FROM THE DEPARTMENT OF DIAGNOSTIC RADIOLOGY, KAROLINSKA SJUKHUSET, S-10401 STOCKHOLM, SWEDEN.
COMPLICATIONS OF PERCUTANEOUS TRANSTHORACIC NEEDLE ASPIRATION BIOPSY W. N. SINNER Since LEYDEN as early as 1883 performed percutaneous lung puncture in order to diagnose microorganisms in pneumonia and MENETRIER in 1886 for the first time diagnosed a pulmonary carcinoma by transthoracic aspiration, the method became widely used during the end of the 19th and the beginning of the 20th century. However, the lack of adequate equipment and visual controlled to major complications. The enthusiasm for this method was also lessened since it was considered to involve risks for tumour cell spread and air embolism (OCHSNER & DEBAKEY 1939). In spite of technical improvement (SILVERMAN 1928, MARTIN & ELLIS 1934) and favourable results (SAPPINGTON & FAVORITE 1936, ROSEMOND et coIl. 1949, LAUBY et colI. 1965) the method was not generally accepted for a long time. Out of fear for complications, some authors suggested its limited use for relatively large, inoperable lesions near the pleura (WIKLUND 1951, DUTRA & GERACI 1954, GRUNZE 1955, PERTTALA 1959). Others (CRAVER & BINKLEY 1939) stated that needle biopsy should not be applied when bronchoscopy or lymph node biopsy could be performed and not until three cytologic sputum examinations had failed to give a positive diagnosis. However, during the last decade, transthoracic percutaneous needle aspiration biopsy has been increasingly accepted as a standard method for the diagnosis of possibly malignant pulmonary lesions for four reasons: (1) improved radiologic technique permitting direct control of the biopsy procedure by television fluoroscopy, (2) advances in, and increased acceptance of, cytologic diagnosis, (3) application of Submitted for publication 30 September 1975. Acta Radiologica Diagnosis 17 (1976) Fasc. 6 November
52 - 765835
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Table 1 Complications of needle biopsy reported in the literature Complication
Reference
Frequency
Pneumothorax
CASTELAIN et coil. (1971) LAUBY et coll. (1965) WEILL et coil. (1970) JOHNSSON & SCHNURER (1971) THORNBURY & WALLS (1973) FONTANA et coll. (1970) THORNBURY & WALLS (1973) CASTELAIN et coIl. (1971) LAUBY et coIl. (1965) JAMESON (1970) THORNBURY & WALLS (1973) LALLI et coil. (1967) DUTRA & GERACI (1954)
None in most cases. A few required 0% 6.1 % aspiration of air (1.4 to 17 %) or chest tube drainage 15% 16.9% 27% 57% 5% 1.25% None. Stopped in all cases within 30 minutes 3.2% 6.0% 7.0% 10.0% 1 case Biopsy performed with Vim-Silverman needle 1 case Biopsy performed with Vim-Silverman needle 2 cases Pathologists differ in opinion on cytologic findings of pleural fluid
Local bleeding Hemoptysis
Implantation of malignant cells WOLINSKY & LISCHNER (1969) into the needle track Spread of tumour BERGER et coIl. (1972) cells to the pleura JAMESON (1970) Air embolism WESTCOTT (1973) ADAMSON & BATES (1967) Mortality
MEYER et colI. (1970) LAUBY et coll. (1965)
WOOLF (1954) WESTCOTT (1973)
JOHNSSON & SCHNURER (1971)
Treatment
0.02% 1 case Patient died 1 case Performed with Vim-Silverman needle. Autopsy revealed pulmonary haemorrhage 1 case Autopsy revealed pulmonary haemorrhage 3 cases Only 1 death directly attributed to the biopsy (untreated tension pneumothorax) 1 case Death due to air embolism 1 case Death due to air embolism (radiographically and pathologically confirmed) 1 case No cause of death found at autopsy
fine needles and (4) improved control of complications. Since NORDENSTROM introduced a technique employing these features into clinical use in 1961, the method has been revitalized. In a monograph, DAHLGREN & NORDENSTROM (1966) summarized the experience during the years 1963 and 1964. Additional impetus was given by the introduction of transjugu1ar paraxiphoid and paravertebral approaches for mediastinal needle biopsy (NORDENSTROM 1967a, b, 1972).
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Table 2 Rate of complications in 2 726 cases
Complication
Frequency
Treatment
Pneumothorax
27.2%
Asymptomatic: observation Symptomatic: exsufflation, chest tube drainage
16.9%
None (resorption in 1-2 weeks)
Local bleeding 20--29 years Whole series Hemoptysis Puncture near hilum Other regions Implantation metastasis into needle track Spread of tumour cells or infection to the pleura Air embolism
Other complications Bilateral pneumothorax Pneumothorax with subcutaneous emphysema Mediastinal emphysema Bleeding Mortality
11%
5% 2%
None
1 case
Extirpation
o 2 possible cases
Vasodilating drugs in one case; the other recovered spontaneously without sequelae
4 cases 7 cases
Exsufflation None
2 cases 1 case
None None
o
Experimental and clinical application of fine needle technique (FRANZEN 1968, DAHLGREN & NORDENSTROM) demonstrated that major complications are rare or entirely absent. The indications for transthoracic biopsy were therefore widened.
Material The complications as reported in the literature are listed in Table 1. Using the technique of DAHLGREN & NORDENSTROM, LALLI et colI. (1967), WALLS et coll, (1970), CASTELAIN et coll. (1971), THORNBURY & WALLS (1973) and others reported no complications other than pneumothorax, hemoptysis and local bleeding, which rarely had to be treated. However, only comparatively small series have previously been analysed for complications. Based on results from the major part of the personal series, the significance of percutaneous transthoracic biopsy in small peripheral and mostly asymptomatic pulmonary lesions with a diameter of less than 2 cm was previously reported (SINNER 1973). In 302 of 2450 patients such lung lesions appeared, 196 (64 %) of which were cytologically classified as benign (chronic inflammatory process including tuber-
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culosis 77, tuberculoma 69, hamartoma 30, bronchial adenoma 11, neurilemmoma 3, chondroma 2, Wegener's granulomatosis 2, aspergillosis 1, plasma cell granuloma 1), while 106 (36 %) yielded cytologic evidence of malignancy (primary bronchogenic carcinoma 58, solitary lung metastasis with extra-pulmonary primary tumour 30, cytologically undecided whether primary or secondary 18). The number and type of complications in small lesions did not differ significantly from those of larger lesions but a more detailed analysis of the complications was not made. Since the previous report the material has increased to 5 300 needle biopsies on 2 726 patients in 3 799 clinical visits. This material is now evaluated with respect to factors influencing risks and complications in needle aspiration biopsy and how to define indications in order to get the maximum benefit out of this method with improved control of complications. Technical variations, which have to be distinguished from the method of DAHLGREN & NORDENSTROM, and which are not discussed in the present report, include (1) the use of the Vim-Silverman needle, the Jack needle or other large bore needles, (2) trephine biopsy using a high speed air drill, (3) open biopsy by thoracotomy. These and similar methods yield tissue specimens for microscopy rather than a cellular aspirate for cytologic analysis. Results In 46.4 % of the total material there was cytologic evidence of malignancy, in 9.8 % of benign tumours or pseudo tumours, in 7.4 % of granulomas of different nature, in 22.5 % of inflammatory lesions, non-specific or specific, and in 1.2 % of other lesions. A cyst was punctured in 1.6 %. In 9.3 % no cytologic diagnosis was possible. The result of the cytologic examination agreed well with the microscopic findings at operation or autopsy. Compared to previous series (SINNER 1973) a relatively larger fraction of malignant lesions was found in the total material (36 % against 46 %) since the nature of small lung lesions is more difficult to assess than larger lesions, infiltrating or with metastases. The present report of the complete series (1961 to 1974) includes the complications previously reported on parts of the material (DAHLGREN & NORDENSTROM, SINNER 1973); they are listed in Table 2. Pneumothorax. The incidence of pneumothorax in the total material related to the number of patients was 27.2 per cent and to hospital visits 18.0 per cent (Fig. 1). The number of puncture procedures could vary from 1 to 5 per hospital visit on an outpatient basis, but was most often 2. As the number of the procedures was not always recorded the corresponding mean percentage of pneumothorax could not be established precisely. However, from the cases where the number of punctures was known, a factor of 1.4 punctures per hospital visit could be calculated. Using this figure, the frequency of pneumothorax related to the number of procedures in the total material can be extrapolated to 12.9 per cent (Fig. 1). Most of these cases were asymptomatic.
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PNEUMOTHORAX
Fig. 1. Relative frequency of pneumothorax in 2 726 patients. ABC in relation to total number of patients, 27.2 %. AB in relation to hospital visits 18 %. A in relation to number of biopsies 12.9 %.
The patients were observed until the air had been completely resorbed. The number of pneumothorax cases being symptomatic or requiring active treatment by simple exsufflation of air or by using a chest tube drainage was 7.7 per cent. The factors influencing the incidence of pneumothorax are presented in Table 3 and Figs 6 and 7. Fig. 2 illustrates the increasing rate of pneumothorax with age. A statistically significant difference in the relative frequency between men and women (X2 test, p 0.05), except that pneumothorax was more frequent with increasing depth of the lesions (Fig. 4). However, a significant difference was found between lung lobes and mediastinum (p < 0.001) and between mediastinum and pleura (p
90 years
Fig. 6
Fig. 5. Frequency of pneumothorax in relation to the outer diameter of the needle and one or two repunctures related to number of patients. 0 first, ~ second, 1m! third biopsy. Fig. 6. Relative frequency in different age groups of pneumothorax requiring treatment in per cent of the entire material. - - pneumothorax in relation to all treatments.. _._. pneumothorax requiring exsufflation. --- pneumothorax requiring chest tube drainage. Po,
Pe,
Cent
c.nt
60
100
90 80
r;:'.
rn
m m
ill ill ill ill
70
il illTI
50
/
/
40
60
-:
30
50 40
20 30
20 10
~ 30-39
~
40-49
~
50-59
~
60-69
~
70-79
~
80-89 Years
-'~ .- -
"I
--
40
-
,, _/
,
---' ,
~.-
_.... 60
60
70
80 V."ra
Fig. 7 Fig. 8 Fig. 7. Relation of asymptomatic and untreated pneumothorax (~I) to pneumothorax requiring treatment (1m) in different age groups. Fig. 8. Correlation between combined factors (size and depth of lesion) and relative frequency of pneumothorax in different age groups (l 500 patients). - - lesions < 2 cm diameter and > 12 em depth. - ' - lesions> 2 em diameter and> 12 depth. ---lesions> 2 ern diameter and < 12 em depth.
Mortality. In this series there was no death which could be attributed to the method. In a 70-year-old man with a previous history of myocardial infarction, there was evidence of an acute myocardial infarction when the patient after a complication-free procedure was under transportation back to the ward; he improved spontaneously. An elderly man with emphysema was subjected to biopsy, performed with the same technique elsewhere and consequently not part of the present series. This patient
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probably developed an unrecognized tension-pneumothorax and died untreated. This mimicks a case reported by LAUBY et colI.; both seem to have been potentially preventable deaths. Thus, it seems that using the present fine needle technique with facilities available for treatment of complications mortality for all practical purposes should be nil. Discussion
The incidence of pneumothorax depends on the condition of the patient and on the technique used but also on the extent with which complications are searched for. This may partly explain the wide range of post-puncture pneumothorax in other reports. In the present series all cases of pneumothorax were included, even those with only 1 to 2 mm of air apically in asymptomatic pneumothorax, or those with pneumothorax not visible immediately after the procedure, but present from several hours up to several days later. Cases with paraxiphoid, transjugular and paravertebral approach were not included (JEREB & SINNER 1973) as they require other techniques (introduced by NORDENSTROM 1967, 1972). The incidence of pneumothorax in such cases for all practical purposes should be nil, as normally the pleura is not punctured. Local bleeding occurred in 11 per cent but was of no clinical importance and in no case required any measures. Hemoptysis occurred in about 5 per cent of the centrally situated lesions but rarely in the peripheral ones (2 per cent of total material). Implantation of malignant cells into the needle track, spread of tumour cells to the pleura, spread of infection and air embolism have been arguments against the use of transthoracic biopsy as a routine diagnostic procedure. Previous reports, based on altogether several thousands of procedures have shown these complications to be very rare. Only 2 instances of needle track implantation have been reported; both after use of large bore needles. Spread of infection also seems to be very rare and can be controlled by modern chemotherapy. Air embolism is a rare, although life-threatening possibility; certain precautions should therefore be taken. Mortality, apparently very rare, should be avoidable if the present technique with fine needles is used properly and if facilities are available for the immediate treatment of complications, especially symptomatic pneumothorax. The present review of complications shows that three main problems may be distinguished. Pneumothorax is the most frequent and practically most important complication of needle biopsy. As was shown in the foregoing, age and sex, the size and depth of the lesions, repunctures, special conditions and diseases, and last but not least experience of the operator influence the relative frequency and the degree of pneumothorax. Awareness of these factors is of practical significance as later developing major complications with potential mortality, like tension-pneumothorax, must be recognized in time and treated adequately.
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Implantation of tumour cells into the needle track seems to be a rare possibility (about 0.04 per cent). In a recently published survey (SINNER 1973) of a major part of the present material the author analysed 106 operated patients with peripherally situated malignant lung lesions under 2 em of real size, all diagnosed at an early stage. The 5-year survival rate was 42 per cent for primary carcinoma and 32 per cent for solitary metastases of extrapulmonary tumours. These results, which may well be compared with those of other reports, indicate that if spread of tumour cells exists, it is of minor importance and more than out-weighed by the advantages of early diagnosis and treatment of pulmonary malignant lesions. MOORE et coll. (1967) and ROBERTS et coll. (1962) have pointed out that diagnostic and therapeutic procedures favour tumour cell spread. Many authors have stated that malignant tumours, not only in the lungs, continuously disseminate tumour cells into the blood stream (SANDBERG et coll. 1959, SINNER & SCHINZ 1964, SINNER 1963, and others). ROBERTS et coil. found tumour cells in the blood in 108 patients with different tumour localizations in 48 per cent before, during and after operation and in 17 per cent only during operation. They also found a significant increase of tumour cells in the blood after manipulations like rectal or gynaecologic examinations, intensive washing of the tumour area (in mammary tumours) and in diagnostic procedures like bone biopsy and curettage of the uterus. However, ENGELL (1955) found malignant cells in blood samples from the tumour area about as often in patients surviving without evidence of recurrence or metastases as in those who developed recurrence or metastases and concluded that this test provided no significant information of prognosis. It may be concluded that in most cases malignant cells entering the blood stream are destroyed. Recently ENGZELL et coil. (1971) investigated the possibility of spread of tumour cells in connection with aspiration biopsy of lymph node metastasis in animal experiments (18 gauge needles) and in a clinical series of 157 patients with pleomorphic adenoma of the salivary glands and of 469 patients with prostatic carcinoma, all diagnosed by fine needle (22 gauge) biopsy. No evidence emerged of local extension of tumour growth or appearance of metastases attributable to the biopsy. Thus, there would seem to be no ground for fear of tumour spread following transthoracic biopsy, resulting in transformation of an early operable lesion into an inoperable or incurable state. Air embolism. In the past air embolism was a well recognised complication of thoracocentesis and therapeutic pneumothorax. Apart from cases in which air is directly introduced into the lung, air embolism is theoretically possible (1) if the tip of the needle is positioned in a pulmonary vein and (with removed mandrin) the atmospheric pressure exceeds the pulmonary venous pressure as might occur under a rapid inspiration, and (2) if an open communication has become established between a bronchus or air space of the lung; in a rigid lung air might be blown into the vein during a coughing episode.
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WESTCOTT (1973) recently described one such case of air embolism with radiographic and pathologic documentation. As this case seems to be the only one strictly documented, air embolism appears to be an extremely rare complication in transthoracic biopsy. In some other cases there is circumstantial clinical evidence rather than pathologic proof. Based on the present material, the relative risk per patient is then estimated to be about 0.07 per cent. However, the incidence may be further reduced or avoided if precautions are taken to warrant that the intrathoracic pressure will exceed the atmospheric pressure. Positive pressure breathing and a Valsalva manoeuver seem not to be practical measures. It is mandatory that patients should not be examined in a half-recumbent or upright position. The open needle should not be left for any length of time in situ if venous blood is obtained. After the needle has reached its definite position the syringe has to be connected without delay after the stylet has been removed. Since a sudden inspiration after an apnoea or a coughing episode might favour that the atmospheric pressure exceeds the pulmonary venous pressure, the patient should breathe normally during the procedure and only thin needles should be used. It may be concluded that few complications occur following needle aspiration biopsy if the procedure is carefully planned and performed on strict indication.
SUMMARY After 5 300 percutaneous transthoracic needle aspiration biopsy procedures in 2 726 patients pneumothorax occurred in 27.2 per cent of the patients. Only 7.7 per cent required exsufflation or drainage. The factors influencing the relative frequency and the severity of pneumothorax are discussed. Bleeding around the punctured lesions was found in 11 per cent, and hemoptysis in 2 per cent but were of no clinical importance. In one case evidence of needle track implantation was found. The theoretical and practical importance of tumour cell spread and spread of infection through the needle track is discussed. No air embolism or mortality occurred.
ZUSAMMENFASSUNG Bei 5 300 perkutanen transthorakalen Nadelaspirationsbiopsien an 2 726 Patienten trat bei 27,2 % der Patienten ein Pneumothorax auf. Nur 7,7% benotigten eine Absaugung der Luft oder eine Drainagebehandlung. Es werden die Faktoren, die die relative Frequenz und den Schweregrad des Pneumothorax ausmachen, besprochen. Eine Blutung urn die Punktionswunde wurde in 11 % beobachtet und Harnoptysen in 2 %; sie waren jedoch ohne klinische Bedeutung. In einem Fall wurden Zeichen einer Implantation im Stichkanal gefunden. Die theoretische und praktische Bedeutung der Streuung von Tumorzellen und Infektionen durch den Stichkanal werden diskutiert. Es traten keine Luftembolien oder Todesfalle auf.
RESUME Apres 5 300 biopsies transthoraciques percutanees a l'aiguille avec aspiration chez 2 726 malades, un pneumothorax est apparu dans 27,2 pour cent des cas. L'exsufflation au Ie
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drainage n'ont ete necessaires que dans 7,7 pour cent. L'auteur examine les facteurs qui influent sur la frequence relative et la gravite des pneumothorax. II y a eu un hematome autour des lesions ponctionnees dans 11 pour cent des cas et une hemoptysie dans deux pour cent mais elles n'ont pas eu d'importance clinique. Dans un cas il y a eu des signes de greffe tumorale Ie long du trajet de l'aiguille. L'auteur examine I'importance theorique et pratique de la dissemination de cellules tumorales et d'infection par Ie trajet de I'aiguille. II n'ya pas eu d'embolie gazeuse ni de mort.
REFERENCES ADAMSON JR J. S. and BATES J. H.: Percutaneous needle biopsy of lung. Arch. intern. Med. 119 (1967), 164. BELCHER J. R.: Pulmonary lesions simulating carcinoma. Acta chir. belg, Suppl. 11 (1955), 28. BERGER R. L., DARGAN E. L. and HUANG B. L.: Dissemination of cancer cells by needle biopsy of the lung. J. thorac. cardiovasc. Surg. 63 (1972), 430. BOYLEN C. T., JOHNSON N. R., RICHTERS V. and BALCHUM O. J.: High speed trephine lung biopsy: Method and results. Chest 63 (1973), 59. CASTELAIN G., CASTELAIN C. et PRETET S.: La ponction transparietale en pneumonologie. J. franc. Med. Chir. thorac. 25 (1971), 91. CHATTENBERG H. J. and ZISKIND J.: Air embolism as a complication of artificial pneumothorax. Amer. J. clin. Pathol. 9 (1939), 477. CRAVER F. L. and BINKLEY J. S.: Aspiration biopsy of tumours of the lung. J. thorac. Surg, 8 (1939), 436. DAHLGREN S.: Aspiration biopsy of intrathoracic tumours. Acta path. microbiol. scand. 70 (1967), 566. - and NORDENSTROM B.: Transthoracic needle biopsy. Year Book Medical Publ., Chicago 1966. DUTRA F. R. and GERACI C. L.: Needle biopsy of the lung. J. Amer. med. Ass. 155(1954), 21. ENGELL H. c.: Cancer cells in the circulating blood. Acta chir. scand. (1955) Suppl, No. 201. - Cancer cells in the blood. Ann. Surg. 149 (1959), 457. ENGZELL D., ESPOSTI P. L., RUBIO C., SIGURDSON A. and ZAJICEK J.: Investigation on tumour spread in connection with aspiration biopsy. Acta radiol. Ther. Phys. BioI. 10 (1971), 385. FONTANA R., MILLER W., BEABOUT J., PAYNE W. and HARRISON JR E.: Transthoracic needle aspiration of discrete pulmonary lesions. Experience in 100 cases. Med. Clin. N. Amer. 54 (1970), 961. GRUNZE H.: Klinische Zytologie der Thoraxkrankheiten. Ferdinand Enke Verlag, Stuttgart 1955. JAMESON J. B.: Aspiration biopsy of localized intrathoracic lesions. Aust. Radiol. 14 (1970), 40. JEREB M. and SINNER W.: Some special procedures in chest disease. Radiol. Clin. N. Amer. 11 (1973), 109. JOHNSSON K. och SCHNURER L. B.: Resultatav punktionscytologi vid utredning av lunginfiltrat. (In Swedish.) Nord. Med. 86 (1971), 1288. LALLI A. F., NAYLOR B. and WHITEHOUSE W.: Aspiration biopsy of thoracic lesions. Thorax 22 (1967), 404.
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LAUBY V. W., BURNETT W. E., ROSEMOND G. P. and TYSON R. R.: Value and risk of biopsy of pulmonary lesions by needle aspiration. J. thorac. cardiovasc. Surg. 49 (1965), 159. LEYDEN O. 0.: Uber inlektiose Pneumonie. Dtsch. med. Wschr. 9 (1883), 52. MARTIN H. E. and ELLIS E. B.: Aspiration biopsy. Surg, Gynec. Obstet, 59 (1934), 578. MENETRIER P.: Cancer primitif du poumon. Bull. Soc. Anat. Paris 11 (1886), 643. MEYER J. E., FERRUCCI JR. J. T. and JANOWER M. L.: Fatal complications of percutaneous lung biopsy. Radiology 96 (1970), 47. MOORE G. E., SANDBERG A. A. and SCHUBARG J. R.: Clinical and experimental observations of the occurrence and fate of tumor cells in the blood stream. Ann. Surg. 146 (1957),580. NORDENSTROM B.: A new technique for transthoracic biopsy of lung changes. Brit. J. Radiol. 38 (1965), 550. - (a) Transjugular approach to the mediastinum for mediastinal needle biopsy. Invest. Radiol. 2 (1967), 134. - (b) Paraxiphoid approach to the mediastinum for mediastinoscopy and mediastinal needle biopsy. Invest. Radiol. 2 (1967), 141. - Paravertebral approach to the posterior mediastinum for mediastinoscopy and needle biopsy. Acta radiol. Diagnosis 12 (1972), 298. - Personal communication. - and KUMAZAKI T.: Aorta, heart and lung vessels in idiopathic pulmonary emphysema related to pulmonary function. Acta radiol. Diagnosis 15 (1974), 197. OCHSNER A. and DEBAKEY M.: Primary pulmonary malignancy. Treatment by total pneumonectomy. Analysis of 79 collected cases and presentation of 7 personal cases. Surg. Gynec. Obstet. 68 (1939), 435. OLIVER T.: Cases in which death or collapse occurred after exploratory puncture of the chest. Lancet 1 (1904), 26. OVERHOLT R. H.: Curability of primary carcinoma of the lung. Early recognition and management. Surg. Gynec. Obstet. 70 (1940), 479. PERTTALA Y.: Needle biopsy in the diagnosis of pulmonary tumour. Ann. Chir. Gynaec, Fenn. 48 (1959), 427. POLLAK M.: Air embolus. Amer. Rev. Tuberc. 28 (1933), 187. REYER G. W. and KOHL H. W.: Air embolism complicating thoracic surgery. J. Amer. med. Ass. 87 (1926), 1626. RIZK G. K. and TOMBE J.: Transbronchial and transthoracic biopsy of pulmonary lesions. J. med, liban. 24 (1971), 4. ROBERTS S., JONASSON 0., LONG L., MAcGREW E. A., MACGRATH R. and COLE W. H.: Relationship of cancer cells in the circulating blood to operation. Cancer 15 (1962), 232. ROSEMOND G., BURNETT W. E. and HALL J.: Value and limitations of aspiration biopsy for lung lesions. Radiology 52 (1949), 506. SANDBERG A. A., MOORE G. E. and SCHUBARG J. R.: 'Atypical' cells in the blood of cancer patients-differentiation from tumor cells. J. nat. Cancer Inst. 22 (1959), 555. SAPPINGTON S. W. and FAVORITE G.: Lung puncture in lobar pneumonia. Amer. J. med. Sci. 191 (1936), 225. SCHLAEPFER K.: Air embolism following various diagnostic or therapeutic procedures in diseases of the pleura and lung. Bull. Johns Hopk. Hosp. 33 (1922), 321. SILVERMAN I.: A new biopsy needle. Amer. J. Surg. 40 (1928), 671. SINNER W. N.: Wert und Bedeutung des Tumorzellnachweises im stromenden Blut. Praxis 44 (1963), 1343. - Transthoracic needle biopsy of small peripheral malignant lung lesions. Invest. Radiol. 8 (1973), 305.
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Wert und Bedeutung der perkutanen transthorakalen Nadelbiopsie fur die Diagnose intrathorakaler Krankheitsprozesse. Fortschr. Rontgenstr, 123 (1975), 197. - und SCHINZ H. R.: Metastasenstrassen. In: Ergebnisse der medizinischen Strahlenf'orschung, Band I, S. 415. Herausgegeben von H. R. Schinz, R. Glauner und A. Riittimann. Georg Thieme Verlag, Stuttgart 1964. - and ZAJICEK J.: Implantation metastasis after percutaneous transthoracic needle aspiration biopsy. Acta radio!. Diagnosis 17 (1976), 473. SMITH W. B.: Needle biopsy of the lung with special reference to diffuse lung disease and the use of a new needle. Thorax 19 (1964), 68. STEVENS G. M., WEIGEN J. F. and LILLINGTON G. A.: Needle aspiration biopsy of localized pulmonary lesions with amplified fluoroscopic guidance. Amer. J. Roentgeno!. 103 (1968), 561. SNEDECOR G. W.: Statistical methods. Jowa, 5th edition, pp. 190 and 227. 1956. TAYLOR J. D.: Post-mortem diagnosis of air embolism by radiography. Brit. med. J. 1 (1952), 890. THORNBURY J. R. and WALLS W. J.: Transthoracic pulmonary needle aspiration biopsy. 5 year experience at the UMMC 1966 to 1971. Unpublished report. TURNER A. F. and SARGENT E. N.: Percutaneous pulmonary needle biopsy-an improved needle for a simple direct method of diagnosis. Amer. J. Roentgeno!. 104 (1968), 846. VANCE, J. W., GOOD C. A., HODGSON c., KIRKIN J. W. and GAGE R. P.: The solitary circumscribed pulmonary lesion due to bronchogenic carcinoma: A 3 year follow-up study of 94 surgical treated patients. Dis. Chest 36 (1959), 231. WEILL F., LEDOUX A., OPPERMANN A., BONNEVILLE J. F., PREVOTAT N., RICATTE J. P. et JACQUEY S.: La ponction-biopsie pulmonaire transcutanee selon Dahlgren et Nordenstrom. Ann. Radio!. 13 (1970), 119. WESTCOTT J. L.: Air embolism complicating percutaneous needle biopsy of the lung. Chest 63 (1973), 198. WIKLUND T.: Bronchogenic carcinoma. Acta chir. scand. (1951) Suppl, No. 162. WOLINSKY H. and LISCHNER M. W.: Needle track implantation of tumor after percutaneous lung biopsy. Ann. intern. Med. 71 (1969),2. WOOLF C. R.: Applications of aspiration lung biopsy with review of literature. Dis. Chest 25 (1954), 286.
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COMPLICATIONS OF PERCUTANEOUS TRANSTHORACIC NEEDLE ASPIRATION BIOPSY W. N. SINNER Since LEYDEN as early as 1883 performed percutaneous lung puncture in order to diagnose microorganisms in pneumonia and MENETRIER in 1886 for the first time diagnosed a pulmonary carcinoma by transthoracic aspiration, the method became widely used during the end of the 19th and the beginning of the 20th century. However, the lack of adequate equipment and visual controlled to major complications. The enthusiasm for this method was also lessened since it was considered to involve risks for tumour cell spread and air embolism (OCHSNER & DEBAKEY 1939). In spite of technical improvement (SILVERMAN 1928, MARTIN & ELLIS 1934) and favourable results (SAPPINGTON & FAVORITE 1936, ROSEMOND et coIl. 1949, LAUBY et colI. 1965) the method was not generally accepted for a long time. Out of fear for complications, some authors suggested its limited use for relatively large, inoperable lesions near the pleura (WIKLUND 1951, DUTRA & GERACI 1954, GRUNZE 1955, PERTTALA 1959). Others (CRAVER & BINKLEY 1939) stated that needle biopsy should not be applied when bronchoscopy or lymph node biopsy could be performed and not until three cytologic sputum examinations had failed to give a positive diagnosis. However, during the last decade, transthoracic percutaneous needle aspiration biopsy has been increasingly accepted as a standard method for the diagnosis of possibly malignant pulmonary lesions for four reasons: (1) improved radiologic technique permitting direct control of the biopsy procedure by television fluoroscopy, (2) advances in, and increased acceptance of, cytologic diagnosis, (3) application of Submitted for publication 30 September 1975. Acta Radiologica Diagnosis 17 (1976) Fasc. 6 November
52 - 765835
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Table 1 Complications of needle biopsy reported in the literature Complication
Reference
Frequency
Pneumothorax
CASTELAIN et coil. (1971) LAUBY et coll. (1965) WEILL et coil. (1970) JOHNSSON & SCHNURER (1971) THORNBURY & WALLS (1973) FONTANA et coll. (1970) THORNBURY & WALLS (1973) CASTELAIN et coIl. (1971) LAUBY et coIl. (1965) JAMESON (1970) THORNBURY & WALLS (1973) LALLI et coil. (1967) DUTRA & GERACI (1954)
None in most cases. A few required 0% 6.1 % aspiration of air (1.4 to 17 %) or chest tube drainage 15% 16.9% 27% 57% 5% 1.25% None. Stopped in all cases within 30 minutes 3.2% 6.0% 7.0% 10.0% 1 case Biopsy performed with Vim-Silverman needle 1 case Biopsy performed with Vim-Silverman needle 2 cases Pathologists differ in opinion on cytologic findings of pleural fluid
Local bleeding Hemoptysis
Implantation of malignant cells WOLINSKY & LISCHNER (1969) into the needle track Spread of tumour BERGER et coIl. (1972) cells to the pleura JAMESON (1970) Air embolism WESTCOTT (1973) ADAMSON & BATES (1967) Mortality
MEYER et colI. (1970) LAUBY et coll. (1965)
WOOLF (1954) WESTCOTT (1973)
JOHNSSON & SCHNURER (1971)
Treatment
0.02% 1 case Patient died 1 case Performed with Vim-Silverman needle. Autopsy revealed pulmonary haemorrhage 1 case Autopsy revealed pulmonary haemorrhage 3 cases Only 1 death directly attributed to the biopsy (untreated tension pneumothorax) 1 case Death due to air embolism 1 case Death due to air embolism (radiographically and pathologically confirmed) 1 case No cause of death found at autopsy
fine needles and (4) improved control of complications. Since NORDENSTROM introduced a technique employing these features into clinical use in 1961, the method has been revitalized. In a monograph, DAHLGREN & NORDENSTROM (1966) summarized the experience during the years 1963 and 1964. Additional impetus was given by the introduction of transjugu1ar paraxiphoid and paravertebral approaches for mediastinal needle biopsy (NORDENSTROM 1967a, b, 1972).
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Table 2 Rate of complications in 2 726 cases
Complication
Frequency
Treatment
Pneumothorax
27.2%
Asymptomatic: observation Symptomatic: exsufflation, chest tube drainage
16.9%
None (resorption in 1-2 weeks)
Local bleeding 20--29 years Whole series Hemoptysis Puncture near hilum Other regions Implantation metastasis into needle track Spread of tumour cells or infection to the pleura Air embolism
Other complications Bilateral pneumothorax Pneumothorax with subcutaneous emphysema Mediastinal emphysema Bleeding Mortality
11%
5% 2%
None
1 case
Extirpation
o 2 possible cases
Vasodilating drugs in one case; the other recovered spontaneously without sequelae
4 cases 7 cases
Exsufflation None
2 cases 1 case
None None
o
Experimental and clinical application of fine needle technique (FRANZEN 1968, DAHLGREN & NORDENSTROM) demonstrated that major complications are rare or entirely absent. The indications for transthoracic biopsy were therefore widened.
Material The complications as reported in the literature are listed in Table 1. Using the technique of DAHLGREN & NORDENSTROM, LALLI et colI. (1967), WALLS et coll, (1970), CASTELAIN et coll. (1971), THORNBURY & WALLS (1973) and others reported no complications other than pneumothorax, hemoptysis and local bleeding, which rarely had to be treated. However, only comparatively small series have previously been analysed for complications. Based on results from the major part of the personal series, the significance of percutaneous transthoracic biopsy in small peripheral and mostly asymptomatic pulmonary lesions with a diameter of less than 2 cm was previously reported (SINNER 1973). In 302 of 2450 patients such lung lesions appeared, 196 (64 %) of which were cytologically classified as benign (chronic inflammatory process including tuber-
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culosis 77, tuberculoma 69, hamartoma 30, bronchial adenoma 11, neurilemmoma 3, chondroma 2, Wegener's granulomatosis 2, aspergillosis 1, plasma cell granuloma 1), while 106 (36 %) yielded cytologic evidence of malignancy (primary bronchogenic carcinoma 58, solitary lung metastasis with extra-pulmonary primary tumour 30, cytologically undecided whether primary or secondary 18). The number and type of complications in small lesions did not differ significantly from those of larger lesions but a more detailed analysis of the complications was not made. Since the previous report the material has increased to 5 300 needle biopsies on 2 726 patients in 3 799 clinical visits. This material is now evaluated with respect to factors influencing risks and complications in needle aspiration biopsy and how to define indications in order to get the maximum benefit out of this method with improved control of complications. Technical variations, which have to be distinguished from the method of DAHLGREN & NORDENSTROM, and which are not discussed in the present report, include (1) the use of the Vim-Silverman needle, the Jack needle or other large bore needles, (2) trephine biopsy using a high speed air drill, (3) open biopsy by thoracotomy. These and similar methods yield tissue specimens for microscopy rather than a cellular aspirate for cytologic analysis. Results In 46.4 % of the total material there was cytologic evidence of malignancy, in 9.8 % of benign tumours or pseudo tumours, in 7.4 % of granulomas of different nature, in 22.5 % of inflammatory lesions, non-specific or specific, and in 1.2 % of other lesions. A cyst was punctured in 1.6 %. In 9.3 % no cytologic diagnosis was possible. The result of the cytologic examination agreed well with the microscopic findings at operation or autopsy. Compared to previous series (SINNER 1973) a relatively larger fraction of malignant lesions was found in the total material (36 % against 46 %) since the nature of small lung lesions is more difficult to assess than larger lesions, infiltrating or with metastases. The present report of the complete series (1961 to 1974) includes the complications previously reported on parts of the material (DAHLGREN & NORDENSTROM, SINNER 1973); they are listed in Table 2. Pneumothorax. The incidence of pneumothorax in the total material related to the number of patients was 27.2 per cent and to hospital visits 18.0 per cent (Fig. 1). The number of puncture procedures could vary from 1 to 5 per hospital visit on an outpatient basis, but was most often 2. As the number of the procedures was not always recorded the corresponding mean percentage of pneumothorax could not be established precisely. However, from the cases where the number of punctures was known, a factor of 1.4 punctures per hospital visit could be calculated. Using this figure, the frequency of pneumothorax related to the number of procedures in the total material can be extrapolated to 12.9 per cent (Fig. 1). Most of these cases were asymptomatic.
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PNEUMOTHORAX
Fig. 1. Relative frequency of pneumothorax in 2 726 patients. ABC in relation to total number of patients, 27.2 %. AB in relation to hospital visits 18 %. A in relation to number of biopsies 12.9 %.
The patients were observed until the air had been completely resorbed. The number of pneumothorax cases being symptomatic or requiring active treatment by simple exsufflation of air or by using a chest tube drainage was 7.7 per cent. The factors influencing the incidence of pneumothorax are presented in Table 3 and Figs 6 and 7. Fig. 2 illustrates the increasing rate of pneumothorax with age. A statistically significant difference in the relative frequency between men and women (X2 test, p 0.05), except that pneumothorax was more frequent with increasing depth of the lesions (Fig. 4). However, a significant difference was found between lung lobes and mediastinum (p < 0.001) and between mediastinum and pleura (p
90 years
Fig. 6
Fig. 5. Frequency of pneumothorax in relation to the outer diameter of the needle and one or two repunctures related to number of patients. 0 first, ~ second, 1m! third biopsy. Fig. 6. Relative frequency in different age groups of pneumothorax requiring treatment in per cent of the entire material. - - pneumothorax in relation to all treatments.. _._. pneumothorax requiring exsufflation. --- pneumothorax requiring chest tube drainage. Po,
Pe,
Cent
c.nt
60
100
90 80
r;:'.
rn
m m
ill ill ill ill
70
il illTI
50
/
/
40
60
-:
30
50 40
20 30
20 10
~ 30-39
~
40-49
~
50-59
~
60-69
~
70-79
~
80-89 Years
-'~ .- -
"I
--
40
-
,, _/
,
---' ,
~.-
_.... 60
60
70
80 V."ra
Fig. 7 Fig. 8 Fig. 7. Relation of asymptomatic and untreated pneumothorax (~I) to pneumothorax requiring treatment (1m) in different age groups. Fig. 8. Correlation between combined factors (size and depth of lesion) and relative frequency of pneumothorax in different age groups (l 500 patients). - - lesions < 2 cm diameter and > 12 em depth. - ' - lesions> 2 em diameter and> 12 depth. ---lesions> 2 ern diameter and < 12 em depth.
Mortality. In this series there was no death which could be attributed to the method. In a 70-year-old man with a previous history of myocardial infarction, there was evidence of an acute myocardial infarction when the patient after a complication-free procedure was under transportation back to the ward; he improved spontaneously. An elderly man with emphysema was subjected to biopsy, performed with the same technique elsewhere and consequently not part of the present series. This patient
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probably developed an unrecognized tension-pneumothorax and died untreated. This mimicks a case reported by LAUBY et colI.; both seem to have been potentially preventable deaths. Thus, it seems that using the present fine needle technique with facilities available for treatment of complications mortality for all practical purposes should be nil. Discussion
The incidence of pneumothorax depends on the condition of the patient and on the technique used but also on the extent with which complications are searched for. This may partly explain the wide range of post-puncture pneumothorax in other reports. In the present series all cases of pneumothorax were included, even those with only 1 to 2 mm of air apically in asymptomatic pneumothorax, or those with pneumothorax not visible immediately after the procedure, but present from several hours up to several days later. Cases with paraxiphoid, transjugular and paravertebral approach were not included (JEREB & SINNER 1973) as they require other techniques (introduced by NORDENSTROM 1967, 1972). The incidence of pneumothorax in such cases for all practical purposes should be nil, as normally the pleura is not punctured. Local bleeding occurred in 11 per cent but was of no clinical importance and in no case required any measures. Hemoptysis occurred in about 5 per cent of the centrally situated lesions but rarely in the peripheral ones (2 per cent of total material). Implantation of malignant cells into the needle track, spread of tumour cells to the pleura, spread of infection and air embolism have been arguments against the use of transthoracic biopsy as a routine diagnostic procedure. Previous reports, based on altogether several thousands of procedures have shown these complications to be very rare. Only 2 instances of needle track implantation have been reported; both after use of large bore needles. Spread of infection also seems to be very rare and can be controlled by modern chemotherapy. Air embolism is a rare, although life-threatening possibility; certain precautions should therefore be taken. Mortality, apparently very rare, should be avoidable if the present technique with fine needles is used properly and if facilities are available for the immediate treatment of complications, especially symptomatic pneumothorax. The present review of complications shows that three main problems may be distinguished. Pneumothorax is the most frequent and practically most important complication of needle biopsy. As was shown in the foregoing, age and sex, the size and depth of the lesions, repunctures, special conditions and diseases, and last but not least experience of the operator influence the relative frequency and the degree of pneumothorax. Awareness of these factors is of practical significance as later developing major complications with potential mortality, like tension-pneumothorax, must be recognized in time and treated adequately.
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Implantation of tumour cells into the needle track seems to be a rare possibility (about 0.04 per cent). In a recently published survey (SINNER 1973) of a major part of the present material the author analysed 106 operated patients with peripherally situated malignant lung lesions under 2 em of real size, all diagnosed at an early stage. The 5-year survival rate was 42 per cent for primary carcinoma and 32 per cent for solitary metastases of extrapulmonary tumours. These results, which may well be compared with those of other reports, indicate that if spread of tumour cells exists, it is of minor importance and more than out-weighed by the advantages of early diagnosis and treatment of pulmonary malignant lesions. MOORE et coll. (1967) and ROBERTS et coll. (1962) have pointed out that diagnostic and therapeutic procedures favour tumour cell spread. Many authors have stated that malignant tumours, not only in the lungs, continuously disseminate tumour cells into the blood stream (SANDBERG et coll. 1959, SINNER & SCHINZ 1964, SINNER 1963, and others). ROBERTS et coil. found tumour cells in the blood in 108 patients with different tumour localizations in 48 per cent before, during and after operation and in 17 per cent only during operation. They also found a significant increase of tumour cells in the blood after manipulations like rectal or gynaecologic examinations, intensive washing of the tumour area (in mammary tumours) and in diagnostic procedures like bone biopsy and curettage of the uterus. However, ENGELL (1955) found malignant cells in blood samples from the tumour area about as often in patients surviving without evidence of recurrence or metastases as in those who developed recurrence or metastases and concluded that this test provided no significant information of prognosis. It may be concluded that in most cases malignant cells entering the blood stream are destroyed. Recently ENGZELL et coil. (1971) investigated the possibility of spread of tumour cells in connection with aspiration biopsy of lymph node metastasis in animal experiments (18 gauge needles) and in a clinical series of 157 patients with pleomorphic adenoma of the salivary glands and of 469 patients with prostatic carcinoma, all diagnosed by fine needle (22 gauge) biopsy. No evidence emerged of local extension of tumour growth or appearance of metastases attributable to the biopsy. Thus, there would seem to be no ground for fear of tumour spread following transthoracic biopsy, resulting in transformation of an early operable lesion into an inoperable or incurable state. Air embolism. In the past air embolism was a well recognised complication of thoracocentesis and therapeutic pneumothorax. Apart from cases in which air is directly introduced into the lung, air embolism is theoretically possible (1) if the tip of the needle is positioned in a pulmonary vein and (with removed mandrin) the atmospheric pressure exceeds the pulmonary venous pressure as might occur under a rapid inspiration, and (2) if an open communication has become established between a bronchus or air space of the lung; in a rigid lung air might be blown into the vein during a coughing episode.
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WESTCOTT (1973) recently described one such case of air embolism with radiographic and pathologic documentation. As this case seems to be the only one strictly documented, air embolism appears to be an extremely rare complication in transthoracic biopsy. In some other cases there is circumstantial clinical evidence rather than pathologic proof. Based on the present material, the relative risk per patient is then estimated to be about 0.07 per cent. However, the incidence may be further reduced or avoided if precautions are taken to warrant that the intrathoracic pressure will exceed the atmospheric pressure. Positive pressure breathing and a Valsalva manoeuver seem not to be practical measures. It is mandatory that patients should not be examined in a half-recumbent or upright position. The open needle should not be left for any length of time in situ if venous blood is obtained. After the needle has reached its definite position the syringe has to be connected without delay after the stylet has been removed. Since a sudden inspiration after an apnoea or a coughing episode might favour that the atmospheric pressure exceeds the pulmonary venous pressure, the patient should breathe normally during the procedure and only thin needles should be used. It may be concluded that few complications occur following needle aspiration biopsy if the procedure is carefully planned and performed on strict indication.
SUMMARY After 5 300 percutaneous transthoracic needle aspiration biopsy procedures in 2 726 patients pneumothorax occurred in 27.2 per cent of the patients. Only 7.7 per cent required exsufflation or drainage. The factors influencing the relative frequency and the severity of pneumothorax are discussed. Bleeding around the punctured lesions was found in 11 per cent, and hemoptysis in 2 per cent but were of no clinical importance. In one case evidence of needle track implantation was found. The theoretical and practical importance of tumour cell spread and spread of infection through the needle track is discussed. No air embolism or mortality occurred.
ZUSAMMENFASSUNG Bei 5 300 perkutanen transthorakalen Nadelaspirationsbiopsien an 2 726 Patienten trat bei 27,2 % der Patienten ein Pneumothorax auf. Nur 7,7% benotigten eine Absaugung der Luft oder eine Drainagebehandlung. Es werden die Faktoren, die die relative Frequenz und den Schweregrad des Pneumothorax ausmachen, besprochen. Eine Blutung urn die Punktionswunde wurde in 11 % beobachtet und Harnoptysen in 2 %; sie waren jedoch ohne klinische Bedeutung. In einem Fall wurden Zeichen einer Implantation im Stichkanal gefunden. Die theoretische und praktische Bedeutung der Streuung von Tumorzellen und Infektionen durch den Stichkanal werden diskutiert. Es traten keine Luftembolien oder Todesfalle auf.
RESUME Apres 5 300 biopsies transthoraciques percutanees a l'aiguille avec aspiration chez 2 726 malades, un pneumothorax est apparu dans 27,2 pour cent des cas. L'exsufflation au Ie
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drainage n'ont ete necessaires que dans 7,7 pour cent. L'auteur examine les facteurs qui influent sur la frequence relative et la gravite des pneumothorax. II y a eu un hematome autour des lesions ponctionnees dans 11 pour cent des cas et une hemoptysie dans deux pour cent mais elles n'ont pas eu d'importance clinique. Dans un cas il y a eu des signes de greffe tumorale Ie long du trajet de l'aiguille. L'auteur examine I'importance theorique et pratique de la dissemination de cellules tumorales et d'infection par Ie trajet de I'aiguille. II n'ya pas eu d'embolie gazeuse ni de mort.
REFERENCES ADAMSON JR J. S. and BATES J. H.: Percutaneous needle biopsy of lung. Arch. intern. Med. 119 (1967), 164. BELCHER J. R.: Pulmonary lesions simulating carcinoma. Acta chir. belg, Suppl. 11 (1955), 28. BERGER R. L., DARGAN E. L. and HUANG B. L.: Dissemination of cancer cells by needle biopsy of the lung. J. thorac. cardiovasc. Surg. 63 (1972), 430. BOYLEN C. T., JOHNSON N. R., RICHTERS V. and BALCHUM O. J.: High speed trephine lung biopsy: Method and results. Chest 63 (1973), 59. CASTELAIN G., CASTELAIN C. et PRETET S.: La ponction transparietale en pneumonologie. J. franc. Med. Chir. thorac. 25 (1971), 91. CHATTENBERG H. J. and ZISKIND J.: Air embolism as a complication of artificial pneumothorax. Amer. J. clin. Pathol. 9 (1939), 477. CRAVER F. L. and BINKLEY J. S.: Aspiration biopsy of tumours of the lung. J. thorac. Surg, 8 (1939), 436. DAHLGREN S.: Aspiration biopsy of intrathoracic tumours. Acta path. microbiol. scand. 70 (1967), 566. - and NORDENSTROM B.: Transthoracic needle biopsy. Year Book Medical Publ., Chicago 1966. DUTRA F. R. and GERACI C. L.: Needle biopsy of the lung. J. Amer. med. Ass. 155(1954), 21. ENGELL H. c.: Cancer cells in the circulating blood. Acta chir. scand. (1955) Suppl, No. 201. - Cancer cells in the blood. Ann. Surg. 149 (1959), 457. ENGZELL D., ESPOSTI P. L., RUBIO C., SIGURDSON A. and ZAJICEK J.: Investigation on tumour spread in connection with aspiration biopsy. Acta radiol. Ther. Phys. BioI. 10 (1971), 385. FONTANA R., MILLER W., BEABOUT J., PAYNE W. and HARRISON JR E.: Transthoracic needle aspiration of discrete pulmonary lesions. Experience in 100 cases. Med. Clin. N. Amer. 54 (1970), 961. GRUNZE H.: Klinische Zytologie der Thoraxkrankheiten. Ferdinand Enke Verlag, Stuttgart 1955. JAMESON J. B.: Aspiration biopsy of localized intrathoracic lesions. Aust. Radiol. 14 (1970), 40. JEREB M. and SINNER W.: Some special procedures in chest disease. Radiol. Clin. N. Amer. 11 (1973), 109. JOHNSSON K. och SCHNURER L. B.: Resultatav punktionscytologi vid utredning av lunginfiltrat. (In Swedish.) Nord. Med. 86 (1971), 1288. LALLI A. F., NAYLOR B. and WHITEHOUSE W.: Aspiration biopsy of thoracic lesions. Thorax 22 (1967), 404.
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LAUBY V. W., BURNETT W. E., ROSEMOND G. P. and TYSON R. R.: Value and risk of biopsy of pulmonary lesions by needle aspiration. J. thorac. cardiovasc. Surg. 49 (1965), 159. LEYDEN O. 0.: Uber inlektiose Pneumonie. Dtsch. med. Wschr. 9 (1883), 52. MARTIN H. E. and ELLIS E. B.: Aspiration biopsy. Surg, Gynec. Obstet, 59 (1934), 578. MENETRIER P.: Cancer primitif du poumon. Bull. Soc. Anat. Paris 11 (1886), 643. MEYER J. E., FERRUCCI JR. J. T. and JANOWER M. L.: Fatal complications of percutaneous lung biopsy. Radiology 96 (1970), 47. MOORE G. E., SANDBERG A. A. and SCHUBARG J. R.: Clinical and experimental observations of the occurrence and fate of tumor cells in the blood stream. Ann. Surg. 146 (1957),580. NORDENSTROM B.: A new technique for transthoracic biopsy of lung changes. Brit. J. Radiol. 38 (1965), 550. - (a) Transjugular approach to the mediastinum for mediastinal needle biopsy. Invest. Radiol. 2 (1967), 134. - (b) Paraxiphoid approach to the mediastinum for mediastinoscopy and mediastinal needle biopsy. Invest. Radiol. 2 (1967), 141. - Paravertebral approach to the posterior mediastinum for mediastinoscopy and needle biopsy. Acta radiol. Diagnosis 12 (1972), 298. - Personal communication. - and KUMAZAKI T.: Aorta, heart and lung vessels in idiopathic pulmonary emphysema related to pulmonary function. Acta radiol. Diagnosis 15 (1974), 197. OCHSNER A. and DEBAKEY M.: Primary pulmonary malignancy. Treatment by total pneumonectomy. Analysis of 79 collected cases and presentation of 7 personal cases. Surg. Gynec. Obstet. 68 (1939), 435. OLIVER T.: Cases in which death or collapse occurred after exploratory puncture of the chest. Lancet 1 (1904), 26. OVERHOLT R. H.: Curability of primary carcinoma of the lung. Early recognition and management. Surg. Gynec. Obstet. 70 (1940), 479. PERTTALA Y.: Needle biopsy in the diagnosis of pulmonary tumour. Ann. Chir. Gynaec, Fenn. 48 (1959), 427. POLLAK M.: Air embolus. Amer. Rev. Tuberc. 28 (1933), 187. REYER G. W. and KOHL H. W.: Air embolism complicating thoracic surgery. J. Amer. med. Ass. 87 (1926), 1626. RIZK G. K. and TOMBE J.: Transbronchial and transthoracic biopsy of pulmonary lesions. J. med, liban. 24 (1971), 4. ROBERTS S., JONASSON 0., LONG L., MAcGREW E. A., MACGRATH R. and COLE W. H.: Relationship of cancer cells in the circulating blood to operation. Cancer 15 (1962), 232. ROSEMOND G., BURNETT W. E. and HALL J.: Value and limitations of aspiration biopsy for lung lesions. Radiology 52 (1949), 506. SANDBERG A. A., MOORE G. E. and SCHUBARG J. R.: 'Atypical' cells in the blood of cancer patients-differentiation from tumor cells. J. nat. Cancer Inst. 22 (1959), 555. SAPPINGTON S. W. and FAVORITE G.: Lung puncture in lobar pneumonia. Amer. J. med. Sci. 191 (1936), 225. SCHLAEPFER K.: Air embolism following various diagnostic or therapeutic procedures in diseases of the pleura and lung. Bull. Johns Hopk. Hosp. 33 (1922), 321. SILVERMAN I.: A new biopsy needle. Amer. J. Surg. 40 (1928), 671. SINNER W. N.: Wert und Bedeutung des Tumorzellnachweises im stromenden Blut. Praxis 44 (1963), 1343. - Transthoracic needle biopsy of small peripheral malignant lung lesions. Invest. Radiol. 8 (1973), 305.
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W. N. SINNER
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Wert und Bedeutung der perkutanen transthorakalen Nadelbiopsie fur die Diagnose intrathorakaler Krankheitsprozesse. Fortschr. Rontgenstr, 123 (1975), 197. - und SCHINZ H. R.: Metastasenstrassen. In: Ergebnisse der medizinischen Strahlenf'orschung, Band I, S. 415. Herausgegeben von H. R. Schinz, R. Glauner und A. Riittimann. Georg Thieme Verlag, Stuttgart 1964. - and ZAJICEK J.: Implantation metastasis after percutaneous transthoracic needle aspiration biopsy. Acta radio!. Diagnosis 17 (1976), 473. SMITH W. B.: Needle biopsy of the lung with special reference to diffuse lung disease and the use of a new needle. Thorax 19 (1964), 68. STEVENS G. M., WEIGEN J. F. and LILLINGTON G. A.: Needle aspiration biopsy of localized pulmonary lesions with amplified fluoroscopic guidance. Amer. J. Roentgeno!. 103 (1968), 561. SNEDECOR G. W.: Statistical methods. Jowa, 5th edition, pp. 190 and 227. 1956. TAYLOR J. D.: Post-mortem diagnosis of air embolism by radiography. Brit. med. J. 1 (1952), 890. THORNBURY J. R. and WALLS W. J.: Transthoracic pulmonary needle aspiration biopsy. 5 year experience at the UMMC 1966 to 1971. Unpublished report. TURNER A. F. and SARGENT E. N.: Percutaneous pulmonary needle biopsy-an improved needle for a simple direct method of diagnosis. Amer. J. Roentgeno!. 104 (1968), 846. VANCE, J. W., GOOD C. A., HODGSON c., KIRKIN J. W. and GAGE R. P.: The solitary circumscribed pulmonary lesion due to bronchogenic carcinoma: A 3 year follow-up study of 94 surgical treated patients. Dis. Chest 36 (1959), 231. WEILL F., LEDOUX A., OPPERMANN A., BONNEVILLE J. F., PREVOTAT N., RICATTE J. P. et JACQUEY S.: La ponction-biopsie pulmonaire transcutanee selon Dahlgren et Nordenstrom. Ann. Radio!. 13 (1970), 119. WESTCOTT J. L.: Air embolism complicating percutaneous needle biopsy of the lung. Chest 63 (1973), 198. WIKLUND T.: Bronchogenic carcinoma. Acta chir. scand. (1951) Suppl, No. 162. WOLINSKY H. and LISCHNER M. W.: Needle track implantation of tumor after percutaneous lung biopsy. Ann. intern. Med. 71 (1969),2. WOOLF C. R.: Applications of aspiration lung biopsy with review of literature. Dis. Chest 25 (1954), 286.
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