The Anatomical Basis of Complete At Rio Ventricular Block in Cats With Hypertrophic Cardiomyopathy

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J. Comp. Path. 2006,Vol. 135, 25^31

The Anatomical Basis of Complete AtrioventricularBlock in Cats with Hypertrophic Cardiomyopathy

T. Kaneshige*, N. Machiday, H. Itohz and Y. Yamane*

Department of *Veterinary Surgery, yPathology, and zVeterinaryTeaching Hospital,Tokyo University of Agriculture and

Technology, 3-5-8 Saiwai-cho, Fuchu,Tokyo 183-8509, Japan

Summary

The cardiac conduction system was examined histologically in 13 feline cases of hypertrophic cardiomyopathy(HCM) with complete atrioventricular (AV) block. Marked degeneration and ¢brous replacement of the AVcon-duction systemwere consistentlyobserved in the combined regions of thebranching portion of theAV bundle andthe upper portion of the left bundle branch. These changes were associated with extensive ¢brosis of the central¢brous body and endocardial and myocardial ¢brosis in the upperborder of the ventricular septum. Chondrome-taplastic lesions or osseous lesions, or both, present in the base of the central ¢brous body, compressed the under-lying penetrating or branching (or both) portions of the AV bundle, causing apparent reduction of the conduction¢bres.The pathologicalprocess and the nature and predilection sites of the lesionsresembled those associated withageing in human patients with complete AV block. It is possible that the pathological process in the cats was fun-damentally related to the normal ageing phenomenon and may have been exacerbated by mechanical forces cre-ated by the cardiac hypertrophy associated with HCM.

r 2006 Elsevier Ltd. All rights reserved.

Keywords: atrioventricular bundle; cat; complete atrioventricular block; conduction system; hypertrophic cardiomyopathy

Introduction

Complete atrioventricular (AV) block is characterizedon an electrocardiogram by a lack of relationship be-tweenthe P waves and the QRS complexes.This occursas a result of a total failure of AVconduction.The atriaand the ventricles beat independently of one anotherand at their own intrinsic rate, that of the ventriclesusually being substantially slower than that of the atria(Kittleson, 1998; Fox and Harpster, 1999; Carr et al .,2001). The QRS-T con¢guration varies and is depen-

dent upon the origin of the ventricular pacemaker tis-sue (Harpster, 1977; Fox et al ., 1991). The clinical signsassociated with completeAV block are exercise intoler-ance, weakness, syncope, or congestive heart failure(Kittleson, 1998; Fox and Harpster, 1999; Carr et al .,2001).

In human patients, the anatomical basis of completeAV block has been the topic of considerable study. Per-

manent complete AV block is almost always due to adirect e¡ect of pathological processes on the conduc-tion system or to extension of pathological processesfrom surrounding areas (Lev, 1964a; Lev and Bharati,1975). These processes include myocarditis, infectiousendocarditis, ischaemic coronary disease, neoplasticdisease, fatty in¢ltration, uraemia, and haemochroma-tosis (Lev, 1964a; Lev and Bharati, 1975; Bharati andLev, 1984; Bharati, 2001). The most common cause of this type of block in elderly human patients is sclerosis

of the left side of the cardiac skeleton (Lev, 1964b; Levand Bharati,1975).In dogs and cats, complete AV block is associated

with heart diseases, especially myocardial disorders,that include congenital heart defects, in¢ltrative cardi-omyopathy (amyloidosis or neoplasia), idiopathic¢brosis, myocardial infarction, hypertrophic cardio-myopathy (HCM), bacterial endocarditis, myocarditisassociated with Lyme disease, and Chagas’ disease(Kittleson, 1998; Fox and Harpster, 1999; Carr et al .,2001). However, there have been few histopathological

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Correspondence to: N. Machida (e-mail: [email protected]).

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studies on the AV conduction system in such cases of complete AV block (Liu etal .,1975), and the anatomicalbasis of the observed electrocardiographic events re-mains unsolved.

The purpose of this study wasto characterizethe his-

topathological lesions observed in the AV conductionsystem in 13 feline cases of HCM with complete AVblock.

Materials and Methods

Animals

The hearts of 13 cats (cases1^13) in which complete AVblock was diagnosed electrocardiographically between1998 and 2005 were studied post mortem.The clinical di-agnosis of the underlying heart disease was invariablyHCM. The cats consisted of eight males and ¢ve fe-

males aged 8^17 years (mean 12 Á3 years). In eight of the 13 cats, the ¢rst symptom was syncope; four catsshowed lethargy or episodic weakness, and in the re-maining animal the AV block was discovered inciden-tally. In all of the cats, the ventricular escape rhythmranged from 38 to102 beats/min and was accompaniedby wide and bizarre QRS complexes (QRS duration inbipolar standard limb lead II was at least 0 Á 06 s; Fig.1).The AV block, which was permanent in all cases, wasobserved for periods of a few days to 27 months beforedeath.Two animals died suddenly, but death was attri-butableto congestive heart failure in seven animals andto aortic thromboembolism in four. A pacemaker hadbeen implanted in three cats, which survived for 12months or longer from the ¢rst syncopal attack.

Control hearts were obtained from10 cats aged11^15years (mean12 Á9 years) that died from neoplasia, withno evidence of clinical cardiovascular disease. Normalelectrocardiograms were taken from these cats duringthe last month of their life.

Histopathology

The heart was removed from each cat within 24 h of death and subjected to gross examination. It was then

weighed and placed in 10% phosphate-bu¡ered forma-lin for at least 5 days. The cardiac conduction systemwas studied with techniques described previously by

James (1962, 1964). Brie£y, the regions of the sinoatrial

(SA) node and its approaches, the AV node and its ap-proaches, andthe AV bundle andbundle branches weresectioned at 3-mm intervals. Multiple myocardial tis-sue blocks were sampled from the left and right ventri-cular free walls and from the ventricular septum.

Samples were processed by routine methods, em-bedded in para⁄n wax, sectioned at 5mm, and stainedwith haematoxylin and eosin (HE) for light microsco-pical examination. Tissue blocks containing the AVnode andthe AV bundle andbundle branches were ¢rstscreened histologically; serial sections (5 mm) of se-lected blocks were then prepared, every ¢fth sectionbeing mounted on a glass slide. Alternate sections werestained with HE and Masson’s trichrome.

The nomenclature of the cardiac conduction systemdescribed by Lev (1964a) was applied in this study. TheAV bundle was divided into penetrating and branching

portions.The rate of reduction of conduction ¢bres wasclassi¢ed as being mild (less than 25% reduction),moderate (25^50% reduction), or severe (more than50% reduction), as estimated from cross-sections of each division of the conduction system.

Results

Macroscopical Findings

The10 control hearts were grossly normal andweighedbetween11and 23 g (mean17 Á4 g).The heart weights of the cats with AV block ranged from 16 to 41g (mean

25 Á8 g); moreover, in these animals the mean relativeheart weight (i.e., heart weight in g/body weight inkg) was markedly greater (6 Á770 Á7 g/kg) than in thecontrol cats (4 Á570 Á2 g/kg). In all a¡ected cats, thehearts were enlarged and globular in shape, with dif-fuse hypertrophy of the left ventricular free wall, ven-tricular septum, and left ventricular papillary muscles,marked dilatation of the left atrium, and a narrow leftventricular cavity. In cases 9,12 and13, the anterior mi-tral lea£et was thickened and there was a marked endo-cardial ¢brous thickening of the ventricular septumthat extended below the aortic valve (Fig. 2). The junc-

tional area of the atrial and ventricular septa was cutinto 3-mm slices perpendicular to the line of junctionof the septa and examined macroscopically; moderateor marked ¢brosis of the central ¢brous body and the

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Fig.1. Electrocardiogram recording, case 4.There is a complete atrioventricular (AV) block witha ventricular rate of 45 beats/min and wideand bizarre QRS complexes of 0 Á10 s duration (arrows). The P waves (P) occur regularly at a rate of 198beats/min. Bipolar standardlimb lead II, 50 mm/s,1 cm/mV.

T. Kaneshige et al .26



uppermost ventricular septum was seen in 11 of the 13cases.

Microscopical Findings

Signi¢cant histological changes were observed in themyocardium of all a¡ected cats but not in the controlcats. Cardiac muscle cells in the ventricular myocar-dium were hypertrophied and disorganized, adjacentcells being aligned perpendicularly and obliquely toeach other. Interstitial myocardial ¢brosis was ob-served with arteriosclerosis of the small intramuralcoronary arteries (¢bromuscular hyperplasia). Thechanges were widespread in the left ventricle and ven-

tricular septum, and were occasionally observed in theright ventricle.

The histopathological ¢ndings in the cardiac con-duction system were as follows. In all 10 control cats,there was a slight increase in ¢brous or ¢bro-fatty tissue

in the SA and AV nodes and their approaches, consis-tent with the ageing process. Slight to moderate ¢brosisof the central ¢brousbody andthe uppermost ventricu-lar septum was seen in most of the control cats, withchondrometaplastic and osseous lesions in ¢ve andthree, respectively. In some animals these focal lesionsappeared to have compressed the underlying penetrat-ing or branching (or both) portions of the AV bundle,with mild degeneration and atrophy; minimal reduc-tion of the conduction ¢bres was evident. Moreover, ¢-brotic changes in the subendocardium of theuppermost ventricular septum a¡ected the branching

portion of the AV bundle and the upper portions of both the left bundle branch (LBB) and right bundlebranch (RBB), usually causing a mild to moderate re-duction of conduction ¢bres.

In all a¡ected cats, the SA and AV nodes and theirapproaches were normal, except for slight to moderateageing changes (i.e., an increase in ¢brous tissue orfatty in¢ltration, or both). However, the AV bundleand bundle branches showed mild to severe reductionof conduction ¢bres due to ¢brous replacement, the de-gree of which varied at di¡erent levels in each case. Asshown inTable 1, the location of the severe lesions in thea¡ected cats was as follows: both penetrating and

branching portions of the AV bundle in two cases; bothpenetrating and branching portions of the AV bundleand the upper portion of the LBB in two cases; thebranching portion of the AV bundle in two cases; and

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Fig. 2. Heart (case 9) transected in the long axis, showing massive

ventricular hypertrophy, marked ¢brosis of the central ¢-brous body (arrow), and a marked endocardial ¢brousthick-ening of the upper portion of the thickened ventricularseptum. LVW, left ventricular wall; VS, ventricular septum.Scale,1mm.

Table 1

Histopathological ¢ndi ngs in the conduction system in feline cases of complete atrioventricular block

Case SA n ode APP to SA n ode APP to AV node AV node AV bundle, penetrating AV bundle, branching LBB RBB

1 Fib-Fat/+1 Fib-Fat Fib-Fat Fib-Fat/+1 Fib/+3 Fib/+3 Fib/+3 Fib/+1

2 No Fib-Fat Fib-Fat Fib/+1 Fib/+3 Fib/+3 Fib/+2 No

3 No No No No Fib/+1 Fib/+3 Fib/+2 Fib/+2



6 Fib/+1 Fib-Fat Fib-Fat Fib/+1 Fib/+1 Fib/+3 Fib/+3 Fib/+1

7 Fib/+1 Fib-Fat Fib-Fat Fib/+1 Fib/+3 Fib/+3 Fib/+3 Fib/+1

8 No Fib-Fat Fib-Fat No Fib/+1 Fib/+3 Fib/+2 No

9 Fib/+1 Fib-Fat Fib-Fat No Fib/+1 Fib/+3 Fib/+3 Fib/+1


11 No No Fib-Fat No Fib/+3 Fib/+3 Fib/+2 No

12 No Fib-Fat Fib-Fat No Fib/+1 Fib/+3 Fib/+3 Fib/+1


Abbreviations: APP, approaches; SA, sinoatrial; AV, atrioventricular; LBB, left bundle branch; RBB, right bundle branch; Fib, ¢brous replacement;

Fib-Fat, ¢bro-fatty replacement; No, no remarkable changes. Rate of reduction of conduction ¢bres: +1, mild (o25% reduction); +2, moderate (25^

50% reduction): +3, severe (450% reduction).

Complete Heart Block in Cats with HCM 27



the branching portion of the AV bundle and the upperportion of the LBB in seven cases.

The central ¢brous body was markedly thickeneddue to ¢brosis, andwas abnormal in all cases: the exten-sive central ¢brous body replaced the delicate areolartissue at the upper border of the ventricular septum,and collagen ¢bres penetrated the uppermost ventricu-

lar septum, encasing or entrapping, either totallyor partly, the AV bundle in the dense ¢brous tissue(Fig. 3A). In addition, a focal chondrometaplastic le-sion was found extending downward from the lower-most portion of the central ¢brous body on to theunderlying penetrating or branching (or both) por-tions of the AV bundle in 10 of the 13 cases, excludingcases 3, 9 and 12. These lesions seemed to compress theconduction ¢bres of the AV bundle, in which in¢ltra-tion of ¢brous tissue was observed among the survivingcells (Fig. 3B). In cases 3, 6, 9, 10,12 and 13, a bone cystwith marrow elements had replacedthe base of the cen-

tral ¢brous body and was compressing the underlyingbranching portion of theAV bundle (Fig. 4A), resultingin various degrees of degeneration, atrophy and ¢brosisof the conduction ¢bres (Fig. 4B). In cases 3, 9 and 12,the branching portion of the AV bundle was totally de-stroyed.

At the upper border of the ventricular septum, mod-erate to marked endocardial ¢brosis was noted on theleft side, causing moderate to severe destruction of theupper portion of the LBB (Fig. 5A). The conduction ¢-bres of the branch had been either partly or totally ob-scured by the dense ¢brous tissue (Fig. 5B). Thispathological process in the subendocardium extended

throughout the entire breadth of the branch, in mostcases extending to the subjacent myocardium. In addi-tion, there was slight to moderate ¢brosis in the moreperipheral areas of the subendocardium, with slight de-generation and atrophy of the conduction ¢bres in themiddle and lower portions of the LBB. This subendo-cardial ¢brous replacement was con¢ned to the branch,

the surrounding and subjacent myocardium being freefrom these abnormal amounts of ¢brous tissue. On theright side of the uppermost ventricular septum, thesubendocardial portion of the RBB was frequently af-fected, but not destroyed, by endocardial ¢brosis; themore peripheral portions of the RBB were preservedin most cases.

Discussion

Complete AV block in cats in the present study was as-sociated with HCM, as con¢rmed by the gross ¢ndings

of massive ventricular hypertrophy and a reduced leftventricular chamber, and the microscopical ¢ndings of hypertrophied and bizarrely arranged cardiac musclecells in the thickened ventricular walls. Additionalcharacteristics of the disease were interstitial ¢brosisand thick-walled, intramural, coronary arteries with anarrowed lumen. Feline cardiomyopathies, includingHCM, are frequently associated with various types of arrhythmia and occasionally with complete AV block(Fox, 1999; Fox and Harpster, 1999; Carr et al ., 2001).However, there have been few histopathological studieson the AV conduction system in cases with completeAV block (Liu et al ., 1975), and the aetiology of the

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Fig. 3. A,B.The AVconduction system (case 7), showing marked atrophy and ¢brous replacement of the branching portion of theAV bundle(arrowhead) due to compression from a chondrometaplastic lesion in the extensive central ¢brousbody (A). The outlined area in A isseen at higher magni¢cation in B. CFB, central ¢brous body; AS, atrial septum;VS, ventricular septum. Masson’s trichrome. A, Â25;B, Â82.




associated electrocardiographic events has not beenelucidated.

In the 13 feline cases in the present study of HCMwith complete AV block, marked degeneration and ¢-brous replacement of the AV conduction system wereobserved consistently in the branching portion of theAV bundle and the upper portion of the LBB, in asso-ciation with extensive ¢brosis of the central ¢brous

body and endocardial and myocardial ¢brosis at theupper border of the ventricular septum. Chondrometa-plastic lesions or osseous lesions, or both, in the base of the central ¢brousbody were found to have compressedthe underlying penetrating or branching (or both) por-tions of the AV bundle, causing an apparent reductionof the conduction ¢bres. The ¢brous replacement of theAV bundle and bundle branches was both qualitatively

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Fig. 4. A,B.The AVconduction system (case 9), showing destruction of the branching portion of the AV bundle (arrowhead), which is com-pressed by a bone cyst with marrow elements in the base of the central ¢brous body (A). The outlined area in A is seen at highermagni¢cation in B.The space between the a¡ected AV bundle andthe ventricular septal crest is an artifact.CFB, central ¢brousbody;BC, bone cyst; VS, ventricular septum. Masson’s trichrome. A, Â25; B, Â82.

Fig. 5. A,B. The AV conduction system (case 5), showing complete disappearance of the conduction ¢bres at the upper portion of the left

bundle branch (arrowhead) as a result of endocardial and upper border ¢brosis at the ventricular septum (A). The outlined area inA is seen at higher magni¢cation in B. The branching portion of the AV bundle is also a¡ected. CFB, central ¢brous body; AS, atrialseptum; VS, ventricular septum. Masson’s trichrome. A, Â25; B, Â82.




and quantitatively more severe than that observed inthe control cats. On the otherhand, in the more periph-eral portions of the LBB and the upper portion of theRBB, only mild replacement of the conduction ¢bresby ¢brosiswas evident. Inthe remainingdistal portions

of the RBB, signi¢cant changes were not observed. Inthe present study, therefore, it was concluded that thesites most vulnerable to lesions in the AV conductionsystem were the combined regions of the branchingportion of the AV bundle and the upper portion of theLBB, which would seem to have been the likely anato-mical basis for the complete AV block.

In human patients with complete AV block, it hasbeen generally assumed that the wide escape-beatQRS complexes may be attributed to lesions in the dis-tal portion of the AV bundle or bilateral lesions of thebundle branches, and that the narrow QRS complexes

may be associated with lesions in the approaches to theAV node, in the AV node itself, or in the proximal por-tion of the AV bundle (Ohkawa et al ., 1981; Myerburget al ., 2001; Olgin and Zipes, 2001). In the 13 feline casesin the present study of HCM with complete AV block,all of which showed wide QRS complexes on their elec-trocardiograms, the main lesions of the cardiac con-duction system were consistently observed in thebranching portion of theAV bundle and the upper por-tion of the LBB. These ¢ndings are compatible withthose observed in human patients with this type of ar-rhythmia.

It is uncertain as to why the degenerative and ¢brotic

changes should have occurred in such locations in theAVconduction system. However, it is interesting to notethat the pathological changes were similar to those as-sociated with the ageing process, seen in the AV con-duction system in the form of ‘‘sclerosis of the left sideof the cardiac skeleton’’ (Lev, 1964b). This is the mostcommon cause of permanent complete AV block in hu-man patients (Lev,1964b; Lev and Bharati,1975), whichis known clinically as idiopathic or primary heart block(Harris,1976). In general, with advancing age, the cen-tral ¢brous body, the pars membranacea, the aortic-mitral annulus, the mitral annulus, the aortic valve

base, and the upper border of the ventricular septumundergo progressive ¢brosis and calci¢cation. The de-generative process may result in disruptive lesions of the AV bundle and the beginning of the bundlebranches, producing complete AV block (Lev, 1964b;Lev and Bharati, 1975; Bharati and Lev,1984; Bharati,2001). Most cases of idiopathic or primary heart blockthat occur as a result of such ageing processes are seenin human patients aged 55 or more years (Bharati,2001). The ages of the 13 a¡ected cats in the presentstudy ranged from 8 to17 years and averaged12.3 years.

The concept of sclerosis of the left side of the cardiacskeleton in elderly human patients with idiopathic or

primary heart block (Lev, 1964b) may be applied tothis type of conduction disturbance in cats with HCM.Inthe present study, there were twopredilection sites of the lesions in theAVconduction system, as in man (Levand Bharati,1975; Bharati and Lev,1984; Bharati, 2001).

One was the branching portion of the AV bundle,where a junction was formed between the hard, non-contracting central ¢brous body and the relatively soft,contracting myocardium of the ventricular septum.The central ¢brous body, as the main structure of thecardiac skeleton, is particularlyexposed tothe mechan-ical stress and strain produced by myocardial contrac-tion; this leads eventually to extensive ¢brosisaccompanied by chondrometaplastic lesions or osseouslesions, or both, which may result in degeneration and¢brous replacement of the AV bundle. The other predi-lection site was the upper portion of the LBB at the left

side of the uppermost ventricular septum. Rapidlyejected blood might have a damaging e¡ect on the en-docardium at the out£ow tract of the left ventricle,which might impair the underlying branch due to en-docardial ¢brosis (Lev, 1964b; Lev and Bharati, 1975).The branching portion of theAV bundle andthe upperportion of the LBB are relatively super¢cial subendo-cardial structures and, as such, are susceptible to thedegenerative changes caused by ageing (Bharati, 2001).

In conclusion, it is presumed that marked degenera-tion and ¢brous replacement of the cardiac conductionsystem in the combined regions of the branching por-tion of the AV bundle and the upper portion of the

LBB lead to impaired AV conduction, which setsthe stage for complete AV block. Bearing in mind thatthe ¢brotic lesions of the AV bundle and bundlebranches observed in the a¡ected cats with HCM werequalitatively similar to, but more severe than, those inthe control cats, it would seem possible that the patho-logical process is fundamentally related to the normalageing phenomenon and is probablyexaggerated or ac-celerated by the abnormal mechanical forces createdby cardiac hypertrophy. Interestingly, in human pa-tients with HCM and subvalvular aortic stenosis (idio-pathic hypertrophic subaortic stenosis) the AV

conduction system is extensively impaired by mechan-ical factors caused by hypertrophy of the ventricularseptum (Bharati et al .,1980).

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Received, October10th, 2005

Accepted, March 22nd, 2006

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The Anatomical Basis of Complete At Rio Ventricular Block in Cats With Hypertrophic Cardiomyopathy