Risk Factors for “Adjacent-Level Ossification Development” Other Than Short Plate-to-Disc Distance and Clinical Implications for Adjacent-Segment Pathology

Article information

Neurospine. 2025;22(1):194-201

Publication date (electronic) : 2025 March 31

doi : https://doi.org/10.14245/ns.2448832.416

Department of Orthopaedic Surgery, The Johns Hopkins University, Baltimore, MD, USA

Corresponding Author Sang Hun Lee Department of Orthopaedic Surgery, The Johns Hopkins University, 601 North Caroline Street JHOC 5241, Baltimore, MD 21287, USA Email: slee439@jhmi.edu

Received 2024 August 13; Revised 2024 November 14; Accepted 2024 November 15.

Abstract

Purpose

To identify factors associated with adjacent-level ossification development (ALOD) after anterior cervical discectomy and fusion (ACDF) and associated clinical outcomes.

Methods

We retrospectively reviewed records of 140 adults who underwent primary ACDF for degenerative disc disease. We compared patients with and without ALOD after ACDF. Radiographic measurements and factors associated with ALOD were assessed preoperatively and at minimum 24-month follow-up. Clinical outcomes were incidence of clinical adjacent-segment pathologies (CASP), revision surgery, and patient-reported outcomes.

Results

Factors associated with both cranial and caudal ALOD were short plate-to-disc distance (PDD), adjacent-segment kyphosis, hyperlordotic ACDF causing junctional segment kyphosis, and preoperative ossification of the anterior longitudinal ligament (OALL). Mean final adjacent-segment range of motion (ROM) was less in those with cranial ALOD (6.9°±2.8°) than in those without cranial ALOD (12°±4.2°) (p<0.01). Mean final adjacent-segment ROM was also less in those with caudal ALOD (5.5°±2.4º) than in those without caudal ALOD (8.2º±3.7º) (p<0.01). The incidence of CASP-required surgery was higher in those with caudal ALOD (p=0.02) but no different in those with cranial ALOD (p=0.69) compared with those without ALOD.

Conclusion

Factors associated with ALOD were a kyphotic segment adjacent to ACDF, hyperlordotic fusion, preoperative OALL, and short PDD. ALOD was associated with less segmental ROM and, for those with caudal but not cranial ALOD, higher incidence of revision surgery for CASP.

Keywords: Cervical vertebrae; Diskectomy; Longitudinal ligaments; Osteogenesis; Spinal fusion

INTRODUCTION

Adjacent-level ossification development (ALOD) refers to heterotrophic ossification occurring at the cranial or caudal spinal segments adjacent to fused segments of the cervical spine [1-4]. ALOD is graded in terms of severity, with grade 0 representing no disease and grade 3 representing complete bridging of bone across the disc space [3].

Even before the first description of ALOD in 2005 [3], a similar ossification phenomenon was reported as “anterior or posterior osteophyte formation” or “late degenerative changes at the disc levels adjacent to the fused area.” [5-7] However, the initial studies included both adjacent-segment degeneration or radiographic adjacent-segment pathology and the current concept of ALOD. Several studies have found that anterior cervical discectomy and fusion (ACDF) using a low-profile anterior cervical fusion device was associated with a lower incidence of ALOD compared with conventional ACDF using an anterior cervical plate [8-11]. Studies have suggested that a surgical technique using the shortest plate and oblique screw trajectories could lower the incidence ALOD [2,12].

Incidence of ALOD after ACDF has been shown to range from 41%–64% [1], with a likelihood of progression during the initial 24 months postoperatively [1-4]. Some risk factors for ALOD have been described. The use of anterior cervical plate and short plate-to-disc distance (PDD) to the adjacent segments are associated with ALOD [1-4]. Yang et al. [13] reported that a longer PDD could prevent ALOD but did not change the incidence of symptomatic and asymptomatic adjacent-segment degeneration in their cohort. Clinical adjacent-segment pathologies (CASP) may also be associated with ALOD after ACDF. However, few studies have investigated other risk factors and the clinical implications of ALOD, leaving a gap in our clinical understanding of the condition.

To our knowledge, no studies have reported on the clinical implications of ALOD, such as patient-reported outcomes (PROs), range of motion (ROM), or the incidence of reoperation. In this retrospective study, we sought to identify (1) risk factors for ALOD after ACDF and (2) clinical outcomes associated with ALOD.

MATERIALS AND METHODS

This study was approved by the Institutional Review Board (IRB) of Johns Hopkins University (IRB00135145) and participants provided informed consent for this study.

1. Patient Sample

We retrospectively analyzed prospectively collected data for patients who had undergone primary ACDF using an anterior cervical plate and screw for the treatment of degenerative disc disease between 2005 and 2014 at our United States academic tertiary care hospital. We included patients who (1) were aged 18 years or older at the time of ACDF; (2) had at least 24 months of clinical follow-up; and (3) had complete data on radiographic and clinical outcomes.

2. Radiographic Evaluation and Defining ALOD

Standard lateral and anteroposterior radiographs of the cervical spine were taken preoperatively, 3–6 weeks after surgery, and at the final follow-up visit. ALOD was assessed using previously described criteria to determine the severity the disease [3]: grade 0, no demonstrable ALOD; grade 1, ALOD covering < 50% of the disc space; grade 2, ALOD covering ≥ 50% of the disc space; grade 3, ALOD with complete bridging across the disc space. Patients were then categorized into the ALOD group (grade 2 or 3) or the non-ALOD group (grade 0 or 1) (Fig. 1). The cranial and caudal ends of the fusion segment were analyzed separately. We excluded radiographs that did not enable adequate visualization of the caudal end of the fusion segment.

Fig. 1.

Serial lateral radiographs taken before (A), immediately after (B), and 38 months after (C) surgery for an 87-year-old man. Images show lordosis of the upper adjacent segment and no evidence of adjacent-level ossification development or clinical adjacent-segment pathologies even with 0 mm of plate-to-disc distance (arrows, B, C).

3. Radiographic Parameters

Radiographic parameters assessed were fusion segment angle (between the upper endplate [UEP] of the cranial vertebra and the lower endplate [LEP] of the caudal vertebra), adjacent-segment angles (cranial adjacent angle measured between the UEP of the upper adjacent vertebra and the UEP of the fusion level; caudal adjacent angle measured between the LEP of the fusion level and the LEP of the caudal adjacent vertebra); C2–7 angle (between the LEP of C2 and the LEP of C7); C0–2 angle (between the LEP of C2 and the foramen magnum line [clivus to posterior foramen magnum]); C2–7 sagittal vertical axis (distance between a vertical line passing through the center of the dens and a vertical line passing through the posterosuperior corner of C7). ROM was assessed as the difference in angles between the flexion and extension radiographs. Negative values indicate kyphosis. Radiographic fusion was determined by evaluating lateral flexion-extension radiographs.

4. Radiographic and Clinical Characteristics

Radiographic and clinical characteristics of interest (potential predictors of ALOD) were a short PDD (< 3 mm), the presence of preoperative ossification of the anterior longitudinal ligament (OALL), the presence of upper-segment kyphosis, hyperlordotic fusion, number of vertebral levels fused, patient age, sex, and the measured radiographic parameters. A hyperlordotic fusion was defined when the fused segment became lordotic with associated new-onset adjacent-segment kyphosis on postoperative radiographs.

5. Outcomes

Outcomes assessed were the incidence of CASP, CASP-required surgery, visual analogue scale (VAS) scores for neck pain and arm pain, and the physical component score (PCS) of the 12-item Short Form health survey (SF-12). CASP was defined by the development of radiculopathy and/or myelopathy symptoms during the follow-up period, prompting additional imaging studies [14]. We did not include temporary symptoms that did not prompt imaging studies.

6. Reliability

To test inter- and intraobserver reliabilities, 2 authors measured the C2–7 angle at the immediate postoperative and final follow-up points in 30 randomly selected cases, with measurements repeated 2 weeks apart. The inter- and intraobserver intraclass correlation coefficients (ICCs) were determined using the mean measurements of each observer.

7. Statistical Analysis

Means and standard deviations or ranges are used to describe continuous variables. Student t-tests were used to compare the means of continuous variables between groups. Chi-square tests were used to compare the distribution of categorical variables between groups. Statistical analysis was performed using SPSS ver. 17.0 (SPSS Inc., Chicago, IL, USA).

RESULTS

1. Patient Characteristics

Of 425 patients who underwent ACDF during the study period, we excluded 245 who had less than 24 months of follow-up, and 40 who had incomplete clinical or radiographic data. The remaining 140 patients (78 women; mean age, 55 years [range, 23–87 years]) were enrolled in the study. Mean duration of follow-up was 48 months (range, 24–140 months).

Of the 140 patients, the primary indication for ACDF was radiculopathy in 73 (52%), myelopathy in 36 (26%), and concomitant radiculopathy and myelopathy in 31 (22%). The mean number of levels fused was 2.1 (range, 1–3) segments. ACDF was 1-level in 30 patients, 2-level in 61 patients, and 3-level in 49 patients. The following 3 types of anterior cervical plate were used: Cervical Spine Locking Plate (DePuy Synthes, Warsaw, IN, USA) in 75 patients (48 developed cranial ALOD, and 37 developed caudal ALOD); Skyline Cervical Arthrodesis plate (DePuy Synthes) in 47 patients (13 developed cranial ALOD and 7 developed caudal ALOD); and MaxAn Anterior Cervical plate (Biomet Spine, Broomfield, CO, USA) in 18 patients (3 developed cranial ALOD). Fixed-angle screws were used for plate fixation. Six patients had pseudarthroses, all of which were single-level nonunions diagnosed using flexion-extension radiographs. One patient had C4–5 nonunion after C4–7 ACDF; 2 patients had C6–7 nonunion after C5–7 ACDF; and 3 patients had C6–7 nonunion after C4–7 ACDF. No patients had ALOD.

We excluded 20 patients from the analysis of caudal ALOD because their segments caudal to the ACDF are not clearly visible on radiographs. Overall, ALOD developed at the cranial segment in 64 of 140 patients (46%) (at C2–3 in 5 patients, C3–4 in 28 patients, C4–5 in 30 patients, and C5–6 in 1 patient) and at the caudal segment in 44 of 120 patients (37%) (at C5–6 in 2 patients, C6–7 in 21 patients, and C7–T1 in 21 patients) (Table 1). CASP-required imaging studies occurred in the cranial segment in 49 of 140 patients (35%) and in the caudal segment in 39 of 120 patients (32.5%). CASP-required revision surgery occurred in 25 patients (18%). Of the 25 patients, 15 patients (60%) were for cranial adjacent-segment, 8 (32%) were for caudal adjacent-segment, and 2 (1%) were for both adjacent segments (Table 1).

Table 1.

Clinical parameters for the caudal and cephalad segments analyzed in patients who underwent anterior cervical discectomy and fusion and did or did not experience postoperative ALOD

2. Cranial ALOD

Mean age, sex, follow-up duration, and number of levels fused differed between the cranial ALOD and non-ALOD groups (all, p>0.05) (Table 1). Short PDD was more common in the ALOD group (56 of 64 patients, 88%) than in the non-ALOD group (47 of 76 patients, 62%), (p=0.01) (Table 2). Hyperlordotic fusion was more common in the ALOD group (34 of 64 patients, 53%) than in the non-ALOD group (25 of 76 patients, 33%) (p=0.01). The incidence of preoperative adjacent-segment kyphosis was higher in the ALOD group (56%) than in the non-ALOD group (38%) (p=0.03). The incidence of preoperative OALL was also higher in the ALOD group (63%) than in the non-ALOD group (43%) (p=0.02) (Table 2).

Table 2.

Radiographic measures in those with and without ALOD of the cranial adjacent level after anterior cervical discectomy and fusion

When comparing mean adjacent-segment angles between groups, the ALOD group presented with a greater mean kyphotic angle than the non-ALOD group both at the preoperative visit (0.4°±3.6° vs. -1.9°±5.1°, p=0.03) and at final follow-up (-1.9°±4.8° vs. -0.01°±4.4°, p=0.02) (Table 2).

The ALOD group had less mean adjacent segmental ROM at final follow-up (6.9°±2.8°) than the non-ALOD group did (12°±4.2°) (p<0.01) (Table 2). However, we found no differences between groups in the incidence of CASP-required revision surgery, the overall incidence of CASP, mean VAS scores for neck and back pain, and mean SF-12 PCS (Tables 1 and 2).

3. Caudal ALOD

We found no differences between the caudal ALOD and non-ALOD groups with respect to age, sex, and follow-up duration (Table 1).

A short PDD was more common in the ALOD group (24 of 44 patients, 55%) than in the non-ALOD group (9 of 76 patients, 12%) (p<0.01) (Table 3). The incidence of hyperlordotic fusion did not differ between groups. The incidence of preoperative adjacent-segment kyphosis was higher in the ALOD group (25%) than in the non-ALOD group (1.3%) (p<0.01). Additionally, incidence of preoperative OALL was higher in the ALOD group (61%) than the non-ALOD group (42%) (p=0.04) (Figs. 1, 2).

Table 3.

Radiographic measures in those with and without ALOD of the caudal adjacent level after anterior cervical discectomy and fusion

Fig. 2.

Serial lateral radiographs taken before (A), immediately after (B), and 26 months after (C) surgery for a 48-year-old woman with ossification of the anterior longitudinal ligament preoperatively (arrows, A). Despite 5 mm of plate-to-disc distance, images show advanced adjacent-level ossification development (arrowhead, C) in the setting of kyphosis of the upper adjacent segment (arrowhead, B). The caudal segment, C6–7, which had preoperative ossification of the anterior longitudinal ligament (arrowhead, A), short plate-to-disc distance, and segmental kyphosis in the immediate postoperative radiograph (arrow, B), showed progression of adjacent-level ossification (arrow, C).

When comparing mean adjacent-segment angles, the ALOD group had a more kyphotic angle than the non-ALOD group both preoperatively (mean, -1.4°±3.2° vs. -4.5°±2.4°, p<0.01) and at final follow-up (-0.44°±3.0° vs. -2.9°±2.7°, p<0.01). Mean final adjacent-segment ROM was lower in the ALOD group (5.5°±2.4º) than in the non-ALOD group (8.2±3.7º) (p<0.01) (Table 3). VAS scores for neck and arm pain, SF-12 PCS, and incidence of CASP did not differ between groups. Unlike cranial ALOD group, the incidence of CASP-required revision surgery was higher in the caudal ALOD group (14%) than in the non-ALOD group (3%) (p=0.02) (Table 1).

4. Reliability

The interobserver ICC was 0.86 (95% confidence interval [CI], 0.76–0.92), and the mean intraobserver ICC was 0.90 (95% CI, 0.84–0.94), representing excellent inter- and intraobserver agreement.

DISCUSSION

ALOD has been associated with several risk factors. Instrumentation use in ACDF and short PDD have been reported to contribute to heterotrophic ossification [4-6]. We aimed to identify additional risk factors for ALOD and to report ROM, incidence of reoperation, and PROs. The reported incidence of ALOD ranges from 59%–72% at the cranial adjacent segments and 20%–54% at the caudal adjacent segments after ACDF using anterior cervical plate and screws [1-4,8,10-13]. The incidence of ALOD in our study was within the reported range, with 46% of our cohort presenting with cranial segment ALOD and 37% presenting with caudal segment ALOD. Additionally, we found that preoperative OALL, short PDD, and greater preoperative kyphotic angles were associated with ALOD after ACDF. Mean adjacent-segment ROM was less in both the cranial and caudal segments of the ALOD groups compared with the non-ALOD groups. We found no difference in the incidence of CASP between the ALOD and non-ALOD groups. PROs, including VAS scores for neck and arm pain and SF-12 PCS did not differ between groups in our study.

We found an incidence of 37% of ALOD in the cranial adjacent segment. Additionally, short PDD in the cranial segments of the surgical construct was associated with ALOD. Lee et al. [2] postulated that the smaller vertebral body remaining after the decompression procedure may leave less PDD at the cranial segment than at the caudal segment, contributing to ALOD at the cranial segment. These findings suggest that care must be taken at the cranial segments of an ACDF construct by avoiding short PDD, thereby reducing the risk of ALOD. In addition, we found that the adjacent segment with greater preoperative kyphotic alignment showed higher incidence of ALOD with short PDD (Fig. 3). Considering that the lower subaxial cervical segments (C6–7, C7–T1) are more likely to have lordotic alignment and less kyphotic adjacent segments than the upper subaxial cervical levels (C2–3, C3–4), our finding may explain the higher incidence of ALOD at the cranial adjacent segments (Figs. 1, 2). In addition, more compressive stress at the cranial cervical segments and more shear force at the caudal cervical segments caused by the overcall cervical alignment may contribute to the higher incidence of ALOD in the cranial adjacent segments than in the caudal.

Fig. 3.

Serial lateral radiographs of a 65-year-old woman taken before (A), immediately after (B), and 30 months after (C) surgery for mild ossification of the anterior longitudinal ligament (arrows in A). The mild ossification at the inferior endplate of C7 (arrowhead in B) progressed to advanced adjacent-level ossification (arrowhead in C), with kyphosis and progression of spondylolisthesis of the lower adjacent segment. The patient underwent posterior decompression and instrumented fusion for the caudal adjacent-segment pathology.

Some notable differences were observed when comparing cranial adjacent segments and caudal adjacent segments in our cohort. We found that a hyperlordotic ACDF surgical construct was associated with higher incidence of ALOD in cranial segments but not with ALOD in caudal segments. We speculate that compensatory kyphosis at the adjacent cranial segment after the hyperlordotic ACDF could have led to ALOD at this level. Also, the incidence of revision surgery for CASP did not differ between the cranial and caudal segments. However, a comparison of caudal and cranial adjacent segments with ALOD showed a higher incidence of revision surgery due to CASP in the caudal segments. It is unclear why caudal adjacent segments with ALOD led to a higher incidence of revision surgeries, but this finding might imply that a kyphotic caudal adjacent segment is a sign of more advanced CASP. Further investigation is needed to clarify this difference in adjacent segments required revision surgery.

Limitations of this study should be considered. First, PDD is commonly defined as < 5 mm in studies of ALOD but we defined PDD as < 3 mm because most anterior plate systems in the current study were not designed to provide oblique screw trajectory with the shortest plate. It is evident that a longer PDD could decrease the risk of ALOD, but Koller et al. [15] proposed a 3-mm PDD cutoff value to minimize adjacent-level degeneration based on their study cohort. The 3-mm criterion in our study is unlikely to have meaningfully influenced our findings about PDD. Second, many otherwise eligible patients did not have a minimum of 24 months of follow-up data to enable their inclusion in this study. Further studies with larger sample sizes and longer follow-up are needed. It is important to note that 58% of patients in this study did not complete the 2-year follow-up period. The incomplete data may have influenced our estimation of the overall incidence of ALOD. Also, given the retrospective design of this study, some of the outcomes were measured at different time points, and adjustment for confounders was not performed.

Based on the results of this study, a higher incidence of ALOD would be expected when the adjacent segment has preoperative kyphosis, the ACDF construct is fused in hyperlordotic alignment, and the PDD is less than 3 mm. Although we found no association between ALOD and CASP, avoidance of hyperlordotic ACDF and preserving maximum PDD are recommended to minimize the risk of heterotopic ossification.

CONCLUSION

ALOD after ACDF was associated with short PDD, hyperlordotic fusion, preoperative OALL, and stopping ACDF adjacent to a kyphotic segment. Also, ALOD was associated with less ROM of adjacent segments but did not appear to affect clinical outcomes or the incidence of CASP. Avoidance of these risk factors and preservation of maximum PDD when performing ACDF could decrease the incidence of ALOD.

Notes

Conflict of Interest

The authors have nothing to disclose.

Funding/Support

This study received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Acknowledgments

For editorial assistance, we thank Rachel Walden, MS, in the Editorial Services group of The Johns Hopkins Department of Orthopaedic Surgery.

Author Contribution

Conceptualization: SHL, DBC, KMK, LHRIII; Methodology: SHL, MR; Project administration: SHL; Writing – original draft: SHL; Writing – review & editing: SHL, MR, DBC, KMK, LHRIII.

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Article information Continued

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Parameter	Cranial segments	p-value	Caudal segments	p-value
Sex, male:female	23:41	39:37	0.68	19:25	35:41	0.76
Age (yr)	53 ± 12	56 ± 11	0.17	53 ± 11	55 ± 12	0.37
No. of fusion levels	2.10 ± 0.75	2.10 ± 0.74	0.88	2.10 ± 0.80	2.10 ± 0.73	0.86
Follow-up time (mo)	51 ± 25	46 ± 28	0.23	52 ± 29	44 ± 26	0.12
CASP-required imaging studies	36%	34%	0.83	63%	70%	0.49
CASP-required surgical treatment	11%	13%	0.69	14%	3%	0.02
VAS score
Neck pain	1.9 ± 2.5	1.6 ± 2.4	0.43	1.9 ± 2.5	1.7 ± 2.4	0.64
Arm pain	1.10 ± 2.25	0.86 ± 2.10	0.50	0.62 ± 1.60	1.10 ± 2.30	0.33
SF-12 PCS	42.0 ± 6.6	44.0 ± 7.8	0.38	43.0 ± 8.7	44.00 ± 6.85	0.70

Table 2.

Radiographic measures in those with and without ALOD of the cranial adjacent level after anterior cervical discectomy and fusion

Parameter	Cranial ALOD (n = 64)	No cranial ALOD (n = 76)	p-value
Preoperative
Cranial segment kyphosis	56%	38%	0.03
Preexisting OALL	63%	43%	0.02
Adjacent-segment angle (º)	0.4 ± 3.6	-1.9 ± 5.1	0.03
Adjacent-segment ROM (º)	8.7 ± 3.15	9.0 ± 3.5	0.64
C2–7 angle (º)	-7.8 ± 1.9	-8.4 ± 9.2	0.86
C0–2 angle (º)	-33 ± 16	-38 ± 17	0.16
C2–7 sagittal vertical axis (mm)	31 ± 19	33 ± 14	0.67
Last follow-up
Hyperlordotic fusion^†	53%	33%	0.01
Plate-to-disc distance group^‡	88%	62%	0.01
Plate-to-disc distance (mm)	0.7 ± 1.7	2.0 ± 1.7	< 0.01
Adjacent-segment angle (º)	-1.9 ± 4.8	-0.01 ± 4.4	0.02
Adjacent-segment ROM (º)	6.9 ± 2.8	12.0 ± 4.2	< 0.01
C2–7 angle (º)	-15 ± 12	-11 ± 11	0.08
C0–2 angle (º)	-39 ± 11	-37 ± 13	0.24
C2–7 sagittal vertical axis (mm)	33 ± 16	31 ± 17	0.53

Values are presented as mean±standard deviation unless otherwise indicated.

ALOD, adjacent-level ossification development; OALL, ossification of the anterior longitudinal ligament; ROM, range of motion.

^†

Hyperlordotic fusion was defined as the fused segment showing substantial lordosis and demonstrating adjacent-segment kyphosis on postoperative radiographs.

^‡

Ratio represents plate-to-disc distance <3 mm:≥3 mm.