Feasibility of Multiparameter MRI-Guided Percutaneous Biopsy for Central Lung Lesions With Atelectasis

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INTRODUCTION

Central lung cancer is usually located near the lung hilum, making surgical resection difficult. In such cases, obtaining a definitive pathological diagnosis and molecular profiling of the tumor are of utmost importance if radiotherapy, chemotherapy, biological targeted therapy, or immunotherapy are planned. Centrally located lung cancer often causes obstructive pneumonia, resulting in lung volume loss and subsequent atelectasis [1, 2]. Thus, distinguishing lung cancer from atelectasis is extremely important for determining the extent of the local tumor and targeting lesions for biopsy. Bronchoscopy is the most common method used for pathological diagnosis of central pulmonary lesions, and its sensitivity for detecting malignancies ranges from 82% to 94% [3, 4, 5, 6, 7]. However, the presence of atelectasis can influence the diagnostic accuracy of bronchoscopy for central lung cancer, even when endobronchial ultrasound-transbronchial needle aspiration (EBUS-TBNA) is used [3, 8]. Occasionally, primary lung lesions are associated with parenchymal consolidation with inflammatory or fibrotic reactions around the main tumor, rendering the tumor undistinguishable on ultrasound [3].

CT is the most widely used imaging method for patients with thoracic diseases. CT provides excellent spatial resolution; however, its inherently poor soft-tissue contrast limits its ability to distinguish some tumors from atelectasis, even with intravenous contrast [2]. PET-CT is excellent for detecting tumors within atelectasis, but its high radiation dose and cost limit its wide application [9, 10]. In comparison with CT, MRI provides excellent soft-tissue contrast, direct multiplanar capabilities, multisequence imaging, and functional imaging [11, 12, 13]. The ability to distinguish tumors from atelectasis has remarkably improved [14]. In this study, we prospectively evaluated the feasibility, accuracy, and safety of MRI-guided percutaneous biopsy for suspicious centrally located lung lesions with associated post-obstructive atelectasis.

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MATERIALS AND METHODS

Study Patients

The study plan was approved by the Institutional Review Board of Shandong Provincial Hospital (IRB No. SD NSFC 2015-277). Informed consent for both participation in the research study and undergoing the procedures was obtained from all patients, and the risks, benefits, and alternatives were explained to the patients in detail. The inclusion and exclusion criteria for this study are shown in Table 1, and the study flow diagram is presented in Figure 1. From July 2015 to December 2020, 113 patients were initially referred for MRI-guided biopsy on the basis of the inclusion criteria, and six patients were subsequently excluded on the basis of the exclusion criteria (severe emphysema, four cases; frequent cough, two cases). A total of 107 patients were enrolled in this study.

Fig. 1

Flow diagram for this study.

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Table 1

The inclusion and exclusion criteria for this study

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Equipment

We used a 1T open MRI scanner (Panorama HFO, Philips Healthcare, Best, The Netherlands) to guide percutaneous lung biopsy, a MR-compatible electrocardiogram monitor (MRGLIFE C PlusTM, Schiller Medical, Bern, Switzerland) to continuously monitor vital signs during the procedure, and a 16-G or 18-G MR-compatible coaxial needle (Wanlin Medical, Qingdao, China) and a 18-G or 20-G semi-automated cutting needle (TSK TM, TSK Laboratory, Tochigi-shi, Japan) to obtain core specimens. The details of these equipment are reported elsewhere [15].

MRI-Guided Biopsy Procedure

All biopsies were performed by two experienced interventional radiologists with more than five years of experience in interventional MRI.

Pre-Procedural Preparation

Preoperative imaging data were reviewed to locate the lesions, assess vascularity, and design the puncture path. The principles employed for designing the puncture approach included avoiding visible bullae and lung fissures and passing through the atelectasis to avoid puncturing the aerated lung to decrease the probability of pneumothorax. Patients were placed in the supine or lateral decubitus position based on lesion accessibility and the safest path to the lesion. The MRI protocols used for lesion localization and atelectasis identification included axial with sagittal/coronal fast T2-weighted imaging (T2WI)-turbo spin echo (TSE) (repetition time [TR], 2702 ms; echo time [TE], 90 ms; flip angle, 90°; slice thickness/separation, 5 mm/1 mm; field of view, 400 mm × 303 mm; matrix, 248 × 153; number of signal averages [NSA], 2; and acquisition time, 39 seconds) and enhanced fast T1-weighted imaging [T1WI]-TSE (TR, 576 ms; TE, 10 ms; flip angle, 90°; slice thickness/separation, 5 mm/1 mm; field of view, 350 mm × 302 mm; matrix, 176 × 115; NSA, 2; and acquisition time, 40.3 seconds). Fast T2WI-TSE usually shows post-obstructive atelectasis as tissue with a higher signal intensity than the central tumor, while enhanced fast T1WI-TSE shows atelectasis as tissue with a higher signal intensity than the central tumor. If atelectasis identification was not possible using these two sequences, diffusion-weighted imaging (DWI) sequences (TR, 1624 ms; TE, 73 ms; flip angle, 90°; slice thickness/separation, 5 mm/1 mm; field of view, 375 × 306; matrix, 108 × 87; b, 600 s/mm2; NSA, 2; and acquisition time, 2 minutes 54 seconds) were used for supplementary scans. The largest lesion diameter was measured on the transverse images. To minimize breathing artifacts, especially in lower lung lesions, a respiratory gating system was employed during image acquisition. The needle entry point was determined by MRI using a matrix grid made of fish oil capsules, the details of which have been previously reported [15]. The approach angle, the distance from the skin to the parietal pleura, and the distance from the skin to the lesion were measured.

Biopsy Procedure

The selected entry site was prepared and draped in a sterile fashion, and local anesthesia (1% lidocaine) was administered subcutaneously. An MR-compatible coaxial needle was gradually inserted into the lesion. Two-cross-sectional images (axial with sagittal or coronal images) of fast T2WI-TSE or enhanced fast T1WI-TSE were acquired to determine the actual needle direction and position (Figs. 2, 3, 4). Once needle-tip placement within the target lesion was confirmed, the table was removed from the MRI scanner. The internal stylet was removed, and the samples were drawn using a semi-automated cutting needle. Three to seven core biopsies were performed for each lesion. If the puncture passed through the lung parenchyma, normal saline (3–10 Ml) was instilled into the puncture access when the trocar needle was removed to seal the needle passage.

Fig. 2

A 61-year-old female with a lesion in the left upper lobe. A, B: Non-contrast-enhanced and contrast-enhanced CT did not allow reliable differentiation of tumors from the adjacent atelectasis. C: Fast T2-weighted imaging-turbo spin echo morphological MRI performed at the same level shows post-obstructive atelectasis (long arrow) with a higher signal intensity than the central tumor (short arrow), reflecting a higher water content. D: MRI-guided puncture needle in the lesion. The biopsy specimen revealed an adenocarcinoma.

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Fig. 3

A 72-year-old male with a lesion in the right upper lobe. A: Fast T2WI-TSE shows a lesion with heterogeneous signal intensity in the right upper lobe; however, the lesion cannot be easily distinguished from atelectasis. B: Diffusion-weighted imaging clearly depicts the difference in water restriction between the tumor tissue (short arrow) and the collapsed lobe (long arrow). C, D: Enhanced fast T1WI-TSE displays hyperintense atelectasis (long arrows) and hypointense lesions (short arrows) in transverse (C) and sagittal images (D). E, F: Multiplanar MRI-guided puncture of the lesion. The biopsy specimen revealed small cell carcinoma. WI = weighted imaging, TSE = turbo spin echo

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Fig. 4

A 54-year-old male with a lesion in the right middle lobe. A, B: Fast T2-weighted imaging-turbo spin echo transverse image (A) and coronal image (B) show post-obstructive atelectasis (long arrows) with a higher signal intensity than the central tumor (short arrows). The ability to perform multiplanar imaging and needle insertion at any angle facilitated the selection of an optimal puncture path to reduce the risk of pneumothorax (B). The biopsy specimen revealed squamous cell carcinoma.

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Post-Procedural Evaluation

Histological cores were fixed in 10% neutral buffered formalin for hematoxylin and eosin and immunohistochemical staining, if necessary. No rapid on-site cytopathological examinations were performed. The procedural time (the interval between the first acquisition and removal of the needle) was recorded. Immediately following biopsy, PD-weighted TSE with respiratory gating (TR, 1575 ms; TE, 30 ms; flip angle, 90°; slice thickness/separation, 5 mm/1 mm; field of view, 350 mm × 299 mm; matrix, 220 × 176; NSA, 2; and acquisition time, 1 minute 3 seconds) was employed to check for pneumothorax; and chest radiography or CT was performed 24 hours later. If a small asymptomatic pneumothorax was present, conservative treatment was administered with monitoring of vital signs and administration of supplemental oxygen. If a large (lung surface retraction ≥30%) or rapidly expanding pneumothorax developed, a pleural drain was inserted. Pneumothorax, pleural drainage, hemoptysis, and other possible complications were recorded.

Data Analysis

Technical success was defined as the acquisition of a tissue specimen adequate for pathological analysis. The specific histological types of the samples were recorded. Final diagnoses were determined by surgical confirmation or clinical follow-up results for at least 24 months. A final diagnosis of negative for malignancy was made when any of the following conditions were met: 1) no malignant tumor was identified during surgery, 2) spontaneous regression of the lesion occurred, 3) no lesion growth was found on subsequent follow-up imaging for more than 24 months, and 4) resolution of the lesion occurred after treatment for conditions other than cancer.

The diagnostic accuracy, sensitivity, specificity, positive predictive value, and negative predictive value of percutaneous biopsy for diagnosing lung malignancies were calculated by comparison with the final diagnoses. Complications were classified as minor or major according to the Society of Interventional Radiology Clinical Practice Guidelines’ criteria.

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RESULTS

Patient Characteristics

The characteristics of the study patients and lung lesions are summarized in Table 2. One hundred and two patients underwent contrast-enhanced CT within 2 weeks before the biopsy procedure, and five patients underwent non-contrast CT due to iodine contrast media allergy (three cases) or renal insufficiency (two cases). The central lesions could be distinguished from post-obstructive atelectasis with CT in 62 patients, but were difficult to distinguish in 45 patients. In 33 and 16 patients, respectively, bronchoscopy- and CT-guided biopsies had previously failed to yield adequate samples or provided indeterminate results. The remaining patients had not undergone lung biopsy by bronchoscopy or CT. All patients were hospitalized.

Table 2

Characteristics of patients and lung lesions (n = 107)

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MRI Findings

In the 107 patients, 96 (89.7%) could be clearly distinguished from post-obstructive atelectasis by multiparameter MRI (central lesion diameter, 1.9–5.6 cm; mean diameter, 3.1 ± 1.0 cm). In 89 cases, lesions were distinguished from atelectasis using fast T2WI-TSE and enhanced fast T1WI-TSE, and the distinction could be performed using only fast T2WI-TSE in 72 patients. The remaining seven cases required DWI. Forty-one patients had central lesions with post-obstructive atelectasis in the entire lobe, and 55 had lesions with segmental or local post-obstructive atelectasis. No typical MR findings of central lesions with atelectasis were observed in the other 11 patients (whole-lesion diameter, 6.7–11.3 cm; mean diameter, 8.2 ± 1.3 cm) (Fig. 5).

Fig. 5

A 66-year-old male with a lesion in the right upper lobe. The bronchoscopy results were negative. A, B: Non-contrast CT (A) and enhanced CT (B) show suspicious central lesions with atelectasis. C-E: However, no typical imaging features are observable on fast T2-weighted imaging-turbo spin echo (C), enhanced fast T1-weighted imaging (D), and diffusion-weighted imaging (E). F: Multiplanar MRI-guided puncture of the lesion. The biopsy specimen revealed an adenocarcinoma.

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MRI-Guided Biopsy Results

One hundred and seven suspicious central lung lesions with associated post-obstructive atelectasis in 107 patients were biopsied using MR-guided percutaneous coaxial cutting biopsy. The procedural characteristics are summarized in Table 3. All patients tolerated the MRI-guided percutaneous biopsy procedure well. Adequate specimens for diagnosis were obtained from all the patients, with a technical success rate of 100%. The biopsy procedure time, which was defined as the interval from pre-procedural MRI until needle removal, varied from 27 to 67 minutes (mean, 36.7 ± 8.7 minutes). Of the 107 lesions, 98 were malignant and nine were benign on MRI-guided biopsy. Finally, 101 malignant and six benign lesions were confirmed on the basis of surgical histopathological results (n = 25) or clinical follow-up findings (n = 82). Among the 49 patients who had previously received negative results for malignancy from bronchoscopic biopsy or CT-guided percutaneous biopsy, 47 showed positive results in MRI-guided percutaneous biopsy.

Table 3

Procedural characteristics of MRI-guided percutaneous biopsy

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Among the 101 malignant lesions, 98 were diagnosed as true-positive and three as false-negative by percutaneous MRI-guided biopsy (Table 4). The first false-negative case was diagnosed as proliferative fibrous tissue by percutaneous biopsy; however, surgical resection was performed, and the histopathological diagnosis was squamous cell carcinoma. In the second case, chronic pulmonary inflammation with atypical hyperplasia of the alveolar epithelium was diagnosed using percutaneous biopsy, and EBUS-TBNA after three months confirmed squamous cell carcinoma. The third patient was diagnosed as showing pulmonary fibrosis with chronic inflammation by percutaneous biopsy; however, subsequent surgical histopathology confirmed an adenocarcinoma. Among the other six patients in this study who received a negative diagnosis through MRI-guided biopsy, one patient with pulmonary tuberculosis was cured after anti-tuberculosis therapy, two patients with chronic inflammation showed significant improvement after anti-infection treatment, and three patients with fibrous tissue exhibited no remarkable changes during a follow-up period of over 24 months.

Table 4

Characterization of specific type of percutaneous biopsy and final diagnoses

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The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of MRI-guided percutaneous biopsy for diagnosing lung malignancy were 97.0% (98/101), 100% (6/6), 100% (98/98), 66.7% (6/9), and 97.2% (104/107), respectively. Self-limiting hemoptysis occurred in three patients (2.8%, 3/107). Pneumothorax occurred in five patients (4.7%, 5/107), of which none required pleural drainage. No serious procedure-related complications occurred.

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DISCUSSION

Because biopsy provides only small tumor fragments, the most suspicious areas should be identified to obtain sufficient tumor-representative materials for analysis [16]. In this study, multiparameter MRI was used as a guidance method to distinguish between tumors and atelectasis in most cases. MRI-guided percutaneous biopsy for diagnosing lung malignancy showed an accuracy of 97.2% for suspicious centrally located lung lesions with associated post-obstructive atelectasis, and no serious procedure-related complications were observed.

Although evaluation of the lungs by MRI is limited by the low proton density of normal lung tissue, respiratory motion, and cardiovascular pulsation artifacts, MRI provides unparalleled soft-tissue contrast, multiparameter imaging, and functional imaging to reflect tissue heterogeneity [11, 14, 17, 18]. On T2WI, atelectasis and post-obstructive pneumonia often exhibit higher signal intensities than the central tumor. Previous studies have reported that approximately 70%–80% of cases can be identified on T2WI [1, 2, 19, 20]. In contrast, atelectasis is characterized by lung collapse. In comparison with normal lung parenchyma, atelectasis tissue shows more blood vessels per volume than normal lung tissue. Therefore, atelectasis usually shows a higher signal intensity than the central tumor on contrast-enhanced T1WI, which may help distinguish obstructive atelectasis from lesions. In this study, fast T2WI-TSE and enhanced fast T1WI-TSE sequences were preferentially used to locate lesions, and these sequences could successfully distinguish atelectasis in 89 patients; in 72 patients, atelectasis was distinguishable using only fast T2WI-TSE. If these two sequences could not conclusively distinguish lesions and atelectasis, DWI was used for supplementary scanning. Previous reports have shown that DWI is feasible for distinguishing lung cancer from post-obstructive lung collapse, and that pre-procedural DWI is helpful in identifying biopsy targets [2, 21, 22, 23, 24]. In our study, DWI facilitated the diagnosis of seven additional lesions that could not be determined using T2WI-TSE and enhanced T1WI-TSE. In addition, the ability to arbitrarily choose the imaging plane in MRI is very important for successful location of lesions and for clearly and intuitively displaying lesions with atelectasis in coronal or sagittal images. This study achieved high diagnostic accuracy, which is closely related to the precise determination of the tumor location by multiparameter MRI, and effectively avoided the interference of atelectasis on the puncture target.

CT is the preferred imaging modality for percutaneous lung biopsy. Previous studies have shown that dynamic enhanced CT scans can distinguish between central pulmonary tumors and atelectasis in 80% of the cases [25]. However, in one study, lung cancer and atelectasis were identified in only 42% of cases using bolus-enhanced CT [2]. Moreover, CT-guided percutaneous biopsies are usually performed under non-enhanced scanning conditions. Even enhanced scanning can only provide a transient differentiation effect. When CT fails to distinguish between atelectasis and tumors, performing PET/CT and MRI before CT-guided biopsy may be beneficial. However, identifying the target during CT-guided biopsy based on preoperative PET/CT or MR results is clearly less accurate than continuously determining the relationship between the puncture needle and the target during MRI-guided biopsy.

In comparison with CT and ultrasound, MRI is time-consuming when performing percutaneous biopsies. The long procedure time limits the usability of MRI guidance for procedures involving aged patients and those with a poor constitution, especially when local anesthesia is used. In our study, the procedure time was relatively short, ranging from 27 to 67 minutes (mean, 36.7 ± 8.7 minutes). Several measures were employed to shorten the procedure time. First, a fast scan sequence (fast T2WI-TSE: 39 seconds; fast T1WI-TSE: 40.3 seconds) was used to replace the conventional diagnostic sequence (conventional T2WI-TSE: 3 minutes; conventional T1WI-TSE: 2 minutes 58 seconds), which reduced the acquisition time while ensuring sufficient imaging quality. Second, although DWI has been reported to be of great value in distinguishing tumors from atelectasis, it can be time-consuming (2 minutes 54 seconds) and is susceptible to artifacts caused by chemical shifts, phase-encoding direction, the puncture needle, and respiratory and cardiac motions [20]. Thus, its use should usually be considered for partial lesions that cannot be clearly distinguished on fast conventional sequences. Consequently, it was not routinely used for all patients in our study. Finally, because MR pulmonary imaging is susceptible to respiratory motion artifacts, respiratory gating is often used to facilitate image acquisition, especially in the lower lungs [15]. However, this significantly extends the procedural time. Therefore, we only used respiratory gating to locate the lesion before the procedure and to determine the final position of the puncture needle, rather than actual guidance. This reduced the time required for respiratory gating.

Because the central lesion is adjacent to the hilum, avoidance of vascular injury during the procedure is the key to safety. The flowing void effect of MRI clearly shows the relationship between the lesion and pulmonary vessels without the need for a contrast agent; thus, the operator can avoid puncturing the vessels during the procedure, reducing the risk of vascular injury. In this study, only three patients experienced self-limiting hemoptysis, and no serious bleeding complications occurred. In addition, MRI can be advantageous for evaluating patients with adverse reactions to intravenous contrast or impaired renal function [14]. Pneumothorax is the most common complication of percutaneous lung biopsy [26]. The incidence of pneumothorax was low in the present study (4.7%). The puncture approach was optimized to pass through the atelectasis tissue as much as possible to avoid pneumothorax. If the puncture passed through normal lung parenchyma, normal saline was injected into the needle passage to seal the needle passage. The literature indicates that sealing the puncture access with saline can significantly reduce the incidence of pneumothorax and prevent subsequent chest tube placement after percutaneous lung biopsy [27, 28].

Our study had three important limitations. First, “gold standard” surgical pathology was performed after percutaneous biopsy in only a small number of patients (25 patients) since most patients had advanced lung cancer, small cell cancer, or advanced age. Second, we did not perform direct comparisons with CT- or bronchoscopy-guided biopsy. Third, the low proportion of patients with pneumothorax in this study may be related to the fact that not all cases were confirmed on CT.

In conclusion, multiparameter MRI allowed distinction of central lung tumors from atelectasis and facilitated accurate and safe guided percutaneous biopsy. MRI-guided percutaneous biopsy may be of value in the diagnosis of central lung disease with associated atelectasis, especially when contrast-enhanced CT yields unclear results and when bronchoscopy fails or shows negative results. Future studies should aim to compare MRI-guided percutaneous biopsy with CT-guided percutaneous biopsy and bronchoscopic biopsy.

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