Computed tomography guided core needle biopsy versus incisional biopsy in diagnosing musculoskeletal lesions

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1 Journal of Orthopaedic Surgery 2013;21(2):204-8 Computed tomography guided core needle biopsy versus incisional biopsy in diagnosing musculoskeletal lesions Piya Kiatisevi, 1 Voranuch Thanakit, 2 Bhasanan Sukunthanak, 1 Mayura Boonthatip, 3 Saraporn Bumrungchart, 3 Kiat Witoonchart 1 1 Orthopaedic Oncology Unit, Institute of Orthopaedics, Lerdsin General Hospital, Bangkok, Thailand 2 Department of Pathology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand 3 Department of Radiology, Lerdsin General Hospital, Bangkok, Thailand ABSTRACT Purpose. To compare computed tomography (CT) guided core needle biopsy (CNB) with incisional biopsy in diagnosing musculoskeletal lesions. Methods. 62 men and 50 women aged 12 to 83 (mean, 45) years who underwent a CT-guided CNB were compared with 31 men and 33 women aged 9 to 81 (mean, 53) years who underwent an incisional biopsy. All specimens had final pathology report to compare with. Comparisons were made in terms of (1) diagnostic rate, (2) accuracy in distinguishing benign from malignant lesions, (3) accuracy in distinguishing low- from high-grade sarcomas, (4) accuracy for histological diagnosis, and (5) complication and repeated biopsy rates. Results. The diagnostic rate of CT-guided CNB and incisional biopsy was not significantly different (92.9% vs. 96.9%, p=0.33), nor were the accuracy in distinguishing benign from malignant lesions (100% vs. 98.4%, p=0.37), the accuracy in distinguishing low- from high-grade sarcomas (100% vs. 100%, p=1.00), the accuracy for specific diagnosis (75.9% vs. 85.2%, p=0.17), the repeated biopsy rate (6.3% vs. 4.7%, p=0.75), and the complication rate (0.9% vs. 4.7%, p=0.14). The accuracy for specific diagnosis was higher for bone than soft-tissue lesions for both CTguided CNB (87.0% vs. 59.5%, p=0.002) and incisional biopsy (87.0% vs. 77.3%, p=0.43). The accuracy of CT-guided CNB for specific diagnosis of benign softtissue tumours as well as infection and inflammation was relatively low. Conclusion. CT-guided CNB is safe, easy to perform, efficient, and less invasive, and should be considered as a first-line biopsy for musculoskeletal lesions. Key words: biopsy, large-core needle; image-guided biopsy; pathology; tomography, X-ray computed INTRODUCTION Incisional biopsy is the gold standard for diagnosing musculoskeletal lesions, as it can obtain sufficient sample size to enable a high diagnostic accuracy (91 96%). 1 3 However, it gives rise to complications such Address correspondence and reprint requests to: Dr Piya Kiatisevi, Orthopaedic Oncology Unit, Institute of Orthopaedics, Lerdsin General Hospital, Bangkok, Thailand. piyamd@yahoo.com

2 Vol. 21 No. 2, August 2013 CT-guided core needle biopsy versus incisional biopsy 205 as seroma, haematoma, infection, wound dehiscence, and tumour contamination, with a rate of up to 16%, and affects 8% of treatment plans. 2,4 Percutaneous core needle biopsy (CNB) is costeffective and has low complication rates and high accuracy (up to 97%). 5 9 It is more accurate and safer when performed under computed tomography (CT) guidance, so as to avoid missing the target and injuring neurovascular structures, especially when the lesions are deeply seated and heterogeneous. This study compared computed tomography (CT)-guided core needle biopsy (CNB) with incisional biopsy in diagnosing musculoskeletal lesions. MATERIALS AND METHODS From January 2008 to December 2010, 143 consecutive patients underwent 154 CT-guided CNBs for musculoskeletal lesions. 31 of whom had no final pathology for comparison and were excluded. Biopsies of the remaining 62 men and 50 women aged 12 to 83 (mean, 45) years were compared with those of 31 men and 33 women aged 9 to 81 (mean, 53) years who underwent an incisional biopsy between June 2004 and December 2007 (before introduction of CNB to our hospital). These specimens had final pathology report to compare with. CT-guided CNB was performed by one of 2 orthopaedic oncologists in conjunction with a radiologist in an out-patient setting for patients with bone and soft-tissue lesions deep to the fascia, heterogeneous on magnetic resonance imaging, or suspected to be malignant. Biopsy principles were strictly adhered so that definitive resection of the tumour was not compromised. The area was prepped and draped and infiltrated for local anaesthesia with 2% lidocaine without adrenalin. A 14-gauge springloaded needle (Supercore; Angiotech, Vancouver, Canada) was used. Six to 10 passes were made through the mass in different directions using single penetration, and cores of tissue were obtained. The number of passes was determined by the orthopaedic oncologists. After taking adequate specimens, the wound was then covered with compressive dressing, and the specimens were immediately fixed in formalin. Each specimen was reviewed by a single pathologist. Special staining and immunohistochemical studies were performed at the discretion of the pathologist. Only sarcoma specimens were graded, and intermediate grade was categorised as high grade. Comparisons were made in terms of (1) diagnostic rate, (2) accuracy in distinguishing benign from malignant lesions, (3) accuracy in distinguishing low- from high-grade sarcomas, (4) accuracy for histological diagnosis, and (5) complication and repeated biopsy rates. All incisional biopsies were performed by one of the orthopaedic oncologists under general or spinal anaesthesia in an in-patient setting. The specimens were reviewed by the same pathologist. Chi-squared test or Fisher s exact test was used as appropriate. Histological pathologies of the biopsies and definitive diagnoses after surgery were compared. A p value of <0.05 was considered statistically significant. Table 1 Histological diagnosis of all lesions (n=176) Diagnosis No. of biopsies Computed tomography guided core needle biopsy (n=112) Incisional biopsy (n=64) Benign bone tumour (n=34, 19%) Giant cell tumour 14 9 Chondroblastoma 3 2 Osteofibrous dysplasia - 2 Simple bone cyst 1 - Aneurysmal bone cyst - 1 Enchondroma 1 - Fibrous dysplasia 1 - Malignant bone tumour (n=42, 24%) Osteosarcoma Lymphoma 3 2 Ewing sarcoma 3 1 Chondrosarcoma 2 2 Parosteal osteosarcoma - 2 Malignant fibrous histicytoma - 1 Malignant giant cell tumour - 1 Chordoma 1 - Leiomyosarcoma of bone 1 - Benign soft-tissue tumour (n=11, 6%) 3 8 Aggressive fibromatosis - 3 Pigmented villonodular synovitis 1 - Neurofibroma - 2 Extraskeletal chondroma - 2 Hemangioma 1 1 Lipoma 1 - Malignant soft-tissue tumour (n=19, %) Malignant fibrous histiocytoma 6 3 Liposarcoma 2 1 Low-grade fibromyxoid sarcoma 1 - Malignant peripheral nerve 1 1 sheath tumours Other sarcomas 3 1 Bone metastasis and myeloma 22 8 (n=30, 17%) Bone metastasis 18 6 Multiple myeloma 4 2 Infectious and inflammatory lesions (n=40, 23%) 31 9

3 206 Kiatisevi et al. Journal of Orthopaedic Surgery RESULTS Out of 176 specimens, 34 (19%) were benign bone tumours, 42 (24%) were malignant bone tumours, 11 (6%) were benign soft-tissue tumours, 19 (11%) were malignant soft-tissue tumours, 30 (17%) were bone metastasis and myeloma, and 40 (23%) were infectious/inflammatory lesions (Table 1). Computed tomography guided core needle biopsy Of the 112 specimens obtained by CT-guided CNB, 8 (7.1%) were non-diagnostic, because the specimens contained inadequate tissue (n=1), necrotic tissue only (n=2), and non-specific tissue (n=5) [Table 2]. Among the remaining 104 specimens, distinguishing benign from malignant lesions and low- from highgrade sarcomas was possible. The diagnostic rate of CT-guided CNB was 92.9% (104/112), for which a specific diagnosis was made in 79 (75.9%) of the specimens (Table 3). To achieve a diagnosis, 7 (6.3%) of the patients underwent repeated biopsies (4 by CT-guided CNB and 3 by incisional biopsy); 5 were initially non-diagnostic and 2 were initially diagnosed as conventional osteosarcoma and haematoma with an unacceptable level of confidence. None of the biopsy errors resulted in erroneous definitive treatment. All the patients tolerated the procedure well without recourse to any analgesic or sedative medication. One patient developed a small haematoma around the needle scar at the right thigh, and was treated with a wide elliptical skin incision during definitive surgery. Incisional biopsy Of the 64 specimens obtained by incisional biopsy, 2 (3.1%) were non-diagnostic, because the specimens contained only necrotic tissue (n=1) and non-specific tissue (n=1) [Table 2]. Among the remaining 62 specimens, distinguishing benign from malignant lesions and low- from high-grade sarcomas was possible in 61. One specimen was diagnosed as lipoma but turned out to be a well-differentiated liposarcoma on the final pathology. The diagnostic rate of incisional biopsy was 96.9% (62/64), for which a specific diagnosis was made in 52 (85.2%) of the specimens (Table 3). Three (4.7%) of the patients underwent repeated incisional biopsies. Two patients developed wound dehiscence, which was managed by debridement and wound closure, and one patient developed a haematoma, which was treated with a wide elliptical skin incision. Comparison of both biopsy methods The diagnostic rate of CT-guided CNB and incisional biopsy was not significantly different (92.9% vs. 96.9%, p=0.33), nor were the accuracy in distinguishing benign from malignant lesions (100% Table 2 Non-diagnostic specimens following computed tomography guided core needle biopsy (CT-guided CNB) or incisional biopsy Biopsy Outcome Site Final diagnosis CT-guided CNB Inadequate sample Proximal femur Chondroblastoma CT-guided CNB Necrotic tissue Femoral diaphysis Multiple myeloma CT-guided CNB Necrotic tissue Proximal femur Multiple myeloma CT-guided CNB Cartilage with atypical cells Proximal humerus Chondrosarcoma CT-guided CNB Non-specific spindle cell lesion Thigh Malignant peripheral nerve sheath tumour CT-guided CNB Atypical cells Arm Squamous cell carcinoma CT-guided CNB Skeletal muscle Thigh Tuberculous myositis CT-guided CNB Fibrin Shoulder Chacot arthropathy Incisional biopsy Bony tissue with atypical cells Distal femur Parosteal osteosarcoma Incisional biopsy Necrotic tissue Proximal tibia Giant cell tumour Table 3 Comparison of computed tomography guided core needle biopsy (CT-guided CNB) with incisional biopsy Rate (%) CT-guided CNB (n=112) Incisional biopsy (n=64) p Value Diagnostic rate Distinguishing benign from malignant lesions Specific diagnostic rate Distinguishing low- from high-grade sarcomas Repeated biopsy rate Complication rate

4 Vol. 21 No. 2, August 2013 CT-guided core needle biopsy versus incisional biopsy 207 vs. 98.4%, p=0.37), the accuracy in distinguishing low- from high-grade sarcomas (100% vs. 100%, p=1.00), the accuracy for specific diagnosis (75.9% vs. 85.2%, p=0.17), the repeated biopsy rate (6.3% vs. 4.7%, p=0.75), and the complication rate (0.9% vs. 4.7%, p=0.14) [Table 3]. The accuracy for specific diagnosis was higher for bone than soft-tissue lesions for both CT-guided CNB (87.0% vs. 59.5%, p=0.002) and incisional biopsy (87.0% vs. 77.3%, p=0.43) [Table 4]. The accuracy of both biopsy methods was not significantly different when only tumour specimens (excluding infectious/ inflammatory specimens, which were mostly softtissue lesions) were considered and when categorised by tumour types (Table 5). The accuracy of CT-guided CNB for specific diagnosis of benign soft-tissue tumours (66.7%) as well as infectious and inflammatory lesions (51.7%) was relatively low (Table 5). Of 3 benign soft-tissue tumours diagnosed by CT-guided CNB, one pigmented-villonodular synovitis specimen was initially reported to be only a histiocytic lesion with round cells and brown pigment. Of the 31 infectious/inflammatory lesions diagnosed by CTguided CNB, 15 were soft-tissue tuberculosis, 7 of which had evidence of granulomatous inflammation with a central necrotic area, whereas 8 had no central necrosis. All tuberculous lesions were diagnosed using acid-fast bacilli stains and polymerase chain reaction before treatment was commenced. DISCUSSION CT- or ultrasonography-guided CNB increases diagnostic accuracy and safety by confirming the targeted areas and avoiding damage to neurovascular bundles, particularly when the lesions are deepseated, located in the pelvis, spine, sacrum or scapula, or close to important structures such as neurovascular bundles. 5,6 The accuracy of imaged-guided CNB for musculoskeletal lesions has been 80% to 97%. 5 7,13 15 However, distinguishing benign lipomas from well-differentiated liposarcomas through biopsy is difficult, because the malignant component may be deep-seated or involved only a small area. Thus, using magnetic resonance imaging to establish the diagnosis is more reliable. When in doubt, biopsy is indicated in lipomatous lesions with more heterogeneity, with gadolinium enhancement or suspected intermediateor high-grade liposarcomas. CT-guided CNB enables visualising the exact location for sampling, especially when the lesion was small or deep. In the current study, the accuracy of CT-guided CNB in distinguishing benign from malignant lesions and low- from high-grade sarcomas was high, because decision was made after careful discussion between the orthopaedic oncologist, pathologist, and radiologist. 10 In addition, we tried not to biopsy lesions that appeared to be low-grade lipomatous tumours, low-grade cartilaginous tumours, or myxoid, as they are difficult to interpret histologically. 3,16 Atypical Table 4 Accuracy of computed tomography guided core needle biopsy (CT-guided CNB) and incisional biopsy for bone versus softtissue lesions Biopsy Accuracy (%) p Value Bone lesions Soft-tissue lesions All specimens CT-guided CNB Incisional biopsy Tumour specimens (excluding infection and inflammation specimens) CT-guided CNB Incisional biopsy Table 5 Accuracy of computed tomography guided core needle biopsy (CT-guided CNB) and incisional biopsy in terms of lesion type Lesion type Accuracy (%) p Value CT-guided CNB biopsy Incisional biopsy Benign bone tumour (n=34) Malignant bone tumour (n=72) Benign soft-tissue tumour (n=11) Malignant soft-tissue tumour (n=19) Bone metastasis and myeloma (n=30) Infection and inflammation (n=40)

5 208 Kiatisevi et al. Journal of Orthopaedic Surgery lipomatous tumour, well-differentiated liposarcoma, or low-grade chondrosarcoma can be safely treated by marginal resection without biopsy 17,18 or extended intralesional curettage, 19,20 as the risk of recurrence is low. Nonetheless, in indeterminate lesions, biopsy is still recommended. Moreover, the number of soft-tissue tumours was fewer than that of bone tumours; soft-tissue tumours such as schwannoma, synovial sarcoma, and angiosarcoma may consist of heterogenic cells or myxoid areas, for which it is difficult to achieve a correct diagnosis or grading. 13 The accuracy of both biopsies for specific diagnosis of bone metastasis and myeloma was relatively high, which was consistent with findings from other studies, 7,10 12 as their homogeneous nature enabled the biopsy to contain diagnostic tumour cells. 13 The accuracy of CT-guided CNB for specific diagnosis of infection/inflammation was relatively low, which was also consistent with studies reporting rates of 50% 6 and 78%. 7 CT-guided CNB is an accurate procedure for diagnosing musculoskeletal lesions. It can be easily repeated without major morbidity. Its complication rates are trivial, 7,13,21 and the repeated biopsy rate is similar to that after incisional biopsy. CT-guided CNB when performed by a multidisciplinary team trained in the musculoskeletal tumour field should be considered as the first-line biopsy for diagnosing musculoskeletal lesions. DISCLOSURE No conflicts of interest were declared by the authors. REFERENCES 1. Mankin HJ, Lange TA, Spanier SS. The hazards of biopsy in patients with malignant primary bone and soft-tissue tumors. J Bone Joint Surg Am 1982;64: Mankin HJ, Mankin CJ, Simon MA. The hazards of the biopsy, revisited. Members of the Musculoskeletal Tumor Society. J Bone Joint Surg Am 1996;78: Adams SC, Potter BK, Pitcher DJ, Temple HT. Office-based core needle biopsy of bone and soft tissue malignancies: an accurate alternative to open biopsy with infrequent complications. Clin Orthop Relat Res 2010;468: Ray-Coquard I, Ranchere-Vince D, Thiesse P, Ghesquieres H, Biron P, Sunyach MP, et al. Evaluation of core needle biopsy as a substitute to open biopsy in the diagnosis of soft-tissue masses. Eur J Cancer 2003;39: Stoker DJ, Cobb JP, Pringle JA. Needle biopsy of musculoskeletal lesions. A review of 208 procedures. J Bone Joint Surg Br 1991;73: Hau A, Kim I, Kattapuram S, Hornicek FJ, Rosenberg AE, Gebhardt MC, et al. Accuracy of CT-guided biopsies in 359 patients with musculoskeletal lesions. Skeletal Radiol 2002;31: Tsukushi S, Nishida Y, Yamada Y, Yoshida M, Ishiguro N. CT-guided needle biopsy for musculoskeletal lesions. Arch Orthop Trauma Surg 2010;130: Yao L, Nelson SD, Seeger LL, Eckardt JJ, Eilber FR. Primary musculoskeletal neoplasms: effectiveness of core-needle biopsy. Radiology 1999;212: Logan PM, Connell DG, O Connell JX, Munk PL, Janzen DL. Image-guided percutaneous biopsy of musculoskeletal tumors: an algorithm for selection of specific biopsy techniques. AJR Am J Roentgenol 1996;166: McCarthy EF. CT-guided needle biopsies of bone and soft tissue tumors: a pathologist s perspective. Skeletal Radiol 2007;36: Skrzynski MC, Biermann JS, Montag A, Simon MA. Diagnostic accuracy and charge-savings of outpatient core needle biopsy compared with open biopsy of musculoskeletal tumors. J Bone Joint Surg Am 1996;78: Fraser-Hill MA, Renfrew DL. Percutaneous needle biopsy of musculoskeletal lesions. 1. Effective accuracy and diagnostic utility. AJR Am J Roentgenol 1992;158: Sung KS, Seo SW, Shon MS. The diagnostic value of needle biopsy for musculoskeletal lesions. Int Orthop 2009;33: Puri A, Shingade VU, Agarwal MG, Anchan C, Juvekar S, Desai S, et al. CT-guided percutaneous core needle biopsy in deep seated musculoskeletal lesions: a prospective study of 128 cases. Skeletal Radiol 2006;35: Mitsuyoshi G, Naito N, Kawai A, Kunisada T, Yoshida A, Yanai H, et al. Accurate diagnosis of musculoskeletal lesions by core needle biopsy. J Surg Oncol 2006;94: Ogilvie CM, Torbert JT, Finstein JL, Fox EJ, Lackman RD. Clinical utility of percutaneous biopsies of musculoskeletal tumors. Clin Orthop Relat Res 2006;450: Dalal KM, Antonescu CR, Singer S. Diagnosis and management of lipomatous tumors. J Surg Oncol 2008;97: Kubo T, Sugita T, Shimose S, Arihiro K, Ochi M. Conservative surgery for well-differentiated liposarcomas of the extremities adjacent to major neurovascular structures. Surg Oncol 2006;15: Mohler DG, Chiu R, McCall DA, Avedian RS. Curettage and cryosurgery for low-grade cartilage tumors is associated with low recurrence and high function. Clin Orthop Relat Res 2010;468: Weber KL, Raymond AK. Low-grade/dedifferentiated/high-grade chondrosarcoma: a case of histological and biological progression. Iowa Orthop J 2002;22: Welker JA, Henshaw RM, Jelinek J, Shmookler BM, Malawer MM. The percutaneous needle biopsy is safe and recommended in the diagnosis of musculoskeletal masses. Cancer 2000;89: