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le wit eI-l-llll red e of~ tre- or !e rage PRIMARY BRONCHIOGENIC CARCINOMA An Analysis cf 190 Cases, 58 of Which Wer~ Successfully Treated by Pneumonectomy, with a Review ~f the Literature INCIDENCE " pKIMAKY bronchiogenic carcinoma has become one of the most frequent malignant neoplasia encountered in humans. Whereas it has been su~ested that the increase in the incidence of these neoplasia js relative and not absolute, it is our conviction fl~at bronchiogenic malignancies have increased and are actually increasing in frequency. On the other hand, there is undoubtedly also a relative increase as well, because the condition is now more frequenfly.smpected and its existence recognized and proved. Unquestionably, before the frequency .of primary bronchiogenic carcinoma was appreciated, there were many cases which were diagnosed as pulmonary abscess, unresolved paeumonia," and many other conditions. As late as 1912, Adler stated, "On one point, however, there is nearly, complete con- sensus of opinion and that is that primary malignant neo- plasms of the lung are among the rarest form of disease." At the present time it is well known that bronchiogenic carci- noma is extremely comnmn and is probably second in frequency to gastric maligTtancies. This is evidenced by ot~'r own exparience and by the experience of Brines and Kenning and Koletsky. That these fig-ures show the true status is e~idenced by the fact that the statistics are based on ~Utopsy e~tminati0ns and not upon clinical di%~nosis. According. to Johnson and Keinha~ the inddence of prima~ bronchiogenic carcingma as determined at autopsy increased from 0.54% in the period from 19~2 to I9~7 " From the Department of Surgery, Sdaool of Medicine, Tulane Vni~er~b/o anti the Oeb~er Clinic. New Oread, 1187 .. . .- • ". .... _

OCHSNER, DIXON, AND DEBAKEY ei to 0.92% in the period from 1937 to 1942. In the Charity pital at New Orleans the incidence of primary carcinoma in 1931 was 0.47% and that of gastric 2.3%," whereas in 1938 these respective incidences were 1.9% (Fig. 1). In this institution the incidence of bronchiogenic as determined at autopsy increased five times in seven Seyfarth ~und increases in the incidence of pulmonary to all carcinomas from 5.05% during 1900 to 1906 to 8.75c ing 1919 to 1923. During the first half of 1942 there was an crease of. 15.5%. Dorn found that between 1914 and 1930 the~ death rote from cancer of the bronchus in the United States im Geased 3.7 times as contrasted with an increase of only 20%..fo~ all forms of cancer combined. He also found that the death rate [or cancer. ing treated {urther est United St ,ut 13,000 ichus. Appro.', time each yea deaths of the respira cardnoma of million as co~ that bronchic and that this the stomach of bronchiog doubled and a primary b: ddence of ( Wegelin ob~, chiogenic ca cases studie~ the number was as follc from 1910 1924, 4.8; ff i-: 1935 to 19 Weller fou: c~rcinomz c incidence iz in 450 case: At the ~ case~ the! period .191 1900 tO 19 genic carc 1914 the i

BRONCHIOGENIC CAKCINOMA ~, 1941, Imonary ght-year 30 the tes in- ,% for.~ rate 1930 emales ent : for cancer. Five of the females and 15 of the males are be- ing treated for cancer of the lung." He further estimates that between 450,000 and 500,000 people in 7the United States are under medical care. for cancer, of which about 13,000 are being treated for primary cancer of the bron- claus. Approximately 8,000 new cases of pr.imary bronchiogenic carcinoma are diag-nosed and receive medical care for the first time each year. Harnett found that whereas the total number of cancer deaths in the British Empire had increased 22%, cancer of the respiratory tract had increased 120%; and the deaths from carcinoma of the lung in males from 1921 to 1930 was 21.1 per million as contrasted with 100.9 per million in 1937. Jaff6 states that bronchiogenic carcinoma represents 11.47% of all carcinomas and that this lesion is second in fr .eftuency onIy to carcLrmma of the stomach and the intestines. According to Dick, the incidence of bronchiogenic carcinoma in the Glasgow Royal Infirmary has doubled and [or the years 1934 to 1938 in 3.98% of all autopsies a primary bronchiogenic carcinoma was found, an admission in- cidence of 0.101 of bronchiogenic carcinoma to all admissions. Wegelin observed a progressive increase in the incidence of bron- chiogenic carcinoma as determined at autopsy. In a series of lit cases studied at the Bern Pathologic Institute, it was found that the number of bronchiogenic carcinomas in each. 1,000 autopsies was as follows: from 1900 to 1904, .9.5; from 1905 to 1909, 1.8; from 1910 to 1914, 1.6; fi:om 1915 to 1919, 7.5; from 19E0 to 1924, 4.8; from 1925 to 19.99, 7.8; from I930 to I934, If2; from 1935 to 1939, 142. At the University of Michigan Hospiuil, Weller found that .in. the first 1,000 autopsies the incidence of carcinoma of the bronchus',to all autopsies was. 0.1% and that this incidence increased to 0.5% in the second thousand, and to 0.8% in 450 cases of the third thousand. At the University of Leipzig, Assmann found that in autopsy cases the incidence of bronchiogenic malignanci.'es during the period 1919 to 1922-was double the inddemce during the p~,'od 1900 to 1906. Hoffanan observed that the inddence of bronchio- genic carcinoma among all deaths has increased. Whereas in 1914 the incidence was 0.6% 100,000 p0pi~lation, in 1924 it had increased to 1.6% and in 1928 to I~9%. According to Fdenczy-

OCHSNER, DIXON, AND DEBAKEY and Matolcsy, the incidence of bronchiogenic carcinoma creased from 0.54% in 1896 to 10.3% in 1925. Fischer in Germany an incidence of bronchiogenic carcinoma creased from one and one-half to three times. According leb and Ang-rist, the incidence of bronchiogenic carcinomas as determined at autopsy is 14.71%, and the of bronchiogenic carcinomas to all autopsies is 2.41%. Staderman found that of the fatal cases that came to auto incidence of bronchiogenic carcinoma to all cancers was as contrasted with a similar incidence of cancer of the - 21.8% and of cancer of the stomach of 14.1%. At the Wisconsin General Hospital, according to 5.9% of deaths from neoplasms coming to autopsy have a chiogenic carcinoma. ~ccording to Olin and Elliott the of-primary bronchiogenic carcinoma to all malignancies as mined clinically was 4.7%. Perrone and Levimon state that of all carcinomas coming to necyopsy are bronchiogenic. .~, Steiner, in a series of collected cases, found that primary chiogenic carcinoma occurred in 0.99% of 93,560 autopsies formed throughout the United States, representing 9.47% ca~;cinomas. He found that at the University of Chicago genic carcinoma was third in f:requenc3" of all carcinomas as mined at autopsy. Holzer'found that the incidence of genic carcinoma as determined at autopsy has increased. 1895 to 1904 the ratio of bronchiogenic carcinoma was 0.07 with an incidence of ~.04% of all carcinomas. From 1905 to these respective incidences increased to 0.19% and 2".36%, from 1915 to 1924 to 0.47 and 6.69%. Olson, in reporting .cases of carcinoma cff the bronchus from the Boston City ' pital, found that the incidence of these lesions to all ~ increased annually from 7.5% in 1929 to 19.1% in 19.34. larly, Matz found that the incidence of bronchiogenic c~rcinoma -~--- toall carcinomas as determined at autopsy in the Veterans' -~r~u Hospital ~as 6.4% for the years 1927 to 1931, 15.8%.for ,years-1932 to .1937, and 23.'~% during th'e year. 1937., L6izaga -. : : ported an.incldence of 5.18% of carcinoma of the bronchus all' carcinomas in .the autopsies at the:'Institute of Anatomy of the Faculty of Ciendes Medicu~ of Buenos

BRONCHIOGENIC CARCINOMA the period 1898 to 1917 and an incidence of 1.4.6% during the od from 1918 to 1937. He also found that the incidence of carcinoma to all carcinomas in autopsy series at Francisco Janvier Hospital was 29.62% during the period to 1931 and 4225,% from 1932 to 1937. The relatively Lter increase in the incidence of bronchiogenic carcinoma is nsrrated by Rasahn's collected cases. Whereas the incidence all carcinomas as determined at autopsy increased from 10.27% period 1910 to I919 to 12% in the period 1920 to 1928, the of bronchiogenic carcinoma to all autopsies increased ~rom 0.44% to 0.89% in these respective periods. Similar result~ ,,ere obtained in the Dresden City, Hospital. Reinhaxd reported of autopsy studies in the period from 1852 to 1856 ix~ which the incidence of bronchiogenic carcinoma to all autopsies Was .0.05~, and to all carcinomas x~a.s 0.92%. Wolf reporting from the mine institution found an incidence of bronchiogenic malig- nancy to all autopsies was 0.35%, and Ran found that from 1909 t6 1914 the incidence of the bronchiogenic lesions to all card- noma was 2.72% knd from 1914 to 1919 was 4.66%. Thus, the incidence of bronchiogenic carizinoma in the same institution as determined at autopsy increased five fold during a 67-year period. We previously showed that from a review of the mortality sta- tistics of all persons dying in the United States of bronchiogenic raalignancies there was not only an actual increase in the number of deaths from this cause but also an annual increase in the death rate per hundred thousand population. We found that bronchio- genic carcinoma is increasiflg more than other malignancies. Whereas in the period from 1920 to 1936, inclusive, the incidences of carcinoma of the stomach, duodenum, liver, g-allbladder, uterus, and skin showed little or no increase, the incidence of cardnoma of the Imag showed a progressive rise." . Of 234,490 admissions m the Chari~y Hospital in New Or- leans from the tint of Janrary 1940 to the first of August 1944, -- bronchioge~|c carcinoma was diagno~, d 175 times, 154 Of which Were histologic~IIy prov~ed and 21 of which were diagnosed clini- .-- cally and by x-my (Fig. 2)- : ...... : ':-.--- - --:" : " ....... , Sex..~Broncl~_iogenic carcinoma occur~ pred~minantIy in males " ... and alth0ugh~the~r~Iative ~cidence.. in females has incr ,ea# re-_ .-_ _ ....~i.-.~.ii_ -~-. . - " Hgl .... ':i~f:)-: ........ " - " "-. ~.-~

OCHSNER, DIXON, AND DEBAKEY cently, it can be stated that there is a definite sex malignant disease of the bronchus in males. In a previous we found that in a series of 8,575 collected cases in which was stated, there were 6,769 males (78.9%) and 1,806 (21%). Thus it is seen that approximately 3 out of every nomas of the lung affect the male. As it has been the ~eater incidence of carcinoma of the bronchus in men past has been due to a ~eater prevalence of smoking sex (Ferrari), there will tend to be an equalization sexes because of the increased smoking among women. A~ cated previously, however, the incidence will probably so ~eat in women as in men because there probably is a predisposition in the male sex. It has been su~ested by that the cases which occlar in women might be due to change occurring on the basis of an adenoma, as adenomas in about equal frequency in both sexes. In Adler's series, mately 70% of the bronchiogenic.carcinomas occurred in W~elin, however, in his series of bronchiogenic mali 96 occurring in males and 21 in females, a relationship tol. Farberov found that of 150 case~ studied at the State Roentgen Radium Oncologic Institute at Karkov, 121 in males and 9 in females. According to Harnett, in a 1,065 cases of bronchiogenic carcinoma there were 871 in and 192 in females, a ratio of 4.5 to 1. In t90 cases of genic carcinomas which we have observed 166 (87.4%) and 24 (12.6%) were women (Fig. 3). In 58 cases in which have done a pneumonectomy for bronchiogenic carcinoma~,:~ (8I%) were in men and 14" (18.9%) in women (Fig. 4). - ~lge Incidence.. Primary bronchiogenic carcinoma with- ~exceptions occlaxs in older persons. Brunn. found that 576 cases occurred between the ages of forty and sixty Weller found the greatest incidence in the sixth and. a~e~. In Olson's series, 73.8% occurred in the seventh decades..F'tscher, in a series of 1,888 collected cases, ~that one-third of the tumors occurred in the fifth third after the ag~ of sixty~ and only 13% under the --There were four tumors in children under $ repo in a b, aca age. A less we itirst decat :fourth de~ d ~ have studi lade 2 fifth decao ~5 (_98.0% s). seventy 8~; the yo~ ectomy pe $e seventh de cent were i nineteen o~ patients. i the age There ge~ted to igeni~ catch

BRONCHIOGENIC C.,-~RCINOMA ere hich of collected cases, found the most frequent occurrence be- the ages of fifty and seventy years. Simons, in a collected of over 5,000 cases, found that over four-fifths of the cases between the ages of forty and seventy. The youngest reported was by iMcAldowie. He described a cancer of the in a child five and one-half months old. The lesion was not by biopsy but was demonstrated at autopsy. Beardsley te- a case which was histologically proved and in which the first nodule was noted at the age of ten months. Weill-Hall4 a primary bronchiogenic carcinoma in a child one year age. A number of cases have been reported occurring in pa- :tients less than I0 years of age (Gould; Lereboullet et al.; L6izaga; Field and Quilliam). In a series of 4,307 collected cases we previously reported, the following results were found: decade, 0.16%; second decade, 0.7%; third decade. 2.9%; fourth decade, 10.7%; fifth decade, 25.4%; sixth decade, 34.1%; seventh decade, 20%; eighth decade, 5.4%; and ninth decade, .0.58%. In the 190 cases of bronchiogenic carcinoma which we • have studied the following age incidences were found: second dec- 2 (1.1%); -,hird decade 2 (1.1%); fourth decade 12 (6.3%); fifth decade 44 (23.2%); sixth decade 64 (33.4%); seventh decade 55 (28_9%); eighth decade 10 (5.3%); ninth decade 1 (0.5%) (Fig. 5). Eighty-five per cent occurred between the ages ,of forty and seventy years. The average age ~-as 54. The oldest patient was 83; the youngest was 19 years of age. In our 58 cases of pneumon- ectomy performed for ,bronchiogenic carkinoma, the ages were as follows: second decade 2 (3.4%); third decade 2 (3.4%); fourth decade 5 (8.6%); fifth decade 14 (24.1%); sixth decade 24 (41.4%); ~. seventh decade 10 (17.2%); eighth decade 1 (1.7%). Sixty-five per cent were in the fifth and sixth decades. The youngest patient was nineteen ariZ._the eldest, seventy-two (Fig. 6). It is obvious the age - of patients subjected to pneumonectomy is somewhat lower than the age of all patients with bronchiogenic carcinoma (Fig. 7). __. -- ETIdLO~Y - " " =~ There have been many-explanations which have beqm sag- gested to account for the increase in the incidence o[ bronchio- genic carcinoma. Wintemi~ Wkson,and McNamara; because Of

OCHSNER, DIXON, AND DEBAKEY ~' anaplasia of the bronchial mucosa in persons dying enza, suggested that this change might be a precancerous and that as a result of the changes occurring in persons from influenza in the epidemic o[ 1918 an increase in dence of bronchiOgenic carcinoma may be accounted for. lar suggestion was made by Askanazy, who [ound in 38 o|.

BRONCHIOGENIC CARCINOMA ent~ dying o[ influenza "the normal columnar epithelium of the is replaced by stratified squamous epithelium or that occurred a metaplasia (protoplasia) of the bronchial mu- Similarly, others .(Barton, Berblinger, l.~schke, Mittasch, ~Mo~e, Schmidtmann, Teutschlaender) have suggested a possible p between the influenza epidemic in 1918 and the in- Fr~. ~ Fro. 5--Grai~hic representation of age inddence according t¢~ decades in Fro. e~Graphi¢ repress/ration of age iaciaen~e~ accSrd!ng to a~a= -

OCHSNER, DIXON, AND D~.BAKEy ~ crease in bronchiogenic carcinoma. Bauer and M( the first to report cases of bronchiogenic carcinoma fluenza. Berblinger and more recendy Oberndorfer that influenza i~ among the principal causes of ~mcer of On the other hand, Fried, in a series of 47 cases carcinoma observed since 1918, had only one in which a history of influenza. He stated the belief that little if any role in causing pulmonary carcinoma. Kiku~ the! thes, don freq~ opin for of th our ~cto~ worl mali: theli ,ot~ ~ fro= bro~ geni, Usp, chio