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A new technique for dorsal sural nerve conduction study with surface strip electrodes
Accepted Manuscript A new technique for dorsal sural nerve conduction study with surface strip electrodes Shoji Hemmi, Katsumi Kurokawa, Taiji Nagai, Ryutaro Kushida, Toshio Okamoto, Tatsufumi Murakami, Yoshihide Sunada PII: DOI: Reference:
S1388-2457(17)30148-7 http://dx.doi.org/10.1016/j.clinph.2017.04.004 CLINPH 2008116
To appear in:
Clinical Neurophysiology
Received Date: Revised Date: Accepted Date:
1 November 2016 6 March 2017 2 April 2017
Please cite this article as: Hemmi, S., Kurokawa, K., Nagai, T., Kushida, R., Okamoto, T., Murakami, T., Sunada, Y., A new technique for dorsal sural nerve conduction study with surface strip electrodes, Clinical Neurophysiology (2017), doi: http://dx.doi.org/10.1016/j.clinph.2017.04.004
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
A new technique for dorsal sural nerve conduction study with surface strip electrodes
Shoji Hemmi, MD1, Katsumi Kurokawa, MD1, Taiji Nagai, MD1, Ryutaro Kushida, MD1, Toshio Okamoto, DMC2, Tatsufumi Murakami, MD1, and Yoshihide Sunada, MD1
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Department of Neurology, Kawasaki Medical School, Kurashiki, Japan
2
Central Laboratory, Kawasaki Medical School, Kurashiki, Japan
Correspondence to: Shoji Hemmi, MD Department of Neurology, Kawasaki Medical School 577 Matsushima, Kurashiki, Okayama, Japan Tel.: +81 86 462-1111 FAX: +81 86 464-1027 Email: [email protected]
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Abbreviations: CoV, coefficient of variation; IDCN, intermediate dorsal cutaneous nerve; LDN, length-dependent neuropathy; MDCN, medial dorsal cutaneous nerve; NCS, nerve conduction study; NCV, nerve conduction velocity; SD, standard deviation; SNAP, sensory nerve action potential; SSEs, surface strip electrodes.
Highlights 1. Our method with surface strip electrodes (SSEs) yielded larger SNAP amplitudes in the dorsal sural nerve (DSN) than did the conventional method. 2. All branches of the DSN could be stimulated at the same time by SSEs. 3. SSEs enable DSN sensory nerve action potentials to be obtained easily even in elderly people.
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Abstract
Objective: To obtain higher amplitude of dorsal sural sensory nerve action potentials (SNAPs), we used a new method for dorsal sural nerve conduction study with surface strip electrodes (SSEs).
Methods: Dorsal sural SNAPs were recorded orthodromically. The recording electrodes were placed behind the lateral malleolus. SSEs were attached to the laterodorsal aspect of the foot for stimulation of the dorsal sural nerve (DSN). We also used a conventional method with a standard bipolar stimulator and compared the findings.
Results: Dorsal sural SNAPs were recordable bilaterally from 49 healthy volunteers. Mean peak-to-peak amplitude for SNAPs was 12.9 ± 6.3 μV, and mean nerve conduction velocity was 44.8 ± 5.5 m/s. The mean amplitude of SNAPs obtained by our method was 118.6% higher than that of SNAPs obtained by the conventional method (12.9 μV vs. 5.9 μV;
P<0.001).
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Conclusions: The highest amplitude of dorsal sural SNAPs was constantly obtained by SSEs since SNAPs arising from whole digital branches of the DSN could be elicited by placement of SSEs.
Significance: When the DSN supplies more cutaneous branches to the lateral half of the foot, SSEs gives higher amplitude of dorsal sural SNAPs than that of the standard innervation type.
Keywords: anatomical variants, dorsal sural nerve, nerve conduction study, sensory nerve action potential, standard bipolar stimulator, surface strip electrodes.
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1. Introduction For recording sensory nerve action potentials (SNAPs) of the sural nerve, surface recording electrodes are placed behind the lateral malleolus, and a bipolar stimulator is placed on the lateral posterior aspect of the mid-calf (Oh, 2003). This antidromic method was accepted as a standard method for sural nerve conduction study (NCS) and has been used routinely for diagnosis of length-dependent neuropathy (LDN), but its diagnostic value is limited due to its more proximal location above the ankle. In LDN, sural NCS may show normal findings by the method for a “proximal segment”. Since the innervation of the feet is most commonly affected in LDN, a reliable sural NCS of a more distal location is needed for early detection. We therefore selected a method for a “distal segment” in this study. The dorsal sural nerve (DSN) is the terminal branch of the sural nerve innervating the lateral dorsal aspect of the foot (Oh, 2003). Although dorsal sural NCS is suitable for detecting LDN due to its more distal location (Dias and Carneiro, 2000; Killian and Foreman, 2001), the small amplitude evoked response has limited the routine use of dorsal sural NCS. According to previous reports, the SNAP amplitude of the DSN was 50% to 73%
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lower than that of the sural nerve by the method for a “proximal segment” (Dias and Carneiro, 2000; Killian and Foreman, 2001; Balci et al., 2005), and to make matters worse, dorsal sural SNAPs were frequently absent even in healthy subjects (Burke et al., 1974; Killian and Foreman, 2001). Oh et al. (2001) established an orthodromic method for dorsal sural NCS and reported that the mean peak-to-peak amplitude for SNAPs was 7.26 ± 6.2 μV. In Oh’s method, a bipolar stimulator was placed on the laterodorsal aspect of the foot for stimulation of the DSN. We hypothesized that the standard bipolar stimulator might have stimulated only a part of the cutaneous branches of the DSN, thus causing the small SNAP amplitude. To solve the problem, a comprehensive knowledge of the anatomical variations of the DSN is very important. The medial dorsal cutaneous nerve (MDCN) and the intermediate dorsal cutaneous nerve (IDCN) are distal branches of the superficial fibular sensory nerve. Our previous study showed that variant innervations were more frequent in the IDCN than in the MDCN due to the anatomical relationship of the IDCN with the DSN (Hemmi et al., 2017). In 93.5% of the feet, the IDCN was partially or totally absent and its place was taken by the DSN. A cadaveric dissection study showed that the IDCN was absent or did not
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innervate any toe in 35% of cases and that the DSN supplied cutaneous branches to the lateral half of the foot and toes instead of the IDCN in 40% of cases (Solomon et al., 2001). Due to the anomalous innervation of the DSN to the IDCN territory, it is thought that a far-reaching strip electrode is needed for obtaining higher dorsal sural SNAP amplitude. Therefore, in this study, we examined the usefulness of dorsal sural NCS with surface strip electrodes (SSEs), which are usually used as disposable digital ring electrodes. We also conducted conventional dorsal sural NCS using the standard bipolar stimulator method established by Oh et al. (2001) on the same nerves and compared the findings.
2. Methods 2.1. Subjects The study subjects were 49 healthy volunteers. Individuals with a previous history of lumbar laminectomy, foot trauma, peripheral neuropathy, diabetes mellitus, or alcoholism were excluded. All subjects signed an informed consent form prior to evaluation. The Ethics Committee of Kawasaki Medical School and Hospital approved this study.
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2.2. New technique, dorsal sural NCS with SSEs All NCSs were performed bilaterally with an electromyography machine (Neuropack MEB-2216; Nihon Kohden, Tokyo, Japan). The bandpass filter was set at 20 Hz - 2 KHz. Subjects lay in a lateral decubitus position with a relaxed foot position. Skin temperature was measured at the plantar surface and was maintained at ≥ 32 °C. The skin of the feet was cleaned with alcohol to decrease impedance. Dorsal sural SNAPs were recorded orthodromically (Fig. 1). Ag-AgCl cup electrodes were used for recording. The active recording electrode was placed at the ankle just behind the lateral malleolus, and the reference recording electrode was placed 3 cm proximal to it. For stimulation of the DSN, we used disposable ring electrodes (disposable pre-gelled, Ag-AgCl ring electrodes, contact area of 8 mm x 95 mm, Natus Neurology, USA) as SSEs. Since the SSEs were a little long, they were truncated to 65 mm before use. We attached the SSE as the stimulating cathode on the lateral dorsal aspect of the foot 10 cm distal to the active recording electrode. The stimulating anode was placed parallel to the stimulating cathode. A ground electrode was placed over the dorsum of the foot between the stimulating and recording electrodes. Stimuli were rectangular electrical pulses of 0.1 ms in duration
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delivered at 1 Hz. Supramaximal stimulation was assured by increasing the stimulus intensity by 25% to 30% beyond the intensity at which a SNAP increased continuously up to the maximum. The SNAPs were averaged at least 20 times until no further change in amplitude, latency, and duration occurred. To assure reproducibility, at least 2 recordings for each SNAP were made. When the conduction parameters were completely matched, the SNAPs were chosen for analysis. Conduction parameters, including onset latency, peak latency, peak-to-peak amplitude, maximum nerve conduction velocity (NCV), negative peak NCV, duration of SNAPs, and side-to-side difference in amplitude, were measured. The conduction parameters from the left and right sides were combined for analysis. Because of the significantly skewed distribution of conduction parameters, the means and standard deviations (SD) of log-transformed data were calculated and then converted back to original units to be used as limits of normal values (Robinson et al., 1991). The value of SNAP amplitude and NCV corresponding to the mean minus 2 SD was considered to be the lower limit of normal, and the latency and SNAP durations corresponding to the mean plus 2 SD were considered to be the upper limit of normal.
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2.3. Conventional technique, dorsal sural NCS with a standard bipolar stimulator We performed conventional dorsal sural NCS on the same nerves (Oh et al., 2001). Dorsal sural SNAPs were recorded orthodromically with surface electrodes. The active recording electrode was placed at the ankle just behind the lateral malleolus, and the reference recording electrode was placed 3 cm proximal to the active recording electrode. For stimulation of the dorsal sural nerve, the conventional bipolar stimulator was placed on the lateral dorsal aspect of the foot 10 cm distal to the active recording electrode.
2.4. Statistical analysis Statistical analysis using the Wilcoxon signed rank test was carried out to compare values obtained by the different methods (dorsal sural NCS with SSEs vs. dorsal sural NCS with a standard bipolar stimulator). We compared multiple different measures (6), and in the absence of a multivariate statistical analysis, P-values for significance were thus adjusted for the multiple testing and set at 0.008 (0.05/6). For descriptive statistics, mean, SD, and coefficient of variation (CoV) were calculated. Statistical analysis using Fisher’s
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exact test was carried out to compare the results for responses to the SSEs and standard bipolar stimulator in normal subjects over 60 years old. The two different tests were performed on the same subjects. P-values < 0.05 were considered statistically significant.
3. Results 3.1. Dorsal sural NCS with SSEs. Dorsal sural SNAPs could be obtained bilaterally from all healthy volunteers (26 men, 23 women) with a mean age of 39.3 ± 16.2 (range, 21-87) years. The amplitudes of SNAPs were 2.6 to 31.5 μV. The normal values are shown in Table 1. The side-to-side difference in amplitude was calculated as a percentage using the following formula: absolute difference in amplitude×100 / maximal amplitude (Therimadasamy A et al., 2012). The mean
side-to-side difference in amplitude was 23.6 ± 17.5% (range, 1.6-65.6%).
3.2. Dorsal sural NCS with a standard bipolar stimulator Among the same healthy volunteers, dorsal sural SNAPs were absent in four nerves (4.1%). The amplitudes of SNAPs were 0 to 20.4 μV. The normal values are shown in Table
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1. In three nerves (3.1%), SNAPs were obscure due to a small amplitude of less than 2.0 μV. All of the low SNAP amplitudes (< 2.0 μV) were from subjects over 60 years old (Table 2). The mean side-to-side difference in amplitude was 24.3 ± 18.2% (range, 0-62.4%).
3.3. Comparison of the two methods The amplitudes of SNAPs elicited with SSEs were always higher than those elicited with the standard bipolar stimulator. Typical SNAPs in the healthy volunteers are shown in Fig. 2. The mean amplitude of SNAPs elicited with SSEs was 118.6% higher than that of SNAPs elicited with a standard bipolar stimulator (12.9 μV vs. 5.9 μV). The difference in the amplitudes of SNAPs was statistically significant and varied widely from 16.9% to 324.3%. However, there was no statistically significant difference in onset latency, peak latency, maximum NCV, negative peak NCV, duration of SNAPs, or side-to-side difference in amplitude when the two methods were compared (Table 1). Stimulus strengths elicited with SSEs and those elicited with a standard bipolar stimulator were supramaximal stimulus. The stimulus strengths elicited with SSEs were always higher than those elicited with the standard bipolar stimulator (24.1 ± 4.0 mA vs. 13.9 ± 2.1 mA; P<0.001).
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4. Discussion This study demonstrated that our technique is a reliable method for measuring conduction of the DSN. The results obtained in normal subjects confirmed that our method using SSEs yielded larger SNAP amplitudes than did the conventional method using a standard bipolar stimulator. Our method using SSEs was particularly reliable in elderly people because all of the SNAPs in people over 60 years old were recordable steadily. In contrast to our method, SNAPs obtained by a standard bipolar stimulator had a low amplitude of less than 2.0 μV in more than half (58.3%) of the same elderly subjects. The difference in frequency of SNAPs with a low amplitude (< 2.0 μV) was statistically significant (P=0.005). In early studies, both antidromic and orthodromic techniques were used for dorsal sural NCS. For the antidromic technique, surface recording electrodes were placed over the lateral dorsal surface of the foot, and a standard bipolar stimulator was placed behind the lateral malleolus (Burke et al., 1974; Lee et al., 1992; Killian and Foreman, 2001; Oh et al., 2001). For the orthodromic technique, the recording site was used for stimulation, and the
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stimulation site was used to record the SNAP (Dias RJ and Carneiro, 2000; Oh et al., 2001). These methods were accepted as standard methods, but SNAPs elicited with a standard bipolar stimulator in both methods had a very small amplitude or were absent. For example, an antidromic technique established by Burke et al. (1974) revealed that the mean peak-to-peak amplitude of dorsal sural SNAPs was only 3.9 ± 2.0 µV even in a younger group between ages of 0 to 20 years and that dorsal sural SNAPs were absent in 7 cases (9%) among 79 normal controls. Since SNAP cannot be obtained in all normal people, the absence of SNAP does not always imply neuropathic abnormality. The demerit of a standard bipolar stimulator may limit the clinical utility of dorsal sural NCS. It would be useful to show the clinical utility of our method compared to the conventional “antidromic” method. However, we compared our method to the conventional “orthodromic” method because we wanted to show that there is an unreported pitfall in the conventional “orthodromic” method in that it cannot stimulate the whole sural nerve. In addition, it is easy to place the recording electrodes just over the sural nerve in the “orthodromic” method because the sural nerve is palpable at the recording point (behind the lateral malleolus) and is not running in a deeper position like the proximal segment.
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Our recent study has shown the clinical utility of orthodromic nerve conduction by using SSEs for evaluation of the whole plantar nerve (Hemmi et al., 2016). Since whole-nerve action potentials arising from a large number of terminal branches could be elicited at the same time by placement of SSEs, the highest amplitude was constantly obtained by our method, even in elderly people. That is the main reason why we attempted to use SSEs instead of the conventional bipolar stimulator to evaluate conduction of the DSN. Besides, we think that the DSN is superior to the plantar nerve in diagnosing LDN, because entrapment of the plantar nerve gives rise to tarsal tunnel syndrome, whereas entrapment of the sural nerve is a rare condition. In this study, the mean amplitude of dorsal sural SNAPs elicited with a standard bipolar stimulator was 54.3% lower than that of SNAPs elicited with SSEs. We assume that this is mainly due to the technical limitation. Because the tiny stainless steel tips of a standard bipolar stimulator could stimulate only a small territory of the DSN, dorsal sural SNAPs might have been evoked insufficiently even with supramaximal stimulation. For that reason, it is thought that wide-strip stimulation over the lateral dorsum of the foot is needed for obtaining true SNAPs. When the two methods were compared, the difference in
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SNAP amplitudes varied widely from 16.9% to 324.3%. This might be due to various anomalous innervations of the DSN to the IDCN territory. Our previous study (Hemmi et al., 2017) showed that "standard innervation type" (the IDCN territory being innervated by the IDCN alone) was in only 6.5% of cases and "sural only type" (the IDCN territory being taken by the DSN alone) was in 14.5% of cases. When the two groups were compared (standard innervation type vs. sural only type), a higher SNAP amplitude could be obtained in the "sural only type" by our method with SSEs (P=0.03) but not by the conventional method with a standard bipolar stimulator (P=0.76). The difference between SNAP amplitudes obtained by the two methods steadily increased in accordance with extension of the DSN territory. When using SSEs, the DSN and the IDCN may be stimulated at the same time due to extension of the electrical stimulation along the strip electrodes. However, we speculate that the SNAP of the IDCN is rarely contaminated because the IDCN runs separately at the recording point for the DSN. Although volume conduction from another nerve may occur when the nerve runs close to the recording point, the recording points for the DSN and the IDCN are at least 6 cm apart. To confirm that volume conduction from the IDCN is
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rare, we stimulated the fourth and fifth branches with a standard bipolar stimulator and recorded SNAPs along the course of the recording point from the IDCN to the DSN at 2-cm intervals (Fig. 3). In all cases of standard innervation type, the SNAP amplitudes were gradually reduced and finally absent behind the lateral malleolus. Typical SNAPs obtained in two cases are shown in Fig. 3. Besides, the SNAP amplitudes with SSEs increased steadily according to extension of the DSN territory. Furthermore, we did additional tests and tried to record the antidromic response using SSEs for recording the DSN as well as the IDCN (Fig 4). To confirm that spread from the IDCN is rare, we additionally stimulated the midpoint between the DSN and the IDCN. When the midpoint between the DSN and the IDCN was stimulated, antidromic responses were absent in all cases. The results indicate that spread from the IDCN is rare because the IDCN runs separately at the stimulating point for the DSN.
Based on the results, we are convinced that the dorsal
sural SNAP rarely increases due to spread from the SNAP of the IDCN. Our method with SSEs has a pitfall in a clinical setting. For side-to-side SNAP amplitude comparison, the general rule that allows for up to a 50% difference in amplitude was unacceptable. A side-to-side difference of more than 50% was found in 5 (10.2%) of the
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49 cases (50.0%, 50.4%, 58.4%, 61.2% and 65.6%, respectively). The cause is unknown, but one possible reason might be different anatomical variation of the branching pattern of the DSN. For judging amplitude abnormality, we believe that an absolute value method is more practical than a side-to-side comparison method. Because the electrical stimulation dispersed widely along the strip electrodes, SSEs always required a stronger stimulus for supramaximal stimulation than did the standard bipolar stimulator (24.1 mA vs. 13.9 mA). However, stimulation by SSEs caused less discomfort than did the standard bipolar stimulator in almost all of the subjects, and the requirement of greater stimulus strength is therefore not a major disadvantage in a clinical setting. In conclusion, the larger responses obtained by our method enable nerve action potentials to be obtained easily in healthy people, even in people over 60 years old, and enable evaluation of a larger number of nerve fibers of the DSN. The clinical utility of diagnostic tests depends on reliability. The method described in this paper fulfills that criterion. Next, we will perform further detailed investigation in order to confirm the effectiveness of our method for detecting LDN.
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Conflict of interest We confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. None of the authors have potential conflicts of interest or financial interest to be disclosed.
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References
Balci K, Karacayir S, Varol G, Utku U. Utility of dorsal sural nerve in early determination of diabetic polyneuropathy. J Peripher Nerv Syst 2005; 10: 342-3.
Burke D, Skuse NF, Lethlean AK. Sensory conduction of the sural nerve in polyneuropathy. J Neurol Neurosurg Psychiatry 1974; 37: 647-52.
Dias RJ, Carneiro AP. Electrophysiological study of the lateral dorsal cutaneous nerve: technical applicability and normal values. Arq Neuropsiquiatr 2000; 58: 257-61.
Hemmi S, Kurokawa K, Nagai T, Okamoto T, Murakami T, Sunada Y. Whole plantar nerve conduction study with disposable strip electrodes. Muscle Nerve 2016; 53: 209-213.
Hemmi S, Kurokawa K, Nagai T, Kushida R, Okamoto T, Murakami T, et al. Variations in the distal branches of the superficial fibular sensory nerve. Muscle Nerve 2017; 55: 74-6.
Killian JM, Foreman PJ. Clinical utility of dorsal sural nerve conduction studies. Muscle Nerve 2001; 24: 817-20.
Kosinski C. The course, mutual relations and distribution of the cutaneous nerves of the metazonal region of the leg and foot. J Anat 1926; 60: 274-97.
Lee HJ, Bach HJ, DeLisa JA. Lateral dorsal cutaneous branch of the sural nerve
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Standardization in nerve conduction study. Am J Phys Med Rehabil 1992; 71: 318-20.
Oh SJ, Demirci M, Dajani B, Melo AC, Claussen GC. Distal sensory nerve conduction of the superficial peroneal nerve: new method and its clinical application. Muscle Nerve 2001; 24: 689-94.
Oh SJ. Clinical electromyography. Nerve conduction studies, 3rd ed. Baltimore: Williams & Wilkins; 2003. p .66.
Robinson LR, Temkin NR, Fujimoto WY, Stolov WC. Effect of statistical methodology on normal limits in nerve conduction studies. Muscle Nerve 1991; 14: 1084-90.
Solomon LB, Ferris L, Tedman R, Henneberg M. Surgical anatomy of the sural and superficial fibular nerves with an emphasis on the approach to the lateral malleolus. J Anat 2001; 199: 717-23.
Therimadasamy A, Wilder-Smith EP, Lim AY, Yap YL, Yeo M, Naidu S, et al. Supraorbital nerve conduction study in normal subjects. Muscle Nerve 2012; 45: 603-4.
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Table 1. Normal values for dorsal sural NCS with SSEs and with a standard bipolar stimulator. Dorsal sural NCS with a standard bipolar stimulator
Dorsal sural NCS with SSEs n=98
SNAP amplitude (μV) Onset latency (ms) Peak latency (ms) Maximum SCV (m/s) Negative peak SCV (m/s) SNAP duration (ms) Side-to-side difference in amplitude (%)
Mean
SD
CoV
Normal limit
Mean
SD
CoV
Normal limit
P-value
12.9
6.3
0.48
4.2
5.9
3.2
0.54
1.7
P<0.001
2.3
0.3
0.13
2.9
2.3
0.3
0.13
3.0
P=0.31
2.9
0.3
0.1
3.5
2.9
0.4
0.14
3.7
P=0.82
44.8
5.5
0.12
34.8
45.0
6.7
0.15
33.4
P=0.54
34.9
3.4
0.1
28.5
35.4
4.5
0.13
27.3
P=0.43
2.0
0.3
0.15
2.6
1.8
0.3
0.17
2.4
P=0.009
23.6
17.5
0.74
24.3
18.2
0.75
P=0.98
CoV, coefficient of variation; NCS, nerve conduction study; SD, standard deviation; SNAP, sensory nerve action potential; SSEs, surface strip electrodes
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Table 2. Dorsal sural SNAPs from normal subjects over 60 years old. n=12
Dorsal sural NCS with SSEs
Dorsal sural NCS with a standard bipolar stimulator
Low amplitude < 2.0 μV
0 (0%)
7 (58.3%)
P=0.005
Absent SNAPs
0 (0%)
4 (33.3%)
P=0.093
P-value
NCS, nerve conduction study; SNAP, sensory nerve action potential; SSEs, surface strip electrodes
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Figure legends
Figure 1. Technique for dorsal sural NCS with SSEs.
Figure 2. Comparison of two methods (dorsal sural NCS with SSEs and with a standard bipolar stimulator) in 3 healthy volunteers.
(A) SNAPs obtained in a 24-year-old woman.
(B) SNAPs obtained in a 50-year-old man. (C) SNAPs obtained in a 67-year-old man. The upper SNAPs were obtained by dorsal sural NCS with SSEs, and the lower SNAPs were obtained by dorsal sural NCS with a standard bipolar stimulator in the same nerves. Two traces were superimposed after
averaging. “Amplitude” represents peak-to-peak
amplitudes (μV), and “NCV” represents maximum NCVs (m/s).
Figure 3. Technique for IDCN NCS with a standard bipolar stimulator. Typical SNAPs of the IDCN (fourth branch) recorded along the course of the recording point from the IDCN to the DCN. (bottom left corner) SNAPs obtained in a 32-year-old man, standard innervation type. (bottom right corner) SNAPs obtained in a 25-year-old man, standard innervation type. A: recording point for the IDCN, B: recording point from the IDCN at 2-cm intervals, C: recording point from the IDCN at 4-cm intervals, D: recording point for the DSN. The distal latencies were gradually prolonged along the course of the recording point from the IDCN to the DSN because the distance between the stimulating cathode and the active recording electrode was extended as it approached the recording point for the DSN.
Figure 4. Antidromic NCS with SSEs for recording the DSN and the IDCN. (bottom left corner) SANPs obtained in a 33-year-old man, standard innervation type. (bottom middle)
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SNAPs obtained in a 47-year-old man, dual innervation type. (bottom right corner) SNAPs obtained in a 47-year-old man, sural only type. A: stimulating point for the IDCN, B: midpoint between the IDCN and the DSN, C: stimulating point for the DSN.
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S1388-2457(17)30148-7 http://dx.doi.org/10.1016/j.clinph.2017.04.004 CLINPH 2008116
To appear in:
Clinical Neurophysiology
Received Date: Revised Date: Accepted Date:
1 November 2016 6 March 2017 2 April 2017
Please cite this article as: Hemmi, S., Kurokawa, K., Nagai, T., Kushida, R., Okamoto, T., Murakami, T., Sunada, Y., A new technique for dorsal sural nerve conduction study with surface strip electrodes, Clinical Neurophysiology (2017), doi: http://dx.doi.org/10.1016/j.clinph.2017.04.004
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1
A new technique for dorsal sural nerve conduction study with surface strip electrodes
Shoji Hemmi, MD1, Katsumi Kurokawa, MD1, Taiji Nagai, MD1, Ryutaro Kushida, MD1, Toshio Okamoto, DMC2, Tatsufumi Murakami, MD1, and Yoshihide Sunada, MD1
1
Department of Neurology, Kawasaki Medical School, Kurashiki, Japan
2
Central Laboratory, Kawasaki Medical School, Kurashiki, Japan
Correspondence to: Shoji Hemmi, MD Department of Neurology, Kawasaki Medical School 577 Matsushima, Kurashiki, Okayama, Japan Tel.: +81 86 462-1111 FAX: +81 86 464-1027 Email: [email protected]
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Abbreviations: CoV, coefficient of variation; IDCN, intermediate dorsal cutaneous nerve; LDN, length-dependent neuropathy; MDCN, medial dorsal cutaneous nerve; NCS, nerve conduction study; NCV, nerve conduction velocity; SD, standard deviation; SNAP, sensory nerve action potential; SSEs, surface strip electrodes.
Highlights 1. Our method with surface strip electrodes (SSEs) yielded larger SNAP amplitudes in the dorsal sural nerve (DSN) than did the conventional method. 2. All branches of the DSN could be stimulated at the same time by SSEs. 3. SSEs enable DSN sensory nerve action potentials to be obtained easily even in elderly people.
3
Abstract
Objective: To obtain higher amplitude of dorsal sural sensory nerve action potentials (SNAPs), we used a new method for dorsal sural nerve conduction study with surface strip electrodes (SSEs).
Methods: Dorsal sural SNAPs were recorded orthodromically. The recording electrodes were placed behind the lateral malleolus. SSEs were attached to the laterodorsal aspect of the foot for stimulation of the dorsal sural nerve (DSN). We also used a conventional method with a standard bipolar stimulator and compared the findings.
Results: Dorsal sural SNAPs were recordable bilaterally from 49 healthy volunteers. Mean peak-to-peak amplitude for SNAPs was 12.9 ± 6.3 μV, and mean nerve conduction velocity was 44.8 ± 5.5 m/s. The mean amplitude of SNAPs obtained by our method was 118.6% higher than that of SNAPs obtained by the conventional method (12.9 μV vs. 5.9 μV;
P<0.001).
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Conclusions: The highest amplitude of dorsal sural SNAPs was constantly obtained by SSEs since SNAPs arising from whole digital branches of the DSN could be elicited by placement of SSEs.
Significance: When the DSN supplies more cutaneous branches to the lateral half of the foot, SSEs gives higher amplitude of dorsal sural SNAPs than that of the standard innervation type.
Keywords: anatomical variants, dorsal sural nerve, nerve conduction study, sensory nerve action potential, standard bipolar stimulator, surface strip electrodes.
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1. Introduction For recording sensory nerve action potentials (SNAPs) of the sural nerve, surface recording electrodes are placed behind the lateral malleolus, and a bipolar stimulator is placed on the lateral posterior aspect of the mid-calf (Oh, 2003). This antidromic method was accepted as a standard method for sural nerve conduction study (NCS) and has been used routinely for diagnosis of length-dependent neuropathy (LDN), but its diagnostic value is limited due to its more proximal location above the ankle. In LDN, sural NCS may show normal findings by the method for a “proximal segment”. Since the innervation of the feet is most commonly affected in LDN, a reliable sural NCS of a more distal location is needed for early detection. We therefore selected a method for a “distal segment” in this study. The dorsal sural nerve (DSN) is the terminal branch of the sural nerve innervating the lateral dorsal aspect of the foot (Oh, 2003). Although dorsal sural NCS is suitable for detecting LDN due to its more distal location (Dias and Carneiro, 2000; Killian and Foreman, 2001), the small amplitude evoked response has limited the routine use of dorsal sural NCS. According to previous reports, the SNAP amplitude of the DSN was 50% to 73%
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lower than that of the sural nerve by the method for a “proximal segment” (Dias and Carneiro, 2000; Killian and Foreman, 2001; Balci et al., 2005), and to make matters worse, dorsal sural SNAPs were frequently absent even in healthy subjects (Burke et al., 1974; Killian and Foreman, 2001). Oh et al. (2001) established an orthodromic method for dorsal sural NCS and reported that the mean peak-to-peak amplitude for SNAPs was 7.26 ± 6.2 μV. In Oh’s method, a bipolar stimulator was placed on the laterodorsal aspect of the foot for stimulation of the DSN. We hypothesized that the standard bipolar stimulator might have stimulated only a part of the cutaneous branches of the DSN, thus causing the small SNAP amplitude. To solve the problem, a comprehensive knowledge of the anatomical variations of the DSN is very important. The medial dorsal cutaneous nerve (MDCN) and the intermediate dorsal cutaneous nerve (IDCN) are distal branches of the superficial fibular sensory nerve. Our previous study showed that variant innervations were more frequent in the IDCN than in the MDCN due to the anatomical relationship of the IDCN with the DSN (Hemmi et al., 2017). In 93.5% of the feet, the IDCN was partially or totally absent and its place was taken by the DSN. A cadaveric dissection study showed that the IDCN was absent or did not
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innervate any toe in 35% of cases and that the DSN supplied cutaneous branches to the lateral half of the foot and toes instead of the IDCN in 40% of cases (Solomon et al., 2001). Due to the anomalous innervation of the DSN to the IDCN territory, it is thought that a far-reaching strip electrode is needed for obtaining higher dorsal sural SNAP amplitude. Therefore, in this study, we examined the usefulness of dorsal sural NCS with surface strip electrodes (SSEs), which are usually used as disposable digital ring electrodes. We also conducted conventional dorsal sural NCS using the standard bipolar stimulator method established by Oh et al. (2001) on the same nerves and compared the findings.
2. Methods 2.1. Subjects The study subjects were 49 healthy volunteers. Individuals with a previous history of lumbar laminectomy, foot trauma, peripheral neuropathy, diabetes mellitus, or alcoholism were excluded. All subjects signed an informed consent form prior to evaluation. The Ethics Committee of Kawasaki Medical School and Hospital approved this study.
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2.2. New technique, dorsal sural NCS with SSEs All NCSs were performed bilaterally with an electromyography machine (Neuropack MEB-2216; Nihon Kohden, Tokyo, Japan). The bandpass filter was set at 20 Hz - 2 KHz. Subjects lay in a lateral decubitus position with a relaxed foot position. Skin temperature was measured at the plantar surface and was maintained at ≥ 32 °C. The skin of the feet was cleaned with alcohol to decrease impedance. Dorsal sural SNAPs were recorded orthodromically (Fig. 1). Ag-AgCl cup electrodes were used for recording. The active recording electrode was placed at the ankle just behind the lateral malleolus, and the reference recording electrode was placed 3 cm proximal to it. For stimulation of the DSN, we used disposable ring electrodes (disposable pre-gelled, Ag-AgCl ring electrodes, contact area of 8 mm x 95 mm, Natus Neurology, USA) as SSEs. Since the SSEs were a little long, they were truncated to 65 mm before use. We attached the SSE as the stimulating cathode on the lateral dorsal aspect of the foot 10 cm distal to the active recording electrode. The stimulating anode was placed parallel to the stimulating cathode. A ground electrode was placed over the dorsum of the foot between the stimulating and recording electrodes. Stimuli were rectangular electrical pulses of 0.1 ms in duration
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delivered at 1 Hz. Supramaximal stimulation was assured by increasing the stimulus intensity by 25% to 30% beyond the intensity at which a SNAP increased continuously up to the maximum. The SNAPs were averaged at least 20 times until no further change in amplitude, latency, and duration occurred. To assure reproducibility, at least 2 recordings for each SNAP were made. When the conduction parameters were completely matched, the SNAPs were chosen for analysis. Conduction parameters, including onset latency, peak latency, peak-to-peak amplitude, maximum nerve conduction velocity (NCV), negative peak NCV, duration of SNAPs, and side-to-side difference in amplitude, were measured. The conduction parameters from the left and right sides were combined for analysis. Because of the significantly skewed distribution of conduction parameters, the means and standard deviations (SD) of log-transformed data were calculated and then converted back to original units to be used as limits of normal values (Robinson et al., 1991). The value of SNAP amplitude and NCV corresponding to the mean minus 2 SD was considered to be the lower limit of normal, and the latency and SNAP durations corresponding to the mean plus 2 SD were considered to be the upper limit of normal.
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2.3. Conventional technique, dorsal sural NCS with a standard bipolar stimulator We performed conventional dorsal sural NCS on the same nerves (Oh et al., 2001). Dorsal sural SNAPs were recorded orthodromically with surface electrodes. The active recording electrode was placed at the ankle just behind the lateral malleolus, and the reference recording electrode was placed 3 cm proximal to the active recording electrode. For stimulation of the dorsal sural nerve, the conventional bipolar stimulator was placed on the lateral dorsal aspect of the foot 10 cm distal to the active recording electrode.
2.4. Statistical analysis Statistical analysis using the Wilcoxon signed rank test was carried out to compare values obtained by the different methods (dorsal sural NCS with SSEs vs. dorsal sural NCS with a standard bipolar stimulator). We compared multiple different measures (6), and in the absence of a multivariate statistical analysis, P-values for significance were thus adjusted for the multiple testing and set at 0.008 (0.05/6). For descriptive statistics, mean, SD, and coefficient of variation (CoV) were calculated. Statistical analysis using Fisher’s
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exact test was carried out to compare the results for responses to the SSEs and standard bipolar stimulator in normal subjects over 60 years old. The two different tests were performed on the same subjects. P-values < 0.05 were considered statistically significant.
3. Results 3.1. Dorsal sural NCS with SSEs. Dorsal sural SNAPs could be obtained bilaterally from all healthy volunteers (26 men, 23 women) with a mean age of 39.3 ± 16.2 (range, 21-87) years. The amplitudes of SNAPs were 2.6 to 31.5 μV. The normal values are shown in Table 1. The side-to-side difference in amplitude was calculated as a percentage using the following formula: absolute difference in amplitude×100 / maximal amplitude (Therimadasamy A et al., 2012). The mean
side-to-side difference in amplitude was 23.6 ± 17.5% (range, 1.6-65.6%).
3.2. Dorsal sural NCS with a standard bipolar stimulator Among the same healthy volunteers, dorsal sural SNAPs were absent in four nerves (4.1%). The amplitudes of SNAPs were 0 to 20.4 μV. The normal values are shown in Table
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1. In three nerves (3.1%), SNAPs were obscure due to a small amplitude of less than 2.0 μV. All of the low SNAP amplitudes (< 2.0 μV) were from subjects over 60 years old (Table 2). The mean side-to-side difference in amplitude was 24.3 ± 18.2% (range, 0-62.4%).
3.3. Comparison of the two methods The amplitudes of SNAPs elicited with SSEs were always higher than those elicited with the standard bipolar stimulator. Typical SNAPs in the healthy volunteers are shown in Fig. 2. The mean amplitude of SNAPs elicited with SSEs was 118.6% higher than that of SNAPs elicited with a standard bipolar stimulator (12.9 μV vs. 5.9 μV). The difference in the amplitudes of SNAPs was statistically significant and varied widely from 16.9% to 324.3%. However, there was no statistically significant difference in onset latency, peak latency, maximum NCV, negative peak NCV, duration of SNAPs, or side-to-side difference in amplitude when the two methods were compared (Table 1). Stimulus strengths elicited with SSEs and those elicited with a standard bipolar stimulator were supramaximal stimulus. The stimulus strengths elicited with SSEs were always higher than those elicited with the standard bipolar stimulator (24.1 ± 4.0 mA vs. 13.9 ± 2.1 mA; P<0.001).
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4. Discussion This study demonstrated that our technique is a reliable method for measuring conduction of the DSN. The results obtained in normal subjects confirmed that our method using SSEs yielded larger SNAP amplitudes than did the conventional method using a standard bipolar stimulator. Our method using SSEs was particularly reliable in elderly people because all of the SNAPs in people over 60 years old were recordable steadily. In contrast to our method, SNAPs obtained by a standard bipolar stimulator had a low amplitude of less than 2.0 μV in more than half (58.3%) of the same elderly subjects. The difference in frequency of SNAPs with a low amplitude (< 2.0 μV) was statistically significant (P=0.005). In early studies, both antidromic and orthodromic techniques were used for dorsal sural NCS. For the antidromic technique, surface recording electrodes were placed over the lateral dorsal surface of the foot, and a standard bipolar stimulator was placed behind the lateral malleolus (Burke et al., 1974; Lee et al., 1992; Killian and Foreman, 2001; Oh et al., 2001). For the orthodromic technique, the recording site was used for stimulation, and the
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stimulation site was used to record the SNAP (Dias RJ and Carneiro, 2000; Oh et al., 2001). These methods were accepted as standard methods, but SNAPs elicited with a standard bipolar stimulator in both methods had a very small amplitude or were absent. For example, an antidromic technique established by Burke et al. (1974) revealed that the mean peak-to-peak amplitude of dorsal sural SNAPs was only 3.9 ± 2.0 µV even in a younger group between ages of 0 to 20 years and that dorsal sural SNAPs were absent in 7 cases (9%) among 79 normal controls. Since SNAP cannot be obtained in all normal people, the absence of SNAP does not always imply neuropathic abnormality. The demerit of a standard bipolar stimulator may limit the clinical utility of dorsal sural NCS. It would be useful to show the clinical utility of our method compared to the conventional “antidromic” method. However, we compared our method to the conventional “orthodromic” method because we wanted to show that there is an unreported pitfall in the conventional “orthodromic” method in that it cannot stimulate the whole sural nerve. In addition, it is easy to place the recording electrodes just over the sural nerve in the “orthodromic” method because the sural nerve is palpable at the recording point (behind the lateral malleolus) and is not running in a deeper position like the proximal segment.
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Our recent study has shown the clinical utility of orthodromic nerve conduction by using SSEs for evaluation of the whole plantar nerve (Hemmi et al., 2016). Since whole-nerve action potentials arising from a large number of terminal branches could be elicited at the same time by placement of SSEs, the highest amplitude was constantly obtained by our method, even in elderly people. That is the main reason why we attempted to use SSEs instead of the conventional bipolar stimulator to evaluate conduction of the DSN. Besides, we think that the DSN is superior to the plantar nerve in diagnosing LDN, because entrapment of the plantar nerve gives rise to tarsal tunnel syndrome, whereas entrapment of the sural nerve is a rare condition. In this study, the mean amplitude of dorsal sural SNAPs elicited with a standard bipolar stimulator was 54.3% lower than that of SNAPs elicited with SSEs. We assume that this is mainly due to the technical limitation. Because the tiny stainless steel tips of a standard bipolar stimulator could stimulate only a small territory of the DSN, dorsal sural SNAPs might have been evoked insufficiently even with supramaximal stimulation. For that reason, it is thought that wide-strip stimulation over the lateral dorsum of the foot is needed for obtaining true SNAPs. When the two methods were compared, the difference in
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SNAP amplitudes varied widely from 16.9% to 324.3%. This might be due to various anomalous innervations of the DSN to the IDCN territory. Our previous study (Hemmi et al., 2017) showed that "standard innervation type" (the IDCN territory being innervated by the IDCN alone) was in only 6.5% of cases and "sural only type" (the IDCN territory being taken by the DSN alone) was in 14.5% of cases. When the two groups were compared (standard innervation type vs. sural only type), a higher SNAP amplitude could be obtained in the "sural only type" by our method with SSEs (P=0.03) but not by the conventional method with a standard bipolar stimulator (P=0.76). The difference between SNAP amplitudes obtained by the two methods steadily increased in accordance with extension of the DSN territory. When using SSEs, the DSN and the IDCN may be stimulated at the same time due to extension of the electrical stimulation along the strip electrodes. However, we speculate that the SNAP of the IDCN is rarely contaminated because the IDCN runs separately at the recording point for the DSN. Although volume conduction from another nerve may occur when the nerve runs close to the recording point, the recording points for the DSN and the IDCN are at least 6 cm apart. To confirm that volume conduction from the IDCN is
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rare, we stimulated the fourth and fifth branches with a standard bipolar stimulator and recorded SNAPs along the course of the recording point from the IDCN to the DSN at 2-cm intervals (Fig. 3). In all cases of standard innervation type, the SNAP amplitudes were gradually reduced and finally absent behind the lateral malleolus. Typical SNAPs obtained in two cases are shown in Fig. 3. Besides, the SNAP amplitudes with SSEs increased steadily according to extension of the DSN territory. Furthermore, we did additional tests and tried to record the antidromic response using SSEs for recording the DSN as well as the IDCN (Fig 4). To confirm that spread from the IDCN is rare, we additionally stimulated the midpoint between the DSN and the IDCN. When the midpoint between the DSN and the IDCN was stimulated, antidromic responses were absent in all cases. The results indicate that spread from the IDCN is rare because the IDCN runs separately at the stimulating point for the DSN.
Based on the results, we are convinced that the dorsal
sural SNAP rarely increases due to spread from the SNAP of the IDCN. Our method with SSEs has a pitfall in a clinical setting. For side-to-side SNAP amplitude comparison, the general rule that allows for up to a 50% difference in amplitude was unacceptable. A side-to-side difference of more than 50% was found in 5 (10.2%) of the
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49 cases (50.0%, 50.4%, 58.4%, 61.2% and 65.6%, respectively). The cause is unknown, but one possible reason might be different anatomical variation of the branching pattern of the DSN. For judging amplitude abnormality, we believe that an absolute value method is more practical than a side-to-side comparison method. Because the electrical stimulation dispersed widely along the strip electrodes, SSEs always required a stronger stimulus for supramaximal stimulation than did the standard bipolar stimulator (24.1 mA vs. 13.9 mA). However, stimulation by SSEs caused less discomfort than did the standard bipolar stimulator in almost all of the subjects, and the requirement of greater stimulus strength is therefore not a major disadvantage in a clinical setting. In conclusion, the larger responses obtained by our method enable nerve action potentials to be obtained easily in healthy people, even in people over 60 years old, and enable evaluation of a larger number of nerve fibers of the DSN. The clinical utility of diagnostic tests depends on reliability. The method described in this paper fulfills that criterion. Next, we will perform further detailed investigation in order to confirm the effectiveness of our method for detecting LDN.
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Conflict of interest We confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. None of the authors have potential conflicts of interest or financial interest to be disclosed.
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References
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Burke D, Skuse NF, Lethlean AK. Sensory conduction of the sural nerve in polyneuropathy. J Neurol Neurosurg Psychiatry 1974; 37: 647-52.
Dias RJ, Carneiro AP. Electrophysiological study of the lateral dorsal cutaneous nerve: technical applicability and normal values. Arq Neuropsiquiatr 2000; 58: 257-61.
Hemmi S, Kurokawa K, Nagai T, Okamoto T, Murakami T, Sunada Y. Whole plantar nerve conduction study with disposable strip electrodes. Muscle Nerve 2016; 53: 209-213.
Hemmi S, Kurokawa K, Nagai T, Kushida R, Okamoto T, Murakami T, et al. Variations in the distal branches of the superficial fibular sensory nerve. Muscle Nerve 2017; 55: 74-6.
Killian JM, Foreman PJ. Clinical utility of dorsal sural nerve conduction studies. Muscle Nerve 2001; 24: 817-20.
Kosinski C. The course, mutual relations and distribution of the cutaneous nerves of the metazonal region of the leg and foot. J Anat 1926; 60: 274-97.
Lee HJ, Bach HJ, DeLisa JA. Lateral dorsal cutaneous branch of the sural nerve
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Standardization in nerve conduction study. Am J Phys Med Rehabil 1992; 71: 318-20.
Oh SJ, Demirci M, Dajani B, Melo AC, Claussen GC. Distal sensory nerve conduction of the superficial peroneal nerve: new method and its clinical application. Muscle Nerve 2001; 24: 689-94.
Oh SJ. Clinical electromyography. Nerve conduction studies, 3rd ed. Baltimore: Williams & Wilkins; 2003. p .66.
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Solomon LB, Ferris L, Tedman R, Henneberg M. Surgical anatomy of the sural and superficial fibular nerves with an emphasis on the approach to the lateral malleolus. J Anat 2001; 199: 717-23.
Therimadasamy A, Wilder-Smith EP, Lim AY, Yap YL, Yeo M, Naidu S, et al. Supraorbital nerve conduction study in normal subjects. Muscle Nerve 2012; 45: 603-4.
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Table 1. Normal values for dorsal sural NCS with SSEs and with a standard bipolar stimulator. Dorsal sural NCS with a standard bipolar stimulator
Dorsal sural NCS with SSEs n=98
SNAP amplitude (μV) Onset latency (ms) Peak latency (ms) Maximum SCV (m/s) Negative peak SCV (m/s) SNAP duration (ms) Side-to-side difference in amplitude (%)
Mean
SD
CoV
Normal limit
Mean
SD
CoV
Normal limit
P-value
12.9
6.3
0.48
4.2
5.9
3.2
0.54
1.7
P<0.001
2.3
0.3
0.13
2.9
2.3
0.3
0.13
3.0
P=0.31
2.9
0.3
0.1
3.5
2.9
0.4
0.14
3.7
P=0.82
44.8
5.5
0.12
34.8
45.0
6.7
0.15
33.4
P=0.54
34.9
3.4
0.1
28.5
35.4
4.5
0.13
27.3
P=0.43
2.0
0.3
0.15
2.6
1.8
0.3
0.17
2.4
P=0.009
23.6
17.5
0.74
24.3
18.2
0.75
P=0.98
CoV, coefficient of variation; NCS, nerve conduction study; SD, standard deviation; SNAP, sensory nerve action potential; SSEs, surface strip electrodes
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Table 2. Dorsal sural SNAPs from normal subjects over 60 years old. n=12
Dorsal sural NCS with SSEs
Dorsal sural NCS with a standard bipolar stimulator
Low amplitude < 2.0 μV
0 (0%)
7 (58.3%)
P=0.005
Absent SNAPs
0 (0%)
4 (33.3%)
P=0.093
P-value
NCS, nerve conduction study; SNAP, sensory nerve action potential; SSEs, surface strip electrodes
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Figure legends
Figure 1. Technique for dorsal sural NCS with SSEs.
Figure 2. Comparison of two methods (dorsal sural NCS with SSEs and with a standard bipolar stimulator) in 3 healthy volunteers.
(A) SNAPs obtained in a 24-year-old woman.
(B) SNAPs obtained in a 50-year-old man. (C) SNAPs obtained in a 67-year-old man. The upper SNAPs were obtained by dorsal sural NCS with SSEs, and the lower SNAPs were obtained by dorsal sural NCS with a standard bipolar stimulator in the same nerves. Two traces were superimposed after
averaging. “Amplitude” represents peak-to-peak
amplitudes (μV), and “NCV” represents maximum NCVs (m/s).
Figure 3. Technique for IDCN NCS with a standard bipolar stimulator. Typical SNAPs of the IDCN (fourth branch) recorded along the course of the recording point from the IDCN to the DCN. (bottom left corner) SNAPs obtained in a 32-year-old man, standard innervation type. (bottom right corner) SNAPs obtained in a 25-year-old man, standard innervation type. A: recording point for the IDCN, B: recording point from the IDCN at 2-cm intervals, C: recording point from the IDCN at 4-cm intervals, D: recording point for the DSN. The distal latencies were gradually prolonged along the course of the recording point from the IDCN to the DSN because the distance between the stimulating cathode and the active recording electrode was extended as it approached the recording point for the DSN.
Figure 4. Antidromic NCS with SSEs for recording the DSN and the IDCN. (bottom left corner) SANPs obtained in a 33-year-old man, standard innervation type. (bottom middle)
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SNAPs obtained in a 47-year-old man, dual innervation type. (bottom right corner) SNAPs obtained in a 47-year-old man, sural only type. A: stimulating point for the IDCN, B: midpoint between the IDCN and the DSN, C: stimulating point for the DSN.
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