AbstractObjectiveMinimally invasive surgery (MIS) techniques, which were initially used for the lumbar spine, are now being increasingly used for the cervical spine as well. This study compared the outcomes of posterior C1–2 fusion performed via MIS versus conventional surgery, as well as the changes in radiologic parameters after surgery.
MethodsThis study compared patients who underwent MIS and conventional surgery for atlantoaxial instability using Harm technique with interlaminar fusion and miniplate to maximize bone fusion between February 2012 and January 2021. Demographic characteristics and radiologic parameters were analyzed preoperatively, immediately postoperatively, and at 2 years postoperatively.
ResultsThe study included 17 patients with more than 2 years of postoperative follow-up, including 7 patients who underwent MIS. Statistically significant differences were found between the 2 groups at the postoperative and intraoperative C1–2 angles (p=0.027 and p=0.001, respectively). There were no significant differences between the preoperative and 2-year postoperative C1–2 angles, or in the radiologic parameters between the MIS and conventional surgery groups. Both groups showed significant positive correlations between the C1–7 angle and T1 slope angle at 2 years postoperatively.
INTRODUCTIONAtlantoaxial instability (AAI) can arise from various causes such as trauma, rheumatoid arthritis, tumors, congenital malformation, or inflammatory diseases [1-3]. Over time, several surgical methods have been developed to address this. Notably, posterior C1–2 fusion stands out as a crucial surgical intervention for addressing different spinal conditions affecting the atlantoaxial joint. The first method introduced for posterior fusion in AAI involved sublaminar wiring techniques [4]. Afterward, other well-known techniques such as transarticular screw fixation, C1 lateral mass and C2 pedicle screw fixation (C1LM-C2PS), and C1 lateral mass and C2 laminar screw fixation were adopted. Among these, C1LM-C2PS has become the preferred approach due to its high fusion rates and maximal stability, making it the gold standard [5]. However, despite the evolution and introduction of numerous methods, these surgeries remain challenging due to the potential severe complications and technical difficulties stemming from the complex bony and neurovascular anatomy in the craniovertebral junction [6-11].
Major complications from cervical surgery using the posterior approach can often result from the dissection of midline structures. To maintain the occipito–cervical tension band, a minimally invasive surgery (MIS) technique for C1LM-C2PS has been developed. This study compared the outcomes of posterior C1–2 fusion done with MIS techniques using a METRx MAST Quadrant Retractor System (Medtronics, Memphis, TN, USA) and conventional surgery in terms of radiologic parameters. Additionally, changes or effects in radiologic parameters after posterior C1–2 fusion are also discussed.
MATERIALS AND METHODSThis was a retrospective observational study. This study was approved by Institutional Review Board (IRB) of Daegu Catholic University Medical Center (IRB No. CR-24-036).
1. Patient SelectionBetween January 2012 and February 2021, patients who underwent C1LM-C2PS for posterior cervical spine surgery at our institution were studied. The indication for posterior C1–2 fusion was mechanical pain and/or cervical myelopathy caused by C1–2 subluxation. The study excluded patients who underwent previous or additional surgery on other cervical levels or revision surgery after posterior C1–2 fusion, those with a follow-up period of less than 2 years, and those with occipito–cervical fusion or underwent other types of posterior C1–2 fusion procedures (e.g., use of C2 translaminar screws and C1–2 intraarticular screws with interlaminar clamps). The criteria for selecting MIS or conventional surgery were dependent on the availability of the procedure at the time of operation. Conventional surgery was implemented earlier in the series because of its popularity at the time, but the follow-up radiographs in both procedures were obtained at the same time after surgery. A total of 17 patients were selected, and all their clinical, radiologic, and surgical reports were reviewed.
2. Surgical Techniques1) Conventional surgery [12]Under general anesthesia, the patient was placed in the prone position, and the neck was held in alignment with a Mayfield. Conventional surgery with a posterior approach refers to open surgery, where a classic midline incision is made, followed by subperiosteal dissection (occiput to C3–4 level) to expose the screw insertion points.
2) MIS technique [13]A Mayfield was used for MIS, similar to conventional surgery. Bilateral paramedian incisions were made 1.5–2 cm from the midline, and the muscles were dissected using a quadrant retractor system. The most important precaution during this surgery was to avoid palpating the C1 posterior arch and to ensure that the smallest dilator was not directed toward the C1–2 joint or into the gap between the C1 posterior arch and C2 lamina. The atlantoaxial complex was exposed up until the lateral border of the C1–2 joint. Bleeding from the epidural venous plexus dissection was controlled with bipolar electrocautery and/or thrombin and Gelfoam with cotton plegets. Afterward, the C1–2 joint was exposed, and the C1 screw entry point was prepared using a 1.7-mm high-speed burr. The pilot hole was drilled with a slight anterior-posterior convergent trajectory, guided by intraoperative landmarks and lateral view of C-arm fluoroscopy. A 4-mm Vertex polyaxial screw (Medtronics) was inserted into the C1 lateral mass. Then, the C2 pedicle screw entry point was marked and prepared on the isthmus surface of C2, with the pilot hole drilled in a convergent and cephalad direction. After tapping, a 4-mm polyaxial screw was inserted. If necessary, the C1 ring was reduced by manipulating the screws and rod fixation to maintain alignment. After screw fixation, a miniplate was used to fixate the interlaminar iliac bone graft. The C1 posterior arch and C2 lamina were decorticated, and tricortical bone taken from the posterior iliac crest was placed between the decorticated surfaces of C1 and C2. There was only minimal dissection of C1 because only the inferoposterior margin needed to be exposed for miniplate fixation. The miniplates were manually molded for optimal bone contact, and screws were placed on the C1, tricortical bone, and C2 surfaces (Figure 1A). Intraarticular fusion was achieved by decorticating the joint surfaces under direct visualization.
3. ParametersRadiographs were taken for all patients in neutral positions preoperatively, immediately postoperatively, and at 2 years postoperatively. The following spinal parameters were assessed: (1) segmental Cobb angle (SCA) (C1–2, C2–7, O–C1, O–C2, O–C7) (Figure 2A), (2) C2–7 sagittal vertical axis (SVA) (Figure 2B), (3) T1 slope angle (T1S) (Figure 2C), (4) chin-brow vertical angle (CBVA) (Figure 2D), and (5) ΔValue, which is the difference between the preoperative and 2-year postoperative values for each parameter.
4. Statistical AnalysisAll statistical analyses were performed using IBM SPSS Statistics ver. 22.0 (IBM Co., Armonk, NY, USA) for Windows. For statistical analyses, the Mann-Whitney U-test and Spearman correlation analysis were used. The differences in radiologic parameters between the 2 groups were evaluated using the Mann-Whitney U-test. The correlations among radiologic parameters were analyzed using Spearman correlation analysis. Values were expressed as the mean±standard deviation, and p<0.05 was considered statistically significant.
RESULTS1. Patient DemographicsThe study included 17 patients who underwent C1LM-C2PS, comprised 8 males and 9 females with an overall average age of 54.2 years. The average age was similar between the conventional surgery and MIS groups (58.0 years vs. 49.0 years, p=0.282). Among the 17 patients, the causes of AAI included rheumatoid arthritis (n=6), os odontoideum (n=4), trauma (n=6), and retro-odontoidal pseudotumor (n=1). Conventional surgery was done in 10 patients, while MIS was done in 7 (Table 1). Solid bone fusion was confirmed on postoperative computed tomography (CT) scan; this was defined as the formation for bony continuity between C1–2 joint (Figure 1B). Bone fusion was successfully achieved in all patients. None of the patients experienced neurological worsening or implant-related complications on follow-up.
2. Case 1A 51-year-old male presented with a generalized tingling sensation for 2 months and had a positive Lhermitte sign. Preoperative cervical x-ray revealed AAI (Figure 3A). After CT and magnetic resonance imaging, he was diagnosed with C1–2 instability due to os odontoideum. He underwent minimally invasive posterior C1–2 fusion. A 3–4 cm incision was made 1.5–2 cm from the midline bilaterally, and the muscle was dissected with the use of the quadrant retractor system (Figures 3 and 4). After screw fixation, autologous bone harvested from the iliac bone was placed between the C1–2 lamina, then fixed with a miniplate. Our MIS technique included individual screw placement in C1 and C2 as suggested by Harms in order to reinforce stabilization and accomplish successful bone fusion [13].
3. Radiologic Parameters1) C1–2 SCA (°)The average C1–2 angles preoperatively, postoperatively, and 2 years postoperatively, respectively, were 17.4°, 18.3°, and 18.3° in the conventional surgery group, while these were 24.5°, 24.8°, and 22.7° in the MIS group. There was a significant difference between the 2 groups in the C1–2 angle postoperative (p=0.027) but not at the other time points (Table 2).
2) C2–7 SCA (°)The average C2–7 angles preoperatively, postoperatively, and 2 years postoperatively, respectively, were 13.5°, 15.2°, and 10.3° in the conventional surgery group, while these were 13.8°, 11.0°, and 7.8° in the MIS group. There were no statistically significant differences between the 2 groups (Table 2).
3) SCA (O–C1, O–C2, C1–7, O–C7) (°), CBVA (°), T1S (°), C2–7 SVA (mm)These radiologic parameters were not significantly different between the 2 groups at all time points (Table 2).
4) Change in radiologic parameters preoperatively versus 2 years postoperativelyThe ΔC1–2 angle and ΔC2–7 angle were similar between the 2 groups. The other Δvalues also did not show any significant differences (Table 3).
5) Correlations of parametersThere was a significant positive correlation between the 2-year postoperative C1–7 angle and T1S in the conventional surgery group (r=0.754) (Table 4), as well as in the MIS group (r=0.865) (Table 5). Additionally, cervical lordosis and T1S had a positive correlation in both groups. In the MIS group, the C1–7 angle had a significant positive correlation with the C2–7 angle (r=0.964) and ΔC2–7 angle (r=0.955), as well as a negative correlation with the ΔC2–7 SVA (r=-0.775). Moreover, the C2–7 angle had a positive correlation with the T1S (r=0.775) and a negative correlation with the ΔC2–7 SVA (r=-0.857). T1S exhibited a positive correlation with the ΔC2–7 angle (r=0.955) and a negative correlation with the ΔC2–7 SVA (r=-0.775). Lastly, the ΔC2–7 angle and ΔC2–7 SVA showed a negative correlation (r=-0.857) (Table 5).
DISCUSSIONPosterior C1–2 fusion was first described by Mixter in 1910, initially using a braided silk thread [4]. More biomechanically stable modifications were gradually made over time, and now, polyaxial screw-rod constructs are used [14]. The conventional approach for the placement of C1LM-C2PS, as originally delineated by Goel and Laheri [15], and subsequently refined by Harms and Melcher [12], requires an extensive midline surgical exposure from the occiput to C3–4 level. This exposure is critical to achieve adequate lateral retraction of the posterior neck muscles, allowing access to the anatomical landmarks necessary for accurate screw insertion.
Today, MIS is a widely utilized approach in spine surgery, particularly for posterior thoracolumbar instrumentation. The key principles of MIS include smaller incisions, paramedian approaches, minimal dissection and muscle stripping, the use of the operating microscopes, specialized retractors, and instruments, and greater reliance on fluoroscopic guidance. MIS techniques primarily aim to reduce iatrogenic muscle injury, minimize postoperative pain, and promote faster recovery [16]. The postoperative outcomes of MIS are comparable, if not superior, to traditional open lumbar procedures, especially in terms of pain relief, blood loss, return to work, and postoperative infections [17]. Although MIS techniques were initially popular for lumbar spine surgeries, they are now being used for the cervical spine as well, as seen in common posterior cervical procedures such as foraminotomy, laminoforaminotomy, stenosis decompression, and lateral mass screw placement [18-20]. In particular, segments C2–6 have been identified as suitable for MIS fusion, with favorable outcomes reported [19,21].
Recent studies have explored the feasibility of minimally invasive posterior C1–2 fusion, aiming to minimize damage to midline structures [13,14,22,23]. Mendez-Gutierrez et al. [24] reported their experience with performing C1LM-C2PS using a paramedian vertical skin incision and a tubular retractor system. It is possible to preserve the occipital–cervical tension band while providing additional biomechanical stability to the construct. Lvov et al. [25] introduced the use of a transmuscular approach with a tubular retractor for transarticular screw insertion; this technique reduces operative time and blood loss and decreases the severity of postoperative pain without additional radiation exposure. They reported that this method could potentially replace the traditional posterior midline approach.
Not exposing the midline structures means preserving the muscular attachments of the C2 spinous process, which serve as stabilizers of the craniocervical junction, thereby preventing postoperative loss of lordosis [23]. This is the first study to compare conventional surgery and MIS in examining the changes in sagittal alignment due to the integrity of the occipito–cervical tension band. We found no significant differences between the 2 groups in terms of the C1–7 angle and the O–C7 angle at the final follow-up. Therefore, the postoperative loss of lordosis was comparable between the MIS and conventional surgery groups.
The ideal angle of C1–2 fusion is approximately 20° according to Toyama et al. [26], while it is 26.5° in males and 28.9° in females as reported by Nojiri et al. [27]. Nevertheless, after posterior C1–2 fusion, some patients develop loss of the normal lordotic curvature of the cervical spine, straight cervical alignment, kyphotic deformity, and even swan neck deformity, alongside anterior motion of the inferior articular process, joint capsule tears, and increased height between spinous processes, resulting in subluxation [26,28]. Subaxial kyphosis after posterior C1–2 fusion is associated with worse clinical outcomes and a higher incidence of lower cervical disc degeneration [29]. Among asymptomatic patients, the alignment of the occiput with the upper cervical spine is related to its alignment with the lower cervical spine [27]. In the current study, the preoperative C1–2 angle was similar between the 2 groups, but there was a significant difference in the postoperative C1–2 angle. To analyze the cause, C-arm fluoroscopy intraoperative images were examined, and the change was attributed to a significant difference in the intraoperative C1–2 angle (Table 2). This is likely because the C1LM-C2PS allows for intraoperative reduction [12,30,31], thus enabling the desired angle to be achieved during surgery. However, no significant differences were observed between the 2 groups at the final follow-up images. Furthermore, there were no significant differences in the ΔC1–2 angle and ΔC2–7 angle between the 2 groups, nor in the C2–7 angle at all time points. Therefore, the 2 surgical methods have no significant difference in the incidence of postoperative subaxial kyphosis.
Nojiri et al. [27] reported significant negative correlations between the O–C2 (measured from the McGregor line) and C2–7 angles, as well as between the C1–2 and C2–7 angles. Oshima et al. [31] found a negative linear correlation between the perioperative changes in the C1–2 and C2–7 angles. Although both groups in our study similarly showed a negative correlation, this was not statistically significant. To decrease the risk of postoperative subaxial kyphotic change, surgeons should take great care in determining the C1–2 fusion angle.
The C1–2 angle may be the terminal link between the cranium and cervical spine which regulates the angle of gaze. This relationship is analogous to how the pelvis tilts to maintain an upright posture [32]. CBVA as a parameter of consideration is significantly correlated with good postoperative outcomes, including ambulation, gaze, and activities of daily living [33-35]. Although the ideal CBVA has not been established, a study of 120 asymptomatic adults found it to be -1.7° [36], whereas another research suggested that a CBVA of ±10° is desirable [34]. Lafage et al. [37] reported that a CBVA between -4.7° and +17.7° was associated with the lowest scores on the Oswestry Disability Index (ODI) in a cohort of 303 patients. In our study, the average 2-year postoperative CBVA was -0.6° for the conventional surgery group and -2.5° for the MIS group. The relationship between these values and clinical outcomes, as well as determining the ideal CBVA, remains a subject for further study.
Anatomically, the cervical spine is located above the T1 vertebral body, fixed to the sternum and the first rib, with minimal movement. Lee et al. [38] demonstrated a significant increase in cervical lordosis with increasing T1S, suggesting compensatory changes in cervical lordosis to maintain horizontal gaze. In the current study, both groups had a significant positive correlation between the C1–7 angle and T1S at 2 years postoperatively. Additionally, the C2–7 SVA, another parameter of cervical sagittal balance, is related to the modified Japanese Orthopaedic Association (mJOA) score, Neck Disability Index (NDI), and 36-item Short Form health survey [32,39]. Hardacker et al. [40] determined that the C2–7 SVA in standing asymptomatic volunteers was around 16.8±11.2 mm. Table 2 shows that the average 2-year postoperative C2–7 SVA was not significantly different between the conventional surgery and MIS groups (15.0 mm vs. 14.5 mm).
The extent of postoperative subaxial kyphosis in the MIS group was noninferior compared to the conventional surgery group. Moreover, the integrity of the occipito–cervical tension band did not significantly influence changes in cervical lordosis. Consequently, further research is warranted to elucidate the relationships among various cervical sagittal parameters and clinical outcomes such as the mJOA score, ODI, and NDI. Additionally, the impact of the integrity of the occipito–cervical tension band on clinical outcomes remains an important subject for further study. Thus, determining the ideal C1–2 fusion angle, CBVA, and C2–7 SVA can minimize potential complications following posterior C1–2 fusion.
This study has several limitations. First, the study has a relatively small sample size and is retrospective in nature. Second, since this was a single-center study, the results cannot be generalized to other populations. Further studies with more follow-up results are needed to assess long-term outcomes.
CONCLUSIONThe radiological findings of the MIS group were comparable to those of the conventional surgery group. MIS involves a smaller incision, which leads to less muscle and ligament damage. Our findings indicate that minimally invasive posterior C1–2 fusion can be effectively performed as a treatment modality. However, since an inadequate C1–2 angle can promote subaxial kyphosis, finding the ideal C1–2 angle remains a challenge to be addressed.
Figure 1.(A) Bone from the iliac crest (the white arrow) was placed between C1 and C2. Miniplates were manually molded for optimal bone contact. Screws were placed on the surfaces of C1, the tricortical bone, and C2. (B) Computed tomography scan revealing the formation of bony continuity (the white arrows) between the C1–2 joint. Bone fusion was successfully achieved. Figure 2.(A) The SCAs of C1–2, C2–7, O–C1, O–C2, and O–C7 were measured from lateral x-rays in the neutral position. The O–C1 angle was measured between McRae line and the line passing through the center of the C1 posterior arch. The O–C2 and O–C7 angles were measured from McRae line to the inferior end plates of the C2 and C7 vertebrae, respectively. The C1–2 angle was measured between the line passing through the center of the C1 anterior arch and the center of the C1 posterior arch and the inferior end plates of the C2 vertebral body. The C2–7 angle was measured between lines parallel to the inferior end plates of C2 and C7. (B) The C2–7 SVA was defined as the distance (mm) between the posterior superior corner of the C7 vertebra and a plumb line dropped from the C2 vertebra. (C) The T1S was defined as the angle between the horizontal plane and the upper end plate of the T1 vertebra. (D) The CBVA was defined as the angle between a line drawn from the patient’s chin to their brow and a vertical line perpendicular to the ground. Tilting the head down (i.e., the gaze is toward the floor) produces a positive CBVA, while tilting it up produces a negative CBVA. SCA, segmental Cobb angle; SVA, sagittal vertical axis; T1S, T1 slope angle; CBVA, chin-brow vertical angle. Figure 3.(A) Preoperative dynamic x-ray during MIS. The black arrow shows a widened ADI when the patient flexes. (B) Intraoperative C-arm fluoroscopy during MIS. (C) Postoperative x-ray after MIS. The stapler mark shows the extent of the paramedian incision. MIS, minimally invasive surgery; ADI, atlantodental interval. Figure 4.Intraoperative picture of minimally invasive surgery via the paramedian approach using a quadrant retractor system. Table 1.Demographics of 17 patients with atlantoaxial instability Table 2.Radiologic parameters Table 3.Changes in radiologic parameters between preoperative and 2-year postoperative values Table 4.Spearman correlation coefficients and p-values for the parameters in the conventional surgery group Table 5.Spearman correlation coefficient and p-value of the parameters in the MIS group REFERENCES1. Liao S, Jung MK, Hörnig L, Grützner PA, Kreinest M. Injuries of the upper cervical spine-how can instability be identified? Int Orthop 2020;44:1239–53.
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