Solutions to the technical challenges embedded in the current methods for intraoperative peripheral nerve action potential recordings

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OBJECTIVE

Intraoperative nerve action potential (NAP) recording is a useful tool for surgeons to guide decisions on surgical approaches during nerve repair surgeries. However, current methods remain technically challenging. In particular, stimulus artifacts that contaminate or mask the NAP and therefore impair the interpretation of the recording are a common problem. The authors’ goal was to improve intraoperative NAP recording techniques by revisiting the methods in an experimental setting.

METHODS

First, NAPs were recorded from surgically exposed peripheral nerves in monkeys. For the authors to test their assumptions about observed artifacts, they then employed a simple model system. Finally, they applied their insights to clinical cases in the operating room.

RESULTS

In monkey peripheral nerve recordings, large stimulus artifacts obscured NAPs every time the nerve segment (length 3–5 cm) was lifted up from the surrounding tissue, and NAPs could not be recorded. Artifacts were suppressed, and NAPs emerged when “bridge grounding” was applied, and this allowed the NAPs to be recorded easily and reliably. Tests in a model system suggested that exaggerated stimulus artifacts and unmasking of NAPs by bridge grounding are related to a loop effect that is created by lifting the nerve. Consequently, clean NAPs were acquired in “nonlifting” recordings from monkey peripheral nerves. In clinical cases, bridge grounding efficiently unmasked intraoperative NAP recordings, validating the authors’ principal concept in the clinical setting and allowing effective neurophysiological testing in the operating room.

CONCLUSIONS

Technical challenges of intraoperative NAP recording are embedded in the current methods that recommend lifting the nerve from the tissue bed, thereby exaggerating stimulus artifacts by a loop effect. Better results can be achieved by performing nonlifting nerve recording or by applying bridge grounding. The authors not only tested their findings in an animal model but also applied them successfully in clinical practice.

ABBREVIATIONS IONM = intraoperative neurophysiological monitoring; NAP = nerve action potential; NMB = neuromuscular blockade.

Article Information

Correspondence Matthias Ringkamp: Johns Hopkins University, Baltimore, MD. platelet@jhmi.edu.

INCLUDE WHEN CITING Published online August 16, 2019; DOI: 10.3171/2019.5.JNS19146.

Disclosures G.W. and M.R. have a patent application pending, but M.R. reports there is no conflict of interest.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Bridge grounding unmasks NAP signals from large stimulus artifacts in recordings from the peripheral nerve of the anesthetized monkey. A: Examples of recordings with or without bridge grounding. The recordings were made from the median nerve in the upper arm. The recording distance was 49 mm, and a constant current stimulus (0.05 msec, 5 mA) was applied. Without bridge grounding, a large stimulus artifact was recorded (blue trace). With the bridge grounding, the artifact was suppressed, and the NAP signal emerged (red trace). B: Photograph and schematic drawing showing the recording setup with bridge grounding. IONM electrodes, including a double-hook recording electrode and a triple-hook stimulating electrode, were applied to the nerve. Saline-soaked gauze was placed around the nerve between the stimulating and recording electrodes to bridge the nerve and the surrounding tissues, serving as bridge grounding. A piece of insulation material was placed underneath each of the electrodes to isolate them from the surrounding tissue.

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    Verification of NAP signals in recordings from the peripheral nerve of the anesthetized monkey. A: Effect of switching the stimulus polarity. The sample trace was taken from the same recording with the bridge grounding shown in Fig. 1A. On reversal of the stimulus polarity (normal: blue trace; reversed: red trace), the stimulus artifact (the voltage deflection prior to N1) was reversed but not the NAP waveform (N1, P1, and N2). Note that the latency of the NAP was shortened by reversing the stimulus polarity. For the normal (reversed) stimulus polarity the middle prong was a cathode (anode) and the outer two prongs were anodes (cathodes). B: Effect of varying the stimulus intensity. The specimen recording was from the ulnar nerve in the upper arm. The size of the stimulus artifact (early deflections circled by a dashed line: S and N1) increased with stimulus intensity whereas NAP signals showed saturation (P1 and N2). The recording distance was 51 mm, and the stimulus duration was 0.1 msec.

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    Evidence obtained in a model system supports the loop hypothesis regarding the exaggerated stimulus artifacts encountered in NAP recordings. A: Stimulus artifacts recorded in the model system without a nerve. The nerve and tissue were mimicked by saline-soaked gauze. A large stimulus artifact was recorded when the “nerve” was lifted up in the air (blue trace). The stimulus artifact was suppressed when the bridge grounding was applied (red trace) or even more diminished by “cutting” the connection between the nerve and the surrounding tissue/body (green trace). The recording distance was 60 mm, and a constant current stimulus (0.05 msec and 2 mA) was applied. B: Signals recorded in the model system using a peripheral nerve segment (monkey tibial nerve, about 10 cm). Again, a large stimulus artifact was recorded when the nerve was lifted up in the air but suppressed by bridge grounding or following a “cut.” In contrast, NAP signals (N1, P1, and N2) underwent little change upon applying the bridge grounding or after “cut.” The recording distance was 50 mm, and a constant current stimulus (0.05 msec, 1 mA) was applied. The recording setup and experimental conditions are schematically illustrated in Fig. 4.

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    Schematic drawings of the recording setup and experimental conditions used in Fig. 3. The nerve lies on the tissue, and arrows show directions of current flow. The grounding is made through the tissue. NAP recordings are made with a bipolar hook electrode and stimulation by a tripolar hook electrode. A: The nerve is lifted (loop is formed). B: The nerve is lifted but connected to the tissue underneath by a bridge (loop is disturbed). C: The nerve is lifted but “cut” at the end close to the stimulation (loop is broken). D: The nerve is not lifted (loop is not present).

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    Nonlifting nerve recording using modified IONM electrodes in the model system. The recordings were made from the monkey tibial nerve. NAP recordings are shown to the left and electrode arrangements to the right. A clean NAP was recorded when the nerve was not lifted (A). NAP signals were lost after the crush lesion was induced by ligating the nerve with a suture (indicated with a red arrow) (B). NAPs returned when the stimulating electrode was moved distally (C, inching). The stimulation (0.05 msec, 2 mA) and other parameters were kept unchanged throughout recordings. Normal stimulus polarity was used.

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    Nonlifting nerve recording in anesthetized monkey. A: Examples of NAP recordings made with in-house-made self-holding electrodes from the ulnar nerve in the upper arm. The recording distance was 31 mm. A constant current stimulus (0.05 msec, 2 mA) was used. B: Photograph and schematic drawings showing configurations of the electrodes and their actual placement. Both stimulation and recording electrodes contain three metal prongs with insulation except for the contact areas (indicated by arrowheads) and the grounding prong of the recording electrode. The nerve was placed between the middle prong and the outer two prongs of each electrode in a sandwich manner so that the electrodes were held in place by the nerve alone in a hands-free manner without the need for additional holding devices. The plastic base provides the electrode with some flexibility when holding the nerve. A and B = inputs for the amplifier; G = ground.

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    Bridge grounding unmasks NAPs recorded intraoperatively in a patient. NAPs were recorded with the standard IONM electrodes and an IONM machine. Large stimulus artifacts were recorded when the nerve was lifted and bridge grounding was not implemented (A). After the bridge grounding was placed and fully engaged, the artifacts were suppressed and NAP signals (N1, P1, and N2) emerged (B). The same stimuli (0.1 msec, 5 mA) were used in A and B (the upper trace was from stimulation with normal polarity and the lower trace was from stimulation with reversed polarity in each panel). The intensity-response test was also performed in this case, and the results are shown in an insert in panel B: 5 mA (two top traces) and 2 mA (two lower traces). The stimulus artifacts are marked by arrows. In contrast to NAP signals, stimulus artifacts did not saturate in size with increasing intensity, and their polarity changed with change in stimulus polarity. C: A photograph showing the recording arrangement. The medial antebrachial cutaneous nerve was dissected and isolated. A bipolar recording electrode and a tripolar stimulating electrode were held by hand, and a large piece of saline-soaked gauze was placed between the recording and stimulation electrodes, serving as bridge grounding. A piece of insulation material was placed underneath the electrodes to isolate them from the surrounding tissue. The recording distance was 4.5 cm. Recordings were made at room temperature (18°C).

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