European Journal ofRadiology, 12 (1991) 98-103 Elsevier
98
EURRAD
00136
Transthoracic aspiration biopsy of pulmonary and mediastinal lesions M.A. de Gregorio Ariza, E.R. Alfonso Aguirhn, J.L. Villavieja Atance, J. Torres Nuez, J.I. Pina Leita, M.D. Ab6s Olivares and J.L. Benito ArCvalo Hospital Chico Universitario.Servicio de Radiodiagnhtico, Zaragoza, Spain (Received 28 February
1990; revised version 14 August; accepted
Key words: biopsy; Lung, neoplasm;
Lung, aspiration;
26 October
Lung neoplasm,
1990)
aspiration
Abstract Thoracic aspiration biopsy (TAB) constitutes a useful technique in establishing a diagnosis in diseases of the lungs and mediastinum. Results obtained from 1046 fluoroscopically-guided TABS are presented with review of the most important aspects of the technique. Diagnostic accuracy in malignancy detection was 93.8% in lung lesions (n = 984) and 74.5% in mediastinal lesions (n = 62). Sensitivity was higher in peripheral than in central lesions (96% vs. 87%, respectively). Specificity was 100% in both groups. Sensitivity in lesions smaller than 2 cm was 70% and 94% in larger lesions. Aspiration biopsies performed with Chiba and Franseen needles showed a similar sensitivity (95%) higher than with other types of needles. A pneumothorax developed in 138 patients (13.2%). Only eight of these required the use of an endothoracic tube (0.8% of all biopsies).
Introduction Transthoracic aspiration biopsy (TAB) is a cheap, quick, simple and safe method in the evaluation of many lesions within the chest. It has a high diagnostic accuracy. Following the work of Leyden [ 1] and Menetrier [ 21, other workers have attempted to find ways of providing a precise preoperative diagnosis. One century of technical development has contributed to TAB becoming a routine procedure in the pathology of the respiratory system [3-81. Since 1981 we have performed a total of 1046 TABS at the University Hospital in Zaragoza. Our experiences, as well as a revision and a discussion of some of the important aspects of this technique are set out in this paper. Patients and Methods 855 TABS have been carried out on men (81.7%) and 191 on women (18.3%). The mean age was 51.6 Address for reprints: M.A. de Gregorio Ariza, M.D., Avda. Gomez Laguna 13, 5B 50.009 Zaragoza, Spain. 0720-048X/91/$03.50
0 1991 Elsevier Science Publishers
years with a range of 13-92. There were 984 pulmonary (94.1%) and 62 media&al lesions (5.9%). The site of the lesions biopsied is set out in Table 1. “Central lesions” are those located either in the mediastinum or less than 4 cm from its external outline. “Diffuse lesions” refers to widespread lesions with systematic alveolar and/or interstitial involvement, as opposed to circumscribed or focal lesions.
TABLE
1
Location of the biopsed lesions (n = 1046) Location
Central Lung Mediastinum Anterior Middle Posterior Peripheral Diffuse
B.V. (Biomedical
Division)
Number of cases (n = 1046) n
%
389 327 62 13 41 8 585 72
37.2 31.3 5.9
55.9 6.9
99
The smallest lesion biopsied in either the mediastinum or lung, was 1 cm. The TAB is performed in a semi-sterile room in the Radio-diagnosis Department, equipped with a C-arm image intensifier and TV chain. In most cases in our series CT guided biopsy and immediate cytological assessment were not available. Different types of needles have been used; e.g., Chiba, Franseen, Westcott and Rotex II, with a gauge of 18-22 and a length of lo-22 cm. The procedure was performed as described by other workers [8-lo]. Lesions were biopsied with an orthogonal approach from the nearest point in the chest wall, attempting to avoid the pleural cavity in mediastinal lesions. The specimens obtained were immediately put into an alcohol based solution used for cytologic treatment using Papanicolaou’s stain, or left to dry when using May Grunwald Giemsa’s method. The need for a second or third pass was usually decided depending on the grossly visual appearance of the first material. Patients remained in hospital for 12- 14 hours after the TAB. Check chest radiographs for pneumothorax were carried out just after the puncture and then 6-8 hours later.
TABLE
Results
as malignant tumours of which the nature could not be established by TAB, 14 (58.3%) proved to be squamous-cell carcinoma, 7 (29.2%) oat-cell carcinoma and 2 (8.3%) large-cell carcinoma. One case is not verified. On the mediastinum, there were no generic malignant diagnoses. For statistical purposes under the term “nonneoplastic conditions” we have grouped together both
The results have been grouped into four sections : (1) Type of malignancy specified; (2) Type of malignancy not specified; (3) Non-neoplastic conditions; (4) No diagnosis due to lack of material. Table 2 shows the different malignancies diagnosed by pulmonary TAB. In the mediastinum 3 1 lesions were found following the spread of bronchogenic tumours. Of these, 19 (61.3 %) were squamous cell carcinomas and 12 (38.7 %) oat-cell carcinomas. The most frequent non-bronchogenic tumour was lymphoma, which represents, with 6 cases, 9.7% of all mediastinal masses. These cytopathological results were confirmed by surgery (38.8%), by clinical features (20.40/‘,), by other diagnostic procedures such as bronchoscopy (26.5%), by lymph-node biopsy and other biopsies (13.1%) and by a second TAB (1.2%). (Tables 3 and 4). The diagnosis of benign neoplasms and cysts by TAB in lung lesions (18 cases in Table 3) were as follows: Castleman’s disease, 4 cases; hamartoma, 3 ; hydatid cyst, 3; adenoma, 2; lipoma, 2; lipoid pneumonia, 2; bronchogenic cyst, 1; and spindle cell tumour, 1. The 4 (other) non-bronchogenic or non-lymphomatous malignant neoplasms of the mediastinum (Table 4) were: 2 embryonal cell carcinomas, 1 malignant teratoma and 1 intrathoracic thyroid carcinoma. Of the 24 cases in the lungs which were diagnosed
2
Cytological diagnosis of malignancy
by TAB in the lung (n = 984)
1. Bronchogenic carcinoma Squamous cell Small cell undifferentiated carcinoma Adenocarcinoma Large cell carcinoma Undifferentiated carcinoma Bronchoalveolar carcinoma
644 (86.4%) 409 (54.95,) 113 (15.27”) 62 (8.3’6) 19 (2.59,) 30 (4.0”/,)
11 (IS”,)
2. Other malignant neoplasms Lymphoma* Sarcoma Multiple myeloma
32 11 8 13
(4.3%) (1.5”/b) (l.l”,O) (1.7%)
3. Metastases Breast Colon Larynx Other
69 26 19 13 11
(9.3%) (3.5 “R~) (2.5”~) (1.7”;) (1.59”)
745 (loo?;)
Total
* Includes cases with nodular intrapulmonary lesions and/or diffuse interstitial involvement proved to be lymphomatous, with or without present extrapulmonary disease.
TABLE
3
Diagnostic
results by TAB in lung lesions (n = 984)
1. Type of malignancy specified Bronchogenic carcinoma Other malignant neoplasms Metastases
644 (65.4jjb) 32 (3.2%) 69 (7.0%)
2. Type of malignancy not specified Malignancy
24 (2.40/h)
3. Non-neoplastic conditions False negative Benign neoplasms Infections Other Not verified
49 18 87 :!l Ill
4. No diagnosis Inadequate material
29 (2.9%)
(5.0%) (1.8:/,) (8.8%) (2.4%) (1.1:;)
100 TABLE 4 Diagnostic
TABLE results by TAB in mediastinal
1. Type of malignancy specified Bronchogenic carcinoma Lymphoma Other malignant neoplasms
lesions (n = 62)
Diagnostic value of the TAB in the lung related to lesion depth and size (n = 984)
31 (50.0%)
0 (0.0%)
3. Non-neoplastic conditions False negative Benign neoplasms Inflammatory disease Hematoma Not verified
0 3 2 4
4. No diagnosis Inadequate material
5 (8.1%)
No. of cases (n = 984) n
%
Central Peripheral Diffuse
327 585 72
33.2 59.4 7.3
B. Size
No. of cases (n = 912)*
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
87.0 96.0 99.1
100 100 100
78.2 90.1 78.1
Sensitivity (%)
Specificity
Accuracy
(%)
(%)
71.2 94.7 97.2 97.3
100 100 100 100
56.3 89.1 91.3 89.1
7 (11.3%) (0.0%) (4.8%) (3.2%) (6.4%)
benign lesions and the false-negative diagnoses of malignancy. This group is detailed in Table 5. No adequate material was available in order to give a diagnosis in 29 cases of the pulmonary TABS (2.9%) and in 5 cases (8.1%) of the mediastinal TABS. In 4 1.3% of all those cases without material, a pulmonary or mediastinal tumour was later confirmed, 5 1.7y0 were inflammatory processes. We have studied the diagnostic value of the TAB (sensitivity and specificity) relating to several factors, such as size and location of the lesion, type of needle and number of needle passes. The findings are shown in Tables 4-8.
(cm)
l-2 2-5 5-10 > 10
n
%
87 595 153 71
9.5 65.2 16.7 8.4
* Diffuse lesions are not included.
There were no major complications due to the use of the technique. The most common complication was pneumothorax, observed in 138 cases (13.2%). It was necessary to place an endothoracic tube in only 8 of these (0.8% of all biopsies). 37 pneumothoraces (26.8%) were detected on 6 hours delayed follow-up TABLE
7
Diagnostic value of the TAB in lung and mediastinum needle type
5
Non-neoplastic
A. Location
6 (9.7%) 4 (6.4%)
2. Type of malignancy not specified Malignancy
TABLE
6
conditions
1. False negative Squamous cell carcinoma Small cell undifferentiated
- diagnosis in TAB of the lung (n = 187) 49 (26.2%) 35 (18.7%) carcinoma
Adenocarcinoma Large cell carcinoma Undifferentiated carcinoma Bronchoalveloar carcinoma
6 4 3 1 9
(3.2%) (2.1%) (1.6%) (0.5%) (4.8%)
2. Inflammatory diseases Tuberculosis
87 (46.5%) 29 (15.5%)
Cryptococcosis Legionellosis Other
5 (2.7%) 8 (4.3%) 45 (24.1%)
3. Not verified
11 (5.9%)
1. Lung (n = 984) Type of needle
Chiba Franseen Westcott Rotex Other
No. of cases n
%
516 296 106 54 12
52.4 30.1 10.8 5.5 1.2
2. Mediastinum
(n = 62)
Type of needle
No. of cases n
4. Benign neoplasms and cyst
18 (9.6%)
5. Other
21 (11.2%)
related to
Chiba Franseen
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
95 95 88 75 80
100 100 100 100 100
88.6 88.6 65.9 68.7 66.6
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
88.0 88.8
100 100
70.9 80.0
% 38 24
61.3 38.7
101
TABLE
8
Diagnostic value of the TAB related to number of needle passes (n = 1046) No. of passes
1 2 3 References
No. of cases Sensitivity -_%) n
0, /o
258 462 326
24.1 44.2 31.2
(see separate
87.2 93.2 91.2
(%)
Specificity
Accuracy (%)
100 100 100
68.9 89.6 65.9
sheet).
radiographs. Self-limited hemoptyses were found in 12 patients (1.1%) and small peripheral alveolar infiltrations on chest radiograph, due to parenchymal haemorrhage, in 8 (0.8%). The rate of hemoptyses was much higher with Rotex needles (6.2%). 59 patients (5.6%) complained of chest pain or discomfort during or after the procedure. It was relieved by simple oral analgesics (Nolotil). There were no complications following the accidental biopsy of the 3 patients with hydatid cysts. The average hospital stay following TAB was 26.8 hours and the average cost of employing this technique in our hospital was $ 340 (41,000 pesetas). Discussion The diagnostic accuracy of TAB is variable. According to different authors, its sensitivity ranges from 72% [ 1 l] to 97% [ 121. Positive results provided by TAB depend on aspects inherent in the lesion, such as its benign or malignant nature, size and location, technical devices (type of imaging-guide and needle and number of needle passes) and finally, those related to human factors (the skill and experience of the medical staff and the co-operation of the patient) [ 13-171. In our series, sensitivity was higher in peripheral than in central lesions (96% and 86%, respectively) and much higher in lesions larger than 2 cm (94% vs. 70% in smaller ones). In the present group of 984 pulmonary lesions, we have achieved a level of accuracy for the diagnosis of malignancy of 93.8x, somewhat above the level we obtained early in our experience [ 181 when employing the same technique (87% in 247 TABS). In the mediastinum, overall sensitivity was 88 % and accuracy 74.8%, similar to the percentages reported by others [ 19-211. Considering the type of needle used, aspiration biopsies performed in our series with Chiba and Franseen needles showed a similar sensitivity (95%) being higher than that achieved with other types of
needle. Each author appears to achieve his best results using the tools with which he has more experience [ 22-241. Many types of needle have been introduced in order to improve results and reduce complications. Publications to which we referred on the subject of abdominal biopsies show that, although the size of the sample obtained is different depending on the type of needle, the quality and the degree of artefact are determined by the calibre of the needle [25]. Wittemberg [26] could not find any difference which implied an important advantage in his study of several types of 22 G needle. We do not think that there is any reason which prevents us from transferring this conclusion to thoracic biopsies, with respect to diagnostic results, if we put to one side the risk of pneumothorax. In our group, sensitivity increased from 86.8% with a single pass to 95.8% with three passes. Immediate microscopic assessment of the cytological quality of the samples improves the efficiency of the technique, decreasing the need for repeated passes and avoiding unnecessary risks [ 271; however, this was not the case in all series [28]. We only used this quick evaluation by the cytologi.st (working in the same X-ray department) in selected cases, where there was at least one previous negative biopsy. We had no false-positive results, either in the lungs or mediastinum. Specificity of the technique and the predictive value of a positive result were 100%. Fluoroscopy is the most suitable imaging procedure for guidance in most cases of TAB of the lung, for both economic and technical reasons. It is generally available and provides real-time imaging of the lesions during the biopsy. However, CT has been shown to be extremely effective for the location and biopsy of small lesions, which are either close to the hilium or to the mediastinum, or which are invisible on fluoroscopy, even though the patient is lying in the most appropriate decubitus for biopsy [29-301. As with CT, ultrasonography also provides valuable diagnostic information about the nature of the lesion, provided that it makes contact with the chest wall. The information obtained by this method can make puncture inadvisable or even contraindicated (as in the case of cystic lesions in patients with clinically or biologically suspected hydatid disease). However, sonography is not useful for guidance at TAB. Theoretically, one could use it to biopsy pleural masses hidden by a pleural effusion, but in such cases, aspirated fluid is suitable material for cytological diagnosis. The value of a non-invasive diagnostic technique depends on the balance between its diagnostic efficien-
102
cy and its safety [lo]. Fatal complications following TAB are extremely rare and are usually due to massive pulmonary haemorrhage and air embolism. Pleural or pulmonary infection and tumour spread through the biopsy needle track are also exceptional [9,31,32]. We have observed none of these complications in our series. If we do not take into account the obvious influence of experience with the technique shown by the radiologist who performs the TAB, then the frequency and degree of complications are essentially determinded by the calibre of the needle, as well as by its design [6,32]. Our overall rate of hemoptyses was low, but it reached 6.2% with the Rotex needle. Pneumothorax is the most frequent complication following TAB. General agreement exists in the literature about three factors which seem to be directly involved in the appearance of pneumothorax after TAB. These are: the presence of objective criteria of chronic obstructive pulmonary disease (estimated by pulmonary function tests) [33], the number of passes and the type and calibre of the needle. Probably, factors such as the size and location of the lesion and the availability of quick cytological examination of samples also have an influence over the risk of post-biopsy pneumothorax, because the number of needle passes varies [ 15,27,28]. We have observed a noticeable decrease in our current percentage of pneumothorax with respect to the first group (23% in 247 TABS), in which three attempts were systematically and habitually made. We have established severe haemorrhagic diathesis and suspected hydatid disease as absolute contraindications of TAB (nevertheless, we have accidentally biopsied three hydatid cysts without later complications). We also consider severe emphysema, pulmonary hypertension and a non-cooperative patient as relative contraindications. Timing for control chest radiographs and clinical follow-up after TAB have been the subject of discussion in the literature [ 341. Several authors report a considerable experience of TAB on non-hospitalized patients, without increasing the number of complications or their severity [35,36]. Patients must be warned not to move any significant distance from the hospital and that they should return to it if symptoms occur. Out-patient biopsy is a safe procedure which reduces hospital charges. In contrast to other series, 26.8% of pneumothoraces in our study were only detectable on subsequent radiographs, taken 6 hours after biopsy. None of them, however, had need of treatment and it is likely that its lack of diagnosis would have had no further consequences but, because of that possibility, we admit
patients on the morning of the biopsy and do not discharge them before 6 or 8 hours after having concluded :+ IL.
Surgical placing of a traditional endothoracic tube is not necessary in every patient with a severe pneumothorax, who needs treatment. According to several reports [8,38] in many cases, aspiration by means of a thin 9 F percutaneous catheter connected to a Heimlich valve [ 371 permits a quick, simple and safe treatment by the radiologist. We have no experience with this procedure, however. In our series, percutaneous puncture only produced slight chest pain or discomfort in 5.6% of cases; overall TAB has a good acceptance by patients. We think that this fact, which has not previously been reported in the literature, implies an important advantage for TAB over other techniques of thoracic biopsy, such as bronchoscopy, and contributes to its establishment and acceptance within the medical community. Diagnostic accuracy of TAB can be compared to that of bronchoscopy, but percutaneous biopsy is especially effective in diagnosis of small peripheral lesions and of those that do not originate from the airways [ 391. The impact of biopsy on patient management and its economic implications are undoubted [ 40,4 11. One TAB requires only cheap instrumentation and uses up a very small share of the working time of an X-Ray telecommanded unit (biplanar fluoroscopy is not routinely needed). TAB decreases both the need for a diagnosis by thoracotomy as well as the time from admission to diagnosis. Therefore, it reduces the time of stay at hospital when carried out on a hospitalized patient; but in any event, there are many cases where TAB can be performed on out-patients, thus decreasing costs without decreasing the safety and utility of the procedure. References 1 Leyden 00. Uber infektiose Pneumonie. Dtsch Med Wchr 1883; 9: 52-56. 2 Menetrier P. Cancer primitif du poumon. Bull Sot Anat Paris 1886; 4: 643. 3 Stewart FW. The diagnosis of tumours by aspiration. Am J Path01 1933; 9: 801-803. 4 Soderstrom N. Identification of normal tissues and tumors by cytologic aspiration biopsy. Acta Sot Med Uppsala 1958; 63: 53-58. 5 Nordenstrom B. A new technique for transthoracic biopsy of lung changes. Br J Radio1 1965; 38: 550-553. 6 Zavala DC, Bedel GN. Percutaneous lung biopsy with a cutting needle. An analysis of 40 cases and comparison with other biopsy techniques. Am Rev Respir Dis 1972; 106: 186-193. 7 Zornoza J, Snow J, Lukeman JM, Libshitz HI. Aspiration biopsy of discrete pulmonary lesions using a new thin needle. Radiology 1977; 123: 519-520.
103 8 Lalli AF, McCormack LJ, Zelch M, Reich NE, Becovich D. Aspiration biopsies of chest lesions. Radiology 1978; 127: 35-40. 9 Perlmutt LM, Johnston WW, Dunnick NR. Percutaneous transthoracic needle aspiration: a review. AJR 1989; 152: 451-455. 10 Greene R. Transthoracic needle aspiration biopsy. In: Athanasoulis ed. Interventional Radiology. Philadelphia: Saunders 1982; 1; 587-634. 11 Lauby VW, Burnett WE, Rosemond GP, Tyson RR. Value and risk of biopsy ofpulmonary lesions by needle aspiration. Twentyone years’ experience. J Thorac Cardiovasc Surg 1965; 49: 1.59-172. 12 Westcott JL. Direct percutaneous needle aspiration of localized pulmonary lesions: results in 422 patients. Radiology 1980; 137: 31-35. 13 Stanley JH, Fish GD, Andriole JG, Gobien RP, Betsill WL, Laden SA, Schabel SI. Lung lesions: cytologic diagnosis by tine needle biospy. Radiology 1987; 162: 389-391. 14 Greene R, Szyfelbein WM, Isler RJ, Stark P, Jantsch H. Supplementary tissue-core histology from line-needle transthoracic aspiration biopsy. AJR 1985; 144: 787-792. 15 Jereb M. The usefulness of needle biopsy in lesions of different sizes and locations. Radiology 1980; 134: 13-15. 16 Williams AJ, Santiago S, Lehrman S, Popper R. Transcutaneous needle aspiration of solitary pulmonary masses: How many passes? Am Rev Respir Dis 1987; 136: 452-454. 17 Khouri NF, Stitik FP, Erozan VS, Gupta PK, Kim WS, Scott WW, Hamper UM, Mann RB, Eggleston JC, Baker RR. Transthoracic needle aspiration biopsy of benign and malignant lung lesions. AJR 1985; 144: 281-288. 18 De Gregorio MA, Conget F, Marco R, Mainar A, Azua J, Rota M. La puncibn aspirativa transtoracica (PAT) coma metodo de diagnbstico en las enfermedades pulmonares. Arch Br 1985; 21: 150-154. 19 Linder J, Olsen GA, Johnston WW. Fine-needle aspiration biopsy of the mediastinum. Am J Med 1986; 81: 1005-1008. 20 Jereb M, Us-Krasovec M. Transthoracic needle biopsy of mediastinal and hilar lesions. Cancer 1977; 40: 1354-1357. 21 Adler OB, Rosenberger A, Peleg H. Invasive radiology in the diagnosis of mediastinal masses. AJR 1983; 140: 893-896. 22 Westcott JL. Percutaneous needle aspiration of hilar and mediastinal masses. Radiology 1981; 141: 323-329. 23 Nahman BJ, Van Aman ME, McLemore WE, O’Toole RV. Use of the Rotex needle in percutaneous biopsy of pulmonary malignancy. AJR 1985; 145: 97-99. 24 House AJS, Thomson KR. Evaluation of a new transthoracic needle for biopsy of benign and malignant lung lesions. AJR 1977; 129: 215-220. 25 Lundquist A. Fine needle aspiration biopsy of the liver. Applica-
26
27
28
29
30
31
32 33
34
35 36 37
38
39
40
41
tions in clinical diagnosis and investigation. Acta Med Stand 1971; 520: l-28. Wittemberg J, Mueller PR, Ferruci JT, Simeone JF, Van Sonnenberg E, Neff CC, Palermo RA, Isler RJ. Percutaneous core biopsy of abdominal tumors using 22 gauge needle: further observations. AJR 1982; 139: 75-80. Miller D, Carrasco CH, Katz RL, Cramer FM, Wallace S, Charnsangavej CH. Fine-needle aspiration biopsy: the role of immediate cytologic assessment. AJR 1986; 147: 155-158. Johnsrude IS, Silverman JF, Weaver MD, McConnel RW. Rapid cytology to decrease pneumothorax incidence after percutaneous biopsy. AJR 1985; 144: 793-794. Gobien RP, Skucas J, Paris BS. CT-assisted fluoroscopically guided aspiration biopsy of central hilar and mediastinal masses. Radiology 1981; 141: 443-447. Cohan RH, Newman GE, Braun SD, Dunnick NR. CT assistance for fluoroscopic guided transthoracic needle aspiration biopsy. J Comput Assist Tomogr 1984; 8: 1093-1098. Nordenstriim B, Sinner WN. Needle biopsies of pulmonary lesions. Precautions and management of complications. RoFo 1978; 129: 414-418. Sinner WN. Complications of percutaneous transthoracic needle aspiration biopsy. Acta Radio1 1976; 17: 813-828. Fish GD, Stanley JH, Miller KS, Schabel SI, Sutherland SE. Postbiopsy pneumothorax: Estimating the risk by chest radiopgraphy and pulmonary function tests. AJR 1988; 150: 71-74. Perlmutt LM, Braun SD, Newman GE, Oke EJ, Dunnick NR. Timing of chest film follow-up after transthoracic needle aspiration. AJR 1986; 146: 1049-1050. Poe RH, Kallay MC. Transthoracic needle biopsy of lung in non hospitalized patients. Chest 1987; 92: 676-678. Stevens GM, Jackman RJ. Outpatient needle biopsy of the lung: its safety and utility. Radiology 1984; 151: 301-304. Sargent EN, Turner AF. Emergency treatment of pneumothorax: a simple catheter technique for use in the radiology department. AJR 1970; 109: 531-535. Casola G, Van Sonnenberg E, Keightley A. Pneumothorax: radiologic treatment with small catheters. Radiology 1988; 166: 89-91. Landman S, Burgener FA, Lim HK. Comparison between bronchial brushing and percutaneous needle biopsy in the diagnosis of malignant lung lesions. Radiology 1975; 115: 275-278. Gobien RP, Bouchard CA, Gobien BS, Valicenti JF, Vujic I. Thin-needle aspiration biopsy of thoracic lesions: impact on hospital charges and patterns of patient care. Radiology 1983; 148: 65-67. Bottles K, Miller TR, Cohen MB, Ljung B. Fine-needle aspiration biopsy. Has its time come? Am J Med 1986; 81: 525-531.
98
EURRAD
00136
Transthoracic aspiration biopsy of pulmonary and mediastinal lesions M.A. de Gregorio Ariza, E.R. Alfonso Aguirhn, J.L. Villavieja Atance, J. Torres Nuez, J.I. Pina Leita, M.D. Ab6s Olivares and J.L. Benito ArCvalo Hospital Chico Universitario.Servicio de Radiodiagnhtico, Zaragoza, Spain (Received 28 February
1990; revised version 14 August; accepted
Key words: biopsy; Lung, neoplasm;
Lung, aspiration;
26 October
Lung neoplasm,
1990)
aspiration
Abstract Thoracic aspiration biopsy (TAB) constitutes a useful technique in establishing a diagnosis in diseases of the lungs and mediastinum. Results obtained from 1046 fluoroscopically-guided TABS are presented with review of the most important aspects of the technique. Diagnostic accuracy in malignancy detection was 93.8% in lung lesions (n = 984) and 74.5% in mediastinal lesions (n = 62). Sensitivity was higher in peripheral than in central lesions (96% vs. 87%, respectively). Specificity was 100% in both groups. Sensitivity in lesions smaller than 2 cm was 70% and 94% in larger lesions. Aspiration biopsies performed with Chiba and Franseen needles showed a similar sensitivity (95%) higher than with other types of needles. A pneumothorax developed in 138 patients (13.2%). Only eight of these required the use of an endothoracic tube (0.8% of all biopsies).
Introduction Transthoracic aspiration biopsy (TAB) is a cheap, quick, simple and safe method in the evaluation of many lesions within the chest. It has a high diagnostic accuracy. Following the work of Leyden [ 1] and Menetrier [ 21, other workers have attempted to find ways of providing a precise preoperative diagnosis. One century of technical development has contributed to TAB becoming a routine procedure in the pathology of the respiratory system [3-81. Since 1981 we have performed a total of 1046 TABS at the University Hospital in Zaragoza. Our experiences, as well as a revision and a discussion of some of the important aspects of this technique are set out in this paper. Patients and Methods 855 TABS have been carried out on men (81.7%) and 191 on women (18.3%). The mean age was 51.6 Address for reprints: M.A. de Gregorio Ariza, M.D., Avda. Gomez Laguna 13, 5B 50.009 Zaragoza, Spain. 0720-048X/91/$03.50
0 1991 Elsevier Science Publishers
years with a range of 13-92. There were 984 pulmonary (94.1%) and 62 media&al lesions (5.9%). The site of the lesions biopsied is set out in Table 1. “Central lesions” are those located either in the mediastinum or less than 4 cm from its external outline. “Diffuse lesions” refers to widespread lesions with systematic alveolar and/or interstitial involvement, as opposed to circumscribed or focal lesions.
TABLE
1
Location of the biopsed lesions (n = 1046) Location
Central Lung Mediastinum Anterior Middle Posterior Peripheral Diffuse
B.V. (Biomedical
Division)
Number of cases (n = 1046) n
%
389 327 62 13 41 8 585 72
37.2 31.3 5.9
55.9 6.9
99
The smallest lesion biopsied in either the mediastinum or lung, was 1 cm. The TAB is performed in a semi-sterile room in the Radio-diagnosis Department, equipped with a C-arm image intensifier and TV chain. In most cases in our series CT guided biopsy and immediate cytological assessment were not available. Different types of needles have been used; e.g., Chiba, Franseen, Westcott and Rotex II, with a gauge of 18-22 and a length of lo-22 cm. The procedure was performed as described by other workers [8-lo]. Lesions were biopsied with an orthogonal approach from the nearest point in the chest wall, attempting to avoid the pleural cavity in mediastinal lesions. The specimens obtained were immediately put into an alcohol based solution used for cytologic treatment using Papanicolaou’s stain, or left to dry when using May Grunwald Giemsa’s method. The need for a second or third pass was usually decided depending on the grossly visual appearance of the first material. Patients remained in hospital for 12- 14 hours after the TAB. Check chest radiographs for pneumothorax were carried out just after the puncture and then 6-8 hours later.
TABLE
Results
as malignant tumours of which the nature could not be established by TAB, 14 (58.3%) proved to be squamous-cell carcinoma, 7 (29.2%) oat-cell carcinoma and 2 (8.3%) large-cell carcinoma. One case is not verified. On the mediastinum, there were no generic malignant diagnoses. For statistical purposes under the term “nonneoplastic conditions” we have grouped together both
The results have been grouped into four sections : (1) Type of malignancy specified; (2) Type of malignancy not specified; (3) Non-neoplastic conditions; (4) No diagnosis due to lack of material. Table 2 shows the different malignancies diagnosed by pulmonary TAB. In the mediastinum 3 1 lesions were found following the spread of bronchogenic tumours. Of these, 19 (61.3 %) were squamous cell carcinomas and 12 (38.7 %) oat-cell carcinomas. The most frequent non-bronchogenic tumour was lymphoma, which represents, with 6 cases, 9.7% of all mediastinal masses. These cytopathological results were confirmed by surgery (38.8%), by clinical features (20.40/‘,), by other diagnostic procedures such as bronchoscopy (26.5%), by lymph-node biopsy and other biopsies (13.1%) and by a second TAB (1.2%). (Tables 3 and 4). The diagnosis of benign neoplasms and cysts by TAB in lung lesions (18 cases in Table 3) were as follows: Castleman’s disease, 4 cases; hamartoma, 3 ; hydatid cyst, 3; adenoma, 2; lipoma, 2; lipoid pneumonia, 2; bronchogenic cyst, 1; and spindle cell tumour, 1. The 4 (other) non-bronchogenic or non-lymphomatous malignant neoplasms of the mediastinum (Table 4) were: 2 embryonal cell carcinomas, 1 malignant teratoma and 1 intrathoracic thyroid carcinoma. Of the 24 cases in the lungs which were diagnosed
2
Cytological diagnosis of malignancy
by TAB in the lung (n = 984)
1. Bronchogenic carcinoma Squamous cell Small cell undifferentiated carcinoma Adenocarcinoma Large cell carcinoma Undifferentiated carcinoma Bronchoalveolar carcinoma
644 (86.4%) 409 (54.95,) 113 (15.27”) 62 (8.3’6) 19 (2.59,) 30 (4.0”/,)
11 (IS”,)
2. Other malignant neoplasms Lymphoma* Sarcoma Multiple myeloma
32 11 8 13
(4.3%) (1.5”/b) (l.l”,O) (1.7%)
3. Metastases Breast Colon Larynx Other
69 26 19 13 11
(9.3%) (3.5 “R~) (2.5”~) (1.7”;) (1.59”)
745 (loo?;)
Total
* Includes cases with nodular intrapulmonary lesions and/or diffuse interstitial involvement proved to be lymphomatous, with or without present extrapulmonary disease.
TABLE
3
Diagnostic
results by TAB in lung lesions (n = 984)
1. Type of malignancy specified Bronchogenic carcinoma Other malignant neoplasms Metastases
644 (65.4jjb) 32 (3.2%) 69 (7.0%)
2. Type of malignancy not specified Malignancy
24 (2.40/h)
3. Non-neoplastic conditions False negative Benign neoplasms Infections Other Not verified
49 18 87 :!l Ill
4. No diagnosis Inadequate material
29 (2.9%)
(5.0%) (1.8:/,) (8.8%) (2.4%) (1.1:;)
100 TABLE 4 Diagnostic
TABLE results by TAB in mediastinal
1. Type of malignancy specified Bronchogenic carcinoma Lymphoma Other malignant neoplasms
lesions (n = 62)
Diagnostic value of the TAB in the lung related to lesion depth and size (n = 984)
31 (50.0%)
0 (0.0%)
3. Non-neoplastic conditions False negative Benign neoplasms Inflammatory disease Hematoma Not verified
0 3 2 4
4. No diagnosis Inadequate material
5 (8.1%)
No. of cases (n = 984) n
%
Central Peripheral Diffuse
327 585 72
33.2 59.4 7.3
B. Size
No. of cases (n = 912)*
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
87.0 96.0 99.1
100 100 100
78.2 90.1 78.1
Sensitivity (%)
Specificity
Accuracy
(%)
(%)
71.2 94.7 97.2 97.3
100 100 100 100
56.3 89.1 91.3 89.1
7 (11.3%) (0.0%) (4.8%) (3.2%) (6.4%)
benign lesions and the false-negative diagnoses of malignancy. This group is detailed in Table 5. No adequate material was available in order to give a diagnosis in 29 cases of the pulmonary TABS (2.9%) and in 5 cases (8.1%) of the mediastinal TABS. In 4 1.3% of all those cases without material, a pulmonary or mediastinal tumour was later confirmed, 5 1.7y0 were inflammatory processes. We have studied the diagnostic value of the TAB (sensitivity and specificity) relating to several factors, such as size and location of the lesion, type of needle and number of needle passes. The findings are shown in Tables 4-8.
(cm)
l-2 2-5 5-10 > 10
n
%
87 595 153 71
9.5 65.2 16.7 8.4
* Diffuse lesions are not included.
There were no major complications due to the use of the technique. The most common complication was pneumothorax, observed in 138 cases (13.2%). It was necessary to place an endothoracic tube in only 8 of these (0.8% of all biopsies). 37 pneumothoraces (26.8%) were detected on 6 hours delayed follow-up TABLE
7
Diagnostic value of the TAB in lung and mediastinum needle type
5
Non-neoplastic
A. Location
6 (9.7%) 4 (6.4%)
2. Type of malignancy not specified Malignancy
TABLE
6
conditions
1. False negative Squamous cell carcinoma Small cell undifferentiated
- diagnosis in TAB of the lung (n = 187) 49 (26.2%) 35 (18.7%) carcinoma
Adenocarcinoma Large cell carcinoma Undifferentiated carcinoma Bronchoalveloar carcinoma
6 4 3 1 9
(3.2%) (2.1%) (1.6%) (0.5%) (4.8%)
2. Inflammatory diseases Tuberculosis
87 (46.5%) 29 (15.5%)
Cryptococcosis Legionellosis Other
5 (2.7%) 8 (4.3%) 45 (24.1%)
3. Not verified
11 (5.9%)
1. Lung (n = 984) Type of needle
Chiba Franseen Westcott Rotex Other
No. of cases n
%
516 296 106 54 12
52.4 30.1 10.8 5.5 1.2
2. Mediastinum
(n = 62)
Type of needle
No. of cases n
4. Benign neoplasms and cyst
18 (9.6%)
5. Other
21 (11.2%)
related to
Chiba Franseen
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
95 95 88 75 80
100 100 100 100 100
88.6 88.6 65.9 68.7 66.6
Sensitivity
Specificity
Accuracy
(%)
(%)
(%)
88.0 88.8
100 100
70.9 80.0
% 38 24
61.3 38.7
101
TABLE
8
Diagnostic value of the TAB related to number of needle passes (n = 1046) No. of passes
1 2 3 References
No. of cases Sensitivity -_%) n
0, /o
258 462 326
24.1 44.2 31.2
(see separate
87.2 93.2 91.2
(%)
Specificity
Accuracy (%)
100 100 100
68.9 89.6 65.9
sheet).
radiographs. Self-limited hemoptyses were found in 12 patients (1.1%) and small peripheral alveolar infiltrations on chest radiograph, due to parenchymal haemorrhage, in 8 (0.8%). The rate of hemoptyses was much higher with Rotex needles (6.2%). 59 patients (5.6%) complained of chest pain or discomfort during or after the procedure. It was relieved by simple oral analgesics (Nolotil). There were no complications following the accidental biopsy of the 3 patients with hydatid cysts. The average hospital stay following TAB was 26.8 hours and the average cost of employing this technique in our hospital was $ 340 (41,000 pesetas). Discussion The diagnostic accuracy of TAB is variable. According to different authors, its sensitivity ranges from 72% [ 1 l] to 97% [ 121. Positive results provided by TAB depend on aspects inherent in the lesion, such as its benign or malignant nature, size and location, technical devices (type of imaging-guide and needle and number of needle passes) and finally, those related to human factors (the skill and experience of the medical staff and the co-operation of the patient) [ 13-171. In our series, sensitivity was higher in peripheral than in central lesions (96% and 86%, respectively) and much higher in lesions larger than 2 cm (94% vs. 70% in smaller ones). In the present group of 984 pulmonary lesions, we have achieved a level of accuracy for the diagnosis of malignancy of 93.8x, somewhat above the level we obtained early in our experience [ 181 when employing the same technique (87% in 247 TABS). In the mediastinum, overall sensitivity was 88 % and accuracy 74.8%, similar to the percentages reported by others [ 19-211. Considering the type of needle used, aspiration biopsies performed in our series with Chiba and Franseen needles showed a similar sensitivity (95%) being higher than that achieved with other types of
needle. Each author appears to achieve his best results using the tools with which he has more experience [ 22-241. Many types of needle have been introduced in order to improve results and reduce complications. Publications to which we referred on the subject of abdominal biopsies show that, although the size of the sample obtained is different depending on the type of needle, the quality and the degree of artefact are determined by the calibre of the needle [25]. Wittemberg [26] could not find any difference which implied an important advantage in his study of several types of 22 G needle. We do not think that there is any reason which prevents us from transferring this conclusion to thoracic biopsies, with respect to diagnostic results, if we put to one side the risk of pneumothorax. In our group, sensitivity increased from 86.8% with a single pass to 95.8% with three passes. Immediate microscopic assessment of the cytological quality of the samples improves the efficiency of the technique, decreasing the need for repeated passes and avoiding unnecessary risks [ 271; however, this was not the case in all series [28]. We only used this quick evaluation by the cytologi.st (working in the same X-ray department) in selected cases, where there was at least one previous negative biopsy. We had no false-positive results, either in the lungs or mediastinum. Specificity of the technique and the predictive value of a positive result were 100%. Fluoroscopy is the most suitable imaging procedure for guidance in most cases of TAB of the lung, for both economic and technical reasons. It is generally available and provides real-time imaging of the lesions during the biopsy. However, CT has been shown to be extremely effective for the location and biopsy of small lesions, which are either close to the hilium or to the mediastinum, or which are invisible on fluoroscopy, even though the patient is lying in the most appropriate decubitus for biopsy [29-301. As with CT, ultrasonography also provides valuable diagnostic information about the nature of the lesion, provided that it makes contact with the chest wall. The information obtained by this method can make puncture inadvisable or even contraindicated (as in the case of cystic lesions in patients with clinically or biologically suspected hydatid disease). However, sonography is not useful for guidance at TAB. Theoretically, one could use it to biopsy pleural masses hidden by a pleural effusion, but in such cases, aspirated fluid is suitable material for cytological diagnosis. The value of a non-invasive diagnostic technique depends on the balance between its diagnostic efficien-
102
cy and its safety [lo]. Fatal complications following TAB are extremely rare and are usually due to massive pulmonary haemorrhage and air embolism. Pleural or pulmonary infection and tumour spread through the biopsy needle track are also exceptional [9,31,32]. We have observed none of these complications in our series. If we do not take into account the obvious influence of experience with the technique shown by the radiologist who performs the TAB, then the frequency and degree of complications are essentially determinded by the calibre of the needle, as well as by its design [6,32]. Our overall rate of hemoptyses was low, but it reached 6.2% with the Rotex needle. Pneumothorax is the most frequent complication following TAB. General agreement exists in the literature about three factors which seem to be directly involved in the appearance of pneumothorax after TAB. These are: the presence of objective criteria of chronic obstructive pulmonary disease (estimated by pulmonary function tests) [33], the number of passes and the type and calibre of the needle. Probably, factors such as the size and location of the lesion and the availability of quick cytological examination of samples also have an influence over the risk of post-biopsy pneumothorax, because the number of needle passes varies [ 15,27,28]. We have observed a noticeable decrease in our current percentage of pneumothorax with respect to the first group (23% in 247 TABS), in which three attempts were systematically and habitually made. We have established severe haemorrhagic diathesis and suspected hydatid disease as absolute contraindications of TAB (nevertheless, we have accidentally biopsied three hydatid cysts without later complications). We also consider severe emphysema, pulmonary hypertension and a non-cooperative patient as relative contraindications. Timing for control chest radiographs and clinical follow-up after TAB have been the subject of discussion in the literature [ 341. Several authors report a considerable experience of TAB on non-hospitalized patients, without increasing the number of complications or their severity [35,36]. Patients must be warned not to move any significant distance from the hospital and that they should return to it if symptoms occur. Out-patient biopsy is a safe procedure which reduces hospital charges. In contrast to other series, 26.8% of pneumothoraces in our study were only detectable on subsequent radiographs, taken 6 hours after biopsy. None of them, however, had need of treatment and it is likely that its lack of diagnosis would have had no further consequences but, because of that possibility, we admit
patients on the morning of the biopsy and do not discharge them before 6 or 8 hours after having concluded :+ IL.
Surgical placing of a traditional endothoracic tube is not necessary in every patient with a severe pneumothorax, who needs treatment. According to several reports [8,38] in many cases, aspiration by means of a thin 9 F percutaneous catheter connected to a Heimlich valve [ 371 permits a quick, simple and safe treatment by the radiologist. We have no experience with this procedure, however. In our series, percutaneous puncture only produced slight chest pain or discomfort in 5.6% of cases; overall TAB has a good acceptance by patients. We think that this fact, which has not previously been reported in the literature, implies an important advantage for TAB over other techniques of thoracic biopsy, such as bronchoscopy, and contributes to its establishment and acceptance within the medical community. Diagnostic accuracy of TAB can be compared to that of bronchoscopy, but percutaneous biopsy is especially effective in diagnosis of small peripheral lesions and of those that do not originate from the airways [ 391. The impact of biopsy on patient management and its economic implications are undoubted [ 40,4 11. One TAB requires only cheap instrumentation and uses up a very small share of the working time of an X-Ray telecommanded unit (biplanar fluoroscopy is not routinely needed). TAB decreases both the need for a diagnosis by thoracotomy as well as the time from admission to diagnosis. Therefore, it reduces the time of stay at hospital when carried out on a hospitalized patient; but in any event, there are many cases where TAB can be performed on out-patients, thus decreasing costs without decreasing the safety and utility of the procedure. References 1 Leyden 00. Uber infektiose Pneumonie. Dtsch Med Wchr 1883; 9: 52-56. 2 Menetrier P. Cancer primitif du poumon. Bull Sot Anat Paris 1886; 4: 643. 3 Stewart FW. The diagnosis of tumours by aspiration. Am J Path01 1933; 9: 801-803. 4 Soderstrom N. Identification of normal tissues and tumors by cytologic aspiration biopsy. Acta Sot Med Uppsala 1958; 63: 53-58. 5 Nordenstrom B. A new technique for transthoracic biopsy of lung changes. Br J Radio1 1965; 38: 550-553. 6 Zavala DC, Bedel GN. Percutaneous lung biopsy with a cutting needle. An analysis of 40 cases and comparison with other biopsy techniques. Am Rev Respir Dis 1972; 106: 186-193. 7 Zornoza J, Snow J, Lukeman JM, Libshitz HI. Aspiration biopsy of discrete pulmonary lesions using a new thin needle. Radiology 1977; 123: 519-520.
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