|Year : 2021 | Volume
| Issue : 1 | Page : 52-64
Traumatic lumbar spondylolisthesis: current concepts and a literature review
Kamran Farooque, Santanu Kar
JPNATC, APEX Trauma Centre, AIIMS, New Delhi, India
|Date of Submission||29-Aug-2020|
|Date of Decision||20-Nov-2020|
|Date of Acceptance||17-Dec-2020|
|Date of Web Publication||28-Jan-2021|
JPNATC, Apex Trauma Centre, AIIMS, E 49, East Ansari Nagar, New Delhi.
Source of Support: None, Conflict of Interest: None
The aim of the study was to review published literature on traumatic lumbar spondylolisthesis. Traumatic spondylolisthesis of the lumbosacral region is a relatively rare but serious spinal injury necessitating careful clinico-radiological evaluation and management for a successful outcome. Limited literature is available to date to guide clinicians to treat the injury comprehensively. This article analyses the published literature and promulgates an evidence-based management plan for this injury. PubMed, Cochrane, Scopus, Google Scholar databases were searched using the keywords “traumatic lumbar” AND “spondylolisthesis” following PRISMA guidelines. In total, 118 relevant articles were considered for full-text review; among them, 68 articles were finally selected for the analysis. In each article, the pathomechanism; clinical and radiological features; classifications; indications for nonoperative and operative management; operative approaches, techniques, and rehabilitation; and long-term outcomes were analyzed. Traumatic lumbar spondylolisthesis is high-energy spine trauma requiring thorough evaluation. Radiographs are the initial investigation technique used in the emergency department, computed tomography scans define the bony details of the injury, and magnetic resonance imaging is important for deciding the treatment protocol depending on the disc injury. Decompression and instrumented fusion are the standard treatment protocol. A satisfactory outcome is to be expected in the majority of cases.
Keywords: Classification, perative treatment of lumbar spondylolisthesis, traumatic lumbar spondylolisthesis, umbar fracture dislocation
|How to cite this article:|
Farooque K, Kar S. Traumatic lumbar spondylolisthesis: current concepts and a literature review. Indian Spine J 2021;4:52-64
| Introduction|| |
Traumatic spondylolisthesis of the lumbosacral region is not a common spine injury. Sir Watson Jones first described this clinical entity in 1940. Injury which is significant enough to disrupt the posterior elements of the spinal column may lead to slippage of one vertebra over another. There is a paucity of literature on traumatic spondylolisthesis. Most of the published literature are case reports.
The aim of this article was to review the published literature and provide a comprehensive understanding of pathomechanism, clinical evaluation, radiological evaluation, management strategy, and prognosis of traumatic spondylolisthesis.
| Materials and Methods|| |
We searched the PubMed, Cochrane, Scopus, Google Scholar databases using the keywords “traumatic lumbar” AND “spondylolisthesis” following PRISMA guidelines. Primary search revealed 1132 articles. After removing the duplicates, 1010 articles were taken for consideration for abstract review. One hundred and eighteen relevant articles were considered for full-text review; among them, 68 articles were finally selected [Figure 1]. Articles mentioning adequate description of the mechanism of injury, preoperative neurological status, radiological investigations, type and approach of the surgical procedure used, and outcome were included for this review. Articles describing nontraumatic spondylolisthesis, chronic spondylolisthesis, spondyloptosis, cervical spondylolisthesis were excluded.
The following parameters were taken into consideration for the analysis of each article:
- The mechanism of traumatic lumbar spondylolisthesis
- Clinical and radiological features that characterize the traumatic lumbar spondylolisthesis
- Treatment strategies—nonoperative vs. operative
- Types of operative treatment and outcome
| Pathomechanism|| |
Watson-Jones suggested that the mechanism for traumatic anterolisthesis involves hyperextension. Roaf proposed that hyperflexion, axial rotation, and compression forces (vertical loading) were responsible for anterior traumatic lumbosacral dislocation and hyperflexion force alone is not sufficient to cause listhesis. Deniz et al. in a description of a case of L4-L5 anterolisthesis concluded that a combination of hyperextension and axial-loading forces are responsible for traumatic spondylolisthesis associated with a laminar fracture but hyperflexion is the causative factor in most of the cases with intact lamina. It is postulated that hyperflexion with various degrees of distraction along with shear forces is the most frequent mechanism of lumbar facet dislocation.,, A classic prototype of hyperflexion injury is the seat belt injury without chest strapping in a motor vehicle accident. However, some authors suggest that anterior L5-S1 spondylolisthesis is caused by a combination of hyperflexion with compression.,,, A few investigators report that anterolisthesis is purely a result of the direct trauma vectors., However, there is no biomechanical study to date to validate the exact mechanism of injury in traumatic spondylolisthesis and there is controversy regarding the causation of such injuries.,,, Future biomechanical studies may help to elucidate this complex injury mechanism.
A retrolisthesis results from a combination of shear forces in the posterior to anterior direction and hyperextension, and there is posterior slippage of vertebra on a relatively fixed pelvis. Bony injury is minimal in this injury as bony elements move away from one another, hence compress the neural structures leading to a higher incidence of neurologic loss. De Oliveira analyzed the mechanism of injury in the cases of traumatic retrolisthesis involving the thoracolumbar spine, and concluded that direct anterior shearing forces at the posterior midline of lumbar vertebra caused the anterior displacement of caudal lumbar segment, while the upper thoracic spinal segment underwent secondary hyperextension because of relative inertia leading to posterior displacement.
In summary, high-energy forces cause hyperflexion, hyperextension, lateral translation, distraction, and rotational injuries, as well as combination of such forces, which may ultimately result in bony and ligamentous failure leading to traumatic spondylolisthesis.,,,
The most common site of traumatic spondylolisthesis is L5-S1.,, Lumbosacral junction is an anatomic transitional zone. There is a change in facet joint orientation from sagitally oriented lumbar facets to coronally oriented L5–S1 facet joint. The presence of sacral slope also contributes to the high incidence of traumatic listhesis at this level.,, From an anatomic perspective, coronally oriented L5-S1 facet joints lead to antero- or retrolisthesis whereas at other thoracolumbar segments failure of sagitally oriented facet joints leads to lateral listhesis. The iliolumbar ligament complex also has a significant role in stabilizing the lumbosacral junction. Dividing the posterior band of iliolumbar ligament increases the flexion arc of lumbosacral junction by 77%. Hence, the anatomic failure of L5 transverse process leading to iliolumbar ligament disruption may be responsible for traumatic listhesis.
| Clinical Evaluation|| |
Patients presenting in the emergency department with thoracolumbar trauma should be clinically evaluated and life-threatening injuries take precedence in management.
Usually, the high-energy trauma causes serious injury to other organ systems which distract the clinician’s attention from spine injury. Abdominal, pelvic, thoracic, and head injuries have been reported in the literature. Step deformity at the lower lumbar spine although described in literature is very difficult to palpate clinically, in the setting of severe low back pain and multiple injuries. As the spinal canal is capacious relative to neural elements at the lumbosacral level, complete neurological deficit is rare in these injuries., In case traumatic spondylolisthesis is suspected, a thorough neurological examination is mandatory to rule out cauda equina syndrome, which is a surgical emergency.,
Anterolisthesis is the most common type of traumatic spondylolisthesis described in the literature. These injuries often have bony fractures of the posterior elements leading to self-decompression and pseudo-widening of the spinal canal, thus creating the room necessary for the neural elements, hence mitigating neural injury.
Traumatic retrolisthesis is relatively rare with less than 10 cases reported to date. Association of retrolisthesis with neurologic injury is higher, as the bony spinal canal is often left intact, causing impingement of neural elements due to translation., Retrolisthesis is also more likely to occur in the setting of more severe traumatic disruption and therefore leads to more neurologic compression.
Another type of traumatic listhesis, which is extremely rare, is lateral displacement of vertebral body, with only five cases described in literature.,,,
There is a wide variation in reported rates of neurological injury in literature. Aihara et al. reported a 68.4% rate of neurologic deficit in 57 cases, whereas only 3 out of 11 patients (27.3%) reported in the series by Vialle et al. had a neurological injury. Grivas reported 58% cases with a neurologic deficit for all lumbosacral fracture dislocations, while Arandi et al. found 89% cases of neurological injury in complete lumbosacral dislocations. Unilateral facetal dislocations are unlikely to cause neurologic compromise., On the contrary, bilateral dislocations, especially those associated with a significant degree of spondylolisthesis, can produce neurologic deficit. The most commonly affected nerve root is S1 and, even with the reduction of the dislocation, only partial recovery of nerve function is anticipated.
| Radiological Evaluation|| |
Careful assessment and stabilization of the patient in the emergency department is a priority in traumatic spine injury. Anteroposterior (AP) [Figure 2] and lateral radiograph [Figure 3] of the lumbosacral spine are obtained in the emergency department. Transverse process fracture [Figure 2], reported in 50–80% of the cases in some series, is recognized as a “sentinel sign” of traumatic listhesis.,, Transverse process fracture can be explained by the violent contraction of psoas major muscle due to differential acceleration–deceleration movement of the spinal column. Increased interspinous distance, a sharp kyphosis at L5-S1, and narrow anterior disc space height are suggestive of spondylopelvic dissociation in lateral X-ray view and in AP view, obliquity of L5 on the sacrum is another reliable sign. Other features suggestive of listhesis in AP radiographs are increased spine radiodensity [Figure 2] due to superimposed vertebral bodies, subtle focal angulation of AP spinal alignment and absence of psoas shadow due to retroperitoneal hemorrhage. However, bowel shadow may obscure these findings and diagnosis can be overlooked.
|Figure 2: AP view of L-S spine suggestive of transverse process fracture of L5—“sentinel sign” (red arrow). Increased radiodensity of vertebral body (yellow arrow) and obliquity of L5 over sacrum are other reliable signs.|
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|Figure 3: Lateral view of L-S spine suggestive of traumatic listhesis and grade of listhesis can be determined reliably in this view.|
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Pure lateral displacement of vertebral body is very difficult to diagnose only with radiographs. Lateral view of the spinal column which is usually performed in an emergency setting often shows normal alignment in this type of displacement. AP view shows subtle malalignment of lumbar and sacral spinous processes in this type of listhesis. Hence, relying only on radiographs may lead to error in diagnosis of this potentially unstable clinical entity.
CT scan is the imaging modality of choice to diagnose a traumatic spondylolisthesis. In unconscious patients, whole-body CT is done to look for other organ system injuries as well as the lumbosacral spine. CT may reveal the “Empty FacetSign” and empty or perched facets on axial cuts., CT with sagittal reconstruction provides excellent visualization of bony structures [Figure 4] and [Figure 5] and allows for measurement of the spinal canal diameter. However, as CT scan is performed in the supine position, the degree of anterolisthesis of the L5 vertebra may be underestimated.
|Figure 4: CT scan defines fracture morphology and associated fractures of posterior elements and endplates (black arrow indicates inferior endplate fracture).|
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MRI is an adjunct to CT for critical evaluation of surrounding soft tissue injury, particularly disc disruptions, and compromise of neural foramina by bony or disc fragments [Figure 6]. Posterior ligament complex (PLC) integrity and neural compression by hematoma or injury are to be critically evaluated with MRI. However, if cauda equine syndrome is suspected clinically, urgent surgical decompression should be performed without waiting for MRI.,,,
|Figure 6: MRI indicating disc disruption (red arrow) in traumatic listhesis. Disc height is markedly diminished at the L5-S1 level|
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CT myelography, although rarely done nowadays, has its role if MRI is contraindicated. It can detect pseudomeningocele as well as nerve root impingement in case fresh neurological deficit appears after reduction.
| Classification|| |
There are several classification systems described in the literature.
Aihara et al. suggested a classification system to clarify the principles of pathology based on involvement of facets, vertebral body, and posterior element with severity of injury increasing from type 1 to type 5 and suggested management according to this classification [Figure 7].
|Figure 7: Classification of traumatic spondylolisthesis by Aihara et al.|
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- Type 1: unilateral lumbosacral facet-dislocation with or without facet fracture
- Type 2: bilateral lumbosacral facet-dislocation with or without facet fracture
- Type 3: unilateral lumbosacral facet-dislocation and contralateral lumbosacral facet fracture
- Type 4: dislocation of the body of L5 with bilateral fracture of the pars interarticularis
- Type 5: dislocation of the body of L5 with fracture of the body and/or pedicle, with or without injury of the lamina and/or facet
Vialle et al. proposed a classification system based on the mechanism of injury [Figure 8]
|Figure 8: Classification of traumatic spondylolisthesis by Veer et al.|
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- Type I: pure dislocation of the articular facets without fracture
- IA: unilateral rotary dislocation secondary to rotational traumatic forces
- IB: bilateral facet joint dislocation with lateral displacement due to hyperflexion associated with a lateral translational force. In this type of injury, severe disc lesions may be found.
- IC: bilateral dislocation with anterior slippage of the L5 vertebra. The mechanism involves flexion-distraction forces.
- Type II: unilateral articular process fracture dislocation. The mechanism is similar to Type IA with higher energy forces producing a fracture of one of the joint facets and a dislocation without fracture on the opposite side. Anterior slippage of L5 is often asymmetrical with associated disc disruption.
- Type III: bilateral fracture dislocation with anterior displacement and disc injury.
- IIIA: bilateral fracture with anterior displacement of L5 caused mainly by a flexion-distraction mechanism.
- IIIB: bilateral fracture with rotational displacement associated with anterior slippage of the L5 vertebra. A combination of high-energy forces that includes flexion-extension and lateral or rotational forces is postulated.
Dimar Jr II classified traumatic spondylolisthesis according to the anatomical site of vertebra involvement [Figure 9]
- Type 1: Facet dislocations
- Type 2: Facet fractures
- Type 3: Pars fractures
- Type 4: Fusion mass fractures
- Type 5: Pedicle fractures
- Type 6: Complex fractures with vertebral body involvement.
- Type 1, 2, 3 low grade and 4, 5, 6 are high grade listhesis.
Comparative assessment of various classification systems is tabulated in [Table 1].
|Table 1: Comparison between various classification systems of traumatic spondylolisthesis|
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| Treatment|| |
There is hardly any role of nonoperative treatment in management of traumatic spondylolisthesis. Few investigators, have reported good results with conservative treatment and acceptance of deformity. Beguiristain et al. published a case of pure traumatic anterior L5-S1 dislocation in a 5-year-old boy managed conservatively with traction, immobilized for 3 months in hyperextension in a lumbar plaster jacket, and obtained excellent outcome 8 years post-injury, even though the dislocation was only partially reduced. He also concluded that due to greater elasticity of the spinal column, even with neuro deficit, children can be managed conservatively with closed reduction. Boger et al., in a case of spontaneously reduced unilateral facetal dislocation, obtained a satisfactory outcome initially with conservative management but the patient experienced chronic low back pain and kyphotic deformity.
However, with conservative treatment, fracture stability depends on fibrous healing alone. Considering the high velocity of injury, there is a risk of slow progression of initial displacement from stretching of scar tissue with consequent deformity progression, appearance of new neurologic deficits, and secondary degenerative changes. Few authors initially opted for nonoperative management, but eventually surgical intervention was undertaken due to the progression of the deformity and secondary neurological deficit.,,, Dewey and Browne attempted manipulation in traction and flexion that resulted in worsening neurologic deficit. Das and McCreath, after analyzing operative findings of four cases, concluded that indirect forces alone cannot achieve a reduction in this type of injury. Conservative management after closed reduction may be adopted in very young children with a satisfactory result.
The Standard of Care for traumatic spondylolisthesis is surgery. The fundamental goals of surgery should be wide decompression of spinal nerve roots, clearance of offending bony fragment or disc material from the spinal canal, reduction of listhetic deformity, and stabilization of the spinal column with instrumentation with or without fusion., There is little controversy in literature regarding the need for early surgery. Delay in surgery may lead to difficulty in obtaining an adequate reduction.,, Fabris et al. pointed out that with proper reduction technique, it is possible to obtain a reduction in the majority of cases. Decompression of nerve roots and reduction of deformity are one of the crucial intraoperative steps of traumatic spondylolisthesis surgery. Laminectomy is done to identify damage to nerve roots or dural sac. Any injured disc which adversely affects reduction is removed. Reduction maneuvers are employed only after wide decompression of the neural elements to minimize the neural injury. The operating table can be used to induce hyperflexion of the spine, which may aid in facetal reduction. The reduction should be achieved with least possible progressive distraction, and partial facetectomy, if required, to minimize the distractive forces. Application of distractive force should be kept to a minimum to avoid potentially dangerous neurologic damage. The use of reduction screws can make the reduction easier. As laminectomy and, if required, facetectomy performed render the posterior column unstable, posterior instrumentation with posterolateral fusion is performed routinely. Adequate visualization of thecal sac and nerve roots by exploration of the canal before and after the reduction is essential to rule out possible compression on neural elements by inadvertent extrusion of the disc material.,, Anterior interbody fusion is added if there is concomitant disc disruption that renders the anterior column unstable, so that the patient can be mobilized immediately post-surgery.
[Table 2] summarizes the articles depicting the post-surgical outcome of posterior instrumentation with posterior fusion. [Table 3] summarizes the articles depicting the post-surgical outcome of anterior interbody fusion with posterior instrumentation (with or without posterior fusion).
|Table 2: Summary of few articles with outcome of posterior instrumentation and posterior spinal fusion|
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|Table 3: Summary of few articles with outcome of posterior instrumentation and interbody fusion|
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There is no standard protocol in literature that defines the levels of instrumentation recommended in traumatic listhesis. Most investigators have performed a short segment instrumentation. A short segment construct may be sufficient in patients with good facet apposition following reduction, but fixation may need to be extended proximally to L4 or distally to the pelvis when bony support is insufficient following reduction. Considering the high energy mechanism of this injury and frequently associated fractures of the posterior elements, it is not prudent to perform a short segment fixation, and, in such cases, it is safer to extend fixation levels. Extensive disruption of L5-S1 articulation may necessitate auxiliary ilio-sacral or pelvic fixation combined with anterior reconstruction and posterior instrumentation [Figure 10].,,, Fixation should be based on the pattern of the instability as well as pedicle integrity and surgeon’s preference. Spinal cord monitoring can be used to confirm intact peripheral nerve function during reduction maneuvers and significant distraction should be avoided during reduction.
|Figure 10: Postoperative X-ray demonstrating spinopelvic fixation and anterior interbody fusion.|
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Historical techniques for instrumentation have included a wide range of constructs, including interspinous screws, posterior articular screws, sublaminar wiring, Harrington hooks and rods, and osteosynthesis with posterior plates or with Cotrel–Dubousset-type instrumentation.,,, There are drawbacks in using interspinous wiring,, or Harrington rods for instrumentation in traumatic listhesis. Interspinous wiring techniques need a long period for fusion. Fusion is unnecessarily extended to adjacent normal levels if Harrington system is used. Hence, pedicle screw fixation has become the standard technique of instrumentation providing a solid and shorter fused area.
There are reported cases of implant failure after isolated posterior fusion,. The current literature also suggests high probability of failure to obtain fusion in nonoperatively treated cases as well as cases of non-instrumented surgical fusion.,
The choices for surgical intervention include posterior spinal instrumentation and posterior spinal fusion (PSF) with the addition of an interbody fusion (PSF+ IB), in patients with incompetent intervertebral disc. Traumatic listhesisis is a three-column injury and anterior column reconstruction is necessary for optimal stability. Intervertebral disc assessment is mandated in every case of traumatic listhesis, as severe intervertebral disc injury requiring interbody fusion may be found, even in the absence of significant listhesis.
It is well accepted in literature that if intervertebral disc injury is present, anterior column reconstruction with placement of interbody fusion graft, or cage supplemented with posterior instrumentation and posterior fusion, should be done..,,,,, If the intervertebral disc is intact on MRI, a posterolateral fusion with pedicle screw fixation is usually sufficient.,, There are definite advantages of combined anteroposterior fusion, like immediate post-operative mobilization of the patient, obtaining greater stability, and less chance of pseudoarthrosis.,, In a systematic analysis of 77 articles including 125 patients, Ver et al. demonstrated that there is no significant difference in fusion rate, ambulation, pain, and neurologic deficits between isolated posterior spinal fusion group and interbody supplemented fusion group if intervertebral disc injury is not present. They also noted that adverse outcomes were more likely in higher grade listhesis (pedicle fracture, and complex fracture) according to their classification.
Interbody fusion allows a higher degree of stability and fusion rate. The anterior support reduces the risk of implant failure. Lim et al. concluded that isolated interbody fusion is superior to posterolateral fusion in terms of achieving union, maintaining reduction of listhesis, providing a larger surface area for bone graft incorporation, preventing union as well as improving symptoms of back pain.
El Assuity et al. concluded that when both the lamina and transverse process are fractured, indicating an unstable situation, relying on only posterolateral fusion is not favorable. Vialle et al. suggested that if the amount of posterior bone resection is significant (to obtain a reduction or to decompress the neural elements), an interbody fusion should be added to posterolateral fusion, even if the disc is not injured.
The choice between posterior-only approach and combined anterior–posterior approach for surgical management is controversial. Analysis of individual articles reflects that majority of the cases described in the literature are approached posteriorly with only a few cases being treated using a combined anterior and posterior approach.,,,, Aihara et al., in their proposed classification system, suggested that acute spondylolytic spondylolisthesis (type 4 listhesis in their classification) is inherently unstable due to disruption of anterior and/or posterior ligamentous structures and needs to be treated with a combined anterior and posterior approach. Tang opined that interbody fusion can be achieved through the posterior-only approach, with a similar clinical outcome. Stuart et al. also concluded that interbody fusion does not have a different functional outcome when achieved through a posterior-only approach rather than a combined anterior and posterior approach.
There is no conclusive literature to date to guide the surgeons to adopt an optimal approach.
Literature analysis revealed that only two cases were treated using an isolated anterior approach. Edvardsen treated one case with an isolated anterior approach due to unfavorable posterior skin condition, and the other case of isolated anterior approach was reported by Grabe. In both these cases, an in situ fusion without reduction was done. Hence, in the absence of a compelling anatomic reason, an anterior-only approach is not conducive to obtain adequate reduction and satisfactory outcome and should not be undertaken.
In the past, anticipating the unstable nature of the injury, 6 weeks of bed rest was practiced postoperatively by some surgeons. Three-column fixation with pedicle screws confers enhanced biomechanical strength, and bed rest for prolonged periods post-surgery is not currently practiced. Postoperatively, the use of brace was a routine in the past but few studies opine that internal fixation obviates the need for bulky orthoses in the postoperative period. Brace confers additional protection and aids with rehabilitation. Duration of bracing varied from 6 weeks to 3 months, to cover the consolidation period of the fusion mass.
Return to function was achieved in most of the cases described in the literature. Full weight bearing can be allowed after 3 months. Patients without or minimal neurologic deficits returned to preinjury activity level after 4 months to 1 year depending on the severity of their injury.,,,, Most of the cases described in literature report satisfactory results in short-term follow-up. There are a dearth of studies with a sufficient number of cases reporting on long-term follow-up after traumatic listhesis.
Adelved et al. in a retrospective study of 13 patients of traumatic listhesis found that functional impairments, pain, and poor patient-reported health were common, along with high rates of neurologic, urinary, and sexual dysfunction.
Long-term prognosis is unclear due to the small number of reported cases with limited follow-up and heterogeneous results.
| Conclusion|| |
Traumatic spondylolisthesis is a rare clinical entity. High index of suspicion is required for diagnosis. Associated injuries of other organ system are a common finding. CT scan is a valuable adjunct to radiographs for assessment of the bony injury. Intervertebral disc assessment is mandated in all cases and is best done with MRI. Nonoperative management does not have a significant role except in very young children. Traumatic listhesis presenting as a cauda equina syndrome should be decompressed on an emergent basis. Operative intervention with decompression, reduction, and posterior instrumented fusion is the standard treatment. An interbody fusion is added in cases with intervertebral disc injury. However, posterolateral fusion and instrumentation may be adopted for cases where intervertebral disc integrity is not compromised. Pedicle screw instrumentation is the standard of care and the level of instrumentation should be determined on a case-by-case basis. Additional illio-sacral or pelvic fixation should be considered in cases with high-grade listhesis. Preoperative neurological status is a significant determinant of postoperative outcome. Spinal column stability and return of function should be expected in the majority of cases with partial cord injury.
We have described the current concepts in the management of traumatic spondylolisthesis based on available literature. We observed that most of the articles report a retrospective analysis of patient outcomes in a small heterogenous group of patients. Significant bias may be associated with such studies. A prospective long-term study with a large homogeneous population may bring forth future recommendations. This review can guide the spine surgeons to approach traumatic spondylolisthesis comprehensively based on the current level of knowledge and evidence.
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Conflicts of interest
The authors declare no conflict of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
[Table 1], [Table 2], [Table 3]