Electrocardiographic findings in healthy Cavalier King Charles Spaniels, Pugs, and English Bulldogs

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Electrocardiographic findings in healthy
Cavalier King Charles Spaniels, Pugs, and English Bulldogs
Giovanni Romito, DVM, MSc, PhD, DECVIM1*; Prisca Castagna, DVM, MSc2; Maria Chiara Sabetti, DVM3;
Mario Cipone, DVM1

1Department     of Veterinary Medical Sciences, Alma Mater Studiorum—University of Bologna, Ozzano dell’Emilia, Italy
2 Freelance   veterinary cardiologist, Bologna, Italy
3Department     of Veterinary Sciences, University of Parma, Parma, Italy
*Corresponding author: Dr. Romito (giovanni.romito2@unibo.it)
Received December 6, 2022.
Accepted January 5, 2023.
doi.org/10.2460/javma.22.12.0542

OBJECTIVE
To describe the ECG findings in 3 different canine brachycephalic breeds: the Cavalier King Charles Spaniel, the Pug,
and the English Bulldog (EB).
ANIMALS
135 healthy dogs (50 Cavalier King Charles Spaniels, 50 Pugs, and 35 EBs).
PROCEDURES
Medical records were retrospectively reviewed to identify healthy dogs ≥ 1 year old that had undergone an ECG. The
Mann-Whitney U test or the Student t test were used to compare continuous variables between male and female
dogs, whereas the χ2 test was used for categorical variables. Spearman correlation coefficients between ECG mea-
surements and age and body weight were also calculated in the case of continuous variables, whereas the Kruskal-
Wallis test was used for categorical ones.
RESULTS
Electrocardiographic parameters of healthy Cavalier King Charles Spaniels overall fitted with traditional reference
intervals cited in textbooks; in contrast, 28% of Pugs and 20% of EBs showed a shift of the QRS-complex mean electri-
cal axis (QRS-MEA). In Pugs and EBs, the mean/median QRS-MEA value was 56° (from 0° to 100°) and 59° (from
20° to 100°), respectively. All axis shifts were left shifts (in Pugs, from 0° to 34°; in EBs, 20° to 39°). Only a few
meaningful differences were found when comparing ECG variables between males and females. Similarly, only 1
statistically significant correlation was found between ECG parameters and age and body weight.
CLINICAL RELEVANCE
Healthy Pugs and EBs present a trend to a left shift of the QRS-MEA. This should be considered when interpreting
ECG tracings in these breeds.

In recent years, canine brachycephalic breeds have
 become increasingly common worldwide.1–5 As
health concerns for brachycephalic dogs have ag-
                                                                    brachycephalic breeds,8–10 studies describing spe-
                                                                    cific ECG features in these breeds are limited.11 Ac-
                                                                    cordingly, ECG analysis in brachycephalic dogs is still
gregated over the past decade, dogs from these                      based on comparison with traditional RIs provided
breeds often undergo veterinary examinations. Due                   by textbooks. Regrettably, this may lead to misdiag-
to the predisposition of some brachycephalic dogs                   nosis, as these ranges represent general cutoffs that
to heart diseases (eg, myxomatous mitral valve dis-                 may be applicable to many, but not all dogs. Such
ease in Cavalier King Charles Spaniels [CKCSs]6 or                  a discrepancy may be become evident in subjects
arrhythmogenic cardiomyopathy in English Bulldogs                   with extreme phenotypes, as in the case of some
[EBs]7), diagnostic tests often include transthoracic               brachycephalic dogs.11 For example, a recent inves-
echocardiography and surface ECG. An essential                      tigation11 in healthy French Bulldogs documented a
step for a proper interpretation of both tests is the               physiological left shift of the ventricular mean elec-
comparison of recorded measurements with refer-                     trical axis (MEA) mimicking a ventricular conduction
ence intervals (RIs). Although many studies have                    disturbance in 30% of the subjects. Given the paucity
provided specific echocardiographic RIs for various                 of data on the ECG parameters of other brachyce-

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phalic breeds, it remains to be clarified whether the     relaxed dogs. All ECGs were recorded using a com-
aforesaid finding is a peculiarity of French Bulldogs     mercially available machine (Cube ECG; Cardioline
alone or whether it also occurs in other brachyce-        SpA). The ECG leads were attached to the skin by
phalic dogs. Furthermore, it remains to be estab-         flattened alligator clips at the level of the olecranon
lished whether brachycephalic breeds different from       on the caudal aspect of the forelimb and over the
the French Bulldog may show further ECG peculiari-        patellar ligaments on the cranial aspect of the hind
ties potentially related to their conformation.           limbs.17 Alcohol was applied to maintain electrical
     Therefore, the aim of this study was to evalu-       contact with the skin. Standard 6-lead ECGs (leads I,
ate the main components of surface ECG in healthy         II, III, aVR, aVL, and aVF) were recorded for at least
dogs from brachycephalic breeds different from the        1 minute in all dogs at a paper speed of 50 mm/s
French Bulldog and to compare the findings with           and paper sensitivity of 10 mm/mV. The same inves-
traditional RIs. We hypothesized that peculiar ECG        tigator (GR) manually measured intervals and ampli-
features diverging from general ranges of normality       tudes using a caliper and ruler with 0.5-mm gradua-
could be identified in the ECG tracings of these dogs.    tions. Initially, the cardiac rhythm was analyzed and
                                                          classified as sinus or pathological rhythm. For the
                                                          purpose of this study, only dogs with sinus rhythms
Materials and Methods                                     could be enrolled. Then, the heart rate in beats per
                                                          minute was calculated by determining the number of
Study population                                          QRS complexes in a 3-second interval and multiply-
     For the purpose of this retrospective analysis,      ing this number by 20. Subsequently, measurements
medical records of healthy CKCSs, Pugs, and EBs           of the main ECG components were made as previ-
that had undergone an ECG as part of their diagnos-       ously described.11,19,20 These included the duration,
tic evaluation at the authors’ institutions between       amplitude, and MEA in the frontal plane of the P
January 2014 and November 2022 were reviewed              wave; PQ-interval duration; duration and MEA of the
by a board-certified cardiologist (GR). These breeds      QRS complex (QRS-MEA); R-wave amplitude; pres-
were purposefully selected for 2 reasons. First, they     ence or absence of ST-segment deviation and its am-
represent the 3 most popular brachycephalic canine        plitude; polarity, amplitude, and MEA of the T wave;
breeds apart from French Bulldogs,1–5 which intrin-       and duration of the QT interval and the QT interval
sically increases the potential clinical utility of our   corrected for heart rate according to the logarith-
research. Second, they allowed the investigation of       mic formula (ie, QT interval corrected for heart rate
the possible effect of somatotype on ECG findings by      = log600 X QT/logRR).21 Three representative con-
creating 3 distinct study groups: (1) brachycephalic      secutive beats were used to measure various ECG
dogs with mesomorphic chest conformation, namely          variables, and the results were averaged for each
CKCSs; (2) small-sized brachycephalic dogs with           variable. Amplitudes and durations were measured
brachymorphic chest conformation, namely Pugs;            in lead II and expressed in millivolts and milliseconds,
and (3) medium-sized dogs with brachymorphic              respectively. Lead II was also used to assess the
chest conformation, namely EBs.12–16 Reasons for          presence or absence of ST-segment deviation and
ECG analysis in an apparently healthy subject could       the T-wave polarity. The MEA was calculated using
include preoperative evaluation before elective sur-      the following equation: MEA = arctan (Iamp, aVFamp)
geries (eg, castration, spaying) or cardiac screening     X 180/π.11,22 The terms right shift and left shift were
in breeds known to be predisposed to heart diseases.      used to define a QRS-MEA between 100° and –80°
To be included, dogs had to be at least 1 year of age     and between 40° and –60°, respectively.11 In addition
and have a complete case record, including signal-        to these variables, we also assessed the QRS-complex
ment, history, clinical findings, and cardiac investi-    morphological pattern in lead II. By convention, we
gation. The latter had to include at least a transtho-    classified it using upper- and lowercase letters when
racic echocardiography and a 1-minute 6-lead ECG          the wave’s amplitude was ≥ 0.5 mV (ie, Q, R, S) or <
performed according to standardized techniques            0.5 mV (ie, q, r, s), respectively.11,22
(details below).17,18 Dogs were considered healthy
based on an unremarkable clinical history and physi-      Statistical analysis
cal examination as well as on normal ECG and echo-            Statistical analysis was performed with com-
cardiographic findings. Dogs were excluded if they        mercially available statistical software (MedCalc ver-
had any cardiac or extracardiac disease and if they       sion 19.5.1; MedCalc Software Ltd). All continuous
needed sedation or were receiving any therapy at          variables were tested for their distribution with a
the time of cardiovascular examination.                   Shapiro-Wilk normality test. Descriptive statistics in-
                                                          cluded mean ± SD for normally distributed data and
ECG analysis                                              median and range (minimum to maximum) for data
    In all dogs, an ECG was conducted with the dogs       that were not normally distributed. The Mann-Whit-
positioned and manually restrained in right lateral re-   ney U test or Student t test were used to compare
cumbency, with the front legs placed parallel to each     continuous variables among male and female dogs
other and perpendicular to the long axis of the body      based on their distribution, whereas the χ2 test was
and the hind limbs in a neutral semiflexed position.17    used for categorical variables. Spearman correlation
The animals were unsedated and were allowed time          coefficients (rs) between ECG measurements and
to acclimatize so that the ECG could be taken from        age and body weight (BW) were also calculated for

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continuous variables, whereas the Kruskal-Wallis test              trated). The median age and BW were 5 years (1 to
was used for categorical ones. A value of P < 0.05 was             15 years) and 8.5 kg (4.7 to 12 kg), respectively. All
considered significant.                                            Pugs had a normal sinus rhythm. All ECG parameters
                                                                   were within the traditional RIs, with the exception
Results                                                            of QRS-MEA (Table 2). Indeed, 14 of 50 (28%) dogs
                                                                   showed a left-shift of QRS-MEA (0° to 34°). Con-
     The study population consisted of 135 healthy                 cerning QRS-complex morphology, 6 patterns were
dogs, including 50 CKCSs, 50 Pugs, and 35 EBs.                     identified; the most common was the qR (24/50
Among the CKCSs, 27 were females (15 entire and                    [48%]), followed by the qRs (9/50 [18%]), the QR
12 spayed) and 23 were males (22 entire and 1 cas-                 (8/50 [16%]), the Rs (6/50 [12%]), the R (2/50 [4%]),
trated). The median age and BW were 3 years (1 to                  and the qr (1/50 [2%]). Concerning ST segment, 5 of
10 years) and 8.7 kg (4.7 to 14.1 kg), respectively. All           50 (10%) dogs showed a deviation; in all cases, it was
CKCSs had a normal sinus rhythm. Moreover, in this                 a segment depression. Concerning T-wave polarity,
breed, the ECG parameters were all within the tradi-               29 of 50 (58%) showed a positive T wave, 13 of 50
tional RIs, with the only exception of 1 dog showing               (26%) a negative one, and 8 of 50 (16%) a neutral one.
a T-wave MEA outside the reported range of normal-                      Among the EBs, 19 were females (16 entire and
ity (ie, –162°; lower RI, –146°19; Table 1). Concern-              3 spayed) and 16 were males (13 entire and 3 cas-
ing QRS-complex morphology, 2 patterns were iden-                  trated). The median age and BW were 2 years (1 to 9
tified; the most common was the qRs (43/50 [86%]                   years) and 26 kg (18 to 33 kg), respectively. All EBs
dogs), followed by the qR (7/50 [14%] dogs). Con-                  had a normal sinus rhythm. All ECG parameters were
cerning ST segment, 31 of 50 (62%) dogs showed a                   within the traditional RIs, with the exception of QRS-
deviation; in all cases, it was a segment depression.              MEA (Table 3). Indeed, 7 of 35 (20%) dogs showed a
Concerning T-wave polarity, 30 of 50 (60%) dogs                    left shift of QRS-MEA (20° to 39°). Concerning QRS-
showed a negative T wave, 17 of 50 (34%) a neutral                 complex morphology, 3 patterns were identified; the
one, and 3 of 50 (6%) a positive one.                              most common was the qR (27/35 [77%]), followed
     Among the Pugs, 23 were females (19 entire and                by the qRs (5/35 [14%]) and the R (3/35 [9%]). Con-
4 spayed) and 27 were males (24 entire and 3 cas-                  cerning ST segment, 3 of 50 (6%) dogs showed a de-

Table 1—Descriptive statistics for selected electrocardiographic parameters in healthy Cavalier King Charles Spaniels.
Variable                           Mean/median                 SD/min-max                    RIs                      References
P duration (ms)                    35                          30 to 40                      ≤ 40                     11, 23, 24
P amplitude (mV)                   0.2                         ± 0.07                        < 0.4                    23, 24
P MEA (°)                          64                          ± 16                          –18 to 90                24
PQ duration (ms)                   85                          ± 13.5                        60 to 130                23, 24
QRS duration (ms)                  70                          60 to 70                      ≤ 70                     11, 24
QRS MEA (°)                        73                          ± 18                          40 to 100                23, 24
Q amplitude (mV)                   –0.3                        ± 0.12                        —                        —
R amplitude (mV)                   1.6                         ± 0.44
Table 3—Descriptive statistics for selected electrocardiographic parameters in healthy English Bulldogs.
Variable                      Mean/median                  SD/min-max               RIs                    References
P duration (ms)               40                           25 to 40                 ≤ 40                   11, 23, 24
P amplitude (mV)              0.18                         ± 0.1                    < 0.4                  23, 24
P MEA (°)                     53                           ± 18                     –18 to 90              24
PQ duration (ms)              93                           ± 16                     60 to 130              23, 24
QRS duration (ms)             56                           ±9                       ≤ 70                   11, 24
QRS MEA (°)                   59                           ± 22                     40 to 100              23, 24
Q amplitude (mV)              –0.25                        ± 0.1                    —                      —
R amplitude (mV)              1.22                         ± 0.3
Figure 1—Electrocardiographic tracing from a Cavalier King Charles Spaniel. Note that the QRS-complex mean elec-
trical axis is normal (87°). Paper speed = 50 mm/s; 1 cm = 1 mV.

Figure 2—Electrocardiographic tracing from an English Bulldog. Note the left shift of the QRS-complex mean elec-
trical axis (30°). Paper speed = 50 mm/s; 1 cm = 1 mV.

which may be also observed by comparing thoracic           the right (up to 120°) are commonly documented in
radiographs of dogs with different chest shapes,31,32      tall persons with long, thin chests, likely as a result of
may allow for different direction of the mean electrical   the position of the hearts, which lies more vertically;
vector. This, in turn, may lead to different QRS-MEA       in contrast, the QRS-MEA of persons with short chests
values in dogs with different thoracic conformations.      is usually shifted toward the left, likely as a result of
Data from human medicine may further support the           a heart lying more horizontally (up to –30°).26 These
importance of the chest shape in determining the           findings highlight the importance of not considering
QRS-MEA. Indeed, QRS-MEA values pointing toward            brachycephalic dogs as a single homogeneous cate-

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gory during ECG analysis. Furthermore, they empha-           ing it isoelectric in some dogs from these breeds. Hy-
size the importance of paying more attention to the          pothetically, the undetectability of the S wave may be
shape of the thorax (ie, by distinguishing dogs with         further exacerbated by the tendency of some brachy-
a brachymorphic chest conformation from those with           morphic dogs to accumulate adipose tissue around the
a mesomorphic/dolichomorphic one) rather than that           heart,39 which has a low electric conductivity and may
of the skull (ie, by merely distinguishing brachyce-         make the detection of low-voltage deflections (such as
phalic dogs from nonbrachycephalic ones), especially         the S wave) more challenging.
when interpreting the QRS-MEA.                                     An additional finding worthy of mention concerns
     The choice of enrolling both small-sized and me-        the T wave, an ECG parameter traditionally neglected
dium-sized brachymorphic dogs (ie, Pugs and EBs,             in the veterinary literature, whose clinical relevance has
respectively) gave us the opportunity to gain data on        been highlighted in dogs in recent years40 and whose
the role of the body dimension on QRS-MEA. Interest-         RIs have recently been documented in this species.19
ingly, similar findings were obtained when analyzing         Intriguingly, negative T waves were overrepresented in
the QRS-MEA in Pugs and EBs, both in terms of medi-          CKCSs, whereas Pugs and EBs showed predominantly
an value and number of subjects showing a left shift.        positive T waves. A previous investigation19 in a large
Moreover, our statistical analysis ruled out a meaning-      population of healthy dogs showed that T-wave polar-
ful effect of BW on QRS-MEA in any of the enrolled           ity can be physiologically positive, negative, and neu-
breeds. These findings suggested that the chest              tral in this species.19 Nevertheless, given the heteroge-
shape is likely to play a more important role than the       nicity of that study population (ie, 129 subjects from
body dimension in influencing the canine QRS-MEA.            25 breeds, including brachymorphic, mesomorphic,
     As age and sex have been reported in humans             and dolichomorphic dogs), whether the T-wave polar-
to have some influence on several ECG parameters,            ity may be influenced by the somatotype in some spe-
including the QRS-MEA,33–36 part of our statistical          cific breeds remains to be conclusively clarified. Results
analysis was aimed at exploring the possible effects         for the present study may have provided preliminary
of these demographic variables on the ECG measure-           information in that regard, suggesting that mesomor-
ment obtained in our study populations. Contrary to          phic and brachymorphic dogs may show an opposite
human medicine, we were unable to observe any sta-           T-wave polarity. As hypothesized for the QRS-MEA,
tistical differences related to age and sex in any breed.    theoretically, this finding could be partially affected by
This may be due to the lack of puppies and juvenile          the chest conformation, which, in turn, may lead to a
dogs (ie, < 1 year old),37 the paucity of geriatric dogs     different orientation of the ventricular repolarization
(≥ 12 years old),37 and the inhomogeneous number of          front. In addition to thoracic shape, other factors that
males and females enrolled in our study. At the same         may differ between mesomorphic and brachymorphic
time, the disagreement between our results and find-         dogs and may affect the T-wave features include the
ings reported in the human literature may also reflect       myocardial mass, the myocardial tissue resistivity, and
intrinsic species-related differences. Anyway, the lack      the extent of epicardial fat.39,41,42 Nevertheless, these
of meaningful effects of the studied demographic             speculations need to be confirmed and expanded fur-
variables (ie, age, sex, and BW) on QRS-MEA seems            ther by additional studies.
to further support the hypothesis that the chest con-              A last interesting result concerned the ST-seg-
formation likely represented the main determinant of         ment deviation, a clinically relevant ECG finding43,44
this ECG parameter in our study population.                  that has recently attracted the attention of veterinary
     Another interesting result from this research con-      cardiologists.20 In our study, ST-segment deviations
cerns the QRS-complex morphological patterns, as             were identified more commonly in CKCSs (62% of
dogs from the brachycephalic breed with a mesomor-           cases), compared with Pugs and EBs (10% and 6% of
phic chest conformation (ie, CKCSs) tended to show           cases, respectively), and manifested predominantly
predominantly a qRs pattern, whereas a qR one was            as a segment depression. The latter finding is in line
overrepresented in dogs from the 2 brachycephalic            with a recent investigation20 on the ST-segment fea-
breeds with brachymorphic chest conformation (ie,            tures from 180 healthy dogs from 34 breeds, as seg-
Pugs and EBs). The latter result appears in line with a      ment depression was overrepresented among dogs
recent study11 on the ECG features of French Bulldogs,       with ST-segment deviation in that study (ie, 84% of
as the qR pattern was the most common in this brachy-        cases). Instead, the high prevalence documented in
morphic breed. The explanations of these results are         CKCSs is somewhat unexpected, as only 24% of dogs
not immediately clear. Admittedly a speculative hy-          had an ST-segment deviation in the aforesaid report.
pothesis, yet plausible, is that the counterclockwise        Further studies are needed to confirm this prelimi-
rotation often observed in many Pugs and EBs may             nary result and conclusively establish whether the
change the alignment between lead II (ie, the lead used      different prevalence of ST-segment deviation among
for analyzing the QRS-complex morphological pattern          CKCSs, Pugs, and EBs documented herein is due,
in the present study as well as the one by Romito et al11    at least in part, to some biological/conformational
on French Bulldogs) and that of the terminal depolar-        characteristics, including the chest shape.
ization wave front depicted by the S wave (ie, the one             Results from this study may be helpful in the clinical
traveling over the Purkinje fibers to depolarize the bas-    setting, for example because they could prevent veteri-
al regions of the left ventricular free wall and septum      narians from interpreting systematically the QRS-MEA
to complete electrical ventricular activation).24,38 This,   of Pugs and EBs as a true disturbance of ventricular con-
in turn, may reduce the amplitude of the S wave, mak-        duction. This, in turn, may contribute to reduce, at least

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in some cases, the unneeded prescription of expensive                  tative study of Danish owners of four small dog breeds.
and potentially stressful complementary diagnostic                     PLoS One. 2017;12(2):e0172091. doi:10.1371/journal.
                                                                       pone.0172091
tests (eg, transthoracic echocardiography) that are of-
                                                                 2.    Le Top 20 des races préférées des Français. Société Centrale
ten requested when an ECG anomaly is suspected.                        Canine. Accessed November 28, 2022. https://www.centrale-
     This study had some limitations. First, although                  canine.fr/articles/statistiques-du-lof-en-2017-le-berger-aus-
the total number of dogs we enrolled is higher than                    tralien-futur-ndeg1
that of previous canine studies11,15 evaluating breed-           3.    Australia’s top trending dog breeds and names. Hill’s Pet
or somatotype-related differences in QRS-MEA, the                      Nutrition. Accessed November 28, 2022. https://www.
                                                                       hillspet.com.au/dog-care/australias-top-trending-dog-
sample size of each single breed was relatively small.
                                                                       breeds
Therefore, additional studies enrolling a higher num-            4.    Leading 20 dog breeds in the United Kingdom (UK) in 2021,
ber of dogs as well as additional brachycephalic breeds                based on number of registrations. Statista. Accessed Novem-
are needed to validate and further expand our data. In                 ber 28, 2022. https://www.statista.com/statistics/915202/
that regard, it is also important to underline that our                top-dog-breeds-by-registered-number-united-kingdom-
findings cannot be extrapolated to all brachycephalic                  uk/
                                                                 5.    Most popular breeds of 2021. American Kennel Club.
dogs, as only 3 brachycephalic breeds were enrolled.
                                                                       Accessed November 28, 2022. https://www.akc.org/
Second, our statistical analysis did not include a cor-                expert-advice/dog-breeds/most-popular-dog-breeds-
relation between ECG variables and body condition                      of-2021/
score. Theoretically, such a correlation could have              6.    O’Brien MJ, Beijerink NJ, Wade CM. Genetics of ca-
added interesting findings, as an increased amount                     nine myxomatous mitral valve disease. Anim Genet.
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heart and electrodes and can change the position of
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the heart in the thorax (which, in turn, can potentially               uation of clinical and histopathologic features, progres-
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were not all systematically subjected to blood tests,                  2022;40:170–183. doi:10.1016/j.jvc.2021.10.003
which made it impossible to conclusively exclude                 8.    Misbach C, Lefebvre HP, Concordet D, et al. Echocardiog-
the possibility that some hematologic abnormalities                    raphy and conventional Doppler examination in clini-
                                                                       cally healthy adult Cavalier King Charles Spaniels: effect
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However, in our opinion, it is unlikely that significant               reference intervals. J Vet Cardiol. 2014;16(2):91–100.
laboratory changes able to remarkably affect the ECG                   doi:10.1016/j.jvc.2014.03.001
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                                                                 10.   Wiegel PS, Nolte I, Mach R, Freise F, Bach JP. Reference
nine investigations aimed at describing ECG features                   ranges for standard-echocardiography in Pugs and im-
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investigations as part of the inclusion criteria.15,16,45–49           way syndrome (BOAS) on echocardiographic parameters.
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CT) has been performed, we cannot completely ex-
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