JAM COll CARDIOl 879 19R3.1(3) R79-R6

PATHOLOGIC STUDIES

Sudden Death in Three Teenagers: Conduction System Studies

SAROJA BHARATI, MD, FACC, ROBERT BAUERNFEIND, MD, FACC. LYNN B. MILLER, MD, FACC, BORIS STRASBERG, MD, FACC, MAURICE LEV, MD, FACC

Chicago. Illinois

The pathologicsubstratefor sudden death in the middle•tient 3 (age 19, feinale) died suddenly at home. Autopsy aged or elderlyad!11tis usually ischemicheartdisease. revealedmitralvalve prolapse, thrombosis of the sino• In contrast,few dataare availableregardingthe pa• atrial(SA) nodeartery,andprematureaging, sclerosis thology of sudden death in teenagers.report This de• of the left side of thecardiacskeleton, with involvement scribes three teenagers without clinically suspectedof theventricularseptum more on the rightventricular disease dying suddenly. Patient 1 (age 15, male)side was and involvement ofatrioventricular the bundle and known to have rightventricularprematureventricular trifascicularconduction system. beats.Postmortemexamination revealed marked pre• In conclusion, unexpected deaths in three teenagers matureaging, sclerosis of thecardiacskeleton extending occurred withdemonstrablepathologic findings in the to the right side of the summit with fibrosis of theheart. left Two of the three patients had pro• and right bundlebranches.Patient 2 (age 17, male) waslapse, one of whom also had thrombosis or embolism of a trainedathlete who died during football scrimmage.thesinoatrialnodeartery.All three had sclerosis of not Autopsy revealed moderate mitral valve prolapseonly and the left side but alsothe right side ofthe ventricular markedprematureaging, sclerosis of the left side of theseptum with involvement of the conduction system. The cardiacskeleton, which extended to theventricular right anatomicsubstratedemonstratedin these three patients side, and secondary involvement oftrifascicular the con• could relate to lethalbradyarrhythmiaor tachyarrhyth• duction system with mononuclear cell infiltration.mia, Pa- or both.

The conductionsystemhas beeninfrequentlyexaminedin cerns threeapparentlyhealthyteenagerswho diedsuddenly. casesof suddendeath inapparentlyhealthyteenagersor The conductionsystem in all threesubjectswas studied young people.The reportsthus far show somepathdlogic extensivelyand the findings arediscussedin relationto changespertinentto theconductionsystemin some cases sudden death. (1-24) and none in others(25,26). Our presentstudy con-

CaseReports Case I From the Congenital Heart DIsease Research and Training Center,The patientwas a 15 yearold boy who was known to have Hektoen Institute for Medical Research, Chicago; the Departments ofright Pa•ventricularprematureventricularcomplexesfor anumberof thology ofNorthwesternUniversity Medical School, Chicago;Pntzker years,butwasapparentlyin good health.He suddenlycollapsed School ofMedicine,University of Chicago, Chicago; The Chicago Medical School,University of Health Sciences; Loyola University, Stritch Schoolwhile playingsoccerwith his friends.Therewas no historyof of Medicine,Chicago; The SectionCardiology, of Department of Medicine trauma.He waspronounceddeadon arrivalat theCanton-Potsdam and theDepartmentof Pathology,AbrahamLincoln School ofMedicine, Hospital,Potsdam,New York about35 minuteslater.Family University of Illinois, Chicago; and the Departments of Pediatrics, Med• historyindicatesthatonebrotherhas aorticstenosis. icine andPathology,Rush Medical College, Chicago. Present address for Drs. Bharati and Lev:Departmentof Pathology,Deborah Heart and Lung Postmortem examination.Acute congestionof the viscera Center,Browns Mills, New Jersey. This study was aided by Grant HLwas noted. 07605 from the National Heart, Lung, and Blood Institute, Bethesda,Heart. The heartweighed300 g Diffusefibrosisof the myo• Maryland,and the National Institutes of Health, Bethesda, Marylandcardiumwas seen at thegross level by the coroner'sphysician. ManuscriptreceivedSeptember13, 1982; revised manuscript received Left ventricularwall thickness em. All the valves October26, 1982, acceptedOctober29, 1982 measuredI 3 Address forrepnnts.Saroja Bharau, MD, Department of Pathology.andthe extramuralcoronaryarterieswerenormal. Deborah Heart and Lung Center, Browns Mills, New Jersey 08015 Conduction system, The heartwassentto (SB andML) in six

© 1983 bytheAmerican Collegeof Cardiology 0735-1097/83/030879-8$0300 880 J AM COLL CARDIOL BHARATI ET AL 1983.1(3) 879- 86

pieces. One fragment that wasapparentl y the main partof the heart was sent from the emb almer. The other pieces of the heart were sent by the pathol ogist. The superior vena cava region , the sinoatrial (SA) noderegion,the atrioventricular (AV) node region, the region and the right and left bundle branch regions were recognized in the part sent byembalmer. the The block containing the SA node and its approaches was serially sectioned and every )Oth section was retained and con• secutively stained withhematoxylin-eosin , Weigert-Van Gieson and Gomori trichromestains . The block conta iningapproach the es to the SA node , the AV node , the AV bundle and the was seriallsectioned y and every 10th section was re• tained . Theapproachesto the AV node and the peripheral portions of the bundlebrancheswerealternatelystained withhematoxylin• eosin andWeigert-VanGiesonstains. Theremainderwas stained with Gomori trichromein addition.The remainderof the myo• cardiumwas cut into blocks and two sections were taken from each block andstainedwith hematoxylin-eosin and Weigert -Van Gieson stains. In thismanner566sections were examined . These were matched withsections of from a similar age group (controls). Microscopic examination.SA node. Fatty infiltration was present at the headof the node . A slightmononuclearcell infil• tration was also seen. Approaches to SA node. There was moderate fatty infiltration. Approaches to AV node. A slight infiltrationmononucle of ar cells was seen. The re was also fatty infiltration. AV node. A slightmononuclear cell infiltration was present. AV bundle. Therewas slight fibrosis in the penetrating portion . A large thin-walledvascularchannel coursed through the pene• tratingortion p . Left bundle branch. There was moderate fibrosis in the beginning. Figure1. Case I. Right bundle branch showingfibros is(arrows). Weig• Right bundle branch . Slight fibrosis was present in the first crt-Van Gieso n slam X45, reduced by 25%.= Vventricular septum part , moderatein the second and considerable in the third (Fig. I). Summit of the ventricular septum . There werenumerousfocal areas of fibrosisthroughoutthe septum, especiallymarked ante• riorly on the right side. Some of the arteriolesthickened were (Fig. 2). Postmortem examination.On gross examination, no ana• Left ventricular myocardium . Large areas of fibrosis were pres•tomic abnormalities were noted in other organs. ent beneath theepicardiumin all sections. Heart. The heart weighed 355 g. There werehypertrophy and dilation of the right . The whole region of the pars membranacea and the adjacent aorticof leafletthe mitral valve Case 2 were thickened for this subject's age andembled res those of a The patient was a 17 year old boy, an honor student andperson a aged 50 years. The mitral orifice was somewhat enlarged. trained athlete, who died durin g football scrimmage. HeThe was posterior leaflet was enlarged and divided intocompo three• I.9 m tall and weighed 77.) kg. The mother related that thenents. boy There was a mild to moderate amountedundan of rcy in the had a temperatureof40.5C 6 month s before death and a physicianentire leaflet. All other valves were normal.coronar They made a diagnosis of viralinfection. Threedays later the boy went were normal. to footballpracticebut sat on the sidelines. Subsequentl y he had Conduction system. The SA and AV nodes and their ap• no complaints andengagedin full athletics . A day or two beforeproaches, the AV bundle and bund le branches up to the periph ery his death, he was noted to be moving his shoulder and claimedwere serially sectioned . Every 20th section was taken from the SA he had a little musclescomfort di . He also had a head cold. The node region. every 10th section from the AV node10 the up day before and on the morn ing of his death he did not eat well.beginning of the bundle branches and every 20th section from the He had beenworkingout for about I hour and 10 minutes whenperiphery of the bundle branches. The remainder of the heart was he collapsed. cut into block s and two sections were taken from each block . All The parents said that the boy had receivedthorough a physic al sections were alternately stained with hematoxylin -eosin and Weigert• checkupapproximately3 weeks before and was reported to be inVan Gieson stains. In this manner , a total of 732 sections were excellentcondition. studied. CONDUCTION SYSTEM IN SUDDEN DEATH JAM cou.CARDIOl 881 1983.1(3)879-86

: , J•, • r.

I

'/

,I

,I, ,

I "I,. I ' , ~ ,

," { ,

I' II I

; •. r

Figure3. Case2. Chromeinflammatorycells(arrow)in thepenetrating Figure2. Case I. Summitof theventricularseptumshowingfibrosison partof thebundleof His Hematoxylin-eosinstainX150,reducedby27o/c. therightventricularside(arrows).Weigert-VanGiesonstainXIO, reduced B = penetratingpartof thebundleofHis; CFB = centralfibrousbody. by27%. B = bundleofHis; LBB = leftbundlebranch;N = AV node; RA = rightatrium;V = ventricularseptum.

Microscopicexamination.SA node. There were no changes. right ventricle. The latter was alsoIn seenthe left ventncle, lower Approaches to the SA node. An occasional infiltrationof mono•part of the ventricular septum and atrial septum. The ventricular nuclear cells was noted. septum also showed a disarray pattern focally. Vacuolar degen• Approaches to the AV node. Distinct small zones of mono• erative changes in nuclei of nerve cells were also noted in the nuclear cell infiltration were accompanied by fatty infiltrationatrial and septum. fibrosis. Mitral valve. There was some loosening of the fibrosa at the AV node. A fine dispersion of mononuclear cells was present.base. AV bundle. penetrating portion. Mononuclear cells were pres• ent in the penetrating portion of the AV bundle with an increase in and elastic fibers (Fig. 3). Case 3 AV bundle, branching portion. There was an increase in col• The patient was a 19 year old girl, a good and stable college lagen and elastic fibers. student, who died suddenly. She had recurrent dizzy spells a few Left bundle branch. Vacuolar degeneration of scattered Pur•days before death. At II :00P.M. while watching television, she kinje cells was in evidence throughout, associated with awas fine startled when her mother entered the living room, and ex• mononuclear cell infiltration. claimed,"You scared me, I thought you werebed!" in She then Right bundle branch. This branch was large. The first andfell to the floor dead. There were no signs of foul play. In the second parts were distinctly fibrosed; the third part was normal.past, she had had recurrent urinary tract infection which had re• Summit of the ventricular septum. There was considerable fi•curred2days before death. Her father died suddenly 4 years earlier brosis on the left and right sides of the septum, more markedat 36 in years of age (autopsy was not done), and his father died a the right side (FIg. 4). This isnormally not seen in a 17 year old few months later, apparently of heart failure,With a history of boy. repeated episodes"passing of out."There were two sisters of the Myocardium elsewhere. Slight fatty infiltration was notedWith father with heart problems. After her father's death, the patient a focal increase in eosinophilic staining of myocardial cells inhad the a psychologic reaction of moderate severity and at a medical 882 J AM COll CARDIOl BHARATI ET Al 1983.1(3):879- 86

Figure 5. Case 3. Leftatrial(LA) and left ventricular (LV) viewof the heartshowing themuralvalve prolapse(arrow)

hematoxylin-eosin. Weigert-Van Gieson and Gomori trichrome stains. The remainder of the sections were stained alternately with hematoxylin-eosin and Weigert-Van Gieson stains. In this manner. 620 sections were examined. Microscopicexamination.SA node. There was an organized thrombus or embolus fillmg part of the SA node in the node (Fig. 6). The arterioles were thickened. Figure4. Case2.Summitof theventricularseptumshowmg fibrosis more Approaches to the SA node. A considerable amount of fat was on therightventricularside (F).Weigert-Van GiesonstainX30, reduced present for this patient' s age. by 27%. B = penetrating part ofbundle the of HIS , V = ventricular septum. Approaches to the AV node. Fat tissue was more abundant than usual for this age. with edema. There was focal infiltration of mononuclear cells. Fibrosis of the nerves with penneural fibrosis was present. evaluation at that time, all tests were normal except for the presenceAV node . This was somewhat compressed against the central of a urinary infection. She had complained of occasional episodesfibrous body. with slight mononuclear cell infiltration. of headaches, dizziness and spinning but these were not evaluatedCentral fibrous body, The central fibrous body sent a thick medically. Her two younger sisters, 17 and 9 years old. bothprong have of connective tissue to the (Fig. 7). mitral valve prolapse and are taking small doses of propranololAV bundle. The penetrating portion was septated (Fig. 8). There (both are asymptomatic according to the clinician). was swelling of the cells on the periphery with acute degeneration Postmortemexamination.Thrs was essentially normal exceptof cytoplasm in cells located in the center with considerable fine for acute pulmonary congestion and chronic thyroiditis of moderatefibrosis. The branching bundle was short and showedfibrosis.The degree. bifurcation showed fibrosis present on the nght Side. Heart. The heart weighed 220 g. There was slight hypertrophyLejt bundle branch There was acute degeneration of the pe• and enlargement of the left and right ventricle. Theripheral mitral cells with slight fibrosis of the anterior radiation. orifice was normal in size. The valve showed distinct prolapseRight of bundle branch . This showed slight fibrosis with acute the posterior leaflet which was redundant and nodose (Fig.degeneration. 5). This redundancy extended to the posterior part of the anteriorVentricular septum, Considerable librosis. more on the right leaflet. All other valves and the were normal.Side than on the left. was noted at the base. with thickening and Conduction system. The SA node and Its approaches. the AVnarrowing of the large arterioles (Fig. 7). node and its approaches. the AV bundle and the bundle branchesMitral valve, There was loosening of the fibrosa with increase up to the level of the were serially sectionedin andspongiosa. every 10th section was retained. The remainder of the heart wasMyocardium. There were no changes in the left ventricle. There cut into blocks and two sections were taken from each block.were The slight fatty infiltration and slight hypertrophy of myocardial sections of the conduction system were stained consecutivelycells with in the right ventricle. CONDUCTION SYSTEM IN SUDDEN DEATH J AM COLL CARDIOL 883 1983.1(3):879-86

Figure6. Case 3. Sinoatrial note (N) and its approaches (A) with an organized thrombus or embolus in the sinoatrialarter.(arrow). Hema• Figure7. Case 3. Summit of the ventricular septum (V) with more fibrosis toxylin-eosin stain X75, reduced by 25%. (arrow) on the right ventricular side (R). Weigert-Van Gieson stain X22.5, reduced by 22%. Note also the arteriolar thickening in the summit of the ventricular septum== B beginning of the penetrating part of the bundle of His; L == left ventricular side.

Discussion Previousreportsof conductionsystem in young per• and AV nodes and in the atrialpreferentialpathways(4,24); sons dyingsuddenly.Suddendeath in young people has 5) ganglionitisand neuritisnear the sinus node, AV node beenassociatedwitharterioscleroticheartdisease(27-35), and atrialseptum(19);6) compressionof the AV node by congenitalanomaliesof the coronaryarteries(22,28,34), anelongatedleftatrium,mitral orifice or invasionofcalcium includingoriginofthe leftcoronaryfrom the right sinusof in anabnormallyformedcentralfibrous body(24);7) per• Valsalva,myocarditis(6,28,29,31 ,37,38):cardiactumors sistent fetaldispersionofAV node, His bundle andcentral (5,28,29), obstructivecardiomyopathy(29,34,36,37),Jer• fibrous body(II); 8) infiltrationofmononuclearcells in the vell-Lange-Nielsondisease(36), Friedreich'sataxia(11), conductionsystem(4); 9) fibromacompressingthe His bun• mitral valveprolapse(36), acuteaneurysmof the aortic dle (5): 10)a right-sidedor septatedHis bundle(17,24); cusp withthrombus(37), endocardial fibroelasto sis(37), II ) fibrosisofthe AV bundle(6,14,23); 12)hemorrhagein progressivemusculardystrophy(II) and intramuralleft the Hisbundle(7); 13) lipomatous interruptionof the His coronaryartery(39,40).Whereconductionsystemstudies bundle(14);14)markednarrowingof the AV nodal artery have been donevarious , abnormalitiesin theconduction (6,8,10,22); and 15)disruptionofthe fibersofthe proximal system have been foundincluding: I) narrowingof the partof both bundlebranches(6,23).However,in many sinus nodeartery(1,10,II ,22,26).with fibrosis or old scars casesofsuddendeath lesions in theconductionsystemare (1,8,14);2) recenthemorrhage in the SA node andadjacent notevident(15,26). areas(I); 3)abnormalcourseandbranchingofthe SA node Presentcases.In Case I, there wasmarkedpatchyfi• artery(14); 4)fattyinfiltrationin theapproachesto the SA brosis of themyocardiumofunknownorigin.The conduc- 884 J AM COLL CARDIOL BHARAT I ET AL I'JS3.1(3) S7'J-Kf>

or embolus in the SA node artery with thickening of the arterioles, fatty infiltration of the approaches to the SA and AV nodes, infiltration of mononuclear cells in the ap• proaches to the AV node and in the AV node. with fibrosis of nerves and perineuralfibrosis, septation of the His bundle with swelling of the cells in the periphery with acute de• generation of the cytoplasm of the cells in the center. and fibrosis of the branching bundle. Thisffi iscult di to cate• gorize as any disease entity with the exception of the pro• lapsed mitral valve. Aging and fibrosis of summit of ventricular sep• tum. One process is present in all three cases. There is distinctly increased aging of the summit of the ventricular septum. This surprisingly involvesright the side ofthe sum• mit more than the left. In the aging process, which we have called sclerosis of the left side of the cardiac skeleton. the left side is more involved. and this may affect the bundle and bundle branches infibrotic a or calcific process. Oc• casionally the AV node may be affected. In our material this usually occurs after the age of 40 (41). The process of fibrosis of the summit of the ventricular septum seen in our three cases is characterized by a prom• inent prong of connective tissue proceeding down to the tricuspid anulus from the central fibrous body. This is as• sociated with considerablefibrosis of the center and right side of the summit. with thickening of the large arterioles in two of the three cases. We do not know the cause of this phenomenon in these teenagers.It is possible that a previous myocarditis may have produced stresses in the fibrous skel• Figure 8. Case 3. Septated penetrating part of the bundle of HIs (B)eton with of the heart in thefirst two cases, or the prolapsed line librosis. Weigert-Van Gieson stain X45. reduced by 250/(,= left L mitral valve in Case 3 may in some way be associated with ventricular side.= R right ventricular side with fibrosis.= ventricular V septum. changes in thefibrous skeleton. It is interesting that this sclerosis is associated withfibrotic changes in the right bundle branch, in contrast to the sclerosis of the left side of the cardiac skeleton where the left bundle branch is in• tion system revealed a slight mononuclear cell infiltrationvolved (4 1). in the SA and AV nodes and their approaches.fi slightbrosis Mechanism of suddendeath.The mechanism of sud• of the AV bundle, moderatefibrosis of the left bundle branchden death as reported in published studies is ventricular and more marked fibrosis of the right bundle branch.fi Thisbrillation or asystole. We do ndt know how the changes may be interpreted as a healing or healed myocarditis,in with the conduction system are related to these phenomena. residual chronic inflammatory and fibrotic changes inIn the our Cases I and 2, it is possible that changes in the conduction system. myocardium itself may have initiated ventricular fibrillation. In Case 2, there were hypertrophy and dilation ofThe the septated bundle in Case 3 may be relatedtothe assumed right ventricle and a somewhat elongated (floppy) mitralarrhythmia in this patient. We have previously described valve. Focal acute degenerative changes were seen insuch all afinding in another case of arrhythmia (\ 7). The fi• parts of the heart. The conduction system showed mono•brosis of the nerves at the approaches to the AV node in nuclear cellfi inltration in the approaches to the SA and AVCase 3 may be associated with a terminal arrhythmia. James nodes, penetrating bundle and left bundle branch and fibrosiset al. (19) have shown the relation of ganglionitis and neu• of both bundle branches. Thesefindings may be interpretedritis in some cases of sudden death. We believe that the as a myocarditis involving mostly the conduction system.nerves can be incriminated only when they are more mark• In Case 3, there was distinct prolapse of the posterioredly involved than the surrounding tissue. In Case 3. the leatlet of the mitral valve and to a lesser extent of the anteriorfibrosis of the nerves in the approaches to the AV node is Icatlet. The myocardium revealed no remarkable change.in the midst of fatty infiltration without fibrosis. The nerve The conduction system showed a small organized thrombuschanges may therefore be of significance. CONDUCTION SYSTEM IN SUDDEN DEATH J AM COLL CARDIOL 885 1983.1(3) 879-86

The fat ty infiltration adjacent to the SA node and its fetal dispersron of the and HIS bundle Within the central fibrous body. Circulation 1976:53:1026-34. approaches and in the approaches to the AV node in Case 12. James TN. Man llery RJ Jr. Mam ou HJL De Subuaners Mortibus I, in the approaches to the AV node in Case 2 and in theXI Young girl wuh palpitations. Circulanon 1975;51:743-8. approaches to the SA and AV nodes in Case 3 may be13 James TN. Marshall TK DeSubrtaneivMortibus. XVII.Mulufocal related to an arrhythmia when seen in young people. Fattystenosis due to fibromuscular dysplasia of the smu-, node artery. Cir• infiltration has previously been noted in association withculation 1976.53'736-42 arrhythmia (17). The cause of the thickeningof the arterioles14 Gotoh K A histopathological study on the conduction system of the so-called" Pokkuridisease" (sudden unexpected cardiac death of un• in the SA node and the presence of an organized thrombusknownong rn m Japan) JpnCrrc J 1976:40.753-6!L or embolus in the SA node artery in Case 3 is not known.15. James TN, De Subuancis Mornbus XXVIII. Apoplexy of the heart. The thrombosis or embolus in the SA node artery may beCirculation 1978;573X5-91. related to the mitral valve prolapse. 16. James TN. FroggattA P. tki nsonWJ Jr. et al. DeSubuanei-,Mortibus Thus, the cause of sudden death in these three teenagersXXX. Observationson the pathophysrology of the long QT syndromes wrth spec ialreference to the neuropathology ofheart. theC irculatron may be associated with the sclerosis of the right side of the1978:57.1221- 31 summit of the ventricular septum due to healed or active17. BharauS. Bauemfemd R. Scheinman M. et al. Congenital abnor• myocarditis in Cases I and 2 and to a prolapsed mitral valvemalities of the conduction system inpatients two with tachyarrhyth• in Case 3, and the effects of these conditions on the con•rruas Circulation 1979:59:595-606 duction system. The patchy fibrosis seen in the ventricular18. Davies M1, Popple A. Sudden unexpected cardiacath- dea practical myocardium on the right side of the summit may facilitateapproach to the forensic problem. Histopathology 1979;3:255-77. a reentrant phenomenon that might result in ventricularfi• 19. James TN.Zl pe ~ DP. Finegan RE. Eisele JW. Carter JE.Cardiac ganghomnv associated with sudden unexpected death Ann Intern Med brillation and sudden death. We cannot, however, overlook1979:91.727- 30. the fatty infiltration in the approaches to the SA and20 AV James TN lntracardrac ganghonms and sudden death. Herpev of the nodes, or the fibrosis of the nerves in the approaches to theheart') Trans Am Clm Climatol Assoc 1979:977-9 1:10 AV node and thrombosis of the SA node artery in Case2 3,1 James TN. Pearce WN Jr. Givhan EG Sudden death while dn vmg. as related to arrhythmia and sudden death. It appears thatRole 01smu s penn odal degenerationcardiac and neuraldegenerat ion sudden death in young people may be produced by variousand ganghoruus Am J Cardiol 19X0:45.1095-102. abnormalities in the conduction system and the myocar•22. Maron BJ.RobertvWe. McAlhstcr HA. Rovmg DR. EpsteinSE Sudden death in young athletes Circulation 1980:62:2I X-29. dium. Much more work needs to be done to answer the 23. Schneider J. Der plotzliche Herzrod als Folge crncr Rcrzleuungssto• riddle of sudden death in young people. rung. J Schweiz Med Wschr 19XI;III :582- 9 1. 24. Bharan S. Cranston AS. Licbson PRoLoeb HS. Rosen KM. Lev M. The conduction system in mitral valve prolapse syndrome with sudden death Am Heart J 19XI.IOI67-70 :6 . 25. Voigt J. The examination of the conduction system of the heart m References medicolegalpracuce.Leg Med Ann I977;X3X3-95 I. James TN . Froggatt P, Marshall TK. Sudden death m young athletes26. Pederson PK. Poor results in attemptmg to demonstrate the cause of Ann Intern Med 1967,67:1013-21. death byexammatronof theconduction system01the heart mcases 2. Green R,KorovetzMJ, Shanklin DR, DevuoJJ,Taylor WJ Sudden of sudden death. ForenSC I lnt 19XO.16:2XI-2. unexpected death m three generations Arch Inlem Med 1969;124.359•27 Berkher serSW Cardiovasculardiseasem the younger age group. 63. Aeros pace Med1970.41:1307-9 3. Schwartz CJ, Walsh WJ The pathologicbasisof sudden death. Prog 28. Jokl E, McClellanJT. Exercise and ca rdiac death. JAMA Cardrovasc Dis 1971,13:465-81. 1970;213.1489-91. 4. Gault JH, Cantwell 1, Lev M, Braunwald E. Fatal familial cardiac29 Jokl E. Exercise and cardiac death JAMA 1971.218:1707-13 arrhythmias. Histologic observations on the cardiac conductionsys• tem. Am J Cardiol 1972;29:548-53. 30. Kuller L. Cooper M. Perpcr J. Epidcrmology of sudden death . Arch Intern Med 1972:129.714- 9. 5. James TN. Derek JL, Carson DJL, Marshall TK.Subnaners De Mor• tibus. I. Fibroma compressing the His bundle. Circulation 1973;48.428• 31 We inbergM Sudden cardiac death. YaleIOI J BMed 1 9 7 8 . 51 : 207~ 33. 17 6. James TN , Armstrong RS, Silverman J, Marshall TK. De Subitaneis32 Warren SD.OI Bce JB. Bloor e. V rcweg WVR The athletic heart Mortibus. VI. Two young soldiers. Circulation 1974:49:1239-46. rcvrsrted West J Med 1979:131:44 1- 7. . 7. Ferris JAJ. Conducting tissue changes m sudden death.CI Law Med S 33. Woodhouse SP. Anderson KR. MulheronOJ Sudden death of a young 1974;14:36-9. man dunn g a sponsored Jogging event NZ Med J 1980.91.454- 6. 8. James TN , Hackel DB, Marshall TK. De Subitaneis Morubus V34 Lynch P.Soldiers.sport. and sudden death. LancetXO ;1.1235 19 -7 Occluded A-V node artery. Circulanon 1974;49.772-7. 35 John-on WD. Strong JP. OalmannMe. Newman WPIII. Tracy RE. 9. LieJT,Titus JL. Pathology of the myocardium and the conduction Rock WA Jr Sudden death from coronary heartdiseaseIII young men system in sudden coronary death. Circulation 1975,52(suppl111).111• Arch Pathol Lab Med 19X1.105'227- 32 41-52 36. Barnes RN. Martt JM Sudden death syndrome Texas Med 1976.72.49• 10. Lie IT. Histopathology of the conduction system in sudden death from57 coronary heart disease.Crrcul atron1975;51:446- 52. 37. Mant AK Sudden death due to unusual cardiac pathology. Forensic II . James TN , Marshall TK DeSubrtanersMornbus, XVIII. Persistent Sci 1976;8:7-8 886 J AM cou,CARDIOl BHARATl ET Al 1983,1(3)879-86

38. HayashiKD, Lew" ER Sudden death in a marathon runner with40. Cheitlin MD. The intramural coronary artery: another cause for sudden widely patent coronary arteries. Clin Cardiol1980;3:288-91. death with exercise? (editorial). Circulanon1980;62:238-48. 39. Morales AR, Romanelli R, Boucek RJ. The mural left anterior de•41. Lev M. The n..nnal anatomy ofconduction the system in man and Its scending coronary artery, strenuous exercise and sudden death. Cir•pathology in atrioventricular block. Ann NY Acad1964;1 Sci II:817• culatIon1980;62.230-7. 29.