(CM1), tethered cord and related syndromes - Springer Link

Neurol Sci (2011) 32 (Suppl 3):S311–S316 DOI 10.1007/s10072-011-0692-3

NEUROPHYSIOLOGY

The neurophysiological balance in Chiari type 1 malformation (CM1), tethered cord and related syndromes Scaioli Vidmer • Curzi Sergio • Saletti Veronica • Tripaldi Flavia • Esposito Silvia • Bulgheroni Sara • Laura Grazia Valentini • Riva Daria • Carlo Lazzaro Solero

Published online: 20 October 2011 Ó Springer-Verlag 2011

Abstract The Chiari malformation (CM) is a syndrome embodied in heterogeneous groups of malformations, spanning from the more benign and known, the CM1, to more complex syndromes such as the rare association with the tethered cord, as spinal lipomas, and the CM2, associated to open spina bifida. The clinical picture may be well expressed and detected at birth or even during intrauterine life, as for CM2, but in the other cases they may run a rather subtle clinical course. The diagnosis of these syndromes is driven by clinical examination and MRI, and it usually requires a multidisciplinary approach in order to plan the therapeutic strategies, such as surgery. Among the diagnostic investigations, the imaging techniques represent the most useful, for their capabilities to detect subclinical lesions, such as syringomyielia and lipoma; the urological investigation is useful to evaluate the urogenital dysfunctions. The neurophysiological investigations represent a non invasive diagnostic procedure to investigate the peripheral nerve, the spinal cord, the brainstem functionalities and more higher brain functions; the nerve conduction studies and the cranial reflexes, the brainstem (BAEP) and the somatosensory (SEPs) evoked potentials (EPs), alone or in combination, can be used for the diagnosis, follow-up and intraoperative monitoring. The most useful diagnostic tools in CM1 are likely represented by the brainstem auditory evoked potentials (BAEPs) and the blink-reflex (BR), while the usefulness of SEPs is still doubtful and debated; in CM2 and tetherd cord the neurophysiological techniques can be combined in

different ways in order to make a functional balance and to answer specific questions. BAEPs and BR can be useful to investigate the brain stem functionality and SEP to evaluate whether the ascending sensory pathway to the cortex can be hampered at some level; the visual EPs are particularly useful to evaluate the integrity of posterior visual pathway and visual cortex in the case of associated hydrocephalus. In the tethered cord, both nerve conduction study and somatosensory evoked potentials (SEPs) are useful to evaluate motor and sensory dysfunction of the lombosacral roots and nerves and spinal cord for their capability to detect subclinical impairment of conduction along the sensory and motor pathway. Finally, last but not the least, the neurophysiological techniques are remarkably useful during surgery; the intraoperative monitoring (IOM) by means of electromyography and direct nerve stimulation and recordings are able to detect early nerve damage, minimize nerve lesions and optimise the surgical techniques. In the operated children with incomplete removal of lipoma and/or persistent tethering, the recordings of SEP and BAEP are useful to demonstrate a conduction deterioration along the ascending sensory pathway due to increasing tethering of the spinal cord due to somatic growth. Keywords Chiari malformation Evoked potential Nerve conduction study Monitoring

Introduction S. Vidmer (&) C. Sergio S. Veronica T. Flavia E. Silvia B. Sara L. G. Valentini R. Daria C. L. Solero Fondazione IRCCS Istituto Nazionale Neurologico C.Besta, Via Celoria 11, 20133 Milan, Italy e-mail: [email protected]

According to the National Registry of Child Malformation (IMER), the defect of neural tube closure resulting in the severe meningomyelocele and related syndromes represent the most common neurological malformation in Italy. They

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account for 27.9% of all the central nervous system malformation, and the 73.2% of them is represented by the closure defect of the spinal cord segment. On the all, in Italy, the spinal cord closure malformation is about 0.5% of the birth yearly registered. These epidemiological data account for the National Health Service efforts for an early detection of the condition, aimed to define the better strategies for the surgical correction, and characterise the diagnostic usefulness of imaging and electophysiological procedures. Early and more recent clinical reports have demonstrated the usefulness of the neurophysiological techniques in Chiari type 1(CM1) malformation and tethered cord [1– 3]. The diagnostic workout and therapeutic strategies of some of these syndromes are still under scientific debate; the usefulness of neurophysiological intraoperative monitoring (IOM) is well established; however, in patients affected by CM2 and re-tethered cord the utility of the neurophysiological techniques is still to be defined. In particular, are still to be characterised the role of neurophysiology in occult condition, as a standalone procedure, or combined with urological evaluation [4–6]. The purpose of this paper is to report on the experience of our Institute in neurophysiologic study in Chiari 1 Malformation (CM1) and tethered cord syndrome, alone or in association with CM1, with particular focus on asymptomatic or mildly symptomatic re-tethered cord, the role of the neurophysiological techniques in the diagnostic workout of late diagnosis of tethered cord and the usefulness of neurophysiological IOM.

Materials and methods Patients A total of 66 patients who have been operated for tethered cord or for a CM1 in our institute and who received a neurophysiological investigation were retrospectively evaluated. The age ranged from 3 months to 60 years; 48 were children and 18 adults. Of the paediatric subgroup, 25 were early infants, 17 school aged and 6 adolescents. The male/female ratio was 3/2. All of the patients had clinical symptoms and signs typical of the spinal cord malformation syndromes at the time of surgery. One or more dermatological signs were present and detected in 58 patients (88%) of the total. Associated malformations have been evaluated and the neurological disability was scored by means of the Hoffman scale. The patients with a normal clinical examination, but definite urological and/or neurophysiological abnormal findings were classified degree 0. The presence and extension of the lipoma was characterised by means of imaging. Six of the patients (9% of the

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total) have been detected some kind of spinal cord associated malformations, such as syringomyelia terminalis and spinal cord splitting. A subset of 37 child patients is still under both clinical and neurophysiological follow-up evaluation because of re-tethering or incomplete de-tethering, and scored neurological deficits. Neurophysiological study The peri-operative neurophysiological study included the nerve conduction study and electromyography of the lower limbs muscle, the lower limbs SEPs, tibial nerve stimulation, and the BAEPs recordings. The IOM monitoring included the EMG recordings by means of monopolar needle electrodes placed into the belly muscle of the lower limbs and of the external sphincter anal muscle; the EMG evaluation included both the spontaneous electrical activity induced by the surgical manoeuvres over the neural structures and the recordings of the muscle action potentials upon monopolar electric stimulation of the operative field in order to check the site and topographycal distribution and side of the nerve roots. The follow-up electrophysiological study in re-tetherd cord and stable patients with CM2, and related syndrome such as syringomyelia and mild tethered cord was carried out by means of the upper and lower limbs SEPs and BAEPs recordings. The program was planned, if the patients were clinically stable, for a yearly clinical, urological and neurophysiological evaluation, while in case of worsening of symptoms, or the detection of sub clinical instrumental changes a further evaluation was performed shortly and eventually the patient was addressed to the surgical team for a further opinion. The patients with CM type1 have been evaluated by means of BAEPs, although in a subset of them SEPs was included in the follow up because of the detection of clinically silent spinal cord cavitation.

Results As far as the patients who underwent surgery are concerned, the duration of the condition was estimated between the time of the confirmed diagnosis and the surgery; the time ranged from 4 months up to 60 years, with a mean time of 7 years; in the adult subset of patient the mean time was 25 years, while in the children subset it was of 5 years. Over the time course between diagnosis and surgery, 75% of the patients complained of clinical worsening of the symptoms, mainly motor defect in the lower limbs, associated with sphincter deficits in a subset of them. At the time of surgery 63% of the patients complained both motor and sphincter deficits. The adult patients complained of a more progressive deterioration


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course when compared with the children, which was due to a delayed diagnosis and prolonged time between diagnosis and surgery. An acute deterioration in the sphincter functionality was observed in 5 patients, 4 adults and 1 child. As far as the 37 children patients under follow-up observational surveillance are concerned, the neurophysiological balance showed a remarkably high incidence of lower limbs SEPs abnormal findings, detected in just over 90% of the patients who were previously submitted to surgery and with incomplete de-tethering. The abnormalities were characterised by prolonged intra-spinal interpeak latencies, deterioration of the cortical SEPs, and evidence of caudal displacement of the lumbar potential (a representative SEPs recording performed in one of our patient is reported in Fig. 1). Associated with lower limbs SEPs abnormal findings were upper limbs SEPs increased latencies and even BAEPs changes in about 20% of the patients, either peripheral or central in origin, suggesting some degree of subtle brainstem dysfunction. The neurophysiological investigation in the fully detethered patients showed a stable or slightly significant improvement of the neurophysiological parameters and in a few patients a normalisation of the central conduction time over a few months after surgery. However, the motor

deficit detected by EMG was persistently stable over the years of follow-up. Of the few pediatric patients with CM1 and under follow-up surveillance, only one showed definite BAEPs and upper limbs SEPs changes; the BAEPs abnormal findings were characterised by unilateral wave I changes, suggesting peripheral hearing loss (Figs. 2, 3) and the upper limbs SEPs showed and increase of the time interval over the spinal N13 component, suggesting slowing conduction along the ascending pathway; the lower limbs SEPs were normal.

Fig. 1 Lower limb, tibial nerve stimulation, SEPs recordings in meningomyelocele. The patient was a female baby of 13 months, affected by a syndromic picture characterised by an external lipoma that was evident at birth; imaging showed a tethered cord and an intraspinal lipoma; a syringomyelic cavitation involving the dorsolumbar tract of the spinal cord was also detected. Before the surgery, the patient underwent neurophysiological examination. The BAEPs revealed signs of brainstem abnormal conduction; the upper limb

SEPs recordings showed well-preserved waveform but with an increased cortical latency and an increase of the central conduction time. The lower limbs SEPs recordings showed normal popliteal potential (bottom trace in the figure), while the lumbar potential was recorded over the L5 (arrow) and with greater amplitude with respect of the L1 lumbar potential (second and third traces from the bottom, respectively). The cortical responses were reduced in amplitude, and remarkably increased in latency (top traces in the figure)

Discussion The results of our extensive neurophysiological study carried out in a series of tethered cord and CM1 patients either as a preoperative evaluation, or during IOM, or as a tool for the evaluation of the operated patients for the characterisation of the neurological deficits and in the follow-up of diagnosed patients without a definite indication to surgery because asymptomatic or clinically stable, showed that the neurophysiological examinations are able to provide useful informations, that need to be weighted with the specific clinical question and goal; only under this

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Fig. 2 BAEPs recordings in CM1 patient. The patient was a 9-yearold girl in follow-up for a CM1 syndrome. She was mildly symptomatic and with normal hearing a year before. The patient underwent to BAEPs, and upper and lower limbs SEPs recordings. SEPs recordings: the responses obtained from the lower limbs stimulation were normal; the responses obtained upon right median nerve stimulation showed a mild increase of the N20 latency, with a mild increase of the central conduction time; the responses obtained

from the left median nerve stimulation were normal. BAEPs recordings: the responses obtained upon right ear stimulation revealed an increased wave I latency (arrow) and reduced amplitude (lower three traces in the figure); the interpeak time I–V was normal; upon left ear stimulation the responses were normal, both in amplitude and latencies (the arrow indicate the wave I); the interpeak time was normal (upper three traces in the figure)

light could be interpreted the results of the electrophysiological changes. According with the follow-up of either operated patients, or non-operated patients waiting for surgery, the data obtained with the neurophysiological investigation can be compared with the clinical scores or with the imaging techniques in order to evaluate the concordance with the clinical course. In the patients not needing an immediate operation, but in prospective of surgical correction of the malformation, whether the neurophysiological changes may be predictive of neurological progression at the extent to indicate the surgery. During surgery, the IOM turned out to be very useful in order to check the neural structure and improve the surgical techniques; in this respect the EMG and the direct nerve stimulation and recordings turned out to be the very best and feasible technique. The results have been so good that the neurophysiological IOM procedures are to be considered an essential component of the surgical plan. Finally, in the operated patients, the neurophysiological investigation was useful in order to evaluate the neurological deficits and the recovery from the defects.

The literature data suggest that the neurophysiological techniques applied to these cases are rather heterogeneous and should be aimed for the different clinical context. The BAEPs and BR are mainly studied for the evaluation of the brainstem structures in CM1 and CM2, the SEPs may be informative for the evaluation of the ascending sensory pathways and the extent of the caudal dislocation of the lumbar tract of the spinal cord both in CM2 and syringomyelia and the tethered cord; the EMG and direct nerve stimulation and recordings are useful during IOM, and, finally, the polysomnography procedure and the oto-neurological testing are studied in a selection of patients affected by sleep disorders of uncertain origin and audiological monitoring of diagnosed patients respectively. The specific role of each of them, alone or in combination, should be evaluated according to single patient’s diagnostic problem and its age. As a matter of fact, in early infancy, literature data suggested that BAEPs display greater diagnostic sensitivity compared with SEPs but, on the other hand, BAEPs don’t provide useful information about the progression of the symptoms, while SEPs do. However, a more recent paper

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Fig. 3 Multimodal evoked potentials recordings in CM type 1 patient. The patient was a 3.5-year-old female with the clinical and the radiologically confirmed features of CM1. However, in the patient were also detected a mid thoracic syrinx and a caudal displacement of the lumbar medulla at L4. The BAEPs recordings (left panel in the figure) showed and increased latency of wave I (arrow; W I) with normal I–V interpeak latency; the wave V was mildly desynchronised. The upper limb median nerve SEPs (mid panel in the figure) were normal. The lower limb, tibial nerve SEPs (right panel in the figure) showed that the amplitude of the lumbar potential N22 was larger over the L5 electrode, of normal latency (lower arrow); the

intraspinal conduction time between the N22 and the cervical P30 (mid arrow) was normal; the cortical P37 component (upper arrow) was slightly increase in latency (36 ms), with a mild increase of the total conduction times N22-P37 (23 ms) and P30-P37. The BAEPs features were those of the CM1 syndrome, and the lower limbs SEPs confirmed the features of the tethered cord. It is worth remarking that the increase of the conduction time occurred in the more cranial segment of the ascending volley. Furthermore, months later, the MRI showed an enlargement of the cavitation; in spite of that, the SEP remain stable, suggesting that the usefulness of the SEPs in these condition is still to be define

on a large series of patients indicates that BAEPs alone is even a useful predictive tool for the timing of surgery. A subsequent paper, in which BAEPs and BR are compared, confirms both the diagnostic sensitivity of both the methods, even though BR show a high degree of concordance with the clinical symptoms or the development of new ones [3, 7–9]. In the late infancy children, BAEPs turned out to be very sensitive as a diagnostic tool in both CM1 and CM2, and with a high degree of correlation with the clinical signs and symptoms. It has also been demonstrated that BAEPs can be associated, and eventually replaced by, with a clinical scores of the audiological symptoms, by means of a self administered test by the patient itself. In CM2, with no other associated malformations, both BAEPs and SEPs have been demonstrated to be sensitive and reliable, but their role in CM1 has not yet been defined [10–14]. The role of the polysomnography is promising, but need further confirmation [15, 16]. On the whole, the literature showed that BAEPs and BR are very useful in CM2. The diagnostic usefullness of BAEPs and SEPs and motor conduction evaluation, as recently reported, during surgery is promising and robustly investigated [17–19].

spectrum of clinical pictures and severity. The natural history is still a debated matter at least for a subset of them, and the results of the surgery revealed some controversial issues among the various teams. On the all, the results of surgery looks like promising and encouraging, promoting a debate addressed to better define more shared strategies and criteria for the patients eligible for surgery. One of the more controversial issues is represented by the short- and long-term neurological complications of surgery and the strategy that prevents or minimizes them. Of the patients operated in our Institute and with more complex malformation, the 70% showed a low incidence of postoperative neurological deterioration at follow-up, and compared with data reported by other teams. Early diagnosis and well planned surgery seemed to be important to minimize postoperative deficit, compared with the waiting longer, until more definite clinical symptoms. Similarly, the IOM by means of elctrophysiological techniques had greatly improved the clinical outcome and made the surgeon more confident with the complexity of the intervention. Without any doubts, the clinical outcomes were far better in the patients with a few symptoms or without symptoms at all and these results were maintained at long-term follow-up. In this respect, the preoperative neurophysiological balance, and more rigorous follow-up strategies in partially de-tethered patients, performed by a multidisciplinary team, are mandatory for a successful outcome in term of the patient’s acceptable quality of life. A key role is also played by the

Conclusion The CM1 and CM2 and the meningomyelocele syndromes represent a wide range of conditions, with a broad

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associations of the parents and patients actively cooperating with the medical teams. Conflict of interest The author’s declare that there is no actual or potential conflict of interest in relation to this article.

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