Relationship between breed, hemivertebra subtype,

and kyphosis in apparently neurologically normal

French Bulldogs, English Bulldogs, and Pugs

Richard Ryan bmed vet OBJECTIVE

To investigate whether hemivertebra subtype as determined via CT was
Rodrigo Gutierrez-Quintana mvz , mvm associated with breed and Cobb angle (a measure of the degree of spi-
Gert ter Haar dvm, phd nal curvature) in apparently neurologically normal French Bulldogs, English
Steven De Decker dvm, phd Bulldogs, and Pugs.
ANIMALS
Received February 14, 2018. Client-owned French Bulldogs (n = 58), English Bulldogs (30), and Pugs (12)
Accepted May 11, 2018.
with thoracic hemivertebrae that underwent CT for reasons unrelated to
spinal disease.
From the Department of Veterinary Clinical Science
and Services, Royal Veterinary College, University of PROCEDURES
London, North Mymms, AL9 7TA, England (Ryan, ter
Haar, De Decker); and the Department of Small Ani- CT scans of each dog were evaluated, and hemivertebrae were catego-
mal Sciences, School of Veterinary Medicine, College rized by subtype (ventral aplasia, ventral hypoplasia, lateral aplasia, lateral
of Medical, Veterinary and Life Sciences, University of hypoplasia, ventrolateral aplasia, ventrolateral hypoplasia, ventral and me-
Glasgow, Glasgow, G61 1QH, Scotland (Gutierrez- dian aplasia, ventral and median hypoplasia, and symmetric hypoplasia). The
Quintana). Dr. ter Haar’s present address is Specialist-
ische Dierenkliniek Utrecht, Middenwetering 19, 3542 Cobb angle was measured, and kyphosis was defined as a Cobb angle > 10°.
Utrecht, Netherlands. Results were compared among breeds.
RESULTS
Address correspondence to Dr. De Decker
([email protected]). 243 hemivertebrae were identified in the French Bulldog group, 100 in the
English Bulldog group, and 19 in the Pug group. Breed was significantly as-
sociated with hemivertebra subtype. Pugs were more likely than French and
English Bulldogs to have ventral hypoplasia and less likely to have ventral and
median hypoplasia. English Bulldogs were more likely than French Bulldogs
to have ventral and median hypoplasia. Compared with other hemivertebra
subtypes, ventral hypoplasia was associated with a greater Cobb angle and a
higher likelihood of kyphosis. Pugs were more likely than the other 2 breeds
to have kyphosis.
CONCLUSIONS AND CLINICAL RELEVANCE
Pugs had a different spectrum of hemivertebra subtypes than French and
English Bulldogs in this study. Additional research is necessary to evaluate
the clinical relevance of this finding. (Am J Vet Res 2019;80:189–194)

T horacic congenital vertebral body malforma-

tions are common in clinically normal, so-
called screw-tail brachycephalic breeds, such as
high prevalence in neurologically normal French
Bulldogs, English Bulldogs, and Pugs.
Hemivertebrae are most common in the midtho-
French Bulldogs, English Bulldogs, and Pugs.1 Al- racic region, can affect single or multiple vertebrae,
though there is some discussion about the most ap- and can be associated with spinal curvature abnor-
propriate terminology,2 congenital vertebral body malities, such as kyphosis and scoliosis.3,6,7 Although
malformations can be classified by defects of seg- the degree of spinal curvature can be quantified in
mentation, including block vertebrae, and defects various ways, the measuring technique described by
of formation, including hemivertebrae. Hemiverte- John Robert Cobb is considered the gold standard.8
brae are the most common type of vertebral mal- This method involves measurement of the angle, re-
formations, and several studies1,3–5 have revealed a ferred to as the Cobb angle, of the most tilted ver-
tebra. The Cobb angle is derived by measuring the
ABBREVIATIONS angle between a line superimposed on the cranial
LA Lateral aplasia
LH Lateral hypoplasia vertebral end plate of the vertebra cranial to a given
SH Symmetric hypoplasia vertebra and a line superimposed on the caudal verte-
VA Ventral aplasia bral end plate of the vertebra caudal to that given ver-
VH Ventral hypoplasia tebra.8 This angle can be measured manually or with
VLA Ventrolateral aplasia
VLH Ventrolateral hypoplasia various digital methods, including computer-assisted,
VMA Ventral and median aplasia automatic, and smartphone-application methods. All
VMH Ventral and median hypoplasia methods have been associated with high degrees of

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 reliability, with digital methods providing slightly signs. All dogs without neurologic signs in that study
better results.9 had undergone thoracic CT while sedated or anesthe-
Although hemivertebrae are typically considered tized for reasons unrelated to spinal or orthopedic dis-
incidental findings on diagnostic imaging, they have ease between October 2010 and February 2016. Dogs
the potential to cause clinical signs of progressive had been excluded from that group if medical records
spinal cord dysfunction.1,3,10,11 The pathophysiologic or imaging studies were incomplete or unavailable for
mechanism underlying the clinical signs is consid- review or if the reason for evaluation was a gait abnor-
ered multifactorial.10 Results of some studies3,7 indi- mality. Most received no neurologic examination and
cate that the presence and severity of kyphosis could were considered apparently neurologically normal if
be risk factors for development of clinical signs in they had been evaluated for a nonneurologic condition
dogs with hemivertebrae, whereas results of another and none of the clinical notes included mention of any
study1 suggest that breed could also be a risk factor. previous or existing gait or neurologic abnormalities. To
More specifically, thoracic hemivertebrae have been be included in the present study, dogs were required
suggested to be of greater clinical importance in Pugs to have been considered as apparently neurologically
than in French and English Bulldogs.1 normal and to have had ≥ 1 thoracic hemivertebra diag-
The reason Pugs with hemivertebrae are more nosed in the previous study.1
likely to develop clinical signs than other screw-tail
brachycephalic dogs is unclear. Although other fac-
tors cannot be excluded, breed-specific differences
may exist in hemivertebra morphology. In both hu-
man and veterinary medicine, efforts have been made
to categorize hemivertebrae into different subtypes
on the basis of their radiographic appearance.5,12,13
In 1 veterinary study,13 hemivertebrae in dogs were
classified into 6 types and several subtypes by use of
the human Nasca classification system, whereas in a
more recent study,5 they were classified into 6 sub-
types in accordance with another human classifica-
tion system.
Recognition of and interest in brachycephalic
breed-related health disorders are increasing,14,15 and
radiographic screening programs for thoracic hemi-
vertebrae have been considered.16,17 However, evalu-
ation of the impact of thoracic hemivertebrae on the
welfare of brachycephalic breeds is complicated by
their uncertain clinical importance, incompletely un-
derstood pathophysiologic mechanism, and possible
breed-specific anatomic differences.
The primary aim of the study reported here was
therefore to compare the spectrum of hemivertebra
subtypes among apparently neurologically normal
French Bulldogs, English Bulldogs, and Pugs. For this
purpose, a previously reported radiographic classifi-
cation system5 was adapted for use with CT images.
An additional objective was to determine whether
various hemivertebra subtypes were associated with
different degrees of kyphosis. We hypothesized that
Pugs would have a different spectrum of hemiverte-
bra subtypes than French and English Bulldogs and
that there would be an association between hemiver-
tebra subtype and the likelihood of kyphosis.

Materials and Methods Figure 1—Diagrams of the subtypes used to classify hemi-
vertebrae in dogs on CT examination. This system is based on
Animals a radiographic classification system, 5 which has been expand-
Dogs were selected for this retrospective cross-sec- ed to include the subtypes SH, VLH, and VMH. (Adapted from
tional study from among those included in a previous Gutierrez-Quintana R, Guevar J, Stalin C, et al. A proposed
radiographic classification scheme for congenital thoracic
retrospective study1 of the prevalence of thoracic ver- vertebral malformations in brachycephalic “screw-tailed” dog
tebral malformations in French Bulldogs, English Bull- breeds. Vet Radiol Ultrasound 2014;55:585–591. Reprinted
dogs, and Pugs with and without associated neurologic with permission.)

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 Data collection Degree of kyphosis was assessed by another ob-
In the previous study,1
information was re- server (SD) and objectively evaluated by measuring
trieved from the medical records of each dog re- the Cobb angle automatically by use of a commercial
garding signalment, reason for evaluation, and re- plug-in device as described elsewhere.7 For the purpose
sults of general physical examination on the date of the present study, kyphosis was defined as a dorsal
of the CT examination. The CT examination had spinal curvature with a Cobb angle > 10°. When mul-
been performed with a 16-slice helical CT scanner,a tiple hemivertebrae were present, the Cobb angle for
with dogs positioned in ventral recumbency. Im- each affected vertebral segment was obtained. Standard
ages had been acquired at 140 kVp and 120 mA in image archiving and communication system softwareb
helical mode, with a 2-mm slice thickness, –1 in- was used to evaluate all images.
terval between slices, 110-mm field of view, bone
and soft tissue reconstruction algorithms, and 512 Statistical analysis
X 512 matrix. After completion of transverse CT Data were analyzed with statistical software.c
scanning, sagittal, dorsal, and 3-D reconstructions Associations between breed and hemivertebra sub-
had been made. type (based on the proportion of a specific hemi-
For the present study, these images were inde- vertebra subtype, compared with the total number
pendently evaluated by 2 observers (RR and RG-Q) of observed hemivertebra in a given breed) and be-
for the presence and type of hemivertebrae. Each tween hemivertebra subtype and presence of ky-
identified hemivertebra was categorized into 1 of 9 phosis were evaluated with the χ2 test followed by
subtypes (VA or dorsal hemivertebra, VH or ventral post hoc analysis with the Mann-Whitney U test. As-
wedged vertebra, LA or lateral hemivertebra, LH or sociations between hemivertebra subtype and Cobb
lateral wedge-shape vertebra, VLA or dorsolateral angle were evaluated with the Kruskal-Wallis test fol-
hemivertebra, VLH, VMA or butterfly vertebra, VMH, lowed by post hoc analysis with the Mann-Whitney U
and SH or short vertebra; Figures 1 and 2) on the test. Values of P < 0.05 were considered significant;
basis of a previously reported radiographic classifica- Bonferroni correction of P values was performed for
tion system5 that was adapted for use with CT images. multiple comparisons.

Figure 2—Representative CT images showing a morphologically normal vertebra (A) and the hemivertebra subtypes VA (B),
VH (C), LA (D), LH (E), VLA (F), VLH (G), VMA (H), VMH (I), and SH (J) in the classification system of Figure 1.

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 Table 1—Number (%) of hemivertebra subtypes identified in CT images of apparently neurologi-
cally normal French Bulldogs (n = 58), English Bulldogs (30), and Pugs (12).
Subtype French Bulldogs English Bulldogs Pugs P value
VA 3 (1.2) 0 0 0.62
VH 16 (6.6) 10 (10) 19 (100) < 0.001
LA 25 (10.3) 5 (5) 0 0.16
LH 45 (18.5) 3 (3) 0 < 0.001
VLA 7 (2.9) 1 (1) 0 0.64
VLH 9 (3.7) 1 (1) 0 0.41
VMA 78 (32.1) 21 (21) 0 0.01
VMH 58 (23.9) 58 (58) 0 0.01
SH 2 (0.08) 1 (1) 0 1.00
Total 243 100 19 NA
NA = Not applicable.

Results vertebra, for a total of 19 hemivertebrae. All identified

hemivertebrae were of the VH subtype, and no other
Animals subtype was observed. The Cobb angle ranged from
A total of 100 dogs, consisting of 58 French Bull- 0.4° to 39.7° (median 25.3°; mean, 20.1°). Eleven Pugs
dogs, 30 English Bulldogs, and 12 Pugs, were includ- had kyphosis, and 1 had a Cobb angle exceeding 35°.
ed in the study. These dogs had undergone CT for
various clinical indications, including brachycephalic Association between breed
obstructive airway syndrome (n = 77), other respira- and hemivertebra subtype
tory disease (7), neoplastic disease (7), gastrointes- A significant (P ≤ 0.001) association was identi-
tinal disease (6), cardiac disease (2), and trauma (1). fied between breed and the hemivertebra subtypes
Eight-two dogs had multiple hemivertebrae, and 18 VH, VMH, LH, and VMA. Specifically, Pugs were
had a single hemivertebra. significantly more likely to be have the VH subtype
French Bulldogs—The group of French Bulldogs con- and significantly less likely to have the VMH subtype
sisted of 50 (86%) males and 8 (14%) females between than French Bulldogs (P < 0.001 for VH and P = 0.007
2 and 135 months of age (median, 19.4 months; mean, for VMH) and English Bulldogs (P < 0.001 for both
29.9 months) and weighing between 6.7 and 16 kg (me- subtypes). No significant difference was identified
dian and mean, 11.4 kg). Forty-nine (84%) French Bull- between French and English Bulldogs in the propor-
dogs had multiple hemivertebrae, and 9 (16%) had a sin- tions with the VH subtype; however, English Bulldogs
gle hemivertebra, for a total of 243 hemivertebrae. The were significantly (P < 0.001) more likely to have the
3 most common hemivertebra subtypes in this breed VMH subtype than French Bulldogs. French Bulldogs
were VMA (32.1% of all hemivertebrae), VMH (23.9%), were significantly (P < 0.001) more likely to have the
and LH (18.5%; Table 1). The measured Cobb angle LH subtype than English Bulldogs. French Bulldogs
ranged from 0.2° to 61.5° (median, 9.4°; mean, 17.9°). were also significantly (P = 0.001) more likely to have
Twenty-five (43%) dogs had kyphosis, and 10 (17%) dogs the VMA subtype than Pugs. No other significant dif-
had Cobb angles exceeding 35° (a value associated with ferences were identified between breeds in propor-
neurologic deficits7). tions with the LH and VMA hemivertebra subtypes
or proportions with the VLH, VLA, SH, VA, and LA
English Bulldogs—The group of English Bulldogs subtypes.
consisted of 20 (67%) males and 10 (33%) females
between 10 and 127 months of age (median, 21.0 Association between hemivertebra
months; mean, 37.4 months) and weighing between subtype and degree of spinal curvature
10.4 and 37.1 kg (median, 23.4 kg; mean, 24.6 kg). Overall, hemivertebra subtype was significant-
Twenty-seven (90%) English Bulldogs had multiple ly (P < 0.001) associated with the Cobb angle and
hemivertebrae, and 3 (10%) had a single hemiverte- with kyphosis. The VH subtype was significantly (P
bra, for a total of 100 hemivertebrae. The 3 most com- < 0.001) associated with higher Cobb angles and a
mon hemivertebra subtypes were VMH (58%), VMA higher likelihood of kyphosis, compared with all oth-
(21%), and VH (10%; Table 1). No English Bulldog had er hemivertebra subtypes combined. No significant
the VA subtype. The measured Cobb angle ranged associations were identified between the other sub-
from 2.4° to 40.0° (median, 11.1°; mean, 14.3°). Seven- types and Cobb angle or kyphosis.
teen (57%) dogs had kyphosis, and 1 (3%) had a Cobb Breed was significantly associated with kypho-
angle exceeding 35°. sis (P < 0.001). More specifically, kyphosis was more
Pugs—The group of Pugs consisted of 7 males and 5 common in Pugs (with hemivertebrae) than it was
females between 8 and 114 months of age (median, 36.5 in French Bulldogs (P < 0.001) and English Bulldogs
months; mean, 44.9 months) and weighing between (P = 0.002). No significant difference was identified
4.2 and 13.7 kg (median, 8.2; mean, 8.2 kg). Six Pugs between French and English Bulldogs in proportions
had multiple hemivertebrae, and 6 had a single hemi- with kyphosis.

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 Discussion could result in underestimation of the complexity
of spinal curvature anomalies. Spinal curvature
Results of the present study involving apparently anomalies can have a combined kyphoscoliosis and
neurologically normal French Bulldogs, English Bull- even rotated nature, which is difficult to quantify
dogs, and Pugs with ≥ 1 hemivertebra identified on with Cobb angles.19
CT images supported the hypotheses that different
The association between development of clinical
screw-tail brachycephalic breeds have a different
signs and hemivertebra subtype has been evaluated
spectrum of hemivertebra subtypes and associated
in dogs.5 The severity of kyphosis12 and the likeli-
degrees of dorsoventral spinal curvature abnormali-
hood of neurologic signs5 have been considered to
ties (ie, kyphosis). Ventral hypoplasias or ventral
correspond with the severity of defects in vertebral
wedge-shape vertebrae were more common in Pugs
body formation. Although the VH subtype (ventral
than in the other 2 breeds. This specific hemivertebra
wedge-shaped vertebra) has been identified in both
subtype (and hence the Pug breed) was associated
with higher Cobb angles and a higher likelihood of clinically affected and clinically unaffected dogs, the
kyphosis than other hemivertebra subtypes. Where- VLA (dorsolateral hemivertebra) and particularly VA
as French and English Bulldogs had a wider variety (dorsal hemivertebra) subtypes have been identified
of hemivertebra subtypes, Pugs exclusively had the only in neurologically affected dogs.5 This is in agree-
VH subtype, so it was not surprising that Pugs were ment with findings of a previous study20 regarding
more likely to have kyphosis than French and English the clinical characteristics of dogs with dorsal hemi-
Bulldogs. vertebrae. In the apparently neurologically normal
The clinical relevance of these findings remains dogs of the present study, VA and VLA subtypes were
unclear, but the findings explain why Pugs appear pre- uncommon, compared with other hemivertebra sub-
disposed to clinical signs associated with hemiverte- types, and identified in only 1.2% to 2.9% of all ob-
brae, compared with other screw-tail brachycephalic served hemivertebrae in French Bulldogs.
breeds.1,5 Although vertebral instability, subluxation, A recent genomic study21 of the genetic signa-
and vertebral canal stenosis may contribute, the pres- tures of dog breed development showed that French
ence and degree of kyphosis have been considered and English Bulldogs are closely related breeds. Pugs,
important risk factors for the development of clinical on the other hand, are not closely related to those
signs in dogs with hemivertebra.3,7 We therefore pro- 2 breeds and should be considered more closely re-
pose that the predisposition of Pugs to the VH hemi- lated to other toy breeds such as the Brussel Griffon
vertebra subtype, which was associated with higher and Papillion.21 Although other factors could not be
Cobb angles and a higher likelihood of kyphosis than excluded, these genetic findings could explain the
other hemivertebra subtypes in the present study, similarities in the prevalence of various hemivertebra
could contribute to their predisposition to develop- subtypes between the French and English Bulldogs
ing clinical signs. and the dissimilarities in prevalences between these
Although uncommon in the apparently neu- breeds and the Pugs in the present study.
rologically normal Pugs and English Bulldogs of Whether VA and VH should be considered 2 dis-
the present study, a Cobb angle exceeding 35° tinct vertebral anomalies or different gradations of
was identified in 17% of apparently neurologically the same congenital malformation is unclear. Ventral
normal French Bulldogs. No neurologic examina- aplasia is characterized by a complete failure of for-
tion was performed, and we could not exclude the mation of the ventral portion of the vertebral body,
possibility that some of these dogs had a subtle leaving a residual wedge-shaped dorsal portion (dor-
gait abnormality at the time of initial evaluation sal hemivertebra) attached to both pedicles and the
or that they developed clinical signs later in life, neural arch.12 Ventral hypoplasia is characterized by
which represents a study limitation. A high degree a partial failure of formation of the ventral portion
of kyphosis may not be the only risk factor for de- of the vertebral body. In contrast to VA, the ventral
velopment of clinical disease, as is suggested by apex of this wedge-shaped vertebra typically extends
previously reported findings of high Cobb angles to the ventral longitudinal ligament.12
exceeding 35° in French Bulldogs without neuro- As previously mentioned, the system used to
logic deficits.18 Indeed, Cobb angle measurements classify hemivertebra subtypes in the present study
may not represent all clinically important charac- was an expansion of a radiographic classification sys-
teristics of spinal curvature abnormalities. It could tem used in a previous study.5 In agreement with the
be that vertebral abnormalities resulting in a sharp- findings of that study, several vertebrae were judged
ly angled kyphosis are more clinically relevant in the present study as having an abnormally short
than vertebral malformations resulting in a similar length but otherwise normal shape of the vertebral
Cobb angle, but with a smoother spinal curvature body. One suggestion that arose from the previous
involving several adjacent vertebrae, as has been study5 was that this type of vertebral malformation
suggested for humans.12 Additional research is nec- should be added to any future classification systems
essary to determine whether the same applies to as SH or short vertebra.5 We further added the hemi-
dogs. Another suggestion is that measurement of vertebra subtypes VLH and VMH for assessment of
spinal curvature anomalies in a sagittal, 2-D plane hemivertebrae on CT images specifically. Use of mul-

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 tiplanar imaging techniques such as CT improves 5. Gutierrez-Quintana R, Guevar J, Stalin C, et al. A proposed
identification and characterization of complex bony radiographic classification scheme for congenital thoracic
vertebral malformations in brachycephalic “screw-tailed”
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