The cranial base is of crucial importance in skull development. Unlike most of the skull bones, it is formed through endochondral ossification of its cartilaginous anlages. During the ontogenesis of the skull, ossification centres form within these cartilages and the segments separating these centres are referred to as synchondroses
. In the postnatal period, ongoing multiplication of chondrocytes and gradual ossification of the synchondroses contributes to the expansion of the cranial base analogous to the growth plates of long bones
. Any disruption of the growth of these synchondroses can lead to skeletal and craniofacial malformations such as achondroplasia. In achondroplastic animals and humans, the growth of all synchondroses is impaired to various degrees, resulting in reduced longitudinal extension of the cranial base as well as in the long bones. Brachycephaly is one consequence of this growth retardation
The volume of the endocranial cavity is reduced less than one would expect from the degree of shortening of the neurocranium
. However, raised ICP has been found in achondroplastic patients. An association between an impaired outflow of blood at the exit foramina of the venous sinuses at the skull base has been proposed as the underlying etiology of this increased ICP, rather than an overall reduced intracranial volume
. The JF provides the extracranial passage for the sigmoid sinus, which is the major drain from the brain via the petrosal and transverse sinuses, flowing into the internal jugular vein
[32, 33]. Obstruction of the cerebral veins will increase ICP in more than one way. Holding of venous blood back in the skull, distention of the cerebral veins and venous hypertension follows. This in turn impairs cerebrospinal fluid (CSF) absorption at the arachnoid granulations, resulting in accumulation of CSF in the ventricles and communicating hydrocephalus
[31, 34, 35]. Enlargement of the jugular foramen in this condition has successfully reduced intracranial pressure and hydrocephalus
. The venous congestion and elevated ICP have also been associated with turbulent flow and jets of CSF as well as with cerebellar herniation
[37, 38]. This might also play a role as a pathogenetic factor in the development of SM in CKCSs, as has been proposed previously
In this study we focused on examination of the JF, because the other exit foramen for cerebral veins, the postglenoid foramen, has been found to be very variable. In canids the postglenoid foramen can even be divided so some dogs can have multiple postglenoid foramina. Its diameter is only 30% of the dimension of the JF in dogs. In contrast the JF is singular and characterized by minor variability in its morphology
. We use the term “jugular foramen” to describe the outflow tract of the intracranial veins for convenience. Actually, the JF is only the internal opening on the floor of the cranial cavity passing into a canal, whose extracranial opening is the tympano-occipital fissure (Figure
2). The JF is not easy to conceptualize due to its curved course. Measurements of the apical diameter of the JF in the two groups were attempted in this study, but minimal deviation of the image plane can lead to very variable diameters. For this reason volumes rather than diameters of the JF were determined, because diameters are strongly influenced by variations in orthograde positioning of the head. One limitation of our study was the exact ventral delineation of the JF, which had to be made by defined lines rather than by natural landmarks.
The results presented in this study can explain turbulent flow of CSF in the subarachnoid space as a consequence of raised ICP. This concept is independent of possible disproportionate volumes of the caudal skull compartment and the cerebellum. The increase in ICP could further exacerbate the CSF pulse pressure created by the decreased compliance in the subarachnoid space, which is considered to be the driving force of SM
. It can also explain why dogs with CM/SM often experience rapid worsening of clinical signs during or immediately after exercise, after abdominal wall straining at defecation or after excitement
. In these conditions return of systemic blood to the heart is impeded by pressure inside the chest and abdomen, leading to backpressure in the venous system and a rise in ICP. This could contribute to an exaggerated systolic CSF pressure in the spinal compartment. However, it seems likely that multiple pathogenetic factors act together or sequentially in the development of SM in the CKCS.
Although the findings of this study seem to present a plausible explanation for an increase in subarachnoid CSF pressure, it must be emphasized that this study merely presents morphological findings and definite data about a functional impairment of venous outflow needs to be obtained. Angiographic presentation of a collateral network of emissary veins trying to compensate for the constrained venous drainage would give further evidence of an existing functional impairment of blood flow
Sagittal sinus blood flow has been reported to be decreased in children with acondroplasia and constrained venous drainage from smaller JFs
. Determination of the blood flow in the sagittal sinus of the CKCS could also give further evidence of an existing functional impairment confirming our hypothesis from pure morphological data. Volume determination of the JF is a time consuming technique requiring specialized software and CT scanning of the dogs. However, quantification of intracranial venous blood flow might be a useful adjunct to the current imaging assessment of CKCS for breeding selection. Using MR-venography and cine phase contrast techniques, it could be possible to identify dogs having a higher risk of developing SM if impaired blood flow could be confirmed in follow-up studies.
Furthermore, treatment of raised ICP in these dogs might be directed at improving intracranial venous drainage rather than at vault expansion or CSF shunting procedures. Relief of raised ICP by surgical decompression of JF stenosis has been reported in children with achondroplasia and craniosynostosis
, and ICP elevation might be amenable to surgical foraminoplasty in the CKCS, too.