Radiographic findings of cardiopulmonary structures can predict hypertrophic cardiomyopathy and congestive heart failure in cats

Soyeon Kim Department of Veterinary Medical Imaging, College of Veterinary Medicine, Seoul National University, Seoul, South Korea

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Dongjae Lee Department of Veterinary Medical Imaging, College of Veterinary Medicine, Seoul National University, Seoul, South Korea

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Seungjo Park Department of Veterinary Medical Imaging, College of Veterinary Medicine, Chonnam National University, Gwangju, South Korea

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Guk Hyun Suh Department of Veterinary Internal Medicine, College of Veterinary Medicine, Chonnam National University, Gwangju, South Korea

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Jihye Choi Department of Veterinary Medical Imaging, College of Veterinary Medicine, Seoul National University, Seoul, South Korea

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Abstract

OBJECTIVE

This study aimed to find the radiographic characteristics for the detection of hypertrophic cardiomyopathy (HCM) and congestive heart failure (CHF) in cats.

ANIMALS

Healthy cats (n = 35) and HCM cats with (21) and without (22) CHF.

METHODS

On radiography, the cardiac size using vertebral heart score, left atrium enlargement (LAE), and dilation of the pulmonary vessels were assessed. The sensitivity and specificity of the radiographic characteristics regarding LAE were evaluated with the echocardiographic left atrium to aortic root ratio as a reference.

RESULTS

In HCM cats, cardiomegaly, LAE, and dilation of the caudal pulmonary artery were found compared with those in healthy cats. The LAE could be predicted using the elevation of the carina with 94.12% specificity but 17.5% sensitivity. When CHF developed, LAE and dilation of the caudal pulmonary vein (PV) were significantly different compared with those in HCM cats without CHF. The distal side of the summated shadow made by the right caudal PV with the ninth rib in HCM cats with CHF was significantly larger than that in HCM cats without CHF and a cut-off value of 5.35 mm was drawn with 75% sensitivity and 100% specificity.

CLINICAL RELEVANCE

Although there was an overlapping of radiographic findings between healthy and HCM cats, radiographic assessment of LAE can be useful for predicting HCM and the distal side of the summated shadow made by the right caudal PV with the ninth rib can predict CHF in HCM cats.

Abstract

OBJECTIVE

This study aimed to find the radiographic characteristics for the detection of hypertrophic cardiomyopathy (HCM) and congestive heart failure (CHF) in cats.

ANIMALS

Healthy cats (n = 35) and HCM cats with (21) and without (22) CHF.

METHODS

On radiography, the cardiac size using vertebral heart score, left atrium enlargement (LAE), and dilation of the pulmonary vessels were assessed. The sensitivity and specificity of the radiographic characteristics regarding LAE were evaluated with the echocardiographic left atrium to aortic root ratio as a reference.

RESULTS

In HCM cats, cardiomegaly, LAE, and dilation of the caudal pulmonary artery were found compared with those in healthy cats. The LAE could be predicted using the elevation of the carina with 94.12% specificity but 17.5% sensitivity. When CHF developed, LAE and dilation of the caudal pulmonary vein (PV) were significantly different compared with those in HCM cats without CHF. The distal side of the summated shadow made by the right caudal PV with the ninth rib in HCM cats with CHF was significantly larger than that in HCM cats without CHF and a cut-off value of 5.35 mm was drawn with 75% sensitivity and 100% specificity.

CLINICAL RELEVANCE

Although there was an overlapping of radiographic findings between healthy and HCM cats, radiographic assessment of LAE can be useful for predicting HCM and the distal side of the summated shadow made by the right caudal PV with the ninth rib can predict CHF in HCM cats.

Hypertrophic cardiomyopathy (HCM) is the most common cardiac disease in cats.1 It is reported in 15% of cats and up to 29% of older cats.2,3 HCM can progress to congestive heart failure (CHF) and cause clinical manifestations such as respiratory distress or paresis and short survival time.46

Echocardiography is used to diagnose HCM based on left ventricular (LV) hypertrophy that is indicated by thickening of the left ventricular wall (LVW) or interventricular septum more than 6 mm during diastole according to the American College of Veterinary Internal Medicine consensus guidelines.3 Echocardiography can also evaluate the LV hypertrophy pattern, the presence of left ventricular outflow tract (LVOT) obstruction, possibly with systolic anterior motion, left atrium enlargement (LAE), and diastolic failure with an elevated LV filling pressure.4 The severity of HCM can be assessed by the LV thickness, left atrium (LA) size, left atrial appendage velocity, and the presence of spontaneous echo contrast, which is a negative prognostic indicator of a significantly shorter mean survival time and an increased risk of cardiac death.4,6,7 Recently, in the emergency department, thoracic ultrasonography has been introduced to determine the treatment plan for heart failure or respiratory disease in dyspneic cats by quickly evaluating the presence of LAE, pleural effusion, and interstitial fluid using comet-tail artifacts.810 However, in cats with HCM, diagnosis of CHF using ultrasonography has limitations. The comet-tail artifacts support the diagnosis of pulmonary edema with a sensitivity of 84% and a specificity of 74%, but it can also lead to misdiagnosis of cardiogenic pulmonary edema.10

In the clinic, thoracic radiography is used to describe the change in the shape and size of the heart and determine CHF in patients with suspected cardiac diseases. Radiography is widely available to most veterinarians, is easier to perform, and facilitates the interpretation of pulmonary edema.1113 Therefore, thoracic radiography is used to screen for CHF as the cause of dyspnea or respiratory distress in dogs.12,14 Cardiogenic pulmonary edema consistent with left-sided congestive heart failure (L-CHF) in dogs exhibits the typical distribution of the alveolar and interstitial infiltrates in the perihilar region and bilateral caudal lobes symmetrically, although an asymmetric or focal distribution can occur.14 Therefore, typical lung infiltrates including the changes in the cardiac shape and size on thoracic radiography can indicate cardiogenic pulmonary edema in dogs. In a study of 23 cats, radiographic appearances of cardiogenic pulmonary edema were more variable than those in dogs: interstitial (100%), alveolar (83%), and bronchial (61%) patterns.8,13,1517 Therefore, cardiogenic pulmonary edema in dogs and cats displays some differences in distribution and pattern. Moreover, the “valentine-shaped” heart is a well-known radiographic finding in HCM; however, it is not specific to the diagnosis of HCM. In a previous study, only 8% were diagnosed with HCM among the cats showing valentine-shaped hearts due to bi-atrial enlargement on radiographs.17 Thoracic radiography also has low sensitivity for the detection of mild cardiac disease.8,13,17

Meanwhile, if symptoms related to HCM occur, thoracic radiography can determine whether the respiratory signs are caused by CHF by comprehensively evaluating cardiomegaly, pulmonary vascular distention, and pulmonary edema or pleural effusion.11 In advanced HCM, the increase in the end-diastolic filling pressure and LA pressure develop and induces the CHF of pulmonary vessels.3,7 Finally, cardiogenic pulmonary edema or pleural effusion occurs.4,7 Therefore, pulmonary vascular changes can be detected on radiography in cats with L-CHF.11,13 A previous study revealed dilation of the pulmonary vein and artery dilation in approximately 50% and 70% of the cats, respectively, with L-CHF caused by various diseases including HCM, congenital cardiac defect, endocarditis, and anemia.13 Cats with HCM had larger diameters of the right cranial lobar vein (0.22 ± 0.04 cm) compared with those of normal cats (0.2 ± 0.03 cm).18 Therefore, comprehensive radiographic evaluation of the cardiac shape, pulmonary vessels, and lung infiltrates may help diagnose CHF in cats without marked cardiac enlargement and predict prognosis.6,11,13,16,17

In this study, the radiographic findings of the cardiac size and shape, pulmonary vascular changes, and presence of pulmonary edema and pleural effusion were assessed in cats with HCM. This study evaluated the clinical significance of these characteristics by comparing the HCM and healthy cats and additionally comparing the HCM cats between the presence and absence of CHF. We hypothesized that the cats with HCM would have larger hearts and LA compared with those of the healthy cats, and that, when CHF develops, the pulmonary veins will be dilated more than those in HCM cats without CHF and healthy cats. This study aimed to evaluate the clinical significance of thoracic radiography in HCM cats and identify the radiographic characteristics of the heart and pulmonary vessels to predict HCM and CHF in cats.

Methods

This study was a retrospective, original investigation that did not require institutional animal care and use committee or institutional review board approval.

Animals

This retrospective, comparative study enrolled cats that underwent thoracic radiography and echocardiography at the Chonnam National University Veterinary Teaching Hospital and Gwangju Sky Animal Medical Center from January 2019 to May 2021. The use of animal data in this study was approved by the hospital directors. Cats were only selected when right lateral and ventrodorsal (VD) views of thoracic radiography were obtained, without anesthesia, and the margins of the heart and pulmonary vessels were clearly visualized. Subsequently, the cats were classified into healthy cats, and HCM cats with and without CHF, by a veterinarian (S.Y.K) with 2 years of radiography experience by reviewing the medical records, radiography, and echocardiography. The inclusion criteria for the healthy cats were no evidence of cardiovascular diseases or abnormalities on echocardiography; no history or clinical signs of cardiovascular or respiratory diseases such as coughing, weakness, open-mouth breathing, or exercise intolerance; and no systemic disease that could affect the hemodynamic condition, such as anemia or infections. The cats with HCM were selected based on the following inclusion criteria: LV hypertrophy with the thickness of LVW and interventricular septum (IVS) over 6 mm from B-mode or M-mode on echocardiography; no underlying disease of secondary LV hypertrophy such as hypertension or hyperthyroidism; no evidence of other cardiac disease or concurrent diseases affecting the cardiovascular system. The cats with HCM were subclassified according to the presence of CHF. The HCM cats with CHF were determined when they presented evidence of pulmonary edema, pleural effusion, or severe tachypnea that showed a clear response to furosemide administration.

The medical records were reviewed for breed, age, sex, body weight, systolic blood pressure measured using a Doppler ultrasound flow detector, and clinical signs. Echocardiography was performed using a Prosound α7 (Hitach Aloka Medical) equipped with a 2.6 to 7.7 MHz phased array transducer probe without anesthesia by a diagnostic imaging professor with 20 years experience of in radiography and echocardiography (J.H.C.) and 2 PhD students (S.J.P., S.K.L.) majoring in veterinary radiology. The thickness of the IVS and LVW was measured on 2D images from the right parasternal long-axis and short-axis views during diastole. LV hypertrophy was defined when the end-diastolic thickness of the IVS or LVW was 6 mm or above. The left atrial-to-aortic root diameter ratio (LA:Ao) was measured on 2D images from the right parasternal short-axis view. From this plane, the LA:Ao was calculated as previously determined.7 The LA size was determined as normal if LA:Ao was ≤1.5 and enlarged if LA:Ao was >1.5.

Thoracic radiography

Radiographic images were obtained using a digital radiographic system (EVA-HF525, Gemss-Medical) using a maximum tube voltage of 125 kV, and a maximum tube current of 500 mA with a cesium-iodine based flat panel detector (FDX4343R, Gemss-Medical) integrated into the table. The radiographs were obtained by placing the cats directly on the table without the use of the grid. A focal film distance of 100 cm was used with an exposure factor ranging from 46–70 kVp, tube current of 300 mA, and exposure time of 0.01 seconds, depending on the size of the cat. Thoracic radiographs in the right lateral and VD views were taken during the full inspiratory phase.

All radiographs were sent to the workstation and assessed on picture archiving and communications systems (Infinitt PACS, Infinitt Healthcare) by a veterinarian (S.Y.K) with 2 years of radiology experience and another veterinarian (D.J.L.) with 1 year of radiology experience individually, under the supervision of a diagnostic imaging professor (J.H.C). Measurements were made using electronic calipers on a Digital Imaging and Communications in Medicine at the workstation. The radiographs were presented to the observers in a random order and assessment was performed in a blinded manner to the cat’s condition and the other’s result.

Image analysis

Radiographic characteristics including the cardiac size, LA, pulmonary vessels, and CHF are presented (Table 1). The cardiac size was measured by vertebral heart score (VHS) and determined as normal if the VHS measured was below 7.8.12 The VHS was measured in the right lateral thoracic radiograph. The long-axis (L) was drawn from the ventral border of the largest of the carina to the most ventral point of the cardiac apex. The short-axis (S) was measured from the caudal border of the cardiac silhouette at the dorsal aspect of the caudal vena cava (CVC) to the cranial border of the cardiac silhouette at the widest part, perpendicular to the L (Supplementary Figure S1). Two lines equal in length to the L and S, respectively, were drawn over the thoracic vertebrae, starting at the cranial border of the fourth thoracic vertebrae, parallel to the vertebral canal. The VHS was calculated as the sum of L and S in vertebral body units.

Table 1

Radiographic evaluation for cardiac size, left cardiac chamber enlargement, dilation of pulmonary vessels, and congestive heart failure.

Evaluation factors Radiographic characteristics Criteria
Cardiac size VHS < 7.8
LA enlargement VLAS
Elevation of the carina Presence or absence
LA bulging 0, Absent LA bulging and definite caudal curvature of the heart
1, Concave dorsocaudal border of the heart
2, Dorsal bulging of the LA above the carina
3, Dorsal bulging of the LA close to the thoracic vertebrae
LAu bulging 0, No bulging of LAu with straight left cardiac margin
1, Mild bulging of LAu with distortion of smooth margin of the heart
2, Moderate bulging of the LAu making distinct concavity
3, Severe bulging of the LAu which is close to left thoracic wall
Pulmonary vessels D-CrPA and D-CrPV Diameters of CrPA and CrPV at the level of the caudal margin of the fourth rib
D-CdPA and D-CdPV Diameters of CdPA and CdPV at the level of the caudal margin of the ninth rib
SD-CdPA and SD-CdPV Distal side of the summation shadow created by CdPA and CdPV with the ninth rib
SD/L-CdPA and SD/L-CdPV Ratio of distal to lateral side of summation shadow of CdPA and CdPV at the ninth rib
Ratio of the pulmonary artery to the accompanying vein in cranial and caudal lobes
Congestive heart failure Pulmonary edema or pleural effusion Presence or absence

CdPA = Caudal lobar pulmonary artery. CdPV = Caudal lobar pulmonary vein. CrPA = Cranial lobar pulmonary artery. CrPV = Cranial lobar pulmonary vein. D-CdPA = Diameter of the caudal lobar pulmonary artery. D-CdPV = Diameter of the caudal lobar pulmonary vein. D-CrPA = Diameter of the cranial lobar pulmonary artery. D-CrPV = Diameter of the cranial lobar pulmonary vein. LA = Left atrium. LAu = Left auricle. SD-CdPA = Distal side of the summated shadow made by the caudal lobar pulmonary artery with the rib. SD-CdPV = Distal side of the summated shadow made by the caudal lobar pulmonary vein with the rib. SD/L-CdPA = Ratio of distal to lateral sides of the summated shadow made by the caudal lobar pulmonary artery with the rib. SD/L-CdPV = Ratio of distal to lateral sides of the summated shadow made by the caudal lobar pulmonary artery with the rib. VHS = Vertebral heart score. VLAS = Vertebral left atrial size.

The assessment of LAE included vertebral left atrial size (VLAS), the elevation of the carina on the lateral view, the dorsal bulging of the LA on the lateral view, and the lateral bulging of left auricle (LAu). The measurement of VLAS was performed in the right lateral thoracic radiograph. A line was drawn from the center of the most ventral aspect of the carina to the caudal border of the LA, where it intersected with the dorsal border of the CVC (Supplementary Figure S2). The equal length of the line was repositioned over the thoracic vertebrae, caudal to the cranial border of the fourth thoracic vertebrae, parallel to the vertebral canal. The VLAS was described in vertebral body units.19 LAE was also evaluated qualitatively based on the elevation of the carina, LA bulging, and LAu bulging (Figure 1).

Figure 1
Figure 1

Thoracic radiography of cats used for grading and evaluation of left atrium (LA) enlargement. (A) The elevation of the carina was evaluated as (A-0) absence or (A-1) presence of the elevation on lateral views. (B) The bulging of LA was evaluated into 4 grades on the lateral view; 0 = absence of LA bulging and definite caudal curvature of the heart (B-0); 1 = concave caudodorsal border of the heart (B-1); 2 = dorsal bulging of the LA above the carina; and 3 = dorsal bulging of the LA close to the thoracic vertebrae (B-3). (C) Lateral bulging of the left auricle (LAu) was evaluated on ventrodorsal views and graded into 0 = no bulging of LAu with straight left cardiac margin (C-0); 1 = mild bulging of LAu with distortion of smooth margin of the heart (C-1); 2 = moderate bulging of the LAu making distinct concavity (C-2); and 3 = severe bulging of the LAu that is close to left thoracic wall (C-3).

Citation: American Journal of Veterinary Research 84, 9; 10.2460/ajvr.23.01.0017

The dilation of the pulmonary vessels was evaluated by measuring the following (Figure 2). On the lateral view, the diameters of the cranial lobar pulmonary artery (CrPA) and cranial lobar pulmonary vein (CrPV) were assessed at the level of the caudal margin of the fourth rib (R4) as D-CrPA and D-CrPV, respectively. The diameter of R4 was measured at the point just distal to the spine.20 On VD view, the caudal lobar pulmonary artery (CdPA) and pulmonary vein (CdPV) were measured from the left and right caudal lobes at the ninth rib (R9) by 2 methods. First, their diameters (D-CdPA, D-CdPV) were measured at the level of the caudal margin of the rib. Second, the distal side of the summation shadow created by each vessel with rib was measured as SD-CdPA and SD-CdPV, respectively. Additionally, the ratio of the distal to the lateral side of the summation shadow of each vessel (SD/L-CdPA, SD/L-CdPV) was obtained. Lastly, the ratio of the pulmonary artery (PA) to the accompanying vein was calculated on both cranial and caudal lobes (D-CrPA/PV, D-CdPA/PV).

Figure 2
Figure 2

Thoracic radiography. (A) Right lateral view illustrating the measuring methods for cranial lobar vessels. On a close-up of the right lateral radiograph, the diameter of the right cranial lobar artery (D-CrPA) and vein (D-CrPV) at the level of the caudal margin of the fourth rib (R4), and the R4 just distal to the spine were measured. (B) Ventrodoral views illustrating the measuring methods for caudal lobar vessels. A close-up of the ventrodorsal radiograph (C) showing the measurement of the diameter of the right caudal lobar artery (D-CdPA) and vein (D-CdPV) at the level of the ninth rib (R9). A close-up of the ventrodorsal radiograph (D) showing the measurement of the distal side (red line) of the summated shadow created by the caudal lobar artery (SD-CdPA) and vein (SD-CdPV) with the ninth rib (R9). Additionally, the lateral side (yellow line) of the summated shadow created by the caudal lobar artery (SL-CdPA) and vein (SL-CdPV) with the R9 were obtained. The ratio of distal to lateral sides of the summated shadow made by the caudal lobar pulmonary artery and vein with the R9 is measured as SD/L-CdPA and SD/L-CdPV, respectively.

Citation: American Journal of Veterinary Research 84, 9; 10.2460/ajvr.23.01.0017

Statistical analysis

Statistical analyses were performed by a statistician (J.Y.L) using commercially available software (SPSS, IBM SPSS Statistics 26, IBM Corp). The normality of the data was performed using all data by Kolmogorov-Smirnov tests. All data were expressed as means ± standard deviations, and a P value was < .05 was considered significant. The correlation between the clinical data and radiographic evaluation factors was analyzed using a Spearman and Pearson correlation analysis. The clinical data (breed, age, sex, body weight, and blood pressure), and echocardiographic and radiographic characteristics were assessed according to the presence of HCM and any CHF using the student t-test, Mann Whitney U-test, and Kruskal Wallis test depending on the normal distribution. The sensitivity, specificity, and positive and negative predictive values of radiography for LAE were assessed. The sensitivity, specificity, and positive and negative predictive values of VHS for CHF, and radiographic characteristics regarding LAE were assessed using echocardiographic LA/Ao > 1.5 as the reference standard. The receiver operating characteristic (ROC) curve analysis was conducted among the radiographic characteristics with significant differences according to the presence of HCM or CHF. From the radiographic characteristics that had an area under curve over 0.6 and a P value was < .05, the cut-off value was obtained as the value having the maximum sum of sensitivity and specificity. The agreement between 2 observers for the radiographic assessment was evaluated using the intraclass correlation coefficient test.

Results

A total of 111 cats who underwent radiography and echocardiography were selected in this retrospective study. Then, 33 cats were excluded from this study due to concurrent cardiac diseases (ventricular septal defect = 7, restrictive cardiomyopathy = 4, atrial septal defect = 1, patent ductus arteriosus = 1, mitral valve dysplasia = 1) and noncardiogenic causes. Finally, 78 cats were enrolled in this study including 35 healthy cats and 43 cats with HCM. Additionally, the HCM cats were subclassified into 21 and 22 cats with and without CHF, respectively.

The cat breeds included were Domestic shorthair (20), Persian (18), Scottish fold (9), Turkish Angora (8), Mixed breed (6), American shorthair (4), British shorthair cats (3), Siamese (3), Bengal (2), Norwegian forest (2), Munchkin (1), Ragdoll (1), and Exotic shorthair cats (1). The mean age was 4.64 ± 3.29 years (range = 4 months to 12 years) and the mean body weight was 4.5 ± 1.6 kg (range = 1.8 to 11.5 kg). They comprised intact males (n = 5), neutered males (n = 41), and spayed females (n = 32). The mean systolic blood pressure was 130.5 ± 22.8 mmHg (range = 80 to 190 mmHg). The mean age of healthy cats was 4.39 ± 3.53 years. This group consisted of intact males (n = 3), neutered males (n = 14), and spayed females (n = 18). In HCM cats, the mean age was 4.85 ± 3.11 years and consisted of intact males (n = 2), neutered males (n = 27), and spayed females (n = 14). The body weight of healthy cats and HCM cats were 4.12 ± 1.27 kg and 4.82 ± 1.81 kg, respectively. The systolic blood pressure was 136.52 ± 21.30 mmHg in healthy cats and 126.26 ± 23.15 mmHg in HCM cats. There was no significant difference in clinical data including age, sex, body weight, and blood pressure in healthy cats and HCM cats.

The cardiac size and LAEs were assessed successfully in all cats except 1 owing to sternal vertebral deformities and deviation of the heart due to collapse of the left cranial lung lobe. The cardiac size assessed using VHS was significantly larger in HCM cats (8.57 ± 0.74) compared with healthy cats (7.57 ± 0.46; P < .001). However, in HCM cats, there was no significant difference in VHS between cats with CHF (8.47 ± 0.75); and without CHF (8.03 ± 0.68; P = .058). In cats with HCM, the sensitivity, specificity, and positive and negative predictive values of VHS for CHF were 76.19%, 40.91%, 55.17%, and 64.29%, respectively.

The radiographic characteristics regarding the enlargement of LA including elevation of the carina and LA bulging, and LAu bulging had a strong significant positive correlation with LA:Ao ratio. The bulging of LA and LAu was significantly higher in HCM cats (0.50 ± 0.83 and 1.56 ± 1.03) than in healthy cats (0.06 ± 0.24 and 0.69 ± 0.68), respectively. In addition, both were significantly higher in HCM cats with CHF (0.81 ± 0.98 and 1.95 ± 0.86) compared with those without CHF (0.19 ± 0.51 and 1.15 ± 1.04), respectively. Meanwhile, VLAS exhibited no significant difference between healthy cats (1.70 ± 0.21) and HCM cats (1.79 ± 0.33), and between HCM cats with (1.86 ± 0.39) and without (1.71 ± 0.24) CHF. The LA:Ao of HCM cats (1.95 ± 0.65) was significantly larger than for healthy cats (1.43 ± 0.26) (P < .001). Moreover, in HCM cats, LA:Ao was significantly larger when CHF was present (HCM cats with CHF, 1.95 ± 0.65; without CHF, 1.43 ± 0.26; P = .012). On echocardiography, LAE was determined in 40 cats with the criteria of LA:Ao > 1.5. The positive predictive value, negative predictive value, sensitivity, and specificity of radiographic characteristics for detecting LAE on echocardiography are presented (Table 2). The bulging of LAu had the highest sensitivity and the elevation of the carina had the highest specificity for detecting LAE on echocardiography.

Table 2

Positive predictive value, negative predictive value, sensitivity, and specificity of the radiographic characteristics for diagnosis of left atrial enlargement using LA:Ao on echocardiography as the criterion.

Radiographic characteristics Positive predictive value (%) Negative predictive value (%) Sensitivity (%) [range] Specificity (%) [range]
Elevation of the carina 77.78 49.23 17.50 [7.34–32.78] 94.12 [80.32–99.28]
LA bulging 62.50 48.26 25 [12.70–41.20] 82.35 [65.47–93.24]
LAu bulging 62.75 28.18 82.05 [66.47–92.47] 44.12 [27.19–62.11]

See Table 1 for key.

In each cat, the pulmonary vessels were measured 19 radiographic characteristics are presented (Tables 3 and 4). On radiography, the pulmonary vessels from the cranial lung lobes were visible on the lateral view for all cats. A few of the pulmonary arteries and veins of the caudal lung lobe were not visualized on the VD view owing to partial to complete superimposition with the CVC, cardiac silhouette, vertebral body, and lung infiltration. In particular, left D-CdPA/PV was measured in only 30% of cats.

Table 3

Radiographic characteristics regarding pulmonary vessels in healthy cats and cats with hypertrophic cardiomyopathy (HCM).

Measuring site Radiographic characteristics Healthy cats (n = 35) HCM cats (n = 43) P value
Cranial pulmonary vessel measured at R4 D-CrPA 2.17 ± 0.55 1.95 ± 0.50 .062
D-CrPV 2.09 ± 0.47 1.92 ± 0.49 .144
D-CrPA/PV 1.04 ± 0.14 1.03 ± 0.19 .739
D-CrPA/R4 0.74 ± 0.21 0.62 ± 0.18 .011
D-CrPV/R4 0.71 ± 0.19 0.62 ± 0.17 .019
Caudal pulmonary vessel measured at R9 Right D-CdPA 3.58 ± 0.76 4.14 ± 1.32 .023
Right SD-CdPA 4.95 ± 1.41 5.36 ± 1.69 .255
Right SD/L-CdPA 1.71 ± 0.31 1.97 ± 0.71 .051
Right D-CdPV 3.47 ± 1.02 4.27 ± 1.05 .039
Right SD-CdPV 4.33 ± 1.16 5.11 ± 1.32 .091
Right SD/L-CdPV 1.58 ± 0.36 1.86 ± 0.62 .134
Left D-CdPA 3.69 ± 0.91 4.28 ± 1.29 .023
Left SD-CdPA 4.92 ± 1.47 5.43 ± 1.73 .178
Left SD/L-CdPA 1.82 ± 0.42 1.86 ± 0.64 .757
Left D-CdPV 4.07 ± 1.31 5.68 ± 2.80 .069
Left SD-CdPV 4.91 ± 1.55 6.09 ± 1.61 .077
Left SD/L-CdPV 1.87 ± 0.75 2.05 ± 0.62 .527
Right D-CdPA/PV 0.98 ± 0.24 0.99 ± 0.27 .983
Left D-CdPA/PV 0.95 ± 0.32 0.90 ± 0.33 .685

D-CdPA/PV = Ratio of the diameter of caudal lobar pulmonary artery to vein. D-CrPA/PV = Ratio of the diameter of caudal lobar pulmonary artery to vein. R4 = The fourth rib. R9 = The ninth rib. See Tables 1 and 2 for the remainder of the key.

The unit of D-CrPA, D-CrPV, D-CdPA, SD-CdPA, D-CdPV, SD-CdPV is millimeter.

Table 4

Radiographic characteristics regarding pulmonary vessels according to the presence of congestive heart failure (CHF) in cats with HCM

Measuring sites Radiographic characteristics HCM cats without CHF (n = 22) HCM cats with CHF (n = 21) P value
Cranial pulmonary vessel measured at R4 D-CrPA 1.82 ± 0.34 2.08 ± 0.61 .096
D-CrPV 1.74 ± 0.41 2.12 ± 0.49 .008
D-CrPA/PV 1.08 ± 0.18 0.98 ± 0.18 .103
D-CrPA/R4 0.57 ± 0.12 0.68 ± 0.22 .061
D-CrPV/R4 0.54 ± 0.13 0.69 ± 0.17 .004
Caudal pulmonary vessel measured at R9 Right D-CdPA 3.78 ± 0.79 4.54 ± 1.65 .060
Right SD-CdPA 5.01 ± 1.09 5.76 ± 2.14 .154
Right SD/L-CdPA 1.77 ± 0.48 2.19 ± 0.86 .056
Right D-CdPV 3.69 ± 0.64 4.51 ± 1.12 .153
Right SD-CdPV 4.11 ± 0.71 5.52 ± 1.31 .013
Right SD/L-CdPV 1.61 ± 0.48 1.97 ± 0.66 .298
Left D-CdPA 4.18 ± 1.40 4.38 ± 1.18 .618
Left SD-CdPA 5.41 ± 1.84 5.45 ± 1.66 .942
Left SD/L-CdPA 1.76 ± 0.74 1.96 ± 0.52 .320
Left D-CdPV 6.07 ± 3.64 5.22 ± 1.58 .640
Left SD-CdPV 6.05 ± 1.57 6.14 ± 1.85 .927
Left SD/L-CdPV 1.72 ± 0.35 2.44 ± 0.68 .077
Right D-CdPA/PV 1.07 ± 0.29 0.95 ± 0.26 .433
Left D-CdPA/PV 0.95 ± 0.39 0.84 ± 0.29 .623

See Tables 1 and 2 for the key.

The unit of D-CrPA, D-CrPV, D-CdPA, SD-CdPA, D-CdPV, SD-CdPV is millimeter.

The ROC curve analysis was performed to define a cut-off to detect the development of CHF in HCM cats using the right SD-CdPV because it showed a significant difference according to the presence of congestion in HCM cats. The right SD-CdPV of 5.35 mm and the area under the curve of 0.867 had 75% sensitivity and 100% specificity, 1.00 positive predictive value, and 0.625 negative predictive value.

All radiographic characteristics had a good-to-excellent agreement between the 2 observers (Table 5).

Table 5

Interobserver intraclass correlation coefficient for radiographic characteristics

Measuring site Radiographic characteristics ICC 95% CI
Cranial pulmonary vessel measured at R4 D-CrPA 0.969 [0.951, 0.980]
D-CrPV 0.954 [0.928, 0.971]
D-CrPA/R4 0.898 [0.840, 0.935]
D-CrPV/R4 0.896 [0.786, 0.935]
Caudal pulmonary vessel measured at R9 Right D-CdPA 0.982 [0.972, 0.989]
Right SD-CdPA 0.967 [0.948, 0.979]
Right SD/L-CdPA 0.937 [0.784, 0.972]
Right D-CdPV 0.995 [0.990, 0.998]
Right SD-CdPV 0.993 [0.986, 0.997]
Right SD/L-CdPV 0.901 [0.790, 0.953]
Left D-CdPA 0.990 [0.984, 0.994]
Left SD-CdPA 0.933 [0.895, 0.958]
Left SD/L-CdPA 0.910 [0.757, 0.957]
Left D-CdPV 0.996 [0.991, 0.998]
Left SD-CdPV 0.987 [0.971, 0.994]
Left SD/L-CdPV 0.903 [0.623, 0.965]
Position of the heart and the left atrium VHS 0.779 [0.684, 0.872]
VLAS 0.922 [0.878, 0.951]
Elevation of the carina 0.786 [0.665, 0.863]
Dorsal bulging of LA 0.933 [0.895, 0.957]
Lateral bulging of LA 0.979 [0.967, 0.987]

ICC = Intraclass correlation coefficient. See Tables 1 and 2 for the remainder of the key.

Discussion

This study was conducted to evaluate whether the radiographic characteristics of the heart and pulmonary vessels can detect HCM in cats and predict the development of CHF. Cardiomegaly, LAE, and dilation of the D-CdPA were found compared with those in healthy cats. The LAE could be predicted using the elevation of the carina. In HCM cats with CHF, LAE and the right SD-CdPV were significantly larger compared with those without CHF. The observation that the larger VHS, LA bulging, and LAu bulging was found in HCM cats, when compared with healthy cats, is consistent with the hypothesis. In addition, HCM cats with CHF had larger the D-CrPV/R4 and the right SD-CdPV compared with those in HCM cats without CHF support the hypothesis that pulmonary veins will be more dilated when CHF develops.

The cardiac size was evaluated by measuring the VHS on thoracic radiography. In normal cats, VHS was 7.57 ± 0.46 in our study, which was similar to previous studies.21,22 Additionally, cardiac size was significantly larger in HCM cats than in healthy cats; however, there was no significant difference in VHS according to the presence of CHF in our study. The change in the cardiac size according to CHF has been controversial in previous studies.13,15 In 23 cats with various myocardial diseases, VHS was larger than the upper limit of normal range in all cats with cardiogenic pulmonary edema.15 However, in another study of 100 cats with acute L-CHF, the VHS was within the normal range even in cats with HCM sufficiently severe to cause CHF.13 Similarly, in our study, 7 cats showed normal VHS among the 21 HCM cats with CHF.

The valentine-shaped heart is a well-known radiographic feature of HCM owing to the enlargement of the LAE.3,11,16 However, the false-positive rate was reported in 7% of cats with valentine-shaped hearts. Moreover, among the cats with valentine-shaped hearts due to biatrial enlargement, only 8% were diagnosed as having HCM.17 Therefore, the elevation of the carina, LA bulging, and LAu bulging were assessed in our study to determine whether these radiographic characteristics can predict the LAE. The LAEs, evaluated by assessing the LA and LAu bulging, were significantly larger in HCM cats compared with those in healthy cats in our study. Additionally, these radiographic factors were larger when CHF was present. In 100 cats with acute L-CHF, 36 cats did not reveal LAE, when it was subjectively evaluated based on the presence or absence of the LAE.13 However, in our study, radiographic characteristics including the elevation of the carina, LA bulging, and LAu bulging had a strong positive correlation between LA:Ao on echocardiography. In particular, the elevation of the carina and LA bulging on the lateral view had high specificity, while LAu bulging had high sensitivity. Based on these findings, the elevation of the carina, LA bulging, and LAu bulging was considered to predict LAE in HCM cats on radiography.

The quantification of LA size was attempted using VLAS in our study, which is used in dogs for assessing LA size.19,23 There was no significant difference in the VLAS regardless of the presence of HCM or CHF in our study. Our VLAS result could not be compared with those reported in previous studies, because based on our literature review, this is the first study to apply VLAS to the assessment of LA size in cats. Meanwhile, the “LA-VHS,” a modified VHS system, has been applied to the assessment of LAE in normal cats, in those with HCM cats, and in those with restrictive cardiomyopathy.24 LA-VHS was measured from the right lateral thoracic radiograph by calculating the perpendicular distance between a line drawn from the cardiac apex to the ventral border of the left mainstem bronchus and the caudal contour of the LA wall just dorsal to the border of the CVC. In the study, the LA-VHS score was significantly higher in LAE, determined via echocardiography compared with normal LA with high specificity (95%); however, low sensitivity (28%).24 However, LA-VHS was not applied to evaluate the LAE in our study because we considered VLAS would better reflect the LAE than LA-VHS since alteration of LA appeared more prominent in the transverse than in the sagittal plane to the vertebral body. VLAS is a quantitative method using the measurement of the most ventral aspect of the carina to the most caudal aspect of the LA where it intersects with the dorsal border of the CVC, which is divided by the length of the fourth thoracic vertebra. Thus, VLAS can reflect the transverse alteration of the LA better than the LA-VHS. Compared with canine studies regarding the changes in the pulmonary circulation in heart diseases such as mitral regurgitation and heartworm, the quantitative data on pulmonary vessels in cats is limited.15,18,26 A study presented that the measurement of the caudal pulmonary vessels was challenging as there were enhanced chances of the overlapping of the vessels with adjacent structures.18 On thoracic radiography, the pulmonary vessels compared with the rib or the ratio between the PA and corresponding pulmonary vein (PV) are used for assessing the pulmonary circulation in heart diseases.18,25,26 In a study comprising 50 healthy cats, the D-CrPA/R4 and D-CrPV/R4 were 0.70 ± 0.13 and 0.69 ± 0.13, respectively, which is similar to our study, although the measuring site of the vessels was different; at the proximal third of the R4 in the study and the R4 just distal to the spine in our study.18 Meanwhile, the D-CdPA of healthy cats in our study was slightly larger than the result of the previous study, 3.07 ± 0.47 mm and 2.95 ± 0.48 mm in the right and left caudal lobes, respectively.26

In HCM cats, hypertrophic changes of the myocardium may lead to diastolic dysfunction, LVOT obstruction by systolic anterior motion, and increased diastolic filling pressure, resulting in increased LA pressure. When the LA pressure is elevated, PV congestion occurs. Along with these changes, pulmonary hypertension may develop causing PA dilation.15 When the radiographic characteristics regarding cranial pulmonary vessels were compared between 50 normal cats and 35 cats with HCM, D-CrPA/R4, and D-CrPV/R4 were not significantly different in the previous study.18 In our study, D-CrPA/R4 and D-CrPV/R4 were even smaller in HCM cats compared with healthy cats. Although elucidating the definitive cause of this finding is challenging, we considered that the radiographic characteristics related to the cranial pulmonary vessels were not useful for detecting HCM in cats, based on a canine study suggesting that the cranial pulmonary vessels cannot reflect congestive changes in mitral regurgitation.25

Considering the caudal lobar vessels, radiographic characteristics related to the PA including the right and left D-CdPA had significant differences between HCM cats and healthy cats. In a previous study about radiographic and echocardiographic assessment of LA size in 100 cats with acute L-CHF, the lobar PA dimension on radiography was larger than those of the accompanying PV in 65 cats and the authors suspected that in those cats may have developed postcapillary or mixed pulmonary arterial hypertension, which could have increased the size of the PA branches.13 However, they did not present the estimated PA pressure that could support their speculation. In our study, the PA measurement was also significantly larger in HCM cats compared with healthy cats. However, we find no reasonable evidence to explain this change in our study. Meanwhile, a significant difference according to the presence of CHF in HCM cats was demonstrated in the radiographic characteristics related to the PV but not the PA. This result may be caused by increased LA pressure in CHF, which causes the congestion and dilation of the PV. In our study, when CHF was present, the right SD-CdPV was significantly larger than HCM cats without CHF. Based on the ROC analysis, when the cut-off value was set as 5.35 mm, the right SD-CdPV level had the best combined 75% sensitivity and 100% specificity to distinguish the presence of CHF in HCM cats. Similarly, in cats with cardiogenic pulmonary edema, most cats had PV dilation with or without PA dilation.15 The measurement of SD-CdPV was performed only in 40% of HCM cats as the vessel was summated with adjacent structures such as CVC, vertebral body, or infiltration suggesting that the clinical usefulness of the measurement of SD-CdPV may be limited. However, CHF in HCM cats had the clinical significance of the increased risk of cardiac death and shorter mean survival time.4,6 Therefore, the measurement of SD-CdPV would be useful for predicting CHF in HCM cats even though it is not easily measured. Moreover, the measurement of SD-CdPV would be useful for differentiating the pulmonary infiltrate caused by CHF in HCM cats from primary pulmonary disease. In HCM cats, it is important to distinguish cardiogenic pulmonary edema from pulmonary distress that is very common. Based on the findings in this study, when a patient displays LAE and PV dilation, CHF caused by HCM is suspected as a cause. On the other hand, when a PA dilation is prominent, the radiographic changes are more likely due to pulmonary disease.26

This study has some limitations. First, this study was performed on a small number of cats with HCM. Second, the timing of radiographs in reference to furosemide administration varied between cases. The administration of diuretics may affect the radiographic findings in some cats by decreasing preload and LV filling pressure. In human studies, the D-CdPV and LA size showed a significant decrease because of 4 months of diuretic therapy for CHF.27 Further investigation of the radiographic changes in response to diuretic therapy is needed. Finally, the cranial lobar vessels were evaluated on the right lateral view of thoracic radiography because of the retrospective study nature and in this view, blood vessels of both left and right cranial lobes may appear overlapped. In conclusion, this study evaluated the clinical significance of thoracic radiography regarding cardiac size, LA size, and the pulmonary vessels in cats with HCM. In cats with HCM, cardiomegaly, LAE, and dilation of the CdPA were found compared with healthy cats. When CHF developed, LAE and CdPV dilation were additionally found compared with the HCM cats without CHF. In particular, the elevation of the carina and the right SD-CdPV using a cut-off of 5.35 mm were determined as the specific radiographic factors for detecting LAE and CHF, respectively. Although there was an overlapping of radiographic findings between healthy and HCM cats, radiographic assessment of LAE can be useful for predicting HCM and the right SD-CdPV with R9 can predict CHF in HCM cats.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org.

Acknowledgments

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science, ICT, and Future Planning (NRF-2021R1A2C200573011).

The authors have no relevant financial interest, arrangement, or affiliation with any company or organization.

The authors declare that there were no conflicts of interest.

The authors appreciate the contribution of Jeongyong Lee to the statistical analysis.

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