The value of intraoperative neurophysiological monitoring for microsurgical removal of conus medullaris lipomas: a 12-year retrospective cohort study

Spinal lipomas are benign tumors of the spinal canal. They consist of up to 90% fat cells but can also contain fibrous, muscular, neural, and other embryogenic tissue. Lipomas are differentiated clinically, pathohistologically, and ontogenically into several types: purely epidural lipomas, purely intradural lipomas, lipomas of the Conus medullaris, lipomas of the Filum terminale, and spinal angiolipomas [1]. Lipomas are one of the main reasons for tethering of the spinal cord (Figure 1), which can lead to progredient neurological deficits, such as pareses, sensory deficits, and bladder or colon dysfunction [1]-[4].

Lipomas of the Conus medullaris are the most common form. They occur with an incidence of 1 in 4000 births in Western countries, and they have a 2:3 male:female ratio [1],[5]. They are categorized into three subgroups, depending upon where they adhere to the Conus: a) dorsal, b) caudal, and c) transitional (Figure 2) [1],[2],[4],[5]. Lipomas of the Conus medullaris are diagnosed as early as a mean age of 6 months, because a soft, subcutaneous mass of fat is palpable in the lumbar vertebral area already by this age in 90% of the children [1]. Further symptoms caused by the lipoma of the Conus medullaris include skin changes (such as hypertrichosis), capillary hemangiomas, and neuroorthopedic deformities of the extremities and feet due to asymmetrical innervation [1],[3],[5],[6]. The neurological symptoms are mostly sensory and motor deficits of the lower extremities, limited or lost bladder and colon control, and back pain (arising mostly later with age) [1]-[3].

Neurosurgical intervention removes the tumor and untethers the nerve roots, in order to improve neurological deficits and prevent further progression of the pathology. There is an surgical morbidity of up to 24%, because the tumor adheres strongly to the spinal cord and the exiting nerve roots and/or because the tumor tissue invades into the dura [7],[8]. Various neurophysiological examination techniques are used to reduce the risk of iatrogenic neurological deficits in spinal-cord surgery [9]. These techniques serve to detect nerve tissue in the operating site and to monitor its function until the end of the operation. Motor evoked potentials (MEPs) have been used to monitor descending pathways. After transcranial electric or magnetic stimulation, muscle response potentials can be recorded electromyographically from defined muscles of the extremities [3],[10]-[13]. Somatosensory evoked potentials (SEPs) are suitable for monitoring ascending pathways. Surface stimulation is delivered over the N. tibialis, and potentials are recorded cranially via scalp electrodes [10]-[14]. Free-running and triggered electromyography (EMG) are two methods for directly testing nerve fibers in the operation site [15]-[17]. The continuous monitoring of the free-running EMG will show any mechanical manipulations of the nerve roots (e.g. during tumor removal). The direct electrical stimulation of triggered EMG can be used to test the transmission capacity of nerve roots.

So far there are no evidence-based recommendations on the choice of the best and most reliable monitoring procedure or combination of procedures. The aim of this study was to evaluate the various monitoring procedures for their effectiveness and prognostic value when used during neurosurgical treatment of spinal lipomas. This report provides an evaluation of each of the procedures and estimation on the best combination.

Spinal lipomas are the cause of tethering of the dura and the exiting nerve roots. Already in early childhood they can lead to several severe functional compromises such as pareses, sensory deficits, or urogenital dysfunctions [1],[3],[6]. Lipomas of the Conus medullaris are the most common form of spinal lipoma, and they have been often discussed in the literature [1],[3]–[5]. There is broad consensus about the choice of treatment for symptomatic Conus lipomas: operative removal of the tumor (to decompress the dural sac and the exiting nerve roots) and untethering [1],[3],[4]. Such an intervention should prevent progression of the neurological symptoms or even improve already existing symptoms [5],[6]. Pareses and bladder function disorders in particular show a positive course after resolution of the Conus base. There is lack of consensus to date about the treatment of asymptomatic lipomas of the Conus medullaris. The value of "prophylactic" operations has been viewed by some authors as completely outweighed by the operating risk taken on [8]. But since the introduction of intraoperative neurophysiological mapping and monitoring techniques into routine surgical procedures, there seems to be a moderately more positive opinion about early operative therapy, because such neurophysiological monitoring will hopefully be able to reduce the postoperative morbidity.

MEP is a way to intraoperatively test the function of the motor pathways. MEPs are described as generally reliable and safe to use for spinal indications [10],[12]–[14]. This is confirmed by the technical success rate of 86.7% in the present study. A disadvantage of this monitoring technique though is that an influence on the potential can arise not only on the path between the operating area and the discharge musculature but also on the entire path between cranial potential evocation and the periphery. So beside various physiological influences, anesthesiological factors affecting the central nervous system have a major influence on the registered potentials. Finally, reversible and irreversible changes of the recorded potentials must be differentiated. Reversible changes in all cases accompany unchanged clinical symptomology or a rapid recovery of short-term functional compromise. These observations are comparable with those for cerebral operations in the central region [18],[19]. Irreversible changes correlated with postoperative neurological deterioration in 7.7%. So these potential changes have a prognostic value, especially since these predicted deteriorations did not improve within the first 3 months after surgery. Immediate clinical deteriorations in cases of reversibly changed MEPs showed a stable status or even improvements in the long-term clinical course. Thus these short-term clinical deteriorations can be best viewed as postoperative swelling phenomena. MEPs that did not change at any time during the operation predict with higher probability an unchanged or improving clinical outcome.

Although our study did show an acceptable success-quota / responder-rate for the tibialis SEPs of 66.7%, the sensitivity for mechanical maneuvers in the operating site was quite low, as already presented by Gunnarsson et al. [20]. Thus, anesthesiological influences have at least as much influence on the tibial SEPs as manipulations by the surgeon. This is partly explained also by the anatomical location of the sensory pathways. Manipulatory changes can therefore be expected at highest on the level of the rear part of the spinal cord – thus only for dorsal lipomas. For anatomical reasons, caudal and transitional Conus lipomas would be difficult to examine by means of tibial SEPs. Tibialis SEPs are also of limited value in the area of the exiting nerve roots. Here, only dermatome-specific SEPs would be available as an examination technique [10],[11],[13],[14], which requires a time investment that is unjustified in our view (both in regards to the number of stimulation sites and also due to the necessary time required for potential averaging). So consistent with most other studies on this topic [10],[11],[13],[14], dermatome-specific SEPs were not used in our study either.

It was technically feasible to carry out EMG in all cases, and there were no anesthesiological or physiological influences to be detected (having in mind, that no muscle relaxants were allowed in the course of surgery). Similar to the study of Valentini et al. [21], it was possible to better identify the neural structures of complex lesions, reducing the risk of surgical damage and incomplete detethering. In a study by Bindal & Ghosh [17], electrophysiological feedback on the patient could be obtained in 76.2% of the cases through intraoperative EMG monitoring procedures for neurosurgical interventions. Our success rate of the initial nerve root identification of 60.2% was below the value reported by Bindal & Ghosh [17], but the rate had reached 76.4% by the end of the operation, which is consistent with the literature.

The specific potential changes in the free-running EMG after mechanical maneuvers were especially helpful for the surgeon. So, main results of this work are that: a) spontaneous activity can be recorded from the examined muscle groups also without manipulation, and it has no pathological value, b) phasic "spikes"/"bursts" are evoked by direct contact of nerve tissue with operating instruments, and c) tonic "trains" can be elicited by stronger traction on the nerve fibers or partial damage. Since spikes/bursts were registered in all 30 cases, these appear to have no immediate pathological value. Yet if these turn into trains from stronger traction, then this can prognostically indicate a mechanical lesion as seen in other studies before [22]. Also, EMG trains appear to be more sensitive than MEPs, for the motor deteriorations that were reversible immediately or within 3 months post-op, as they were all prefigured by train activity. There were even 4 cases where train activity left no immediate clinical harm, thus confirming that trains might have worked as a very sensitive warning signal in these cases – forcing the surgeon to immediately change the surgical strategy. This includes immediate reduction of compression, traction or stretching neural structures to reduce neuropraxia as well as stopping thermal/bipolar dissection and mechanical ligation to reduce ischemic damage. Furthermore, the temperature of the irrigation saline has to be checked routinely. A detailed analysis of train duration, frequency of train recurrence, or train amplitudes in a larger patient sample might provide better information.

Nerve tissue could be distinguished from non-nerval tissue (tumor tissue, connective tissue etc.) by triggered EMG/direct bipolar stimulation in 60.2% of cases right after opening of the dura. Preexisting pareses equal or less than BMRC grade 2/5 were one reason for lack of stimulation success. Tumor masses at the beginning of the operation were another reason, as they might have covered or suppressed the exiting nerve roots. The stimulation gains are due to the tumor removal and preparing free the tumor-covered nerve roots. However, anatomical liberation of tumor-covered nerve roots does not seem to correlate with improved post-op function. This may be due to the fact, that dislocated nerve roots still may work properly or non-working nerve roots will not regain function after free-preparation. Stimulation losses on the other hand appear to have the potential to forewarn of postoperative clinical deteriorations. Our findings are consistent with a previous study that found that the simultaneous use of EMG and MEP monitoring procedures is a reliable method for the differentiation of neural vs. fibrous or tumorous tissue [16].

There are many methodological difficulties in evaluating the optimal intraoperative monitoring procedures for surgery of spinal lipomas in the Conus medullaris. Looking exclusively at statistical parameters (such as sensitivity, specificity, or predictive value), the previously described discrepancies (e.g. about the value of SEPs) can be found in the literature. This is partly due to the fact that many studies do not differentiate between surgeries on the spinal cord, Conus, or Cauda, but instead evaluate them all together as "spinal operations". Studies that occupy themselves electrophysiologically only with Conus tumors are, like the present study, mostly rather small, so that valid statistical analysis is only possible with qualifications. Furthermore, the evaluation and analysis of the neurophysiological signals generated depends heavily on the experience of the investigators with the various techniques yet also on their preferences for one or another of them. Also, the prognostic and predictive explanatory power of observed signal changes can only be determined with qualifications, because changes in potential (which in part are arbitrarily defined differently by different research groups) are taken as warning signals and therefore have an immediate effect on the operative process. So the actual specifity of "train" activity in the free-running EMG (for example) remains unclear, because their intraoperative occurrence may lead directly to a consequence in the surgical strategy. Yet there is no way around this, because a scientifically motivated "wait-and-see" approach would be ethically indefensible. But now, with all these methodological caveats aside, what would be the most reliable (yet time and cost efficient) examination set-up, for intraoperative monitoring in the Conus medullaris?

According to the results of this study, the authors favor a routine set-up of intraoperative neurophysiological monitoring for spinal lipomas in the area of the Conus medullaris consisting of transcranial evoked MEP, free-running EMG, and triggered EMG. This enables a site cartography at the beginning of the operation, continuous intraoperative functional testing (nerve vs. non-nerve tissue), and a prognostic evaluation about the expectable post-operative symptomology.