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Ɓ�����(��9 �=�>0�>�9�E)dE(�:�:\E��:�y)���>>y)����>������������������������������������������������������������������������E���������` �:	Stimulus-evoked EMG monitoring during transpedicular implantation of screws in the lumbosacral spine 

Yunfen Wu MD

Study Design: Literature review.


ABSTRACT

Objective: The objective of this article is to examine stimulus-evoked electromyography (EMG) and its application in open and minimally invasive transpedicular lumbosacral spinal fixation. Different influential factors (physiological condition such as bone mineral density and other factors such as shape, size and composition in the implanted instrumentation devices, etc.) will be discussed. 
Background: A neurophysiological monitoring technique such as stimulus-evoked EMG has been developed to increase the safety of transpedicular placement of screws. There is more consensus about this stimulation methodology in open lumbar spinal fixation surgery. Nevertheless, there are no uniform protocols of this testing modality in minimally invasive surgery.
Methods: Review of the literature was performed using the Web of Science and PubMed databases. Given the fact that constant current stimulation remains the most commonly used type of stimulation, only English language articles involving studies performed on humans with this stimulation technique were included. 
Results: In total, twenty-two studies on the accuracy of stimulus-evoked EMG monitoring during transpedicular implantation of screws in the lumbosacral spine articles were identified. Only thirteen (nine on open surgery and four on minimally invasive surgery) were included in this review. Few studies have described detail methodologies. The reported reliability of stimulus-evoked EMG in identifying malpositioned pedicle screws is significantly variable in both open and minimally invasive surgery. 
Conclusion: Stimulus-evoked EMG offers some advantages in comparison to assistive techniques. Laminectomy for direct                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                     inspection of the placed screws increases operative time and morbidity. In addition, fluoroscopy and CT increase radiation exposure. However, stimulus-evoked EMG monitoring should be used in conjunction with imaging techniques to optimize the accuracy of transpedicular screw implantation. Moreover, a variation of physiological conditions (i.e. the bone mineral density) and other factors such as shape, size, and composition in the implanted instrumentation devices should be considered for a judgment of the stimulation threshold for safe implantation.

KEY WORDS. Electromyography (EMG), pedicle screw, lumbosacral spine fixation 

ABBREVIATIONS. Electromyography (EMG), computed tomographic (CT), compound muscle action potential (CMAP).

1. INTRODUCTION

The implantation of pedicle screw instrumentation in the spine was introduced by King [1,2] in the decade of the 1940s. Two decades later, Roy-Camille and colleagues were the pioneers in using a plate that connected implanted pedicle screws to enhance mechanical stability [3]. Currently, transpedicular instrumentation is widely used for treatment of spinal degenerative changes, traumatic lesions and spinal deformities [4]. Furthermore, minimally invasive pedicle screw fixation of the lumbar spine was introduced by Foley and Gupta and Khoo et al in 2002 [5]. Minimally invasive procedures are gaining wide-spread application in lumbar fixation by providing advantages such as smaller incisions, less morbidity and postoperative pain, and a shorter rehabilitation. 

There is a lack of a complete reliability for identifying misplaced screws even when using computed tomographic (CT) scanning (3D image) [6]. In addition, the excessive time and morbidity are associated with direct inspection of each pedicle. An electrophysiological technique such as stimulus-evoked electromyography (EMG) is therefore used to improve the safe and appropriate placement of pedicle screws.
 
Intraoperative neuromonitoring for evaluating the structural integrity of the pedicle during transpedicular instrumentation was introduced in the decade of the 1990s [7,8]. This technique has a special relevance in minimally invasive procedures, where lack of direct visualization of landmark poses a greater risk to nerve injury than open surgeries [9,10]. There is more consensus about the stimulation techniques and alarm criteria for an acceptable transpedicular placement of screws in open lumbar spinal fixation surgery. Nevertheless, there are no uniform protocols and reports on the reliability of this testing modality in minimally invasive surgery. 

The aim of this review consists of the integration and summarization of the preliminary findings of the completed studies on stimulation methodologies of pedicle screw for lumbosacral spinal fixation, the discussion on the potential significance of this method and different influential factors, and the proposition of future research.
	
2. METHODS

2.1. Selection of studies and inclusion criteria 

A systematic literature search was conducted using Web of Science and PubMed databases (until December, 2013), including the following criteria:
(1) English language articles.
(2) Human study.
(3) Pedicle screw stimulation during lumbosacral spinal fixation.
(4) Use of constant-current stimulation.
(5) Evaluation of pedicle screws position.
(6) Assessment of the reliability of stimulus-evoked EMG during pedicle screw placement.

2.2. Collection of data

The following variables were extracted from all studies when available, and then were collected using a table: 
(a) Number of patients.
(b) Etiological diagnoses.
(c) Number and type of implanted pedicle screws.
(d) The warning threshold to advise a possible breach of a pedicle wall.
(e) Data of positive EMG (lower threshold value than the determined alarm threshold) and breaches. 

3. RESULTS

Twenty-two studies were identified and thirteen were selected.

The characteristics of the reviewed pedicle screw stimulation methodologies and accuracy in open lumbosacral spinal fixation surgery are presented in table I and those variables extracted from studies on minimally invasive surgery are summarized in table II. 


Categorization of statistical results: 


Sensitivity: a true positive finding is defined as a low threshold with a confirmed malpositioned screw.

Specificity: a true negative finding is defined as an �acceptable� screw threshold corresponding to a correctly positioned screw.

A false positive finding is defined as a low screw threshold with a correctly positioned screw. 

A false negative finding is defined as an �acceptable� threshold with a confirmed malpositioned screw.

3.1 THRESHOLD TESTING IN OPEN SURGERY

Six studies described the detailed parameters of stimulation. Three studies employed the same stimulation duration (200us) [8,11,12]. Two out of these studies employed 3 Hz of stimulation frequency [8,11]. Calancie et al. reported a higher false positive rate by application of a lower alarm threshold (7mA) in comparison to the rest of two studies [8]. In the study by Clement et al., twelve breaches associated to malpositioned screws were identified by palpation. All breached screws had a positive EMG or low threshold (�11mA) in relation to the referential threshold. In this group, new radiculopathy was reported in only one patient. These authors reported a higher sensitivity of stimulus-evoked EMG in identifying malpositioned screws, since x-ray technique detected only four out of these twelve breaches [11]. Toleikis et al. reported one false negative case. This patient developed unilateral leg pain after surgery despite an apparent acceptable threshold of stimulation (40-50mA for the four placed screws) [12]. 

Glassman et al. employed the highest alarm threshold among the reviewed studies. However, in this study, despite applying a higher rate of stimulation in comparison to the classical method described by Calancie et al. study, the duration (50us) of stimulation was shorter. Radiographic and CT studies revealed a total of fourteen breaches associated with malpositioned screws. All of these breaches had stimulation thresholds greater than 15mA. Nevertheless, clinical consequences were not reported [13].

Three groups of authors [14-16] applied stimulation threshold of 8mA to determine electrical breaches of the pedicle wall. Only Raynor and colleagues specified the duration (300us) of stimulation. In Raynor et al. study, sensitivity dramatically decreased by reducing alarm threshold. A better sensitivity and specificity in combination were observed at 8mA cutoff [14]. In regards to the study by Kim et al., only data of placed pedicle screws in the lumbosacral spine were included. No statistically significant differences between the four types (virgin, previous hole, fusion mass and pseudarthrosis) of pedicle screws were observed. No chronic complication associated to screw placement have been reported. In addition, the accuracy of the stimulation method was comparable to the radiographic evaluation in this study [15]. On the other hand, study by Alemo et al. reported three false negative cases. Two out of these three patients developed chronic neurologic deficit [16].

The two remaining groups of authors applied a screening stimulus at 10mA. In the study performed by Parker et al., the surgeons elected to revise the screw position when a threshold was less than 7 mA. In this study, sensitivity was also dramatically decreased by reducing the alarm threshold [17]. Kulik et al. reported a low sensitivity of threshold testing. No different stimulation threshold was observed in compressive nerve roots. Furthermore, there was no correlation between the screw edge, the pedicle edge and the corresponding threshold [18].

3.2 THRESHOLD TESTING IN MINIMALLY INVASIVE SURGERY

Few neuromonitoring studies have described in detail the methodologies for minimally invasive lumbosacral spinal fixation surgery. For this review, four studies have been selected.

Ozgur et al. applied an alarm criterion of 10.0 mA at lumbar levels and 8 mA at sacral levels. 89% of the tap threshold was higher than the k-wire threshold, and the remaining 11% was less [9]. 

Bindal and Ghosh et al. reported 76% of screw placements required changes in the trajectory of the pedicle access needle. Although the resulted threshold was >15.0 mA in all tested pedicle screws, postoperative images revealed three cases of lateral breach. However, no clinical complications occurred [10]. 

Wang et al. study reported that all 5 breaches associated with malpositioned screws had a threshold >12mA. Two medial pedicle breaches were associated with sensory symptoms. In one case, the patient developed transient numbness. In another case, screw removal resulted in relief of the painful symptom [19].

The study by Wood and Mannion concluded that using the combination of navigation technique and stimulus-evoked EMG resulted in a lower rate of pedicle screw malposition in comparison with the use of the navigation modality alone [20].

4. DISCUSSION

Constant current stimulation remains the most commonly used type of stimulation. In this review, studies that used constant current stimulation were included to reach a better comparative analysis between the reviewed stimulus-evoked EMG methodologies during the transpedicular screw placement. The required intensity of a single pulse of current to activate a spinal nerve root for eliciting a constant and minimal compound muscle action potential (CMAP) is defined as the threshold. The classical stimulation technique described by Calancie et al. consists of an application of constant cathodic current pulses of 200us at a rate of 3 Hz. A threshold�7mA was considered by these authors as an indicator of alarm from stimulation of nerve roots [8]. An important variance in threshold values (ranged from 8-15mA) and parameters of stimulation have been investigated after Calancie et al. study. Nevertheless, the reported reliability of identification of malpositioned pedicle screws was significantly variable. 

Theoretically, a low intensity of current pulse passed through the implanted screw and/or intervening bony structure of the pedicle, and consequently eliciting a CMAP may suggest pedicle screw malposition (such as a potential pedicle fracture, canal breach, or foraminal encroachment, etc) based on lowered resistance. Moreover, the risk of neurological injury is higher when a screw is placed at or through the site of an inferior-medial perforation in comparison with a lateral perforation [21,22]. Lower threshold values are more accurate in identifying a medially malpositioned screws [14]. Nevertheless, a low stimulation threshold does not necessarily indicate a threat of potential neurological injury. The decision whether the location of the pedicle screw is acceptable in the presence of a perforation should not be based only on the threshold. Several additional considerations should be regarded for threshold judgment throughout transpedicular implantation of screws into the lumbosacral spine.

Parameters of stimulation:
Based on the different stimulus results from variable combinations of intensity, duration and frequency throughout stimulation, the accuracy in identifying misplaced screw may be inconstant. In minimally invasive surgeries, constant stimulation offers a greater advantage in comparison with the intermittent and sequential stimulation technique by providing an early warning during hole formation and insertion of the pedicle screw [23].

Physiological condition: 
S1 pedicle has thinner cortical walls and a lower bone mineral density with poor impedance in comparison with the lumbar levels. In contrast, L4 pedicle and cortex have the highest bone mineral density of the lumbosacral vertebrae [24]. Although exact values have not been reported, a higher threshold for the L4 pedicle and a lower threshold than normal for the S1 pedicle might be expected. In addition, the anatomical proximity of the neurological structures to the implanted pedicle screw also has an important role in affecting threshold value [9]. 

Pathological condition:
Low thresholds can be associated with implanted screws in osteoporotic pedicles in the absence of a breach [25]. Opposite phenomenon can be observed in chronic nerve compression (with axonotmesis and axon loss) [26] and metabolic disorders (e.g. diabetes) [12]. Nevertheless, Kulik and colleagues did not observe any difference in the screw stimulation threshold in patients with diagnosis of chronic neuropathy [18]. 

Distance between the pedicle edge and screw edge: 
After the redirection/reposition of a screw in consequence of a determination of a significantly low threshold due to a pedicle wall defect, the retesting threshold may yield a higher value. Nevertheless, Kulik et al. reported the lack of direct correlation between the screw edge and pedicle edge and the corresponding threshold [18]. 

Screw composition and shapes:
There is no data about composition-conductivity of screw and the resulting threshold. Nevertheless, a "conductive variability" may exist between different types of screws. Titanium screws with high aluminum content have been found to have an increased conductance. On the other hand, alarm threshold for minimally invasive surgery is based on referential value for open surgery. However, in open surgery, solid pedicle screws are mostly used. In contrast, polyaxial hollow pedicle screws are usually employed in minimally invasive surgery. Since the resistance of hollow pedicle screws is higher than solid pedicle screws [27], alarm threshold might be different for pedicle screw testing in minimally invasive surgery.

Instrumentation size:
The same threshold stimulation was applied to all tested instrumentation devices in each reviewed study of minimally invasive surgery. However, the tap screw is typically larger than the pedicle access needle. The guide-wire has the smallest diameter. In this regard, the alarm threshold of stimulation might be different for each of these instrumentation devices. 

Isolation system:
During minimally invasive pedicle screw placement, the conductivity of wound fluids and soft tissue can influence the resulting threshold.  An adequate isolation of the soft tissue and suction of wound fluids is crucial for an accurate evaluation of the instrumentation device stimulation threshold to prevent conduction phenomenon in minimally invasive surgery. Non-metal dilator sleeves provide a more isolated effect and consequently a more accurate predictor of cortical breach when it is compared with the metallic dilator. However, using a traditional suction system does not allow continuous suction of the wound fluid during minimally invasive pedicle screw placement. 

Myotomal for stimulus-evoked EMG Monitoring
Since lower extremity muscles (myotomes) often receive innervations from multiple spinal nerve roots, EMG recording from different muscles of the same myotome may increase the sensitivity of the stimulation technique of screws at one lumbar level.

Proposal for further research for minimally invasive pedicle screw placement:
According to the different sizes and compositions between the guide-wire, the pedicle access needle, the tap and the screws, different alarm thresholds should be assigned for testing.
In regards to the small incision of the minimally invasive surgery, isolation still has some limitations even with the use of non-metallic sleeves. Continuous suction of the wound fluid using a traditional suction system during the testing technique is impossible. The wound liquid in the stimulating field may alter the resulting threshold due to the current shunting. The incorporation of an adapted continuous suction system may overcome this limitation and consequently optimize the stimulation accuracy. 

5. CONCLUSION.

Accurate pedicle screw placement is essentially a technical challenge. Stimulus-evoked EMG offers some advantages in comparison to assistive techniques. First, laminectomy for direct                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                  inspection of the placed screws increases operative time and morbidity. In addition, fluoroscopy and CT increase radiation exposure. However, neurophysiology monitoring should be used in conjunction with imaging techniques to optimize the safety of screw implantation. Moreover, a variation of physiological conditions (i.e. the bone mineral density) and other factors such as shape, size, and composition in the implanted instrumentation devices should be considered for a judgment of the stimulation threshold. 

6. ACKNOWLEDGMENT

I would like to acknowledge Dr. Sedat Ulkatan for his many insightful suggestions and teachings during my fellowship in Intraoperative Neurophysiology. I thank Dr. Vedran Deletis for giving me the opportunity to participate in the fellowship program at Mount Sinai Roosevelt Hospital in New York City. I would also like to thank Drs. Mar HYPERLINK "http://en.wikipedia.org/wiki/Dulce_Mar%C3%ADa" �a Angeles Mart HYPERLINK "http://en.wikipedia.org/wiki/Mart%C3%ADnez" �nez Mart HYPERLINK "http://en.wikipedia.org/wiki/Mart%C3%ADnez" �nez and Roberto Oc HYPERLINK "http://catalandeocon.com/" �n Quintial for their mentoring in Intraoperative Neurophysiology throughout my residency at Hospital Universitario Marqu�s de Valdecilla in Santander, Spain. 

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