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Abstract

Objective

This study aims to assess the impact of surgical approaches and other factors on the incidence of Adjacent Segment Degeneration (ASD) following Spinal Fusion for Adolescent Idiopathic Scoliosis (AIS).

Methods

We conducted a comprehensive search of four electronic databases from their inception until March 30, 2023. Two independent reviewers screened titles, abstracts, and full texts and evaluated the methodological quality of the studies. A random-effects model was used to calculate the incidence of ASD.

Results

Our analysis included 14 studies involving 651 individuals. The overall incidence of ASD was 47% (95%CI: 0.37, 0.56). Subgroup analyses revealed that the prevalence of ASD increased with postoperative time (53% (95%CI: 0.31, 0.75) versus 48% (95%CI: 0.36, 0.60) versus 39% (95%CI: 0.22, 0.56)). For the number of fused segments, a group with more than 10 segments had a higher prevalence (49% (95%CI: 0.38, 0.60) versus 44% (95%CI: 0.21, 0.69)). In terms of regions, East Asia had the highest prevalence, followed by Occident and West Asia (52% (95%CI: 0.41, 0.62) versus 43% (95%CI: 0.20, 0.68) versus 37% (95%CI: 0.17, 0.59)). However, the surgical approach, male ratio, and the position of the lowest instrumented vertebra (LIV) did not show significant differences between groups. Funnel plots and Egger’s test did not reveal any significant publication bias (Egger’s test: t = 1.62, p-value = .1274).

Conclusion

This meta-analysis found that nearly half of AIS patients following spinal fusion surgery experienced ASD. Long-term follow-up, regular screening, and timely interventions are essential to reduce the prevalence of ASD.

Keywords

adjacent segment adolescent idiopathic scoliosis degeneration lumbar spinal fusion

Introduction

Adolescent idiopathic scoliosis (AIS) is a three-dimensional spinal deformity characterized by a lateral and rotated curvature exceeding 10.1° in the coronal plane.^1,2 Compared with congenital scoliosis and syndromic scoliosis, idiopathic scoliosis has no clear etiology, and can be classified as infantile, juvenile, and adolescent idiopathic scoliosis according to the onset age, 0–3 years, 4–10 years, and >10 years, respectively.¹ Epidemiological studies suggest that 2%–3% of children aged 10–16 years have spinal curvature, with most not requiring intervention.^3–6 Spinal fusion surgery is an effective treatment for AIS patients with a Cobb angle greater than 45°.² However, this surgery may lead to Adjacent Segment Degeneration (ASD), a potential long-term complication.⁷ After surgical intervention, the evidence of disc deterioration in segments adjacent to the surgically treated disc, shown in radiography, is defined as Adjacent Segment Degeneration (ASD), one of the potential long-term complications.^8,9 The occurrence of ASD may result from abnormal intradiscal pressure and excessive movement in adjacent segments or may be a natural aging process not associated with surgery.^10–12 While previous studies have focused on cervical and lumbar disc diseases, there has been no systematic review or meta-analysis summarizing the risk factors for ASD incidence in AIS following spinal fusion surgery. This article aims to explore the incidence of ASD and its related factors.

Methods

Search strategy and identification of studies

This meta-analysis was performed according to Meta-analysis of Observational Studies in Epidemiology (MOOSE) recommendations.¹³ We conducted a systematic search of electronic databases, including PubMed, The Cochrane Library, Embase, and Web of Science, using specific keywords “Adolescent Idiopathic Scoliosis” “Fusion” “Adjacent segment degeneration”. The search encompassed studies published in English up to April 01, 2023. Two investigators independently reviewed titles, abstracts, and full-text articles for eligibility.

Inclusion and exclusion criteria

Included studies must meet the following criteria: (1) study population must be patients with AIS, the cobb angle >10.1°, based on standing anteroposterior radiographs of the whole spine; (2) study must be longitudinal or case control studies (3) the study must be clearly stated the definition of ASD; (4) the patients accepted anterior or posterior spinal fusion surgery and follow-up time were more than 2 years (5) measured outcomes of the occurrence of ASD. Studies were excluded if they (1) were abstracts, letters, reviews, or case reports; (2) had repeated data (3) had other concomitant spinal diseases or spinal surgery, excluding revision surgery after fusion.

Data extraction and quality of studies

Two investigators independently extracted data, including first authors, publication year, country, sample size, ASD incidence, mean age at surgery, follow-up duration, type of article, male ratio, surgical approach, and fused segments. The quality of included articles was assessed using the Agency for Healthcare Research and Quality (AHRQ) criteria by two investigators, the inclusion decision needs them to agree together. The information included in the study was tabulated and publication bias was inspected with the funnel plot, which should be asymmetric if no publication bias.

Statistical analysis

The meta-analysis was conducted using R software with the “meta” package. The “metaprop” command was employed to estimate weighted pooled proportions using a binomial distribution and Freeman-Tukey Double Arcsine Transformation. A random-effects model was utilized to calculate the incidence and 95% confidence interval (95%CI) of ASD in AIS following spinal fusion surgery.¹⁴ I² statistic was was applied to assess the heterogeneity of the studies, with I² values of 25%, 50%, and 75% representing low, moderate, and high heterogeneity, respectively.¹⁵ Egger test was performed to measure the funnel plot with a significant p-value <.1.^16,17 Subgroup analysis was also carried out, considering surgical approach, male ratio, region, follow-up time, and number of fused segments, and p-value <.05 is considere statistically significant.

Results

A total of 262 studies were initially identified in the database search. Of these, 123 records were excluded due to duplication, and an additional 111 studies were eliminated after reviewing their titles and abstracts. In the remaining 42 literature, 14 reports were not retrievable, and another 14 reports were excluded after a thorough review of their full-text content. Ultimately, 14 studies involving 651 individuals were included in this meta-analysis. The process of identifying eligible literature is visually represented in Figure 1.

Figure 1.

Flow chart summarizing results of the literature search.

The characteristics of the 14 studies are presented in Table 1. For each study, the incidence and 95%CI of ASD following spinal fusion surgery in AIS were calculated. The overall incidence of ASD was found to be 47% (95%CI:37%–56%), as shown in Figure 2.

Table 1.

Characteristic of the studies.

Study	Year	Area	Design	Identification of degeneration	N	Male	Age	Average follow up	LIV	DD%	Fusion segments	Type of surgery
[^a]	Aina J 2001	Sweden	Retrospective	Weiner	139	10	15.0	23.2		23.74	9	PSF
[^b]	Nohara 2015	Japan	Retrospective	Pffirrman	30	0	15.7	14.2		53.33	10.7	PSF
[^b]	Nohara 2015	Japan	Retrospective	Pffirrman	30	0	15.5	11		70.00	7.2	ASF
[^c]	Enercan 2016	Turkey	Retrospective	Pffirrman	21	3	13.4	7.4	L3	28.57		PSF
[^c]	Enercan 2016	Turkey	Retrospective	Pffirrman	16	4	13.7	9	L4	25.00		PSF
[^d]	Dehnokhalaji 2018	Iran	Retrospective	Pffirrman	15	4	14.1	4.85		73.33	12.7	PSF
[^e]	Green 2011	America	Retrospective	Pffirrman	20	3	14.2	11.8		45.00		PSF
[^f]	Ghandhari 2018	Iran	Retrospective	J. Khanna	42	7	20.5	5.6		26.19		PSF
[^g]	Sudo 2013	Japan	Retrospective	Kelly DM	30	4	14.4	17.2	L3	23.33	3.7	ASF
[^h]	Chiu 2021	Malaysis	Retrospective	Pfirrmann	19	3	14.0	18.7	L3	34.3	10.8	PSF
[^h]	Chiu 2021	Malaysis	Retrospective	Pfirrmann	29	0	16.0	17.0	L4	34.0	10.9
[ⁱ]	Akazawa 2017	Japan	Retrospective	Pfirrmann	26	4	14.8	36.1		61.54		PSF
[^j]	Akazawa 2019	Japan	Retrospective	Pfirrmann	19	2	15.3	7.7		47.37	10.3	PSF
[^k]	Burrows 2023	New Zealand	Retrospective	Mimura	36		15.5	21.2		64.00		PSF
[^l]	Akazawa 2017	Japan	Retrospective	Pfirrmann	27	4	13.44	35.44	L3	59.26		PSF/ASF
[^l]	Akazawa 2017	Japan	Retrospective	Pfirrmann	8	1	15.25	33.875	L4	100		PSF/ASF
[^m]	Nohara 2015	Japan	Retrospective	Pfirrmann	93	3	15.2	12.8		48.38	11.0	PSF/PSF + SDF
[ⁿ]	Nohara 2017	Japan	Retrospective	Pfirrmann	51	0	18.2	12.5	L3	62.75	9.7	PSF/ASF/ASF + PSF

^aDanielsson AJ, Nachemson AL. Radiologic findings and curve progression 22 years after treatment for adolescent idiopathic scoliosis: comparison of brace and surgical treatment with matching control group of straight individuals. 2001: DOI: 10.1097/00007632-200103010-00015.

^bNohara A, Kawakami N, Saito T et al. Comparison of surgical outcomes between anterior fusion and posterior fusion in patients with AIS lenke type 1 or 2 that underwent selective thoracic fusion-long-term follow-up study longer than 10 postoperative years. Spine 2015; 40: 1681-1689 DOI: 10.1097/BRS.0000000000001121.

^cEnercan M, Kahraman S, Yilar S et al. Does It Make a Difference to Stop Fusion at L3 versus L4 in Terms of Disc and Facet Joint Degeneration: An MRI Study With Minimum 5 Years Follow-up. Spine Deform 2016; 4: 237-244 DOI: 10.1016/j.jspd.2015.12.001.

^dDehnokhalaji M, Golbakhsh MR, Siavashi B et al. Evaluation of the Degenerative Changes of the Distal Intervertebral Discs after Internal Fixation Surgery in Adolescent Idiopathic Scoliosis. Asian spine journal 2018; 12: 1060-1068 DOI: 10.31616/asj.2018.12.6.1060.

^eGreen DW, Lawhorne TW, 3rd, Widmann RF et al. Long-term magnetic resonance imaging follow-up demonstrates minimal transitional level lumbar disc degeneration after posterior spine fusion for adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2011; 36: 1948-1954 DOI: 10.1097/BRS.0b013e3181ff1ea9.

^fGhandhari H, Ameri E, Nikouei F et al. Long-term outcome of posterior spinal fusion for the correction of adolescent idiopathic scoliosis. Scoliosis and spinal disorders 2018; 13: 14 DOI: 10.1186/s13013-018-0157-z.

^gSudo H, Ito M, Kaneda K et al. Long-term outcomes of anterior dual-rod instrumentation for thoracolumbar and lumbar curves in adolescent idiopathic scoliosis: a twelve to twenty-three-year follow-up study. J Bone Joint Surg Am 2013; 95: e49 DOI: 10.2106/jbjs.L.00781.

^hChiu CK, Tan CS, Chung WH et al. Mid-long-term outcome and degeneration of the remaining unfused lumbar intervertebral disc in adolescent idiopathic scoliosis patients who had posterior spinal fusion surgery. Eur Spine J 2021; 30: 1978-1987 DOI: 10.1007/s00586-021-06874-5.

ⁱAkazawa T, Kotani T, Sakuma T et al. Modic Changes and Disc Degeneration of Nonfused Segments 27 to 45 Years After Harrington Instrumentation for Adolescent Idiopathic Scoliosis: Comparison to Healthy Controls. Spine (Phila Pa 1976) 2018; 43: 556-561 DOI: 10.1097/brs.0000000000002362.

^jAkazawa T, Umehara T, Iinuma M et al. Spinal Alignments of Residual Lumbar Curve Affect Disc Degeneration after Spinal Fusion in Patients with Adolescent Idiopathic Scoliosis: Follow-up after 5 or More Years. Spine surgery and related research 2019: DOI: 10.22603/ssrr.2019-0048.

^kBurrows KR, Henzell IS, Martin G et al. Long-term adjacent segment degeneration at average 21-years follow-up of posterior instrumented fusion for adolescent idiopathic scoliosis. Spine Deform 2023: DOI: 10.1007/s43390-023-00652-7.

^lAkazawa T, Kotani T, Sakuma T et al. Spinal fusion on adolescent idiopathic scoliosis patients with the level of L4 or lower can increase lumbar disc degeneration with sagittal imbalance 35 years after surgery. Spine surgery and related research 2017; 1: 72-77 DOI: 10.22603/ssrr.1.2016-0017.

^mNohara A, Kawakami N, Seki K et al. The Effects of Spinal Fusion on Lumbar Disc Degeneration in Patients with Adolescent Idiopathic Scoliosis: A Minimum 10-Year Follow-Up. Spine Deform 2015; 3: 462-468 DOI: 10.1016/j.jspd.2015.04.001.

ⁿYoung E, Regan C, Currier BL et al. At Mean 30-Year Follow-Up, Cervical Spine Disease Is Common and Associated with Thoracic Hypokyphosis after Pediatric Treatment of Adolescent Idiopathic Scoliosis. J Clin Med 2022; 11: DOI: 10.3390/jcm11206064.

Figure 2.

The prevalence of ASD in AIS following spinal fusion surgery.

Subgroup analysis

We also conducted a subgroup analysis, and the results are presented in Table 2. When considering the surgical approach, the analysis revealed that the incidence of ASD was lower in patients who underwent posterior spinal fusion (PSF) (42% (95%CI: 0.32, 0.53)) compared to anterior spinal fusion (ASF) (46% (95%CI: 0.07, 0.89)). The incidence was similar between patients with a male ratio of ≤15% and >15% (45% (95%CI: 0.35, 0.56) versus 46% (95%CI: 0.22, 0.70)). Furthermore, the incidence was associated with the postoperative time, with a higher incidence observed in patients with longer follow-up periods compared to those with shorter follow-up times (53% (95%CI: 0.31, 0.75) versus 48% (95%CI: 0.36, 0.60) versus 39% (95%CI: 0.22, 0.56)). In terms of the lowest instrumented vertebra (LIV), patients with LIV ≤ L4 had a slightly lower incidence compared to those with LIV ≥ L3 (42% (95%CI: 0.27, 0.57) versus 43% (95%CI: 0.17, 0.71)). Additionally, patients who had fewer than 10 fused segments had a lower incidence than those with more than 10 fused segments (49% (95%CI: 0.38, 0.60) versus 44% (95%CI: 0.21, 0.69)). Regarding regions, East Asia had the highest incidence compared to Occident and West Asia (52% (95%CI: 0.41, 0.62) versus 43% (95%CI: 0.20, 0.68) versus 37% (95%CI: 0.17, 0.59)).

Table 2.

Subgroup analysis of prevalence of ASD in patients with AIS following spinal fusion surgery.

Subgroup	Number of studies	Total	Events	Prevalence(%)	95%CI(%)	Heterogeneity I²(%)	p-value
Surgery approach
PSF	11	412	154	42	32–53	78	p < .01
ASF	2	60	28	46	7–89	93	p < .01
Male ratio
≤15%	11	516	218	45	35–56	83	p < .01
>15%	4	99	42	46	22–70	81	p < .01
Follow up
≤10 years	5	113	41	39	22–56	68	p = .02
10<y < 20	7	302	146	48	36–60	73	p < .01
≥20 years	4	236	96	53	31–75	93	p < .01
LIV
≥L3	5	138	58	42	27–57	70	p = .01
≤L4	3	79	31	43	17–71	77	p = .01
Fused segments
<10	5	205	97	49	38–60	51	p = .08
>10	4	250	93	44	21–69	93	p < .01
Area
East Asia	9	362	186	52	41–62	72	p < .01
Occident	3	195	65	43	20–68	90	p < .01
West Asia	4	94	32	37	17–59	73	p = .01

Assessment of publication bias

Upon visual inspection of the funnel plot and conducting Egger’s test, no significant asymmetry was observed (Egger’s test: t = 1.62, p-value = .1274).

Discussion

Teenagers with AIS often confront challenges related to spinal function, breathing, quality of life, and back pain due to the progressive curvature and rotation of the spine.^2,18,19 The two primary forms of treatment for AIS, depending on the severity of the major curve angle, are bracing and spinal fusion with instrumentation.² However, the long-term consequences for AIS patients who have undergone spinal fusion remain unclear, and significant intervertebral disc degeneration can be observed in the segments that have undergone surgical fusion.^11,20–22 While some studies suggest that ASD is a natural part of the aging process and degenerative changes, it is also influenced by the stress placed on adjacent segments after spinal fusion.²³ Low back pain is a common symptom for AIS patients after fusion surgery. However, there no strong relationship was found between the radiographic findings of ASD and clinical systems.²⁴ It is worth noting that for patients with severe scoliosis, which required surgical intervention required, surgery can effectively reduce low back pain and disc degeneration.²⁵ The prevalence of ASD varies between studies, most of them are based on radiographic findings, which may lead to a higher prevalence. The degree of long-term degeneration in adjacent segments can be assessed through plain radiographs and MRI scans, using classification systems such as J. Khanna, Pfirrmann, Weiner, Kelly DM and Mimura classification.^21,24–36 Among these, the Pfirrmann classification is one of the most commonly utilized methods. It categorizes discs into grades I and II, indicating normal discs, and grades III, IV, and V, indicating degenerated discs. These classifications are based on the structural integrity of the disc, signal intensity, the distinction between the nucleus and annulus, and disc height.³⁷

In this article, we have provided an initial summary of ASD in patients with AIS, a common complication that often follows spinal fusion surgery. Our analysis encompassed data from 14 studies involving 651 patients, revealing that 47% of AIS patients who underwent spinal fusion surgery tested positive for ASD.

Upon conducting a subgroup analysis, we observed that patients who underwent PSF appeared to have a lower incidence of ASD compared to those who had ASF, although the difference was not statistically significant, as well as in its location. It is worth noting that both ASF and PSF have demonstrated similar effectiveness in correcting the primary curvature, addressing secondary minor curvatures, and improving coronal balance.^38,39 However, PSF may offer advantages in terms of sagittal plane correction. Given that factors like scoliosis in the unfused segments, lumbar lordosis, and disc instability can influence disc degeneration, our results suggest that the choice of surgical approach may not be a significant risk factor for the development of ASD.

Gender plays a significant role in the prevalence and severity of AIS. Studies have reported that females exhibit a higher prevalence, more pronounced Cobb angles, and a propensity for easier progression of the condition.^40,41 However, our results did not show a significant difference in the prevalence of ASD between different male-to-female ratio groups.

The study’s findings also indicated that the longer the post-operative period, the higher the prevalence of ASD. Additionally, when compared to the general population or brace treatment, several studies have demonstrated that patients with AIS who undergo surgery tend to have a higher prevalence of ASD. This suggests that degeneration is not solely a result of natural progression but may be influenced by the surgical intervention itself.^26,42 It is important to note that no significant correlation has been identified between radiographic changes associated with degeneration and clinical symptoms.^{24,30,43–45} Therefore, a long-term follow-up of patients is crucial to determine whether degeneration can lead to delayed and clinically significant spondylosis.

In the comparison between groups with the LIV ≤L4 or ≥L3, the results showed that LIV ≤L4 had a slightly higher prevalence. Several studies have demonstrated two groups has similar postoperative radiological parameters. However, the group with LIV ≤L4 tends to have a larger interbody tilt angle and less lumbar lordosis, factors that have been associated with degeneration.^31,33,35 It’s important to note that patients with LIV at a lower position more frequently experience back pain. Therefore, it may be advisable to consider placing the LIV at a higher position, as recommended by previous research.^28,46–48 In summary, our analysis suggests that the choice of LIV may not have a significant impact on the degeneration of adjacent segments.

Some studies have proposed that the prevalence of ASD increases with a greater number of fused segments, likely due to the longer lever arm and the transfer of stress.^8,49–52 However, contradictory findings have indicated that reducing the number of unfused segments may lead to a lower prevalence of ASD in patients who have undergone multi-level fusion surgeries.^{24,29,53–56} In our study, we found that a higher number of fused segments was associated with a higher prevalence of ASD.

The results of our analysis also highlighted regional differences in the prevalence of ASD, with East Asia having the highest incidence, followed by Occident and West Asia. While previous research has shown that surgical outcomes are not significantly influenced by race, these regional variations may be partially attributed to differences in medical conditions and lifestyle habits.^57–59

This meta-analysis represents an initial investigation into the prevalence and risk factors of ASD in patients with AIS following spinal fusion surgery, incorporating subgroup analysis.

However, there are several limitations to this study. Firstly, due to a lack of sufficient data, certain factors associated with ASD, such as pelvic tilt angle and fixation instruments, were not included in the analysis. Secondly, our study focused on adjacent segment degeneration and did not explore adjacent segment diseases, nor did it establish the relationship between degeneration and clinical symptoms. Additionally, several risk factors, which remain a subject of debate, such as surgery age, BMI, radiographic parameters in the coronal and sagittal planes, preoperative disc conditions, osteoporosis, physical activity, were not considered due to data limitations.^{31,33,37,60–64} Lastly, it’s important to note that high heterogeneity is often unavoidable in meta-analyses of epidemiological studies, despite our efforts to conduct subgroup analyses to address this issue.

In conclusion, the prevalence of ASD for patients with AIS following spinal fusion surgery is approximately 50%. The incidence of ASD is influenced by the postoperative time, the number of fused segments, and the patient’s geographical region. In contrast, the choice of surgical approach, male-to-female ratio, and the position of the LIV have only a minor impact. Based on our findings, it appears that opting for a smaller number of fused segments while still achieving successful surgical outcomes may be associated with improved long-term results. However, further long-term, standardized follow-up studies are necessary to better understand the clinical significance of degenerative changes and their impact on AIS patients.

Supplemental Material

Supplemental Material - Half of the adolescent idiopathic scoliosis patients may have lumbar adjacent segment degeneration following spinal fusion: A systemic review and meta-analysis

Supplemental Material for Half of the adolescent idiopathic scoliosis patients may have lumbar adjacent segment degeneration following spinal fusion: A systemic review and meta-analysis by Fuze Liu, Fuhui Liu and Hai Wang in Journal of Orthopaedic Surgery.

Footnotes

Author contributions

Fuze Liu, Fuhui Liu and Hai Wang participated in reviewing the articles. Fuze Liu wrote the manuscript, and completed analysis and interpretation of data. All authors approved the final version of this manuscript.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by National High Level Hospital Clinical Research Funding 2022-PUMCH-A-120 and National Natural Science Foundation of China (82172450).

ORCID iD

Hai Wang

Supplemental Material

Supplemental material for this article is available online.

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