Thorax (1955), 10, 220.

A CLINICO-PATHOLOGICAL STUDY OF ATELECTASIS INPULMONARY TUBERCULOSIS

BY

LESLIE J. TEMPLEFrom the Department of Surgery, University of Liverpool

(RECEIVED FOR PUBLICATION APRIL 12, 1955)

The literature of atelectasis in pulmonarytuberculosis is both vast and controversial. Inthe past, attention has been drawn mainly toatelectasis of lung complicating artificial pneumo-thorax. With the decrease in this method oftreatment, however, the problem of atelectasis hasnot disappeared. The association between bron-chial obstruction and atelectasis was noted byboth Gairdner (1851) and by Bastian (1871), butthe examples they observed were not tuberculous.The mechanism of this type of atelectasis has beenvery fully discussed by Pasteur (1908, 1914), byLee Lander (1936, 1946), and by Lee Lander andMaurice Davidson (1938a and b). None of theseobservations, however, can be taken as necessarilyapplicable to atelectasis in pulmonary tuberculosis.

Coryllos (1933) examined the question exhaus-tively. He considered that atelectasis was alwaysdue to bronchial obstruction and believed thatobstruction of the bronchus with atelectasisinvariably produced cavity closure unless thecavity wall was too rigid. That his concept is notentirely correct is shown in the first illustration hegives of atelectasis of the right upper lobe; afterthe induction of artificial pneumothorax the" atelectatic " upper lobe is clearly larger than theaerating lower lobe. The condition, therefore, isnot one of true atelectasis. Moreover, his illus-trations of stem cavities show a patent bronchusopening into the cavity and surrounding it is aring of atelectasis. An explanation of this con-dition is offered in the ensuing section. Coryllosdenied the existence of pressure atelectasis andconsidered that closure of cavities was always dueto bronchial obstruction.Erwin (1939) reviewed a similar group of cases

and he too believed that atelectasis was always dueto bronchial obstruction but noted its rarity as asegmental disease. Pinner (1945) believed thatuncomplicated atelectasis in pulmonary tubercu-losis was rare and he had never in fact seen it atnecropsy. He pointed out the snares in the

diagnosis of atelectasis and observes that manyexamples so diagnosed are not the simple atelec-tasis which one would expect if the collapse weredue to bronchial occlusion. More recently Clegg(1953), in discussing the distal lymphatic endo-bronchial spread of tuberculosis, has shown in thelater stage of this lesion that when the bronchialwall has been destroyed patches of atelectasisappear round the bronchus. If this happens inrelation to several small bronchi these patchestend to approximate and finally to fuse. How-ever, in those examples of healed disease of thistype in which he shows a segmental bronchuscompletely occluded, there is no atelectasis. Thissuggests that his explanation is inadequate, andthat atelectasis cannot be due merely to theblocking of a small peripheral bronchus. Whit-well (1952) in writing of bronchiectasis has shownthat even though all communications between asegmental bronchus and the lung may be sealedoff, the alveoli remain well aerated-evidentlyfrom other bronchi.

Other theories of the causation of atelectasishave been put forward, and the suggestion thatreflex spasm of the involuntary muscle fibre of thelung is responsible for it has been made byXalabarder (1949) and Hoffstaedt (1953). Theyrecognize that bronchial obstruction alone is notalways responsible for the atelectasis of part of alung, but suggest that it may be one of the stimulithat result in " reflex atelectasis."The clinical aspects of this condition have been

discussed by Sadler (1954), who followed uppatients who developed atelectasis after treatmentby artificial pneumothorax at the Cheshire JointSanatorium. He tried to trace the subsequentcourse of the disease in patients with and withoutatelectasis. He demonstrated a clear correlationbetween atelectasis and the onset of pleuraleffusion, although he believes this to be due to thegreater extent of the disease in the patients withatelectasis. The long-term follow-up is limited to

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CLINICAL PATHOLOGY OF ATELECTASIS

159 patients out of 266, and only in three casesout of 20 of persistent cavitation was a follow-upobtained. This in itself is an indication of thebad prognosis associated with atelectasis in cavi-tating disease. He concludes like Erwin thatpermanent atelectasis is a desirable end-result fora severely diseased lobe. Nevertheless in the finaltable, after excluding patients with a persistentcavity, he shows that within eight years the deathrate for total atelectasis is 15.4%, for lobaratelectasis 6.8%, for segmental atelectasis 5.9%,and for non-atelectatic disease 2.3%.Houghton (1950) stated: " Atelectasis as a com-

plication of pneumothorax is a constant precursorof tuberculous empyema and is frequently asso-ciated with ultimate relapse." Many chestphysicians with whom the present author hasworked would, from their own experience, echothis statement. Maher-Loughnan (1950) alsoshowed that patients with atelectasis complicatingan artificial pneumothorax are very likely to deve-lop pleural effusion, empyema, and bronchialspread. Not all writers, however, accept this, andFarquharson (1951) does not think that the prog-nosis in such patients is necessarily bad.

Coello (1951) and Coello and Nagley (1948),observing atelectatic areas through the thoraco-scope, tried to distinguish two types of atelectasis-one relatively benign, the other dangerous andliable to lead to empyema. Similar conclusionsare reached in the present paper, and a patho-logical basis suggested.

METHOD OF INVESTIGATION

An examination of specimens of lung or por-tions of lungs resected for pulmonary tuberculosishas been carried out since 1949. Each specimenis distended and fixed with formalin at such apressure as to maintain it in its original life size.It is then embedded in gelatin, frozen, and slicedas a whole into sections 500 ,u thick in a coronalplane, sectioning as far as possible the wholespecimen. At appropriate points through theblocks small pieces of tissue are removed formicroscopic examination. The methods usedthroughout have been a modification of those ofGough and Wentworth (1949). An examination iscarried out of every section so that it is possibleto build up the entire anatomy of the specimen.The bronchi are followed through the sections,and their relationship to cavities and other lesionsis noted. A few representative sections aremounted. To this gross anatomical study is addeda report of the histology, and then an attempt is

made to correlate the picture presented with theradiographs and the clinical details of the patientbefore and after operation. In this way 125specimens have so far been examined, and a pre-liminary attempt has been made to separate theminto different clinical types of disease. This paperconcerns those patients on whom a pre-operativediagnosis of atelectasis was made.The resections in every one of these patients

were carried out because clinically it was con-sidered advisable to do so, and not because of anypreconceived theory that resection should be donein every patient in whose lungs a patch of atelec-tasis was seen. To this extent only are the patientsa selected group and it was inevitable that theselection was largely of those whose clinical coursewas not satisfactory.

ILLUSTRATIVE RECORDS

In the first group of patients, there was com-plete or almost complete stricture of a mainbronchus. Most of the specimens in this groupare whole lungs with stricture of a main bronchus,but there are a few in which a lobar bronchusonly is involved, the interlobar fissure is complete,and atelectasis is limited to a lobe. All thesespecimens show gross bronchiectasis, and thealveolar tissue consists of an atelectatic rind arounddilated bronchi filled with inspissated tuberculouspus. Fig. 1 is a section through a complete rightlung. In this patient the right main bronchus wasonly 2 mm. in diameter at the carina, and radio-graphic examination showed that the right lungwas non-aerating. The sputum occasionally con-tained tubercle bacilli and on two occasions aminor spread of disease to the left lung took place.On first sectioning the resected lung, all the spaceswere filled with caseous material (some of it hasdropped out in the mounted section). Microscopyshowed the caseous masses to be contained by alayer of ciliated epithelium, that is, they are lyingin greatly distended bronchi. The lung tissueremaining between the bronchi is fibrotic and thesmall foci in it well healed. Fig. 2 is a similarspecimen which actually demonstrates the stric-ture. All the caseous contents have dropped out.Fig. 3 shows a left lung with atelectasis of theupper lobe only. The main bronchus wasnarrowed, but the upper lobe bronchus had dis-appeared completely. The upper lobe consists ofdilated bronchi embedded in atelectatic fibroticlung.

All these specimens show pathological featuresidentical with a group of lungs diagnosed pre-

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FIG. 1.-Section of a totally atelectatic lung with bronchi full ofcaseous material.

FIG. 2.-Section of whole lung showing bronchial stricture.

FIG. 3.-Lung with stricture of upper lobe only.7

FDo. 3

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CLINICAL PATHOLOGY OF ATELECTASIS

operatively as tuberculous bronchiectasis or des-troyed lung. They differ only in the presence of amajor bronchial stricture. In the group without astricture the bronchi are largely empty and thepre-operative radiological appearance has sug-gested extensive bronchiectasis or cavitation andnot atelectasis. In both types there is littleevidence of active disease and the main danger tothe patient appears to be due to the retention ofcaseous material or pus which might on occasionflood the healthy lung.The second group of patients showed atelectatic

lobes which contained large, patent cavities. Thealveolar tissue forms the thick wall of the cavity.Fig. 4 is the radiograph of a young woman whohad a cavity in the left upper lobe. An artificialpneumothorax produced atelectasis of the lobewhich persisted even after the artificial pneumo-thorax was abandoned. In spite of total collapseof the lobe the cavity remained patent. Fig. 5 isa section of the removed lobe. The cavity is linedby cascous material and granulation tissue whichextends irregularly into the surrounding atelectaticlung. There is almost no fibrosis and little locali-zation of the disease. The cavity did not collapsewith the lobe for the same reason that the cavitiesin a Gruyere cheese do not collapse-the caseouswall is too rigid. The lobar bronchus showsneither narrowing nor marked endobronchialdisease.The third group of patients were those show-

ing only partial atelectasis of a lobe. Most ofthese were removed from under an artificialpneumothorax. It was in this group that a num-ber of specimens diagnosed pre-operatively asatelectasis proved to have no collapse pf lung, buta solid mass of disease. These were naturallyrejected from the series. In none of these speci-mens of partial atelectasis did the area collapsedcorrespond to a segment and in no instance wasstricture of a segmental bronchus found.

Fig. 6 is the tomograph of a patient whose pul-monary cavity closed while in a sanatorium andwhose treatment included an artificial pneumo-thorax. As is shown in the radiograph a patch ofatelectasis persisted in the left upper lobe. Theclinician in charge was unhappy about this patient,not because of the radiological appearance, butbecause the clinical progress was unsatisfactory.The lobe was therefore resected. Fig. 7 is a sectionthrough the lobe; it shows two caseous noduleslying astride an intersegmental plane and sur-rounded by a mass of atelectatic lung. A sectionmore anteriorly (Fig. 8) shows fusion of nodulesand disease spreading into the atelectatic area. Aphotomicrograph (Fig. 9) of the caseous edge of

FIG. 4.-Radiograph showing atelectatic left upper lobe with cavity.

FIG. 5.-Section of lobe removed from patient whose radiograph isshown in Fig. 4.

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FIG. 6.-Tomogram showing area of atelectasis in left lung. FIG. 9.-Photomicrograph from edge of tuberculous area in the samecase..._..

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FiG. 7.-Section through upper lobe from Fig. 6.

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FIG. 8.-Section through same lobe further forwards.

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the disease makes it clear that there is no delimit-ing encapsulation. The tuberculous process isextending freely into the surrounding compressedand flattened alveoli. The absence of anyfibrosis underlines what might be called themalignancy of the advancing tuberculous disease.

Fig. 10 is a section of a lobe showing patchyatelectasis between solid nodules of disease;localization of the lesion is poor and incomplete.This specimen was removed from a patient whoseradiograph showed areas of atelectasis after in-duction of an artificial pneumothorax.

Fig. 11 is the radiograph of a patient with anartificial pneumothorax on the left side. Partialatelectasis of the upper lobe is present. Section ofthis lobe (Fig. 12) shows two areas which consistof caseous nodules embedded in atelectatic lung.The histological examination of these areasrevealed actively spreading disease.

In the patient whose lung section is illustratedin Fig. 13 half of the upper lobe is atelectatic,lying compressed between irregularly fusingnodules of disease. The area corresponds to nosegmental distribution.

In another patient, who developed an area ofatelectasis under an artificial pneumothorax, the FIG. 10.-Tuberculous nodules and surrounding atelectasis.

FIG. 11.-Radiograph showing partial atelectasis of right upper lobe 1. . 12.-Section through Lobe removed from the same patient.under an artificial pneumothorax.

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FIG. 13.-Caseous nodules and compressed surrounding lung.

FIG. 15.-Caseous lesion with atelectasis in apical segment of lowerlobe and similar lesion below the apical bronchus.

FIG. 14.-Caseous nodules and surrounding compressed lung.

artificial pneumothorax was nevertheless main-tained, and eventually an effusion formed.Lobectomy was later carried out, and the specimen(Fig. 14) shows the airless alveoli compressed be-tween nodules of actively spreading disease.The next example illustrated (Fig. 15) had a

pneumoperitoneum and phrenic crush beforeremoval of the left lower lobe. The apical caseousmass has a rind of atelectatic lung around it anda similar small nodule near by-not in the apicalsegment-has a similar rind. There was no grossdisease of the segmental bronchi.

DISCUSSIONAll the specimens examined, including the

examples described, seem to fall into one or otherof two different pathological entities. On the onehand there are the destroyed lungs with bronchialstricture. What remains of the lung tissue isfibrotic and completely airless; it shows excellenthealing, and these lungs are dangerous only whenthere is pent-up tuberculous material which may onoccasion flood over and infect the opposite lung.In these patients the atelectasis is not in itselfharmful.

Fl,

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CLINICAL PATHOLOGY OF ATELECTASIS

The other pathological entity is shown in theexamples described of lobar atelectasis and partialatelectasis of the lobe. This type of disease ischaracterized by the relentless spread of activeinfection into the surrounding atelectatic lungwith histological evidence of inadequate resis-tance. In the past, partial atelectasis in a lobe hasbeen regarded as segmental, and associated withobstruction of the corresponding bronchi. In fact,in no case examined was a segmental bronchusfound to be involved by the disease, and thedistribution of the lesions followed no segmentalpattern. This could have been anticipated fromthe experience of all thoracic surgeons that a seg-mental bronchus can be clamped at operationwithout producing any atelectasis. When a lungis relaxed, as, for example by artificial pneumo-thorax, the structures in it tend to get smaller;tuberculous lesions, such as cavities and fibroticinfiltrations, will presumably contract in propor-tion to or even selectively to a relatively greaterextent than the surrounding alveoli. If, on theother hand, the disease is solid or infiltrating intothe surrounding tissue so that the alveoli containoedema fluid and their walls show cellular infil-tration, the diseased portion of lung will be rigidand cannot occupy a lesser volume when the wholelung volume is reduced. Consequently the sur-rounding alveoli are compressed by this islet ofsolid material in the collapsing lung and atelectasisforms in a layer around the lesion. Where anumber of lesions are in fairly close proximitycollapse will bring them closer together and theirrinds of atelectatic lung are likely to fuse into asingle mass which becomes visible radiologicallyas a partial atelectasis. This has been clearlydemonstrated by Clegg in the work previouslyreferred to. Fig. 16 is an attempt to illustrate thisphenomenon diagrammatically. Here, atelectasisis a manifestation that the disease is still activelvinfiltrating into surrounding lung.A similar argument applies with regard to cavi-

tating disease. If the cavity wall is thin andfibrotic it will at least diminish in proportion tothe relaxation of the lung (Fig. 17). On the otherhand, if the disease is still actively infiltrating intoand destroying alveolar tissue, the wall is rigidwith caseous material and oedema, and it cannotrelax. It is against this rigid lesion that the sur-rounding alveoli are compressed and become air-less. (Fig. 18, which represents this diagrammatic-ally, should be compared with Fig. 5.)

CONCLUSIONS AND SUMMARYA clinico-pathological investigation of atelec-

tasis in pulmonary tuberculosis indicates that it

FIG. 16.-Diagram illustrating the effect of artificial pneumothorax ontwo active lesions with compression of intervening lung.

FIG. 17.-Fibrotic healing cavity closing with artificial pneumothorax.

FiG. 18.-Thick-walled cavity failing to close with artificial pneumo-thorax and with compression of surrounding lung.

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LESLIE J. TEMPLE

may be comparatively harmless or it may bedangerous. Collapse of a whole lobe or of a lungmay be due to bronchial occlusion, either byreason of tuberculous stricture, or of obstructionby tuberculous glands from without or accumu-lated secretions within the bronchus. The con-dition which results is essentially one ofbronchiectasis with or without the retention ofcaseous material in the dilated bronchi. Coello's"safe atelectasis " is probably of this nature.Moreover, a lung with fairly extensive tuber-

culosis may, after collapse therapy, show conden-sation of the disease, but no true compression ofalveoli ; the patient does well, and experienceshows that this is in fact a healing stage in thedisease.On the other hand, if the lesion in the lung is

comparatively small, yet after the induction ofartificial pneumothorax or other measures ofcollapse appreciable areas of atelectasis appear,then the disease should be regarded as highlyactive. Obstruction of the segmental bronchi doesnot appear to be a causal factor. The alveolisurrounding the lesion are compressed by therigid mass of active tuberculous infiltration andoedema. This type of "compression atelectasis"is a danger signal to warn that the disease is activeand still advancing and that it may sooner or laterinvolve the pleura, with consequent tuberculousempyema. Furthermore, it is not surprising thatcavities with similarly infiltrated walls fail to closewhen collapse therapy is attempted.

While I take sole responsibility for all the viewsexpressed, I must acknowledge my indebtedness tomy various colleagues on the Liverpool Chest Unitboth for letting me have some of the specimens andfor criticism and discussion. In particular I shouldlike to thank Dr. Robert Coope. All the technicalwork of this investigation has been carried out byMr. Harold Nevin and Miss Maureen Litchfield, ofthe Liverpool Department of Surgery. I have tothank Professor Gough, of Cardiff, for the patientinstruction so kindly given me in his laboratory tech-niques. The work was carried out at the Departmentof Surgery, University of Liverpool, with the help andencouragement of Professor Charles Wells and withthe aid of a grant from the United LiverpoolHospitals.

REFERENCES

Bastian, H. C. (1871). In A Systenm of .wedicine, ed. J. R. Reynolds.Macmillan, London. Vol. 3. p. 830.

Clegg, J. W. (1953). Tfiorax, 8, 167.Coello, A. J. (1951). J. thorac. Surg., 21, 135.- and Nagley, M. M. (1948). Tubercle, 29, 231.Corvllos, P. N. (1933). Amer. Rev. Tuberc., 28, 1.Erwin, G. S. (1939). Bromptoan Hosp. Rep., 8, 43.Farquharson, M. (1951). Tubercle, 32, 108.Gairdner, W. T. (1851). Monthly J. med. Sci., 12, 440.CGough, J., James, W. R. L., and Wentworth, J. E. (1949). J. Fac.

Radiol., Lond., 1, 28.Hoffstaedt, E. G. W. (1953). Tuibercle, 34, 234.Houghton, L. E. (1950). Ibid., 31, 50.Lander, F. Lee (1936). Proc. roy. Soc. Mted., 29. 1383.--(1946). Thorax, 1, 198.

and Davidson, M. (1938a). Brit. miied. J., 1, 1047.(1938b). Brit. J. Radiol., 11, 65.

Maher-Loughnan, G. P. (1950). Tubercle, 31, 74.Pasteur. W. (1908). Lancet, 2, 1351.

-(1914). Brit. J. Surg., 1, 587.Pinner, M. (1945). PulmonarY Tutberculosis in the Adult. Thomas,

Springfield, Illinois.Sadler, R. L. (1954). Brit. med. J., 1, 359.Whitwell, F. (1952). Thlorax, 7, 213.Xalabarder, C. (1949). Tutbercle, 30, 266.

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