Eriksen et al.

BMC Veterinary Research (2016) 12:8

DOI 10.1186/s12917-016-0634-7

RESEARCH ARTICLE Open Access

Cranial morphology in the brachygnathic

sheep
T. Eriksen1,3*, M. Ganter2, O. Distl3 and C. Staszyk1,4

Abstract
Background: Craniofacial morphology of sheep with phenotypically observed mandibular distocclusion was
analysed using the multivariate techniques principle component analysis and cluster analysis in order to test
whether different types of craniofacial malformations can be distinguished.
Results: The results showed 8 principal components with a variance of 82.72 % in the database. The method
creates new variables then used in the Cluster analysis indicating 7 clusters with 3 different facial types: Normal,
prognathia inferior and brachygnathia inferior.
Conclusion: The brachygnathic facial type was mainly characterised as a shortened mandible, the upper jaw
is not significantly involved. The correlations to the temporomandibular joint were shown. Molar and
premolar malocclusions were revealed in two of three Clusters. Phenotypical distocclusion was not a single
criterion for the affected sheep.
Keywords: Brachygnathia inferior, Cluster analyse, Principal component analyse, Sheep, Skull

Background measurements in these parameters. Measurements of

Dysgnathia appears as brachygnathia inferior [1–4] or the mandibular distocclusion were frequently based
brachygnathia superior [5]. Other terms used for on the distance of the rostral point of the incisor to
brachygnathia inferior are overbite, undershot, parrot the dental pad [5, 9, 10]. As indicated by [8] with de-
mouth, prognathia superior whereas brachygnathia su- scriptive statistic programs, different particular parts
perior is referred as underbite, overshot, prognathia of the mandible succumb to shortening; other cranio-
inferior [1, 3, 5, 6]. Dysgnathia is a common congenital facial abnormalities in sheep were not identified in
anomaly in sheep that could be reproduced in a breeding this study.
trial with East Friesian sheep [1, 7]. Due to the shorten- As found in the above cited literature (except [8]),
ing of specific parts of the mandible, the ovine craniofa- measurements were carried out using macerated skulls.
cial malformation is best described as brachygnathia Today, due to the progressive development of x-ray
inferior in sheep [1, 8]. technology, animals can also be assessed in vivo. As a
Different measurement approaches have been chosen starting point for the following study, advanced tech-
in sheep with brachygnathia inferior. Nordby et al. [5] niques used for evaluation of x-rays in orthodontics
found a shortening of the interalveolar part of the man- human medicine were adopted. The laterolateral x-ray
dible and an elongation of the rostral part of the maxilla. can be analysed by means of cephalometric measure-
The measurements of premolar/molar parts were actu- ment points. Structures or positional relationships of
ally also considered by [5] but sheep with brachygnathia skull bones, soft tissues, growth forecasts or treatment
inferior did not show any deviations from standard options will be shown.
According to [11], there is no uniform nomencla-
ture or classification for the different types of dys-
* Correspondence: [email protected]
1
Institute of Anatomy, University of Veterinary Medicine Hannover, gnathia. Even today, the starting point for diagnosing
Bischofsholer Damm 15, D-30173 Hannover, Germany dysgnathia is the classification according to [12] based
3
Institute for Animal Breeding and Genetics, University of Veterinary Medicine on molar teeth-occlusion. This is the same also
Hannover, Bünteweg 17p, D-30559 Hannover, Germany
Full list of author information is available at the end of the article internationally.

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 2 of 8

Angle-Class I defines normocclusion; Angle-Class II clinically healthy sheep. The next generations have also
classifies the rostral placement of the maxillary first been used for breeding and mated with each other as
molar and is subdivided into two groups. Shortened well as with the founder animals.
mandible and elongated maxilla and the mandible in Latero-lateral x-rays of the skull were taken, which
posterior position and the maxilla in anterior position included cadaveric and living animals, whereas the
[13]. Angle-Class III is used to classify a caudal place- condition of the animals showed no differences in
ment of the maxillary first molar. quality. The radiographic reference points and
Additionally the different affected two Angle Classes methods from previous study were applied for our
could share in altered region (alveolar, skeletal) and analysis [8]. The reference points are dorsal point of
changes in main directions (vertical, sagittal and trans- the frontonasal suture (1), external occipital protu-
verse) [11]. Gattinger and Obwegeser [14] divided the berance (2), suture between maxilla and the incisive
malocclusion in the hypo- / hyperplasia of mandible and bone (3), ventral point of the sphenoid bone (4), caudal
maxilla. point of the alveolar process of the first incisor (5), dor-
The projection onto affected sheep, we are trying to sum nasi (6), rostral point of the rostral process of
implement in this study. A valid normocclusion for the the nasal bone (7), rostral point of the incisive bone
sheep shall be found. Additional changes of other bones (8), labial border of the incisors (9), rostral point of
of skull which are affected by malformations will be the dental pad (10), rostral point of the mandible
proved. Based on the current human medical knowledge, (11), caudo-dorsal part of the mandibular condyle
we will try to find a descriptive definition to represent (12), dorso-median point of the mandibular fossa
the exact localization of changes by applying multivariate (13), ventral point of the corpus mandibulae (14),
statistics. caudal point of the ramus mandibulae (15), rostral
point of the lower second premolar (16), rostral point
Methods of the upper second premolar (17), caudal point of
Digital radiographs of the head were taken from 101 ju- the lower third molar (18), caudal point of the upper
venile and adult sheep including mainly East Friesian third molar (19), designed intercept point of the tan-
milk sheep. These were part of a breeding experiment gents from references points 14 and 15 (20) (Fig. 1
from 2005 to 2008 conducted over four generations ap- [8]). From these reference points the reference lines
proved by the federal state government of Hannover, are derived: Baseline (A), bridge-line (B), mandible-
Germany (AZ: 05/ 918). An obviously affected goat with line (C), skull-line (D), sphenoid-mandible-line (E)
brachygnathia inferior was mated to both affected and (Fig. 2 [8]). Sixteen measurements were determined

Fig. 1 Laterolateral radiograph of the skull of a 6-year-old female sheep. Numbers indicate reference points ([8], figure reproduced with the
permission of the publisher)

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 3 of 8

Fig. 2 Laterolateral radiograph of the skull of a 6-year-old female sheep. Characters indicate reference lines (blue), perpendicular (orange) and
measure-lines (green) ([8], figure reproduced with the permission of the publisher)

by reference points, reference lines and perpendiculars was used to remove the fixed effects of sex and age. The
(Figs. 3 and 4 [8]). residuals were standardized onto a mean of zero and a
The measurements were standardized to a relative standard deviation of 1.
scale using the skull-line to minimize the effects of the Principal Component Analysis (PCA) was used to cal-
different skull sizes. A generalized linear model (GLM) culate eigenvalues and eigenvectors. Eigenvalues larger

Fig. 3 Laterolateral radiograph of the skull of a 6-year-old female sheep. Characters indicate the mandible-line (blue), perpendicular (orange) and
measure-lines (green) ([8], figure reproduced with the permission of the publisher)

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 4 of 8

Fig. 4 Laterolateral radiograph of the skull of a 6-year-old female sheep. Characters indicate measured angles (turquoise) ([8], figure reproduced
with the permission of the publisher)

than one were significant. The factor scores for the indi- mandible and the third PC by mandibular distocclusion.
viduals were calculated for new variables. The following The fourth PC was mainly composed of measurements
Cluster analysis summarized the multidimensional data of the cranium and the fifth PC of incisor length and
space. measurements of the pars alveolare from the check
teeth. The sixth PC was characterised by measurements
Results of the mandible and maxilla. The seventh PC was mainly
PCA could extract eight principal components (PC) with composed of measurements describing the temporo-
eigenvalues >1 using measurements normalized onto a mandibular joint and the eighth PC of measurement of
standard normal distribution. The variance captured by the incisive bone.
these 8 PCS amounted to 82.72 % (Table 1). A scree plot For each individual sheep the factor scores were evalu-
graphically shows the variance of each PC (Fig. 5). ated and used as a new variable in the cluster analysis
The loadings of the eigenvectors indicate the propor- with the Ward method. The cubic clustering criterion
tion of variance attributable to the single measure- (CCC) was used to differentiate significant from non-
ments (Table 2). significant clusters. In total, seven significant clusters of
The first PC was mainly composed of the angles. The the craniofacial malformation could be distinguished
second PC was characterised by variables describing (Fig. 6). The largest cluster (cluster no. 7) contained 33
animals (40 %) and the smallest cluster (cluster no. 18)
Table 1 Variance of the Principal component consisted of 2 animals (Table 3).
Eigenvalue Difference Proportion Cumulative The common characteristic of cluster 14 with nine ani-
1 6.6145437 1.5596872 0.245 0.245 mals is an elongation of the incisive bone (I), the cerebral
2 5.0548565 1.6915844 0.1872 0.4322
cranium (J) and the shortening of the maxilla (H). The
temporomandibular joint (G) was in caudal position.
3 3.3632722 1.1787174 0.1246 0.5568
Cluster 32 differs mainly in shortening of the incisive bone
4 2.1845548 0.5926245 0.0809 0.6377 (I) and the cerebral cranium (J). Cluster 11 shows an
5 1.5919303 0.2637301 0.059 0.6966 elongation of the maxilla (H) and the nose (B and F). The
6 1.3282002 0.1990405 0.0492 0.7458 temporomandibular joint (G) was in rostral position. The
7 1.1291597 0.0617238 0.0418 0.7876 measure-lines C and E (mandible-line) were reduced and
8 1.0674359 0.1894865 0.0395 0.8272
the measure-line M (incisor length) was elongated like the
rest in the upper types. Only clusters 32 and 14 were
9 0.8779494 0.1062893 0.0325 0.8597
phenotypically classified as brachygnathic sheep.

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 5 of 8

Fig. 5 Scree plot. The variance of each PC

Table 2 Loadings of the eigenvectors (standardised measurements of the skull) for principal components (Prin1- Prin8)
Prin1 Prin2 Prin3 Prin4 Prin5 Prin6 Prin7 Prin8
b 0.260512 0.16943 0.138514 −0.31995 0.004763 −0.109674 0.024279 0.166586
a 0.210661 0.239707 0.316499 0.081616 −0.103967 −0.075809 −0.063305 −0.003094
F 0.203304 0.08517 −0.020909 −0.343357 −0.067752 −0.282682 0.040735 0.289523
g 0.048255 −0.222811 0.131433 −0.059791 −0.119593 0.206556 −0.437608 −0.053805
i −0.059117 0.226485 0.169766 0.047072 −0.043878 0.479737 −0.020836 0.443369
h 0.279343 0.025555 0.042639 −0.311058 0.014902 −0.308813 0.032494 −0.127343
j 0.044539 0.176961 0.311619 0.401739 −0.129603 −0.138888 −0.079028 −0.192877
l 0.129432 0.184688 0.165806 −0.187116 0.313292 0.288096 0.010792 −0.141651
s 0.107072 0.211717 0.229355 0.374218 −0.072467 −0.219437 0.128797 −0.076414
e 0.177303 0.339295 −0.001585 0.085101 0.030029 0.037648 −0.000223 0.003641
k 0.083634 0.191221 0.152947 0.00207 0.532159 0.060321 0.098297 −0.249258
m 0.026714 −0.064074 0.167117 −0.132598 0.48245 −0.193502 −0.113828 0.053702
n −0.111563 −0.12682 0.385271 −0.184432 −0.234753 −0.012267 −0.03785 −0.16482
o 0.141251 0.106741 −0.426021 0.19523 0.131828 −0.103627 −0.088336 0.006431
p −0.1376 −0.109094 0.434017 −0.178565 −0.109052 0.100598 0.04942 0.016676
q 0.216362 0.191487 −0.082302 0.006879 −0.209547 0.034904 −0.334733 0.202341
r −0.104137 0.249953 0.023715 0.051262 −0.164301 −0.04845 0.47971 0.280733
c 0.272892 0.17652 −0.156788 −0.019913 −0.136846 0.254788 −0.079413 −0.192924
t 0.243845 0.081729 −0.074399 −0.107708 −0.086393 0.349988 0.311518 −0.190954
u 0.206073 0.091023 −0.076007 −0.122156 −0.193091 0.050122 −0.280342 −0.226584
a1 0.302149 −0.215531 0.060091 0.036928 −0.027133 −0.030557 0.027869 0.189831
a2 0.294529 −0.226151 −0.027649 −0.010197 0.005965 0.052971 0.072626 0.224069
a3 0.17492 −0.266372 −0.023934 −0.05119 −0.033548 0.206697 0.398068 −0.076868
a4 0.226399 −0.209417 0.131739 0.203875 0.060208 −0.162003 −0.014389 0.246418
a5 0.11023 −0.124019 0.104516 0.239457 0.318966 0.229965 −0.173376 0.288112
a6 0.255131 −0.257778 0.016076 0.182813 −0.046198 0.007964 0.129697 −0.170123
a7 0.265894 −0.245075 0.093553 0.198069 −0.05404 0.032331 0.088314 −0.086675

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 6 of 8

Fig. 6 Cluster-analyse in the tree dendrogram. Name of clusters and observations. The first row represents each individual sheep. The remaining
branches show the potential clusters

Clusters 9, 7 and 12 were classified as normal or Cluster 7 differs from cluster 9 and 12 with an elong-
prognathia inferior and were identified by the ation of the cerebral cranium (J). Cluster 12 is char-
measure-lines p, o and n. The measure-lines C and E acterised by an elongated maxilla (H) and shortening
were elongated. The measure-lines B and F, affecting of the incisive bone (I) and cerebral cranium (J). Only
the nose, were in median or in elongation. Differences in Cluster 12, the temporomandibular joint (G) was
were identified in measure-lines which concerned the in caudal position (Fig. 7).
upper jaw. Cluster 9 was characterised by an elon-
gated incisive bone (I) and baseline (A) and shorten- Discussion
ing of the maxilla (H) and cerebral cranium (J). Facial types could be defined in our analysis that could
applied for the description of dysgnathia. The cluster 32,
Table 3 Observation (n) frequency of different cluster types
11 and 14 were classified as affected sheep with
shortening of the mandible. The discrepancy between
Cluster (Type) Frequency (n) Percent (%)
the position of the mandibular incisor and the dental
7 33 39.76
pad [1, 10] was not a single criterion for an affected
9 20 24.1 sheep.
11 8 9.64 The craniofacial malformation should be defined as
12 6 7.23 brachygnathia inferior because the lower jaw is in all
14 9 10.84 cases shortened [5, 8]. The upper jaw is involved but of
18 2 2.41
only limited informative value for the definition of the
brachygnathia inferior. Molar and premolar malocclu-
32 5 6.02
sions of different types were shown (measure-line N). In

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 7 of 8

Fig. 7 Means and standard deviations for all animals in the certain clusters. Positive and negative standard deviation (end of the whiskers) from
the mean (top of the box) of the population

comparison to the horse, it was interesting that in sheep In human medicine, the focus on the temporoman-
the malformation was only restricted to the rostral part dibular joint was in correlation to the mandible bone
of the mandible. The molar and premolar occlusion was [16, 17]. There were examinations with focus on the
commonly not affected [15]. temporomandibular joint and the dysgnathia. As a
The phenotypical classification was not in accord- result, in Angle Class II the fossa mandibularis shifts
ance with cluster 11, even though the shortening of in the caudal position [18, 19]. In order to achieve
the mandible exists. The temporomandibular joint more detailed information about the correlation of
(measure-line G) was in rostral position and the man- the temporomandibular joint and the brachygnathia
dibular incisor (measure-line M) was elongated, so inferior a three-dimensional view like the computer
the length of the mandible was apparently corrected. tomography (CT) is vital. Based on cross-sectional
In our study there were statistically more affected images the skull can be reconstructed with special
sheep than from a clinical point of view shown. The software programs.
temporomandibular joint was in correlation with the
mandible in brachygnathic sheep. Conclusions
The other 3 facial types were classified as prog- The brachygnathia inferior is characterised as a signifi-
nathia inferior or normal. In the cluster 9 and 7, the cant shortened mandible. The distance between the pos-
maxilla was elongated with a more rostral location ition of the mandibular incisor and the dental pad is not
from the temporomandibular joint. In contrast, in a single criterion.
cluster 12, the temporomandibular joint was in the
caudal position. What remains for discussion is the Abbreviations
CCC: cubic clustering criterion; CT: computer tomography; Fig.: figure;
influence of the temporomandibular joint to the GLM: generalized linear model; No.: number; PC: principal component;
dysgnathia. PCA: principal component analyse.

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Eriksen et al. BMC Veterinary Research (2016) 12:8 Page 8 of 8

Competing interests 18. Baccetti T, Antonini A, Franchi L, Tonti M, Tollaro L. Glenoid fossa
The authors declare that they have no competing interests. position in different facial types: a cephalometric study. Br J Orthod.
1997;24(1):55–9.
19. Giuntini V, De Toffol T, Franchi L, Baccetti T. Glenoid fossa position in Class II
Authors’ contributions malocclusion associated with mandibular retrusion. Angle Orthod.
TE carried out the study including the gathering of roentgenologic aspects, 2008;78(5):808–12.
statistical analysis and evaluation and drafted the manuscript. CS and OD
conceived the study, participated in its design and coordination. OD
additionally supported in drafting the manuscript. MG provided support for
the data gathering with regards to roentgenologic aspects. All authors read
and approved the final manuscript.

Author details
1
Institute of Anatomy, University of Veterinary Medicine Hannover,
Bischofsholer Damm 15, D-30173 Hannover, Germany. 2Clinic for Swine,
Small Ruminants, Forensic Medicine and Ambulatory Service, University of
Veterinary Medicine Hannover, Bischofsholer Damm 15, D-30173 Hannover,
Germany. 3Institute for Animal Breeding and Genetics, University of
Veterinary Medicine Hannover, Bünteweg 17p, D-30559 Hannover, Germany.
4
Institute of Veterinary Anatomy, Histology and Embryology, Faculty of
Veterinary Medicine, Justus-Liebig-University Giessen, Frankfurter Str. 98,
D-35392 Giessen, Germany.

Received: 13 April 2015 Accepted: 7 January 2016

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