Abstract
The popularity and availability of echocardiography in veterinary practice for companion animals have substantially increased in recent years. The results obtained during the procedure are compared to reference values established for the general dog population or to standards developed for a specific dog breed. The aim of this study was to determine whether individual dog traits, such as body weight, chest structure, and level of physical activity and performance, affect the reference values for echocardiographic parameters. Published reference values for echocardiographic examination parameters for 32 dog breeds were analyzed and the relationship between individual echocardiographic parameters and body weight, chest structure, and level of physical activity and performance was then statistically analyzed. It was found that echocardiographic parameters are affected by the dog’s weight and physical activity. There was no significant relationship between heart size and chest structure. The great variety of dog breeds means that echocardiographic findings should be individually interpreted rather than establishing reference ranges for each breed in population studies. This will allow for a more accurate interpretation of the results obtained in the echocardiographic examination and consequently lead to earlier diagnosis of changes in myocardial morphology.
Résumé
La popularité et la disponibilité de l’échocardiographie dans la pratique vétérinaire pour les animaux de compagnie ont considérablement augmenté ces dernières années. Les résultats obtenus au cours de la procédure sont comparés à des valeurs de référence établies pour la population canine générale ou à des normes développées pour une race de chien spécifique. Le but de cette étude était de déterminer si les caractéristiques individuelles du chien, tels que le poids corporel, la structure de la poitrine et le niveau d’activité physique et de performance, affectent les valeurs de référence des paramètres échocardiographiques. Les valeurs de référence publiées pour les paramètres d’examen échocardiographique pour 32 races de chiens ont été analysées et la relation entre les paramètres échocardiographiques individuels et le poids corporel, la structure thoracique et le niveau d’activité physique et de performance a ensuite été analysée statistiquement. Il a été constaté que les paramètres échocardiographiques sont affectés par le poids et l’activité physique du chien. Il n’y avait pas de relation significative entre la taille du coeur et la structure thoracique. La grande variété des races de chiens signifie que les résultats échocardiographiques devraient être interprétés individuellement plutôt que d’établir des plages de référence pour chaque race dans des études de population. Cela permettra une interprétation plus précise des résultats obtenus à l’examen échocardiographique et conduira par conséquent à un diagnostic plus précoce des modifications de la morphologie myocardique.
(Traduit par Docteur Serge Messier)
Introduction
Echocardiography is a non-invasive imaging method for diagnosing heart disease. It allows the morphology and function of the cardiac muscle and major blood vessels to be assessed. Reference values for echocardiographic examination for the general dog population are available in the form of tables (1–4), echocardiographic calculators (www.beta.vin.com), or as applications for iPhones (Cardio-Calculator by Melastudio Arti Grafiche, www.appadvice.com).
All echocardiographic reference values for dogs have been set based only on the body weight or body surface area (BSA) and do not include other characteristics, such as breed, chest structure, or level of physical activity or performance. Due to the growing popularity and availability of echocardiographic examination in veterinary medicine in recent years, a trend has emerged to set specific reference values for individual breeds. This would increase the accuracy of the examination and allow even small deviations from the normal value to be detected, as well as improve breeding programs for a given breed. To date, reference values for echocardiographic examination have been published for over 37 breeds (5).
The aim of this study was to determine the relationship between the individual dog’s characteristics, such as body weight, chest structure, and level of physical activity and performance, and reference values for echocardiographic parameters.
Materials and methods
Reference values for echocardiographic examination for 32 dog breeds published in the scientific literature were reviewed (Table I). In the available publications, the examined dogs were of different ages and sexes, except for beagles, whose standards were set on a homogeneous female population, aged 21 mo (6). All dogs for which the breed reference values were established were clinically healthy and in good condition, with no acquired or congenital heart disease detected by echocardiography. Chest structure and level of physical activity and performance of individual dog breeds were determined according to the American Kennel Club guidelines (www.akc.org) (Table II). Reference values for 4 breeds (German shepherd, whippet, Irish wolfhound, and Labrador retriever) were described in 2 independent publications, which were also included in the statistics (2,7,13,18,25,26,31,32). Reference values for echocardiographic parameters for Labrador retrievers from Saini’s study have been broken down by range of body weight (7).
Table I.
Sources of reference values for echocardiographic measurements for 32 dog breeds.
| Breed | Age (months) | Number of dogs enrolled in study | Reference |
|---|---|---|---|
| Miniature poodle | 24 to 84 | 20 | (12) |
| Italian greyhound | 18 to 108 | 20 | (18) |
| Dachshund | 9 to 192 | 41 | (19) |
| Indian spitz | 36 to 60 | 24 | (20) |
| English cocker spaniel | — | 12 | (15) |
| Hungarian mudi | 12 to 144 | 28 | (21) |
| Whippet | 10 to 169 | 105 | (22) |
| Whippet | 18 to 84 | 20 | (18) |
| Cavalier King Charles spaniel | 12 to 145.2 | 134 | (11) |
| Corgi (Welsh corgi) | 24 to 84 | 20 | (12) |
| Beagle (females) | 21 | 6 | (6) |
| Border collie | 24 to 144 | 20 | (5) |
| English springer spaniel | 30 to 153.6 | 39 | (23) |
| English pointer | — | 16 | (16) |
| Hungarian greyhound | 12 to 132 | 22 | (21) |
| Hungarian vizsla | 6 to 120 | 45 | (21) |
| Afghan hound | 24 to 84 | 20 | (12) |
| Greyhound | 18 to 84 | 20 | (18) |
| Saluki | 28 to 124 | 75 | (24) |
| Labrador retriever | 16 to 48 | 24 | (25) |
| Labrador retriever | 12 to > 60 | 24 | (7) |
| Labrador retriever | 12 to > 60 | 7 | (7) |
| Golden retriever | 24 to 84 | 20 | (12) |
| German shepherd | 12 to 96 | 50 | (26) |
| German shepherd | 12 to 60 | 60 | (13) |
| Doberman pinscher | 12 to 132 | 39 | (27) |
| Estrela Mountain dog | 18 to 123 | 74 | (28) |
| English bull terrier | 9 to 30 | 14 | (14) |
| Alaskan malamute | 24 to 108 | 77 | (17) |
| English bulldog | — | 18 | (29) |
| Boxer | 25.2 to 132 | 81 | (30) |
| Irish wolfhound | 12 to 108 | 20 | (31) |
| Irish wolfhound | 12 to 102 | 262 | (32) |
| Great Dane | 12 to 72 | 15 | (31) |
| Spanish mastiff | 24 to 48 | 12 | (33) |
| Bordeaux dog | 12 to 84 | 31 | (34) |
| Newfoundland | 12 to 132 | 27 | (31) |
Table II.
Chest structure and level of physical activity and performance of individual dog breeds.
| Breed | Chest structure | Physical activity | Performance |
|---|---|---|---|
| Miniature poodle | Deep | Moderate | Hunting |
| Italian greyhound | Deep | Vigorous | Racing |
| Dachshund | Deep | Moderate | Hunting |
| Indian spitz | Deep | Light | Companion |
| English cocker spaniel | Deep | Moderate | Hunting |
| Hungarian mudi | Deep | Moderate | Shepherd |
| Whippet | Deep | Vigorous | Racing |
| Cavalier King Charles spaniel | Barrel | Light | Companion |
| Corgi (Welsh corgi) | Barrel | Moderate | Shepherd |
| Beagle | Barrel | Moderate | Hunting |
| Border collie | Deep | Shepherd | |
| English springer spaniel | Deep | Moderate | Hunting |
| English pointer | Deep | Moderate | Hunting |
| Hungarian greyhound | Deep | Vigorous | Racing |
| Hungarian vizsla | Deep | Moderate | Hunting |
| Afghan hound | Deep | Moderate | Shepherd |
| Greyhound | Deep | Vigorous | Racing |
| Saluki | Deep | Vigorous | Racing |
| Labrador retriever | Deep | Moderate | Water |
| Golden retriever | Deep | Moderate | Water |
| German shepherd | Deep | Moderate | Shepherd |
| Doberman pinscher | Deep | Moderate | Defensive |
| Estrela Mountain dog | Deep | Moderate | Shepherd |
| English bull terrier | Barrel | Moderate | Defensive |
| Alaskan malamute | Barrel | Vigorous | Draft |
| English bulldog | Barrel | Light | Companion |
| Boxer | Barrel | Moderate | Defensive |
| Irish wolfhound | Deep | Moderate | Hunting |
| Great Dane | Deep | Moderate | Defensive |
| Spanish mastiff | Barrel | Moderate | Defensive |
| Bordeaux dog | Barrel | Moderate | Defensive |
| Newfoundland | Barrel | Moderate | Water |
Echocardiographic parameters were divided into primary and secondary measurements. Primary measurements were left ventricular dimension in diastole (LVDd), left ventricular dimension in systole (LVDs), interventricular septum in diastole (IVSd), interventricular septum in systole (IVSs), left ventricular free wall in diastole (LVWd), left ventricular free wall in systole (LVWs), left atrial dimension (LA), and aortic root diameter (Ao).
Secondary echocardiographic measures were fractional shortening (FS%) and left atrium-to-aorta ratio (LA:Ao). Fractional shortening (FS%) is an echocardiographic parameter calculated using the following formula:
LA:Ao was calculated using the following formula:
We were not able to determine the impact of level of performance on echocardiographic parameters as echocardiographic values for too few existing dog breeds have been examined and published. Thirty-two dog breeds included in the analysis were assigned to 7 types of performance, which meant that the groups obtained were too small for conducting the analysis (Table II).
Statistical analysis
The analysis was based on the mean or median values of echocardiographic measurements and body weight published in scientific articles. In several articles in which only ranges were presented, the average of the minimum and maximum was included in the analysis. Normality of distribution of numerical variables was verified using the Shapiro-Wilk W-test and body weight (BW), the only non-normally distributed variable, was logarithmically transformed (natural logarithm). The relationship between echocardiographic measurements and BW was analyzed using Pearson’s linear correlation coefficient (r) and reported with its 95% confidence interval (CI), and the coefficient of determination (R2), which indicates the part of variance of the echocardiographic measurement that could be explained by the correlation with BW. Based on the Pearson’s coefficient, correlations were classified as very high when absolute value of r ≥ 0.9 to 1.0, high when r ≥ 0.7 to 0.9, moderate when r ≥ 0.5 to 0.7, low when r ≥ 0.3 to 0.5, and negligible when r = 0.0 to 0.3 (8).
As BW proved significantly linked to almost all echocardiographic measurements, it was included as a covariate in the further analyses of the relationship between echocardiographic measurements and categorical characteristics of dog breeds. These analyses were carried out first with the use of the multivariate analysis of covariance (MANCOVA) and then, if it proved significant, with the univariate analysis of covariance (ANCOVA) with the Bonferroni post-hoc test. All tests were 2-sided. A significance level (α) was set at 0.05. Statistical analysis was conducted in TIBCO Statistica 13.3.0 (TIBCO Statistics, Palo Alto, California, USA).
Results
Impact of body weight on echocardiographic measurements
All primary measurements revealed a significant high positive linear correlation with the logarithm of body weight (Table III). Fractional shortening (FS%) showed a significant moderate negative linear correlation with the logarithm of body weight (Figure 1). There was no significant correlation between LA:Ao and the dog’s body weight (P = 0.759) (Figure 2; Table III).
Table III.
Relationship between echocardiographic measurements and dog’s body weight.
| Echocardiographic measurement | n | Pearson’s linear correlation coefficient (r) with 95% CI | P-value | R2 |
|---|---|---|---|---|
| LVDd | 37 | 0.87 (0.76, 0.93) | < 0.001 | 75% |
| LVDs | 33 | 0.79 (0.62, 0.89) | < 0.001 | 63% |
| IVSd | 37 | 0.75 (0.56, 0.86) | < 0.001 | 57% |
| IVSs | 33 | 0.72 (0.50, 0.85) | < 0.001 | 52% |
| LVWd | 37 | 0.69 (0.47, 0.83) | < 0.001 | 47% |
| LVWs | 33 | 0.76 (0.56, 0.88) | < 0.001 | 58% |
| LA | 36 | 0.81 (0.66, 0.90) | < 0.001 | 65% |
| Ao | 36 | 0.89 (0.79, 0.94) | < 0.001 | 79% |
| FS% | 37 | −0.52 (−0.72, −0.24) | 0.001 | 27% |
| LA:Ao | 36 | −0.05 (−0.37, 0.28) | 0.759 | — |
R2 — coefficient of determination; LVDd — left ventricular dimension in diastole; LVDs — left ventricular dimension in systole; IVSd — interventricular septum in diastole; IVSs — interventricular septum in systole; LVWd — left ventricular free wall in diastole; LVWs — left ventricular free wall in systole; LA — left atrial dimension; Ao — aortic root diameter; FS% — fractional shortening; LA:Ao — left atrium-to-aorta ratio.
Figure 1.
A scatter plot of the correlation between the fractional shortening (FS%) and the natural logarithm of body weight.
Figure 2.
A scatter plot of the correlation between the left atrium-to-aorta ratio (LA:Ao) and the natural logarithm of body weight.
Impact of chest structure on echocardiographic measurements
No significant relationship was found between echocardiographic measurements and chest conformation (P = 0.727).
Impact of physical activity on echocardiographic measurements
Multivariate analysis, including body weight as a covariate, showed that there was a significant relationship between level of physical activity of the dog breed and one of the echocardiographic measurements (P = 0.041). One-dimensional analysis showed that such a relationship existed for fractional shortening (FS%). Controlling for body weight, FS% was significantly linked to physical activity (P = 0.002). In dogs with high activity, FS% was significantly lower than in dogs with low (P = 0.008) and moderate (P = 0.047) activity (Figure 3).
Figure 3.
Relationship between the mean fractional shortening (FS%) (with 95% CI) and the physical activity of the dog breed adjusted by the natural logarithm of body weight.
Discussion
It is important to establish echocardiographic values for individual dog breeds, not only for primary measurements such as left ventricular dimension or left atrial dimension, but also for secondary measurements. Even though FS and LA:Ao are secondary echocardiographic measurements, they play an important role in diagnosing numerous heart diseases in dogs. Fractional shortening (FS%) is a parameter based on which left ventricular systolic function is assessed. Its measurement is used to diagnose and monitor the course of dilated cardiomyopathy (DCM), which occurs, among other criteria, with left ventricular systolic dysfunction (1). The LA:Ao parameter is used, among other criteria, in patients diagnosed with mitral valve disease (MVD). It is one of the criteria used to assign patients to individual stages of the disease. According to the guidelines of the American College of Veterinary Internal Medicine, MVD has 4 stages: A, B, C, and D, and its treatment should be started when the heart cavities have become enlarged (stage B2). Thanks to the LA/Ao calculation, among others, it is possible to recognize whether the patient has an enlarged left atrium, classify them to stage B2 of the disease, and start treatment to delay its progression (9).
Many publications to date have clearly stated that the size of the heart cavity depends primarily on body weight (1–4,7). However, it seems that this parameter may not be the only significant indicator affecting echocardiographic reference values. The published reference values are based on healthy dogs, usually with normal body weight. Over the past years, obesity has become a major medical problem in pets. There is a growing tendency for pathological weight gain in dogs, which seems to reflect the scale of the problem in humans (10). Dogs whose body weight deviates significantly from the permissible weight standards are often brought to the cardiology practice. These situations may be associated with obesity, but can also be associated with cachexia, which can be cardiac or resulting from comorbidities, such as cancer. After echocardiographic examination and measurements, it is not clear whether obtained results should be compared to the reference values set according to the patient’s current, too high or low body weight, or to their ideal body weight. As this issue has not been clarified, more research is needed to answer this question and determine whether echocardiographic parameters in obese dogs can be compared to the norms for their breed.
In this study, the body condition was not analyzed because authors of the publications reviewed stated that the population of dogs studied was in normal condition.
Contrary to the conclusion in publications outlining echocardiographic standards for individual breeds that the traits of dogs affect echocardiographic parameters (11–14), the analysis conducted by the authors of the present study demonstrated that chest structure, one of these characteristics, does not affect heart size. In addition, dogs do not always participate in activities typical of their breed, e.g., it cannot be assumed that each of the tested sighthounds, which is a sporting breed, was subjected to intense training. The analysis should therefore be repeated in the future when most dog breeds will undergo cardiology tests.
There are many studies on the significant effects of physical activity on cardiac morphology (12,15–17). Intense physical effort has been shown to result in weight gain and so-called “athlete’s heart” in working and athletic dogs, including border collies, Alaskan malamutes, and whippets and other sighthounds. Vigorous physical activity leads to cardiac dilation, hypertrophy, or increased vagal nerve tension, which result in a slower heart rate (17). The use of reference values for the general population in dogs subjected to intense physical effort will therefore probably lead to misinterpretation of the obtained echocardiographic examination results and prevent a correct diagnosis.
The analysis in this study was based on various studies carried out on a specific breed of dogs of different sex and age (except for beagles), which is the limitation of this study. Another limitation was the large difference between the minimum and maximum values, which is a common problem in clinical trials conducted on animals due to the differences in size and weight in a given breed.
Due to the wide variety of dog breeds and inhomogeneous research groups, echocardiographic measurements should be established individually for each breed based on a population study. This will allow for a more accurate interpretation of the results obtained in the echocardiographic examination and lead to earlier diagnosis of heart disease.
The analysis in this study confirmed that all primary echocardiographic parameters are dependent on body weight, although other factors that may affect these values, such as chest structure and physical activity, were also noted. These particular correlations were not found in this study, however, and should be confirmed in another study with a research group selected on the basis of chest structure or properly defined physical activity, not just breed. While this study has several limitations, it has shown that many factors should be considered when determining echocardiographic values.
References
- 1.Boon JA. Veterinary Echocardiography. 2nd ed. Oxford, UK: Wiley-Blackwell; 2011. pp. 538–541. [Google Scholar]
- 2.De Madron E, Chetboul V, Bussadori C. Clinical Echocardiography of the Dog and Cat. Missouri: Elsevier; 2016. p. 25. [Google Scholar]
- 3.Tilley LP, Smith FWK, Oyama M, Sleeper M. Manual of Canine and Feline Cardiology. 5th ed. St. Louis, Missouri: Elsevier; 2015. pp. 422–423. [Google Scholar]
- 4.Cornell CC, Kittleson MD, della Torre P, et al. Allometric scaling of M-mode cardiac measurements in normal adult dogs. J Vet Intern Med. 2004;18:311–321. doi: 10.1892/0891-6640(2004)18<311:asomcm>2.0.co;2. [DOI] [PubMed] [Google Scholar]
- 5.Jacobson JH, Boon JA, Bright JM. An echocardiographic study of healthy Border Collies with normal reference ranges for the breed. J Vet Cardiol. 2013;15:123–130. doi: 10.1016/j.jvc.2012.12.005. [DOI] [PubMed] [Google Scholar]
- 6.Diez-Prieto I, García-Rodríguez MB, Ríos-Granja MA, Cano-Rábano MJ, Peña-Penabad M, Pérez-García CC. M-mode echocardiographic changes in growing beagles. J Am Assoc Lab Anim Sci. 2010;49:31–35. [PMC free article] [PubMed] [Google Scholar]
- 7.Saini N, Uppal SK, Randhawa CS. Echocardiographic parameters and indices in healthy Labrador retriever dogs. Israel J Vet Med. 2017;72:28–34. [Google Scholar]
- 8.Mukaka MM. Statistics corner: A guide to appropriate use of correlation coefficient in medical research. Malawi Med J. 2012;24:69–71. [PMC free article] [PubMed] [Google Scholar]
- 9.Boswood A, Häggström J, Gordon SG, et al. Effect of pimobendan in dogs with preclinical myxomatous mitral valve disease and cardiomegaly: The EPIC study — A randomized clinical trial. J Vet Intern Med. 2016;30:1765–1779. doi: 10.1111/jvim.14586. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.German AJ. The growing problem of obesity in dogs and cats. J Nutr. 2006;136:1940–1946. doi: 10.1093/jn/136.7.1940S. [DOI] [PubMed] [Google Scholar]
- 11.Misbach C, Lefebvre HP, Concordet D, et al. Echocardiography and conventional Doppler examination in clinically healthy adult Cavalier King Charles spaniels: Effect of body weight, age, and gender, and establishment of reference intervals. J Vet Cardiol. 2014;16:91–100. doi: 10.1016/j.jvc.2014.03.001. [DOI] [PubMed] [Google Scholar]
- 12.Morrison SA, Moise NS, Scarlett J, Mohammed H, Yeager AE. Effect of breed and body weight on echocardiographic values in four breeds of dogs of differing somatotype. J Vet Intern Med. 1992;6:220–224. doi: 10.1111/j.1939-1676.1992.tb00342.x. [DOI] [PubMed] [Google Scholar]
- 13.Muzzi RA, Muzzi LA, de Araújo RB, Cherem M. Echocardiographic indices in normal German shepherd dogs. J Vet Sci. 2006;7:193–198. doi: 10.4142/jvs.2006.7.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.O’Leary CA, MacKay BM, Taplin RH, Atwell RB. Echocardiographic parameters in 14 healthy English Bull Terriers. Aust Vet J. 2013;81:535–542. doi: 10.1111/j.1751-0813.2003.tb12881.x. [DOI] [PubMed] [Google Scholar]
- 15.Gooding JP, Robinson WF, Mews GC. Echocardiographic assessment of left ventricular dimensions in clinically normal English cocker spaniels. Am J Vet Res. 1986;47:296–300. [PubMed] [Google Scholar]
- 16.Snyder PS, Sato T, Atkins CE. A comparison of echocardiographic indices of the nonracing, healthy greyhound to reference values from other breeds. Vet Radiol Ultrasound. 1995;36:387–392. [Google Scholar]
- 17.Stepien RL, Hinchcliff KW, Constable PD, Olson J. Effect of endurance training on cardiac morphology in Alaskan sled dogs. J Appl Physiol. 1985;85:1368–1375. doi: 10.1152/jappl.1998.85.4.1368. [DOI] [PubMed] [Google Scholar]
- 18.della Torre PK, Kirby AC, Church DB, Malik R. Echocardiographic measurements in greyhounds, whippets and Italian greyhounds — Dogs with a similar conformation but different size. Aust Vet J. 2000;78:49–55. doi: 10.1111/j.1751-0813.2000.tb10361.x. [DOI] [PubMed] [Google Scholar]
- 19.Garncarz M, Parzeniecka-Jaworska M, Czopowic M, Hulanicka M, Jank M, Szaluś-Jordanow O. Reference intervals for transthoracic echocardiographic measurements in adult Dachshunds. Pol J Vet Scien. 2018;21:779–788. doi: 10.24425/pjvs.2018.125991. [DOI] [PubMed] [Google Scholar]
- 20.Bodh D, Hoque M, Saxena AC. Echocardiographic study of healthy Indian Spitz dogs with normal reference ranges for the breed. Vet World. 2019;12:740–747. doi: 10.14202/vetworld.2019.740-747. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Vörös K, Hetyey C, Reiczigel J, Czirok GN. M-mode and two-dimensional echocardiographic reference values for three Hungarian dog breeds: Hungarian Vizsla, Mudi and Hungarian Greyhound. Acta Vet Hung. 2009;57:217–227. doi: 10.1556/AVet.57.2009.2.3. [DOI] [PubMed] [Google Scholar]
- 22.Bavegems V, Duchateau L, Stanislas US, De Rick A. Echocardiographic reference values in whippets. Vet Radiol Ultrasound. 2007;48:230–238. doi: 10.1111/j.1740-8261.2007.00234.x. [DOI] [PubMed] [Google Scholar]
- 23.Dickson D, Shave R, Rishniw M, Harris J, Patteson M. Reference intervals for transthoracic echocardiography in the English springer spaniel: A prospective, longitudinal study. J Small Anim Pract. 2016;57:520–528. doi: 10.1111/jsap.12536. [DOI] [PubMed] [Google Scholar]
- 24.Giraut S, Häggström J, Koskinen LLE, Lohi H, Wiberg M. Breed-specific reference ranges for standard echocardiographic measurements in salukis. J Small Anim Pract. 2019;60:374–378. doi: 10.1111/jsap.12975. [DOI] [PubMed] [Google Scholar]
- 25.Gugjoo MB, Hoque M, Saxena AC, Shamsuz Zama MM, Dey S. Reference values of M-mode echocardiographic parameters and indices in conscious Labrador Retriever dogs. Iran J Vet Res. 2014;15:341–346. [PMC free article] [PubMed] [Google Scholar]
- 26.Kayar A, Gonul R, Or ME, Uysal A. M-mode echocardiographic parameters and indices in the normal German shepherd dog. Vet Radiol Ultrasound. 2006;47:482–486. doi: 10.1111/j.1740-8261.2006.00166.x. [DOI] [PubMed] [Google Scholar]
- 27.Kobal M, Domanjko-Petrič A. Diastolic indices of the left ventricle in normal Doberman Pinschers and retrievers. Slov Vet Res. 2007;44:31–40. [Google Scholar]
- 28.Lobo L, Canada N, Bussadori C, Gomes JL, Carvalheira J. Transthoracic echocardiography in Estrela Mountain dogs: Reference values for the breed. Vet J. 2008;177:250–259. doi: 10.1016/j.tvjl.2007.03.024. [DOI] [PubMed] [Google Scholar]
- 29.Giannico AT, Dittrich G, Brüler BC, Froes TR, Sousa MG. Echocardiographic parameters in English bulldogs: Reference values for the breed. Proc WSAVA. 2016 [Google Scholar]
- 30.Cunningham SM, Rush JE, Freeman LM, Brown DJ, Smith CE. Echocardiographic ratio indices in overtly healthy Boxer dogs screened for heart disease. J Vet Intern Med. 2008;22:924–930. doi: 10.1111/j.1939-1676.2008.0121.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Koch J, Pedersen HD, Jensen AL, Flagstad A. M-mode echocardiographic diagnosis of dilated cardiomyopathy in giant breed dogs. J Vet Med. 1996;43:297–304. doi: 10.1111/j.1439-0442.1996.tb00456.x. [DOI] [PubMed] [Google Scholar]
- 32.Vollmar AC. Echocardiographic measurements in the Irish wolfhound: Reference values for the breed. J Am Anim Hosp Assoc. 1999;35:271–277. doi: 10.5326/15473317-35-4-271. [DOI] [PubMed] [Google Scholar]
- 33.Bayón A, Fernández del Palacio MJ, Montes AM, Gutiérrez Panizo C. M-mode echocardiography study in growing Spanish mastiffs. J Small Anim Pract. 1994;35:473–479. [Google Scholar]
- 34.Locatelli C, Santini A, Bonometti GA, et al. Echocardiographic values in clinically healthy adult dogue de Bordeaux dogs. J Small Anim Pract. 2011;52:246–253. doi: 10.1111/j.1748-5827.2011.01055.x. [DOI] [PubMed] [Google Scholar]



