Introduction
Myxomatous mitral valve disease (MMVD) is the most common heart disease in dogs in many parts of the world.1 Affected dogs may have no clinical signs throughout their lives or may develop severe clinical consequences, including arrhythmias, congestive heart failure (CHF), and pulmonary hypertension.2 The determining factors for this variation in disease progression among dogs are not fully understood. A substantial amount of literature is available describing MMVD in Cavalier King Charles Spaniels, Dachshunds, and Miniature Poodles.3,4,5,6,7 The Miniature Schnauzer and Yorkshire Terrier are breeds that commonly develop MMVD, and both are popular dog breeds in North America.8,9 However, MMVD has not been specifically characterized in these breeds nor have features of the disease in these breeds been compared with findings for other dog breeds.
Miniature Schnauzers and Yorkshire Terriers, although both small in stature, have varied genetic backgrounds. Miniature Schnauzers are genetically more closely related to Standard Schnauzers than to other small-breed dogs.10 Yorkshire Terriers are considered to be one of the most genetically diverse breeds of dogs, with a very low inbreeding coefficient.11 Although the Yorkshire Terrier breed has a diverse genetic background, it is a member of the Mastiff-Terrier phylogenetic group and is closely related to the Cairn Terrier and West Highland White Terrier breeds,12 which are breeds with a lower risk for developing MMVD.13,14 Therefore, features of MMVD in Miniature Schnauzers and Yorkshire Terriers may be dissimilar to each other and to features of MMVD in other small-breed dogs, including Cavalier King Charles Spaniels and Dachshunds.
The objective of the study reported here was to characterize specific features of MMVD in the Miniature Schnauzer and Yorkshire Terrier breeds. We performed a retrospective analysis of the clinical characteristics of MMVD in both breeds using data for dogs evaluated at a tertiary hospital over a 10-year period.
Materials and Methods
Case selection criteria
The medical records of Miniature Schnauzers and Yorkshire Terriers examined at a veterinary teaching hospital and for which a diagnosis of MMVD was made on the basis of echocardiographic findings between January 1, 2007, and December 31, 2016, were reviewed retrospectively. The total number of dogs of each breed that were > 3 years of age and were examined during the same period was also obtained for comparison to help assess the prevalence of disease among age-appropriate dogs. For each dog, only data from the initial examination at which MMVD was diagnosed were considered for analysis.
Because of the retrospective nature of the study, the data were collected directly from the medical records; for some dogs, some data were missing and could not be obtained. Data collected included signalment, age at the time of MMVD diagnosis, medical history with regard to clinical signs potentially referable to heart disease, cardiovascular and physical examination findings, blood pressure measurement, ECG rhythm diagnosis, Holter monitoring data (when available), and thoracic radiographic and echocardiographic findings.
For inclusion of a dog in the study, a diagnosis of mitral valve degeneration (mitral valve thickening, prolapse, or regurgitation) had to have been made by a board-certified veterinary cardiologist or a cardiology resident under the supervision of a board-certified veterinary cardiologist on the basis of echocardiographic examination findings.15 Dogs were excluded from further evaluation if they were not purebred; had echocardiographic evidence of congenital heart disease, cardiomyopathy, neoplasia, or possible endocarditis; or had systolic arterial blood pressure > 160 mm Hg.
Medical records review
Baseline data collected for each dog included sex; age at the time of diagnosis of MMVD; presence or absence of cough, syncope, and exercise intolerance; and previous or current treatment with cardiac medications. Electrocardiographic data were evaluated for presence of pathological arrhythmias. Holter data were evaluated for maximum, minimum, and mean heart rate; arrhythmias; and pauses on a 24-hour recording. Thoracic radiographic data collected included presence or absence of CHF (pulmonary edema or venous congestion) and vertebral heart scale (VHS) scores, as obtained with a standard method16 from right lateral radiographic views. A VHS score of 9.7 was considered normal for Miniature Schnauzers, and a VHS score of 9.9 was considered normal for Yorkshire Terriers.17,18
Echocardiographic data collected included evidence of and subjective scoring of mitral valve regurgitation (mild, moderate, or severe) based on the size of the mitral regurgitation jet, compared with the left atrium, and mitral valve prolapse (none, mild, moderate, or severe) based on degree of protrusion of the leaflets into the left atrium, as noted on a right parasternal, long-axis, 2-D echocardiogram.19 Measurements of dimensions obtained with M-mode echocardiography from the right parasternal short-axis view included those of the left atrium and aorta, left ventricular internal end diastolic diameter (LVIDd), and left ventricular internal end systolic diameter (LVIDs); the latter 2 measurements were also recorded with normalization to body weight, as previously described (ie, left ventricular internal end diastolic diameter normalized to body weight [LVIDdN] and left ventricular internal end systolic diameter normalized to body weight [LVIDsN]).20 Fractional shortening and the left atrium diameter to aortic diameter (LA:Ao) ratio were calculated. Presence or absence of pulmonary hypertension, as determined by Doppler echocardiographic measurement of velocity of the tricuspid valve regurgitation (TVR) jet, was noted. Pulmonary hypertension was assessed for the purposes of the study if the medical record indicated that a TVR21 ≥ 3.0 m/s had been identified. With regard to MMVD classification, a stage from B1 to D was assigned for each dog on the basis of published consensus guidelines for chronic valvular heart disease.22
Statistical analysis
Summary statistics were determined for age at the time of diagnosis, VHS score (values that exceeded the reference limit), echocardiographic data (LVIDd, LVIDs, LVIDdN, and LVIDsN), fractional shortening [FS%], M-mode LA:Ao ratio, and TVR velocity for each breed. By use of the D’Agostino-Pearson normality test, each data set was tested for normality. Data that were normally distributed are reported as means and SDs and ranges, whereas data that were not normally distributed are reported as medians and interquartile (25th to 75th percentile) ranges. Comparison of age at the time of diagnosis between breeds was performed with a Student t test. Statistical analysis of the prevalence of MMVD and CHF and frequencies of mitral valve prolapse, syncope, and cough, abnormally high VHS score, and treatments with cardiac medications between breeds was performed with a Fisher exact test. A value of P < 0.05 was considered significant.
Results
During the 10-year period, 69 of 536 (12.9%) Miniature Schnauzers and 65 of 1,134 (5.7%) Yorkshire Terriers that were > 3 years old and had MMVD met the inclusion criteria. Among the Miniature Schnauzers, there were 1 sexually intact female, 40 spayed females, 1 sexually intact male, and 27 castrated males. Among the Yorkshire Terriers, there were 4 sexually intact females, 22 spayed females, 6 sexually intact males, and 33 castrated males. The mean ± SD age at the time of diagnosis of MMVD for the Miniature Schnauzers and Yorkshire Terriers was 10 ± 2.0 years (range, 4 to 15 years) and 11 ± 3 years (range, 6 to 17 years), respectively.
Miniature Schnauzers
The most common cardiovascular sign among the Miniature Schnauzers was syncope, which was documented for 30 of the 69 (43.5%) dogs. Rhythm assessment (determined from a lead II ECG tracing) was available for 55 dogs. Of those 55 dogs, 38 (69.1%) had sinus rhythm or sinus arrhythmia, 5 (9.1%) had a sinus rhythm with occasional atrial premature complex (APCs), 1 (1.8%) had sinus bradycardia, 1 (1.8%) had sinus arrest, 2 (3.6%) had sinus rhythm and ventricular premature complex (VPCs), and 8 (14.6%) had findings consistent with sick sinus syndrome including periods of sinus arrest, atrioventricular block, and supraventricular tachycardia.
Four of the 8 dogs with sick sinus syndrome underwent Holter monitoring. The mean minimum heart rate was 31 ± 8 beats/min (range, 20 to 39 beats/min), mean heart rate was 60 ± 13 beats/min (range, 46 to 68 beats/min), and mean maximum heart rate was 193 ± 32 beats/min (range, 160 to 225 beats/min). The mean number of pauses of > 3 seconds’ duration was 2,052/24 ± 2,384 hours (range, 6 to 5,016) and the mean maximum pause duration was 8 ± 3 seconds (range, 5 to 13 seconds). The mean number of VPCs was 5,863 ± 9,440 (range, 0 to 19,797 VPCs), mean number of APCs was 17 ± 33 (range, 0 to 60 APCs).
Thoracic radiographic views were available for 57 of the 69 Miniature Schnauzers. The mean VHS score was 12 ± 1 (range, 10 to 14). Fifty-five of the 57 (96.5%) dogs had a VHS score > 9.7. Of the 57 dogs, 42 (73.7%) had evidence of left atrial enlargement and 16 (28.1%) had evidence of left ventricular enlargement. Sixteen (28.1%) dogs had radiographic evidence of CHF.
Echocardiographic left ventricular dimensions were available for 65 of the 69 Miniature Schnauzers. The remaining 4 dogs had subjective echocardiographic information in their medical records, but measurements were absent. Among the 65 dogs for which data were available, mean LVIDd and LVIDs were 3.4 ± 0.6 cm (range, 2.3 to 4.7 cm) and 1.8 ± 0.4 cm (range, 1.1 to 2.7 cm), respectively and mean LVIDdN and LVIDsN were 1.9 cm ± 0.1(range, 1.1 to 2.6) and 0.94 ± 0.1 (range, 0.54 to 1.4), respectively. The mean LA:Ao ratio was 1.7 ± 0.5 (range, 0.8 to 3.0) and mean FS% was 47% ± 8 (range, 26% to 61%). A diagnosis of pulmonary hypertension was made for 16 of the 69 (23.2%) dogs. Eleven of the 16 dogs with pulmonary hypertension had TVR velocity noted in their records, and the median velocity was 3.3 m/s (interquartile range, 3.1 to 3.5 m/s).
Among the 69 Miniature Schnauzers, mitral valve regurgitation was classified as trace for 3 (4.3%) dogs, mild for 11 (15.9%) dogs, moderate for 22 (31.9%) dogs, and severe for 29 (42.0%) dogs. Severity of mitral valve regurgitation was not noted for 4 (6%) dogs. Forty-one of the 69 (59.4%) dogs had mitral valve prolapse; the subjective severity of mitral valve prolapse was noted for 37 dogs, and was graded as mild for 12 dogs, moderate for 18 dogs, and severe for 7 dogs.
For the 30 dogs that were presented because of syncope, the mechanism of the syncope was considered multifactorial or was undetermined. Many of these dogs, in addition to their mitral valve disease, had other cardiovascular issues that could have contributed to the development of syncope including sick sinus syndrome (n = 8), pulmonary hypertension (9), or arrhythmias (APCs [2] and VPCs [1]). Left-sided CHF was evident in 8 of the syncopal Miniature Schnauzers.
With regard to MMVD classification among the 69 Miniature Schnauzers, 22 (31.9%) were classified as stage B1, 21 (30.4%) were classified as stage B2, and 25 (36.2%) were classified as stage C. None of the Miniature Schnauzers had a classification of stage D. At the time of diagnosis of MMVD, 30 of the 69 (43.5%) dogs were being treated or had been previously administered cardiac medications. Among the treated dogs, the most common medications administered were angiotensin-converting enzyme inhibitors (enalapril or benazepril; 30 [100%] dogs), diuretics (furosemide; 17 [56.7%] dogs), and inodilators (pimobendan; 14 [46.7%] dogs). Three dogs were prescribed medical treatment for sick sinus syndrome including theophylline (n = 2) and propantheline (1). Four dogs with sick sinus syndrome were treated with pacemaker implantation.
Yorkshire Terriers
The most common cardiovascular sign among Yorkshire Terriers was coughing, which was documented for 41 of the 65 (63.1%) dogs. Rhythm assessment (determined from a lead II ECG tracing) was available for 46 dogs, of which 45 (97.8%) had sinus rhythm or sinus arrhythmia. One of the 65 (1.5%) dogs had third-degree atrioventricular block. Electrocardiograms were not available for 19 (29%) dogs. None of the Yorkshire Terriers had Holter data available for review.
Thoracic radiographic views were available for 53 of the 65 Yorkshire Terriers. The mean VHS score was 11 ± 1 (range, 9.2 to 14). Fifty of the 53 (94.3%) dogs had a VHS score > 9.9. Of the 53 dogs, 36 (67.9%) had evidence of left atrial enlargement and 11 (20.8%) had evidence of left ventricular enlargement. Ten of 53 (18.9%) dogs had radiographic evidence of CHF.
Echocardiographic left ventricular dimensions were available for 61 of the 65 Yorkshire Terriers. Among the 61 dogs for which data were available, mean LVIDd and LVIDs were 2.5 ± 0.8 cm (range, 0.7 to 4.4 cm) and 1.2 cm ± 0.4 (range, 0.5 to 2.4 cm), respectively and mean LVIDdN and LVIDsN were 1.7 cm ±0.2 (range, 0.49 to 2.9) and 0.78 ± 0.1(range, 0.39 to 1.4), respectively. Median LA:Ao ratio was 1.6 (interquartile range, 1.0 to 3.8). The mean FS% was 52% ± 9 (range, 27% to 77%). A diagnosis of pulmonary hypertension was made for 13 of the 65 (20.0%) dogs. Seven of the 13 dogs with pulmonary hypertension had TVR velocity noted in their records, and the mean velocity was 4.2 ± 0.7 m/s (range, 3.3 to 4.9 m/s).
Among the 65 Yorkshire Terriers, mitral valve regurgitation was classified as mild for 24 (36.9%) dogs, moderate for 14 (21.5%) dogs, and severe for 18 (27.7%) dogs; no mitral valve regurgitation was noted for 9 (13.8%) dogs. Seventeen of the 65 (26.2%) dogs had mitral valve prolapse; the subjective severity of mitral valve prolapse was noted for all 17 dogs, and was graded as mild for 6 dogs, moderate for 6 dogs, and severe for 5 dogs.
Twelve Yorkshire Terriers had a history of syncope; however, Holter monitor recordings were not available for any of those dogs. On the basis of ECG data for 7 dogs, 5 had a sinus rhythm and 2 had sinus arrhythmia; ECG recordings were not available for 5 dogs with syncope. One dog with third-degree AV block was not known to be syncopal.
With regard to MMVD classification among the 65 Yorkshire Terriers, 21 (32.3%) were classified as stage B1, 27 (41.5%) were classified as stage B2, 15 (23.1%) were classified as stage C, and 2 (3.1%) were classified as stage D. At the time of diagnosis of MMVD, 49 of the 65 (75%) dogs were being treated or had been previously administered cardiac medications. Among the treated dogs, the most common medications were angiotensin-converting enzyme inhibitors (enalapril; 41 [83.7%] dogs), diuretics (furosemide; 20 [40.8%] dogs), and inodilators (pimobendan; 24 [49%] dogs).
Interbreed comparisons
Compared with findings for Yorkshire Terriers, the prevalence of MMVD was significantly (P < 0.001) higher and the disease was diagnosed at a significantly (P = 0.002) younger age in Miniature Schnauzers. The frequencies of mitral valve prolapse (P < 0.001) and syncope (P = 0.003) were significantly greater among Miniature Schnauzers, compared with Yorkshire Terriers. The frequencies of abnormally high VHS scores (P = 0.67) and radiographic evidence of CHF (P = 0.39) did not differ between the 2 breeds. Among Yorkshire Terriers, the number of dogs that had coughing as a presenting clinical sign (P = 0.006) and the number of dogs that had previously been treated or were receiving cardiac medications at the time of presentation (P < 0.001) were significantly greater, compared with findings for Miniature Schnauzers.
Discussion
On the basis of the medical record data examined in the present study, the prevalence of MMVD among Miniature Schnauzers (relative to the general hospital population of canine patients) was significantly higher than that among Yorkshire Terriers. Although this finding could indicate that the disease is more common in Miniature Schnauzers, the total number of Miniature Schnauzers presented to the tertiary hospital in this study was lower (536 dogs) than the number of Yorkshire Terriers (1,134 dogs) presented in the same period, which could have biased the results. The disparate numbers of dogs could have reflected the popularity of Yorkshire Terriers locally or more frequent referral of dogs of this breed to our institution for assessment of noncardiac conditions, thereby facilitating ancillary cardiac evaluation.
Results of the present study indicated that some features of MMVD in Miniature Schnauzers and Yorkshire Terriers were demonstrably similar to features of MMVD in other breeds, although some differences were also apparent. In the present study, the Miniature Schnauzers were significantly younger at the time of MMVD diagnosis than were the Yorkshire Terriers; however, the mean ages of both groups were comparable to the ages of other dog breeds at the time of MMVD diagnosis.23,24,25
The presenting clinical signs were different for Miniature Schnauzers and Yorkshire Terriers. Among the Miniature Schnauzers, syncope was the most common clinical sign reported (30/69 dogs) and was significantly more common for this breed than for Yorkshire Terriers. Syncope as the most common presenting sign differs from what has been reported for some other breeds of dog with MMVD.26,27,28 Syncope may have been associated with sick sinus syndrome, which is a disease that commonly affects Miniature Schnauzers; in the present study 8 Miniature Schnauzers had sick sinus syndrome. The actual association of syncope with sick sinus syndrome may have been underestimated in the present study because many of the syncopal dogs did not undergo Holter monitoring. Coughing was the most common clinical sign among Yorkshire Terriers in the present study, with 41 dogs presenting with a cough. Ten of those dogs had evidence of CHF and 36 dogs had left atrial enlargement with or without CHF; both CHF and left atrial enlargement are possible causes of coughing in dogs.29 Coughing could have also been associated with concurrent respiratory disease because tracheal collapse is a common cause of cough and dyspnea in dogs and is frequently detected in Yorkshire Terriers.30,31 Approximately 75% of the 65 Yorkshire Terriers in the present study had been treated previously or were being treated with cardiac medications at the time of presentation, which was significantly greater than the percentage of treated Miniature Schnauzers; this finding may have been a reflection of attempted cough management in the Yorkshire Terriers.
Another discernable difference in the features of MMVD in these 2 dog breeds was the presence of mitral valve prolapse, which was detected more frequently in Miniature Schnauzers. The pathophysiologic reason for this interbreed difference in the prevalence of mitral valve prolapse remains unknown.
As with many retrospective studies, the present study had limitations. The data collected were obtained for dogs with MMVD that were evaluated at a tertiary hospital. Therefore, the number of dogs evaluated during the 10-year period likely represented only a small portion of the overall population of Miniature Schnauzers and Yorkshire Terriers with MMVD and may have been influenced by factors such as concurrent diseases, referral biases, and owners’ finances. Echocardiographic measurements were not consistently performed by 1 individual, creating potential biases among those data. Clinical data were missing for some dogs and long-term follow-up information was not obtained. Additionally, a well-defined reference limit for the VHS score for Miniature Schnauzers has not been fully characterized, which could have impacted the interpretation of radiographic cardiac enlargement. Finally, some dogs from both breeds were syncopal, but the cause of the syncope was not clearly identified for many of the dogs. Regardless, the data obtained in the present study have provided some understanding of the features of MMVD in Miniature Schnauzers and the Yorkshire Terriers. Future work should include prospective studies to provide additional insight into the natural progression of MMVD in these 2 breeds.
Acknowledgments
This study was funded by the Mark L. Morris Jr. Investigator Award, D16CA509, Morris Animal Foundation and the American Kennel Club Canine Health Foundation.
None of the authors has any financial or personal relationships that could inappropriately influence or bias the content of the paper.
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