Acute thoracolumbar IVDH, which commonly affects chondrodystrophoid breeds of dogs such as Miniature Dachshunds,1 can be classified as grade 1 to 5 on the basis of the severity of observed neurologic dysfunction of the thoracolumbar portion of the spinal cord.2 Although this classification system largely focuses on clinical signs, including sensation, paresis, paralysis, and urinary incontinence, these signs reflect different pathophysiologic changes in the affected anatomic region, which is comprised of sensory and motor tracts and motor neurons. Consequently, the underlying pathophysiologic mechanisms of thoracolumbar IVDH are not explained by clinical grade alone.
An electrophysiologic examination, including somatosensory evoked potential analysis, motor and sensory nerve conduction analysis, and electromyography, can be performed to objectively assess nerve and muscle function. F-waves represent muscle action potentials resulting from excitation of the α-motor neurons after antidromic stimulation of a peripheral motor nerve.3 They reflect nervous conduction to and from the spinal cord as well as the activity of some motor neurons in the ventral horn of the spinal cord. F-wave parameters such as minimum and mean latency, conduction velocity, duration, persistence, and Famp:Mamp are used for the diagnosis of not only neuropathies but also spinal cord diseases in humans.4,5 Abnormalities in F-wave persistence (occurrence rate) and duration and in Famp:Mamp have been noted in humans with CNS disorders who have UMN signs.4,5 In dogs with experimentally induced myelopathy, high F-wave amplitude and persistence have been observed.6 To our knowledge, except in that experimental condition, F-wave examination has not been applied for evaluation of UMN disorders in dogs. Because UMN signs in the hind limbs are recognized to be caused by dysfunction of inhibitory tracts in the upper spinal cord, we considered that F-wave abnormalities of the tibial nerve would be observed in dogs with thoracolumbar IVDH.
The purpose of the study reported here was to determine values of F-wave parameters for tibial nerve stimulation of the interosseous muscles in clinically normal Miniature Dachshunds, a chondrodystrophoid breed, and compare parameter values between those dogs and Miniature Dachshunds with various clinical grades of thoracolumbar IVDH.
Materials and Methods
Animals
All dogs enrolled in the study were handled in compliance with Azabu University Animal Experiment Guidelines (April 2000). Dogs were considered eligible for enrollment after informed owner consent was obtained.
Clinically normal dogs—Ten Miniature Dachshunds (5 females and 5 males) that were scheduled to undergo gonadectomy were included in a clinically normal group. The dogs had no evidence of neurologic impairment or hematologic abnormalities as determined before surgery by conventional neurologic examination and hematologic testing. Mean ± SD (range) age and body weight were 1.8 ± 0.8 years (0.8 to 3 years) and 4.6 ± 0.5 kg (3.8 to 5.2 kg), respectively.
Dogs with IVDH—Forty-three Miniature Dachshunds (26 females and 17 males) with a diagnosis of thoracolumbar IVDH as established via conventional neurologic examination and CT with or without myelography or MRI were included in the IVDH group. Mean ± SD (range) age and body weight were 5.8 ± 1.5 years (4 to 8 years) and 5.3 ± 1.1 kg (3.2 to 8.3 kg), respectively. The location of disk herniation differed among the dogs (Appendix).
Subgroups were created on the basis of clinical grade of IVDH, which was assigned on the basis of severity of clinical signs in accordance with a previously reported classification system2 as follows: 1 = signs of pain only (n = 5); 2 = ataxia, conscious proprioception deficit, and paraparesis (10); 3 = paraplegia (8); 4 = paraplegia with urinary retention and overflow (10); and 5 = paraplegia, urinary retention and overflow, and loss of deep pain sensation (10).
Experimental procedures
F-wave examination—In preparation for F-wave examination, dogs received atropine sulfatea (0.04 mg/kg, SC). Anesthesia was subsequently induced with thiamylal sodiumb (8 to 10 mg/kg, IV) and was maintained throughout the examination with isoflurane.c The temperature of the examination room was maintained at 25°C. The examination was completed within 5 minutes after induction of anesthesia.
F-waves elicited by tibial nerve stimulation of the interosseous muscles were measured as reported previously.7 Briefly, the portion of 1 tibial nerve immediately proximal to the tarsal joint was stimulated with needle electrodes at a frequency of 1 Hz, duration of 0.2 milliseconds, and supramaximal intensity by use of a system for measurement and recording of evoked potentialsd; 32 responses of the interosseous muscles were recorded by surface disk electrodes. The intensity of the current required for maximal stimulation was defined as the current at which a stable action potential was maintained even when the current was increased. Supramaximal intensity was defined as a current 20% greater than the current at maximal stimulation. Tibial nerve length was measured as the distance from the stimulus point of the cathode electrode to the cranial border of the L5 spinous process (Figure 1).
Diagram of electrode placement and F-wave measurements for stimulation of the tibial nerve in dogs. The recording electrode was placed over the interosseous muscles of the hind limb, and the reference electrode was positioned on the dorsum of a digit. Stimulating electrodes were placed proximal to the tarsal joint. Length of the tibial nerve was measured as the distance from the stimulus point to the cranial border of the L5 spinous process.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Diagram of electrode placement and F-wave measurements for stimulation of the tibial nerve in dogs. The recording electrode was placed over the interosseous muscles of the hind limb, and the reference electrode was positioned on the dorsum of a digit. Stimulating electrodes were placed proximal to the tarsal joint. Length of the tibial nerve was measured as the distance from the stimulus point to the cranial border of the L5 spinous process.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Diagram of electrode placement and F-wave measurements for stimulation of the tibial nerve in dogs. The recording electrode was placed over the interosseous muscles of the hind limb, and the reference electrode was positioned on the dorsum of a digit. Stimulating electrodes were placed proximal to the tarsal joint. Length of the tibial nerve was measured as the distance from the stimulus point to the cranial border of the L5 spinous process.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
F-wave analysis—The shortest and mean (of the 32 responses) latency, FWCV, mean duration, persistence, and Famp:Mamp were determined by use of computer softwaree linked to a recording system.d Latencies were measured from the stimulus artifact to the beginning of the F-waves as negative or positive. The FWCV was calculated by use of the following equation7:
where M response latency represents the latency of the first compound muscle action potential of 32 M responses.
Mean duration was calculated as the mean of the 32 F-wave durations that were measured from the onset of the deflection to the final return to baseline. Persistence was calculated by dividing the number of measurable F-waves by the 32 stimuli. The Famp:Mamp was calculated as follows:
where M response amplitude represents the amplitude of the first compound muscle action potential of 32 M responses. The person estimating the F-wave parameters was aware of the clinical condition of all dogs.
Statistical analysis
Values of F-wave parameters (shortest and mean latency, FWCV, mean duration, persistence, and Famp:Mamp) are reported as mean ± SD. Linear regression was performed to evaluate correlations between grade of IVDH (with clinically normal dogs assigned a grade of 0) and F-wave parameter values.
Results
F-wave examination resulted in detectable F-waves in all included dogs. The mean ± SD current of maximal stimulation was 9.3 ± 2.4 mA. F-wave persistence was 100% in all dogs. Results for Miniature Dachshunds in the clinically normal and IVDH subgroups were summarized (Table 1). Mean F-wave duration (for the 32 stimuli/dog) was correlated with grade of IVDH (Figures 2–5). Linear regression analysis yielded the following regression equation: F-wave duration (milliseconds) = 6.0 + 2.7 × IVDH grade (whereby clinically normal dogs were considered grade 0; Figure 6). The coefficient of determination (R2) for this equation was 0.98. One dog with grade 2 IVDH had a shorter F-wave duration than did all 5 dogs with grade 1 IVDH (Figure 7). One dog with grade 3 IVDH had a longer F-wave duration than did all 10 dogs with grade 4 IVDH (Figure 8). No other differences in values were identified among the clinically normal dogs and those in the various IVDH subgroups.
Representative recording of M responses (black triangle) and F-waves (white triangle) in the interosseous muscles as elicited by stimulation of the tibial nerve in a clinically normal Miniature Dachshund. Mean F-wave duration of 32 responses for this dog was 4.7 milliseconds. Negative polarity is indicated by upward deflection. Note that the recording sensitivity was changed after obtaining the M response (vertical line; see calibration). SA = Electrical stimulation artifact.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses (black triangle) and F-waves (white triangle) in the interosseous muscles as elicited by stimulation of the tibial nerve in a clinically normal Miniature Dachshund. Mean F-wave duration of 32 responses for this dog was 4.7 milliseconds. Negative polarity is indicated by upward deflection. Note that the recording sensitivity was changed after obtaining the M response (vertical line; see calibration). SA = Electrical stimulation artifact.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses (black triangle) and F-waves (white triangle) in the interosseous muscles as elicited by stimulation of the tibial nerve in a clinically normal Miniature Dachshund. Mean F-wave duration of 32 responses for this dog was 4.7 milliseconds. Negative polarity is indicated by upward deflection. Note that the recording sensitivity was changed after obtaining the M response (vertical line; see calibration). SA = Electrical stimulation artifact.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 1 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 7.6 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 1 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 7.6 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 1 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 7.6 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 14.5 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 14.5 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 14.5 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 5 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 24.1 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 5 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 24.1 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Representative recording of M responses and F-waves for a Miniature Dachshund with grade 5 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 24.1 milliseconds. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Scatterplot of mean F-wave durations (circles; mean of 32 responses/dog) for clinically normal Miniature Dachshunds (n = 10) and those with grade 1 (5), 2 (10), 3 (8), 4 (10), and 5 (10) thoracolumbar IVDH. A linear regression line is shown, the equation for which was as follows: F-wave duration = 6.0 + 2.7 × IVDH grade. The coefficient of determination (R2) was 0.98.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Scatterplot of mean F-wave durations (circles; mean of 32 responses/dog) for clinically normal Miniature Dachshunds (n = 10) and those with grade 1 (5), 2 (10), 3 (8), 4 (10), and 5 (10) thoracolumbar IVDH. A linear regression line is shown, the equation for which was as follows: F-wave duration = 6.0 + 2.7 × IVDH grade. The coefficient of determination (R2) was 0.98.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Scatterplot of mean F-wave durations (circles; mean of 32 responses/dog) for clinically normal Miniature Dachshunds (n = 10) and those with grade 1 (5), 2 (10), 3 (8), 4 (10), and 5 (10) thoracolumbar IVDH. A linear regression line is shown, the equation for which was as follows: F-wave duration = 6.0 + 2.7 × IVDH grade. The coefficient of determination (R2) was 0.98.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 2 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 5.0 milliseconds, which was shorter than that of all 5 dogs with grade 1 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 2 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 5.0 milliseconds, which was shorter than that of all 5 dogs with grade 1 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 2 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 5.0 milliseconds, which was shorter than that of all 5 dogs with grade 1 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 22.0 milliseconds, which was longer than that of all 10 dogs with grade 4 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 22.0 milliseconds, which was longer than that of all 10 dogs with grade 4 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Recording of M responses and F-waves for a Miniature Dachshund with grade 3 thoracolumbar IVDH. Mean F-wave duration of 32 responses for this dog was 22.0 milliseconds, which was longer than that of all 10 dogs with grade 4 IVDH. See Figure 2 for remainder of key.
Citation: American Journal of Veterinary Research 81, 5; 10.2460/ajvr.81.5.422
Mean ± SD values of F-wave parameters for stimulation of the tibial nerve as measured at the interosseous muscles in clinically normal Miniature Dachshunds and Miniature Dachshunds with various grades of thoracolumbar IVDH.
| Dog group | Shortest F-wave latency (ms) | Mean* F-wave latency (ms) | Mean* F-wave duration (ms) | FWCV (m/s) | Famp:Mamp (%) |
|---|---|---|---|---|---|
| Normal (n = 10) | 8.6 ± 0.6 | 9.5 ± 0.8 | 83.7 ± 6.1 | 6.6 ± 1.5 | 9.8 ± 8.5 |
| IVDH† | |||||
| Grade 1 (n = 5) | 9.3 ± 0.6 | 10.7 ± 0.8 | 78.5 ± 6.3 | 7.2 ± 1.5 | 5.6 ± 2.1 |
| Grade 2 (n = 10) | 8.4 ± 0.6 | 9.2 ± 0.5 | 82.5 ± 8.1 | 11.2 ± 2.6 | 9.5 ± 7.8 |
| Grade 3 (n = 8) | 8.7 ± 0.4 | 9.6 ± 0.7 | 80.5 ± 7.1 | 15.1 ± 3.3 | 11.7 ± 8.4 |
| Grade 4 (n = 10) | 9.1 ± 0.9 | 9.7 ± 1.0 | 80.2 ± 6.3 | 16.7 ± 2.8 | 9.3 ± 7.7 |
| Grade 5 (n = 10) | 8.5 ± 0.7 | 9.0 ± 1.0 | 82.5 ± 5.9 | 19.7 ± 3.7 | 9.5 ± 6.6 |
A total of 32 responses/dog were measured, and the mean value for each dog was calculated.
Severity of IVDH was graded on the basis of clinical signs2 as follows: 1 = signs of pain only; 2 = ataxia, conscious proprioception deficit, and paraparesis; 3 = paraplegia; 4 = paraplegia with urinary retention and overflow; and 5 = paraplegia, urinary retention and overflow, and loss of deep pain sensation.
Discussion
F-waves reflect the activity of α-motor neurons and conductivity of nervous impulses with antidromic stimulation of the peripheral motor nerves. F-wave examination is mainly used in the diagnosis of peripheral nerve disorders such as Guillain-Barré syndrome, diabetic polyneuropathy, and radiculopathy in humans.4,5 In veterinary medicine, F-wave examination has been used in the diagnosis of acute demyelinating neuropathy8,9 and diabetic neuropathy.10
In the present study, F-waves were elicited in all clinically normal Miniature Dachshunds and in all Dachshunds with various clinical grades of IVDH. The shortest and mean latencies and FWCV did not differ among dogs grouped by clinical grade. Because no difference was identified in latency and FWCV between those dogs and the clinically normal dogs, the conductive function of the tibial nerve may not have been affected in the dogs with thoracolumbar IVDH.
The F-wave is a compound muscle action potential resulting from the excitation of α-motor neurons in the ventral horn of the spinal cord. Thus, the Famp:Mamp would be expected to increase if the probability of neuron discharge increased. Indeed, F-wave amplitude and persistence reportedly increased in dogs with experimentally induced myelopathy.6 Because the amplitudes of F-waves and M responses were obtained by use of surface disk electrodes in the present study and were influenced by impedance between the electrodes and the skin surface, the Famp:Mamp could be presumed to have reflected the excitability of α-motor neurons more correctly than did the F-wave amplitude itself. Nevertheless, the Famp:Mamp was not greater in the dogs with thoracolumbar IVDH than in the clinically normal dogs. F-wave persistence in the interosseous muscles with tibial nerve stimulation was 100% even in clinically normal dogs, suggesting that maximal excitation of the involved α-motor neurons had been achieved, which could account for the nonexistent correlation between the Famp:Mamp and the severity of IVDH.
Although thoracolumbar IVDH likely affects both sensory and motor tracts in the spinal cord, the severity of dysfunction of these 2 tracts may differ among affected dogs. The conventional neurologic examination involves assessment of reflexes and reactions, which involve excitation of both sensory and motor pathways; therefore, it is difficult to determine the severity of dysfunction of the sensory and motor tracts in the spinal cord separately. Because the excitability of α-motor neurons in the ventral horn is influenced by the inhibitory tracts in the spinal cord, F-waves, which reflect excitability of a portion of α-motor neurons, must be affected in dogs with UMN signs.5 In the study reported here, the mean F-wave duration was well correlated with the severity of IVDH as graded on the basis of clinical signs, suggesting that in dogs with IVDH the inhibitory upper α-motor neurons may be proportionally affected; that is, they are more affected as the grade increases. However, 1 dog with grade 2 IVDH had a shorter mean F-wave duration than did all 5 dogs with grade 1 IVDH and 1 dog with grade 3 IVDH had a longer mean F-wave duration than did all 10 dogs with grade 4 IVDH. It is conceivable that in this dog with grade 2 IVDH, the UMNs were as affected as those in dogs with less severe neurologic signs (ie, grade 1 IVDH), despite having clinical signs classified as grade 2. Similarly, in the aforementioned dog with grade 3 IVDH, the UMNs may have been affected as severely as those in dogs with grade 4 or 5 IVDH. F-wave duration may reflect the severity of functional impairment of the inhibitory tracts for the motor neurons in the spinal cord. This information would be useful for determining the pathophysiologic mechanisms of spinal cord diseases and establishing a rehabilitation treatment strategy for affected dogs.
Overall, our findings suggested not only that mean F-wave duration is well correlated with clinical grade of IVDH but also that the effects of IVDH on the function of motor and sensory tracts in the spinal cord differ among dogs. F-wave analysis may be useful for objective evaluation of functional impairment of motor nerves as well as the inhibitory UMN tract in the spinal cord of dogs.
Acknowledgments
None of the authors had any financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of this report.
The authors thank Dr. Norio Sugimoto for assistance with the statistical analysis.
ABBREVIATIONS
| Famp:Mamp | Ratio of the mean F-wave amplitude to M response amplitude |
| FWCV | F-wave conduction velocity |
| IVDH | Intervertebral disk herniation |
| UMN | Upper motor neuron |
Footnotes
Mitsubishi Tanabe Pharma Corp, Osaka, Japan.
Isozol, Nichi-iko Pharmaceutical Co Ltd, Osaka, Japan.
Sumitomo Dainippon Pharma Co Ltd, Tokyo, Japan.
Neuropack MEB-9404, Nihon Kohden Corp, Tokyo, Japan.
QP-964B, Nihon Kohden, Tokyo, Japan.
References
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7. Okuno S, Kobayashi T, Orito K. F-wave latency and F-wave conduction velocity for the tibial nerve in clinically normal dogs. Am J Vet Res 2002;63:1262–1264.
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Appendix
Location of disk herniation for the 43 Miniature Dachshunds with thoracolumbar IVDH included in the study, by clinical grade of IVDH.
| Location | Total | Grade 1 | Grade 2 | Grade 3 | Grade 4 | Grade 5 |
|---|---|---|---|---|---|---|
| T11–12 | 5 | 0 | 0 | 1 | 0 | 4 |
| T12–13 | 11 | 0 | 1 | 2 | 6 | 2 |
| T13–L1 | 9 | 2 | 4 | 0 | 1 | 2 |
| L1–2 | 16 | 3 | 4 | 5 | 2 | 2 |
| L2–3 | 2 | 0 | 1 | 0 | 1 | 0 |
Data represent the number of dogs with IVDH at the indicated location.
