Thorax (1955), 10, 309.

BRONCHOGRAPHY IN PULMONARY TUBERCULOSISBY

PAUL FORGACSFrom Kettlewell Hospital, Swanley, Kent

(RECEIVED FOR PUBLICATION FEBRUARY 22, 1955)

For 30 years after the introduction of broncho-graphy by Sicard and Forestier (1922) iodized oilremained the only contrast medium in general use.During this period a large amount of informationwas published about the radiographic appearanceof the bronchi in most varieties of chronic pul-monary disease. The literature dealing withbronchography in pulmonary tuberculosis is scantyby comparison. Early hopes that iodized oilmight help to demonstrate tuberculous cavitiesmet with disappointment, because the bronchidraining them are usually too narrow and tortuousto admit the contrast medium (Landau, 1925).Dilatation of the bronchi leading to tuberculouslesions was noted by Grill (1927), who alsodescribed stenosis of one of the main bronchi inone of his cases. The appearance of the bronchiin pulmonary tuberculosis was discussed in moredetail by Leuret, Secousse, and Caussimon (1927),in an account based on 55 cases. They demon-strated fusiform and saccular dilatation of thebronchi, stenosis, and obstruction; but, like others,they were rarely successful in outlining cavities.For some years after these early reports interestin bronchography of tuberculous patients wastemporarily lost until the wider application ofsurgical treatment brought with it the need formore precise information about the topographyof the infection. The practical value of broncho-graphy in the localization of cavities was stressedfor the first time by Neuhof (1934), while Potterand Pagliughi (1936) and Cabitt, Singer, andGraham (1936) found that the calibre of thebronchi under a thoracoplasty gave some indica-tion of the success of the operation. The largestseries of tuberculous patients studied by broncho-graphy was reported in a series of papers byDormer, Friedlander, and Wiles (1944, 1945), wholaid emphasis on the more striking bronchialchanges, especially dilatation, encountered amongstover 2,000 bronchograms. An attempt to estimatethe incidence of bronchiectasis in tubercu!ouslesions was made by Murphy (1934), who notedit in 60% of his bronchograms, and by Boyer

(1946), who studied a series of 50 unselected casesand found dilatation in 85%. The somewhatlower figure of 51.8% is given by Buckles, Potts,Davidson, and Neptune (1951) in their report onthe bronchograms of 222 consecutive tuberculouspatients.As long as iodized oil remained the only con-

trast medium available for bronchography, thegeneral reluctance to carry out this investigationon tuberculous patients was well founded. It waswidely believed that a local tissue reaction toresidues of oil or the general effects of the iodineliberated might aggravate the disease, and that theintroduction of a large volume of liquid into thelung, irrespective of its chemical composition,might disseminate tubercle bacilli. The literaturebearing on this subject was reviewed by Marchese,Klassen, and Curtis (1952), who also studied theeffect of iodized oil in 49 of their own cases.They concluded that in stable or healing diseasethe method was safe, but in progressive pulmonarytuberculosis there was a risk of spreading theinfection. Another objection to the use of iodizedoil is its persistence. In a disease where progressis judged to a large extent by comparison of serialradiographs this disadvantage was serious enoughby itself to make the investigation unpopular.

Several favourable reports have appeared inthe last two years on the use of propyliodone(" dionosil ") in pulmonary tuberculosis. Theyall agree that the risk of spreading the disease isnegligible and that the clarity of subsequent radio-graphs is not impaired (McKechnie, 1953; Elphin-stone, Iles, and Laidlaw, 1954; Holden, 1954). AtKettlewell Hospital aqueous propyliodone, intro-duced by crico-thyroid puncture, has been exten-sively used since 1952, without any complicationmore serious than a transient febrile reaction.Now that the safety of this procedure is estab-lished the time seems opportune to examine thefirst consecutive sets of 120 bronchograms in orderto estimate the incidence of the bronchial changesand to assess the value of this investigation inpulmonary tuberculosis.

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PAUL FORGACS

SELECTION OF CASESA reliable estimate of the incidence of broncho-

graphic abnormalities in tuberculosis could bebased only on a series of unselected cases. Theperformance of such an uncomfortable investiga-tion at random cannot be justified, and only thosecases were therefore chosen where the broncho-gram might have provided information of prac-tical value. The grounds on which this selectionwas made were as follows. In one group of cases

bronchial changes were expected because of lobaror segmental consolidation, rapid inflation of acavity, or the presence of a large primary complex.In others bronchography was carried out beforeresection in order to study the extent of thedisease, or to localize a small lesion accurately,and to provide a guide to the origin and distribu-tion of the segmental bronchi. In a third group

the purpose of the investigation was to excludebronchial stenosis in patients about to undergocollapse therapy. Bronchograms were also takenoccasionally both before and during pneumo-

peritoneum treatment to study the degree ofrelaxation of individual segments.The extent and type of disease included in these

groups are not readily amenable to classification.Of the 120 patients, 76 were men and 44 were

women, between 17 and 67 years of age. Theyrepresent the population of a hospital treating allforms of pulmonary tuberculosis with the excep-

tion of advanced chronic disease. The broncho-grams were usually taken within the first threemonths of treatment.

ANALYSIS OF THE BRONCHOGRAMSBefore considering the bronchographic findings in

detail the limitations of this method of investigationshould be appreciated. Stenosis and obstruction ofperipheral bronchi, the study of which would be ofgreat interest, are difficult to demonstrate. Appear-ances suggesting such changes may be due to incom-plete filling; on the other hand a determined attemptto fill peripheral branches defeats its object by pro-

ducing a network of overlapping shadows. Cavitiescan rarely be outlined owing to the small calibre ofthe draining bronchus; in the present series this was

achieved in two cases only. Abnormal appearances

regularly demonstrable by bronchography are con-fined to variations of calibre and deviation of thelarger bronchi. Such changes may be of interest inthemselves and may also provide a clue to the anatomi-cal localization of lesions within their territory. Whenthe outline of the bronchi is normal, the bronchialtree can be used as a grid of reference against whichshadows in the lung may be accurately localized. Thebronchograms also provide evidence of variation inthe size of individual segments.

NORMAL BRONCHOGRAMS.-In 50 patients thebronchograms were normal. While this was to beforeseen in patients with small and localized tubercu-lous lesions, it was surprising to find consolidation ofa segment or a lobe resolve without leaving any dis-tortion of the bronchi. Even where the lung still con-tained extensive and conspicuous lesions it was notunusual to find the bronchi leading to them perfectlynormal. So much stress has been laid on broncho-graphic abnormalities in tuberculosis that their absencein nearly half of the cases in a series selected with abias towards bronchial disease is worth noting.BRONCHIAL DILATATION.-This is the commonest of

all bronchographic abnormalities seen in pulmonarytuberculosis. The picture is that familiar in mild chronicbronchiectasis, with beading of the larger bronchiand cylindrical widening of their branches. Grossbronchial dilatation comparable in degree with severechronic bronchiectasis was not seen, even in segmentsor lobes destroyed by tuberculosis. This was un-expected in the light of previous reports which havelaid emphasis on such changes (Dormer and others,1945). In our series bronchial dilatation was foundin 33 cases, and in all but eight it was slight.DIVERTICULOSIS.-Small diverticula, less than 1

mm. wide and projecting 1-2 mm. beyond thebronchial silhouette, were seen in 16 bronchograms(Fig. 1). They usually occurred in groups, giving acrenated outline to the bronchus, closely resemblingdiverticulosis of the colon on a miniature scale. Theinferior profile of the left upper lobe bronchus andof the trunk of the lingula are the commonest sitesof these diverticula. They may be encountered occa-sionally on the primary branches of the segmentalbronchi, but do not occur more peripherally. Theirappearance is identical with that of the diverticuladescribed in chronic bronchitis (Stutz, 1948; Fischer,1950; Simon and Galbraith, 1953). It is known thatthey represent dilated ducts of the bronchial mucousglands (Stutz, 1948; Duprez and Mampuys, 1953).BRONCHIAL STENOsIs.-Stenosis of a lobar or seg-

mental bronchus was demonstrated in two cases only.They were suffering from primary tuberculous infec-tion of the lung supplied by the stenosed bronchus.In one of these the right upper lobe bronchus wasnarrowed to half its normal diameter and its anteriordivision tapered to a complete obstruction. A secondbronchogram after eight months' treatment showedno change in the anterior segmental bronchus, butthe localized stenosis of the lobar bronchus had dis-appeared (Fig. 2). The bronchograms of the otherpatient demonstrated stenosis in two places: in theleft upper lobe bronchus, and in its superior divisionimmediately beyond its origin. At both sites thebronchus was narrowed to half its normal calibre.This patient had already received six months' chemo-therapy and the stenosis was therefore considered tobe permanent.The difficulty of demonstrating stenosis in peri-

pheral bronchi has already been mentioned. Because

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FIG. I.-Diverticulosis of the left upper lobe bronchus and ofits two primary divisions.

FIG. 3.-Characteristic tapering and irregularity of a bronchus draining a cavity inthe apical segment of the right lower lobe.

FIG. 2A.-Inflssrrimariy stercsis of rl-e right upper lobe bionchus FIG. 2B.-After five months' cherroti erapy the calibre of the rightand obstruction of its anterior brsnch. upper lobe bronchus is normal, but the obstruction of its anterior

branch remains.

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PAUL FORGACS

of this no reliable estimate can be made of its inci-dence. Amongst the bronchograms in which peri-pheral filling was adequate and at the same time detailwas not lost in the maze of superimposed shadows,stenosis of the bronchus draining a cavity was seen

in three instances. The appearance of such bronchiis characteristic. The normally smooth silhouette ofthe bronchus becomes grossly irreguiar and tapers toa fine point over a distance of about 1 cm. (Fig. 3).

OTHER ABNORMALITIES.-Unexpected bronchiectasisof the lower lobe in the presence of abnormal shadowsconfined to the upper lobe was found in two patients.There was no indication in their past history, physicalsigns, and in the standard radiographs of disease ofthe lower lobe. In another patient collapse of theright middle lobe was discovered by bronchography.

PRACTICAL APPLICATIONSThe conclusion reached from a review of 120

consecutive bronchograms of tuberculous patientsis that the practical value of this investigation islimited. The information it provides is useful,but often obtainable by simpler methods. Onthe other hand, bronchography may occasionallydemonstrate some unsuspected and importantabnormality, and has therefore certain indications.The most useful place of bronchography is

amongst the preliminary investigations leading tomajor thoracic surgery. As a method of localiz-ing tuberculous lesions to a segment or to its sub-divisions it is helpful but not superior to lateraltomography. Both methods have their limita-tions: bronchography provides an excellent frameof reference, but the lesion to be localized is notso clearly shown as in tomograms, while the frameof reference provided by vessels, bronchi, andfissures in lateral tomograms is less precise,especially where segmental subdivisions are con-

cerned. Bronchograms were found particularlyvaluable in localizing the disease to subdivisionsof segments, and in deciding whether disease inthe upper lobes was confined to the apical andposterior segments or extended into the anteriorsegment or into the apical segment of the lowerlobe. Advance information about the configura-tion of the bronchial tree, especially in theanatomically variable left upper lobe, can alsobe useful at the time of the operation.

Similar conclusions about the value of broncho-graphy before resection were reached by severalauthors. Gordon, Zinn, Brook, and Pratt (1951)compared their bronchograms with necropsy andresection specimens injected by radio-opaquematerial and found the bronchographic changesa useful guide to the localization of pulmonarylesions. They also pointed out that the bronchial

changes in a lung covered by thickened pleurareflect the extent and severity of the disease andhelp to decide whether decortication is advisable.The advantages of bronchography in planning theextent of resections are stressed by Ibers, Vieten,and Willmann (1951), by Thurn (1954), and byShaw, Collins, and MacNamara (1954).The occasional discovery of unsuspected bronchi-

ectasis of the lower lobe in the presence of tuber-culosis would by itself justify the routine use ofbronchography before resection. The chancefinding of silent bronchiectasis in a healthyperson may not be of immediate relevance, butin a tuberculous patient it demands investigationto see whether tubercle bacilli are established inthe bronchiectatic lobe. The importance of thisfinding in the two patients reported was evengreater, for in both resection of the upper lobehad been contemplated. Even where the difficulttask of excluding a tuberculous infection in thebronchiectatic lobe can be accomplished in suchcircumstances, the danger of post-operative failureof expansion and of secondary infection remains.The choice lies between extending the resection tothe bronchiectatic lobe and removing the lung, aswas done in both these cases, or abandoning theidea of resection in favour of some more conserva-tive line of treatment. This particular problem,with a case illustrating it, is mentioned by Rabino-witz and Harper (1951).As a diagnostic aid in pulmonary tuberculosis

bronchography is of limited value, since most ofthe bronchial changes discovered are not peculiarto this disease. The only exception is bronchialstenosis found at a distance from a lung shadow.This, being a feature of tuberculous bronchitis,may help to exclude other inflammatory or neo-plastic conditions.Where the diagnosis of pulmonary tuberculosis

is already established, bronchography contributeslittle to a fuller understanding of the disease. Thebronchi draining tuberculous cavities are usuallytoo small to be studied by bronchography, and,although they may be demonstrated accidentally,more often they are lost in a network of super-imposed shadows. The study of tuberculosisspreading along the submucosal lymphatic chan-nels and of the lesions arising from this type ofinfection also proved unrewarding for the samereason. Cavities were outlined very rarely and inno instance was an unsuspected cavity demon-strated by the contrast medium.The practical value of detecting dilated bronchi

within a tuberculous lobe or segment is small.When the surrounding parenchyma is atelectatic,

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BRONCHOGRAPHY IN PULMONARY TUBERCULOSIS

the dilation may be due entirely to the increasedpressure gradient on either side of the bronchialwall, so that damage to the bronchus cannot beinferred. In most bronchograms, however, shrink-ing of the lung could not be held responsible forthe bronchial dilation, which was thereforeattributed to damage to the bronchial wall by thetuberculous infection. Active and healed tuber-culous bronchitis could not be distinguished bythe appearance of the dilated bronchi, since theywere similar in untreated cases and in thosewhich had received adequate chemotherapy. On

bronchoscopy the segmental orifice leading tosuch dilated bronchi was in some patients con-

gested and discharging pus; in others the mucosa

was normal, but mucus was oozing from thebronchus; in many cases, however, the bronchialorifice was normal. The conclusion to be drawnfrom these observations is that bronchial dilatationis as likely to be due to active as to healed tuber-culous bronchitis, and that its presence merelyreflects one aspect of the destruction wrought bythe disease. It is rarely severe enough to beregarded as bronchiectasis in the clinical sense.

It was never found to be responsible for thecircular or oval translucencies in plain radio-graphs, which are so often attributed to it.

Diverticulosis of the! bronchi may be a sequelof tuberculous bronchitis and can be interpretedas such when these bronchi lead to tuberculousparenchymal disease. It may also occur in othersituations, where it may be the sequel of otherforms of bronchitis. The reason for the highincidence of diverticula on the inferior profile ofthe left upper lobe bronchus and on the trunk ofthe lingular bronchus, common to chronic bron-chitis and tuberculosis, is not known.

COMPLICATIONSNo serious complication occurred, and spread

of tuberculosis, in particular, was never seen.

The lungs were usually clear of contrast mediumwithin 48 hours and always within a week, excepton one occasion when propyliodone entered a

cavity and persisted for 28 days.Occasional fluctuations of temperature above

990 F. (37.2° C.) were common in these tuber-culous patients, and a pyrexia exceeding 99.6° F.(37.60 C.) on the day following bronchographywas therefore arbitrarily chosen as evidence of a

reaction to propyliodone. It occurred in 34patients, rarely lasted longer than 24 hours, andalways settled in less than four days. The pyrexiawas sometimes accompanied by malaise, headache,and pains in the limbs. Radiographs taken during

this reaction did not show pulmonary consolida-tion, the white cell count and the sedimentationrate did not rise, and the urine remained normal.Amongst the 21 patients subjected to a secondbronchography, usually after an interval of threemonths, this pyrexial reaction was observed onthe first occasion alone in seven, on the secondoccasion alone in two, and both times in three.The amount of residual propyliodone in the lungsor the amount swallowed during the injection boreno relation to the incidence or severity of thesesymptoms. The cause of the reaction is probablya toxic effect of propyliodone absorbed from thelungs. It is evidently not due to infection or tosensitization by the contrast medium. It alsooccurs after bronchography in other diseases andcannot therefore be attributed to a tuberculinreaction.

SUMMARYA series of 120 bronchograms performed with

aqueous propyliodone (" dionosil ") in patientswith pulmonary tuberculosis is reviewed. It isconcluded that this procedure is safe and holds amodest place amongst other investigations as apreliminary to major surgical procedures, especi-ally resection. It can be of considerable help inlocalizing the site of the disease with precision,and in demonstrating unsuspected bronchialabnormalities in radiologically intact parenchyma.Since no bronchographic feature peculiar to activetuberculosis was discovered, this investigationprovides no indication of the state of healing ofthe disease.

REFERENCESBoyer, L. B. (1946). Amer. Rev. Tuberc., 54 111.Buckles, M. G., Potts, W. L., Davidson, H. B., and Neptune, W. B.

(1951). Ibid., 64, 394.Cabitt, H. L., Singer, J. J., and Graham, E. A. (1936). J. thorac.

Surg., 5, 259.Dormer, B. A., Friedlander, J., and Wiles, F. J. (1944). Amer. Rev.

Tuberc., 50, 283.- (1945). Ibid., 51, 62, 455, 519.

Duprez, A., and Mampuys, R. (1953). Thorax, 8, 141.Elphinstone, N. C., Iles, K. C., and Laidlaw, E. F. (1954). Brit. J.

Tuberc., 48, 33.Fischer, F. K. (1950). Fortschr. Rontgenstr., 72, 653.Gordon, J., Zinn, B. W., Brook, R., and Pratt, P. C. (1951). J.

thorac. Surg., 22, 109.Grill, C. (1927). Acta med. scand., 65, 300.Holden, W. S. (1954). Paper read at the Meeting of the British

Tuberculosis Association, Oxford.Ibers, G., Vieten, H., and Willmann, K. H. (1951). Fortschr. Ront-

genstr., 74, 667.Landau, W. (1925). Klin. Wschr., 4, 1861.Leuret, E., Secousse, H., and Caussimon, J. (1927). J. Mid. Bordeaux,

104, 215.McKechnie, J. K. (1953). Tubercle, Lond., 34, 271.Marchese, V., Klassen, K. P., and Curtis, G. M. (1952). Amer.

Rev. Tuberc., 66, 699.Murphy, J. E. (1934). Amer. J. Roentgenol., 31, 301.Neuhof, H. (1934). Ibid., 31, 289.Potter, B. P., and Pagliughi, J. (1936). Ibid., 36, 30.Rabinowitz, P.. and Harper, I. S. H. (1951). Dis. Chest, 19, 66.Shaw, K. M., Collins, D. M., and MacNamara, J. (1954). Amer. Rev.

Tuberc., 70, 274.Sicard, J. A., and Forestier, J. (1922). Bull. Soc. med. H6p. Paris

46, 463.Simon, G., and Galbraith, H. J. B. (1953). Lancet, 2, 850.Stutz, E. (1948). Rontgenpraxis, 17, 91.Thurn, P. (1954). Fortschr. Rontgenstr., 80, 198.

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