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Keywords:

  • conventional nerve conduction study;
  • diabetes mellitus;
  • distal symmetrical sensory polyneuropathy;
  • motor nerve impairment;
  • single fiber conduction velocity

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

Introduction: In this study we investigated the clinical utility of single fiber conduction velocity (SF-CV) testing in the evaluation of motor nerve function in diabetic patients with signs and symptoms of symmetrical distal sensory polyneuropathy (DSP). SF-CV findings were compared with conventional nerve conduction studies (NCS). Methods: Twenty-eight consecutive type 2 diabetic patients with clinically diagnosed DSP were studied. Results: SF-CV testing of the tibial nerve was abnormal in 16 (57.1%) patients. Twelve patients with normal conventional motor NCS had abnormal findings by tibial SF-CV. SF-CV testing of the tibial nerve was significantly superior to all other motor NCS. Conclusions: SF-CV testing of the tibial nerve often demonstrates motor nerve impairment in diabetic patients with sensory DSP when conventional NCS are normal. Muscle Nerve 49: 84–89, 2014

Abbreviations
CMAP

compound muscle action potential

C-CV

conventional conduction velocity

CV

conduction velocity

DIP

distal interphalangeal

EMG

electromyography

DSP

distal symmetrical polyneuropathy

FPG

fasting plasma glucose

HbA1c

glycated hemoglobin

MP

medial plantar

NAP

nerve action potential

NCS

nerve conduction study

SFEMG

single fiber electromyography

SF-CV

single fiber conduction velocity

SF

superficial fibular

Distal symmetric polyneuropathy (DSP) is the most common neuropathy in patients with diabetes. Conventional nerve conduction studies (NCS) are the “gold standard” in evaluation of DSP.[1] The most commonly observed electrophysiological abnormality associated with DSP is axonal neuropathy predominantly affecting the most distal sensory nerves, which is characteristic of the “dying-back” mechanism of the disease.[2, 3] Other sensitive indices of DSP are decreases in sensory and motor nerve conduction velocity (CV) and abnormalities on autonomic testing.[1]

Early detection of motor nerve involvement in patients with DSP is important, because subtle motor nerve changes may lead to abnormalities of foot posture that contribute to foot ulceration and gait imbalance.[4] Unfortunately, conventional NCS do not assess optimally the overall conduction properties of a nerve.[5] The CV of a normal axon is proportional to its diameter, and conventional NCS record the fastest-conducting sensory and motor fibers. However, many pathological processes do not affect nerves uniformly, and nerve CV may lie within the normal range until fast-conducting fibers are affected.[6-8] A novel electrophysiological approach, the single fiber conduction velocity (SF-CV) study, assesses the CV of a small sample of axons.[7] The value of this method in assessing different neuropathic processes has been reported[7, 9]; however, there are no data regarding the clinical utility of the SF-CV test in individual diabetic patients with clinical signs and symptoms of sensory neuropathy. We assessed the clinical utility of SF-CV testing in evaluation of motor nerve involvement in a group of diabetic patients with sensory signs and symptoms of DSP and compared the SF-CV test results with conventional NCS and clinical and laboratory findings.

METHODS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

Participants

This study included 28 consecutive type 2 diabetic patients with clinically diagnosed DSP and 46 healthy age- and gender-matched controls who did not have sensory symptoms, a history of diseases that might cause polyneuropathy, or abnormalities on neurological examination. Patients from the diabetic outpatient clinic who presented with symmetrical pain and/or numbness in the toes, feet, or legs, as well as those with diminished or absent ankle tendon reflexes (with other deep tendon reflexes intact) or vibration impairment only in the toes were included. Glycated hemoglobin (HbA1c) and fasting plasma glucose (FPG) were measured in all participants.

Exclusion criteria were as follows: (1) motor weakness; (2) any disease other than diabetes that could cause peripheral neuropathy; (3) radiculopathy, mononeuropathy, or plexopathy; and (4) skin disorders in the hands or feet that would interfere with NCS. All patients underwent complete routine physical and neurological examinations. Fine touch was defined as normal if a 10-g monofilament was felt 9 of 10 times on the dorsum of the foot and hand. Vibration sense was defined as normal if perceived for at least 8 s on the hallux and 15 s on the distal interphalangeal joint of the hand when measured with a vibrating 128-Hz tuning fork.

Normative data for electrophysiological studies were obtained from the 46 healthy controls. The study protocol was in accordance with the Helsinki Declaration of Human Rights, and was approved by the local ethics committee; all patients and controls provided written informed consent.

Electrophysiological Investigation

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

Two investigators (G.S and C.S.) performed all of the electrophysiological studies and 1 investigator (K.U.) reviewed all the data offline. Those 3 investigators were blinded to patient and control groups.

Conventional Motor and Sensory NCS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

NCS were performed using an electromyography device (Medelec Synergy EMG; Oxford Instruments, Old Woking, Surrey, UK). Surface bar recording and bipolar surface recording electrodes (Teca Corp.) were used. All patients and controls underwent routine nerve conduction studies bilaterally of posterior tibial and common fibular motor nerves, sural and superficial fibular (SF) sensory nerves, and medial plantar (MP) mixed nerves in the lower extremities. In the upper extremities, motor and sensory branches of the median and ulnar nerves, and radial sensory nerves on the non-dominant side were studied. Except for MP NCS, sensory NCS were performed antidromically.[10-12]

Sural sensory NCS were performed by recording the sensory nerve action potential (NAP) posterior to the lateral malleolus. Stimulation was administered 140 mm proximally at the midcalf. For SF NAP, the active side of the bar recording electrode was placed at the level of the ankle at 1 fingerbreadth medial to the lateral malleolus, and the nerve was stimulated 12 cm proximal to the active recording electrode.[10] For MP mixed NCS, the medial sole was stimulated, and the NAP was recorded over the tibial nerve above and posterior to the medial malleolus at a distance of 140 mm.[13] The onset latency, velocity, and amplitude (baseline to negative peak) were measured for sensory NCS. Signal averaging of 5–10 responses was used.

Compound muscle action potential (CMAP) amplitude, distal latency, conventional CV (C-CV), and minimum F-wave latency (F-latency; i.e., the shortest latency to the onset of the first deflection from baseline) were calculated for motor NCS. For the F-waves, 20 stimuli were given at a frequency of 1/s. No facilitation was used. An F-wave was defined as an action potential with peak-to-peak amplitude of ≥40 μV.

Filter settings were 5 Hz to 10 kHz for motor studies and 20 Hz to 2 kHz for sensory studies. Skin temperature was maintained between 33° and 34°C. All measured parameters were considered normal or abnormal based on the 5th–95th percentile range for controls.

Single Fiber Conduction Study

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

SF-CV was studied at 2 recording sites using the 5-step method described by Padua et al.[7] A single fiber needle electrode was used to record the CV of individual motor units. Filters were set at 500 Hz and 10 kHz. Right tibial and ulnar motor nerves on the non-dominant side were studied. The tibial nerve was studied in the leg, recording from the abductor hallucis muscle with stimulation at the medial malleolus and popliteal fossa. The ulnar nerve was studied in the forearm, recording from the abductor digiti minimi muscle with stimulation at the wrist and below the elbow.

The SF needle was inserted into the muscle. To minimize movement of the needle due to muscle contraction, the wire of the needle was tightly affixed to the extremity with tape. As with the C-CV study procedure, supramaximal stimulation was administered percutaneously to the relevant nerve at distal and proximal sites. Initially, a potential was recorded via supramaximal stimulation of the nerve at the distal site. The criteria used for an adequate recording were as follows: sharp, spiky, and rapid rise time. Then, a second supramaximal stimulus was administered at the same distal site to verify that the needle position had not changed after the first stimulus. If the 2 potentials differed, the needle was repositioned, and the procedure was repeated. The same technique was used at the proximal site. For the fifth and last step, supramaximal stimulation was administered to the first distal site to ensure that the needle did not move and to show that the last potential from the distal site had the same shape, amplitude, and delay as obtained initially.

SF-CV was calculated at the onset, and sometimes at a well-defined peak of the response. We acquired 10 SF-CVs for each nerve, moving the single fiber electromyography (SFEMG) electrode randomly each time. According to the literature, 36 m/s is accepted as the lower limit CV value for the slowest alpha motor axons[9, 14-19]; therefore, any velocity <36 m/s obtained with the SF-CV method was considered abnormal.

SF-CV evaluation of the tibial and ulnar nerves was performed in the control group [7 men and 7 women, age (mean ± standard deviation) 54.67 ±  11.39 years]. The mean ± SD of SF-CV of the tibial nerve was 43.05 ± 3.03 m/s (range 39.2–50.6 m/s), with a lower limit of normal (i.e., mean − 2 SD) of 36.99 m/s. The mean ± SD of SF-CV of the ulnar nerve was 56 ± 2.68 m/s (range 54.1–67.9 m/s, lower limit of normal 50.64 m/s). There were no complications from electrophysiological testing.

Statistical Analysis

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

Clinical and electrophysiological measures were compared using the Student t-test, Mann–Whitney U-test, or chi-square test, as appropriate. Correlation analysis was performed using Pearson and Spearman rank correlation coefficients. P < 0.05 was considered significant, with a Bonferroni correction for multiple comparisons.

RESULTS

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

Clinical and Laboratory Findings

The age (mean ± SD) of patients was 55.36 ± 8.03 years (range 42–70 years) vs. 52.61 ± 8.35 years (range 33–70 years) in the control group (P = 0.168). The mean body mass index in the patient group (32.72 ± 6.47) was significantly higher than in the control group (28.22 ± 5.03) (P = 0.001). The mean HbA1c and FPG in the patient group were 6.82 ± 0.65% (range 5.6–9.08%) and 123.45 ± 23.87 mg/dl (range 82–164 mg/dl), respectively. The mean duration of diabetes mellitus was 102.07 ± 78.53 months (range 24–360 months). In all, 18 (64.2%) of the patients were taking insulin, 14 (50%) were receiving oral antidiabetic treatment, and 5 (17.8%) were taking both insulin and oral antidiabetic drugs. The mean duration of neuropathic symptoms at the time of evaluation was 44.14 ± 28.15 months (range 12–120 months). All patients noted symmetrical painful dysesthesias, including burning or lightning pain and/or numbness in the feet and lower legs. Twenty-six (92.8%) patients reported having numbness, 11 (39.2%) reported hyperalgesia, and 10 (35.7%) reported allodynia. Neurological examination showed that 23 (82.1%) patients had reduced light touch sensitivity, and 16 (57.1%) had reduced pinprick sensitivity and temperature loss. Vibration sensation was abnormal in 21 (75%) patients, and 3 (10.7%) had abnormal proprioception. Muscle stretch reflexes at the ankles were reduced in 14 (50%) patients and absent in 2 (7.1%).

Electrophysiological Findings

Conventional NCS

None of the controls had an electrophysiological value beyond the normal limits.

Except for the radial sensory nerve (P = 0.25), the mean sensory and mixed NAP amplitudes in the patient group were significantly lower than in the control group (Table 1). In addition, MP, SF, and sural nerve CV values were significantly lower in the patients. The mean tibial nerve CMAP amplitude was significantly lower in the patients than in the controls (P = 0.004). In addition, mean motor nerve CV values of all tested nerves in the patient group were significantly slowed when compared with controls (Table 2). The tibial nerve F-latency was significantly longer in the patient group.

Table 1. Comparison of sensory nerve conduction results in the control and patient groups
Sensory nerveParameterControlsaPatientsaPLL/UL of normal (5th or 95th percentile)
  1. Bold P-values are statistically significant. LL, lower limit (for amplitude and velocity); UL, upper limit (for latency parameters); MP, medial plantar; SF, superficial fibular.

  2. a

    Data expressed as mean ± SD.

MPAmplitude (µV)8.4 ± 3.62.1 ± 2.90.000014.5
Velocity (m/s)59.0 ± 7.455.1 ± 8.10.008646.7
SFAmplitude (µV)10.3 ± 4.75.1 ± 5.50.000015.3
Velocity (m/s)52.8 ± 7.349.0 ± 7.40.004740.2
SuralAmplitude (µV)17.0 ± 6.49.2 ± 6.60.000016.8
Velocity (m/s)52.2 ± 6.446.9 ± 6.30.0000142.9
MedianAmplitude (µV)29.7 ± 13.017.6 ± 10.10.000510
Velocity (m/s)57.0 ±5.754.6 ± 6.70.2550
UlnarAmplitude (µV)27.2 ± 13.016.5 ± 5.70.0003710
Velocity (m/s)54.5 ± 4.552.8 ± 4.40.1948
RadialAmplitude (µV)21.2 ± 7.418.3 ± 7.00.2511.6
Velocity (m/s)61.6 ± 5.959.9 ± 6.10.2351.5
Table 2. Comparison of motor nerve conduction results in the control and patient groups
Motor nerveParameterControlsaPatientsaPLL/UL of normal (5th or 95th percentile)
  1. Bold values are statistically significant. LL, lower limit (for amplitude and velocity); UL, upper limit (for latency parameters).

  2. a

    Data expressed as mean ± SD.

TibialDistal latency (ms)4.5 ± 0.74.3 ± 0.50.406
Amplitude (mV)7.7 ± 1.66.6 ± 2.50.0045.4
Velocity (m/s)45.3 ± 3.042.1 ± 3.40.000140.6
Minimum F-latency (ms)46.9 ± 4.254.7 ± 5.10.0000155.5
FibularDistal latency (ms)3.8 ± 0.64.7 ± 0.30.085
Amplitude (mV)4.3 ± 1.63.5 ± 1.60.062.1
Velocity (m/s)50.3 ± 5.244.5 ± 4.60.0000442.8
Minimum F-latency (ms)45.1 ± 4.547.3 ± 3.90.0754.7
MedianDistal latency (ms)3.1 ± 0.63.4 ± 0.30.0584.4
Amplitude (mV)8.5 ± 1.97.9 ± 1.20.176.2
Velocity (m/s)58.2 ± 3.755.1 ± 3.50.0450.7
Minimum F-latency (ms)24.9 ± 2.225.3 ± 3.10.0729
UlnarDistal latency (ms)2.4 ± 0.32.5 ± 0.40.1023
Amplitude (mV)9.8 ± 2.210.1 ± 3.00.936.6
Velocity (m/s)63.3 ± 7.455.4 ± 6.50.0000350.5
Minimum F-latency (ms)25.2 ± 2.526.3 ± 3.10.0930.1

In clinical practice, detection of abnormalities in individual patients is more valuable than group means. Among the 28 clinically diagnosed diabetic DSP patients, 23 (82.1%) had abnormal MP NAP amplitudes bilaterally. The second most frequent abnormality observed using routine NCS was low SF nerve amplitude [n = 19 (67.9%)]. On the other hand, among the patients with an obtainable NAP, 5 had abnormal MP nerve latency and amplitude. Abnormal SF nerve latency or velocity was found in 4 patients. Sural NAP amplitude and velocity values were abnormal in 13 (43%) patients bilaterally. Based on conventional motor NCS, the most commonly observed abnormality was prolonged F-latency of the tibial nerve [n = 9 (32%)]. The tibial nerve distal latency was prolonged in 7 (25%) patients. Tibial and fibular C-CVs were abnormal in 4 (14%) patients.

A highly significant correlation was detected between HbA1c levels and NAP amplitudes of MP and SF nerves (P < 0.001). In addition, MP and SF NAP amplitudes were inversely correlated with the duration of diabetes (P < 0.01).

Single Fiber Conduction Velocity Study

Tibial nerve SF-CV in the patients (37.7 ± 5.04 m/s, range 18.2–51.6 m/s) was significantly lower than in controls (P = 0.03). Tibial nerve SF-CV was abnormal in 16 (57.1%) patients (Table 3). Ulnar nerve SF-CV in the patients was 51.97 ± 5.96 m/s (range 34.1–63.2 m/s, lower limit of normal 40.05 m/s) and did not differ from controls. Only 1 (3.6%) patient had an abnormal ulnar nerve SF-CV value. In all patients with abnormal tibial nerve C-CV, the SF-CV value was also abnormal. Based on the tibial nerve SF-CV test, 12 of the diabetic patients who had been considered normal according to conventional motor NCS had abnormal findings. On the other hand, whereas ulnar nerve C-CV was abnormal in 5 patients, SF-CV test findings indicated abnormality in only 1 of them. In comparison with the other tested motor NCS, tibial nerve SF-CV was significantly superior to the other tests in detection of abnormality in diabetic patients (P < 0.05 for all comparisons).

Table 3. Electrophysiological characteristics of patients with abnormal tibial SF-CV results
Patient numberNumber of abnormal SF-CV sites out of the 10 sitesLowest SF-CV value (m/s)
  1. SF-CV, single fiber conduction velocity.

1335.4
2330.9
3333.9
41018.2
5233.6
6334.7
7927.8
8728.0
9431.3
10829.3
111027.6
12830.1
13134.9
14131.9
15335.2
16135.9

There were no significant correlations between tibial nerve SF-CV results and sensory and/or mixed NAP amplitudes (P > 0.05). However, there was a significant correlation between SF-CV and tibial nerve F-latency (P = 0.001). In addition, patients with abnormal SF-CV findings had higher HbA1c levels and a longer duration of diabetes (P = 0.001 and P = 0.03, respectively).

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES

In this study we aimed to investigate the utility of SF-CV testing in detecting motor nerve involvement in a group of diabetic patients with sensory signs and symptoms of DSP. We found that tibial nerve SF-CV testing detected motor nerve impairment in diabetic DSP patients with higher sensitivity than C-CV. Our results show that ≥50% of the patients with diabetic sensory DSP had subclinical motor nerve involvement that routine NCS could not detect. In addition, among all the electrophysiological tests, tibial nerve SF-CV testing was the third most sensitive in detecting abnormality in the patient group. Also, in comparison with other motor NCS parameters (i.e., amplitude, distal latency, C-CV, and minimum F-wave latency), tibial nerve SF-CV testing was the most sensitive in detecting abnormality in motor fibers. Our results show that SF-CV values correlate well with demographic features of diabetic patients. Patients with abnormal tibial SF-CV values had more prolonged exposure to diabetes, as evidenced in higher HbA1c levels and longer duration of diabetes. These factors are positively related to DSP.[20] Although the tibial nerve SF-CV test was sensitive in detecting motor nerve impairment in diabetic DSP patients, ulnar nerve SF-CV test was not. This finding may be related to the length-dependent nature of DSP in which upper extremity nerves are affected later than the lower extremity ones.

NCS of sensory nerves, predominantly distal ones, are expected to be more sensitive than those of motor nerves in detecting length-dependent polyneuropathy.[2, 3] In agreement with the studies mentioned above, our findings confirm that the MP NCS was more frequently abnormal than NCS of pure sensory nerves. Although the MP nerve is a mixed nerve, the main contribution to the response obtained is the sensory component.[21] The SP NAP amplitude was the second most sensitive electrophysiological abnormality for detecting neuropathy. Similar to the SF-CV abnormalities, patients with abnormal MP and SF NAP amplitudes had higher HbA1c levels and a longer duration of diabetes.

Among conventional motor NCS, tibial F-latency, mean tibial CMAP amplitude, and mean CV in all motor nerves of patients were significantly different from those of the control subjects. The clinical utility of F-latency for detection of diabetic DSP has been demonstrated previously.[22, 23] Although 3 motor NCS parameters showed significantly different results between our patients and control groups, in agreement with the aforementioned studies, we found that tibial F-latency was the only parameter that detected individual abnormality in the patients. In addition, there were significant correlations between F-latency, SF-CV values, and demographic findings in the patients. The SF-CV method defined significantly more patients with motor nerve impairment than assessment of F-latency.

A limitation of SF-CV is that it is an invasive and relatively time-consuming procedure; however, only a small number of the study participants (n = 3) reported discomfort different from what they experienced with conventional NCS, and no complications related to the SFEMG needle electrode were observed. We spent no more than 30–40 min studying both the tibial and ulnar nerves. Motor nerve impairment in DSP has been investigated with different invasive neurophysiological techniques (i.e., assessment of fiber density by the single fiber EMG technique or quantitative EMG), and our study expands this repertoire of techniques. It is known that the degree of motor CV slowing is correlated with the duration and severity of diabetic neuropathy.[24] Thus, additional research on the sensitivity of SF-CV in assessment of the severity of DSP could be useful. In addition, the SF-CV technique may be helpful for comparing neuropathic vs. non-neuropathic symptoms in diabetic patients or for evaluating patients with suspected neuropathy who have normal findings on conventional NCS.

In conclusion, these findings show that assessment of SF-CV in the tibial nerve is superior to conventional motor NCS for detecting motor nerve impairment in patients with early diabetic DSP. Although SF-CV testing has some limitations that could influence its use in routine daily practice, it may be a useful technique in clinical trials as a sensitive measure for assessment of motor nerves.

REFERENCES

  1. Top of page
  2. ABSTRACT
  3. METHODS
  4. Electrophysiological Investigation
  5. Conventional Motor and Sensory NCS
  6. Single Fiber Conduction Study
  7. Statistical Analysis
  8. RESULTS
  9. DISCUSSION
  10. REFERENCES
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