Joint Bone Spine 73 (2006) 532–537 http://france.elsevier.com/direct/BONSOI/

Original article

Percutaneous computed-tomography-guided biopsy of the spine: 229 procedures Hasan Kamil Sucu a,*, Canan Çiçek a, Türkan Rezanko b, Hamdi Bezircioğlu a, Yusuf Erşahin c, Mine Tunakan b, Mustafa Minoğlu a a

Department of Neurosurgery, Atatürk Training and Research Hospital, Izmir, Turkey b Department of Pathology, Atatürk Training and Research Hospital, Izmir, Turkey c Division of Pediatric Neurosurgery, Ege University Faculty of Medicine, Izmir, Turkey Received 7 September 2005; accepted 18 January 2006 Available online 29 March 2006

Abstract Objectives: Percutaneous biopsy of the spine is an effective and well-evaluated procedure. Only very few series containing more than a hundred patients have been reported so far and there is no agreement about the factors affecting the diagnostic rate. We aimed to find out if there is any factor influencing the success rate of the spinal biopsy using our biopsy series. Methods: Two hundred and twenty-nine procedures were performed in 201 patients between November 2001 and August 2005. All procedures were performed under computed tomography guidance. The side was chosen according to the extension of the lesion. When the lesion was in the midline or extended to both sides, we preferred to obtain biopsy from the right side. The puncture point and the needle trajectory were planned on both lateral computed tomography scout scan and axial scans. Results: We found that the diagnostic rate was not affected by the variables such as age, gender, type and diameter of the biopsy needle, diagnosis as well as lesion localization and level. The success rate of the repeat biopsies was considerably lower than the first procedures. Conclusions: The diagnostic rate is not affected by any of the variables but the approach, chosen can vary with the level, localization, and lesion characteristics. © 2006 Elsevier SAS. All rights reserved. Keywords: Computerized tomography; Percutaneous spinal biopsy; Spine

1. Introduction The percutaneous spinal biopsy can provide an accurate diagnosis and facilitate treatment in the various spinal pathological entities. Its efficacy in the management of spinal lesions has been extensively evaluated in the literature [1–9]. The most common approach to biopsy of the vertebral bodies is posterolateral [2–4,7,8]. However, different approaches have been described as an alternative to the classic posterolateral approach because of the technique-related difficulties and the risk of complications. Brugieres et al. [10] described the transcostovertebral approach for performing biopsy in the thoracic region in 1990. One year later Renfrew et al. [7]

* Corresponding

author. E-mail address: [email protected] (H.K. Sucu).

1297-319X/$ - see front matter © 2006 Elsevier SAS. All rights reserved. doi:10.1016/j.jbspin.2006.01.013

published the transpedicular biopsy technique. We also described the transforaminodiskal approach in 2003 [11]. It is generally accepted that the larger needle diameter [3,12, 13] and the osteolytic lesions [8,10,14] are the factors increasing the diagnostic rate in the percutaneous CT-guided spinal biopsies. However dubious results regarding the gender [5,12, 15] and spinal level [5,8,12,14–17] have been shown, and there is no consensus in these matters. There has been no study comparing the diagnostic rates of different biopsy techniques. We aimed to find out if there is any factor influencing the success rate of the spinal biopsy using our biopsy series. 2. Methods Between November 2001 and August 2005, 229 percutaneous spinal biopsy procedures were performed in 201 patients (Table 1). There were 115 male and 86 female patients, ran-

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ging in age from 11 to 81 years (mean 57 years). All biopsy procedures were performed by the two neurosurgeons (HKS, CÇ) and the data regarding the patients and lesion, details of the procedures, type and size of the needles, pathological examinations and results of the cultures were prospectively recorded. The advances in the magnetic resonance imaging allow detection of vertebral lesions at an earlier stage and there is an increase in proportion of vertebral lesions with intensity changes on MRI scans only when the patients are referred for biopsy. Because of this we did not divided the lesions into two groups as osteolytic and osteosclerotic prospectively. Needle biopsy was performed in all spinal column segments, only except for C1 (20 cervical, 66 thoracic, 117 lumbar, 23 sacral, two lumbo-sacral and one coccygeal lesion). In five patients we were able to obtain biopsy samples from two vertebrae at the same puncture (Fig. 1). The target was the posterior part of vertebra in 15 and the anterior part of vertebra (vertebral body) in 214 biopsy procedures. We used the anterolateral approach for uppermost thoracic spine in four cases for the first time to our knowledge (Fig. 2). Anterolateral approach is easier and more reliable than posterior approaches particularly for T1 and some T2 lesions (Table 3). The anterolateral approach to the vertebral body was used in 11 and four times in the cervical region (Fig. S1; see the Supplementary Material available with this article online) and in the uppermost thoracic vertebra, respectively. The subgroups of posterior approach to the vertebral body are as follows: the classical posterolateral (paravertebral) approach in 18, intertransversocostal approach in 20, transpedicular approach in 54 and transforaminodiskal approach in 107 procedures. All procedures were performed under CT guidance. All patients were injected with diazepam and of diclofenac sodium intramuscularly 30 min before the procedure as premedication. The skin of the biopsy site was infiltrated with the local anesthetic (prilocaine). We initially used 14 Gauge (G) Tru-Cut needle (23 patients) and had a difficulty in penetrating the cortical bone (P < 0.0001). Then we started using the 10-cm-long Jhamshidi needles. We switched to the 11G- Jhamshidi needles in order to obtain greater specimen after using the 13G- Jhamshidi needles at first. The side of the approach was determined on the CT scans, obtained just before the procedure. The side that the lesion had been predominantly located was chosen for biopsy. When the lesion was in the midline or extended to both sides, we preferred to obtain biopsy from the right side just because we put the biopsy table on the right sight of the patient. The puncture point and the needle trajectory were planned on both lateral CT scout scan and axial scans. Every biopsy specimen was processed for pathological examinations and culture. In addition, biopsy samples were also sent for acid-fast staining and microscopic examination for searching pathogen microorganism. The inconclusive pathological examinations that had no effect on the management of the patients were considered unsuccessful. Vancomycin, cefotax-

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Fig. 1. (a) 69-year-old male patient had been suspected L5-S1 spondylodiscitis and the diagnosis confirmed by percutaneous spinal biopsy. Jhamshidi biopsy needle is advance perpendicular to the patient’s vertical axis. (b) Entering the pedicle, the needle first passes the S1 corpus then L5-S1 intervertebral disc and L5 corpus lastly. (This procedure could obtain biopsy specimen shaped as a cylinder consisting bone at the both end and intervertebral disc tissue between them.).

ime and rifampicin were administered in patients with non-specific infections. Generally, chi-square tests were used in statistical analyses. Only for comparing the mean ages of diagnostic and non-diagnostic groups t-test was used. P < 0.05 was considered statistically significant. 3. Results 3.1. Diagnostic rates 3.1.1. Overall In 197 of 229 procedures we were able to obtain the biopsy samples from the desired places of the spine. In 15 biopsy sam-

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Table 1 The summary of our 229 biopsy procedures (201 patients)

22

40

7

No follow up, 15 biopsies

No sample, 32 biopsies Biopsy sample couldn’t obtained from the right place of the spine: 31 cases Surgeon related reasons: 6 cases Needle related reasons: 25 cases The needle The needle was The needle The needle Couldn’t reach the punctured the able to puncture the couldn’t puncture the vertebrae in vertebrae but vertebrae in 4 cases wrong place in 6 cases (6 Tru-cut) couldn’t get 2 cases (4 Jhamshidi) enough specimen (1 Jhamshidi, 1 Tru-cut) in 19 cases (18 Jhamshidi, 1 Jhamshidi + Tru-Cut)

The biopsy procedure was abandoned because of the pain: 1 case

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No of biopsies 73

Sample obtained, 197 biopsies Follow up, 182 biopsies Accurate diagnosis, 142 procedures Inconclusive results, 40 procedures No of Type of Pathological diagnosis patients lesion for biopsies (False negative: 22 73 Infection 51 non-specific Misdiagnosis: 4; infections Necrosis or chronic 22 tuberculoses inflammatory granulation 21 Primary 8 lymphoma tissue, but the etiology neoplasm 7 plasmocytoma is not certain: 9 1 chronic myelocytic Etiology is infection, leukemia but it is not certain 1 Ewing’s sarcoma whether it is NSE or 2 chordoma TBC: 3 1 osteoblastoma Etiology is malignancy, 1 chondrosarkoma but the type of it could 1 osteosarkoma not been defined: 2 39 Metastasis 6 lung cancer 4 kidney cancer 2 breast cancer 2 thyroid cancer 2 prostat cancer 1 carcinoma of ovary 1 colon cancer 1 malignant melanoma 21 unknown 6 Normal 6 normal bone

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Table 2 Diagnostic rates for procedures and patients

Procedures Patients Biopsy samples

Total Number 229 201 197

Excluded Number 15 15 15

Diagnosed Cases 142 139 142

Diagnostic rate 66% (142/214) 75% (139/186) 78% (142/182)

3.1.4. First vs. Repeat biopsies Because we had got inconclusive results, in 26 patients biopsy procedures were performed two times and in one patient biopsy procedures were performed three times. The success rates of the first (68.8%) and repeated (44%) biopsies varied significantly (P = 0.014). 3.1.5. Anterior vs. posterior sampling When we sampled the biopsy specimen from the posterior part of vertebrae diagnostic rate was 80.0%. In contrary, diagnostic rate was 65.3% for vertebral body. However this difference was not significant. 3.1.6. Diagnostic rates in terms of level Our diagnostic rate for cervical biopsies (65.0) was not differing from other parts of spine (66.5%). We didn’t find significant difference between the diagnostic rates of the lumbar (65.1%) and thoracic biopsies (68.3%). In our series, the diagnostic rate for sacral biopsies was 68.0% (17/25) and was not different from the other parts of the spine. 3.1.7. Approaches We did not find a difference between the diagnostic rates for different approaches for thoracolumbar region. 3.2. Diagnosis Fig. 2. (a) The anterolateral approach for the uppermost thoracic region. (b) The needle is starting to enter the anterior-inferior part of T2 vertebrae. T3 vertebrae can be seen posterior to the T2 vertebrae.

ples of 15 patients, pathological examination turned out to be a normal bone matrix and had been lost to follow-up. Therefore, the data of these 15 procedures were not included in the statistical analyses. (Table 1). The overall success rates per procedure and per patient were 66% and 75%, respectively (Table 2).

3.1.2. Age–gender We did not find any significant difference between the male’s diagnostic rate (74.8%) and female’s diagnostic rate (74.7%). The mean age of the diagnostic group was 56.3 years and for the non-diagnostic group was 54.1 years. This difference is not statistically significant. 3.1.3. Needle type and diameter The needle types (Jhamshidi vs. tru-cut) did not have a significant difference in terms of diagnostic rate. Also, we did not find any significant difference between the large (8 and 11 gauge) and small (13 gauge) diameter Jhamshidi needles.

We were able to make the diagnosis in 142 biopsy procedures (139 patients) (Table 1). In four patients the pathological diagnosis of needle biopsy was different from that of the open surgery. The different pathological diagnoses of needle biopsy and open surgery were as follows: lymphoma and Ewing sarcoma in S2, non-specific infection and plasmocytoma in T2 and T4, indifferent malignant tumor and myxopapillary ependymoma in S5, respectively. The culture from the biopsy material was positive in only 10 patients (9 Mycobacterium tuberculosis and one Kytococcus sedentarius). 3.3. Complications We had one major complication. In a 69-year-old male patient who had undergone a spinal biopsy using the classic posterolateral approach, a large retroperitoneal hematoma developed (Fig. S2). The patient was operated on for the hematoma and survived. No vessel injury was detected at surgery and bleeding was presumably from the psoas muscle. Only one patient could not tolerate the pain and we had to abandon the procedure. In all other patients no back or radicular pain was observed, either immediately after biopsy or dur-

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Table 3 Summary of the recommended biopsy approaches according to the level of the lesions Condition Lesion in both anterior (vertebral body) and posterior (neural arch) of the vertebra Lesion in several vertebrae

Lesion in or near the pedicle Lesion in cervical region Lesion in T1 vertebral body Lesion in T2 vertebral body patient’s neck is long and thin. Lesion in the disc space of T2–L5 a large paravertebral mass Lesion in T3–T6 vertebral body Lesion in T7–L5 vertebral body and near upper end plate Lesion in T7–L5 vertebral body and near lower end plate Lesion in L5–S1 disc space with neighboring end plates Lesion in the sacrum

Recommendation Obtain the biopsy specimen from the posterior part of vertebrae Select the lumbar region first because it is easy to perform the biopsy procedure and it has lower complication risk, higher diagnostic rate and then select the sacral region and lower complication risk Transpedicular Anterolateral approach Anterolateral approach Anterolateral or transpedicular approach Posterolateral approach Posterolateral approach Transcostovertebral approach Transforaminodiscal approach Transpedicular approach Perform transpediculo-disco-vertebral approach Transpedicular approach

ing the days that followed, and no complications were observed. 4. Discussion Many authors have suggested that some factors may influence the success rate of spinal biopsies. Kattapuram et al. [12] found the mean age of the diagnostic group (56 years) older than the non-diagnostic group (54 years) and proposed that there was a trend toward better results in female patients (97%) than in male (86%). Fyfe et al. [3], Kattapuram et al. [12], and Ward et al. [13] reported that larger needles in diameter had a higher diagnostic rate than the smaller ones. Diagnostic rates were compared mainly between thoracic biopsies and lumbar biopsies in the reported series. Generally lower diagnostic rates were found in thoracic level biopsies in many previous studies [8,14–16]. Brugieres et al. [16] and Lis et al. [5] found high accuracy rates (90% and 100% respectively) for cervical biopsies. Kattapuram et al. [12], Kornblum et al. [15] and Lis et al. [5] reported similar high diagnostic rates for sacral biopsies such as 86.7%, 92%, and 96% respectively. On contrary, Ozerdemoglu et al. [17] found very low diagnostic rate for sacral needle biopsies (12%). In spite of these reports we did not find any relation between the success rate of spinal biopsies and the factors above mentioned. Similarly, we did not find a difference between the diagnostic rates for different approaches but we have learnt from our experiences that different approaches can be appropriate for different conditions (Table 3). Posterolateral (paravertebral) approach should not be the first choice because of its high complication risk [3,8,10,12], except for the disc space biopsies [6]. It can also be preferred in large paravertebral masses or abscesses. The transcostovertebral approach can be performed in thoracic region only. A narrow space between the elongated transverse process and neighboring rib may hinder the penetration of the vertebral body. Although the transpedicular technique seems to be reliable [7,13], it is not easy to penetrate the cortical shell of the bone [11]. Another limiting factor of the transpedicular ap-

proach can be the pedicle width. [18,19]. This technique is particularly useful when the lesion is located in or near the pedicle. The approach we used mostly was the transforaminodiscal one, because of its easy application and a low complication risk [11]. We prefer this approach especially to obtain biopsy sample from the cranial part of vertebra. The biopsy procedure can be repeated easily if the first one fails. However the success rate in the repeat biopsies was considerably lower than that of the first biopsies. Performing a repeat biopsy may lead to a delay in the appropriate treatment. Instead of the needle biopsy, open biopsy can be considered in those cases. The technically difficult location and the patient’s incompatibility may presumably lead to the lower diagnostic rate of repeat biopsies. In conclusion, percutaneous spinal biopsy is a simple and repeatable procedure. Its complication rate is acceptable. Patients usually tolerate spinal biopsy well with local anesthesia. The diagnostic rate does not seem to vary with any of the variables evaluated in this study. Supplementary Material Supplementary data (Fig. S1, S2) associated with this article can be found, in the online version, at doi: 10.1016/j. jbspin.2006.01.013. References [1] Babu NV, Titus VT, Chittaranjan S, Abraham G, Prem H, Korula RJ. Computed tomographically guided biopsy of the spine. Spine 1994;19: 2436–42. [2] Bender CE, Berquist TH, Wold LE. Imaging-assisted percutaneous biopsy of the thoracic spine. Mayo Clin Proc 1986;61:942–50. [3] Fyfe IS, Henry AP, Mulholland RC. Closed vertebral biopsy. J Bone Joint Surg Br 1983;65:140–3. [4] Laredo JD, Bard M. Thoracic spine: percutaneous trephine biopsy. Radiology 1986;160:485–9. [5] Lis E, Bilsky MH, Pisinski L, Boland P, Healey JH, O’Malley B, et al. Percutaneous CT-guided biopsy of osseous lesion of the spine in patients with known or suspected malignancy. AJNR 2004;25:1583–8.

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