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- 688 JAVMA | MAY 2023 | VOL 261 | NO. 5 Unauthenticated | Downloaded 01/16/24 01:21 AM UTC
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 JAVMA | MAY 2023 | VOL 261 | NO. 5 689 Unauthenticated | Downloaded 01/16/24 01:21 AM UTC
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- 692 JAVMA | MAY 2023 | VOL 261 | NO. 5 Unauthenticated | Downloaded 01/16/24 01:21 AM UTC
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 JAVMA | MAY 2023 | VOL 261 | NO. 5 693 Unauthenticated | Downloaded 01/16/24 01:21 AM UTC
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. of thoracic fat can increase the distance between the 2021;52(4):409–421. doi:10.1111/age.13082 7. Holdt SL, Peckens NK, Rosenthal S, Cober R. Arrhythmo- heart and electrodes and can change the position of genic right ventricular cardiomyopathy in Bulldogs: eval- the heart in the thorax (which, in turn, can potentially uation of clinical and histopathologic features, progres- alter some ECG variables). Third, the enrolled dogs sion, and outcome in 71 dogs (2004–2016). J Vet Cardiol. 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 could have occurred at the time of the ECG analysis. of body weight, age, and gender, and establishment of 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 variables, especially the QRS-MEA, would have been 9. Vurucu M, Ekinci G, Gunes V. An echocardiographic study present in light of the good clinical condition of the of breed-specific reference ranges in healthy French dogs and their unremarkable anamnesis. Moreover, it Bulldogs. Vet Radiol Ultrasound. 2021;62(5):573–582. doi:10.1111/vru.12997 is important to note that the majority of previous ca- 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- of apparently healthy dogs did not include laboratory pact of clinical severity of brachycephalic obstructive air- investigations as part of the inclusion criteria.15,16,45–49 way syndrome (BOAS) on echocardiographic parameters. Finally, since no advanced test aimed at providing fur- BMC Vet Res. 2022;18(1):282. doi:10.1186/s12917-022- ther information on ventricular anatomy (eg, cardiac 03348-8 11. Romito G, Castagna P, Sabetti MC, Cipone M. Physiologi- CT) has been performed, we cannot completely ex- cal shift of the ventricular mean electrical axis in healthy clude that, in some Pugs or EBs, the left-axis devia- French Bulldogs: a retrospective electrocardiographic tion was the result of a myocardial abnormality un- analysis of 80 healthy dogs. 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