Reciprocal change of occipitocervical parameters after anterior cervical discectomy and fusion

To evaluate the reciprocal changes in occipitocervical parameters according to the recovery of cervical lordosis (CL) after anterior cervical discectomy and fusion (ACDF) in patients with sagittal imbalance. Sixty-five cases that underwent ACDF were followed. They were divided according to the recovery of the CL: Group 1 (ΔCL > 5°, 30 cases) and Group 2 (ΔCL < 5°, 35 cases). The following parameters were measured: occiput-cervical inclination (OCI), CL, occiput-C2 angle (OC2A), distance between external occipital protuberance and spinous process of C2 (OC2D), distance between spinous processes of C2 and C7 (C27D), and shortest distance between the plumb line of C2 body and posterosuperior corner of C7 (C27SVA). Overall, all parameters changed significantly after ACDF. Preoperative CL and preoperative C27D showed a correlation with ΔCL. ΔCL was negatively correlated with ΔC27D and ΔC27SVA. In Group 1, CL increased from − 2.60 ± 1.88° to 11.57 ± 1.83°, OC2A decreased from 23.96 ± 2.05° to 19.87 ± 1.36°, OC2D increased from 82.96 ± 1.48 mm to 86.50 ± 1.81 mm, C27D decreased from 95.61 ± 2.66 mm to 87.01 ± 2.50 mm, and C27SVA decreased from 24.14 ± 2.20 mm to 17.06 ± 2.14 mm. In Group 2, only OCI decreased significantly after ACDF. ACDF can increase CL postoperatively in patients with cervical sagittal imbalance. Patients with significant CL recovery after ACDF showed a reciprocal change in occipitocervical parameters. (OC2A, OC2D).

Operative technique. The patient was placed in supine position with padding beneath the posterior neck.
The index level was identified on the lateral view of the fluoroscope. Transverse skin incision along the skin crease was made. After longitudinal platysma splitting, a standard Smith-Robinson approach was performed. Discectomy and endplate cartilage removal were performed. In patients with cervical spondylotic radiculopathy or amyotrophy, longus colli muscles were dissected more laterally until full exposure of the uncovertebral joint to perform additional uncinectomy. Polyetheretherketone (PEEK) cage (Cervios ChronOS, Synthes GmbH, Oberdorf, Switzerland), allogenic fibular bone (Matrispine, Lifenet Health, Virginia Beach, VA, USA), or autogenous iliac strut bone was used for an interbody spacer. PEEK cage had 7.5° of lordosis, allogenic fibular bone had 7° of lordosis, and autogenous iliac strut bones were trimmed to the desired angle of the index disc space. To minimize adjacent segment disease, the height of the plate was adjusted that the distance between the plate and adjacent disc space was at least 5 mm on the sagittal plane. Patients were recommended to use the Philadelphia brace for 6 weeks after surgery.
Radiographic evaluation. All measurements were performed by a picture-archiving communication system (PACS) (INFINTT PACS; INFINITT Healthcare, Seoul, Korea). We collected the preoperative and postoperative follow-up plain radiographs of the lateral cervical spine. The patients were placed on a comfortable standing position while maintaining a horizontal gaze while the radiographs were obtained. Occipitocervical inclination (OCI), CL, OC2A, occiput-C2 interspinous process distance (OC2D), C2-7 interspinous process distance (C27D), and C27SVA were measured. The measuring methods for each parameter were as follows ( A paired t-test or Wilcoxon sign rank test was used for change in cervical parameters. Student's t-test and independent t-test were performed for continuous variables, and chi-square test was performed for categorical variables. A p-value < 0.05 was considered statistically significant. The intraclass correlation coefficient was calculated based on absolute agreement and two-way mixed-effects model. Values < 0.5, between 0.5 and 0.75, between 0.75 and 0.9, and > 0.9 indicated poor, moderate, good, and excellent reliability, respectively 15 .

Results
After selecting the patients according to our criteria, a total of 65 patients were eligible in this study. We divided the patients according to the recovery of CL postoperatively. Patients with postoperative CL change (ΔCL) of ≥ 5° were designated as Group 1, and patients with ΔCL < 5° were designated as Group 2. Positive value of ΔCL indicated postoperative increment and vice versa. The demographics and operative details of both groups are described in Table 1. All variables did not show a significant difference between the two groups. www.nature.com/scientificreports/ A 55-year-old man who underwent ACDF on C6-7 due to soft disc herniation (a) Preoperative lateral X-ray (b) Postoperative follow-up lateral X-ray. Note the increment of CL and OC2D and decrement of OC2A and C27SVA. ① McGregor line ② C2 lower endplate ③ posterior border of the fourth cervical vertebral body ④ C7 lower endplate ⑤ distance between external occipital protuberance and most prominent portion of C2 spinous process (OC2D) ⑥ distance between the C2 and C7 spinous process (C27D) ⑦ shortest distance between the plumb line from the center of second cervical vertebrae body and posterosuperior corner of seventh cervical vertebrae body (C27SVA). OCI, angle between ① and ③; OC2A, angle between ① and ②; CL, angle between ② and ④. Lordotic angle is measured as positive value, and kyphotic angle is measured as negative value. Positive C27SVA indicates that the C2 plumb line is anterior to posterosuperior corner of C7 body and vice versa. ACDF, anterior cervical discectomy and fusion; CL, cervical lordosis; OC2D, occiput-C2 distance; OC2A, occiput-C2 angle; C27SVA, C2-7 sagittal vertical axis; C27D, C2-C7 interspinous process distance; OCI, occipitocervical inclination. .40 mm to 20.08 ± 11.54 mm ( Table 2). The overall correlation between preoperative and change in parameters are summarized in Table 3. Preoperative CL and preoperative C27D showed a correlation with ΔCL (r = − 0.413 and p = 0.000, and r = 0.210 and p = 0.013, respectively) ( Fig. 2). In other words, lower preoperative CL and higher preoperative C27D showed more increment of CL postoperatively. ΔCL was negatively correlated with ΔC27D and ΔC27SVA (r = − 0.551, p = 0.000 and r = − 0.206, p = 0.015, respectively) ( Fig. 3). In other words, more increase of CL was related to more decrease in C27D and C27SVA. Preoperative CL was significantly lower and preoperative C27D was significantly higher in Group 1 compared to Group 2. Other preoperative radiographic parameters were not significantly different between the two groups (Table 4).

Discussion
Our study showed that ACDF increased CL and OC2D and decreased OCI, OC2A, C27D, and C27SVA postoperatively. Specifically, patients with ΔCL > 5° showed a significant change in all parameters except for OCI. On the other hand, patients with ΔCL < 5° showed no significant change in cervical sagittal parameters after surgery except for OCI.
Essentially, to maintain a horizontal gaze, the curvature of the cervical spine changes 17 . The classical parameter used for measurement of horizontal gaze is the chin-brow vertical angle (CBVA), with others including McGregor slope (McGS) and slope of the line of sight 4,18 . However, the landmarks of CBVA were not all readily measured on our plain radiographs. A study revealed that McGS was significantly correlated with CBVA; thus, McGS was measured in our study to evaluate the horizontal gaze 18  There are three main methods of measuring the CL: Cobb's method, Harrison posterior tangent method, and Jackson's physiological stress line method. Cobb's method of CL can be measured at C1-7 or C2-7. CL using Table 2. Overall patients change of cervical sagittal parameters. All continuous values are in mean ± standard deviation. Values for OCI, CL, and OC2A are degrees, and for OC2D, C27D, and C27SVA are millimeters. OCI, occipitocervical inclination; CL, cervical lordosis; OC2A, occiput-C2 angle; OC2D, occiput-C2 spinous process distance; C27D, C2-C7 interspinous process distance; SVA, C2-C7 sagittal vertical axis. p value below 0.05 is considered statistically significant. www.nature.com/scientificreports/ Cobb's method in C1-7 tend to overestimate the angle, and that in C2-7 underestimates the angle, while the Harrison posterior tangent method provides the most accurate value. However, due to the advantages of picture archiving and communicating systems with good intra-and interobserver reliability, Cobb's angle method is the most common measurement method 1,10 . Preoperative CL was negatively correlated with ΔCL, while preoperative C27D positively correlated with ΔCL. The flexion posture of the head increases the lower cervical foraminal areas 6 . Since the patients in this study had neurologic symptoms, preoperatively, patients tend to maintain flexion posture resulting in lower preoperative CL and higher C27D. We assume that, postoperatively, patients tend to recover CL not only because of the lordotic-shaped implants but also due to decompression of the neural elements. Bao et al. divided individuals with or without neck symptoms and compared the sagittal parameters using biplanar stereoradiographic imaging. Among the numerous values, C27SVA, SLS, McGS, and TK showed a significant difference between the two groups, while CL did not. Especially, C27SVA was an independent predictor of cervical disability 4 . Miyazaki et al. analyzed the postoperative change in cervical alignments after cervical laminoplasty. They have concluded that the change in C27SVA was correlated with the change in OC2A. This reciprocal change was assumed to be attributed by maintaining the horizontal gaze of the individuals 17 . An experimental model of the cervical spine showed similar results. The increase in the C27SVA beyond the normal range subsequently increased OC2A 3 . Whereas cervical laminoplasty deteriorates C27SVA 19 , our results of ACDF show that C27SVA improves after surgery along with CL, which can be related to improved QOL. www.nature.com/scientificreports/ The suboccipital muscles are a group of four muscles, located below the occipital bone, and involved in the extension and rotation of the occipitocervical junction. These include the rectus capitis posterior major, rectus capitis posterior minor, obliquus capitis superior, and obliquus capitis inferior. To assess the overall length of suboccipital muscles, we have measured the OC2D. Spinalis cervicis originate from the spinous process of C7 and attach to the spinous process of the axis, forming the lower part of the ligamentum nuchae. Splenius cervicis,  www.nature.com/scientificreports/ trapezius, and semispinalis cervicis are also located in the posterior neck. We have measured the distance between the prominent posterior points of C2 and C7 spinous processes to distinguish the subaxial cervical movement from the occipitocervical junction. Flexion posture of the head may cause prolonged abnormal contraction of the suboccipital muscles 20 . In addition, the greater occipital nerve that resides in the suboccipital triangle may be impinged due to muscle contraction 6 . Our result showed increased OC2D and decreased C27D. We assume that increased OC2D will result in the relaxation of suboccipital muscles, which may, in turn, decompress the impinged greater occipital nerve. Decrement in C27D is considered a result of the improvement of CL and C27SVA, and such changes may lead to clinically favorable results. OCI was introduced in order to account for the measurement of the occiptocervical alignment, which can be adopted during upper cervical fusion surgery 16 . It is the angle formed by the line connecting the posterior border of the C4 vertebral body and McGregor's line. Measurement of OCI is easier to measure compared to the posterior occipitocervical angle (POCA) 21 , and can be measured consistently compared to occipitocervical distance (OCD), which is influenced by the morphologic variation of the C2 spinous process. OCI changes statistically significantly at the flexion and extension of the neck, and especially at the neutral position, is known to reflect CL. However, in our study, OCI did not change postoperatively in patients with significant recovery of CL, whereas it changed in patients without recovery of CL. The ramification of such a phenomenon is unclear.
There are a few limitations in our study. First, we could not involve the parameters, such as T1 slope and thoracic inlet angle. About half of patients with lateral radiographs were unable to measure such parameters.
Since such values are correlated with cervical parameters 22 , future studies with larger series should be performed in the future. Second, we did not account for the correlation with spinopelvic parameters in this study. Pelvic incidence and tilt are reported to be correlated with CL and should be considered in a future study on cervical parameter changes 10,22 . Third, since this was a radiographic study, consideration of clinical outcomes should be analyzed in future studies. Finally, equivocal landmarks and heterogeneous morphology of landmarks made the measurement difficult. To minimize the errors, the observers placed preoperative and postoperative images simultaneously on the same monitor and zoomed in the images for precise and identical identification of the landmarks. OC2D showed lower reliability compared to other parameters, probably due to the equivocal reference point. Still, the inter-and intraobserver correlations were 0.879 and 0.857, respectively, showing "good" reliability. Whereas there was a study on reciprocal change of upper cervical alignment after posterior cervical surgery 17 , no previous study focused on such postoperative change after ACDF. The additional strength of our study is that we have adopted novel parameters using the distance between the landmarks of the occipitocervical and subaxial cervical region. Table 4. Preoperative values of cervical sagittal parameters of both groups. All continuous values are in mean ± standard deviation. OCI, occipitocervical inclination; CL, cervical lordosis; OC2A, occiput-C2 angle; OC2D, occiput-C2 spinous process distance; C27D, C2-C7 interspinous process distance; SVA, C2-C7 sagittal vertical axis. p value below 0.05 indicates statistically significant difference between two groups. www.nature.com/scientificreports/ Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/.