Relationship between breed, hemivertebra subtype, and kyphosis in apparently neurologically normal French Bulldogs, English Bulldogs, and Pugs

Richard Ryan Department of Veterinary Clinical Science and Services, Royal Veterinary College, University of London, North Mymms, AL9 7TA, England.

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Rodrigo Gutierrez-Quintana Department of Small Animal Sciences, School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G61 1QH, Scotland.

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Gert ter Haar Department of Veterinary Clinical Science and Services, Royal Veterinary College, University of London, North Mymms, AL9 7TA, England.

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Steven De Decker Department of Veterinary Clinical Science and Services, Royal Veterinary College, University of London, North Mymms, AL9 7TA, England.

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Abstract

OBJECTIVE To investigate whether hemivertebra subtype as determined via CT was associated with breed and Cobb angle (a measure of the degree of spinal curvature) in apparently neurologically normal French Bulldogs, English Bulldogs, and Pugs.

ANIMALS Client-owned French Bulldogs (n = 58), English Bulldogs (30), and Pugs (12) with thoracic hemivertebrae that underwent CT for reasons unrelated to spinal disease.

PROCEDURES CT scans of each dog were evaluated, and hemivertebrae were categorized by subtype (ventral aplasia, ventral hypoplasia, lateral aplasia, lateral hypoplasia, ventrolateral aplasia, ventrolateral hypoplasia, ventral and median aplasia, ventral and median hypoplasia, and symmetric hypoplasia). The Cobb angle was measured, and kyphosis was defined as a Cobb angle > 10°. Results were compared among breeds.

RESULTS 243 hemivertebrae were identified in the French Bulldog group, 100 in the English Bulldog group, and 19 in the Pug group. Breed was significantly associated 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.

Abstract

OBJECTIVE To investigate whether hemivertebra subtype as determined via CT was associated with breed and Cobb angle (a measure of the degree of spinal curvature) in apparently neurologically normal French Bulldogs, English Bulldogs, and Pugs.

ANIMALS Client-owned French Bulldogs (n = 58), English Bulldogs (30), and Pugs (12) with thoracic hemivertebrae that underwent CT for reasons unrelated to spinal disease.

PROCEDURES CT scans of each dog were evaluated, and hemivertebrae were categorized by subtype (ventral aplasia, ventral hypoplasia, lateral aplasia, lateral hypoplasia, ventrolateral aplasia, ventrolateral hypoplasia, ventral and median aplasia, ventral and median hypoplasia, and symmetric hypoplasia). The Cobb angle was measured, and kyphosis was defined as a Cobb angle > 10°. Results were compared among breeds.

RESULTS 243 hemivertebrae were identified in the French Bulldog group, 100 in the English Bulldog group, and 19 in the Pug group. Breed was significantly associated 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.

Thoracic congenital vertebral body malformations are common in clinically normal, so-called screw-tail brachycephalic breeds, such as French Bulldogs, English Bulldogs, and Pugs.1 Although there is some discussion about the most appropriate terminology,2 congenital vertebral body malformations can be classified by defects of segmentation, including block vertebrae, and defects of formation, including hemivertebrae. Hemivertebrae are the most common type of vertebral malformations, and several studies1,3–5 have revealed a high prevalence in neurologically normal French Bulldogs, English Bulldogs, and Pugs.

Hemivertebrae are most common in the midthoracic region, can affect single or multiple vertebrae, and can be associated with spinal curvature abnormalities, such as kyphosis and scoliosis.3,6,7 Although the degree of spinal curvature can be quantified in various ways, the measuring technique described by John Robert Cobb is considered the gold standard.8 This method involves measurement of the angle, referred to as the Cobb angle, of the most tilted vertebra. The Cobb angle is derived by measuring the angle between a line superimposed on the cranial vertebral end plate of the vertebra cranial to a given vertebra and a line superimposed on the caudal vertebral end plate of the vertebra caudal to that given vertebra.8 This angle can be measured manually or with various digital methods, including computer-assisted, automatic, and smartphone-application methods. All methods have been associated with high degrees of reliability, with digital methods providing slightly better results.9

Although hemivertebrae are typically considered incidental findings on diagnostic imaging, they have the potential to cause clinical signs of progressive spinal cord dysfunction.1,3,10,11 The pathophysiologic mechanism underlying the clinical signs is considered multifactorial.10 Results of some studies3,7 indicate that the presence and severity of kyphosis could be risk factors for development of clinical signs in dogs with hemivertebrae, whereas results of another study1 suggest that breed could also be a risk factor. More specifically, thoracic hemivertebrae have been suggested to be of greater clinical importance in Pugs than in French and English Bulldogs.1

The reason Pugs with hemivertebrae are more likely to develop clinical signs than other screw-tail brachycephalic dogs is unclear. Although other factors cannot be excluded, breed-specific differences may exist in hemivertebra morphology. In both human 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 subtypes in accordance with another human classification system.

Recognition of and interest in brachycephalic breed-related health disorders are increasing,14,15 and radiographic screening programs for thoracic hemivertebrae have been considered.16,17 However, evaluation of the impact of thoracic hemivertebrae on the welfare of brachycephalic breeds is complicated by their uncertain clinical importance, incompletely understood 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 classification 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 hemivertebra subtypes than French and English Bulldogs and that there would be an association between hemivertebra subtype and the likelihood of kyphosis.

Materials and Methods

Animals

Dogs were selected for this retrospective cross-sectional study from among those included in a previous retrospective study1 of the prevalence of thoracic vertebral malformations in French Bulldogs, English Bulldogs, and Pugs with and without associated neurologic signs. All dogs without neurologic signs in that study had undergone thoracic CT while sedated or anesthetized for reasons unrelated to spinal or orthopedic disease between October 2010 and February 2016. Dogs had been excluded from that group if medical records or imaging studies were incomplete or unavailable for review or if the reason for evaluation was a gait abnormality. Most received no neurologic examination and were considered apparently neurologically normal if they had been evaluated for a nonneurologic condition and none of the clinical notes included mention of any previous or existing gait or neurologic abnormalities. To be included in the present study, dogs were required to have been considered as apparently neurologically normal and to have had ≥ 1 thoracic hemivertebra diagnosed in the previous study.1

Data collection

In the previous study,1 information was retrieved from the medical records of each dog regarding signalment, reason for evaluation, and results of general physical examination on the date of the CT examination. The CT examination had been performed with a 16-slice helical CT scanner,a with dogs positioned in ventral recumbency. Images had been acquired at 140 kVp and 120 mA in helical mode, with a 2-mm slice thickness, –1 interval between slices, 110-mm field of view, bone and soft tissue reconstruction algorithms, and 512 × 512 matrix. After completion of transverse CT scanning, sagittal, dorsal, and 3-D reconstructions had been made.

For the present study, these images were independently evaluated by 2 observers (RR and RG-Q) for the presence and type of hemivertebrae. Each identified hemivertebra was categorized into 1 of 9 subtypes (VA or dorsal hemivertebra, VH or ventral wedged vertebra, LA or lateral hemivertebra, LH or lateral wedge-shape vertebra, VLA or dorsolateral hemivertebra, VLH, VMA or butterfly vertebra, VMH, and SH or short vertebra; Figures 1 and 2) on the basis of a previously reported radiographic classification system5 that was adapted for use with CT images.

Figure 1—
Figure 1—

Diagrams of the subtypes used to classify hemivertebrae in dogs on CT examination. This system is based on a radiographic classification system,5 which has been expanded to include the subtypes SH, VLH, and VMH. (Adapted from Gutierrez-Quintana R, Guevar J, Stalin C, et al. A proposed radiographic classification scheme for congenital thoracic vertebral malformations in brachycephalic “screw-tailed” dog breeds. Vet Radiol Ultrasound 2014;55:585–591. Reprinted with permission.)

Citation: American Journal of Veterinary Research 80, 2; 10.2460/ajvr.80.2.189

Figure 2—
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.

Citation: American Journal of Veterinary Research 80, 2; 10.2460/ajvr.80.2.189

Degree of kyphosis was assessed by another observer (SD) and objectively evaluated by measuring the Cobb angle automatically by use of a commercial plug-in device as described elsewhere.7 For the purpose of the present study, kyphosis was defined as a dorsal spinal curvature with a Cobb angle > 10°. When multiple hemivertebrae were present, the Cobb angle for each affected vertebral segment was obtained. Standard image archiving and communication system softwareb was used to evaluate all images.

Statistical analysis

Data were analyzed with statistical software.c Associations between breed and hemivertebra subtype (based on the proportion of a specific hemivertebra subtype, compared with the total number of observed hemivertebra in a given breed) and between hemivertebra subtype and presence of kyphosis were evaluated with the χ2 test followed by post hoc analysis with the Mann-Whitney U test. Associations between hemivertebra subtype and Cobb angle were evaluated with the Kruskal-Wallis test followed by post hoc analysis with the Mann-Whitney U test. Values of P < 0.05 were considered significant; Bonferroni correction of P values was performed for multiple comparisons.

Results

Animals

A total of 100 dogs, consisting of 58 French Bulldogs, 30 English Bulldogs, and 12 Pugs, were included in the study. These dogs had undergone CT for various clinical indications, including brachycephalic obstructive airway syndrome (n = 77), other respiratory disease (7), neoplastic disease (7), gastrointestinal disease (6), cardiac disease (2), and trauma (1). Eight-two dogs had multiple hemivertebrae, and 18 had a single hemivertebra.

French Bulldogs—The group of French Bulldogs consisted of 50 (86%) males and 8 (14%) females between 2 and 135 months of age (median, 19.4 months; mean, 29.9 months) and weighing between 6.7 and 16 kg (median and mean, 11.4 kg). Forty-nine (84%) French Bulldogs had multiple hemivertebrae, and 9 (16%) had a single hemivertebra, for a total of 243 hemivertebrae. The 3 most common hemivertebra subtypes in this breed were VMA (32.1% of all hemivertebrae), VMH (23.9%), and LH (18.5%; Table 1). The measured Cobb angle ranged from 0.2° to 61.5° (median, 9.4°; mean, 17.9°). Twenty-five (43%) dogs had kyphosis, and 10 (17%) dogs had Cobb angles exceeding 35° (a value associated with neurologic deficits7).

Table 1—

Number (%) of hemivertebra subtypes identified in CT images of apparently neurologically normal French Bulldogs (n = 58), English Bulldogs (30), and Pugs (12).

SubtypeFrench BulldogsEnglish BulldogsPugsP value
VA3 (1.2)000.62
VH16 (6.6)10 (10)19 (100)< 0.001
LA25 (10.3)5 (5)00.16
LH45 (18.5)3 (3)0< 0.001
VLA7 (2.9)1 (1)00.64
VLH9 (3.7)1 (1)00.41
VMA78 (32.1)21 (21)00.01
VMH58 (23.9)58 (58)00.01
SH2 (0.08)1 (1)01.00
Total24310019NA

NA = Not applicable.

English Bulldogs—The group of English Bulldogs consisted of 20 (67%) males and 10 (33%) females between 10 and 127 months of age (median, 21.0 months; mean, 37.4 months) and weighing between 10.4 and 37.1 kg (median, 23.4 kg; mean, 24.6 kg). Twenty-seven (90%) English Bulldogs had multiple hemivertebrae, and 3 (10%) had a single hemivertebra, for a total of 100 hemivertebrae. The 3 most common hemivertebra subtypes were VMH (58%), VMA (21%), and VH (10%; Table 1). No English Bulldog had the VA subtype. The measured Cobb angle ranged from 2.4° to 40.0° (median, 11.1°; mean, 14.3°). Seventeen (57%) dogs had kyphosis, and 1 (3%) had a Cobb angle exceeding 35°.

Pugs—The group of Pugs consisted of 7 males and 5 females between 8 and 114 months of age (median, 36.5 months; mean, 44.9 months) and weighing between 4.2 and 13.7 kg (median, 8.2; mean, 8.2 kg). Six Pugs had multiple hemivertebrae, and 6 had a single hemivertebra, for a total of 19 hemivertebrae. All identified hemivertebrae were of the VH subtype, and no other subtype was observed. The Cobb angle ranged from 0.4° to 39.7° (median 25.3°; mean, 20.1°). Eleven Pugs had kyphosis, and 1 had a Cobb angle exceeding 35°.

Association between breed and hemivertebra subtype

A significant (P ≤ 0.001) association was identified between breed and the hemivertebra subtypes VH, VMH, LH, and VMA. Specifically, Pugs were significantly more likely to be have the VH subtype and significantly less likely to have the VMH subtype than French Bulldogs (P < 0.001 for VH and P = 0.007 for VMH) and English Bulldogs (P < 0.001 for both subtypes). No significant difference was identified between French and English Bulldogs in the proportions with the VH subtype; however, English Bulldogs were significantly (P < 0.001) more likely to have the VMH subtype than French Bulldogs. French Bulldogs were significantly (P < 0.001) more likely to have the LH subtype than English Bulldogs. French Bulldogs were also significantly (P = 0.001) more likely to have the VMA subtype than Pugs. No other significant differences were identified between breeds in proportions with the LH and VMA hemivertebra subtypes or proportions with the VLH, VLA, SH, VA, and LA subtypes.

Association between hemivertebra subtype and degree of spinal curvature

Overall, hemivertebra subtype was significantly (P < 0.001) associated with the Cobb angle and with kyphosis. The VH subtype was significantly (P < 0.001) associated with higher Cobb angles and a higher likelihood of kyphosis, compared with all other hemivertebra subtypes combined. No significant associations were identified between the other subtypes and Cobb angle or kyphosis.

Breed was significantly associated with kyphosis (P < 0.001). More specifically, kyphosis was more common in Pugs (with hemivertebrae) than it was in French Bulldogs (P < 0.001) and English Bulldogs (P = 0.002). No significant difference was identified between French and English Bulldogs in proportions with kyphosis.

Discussion

Results of the present study involving apparently neurologically normal French Bulldogs, English Bulldogs, and Pugs with ≥ 1 hemivertebra identified on CT images supported the hypotheses that different screw-tail brachycephalic breeds have a different spectrum of hemivertebra subtypes and associated degrees of dorsoventral spinal curvature abnormalities (ie, kyphosis). Ventral hypoplasias or ventral wedge-shape vertebrae were more common in Pugs than in the other 2 breeds. This specific hemivertebra subtype (and hence the Pug breed) was associated with higher Cobb angles and a higher likelihood of kyphosis than other hemivertebra subtypes. Whereas French and English Bulldogs had a wider variety of hemivertebra subtypes, Pugs exclusively had the VH subtype, so it was not surprising that Pugs were more likely to have kyphosis than French and English Bulldogs.

The clinical relevance of these findings remains unclear, but the findings explain why Pugs appear predisposed to clinical signs associated with hemivertebrae, compared with other screw-tail brachycephalic breeds.1,5 Although vertebral instability, subluxation, and vertebral canal stenosis may contribute, the presence and degree of kyphosis have been considered important risk factors for the development of clinical signs in dogs with hemivertebra.3,7 We therefore propose that the predisposition of Pugs to the VH hemivertebra subtype, which was associated with higher Cobb angles and a higher likelihood of kyphosis than other hemivertebra subtypes in the present study, could contribute to their predisposition to developing clinical signs.

Although uncommon in the apparently neurologically normal Pugs and English Bulldogs of the present study, a Cobb angle exceeding 35° was identified in 17% of apparently neurologically normal French Bulldogs. No neurologic examination was performed, and we could not exclude the possibility that some of these dogs had a subtle gait abnormality at the time of initial evaluation or that they developed clinical signs later in life, which represents a study limitation. A high degree of kyphosis may not be the only risk factor for development of clinical disease, as is suggested by previously reported findings of high Cobb angles exceeding 35° in French Bulldogs without neurologic deficits.18 Indeed, Cobb angle measurements may not represent all clinically important characteristics of spinal curvature abnormalities. It could be that vertebral abnormalities resulting in a sharply angled kyphosis are more clinically relevant than vertebral malformations resulting in a similar Cobb angle, but with a smoother spinal curvature involving several adjacent vertebrae, as has been suggested for humans.12 Additional research is necessary to determine whether the same applies to dogs. Another suggestion is that measurement of spinal curvature anomalies in a sagittal, 2-D plane could result in underestimation of the complexity of spinal curvature anomalies. Spinal curvature anomalies can have a combined kyphoscoliosis and even rotated nature, which is difficult to quantify with Cobb angles.19

The association between development of clinical signs and hemivertebra subtype has been evaluated in dogs.5 The severity of kyphosis12 and the likelihood of neurologic signs5 have been considered to correspond with the severity of defects in vertebral body formation. Although the VH subtype (ventral wedge-shaped vertebra) has been identified in both clinically affected and clinically unaffected dogs, the VLA (dorsolateral hemivertebra) and particularly VA (dorsal hemivertebra) subtypes have been identified only in neurologically affected dogs.5 This is in agreement with findings of a previous study20 regarding the clinical characteristics of dogs with dorsal hemivertebrae. In the apparently neurologically normal dogs of the present study, VA and VLA subtypes were uncommon, compared with other hemivertebra subtypes, and identified in only 1.2% to 2.9% of all observed hemivertebrae in French Bulldogs.

A recent genomic study21 of the genetic signatures of dog breed development showed that French and English Bulldogs are closely related breeds. Pugs, on the other hand, are not closely related to those 2 breeds and should be considered more closely related to other toy breeds such as the Brussel Griffon and Papillion.21 Although other factors could not be excluded, these genetic findings could explain the similarities in the prevalence of various hemivertebra subtypes between the French and English Bulldogs and the dissimilarities in prevalences between these breeds and the Pugs in the present study.

Whether VA and VH should be considered 2 distinct vertebral anomalies or different gradations of the same congenital malformation is unclear. Ventral aplasia is characterized by a complete failure of formation of the ventral portion of the vertebral body, leaving a residual wedge-shaped dorsal portion (dorsal hemivertebra) attached to both pedicles and the neural arch.12 Ventral hypoplasia is characterized by a partial failure of formation of the ventral portion of the vertebral body. In contrast to VA, the ventral apex of this wedge-shaped vertebra typically extends to the ventral longitudinal ligament.12

As previously mentioned, the system used to classify hemivertebra subtypes in the present study was an expansion of a radiographic classification system used in a previous study.5 In agreement with the findings of that study, several vertebrae were judged in the present study as having an abnormally short length but otherwise normal shape of the vertebral body. One suggestion that arose from the previous study5 was that this type of vertebral malformation should be added to any future classification systems as SH or short vertebra.5 We further added the hemivertebra subtypes VLH and VMH for assessment of hemivertebrae on CT images specifically. Use of multiplanar imaging techniques such as CT improves identification and characterization of complex bony malformations, compared with use of 2-D radiography.19,22 Computed tomography has therefore been proposed as the technique of choice for classifying defects of vertebral formation in humans19 and in dogs.23

Interobserver agreement in hemivertebra subtype classification was not evaluated in the present study. In a previous study,23 interobserver agreement in the detection and classification of hemivertebra in dogs by use of the aforementioned radiographic classification system5 was better when CT versus radiography was used. When CT was used, interobserver agreement in hemivertebra classification with that system ranged from fair to good.23

Overall, the results of the study reported here indicated a significant association between hemivertebra subtype, breed, and kyphosis in apparently neurologically normal French Bulldogs, English Bulldogs, and Pugs. Whereas French and English Bulldogs had a variety of hemivertebra subtypes, VH or a ventral wedge-shaped vertebra was the only subtype identified in Pugs. The VH subtype was associated with higher Cobb angles and a higher likelihood of kyphosis than other subtypes. Although these findings might help explain the apparent predisposition of Pugs to developing clinical signs attributable to hemivertebrae, additional research is necessary to determine the clinical importance of specific hemivertebra subtypes and the value of screening programs for specific congenital vertebral body malformations in dogs.

ABBREVIATIONS

LA

Lateral aplasia

LH

Lateral hypoplasia

SH

Symmetric hypoplasia

VA

Ventral aplasia

VH

Ventral hypoplasia

VLA

Ventrolateral aplasia

VLH

Ventrolateral hypoplasia

VMA

Ventral and median aplasia

VMH

Ventral and median hypoplasia

Footnotes

a.

PQ 500, GE Healthcare, Milwaukee, Wis.

b.

Osirix, version 5.5.2, Osirix Foundation, Geneva, Switzerland.

c.

IBM SPSS Statistics, version 22, SPSS Inc, Armonk, NY.

References

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  • Figure 1—

    Diagrams of the subtypes used to classify hemivertebrae in dogs on CT examination. This system is based on a radiographic classification system,5 which has been expanded to include the subtypes SH, VLH, and VMH. (Adapted from Gutierrez-Quintana R, Guevar J, Stalin C, et al. A proposed radiographic classification scheme for congenital thoracic vertebral malformations in brachycephalic “screw-tailed” dog breeds. Vet Radiol Ultrasound 2014;55:585–591. Reprinted with permission.)

  • 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.

  • 1. Ryan R, Gutierrez-Quintana R, Ter Haar G, et al. Prevalence of thoracic vertebral malformations in French Bulldogs, Pugs and English Bulldogs with and without associated neurological deficits. Vet J 2017;221:2529.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Westworth DR, Sturges BK. Congenital spinal malformations in small animals. Vet Clin North Am Small Anim Pract 2010;40:951981.

  • 3. Moissonnier P, Gossot P, Scotti S. Thoracic kyphosis associated with hemivertebra. Vet Surg 2011;40:10291032.

  • 4. Aikawa T, Shibata M, Asano M, et al. A comparison of thoracolumbar intervertebral disk extrusion in French Bulldogs and Dachshunds and association with vertebral anomalies (Erratum published in Vet Surg 2015;44:135). Vet Surg 2014;43:301307.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Gutierrez-Quintana R, Guevar J, Stalin C, et al. A proposed radiographic classification scheme for congenital thoracic vertebral malformations in brachycephalic “screw-tailed” dog breeds. Vet Radiol Ultrasound 2014;55:585591.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Faller K, Penderis J, Stalin C, et al. The effect of kyphoscoliosis on intervertebral disc degeneration in dogs. Vet J 2014;200:449451.

  • 7. Guevar J, Penderis J, Faller K, et al. Computer-assisted radiographic calculation of spinal curvature in brachycephalic “screw-tailed” dog breeds with congenital thoracic vertebral malformations: reliability and clinical evaluation. PLoS One 2014;9:e106957.

    • Crossref
    • Search Google Scholar
    • Export Citation
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