9.2 Intracompartmental Compared with Extracompartmental Spread
Determination of whether the location and/or exten- sion of a tumor is intracompartmental or extracom- partmental is an important element in staging. Extra- compartmental spread and inadvertent tumor spread can be due to a poorly planned biopsy [4]. If uninvolved anatomical compartments are crossed to obtain the biopsy specimen, the result may be a more radical resec- tion or even amputation. Therefore, knowledge of com- partmental anatomy is mandatory for planning and performance of a percutaneous needle biopsy [5, 6]. For treatment of the different compartments of the upper and lower extremities, the reader is referred to the ex- cellent article of Anderson et al. [6], whose cross-sec- tional diagrams of the different compartments are reprinted here (Figs. 9.1–9.5).
Generally, skin and subcutaneous fat, bone, paraos- seous spaces, and joint spaces are regarded as intracom- partmental. For the upper extremity, the periclavicular region, axilla, antecubital fossa, wrist, and dorsum of the hand, and for the lower extremity the groin, popliteal fossa, ankle and dorsum of the foot are considered extracompartmental.
9.1 Introduction
Staging of soft tissue tumors frequently includes a biopsy that is mostly performed percutaneously using imaging guidance (ultrasound, computed tomography CT, or magnetic resonance imaging, MRI).A biopsy is necessary when the orthopedic surgeon and the radiologist believe they are dealing with a progressive process, requiring in- tervention [1]. Otherwise, unexpected manipulation of a soft tissue sarcoma (STS) can influence its biological be- havior and prognosis [2]. Moreover, biopsy of soft tissue tumors with large needles involves a risk of seeding ma- lignant cells along the needle track. Because biopsy is considered part of the surgical therapy, en bloc resection of tumor and needle track is usually needed [3].
Biopsy of Soft Tissue Tumors
J. Gielen, A. De Schepper
9
9.1 Introduction . . . 117
9.2 Intracompartmental Compared with Extracompartmental Spread . . . 117
9.3 General Rules for Biopsy Safety . . . 121
9.4 Diagnostic Accuracy . . . 121
9.5 Immunohistochemistry . . . 122
9.6 Technique and Choice of Needle . . . 123
9.7 Conclusion . . . 123
References . . . 123 Contents
Fig. 9.1. Cross section of mid-upper arm shows contents of anterior and posterior compartments. (Reprinted from [6]
with permission)
Fig. 9.2. Cross section of mid-forearm shows contents of volar and dorsal compartments. (Reprinted from [6]
with permission)
Fig. 9.3Ia–c. Cross section of thigh shows contents and relative positions of anterior, medial, and posterior compartments at these levels. a Proximal thigh; b mid-thigh;
cdistal thigh. (Reprinted from [6] with permission)
a
b
Fig. 9.5. Cross section of foot shows contents of medial, central, and lateral compartments. (Reprinted from [6]
with permission)
Fig. 9.4Ia, b. Lower leg. Cross section of aproximal calf and b mid-calf show contents of anterior, deep posterior, posterior, and lateral compartments.
(Reprinted from [6] with permission)
a
b
Open surgical biopsy is advocated by Huvos [9], who claims that only an adequate amount of removed tissue will allow for a maximal diagnostic benefit.
Kilpatrick et al. [10] have used FNAB and obtained a histogenetically specific diagnosis in 93% of cases of pe- diatric bone and soft tissue tumors, all of which were cor- rectly recognized as either benign or malignant. In adults fine-needle aspiration biopsy is recommended for diag- nosis of tumors in the head and neck region [11] and whenever direct incisional biopsy is contraindicated [7, 12]. Gonzalez [12, 13] have reported a specificity of FNAB of more than 90%, the method being most effective when performed by an experienced pathologist.Agreement be- tween FNAB histopathological and cytological grading in musculoskeletal sarcomas treated by FNAB has been studied by Jones et al. [14] Although a statistically signif- icant correlation between cytologically assigned grade and final histo-pathological grade is found, statistical analysis reveals only a moderate correlation between the two, with an overall r value of approximately 0.57. Cyto- logical analysis tends to undergrade in comparison with final histopathological grading. FNAB is moderately suc- cessful at predicting histopathological grading. Only analysis of nuclear atypia shows good correlation with fi- nal surgical grade [14].
Skrzynski et al. [15] have performed a prospective study on the value of closed CNB in 62 patients with soft tissue tumors or bone tumors with soft tissue extension.
The diagnostic accuracy is 84% or 96%, respectively, for groups of patients who have undergone open biopsy performed by the same surgeon. Disadvantages include a nondiagnostic biopsy, indeterminate biopsy, and po- tential errors in histological grade. The hospital charges for a closed core biopsy are much less than those for an open biopsy! Comparable results are reported by Hodge [16], with a diagnostic accuracy of 76.9%.
Bennert [17] has evaluated the diagnostic yield of FNAB relative to that of CNB in 117 patients with soft tissue lesions. FNAB was unsatisfactory in 44 patients, 22 of whom were correctly diagnosed with CNB. The author’s conclusion is that FNAB gives a yield identical to that of CNB and that unsatisfactory FNAB should prompt further evaluation by CNB.
Hau et al. [18] have studied the accuracy of CT-guid- ed FNAB relative to CNB in a large number of patients (n=359) with musculoskeletal lesions. They found an overall accuracy of 71%, i.e., 63% for FNAB (n=101) and 74% for CNB (n=258). Biopsies of 81 pelvic lesions had a higher rate of diagnostic accuracy (81%) than nonpelvic sites (68%). The lowest accuracies (61% and 50%, respectively) have been noted in lesions of the spine and infectious diseases [18].
The best results have been reported by Dupuy et al.
[19], who performed 176 CNB and 45 FNAB of muscu- loskeletal neoplasms under CT guidance. They obtained
9.3 General Rules for Biopsy Safety
A CT scan is performed to localize the lesion precisely.
Ultrasound may be used in superficial lesions. The entry point and the pathway are determined, avoiding nerve, vascular, and visceral structures (Figs. 9.6–9.7).
General principles for safe percutaneous biopsy:
1. The shortest path between skin and the lesion should be chosen.
2. The needle should not traverse an uninvolved com- partment.
3. The joint or neurovascular bundle and the anticipat- ed needle path should be discussed with the surge on who will be performing the definitive surgery (Fig. 9.6).
9.4 Diagnostic Accuracy
Percutaneous musculoskeletal biopsy (PMSB) can be performed by fine-needle aspiration (FNAB), core-nee- dle biopsy (CNB), or open (incisional) biopsy. Excision- al biopsy should be used only for small lesions (less than 3 cm) or when the radiologist is convinced that the le- sion is benign [7, 8].
Fig. 9.6. Percutaneous core-needle biopsy, with CT guidance, of a deeply seated mass lesion with intralesional calcification. Histo- logical examination revealed a myositis ossificans. Control exami- nation after conservative therapy showed more typical, zonal cal- cification of the lesion
an accuracy of 93% for CNB and 80% for FNAB. Com- plication rate was less than 1%.
Ray-Coquard et al. have evaluated CNB in 110 STS patients. They found lower sensitivity in low-grade sar- comas (85%) than in high-grade sarcomas (100%). His- tological grading on CNB seems hardly feasible, except for grade III tumors [21].
In cases of impalpable soft tissue tumors, a needle containing a hookwire with an overbent hook that springs open when protruded beyond the needle top and anchors the wire in the lesion is positioned under ultrasound guidance and will facilitate excisional biop- sy [20]. As a consequence, diagnostic accuracy of PMSB is not only dependent on the specific sampling tech- nique but also on the location and the ultimate histolog- ical diagnosis of the lesion [21].
9.5 Immunohistochemistry
Considerable progress has been made in the clinical and biological understanding of soft tissue sarcomas. This led to the launch of a new WHO classification of soft tis-
sue tumors in 2002, which integrates morphological da- ta with tumor-specific (cyto-)genetics. Worldwide con- sensus has grown on how to predict clinical behavior based on a specific grading system and which specific types of tumors seem not to obey these rules. Immuno- histochemical characterization plays a key role in the diagnostic workup of STS. The determination line is crucial in order not only to ensure proper classification, but also to provide predictive information. The recent identification of tumor-specific drug targets by im- munohistochemistry has had impact on specimen re- quirements and handling as well as laboratory stan- dards [22]. Thus these new insights influence sampling technique. Tissue-sample fixation is adapted to permit immunohistochemical characterization. Acetic acid so- lutions are avoided because mitotic components are hardly visible after treatment with 70% acetic acid.
Thus the formerly used technique with alcohol-forma- lin-acetic acid (AFA) fixation has been abandoned [23].
A buffered 4% dilution of formalin (NF4) is recom- mended for tissue samples (CNB), and an alcoholic solution (Saccomano) is used for cell samples (FNAB) [24, 25].
Fig. 9.7Ia–c. Small, pigmented villonodular synovitis (PVNS) in a young female patient at the right popliteal space. a MRI of both knees in supine position, axial spin-echo T1-weighted image with fat suppression (FS) and after intravenous gadolinium-DTPA administration. A small, markedly enhanc- ing mass lesion at the left popliteal space adjacent to the popliteal neurovascular structures is seen (white arrow). b Computed tomography of the left knee, axial plane in prone position with soft tissue window and level settings and after intravenous adminis- tration of iodinated contrast material. The nonenhancing, hypointense mass lesion is seen at the lateral aspect of the enhancing popliteal neurovascular bundle (circle).
Entry point in relation to an external radioopaque marker is measured (arrow- heads), biopsy pathway (arrow), and skin- to-lesion interval and skin to deepest margin of the lesion (braces) are determined.
cComputed tomography of the left knee after insertion of biopsy needle, comparable axial plane, verification of needle position before cut
a
b c
surgery or neoadjuvant chemotherapy when combined with appropriate imaging. Except for FNAB, it is less time-consuming, less painful, and cheaper than other procedures. It can be performed under CT or ultra- sound guidance, CT being preferred for deep-seated le- sions or those that are difficult to reach. There are only few reports of MR guidance. The entry point and the pathway are determined in cross talk with the managing surgeon, avoiding nerve, vascular, and visceral struc- tures. Two or more slightly angled trajectories that involve the same anatomical compartments may be nec- essary in radiologically nonhomogeneous lesions. Tis- sue-sample fixation is adapted to permit immunohisto- chemical characterization. Open biopsy is mandatory if CNB is inadequate.
Things to remember:
1. The shortest path between skin and the lesion should be chosen and the anticipated needle path should be discussed with the surgeon who will be performing the definitive surgery.
2. The needle should not traverse an uninvolved compartment.
3. Compared with FNAB, CNB is able to provide a tissue sample in which matrix is disclosed with preservation of the tumor’s architectural struc- ture.
4. Soft tissue tumors often are spatially heteroge- neous with respect to tumor grade and character- ization features, and tumor necrosis may be wide- spread. Thus two or more slightly angled biopsy trajectories may be necessary.
5. Tissue-sample fixation is adapted to permit im- munohistochemical characterization. A buffered 4% dilution of formalin (NF4) is recommended for tissue samples (CNB), and an alcoholic solu- tion (Saccomano) is used for cell samples (FNAB).
References
1. Peabody TD, Simon MA (1996) Making the diagnosis: keys to a successful biopsy in children with bone and soft-tissue tu- mors. Orthop Clin North Am 27(3):453–459
2. Van Geel AN,Van Unnik JA, Keus RB (1995) Consensus soft tis- sue tumors. Dutch Workgroup Soft-Tissue Tumors. Ned Tijd- schr Geneeskd 139(6):833–837
3. Laredo JD (1999) Percutaneous biopsy of primary soft tissue tumors. Semin Musculoskeletal Radiol 3:139–144
4. Aboulafia AJ (1999) Biopsy. Instr Course Lect 48:587–590 5. Bickels J, Jelinek JS, Shmookler BM, Neff RS, Malawer MM
(1999) Biopsy of musculoskeletal tumors. Current concepts.
Clin Orthop 368:212–219
6. Anderson MW, Temple HT, Dussault RG, Kaplan PA (1999) Compartmental anatomy: relevance to staging and biopsy of musculoskeletal tumors. AJR Am J Roentgenol 173:1663–1671 7. Frassica FJ, McCarthy EF, Bluemke DA (2000) Soft-tissue mass-
es: when and how to biopsy. Instr Course Lect 49:437–442 8. Iwamoto Y (1999) Diagnosis and treatment of soft tissue tu-
mors. J Orthop Sci 4(1):54–65
9.6 Technique and Choice of Needle
In STS not only cytology but also matrix, architectural structure, and immunohistochemistry may add to the pathological diagnostic clues. FNAB essentially obtains cells without revealing its tissue architecture or matrix.
It is able to study cytonuclear disturbances but not tu- mor differentiation and matrix components. The patho- logist is often only able to differentiate malignant from benign lesions [26, 27]. It gives good results in tumors at the soft tissues in patients with known adenocarcinoma or myeloma and lymphoma or if the MRI characteris- tics are suggestive for lymphoma. In bone lesions it gives also good results in cases of Langerhans cell histi- ocytosis, chondroblastoma, chordoma, and giant cell tumor [28].
CNB is able to provide tissue in which matrix is dis- closed and the architectural structure may be pre- served. It is evident that 14-gauge needles produce bet- ter results than 20-gauge needles. Open incisional or ex- cisional biopsy also provides information of the reactive processes around the lesion. These latter techniques (CNB and open biopsy) show best diagnostic accuracy in cases of primary soft tissue tumors.
Moreover nonhomogeneity of tumors also may influ- ence CNB technique. Highest-graded zones in a tumor predict outcome, lowest-graded zones are best differen- tiated, may produce matrix, and help to characterize le- sions. As a consequence location of the biopsy trajecto- ry in the lesion itself depends on its imaging character- istics. In homogeneous lesions, the trajectory is only determined according to its compartmental anatomy.
Best results in nonhomogeneous lesions are gained if al- so the lesion’s inner architecture is taken into account. If possible a single long trajectory which encompasses evolving segments with imaging characteristics of high grade, i.e., cellular or lytic parts avoiding necrotic parts and parts that produce more differentiated matrix (cal- cified). Two or more slightly angled trajectories that involve the same anatomical compartments may be necessary.
For these reasons, consensus is growing to centralize tissue sampling to dedicated centers and to prefer CNB over FNAB.
9.7 Conclusion
Although the choice of biopsy type largely depends on the particular clinical setting and the experience of the clinician, radiologist, orthopedic surgeon, and patholo- gist, CNB is recommended as the procedure of first choice for obtaining representative specimens of soft tissue tumors for histological and immunohistochemi- cal examination because of its high diagnostic accuracy and low complication rate. It allows planning for single
9. Huvos AG (1995) The importance of the open surgical biopsy in the diagnosis and treatment of bone and soft-tissue tumors.
Hematol Oncol Clin North Am 9(3):541–544
10. Kilpatrick SE, Ward WG, Chauvenet AR, Pettenati MJ (1998) The role of fine-needle aspiration biopsy in the initial diagno- sis of pediatric bone and soft tissue tumors: an institutional experience. Mod Pathol 11(10):923–928
11. Skoog L, Pereira ST, Tani E (1999) Fine-needle aspiration cytol- ogy and immunocytochemistry of soft-tissue tumors and os- teo/chondrosarcomas of the head and neck. Diagn Cytopathol 20(3):131–136
12. Gonzalez Campora R (2000) Fine needle aspiration cytology of soft tissue tumors. Acta Cytol 44(3):337–343
13. Gonzalez Campora R, Munoz Arias G, Otal Salaverri C et al (1992) Fine needle aspiration cytology of primary soft tissue tumors. Morphologic analysis of the most frequent types. Acta Cytol 36(6):905–917
14. Jones C, Liu K, Hirschowigz S, Klipfel N, LayfieldLJ (2002) Con- cordance of histopahtologic and cytologic grading in muscu- loskeletal sarcomas: can grades obtained from analysis by the fine-needle aspirates serve as the basis for therapeutic deci- sions? Cancer 96(2):83–91
15. Skrzynski MC, Biermann JS, Montag A, Simon MA (1996) Di- agnostic accuracy and charge-savings of outpatient core nee- dle biopsy compared with open biopsy of musculoskeletal tu- mors. J Bone Joint Surg Am 78(5):644–649
16. Hodge JC (1999) Percutaneous biopsy of the musculoskeletal system : a review of 77 cases. Can Assoc Radiol J 50(2):121–125 17. Bennert KW, Abdul Karim FW (1994) Fine needle aspiration cytology vs. needle core biopsy of soft tissue tumors. A com- parison. Acta Cytol 38(3):381–384
18. Hau MA, Kim JI, Kattapuram S, Hornicek FJ, Rosenberg AE, Gebhardt MC, Mankin HJ (2002) Accuracy of CT-guided biop- sies in 359 patients with musculoskeletal lesions. Skeletal Radi- ol 31:349–353
19. Dupuy DE, Rosenberg AE, Punyaratabandhu T, Tan MH, Mankin HJ (1998) Accuracy of CT-guided needle biopsy of musculoskeletal neoplasms. Am J Roentgenol 171(3):759–762 20. Rutten MJ, Schreurs BW, van Kampen A, Schreuder HW (1997)
Excisional biopsy of impalpable soft tissue tumors. US-guided preoperative localization in 12 cases. Acta Orthop Scand 68(4):384–386
21. Ray-Coquard I, Ranchere-Vince D, Thiesse P, Ghesquieres H, Biron P, Sunyach MP, Rivoire M, Lancry L, Meeus P, Sebban C, Blay JY (2003) Evaluation of core needle biopsy as a substitute to open biopsy in the diagnosis of soft-tissue masses. Eur J Cancer 39(14):2021–2025
22. Hogendoorn PCW, Collin F, Daugaard S, Dei Tos PA, Fisher C, Schneider U, Sciot R/Pathology and Biology Subcommittee of the EORTC Soft Tissue and Bone Sarcoma Group (2004) Changing concepts in the pathological basis of soft tissue and bone sarcoma treatment. Eur J Cancer 40(11):1644–1654 23. Bettio D, Rizzi N, Colombo P, Bianchi P, Gaetani P (2004) Un-
usual cytogenetic findings in a synovial sarcoma arising in the paranasal sinuses. Cancer Genet Cytogenet 155(1):79–81 24. Werner M, Chott A, Fabiano A, Battifora H (2000) Effect of for-
malin tissue fixation and processing on immunohistochem- istry. Am J Surg Pathol 24(7):1016–1019
25. Kurtycz DF, Logrono R, Leopando M, Slattery A, Inhorn SL (1997) Immunocytochemistry controls using cell culture. Di- agn Cytopathol 17(1):74–79
26. Amin MS, Luqman M, Jamal S, Mamoon N, Anwar M (2003) Fine needle aspiration biopsy of soft tissue tumors. J Coll Physicians Surg Pak 13(11):625–628
27. Nagira K,Yamamoto T, Akisue T, Marui T, Hitora T, Nakatani T, Kurosaka M; Ohbayashi C (2002) Reliability of fine-needle as- piration biopsy in the initial diagnosis of soft-tissue lesions.
Diagn Cytopathol 27(6):354–361
28. Gangi A, Guth S, Dietemann J-L, Roy C (2001). Interv Muscu- loskeletal Procedures Radiographics 21:E1-e1 (online only)
