Tethered cord release in patients after open fetal myelomeningocele closure: Intraoperative neuromonitoring data and patient outcomes

Study Design/Participants

This is a single-center, retrospective observational study at the Children’s Hospital of Philadelphia (CHOP) from 2009 to 2021. The local Institutional Review Board approved this study. The subjects were all patients who had previously undergone fetal MMC closure at our institution and then subsequently returned for tethered cord release. The initial fetal closure was performed at CHOP from 2007 to 2019. All surgical detethering operations were performed by the senior author (G.G.H.). The IONM analysis was performed by a board-certified neurophysiologist (A.J.F.).

Outcomes and Exploratory Measures

The first author (T.M.F.) performed all the chart reviews. The primary outcome was the motor level as determined by IONM. The secondary outcome was the manual motor level as determined postoperatively in the outpatient setting and defined as the best functional myotome documented in the medical record by a physical therapist (K.L.L. or S.R.P.) in Spina Bifida Clinic (graded on the Medical Research Council scale with a strength score of 3/5 as required for myotome level assignment).[14] If a patient had a different motor level on the left and the right, the higher (worse) level was assigned. Testing occurred in patients who could follow commands and participate or was done with clinical observation in young children who could not participate in the motor exam. Exploratory measures were: gender, age at surgery, indication for surgery, the rate of resolution of IONM alerts intraoperatively, and the bony level of defect as seen on prenatal spinal ultrasound. The functional level was determined using the same method as used in MOMS.[2]

Analysis

Study data was collected and managed using REDCap electronic data hosted at our institution.[15] Descriptive statistics (mean, median, and range) were performed with Stata (StataCorp LLC, version 15.1, College Station, TX).

Demographics

From 2009 to 2021, 51 patients (female = 29, 57%) who had previously undergone fetal myelomeningocele closure also underwent tethered cord release. The average age of preoperative assessment by a physical therapist was 2 years, 4 months (median = 1 year, 11 months, range = 1.5 months to 8 years, 9 months). The average interval between preoperative assessment and surgery was 9 months (median = 3 months, range = 0 to 4 years, 7 months). The average age at the time of tethered cord release was 2 years 10 months (median = 2 years, range = 6 months to 15 years, 10 months). The average interval between surgery and postoperative assessment was 12 months (median = 10 months, range = 2 months to 3 years, 5 months). The average age of postoperative assessment by a physical therapist was 3 years, 7 months (median = 3 years, range = 8 months to 10 years, 7 months). The surgical indications were: urologic dysfunction, motor deficits, pain/sensory issues, or radiographic progression. Of these, 35 (62.5%) patients had one indication, 17 (30.4%) had two indications, and 4 (7.1%) had three indications (Table 1). The bony levels of defect are outlined in Table 2. Three patients had more than one complex detethering procedure.

Motor and Sensory Level

The anatomic level, the electrophysiological level, and the manual motor testing level data are reflected in Figs. 1–4. Patients on average had an anatomic level of L4 and were found on manual motor testing to have a functional level of S1.

Figure 1 illustrates that the functional motor level is often better than the anatomic level as demonstrated on prenatal ultrasound imaging. On average, the functional preoperative motor level was found to be 2 levels better than the bony level of defect (median = 2 levels). 

Figure 2 shows that the level as determined by IONM on average was similar to the preoperative motor level (median = 0 levels).

Figure 3 shows that the majority of patients have improved postoperative motor levels when compared to the preoperative anatomic level shown on prenatal ultrasound imaging; on average, patients have 2 levels of improvement on postoperative motor testing than the bony level of defect (median = 2 levels).

Figure 4 depicts that the electrophysiologic level was better than the bony level of defect; on average, this was found to be 2.5 levels better (median = 3 levels). Most patients remained neurologically stable when comparing preoperative and postoperative manual motor testing.

With regard to somatosensory evoked potentials (SSEPs), 46 (90%) of patients had unreliable or undetectable signals in the lower extremities. Figure 5 demonstrates a patient who had electrophysiologic asymmetry. The patient had a functional electrophysiological level of S2 on the left as seen by the abductor hallucis findings (Fig. 5A) but an electrophysiological level of L4 on the right with quadriceps findings (Fig. 5B). There were intermittent motor evoked potentials (MEPs) below the quadriceps muscle that were not consistently reproducible. Somatosensory evoked potentials (SSEPs) were undetectable in both legs (Figs. 5A and 5B).

Figure 5 shows the intraoperative neuromonitoring (IONM) findings for a patient who had asymmetry noted in their electrophysiology. Figure 5A shows that this patient has a functional IONM level to S2 on the left, illustrated by abductor hallucis findings. Figure 5B shows that the patient’s functional IONM level is to L4 on the right, as seen by the findings in the quadriceps. These are both low in amplitude and deemed unreliable. Figure 5B further illustrates that there were intermittent motor evoked potentials (MEPs) below the quadriceps muscle, they are not consistently reproducible and are seen as inconsistent. Figures 5A and 5B both illustrate that the patients somatosensory evoked potentials (SSEPs) are unmonitorable in both legs.

Summary

We present a large series of patients who have undergone fetal MMC closure. Patients with fetal closure have better functional and electrophysiologic motor levels than would be expected from their anatomic levels.

Interpretation

Our findings that patients with fetal surgery have better functional levels and electrophysiologic levels when compared to anatomic levels corroborates the findings from MOMS, MOMS2, and the post-MOMS CHOP data.[2], [3], [16] This larger series confirms a motor-sensory discordance seen in neuromonitoring in fetal patients.[13]

Patients with myelomeningocele closure commonly have tethered cords. The development of symptomatic tethered cord can be concerning as the syndrome can lead to new and potentially irreversible dysfunction. The surgery itself can be difficult, and the indications, technique, and timing have been extensively debated in the literature and at pediatric neurosurgery meetings.[17]–[19] This is particularly the case for patients who have undergone fetal closure of their MMC. Our data indicate that patients can safely undergo tethered cord release after fetal closure without clinically significant changes in electrophysiologic or functional motor levels. We believe that patient should be closely followed with serial clinical exams in multidisciplinary spina bifida clinics. As a patient presents with changes in clinical parameters, we propose that patient should be followed closely for the first signs of physical exam deficits, urologic dysfunction, or radiographic changes. If motor, pain, or urologic decline is noted, the clinician must question whether this neurologic change is a result of tethering. Patients should further be followed with serial imaging; while all MMC patients will show radiographic features of tethering, there are some early warning signs in fetal patients such as the development of enlarging inclusion cysts or enlarging syrinxes. Early recognition and prompt surgical treatment of TCS maximizes clinical and functional outcome in these patients.

The reproducible discordance between the motor and sensory function in this patient group is paramount in the recovery of these patients. IONM found absent or dysfunctional SSEPs in these children. Anecdotally, the senior author has found that these sensory deficits present in a variable fashion. Patients are able to sense gross touch in the lower extremities but appear to have impaired fine touch as well as pain response and altered proprioception. The IONM data suggests that these children have altered somatosensory pathways, which may negatively affect any chances of complete functional recovery. If the patient is unable to incorporate somatosensory information of their extremities in motor action, this raises the question of whether or not clinicians and physical/occupational therapists need to refocus postnatal or postoperative effects on sensory rehabilitation and specific sensory modalities rather than motor alone in order to provide a 360^o approach to recovery in these patients. This data further supports the concept that damage in the spinal cord is progressive over time with damage to the more dorsally located sensory areas occurring first with abnormal spinal cord formation or early traumatic injury.[20]

Tethered cord release in this unique patient population is a technically difficult surgery as surgical planes can be difficult to develop and define. This study cannot judge how the initial closure impacts the repeat surgery, but there are likely effects of how the closure surgery was performed on the safety of the later tethered cord release. IONM is an excellent intraoperative adjunct for explicit identification of spinal cord elements. Compound muscle action potentials from direct bipolar stimulation of spinal nerve roots clearly identifies nerve root level. The electrophysiological level was often better than the preoperative manual motor testing as well as the anatomic level, which indicates that the underlying neural elements are functioning on some level in these patients. This study shows direct evidence that there are intact neural pathways in these patients who have undergone fetal closure. This suggests that there is a chance of meaningful recovery given the intensive therapy in these patients.

Limitations

This study has the inherent limitations seen with retrospective data analysis. Importantly, there is a risk of selection bias given that the patient population is restricted and limited. The reliability of the muscle grades is unknown given that there were more than one physical therapist performing the manual muscle testing. Separately, somatosensory evoked potentials utilize mixed-nerve conduction instead of specific tracts, so there is more difficulty with specific localization.

Future Directions

Direct comparison of tethered cord release IONM data from patients closed with varying closure timing and techniques could provide further information on the ideal surgical technique and the MMC and TCS disease process. Attempts should be made to target directly and reduce inflammation and scarring in MMC patients. Any modifications in closure should be analyzed for several years to show the impact of these modifications on tethering and release surgery. In lieu of these long-term studies, neurosurgeons may want to consider the principles laid out in the discussion above.