Evolution of surgical techniques in the management of vertebral body tumours and the current status
Primary vertebral body tumours constitute only about 5% of skeletal tumours. Their morbidity is high due to instability and neurological deficits related to the spine. The complex anatomy further highlights the expertise needed in their management. A multidisciplinary management has heralded tremendous improvements in the treatment of primary vertebral body tumours. From incomplete resection with a high recurrence of these tumours in the early 20th century, to the present day complete en-bloc excision of the tumours, guided by the well-established staging and classification systems, have been the significant changes brought about in the long course of treatment of these complex tumours. The overall results are better with radical excision in combination with adjuvant therapies. Complex and previously unimaginable surgical techniques are accomplished easily with a multi-disciplinary approach and with newer spinal instrumentation. Understanding of the evolution of surgical techniques and the prevalent classifications are essential in the surgical management of vertebral body tumours.
Keywords: Vertebral body tumour, Enneking staging, Weinstein-Boriani-Biagini classification, vertebrectomy, stabilisation
Primary bony vertebral tumours are uncommon entities representing less than 5% of all primary bone tumours., Due to their rare occurrence, the experience of most surgeons in dealing with this entity is limited. Thus, the expertise and available literature emanates from a few centres that are equipped with a multidisciplinary team with experience in the management of vertebral body tumours. Surgery still remains the cornerstone of treatment of both benign and malignant tumours of the spine. Until a few decades ago, the treatment of spinal tumours was riddled with recurrence, morbidity, and poor surgical outcomes. The reason for this has been multi-fold. Firstly, the evidence was poor due to both a low incidence of these tumours, as well as the principles of surgery being extrapolated from the experience gained from appendicular bony tumours which did not take into account the associated instability produced by spinal tumours. Secondly, the imaging was still evolving and so was the surgical expertise. Thirdly, the reconstructive armamentarium available was still in its infancy. Constantin Arseni, in his seminal paper mentioned that during the period form 1935 to 1957, the surgical outcome was good for benign rather than malignant tumours. During this period, radiation therapy was added as a treatment modality. Radiculotomy was strongly recommended to alleviate the patient's suffering. Sometimes, a cordotomy was also performed. It was found that the radiation therapy following surgery was more beneficial in case of an angioma, with a few cases being considered cured. For the management of pain, subarachnoid alcoholization of posterior spinal nerve roots was advocated by Dogliotti (1931), Horrax (1966) and White (1938).
In the 1970s, Stener first applied the oncologic criteria in resecting spinal tumours and performed en bloc resections, as they were already being performed for tumours of the gastrointestinal tract. Later, Roy-Camille popularised the technique of en bloc resection in the thoracic spine by the posterior approach, and in the lumbar spine by a combined posterior and anterior approach.,,, After that, Tomita proposed a similar technique for en bloc removal of spinal tumours. The concept of excision of the tumour with safe margins was first applied to bone tumours by Enneking, and more specifically to the spine by Campanacci and Talac., A review of the recent literature has revealed that technically demanding surgical procedures may performed for resection of tumours of the cervical or cervico-thoracic spine, with achievement of tumour-free margins.
The primary tumours of the spine are classified as benign or malignant tumours. The most common primary benign tumour of the spine is a hemangioma that is usually asymptomatic. The other common symptomatic benign tumours are osteoid osteoma, osteochondroma and chondroblastoma, among several other tumours [Table 1]. Benign tumours arise either from the anterior or the posterior elements of the spine, as depicted in [Figure 1] and [Figure 2]. The most common malignant bone tumour is of hematopoietic origin (a myeloma). The other common malignant tumours are chondrosarcoma, Ewing's sarcoma, chordoma, etc. [Table 2].
Primary tumours of the spine often present incidentally following a workup for non-specific axial skeletal pain. These primary tumours are usually localised to a single location and offer the potential for true cure. However, this possibility may be eliminated by their late recognition or an improper workup. This is because these tumours often present late, as the symptoms are usually due to periosteal stretching as a result of excessive growth of the tumour and the localised bony destruction. About 80-85% of patients present with unremitting pain that worsens at night or in the supine position. The age of presentation gives a clue in deciding the type of tumour. To quote an example, Ewing's tumour presents in childhood while a myeloma present in the older population [Figure 3]. In young patients, a new or progressive deformity may be the presenting feature. A neurological presentation is seen in less than 14% of patients and is commonly seen with thoracic involvement of the tumour. Bowel and bladder disturbances are seen as the presenting complaint in 2-3% of large tumours of the sacrum.
Plain radiographs should be the preliminary investigation of choice, followed by magnetic resonance imaging (MRI) with contrast enhanced images. The latter is excellent at delineating soft tissues, paraspinal lesions, neural encroachment, bone marrow infiltration, and epidural extension. The computed tomographic (CT) scan provides superior information on the status of the cortical bone and the tumour calcification.
Primary malignant lesions, such as sarcomas, are known to metastasise, which will significantly alter the surgical plan from aggressive surgery (that may carry the risk of at least a temporary functional loss), to a less aggressive debulking of tumour (with a meticulous preservation of function), or to a state of completely forgoing resection (the latter choice prevails if the patient is in a very poor neurological status or has multiple metastases with a life expectancy of less than 2 months). If radiological investigations are suggestive of such aggressive tumours, it is imperative to confirm, both radiologically and histologically, the presence of metastatic foci. The 18F-fluorodeoxy glucose- positron emission tomography ([18F] FDG-PET) is an excellent option in such cases. In addition, a CT scan of the chest, abdomen, and pelvis, as well as a bone scan, are other appropriate options. In the case of suspected plasmacytoma or multiple myeloma, a skeletal survey, a bone marrow biopsy, and serum immuno-electrophoresis are useful investigations. Approximately 50% of patients with a solitary plasmacytoma are known to develop multiple myeloma at a follow up of 2 years. In the presence of widespread diseases such as lymphoma or multiple myeloma, that have also infiltrated into the bone marrow, osteoporosis with the propensity to precipitate vertebral fractures may also occur. In this situation, a bone mineral density test may also be an extremely useful investigation.
Tumour board – A multidisciplinary approach to primary spine tumours
Considering the complexity of management of the primary spinal tumours, centres which treat primary spinal tumours have evolved the concept of a “Tumour Board” encompassing specialists from multiple interrelated departments. This concept has significantly changed the way the treatment is administered and has also helped in improving the prognosis. The multidisciplinary team usually includes the spinal surgeon, the oncologist, the radiation therapist, the radiologist (including the interventional radiologist), and the rehabilitation specialists. It is mandatory to take every members' opinion before considering any treatment strategy for these complex tumours. We follow this treatment algorithm in our oncologic centre for the management of primary spinal tumours [Figure 3].
A biopsy is mandatory in any primary spinal tumour when the radiological and biochemical markers are not conclusive. The results of the biopsy will dictate the treatment paradigm and should be discussed in the tumour board before including the patient in a treatment protocol. Four main types of biopsy techniques may be attempted in these patients. They include the fine needle aspirate biopsy (FNAB), core needle biopsy, incisional biopsy and excisional biopsy.
A CT-guided FNAB is the most common procedure performed, yielding a tissue diagnosis in 90% to 98% of the procedures. A core needle biopsy permits the obtaining of a column of tissue and should be considered if the FNAB is non-diagnostic, although a higher likelihood of tumour spillage may exist. The chances of tumour disruption and local spread are high in the case of both incisional and excisional biopsies; thus, a FNAB is recommended if the lesion is likely to harbour a malignant histology. To reduce the likelihood of tumour spread, sealing the biopsy site with bone wax, and/or injecting a colour dye to delineate the trajectory to be undertaken during the definitive surgery, are recommended. Inclusion of the biopsy tract in the operative incision is of paramount importance in such cases. Thus, it is beneficial for the spinal surgeon to discuss the likely surgical trajectory with the interventional radiologist in the tumour board meeting prior to the conduction of biopsy. An excisional biopsy may be appropriate for both the diagnosis and treatment of benign tumours.
A work-up to define instability of the spine
The Spine Oncology Study Group has come out with a new scoring system [Table 3] in 2010 to assess the spinal instability in spinal tumours, including the metastatic ones. It is based on six variables. These include the location of the lesion, the characterisation of pain, the type of bony lesion, the radiographic spinal alignment, the degree of vertebral body destruction, and the involvement of postero-lateral spinal elements. Each variable is given a score. The score assigned to each of the variables is summed up for calculating a final score, which determines the extent of spinal stability. The total score ranges from a minimum score of 0 to a maximum score of 18. A stable spine has a score that ranges between 0 to 6, a spine of indeterminate or doubtful stability is assigned a score that ranges between 7 to 12, and, the presence of a definite instability is assigned a score that ranges between 13-18. Surgical stabilisation is recommended in the cases where the total score is greater than 7.
The Weinstein-Boriani-Biagini (WBB) system was designed to plan surgery along with the the other staging systems. For staging the tumour based upon the WBB staging system, a preoperative MRI scan and a CT scan are required to provide the details of tumour extension and the relationship of the normal tissues in the vicinity of the tumour. As the goal of surgery is to obtain a tumour-free margin, the surgical planning should include in the resected specimen, at least one sector, and one layer outside the tumour border [Figure 4]. The WBB staging system focuses on the extent and location of the tumour. In the transverse plane, the vertebra is divided into 12 radiating zones (numbered 1 to 12 in a clock-wise order) and into five layers from the prevertebral to the dural involvement (A through E). The longitudinal extent of the tumour is recorded by identifying the specific vertebrae involved. This system has permitted a more rational approach to surgical planning, provided that all efforts are made to perform surgery along the required margins. Extension into the zone D can preclude one from obtaining a negative tumour margin unless a layer of healthy tissue exists between the tumour and the dura. It is not always possible to know this fact until the time that the actual surgical exposure has been performed. A close attention should be paid to the zone A extension. The anterior approach should be directed toward the side with maximum zone A involvement to permit the best visualisation of the vertebral body during tumour excision. In addition to these manoeuvres, one must pay a close attention to the cephalo-caudal extent of the tumour. This will help to determine whether or not the transverse cuts should be made through a disc or vertebral body. If a foramen is involved, then the nerve root in that foramen needs to be taken with the tumour to obtain a tumour -free margin. It may be necessary to remove a nerve root to facilitate tumour exposure even on the side of the vertebra where the tumour is not present. This procedure is easily accepted by the patient as it is associated with a low morbidity (in the form of hypoaesthesia) in the thoracic spine.
According to the WBB planning system [Figure 4], four general types of en-bloc resection in the thoracic and lumbar spine can be identified: anterior, posterior, anterior followed by posterior, and posterior followed by simultaneous anterior and posterior. A tumour that is localized to zone 4-8 or zone 5-9 has at least one pedicle intact. Therefore, excision of the posterior elements with cauterization of the epidural venous plexus, internal fixation, resection and reconstruction at anterior or posterior vertebral body may be carried out. A tumour invading the zone 3-5 or the zone 8-10 requires an axial resection; multiple vertebral invasion or rib invasion may also require resection. A tumour in zone 10-3 will require a posterior laminectomy, superior and inferior pedicle resection, and lateral dissection is performed to osteotomize and excise the lamina.
An en-bloc excision from a posterior-only approach is possible for vertebral body or eccentric tumours, but it provides an adequate oncologic margin only for tumours without extension into zone A. For all tumours that extend into zone A, the recommended plan is a staged posterior and anterior procedure, the anterior release being the first step. Staged approaches are safer and permit the achievement of the best oncologic margins.
By incorporating information about the pathology, general morphology, and metastatic status of a lesion, generalisations about growth and behaviour can be made in order to dictate the surgical approach using the Enneking classification  [Table 4]. In the Enneking staging, benign tumours are classified as latent, active and aggressive, while the malignant tumours are classified as low and high grade, with and without metastasis.
The preferred surgical approach to a lesion is dictated by the tumour pathology, morphology, and metastatic status. The two main surgical goals involve resecting the tumour and reconstructing the load-bearing capacity of the spine. Once the preferred method of resection has been determined, the patients must be surgically staged to determine the technical feasibility of the procedure. En-bloc resection is preferred in every tumour. However, the presence or absence of a surgical corridor to deliver the tumour in a single piece without disrupting vital structures, especially in presence of invasion into the nearby unresectable structures, has to be determined.
Types of surgical resection
Depending upon the biopsy results and the classification of tumours, 3 types of surgeries are recommended for the patients with primary spinal tumours:
En-bloc resections involve the removal of the tumour in one non-violated piece and it conveys a survival advantage.,,, En-bloc resection may require sacrifice of adjacent structures to remove the tumour in one piece, resulting in a planned resection that encompasses the risk of an acceptable degree of morbidity. Nerve roots, major vessels, and dura are commonly resected along with the tumour mass to remove the lesion in an en-bloc fashion. In addition, a planned tracheostomy, feeding tube placement, and an ileostomy or colostomy may be necessary, as and when the situation demands. The patient should be thoroughly counselled prior to surgery regarding the expected permanent loss of function. Thus, the decision to continue with en-bloc resection must be based on a trade-off between the expectation of increased survival brought about by the procedure and the surgical morbidity rates. In cervical lesions, en-bloc resections are difficult to achieve at the cranio-vertebral junction (CVJ) due to the difficulty in mobilisation of the vertebral arteries, as a result of their tortuosity, unpredictable dominance of one side, and significant atherosclerotic changes within them in the elderly patients, which might lead to their thrombosis on mobilisation. Even when en-bloc resection is done, instrumentation of the anterior segment of the CVJ is difficult to perform due to the problems that arise with reconstruction along the clivus. We had a case of C1-2 Langerhans cell histiocytosis with neurological involvement, associated with instability at the C1-2 level, which was dealt with by surgical stabilisation and adjuvant chemotherapy [Figure 5]. In the subaxial spine, the presence of the brachial plexus with varied innervations on either side, along with the need to perform vertebral artery mobilisation, pose a challenge. At the cervico-thoracic junction, in addition to encountering the brachial plexus, the additional presence of mediastinal and thoracic inlet structures need to be dealt with. In addition, in the subaxial cervical spine, an en-bloc excision is challenging because of the exiting innervation to the upper extremity and the diaphragm, the presence of bilateral vertebral arteries, as well as the trachea, and the oesophagus being in close proximity. Thoracic tumours, where the thoracic nerve roots may be sacrificed without much morbidity, are relatively less difficult to remove using en-bloc resections. We had a case of D6 chondrosarcoma where an en-bloc excision yielded a good long term result [Figure 6]. Similarly, in the lumbar region, the presence of obliquely traversing nerve roots along with their plexus, the bulky psoas muscles and the presence of the large, bifurcating aorta and vena cava pose a challenge in achieving an en-bloc resection. Both in the cervical and the lumbar regions, a combined antero-posterior approach must be adapted to achieve this goal. At the sacral level, a total en-bloc resection can be attempted without much difficulty when the lesion is below the S2 segment. At least one S2 root should be preserved to prevent sphincteric disturbances. When the lesion involves the S1 segment, a urinary and a bowel diversion technique has to be considered to achieve a en-bloc resection. A stand-alone posterior approach for achieving an en-bloc resection in the form of partial sacrectomy below the S1 level is possible, with much lesser morbidity [Figure 7]. The protocol of the en-bloc excision of primary spinal tumours is given in a step-by-step approach in a flow-chart [Figure 8].
The goal of reconstruction is to permit an adequate load transfer while protecting the nearby spinal cord, the remaining nerve roots, and other vital organs. It is worth noting that the patient may permanently rely on the implanted instrumentation to maintain stability, as bony union in the face of massive reconstruction and cytotoxic adjuvant therapy is often challenging to achieve. The anterior load-bearing constructs are more likely to achieve fusion than the posterior constructs. Whenever spinal stabilisation is carried out for palliative care, it can be effectively achieved with minimally invasive techniques. A fusion of up to 5 vertebral levels can be achieved in the present day scenario with the available instrumentation systems.
Radiotherapy can be used as an adjunct to surgery, at times as the sole treatment, or as a neo-adjuvant regimen to shrink the tumour prior to its complete resection. It is mostly used in malignancies that arise from the soft tissues (such as sarcomas) and from the hematopoietic cells (hematopoietic cancers). Various techniques of delivery of radiotherapy have been developed in the recent times. These include two-dimensional radiotherapy, three-dimensional conformal radiotherapy, intensity-modulated radiotherapy, stereotactic radiotherapy and particle beam radiotherapy (the proton beam therapy) techniques. These techniques have helped in preventing and delaying the local recurrence rate in patients with primary bone tumours. Lymphomas, Ewing's sarcomas, chordomas and osteosarcomas often respond well to both the conventional as well as the stereotactic forms of radiotherapy including the gamma knife, the cyber knife and the proton beam therapies.,, In case neurological deficits develop due to spinal canal compromise, or spinal instability causes severe pain, surgery may be considered. Even in the presence of a radiation responsive tumour, surgery may be done to decompress the spinal canal and restore stability of the spine. This is accomplished by performing a vertebral augmentation. Thus, a complete resection and reconstruction is often performed. A minimalistic procedure, such as establishing a reasonable margin between the tumour and the spinal cord (the “separation surgery”), may often have to be carried out to optimize the subsequent radiation treatment.
Moderately responsive tumours
In Ewing's sarcoma, which is also the most common primary spinal column tumour in children, surgical treatment is reserved for issues of stability and neurological compromise. Surgical treatment has not been shown to improve local control. The 5-year survival rate of less than 50% has been seen in certain subsets of patients.
Role of chemotherapy
Lymphoma, Langerhans cell histiocytosis, eosinophilic granuloma, plasmacytoma and multiple myeloma can be treated with chemotherapy alone, unless they are detected when their extensive dissemination has led to spinal instability. We had a patient with a D5 vertebra pathological collapse and an intact neurological status, where the biopsy showed the presence of histiocytosis. The patient was exclusively managed with vinblastine and prednisolone [Figure 9]. Neoadjuvant chemotherapies have significantly improved the prognosis in primary vertebral body tumours. Chemotherapy helps in downsizing of the lesion, and once the tumour shrinks, it helps in identifying the proper tumour border and in preserving adjacent structures (which might otherwise appear to be involved on the pre-chemotherapy images).
Giant cell tumours (GCTs), Ewing's tumours and sarcomas require preoperative neo-adjunctive chemotherapy for cytoreduction, in the cases when a doubtful residual tumour remains, or following an operative intervention as a continuum of therapy. A GCT is locally aggressive and can rarely metastasize. Its local recurrence is reported to occur in approximately 19–50% of cases and usually occurs within 2 years. Denosumab humanised monoclonal antibody to the receptor activator of nuclear factor kappa-B (RANK) ligand (RANKL), a key mediator of osteoclast activity, has been utilized both as a neo-adjuvant treatment option prior to surgery and also to prevent an increase in the size of the residual tumour., In addition to the benefit of reducing tumour volume, it also reduces blood loss from intralesional curettage, due to conversion of the neoplastic cells to a fibrous matrix with decreased angiogenesis. Definitive surgery, either in the form of en-bloc resection or curettage, should be done within 3-4 months of starting the medication, before the formation of the thickened sclerotic ring. Unlike zolandronic acid, denosumab does not influence cell viability and the expression of the RANKL/osteoprotegerin (OPG) gene, alkaline phosphatase levels, and collagen alpha 1-type I in GCT stromal cells, and hence, recurrence is bound to occur with the stoppage of the denosumab., On the contrary, zolandronic acid (a biphosphonate) induces a dose-dependent cell inhibition and apoptosis in GCT stromal cells; it also decreases the alkaline phosphatase activity in some GCT stromal cell lines.
Primary spinal tumours are fortunately rare. However, there is a significant improvement in its management protocol in the last two decades. A multi-disciplinary tumour board is mandatory in the present times to treat this complex entity. With the advent of newer imaging modalities (including the PET scan), and the availability of neo-adjuvant chemo-radiation therapies, most of these tumours can be removed en-bloc. Every attempt should be made to remove the tumour en-bloc as the procedures ensure either a cure or a prolonged recurrence-free interval. The improvements in the surgical and stabilisation procedures of the spine has resulted in a better prognosis for patients with primary vertebral body tumours.
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Conflicts of interest
There are no conflicts of interest.
[Additional file 1]
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
[Table 1], [Table 2], [Table 3], [Table 4]