mage-guided needle biopsy of bone lesions generally is performed under fluoroscopic or CT guidance.1 For soft tissue masses about
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 proce-dure, which may last approximately 30 min. The dif-ficulty 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. Real-time ultrasound-guided needle biopsy, on the other hand, provides a much more flexible patient posi-tioning. Interval change in the patient’s position is acceptable. However, ultrasonography is used infre-quently to guide a bone biopsy owing to its lack of
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, 2000.
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.
CT, Computed tomography; FNA, Fine needle aspiration; FNAC, Fine needle aspiration cytology
2000 by the American Institute of Ultrasound in Medicine • J Ultrasound Med 19:849–855, 2000 • 0278-4297/00/$3.50
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. Sonog-raphically guided needle biopsies were performed without an on-site pathologist. A diagnostic sensi-tivity 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 pre-cise needle placement into the targets, avoidance of hypervascular areas, and flexibility of patient positioning so that needle biopsy can be per-formed quickly and safely on soft tissue masses about superficial bone lesions. KEY WORDS: Bone,
depth penetration of soft tissue and its inability to penetrate bone cortex.1,2 Two reported series3,4 obtained diagnostic sensitivities of 93% and 87.5% for superficial bony destructions using only FNAC. In our experience, a core needle specimen may occa-sionally be needed when FNA did not obtain an ade-quate 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 sta-bilizing a cutting needle when CT guidance was used in previous biopsies. Using ultrasound as guid-ance, the operator could hold a needle in one hand and the ultrasound probe in the other. One interven-tional 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 superfi-cial bone lesions as revealed by CT scans were fur-ther 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 sur-roundings), their thickness, and whether the under-lying 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 inci-sion 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
tech-nique. 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 com-pressed the puncture sites immediately after the biopsy procedure for about 10 min. After a short period of observation outside our ultrasound labora-tory, the patients were routinely asked if they felt increased pain over the biopsy sites, and the punc-ture sites were checked by the interventional radiol-ogist for evidence of local swelling. If the patient had any questionable local discomfort or swelling accom-panied 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 cyto-logic 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 nee-dle biopsy was selected as the preferred biopsy tech-nique when (1) the targeted lesion had a soft tissue component greater than 2 cm in depth, (2) the patho-logic diagnosis of a primary tumor occurring else-where 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 characteri-zation of tumor tissue and histochemical staining. Hypervascularity of the target lesions was not a con-traindication 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 ultrasound-guided 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
used as standards for establishing the diagnoses of malignancies. Thus, the pathologic or classic radio-logic diagnoses of primary site masses and the clini-cal follow-up of the course of primary masses were used as the gold standards for calculation of sensitiv-ity 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 appro-priate chemotherapeutic agents were used as diag-nostic standards of comparison. The sensitivity and specificity of ultrasonographically guided needle biopsy were calculated using 2 ×2 contingency tables.
All 20 patients tolerated the needle biopsy proce-dures well. Thirteen patients (65%) had undiagnosed tumor masses elsewhere in the body, which were dif-ficult to access by needle biopsy due to the patients’ poor clinical status. In 14 patients (70%), the soft tis-sue masses about the superficial bone lesions were not palpable. The target lesions were visible sono-graphically 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 fre-quent 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 tis-sue confirmation. In four patients, only FNAC was possible because the soft tissues about minor irregu-lar 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 carcinomas, 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 dis-tinguished (1 core needle biopsy required CT-guided core biopsy for diagnosis), resulting in a diagnostic sensitivity of 95% and specificity of 100% in separat-ing 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 dif-ferentiated metastatic carcinoma; 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 blad-der cancer, which was confirmed on subsequent cys-toscopy 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 1A 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.
In this study of 20 consecutive patients with soft tis-sue masses about superficial bone lesions, which were within 5 cm from skin surface, ultrasound-guided 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 direct-ing 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 nee-dle or a cutting neenee-dle) were needed as ultrasound provided a clear target for needle biopsy. Areas of hypervascularity found in three metastatic hepatocel-lular carcinomas were avoided with the help of color Doppler flow mapping when they were sampled using core needles. No immediate bleeding compli-cation was encountered in this series.
Needle biopsy of soft tissue masses about super-ficial bone lesions occurring in more complex anatomic locations, such as small, round, and shal-low 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 nee-dle during neenee-dle positioning may cause injury to the brain or the lung.3,4In contrast, patient position-ing 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 ultrasound-guided needle biopsy of soft tissue masses about
superficial bone lesions, patients need not hold their breaths during needle excursion or firing. The tech-nique should be widely applicable as long as the lesion can be demonstrated by ultrasound.
Much debate has occurred on the diagnostic accu-racy 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 carcinomas, and lymphomas, uncertainty in cyto-logic diagnosis may be encountered if FNAC alone is 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 hyper-echoic bone cortex (R).
Figure 3 Cross-sectional high-resolution sonogram of the same lesion as in Figure 2B shows a fine needle (arrow) enter-ing the hypoechoic paraosseous soft tissue lesion. Cytology result revealed a metastatic poorly differentiated carcinoma, which has the same pathologic pattern as the original nasopharyngeal cancer. R, Cortex of the rib.
performed.5We 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 pri-mary 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%.7An additional advantage of core needle biopsy is that tissue speci-mens 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 lym-phoma and a primary rib sarcoma after special histo-chemical staining. The core needle specimens obtained from such soft tissues about superficial bone lesions permitted the pathologist to give an accurate 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 carcinoma 46M Skull, 1.5 cm Nasopharyngeal 18 gauge, core Metastatic poorly differentiated
carcinoma nasopharyngeal carcinoma
61F Mandibular condyle, Colon carcinoma 23 gauge, FNA Metastatic colon adenocarcinoma 2 cm
66M Clavicle, 10 cm Liver tumor 18 gauge, core Metastatic hepatocellular carcinoma 63F Clavicle, 1.5 cm Lung tumor 23 gauge, FNA Metastatic non–small cell lung carcinoma 57F Scapula, 2.5 cm Breast carcinoma 16 gauge, core Metastatic breast adenocarcinoma
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 carcinoma 23 gauge, FNA Benign
53M Rib, 2.7 cm Lung carcinoma 23 gauge, FNA Metastatic lung adenocarcinoma
32M Rib, 4.4 cm Esophageal squamous 23 gauge, FNA Metastatic squamous cell carcinoma
cell carcinoma of esophagus
71M Rib, 5 cm Hepatocellular 16 gauge, core Metastatic hepatocellular carcinoma carcinoma
69M Rib, 7 cm Thymic tumor 18 gauge, core Metastatic thymic carcinoma
26M Rib, 8 cm Nasopharyngeal carcinoma 23 gauge, FNA Metastatic poorly differentiated carcinoma
40M Sacrum, 3 cm Parotid adenocystic 18 gauge, core Metastatic adenocystic carcinoma carcinoma
65F Iliac bone, 6.5 cm No 16 gauge, core Poorly differentiated transitional cell carcinoma
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 pri-mary 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 tech-nique feasible because of the limited purchase by the biopsy needle. In general, an FNA is safer in obtain-ing a specimen from soft tissue masses about superfi-cial bone lesions located in the vicinity of vital organs, such as the brain and the lung.4A 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 on-site 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 metas-tases to bone. The management of a suspected bone metastasis9 depends on its pathologic diagnosis, which can be obtained using a variety of biopsy tech-niques. 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.10,11As 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 dur-ing the procedure could be monitored under real-time imaging to ensure accurate sampling of target lesions. The results of this study indicate that ultra-sound-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 tar-get 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 ultra-sound beam. We recommend that ultraultra-sound- ultrasound-guided needle biopsy be performed on soft tissue masses about superficial bone lesions occurring within 5 cm from the skin surface when using a high-resolution 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 partic-ularly valuable in guiding needle biopsies of hyper-vascular 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; other-wise, core needle biopsy may either be done as an initial technique or subsequent to an ambiguous cytology result.
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