lung scanning in carcinoma bronchus

Thorax (1971), 26, 23.

Lung scanning in carcinoma of the bronchusR. H. SECKER WALKER, J. L. PROVAN1, J. A. JACKSON,

and J. GOODWIN

The Medical Unit, University College Hospital Medical School, University Street, London W.C.I

The lung scans of 101 patients with carcinoma of the bronchus have been compared with thebronchoscopic and radiographic findings. As the tumour approaches the hilum as judged bybronchoscopy or the chest radiograph the relative perfusion of the affected lung decreases. Whenthe relative perfusion of the affected lung is less than one third of the total the tumour is likelyto be inoperable. The reduction in perfusion is related to involvement of the vessels in the hilumby tumour and to a lesser extent to bronchial obstruction.

Defects in perfusion in the unaffected lung were seen in 53 patients and were usually due tochronic bronchitis and emphysema or inactive pulmonary tuberculosis.

In the management of patients with carcinoma of the bronchus lung scans are of value inpredicting when a tumour is likely to be inoperable and also in giving an indication as to whethera pneumonectomy or lobectomy will be possible. In addition, defects in the contralateral lungmay be sufficiently large to contraindicate surgery.

Lung scanning is a safe and effective way ofdemonstrating the relative pulmonary arterialblood flow to each lung (Sabiston and Wagner,1964; Tauxe, Burchell, and Black, 1967) and hasbeen used in this way to assess lung function inpatients with carcinoma of the bronchus (Hatch,Maxfield, and Ochsner, 1965; Garnett, Goddard,Fraser, and Macleod, 1968). Defects in perfusionvary in size from those corresponding to the lesionvisible on the chest radiograph to absent perfu-sion of an entire lung, while minor abnormalitiesare commonly seen in the opposite lung.

This paper compares the lung scan findings withthe bronchoscopic and radiographic appearancesin patients with carcinoma of the bronchus seenbetween 1967 and 1969, and discusses the practicalvalue of this technique.

PATIENTS AND METHODS

The patients studied all had untreated carcinoma ofthe bronchus at the time of their lung scan.The diagnosis of carcinoma of the bronchus was

established by sputum cytology, biopsy at broncho-scopy or thoracotomy or from the histology of theresected tumour or at necropsy.Each patient was given 1 5-20 mCi of technetium

9m labelled macroaggregated human serum albuminintravenously and the lung scans were made with aPicker Magnascanner m. Anterior and posteriorcolour scans and photoscans were produced.'Present address: Department of Surgery, The Welksley Hospital,160 Wellesley Street East, Toronto 5, Ontario, Canada

The relative pulmonary arterial blood flow (relativeperfusion) of each lung has been determined fromthe colour dot scans by expressing the counts ofradioactivity in the affected lung as a percentage ofthe total counts in the scan. This method correlateswell with differential bronchospirometry as a measureof relative pulmonary blood flow (Chemick, Lopez-Majano, Wagner and Dutton, 1965; Rogers, Kuhl,Hyde, and Mayock, 1967; Gamett, Goddard,Machell, and Macleod, 1969).

In addition a semiquantitative method, also basedon the colour dot scans, has been used to assess thesize of the defects in perfusion in the unaffected lung.The recognition of such defects and the assessmentof their size depend on a subjective comparison withthe normal pattern of perfusion so that a trulyquantitative method is not possible at present. Asimple and rapid scoring method has been used inwhich each lung is divided into three zones on theanterior and posterior scans, and then each zone isscored from 0 to 4 (absent perfusion scoring 0, anda normal pattern 4) depending on the size of thedefect and the level of activity present. A normallung would score 24 (100%) and the defects havebeen expressed as a percentage of this. When thesame observer scored the scans on a second occasionthe maximum error was 7%. By expressing the scorefor each lung as a percentage of the total score an-other estimate of relative perfusion can be made.There is an excellent correlation between this methodof estimating relative perfusion and that derived fromthe counts of radio-activity in each lung (r=0-986,P<0001) (Secker Walker, Jackson, and Goodwin,1970).

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R. H. Secker Walker, J. L. Provan, J. A. Jackson, and J. Goodwin

RESULTS

Lung scans have been carried out on 101 patientswith carcinoma of the bronchus. Fifty-two patients(44 men and 8 women) were considered on eitherbronchoscopic grounds (11) or because of poorrespiratory function (FEV1<15 litres) (16) orother diseases (5) or because of the presence ofextrathoracic metastases (16) or superior venacaval obstruction (4) to be unsuitable for surgery.Forty-nine patients (35 men and 14 women) wereconsidered on clinical and bronchoscopic groundsto have operable tumours, but three refused sur-gery so that 46 underwent thoracotomy. Theaverage age of these 46 patients was 55 2, range41-68 years, and the average age of the remaining55 patients was 617, range 44-77 years.There were 21 squamous carcinomas, 16 oat-

cell or anaplastic carcinomas, and 9 adeno-carcinomas in the patients undergoing surgery,and 27 squamous carcinomas, 13 oat-cell or ana-plastic carcinomas, 5 adenocarcinomas, and 10carcinomas of undetermined cell type in the otherpatients.The relative perfusion of the affected lung,

determined from the lung scans, has been com-

pared with both the bronchoscopic and chestradiograph findings (Tables I and II). Thirty-fourpatients had normal bronchoscopies. The mean

TABLE I

Bronchoscopyl No. of Mean Relative Perfusion ofBronchoscopy' Patients Affected Lung (%± S.E.M.)Normal 34 42-8 ±26Tumour visible in, or nar- t =2.97: p <0005

rowing of, lobar bronchus 33 32-4±23)Tumour visible in, or nar-

rowing of, main bronchus 12 16-6±338 t= 353; P<0'001

'Two patients with a widened main carina, two patients with astiff main bronchus, and 18 patients who did not have a bronchoscopyare not included in this table.

TABLE II

Chest Radiograph No. of Mean Relative Perfusion ofChest Radiograph Patients Affected Lung (%,±S.E.M.)Localized mass' 31 45-5±2i21Localized mass or small

area ofconsolidation andabnormal hilum 23 30 813 3 t=3 89; P<0001

Larger area of collapse orconsolidation involvinghilum 22 25-4±3-7 t=4 97; P<0*001

Hilar mass alone 16 29 714-1 t=3-75; P<s0001

Five patients with normal chest radiographs and four with otherfindings described in the text are not included.

'For Student's t test the patients with a localized mass have beenicompared with each of the other groups.

Legend to Fig. I a on page 26.

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FIG. 1. Mr. J. E. aged 59. Squamous-cell carcinoma. Characteristic squamous carcinoma cells were found inthe splutum in September 1967. Bronchoscopy and chest radiography (a), including tomography of the hilar regions,were normal. The lung scans (b, anterior, c, posterior) show a defect in perfusion in the right upper lobe. Minordefects are present elsewhere. These findings were unchanged nine months later.

After a pneumonic illness in February 1970 he was found to have some patchy consolidation in the right uppellobe (d). At bronchoscopy the tumour was visible in the right upper lobe bronchus. Lung scans (e, anterior,f, posterior) on the gamma camera (these are composite pictures) show a larger defect in the right upper lobe,but elsewhere the appearance is as before. He underwent a right upper lobectomy.

relative perfusion in these patients was 428% +2-6 (S.E.M.). In 33 patients in whom the tumourwas visible in a lobar bronchus, or there wasnarrowing of a lobar bronchus, the mean rela-tive perfusion was 32-4% ±2-3. In 12 patients inwhom the tumour was visible in the mainbronchus or there was narrowing of the mainbronchus, the mean relative perfusion was16 6% ±3 8 (one of these, in spite of the broncho-scopic appearance, was considered operable). Thedifferences between these three groups are statistic-ally significant. The main carina was widenedin two patients and the main bronchus was stiffin two patients, but bronchoscopy was not under-taken in the remainder.

In 31 patients the chest radiograph showed alocalized mass and the hilum was normal. Themean relative nerfusion of the affected lung inthese patients was 45-5 % +±22. In 23 patientsthere was a localized mass or small area of con-solidation and the hilum was also abnormal: theirmean relative perfusion was 30-8 %/O ± 3 3. In 22

patients there was a larger area of either collapseor consolidation, spreading from the hilum, andtheir mean relative perfusion was 25 4c,, + 3 7. In16 patients there was a hilar mass without paren-chymal shadowing and they had a mean relativeperfusion of 29-7% +4 1. In five patients thetumour was not visible on the chest radiographbut the lung scan was abnormal in each of them.In one of these, with a normal bronchoscopy andmalignant cells in the sputum, the tumour ap-peared two and a half years later at the site ofthe abnormality and has been successfully resec-ted (see Fig. 1). Two patients had a widenedmediastinum, one bilateral pleural effusions andone bilateral peripheral shadows.The mean relative perfusion of the affected lung

in the patients with normal chest radiographs andthose with a localized mass only are significantlygreater than the mean relative perfusion of eachof the other groups.

Figures 2 to 4 show examples of the lung scanfindings.

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oIG. 2. Mrs. D. H. aged 59. Squamous-cell carcinoma. Bronchoscopy was normal. The lung scan shows a defectcorresponding to the mass on the chest radiograph and several other defects in perfusion in each lung. The relativeperfiusion of the right lung was 46% and she underwent a right upper lobectomy. (b) Anterior scan; (c) posterior scan.

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FIG. 3. Mr. J. L aged 59. Squamous-cell carcinoma. At bronchoscopy the tumour was seen in the right lower lobebronchus which was narrowed. The lung scan shows reduced perfusion of the right lung, especially in the lowertwo-thirds. The relative perfusion of the right lung was 34% and he underwent a right pneumonectomy. (b)Anterior scan; (c) posterior scan.

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FIG. 4. Mr. J. G. aged 51. Oat-cell carcinoma. Bronchoscopy was normal. The lung scan shows very little per-fusion of the right lung, the relative perfusion of this side being 8 %. He was treated with cyclophosphamide anddied one month laterfrom cerebral metastases. (b) Anterior scan; (c) posterior scan.

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Defects in the pattern of perfusion in the un-affected lung were seen in 53 patients (Table III),and such defects may give rise to misleadinglyhigh values for the relative perfusion of the affec-ted lung. The majority of such defects were rela-tively small, scoring less than 25% by the semi-quantitative method, in 36 patients. In the remain-ing 17 patients the defects were larger. Seven ofthese patients had clinical evidence of chronic

TABLE IIIDEFECTS IN PATTERN OF PERFUSION IN UNAFFECTEDLUNG AS DETERMINED BY THE SEMIQUANTITATIVE

METHOD

Findings inUnaffected Lung

Normal Minor MajorPattern Defects Defects

Score <l0°/, 10-25% 25%

Patients undergoing thoracotomy 23 19 4Patients not undergoing thora-cotomy 25 17 13

Total

46

55

lung disease to account for the defects (chronicbronchitis and emphysema, bronchial asthma, in-active pulmonary tuberculosis) and eight had evi-dence of metastatic spread either to the oppositelung (4) or outside the chest (4). The defects inperfusion in one patient were related to left ven-

tricular failure associated with hypertension andischaemic heart disease, and were not explainedin one other patient.The 16 patients with extrathoracic metastases

had a mean relative perfusion of 28-5 % ± 46,while the mean relative perfusion in the patientswith poor respiratory function (16), ischaemicheart disease (4), and uraemia (1) was 41 -1,%3-4.The majority of the patients who underwent

thoracotomy have been considered in more detailelsewhere (Secker Walker and Provan, 1969), butthe essential findings, with the addition of threemore patients, were as follows.

Forty-six patients had clinically and broncho-scopically operable tumours and underwent thora-cotomy, but 16 (350%0() were found to have un-resectable tumours, 15 (32-5%) underwent pneu-monectomy, and 15 (32 5%) underwent lobectomyor segmental resection. As might be expected, thepatients who had lobectomies or segmental resec-

tions had more normal bronchoscopies, less hilarinvolvement on the chest radiograph, and fewerabnormalities on their lung scans than the othertwo groups in whom the findings were similar.No abnormality was seen in the lung scans of two

patients with small peripheral tumours. Inthe remaining patients the defects ranged insize from those corresponding to the size of thetumour on the chest radiograph to absent perfu-sion of the entire lung. Irregularities in the patternof perfusion in the unaffected lung were seen in21 of these patients (46%), and were larger than25% in the two patients who underwent segmen-tal resection, and in two who were unresectable.The mean relative perfusion of the affected lung

in the inoperable group was 28 8% ± 3-8 (S.E.M.),in the pneumonectomy group 37 7% + 23, and inthe lobectomy group 50(2 % ± 1-5. The differencebetween the inoperable and pneumonectomygroups just fails to reach significance at the 5%level, but both are significantly different from thelobectomy group, P<0001. With one exceptionall the patients with a relative perfusion of theaffected lung of less than one third of the totalhad unresectable tumours. The exception under-went pneumonectomy. His left pulmonary arterywas completely surrounded and compressed bytumour sufficiently far from its origin to enablethis operation to be carried out. Six of the patientsin the inoperable group had relative perfusions ofmore than 34%. In two, perfusion of the oppositelung was reduced, due to spread of the tumouracross the mediastinum in one, and possibly alsoin the other, so that the relative perfusion of theaffected lung was little reduced. In the other fourthe tumour was inoperable because the thoracicspine or pericardium and atria were involved bygrowth with only minimal involvement of thehilum.When the relative perfusion lay between 34 and

40% a pneumonectomy was usually possible, only2 of 12 patients in this group being unresectable.Above 40 % a lobectomy or segmental resectionwas usually possible (15 patients), four patients inthis group being inoperable and four requiring apneumonectomy. The relative perfusion of theaffected lung in the two patients undergoing seg-mental resection was 59 and 60%, making moreradical surgery unwise.

At thoracotomy the defects in perfusion wereseen to be related to distortion or compression orinvasion of the pulmonary vessels at the hilum bytumour tissue or secondary deposits in the hilarglands. As would be expected, there was scarcelyany involvement of the hilar structures in thepatients undergoing lobectomy or segmental resec-tion. Most involvement was seen in the patientswith inoperable tumours, and rather less in thepatients who underwent pneumonectomy. Bron-chial obstruction played a smaller part as perfu-

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sion of the affected lobe was moderately or greatlyreduced in 11 of 14 patients with a narrow orobstructed bronchus, but in 10 of these there wasalso a reduction in perfusion of the abjacent un-obstructed lobe. Six other patients with normalbronchoscopies had large defects in perfusionindicating that bronchial obstruction is not themajor cause of the reduced perfusion.

DISCUSSION

In patients with carcinoma of the bronchus, lungscanning provides an indirect assessment of theextent of involvement of the hilar regions bytumour tissue. As the tumour approaches thehilum, the relative perfusion of the affected lungdecreases. The size of the defect in perfusion ismore closely related to the amount of distortion orcompression or invasion of the pulmonary vesselsthan to bronchial obstruction. Bronchial car-cinomas derive most of their blood supply fromthe bronchial circulation, so that peripheraltumours show up as defects in the pattern of per-fusion corresponding to their size on the chestradiograph. Small peripheral tumours, that istumours less than 2-3 cm in diameter on the chestradiograph, are unlikely to be detected by scan-ning, for the resolution of the scanning systemdoes not enable defects of this size to be distin-quished from the surrounding radioactivity. How-ever, a centrally placed tumour of similar size andeven tumours invisible on the chest radiograph oron bronchoscopy may produce readily visible andsometimes unexpectedly large defects in perfu-sion because of involvement of the hilar vessels.Our figures indicate that the relative perfusion

of the affected lung tends to diminish as thetumour approaches the main bronchus, as judgedby both bronchoscopy and the chest radiograph.In addition, the presence of extrathoracic metas-tases is associated with a considerable reductionin the relative perfusion of the affected lung.Lung scanning can be of considerable value in

the management of patients with carcinoma of thebronchus for it gives information about the rela-tive perfusion of each lung and the regional perfu-sion within each lung that is not obtainable fromeither radiography, routine spirometry, or bloodgas analysis. The more complicated technique ofdifferential bronchospirometry also gives informa-tion about the relative perfusion of each lung, andthe good correlation that exists between these twomethods (Chernick et al., 1965; Rogers et al.,1967) has led Garnett and his colleagues toabandon differential bronchospirometry in favourof lung scanning (Garnett et al., 1969).

The relative perfusion of the tumour-bearinglung in all the patients with bronchoscopically in-operable tumours was less than one third of thetotal, and it was also below this figure in 10 of the16 patients whose tumours were found to be un-resectable at thoracotomy. The only indication ofextensive hilar involvement by the tumour in thesepatients was the unexpected reduction in perfu-sion of the affected lung, for on clinical, broncho-scopic, and radiological grounds they were con-sidered operable.

In only one patient out of 22 with a relativeperfusion of less than 33-3% was it possible toremove the tumour (11 were bronchoscopicallyinoperable and 10 unresectable at thoracotomy)so that the chances of being able to resect atumour in these circumstances are less than 5%.About one-third of patients undergoing thora-

cotomy are found to have unresectable tumours(Belcher and Anderson, 1965 ; Price Thomas, 1960)because of either extensive spread of the diseaseor invasion of vital structures which had not beenappreciated preoperatively. Thirty-five per cent ofour patients were found to have unresectabletumours, but this figure could have been reducedto 16 5% if thoracotomy had not been under-taken when the relative perfusion was less than33*3 %. If pneumonectomy is contemplated thefunction of the remaining lung is clearly of vitalimportance. Abnormalities in perfusion of the un-affected lung are common and occurred in morethan half of these patients. The majority of thesedefects (68 %) were relatively small but in 17patients (32%) they were larger. Sometimes suchdefects are large enough to contraindicate surgery(Garnett et al., 1968) or limit this to segmentalresection when the tumour-bearing lung has thegreater blood flow. In four of the patients whounderwent thoracotomy, the defect in the patternof perfusion in the unaffected lung was scored aslarger than 25%, but neither the chest radiographnor spirometry gave any indication that such largedefects would be found.When lung scans are combined with the clinical

picture, chest radiographs, bronchoscopy findings,and spirometry tests, the selection of patients forthoracotomy can be improved for, in addition topredicting when a tumour is likely to be inoper-able and giving some indication as to whether a

pneumonectomy or a lobectomy is the more prob-able, they may show unsuspected defects in thecontralateral lung.Lung scans, using radioactive particles, show the

distribution of pulmonary arterial blood flow andbecause so many cardiorespiratory conditions dis-

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turb this flow a lung scan by itself is of little diag-nostic value. Large and persistent defects in per-fusion, in association with either peripheral orhilar shadows on the chest radiograph, make thediagnosis of malignant disease likely, but they donot establish it. Sometimes a lung scan will indi-cate the likely site of a carcinoma in that smallgroup of patients (5% of this series) with malig-nant cells in the sputum and normal chest radio-graphs and bronchoscopies. A single persistentdefect in these circumstances should lead to fur-ther measures, such as angiography of the greatveins and pulmonary arteries, in the hope of estab-lishing the site more precisely.

We are grateful to Miss D. Nightingale, ProfessorR. S. Pilcher, Dr. H. Nicholson, Dr. P. J. D. Heaf,and Dr. P. D. B. Davies for allowing us to studypatients under their care.The photographs were kindly prepared by the Uni-

versity College Hospital Medical School PhotographicDepartment.

This work was supported by a generous grant fortechnical assistance from the British Empire CancerCampaign.

REFERENCES

Belcher, J. R., and Anderson, R. (1965). Surgical treatmenof carcinoma of the bronchus. Brit. med. J., 1, 948.

Chernick, V., Lopez-Majano, V., Wagner, H. N., Jr., andDutton, R. E. Jr. (1965). Estimation of differentialpulmonary blood flow by bronchospirometry and radio-isotope scanning during rest and exercise. Amer.Rev. resp. Dis., 92, 958.

Garnett, E. S., Goddard, B. A., Fraser, H. S., and Macleod,W. M. (1968). Lung perfusion patterns in carcinomaof bronchus. Brit. med. J., 2, 209.

Machell, E. S., and Macleod, W. M. (1969).Quantitated scintillation scanning for the measurementof lung perfusion. Thorax, 24, 372.

Hatch, H. B., Maxfield, W. S., and Ochsner, J. L. (1965).Radioisotope lung scanning in bronchogenic carcinoma.J. thorac. cardiovasc. Surg., 50, 634.

Price Thomas, C. (1960). Lobectomy with sleeve resection.Thorax, 15, 9.

Rogers, R. M., Kuhl, D. E., Hyde, R. W., and Mayock, R. L.(1967). Measurement of the vital capacity and perfusionof each lung by fluoroscopy and macroaggregated albu-min lung scanning. Ann. intern. Med., 67, 947.

Sabiston, D. C. Jr., and Wagner, H. N. Jr. (1964). Thediagnosis of pulmonary embolism by radioisotopescanning. Ann. Surg., 160, 575.

Secker Walker, R. H., Jackson, J. A., and Goodwin, J.(1970). Resolution of pulmonary embolism. Brit. med. J,,4, 135.and Provan, J. L. (1969). Scintillation scanning oflungs in preoperative assessment of carcinoma ofbronchus. Brit. med. J., 3, 327.

Tauxe, W. N., Burchell, H. B., and Black, L. F. (1967).Clinical applications of lung scanning. Mayo Clin.Proc., 42, 473.

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