INTRODUCTION
Atlas fractures account for approximately 2%–13% of cervical fractures and approximately 1%–2% of total spinal fractures [
1]. Currently, conservative treatment is favored for stable atlas fractures [
2,
3]. However, how to handle unstable atlas fractures, which include all fractures except anterior arch single fractures without transverse ligament rupture or posterior arch fractures, is debatable [
4]. Conventional atlantoaxial or upper cervical fusion can result in loss of cervical motor function and lower quality of life [
5], while nonsurgical treatment methods are associated with a high nonunion rate of atlas fracture [
6]. In 2004, Ruf et al. [
7] first proposed C1-ring osteosynthesis via a transoral approach to treating unstable Jefferson fractures. Subsequently, C1-ring osteosynthesis has gradually become one of the ideal procedures for treating unstable atlas fractures because it can instantly reduce and fix fractures while preserving the motor function of the upper cervical spine [
5,
8-
10].
Currently, C1-ring osteosynthesis is most commonly performed via transoral anterior plate fixation [
9,
11] and posterior screw-rod fixation [
12,
13]. Previous studies have aimed to investigate the effectiveness of each C1-ring osteosynthesis procedure. However, to the best of our knowledge, no comparative studies of these 2 procedures have been reported. In this study, we retrospectively analyzed the clinical data of 49 patients with unstable atlas fractures treated with C1-ring osteosynthesis via the use of the transoral anterior Jefferson-fracture reduction plate (JeRP) [
14,
15] or the conventional posterior screw rod (PSR). We compared the clinical efficacy of these 2 procedures, which is important for the selection of clinical procedures.
RESULTS
1. Patient Characteristics
All 49 patients completed the surgery successfully. The mean surgical times were 104.5 ± 14.7 minutes (JeRP group) and 110.6 ± 18.5 minutes (PSR group), with no significant difference between the 2 groups (p = 0.214). The mean blood loss in the JeRP group was lower (69.4 ± 20.2 mL vs. 103.3 ± 25.4 mL, p < 0.001). The mean length of stay in the PSR group was 8.1 ± 1.6 days, which was significantly shorter than the 11.6 ± 1.6 days in the JeRP group (p < 0.001).
2. Clinical Symptom Parameters
There was no significant difference in the preoperative VAS scores (5.5 ± 1.1 vs. 5.3 ± 1.0, p = 0.569) or NDI (58.1% ± 4.1% vs. 57.6% ± 4.2%, p = 0.640) between the 2 groups. The postoperative (JeRP: 5.5 ± 1.1 vs. 0.8 ± 0.8, p < 0.001; PSR: 5.3 ± 1.0 vs. 1.1 ± 0.8, p < 0.001) and final follow-up (JeRP: 5.5 ± 1.1 vs. 0.4 ± 0.5, p < 0.001; PSR: 5.3 ± 1.0 vs. 0.3 ± 0.5, p < 0.001) VAS scores of both groups were significantly greater than the preoperative scores, with no difference between groups (0.8 ± 0.8 vs. 1.1 ± 0.8, p = 0.312; 0.4 ± 0.5 vs. 0.3 ± 0.5, p = 0.714). The NDI was significantly lower in both groups after surgery (JeRP: 58.1% ± 4.1% vs. 26.8% ± 4.0 %, p < 0.001; PSR: 57.6% ± 4.2% vs. 26.3% ± 4.4%, p < 0.001) and at final follow-up (JeRP: 58.1% ± 4.1% vs. 1.7% ± 2.4%, p < 0.001; PSR: 57.6% ± 4.2% vs. 2.2% ± 2.4%, p < 0.001), with no differences between the groups (26.8% ± 4.0% vs. 26.3% ± 4.4%, p = 0.721; 1.7% ± 2.4% vs. 2.2% ± 2.4%, p = 0.501).
3. Radiographical Parameters
There were no differences in preoperative parameters, such as DAAF, DPAF, LMD, or the Redlund-Johnell value, between the 2 groups. Postoperative DAAF and DPAF were significantly smaller in the PSR group (7.1 ± 2.0 mm vs. 4.6 ± 4.9 mm, p = 0.006; 2.9 ± 1.9 mm vs. 1.1 ± 1.4 mm, p < 0.001). In the JeRP group, the postoperative DAAF was also significantly smaller (7.2 ± 3.1 mm vs. 1.5 ± 1.6 mm, p < 0.001), whereas there was no significant difference in the DPAF reduction (2.2 ± 1.4 mm vs. 2.0 ± 1.4 mm, p = 0.408). However, the postoperative DAAF in the JeRP group was much smaller than that in the PSR group (1.5 ± 1.6 mm vs. 4.6 ± 4.9 mm, p = 0.002), while the postoperative DPAF in the JeRP group was greater than that in the PSR group (2.0 ± 1.4 mm vs. 1.1 ± 1.4 mm, p = 0.028). The LMDs of the JeRP group were 5.6 ± 2.6 mm, 0.9 ± 1.4 mm, and 0.5 ± 1.1 mm before surgery, after surgery, and at the last follow-up, respectively; and those of the PSR group were 5.5 ± 3.3 mm, 2.2 ± 2.8 mm, and 1.9 ± 3.0 mm, respectively. The LMDs in both groups was significantly smaller after surgery (JeRP: p < 0.001; PSR: p < 0.001), and the postoperative and final follow-up LMDs in the JeRP group were significantly smaller than those in the PSR group (0.9 ± 1.4 mm vs. 2.2 ± 2.8 mm, p = 0.042; 0.5 ± 1.1 mm vs. 1.9 ± 3.0 mm, p = 0.025). The Redlund-Johnell values in the JeRP group were 37.9 ± 4.9 mm, 40.9 ± 4.3 mm, and 40.7 ± 4.2 mm before surgery, after surgery, and at the last follow-up, respectively; and these values equal 37.3 ± 2.7 mm, 38.5 ± 2.1 mm, and 38.6 ± 2.1 mm, respectively, in the PSR group. After surgery (JeRP: 37.9 ± 4.9 mm vs. 40.9 ± 4.3 mm, p < 0.001; PSR: 37.3 ± 2.7 mm vs. 38.5 ± 2.1 mm, p < 0.001) and at the last follow-up (JeRP: 37.9 ± 4.9 mm vs. 40.7 ± 4.2 mm, p < 0.001; PSR: 37.3 ± 2.7 mm vs. 38.6 ± 2.1 mm, p = 0.002), the Redlund-Johnell value significantly improved in both groups, and the Redlund-Johnell value was greater in the JeRP group than in the PSR group (40.9 ± 4.3 mm vs. 38.5 ± 2.1 mm, p = 0.014; 40.7 ± 4.2 mm vs. 38.6 ± 2.1 mm, p = 0.029). Both observers’ intraobserver and interobserver reliability showed well in all radiographic parameters measured, including preoperative DAAF (ICC, 0.91; ICC, 0.86), postoperative DAAF (ICC, 0.89; ICC, 0.83), preoperative DPAF (ICC, 0.90; ICC, 0.84), postoperative DPAF (ICC, 0.91; ICC, 0.81), preoperative LMDs (ICC, 0.84; ICC, 0.80), postoperative LMDs (ICC, 0.85; ICC, 0.80), last followed-up LMDs (ICC, 0.88; ICC, 0.81), preoperative R-J value (ICC, 0.90; ICC, 0.81), postoperative R-J value (ICC, 0.91; ICC, 0.83), and last followed-up R-J value (ICC, 0.87; ICC, 0.84).
4. Complications and Healing
There was no difference in the incidence of complications after surgery between the 2 groups (atlantoaxial instability: p = 0.9; implants loosing: p = 0.526; screw misplacement: p = 0.13). Bone fusion was confirmed by continuous bone bridge formation without a visible fracture line at the fracture site on x-ray or thin-layer CT (0.9 mm) images [
17,
18]. Fracture healing was independently diagnosed by 2 orthopedic surgeons based on imaging. The fracture healing rates at 3, 6, and 12 months after surgery were 61.3%, 83.9%, and 90.3%, respectively, in the JeRP group. Similarly, the rates were 22.2%, 66.7%, and 83.3% in the PSR group, respectively. The fracture healing rate at 3 months after surgery was greater in the JeRP group (61.3% vs. 22.2%, p = 0.008), but no differences were found between the 2 groups at 6 and 12 months after surgery (83.9% vs. 66.7%, p = 0.286; 90.3% vs. 83.3%, p = 0.656). Two patients in the JeRP group and one patient in the PSR group exhibited atlantoaxial instability after surgery, which were revised by posterior atlantoaxial fixation and fusion; 2 patients with osteoporosis in the JeRP group developed implant loosening and were revised by posterior atlantoaxial fixation fusion after the anterior implants were removed; 2 cases of screw misplacement occurred in the PSR group after surgery and was revised by adjusting the screw position (
Table 2). Well intraobserver and interobserver agreements were found for bone fusion rate at 3-month (κ = 0.86; κ = 0.79), 6-month (κ = 0.84; κ = 0.81) and 12-month (κ = 0.82; κ = 0.78) follow-up.
DISCUSSION
In this study, we compared imaging and clinical indices between 2 types of C1-ring osteosynthesis. We found that there was no difference in surgical time between the 2 groups. The PSR group had more intraoperative blood loss but a shorter length of stay. The posterior pharyngeal wall is adjacent to the prevertebral fascia without much neuromuscular tissue. Compared with the posterior approach, the anterior approach does not require more dissection of paravertebral tissue for exposure. However, the anterior approach is linked to a greater risk of infection because of the complex intraoral bacterial environment. To prevent infection, patients in the JeRP group had greater difficulty in perioperative care. In addition, patients’ tracheal tubes cannot be removed immediately after JeRP, and transoral feeding should also be avoided with careful incision management. These factors lead to a longer hospital stay. The PSR group showed better improvement in postoperative DPAF than the JeRP group did, while the JeRP group showed better improvements in postoperative DAAF, LMDs, and the Redlund-Johnell value. Obviously, since the compression forces of the 2 procedures act directly on the anterior and posterior atlantoaxial arches, respectively, this could explain the greater postoperative improvement of the DAAF in the JeRP group and the greater postoperative improvement of the DPAF in the PSR group. The anterior arch participates in the construction of the atlantooccipital joint, atlantodental joint, and atlantoaxial lateral mass joint. In addition, anterior arch fractures are more likely to result in the displacement of bone fragments or atlantoaxial dislocation [
3,
19]. Thus, for unstable atlantoaxial fractures, especially when combined with posterior arch fractures, the reduction of anterior arch fractures is more important for stabilizing the upper cervical spine [
1,
9]. We suggest that the main reason is that the transoral anterior approach is the most direct way to reduce fractures in the anterior arch. This approach can restore the separated lateral mass with a smaller torque, which results in significant relief of lateral mass separation and upward displacement of the dentate process due to fracture of the anterior arch. And therefore, improve the reduction and recovery of LMDs and the Redlund-Johnell value. Although PSR fixation can directly reduce posterior arch fractures via compression at the end of bilateral screws, it can also cause the front of the lateral mass to swing laterally, leading to deviation of the reduction force transmission, insufficient anterior arch fracture reduction and even lateral mass dislocation. Especially when the anterior arch fracture distance is significantly greater than that of the posterior arch, posterior compression is stretched to the limit to close the anterior arch fracture completely. These imaging findings revealed that transoral anterior JeRP fixation provides better integral reduction than PSR fixation does. Additionally, which could explain why the short-term (3-month follow-up) postoperative fracture healing rate was greater in the JeRP group. This suggests that our patients who underwent JeRP could start functional exercises earlier than those who underwent posterior surgery, which is important for preventing postoperative complications such as scarring. Although both groups showed significant postoperative improvements in VAS scores and NDI, there was no statistically significant difference between the 2 groups. The effects of the 2 procedures on improving clinical symptoms were similar.
There was no difference in the overall complication rate between the 2 groups. Two of the 5 patients with osteoporosis in the JeRP group experienced internal fixation loosening at the long-term follow-up. The diagnostic criterion for osteoporosis was a DXA test with the T value less than -2.5. The anterior lateral mass screw fixation was performed in transoral anterior JeRP fixation, whose fixation strength is weaker than that of posterior pedicle screw fixation, especially in osteoporosis patients. Three cases of postoperative atlantoaxial instability were observed in both groups. This finding is similar to that of Tu et al. [
14], which suggests that C1-ring osteosynthesis may not be infallible. Because injuries of the transverse ligament itself are difficult to heal over time. At the same time, patients may also have injuries of muscles and other ligaments while the bonemuscle-ligament complex plays a crucial role in joint stabilization. Therefore, we suggest that preoperative 3-dimensional CT reconstruction of the ligaments around the atlantoaxial joint should be performed to more definitively judge ligament injuries, including the transverse ligament and others. It is also recommended that dynamic cervical x-rays be taken to judge the potential risk of atlantoaxial instability at postoperative follow-up. No postoperative complications such as dysphagia, hoarseness, and any disturbance in drinking and eating occurred in the JeRP group. We consider possible reasons including the small size of the steel plates used in JeRP and less postoperative stimulation of the esophagus and trachea. Besides, the indications for JeRP do not involve lateral mass fractures, with small surgical exposure and low risk of peripheral nerve injury. All surgeries were performed by an experienced senior surgeon, and surgical proficiency is also an important factor in minimizing complications such as peripheral nerve injuries.
In 1919, Jefferson [
20] first proposed one classification method for atlas fractures based on the mechanism of injury and anatomical site. In 1988, Landells and Van Peteghem [
21] categorized atlas fractures into 3 types: anterior or posterior arch fractures, anterior-posterior arch fractures, and lateral mass fractures. Subsequently, in 1991, Levine and Edwards [
22] also divided atlas fractures into 3 types, namely, posterior arch fractures, lateral mass fractures, and both anterior and posterior arch fractures. Both Landells and Levine-Edwards classifications take fracture morphology into consideration and are widely used.
According to the guidelines of the American Congress of Neurological Surgeons (CNS), the integrity of the transverse ligament is the main basis for assessing the stability of atlas fractures, which means that atlas fractures with the intact transverse ligament are considered stable fractures; otherwise, fractures with the ruptured transverse ligament are considered unstable [
23]. This method is now widely accepted. Then Dickman et al. [
24] also described atlantoaxial transverse ligament injuries, where type I refers to rupture in the middle of the transverse ligament and type II refers to avulsion fracture of the transverse ligament at the attachment point of the lateral mass. However, through retrospective analysis of a large number of cases, Lee and Woodring [
4] concluded that only anterior arch single fractures without combined transverse ligament rupture or simple posterior arch fractures should be considered stable fractures, while all other types of fractures are unstable fractures. The reason is that when multiple fractures of the anterior arch exist, even if the transverse ligament is intact, the anterior arch is too weak to restrain the odontoid from moving forward, thus leading to posterior dislocation. Additionally, when the anterior and posterior arches are both fractured, although the intact transverse ligament may prevent the separation of the lateral mass, there is a possibility of rotational displacement of the fractured mass using the attachment point of the transverse ligament as the fulcrum. Radcliff et al. [
25] pointed out that the traditional Spence Rule which states that a displacement of the C1 lateral masses by > 6.9–8.1 mm suggests the loss of transverse ligament integrity, can be inaccurate. Based on the above, we believe that the method of assessing whether a C1 fracture is stable based on the integrity of the transverse ligament may not be accurate. We are inclined to Lee et al., that is, all fractures except for anterior arch single fracture without transverse ligament rupture and posterior arch fracture are unstable fractures, which is one of the exclusion criteria of this study.
Usually, separation and displacement of the atlas increase the space of the spinal canal, and patients with neurological dysfunction are rare. Therefore, reduction and stabilization are the most important aspect in the treatment of unstable atlas fractures. Nonoperative treatment is still recommended for patients with stable atlas fractures in the first stage. However, this therapy may not be appropriate for unstable fractures. One multicenter study indicated that surgical treatment was associated with a higher fusion rate, shorter fracture healing time, more favorable clinical outcomes, and better fracture reduction for unstable atlas fractures [
6].
For surgical methods, atlantoaxial fusion has been used mostly in the past and has been tested in a timely manner to obtain satisfactory results [
26]. However, this surgery sacrifices a significant portion of the motor function of the upper cervical spine, especially axial rotational motion, thus reduces the life quality of patients after surgery. In 2004, Ruf et al. [
7] first treated 6 Jefferson-fracture patients with transverse ligament rupture via transoral anterior screw-rod fixation as C1-ring osteosynthesis. With no postoperative atlantoaxial instability, all patients achieved good outcomes with preserved cervical motion. Subsequently, reports of C1-ring osteosynthesis for unstable atlas fractures, a physiological surgical fixation, have increased. However, whether transverse ligament rupture leads to late atlantoaxial instability has become a point of controversy for this surgery. Li et al. [
8] proposed the “buoy phenomenon,” suggesting that C1-ring osteosynthesis can restore the height of the occipital-atlantoaxial complex, which tightens the loose longitudinal ligaments to maintain the stability of the atlantoaxial joints. Kollerd et al. [
27] and Li-Jun et al. [
28] also reported in their biomechanical studies that C1-ring osteosynthesis can restore the stability of the atlantoaxial joints when combined with atlas fracture and transverse ligament rupture. A study showed that posterior C1-ring osteosynthesis is superior to atlantoaxial fusion in terms of preserving the physiological function of the cervical spine and long-term relief of neck pain [
5].
Now, the mainstream approaches for C1-ring osteosynthesis include the posterior and transoral anterior approaches. Posterior C1-ring osteosynthesis is typically represented by horizontal screw-rod fixation [
8,
12]. Ruf et al. [
7] used a transoral anterior screw rod system to fix the atlas with satisfactory results, but this method did not fit the anatomical features of the anterior atlas structures. Transoral anterior C1-ring osteosynthesis is now most often performed with plate fixation [
1,
7,
9]. The JeRP fixation system based on the anatomical parameters of the anterior atlantoaxial spine was designed by General Hospital of Southern Theatre Command of PLA for transoral anterior C1-ring osteosynthesis and has showed satisfactory results in clinical application [
14,
15]. It is important to mention that for the JeRP technique, when exposing C1, especially the lateral side of the lateral mass, some important anatomical structures around C1, such as the internal carotid artery (IC) and hypoglossal nerve and so on should receive more attentions. In cases of poor preoperative conditions, such as elderly patients with atherosclerosis of IC or in cases where the fracture extends far enough to make exposure difficult, intraoperative maneuvers should be performed with greater caution.
Our study presents some limitations. First, as our study was retrospective in nature, selection bias was inevitable in the case and procedure selection process. Particularly, for different procedures we did not use more sophisticated algorithms to screen for, and these make our results potentially biased and need to be confirmed by more prospective studies in the future. In addition, the sample size in this study was small, and a larger number of patients is needed to validate the differences between the 2 techniques. Finally, the follow-up period was short, and additional attention should be given to distant complications in the future.