Syringohydromyelia, especially in the cervical spinal cord, may develop from altered CSF pressure secondary to obstructed flow through the foramen magnum by tumors or anatomic malformations.1-8 In small-breed dogs and humans, obstruction of CSF flow through the foramen magnum is frequently attributed to a malformation that decreases the size of the infratentorial portion of the cranial cavity such that it is too small to accommodate the normally sized cerebellum and brainstem (eg, caudal occipital malformation syndrome and Chiari type I malformation).1-3
Comparison of magnetic resonance images of the heads of clinically normal dogs with images from affected dogs has revealed certain commonly reported signs of caudal occipital malformation syndrome in affected dogs (eg, buckling of the brainstem, herniation of the cerebellum through the foramen magnum, compression of the dorsal aspect of the subarachnoid space, and syringohydromyelia).2 In that study,2 the cerebral hemispheres in affected dogs appeared shorter rostrocaudally and arched more dorsally with the frontal lobes folded ventrally, possibly displacing the entire brainstem and cerebellum caudally against the occipital bone. Although this general appearance is common in small-breed dogs with a dome-shaped head, we questioned whether syringohydromyelia was caused by decreased volume in the infratentorial portion of the cranial cavity, the supratentorial portion, or the entire cranial cavity.
A round or dome-shaped cranium is a desirable conformational feature in some small-breed dogs and is frequently unaccompanied by neurologic signs. However, if such conformation resulted in decreased volume in the cranial cavity without an appropriate decrease in brain size, overcrowding in the infratentorial portion of the cranium could result in obstruction of CSF flow through the foramen magnum and a subsequent alteration in CSF pressure. It is possible that this group of morphologic findings exists as a continuum from normal and desirable to abnormal and undesirable.
If this view of a continuum of cranial conformation aspects in some small-breed dogs is correct, it suggests that there may be alternative explanations for the fact that some dogs with syringohydromyelia have neurologic signs related to the forebrain and why there is no apparent correlation between neurologic signs and severity of cerebellar herniation and syringohydromyelia.9 It also suggests that the inciting developmental changes are not arising from or limited to the caudal aspect of the cranium, but rather may arise from the rostral portion of the cranium (and the occipital changes are secondary) or from the entire cranium. If this is true, there may be implications for the success of certain types of treatments and the development of screening or diagnostic tests. The objective of the present study was to determine whether there was an association between small frontal sinuses and syringohydromyelia in smallbreed dogs that underwent MRI during a 20-month interval. We hypothesized that small frontal sinuses were associated with development of syringohydromyelia.
Materials and Methods
Case selection—A cross-sectional (prevalence) study was performed by evaluating records of all smallbreed (weight, < 15 kg) dogs that were ≥ 6 months old and underwent MRI of the brain and at least the cranial part of the cervical portion of the spinal cord at the Cornell University Hospital for Animals from October 2004 through June 2006. Records were reviewed, and signalment information was collected.
Procedures—Images were obtained with a 0.2-Tesla MRI system.a Multiple and variable sequences and anatomic planes were used in different dogs. The protocol at the authors' institution is to obtain images in the dorsal plane parallel to the hard palate and in the transverse plane perpendicular to the dorsal plane. For all dogs, images were evaluated by a board-certified veterinary radiologist (MST) for frontal-sinus size and by a third-year resident in veterinary diagnostic imaging (KRW) for the presence of syringohydromyelia. The assessment of frontal-sinus size was made after viewing multiple scans through the entire area of both frontal sinuses in 2 or 3 planes (transverse, sagittal, and dorsal). Both examiners were blinded to the aim of the study, which was to investigate a possible association between frontal-sinus size and syringohydromyelia. Examiners were also unaware of each other's evaluation. Air-filled frontal sinuses were scored as absent (no air and no diploë), miniscule (some diploë may be seen), small (but normal), normal, or enlarged (secondary to disease). The size and shape of the frontal sinus vary normally among dogs; therefore, normal was defined as a gas-filled space exceeding the size of diploë between the superficial and deep laminae of the frontal bone. Syringohydromyelia was scored as present, questionable, or absent depending on whether linear or focal fluid accumulation was detected in the spinal cord. The severity of syringohydromyelia was not assessed, so mild enlargement of the central canal and severe loss of spinal cord parenchyma were both considered as syringohydromyelia.
Dogs were categorized on the basis of whether absent or miniscule air-filled frontal sinuses were present and whether syringohydromyelia was definitely present (for purposes of the study, dogs with absent or miniscule air-filled frontal sinuses were defined as having small frontal sinuses, and the remaining dogs were defined as having large frontal sinuses). The frequencies of these findings were used to calculate the prevalence and 95% confidence intervals for syringohydromyelia in dogs with and without small frontal sinuses.
Statistical analysis—A Yates-corrected, 2-tailed χ2 test was used to investigate the null hypothesis that there is no association between the 2 conditions. If the null hypothesis could be rejected at the 5% level, the strength of the association was further evaluated by estimating the relative risk on the basis of the prevalence and odds ratios. Statistical analyses were performed by use of commercially available software.b
Results
Sixty-two dogs met the selection criteria. Small frontal sinuses were detected in 28 of 62 (45%) dogs. Mean age was 6.7 years (range, 0.6 to 17.4 years), and mean body weight was 5.3 kg (range, 1.1 to 12.3 kg). Four of 28 (14%) dogs were sexually intact females, 14 of 28 (50%) were neutered females, 4 of 28 (14%) were sexually intact males, and 6 of 28 (21%) were neutered males.
Large frontal sinuses were detected in 34 of 62 (55%) dogs (no dog had enlarged frontal sinuses secondary to sinus disease). In this group, the mean age was 7.4 years (range, 1 to 15.7 years) and mean body weight was 7.5 kg (range, 1.7 to 14.6 kg). Two of the 34 (6%) dogs were sexually intact females, 14 of 34 (41%) were neutered females, 1 of 34 (3%) were sexually intact males, and 17 of 34 (50%) were neutered males.
The sample population was composed of 25 breeds. Small frontal sinuses were detected in the following breeds: Yorkshire Terrier (n = 6); Boston Terrier (4); Shih Tzu (4); Chihuahua (3); Maltese (3); Cavalier King Charles Spaniel (2); Pug (2); and 1 each of Jack Russell Terrier, mixed, Papillon, and Pomeranian. Large frontal sinuses were detected in the following breeds: mixed (n = 5); Maltese (3); Poodle (3); Shetland Sheepdog (3); Beagle (2); Cavalier King Charles Spaniel (2); Dachshund (2); Lhasa Apso (2); Miniature Pinscher (2); Cairn Terrier (2); and 1 each of Bichon Frise, Chinese Crested, Cocker Spaniel, Miniature Schnauzer, Pomeranian, Schnauzer, Silky Terrier, and Wire Fox Terrier.
Syringohydromyelia was detected in 12 of 62 (19%) dogs. Mean age was 5 years (range, 1.3 to 9.4 years), and mean body weight was 4.8 kg (range, 1.1 to 10.8 kg). One of the 12 dogs was a sexually intact female, 7 of 12 were neutered females, 2 of 12 were sexually intact males, and 2 of 12 were neutered males. The following breeds were included: Yorkshire Terrier (n = 5); Cavalier King Charles Spaniel (3); and 1 each of Chihuahua, Lhasa Apso, Maltese, and Papillon. In dogs without syringohydromyelia, mean age was 7.6 years (range, 0.6 to 17.4 years) and mean body weight was 6.8 kg (range, 1.1 to 14.6 kg).
Dogs were categorized according to frontal-sinus size and whether syringohydromyelia was present by use of a 2 × 2 frequency table (Figures 1 and 2). Syringohydromyelia was detected in 10 of 28 dogs with small frontal sinuses (prevalence, 36%; 95% confidence interval, 16% to 55%) and in 2 of 34 dogs with large frontal sinuses (prevalence, 6%; confidence interval, 0% to 15%). The probability of detecting syringohydromyelia in dogs with small frontal sinuses was significantly (P = 0.008) greater than detecting syringohydromyelia in dogs with large frontal sinuses. The prevalence ratio was 6.1, and the odds ratio was 8.9.
Sagittal plane T1-weighted magnetic resonance images of the head and proximal portion of the neck in a male small breed–mix dog (weight, 4.4 kg) with large frontal sinuses and no syringohydromyelia. Notice the air-filled frontal sinuses (arrows) on the dorsal-plane image (insert; image was obtained through the largest part [line] of the frontal sinuses).
Citation: American Journal of Veterinary Research 68, 6; 10.2460/ajvr.68.6.610
Sagittal plane T1-weighted magnetic resonance image of the head and proximal portion of the neck in a neutered female Cavalier King Charles Spaniel (weight, 4.8 kg) with syringohydromyelia. Buckling of the brainstem, prominent lateral ventricles, compression of the dorsal aspect of the spinal subarachnoid space at the foramen magnum, and small frontal sinuses are evident. Notice the small frontal sinuses (arrows) on the dorsal-plane image (insert; image was obtained through the largest part [line] of the frontal sinuses).
Citation: American Journal of Veterinary Research 68, 6; 10.2460/ajvr.68.6.610
Small frontal sinuses and syringohydromyelia were detected in slightly more females than males. Therefore, data were stratified by sex and the analysis was repeated. Because we found no difference in the odds ratio and to increase statistical power, only the combined data were reported.
Discussion
Cross-sectional studies are useful in revealing associations that can be evaluated further in studies that provide stronger evidence of association (eg, case-control or cohort studies). The cross-sectional study design of the present study revealed an association between small frontal sinuses and syringohydromyelia in smallbreed dogs that underwent MRI from 2004 to 2006, but a causal relationship cannot be established with our data. Furthermore, because we frequently observed small frontal sinuses in dogs with and without syringohydromyelia and observed syringohydromyelia in dogs with large frontal sinuses, there may be another factor or factors (eg, genetic traits) that cause both conditions or a more global malformation of the head. A genetic pathogenesis is likely, given that syringohydromyelia has been reported in many small-breed dogs but appears to be more frequent in certain breeds, including Cavalier King Charles Spaniel, Pomeranian, Yorkshire Terrier, Maltese, and miniature and toy Poodles.2,10 Syringohydromyelia is not always clinically important and does not necessarily lead to neurologic abnormalities or the need for treatment. For instance, in our study population, syringohydromyelia was mild in some instances and was considered to be incidental to the primary diagnosis or a secondary problem in others. Our results did not indicate that small frontal sinuses are associated with altered CSF pressure at the foramen magnum or with small size of the supratentorial part or entire volume of the cranial cavity. Similarly, no claim can be made about an association between frontal-sinus size and syringohydromyelia in large-breed dogs.
Our data do suggest, however, that the pathogenesis of syringohydromyelia in small-breed dogs may involve the supratentorial portion of the cranial cavity. We postulate that syringohydromyelia develops in many small-breed dogs and certain breeds in particular as a result of global malformation of the entire cranial cavity or supratentorial portion of the cavity and is not limited to the infratentorial portion of the cranial cavity. If this is true and results can be generalized to the target population, our understanding of the pathogenesis of syringohydromyelia in small-breed dogs and several aspects of clinical management (eg, screening and diagnostic testing, breeding recommendations for dogs with dome-shaped heads, and treatments) will require further investigation.
Syringohydromyelia is not always related to cranial conformation.11 A Lhasa Apso in the present study (1/2 dogs with large frontal sinuses and syringohydromyelia) had a histologically confirmed choroid plexus papilloma in the left lateral aperture. Syringohydromyelia may have developed in this dog because the neoplasm obstructed CSF flow through the foramen magnum. Cranial conformation, however, may be the most common cause of syringohydromyelia in certain small-breed dogs. Additional morphometric studies are needed to determine whether small frontal sinuses are associated with factors such as small size of the supratentorial portion or entire cranial cavity or an abnormal angle between the floor of the cranial cavity and the neck. Additional studies are also needed to determine whether dogs with small frontal sinuses and syringohydromyelia have a smaller supratentorial portion or entire cranial cavity volume than dogs with large frontal sinuses and no syringohydromyelia.
Although we did not detect differences in prevalence ratios by sex, weight, age, or breed, further evaluation of the associations between those factors and syringohydromyelia is needed. Because a small frontal sinus is a common finding in small-breed dogs and many small-breed dogs do not develop syringohydromyelia, longitudinal studies in clinically normal young dogs with and without small frontal sinuses are also needed to determine the attributable risk of developing syringohydromyelia. Attributable risk, which in this instance is a measure of the risk of syringohydromyelia attributed to having small frontal sinuses, is the difference in incidence rates of syringohydromyelia between small-breed dogs with and without small frontal sinuses.
ABBREVIATION
| MRI | Magnetic resonance imaging |
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