Subaxial Cervical Spine Fractures: Historical Systems and Advancements With the AO Spine Classification

Abstract

Study Design

Systematic Review.

Objectives

A vast array of historical subaxial cervical spine fracture classifications. This initially comprised crude non-hierarchial schemes based upon mechanism on injury alone including compression, flexion, extension or lateral flexion. Allen and Ferguson advanced this by offering 6 categories of subaxial cervical spine injuries. Beyond this, Aebi and Nazarian appreciated the nuances of whether was was ligamentous injury in addition to pure bony involvement. These existing simplistic classifications failed to guide clinicians as to whether operative or non-operative management is appropriate. We describe the evolution of existing subaxial cervical spine classification systems and the development of the AO Cervical Spine Injury Classification System.

Methods

A systematic review of MEDLINE, EMBASE and Cochrane Databases was performed in keeping with the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) guidelines to identify all existing subaxial cervical spine classification systems.

Results

483 articles were initially retrieved which were distilled to 11 articles which pioneered individual classification systems. The AO Cervical Spine Injury Classification System resolves this with its hallmark 3 categories of escalating injury types from the type A compression injuries, to type B tension band injuries and finally the grossly unstable type C translation/displacement injuries. The addition of modifiers such as critical disc herniation or stiffening bony disease further strengthens the encompassing nature of this classification.

Conclusions

The AO Spine Cervical Spine Injury Classification System is a testament of the historical classification grading schemes but provides a structured means of evaluating injuries. This progressive system provides a foundation upon which objective scoring management methods can be developed to guide operative or non-operative management.

Keywords

subaxial cervical spine spinal fracture flexion extension biomechanics

Introduction

The cervical spine is a mobile dynamic region which simultaneously affords a wide range of motion whilst guarding the cervical spinal cord.¹ In particular, the subaxial cervical spine is reliant upon ligamentous support in order to maintain stability.² For this reason, a complex array of factors needs to be considered when evaluating the injuries of the subaxial cervical spine. This include inspection of the vertebral body itself with its neural arches, degree of bony retropulsion if present and injury to the posterior facet joints. Additionally, the integrity of the ligamentous structures including the anterior longitudinal ligament, posterior longitudinal ligament and posterior ligamentous complex need to be evaluated. Finally, the preservation of cervical lordosis and whether any loss or kyphosis is merely pre-existent or actually traumatic in the context of overall cervical spine alignment needs to be carefully considered.

The number of structures which require clinician evaluation and synthesis has led to numerous historical classifications each with a unique formulation of grading severity of injury. For example, some utilize the mechanism of injury as a means of classification which, whilst logical, fails to convey the severity of the injury.^3-5 There has yet to be a unified globally validated system which takes into account both the patient’s neurological status, the overall injury across the bony and ligamentous structures, as well as unique situations such as ossifying bony disease. As such, it is crucial such a system is developed given progression to a treatment algorithm is only possible with the fundamental accepted classification in place. Finally, potential future areas of classification development are discussed including the idea that cervicothoracic junctional fractures are perceived by surgeons as being more unstable and likely to require operative intervention.⁴

We describe the historical subaxial cervical spine classification systems and their individual benefits and flaws. The trend from classifications upon pure mechanism or vector of force to morphological classifications based upon increasing likelihood to demand operative fixation was evident in our review. The AO Spine Cervical Spine Injury Classification System is then introduced and the manner in which it integrates each of these existing systems is described. Finally, potential future areas of classification development are discussed, including the idea that cervicothoracic junctional fractures are perceived by surgeons as being more unstable.⁴

Methods

Search and Eligibility Criteria

The authors conducted a systematic electronic search of the Medline, EMBASE and Cochrane Database of Systematic Reviews from their date of inception to August 2024 was conducted in keeping with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Databases were queried with the proceeding terms combined with various Boolean operators: ‘subaxial cervical’, ‘injur*’, ‘classification’, ‘system’ and ‘fracture’. Only studies examining human subjects in the language English or with available English translations were included. No registered review protocol exists for this study.

Inclusion and Exclusion Criteria

Eligible abstracts checked by 2 authors (B.T.S.K and J.W.T), before appropriate articles for full-text examination were inspected. Bibliographies of included studies were also searched for further eligible articles. Discrepancies were examined until consensus attained. Inclusion criteria were defined as: 1. Any form of article, whether randomised or non-randomised controlled trials, cohort study, case series, case report or review article which proposed a new classification system defined as a method of grading fractures upon a rational basis with 2 or more categories 2. Any article which added a new category to an established classification system 3. Human Subjects.

Study Selection and Data Extraction

Extraction of data into a preformatted spreadsheet was performed independently by 1 author (B.T.S.K) and cross-checked by another (J.W.T) in accordance with the Cochrane Handbook for Systematic Reviews.⁶ No authors were contacted for further unpublished data.

Appraisal and Synthesis of Results

The Risk Of Bias In Non-Randomized Studies of Interventions (ROBINS-I) tool and Murad et al instrument was applied for included non-randomized studies and case studies or case reports respectively.^7,8 Study quality was independently assessed by 2 authors (B.T.S.K and J.W.T) with consensus attained following discussion. The ‘Robvis’ tool was utilised to generate the traffic light plot in accordance with Cochrane recommendation.⁹ No registered protocol exists for this study.

Results

Study Selection

The primary search retrieved 483 articles which was filtered to 310 after duplicates were removed (Supplemental Figure 1). 78 studies fulfilled the criteria for full-text assessment for eligibility after screening was concluded. 11 studies were eventually included in the systematic review. The most common for exclusion of articles after screening was failure to offer a new classification system.

Study Quality

Assessment of risk of bias of included studies was generally low as assessed by the instruments of Murad et al (Table 1) and the Risk of Bias In Non-Randomised Studies (ROBINS-I) tool (Supplemental Figure 2).

Table 1.

Risk of Bias Assessment of Included Case Series and Case Report Studies Assessed by the Tool Developed by Murad et al.¹

Domain	Selection	Ascertainment		Causality				Reporting	Overall risk of bias
Question	1	2	3	4	5	6	7	8	Overall risk of bias
Holdsworth, 1970⁶	-	+	+	NA	NA	NA	+	+	Low
Jacobs et al., 1975⁸	-	+	+	NA	NA	NA	+	-	Moderate
Babcock et al., 1976⁹	-	+	+	NA	NA	NA	-	+	Moderate
Allen et al., 1982¹⁰	-	+	+	NA	NA	NA	+	-	Moderate
Harris et al., 1986⁴⁵	-	+	+	NA	NA	NA	-	+	Moderate
Aebi and Nazarian, 1987¹³	-	+	+	NA	NA	NA	+	+	Low
Moore et al., 2006¹⁴	-	+	+	NA	NA	NA	+	-	Moderate

Questions Within Domains

1. Does the patient represent the whole experience of the centre, or is the selection method unclear to the extent other patients with similar presentation may not have been reported?

2. Was the exposure adequately ascertained?

3. Was the outcome adequately ascertained?

4. Were other alternative causes that may explain the observation ruled out?

5. Was there a challenge/rechallenge phenomenon?

6. Was there a dose-response effect?

7. Was follow-up long enough for outcomes to occur?

8. Is the case(s) described with sufficient details to allow other investigators to replicate the research or to allow practitioners to make inferences related to their own practice?

Classification Systems

11 classification systems were identified spanning the mechanism based injuries such as that proposed by Jacobs et al or Holdsworth et al.^10,11 This was further expanded to the 6 item system of Allen et al before Vaccaro et al refined this to the AO Spine Subaxial Cervical Spine Injury Classification System.^12,13

Discussion

Subaxial Cervical Spine Historical Classification Systems

Subaxial cervical spine injury classification systems have evolved since Holdsworth admirably attempted to formulate a universal system in 1970 (Table 2).¹⁰ In this era, the ultimate goal of the scheme was to classify injuries into either stable injuries, such as simple wedge fractures or burst fractures, or unstable rotational fracture-dislocations requiring surgical stabilization.^10,14 Other historical classification systems such as that proposed by Jacobs et al and Babcock et al similarly relied purely upon the presumed mechanism of injury to stratify risk.^11,15 Fractures were merely divided into the 4 categories of compression, flexion, extension or lateral flexion injuries without clinical translation to assist surgeons in everyday decision making.^11,15 As an advancement, Allen and Ferguson’s classification was more detailed by dividing injuries into 6 separate categories but again failed to offer any objective scoring system.^14,16 This trend of merely expanding the detailed description of fractures continued when Harris et al divided cervical spine injuries into 7 groups.¹⁷ It can be deduced that these archaic schemes formed the framework of defining the archetypical cervical spine fractures, but the clinical implications of these injury patterns were not truly recognised.

Table 2.

Integration Between AO Subaxial Cervical Spine Classification System and Existing Classification Systems

Classification element considered
Study	Stability	Neurological deficit	Hierarchical	Consideration of unique qualifiers	Reliability assessed	Relevance to AO classification system
Subaxial cervical spine
Holdsworth, 1970¹⁰	Yes	No	Yes	No	No	Groups A, B and C
Jacobs et al., 1975¹¹	Yes	Yes	No	No	No	Groups A and B
Babcock et al, 1976¹⁵	Yes	No	No	No	No	Groups A and B
Bohlman et al, 1979²¹	Yes	No	No	No	No	Groups A and B
Allen et al., 1982¹⁶	Yes	Yes	No	No	No	Groups A and B
Harris et al., 1986⁴⁹	Yes	No	No	No	No	Groups A and B
Aebi and Nazarian, 1987¹⁹	Yes	Yes	Yes	No	No	Groups A and B
Argenson et al., 1997⁵⁰	Yes	Yes	Yes	No	No	Groups A, B and C
Moore et al., 2006²⁰	Yes	No	No	Yes	Yes	Groups A and B
Vaccaro et al., 2007¹³	Yes	Yes	Yes	Yes	Yes	Groups A, B and C
Vaccaro et al., 2016¹²	Yes	Yes	Yes	Yes	Yes	Groups A, B and C

It was Argenson et al who identified this and proposed a simple 3 category classification of subaxial cervical spine fractures in 1997 dividing injuries into compression injuries (33%), flexion-distraction injuries (28%) and rotation injuries (39%).¹⁸ Notably, this system recognised the importance of rotational injuries, which are type C injuries in the AO Spine Subaxial Cervical Spine Injury Classification System, as being inherently unstable and warranting a separate category.¹⁸ Beyond this, Aebi and Nazarian also considered whether there was pure bony or ligamentous involvement as there has been no universally accepted classification scheme to date.^11,15,19 In attempting to develop a universally applicable and validated classification system, Moore et al sought to demonstrate it was possible for such as a scheme to have excellent inter-observer reliability.²⁰ Unfortunately, the reliability study was conducted based upon a purely structural system proposed by Bohlman et al in 1979 in which injuries were segregated into the anterior column, middle column and posterior column based.^20,21 Nevertheless, it was useful for clinicians to appreciate the utility of a classification system as the basis upon which standardized treatment algorithms could be tested. In the following section we discuss our original research in developing the AO Subaxial Cervical Spine Injury Classification System, based upon the landmark scheme proposed by Vaccaro et al in 2007 and advanced into a quantitative scoring system in 2016.^12,13

Subaxial Cervical Spine Classification Systems – AO Spine Classification

The AO Subaxial Cervical Spine Injury Classification System introduces fractures from a logical manner with Type A compression injuries consisting of the minor and stable A0 minor non-structural fractures, A1 compression fractures or the A2 pincer fractures (Figure 1).^12,13 Along the spectrum lies the incomplete A3 burst fracture and complete A4 burst fracture whose differentiation in severity has been heavily interrogated in recent studies (Figure 2).^4,12,13 This is proceeded by type B tension band injuries and the grossly unstable type C displacement injuries (Figures 3 and 4).^12,13 A separate gradated introduction to facet fractures has also been described (Figure 5) before this is amalgamated into a universally accepted classification with relevant modifiers (Figure 6). This novel system draws upon the basic morphological compression fracture subtypes introduced by Holdsworth and Babcock et al, before also acknowledging the importance of ligamentous disruption as Aebi and Nazarian argued regardless of whether this is the posterior tension band or anterior tension band in type B fractures.^10,15,19 Lastly, the AO Spine system also nods to the rotational injury category, which generally causes displacement as proposed by Argenson et al.¹⁸ Vitally, a number of studies have validated this AO Spine classification system as the culmination of these previous historical schemes.^{10,11,15,18-21}

Figure 1.

Type A compression injuries ranging from A0 stable injuries of the spinous process or lamina to the compression fractures represented by the A1 category. In contrast, A2 fractures are coronal split deformities involving both vertebral body endplates

Figure 2.

A3 injuries are single endplate burst fractures whereas A4 are complete burst fractures involving both endplates

Figure 3.

Type B injuries are those which affect the tension band. The B1 subtype class is typified by failure of the bony posterior tension band, whilst B2 are characterized by ligamentous posterior tension band injury. The B3 injuries are those in which the anterior tension band is disrupted

Figure 4.

Type C translational injuries are the most severe and are biomechanically unstable with the highest rate of neurological deficit

Figure 5.

Facet injuries are classified into their own class with F1 non-displaced facet fractures being generally stable, proceeded by F2 facet fractures involving greater than 1 centimetre bony fragmentation or greater than 40% of the lateral mass. The F3 group is the floating lateral mass injury with the F4 being the most unstable subluxed or perched facets

Figure 6.

The AO Spine Cervical Spine Injury Classification System distilled into a flowchart but note is made that the degree of neurological injury is also taken into consideration

More than this, the AO Spine Cervical Spine Injury Classification System argues that the subaxial cervical spine should not be perceived as a single entity but as different components being divided into the upper (C3 and C4), middle (C5) and lower (C6 and C7) regions.²² In fact, 55% of cervical spine injuries are located at the level of C5/6 and C6/7.²³ Furthermore, 21.2% of cervical fractures occur at the level of C6/7 and 14.0% at C7 or C7/T1.²⁴ We determined that surgeons were far more likely to operatively manage incomplete and complete burst fractures if they were located at the lower junctional cervical spine than located elsewhere.²² It was also striking that this was a universal finding which did not change irrespective of geographical region, surgeon experience or clinician specialty.²² There are numerous biomechanical reasons for why surgeons perceive injuries to the lower junctional cervical spine as more severe and likely to require surgical stabilization.^25-28

Firstly, the main movement of flexion and extension is initiated by the middle and lower cervical spine segments.² Indeed, the C6/7 segment initiates flexion-extension and also contributes the most to the range of motion followed by C5/6 and C4/5.² Maiman et al determined that the C5/6 (17.1 ± 3.9°) and C6/7 (18.1 ± 6.1°) levels underwent the most flexion-extension compared to the upper and middle cervical spine.²⁹ Dowdell et al argued that the facet joint angles are usually oriented at 45° in the axial plane and 85° in the sagittal plane but increase in the lower subaxial cervical spine.³⁰ This coronal orientation of the facets facilitates the flexion-extension of the cervical spine. Secondly, a defining feature of the lower cervical spine is that the instantaneous centre of rotation (ICR) is located progressively more cranial in the lower cervical spine.³¹ Bogduk et al found that when the cervical spine undergoes deformation after an impact, it is the lower cervical segments which sustain an unusual amount of posterior rotation leading to impaction of the facet joints.³² Finally, Ivancic et al recognised this observation that the majority of cervical fractures occurred at the lower cervical spine and investigated the forces required to cause bilateral facet dislocation.^33,34 It was striking that the average peak forces to produce the desired injury were lowest at the junctional region C7/T1 (108.3 N) compared to C5/6 (264.5 N) or C3/4 (136.2 N).

As such, injuries sustained at the cervicothoracic junction are likely to be more severe and therefore requiring operative fixation. These findings suggest that the subaxial cervical spine cannot be considered a unified entity, and this concept underpins our novel clinical study which found that surgeons were more likely to surgically fixate both A3 (P < 0.001) and A4 (P < 0.001) fractures located in the lower subaxial cervical spine compared with fractures at the upper or middle subaxial cervical regions.²² This is well reflected by Steinmetz et al who performed 593 cervico-thoracic junction operations and found that given the higher flexion-extension stresses at C7/T1 there was a much greater rate of fusion failure with both un-instrumented laminectomies and ventral multi-level corpectomies.³⁵

Several studies have investigated the injury propensity phenomenon of the lower junctional area of the subaxial cervical spine in cadaver head-neck models.³⁶ The fidelity of these animal models to the living human spine is under investigation. The cervical spine of sheep may mimic the human spine in terms of lordotic curvature and movement under stress, but these models lack consideration of the soft tissue elements which are also involved in stabilizing the human spine.^36,37 For example, Vasavada et al found the human neck muscles could generate in males and females 35 N and 15 N of force at C4 respectively, and even greater forces of 52 N and 21 N at C7.³⁸ With age, muscles may fatigue and this may also explain a greater incidence of mortality in elderly patients after injury.³⁹ Panjabi et al noted that the muscles forces of the cervical spine were more important in generating axial rotation as well as flexion/extension and muscle dysfunction was a potential cause of instability.⁴⁰ Indeed, rotation is such an important motion at this level that biomechanically the spine had greater rotary motion when in flexion by 1.4°.⁴⁰ Indeed, the spine unit was most unstable when posterior injury was combined with flexion load and anterior injury with extension load.⁴⁰

A more elegant method of investigating the biomechanics of the cervical spine is with the use of finite element analysis (FEA) models which usually consider a combination of factors including the bone (cortical vs cancellous), as well as ligament and intervertebral disc tissues (annulus fibrosus and nucleus pulposus).^41,42 With FEA models, a validated cervical spine model enables multiple simulation analyses in various scenarios to be performed without the need for repeated animal model testing.⁴³ Nonetheless, our real-world AO Spine classification study is consistent with the finding that surgeons, irrespective or geography of practice or years of experience, perceive lower subaxial cervical spine fractures as more unstable than those located in the upper and middle regions.²²

This is especially important when attempting to evaluate unique injury conditions which are not considered by traditional spine trauma classification systems. For this reason, the AO Spine Cervical Spine Injury Classification system also has a separate modifier for long segment ossifying bone disease.¹² Indeed, the strength of a column is proportional to its cross-sectional area but inversely related to its length. Consequently, the long levers created by ossifying bone disease such as ankylosing spondylitis or diffuse idiopathic skeletal hyperostosis means that longer columns fail with considerably less force than shorter segments. As such, Liu et al found that long segment fixation approaches produced better stability and lowered the maximal stress in cervical spine fractures in the setting of ankylosing spondylitis.^44-48 This scenario is one in which a change in the biomechanics of the spine means that the operative strategy must be adapted.

Evidently, future more sophisticated classification systems will be based upon not only biomechanical stability but also neurological deficit as well as taking into consideration unique bone conditions. It is also likely that increasingly advanced automated imaging will be able to generate standard biomechanical variables before integration for spinal clinicians.

Conclusions

Our review demonstrates the current AO Spine Cervical Spine Injury Classification System is reliable and logical in its introduction of morphological fracture subtypes. It represents the evolution of existing historical systems and progression into its easily recognizable three discrete fracture morphology categories to facilitate efficient clinical communication about the severity and stability of sustained fractures. Further work in advancing and developing universal treatment algorithms is still required given this fundamental classification has now been validated.

Supplemental Material

Supplemental Material - Subaxial Cervical Spine Fractures: Historical Systems and Advancements With the AO Spine Classification

Supplemental material for Subaxial Cervical Spine Fractures: Historical Systems and Advancements With the AO Spine Classification by Barry Ting Sheen Kweh, Alexander R. Vaccaro, Gregory Schroeder, Jose A Canseco, Maximilian Reinhold, Mohamed Aly, Sebastian Bigdon, Mohammad El-Sharkawi, Richard J. Bransford, Andrei Fernandes Joaquim, Harvinder Singh Chhabra, Emiliano Vialle, Rishi M. Kanna, Charlotte Dandurand, Cumhur Öner, Jin Wee Tee in Global Spine Journal

Footnotes

Acknowledgements

This study was organized and funded by AO Spine through the AO Spine Knowledge Forum Trauma, a focused group of international Trauma experts. AO Spine is a clinical division of the AO Foundation, which is an independent medically-guided not-for-profit organization. Study support was provided directly through AO Network Clinical Research.

ORCID iDs

Barry Ting Sheen Kweh

Jose A Canseco

Maximilian Reinhold

Mohamed Aly

Sebastian Bigdon

Mohammad El-Sharkawi

Richard J. Bransford

Andrei Fernandes Joaquim

Emiliano Vialle

Rishi M. Kanna

Charlotte Dandurand

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was organized and funded by AO Spine, AO Network Clinical Research through the AO Spine Knowledge Forum Trauma.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Supplemental Material

Supplemental material for this article is available online.

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Supplementary Material

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