Cardiovasc Intervent Radiol DOI 10.1007/s00270-014-0915-0
CLINICAL INVESTIGATION
Diagnostic Accuracy of MRI-guided Percutaneous Transthoracic Needle Biopsy of Solitary Pulmonary Nodules Shangang Liu • Chengli Li • Xuejuan Yu Ming Liu • Tingyong Fan • Dong Chen • Pinliang Zhang • Ruimei Ren
•
Received: 9 November 2013 / Accepted: 10 April 2014 Ó Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2014
Abstract Objective The purpose of our study was to evaluate the diagnostic accuracy of MRI-guided percutaneous transthoracic needle biopsy (PTNB) of solitary pulmonary nodules (SPNs). Methods Retrospective review of 69 patients who underwent MR-guided PTNB of SPNs was performed. Each case was reviewed for complications. The final diagnosis was established by surgical pathology of the nodule or clinical and imaging follow-up. Pneumothorax rate and diagnostic accuracy were compared between two
S. Liu X. Yu T. Fan D. Chen P. Zhang R. Ren (&) Department of Radiation Oncology, Shandong Cancer Hospital and Institute, School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Science, 440 Jiyan Road, Jinan 250117, Shandong Province, China e-mail: [email protected] S. Liu e-mail: [email protected] X. Yu e-mail: [email protected] T. Fan e-mail: [email protected] D. Chen e-mail: [email protected] P. Zhang e-mail: [email protected] C. Li M. Liu Department of Interventional MRI, Shandong Medical Imaging Research Institute, Shandong University, Weiqi Avenue, Jingwu Road, Jinan 250021, Shandong Province, China e-mail: [email protected] M. Liu e-mail: [email protected]
groups according to nodule diameter (B2 vs. [2 cm) using v2 chest and Fisher’s exact test, respectively. Results The success rate of single puncture was 95.6 %. Twelve (17.4 %) patients had pneumothorax, with 1 (1.4 %) requiring chest tube insertion. Mild hemoptysis occurred in 7 (7.2 %) patients. All of the sample material was sufficient for histological diagnostic evaluation. Pathological analysis of biopsy specimens showed 46 malignant, 22 benign, and 1 nondiagnostic nodule. The final diagnoses were 49 malignant nodules and 20 benign nodules basing on postoperative histopathology and clinical follow-up data. One nondiagnostic sample was excluded from calculating diagnostic performance. A sensitivity, specificity, accuracy, positive predictive value, and negative predictive value in diagnosing SPNs were 95.8, 100, 97.0, 100, and 90.9 %, respectively. Pneumothorax rate, diagnostic sensitivity, and accuracy were not significantly different between the two groups (P [ 0.05). Conclusions MRI-guided PTNB is safe, feasible, and high accurate diagnostic technique for pathologic diagnosis of pulmonary nodules. Keywords Interventional radiology Magnetic resonance imaging Lung biopsy Solitary pulmonary nodule
Introduction A solitary pulmonary nodule (SPN) is radiologically defined as an intraparenchymal lung lesion that has 3 cm diameter or less and is not associated with lymphadenopathy, atelectasis, or pneumonia on the same chest X-ray or CT-scan film [1]. An accurate and timely diagnosis of the nature of a SPN is fundamental to providing the patient
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with malignancy a potential for optimized cure. Spiral CT with contrast enhancement has been become the imaging modality of diagnosis for the SPN, but it is not ascertain the etiology of some nodules [2]. Histopathology of lesion is essential for clinical treatment, especially for resectable malignancy. Percutaneous transthoracic needle biopsy (PTNB) has been proven as a sensitive means to the tissue diagnosis of lung lesions in minimally invasive manner [3]. CT-guided PTNB has been confirmed as a safe and feasible technique in the histological diagnosis of the chest lesions and accepted generally as the principal imaging-guided technique [4]. The potential and actual excellent clinical results of MRI guidance have been successfully established in percutaneous biopsy and also have shown some advantages in various lesions [5–8]. However, there are relatively few reports about the role of MRI guidance in lung biopsy [9]. The purpose of this study was to evaluate retrospectively the technical success rate, mean procedure time, complication rate, and diagnostic performance of MR-guided PTNB.
Materials and Methods Institutional Review Board approval for the study was obtained and waived informed patient consent.
Medical Systems, Finland) was used to guide and monitor PTNB [8]. The biopsies were performed by one of three experienced interventional MR radiologists who had more than 5 years of experience performing thoracic biopsy. A coaxial approach was implemented in all patients by using a 15-cm, 16G MR compatibility coaxial needle (CoaxNeedleTM, Invivo Germany GmbH, Schwerin, Germany, titanium alloy) and a 22-cm, 18G MR-incompatible biopsy needle (semiautomatic biopsy needle, TSKTM, TSK Laboratory, Tochigi-Shi, Japan). When the MRcompatible needle tip reached the nodule, the operation table was moved out of the MR system and the core specimens were obtained outside with biopsy needle. The procedure was performed with the patient in a prone, supine, or lateral decubitus position on the table of the MR system, depending on the location of the nodule. A transmit-receive-type flexible surface coil (30 cm in diameter) was placed on the area of skin entry point for intraoperative imaging. A T1-weighted field echo sequence (T1W FE, slices 5/3, TR/TE 60/7 ms, flip angle 60°, slice thickness/interval 8.0/8.0 mm, field of view 30 cm, matrix 160 9 192, acquisition time 18/12 s) or a T1-weighted fast spin echo sequence (T1W FSE, slices 5, TR/TE 400/16 ms, flip angle 90°, acquisition time 21 s) was used to acquire repeatedly images during the procedure. The imaging sequence was selected depending on the duration of patient’s breath-hold.
Study Population and Biopsy Indication Biopsy Procedure We retrospectively reviewed our consecutive case series of 69 hospitalized patients with SPNs who underwent MRguided PTNB at our electronic health record system August 2010 to March 2012. The study sample consisted of 69 patients (39 males, 30 females, age range 19–79 years, mean age 60.17 years). The mean nodule diameter was 2.1 ± 0.6 (SD) cm (range 0.9–3.0 cm). Forty-four nodules were in the upper or middle lobes and 25 nodules in the lower lobes. Patients were excluded due to patient factors, such as severe emphysema, bleeding diathesis, and contraindications to MRI. Depending on the plain and enhanced chest CT images, the safe needle route was planned before biopsy. All biopsies were performed at the request of pulmonary physicians or surgeons due to a clinical suspicion of pulmonary malignancy. All patients were trained to breathe hold their breathing at the end of expiration to facilitate image acquisition before operation. Equipment and Technique A 0.23 T open configuration MRI scanner equipped with optical navigation system of Ipath200 (Proview, Philips
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Tri-plane imaging was acquired for localization of nodules and demonstration of the anatomic relationships. The navigation system allowed for multiplanar image acquisition and tracked the puncture route automatically. A blue graphic overlay line on the MR images displayed on the inroom monitor indicated biopsy needle location. This overlay line was used for determination of the skin entry point, needle route, and intraoperative guidance (Fig. 1B, C). All procedures were performed under local anesthesia. Two cross-sectional images of T1-weighted FE or FSE with breath-hold technique were used for guiding needle placement. The operator used the intermittently acquired images for tracking and adjustment of the needle trajectory until the tip was reached the targeted nodule through the pleura. After the position of the needle tip was confirmed on MR scans, the operation table was moved beyond the 5 Gauss line and the needle biopsy system was fired (Figs. 1D, 2B–D, 3B). The specimens were fixed in 10 % formalin for pathologic diagnostic examination. No pathologist or cytologist was on-site during the procedure. Decisions to perform additional needle biopsies were based on whether the specimen quantity was deemed safe and
S. Liu et al.: Interventional Radiology
Fig. 1 A 54-year-old woman who underwent MRI-guided percutaneous needle biopsy. A CT shows a 1.8-cm solid nodule in right upper lung lobe. Nodule (white arrow) can be displayed clearly on transverse image (B) and sagittal image (C) of T1-weighted FE. A
graphic overlay line (black arrow) on the MR image was used to choose the puncture path and to determine the target point (grey point). D Transverse image of T1-weighted FE shows the biopsy needle (arrow). The needle biopsy result was lung adenocarcinoma
Fig. 2 A 74-year-old man who underwent MRI-guided percutaneous needle biopsy. A CT shows a 2.8-cm solid nodule in left lower lung lobe. B–D Sagittal images of T1-weighted FE show the percutaneous
procedure of biopsy needle (arrow). The needle biopsy result was lung squamous cell carcinoma
sufficient for diagnosis by the radiologists. Vital signs were continuously monitored by a MR-compatible patient monitoring system (MRGLIFE C PlusTM, Schiller Medical, Switzerland) during the procedure. After the procedure, the patients were monitored for 24 h for potential postinterventional complications in a ward. Chest radiographs were immediately obtained to evaluate pneumothorax after biopsy in patients. If a small asymptomatic pneumothorax presented, the patient was treated conservatively with monitoring of vital signs, administration of supplemental oxygen, and follow-up chest radiography 1 or 2 h later to evaluate the stability of the pneumothorax. If a large or rapidly enlarging pneumothorax (C30 %) was found, a chest tube was placed.
diagnosis. Procedure time was defined as from the first image acquisition to the finally withdrawing the biopsy needle. The complications were classified as the minor or major according to the Society of Interventional Radiology Clinical Practice Guidelines’ criteria [10]. Diagnostic performance was evaluated by determining sensitivity, specificity, accuracy positive predictive value, and negative predictive value. The final diagnosis was based on by a pathologic examination of surgical specimens. For nodules in which no surgical resection was performed, the final diagnosis was based on the subsequent follow-up data on the basis of clinical and imaging follow-up for at least 12 months after biopsy. We compared the pneumothorax rate with v2 test, and diagnostic sensitivity and accuracy with Fisher’s exact test between the two group according to lesion size (B2 vs. [2 cm), with a P values \0.05 considered to indicate significant differences.
Data Collection and Statistical Analysis Data were assessed for number of pleural passes, technical success, procedure time, complications, and diagnostic performance. The number of pleural passes was defined as the operator attempted to directly puncture the pleura during one session. Technical success was defined as the acquisition of a tissue specimen adequate for pathological
Results The number of pleural passes was total 69 with single puncture for 66 nodules and two punctures for 3 nodules
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S. Liu et al.: Interventional Radiology Table 1 Final diagnoses of 69 solitary pulmonary nodules Diagnosis
Number of nodules
Malignant nodules Squamous cell carcinoma Adenocarcinoma
9 32
Small cell lung cancer
1
Metastatic tumor
4
Benign nodules Tuberculosis
6
Chronic inflammation
11
Fibrosis
2
Inflammatory pseudotumour
1
Squamous cell carcinomaa Adenocarcinomaa
1 1
Nondiagnostic nodules Squamous cell carcinoma Total a
1 69
False-negative case
Table 2 Pneumothorax rate and diagnostic accuracy based on nodule size Variables
Diameter
Pneumothorax rate Fig. 3 A 57-year-old woman who underwent MRI-guided percutaneous needle biopsy. A CT shows a 1.5-cm solid nodule in left lower lung lobe. B Sagittal image of T1-weighted FE shows the percutaneous procedure of biopsy needle (arrow). The needle biopsy result was lung inflammatory pseudotumour
during one session. The single puncture rate was 95.6 % (66/ 69). Technical success was achieved in all 69 procedures. The mean procedure time was 25.26 (range 19–48) min. Major complication occurred in one case of pneumothorax (4.8 %, 1/69) with chest tube placement because of enlarging pneumothorax (C30 %). There were 16 minor complications (23.2 %, 16/69), including 11 cases of small pneumothorax (15.9 %, 11/69) and 5 cases of mild hemoptysis (7.2 %, 5/69). All minor complications were selflimited without need of treatment. Pathological analysis of biopsy specimens showed 46 of 69 malignant nodules, 22 of 69 benign nodules, and 1 of 69 nondiagnostic nodules. In 42 (41 malignant and 1 benign) cases, surgical pathology was consistent with the biopsy results. Twenty-four (5 malignant and 19 benign) cases were confirmed by clinical follow-up. Two of 22 falsenegatives [adenocarcinoma (n = 1), squamous cell carcinoma (n = 1)] were confirmed by surgical pathology. one nondiagnostic sample was excluded from calculating diagnostic performance. The diagnostic performance was
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Diagnostic sensitivity Diagnostic accuracya
a
P
[2 cm
B2 cm
19.4 % (7/36)
15.2 % (5/33)
0.638b
95.8 % (23/24)
95.4 % (21/22)
1.000c
97.1 % (34/35)
96.9 % (32/33)
1.000c
a Diagnostic sensitivity and accuracy were calculated on basis of 68 biopsy results, excluding one nondiagnostic sample b
v2 test
c
Fisher’s exact test
as follows: sensitivity 95.8 % (46/48), specificity 100 % (20/20), accuracy 97.0 % (66/68), positive predictive value of 100 % (46/46), and negative predictive value of 90.9 % (20/22). Of one nondiagnostic nodule, postsurgical pathology revealed a squamous cell carcinoma (Table 1). Results for nodules B2 cm in diameter [n = 33; pneumothorax rate 15.2 % (5/33), sensitivity 95.4 % (21/22), accuracy 96.9 % (32/33)] were not statistically different from those for nodules [2 cm in diameter [n = 36; pneumothorax rate 19.4 % (7/36), sensitivity 95.8 % (23/ 24), accuracy 97.1 % (34/35)] (v2 test: P = 0.638; Fisher’s exact test: P = 1.000; Table 2).
Discussion CT-guided PTNB is a well-established and common method for cytological and pathological diagnosis of
S. Liu et al.: Interventional Radiology
pulmonary lesions in clinical practice. However, MR-guided needle biopsy has been as a guide tool and established as an option to more conventional means in selected indications including lung lesions. Sakarya et al. [9] first reported MR fluoroscopy-guided transthoracic fine-needle aspiration biopsy of lung masses that were 2–7 cm in diameter in 2003. MRI is not routinely used for evaluation of the lungs, mediastinum, or pleura in practice due to low proton density in the lung and the fast signal decay due to susceptibility artifacts at air–tissue interfaces [11]. However, MRI is an established alternative to CT for evaluation of the thoracic vasculature and mediastinal, hilar, and chest wall abnormalities [12]. MRI facilitates good soft-tissue contrast without contrast medium, has multiplanar capability, intrinsic flow sensitivity, near real-time imaging, and involves no ionizing radiation. The images can be acquired with short scan times with the breath-hold technique to guide the procedure of needle biopsy. The open device allows good access to the patients and has adequate space for interventional procedure. The Ipath200 optical system automatically and dynamically shows the needle route as a virtual overlay and gives precise navigation for insertion with a favorable efficiency profile. The MR-image quality of chest largely depends on the breath-hold duration and compliance of the patient. The patients were requested to hold their breath at the end of the normal expiration cycle as long as possible in order to avoid respiratory motion artifact during acquiring images. In our study, T1W FE was most commonly used for guiding the needle placement during the procedures with shorter acquisition time (12 or 18 s). If a patient could not tolerate well the breath-hold for 18 s, T1W FE sequence (three slices, 12 s) was used to shorten the patient’s breathhold time. If the visualization of nodule has interference from pulse artefacts on TW FE images, the T1W FSE sequence may be used for locating the nodule and planning the access. Although the image update delayed 12–21 s under low-field MRI system, the mean procedural time was 25.26 (range 19–48) min in this study, which was equal to CT guidance (23–37 min) [13–15] but longer than that of CT fluoroscopy (12.3–23.8 min) [14–16]. Compared with CT guidance, the longer acquisition time of the low-field MR system made us carefully select patients for PTNB. Major complications occurred in 1 case (4.8 % pneumothorax with chest tube placement) and minor complications occurred in 16 cases (15.9 % pneumothorax and 7.2 % hemoptysis) in our study. Pneumothorax is the most commonly reported complication of imaging-guided PTNB. In our study, the pneumothorax rate was 17.4 % (12/69) with one patient requiring chest tube insertion. It was at a relatively low level compared with reports in the previous literature of CT-guided PTNB in the diagnosis of SPNs (22–26 %) [13, 17–19]. This result might be
explained that the use of coaxial biopsy systems and tracking navigation decreased the number of passes through the pleura to reduce the frequency of pneumothorax and the necessity for chest tube placement. The single puncture rate was 95.6 % in our study. In our study, the cases that inserted a chest tube had two punctures, which could result in severe pneumothorax. A major disadvantage of MRI is that it cannot quickly identify pneumothorax; hence, chest radiographs or CT scans are obtained immediately or follow-up after operation. It is particularly emphasized that the plan of needle route should depend on CT images before the operation to avoid visible bullae and pulmonary fissure and to cross as few pleural surfaces as possible. In this study, the diagnostic accuracy (97 %) of the MRI-guided PTNB for SPNs compares parallelly with reported rates of CT-guided PTNB (81–99 %) [12, 16–18]. The target site must been selected in the suitable location to ensure obtaining representative and sufficient sample for the diagnosis. The needle path of sampling should not pass through the necrotic zone of lesion, which can increase the diagnosis of false-negative [20]. Two false-negative nodules diagnosed as inflammation by needle biopsy were proved to be malignancy by postsurgical pathology in this series. The samples might be obtained from the inflammatory tissue in the vicinity of the nodule. If the nodule tends to malignancy by characteristic of CT images, even though the diagnosis of biopsy is benign, further evaluation is required to determinate its nature as early as possible. Previous studies have found that the lesion size has a correlation with pneumothorax rate and diagnostic accuracy [21–23]; however, our results did not support these findings. We compared the pneumothorax rate and diagnostic accuracy between the two groups according to lesion size, and no statistically significant difference was seen. It might be related to the use of multiple plane imaging and tracing navigation system under MR guidance, which precisely localized the target nodule. Our study had limitations. First, the retrospective analysis may introduce a case-selection bias. Second, while the final diagnosis of surgical histopathology was only 45 nodules in all patients, 24 lesions required clinical and imaging follow-ups. In addition, the follow-up period was relatively short. SPN, such as atypical adenomatous hyperplasia or adenocarcinoma in situ, may persist without an internal change long after a 2-year follow-up period [24]. In conclusion, our study showed that MRI-guided PTNB is a safe, feasible, and highly accurate diagnostic technique for histopathologic diagnosis of pulmonary nodules. Conflict of interest All authors declare that we have no conflict of interest about this paper.
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References 1. Midthun DE, Swensen SJ, Jett JR (1993) Approach to the solitary pulmonary nodule. Mayo Clin Proc 68:378–385 2. Swensen SJ, Brown LR, Colby TV et al (1996) Lung nodule enhancement at CT: prospective findings. Radiology 201:447–455 3. Gardner D, vanSonnenberg E, D’Agostino HB et al (1991) CTguided transthoracic needle biopsy. Cardiovasc Interv Radiol 14:17–23 4. vanSonnenberg E, Lin AS, Deutsch AL, Mattrey RF (1983) Percutaneous biopsy of difficult mediastinal, hilar, and pulmonary lesions by computed-tomographic guidance and a modified coaxial technique. Radiology 148:300–303 5. Fritz J, Tzaribachev N, Thomas C et al (2012) Magnetic resonance imaging-guided osseous biopsy in children with chronic recurrent multifocal osteomyelitis. Cardiovasc Interv Radiol 35:146–153 6. Fried MP, Hsu L, Jolesz FA (1998) Interactive magnetic resonance imaging guided biopsy in the head and neck: initial patient experience. Laryngoscope 108:488–493 7. Fischbach F, Bunke J, Thormann M, Gaffke G et al (2011) MRguided freehand biopsy of liver lesions with fast continuous imaging using a 1.0-T open MRI scanner: experience in 50 patients. Cardiovasc Interv Radiol 34:188–192 8. Blanco Sequeiros R, Klemola R, Ojala R (2002) MRI-guided trephine biopsy and fine-needle aspiration in the diagnosis of bone lesions in low-field (0.23 T) MRI system using optical instrument tracking. Eur Radiol 12:830–835 9. Sakarya ME, Ynak O, Ozbay B et al (2003) MR fluoroscopyguided transthoracic fine-needle aspiration biopsy: feasibility. Radiology 228:589–592 10. Sacks D, McClenny TE, Cardella JF, Lewis CA (2003) Society of Interventional Radiology clinical practice guidelines. J Vasc Interv Radiol 14:199–202 11. Biederer J, Both M, Graessner J et al (2003) Lung morphology: fast MR imaging assessment with a volumetric interpolated breath-hold technique: initial experience with patients. Radiology 226:242–249 12. Puderbach M, Hintze C, Ley S et al (2007) MR imaging of the chest: a practical approach at 1.5 T. Eur J Radiol 64:345–355
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13. Ohno Y, Hatabu H, Takenaka D, Imai M, Ohbayashi C, Sugimura K (2004) Transthoracic CT-guided biopsy with multiplanar reconstruction image improves diagnostic accuracy of solitary pulmonary nodules. Eur J Radiol 51:160–168 14. Carlson SK, Felmlee JP, Bender CE et al (2005) CT fluoroscopyguided biopsy of the lung or upper abdomen with a breath-hold monitoring and feedback system: a prospective randomized controlled clinical trial. Radiology 237:701–708 15. Froelich JJ, Ishaque N, Regn J, Saar B, Walthers EM, Klose KJ (2002) Guidance of percutaneous pulmonary biopsies with realtime CT fluoroscopy. Eur J Radiol 42:74–79 16. Schaefer PJ, Schaefer FK, Heller M, Jahnke T (2007) CT fluoroscopy guided biopsy of small pulmonary and upper abdominal lesions: efficacy with a modified breathing technique. J Vasc Interv Radiol 18:1241–1248 17. Santambrogio L, Nosotti M, Bellaviti N et al (1997) CT-guided fine-needle aspiration cytology of solitary pulmonary nodules: a prospective, randomized study of immediate cytologic evaluation. Chest 112:423–425 18. Golfieri R, Sbrozzi F, de Santis FD et al (1998) Clinical role of CT-guided transthoracic needle biopsy in the diagnosis of solitary pulmonary nodules. Radiol Med 95:329–337 19. Khan KA, Zaidi S, Swan N (2012) The use of computerised tomography guided percutaneous fine needle aspiration in the evaluation of solitary pulmonary nodules. Ir Med J 105:50–52 20. Birchard KR (2011) Transthoracic needle biopsy. Semin Interv Radiol 28:87–97 21. Li H, Boiselle PM, Shepard JO, Trotman-Dickenson B, McCloud TC (1996) Diagnostic accuracy and safety of CT-guided percutaneous needle aspiration biopsy of the lung: comparison of small and large pulmonary nodules. Am J Roentgenol 167:105–109 22. Cox JE, Chiles C, Aquino SL, Choplin RH (1999) Transthoracic needle aspiration biopsy: variables that affect risk of pneumothorax. Radiology 212:165–168 23. Tsukada H, Satou T, Iwashima A, Souma T (2000) Diagnostic accuracy of CT-guided automated needle biopsy of lung nodules. Am J Roentgenol 175:239–243 24. Cummings SR, Lillington GA, Richard RJ (1986) Estimating the probability of malignancy in solitary pulmonary nodules: a Bayesian approach. Am Rev Respir Dis 134:449–452
CLINICAL INVESTIGATION
Diagnostic Accuracy of MRI-guided Percutaneous Transthoracic Needle Biopsy of Solitary Pulmonary Nodules Shangang Liu • Chengli Li • Xuejuan Yu Ming Liu • Tingyong Fan • Dong Chen • Pinliang Zhang • Ruimei Ren
•
Received: 9 November 2013 / Accepted: 10 April 2014 Ó Springer Science+Business Media New York and the Cardiovascular and Interventional Radiological Society of Europe (CIRSE) 2014
Abstract Objective The purpose of our study was to evaluate the diagnostic accuracy of MRI-guided percutaneous transthoracic needle biopsy (PTNB) of solitary pulmonary nodules (SPNs). Methods Retrospective review of 69 patients who underwent MR-guided PTNB of SPNs was performed. Each case was reviewed for complications. The final diagnosis was established by surgical pathology of the nodule or clinical and imaging follow-up. Pneumothorax rate and diagnostic accuracy were compared between two
S. Liu X. Yu T. Fan D. Chen P. Zhang R. Ren (&) Department of Radiation Oncology, Shandong Cancer Hospital and Institute, School of Medicine and Life Sciences, University of Jinan-Shandong Academy of Medical Science, 440 Jiyan Road, Jinan 250117, Shandong Province, China e-mail: [email protected] S. Liu e-mail: [email protected] X. Yu e-mail: [email protected] T. Fan e-mail: [email protected] D. Chen e-mail: [email protected] P. Zhang e-mail: [email protected] C. Li M. Liu Department of Interventional MRI, Shandong Medical Imaging Research Institute, Shandong University, Weiqi Avenue, Jingwu Road, Jinan 250021, Shandong Province, China e-mail: [email protected] M. Liu e-mail: [email protected]
groups according to nodule diameter (B2 vs. [2 cm) using v2 chest and Fisher’s exact test, respectively. Results The success rate of single puncture was 95.6 %. Twelve (17.4 %) patients had pneumothorax, with 1 (1.4 %) requiring chest tube insertion. Mild hemoptysis occurred in 7 (7.2 %) patients. All of the sample material was sufficient for histological diagnostic evaluation. Pathological analysis of biopsy specimens showed 46 malignant, 22 benign, and 1 nondiagnostic nodule. The final diagnoses were 49 malignant nodules and 20 benign nodules basing on postoperative histopathology and clinical follow-up data. One nondiagnostic sample was excluded from calculating diagnostic performance. A sensitivity, specificity, accuracy, positive predictive value, and negative predictive value in diagnosing SPNs were 95.8, 100, 97.0, 100, and 90.9 %, respectively. Pneumothorax rate, diagnostic sensitivity, and accuracy were not significantly different between the two groups (P [ 0.05). Conclusions MRI-guided PTNB is safe, feasible, and high accurate diagnostic technique for pathologic diagnosis of pulmonary nodules. Keywords Interventional radiology Magnetic resonance imaging Lung biopsy Solitary pulmonary nodule
Introduction A solitary pulmonary nodule (SPN) is radiologically defined as an intraparenchymal lung lesion that has 3 cm diameter or less and is not associated with lymphadenopathy, atelectasis, or pneumonia on the same chest X-ray or CT-scan film [1]. An accurate and timely diagnosis of the nature of a SPN is fundamental to providing the patient
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with malignancy a potential for optimized cure. Spiral CT with contrast enhancement has been become the imaging modality of diagnosis for the SPN, but it is not ascertain the etiology of some nodules [2]. Histopathology of lesion is essential for clinical treatment, especially for resectable malignancy. Percutaneous transthoracic needle biopsy (PTNB) has been proven as a sensitive means to the tissue diagnosis of lung lesions in minimally invasive manner [3]. CT-guided PTNB has been confirmed as a safe and feasible technique in the histological diagnosis of the chest lesions and accepted generally as the principal imaging-guided technique [4]. The potential and actual excellent clinical results of MRI guidance have been successfully established in percutaneous biopsy and also have shown some advantages in various lesions [5–8]. However, there are relatively few reports about the role of MRI guidance in lung biopsy [9]. The purpose of this study was to evaluate retrospectively the technical success rate, mean procedure time, complication rate, and diagnostic performance of MR-guided PTNB.
Materials and Methods Institutional Review Board approval for the study was obtained and waived informed patient consent.
Medical Systems, Finland) was used to guide and monitor PTNB [8]. The biopsies were performed by one of three experienced interventional MR radiologists who had more than 5 years of experience performing thoracic biopsy. A coaxial approach was implemented in all patients by using a 15-cm, 16G MR compatibility coaxial needle (CoaxNeedleTM, Invivo Germany GmbH, Schwerin, Germany, titanium alloy) and a 22-cm, 18G MR-incompatible biopsy needle (semiautomatic biopsy needle, TSKTM, TSK Laboratory, Tochigi-Shi, Japan). When the MRcompatible needle tip reached the nodule, the operation table was moved out of the MR system and the core specimens were obtained outside with biopsy needle. The procedure was performed with the patient in a prone, supine, or lateral decubitus position on the table of the MR system, depending on the location of the nodule. A transmit-receive-type flexible surface coil (30 cm in diameter) was placed on the area of skin entry point for intraoperative imaging. A T1-weighted field echo sequence (T1W FE, slices 5/3, TR/TE 60/7 ms, flip angle 60°, slice thickness/interval 8.0/8.0 mm, field of view 30 cm, matrix 160 9 192, acquisition time 18/12 s) or a T1-weighted fast spin echo sequence (T1W FSE, slices 5, TR/TE 400/16 ms, flip angle 90°, acquisition time 21 s) was used to acquire repeatedly images during the procedure. The imaging sequence was selected depending on the duration of patient’s breath-hold.
Study Population and Biopsy Indication Biopsy Procedure We retrospectively reviewed our consecutive case series of 69 hospitalized patients with SPNs who underwent MRguided PTNB at our electronic health record system August 2010 to March 2012. The study sample consisted of 69 patients (39 males, 30 females, age range 19–79 years, mean age 60.17 years). The mean nodule diameter was 2.1 ± 0.6 (SD) cm (range 0.9–3.0 cm). Forty-four nodules were in the upper or middle lobes and 25 nodules in the lower lobes. Patients were excluded due to patient factors, such as severe emphysema, bleeding diathesis, and contraindications to MRI. Depending on the plain and enhanced chest CT images, the safe needle route was planned before biopsy. All biopsies were performed at the request of pulmonary physicians or surgeons due to a clinical suspicion of pulmonary malignancy. All patients were trained to breathe hold their breathing at the end of expiration to facilitate image acquisition before operation. Equipment and Technique A 0.23 T open configuration MRI scanner equipped with optical navigation system of Ipath200 (Proview, Philips
123
Tri-plane imaging was acquired for localization of nodules and demonstration of the anatomic relationships. The navigation system allowed for multiplanar image acquisition and tracked the puncture route automatically. A blue graphic overlay line on the MR images displayed on the inroom monitor indicated biopsy needle location. This overlay line was used for determination of the skin entry point, needle route, and intraoperative guidance (Fig. 1B, C). All procedures were performed under local anesthesia. Two cross-sectional images of T1-weighted FE or FSE with breath-hold technique were used for guiding needle placement. The operator used the intermittently acquired images for tracking and adjustment of the needle trajectory until the tip was reached the targeted nodule through the pleura. After the position of the needle tip was confirmed on MR scans, the operation table was moved beyond the 5 Gauss line and the needle biopsy system was fired (Figs. 1D, 2B–D, 3B). The specimens were fixed in 10 % formalin for pathologic diagnostic examination. No pathologist or cytologist was on-site during the procedure. Decisions to perform additional needle biopsies were based on whether the specimen quantity was deemed safe and
S. Liu et al.: Interventional Radiology
Fig. 1 A 54-year-old woman who underwent MRI-guided percutaneous needle biopsy. A CT shows a 1.8-cm solid nodule in right upper lung lobe. Nodule (white arrow) can be displayed clearly on transverse image (B) and sagittal image (C) of T1-weighted FE. A
graphic overlay line (black arrow) on the MR image was used to choose the puncture path and to determine the target point (grey point). D Transverse image of T1-weighted FE shows the biopsy needle (arrow). The needle biopsy result was lung adenocarcinoma
Fig. 2 A 74-year-old man who underwent MRI-guided percutaneous needle biopsy. A CT shows a 2.8-cm solid nodule in left lower lung lobe. B–D Sagittal images of T1-weighted FE show the percutaneous
procedure of biopsy needle (arrow). The needle biopsy result was lung squamous cell carcinoma
sufficient for diagnosis by the radiologists. Vital signs were continuously monitored by a MR-compatible patient monitoring system (MRGLIFE C PlusTM, Schiller Medical, Switzerland) during the procedure. After the procedure, the patients were monitored for 24 h for potential postinterventional complications in a ward. Chest radiographs were immediately obtained to evaluate pneumothorax after biopsy in patients. If a small asymptomatic pneumothorax presented, the patient was treated conservatively with monitoring of vital signs, administration of supplemental oxygen, and follow-up chest radiography 1 or 2 h later to evaluate the stability of the pneumothorax. If a large or rapidly enlarging pneumothorax (C30 %) was found, a chest tube was placed.
diagnosis. Procedure time was defined as from the first image acquisition to the finally withdrawing the biopsy needle. The complications were classified as the minor or major according to the Society of Interventional Radiology Clinical Practice Guidelines’ criteria [10]. Diagnostic performance was evaluated by determining sensitivity, specificity, accuracy positive predictive value, and negative predictive value. The final diagnosis was based on by a pathologic examination of surgical specimens. For nodules in which no surgical resection was performed, the final diagnosis was based on the subsequent follow-up data on the basis of clinical and imaging follow-up for at least 12 months after biopsy. We compared the pneumothorax rate with v2 test, and diagnostic sensitivity and accuracy with Fisher’s exact test between the two group according to lesion size (B2 vs. [2 cm), with a P values \0.05 considered to indicate significant differences.
Data Collection and Statistical Analysis Data were assessed for number of pleural passes, technical success, procedure time, complications, and diagnostic performance. The number of pleural passes was defined as the operator attempted to directly puncture the pleura during one session. Technical success was defined as the acquisition of a tissue specimen adequate for pathological
Results The number of pleural passes was total 69 with single puncture for 66 nodules and two punctures for 3 nodules
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S. Liu et al.: Interventional Radiology Table 1 Final diagnoses of 69 solitary pulmonary nodules Diagnosis
Number of nodules
Malignant nodules Squamous cell carcinoma Adenocarcinoma
9 32
Small cell lung cancer
1
Metastatic tumor
4
Benign nodules Tuberculosis
6
Chronic inflammation
11
Fibrosis
2
Inflammatory pseudotumour
1
Squamous cell carcinomaa Adenocarcinomaa
1 1
Nondiagnostic nodules Squamous cell carcinoma Total a
1 69
False-negative case
Table 2 Pneumothorax rate and diagnostic accuracy based on nodule size Variables
Diameter
Pneumothorax rate Fig. 3 A 57-year-old woman who underwent MRI-guided percutaneous needle biopsy. A CT shows a 1.5-cm solid nodule in left lower lung lobe. B Sagittal image of T1-weighted FE shows the percutaneous procedure of biopsy needle (arrow). The needle biopsy result was lung inflammatory pseudotumour
during one session. The single puncture rate was 95.6 % (66/ 69). Technical success was achieved in all 69 procedures. The mean procedure time was 25.26 (range 19–48) min. Major complication occurred in one case of pneumothorax (4.8 %, 1/69) with chest tube placement because of enlarging pneumothorax (C30 %). There were 16 minor complications (23.2 %, 16/69), including 11 cases of small pneumothorax (15.9 %, 11/69) and 5 cases of mild hemoptysis (7.2 %, 5/69). All minor complications were selflimited without need of treatment. Pathological analysis of biopsy specimens showed 46 of 69 malignant nodules, 22 of 69 benign nodules, and 1 of 69 nondiagnostic nodules. In 42 (41 malignant and 1 benign) cases, surgical pathology was consistent with the biopsy results. Twenty-four (5 malignant and 19 benign) cases were confirmed by clinical follow-up. Two of 22 falsenegatives [adenocarcinoma (n = 1), squamous cell carcinoma (n = 1)] were confirmed by surgical pathology. one nondiagnostic sample was excluded from calculating diagnostic performance. The diagnostic performance was
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Diagnostic sensitivity Diagnostic accuracya
a
P
[2 cm
B2 cm
19.4 % (7/36)
15.2 % (5/33)
0.638b
95.8 % (23/24)
95.4 % (21/22)
1.000c
97.1 % (34/35)
96.9 % (32/33)
1.000c
a Diagnostic sensitivity and accuracy were calculated on basis of 68 biopsy results, excluding one nondiagnostic sample b
v2 test
c
Fisher’s exact test
as follows: sensitivity 95.8 % (46/48), specificity 100 % (20/20), accuracy 97.0 % (66/68), positive predictive value of 100 % (46/46), and negative predictive value of 90.9 % (20/22). Of one nondiagnostic nodule, postsurgical pathology revealed a squamous cell carcinoma (Table 1). Results for nodules B2 cm in diameter [n = 33; pneumothorax rate 15.2 % (5/33), sensitivity 95.4 % (21/22), accuracy 96.9 % (32/33)] were not statistically different from those for nodules [2 cm in diameter [n = 36; pneumothorax rate 19.4 % (7/36), sensitivity 95.8 % (23/ 24), accuracy 97.1 % (34/35)] (v2 test: P = 0.638; Fisher’s exact test: P = 1.000; Table 2).
Discussion CT-guided PTNB is a well-established and common method for cytological and pathological diagnosis of
S. Liu et al.: Interventional Radiology
pulmonary lesions in clinical practice. However, MR-guided needle biopsy has been as a guide tool and established as an option to more conventional means in selected indications including lung lesions. Sakarya et al. [9] first reported MR fluoroscopy-guided transthoracic fine-needle aspiration biopsy of lung masses that were 2–7 cm in diameter in 2003. MRI is not routinely used for evaluation of the lungs, mediastinum, or pleura in practice due to low proton density in the lung and the fast signal decay due to susceptibility artifacts at air–tissue interfaces [11]. However, MRI is an established alternative to CT for evaluation of the thoracic vasculature and mediastinal, hilar, and chest wall abnormalities [12]. MRI facilitates good soft-tissue contrast without contrast medium, has multiplanar capability, intrinsic flow sensitivity, near real-time imaging, and involves no ionizing radiation. The images can be acquired with short scan times with the breath-hold technique to guide the procedure of needle biopsy. The open device allows good access to the patients and has adequate space for interventional procedure. The Ipath200 optical system automatically and dynamically shows the needle route as a virtual overlay and gives precise navigation for insertion with a favorable efficiency profile. The MR-image quality of chest largely depends on the breath-hold duration and compliance of the patient. The patients were requested to hold their breath at the end of the normal expiration cycle as long as possible in order to avoid respiratory motion artifact during acquiring images. In our study, T1W FE was most commonly used for guiding the needle placement during the procedures with shorter acquisition time (12 or 18 s). If a patient could not tolerate well the breath-hold for 18 s, T1W FE sequence (three slices, 12 s) was used to shorten the patient’s breathhold time. If the visualization of nodule has interference from pulse artefacts on TW FE images, the T1W FSE sequence may be used for locating the nodule and planning the access. Although the image update delayed 12–21 s under low-field MRI system, the mean procedural time was 25.26 (range 19–48) min in this study, which was equal to CT guidance (23–37 min) [13–15] but longer than that of CT fluoroscopy (12.3–23.8 min) [14–16]. Compared with CT guidance, the longer acquisition time of the low-field MR system made us carefully select patients for PTNB. Major complications occurred in 1 case (4.8 % pneumothorax with chest tube placement) and minor complications occurred in 16 cases (15.9 % pneumothorax and 7.2 % hemoptysis) in our study. Pneumothorax is the most commonly reported complication of imaging-guided PTNB. In our study, the pneumothorax rate was 17.4 % (12/69) with one patient requiring chest tube insertion. It was at a relatively low level compared with reports in the previous literature of CT-guided PTNB in the diagnosis of SPNs (22–26 %) [13, 17–19]. This result might be
explained that the use of coaxial biopsy systems and tracking navigation decreased the number of passes through the pleura to reduce the frequency of pneumothorax and the necessity for chest tube placement. The single puncture rate was 95.6 % in our study. In our study, the cases that inserted a chest tube had two punctures, which could result in severe pneumothorax. A major disadvantage of MRI is that it cannot quickly identify pneumothorax; hence, chest radiographs or CT scans are obtained immediately or follow-up after operation. It is particularly emphasized that the plan of needle route should depend on CT images before the operation to avoid visible bullae and pulmonary fissure and to cross as few pleural surfaces as possible. In this study, the diagnostic accuracy (97 %) of the MRI-guided PTNB for SPNs compares parallelly with reported rates of CT-guided PTNB (81–99 %) [12, 16–18]. The target site must been selected in the suitable location to ensure obtaining representative and sufficient sample for the diagnosis. The needle path of sampling should not pass through the necrotic zone of lesion, which can increase the diagnosis of false-negative [20]. Two false-negative nodules diagnosed as inflammation by needle biopsy were proved to be malignancy by postsurgical pathology in this series. The samples might be obtained from the inflammatory tissue in the vicinity of the nodule. If the nodule tends to malignancy by characteristic of CT images, even though the diagnosis of biopsy is benign, further evaluation is required to determinate its nature as early as possible. Previous studies have found that the lesion size has a correlation with pneumothorax rate and diagnostic accuracy [21–23]; however, our results did not support these findings. We compared the pneumothorax rate and diagnostic accuracy between the two groups according to lesion size, and no statistically significant difference was seen. It might be related to the use of multiple plane imaging and tracing navigation system under MR guidance, which precisely localized the target nodule. Our study had limitations. First, the retrospective analysis may introduce a case-selection bias. Second, while the final diagnosis of surgical histopathology was only 45 nodules in all patients, 24 lesions required clinical and imaging follow-ups. In addition, the follow-up period was relatively short. SPN, such as atypical adenomatous hyperplasia or adenocarcinoma in situ, may persist without an internal change long after a 2-year follow-up period [24]. In conclusion, our study showed that MRI-guided PTNB is a safe, feasible, and highly accurate diagnostic technique for histopathologic diagnosis of pulmonary nodules. Conflict of interest All authors declare that we have no conflict of interest about this paper.
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