Keywords craniovertebral junction - muscle cross-sectional area - ratio of moments - cervical
spine - head-neck position
Introduction
Atlantoaxial instability (AAI) is a common condition among small breed dogs. It is
in many cases a congenital condition with the first clinical signs occurring before
the age of 1 year, whereas older dogs often show signs of AAI after trauma. The resulting
instability leads to a dorsal dislocation of the dens axis causing compression of
the cervical spinal cord. The clinical signs range from neck pain to tetraplegia and
in severe cases even respiratory paralysis and death.[1 ]
[2 ]
[3 ]
[4 ]
[5 ]
[6 ] Atlantoaxial instability is frequently diagnosed in combination with other craniovertebral
junction (CVJ) anomalies.[6 ]
The atlantoaxial joint is a pivot joint that allows the head and first cervical vertebra
to rotate around the longitudinal axis of the dens.[7 ] The surrounding ligaments, muscles and fasciae play an important role in the stabilization
of the atlantoaxial joint. The dorsal atlantoaxial ligament and the alar ligaments
prevent overrotation, while the transverse ligament limits the dorsal displacement
of the dens axis during flexion of the head.[5 ]
[8 ]
[9 ] Furthermore, the joint is stabilized by paraspinal muscles that insert on the cranial
cervical vertebrae or the occiput. They are divided in epaxial and hypaxial musculature
and most of the muscles that span the atlantoaxial joint control the movement of the
head ([Table 1 ]). They include the Musculus obliquus capitis caudalis, which has the biggest impact
on the joint and acts as its rotator.[7 ]
Table 1
Overview of considered epaxial and hypaxial musculature at the three different levels
Level
Epaxial musculature
Hypaxial musculature
1
M. longissimus capitis
M. longus capitis
M. semispinalis capitis
Mm. rectus capitis ventralis
M. rectus capitis dorsalis major
Mm. rectus capitis lateralis
M. rectus capitis dorsalis minor
M. obliquus capitis cranialis
2
M. longissimus
M. longus colli
M. spinalis et semispinalis cervicis
M. longus capitis
M. semispinalis capitis
Mm. rectus capitis ventralis
M. rectus capitis dorsalis major
Mm. rectus capitis lateralis
M. rectus capitis dorsalis minor
M. obliquus capitis cranialis
M. obliquus capitis caudalis
Mm. intertransversarii dorsales cervicis
3
M. longissimus
M. longus colli
M. spinalis et semispinalis cervicis
M. longus capitis
M. semispinalis capitis
Mm. rectus capitis ventralis
Mm. multifidi
Mm. rectus capitis lateralis
M. rectus capitis d. major
M. obliquus cap. cranialis
M. obliquus cap. caudalis
Mm. intertransversarii dorsales cervicis
The pathogenesis of AAI is still not fully understood. Many studies have shown that
a lack of ligamentous support, usually in combination with congenital malformations,
plays an important role and facilitates the dislocation of the dens.[4 ]
[8 ]
[9 ]
[10 ] The role of the musculature in the pathogenesis of AAI is yet to be evaluated as
studies about the subject are scarce. If the joint is unstable due to lack of ligamentous
support, other supportive structures such as musculature experience an increased load,
which could lead to a chronic compensatory hypertrophy of the musculature.[11 ] Quantifying the extent of hypertrophy is possible by examining the increase in cross-sectional
area of the muscle in computed tomography (CT) imaging.[12 ]
[13 ]
[14 ]
The aim of this study was to evaluate whether there is a difference in cross-sectional
paraspinal muscle surface area and ratio of moments between small breed dogs with
and without AAI using CT scans. We hypothesized that there are differences in ratio
of moments between dogs with and without AAI and that the paraspinal muscle cross-sectional
area is increased in dogs with AAI due to compensatory mechanisms and the chronicity
of the disease.
Materials and Methods
Patient Selection
Medical records of four different institutions (University of Bern Switzerland, Davies
Veterinary Specialists United Kingdom, Justus-Liebig-University Giessen Germany and
University Cardenal Herrera-CEU Spain) were retrospectively searched for toy and small
breed dogs with CT scans of the craniocervical region presented between 2009 and 2020.
Data retrieved from medical records included signalment, clinical signs and the CT
scans of the craniocervical region. Dogs with clinical signs and radiologically confirmed
AAI were assigned to the AAI-group. The control group consisted of dogs without clinical
or radiological findings of AAI or any other cervical spinal disease. Computed tomography
scans in those dogs had been performed to evaluate health issues unrelated to the
CVJ, such as rhinitis or tracheal collapse.
Regarding the age, the patients were divided into two groups; dogs ≤1 year and dogs > 1
year of age. Regarding head-neck position, the patients were divided into two categories:
extended for head-neck positions < 25 degrees and flexed for positions ≥ 25 degrees.
The angle of the head-neck position for each patient was measured according to Upchurch
and colleagues ([Fig. 1 ]).[15 ] Head-neck positions were included in our statistical analysis to avoid bias caused
by different positioning of the patients during CT.
Fig. 1 Method of measuring the angle of the head position according to Upchurch and colleagues.[15 ]
Imaging and Image Review
The CT scans were performed at different institutions without a standardized protocol.
The scans had to include the atlantooccipital joint and the first two vertebrae. If
this region was not entirely visible on the CT scans, only the available levels were
analysed. The CT scans were reviewed by a single observer, a graduated veterinarian
after training (A.M.) under the supervision of a board-certified veterinary radiologist
(C.P.) using the DICOM viewer IMPAX EE (IMPAX EE, Agfa Healthcare, Belgium). The reviewer
was blinded to group information.
Measurements
Every measurement was performed at three different anatomical levels on transverse
reconstructed CT scans in the soft tissue window. The exact position of the level
was determined on sagittal reconstructions ([Fig. 2 ]). Level 1 was defined as the connection line between basion and opisthion, traversing
across the base of the occiput (also known as the McRae's line). Level 2 was set at
the centre of the dorsal arch of the atlas. Level 3 was set at the centre of the vertebral
body of the axis. Level 2 and 3 were planned parallel to level 1 to minimize the variations
caused by obliquity. To normalize for differences in body weight and size, we used
ratios to describe muscle cross-sectional area. At each level, the following measurements
were performed on transverse reconstructed CT scans.
Fig. 2 Sagittal reconstructed computed tomography scan showing the localization of the three
different levels where measurements were performed. The blue dotted lines illustrate
which landmarks were used to determine the centre of the atlas and axis respectively.
Muscle Cross-Sectional Area Ratio (d-v-Ratio)
The paraspinal musculature was outlined using the integrated freehand tool and the
area was calculated by the DICOM viewer program. At each level, only muscle groups
that could clearly be identified on consecutive images were considered ([Table 1 ]). Cross-sectional area of the left- and right-hand side musculature was summarized
to epaxial and hypaxial musculature respectively ([Fig. 3 ]). The area ratio between the epaxial and hypaxial musculature cross-sectional area
was calculated using the following equation:
Fig. 3 Transverse reconstructed computed tomography scans of a patient from the control
(A , C , E ) and atlantoaxial instability (B , D , F ) group, respectively, at levels 1 (A and B ), 2 (C and D ) and 3 (E and F ) illustrating the cross-sectional muscle area used to calculate the d-v-ratio, the
d-C2 ratio and the v-C2 ratio.
Ratio of Epaxial and Hypaxial Muscle Cross-Sectional Area to the Height of C2 (d-C2-Ratio
and v-C2-Ratio)
To normalize muscle cross-sectional area to the size of the dog, a ratio between the
muscle cross-sectional area and the height of the vertebral body C2 was calculated.
The muscle cross-sectional area was measured as described under section ‘Muscle Cross-Sectional
Area Ratio (d-v-Ratio)’. It was set in relation to the height of the vertebral body
of C2, measured at the narrowest level of the vertebral body of C2, perpendicular
to the spinal canal. The ratio was calculated for epaxial (dorsal) and hypaxial (ventral)
musculature separately using the following formulas, resulting in two separate values:
Ratio of Moments
The ratio of dorsal-to-ventral moments was calculated as described previously by Hartmann
and colleagues[16 ] to evaluate estimated moments exerted on the dens axis. The dens is assumed to be
the centre of the force transmission in our area of interest since it works as the
central rotation point in the movement of the atlantoaxial joint. It was therefore
used as central reference point to describe the lever arms of each muscle group instead
of the centre of the intervertebral disc. Using a line parallel to the vertebral body,
the dens was projected from its anatomical localization onto the levels cranial and
caudal to the dens (level 1 and 3). If the dens was fractured or not identifiable
due to hypoplasia, the reference point was set at the location where the dens was
to be expected. According to Hartmann and colleagues, four ellipsoid models were applied
over the epaxial and hypaxial left and right muscle area. The assumptive centre of
the muscle area was assumed to be the centre of the ellipsoid models. It was determined
by fitting points to the four apexes of the ellipsoid model and by then connecting
the points with two perpendicular lines. A line was drawn from these assumptive centres
to the centre of the dens or its level respectively ([Figs. 4 ] and [5 ]).[16 ] The following formula was used to calculate the ratio of moments:
Fig. 4 Transverse reconstructed computed tomography scans with area measurements of the
epaxial (green) and hypaxial (orange) musculature at level 1 (A ), 2 (B ) and 3 (C ). (dr, dorsal right; dl, dorsal left; vr, ventral right; vl, ventral left). D : The oval shapes represent the assumptive muscle area for calculations (green for
epaxial musculature, orange for hypaxial musculature). Black lines show the distance
from the assumptive muscle centre to the approximate location of the dens axis (DR,
dorsal right; DL, dorsal left; VR, ventral right; VL, ventral left). Yellow lines
show how the assumptive centre of the musculature was measured.
Fig. 5 Transverse reconstructed computed tomography scans of a patient from the control
(A , C , E ) and atlantoaxial instability (B , D , F ) group, respectively, at levels 1 (A and B ), 2 (C and D ) and 3 (E and F ) illustrating the ratio of moments.
Statistical Analysis
All statistical analyses were performed using NCSS 2021 Statistical Software (NCSS;
LCC, Kaysville, Utah, United States). For all data, descriptive statistics were performed
and the normality of the variables was first visualized using histograms and then
tested using Shapiro–Wilk and D'Agostino-Pearson Omnibus test. To test for differences
between the groups for the four main variables (ratio of moments, dv-ratio, d-C2-ratio,
v-C2-ratio) and adjusting for age, gender and head-neck position, the multivariate
analysis of variance (MANOVA) was used. Breed could be tested for Yorkshire Terriers
only as other breeds were not sufficiently represented in our sample to test for their
influence. There was not enough data available to test for the difference between
institutions. In the final MANOVA model, we only included groups and head-neck positions
as the other variables did not show significant differences between the groups.
Additionally, in the absence of evidence of an influence of age, gender and breed
in our sample, MANOVAs for differences between the two groups (AAI and control) for
the three main variables were performed for each extended and flexed head-neck position
separately.
All analyses were performed for each level separately and the level of significance
was set at a value of p < 0.05.
Results
Computed tomography scans of a total of 83 dogs were analysed with 34 dogs in the
AAI group and 49 dogs in the control group, after excluding the datasets of 4 dogs
of the control group due to poor image quality. Twenty-six dogs from the control group
had been euthanatized for medical reasons unrelated to this study before CT examination.
In the AAI group, the most frequent breed was Yorkshire Terrier (n = 14), followed by Chihuahua (n = 10), Maltese (n = 3), Bichon Frisé (n = 1), Toy Poodle (n = 1), Miniature Pinscher (n = 1), Havanese dog (n = 1), Cavalier King Charles Spaniel (n = 1), Pug (n = 1) and Italian Greyhound (n = 1). There were 17 female and 17 male patients in the AAI group. The mean age ± standard
deviation [SD] was 3.17 ± 2.94 years. Most of the dogs (n = 27) were examined and scanned at the University of Bern and seven dogs in other
institutions (Davies Veterinary Specialists, United Kingdom (n = 3), Justus-Liebig-University Giessen, Germany (n = 1) and University Cardenal Herrera-CEU, Spain (n = 3). Fifteen dogs were scanned in flexed and 19 dogs in extended head-neck position.
In the control group, the breeds included Yorkshire Terrier (n = 18), Chihuahua (n = 16), Papillon (n = 8), Maltese (n = 2), Miniature Pinscher (n = 2), Shih Tzu (n = 2) and Japanese Chin (n = 1). Twenty-seven patients were female and 22 were male. The mean age ± SD was 5.2 ± 4.17
years. The dogs in the control group were significantly (p < 0.001) older than in the AAI group. All dogs were scanned at the University of
Bern. Eight dogs were scanned in flexed, and 41 dogs in extended head-neck position.
There was no evidence of a difference between the two age groups or the gender on
variables obtained to describe the muscle cross-sectional area, or between measurements
obtained from euthanatized dogs compared with dogs under anaesthesia.
The results of the analysis of differences between AAI and control groups adjusted
for age, gender and head-neck position are presented in [Table 2 ]. The d-v-ratio was significantly smaller in the affected dogs at level 2 (p = 0.044) and level 3 (p = 0.016). The d-C2-ratio was significantly lower in affected dogs at level 2 (p = 0.046). There was no significant difference of the v-C2-ratio between groups. The
affected dogs showed a significantly lower mean ratio of moments compared with the
control group at level 1 (p < 0.001), level 2 (p < 0.001) and level 3 (p = 0.012).
Table 2
Count (c = control / a= AAI-affected), mean and standard deviation at each level and
p -values for differences between groups as well as head-neck positions (MANOVA model
taking group and head-neck position into account)
Variable
Level
Count (c/a)
Mean ± SD control
Mean ± SD AAI
p -Value for differences between groups
p -Value for differences between head-neck positions
Dorsal-to-ventral ratio
1
49/34
4.04 ± 0.82
3.61 ± 0.70
Not significant
< 0.001
2
48/34
4.18 ± 0.79
3.39 ± 0.71
0.044
< 0.001
3
47/28
3.55 ± 0.56
3.07 ± 0.54
0.016
< 0.001
Dorsal muscle CSA to height of C2
1
48/33
143.42 ± 60.04
120.54 ± 47.24
Not significant
0.011
2
47/33
163.88 ± 66.19
124.55 ± 44.54
0.046
Not significant
3
46/27
258.12 ± 126.31
220.59 ± 73.99
Not significant
Not significant
Ventral muscle CSA to height of C2
1
48/33
35.67 ± 14.70
33.45 ± 9.78
Not significant
Not significant
2
47/33
40.24 ± 16.84
36.78 ± 9.42
Not significant
Not significant
3
46/27
73.13 ± 35.02
72.06 ± 19.60
Not significant
Not significant
Ratio of moments
1
49/34
7.83 ± 2.43
4.40 ± 2.04
< 0.001
< 0.001
2
48/34
7.24 ± 1.95
4.04 ± 1.75
< 0.001
< 0.001
3
47/28
5.07 ± 1.14
4.21 ± 1.03
0.012
0.012
Abbreviations: AAI, atlantoaxial instability; CSA, cross-sectional area; MANOVA, multivariate
analysis of variance; SD, standard deviation.
Note: Cross-sectional area is referred to as CSA. p -values >0.05 are not shown.
The influence of the head-neck position was significant for the ratio of moments at
all levels (p < 0.001, p < 0.001 and p = 0.012 respectively) as well as for d-v-ratio (p < 0.001 for all levels). It showed significance for d-C2-ratio at level 1 (p = 0.011), but not for level 2, at which the difference between groups for d-C2-ratio
was significant.
The results of the separate analysis for the extended and flexed head-neck position,
respectively, are presented in [Tables 3 ] and [4 ]. The d-C2-ratio showed a significant decrease for dogs with AAI at level 2 (p = 0.046) in flexed head-neck position. The ratio of moments was significantly lower
for dogs with AAI in both extended and flexed head-neck position at level 1 (p < 0.001 for both) and level 2 (p < 0.001 and p = 0.008 respectively). No significant differences between groups in all other measurements
of the muscle area ratios were detected when head-neck positions were analysed separately.
Table 3
Count (c = control / a= AAI-affected), mean and standard deviation at each level and
p -values for differences between groups in flexed head position (MANOVA model with
group only)
Variable
Level
Count (c/a)
Mean ± SD control
Mean ± SD AAI
p -Value for differences between groups
Dorsal-to-ventral ratio
1
8/15
3.46 ± 0.61
3.23 ± 0.61
Not significant
2
7/15
3.47 ± 0.99
2.83 ± 0.57
Not significant
3
7/10
3.33 ± 0.62
2.67 ± 0.43
Not significant
Dorsal muscle CSA to height of C2
1
8/14
115.17 ± 20.60
92.71 ± 17.93
0.046
2
7/14
151.99 ± 49.28
94.26 ± 20.40
Not significant
3
7/9
209.91 ± 51.17
173.76 ± 31.33
Not significant
Ventral muscle CSA to height of C2
1
8/14
34.09 ± 8.24
30.13 ± 7.13
Not significant
2
7/14
45.82 ± 17.46
34.54 ± 5.96
Not significant
3
7/9
64.84 ± 19.90
67.64 ± 13.86
Not significant
Ratio of moments
1
8/15
6.74 ± 2.25
3.17 ± 1.61
0.001
2
7/15
5.68 ± 2.20
2.81 ± 1.46
0.008
3
7/10
4.82 ± 1.54
3.43 ± 0.79
Not significant
Abbreviations: AAI, atlantoaxial instability; CSA, cross-sectional area; MANOVA, multivariate
analysis of variance; SD, standard deviation.
Note: p -Values >0.05 are not shown.
Table 4
Count (c = control / a= AAI-affected), mean and standard deviation at each level and
p -values for differences between groups in extended head position (MANOVA model with
group only)
Variable
Level
Count (c/a)
Mean ± SD control
Mean ± SD AAI
p -Values
Dorsal-to-ventral ratio
1
41/19
4.16 ± 0.81
3.91 ± 0.64
Not significant
2
41/19
4.28 ± 0.72
3.83 ± 0.44
Not significant
3
40/18
3.59 ± 0.56
3.30 ± 0.47
Not significant
Dorsal muscle CSA to height of C2
1
40/19
137.92 ± 38.07
141.04 ± 51.86
Not significant
2
40/19
155.09 ± 48.51
146.85 ± 44.58
Not significant
3
39/18
241.76 ± 77.97
244.00 ± 78.55
Not significant
Ventral muscle CSA to height of C2
1
40/19
33.06 ± 8.44
35.89 ± 10.88
Not significant
2
40/19
36.86 ± 12.47
38.43 ± 11.20
Not significant
3
39/18
67.63 ± 21.94
74.26 ± 21.94
Not significant
Ratio of moments
1
41/19
8.08 ± 2.48
5.36 ± 1.83
< 0.001
2
41/19
7.49 ± 1.86
5.01 ± 1.29
< 0.001
3
40/18
5.12 ± 1.10
4.64 ± 0.89
Not significant
Abbreviations: AAI, atlantoaxial instability; CSA, cross-sectional area; MANOVA, multivariate
analysis of variance; SD, standard deviation.
Note: p -Values >0.05 are not shown.
As supplementary material, the absolute measures of the epaxial (dorsal) and hypaxial
(ventral) muscle area measurements are presented in [Supplementary Table S1 ] (online only).
Discussion
This study compared cross-sectional paraspinal muscle surface area and ratio of moments
of small breed dogs with and without AAI using CT scans with the aim to evaluate the
role of the paraspinal musculature in AAI.
The ratio of moments showed a significant decrease in dogs with AAI at all levels.
Analysing the flexed and extended head-neck positions separately, the ratio of moments
was significantly lower for dogs with AAI at level 1 (Occiput/C1) and 2 (mid-C1).
This may be explained by the dorsal luxation of the axis and/or dorsal angulation
of the dens due to disruption of the ligaments of the atlantoaxial joint.[8 ]
[9 ] The dorsal dislocation of the dens axis as the central reference point of forces
leads to a decreased length of the lever arms of the epaxial musculature and increased
length of the ventral musculature resulting in a lower ratio of moments. The d-v-ratio
was significantly lower in dogs with AAI at level 2 (mid-C1) and 3 (mid-C2). Interpreted
in combination with the d-C2-ratio, which was significantly smaller in affected dogs
at level 2, the results indicate a decrease in epaxial musculature cross-sectional
area in dogs with AAI. However, when analysing head-neck positions separately, a significantly
lower d-C2-ratio was observed at level 2 in a flexed head-neck position only. Therefore,
our hypothesis of an increased paraspinal muscle cross-sectional area in dogs with
AAI due to compensatory hypertrophy is not supported.
To our knowledge, no previous studies have assessed the changes in paraspinal musculature
cross-sectional area around the atlantoaxial joint in small breed dogs with AAI. Literature
on the topic is limited. A theory for the lack of compensatory mechanisms or increase
in paraspinal musculature cross-sectional area was found in human literature. A similar
situation occurs in patients with acute and chronic low back pain, where instability
of the lumbar spine plays a role in the pathogenesis.[17 ] In acute low back pain, there is evidence of a reduction in cross-sectional area
for the multifidus muscle.[18 ]
[19 ] The mechanism seems to be of neural origin, where reduced muscle activation leads
to disuse and therefore atrophy of the muscle. In an experimental study in pigs, it
was shown that atrophy after disc lesions occurs as early as 3 days after injury.[20 ] In subacute or chronic low back pain, muscle atrophy tends to recover to a certain
degree but structural inflammatory-related changes such as fibrosis, fatty infiltration
and slow-to-fast muscle fibre transition are commonly described. However, only the
multifidus muscle showed a consistent decrease in cross-sectional area. Similar to
our study, results for the other muscles varied and did not show final evidence of
a measurable change in muscle cross-sectional area.[18 ]
Whether the pathogenesis of AAI in patients in our study was acute or chronic remains
unknown. Despite the usually acute clinical onset, changes such as distended or missing
atlantoaxial ligaments make a chronic course of the disease likely, which is also
assumed to be the case for the patients in our study. One sign consistent with an
acute event is a longitudinal tear in the tectorial membrane.[21 ] The tectorial membrane is formed by the fibrous layer of the joint capsule and extends
dorsally between the arch of the atlas and the axis as the dorsal atlantoaxial membrane.[9 ] In our CT scan-based study, the tectorial membrane could not be evaluated. A prospective
study of AAI cases with repetitive magnetic resonance imaging studies would be necessary
to draw conclusions on imaging-based evaluation of an acute or chronic pathogenesis
of AAI and the evolution of muscle cross-sectional area and composition over time.
The head-neck position was an important factor for both the measurement of the ratio
of moments and the muscle cross-sectional area ratios. Results for the multivariate
analysis showed a significant influence of the head-neck position on the ratio of
moments and d-v-ratio at all levels and d-C2-ratio at level 1. This supports the results
of a recent study, which has shown the importance of standardized head-neck positioning
for diagnostic imaging of the CVJ.[22 ] If the head-neck positions were analysed separately, a significantly decreased d-C2-ratio
was observed at level 2 in a flexed head-neck position. This observation may be indicating
a lower epaxial muscle cross-sectional area due to excessive stretching of the dorsal
muscle segment in dogs with an unstable atlantoaxial transition rather than a true
atrophy. In addition, the sample size of dogs in flexed head position (affected and
control) was rather small and might have affected the validity of these results. For
future studies examining the musculature of the cranial cervical spine, it is advisable
to use a standardized head-neck position.
When considering the statistical results of the three different levels, it becomes
evident that most of the significant changes are shown at level 1 and 2. These levels
are measured at the McRae line and centrally in the dorsal arch of the atlas, respectively,
and therefore closest to the centre of forces. At level 3, most variables show no
or only little significance. In human lower back pain, a similar effect can be seen.
Changes in musculature cross-sectional area shortly after a disc injury in the lumbar
spine area occur mostly at the affected segment and become generalized after many
months only.[18 ]
[20 ]
The success of AAI therapy depends on the formation of fibrous connective tissue around
the atlantoaxial joint, especially when a conservative approach, such as external
stabilization and cage rest, is chosen.[4 ]
[23 ]
[24 ] Muscle strengthening as well is a suggested therapy option in dogs with AAI, and
understanding factors such as development of muscle atrophy, or imbalance of strength
between epaxial and hypaxial muscles could help to further guide therapy.
There are several limitations to this study, mostly due to its retrospective nature.
First, the distribution of the patients' age was not matched. Age affects muscle mass
and muscle quality in older dogs. They show muscle loss and an increased fat content
of the musculature as compared with younger dogs.[25 ] Yet the significance of the results remained unchanged when the age was taken into
account in the statistical analysis. No standardized imaging protocol was used in
this multicentre study. The main issue arising from this shortcoming is the variability
in head-neck positioning and its possible influence on the CVJ. To address this issue,
we included the factor head-neck-position in our statistical analysis.
The choice of analysing CT scans was made due to CT being a reliable tool for the
evaluation of paraspinal musculature cross-sectional area and ratio of moments along
with the availability of a larger number of patients.[14 ]
[16 ]
[26 ] For future research, it might be of interest to analyse the composition and quality
of the musculature as well, preferably in magnetic resonance imaging studies. Increased
fat content of the musculature is a common finding in dogs as well as humans with
chronic spinal disease and it is likely that dogs with AAI have lower quality musculature
as well.[18 ]
[27 ] Evaluating this might provide interesting insights into management options and possibly
highlight the importance of muscle strengthening further.
In conclusion, our study showed that the role of musculature in the pathogenesis of
AAI is limited. We could not demonstrate a consistent change in paraspinal musculature
cross-sectional area for small breed dogs with AAI compared with unaffected individuals,
but instead confirm an altered ratio of moments in those dogs in the area of the atlantoaxial
joint. The study further emphasizes the importance of standardized imaging protocols
including standardized head-neck position when examining the CVJ.
