Breeding of dogs in accordance with breed standards and by use of closed stud registers, which were developed approximately 100 years ago, has resulted in different physical characteristics in domestic dogs (Canis lupus familiaris) of the various pedigree breeds. Within some pedigree breeds, selection for physical traits considered desirable by dog breeders has resulted in extreme phenotypes for certain characteristics. Some of these phenotypes are associated with health benefits, but many are associated with negative effects on the health and welfare of dogs. These detrimental effects may be directly related to expression of a particular selected phenotype or indirectly related to expression of an unrelated coselected phenotype.
Selective breeding has resulted in adverse health effects in dogs of certain breeds that have a brachycephalic head conformation. Dogs have historically been categorized as having dolichocephalic, mesaticephalic, or brachycephalic head conformations by use of various head conformation (cephalic) indices; 2 of these indices1,2 are more widely accepted3,4 than other indices. The exact demarcation among dolichocephalic, mesaticephalic, and brachycephalic head conformations is poorly defined; 1 author1 classified dogs as brachycephalic, mesaticephalic, or dolichocephalic on the basis of a ratio of skull width to skull length of 0.81, 0.52, or 0.39, respectively. In dogs of brachycephalic breeds, there is marked shortening of the rostral aspect of the skull, particularly the facial bones, nasal cavity, and frontal sinuses, and the orbits are widely spaced and round. Such dogs often have prognathism. In conjunction with a short rostral aspect of the head, dogs of brachycephalic breeds have dorsal rotation of the rostral aspect of the maxilla. These dogs have canine teeth positioned in a nearly horizontal orientation, an altered position of the nasal turbinates, small frontal sinuses (or absent frontal sinuses in dogs with extreme brachycephalia), and a different angle of the nasolacrimal drainage pathway, compared with dogs of other breeds.5 Dorsal rotation of the rostral maxilla in these dogs results in a smaller craniofacial angle,6 compared with dogs of other breeds. The gene associated with a brachycephalic head shape has been mapped to a region on canine chromosome 1 and seems to be common to all dogs of brachycephalic breeds. Candidate genes within this chromosome region that may be associated with brachycephalia include THBS2 and SMOC-2, although there is a high probability that genes in other chromosome regions are modified in brachycephalic dogs.7,8
Dogs of brachycephalic breeds, including Boxers, English Bulldogs, French Bulldogs, Pugs, and Boston Terriers, are popular pets. One reason that has been proposed for the popularity of these breeds is the similarity between the brachycephalic head shape in those dogs and the head shape of human infants.9 The popularity of brachycephalic dogs as pets has resulted in breeding selection for physical appearance rather than for function. Survival of dogs with extreme brachycephalia may only be possible in some instances with breeding, medical, or surgical interventions (eg, artificial insemination and cesarean section in English Bulldogs10). Brachycephalic head conformation is correlated with high bite strength and is considered to impart a selective advantage in certain groups of wild carnivora (eg, hyenas [which are able to crush bone with their jaws] and extinct scavengers); this perceived benefit is the basis for selective breeding of dogs used for fighting.11,12 Comparison of head conformations among dogs of different breeds and dogs within a breed is possible by use of head conformation indices1,2; dogs that have similar head conformation index values have similar head shape characteristics and predispositions to particular diseases. Dogs of brachycephalic breeds are predisposed to the development of a variety of diseases affecting the upper airways, eyes, facial morphology, and CNS. These disease predispositions can be directly or indirectly attributed to the brachycephalic head phenotype; some examples include cleft palate and lip, brachycephalic obstructive airway syndrome, quadrigeminal cysts, and gliomas.9,13–15
Examination of physical characteristics of pedigree dog breeds may be useful in understanding the anatomic basis of a variety of diseases. Although head conformation indices provide objective measures of the degree of brachycephalia in dogs, they are not accurate measures of other physical characteristics that are related to brachycephalia. Development of such physical characteristics is presumably mediated through expression of modifying genes other than those responsible for brachycephalic head conformation. In particular, the head conformation characteristics associated with a small craniofacial angle (which affects the physical characteristics of eyes, airways, and CNS) cannot be predicted with traditional head conformation indices. Descriptions of the physical characteristics of the brain associated with a small craniofacial angle are extremely limited. One physical CNS characteristic that seems to be related to head conformation and may be directly related to the position of ethmoid turbinates (which is different in brachycephalic dogs than in dogs of other head conformations) is the position of olfactory bulbs. Olfactory bulb position may be best determined by evaluation of MRI images but can also be determined by evaluation of radiographic and CT images of the head. A quantitative measure of extreme brachycephalia would be useful for the prediction of brachycephalic-related disease predispositions in dogs and for the selection of dogs for breeding. The purposes of the study reported here were to determine the association between head conformation (brachycephalic, mesaticephalic, and dolichocephalic) and olfactory bulb angle and orientation, to determine the olfactory bulb angle and orientations associated with brachycephalia, and to determine whether the degree of ventral olfactory bulb orientation correlates with the degree of brachycephalia (which would allow that measure to be used as an indicator of extreme brachycephalia).
Head conformation index calculated by use of skull width and skull base length (prosthion to basion) measurements
Head conformation index calculated by use of skull width and skull length (prosthion to inion) measurements
Magnetom, Siemens AG, Erlangen, Germany.
Magnevist, Bayer HealthCare Pharmaceuticals, Newbury, West Berkshire, England.
GraphPad Prism, version 5.0, GraphPad Software Inc, La Jolla, Calif.
2. Stockard CR. The genetic and endocrine basis for differences in form and behavior. New York: The Wistar Institute of Anatomy and Biology, 1941.
6. Regodón S, Vivo JM, Franco A, et al. Craniofacial angle in dolicho-, meso- and brachycephalic dogs: radiological determination and application. Ann Anat 1993; 175:361–363.
7. Bannasch D, Young A, Myers J. Localization of canine brachycephaly using an across breed mapping approach. PLoS One 2010; 5:e9632.
8. Hunemeier T, Salzano FM, Bortolini MC. TCOF1 T/Ser variant and brachycephaly in dogs. Anim Genet 2009; 40:357–358.
9. Nöller C, Hueber J, Aupperle H, et al. New aspects of brachycephalia in dogs & cats basics: insights into embryology, anatomy & pathophysiology. Proceedings of the ACVIM Forum, San Antonio, Texas, USA, 2008;713–715.
10. Smith FO. Challenges in small animal parturition—timing elective and emergency cesarian sections. Theriogenology 2007; 68:348–353.
11. Tseng ZJ, Wang X. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). J Morphol 2010; 271:1386–1398.
12. Ellis JL, Thomason J, Kebreab E, et al. Cranial dimensions and forces of biting in the domestic dog. J Anat 2009; 214:362–373.
13. Foley CW, Lasley JF, Osweiler GD. Digestive system: abnormalities of companion animals: analysis of heritability. Ames, Iowa: Iowa State University Press, 1979;119–120.
15. Hedlund C. Brachycephalic syndrome. In: Bojrab MJ, ed. Current techniques in small animal surgery. 4th ed. Baltimore: The Williams & Wilkins Co, 1998;358–362.
18. Schwarz T, Sullivan M, Hartung K. Radiographic anatomy of the cribriform plate (lamina cribosa). Vet Radiol Ultrasound 2000; 41:220–225.
19. Hayes HM, Priester WA, Pendergrass TW. Occurrence of nervous tissue tumors in cattle, horses, cats and dogs. Int J Cancer 1975; 15:39–47.
21. Weidenreich F. The brain and its role in the phylogenetic transformation of the human skull. Trans Am Philos Soc 1940; 31:320–442.