Introduction

Syringomyelia (SM) was first identified in the Cavalier King Charles Spaniel (CKCS) in 1997¹ and was first described in 2000². The syringomyelia occurs secondary to foramen magnum overcrowding and the clinical signs that develop are consistent with a central cervical spinal cord lesion. ² Syringomyelia in the CKCS is a hereditary disease that places pressure on the breeding stock in light of the other hereditary conditions of mitral valve dysplasia and idiopathic epilepsy.¹ Screening for syringomyelia is performed with MRI evaluation of the caudal brain and cranial cervical spinal cord. Clare Rusbridge has developed appropriate screening criteria which, if implemented by breeders, may help reduce the incidence in the breed. Eighty-five CKCS have been screened through my practice and the incidence of syringomyelia has been calculated at 41%.

Clinical Signs

Clinical signs are secondary to the fluid-filled cavity (syrinx) in the cervical spinal cord and are listed below^2,3

 Persistent scratching at one side of the shoulder/neck area, seen most commonly when walking the dog on a leash. No skin contact is made with the scratching.

 Excitement, exertion, and barking could also elicit the response.

 Neck pain.

 Owners report that dogs resent any touching or grooming of the ear, limb, or neck of the "scratched" side.

 Lower motor neuron deficits of the thoracic limb ipsilateral "scratched" side.

 Proprioceptive deficits and ataxia of the pelvic limbs.

 Facial nerve paralysis.

 Head twisted to the "scratched" side.

Clinical signs are first noted between 6 months and 3 years of age.³ Signs of pain are not well correlated with the size of the syrinx.

History of Syringomyelia and Chiari Formation

Cavitation within the spinal cord was first described in the 16th century and the term syringomyelia was first used in 1824, and the cavity was thought to be a dilatation of the central canal that was in communication with the fourth ventricle.³ We now know that in less than 10% of human patients there is communication between the syrinx and the fourth ventricle. The fluid in the spinal cavities closely resembles CSF. The syrinx may be lined with glial cells and if it communicates with the central canal it may be partially lined with ependymal cells.³ In 1891, Hans von Chiari, a pathologist, described four different types of abnormalities based on autopsy results of infants who died shortly after birth with hydrocephalus.³ Type 1 malformation described elongation of the cerebellar tonsils and the medial part of the cerebellar lobes which accompanied the medulla into the spinal canal. The term is incorrectly applied to the dog as the dog does not have cerebellar tonsils, and it may be more correct to use the terms "occipital hypoplasia with syringomyelia," or caudal occipital malformation syndrome." In November 2006, an international conference on CKCS and syringomyelia was held in London and the term "Chiari-like malformation and syringomyelia" was adopted as the preferred name for the condition at this time.⁵

Pathophysiology of Syringomyelia

It is accepted that the syringomyelia that develops in the cervical spinal cord is associated with the caudal occipital hypoplasia.^2-4 In the normal mammal, CSF moves caudally and rostrally between the head and the vertebral column. This rapid efflux and influx occurs as a result of the expansion and contraction of the intracranial arteries during the cardiac cycle.³ When there is obstruction to this flow because of overcrowding of the foramen magnum, then a syrinx may develop. A number of theories have developed over the years that have tried to explain this phenomenon. Currently, there are two main theories that are accepted as plausible:³ the piston theory and the intramedullary pulse pressure theory.

1. Piston Theory⁴

 The Chiari malformation partially obstructs CSF pathways at the foramen magnum.

 The normally rapid efflux and influx of CSF between the head and the spine, which compensates for the brain expansion and contraction during the cardiac cycle, is blocked.

 The cerebellar tonsils are displaced during the cardiac cycle, in lieu of CSF, creating a piston effect on the partially enclosed subarachnoid space.

 Enlarged cervical subarachnoid pressure waves are created, which compress the spinal cord from without, direct CSF into the spinal cord, and cause pulsatile syrinx flow.

 This leads to syrinx progression.

2. Intramedullary Pulse Pressure Theory³

 Syringomyelia caused by repeated mechanical distention of the spinal cord.

 Cavitation arose from the fluid in the high pressure microcirculation in the spinal cord and not the CSF.

 The pressure wave of CSF created by the arterial pulsation is called the systolic CSF pulse pressure.

 With subarachnoid blockage there is decreased transmission of pressure to CSF below the obstruction.

 Consequently, increased reflection of pressure into the spinal cord proximal to the obstruction.

 Therefore, increased pulse pressure in the spinal cord and decreased pressure in the subarachnoid space distal to this result in distention of the spinal cord distal to obstruction. This results in syrinx formation.

 With partial obstruction also gets a venture effect causing further decreased subarachnoid pressure distal to obstruction (i.e., fast flow of fluid across the obstruction).

 Partial obstruction at the disc space C2/C3 is very susceptible to the venture effect.

Diagnosis of Syringomyelia

Diagnosis of SM can only be made on MRI imaging of the caudal brain and the spinal cord. The goal of imaging is to confirm syrinx formation in the spinal cord and also to demonstrate Chiari type 1 malformation. The caudal basioccipital bone is short resulting in reduced caudal fossa volume with the caudal cerebellar vermis and medulla extending through the foramen magnum.³ The ventricles in the brain are also often distended.^2,3

These dogs also often have fluid-filled tympanic bulla. As a minimum, both T1 and T2 sagittal sequences of the caudal brain and proximal spinal cord should be taken together with T2 transverse sequences through the proximal spinal cord (e-mail Clare Rusbridge).

Treatment of Syringomyelia

Treatment involves both medical and surgical management. Not all patients require treatment and particularly when the syrinx is small or asymptomatic.³ Medical treatment revolves around the use of three groups of drugs: analgesics, drugs that reduce CSF production, and corticosteroids.³ Analgesics that can be considered are the NSAIDs, oral opioids. Gabapentin may also be used as it has a damping effect on the hyperexcitable damaged nervous tissue. Furosemide decreases CSF production and is a useful drug in the management of SM.³ The carbonic anhydrase inhibitor acetazolamide may also help but can have unpleasant abdominal side effects. Corticosteroids are very effective in reducing pain and neurological deficits but the mechanism of action is unknown.

It is recommended that furosemide is tried first for 2 weeks and response is evaluated. If response is poor, then a NSAID is added. This is tried for 2 weeks. If poor response, then NSAIDs are dropped and gabapentin is tried. If clinical signs are still not controlled, then furosemide is discontinued and corticosteroids are tried.

Surgical treatment is reserved for those dogs with refractory pain or worsening of the neurological signs.³ The aim of surgery is to restore the CSF dynamics. This is achieved by suboccipital decompression where most of the supraoccipital bone and sometimes the cranial dorsal laminae of the atlas are removed. The largest case series of 16 dogs found that 81.25% of affected dogs had improvement or resolution of clinical signs, but 25% had relapses within the follow-up period. The earlier the surgery was performed, the better the outcome.³

Inheritance of Syringomyelia in the CKCS¹

Studies on the inheritance of SM in the CKCS are ongoing and the findings to date are listed below:

 It is likely that the condition follows a recessive mode of inheritance.

 Six to 8 grandparents of all affected dogs could be traced back to 2 female ancestors.

 The disease appears to be more severe and have an earlier onset with increased inbreeding.

 Selection for coat colour is believed to have influenced the development of SM.

 Breeding guidelines to reduce the incidence of mitral valve disease have put increased pressure on the gene pool.

 To date, there is no evidence supporting a sex-linked mode of inheritance.

Grading of Syringomyelia for Breeding

In November 2006 a grading scheme was adopted at an international syringomyelia conference. This has been in place since November 2006 until early 2012 when a new grading scheme was introduced.

2012 Grading Scheme⁶

The certificate will detail the following:

a. Chiari-like malformation (CM), graded as follows:

 (i) Grade 0, no CM - the cerebellum has a rounded shape with signal consistent with cerebrospinal fluid (CSF) between the caudal cerebellar vermis and the foramen magnum.

 (ii) Grade 1 CM - the cerebellum does not have a rounded shape (i.e., there is indentation by the supraoccipital bone), but there is a signal consistent with CSF between the caudal vermis and the foramen magnum.

 (iii) Grade 2 CM - the cerebellar vermis is impacted into or herniated through the foramen magnum.

NB: At the present time, most Cavalier King Charles Spaniels scanned have Chiari-like malformation.

b. Syringomyelia (SM), graded as follows:

Syringomyelia (SM) is defined as a fluid-filled cavity that includes or is distinct from the central canal of the spinal cord and is graded according to its maximum internal diameter in a transverse plane.

Pre-syrinx is defined as spinal cord oedema, may be a transitional state prior to development of syringomyelia.

Pre-syrinx has the appearance of high signal intensity on T2W images, consistent with marked increased fluid content within the spinal cord substance but not of free fluid. On T1W images the spinal cord is either normal or has a slightly hypointense signal.

(i) Grade 0 - normal.

(ii) Grade 1 - central canal dilation which has an internal diameter of less than 2 mm.

(iii) Grade 2 - syringomyelia (central canal dilation which has an internal diameter of 2 mm or greater), separate syrinx, or pre-syrinx with or without central canal dilation.

The grade is qualified with a letter indicating the age group at the time of scanning as follows: a = more than five years of age; b = three to five years of age; c = one to three years of age. The grade is not valid without the qualifying letter.

Discussion and Prevalence In South Africa

Syringomyelia is highly prevalent within the South African Cavalier King Charles Spaniels. I have been involved in a screening program with the CKCS breeders and to date we have screened about 85 dogs and this process is ongoing at the moment. The prevalence of syringomyelia in CKCS in South Africa is 41%. The grading system provides information for the breeders with regards to selecting dogs for breeding and reducing the incidence of syringomyelia. The major shortfall of the grading system (2006 grading system) is that it relies on the breeder to declare any clinical signs that are evident in their dogs that are noticed in the home environment as the clinical signs are often subtle and not evident in the consulting room. This makes differentiation between the grading of D and E from F dependent on the breeder, which is critical to the breeding program, and if the breeder wants to conceal the clinical symptoms the eradication of the problem will be hindered. The 2012 grading scheme is more simplified and does away with clinical signs as part of the grading criteria, except to say that if clinical signs are evident, then dogs should not be used for breeding. The CKCS also suffers from hereditary mitral valve disease and this needs to be screened at the same time as syringomyelia screening. If the breeders are to reduce the incidence of the condition, then strict screening and breeding programs will need to be implemented.

Table 1

References

1.  Rusbridge C, Knowler S. Inheritance of occipital bone hypoplasia (Chiari type 1 malformation) in Cavalier King Charles Spaniels. J Vet Intern Med. 2004;18:673–678.

2.  Rusbridge C, MacSweeny JE, Davies JV, et al. Syringohydromyelia in Cavalier King Charles Spaniels. J Am Anim Hosp Assoc. 2000;36:34–41.

3.  Rusbridge C, Greitz D, Iskandar BJ. Syringomyelia: current concepts in pathogenesis, diagnosis, and treatment. J Vet Intern Med. 2006;20:469–479.

4.  Heiss JD, Patronas N, DeVroom HL, et al. Elucidating the pathophysiology of syringomyelia. J Neurosurg. 1999;91:553–562.

5.  International Conference on Syringomyelia; Saturday 11th November 2006; Royal Veterinary College, London, UK.

6.  British Veterinary Association/Kennel Club. Chiari malformation/Syringomyelia (CM/SM) scheme - Procedure Notes.