Curtis W. Dewey,     Ithaca, New York

Dominic J. Marino,     Plainview, New York

Catherine A. Loughin,     Plainview, New York

Pathophysiology and Clinical Features

Chiari-like malformation, as noted earlier, is thought to be the canine analog of Chiari type I malformation in people. As in the human disorder, the cranial cavity is too small to accommodate the contents of the caudal fossa (cerebellum and brainstem), which results in overcrowding of the cerebellomedullary region of the brain (Figure 237-1). On MRI, the abnormality of the supraoccipital bone that causes an indentation of the caudal cerebellum often is visible. In addition, an impingement of the dorsal subarachnoid space typically occurs at the level of the cervicomedullary junction. Herniation of the caudal aspect of the cerebellum through the foramen magnum also is commonly appreciated (Figure 237-2). Most of these dogs also have cervical SM, evident on MRI (Figure 237-3). CM generally has been considered a congenital malformation of the caudal occipital region of the skull, leading to overcrowding of the caudal fossa and compression of the cervicomedullary junction at the level of the foramen magnum. However, the anatomic abnormalities associated with CM are far more complicated than simply a malformed skull in the caudal-most aspect of the occipital bone region causing a physical constriction near the foramen magnum. It is now apparent that the malformations of CM are not limited only to the caudal part of the skull. In addition, there is convincing evidence in Cavalier King Charles spaniels that there is a mismatch between the volume available in the caudal fossa region (also referred to as the caudal cranial fossa) and the parenchyma (cerebellum and brainstem) that resides within this volume; in other words, there is too much brain parenchyma in too small a space in the caudal fossa of Cavalier King Charles spaniels (compared with other small-breed dogs and Labrador retrievers). This mismatch between parenchyma and available volume also has been demonstrated in the cranial fossa (rostral and middle fossae) of Cavalier King Charles spaniels. Increased ventricular size, increased relative parenchymal volume in the caudal fossa (as a percentage of total brain parenchymal volume), and increased relative cerebellar volume all have been associated with increased likelihood of the presence of SM in the cavalier King Charles spaniel breed. Increased syrinx width also has been associated with increased ventricular size and relative caudal fossa parenchymal volume in this breed. There is some evidence in the cavalier King Charles spaniel breed that the caudal fossa volume itself often is too small compared with other dog breeds. Other anatomic abnormalities of the skull reported in dogs with SM include minute or absent frontal sinuses and abnormally small jugular foramen volumes. With regard to this latter abnormality, it is hypothesized that the constricted venous drainage from the brain caused by small jugular foramina leads to intracranial venous hypertension and increased intracranial pressure; this would lead to an increased pressure differential between cranial and spinal compartments and an increased likelihood of SM development.

In atlantooccipital overlap, the atlas (C1) is cranially displaced into the foramen magnum, and there is overlap of the occipital bone and the atlas (Figure 237-4). This displacement tends to compress the caudal aspect of the cerebellum and elevate and compress the caudal medulla (medullary kinking). AOO likely is a form of basilar invagination. Basilar invagination is a human craniocervical junction disorder in which the atlas or axis (C2), or both, telescope toward the foramen magnum. It is possible that some cases of atlantoaxial instability in dogs are also analogs of basilar invagination. Based on combined MRI and CT imaging of dogs with CJAs, there is evidence that a substantial proportion (nearly 30%) of dogs diagnosed with CM based on MRI scans actually may have AOO as the main anatomic abnormality causing compression at the cervicomedullary junction. Bone is poorly visualized by MRI, but CT images clearly delineate what bony structures are causing compression at the cervicomedullary junction. In short, it is likely that many dogs with constrictive disorders at the cervicomedullary junction that are diagnosed via MRI as having CM actually may have AOO.

Similar to the AOO seen in small- and toy-breed dogs, we have seen a large number of dogs with dorsal compression at the level of C1 and C2. This compression varies in severity, with some dogs having a mild divot in the dorsal subarachnoid space and others having severe cervical spinal cord compression (Figure 237-5). At surgery, the majority of this compressive mass appears to be soft tissue, although several cases have had an obvious bony component. We believe that this disorder also may involve instability at the C1-C2 junction and possibly represents a form of basilar invagination like the AOO problem. It can occur as a sole entity or in combination with CM or atlantoaxial instability.

Syringomyelia most often is discussed in the context of CM as a causative disorder. However, SM can occur secondary to any CJA or to any disorder that disturbs normal laminar CSF flow in the subarachnoid space of the vertebral canal. Multiple mechanisms have been proposed for the formation of SM, all of which are based on the pressure differential between cranial and spinal compartments created by constriction at the cervicomedullary junction. We have found that of dogs that undergo MRI of their entire spine (not just the cervical region), most have syrinxes in the thoracic and lumbar spinal cord regions in addition to the cervical region. In a recent review of our unpublished MRI data for over 350 dogs, we found that syrinx formation begins in the cervical region and sequentially progresses to the thoracic region and finally to the lumbar region without skipping over a region. In one study of 49 Cavalier King Charles spaniels, 76% of the dogs had syrinxes in thoracic or lumbar regions or both, in addition to cervical SM (Loderstedt et al, 2011).

CM typically is encountered in small-breed dogs, with the cavalier King Charles spaniel being the most commonly affected. Other breeds affected by this disorder are the Brussels griffon, miniature poodle, Yorkshire terrier, Maltese, Chihuahua, bichon frise, Staffordshire terrier, pug, Shih Tzu, miniature dachshund, miniature pinscher, French bulldog, Pekingese, and Boston terrier. The typical age range at presentation appears to have changed over time, with many dogs developing clinical signs within the first year of life. In general, although the age range at clinical presentation is broad, CM is identified in most dogs by the time they are 4 years old. Dogs that are brought to the veterinarian at younger than 2 years of age often have more severe clinical signs than older dogs. In recent years, we have seen an increasing number of younger patients (<1 year of age); whether this trend reflects increasing severity of the disorder with subsequent generations, increased awareness within the veterinary community and the general public and hence earlier diagnosis, or a combination of these factors is unknown. Although AOO and dorsal C1-C2 compression are not as well characterized as CM, dogs with these disorders also tend to be young small-breed dogs, similar to the non-cavalier King Charles spaniel CM population. In our experience, the very small breeds (e.g., Yorkshire terrier, Chihuahua) tend to be diagnosed more frequently with AOO than with CM.

Clinical signs of CM and related disorders are variable, but the most consistent clinical features are cervical pain and apparent pruritus of the head, neck, and shoulder regions. Clinical signs of CM with SM include neck pain, back pain, vestibular dysfunction, cervical myelopathy, incessant scratching activity, lameness, diminished hearing, and scoliosis. Cervical myelopathy (with associated neck pain) and cerebellovestibular dysfunction (e.g., strabismus, decreased menace response with normal vision, head tilt, nystagmus) are encountered most commonly. In most cases, cerebellovestibular dysfunction is revealed during a neurologic examination and has not necessarily been observed by the pet owner. Many dogs with CM have decreased to absent menace responses with normal vision as well as varying degrees of positional ventrolateral strabismus. An unusual and distinctive feature of the scratching activity associated with CM in dogs is that these patients typically do not make contact with the skin while scratching at the head and shoulder regions, so-called phantom scratching or air guitar. Scratching often occurs on only one side. Facial rubbing (pawing at the face or rubbing against objects) also is encountered in some dogs and is considered to be a manifestation of pain or paresthesia. Spinal hyperpathia (typically cervical), scratching activity, and scoliosis all are generally believed to be related to interference of the syrinx cavity with ascending sensory pathways in the spinal cord. Scratching activity and neck discomfort often are exacerbated by abrupt weather changes, stress, or excitement, and by physical contact with the neck and shoulder region. The presence of both pain and scoliosis is correlated with syrinx width in cavalier King Charles spaniels with SM secondary to CM. Some of the neck pain may be related directly to constriction at the cervicomedullary junction or comorbid CJA. Occasionally dogs with CM and cervical SM have a specific variant of cervical myelopathy called central cord syndrome.

In these cases the outwardly expanding syrinx in the cervicothoracic intumescence causes damage to the lower motor neurons of the thoracic limbs within the regional gray matter; this leads to lower motor neuron paresis of the thoracic limbs while sparing the more peripherally located white matter tracts (upper motor neurons to the pelvic limbs). Damage to the regional white matter would cause general proprioceptive and upper motor neuron paresis in the pelvic limbs. The result is thoracic limb paresis (lower motor neuron in nature) that is notably worse than pelvic limb paresis. In some dogs with this syndrome, the pelvic limbs may appear normal.

Clinical signs in dogs with AOO typically are neck pain and varying degrees of ataxia of all four limbs. Similar clinical signs have been noted in dogs with dorsal compressive lesions at C1 and C2. It is important to realize that, especially in the cavalier King Charles spaniel breed, conditions other than CM-SM may account for some or all of the clinical signs identified. Recently it has been reported that more than 40% of cavalier King Charles spaniels with CM-SM are asymptomatic for the disorder, according to the dogs’ owners (Couturier et al, 2008); however, in a recent unpublished pilot study we found that 41% of 227 dogs demonstrated clinical signs that went unrecognized by their owners. Idiopathic epilepsy also is a prevalent disorder in the cavalier King Charles spaniel breed.

Seizures have been reported to occur in 10% to 12% of humans with Chiari type I malformation; in the authors’ experience, seizure activity is an infrequent occurrence in dogs with CM, and it is not possible to distinguish whether this seizure activity is due to CM or represents concurrent idiopathic epilepsy.

Congenital deafness also is well described in the cavalier King Charles spaniel breed. The severity and rate of progression of CM in dogs are variable, ranging from absence of symptoms (i.e., evidence of CM is found when imaging is performed for some other reason) to extreme pain and debilitation with rapid worsening over a short period. In addition, some dogs with CM have other unrelated concurrent disorders (e.g., disk extrusion, inflammatory brain disease) that could explain observed clinical signs. In such situations, it may be difficult to discern whether CM is the main problem, a contributory condition, or an incidental finding. An enigmatic ear problem seen in the cavalier King Charles spaniel breed called primary secretory otitis media also has been described. Clinical signs of primary secretory otitis media include apparent pain around the head and neck area, scratching of the head and neck, facial paralysis, and head tilt. Finally, other CJAs can occur concurrently with or be mistaken for CM. In the authors’ opinion, determination of a complete and accurate diagnosis, including identification of all types of CJA, is essential for development of an effective treatment plan for dogs with suspected CM.