Accuracy of radiographic vertebral heart score and sphericity index in the detection of pericardial effusion in dogs

Carlo Guglielmini Department of Veterinary Clinical Sciences, University of Teramo, 64100 Teramo, Italy.

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Alessia Diana Department of Veterinary Medical Sciences, Alma Mater Studiorum, University of Bologna, 40064 Ozzano Emilia, Italy.

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Giorgia Santarelli Department of Veterinary Medical Sciences, Alma Mater Studiorum, University of Bologna, 40064 Ozzano Emilia, Italy.

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Alessandra Torbidone Department of Veterinary Clinical Sciences, University of Teramo, 64100 Teramo, Italy.

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Morena Di Tommaso Department of Veterinary Clinical Sciences, University of Teramo, 64100 Teramo, Italy.

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Marco Baron Toaldo Department of Veterinary Medical Sciences, Alma Mater Studiorum, University of Bologna, 40064 Ozzano Emilia, Italy.

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Mario Cipone Department of Veterinary Medical Sciences, Alma Mater Studiorum, University of Bologna, 40064 Ozzano Emilia, Italy.

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Abstract

Objective—To evaluate the diagnostic accuracy of radiographically derived measurements of vertebral heart score (VHS) and sphericity index (SI) in the detection of pericardial effusion (PE) in dogs.

Design—Retrospective case-control study.

Animals—51 dogs with PE associated with various cardiac disorders, 50 dogs with left- or right-sided cardiac disorders without PE, 50 dogs with bilateral cardiac disorders without PE, and 50 healthy dogs.

Procedures—Measurements of VHS on lateral (lateral VHS) and ventrodorsal (ventrodorsal VHS) radiographs, SI on lateral (lateral SI) and ventrodorsal (ventrodorsal SI) radiographs, and global SI (mean of lateral SI and ventrodorsal SI) were obtained. Receiver operating characteristic curves were calculated to evaluate the diagnostic accuracy of the radiographic indexes at differentiating dogs with PE from those with other cardiac disorders without PE.

Results—Measurements of lateral and ventrodorsal VHS were significantly higher in dogs with PE, compared with values for all dogs without PE. Measurements of lateral, ventrodorsal, and global SI were significantly lower in dogs with PE, compared with values for all dogs without PE. Cutoff values of > 11.9, > 12.3, and ≤ 1.17 for lateral VHS, ventrodorsal VHS, and global SI, respectively, were the most accurate radiographic indexes for identifying dogs with PE.

Conclusions and Clinical Relevance—Cardiac silhouettes of dogs with PE were larger and more rounded, compared with those of dogs with other cardiac disorders without PE. Objective radiographic indexes of cardiac size and roundness were only moderately accurate at distinguishing dogs with PE from dogs with other cardiac disorders without PE.

Abstract

Objective—To evaluate the diagnostic accuracy of radiographically derived measurements of vertebral heart score (VHS) and sphericity index (SI) in the detection of pericardial effusion (PE) in dogs.

Design—Retrospective case-control study.

Animals—51 dogs with PE associated with various cardiac disorders, 50 dogs with left- or right-sided cardiac disorders without PE, 50 dogs with bilateral cardiac disorders without PE, and 50 healthy dogs.

Procedures—Measurements of VHS on lateral (lateral VHS) and ventrodorsal (ventrodorsal VHS) radiographs, SI on lateral (lateral SI) and ventrodorsal (ventrodorsal SI) radiographs, and global SI (mean of lateral SI and ventrodorsal SI) were obtained. Receiver operating characteristic curves were calculated to evaluate the diagnostic accuracy of the radiographic indexes at differentiating dogs with PE from those with other cardiac disorders without PE.

Results—Measurements of lateral and ventrodorsal VHS were significantly higher in dogs with PE, compared with values for all dogs without PE. Measurements of lateral, ventrodorsal, and global SI were significantly lower in dogs with PE, compared with values for all dogs without PE. Cutoff values of > 11.9, > 12.3, and ≤ 1.17 for lateral VHS, ventrodorsal VHS, and global SI, respectively, were the most accurate radiographic indexes for identifying dogs with PE.

Conclusions and Clinical Relevance—Cardiac silhouettes of dogs with PE were larger and more rounded, compared with those of dogs with other cardiac disorders without PE. Objective radiographic indexes of cardiac size and roundness were only moderately accurate at distinguishing dogs with PE from dogs with other cardiac disorders without PE.

Pericardial effusion is defined as abnormal accumulation of fluid within the pericardial space and is the most frequent pericardial disorder in dogs.1–3 Small amounts of pericardial fluid are often clinically irrelevant, but large amounts of fluid or a rapid increase in pericardial pressure can lead to cardiac tamponade and heart failure, resulting in a life-threatening clinical condition.1–3 The most commonly reported cause of PE in dogs and subsequent cardiac tamponade is intrapericardial neoplasia, with hemangiosarcoma and heart base tumors accounting for most cases.1–8 The most frequent nonneoplastic disorder associated with PE and cardiac tamponade in dogs is IPE.1–8 Other reported causes of PE include right-sided congestive heart failure, left atrial rupture secondary to CDVD, toxicosis, and infections.1–11

Radiographically, PE can alter the shape and size of the cardiac silhouette. Commonly, PE manifests radiographically as a generalized enlargement of the cardiac silhouette in both the lateral and ventrodorsal or dorsoventral views of the thorax, although radiographic findings can be normal or only mildly abnormal in some cases.2–4,6–8,12,13 The degree of cardiomegaly observed in thoracic radiographs depends on both the amount of fluid accumulated within the pericardial space and the rate of fluid accumulation. Pronounced effusion can lead to dramatic enlargement of the cardiac silhouette, resulting in a globoid or rounded shape.2–4,6–8,12,13 However, other conditions, such as DCM and tricuspid dysplasia, may produce similar radiographs when cardiomegaly is severe.2 Furthermore, dogs that develop PE secondary to either CDVD or DCM may have generalized cardiomegaly that may not be identified as PE induced.4 Pleural effusion, enlarged caudal vena cava, hepatomegaly, or ascites have also been associated with cases of cardiac tamponade and right-sided heart failure.2,3,12,13 Furthermore, nodular or interstitial pulmonary parenchymal changes have been observed in dogs with metastatic disease.2,3,12 However, the radiographic findings are not specific for dogs with PE. Echocardiography is the imaging modality of choice in the diagnosis of PE, and even small amounts of fluid are appreciable via diagnostic ultrasonography.2–12 In addition, echocardiography is essential for the identification and localization of intrapericardial masses, the detection of structural or functional cardiac disease associated with PE, and the assessment of the severity of the effusion.2–12

To the best of our knowledge, systematic studies aimed at establishing the diagnostic value of thoracic radiography when identifying dogs with PE are lacking. Therefore, the aim of the study reported here was to estimate the diagnostic accuracy of survey thoracic radiography in the diagnosis of PE in dogs. For this purpose, quantitative parameters, such as VHS and SI, were used as objective measurements of cardiac silhouette enlargement and roundness, respectively.

Materials and Methods

Criteria for case selection—Medical records of dogs with PE at the cardiology service of the Veterinary Teaching Hospital at the University of Teramo and Bologna from January 2000 through December 2009 were retrospectively reviewed. Diagnoses of PE and the underlying diseases causing the PE were determined on the basis of combined clinical, radiographic, echocardiographic, and Doppler echocardiographic findings. During the same study period, 3 groups, each consisting of 50 dogs, were selected: dogs with UCD (left- or right-sided cardiac disorders) and without PE, dogs with BCD (cardiac disorders involving both sides of the heart) and without PE, and healthy dogs without clinical and echocardiographic evidence of cardiac disorders. Dogs assigned to the UCD, BCD, or PE group were required to have a definitive diagnosis by echocardiography within 24 hours after thoracic radiographic examination. Transthoracic echocardiography was always performed by the same experienced operator (CG or MC) at the 2 centers. Echocardiography was also used to classify PE severity via a method described for humans14 that was modified to consider differences in canine body weight and cardiac size. Briefly, with the right parasternal window, the sum of the anterior and posterior echo-free space between the epicardium and pericardium was measured on 2-D echocardiography. Mild PE was defined as when this sum was ≤ 8 and ≤ 10 mm in dogs weighing ≤ 20 and ≥ 21 kg (≤ 44 and ≥ 46.2 lb), respectively; moderate PE was defined as when the sum of the echo-free distance between the epicardium and pericardium was 9 to 25 mm and 11 to 30 mm in dogs weighing ≤ 20 and ≥ 21 kg, respectively; severe PE was defined as when the sum of the echo-free distance between the epicardium and pericardium was ≥ 26 and ≥ 31 mm in dogs weighing ≤ 20 and ≥ 21 kg, respectively.

Only dogs with 2 orthogonal radiographic images of the thorax were included in this study. Exclusion criteria included incorrect positioning of the patient for thoracic radiography or the radiographic observation of pleural effusion or a mediastinal mass obscuring the cardiac silhouette such that accurate cardiac measurement could not be performed.

Procedures—Blinded evaluations of right lateral and ventrodorsal radiographic views of the thorax were performed by the same investigator (AD) who was unaware of the echocardiographic findings. The cardiac dimensions were assessed by measuring VHS, as described.15 Briefly, cardiac long and short axes were measured on both thoracic views and were then compared with the length of the vertebral bodies of thoracic vertebrae in the lateral view. In particular, in the right lateral view, the cardiac long axis was measured from the ventral border of the largest of the main stem bronchi seen in cross section to the most distant point of the cardiac apex; the cardiac short axis was measured perpendicular to the measurement of the long axis at the point of maximum cardiac width. In the ventrodorsal view, the maximal long and short axes of the heart were determined in a similar fashion. The VHS measured on lateral radiographs (lateral VHS) and the VHS measured on ventrodorsal radiographs (ventrodorsal VHS) are the vertebral scale sum of the long and short axes and were obtained from right lateral and ventrodorsal radiographic views, respectively, and measured caudally from the cranial edge of the fourth thoracic vertebra.

Cardiac roundness was evaluated by calculating the SI as follows: the ratio between the maximal long axis and the maximal short axis of the cardiac silhouette, measured via the VHS system, was determined from the lateral and ventrodorsal radiographic views of the thorax to obtain the lateral SI and ventrodorsal SI, respectively. The mean of the lateral and ventrodorsal SI values represents the global SI.

Statistical analysis—A Kolmogorov-Smirnov test was applied to test for normal distribution of the data. The 1-way ANOVA was used to analyze normally distributed continuous data, followed by the Tukey post-test for multiple comparisons.

The ability of each radiographic index (lateral VHS, ventrodorsal VHS, lateral SI, ventrodorsal SI, and global SI) to distinguish between dogs with PE and those with other cardiac disorders without PE (ie, dogs with UCD and BCD) was evaluated by receiver operating characteristic curve analysis. The same analysis was performed for the 3 subgroups of dogs with PE (ie, dogs with mild, moderate, and severe PE). In particular, the sensitivity, specificity, positive likelihood ratio, and negative likelihood ratio were calculated at various cutoffs. The value of the AUC as a criterion of the accuracy of the tested indexes was considered as follows: low, 0.5 to 0.7; moderate, 0.7 to 0.9; and high, > 0.9.16

All analyses were performed with statistical software packages.a,b Values of P < 0.05 were considered significant.

Results

Of 65 dogs with PE during the study period, 51 dogs met the inclusion criteria. All 51 dogs had a right lateral radiographic view of the thorax available; 30 of 51 dogs had a ventrodorsal and 21 had a dorsoventral radiographic view of the thorax available. The signalment of each patient group and the cardiac diagnosis for dogs with PE, UCD, and BCD were summarized (Table 1).

Table 1—

Signalment and cardiac disorders in 50 healthy dogs (control), 51 dogs with PE, 50 dogs with a UCD without PE, and 50 dogs with a BCD without PE.

GroupAge (y)Body weight (kg)Sex*Cardiac disorder*
SIFSFSIMNMDCMIPEIPNMRMR, TRMR, TR, IPNPSSASTR
Healthy7.2 ± 4.221.5 ± 10.9302171NANANANANANANANANA
PE9.9 ± 3.024.5 ± 14.7763711 (2.0)11 (21.6)16 (31.4)4 (7.8)17 (33.3)2 (3.9)0 (0)0 (0)0 (0)
UCD7.2 ± 4.517.5 ± 13.71372910 (0)0 (0)0 (0)28 (56)0 (0)0 (0)6 (12)10 (20)6 (12)
BCD10.0 ± 3.117.0 ± 15.61233327 (14)0 (0)0 (0)0 (0)43 (86)0 (0)0 (0)0 (0)0 (0)

Number of dogs (percentage).

Mean ± SD.

IPN = Intrapericardial neoplasia. MR = Mitral valve regurgitation. NA = Not applicable. NM = Neutered male. PS = Pulmonic stenosis. SAS = Subaortic stenosis. SF = Spayed female. SIF = Sexually intact female. SIM = Sexually intact male. TR = Tricuspid valve regurgitation.

Dogs with PE were significantly older, compared with healthy dogs (P = 0.001) and dogs with UCD (P < 0.001), and had a significantly higher body weight, compared with dogs with UCD (P = 0.045) and BCD (P = 0.030). The most common cardiac disorders associated with dogs with PE included mitral and tricuspid valve regurgitation due to CDVD (17/51 [33.3%] dogs), intrapericardial neoplasia (16/51 [31.4%] dogs), and IPE (11/51 [21.6%] dogs). Mitral valve regurgitation (28/50 [56%] dogs) and subaortic stenosis (10/50 [20%] dogs) were most frequently associated with dogs with UCD, whereas mitral and tricuspid valve regurgitation due to CDVD (43/50 [86%] dogs) and DCM (7/50 [14%] dogs) were most frequently associated with dogs with BCD.

Mild PE was diagnosed in 21 of 51 (41.2%) dogs (17 dogs with CDVD, 2 dogs with intrapericardial neoplasia, 1 dog with IPE, and 1 dog with CDVD associated with intrapericardial neoplasia). Moderate PE was diagnosed in 14 of 51 (27.5%) dogs (7 dogs with intrapericardial neoplasia, 3 dogs with CDVD, 3 dogs with IPE, and 1 dog with CDVD associated with intrapericardial neoplasia). Severe PE was diagnosed in 16 of 51 (31.4%) dogs (7 dogs with IPE, 5 dogs with intrapericardial neoplasia, 2 dogs with CDVD, 1 dog with CDVD associated with intrapericardial neoplasia, and 1 dog with DCM). The sum of the pericardial echo-free space in these dogs ranged from 27 to 70 mm.

Radiographic indexes for the 4 groups of dogs were summarized (Table 2). Lateral (Figure 1) and ventrodorsal (Figure 2) VHS were significantly higher in dogs with PE than in the other 3 groups of dogs.

Table 2—

Measured values for 5 radiographic cardiac indexes in 50 healthy dogs (control), 51 dogs with PE, 50 dogs with a UCD without PE, and 50 dogs with a BCD without PE.

GroupVHSSI
LateralVentrodorsalLateralVentrodorsalGlobal
Healthy10.4 ± 0.610.4 ± 0.81.25 ± 0.111.35 ± 0.111.30 ± 0.10
PE13.1 ± 1.113.4 ± 1.51.11 ± 0.111.13 ± 0.091.12 ± 0.07
UCD11.6 ± 1.011.8 ± 1.41.22 ± 0.111.24 ± 0.151.23 ± 0.10
BCD11.7 ± 1.011.4 ± 1.21.20 ± 0.121.22 ± 0.111.21 ± 0.09

Data are reported as mean ± SD.

Of the 51 dogs with PE, 30 had ventrodorsal radiographs available (the remaining 21 dogs had dorsoventral radiographs).

Figure 1—
Figure 1—

Vertebral heart score measured from lateral thoracic radiographs (L-VHS) of 50 healthy dogs (C), 51 dogs with PE, 50 dogs with a UCD (without PE), and 50 dogs with a BCD (without PE). The horizontal line in each box represents the median. Boxes represent the interquartile range (25th to 75th percentile). Whiskers represent the 5th and 95th percentiles. Outliers are plotted separately as squares. *Value is significantly (P < 0.001) different from that of healthy dogs. §Value is significantly (P < 0.001) different from that of dogs with a UCD or BCD. NS = Not significantly different.

Citation: Journal of the American Veterinary Medical Association 241, 8; 10.2460/javma.241.8.1048

Figure 2—
Figure 2—

Vertebral heart score measured from ventrodorsal thoracic radiographs (VD-VHS) of the same dogs as in Figure 1. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 241, 8; 10.2460/javma.241.8.1048

Lateral and ventrodorsal VHS in dogs with UCD and BCD were, in turn, significantly higher than those for healthy dogs. No significant differences in lateral and ventrodorsal VHS were found between dogs with UCD or BCD.

Lateral (Figure 3), ventrodorsal (Figure 4), and global (Figure 5) SI values were significantly lower in dogs with PE than in the other 3 groups of dogs. Ventrodorsal and global SI values in dogs with UCD or BCD were, in turn, significantly lower than those for healthy dogs. No significant differences were found between lateral, ventrodorsal, and global SI values in dogs with UCD and BCD and between lateral SI values in dogs with either UCD or BCD and healthy dogs.

Figure 3—
Figure 3—

Sphericity index measured from lateral thoracic radiographs (L-SI) of the same dogs as in Figure 1. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 241, 8; 10.2460/javma.241.8.1048

Figure 4—
Figure 4—

Sphericity index measured from ventrodorsal thoracic radiographs (VD-SI) of the same dogs as in Figure 1. §Value is significantly (P < 0.01) different from that of dogs with a UCD. #Value is significantly (P < 0.05) different from that of dogs with a BCD. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 241, 8; 10.2460/javma.241.8.1048

Figure 5—
Figure 5—

Global SI (G-SI) as the mean of the lateral and ventrodorsal SI values of the same dogs as in Figure 1. *Value is significantly (P ≤ 0.001) different than that of healthy dogs. See Figure 1 for remainder of key.

Citation: Journal of the American Veterinary Medical Association 241, 8; 10.2460/javma.241.8.1048

Receiver operating characteristic curve characteristics for each radiographic index that was used to distinguish dogs with PE from those with various cardiac disorders without PE were summarized (Table 3). All radiographic indexes were moderately accurate at identifying PE, with AUC ± SE values of 0.839 ± 0.037 (lateral VHS), 0.842 ± 0.047 (ventrodorsal VHS), 0.747 ± 0.040 (lateral SI), 0.736 ± 0.047 (ventrodorsal SI), and 0.827 ± 0.037 (global SI). Cutoffs of > 11.9, > 12.3, and ≤ 1.17 for lateral VHS, ventrodorsal VHS, and global SI, respectively, had the best equilibrium between sensitivity and specificity, and these were the most accurate radiographic indexes for distinguishing dogs with PE from dogs with various cardiac disorders without PE.

Table 3—

Diagnostic accuracy of 5 radiographic indexes for distinguishing dogs with PE from dogs with various cardiac disorders without PE.

IndexAUC ± SE95% CICutoffSensitivitySpecificityPLRNLR
Lateral VHS0.839 ± 0.0370.771–0.894> 10.91.000.261.350.00
> 11.9*0.900.662.650.15
> 14.20.121.00NA0.88
Ventrodorsal VHS0.842 ± 0.0470.768–0.900> 11.21.000.421.720.00
> 12.3*0.730.763.060.35
> 15.00.071.00NA0.93
Lateral SI0.747 ± 0.0400.670–0.814≤ 1.351.000.061.060.00
≤ 1.16*0.710.692.280.43
≤ 0.900.041.00NA0.96
Ventrodorsal SI0.736 ± 0.0470.651–0.809≤ 1.301.000.311.450.00
≤ 1.17*0.730.702.440.38
< 0.880.001.00NA1.00
Global SI0.827 ± 0.0370.750–0.887≤ 1.301.000.181.220.00
≤ 1.17*0.870.712.990.19
≤ 1.000.031.00NA0.97

Values with the best equilibrium between sensitivity and specificity.

CI = Confidence interval. NA = Not applicable. NLR = Negative likelihood ratio. PLR = Positive likelihood ratio.

Radiographic indexes obtained after further grouping of the dogs according to PE severity were summarized (Table 4). No significant differences were found for lateral and ventrodorsal VHS and global SI values among the 3 subgroups of dogs with PE. The lateral SI in dogs with severe PE was significantly (P = 0.035) lower than in dogs with mild PE.

Table 4—

Measured values for 5 radiographic cardiac indexes in 51 dogs with PE classified as mild PE, moderate PE, and severe PE.

GroupNo. of radiographsVHSSI
LateralVentrodorsalLateralVentrodorsalLateralVentrodorsalGlobal
Mild PE21813.1 ± 0.913.8 ± 1.01.15 ± 0.111.19 ± 0.081.16 ± 0.10
Moderate PE141113.0 ± 0.913.3 ± 1.41.08 ± 0.091.14 ± 0.071.11 ± 0.07
Severe PE161113.3 ± 1.413.4 ± 1.21.07 ± 0.111.13 ± 0.091.09 ± 0.06

See Table 2 for key.

Receiver operating characteristic curve characteristics for each of the considered radiographic indexes used to distinguish dogs with mild, moderate, and severe PE from dogs with various cardiac disorders without PE were summarized (Table 5). The diagnostic accuracy of lateral and ventrodorsal VHS to distinguish dogs with different severity of PE from dogs with cardiac diseases without PE was basically moderate, with a high diagnostic accuracy for ventrodorsal VHS in dogs with mild PE (AUC ± SE, 0.908 ± 0.082). The diagnostic accuracy of lateral, ventrodorsal, and global SI to distinguish dogs with different severities of PE from dogs with cardiac diseases without PE was low for dogs with mild PE and moderate for dogs with moderate and severe PE. In particular, the accuracy of global SI in dogs with severe PE was close to a high level (AUC ± SE, 0.897 ± 0.035).

Table 5—

Diagnostic accuracy of 5 radiographic indexes for distinguishing dogs with differing degrees of PE from dogs with various cardiac disorders without PE.

IndexDegree of PEAUC ± SE95% CICutoffSensitivitySpecificityPLRNLR
Lateral VHSMild0.849 ± 0.0550.772–0.907> 11.90.950.662.800.07
Moderate0.824 ± 0.0700.741–0.889> 12.10.860.692.760.21
Severe0.840 ± 0.0640.760–0.901> 11.90.880.662.570.19
Ventrodorsal VHSMild0.908 ± 0.0820.836–0.955> 13.20.830.897.580.19
Moderate0.820 ± 0.0800.736–0.886> 11.51.000.552.220.00
Severe0.843 ± 0.0760.762–0.905> 12.70.820.814.310.22
Lateral SIMild0.638 ± 0.0620.546–0.723≤ 1.150.570.701.900.61
Moderate0.816 ± 0.0490.732–0.882≤ 1.160.860.692.760.21
Severe0.829 ± 0.0440.748–0.893≤ 1.180.940.592.290.11
Ventrodorsal SIMild0.629 ± 0.1070.530–0.721≤ 1.301.000.311.450.00
Moderate0.754 ± 0.0650.663–0.830≤ 1.170.820.702.730.26
Severe0.771 ± 0.0620.682–0.845≤ 1.140.730.763.030.36
Global SIMild0.669 ± 0.1010.571–0.758≤ 1.170.670.712.300.47
Moderate0.844 ± 0.0480.763–0.906≤ 1.170.910.713.130.13
Severe0.897 ± 0.0350.825–0.947≤ 1.150.910.794.330.12

See Table 3 for key.

Discussion

Although it is generally accepted that cardiac silhouettes are usually enlarged and rounded in dogs with PE, to the best of our knowledge, the present study is the first to attempt to objectively evaluate the characteristics in thoracic radiographs obtained from a large group of dogs with PE. In addition, the present study included dogs with different severities of PE, ranging from a mild volume of fluid, mainly found in dogs with congestive heart failure due to CDVD, to moderate or severe volumes of fluid, mainly found in dogs with intrapericardial neoplasia and IPE. Furthermore, in addition to healthy dogs, dogs with various cardiac disorders without PE were used as control dogs.

The mean lateral and ventrodorsal VHS of dogs with cardiac diseases were significantly higher than those of healthy dogs. More importantly, dogs with PE had significantly higher lateral and ventrodorsal VHS than did dogs with different cardiac diseases without PE. These findings confirm the fact that PE is usually associated with a severe enlargement of the cardiac silhouette. Vertebral heart scores refect the overall dimensions of the cardiac silhouette and incorporate all chambers of the heart, including the myocardium and pericardium.15,17–20 Cardiac diseases associated with an increase in chamber dilatation (cardiac eccentric hypertrophy) are the main reported causes of a high VHS.18–22 In the present study, 2 pathophysiologic mechanisms were found to be responsible for the high VHS observed in dogs with PE. First, the enlarged cardiac silhouettes and high VHS measured in dogs with severe PE were mainly due to large amounts of fluid within the pericardial sac, and the cardiac chambers were usually not dilated in these dogs. In contrast, in dogs with mild PE, severe cardiac eccentric hypertrophy due to decompensated valvular disease associated with mild volumes of fluid in the pericardial sac was responsible for the enlarged cardiac silhouette observed, and CDVD was mainly diagnosed in these dogs. A combination of these 2 mechanisms was found in dogs with moderate PE. However, the accuracy of VHS used to distinguish dogs with PE from dogs with cardiac disorders without PE was only moderate. Highly similar AUCs, with slightly different sensitivity, specificity, positive likelihood ratio, and negative likelihood ratio, were obtained for both lateral and ventrodorsal VHS. A cutoff of 11.9 for lateral VHS, which is the most frequently used method for cardiomegaly quantification in dogs, had a sensitivity of 0.90 and a specificity of 0.66 in distinguishing dogs with PE from dogs with cardiac disorders without PE. This low specificity was caused by the increased cardiac dimensions found in many dogs with either UCD or BCD without PE, particularly in dogs with CDVD or DCM with moderate to severe eccentric cardiac hypertrophy. Therefore, although dogs with PE had significantly increased mean VHS, compared with dogs with cardiac disorders without PE, a considerable overlap in the measured VHS was observed. These findings were confirmed by successive analysis conducted after separating dogs with PE according to the amount of fluid accumulating into the pericardial sac. No significant differences were found for lateral and ventrodorsal VHS among dogs with mild, moderate, and severe PE. Accordingly, only slight differences were found in the diagnostic accuracy of lateral and ventrodorsal VHS in differentiating dogs with differing degrees of PE from dogs with cardiac disorders without PE. Surprisingly, the highest diagnostic accuracy of these indexes was found in dogs with mild PE, in particular the use of the ventrodorsal VHS. These findings suggest that the combined effect of eccentric cardiac hypertrophy and the presence of even a small amount of PE is responsible for the highest enlargement of the cardiac silhouette in dogs with PE, and this effect is mainly evident in the ventrodorsal radiographic view of the thorax.

Sphericity index is another index that can be used to evaluate both the globular shape of the whole cardiac silhouette and specific heart chambers.19,23,24 In the present study, lateral and ventrodorsal SI values were obtained by calculating the ratio of the long axis to the short axis of the cardiac silhouette with lateral and ventrodorsal radiographic views of the thorax, respectively. Furthermore, global SI values were calculated as the mean value between the lateral and ventrodorsal SI values. An index of 1.0 indicates a circular figure, whereas an elongated cardiac silhouette results in an increased value. In the present study, lateral and ventrodorsal SI values were the least accurate indexes for diagnosing PE. In particular, both lateral and ventrodorsal SI values had a low sensitivity and specificity. The low sensitivity of these indexes was mainly the result of high values observed in some dogs with PE, particularly dogs with deep and narrow chests. Conversely, the low specificity of the indexes was due to the low values observed in some dogs with cardiac diseases without PE, particularly dogs with BCD. The low specificity calculated for ventrodorsal SI was not surprising because cardiac silhouettes appear rounded in the ventrodorsal radiographic view of the thorax in healthy dogs with deep and narrow chests.25 However, global SI was more accurate for the identification of dogs with PE, compared with either lateral or ventrodorsal SI alone. In particular, a global SI cutoff ≤ 1.17 resulted in a sensitivity of 0.87 and specificity of 0.71 for distinguishing dogs with PE from dogs with cardiac disorders without PE. This low specificity was mainly attributed to high global SI values (≥ 1.20) observed in 4 dogs with PE (3 dogs with intrapericardial tumors and 1 dog with decompensated CDVD) coupled with the low global SI values (≤ 1.14) measured in 10 dogs with combined mitral and tricuspid regurgitation. The sensitivity of subjective evaluations of globoid-shaped cardiac silhouettes in dogs with PE from others studies6–8 ranged from 0.33 to 0.87. However, there are important differences between those studies6–8 and the present study. Compared with other studies, which mainly included dogs with moderate to severe PE, our study addressed a wider distribution of PE severities, and > 40% of the dogs included in the present study had mild PE. Furthermore, in addition to healthy dogs, control dogs with various cardiac disorders were used for comparison. After separating dogs with PE according to the amount of fluid accumulating into the pericardial sac, significantly different values were only found for lateral SI among dogs with severe PE, compared with dogs with mild PE. Accordingly, all SI values had low accuracy for distinguishing dogs with mild PE from dogs with cardiac diseases without PE and were still moderately accurate for distinguishing dogs with moderate or severe PE from dogs with cardiac diseases without PE. A notably high diagnostic accuracy was only found for the cutoff of global SI ≤ 1.15 in dogs with severe PE.

This study has some limitations that need to be emphasized. First, because we used a retrospective study design, adherence to a consistent standardized protocol for obtaining the thoracic radiographs was not possible. Calculated VHS for the same dog can vary in the right lateral view, compared with the left lateral view, and in the ventrodorsal view, compared with the dorsoventral view.15,18,26 Only radiographs obtained in right lateral and ventrodorsal views were used for statistical analysis in this study. Sternal recumbency has been used for some dogs with PE and orthopnea, so the number of available ventrodorsal views was lower (ie, 30), compared with the right lateral view, limiting the sample size for calculating ventrodorsal VHS, ventrodorsal SI, and global SI. Second, although most dogs have the same upper lateral VHS limit (≤ 10.5) for normal cardiac size,15 higher upper lateral VHS limits have been reported for some breeds (eg, Boxers, Cavalier King Charles Spaniels, Labrador Retrievers, Whippets, Beagles, and Greyhounds).27–30 Therefore, it is possible that breed influence was partially responsible for the overlapping lateral VHS we observed because some Boxers (4 dogs with PE, 2 with UCD, and 5 with BCD) and Cavalier King Charles Spaniels (1 dog with PE, 1 with UCD, and 5 with BCD) and 1 Labrador Retriever (in the PE group) were included in the study reported here. Third, VHS can be influenced by concurrent vertebral malformations or disk degeneration, causing vertebral shortening and narrowing of the disk space, respectively; by the observer's experience; and by choice of landmarks for measurements.17 The effect of degenerative changes of the vertebral column could be even more pronounced in the oldest dogs of the present study (ie, dogs from PE and BCD groups), leading to increased variability in the calculated VHS. The same experienced observer obtained all VHS measurements in dogs of the present study using the method proposed by Buchanan and Bucheler.15 A slightly modified method of measuring the short axis of the cardiac silhouette uses the midpoint of the caudal vena cava as a landmark to improve the precision of anatomic points for measurement of lateral VHS.17 However, in dogs with globoid hearts and dorsally displaced caudal vena cava (ie, those with BCD and PE), substantially different lateral VHS can be obtained; therefore, we decided to measure the short axis at the point of maximum cardiac width. Finally, the results obtained after further grouping of dogs according to PE severity should be interpreted with caution because of the low sample size of the 3 groups of dogs and the lack of a precise and standardized protocol for classifying PE severity in dogs, particularly when a retrospective study design is used.

In conclusion, the present study confirms that cardiac silhouettes in dogs with PE are larger and more rounded, compared with dogs with cardiac disorders without PE. Cutoffs of > 11.9, > 12.3, and ≤ 1.17 for lateral VHS, ventrodorsal VHS, and global SI, respectively, can be useful indicators of PE in dogs. However, objective radiographic indexes of cardiac size and roundness are only moderately accurate at distinguishing dogs with PE from dogs with other cardiac disorders without PE. The diagnostic accuracy of the considered radiographic indexes does not substantially improve after further grouping of dogs on the basis of amounts of pericardial fluid. However, cutoff values of > 13.2 and ≤ 1.15 for ventrodorsal VHS and global SI, respectively, can be useful to differentiate dogs with mild and severe PE from dogs with cardiac disorders without PE. Echocardiography was used as the standard in this study for detection and severity of PE and remains the most accurate noninvasive method for pericardial evaluation in dogs. Despite overlap in ranges of radiographic measurement techniques in classes of cardiac disease found in this study, the presence of PE was readily observed on echocardiography, regardless of underlying cardiac disease.

ABBREVIATIONS

AUC

Area under the curve

BCD

Bilateral cardiac disorder

CDVD

Chronic degenerative valvular disease

DCM

Dilated cardiomyopathy

IPE

Idiopathic pericardial effusion

PE

Pericardial effusion

SI

Sphericity index

UCD

Unilateral cardiac disorder

VHS

Vertebral heart score

a.

SPSS 15.0 for Windows, SPSS Inc, Chicago, Ill.

b.

MedCalc, version 7.3, Mariakerke, Belgium.

References

  • 1. Shaw PS, Rush JE. Canine pericardial effusion: pathophysiology and cause. Compend Contin Educ Pract Vet 2007; 29:400404.

  • 2. Ware W. Pericardial disease and cardiac tumors. In: Cardiovascular disease in small animal medicine. London: Manson Publishing, 2007;320327.

    • Search Google Scholar
    • Export Citation
  • 3. Tobias AH. Pericardial diseases. In: Ettinger SJ, Feldman CE, eds. Textbook of veterinary internal medicine. 7th ed. St Louis: Saunders Elsevier, 2010;13421352.

    • Search Google Scholar
    • Export Citation
  • 4. Berg R, Wingfield W. Pericardial effusion in the dog: a review of 42 cases. J Am Anim Hosp Assoc 1984; 20:721730.

  • 5. Dunning D, Monnet E, Orton C, et al. Analysis of prognostic indicators for dogs with pericardial effusion: 46 cases (1985–1996). J Am Vet Med Assoc 1998; 212:12761280.

    • Search Google Scholar
    • Export Citation
  • 6. Stepien RL, Whitley NT, Dubielzig RR. Idiopathic or mesothelioma-related pericardial effusion: clinical findings and survival in 17 dogs studied retrospectively. J Small Anim Pract 2000; 41:342347.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Stafford Johnson M, Martin M, Binns S, et al. A retrospective study of clinical findings, treatment and outcome in 143 dogs with pericardial effusion. J Small Anim Pract 2004; 45:546552.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. MacDonald KA, Cagney O, Magne ML. Echocardiographic and clinicopathologic characterization of pericardial effusion in dogs: 107 cases (1985–2006). J Am Vet Med Assoc 2009; 235:14561461.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Aronson LR, Gregory CR. Infectious pericardial effusion in five dogs. Vet Surg 1995; 24:402407.

  • 10. Petrus DJ, Henik RA. Pericardial effusion and cardiac tamponade secondary to brodifacoum toxicosis in a dog. J Am Vet Med Assoc 1999; 215:647648.

    • Search Google Scholar
    • Export Citation
  • 11. Reineke EL. Burkett DE. Drobatz KJ. Left atrial rupture in dogs: 14 cases (1990–2005). J Vet Emerg Crit Care 2008; 18:158164.

  • 12. Shaw PS, Rush JE. Canine pericardial effusion: diagnosis, treatment, and prognosis. Compend Contin Educ Pract Vet 2007; 29:405411.

    • Search Google Scholar
    • Export Citation
  • 13. Bahr RJ. Heart and pulmonary vessels. In: Thrall DE, ed. Textbook of veterinary diagnostic radiology. 5th ed. St Louis: Saunders Elsevier, 2007;568590.

    • Search Google Scholar
    • Export Citation
  • 14. Maisch B, Seferovic PM, Ristic AD, et al. Guidelines on the diagnosis and management of pericardial diseases executive summary. The Task Force on the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology. Eur Heart J 2004; 25:587610.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Buchanan JW, Bucheler J. Vertebral scale system to measure canine heart size in radiographs. J Am Vet Med Assoc 1995; 206:194199.

  • 16. Gardner IA, Greiner M. Receiver-operating characteristics curves and likelihood ratios: improvements over traditional methods for the evaluation and application of veterinary clinical pathology tests. Vet Clin Pathol 2006; 35:817.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Hansson K, Häggström J, Kvart C, et al. Interobserver variability of vertebral heart size measurements in dogs with normal and enlarged hearts. Vet Radiol Ultrasound 2005; 46:122130.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Lamb CR, Tyler M, Boswood A, et al. Assessment of the value of the vertebral heart scale in the radiographic diagnosis of cardiac disease in dogs. Vet Rec 2000; 146:687690.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Nakayama H, Nakayama T, Hamlin R. Correlation of cardiac enlargement as assessed by vertebral heart size and echocardiographic and electrocardiographic findings in dogs with evolving cardiomegaly due to rapid ventricular pacing. J Vet Intern Med 2001; 15:217221.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Lamb CR, Boswood A. Role of survey radiography in diagnosing canine cardiac disease. Compend Contin Educ Pract Vet 2002; 24:316326.

    • Search Google Scholar
    • Export Citation
  • 21. Guglielmini C, Diana A, Pietra M, et al. Use of vertebral heart score in coughing dogs with chronic degenerative mitral valve disease. J Vet Med Sci 2009; 71:913.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Lord P, Hansson K, Kvart C, et al. Rate of change of heart size before congestive heart failure in dogs with mitral regurgitation. J Small Anim Pract 2010; 51:210218.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Dukes-McEwan J, Borgarelli M, Tidholm A, et al. Proposed guidelines for the diagnosis of canine idiopathic dilated cardiomyopathy. J Vet Cardiol 2003; 5:719.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Carlsson C, Häggström J, Eriksson A, et al. Size and shape of right heart chambers in mitral valve regurgitation in small-breed dogs. J Vet Intern Med 2009; 23:10071013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Berry CR, Graham JP, Thrall DE. Interpretation paradigms for the small animal thorax. In: Thrall DE, ed. Textbook of veterinary diagnostic radiology. 5th ed. St Louis: Saunders Elsevier, 2007;462485.

    • Search Google Scholar
    • Export Citation
  • 26. Greco A, Meomartino L, Raiano V, et al. Effect of left vs. right recumbency on the vertebral heart score in normal dogs. Vet Radiol Ultrasound 2008; 49:454455.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Lamb CR, Wikeley H, Boswood A, et al. Use of breed-specific ranges for the vertebral heart scale as an aid to the radiographic diagnosis of cardiac disease in dogs. Vet Rec 2001; 148:707711.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Bavegems V, Van Caelenberg A, Duchateau L, et al. Vertebral heart size ranges specific for whippets. Vet Radiol Ultrasound 2005; 46:400403.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Marin LM, Brown J, McBrien C, et al. Vertebral heart size in retired racing Greyhounds. Vet Radiol Ultrasound 2007; 48:332334.

  • 30. Kraetschmer S, Ludwig K, Meneses F, et al. Vertebral heart scale in the Beagle dog. J Small Anim Pract 2008; 49:240243.

  • Figure 1—

    Vertebral heart score measured from lateral thoracic radiographs (L-VHS) of 50 healthy dogs (C), 51 dogs with PE, 50 dogs with a UCD (without PE), and 50 dogs with a BCD (without PE). The horizontal line in each box represents the median. Boxes represent the interquartile range (25th to 75th percentile). Whiskers represent the 5th and 95th percentiles. Outliers are plotted separately as squares. *Value is significantly (P < 0.001) different from that of healthy dogs. §Value is significantly (P < 0.001) different from that of dogs with a UCD or BCD. NS = Not significantly different.

  • Figure 2—

    Vertebral heart score measured from ventrodorsal thoracic radiographs (VD-VHS) of the same dogs as in Figure 1. See Figure 1 for remainder of key.

  • Figure 3—

    Sphericity index measured from lateral thoracic radiographs (L-SI) of the same dogs as in Figure 1. See Figure 1 for remainder of key.

  • Figure 4—

    Sphericity index measured from ventrodorsal thoracic radiographs (VD-SI) of the same dogs as in Figure 1. §Value is significantly (P < 0.01) different from that of dogs with a UCD. #Value is significantly (P < 0.05) different from that of dogs with a BCD. See Figure 1 for remainder of key.

  • Figure 5—

    Global SI (G-SI) as the mean of the lateral and ventrodorsal SI values of the same dogs as in Figure 1. *Value is significantly (P ≤ 0.001) different than that of healthy dogs. See Figure 1 for remainder of key.

  • 1. Shaw PS, Rush JE. Canine pericardial effusion: pathophysiology and cause. Compend Contin Educ Pract Vet 2007; 29:400404.

  • 2. Ware W. Pericardial disease and cardiac tumors. In: Cardiovascular disease in small animal medicine. London: Manson Publishing, 2007;320327.

    • Search Google Scholar
    • Export Citation
  • 3. Tobias AH. Pericardial diseases. In: Ettinger SJ, Feldman CE, eds. Textbook of veterinary internal medicine. 7th ed. St Louis: Saunders Elsevier, 2010;13421352.

    • Search Google Scholar
    • Export Citation
  • 4. Berg R, Wingfield W. Pericardial effusion in the dog: a review of 42 cases. J Am Anim Hosp Assoc 1984; 20:721730.

  • 5. Dunning D, Monnet E, Orton C, et al. Analysis of prognostic indicators for dogs with pericardial effusion: 46 cases (1985–1996). J Am Vet Med Assoc 1998; 212:12761280.

    • Search Google Scholar
    • Export Citation
  • 6. Stepien RL, Whitley NT, Dubielzig RR. Idiopathic or mesothelioma-related pericardial effusion: clinical findings and survival in 17 dogs studied retrospectively. J Small Anim Pract 2000; 41:342347.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Stafford Johnson M, Martin M, Binns S, et al. A retrospective study of clinical findings, treatment and outcome in 143 dogs with pericardial effusion. J Small Anim Pract 2004; 45:546552.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. MacDonald KA, Cagney O, Magne ML. Echocardiographic and clinicopathologic characterization of pericardial effusion in dogs: 107 cases (1985–2006). J Am Vet Med Assoc 2009; 235:14561461.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Aronson LR, Gregory CR. Infectious pericardial effusion in five dogs. Vet Surg 1995; 24:402407.

  • 10. Petrus DJ, Henik RA. Pericardial effusion and cardiac tamponade secondary to brodifacoum toxicosis in a dog. J Am Vet Med Assoc 1999; 215:647648.

    • Search Google Scholar
    • Export Citation
  • 11. Reineke EL. Burkett DE. Drobatz KJ. Left atrial rupture in dogs: 14 cases (1990–2005). J Vet Emerg Crit Care 2008; 18:158164.

  • 12. Shaw PS, Rush JE. Canine pericardial effusion: diagnosis, treatment, and prognosis. Compend Contin Educ Pract Vet 2007; 29:405411.

    • Search Google Scholar
    • Export Citation
  • 13. Bahr RJ. Heart and pulmonary vessels. In: Thrall DE, ed. Textbook of veterinary diagnostic radiology. 5th ed. St Louis: Saunders Elsevier, 2007;568590.

    • Search Google Scholar
    • Export Citation
  • 14. Maisch B, Seferovic PM, Ristic AD, et al. Guidelines on the diagnosis and management of pericardial diseases executive summary. The Task Force on the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology. Eur Heart J 2004; 25:587610.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Buchanan JW, Bucheler J. Vertebral scale system to measure canine heart size in radiographs. J Am Vet Med Assoc 1995; 206:194199.

  • 16. Gardner IA, Greiner M. Receiver-operating characteristics curves and likelihood ratios: improvements over traditional methods for the evaluation and application of veterinary clinical pathology tests. Vet Clin Pathol 2006; 35:817.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Hansson K, Häggström J, Kvart C, et al. Interobserver variability of vertebral heart size measurements in dogs with normal and enlarged hearts. Vet Radiol Ultrasound 2005; 46:122130.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Lamb CR, Tyler M, Boswood A, et al. Assessment of the value of the vertebral heart scale in the radiographic diagnosis of cardiac disease in dogs. Vet Rec 2000; 146:687690.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Nakayama H, Nakayama T, Hamlin R. Correlation of cardiac enlargement as assessed by vertebral heart size and echocardiographic and electrocardiographic findings in dogs with evolving cardiomegaly due to rapid ventricular pacing. J Vet Intern Med 2001; 15:217221.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Lamb CR, Boswood A. Role of survey radiography in diagnosing canine cardiac disease. Compend Contin Educ Pract Vet 2002; 24:316326.

    • Search Google Scholar
    • Export Citation
  • 21. Guglielmini C, Diana A, Pietra M, et al. Use of vertebral heart score in coughing dogs with chronic degenerative mitral valve disease. J Vet Med Sci 2009; 71:913.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. Lord P, Hansson K, Kvart C, et al. Rate of change of heart size before congestive heart failure in dogs with mitral regurgitation. J Small Anim Pract 2010; 51:210218.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Dukes-McEwan J, Borgarelli M, Tidholm A, et al. Proposed guidelines for the diagnosis of canine idiopathic dilated cardiomyopathy. J Vet Cardiol 2003; 5:719.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Carlsson C, Häggström J, Eriksson A, et al. Size and shape of right heart chambers in mitral valve regurgitation in small-breed dogs. J Vet Intern Med 2009; 23:10071013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Berry CR, Graham JP, Thrall DE. Interpretation paradigms for the small animal thorax. In: Thrall DE, ed. Textbook of veterinary diagnostic radiology. 5th ed. St Louis: Saunders Elsevier, 2007;462485.

    • Search Google Scholar
    • Export Citation
  • 26. Greco A, Meomartino L, Raiano V, et al. Effect of left vs. right recumbency on the vertebral heart score in normal dogs. Vet Radiol Ultrasound 2008; 49:454455.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Lamb CR, Wikeley H, Boswood A, et al. Use of breed-specific ranges for the vertebral heart scale as an aid to the radiographic diagnosis of cardiac disease in dogs. Vet Rec 2001; 148:707711.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Bavegems V, Van Caelenberg A, Duchateau L, et al. Vertebral heart size ranges specific for whippets. Vet Radiol Ultrasound 2005; 46:400403.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Marin LM, Brown J, McBrien C, et al. Vertebral heart size in retired racing Greyhounds. Vet Radiol Ultrasound 2007; 48:332334.

  • 30. Kraetschmer S, Ludwig K, Meneses F, et al. Vertebral heart scale in the Beagle dog. J Small Anim Pract 2008; 49:240243.

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