Electrophysiologic responses of human sural nerve to temperature.

Electrophysiologic Responses of Human Sural Nerve to Temperature The initial manifestation of a polyneuropathy is frequently related to malfunctions of sensory nerve fibers in the distal lower limbs. [1] The sural nerve, a pure sensory nerve, supplies the skin of the posterior calf and lateral side of the foot. [2] The neural conduction examination is one diagnostic test used to evaluate a patient for possible polyneuropathies involving the sural and other peripheral nerves. [1,3-5] The assessment of sural nerve evoked responses is an important part of a complete electroneuromyographic (ENMG) examination because the sural nerve is frequently involved in the early stages of peripheral neuropathy. [1,3-5]

Neural conduction studies can be affected by the intraneural temperature. [3-5] The control of limb temperature, therefore, is necessary for clinicians who perform neural conduction studies because changes in temperature may alter the results and consequently make the findings of the examination inaccurate. Henriksen studied the temperature effects from 12[degrees] to 40[degrees]C on the motor conduction of human nerves. [6] He found that between 29[degrees] and 38[degrees]C the motor conduction velocity decreased 2.4 m/sec for each 1[degree]C decrease in temperature. Similar decreases in neural conduction as a function of a 1[degree]C decrease in limb temperature were reported by Buchthal and Rosenfalck (2.0 m/sec), [7] McLeod (2.6 m/sec), [8] de Jesus et al (2.1 m/sec), [9] Ludin and Beyeler (1.51 m/sec), [10] and Bolton et al (2.1 m/sec). [11]

No studies exist that evaluate the effect of intraneural temperature on the conduction of the sural nerve. Effects of temperature variation might affect conduction of the sural nerve and could be misinterpreted by the clinical electroneuromyographer as evidence of peripheral nerve pathology. The purpose of this study was to assess the conduction, specifically the latency and amplitude of the sensory nerve action potential (SNAP), of the sural nerve as a function of intraneural temperature. The null hypothesis for this study was that a change in intraneural temperature will not affect the conduction of the sural nerve. Conversely, the directional hypothesis was that if the intraneural temperature decreases (limb is cooled), the neural conduction (ie, the distal sensory latency [DSL]) will become prolonged, and if the intraneural temperature increases (limb is warmed), the DSL will become shortened. For clinicians performing neural conduction studies, the control of limb temperature is necessary to provide accurate and consistent results.

Method

Procedure and Instrumentation

Twenty-two volunteer subjects (13 male, 9 female) participated in the present study. The age of the subjects ranged from 20 to 34 years (X = 26.3 years). The subjects were clinically screened (history and physical examination) for neuropathies, lower extremity nerve injuries, and other associated medical problems that would affect the sensory conduction of the sural nerve. The physical examination consisted of muscle, sensory, and reflex (muscle stretch reflex) testing of both lower extremities. All subjects were informed of the experimental protocol and risks, and each subject gave written consent before participating in the study. The study was approved by the Human Investigation Committee (University of Kentucky Medical Center).

The temperature of the room was kept constant at 23[degrees]C. The sural nerves in both limbs of each subject were located in the following manner. The subject was positioned prone on the treatment table with a pillow under both lower limbs below the knees. The skin 2 cm distal to the lateral malleolus was cleaned with alcohol swabs and abraded with fine sandpaper. The negative recording disk electrode (4 mm diameter, steel) was placed on the skin 2 cm distal to the lateral malleolus, and the positive disk electrode was located 2 cm distal to the negative recording electrode. The recording electrodes were placed parallel to the sole of the foot. The ground electrode was placed on the dorsum of the foot. The electrodes were coated with conduction medium (*1) and secured in place with plastic tape.

After the recording electrodes had been secured, a point on the lateral posterior calf 140 mm proximal from the center of the negative electrode was located (Fig. 1). This skin area was cleaned with alcohol swabs and abraded with fine sandpaper. A cathode stimulating electrode was then placed exactly 140 mm from the negative recording electrode (positive electrode proximally toward knee), and the sural nerve was stimulated via a DISA 15E06 stimulator (*2) and a TECA RM 564 oscilloscope and amplifiers. (*3) The stimulus was a monophasic pulse of 0.1 msec duration, delivered once per second. The bandwidth of the amplifier was 16 Hz to 1.6 kHz. The evoked SNAP was then recorded (Fig. 2). The DSL of the SNAP was measured from the stimulus artifact to the peak of the SNAP. The amplitude was measured from peak to peak of the recorded SNAP. After completing the pretreatment recordings, the position of cathode stimulation and negative and positive recording electrode placements were marked with indelible pen and the electrodes were removed. The identical procedure was performed on both right and left legs.

The subject than sat upright on the treatment table and submersed both feet and legs (below the knee) into ice water (4[degrees]-6[degrees]C). The subject underwent the cooling procedure for a maximum period of five minutes or to tolerance. Immediately following the cooling procedure, the patient resumed the prone position on the treatment table and the negative and positive recording and ground electrodes were reattached over the marked points. A sterile, 24-gauge YSI Model 524 needle thermistor probe (*4) was inserted subcutaneously 2 cm into the subject's leg within 1 cm of the stimulation site (cathode) near the sural nerve (Fig. 1). The thermistor needle probe was connected in series with a YSI scanning telethermometer, (*4) which was accurate to [+ or -] 0.05[degree]C.

Temperature and SNAP latency and amplitude measurements were recorded from both legs. Subsequent (posttreatment) SNAP latency and amplitude measurements were taken at 1[degree]C increments in the subcutaneous tissue. After limb temperature returned to 36[degrees]C, the subject's legs were exposed to infrared heat. Assessment of SNAP latency and amplitude was continued at 1[degree]C intervals to a maximum subcutaneous temperature of 40[degrees]C, unless the subject experienced discomfort at a lower temperature.

Data Analysis

Descriptive statistics were calculated for the sural evoked SNAP latencies and amplitudes at each individual temperature. An analysis of covariance (ANCOVA) was used to elevate for the evoked SNAP latencies and amplitudes to determine the effect of gender and leg (right and left) on these variables at each individual temperature level. Regression analysis was then used on pooled data to determine the effect of temperature on sural SNAP latency and amplitude. Statistical significance was determined at the .05 level.

Results

Latency

Descriptive statistics for sural evoked SNAP latencies at each temperature level were calculated and are presented in Table 1. An ANCOVA was performed for mean sural SNAP latency as a function of leg (right or left (Tab. 2, Fig. 3) and gender (Tab. 3, Fig. 4). This analysis did not demonstrate an effect of leg or gender on sural SNAP latency at each individual temperature. We therefore pooled the SNAP latency data and plotted a regression equation (Fig. 5). The graph of the mean pooled SNAP latencies revealed an inverse relationship between the DSL of the sural nerve and temperature (ie, lower temperatures evoked prolonged latencies, and higher temperatures evoked faster latencies). The regression equation is as follows:

Latency = 8.48 - 0.12 (Temperature)

where the coefficient of determination is 73. Because the temperature increased from 23[degrees] to 40[degrees]C, the mean difference of the sural SNAP latency per degree of temperature change was calculated as 0.1 m/sec for each 1[degree]C increase.

Amplitude

Descriptive statistics for sural SNAP amplitudes at each temperature level were calculated and are presented in Tab. 4. An ANCOVA was performed for sural SNAP amplitude as a function of leg (right or left) (Tab. 5, Fig. 6) and gender (Tab. 6, Fig. 7). This analysis did not demonstrate an effect of gender on sural SNAP amplitude at each individual temperature level. Although the statistical analysis did reveal a significant difference (p < .0001) attributable to the effect of the right and left legs (Tab. 5), we did not consider this difference to be clinically significant. We therefore pooled the sural SNAP amplitude data and plotted a regression equation (Fig. 8). The graph of the mean combined sural SNAP amplitudes revealed a direct relationship between the mean SNAP amplitude of the sural nerve and temperature (ie, lower temperatures evoked lower amplitudes, and higher temperatures evoked higher amplitudes). The regression equation is as follows:

Amplitude = 1.18 + 0.44 (Temperature) (2)

where the coefficient of determination is 26. Because the temperature increased from 23[degrees] to 40[degrees]C, the mean difference of the sural SNAP amplitude per degree of temperature change was calculated as 0.3 [mu]V for each 1[degrees]C increase.

Discussion

An inverse relationship was observed between the DSL of the sural SNAP and the temperature of the leg. Similar findings have been reported by other investigators. [3-11] A possible explanation for this increase in latency of the SNAP (decreased neural conduction) with decreased temperature is that sodium permeability of nerve axons may be less during excitation, resulting in a slower sodium influx and an increased latency (slowed neural conduction). Thus, the null hypothesis for this study that a change in intraneural temperature will not affect the conduction of the sural nerve was rejected in favor of the directional hypothesis.

A direct relationship was observed between the distal sensory amplitude of sural SNAP and the temperature of the leg. Ludin and Beyeler have reported that between 22[degrees] and 26[degrees]C the amplitude of SNAPs decreased with lowering temperatures of the limb. [10] Oh [4] and Ludin and Beyeler [10] attributed an increase in SNAP amplitude with a concomitant increase in limb temperature to a smaller temporal dispersion of the SNAPs for different fibers and to a sequential shortening of the SNAP spike. As temporal dispersion diminishes with an increase in limb temperature, the SNAP amplitude increases. [4,10] Bolton et al, however, found that between limb temperatures of 21[degrees] to 31[degrees]C, the amplitude of the SNAP showed a progressive linear increase with decreasing temperature. [11] This increase in SNAP amplitude with decreasing temperatures may be explained by a decrease in temporal dispersion rather than a real increase in height (amplitude) of the SNAP. [4,10] It appears that limb temperature indeed has an effect on amplitude of the SNAP, and limb temperature must be monitored and controlled during neural conduction testing. [4] Further research in the area of limb temperature effects on the amplitude of the SNAP is warranted.

No significant difference in the mean SNAP latency or amplitude was detected between the sural nerves of left and right legs. LaFratta and Smith found no significant differences in motoneuron conduction of right and left ulnar nerves in male subjects. [12]. Although a higher nerve conduction velocity was measured on the dominant than on the nondominant side, the actual numercial differences were not significant. LaFratta and Smith, however, found that gender was a variant in neural conduction testing. [12] They reported a faster conduction of the median nerve in female subjects than in male subjects. In the present study, no significant difference in conduction of the sural nerve's SNAP was detected between male and female subjects. Other studies describing differences in nerve conduction as a function of gender have not been reported; consequently, ENMG clinics regard male and female subjects' conduction values as equal.

We suggest that the temperature of the lower limbs must be calculated whenever sensorineural conduction of the lower limbs is performed. If the temperature of the lower leg and foot is suspected to be reduced, as frequently occurs in the fall and winter months for outpatients, the latency of the evoked SNAP may be prolonged. A prolonged latency caused by decreased temperature of the leg may preclude an accurate measurement of the DSL. Thus, clinicians must account for the temperature of the patient's lower limbs when measuring neural conduction velocity. The lower limbs could be warmed to normal temperature by moist heat packs, infrared radiation, whirlpool, or other conventional methods. [3] Such procedures, however, are lengthy and often inconvenient in the clinic.

Alternatively, the DSL of the sural nerve could be determined, followed by recording skin temperature of the leg. After determining the skin temperature of the leg near the sural nerve, obtained neural latencies could be compared with temperature conversion charts previously reported in the literature by ENMG laboratories, [9,13] De Jesus et al [9] and Geerlings and Mechelse [13] indicated the need to account for temperature when neural conduction velocity is measured. These researchers indicated that in clinical settings, it is too time-consuming to warm an extremity with warm water or infrared radiation and proposed that skin temperature be used to adjust neural conduction values. All of these researchers used skin temperatures to adjust the neural conduction values; however, Geerlings and Mechelse also found similar neural conduction values using muscle temperatures. [13]

Conclusion

The present investigation revealed that the sural nerve can be used effectively and efficiently to evaluate sensorineural conduction. Temperature of the lower leg and foot, however, must be calculated whenever sensorineural conduction of the lower limbs is performed. Temperature has a profound inverse effect on SNAP latency and must be accounted for during clinical electrophysiological examinations. Conversely, temperature has a direct effect on SNAP amplitude and must also be considered during ENMG examinations. If the temperature of the lower leg or foot is found to be decreased, either the extremity could be warmed before measuring the SNAP latency and amplitude or a chart using temperature to normalize SNAP latency and amplitude could be used.

Neither the effects of leg (right or left) nor gender (male or female) were found to be significant factors in determining sural SNAP latency and amplitude. Neural conduction charts of normal values currently used in ENMG clinics without regard for leg or gender, therefore, are correctly being used.

Acknowledgment

We thank Nick Fusco, Information Management Division, US Army Academy of Health Sciences, for his assistance in preparing Figure 1.

(*1) Aquasonic [R] 100, Parker Laboratories Inc, 307 Washington St, Orange, NJ 07050.

(*2) DISA Electronics, Franklin Lakes, NJ 07417.

(*3) TECA Corp, 3 Campus Dr, Pleasantville, NY 10570.

(*4) Yellow Springs Instrument Co, PO Box 279, Yellow Springs, OH 45387.

References

[1] Ashworth B, Saunders M: Management of Neurological Disorders. Boston, MA, Butterworth Publishers, 1985, p 253

[2] Goss CM: Gray's Anatomy. New York, NY, Lea & Febiger, 1968, p 1003

[3] Kimura J: Electrodiagnosis in Diseases of Nerve and Muscle: Principles and Practice. Philadelphia, PA, F A Davis Co, 1986

[4] Oh SJ: Clinical Electromyography and Nerve Conduction Studies. Baltimore, MD, University Park Press, 1984

[5] Johnson EW: Practical Electromyography. Baltimore, MD, Williams & Wilkins, 1988

[6] Henriksen JD: Conduction Velocity of Motor Nerves in Normal Subjects and Patients with Neuromuscular Disorders. Master's Thesis. Minneapolis, MN, University of Minnesota, 1956

[7] Buchthal F, Rosenfalck A: Evoked action potentials and conduction velocity in human sensory nerves. Brain Res 3:1-122, 1966

[8] McLeod JG: Digital nerve conduction in the carpal tunnel syndrome after mechanical stimulation of the finger. J Neurol Neurosurg Psychiatry 29:12-22, 1966

[9] de Jesus PV, Hausmanowa-Petrusewicz I, Baschi RL: The effect of cold on nerve conduction of human slow and fast nerve fibers. Neurology 23:1182-1189, 1973

[10] Ludin HP, Beyeler F: Temperature dependence of normal sensory nerve action potentials. J Neurol 216:173-180, 1977

[11] Bolton CF, Sawa GM, Carter K: The effects of temperature on human compound action potentials. J. Neurol Neurosurg Psychiatry 44:407-413, 1981

[12] Lafratta CW, Smith OH: A study of the relationship of motor nerve conduction velocity the adult to age, sex and handedness. Arch Phys Med Rehabit 45:407-412, 1964

[13] Geerlings AHC, Mechelse K: Temperature and nerve conduction velocity: Some practical problems. Electromyogr Clin Neurophysiol 25:253-260, 1985

D Greathouse, PhD, PT, is Director, US Army-Baylor University Graduate Program in Physical Therapy, US Army Academy of Health Sciences, and Associate Director, Electrodiagnostic Laboratory, Neurology Service, Brooke Army Medical Center, Fort Sam Houston, TX 78234-6100 (USA). At the time of the study, he was a doctoral candidate, Department of Anatomy, University of Kentucky, Lexington, KY 40536.

D Currier, PhD, PT, is Professor and Chairman, Department of Physical Therapy, University of Kentucky Medical Center, Annex 1, Lexington, KY 40536-0079.

B Joseph, MD, is a practicing neurologist, Encinitas, CA 92024. At the time of this study, he was Assistant Professor of Neurology and Director of Clinical Electrophysiology, University of Kentucky Medical Center.

R Shippee, PhD, is Assistant Professor, US Army-Baylor University Graduate Program in Physical Therapy, US Army Academy of Health Sciences.

D Matulionis, PhD, is Associate Professor, Department of Anatomy, University of Kentucky.

The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the US Department of the Army or the US Department of Defense.