another purpose of untethering surgery in these two patients is to return the cord into the spinal canal and correct its severe dorsal bending. Although the former purpose was achieved in both cases, the latter purpose has not been fully achieved in patient 2. The cause is not clear, but it may involve physiological kyphosis of the thoracic spine. Since both of the remnant thick stalk in patient 1 and the dorsal bending of the cord in patient 2 may cause the re-tethered cord syndrome,22) close observation with repeated MRI is needed.
Another noteworthy finding on postoperative MRI was the development of syringomyelia immediately rostral to the stalk–cord attachment. The caudal pole of the syrinx extended to the stalk at the attachment instead of the caudal cord. This finding was consistent with our previous report and further supported the idea that herniation of the hydromyelic central canal to the stalk is a possible pathophysiological mechanism underlying syringomyelia development.12) Since the natural course of LDM-associated syringomyelia is still unknown,8,12) close observation is also important in this regard.
All of the stalks in patient 1 and two stalks in patient 2 had GFAP-immunopositive neuroglial tissues in the fibrocollagenous stalk, which is a typical histopathological finding of LDM.1–6) In patient 2, the attachment of the rostral stalk to the sac had a partial ependymal lining. This finding may support the idea that segmental myelocystocele is involved in the development of saccular LDM.1–4,12)
A notable histopathological finding of the caudal stalk in patient 2 was the presence of endodermal (neurenteric) cyst. The development of the endodermal cyst may be involved in the type II SCM in patient 2, as demonstrated by previous authors, including us.1,2,5) The embryogenesis is thought to involve dorsally displaced endodermal stem cells through the reminiscent of the ventrodorsal endomesenchymal tract that traverses the entire embryonic plate from the amniotic cavity to the yolk sac.23,24)
We thank Dr. Tadahisa Shono, Department of Neurosurgery, Harasanshin Hospital for supporting our study. We thank Editage for editing a draft of this manuscript.
Written informed consent was obtained from the parents of the children for the publication of this case report
This work was partly supported by the Research Foundation of Fukuoka Children’s Hospital.
Kurogi A, Morioka T, Murakami N, and Suzuki SO: Study design and project outline. Kurogi A, Takafumi Shimogawa, Nobutaka Mukae, Matsuo Y, Imamoto N, and Tateishi Y: Data acquisition, analysis, and manuscript drafting. Morioka T, Murakami N, and Suzuki SO: Critical revision of the manuscript and figures.
The authors declare that they have no conflicts of interest.
