Thorax 1990;45:503-508

Bronchography in the assessment of patients withlung collapse for endoscopic laser therapy

P J M George, M C Pearson, D Edwards, RM Rudd, M R Hetzel

AbstractIn an attempt to improve selection ofpatients and the efficacy of endoscopiclaser treatment, a bronchographic tech-nique has been developed for patientswith tumours causing completeendobronchial obstruction. This tech-nique has shown patent distal airways in16 out of 17 patients with a collapsed lungor lobe. These airways were abnormallydilated in each case, suggestingbronchiectasis. In one patient theappearances of bronchiectatasis weresufficiently severe to decide againstattempting treatment. Treatment wasnot attempted in another patientas a large cavity was seen within thecollapsed lung and this was thought tocarry a risk of postoperative infectionand haemorrhage. Treatment with aneodymium YAG laser under generalanaesthesia successfully recanalised theairway in 12 of the 15 remaining patientsand was associated with a substantialreduction in breathlessness. Theprocedure was abandoned prematurelyin one patient because of life threateninghaemorrhage. In the remaining twopatients in whom treatment was unsuc-cessful bronchography had suggestedvery extensive endobronchial obstruc-tion. Spirometry and radionuclide lungscans were performed before and aftertreatment in eight patients treatedsuccessfully and showed significantimprovements. Four patients wereinvestigated within two weeks of lungre-expansion by repeat bronchography(three patients) or computed tomo-graphy (one patient); in each case thecalibre of the airways had returnedalmost to normal. Thus the radiologicaldemonstration of bronchial dilatation ina collapsed lung does not necessarilyimply a diagnosis of irreversible bron-chiectasis and should not be regarded asa contraindication to treatment. It isconcluded that preoperative bron-chography provides reliable data on theextent of tumour, the patency of the dis-tal airways, and presence of extensivecavitation. This information shouldfacilitate successful laser treatment.

The neodymium YAG laser provides a con-venient method of relieving large airwayobstruction in patients with advanced lung

cancer. The thermal effects of the laser maybe used to resect and cauterise intraluminaltumour and, in appropriately selected cases, topalliate breathlessness and other obstructivesymptoms. Treatment produces symptomaticimprovement in about 70-80% patients withpartial airway obstruction but is considerablyless successful in patients with tumours caus-ing complete endobronchial obstruction andatelactasis.'2 For example, successful re-expansion was achieved in only five of 17patients with a collapsed lung or lobe.'There are several possible explanations for

this lack of success in treating patients withcomplete endobronchial obstruction. Firstly,the operator may have difficulty in selectingthe correct plane of dissection through thetumour because the normal anatomical land-marks are lost. Secondly, the operator has noknowledge of the amount of tumour that mustbe removed before he can reach patent distalairways. Treatments may therefore be aban-doned prematurely in patients with salvage-able lungs. Finally, the operator does notknow whether patent distal airways existbeyond the tumour. The tumour may extendinto the periphery of the lung and beassociated with extensive damage, so thatpatients with non-viable lungs may be subjec-ted needlessly to the hazards of laser treat-ment.

In an attempt to overcome these problems,we have developed a bronchographic tech-nique to show the endobronchial extent of thetumour and patency of the distal airwaysbefore laser treatment is attempted. The tech-nique and our results are described in thispaper.

Patients and methodsPATIENTSWe studied 17 patients (10 males and sevenfemales) with inoperable bronchial malig-nancy. The average age was 66 with a range of43-78 years. All patients were severely limitedby breathlessness and their airways wereobstructed predominantly by intraluminaltumour. Obstruction was within a main bron-chus in each case; 16 patients had collapse of alung and one collapse of a lower lobe. Serialchest radiographs indicated that collapse hadbeen present for at least one month. Thehistological types of the tumours were:squamous cell carcinoma (10 patients), largecell carcinoma (5), small cell carcinoma (1),and undifferentiated carcinoma (1). Sevenpatients had not received any previous treat-

Department ofThoracic MedicineP J M GeorgeR M RuddDepartment ofRadiologyM C PearsonLondon ChestHospital, LondonDepartment ofThoracic MedicineM R HetzelDepartment ofRadiologyD EdwardsUniversity CollegeHospital, LondonAddress for reprint requests:Dr P J M George, LondonChest Hospital, London E29JXAccepted 25 April 1990

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BRONCHOGRAPHYAfter premedication with intramuscular injec-tions of papavaretum and atropine, fibreopticbronchoscopy was performed under localanaesthesia with topical lignocaine. If neces-sary, additional sedation was produced withup to 10 mg intravenous diazepam. A multi-purpose angiographic catheter (Cordis,FG 7), containing a J guide wire, was passedthrough the biopsy channel of the broncho-scope and directed through the tumour underradiographic screening. The J guide wire wasadvanced beyond the tip of the catheter toallow the catheter to pass into the distal air-ways with minimal trauma.When the catheter had been advanced 3-

4 cm beyond the proximal border of thetumour, the guide wire was removed andwater soluble radio-opaque contrast(Omnipaque) was injected through the cath-eter under screen control. The air within thecatheter, which was expelled, outlined thedistal airways, which were then opacified withcontrast. If distal airways were not seen, theguide wire was replaced and the catheteradvanced. The procedure was repeated untilbronchi were identified. The catheter wasthen slowly withdrawn while continuing toinject contrast in order to demonstrate theproximal and distal margins of the tumour inaddition to the bronchial tree beyond (fig 1).Figure 1 A collapsed left

lung (a) caused by atumour occluding the leftmain bronchus. The tip ofthe catheter has beenadvanced into the lowerlobe and radio-opaquecontrast has been injectedto reveal patent distalairways; the proximal anddistal margins of thetumour are also welldemonstrated (b). Lasertreatnment successfullyrestored an airway to thelower lobe, which then re-expanded.

ment and seven had undergone radiotherapy,two chemotherapy and radiotherapy, and onechemotherapy alone.We studied two additional patients with

squamous cell carcinomas causing obstructionof a main bronchus. Although both hadpresented with a collapsed lung, their lungshad re-expanded at the time of admission tohospital. Re-expansion occurred spontan-eously in one patient and after a course ofpalliative radiotherapy in the other. Serialchest radiographs indicated that the intervalbetween re-expansion and bronchography wasno greater than two weeks.

LASER TREATMENTTreatments were given with neodymiumYAG lasers operating at a wavelength ofeither 1-064 gm (Fiberlase 100, PilkingtonMedical Systems; University College Hos-pital) or 1-32 gm (MBB-Medizintechnic;London Chest Hospital). Treatment with thetwo lasers was essentially the same; both useda combination of rigid and flexible broncho-scopes, with general anaesthesia produced byintravenous agents.3 For treatment with the1 064 jIm laser, however, we used power set-tings of 40-70 watts in pulses of up to twoseconds, but with the 1 32 gm laser powers of10-20 watts in pulses of up to one second.

PREOPERATIVE AND POSTOPERATIVEASSESSMENTSLung re-expansion was assessed in all patientswith chest radiographs. Breathlessness wasgraded on the basis of the Medical ResearchCouncil (MRC) questionnaire.4 Measure-ments of peak expiratory flow (PEF), forcedexpiratory volume in one second (FEVI), andforced vital capacity (FVC) were obtainedwhenever possible.We also attempted to evaluate changes in

ventilation and perfusion within the treatedlung by comparing preoperative and post-operative radionuclide lung scans. Perfusionwas assessed by using technetium-99mlabelled human albumin macroaggregates, andventilation with either krypton-81m gas(University College Hospital) or 99`T labelledDTPA aerosols (London Chest Hospital).Anterior and posterior views were obtainedand the number of counts was averaged bytaking the geometric mean counts from the

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Bronchography in the assessment ofpatients with lung collapse for laser therapy

two views. Ventilation and perfusion werequantified by expressing the mean number ofcounts in the treated lung as a percentage ofthe sum of the counts in both lungs toproduce a fractional score. Full details of thismethod have been described.5 Patients whoseairways had not been recanalised were notasked to repeat these tests after the procedure.

ANALYSISMean values for breathlessness score (MRCgrade) were compared before and after treat-ment by Wilcoxon's matched pairs signedrank test. Student's paired t test was used toassess lung function (FEVy, FVC, PEF) andfractional scores of ventilation and perfusionbefore and after treatment.

Figure 2 Preoperativebronchographsfrom twopatients who were nottreated with the laser.(a) Bronchograph in apatient with tumouroccluding the left mainbronchus, showing severedilatation of the airwaysbeyond the obstruction.The "bronchiectatic"appearances were so severethat it was decided not toattempt laser treatment;more recent experience,however, has shown thatthese appearances mayresolve after lasertreatment (see fig 4).(b) Bronchograph in apatient with a collapsedright lung, showing a largecavity within the upperlobe. Previous experiencehas shown that thesepatients are prone to severeinfection and haemorrhageafter the treatment.

Ia

ResultsBRONCHOGRAPHY IN 17 PATIENTS WITH ACOLLAPSED LUNG OR LOBEBronchography was well tolerated by allpatients and there were no complications.Patent distal airways were seen in 16 of the 17patients with a collapsed lung or lobe. Thebronchi in these 16 cases were abnormallydilated, suggesting radiographic bronchiec-tasis. In one patient the appearances of severebronchiectasis led to a decision not to attemptlaser treatment (fig 2a).

In two patients cavities were seen within thecollapsed lung. Treatment was not attemptedin one of these patients (fig 2b) because thecavity was thought to carry a serious risk ofpostoperative infection and haemorrhage. Inthe other patient treatment was directed at theunaffected lobe, no attempt being made torecanalise the bronchus supplying the cavitatedlobe.

LASER TREATMENT IN 15 PATIENTSEndoscopic laser treatment was attempted in15 patients and achieved successful recanalisa-tion in 12. Treatment was successful initially inonly nine patients but it was repeated in fourwhose bronchograms had shown patent distalairways. Repeat treatments resulted in success-ful recanalisation in three of these patients.

Preoperative bronchography suggested veryextensive tumour in two of the three patientswhose treatment was unsuccessful. In one casepatent distal airways could not be seen, and inthe other case tumour was shown to extendfrom the orifice of the left main bronchus to thesegmental divisions of the lower lobe. In thethird patient, although bronchography showedlimited endobronchial obstruction, treatmenthad to be abandoned prematurely as a result oflife threatening haemorrhage.

ASSESSMENTS IN PATIENTS WITH RECANALISEDAIRWAYSIn patients with a collapsed lung postoperativechest radiographs showed complete re-expan-sion in six and partial re-expansion in five. Re-expansion was also obtained in the patient witha collapsed lobe. In each case breathlessnesswas reduced to such an extent that the MRCgrade in the 12 patients improved from a meanvalue of 4-4 to 2-8 (p = 0-002).

Respiratory function was assessed before andafter treatment in eight patients (table). Therewas a significant increase in mean values ofFEV1 and FVC (p = 0-05 and 0 005) but nochange in PEF. The most strikingimprovements were observed in patients with

Mean (SD) peak expiratory flow (PEF),forcedexpiratory volume in one second (FEV,), andforcedvital capacity (FVC) before and after laser treatment ineight patients in whom a lung or lobe was re-expanded

Before After

PEF (1/min) 191 (48) 188 (78)FEV, (1) 1-26 (0 42) 1-49 (0-55)*FVC (1) 1 91 (0 79) 2-42 (095)**

*p = 0-05; **p = 0-005 (paired Student's t test).10)

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Figure 3 Fractionalscores of (a) ventilationand (b) perfusion beforeand after treatment ineight patients whose lungsor lobes were re-expandedwith the laser. Mean scoresare shown by solid squares.Seven patients weretreatedfor completecollapse of a lung and theirpretreatment scores ofventilation representbackground counts.

Ventilationscore50 1r-

40,

30

20

10

0

(a)

Perfusionscore

sO -r._v

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Belotre After

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Before After

complete lung re-expansion; there was a widevariation, however, in the magnitude ofchange, the increase in FVC ranging from 7%to 690o.The results obtained with radionuclide lung

scans are summarised in figure 3. The mean

fractional score of ventilation rose from 5 4 to26 4, and the mean fractional score ofperfusionfrom 8 9 to 20 1 (p = 0003 for both).Although the most striking improvementswere seen in patients with complete lung re-

expansion, there was again a wide variation inthe magnitude of change.

ASSESSMENT OF THE REVERSIBILITY OFBRONCHIAL DILATATIONRepeat bronchography and computerisedtomography Bronchography was repeated inthree patients within two weeks of lung re-

expansion. In all cases the calibre ofthe airwayshad returned to almost normal (fig 4). In a

fourth patient the re-expanded lung was asses-sed by computed tomography. This showedonly slight thickening of the bronchial wall anddilatation of the airways, indicating consider-able improvement by comparison with thepreoperative bronchogram.Bronchography after recent expansion Bron-chography was performed in two additionalpatients with endobronchial tumours, whoselungs had recently re-expanded after a periodof collapse-one spontaneously and one afterradiotherapy. In both cases bronchographydelineated the endobronchial extent of thetumour but showed that the distal alrways wereof normal calibre.

DiscussionIn an attempt to evaluate patients with acollapsed lung, we initially performed com-puted tomography but found that the scanscould not define bronchial anatomy within thearea of the collapse. Our experience withpreoperative bronchography has been moreencouraging, however, as it has provided re-liable information on the extent of tumour andpatency of the distal airways. It has alsoenabled us to avoid the potential hazards ofinfection and haemorrhage, which we havepreviously encountered after recanalisingcavitated lung. The technique has been easy toperform and well tolerated, and appears to besafe.

In addition to its value as a preoperativescreening procedure, bronchography mayimprove the chances of achieving successful re-expansion. Without the knowledge that patentdistal airways existed beyond the tumour,treatment might have been abandonedprematurely and would not have been repeatedin three patients in this series whose lungssubsequently re-expanded. The patients withcomplete endobronchial obstruction who wereselected for bronchography had longstandingcollapse and thus represented the most challen-ging group of patients to be treated. Successfulrecanalisation in 12 of the 15 patients comparesfavourably with previously published figures of5 of 17,' 11 of 23,2and 7 of 11.6Although radiological re-expansion provides

a convenient end point, it represents a poorindex of functional improvement. In thepresent study spirometry and radionuclidelung scanning revealed a wide range ofimprovement, which could not have beenpredicted from the plain chest radiograph.Differences in postoperative airway calibre andthe inconsistent effects on the lung ofextrabronchial tumour and previous radio-therapy may have contributed to thisvariability. Nevertheless, successful recanalisa-tion resulted in a significant functionalimprovement and a valuable reduction inbreathlessness.

Laser recanalisation in patients with acollapsed lung may be further helped by thetechnique of intraoperative bronchography,developed by Joyner et al.7 Their techniqueuses a transbronchial biopsy needle to perforatethe obstructing tumour and then inject radio-opaque contrast distally. The angle of theneedle is adjusted until contrast flows freelyinto the distal airway, thereby providing infor-mation that guides the operator's plane ofdissection through the tumour. The best poss-ible results therefore may be obtained whenintraoperative bronchography is used to guidetreatment in patients selected by preoperativebronchography.

In the present study preoperative bron-chography consistently showed abnormalbronchial dilatation within the collapsed lungand suggested the presence of radiographicbronchiectasis. These findings were of concernas it was feared that re-expansion of a lung orlobe with the laser might add to the patient'sdistress by causing chronic productive cough.

p = 0003

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Bronchography in the assessment of patients with lung collapse for laser therapy 507

Figure 4 Example ofreversible bronchialdilatation. Collapsed rightlung (a), caused by atumour occluding the rightmain bronchus.Preoperative broncho-graphy (b) showed tumourextending from the orifice Aof the right main bronchusto the intermediatebronchus. The middle andlower lobe bronchi werepatent but dilated. Theupper lobe bronchus couldnot be identified.Endoscopic laser resectionsuccessfully recanalised anairway to the intermediatebronchus but not to theupper lobe, and resulted inre-expansion of the middleand lower lobes (c).Bronchography two weekslater showed that thecalibre of the right middleand lower lobe bronchi hadimproved substantially (dand e). LI

Furthermore, our previous experience hasshown that patients whose lungs or lobes are

successfully expanded are particularly at risk ofdeveloping pneumonia after the procedure,I j ~~~~~~~~~~~occasionally with fatal outcome.'Joyner et al do not say whether any of their

patients had bronchial dilatation.7 Neverthe-less, the finding of bronchial dilatation is wellknown in atelectatic lungs obstructed byendobronchial tumours8 and inhaled foreignbodies.9 In the present study the finding ofnormal bronchial calibre in two patients whoselungs had re-expanded after a period ofcollapse and of reversible bronchial dilatation(fig 4) in four patients suggests that the dilata-tion is not necessarily permanent and may be

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reversed when the lung or lobe re-expands.The decision not to treat the patient with severebronchial dilatation (fig 2a) was taken beforewe had observed this reversibility and wouldnot have been made in the light of our more

recent experience.Reversible bronchial dilatation has been

observed in patients with atelectasis associatedwith viscid secretions and severe infection.""'6In these cases repeat bronchography showedthat the airways had returned to a normalcalibre when the infection and secretions hadbeen treated satisfactorily and the lung had re-expanded. Whether these cases and thosepresented in this paper should be regarded as

genuine cases of bronchiectasis is debatable.The term bronchiectasis literally means dilata-tion of the bronchi; it has been argued,however, that the dilatation should be perman-ent before such a term is used." '7 It has beensuggested that bronchial dilatation occurs inpatients with atelectatic lungs as a result ofdistension caused by an accumulation of viscidsecretions8 and that collapse may lead to fore-shortening of the airways and so furtherenhance the appearances of bronchiectasis.7Prompt relief of the obstruction with drainageof secretions and re-expansion of the lungshould therefore restore a normal airway. Ifinfection supervenes, however, it is suggestedthat the bronchial wall is weakened and theadjacent lung becomes fibrosed.8 The combin-ation of mural weakening and traction by thesurrounding fibrosis is thought to produce thecharacteristic changes of irreversible bronchi-ectasis.

If these suggestions are correct, it is clearlyimportant to use the laser to attempt lung re-

expansion as promptly as possible before infec-tion and fibrosis have become established. Theduration of complete endobronchial obstruc-tion and of collapse could not be documentedprecisely in our patients but were probably inthe region of one to two months. In Linton'sseries of 16 patients irreversible bronchiectasiswas observed in four patients seven months tosix years after inhalation of a foreign body.9The finding of bronchial dilatation in

patients with a collapsed lung does nottherefore necessarily imply a diagnosis of

irreversible bronchiectasis and should not beregarded as a contraindication to attemptinglaser treatment. We believe that broncho-graphy is a valuable preoperative screeningprocedure as it identifies patients with patentdistal airways in whom treatment is likely tolead to a worthwhile symptomatic and func-tional improvement. It also enables theunnecessary risks of treatment under generalanaesthesia to be avoided in patients with non-viable lungs. The technique may also have awider value in assessing patients before otherpalliative treatments, such as radiotherapy, areattempted.

This work was generously supported by the North East ThamesRegional Health Authority, Pilkington Medical Systems, andMBB-Medizintechnic. We would like to thank the endoscopystaff and radiographers in our two hospitals for their technicalassistance. We are also grateful to Mr J R Belcher for his helpfuladvice and comments on this work.

I Hetzel MR, Nixon C, Edmonstone WM, et al. Laser therapyin 100 tracheobronchial tumours. Thorax 1985;40:341-5.

2 Gelb AF, Epstein JD. Neodymium-yttrium-garnet laser inlung cancer. Ann Thorac Suirg 1987;43:164-7.

3 George PJM, Garrett CPO, Nixon C, et al. Laser treatmentfor tracheobronchial tumours: local or general anaes-thesia? Thorax 1987;42:656-60.

4 Medical Research Council. Questionnaire on respiratorsynmptoms. London: Medical Research Council, 1966.

5 George PJM, Clarke G, 'l'olfree S, Garrett CPO, HetzelMR. Changes in regional ventilation and perfusion of thelung after endoscopic laser treatment. Thorax 1990;45:248-53.

6 Haubinger K, Held E, Huber R. Endobronchial lasertherapy-differential therapeutic use and clinical value.Klin Wochenschr 1984;62:74-80.

7 Joyner LR, Maran AG, Sarama R, Yakaboski A.Neodymium-YAG laser treatment of intrabronchiallesions: a new mapping technique via the flexible fibre-optic bronchoscope. Chest 1985;87:418-27.

8 Spencer H. Pathology of the lunlg. 4th ed. Vol 1. Oxford:Pergamon Press, 1985:131-65.

9 Linton JSA. Long-standing intrabronchial foreign bodies.Thorax 1957;12:164-70.

10 Findlay L. Atelectatic or compensatory bronchiectasis. ArchDis Child 1935;10:61-84.

11 Jennings GH. Re-expansion of the atelectatic lower lobe anddisappearance of bronchiectasis. Br Med J 1937;ii:963-5.

12 Lander FPL, Davidson M. The aetiology of bronchiectasis(with special reference to atelectasis). Br J Radiol1938;122:65-89.

13 Fleischner FG. Reversible bronchiectasis. AJR 194146:166-72.

14 Ogilvie AG. The natural historv of bronchiectasis: a clinicalroentgenologic and pathologic studv. Arch Intern Med1941 ;68:395-465.

15 Blades B, Dugan DJ. Pseudobronchiectasis. J Thorac Surg1944;13:40-8.

16 Lander FPL. Bronchiectasis and atelectasis: temporary andpermanent changes. Thorax 1946;1:198-210.

17 Hinshaw HC, Schmidt HW. Some clinical problems inbronchiectasis. Dis Chest 1944;10:1 15-22.

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