11
Tumor Metastasis to the Heart By J. M. YOUNG, M.D., AND I. RALPH GOLDMAN, M.D., F.C.C.P. This article is a survey of 476 consecutive cases of tumor death for heart involvement. The some- what selected group of cases (from a Veterans Administration hospital) shows an incidence of cardiac metastasis of 19.1 per cent. The bulk of tumors metastasizing to the heart were broncho- genic carcinoma, malignant melanoma, malignant lymphoma, and carcinoma of the pancreas and esophagus. Electrocardiographic changes were frequent and correlated fairly closely with the anatomic extent of the disease. The related literature is reviewed. M YOCARDIAL involvement by neo- plasms arising elsewhere in the body is no longer considered rare. A survey of the literature discloses a gradually rising incidence of myocardial metastasis as this subject is more closely explored. It has re- cently been estimated that more than 500 instances of tumor metastasis to the heart are now recorded, and more than 20 of these were diagnosed before death.1 In the earlier litera- ture, summarized by Morris,2 Yater,3 Lisa and co-workers,4 Doane and Pressman,5 and Willis,6 one finds that the incidence figures were almost always below 2 per cent. Often, however, the number of tumor deaths was not mentioned. Carcinoma of the breast, lung, esophagus, pancreas, malignant melanoma, and malignant lymphoma are mentioned most frequently in the literature as the primary tumor. In fact, almost all types of tumors have occasionally metastasized to the heart. Very often the total of tumors of each kind is not given. Notable exceptions are the series of Herbut and Maisell7 and Willis.6 Scott and Garvins found a 10.9 per cent incidence of cardiac involyement in 1082 cases of tumor death. Likewise, Dimmette9 re- ported a figure of 8.35 per cent in 455 cases. This present report does not represent the expected frequency of cardiac metastasis in a general hospital, but rather that found in a large general medical and surgical Veterans Administration hospital which is also a refer- ence center for thoracic surgery and for many cases of malignant lymphoma. Another factor in our high incidence is probable longer survival From the Laboratory Service and Medical Service, Veterans Administration Medical Teaching Group (VAMTG) Hospital, Memphis, Tenn. 220 of our cases, since many remained hospital cases throughout their terminal course. This longer survival likely has allowed more wide- spread metastasis. MATERIAL During approximately six and one-half years 1400 autopsies have been performed, and 586 of these were upon patients who had died of tumor (41.9 per cent). Leukemia cases and brain tumors have been excluded, since the former show cardiac infiltrations frequently, and the latter almost never metastasize outside the central nervous system. (See table 1.) In 54 cases of leukemia there were 25 with myocardial infiltrations, and seven of these were of moderate or marked degree (fig. 1). Fifteen of 30 granulocytic leukemia cases and 5 of 16 lymph- old leukemia cases disclosed cardiac infiltrations. In the remaining 476 cases of tumor death there were 91 with cardiac involvement, an incidence of 19.1 per cent. Examination of table 2 explains this high percentage since a large proportion of our cases have been bronchogenic carcinoma, malignant melanoma, malignant lymphoma, and carcinoma of the pancreas and esophagus. Six of these cases have been reported previously in detail by Lefkovits.'0 In all cases there were metastases to sites other than the heart. In most of the reported series the right side of the heart has been more frequently involved than the left, but in some series6-8 more nearly equal involve- ment of the right and left sides has been noted. In our cases with hematogenous metastases, the right side was involved alone in but seven cases, the left side in 13 cases, and both sides in nine cases. There was bilateral involvement, considering all metastatic pathways, in 63 cases and endocardial involvement only in two cases. In the other six cases insufficient TABLE 1.-Incidence of Cardiac Metastases Total Autopsies.............. 1400 Tumor Deaths .............. 586 (41.9%) Tumor Deaths Less Leuke- mias and Brain Tumors..... 476 Cases with Heart Metastases.. 91 (19.1%) Circulation, Volume IX, February, 1954 by guest on July 14, 2018 http://circ.ahajournals.org/ Downloaded from

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Tumor Metastasis to the HeartBy J. M. YOUNG, M.D., AND I. RALPH GOLDMAN, M.D., F.C.C.P.

This article is a survey of 476 consecutive cases of tumor death for heart involvement. The some-what selected group of cases (from a Veterans Administration hospital) shows an incidence ofcardiac metastasis of 19.1 per cent. The bulk of tumors metastasizing to the heart were broncho-genic carcinoma, malignant melanoma, malignant lymphoma, and carcinoma of the pancreas andesophagus. Electrocardiographic changes were frequent and correlated fairly closely with theanatomic extent of the disease. The related literature is reviewed.

MYOCARDIAL involvement by neo-plasms arising elsewhere in the bodyis no longer considered rare. A survey

of the literature discloses a gradually risingincidence of myocardial metastasis as thissubject is more closely explored. It has re-cently been estimated that more than 500instances of tumor metastasis to the heart arenow recorded, and more than 20 of these werediagnosed before death.1 In the earlier litera-ture, summarized by Morris,2 Yater,3 Lisaand co-workers,4 Doane and Pressman,5 andWillis,6 one finds that the incidence figureswere almost always below 2 per cent. Often,however, the number of tumor deaths was notmentioned. Carcinoma of the breast, lung,esophagus, pancreas, malignant melanoma,and malignant lymphoma are mentioned mostfrequently in the literature as the primarytumor. In fact, almost all types of tumorshave occasionally metastasized to the heart.Very often the total of tumors of each kind isnot given. Notable exceptions are the seriesof Herbut and Maisell7 and Willis.6

Scott and Garvins found a 10.9 per centincidence of cardiac involyement in 1082cases of tumor death. Likewise, Dimmette9 re-ported a figure of 8.35 per cent in 455 cases.This present report does not represent theexpected frequency of cardiac metastasis ina general hospital, but rather that found ina large general medical and surgical VeteransAdministration hospital which is also a refer-ence center for thoracic surgery and for manycases of malignant lymphoma. Another factorin our high incidence is probable longer survival

From the Laboratory Service and Medical Service,Veterans Administration Medical Teaching Group(VAMTG) Hospital, Memphis, Tenn.

220

of our cases, since many remained hospitalcases throughout their terminal course. Thislonger survival likely has allowed more wide-spread metastasis.

MATERIAL

During approximately six and one-half years1400 autopsies have been performed, and 586 ofthese were upon patients who had died of tumor(41.9 per cent). Leukemia cases and brain tumorshave been excluded, since the former show cardiacinfiltrations frequently, and the latter almost nevermetastasize outside the central nervous system.(See table 1.) In 54 cases of leukemia there were 25with myocardial infiltrations, and seven of thesewere of moderate or marked degree (fig. 1). Fifteenof 30 granulocytic leukemia cases and 5 of 16 lymph-old leukemia cases disclosed cardiac infiltrations.

In the remaining 476 cases of tumor death therewere 91 with cardiac involvement, an incidence of19.1 per cent. Examination of table 2 explains thishigh percentage since a large proportion of our caseshave been bronchogenic carcinoma, malignantmelanoma, malignant lymphoma, and carcinoma ofthe pancreas and esophagus. Six of these cases havebeen reported previously in detail by Lefkovits.'0In all cases there were metastases to sites other thanthe heart.

In most of the reported series the right side of theheart has been more frequently involved than theleft, but in some series6-8 more nearly equal involve-ment of the right and left sides has been noted. Inour cases with hematogenous metastases, the rightside was involved alone in but seven cases, the leftside in 13 cases, and both sides in nine cases. Therewas bilateral involvement, considering all metastaticpathways, in 63 cases and endocardial involvementonly in two cases. In the other six cases insufficient

TABLE 1.-Incidence of Cardiac Metastases

Total Autopsies.............. 1400Tumor Deaths.............. 586 (41.9%)Tumor Deaths Less Leuke-mias and Brain Tumors..... 476

Cases with Heart Metastases.. 91 (19.1%)Circulation, Volume IX, February, 1954

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J. M. YOUNG AND I. RALPH GO()LD)MAN

$1

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p:

?g.i4i

FiG. 1 (top left). Subepicardial and myocardial infiltration in chronic granulocytic leukemia.(X 45)

FIG. 2 (top right). Bronchogenic carcinoma. Note dilated lymphatics filled with tumor tissue andthe accompanying inflammatory reaction. (X 45)

FIG. 3 (middle left). Myocardial tumor nodules in malignant melanoma. (X 45)FIc. 4 (middle right). Lymphocytic lymphosarcoma. Note widespread invasion and separation of

muscle fibers and bundles. (X 45)FIG. 5 (bottom). Testicular tumor with hematogenous chorionepithelioma cardiac metastasis.

Note necrosis accompanying tumor. (X 45)

data were given to classify the extent and locationsof the metastases.The epicardial and subepicardial lymphatics were

most often involved in our cases. Sixty cases showedinvolvement in this manner, while 29 had myo-

cardial (hematogenous) metastases and two hadendocardial implants. In the group with subepi-cardial lymphatic involvement, the right side of theheart, particularly the auricle, was most affected. Inmost cases the extent of the metastasis was grossly

221

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TUMOR METASTASIS TO THE HEART

TABLE 2.-Tumor Types with Percentages ShowingHeart Metastases

Primary Site

Bronchus....................Malignant Melanoma........Malignant Lymphoma.......Pancreas....................Esophagus...................Kidney.....................Testicle.....................Stomach.....................Prostate.....................Bladder.....................Larynx......................Skin.........................Adrenal.....................Paranasal Sinus.............Lip..........................

TotalCases

10917603333

159

342715115322

Metas-tasis toHeart

40119764422111111

evident, but in 12 the metastases were of micro-scopic proportions. No case having only parietalpericardial involvement is included as a case withmetastasis.The high incidence of mediastinal involvement

in tumors metastatic to the heart has been noted bymany observers, and this has been stressed partic-ularly by Morris2 and Lymburner." The filling ofthe lymph nodes and mediastinal tissues blocks thelymphatic channels draining the heart and allowsretrograde extension through the subepicardiallymphatic vessels. In this series the mediastinumwas significantly involved in 66 cases (72.5 per cent);this was very evident in the cases of bronchogeniccarcinoma where 37 of the 40 cases had mediastinalinvolvement.

Electrocardiograms were available for study in35 cases. We have excluded 12 because of priorchanges due to other forms of heart disease. Theremaining 23 were obtained within six months ofthe time of death, and a summary of the findingscorrelated with the anatomic changes is presentedin table 3. There was positive correlation in 16instances; the changes noted most frequently weresinus tachycardia (11 times), low voltage (10 times),changes typical of pericardial or myocardial involve-ment (10 times), auricular fibrillation (four times),auricular flutter (three times), varying degrees ofA-V block (two times), and bundle branch block(one time). In 14 cases the electrocardiographictracings were taken within one month of death.While the various rhythm changes and degrees ofblock were often transient, low voltage, once it ap-peared, remained. Low voltage often accompaniedpericardial effusion and obliteration of the peri-cardial sac by tumor and adhesions.

TUMORS BY TYPES

Bronchogenic CarcinomaIn the 109 cases in this group, 40 disclosed

cardiac involvement. Twenty-three tumorsarose in the right lung, 16 in the left lung,and one was a terminal bronchiolar carcinomawith bilateral involvement. In 37 of the 40cases there was definite mediastinal involve-ment, and this most often was marked. Theroute of involvement was via the lymphatics(retrograde extension) in 34 cases and hematog-enous in six. In the cases showing subepi-cardial tumor, the right auricle was usuallymore markedly involved (see fig. 2).The pericardial sac was obliterated by

tumor and adhesions in seven cases. Therewas significant pericardial effusion in 14 cases;this was sanguineous in eight. The heartweight was above 350 Gm. in 16 cases, butonly two of these weighed more than 550 Gm.

Electrocardiographic tracings were made in16 cases. Table 3 lists the cases and correlatesthe anatomic findings and electrocardiographicchanges. Those showing low voltage usuallyhad obliteration of the pericardial sac or peri-cardial effusion. A pattern of epicardial ormyocardial involvement was present in sixtracings, and in two of these, serial tracingsdisclosed partial resolution of the process.

Malignant MelanomaThis tumor most often involves the heart by

the hematogenous pathway (see fig. 3).Eleven of our 17 cases disclosed cardiac me-tastases (64.7 per cent), and in eight themetastases were blood-borne. In three therewas significant serous pericardial effusion.Mediastinal involvement was notable in fivecases, and three of these showed subepicardialmetastases. Heart weight was increased inthree cases where numerous tumor noduleswere present. In one case, these nodules ul-cerated through the endocardium, resultingin implants between the trabeculae and on thevalves. Unfortunately, in only one case wasan electrocardiogram taken. This disclosed lowvoltage and a pattern suggestive of myo-cardial spread.

__

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TABLE 3.-Correlation of Anatomic Findings and Electrocardiographic Changes

Case Anatomic Findings Electrocardiographic Changes Correlation

Bronchogenic Carcinoma

Obliteration of pericard. sac by fibrousadhesions and tumor.

Many tumor nodules through subepi-card. region with infiltration of outerlayer of myocard.

Subepicard. lymphatic and pericard.involvement by tumor tissue.

Numerous tumor nodules in left aur.,

right vent. and I.V. septum, and one

nodule present in septum betweenthe tricuspid and mitral valve rings.

Slight subepicard. lymphatic involve-ment with invasion of outer layer ofmyocard.

Sanguineous pericard. effusion.Marked subepicard. lymphatic in-volvement with infiltration of outermyocard. layer by tumor tissue.

2 cm. tumor nodule in left aur. andinvolvement of subepicard. lym-phatics.

Subepicard. lymphatic involvementwith myocard. infiltration in bothaur.

Obliteration of pericard. sac by ad-hesions and tumor tissue.

Extension of tumor tissue down greatvessels with invasion of pericard. atbase of heart and seeding of epicard.

Pericard. sac obliterated by adhesionsand tumor tissue. Nodules presentin myocard. of both ventricles.

Pericard. sac obliterated by fibrousadhesions and tumor tissue.

Serosanguineous pericard. exudatewith multiple small white tumor

nodules scattered over parietal andvisceral pericard. with early myo-card. invasion.

Low voltage. Complete A-V dissoc. In-verted T in CFs. Ventric. prematuresystoles. This later showed P pul-monale with a prolonged Q-Tinterval.

Inverted T wave in CF2. Last tracingobtained 35 days before death.

Normal ECG taken 24 days beforedeath.

Pattern of left bundle branch block.

Digitalis effect. Last tracingdays before death.

Pos.

Neg.

Neg.

Pos.

taken 18 Neg.

Sinus tachycard. changing to auric.flutter with spontaneous reversion tosinus tachycard. T-wave changes inchest leads typical of either peri-carditis or myocarditis.

P pulmonal which later changed to-auric. flutter. Last tracing taken 3months prior to death.

Auric. fibrill. with T-wave changes inchest leads typical of myocarditisand digitalis effect.

Rhythm fluctuating from sinus tachy-card. to auric. fibrill. ST and T-wavechanges typical of pericarditis.

Sinus tachycard. in tracing taken 1month before death.

Rhythm varying between sinus tachy-card., auric. fibrill. and auric.flutter. Varying degrees ofA-V block.

Low voltage. Changes typical of peri-carditis.

Sinus tachycard. Low voltage.Changes typical of pericarditis.

Pos.

Equivocal

Pos.

Pos.

Neg.

Pos.

Pos.

Pos.

(continued)223

(1)P.M.162

(2)P.M.350

(3)P.M.361

(4)P.M.374

(5)P.M.482

(6)P.M.537

(7)P.M.570

(8)P.M.610

(9)P.M.640

(10)P.M.721

(11)P.M.757

(12)P.M.902

(13)P.M.1046

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TABLE 3.-Continued

Case Anatomic Findings Electrocardiographic Changes Correlation

Bronchogenic Carcinoma-Continued

(14) Sanguineous pericard. effusion. Sub- Sinus tachycard., nodal premature Pos.P.M. epicard. lymphatics filled with tumor systoles with short P-R interval and1135 tissue with early invasion of outer prolonged QRS complexes.

layer of myocard.

(15) Involvement of subepicard. lym- Low voltage with a small Q wave and EquivocalP.M. phatics by tumor tissue. inverted T wave present in aV1. Last1307 tracing taken 24 days before death.

(16) Pericard. sac obliterated by 2 cm. thick Low voltage. Changes typical of Pos.P.M. layer of tumor tissue. Subepicard. chronic pericarditis.1349 lymphatics filled with tumor tissue

with early myocard. invasion.

Malignant Melanoma

(1) Parietal and visceral pericard. contain Low voltage. Tracing suggests myo- Pos.P.M. numerous tumor nodules. Numerous cardial disease.121 nodules scattered throughout myo-

card. of all 4 heart chambers.

Malignant Lymphoma

(1) Serosanguineous pericard. effusion. Low voltage. Sinus tachycard. Tracing Pos.P.M. Subepicard. lymphatics contain consistent with early pericarditis.216 tumor tissue (lymphocytic lympho-

sarcoma).

(2) Scattered gray nodules in subepicard. Sinus tachycard. Low voltage. Pos.P.M. region. (Hodgkins) Changes typical of chronic pericar-269 ditis.

(3) Pericard. sac obliterated by sheet of Sinus tachycard. Tracing typical of Pos.P.M. tumor tissue (reticulum cell chronic pericarditis.806 sarcoma).

Carcinoma of Pancreas

(1) Serosanguineous pericard. effusion. Sinus tachycard. Low voltage. Pos.P.M. Epicard. surface covered by fibrin- Changes typical of chronic1095 ous exudate. Subepicard. lymphatics pericarditis.

filled with tumor tissue with earlymyocard. invasion.

Carcinoma of Kidney

(1) Pericard. sac obliterated by adhesions Auric. fibrill. with ventric. premature Pos.P.M. and tumor tissue. Tumor nodules systoles arising in left ventricle.529 present in epicard.

Carcinoma of Prostate

(1) Scattered small microscopic tumor Low voltage. Left ventric. hy- EquivocalP.M. nodules in myocard. Mild left ven- pertrophy pattern which reverted to1075 tric. hypertrophy. normal just prior to death. Last

tracing taken 27 days before death.

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J. M. YOUNG AND I. RALPH GOLDMAN

Malignant LymphomaIn this series of tumor deaths, there were

60 cases with malignant lymphoma. Twelvehad lymphosarcoma, and five of these showedmyocardial involvement (see fig. 4). In onecase the pericardial sac was obliterated, andthe electrocardiogram showed low voltage,sinus tachycardia and changes consistentwith pericarditis. In two other cases therewas a serosanguineous pericardial effusion.The heart weight was increased in one case.There was epicardial spread in four cases andmyocardial nodules in one case. The medias-tinum contained tumor in three cases.Two of seven cases of reticulum cell sarcoma

had epicardial tumor, and in both the medias-tinum was involved. The pericardial sac wasobliterated in one case, and an electrocardio-gram showed sinus tachycardia and changestypical of chronic pericarditis.Of 39 cases of Hodgkin's disease, only two

disclosed heart metastases. In both the epi-cardial layer was involved. An electrocardio-gram in one case showed sinus tachycardia,low voltage, and changes consistent withpericarditis. Mediastinal involvement waspresent in both cases.Two cases of mycosis fungoides had no

cardiac metastases.

Carcinoma of PancreasSeven of the 33 cases of carcinoma of the

pancreas had cardiac metastases. Four ofthese followed lymphatic pathways and in-volved the subepicardial region, while twoshowed myocardial nodules and one had im-plants only between the trabeculae of theright ventricle. In four cases there was peri-cardial effusion, and in one of these, theeffusion was serosanguineous. The electro-cardiogram of the last mentioned case dis-closed sinus tachycardia, low voltage, andchanges typical of chronic pericarditis. Medias-tinal involvement was noted in three cases.

Carcinoma of the EsophagusSix of the 33 cases in this group had cardiac

involvement, and one of these showed direct

extension through the pericardium. In fourthere was subepicardial and mediastinal in-volvement, and in two the metastases wereblood-borne. In three instances there waspericardial effusion, one being sanguineous.One case disclosed obliteration of the peri-cardial sac by tumor tissue. No electrocardio-grams were taken.

Carcinoma of the KidneyFour of 15 cases in this group had cardiac

metastases. Epicardial and mediastinal in-volvement was present in three instances,while the fourth case had endocardial implantsattached to the papillary bundles of the rightventricle. The pericardial sac was obliteratedby tumor in one case, and an electrocardio-gram disclosed auricular fibrillation andventricular premature systoles.Testicular TumorsFour of nine testicular tumors metastasized

to the heart, three via the blood stream andone through lymphatic channels (see fig. 5).In one case there was bloody pericardial effu-sion. No electrocardiograms were taken.

Other TumorsIn both cases of carcinoma of the stomach

the metastases were blood-borne. One caseof prostatic carcinoma had hematogenousmetastases, while in the other they were lym-phatic. In the cases with carcinoma of thebladder and adrenal gland the metastases werevia lymphatics, and both cases showed peri-cardial effusion. The other cases had hematog-enous metastases, and none had significantpericardial effusion.

DISCUSSIONThe symptoms most frequently listed in

cases with heart metastases are tachycardia,dyspnea, cough, cyanosis, precordial pain,arrhythmias, and edema of the lower extrem-ities. Symptoms alone are not diagnostic ofmyocardial metastasis.

Clinically, the patient with cardiac metas-tases may exhibit a number of findings sug-gesting the diagnosis. In addition to the

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TUMOR METASTASIS TO THE HEART

irregularities of rhythm mentioned above,there may be a pericardial friction rub, heartfailure refractory to treatment, pericardialeffusion which is often bloody, diminishedheart sounds, and falling blood pressure. Anoccasional case may show the findings ofchronic constrictive pericarditis,'2-'6 and rarelythere may be sudden death.The roentgenographic and fluoroscopic

changes may be helpful. These include largeheart shadow, findings of pericardial effusion,and fixation of a border of the heart. Thesechanges have been given attention in thefollowing reports.3' 4, 5, 7, 17

As stressed by Yater,3 the onset of cardiacsymptoms or findings of cardiac disease with-out apparent cause in a patient with knownmalignancy is highly suggestive of cardiac in-volvement by tumor.

Electrocardiographic changes in cases withheart metastases have received much atten-tion in the literature. Fishberg,'s who was thefirst in America to report cases of cardiacmetastases diagnosed during life, in 1930 notedauricular fibrillation and flutter in his threecases, while Willius and Amberg'9 also in 1930reported a case diagnosed during life in whichthe electrocardiogram disclosed incompletebundle branch block, low amplitude, and T-wave changes.

In 1933 Siegel and Young20 reviewed muchof the literature concerning electrocardio-graphic changes and felt that records in tumorcases gave some evidence as to the locationof the heart metastases. Scott and Garvinsfound auricular fibrillation and flutter andauricular premature contractions the common-est changes in their series. The commonlyreported changes include sinus tachycardia,auricular fibrillation and flutter, auricularpremature contractions, varying degrees ofA-V dissociation, ventricular premature con-tractions, low voltage, and changes suggestiveof myocardial or pericardial involvement,but these changes by themselves are not diag-nostic.The metastatic pathways taken by tumors

reaching the heart are usually listed as theblood stream, lymphatics, and direct exten-

sion, the last being unusual since the pericar-dium is a strong barrier.

It is at times difficult to ascertain the exactroute taken in myocardial involvement. Whenmediastinal involvement is marked, con-tinuous retrograde lymphatic permeation canoccur, or there may be retrograde lymphaticembolization. We have accepted isolated in-tramural nodules as hematogenous metastases,though it seems possible that some of thesemay have begun from small tumor emboli inperivascular myocardial lymphatics.

Willis6 has classified involvement as arisingfrom (a) direct nonmetastatic invasion fromcontiguous growths, via lymphatics, via thevenae cavae, and via the pulmonary veins,and (b) true embolic metastasis by endocar-dial implantation and via the coronary ar-teries. Morris2 in 1927 felt that the hematoge-nous route was the most common, but onemust consider the tumor type when pathwaysare discussed. True endocardial implants repre-sent an uncommon type of metastasis, andthese are discussed by Willis,6 Coller andassociates,21 Nicholls,22 and Herbut and Mai-sell.7 In our series, endocardial implantsoccurred in a case of carcinoma of the pan-creas and a case of carcinoma of the kidney.Myocardial nodules may ulcerate through theendocardium and implant within the chambers.We noted this latter occurrence in singlecases of malignant melanoma, bronchogeniccarcinoma, and carcinoma of a paranasalsinus. Tumors which most frequently implanton the endocardium are those of the genito-urinary tract, chiefly the testicular and kidneytumors, and those of the gastrointestinal tract.In this series no case of direct extensionthrough the venae cavae was noted.The supposed infrequency of cardiac metas-

tases has been explained in several ways.Recently these were summarized by Prichard1as (a) the strong kneading action of the heart,(b) the metabolic peculiarities of striated mus-cle, (c) the rapid blood flow through the heart,and (d) the restricted lymphatic connectionsmaking retrograde lymphatic extension neces-sary. Another factor mentioned is that thecoronary arteries arise from the aorta at right

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J. M. YOUNG AND I. RALPH GOLDMAN

angles. Actually, for types of tumors such asbronchogenic carcinoma, carcinoma of thebreast, malignant melanoma, malignant lym-phoma, and carcinoma of the pancreas andesophagus, cardiac metastases are relativelycommon.1', 6-9, 23-26

Bronchogenic carcinoma frequently involvesthe heart usually by way of the mediastinallymphatics. This mode of spread has beenstressed by Morris2 and Willis.6 As early as1912 Adler27 had noted frequent pericardialand cardiac involvement, and Simpson28 in1929 found 62 of 139 cases of bronchogeniccarcinoma with pericardial invasion. A surveyof many case reports emphasizes the frequentpericardial and epicardial involvement witheffusion or obliteration of the pericardialspace.

It has been estimated29 that half the casesof malignant melanoma show cardiac metas-tases; these usually follow the hematogenousroute and are extensive. Reviews emphasizingsecondary melanoma in the heart30' 31 showthat few electrocardiographic tracings havebeen obtained. Certainly, many of thesecases terminally should show significantchanges in their tracings. The few changesreported are low voltage, sinus tachycardia,and findings suggesting myocardial involve-ment.Of the malignant lymphomas, lymphocytic

and lymphoblastic lymphosarcoma most fre-quently involve the heart,7 ,32, 3 and this wasparticularly prominent in our series. Themethod of extension may be lymphatic, infil-trative, or rarely hematogenous with forma-tion of nodules. Epicardial and pericardial in-volvement with effusion is the usual finding.Reticulum cell sarcoma shows a somewhat lessstriking tendency for cardiac metastasis.34'35Hodgkin's disease, on the other hand, evenless frequently shows cardiac spread. Rottinoand Hoffman36 in 1952 reported five instancesin a series of 63 cases. Herbut and Maisell7had 2 instances in 13 cases, while Lucia andco-workers33 noted 3 cases in 18. Other articlesconcerning Hodgkin's disease with cardiacinvolvement are those of Harrell,37 Garvin,38and Ritvo.39

In the malignant lymphomas the mostsignificant involvement is usually in the epi-cardium and pericardium with effusion orobliteration of the sac, giving findings andelectrocardiographic changes of pericarditisand eveil constrictive pericarditis.Our cases of carcinoma of the pancreas and

esophagus disclosed frequent epicardial andpericardial involvement, and more than halfhad notable pericardial effusion. This is inagreement with cases reported in the literature.

OBSERVATIONS AND CONCLUSIONSThe diagnosis of secondary neoplastic spread

to the heart offers a challenge to the clinician.If one is alert to this possibility, there arefrequently symptoms, signs, and laboratorychanges indicating the diagnosis, especiallyin the patient with known malignant disease.While such a diagnosis is usually of little im-portance in the patient's course, a few investi-gators9' 38, 40, 41 have used pericardial aspira-tion and/or deep roentgen therapy with bene-ficial though temporary results. Roentgentherapy in these cases, particularly in malig-nant lymphoma and small cell bronchogeniccarcinoma with cardiac spread, deserves fur-ther investigation. Pericardial aspiration mayhelp establish the diagnosis if the fluid is ex-amined for tumor cells.The authors, after a survey of the literature

and study of this series of tumor deaths, feelthat the following observations are in order.

1. Malignant tumors, particularly broncho-genic carcinoma, malignant melanoma, malig-nant lymphoma, and carcinoma of the breast,pancreas, and esophagus, involve the heartsecondarily with relative frequency.

2. The diagnosis of cardiac spread in thesecases can often be made by the alert clinicianwho makes use of the symptoms, signs, elec-trocardiographic and roentgen changes oftenpresent.

3. While there are no electrocardiographicchanges pathognomonic of cardiac metastasis,certain changes do occur, and these show fairlyclose correlation with the anatomic changespresent.

4. Deep roentgen therapy deserves further

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TUMOR METASTASIS TO THE HEART

study as a means of relieving the embarrassedheart.

SUMMARYA large series of tumor deaths was studied

for cardiac metastases in a Veterans Adminis-tration hospital. The incidence of cardiacmetastasis in this somewhat selected groupwas 19.1 per cent. The bulk of the cases werebronchogenic carcinoma, malignant melanoma,malignant lymphoma, and carcinoma of thepancreas and esophagus. Correlation of elec-trocardiographic changes and anatomic find-ings is given. Likewise, the behavior of theindividual types of tumors with reference topathologic findings is presented.

SUMARIO ESPANOLEste articul6 es un repaso de 476 casos con-

secutivos de muertes debido a envolvimientodel coraz6n por tumor. Este grupo de casosalgo seleccionado (de un Hospital de la Ad-ministraci6n de Veteranos) muestra una inci-dencia de met&stasis cardiaca de 19.1 porciento. El volumen de tumores con metastasisal coraz6n fueron los carcinomas bronquiogeni-cos, melanoma maligno, linforma maligno, ycarcinoma del pancreas y el es6fago. Cambioselectrocardiogr&ficos fueron frecuentes y cor-relacionaron bastante cercanamente con laextensi6n anat6mica de la enfermedad. Laliteratura relacionada se repasa.

REFERENCES'PRICHARD, R. W.: Tumors of the heart. Arch.

Path. 51: 98, 1951.2 MORRIS, L. M.: Metastases to the heart from

malignant tumors. Am. Heart J. 3: 219, 1927.3 YATER, W. M.: Tumors of the heart and peri-

cardium. Arch. Int. Med. 48: 627, 1931.4 LISA, J. R., HIRSCHHORN, L., AND HART, C. A.:

Tumors of the heart. Ann. Int. Med. 67: 91,1941.

5 DOANE, J. C., AND PRESSMAN, R.: Antemortemdiagnosis of tumors of the heart. Am. J. M. Sc.203: 520, 1942.

6 WILLIS, R. A.: The Spread of Tumours in theHuman Body. London, Butterworth & Co.,1952. Pp. 187-194.

7 HERBUT, P. A., AND MAISEL, A. L.: Secondarytumors of the heart. Arch. Path. 34: 358, 1942.

s SCOTTvr, R. W., AND GARVIN, C. F.: Tumors of theheart and pericardium. Am. Heart J. 17: 431,1939.

9 DIMMETTE, R. M.: The antemortem diagnosis ofsecondary tumors of the heart. U. S. ArmedForces M. J. 1: 750, 1950.

10 LEFKOVITS, A. M.: Neoplastic metastasis to theheart. Am. Heart J. 36: 610, 1948.

11 LYMBURNER, R. M.: Tumors of the heart. Histo-pathological and clinical study. Canad. M. A.J. 30: 368, 1934.

12 LANFORD, J. A., AND THOMAS, E. P.: Obliteratedpericardium by hypernephroma metastasis.South. M. J. 26: 929, 1933.

13 BECK, C. S.: Acute and chronic compression of theheart. Am. Heart J. 14: 515, 1947.

14WALLACE, J. J., AND LOGUE, R. B.: Metastaticcarcinoma as a cause of constrictive pericarditis.Am. Heart J. 31: 223,1946.

15 FISCHER, J. W.: Neoplastic involvement of thepericardium producing the syndrome of con-strictive pericarditis. Am. Heart J. 35: 813,1948.

16 SLATER, S. R., KROOP, I. G., AND ZUCKERMAN, S.:Constrictive pericarditis caused by solitarymetastatic carcinosis of the pericardium andcomplicated by radiation fibrosis of the medi-astinum. Am. Heart J. 43: 401, 1952.

17 RAVID, J. M., AND SACHS, J.: Tumors of the heart.Am. Heart J. 26: 385, 1943.

18 FISHBERG, A. M.: Auricular fibrillation andflutter in metastatic growths of the right auricle.Am. J. M. Sc. 180: 629,1930.

19 WILLIUS, F. A., AND AMBERG, S.: Two cases ofsecondary tumor of the heart in children, in oneof which the diagnosis was made during life.M. Clin. North America 13: 1307, 1930.

20 SIEGEL, M. L., AND YOUNG, A. M.: Electrocardio-graphic findings in tumors of the heart. Am.Heart J. 8: 682, 1933.

21 COLLER, F. C., INKLEY, J. J., AND MIORAGUES, V.:Neoplastic endocardial implants. Am. J. Clin.Path. 20: 159, 1950.

22 NICHOLLS, A. G.: Secondary carcinoma implantedon the endocardium of the right ventricle.Canad. M. A. J. 17: 798, 1927.

23 POLLIA, J. A., AND GOGOL, L. J.: Some notes onmalignancies of the heart. Am. J. Cancer 27:329, 1936.

24 RITCHIE, G.: Metastatic tumors of the myo-cardium. Am. J. Path. 17: 483, 1941.

25 Exhibit "Metastatic Neoplasms of the Heart."Armed Forces Institute of Pathology, Registryof Cardiovascular Pathology, Washington,D.C.

26 MATOUSEK, W. C.: The recognition of metastases.U. S. Armed Forces M. J. 4: 733, 1953.

2 ADLER, I.: Cited by Simpson, S. L.28 SIMPSON, S. L.: Primary carcinoma of the lung.

Quart. J. Med. 22: 413, 1929.29 ACKERMAN, L. V., AND DEL REGATO, J. A.: Cancer.

Diagnosis, Treatment, and Prognosis. St.Louis, C. V. Mosby, 1947. P. 171.

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30 MORAGUES, V.: Cardiac metastasis from malig-nant melanoma. Am. Heart J. 18: 579, 1939.

31 RITZ, N. D.: Diffuse melanosis, pericardialeffusion, and melanuria associated with malig-nant melanoma. Ann. Int. Med. 30: 184, 1949.

32STEVEN, R. A.: Heart tumor. Report of a case.

Am. Heart J. 30: 411, 1945.33 LUCIA, S. P., MILLS, H., LOWENHAUP.T, E., AND

HUNT, M. L.: Visceral involvement in primaryneoplastic diseases of the reticulo-endothelialsystem. Cancer 5:1193, 1952.

34 BRICK, I. B., AND GREENFIELD, M.: Reticulumcell sarcoma with cardiac metastasis. Am.Heart J. 34: 599, 1947.

35 GREINER, D. J.: Reticulum cell sarcoma involvingthe heart and pericardium. Bull. School Med.Univ. Maryland 25: 44, 1940.

ROTTINO, A., AND HOFFMAN, G. T.: Cardiac

involvement in Hodgkin's disease. Am. HeartJ. 43: 115, 1952.

37 HARRELL, G. T.: Hodgkin's disease with invasionof pericardium and gallbladder. Arch. Path.28: 58, 1939.

38 GARVIN, C. F.: Hodgkin's disease of the heart andpericardium. J. A. M. A. 1172: 1876, 1941.

39 RITVO, M.: Hodgkin's disease. Report of a casewith unusual longevity and invasion of theheart and pericardium. New England J. Med.223: 891, 1940.

40 SHELBURNE, S. A., AND ARONSON, H. S.: Tumorsof the heart. II. Report of a secondary tumor ofthe heart involving the pericardium and thebundle of His with remission following deeproentgen therapy. Ann. Int. Med. 14: 728, 1940.

41 FRIEDBERG, C. K.: Diseases of the Heart. Phila-delphia, W. B. Saunders Co., 1949. Pp. 1003-1004.

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J. M. YOUNG and I. RALPH GOLDMANTumor Metastasis to the Heart

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright © 1954 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Circulation doi: 10.1161/01.CIR.9.2.220

1954;9:220-229Circulation. 

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