Long-term evaluation of intraoperative neurophysiological monitoring-assisted tethered cord surgery

Spinal dysraphism refers to a large variety of congenital malformations, including lipomyelomeningocele, split cord malformation, myelomeningocele, tight filum terminale, and dermoid sinus [14]. As soon as a patient with a tethered cord morphology becomes symptomatic one speaks of a tethered cord syndrome [21, 42]. The symptoms associated with tethered cord syndrome may affect four different fields: (1) neurological, (2) urological, (3) pain, and (4) orthopedic. Neurological symptoms appear as sensory and/or motor loss of the caudal nerve roots involved. Urological disturbances affect bladder function. This may start subtle, and urodynamic investigation is used for diagnosis. Orthopedical symptoms may express as structural deformations like a clubfoot or progressive scoliosis. Pain can be atypical without the classical features of radicular or neurogenic pain. The presence of these symptoms determines the indication for surgical detethering, although prophylactic surgery is recommended in asymptomatic young children with lipomyelomeningocele [4, 12, 36, 38]. The assessment of symptoms pre- and postoperatively helps to define the outcome of the surgery, but the evaluation of the quality of the surgical detethering appears to be more complicated [13]. The distinction between symptoms due to tethering versus myelodysplasia cannot always be made, and the reversibility of symptomatic tethering is also related to the timing of surgical release. These aspects complicate the evaluation of the use of intraoperative neurophysiological monitoring (IONM) in tethered cord surgery. IONM has been widely used as a tool to improve surgical results concerning safety (prevention of neurological morbidity) and efficacy (lasting effect of detethering) [17, 18, 21, 28, 32, 39].

In IONM, we can distinguish between mapping and monitoring. Mapping refers to identification of functional nerve roots by means of direct nerve root stimulation [35]. In the same manner, non-functional tethering structures can be identified and safely cut. Monitoring provides continuous information about the preservation of the motor and/or sensory pathways, and in this way, it may serve as a reassurance for the neurosurgeon during the process of surgical detethering [35]. Besides mapping, motor evoked potentials, sensory evoked potentials, or bulbocavernosus reflexes are being used for monitoring in tethered cord surgery, although the clinical relevance is unknown yet [35].

In our previous report on a series of 65 patients with tethered cord based on spinal dysraphism, that had been surgically detethered with the use of IONM, we concluded that the use of IONM, both mapping and monitoring, appeared to be feasible in all patients irrespective of age, and that its use might have contributed to the prevention of preoperative neurological and urological morbidity in the high-risk group [13]. This high-risk group consisted of patients with lipomyelomeningoceles [29] or with split cord malformations type I [26], while the higher risk profile referred to the increased risk of surgical morbidity in these patients. The surgical strategy in lipomyelomeningoceles at that time was to perform a maximal resection of the lipoma in addition to creating a maximal safe detethering. Lipomas were not resected radically, and a small remnant was considered acceptable. The mean follow-up (FU) in this series was 4.2 years, and the secondary progression of symptoms was described.

An additional indication of effective surgical detethering might be concluded from the long-term evaluation of these patients. The duration of stabilization of symptoms versus recurrence of identical symptoms or appearance of new symptoms might be related to the surgical detethering. This study presents the long-term FU results of the same cohort of patients that have been reported on before [13].

Tethered spinal cord surgery with the use of IONM seems to be long-term effective on the neurological, urological, and pain domains. However, in our study, a high rate of progressive scoliosis was found in the long-term in a group defined by females who underwent surgery at an age at or younger than 12 years.

In Fig. 2, the overall outcome for this group shows a stable long-term outcome in the urological, neurological, and pain domains. However, slight changes in the number of symptomatic patients and the severity of the symptoms, as shown in Table 3 in the appendix, do occur.

A slight decrease in the number of patients with deficits in the neurological and urological domains was observed over time but might be related to better coping of the patients. Pain symptoms decreased primarily postoperatively and remained stable during FU. This indicates that detethering has an immediate and long-term effect on pain. A prospective study would be required to validate these indications.

Scoliosis appeared to be progressive in 11 patients consisting of young females that underwent tethered cord surgery aged 12 years or younger. The question remains whether the progressive scoliosis is due to the tethered cord or caused by other reasons. Several studies, in which patients underwent IONM-assisted tethered cord surgery, do not mention progressive scoliosis as a long-term outcome measure [20, 27, 30, 31, 37, 41]. Few studies present the correlation between tethered cord and the presence of scoliosis [3, 11, 15, 22, 33].

According to Cardoso et al., patients with spinal dysraphism associated with tethering had predisposing factors causing scoliosis [3]. These predisposing factors consisted of unequal growth caused by congenital abnormalities of the spine, instability of the spine caused by missing posterior spinal elements, and paralysis in different severities.

Two earlier studies showed a correlation between scoliosis and tethered spinal cord. McLone et al. focused only on myelomeningoceles. They showed that of patients with curves <50°, 33% had improved and 63% had remained stable 1 year after detethering. At maximum FU of 5 years after detethering, 21% were still improved and 42% were still stable [22]. Reigel et al. followed 262 patients over 20 years to see the effects on progression of scoliosis after tethered cord surgery [22, 33]. They showed that after tethered cord surgery, the progression of scoliosis decreased or reached a plateau when lumbar or sacral surgery had been performed [33]. Besides myelomeningoceles, scoliosis is associated with split cord malformation as well. According to Hilal et al., 40% of patients with split cord malformation will develop scoliosis, especially older children [11].

Tao Yang et al. investigated the clinical presentation of intramedullary neurenteric cysts [43]. They found scoliosis in three patients (23.1%), comparable with our finding of three patients (27.3%) with intramedullary cysts. In three of 11 patients, syringomyelia was present. According to several studies, syringomyelia can be associated with scoliosis [3, 5, 9, 10, 16, 24, 25]. The incidence of scoliosis associated with syringomyelia ranges from 25 to 85% [5, 10, 16].

Jankowski et al. showed that scoliosis is associated with tethered spinal cord and syringomyelia [15]. His patient groups underwent neurosurgery at a young age comparable with our patient group. Jankowski et al. advised that patients with a Cobb angle, <30° should undergo a neurosurgical intervention followed by a period of monitoring for progressive scoliosis. Our findings might suggest that tethered cord surgery may not prevent progression of scoliosis in patients, defined as females that underwent tethered cord surgery before or including the age of 12 years. Like Jankowski et al., we advise close monitoring during FU in order to minimalize the extent of scoliosis progression in these patients.

Both the diagnosis of tethered cord syndrome, in particular split cord malformation, lipomyelomeningocele, and myelomeningocele, and the additional pathology consisting of intramedullary neurenteric cysts and syringomelia indicate a higher chance of obtaining progressive scoliosis. However, this does not explain the high percentage (90.9%) of young females with progressive scoliosis in our sample. When looking at adolescent idiopathic scoliosis, females and males are affected equally. However, progressive scoliosis occurs 10 times more often in females than in males [23]. This might partly explain our high rate of progressive scoliosis in females.

However, when observing the total population in our research with the age of 12 years old or younger, we found that 13 out of 19 (68.4%) females had scoliosis at FU2, and 1 out of 12 (8.3%) males had scoliosis at FU2. Females and males in our sample are therefore not equally affected. It seems there is a predisposition to (progressive) scoliosis in females diagnosed with tethered cord syndrome when taking both diagnosis and comorbidity into account.

Our subgroup analysis of patients with a lipomyelomeningocele showed no deterioration postoperatively.

This may underscore the value of using IONM during high-risk detethering procedures. Concerning the lasting effect of detethering on symptoms as a possible indication of efficacy, our patients with partially resected lipomyelomeningoceles had a PFS of 64.3% after 12.4 years. Other studies with patients with partially resected lipomyelomeningoceles showed a PFS of 52.0% after 10 years [6] and 40.0% after 10 years [29], of which only in the latter study IONM was used. Another study by Pang et al. compared a group of patients with partially resected lipomyelomeningocele and a group with total to near-total resected lipomyelomeningocele [27]. The partially resected group had a PFS of 34.6% after 10.5 years, and the total to near-total group had a 82.8% PFS after 16 years. When only looking at the asymptomatic patients, our series had a PFS of 50% after 11.6 years, while Pang’s series showed a 43.3% PFS in the partially resected group and a 98.4% PFS in the total to near-total resected group. In the total to near-total-resection group, all patients were operated with extensive standard use of IONM. Our series showed a higher PFS when comparing with the other partially resected groups. This might be related to the standard use of IONM in our study. However, Pang’s scorings in the total to near-total resected group, especially asymptomatic patients, would suggest to perform a total to near-total resection in these patients. In a study of Kulkarni et al., a group of asymptomatic patients with lipomyelomeningocele were followed without surgery and showed a PFS of 67% after 9 years [19]. This is even a better result than in our partially resected patients and might be explained by a selection bias due to the small size of our series of asymptomatic lipomyelomeningocele patients.

Although there are different opinions on deciding whether to surgically treat tight filum terminale or not, our series showed an effective surgical outcome with a PFS of 80.0% after 10.5 years with improvements in 40.0% when comparing postoperative with FU2 results.

Drake et al. question whether surgical treatment is doing more good than harm [7, 8]. We propose that when proper criteria are used, consisting of a tethered cord syndrome and the presence of thickened filum in combination with a low-lying conus, improvement can be expected as illustrated in this study.

The quality of life in TC children scored higher than in the healthy Dutch population on every domain except the physical functioning scale. Since the SF-36 is only validated from the age of 16 years old, no strong conclusions can be taken from the results of the TC children group. However, their high score on every scale is still an interesting result. This might be due to the fact that their questionnaire was mostly filled in by their parents. Children themselves also may not completely understand the meaning of their impairments and therefore do not apply their impairments on their quality of life.

The myelomeningocele population scored higher than our series and was even comparable with the scores obtained by the healthy Dutch population. Since symptoms due to myelomeningocele are present from birth, these patients, comparing with tethered spinal cord patients, never knew how it was without their symptoms and therefore might cope better with their symptoms resulting in a higher quality of life.

When comparing with another quality of life study in patients with spina bifida occulta, similar results with our population were observed [40].

Tethered cord surgery has been widely practiced in patients with various forms of spinal dysraphism. The usefulness of IONM during these surgical procedures remains a topic of debate, since its value is difficult to evaluate in an objective manner. A randomized controlled trial will not be feasible to conduct. Most series report on personal experiences and preferences with regard to its use [35]. The prospective cohort study by Pang illustrates the importance of the use of IONM when striving for radical resection of lipomyelomeningoceles. The validation of the use of IONM in tethered cord surgery will grow when it is applied in a standardized fashion and more series will be described. These reports will be valuable in order to define criteria for the use of IONM in tethered cord surgery.