Percutaneous Lung Biopsy in a Patient with a Cavitating Lung Mass: Indications, Technique, and Complications

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1 Interventional Radiology Case Conference Chest Imaging Interventional Radiology Case Conference Massachusetts General Hospital Michael M. Maher 1,2 Mannudeep K. Kalra 2 Ross L. Titton 2 Giles W. Boland 2 Conrad Wittram 1 Suzanne Aquino 1 Peter R. Mueller 2 Jo-Anne O. Shepard 1 Maher MM, Kalra MK, Titton RL, et al. DOI: /AJR Received March 19, 2005; accepted after revision March 23, Division of Thoracic Radiology, Massachusetts General Hospital, 55 Fruit St., Boston, MA Address correspondence to M. M. Maher (mmaher@partners.org). 2 Division of Abdominal Imaging and Interventional Radiology, Massachusetts General Hospital, Boston, MA. AJR 2005; 185: X/05/ American Roentgen Ray Society Percutaneous Lung Biopsy in a Patient with a Cavitating Lung Mass: Indications, Technique, and Complications Case History A 75-year-old man was admitted to the hospital with an acute myocardial infarction. The patient was a former heavy smoker. A chest radiograph revealed a left apical lung mass (Fig. 1). A CT scan showed a cavitary left upper lobe lung mass measuring cm (Fig. 2A) with an additional 3 2 cm mass at the left hilum (Fig. 2B). A wholebody PET scan showed the left upper lobe mass and at the left hilum, increased 18 F-FDG uptake that was suggestive of lung neoplasm metastatic to the left hilum (Fig. 3). Therefore, a thoracic radiologist was consulted for biopsy of the left upper lobe lung mass. Dr. Titton. It is interesting to note that a PET scan was obtained for this patient. What is the role of 18 F-FDG PET in the evaluation of patients with a pulmonary nodule or lung cancer? Dr. Kalra. In the evaluation of patients with a solitary pulmonary nodule, 18 F-FDG PET improves characterization of the nodule by estimating the probability of malignancy. The high positive predictive value for malignancy in nodules greater than 1 cm in diameter suggests that those with positive scan results should undergo either percutaneous biopsy or surgical resection. Histologic examination of PET-positive lesions is necessary because false-positive PET findings can be encountered with granulomatous lesions secondary to sarcoidosis, tuberculosis, or infection [1]. False-negative PET findings are seen in patients with small lesions (< 1 cm) and in selected malignancies, such as bronchioalveolar cell carcinoma or well-differentiated adenocarcinoma or carcinoid tumor. For this reason, regardless of PET findings, Fig. 1 Frontal chest radiograph showing left upper lobe opacity suggestive of lung mass. Left hilar mass is present. AJR:185, October

2 Fig. 2 Contrast-enhanced CT of chest. A, Scan showing cm left upper lobe mass with central cavitation. B, Scan showing left hilar mass, consistent with left hilar lymphadenopathy. Fig F-FDG PET scan showing avid uptake in left upper lobe mass and in left hilum (arrows), suggesting left upper lobe neoplasm with ipsilateral lymphadenopathy. A new and enlarging lesions, if amenable to biopsy, should undergo percutaneous lung biopsy (PLB) to exclude tumor. In our experience, PET is frequently useful before PLB in patients with more than one lung lesion amenable to percutaneous biopsy. In this scenario, it is usually wise to perform a biopsy of the lesion that shows most metabolic activity on PET. PET is also used in patients who are at high risk for development of complications after needle biopsy or a surgical procedure. Positive PET findings will support the need for immediate intervention, either PLB or surgical resection, whereas negative findings may support careful follow-up with imaging. Dr. Boland. What are the contraindications to PLB? Dr. Maher. There are several relative contraindications to PLB. First, centrally located lesions with an endobronchial component usually are amenable to biopsy at bronchoscopy. Abnormal coagulation parameters should be corrected before PLB. Pulmonary arterial hypertension is a contraindication to biopsy of lesions located deep in the lung, and PLB should be undertaken only when lesions are peripheral and the pulmonary arterial hypertension is controlled. Uncooperative patients such as those with mental retardation or with cognitive dysfunction need to be sedated carefully before biopsy. Rarely, these biopsies may need to be performed under general anesthesia. If the patient is ventilated, it is still possible to perform PLB but it is important to keep the patient apneic for short periods, during individual needle manipulations, to avoid acute air embolism. A respiratory therapist and an anesthesiologist should be present during the biopsy. Severe respiratory compromise again is a relative contraindication to lung biopsy. PLB still can be performed even with severe background interstitial lung disease, emphysema, or a history of contralateral pneumonectomy, provided the operators are experienced in chest tube placement and surgical backup is available. These patients are usually admitted overnight, after biopsy, for observation. Small lesions near the diaphragm may move significantly during respiration, making needle biopsy difficult or impossible. Dr. Kalra. What is the appropriate preprocedure care for a patient undergoing PLB? Dr. Shepard. In our institution, we have developed protocols that standardize patient care before, during, and after all interventional radiology procedures. An interventional radiologist approves the procedure initially, after discussion of the case with the referring physician and review of the available imaging. All patients receive procedurespecific instructions by mail, and high-risk patients are telephoned by an interventional nurse practitioner. During these conversations, additional information is obtained on background medical problems; medications such as warfarin, aspirin, clopidogrel bisulfate (Plavix, Sanofi-Synthelabo), and nonsteroidal antiinflammatory drugs; and social problems such as language or translation issues, transportation issues, or lack of supervi- B 990 AJR:185, October 2005

3 Interventional Radiology Case Conference sion in the home on the night after the biopsy. Using this approach, most problems are discovered in advance and the cancellation rate on the day of lung biopsy is reduced. Dr. Titton. What is your specific advice about preprocedure laboratory tests and medications? Dr. Maher. Fortunately, the risk of bleeding with PLB is low. Hemorrhage can manifest as parenchymal hemorrhage, hemothorax, or hemoptysis, and the inability of the lung to tamponade bleeding means that bleeding can be difficult to control. Hemorrhage has been reported to occur in 5% of patients [2], with hemoptysis reported in 3.4% of patients [3]. However, even minor hemoptysis with PLB needs to be avoided because it can cause coughing, which may precipitate pneumothorax or air embolism. Patients are asked whether they have a history of abnormal bleeding or excessive bruising. All patients have their platelet count, prothrombin ratio, and activated thromboplastin time determined within 1 month of the procedure [2], and these values should be within normal limits before biopsy. With regard to medications, patients on warfarin should stop this medication, in consultation with the referring physician, at least 5 days before the procedure and their prothrombin ratio should be determined again to confirm that coagulation has returned to the normal range. Patients who must continue receiving anticoagulation therapy are hospitalized before the biopsy, IV heparin is given instead of warfarin, and the heparin is stopped 4 6 hr before the procedure. Aspirin and Plavix should be stopped 7 days before biopsy. Patients receiving lowmolecular-weight heparin treatment (e.g., enoxaparin) subcutaneously should stop taking it 12 hr before the procedure. Dr. Mueller. What imaging techniques are used for performing PLBs? Dr. Wittram. In the past, PLBs were performed under fluoroscopic guidance [3]. The advantages of fluoroscopic guidance included real-time visualization of the lung mass, which is important for PLB because lesions tend to move with respiration [2]. However, there are many disadvantages to using fluoroscopic guidance. Only large lesions that can be seen clearly in frontal and lateral projections are amenable to biopsy. More central lesions cannot undergo biopsy safely because they frequently are obscured by mediastinal anatomy and because visualization of larger central pulmonary vasculature and airways is suboptimal [2, 4]. In conventional fluoroscopy, a C-arm is helpful in providing rapid biplane fluoroscopy without the need to reposition the patient, thus facilitating safe and accurate needle positioning within the lung lesion. The accuracy of fluoroscopically guided chest biopsy has been reported to be 61 97% [5]. However, close inspection of the data shows that the accuracy of PLB of lesions larger than 2 cm is approximately 80%, compared with 60% for lesions smaller than 1 cm [5]. With the increasing availability of dedicated interventional CT scanners, and as requests for biopsy of lesions as small as 7 8 mm increase, PLBs are increasingly being performed using CT guidance [2, 4]. PLB performed under CT guidance is safe, effective, and accurate, with a reported sensitivity of 90% for malignant lesions and slightly less for nonmalignant lesions [3]. There is little dispute that for lesions smaller than 1.5 cm, CT is the imaging technique of choice. Two studies have documented technical success rates varying from 74% to 93% for CTguided PLB of small lung nodules [4, 6, 7]. From a technical standpoint, CT-guided PLB has the advantage of allowing an accurate choice of needle access; avoiding the bones, adjacent organs, pulmonary vessels, bullae, and fissures; and accurately depicting the final needle position [5]. Avoidance of systemic vessels such as internal mammary vessels, intercostals, and pericardial vessels is particularly important because injury to these can result in significant hemorrhage. A potential pitfall with larger lesions is positioning of the needle within a necrotic component of the lesion. When necrosis is suspected, the needle should be directed to the solid component of the lesion, after correlation with a contrastenhanced CT scan. For biopsy of a cavitated lesion, as in the case presented, a tangential approach is advisable for three reasons. First, the diagnostic yield is greatest from the wall because a tangential approach maximizes the length of pathologic tissue being sampled. Second, the wall of a cavity is vascular and, if entered by the needle, can bleed and is less likely to tamponade itself. In addition, cavities can communicate with the airway, thus heightening the risk of significant hemoptysis and coughing. Third, compared with biopsy of solid nodules, biopsy of cavitary lesions is believed to be associated with an increased risk of air embolism. The major disadvantage of using CT guidance for PLB is the lack of real-time imaging a significant problem for biopsy of small lesions, particularly in the lower lobes, which can significantly change position with respiration and diaphragmatic motion [2, 3]. CT fluoroscopy is believed by many authors to have potential in guiding needle placement when lesion movement occurs during lung biopsy [4]. However, CT fluoroscopy does increase associated radiation dose to the operators and patient. Sonography can be considered as guidance for large lung lesions that are widely adherent to the pleura and chest wall, for large pleural masses, and for lesions of the chest wall [8]. Like fluoroscopy, its advantage is the ability to image the needle and the lesion in real time. Dr. Mueller. Why do you recommend that PLB be performed with the patient under conscious sedation? Dr. Maher. Undoubtedly, PLB can be performed safely and effectively in many patients with just local anesthetic. However, anxious patients breathe more deeply during PLB. In addition, many elderly patients who have arthritic complaints cannot lie still for the typical 1- to 1.5-hr duration of PLB. Respiratory motion is likely to affect the technical performance of the biopsy negatively, especially biopsies of small lesions in the lower lobes near the diaphragm or lesions near large central vessels, which require that the patient be immobilized so that respiration is regular and reproducible. PLB is not usually painful, and therefore pain relief is not the primary goal of conscious sedation. In recent years, we have noticed that our biopsy population is becoming more critically ill and more elderly, and at the same time the technical difficulty of PLB has increased because of the increasing numbers of requests for biopsy of smaller lesions in more difficult locations. One important point about conscious sedation and the performance of PLB is that the patient should be sedated to the desired depth before the planning CT scans are obtained. During conscious sedation, breathing becomes more shallow and lesion position may differ from that on presedation scans. Dr. Boland. When performing PLB, what are the important considerations for positioning the patient? Dr. Shepard. It is important, when possible, to select the access route that has the shortest needle track through lung and avoids the fissures, bullae, large vessels, bronchi, and bone structures [9]. To achieve such a route, some authors prefer to position the patient slightly oblique to the supine or prone positions. When either prone or supine positioning is feasible, most thoracic radiologists opt for prone posi- AJR:185, October

4 Fig. 4 CT scan showing importance of visualization of entire needle track in same plane as lesion to increase likelihood that needle will reach lesion after pleural puncture. tioning [5]. Prone positioning is preferable because the posterior interspaces are wider than the anterior ones, where costal cartilages may be large and calcified. In addition, the posterior ribs move less with respiratory motion than do the anterior ribs. A second advantage is that after biopsy we favor placing the patient such that the site of pleural puncture is dependent [10]. Therefore, after a prone biopsy, patients are placed supine during recovery, a position they generally find more comfortable. A third important advantage of prone positioning is that the patient cannot see the needle during the biopsy, reducing procedural anxiety in many patients [5]. Patients are more stable in the supine position or prone position. They tend to tilt or move more in the decubitus position, and the lateral approach has proven to have a higher pneumothorax rate than does the anterior or posterior approach [11]. However, the lateral approach is preferred when the needle will enter a lesion directly, without entering aerated lung. When one applies these important considerations to the practical positioning of the patient on the CT table before biopsy of lesions in different positions, the following factors are important. For upper lobe lesions superior to the level of the oblique fissure, most biopsies take place with the patient prone because we prefer this position and because in an anterior approach, intervening subclavian vessels frequently prevent access to the lesion. In addition, we prefer to avoid traversing the breast if possible because of the difficulty of stabilizing the needle in breast tissue. Needle positioning in the breast can be difficult in large or very firm breasts. At lower levels, in the posterior segments of the upper lobes, the oblique fissure may intervene and lessen the feasibility of a posterior approach. Even when the major fissure intervenes, biopsy of upper lobe lesions with the patient prone occasionally is possible by angling the gantry. A more cranial skin access point can then be chosen by angling the needle caudally, traversing an oblique path superior to the major fissure. For lesions in the superior and middle portions of the lower lobes, access can be gained only from a posterior approach with the patient prone. For lesions in the extreme lower lobes, patient positioning is determined by the relative distance of the lesion from the pleural puncture site when the patient is prone and supine. Lesions in the middle lobe and lingula are typically accessed with the patient supine or supine oblique. In the case presented, the lesion was inferior within the left upper lobe, and a posterior approach was not feasible because of the intervening oblique fissure. An anterior approach was safe because the lesion was below the level of the subclavian vessels and, despite significant patient anxiety, was reached without difficulty. Dr. Kalra. What maneuvers can be done to avoid intervening ribs, spine, and scapulae? Dr. Maher. To avoid the scapulae in the prone position, it is helpful to place the arms Fig. 5 CT scan showing satisfactory final needle position, with needle positioned in wall away from cavity. by the patient s sides and rotate the arms inward, resulting in lateral movement of the scapulae. To avoid the ribs, it is usually helpful to angle the gantry so that an angled needle course through the rib interspace can be negotiated. Angulation of the gantry allows the course of the needle to be planned before and during the biopsy. Dr. Boland. It would appear to interventional radiologists that PLB requires more painstaking refinements of needle positions than does the typical biopsy performed in the abdomen and pelvis. Please describe the vital steps in successful completion of PLB in this patient. Dr. Maher. PLB differs from a visceral biopsy in the abdomen in a few important ways. Because of the significant difference in contrast between lesion (independent of size) and surrounding lung, lesions are usually conspicuous. However, during a procedure, a small lesion can become obscured by surrounding parenchymal hemorrhage after initial fineneedle aspiration. Once the patient is positioned and conscious sedation has been administered safely, needle advancement must be planned carefully. CT is performed with a slice thickness of mm to ensure accurate needle placement and avoid partial-volume averaging of ribs. Multiple fine adjustments of the needle are necessary before the pleura is crossed, to ensure that the needle trajectory is correct (Fig. 4). The policy that the entire needle 992 AJR:185, October 2005

5 Interventional Radiology Case Conference must be visualized in the same plane as the lesion increases the likelihood that the needle will reach the lesion after pleural puncture. The reason for such careful planning of the needle course is underlined by a mathematic calculation suggesting that only a 3 malalignment of the needle over a distance of 10 cm will cause the needle to miss a stationary 1-cm nodule [5]. It is important that the pleura be punctured only once during the biopsy, to avoid a pneumothorax. The needle is therefore advanced toward the pleura and positioned deep in relation to the intercostal muscles, 3 4 mm short of the pleura. The pleura is then crossed and the needle advanced 2 3 cm into the lung in a single swift motion. The needle is then advanced in 3- to 4-cm increments toward the lesion while scanning is performed to confirm satisfactory needle positioning [5]. Because the lesion in this patient was cavitary, the needle was positioned with its tip in the wall away from the cavitated center (Fig. 5). Once the needle is in a good position, the inner stilette is removed. Suction of air though the lumen of the needle is avoided by never allowing the lumen of the 19-gauge needle to be open to air. Saline is placed in the well of the 19-gauge needle during needle exchange to provide a water seal. The 22-gauge Chiba needle is advanced through the lumen of the 19-gauge needle and is advanced through the lesion in quick, short increments. The 22-gauge needle is then withdrawn, and the aspirate is carefully spread onto a cytology slide and given directly to the cytopathologist. Dr. Titton. How are the cytology specimens handled? Dr. Aquino. At our institution, the cytopathologists routinely do a rapid interpretation of the slides. On-site cytopathologic examination guides the radiologist regarding the cellularity of the aspirated sample, or the likelihood that the aspirated sample is representative of the radiographic diagnosis, and regarding the need for a core biopsy. If inflammatory cells are aspirated, a smear is obtained for routine culture, acid-fast bacilli, and fungal and anaerobic organisms. If a specific diagnosis is not obtained by cytologic examination, repeated biopsies or core biopsies are performed [12, 13]. Core biopsies are particularly helpful in establishing benign diagnoses such as hamartomas and granulomas and in establishing a specific diagnosis for neuroendocrine tumors such as carcinoid and atypical carcinoid tumors and also for lymphoma. Flow cytometry is required for lesions suspected of being lymphoma. Core biopsies are performed if the lesion is of sufficient size and away from sizeable pulmonary vessels or organs such as the heart, hila, or aorta; if the patient is stable; and if there is no evidence of significant parenchymal hemorrhage. When a core biopsy is deemed necessary, we use a 20-gauge Quick- Core biopsy needle (Cook). The advantage of this biopsy apparatus is that it fits through the lumen of the 19-gauge ultrathin needle and has a 1- or 2-cm needle throw. Boiselle et al. [13] reported that the routine addition of a core biopsy to a fine-needle aspiration biopsy of the lung did not result in increased complication rates. In the patient described here, the cytopathology specimen yielded abundant atypical cells. Analysis of the specimen by the cytopathologist showed it to be diagnostic of adenocarcinoma. Once a satisfactory specimen has been taken, the needle is withdrawn in a single movement and the patient is immediately rolled onto the stretcher in the biopsydown position. The patient is moved to the postprocedure area and is instructed not to move, talk, laugh, or cough during the 3-hr recovery period. Dr. Mueller. Please describe patient care after the lung biopsy. Dr. Wittram. The patient receives oxygen continuously by nasal cannula at a rate of 2 L/sec. Inhalation of increased PO 2 helps to resorb a pneumothorax more rapidly than does inhalation of room air. Pulse rate, respiratory rate, blood pressure, and oxygen saturation level are monitored closely for 3 hr. Dr. Mueller. What are common complications of PLB? Dr. Aquino. In one of the largest reviews of PLBs, Richardson et al. [14] reviewed 5,444 lung biopsies and reported complications including pneumothorax (20.5%), pneumothorax requiring chest tube placement (3.1%), hemoptysis (5.3%), and death (0.15%). Case reports have described the occurrence of air embolism after PLB of hypervascular nodules or cavitating nodules such as in Wegener s granulomatosis [9]. Saji et al. [15] used multivariate analysis to assess risk factors for development of pneumothorax after PLB and found that greater lesion depth, wider needle trajectory angle, and increased patient-forced vital capacity were independent risk factors for pneumothorax and that lesion depth and wider needle trajectory angle were risk factors for pneumothorax requiring chest tube placement. Richardson et al. [14], in a multicenter study, found similar pneumothorax rates between centers that performed mostly core biopsies and centers that most commonly performed fine-needle aspiration. Ko et al. [11] reviewed the factors associated with a higher pneumothorax rate and concluded that the more acute the needle pleura angle, the higher the risk of pneumothorax. However, in the same paper, a longer needle dwelling time was not associated with an increase in pneumothorax rate. Tumor seeding by the needle is a theoretic possibility that is rarely observed with fine-needle biopsies. Dr. Boland. How do you manage a pneumothorax? Dr. Shepard. Intraprocedural pneumothorax makes biopsy difficult because the lesion changes position as it retracts with the collapsing lung to a more central location and the lung becomes difficult to puncture when retracted. In that situation, it can be helpful to place a second needle into the pleura under CT guidance and aspirate air from the pleural cavity, thus allowing the lung to reexpand. If a significant pneumothorax is seen at the end of the biopsy, withdrawal of the needle into the pleural cavity is advisable so that the pneumothorax can then be aspirated completely. If a pneumothorax is seen on postprocedure chest radiographs, it usually can be managed conservatively by placing the patient biopsy side down, thus encouraging the atelectatic lung to adhere to the parietal pleural surface. However, if the patient is symptomatic, or if the pneumothorax is seen to increase on serial chest radiographs, a chest tube is inserted under either CT or fluoroscopic guidance. Dr. Mueller. What are the recommendations regarding management of patients with hemoptysis or air embolism? Dr. Wittram. Hemoptysis is usually selflimited, provided coagulation parameters are normal, and patients should be reassured. They should be placed in the biopsy-down position to avoid transbronchial spillage of blood into the contralateral lung and closely monitored. If significant hemoptysis persists, the surgeons should be consulted regarding bronchoscopy and suctioning of airways. If large amounts of hemoptysis continue, a double-lumen endotracheal tube should be placed to protect the opposite lung. Fortunately, air embolism is rare. It can occur as a result of air entering the introducer needle or as a result of an internal fistula between a vessel and a bronchus. To avoid air embolism, one must not allow the needle to traverse central pulmonary veins and must avoid actions that might cause the patient to AJR:185, October

6 cough during the procedure. When air embolism is encountered, administration of 100% oxygen is important. The patient should be placed in the left lateral position to confine the air to the right heart. Dr. Maher. In summary, a 75 year-old man presented with an incidentally discovered cavitating mass in the left upper lobe with ipsilateral hilar lymphadenopathy. CT-guided lung biopsy was performed under conscious sedation. Cytopathologic examination revealed adenocarcinoma. No complications occurred during or after the procedure. References 1. Hain SF, Curran KM, Beggs AD, Fogelman I, O Doherty MJ, Maisey MN. FDG-PET as a metabolic biopsy tool in thoracic lesions with indeterminate biopsy. Eur J Nucl Med 2001; 28: Klein JS, Zarka MA. Transthoracic needle biopsy. Radiol Clin North Am 2000; 38: Swischuk JL, Castaneda F, Patel JC, et al. Percutaneous transthoracic needle biopsy of the lung: review of 612 lesions. J Vasc Interv Radiol 1998; 9: White CS, Meyer CA, Templeton PA. CT fluoroscopy for thoracic interventional procedures. Radiol Clin North Am 2000; 38: Yankelevitz DF, Vazquez M, Henschke CI. Special techniques in transthoracic needle biopsy of pulmonary nodules. Radiol Clin North Am 2000; 38: 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. AJR 1996; 167: Weisbrod GL. Transthoracic needle biopsy. World J Surg 1993; 17: Yang PC. Ultrasound-guided transthoracic biopsy of the chest. Radiol Clin North Am 2000; 38: Mokhlesi B, Ansaarie I, Bader M, Tareen M, Boatman J. Coronary artery air embolism complicating a CT-guided transthoracic needle biopsy of the lung. Chest 2002; 121: Moore EH, LeBlanc J, Montesi SA, Richardson ML, Shepard JA, McLoud TC. Effect of patient positioning after needle aspiration lung biopsy. Radiology 1991; 181: Ko JP, Shepard JO, Drucker EA, et al. Factors influencing pneumothorax rate at lung biopsy: are dwell time and angle of pleural puncture contributing factors? Radiology 2001; 218: Greif J, Marmur S, Schwarz Y, Man A, Staroselsky AN. Percutaneous core cutting needle biopsy compared with fine-needle aspiration in the diagnosis of peripheral lung malignant lesions: results in 156 patients. Cancer 1998; 84: Boiselle PM, Shepard JO, Mark EJ, et al. Routine addition of an automated biopsy device to fine-needle aspiration of the lung: a prospective assessment. AJR 1997; 169: Richardson CM, Pointon KS, Manhire AR, Macfarlane JT. Percutaneous lung biopsies: a survey of UK practice based on 5444 biopsies. Br J Radiol 2002; 75: Saji H, Nakamura H, Tsuchida T, et al. The incidence and the risk of pneumothorax and chest tube placement after percutaneous CT-guided lung biopsy. Chest 2002; 121: AJR:185, October 2005