Conformational indicators

The study found two aspects of conformation to be associated with the development of SM in the CKCS: the cephalic index and the distribution of cranium across the length of the head. It was found that a higher cephalic index and, separately, a lower percentage of the cranium distributed caudally were significantly associated with disease development.The human medical definition of cephalic index was used in this study, and the findings indicate that as the cranium is shortened and broadened, the risk of developing SM increases (Figure 5). In this case, the indicator is specifically at the level of below three years compared to those clear over five years of age, indicating it was protective against developing the condition at a young age but also protective in maintaining SM clear status over the age of five. Limited variability in this trait across the sample, seen in the narrow confidence interval upon exploration, may explain the limited variation in condition presence across the population. Craniofacial index was not a significant indicator, demonstrating the unimportance of muzzle length in disease progression. The increasing cephalic index in individuals was found to be highly associated with a more domed head.A higher percentage of cranium distributed in the fourth quadrant of the head was found to be significantly protective at all age levels analysed (most caudal area; green, Figure 6). As this was a percentage, the final value depended on two qualities: the amount of cranium in the fourth quadrant (green, Figure 6) but also the amount of cranium distributed rostrally to that quadrant (red, Figure 6). This inclusion of two qualities of head shape in the variable may explain the very high odds ratios.

Figure 5 Example of cephalic index differences in young affected and older clear individuals. The shorter and broader cranium is clearly demonstrated in the early SM affected individual. Red asterisk represents the point of the occipital protuberance and the line represents the breadth of the head at its widest points. Full size image

Figure 6 Example of caudal cranium distribution differences in young affected and older clear individuals. The cranium in the fourth quadrant in the SM clear individual shows an increased coverage of the grid relative to the first, second and third quadrants, resulting in a high percentage distribution in the fourth quadrant of 24%. Conversely, in the early SM affected individual, an increased coverage in the first, second and third quadrants and a decreased coverage in the fourth quadrant leads to a decreased percentage cranium distribution in the fourth quadrant of 12%. Full size image

Further analysis of dependence revealed a strong association between the two characteristics. The two variables did not share information. An explanation for this association may be a limit of conformation in nature or they may represent components of a common type within the breed. Based on plausible selection pressures, the loss of cranium distributed towards the back of the head could be a consequence of selection for a broader and shorter head (a higher cephalic index) and/or selection for more doming towards the front of the head to produce a deeper stop. No significant gender differences were apparent in these traits.

The results that were not significant but maintained in the final model may have been found to be significant (or not) with more accurate divisions in phenotype or a larger population. Of particular interest is palpebral aperture. It is a misconception that the “large” eye stipulated in the breed standard of the CKCS reflects the size of the globe; instead it reflects the aperture and degree of globe exposure. The trends relating to palpebral aperture found in two separate models both suggest that an increasing palpebral aperture is indicative of disease presence; however, the breed standard directly requires the breed to have “large” eyes [16]. Further characterisation of the relationships between brachycephaly and other aspects of cranial morphology, as well as contributing to the evidence-base on other associated conditions (such as airway obstruction), would proffer further conformational indicators and a more complete illustration of risk phenotype.

These findings are in parallel to those of the radiographic study performed on the Griffon Bruxellois that found that shortening of the basicranium was associated with CM, a rounding of the skull dorsally (compensatory parietal lengthening) and a comparatively broad head [11]. A further MRI study on CM and SM affected Griffon Bruxellois found increased height of the rostral cranial cavity was the most significant predictor of disease [12]. Previous observations of the changes in CKCS skull morphology included concavity, or flattening of the supraoccipital bone and caudal cranium.

As the foetus develops, the cartilaginous foundation of the base of the skull is replaced with bone by the process of endochondral ossification. Cranial synchondroses, however, remain within the neonate and represent cartilaginous boundaries where growth can continue through continual production of cartilaginous matrix and ossification. Later, complete ossification of the plates determines the end of bone growth. The closing of these synchondroses has been found to differ between bones but also between breeds of dog [17, 18]. This study supports the hypothesis of an overly short skull base through premature synchondrosis closure - a craniosynostosis - in the CKCS, resulting in a shortening of the basicranial axis and compensatory lengthening of other bones, especially of the calvaria. The craniosynostosis, as well as reducing the rostrocaudal length of the skull and contributing to neural tissue overcrowding may also reduce the volume of the jugular foramen, which may cause an intracranial hypertension and predispose syrinx development. Schmidt et al. (2013) determined a craniosynostosis relative to mesaticephalic breeds (for example, Labrador and German shepherd dog) in the CKCS spheno-occipital synchondrosis. This synchondrosis contributes especially to post-natal cranial base elongation in humans, and the difference in closure time found in the CKCS was also significant when comparing to other brachycephalic breed such as Pugs and Pekingese [19]. The study findings of loss of cranium distributed towards the back of the head could also support a CM hypothesis of occipital hypoplasia [8].

The conformational indicators found were able to correctly classify between 69% and 89% of cases as SM clear or affected at various age levels. Furthermore, they were found to explain up to 50% of the variability in condition presence. This suggests that these morphological characteristics of the skull are implicated in, or at least indicative of, the pathogenesis of SM as discussed above. This study was unable to determine conformational indicators at the level of CM in the CKCS due to lack of CM clear controls; however, the age at which an individual develops a syrinx may relate to slight graduations in CM so may be an indirect measure of CM severity or type.

A cephalic index calculation (Table 3; Figure 5) may represent a particularly useful measure in that it can be calculated with little skill (with low-cost tools), is visually obvious and gives a numerical output. The authors chose not to estimate a cut-off value for cephalic index as the information would be better employed in decreasing the cephalic index with each generation in the form of a selection pressure rather than removing individuals outright from the limited gene pool. This numerical output would be particularly effective in a population where trait variability was low, as demonstrated here, and could be incorporated into Estimated Breeding Value calculations or as part of the Mate Select system of the Kennel Club in a similar manner to that of hip scores.