Electromyography of the neck and its relations to
pathological changes in corresponding nervous tissue
and the spine in horses with spinal ataxia
A retrospective study
C.S. (Charlotte) de Lege, BSc
Supervisors:
Mw. Dr. I.D. Wijnberg
Department of Equine Science
Faculty of Veterinary Medicine
Utrecht University
Mw. Drs. W. Bergmann
Department of Pathobiology
Faculty of Veterinary Medicine
Utrecht University
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Abstract
Objective: Spinal ataxia or lameness in the horse can be caused by lesions of the cervical spine. Clinical signs
can be caused by compression of the spinal cord or spinal nerve roots. In addition to clinical neurological and
orthopaedic examination, electromyography (EMG) can be a helpful tool in determining the nature,
localisation and severity of the problem.
The aim of this study was to examine if EMG is a reliable predictor for the site of histologically visible
neurological damage in horses with neck problems. We also examined whether lower motor neuron
abnormalities based on EMG results can be indicative for the sites of upper motor neuron damage in horses
with spinal ataxia and we examined the predictive value of EMG for the site of gross spinal pathology.
Methods: The study was done in retrospective. EMG results of thirteen horses with spinal ataxia were
compared to results of gross post mortem examination of the cervical spine and histological examination of
the cervical spinal cord, nerve roots and spinal nerves Gross post mortem examination and histological
examination were also compared to each other. Neuropathic or reinnervation motor unit action potentials
(MUAP’s) were defined as MUAP’s with increased duration, amplitude, number of turns or number of
phases, or a combination of any number of these. The histological samples of the spinal cord and nerve roots
were all re-evaluated for this study.
Results: All patients had neuropathic or reinnervation MUAP’s in the cervical area. The prevalence was
highest at the levels of C5 – C7 (85-100%). The prevalence of morphological UMN changes was highest at the
levels of C3-C5 (86-100%). The prevalence of morphological LMN changes was highest at C6 (44%). Changes
consisted mostly of Wallerian degeneration. Pathological changes of the cervical facet joints were found in
12 patients (92%) and pathological changes of intervertebral discs or ligaments were found in 6 patients
(46%). The highest prevalence of spinal column deficits was in the joints between C3-C4 (85%) followed by
C5-C6 (77%). No significant associations were found between EMG and histological changes or between
histological changes of the nervous tissue and gross changes of the spine. No statistical model could be fitted
to compare EMG results with gross spinal changes, due to little variance in results.
Conclusion: In this study we could not demonstrate significant associations between EMG and post mortem
examination results. However, the retrospective and exploratory character of the study provided some
limitations and this gave us insight in what changes in methodology could be made in future study designs
for this subject. With the right adjustments, significant results may be obtained in future studies.
1
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Introduction
Spinal ataxia or lameness in the horse can be caused by lesions of the cervical spine, that compromise the
spinal cord or nerve roots, causing damage to the upper- or lower motor neurons in the spinal cord or to the
peripheral nerves. When clinical signs are caused by compression of the spinal cord, this is called cervical
vertebral stenotic /compressive myelopathy. In young horses (≤18 months old) this is often dynamic
compression and located at the site of C3-C4 and C4-C5. In older horses (≥ 4 years old) it is usually static
compression, caused by arthropathy of the caudal cervical articular process joints (‘facet joints)’. This is
mostly located at the site of C5-C6 and C6-C7.1-3 This will usually lead to signs of upper motor neuron (UMN)
disease, like ataxia and hypermetria. When lesions of the vertebra or facet joints compromise the ventral
grey matter and/or the spinal nerve roots there will be signs of lower motor neuron (LMN) disease, like focal
muscle atrophy.4,5 To determine the nature and location of the problem, thorough clinical neurological and
orthopaedic examination has to be performed. Additional diagnostic tests, such as electromyography and
diagnostic imaging, can be very helpful in further defining the nature, localisation and severity of the
problem. 5
In human medicine, electromyography was first used in the 1950’s. Since then a lot of research has been
done and it has become a valuable and often used diagnostic tool.6 Its possibilities and limitations are wellexplored in humans. In horses however, the technique is not quite as commonly used yet.
With concentric needle electromyography (EMG) the electric activity of the muscle is recorded during
contraction or at rest. It does not involve muscle or nerve stimulation.6 It is used to evaluate the
functionality of the lower motor neurons and the motor unit. In horses, shape and duration of motor unit
action potentials (MUAP) can help to determine if a disorder is neurogenic or myogenic of nature5,7
Fig. 1: Motor unit action potential of a) mature healthy horse and b) mature neuropathic horse 6
In this study, we compared EMG results to histological visible damage of the nervous tissue.
When nervous tissue is focally traumatised, chromatolytic, atrophic or necrotic neurons can be found at the
site of the lesion, as well as spheroids and gliosis. Myelin loss and vacuolated degeneration of the white
matter of the spinal cord have also been reported. At a distance of the primary lesion, Wallerian
degeneration of the axons can be found.2,8 When the trauma directly causes death of the cell body or if the
axonal damage is close to the cell body, the entire neuron will die. It is also possible that an axon only
becomes non-viable distal from the injury and regeneration will take place through collateral sprouting.8 In
studies about chronic nerve root compression in pigs and rats, degenerative changes were found in the
myelinated axons of the nerve root, both at the site of compression itself and more proximal and more distal
to the spinal cord then the compression site. These changes included a reduction in axonal volume with
2
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
condensation of axoplasm, separation of the myelin sheath from the axon, fragmentation of the myelin and
severe wrinkling of the myelin sheath. Most changes occurred in large myelinated axons (>10 µm). 9,10
When regeneration through collateral sprouting occurs, electromyographical signs of reinnervation can be
seen as early as a few weeks after injury. In this early stage, there is decreased duration and amplitude of
the MUAP’s6. As the process continues, MUAP’s become more complex and polyphasic. When
reinnervation is complete, the MUAP’s are polyphasic and of increased duration and amplitude. This is
because larger motor units are formed by the reinnervation. 6,11 Not all nerve injury will lead to axonal
damage. In mild lesions, there may be only demyelination, even though the nerve is unable to transmit
signals. When EMG is performed in the corresponding affected muscle, a decreased number of active motor
neurons can be found, while evaluating the interference pattern. The neurons will fire more rapidly, since
the unaffected motor units must compensate for the motor units that are temporarily not receiving
stimulation.
Summarized, al lot of factors need to be taken into account when interpreting EMG results. The amount of
literature on the use of EMG in horses is starting to extent, now the use of it as aid in orthopaedic and
neurologic examination is emerging. There is however not a lot of literature on the predictable value of EMG
for the point of origin of orthopaedic or neurological problems in horses and as far as we know, no study has
been published that describes which abnormalities are actually visible in the nervous tissue in horses with
abnormal EMG results.
In this study we are comparing the EMG results of patients with cervical spinal ataxia with the results of
histological and gross examination of the cervical spinal cord and the cervical spinal nerves. We
hypothesized that EMG will be a reliable predictor for the site of morphologically visible neurological
damage in horses with neck problems.
Another of our aims is to see if lower motor neuron abnormalities based on EMG results can be indicative for
the sites of UMN damage in horses with spinal ataxia. If during pathological examination any abnormalities
of the vertebrae, intervertebral discs or the facet joints were found, we also compared these to the EMG
results to evaluate the predictive value of EMG for the site of gross spinal pathology.
3
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Materials and Methods
Study design
The study was performed retrospectively. Medical records were reviewed to select ataxic patients that
fulfilled the inclusion criteria based on clinical neurological examination, EMG and post-mortem
examination, including histopathology of the spinal cord. Data on the patients clinical signs and outcome of
EMG examination, macroscopic examination of the spine and histology of nervous tissue were all extracted
and reviewed.
Horses
Thirteen horses at the age of 13 months to 11 years old (mean age 5.3 y ± 2.8 y) with cervical neurological
problems were used in this study. The group consisted of 12 Royal Dutch Sport Horses and 1 Standardbred; 7
geldings, 2 stallions and 3 mares. The horses were all presented as patients at the Department of Equine
Science at the Veterinary Faculty of the University of Utrecht, in the period from March 2006 to January
2013. The horses had a variety of problems, such as lameness of unknown origin, muscle atrophy, poor
performance or resistance at work. The clinical signs were listed and categorized to determine the
prevalence among the patients used in this study (appendix I). Lameness that is listed among these signs is
considered of neurogenic origin, if orthopaedic problems were excluded by thorough examination by
European specialists in Equine Orthopaedic Surgery. Two horses had relevant lesions in other parts of the
spine and/or nervous tissue besides the cervical region and their clinical signs were not included in the
results displayed in figure 1.
All of the horses were clinically examined first. This included orthopaedic and neurological examination. If
neurological abnormalities were found, a needle EMG examination was performed. After euthanasia, gross
and histological pathological examination of the spine and spinal cord were performed.
EMG examination
A portable EMG apparatusa was connected to a laptop computerb to register, visualise, measure and store
the EMG signals. The activity of the resting muscle was recorded with an amplifier gain of 50 µV/division and
a sweep speed of 20 ms/division. Filter settings were 5 Hz and 10 kHz. For the recording of motor unit action
potentials (MUAP), the amplifier gain was 100 to 500 µV, depending on the size of the MUAP. The sweep
speed was 20 ms/division. A 26-gauge concentric needlec was used as recording electrode. A surgical pad
was attached to the horse with a girdle and served as a ground electrode. The correct sites for
measurements in the neck were estimated by palpating the transverse processes of the cervical vertebrae.
Insertional activity of the muscles was measured at least 3 times. After this it was checked if spontaneous
activity was present in the muscle. For MUAP sampling, the needle was inserted in at least 3 areas of each
muscle and it was redirected several times in each area, without passing the skin. The needle was withdrawn
in steps of 3 mm, to make sure there was sampling throughout the entire muscle. Only reproducible MUAP’s
with a risetime of less than 0.8 ms were analysed. All examinations were performed by a specialist in Equine
Internal Medicine.
This examination procedure has been described previously by Wijnberg et al. 12,13
The electromyography was performed on indication, based on the results of the clinical examination. In this
study we only included the outcomes of muscles that are innervated by nerves that originate from the
cervical spinal cord. Other results were ignored.
4
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Neuropathic or reinnervation MUAP’s are defined as MUAP’s with increased duration, amplitude, number of
turns or number of phases, or a combination of any number of these. Reference values were used from
previous research. 13-15
Post mortem examination
During necropsy, the nervous tissue of the neck was examined grossly and histologically. The histological
slides could include cervical spinal cord, exiting nerve roots, spinal nerves and/or spinal ganglia. The variation
in content of the slides is due to the fact that the study was done in retrospective and no strict protocol was
in place at the time of the necropsies. The nervous tissue samples were taken from between adjacent
vertebrae. Which segments were sampled varies between patients and is dependent on requests for
examination and on gross findings during necropsy. Examination requests were based on either physical
examination, radiography and/or EMG results. Sampled segments for each patient are described in appendix
III. Tissue samples of the nervous tissue were fixed in 10 % neutral buffered formalin and sections were
routinely embedded in paraffin. Slices of 4 µm were stained with haematoxylin and eosin. For this study, all
the samples were re-examined by a board certified veterinary pathologist.
When clinical and/or EMG examination indicated problems with the plexus brachialis, this was also included
in the examination. Also the cervical vertebrae, facet joints and intervertebral discs were grossly examined
in all the patients. Special attention was paid to the alignment of the vertebrae and discs and the integrity of
the discs and ligaments. The facet joints were examined thoroughly for any form of arthropathy.
Statistical analysis
Statistical analysis was performed by a statistician, with a commercially available program, R.16 A logistic
regression model was performed with random patient effects and the Akaike information criterion (AIC) was
used for model building. When comparing site of lesion indicated by EMG results with site of histopathology
and with site of gross spinal anomalies, anatomical site in the neck and EMG results were used as fixed
effects and, respectively, presence of histopathology and presence of gross spinal anomalies were used as
variables. When comparing site of gross spinal anomalies with site of histopathology, anatomical site in the
neck and presence of gross spinal anomalies were used as fixed effects and presence of histopathology was
used a variable. Significance was set at P < 0.05.
For descriptive statistic, SPSS17 was used.
a: Nicolet Meridian EMG apparatus, Nicolet Biomedical Inc, Madison,Wis.
b: Topline 8000,Topline, Hoevelaken, The Netherlands.
c: EMG concentric needle electrode, Nicolet Biomedical Inc, Madison,Wis.
5
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Results
Clinical signs
In appendix I the horses’ clinical signs are described. The prevalence of observed clinical signs in the
patients with only cervical problems is displayed in figure 2. Two horses also had lesions in the thoracic
and/or lumbar part of the spine and were therefore not included in the data displayed in figure 2.
Figure 2: Prevalence of specific clinical signs in eleven ataxic
neckpatients
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
EMG examination
Neuropathic or reinnervation MUAP’s were found in all 13 patients. An detailed description of abnormalities
can be found in Appendix II.
Segments C5, C6 and C7 were examined in all patients. C5 was abnormal in 11 patients (85%), C6 was
abnormal in 12 patients (92%) and C7 was abnormal in all patients. Segment T1 was examined in 4 patients
and was abnormal in 3 patients (75%). Both segments C3 and C4 were examined in 6 patients, C3 was
abnormal in 2 patients(33%) and C4 was abnormal in 3 patients (50%). Segment C2 was examined in 2
patients and was abnormal in 1 patient(50%). Segment C1 was not examined.
This data are displayed per segment in figure 3. Since not every segment was examined in all horses, a
percentage is displayed instead of an absolute number.
6
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Percentage of abnormal results per
segment
Figure 3: Abnormal EMG results per cervical segment
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
C2
C3
C4
C5
C6
C7
T1
Histopathology of the nervous tissue
In 11 patients, mild histological changes were found in various parts of the examined nervous tissue and in
two patients moderate changes were found. A detailed description of the changes can be found in Appendix
III. The plexi brachialis were examined in one patient, but no changes were found. Segment C1 was
examined in 7 patients, of which 5 (71%) had changes in UMN on this level and 2 (29%) had changes in the
LMN on this level. C2 was examined in 7 patients, of which 5 (71%) had UMN changes and 0 had LMN
changes. C3 was examined in 8 patients, all of which had UMN changes (100%) and 2 (25%) had LMN
changes. C4 was examined in 7 patients, 6 (86%) had UMN changes and 0 had LMN changes. C5 was
examined in 9 patients, 8 (89%) had UMN changes and 2 (22%) had LMN changes. C6 was examined in 9
patients, 6 (67%) had UMN changes and 4 (44%) had LMN changes. C7 was examined in 8 patients, 6 (75%)
had UMN changes and 1 (13%) had LMN changes. T1 was examined in 4 patients, 2 (50%) had UMN changes
and 0 had LMN changes. The exact nature and location of the changes is described in Appendix III.
This data is displayed in figures 4a (UMN) and 4b (LMN).
In some of the patients swollen, basophilic axons were found in the spinal and/or peripheral nerves
(Appendix III). These are highly suspected of being artefacts, since they were also found in other studies in
stillborn foals (W. Bergmann, personal correspondence). Therefore they were not included in the results.
Prevalence of morfological UMN
abnormalities per segment
Figure 4a: Histopathology of the upper motor neurons
100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
C1
C2
C3
C4
C5
C6
C7
T1
7
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Prevalence of morfological LMN
abnormalities per segment
Figure 4b: Histopathology of the lower motor neurons
50%
45%
40%
35%
30%
25%
20%
15%
10%
5%
0%
C1
C2
C3
C4
C5
C6
C7
T1
We compared the locations of histologically visible UMN lesions and histologically visible LMN lesions (fig.
4c). 59 locations in the neck were examined, in 11 horses. In 12 locations (20%), both UMN and LMN lesions
were present. In 10 locations (17%) there were no lesions at all. In 36 locations (61%) we did find UMN
lesions, but no LMN lesions. In only 1 location (2%)we found LMN lesions, but no UMN lesions.
Figure 4c: Comparison histopathology LMN vs UMN
LMN
No lesion
UMN
Lesion
Total
No lesion
12
1
13
Lesion
36
10
46
48
11
59
Total
Comparison EMG – histopathology
Both EMG and histopathology results were available for 32 locations in 11 patients.
EMG results and histopathology results of the LMN agreed on the absence or presence of abnormalities in 9
of 32 locations. (fig. 5). Presumed artefacts in histology are not included in this comparison.
When these data were statistically analysed, no significant association was found between locations with
abnormal EMG results and locations with abnormal histology of the LMN.
Figure 5: Comparison of EMG and histopathology of LMN
LMN
No lesion
EMG No lesion
Lesion
Total
Lesion
Total
4
3
7
20
5
25
24
8
32
8
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
When EMG results and histology results of the UMN were compared, they agreed on the absence or
presence of abnormalities in 21 of 32 locations (fig. 6).
When these data were statistically analysed, no significant association was found between locations with
abnormal EMG results and locations with abnormal histology of the UMN.
Figure 6 : Comparison of EMG results and
histopathology of the UMN
UMN
No lesion
EMG No lesion
Lesion
Total
Lesion
Total
1
6
7
5
20
25
6
26
32
Gross pathological examination of the cervical spine
In 12 patients (92%), changes of the cervical facet joints were found. 11 of these patients had degenerative
changes of the cartilage, varying from mild to severe, and one patient had osteochondrosis in one facet joint.
A detailed description of the changes can be found in Appendix IV.
In 6 patients (46 %) deficits of intervertebral discs or intervertebral ligaments were found. In all 6 of these
patients there were abnormalities between C6-C7. In none of the patients abnormalities of discs and/or
ligaments were found between C1-C2 and C2-C3. (Appendix IV)
Figure 7 displays the prevalence of abnormalities per anatomical location.
prevalence of gross anomalies per
segment
Figure 7: Gross anomalies of the cervical spine
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
C1-C2 C2-C3 C3-C4 C4-C5 C5-C6 C6-C7 C7-T1
Comparison EMG – gross pathological examination of the cervical spine
Both EMG results and results of gross examination of the cervical spine (including ligaments, intervertebral
discs and the facet joints)were available for 50 locations in 12 patients.
EMG results and results of gross examination of the spine agreed in the absence or presence of
abnormalities in 29 of 50 locations (fig. 8a). Due to little variance in results, no statistical model could be
fitted and analysis was not possible.
9
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Figure 8a: Comparison of results of EMG and gross
examination of the cervical spine
Spine
Normal
EMG
Normal
Abnormal
Total
Abnormal
Total
4
7
11
14
25
39
18
32
50
We also looked at the facet joints separately from the rest of the spine, so we could further differentiate the
locations in left side and right side of the patient. We then had 86 locations for which both EMG results and
pathology results were available. The EMG results and results of gross examination of the facet joints agreed
on the absence or presence of abnormalities in 51 of 86 locations (Fig. 8b).
Due to little variance in results, no statistical model could be fitted and analysis was not possible.
Figure 8b: Comparison of results of EMG and gross
examination of the cervical facet joints
Facet Joints
Normal
EMG
Abnormal
Total
Normal
14
13
27
Abnormal
22
37
59
36
50
86
Total
Comparison gross spinal anomalies – histopathology nervous tissue
Both results of histopathology of the nervous tissue and results of gross pathological examination of the
cervical spine were available of 59 locations in 11 patients.
Results of LMN histopathology and gross examination of the spine agreed on the absence or presence of
abnormalities in 27 of 57 locations (fig. 9a) Presumed artefacts in histopathology were not included in this
comparison.
When this data was statistically analysed, no significant association was found between locations with
abnormal LMN histopathology and locations with gross spinal anomalies.
Figure 9a: Comparison of gross spinal anomalies with
histopathology of the LMN
Spine
Normal
LMN
Normal
Abnormal
Total
Abnormal
Total
17
29
46
1
10
11
18
39
57
10
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Results of UMN histopathology and gross examination of the spine agreed on the absence or presence of
abnormalities in 36 of 57 locations (fig. 9b).
When this data was statistically analysed, no significant association was found between locations with
abnormal LMN histopathology and locations with gross spinal anomalies.
Figure 9b: Comparison of gross spinal anomalies with
histopathology of the UMN
Spine
Normal
UMN
Normal
Abnormal
Total
Abnormal
Total
4
7
11
14
32
46
18
39
57
11
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Discussion
The primary aim of our study was to examine if EMG is a reliable predictor for the site of neurological
damage in horses with neck problems. We did this by comparing the EMG results of patients with cervical
spinal ataxia with the results of post mortem histological and gross examination of the cervical spinal cord
and spinal nerves. Besides this, we also compared the histological findings of the spinal cord and spinal
nerves, with the results of gross examination of the spinal column and its joints and ligaments.
Unfortunately, we were not able to demonstrate any statistical significant relation between the EMG results
and the changes we found during necropsy. Neither did we find any statistical significant relation between
histological findings of the nervous tissue and gross examination of the spinal column. However, in the
course of this retrospective study we found some issues with the methodology that influenced the results
and the outcome of the statistical analysis. These issues will be discussed here and in further research, the
methodology will be adjusted according to the results in this study.
All subjects had neuropathic or reinnervation MUAP’s in the cervical area. The prevalence was highest in C5
– C7 (85-100%). Wijnberg et al (2004) also found the highest prevalence of neuropathic EMG results in the
caudal neck (C5-T1). 5
In the nervous tissue of our subjects, there was mostly a mild number of histological changes. In 2 patients a
moderate number of changes was found. Unfortunately there was no standardised scoring system used in
the evaluation of the histological slides. The prevalence of histological UMN changes was highest at the level
of C3-C5 (86-100%). The prevalence of histological LMN changes was highest at C6 (44%). This is in
agreement with the fact that we found the highest prevalence of abnormal EMG results in the area between
C5 and C7. The histological changes consisted mostly of Wallerian degeneration. Also some necrotic neurons
and hypereosinofilic, swollen axons (spheroids) were found. In a few horses we found gliosis or neurons with
lipofuscin in the cytoplasm. In several slides we found swollen, basophilic axons. We suspected that these
were artefacts, since in axonopathy and Wallerian degeneration, the swollen axons become
hypereosinophilic.8 This is supported by the fact that these swollen, basophilic axons have also been found in
a study with stillborn foals (W. Bergmann, personal correspondence). For completeness, they are mentioned
in appendix III, but they are further ignored in the results.
Overall we found low prevalences of LMN changes. This is surprising, since neuropathic EMG results were
found in all patients. This can also be seen in appendix V, which summarizes for each patient which of the
from EMG, histology of LMN and UMN and pathology of the spinal column, were abnormal in which cervical
segment. No histological LMN changes were discovered at the levels of C2, C4 and T1 in any of the horses,
while there were several patients with neuropathic EMG results at this levels.
An explanation for these unexpected results is that nearly all examined nervous tissue came from within the
vertebral canal, while nerve root compression mostly affects the dorsal root ganglion or exiting nerve root.
Previous studies about chronic nerve root compression in pigs and rats has been focused on the compression
site of the dorsal root ganglion or exiting nerve root itself and its close proximity (≤ 18 mm). Here they found
a reduction in axonal volume with condensation of axoplasm, separation of the myelin sheath from the axon,
fragmentation of the myelin, severe wrinkling of the myelin sheath and a reduction in (large) myelinated
axons. 9,10 However, in these studies a controlled amount of compression was applied to the nerve roots.
This was not the case in our patients, so we can assume that a difference existed in the amount of
compression of the roots between our patients themselves and with the subjects in these previous studies.
12
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
This may influence the presence and visibility of histological changes. We should also take into consideration
that in nervous tissue functional deficits can precede any morphological changes that would be visible with
light microscopy. 8
We found no significant association between the location of histological LMN abnormalities and abnormal
EMG results. This is most likely caused by the small number of LMN abnormalities that was found, as
discussed earlier. Also, in human medicine there is known to be significant overlap in EMG results between
C5 and C6 radiculopathy and C6 and C7 radiculopathy.18 Such overlap could also exist in cervical
radiculopathies in horses, which would create more room for errors in defining which precise nerve root is
affected with help of EMG. Another factor in this is that the sites for EMG measurements in the neck were
estimated by palpating the transverse processes of the cervical vertebrae, which can also lead to errors in
defining of which exact nerve root the functionality is tested.
In horses with nerve root compression caused by facet joint malformation, concurrent central compression
can occur on the same location. Besides encroaching in the intervertebral foramen, the facet joints can also
enlarge towards the spinal cord.4,19 With this in mind, we wanted to examine if lower motor abnormalities
based on EMG results could be indicative for the site of UMN damage in horses with cervical spinal ataxia. In
appendix V we can see that histological UMN abnormalities were found in all patients. This was to be
expected, since the presence of spinal ataxia, which is caused by UMN problems, was an inclusion criterion
for this study. EMG and histopathology of the UMN agreed on the presence or absence of abnormalities in
21 of 32 examined locations. This result is statistically not significant. Therefore we could conclude that EMG
results of the neck are not indicative for location of histological visible UMN damage in the cervical spinal
cord. However, a factor in this non-significant result could be that EMG was not performed on the entire
neck of most subjects, but only on locations were abnormalities were expected, based on clinical
examination. This leads to an incomplete data set, since different segments were examined in different
subjects. The same holds for the histopathological examination, since in only a few subjects slides were
taken from all segments of the cervical spinal cord.
If during pathological examination any abnormalities of the vertebrae, intervertebral discs or the facet joints
were found, we also compared these to the EMG results to evaluate the predictive value of EMG for the site
of gross spinal pathology. In 12 out of 13 patients, deficits of the cervical facet joints were found. Six patients
had deficits of intervertebral discs or soft tissue. The highest prevalence of gross spinal column deficits found
with necropsy, was in C3-C4 (85%) followed by C5-C6 (77%). This seems to be in agreement with our
histological findings in the nervous tissue, were highest prevalences of UMN changes were found in the
nervous tissue of C3 – C5 and highest prevalences of LMN changes at C6. Although most degenerative joint
changes are usually found in the caudal neck, it is not completely unexpected that we also have a lot of
changes more cranial in the neck. The degenerative joint changes in the caudal neck are often seen in older
horses, due to wearing from work.3,19 But in this study there were also a lot of younger patients (mean age
5.3 years). It is plausible that some of the abnormalities we found in the patients were actually caused by
some form of trauma, leading to different locations of abnormalities than just the caudal neck.
EMG and pathological examination of the spinal column, and its joints and ligaments, agreed on the
presence or absence of abnormalities in 29 out of 50 examined anatomical sites. When we excluded the
abnormalities of the intervertebral discs and soft tissue and only focussed on the facet joints, EMG and
pathological examination agreed on 51 out of 86 examined anatomical sites. Both results were statistically
not significant. The higher number of examined sites when we focussed on facet joints is caused by the fact
13
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
that here we also made a left and right distinction instead of looking at the whole segment. A noticeable
observation was that in both cases, EMG showed slightly more abnormalities than pathology. In other
studies, degenerative joint disease was also found in control horses or was not related to clinical signs.19,20
Therefore it could have been expected that in this study we found more spinal column abnormalities than
EMG abnormalities. A possible explanation for the unexpected result is that the spinal column, and
especially the facet joints, has not been checked equally thorough in all of our patients. The research was
done in retrospective and no scoring protocol was used in earlier patients. In these patients, the spinal
column was mostly examined for changes in vertebrae, ligaments and intervertebral discs, and less attention
was paid to the facet joints. In patients that were admitted later in the time frame, a closer look was taken at
the facet joints and more abnormalities were found.
When we compared the results of gross examination of the spinal column with histopathology of the LMN
and UMN, we found no significant association for abnormal anatomical locations. Issues that probably have
a part in this lack of significance are discussed in earlier paragraphs. These include the location of which
histological samples were taken, the absence of a protocol for examining the slides and the fact that gross
examination of the facet joints was not done by a protocol in earlier patients.
Little research has been done to the direct relation between gross pathology of the spinal column and
histological changes in the spinal cord and exiting nerves. Moore et al 4 found that contrast-enhanced
computed tomography (CT) correctly identified 10 out of 10 histopathological confirmed compressive lesions
of the cervical spinal cord and falsely identified 1 histopathologically normal site as a compressive lesion.
Also, the CT measurements of minimal sagittal diameter (MSD) in that study were strongly correlated (r
=0.92)to necropsy measurements of the MSD. However, necropsy of the spinal column and histopathology
were not directly compared, so no relations were established between these. In a cadaver study by Claridge
et al 21, extending of the articular process joints into the vertebral space was not severe enough to directly
cause compression of the spinal cord, in absence of other spinal column pathology. This is consistent with
our finding that spinal column changes were not significantly associated with histologically visible UMN
changes.
Unfortunately, we were not able to get statistically significant results in this study. This is most likely due to
the above mentioned limitations that were caused by the retrospective and exploratory character of the
study. For future studies on this subject, it is first of all important that complete data sets are available. This
would mean that with EMG examination, all cervical segments have to be examined instead of only the
segments with suspected problems. Also, at least one or a few slides from all cervical segments will have to
be available for histological examination. Second, the locations from which the histological slides are taken
should be extended to further outside the vertebral column, including more of the nerve roots , exiting
nerves and spinal ganglia, so that damage of the exiting nerve roots can be detected and a full examination
of the LMN’s can be established. Also a standardized protocol has to be used for evaluation of the
histological slides. Last, it would be preferable to have more patients in the study, to get solid statistical
results. This research will continue with changes in methodology, mostly in the protocols for EMG
examination and histology sampling, based on the results of this study.
14
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
Acknowledgements
I want to thank my supervisors for their help, feedback and support. They really helped me with
understanding the sometimes difficult matter and with collecting all the data from different systems in
different departments. They also made time, if necessary, to go over the EMG results again with me and to
re-evaluate the histological slides.
Also I want to thank Jan van den Broek for helping me with the complicated statistics of this project.
15
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
APPENDIX I: Clinical data of thirteen horses with spinal ataxia
Patient
no:
1
Age
Sex
Breed
Clinical signs
8 yr
Gelding
Royal Dutch
Sporthorse
2
2 yr
Stallion
3
6 yr
Gelding
Royal Dutch
Sporthorse
Royal Dutch
Sporthorse
4
1 yr
Stallion
Carries tail to the left. Abduction RH. Atrophy of neck
muscles, painful on C3-C4 R. Decreased tail tone. Delayed
postural reactions LH+RH.
Knuckling LF, atrophy of biceps and triceps, decreased neck
mobility, caudal 1/3 of neck is painful
Lameness LF + RF. Resistance at work when going
clockwise. Incoordination and dysmetria when walking with
lifted head and tail-pull. Decreased mobility of the neck.
Delayed postural reactions on RH+LH> RF+LF
Shivers (hypermetria) on hindlimbs
5
5 yr
Mare
6
6 yr
Gelding
Royal Dutch
Sporthorse
7
9 yr
Mare
Royal Dutch
Sporthorse
8
6 yr
Mare
Royal Dutch
Sporthorse
9
4 yr
Gelding
Royal Dutch
Sporthorse
10
3 yr
Gelding
Standardbred
11
4 yr
Gelding
Royal Dutch
Sporthorse
12
4 yr
Gelding
Royal Dutch
Sporthorse
13
11 yr
Gelding
Royal Dutch
Sporthorse
Royal Dutch
Sporthorse
Royal Dutch
Sporthorse
Hypermetria LH. Muscle atrophy of caudal neck, both sides,
C6/C7 painful. Delayed postural reactions LF+RF, absent
LH+RH
Hypermetria, abduction and knuckling LH+RH, weakness in
hindlimbs when going backwards. Problems with tight
circles, lack of coordination when trotting. Slips on hard
surface. Atrophy of neck muscles, swelling around C3. C5
mildly painful. Decreased mobility of the neck. Strongly
delayed postural reactions in all limbs.
Abduction of LH + RH on circle, standing on own feet while
spinning. Decreased mobility of the neck and painful neck.
Bunny hop. Delayed postural reactions RH.
Resistance at work, hypermetric front. Decreased neck
mobility, C3-C4 painful. Postural reactions delayed in all
limbs, decreased control on tail-pull.
Stumbling, hypermetria LH. Abduction of hindlimbs.
Decreased neck mobility, C7 painful. Delayed postural
reactions LH + RH
Gait and stance deficits, including hypermetria. Abduction of
hindlimbs. Delayed postural reactions LH + RH
Problems with spinning clockwise, hypermetria LF+RF
when walking with head lifted. Poor muscularity caudal
neck, C6+C7 painful, decreased mobility of neck. Delayed
postural reactions LH+RH.
Mild lameness RF, C5-C7 painful, decreased neck mobility to
the left. Delayed postural reactions RF+RH, decreased
control on tail-pull
Lameness RF, intermittent hypermetric + abduction RH,
bunny hop on clockwise circle, problems with spinning
clockwise, amble when walking with head lifted Decreased
neckmobility L+R. Delayed postural reaction RH.
RH: Right hindlimb; LH: Left hindlimb; RF: Right frontlimb; LF: Left frontlimb; Cx: Cervical vertebrae x
16
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
APPENDIX II: Electromyographical results in thirteen horses with spinal ataxia
Patient
no.
Examined muscles
Findings
1
Unknown
2
Scl, pect.desc, pect.trans, serr.v C6-C7,
tric.brach, splen.cerv C2-C3
Scl L&R, Serr.v C4-C7 L&R, splen.cerv
C3 R, brceph C7 L&R
Scl L&R, serr.v C6-C7 L&R, pect.desc R
Scl L&R, serr.v C6 L&R
Scl L&R, serr.v C4-C7 L + C5-C7 R
Scl L&R, serr.v C6-C7 L&R
Scl L&R, serr.v C4 L + C5-C7 L&R,
splen.cerv C3 L
C3-C5 L reinn MUAP’s, but also some high,
narrow MUAP’s. Scl, C6, C7 L some reinn
MUAP’s, but mostly normal.
Neuropathic MUAP’s on C7, tric. brach, pect.
trans. Pect.trans poor i.p.
Neuropathic MUAP’s scl, C6, C7 L&R, C3-C5
R. L>R
Neuropathic MUAP’s on scl, C7 L+R, C6 R
Reinn MUAP’s on scl R
Neuropathic MUAP’s on C6, C7 L>R, C4 L
Neuropathic MUAP’s on C6,C7 R>L, Scl R.
Abnormal on C7>C6>C5, L>R. MUAP’s are
complex, high and narrow. Sometimes
broad or polyphasic.
Neuropathic MUAP’s on C7,T1 L&R, C5-C6
L.
Neuropathic MUAP’s on C4-C5 R + C2, C5-C7
L. L>R
Neuropathic MUAP’s on scl L&R, C6 L&R, C7
R. C3 normal. R>L
Neuropathic MUAP’s on C5 + C7 L+R
3
4
5
6
7
8
9
Scl L&R, serr.v C4 R + C5-C7 L&R,
pect.desc L
10
Serr.v C4 R + C5-C7 L&R, Splen.cerv
C2 L&R + C3 R
11
Scl L&R, serr.v C6-C7 L&R, splen.cerv
C3 R
12
Scl L&R, serr.v C5-C7 L&R+C4 R,
Brceph C7 L
13
Scl L&R, serr.v C5, C7 L&R + C6 R,
Scl L&R poor ip, delt & inf.spin R PSA, pw,
splen.cerv C3 L, inf.spin L&R, sup.spin fib & nmyot. Neuropathic on C3, C5, C7 L +
L&R, delt L&R
C5-C7 R.
Scl: m. subclavius; Serr.v: m. serratus ventralus ; Ext.rad: m. extensor carpi radialis; Splen.cerv: m.
splenius pars vervicalis; Pect.desc: m. pectroralis descendens; Pect.trans: m. pectoralis transversus;
Tric.brach: m. triceps brachii; Sup.spin: m. supraspinatus; Inf.spin: m. infraspinatus; Brceph: m.
brachiocephalicus; ip:interference pattern; Delt: m. deltoideus; PSA: pathological spontaneous
activity
17
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
APPENDIX III: Histopathological findings in thirteen horses with spinal ataxia
Patient
No.
1
Examined
nervous
tissue
C3-T1
2
C1, C3, C5, T1
3
C1 – C3, C5,
C7
4
C2, C6, C7
5
6
Spinal cord,
location
unknown
C1 – C7
7
C1 – C7
8
C2, C6, T1
9
Spinal cord,
location
unknown
C1, C3 – C6
10
11
C1 – C7
Plexi
brachialis,
peripheral
Findings
C3: Mild wallerian degeneration (wd) in all funiculi (fun). Basophil,
swollen axons in L+R peripheral nerve (p.nerve); C4: mild wd in lateral
(lat) + ventral (ven) fun; C5: moderate wd in all fun. Swollen, basophil
axon in p.nerve; C6: mild wd in lat + ven fun, mild wd in p.nerve; C7: mild
wd in ven + lat fun. Swollen, basophil axon in p.nerve; T1: mild wd in lat
fun. Swollen, basophil axons in p.nerve.
C1: some dilated myelinsheats in all fun. Mild wd in ven fun.; C3: mild wd
in lat fun. Some dilated myelinsheats in ven fun. Necrotic neuron in ven
horn; C5: Mild wd in ven fun; T1: Mild wd in ven and lat fun.
C1: No changes; C2: spheroid on transition grey-white matter, L lat fun.
Mild wd in L lat fun; C3: mild wd in L lat fun; C5: mild wd in L ven + lat
fun; C7: mild wd in L lat fun
C2: No changes; C6: Swollen, basophil axons in dorsal (dors) spinal nerve
C7: digestion chamber in L dors-lat white matter
Some dilated myelin sheaths in lat fun, but without swollen axons.
Suspected artefact
C1: Necrotic neuron in centre grey matter. Moderate wd in all fun. Mild wd
in ventral spinal nerve; C2: moderate wd in all fun. ; C3: moderate wd in
dors fun, mild wd in ven fun; C4: moderate wd in ven fun, mild wd in lat
fun; C5: moderate wd in dors fun, mild wd in ven fun; C6: mild wd in dors
fun, moderate wd in ven fun; C7: mild wd in dors fun, moderate wd in ven
fun.
C1: Mild wd in lat fun; C2: No changes; C3: mild wd in lat fun; C4: mild wd
in ven fun; C5: mild wd in lat + dors fun; C6: mild wd in ven fun; C7: mild
wd in dors + ven fun
C2: mild wd in dors and ven fun, spheroid in dors fun; C6: mild wd in R+L
ven fun; T1: no changes
Few neurons with lipofuscin in cytoplasma. Wd in ven fun. Some
eosinophilic material in grey matter, unclear if necrotic neuron of spheroid
C1: No changes; C3: Mild wd in dors + ven fun; C4: mild wd in dors fun; C5:
No changes; C6: focal gliosis in grey matter, mild wd in dors + ven fun
C1: mild wd in R lat fun. Dilated myelinsheat in L lat + dors fun. Hypereos,
swollen axon/dendrite in R dors horn; C2: dilated myelinsheat in R ven
fun, swollen, hypereos axon in L lat fun. Swollen, basophil axon in L+R
p.nerve; C3: mild wd in lat fun. Hypereos, swollen axons in ven horn; C4:
18
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
nerves
swollen, basophil axon in R p.nerve; C5: dilated myelinsheat in L+R ven
fun. Swollen, basophil axon in R p.nerve; C6: swollen, basophil axon in R
p.nerve; C7: swollen, basophil axon in p.nerve; Plex brach L+R: no changes
12
C4 – T1
C4: Spheroid in L dors horn. Mild wd in L dors fun + L p.nerve; C5: Mild wd
in L&R lat fun + R ven fun. Hypereos swollen axons in L p.nerve, Swollen,
basophil axons in R p.nerve; C6: Spheroid in L ven horn; C7: Swollen,
basophil axons in R p.nerve; T1: Swollen, basophil axons in R p.nerve.
13
C1 – C7
C1: Mild wd in L lat + ven fun. Dilated myelinsheats in L p.nerve; C2: Mild
wd in dors fun. Swollen, basophil axons in R p.nerve. C3: Mild wd in R lat
fun. Swollen, basophil axons in R p.nerve; C4: Mild wd in L&R dors + ven
fun. Swollen, basophil axons in L&R p.nerve; C5: Mild wd in L&R dors +
ven fun + R lat fun. Dilated myelinsheat + swollen, basophil axons in R
p.nerve; C6: Spheroids in L ven horn. Mild wd in L&R ven + lat fun + R dors
fun. Swollen, basophil axons in L p.nerve; C7: Mild wd in L&R lat fun + R
dors + ven fun. Dilated myelinsheats in R p.nerve. Swollen, basophil axons
in L p.nerve.
Wd: Wallerian degeneration; L:left; R:right; dors: dorsal; ven: ventral; lat: lateral; fun: funiculus/funiculi;
hypereos: hypereosinophilic; p.nerve: peripheral nerve; Cx/Tx: nervous tissue on the level of cervical
vertebra Cx/Tx
19
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
APPENDIX IV: Gross anomalies in the cervical spine of thirteen horses with spinal ataxia
Patient
no.
1
2
Findings
Mild dorsal protrusion of intervertebral ligament between C3-C4 and C6-C7
Protrusion of the intervertebral discs into the spinal canal, between C5-C6, C6C7, C7-T1. Mild cartilage defects on the left facet joints C3-C4.
3
Multifocal, mild to moderate chronic degeneration of the facet joints of C2-T1
L+R, except for C5-C6 R. Chondrones in dorsal intervertebral ligament C6-C7.
4
Focal, mild osteochondrosis of the cartilage on the cranial facet joint C6.
5
Mild to moderate chronic degeneration of the cranial facet joints of C2-C6,
bilaterally. The degeneration became more mildly on the more caudal cervical
vertebrae.
6
Mild to moderate chronic degeneration of the facet joints of C1-C5, bilateral.
Bilateral rupture of the ligamentum flavum C6-C7
7
Multifocal, moderate chronic degeneration of the facet joints of C3-C7
bilaterally, C2-C3 R.
8
Multifocal, moderate to severe chronic degeneration of the cranial facet joints
of C3, C4 bilaterally and C5, C6 R. Also of the fovea articularis caudalis on C1 R.
9
Multifocal chronic degeneration of the facet joints C1-C3 L + C5-T1 L&R.
Protrusion of intervertebral discs, moderate between C5-C6, mild between C6C7.
10
Moderate irregularity of the facet joints between C3-C4 and C5-C6, bilateral.
11
Moderate to severe chronic degeneration of all cervical facet joints, bilaterally,
including C7-T1. Most severe C7 L.
12
Degenerative changes in all cervical facet joints, bilaterally, including C7-T1.
Enlarged facets between C4-C5 L&R + C5-C6 R.
13
Moderate intrusion intervertebral disc C4-C5, intervertebral discs C4-C5, C5C6, C6-C7, C7-T1 all partially ruptured. Degenerative changes in all cervical
facet joints, bilaterally, including C7-T1. Stenosis of vertebral canal on level of
C6-C7 R.
Cx: Cervical vertebra nr x; T1: Thoracic vertebra nr 1.
20
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
APPENDIX V: Summary of abnormalities per patient per cervical segment
Patient
1
2
3
4
5
6
Cervical
segment
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
EMG
Histology
LMN
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Histology
UMN
Clinical
signs
(Pain,
muscle
atrophy)
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
-
+
+
-
+
+
+
+
+
+
-
+
+
+
+
+
+
+
+
-
-
-
-
+
+
-
+
+
+
+
Pathology
spinal
column
+
+
-
+
+
+
+
+
+
+
+
+
+
+
+
21
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
7
8
9
10
11
12
13
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
C6
C7
T1
C1
C2
C3
C4
C5
+
+
-
+
+
+
+/+
-
+
+
+
-
+
+
+
+
+
+
+
+
+
+
+
-
-
+
+
+
+
+
-
+
+
+
-
+
+
+
+
+
+
+
+
+
+
+
+
-
-
-
+
+
+
+
+
+
+
+
+
+
-
+
+
+
+
-
+
+
+
+
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
-
+
+
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
-
+
22
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
C6
+
C7
+
T1
+) Abnormal result - ) No abnormalities
+
+
+
+
+
+
References
1. Dyson SJ. Lesions of the equine neck resulting in lameness or poor performance. Veterinary Clinics of
North America - Equine Practice. 2011;27(3):417-437
2. Nout YS, Reed SM. Cervical vertebral stenotic myelopathy. Equine Veterinary Education.
2003;15(4):212-223.
3. Levine JM, Adam E, MacKay RJ, Walker MA, Frederick JD, Cohen ND. Confirmed and presumptive
cervical vertebral compressive myelopathy in older horses: A retrospective study (1992-2004). Journal
of Veterinary Internal Medicine. 2007;21(4):812-819.
4. Moore BR. Contrast-enhanced computed tomography and myelography in six horses with cervical
stenotic myelopathy. Equine Vet J. 1992;24(3):197-202.
5. Wijnberg ID, Back W, De Jong M, Zuidhof MC, Van Den Belt AJM, Van Der Kolk JH. The role of
electromyography in clinical diagnosis of neuromuscular locomotor problems in the horse. Equine Vet J.
2004;36(8):718-722.
6. Wijnberg ID. A review of the use of electromyography in equine neurological diseases. Equine
Veterinary Education. 2005;17(3):123-127.
7. Wijnberg ID, Franssen H, Jansen GH, Back W, Van Der Kolk JH. Quantitative electromyographic
examination in myogenic disorders of 6 horses. Journal of Veterinary Internal Medicine. 2003;17(2):185193. Accessed 20 March 2013.
8. Maxie MG. Jubb, kennedy & palmer's pathology of domestic animals. Jubb, Kennedy & Palmer's
Pathology of Domestic Animals. 2007.
9. Cornefjord M, Sato K, Olmarker K, Rydevik B, Nordborg C. A model for chronic nerve root
compression studies: Presentation of a porcine model for controlled, slow-onset compression with
analyses of anatomic aspects, compression onset rate, and morphologic and neurophysiologic effects.
Spine. 1997;22(9):946-957.
10. Jancalek R, Dubovy P. An experimental animal model of spinal root compression syndrome: An
analysis of morphological changes of myelinated axons during compression radiculopathy and after
decompression. Experimental Brain Research. 2007;179(1):111-119.
11. Campbell WW. Evaluation and management of peripheral nerve injury. Clinical Neurophysiology.
2008;119(9):1951-1965.
12. Wijnberg ID, Franssen H, Van Der Kolk JH, Breukink HJ. Quantitative motor unit action potential
analysis of skeletal muscles in the warmblood horse. Equine Vet J. 2002;34(6):556-561.
23
Electromyography of the neck and its relations to pathological changes in corresponding nervous tissue and
the spine in horses with spinal ataxia – C.S. de Lege, BSc
13. Wijnberg ID, Franssen H, van der Kolk JH, Breukink HJ. Quantitative analysis of motor unit action
potentials in the subclavian muscle of healthy horses. Am J Vet Res. 2002;63(2):198-203.
14. Wijnberg ID, Franssen H, van der Kolk JH. Influence of age of horse on results of quantitative
electromyographic needle examination of skeletal muscles in dutch warmblood horses. Am J Vet Res.
2003;64(1):70-75.
15. Wijnberg ID, Graubner C, Auriemma E, van de Belt AJ, Gerber V. Quantitative motor unit action
potential analysis in 2 paraspinal neck muscles in adult royal dutch sport horses. Journal of Veterinary
Internal Medicine. 2011;25(3):592-597.
16. R Core Team. R: A language and environment for statistical computing. 2013.
17. IBM SPSS statistics for windows. 2013.
18. Levin KH, Maggiano HJ, Wilbourn AJ. Cervical radiculopathies: Comparison of surgical and EMG
localization of single-root lesions. Neurology. 1996;46(4):1022-1025.
19. Down SS, Henson FMD. Radiographic retrospective study of the caudal cervical articular process
joints in the horse. Equine Vet J. 2009;41(6):518-524.
20. Mitchell CW, Nykamp SG, Foster R, Cruz R, Montieth G. The use of magnetic resonance imaging in
evaluating horses with spinal ataxia. Veterinary Radiology and Ultrasound. 2012;53(6):613-620.
21. Claridge HAH, Piercy RJ, Parry A, Weller R. The 3D anatomy of the cervical articular process joints in
the horse and their topographical relationship to the spinal cord. Equine veterinary journal.
2010;42:726-731.
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