The advantages of ultrasound-guided biopsy for the diagnosis of musculoskeletal tissue lesions are well-known(1–3). A modern approach to diagnosis and the importance of the multidisciplinary tumor board in patient survival have been emphasized(4–6). Diagnostic imaging with radiography, magnetic resonance imaging (MRI), computed tomography (CT), and ultrasonography is helpful in the process of differential diagnosis. It is, however, difficult in most cases to sufficiently narrow the range of differential diagnoses of a soft tissue lesion using radiology alone. A histopathological verification may be necessary in cases where the radiological signs are not typical or the clinical presentation is inconsistent with the radiological findings(7). Ultrasound-guided core needle biopsy (US-CNB) is performed not only to make the diagnosis, but also to assess tumor viability, which helps to choose the optimal treatment. Biopsy accuracy has been reported as ranging between 60% and 97% for ultrasound-guided biopsy. It varies between reports because of different indications, different selection of needles (fine or core needle) and different selection of lesions(1,3,8–14). The success of a biopsy – measured by the ability of establishing a histopathological diagnosis from a tissue sample – may depend on the selection of patients, so multidisciplinary cooperation is necessary(7,13).
US-CNB is a safe procedure, without major complications. Pain, bleeding, needle breakage, nerve or vessel injury, or pneumothorax, occur rarely (0.5–10%)(7,14). The rate of complications after surgical or excisional biopsy has been reported as higher than for US-CNB (8–17%)(2,9,12,13). It is possible to improve the safety of the biopsy procedure by using ultrasound guidance with color Doppler, thus avoiding injury to major vessels or nerves adjacent to the tumor(7,8). The risk of neoplastic seeding in the needle tract is much lower compared to surgical biopsy, the rate being reported at approximately 0,003-0,005% or not observed at all(8,13,15,16).
The current study aimed to assess the value of ultrasound-guided biopsy of solid tumors in the musculoskeletal system using a 16-gauge needle.
The study site is a university hospital with a dedicated multidisciplinary team concerned with the diagnosis and treatment of bone and soft-tissue sarcomas. In a retrospective analysis, a total of 102 referrals were received for ultrasound-guided biopsy of a musculoskeletal soft tissue lesion during 2019. The exclusion criteria were fear of medical procedures involving needles (4 patients), purely cystic lesions (6 patients), and biopsy of lymph nodes (5 patients) (Fig. 1). Further 12 patients were excluded from the study since their biopsy was performed under CT guidance. Ultimately, 73 patients with a primary US-CNB of a soft tissue lesion in the musculoskeletal system were included. The group of 73 patients included 34 males and 39 females, with a mean age of 57.7 years (range 8–89). The most common localization of lesions was the lower extremity, followed by the upper extremity. The patients were followed up for at least 6 months (
All the procedures were performed using a LOGIQ E9 (General Electrics) ultrasound scanner with a linear or convex transducer, as appropriate. The shortest distance from the skin to the lesion was measured on the ultrasound scan. The mean volume of the lesion was calculated by the formula for volume in ultrasound(17). A 16-gauge automatic biopsy needle with a coaxial introducer needle was used. All the procedures were done by radiologists specializing in musculoskeletal radiology. Under local anesthesia (maximum 10 ml Mepivacain 10 mg/ml), in sterile conditions, and with ultrasound guidance, at least 2 core biopsy samples were obtained with a minimum length of 1 cm, and fixed in 10% formaldehyde. All patients were observed for at least 30 minutes after the procedure to check for complications, and received information about possible late complications.
All biopsy specimens were evaluated by pathologists specializing in musculoskeletal pathology at the study hospital. There are no strict definitions related to the evaluation of biopsy effectiveness. In the current study, the following classification was applied: biopsies were classified as diagnostic or not, and accurate or not, based on the pathological findings and the clinical follow-up data. A biopsy was considered diagnostic when a definitive pathological diagnosis could be made from the first biopsy, which was consistent with the clinical findings and follow-up. A biopsy was considered accurate if the tumor could be classified as malignant or benign, and the classification was consistent with subsequent findings from a repeat biopsy, an excisional biopsy, or with the clinical findings, and there was at least 6 months’ clinical and radiological follow-up. The overall biopsy success was estimated as the sum of diagnostic biopsies and accurate biopsies, divided by the total number of procedures.
We investigated whether lesions in the groups of accurate and diagnostic biopsies differed regarding calcifications, fat, volume, depth to the skin surface, and their malignant or benign nature.
A
Statistical analysis was performed using SPSS 8.0.
Bioethical approval for the current retrospective study was obtained, and the need for informed consent was waived (2020.00158).
In all 73 patients, US-CNB provided enough tissue to make a histopathological diagnosis in 61 diagnostic biopsies (84%) (Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8, Tab. 1). The number of diagnostic biopsies was higher in the group of malignant lesions than benign lesions (88% vs. 81%,
Biopsy | Malignant lesion |
Benign |
lesion 47 | Overall |
||
---|---|---|---|---|---|---|
n | % | n | % | n | % | |
Diagnostic | 23 | 88% | 38 | 81% | 61 | 84% |
Accurate | 3 | 12% | 9 | 19% | 12 | 16% |
Inaccurate | 0 | 0% | 0 | 0% | 0 | 0% |
Successful | 26 | 100% | 47 | 100% | 73 | 100% |
Final diagnosis for accurate biopsies in alphabetical order |
---|
Benign peripheral nerve sheath tumor (Fig. 9) |
Endometriosis |
Giant cell tumor |
Metastatic chondroblastoma |
Myositis ossificans |
Nodular fasciitis (Fig. 11) |
Osteoblastoma (Fig. 10) |
Unclear case, malign tumor, probably low-grade myxofibrosarcoma, |
[1 mitosis per 10 high power fields] |
Benign, mesenchymal tissue, without atypia |
Vascular malformation (Fig. 8), 2 patients |
Well-differentiated liposarcoma |
The study cohort comprised mostly benign lesions (64%; Tab. 3). The three most common benign lesions were tumor-like lesions (inflammation; Fig. 7), lipoma, and desmoid. Regarding malignant lesions, liposarcoma (Fig. 3) and metastasis were the most common.
Benign | Malignant | ||
---|---|---|---|
Inflammation | 8 | Well-differentiated liposarcoma | 7 |
Lipoma | 6 | Chondrosarcoma | 2 |
Desmoid | 5 | Metastatic gastric cancer | 2 |
Vascular malformation | 4 | Metastatic malignant me- | 2 |
Intramuscular lipoma | 3 | Pleomorphic spindle cell sarcoma (high grade) | 2 |
Myxoma | 3 | Dedifferentiated liposarcoma | 1 |
Neurofibroma | 2 | Leiomyosarcoma | 1 |
Pigmented villonodular synovitis | 2 | Lymphoma | 1 |
Atheroma | 1 | Metastatic breast cancer | 1 |
Endometriosis | 1 | Metastatic chondroblastoma | 1 |
Fibroma | 1 | Metastatic lung cancer | 1 |
Giant cell tumor (CT) | 1 | Metastatic prostate cancer | 1 |
Hematoma | 1 | Metastatic squamous cell carcinoma | 1 |
Hibernoma | 1 | Myeloma/plasmocytoma | 1 |
Lipoma arborescens | 1 | Recurrent Ewing’s sarcoma | 1 |
Myositis ossificans (CT) | 1 |
|
|
Nodular fasciitis (CT) | 1 |
|
|
Osteomyelitis | 1 | Benign, mesenchymal tissue, without atypia | 1 |
Schwannoma | 1 | Malign, unclear case, probably low-grade myxofibro-sarcoma | 1 |
Solitary fibrous tumor | 1 | [1 mitosis per 10 high power fields] | |
Vascular hamartoma | 1 |
|
|
|
|
Two cases could only be classified as benign or malignant without a definitive pathological diagnosis (Tab. 3). In a single case, there was enough material to determine the benign nature of the lesion; however, no unequivocal final diagnosis could be made, so the biopsy was classified as accurate but not diagnostic. In another case, a low-grade myxofibrosarcoma was considered on histopathology; however, it was inconsistent with other tests (Tab. 1, Tab. 3). The biopsy was repeated without a definitive pathological diagnosis; however, the malignant character was upheld. The working diagnosis became myxofibrosarcoma.
The average minimum distance from the skin to the lesion was 11 mm (range 2–50 mm), while the mean volume was 70.4 ml (range 0.02–1724 ml). The mean volume of the tumor in accurate biopsies was 154.2 ml vs. 27.8 ml in diagnostic biopsies (
|
|
|
|
---|---|---|---|
Average age [years] | 47 | 60 | |
SD |
26.1 |
18.2 |
0.13 |
max | 75 | 89 | |
Male [ |
6 |
31 |
0.96 |
Benign [ |
9 |
38 |
0.35 |
Malign [ |
3 |
23 |
0.28 |
Fat [ |
2 |
13 |
0.44 |
Calcification [ |
3 |
3 |
0.27 |
Volume [cm3] | 154.2 | 27.8 | |
SD |
494.7 |
64.0 |
<0.001 |
max | 1724.8 | 415.8 | |
Depth [mm] | 12.8 | 9.7 | |
SD |
7.6 |
7.8 |
0.18 |
max | 27.4 | 31.5 |
Upper extremity | 26 |
Shoulder | 11 |
Upper arm | 7 |
Elbow | 3 |
Forearm | 5 |
Lower extremity | 35 |
Pelvis and hip | 13 |
Thigh | 12 |
Knee | 5 |
Lower leg | 4 |
Ankle | 1 |
Trunk | 12 |
Chest wall | 5 |
Abdominal wall and retroperitoneal space | 4 |
Paravertebral soft tissue | 3 |
Total | 73 |
Appropriate treatment of soft tissue tumors in the musculoskeletal system requires an unquestionable diagnosis. In many cases, the radiological image may not be typical or might not match the clinical symptoms. In such situations, histopathological confirmation of the diagnosis is necessary(7,13). US-CNB is suitable for making a diagnosis in such borderline or unclear cases where the radiological signs or clinical symptoms are ambiguous(2,7).
A final diagnosis, without differential diagnoses (called a
Most of previously published reports rely on retrospective data, so similarly to the current study, information about the exact quantity of the tissue samples taken during biopsy may be lacking. There are also differences in the needles used during biopsy. Some studies have used 14-gauge to 23-gauge biopsy needles(8,10,19), while in the current study all biopsies were performed with a 16-gauge needle.
US-CNB allows the safe passage of the biopsy needle even into small and difficult-to-reach lesions, so that damage to important structures including the nerves or vessels can be avoided(7,20). Ultrasound guidance has a well-established position in the multidisciplinary diagnosis of musculoskeletal lesions because of its high accuracy and low complication rate. However, the success of a biopsy seems to be variable and depending on several factors such as operator expertise, tumor structure, amount of retrieved material, needle diameter, and patient selection(2,9,18).
In our study, we demonstrated a difference in tumor volume between the accurate and diagnostic biopsy groups. We found a significantly higher volume of tumor in the group of accurate biopsies compared to diagnostic biopsies. This may seem paradoxical, but larger tumors tend to be more heterogeneous, with more necrosis, making it more challenging to collect an appropriate tissue sample. The procedure of tissue sample collection from larger and more heterogeneous tumors can be challenging, as it requires performing a biopsy in different directions to obtain samples from various parts of the tumor. It is easier to assess the structure of more solid and homogenous tumors on ultrasound and thus simpler to perform a biopsy, with better yield(8–10). However, there are some studies of non-musculoskeletal tumors where the size of the lesion was not correlated with biopsy success(26). Patient selection and the smaller number of patients in the group of malignant tumors may also have affected our observations.
There are some disadvantages of US-CNB compared to open biopsy(3,12,24). The main disadvantage is the smaller amount of retrieved tissue, which may require additional tests to obtain the final diagnosis(20). We have not shown any significant differences in tumor depth between the groups of benign and malignant lesions. With more deeply located tumors, it is harder to obtain a good quality of tissue sample using ultrasound; therefore CT-guided biopsy should be taken into consideration in such cases(9,19). In previous studies, a high value of biopsy has been shown even for lesions smaller than 2 cm(24). A perusal of the literature has not revealed any previous reports correlating biopsy success or accuracy with lesion volume. Most typically, only one dimension is used, which does not fully characterize the tumor(24).
The presence of calcifications or fat in the tumor may have an influence on tumor visualization on ultrasound, which may correlate with the ability to collect appropriate tissue material. In the current study, the incidence of diagnostic biopsy was higher, though without statistical significance, in the group of malignant lesions, which is in contrast with previously published results(10,12,20).
Diagnostic imaging is crucial when considering lesions for imaging-guided biopsy. Some benign lesions may mimic malignant lesions at the microscopic examination. An example of such a lesion is myositis ossificans, which may resemble osteosarcoma(27) in the histopathological examination, but the radiological image is more characteristic. Therefore, the radiologist’s role is to prevent an unnecessary biopsy when a typical radiological image is obtained.
There are some limitations of the current study, such as its retrospective character. Furthermore, only some of the patients were operated on, so the results of excisional biopsies are available in only a few cases. Finally, information about the quantity and length of the tissue sample was often missing.
In conclusion, the diagnostic value of ultrasound-guided percutaneous core needle biopsy of musculoskeletal soft tissue lesions performed with 16-gauge needle is good, with a high rate of diagnostic biopsies, both for benign and malignant lesions. Ultrasound-guided core biopsy of solid musculoskeletal lesions is an important tool to obtain tissue samples after an appropriate selection of patients based on previous CT or MRI evaluation. Factors including the presence of fat, calcification, benign or malignant character of the tumor, depth or anatomical localization do not differ significantly between groups of accurate and diagnostic biopsies. Tumor volume varied between the study groups, and was higher in the group of accurate biopsies. A multidisciplinary approach to the diagnosis of soft tissue tumors facilitates an appropriate selection of patients for this procedure.