Image-guided percutaneous biopsy and pathological diagnosis in atypical tuberculous spondylitis: a case series and clinical outcomes

Introduction

Tuberculosis (TB) is caused by Mycobacterium tuberculosis (M. tuberculosis) and is more common in older people and immune-compromised populations like HIV positive patients (1). The spine is the most common site of musculoskeletal TB. Tuberculous spondylitis was originally known as Pott’s Disease and represents the most common form of extrapulmonary TB (2-4).

The typical imaging manifestation of spinal TB is vertebral destruction caused by the spread of infection originating from the intervertebral space to the opposing end plates and two adjacent vertebral bodies, with or without a paravertebral abscess (5). Spinal TB without the typical features mentioned above is harder to recognize and diagnose (6), and degenerative disc disease, pyogenic and fungal infections, or inflammatory and neoplastic lesions are common differential diagnoses under these circumstances. The atypical imaging manifestations and the wide range of clinical presentations for patients with spinal TB may result in difficulties and delays in diagnosis, with possible associated unnecessary morbidity (1-3). The treatment of atypical tuberculous spondylitis reported in the literature is mostly in the form of case report and literature review. A study with a larger sample size with a consequence of the selectivity of the inclusion criteria and the size population like ours, presents a valuable opportunity for further investigation on this issue.

Image-guided percutaneous biopsy plays an essential role in the diagnosis of musculoskeletal lesions. Its accuracy, safety, and cost-effectiveness have been well documented (4). But given the rarity of atypical tuberculous spondylitis, there has been a lack of reports validating the feasibility and results on the use of image-guided percutaneous biopsy and histopathological analysis for the diagnosis of atypical tuberculous spondylitis. Here, we retrospectively report a group of atypical imaging features of TB spondylitis diagnosed by image-guided percutaneous biopsy and pathological analysis. This study aims to underscore the utility and importance of image-guided percutaneous biopsy in the diagnosis of TB spondylitis with atypical imaging features, as well as describe the associated clinical features and outcomes. We present the following article in accordance with the STROBE and AME Case Series reporting checklists (available at https://atm.amegroups.com/article/view/10.21037/atm-22-4661/rc).

Methods

We retrospectively reviewed the medical records and follow-up results of patients admitted to The Third Affiliated Hospital of Southern Medical University between 2013 and 2020 who were diagnosed with TB spondylitis. From this cohort, patients with atypical imaging features were selected after review of their imaging and medical records. The definition of atypical imaging features in spinal TB were as follows: anterior subperiosteal lesion, central vertebral bony lesion with disc preservation, multivertebral lesions (skip lesions), isolated involvement of the posterior elements of the vertebral body, extradural mass lesion, and intramedullary lesion (tuberculoma) (3,6-9). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics committee of The Third Affiliated Hospital of Southern Medical University (No. 2022-008). Informed consent was taken from all the patients.

For each patient identified, clinical presentations, physical examinations, routine laboratory tests [including erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), tuberculin skin testing with purified protein derivative (PPD), serum tuberculosis antibody (TA) IgG], imaging and histopathology studies, management, and clinical and imaging outcomes were reviewed. Biopsy was performed under image-guided CT or C-arm fluoroscopy. The route of the needle puncture was based on the location and extent of the lesion. In the presence of multiple lesions, puncture was performed on the most viable and safest part of the lesion. Guided by imaging, a standard 12-gauge core needle biopsy set (Guanlong, Shandong, China) was used to perform the biopsy. After confirming the needle tip had reached the lesion, a specimen was obtained, and the needle was withdrawn. The samples obtained from the biopsy were submitted for cytologic, histologic, and bacteriologic examination. The diagnosis of TB spondylitis was confirmed when the tissue culture positive for M. tuberculosis, or the histological and cytological examination of specimens revealed granulomas, multinucleated giant cells, Langhans’ giant cells, or Ziehl-Neelsen staining demonstrating acid-fast bacilli (AFB).

Surgery was considered for those patients who had vertebral compression with progressive neurological symptoms or unstable vertebral column deformity. Vertebral surgery was performed under general anesthesia in a prone position. After exposing the lamina, facet joints, and transverse processes from the posterior midline approach, transpedicular screws were installed in the thoracolumbar vertebral body at least one level above and below the diseased vertebra(e). A temporary rod was fixed to stabilize the spine and avoid spinal cord injury during decompression and debridement. A unilateral facetectomy and semi-laminectomy decompression were then performed on the affected side. After pediculectomy of the affected vertebra(e), curettage of the lesion in the vertebral body was performed using the transpedicular approach. The cavity formed after debridement of the lesion inside the vertebral body was filled with autogenous bone from the healthy lamina or an autogenous iliac bone graft, and correction of the deformity was accomplished by installing permanent rods with moderate compression maneuvers. Debridement and decompression without fixation were performed in patients with severe neurological defects or progressive neurological symptoms, with slight bone destruction and good spinal stability.

A combination of anti-tuberculous medications was given to all the patients for a total of 1 year once confirmed as TB spondylitis, including rifampicin (RMP) 450 mg/day, ethambutol (EMB) 750 mg/day, pyrazinamide (PZA) 750 mg/day, and isoniazid (INH) 300 mg/day. Streptomycin [(SM) 750 mg/day] was only given in the first month to avoid the possible cumulative dose ototoxicity. A decreased ESR and CRP was considered a useful measure of valid response to the treatment. Renal and liver functioning were monitored dynamically to detect hepatorenal toxicity when the patient was taking an anti-tuberculous medication.

Radiographs, CT scans and MR imaging were taken of each patient before hospital discharge and during follow-up, monitoring the sites for bone healing or bone graft fusion, hardware failure, as well as signs of recurrence. The incidence of complications (intra- and postoperative), changes in neurological status at the final follow-up, and clinical outcomes were evaluated. Neurological function was evaluated according to the Frankel grading system. The patients’ clinical outcomes were evaluated by Visual Analogic Scale (VAS) scores for pain, imaging [X-ray, computed tomography (CT), and magnetic resonance imaging (MRI)] results, and laboratory examination.

Statistical analysis

Comparison of VAS scores was made by Student t-test. All statistical analyses were performed using SPSS version 19.0 (IBM Corp., Armonk, NY, USA). A P<0.05 was considered statistically significant.

Results

Eight patients (two females and six males) with a mean age of 41.6 years (range, 18–61 years) met these criteria (Table 1). All the eight patients presented with atypical imaging features of spinal TB: three had central vertebral body lesion with preserved discs, three had multiple skip vertebral lesions, one had extradural mass lesion, and one had anterior subperiosteal lesion. All patients presented with back pain and tenderness. Two patients had unexplained recurrent fever, one had mild kyphosis deformity in the thoracolumbar junction, and six had neurologic deficits on physical and neurological examinations. HIV and PPD tests were negative in all eight patients. TB antibody tests were positive in two cases. Bacteriologic culture results were negative in all cases except one case was not submitted for examination. Serum T cell spot test of TB infection (T-SPOT) and TB PCR (GeneXpertMTB/RIF) tests were only performed at our hospital after 2016, and when these results were available, they were included in the review. The T-SPOT test was performed in two cases, both with negative results. GeneXpertMTB was performed in one case with negative result. All eight patients received a confirmed diagnosis of TB following histological and cytological examination of the specimens obtained by image-guided biopsy, which revealed granulomas, multinucleated giant cells, Langhans’ giant cells, or Ziehl-Neelsen staining demonstrating AFB. All patients received anti-TB medication for one year. Two patients who had no neurological deficit symptoms received anti-TB medication alone. Five patients underwent surgery that included decompression by laminectomy, transpedicular curettage of the lesions, and stabilization of the spine using a posterior approach. One patient received debridement and decompression of the thoracic spine without fixation due to progressive neurological symptoms. This patient suffered pleural effusion after debridement of the thoracic lesion, which resolved after thoracic drainage. All patients were followed up for at least 6 months after treatment completion (median, 16.2 months; range, 6–37 months). Decreased VAS scores and improved neurological function were observed in all patients. At the final follow-up, back pain and neurological deficits had completely resolved in all cases. Solid fusion and osteogenic osteosclerosis were observed at the last follow-up, and no recurrence was observed in any patients. No complications were observed during the follow-up period.

Figures 1-3 illustrate the process of diagnosis and treatment in 3 of our patients.

Figure 1 A 41-year-old woman with atypical spinal TB at L3. (A) Sagittal MR image showing lobulated pre- and paravertebral lesion at the L3 level. (B) Enhanced MRI scan revealing rim enhancement of the L3 vertebral and paravertebral lesions. (C) Sagittal CT images show bony destruction involving the L3 vertebra. (D) Axial MR image shows the involvement of the L3 vertebral body and the posterior elements associated with posterior epidural extension, forming an epidural lesion and causing a slight degree of dural compression. (E) Axial CT image showing osteolytic destruction of the L3 vertebral body. (F,G) Biopsy is performed using a transpedicular approach of the L3 vertebral body lesion. (H) The histopathologic analysis reveals fibro-collagenous tissue with numerous epithelioid granulomata mixed with multinucleated giant cells (HE staining, ×100). (I) Ziehl-Neelsen staining (×400) demonstrates AFB (arrows). (J,K) Postoperative anteroposterior and lateral X-ray images. (L,M) Axial and sagittal CT images show good fusion of the bone grafts inside the L3 vertebral body one year after surgery. TB, tuberculosis; MR, magnetic resonance; AFB, acid-fast bacilli; CT, computed tomography; HE, hematoxylin and eosin.

Figure 2 A 58-year-old woman with multiple osteolytic lesions. (A,B) X-rays of the right humerus, right radius, and left fibula demonstrated lytic bone lesions (arrows). (C,D) CT imaging of the chest and thoracic spine showed bilateral pleural effusion, osteolysis, and secondary pathologic fracture of the T8 vertebra. (E) Using a posterolateral approach biopsy is performed of the right humerus lesion. (F) The histopathologic analysis revealed damaged bone tissue with numerous neutrophils without granulomata. Ziehl-Neelsen staining (×400) shows AFB (arrows). CT, computed tomography; AFB, acid-fast bacilli.

Figure 3 An 18-year-old man with atypical spinal TB in the lumbar spine. (A,C) Axial and sagittal MR images show lytic lesions in the first and fifth lumbar vertebral bodies and the third lumbar vertebral pedicle without disc involvement. (B,D) Axial and sagittal CT images show collapse of the L1 vertebral body in addition to dural sac compression. (E) The histopathology shows fibro-collagenous tissue with numerous epithelioid cells mixed with multinucleated giant cells. Extensive areas of caseous necrosis are seen (HE staining, ×100). (F) Ziehl-Neelsen staining (×400) shows AFB (arrows). (G,H) Postoperative axial and sagittal CT images. (I,J) Axial and sagittal CT images one year postoperatively show good fusion of the bone grafts inside the L1 vertebral body. TB, tuberculosis; CT, computed tomography; HE, hematoxylin and eosin; AFB, acid-fast bacilli.

Discussion

Spinal TB is one of the oldest diseases known to mankind and has a common occurrence with high morbidity and mortality, particularly in those with low immunity or poor nutritional status (5). Early diagnosis and treatment are considered the most important strategies to preserve neurological function and prevent spinal deformity (5). However, there are insufficient discussions on the diagnostic and treatment criteria for spinal TB with atypical imaging findings.

Biopsy is indicated when a lesion requires tissue sampling to establish aetiology, or to understand important treatment or prognostic information (5). In cases of possible spinal TB, tissue biopsy is important, not only because the diagnosis can often be adequately made on the basis of supporting histological features or the presence of AFB, but because a positive culture for M. tuberculosis remains the gold-standard for diagnosis and allows for drug susceptibility testing which is critical in guiding treatment. Tissue biopsy is essential in those cases where imaging features are not typical, as a combination of histological assessment, microscopy to detect the presence of AFB and tissue culture can differentiate TB spondylitis from alternative diagnoses such as vertebral neoplasm or pyogenic spondylitis (5). Compared to incisional biopsy, image-guided percutaneous needle biopsy is safer. The latter approach offers precise spatial localization and is relatively safe procedure with lower risk of complications (10). Reported percutaneous risk rates are 0–10% compared to 16% for open biopsy (11,12). Hemorrhage, nerve injury, and infection are the main complications in percutaneous biopsy (11).

Currently, CT-guided bone biopsy is considered to be the best modality (13). It provides an accurate three-dimensional image of the lesion location, allowing better navigation of the puncture route to safely avoid injury to neurovascular structures (13,14). Puncture needle biopsy guided by C-arm fluoroscopy is also commonly used to perform bone biopsies. Compared to CT, fluoroscopy has less ionizing radiation, a lower cost, and a shorter procedure time. However, its accuracy in targeting lesions is less precise, especially with soft tissue lesions. Therefore, C-arm fluoroscopy is reserved for biopsies of large bone lesions without vital neurovascular structure involvement.

Most percutaneous vertebral biopsies are performed using a posterior approach. An approach through bone structures (transpedicular) is safer than traversing through soft tissue and has greater yield for lytic than blastic lesions (5). The transpedicular procedure is the safest way to biopsy lesions from a vertebral body without violating the epidural space. Care must be taken to avoid breakage of the pedicle with consequent epidural space contamination (15). When multiple lesions are present, the selection of the biopsy site and puncture approach should be carefully considered, including safety issues, ease of accessibility, and the most representative lesion found on imaging.

Etiological confirmation can be made either by demonstration of AFB on the pathological specimens and/or histopathological evidence of necrotizing (or non-necrotizing) granulomatous inflammation in the appropriate clinical context (16). Ziehl-Neelsen staining for AFB has low sensitivity and specificity, particularly for pauci-bacillary TB as is commonly the case in TB spondylitis (17). Indeed, only a 52% smear positivity rate for AFB has been reported for spinal TB (18). Cytologic examination of the sample can help confirm the inflammatory process, including direct visualization of pathogen with proper staining. In our case series, AFB were observed microscopically in five cases, suggesting a diagnosis of TB. Ultimately, clinical and radiological resolution with TB treatment provides further reassurance as to the underlying diagnosis of TB spondylitis in each of these eight cases. The culture positivity rate of M. tuberculosis has been reported to be 83% in spinal TB (18); in contrast, negative positive culture results were demonstrated in seven of our cases who received bacteriologic culture. Our results of failed positive culture may be due to the fact that most patients were receiving anti-TB medication at the time of the biopsy. Therefore, histological evidence for a diagnosis of TB is critical for timely treatment. The literature shows that approximately 60% of spinal TB diagnoses are confirmed by histology (5). Epithelioid cell granulomas, granulomatous necrotic background, and lymphocytic infiltration are the three most common histopathologic findings (19,20), whereas typical scattered multinucleated and Langhans’ giant cells were observed in only 56% of the patients (19). False-negative biopsy results in TB are not uncommon. When bacteriology proves negative, an empiric treatment with anti-TB medication can be considered if the clinical symptoms and imaging are consistent with spinal TB (5).

The treatment principles for spinal TB with atypical imaging findings are similar to cases with typical imaging findings (21). Anti-TB medication treatment is considered essential and should be started as early as the diagnosis is made or highly suspected, preferably after tissue sampling is obtained (5). The precise role of surgery in the management of spinal TB is controversial. Previous study have reported that different levels of neurological recovery can be observed in approximately 40% of spinal TB patients with paraplegia who are treated with anti-TB treatment, rest, and/ or traction without spinal surgery (22). Anti-TB treatment alone can be effective in improving neurological symptoms and preventing the progression of spinal deformity (22,23). In some cases, however, surgery may be indicated and can provide benefits such as more timely pain relief, effective neurological recovery, less deformity progression, earlier mobility, a higher bone fusion rate, and a shorter hospital stay (5). Some experts have suggested that indications for surgery include tissue sampling for diagnosis when less invasive approaches are not feasible or available, clinical deterioration or lack of clinical improvement, progressive neurological deficit, recurrent neurologic complications, abscess drainage in the cervical spine, large paravertebral abscess drainage, spinal instability, pan-vertebral lesions, severe kyphotic deformity, and refractory disease (24-30).

Oguz et al. (27) proposed a new classification to guide the surgical treatment of spinal TB based on seven clinical and radiological criteria (abscess formation, disc degeneration, vertebral collapse, kyphosis, sagittal index, instability, and neurological problems). This classification system divides spinal TB into three types and recommends specific treatment approaches for each type (drug treatment alone or with abscess drainage and debridement, debridement and fusion with or without decompression, and correction of deformity with internal fixation). Nearly two decades ago, we first reported the one-stage anterior interbody autografting and instrumentation in thoracolumbar spinal TB, resulting in remarkable clinical efficacy (28). In the present study, one-stage posterior debridement using the transpedicular approach was adopted in two cases, followed by anti-TB treatment. Recently, Wang et al. (29) reported that one-stage posterior debridement using titanium mesh cages and posterior instrumentation, achieving excellent clinical results in aged patients with lumbosacral spinal TB. One-stage anterior or posterior surgery in selected cases can significantly improve the efficiency and safety of the operation. These types of surgical approaches for treatment of spinal TB are viable and safe surgical options (27). The appropriate choice of timing, indication, and surgical intervention procedure is vital when treating spinal TB (31-33).

Limitations of this study include: (I) retrospective analysis and thus the possibility of patient selection bias for biopsy; (II) single center experience and referral bias; (III) possibility of both false positive and false negative diagnoses given the lack of sensitivity of the gold standard of tissue culture and TB PCR on pauci-bacillary specimens, which would be inherent in all such studies.

In summary, spinal TB with atypical imaging features has been well documented but is difficult to distinguish from nonspecific infections and malignancies, which can lead to misdiagnosis and inappropriate treatment. However, when diagnosed and adequately treated, long term clinical, microbiological and radiological outcomes are favourable. Unless the clinical and imaging findings are very strongly supportive of a diagnosis of TB spondylitis, pathological analysis should always be conducted to help confirm the diagnosis. Additionally image-guided biopsy to obtain samples for mycobacterial culture (+/− PCR) should always be strongly considered where TB is in the differential diagnosis, in order to not only confirm the diagnosis of spinal TB but to determine the drug susceptibility profile.

Acknowledgments

We acknowledge all authors whose publications are referred to in our article. The authors appreciate the academic support from the AME Tuberculous Collaborative Group.

Funding: This work was financially supported by the Research and Development Projects in Key Areas of Guangdong Province (No. 2019B020201015 to Haomiao Li) and the Natural Science Foundation of Guangdong Province (No. 2021A1515011313 to Ming Lu).

Footnote

Reporting Checklist: The authors have completed the STROBE and AME Case Series reporting checklists. Available at https://atm.amegroups.com/article/view/10.21037/atm-22-4661/rc

Data Sharing Statement: Available at https://atm.amegroups.com/article/view/10.21037/atm-22-4661/dss

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://atm.amegroups.com/article/view/10.21037/atm-22-4661/coif). ML reports that this work was supported by the Natural Science Foundation of Guangdong Province (No. 2021A1515011313). HL reports that this work was supported by the Research and Development Projects in Key Areas of Guangdong Province (No. 2019B020201015). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics committee of The Third Affiliated Hospital of Southern Medical University (No. 2022-008). Informed consent was taken from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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(English Language Editor: D. Fitzgerald)