MALIGNANT TUMORS AND THEIR METASTASESA SUMMARY OF THE NECROPSIES ON EIGHT HUNDRED SIXTY-FIVECASES PERFORMED AT THE BELLEVUE HOSPITAL OF NEW YORK

BY JOHN E. MCWHORTER, M.D.AND

ALBERT W. CLOUD, M.D.OF NEW YORK, N. Y.

FROM THE PATHOLOGICAL LABORATORIES OF BELLEVUE IIOSPITAL

THIS brief review of a series of malignanit tumors was collected fromthe autopsy protocols of Bellevue Hospital, New York City, and covers aperiod of twenty-three years. During that time, 13,500 autopsies had beenperformed, and out of that numl)er 865 were done on malignant tumors,approximately 6 per cent. Of these tumors, 770 were of epithelial origin,while ninety-five arose from connective tissue, a ratio of eight to one.

The object of this paper is to emphasize the end-results in malignanttumors, as seen at necropsy, particularly their anatomical distribution andthe distribution of their metastases. For purposes of description, metastasesin this series have been divided into three groups: (I) local, in which theneoplasm confinedl itself to the organ in which it arose or metastasized, onlyto immediately adljacent structures or lymph-nodes; (2) multiple local, inwhich the growth invaded, probably by direct extension, the neighboringorgans and structures; (3) diffuse, in which the tumor not only invaded theneighborinig tissues, but, in addition, metastasized to some remotely placedorgan or structure.

TONGUE.-Nine cases, all males, average age fifty-one years, youngestforty-one, oldlest sixty-one. The majority of these tumors involved theregional lymph-nodes, while only about 30 per cent. invaded distant struc-tures, as the lung, heart, liver and brain.

(EsOPHAGUS.-Of the eighty-three cases, all but two occurred in males-eighty-onie males, two females. This interesting sex ratio checks up veryclosely with the surgical records of the first division, for out of forty casesfrom which tissue was taken for biopsy, all but one occurred in males.Carcinoma of this structure seems to be associated with the latter decades oflife, as the average was sixty-one years, and in only twenty-three cases didit occur below fifty. In the majority of cases this neoplasm showed a markedtendlenicy to remain local, inva(dinig usually the immediately a(ljacent struc-tures, as the lymph-nodes, lungs and liver. Occasionally, regardless of ageof patienit, or morphology of tumor, these tumors widlely disseminate them-selves throughout the body, but this is the exception and not the rule. Thefact that the majority of these tumors are of local growth may be due tothe fact that ulceration and obstruction probably occur early in their course,

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and the resultant infection and starvationi terminate the case before distantmetastases have time to form.

STOMACH.-Number of cases, 208. Of this number I55 occurred inmales and fifty-three in females, a ratio of three to one. The average agewas fifty-six years, with an extreme variation of twenty-eight to ninety years.The pyloric endl was inivolved in 8o per cent. of the cases, the cardia in IOper cent., and the lesser anct greater curvature in io per cent. When thecardia is involved the growth usually extends inito the oesophagus, thus mak-ing it dlifficult to deterninie whether the growth arose primiiarily in the stomaclor cesophagus. In this series there were blit four cases of liniitis plastica.It is of particular interest to note that thirty-two cases, or I 5 per cenlt., showedno obvious evidenice of metastases. The usual site of miietastases is the lymph-nodes and liver, the latter organ being involve(d in 45 per cent. of the cases,and the lymph-nodes in 44 per cent. The lymph-nodes most usually invadedare, first, the suprapancreatic andI retroperitonieal and, second(lly, the gastric.The lungs were involved in only 6 per cenit. of the cases. It mlay be said ingeneral, that carcinoma of the stomach is either distinlctly local or multiplelocal in growth.

SMIALL INTESTINE. Number of cases, three males two, feiliales one.The average age was fifty-five, the younigest being forty-one and the oldestseventy years. Two of these cases arose in the duodenum and one in thejejunum. The metastases were distinctly local in character, inivolving theimmediately adjacent organs and lymph-nodes.

LARGE INTESTINE.-Number of cases, sixty-onie. The average age isabout the same as that for the stomach, nanmely, fifty-five years, with extremevariation of twenty to eighty-four years. Although the average age of fifty-five was about the same as that of the stomach, 33 per cent. of the casesoccurred below fifty a very much lower age average than that for car-cinoma of the stomach. The sexes were more equally divided, being thirty-six males to twenty-five females, a strikinig difference to that of the stomach,in which the proportion was three males to one female. In the large intestine,the site most frequently involved was the sigmoid; next, the coecum, thenthe descending colon with splenic flexure of the colon fourth. The transverseand ascending colon, excepting at the hepatic and splenic flexures, wereseldom affected. Metastases usually were local in their distribution, involvingthe neighboring nodes anid adjacent tissues. The liver, pancreas and( spleenwere seldom invaded, excepting where the primary growth originated in thenear viciniity of these organs. Remote metastases to the pleural cavity wereexceedingly uncommoni, while the number of cases showing Ino obviousmetastases was a strikingly common occurrence. It is of considerable interestto note that 25 per cent. of these autopsies showed that the primary causeof death was due to perforation and peritonitis. MIetastases: local, forty-eight, multiple local, seven, diffuse, six.

RECTUM.-Number of cases, twenty-six-average age, fifty-six years;limits seventy-five to forty-four years. Sex: males, twenty-one, females,

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five. In this site, carcinoma generally appears to be a far more widelymetastasizing tumor than it is in any other position in the whole alimentarytract. It involves, in general, the neighboring nodes and adjacent tissues, theliver in 50 per cent. of the cases, and, not infrequently, other abdominalorgans and the lungs. Metastases: local, eight, multiple local, four, diffuse,fourteen.

PHARYNX, LARYNX AND TRACHEA.-Number of cases, seven-averageage, about fifty-two years; sex, all males. MIetastases usually very local intheir distribution, infiltrating the surrouniding tissues and invading the neigh-boring nodes. Occasionally, these tumors invaded the lung and even theheart, but this seemed to be a rare occurrence. Ulceration with its subse-quent infectioin seemed to be the nmost obvious cause of death. Metastases:local, five, multiple local, two.

LUNGS.-Number of cases, thirty-seven-average age, forty-nine, limitstwenty-four to seventy-three years; sex, thirty-four males, three females.Three-quarters of these tumors were carcinomatous or adenocarcinomatousin type and arose probably in the bronchi. The remaining quarter were notgland-cell tumors, being more of the epitheliomatous or squamous type. Theadenomatous tumors usually metastasize(d widely throughout the thoraciccavity, and in most cases involved many of the abdominal organs. Thesquamous-cell type of tumor was usually local in its growth, only one casemetastasized distally to the kidney. Metastases: local, eight, multiple local,twenty-two, diffuse, seven.

BREAST.-Number of cases, fifty-one-average age, fifty-five, withextreme variations of twenty-one to eighty years; sex, one male, fiftyfemales. This neoplasm in the latter stages of its course metastasizes exten-sively, locally and (listantly. One of the interesting findings in this serieswas the more frequent involvement of the liver than the lungs, the formeroccurred in 34 per cent. of cases, while the latter in only 20 per cent. Bones,usually the ribs, were invaded in 22 per cent. of the cases; the involved ribswere probably local extensions. Occasionally these tumors widely disseminatethemselves throughout the bo(ly, invading diffusely many organs and struc-tures. Metastases: local, six, multiple local, thirty-three, diffuse, twelve.

OVARY.-Number of cases, six-average age sixty years, limits forty-threeand seventy years. Metastases usually diffuse involving the surroundingstructures, the retroperitoneal nodes, the liver andl lungs. Metastases: local,one, diffuse, five.

CERVIX AND LTTERUs.-Number of cases, twenty-two, of which sixteenoccurred in the cervix and six in the body of the uterus. The average agewas forty-five years, with limits of twenty-eight and sixty years. About 50per cent. of cases occurred in women under forty-five. Metastases bothcervix and uterus were usually local or multiple local, invading presumablyby direct extension the bladder, surrounding tissues and regional lymph-nodes. Only four cases involved distant organs, one of which arose in thecervix and three in the uterus. The one arising from the cervix metastasized

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MALIGNANT TUMORS AT BELLEVUE HOSPITAL

to the lungs, while of the three arising from the uterus, one metastasized tothe pancreas, one to the pleura, lungs, liver and sacral vertebrae and one tothe lungs. Metastases: local, thirteen, multiple local, five, diffuse, four.

PROSTATE.-Number of cases, forty-average age, between fifty-five andsixty years, with extreme variations of twenty-four to eighty years. Aboutone-half the cases occurred in men of sixty years or over. These tumorsusually showed extensive local involvement of bladder and regional nodes.The vertebrae was affected in about one-third of the cases, while extensiveinvolvement of peritoneal and pleural cavities were the rule rather than theexception. Metastases: local, thirteen, multiple local, fourteen, diffuse,thirteen.

TESTICLE.-Number of cases, three. The number of cases in this serieswas so few that the age incident is of little, if any value. Average age wasforty-four years, with thirty-eight years the youngest and fifty-five years theoldlest. The metastases were mostly distant, involving extenlsively the lung,liver, the pleural and peritoneal cavities and occasionally the vertebroe.\Jetastases: diffuse, three.

URINARY BLADDER.-Number of cases, twenty-nine-average age, aboutfifty years, the youngest being thirty-eight, the oldest seventy-four years.Sex, twenty-seven males, and two females. This neoplasm in its growthshows a marked tendency to remain local, as over one-half the cases showedeither no obvious evidence of metastases or else invaded only the imme-diately adjacent tissues. In less than one-half the cases the retroperitonealnodes were involved, and distant metastases to lung, liver and bone werenoted in but three cases. Metastases: local, sixteen, multiple local, ten,diffuse, three.

KIDNEY.-Number of cases, ten--average age fifty-five years, limitstwenty-five to eighty. Sex, eight males, one female. Metastases almostinvariably widespread, involving diffusely the ad(lominal and( thoracic organsand lymph-nodes. The two cases of no metastases noted in the chart wereprobably adenomas. Metastases: local, three, diffuse, seven.

HYPERNEPHROMA.-Number of cases, thirty-two-average age, fifty-four,with the youngest eighteen, and the oldest seventy-one years. Sex, twenty-two males, five females. It is of interest to note that the average age forfemales was thirty-six years, while the average for males was fifty-five years.As a general rule, this is perhaps one of the most diffusely and profuselymetastasizing tumors that we see, as it involves in most of the cases eitherthe thorax or abdominal cavities or both, and in 20 per cent. of the casesbone. Metastases: local, four, multiple local, two, diffuse, twenty-six.

LIVER.-Number of cases, thirty-nine-average age, forty-six, limitseighty-five to twenty-four years. In a little less than half of the cases theage was forty-five years. Sex, thirty males, nine females. The growth inmost cases seemed to be localized to the liver, but in 35 per cent., thetumor was a widely metastasizing one, extensively involving the lymplh-nodes,peritoneum, many organs of the abdominal cavity, anid rather infrequently the

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lungs and pleura. Metastases: local, twenty-two, multiple local, three, dif-fuse, fourteen.

GALL-BLADDER AND BILE-DUCTS.-Number of cases, thirty-two. Theaverage age incidenit is similar to that of the liver. The sex ratio was twenty-one males to eleven females. These tumors in about one-half the casesinvaded the liver, evidently by direct extension. In other respects it metas-tasizes as does the primary carcinoma of the liver; that is, about twenty-onelocal and seven diffuse.

PANCREAS.-Number of cases, thirty-four-average age, fifty-six, limitsseventy-five to thirty-three years. In only nine cases out of thirty-fourdid it occur at ages under fifty. Sex, twenty-seven males, seven females.Metastases in the majority (6o per cent.) of cases invaded the liver andusually disseminated itself widely throughout the abdominal cavity, but onlyinfrequently involved the lung (four times). Metastases: local, thirteen,multiple local, three, diffuse, eighteen.

THYROID.-Number of cases, five-average age, forty-four years, lim.tsthirty-five to sixty years. Sex, three males, 2 females. One of these tumorswas of local growth, four extensively involved the liver and lungs and supra-clavicular nodes. Metastases: local, one, diffuse, three.

PAROTID.-Number of cases, three-average age, fifty-two years; alloccurred in males. The two that metastasized were remarkable, in that theirmetastases were widely distributed throughout the body, involving almost allthe organs and structures of the thoracic cavity, the liver in one case and theadrenals and kidneys in both. The one case that did not metastasize wasevidently the local growing, non-metastasizing type of mixed tumor. Metas-tases: local, one, diffuse, two.

BRANCHIOGENIc.-Number of cases, three-average age, fifty-five, withthe youngest forty-four and the oldest seventy years. Sex, two males, onefemale. In one of the cases the neoplasm remained of local growth, involvingextensively the tissues of the neck. The remaining two cases involved notonly the structures of the neck, but metastasized distantly to the liver. Metas-tases: local, one, diffuse, two.

THYMUS. Number of cases, one-age five; sex, male. In this case thetumor metastasized to the neighboring nodes, lung and pleura. Metastases:diffuse, one.

SKIN.-Number of cases, seven, limits twenty-nine to sixty years, averageage about fifty years. Sex, all males. Two of these cases arose from theskin of the neck, one on chest and one on leg, face, scrotum and penis. Allof these tumors excepting two invaded the neighboring nodes alone. Of thetwo exceptions, one arose from the skin of the chest and metastasized tothe lungs, the other arose in the neck and metastasized to the liver. Metas-tases: local, five, diffuse, two.

MELANOCARCINOMA.-Number of cases, nine-average age, forty years.Sex, all males. Two of these cases arose in the small intestine, two in theeye, four in the skin of the toe, leg and scapula. The origin of the other was

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unknown. The outstandinlg characteristics of this tumor are its frequentwidespread metastases. Few of the malignant tumors possess this power ofgrowth; certainly there are none that exceed it. It is of interest to note that,regardless of its site of origin, the liver is frequently involved, while thelymph-glands, though usually invaded, sometimes seeme(d to be entirely free.Metastases: diffuse, ninie.

PITUITARY.-Number of cases, one age thirty-ninie, sex, male. Thisneoplasm invaded locally the tissues, l)ut did not metastasize.

TOOTH BUD (ADAMANTINOMA). Number of cases, oine-age fifty-five;sex, male. This tumor extensively invaded the tissues locally and involvedthe neighboring lymph-nodes.

CARCINOMA OF UNKNOWN ORIGIN. Number of cases, twenty-averageage, fifty-two years, limits thirty to seventy years. Sex, niine males, elevenfemales. Because of the diffuse nature of their growths, their site of originwas unknown. It is extraordinary the power of growth some of thesetumors possess. One cannot help but be astounded by the remarkable powersof the living organism to withstand this onslaught for so long a time.Metastases: diffuse, twenty.

SARCOM ATA

Sarcomata, unlike carcinonmata, show no definite evidlences in nmany casesof their site of origin, and( are usually so diffusely distril)uted that theirprimary foci cannot with any (legree of accuracy be (letermine(l. This isparticularly true of lympho-sarcoma. Even in this series, some of thesetumors seem to have involved, either primarily or secondarily, most organsand structures of the body. For this reason, it wouldl seem advisable topresent them in roughly classifie(d groups, rather than to attempt a detaileddescription.

The average age was forty-five years, limits from three to seventy-fouryears. Twenty-five per cent. of the cases occurred at thirty-five or under.Sex, sixty-six males, twenty-ninie females. Nearly half the cases (thirty-nine) were classified un(ler the diagnosis of lympho-sarconma. The averageage for this group was forty-two years, with an extreme variation of fromthree to seventy-four years. Sex, twenty-eight males, eleven femlales. Abouttwo-thirds of the cases involvedl the lymph-glands, usually the retroperitoneal,seldom the cervical. In maniy cases, the lymph-glands were diffusely involved,while other organs and structures of the body were relatively free. Thelungs and mediastinal nodes were seldom the primary site. The stomachwas involved in but one case, the intestinal canal in seven, the liver in threeand the thymus in six. The retroperitonieal region was (liffusely invaded innine cases. Metastases were usually very diffuse, tumors arising probablyin the thymic and cervical region practically always invaded the mediastinumiianid not infrequently the retroperitoneal nodes, but, strangely enough, thelungs were often free. Tumors arising in the retroperitoneal region or retro-peritoneal nodes, or in other structures in the albdlominal cavity usually

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involved diffusely the lymph-glands and surrounding tissues, and not infre-quently the liver and spleen. The mediastinal and bronchial nodes wereinvaded in less than one-half of the cases, while the lung appeared to be aninfrequent site. Age in no way influenced the growth. The metastases atseventeen were not more extensive than were those of sixty.

TABLE IIEpithelial Tumors Arising from Skin and Mucous Membrane

Age 10-20 21-30 31-40 41-50 51-60 61-70 7I-80 8i-go

Skin. I 2 2 ITongue 3 4 IPharynx.

.. . . .

Larynx I I 5 ITrachea - - - - - - - I I 5Lung ...................... . . I 6 I4 II 3(Esophagus.. . 2 23 30 20 4Stomach ................... 6 21 54 59 44 17 4Intestine . .................... I 46 Io 15 I9 5 2Rectum .. .3 4 7 9 IUrinary Bladder I 5 9 9 2 IGall-bladder 4 7 12 6 2 ICervix and Uterus .. 6 I I 4

Epithelial Tumors Arising in Glandular Organs

Breast .2 2 15 ll 5 3Prostate ........I............. 4 5 IO 9 10 ITesticle . .2 IKidney .3 2 6 8 3 3Adrenal .I 3IPancreas .2 7 II 1IO 3Liver ........................ 2 IO 6 5 10 4

The breast was the primary site in two cases, both females. In one, themetastases widely involved the lymph-glands, in the other, besides the nodes,the lung, liver and rectum were invaded. It occurred in the prostate in onecase. From the number of other structures involved, it would be difficultto state whether the tumor, at this site, was primary or secondary. Six ofthese tumors were thought to have originated in the lung, all occurred inmales and at the average age of fifty years. Two-thirds of them extensivelyinvolved the lung, but did not invade other tissues. Of the remaining two,one metastasized to ribs and dura, the other to the kidney.

There were eleven primary tumors of bone, five of which occurred inthe femur, three in the lower end of the tibia, two in sternum and ribs andone in the vertebrae. The average age was forty-four years and there wereeight males to three females. Most of these tumors metastasized to the lung.A few were bizarre in their selection; for one from the ankle metastasizedto the scalp, another from the femur to the heart, another from the sternumand ribs to the liver, while still another, an osteosarcoma of the right ankle,metastasized to the femoral glands.

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McWHORTER AND CLOUD

Under the diagnosis of endothelioma of the dura were eleven cases. Theirmain interest lies in their benign character, for none of these tumorsmetastasized.

BRAIN.-Number of cases, e&ght average age, twenty-seven, with extremevariations of from three to fifty-five years. Half of these cases occurredbelow twenty years, while three of this numniber were below ten. Sex, fourmales, four females. In five of the eight cases the condition was that of aglioma. Of the remaining three, two were spongioblastomas and one a neuro-blastoma. All of these neoplasms were of local growth.

SPINAL CORD.-Number of cases, three average age, forty-nine years.Sex, males two, females one. None of these tumors metastasized.

EYE.-Number of cases, one. It occurred in a male, aged four years.This neoplasm involved the optic nerve and metastasized distantly to the liver.

Com1Xlmenit.-In analyzing this series of cases, certain features presentthemselves as being of unusual interest. Briefly stated, they are as follows:

(i) The average age for all malignant tumors at autopsy was fifty-one.Men seem to be affected somewhat later in life than women. Tumors arisingin the female organs of reproduction apparently occur at an earlier age thando those arising in other organs of the body. Malignant connective tissuetumors usually occur in the earlier decades of life, for the average age wasforty-five years.

(2) The sex ratio of three males to one female would seem to be anexaggerated one, the probable explanationl being that more males are autopsiedthan females. However, the ratio for csophagus, stomach and intestinescorresponds with the surgical ratio compiled from the combined records ofthe Presbyterian and French Hospitals, and from the First Surgical Divisionof Bellevue Hospital.

(3) The site of many of these tumors seems to a marked degree to beinfluencecl by sex, as, for example, there are Ino necropsy records or surgicalrecords on the First Division of an epithelioma arising from the mucousmembrane of the mouth or tongue in a female. From the same records thereare but two epitheliomas of the cesophagus occurring in women. In thestomach, the ratio is a little over three to one, while in carcinoma of theintestinal canal, the ratio is more nearly equal.

(4) Excepting in the very aged, age dloes not seem to influence metas-tases, for tumors occurring in those below thirty were not, as a general rule,more widely distribute(d than they were in those of fifty or sixty years.In the aged, the neoplasm was usually of local growth.

(5) In carcinoma of the stomach and intestines, the immediate cause ofdeath in about 15 per cent. of the cases was perforation and peritonitis. Itis interesting to note in this connection that, in the majority of these casesof the intestine, only definite symptoms were those of peritonitis.

(6) About 69 per cent. of the malignanit epithelial tumors arising in, orfrom, the skin andl mucous miembrane remained local in their growth, invad-ing either the neighboring lymph-glands and adjacelnt tissues or both, while

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only 28 per cent. of the cases arising in gland(lular organs showed the samelocal tendency of growth.

(7) One of the very interestinig findings in this review was the numberof cases that showed only local invasion of the neighboring tissues andadjacent lymplh-nodes. Perhaps, what is even of greater interest, are thecases in which the neighboring nodes were alone involved. This held truefor carcinomata regardless of their site of origin, but were much morefrequently found in the cases whose site of origin was the stomach, largeintestine, urinary bladder and cervix.

(8) The most interesting feature of this series is the number of casesof supposedly malignant tumors that did not metastasize. Out of 770morphologically maligniant epithelial neoplasms, I87 showed no obvious evi-dences of metastases. In the stomach and large intestine, I5 per cent. ofthe cases were of local growth, this fact being particularly emphasized inmaniy of the autopsy protocols. Any attempt to explain these findings wouldat least be speculative. Two, however, may be considered, as they seem tobe supported by a certain amount of evidence: (a) the existence of twotypes of tumiors, both of which show the same microscopic picture and reactin a similar mainner to the tissues in which they originate, but otherwise aredissimilar, for the course of one is that of a metastasizing tumor, while thatof the other is local in its growth; (b) that all tumors of this type arepotentially malignant, but their future course is guided and controlled bysome factor or factors, which, for purposes of conveniience, may be calledresistance.

Perhaps the true explanation of why some malignant neoplasms diffuselymetastasize and others (lo not may be entirely a matter of virulence and bodyresistance. To reason by analogy, from bacterial infections to malignancy,may not be tenable, but in any event both have enough in commoni to raisethe question as to whether or not virulence and body resistance, are not theguiding factors in the growth of all malignant neoplasms, as they seem tobe in all infections.

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