Craniocervical junction abnormality is a general term for a malformation (CLM,1–5,a atlantooccipital instability,6,7 atlantoaxial instability,8–10 occipitoatlantoaxial malformation,11,b AOO,12 and DA13–15) that occurs in the craniocervical region of small-breed dogs. These CJAs are common and clinically challenging disorders.1,10,11,14,15 The CLM, which is analogous to Chiari type I malformation in humans, is a cause of major health problems in small-breed dogs and most commonly affects CKCSs.2–5,16–19,a The term CLM is commonly used in the veterinary medical field to denote disorders causing neural tissue constriction at the cervicomedullary junction, as detected via MR imaging. Most definitions of CLM include a statement that the presence of an abnormally shaped supraoccipital bone results in rostrally directed compression of the caudal aspect of the cerebellum. It is often difficult or impossible to determine what structure or structures are causing CC by evaluating MR images because the visualization of bone in MR images is poor. In dogs, rostral compression of the cerebellum detected by evaluation of MR images is often attributed to a malformed supraoccipital bone and such cases are given a diagnosis of CLM. With regard to a CJA in humans known as basilar invagination, a rostrally displaced C1 dorsal arch can cause CC20,21; AOO is a similar condition in dogs.10 Computed tomography is often performed in addition to MR imaging in humans with CJAs to determine what structures are causing neural tissue compression.20,21 Similarly, we routinely perform CT immediately following MR imaging in dogs with CJAs.
It is difficult to interpret morphological abnormalities of the cranial cavity and to relate these abnormalities to intracranial and vertebral column diseases because of the wide variation in skull size and shape in small-breed dogs. Additionally, concurrent neural disease is commonly identified in dogs undergoing imaging because of CLM.1,5,10,14,18,22,a Concurrent neural disease is also commonly identified in humans with Chiari type I malformation23,24 and is thought to contribute to a poor outcome in patients undergoing foramen magnum decompression for treatment of the malformation.25,26
Techniques have been reported that use linear and 3-D measurements of MR and CT images to determine total brain volume, total cranial volume, and cranial and caudal fossa volumes.1,27–29 Studies have identified positive associations between the caudal fossa volume-to-total cranial volume ratio and neurologic signs,1 between volume ratios and linear measurements,28 and between decreased caudal fossa volume and syringomyelia.27 Other investigators found that there is no association between decreased caudal fossa volume and syringomyelia.1,29
In our experience, evaluation of MR images of dogs being screened because of suspected CLM commonly reveals CC (defined as an indentation of the cerebellum19), MK (defined as an elevation of the medulla at the cervicomedullary junction caused by the dens4,11–13,19), and DC (ie, DC of the spinal cord at C1–C21,a). Several studies have attempted to determine whether there is an association between CC,1,27,29,30 MK,1,30 or DC1,a and clinical signs or syringomyelia in dogs. However, these studies have had low case numbers and provided conflicting results. To the authors' knowledge, associations among CC, MK, and DC in dogs have not been examined in a large-scale study. Furthermore, the presence of AOO as either a primary or a comorbid disease in dogs evaluated because of suspected CLM has not been investigated. The purpose of the study reported here was to quantify CC, MK, and DC in dogs that underwent MR imaging and CT because of suspected CLM and to report associations between CC, MK, or DC and the presence of other CJAs.
Materials and Methods
Animals—Two hundred seventy-four dogs were included in the study. Owner consent for inclusion of patient data in this clinical study was obtained in all cases. Recruitment of CKCSs was accomplished by advertising a low-cost screening program for detection of CLM to CKCS breed clubs in the United States during 2007 through 2010. Screening for detection of CLM was performed at The Canine Chiari Institute at Long Island Veterinary Specialists. Additionally, dogs of breeds other than CKCS that had been evaluated by the neurology service at Long Island Veterinary Specialists and in which CLM had been diagnosed on the basis of MR imaging were included in this study. Only dogs that had CLM as determined by observation of CC on MR images were included.
Procedures and imaging—A neurologic examination, CBC, and serum biochemical analysis were performed at Long Island Veterinary Specialists on all dogs within 14 days before participation in the study. A detailed history for each dog was obtained from its owner. Each dog was premedicated with butorphanol tartrate (0.2 mg/kg, IV) and atropine sulfate (0.08 mg/kg, IV). Anesthesia was induced with propofol (11 mg/kg, IV) and maintained with isoflurane in oxygen. Mean arterial blood pressure, end-tidal CO2 concentration, ventilatory rate, esophageal temperature, and heart rate were monitored, and values were maintained within physiologic limits during the anesthetic episode. All dogs underwent cervical radiography, MR imaging,c and CT.d
Magnetic resonance images of the brain and spinal cord of each dog were acquired by use of an MR scanner with a 3.0-T magnet.c Each dog was placed in dorsal recumbency with the neck in partial flexion (between 100° and 138°) to approximate the craniocervical angle in standing CKCSs as previously described.31 Sagittal T2-weighted, axial T2-weighted, and axial T1-weighted fluid-attenuated inversion recovery images of the brain were acquired in each dog. Axial T2-weighted images of the cervical, thoracic, and lumbar regions were acquired in each dog.
Computed tomographic images of the head and cranial vertebral column including C3 were acquired by use of a multidetector CTd operating at 140 kV and 150 mA; a bone reconstruction filter was used during image acquisition. Dogs were placed in sternal recumbency with the neck in partial flexion (between 100° and 138°). Contiguous 1-mm collimated images were obtained by use of helical acquisition. Images were interpreted by use of a bone algorithm (window width, 3,000 Hounsfield units; window length, 500 Hounsfield units) and 3-D reconstruction.
All CT and MR images were reviewed by 2 of the authors (DJM and CAL). Compression was defined as indentation of the subarachnoid space or neural parenchyma by adjacent soft tissue or bone. The CL for each anatomic location of compression (CC, MK, and DC) was determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression on MR images. A compression index was calculated for CC, MK, and DC to account for size differences among dogs. Compression indices for MK and DC were calculated by dividing CL at those locations by the diameter of the adjacent normal portion of the cervical spinal cord and subarachnoid space (distance between 2 parallel lines placed at the outer limit of the subarachnoid space adjacent to the site of compression) and multiplying by 100 (Figures 1 and 2). The compression index for CC was calculated by dividing CL, determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression, by the diameter of a circle placed over the widest part of the cerebellum and multiplying by 100 (Figure 3). A diagnosis of AOO was confirmed by evaluation of 3-D reconstructed CT images as previously described10 (Figure 4).
Representative sagittal T2-weighted MR image of the head and cranial cervical region of a dog with CLM illustrating measurements for determination of the MK index. Medullary kinking was defined as an elevation of the medulla at the cervicomedullary junction caused by the dens. The MK index was calculated by dividing CL, determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression, by the diameter (D) of the adjacent normal portion of the cervical spinal cord and subarachnoid space and multiplying by 100.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.105
Representative sagittal T2-weighted MR image of the head and cranial cervical region of a dog with CLM illustrating measurements for determination of the DC (ie, DC of the spinal cord at C1–C2) index. The DC index was calculated by dividing CL, determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression, by the diameter (D) of the adjacent normal portion of the cervical spinal cord and subarachnoid space and multiplying by 100.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.105
Representative sagittal T2-weighted MR image of the head and cranial cervical region of a dog with CLM illustrating measurements for determination of the CC index. Cerebellar compression was defined as an indentation of the cerebellum. The CC index was calculated by dividing CL, determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression, by the diameter (D) of a circle placed over the widest part of the cerebellum and multiplying by 100.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.105
Representative 3-D reconstructed CT images of the head and cranial cervical region of 2 anesthetized dogs with CLM. A—Image of a dog with AOO. Notice that the cranial aspect of the C1 vertebral body is located partially within the cranium. B—Image of a dog with normal atlantooccipital articulation. In both images, the endotracheal tube is visible.
Citation: American Journal of Veterinary Research 73, 1; 10.2460/ajvr.73.1.105
Statistical analysis—Prior to conducting the primary statistical analyses, intraobserver and interobserver reliabilities of the compression index calculations were determined. A sagittal T2-weighted MR image of the head and cranial cervical region of each of 15 dogs was randomly selected; each investigator (DJM and CAL) independently calculated the CC, MK, and DC indices for each dog on 2 separate occasions; and intraobserver and interobserver intraclass correlations were determined by use of a statistical software program.e The investigators were blinded to the patient's identity on each occasion.
Univariable and multiple logistic regression analysese were used to calculate the probability of other CJAs as a function of breed (CKCS vs non-CKCS dogs) and the specific predictors (CC index, presence of MK, and presence of DC). The MK and DC indices were used for the purpose of determining presence or absence of compression. The degree of compression was not compared with other findings.
Receiver operating characteristic curves were computed for each predictor for CKCSs and non-CKCS dogs separately. To find an optimal cutoff point (ie, a value above which the compression type would be classified as AOO), the Euclidean distance from the best receiver operating characteristic point (0, 1) to the ordered pair (1 − specificity, sensitivity) corresponding to each value of the selected predictor was calculated. The value of the predictor corresponding to the shortest distance was used as the optimal cutoff point.32 Values of P < 0.05 were considered significant.
Results
Two hundred seventy-four dogs were included in the study; 216 (78.8%) were CKCSs and 58 (21.2%) were non-CKCS dogs. Non-CKCS dog breeds included Yorkshire Terrier (n = 15), Chihuahua (11), Maltese (7), Pomeranian (4), Pug (3), Boston Terrier (3), Miniature Poodle (3), Shih-Tzu (2), mixed (2), Beagle (1), Affenpinscher (1), Brussels Griffon (1), French Bull Dog (1), Maltese-Poodle cross (1), Miniature Dachshund (1), Papillon (1), and Tibetan Spaniel (1). Among the 274 dogs, there were 119 (43.4%) males and 155 (56.6%) females. The median age was 21 months (range, 5 to 132 months) and the median weight was 7.3 kg (range, 1.4 to 16.8 kg).
All dogs had some degree of CC. Among the 274 dogs, there were 187 (68.2%) dogs with concurrent MK and 104 (38.0%) with concurrent DC. Based on evaluation of 3-D reconstructed CT images, 76 of 274 (27.7%) dogs with CC had AOO. Atlantooccipital overlapping was found in 44 of 216 (20.4%) CKCSs and 32 of 58 (55.2%) non-CKCS dogs.
Intraobserver reliability for the DC and MK indices ranged from 0.94 to 0.99, indicating outstanding reliability with repetition. Intraobserver reliability for the CC index ranged from 0.51 to 0.74. Similarly, interobserver reliabilities for the DC and MK indices (range, 0.93 to 0.99) were higher than that for the CC index (range, 0.52 to 0.70).
Univariable logistic regression analysis revealed that non-CKCS breed (P < 0.001) and CC index (P < 0.003) were significantly associated with AOO, but the presence of DC (P = 0.251) and MK (P < 0.141) was not. Similarly, multiple logistic regression analysis involving all 4 predictor variables (breed classification, CC index, and presence of MK or DC) revealed that non-CKCS breed (P < 0.001) and CC index (P < 0.009) were jointly significant as predictors of AOO (Table 1). When the final logistic regression equation was revised to include only breed classification and AOO, CKCSs had an approximately 5-fold decrease in risk of AOO, compared with non-CKCS dogs (P < 0.001; odds ratio, 0.208), and the risk of AOO increased by a factor of 1.07 for every 1% increase in the CC index (ie, for every 10% increase in CC index, the risk of AOO nearly doubled [1.079 = 1.97]). This model was used to compute predicted probabilities of AOO (Table 2), and optimal cutoff points were determined for the prediction of AOO on the basis of the CC index. A CKCS was classified as having AOO if the CC index was > 16.1%; a non-CKCS dog was classified as having AOO if CC index was > 12.3%.
Results of multiple logistic regression analysis of data obtained from 216 CKCSs and 58 non-CKCS dogs used to calculate the probability of AOO as a function of breed (CKCS vs non-CKCS), CC index, and the presence of DC (ie, DC of the spinal cord at C1–C2) or MK.
| Effect | Estimate | SE | P value | Odds ratio | 95% Wald confidence limits |
|---|---|---|---|---|---|
| Intercept | −0.8938 | 0.5612 | 0.111 | — | — |
| CKCS vs non-CKCS | −1.6530 | 0.3539 | < 0.001 | 0.191 | 0.096–0.383 |
| DC (present vs absent) | −0.2859 | 0.3233 | 0.377 | 0.751 | 0.399–1.416 |
| MK (present vs absent) | 0.1742 | 0.3241 | 0.591 | 1.190 | 0.631–2.247 |
| CC index | 0.0686 | 0.0263 | 0.009 | 1.071 | 1.017–1.128 |
Medullary kinking was defined as an elevation of the medulla at the cervicomedullary junction caused by the dens. Cerebellar compression was defined as an indentation of the cerebellum, and the CC index was calculated by dividing CL, determined by measuring the distance from the outer limit of the subarachnoid space to the point of greatest neural compression, by the diameter of a circle placed over the widest part of the cerebellum and multiplying by 100. Each effect had 1 df.
— = Not applicable.
Predicted probabilities of AOO for CKCSs and non-CKCS dogs at various values of CC index.
| CC index (%) | CKCS | Non-CKCS |
|---|---|---|
| 5 | 0.1037 | 0.3568 |
| 10 | 0.1395 | 0.4374 |
| 20 | 0.2415 | 0.6043 |
| 30 | 0.3847 | 0.7500 |
| 40 | 0.5511 | 0.8549 |
| 50 | 0.7069 | 0.9204 |
Probabilities were calculated on the basis of data obtained from 216 CKCSs and 58 non-CKCS dogs.
See Table 1 for remainder of key.
Discussion
The presence of 1 or more CJAs in dogs with suspected CLM1,5,10,11,14,19,22,a and in people with Chiari malformation23–26 has been reported. To our knowledge, the detection of multiple areas of neural tissue compression in dogs with CLM in a large-scale study has not been reported. Because the present study enrolled dogs with suspected CLM, all dogs had some degree of CC; 187 of 274 (68.2%) dogs had concurrent MK, and 104 of 274 (38.0%) dogs had concurrent DC. In addition, 76 of 274 (27.7%) dogs with CC had AOO rather than CLM; CC was caused by C1 vertebral body impingement rather than supraoccipital bone impingement in these dogs. These findings underscore the need for thorough diagnostic evaluation, including MR imaging and CT, to completely assess the magnitude and complexity of CJAs in dogs with suspected CLM. Failure to address concurrent CJAs in humans undergoing surgery for Chiari malformation can result in suboptimal outcomes.25,26 We suspect that this is also true in dogs with suspected CLM that are surgically treated. The relationships between various CJAs and Chiari malformations in humans have been described in detail.21,25,33–35 Several authors have speculated that relationships exist between CC, MK, or DC and AOO in dogs1,10,11,14; however, the relationships have not been reported.
The breeds and median weight of dogs in the present study were consistent with those in previous studies,1,3–5,10,18,36,a suggesting that CJAs predominantly affect small-breed dogs. The number of CKCSs in the present study was disproportionately high because recruitment was targeted toward CKCS breed clubs. Therefore, these results cannot be used to determine prevalence of CJAs in CKCSs.
In the present study, results of both univariable and multiple logistic regression analyses indicated that non-CKCS breed and CC index were significantly associated with AOO. Optimal cutoff points for the prediction of AOO based on the CC index were determined in this study. A CKCS was classified as having AOO if the CC index was > 16.1%; a non-CKCS dog was classified as having AOO if the CC index was > 12.3%. The impact of AOO on the treatment outcome of dogs undergoing surgery because of CLM was not determined in this study; however, the effect of AOO on caudal fossa overcrowding should be considered when generating a treatment plan for those patients. In humans, basilar invagination, which is analogous to AOO in dogs, has been reported to exacerbate overcrowding of the posterior fossa in patients with Chiari malformation.37
In the present study, 187 of 274 (68.2%) dogs with CLM had MK. Dorsal position of the dens causing spinal cord compression in dogs with CLM has been reported1,11 and was detected in 66% of 64 dogs evaluated in a recent study.1 In 1 study,26 96 of 364 (26.4%) humans with Chiari malformation had DA. In another study,38 females with Chiari malformation were more commonly affected with DA. In humans, kinking of the brain stem that is secondary to DA alters the dynamics of CSF and the local flow of blood; this causes compression myelopathy and results in development of various clinical signs attributable to brainstem compression.25,26,39 Several reports40–43 stress the importance of stretch-related myelopathy in the development of clinical signs. Stretching of the axolemma may result in the loss of microtubules and neurofilaments, loss of axonal transport, and an accumulation of axoplasmic material known as a retraction ball.40–46 Axon retraction balls, also known as axon bulbs, develop as a result of stretch injuries associated with basilar invagination40–42,47 and abusive head trauma (shaken baby syndrome).48,49 Current treatment recommendations for humans with Chiari malformation and concurrent MK include decompression of the MK via ventral cervical vertebral fusion, which restores the clivoaxial angle and lessens or eliminates the tractional injury to the cervical spinal cord, followed by foramen magnum decompression.50
In the present study, 104 of 274 (38.0%) dogs with CLM had DC. Dorsal compression of the spinal cord at the C1–2 intervertebral space in dogs with CJAs has been reported.1,2,5,10,51,52 Although the exact cause has not been established, lymphocytic or plasmacytic inflammation, fibrosis, and ossification of the soft tissues have been observed during histologic evaluation of dural biopsy samples from the affected regions.1,2 In our experience, the DC is best visualized on sagittal T2-weighted images of the craniocervical junction. Dorsal compression may represent hypertrophy (of the ligamentum flavum or dura) or osseous compression (secondary to malformation or vertebral body malarticulation), and it may be caused by different mechanisms in CKCSs versus other small-breed dogs. This was suggested by the finding in the present study that there is a lower risk of AOO in CKCSs, compared with non-CKCS dogs. Malarticulations between the occipital condyles, atlas, and axis appear to contribute to DC at the C1–2 intervertebral space. The importance of DC and its impact on clinical outcome is unknown at this time. It is reasonable to assume that DC can have detrimental effects via the same mechanisms that are responsible for pathological sequelae of other CJAs, such as compression of axons and disturbance of normal flow of CSF and blood. When DC is identified in dogs with CLM, further diagnostic testing should be considered to detect AOO. Additional diagnostic testing, including CT, has been recommended in dogs with AOO to determine the extent of disease and formulate a comprehensive treatment plan.10
For dogs with CJAs, it is recommended that diagnostic imaging be performed in multiple neck positions ranging from mild extension to mild flexion because CJAs are typically dynamic lesions.10 In the present study, dogs were placed in dorsal (MR imaging) or sternal (CT) recumbency with the neck in partial flexion (between 100° and 138°), which approximated the craniocervical angle in standing CKCSs; multiple neck positions were not used. This study limitation may have affected the accurate detection of CJAs. However, the prolonged time required when multiple neck positions are used during MR imaging and CT may preclude clinical application of this technique.
For dogs with suspected CLM examined in the present study, CC, MK, and DC were detected via MR imaging and respective compression indices were calculated. Only CC index and breed (CKCS vs non-CKCS breeds) were significant predictors of AOO. Cavalier King Charles Spaniels had an approximately 5-fold decrease in the risk of AOO, compared with non-CKCS dogs, and for every 10% increase in CC index, the risk of AOO nearly doubled.
ABBREVIATIONS
| AOO | Atlantooccipital overlapping |
| CC | Cerebellar compression |
| CJA | Craniocervical junction abnormality |
| CKCS | Cavalier King Charles Spaniel |
| CL | Compression length |
| CLM | Chiari-like malformation |
| CT | Computed tomography |
| DA | Dens abnormality |
| DC | Dorsal compression |
| MK | Medullary kinking |
| MR | Magnetic resonance |
Dewey CW, Berg JM, Barone G, et al. Treatment of caudal occipital malformation syndrome in dogs by foramen decompression (abstr). J Vet Intern Med 2005;19:418.
Petite A, McConnell F, De Stefani A, et al. Congenital occipito-atlanto-axial malformation in five dogs (abstr). Vet Radiol Ultrasound 2009;50:118.
Achieva 3.0-T MR imaging unit, Philips, Andover, Mass.
Marconi Mx8000, Marconi Medical Systems Inc, Cleveland, Ohio.
SAS, version 9.2, SAS Institute Inc, Cary, NC.
References
- 1.↑
Cerda-Gonzalez S, Olby NJ, McCullough S, et al. Morphology of the caudal fossa in Cavalier King Charles Spaniels. Vet Radiol Ultrasound 2009; 50:37–46.
- 2.
Dewey CW, Berg JM, Barone G, et al. Foramen magnum decompression for treatment of caudal occipital malformation syndrome in dogs. J Am Vet Med Assoc 2005; 227:1270–1275.
- 3.
Dewey CW, Marino DJ, Bailey KS, et al. Foramen magnum decompression with cranioplasty for treatment of caudal occipital malformation syndrome in dogs. Vet Surg 2007; 36:406–415.
- 4.
Dewey CW, Barone G, Stefanacci JD, et al. Caudal occipital malformation syndrome in dogs. Compend Contin Educ Pract Vet 2004; 26:886–895.
- 5.
Rusbridge C. Chiari-like malformation with syringomyelia in the Cavalier King Charles Spaniel: long-term outcome after surgical management. Vet Surg 2007; 36:396–405.
- 6.
McCarthy RJ, Hosgood G. Atlantoaxial subluxation in dogs. Compend Contin Educ Pract Vet 1995; 17:215–227.
- 7.
Wheeler SJ. Atlantoaxial subluxation with absence of dens in a Rottweiler. J Small Anim Pract 1992; 33:90–93.
- 8.
LeCouteur RA, McKeown D, Johnson J, et al. Stabilization of atlantoaxial subluxation in the dog, using the nuchal ligament. J Am Vet Med Assoc 1980; 177:1011–1017.
- 9.↑
Watson AG, de Lahunta A, Evans HE. Morphology and embryological interpretation of a congenital occipito-atlanto-axial malformation in a dog. Teratology 1988; 38:451–459.
- 10.↑
Cerda-Gonzalez S, Dewey CW, Scrivani PV. Imaging features of atlanto-occipital overlapping in dogs. Vet Radiol Ultrasound 2009; 50:264–268.
- 11.↑
Bynevelt M, Rusbridge C, Britton J. Dorsal dens angulation and a Chiari type malformation in a Cavalier King Charles Spaniel. Vet Radiol Ultrasound 2000; 41:521–524.
- 12.↑
Ladds P, Guffy M, Blauch B, et al. Congenital odontoid process separation in two dogs. J Small Anim Pract 1971; 12:463–471.
- 13.
Parker AJ, Park RD, Cusick PK. Abnormal odontoid process angulation in a dog. Vet Rec 1973; 93:559–561.
- 14.
Cerda-Gonzalez S, Dewey CW. Congenital diseases of the craniocervical junction in the dog. Vet Clin North Am Small Anim Pract 2010; 40:121–141.
- 15.
Gibson KL, Hogan PM. Severe spinal cord compression caused by a dorsally angulated dens. Prog Vet Neurol 1995; 6:55–57.
- 16.
Rusbridge C, Jeffery ND. Pathophysiology and treatment of neuropathic pain associated with syringomyelia. Vet J 2008; 175:164–172.
- 17.
Rusbridge C, Knowler P, Rouleau GA, et al. Inherited occipital hypoplasia/syringomyelia in the Cavalier King Charles Spaniel: experiences in setting up a worldwide DNA collection. J Hered 2005; 96:745–749.
- 18.
Rusbridge C, Knowler SP, Pieterse L, et al. Chiari-like malformation in the Griffon Bruxellois. J Small Anim Pract 2009; 50:386–393.
- 19.↑
Rusbridge C, MacSweeny JE, Davies JV, et al. Syringohydromyelia in Cavalier King Charles Spaniels. J Am Anim Hosp Assoc 2000; 36:34–41.
- 20.
Botelho RV, Neto EB, Patriota GC, et al. Basilar invagination: craniocervical instability treated with cervical traction and occipitocervical fixation. Case report. J Neurosurg Spine 2007; 7:444–449.
- 21.
Goel A, Bhatjiwale M, Desai K. Basilar invagination: a study based on 190 surgically treated patients. J Neurosurg 1998; 88:962–968.
- 22.
Dewey CW, Cerda-Gonzalez S, Scrivani PV, et al. Surgical stabilization of a craniocervical junction abnormality with atlanto-occipital overlapping in a dog. Compend Contin Educ Pract Vet 2009; 31:E1–E6.
- 23.
Schady W, Butler P. The incidence of craniocervical bony anomalies in the adult Chiari malformation. J Neurol Sci 1987; 82:193–203.
- 24.
Levy LJ, Hahn JF. Chiari malformation presenting in adults: a surgical experience in 127 cases. Neurosurgery 1983; 1983:377–389.
- 25.
Grabb PA, Mapstone TB, Oakes WJ. Ventral brain stem compression in pediatric and young patients with Chiari I malformations. Neurosurgery 1999; 44:520–527.
- 26.↑
Milhorat TH, Chou MW, Trinidad EM, et al. Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 1999; 44:1005–1017.
- 27.↑
Carrera I, Dennis R, Mellor DJ, et al. Use of magnetic resonance imaging for morphometric analysis of the caudal cranial fossa in Cavalier King Charles Spaniels. Am J Vet Res 2009; 70:340–345.
- 28.↑
Garcia-Real I, Kass PH, Sturges BK, et al. Morphometric analysis of the cranial cavity and caudal cranial fossa in the dog: a computerized tomographic study. Vet Radiol Ultrasound 2004; 45:38–45.
- 29.
Schmidt MJ, Biel M, Klumpp S, et al. Evaluation of the volumes of cranial cavities in Cavalier King Charles Spaniels with Chiari-like malformation and other brachycephalic dogs as measured via computed tomography. Am J Vet Res 2009; 70:508–512.
- 30.
Lu D, Lamb CR, Pfeiffer DU, et al. Neurological signs and results of magnetic resonance imaging in 40 Cavalier King Charles Spaniels with Chiari type 1-like malformations. Vet Rec 2003; 153:260–263.
- 31.↑
Cerda-Gonzalez S, Olby NJ, Broadstone R, et al. Characteristics of cerebrospinal fluid flow in Cavalier King Charles Spaniels analyzed using phase velocity cine magnetic resonance imaging. Vet Radiol Ultrasound 2009; 50:467–476.
- 32.↑
Perkins NJ. The inconsistency of “optimal” cutpoints obtained using two criteria based on the receiver operating characteristic curve. Am J Epidemiol 2006; 163:670–675.
- 33.
Tassanawipas A, Mokhavesa S, Chatchavong S, et al. Magnetic resonance imaging study of the craniocervical junction. J Orthop Surg (Hong Kong) 2005; 13:228–231.
- 34.
McGregor M. The significance of certain measurements of the skull in the diagnosis of basilar impression. Br J Radiol 1948; 21:171–181.
- 35.
Koenigsberg RA, Vakil N, Hong TA, et al. Evaluation of platybasia with MR imaging. A JNR Am J Neuroradiol 2005; 26:89–92.
- 36.
Rusbridge C, Carruthers H, Dube MP, et al. Syringomyelia in Cavalier King Charles Spaniels: the relationship between syrinx dimensions and pain. J Small Anim Pract 2007; 48:432–436.
- 37.↑
Nishikawa M, Sakamoto H, Hakuba A, et al. Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 1997; 86:40–47.
- 38.↑
Tubbs RS, Wellons JC III, Blount JP, et al. Inclination of the odontoid process in the pediatric Chiari I malformation. J Neurosurg 2003; 98:43–49.
- 39.
Menezes AH. Transoral-transpharyngeal approach to the anterior craniocervical junction. Ten-year experience with 72 patients. J Neurosurg 1988; 69:895–903.
- 40.
Henderson F, Benzel E, Vaccaro AR. Stretch-related myelopathy. Semin Spine Surg 2005; 17:2–7.
- 41.
Henderson F, Benzel EC, Kim D, et al. Pathophysiology of cervical myelopathy: biomechanical concepts. In: Benzel EC, ed. Spine surgery: techniques, complication avoidance, and management. 2nd ed. Philadelphia: Elsevier Churchill Livingstone, 2005;100–108.
- 42.
Henderson FA, Geddes JF, Vaccaro AR, et al. Stretch-associated injury in cervical spondylotic myelopathy: new concept and review. Neurosurgery 2005; 56:1101–1113.
- 43.
Maxwell WL, Domleo A, McColl G, et al. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J Neurotrauma 2003; 20:151–168.
- 44.
Maxwell WL, Islam MN, Graham DI, et al. A qualitative and quantitative analysis of the response of the retinal ganglion cell soma after stretch injury to the adult guinea-pig optic nerve. J Neurocytol 1994; 23:379–392.
- 45.
Maxwell WL, Kosanlavit R, McCreath BJ, et al. Freeze fracture and cytochemical evidence for structural and functional alteration in the axolemma and myelin sheath of adult guinea pig optic nerve fibers after stretch injury. J Neurotrauma 1999; 16:273–284.
- 46.
Henderson FC, Geddes JF, Crockard HA. Neuropathology of the brainstem and spinal cord in end stage rheumatoid arthritis: implications for treatment. Ann Rheum Dis 1993; 52:629–637.
- 47.
Bunge RP, Puckett WR, Becerra JL, et al. Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 1993; 59:75–89.
- 48.
Geddes JF, Hackshaw AK, Vowles GH, et al. Neuropathology of inflicted head injury in children. I. Patterns of brain damage. Brain 2001; 124:1290–1298.
- 49.
Geddes JF, Vowles GH, Hackshaw AK, et al. Neuropathology of inflicted head injury in children. II. Microscopic brain injury in infants. Brain 2001; 124:1299–1306.
- 50.↑
Kubota M, Yamauchi T, Saeki N. Surgical results of foramen magnum decompression for Chiari type I malformation associated with syringomyelia: a retrospective study on neuroradiological characters influencing shrinkage of syringes. Spinal Surg 2004; 18:81–86.
- 51.
Tagaki S, Kadosawa T, Ohsaki T, et al. Hindbrain decompression in a dog with scoliosis associated with syringomyelia. J Am Vet Med Assoc 2005; 226:1359–1363.
- 52.
Vermeersch K, Van Ham L, Caemaert J, et al. Suboccipital craniectomy, dorsal laminectomy of C1, durotomy and dural graft placement as a treatment for syringohydromyelia with cerebellar tonsil herniation in Cavalier King Charles Spaniels. Vet Surg 2004; 33:355–360.
