Odontoid fractures, particularly Anderson–D’Alonzo type II fractures [1], are the most common upper cervical spine injuries in adults aged 70 years and older [2]. These fractures are associated with relatively high mortality rates among patients who undergo operative treatment (3.6%) and those who receive nonoperative treatment (5.9%) [3]. Because the elevated rates of mortality and morbidity remain a pressing challenge in contemporary healthcare, the predisposing factors should be identified [4]. As the aging population increases, the incidence of odontoid fractures is expected to increase; thus, effective treatment strategies and targeted preventive measures are urgently needed.

In older adults, age-related bone degeneration increases stiffness and reduces mobility in the middle and lower cervical spine; motion is therefore shifted to the upper cervical spine, which increases the incidence of injuries in that region [5]. In younger patients, cervical fractures often result from high-energy trauma, whereas in older adults, these fractures are caused primarily by low-energy trauma mechanisms, such as falls from a standing or seated position [6]. These characteristics of cervical spine fractures in elderly people prompt the question of which structural or age-related bone and joint alterations actually increase vulnerability to type II odontoid fractures (T2OFs). Results of previous studies suggest that differing levels of osteoarthritic degeneration in the atlanto-odontoid joint and the lateral atlanto-axial joints may predispose older adults to T2OF [7]. According to research in western Europe, however, these degenerative changes are probably secondary to bone loss and aging, rather than serving as independent predisposing factors [8]. This divergence in findings indicates that a consensus about causes has not yet been reached.

Prior studies of T2OF risk factors have not addressed the potential role of ankylosing spinal disorders, such as diffuse idiopathic skeletal hyperostosis (DISH) and ankylosing spondylitis. DISH is a noninflammatory condition in which the spinal longitudinal ligaments and entheses gradually ossify, reducing mobility in the affected section [9]. According to a report from Japan, the prevalence of DISH is 26% in the general population, increasing to 48% among patients aged 70 years and older. Although results of some studies suggest no regional differences in DISH prevalence [10], analyses of whole-spine computed tomographic (CT) scans have revealed slight regional variations; the prevalence ranges from 13.2% to 19.5% [11,12]. DISH is associated with older age, obesity, hypertension, diabetes mellitus, and male sex [10], and it adversely affects bone mineral density and bone quality [13,14]. Furthermore, DISH is associated with a predisposition to spinal fractures even with low-energy trauma in elderly people [15]. DISH not only may cause an imbalance in mechanical stress on the cervical spine but also may directly affect bone strength; thus, it may be among the risk factors for T2OF.

Our aim was to assess the predisposition to T2OF in elderly patients through a comparative analysis of those with T2OFs and those with sub-axial fractures. We focused on identifying risk factors for T2OF, including bone quality, degenerative changes in adjacent upper cervical joints, and the potential role of spinal ankylosis.

Fig. 2 is the flowchart of patient selection. This study included 45 patients with T2OFs and 79 with sub-axial fractures aged 75 years or older. Table 1 lists patient characteristics, bone quality, and cervical spine degeneration. HU values at C2, C3, and C4 were significantly lower in among patients with T2OFs than in those with sub-axial fractures (ps=0.003, 0.04, and 0.049, respectively). Among patients with T2OFs, degeneration of the atlanto-occipital joint was significantly less severe (mean grade: 0.97) than among patients with sub-axial fractures (mean grade: 1.26; p=0.009), whereas facet joint degeneration was significantly more severe (p=0.03). Spinal ankylosis was more prevalent among patients with sub-axial fractures (n=27 [31.7%]) than among those with T2OFs (n=1 [2.2%], p<0.001). Table 2 lists multivariable logistic regression results that reveal risk factors for T2OF. Significant factors included atlanto-occipital degeneration (odds ratio [OR], 0.335; 95% confidence interval [CI], 0.118–0.781; p=0.02) and spinal ankylosis (OR, 0.06; 95% CI, 0.003–0.36; p=0.01). The proportion of cases with a degeneration grade difference of ≥2 between the atlanto-odontoid and lateral atlanto-axial joints was similar in both groups: three patients (6.6%) with T2OFs and 5 (6.3%) with sub-axial fractures (p>0.99).

Our study revealed that spinal ankylosis was significantly less prevalent among elderly patients with T2OFs than among those with sub-axial fractures. Moreover, multivariable logistic regression analysis showed that spinal ankylosis was associated with a lower risk of odontoid fracture. Sub-axial fractures are frequently associated with spinal ankylosis, especially in patients with DISH, and are characterized by low-energy traumatic causes, a high complication rate, poor neurological outcomes, and a 3-month mortality rate of up to 20% [22], whereas odontoid fractures have been documented in only a limited number of patients with spinal ankylosis [23].

DISH is a systemic metabolic disorder marked by the development of new bone formations and enthesopathies that affect both the axial and peripheral skeleton. Although the pathogenesis of DISH has not yet been fully elucidated, Okada et al. [24] reported that metabolic syndrome was significantly associated with DISH. Metabolic syndrome was recently reported to be associated with ossification of the posterior longitudinal ligament (OPLL) as well as with DISH [25], and OPLL was shown to be associated with an increase in systemic bone mineral density [26]. In some cases of DISH in the cervical or thoracic spine, bone density is increased in the lumbar spine (L1–L4) [13]; however, significant reductions of HU values have been reported in the middle of autofused long segments, which is consistent with stress shielding [14]. In cervical DISH, the middle to lower cervical vertebrae are often fused [11], whereas C2 is positioned in a region less affected by stress shielding from long segment autofusion. In addition, cervical spinal fractures associated with DISH tend to occur at the level of the intervertebral disc rather than that of the vertebral body, whereas the opposite is true of DISH-related fractures of the thoracic spine [27]. This observation further suggests that T2OFs may be less likely to occur in patients with DISH than in those without.

In this study, of the patients with cervical fractures, those with spinal ankylosis exhibited significantly higher HU values at C2 than did those without spinal ankylosis. Investigators have examined cervical HU values in patients with axial spondyloarthritis (mean age: 49 years), reporting values higher than those in our study: 354 at C3 and 350 at C4 [28]. In addition, Han et al. [18] found that the average HU value at C3 was 231.5±52 in individuals with osteoporosis and 284.0±63.3 in those with osteopenia. Therefore, in both the patients with T2OFs and those with sub-axial fractures in our study, bone quality was probably impaired. Our logistic regression analysis revealed an association between lower HU values at C2 and the occurrence of T2OF. Furthermore, of the female patients, those with T2OFs had significantly lower HU values at C2–C4 than did those with sub-axial fractures. At this time, our findings are primarily of academic significance and do not reveal strategies for preventing T2OF. However, they suggest that osteoporosis may play a role in T2OF development, particularly in women, and that improving bone quality through osteoporosis treatment could help reduce its incidence. Further research is needed to determine the effectiveness of osteoporosis treatment in lowering T2OF risk.

We also found that degeneration of the atlanto-occipital joint was significantly associated with a reduced incidence of T2OF. Although this finding contradicts those of previous reports [8], one possible reason may lie in the choice of control group in our study, which comprised patients with sub-axial fractures. The atlanto-occipital joint contributes to approximately 50% of cervical flexion [29]; therefore, increased degeneration may lead to limited flexion–extension mobility of the entire cervical spine. As a result, sub-axial fractures may have occurred more frequently than T2OFs, which are typically associated with rotational mechanisms.

Investigation of the predisposing factors for odontoid fractures in elderly people is made more complex by the difficulty in establishing an appropriate control group. Because the control group must consist of patients with cervical spine trauma, previous researchers have enrolled controls such as patients with C2 fractures other than T2OFs [7], those with sub-axial fractures [8], or a combination of patients without fractures and those with non-odontoid cervical fractures [30]. Because the control groups differ among studies, direct comparisons are challenging. In addition, our sex-specific analysis revealed notable patterns. The prevalence of spinal ankylosis was significantly lower among men with T2OFs than among men with sub-axial fractures. Conversely, HU values at C2, C3, and C4 were significantly lower in women with T2OFs than in women with sub-axial fractures, although the prevalence of spinal ankylosis did not differ between those two groups. Investigators in previous studies have reached no clear consensus about which sex is more susceptible to T2OF. Spinal ankylosis is more prevalent in men, whereas osteoporosis is more common in women; because both conditions tend to progress with age, sex-specific analyses may provide valuable insights, particularly in elderly populations.

This study had several limitations. First, as a retrospective study, it was prone to selection bias. Second, because the sample size was small, the generalizability of the findings is limited. In addition, patients with T2OFs had low-energy trauma injuries without spinal cord injury, whereas those with sub-axial fractures included patients with spinal cord injuries. Further research with larger, sex-stratified cohorts and comparable trauma severity is needed. Third, we studied ankylosing spinal disorders collectively without distinguishing patients with DISH from those with ankylosing spondylitis, despite the differing inflammatory mechanisms of these diseases [31]. In future studies, researchers should examine these conditions separately. Last, although the prevalence of spinal ankylosis in our study population was similar to that in the national registry, the prevalence of DISH was high in our study. Because DISH incidence varies by region, genetics, and nutrition [32], our findings may not be generalizable to other populations; thus, further research is warranted.

In this study, multivariate regression logistic analysis revealed spinal ankylosis and degenerative changes of atlanto-occipital joints as statistically significant predisposing factors for T2OF. Moreover, sex-specific analysis revealed distinct trends: spinal ankylosis was significantly less prevalent among men with T2OFs than among men with sub-axial fractures, whereas C2–C4 HU values were significantly lower in women with T2OFs than in women with sub-axial fractures.