A NEW PITFALL IN A SENSORY CONDUCTION STUDY OF THE LATERAL ANTEBRACHIAL CUTANEOUS NERVE: SPREAD TO THE RADIAL NERVE CHIZUKO OISHI, MD,1 MASAHIRO SONOO, MD,2 HIROKO KURONO, MD,2 YUKI HATANAKA, MD,2 TERUO SHIMIZU, MD,2 ATSURO CHIBA, MD,1 and MANABU SAKUTA, MD1 1 2
Department of Neurology, Faculty of Medicine, Kyorin University, Tokyo, Japan Department of Neurology, Teikyo University School of Medicine, Tokyo, Japan
Accepted 20 November 2013 ABSTRACT: Introduction: We describe a previously unreported pitfall, spread of the stimulus at the elbow to the radial nerve, in an antidromic sensory nerve conduction study of the lateral antebrachial cutaneous (LAC) nerve. Methods: Subjects consisted of 80 healthy volunteers, and both sides were examined for each subject. Besides routine recording of the LAC nerve, sensory nerve action potentials (SNAPs) of the radial nerve were recorded distally. Results: The spread phenomenon occurred in 73 of 160 arms (46%), and the SNAP amplitude increased due to contamination of the radial SNAP up to 6.7 times the genuine LAC SNAP. In 10 arms (6%), the spread started before the LAC SNAP was saturated, and the genuine LAC SNAP was unknown due to an anatomical variation in at least 1 arm. Conclusions: Without monitoring distal radial SNAPs, the spread phenomenon will remain unrecognized. This pitfall undermines the reliability of the test. Muscle Nerve 50: 186–192, 2014
The lateral antebrachial cutaneous nerve (LAC) is the terminal branch of the musculocutaneous nerve. Antidromic sensory nerve conduction study (SCS) of the LAC nerve is widely employed for diagnosis of plexopathy or musculocutaneous nerve palsy.1–3 Several studies have addressed its normal values.1,4–8 However, some of them reported rather large intersubject and interside variations in the amplitude of the sensory nerve action potential (SNAP) of this nerve,8 which may limit the clinical utility of this test. We found a previously unreported pitfall in the antidromic SCS of the LAC nerve: the spread of stimulation to the radial nerve at the elbow level.9,10 For routine antidromic SCS of the LAC, the nerve is stimulated just lateral to the biceps brachii tendon, and the SNAP is recorded 12 cm distally.11 The radial nerve may run unexpectedly close to the stimulus point for the LAC.12 If the Abbreviations: EPL, extensor polllicis longus; LAC nerve, lateral antebrachial cutaneous nerve; SCS, sensory nerve conduction study; SNAP, sensory nerve action potential Key words: lateral antebrachial cutaneous nerve; pitfall; radial nerve; sensory nerve conduction study; spread phenomenon This study was supported by Grants-in-Aid for Scientific Research (19591011 and 23591285) from the Ministry of Education, Science, Sports and Culture of Japan, and by Health and Labour Sciences Research Grants for research on intractable diseases (Neuroimmunological Disease Research Committee) from the Ministry of Health, Labour and Welfare of Japan. Correspondence to: M. Sonoo; e-mail: [email protected] C 2013 Wiley Periodicals, Inc. V
Published online 24 November 2013 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24129
186
Pitfall in LAC Conduction
stimulation spreads to the radial nerve, the SNAP of the superficial branch of the radial nerve, which also runs close to the LAC nerve at the recording point for the LAC,12 will contaminate its SNAP and will result in an erroneously enlarged potential. We investigated the frequency of this spread phenomenon among control subjects and evaluated its influence on the SCS of the LAC nerve. METHODS
Subjects consisted of 80 healthy volunteers (39 men and 41 women, aged 24–82 years). All subjects gave informed consent to participate, and the study was approved by the clinical ethics committee of the Teikyo University School of Medicine (approval number: 09-059). A square-wave pulse of 0.2-ms duration was given using surface stimulating electrodes. The SNAPs were recorded using a number of different types of electrodes, as explained later. The responses were amplified and filtered between 10 HZ and 5 kHZ (23 dB) using an electromyography machine (Neuropack 2000; Nihon Kohden Co.). The amplifier gain was set at 10–50 lV/division, depending on the size of the SNAPs, and the analysis time was set at 20 ms. Usually, 10–20 responses were averaged, and the onset latency and peak-topeak amplitude of the SNAP were measured. Both sides were examined for each subject. The forearm skin temperature was monitored and was maintained at 33 C throughout the examination. For antidromic SCS of the LAC nerve, stimulation was given at the elbow just lateral to the tendon of the biceps brachii muscle, and the LAC SNAP was recorded 12 cm distal to the stimulation over the forearm using a saddle-type electrode (Oxford Instruments Co.) with 20 3 7-mm bar electrodes separated by 19 mm from one another in the center. In addition, SNAPs of the superficial branch of the radial nerve were recorded distally using the following 2 derivations to judge whether stimulation of the LAC nerve spread to the radial nerve (Fig. 1). First, ring electrodes were placed around the thumb, the active electrode at the base and the reference electrode distally. Second, electroencephalographic disk electrodes were used; the active electrode was placed over the superficial radial nerve crossing over the tendon of the MUSCLE & NERVE
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FIGURE 1. Electrode placement. Stimulation of the LAC nerve was applied at the elbow, and the LAC SNAP was recorded 12 cm distally on the forearm (channel 1). The SNAPs of the superficial branch of the radial nerve were recorded distally around the thumb (channel 2) and on the tendon of the extensor pollicis longus muscle (channel 3). Stimulation of the LAC nerve may spread to the superficial branch of the radial nerve running nearby, and its SNAP may contaminate the recording in channel 1. Ch, channel; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
extensor pollicis longus (EPL), and the reference electrode was placed distally over the metacarpophalangeal joint of the index finger. Before performing antidromic SCS, the best recording point was determined by orthodromic SCS, just as is typically done for the medial antebrachial cutaneous nerve.13 First, the recording electrode was placed at the elbow, and stimulation was given on the forearm. The position of the stimulating electrode was moved minutely, and the point evoking the orthodromic SNAP with the lowest threshold was found. Very weak stimulation, usually 6 times the true LAC SNAP (7.3 lV at 2 mA). Pattern C: a 37-year-old man. Spread to the radial nerve started at the lowest intensity (0.8 mA), and both the forearm and radial SNAPs were saturated at 2.0 mA. EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
A and B. This SNAP solely attributable to the LAC nerve was defined as the “true SNAP.” The true SNAP for pattern A and the false SNAPs for patterns B and C would be taken to be the maximum LAC SNAPs when the radial SNAPs are not monitored. Therefore, these measurements were collectively termed the “apparent (LAC) SNAP.” The peak-to-peak amplitude values of the true and false SNAPs were recorded, as well as the current values of: (a) the maximum intensity for the LAC SNAP; (b) the threshold for radial spread; and (c) the maximum intensity for the radial SNAP. The interside difference of the SNAP amplitude, which has been used widely as the criterion to determine abnormality in SCSs,2,14 was evaluated for both the true and apparent SNAPs. For some subjects, additional experiments were performed to investigate the possibility of anatomical variation, especially for pattern C arms. Using similar recording electrodes, proximal stimulation of the radial or musculocutaneous nerve was also conducted. The radial nerve was stimulated in the arm at the spiral groove. The musculocutaneous 188
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nerve was stimulated distal to the axilla posteromedial to the biceps brachii muscle. The CMAP of the biceps brachii muscle was used as an index of musculocutaneous nerve stimulation. To confirm that the superficial radial SNAP was also recorded by the recording electrode for the LAC nerve, we conducted an additional experiment to stimulate the radial nerve distally over the EPL tendon in 4 arms (1 pattern A and 3 pattern B arms) of 4 control subjects. For these arms, the optimal stimulation site for the superficial radial nerve was also localized at the mid-forearm level and was compared with the optimal site for the LAC nerve. Thumb stimulation was also performed in 2 of these arms. For statistical analysis, SNAP amplitude values of different subject groups were compared using the 2-sample t-test. RESULTS
Patterns A, B, and C were observed in 87, 63, and 10 of the 160 arms examined, respectively. The amplitudes of true and false LAC SNAPs for MUSCLE & NERVE
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Table 1. SNAP amplitude for each pattern.
Pattern A True SNAP* Pattern B True SNAP* False SNAP† Pattern C False SNAP† All True SNAP Apparent SNAP‡
N
ppAmp (mV)[mean 6 SD (range)]
87
27.3 6 12.9 (7.9–74.0)
63 63
29.7 6 16.9 (5.4–98.0) 52.6 6 24.2 (7.2–152.5)
10
59.2 6 21.4 (31.9–96.8)
150 160
28.3 6 14.7 (5.4–98.0) 39.3 6 22.8 (7.2–152.5)
False/true ppAmp ratio 206 6 101% (105–674%)
LAC, lateral antebrachial cutaneous (nerve); ppAmp, peak-to-peak amplitude; SNAP, sensory nerve action potential. *True SNAP: pure LAC SNAP saturated without contamination by spread to the radial nerve. This was defined only for patterns A and B. †
False SNAP: SNAP saturated for both the LAC and radial nerves. This was defined only for patterns B and C.
‡
Apparent SNAP indicates the true SNAP for pattern A and false SNAPs for patterns B and C.
each pattern are summarized in Table 1. The amplitude of the false SNAP was 206 6 101% (range 105–674%) of the true SNAP for 63 pattern B arms; that is, the false SNAP may reach as much as 7 times the true SNAP. The stimulus intensity that achieved maximum stimulation of the LAC nerve was usually low, 4.7 6 1.7 mA (1.6–11.0 mA). Spread to the radial nerve started at 10.0 6 5.5 mA (0.8–26 mA), and at 10 mA for 63% of pattern B or C arms. The interside difference in true SNAPs was 26.8 6 18.1% (range 0.4–76.3%) and exceeded 50% in 8 of 71 subjects (11%) for whom it was definable (neither arm was pattern C). The interside difference of apparent SNAPs was 31.4 6 20.2% (0.4–86.0%) and exceeded 50% in 12 of 80 subjects (15%). The amplitudes of the true LAC SNAPs for each age and gender group are summarized in Table 2. Older subjects (60 years) had significantly lower amplitudes than young or middleaged subjects. Men had significantly higher amplitudes than women. However, the intersubject variation of the SNAP amplitude was rather large and far exceeded the effect of such intergroup variations; the true SNAP amplitude for all arms was 28.3 6 14.7 lV (range 5.4–98.0 lV). For 3 arms in 3 subjects with pattern C, proximal radial and musculocutaneous stimulations were investigated. In 1 arm (Fig. 3), both the forearm LAC SNAP and distal radial SNAPs were elicited by musculocutaneous nerve stimulation, whereas proximal radial nerve stimulation elicited neither response. In another pattern C arm (Fig. 4) and 1 arm each of patterns A and B, musculocutaneous nerve stimulation elicited the forearm LAC SNAP, whereas proximal radial nerve stimulation elicited the distal radial SNAPs as well as the SNAP at the forearm recording electrode for LAC, Pitfall in LAC Conduction
which actually must have been caused by spread of the radial SNAP. In the last pattern C arm, none of the musculocutaneous, radial, or median nerve stimulations of the arm elicited a response at the forearm “LAC” electrode that was comparable to that elicited after elbow stimulation. Supramaximal stimulation at the Erb point was not possible in this subject. In the additional experiment of orthodromic radial nerve stimulation, stimulation of the superficial radial nerve over the EPL tendon elicited sizable SNAPs over both the thumb and over the forearm recording site for the LAC in all 4 arms. Typical results in a pattern B arm are illustrated in Table 2. Amplitude of true LAC SNAP in each subject group. Subjects (N) Young (20–39 years) Men 17 Women 19 All 36 Middle-age (40–59 years) Men 11 Women 10 All 21 Aged (601 years) Men 11 Women 11 All 22 All ages Men 39 Women 40 All 79
Arms (N)
ppAmp [mean 6 SD (range)]
33 37 70
36.0 6 16.9 (9.1–74.0) 27.0 6 15.4 (9.0–98.0) 31.3 6 16.7 (9.0–98.0)
22 17 39
31.7 6 12.6 (10.3–57.7) 26.6 6 10.6 (13.2–49.7) 29.5 6 11.9 (10.3–57.7)
20 21 41
25.0 6 12.6 (7.9–43.1) 19.4 6 10.2 (5.4–45.8) 22.1 6 11.6 (5.4–45.8)*
75 75 150
31.8 6 15.2 (7.9–74.0) 24.8 6 13.4 (5.4–98.0)† 28.3 6 14.7 (5.4–98.0)
The intersubject variation of the SNAP amplitude is rather large and far exceeds intergroup variations. LAC, lateral antebrachial cutaneous (nerve); ppAmp, peak-to-peak amplitude; SNAP, sensory nerve action potential. *Older subjects had a significantly lower amplitude compared with young (P < 0.002) or middle-aged (P < 0.01) subjects. †
Men had a significantly higher amplitude than women (P < 0.005).
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FIGURE 3. Pattern C arm shows the lack of the superficial branch of the radial nerve (same subject as shown in Fig. 2 for pattern C). Both the forearm LAC SNAP and distal radial SNAPs were elicited by musculocutaneous nerve stimulation of the proximal arm. Proximal radial nerve stimulation elicited neither response. Bic, biceps brachii; CMAP, compound muscle action potential; EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
FIGURE 4. Pattern C arm, with no anomaly, of a 25-year-old woman. Elbow stimulation revealed that the weakest stimulation elicited both forearm and distal radial SNAPs (therefore, pattern C). Isolated stimulation of the LAC nerve was not possible despite extensive exploration of the appropriate stimulation site at the elbow. Musculocutaneous nerve stimulation elicited a forearm LAC SNAP (plus a small SNAP around the thumb), whereas proximal radial nerve stimulation elicited distal radial SNAPs as well as the SNAP in the forearm recording electrode for LAC, which must actually be spread of the radial SNAP. In this subject, no anomaly existed, and the spread was caused only by the close proximity of the 2 nerves. Bic, biceps brachii; CMAP, compound muscle action potential; EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential. 190
Pitfall in LAC Conduction
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FIGURE 5. Distal radial nerve stimulation in a 37-year-old woman. First, we determined the best recording site for the LAC nerve using orthodromic LAC recording, and the site that activated the superficial radial nerve with the lowest threshold by monitoring the distal radial SNAPs. The image represents the stage at which these localizations were completed. The radial nerve was 7 mm lateral to the LAC nerve (2 arrow heads). Then, the superficial radial nerve over the EPL tendon was stimulated, and the orthodromic forearm response and the antidromic thumb responses were recorded (lower left). Saturated stimulation of the radial nerve over the EPL tendon was achieved at a rather low intensity (5 mA). The electrode over the LAC nerve clearly recorded a sizable SNAP, which was only slightly smaller than that recorded over the best recording site for the radial nerve. The results of LAC stimulation at the elbow (lower middle), without (6 mA) and with (14 mA) spread to the radial nerve, are also shown. EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
Figure 5. At the forearm level, the site that activated the radial nerve with the lowest threshold (determined by distal radial response over the thumb and the EPL tendon) was 4–9 mm lateral to the site that solely activated the LAC nerve with the lowest threshold (determined by the orthodromic LAC recording) for 4 arms. After distal radial nerve stimulation, the SNAP recorded over the LAC recording site at the forearm was only slightly smaller than that recorded over the radial recording site determined above (Fig. 5) for all arms. Thumb stimulation also elicited a radial nerve SNAP over the LAC recording site at the forearm (not shown). DISCUSSION
We have described a previously unreported pitfall of stimulus spread to the radial nerve during antidromic SCS of the LAC nerve. This pitfall would not be noticed without monitoring radial SNAPs distally. The spread phenomenon occurred in as many as 46% of the arms of control subjects, and in at least 1 arm of 59% of subjects. In 6% (10 of 160) of examined arms, the spread started before the LAC SNAP was maximized, and the maximum amplitude of the genuine LAC SNAP was unknown (pattern C). Pitfall in LAC Conduction
The maximum intensity required to achieve saturation of the genuine LAC SNAP was usually very low, 10 mA in 99% of arms (all but 1) and 5 mA in 75% of arms using a 0.2-ms duration. Therefore, if the LAC amplitude continued to increase over 10 mA, this was probably due to spread of stimulation to the radial nerve. However, this pitfall cannot be avoided by this strategy, because even spread to the radial nerve often started at 10 mA (63% of arms where the spread occurred). As shown by the distal radial nerve stimulation experiment, the superficial radial nerve runs close to the LAC nerve at the forearm level, and a radial SNAP will be recorded at the ordinary LAC recording site if the radial nerve is coactivated during LAC stimulation at the elbow. Without monitoring distal radial SNAPs, the SNAP measured at saturation for both the LAC and radial nerves would be assumed to be the “LAC SNAP” (false SNAP) for patterns B and C. The amplitude of this type of false SNAP may be almost 7 times the genuine LAC SNAP. The reported large intersubject variation1,6–8 and the large intrasubject right-to-left difference8 of the LAC SNAP amplitude may well be due to this pitfall. This study has revealed that both intersubject variation and intrasubject side differences were larger for the apparent SNAP MUSCLE & NERVE
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(genuine SNAP for pattern A and false SNAPs for patterns B and C) than for the genuine SNAP (measurable for patterns A and B). However, even the interside difference for genuine SNAPs exceeded 50% in 11% of subjects for whom the difference was measurable. The maximum side-toside difference was 76%. In this regard, the “50% rule” is not always applicable to the LAC nerve, and we should be careful in using it for evaluation of plexopathy.2,14 Pattern C may be due to anatomical variation of the paths of the radial and musculocutaneous nerves. This possibility was investigated in 3 arms showing pattern C. Absence of the superficial branch of the radial nerve and total replacement of the innervation to the dorsum of the thumb and index finger by the LAC nerve has been reported.15–17 One of the 3 pattern C arms in this series was found to have this variation (Fig. 3). Results in another pattern C arm indicated that the inability to carry out separate stimulations at the elbow was due to close proximity of the 2 nerves, as proximal stimulation elicited different responses from these 2 nerves, respectively, as expected (Fig. 4). The results for the last pattern C arm could not be explained. None of the radial, musculocutaneous, or median nerve stimulations at the arm level elicited a response comparable to that elicited after elbow stimulation. This may have been due to the general difficulty in applying stimulations in this muscular male subject. In any case, the relative contribution of the 2 causes of difficult separation, anatomical variation or simple proximity, needs further investigation.
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REFERENCES 1. Spindler HA, Felsenthal G. Sensory conduction in the musculocutaneous nerve. Arch Phys Med Rehabil 1978;59:20–23. 2. Ferrante MA, Wilbourn AJ. The utility of various sensory nerve conduction responses in assessing brachial plexopathies. Muscle Nerve 1995;18:879–889. 3. Sander HW, Quinto CM, Elinzano H, Chokroverty S. Carpet carrier’s palsy: musculocutaneous neuropathy. Neurology 1997;48:1731–1732. 4. Trojaborg W. Motor and sensory conduction in the musculocutaneous nerve. J Neurol Neurosurg Psychiatry 1976;39;890–899. 5. Kimura I, Ayyar DR. Sensory nerve conduction study in the medial antebrachial cutaneous nerve. Tohoku J Exp Med 1984;142:461–466. 6. Izzo KL, Aravabhumi S, Jafri A, Sobel E, Demopoulos JT. Medial and lateral antebrachial cutaneous nerves: standardization of technique, reliability and age effect on healthy subjects. Arch Phys Med Rehabil 1985;66:592–597. 7. Karandreas N, Papatheodorou A, Triantaphilos I, Mavridis M, Lygidakis C. Sensory nerve conduction studies of the less frequently examined nerves. Electromyogr Clin Neurophysiol 1995;35:169–173. 8. Buschbacher R, Koch J, Emsley C, Katz B. Electrodiagnostic reference values for the lateral antebrachial cutaneous nerve: standardization of a 10-cm distance. Arch Phys Med Rehabil 2000;81:1563–1566. 9. Oishi C, Sonoo M, Kurono H, Shiimzu T, Sakuta M. A new pitfall in sensory conduction study of LAC: spread to the radial nerve. Muscle Nerve 2006;34:530. 10. Oishi C, Sonoo M, Shimizu T, Chiba A. Normal valuse of the lateral antebrahial cutaneous nerve (LAS) sensory. J Neurol Sci 2009; 285(suppl):S329. 11. Ma DM, Liveson JA. Nerve conduction handbook. Philadelphia: F.A. Davis; 1983. p 62. 12. Beldner S, Zlotolow DA, Melone CP Jr, Agnes AM, Jones MH. Anatomy of the lateral antebrachial cutaneous and superficial radial nerves in the forearm: a cadaveric and clinical study. J Hand Surg 2005;30:1226–1230. 13. Higashihara M, Sonoo M, Tsuji S, Ugawa Y. Two-step technique to optimize the medial antebrachial cutaneous nerve response. Clin Neurophysiol 2010;121:712–713. 14. Bromberg MB, Jaros L. Symmetry of normal motor and sensory nerve conduction measurements. Muscle Nerve 1998;21:498–503. 15. Appleton AB. A case of abnormal distribution of the N. musculocutaneus, with complete absence of the ramus cutaneus N. radialis. J Anat Physiol 1911;46:89–94. 16. Yogesh A, Marathe R, Pandit S. Musculocutaneous nerve substituting for the distal part of radial nerve: a case report and its embryological basis. J Neurosci Rural Pract 2011;2:74–76. 17. Davidovich ER, Caetano MR, Nascimento OJ. Total lesion of the radial nerve in the arm with preservation of the superficial radial nerve sensory action potential. Arq Neuropsiquiatr 2013;71:67–68.
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Department of Neurology, Faculty of Medicine, Kyorin University, Tokyo, Japan Department of Neurology, Teikyo University School of Medicine, Tokyo, Japan
Accepted 20 November 2013 ABSTRACT: Introduction: We describe a previously unreported pitfall, spread of the stimulus at the elbow to the radial nerve, in an antidromic sensory nerve conduction study of the lateral antebrachial cutaneous (LAC) nerve. Methods: Subjects consisted of 80 healthy volunteers, and both sides were examined for each subject. Besides routine recording of the LAC nerve, sensory nerve action potentials (SNAPs) of the radial nerve were recorded distally. Results: The spread phenomenon occurred in 73 of 160 arms (46%), and the SNAP amplitude increased due to contamination of the radial SNAP up to 6.7 times the genuine LAC SNAP. In 10 arms (6%), the spread started before the LAC SNAP was saturated, and the genuine LAC SNAP was unknown due to an anatomical variation in at least 1 arm. Conclusions: Without monitoring distal radial SNAPs, the spread phenomenon will remain unrecognized. This pitfall undermines the reliability of the test. Muscle Nerve 50: 186–192, 2014
The lateral antebrachial cutaneous nerve (LAC) is the terminal branch of the musculocutaneous nerve. Antidromic sensory nerve conduction study (SCS) of the LAC nerve is widely employed for diagnosis of plexopathy or musculocutaneous nerve palsy.1–3 Several studies have addressed its normal values.1,4–8 However, some of them reported rather large intersubject and interside variations in the amplitude of the sensory nerve action potential (SNAP) of this nerve,8 which may limit the clinical utility of this test. We found a previously unreported pitfall in the antidromic SCS of the LAC nerve: the spread of stimulation to the radial nerve at the elbow level.9,10 For routine antidromic SCS of the LAC, the nerve is stimulated just lateral to the biceps brachii tendon, and the SNAP is recorded 12 cm distally.11 The radial nerve may run unexpectedly close to the stimulus point for the LAC.12 If the Abbreviations: EPL, extensor polllicis longus; LAC nerve, lateral antebrachial cutaneous nerve; SCS, sensory nerve conduction study; SNAP, sensory nerve action potential Key words: lateral antebrachial cutaneous nerve; pitfall; radial nerve; sensory nerve conduction study; spread phenomenon This study was supported by Grants-in-Aid for Scientific Research (19591011 and 23591285) from the Ministry of Education, Science, Sports and Culture of Japan, and by Health and Labour Sciences Research Grants for research on intractable diseases (Neuroimmunological Disease Research Committee) from the Ministry of Health, Labour and Welfare of Japan. Correspondence to: M. Sonoo; e-mail: [email protected] C 2013 Wiley Periodicals, Inc. V
Published online 24 November 2013 in Wiley Online Library (wileyonlinelibrary. com). DOI 10.1002/mus.24129
186
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stimulation spreads to the radial nerve, the SNAP of the superficial branch of the radial nerve, which also runs close to the LAC nerve at the recording point for the LAC,12 will contaminate its SNAP and will result in an erroneously enlarged potential. We investigated the frequency of this spread phenomenon among control subjects and evaluated its influence on the SCS of the LAC nerve. METHODS
Subjects consisted of 80 healthy volunteers (39 men and 41 women, aged 24–82 years). All subjects gave informed consent to participate, and the study was approved by the clinical ethics committee of the Teikyo University School of Medicine (approval number: 09-059). A square-wave pulse of 0.2-ms duration was given using surface stimulating electrodes. The SNAPs were recorded using a number of different types of electrodes, as explained later. The responses were amplified and filtered between 10 HZ and 5 kHZ (23 dB) using an electromyography machine (Neuropack 2000; Nihon Kohden Co.). The amplifier gain was set at 10–50 lV/division, depending on the size of the SNAPs, and the analysis time was set at 20 ms. Usually, 10–20 responses were averaged, and the onset latency and peak-topeak amplitude of the SNAP were measured. Both sides were examined for each subject. The forearm skin temperature was monitored and was maintained at 33 C throughout the examination. For antidromic SCS of the LAC nerve, stimulation was given at the elbow just lateral to the tendon of the biceps brachii muscle, and the LAC SNAP was recorded 12 cm distal to the stimulation over the forearm using a saddle-type electrode (Oxford Instruments Co.) with 20 3 7-mm bar electrodes separated by 19 mm from one another in the center. In addition, SNAPs of the superficial branch of the radial nerve were recorded distally using the following 2 derivations to judge whether stimulation of the LAC nerve spread to the radial nerve (Fig. 1). First, ring electrodes were placed around the thumb, the active electrode at the base and the reference electrode distally. Second, electroencephalographic disk electrodes were used; the active electrode was placed over the superficial radial nerve crossing over the tendon of the MUSCLE & NERVE
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FIGURE 1. Electrode placement. Stimulation of the LAC nerve was applied at the elbow, and the LAC SNAP was recorded 12 cm distally on the forearm (channel 1). The SNAPs of the superficial branch of the radial nerve were recorded distally around the thumb (channel 2) and on the tendon of the extensor pollicis longus muscle (channel 3). Stimulation of the LAC nerve may spread to the superficial branch of the radial nerve running nearby, and its SNAP may contaminate the recording in channel 1. Ch, channel; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
extensor pollicis longus (EPL), and the reference electrode was placed distally over the metacarpophalangeal joint of the index finger. Before performing antidromic SCS, the best recording point was determined by orthodromic SCS, just as is typically done for the medial antebrachial cutaneous nerve.13 First, the recording electrode was placed at the elbow, and stimulation was given on the forearm. The position of the stimulating electrode was moved minutely, and the point evoking the orthodromic SNAP with the lowest threshold was found. Very weak stimulation, usually 6 times the true LAC SNAP (7.3 lV at 2 mA). Pattern C: a 37-year-old man. Spread to the radial nerve started at the lowest intensity (0.8 mA), and both the forearm and radial SNAPs were saturated at 2.0 mA. EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
A and B. This SNAP solely attributable to the LAC nerve was defined as the “true SNAP.” The true SNAP for pattern A and the false SNAPs for patterns B and C would be taken to be the maximum LAC SNAPs when the radial SNAPs are not monitored. Therefore, these measurements were collectively termed the “apparent (LAC) SNAP.” The peak-to-peak amplitude values of the true and false SNAPs were recorded, as well as the current values of: (a) the maximum intensity for the LAC SNAP; (b) the threshold for radial spread; and (c) the maximum intensity for the radial SNAP. The interside difference of the SNAP amplitude, which has been used widely as the criterion to determine abnormality in SCSs,2,14 was evaluated for both the true and apparent SNAPs. For some subjects, additional experiments were performed to investigate the possibility of anatomical variation, especially for pattern C arms. Using similar recording electrodes, proximal stimulation of the radial or musculocutaneous nerve was also conducted. The radial nerve was stimulated in the arm at the spiral groove. The musculocutaneous 188
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nerve was stimulated distal to the axilla posteromedial to the biceps brachii muscle. The CMAP of the biceps brachii muscle was used as an index of musculocutaneous nerve stimulation. To confirm that the superficial radial SNAP was also recorded by the recording electrode for the LAC nerve, we conducted an additional experiment to stimulate the radial nerve distally over the EPL tendon in 4 arms (1 pattern A and 3 pattern B arms) of 4 control subjects. For these arms, the optimal stimulation site for the superficial radial nerve was also localized at the mid-forearm level and was compared with the optimal site for the LAC nerve. Thumb stimulation was also performed in 2 of these arms. For statistical analysis, SNAP amplitude values of different subject groups were compared using the 2-sample t-test. RESULTS
Patterns A, B, and C were observed in 87, 63, and 10 of the 160 arms examined, respectively. The amplitudes of true and false LAC SNAPs for MUSCLE & NERVE
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Table 1. SNAP amplitude for each pattern.
Pattern A True SNAP* Pattern B True SNAP* False SNAP† Pattern C False SNAP† All True SNAP Apparent SNAP‡
N
ppAmp (mV)[mean 6 SD (range)]
87
27.3 6 12.9 (7.9–74.0)
63 63
29.7 6 16.9 (5.4–98.0) 52.6 6 24.2 (7.2–152.5)
10
59.2 6 21.4 (31.9–96.8)
150 160
28.3 6 14.7 (5.4–98.0) 39.3 6 22.8 (7.2–152.5)
False/true ppAmp ratio 206 6 101% (105–674%)
LAC, lateral antebrachial cutaneous (nerve); ppAmp, peak-to-peak amplitude; SNAP, sensory nerve action potential. *True SNAP: pure LAC SNAP saturated without contamination by spread to the radial nerve. This was defined only for patterns A and B. †
False SNAP: SNAP saturated for both the LAC and radial nerves. This was defined only for patterns B and C.
‡
Apparent SNAP indicates the true SNAP for pattern A and false SNAPs for patterns B and C.
each pattern are summarized in Table 1. The amplitude of the false SNAP was 206 6 101% (range 105–674%) of the true SNAP for 63 pattern B arms; that is, the false SNAP may reach as much as 7 times the true SNAP. The stimulus intensity that achieved maximum stimulation of the LAC nerve was usually low, 4.7 6 1.7 mA (1.6–11.0 mA). Spread to the radial nerve started at 10.0 6 5.5 mA (0.8–26 mA), and at 10 mA for 63% of pattern B or C arms. The interside difference in true SNAPs was 26.8 6 18.1% (range 0.4–76.3%) and exceeded 50% in 8 of 71 subjects (11%) for whom it was definable (neither arm was pattern C). The interside difference of apparent SNAPs was 31.4 6 20.2% (0.4–86.0%) and exceeded 50% in 12 of 80 subjects (15%). The amplitudes of the true LAC SNAPs for each age and gender group are summarized in Table 2. Older subjects (60 years) had significantly lower amplitudes than young or middleaged subjects. Men had significantly higher amplitudes than women. However, the intersubject variation of the SNAP amplitude was rather large and far exceeded the effect of such intergroup variations; the true SNAP amplitude for all arms was 28.3 6 14.7 lV (range 5.4–98.0 lV). For 3 arms in 3 subjects with pattern C, proximal radial and musculocutaneous stimulations were investigated. In 1 arm (Fig. 3), both the forearm LAC SNAP and distal radial SNAPs were elicited by musculocutaneous nerve stimulation, whereas proximal radial nerve stimulation elicited neither response. In another pattern C arm (Fig. 4) and 1 arm each of patterns A and B, musculocutaneous nerve stimulation elicited the forearm LAC SNAP, whereas proximal radial nerve stimulation elicited the distal radial SNAPs as well as the SNAP at the forearm recording electrode for LAC, Pitfall in LAC Conduction
which actually must have been caused by spread of the radial SNAP. In the last pattern C arm, none of the musculocutaneous, radial, or median nerve stimulations of the arm elicited a response at the forearm “LAC” electrode that was comparable to that elicited after elbow stimulation. Supramaximal stimulation at the Erb point was not possible in this subject. In the additional experiment of orthodromic radial nerve stimulation, stimulation of the superficial radial nerve over the EPL tendon elicited sizable SNAPs over both the thumb and over the forearm recording site for the LAC in all 4 arms. Typical results in a pattern B arm are illustrated in Table 2. Amplitude of true LAC SNAP in each subject group. Subjects (N) Young (20–39 years) Men 17 Women 19 All 36 Middle-age (40–59 years) Men 11 Women 10 All 21 Aged (601 years) Men 11 Women 11 All 22 All ages Men 39 Women 40 All 79
Arms (N)
ppAmp [mean 6 SD (range)]
33 37 70
36.0 6 16.9 (9.1–74.0) 27.0 6 15.4 (9.0–98.0) 31.3 6 16.7 (9.0–98.0)
22 17 39
31.7 6 12.6 (10.3–57.7) 26.6 6 10.6 (13.2–49.7) 29.5 6 11.9 (10.3–57.7)
20 21 41
25.0 6 12.6 (7.9–43.1) 19.4 6 10.2 (5.4–45.8) 22.1 6 11.6 (5.4–45.8)*
75 75 150
31.8 6 15.2 (7.9–74.0) 24.8 6 13.4 (5.4–98.0)† 28.3 6 14.7 (5.4–98.0)
The intersubject variation of the SNAP amplitude is rather large and far exceeds intergroup variations. LAC, lateral antebrachial cutaneous (nerve); ppAmp, peak-to-peak amplitude; SNAP, sensory nerve action potential. *Older subjects had a significantly lower amplitude compared with young (P < 0.002) or middle-aged (P < 0.01) subjects. †
Men had a significantly higher amplitude than women (P < 0.005).
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FIGURE 3. Pattern C arm shows the lack of the superficial branch of the radial nerve (same subject as shown in Fig. 2 for pattern C). Both the forearm LAC SNAP and distal radial SNAPs were elicited by musculocutaneous nerve stimulation of the proximal arm. Proximal radial nerve stimulation elicited neither response. Bic, biceps brachii; CMAP, compound muscle action potential; EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
FIGURE 4. Pattern C arm, with no anomaly, of a 25-year-old woman. Elbow stimulation revealed that the weakest stimulation elicited both forearm and distal radial SNAPs (therefore, pattern C). Isolated stimulation of the LAC nerve was not possible despite extensive exploration of the appropriate stimulation site at the elbow. Musculocutaneous nerve stimulation elicited a forearm LAC SNAP (plus a small SNAP around the thumb), whereas proximal radial nerve stimulation elicited distal radial SNAPs as well as the SNAP in the forearm recording electrode for LAC, which must actually be spread of the radial SNAP. In this subject, no anomaly existed, and the spread was caused only by the close proximity of the 2 nerves. Bic, biceps brachii; CMAP, compound muscle action potential; EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential. 190
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FIGURE 5. Distal radial nerve stimulation in a 37-year-old woman. First, we determined the best recording site for the LAC nerve using orthodromic LAC recording, and the site that activated the superficial radial nerve with the lowest threshold by monitoring the distal radial SNAPs. The image represents the stage at which these localizations were completed. The radial nerve was 7 mm lateral to the LAC nerve (2 arrow heads). Then, the superficial radial nerve over the EPL tendon was stimulated, and the orthodromic forearm response and the antidromic thumb responses were recorded (lower left). Saturated stimulation of the radial nerve over the EPL tendon was achieved at a rather low intensity (5 mA). The electrode over the LAC nerve clearly recorded a sizable SNAP, which was only slightly smaller than that recorded over the best recording site for the radial nerve. The results of LAC stimulation at the elbow (lower middle), without (6 mA) and with (14 mA) spread to the radial nerve, are also shown. EPL, extensor pollicis longus; LAC, lateral antebrachial cutaneous (nerve); SNAP, sensory nerve action potential.
Figure 5. At the forearm level, the site that activated the radial nerve with the lowest threshold (determined by distal radial response over the thumb and the EPL tendon) was 4–9 mm lateral to the site that solely activated the LAC nerve with the lowest threshold (determined by the orthodromic LAC recording) for 4 arms. After distal radial nerve stimulation, the SNAP recorded over the LAC recording site at the forearm was only slightly smaller than that recorded over the radial recording site determined above (Fig. 5) for all arms. Thumb stimulation also elicited a radial nerve SNAP over the LAC recording site at the forearm (not shown). DISCUSSION
We have described a previously unreported pitfall of stimulus spread to the radial nerve during antidromic SCS of the LAC nerve. This pitfall would not be noticed without monitoring radial SNAPs distally. The spread phenomenon occurred in as many as 46% of the arms of control subjects, and in at least 1 arm of 59% of subjects. In 6% (10 of 160) of examined arms, the spread started before the LAC SNAP was maximized, and the maximum amplitude of the genuine LAC SNAP was unknown (pattern C). Pitfall in LAC Conduction
The maximum intensity required to achieve saturation of the genuine LAC SNAP was usually very low, 10 mA in 99% of arms (all but 1) and 5 mA in 75% of arms using a 0.2-ms duration. Therefore, if the LAC amplitude continued to increase over 10 mA, this was probably due to spread of stimulation to the radial nerve. However, this pitfall cannot be avoided by this strategy, because even spread to the radial nerve often started at 10 mA (63% of arms where the spread occurred). As shown by the distal radial nerve stimulation experiment, the superficial radial nerve runs close to the LAC nerve at the forearm level, and a radial SNAP will be recorded at the ordinary LAC recording site if the radial nerve is coactivated during LAC stimulation at the elbow. Without monitoring distal radial SNAPs, the SNAP measured at saturation for both the LAC and radial nerves would be assumed to be the “LAC SNAP” (false SNAP) for patterns B and C. The amplitude of this type of false SNAP may be almost 7 times the genuine LAC SNAP. The reported large intersubject variation1,6–8 and the large intrasubject right-to-left difference8 of the LAC SNAP amplitude may well be due to this pitfall. This study has revealed that both intersubject variation and intrasubject side differences were larger for the apparent SNAP MUSCLE & NERVE
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(genuine SNAP for pattern A and false SNAPs for patterns B and C) than for the genuine SNAP (measurable for patterns A and B). However, even the interside difference for genuine SNAPs exceeded 50% in 11% of subjects for whom the difference was measurable. The maximum side-toside difference was 76%. In this regard, the “50% rule” is not always applicable to the LAC nerve, and we should be careful in using it for evaluation of plexopathy.2,14 Pattern C may be due to anatomical variation of the paths of the radial and musculocutaneous nerves. This possibility was investigated in 3 arms showing pattern C. Absence of the superficial branch of the radial nerve and total replacement of the innervation to the dorsum of the thumb and index finger by the LAC nerve has been reported.15–17 One of the 3 pattern C arms in this series was found to have this variation (Fig. 3). Results in another pattern C arm indicated that the inability to carry out separate stimulations at the elbow was due to close proximity of the 2 nerves, as proximal stimulation elicited different responses from these 2 nerves, respectively, as expected (Fig. 4). The results for the last pattern C arm could not be explained. None of the radial, musculocutaneous, or median nerve stimulations at the arm level elicited a response comparable to that elicited after elbow stimulation. This may have been due to the general difficulty in applying stimulations in this muscular male subject. In any case, the relative contribution of the 2 causes of difficult separation, anatomical variation or simple proximity, needs further investigation.
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