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1 All authors: Department of Radiology, Kyoto Prefectural University of Medicine, 465 Kajii, Kawaramachi-Hirokoji, Kamigyo, Kyoto, 602-8566, Japan.
Received June 7, 2002;
accepted after revision August 9, 2002.
Address correspondence to T. Yamagami.
Abstract
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SUBJECTS AND METHODS. One hundred thirty-eight percutaneous needle lung biopsy samples were obtained by two methods. The samples obtained by tissue fine-needle aspiration underwent cytologic evaluation, and those obtained by core biopsy using an automated cutting needle underwent histologic evaluation. The final diagnosis was confirmed by independent surgical pathologic findings, independent culture results, or clinical follow-up.
RESULTS. Rates of adequate specimens obtained and of precise diagnosis by combined use of fine-needle aspiration and core biopsy were 97.1% (134/138) and 94.2% (130/138) evaluated lung lesions, respectively, whereas those rates were 84.8% (117/138) and 79.7% (110/138) by fine-needle aspiration alone and 91.3% (126/138) and 89.1% (123/138) by core biopsy alone, respectively. Precise diagnosis was achieved by the combined use of the techniques in 30 (93.8%) of 32 lesions ranging from 3 to 10 mm in diameter, 42 (93.3%) of 45 lesions ranging from 11 to 20 mm, 43 (93.5%) of 46 lesions ranging from 21 to 30 mm, and 100% of 15 lesions ranging from 31 to 100 mm. In 89 of 90 lesions shown to be malignant by CT-guided lung biopsy and 30 of 44 shown to be benign, specific cell types could be proven from specimens obtained by the combined use of the two different types of needle biopsy.
CONCLUSION. The combined use of fine-needle aspiration and core biopsy improves the diagnostic ability of CT fluoroscopy—guided lung biopsy, even in small lesions.
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Most CT-guided lung biopsies described in earlier reports were performed with fine-needle aspiration for cytology and were useful in differentiating malignant from benign lesions [6, 7]. More recently, tissue core biopsy using an automated cutting needle, which enables the histologic evaluation of obtained samples [8,9,10], has been implemented, although it remains controversial whether cytology or histology is more useful in diagnosing lung nodules [6,7,8,9,10,11]. In efforts to improve the diagnostic ability of lung biopsy, several researchers have reported that the combined use of fine-needle aspiration and tissue core biopsy is helpful [12, 13].
In our institution, both fine-needle aspiration and tissue core biopsy under CT fluoroscopy guidance have been routinely performed during the same procedure with the objective of performing these procedures safely, correctly, and as rapidly as possible. Performing the two different biopsies during the same procedure was simplified through the use of CT fluoroscopy. The present study had two purposes. The first was to clarify whether the combination of fine-needle aspiration and tissue core biopsy results in an improvement in diagnosis of lung nodules compared with the single use of either biopsy. The second was to determine the value of CT fluoroscopy in performing two different percutaneous needle lung biopsies during a single procedure.
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Biopsy Procedures
A 21-gauge Sonopsy needle (Hakko, Nagano, Japan) was used for all
fine-needle aspirations, and a 20-gauge Auto Surecut needle (Create Medics,
Yokohama, Kanagawa, Japan) was used in 127 of the 138 tissue core biopsies.
For the other 11 core biopsies, either an 18- or 20-gauge Monopty needle
(Bard, Covington, GA) or an 18-gauge ASAP needle (Boston Scientific Japan,
Tokyo, Japan) was used.
All patients had undergone diagnostic CT of the chest with 10-mm-thick contiguous axial tomographic sections before the biopsy. At the time of biopsy, preliminary single-detector helical CT images were obtained in 5-mm-thick sections through the lesion. From a review of these preliminary images, the patient's position, the level of the site of needle entry, and the direction of approach for the biopsy were planned to provide the most direct route for biopsy, to traverse the least amount of aerated lung, and to avoid bullae and fissures. During biopsy, patients were in a supine (n = 64), prone (n = 56), or lateral (n = 18) position. The CT unit used was the X Vigor Laudator (Toshiba Medical Systems, Tokyo, Japan).
Each procedure was performed by one of three interventional radiologists experienced in CT-guided biopsy after informed consent had been obtained from the patient. A CT fluoroscopy imaging system was used for all CT-guided biopsy procedures. Details of CT fluoroscopy are described elsewhere [14]. The CT beam width was collimated to 3 mm. Imaging parameters during CT fluoroscopy included a CT beam width collimated to 3 mm, tube voltage of 120 kVp, tube current of 30-50 mA, and a scanning speed of 0.75 sec per rotation (360°).
Each CT-guided lung biopsy procedure was performed in a stepwise manner with quick application of CT fluoroscopy to confirm the path of the needle, while meticulous care was taken to minimize direct radiation to the operator's hands. Details of the biopsy procedure were described in our previous report [15].
Patients who could not cooperate with breath-holding underwent the procedure during usual respiration. After confirming that the needle tip had reached the lesion, the operator obtained a specimen and withdrew the needle. For all patients, fine-needle aspiration biopsy was performed first, followed by tissue core biopsy. When the operator was uncertain as to whether the needle tip reached the lesion or whether the specimen was sufficient, a repeated biopsy was performed. An on-site cytopathologist was not present during the procedure, and frozen-section analysis cannot be performed at the time of biopsy at our institution.
All biopsy procedures were performed with the patient under local anesthesia. After the biopsy procedure, axial CT images were obtained during a single breath-hold at the level of the biopsy site or, if necessary, through the whole chest using helical CT to evaluate for the presence of complications such as pneumothorax. While still on the scanner table, patients with a moderate or severe pneumothorax or with symptoms of pneumothorax underwent immediate manual aspiration of air from the pleural space with an 18-gauge IV catheter or placement of a chest tube, if necessary. The patients with pneumothorax were transferred to the recovery room where oxygen (100%) was administered by nasal cannula at a rate of 3 L/min.
Specimens obtained by fine-needle aspiration were evaluated cytologically, and those obtained by core biopsy were evaluated histologically. All cytologic and histologic evaluations were performed separately by different experienced chest cytopathologists. They were required not only to classify obtained specimens as showing positive or negative findings for malignancy but also to identify specific cell types (e.g., adenocarcinoma, small cell carcinoma) in cases of malignant lesions and to diagnose conditions (e.g., hamartoma and tuberculosis) in cases of benign lesions if possible.
Investigated Parameters
The ability to determine whether the lesion was malignant or benign and the
ability to characterize specific cell types in each category of lesion size
were compared among results of fine-needle aspiration biopsy alone, tissue
core biopsy alone, and the combination of both.
Statistical analysis was performed using Fisher's exact test to evaluate the differences among fine-needle aspiration alone, core biopsy alone, and combined use of these biopsy methods in the ability to differentiate a malignant from a benign lesion and to evaluate the difference between fine-needle aspiration and tissue core biopsy in the ability to obtain a specific diagnosis.
The final diagnosis was confirmed by independent surgical pathology (n = 72), independent culture results (n = 3), or clinical follow-up (n = 63). Clinical proof of a malignant lesion was accepted if the patient was treated for malignancy and the subsequent clinical course and response to therapy were appropriate. Clinical proof of a benign lesion was accepted if any of the following three conditions was satisfied: spontaneous resolution; resolution after treatment for conditions other than cancer, such as antibiotic treatment; and no change in the size of the lesion for more than 12 months.
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Of the 138 procedures, specimens adequate for cytopathologic evaluations were obtained in 134 (97.1%) either by fine-needle aspiration biopsy or by tissue core biopsy, in 117 (84.8%) by fine-needle aspiration alone, and in 126 (91.3%) by core biopsy alone (Table 1). The biopsy was deemed inadequate if specimens collected contained only blood or normal lung cells.
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The combined use of fine-needle aspiration and tissue core biopsy resulted in a higher rate of precise diagnosis than the use of either technique alone: 130 (94.2%) of 138 specimens were precisely diagnosed (true-positive, n = 90; true-negative, n = 40) by the combination, whereas 110 (79.7%) were precisely diagnosed by fine-needle aspiration alone and 123 (89.1%) by core biopsy alone. Separate analysis was done according to the size of the lesion (Table 1). For each size range, the rate of precise diagnosis was higher for the combination of procedures than for each method individually. However, the difference in the rate of precise diagnosis was particularly marked among the 32 lesions ranging in size from 3 to 10 mm, with rates of 71.9% (n = 23), 84.4% (n = 27), and 93.8% (n = 30) by fine-needle aspiration alone, core biopsy alone, and the combination of both techniques, respectively.
Frequency analysis of possible precise diagnosis resulting from each of the two diagnostic methods or both using Fisher's exact test is shown in Table 2. For the lesions that ranged from 3 to 10 mm, the rate of precise diagnosis resulting from the combination of fine-needle aspiration and core biopsy was significantly higher than that resulting from fine-needle aspiration alone (30/32 vs 23/32; p = 0.0217). Overall, precise diagnoses resulting from core biopsy alone and the combination of fine-needle aspiration and core biopsy were significantly higher than that resulting from fine-needle aspiration alone (p = 0.0227 and 0.0003, respectively). No significant difference was seen in other comparisons.
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In 90 lesions precisely diagnosed as malignant through the combination of fine-needle aspiration and tissue core biopsy for lung nodules under CT fluoroscopy guidance, 77 were diagnosed as malignant by both methods, but four were precisely diagnosed only by fine-needle aspiration biopsy and nine only by core biopsy (Table 3). On the other hand, of the 40 lung lesions precisely shown to be benign when we used the combination of fine-needle aspiration and core biopsy under CT fluoroscopy guidance, 26 were precisely revealed to be benign by both methods, three by only fine-needle aspiration biopsy, and 11 by only core biopsy (Table 3). Details of results analyzed according to tumor size of both malignant and benign lesions are also shown in Table 3. Incidentally, it should be mentioned that in six of seven lesions (malignant, n = 4; benign, n = 3) that were precisely diagnosed by fine-needle aspiration biopsy alone, it was only with core biopsy that specimens inadequate for evaluation were obtained.
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In 89 (98.9%) of the 90 lesions revealed to be malignant by CT-guided lung biopsy, specific cell types were clarified from analysis of specimens obtained with fine-needle aspiration biopsy alone (n = 4), core biopsy alone (n = 12), or both methods (n = 73) (Table 4). The rate of determination of cell type was significantly higher with core needle biopsy (85/90 [94.4%]) than with fine-needle aspiration biopsy (77/90 [85.6%]) according to Fisher's exact test (p = 0.0398). Specific cell types determined for primary malignant lesions were adenocarcinoma (3-10 mm, n = 8; 11-20 mm, n = 16; 21-30 mm, n = 21; 31-100 mm, n = 7), small cell carcinoma (3-10 mm, n = 1; 11-20 mm, n = 1; 21-30 mm, n = 4; 31-100 mm, n = 1), squamous cell carcinoma (11-20 mm, n = 4; 21-30 mm, n = 3; 31-100 mm, n = 3), malignant non-Hodgkin's lymphoma (31-100 mm, n = 1), and non—small cell carcinoma (11-20 mm, n = 2; 21-30 mm, n = 2). Cell types were identified in 15 metastatic malignant lesions (3-10 mm, n = 6; 11-20 mm, n = 6; 21-30 mm, n = 3). The origin of the metastatic lesions was colorectum (n = 8), breast (n = 4), eye (n = 1), ureter (n = 1), or parotid gland (n = 1).
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In 30 of the 44 lesions shown to be benign by CT-guided lung biopsy (including false-negative cases), specific cell types were determined in four from analysis of specimens obtained from fine-needle aspiration biopsy and in 30 from core biopsy (four overlapped) (Table 4). This rate of identification was significantly higher with core needle biopsy (30/44 [68.2%]) than with fine-needle aspiration biopsy (4/44 [9.1%]) according to Fisher's exact test (p < 0.0001). The specific cell types identified were granuloma (3-10 mm, n = 3; 11-20 mm, n = 3; 21-30 mm, n = 5), hamartoma (3-10 mm, n = 3), tuberculosis (11-20 mm, n = 1; 21-30 mm, n = 1; 31-100 mm, n = 1), mycobacterium nontuberculosis (3-10 mm, n = 1), pleuritis (11-20 mm, n = 1), adenomatous hyperplasia (11-20 mm, n = 1), aspergilloma (21-30 mm, n = 1), asbestosis (21-30 mm, n = 1), sarcoidosis (31-100 mm, n = 1), Wegener's granulomatosis (31-100 mm, n = 1), and nonspecific inflammation (3-10 mm, n = 1; 11-20 mm, n = 4; 21-30 mm, n = 1). The case diagnosed as adenomatous hyperplasia on CT-guided core biopsy was a false-negative; this lesion was revealed to be adenocarcinoma at surgery performed later. The remaining 29 cases were true-negative cases.
Regarding biopsy-induced complications, pneumothorax, which was the most frequent complication in the present study, appeared on CT images obtained immediately after biopsy in 45 (32.6%) of the 138 procedures. Immediate manual aspiration was performed in 21 of these patients, and further treatment with chest tube insertion was necessary in five (3.6%) of 138. In 35 patients (25.4%), parenchymal hemorrhage along the route of the advancing biopsy needle was revealed on CT images obtained after biopsy. In nine patients (6.5%), hemoptysis occurred after biopsy. Subcutaneous hematoma around the region of needle insertion occurred in one patient. None of the patients had serious complications.
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1.5 cm in diameter) and 96% for 70 larger lesions (>1.5
cm in diameter), a statistically significant difference. In a review of 89
consecutive patients who underwent percutaneous tissue core biopsy with an
automated cutting needle biopsy system, Lucidarme et al.
[9] found a lower but
statistically insignificant degree of accuracy for lesions 2.0 cm or smaller
compared with lesions larger than 2.0 cm (81%, 2.0 cm; 91%, >2.0 cm).
Tsukada et al. [10], using
CT-guided automated needle biopsy for lung nodules, also described a decrease
in diagnostic accuracy with decreases in lesion size. In their study,
diagnostic accuracy was as follows according to lesion size: 50-100 mm, 100%;
31-50 mm, 93.3%; 21-30 mm, 86.7%; 11-20 mm, 78.9%; and 6-10 mm, 66.7%. In the present study, the rate of precisely diagnosed cases (i.e., true-positive + true-negative) decreased. This decrease paralleled a decrease in lesion size if the evaluation was performed either by cytologic analysis of samples obtained by fine-needle aspiration alone or by histologic analysis of samples obtained solely by tissue core biopsy with an automated cutting needle. Only in lesions larger than 30 mm in diameter was the rate of precise diagnosis with core biopsy slightly lower than that of smaller lesions, which could have resulted from the small number of lesions in this category. On the other hand, if evaluation was performed from the combination of fine-needle aspiration and core biopsy, the rates of true-positive plus true-negative cases were high even as lesion size decreased.
In all size categories, lung lesions were more precisely diagnosed by combined use of fine-needle aspiration and tissue core biopsy than by the single use of either of these techniques. For example, 13 malignant lesions and 14 benign lesions were correctly shown to be malignant or benign by only one of the two procedures—that is, either by the fine-needle aspiration or tissue core biopsy. Thus, the use of the two different biopsy methods contributed to the accurate diagnosis in these cases. In other words, these lesions might have been incorrectly diagnosed if both fine-needle aspiration and core biopsy were not routinely performed for CT-guided lung biopsy.
Undoubtedly, the purpose of lung biopsy is to differentiate malignant from benign lesions. However, lung biopsy is also needed to determine the specific cell type, especially to discern whether the lesion is small or non-small cell carcinoma of the lung or metastasis, because treatment of lesions proven to be malignant by needle biopsy wll be selected on the basis of this information. When a lesion is proven to be benign, clarification of the specific cell type also may be necessary. Otherwise, for example, when a diagnosis of a biopsy sample is simply "negative for malignancy," long-term follow-up or biopsy with another procedure would be necessary [12] because in some cases, these lesions are found to be malignant at the second biopsy or on the follow-up study [2]. On the other hand, once the specific cell type of a benign lesion is clarified with biopsy, no further follow-up is required, which would minimize costs and inconvenience to the patient.
Specific cell types were identified in 89 (98.9%) of 90 lesions shown to be malignant using CT-guided needle biopsy in the present study. Among these 89 lesions, specific cell types in 73 lesions were diagnosed with both fine-needle aspiration and core biopsy; however, 16 (18.0%) were diagnosed with a single method (fine-needle aspiration alone, n = 4; core biopsy alone, n = 12). Of the 44 lesions diagnosed as showing negative findings for malignancy by needle biopsy (including false-negative cases), the specific cell types were determined in 30 lesions (68.2%). All benign lesions revealed by CT-guided biopsy were proven with core biopsy, but none by fine-needle aspiration alone.
The results of our study show that although the number of precise diagnoses of either a malignant or benign lesion is greater with core biopsy than with fine-needle aspiration when specimens are evaluated by a single biopsy method, the combination of the two different biopsy methods decreases the number of incorrect diagnoses. This combined use enabled us to differentiate small malignant and benign lesions, such as those less than 10 mm in diameter, as precisely as larger lesions. Also, from the point of view of clarifying specific cell types, especially in malignant lesions for which specific cell types were shown by either fine-needle aspiration or core biopsy at a moderate rate (i.e., 18.0% [16/89]) in the present study, the combined use of these biopsy methods would improve the quality of CT-guided lung biopsy, although in benign lesions the role of fine-needle aspiration is relatively small.
CT-guided lung biopsy has found wide-spread acceptance as a principal method of diagnosing lung nodules. The success rate in obtaining sufficient samples for cytohistologic evaluations (rate of adequate biopsy) has been reported to range from 80% to 100%, and its diagnostic accuracy has been described to be high, 81-96% [3, 9, 11, 16,17,18]. The most common complication of CT-guided lung biopsy is pneumothorax, with a frequency from 17.9% [3] to 54.3% [12] according to reports published in the past 10 years that included a large number of subjects [3, 12, 15, 18,19,20,21,22,23]. The average time for a CT-guided lung biopsy performed with conventional or helical CT has been reported to range from 22.7 min to approximately 1 hr [3, 10, 12, 17].
The technical success rate and frequency of biopsy-induced complications in the present study were similar to those in previous reports. Nevertheless, two different biopsies were performed during a single biopsy procedure, the mean number of punctures per procedure was few (average, 2.4) and the required time was short (average, 25.6 min), even though the time needed for management of complications, such as immediate aspiration for pneumothorax, was included. Furthermore, a high number of specimens that were sufficient for cytologic or histologic evaluation (or for both evaluations) were obtained (134/138 [97.1%] lesions), and the rate of diagnosis of whether a lesion was malignant or benign was also high (130/138 [94.2%]). In addition, the specific cell type was proven by needle biopsy in 119 lesions (86.2%).
We believe that these good results are mainly a result of the following two points: performing both fine-needle aspiration and core biopsy for a single lesion and advancing the needle tip toward the target lesions in real-time visualization under CT fluoroscopy guidance [4, 5, 14]. A higher rate of complications was reported to occur with the combined use of two types of biopsies compared with their single use in research by Klein et al. [12]; however, these researchers performed their study with techniques other than CT fluoroscopy and published their results when CT fluoroscopy was still rare. This problem may be almost resolved by performing a series of biopsy procedures more safely, more precisely, and more conveniently [4, 5] using real-time CT fluoroscopy.
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