vanStaverenand Szatmári
Acta Vet Scand (2020) 62:37
https://doi.org/10.1186/s13028-020-00535-1
RESEARCH
Detecting andrecording cardiac murmurs
inclinically healthy puppies inrst opinion
veterinary practice attherst health check
Marie Dirkje Beijken van Staveren and Viktor Szatmári
*
Abstract
Background: The frequency that cardiac murmurs are identified and recorded in first opinion veterinary practices at
the first health check in puppies is unknown. The aims of the study were to assess the agreement between first opin-
ion veterinary practitioners, a veterinary student and a veterinary cardiology specialist on detecting murmurs, and to
establish whether abnormal auscultation findings had been recorded in the health certificates of clinically healthy
puppies. The study included prospective and retrospective investigations, where the prospectively collected ausculta-
tion findings from a veterinary cardiology specialist and a trained veterinary student were compared to auscultation
findings recorded by first opinion veterinary practitioners.
Results: Cardiac auscultation was performed on 331 client-owned, clinically healthy dogs at two time points: at age
34–69 days by a first opinion veterinary practitioner and at age 45–76 days, on average 9 days later, by a veterinary
cardiology specialist and a trained veterinary student. Agreement among the three was compared for the presence
of a murmur. The degree of inter-observer agreement was evaluated using Cohens kappa. Auscultation findings, as
noted in the pets passports, from 331 puppies and 43 different first opinion veterinary practices, were retrospectively
reviewed and prospectively compared with auscultation findings from a veterinary cardiology specialist. Agreement
between the veterinary cardiology specialist and the first opinion veterinary practitioners was poor (ϰ = 0.01) and
significantly different (P < 0.001). First opinion veterinary practitioners had recorded a cardiac murmur in only 1 of the
97 puppies in which the veterinary cardiology specialist detected a murmur. Two-hundred-and-fifty-two puppies
were auscultated by both the veterinary cardiology specialist and the student. Their agreement was fair (ϰ = 0.40) and
significantly different (P = 0.024). The agreement between the student and a first opinion veterinary practitioner on
these 252 puppies was poor (ϰ = 0.03) and significantly different (P < 0.001).
Conclusions: This study shows that soft cardiac murmurs are rarely documented during the first veterinary health
check in puppies by first opinion veterinary practitioners. Although soft murmurs may not be clinically relevant, find-
ing and recording them is evidence of a carefully performed auscultation. Missing a non-pathological murmur is not
of clinical importance; however, missing a pathological murmur could prove detrimental for the individual puppy.
Keywords: Auscultation, Dogs, Inter-observer variability, Screening, Stethoscope
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Background
Soft cardiac murmurs are commonly detected in clini-
cally healthy puppies at 6–8weeks of age, when the first
veterinary health checks generally take place [14]. Soft
murmurs can be either pathologic or non-pathologic [1].
Non-pathological cardiac murmurs are audible murmurs
Open Access
Acta Veterinaria Scandinavica
*Correspondence: v.szatmari@uu.nl
Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht
University, Yalelaan 108, 3584 CM Utrecht, The Netherlands
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vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
in the absence of structural cardiovascular anomalies,
which in puppies and children tend to disappear spon
-
taneously with age [16]. Pathological murmurs in pup-
pies, however, are caused by structural cardiovascular
lesions, most likely due to congenital cardiac anomalies
[1, 7]. ough non-pathological murmurs have no con
-
sequences for the quality of life or life expectancy of
the pet, pathological murmurs may be associated with
increased morbidity and mortality.
Pet passports are official veterinary documents that
contain the individual’s vaccination record and, in the
country in which the present study took place, a section
about the serial health status of each organ (including the
heart) of the puppy. is certificate is filled out by first
opinion veterinary practitioners at each veterinary health
check, which typically coincides with the vaccinations.
e first vaccination usually takes place at 6weeks of age.
Notes in the passport on this date are the only health-
related documentation available for the new owner when
the breeder is selling the puppy shortly after the first
vaccination.
e aims of the present study were to assess the agree
-
ment between first opinion veterinary practitioners, a
student and a veterinary cardiology specialist on detect
-
ing murmurs, and to establish whether or not abnormal
auscultation findings were recorded in the health cer
-
tificates of clinically healthy puppies at the initial physi-
cal examination at the age of 6–8weeks by first opinion
veterinary practitioners. An additional aim of the study
was to compare the auscultation findings of a veterinary
cardiology specialist and a final year specifically trained
veterinary student.
Methods
Study design
e present study includes a combination of prospective
and retrospective investigations, where the prospectively
collected auscultation findings from the veterinary cardi
-
ology specialist and the trained student were compared
to auscultation findings recorded by first opinion vet
-
erinary practitioners. is study design is intentional in
order to assess murmur documentation in first opinion
veterinary practices.
Animals
Between October 2015 and June 2016, 359 client-owned,
apparently healthy puppies from 80 different litters were
brought to the authors’ clinic by their breeders for vol
-
untary screening for congenital portosystemic shunts
using venous blood ammonia concentration measure
-
ment. Puppies were included in the present study if they
were less than 90days old when they were auscultated
by a veterinary cardiology specialist (VSz) and when
their health certificates (i.e. pet passports) were available.
Exclusion criteria were puppies older than 90days of age
and the absence of written documentation in the puppys
health certificate regarding the presence or absence of a
cardiac murmur by a first opinion veterinary practitioner.
In order to establish that the puppies were healthy, the
veterinary cardiology specialist conducted a short owner
interview and performed a focused clinical examination.
Auscultation
All owners signed an informed consent. Each puppy was
placed on a table in a quiet examination room and was
identified by its microchip number. Auscultation was
performed in a standing position on the left and right
hemithorax. After auscultation on the left apical and
basal cardiac regions, the right apical and basal regions
were examined, and finally the left side was auscultated
for a second time [2]. When a murmur was detected,
its intensity (on a scale of 1–6, with 1 being the softest),
the point of maximal intensity (left or right cardiac base
or apex), the timing (systolic and/or diastolic, or con
-
tinuous) and its additional character, such as musical or
intermittently audible, were described [1, 2]. A murmur
was classified as grade 1, if it was very soft, focal and was
heard only after several seconds of careful auscultation;
while a murmur was classified as grade 2 if it was soft,
focal, but was heard immediately [14]. A murmur was
defined as intermittent if a soft (1 or 2 out of 6) mur
-
mur was heard for the first time on the left hemithorax,
but either it disappeared while the auscultation was still
ongoing on the same anatomical location or it could
not be identified when the left hemithorax was aus
-
cultated again [24]. Musical character of the murmur
was defined as a soft, low- to medium-pitched vibrating
sound [2, 5].
Puppies were auscultated by both the veterinary car
-
diology specialist and the student within a 1-h interval.
Both investigators were blinded to each other’s findings
and to the findings of the first opinion veterinary prac
-
titioner until completion of the auscultation of all the
puppies on that day. Heart rates were not recorded. Both
investigators used an acoustic stethoscope with a mem
-
brane diaphragm. e veterinary cardiology specialist’s
stethoscope had a diaphragm diameter of 30mm and the
student’s diaphragm was 45mm. e reasons for using
different stethoscopes were personal preference, logistics
and hygiene.
Prior to participation in the study, the student had
received additional training in cardiac auscultation from
the veterinary cardiology specialist. For this purpose she
auscultated 62 puppies together with the veterinary car
-
diology specialist using her own acoustic stethoscope and
an electronic stethoscope (with a recording possibility)
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vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
on three separate days, approximately 1h per day, in the
first 3weeks of October 2015. e veterinary cardiology
specialist found a murmur in 8 of these puppies. e fol
-
lowing breeds were represented in this subset of dogs: 18
Cairn terriers, 10 Irish wolfhounds, 8 Barbets, 7 Bernese
mountain dogs, 7 Jack Russell terriers, 7 Yorkshire terri
-
ers and 5 Pugs. All but 3 of these puppies (all Yorkshire
terriers) were included in the study population, as both
the veterinary cardiology specialist and a first opinion
veterinary practitioner auscultated them.
e pet passports were examined to assess if the first
opinion practitioners had recorded abnormal ausculta
-
tion findings. ese data were collated after completing
all the examinations for that day. Clinical records from
the first opinion veterinary practitioners were not avail
-
able, as none of the puppies had been referred.
After completion of the data analysis, the veterinary
cardiology specialist phoned each veterinary practice
that was involved in the health checks of at least 3 dogs in
which a cardiac murmur was noted by the veterinary car
-
diology specialist but not by the first opinion veterinary
practitioner. e telephone interviews were conducted
in order to establish documentation routines during the
physical examination. e first opinion veterinarians
were asked whether or not they would routinely record
the presence of soft murmurs on the pet passports even
if the murmurs were suspected to be innocent. e tel
-
ephone interviews with each veterinarian followed the
same structure.
Statistical methods
A commercially available statistical software package
(SPSS 24.0, IBM Corp., Chicago, IL, USA) was used for
data analysis. A P-value of less than 0.05 was considered
to be significant. e age of the dogs is reported in days
as median and range.
e degree of inter-observer agreements were evalu
-
ated by paired comparisons between the veterinary
cardiology specialist, the first opinion veterinary practi
-
tioners and the veterinary student using Cohens kappa
(ϰ). Agreement was regarded as: ‘poor’ ϰ 0.20, ‘fair’
0.21 ϰ 0.40, ‘moderate’ 0.41 ϰ 0.60, substantial’
0.61 ϰ 0.80 or good’ > 0.80.
Results
From the 359 puppies, 28 were excluded from the study
because 1 was too old (262days), 1 had no age recorded,
7 had not been auscultated by a first opinion veterinary
practitioner and 19 were not auscultated by the veteri
-
nary cardiology specialist. A total of 331 puppies from
71 litters, belonging to 10 different breeds, were enrolled.
e following breeds were represented: 214 Cairn terri
-
ers (65%), 26 Dachshunds, 22 Bernese mountain dogs,
16 Jack Russell terriers, 11 Yorkshire terriers, 10 Irish
wolfhounds, 10 Nova Scotia duck tolling retrievers, 9
Norfolk terriers, 8 Barbets and 5 Pugs. e Cairn terriers
belonged to 51 litters and the other breeds belonged to
20 litters.
e median age of the 331 dogs at the time of ausculta
-
tion at the authors’ clinic was 53days (range 45–76days).
e median age of the same dogs when the ausculta
-
tion was performed by a first opinion veterinary practi-
tioner was 45days (range 34–69days), on average 9days
younger. First opinion veterinary practitioners from 43
different veterinary practices filled in the health certifi
-
cates of the puppies. In most instances only the name of
the veterinary practice, but not the veterinarian’s name,
was identifiable in the passports. Because multiple vet
-
erinarians were employed at the majority of the practices,
the number of veterinarians involved was higher than
the number of practices. e exact number is unknown
because the signatures were illegible. ere was no fur
-
ther information available about the circumstances of the
auscultation performed by the first opinion veterinary
practitioners; only the presence or absence of a murmur
was noted.
e veterinary cardiology specialist detected a murmur
in 97 of the 331 puppies (29.3%). e median age of the
puppies with a murmur was 53days (range 45–76days).
Of the 214 Cairn terriers, 80 (37%) had a murmur,
whereas only 17 of the 117 remaining auscultated dogs
(15%) had a murmur. All murmurs were systolic and the
murmur in 82 puppies (85%) had a musical character. e
murmur intensity was grade 2 in 38 puppies and grade 1
in 59 puppies. Of the latter group, the murmur was inter
-
mittently audible in 14 puppies. e point of maximal
intensity was at the region of the left cardiac base in 88
dogs (91%).
In the passports of the 331 puppies, only 2 dogs had a
murmur noted. A murmur was documented by first opin
-
ion veterinary practitioners in only 1 of the 97 puppies
(1%), in which the veterinary cardiology specialist heard
a murmur (Table1). In the other puppy whose passport
recorded the presence of a murmur, the veterinary cardi
-
ology specialist did not hear a murmur (Table1). When
the results of the veterinary cardiology specialist and
the first opinion veterinary practitioners were compared
using Cohens kappa, a poor agreement (ϰ = 0.01) and a
significant difference (P < 0.001) were found.
Of the 331 puppies, 252 were also auscultated by the
trained student. In 66 of these puppies, a murmur was
detected by her. When the results of the student and
the veterinary cardiology specialist were compared, a
fair agreement (ϰ = 0.40) with a significant difference
(P = 0.024) was found (Table2). Comparing the results
of the student and first opinion veterinary practitioners,
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vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
a poor agreement (ϰ = 0.03) with a significant difference
(P < 0.001) was found (Table3).
A number of murmur characteristics were compared
between the student and the veterinary cardiology spe
-
cialist for the 252 dogs that were auscultated by both
investigators. ere was complete agreement about the
timing of the murmurs between both the observers; all
murmurs were recorded as systolic. e point of maxi
-
mal intensity differed between the two observers in only
1 of the 43 dogs: the veterinary cardiology specialist
noted that the point of maximal intensity was the right
cardiac base and the student noted the left cardiac base.
e findings of the two observers on the intensity of the
murmurs showed much more variability, which is shown
in Table4. e most important differences on this aspect
were that the student did not classify any murmur as
being intermittent. e other striking difference was that
in 30 puppies where the veterinary cardiology specialist
detected a murmur, the student recorded no murmur.
Finally, in 13 puppies where the veterinary cardiology
specialist found a grade 2 murmur, the student recorded
the murmur as grade 1.
Ten first opinion veterinary practices were identified
that performed the health checks of at least three dogs in
which a cardiac murmur was noted by the veterinary car
-
diology specialist but not by the first opinion veterinary
practitioner. Veterinarians from these ten first opinion
veterinary practices performed the cardiac auscultation
on 43 of the 96 puppies (45%) in which the cardiolo
-
gist detected a murmur, but in their passports no mur-
mur was noted. In the telephone interview, eight of the
ten veterinarians said that they would always record the
presence of a cardiac murmur in the puppies’ passports
regardless of the murmur intensity. However, there were
two veterinarians who admitted that they do not always
make a note about the presence of a soft murmur in the
passport if they thought that it was innocent.
Discussion
e present study found a poor agreement between the
documented auscultation findings of a veterinary cardi
-
ology specialist and first opinion veterinary practition-
ers regarding the presence of (soft) cardiac murmurs in
331 clinically healthy puppies. A cardiac murmur was
documented by a first opinion veterinary practitioner in
only 1 of the 97 puppies, in which the veterinary cardi
-
ology specialist detected a murmur. On the other hand,
there was only 1 puppy where the first opinion veterinary
Table 1 Results of a veterinary cardiology specialist
(cardiologist) and various rst opinion veterinary
practitioners (practitioners) on the presence or absence
ofacardiac murmur in331 clinically healthy puppies
Practitioners
No murmur Murmur Total
Cardiologist
No murmur 233 1 234
Murmur 96 1 97
Total 329 2 331
Table 2 Results of a veterinary cardiology specialist
(cardiologist) and a trained nal year veterinary student
(student) onthepresence orabsence ofacardiac murmur
in252 clinically healthy puppies
Student
No murmur Murmur Total
Cardiologist
No murmur 145 23 168
Murmur 41 43 84
Total 186 66 252
Table 3 Results of various rst opinion veterinary
practitioners (practitioners) and a trained nal year
veterinary student (student) onthe presence or absence
ofacardiac murmur in252 clinically healthy puppies
Practitioners
No murmur Murmur Total
Student
No murmur 186 0 186
Murmur 64 2 66
Total 250 2 252
Table 4 Dierences intheresults betweentheveterinary
cardiology specialist (cardiologist) and the last year
veterinary student on murmur intensities of the 84
puppies in which the veterinary cardiology specialist
detected amurmur
1/6 = murmur intensity of 1 out of 6
Student
No murmur Intermittent
murmur
1/6 2/6
Cardiologist
Intermittent
murmur
12 0 2 0
1/6 19 0 21 0
2/6 11 0 13 6
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vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
practitioner noted a murmur, but the veterinary cardiol-
ogy specialist did not hear a murmur. is latter puppy
had either a non-pathological murmur that disappeared
spontaneously between the two moments of auscultation
or the stress level (and therefore the heart rate) on the
two occasions was different, making the murmur inaudi
-
ble on the second occasion.
ere are a number of possible explanations for the
discrepancy between the auscultation findings of the vet
-
erinary cardiology specialist and the first opinion veteri-
nary practitioners, including: (1) first opinion veterinary
practitioners did not recognise the soft murmurs, (2)
the health certificates of the pet passports were filled in
without the first opinion veterinary practitioners having
performed an auscultation on the puppies, (3) the first
opinion veterinary practitioners did perform the auscul
-
tation and did hear the murmurs, but they did not note
them in the puppies’ passports, (4) the puppies were aus
-
cultated by the first opinion veterinary practitioners, but
the murmurs were absent at that time, or (5) the veteri
-
nary cardiology specialist overanalysed the presence of
murmurs.
A possible reason why first opinion veterinary prac
-
titioners less frequently noted a cardiac murmur in
the present study could be that they have less time to
devote to cardiac auscultation than a veterinary cardiol
-
ogy specialist, and a murmur with a maximal intensity of
grade 1 may not be immediately noticed [1]. Time pres
-
sure can also mean that no efforts were made to look
for a quiet room, if one was available. Pretest probabil
-
ity of finding a pathological murmur in this population
is very low, because congenital cardiac anomalies have
a low prevalence in the general canine population [7].
However, screening for congenital cardiac anomalies
with a stethoscope is a quick, inexpensive and sensitive
test, which would lead to documentation of the more
prevalent non-pathological cardiac murmurs [2]. e
prevalence of pathological murmurs caused by congeni
-
tal cardiac anomalies in a general, non-referred canine
population was reported to be 0.1% based on a popula
-
tion of 76,301 dogs [7], whereas the prevalence of non-
pathological murmurs in puppies at the age of 7–8weeks
was reported to be 15–31% [2, 3]. e results of the tel
-
ephone interview with the first opinion veterinary prac-
titioners suggest that either the murmur was inaudible
at the time of their auscultation, or they did not detect
them. ough pet passports are official documents, they
might not be the correct source of information, as the
clinical records of the dogs might contain different infor
-
mation. Although differentiating non-pathological from
pathological murmurs can be extremely challenging, if
not impossible by auscultation, especially in cases of soft
systolic murmurs, it is of major importance to perform
the auscultation according to a systematic approach to
detect local murmurs, as well as to document each car
-
diac murmur on the health certificate (i.e. pet passport)
of the puppy at the first veterinary health check. In the
country in which the study was performed, the pet pass
-
port is the only official document about the health status
of the puppy that is available for the new owner when the
breeder sells the puppy.
A minority of interviewed first opinion veterinary prac
-
titioners admitted that they would not always document
the presence of a soft murmur in the health certificate of
the puppy. ere are two possible reasons for this behav
-
iour: (a) assuming that the murmur is non-pathologic or
(b) wanting to avoid conflict with the owner, who is typi
-
cally the breeder at the time of the first health check.
e murmurs in the present study were presumed to
be non-pathologic, however no additional tests, such as
echocardiograms, were performed to establish the origin
of the murmurs, as it was not an aim of the study. Based
on human studies and our previous studies, all murmurs
in the presented group were thought to be innocent [1
6]. is assumption is supported by the fact that the prev
-
alence of soft cardiac murmurs in the population of the
present study (29%) was comparable to the prevalence of
innocent murmurs of our earlier studies (28% and 31%)
performed on populations with very similar characteris
-
tics [2, 3]. Moreover, 20 Cairn terriers from the present
cross-sectional study participated in a longitudinal study
where they were followed up at approximately monthly
intervals [4]. e murmurs in all 20 puppies disappeared
spontaneously [4]. In our experience, non-pathological
murmurs in puppies have auscultation characteristics
similar to the most common type of non-pathological
murmur in children, the “Still’s murmur” [26]. Non-
pathological murmurs in clinically healthy puppies are
always soft (1–2 out of 6) and systolic, and the major
-
ity have a low- to medium-pitched musical (vibrating)
character [24]. According to fairly recently published
guidelines on incidentally detected murmurs in dogs,
non-pathological murmurs can be classified either as
functional or innocent [1]. In both cases no structural
heart disease is present. e difference between the two
types of murmurs is that for the functional murmur a
plausible physiologic explanation can be found (such as
anaemia), whereas for innocent murmurs, no physiologic
explanation can be identified [1]. e genesis of non-
pathological murmurs in the dog is poorly documented.
In children, non-pathological (accidental) murmurs are
thought to arise from turbulent flow in the aorta [5, 6].
In puppies, physiological anaemia has been described as
one of the contributors of the genesis of innocent mur
-
murs, as lower blood viscosity can cause turbulent flow
at lower velocity, presumably in the aorta [1, 2]. With this
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vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
aetiology of physiological anaemia, the above described
veterinary classification of functional versus innocent
murmur is difficult to apply to non-pathological mur
-
murs in healthy puppies.
e murmur intensity in the present population did
not exceed 2 out of 6. Very soft and especially intermit
-
tently audible murmurs can be missed even by veterinary
cardiology specialists who are less experienced in specifi
-
cally searching for innocent murmurs in young puppies,
as shown in our previous studies [2]. Failure to recognise
innocent murmurs does not have negative consequences
for the puppies [1, 2]. However, a potential danger of
missing soft cardiac murmurs is that a louder, possibly
pathological murmur could be classified as a soft, and
probably non-pathological, murmur, and consequently
no referral to a veterinary cardiology specialist would
be recommended to the breeder or the new owner. To
explore this hypothesis, more studies are needed. Miss
-
ing a non-pathological murmur is not clinically impor-
tant, however missing a pathological murmur could be
detrimental for the individual puppy with emotional and
financial sequelae for the breeder and the new owner, as
well as legal consequences for the breeder and for the
first opinion veterinary practitioner. In addition, using a
standardised systematic auscultation protocol, i.e. listen
-
ing in the left and right apical and basal cardiac areas, is
essential to detect non-pathological as well as pathologi
-
cal murmurs. Despite applying a systematic auscultation
protocol, the interpretation of auscultation findings can
still remain subjective [810]. Whether or not the first
opinion veterinary practitioners, whose results were
assessed in the present study, used a standardized sys
-
tematic auscultation protocol remains unknown.
e final year veterinary student, who was trained to
recognise soft cardiac murmurs in puppies immediately
before the start of the study (in a total of 3h on 3 sepa
-
rate days with weekly intervals), had a better agreement
with the veterinary cardiology specialist than first opin
-
ion veterinary practitioners in identifying soft murmurs.
Various human and veterinary studies have investigated
inter-observer variability and the effect of teaching on
recognising cardiac murmurs [816]. e majority of
these studies describe a high inter-observer variability
[810] and conclude that training has a positive effect
on detecting murmurs, especially those with a low inten
-
sity [1113, 1517]. One of these studies investigated
the inter-observer variability of six veterinarians with
different levels of experience in auscultation on recog
-
nising soft systolic murmurs in Cavalier King Charles
spaniels caused by mitral valve insufficiency [8]. e
degree of agreement was found to be poor [8]. Another
study group compared the auscultation skills of ten inter
-
nal medicine specialists, ten first opinion veterinary
practitioners and ten veterinary students in describing
murmur characteristics on recorded equine heart sounds
[9]. High inter-observer variability was found, where only
the specialists were able to provide correct descriptions
[9]. In a different study, six veterinarians with different
levels of experience in cardiac auscultation examined 27
Boxer dogs with and without a murmur [10]. Variable
levels of agreement (Cohens kappa of 0.14–0.75) rang
-
ing from poor to substantial was found, with a positive
correlation with the level of experience [10]. It has been
shown in a human study that even a 1-h long online
teaching session resulted in a significant improvement of
auscultation skills [16]. Another human study emphasises
the importance of repetition (i.e. practice), which is in
line with our previous experience (i.e. learning curve) [2,
12]. Again another human study confirmed that training
led to improved detection of soft, non-pathological mur
-
murs in particular [15]. In children, the observers’ experi-
ence and training were shown as important factors that
played a role in differentiating innocent from pathologic
murmurs [5, 6]. e use of electronic stethoscopes has
been shown to have a positive effect in teaching auscul
-
tation skills [17]. is tool was utilised in the training of
the student of the present study too. However, the type of
stethoscope does not seem to have a documented posi
-
tive effect in identifying auscultation abnormalities [14].
Limitations
An important weakness of the present study is that the
auscultation findings of one veterinary cardiology spe
-
cialist was used as gold standard. However, this study
design is not unusual, as in a similar study with children
the findings of a single paediatric cardiologist were used
as the gold standard [5]. Our previous study on puppies
with non-pathological murmurs showed that an analys
-
able phonocardiogram could only be recorded in 71%
of the population, therefore phonocardiography could
not be used as a gold standard [3]. Including another
veterinary cardiology specialist in the study would have
resulted in more objective findings, as the two specialists
could have acted as each others controls. Unfortunately,
at the time of the study only one veterinary cardiology
specialist was employed at the authors’ institution.
Auscultation by the veterinary cardiology specialist
and the first opinion veterinary practitioners took place
on different days and in different locations. e possi
-
ble importance of these variables is that stress level of
the dogs might have been different, which is thought
to influence the development of soft cardiac murmurs
because of changes in heart rates [1, 10, 18]. First opin
-
ion veterinary practitioners auscultated the puppies on
average 9days before the veterinary cardiology special
-
ist and the trained student. Because lower haematocrit
Page 7 of 8
vanStaverenand Szatmári Acta Vet Scand (2020) 62:37
is known to contribute to the genesis of non-patholog-
ical cardiac murmurs in puppies, the prevalence of soft
(innocent) cardiac murmurs should theoretically be
at least as high or even higher at a younger age, since
(physiological) anaemia has been shown to be less
common with increasing age [1, 2, 19]. erefore, the
discrepancy between the findings of the veterinary car
-
diology specialist and the first opinion veterinary prac-
titioners was less likely the result of a possibly different
prevalence of cardiac murmurs at the two time points;
however, this possibility cannot be ruled out. e dif
-
ferent size of the puppies at the two time points might
have had an effect on the different auscultation findings
too. On the other hand, the authors hypothesise that
the reason for higher prevalence of non-pathological
murmurs in the Cairn terrier breed compared to other
breeds is probably the small size of this breed since
thicker thoracic walls of large-breed dogs may dampen
the soft murmurs to an inaudible level [2]. e greater
degree of agreement between the trained student and
the veterinary cardiology specialist could potentially
be due to the fact that they performed the auscultation
in the same location and within a 1h interval. ere
-
fore, the conditions, which might influence the pres-
ence of non-pathological cardiac murmurs, were more
similar, compared to the conditions of the first opin
-
ion veterinary practitioners. Despite the above men-
tioned shortcomings, the design of the present study
was intentional in order to assess murmur documen
-
tation in first opinion veterinary practices in the field
in a realistic manner. Likewise, an inter-observer vari
-
ability study on schoolchildren in identifying innocent
cardiac murmurs by a single paediatric cardiologist and
several school medical officers had a comparable study
design as that of the present study [5]. at study had
a very similar time interval between the two examina
-
tions (namely 2weeks), and also showed a high inter-
observer variability [5].
e discrepancy between the auscultation findings of
the veterinary cardiology specialist and the student, as
well as that between the veterinary cardiology special
-
ist and the first opinion veterinary practitioners, could
also be the result of the different type of stethoscopes
with different sizes of membrane used. However, in
humans the type of equipment and the diaphragm size
has not been shown to influence the precision of aus
-
cultation [13, 20].
Another limitation of the present study is that the
puppies’ clinical records were not available for review.
It is possible that the presence of a murmur was noted
in the clinical record of the first opinion veterinary
practice, but not in the health certificates (i.e. pet pass
-
ports) of the puppies.
Finally, awareness bias could have played a role in the
different findings between the first opinion veterinary
practitioners and the veterinary cardiology specialist.
e veterinary cardiology specialist and the student
were both aware of their participation in a study con
-
cerning cardiac murmurs, however the first opinion
practitioners were not. If someone is actively searching
for a murmur they are more likely to find one. On the
other hand, in an ideal situation, each examination in
the field should be performed as if the investigator was
participating in a study.
Conclusions
e present study shows that soft cardiac murmurs are
rarely documented during the first veterinary health
check in clinically healthy puppies by first opinion vet
-
erinary practitioners. e most likely explanation for
this finding is that the soft murmurs were not recog
-
nised. ough soft cardiac murmurs may not be clini-
cally relevant, finding them is evidence of a carefully
performed auscultation. Missing an innocent murmur
is not of great clinical importance, but missing a patho
-
logical murmur could prove detrimental for the indi-
vidual puppy. Finally, we conclude that auscultation
skills can be learnt and improved by education and by
adopting a systematic and thorough approach.
Acknowledgements
The authors are grateful to Mrs. Marijke de Vries (Dutch Cairn Terrier Club) and
all the other participating breeders for their voluntary participation in this
project.
The authors thank Dr. Meredith ‘t Hoen and Dr. Simon Swift for the English
linguistic corrections of the manuscript.
Prior publication
A part of this study was presented as an oral research abstract at the yearly
congress of the European College of Veterinary Internal Medicine-Companion
Animals (ECVIM-CA), in Malta on 15 September 2017.
Authors’ contributions
VSz was responsible for the study design. Both authors have equally contrib-
uted to the data collection, data analysis, interpretation of the findings and
writing the manuscript. Both authors read and approved the final manuscript.
Funding
No external funding was involved in this study.
Availability of data and materials
The datasets used and/or analysed during the current study are available from
the corresponding author on reasonable request.
Ethics approval and consent to participate
This study did not require official or institutional ethical approval. The animals
were handled according to high ethical standards and national legislation.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Page 8 of 8
vanStaverenand Szatmári
Acta Vet Scand (2020) 62:37
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Received: 30 January 2020 Accepted: 16 June 2020
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van Staveren and Szatmári Acta Vet Scand (2020) 62:37 Acta Veterinaria Scandinavica
https://doi.org/10.1186/s13028-020-00535-1 RESEARCH Open Access
Detecting and recording cardiac murmurs
in clinically healthy puppies in first opinion
veterinary practice at the first health check
Marie Dirkje Beijken van Staveren and Viktor Szatmári* Abstract
Background: The frequency that cardiac murmurs are identified and recorded in first opinion veterinary practices at
the first health check in puppies is unknown. The aims of the study were to assess the agreement between first opin-
ion veterinary practitioners, a veterinary student and a veterinary cardiology specialist on detecting murmurs, and to
establish whether abnormal auscultation findings had been recorded in the health certificates of clinically healthy
puppies. The study included prospective and retrospective investigations, where the prospectively collected ausculta-
tion findings from a veterinary cardiology specialist and a trained veterinary student were compared to auscultation
findings recorded by first opinion veterinary practitioners.
Results: Cardiac auscultation was performed on 331 client-owned, clinically healthy dogs at two time points: at age
34–69 days by a first opinion veterinary practitioner and at age 45–76 days, on average 9 days later, by a veterinary
cardiology specialist and a trained veterinary student. Agreement among the three was compared for the presence
of a murmur. The degree of inter-observer agreement was evaluated using Cohen’s kappa. Auscultation findings, as
noted in the pets’ passports, from 331 puppies and 43 different first opinion veterinary practices, were retrospectively
reviewed and prospectively compared with auscultation findings from a veterinary cardiology specialist. Agreement
between the veterinary cardiology specialist and the first opinion veterinary practitioners was poor (ϰ = 0.01) and
significantly different (P < 0.001). First opinion veterinary practitioners had recorded a cardiac murmur in only 1 of the
97 puppies in which the veterinary cardiology specialist detected a murmur. Two-hundred-and-fifty-two puppies
were auscultated by both the veterinary cardiology specialist and the student. Their agreement was fair (ϰ = 0.40) and
significantly different (P = 0.024). The agreement between the student and a first opinion veterinary practitioner on
these 252 puppies was poor (ϰ = 0.03) and significantly different (P < 0.001).
Conclusions: This study shows that soft cardiac murmurs are rarely documented during the first veterinary health
check in puppies by first opinion veterinary practitioners. Although soft murmurs may not be clinically relevant, find-
ing and recording them is evidence of a carefully performed auscultation. Missing a non-pathological murmur is not
of clinical importance; however, missing a pathological murmur could prove detrimental for the individual puppy.
Keywords: Auscultation, Dogs, Inter-observer variability, Screening, Stethoscope Background
Soft cardiac murmurs are commonly detected in clini-
cally healthy puppies at 6–8 weeks of age, when the first
veterinary health checks generally take place [1–4]. Soft
*Correspondence: v.szatmari@uu.nl
Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht
murmurs can be either pathologic or non-pathologic [1].
University, Yalelaan 108, 3584 CM Utrecht, The Netherlands
Non-pathological cardiac murmurs are audible murmurs
© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and
the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material
in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material
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zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
van Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 2 of 8
in the absence of structural cardiovascular anomalies, their health certificates (i.e. pet passports) were available.
which in puppies and children tend to disappear spon-
Exclusion criteria were puppies older than 90 days of age
taneously with age [1–6]. Pathological murmurs in pup-
and the absence of written documentation in the puppy’s
pies, however, are caused by structural cardiovascular health certificate regarding the presence or absence of a
lesions, most likely due to congenital cardiac anomalies cardiac murmur by a first opinion veterinary practitioner.
[1, 7]. Though non-pathological murmurs have no con-
In order to establish that the puppies were healthy, the
sequences for the quality of life or life expectancy of veterinary cardiology specialist conducted a short owner
the pet, pathological murmurs may be associated with interview and performed a focused clinical examination.
increased morbidity and mortality.
Pet passports are official veterinary documents that Auscultation
contain the individual’s vaccination record and, in the All owners signed an informed consent. Each puppy was
country in which the present study took place, a section placed on a table in a quiet examination room and was
about the serial health status of each organ (including the identified by its microchip number. Auscultation was
heart) of the puppy. This certificate is filled out by first performed in a standing position on the left and right
opinion veterinary practitioners at each veterinary health hemithorax. After auscultation on the left apical and
check, which typically coincides with the vaccinations. basal cardiac regions, the right apical and basal regions
The first vaccination usually takes place at 6 weeks of age. were examined, and finally the left side was auscultated
Notes in the passport on this date are the only health-
for a second time [2]. When a murmur was detected,
related documentation available for the new owner when its intensity (on a scale of 1–6, with 1 being the softest),
the breeder is selling the puppy shortly after the first the point of maximal intensity (left or right cardiac base vaccination.
or apex), the timing (systolic and/or diastolic, or con-
The aims of the present study were to assess the agree-
tinuous) and its additional character, such as musical or
ment between first opinion veterinary practitioners, a intermittently audible, were described [1, 2]. A murmur
student and a veterinary cardiology specialist on detect-
was classified as grade 1, if it was very soft, focal and was
ing murmurs, and to establish whether or not abnormal heard only after several seconds of careful auscultation;
auscultation findings were recorded in the health cer-
while a murmur was classified as grade 2 if it was soft,
tificates of clinically healthy puppies at the initial physi-
focal, but was heard immediately [1–4]. A murmur was
cal examination at the age of 6–8 weeks by first opinion defined as intermittent if a soft (1 or 2 out of 6) mur-
veterinary practitioners. An additional aim of the study mur was heard for the first time on the left hemithorax,
was to compare the auscultation findings of a veterinary but either it disappeared while the auscultation was still
cardiology specialist and a final year specifically trained ongoing on the same anatomical location or it could veterinary student.
not be identified when the left hemithorax was aus-
cultated again [2–4]. Musical character of the murmur Methods
was defined as a soft, low- to medium-pitched vibrating Study design sound [2, 5].
The present study includes a combination of prospective
Puppies were auscultated by both the veterinary car-
and retrospective investigations, where the prospectively diology specialist and the student within a 1-h interval.
collected auscultation findings from the veterinary cardi-
Both investigators were blinded to each other’s findings
ology specialist and the trained student were compared and to the findings of the first opinion veterinary prac-
to auscultation findings recorded by first opinion vet-
titioner until completion of the auscultation of all the
erinary practitioners. This study design is intentional in puppies on that day. Heart rates were not recorded. Both
order to assess murmur documentation in first opinion investigators used an acoustic stethoscope with a mem- veterinary practices.
brane diaphragm. The veterinary cardiology specialist’s
stethoscope had a diaphragm diameter of 30 mm and the Animals
student’s diaphragm was 45 mm. The reasons for using
Between October 2015 and June 2016, 359 client-owned, different stethoscopes were personal preference, logistics
apparently healthy puppies from 80 different litters were and hygiene.
brought to the authors’ clinic by their breeders for vol-
Prior to participation in the study, the student had
untary screening for congenital portosystemic shunts received additional training in cardiac auscultation from
using venous blood ammonia concentration measure-
the veterinary cardiology specialist. For this purpose she
ment. Puppies were included in the present study if they auscultated 62 puppies together with the veterinary car-
were less than 90 days old when they were auscultated diology specialist using her own acoustic stethoscope and
by a veterinary cardiology specialist (VSz) and when an electronic stethoscope (with a recording possibility)
v an Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 3 of 8
on three separate days, approximately 1 h per day, in the 16 Jack Russell terriers, 11 Yorkshire terriers, 10 Irish
first 3 weeks of October 2015. The veterinary cardiology wolfhounds, 10 Nova Scotia duck tolling retrievers, 9
specialist found a murmur in 8 of these puppies. The fol-
Norfolk terriers, 8 Barbets and 5 Pugs. The Cairn terriers
lowing breeds were represented in this subset of dogs: 18 belonged to 51 litters and the other breeds belonged to
Cairn terriers, 10 Irish wolfhounds, 8 Barbets, 7 Bernese 20 litters.
mountain dogs, 7 Jack Russell terriers, 7 Yorkshire terri-
The median age of the 331 dogs at the time of ausculta-
ers and 5 Pugs. All but 3 of these puppies (all Yorkshire tion at the authors’ clinic was 53 days (range 45–76 days).
terriers) were included in the study population, as both The median age of the same dogs when the ausculta-
the veterinary cardiology specialist and a first opinion tion was performed by a first opinion veterinary practi-
veterinary practitioner auscultated them.
tioner was 45 days (range 34–69 days), on average 9 days
The pet passports were examined to assess if the first younger. First opinion veterinary practitioners from 43
opinion practitioners had recorded abnormal ausculta-
different veterinary practices filled in the health certifi-
tion findings. These data were collated after completing cates of the puppies. In most instances only the name of
all the examinations for that day. Clinical records from the veterinary practice, but not the veterinarian’s name,
the first opinion veterinary practitioners were not avail-
was identifiable in the passports. Because multiple vet-
able, as none of the puppies had been referred.
erinarians were employed at the majority of the practices,
After completion of the data analysis, the veterinary the number of veterinarians involved was higher than
cardiology specialist phoned each veterinary practice the number of practices. The exact number is unknown
that was involved in the health checks of at least 3 dogs in because the signatures were illegible. There was no fur-
which a cardiac murmur was noted by the veterinary car-
ther information available about the circumstances of the
diology specialist but not by the first opinion veterinary auscultation performed by the first opinion veterinary
practitioner. The telephone interviews were conducted practitioners; only the presence or absence of a murmur
in order to establish documentation routines during the was noted.
physical examination. The first opinion veterinarians
The veterinary cardiology specialist detected a murmur
were asked whether or not they would routinely record in 97 of the 331 puppies (29.3%). The median age of the
the presence of soft murmurs on the pet passports even puppies with a murmur was 53 days (range 45–76 days).
if the murmurs were suspected to be innocent. The tel-
Of the 214 Cairn terriers, 80 (37%) had a murmur,
ephone interviews with each veterinarian followed the whereas only 17 of the 117 remaining auscultated dogs same structure.
(15%) had a murmur. All murmurs were systolic and the
murmur in 82 puppies (85%) had a musical character. The Statistical methods
murmur intensity was grade 2 in 38 puppies and grade 1
A commercially available statistical software package in 59 puppies. Of the latter group, the murmur was inter-
(SPSS 24.0, IBM Corp., Chicago, IL, USA) was used for mittently audible in 14 puppies. The point of maximal
data analysis. A P-value of less than 0.05 was considered intensity was at the region of the left cardiac base in 88
to be significant. The age of the dogs is reported in days dogs (91%). as median and range.
In the passports of the 331 puppies, only 2 dogs had a
The degree of inter-observer agreements were evalu-
murmur noted. A murmur was documented by first opin-
ated by paired comparisons between the veterinary ion veterinary practitioners in only 1 of the 97 puppies
cardiology specialist, the first opinion veterinary practi-
(1%), in which the veterinary cardiology specialist heard
tioners and the veterinary student using Cohen’s kappa a murmur (Table 1). In the other puppy whose passport
(ϰ). Agreement was regarded as: ‘poor’ ϰ ≤ 0.20, ‘fair’ recorded the presence of a murmur, the veterinary cardi-
0.21 ≤ ϰ ≤ 0.40, ‘moderate’ 0.41 ≤ ϰ ≤ 0.60, ‘substantial’ ology specialist did not hear a murmur (Table 1). When
0.61 ≤ ϰ ≤ 0.80 or ‘good’ > 0.80.
the results of the veterinary cardiology specialist and
the first opinion veterinary practitioners were compared Results
using Cohen’s kappa, a poor agreement (ϰ = 0.01) and a
From the 359 puppies, 28 were excluded from the study significant difference (P < 0.001) were found.
because 1 was too old (262 days), 1 had no age recorded,
Of the 331 puppies, 252 were also auscultated by the
7 had not been auscultated by a first opinion veterinary trained student. In 66 of these puppies, a murmur was
practitioner and 19 were not auscultated by the veteri-
detected by her. When the results of the student and
nary cardiology specialist. A total of 331 puppies from the veterinary cardiology specialist were compared, a
71 litters, belonging to 10 different breeds, were enrolled. fair agreement (ϰ = 0.40) with a significant difference
The following breeds were represented: 214 Cairn terri-
(P = 0.024) was found (Table 2). Comparing the results
ers (65%), 26 Dachshunds, 22 Bernese mountain dogs, of the student and first opinion veterinary practitioners,
van Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 4 of 8
Table 1 Results of a veterinary cardiology specialist Table 4 Differences in the results between the veterinary
(cardiologist) and various first opinion veterinary cardiology specialist (cardiologist) and the last year
practitioners (practitioners) on the presence or absence veterinary student on murmur intensities of the 84
of a cardiac murmur in 331 clinically healthy puppies
puppies in which the veterinary cardiology specialist detected a murmur Practitioners Student No murmur Murmur Total No murmur Intermittent 1/6 2/6 Cardiologist murmur No murmur 233 1 234 Murmur 96 1 97 Cardiologist Total 329 2 331 Intermittent 12 0 2 0 murmur 1/6 19 0 21 0 2/6 11 0 13 6
Table 2 Results of a veterinary cardiology specialist 1/6 = murmur intensity of 1 out of 6
(cardiologist) and a trained final year veterinary student
(student) on the presence or absence of a cardiac murmur
in 252 clinically healthy puppies
The findings of the two observers on the intensity of the Student
murmurs showed much more variability, which is shown
in Table 4. The most important differences on this aspect No murmur Murmur Total
were that the student did not classify any murmur as Cardiologist
being intermittent. The other striking difference was that No murmur 145 23 168
in 30 puppies where the veterinary cardiology specialist Murmur 41 43 84
detected a murmur, the student recorded no murmur. Total 186 66 252
Finally, in 13 puppies where the veterinary cardiology
specialist found a grade 2 murmur, the student recorded the murmur as grade 1.
Ten first opinion veterinary practices were identified Table
3 Results of various first opinion veterinary that performed the health checks of at least three dogs in
practitioners (practitioners) and a trained final year
veterinary student (student) on the presence or absence which a cardiac murmur was noted by the veterinary car-
of a cardiac murmur in 252 clinically healthy puppies
diology specialist but not by the first opinion veterinary
practitioner. Veterinarians from these ten first opinion Practitioners
veterinary practices performed the cardiac auscultation No murmur Murmur Total
on 43 of the 96 puppies (45%) in which the cardiolo-
gist detected a murmur, but in their passports no mur- Student
mur was noted. In the telephone interview, eight of the No murmur 186 0 186
ten veterinarians said that they would always record the Murmur 64 2 66
presence of a cardiac murmur in the puppies’ passports Total 250 2 252
regardless of the murmur intensity. However, there were
two veterinarians who admitted that they do not always
make a note about the presence of a soft murmur in the
a poor agreement (ϰ = 0.03) with a significant difference passport if they thought that it was innocent.
(P < 0.001) was found (Table 3).
A number of murmur characteristics were compared
between the student and the veterinary cardiology spe- Discussion
cialist for the 252 dogs that were auscultated by both The present study found a poor agreement between the
investigators. There was complete agreement about the documented auscultation findings of a veterinary cardi-
timing of the murmurs between both the observers; all ology specialist and first opinion veterinary practition-
murmurs were recorded as systolic. The point of maxi-
ers regarding the presence of (soft) cardiac murmurs in
mal intensity differed between the two observers in only 331 clinically healthy puppies. A cardiac murmur was
1 of the 43 dogs: the veterinary cardiology specialist documented by a first opinion veterinary practitioner in
noted that the point of maximal intensity was the right only 1 of the 97 puppies, in which the veterinary cardi-
cardiac base and the student noted the left cardiac base. ology specialist detected a murmur. On the other hand,
there was only 1 puppy where the first opinion veterinary
v an Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 5 of 8
practitioner noted a murmur, but the veterinary cardiol-
the auscultation according to a systematic approach to
ogy specialist did not hear a murmur. This latter puppy detect local murmurs, as well as to document each car-
had either a non-pathological murmur that disappeared diac murmur on the health certificate (i.e. pet passport)
spontaneously between the two moments of auscultation of the puppy at the first veterinary health check. In the
or the stress level (and therefore the heart rate) on the country in which the study was performed, the pet pass-
two occasions was different, making the murmur inaudi-
port is the only official document about the health status ble on the second occasion.
of the puppy that is available for the new owner when the
There are a number of possible explanations for the breeder sells the puppy.
discrepancy between the auscultation findings of the vet-
A minority of interviewed first opinion veterinary prac-
erinary cardiology specialist and the first opinion veteri-
titioners admitted that they would not always document
nary practitioners, including: (1) first opinion veterinary the presence of a soft murmur in the health certificate of
practitioners did not recognise the soft murmurs, (2) the puppy. There are two possible reasons for this behav-
the health certificates of the pet passports were filled in iour: (a) assuming that the murmur is non-pathologic or
without the first opinion veterinary practitioners having (b) wanting to avoid conflict with the owner, who is typi-
performed an auscultation on the puppies, (3) the first cally the breeder at the time of the first health check.
opinion veterinary practitioners did perform the auscul-
The murmurs in the present study were presumed to
tation and did hear the murmurs, but they did not note be non-pathologic, however no additional tests, such as
them in the puppies’ passports, (4) the puppies were aus-
echocardiograms, were performed to establish the origin
cultated by the first opinion veterinary practitioners, but of the murmurs, as it was not an aim of the study. Based
the murmurs were absent at that time, or (5) the veteri-
on human studies and our previous studies, all murmurs
nary cardiology specialist overanalysed the presence of in the presented group were thought to be innocent [1– murmurs.
6]. This assumption is supported by the fact that the prev-
A possible reason why first opinion veterinary prac-
alence of soft cardiac murmurs in the population of the
titioners less frequently noted a cardiac murmur in present study (29%) was comparable to the prevalence of
the present study could be that they have less time to innocent murmurs of our earlier studies (28% and 31%)
devote to cardiac auscultation than a veterinary cardiol-
performed on populations with very similar characteris-
ogy specialist, and a murmur with a maximal intensity of tics [2, 3]. Moreover, 20 Cairn terriers from the present
grade 1 may not be immediately noticed [1]. Time pres-
cross-sectional study participated in a longitudinal study
sure can also mean that no efforts were made to look where they were followed up at approximately monthly
for a quiet room, if one was available. Pretest probabil-
intervals [4]. The murmurs in all 20 puppies disappeared
ity of finding a pathological murmur in this population spontaneously [4]. In our experience, non-pathological
is very low, because congenital cardiac anomalies have murmurs in puppies have auscultation characteristics
a low prevalence in the general canine population [7]. similar to the most common type of non-pathological
However, screening for congenital cardiac anomalies murmur in children, the “Still’s murmur” [2–6]. Non-
with a stethoscope is a quick, inexpensive and sensitive pathological murmurs in clinically healthy puppies are
test, which would lead to documentation of the more always soft (1–2 out of 6) and systolic, and the major-
prevalent non-pathological cardiac murmurs [2]. The ity have a low- to medium-pitched musical (vibrating)
prevalence of pathological murmurs caused by congeni-
character [2–4]. According to fairly recently published
tal cardiac anomalies in a general, non-referred canine guidelines on incidentally detected murmurs in dogs,
population was reported to be 0.1% based on a popula-
non-pathological murmurs can be classified either as
tion of 76,301 dogs [7], whereas the prevalence of non-
functional or innocent [1]. In both cases no structural
pathological murmurs in puppies at the age of 7–8 weeks heart disease is present. The difference between the two
was reported to be 15–31% [2, 3]. The results of the tel-
types of murmurs is that for the functional murmur a
ephone interview with the first opinion veterinary prac-
plausible physiologic explanation can be found (such as
titioners suggest that either the murmur was inaudible anaemia), whereas for innocent murmurs, no physiologic
at the time of their auscultation, or they did not detect explanation can be identified [1]. The genesis of non-
them. Though pet passports are official documents, they pathological murmurs in the dog is poorly documented.
might not be the correct source of information, as the In children, non-pathological (accidental) murmurs are
clinical records of the dogs might contain different infor-
thought to arise from turbulent flow in the aorta [5, 6].
mation. Although differentiating non-pathological from In puppies, physiological anaemia has been described as
pathological murmurs can be extremely challenging, if one of the contributors of the genesis of innocent mur-
not impossible by auscultation, especially in cases of soft murs, as lower blood viscosity can cause turbulent flow
systolic murmurs, it is of major importance to perform at lower velocity, presumably in the aorta [1, 2]. With this
van Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 6 of 8
aetiology of physiological anaemia, the above described practitioners and ten veterinary students in describing
veterinary classification of functional versus innocent murmur characteristics on recorded equine heart sounds
murmur is difficult to apply to non-pathological mur-
[9]. High inter-observer variability was found, where only murs in healthy puppies.
the specialists were able to provide correct descriptions
The murmur intensity in the present population did [9]. In a different study, six veterinarians with different
not exceed 2 out of 6. Very soft and especially intermit-
levels of experience in cardiac auscultation examined 27
tently audible murmurs can be missed even by veterinary Boxer dogs with and without a murmur [10]. Variable
cardiology specialists who are less experienced in specifi-
levels of agreement (Cohen’s kappa of 0.14–0.75) rang-
cally searching for innocent murmurs in young puppies, ing from poor to substantial was found, with a positive
as shown in our previous studies [2]. Failure to recognise correlation with the level of experience [10]. It has been
innocent murmurs does not have negative consequences shown in a human study that even a 1-h long online
for the puppies [1, 2]. However, a potential danger of teaching session resulted in a significant improvement of
missing soft cardiac murmurs is that a louder, possibly auscultation skills [16]. Another human study emphasises
pathological murmur could be classified as a soft, and the importance of repetition (i.e. practice), which is in
probably non-pathological, murmur, and consequently line with our previous experience (i.e. learning curve) [2,
no referral to a veterinary cardiology specialist would 12]. Again another human study confirmed that training
be recommended to the breeder or the new owner. To led to improved detection of soft, non-pathological mur-
explore this hypothesis, more studies are needed. Miss-
murs in particular [15]. In children, the observers’ experi-
ing a non-pathological murmur is not clinically impor-
ence and training were shown as important factors that
tant, however missing a pathological murmur could be played a role in differentiating innocent from pathologic
detrimental for the individual puppy with emotional and murmurs [5, 6]. The use of electronic stethoscopes has
financial sequelae for the breeder and the new owner, as been shown to have a positive effect in teaching auscul-
well as legal consequences for the breeder and for the tation skills [17]. This tool was utilised in the training of
first opinion veterinary practitioner. In addition, using a the student of the present study too. However, the type of
standardised systematic auscultation protocol, i.e. listen-
stethoscope does not seem to have a documented posi-
ing in the left and right apical and basal cardiac areas, is tive effect in identifying auscultation abnormalities [14].
essential to detect non-pathological as well as pathologi-
cal murmurs. Despite applying a systematic auscultation Limitations
protocol, the interpretation of auscultation findings can An important weakness of the present study is that the
still remain subjective [8–10]. Whether or not the first auscultation findings of one veterinary cardiology spe-
opinion veterinary practitioners, whose results were cialist was used as gold standard. However, this study
assessed in the present study, used a standardized sys-
design is not unusual, as in a similar study with children
tematic auscultation protocol remains unknown.
the findings of a single paediatric cardiologist were used
The final year veterinary student, who was trained to as the gold standard [5]. Our previous study on puppies
recognise soft cardiac murmurs in puppies immediately with non-pathological murmurs showed that an analys-
before the start of the study (in a total of 3 h on 3 sepa-
able phonocardiogram could only be recorded in 71%
rate days with weekly intervals), had a better agreement of the population, therefore phonocardiography could
with the veterinary cardiology specialist than first opin-
not be used as a gold standard [3]. Including another
ion veterinary practitioners in identifying soft murmurs. veterinary cardiology specialist in the study would have
Various human and veterinary studies have investigated resulted in more objective findings, as the two specialists
inter-observer variability and the effect of teaching on could have acted as each other’s controls. Unfortunately,
recognising cardiac murmurs [8–16]. The majority of at the time of the study only one veterinary cardiology
these studies describe a high inter-observer variability specialist was employed at the authors’ institution.
[8–10] and conclude that training has a positive effect
Auscultation by the veterinary cardiology specialist
on detecting murmurs, especially those with a low inten-
and the first opinion veterinary practitioners took place
sity [11–13, 15–17]. One of these studies investigated on different days and in different locations. The possi-
the inter-observer variability of six veterinarians with ble importance of these variables is that stress level of
different levels of experience in auscultation on recog-
the dogs might have been different, which is thought
nising soft systolic murmurs in Cavalier King Charles to influence the development of soft cardiac murmurs
spaniels caused by mitral valve insufficiency [8]. The because of changes in heart rates [1, 10, 18]. First opin-
degree of agreement was found to be poor [8]. Another ion veterinary practitioners auscultated the puppies on
study group compared the auscultation skills of ten inter-
average 9 days before the veterinary cardiology special-
nal medicine specialists, ten first opinion veterinary ist and the trained student. Because lower haematocrit
v an Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 7 of 8
is known to contribute to the genesis of non-patholog-
Finally, awareness bias could have played a role in the
ical cardiac murmurs in puppies, the prevalence of soft different findings between the first opinion veterinary
(innocent) cardiac murmurs should theoretically be practitioners and the veterinary cardiology specialist.
at least as high or even higher at a younger age, since The veterinary cardiology specialist and the student
(physiological) anaemia has been shown to be less were both aware of their participation in a study con-
common with increasing age [1, 2, 19]. Therefore, the cerning cardiac murmurs, however the first opinion
discrepancy between the findings of the veterinary car-
practitioners were not. If someone is actively searching
diology specialist and the first opinion veterinary prac-
for a murmur they are more likely to find one. On the
titioners was less likely the result of a possibly different other hand, in an ideal situation, each examination in
prevalence of cardiac murmurs at the two time points; the field should be performed as if the investigator was
however, this possibility cannot be ruled out. The dif- participating in a study.
ferent size of the puppies at the two time points might
have had an effect on the different auscultation findings
too. On the other hand, the authors hypothesise that Conclusions
the reason for higher prevalence of non-pathological The present study shows that soft cardiac murmurs are
murmurs in the Cairn terrier breed compared to other rarely documented during the first veterinary health
breeds is probably the small size of this breed since check in clinically healthy puppies by first opinion vet-
thicker thoracic walls of large-breed dogs may dampen erinary practitioners. The most likely explanation for
the soft murmurs to an inaudible level [2]. The greater this finding is that the soft murmurs were not recog-
degree of agreement between the trained student and nised. Though soft cardiac murmurs may not be clini-
the veterinary cardiology specialist could potentially cally relevant, finding them is evidence of a carefully
be due to the fact that they performed the auscultation performed auscultation. Missing an innocent murmur
in the same location and within a 1 h interval. There-
is not of great clinical importance, but missing a patho-
fore, the conditions, which might influence the pres-
logical murmur could prove detrimental for the indi-
ence of non-pathological cardiac murmurs, were more vidual puppy. Finally, we conclude that auscultation
similar, compared to the conditions of the first opin-
skills can be learnt and improved by education and by
ion veterinary practitioners. Despite the above men-
adopting a systematic and thorough approach.
tioned shortcomings, the design of the present study
was intentional in order to assess murmur documen- Acknowledgements
The authors are grateful to Mrs. Marijke de Vries (Dutch Cairn Terrier Club) and
tation in first opinion veterinary practices in the field all the other participating breeders for their voluntary participation in this
in a realistic manner. Likewise, an inter-observer vari- project.
ability study on schoolchildren in identifying innocent
The authors thank Dr. Meredith ‘t Hoen and Dr. Simon Swift for the English
linguistic corrections of the manuscript.
cardiac murmurs by a single paediatric cardiologist and
several school medical officers had a comparable study Prior publication
design as that of the present study [5]. That study had A part of this study was presented as an oral research abstract at the yearly
congress of the European College of Veterinary Internal Medicine-Companion
a very similar time interval between the two examina-
Animals (ECVIM-CA), in Malta on 15 September 2017.
tions (namely 2 weeks), and also showed a high inter- observer variability [5]. Authors’ contributions
VSz was responsible for the study design. Both authors have equally contrib-
The discrepancy between the auscultation findings of uted to the data collection, data analysis, interpretation of the findings and
the veterinary cardiology specialist and the student, as writing the manuscript. Both authors read and approved the final manuscript.
well as that between the veterinary cardiology special- Funding
ist and the first opinion veterinary practitioners, could No external funding was involved in this study.
also be the result of the different type of stethoscopes
with different sizes of membrane used. However, in Availability of data and materials
The datasets used and/or analysed during the current study are available from
humans the type of equipment and the diaphragm size the corresponding author on reasonable request.
has not been shown to influence the precision of aus- cultation [13, 20].
Ethics approval and consent to participate
This study did not require official or institutional ethical approval. The animals
Another limitation of the present study is that the were handled according to high ethical standards and national legislation.
puppies’ clinical records were not available for review.
It is possible that the presence of a murmur was noted Consent for publication Not applicable.
in the clinical record of the first opinion veterinary
practice, but not in the health certificates (i.e. pet pass- Competing interests ports) of the puppies.
The authors declare that they have no competing interests.
van Staveren and Szatmári Acta Vet Scand (2020) 62:37 Page 8 of 8
Received: 30 January 2020 Accepted: 16 June 2020
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Document Outline

  • Detecting and recording cardiac murmurs in clinically healthy puppies in first opinion veterinary practice at the first health check
    • Abstract
      • Background:
      • Results:
      • Conclusions:
    • Background
    • Methods
      • Study design
      • Animals
      • Auscultation
      • Statistical methods
    • Results
    • Discussion
      • Limitations
    • Conclusions
    • Acknowledgements
    • References