Clinical significance of the C2 slope after multilevel cervical spine fusion

Namhoo Kim Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and
Spine Center, Hallym University Sacred Heart Hospital, Hallym University College of Medicine, Anyang, Korea

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Kyung-Soo Suk Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Ji-Won Kwon Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Joonoh Seo Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Hunjin Ju Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Byung Ho Lee Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Seong-Hwan Moon Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Hak-Sun Kim Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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Hwan-Mo Lee Department of Orthopedic Surgery, Yonsei University College of Medicine, Seoul; and

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OBJECTIVE

The C2 slope (C2S) is one of the parameters that can determine cervical sagittal alignment, but its clinical significance is relatively unexplored. This study aimed to evaluate the clinical significance of the C2S after multilevel cervical spine fusion.

METHODS

A total of 111 patients who underwent multilevel cervical spine fusion were included in this study. The C2S, cervical sagittal vertical axis (cSVA), C2–7 lordosis, and T1 slope (T1S) were measured in standing lateral cervical spine radiographs preoperatively and 2 years after the surgery. Clinical outcome measures were visual analog scale (VAS) neck and arm pain scores, Neck Disability Index (NDI), Japanese Orthopaedic Association (JOA) scale score, and patient-reported subjective improvement rate (IR) percentage. Statistical analysis was performed using a paired-samples t-test and Pearson’s correlation, and a receiver operating characteristic (ROC) curve to determine the cutoff values of C2S.

RESULTS

C2S demonstrated a significant correlation with the cSVA, C2–7 lordosis, T1S, and T1S minus cervical lordosis. C2S revealed a significant correlation with the JOA, neck pain VAS, and NDI scores at 2 years after surgery. Change in the C2S correlated with postoperative neck pain and NDI scores. ROC curves demonstrated the cutoff values of C2S as 18.8°, 22.25°, and 25.35°, according to a cSVA of 40 mm, severe disability expressed by NDI, and severe myelopathy, respectively.

CONCLUSIONS

C2S can be an additional cervical sagittal alignment parameter that can be a useful prognostic factor after multilevel cervical spine fusion.

ABBREVIATIONS

AUC = area under the curve; C2S = C2 slope; CL = cervical lordosis; cSVA = cervical sagittal vertical axis; IR = improvement rate; JOA = Japanese Orthopaedic Association; NDI = Neck Disability Index; ROC = receiver operating characteristic; T1S = T1 slope; T1S-CL = T1S minus CL; VAS = visual analog scale.

OBJECTIVE

The C2 slope (C2S) is one of the parameters that can determine cervical sagittal alignment, but its clinical significance is relatively unexplored. This study aimed to evaluate the clinical significance of the C2S after multilevel cervical spine fusion.

METHODS

A total of 111 patients who underwent multilevel cervical spine fusion were included in this study. The C2S, cervical sagittal vertical axis (cSVA), C2–7 lordosis, and T1 slope (T1S) were measured in standing lateral cervical spine radiographs preoperatively and 2 years after the surgery. Clinical outcome measures were visual analog scale (VAS) neck and arm pain scores, Neck Disability Index (NDI), Japanese Orthopaedic Association (JOA) scale score, and patient-reported subjective improvement rate (IR) percentage. Statistical analysis was performed using a paired-samples t-test and Pearson’s correlation, and a receiver operating characteristic (ROC) curve to determine the cutoff values of C2S.

RESULTS

C2S demonstrated a significant correlation with the cSVA, C2–7 lordosis, T1S, and T1S minus cervical lordosis. C2S revealed a significant correlation with the JOA, neck pain VAS, and NDI scores at 2 years after surgery. Change in the C2S correlated with postoperative neck pain and NDI scores. ROC curves demonstrated the cutoff values of C2S as 18.8°, 22.25°, and 25.35°, according to a cSVA of 40 mm, severe disability expressed by NDI, and severe myelopathy, respectively.

CONCLUSIONS

C2S can be an additional cervical sagittal alignment parameter that can be a useful prognostic factor after multilevel cervical spine fusion.

In Brief

The authors evaluated the clinical significance of C2 slope (C2S) in patients who underwent multilevel cervical spine fusion. Increased C2S correlated with worse neck pain, Neck Disability Index, and Japanese Orthopaedic Association scale scores after surgery, and its cutoff values were determined. C2 slope may be a simple yet effective parameter that can be utilized to determine cervical sagittal alignment.

Cervical sagittal alignment is gaining attention as an important factor related to postoperative clinical outcomes.13 Cervical sagittal malalignment may cause severe impairment in maintaining an erect posture along with horizontal gaze, and compensatory mechanisms potentially lead to further pain and disability.4,5 Cervical alignment may also contribute to the pathogenesis of cervical myelopathy.6 Numerous studies have suggested various radiographic parameters to evaluate sagittal balance.4,7 The most commonly used parameter to define sagittal malalignment is the cervical sagittal vertical axis (cSVA), which is known to correlate with health-related quality of life.1 However, this parameter includes the lower cervical spine components, which can be easily obstructed on plain radiographs, especially in short-neck and muscular patients (Fig. 1).810

FIG. 1.
FIG. 1.

The lower cervical spine and T1 can be easily obstructed on plain radiographs, especially in short-neck and muscular patients.

The C2 slope (C2S) is a recently introduced and relatively unexplored parameter that can substitute for the T1 slope (T1S) minus cervical lordosis (T1S-CL) parameter and may correlate with health-related outcome measures.11 It uses a clearly visible landmark, C2, on lateral cervical radiographs. This study aimed to assess the association of C2S with established radiographic parameters used to define cervical sagittal alignment and with clinical outcomes in patients who underwent multiple levels of cervical spine fusion.

Methods

Patient Selection

After IRB approval from Yonsei University Gangnam Severance Hospital, patients diagnosed with severe cervical spondylotic myeloradiculopathy who required three or more levels of cervical spine fusion between 2014 and 2019 were retrospectively identified. Patients with 2 or more years of follow-up were included. Patients’ sex, age, follow-up duration, number of levels fused, BMI, smoking status, and osteoporosis status were reviewed. Trauma, tumor, and infection cases were excluded. All included patients had multilevel cord compression along with foraminal stenosis with significant disc height loss, resulting in interpedicular foraminal height narrowing. Foraminotomy increases the anteroposterior dimension of the foramen but not its height.12 Therefore, to manage these pathologies, patients had to undergo a staged combined anterior and posterior cervical spine fusion.

Radiographic Parameters

Neutral lateral plain radiographs of patients in the standing position were obtained. The following parameters were measured using the Centricity Web (Enterprise Web version 3.0, GE Healthcare) PACS: C2S, cSVA, C2–7 lordosis, T1S, and T1S-CL were measured preoperatively and 2 years after surgery. The C7 slope was measured in patients in whom T1 was obstructed on plain radiographs.9 The radiographic measurements were defined as follows: 1) C2S = the angle between the lower endplate of C2 and the horizontal plane;11 2) cSVA = the distance between the C2 plumb line and the superior posterior endplate of C7;13 3) C2–7 lordosis = the Cobb angle between the lower endplates of C2 and C7;14 and 4) T1S = the angle between the upper endplate of T1 and the horizontal plane (Fig. 2).15,16 Two independent observers (spine fellows, N.K. and J.S.) measured the parameters, and each observer repeated the measurements with 2-week intervals.

FIG. 2.
FIG. 2.

Pre- (left) and postoperative (right) radiographic measurements used in this study: C2S, T1S, cSVA, and C2–7 lordosis.

Clinical Outcome Measures

The following clinical outcome measures were obtained preoperatively and at the 2-year follow-up: visual analog scale (VAS) scores for neck and arm pain, Neck Disability Index (NDI),17 Japanese Orthopaedic Association (JOA) score,18 patient-reported subjective improvement rate (IR) percentage, and the EQ-5D. The total NDI score was converted into a percentage score to compensate for nondrivers. The EQ-5D profile was converted into a time trade-off value for analysis.19

Statistical Analysis

Demographics, radiographic parameters, and clinical outcome measurements are presented as means ± standard deviations or total numbers (percentages). Changes in the radiographic and clinical outcome parameters from the preoperative period to the 2-year postoperative period were compared using paired-samples t-tests. Intra- and interobserver reliability of radiographic parameters were assessed using the intraclass correlation coefficient. Pearson’s correlation was used to analyze correlations between C2S and conventional radiographic parameters and clinical outcomes. It was also used to analyze correlations between the postoperative changes in C2S with radiographic parameter changes and clinical outcomes. Receiver operating characteristic (ROC) curve analysis was performed, and the Youden index was calculated to determine the matching C2S cutoff values according to the established radiographic parameters and clinical outcome predictors. All statistical analyses were performed using IBM SPSS Statistics (version 25, IBM Corp.). Results were considered significant when the p value was < 0.05.

Results

A total of 133 patients diagnosed with cervical spondylotic myeloradiculopathy underwent surgery. Excluding patients with a follow-up less than 24 months (n = 22), 111 patients (74 men and 37 women) were included in this study. The mean patient age was 61.5 ± 10.8 years, and the average follow-up duration was 33.8 ± 13.9 months. BMI was 25.3 ± 3.2 kg/m2 on average; smoking status (84 nonsmokers, 16 past smokers, and 11 current smokers) and osteoporosis status (n = 15 with osteoporosis) were also reviewed. The average blood loss was 432.79 ± 271.24 ml, the mean surgery time was 317.43 ± 92.53 minutes, and patients had a mean of 1.40 ± 1.08 (range 0–5) comorbidities. A mean of 4.1 ± 0.7 (range 3–6) levels of staged, circumferential fusion were performed. Among these levels, a mean of 3.1 ± 0.6 (range 2–5) levels of anterior fusion and 4.1 ± 0.7 (range 3–6) levels of posterior fusion were combined. Good to excellent intra- and interobserver reliability for all radiographic measurements was observed.

Postoperative Changes in Radiographic and Clinical Outcome Parameters

Decreases in C2S (from 15.8° to 12.0°, p < 0.001) and T1S-CL (from 17.0° to 11.9°, p < 0.001) and increases in T1S (from 21.6° to 29.6°, p < 0.001) and C2–7 lordosis (from 4.5° to 17.8°, p < 0.001) were observed. An overall improvement in the clinical outcome parameters was observed after surgery (Table 1).

TABLE 1.

Changes in radiographic and clinical outcome parameters between the pre- and postoperative periods

ParameterPreop2 Yrs Postopp Value
C2S (°)15.81 ± 9.3212.02 ± 8.1<0.001
T1S (°)21.56 ± 7.9529.64 ± 7.73<0.001
cSVA (mm)22.64 ± 13.1824.45 ± 12.000.122
C2–7 lordosis (°)4.54 ± 11.5917.79 ± 8.94<0.001
T1S-CL (°)17.01 ± 9.3911.85 ± 8.31<0.001
Neck pain VAS score5.00 ± 2.420.20 ± 0.68<0.001
Arm pain VAS score4.50 ± 2.800.30 ± 1.01<0.001
JOA score11.86 ± 3.2115.82 ± 1.72<0.001
NDI (%)39.00 ± 17.6822.40 ± 14.58<0.001

Pre- and postoperative values given as mean ± standard deviation. Boldface type indicates statistical significance.

Correlations

Between C2S and Conventional Radiographic Parameters

C2S correlated with T1S (r = 0.350, p < 0.001 postoperatively), cSVA (r = 0.534, p < 0.001 preoperatively; and r = 0.404, p < 0.001 postoperatively), C2–7 lordosis (r = −0.711, p < 0.001 preoperatively; and r = −0.582, p < 0.001 postoperatively), and T1S-CL (r = 0.977, p < 0.001 preoperatively; and r = 0.951, p < 0.001 postoperatively; Table 2).

TABLE 2.

Correlation between radiographic parameters preoperatively and at the 2-year follow-up

VariableC2ST1ScSVAC2–7 LordosisT1S-CL
Preop
 C2S
  R value10.1180.5340.7110.977
  p value0.219<0.001<0.001<0.001
 T1S
  R value10.2160.5930.114
  p value0.023<0.0010.232
 cSVA
  R value10.2400.478
  p value0.011<0.001
 C2–7 lordosis
  R value10.732
  p value<0.001
2-yr follow-up
 C2S
  R value10.3500.4040.5820.951
  p value<0.001<0.001<0.001<0.001
 T1S
  R value10.4700.5110.380
  p value<0.001<0.001<0.001
 cSVA
  R value10.0820.349
  p value0.394<0.001
 C2–7 lordosis
  R value10.600
  p value<0.001

Boldface type indicates statistical significance.

Between Radiographic Parameters and Clinical Outcome Measures

C2S positively correlated with neck pain (r = 0.232, p = 0.016) and NDI (r = 0.325, p = 0.001) scores at the postoperative 2-year follow-up. C2S negatively correlated with JOA score (r = −0.306, p = 0.002) at the postoperative 2-year follow-up. T1S-CL also demonstrated a significant correlation with neck pain (r = 0.244, p = 0.011), JOA (r = −0.220, p = 0.026), and NDI (r = 0.273, p = 0.006) scores at the 2-year follow-up. The cSVA significantly correlated with JOA (r = −0.367, p < 0.001) and NDI (r = 0.250, p = 0.011) scores. C2–7 lordosis did not significantly correlate with the clinical outcome measures (Table 3).

TABLE 3.

Correlation between radiographic parameters and clinical outcome measures preoperatively and at the 2-year follow-up

ParameterC2ST1ScSVAC2–7 LordosisT1S-CL
R Valuep ValueR Valuep ValueR Valuep ValueR Valuep ValueR Valuep Value
Preop
 Neck pain VAS score (n = 111)0.0540.575−0.1370.151−0.0400.680−0.1330.1630.0490.613
 Arm pain VAS score (n = 111)−0.0710.462−0.0650.497−0.1000.2960.0410.880−0.0730.446
 JOA score (n = 111)0.0080.9300.2190.021−0.1810.057−0.1690.0770.0230.814
 NDI (n = 111)0.0240.7990.0480.620−0.0810.3960.0200.8370.0160.868
2-yr follow-up
 IR (n = 105)−0.1710.082−0.0420.669−0.1270.1950.1220.216−0.1700.083
 Neck pain VAS score (n = 107)0.2320.0160.2220.0220.1170.230−0.0340.7260.2440.011
 Arm pain VAS score (n = 106)0.1010.3020.1310.1810.1320.1780.0060.9490.1190.226
 JOA score (n = 102)0.3060.0020.2130.0320.367<0.0010.0200.8400.2200.026
 NDI (n = 102)0.3250.0010.1450.1470.2500.011−0.1280.1990.2730.006
 EQ-5D index (n = 65)−0.0570.650−0.0560.655−0.2390.0550.0000.999−0.0440.725
 EQ-5D VAS score (n = 65)−0.1270.3150.0430.731−0.1830.1460.1500.234−0.1190.346

Boldface type indicates statistical significance.

Between Changes in Radiographic Parameters

Change in the C2S positively correlated with the changes in cSVA (r = 0.604, p < 0.001) and T1S-CL (r = 0.940, p < 0.001). Change in the C2S negatively correlated with the change in C2–7 lordosis (r = −0.733, p < 0.001; Table 4).

TABLE 4.

Correlation between changes in radiographic parameters

ParameterΔC2SΔT1SΔcSVAΔC2–7 LordosisΔT1S-CL
ΔC2S
 R value1−0.0270.6040.7330.940
 p value0.775<0.001<0.001<0.001
ΔT1S
 R value10.1230.648−0.015
 p value0.199<0.0010.872
ΔcSVA
 R value10.3430.553
 p value0.011<0.001
ΔC2–7 lordosis
 R value10.771
 p value<0.001

Δ = change from pre- to postoperatively.

Boldface type indicates statistical significance.

Between the Change in Radiographic Parameters and Clinical Outcome Measures

Change in the C2S negatively correlated with neck pain (r = −0.192, p = 0.047) and NDI (r = −0.279, p = 0.004) scores at the postoperative 2-year follow-up (Table 5).

TABLE 5.

Correlation between change in radiographic parameters and clinical outcome measures at the 2-year follow-up

ParameterΔC2SΔT1SΔcSVAΔC2–7 LordosisΔT1S-CL
R Valuep ValueR Valuep ValueR Valuep ValueR Valuep ValueR Valuep Value
IR (n = 105)0.1850.0590.0830.4020.1440.1420.0900.3590.1870.056
Neck pain VAS score (n = 107)0.1920.047−0.0670.4920.2000.0390.0790.420−0.1590.101
Arm pain VAS score (n = 106)−0.0870.3770.0180.857−0.1760.0710.0590.549−0.0620.527
JOA score (n = 102)0.1340.1800.1190.2330.1450.1470.0600.5480.0200.839
NDI (n = 102)0.2790.004−0.0250.8050.2510.0110.1580.1140.2240.024
EQ-5D index (n = 65)0.0240.849−0.1280.3110.0760.549−0.1020.4180.0300.811
EQ-5D VAS score (n = 65)0.1260.3170.2750.0270.0570.6530.2630.0340.1210.336

Boldface type indicates statistical significance.

C2S Cutoff Values as a Potential Predictor of Postoperative Sagittal Alignment

C2S had cutoff points of 18.8° (Fig. 3A), 22.25° (Fig. 3B), and 25.35° (Fig. 3C) according to a cSVA of 40 mm (area under the curve [AUC] 0.746, sensitivity 0.615, specificity 0.898), severe disability expressed by NDI (NDI ≥ 50%; AUC 0.973, sensitivity 1, specificity 0.960), and severe myelopathy (JOA score < 9; AUC 0.970, sensitivity 1, specificity 0.970), respectively.

FIG. 3.
FIG. 3.

ROC analysis to determine matching C2S cutoff values according to established radiographic parameters and clinical outcome predictors. A: C2S cutoff value of 18.8° according to a cSVA of 40 mm (AUC 0.746, sensitivity 0.615, specificity 0.898). B: C2S cutoff value of 22.25° according to severe disability by NDI (AUC 0.973, sensitivity 1, specificity 0.960). C: C2S cutoff value of 25.35° according to severe myelopathy (AUC 0.970, sensitivity 1, specificity 0.970).

Discussion

C2S demonstrated a significant correlation with the conventional radiographic parameters used to define cervical sagittal alignment in this study. C2S negatively correlated with C2–7 lordosis and positively correlated with cSVA and T1S. As expected, because C2S is a mathematical approximation of T1S-CL, the strongest correlation was observed between C2S and T1S-CL. These correlations can be easily explained using the formula from which C2S is deduced from T1S-CL.11 Cervical malalignment can be defined as an imbalance between cervical lordosis (CL) and upper thoracic kyphosis. When CL is not sufficient for T1S, C2 tilts anteriorly, increasing the angle of C2S.20 Based on this result, C2S can safely substitute for the existing radiographic parameters, especially T1S-CL, because C2 is easier to visualize on plain cervical radiographs than T1 and the lower cervical spine, especially in short-neck or muscular patients.8,9 Moreover, the C2S can help minimize interobserver errors because only one measurement is required, in contrast with T1S-CL, which requires three measurements.2,11

C2S is also potentially useful in predicting postoperative clinical outcomes in patients with multilevel fusion based on the results of this study. Postoperative C2S and its degree of change after surgery correlated with the postoperative neck pain VAS and NDI scores. In patients with cervical malalignment, the neck musculature may become fatigued, and the cervical spine becomes kyphotic. Compensatory mechanisms to maintain an erect posture and horizontal gaze lead to pain and disability.4,5 This potentially explains the correlations of C2S with neck pain and the NDI. This result is similar to that of Tang et al., who demonstrated that malalignment was associated with worsened NDI and the 36-Item Short-Form Health Survey scores.1 The correlation between the JOA score and alignment parameters in this study can be explained by the pathophysiology of cervical spondylotic myelopathy. Degenerative changes in the cervical spine lead to cord compression and loss of normal alignment.2123 This malalignment results in the draping of the spinal cord against the vertebral bodies and anterior pathology, which increases cord tension and intramedullary pressure, flattens the cord, and reduces blood supply, eventually resulting in neurological compromise.6,2426 Therefore, a negative correlation was observed between C2S and postoperative JOA scores.

Notably, the study demonstrated that postoperative CL itself did not correlate with the clinical outcomes, whereas the alignment parameters such as C2S, T1S-CL, and cSVA did. Although the cohort did not include severely kyphotic patients due to surgical treatment, this finding is similar to that obtained in a study by Smith et al., which suggested that sagittal alignment, as described by the cSVA, and not just kyphosis is a determining factor for myelopathy severity.27 This result is also consistent with previous studies, whose findings suggest that cervical segmental kyphosis itself may be a normal variant.13,28,29 Therefore, it can be hypothesized that clinical outcomes in cervical spondylotic myeloradiculopathy patients undergoing multiple levels of fusion may be better predicted by sagittal alignment parameters such as C2S, T1S-CL, and cSVA.

A recent study by Divi et al. did not identify any correlation of C2S and cSVA with clinical outcome parameters.30 However, in their study, T1S-CL demonstrated some correlation with postoperative outcomes. Because C2S is an approximation of T1S-CL, further studies are required to corroborate this result. The difference in results between these studies may be due to patient cohort differences. Patients underwent 1- to 3-level anterior cervical discectomy and fusion in the study by Divi et al. In contrast, three or more levels of anterior-posterior combined fusion were performed in this study. The difference in the number of levels fused and different approaches might have been the reason underlying the dissimilar results.

Although data on "normal" C2S are scarce, Iyer et al. reported a mean T1S of 26.1° ± 9° and CL of −12.2° ± 13.6°, resulting in a T1S-CL value of 13.9° in a cohort of normal asymptomatic adults.31 Staub et al. reported a normative T1S-CL value of 16.5°.32 Because C2S is an approximation of T1S-CL, the normative C2S value can be assumed to be near these values.11 Other studies have indicated C2S to assume a value near 15° for a comfortable horizontal gaze because occiput-to-C2 lordosis is 30° in asymptomatic individuals in a standing posture.4,33 ROC curve analysis in this study demonstrated a C2S of 18.8° to match a cSVA of 40 mm postoperatively. This value was relatively smaller than the cutoff value of 36° suggested by Protopsaltis et al.11 This difference might have been the result of different patient cohorts, which in this study comprised patients with cervical spondylotic myeloradiculopathy, and in the other study adults with cervical deformity. Severe disability expressed by NDI matched a C2S of 22.25°, and severe myelopathy was found to match a C2S of 25.35°. Hyun et al. reported a T1S-CL value of 22.2° as the cutoff value for predicting severe NDI, and it was similar to the cutoff value in this study.34 In an extension of these data, these values might be used as a goal for surgical planning, similar to pelvic incidence minus lumbar lordosis in lumbar surgeries.

Strengths and Limitations

To the best of the authors’ knowledge, this is the first study to assess the association between C2S and its changes after surgical treatment using clinical outcome parameters over a minimum 2-year follow-up. The strength of this study is that it enrolled a large number of patients with a standardized diagnosis and treatment protocols by a single experienced surgeon. Through this standardized treatment protocol, the degree of stenosis decompression would not have differed greatly among the included patients. This standardization would make this patient population a good cohort for studying the correlation between radiographic changes and clinical outcomes. In this study, the cervical spondylotic myeloradiculopathy patient cohort underwent combined anterior-posterior fusion, through which both neural decompression and sagittal alignment correction could be achieved.35 This process rendered the cohort ideal for studying the correlation between alignment parameters and clinical outcomes. Furthermore, this study can provide a foundation for further research on ideal alignment targets. The limitations of this study include its retrospective design and single-center data collection. The retrospective nature of the study limited the acquisition of EQ-5D scores in some patients during their preoperative and 2-year follow-up periods. Second, whole-spine standing radiographs were not used in this study due to their availability and because of the cervical spine visibility in some patients. However, cervical radiographs were obtained in the same standing position, and this would have minimized errors when evaluating sagittal parameters. Moving forward, larger prospective studies will be required to further validate C2S and other sagittal alignment parameters as predictors of clinical outcome.

Conclusions

C2S can be an additional cervical sagittal alignment parameter that can be a useful prognostic factor after multilevel cervical spine fusion.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Suk, N Kim. Acquisition of data: Suk, N Kim, Seo, Ju. Analysis and interpretation of data: Suk, N Kim, Kwon, BH Lee, Moon, HS Kim, HM Lee. Drafting the article: N Kim. Critically revising the article: Suk, N Kim, Kwon, BH Lee, Moon, HS Kim, HM Lee. Reviewed submitted version of manuscript: Suk, N Kim, Kwon, Seo, Ju, BH Lee. Approved the final version of the manuscript on behalf of all authors: Suk. Statistical analysis: N Kim. Administrative/technical/material support: Suk, Seo, Ju. Study supervision: Suk, N Kim, Kwon, Moon, HS Kim, HM Lee.

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  • 11

    Protopsaltis TS, Ramchandran S, Tishelman JC, et al. The importance of C2 slope, a singular marker of cervical deformity, correlates with patient-reported outcomes. Spine (Phila Pa 1976). 2020;45(3):184192.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Joaquim AF, Lee NJ, Riew KD. Circumferential operations of the cervical spine. Neurospine. 2021;18(1):5566.

  • 13

    Hardacker JW, Shuford RF, Capicotto PN, Pryor PW. Radiographic standing cervical segmental alignment in adult volunteers without neck symptoms. Spine (Phila Pa 1976). 1997;22(13):14721480.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Cobb JR. Outlines for the study of scoliosis measurements from spinal roentgenograms. Phys Ther. 1948;59:764765.

  • 15

    Knott PT, Mardjetko SM, Techy F. The use of the T1 sagittal angle in predicting overall sagittal balance of the spine. Spine J. 2010;10(11):994998.

  • 16

    Lee SH, Kim KT, Seo EM, Suk KS, Kwack YH, Son ES. The influence of thoracic inlet alignment on the craniocervical sagittal balance in asymptomatic adults. J Spinal Disord Tech. 2012;25(2):E41E47.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Vernon H. The Neck Disability Index: state-of-the-art, 1991-2008. J Manipulative Physiol Ther. 2008;31(7):491502.

  • 18

    Yonenobu K, Abumi K, Nagata K, Taketomi E, Ueyama K. Interobserver and intraobserver reliability of the Japanese Orthopaedic Association scoring system for evaluation of cervical compression myelopathy. Spine (Phila Pa 1976). 2001;26(17):18901895.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee YK, Nam HS, Chuang LH, et al. South Korean time trade-off values for EQ-5D health states: modeling with observed values for 101 health states. Value Health. 2009;12(8):11871193.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lee SH, Son ES, Seo EM, Suk KS, Kim KT. Factors determining cervical spine sagittal balance in asymptomatic adults: correlation with spinopelvic balance and thoracic inlet alignment. Spine J. 2015;15(4):705712.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Iyer A, Azad TD, Tharin S. Cervical spondylotic myelopathy. Clin Spine Surg. 2016;29(10):408414.

  • 22

    Matz PG, Anderson PA, Holly LT, et al. The natural history of cervical spondylotic myelopathy. J Neurosurg Spine. 2009;11(2):104111.

  • 23

    Choi SH, Kang CN. Degenerative cervical myelopathy: pathophysiology and current treatment strategies. Asian Spine J. 2020;14(5):710720.

  • 24

    Shimizu K, Nakamura M, Nishikawa Y, Hijikata S, Chiba K, Toyama Y. Spinal kyphosis causes demyelination and neuronal loss in the spinal cord: a new model of kyphotic deformity using juvenile Japanese small game fowls. Spine (Phila Pa 1976). 2005;30(21):23882392.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Chavanne A, Pettigrew DB, Holtz JR, Dollin N, Kuntz C IV. Spinal cord intramedullary pressure in cervical kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976). 2011;36(20):16191626.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Farley CW, Curt BA, Pettigrew DB, Holtz JR, Dollin N, Kuntz C IV. Spinal cord intramedullary pressure in thoracic kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976). 2012;37(4):E224E230.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Smith JS, Lafage V, Ryan DJ, et al. Association of myelopathy scores with cervical sagittal balance and normalized spinal cord volume: analysis of 56 preoperative cases from the AOSpine North America Myelopathy study. Spine (Phila Pa 1976). 2013;38(22 suppl 1):S161S170.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Le Huec JC, Demezon H, Aunoble S. Sagittal parameters of global cervical balance using EOS imaging: normative values from a prospective cohort of asymptomatic volunteers. Eur Spine J. 2015;24(1):6371.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Kuntz C IV, Levin LS, Ondra SL, Shaffrey CI, Morgan CJ. Neutral upright sagittal spinal alignment from the occiput to the pelvis in asymptomatic adults: a review and resynthesis of the literature. J Neurosurg Spine. 2007;6(2):104112.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Divi SN, Bronson WH, Canseco JA, et al. How do C2 tilt and C2 slope correlate with patient reported outcomes in patients after anterior cervical discectomy and fusion? Spine J. 2021;21(4):578585.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Iyer S, Lenke LG, Nemani VM, et al. Variations in sagittal alignment parameters based on age: a prospective study of asymptomatic volunteers using full-body radiographs. Spine (Phila Pa 1976). 2016;41(23):18261836.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Staub BN, Lafage R, Kim HJ, et al. Cervical mismatch: the normative value of T1 slope minus cervical lordosis and its ability to predict ideal cervical lordosis. J Neurosurg Spine. 2018;30(1):3137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Gore DR, Sepic SB, Gardner GM. Roentgenographic findings of the cervical spine in asymptomatic people. Spine (Phila Pa 1976). 1986;11(6):521524.

  • 34

    Hyun SJ, Kim KJ, Jahng TA, Kim HJ. Clinical impact of T1 slope minus cervical lordosis after multilevel posterior cervical fusion surgery: a minimum 2-year follow up data. Spine (Phila Pa 1976). 2017;42(24):18591864.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Song KJ, Song JS, Kim DY, Shim DG, Lee KB. Efficacy of combined anteroposterior fusion with no plate versus anterior fusion alone with cage and plate for multilevel degenerative cervical disease. Spine J. 2014;14(4):598603.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Illustration from Beck et al. (pp 147–152). © Department of Neurosurgery, Freiburg Medical Center; published with permission.

  • FIG. 1.

    The lower cervical spine and T1 can be easily obstructed on plain radiographs, especially in short-neck and muscular patients.

  • FIG. 2.

    Pre- (left) and postoperative (right) radiographic measurements used in this study: C2S, T1S, cSVA, and C2–7 lordosis.

  • FIG. 3.

    ROC analysis to determine matching C2S cutoff values according to established radiographic parameters and clinical outcome predictors. A: C2S cutoff value of 18.8° according to a cSVA of 40 mm (AUC 0.746, sensitivity 0.615, specificity 0.898). B: C2S cutoff value of 22.25° according to severe disability by NDI (AUC 0.973, sensitivity 1, specificity 0.960). C: C2S cutoff value of 25.35° according to severe myelopathy (AUC 0.970, sensitivity 1, specificity 0.970).

  • 1

    Tang JA, Scheer JK, Smith JS, et al. The impact of standing regional cervical sagittal alignment on outcomes in posterior cervical fusion surgery. Neurosurgery. 2012;71(3):662669.

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  • 2

    Iyer S, Nemani VM, Nguyen J, et al. Impact of cervical sagittal alignment parameters on neck disability. Spine (Phila Pa 1976). 2016;41(5):371377.

  • 3

    Villavicencio AT, Babuska JM, Ashton A, et al. Prospective, randomized, double-blind clinical study evaluating the correlation of clinical outcomes and cervical sagittal alignment. Neurosurgery. 2011;68(5):13091316.

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  • 4

    Scheer JK, Tang JA, Smith JS, et al. Cervical spine alignment, sagittal deformity, and clinical implications: a review. J Neurosurg Spine. 2013;19(2):141159.

  • 5

    Park MS, Moon SH, Lee HM, et al. The effect of age on cervical sagittal alignment: normative data on 100 asymptomatic subjects. Spine (Phila Pa 1976). 2013;38(8):E458E463.

    • Crossref
    • PubMed
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  • 6

    Ames CP, Blondel B, Scheer JK, et al. Cervical radiographical alignment: comprehensive assessment techniques and potential importance in cervical myelopathy. Spine (Phila Pa 1976). 2013;38(22 suppl 1):S149S160.

    • Crossref
    • PubMed
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  • 7

    Lee SH, Hyun SJ, Jain A. Cervical sagittal alignment: literature review and future directions. Neurospine. 2020;17(3):478496.

  • 8

    Zhang J, Buser Z, Abedi A, Dong X, Wang JC. Can C2-6 Cobb angle replace C2-7 Cobb angle? An analysis of cervical kinetic magnetic resonance images and x-rays. Spine (Phila Pa 1976). 2019;44(4):240245.

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  • 9

    Tamai K, Buser Z, Paholpak P, Sessumpun K, Nakamura H, Wang JC. Can C7 slope substitute the T1 slope? An analysis using cervical radiographs and kinematic MRIs. Spine (Phila Pa 1976). 2018;43(7):520525.

    • Crossref
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  • 10

    Marques C, Granström E, MacDowall A, Moreira NC, Skeppholm M, Olerud C. Accuracy and reliability of x-ray measurements in the cervical spine. Asian Spine J. 2020;14(2):169176.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Protopsaltis TS, Ramchandran S, Tishelman JC, et al. The importance of C2 slope, a singular marker of cervical deformity, correlates with patient-reported outcomes. Spine (Phila Pa 1976). 2020;45(3):184192.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Joaquim AF, Lee NJ, Riew KD. Circumferential operations of the cervical spine. Neurospine. 2021;18(1):5566.

  • 13

    Hardacker JW, Shuford RF, Capicotto PN, Pryor PW. Radiographic standing cervical segmental alignment in adult volunteers without neck symptoms. Spine (Phila Pa 1976). 1997;22(13):14721480.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Cobb JR. Outlines for the study of scoliosis measurements from spinal roentgenograms. Phys Ther. 1948;59:764765.

  • 15

    Knott PT, Mardjetko SM, Techy F. The use of the T1 sagittal angle in predicting overall sagittal balance of the spine. Spine J. 2010;10(11):994998.

  • 16

    Lee SH, Kim KT, Seo EM, Suk KS, Kwack YH, Son ES. The influence of thoracic inlet alignment on the craniocervical sagittal balance in asymptomatic adults. J Spinal Disord Tech. 2012;25(2):E41E47.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Vernon H. The Neck Disability Index: state-of-the-art, 1991-2008. J Manipulative Physiol Ther. 2008;31(7):491502.

  • 18

    Yonenobu K, Abumi K, Nagata K, Taketomi E, Ueyama K. Interobserver and intraobserver reliability of the Japanese Orthopaedic Association scoring system for evaluation of cervical compression myelopathy. Spine (Phila Pa 1976). 2001;26(17):18901895.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee YK, Nam HS, Chuang LH, et al. South Korean time trade-off values for EQ-5D health states: modeling with observed values for 101 health states. Value Health. 2009;12(8):11871193.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Lee SH, Son ES, Seo EM, Suk KS, Kim KT. Factors determining cervical spine sagittal balance in asymptomatic adults: correlation with spinopelvic balance and thoracic inlet alignment. Spine J. 2015;15(4):705712.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Iyer A, Azad TD, Tharin S. Cervical spondylotic myelopathy. Clin Spine Surg. 2016;29(10):408414.

  • 22

    Matz PG, Anderson PA, Holly LT, et al. The natural history of cervical spondylotic myelopathy. J Neurosurg Spine. 2009;11(2):104111.

  • 23

    Choi SH, Kang CN. Degenerative cervical myelopathy: pathophysiology and current treatment strategies. Asian Spine J. 2020;14(5):710720.

  • 24

    Shimizu K, Nakamura M, Nishikawa Y, Hijikata S, Chiba K, Toyama Y. Spinal kyphosis causes demyelination and neuronal loss in the spinal cord: a new model of kyphotic deformity using juvenile Japanese small game fowls. Spine (Phila Pa 1976). 2005;30(21):23882392.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Chavanne A, Pettigrew DB, Holtz JR, Dollin N, Kuntz C IV. Spinal cord intramedullary pressure in cervical kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976). 2011;36(20):16191626.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Farley CW, Curt BA, Pettigrew DB, Holtz JR, Dollin N, Kuntz C IV. Spinal cord intramedullary pressure in thoracic kyphotic deformity: a cadaveric study. Spine (Phila Pa 1976). 2012;37(4):E224E230.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Smith JS, Lafage V, Ryan DJ, et al. Association of myelopathy scores with cervical sagittal balance and normalized spinal cord volume: analysis of 56 preoperative cases from the AOSpine North America Myelopathy study. Spine (Phila Pa 1976). 2013;38(22 suppl 1):S161S170.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Le Huec JC, Demezon H, Aunoble S. Sagittal parameters of global cervical balance using EOS imaging: normative values from a prospective cohort of asymptomatic volunteers. Eur Spine J. 2015;24(1):6371.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Kuntz C IV, Levin LS, Ondra SL, Shaffrey CI, Morgan CJ. Neutral upright sagittal spinal alignment from the occiput to the pelvis in asymptomatic adults: a review and resynthesis of the literature. J Neurosurg Spine. 2007;6(2):104112.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Divi SN, Bronson WH, Canseco JA, et al. How do C2 tilt and C2 slope correlate with patient reported outcomes in patients after anterior cervical discectomy and fusion? Spine J. 2021;21(4):578585.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Iyer S, Lenke LG, Nemani VM, et al. Variations in sagittal alignment parameters based on age: a prospective study of asymptomatic volunteers using full-body radiographs. Spine (Phila Pa 1976). 2016;41(23):18261836.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Staub BN, Lafage R, Kim HJ, et al. Cervical mismatch: the normative value of T1 slope minus cervical lordosis and its ability to predict ideal cervical lordosis. J Neurosurg Spine. 2018;30(1):3137.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Gore DR, Sepic SB, Gardner GM. Roentgenographic findings of the cervical spine in asymptomatic people. Spine (Phila Pa 1976). 1986;11(6):521524.

  • 34

    Hyun SJ, Kim KJ, Jahng TA, Kim HJ. Clinical impact of T1 slope minus cervical lordosis after multilevel posterior cervical fusion surgery: a minimum 2-year follow up data. Spine (Phila Pa 1976). 2017;42(24):18591864.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Song KJ, Song JS, Kim DY, Shim DG, Lee KB. Efficacy of combined anteroposterior fusion with no plate versus anterior fusion alone with cage and plate for multilevel degenerative cervical disease. Spine J. 2014;14(4):598603.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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