- Email: [email protected]
Percutaneous biopsy in lung cancer
European Journal of Radiology 45 (2003) 60 /68 www.elsevier.com/locate/ejrad
Percutaneous biopsy in lung cancer Franc¸ois Laurent , Michel Montaudon, Vale´rie Latrabe, Hugues Be´gueret Unite´ d’Imagerie Thoracique et Cardiovasculaire, Hoˆpital du Haut-Le´veˆque, Centre Hospitalier Universitaire de Bordeaux, Avenue de Magellan, Pessac 33604, France Received 17 September 2002; received in revised form 18 September 2002; accepted 19 September 2002
Abstract This paper presents current indications, contraindications, technical aspects, complications and yield of diagnosis of percutaneous lung biopsy in the setting of lung cancer. Percutaneous lung biopsy should be performed each time that the therapeutic strategy can be significantly influenced, when the procedure is technically feasible and to patients for which the benefits outweigh the risks, that are pneumothorax and pulmonary haemorrhage. Factors identified as potentially favouring post-biopsy pneumothorax are numerous whereas the use of a needle size larger than 18 gauge is the major risk factor of bleeding. Although a coaxial system is highly suitable in any case, two categories of needles can be used; those providing aspiration and those for core biopsies. Both offer similar yields for the diagnosis of malignancy, but core biopsies are more efficient for the specific diagnosis of benignity and lymphoma. Technical improvements of guidance, needle design and pathological techniques may contribute to lower the size limit of the nodule to be biopsied, to decrease the complication rate and their severity and to increase the yield of diagnosis. # 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Lung; Tumour; Percutaneous biopsy; Complications
1. Introduction
2. Indications
Percutaneous biopsy has emerged as an invasive procedure of choice for the diagnosis of lung cancer over the past three decades. The technique has been popularized by Nordenstrom [1] with the introduction of thin-walled needles with an outer diameter of 1 mm or less, quieting early concerns about the safety of biopsies using large cutting needles. Increased expertise of cytopathologists and operators and advances in imaging technique guidance have mainly contributed to the growing acceptance of the method. Nevertheless, many aspects of the topic have not been submitted to large control trials and remain controversial.
Biopsy during flexible bronchoscopy and percutaneous biopsy are the techniques most widely used for providing an accurate cytologic or histologic diagnosis of lung cancer. They should be considered as complementary procedures, although their position in the diagnostic algorithm remains a subject of debate. Percutaneous biopsy is mainly indicated when the histological diagnosis can influence the therapeutic strategy or modify the staging of the disease and when the diagnosis cannot be established by bronchoscopic techniques. For central lesions with an endobronchial component, the various sampling techniques associated with flexible bronchoscopy have a high diagnostic accuracy, but peripheral tumours not visible on endobronchial examination are diagnosed less readily. For most experts, peripheral lesions smaller than 3 cm in diameter and not showing the computed tomography (CT) bronchus sign, e.g. a bronchus seen entering the
Corresponding author. Tel.: /33-5-57-65-65-42; fax: /33-5-5765-68-80 E-mail address: [email protected] (F. Laurent).
0720-048X/02/$ - see front matter # 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 0 2 ) 0 0 2 8 6 - 3
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
proximal portion of the lesion, are diagnosed more accurately by percutaneous biopsy [2,3]. Percutaneous biopsy has a high accuracy when positive for malignancy, but the question whether a non-specific benign diagnosis can obviate surgery remains open. This situation is frequent since the sensitivity for a specific benign diagnosis has been reported to be ranged from 11.7 to 68% [4]. A meta-analysis performed on 48 studies calculated the likelihood ratio for malignancy based on the percutaneous biopsy result, given a pretest probability of malignancy of 50%. A result of malignancy carried a likelihood ratio of 72 whereas a benign result had a likelihood ratio of 0.07 [4]. Therefore, whereas findings of malignant or specific diagnosis of a benign condition provide definitive results, a ‘‘suspicious’’ benign markedly decreases the probability of malignancy but cannot be considered as definitive and requires further evaluation. The need for preoperative diagnosis of a pulmonary nodule that would obviate an unnecessary surgical thoracoscopy or thoracotomy varies from one institution to the other, and depends on the pretest probability of diagnosing a lesion. There is a general agreement that biopsy is indicated in patients who are inoperable because of tumour invasion, metastatic disease or general condition and to determine the cell type in a lesion suspected of being either a metastasis or a second primary pulmonary carcinoma. Conversely, proceeding directly to thoracotomy is appropriate when preoperative diagnosis is unlikely to alter patient management, especially in the case of an operable patient with a high probability of malignancy. Debate exists, however, to know whether percutaneous biopsy should also be performed in patients who are at surgical risk, in whom a positive biopsy would permit acceptance of the risk. Advantages of a preoperative diagnosis of lung cancer are identification of small cell carcinomas, planning therapy and avoidance of unnecessary resection of benign lesions. Percutaneous biopsy of mediastinal or hilar lymph nodes has been recommended by several investigators for obtaining tissue from enlarged lymph nodes or suspected mediastinal invasion in patients with known or suspected lung carcinoma, based on the accuracy and advantages compared with mediastinoscopy [5 /7]. All regions of the mediastinum are potentially accessible with percutaneous biopsy. However, the main limitation of the technique is that a negative percutaneous biopsy of a single enlarged lymph node does not mean that the mediastinum is benign. In addition, normal-sized nodes are not evaluated by the method which is, therefore, only used in selected cases [7]. The diagnosis of chest wall and pleural lesions by percutaneous biopsy [8] as well as the diagnosis of extrathoracic malignancy such as adrenal masses can also be performed by percutaneous biopsy in the clinical setting of a lung cancer.
61
3. Contraindications Percutaneous biopsy should be limited to cases that are both truly indicated, technically feasible and for which the possible benefits outweigh the risks. Abnormal clotting function or thrombocytopenia should be recognized and corrected before the procedure. Suspected hydatid cyst or arterio-venous malformation should not be biopsied but can be identified or at least strongly suspected on CT. Mechanical ventilation which may lead to pneumothorax and favours air embolism, inability of a patient to cooperate during the procedure or to suspend respiration on request or control cough are the major contraindications. A unique functional lung, severe chronic obstructive pulmonary disease, pulmonary hypertension or cardiac insufficiency do not constitute absolute contraindications but render any complication more significant [9]. In any case, the risks must be weighted against the benefit judiciously, the availability of alternate procedures must be taken into account. Some of the contraindications with traditional guidance methods may be overcome in the near future by the use of sophisticated real-time guidance techniques such as fluoro-CT.
4. Technique 4.1. Imaging modality Fluoroscopic guidance has represented the traditional imaging modality for percutaneous biopsy [1]. The main advantages over CT guidance are the short procedure time, the real-time visualization of needle advancement and the low cost. Disadvantages include difficult access to central lesions and difficult avoidance of bullae and vascular structures in the needle pass [10]. CT has been used for 20 years and has become the standard in many institutions. CT permits planning a trajectory that avoids passage through aerated lung, avoidance of bullae, fissures or vessels and that allows possible access to central lesions. CT also helps to distinguish necrotic from solid portions of the lesion and to document unequivocally the needle tip within the lesion, a point of major value in the interpretation of absence of malignant cells [11]. The length of the procedure, one of the most reported drawbacks of CT guidance, has significantly decreased with spiral CT and today with CT fluoroscopy. CT fluoroscopy offers advantages combining those of both fluoroscopy and CT, permitting to biopsy smaller lesions, lesions that are situated in less favourable locations such as those in the costophrenic recess or close to the mediastinum, and to perform the procedure more quickly in less cooperative patients [12]. One of the major concerns of CT fluoroscopy is the increased radiation dose compared with that
62
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
of spiral CT, although irradiation may be lowered substantially [13]. US has a limited use to peripheral, pleural-based lesions producing an acoustic window but avoids irradiation. Both fine and cutting needles have been employed safely with this guidance modality with excellent performances. Major advantages are the possible fine adjustments of the tip of the needle monitored quickly and precisely throughout the procedure and the value in the biopsy of large necrotic masses [14,15].
dles is depending on many factors including personal experience, the risk of complication and the availability of a pathologist on-site. In many institutions, with no pathologist available on-site, the use of core biopsy needle is recommended at a first approach when there is a strong suspicion of a benign lesion or of a lymphoma. In other situations, especially when there is a strong suspicion of malignancy and when a pathologist is available on-site, fine-needle aspiration is recommended first [24].
4.2. Needles
4.3. Biopsy process
The use of various needle sizes, tip design and sampling mechanism have been reported in percutaneous biopsy of the lung. Requirements for an ideal biopsy needle are to minimize bleeding complications and maximize the specimen obtained. Minimizing the bleeding complications is achieved today by using needles smaller than 18 gauge. Single-pass and multiple-pass coaxial needles have been used in percutaneous biopsy of thoracic lesions. The coaxial system, which consists of inserting a thin inner needle through a larger outer needle placed at the edge or within the lesion, has numerous advantages over the single needle technique including the limitation of the number of pleural punctures, easy repositioning of the needle when correction of the course is needed and the possible use of techniques preventing air leakage [16]. Ultra-thin needles cannot be employed with a coaxial system (24 and 25 gauge) although they have been advocated by some authors to provide similar yield with fewer complications [17]. Needles are divided into two broad categories, aspiration needles providing cytology and cutting needles able to provide histology samples. With some specifically designed fine-needles, in addition to aspiration materials, small tissue fragments can be obtained for histologic examination in about 50% of cases [9]. Large cores of tissue are obtained with powered Tru-Cut type of needle with throw-lengths of 1 /2 cm and variable throw options (Fig. 1). Recently, coaxial models with small diameter have become available allowing to obtain multiple core specimens with a single pleural puncture [18 /20]. However, there is no proof that any type of needle design is superior to other types in terms of diagnostic yield and complication rate. Histology offers no advantage over fine-needle aspiration (Fig. 2) in the diagnosis of pulmonary carcinoma [21]. Nevertheless, cutting needles have been demonstrated to be more accurate in the specific diagnosis of benign lesions, in the diagnosis of lymphoma and in the case of absence of a cytopathologist on-site [18,19,22]. Both techniques are often complementary, aspiration being used initially and cutting needle proposed when malignant diagnosis is not made [23]. Therefore, the first choice between fine-needle aspiration and cutting nee-
Recent reports have detailed the technical aspect of the procedure that varies somewhat with the type of needle used [9,10,16,25]. When fine-needles are used, suction generated by a syringe, back and forth movements of the needle and multiple needle passes improved the yield of the method compared with the capillary technique. A recent study has shown that the majority of carcinomas contain a reactive zone of variable thickness, representing about 10% of the total tumour diameter [26], reinforcing the concept that multiple sampling should be done in several parts of a lesion. The wall of a necrotic or cavitary lesion should be carefully sampled. However, malignant cells tend to desquamate especially in squamous cell carcinoma and aspiration of necrosis is also recommended (Fig. 3). Ideally, a portion of the aspirate is stained and examined by a cytopathologist at the time of the procedure. This practice enables rapid assessment of the specimen so that repeat aspirations or cutting needle biopsy can be performed immediately. Specimen adequacy is determined by the cytopathologist who evaluates both cellularity and cellular preparation for reaching a definitive diagnosis. Cellular and necrotic specimens are smeared with various staining methods, and the needle is rinsed in appropriate solutions whereas blood-containing specimens are fixed in formalin for cellblock preparation [25].
5. Results An overall sensitivity of 70/100% has been reported for the diagnosis of malignancy, most reports being in the 85/95% range [10]. In a large study involving almost 12 000 transthoracic needle aspiration specimen and more than 400 institutions, sensitivity was 89%, specificity 95%, positive predictive value 99% and negative predictive value 70% [27]. The most common causes of false-negative are sampling error and inaccurate needle placement [25]. Some investigators have stressed the importance of repeating biopsy when the initial result was negative [28,29]. The rate of false-positive diagnosis remains very low in the hands of experienced cytopathologists [30]. The duration of the procedure due to
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
63
Fig. 1. Percutaneous biopsy of a pulmonary nodule using a coaxial cutting needle. Mediastinal window setting shows the needle tip of the needle within the edge of the lesion (a). Photograph of the biopsy specimen (b). The diagnosis of malignancy is based on abnormal architectural distortion and cellular atypia. Diagnosis was adenocarcinoma. CT immediately after the biopsy (c) showing area of ground-glass intensity indicating alveolar haemorrhage along the needle-track.
his presence in the biopsy room to provide immediate examination of the sample does not increase the complication rate but controversial results have been published regarding the impact on diagnostic yield [31 / 34]. Conflicting results have also been reported in the
literature concerning the diagnostic yield of small nodules, some authors report a lower accuracy with nodules smaller than 15 mm [35,36] whereas such a result has not been found by others using aspiration [37] or cutting needles [38]. Inter- and intra-observer repro-
64
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
Fig. 2. Percutaneous biopsy of a central pulmonary nodule. Prone CT during biopsy of the nodule and a small pneumothorax. Aspirated specimen showing malignant cells with high nuclear cytoplasmic ratio. Diagnosis was adenocarcinoma.
ducibilities have been shown to reach more than 90% agreement for the diagnosis of malignancy but slightly less for determining the specific histologic type [39]. Agreement has been reported between 60 and 90% of
cases between the percutaneous biopsy cancer cell type and surgical pathology cell type [40,41]. Fortunately, disagreement mostly occurs among undifferenciated and poorly differenciated non-small cell types.
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
65
Fig. 3. Percutaneous biopsy of a pulmonary lesion extending within the mediastinum. CT during biopsy (a) showing a needle pass between the sternum and mammary vessels enabling to biopsy the lesion without passing through aerated lung. The lesion was necrotic and necrosis aspirated. Aspirated specimen (b) showing typical carcinomatous cells with large nucleolus and inflammatory cells. Diagnosis was squamous cell carcinoma.
6. Complications Common complications of percutaneous biopsy of the lung are pneumothorax and bleeding. Pneumothorax
has been reported from 0 to 61%, 20% in most recent large series and the rate of pneumothoraces requiring treatment with chest tube varies from 1.6 to 17% [10]. Most pneumothoraces are detected within the first hour
66
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
post-procedure, do not require drainage, and can be managed conservatively. Large, symptomatic and expanding pneumothoraces need a chest tube placement, usually of small bore type. Aspiration of air at the end of the procedure may decrease the need for a chest tube placement [25]. One or serial chest X-ray 1 /3 h following the procedure are usually performed to detect those undetected immediately after the needle has been withdrawn. Today the practice of percutaneous biopsy is performed in many institutions on an outpatient basis and early discharge has been shown to be safe [42]. Recent reports have demonstrated that pneumothoraces can be managed safely in such outpatients in about half of the cases [43,44]. Risk factors for the development of pneumothorax have been the subject of intensive research and a lot of controversy in the literature regarding the presence of obstructive lung disease and hyperinflation. In the most recent series, the risk factors identified were the lesion size [45] and its depth [45,46], the presence of emphysema on CT, a small angle of the needle with the thoracic pleura, multiple repositioning of the needle and a great number of sampling, but not the duration of the procedure [47]. Various techniques such as positioning the patient biopsy-side down [16] and plugging the needle with a clot, the so-called blood-patch technique [16], or foam plugs [48] have been proposed to reduce the incidence of a significant pneumothorax but their true efficacy remains unclear [49]. Haemorrhage, most often a self-limited complication, is the second most common and the most dangerous potential complication of percutaneous biopsy. Massive haemoptysis requiring bronchoscopic tamponade, arterial embolization or surgery has become extremely rare with small calibre needles. Haemoptysis occurs in approximately 5 /10% in most series and is slightly more frequent with cutting needles [9,10]. Unusually blood emerging from the hub of the outer needle and alveolar haemorrhage identified as a ground-glass attenuation in the area of the biopsy or along the needle tract are often the only manifestations of bleeding during the procedure but should be considered as clues to the onset of haemoptysis (Fig. 4). Rare reported complications are vaso-vagal reaction, lung torsion, air embolism, needle tract implantation of tumour cells and cardiac tamponade [10]. Air embolism is an often fatal condition due to entry of air in the pulmonary venous circulation and subsequent myocardial infarction, stroke or death. This complication is often fatal, but fortunately very rare [50]. The incidence of needle tract metastasis is also very rare, estimated 0.012%, with a mean time of 2.6 months between the moment of the biopsy and the development of metastasis [51]. The mortality rate of percutaneous biopsy has been estimated globally to 0.02%, mainly by air embolism or massive haemoptysis [10].
Fig. 4. Percutaneous biopsy of an undifferenciated carcinoma via an anterior pass to avoid peripheral bullae. CT after the biopsy showing an area of ground-glass attenuation due to alveolar haemorrhage but no pneumothorax.
7. Conclusion Percutaneous biopsy is today a well-established technique for the diagnosis of lung cancer. Technical improvements of guidance, needle design and pathological techniques may contribute to push back technical limitations, to decrease the rate of biopsies technically impracticable, the rate of complications and their severity and to increase the yield of specific diagnosis.
References [1] Nordenstrom B. Transthoracic needle biopsy. New Engl J Med 1967;276(19):1081 /2. [2] Aristizabal JF, Young KR, Nath H. Can chest CT decrease the use of preoperative bronchoscopy in the evaluation of suspected bronchogenic carcinoma? Chest 1998;113:1244 /9. [3] Mazzone P, Jain P, Arroliga AC, Matthay RA. Bronchoscopy and needle biopsy techniques for diagnosis and staging of lung cancer. Clin Chest Med 2002;23:137 /58. [4] Lacasse Y, Wong E, Guyatt GH, Cook DJ. Transthoracic needle aspiration biopsy for the diagnosis of localised pulmonary lesions: a meta-analysis. Thorax 1999;54:884 /93. [5] Zafar N, Moinuddin S. Mediastinal needle biopsy: a 15-year experience with 139 cases. Cancer 1995;76:1065 /8.
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68 [6] Westcott JL. Percutaneous needle aspiration of hilar and mediastinal masses. Radiology 1981;141:323 /9. [7] Protopapas Z, Westcott JL. Transthoracic needle biopsy of mediastinal lymph nodes for staging lung and other cancers. Radiology 1996;199:489 /96. [8] Screaton NJ, Flower CD. Percutaneous needle biopsy of the pleura. Radiol Clin North Am 2000;38:293 /301. [9] Shaham D. Semi-invasive and invasive procedures for the diagnosis and staging of lung cancer. I. Percutaneous transthoracic needle biopsy. Radiol Clin North Am 2000;38:525 /34. [10] Klein JS, Zarka MA. Transthoracic needle biopsy. Radiol Clin North Am 2000;38:235 /66. [11] Yankelevitz DF, Henschke CI, Koizumi JH, Altorki NK, Libby D. CT-guided transthoracic needle biopsy of small solitary pulmonary nodules. Clin Imaging 1997;21:107 /10. [12] Daly B, Templeton PA. Real-time CT fluoroscopy: evolution of an interventional tool. Radiology 1999;211:309 /15. [13] Paulson EK, Sheafor DH, Enterline DS, McAdams HP, Yoshizumi TT. CT fluoroscopy-guided interventional procedures: techniques and radiation dose to radiologists. Radiology 2001;220:161 /7. [14] Liao WY, Chen MZ, Chang YL, Wu HD, Yu CJ, Kuo PH, et al. US-guided transthoracic cutting biopsy for peripheral thoracic lesions less than 3 cm in diameter. Radiology 2000;217:685 /91. [15] Pan JF, Yang PC, Chang DB, Lee YC, Kuo SH, Luh KT. Needle aspiration biopsy of malignant lung masses with necrotic centers: improved sensitivity with ultrasonic guidance. Chest 1993;103:1452 /6. [16] Moore EH. Technical aspects of needle aspiration lung biopsy: a personal perspective. Radiology 1998;208:303 /18. [17] Zavala DC, Schoell JE. Ultra-thin needle aspiration of the lung in infectious and malignant disease. Am Rev Respir Dis 1981;123:125 /31. [18] Haramati LB. CT-guided automated needle biopsy of the chest. Am J Roentgenol 1995;165:53 /5. [19] Klein JS, Salomon G, Stewart EA. Transthoracic needle biopsy with a coaxially placed 20-gauge automated cutting needle: results in 122 patients. Radiology 1996;198:715 /20. [20] Lucidarme O, Howarth N, Finet JF, Grenier PA. Intrapulmonary lesions: percutaneous automated biopsy with a detachable, 18gauge, coaxial cutting needle. Radiology 1998;207:759 /65. [21] Greif J, Marmur S, Schwarz Y, Man A, Staroselsky AN. Percutaneous core cutting needle biopsy compared with fineneedle aspiration in the diagnosis of peripheral lung malignant lesions: results in 156 patients. Cancer 1998;84:144 /7. [22] Greif J, Marmor S, Schwarz Y, Staroselsky AN. Percutaneous core needle biopsy vs. fine-needle aspiration in diagnosing benign lung lesions. Acta Cytol 1999;43:756 /60. [23] Staroselsky AN, Schwarz Y, Man A, Marmur S, Greif J. Additional information from percutaneous cutting needle biopsy following fine-needle aspiration in the diagnosis of chest lesions. Chest 1998;113:1522 /5. [24] McLoud TC. Should cutting needles replace needle aspiration of lung lesions? Radiology 1998;207:569 /70. [25] Yankelevitz DF, Vazquez M, Henschke CI. Special techniques in transthoracic needle biopsy of pulmonary nodules. Radiol Clin North Am 2000;38:267 /79. [26] Layfield LJ, Liu K, Erasmus JJ. Radiologically determined diameter, pathologic diameter, and reactive zone surrounding pulmonary neoplasms: implications for transthoracic fine-needle aspiration of pulmonary neoplasms. Diagn Cytopathol 1999;21:250 /2. [27] Zarbo RJ, Fenoglio-Preiser CM. Inter-institutional database for comparison of performance in lung fine-needle aspiration cytology: a College of American Pathologists Q-Probe Study of 5264 cases with histologic correlation. Arch Pathol Lab Med 1992;116:463 /70.
67
[28] Wescott JL. Percutaneous transthoracic needle biopsy. Radiology 1988;169:593 /601. [29] Westcott JL. Direct percutaneous needle aspiration of localized pulmonary lesions: result in 422 patients. Radiology 1980;137:31 / 5. [30] Charig MJ, Stutley JE, Padley SP, Hansell DM. The value of negative needle biopsy in suspected operable lung cancer. Clin Radiol 1991;44:147 /9. [31] Santambrogio L, Nosotti M, Bellaviti N, Pavoni G, Radice F, Caputo V. CT-guided fine-needle aspiration cytology of solitary pulmonary nodules: a prospective, randomized study of immediate cytologic evaluation. Chest 1997;112:423 /5. [32] Austin JH, Cohen MB. Value of having a cytopathologist present during percutaneous fine-needle aspiration biopsy of lung: report of 55 cancer patients and meta-analysis of the literature. Am J Roentgenol 1993;160:175 /7. [33] Padhani AR, Scott WW, Jr., Cheema M, Kearney D, Erozan YS. The value of immediate cytologic evaluation for needle aspiration lung biopsy. Invest Radiol 1997;32:453 /8. [34] Miller DA, Carrasco CH, Katz RL, Cramer FM, Wallace S, Charnsangavej C. Fine-needle aspiration biopsy: the role of immediate cytologic assessment. Am J Roentgenol 1986;147:155 /8. [35] Li H, Boiselle PM, Shepard JO, Trotman-Dickenson B, McLoud TC. Diagnostic accuracy and safety of CT-guided percutaneous needle aspiration biopsy of the lung: comparison of small and large pulmonary nodules. Am J Roentgenol 1996;167:105 /9. [36] Layfield LJ, Coogan A, Johnston WW, Patz EF. Transthoracic fine-needle aspiration biopsy: sensitivity in relation to guidance technique and lesion size and location. Acta Cytol 1996;40:687 / 90. [37] Westcott JL, Rao N, Colley DP. Transthoracic needle biopsy of small pulmonary nodules. Radiology 1997;202:97 /103. [38] Laurent F, Latrabe V, Vergier B, Montaudon M, Vernejoux JM, Dubrez J. CT-guided transthoracic needle biopsy of pulmonary nodules smaller than 20 mm: results with an automated 20-gauge coaxial cutting needle. Clin Radiol 2000;55:281 /7. [39] Taft PD, Szyfelbein WM, Greene R. A study of variability in cytologic diagnosis based on pulmonary aspiration specimens. Am J Clin Pathol 1980;73:36 /40. [40] Thornbury JR, Burke DP, Naylor B. Transthoracic needle aspiration biopsy: accuracy of cytologic typing of malignant neoplasms. Am J Roentgenol 1981;136:719 /24. [41] Horrigan TP, Bergin KT, Snow N. Correlation between needle biopsy of lung tumours and histopathologic analysis of resected specimens. Chest 1986;90:638 /40. [42] Dennie CJ, Matzinger FR, Marriner JR, Maziak DE. Transthoracic needle biopsy of the lung: results of early discharge in 506 outpatients. Radiology 2001;219:247 /51. [43] Gurley MB, Richli WR, Waugh KA. Outpatient management of pneumothorax after fine-needle aspiration: economic advantages for the hospital and patient. Radiology 1998;209:717 /22. [44] Brown KT, Brody LA, Getrajdman GI, Napp TE. Outpatient treatment of iatrogenic pneumothorax after needle biopsy. Radiology 1997;205:249 /52. [45] Cox JE, Chiles C, McManus CM, Aquino SL, Choplin RH. Transthoracic needle aspiration biopsy: variables that affect risk of pneumothorax. Radiology 1999;212:165 /8. [46] Laurent F, Michel P, Latrabe V, Tunon de Lara M, Marthan R. Pneumothoraces and chest tube placement after CT-guided transthoracic lung biopsy using a coaxial technique: incidence and risk factors. Am J Roentgenol 1999;172:1049 /53. [47] Ko JP, Shepard JO, Drucker EA, Aquino SL, Sharma A, Sabloff B, et al. Factors influencing pneumothorax rate at lung biopsy: are dwell time and angle of pleural puncture contributing factors? Radiology 2001;218:491 /6.
68
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
[48] Engeler CE, Hunter DW, Castaneda-Zuniga W, Tashjian JH, Yedlicka JW, Amplatz K. Pneumothorax after lung biopsy: prevention with transpleural placement of compressed collagen foam plugs. Radiology 1992;184:787 /9. [49] Collings CL, Westcott JL, Banson NL, Lange RC. Pneumothorax and dependent vs. nondependent patient position after needle biopsy of the lung. Radiology 1999;210:59 /64.
[50] Aberle DR, Gamsu G, Golden JA. Fatal systemic arterial air embolism following lung needle aspiration. Radiology 1987;165:351 /3. [51] Ayar D, Golla B, Lee JY, Nath H. Needle-track metastasis after transthoracic needle biopsy. J Thorac Imaging 1998;13:2 /6.
Percutaneous biopsy in lung cancer Franc¸ois Laurent , Michel Montaudon, Vale´rie Latrabe, Hugues Be´gueret Unite´ d’Imagerie Thoracique et Cardiovasculaire, Hoˆpital du Haut-Le´veˆque, Centre Hospitalier Universitaire de Bordeaux, Avenue de Magellan, Pessac 33604, France Received 17 September 2002; received in revised form 18 September 2002; accepted 19 September 2002
Abstract This paper presents current indications, contraindications, technical aspects, complications and yield of diagnosis of percutaneous lung biopsy in the setting of lung cancer. Percutaneous lung biopsy should be performed each time that the therapeutic strategy can be significantly influenced, when the procedure is technically feasible and to patients for which the benefits outweigh the risks, that are pneumothorax and pulmonary haemorrhage. Factors identified as potentially favouring post-biopsy pneumothorax are numerous whereas the use of a needle size larger than 18 gauge is the major risk factor of bleeding. Although a coaxial system is highly suitable in any case, two categories of needles can be used; those providing aspiration and those for core biopsies. Both offer similar yields for the diagnosis of malignancy, but core biopsies are more efficient for the specific diagnosis of benignity and lymphoma. Technical improvements of guidance, needle design and pathological techniques may contribute to lower the size limit of the nodule to be biopsied, to decrease the complication rate and their severity and to increase the yield of diagnosis. # 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Lung; Tumour; Percutaneous biopsy; Complications
1. Introduction
2. Indications
Percutaneous biopsy has emerged as an invasive procedure of choice for the diagnosis of lung cancer over the past three decades. The technique has been popularized by Nordenstrom [1] with the introduction of thin-walled needles with an outer diameter of 1 mm or less, quieting early concerns about the safety of biopsies using large cutting needles. Increased expertise of cytopathologists and operators and advances in imaging technique guidance have mainly contributed to the growing acceptance of the method. Nevertheless, many aspects of the topic have not been submitted to large control trials and remain controversial.
Biopsy during flexible bronchoscopy and percutaneous biopsy are the techniques most widely used for providing an accurate cytologic or histologic diagnosis of lung cancer. They should be considered as complementary procedures, although their position in the diagnostic algorithm remains a subject of debate. Percutaneous biopsy is mainly indicated when the histological diagnosis can influence the therapeutic strategy or modify the staging of the disease and when the diagnosis cannot be established by bronchoscopic techniques. For central lesions with an endobronchial component, the various sampling techniques associated with flexible bronchoscopy have a high diagnostic accuracy, but peripheral tumours not visible on endobronchial examination are diagnosed less readily. For most experts, peripheral lesions smaller than 3 cm in diameter and not showing the computed tomography (CT) bronchus sign, e.g. a bronchus seen entering the
Corresponding author. Tel.: /33-5-57-65-65-42; fax: /33-5-5765-68-80 E-mail address: [email protected] (F. Laurent).
0720-048X/02/$ - see front matter # 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 0 2 ) 0 0 2 8 6 - 3
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
proximal portion of the lesion, are diagnosed more accurately by percutaneous biopsy [2,3]. Percutaneous biopsy has a high accuracy when positive for malignancy, but the question whether a non-specific benign diagnosis can obviate surgery remains open. This situation is frequent since the sensitivity for a specific benign diagnosis has been reported to be ranged from 11.7 to 68% [4]. A meta-analysis performed on 48 studies calculated the likelihood ratio for malignancy based on the percutaneous biopsy result, given a pretest probability of malignancy of 50%. A result of malignancy carried a likelihood ratio of 72 whereas a benign result had a likelihood ratio of 0.07 [4]. Therefore, whereas findings of malignant or specific diagnosis of a benign condition provide definitive results, a ‘‘suspicious’’ benign markedly decreases the probability of malignancy but cannot be considered as definitive and requires further evaluation. The need for preoperative diagnosis of a pulmonary nodule that would obviate an unnecessary surgical thoracoscopy or thoracotomy varies from one institution to the other, and depends on the pretest probability of diagnosing a lesion. There is a general agreement that biopsy is indicated in patients who are inoperable because of tumour invasion, metastatic disease or general condition and to determine the cell type in a lesion suspected of being either a metastasis or a second primary pulmonary carcinoma. Conversely, proceeding directly to thoracotomy is appropriate when preoperative diagnosis is unlikely to alter patient management, especially in the case of an operable patient with a high probability of malignancy. Debate exists, however, to know whether percutaneous biopsy should also be performed in patients who are at surgical risk, in whom a positive biopsy would permit acceptance of the risk. Advantages of a preoperative diagnosis of lung cancer are identification of small cell carcinomas, planning therapy and avoidance of unnecessary resection of benign lesions. Percutaneous biopsy of mediastinal or hilar lymph nodes has been recommended by several investigators for obtaining tissue from enlarged lymph nodes or suspected mediastinal invasion in patients with known or suspected lung carcinoma, based on the accuracy and advantages compared with mediastinoscopy [5 /7]. All regions of the mediastinum are potentially accessible with percutaneous biopsy. However, the main limitation of the technique is that a negative percutaneous biopsy of a single enlarged lymph node does not mean that the mediastinum is benign. In addition, normal-sized nodes are not evaluated by the method which is, therefore, only used in selected cases [7]. The diagnosis of chest wall and pleural lesions by percutaneous biopsy [8] as well as the diagnosis of extrathoracic malignancy such as adrenal masses can also be performed by percutaneous biopsy in the clinical setting of a lung cancer.
61
3. Contraindications Percutaneous biopsy should be limited to cases that are both truly indicated, technically feasible and for which the possible benefits outweigh the risks. Abnormal clotting function or thrombocytopenia should be recognized and corrected before the procedure. Suspected hydatid cyst or arterio-venous malformation should not be biopsied but can be identified or at least strongly suspected on CT. Mechanical ventilation which may lead to pneumothorax and favours air embolism, inability of a patient to cooperate during the procedure or to suspend respiration on request or control cough are the major contraindications. A unique functional lung, severe chronic obstructive pulmonary disease, pulmonary hypertension or cardiac insufficiency do not constitute absolute contraindications but render any complication more significant [9]. In any case, the risks must be weighted against the benefit judiciously, the availability of alternate procedures must be taken into account. Some of the contraindications with traditional guidance methods may be overcome in the near future by the use of sophisticated real-time guidance techniques such as fluoro-CT.
4. Technique 4.1. Imaging modality Fluoroscopic guidance has represented the traditional imaging modality for percutaneous biopsy [1]. The main advantages over CT guidance are the short procedure time, the real-time visualization of needle advancement and the low cost. Disadvantages include difficult access to central lesions and difficult avoidance of bullae and vascular structures in the needle pass [10]. CT has been used for 20 years and has become the standard in many institutions. CT permits planning a trajectory that avoids passage through aerated lung, avoidance of bullae, fissures or vessels and that allows possible access to central lesions. CT also helps to distinguish necrotic from solid portions of the lesion and to document unequivocally the needle tip within the lesion, a point of major value in the interpretation of absence of malignant cells [11]. The length of the procedure, one of the most reported drawbacks of CT guidance, has significantly decreased with spiral CT and today with CT fluoroscopy. CT fluoroscopy offers advantages combining those of both fluoroscopy and CT, permitting to biopsy smaller lesions, lesions that are situated in less favourable locations such as those in the costophrenic recess or close to the mediastinum, and to perform the procedure more quickly in less cooperative patients [12]. One of the major concerns of CT fluoroscopy is the increased radiation dose compared with that
62
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
of spiral CT, although irradiation may be lowered substantially [13]. US has a limited use to peripheral, pleural-based lesions producing an acoustic window but avoids irradiation. Both fine and cutting needles have been employed safely with this guidance modality with excellent performances. Major advantages are the possible fine adjustments of the tip of the needle monitored quickly and precisely throughout the procedure and the value in the biopsy of large necrotic masses [14,15].
dles is depending on many factors including personal experience, the risk of complication and the availability of a pathologist on-site. In many institutions, with no pathologist available on-site, the use of core biopsy needle is recommended at a first approach when there is a strong suspicion of a benign lesion or of a lymphoma. In other situations, especially when there is a strong suspicion of malignancy and when a pathologist is available on-site, fine-needle aspiration is recommended first [24].
4.2. Needles
4.3. Biopsy process
The use of various needle sizes, tip design and sampling mechanism have been reported in percutaneous biopsy of the lung. Requirements for an ideal biopsy needle are to minimize bleeding complications and maximize the specimen obtained. Minimizing the bleeding complications is achieved today by using needles smaller than 18 gauge. Single-pass and multiple-pass coaxial needles have been used in percutaneous biopsy of thoracic lesions. The coaxial system, which consists of inserting a thin inner needle through a larger outer needle placed at the edge or within the lesion, has numerous advantages over the single needle technique including the limitation of the number of pleural punctures, easy repositioning of the needle when correction of the course is needed and the possible use of techniques preventing air leakage [16]. Ultra-thin needles cannot be employed with a coaxial system (24 and 25 gauge) although they have been advocated by some authors to provide similar yield with fewer complications [17]. Needles are divided into two broad categories, aspiration needles providing cytology and cutting needles able to provide histology samples. With some specifically designed fine-needles, in addition to aspiration materials, small tissue fragments can be obtained for histologic examination in about 50% of cases [9]. Large cores of tissue are obtained with powered Tru-Cut type of needle with throw-lengths of 1 /2 cm and variable throw options (Fig. 1). Recently, coaxial models with small diameter have become available allowing to obtain multiple core specimens with a single pleural puncture [18 /20]. However, there is no proof that any type of needle design is superior to other types in terms of diagnostic yield and complication rate. Histology offers no advantage over fine-needle aspiration (Fig. 2) in the diagnosis of pulmonary carcinoma [21]. Nevertheless, cutting needles have been demonstrated to be more accurate in the specific diagnosis of benign lesions, in the diagnosis of lymphoma and in the case of absence of a cytopathologist on-site [18,19,22]. Both techniques are often complementary, aspiration being used initially and cutting needle proposed when malignant diagnosis is not made [23]. Therefore, the first choice between fine-needle aspiration and cutting nee-
Recent reports have detailed the technical aspect of the procedure that varies somewhat with the type of needle used [9,10,16,25]. When fine-needles are used, suction generated by a syringe, back and forth movements of the needle and multiple needle passes improved the yield of the method compared with the capillary technique. A recent study has shown that the majority of carcinomas contain a reactive zone of variable thickness, representing about 10% of the total tumour diameter [26], reinforcing the concept that multiple sampling should be done in several parts of a lesion. The wall of a necrotic or cavitary lesion should be carefully sampled. However, malignant cells tend to desquamate especially in squamous cell carcinoma and aspiration of necrosis is also recommended (Fig. 3). Ideally, a portion of the aspirate is stained and examined by a cytopathologist at the time of the procedure. This practice enables rapid assessment of the specimen so that repeat aspirations or cutting needle biopsy can be performed immediately. Specimen adequacy is determined by the cytopathologist who evaluates both cellularity and cellular preparation for reaching a definitive diagnosis. Cellular and necrotic specimens are smeared with various staining methods, and the needle is rinsed in appropriate solutions whereas blood-containing specimens are fixed in formalin for cellblock preparation [25].
5. Results An overall sensitivity of 70/100% has been reported for the diagnosis of malignancy, most reports being in the 85/95% range [10]. In a large study involving almost 12 000 transthoracic needle aspiration specimen and more than 400 institutions, sensitivity was 89%, specificity 95%, positive predictive value 99% and negative predictive value 70% [27]. The most common causes of false-negative are sampling error and inaccurate needle placement [25]. Some investigators have stressed the importance of repeating biopsy when the initial result was negative [28,29]. The rate of false-positive diagnosis remains very low in the hands of experienced cytopathologists [30]. The duration of the procedure due to
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
63
Fig. 1. Percutaneous biopsy of a pulmonary nodule using a coaxial cutting needle. Mediastinal window setting shows the needle tip of the needle within the edge of the lesion (a). Photograph of the biopsy specimen (b). The diagnosis of malignancy is based on abnormal architectural distortion and cellular atypia. Diagnosis was adenocarcinoma. CT immediately after the biopsy (c) showing area of ground-glass intensity indicating alveolar haemorrhage along the needle-track.
his presence in the biopsy room to provide immediate examination of the sample does not increase the complication rate but controversial results have been published regarding the impact on diagnostic yield [31 / 34]. Conflicting results have also been reported in the
literature concerning the diagnostic yield of small nodules, some authors report a lower accuracy with nodules smaller than 15 mm [35,36] whereas such a result has not been found by others using aspiration [37] or cutting needles [38]. Inter- and intra-observer repro-
64
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
Fig. 2. Percutaneous biopsy of a central pulmonary nodule. Prone CT during biopsy of the nodule and a small pneumothorax. Aspirated specimen showing malignant cells with high nuclear cytoplasmic ratio. Diagnosis was adenocarcinoma.
ducibilities have been shown to reach more than 90% agreement for the diagnosis of malignancy but slightly less for determining the specific histologic type [39]. Agreement has been reported between 60 and 90% of
cases between the percutaneous biopsy cancer cell type and surgical pathology cell type [40,41]. Fortunately, disagreement mostly occurs among undifferenciated and poorly differenciated non-small cell types.
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
65
Fig. 3. Percutaneous biopsy of a pulmonary lesion extending within the mediastinum. CT during biopsy (a) showing a needle pass between the sternum and mammary vessels enabling to biopsy the lesion without passing through aerated lung. The lesion was necrotic and necrosis aspirated. Aspirated specimen (b) showing typical carcinomatous cells with large nucleolus and inflammatory cells. Diagnosis was squamous cell carcinoma.
6. Complications Common complications of percutaneous biopsy of the lung are pneumothorax and bleeding. Pneumothorax
has been reported from 0 to 61%, 20% in most recent large series and the rate of pneumothoraces requiring treatment with chest tube varies from 1.6 to 17% [10]. Most pneumothoraces are detected within the first hour
66
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
post-procedure, do not require drainage, and can be managed conservatively. Large, symptomatic and expanding pneumothoraces need a chest tube placement, usually of small bore type. Aspiration of air at the end of the procedure may decrease the need for a chest tube placement [25]. One or serial chest X-ray 1 /3 h following the procedure are usually performed to detect those undetected immediately after the needle has been withdrawn. Today the practice of percutaneous biopsy is performed in many institutions on an outpatient basis and early discharge has been shown to be safe [42]. Recent reports have demonstrated that pneumothoraces can be managed safely in such outpatients in about half of the cases [43,44]. Risk factors for the development of pneumothorax have been the subject of intensive research and a lot of controversy in the literature regarding the presence of obstructive lung disease and hyperinflation. In the most recent series, the risk factors identified were the lesion size [45] and its depth [45,46], the presence of emphysema on CT, a small angle of the needle with the thoracic pleura, multiple repositioning of the needle and a great number of sampling, but not the duration of the procedure [47]. Various techniques such as positioning the patient biopsy-side down [16] and plugging the needle with a clot, the so-called blood-patch technique [16], or foam plugs [48] have been proposed to reduce the incidence of a significant pneumothorax but their true efficacy remains unclear [49]. Haemorrhage, most often a self-limited complication, is the second most common and the most dangerous potential complication of percutaneous biopsy. Massive haemoptysis requiring bronchoscopic tamponade, arterial embolization or surgery has become extremely rare with small calibre needles. Haemoptysis occurs in approximately 5 /10% in most series and is slightly more frequent with cutting needles [9,10]. Unusually blood emerging from the hub of the outer needle and alveolar haemorrhage identified as a ground-glass attenuation in the area of the biopsy or along the needle tract are often the only manifestations of bleeding during the procedure but should be considered as clues to the onset of haemoptysis (Fig. 4). Rare reported complications are vaso-vagal reaction, lung torsion, air embolism, needle tract implantation of tumour cells and cardiac tamponade [10]. Air embolism is an often fatal condition due to entry of air in the pulmonary venous circulation and subsequent myocardial infarction, stroke or death. This complication is often fatal, but fortunately very rare [50]. The incidence of needle tract metastasis is also very rare, estimated 0.012%, with a mean time of 2.6 months between the moment of the biopsy and the development of metastasis [51]. The mortality rate of percutaneous biopsy has been estimated globally to 0.02%, mainly by air embolism or massive haemoptysis [10].
Fig. 4. Percutaneous biopsy of an undifferenciated carcinoma via an anterior pass to avoid peripheral bullae. CT after the biopsy showing an area of ground-glass attenuation due to alveolar haemorrhage but no pneumothorax.
7. Conclusion Percutaneous biopsy is today a well-established technique for the diagnosis of lung cancer. Technical improvements of guidance, needle design and pathological techniques may contribute to push back technical limitations, to decrease the rate of biopsies technically impracticable, the rate of complications and their severity and to increase the yield of specific diagnosis.
References [1] Nordenstrom B. Transthoracic needle biopsy. New Engl J Med 1967;276(19):1081 /2. [2] Aristizabal JF, Young KR, Nath H. Can chest CT decrease the use of preoperative bronchoscopy in the evaluation of suspected bronchogenic carcinoma? Chest 1998;113:1244 /9. [3] Mazzone P, Jain P, Arroliga AC, Matthay RA. Bronchoscopy and needle biopsy techniques for diagnosis and staging of lung cancer. Clin Chest Med 2002;23:137 /58. [4] Lacasse Y, Wong E, Guyatt GH, Cook DJ. Transthoracic needle aspiration biopsy for the diagnosis of localised pulmonary lesions: a meta-analysis. Thorax 1999;54:884 /93. [5] Zafar N, Moinuddin S. Mediastinal needle biopsy: a 15-year experience with 139 cases. Cancer 1995;76:1065 /8.
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68 [6] Westcott JL. Percutaneous needle aspiration of hilar and mediastinal masses. Radiology 1981;141:323 /9. [7] Protopapas Z, Westcott JL. Transthoracic needle biopsy of mediastinal lymph nodes for staging lung and other cancers. Radiology 1996;199:489 /96. [8] Screaton NJ, Flower CD. Percutaneous needle biopsy of the pleura. Radiol Clin North Am 2000;38:293 /301. [9] Shaham D. Semi-invasive and invasive procedures for the diagnosis and staging of lung cancer. I. Percutaneous transthoracic needle biopsy. Radiol Clin North Am 2000;38:525 /34. [10] Klein JS, Zarka MA. Transthoracic needle biopsy. Radiol Clin North Am 2000;38:235 /66. [11] Yankelevitz DF, Henschke CI, Koizumi JH, Altorki NK, Libby D. CT-guided transthoracic needle biopsy of small solitary pulmonary nodules. Clin Imaging 1997;21:107 /10. [12] Daly B, Templeton PA. Real-time CT fluoroscopy: evolution of an interventional tool. Radiology 1999;211:309 /15. [13] Paulson EK, Sheafor DH, Enterline DS, McAdams HP, Yoshizumi TT. CT fluoroscopy-guided interventional procedures: techniques and radiation dose to radiologists. Radiology 2001;220:161 /7. [14] Liao WY, Chen MZ, Chang YL, Wu HD, Yu CJ, Kuo PH, et al. US-guided transthoracic cutting biopsy for peripheral thoracic lesions less than 3 cm in diameter. Radiology 2000;217:685 /91. [15] Pan JF, Yang PC, Chang DB, Lee YC, Kuo SH, Luh KT. Needle aspiration biopsy of malignant lung masses with necrotic centers: improved sensitivity with ultrasonic guidance. Chest 1993;103:1452 /6. [16] Moore EH. Technical aspects of needle aspiration lung biopsy: a personal perspective. Radiology 1998;208:303 /18. [17] Zavala DC, Schoell JE. Ultra-thin needle aspiration of the lung in infectious and malignant disease. Am Rev Respir Dis 1981;123:125 /31. [18] Haramati LB. CT-guided automated needle biopsy of the chest. Am J Roentgenol 1995;165:53 /5. [19] Klein JS, Salomon G, Stewart EA. Transthoracic needle biopsy with a coaxially placed 20-gauge automated cutting needle: results in 122 patients. Radiology 1996;198:715 /20. [20] Lucidarme O, Howarth N, Finet JF, Grenier PA. Intrapulmonary lesions: percutaneous automated biopsy with a detachable, 18gauge, coaxial cutting needle. Radiology 1998;207:759 /65. [21] Greif J, Marmur S, Schwarz Y, Man A, Staroselsky AN. Percutaneous core cutting needle biopsy compared with fineneedle aspiration in the diagnosis of peripheral lung malignant lesions: results in 156 patients. Cancer 1998;84:144 /7. [22] Greif J, Marmor S, Schwarz Y, Staroselsky AN. Percutaneous core needle biopsy vs. fine-needle aspiration in diagnosing benign lung lesions. Acta Cytol 1999;43:756 /60. [23] Staroselsky AN, Schwarz Y, Man A, Marmur S, Greif J. Additional information from percutaneous cutting needle biopsy following fine-needle aspiration in the diagnosis of chest lesions. Chest 1998;113:1522 /5. [24] McLoud TC. Should cutting needles replace needle aspiration of lung lesions? Radiology 1998;207:569 /70. [25] Yankelevitz DF, Vazquez M, Henschke CI. Special techniques in transthoracic needle biopsy of pulmonary nodules. Radiol Clin North Am 2000;38:267 /79. [26] Layfield LJ, Liu K, Erasmus JJ. Radiologically determined diameter, pathologic diameter, and reactive zone surrounding pulmonary neoplasms: implications for transthoracic fine-needle aspiration of pulmonary neoplasms. Diagn Cytopathol 1999;21:250 /2. [27] Zarbo RJ, Fenoglio-Preiser CM. Inter-institutional database for comparison of performance in lung fine-needle aspiration cytology: a College of American Pathologists Q-Probe Study of 5264 cases with histologic correlation. Arch Pathol Lab Med 1992;116:463 /70.
67
[28] Wescott JL. Percutaneous transthoracic needle biopsy. Radiology 1988;169:593 /601. [29] Westcott JL. Direct percutaneous needle aspiration of localized pulmonary lesions: result in 422 patients. Radiology 1980;137:31 / 5. [30] Charig MJ, Stutley JE, Padley SP, Hansell DM. The value of negative needle biopsy in suspected operable lung cancer. Clin Radiol 1991;44:147 /9. [31] Santambrogio L, Nosotti M, Bellaviti N, Pavoni G, Radice F, Caputo V. CT-guided fine-needle aspiration cytology of solitary pulmonary nodules: a prospective, randomized study of immediate cytologic evaluation. Chest 1997;112:423 /5. [32] Austin JH, Cohen MB. Value of having a cytopathologist present during percutaneous fine-needle aspiration biopsy of lung: report of 55 cancer patients and meta-analysis of the literature. Am J Roentgenol 1993;160:175 /7. [33] Padhani AR, Scott WW, Jr., Cheema M, Kearney D, Erozan YS. The value of immediate cytologic evaluation for needle aspiration lung biopsy. Invest Radiol 1997;32:453 /8. [34] Miller DA, Carrasco CH, Katz RL, Cramer FM, Wallace S, Charnsangavej C. Fine-needle aspiration biopsy: the role of immediate cytologic assessment. Am J Roentgenol 1986;147:155 /8. [35] Li H, Boiselle PM, Shepard JO, Trotman-Dickenson B, McLoud TC. Diagnostic accuracy and safety of CT-guided percutaneous needle aspiration biopsy of the lung: comparison of small and large pulmonary nodules. Am J Roentgenol 1996;167:105 /9. [36] Layfield LJ, Coogan A, Johnston WW, Patz EF. Transthoracic fine-needle aspiration biopsy: sensitivity in relation to guidance technique and lesion size and location. Acta Cytol 1996;40:687 / 90. [37] Westcott JL, Rao N, Colley DP. Transthoracic needle biopsy of small pulmonary nodules. Radiology 1997;202:97 /103. [38] Laurent F, Latrabe V, Vergier B, Montaudon M, Vernejoux JM, Dubrez J. CT-guided transthoracic needle biopsy of pulmonary nodules smaller than 20 mm: results with an automated 20-gauge coaxial cutting needle. Clin Radiol 2000;55:281 /7. [39] Taft PD, Szyfelbein WM, Greene R. A study of variability in cytologic diagnosis based on pulmonary aspiration specimens. Am J Clin Pathol 1980;73:36 /40. [40] Thornbury JR, Burke DP, Naylor B. Transthoracic needle aspiration biopsy: accuracy of cytologic typing of malignant neoplasms. Am J Roentgenol 1981;136:719 /24. [41] Horrigan TP, Bergin KT, Snow N. Correlation between needle biopsy of lung tumours and histopathologic analysis of resected specimens. Chest 1986;90:638 /40. [42] Dennie CJ, Matzinger FR, Marriner JR, Maziak DE. Transthoracic needle biopsy of the lung: results of early discharge in 506 outpatients. Radiology 2001;219:247 /51. [43] Gurley MB, Richli WR, Waugh KA. Outpatient management of pneumothorax after fine-needle aspiration: economic advantages for the hospital and patient. Radiology 1998;209:717 /22. [44] Brown KT, Brody LA, Getrajdman GI, Napp TE. Outpatient treatment of iatrogenic pneumothorax after needle biopsy. Radiology 1997;205:249 /52. [45] Cox JE, Chiles C, McManus CM, Aquino SL, Choplin RH. Transthoracic needle aspiration biopsy: variables that affect risk of pneumothorax. Radiology 1999;212:165 /8. [46] Laurent F, Michel P, Latrabe V, Tunon de Lara M, Marthan R. Pneumothoraces and chest tube placement after CT-guided transthoracic lung biopsy using a coaxial technique: incidence and risk factors. Am J Roentgenol 1999;172:1049 /53. [47] Ko JP, Shepard JO, Drucker EA, Aquino SL, Sharma A, Sabloff B, et al. Factors influencing pneumothorax rate at lung biopsy: are dwell time and angle of pleural puncture contributing factors? Radiology 2001;218:491 /6.
68
F. Laurent et al. / European Journal of Radiology 45 (2003) 60 /68
[48] Engeler CE, Hunter DW, Castaneda-Zuniga W, Tashjian JH, Yedlicka JW, Amplatz K. Pneumothorax after lung biopsy: prevention with transpleural placement of compressed collagen foam plugs. Radiology 1992;184:787 /9. [49] Collings CL, Westcott JL, Banson NL, Lange RC. Pneumothorax and dependent vs. nondependent patient position after needle biopsy of the lung. Radiology 1999;210:59 /64.
[50] Aberle DR, Gamsu G, Golden JA. Fatal systemic arterial air embolism following lung needle aspiration. Radiology 1987;165:351 /3. [51] Ayar D, Golla B, Lee JY, Nath H. Needle-track metastasis after transthoracic needle biopsy. J Thorac Imaging 1998;13:2 /6.