Letter to the Editor: Evoked potentials and Chiari malformation Type 1

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TO THE EDITOR: We read with interest the study by Moncho et al.9 (Moncho D, Poca MA, Minoves T, et al: Are evoked potentials clinically useful in the study of patients with Chiari malformation Type 1? J Neurosurg [epub ahead of print April 15, 2016. DOI: 10.3171/2015.11. JNS151764]). In their retrospective analysis of prospectively collected data, the authors suggest that evoked potential aberrations in preoperative workup of patients with Chiari malformation Type 1 (CM-1) do not contribute to establishment of treatment algorithms, yet somatosensory evoked potential (SSEP) and brainstem auditory evoked potential (BAEP) changes may help to establish evidence of subclinical dysfunctions.

In the accompanying editorial,1 Dr. Adelson describes the complexity of decision making in these cases and the inability of electrophysiological testing to indicate either dysfunction or disease progression, which also emphasizes the unestablished indications for preoperative nerve monitoring evaluation.

The role of intraoperative evoked potential monitoring in CM-1, traditionally using SSEP and BAER modalities (auditory brainstem response), remains, in our opinion, unclear. In our recent study2 we addressed this issue in addition to questioning the potential benefit of adding transcranial motor evoked potential (TcMEP) monitoring to the equation in an attempt to improve sensitivity and specificity to detect postoperative deficits. We presented data that demonstrate that the use of multimodality intraoperative neurophysiological monitoring (INM), including TcMEP, could be beneficial in detecting and avoiding iatrogenic injury stemming from inappropriate patient positioning and could possibly contribute to the decision-making process of deciding when adequate decompression has been achieved on an individual-patient basis.

As was the case for image-guided neuronavigation that began as a useful tool in neurosurgical procedures and today is widespread and often considered standard of care, INM is rapidly becoming a “must” in various surgeries, including treatment of brainstem and spinal cord tumors,6,7,10 tethered cord syndrome,4 scoliosis and other spinal deformities,3,8 syringomyelia,13 and degenerative cervical spine disorders,5 as well as supratentorial surgery.11,12

In the modern era of neurosurgery, and when taking into account factors of “defensive medicine,” prioritization in the use of INM as a surgical adjunct must be addressed. In this light, we see Moncho and colleagues' study as an opportunity to call attention to this dilemma and urge further large-scale studies regarding the role of electrophysiological testing in CM-1 both preoperatively and intraoperatively.

References

Disclosures

The authors report no conflict of interest.

Response

We would like to thank Dr. Barzilai and colleagues for their letter regarding our recent paper on the BAEP and SSEP alterations found in patients with CM-1. We are familiar with Dr. Barzilai's studies in the field of INM in treating pediatric CM-1,4 and therefore his interest and comments on our work are greatly appreciated. At the same time, his letter gives us the opportunity to broaden the discussion and address the still-controversial topic of the usefulness and clinical relevance of intraoperative evoked potential monitoring in patients with CM-1.

The application of INM has expanded rapidly over the past 2 decades, as seen in the large number of studies published in different disciplines, including neurosurgery, neurophysiology, orthopedic and vascular surgery, otolaryngology, and neurology. The main objective of INM is to protect the vulnerable neural structures by allowing early detection of reversible neurophysiological dysfunction during surgery, thus preventing permanent neurological damage. INM is a very interesting field, not only from a clinical point of view, but also because it is an attractive instrument for research.10 At present, however, there is still much to learn and do in order to demonstrate the real benefit of these techniques in some pathologies. Given the current low volume of evidence, we do not agree with Dr. Barzilai and colleagues' opinion that INM may be used as an instrument of “defensive” medicine. As far as we know, no studies have shown the sensitivity, specificity, and predictive values (either positive or negative) of INM in CM-1 patients. This is a requirement for any diagnostic tool to be routinely used in the operating room. In addition, INM increases anesthesia, surgical time, and monetary costs and, when applied to CM-1 surgery, can lead to erroneous, or at least questionable, decisions.

Some authors have proposed INM during surgery in patients with CM-1, mainly in the following 3 scenarios: 1) during placement of the patient before surgery, 2) to de termine when adequate decompression has been achieved and therefore to design surgery on an individualized basis, and 3) to detect intraoperative evoked potential worsening.

For surgical positioning in patients with CM-1, the rationale for intraoperative evoked potential monitoring is that it can diminish the risk of neurological injury at a time when it can be reversed. Anderson et al. reported the case of a 14-year-old patient with CM-1 and a holocord syrinx who underwent suboccipital decompressive craniectomy and in whom surgical positioning had to be modified after a dramatic deterioration of baseline SSEPs.2 After the patient's neck was repositioned, the left median nerve potential improved but did not return to baseline. Postoperatively, the patient had decreased proprioception of the left arm that persisted for 2 weeks.2 In that case report, the first figure shows that the patient had severe CM, with the obex below the foramen magnum, significant tonsillar descent, and possible basilar impression with anterior compression. Using the new classification, this patient would have been included in the category of CM Type 1.5 (CM-1.5), or even been diagnosed as having a complex craniocervical junction malformation. Other studies have reported that the patients with impaired evoked potentials during surgical positioning were those with complex craniovertebral junction abnormalities.9

At our center, surgery is always performed with the patient in the prone position, with cranial flexion and discrete cervical distraction, and the head fixed in the May-field headholder. In all patients, a tolerance test is always performed before surgery: the patient is asked to maintain cervical hyperflexion—similar to that used during surgery—for at least 2.5 hours while they carry out a routine activity, such as reading. The few patients reporting neurological symptoms during this test are placed with their neck in a neutral position. After treating more than 300 patients with CM-1, we have not detected any neurological complications related to head positioning. However, we agree with Dr. Barzilai and colleagues that evoked potential monitoring during head positioning may be useful in some CM patients, especially those with more severe malformations who are at risk for neck flexion.

The most controversial aspect of this topic is, in our opinion, the use of INM to limit the degree of posterior fossa decompression (PFD) and guide the decision of whether or not to open the dura mater. Some authors have argued that an extradural approach—that is, suboccipital craniectomy with a C-1 laminectomy and resection of the fibrous band at the level of foramen magnum, with eventual serial incisions of the outer layer of the dura without opening it—is enough to relieve the pressure gradient at the craniocervical junction and improve clinical symptoms.5 Intraoperative ultrasonography and/or BAEP monitoring have been used by several authors to decide whether to open the dura in CM patients, especially children. Zamel et al. reported that PFD involving bone removal alone significantly improved conduction time in BAEPs in most pediatric patients with CM-112 and that the use of duraplasty allowed for a greater improvement in conduction time in only 20% of patients when compared to surgery involving bone decompression alone.12 Anderson et al. reported improved BAEP conduction times in most patients who had undergone PFD with duraplasty, but the authors stated that the majority of improvements were also observed after bony decompression.3 These results suggest that opening the dura mater is not necessary in the treatment of CM, especially in patients without syringomyelia. However, in the Zamel series, postoperative brain MRI studies were only available for 55 of the 80 patients treated and showed normalization of the position of the cerebellar tonsils in only 54.5% of patients in whom a pure extradural approach was taken; this rate increased to 84% in patients who underwent duraplasty.12 Similar negative findings were observed in the position of the cerebellar tonsils on the postoperative MRI studies of most of the 30 pediatric patients with CM-1 treated by Caldarelli and colleagues using a purely extradural procedure.5 Taking into account these results, we cannot consider that optimal treatment was applied based on evoked potential findings.

It is well known that opening the dura mater and carrying out a dural graft increase the risk of CSF leakage, pseudomeningocele, and aseptic meningitis. However, restoring “normal” CSF circulation through the foramen magnum is essential in the surgical treatment of CM. It is well established that PFD and duraplasty achieve the best results in the treatment of CM, regardless of whether it is associated with syringomyelia or not,1,7,11 in both adults and children. This has also been the case in most CM-1 patients admitted to our department for a second-look surgery after an extradural procedure (see example in Fig. 1). It is also important to note the potent osteogenic effect of the dura mater in the process of calvarial regeneration,6 which can explain the partial posterior fossa reossification observed in some pediatric patients with CM-1 treated without duraplasty (Fig. 2). In terms of security, we want to emphasize that when surgery involves wide suboccipital craniectomy, resection of the posterior arch at C-1 and opening the dura with preservation of the arachnoid membrane (a surgical technique we named “posterior fossa reconstruction” in 1994)8 produces excellent morphological results, with cranial ascent of the hindbrain, good clinical outcomes, and minimal complications. This technique has been used in most patients who undergo this type of surgery at our institution for the last 20 years.

FIG. 1.
FIG. 1.

Presurgical MR image (A) and sagittal CT scan (B) in an 11-year-old boy with CM-1.5 and a moderate basilar impression, in whom a PFD was performed at another institution without opening the dura mater (B). The postoperative control images 4 years after surgery (C and D) did not show any change in the cerebellar tonsil position or in the size and extension of the syringomyelia. The patient underwent a second surgery at the age of 16 years, involving an increased occipital bone resection, opening of the dura mater, and a wide duraplasty. The postoperative MR images (E and F) showed cerebellar remodeling with a large pseudocisterna magna, a significant tonsillar repositioning, and a small residual syrinx.

FIG. 2.
FIG. 2.

A 6-year-old girl with a treated syndromic craniosynostosis who, when she was 6 months old, underwent PFD without opening the dura mater. Follow-up MR image (A) obtained when she was referred to our institution at the age of 4. At the age of 6, a follow-up CT scan showed a partial reossification of the occipital bone (B and C). Figure is available in color online only.

With regard to the use of evoked potentials for monitoring neurological worsening during surgery, Zamel and coworkers' study reported that none of the 80 children with CM-1 in whom BAEPs were monitored showed any significant worsening during surgery that would have prompted the surgical team to modify their surgical strategy.12 Similarly, of the 22 patients of the Barzilai et al. study, none had evoked potential alterations during surgery, although 3 patients displayed significant SSEP attenuation concomitant with patient positioning.4 These findings confirm that the incidence of neurological complications once the patient is positioned is very low9 and therefore raise doubt about the cost-effectiveness of this procedure.

We completely agree with Dr. Barzilai and colleagues' opinion that there is a need to establish an optimal, cost-effective monitoring protocol for posterior fossa surgery in patients with CM-1.4 However, the evidence to date shows that the only potential benefit of evoked potential monitoring in CM-1 is during patient positioning and only in a small number of patients who could most likely be identified before surgery, making the routine use of INM difficult to justify.

References

  • 1

    Alamar MTeixidor PColet SMuñoz JCladellas JMHostalot C: [Comparison [corrected] of Chiari I malformation treatment using suboccipital craniectomy and posterior arch of C1 resection with or without dural graft.]. Neurocirugia (Astur) 19:2332412008. (Span)

  • 2

    Anderson RCEmerson RGDowling KCFeldstein NA: Attenuation of somatosensory evoked potentials during positioning in a patient undergoing suboccipital craniectomy for Chiari I malformation with syringomyelia. J Child Neurol 16:9369392001

  • 3

    Anderson RCEmerson RGDowling KCFeldstein NA: Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 98:4594642003

  • 4

    Barzilai ORoth JKorn AConstantini S: The value of multimodality intraoperative neurophysiological monitoring in treating pediatric Chiari malformation type I. Acta Neurochir (Wien) 158:3353402016

  • 5

    Caldarelli MNovegno FVassimi LRomani RTamburrini GDi Rocco C: The role of limited posterior fossa craniectomy in the surgical treatment of Chiari malformation Type I: experience with a pediatric series. J Neurosurg 106:1871952007

  • 6

    Gosain AKSantoro TDSong LSCapel CCSudhakar PVMatloub HS: Osteogenesis in calvarial defects: contribution of the dura, the pericranium, and the surrounding bone in adult versus infant animals. Plast Reconstr Surg 112:5155272003

  • 7

    Munshi IFrim DStine-Reyes RWeir BKHekmatpanah JBrown F: Effects of posterior fossa decompression with and without duraplasty on Chiari malformation-associated hydromyelia. Neurosurgery 46:138413892000

  • 8

    Sahuquillo JRubio EPoca MARovira ARodriguez-Baeza ACervera C: Posterior fossa reconstruction: a surgical technique for the treatment of Chiari I malformation and Chiari I/syringomyelia complex—preliminary results and magnetic resonance imaging quantitative assessment of hindbrain migration. Neurosurgery 35:8748841994

  • 9

    Sala FSquintani GTramontano VCoppola AGerosa M: Intraoperative neurophysiological monitoring during surgery for Chiari malformations. Neurol Sci 32:Suppl 3S317S3192011

  • 10

    Simon MV: Intraoperative Clinical Neurophysiology. A Comprehensive Guide to Monitoring and Mapping New YorkDemos Medical2010

  • 11

    Sindou MChavez-Machuca JHashish H: Cranio-cervical decompression for Chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases— comparison with literature data. Acta Neurochir (Wien) 144:100510192002

  • 12

    Zamel KGalloway GKosnik EJRaslan MAdeli A: Intraoperative neurophysiologic monitoring in 80 patients with Chiari I malformation: role of duraplasty. J Clin Neurophysiol 26:70752009

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Article Information

INCLUDE WHEN CITING Published online September 9, 2016; DOI: 10.3171/2016.4.JNS161061.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Presurgical MR image (A) and sagittal CT scan (B) in an 11-year-old boy with CM-1.5 and a moderate basilar impression, in whom a PFD was performed at another institution without opening the dura mater (B). The postoperative control images 4 years after surgery (C and D) did not show any change in the cerebellar tonsil position or in the size and extension of the syringomyelia. The patient underwent a second surgery at the age of 16 years, involving an increased occipital bone resection, opening of the dura mater, and a wide duraplasty. The postoperative MR images (E and F) showed cerebellar remodeling with a large pseudocisterna magna, a significant tonsillar repositioning, and a small residual syrinx.

  • View in gallery

    A 6-year-old girl with a treated syndromic craniosynostosis who, when she was 6 months old, underwent PFD without opening the dura mater. Follow-up MR image (A) obtained when she was referred to our institution at the age of 4. At the age of 6, a follow-up CT scan showed a partial reossification of the occipital bone (B and C). Figure is available in color online only.

References

  • 1

    Adelson PD: Editorial. Evoked potentials and Chiari malformation Type 1. J Neurosurg [epub ahead of print April 15 2016. 10.1371/201511.JNS152624]

  • 2

    Barzilai ORoth JKorn AConstantini S: The value of multimodality intraoperative neurophysiological monitoring in treating pediatric Chiari malformation type I. Acta Neurochir (Wien) 158:3353402016

  • 3

    Burke DHicks RStephen JWoodforth ICrawford M: Assessment of corticospinal and somatosensory conduction simultaneously during scoliosis surgery. Electroencephalogr Clin Neurophysiol 85:3883961992

  • 4

    Husain AMShah D: Prognostic value of neurophysiologic intraoperative monitoring in tethered cord syndrome surgery. J Clin Neurophysiol 26:2442472009

  • 5

    Kelleher MOTan GSarjeant RFehlings MG: Predictive value of intraoperative neurophysiological monitoring during cervical spine surgery: a prospective analysis of 1055 consecutive patients. J Neurosurg Spine 8:2152212008

  • 6

    Korn AHalevi DLidar ZBiron TEkstein PConstantini S: Intraoperative neurophysiological monitoring during resection of intradural extramedullary spinal cord tumors: experience with 100 cases. Acta Neurochir (Wien) 157:8198302015

  • 7

    Kothbauer KFDeletis VEpstein FJ: Motor-evoked potential monitoring for intramedullary spinal cord tumor surgery: correlation of clinical and neurophysiological data in a series of 100 consecutive procedures. Neurosurg Focus 4:5e11998

  • 8

    Langeloo DDJournée HLde Kleuver MGrotenhuis JA: Criteria for transcranial electrical motor evoked potential monitoring during spinal deformity surgery A review and discussion of the literature. Neurophysiol Clin 37:4314392007

  • 9

    Moncho DPoca MAMinoves TFerré ACañas VSahuquillo J: Are evoked potentials clinically useful in the study of patients with Chiari malformation Type 1?. J Neurosurg [epub ahead of print April 15 2016. 10.3171/201511.JNS151764]

  • 10

    Morota NDeletis VConstantini SKofler MCohen HEpstein FJ: The role of motor evoked potentials during surgery for intramedullary spinal cord tumors. Neurosurgery 41:132713361997

  • 11

    Neuloh GPechstein UCedzich CSchramm J: Motor evoked potential monitoring with supratentorial surgery. Neurosurgery 61:3373482007

  • 12

    Nossek EKorn AShahar TKanner AAYaffe HMarcovici D: Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation. Clinical article. J Neurosurg 114:7387462011

  • 13

    Pencovich NKorn AConstantini S: Intraoperative neurophysiologic monitoring during syringomyelia surgery: lessons from a series of 13 patients. Acta Neurochir (Wien) 155:7857912013

  • 1

    Alamar MTeixidor PColet SMuñoz JCladellas JMHostalot C: [Comparison [corrected] of Chiari I malformation treatment using suboccipital craniectomy and posterior arch of C1 resection with or without dural graft.]. Neurocirugia (Astur) 19:2332412008. (Span)

  • 2

    Anderson RCEmerson RGDowling KCFeldstein NA: Attenuation of somatosensory evoked potentials during positioning in a patient undergoing suboccipital craniectomy for Chiari I malformation with syringomyelia. J Child Neurol 16:9369392001

  • 3

    Anderson RCEmerson RGDowling KCFeldstein NA: Improvement in brainstem auditory evoked potentials after suboccipital decompression in patients with Chiari I malformations. J Neurosurg 98:4594642003

  • 4

    Barzilai ORoth JKorn AConstantini S: The value of multimodality intraoperative neurophysiological monitoring in treating pediatric Chiari malformation type I. Acta Neurochir (Wien) 158:3353402016

  • 5

    Caldarelli MNovegno FVassimi LRomani RTamburrini GDi Rocco C: The role of limited posterior fossa craniectomy in the surgical treatment of Chiari malformation Type I: experience with a pediatric series. J Neurosurg 106:1871952007

  • 6

    Gosain AKSantoro TDSong LSCapel CCSudhakar PVMatloub HS: Osteogenesis in calvarial defects: contribution of the dura, the pericranium, and the surrounding bone in adult versus infant animals. Plast Reconstr Surg 112:5155272003

  • 7

    Munshi IFrim DStine-Reyes RWeir BKHekmatpanah JBrown F: Effects of posterior fossa decompression with and without duraplasty on Chiari malformation-associated hydromyelia. Neurosurgery 46:138413892000

  • 8

    Sahuquillo JRubio EPoca MARovira ARodriguez-Baeza ACervera C: Posterior fossa reconstruction: a surgical technique for the treatment of Chiari I malformation and Chiari I/syringomyelia complex—preliminary results and magnetic resonance imaging quantitative assessment of hindbrain migration. Neurosurgery 35:8748841994

  • 9

    Sala FSquintani GTramontano VCoppola AGerosa M: Intraoperative neurophysiological monitoring during surgery for Chiari malformations. Neurol Sci 32:Suppl 3S317S3192011

  • 10

    Simon MV: Intraoperative Clinical Neurophysiology. A Comprehensive Guide to Monitoring and Mapping New YorkDemos Medical2010

  • 11

    Sindou MChavez-Machuca JHashish H: Cranio-cervical decompression for Chiari type I-malformation, adding extreme lateral foramen magnum opening and expansile duroplasty with arachnoid preservation. Technique and long-term functional results in 44 consecutive adult cases— comparison with literature data. Acta Neurochir (Wien) 144:100510192002

  • 12

    Zamel KGalloway GKosnik EJRaslan MAdeli A: Intraoperative neurophysiologic monitoring in 80 patients with Chiari I malformation: role of duraplasty. J Clin Neurophysiol 26:70752009

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