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A Histological Study of the Cardiac Conduction System in a Heifer with Complete Atrioventricular Block
J. Comp. Path. 2005, Vol. 133, 68–72
SHORT PAPER
www.elsevier.com/locate/jcpa
A Histological Study of the Cardiac Conduction System in a Heifer with Complete Atrioventricular Block N. Machida, S. Katsuda*, Y. Kobayashi† and K. Mitsumori Department of Veterinary Pathology, Tokyo University of Agriculture and Technology, Faculty of Agriculture, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, *Department of Physiology, Fukushima Medical University School of Medicine, 1 Hikari-ga-oka, Fukushima 960-1295, and †Department of Pathological Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan
Summary A case of complete atrioventricular (AV) block of congenital origin in a 16-month-old Holstein heifer was studied histologically with serial sectioning of the cardiac conduction system. The heart was enlarged and showed moderate dilatation of the left and right ventricles. Histologically, the abnormally placed and poorly formed AV bundle was observed in association with abnormality in the tricuspid extension of the central fibrous body, suggesting that the pathological state of the AV bundle had been responsible for the complete AV block. This type of anatomical fault in the AV bundle is considered to be part of an embryological, developmental malformation of the central fibrous body. q 2005 Elsevier Ltd. All rights reserved. Keywords: atrioventricular block; cardiac conduction; cattle
Complete atrioventricular (AV) block occurs when no atrial activity is conducted to the ventricles and, therefore, the atria and ventricles are controlled by independent pacemakers (Olgin and Zipes, 2001). In human patients, such conduction disturbance may be due to congenital or acquired lesions; it may result from a block at the level of the AV node (usually congenital), within the AV bundle, or distal to the AV bundle in the Purkinje system (usually acquired) (Narula, 1980; Olgin and Zipes, 2001). Although complete AV block has been recorded in various animal species other than man, including cattle (Brooijmans, 1956; Tsuji et al., 1992), very few reports have included any morphological details of the cardiac conduction system; thus, only Liu et al. (1975), in a study in cats, examined systematically the relation between anatomical lesions and physiological events in the cardiac conduction system. The present report describes a serial section study of the conduction 0021-9975/$ - see front matter
doi:10.1016/j.jcpa.2004.12.004
system in a 16-month-old Holstein heifer with congenital complete AV block. The calf was born after an uneventful pregnancy and normal delivery, but it remained sedentary after birth. At the age of one month, a periodic physical examination revealed that it had an almost regular, but slow, pulse, but no detailed cardiological investigation was undertaken at that time. At the age of 13 months, the animal suffered a syncopal attack. An electrocardiogram revealed sinus rhythm with a rate of 120 beats/min and complete AV block with a ventricular escape rate of 30 beats/min (Fig. 1). Since its general condition was good, the animal was not considered to require any treatment. However, a further examination 3 months later revealed congestive heart failure with extensive subcutaneous and pulmonary oedema. Complete AV block, with an atrial rate of 110 to 130 beats/min and a ventricular rate of 20 to 35 beats/min, was still shown by electrocardiography. Multiple premature q 2005 Elsevier Ltd. All rights reserved.
Complete atrioventricular block in a heifer
69
Fig. 1. Electrocardiogram from heifer aged 13 months. A complete atrioventricular (AV) block with a ventricular escape rhythm (arrowheads) of 30 beats/min is demonstrated. The P waves (P) occur regularly at a rate of 120 beats/min. Base-apex lead, 25 mm/sec, 1 cm/mV.
ventricular contractions were also noted. Because of the poor prognosis, the animal was humanely killed. At necropsy, a considerable amount of strawcoloured fluid with a few, gelatinous, fibrin clots was seen in the thoracic and abdominal cavities. The pericardial sac was slightly thickened and contained about 1100 ml of yellowish serous fluid. The heart was enlarged with moderate dilatation of the left and right ventricles and endocardial thickening. The lungs were diffusely congested, oedematous and firm on palpation, and the trachea and bronchi contained a frothy fluid. The liver was moderately congested and enlarged, and the spleen slightly so. No other gross abnormalities were detected. Tissue samples from the lungs, thyroid glands, parathyroid glands, oesophagus, stomach, small and large intestines, pancreas, liver, mesenteric lymph nodes, spleen, adrenal glands, kidneys, urinary bladder, ovaries, uterus, brain, spinal cord and skin were fixed in 10% phosphate-buffered formalin, embedded in paraffin wax, sectioned at 5 mm, and stained with haematoxylin and eosin for light microscopy. A histological study of the cardiac conduction system was performed with the techniques described by James (1962, 1964, 1965). The regions of the sinoatrial (SA) node, the AV node, and the AV bundle and bundle branches were sectioned subserially at 3–5-mm intervals. Tissue blocks containing the AV node and bundle, which encompass the region from the posterior margin of the aorta back through the coronary sinus, were decalcified before microtome sectioning. After cutting screening sections 5 mm thick, serial sections of selected blocks were prepared, and every tenth section was mounted on a glass slide. The left and right ventricular free walls and the left atrium were cut into 72 blocks, and two sections were taken from each block.
The sections were alternately stained with Masson’s trichrome and elastica-van Gieson stains. The histopathological findings of the cardiac conduction system were as follows. The SA node and its approaches were intact and showed no changes. The AV node was normal in situation and size and the atrial muscle bundles were connected normally to it. The penetrating AV bundle was normal in location and size at its origin, but its proximal portion ran anteriorly, descending toward the tricuspid annulus, where it had come to lie on the right side of the ventricular septum (Fig. 2). The middle and distal portions of the penetrating AV bundle ran immediately beneath the endocardium just below the insertion of the base of the septal leaflet of the tricuspid valve (Fig. 3A). The middle portion was encased in dense fibrous tissue and its stem consisted at most of a few single-cell strands throughout its course; thus, continuity of the AV bundle was maintained only by “frayed strands” (Fig. 3B). This fibrous tissue involved the entire breadth of the penetrating AV bundle and was confined to it, the subjacent myocardium being normal. In the distal portion of the penetrating AV bundle, the narrow stem became thicker, though flattened in a vertical direction and smaller than normal, as it passed forward (Fig. 4A). Marked fibrous tissue was observed among the conducting fibres (Fig. 4B). In more anterior sections where the conal septal musculature appeared on the upper-left side of the summit of the main ventricular septal musculature, the terminal portion of the penetrating AV bundle expanded rapidly and bifurcated, giving rise to the left bundle branch (LBB) as a characteristic broad sheet and the right bundle branch (RBB) as a single discrete fascicle. The proximal portion of the LBB contained an abnormal amount of fibrous tissue and coursed to the left side, penetrating
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Fig 2. A,B. Heifer, heart, proximal portion of the penetrating AV bundle (AVB). The AV bundle is displaced to the right side of the ventricular septum (A). The outlined area in A is seen at higher magnification in B. CFB, central fibrous body; TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
between the conal septal and main ventricular septal musculature; the RBB proceeded forward and downward to enter the myocardium. When traced distally, the conducting fibres of the LBB were observed to be involved in the thick
endocardial fibroelastosis of the left ventricle. The RBB could not be followed more peripherally. Except in the region of the junction between the AV node and bundle, the tricuspid extension of the central fibrous body was abnormal. Far thicker
Fig 3. A,B. Heifer, heart, middle portion of the penetrating AV bundle (AVB). The right-sided AV bundle is attenuated and its narrow stem is encased in dense fibrous tissue (A). The outlined area in A is seen at higher magnification in B. TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
Complete atrioventricular block in a heifer
71
Fig 4. A,B. Heifer, heart, distal portion of the penetrating AV bundle (AVB). The narrow stem of the right-sided AV bundle becomes thicker, though flattened in a vertical direction and smaller than normal. The outlined area in A is seen at higher magnification in B. TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
strands of collagenous tissue than would be expected in the normal heart proceeded from the inferior tip of the os cordis toward the tricuspid annulus and involved the AV bundle in the dense fibrous environment (Figs 2–4). As a result, the AV bundle was displaced to the right side and its penetrating portion was attenuated. Endocardial fibroelastosis was diffuse in both ventricles, being more marked in the left. Focal fibrosis was present in some areas of the left ventricle and ventricular septum, with occasional infiltration of mononuclear inflammatory cells. Other significant histological changes were confined to the liver, spleen and lungs. The liver had centrilobular congestion with necrotic hepatocytes and dilatation of the lymphatics. In the spleen, vascular congestion and expansion of the red pulp were present, and the lungs showed marked alveolar oedema with numerous macrophages containing erythrocytes or haemosiderin. The remaining organs were normal. Histological study in the present case revealed an abnormally placed and poorly formed AV bundle, considered to have been the likely anatomical basis for the complete AV block. Although this case was not electrocardiographically documented as complete AV block until the heifer was 13 months old, it may represent an example of congenital AV block because the heifer had a slow pulse as early as one month of age and histological examination
revealed an unusual type of AV bundle defect. Similar lesions of the AV bundle have been documented in human cases of congenital complete AV block and it has been suggested that these were responsible for the conduction disturbance (Lev et al., 1971; James et al., 1976) There are three morphological types of congenital AV block in man, namely, (1) lack of connection between the atria and the peripheral conduction system, (2) interruption of the AV bundle, and (3) abnormal formation of the bundle branches (Lev, 1964a; Lev and Bharati, 1975; Bharati and Lev, 1984). Such lesions may be basic malformations of the conduction system or related to other malformations of the heart, such as atrial septal defect, ventricular septal defect, aneurysm of the pars membranacea, or tetralogy of Fallot (Lev, 1964a,b; Lev and Bharati, 1975). Although the present case was not related to any one type of gross congenital anomaly of the heart, the pathological changes in the AV conduction system were associated with an abnormality in the tricuspid extension of the central fibrous body: the abnormal architecture of the central fibrous body displaced the AV bundle to the right side and attenuated its penetrating portion. Thus, an anatomical fault of the AV bundle is considered to be part of an embryological developmental malformation of the central fibrous body in this case (Lev et al., 1971; James et al., 1976).
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Acknowledgments This study was supported in part by a Grant-in-Aid for Scientific Research (No. 15580288) from the Ministry of Education, Science, Sports and Culture of Japan.
References Bharati, S. and Lev, M. (1984). Pathology of atrioventricular block. Cardiology Clinics, 2, 741–751. Brooijmans, A. W. M. (1956). Electrocardiography in Horses and Cattle: Theoretical and Clinical Aspects, Uitgeverij Cantecleer, Utrecht. James, T. N. (1962). Anatomy of the sinus node of the dog. Anatomical Record, 143, 251–265. James, T. N. (1964). Anatomy of the A-V node of the dog. Anatomical Record, 148, 15–27. James, T. N. (1965). Anatomy of the sinus node, AV node and os cordis of the beef heart. Anatomical Record, 153, 361–371. James, T. N., Spencer, M. S. and Kloepfer, J. C. (1976). De subitaneis mortibus. XXI. Adult onset syncope, with comments on the nature of congenital heart block and the morphogenesis of the human atrioventricular septal junction. Circulation, 54, 1001–1009. Lev, M. (1964a). Anatomic basis for atrioventricular block. American Journal of Medicine, 37, 742–748.
Lev, M. (1964b). The normal anatomy of the conduction system in man and its pathology in atrioventricular block. Annals of the New York Academy of Sciences, 111, 817–829. Lev, M. and Bharati, S. (1975). Atrioventricular and intraventricular conduction disease. Archives of Internal Medicine, 135, 405–410. Lev, M., Cuadros, H. and Paul, M. H. (1971). Interruption of the atrioventricular bundle with congenital atrioventricular block. Circulation, 43, 703–710. Liu, S.-K., Tilley, L. P. and Tashjian, R. J. (1975). Lesions of the conduction system in the cat with cardiomyopathy. Recent Advances in Studies on Cardiac Structure and Metabolism, 10, 681–693. Narula, O. S. (1980). Atrioventricular block. In: Cardiac Arrhythmias, O. S. Narula, Ed., Williams and Wilkins, Baltimore, pp. 85–113. Olgin, J. E. and Zipes, D. P. (2001). Specific arrhythmias: diagnosis and treatment. In: Heart Disease, 6th Edit., E. Braunwald, D. P. Zipes and P. Libby, Eds, W.B. Saunders, Philadelphia, PA, pp. 815–889. Tsuji, N., Itabisashi, T., Nakamura, Y., Taira, N., Kubo, M., Ura, S. and Genno, A. (1992). Sudden cardiac death in calves with experimental heavy infection of Strongyloides papillosis. Journal of Veterinary Medical Science, 54, 1137–1143.
Received; July 27th; 2004 Accepted; December 17th; 2004
SHORT PAPER
www.elsevier.com/locate/jcpa
A Histological Study of the Cardiac Conduction System in a Heifer with Complete Atrioventricular Block N. Machida, S. Katsuda*, Y. Kobayashi† and K. Mitsumori Department of Veterinary Pathology, Tokyo University of Agriculture and Technology, Faculty of Agriculture, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509, *Department of Physiology, Fukushima Medical University School of Medicine, 1 Hikari-ga-oka, Fukushima 960-1295, and †Department of Pathological Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan
Summary A case of complete atrioventricular (AV) block of congenital origin in a 16-month-old Holstein heifer was studied histologically with serial sectioning of the cardiac conduction system. The heart was enlarged and showed moderate dilatation of the left and right ventricles. Histologically, the abnormally placed and poorly formed AV bundle was observed in association with abnormality in the tricuspid extension of the central fibrous body, suggesting that the pathological state of the AV bundle had been responsible for the complete AV block. This type of anatomical fault in the AV bundle is considered to be part of an embryological, developmental malformation of the central fibrous body. q 2005 Elsevier Ltd. All rights reserved. Keywords: atrioventricular block; cardiac conduction; cattle
Complete atrioventricular (AV) block occurs when no atrial activity is conducted to the ventricles and, therefore, the atria and ventricles are controlled by independent pacemakers (Olgin and Zipes, 2001). In human patients, such conduction disturbance may be due to congenital or acquired lesions; it may result from a block at the level of the AV node (usually congenital), within the AV bundle, or distal to the AV bundle in the Purkinje system (usually acquired) (Narula, 1980; Olgin and Zipes, 2001). Although complete AV block has been recorded in various animal species other than man, including cattle (Brooijmans, 1956; Tsuji et al., 1992), very few reports have included any morphological details of the cardiac conduction system; thus, only Liu et al. (1975), in a study in cats, examined systematically the relation between anatomical lesions and physiological events in the cardiac conduction system. The present report describes a serial section study of the conduction 0021-9975/$ - see front matter
doi:10.1016/j.jcpa.2004.12.004
system in a 16-month-old Holstein heifer with congenital complete AV block. The calf was born after an uneventful pregnancy and normal delivery, but it remained sedentary after birth. At the age of one month, a periodic physical examination revealed that it had an almost regular, but slow, pulse, but no detailed cardiological investigation was undertaken at that time. At the age of 13 months, the animal suffered a syncopal attack. An electrocardiogram revealed sinus rhythm with a rate of 120 beats/min and complete AV block with a ventricular escape rate of 30 beats/min (Fig. 1). Since its general condition was good, the animal was not considered to require any treatment. However, a further examination 3 months later revealed congestive heart failure with extensive subcutaneous and pulmonary oedema. Complete AV block, with an atrial rate of 110 to 130 beats/min and a ventricular rate of 20 to 35 beats/min, was still shown by electrocardiography. Multiple premature q 2005 Elsevier Ltd. All rights reserved.
Complete atrioventricular block in a heifer
69
Fig. 1. Electrocardiogram from heifer aged 13 months. A complete atrioventricular (AV) block with a ventricular escape rhythm (arrowheads) of 30 beats/min is demonstrated. The P waves (P) occur regularly at a rate of 120 beats/min. Base-apex lead, 25 mm/sec, 1 cm/mV.
ventricular contractions were also noted. Because of the poor prognosis, the animal was humanely killed. At necropsy, a considerable amount of strawcoloured fluid with a few, gelatinous, fibrin clots was seen in the thoracic and abdominal cavities. The pericardial sac was slightly thickened and contained about 1100 ml of yellowish serous fluid. The heart was enlarged with moderate dilatation of the left and right ventricles and endocardial thickening. The lungs were diffusely congested, oedematous and firm on palpation, and the trachea and bronchi contained a frothy fluid. The liver was moderately congested and enlarged, and the spleen slightly so. No other gross abnormalities were detected. Tissue samples from the lungs, thyroid glands, parathyroid glands, oesophagus, stomach, small and large intestines, pancreas, liver, mesenteric lymph nodes, spleen, adrenal glands, kidneys, urinary bladder, ovaries, uterus, brain, spinal cord and skin were fixed in 10% phosphate-buffered formalin, embedded in paraffin wax, sectioned at 5 mm, and stained with haematoxylin and eosin for light microscopy. A histological study of the cardiac conduction system was performed with the techniques described by James (1962, 1964, 1965). The regions of the sinoatrial (SA) node, the AV node, and the AV bundle and bundle branches were sectioned subserially at 3–5-mm intervals. Tissue blocks containing the AV node and bundle, which encompass the region from the posterior margin of the aorta back through the coronary sinus, were decalcified before microtome sectioning. After cutting screening sections 5 mm thick, serial sections of selected blocks were prepared, and every tenth section was mounted on a glass slide. The left and right ventricular free walls and the left atrium were cut into 72 blocks, and two sections were taken from each block.
The sections were alternately stained with Masson’s trichrome and elastica-van Gieson stains. The histopathological findings of the cardiac conduction system were as follows. The SA node and its approaches were intact and showed no changes. The AV node was normal in situation and size and the atrial muscle bundles were connected normally to it. The penetrating AV bundle was normal in location and size at its origin, but its proximal portion ran anteriorly, descending toward the tricuspid annulus, where it had come to lie on the right side of the ventricular septum (Fig. 2). The middle and distal portions of the penetrating AV bundle ran immediately beneath the endocardium just below the insertion of the base of the septal leaflet of the tricuspid valve (Fig. 3A). The middle portion was encased in dense fibrous tissue and its stem consisted at most of a few single-cell strands throughout its course; thus, continuity of the AV bundle was maintained only by “frayed strands” (Fig. 3B). This fibrous tissue involved the entire breadth of the penetrating AV bundle and was confined to it, the subjacent myocardium being normal. In the distal portion of the penetrating AV bundle, the narrow stem became thicker, though flattened in a vertical direction and smaller than normal, as it passed forward (Fig. 4A). Marked fibrous tissue was observed among the conducting fibres (Fig. 4B). In more anterior sections where the conal septal musculature appeared on the upper-left side of the summit of the main ventricular septal musculature, the terminal portion of the penetrating AV bundle expanded rapidly and bifurcated, giving rise to the left bundle branch (LBB) as a characteristic broad sheet and the right bundle branch (RBB) as a single discrete fascicle. The proximal portion of the LBB contained an abnormal amount of fibrous tissue and coursed to the left side, penetrating
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N. Machida et al.
Fig 2. A,B. Heifer, heart, proximal portion of the penetrating AV bundle (AVB). The AV bundle is displaced to the right side of the ventricular septum (A). The outlined area in A is seen at higher magnification in B. CFB, central fibrous body; TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
between the conal septal and main ventricular septal musculature; the RBB proceeded forward and downward to enter the myocardium. When traced distally, the conducting fibres of the LBB were observed to be involved in the thick
endocardial fibroelastosis of the left ventricle. The RBB could not be followed more peripherally. Except in the region of the junction between the AV node and bundle, the tricuspid extension of the central fibrous body was abnormal. Far thicker
Fig 3. A,B. Heifer, heart, middle portion of the penetrating AV bundle (AVB). The right-sided AV bundle is attenuated and its narrow stem is encased in dense fibrous tissue (A). The outlined area in A is seen at higher magnification in B. TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
Complete atrioventricular block in a heifer
71
Fig 4. A,B. Heifer, heart, distal portion of the penetrating AV bundle (AVB). The narrow stem of the right-sided AV bundle becomes thicker, though flattened in a vertical direction and smaller than normal. The outlined area in A is seen at higher magnification in B. TV, tricuspid valve; and VS, ventricular septum. Masson’s trichrome. A,!10; B,!80.
strands of collagenous tissue than would be expected in the normal heart proceeded from the inferior tip of the os cordis toward the tricuspid annulus and involved the AV bundle in the dense fibrous environment (Figs 2–4). As a result, the AV bundle was displaced to the right side and its penetrating portion was attenuated. Endocardial fibroelastosis was diffuse in both ventricles, being more marked in the left. Focal fibrosis was present in some areas of the left ventricle and ventricular septum, with occasional infiltration of mononuclear inflammatory cells. Other significant histological changes were confined to the liver, spleen and lungs. The liver had centrilobular congestion with necrotic hepatocytes and dilatation of the lymphatics. In the spleen, vascular congestion and expansion of the red pulp were present, and the lungs showed marked alveolar oedema with numerous macrophages containing erythrocytes or haemosiderin. The remaining organs were normal. Histological study in the present case revealed an abnormally placed and poorly formed AV bundle, considered to have been the likely anatomical basis for the complete AV block. Although this case was not electrocardiographically documented as complete AV block until the heifer was 13 months old, it may represent an example of congenital AV block because the heifer had a slow pulse as early as one month of age and histological examination
revealed an unusual type of AV bundle defect. Similar lesions of the AV bundle have been documented in human cases of congenital complete AV block and it has been suggested that these were responsible for the conduction disturbance (Lev et al., 1971; James et al., 1976) There are three morphological types of congenital AV block in man, namely, (1) lack of connection between the atria and the peripheral conduction system, (2) interruption of the AV bundle, and (3) abnormal formation of the bundle branches (Lev, 1964a; Lev and Bharati, 1975; Bharati and Lev, 1984). Such lesions may be basic malformations of the conduction system or related to other malformations of the heart, such as atrial septal defect, ventricular septal defect, aneurysm of the pars membranacea, or tetralogy of Fallot (Lev, 1964a,b; Lev and Bharati, 1975). Although the present case was not related to any one type of gross congenital anomaly of the heart, the pathological changes in the AV conduction system were associated with an abnormality in the tricuspid extension of the central fibrous body: the abnormal architecture of the central fibrous body displaced the AV bundle to the right side and attenuated its penetrating portion. Thus, an anatomical fault of the AV bundle is considered to be part of an embryological developmental malformation of the central fibrous body in this case (Lev et al., 1971; James et al., 1976).
72
N. Machida et al.
Acknowledgments This study was supported in part by a Grant-in-Aid for Scientific Research (No. 15580288) from the Ministry of Education, Science, Sports and Culture of Japan.
References Bharati, S. and Lev, M. (1984). Pathology of atrioventricular block. Cardiology Clinics, 2, 741–751. Brooijmans, A. W. M. (1956). Electrocardiography in Horses and Cattle: Theoretical and Clinical Aspects, Uitgeverij Cantecleer, Utrecht. James, T. N. (1962). Anatomy of the sinus node of the dog. Anatomical Record, 143, 251–265. James, T. N. (1964). Anatomy of the A-V node of the dog. Anatomical Record, 148, 15–27. James, T. N. (1965). Anatomy of the sinus node, AV node and os cordis of the beef heart. Anatomical Record, 153, 361–371. James, T. N., Spencer, M. S. and Kloepfer, J. C. (1976). De subitaneis mortibus. XXI. Adult onset syncope, with comments on the nature of congenital heart block and the morphogenesis of the human atrioventricular septal junction. Circulation, 54, 1001–1009. Lev, M. (1964a). Anatomic basis for atrioventricular block. American Journal of Medicine, 37, 742–748.
Lev, M. (1964b). The normal anatomy of the conduction system in man and its pathology in atrioventricular block. Annals of the New York Academy of Sciences, 111, 817–829. Lev, M. and Bharati, S. (1975). Atrioventricular and intraventricular conduction disease. Archives of Internal Medicine, 135, 405–410. Lev, M., Cuadros, H. and Paul, M. H. (1971). Interruption of the atrioventricular bundle with congenital atrioventricular block. Circulation, 43, 703–710. Liu, S.-K., Tilley, L. P. and Tashjian, R. J. (1975). Lesions of the conduction system in the cat with cardiomyopathy. Recent Advances in Studies on Cardiac Structure and Metabolism, 10, 681–693. Narula, O. S. (1980). Atrioventricular block. In: Cardiac Arrhythmias, O. S. Narula, Ed., Williams and Wilkins, Baltimore, pp. 85–113. Olgin, J. E. and Zipes, D. P. (2001). Specific arrhythmias: diagnosis and treatment. In: Heart Disease, 6th Edit., E. Braunwald, D. P. Zipes and P. Libby, Eds, W.B. Saunders, Philadelphia, PA, pp. 815–889. Tsuji, N., Itabisashi, T., Nakamura, Y., Taira, N., Kubo, M., Ura, S. and Genno, A. (1992). Sudden cardiac death in calves with experimental heavy infection of Strongyloides papillosis. Journal of Veterinary Medical Science, 54, 1137–1143.
Received; July 27th; 2004 Accepted; December 17th; 2004