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Transbronchial aspiration of subcarinal lymph nodes
Br. J. Dis. Chest (1988) 82, 149
TRANSBRONCHIAL SUBCARINAL A. D. BLAINEY*, *Department
ASPIRATION OF LYMPH NODES
M. CURLING? AND MALCOLM
of Respiratory
Medicine and t Department St Bartholomews Hospital, London
GREEN* of Cytology,
Summary
Transbronchial needle aspiration of subcarinal lymph nodes has been undertaken in 60 consecutive patients with pulmonary malignancies undergoing routine fibreoptic bronchoscopy. Four aspirates from the subcarinal nodes contained malignant cells; three squamous cell carcinoma and one adenocarcinoma. Four of 40 (10%) of patients with nonsmall-cell carcinoma of the lung had a positive aspirate. We have not confirmed the high positive rate previously reported, but nevertheless transbronchial needle aspiration provided useful staging information in some patients. The technique is rapid, safe and simple, and can easily be applied in a routine bronchoscopy service for all patients with suspected cancer, or selected patients under active consideration for surgery. INTRODUCTION It is generally agreed that surgery offers the best hope of cure for non-small-cell carcinoma of the lung, but only a small proportion of these tumours are resectable. It is often difficult to decide whether operation is appropriate for a particular patient. Many factors, including age, pulmonary function, and the stage of the disease, contribute to this decision. Staging includes the assessment of mediastinal lymph node involvement by tumour (1). Many surgeons recommend invasive investigation such as mediastinoscopy to assess this, but some lymph node groups-particularly those in the subcarinal area-are inaccessible to mediastinoscopy. Even with mediastinoscopy, a substantial proportion of patients end up with a higher stage of disease (more extensive local involvement) when assessed at thoracotomy (2). Recently American authors have suggested that needle aspiration at fibreoptic bronchoscopy may help to identify involvement of lymph nodes. This technique was originally developed for use with the rigid bronchoscope (3), but has recently been extended to the fibreoptic bronchoscope using a flexible needle by Wang and Terry (4). They reported that as many as 60% of patients undergoing fibreoptic bronchoscopy for carcinoma of the lung had lymph nodes involved by malignant tumour. A more recent study from the USA evaluating this technique in clinical practice found that 37% of Correspondence to: Dr Malcolm Green, Department of Respiratory Medicine, Brompton Hospital, London SW3 6HP.
150
BR.
.I. DIS.
CHEST:
VOL.
82 NO.
2
patients with carcinoma of the lung had a positive lymph node aspirate (5). If these figures reflected routine clinical practice in the UK, then this technique clearly deserves to be more widely applied. Alternatively it might be that these patients represented a selected group and therefore the technique is not of value in routine practice. We therefore set out to study this technique in the clinical setting of a routine bronchoscopy service for patients attending a chest clinic with possible carcinoma of the lung. Methods and Subjects Subjects We have studied all patients undergoing fibreoptic bronchoscopy over a 9-month period in whom a diagnosis of pulmonary malignancy was confirmed. This totalled 60 patients; 39 were male and 21 female. Ages ranged from 27 to 79 years. All of these patients were undergoing routine fibreoptic bronchoscopy for the diagnosis of bronchial carcinoma, or the assessmentof operability. All patients gave informed written consent for the bronchoscopy which was undertaken as part of necessary clinical investigation. Methods Fibreoptic bronchoscopy was carried out under local anaesthesia with 4% lignocaine; either an opiate premeditation or intravenous diazepam was used to sedate the patient. After the transnasal passageof the bronchoscope and a preliminary inspection of the bronchial tree, the instrument was positioned just above the carina. The needle used for transbronchial aspiration was the Microvasive 10 mm sclerotherapy needle (Microvasive Corp, USA; supplied by Keymed, Southend; Fig. 1). This is passed through the bronchoscope completely enclosed in its outer sheath. It is then positioned just below and to the right of the carina in the posterior wall of the bronchus, and the needle is pushed out through the bronchoscope and into the subcarinal tissue. Penetration of the needle can be confirmed by visual inspection. A steady aspiration pressure is then applied with a syringe at the proximal end of the needle for at least 1 minute, while the needle is moved gently up and down and rotated within the subcarinal tissue. The material aspirated into the needle is then expelled on to a cytology slide. The aspirate is spread and fixed immediately in 50% ether/50% ethyl alcohol. Slides were stained with a Papanicolou stain using haematoxylin orange G and eosin 50, then mounted ready for screening. Bronchial brushings, washings and biopsies were taken after transbronchial needle aspiration. These were processed by the departments of cytology and histology in routine fashion. The aspirate was regarded as positive where malignant cellsof identical appearance to those seen in sputum, wash or brushings were identified scattered widely throughout the aspirate. A single clump of malignant cells was not regarded as a positive aspirate, since this appearance may result from contamination with malignant cells within the bronchial tree (6).
lctbl
II
21
Fig. 1. Photograph of aspiration needle projecting from its outer sheath which in turn is protruding from the tip of the bronchoscope
BLAINEY,
CURLING,
GREEN:
TRANSBRONCHIAL
ASPIRATION
151
RESULTS The results of subcarinal lymph node aspiration in 60 patients with malignant pulmonary disease are shown in Table I. Thirty-two patients had squamous cell carcinoma, and the aspirate contained malignant cells in three of these. In one out of eight patients with adenocarcinoma the aspirate was positive. Malignant cells were scattered widely throughout the slide in all positive aspirates. Aspiration was negative in 12 patients with oat cell carcinoma and eight patients with other pulmonary malignancies, which were mostly lymphomas. Overall, 4/40 (10%) of patients with non-small-cell carcinoma of the lung had positive aspirates. Further details of the patients with positive aspirates are shown in Table II. In the three patients with squamous cell carcinoma, the tumour was right sided-in the RUL in two and the RLL in the other. The tumour was also right sided in the patient with adenocarcinema who had a positive aspirate. In two of these patients the carina appeared normal at bronchoscopy, and neither of these two patients had radiological evidence (on CT scan) of subcarinal node enlargement. One of the patients with a positive aspirate had positive sputum cytology, but in the other three the diagnosis of carcinoma of the lung was confirmed by bronchial brushings or biopsy. Ten patients with non-small-cell carcinoma who had negative aspirates have undergone surgery. Details of these patients are shown in Table III. Seven had squamous cell carcinoma, two had adenocarcinoma and one had a thymoma. Six of these patients had enlarged subcarinal lymph nodes, as assessed by the surgeon at the time of operation, but histological examination of the operative specimen revealed malignant lymph node involvement in only two of these.
Table 1. Sixty patients with pulmonary
neoplasm
Neoplasm
N
Positive aspirate
70
Squamous cell Adenocarcinoma Oat cell Other Total
32 8 12 8 60
3 1 0 0 4
9.4 12.5 6.67
Table II. Patients
with positive
Histology
Tumour
Squamous cell Adenocarcinoma Squamous cell Squamous cell
RLL RML RUL RUL
*FOB,
fibreoptic
site
bronchoscopy.
aspirates ‘Curina involved’ at FOB* No No Yes Yes
152
BR.
Table III.
.I. DIS.
CHEST:
VOL.
Patients with negative undergoing surgery
82 NO.
2
subcarinal
aspirates
Histology
Number
Nodes enlarged clinically
Nodes involved histologically
Squamous cell Adenocarcinoma Other
7
5 1
2 0
0
0
2 1
Some aspirates contained no cells, or very few cells. These were reported by the cytologist as having insufficient material for diagnosis. Overall, 9/60 (15%) of aspirates were technically inadequate in this way. Of the patients undergoing surgery, two aspirates had insufficient material for diagnosis, but neither of these two patients had malignant involvement of the subcarinal lymph nodes at histology. No adverse effects were recorded. A small amount of bleeding was often observed at the puncture site. This was always short-lived and never amounted to more than a few ml of blood. No pneumothoraces were observed after this procedure. DISCUSSION The use of transbronchial needle aspiration to diagnose benign or malignant lung tumours outside the bronchial lumen has been advocated for use with the fibreoptic bronchoscope for several years (7-9). This technique has not been widely adopted for the sampling of extrabronchial lymph node tissue in the UK, despite reports from the USA that a high proportion of aspirates were positive. The series reported here does not confirm these very high proportions of positive results, but does suggest that the technique could be of value in routine clinical practice in this country, since 10% of patients presenting with non-smallcell carcinoma of the lung had a positive aspirate, providing in them useful staging information. The proportion of positive aspirates in this series, at 10%) was considerably lower than that reported elsewhwere. Wang & Terry (4) reported 60% positive aspirates and Harrow et al. (5) reported 37%. This may reflect differences in clinical practice. We included in this series all patients proven to have a malignancy undergoing fibreoptic bronchoscopy as part of their routine investigation over a 9-month period. However, at this hospital, where the cytology service has been shown to be effective in the diagnosis of carcinoma of the lung (lo), not all patients with carcinoma of the lung undergo fibreoptic bronchoscopy. If sputum cytology is positive and operative intervention precluded because of age, poor pulmonary function or other factors, bronchoscopy is regarded as unnecessary. Many of the patients reported in this series were being actively considered for surgical referral, and few had extensive malignant disease. Furthermore, no attempt was made in this series to assess malignant involvement of paratracheal nodes. Had this been done, a higher proportion of positive aspirates might have been found. This study was not designed to assess the false positive and false negative rate of the technique. Clearly the question of false positives is of particular importance, as there is a
BLAINEY,
CURLING,
GREEN:
TRANSBRONCHIAL
ASPIRATION
153
possibility that the aspirate may be contaminated by malignant cells from the bronchial lumen. Indeed one such false positive aspirate has been reported (6). In this case, however, only a single clump of malignant cells was found in the aspirate, whereas in all the aspirates that we reported as positive, malignant cells were scattered widely throughout the aspirate. Furthermore, lymphocytes were identified in all the positive aspirates, suggesting that a lymph node had been entered by the aspirating needle. For these reasons we believe it unlikely that any of these were false positive aspirates. Clearly only surgical removal and histological examination of these nodes can answer this question, and none of the patients with positive aspirates in this series has undergone thoracic surgery. We therefore regard a positive aspirate as a strong contraindication to surgery, although the patients with positive aspirates in this series had other factors (such as age, pulmonary function) which were additional relative contraindications. An indication of the proportion of false negatives is provided by the 10 patients with non-small-cell carcinoma of the lung and negative aspirates who have undergone surgery. Although the subcarinal lymph nodes were clinically enlarged in six of these patients at the time of operation, only two (20%) had histological evidence of malignant involvement. This false negative rate of 20% is the same as that reported by others (5). Transbronchial aspiration of lymph nodes appears to be very safe. No serious complications have occurred in our series, and the bleeding at the puncture site which is usually seen after the needle has been removed is minor. The technique is also rapid and simple, and can easily be incorporated into a routine fibreoptic bronchoscopy. Providing sufficient time is allowed for aspiration to allow malignant cells to get into the needle, adequate samples can generally be obtained. In conclusion, transbronchial aspiration is a safe and simple method of sampling subcarinal lymph nodes. In this series, the technique made a useful contribution to the staging of non-small-cell carcinoma of the lung in 10% of patients presenting with this condition. It could be included in the routine bronchoscopic assessment of patients with pulmonary malignancy or used selectively in those where surgery is actively contemplated.
ACKNOWLEDGEMENTS We are grateful to the Cancer Research Campaign who provided financial support for this study, and to the nursing staff of the endoscopy theatre and the technicians of the Department of Cytology at St Bartholomew’s Hospital for their practical assistance.
REFERENCES 1. Fosburg RG, O’Sullivan MJ, Ah Tye P, Gibbons JA, Oury JH. Positive mediastinoscopy; an ominous finding. Ann Thorac Surg 1984;20:678-81. 2. Henney J, Ishikawa S, Jacobs EM. Lung cancer: surgical aspects overview. Prog Cancer Res Ther 1979;11:231-5.
3. Wang KP, Terry P, Marsh B. Bronchoscopic needle aspiration biopsy of paratracheal tumours. Am Rev Resp Dis 1978;118:17-21.
4. Wang KP, Terry P. Transbronchial needle aspiration in the diagnosis and staging of bronchogenie carcinoma. Am Rev Resp Dis 1983;127:3447.
154
BR.
J. DIS.
CHEST:
VOL.
82 NO. 2
5. Harrow EM, Oldenburg FA, Smith AM. Transbronchial needle aspiration in clinical practice. Thorax
1985;40:756-9.
6. Cropp AJ, DiMarco AF, Lankerani M. False positive transbronchial needle aspiration in bronchogenic carcinoma. Chest 1984;84:696-7. 7. Buirski G, Calverley PMA, Douglas NJ, et al. Bronchial needle aspiration in the diagnosis of bronchial carcinoma. Thorax 1981;36:508-11. 8. Schwartz DB, Beals JF, Wimbish KJ, Hammersley JR. Transbronchial fine needle aspiration of bronchogenic cysts. Chest 1985;84:.573-5. 9. Schenk DA, Bower JH, Bryan CL, et al. Transbronchial needle aspiration staging of bronchogenie carcinoma. Am Rev Resp Dis 1986;134:1468. 10. Oswald NC, Hanson KFW, Canti G, Miller AB. The diagnosis of primary lung cancer with special reference to sputum cytology. Thorax 1971;26:623-9.
Date accepted 21 January
1987
TRANSBRONCHIAL SUBCARINAL A. D. BLAINEY*, *Department
ASPIRATION OF LYMPH NODES
M. CURLING? AND MALCOLM
of Respiratory
Medicine and t Department St Bartholomews Hospital, London
GREEN* of Cytology,
Summary
Transbronchial needle aspiration of subcarinal lymph nodes has been undertaken in 60 consecutive patients with pulmonary malignancies undergoing routine fibreoptic bronchoscopy. Four aspirates from the subcarinal nodes contained malignant cells; three squamous cell carcinoma and one adenocarcinoma. Four of 40 (10%) of patients with nonsmall-cell carcinoma of the lung had a positive aspirate. We have not confirmed the high positive rate previously reported, but nevertheless transbronchial needle aspiration provided useful staging information in some patients. The technique is rapid, safe and simple, and can easily be applied in a routine bronchoscopy service for all patients with suspected cancer, or selected patients under active consideration for surgery. INTRODUCTION It is generally agreed that surgery offers the best hope of cure for non-small-cell carcinoma of the lung, but only a small proportion of these tumours are resectable. It is often difficult to decide whether operation is appropriate for a particular patient. Many factors, including age, pulmonary function, and the stage of the disease, contribute to this decision. Staging includes the assessment of mediastinal lymph node involvement by tumour (1). Many surgeons recommend invasive investigation such as mediastinoscopy to assess this, but some lymph node groups-particularly those in the subcarinal area-are inaccessible to mediastinoscopy. Even with mediastinoscopy, a substantial proportion of patients end up with a higher stage of disease (more extensive local involvement) when assessed at thoracotomy (2). Recently American authors have suggested that needle aspiration at fibreoptic bronchoscopy may help to identify involvement of lymph nodes. This technique was originally developed for use with the rigid bronchoscope (3), but has recently been extended to the fibreoptic bronchoscope using a flexible needle by Wang and Terry (4). They reported that as many as 60% of patients undergoing fibreoptic bronchoscopy for carcinoma of the lung had lymph nodes involved by malignant tumour. A more recent study from the USA evaluating this technique in clinical practice found that 37% of Correspondence to: Dr Malcolm Green, Department of Respiratory Medicine, Brompton Hospital, London SW3 6HP.
150
BR.
.I. DIS.
CHEST:
VOL.
82 NO.
2
patients with carcinoma of the lung had a positive lymph node aspirate (5). If these figures reflected routine clinical practice in the UK, then this technique clearly deserves to be more widely applied. Alternatively it might be that these patients represented a selected group and therefore the technique is not of value in routine practice. We therefore set out to study this technique in the clinical setting of a routine bronchoscopy service for patients attending a chest clinic with possible carcinoma of the lung. Methods and Subjects Subjects We have studied all patients undergoing fibreoptic bronchoscopy over a 9-month period in whom a diagnosis of pulmonary malignancy was confirmed. This totalled 60 patients; 39 were male and 21 female. Ages ranged from 27 to 79 years. All of these patients were undergoing routine fibreoptic bronchoscopy for the diagnosis of bronchial carcinoma, or the assessmentof operability. All patients gave informed written consent for the bronchoscopy which was undertaken as part of necessary clinical investigation. Methods Fibreoptic bronchoscopy was carried out under local anaesthesia with 4% lignocaine; either an opiate premeditation or intravenous diazepam was used to sedate the patient. After the transnasal passageof the bronchoscope and a preliminary inspection of the bronchial tree, the instrument was positioned just above the carina. The needle used for transbronchial aspiration was the Microvasive 10 mm sclerotherapy needle (Microvasive Corp, USA; supplied by Keymed, Southend; Fig. 1). This is passed through the bronchoscope completely enclosed in its outer sheath. It is then positioned just below and to the right of the carina in the posterior wall of the bronchus, and the needle is pushed out through the bronchoscope and into the subcarinal tissue. Penetration of the needle can be confirmed by visual inspection. A steady aspiration pressure is then applied with a syringe at the proximal end of the needle for at least 1 minute, while the needle is moved gently up and down and rotated within the subcarinal tissue. The material aspirated into the needle is then expelled on to a cytology slide. The aspirate is spread and fixed immediately in 50% ether/50% ethyl alcohol. Slides were stained with a Papanicolou stain using haematoxylin orange G and eosin 50, then mounted ready for screening. Bronchial brushings, washings and biopsies were taken after transbronchial needle aspiration. These were processed by the departments of cytology and histology in routine fashion. The aspirate was regarded as positive where malignant cellsof identical appearance to those seen in sputum, wash or brushings were identified scattered widely throughout the aspirate. A single clump of malignant cells was not regarded as a positive aspirate, since this appearance may result from contamination with malignant cells within the bronchial tree (6).
lctbl
II
21
Fig. 1. Photograph of aspiration needle projecting from its outer sheath which in turn is protruding from the tip of the bronchoscope
BLAINEY,
CURLING,
GREEN:
TRANSBRONCHIAL
ASPIRATION
151
RESULTS The results of subcarinal lymph node aspiration in 60 patients with malignant pulmonary disease are shown in Table I. Thirty-two patients had squamous cell carcinoma, and the aspirate contained malignant cells in three of these. In one out of eight patients with adenocarcinoma the aspirate was positive. Malignant cells were scattered widely throughout the slide in all positive aspirates. Aspiration was negative in 12 patients with oat cell carcinoma and eight patients with other pulmonary malignancies, which were mostly lymphomas. Overall, 4/40 (10%) of patients with non-small-cell carcinoma of the lung had positive aspirates. Further details of the patients with positive aspirates are shown in Table II. In the three patients with squamous cell carcinoma, the tumour was right sided-in the RUL in two and the RLL in the other. The tumour was also right sided in the patient with adenocarcinema who had a positive aspirate. In two of these patients the carina appeared normal at bronchoscopy, and neither of these two patients had radiological evidence (on CT scan) of subcarinal node enlargement. One of the patients with a positive aspirate had positive sputum cytology, but in the other three the diagnosis of carcinoma of the lung was confirmed by bronchial brushings or biopsy. Ten patients with non-small-cell carcinoma who had negative aspirates have undergone surgery. Details of these patients are shown in Table III. Seven had squamous cell carcinoma, two had adenocarcinoma and one had a thymoma. Six of these patients had enlarged subcarinal lymph nodes, as assessed by the surgeon at the time of operation, but histological examination of the operative specimen revealed malignant lymph node involvement in only two of these.
Table 1. Sixty patients with pulmonary
neoplasm
Neoplasm
N
Positive aspirate
70
Squamous cell Adenocarcinoma Oat cell Other Total
32 8 12 8 60
3 1 0 0 4
9.4 12.5 6.67
Table II. Patients
with positive
Histology
Tumour
Squamous cell Adenocarcinoma Squamous cell Squamous cell
RLL RML RUL RUL
*FOB,
fibreoptic
site
bronchoscopy.
aspirates ‘Curina involved’ at FOB* No No Yes Yes
152
BR.
Table III.
.I. DIS.
CHEST:
VOL.
Patients with negative undergoing surgery
82 NO.
2
subcarinal
aspirates
Histology
Number
Nodes enlarged clinically
Nodes involved histologically
Squamous cell Adenocarcinoma Other
7
5 1
2 0
0
0
2 1
Some aspirates contained no cells, or very few cells. These were reported by the cytologist as having insufficient material for diagnosis. Overall, 9/60 (15%) of aspirates were technically inadequate in this way. Of the patients undergoing surgery, two aspirates had insufficient material for diagnosis, but neither of these two patients had malignant involvement of the subcarinal lymph nodes at histology. No adverse effects were recorded. A small amount of bleeding was often observed at the puncture site. This was always short-lived and never amounted to more than a few ml of blood. No pneumothoraces were observed after this procedure. DISCUSSION The use of transbronchial needle aspiration to diagnose benign or malignant lung tumours outside the bronchial lumen has been advocated for use with the fibreoptic bronchoscope for several years (7-9). This technique has not been widely adopted for the sampling of extrabronchial lymph node tissue in the UK, despite reports from the USA that a high proportion of aspirates were positive. The series reported here does not confirm these very high proportions of positive results, but does suggest that the technique could be of value in routine clinical practice in this country, since 10% of patients presenting with non-smallcell carcinoma of the lung had a positive aspirate, providing in them useful staging information. The proportion of positive aspirates in this series, at 10%) was considerably lower than that reported elsewhwere. Wang & Terry (4) reported 60% positive aspirates and Harrow et al. (5) reported 37%. This may reflect differences in clinical practice. We included in this series all patients proven to have a malignancy undergoing fibreoptic bronchoscopy as part of their routine investigation over a 9-month period. However, at this hospital, where the cytology service has been shown to be effective in the diagnosis of carcinoma of the lung (lo), not all patients with carcinoma of the lung undergo fibreoptic bronchoscopy. If sputum cytology is positive and operative intervention precluded because of age, poor pulmonary function or other factors, bronchoscopy is regarded as unnecessary. Many of the patients reported in this series were being actively considered for surgical referral, and few had extensive malignant disease. Furthermore, no attempt was made in this series to assess malignant involvement of paratracheal nodes. Had this been done, a higher proportion of positive aspirates might have been found. This study was not designed to assess the false positive and false negative rate of the technique. Clearly the question of false positives is of particular importance, as there is a
BLAINEY,
CURLING,
GREEN:
TRANSBRONCHIAL
ASPIRATION
153
possibility that the aspirate may be contaminated by malignant cells from the bronchial lumen. Indeed one such false positive aspirate has been reported (6). In this case, however, only a single clump of malignant cells was found in the aspirate, whereas in all the aspirates that we reported as positive, malignant cells were scattered widely throughout the aspirate. Furthermore, lymphocytes were identified in all the positive aspirates, suggesting that a lymph node had been entered by the aspirating needle. For these reasons we believe it unlikely that any of these were false positive aspirates. Clearly only surgical removal and histological examination of these nodes can answer this question, and none of the patients with positive aspirates in this series has undergone thoracic surgery. We therefore regard a positive aspirate as a strong contraindication to surgery, although the patients with positive aspirates in this series had other factors (such as age, pulmonary function) which were additional relative contraindications. An indication of the proportion of false negatives is provided by the 10 patients with non-small-cell carcinoma of the lung and negative aspirates who have undergone surgery. Although the subcarinal lymph nodes were clinically enlarged in six of these patients at the time of operation, only two (20%) had histological evidence of malignant involvement. This false negative rate of 20% is the same as that reported by others (5). Transbronchial aspiration of lymph nodes appears to be very safe. No serious complications have occurred in our series, and the bleeding at the puncture site which is usually seen after the needle has been removed is minor. The technique is also rapid and simple, and can easily be incorporated into a routine fibreoptic bronchoscopy. Providing sufficient time is allowed for aspiration to allow malignant cells to get into the needle, adequate samples can generally be obtained. In conclusion, transbronchial aspiration is a safe and simple method of sampling subcarinal lymph nodes. In this series, the technique made a useful contribution to the staging of non-small-cell carcinoma of the lung in 10% of patients presenting with this condition. It could be included in the routine bronchoscopic assessment of patients with pulmonary malignancy or used selectively in those where surgery is actively contemplated.
ACKNOWLEDGEMENTS We are grateful to the Cancer Research Campaign who provided financial support for this study, and to the nursing staff of the endoscopy theatre and the technicians of the Department of Cytology at St Bartholomew’s Hospital for their practical assistance.
REFERENCES 1. Fosburg RG, O’Sullivan MJ, Ah Tye P, Gibbons JA, Oury JH. Positive mediastinoscopy; an ominous finding. Ann Thorac Surg 1984;20:678-81. 2. Henney J, Ishikawa S, Jacobs EM. Lung cancer: surgical aspects overview. Prog Cancer Res Ther 1979;11:231-5.
3. Wang KP, Terry P, Marsh B. Bronchoscopic needle aspiration biopsy of paratracheal tumours. Am Rev Resp Dis 1978;118:17-21.
4. Wang KP, Terry P. Transbronchial needle aspiration in the diagnosis and staging of bronchogenie carcinoma. Am Rev Resp Dis 1983;127:3447.
154
BR.
J. DIS.
CHEST:
VOL.
82 NO. 2
5. Harrow EM, Oldenburg FA, Smith AM. Transbronchial needle aspiration in clinical practice. Thorax
1985;40:756-9.
6. Cropp AJ, DiMarco AF, Lankerani M. False positive transbronchial needle aspiration in bronchogenic carcinoma. Chest 1984;84:696-7. 7. Buirski G, Calverley PMA, Douglas NJ, et al. Bronchial needle aspiration in the diagnosis of bronchial carcinoma. Thorax 1981;36:508-11. 8. Schwartz DB, Beals JF, Wimbish KJ, Hammersley JR. Transbronchial fine needle aspiration of bronchogenic cysts. Chest 1985;84:.573-5. 9. Schenk DA, Bower JH, Bryan CL, et al. Transbronchial needle aspiration staging of bronchogenie carcinoma. Am Rev Resp Dis 1986;134:1468. 10. Oswald NC, Hanson KFW, Canti G, Miller AB. The diagnosis of primary lung cancer with special reference to sputum cytology. Thorax 1971;26:623-9.
Date accepted 21 January
1987