of the secondary cardiomyopathies pathologist's · Postgraduate MedicalJournal(December 1972) 48, 714-721. Classification of the secondary cardiomyopathies The pathologist's view

Postgraduate Medical Journal (December 1972) 48, 714-721.

Classification of the secondary cardiomyopathiesThe pathologist's view

ARIELA POMERANCE

SECONDARY cardiomyopathy is defined as heartmuscle disease of known cause or association.Naming particular diseases is preferable whereindividual conditions are being referred to e.g.myocardial sarcoid, cardiac amyloidosis, scleroder-ma heart disease, since the term cardiomyopathywithout qualification is generally accepted as refer-ring to the primary forms. Nevertheless, a convenientcollective term is needed to cover all the conditionswhich have to be excluded before a diagnosis ofprimary cardiomyopathy can be made. There are avery large number of such conditions and Hudson(1970) lists over 100. Faced with an exercise inclassification of this magnitude most pathologistswould first divide the conditions according to anato-mical pathology, then consider the types of patho-logical reaction and finally the aetiology (Table 1).The material seen by the pathologist ranges from

a single stained slide to the complete body fornecropsy, with full clinical data. The first step is to

exclude vascular or valvular conditions which maybe responsible for the heart muscle disease. Of thevascular lesions, coronary atheroma is the common-est known cause of heart muscle disease, so muchso, that ischaemic heart disease is not usuallyregarded as a secondary cardiomyopathy. Rarercauses of coronary occlusion such as vasculitis withthrombosis, or fibrosis following trauma (includingcardiac surgery) should also be kept in mind.Valvular incompetence secondary to aortic walldisease may be due to cystic medionecrosis either asin the Marfan syndrome and similar uncommongenetically determined connective tissue disordersor more often as an isolated finding. It may alsooccur due to inflammatory changes as in ankylosingspondylitis and syphilis. Primary valve disease caus-ing myocardial changes is mainly fibrotic as inrheumatic-type valve disease, or calcific as in isolatedaortic stenosis. Less common underlying pathologiesare perforation of valve cusps following infective

TABLE 1. Pathology of secondary cardiomyopathiesMicroscopic pathology Causes

VesselsCoronary AtherosclerosisAorta Medionecrosis Generalized or localized connective tissue defect

Inflammation Ankylosing spondylitis.Syphilis

Valves Fibrosis Valvulitis (rheumatic and other)Calcification Degenerative or past inflammationMucoid degeneration Genetic or isolated

Myocardium Inflammation:activechronicgranulomatous See Table 2with collagen changes J

Fibrosis Post-inflammatoryGenetic ataxias and dystrophiesMucoviscidosisCollagen diseasesPost-surgery

Depositions:in muscle fibres Glycogen storage disease; haemochromatosis; calcificationbetween muscle fibres Mucopolysaccharidoses; oxalosis; myxoedema; amyloidosis

Small vessel changesembolic Bacterial and non-bacterial endocarditisinflammatory Collagen diseases

Non-specific changes or no Nutritionalapparent abnormality Toxic

Endocrine diseasesVascular shuntsChronic lung disease

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Pathologist's view of cardiomyopathies 715

endocarditis, mucoid degeneration producing'floppy'mitral or aortic cusps, and, very rarely, storagediseases such as mucopolysaccharidoses and hyper-cholesterolaemia.

Having excluded vascular and valvular causes ofheart muscle disease we come to conditions directlyinvolving the myocardium. Microscopy may showinflammatory changes of various types, fibrosis,abnormal depositions or abnormalities of smallvessels, but in many conditions the histologicalchanges appear minor and non-specific or noabnormality may be apparent on ordinary lightmicroscopy.

Inflammatory myocardial disease (Table 2)An infective aetiology is suggested by the presence

of large numbers of inflammatory cells with relativelylittle myocardial necrosis (Fig. 1).

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FIG. 1. Acute myocarditis. Focal myocardial necrosis ispresent but the picture is dominated by the dense pleo-morphic inflammatory cell infiltrate. From a baby dyingof Coxsackie myocarditis. H & E, x 290.

TABLE 2. Conditions associated with inflammatorymyocardial disease

InfectionsVirus Coxsackie, mumps, influenza, psittacosisRickettsial Q feverBacterial Diphtheria, brucella, tubercleSpirochaetal Leptospira, syphilisFungal Histoplasma, candidaProtozoal Toxoplasma, trypanosomaHelminthic Cysticercus, echinococcus

Granulomatous SarcoidGiant cell myocarditis

'Collagen' Rheumaticdiseases Rheumatoid

Scleroderma

In the later stages only scanty small aggregates ofinflammatory cells are present. These are mainlymononuclear, usually including a few plasma cells,and there is an increase in interstitial connectivetissue (Fig. 2).

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FIG. 2. Chronic myocarditis. Scanty chronic inflammatorycell foci, including plasma cells, with early fibrosis betweenmyofibres. From a child with 4 weeks' general malaisefollowing a febrile episode, who died of congestive cardiacfailure. H & E, x 320.


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716 Ariela Pomerance

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giant cells is clearly seen. H & E, x 320.

Giant cell granulomas are of two types. In giantcell myocarditis (Fig. 3) the myogenic nature of thegiant cells is clear. Various stages from abnormalmyofibres to isolated multinucleate giant cells canusually be readily identified. The giant cells ofsarcoid (Fig. 4) tuberculous or fungal myocarditisare larger, with no features suggesting a myofibreorigin and may contain inclusions or micro-organ-isms which can be demonstrated by appropriatestains.

In the collagen diseases inflammation is associatedwith fibrinoid or basophilic degeneration of inter-stitial myocardial connective tissue which is usuallybest seen around small vessels.Most examples of inflammatory myocardial

disease are either infective or of unknown patho-genesis. Myocarditis has been reported with almostevery known human pathogenic organism, andTable 2 makes no attempt at comprehensiveness.

In this country Coxsackie infections are compar-atively common, and tuberculous infections areincreasingly diagnosed, particularly in the elderly.

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FIG. 4. Sarcoid heart disease. Granulomatous lesionswith no apparent transition forms between myofibresand giant cells. H & E, x 65.

Fungal infections are rare and occur mainly inpatients already in hospital, either on immuno-suppressive therapy or with conditions such as dis-seminated malignancy in which the body immun-ology is abnormal. Of the protozoal diseases, toxo-plasma myocarditis is well recognized, and in SouthAmerica, Chagas' disease is common. Helminthicinfestation of the heart is rare and from my verylimited experience of this pathological curiosity itseems that extensive myocardial involvement maybe present without any clinical symptoms. Giantcell granulomatous reactions may be caused bymycobacteria or fungi but most cases are of unknownaetiology. There is a possibility that a transmissibleagent has been identified in sarcoid, but similarattempts in giant cell myocarditis have so far beenunsuccessful. Apart from the proven associationbetween group A haemolytic streptococcal infectionand rheumatic fever the pathogenesis of the collagendiseases is still obscure, although there is strongevidence suggesting that immunological factors areconcerned in all.


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FIG. 5. Diffuse myocardial fibrosis. The fibrous tissuesurrounds small groups and isolated myofibres. Manylarge bizarre nuclei are present. From a patient withmuscular dystrophy. H & E, x 65.

Diseases associated with myocardial fibrosisHistological changes vary from the fine inter-

stitial strands of collagen which develop followingmyocarditis, to extensive replacement of myofibresby large areas of fibrous tissue, as in scleroderma.Marked variation in fibre size, vacuolation andbizarre large nuclei are not uncommon and have nodiagnostic significance. In most cases the aetiologyof the fibrosis is no longer apparent. Pathologistsgenerally assume such cases are due to previousmyocarditis, although some classify them as primarycardiomyopathies when no clinical evidence of anacute illness is obtained. Less common causes ofnon-coronary myocardial fibrosis are the geneticneuromuscular diseases, in particular Freidreich'sataxia and the muscular dystrophies (Fig. 5) andthe collagen diseases. Marked myocardial fibrosis iscommon in scleroderma, and rheumatic carditis mayalso be followed by quite extensive myocardial fibrosis.Rarely mucoviscidosis is associated with extensivemyocardial fibrosis, which has been attributed to vita-min deficiencies from malabsorption. Iatrogenic fibro-sis is an occasional sequel of cardiac surgery and may

also follow radiotherapy for carcinoma of breast orlung if the patient survives long engugh. Cardiacfibrosis has also been attributed to methysergide,but cases reported so far have mainly involved thebase of the heart or valves.

Abnormal depositions and infiltrationsThe abnormality may be in the myofibres or in

interstitial tissues. In glycogen storage disease themyofibres are grossly distorted, producing a charac-teristic lace-like pattern on histology (Fig. 6).Accumulations of inorganic substances produce

no significant distortion of the myofibres in mostcases (Fig. 7). Cysts may form in severe haemo-chromatosis or haemosiderosis, and in dystrophiccalcification the calcium often appears encrusted onthe surface of the fibres.Abnormal deposition between myofibres may be

within histiocytes, as in mucopolysaccharidosis(Fig. 8) or extracellular, as in amyloidosis (Figs.9 and 10) and myxoedema.

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FIG. 6. Glycogen storage disease. All myofibres are dis-tended by glycogen, resulting in a characteristic lace-likeappearance. From a child dying, aged 8 months, withhemiplegia, congestive cardiac failure and broncho-pneumonia. H & E, x 65.


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FIG. 7. Haemochromatosis. Granular pigment in musclefibres which retain their normal size and shape. Perl'sstain, x 290.

Amyloidosis is the only common condition in thiscategory and cases fall into two distinct groups.The most familiar type is the classical primary typewhich occurs mainly in patients between 45 and 70years and in which cardiomegaly is a prominentfeature and amyloid is usually plentiful in otherorgans. The other type, senile cardiac amyloid, ismuch more common, being found in about 10% ofpatients over 70 years old; it also may be respon-sible for cardiac failure. These patients are usuallyseen by the general practitioner or geriatrician andare rarely seen in specialized cardiac units. Incontrast to the classical primary type the amyloid is,for all practical purposes, confined to the heart, anddoes not cause cardiomegaly. The pathology of theheart differs slightly in these two forms, compressionatrophy of surrounded myofibres being a prominentfeature of the senile cardiac type (Fig. 9), while in theclassical type myofibres are widely separated byamyloid (Fig. 10) and atrophy is not conspicuousuntil a very late stage. Amyloid thus tends simply toreplace myofibres in the senile type and no increasein weight occurs, while in primary amyloidosis itadds to the substance of the heart and weights of upto 1000 g are not uncommon.

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FIG. 8. Mucopolysaccharidosis. An area of myocardialfibrosis containing numerous large 'clear cells', which arehistiocytes distended by mucopolysaccharide. From an1 -year-old-girl with gargoylism. H & E x 65.

Many of the conditions in this group are gene-tically determined. In glycogen and lipid storagediseases, mucopolysaccharidoses and oxalosis, en-zyme deficiencies are present while in haemochro-matosis the deficiency is in the gastric substancecontrolling iron absorption. Calcium depositionresults from either generalized or localized metabolicabnormalities and can occur in any condition inwhich the serum calcium is high, as well as inlocalized areas of degenerate myocardium from anycause. The aetiology of amyloidosis is obscure. It isknown to be associated with ageing in many animalsincluding man. Some cases are undoubtedly familialand it has been suggested that isolated cases ofprimary amyloidosis are simply sporadic cases of agenetically determined form.

Small vessel diseaseThis may not be suspected on gross examination,

but cardiac failure from multiple small coronaryemboli is not uncommon in infective endocarditis(Fig. 11). Emboli have been reported in up to 66%of cases of non-bacterial endocarditis, though this


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FIG. 9. Senile cardiac amyloidoisis, showing compressionand atrophy of myofibres and replacement by amyloiddeposits. No amyloid is present in the vessels. From aman of 82. Crystal violet, x 80.

is rarely of clinical importance since most of thesepatients have died with disseminated malignantdisease. Inflammatory small vessel (Fig. 12) disease isusually found in the collagen diseases group, inparticular polyarteritis nodosa and Wegener'sgranulomatosis. It is characterized by necrosis anddense inflammatory cell infiltration of the walls ofsmall arteries. Non-inflammatory focal degenerationof small coronary arteries has also been described(James, 1967).

Non-specific changes and conditions with noapparent changes

In many conditions known to be associated withcardiac failure routine sections show either noapparent abnormality or only minor non-specificchanges such as a minor degree of fatty change inmyofibres, focal myofibre necrosis, and scantysmall aggregates of polymorphs. These findings arenon-specific and are not infrequently observed inpatients dying of non-cardiac conditions. Specializedhistochemistry and electron microscopy may show

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changes where no abnormality is apparent on routineH & E stained material, but such techniques are notpracticable in most hospital pathology departments.The nutritional, toxic and endocrine causes of heartdisease all come into this group. Nutritional heartdisease includes vitamin and possibly proteindeficiencies and the anaemias. Chemicals known to beresponsible for heart disease include emetine,antimony and cobalt, which is sometimes a con-stituent of beer. Alcohol must be included as a toxin,although nutritional factors may also be involved inalcoholic heart disease. The phenothiazine group oftranquillizers have recently come under suspicion asa cause of myocardial abnormalities and suddendeath. Amongst endocrine causes of cardiac failurethyrotoxicosis is the most common, particularly inelderly patients, but cardiomegaly and failure arewell recognized features of myxoedema, acromegalyand Cushing's disease. Finally, specific pathology isalso absent in heart disease secondary to chroniclung disease or to vascular shunts, and althoughthese conditions are not usually included as secon-dary cardiomyopathies, they must nevertheless be


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FIG. II. Coronary microembolism in infective endo-carditis. Fragments of bacterial vegetation occlude asmall artery. H & E, 150.

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FIG. 12. Inflammatory small vessel disease. A smallcoronary artery shows necrosis and inflammatory cellinfiltration of the wall, with giant cells, and the lumen isoccluded by thrombus. From a patient with Wegener'sgranulomatosis. H & E, x 115.

excluded before a diagnosis of primary cardio-myopathy can be made.

This classification of secondary cardiomyopathiesdiffers in presentation from the usual list found inpapers on cardiomyopathies, although the con-ditions included are the same. The known causes orassociations of heart muscle disease have beengrouped according to the pathological findingssince this is the view seen by the pathologist.

AcknowledgmentsThanks are due to the friends and colleagues who provided

material for many of the illustrations-Dr J. W. Lacey forCoxsackie myocarditis, sarcoidosis and muscular dystrophy,Dr M. Bennett for glycogen storage disease, and Dr J.Bradley-Watson for chronic myocarditis and cardiacamyloidosis. I am also grateful to Dr M. J. Davies forFigs. I and 3.

Figs. I and 3-10 inclusive are from Pomerance and Davics.Pathology of the Heart, 1972, and are reproduced by per-mission of Blackwell's Scientific Publications Ltd.

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HUDSON, R.E.B. (1970) The cardiomyopathies: order fromchaos. American Journal of Cardiology, 25, 70.

PERLOFF, J.K. (1971). The cardiomyopathies-current per-spectives. Circulation, 44, 942.

PERLOFF, J.K., LINDGREN, K.M. & GROVES, B.M. (1970)Uncommon or commonly unrecognized causes of heartfailure. Progress in Cardiovascular Diseases, 12, 409.

Cardiac involvment in individual diseasesABELMANN, W.H. (1966) Myocarditis. New England Journal

of Medicine, 275, 832.ABELMANN, W.H. (1971) Virus and the heart. Circulation,

44, 950.ALEXANDER, C.S. (1968) The concept of alcoholic myo-

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cardial changes in dystrophia myotonica. Acta MedicaScandinavica, 176, 535

BARBORIK, M. & DUSEK, J. (1972) Cardiomyopathy accom-panying industrial cobalt exposure. British Heart Journal,34, 113.

BASHOUR, F.A., MCCONNELL, T. SKINNER, W. & HANSON,M. (1968) Myocardial sarcoidosis. Diseases of the Chest,53, 413.

BRITISH MEDICAL JOURNAL (1971) Cardiovascular complica-tions from psychotropic drugs. Leading article. 1, 3.

BRIGDEN, W. (1964) Cardiac amyloidosis. Progress in Cardio-vascular Discases, 7, 142.


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BUERGER, L. & BRAUNSTEIN, H. (1960) Senile cardiac amy-loidosis. American Journal of Medicine, 28, 357.

BUJA, L.M. & ROBERTS, W.C. (1971) Iron in the heart.American Journal of Medicine, 51, 209.

BUJA, L.M., KHOI, N.B. & ROBERTS, W.C. (1970) Clinicallysignificant cardiac amyloidosis. Clinicopathologic findingsin fifteen patients. American Journal of Cardiology, 26,394.

EHLERS, K.H., HAGSTROM, J.W.C., LUKAS, D.S., REDO, S.F.& ENGLE, M.A. (1962) Glycogen-storage disease of themyocardium with obstruction to left ventricular outflow.Circulation, 25, 96.

FAJARDO, M.D., STEWART, J.R. & COHN, K.E. (1968) Mor-phology of radiation-induced heart disease. Archives ofPathology, 86, 512.

GAFNI, J., SOHAR, E. & HELLER, H. (1964) The inheritedamyloidoses: their clinical and theoretical significance.Lancet, i, 71.

GILROY, J., CAHALAN, J.L., BERMAN, R. & NEWMAN, M.(1963) Cardiac and pulmonary complications inDuchenne's progressive muscular dystrophy. Circulation.27, 484.

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HEWER, R.L. (1969) The heart in Friedreich's ataxia. BritishHeart Journal. 31, 5.

JAMES, T.N. (1967) Pathology of small coronary arteries.American Journal of Cardiology, 20, 679.

KLEMPERER, P., POLLACK, A.D. & BAEHR, G. (1941) Path-ology of disseminated lupus erythematosus. Archives ofPathology, 32, 569.

KOTEN, J.W., VAN GASTEL, C., DORHOUTMEES, E.J., HOLLE-MAN, L.W.J. & SCHUILING, R.D. (1965) Two cases ofprimary oxalosis. Journal of Clinical Pathology, 18, 223.

McKusICK, V.A. (1966) Heritable Disorders of ConnectiveTissue, 3rd edn. C. V. Mosby, St Louis.

MoUY, A. & TORDJMANN, M. (1968) Myocardial fibrosis inthe course of mucoviscidosis. Archives francaises depediatrie, 25, 687.

MULLER, O.F., BELLET, S. & ERTRUGRUL, A. (1961) Gly-cogen-storage disease. Report of a case with generalisedglycogenosis and a review of the literature. Circulation,23, 264.

ORAM, S. & STOKES, W. (1961) The heart in scleroderma.British Heart Journal, 23, 243.

PERLOFF, J.K. (1971) Cardiomyopathy associated with here-dofamilial neuromyopathic diseases. Modern Concepts ofCardiovascular Disease, 40, 23.

POMERANCE, A. (1966) The pathology of senile cardiac amy-loidosis. Journal of Pathology and Bacteriology, 91, 357.

PORTER, G. ( 1960) Sarcoid heart disease. New England Journaof Medicine, 263, 1350.

PYUN, K.S., KIM, Y.H., KATZENSTEIN, R.E. & KIKKAWA, Y.(1970) Giant cell myocarditis. Archives of Pathology, 90,181.

SLAMA, R., Josso, F. & ANTOINE, B. (1960) Myocardialmanifestations of oxalosis. Archives des maladies du coeuret des vaisseaux, 53, 917.

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WHITEHEAD, R. (1965) Isolated myocarditis. British HeartJournal, 27, 220.


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