Diagnostic Sensitivity of Ultrasound-Guided Needle Biopsy in Soft Tissue Masses About Superficial Bone Lesions

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1 Diagnostic Sensitivity of Ultrasound-Guided Needle Biopsy in Soft Tissue Masses About Superficial Bone Lesions Kee-Min Yeow, MD, Chih-Feng Tan, MD, Jen-Shi Chen, MD, Cheun Hsueh, MD We evaluated the value of ultrasound-guided needle biopsy in 20 soft tissues masses about superficial bone lesions in 20 oncology patients. Sonographically guided needle biopsies were performed without an on-site pathologist. A diagnostic sensitivity of 95% and specificity of 100% in separating a benign or a malignant lesion was obtained. Fine needle aspiration cytology allowed the specific cell type of malignancy to be diagnosed in 80% of cases, while core needle biopsy allowed it in 91%. Real-time ultrasonographic guidance permits precise needle placement into the targets, avoidance of hypervascular areas, and flexibility of patient positioning so that needle biopsy can be performed quickly and safely on soft tissue masses about superficial bone lesions. KEY WORDS: Bone, neoplasm; Needle biopsy; Masses, soft tissue. Image-guided needle biopsy of bone lesions generally is performed under fluoroscopic or CT guidance. 1 For soft tissue masses about ABBREVIATIONS CT, Computed tomography; FNA, Fine needle aspiration; FNAC, Fine needle aspiration cytology Received January 28, 2000, from the Departments of Diagnostic Radiology (K.-M.Y., C.-F.T.), Oncology (J.-S.C.), and Pathology (C.H.), Chang Gung University, Chang Gung Memorial Hospital, Taiwan. Revised manuscript accepted for publication August 14, Address correspondence and reprint requests to K.M. Yeow, MD, Department of Diagnostic Radiology, No. 404, 11th Floor, Chang Gung Medical Community Village, Kwei Shan, Tao Yuan 333, Taiwan. superficial bone lesions, a needle biopsy guided by fluoroscopy or CT is cumbersome because of the poor stability of needle in the shallow tissue tract. Awkwardness of the needle manipulation during a fluoroscopic or CT-guided biopsy can result in an accidental puncture of the underlying organ. A patient is expected to lie stationary for a period of time, from target localization to the actual needle puncture during a CT-guided needle biopsy procedure, which may last approximately 30 min. The difficulty and risk of a CT-guided needle biopsy increases in clinical ill patients, as the underlying bone pain may prevent patients from staying still. Any complication resulting from a needle biopsy may be detrimental to this group of patients. Realtime ultrasound-guided needle biopsy, on the other hand, provides a much more flexible patient positioning. Interval change in the patient s position is acceptable. However, ultrasonography is used infrequently to guide a bone biopsy owing to its lack of 2000 by the American Institute of Ultrasound in Medicine J Ultrasound Med 19: , /00/$3.50

2 850 NEEDLE BIOPSY OF MASSES ABOUT BONE LESIONS J Ultrasound Med 19: , 2000 depth penetration of soft tissue and its inability to penetrate bone cortex. 1,2 Two reported series 3,4 obtained diagnostic sensitivities of 93% and 87.5% for superficial bony destructions using only FNAC. In our experience, a core needle specimen may occasionally be needed when FNA did not obtain an adequate specimen to provide a definite pathologic diagnosis. In this report we evaluate the sensitivity and safety of ultrasound-guided needle biopsies (11 FNAC, 11 core needle biopsies) for soft tissue masses about superficial bone lesions (mostly nonpalpable) overlying the vital organs in 20 oncology patients. PATIENTS AND METHODS From January 1995 to June 1999, 20 consecutive patients (10 male, 10 female; age range, 26 to 70 years; mean, 56.8 years) who were found to have soft tissue masses about superficial bone lesions initially detected by CT were referred by an oncologist for ultrasound-guided needle biopsy after consultation with the interventional radiologist (K.M.Y). Ultrasound was selected for guiding needle biopsy on soft tissue masses about superficial bone lesions because we have encountered some difficulty in stabilizing a cutting needle when CT guidance was used in previous biopsies. Using ultrasound as guidance, the operator could hold a needle in one hand and the ultrasound probe in the other. One interventional radiologist (K.-M.Y.) performed all the needle biopsies. When multiple bone lesions were noted on CT, soft tissue masses about superficial bone lesions that were located less than 5 cm from the skin surface were selected arbitrarily as targets for echo-guided needle biopsy. The soft tissue masses about superficial bone lesions as revealed by CT scans were further evaluated with a 7.5 MHz high-resolution ultrasound probe (Acuson, Mountain View, CA). No standoff pad was used. The soft tissue masses about superficial bone lesions were examined carefully by noting their echogenicity in relation to surrounding muscles (how well they stand out from their surroundings), their thickness, and whether the underlying bony cortex was intact, eroded, or destroyed. The size of the target lesions was recorded. The skin around the targeted area was sterilized, and an incision was made with a #11 scalpel blade after local injection of anesthetic agent. Needle biopsies were performed directly on the soft tissue masses about the superficial bone lesions by using either a 23 gauge hypodermic needle (11 patients) or a 16 to 18 gauge cutting needle (11 patients) (Temno, Bauer Medical, Clearwater, FL) using a free-hand technique. We did not attempt to penetrate an intact bone cortex unless the ultrasound beam was able to resolve the soft tissue beyond an attenuated cortex. At least two passes were performed for FNAC, and at least two tissue specimens were obtained when core needles were used. Confirmation of needle paths within the soft tissue lesions was obtained in all patients. A physician s assistant routinely compressed the puncture sites immediately after the biopsy procedure for about 10 min. After a short period of observation outside our ultrasound laboratory, the patients were routinely asked if they felt increased pain over the biopsy sites, and the puncture sites were checked by the interventional radiologist for evidence of local swelling. If the patient had any questionable local discomfort or swelling accompanied by local tenderness, he or she was scanned with ultrasound for evidence of increased swelling, fluid collection, or hematoma formation along the biopsy needle paths. The procedure time from initial high-resolution ultrasound evaluation to completion of needle biopsy for FNAC was about 7 min, whereas core needle biopsy took about 15 min. The cellular smears and tissue specimens obtained were sent for pathologist s review. No immediate cytologic evaluation was performed by a pathologist. The type of needle selected was based primarily on the thickness of the targeted soft tissue mass lesions. A minimum thickness of 2 cm is be needed to permit the use of a cutting needle that has a standard cutting trough measuring 1.7 cm in length. The selection of a core needle as the initial needle biopsy technique, however, depended on a number of factors. Core needle biopsy was selected as the preferred biopsy technique when (1) the targeted lesion had a soft tissue component greater than 2 cm in depth, (2) the pathologic diagnosis of a primary tumor occurring elsewhere was unknown at the time of needle biopsy, (3) the initial FNAC failed to provide a tissue-specific diagnosis or the FNAC result was ambiguous, (4) a large tissue sample was needed for better characterization of tumor tissue and histochemical staining. Hypervascularity of the target lesions was not a contraindication for the use of a core needle, as color flow mapping was routinely used to avoid any obvious feeding artery or draining vein. The pathologic diagnoses obtained by ultrasoundguided needle biopsies were compared with known causes of pathology at primary sites to correlate for agreement in cellular or histologic pattern. When pathologic specimens of masses from primary sites were not available for comparison with specimens obtained by needle biopsies, the classic radiologic diagnoses associated with distant metastases were

3 J Ultrasound Med 19: , 2000 YEOW ET AL 851 used as standards for establishing the diagnoses of malignancies. Thus, the pathologic or classic radiologic diagnoses of primary site masses and the clinical follow-up of the course of primary masses were used as the gold standards for calculation of sensitivity of ultrasound-guided needle biopsy. In patients without a known primary malignancy, the classic radiologic diagnoses and clinical response of the soft tissue masses about superficial bone lesions to appropriate chemotherapeutic agents were used as diagnostic standards of comparison. The sensitivity and specificity of ultrasonographically guided needle biopsy were calculated using 2 2 contingency tables. RESULTS All 20 patients tolerated the needle biopsy procedures well. Thirteen patients (65%) had undiagnosed tumor masses elsewhere in the body, which were difficult to access by needle biopsy due to the patients poor clinical status. In 14 patients (70%), the soft tissue masses about the superficial bone lesions were not palpable. The target lesions were visible sonographically either as cortical disruptions, soft tissue masses about an intact bone cortex (Figs. 1 to 3), hypoechoic masses, or soft tissue tumors about destructive bones. A relatively hypoechoic soft tissue mass in relation to adjacent muscle was the most frequent sonographic finding, and this was seen in 19 lesions; of these, 3 masses were hypervascular. The soft tissues about superficial bone lesions were located in skull (2 cases), rib (10 cases), clavicle (two cases), scapula (2 cases), iliac bone (2 cases), mandibular condyle (1 case), and sacrum (1 case). Nine patients underwent FNA, nine had cutting needle biopsy, and two patients who had initial FNA had repeat cutting needle biopsies performed for tissue confirmation. In four patients, only FNAC was possible because the soft tissues about minor irregular bone cortices were too shallow for the insertion of cutting needles. Two patients with ambiguous FNAC results required repeat core needle biopsies for tissue confirmation. The average procedure time for FNAC was about 7 min and for core needle biopsy was about 15 min. All tissue samples obtained by FNA and cutting needle biopsies were satisfactory for review by a pathologist. The soft tissue masses about superficial bone lesions were malignant in 19 patients and benign in 1. The diagnoses were 17 metastatic s, 1 malignant lymphoma, 1 fibrosarcoma, and 1 benign bone marrow aspirate (from a forgotten rib trauma with residual expansile lytic lesion in a patient with colon cancer). Twenty-one of 22 ultrasound-guided soft tissue needle biopsies of soft tissue masses about bone lesions allowed benign versus malignant to be distinguished (1 core needle biopsy required CT-guided core biopsy for diagnosis), resulting in a diagnostic sensitivity of 95% and specificity of 100% in separating benign and malignant lesions. FNAC allowed all malignancies to be diagnosed (100%), but only 8 of 10 FNAC permitted a specific diagnosis of cell type of malignancy (2 required ultrasound-guided core biopsy). One of these FNAC findings, in a mass about a destroyed rib, was a spindle cell malignant tumor of uncertain nature; repeat core needle biopsy revealed a primary spindle cell sarcoma. Another FNAC result in a mass about an expansile and destructive sternum was suggestive of a poorly differentiated metastatic ; repeat core needle obtained sufficient tissue for further histochemical staining, which confirmed an anasplastic large cell lymphoma. As a result, FNAC allowed diagnosis of 80% (8 of 10), whereas core needle biopsy allowed diagnosis of 91% (10 of 11) specific cell types of malignancy. Biopsy of a soft tissue mass about an iliac bone lytic lesion revealed only fibrotic tissues and muscle fragments. A repeat percutaneous needle biopsy under CT guidance revealed a metastatic transitional cell cancer from an occult urinary bladder cancer, which was confirmed on subsequent cystoscopy study. The pathologic results obtained by ultrasound-guided needle biopsy are listed in Table 1. No complications related to the ultrasound-guided needle biopsies occurred. Figure 1 A 26 year old man with nasopharyngeal cancer had just completed radiation therapy. A left chest wall tender bulge was felt. Contrast-enhanced chest CT reveals a focal asymmetry (arrow) over the anterolateral aspect of left fourth rib. No bone destruction is noted.

4 852 NEEDLE BIOPSY OF MASSES ABOUT BONE LESIONS J Ultrasound Med 19: , 2000 A B Figure 2 A, Same patient as in Figure 1. High-resolution ultrasound study reveals a hypoechoic soft tissue lesion (arrows) over the anterior aspect of the apparently intact rib cortex (R). B, A sonogram of an adjacent rib structure of the same patient with a magnification similar to that in A shows a normal thin layer of hypoechoic musculature (arrows) overlying the reflective hyperechoic bone cortex (R). DISCUSSION In this study of 20 consecutive patients with soft tissue masses about superficial bone lesions, which were within 5 cm from skin surface, ultrasoundguided needle biopsy was effective in obtaining a tissue sample in 21 of 22 biopsies. Ultrasound-guided needle biopsy is monitored in a real-time fashion; thus, a more precise tissue sampling is facilitated. Ultrasonographic guidance also is helpful in directing needle biopsy of a necrotic tumor, as it helps to guide the needle to the solid component. In our series, only two needle passes (either with a fine needle or a cutting needle) were needed as ultrasound provided a clear target for needle biopsy. Areas of hypervascularity found in three metastatic hepatocellular s were avoided with the help of color Doppler flow mapping when they were sampled using core needles. No immediate bleeding complication was encountered in this series. Needle biopsy of soft tissue masses about superficial bone lesions occurring in more complex anatomic locations, such as small, round, and shallow structures in the skull or rib, can be difficult to perform when CT or fluoroscopic guidance is used. In these areas, accidental slippage of the biopsy needle during needle positioning may cause injury to the brain or the lung. 3,4 In contrast, patient positioning is very flexible when ultrasound guidance is used. Interval change in patient position is much more tolerable during ultrasound-guided needle biopsy than during CT guidance. In ultrasoundguided needle biopsy of soft tissue masses about superficial bone lesions, patients need not hold their breaths during needle excursion or firing. The technique should be widely applicable as long as the lesion can be demonstrated by ultrasound. Much debate has occurred on the diagnostic accuracy of FNA or core biopsy technique, but most authors believe that the results obtained by these techniques are complementary to one another. 5,6 However, in certain sarcomas, poorly differentiated s, and lymphomas, uncertainty in cytologic diagnosis may be encountered if FNAC alone is Figure 3 Cross-sectional high-resolution sonogram of the same lesion as in Figure 2B shows a fine needle (arrow) entering the hypoechoic paraosseous soft tissue lesion. Cytology result revealed a metastatic poorly differentiated, which has the same pathologic pattern as the original nasopharyngeal cancer. R, Cortex of the rib.

5 J Ultrasound Med 19: , 2000 YEOW ET AL 853 Table 1: Results of Ultrasonographically Guided Needle Biopsy in 20 Soft Tissues Masses About Superficial Bone Lesions Age (yr), Site and Size Known Primary Lesions Needle Used Final Pathologic or Sex of Masses (cm) at Time of Needle Biopsy (FNAC/Core) Clinical and Image Diagnosis 78M Skull, 2.2 cm Liver tumor 18 gauge, core Metastatic hepatocellular 46M Skull, 1.5 cm Nasopharyngeal 18 gauge, core Metastatic poorly differentiated nasopharyngeal 61F Mandibular condyle, Colon 23 gauge, FNA Metastatic colon adeno 2 cm 66M Clavicle, 10 cm Liver tumor 18 gauge, core Metastatic hepatocellular 63F Clavicle, 1.5 cm Lung tumor 23 gauge, FNA Metastatic non small cell lung 57F Scapula, 2.5 cm Breast 16 gauge, core Metastatic breast adeno 30M Sternum, 5 cm No 23 gauge, FNA; Anaplastic large cell lymphoma 16 gauge, core 64 F Rib, 7 cm No 23 gauge, FNA; Rib spindle cell sarcoma 16 gauge, core 70F Rib, 10 cm Lung tumor 23 gauge, FNA Metastatic lung squamous cell 50F Rib, 5 cm Lung tumor 14 gauge, core Metastatic lung squamous cell 66M Rib, 4 cm Lung tumor 23 gauge, FNA Metastatic poorly differentiated 54F Rib, 6 cm Colon 23 gauge, FNA Benign 53M Rib, 2.7 cm Lung 23 gauge, FNA Metastatic lung adeno 32M Rib, 4.4 cm Esophageal squamous 23 gauge, FNA Metastatic squamous cell cell of esophagus 71M Rib, 5 cm Hepatocellular 16 gauge, core Metastatic hepatocellular 69M Rib, 7 cm Thymic tumor 18 gauge, core Metastatic thymic 26M Rib, 8 cm Nasopharyngeal 23 gauge, FNA Metastatic poorly differentiated 40M Sacrum, 3 cm Parotid adenocystic 18 gauge, core Metastatic adenocystic 65F Iliac bone, 6.5 cm No 16 gauge, core Poorly differentiated transitional cell 56M Iliac bone, 2 cm No 23 gauge, FNA Metastatic of unknown origin performed. 5 We use a core needle for repeat biopsy whenever possible if the initial cytologic specimen was adequate but the pathologic diagnosis was ambiguous. We also use a core needle for obtaining tissue specimen when there was no prior pathologic diagnosis of an existing dominant tumor in another part of the body so that detail classification of the primary tumor can be made. 7 When a primary bone tumor is suspected, a core needle biopsy is preferred over FNA, as it has a higher reported diagnostic accuracy of 76 to 96%, in comparison to the accuracy of FNAC, which can be as low as 54%. 7 An additional advantage of core needle biopsy is that tissue specimens obtained can be kept in a paraffin block, which can be used for further histochemical analysis. 8 In two of our cases in which the initial FNAC revealed malignancies of uncertain nature, the final diagnoses obtained by core biopsies confirmed a sternal lymphoma and a primary rib sarcoma after special histochemical staining. The core needle specimens obtained from such soft tissues about superficial bone lesions permitted the pathologist to give an accurate

6 854 NEEDLE BIOPSY OF MASSES ABOUT BONE LESIONS J Ultrasound Med 19: , 2000 histologic diagnosis, and core biopsy also helped solve ambiguity in cytologic diagnosis. Although core needle biopsy has its merits, nevertheless, FNAC of soft tissue masses about superficial bone lesions is easier and less time consuming than core needle biopsy. In most cases of metastases from a known primary malignancy, an FNAC study is adequate. 1,2 When minor cortical bone disruption or bone destruction is associated only with scanty paraosseous tumor soft tissues, FNA is the only technique feasible because of the limited purchase by the biopsy needle. In general, an FNA is safer in obtaining a specimen from soft tissue masses about superficial bone lesions located in the vicinity of vital organs, such as the brain and the lung. 4 A cytopathologist s presence during an FNA may enhance the adequacy of cellular aspirates, but our limited experience on using real-time ultrasound guidance shows that it may not be necessary for a pathologist to be present at the site of needle aspiration because the target is accurately localized and a core needle biopsy can be performed safely when necessary. However, an onsite pathologist is helpful in deciding whether a core needle specimen should be obtained immediately after an ambiguous cytology result was found. Most of our needle biopsy results from soft tissue masses about superficial bone lesions were metastases to bone. The management of a suspected bone metastasis 9 depends on its pathologic diagnosis, which can be obtained using a variety of biopsy techniques. The commonly used techniques for obtaining a pathologic diagnosis for soft tissue masses about superficial bone lesions include needle biopsy guided by palpation, needle biopsy using an image guidance (fluoroscopic, CT, or ultrasound guidance), and open surgical biopsy. The minimally invasive image guided percutaneous needle biopsy may be tried before resorting to the more costly conventional open surgical biopsy. 10,11 As we gained in experience, ultrasound was preferred over CT for guiding needle biopsy of soft tissue masses about superficial bone lesions because needle insertion and excursion during the procedure could be monitored under realtime imaging to ensure accurate sampling of target lesions. The results of this study indicate that ultrasound-guided needle biopsy may be the method of choice for most soft tissue masses about superficial bone lesions accessible by sonography. However, the use of a particular image guidance technique depends on preference of the operator and also on the ability of that image modality to delineate the target lesion. Ultrasound-guided needle biopsy is an excellent technique for obtaining a pathologic diagnosis for soft tissue masses about superficial bone lesions; however, its application in deeper bone lesions may be limited by the natural attenuation of the ultrasound beam. We recommend that ultrasoundguided needle biopsy be performed on soft tissue masses about superficial bone lesions occurring within 5 cm from the skin surface when using a highresolution ultrasound probe. Although similar lesions occurring slightly deeper may be sampled with a lower frequency probe, the image resolution may not be adequate in demonstrating the needle path. In this instance CT-guided needle biopsy is preferable. Ultrasonographic guidance also is limited in cases of bone lesions with intact cortices, by which ultrasound beam is attenuated. In conclusion, ultrasound-guided needle biopsy is an effective method for the pathologic diagnosis of soft tissue masses about superficial bone lesions. The real-time and color capability of ultrasound is particularly valuable in guiding needle biopsies of hypervascular lesions and lesions occurring in complex anatomic locations overlying vital organs, such as the brain and the lung. FNAC often is adequate for diagnosing soft tissue masses about superficial bone lesions with known primary site pathologies; otherwise, core needle biopsy may either be done as an initial technique or subsequent to an ambiguous cytology result. REFERENCES 1. Ng CS, Salisbury JR, Darby AJ, et al: Radiologically guide bone biopsy: Results of 502 biopsies. Cardiovasc Intervent Radiol 21:122, Chhem RK, Schmutz GR, Huynh HH, et al: Ultrasonography of a bone metastasis. Can Assoc Radiol J 43:138, Civardi G, Livraghi T, Colombo P, et al: Lytic bone lesions suspected for metastasis: Ultrasonically guided fineneedle aspiration biopsy. J Clin Ultrasound 22:307, Targhetta R, Balmes P, Marty-Duoble C, et al: Ultrasonically guided aspiration biopsy in osteolytic bone lesions of the chest wall. Chest 103:1403, Koscick RL, Petersilge CA, Makley JT, et al: CT-guided fine needle aspiration and needle core biopsy of skeletal lesions: Complementary diagnostic techniques. Acta Cytol 43:697, Schweiter ME, Gannon FH, Deely DM, et al: Percutaneous skeletal aspiration and core biopsy: Complimentary techniques. AJR 166:415, Skrzynski MC, Biermann JB, Montag A, et al: Diagnostic accuracy and charge-savings of outpatient core needle biopsy compared with open biopsy of musculoskeletal tumors. J Bone Joint Surg [Am] 78:644, 1996

7 J Ultrasound Med 19: , 2000 YEOW ET AL Barth RJ Jr, Merino MJ, Solomon D, et al: A prospective study of the value of core needle biopsy and fine needle aspiration in the diagnosis of soft tissue masses. Surgery 112:536, Mink J: Percutaneous bone biopsy in the patient with known or suspected osseous metastases. Radiology 161:653, Fraser-Hill MA, Renfrew DL: Percutaneous needle biopsy of musculoskeletal lesions. 1. Effective accuracy and diagnostic utility. AJR 158: 809, Fraser-Hill MA, Renfrew DL, Hilsenrath PE: Percutaneous needle biopsy of musculoskeletal lesions. 2. Costeffectiveness. AJR 158:813, 1992