Morphological variation of the caudal fossa of domestic cat skulls assessed with CT and geometric morphometrics analysis

Abstract

Objectives

This study aimed to investigate differences and demonstrate a normal range of morphological variation of the caudal fossa of the cranium of domestic cats.

Methods

CT scans of 32 domestic cat heads of 11 breeds were included. Isosurfaces from skulls were characterised through three-dimensional geometric morphometrics using geographical landmarks placed on the internal surface of the caudal fossa and foramen magnum. Raw data was transformed with a Procrustes fit and coordinate covariance was analysed by principal components to establish breed- and sex-level differences. Skulls were also classified according to the number of concavities along the mid-sagittal vermiform impression. Differences were investigated between breed groups and sex, and correlation was sought with age.

Results

Analyses revealed size-independent differences in occipital bone morphology across breeds and sex; however, no clustering was evident. Most variability was observed at the exoccipital bones, ventral portion of the supraoccipital bone, dorsum sellae of the basisphenoid and the osseous tentorium cerebelli. No statistically significant differences were identified via two-sample t-tests between breed groups or sexes. No statistically significant correlation using Spearman rho correlation coefficient was identified with age.

Conclusions and relevance

The feline caudal fossa displays a wide range of intra- and inter-breed variation, not linked to age or sex. Concavities along the vermiform impression have not previously been described. As advanced imaging modalities are becoming more frequently used for domestic felids, an established range of normality is important for discriminating pathological changes from anatomical variances.

Introduction

The caudal fossa has been the focus of extensive research in humans and canids, in part owing to its role in the pathogenesis of various disorders such as Chiari and Chiari-like malformations, as well as occipital dysplasia.^1–8 There is, however, a paucity of information regarding variability in skull morphology among existing breeds of the domestic cat (Felis catus). With the increasing use of advanced diagnostic imaging in this species, recognition of the breadth of normal anatomical variation is crucial. In our experience, cats display a wide variability in caudal fossa shape in the absence of associated clinical signs.

The caudal fossa of the cranial cavity encompasses the midbrain, pons and medulla oblongata ventrally and the cerebellum dorsally. Rostrally it extends to the dorsum sellae of the sphenoid bone and the osseous tentorium cerebelli of the occipital bone. Caudally it is enclosed by the supraoccipital bone, which forms the dorsal border of the foramen magnum. ⁹ The internal surface of the supraoccipital bone displays shallow depressions, which conform to the surface of the cerebellum – the vermiform impression. ⁹ The basioccipital bone forms the ventral border of the foramen magnum and joins the basisphenoid via a cartilaginous suture. The exoccipital bones form the lateral portions of the foramen magnum and bear the convex occipital condyles. ⁹

The objectives of this study were to investigate and describe differences in caudal fossa shape and determine whether these differences are stereotyped by breed or sex. To detect shape trends of the caudal fossa, we used CT, an imaging modality that is amenable to geometric morphometrics analysis.

Materials and methods

Sample population

Imaging records of our academic veterinary referral hospital were searched retrospectively between January 2011 and December 2015 to identify adult cats (>12 months of age) that had undergone a CT examination of the entire head to at least the level of the second cervical vertebra. Studies were excluded if there were any pathological cranial or neural abnormalities identified on the imaging study or clinical records. All CT examinations were acquired with the same four-slice CT unit (Siemens Somatom) using a 1 mm slice width, 1.5 pitch, 130 mAs, 120 kV, 0.75 s tube rotation time and high-resolution image kernels (proprietary term U90).

Three-dimensional landmarking

Skull isosurfaces were generated from DICOM images using Stratovan Checkpoint (v2016.11.21.0711). Twelve geographical landmarks were placed on the internal surface of the caudal fossa and foramen magnum of each skull (Figure 1a,b) to represent the overall shape and dimensions. Specifically, landmarks were placed at the osseous tentorium cerebelli, along the internal sagittal curvature of the caudal fossa, opisthion, basion, the basioccipital bone, dorsum sellae and the lateral-most points of the internal surface of the foramen magnum.

Figure 1

Landmarks along the internal surface of the (a) caudal fossa and (b) foramen magnum. Images are not to scale. In (b), a portion of the occipital bone has been cropped out

Geometric morphometric analysis

Landmark coordinates and classifier data were imported into MorphoJ (v1.06d) ¹⁰ for geometric morphometric analysis. Superimposition, translation, rotation and scaling of landmark configurations were performed via a generalised Procrustes fit prior to generating a covariance matrix. ANOVA was used to evaluate differences in centroid size (the square root of the sum of squared distances of landmarks from the central point) among breed groups. A multivariate regression of the symmetrical component of shape vs log centroid size was performed to remove the influence of allometry, the shape changes correlating to changes in size. Principal components analysis (PCA) is a mathematical algorithm that reduces and expresses a dataset in terms of vectors along which variation is maximal. A PCA of the resulting regression residuals was used to explore patterns of covariance among landmarks. ¹¹

Classification

A midline sagittal CT image was created for each cat using multiplanar reconstruction on freely available DICOM viewing software (Horos v2.0). The skulls were classified into groups based on the number of concavities along the vermiform impression of the caudal fossa. One reader, a second-year radiology resident, categorised each image, blinded to the signalment of each case. A two-sample t-test was used to evaluate differences in concavity number between sexes, and between breed groups. A Spearman rank correlation coefficient (r_s) sought correlations between the number of concavities and age, principal component (PC)1, PC2 and centroid size of the caudal fossa. A P value <0.05 was considered significant.

Results

The study population comprised of 32 CT scans of domestic cat heads. There were two entire females, one entire male, 11 neutered females and 18 neutered males. Entire and neutered cats were grouped together for statistical purposes; thus, the overall study numbers were 13 (41%) female and 19 (59%) male. Eleven breeds were represented, including Abyssinian (n = 1), British Shorthair (n = 1), Bengal (n = 1), Burmese (n = 2), Chinchilla (n = 1) domestic longhair (DLH) (n = 3), domestic shorthair (DSH) (n = 15), Maine Coon (n = 4), Ragdoll (n = 1), Siamese (n = 2) and Tonkinese (n = 1). For statistical purposes, cats were grouped according to phylogenetic origin into Asian cats (Burmese, Siamese, Ragdoll, Tonkinese; n = 6), Western European cats (Abyssinian, Maine Coon, British Shorthair, Chinchilla; n = 7) and mixed breeds (DLH, DSH, Bengal; n = 19). ¹² CT images of all cats were sufficiently detailed to allow consistent placement of all landmarks on stereotyped locations of the caudal fossa and foramen magnum.

Geometric morphometrics

For the symmetric component of shape with allometry, PC1 accounted for 21.6% of the variation among all cats. PC2 accounted for 15.4% of variation. Thus, PC1 and PC2 cumulatively accounted for 37.0% of the observed variation. Most variability explained by PC1 was observed at the exoccipital bones and dorsum sellae. As the exoccipital markers shifted caudally, the dorsum sellae shifted dorsally, whereas the roof of the cranial fossa shifted, less markedly, in an overall rostral direction. Neighbouring landmarks along the roof of the caudal fossa varied between rostroventral and rostrodorsal trends. Variability explained by PC2 was observed at the osseous tentorium cerebelli and foramen magnum. As the tentorium shifted ventrally, the basion and ventral portion of the supraoccipital bone shifted dorsally and caudally, respectively. None of the PCs discriminated subpopulations based on sex (Figure 2a) or breed groups (Figure 2b). Western European cat breeds demonstrated the largest mean caudal fossa size and Asian cats the smallest; however, centroid sizes were not significantly different between breed groups (P = 0.432) (Figure 3).

Figure 2

Principal component (PC)1 vs PC2 of the symmetric component displaying PC scores classified by (a) sex and (b) breed

Figure 3

Box and whisker diagram of centroid size among breed groups. The horizontal line within each box represents the median

After controlling allometry by regressing out isometric size, PC1 accounted for 20.3% and PC2 16.0% of the shape variation, cumulatively 36.3%. Overall shape trends matched the raw data in terms of direction but varied slightly in increments. Size-corrected PCA revealed no segregation of PC scores between males and females (Figure 4a), nor was there any clustering among breeds (Figure 4b).

Figure 4

Principal component (PC)1 vs PC2 after controlling for allometry displaying PC scores classified by (a) sex and (b) breed

Occipital bone classification

Three cats displayed zero internal concavities along the vermiform impression, 14 displayed one concavity, eight cats displayed two and seven cats displayed three (Figure 5 and Tables 1 and 2). No statistically significant differences were identified between the number of concavities along the mid-sagittal vermiform impression of males compared to females (P = 0.917), nor was there significant difference between the mixed breeds and purebreds (P = 0.634). No significant correlation was identified between the number of concavities and age (P = 0.527), PC1 (P = 0.562), PC2 (P = 0.873) and centroid size (P = 0.086).

Figure 5

Concavities along the vermiform impression: (a) zero, (b) one, (c) two, (d) three

Table 1

Relationship between vermiform impression morphology and sex

Concavities	Male	Female
0	2 (11)	1 (8)
1	8 (42)	6 (46)
2	5 (26)	3 (23)
3	4 (21)	3 (23)
Total	19 (100)	13 (100)

Data are n (%)

Table 2

Relationship between vermiform impression morphology and breed group

Concavities	Purebred	Mixed breed
0	2 (15)	1 (5)
1	5 (38)	9 (47)
2	3 (23)	5 (26)
3	3 (23)	4 (21)
Total	13 (99)	19 (99)

Data are n (%)

Discussion

A wide range of morphometric variation of the caudal fossa and foramen magnum was observed in this study population of neurologically normal cats, with no identified links to breed, sex or age. Because PC shape trends were similar between the raw data and the regression residuals, and there were no significant differences in centroid sizes between breed groups, we conclude that allometry had negligible influence on shape differences of the caudal fossa.

Shape variability demonstrated by PC1 may be interpreted anatomically as a lengthening of the exoccipital bones occurring alongside a relative dorsoventral flattening of the entrance to the caudal fossa caused by dorsal shifting of the dorsum sellae. Rostral shifting of the roof of the caudal fossa reflects an alteration in space distribution. A previous morphometric study categorised feline skulls into three phenotypically different skull formations: rounded, triangular and cuneiform. ¹³ This study identified a frequent variant of the round-shaped skulls where the foramen magnum extended more distantly between the occipital condyles thereby acquiring a bilaterally narrowed oval shape, similar to the findings of the current study. Variability of rostroventral vs rostrodorsal directions of this shift among neighbouring landmarks of the caudal roof of the fossa demonstrates an irregular contour of this internal bony surface. The vermiform impression is described in dogs as an irregular excavation of the median portion on the cerebellar surface of the squamous part of the occipital bone. ¹⁴ This is, to our knowledge, the first description of this anatomical feature specifically in the cat.

Shape variability demonstrated by PC2 may be interpreted anatomically as an overall dorsoventral flattening of the entrance to the caudal fossa owing to ventral shifting of the osseous tentorium cerebelli. Caudal extension of the foramen magnum coinciding with relative dorsoventral narrowing of the foramen reflects an overall redistribution of space. The ventral portion of the supraoccipital bone shifted caudally, independently of the more dorsal landmarks, demonstrating a variable caudal angulation of this site relative to the internal contour of the caudal fossa. Similar findings have been reported in a recent MRI study of cats which described variants of the ventral aspect of the supraoccipital bone of cats as straight throughout, caudally angulated, blunt ended and/or ventrally thickened. ¹⁵ The same study also found that cats could be divided into those with a thin and those with a thick occipital bone. Compared with MRI, CT has a higher sensitivity for accurately displaying osseous contours, and adds further validation to these findings.

Morphology of the external squamous part of the occipital bone and foramen magnum of cats has been described in a study involving gross morphology of 50 European cat cadavers. ¹⁶ Two morphological patterns of the squamous part of the occipital bone were identified; a triangular shape and a semi-oval shape, denoting normal variation of this external surface among European cats. None of the specimens in this previously reported study displayed a dorsal notch, nor any other defect at the foramen magnum. The authors concluded that, in the European cat, the foramen magnum is free from pathology and its shape is conservative. In contrast, a morphometric study of 69 purebred cat skulls identified two individuals with a keyhole-shaped foramen. ¹³ Dogs display a wide diversity of shape of the foramen magnum, many of which are considered as physiological variations of morphology.^8,17 It is apparent that a degree of physiological variation is also present in the cat and that the spectrum of morphologies observed in purebreds is also seen in mixed-breed cats. From a clinical perspective, this variation is important to recognise so that pathological processes are not falsely assigned.

The majority (69%) of the study population displayed one or two concavities along the vermiform impression on median plane CT images. No sexual dimorphism was identified, nor did these concavities differ between purebreds and mixed breeds, nor correlate with age. Concavities along the vermiform impression have not previously been described. A certain degree of care must be taken comparing the appearance of the caudal fossa on CT with the anatomy. Post-mortem examinations to confirm the shape of the caudal fossa were not performed because none of these clinical cases were available for necropsy examination. The high spatial frequency allowed by CT, however, ensures a detailed and accurate representation of the osseous surface. ¹⁸ Although the current study did not identify significant differences between breed groups or sexes, or correlate with age, it is evident that the shape of this vermiform impression is not uniform among cats and these variants should be clinically recognised.

A limitation of this study is the relatively small sample size. The lack of segregation in the PCA and, likewise, the lack of differences among vermiform impression groups may reflect the small numbers of individuals representing each breed, age and sex, and thus the inability to achieve statistical significance. Categorisation of vermiform impression concavities was somewhat subjective and prone to bias due to the use of only one evaluator. Additional studies inclusive of larger groups of feline breeds would be recommended to further investigate interbreed morphology differences. Breeds of particular interest are those that are brachycephalic, as brachycephaly has been shown in dogs to be associated with Chiari-like malformation and occipital dysplasia.^17,19 Further studies could also include lateralised landmarks along the caudal fossa, not included in the current study, which may uncover further variants.

Conclusions

A wide range of inter-breed morphometric variation of the feline caudal fossa was observed in this population, which was not linked to age or sex, demonstrating that caudal fossa anatomy is not homogeneous among cats. The findings support and expand on those previously reported.^13,15,16 An established range of normality is important for accurate discrimination between pathological changes and normal anatomical variants, and for the recognition of potential trends associated with disease in this popular companion animal.