AORTIC AND CARDIAC MINERALIZATION IN THE DOG

AORTIC AND CARDIAC MINERALIZATION IN THE DOG

TOBIAS SCHWARZ, MA, DR. MED. VET., MARTIN SULLIVAN, BVMS, PHD, CHRISTOPH K. STORK, DR. MED. VET., RUTH WILLIS, BVM&S, Ross HARLEY, BVM&S, MSc, DOMINIC J. MELLOR, BVMS, PHD

Aortic and cardiac mineralization was found in 21 of 3443 (0.61%) canine thoracic radiographs. In none of 786 feline thoracic radiographs reviewed were such lesions present. Mineralizations were superimposed on the ascending aorta (19 dogs) or on the caudal cardiac silhouette (2 dogs). In 2 of 4 dogs mineralization was identified echocardiographically dorsal to the aortic valve in close proximity to coronary arteries. Computed tomography confirmed mineralization of the aortic arch and root in 2 of 2 dogs. Necropsy and histopathologic examination in 1 dog revealed multiple nodular aortic tunica media calcifications with adjacent areas of degeneration. Lesions were significantly overrepresented in older dogs and in Rottweilers, and regarded as dystrophic calcification, caused either by age-related degenerative changes or chronic disease-related processes. There was no evidence of clinical significance attributed to the mineralization in any dog. Aortic and cardiac mineralization should be recognized as an incidental, non-significant finding in dogs of advanced age and differentiated from pleural and pulmonary structures. Veterinary Radiology & Ultrasound, Vol. 43, No. 5, 2002, pp 419427.

Key words: canine, cardiac mineralization, aortic calcification, conventional radiography, echocardi- ography, computed tomography, coronary arteries, aorta, cardiac fibroskeleton, Rottweiler.

Introduction

ORTIC OR CARDIAC mineralization is rarely reported in A dogs and cats.’32 In contrast to larger animals, where heterotopic cardiac ossification centres exist (ossa cordis in bovines), the canine and feline heart and aorta are soft tissue structures. Therefore, if mineralizations are visible on radiographs, they raise the question of clinical significance. After we initially found linear mineral opacities within the cardiac and aortic silhouette on lateral radiographs in three dogs with histopathologic confirmation in one dog, a retrospective study was undertaken to investigate the prevalence and significance of such lesions in dogs and cats.

Materials and Methods

The radiographic files of 3443 dogs and 786 cats admitted to Glasgow University Veterinary School with thoracic radiographs were reviewed by three examiners in a consen-

From the Department of Veterinary Clinical Studies, University of Glas- gow, Bearsden Road, Glasgow G61 lQH, Scotland, the Service de Chiru- rgie des Petits Animaux, UniversitC de Lihge, Boulevard de Colonster 20 - B44, B-4000 Likge, Belgium (Stork) and the Department of Clinical Veterinary Medicine, University of Cambridge, Madingley Road, Cam- bridge CB3 OES England, UK (Harley).

This work was submitted as part of the requirements for the RCVS Diploma in Veterinary Radiology of Dr. Schwarz in 2000.

Address correspondence and reprint requests to Dr. Schwarz, Depart- ment of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, 3850 Spruce St., Philadelphia, PA 19104, USA.

Received April 9, 2001; accepted for publication January 10, 2002.

sus mode for the presence of mineralization within the cardiac and thoracic aortic silhouettes. These files included all available canine and feline patients with lateral thoracic radiographs made between 1989 and 2000, except patients in which the cardiac silhouette was obliterated by other intrathoracic structures (pleural effusion, diaphragmatic rupture, extensive alveolar lung pattern, large intrathoracic masses) or in which the cardiac shadow included an en- larged pericardial space (pericardial effusion, peritoneo- pericardial hernia) or was not visible due to poor radiographic technique. Breed, sex, and age at the time of radiography were recorded to characterize the study population.

Aortic and cardiac mineralization was assumed if mineral opacities were superimposed on the heart and thoracic aorta on lateral radiographs and differed in orientation from bronchial and pulmonary vascular structures. The radiographic opacity of cardiovascular mineralization was subjectively graded as mild, moderate or marked by three reviewers (Schwarz, Sullivan, Stork) in a consensus mode. Similarly, the texture of the mineralization was assessed as homogenous or irregular.

In this study the term “cardiac” includes all structures within the confines of the radiographic cardiac silhouette with the exception of the ascending aorta. Where available, dorsoventral (DV) or ventrodorsal (VD) radiographs were used to confirm the cardiadaortic location. Bronchial and pulmonary mineralization was also noted in affected animals and graded as absent, mild or marked by all three reviewers in a consensus mode. The term “pulmonary” used

419

420 SCHWARZ ET AL. 2002

here included nodular mineralized pleural and true pulmonary lesions, as they are both radiographically indistinguish- able.3

Lesions were characterised according to their anatomic location using the cardiac long axis on lateral radiograph^.^ The extent of lesions was compared to the tracheal diameter at the level of the fourth ribs, with those smaller or equal to this diameter being classified as short lesions, and those longer as elongated lesions. In branching lesions, the long- est continuous branch was used for assessment of extent. The continuity of the intrathoracic tracheal diameter was assessed to rule out tracheal collapse, which could have hampered lesion assessment. Cardiac angiography radiographs from dogs not included in the study were used to clarify the canine cardiac and aortic radiographic anatomy (Fig. 1).

A full echocardiographic examination was performed in 4 dogs. In all 4 dogs, the echocardiographic exam was either performed after the detection of mineralization on radio-

graphs, or it was repeated with the particular focus on the detection of these lesions. Standard echocardiographic assessment included left and right parasternal short and long axis views in B-mode, M-mode and pulsed Doppler tech- niques.

Computed tomography (CT) was performed in two dogs using a third generation axial CT unit* with a slice width and interval of 2.5 mm. To reduce cardiac motion artifacts, acquisition times of 0.5s and 1.1 s were used. Post-contrast images were acquired 20 seconds after rapid manual intra- venous injection of 1 ml sodium iothalamatelkg body weight.? Images were reviewed using different mediastinal windows (center 40 Hounsfield units [HU], width 400 HU; center 00 HU, width 800 HU) with slight adjustments to emphasize visualization of particular structures and contrast medium uptake. Reconstructed and three-dimensional images were used to confirm the exact location and spatial dimension of lesions.

The medical history of all dogs with evidence of aortic and cardiac mineralization was reviewed. Particular atten- tion was paid to possible links to cardiovascular and renal disease, disturbances of fat, calcium and phosphorus metabolism, and hypothyroidism.

Statistical analysis was performed using two professional software programs.$ The study population consisted of the 3443 dogs investigated. The 21 dogs with cardiadaortic mineralization formed the case group. Using a random number generator, a random sample of 84 animals was selected to form a control group from the unaffected reference population (3422 dogs) giving a case: control ratio of 1:4. The control group was representative of the unaffected reference population for the parameters analyzed in this study. Case and control groups were compared on the basis of age, breed and sex using the two-sample t-test, chi-square and Fisher’s exact test as appropriate. Only the Rottweiler and Retriever breeds had enough individuals in the case group to be analysed statistically. The Labrador Retriever, Golden Retriever and Black Labrador breeds were merged into the category of “Retriever breeds,” because reliable distinction between them was impossible with available data. For the same rea- son, intact and neutered dogs were also merged into one gender group.

Necropsy and microscopic examination was carried out in one dog. This dog was admitted to Cambridge University Veterinary School. As it belonged to a different reference population, which was not assessed here, this dog was not included into statistical analysis and is reported separately.

FIG. 1. Lateral aortogram in a dog with a patent ductus arteriosus (p) The following anatomic landmarks are visible: Aortic valve, left and righl coronary arteries arising from the sinuses of Valsalva (arrowheads), ascending aorta, descending aorta with the branching brachiocephalic trunk (b) and left subclavian artery (c).

*Exel 2400 elite@, Elscint Ltd, Haifa, Israel. ?Conray 4200,420 mg iodindml, Mallinckrodt Medical Ltd, Northamp-

+Minitab v. 12.00, Minitab statistical software Inc., State College, USA; ton, UK.

SYSTAT 8.0.m. SPSS lnc., Chicago, USA.

VOL. 43. No. 5

Results

AORTIC AND CARDIAC MINERALIZATION IN THE Doc 42 1

Evidence of cardiac mineralization was found in 21 dogs (0.61% of the study population) and none of the 786 cats. The mean k standard deviation (SD) age of the case population was 9.5 & 3.9 years (range 1.5-16.5 years) and was significantly ( P = 0.001) greater than that of the control group (mean k SD age: 6.5 k 4.0 years, range: 0.2-14.0 years). There was no significant difference in the proportion of male and female animals between the case and the control group. In terms of breed, there were 5 Rottweilers in the case population and only 2 in the control group. Using Fisher’s exact test this difference was significant ( P =

0.003). There was no significant difference in the proportion of Retriever breeds dogs between the case and the control group. Dogs of other individual breeds in the case group were too few to be compared statistically with the control group.

According to location, lesions could be divided into those located cranial (1 9 dogs) or caudal to the cardiac long axis (2 dogs). The cranial lesions were all, at least in part, superimposed on the ascending aorta or the aortic valve. Eight of these dogs had elongated lesions superimposed on the ascending aorta with smaller fragmentary branches (Fig. 2). In one dog, a similar branching opacity could be seen in the proximal descending aorta and in the cranial mediastinum cranial to the aortic arch (Fig. 3 ) . Short lesions superimposed on the ascending aorta and the aortic valve were found in 1 1 dogs (Fig. 4). In 2 dogs, a linear mineral opacity with a dorsoventral orientation in a zigzag shape or as a short branching stripe was found caudal to the cardiac long axis. The degree of mineralization was generally marked in extensive lesions and mild in small lesions. In 15 dogs, the texture of the mineralization was irregular; in 6 dogs, it had a more homogenous appearance. The irregularity of mineralization manifested in a linear accumulation of small plaque-like structures, giving it an appearance of a stack of coins. Marked aortic or cardiac mineralization only occurred in dogs with elongated lesions. All dogs with lesions had bronchial mineralization and 5 dogs had nodular pulmonary mineralization.

VD or DV radiographs were available in 8 of the 2 1 dogs. The lesion was visible in only 2 dogs, and appeared as a curvilinear stripe superimposed on the aortic arch. In both, mineralization was marked and the lesion was not superimposed on the thoracic vertebrae or sternum, either due to an oblique projection or a shift of the cardiac silhouette due to lung lobe collapse (Fig. 5) .

By echocardiographic examination, mitral valve regurgitation and left atrial enlargement was found in a 13-year-old Cavalier King Charles spaniel and a patent ductus arteriosus with a left-to-right shunt in a 3.5-year-old dog. Cardiac function and morphology was normal in an 8.5-year-old

FIG. 2. A. Marked elongated irregular mineralization of the ascending aorta in an 8.5-year-old Rottweiler (arrow). B. Close-up. Note the texture resembling a stack of coins and the branching nature of the lesion.

Rottweiler and a 10-year-old Weimaraner. In the Cavalier King Charles spaniel with mitral valve disease and in the Rottweiler with normal cardiac function, marked acoustic shadowing and comet tail artifacts occurred at the aortic root from the coronary arteries in left and right parasternal short axis views (Fig. 6). Both artifacts originated from the proximity of these vessels and were repeatable as these vascular structures were followed. However, similar artifacts were not found further ventrally in the ventricular myocardium. In the other two dogs examined, no evidence of mineralization was found.

On computed tomography of the 8.5-year-old Rottweiler and the 3.5-year-old dog with the patent ductus arteriosus,


FIG. 4. Marked short homogenous curvilinear mineralization of the aortic bulb or the annulus of the aortic valve in a 12-year-old cross breed dog.

FIG. 3. Marked elongated homogenous mineralization of the ascending aorta in a 12-year-old Retriever. Two additional mineralizations are superimposed on the proximal descending aorta and the craniodorsai mediasti- nuin (arrowheads).

irregular mineralization was seen encircling the ascending aorta in pre- and post-contrast images. This mineralization was associated with streak artefacts. In the 8.5-year-old Rot- tweiler, this lesion extended into the branches of the left subclavian artery brachiocephalic trunk, aortic root and the proximal part of the descending aorta (Fig. 7). No evidence of mineralization was found in ventricular soft tissue structures in either dog.

Dogs in this study underwent thoracic radiography as part of an oncologic, cardiologic, medical, neurologic or ortho- paedic work-up or a combination of those. Due to the lack of consistent historical or clinical association with the lesions, medical historical data were not analysed statistically. Thyroid function was investigated in three dogs. Only one dog was hypothyroid and treated as such, one further dog had high cholesterol levels and tested positive for thyro- globulin autoantibodies which are a marker of thyroiditis, suggesting a risk of becoming hypothyroid in the future. Cholesterol levels were high or borderline high in three other dogs, suggestive of abnormal lipid metabolism. Serum calcium and phosphorus levels were within normal limits for all affected dogs. There was no history of renal disease

in any affected dog. Evidence of cardiovascular disease was found in 4 dogs. In 2 dogs, moderate mitral valve disease was found, of which one died eventually. No further work- up was done in one dog with premature ventricular com- plexes on ECG and the 3.5-year-old dog with a patent ductus arteriosus, but without clinical signs.

A 6-year-old German shepherd dog admitted to Cam- bridge Veterinary School was treated for severe broncho- pneumonia and severe cellulitis of the neck and had a moderately mineralized elongated irregular lesion superimposed on the ascending aorta. Unfortunately, the animal failed to respond to treatment and died. At necropsy, multifocal linear gritty protrusions were present in the wall of the root of the aorta dorsal to the aortic valve (Fig. 8). A focal gritty nodule was also noted in the wall of the root of the pulmonary artery. Microscopically, tissue sections from the aortic and pulmonary artery roots contained multifocal nodules within the tunica media, often extending into the tunica intima and adventitia. The nodules were comprised of areas of extensively calcified necrotic granular material and irregular fragments of bone (Fig. 9A). The tunica media sur- rounding and adjacent to the nodules had degenerative foci in the collagen connective tissue and calcification of the elastic sheets (Fig. 9B).

Discussion With a prevalence of 0.61% in the study population, aor-

tic and cardiac mineralizations are a relatively rare radio-

VOL. 43, No. 5 AORTIC AND CARDIAC MINERALIZATION I N THE DOG 423

FIG. 5. A. Dorsoventral view of a marked elongated aortic mineralization in a 14-year-old Miniature poodle in form of an inverse S-shaped opacity close to the lateral border of the aortic arch (arrowhead). The lesion is visible because the heart is shifted to the left due to lung collapse. B. Lateral view. Note the elongated homogenous branching nature of the lesion superimposed on the ascending aorta.

graphic finding in the dog. Evidence of these lesions being over-represented in older dogs suggests aortic and cardiac mineralizations are caused either by age-related degenerative changes or chronic disease processes that occur at advanced age. Overrepresentation of lesions in Rottweilers should be interpreted cautiously given the low number of affected dogs.

The fact that no lesions were detected in cats suggests that they are rare in this species. Radiographically evident cardiac and aortic mineralizations in cats have been reported only in single reports of patients with severe chronic renal failure, suspected systemic hypertension and severe chronic aortic and mitral valvular end~card i t i s . ' ,~ ,~ There is also a report of a cat with extensive aortic sclerosis and calcifica- t i o n ~ . ~

Based on canine angiographic anatomy and our findings, lesions located cranial to the cardiac long axis most likely represent mineralization in the ascending aorta. Some of these structures could also involve the right coronary artery and the cardiac fibroskeleton. The short curvilinear lesion at the level of the aortic valve most likely represents aortic root structures or annular calcification of the aortic valve ring. Lesions located caudal to the cardiac long-axis cannot be in the aorta. They probably represent altered segments of branches of the left coronary artery or parts of the cardiac fibroskeleton.

Cardiac and aortic mineralization has been reported as a post mortem finding in the dog.'-' ' Some veterinary pathology texts report calcification of the tunica media of the thoracic aorta and left atrium in dogs and associate it with degenerative changes of the elastic tissue, similar to degenerative processes in man.'" Ulcerative endocarditis in renal failure is also mentioned as a possible underlying pathology,9 which would not be consistent with the clinical history in any dog studied here. In one study of 40 hearts of large breed dogs, where death was unrelated to cardiovascular diseases, fibrosis, chondroid metaplasia and subsequent mineralization of the cardiac fibroskeleton and aortic root were consistently found." Such lesions were present in all 10 Doberman hearts examined. Rottweiler hearts were not investigated. Bone formation was found in 8 hearts. Changes occurred in dogs of all ages but the extent and degree was increased at advanced age. These degenerative changes were considered to be age-related and of no clinical significance. The necropsy and histopathologic findings in the dog investigated in our study were consistent with such changes. We could identify degenerative changes in the collagen connective tissues and calcification of the elastin sheets, and additional nodules of calcified material and ma- ture bone. We suspect these respective features represent progressive stages in the pathogenesis of the lesions. In a report of a dog with severe chronic mitral and tricuspid and


FIG. 7. Transverse non-contrast computed tomogram of the same dog as in Fig. 2 at the level of the 5"' thoracic vertebra. A soft-tissue window (center 00 HU, width 800 HU) enables identification of trachea (TRA), oesophagus (OES), cranial vena cava (CRVC), aortic bulb, descending aorta (DESC AORTA), main pulmonary artery (MPA) and right auricle (R AUR). Marked mineralization encircles the aortic bulb and descending aorta. Star-like streak artifacts (arrowhead) are due to movement blur and the intense minerali7ation.

FIG. 6. Right parasternal echocardiographic short axis view (A) and associated drawing ( B ) of the aortic bulb (Ao) and coronary arteries (arrowheads), main pulmonary artery (MPA), left atrium (LA) and right heart (RH) in a 13-year-old Cavalier King Charles spaniel. There is a comet tail artifact (c) arising from the aortic wall in the proximity of a coronary artery consistent with mineralization of a coronary artery or adjacent aortic wall.

mild aortic valvular disease, two annular, slightly constric- tive mineralizations of the proximal descending aorta were seen at necropsy and thought to represent mild aortic coarctation.' I The cranial lesions in our study were almost all superimposed on the ascending aorta. Necrosis of the elastic fibres in the aortic tunica media without mentioning of calcification has been reported in dogs as a frequent, age- related change with the potential to develop into a dissecting aortic aneurysm.'* In 2 dogs in another report, similar lesions with a suspected genetic background resulted in a rupture Of the aortic Dissecting aortic aneurysms are extremely rare in dogs and none of the dogs described here had evidence of that.I4,l5 Interestingly, endocardiosis, the most common cardiovascular disease in the dog, leads to a number of marked, gross pathologic and

and sudden FIG. 8. Post mortem photograph of the opened aortic valve and root of a 6-year-old German shepherd dog. Notice the multiple gritty pale protrusions dorsal to the aortic valve in a linear arrangement (arrows). Radio- graphically, the dog had a moderately mineralized elongated irregular lesion superimposed on the ascending aorta, A color version of this image is available at http://www.acvr.uddvis.edu/Journal/manuscripts/01_33.htmI

VOL. 43, No. 5 AORTIC AND CARDIAC MINERALIZATION IN THE DOG 425

histological changes of the valves, but calcification is not menti~ned.' , '" '~ Arteriosclerosis, a chronic arterial change consisting of hardening, loss of elasticity and luminal nar- rowing caused by proliferative and degenerative changes of the media and interna, is common in domestic animals but probably of little clinical importance,' although it recently has been associated with dilated cardiomyopathy and mitral valve regurgitation in dogs. '' Atherosclerosis, a specific form of arteriosclerosis in which degenerative fatty changes also occur, is the most common type in humans but rare in animals.9 Apart from several avian species,'y~20 the dog is the only domestic animal in which atherosclerosis occurs as a rare consequence of altered lipid metabolism caused by hypothyroidism"' or diabetes mellitus.Y.2s Microscopic evidence of mineralization of atherosclerotic plaques has

FIG. 9. A. Section of the aortic and pulmonic root from the same dog as in Fig. 8. The tunica intima (TI with arrowhead) of the pulmonic root is marked by an arrowhead. Notice foci of calcified material (arrows) and bone (arrowheads) within the tunica media (TM) of the common wall of the roots of the aorta and pulmonary artery. (H&E x 20). A color version of this image is available at http://www.acvr.uddvis.edu/ journal/manuscripts/O1-33.html B. Section of the aortic root from the same dog as in Fig. 8. There are disrupted calcified depos- its within a nodule (arrows) and calcification of the elastin sheets in areas of degeneration within the aortic tunica media (arrowheads and inset) (Von Kossa x 100; inset x 400). A color version of this image is available at http://www.acvr.udavis.edu/ journal/manuscripts/O I -33.html

been reported but is not a dominating feature as in

Radiographically, cardiovascular mineralization has been rarely reported in dogs. In one report, a mineralized aortic valve was described in a dog with confirmed aortic coarctation? In another report mineralization of iliac, femoral and renal arteries and the abdominal aorta was described in a dog with severe a r te r iosc le r~s is .~~ In a further dog, a faint, irregular mineralization with a patchy appearance and vaguely cylindrical shape was described in the caudal ret- roperitoneal space.2 The lesion represented a thrombotic caudal abdominal aorta with mineralized arteriosclerotic plaque lesions. Finally, short linear mineralizations of the proximal descending aorta are described in dogs with spirocercosis."

I ,2324


The medical history of affected dogs was not consistent with a clinical finding or disease that could be linked with cardiac and aortic mineralization, except in the dog with a patent ductus arteriosus and a curvilinear mineralization in the ascending aorta. Here, one could speculate about an association between both lesions. The retrospective nature of the study did not peimit us to fully evaluate the possible link between cardiovascular mineralization and atherosclerosis as a result of hypothyroidism. The clinical significance of these aortic and cardiac lesions appears to be low and unrelated to cardiovascular problems. Normal calcium and phosphorus serum levels and the focal nature of mineralization rules out metastatic mineralization.

The opacity of cardiac mineralization was most intense in older dogs with elongated lesions. The predominantly irregular texture of mineralization is in good agreement with our necropsy findings and the above-mentioned literature on such lesions, where they are described as an accumulation of gritty nodules. Together with the linear arrangement of all lesions, this supports the idea that such mineralizations represent a degeneration of elastic tissue, where necrotic changes occur at several points of maximal elastic stress but along the fibre orientation. The omnipresence of bronchial mineralization in this study was interpreted as a feature of the ageing dog.29 The fact, that 2 of the 4 dogs with marked cardiac mineralization also had marked pulmonary mineralization suggests these dogs have a greater tendency to- wards mineralization, due to either age or disease.

Mineralization that occurred in close proximity to the coronary sinuses and arteries was identifiable by echocar- diography in two of four dogs. We interpreted this initially as coronary artery mineralization.3o3’‘ However, due to the close proximity to the aortic bulb, these lesions may in fact represent aortic mineralization. This was suggested by the

CT examination in one of these dogs, where the mineralization was found in the aortic wall. To determine the in- volvement of the coronary arteries, coronary angiography, or an intravascular sonography would have been helpful, neither of which were available or clinically indicated.

Radiographic patterns of aortic and cardiac mineralization of dogs in this study most closely resembled aortic, annular and coronary patterns of cardiovascular calcification in man. Aortic calcification, particularly in the region of the arch, is almost ubiquitous in people over the age of 50 and is of no clinical significance.323” Aortic annular calcification is found in the valve rings of the cardiac fibroskeleton, and is regarded as an age-related degenerative pro- cess in man that may also extend into the ascending aorta, interventricular septum and the trigones of the cardiac fibroskeleton.’2,3’ Coronary artery calcification is regarded as an advanced stage of coronary arteriosclerosis in man and can be used to monitor the evolution of atherosclerotic plaques.’*

Results of this study suggest that aortic and cardiac mineralization in the dog is a relatively rare manifestation of chronic degenerative changes of the cardiovascular system without clinical significance. The time of onset of such changes may be beyond the life span of many dogs, which explains the low prevalence and late occurrence reported here. These often very obvious and potentially confusing radiographic features should be recognized as a non- significant, incidental finding in the ageing dog and differentiated from pleural and pulmonary lesions.

ACKNOWLEDGMENTS

We wish to thank Calum Paterson, Mala Renwick, Rachel Barrett, Frdser McConnell, Nicola Milne, Allan May, Drs. Paul Wotton and Christine Thomson for their support in carrying out this study. Tobias Schwarz’s diagnostic imaging residency was funded by BSAVA Petsavers.

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