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Do dog owners perceive the clinical signs related to conformational inherited disorders as ‘normal’ for the breed? A potential constraint to improving canine welfare

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Do dog owners perceive the clinical signs related to conformational inherited disorders as 'normal' for the breed? A potential constraint to improving canine welfare Abstract Selection for brachycephalic (foreshortened muzzle) phenotypes in dogs is a major risk factor for brachycephalic obstructive airway syndrome (BOAS). Clinical signs include respiratory distress, exercise intolerance, upper respiratory noise and collapse. Efforts to combat BOAS may be constrained by a perception that it is 'normal' in brachycephalic dogs. This study aimed to quantify owner-perception of the clinical signs of BOAS as a veterinary problem. A questionnaire-based study was carried out over five months on the owners of dogs referred to the Queen Mother Hospital for Animals (QMHA) for all clinical services, except for Emergency and Critical Care. Owners reported the frequency of respiratory difficulty and characteristics of respiratory noise in their dogs in four scenarios, summarised as an 'owner-reported breathing' (ORB) score. Owners then reported whether their dog currently has, or has a history of, 'breathing problems'. Dogs (n = 285) representing 68 breeds were included, 31 of which were classed as 'affected' by BOAS either following diagnostics, or by fitting case criteria based on their ORB score, skull morphology and presence of stenotic nares. The median ORB score given by affected dogs' owners was 20/40 (range 8–30). Over half (58%) of owners of affected dogs reported that their dog did not have a breathing problem. This marked disparity between owners' reports of frequent, severe clinical signs and their perceived lack of a 'breathing problem' in their dogs is of concern. Without appreciation of the welfare implications of BOAS, affected but undiagnosed dogs may be negatively affected indefinitely through lack of treatment. Furthermore, affected dogs may continue to be selected in breeding programmes, perpetuating this disorder.
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81
© 2012 Universities Federation for Animal Welfare
The Old School, Brewhouse Hill, Wheathampstead,
Hertfordshire AL4 8AN, UK
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
ISSN 0962-7286
Do dog owners perceive the clinical signs related to conformational
inherited disorders as ‘normal’ for the breed? A potential constraint to
improving canine welfare
RMA Packer*, A Hendricks and CC Burn
Centre for Animal Welfare, Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Hertfordshire AL9 7TA, UK
* Contact for correspondence and requests for reprints: rpacker@rvc.ac.uk
Abstract
Selection for brachycephalic (foreshortened muzzle) phenotypes in dogs is a major risk factor for brachycephalic obstructive airway
syndrome (BOAS). Clinical signs include respiratory distress, exercise intolerance, upper respiratory noise and collapse. Efforts to
combat BOAS may be constrained by a perception that it is ‘normal’ in brachycephalic dogs. This study aimed to quantify owner-
perception of the clinical signs of BOAS as a veterinary problem. A questionnaire-based study was carried out over five months on
the owners of dogs referred to the Queen Mother Hospital for Animals (QMHA) for all clinical services, except for Emergency and
Critical Care. Owners reported the frequency of respiratory difficulty and characteristics of respiratory noise in their dogs in four
scenarios, summarised as an ‘owner-reported breathing’ (ORB) score. Owners then reported whether their dog currently has, or has
a history of, ‘breathing problems’. Dogs (n = 285) representing 68 breeds were included, 31 of which were classed as ‘affected’ by
BOAS either following diagnostics, or by fitting case criteria based on their ORB score, skull morphology and presence of stenotic nares.
The median ORB score given by affected dogs’ owners was 20/40 (range 8–30). Over half (58%) of owners of affected dogs reported
that their dog did not have a breathing problem. This marked disparity between owners’ reports of frequent, severe clinical signs and
their perceived lack of a ‘breathing problem’ in their dogs is of concern. Without appreciation of the welfare implications of BOAS,
affected but undiagnosed dogs may be negatively affected indefinitely through lack of treatment. Furthermore, affected dogs may
continue to be selected in breeding programmes, perpetuating this disorder.
Keywords:animal welfare, brachycephalic, conformation, dog, owner perception, pedigree
Introduction
Recognition of the clinical signs of disease by companion
animal owners is an important initial step in the process of
perceiving a ‘problem’, and deciding to seek veterinary
attention for the investigation and potential treatment of any
disease that may be present. Lack of recognition of clinical
signs as indicative of disease, and instead considered
‘normal’ for certain demographics, was recently demon-
strated in geriatric horses, with regard to owner-perceived
‘benign’ age-related changes (Ireland et al 2012). Lack of
recognition of clinical signs of disease, or lack of perception
that these signs indicate a ‘problem’ that requires veterinary
attention, are potential constraints to improving the welfare
of clinically affected animals. The resulting lack of
treatment may lead to the continuation of clinical signs that
may negatively affect an animal’s welfare.
A duty of care is imposed upon the owners of all
companion animals through the Animal Welfare Act 2006
(S9[2]) and the Welfare of Animals Act (Northern Ireland)
2011 (S9[2]), where one of the five ‘needs’ of animals
protected under the Act is “Protection from pain, suffering,
injury and disease”. This ‘need’ potentially conflicts with
practices employed in the breeding of companion animals
of several species, whereby selection for extreme morpho-
logical characteristics to conform to breed standards has
led to a variety of associated disorders (eg in dogs: Peyer
1997; McGreevy & Nicholas 1999, cats: Wegner 1995;
Steiger 2005). In these cases, breeding may put animals
bred for certain conformational traits at an increased risk
of pain, suffering, injury and/or disease, and as noted by
Serpell (2002), many companion animal breeds have
effectively become handicapped by selection for traits that
appeal to our anthropomorphic perceptions.
Universities Federation for Animal Welfare Science in the Service of Animal Welfare
82 Packer et al
Brachycephalic Obstructive Airway Syndrome (BOAS)
Sixty-three disorders were recently identified as directly
related to conformational traits in the top 50 UK Kennel
Club breeds (Asher et al 2009). Within that review, one of
the disorders identified as most severe according to the
Generic Illness Severity Index for Dogs was
Brachycephalic Obstructive Airway Syndrome (BOAS).
BOAS describes a syndrome of the upper airway that leads
to restricted breathing, characterised by clinical signs such
as dyspnoea (shortness of breath), stertor (snoring), stridor
(wheezing), exercise intolerance, gagging, regurgitation and
vomiting. Episodes of severe dyspnoea can also occur,
leading to cyanosis (blueish skin/mucous membranes),
hyperthermia and syncope (fainting) (Riecks et al 2007).
Clinical signs are often severe by 12 months of age (Knecht
1979) and are life-long thereafter. These signs arise as a
result of obstruction of the upper airways caused by
anatomical abnormalities often seen in brachycephalic dogs
(those with foreshortened muzzles), and have been reported
in over ten brachycephalic breeds internationally (Table 1).
A recent risk factor analysis found brachycephalic dogs to
be 38 times more likely to have BOAS than non-brachy-
cephalic dogs (Njikam et al 2009).
Brachycephaly is a discrete skeletal mutation (Pollinger
et al 2005), where altered growth of the basioccipital and
basisphenoid bones manifests in a shortening of the basicra-
nial axis (Stockard 1941). Shortening of the skeletal muzzle
appears not to be accompanied by corresponding soft tissue
shortening, leading to a mismatch in proportion. This
creates a cramming effect within the skull, with too much
tissue in the available space (Harvey 1989), which partially
blocks the larynx and interferes with the passage of air
during inspiration and expiration. Additionally, the nares
(nostrils) of brachycephalic dogs are often stenotic
(narrowed), due to poor development (Wykes 1991),
causing the wing of the nostril to obstruct the airway and
collapse on inspiration, exacerbating the obstruction
(Leonard 1956). These abnormalities encourage collapse of
the airways due to significant, negative intra-airway
pressures created in an effort to overcome the increased
resistance to airflow (Wykes 1991). This can lead to
secondary changes to the airway, the most common being
the first stage of laryngeal collapse, everted laryngeal
saccules, causing yet further obstruction (Koch et al 2003).
Increased airway resistance is often manifested in altered
respiratory noise, with the nature and magnitude associ-
ated with the site and severity of obstruction. In animals
with minimal obstruction, slightly ‘stertorous’ or ‘stri-
dorous’ noises are often the only easily detectable abnor-
mality (Holt 2004). Stertor is described as similar to
snoring in humans (Holt 2004) or ‘a snorting noise’ (Hunt
et al 2002), and is thought to be associated with excessive
tissue in the upper portion of the airway (Riecks et al
2007). Stertor has been reported in brachycephalic dogs
while awake and asleep, and alongside episodes of sleep
apnoea (Hendricks 1987). Stridor, described as audible
© 2012 Universities Federation for Animal Welfare
Table 1 Caseload breed demographics of six recent studies of BOAS (2005–2010) breeds reported highlighted for each
study.
Breed/Study
Breed representation in BOAS case series’ (%)
Riecks
(2007)
62 dogs,
USA
De Lorenzi et al
(2009)
40 dogs,
Italy
Poncet et al
(2005)
73 dogs,
France
Torrez and Hunt
(2006)
73 dogs,
Australia
Ginn et al
(2008)
53 dogs,
USA
Njikam et al
(2009)
39 dogs,
Belgium
Bulldog 43.6 32.5 17.8 19.2 18.0 30.8
Pug 21.0 50.0 6.8 26.0 32.0 38.5
Cavalier King Charles Spaniel 0 0 0 20.6 0 2.6
Staffordshire Bull Terrier 0 0 0 5.5 0 0
French Bulldog 3.2 17.5 67.0 2.7 6.0 17.9
Boxer 0 0 1.4 1.4 9.0 0
Shih Tzu 0 0 0 1.4 11.0 5.1
Boston Terrier 12.9 0 1.4 0 6.0 0
Pekingese 6.5 0 2.8 2.7 3.0 0
Shar Pei 1.6 0 1.4 1.4 0 0
Rottweiler 0 0 0 1.4 0 0
Chow Chow 1.6 0 0 0 0 0
Pomeranian 3.2 0 0 0 0 0
Bullmastiff 3.2 0 0 1.4 0 0
Lhasa Apso 0 0 1.4 0 3.0 2.6
Owner recognition of breathing disorders in brachycephalic dogs 83
wheezing, is often associated with restricted airflow at the
level of the larynx, and is a common manifestation of
laryngeal collapse (Riecks et al 2007).
To diagnose palate and laryngeal abnormalities, pharyngo-
scopic and laryngoscopic examinations are performed on
induction of general anaesthesia prior to surgery, as visuali-
sation of the oropharynx in the conscious animal is difficult
and can induce extreme distress (Hendricks 1992).
Diagnosis under general anaesthesia is often followed
immediately by surgical ‘correction’ to relieve obstructions
(Hedlund 1998), as anaesthesia is high risk in brachy-
cephalic breeds (Riecks et al 2007). Surgical treatment
includes the resection of the soft palate (staphylectomy:
Schlotthauer 1929) and reshaping of the nares (rhinoplasty:
Trader 1949). If these features are left untreated, changes to
the larynx can progress to laryngeal collapse, where the
cartilages collapse and cause further obstruction (Leonard
1960). Laryngeal collapse carries a guarded prognosis
(Aron & Crowe 1985) and represents the most severe and
hardest to treat stage of BOAS, with permanent
tracheostomy required in severe cases to bypass the upper
airways (Monnet 2003). A recent case series of seven
immature brachycephalic dogs found that puppies aged
under six months already exhibited these severe secondary
changes (Pink et al 2006), highlighting the importance of
early surgical intervention where indicated.
Prognosis and owner perception
To reduce the welfare impact of this condition, with regard
to the severity and duration of clinical signs, treatment to
improve the welfare of affected animals is desirable. It has
been noted that the owners of brachycephalic dogs may be
more tolerant of clinical signs of airway obstruction than
non-brachycephalic dog owners, so may be prepared to
tolerate a greater degree of respiratory compromise in their
pets before seeking help (Torrez & Hunt 2006). Due to the
chronic and prevalent nature of clinical signs, they may be
‘accepted’ by owners and not perceived as abnormal. As
noted by Stafford and Martin (2008), due to owners’ accept-
ance of ongoing dyspnoea, it may require a particularly
acute or severe attack for owners to perceive a problem and
present their dog to a veterinarian. This is problematic, as it
may mean that many brachycephalic dogs are experiencing
chronic negative effects on their welfare without serious
appreciation of their clinical signs by their owners.
The aim of this study was to quantify owner recognition of
clinical signs of BOAS, and whether these signs are
perceived as a problem.
Materials and methods
Recruitment of owners and study dogs
Between December 2010 and May 2011, dogs referred to
the Queen Mother Hospital for Animals (QMHA) were
recruited for inclusion in the study. Owners of dogs
referred to the orthopaedic, soft tissue surgery, neurology
and neurosurgery, internal medicine, oncology, cardiology,
dermatology and hydrotherapy services were approached.
As appointments were booked in advance, all dogs were
considered for recruitment prior to their arrival at the
hospital and were excluded on a case-by-case basis if they
were: (i) being presented for a disorder that would make
them unsuited to leaving wards/nursing care during their
stay in the hospital, or too painful/uncomfortable to be
handled (clinicians were sought in these cases prior to the
appointments to advise their suitability); (ii) known to be
aggressive (either through previous experience at the study
hospital, or through information provided by their
referring veterinarian), and therefore not suitable for the
handling aspect of the study; (iii) isolated from the general
hospital population due to risk of disease transmission;
and (iv) already recruited to a separate clinical trial/study
within the study hospital.
Dogs referred to the emergency and critical care service, or
presented to the out-of-hours first opinion service were not
approached, due to the emergency nature of these cases
meaning that they would be excluded under criteria (i). The
owners of the remaining dogs deemed suitable were
approached in the waiting room prior to their consultation,
to request consent for their involvement in a broader
research project investigating conformational inherited
disorders in domestic dogs. Questionnaires were given to
owners, with regard to their dog’s behaviour, health and
lifestyle. For newly referred cases, owners were requested
to answer with regard to their dog’s current state, and for
cases presented for re-examination, owners were requested
to answer with regard to their dog’s state prior to treatment.
Questionnaire design
Prior to the study, the questionnaire was approved by the
RVC’s Ethical Review Committee (reference number: URN
2010 1054) and piloted on dog-owning members of staff and
students at the RVC with both a clinical and non-clinical
veterinary background, to check suitability and under-
standing for lay persons, and appropriate use of terminology.
The questionnaire contained several sections relevant to the
current study (as well as information relevant to the wider
project, not reported here), with information most pertinent
to BOAS in the ‘breathing difficulty’ and ‘breathing sounds’
sections. The frequency of breathing difficulties and the
severity of breathing sounds were requested in four activity
scenarios (Tables 2[a] and [b]). With regard to BOAS-
affected dogs, to capture the spectrum of severity of respi-
ratory-noise abnormalities, options from ‘slight’ through to
‘almost continuous’ stertor and stridor were offered. To use
non-technical terminology for owners, stertor was described
as ‘snoring or snorting’, and stridor as ‘wheezing’.
The degree of owner-reported respiratory difficulty and
respiratory noise in the four scenarios was later quantified
into a composite score, the ‘owner-reported breathing’
(ORB) score. The total score was out of 40, with scores out
of five for each scenario, for both respiratory difficulty
(Table 2[a]) and respiratory noise (Table 2[b]). A score of 0
would indicate respiratory difficulty had never been experi-
enced and breathing sounds were ‘very quiet’ in all four
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
84 Packer et al
© 2012 Universities Federation for Animal Welfare
Table 2 Summary of questions regarding respiratory signs in dogs. Questions concerning signs of (a) breathing difficulties
and (b) breathing sounds while at rest, gently walking, activity/exercising, and asleep are shown. Owners were indicated to
tick the appropriate boxes, and designated scores (not present on the questionnaire) were used to calculate the owner-
reported breathing (ORB) score. While (c) summarises a section later in the questionnaire where data were gathered on
whether the owner perceived their dog to have a breathing problem and, if so, relevant clinical details.
BREATHING DIFFICULTY – How often does your dog show difficulty breathing in the following situations?
Difficulty breathing could include your dog appearing very short of breath (more so than gentle panting), appearing unable to keep up
with you or engage in physical activity, may appear anxious. During sleep this may include episodes where your dog stops breathing.
Never
(Score = 0)
Rarely
(Score = 1)
Monthly
(Score = 2)
Weekly
(Score = 3)
Daily
(Score = 4)
More than
once per day
(Score = 5)
At rest, eg while lying down awake
Gently walking eg walking around the house
Activity/exercising, eg on a walk, while playing
Asleep
BREATHING SOUNDS – What does your dog’s breathing sound like in the following circumstances?
Very quiet
(Score = 0)
Panting
but no
snoring/
snorting/
wheezing
(Score = 1)
Slight
snoring/
snorting/
wheezing
(Score = 2)
Some
snoring/
snorting/
wheezing
(Score = 3)
Frequent
snoring/
snorting/
wheezing
(Score = 4)
Almost
continuous
snoring/
snorting/
wheezing
(Score = 5)
At rest, eg while lying down awake
Gently walking, eg walking around the house
Activity/exercising eg on a walk, while playing
Asleep
Does your dog currently have, or have a history of BREATHING PROBLEMS? YES NO
IF YES, PLEASE ANSWER THE FOLLOWING QUESTIONS:
If known, what was your dog diagnosed with?
What treatment (IF ANY) has your dog received for this
condition?
(PLEASE TICK AND FILL IN ANY ADDITIONAL
INFORMATION)
Surgery
Medication
At what age did you first notice this condition? Years Months
What first made you notice this condition? eg change in
behaviour, collapse (PLEASE STATE)
How quickly did these signs appear?
(PLEASE CIRCLE)
Suddenly over a
few hours Over a few days Gradually over a
few weeks
Gradually over
several months
Gradually over
longer than 1 year
Do you believe this
condition is:
(PLEASE CIRCLE)
Resolved Getting better Getting worse Staying the same Comes and goes
(but always there)
Episodic,
sometimes free of
problem
If episodic, how many episodes have
occurred:
If your dog has previously been treated for
this condition, for how long were they
‘improved’?
(a)
(b)
(c)
Owner recognition of breathing disorders in brachycephalic dogs 85
scenarios. By contrast, a score of 40 would indicate respira-
tory difficulty more than once per day in all four scenarios,
with corresponding respiratory noise classed as ‘almost
continuous snoring/snorting/wheezing’.
A ‘breathing problem’?
In the final section of the questionnaire, ‘Medical history’,
owners were asked to report whether their dog has, or has a
history of ‘breathing problems’ (Table 2[c]). This termi-
nology was chosen rather than ‘respiratory disease’, for
example, both to use lay terms and to imply it did not have
to be a diagnosed disease, rather a problem with breathing
that they had noticed in their dog. Further details were then
requested if the dog had been formally diagnosed for the
purpose of the broader study.
Morphological data
Stenotic nares
All study dogs were examined for stenotic nares. This
external abnormality is comparatively simple to diagnose
compared with the invasive diagnosis of internal airway
abnormalities; however, the severity of stenosis normally
involves a subjective visual assessment (Brown & Gregory
2005). In some dogs, stenosis may be mild, while in others
can result in the necessity to almost continually breathe with
the mouth open (Hendricks 1992). To make this assessment
more objective, a novel quantification of the degree of
superficial stenosis of the external nares was carried out.
Photographs of the nares were taken using a digital camera
(Canon EOS 500D, Taiwan), with the nasal planum perpen-
dicular to the field of view, and nares central to the photo-
graph. To quantify the degree of narrowing of the external
nares, four transverse measures of the width of the alae nasi
(Figure 1[a]) were taken from a single photograph of each
nare (using ImageJ© [Imaging Process and Analysis in
Java, http://rbsweb.nih.gov/ij/]), along with the transverse
width of the adjacent airspace (Figure 1[b]). An overall ratio
of alae nasi to airway diameter (‘nares ratio’) was calcu-
lated for each dog from these measures.
Skull conformation
Morphometric data were collected for each dog as part of the
larger research project investigating conformational inherited
disorders using measuring protocols from Sutter et al (2008).
These measurements included cranial length and muzzle
length, used to calculate the craniofacial index, a potential
risk factor for BOAS, as it reflects the degree of skeletal
shortening of the muzzle. Cranial length was measured ‘From
just between the eyes (Figure 2[b]) up the face, between the
ears, to the back of the head where the bony process projects
out’ (Figure 2[a]). Muzzle length was measured ‘From the tip
of nose (Figure 2[c]) to just between the eyes where the inside
corners of the eyes meet (Figure 2[b])’. Both measures were
taken using a standard 1 m soft measuring tape. The cranio-
facial ratio was then calculated for each dog by dividing the
muzzle length by the cranial length, to provide an objective
measure of relative muzzle length.
Clinical classification
Dogs received a formal BOAS ‘affected’ status if they
underwent internal airway assessment by soft tissue surgeons
at the QMHA, and stenotic nares, elongation of the soft palate
or everted laryngeal saccules were detected. Because of the
invasive nature of formal BOAS diagnosis, brachycephalic
dogs presented for problems other than BOAS would not
routinely undergo airway assessment, but may still be
affected by this condition. As such, dogs were also assigned
as affected if they met the following criteria: i) Craniofacial
ratio within or lower than the 95% confidence interval of
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
Figure 1
Photograph of the external nares, used to
quantify the degree of narrowing of the
transverse diameter of the nares. Dotted
lines (a) indicate the width of the alae
nasi, while the solid lines (b) indicate the
width of the adjacent external airway.
The central line indicates the philtrum,
delineating the left and right sides of the
nasal planum.
86 Packer et al
formally diagnosed affected dogs; (ii) ORB score within the
range or higher than that of formally diagnosed affected dogs;
and iii) nares ratio within or lower than the 95% confidence
interval of formally diagnosed affected dogs.
Dogs matching two of these criteria, that may
represent possible BOAS cases, were classed as
‘ambiguous’ due to the uncertainty of their status as
affected or unaffected, and were thus excluded from
the analyses. Dogs meeting only one or none of the
criteria were classed as unaffected.
Statistical analysis
ORB scores, craniofacial ratios and nares ratios were calcu-
lated as described above for all study dogs. Summary statis-
tics for these parameters were calculated for the affected
and unaffected groups, along with detailed descriptives of
each clinical class’s reports for individual clinical signs.
Proportions of owners in each class reporting a ‘breathing
problem’ in their dog were calculated. All statistics were
carried out in PASW Statistics 18 (SPSS).
Results
Demographics
During the study period, of the dogs deemed suitable and
subsequently approached, 285/290 (98.3%) agreed to
participate. The five owners that declined were all of
different breeds, with three of whom indicating their dog
was not comfortable being handled by strangers, and the
remaining two citing lack of time to fill out the question-
naire. A total of 285 owners completed the questionnaires
on 48 crossbred and 237 purebred dogs of 68 breeds. The
study population consisted of 172 males and
113 females, of which 72% were neutered. Dogs
exhibited a wide variety of morphologies, with craniofa-
cial ratios from 0.03 to 0.93
(mean [± SEM] = 0.50 [± 0.01]). This represents the most
extreme end of brachycephaly where, in some cases, the
overnose wrinkle extends more cranially than the length
of the muzzle (Figure 3) through to doliocephalic dogs,
where the muzzle length approaches the cranial length.
Clinical classification
A total of 17 dogs of the study population were referred to
the QMH for investigation of suspected BOAS, and subse-
quently all received a formal diagnosis. These dogs repre-
sented six breeds, and a cross of one of these breeds
(Table 3). From these dogs, inclusion criteria for the
affected group were set as: i) craniofacial ratio 95% confi-
dence interval: 0.12 – 0.23 (or below); ii) ORB score range:
8–27 (or above); and iii) nares ratio 95% confidence
interval: 0.19–0.33 (or below).
A further 14 dogs of the study population that were referred
for disorders other than BOAS met these criteria, resulting
in a total of 31 dogs being classed as affected. Eleven dogs
met two of the three criteria, and were classed as
ambiguous, and 243 met either one (16) or none (227) of the
criteria and were classed as unaffected.
© 2012 Universities Federation for Animal Welfare
Figure 2
Three points on the canine skull used to measure cranial
length (A to B) and muzzle length (B to C). Cranial and muzzle
length, along with muzzle width, have been used to define
terms for certain head shapes, with three terms commonly
used: ‘doliocephalic’, meaning long and narrow headed (as
demonstrated in the English Bull Terrier), ‘mesaticephalic’ or
‘mesocephalic’, meaning a head of medium proportions (as
demonstrated in the Labrador Retriever), and ‘brachycephalic’,
meaning short, wide-headed (as demonstrated in the French
Bulldog) (Evans 1993).
Owner recognition of breathing disorders in brachycephalic dogs 87
Morphometrics
The affected class was represented by seven breeds, and a
cross of one of these breeds (mean craniofacial ratio 0.15).
Five of these breeds were also represented in the
‘ambiguous’ class (mean craniofacial ratio 0.26), along
with a cross of one of these breeds, and a further two breeds
(Table 3). The unaffected class (mean craniofacial ratio
0.56) was represented by 67 purebreeds and their crosses.
Of the 31 affected cases, nares-ratio data were available for
30 dogs (one case underwent emergency airway surgery so
photographs were not possible). The mean nares ratio of
the affected group was 0.24, in comparison to 0.81 in the
unaffected group.
Owner-reported breathing (ORB) score
The median ORB score was 20/40 (range 8–30) for affected
dogs, and 1/40 (range 0–13) for unaffected dogs. Examining
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
Table 3 Breed representation of ‘affected’ and ‘ambiguous’ BOAS cases, breed representation in the whole study
population (including unaffected dogs of the listed breeds), and the mean craniofacial index of these breeds.
Figure 3
Over-nose wrinkle (ONW) extending
more cranially than the tip of the muzzle
and obscuring the nares (N) in the Pug.
NB This feature is discouraged in the Pug
breed standards (Kennel Club 2009):
“Eyes or nose never adversely affected or
obscured by over nose wrinkle. Pinched
nostrils and heavy over nose wrinkle is
unacceptable and should be heavily
penalised”.
Breed ‘Affected’ cases
(n)
‘Ambiguous’
cases (n)
Study population
(n)
Craniofacial index
(mean ± SEM)
Pug 11 1 13 0.08 (± 0.01)
French Bulldog 8 0 8 0.19 (± 0.02)
Bulldog 4 3 9 0.22 (± 0.02)
Boston Terrier 4 0 4 0.15 (± 0.02)
Dogue de Bordeaux 1 2 5 0.36 (± 0.01)
Cavalier King Charles Spaniel 1 0 9 0.38 (± 0.02)
‘Victorian’ Bulldog (Bulldog x Boxer) 1 1 4 0.34 (± 0.06)
Pekingese 1 0 1 0.10
Boxer 0 2 6 0.31 (± 0.01)
Shih Tzu 0 1 7 0.20 (± 0.02)
‘Jug’ (Jack Russell x Pug) 0 1 2 0.25 (± 0.04)
Owner-reported frequencies of breathing difficulties and breathing sounds in BOAS affected and unaffected dogs for (a) owner-
reported frequency of breathing difficulties during activity/exercise, (b) owner-reported frequency of breathing difficulties while asleep,
(c) owner-reported breathing sound characteristics during activity/exercise and (d) owner-reported breathing sound characteristics
reported while asleep.
88 Packer et al
© 2012 Universities Federation for Animal Welfare
Figure 4
Owner recognition of breathing disorders in brachycephalic dogs 89
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
Figure 4 (cont)
90 Packer et al
owner reports of constituent clinical signs of the ORB score
revealed marked differences between the affected and unaf-
fected groups (Figure 4 [a]-[d]). Over 60% of affected cases
(19/31) displayed breathing difficulties during
activity/exercise either daily or more than once per day, in
contrast to unaffected dogs, of which 90% had never expe-
rienced this clinical sign. Also, in this scenario, 68% of
affected dogs were described as ‘snoring, snorting or
wheezing’, in comparison to < 2% of unaffected dogs. The
majority of unaffected dogs (68%) were reported to exhibit
panting during activity/exercise, but with no accompanying
abnormal respiratory noises. One hundred percent of
affected cases were reported to snore while asleep, with
nearly one-third (32.3%) reported to snore almost continu-
ously. In contrast, three-quarters (75.7%) of unaffected dogs
were reported to be ‘very quiet’ while asleep, with snoring
reported in just 21%.
A ‘breathing problem’?
Despite reports of high frequency and severe clinical signs
of BOAS, 58% (18/31) of the owners of BOAS-Affected
dogs reported that their dog did not currently have, or have
a history of, breathing problems. This even included 7/17 of
the owners of formally affected dogs referred for this
disorder, who reported no breathing problem despite the
official diagnosis. This was yet more pronounced in the 14
affected dogs that were not referred for BOAS, of which
only three owners perceived a breathing problem in their
dog. Additional spontaneous comments were provided by
eight of the owners, in explanation of their answer ‘No’, to
the question of the presence of breathing problems. These
comments comprised: “No to breathing problem — other
than being a Bulldog” and “(No,) but he is a Pug!”, with six
other owners simply stating the breed name (two Pugs, two
Bulldogs, one Pekingese and one French Bulldog) in paren-
theses next to this question when answering ‘No’.
Discussion
The aim of this study was to quantify owner recognition of
clinical signs of BOAS, and investigate whether the owners
of dogs exhibiting these signs perceive them as a ‘problem’.
We have demonstrated a disparity in recognition and
perception, with well over half of affected dog owners
reporting a high frequency and severity of clinical signs in
their dogs, without perceiving them as a problem.
Spontaneous comments indicate that this may be due to a
perception of such signs being ‘normal’ in these breeds, and
are consequently accepted as having no immediate need for
veterinary intervention (Torrez & Hunt 2006). In a recent
study of geriatric horses, a similar under-recognition of
disease — especially respiratory disease — was attributed
to owners either mistakenly regarding changes observed in
their animals as normal, benign signs of ageing, rather than
diseases requiring intervention, or being unaware of the
significance of clinical signs, and therefore not seeking
appropriate veterinary attention (Ireland et al 2012). The
concept of age-related ‘normality’ of certain disorders has
similarly been discussed in dogs, in relation to osteoarthritic
disease (Lascelles & Main, 2002). Here, the authors high-
lighted that the presence of this painful disorder in older
animals is often seen as ‘something they have to live with’,
leading to under-recognition of the problem, and under-
treatment of the pain. Human misinterpretation of the
clinical signs of disorders affecting companion animals is
not limited to physical health. A recent study revealed that
dogs exhibiting tail-chasing behaviours at clinical intensi-
ties were over six times more frequently described as
‘stupid’ or ‘funny’ than other dogs, so despite tail-chasing
sometimes being a pathological behaviour, it can remain
untreated, or even be encouraged, because of an assumption
that it is ‘normal’ dog behaviour (Burn 2011).
‘Normal for the breed’
The concept of disorders being ‘normal’ for certain demo-
graphics is a likely constraint to improving the welfare of
clinically affected animals, because if something is consid-
ered ‘normal’ then there may be a perception of no require-
ment to change it. The phrase ‘normal for the breed’, used
by veterinarians, pet owners and breeders alike, indicates a
culture of acceptance of certain problems in certain types of
dog. The following statement, found on several Bulldog
breeding websites internationally as part of a ‘puppy
guarantee’, explicitly demonstrates this acceptance of
certain diseases, including BOAS, as ‘normal’:
English Bulldogs are only covered for a period of one
(1) year from original purchase date. During which
time, this guarantee does not cover what in Bulldog
breeds we consider normal: ‘cherry eye’, entropion,
‘loose hips’, skin allergies, elongated soft palate, small
trachea, stenotic nares (eg Purebred Breeders 2011).
Although some disorders are potentially high prevalence
within certain breeds, the acceptance of them not being a
problem due to their high frequency is detrimental to animal
welfare, and as recently stated by Laurence (2009):
I don’t think it’s acceptable for us to ignore the fact that
every peke and pug has noisy breathing because it has
upper respiratory obstruction. And, I think — and I
include myself in this — we have become immune to
the consequences of these conformations because they
are ‘normal’ for the breed.
The nature of change — at breed and individual dog
level
The gradual nature of changes brought about by selective
breeding has been suggested as a factor contributing to
what we perceive as ‘normal’ (The Boyd Group 1999), as
part of a phenomenon coined by Temple Grandin: “bad
becomes normal” (Grandin & Johnson 2005). Breathing
problems within certain breeds have led to practices to
ameliorate these signs, compensating for physically
compromised animals, with reports over two decades ago
illustrating such practices. Harvey (1989) noted that
breeders of Bulldogs and other brachycephalic breeds carry
oxygen cylinders to shows, and routinely arrange for
Caesarean-section birth of puppies so as not to cause
asphyxiation of the whelping bitch. Such extreme measures
may again be viewed as ‘normal’ to those involved.
© 2012 Universities Federation for Animal Welfare
Owner recognition of breathing disorders in brachycephalic dogs 91
The temporal aspect of change may also act as a
contributing factor to the perception of normality, not just at
breed level, but at the individual dog level. BOAS is a
chronic condition, with early onset of clinical signs, and
severe secondary airway changes observed in immature
dogs aged < 6 months (Pink et al 2006). For owners of dogs
exhibiting signs from such a young age, a truly ‘normal’ or
healthy reference point for their dog may not be present, and
the gradual deterioration of clinical signs associated with
progressive airway changes may not be perceived.
Behavioural changes, such as continual open-mouth
breathing (Hendricks 1992), or extending their head and
neck to keep the airway open (Forrester et al 2001) may not
be perceived as abnormal by owners, as many brachy-
cephalic dogs exhibit these behaviours for the majority of
the time while they are awake. There have previously been
comments that clinical signs such as respiratory noise and
snoring are thought of as ‘cute’ by owners (Milne 2007),
and that other clinical signs such as exercise intolerance
may just be perceived as an ‘inconvenience’, with only
collapse classed as ‘alarming’ to the owner (Singleton
1962). A situation in which clinical signs of a disorder that
has the potential to negatively impact upon affected
animals’ welfare, are perceived by owners as a positive
aspect of their dog, is of particular concern.
The way forward
Due to the welfare implications of BOAS, efforts to
reduce the prevalence of this disorder are needed.
Brachycephalic dogs are increasing in popularity, with
registrations of the Pug alone increasing from 3,500 to
nearly 6,000 per year between 2007 and 2010 (Kennel
Club 2007, 2010b). In terms of the demand for predis-
posed breeds, although the strict criteria dictated by breed
standards for show animals may not be required by
potential pedigree dog purchasers, aesthetics are still
likely to play an important role in what type of dogs are
in demand, with pet breeding strongly linked to fashion
(Ott 1996). Raising awareness of the potential problems
associated with such breeds and conformations may play
an important role here, to ensure informed decisions are
made when selecting puppies; encouraging selection to be
based upon health and not solely on the aesthetics of their
chosen breed. This could be carried out through educa-
tional resources (eg UFAW 2011) and through individual
veterinarian-to-client communications.
Changes to the conformation and subsequent health of
future dogs lies primarily with breeders, as the stakeholders
who make individual breeding decisions. Breeders of
brachycephalic dogs intended for the show ring are
motivated to select animals to maintain breed standards;
however, some standards are inherently putting dogs at risk
of BOAS. BOAS has long been thought of as a consequence
to pedigree breeding practices and breed standards, with
reports from the 1960s stating that:
Present day trends in the breeding of brachycephalic
dogs produce specimens which suffer from dyspnoea to
an ever-increasing degree” (eg Singleton 1962).
Breed standards have recently been updated to help avoid
exaggeration, although there is still room for continued
improvement, as standards still encourage at-risk brachy-
cephalic conformations, eg ‘Muzzle short’ (Japanese Chin:
Kennel Club 2009a), ‘Muzzle relatively short’ (Pug:
Kennel Club 2009a), and ‘Muzzle short, broad, turned
upwards’ (Bulldog: Kennel Club 2010a). Research to
quantify the risk of BOAS across the spectrum of cranio-
facial indices, and the creation of quantitative ‘limits’ to
these extreme conformations, is required to help refine
breed standards in line with health and welfare.
Following recent criticisms of pedigree dogs, the UK
Kennel Club has responded with several initiatives that
have made reference to BOAS, raising awareness of this
problem to breeders. For example, ‘Fit For Function: Fit For
Life’ states that “every dog… should be able to breathe
freely” (Kennel Club 2008). This sentiment is again echoed
in Breed Watch, where obvious breathing difficulty is cited
as an example of poor health and welfare to be avoided, and
‘pinched nostrils’ are classed as undesirable in several
breeds, such as the Pekingese (Kennel Club 2011). As such,
we may be less likely to attribute lack of information as a
reason for the continued breeding of dogs exhibiting clinical
signs and at-risk conformations.
Animal welfare implications
BOAS has potentially severe welfare implications, and if
considered in line with the Companion Animal Welfare
Council’s (CAWC) (2006) assessment of inherited disorders
it can be seen that BOAS:
• Has the potential to affect large numbers of animals; all
brachycephalic dogs may be respiratory compromised to
some degree, with > 10 breeds reported with this disorder in
case series internationally (Table 1);
• Has the potential to continue to do so generation after
generation into the future due to its inherent link with the
brachycephalic conformation — if dogs with at-risk confor-
mations continue to be bred then this problem will be
perpetuated;
• Can have a severe adverse impact on animals’ feelings;
affected dogs are reported to be in chronic respiratory
distress, thermal and physical discomfort, and experience
behavioural restriction due to their impaired physical capa-
bilities; and
• These effects can be of long duration, potentially affecting
the dog for a large part of, or throughout, its life.
Our results show that 58% of the owners of affected animals
claim their dogs have no breathing problem. This suggests
that most dogs with BOAS are not referred for veterinary
advice to help ameliorate the welfare problems associated
with their condition. Without serious appreciation of the
welfare implications of BOAS and effective recognition of
its clinical signs, efforts to reduce the number of affected
animals may be hampered, affected dogs may continue to be
used in breeding programmes, and they may be left
untreated to experience the chronic negative effects of
BOAS for the rest of their lives.
Animal Welfare 2012, 21(S1): 81-93
doi: 10.7120/096272812X13345905673809
92 Packer et al
Acknowledgements
We thank the owners and dogs involved in the study for
their time and co-operation, elective student Joy Axe for
assistance in data collection, the staff of the Clinical
Investigations Centre and the Queen Mother Hospital for
Animals for their ongoing support, UFAW for the
Research and Project Awards funding this work and the
RVC/BBRSC for the Quota Studentship funding RMAP.
The paper was approved for submission (Manuscript ID
number VCS_00256).
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doi: 10.7120/096272812X13345905673809
... The owners' attitude towards health issues related to brachycephalism was examined previously. Health issues are frequently considered normal for the breed in brachycephalic dogs 49 . Even if the dogs show clinical signs of diseases, owners do not perceive these as problems but rather as normal features of the breed 49 . ...
... Health issues are frequently considered normal for the breed in brachycephalic dogs 49 . Even if the dogs show clinical signs of diseases, owners do not perceive these as problems but rather as normal features of the breed 49 . Also, despite the symptoms, owners say their dog is in good health compared to the rest of the breed 47 . ...
... Moreover, they often nd it as a cute feature of their dog 47,49 . However, these symptoms should not be ignored, accepted or liked because they indicate respiratory problems, obstruction of breathing and need intervention 7 . ...
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Full-text available
Brachycephalic (“flat-faced”) dogs are popular despite their health problems. We assumed that people who like brachycephalic dogs have lower knowledge about the associated health problems; they have a specific personality profile and highly value these dogs’ tendencies to form eye contact with humans. We applied an online survey (N = 1156 respondents) and found that, in contrast to our expectations, people with a positive attitude toward brachycephalism associated more health problems with it and did not prefer photos of dogs looking into the camera (“forming eye-contact”) over dogs looking away. In addition, they were more often younger, were women, had children, were less educated, and had a higher level of agreeableness and dog-directed emotional empathy. The results suggest that brachycephalic dogs’ tendency to form eye contact does not contribute to their popularity, and neither high emotional empathy nor knowledge about health problems deters people from liking these dogs. Future research should examine how dog behaviours other than forming eye-contact maintain the popularity of flat-faced dogs and how owners’ sensitivity to fashion trends as well as not recognizing that a dog is suffering from health issues, contribute.
... 3 Many BC dog owners perceive these clinical abnormalities to be normal traits for the breed without being aware of the welfare implications on their pet. 3,18 The perception that these clinical abnormalities are normal is a major barrier to welfare and quality of life improvement in dogs with BOAS. 18 A study of veterinary attitudes towards tackling inherited disorders of pedigree dogs such as BOAS found that one of the most common suggestions to decrease disorder prevalence is to educate the public and potential buyers. ...
... 3,18 The perception that these clinical abnormalities are normal is a major barrier to welfare and quality of life improvement in dogs with BOAS. 18 A study of veterinary attitudes towards tackling inherited disorders of pedigree dogs such as BOAS found that one of the most common suggestions to decrease disorder prevalence is to educate the public and potential buyers. 19 To the authors' knowledge, there has been very little published on the use and impact of an educational intervention on the general public's opinion of BOAS. ...
... 20 In one study, 58% of owners of BC dogs with an owner reported breathing score indicative of BOAS reported that their dogs did not suffer from breathing problems. 18 This included 7/17 dogs which were referred for breathing problems. In our study only 27.9% of BC dog owners believed that their dog had a breathing problem. ...
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Background: The popularity of brachycephalic dogs continues to increase despite inherent breed health problems. Increased education of current and potential brachycephalic dog owners could reduce the desirability of severely affected dogs. Methods: Members of the general public were prospectively recruited to assess their understanding and opinions of brachycephalic breed-related health problems, before and after an educational intervention on brachycephalic obstructive airway syndrome (BOAS). Results: A total of 587 people participated. Before the intervention most participants considered characteristics of BOAS to be normal for brachycephalic dogs. Following the intervention this was moderately reduced. Responses highlighted that defining 'normal' for a breed is difficult. Referring to a trait as 'normal', even in a negative context results in normalisation. 99.7% of participants had an improved understanding of BOAS following the intervention. However, only 53.0% of the total participants and 29.3% of brachycephalic dog owning participants had their opinion of brachycephalic dogs changed. 99.5% of participants believed that potential owners should be more aware of BOAS and 57.3% of brachycephalic dog owners would have liked further information about breed health problems before purchasing their dog. Conclusion: Educational interventions may be beneficial in improving understanding and awareness of BOAS however, normalisation of clinical signs of BOAS remains prevalent.
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... Normalisation of English Bulldogs with clinical signs of BOAS such as stertor, stridor or stenotic nares as 'not unhealthy' appears to be common in the UK, with the owners of over half of brachycephalic dogs with BOAS perceiving these clinical signs (e.g. increased and abnormal respiratory noise) as 'normal for the breed' in two separate populations [63,66]. Mandibular prognathism constitutes a different type of ultra-predisposition in the English Bulldog population surveyed and raises the thorny question of why a conformation that would be considered a serious health issue in one dog breed can be actively selected as a desirable trait in another. ...
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... Despite worryingly high prevalence of BOAS, a condition with a high welfare impact [48], it is likely that the true prevalence of BOAS in Pugs is much higher than reported in the current study. There is strong evidence that the dyspnoea, snoring, air hunger and sleep apnoea that are typical clinical signs of BOAS are widely normalised within the breed (and also in other brachycephalic breeds) and therefore accepted as just being part of 'what makes a Pug a Pug' and adds to the experience of humans of owning a Pug [18,51,58]. Perhaps of even greater concern is that some of these pathological signs are celebrated as desirable characteristic of Pugs, including perceived 'laziness' [51]. ...
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