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Cited by 148Human-Animal Interaction StudiesVeterinary Medicine and SurgeryVeterinary Equine Medical Research

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Conformational risk factors of brachycephalic obstructive airway syndrome (BOAS) in pugs, French bulldogs, and bulldogs

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Liu, Nai-Chieh, Troconis, Eileen L., Kalmar, Lajos, Price, David J., Wright, Hattie E., Adams, Vicki J., Sargan, David R., Ladlow, Jane F.·2017·PLOS ONE
DOI 10.1371/journal.pone.0181928PMC PMC5538678
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Abstract

Extremely brachycephalic, or short-muzzled, dog breeds such as pugs, French bulldogs, and bulldogs are prone to the conformation-related respiratory disorder-brachycephalic obstructive airway syndrome (BOAS). Affected dogs present with a wide range of clinical signs from snoring and exercise intolerance, to life-threatening events such as syncope. In this study, conformational risk factors for BOAS that could potentially aid in breeding away from BOAS were sought. Six hundred and four pugs, French bulldogs, and bulldogs were included in the study. Soft tape measurements of the head and body were used and the inter-observer reproducibility was evaluated. Breed-specific models were developed to assess the associations between the conformational factors and BOAS status based on functional grading. The models were further validated by means of a BOAS index, which is an objective measurement of respiratory function using whole-body barometric plethysmography. The final models have good predictive power for discriminating BOAS (-) and BOAS (+) phenotypes indicated by the area under the curve values of >80% on the receiver operating curves. When other factors were controlled, stenotic nostrils were associated with BOAS in all three breeds; pugs and bulldogs with higher body condition scores (BCS) had a higher risk of developing BOAS. Among the standardized conformational measurements (i.e. craniofacial ratio (CFR), eye width ratio (EWR), skull index (SI), neck girth ratio (NGR), and neck length ratio (NLR)), for pugs EWR and SI, for French bulldogs NGR and NLR, and for bulldogs SI and NGR showed significant associations with BOAS status. However, the NGR in bulldogs was the only significant predictor that also had satisfactory inter-observer reproducibility. A NGR higher than 0.71 in male bulldogs was predictive of BOAS with approximately 70% sensitivity and specificity. In conclusion, stenotic nostrils, BCS, and NGR were found to be valid, easily applicable predictors for BOAS (+).

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Figures

Fig 1 Examples of different degrees of nostril stenosis in pugs, French bulldogs, and bulldogs. The following descriptions were adapted from a previously published figure by the authors (Fig 1 in Liu et al. 2016): “Open nostrils: nostrils are wide open; mildly stenotic nostrils: slightly narrowed nostrils where the lateral nostril wall does not touch the medial nostril wall. Immediately after the exercise tolerance test (ETT), the nostril wings should move dorsolaterally to open on inspiration; moderately stenotic nostrils: the lateral nostril wall touches the medial nostril wall at the dorsal part of the nostrils and the nostrils are only open at the bottom. Immediately after the ETT, the nostril wings are not able to move dorsolaterally and there may be nasal flaring (ie, muscle contraction around the nose trying to enlarge the nostrils; severely stenotic nostrils: nostrils are almost closed. The dog may switch to oral breathing from nasal breathing with stress or very gentle exercise such as playing.” (Liu et al. 2016).
Fig 1 Examples of different degrees of nostril stenosis in pugs, French bulldogs, and bulldogs. The following descriptions were adapted from a previously published figure by the authors (Fig 1 in Liu et al. 2016): “Open nostrils: nostrils are wide open; mildly stenotic nostrils: slightly narrowed nostrils where the lateral nostril wall does not touch the medial nostril wall. Immediately after the exercise tolerance test (ETT), the nostril wings should move dorsolaterally to open on inspiration; moderately stenotic nostrils: the lateral nostril wall touches the medial nostril wall at the dorsal part of the nostrils and the nostrils are only open at the bottom. Immediately after the ETT, the nostril wings are not able to move dorsolaterally and there may be nasal flaring (ie, muscle contraction around the nose trying to enlarge the nostrils; severely stenotic nostrils: nostrils are almost closed. The dog may switch to oral breathing from nasal breathing with stress or very gentle exercise such as playing.” (Liu et al. 2016).CC BY · PubMed Central
Fig 2 Demonstration of the soft tape measurements. Nine measurements were made with a firmly held soft tape measure with the dog standing and at rest: Skull length (SL), cranial length (CL), snout length (SnL), neck length (NL), body length (BL), eye width (EW), and skull width (SW). The detailed definitions of the measurements are shown in Table 1. The photos of the dogs were taken from two of the study dogs by the authors.
Fig 2 Demonstration of the soft tape measurements. Nine measurements were made with a firmly held soft tape measure with the dog standing and at rest: Skull length (SL), cranial length (CL), snout length (SnL), neck length (NL), body length (BL), eye width (EW), and skull width (SW). The detailed definitions of the measurements are shown in Table 1. The photos of the dogs were taken from two of the study dogs by the authors.CC BY · PubMed Central
Fig 3 Scatter plots show the inter-observer reproducibility of the conformational soft tape measures. The diagonal red line indicates perfect agreement. ICC, intra-class correlation coefficient; CFR, craniofacial ratio; EWR, eye width ratio; SI, skull index; NGR, neck girth ratio; NLR, neck length ratio.
Fig 3 Scatter plots show the inter-observer reproducibility of the conformational soft tape measures. The diagonal red line indicates perfect agreement. ICC, intra-class correlation coefficient; CFR, craniofacial ratio; EWR, eye width ratio; SI, skull index; NGR, neck girth ratio; NLR, neck length ratio.CC BY · PubMed Central
Fig 4 Stacked bar charts demonstrate the relationship between BOAS functional grade and body condition score (BCS), and the degree of nostril stenosis. The y-axis shows the percentage of dogs of that functional grade showing each degree of BCS or nostril stenosis. Note the clear trends of an increased proportion of obese dogs and dogs with moderately or severely stenotic nostrils with an increase in functional grade. In French bulldogs, there were over 10% of Grade III dogs that had BCS of 3. The underweight condition was attributed to BOAS-related frequent regurgitation.
Fig 4 Stacked bar charts demonstrate the relationship between BOAS functional grade and body condition score (BCS), and the degree of nostril stenosis. The y-axis shows the percentage of dogs of that functional grade showing each degree of BCS or nostril stenosis. Note the clear trends of an increased proportion of obese dogs and dogs with moderately or severely stenotic nostrils with an increase in functional grade. In French bulldogs, there were over 10% of Grade III dogs that had BCS of 3. The underweight condition was attributed to BOAS-related frequent regurgitation.CC BY · PubMed Central
Fig 5 Univariate logistic regression plots demonstrate the trend of the five conformational ratios against the estimated BOAS probability. The x-axis is the numeric data of each ratio in percentage; the y-axis is the estimated probability of BOAS. CFR, craniofacial ratio; EWR, eye width ratio; SI, skull index; NGR, neck girth ratio; NLR, neck length ratio.
Fig 5 Univariate logistic regression plots demonstrate the trend of the five conformational ratios against the estimated BOAS probability. The x-axis is the numeric data of each ratio in percentage; the y-axis is the estimated probability of BOAS. CFR, craniofacial ratio; EWR, eye width ratio; SI, skull index; NGR, neck girth ratio; NLR, neck length ratio.CC BY · PubMed Central
Fig 6 The predictive performance of the breed specific models. (A) boxplots show the distributions of the estimated probability of being BOAS-affected. The dotted line at 50% of the probability represents the raw predictive cut-off. For pugs and French bulldogs, the cut-off values can be adjusted to improve the specificity of the models; (B) receiver operating characteristic (ROC) curves show the predictive performance of the breed specific models. Area under the curve (AUC) was computed with its 95% confidence interval in the bracket.
Fig 6 The predictive performance of the breed specific models. (A) boxplots show the distributions of the estimated probability of being BOAS-affected. The dotted line at 50% of the probability represents the raw predictive cut-off. For pugs and French bulldogs, the cut-off values can be adjusted to improve the specificity of the models; (B) receiver operating characteristic (ROC) curves show the predictive performance of the breed specific models. Area under the curve (AUC) was computed with its 95% confidence interval in the bracket.CC BY · PubMed Central
Fig 7 An illustration demonstrates the relationship between the external craniofacial ratio (CFR) measurement and the corresponding internal anatomical structures of the upper airway. The realistic anatomical illustration was made according to a computed tomographic 3-dimensional rendering image of a French bulldog. The illustration was reprinted from the Cambridge BOAS research group website (http://www.vet.cam.ac.uk/boas) under a CC BY license, with permission from the group in the University of Cambridge, original copyright 2016.
Fig 7 An illustration demonstrates the relationship between the external craniofacial ratio (CFR) measurement and the corresponding internal anatomical structures of the upper airway. The realistic anatomical illustration was made according to a computed tomographic 3-dimensional rendering image of a French bulldog. The illustration was reprinted from the Cambridge BOAS research group website (http://www.vet.cam.ac.uk/boas) under a CC BY license, with permission from the group in the University of Cambridge, original copyright 2016.CC BY · PubMed Central

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Citations

Cites

Show all 41 references

Research works printed but not linked: 5

  1. C Knecht, 1979, Upper airway obstruction in brachycephalic dogs, Comp Cont Educ Pract, 1, 25
  2. JC Hendricks, 1992, Brachycephalic airway syndrome, Vet Clin North Am Small Anim Pract, 22, 1145, 10.1016/S0195-5616(92)50306-0 · DOI
  3. D Koch, 2015, Veränderung des Schädels bei brachycephalen Hunden im Verlaufe der letzten 100 Jahre, Kurzmitteilungen, 157, 1
  4. NC Liu, 2016, Whole-body barometric plethysmography characterizes upper airway obstruction in 3 brachycephalic breeds of dogs, J Vet Intern Med, 30, 853, 10.1111/jvim.13933 · DOI
  5. J Hendricks, 1987, The English bulldog: a natural model of sleep-disordered breathing, J Appl Physiol, 63, 1344, 10.1152/jappl.1987.63.4.1344 · DOI

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Metadata

Authors
Liu, N.-C., Troconis, E. L., Kalmar, L., Price, D. J., Wright, H. E., Adams, V. J., Sargan, D. R., & Ladlow, J. F.
Affiliations
  • University of Cambridge (GB)
  • Suffolk University Madrid (ES)
Corresponding author
Ladlow, Jane F.
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2017-08-01
Volume
12
Issue
8
Pages
e0181928
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0181928
PMC
PMC5538678
OpenAlex
W2740722812
Cited by
148
References
41
Citations by year
2026: 7 · 2025: 24 · 2024: 22 · 2023: 27 · 2022: 32 · 2021: 17 · 2020: 5 · 2019: 7 · 2018: 7
FWCI
3.45
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Minerva Access (University of Melbourne) (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
Funders
  • The Kennel Club Charitable Trust (RG71960)
  • Cambridge Overseas Trust
Topics
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Human-Animal Interaction Studies
  • Health Sciences › Veterinary › Small Animals › Veterinary Medicine and Surgery
  • Health Sciences › Veterinary › Equine › Veterinary Equine Medical Research
Keywords
brachycephalic obstructive airway syndrome, Pug, French bulldog, bulldogs, body condition score, barometric plethysmography, interobserver reproducibility, dog breeding
MeSH terms
Airway Obstruction, Animals, Breeding, Craniosynostoses, Dog Diseases, Dogs, Female, Male, Plethysmography, Whole Body, Regression Analysis, Risk Factors, Species Specificity, Syndrome, Reproducibility of Results, Observer Variation

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