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Systematic Review/Meta-Analysis| Volume 22, ISSUE 6, P1038-1069, June 2022

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Demographic, clinical, and operative risk factors associated with postoperative adjacent segment disease in patients undergoing lumbar spine fusions: a systematic review and meta-analysis

Open AccessPublished:December 08, 2021DOI:https://doi.org/10.1016/j.spinee.2021.12.002

      ABSTRACT

      BACKGROUND CONTEXT

      Adjacent segment disease (ASD) is a potential complication following lumbar spinal fusion.

      PURPOSE

      This study aimed to demonstrate the demographic, clinical, and operative risk factors associated with ASD development following lumbar fusion.

      STUDY DESIGN/SETTING

      Systematic review and meta-analysis.

      PATIENT SAMPLE

      We identified 35 studies that reported risk factors for ASD, with a total number of 7,374 patients who had lumbar spine fusion.

      OUTCOME MEASURES

      We investigated the demographic, clinical, and operative risk factors for ASD after lumbar fusion.

      METHODS

      A literature search was done using PubMed, Embase, Medline, Scopus, and the Cochrane library databases from inception to December 2019. The methodological index for non‐randomized studies (MINORS) criteria was used to assess the methodological quality of the included studies. A meta-analysis was done to calculate the odds ratio (OR) with the 95% confidence interval (CI) for dichotomous data and mean difference (MD) with 95% CI for continuous data.

      RESULTS

      Thirty-five studies were included in the qualitative analysis, and 22 studies were included in the meta-analyses. The mean quality score based on the MINORS criteria was 12.4±1.9 (range, 8–16) points. Significant risk factors included higher preoperative body mass index (BMI) (mean difference [MD]=1.97 kg/m2; 95% confidence interval [CI]=1.49–2.45; p<.001), floating fusion (Odds ratio [OR]=1.78; 95% CI=1.32–2.41; p<.001), superior facet joint violation (OR=10.43; 95% CI=6.4–17.01; p<.001), and decompression outside fusion construct (OR=1.72; 95% CI=1.25–2.37; p<.001).

      CONCLUSIONS

      The overall level of evidence was low to very low. Higher preoperative BMI, floating fusion, superior facet joint violation, and decompression outside fusion construct are significant risk factors of development of ASD following lumbar fusion surgeries.

      Keywords

      Introduction

      Low back pain caused by lumbar spondylosis is a common problem with an estimated prevalence of 5.7% and 4.5% of adult population in Europe and North America, respectively [
      • Ravindra VM
      • Senglaub SS
      • Rattani A
      • Dewan MC
      • Hartl R
      • Bisson E
      • et al.
      Degenerative lumbar spine disease: estimating global incidence and worldwide volume.
      ].
      There has been an annual increase in rates of lumbar decompression and fusion surgeries for the management of degenerative lumbar spine pathologies [
      • Yoshihara H
      • Yoneoka D.
      National trends in the surgical treatment for lumbar degenerative disc disease: United States, 2000 to 2009.
      ,
      • Yavin D
      • Casha S
      • Wiebe S
      • Feasby TE
      • Clark C
      • Isaacs A
      • et al.
      Lumbar fusion for degenerative disease: a systematic review and meta-analysis.
      ,
      • Makanji H
      • Schoenfeld AJ
      • Bhalla A
      • Bono CM.
      Critical analysis of trends in lumbar fusion for degenerative disorders revisited: influence of technique on fusion rate and clinical outcomes.
      ]. Fusion procedures provide stability and have good functional outcomes evidenced by reduced pain and disability scores [
      • Reid PC
      • Morr S
      • Kaiser MG.
      State of the union: a review of lumbar fusion indications and techniques for degenerative spine disease.
      ].
      However, adjacent segment disease (ASD) is a potential complication of fusion procedure, and may necessitate second surgery [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Duan PG
      • Mummaneni PV
      • Guinn JMV
      • Rivera J
      • Berven SH
      • Chou D.
      Is the Goutallier grade of multifidus fat infiltration associated with adjacent-segment degeneration after lumbar spinal fusion?.
      ]. ASD is a degenerative change that occurs at a level above or below the fusion [
      • Tobert DG
      • Antoci V
      • Patel SP
      • Saadat E
      • Bono CM.
      Adjacent segment disease in the cervical and lumbar spine.
      ]. The degenerative changes associated with ASD include disc degeneration or herniation, osteophyte formation, canal stenosis, spondylolisthesis, or scoliosis [
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Scemama C
      • Magrino B
      • Gillet P
      • Guigui P.
      Risk of adjacent-segment disease requiring surgery after short lumbar fusion: results of the French Spine Surgery Society Series.
      ,
      • Lawrence BD
      • Wang J
      • Arnold PM
      • Hermsmeyer J
      • Norvell DC
      • Brodke DS.
      Predicting the risk of adjacent segment pathology after lumbar fusion: a systematic review.
      ]. ASD is believed to be caused by disturbance of normal biomechanics of the adjacent unfused segments, including increased mobility and loading and elevated intradiscal pressure, leading to accelerated degenerative changes [
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Li XF
      • Jin LY
      • Liang CG
      • Yin HL
      • Song XX.
      Adjacent-level biomechanics after single-level anterior cervical interbody fusion with anchored zero-profile spacer versus cage-plate construct: a finite element study.
      ].
      The incidence of ASD following lumbar fusion is widely variable in the literature, with a reported range between 4.7% and 27.4% [
      • Lee JC
      • Kim Y
      • Soh JW
      • Shin BJ.
      Risk factors of adjacent segment disease requiring surgery after lumbar spinal fusion: comparison of posterior lumbar interbody fusion and posterolateral fusion.
      ,
      • Sato S
      • Yagi M
      • Machida M
      • Yasuda A
      • Konomi T
      • Miyake A
      • et al.
      Reoperation rate and risk factors of elective spinal surgery for degenerative spondylolisthesis: minimum 5-year follow-up.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Ghiselli G
      • Wang JC
      • Bhatia NN
      • Hsu WK
      • Dawson EG.
      Adjacent segment degeneration in the lumbar spine.
      ]. This variation is possibly due to differences in populations, pathologies, or fusion procedures. The onset of ASD was reported following different lumbar fusion approaches including, posterior lumbar interbody fusion (PLIF), posterolateral fusion (PLF), transforaminal lumbar interbody fusion (TLIF), anterior lumbar interbody fusion (ALIF), and lateral lumbar interbody fusion (LLIF) [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Lee YS
      • Kim YB
      • Park SW.
      Survival rates and risk factors for cephalad and L5-S1 adjacent segment degeneration after L5 floating lumbar fusion: a minimum 2-year follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ,
      • Ma Z
      • Huang S
      • Sun J
      • Li F
      • Sun J
      • Pi G
      Risk factors for upper adjacent segment degeneration after multi-level posterior lumbar spinal fusion surgery.
      ].
      Several risk factors have been reported to be associated with the development of ASD, including age, gender, high body mass index (BMI), pre-existing spinal stenosis; however, inconsistencies and controversies exist between different studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Lee JC
      • Kim Y
      • Soh JW
      • Shin BJ.
      Risk factors of adjacent segment disease requiring surgery after lumbar spinal fusion: comparison of posterior lumbar interbody fusion and posterolateral fusion.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ].
      The current systematic review and meta-analysis study was conducted to evaluate the epidemiological, clinical, and operative risk factors associated with the development of ASD following lumbar spine fusion.

      Methods

      Conducting and reporting this systematic review was accomplished adhering to the Preferred Reporting Items for Systematic Reviews and Meta‑Analyses (PRISMA) statement guidelines and the current recommendations of the Cochrane Collaboration [
      • Liberati A
      • Altman DG
      • Tetzlaff J
      • Mulrow C
      • Gotzsche PC
      • Ioannidis JP
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
      ,
      • Higgins JPT
      • Thomas J
      • Chandler J
      • Cumpston M
      • Li T
      • Page MJ
      • et al.
      Cochrane handbook for systematic reviews of interventions version 6.2.
      ].

      Search strategy

      Firstly, we used a broad search terminology that included “adjacent segment” or “adjacent level” and “fusion” without filters. The retrieved studies were then divided into different groups to be included in each systematic review.
      A thorough literature search using PubMed, Embase, Medline, Scopus, and the Cochrane library databases from the commencement to December 2019 was conducted to find relevant studies. Additionally, references of the retrieved studies were screened for relevant articles that could meet the inclusion criteria. The MeSH terms for PubMed and EMTREE terms for Embase were utilized during the search.

      Studies selection

      Screening and evaluation of the titles and abstracts of studies identified through the search process against the eligibility criteria were conducted by three independent reviewers (M.M., N.L., and B.Y.) for qualification for full-text review. Irrelevant or duplicate studies were excluded. The full-text assessment was then conducted for inclusion according to the study goals.

      Inclusion and exclusion criteria

      The inclusion criteria for this systematic review were: (1) Studies that included adult patients with lumbar spine pathology who underwent lumbar spine fusion. (2) Studies that reported and compared two groups of patients with and without ASD regarding the clinical risk factors. (3) Studies published in the English language with available full text. (4) Studies with a minimum of 10 patients per treatment group and a minimum follow-up period of 12 months.
      Exclusion criteria included: (1) Studies with congenital or traumatic pathologies, infection, or malignancy. (2) Studies with radiological risk factors only. (3) Studies that focused solely on the incidence of ASD without evaluating the clinical risk factors. (4) Nonclinical studies, animal studies, systematic reviews and meta-analysis, case reports, biomechanical studies, conference abstracts (Table 1).
      Table 1Inclusion and exclusion criteria
      Study componentInclusionsExclusions
      ParticipantsPatients with lumbar spine pathologyCongenital or traumatic pathologies, infection, or malignancy
      InterventionLumbar spine surgeryThoracolumbar surgeries
      ComparatorsPatients with and without postoperative adjacent segment disease (ASD)
      • ASD vs. subclinical ASD
      • Early ASD vs. late ASD
      OutcomesClinical risk factors for developing ASD
      • Nonclinical risk factors, including radiological risk factors
      • Treating ASD without reporting risk factors
      Study design
      • Prospective
      • Retrospective
      • Randomized controlled trials
      • Nonclinical studies or animal studies
      • Narrative reviews
      • Systematic reviews and meta-analysis
      • Abstracts, editorials, letters, posters, or erratum
      • Case reports
      • Biomechanical studies
      • Single reports from multicenter trials
      • Comparative studies with <10 patients per treatment group
      Publication•Full paper•English language
      • Duplicate publications of the same study without reporting on different outcomes
      • Studies reporting on the technical aspects of biologics use in fusion surgeryWhite papersArticles identified as preliminary reports when results are published in later versions
      • Papers that mentioned ASD as one of the complications but do not focus on it
      • Papers focusing only on the incidence of ASD
      • ASD impact on future surgeries
      TimingPostoperative ASDPreoperative ASD
      Any dispute over the inclusion qualification of the studies was settled by a discussion between the three reviewers with the involvement of two other reviewers (Z.B. and A.A.).

      Data extraction

      After the final selection of the included studies, the pertinent details were extracted in a custom data extraction sheet. Three reviewers (M.M., N.L., and B.Y.) independently extracted data from each study, including the author's last name, the study year and type, the demographics, the spine pathology, the surgery, the number of levels, the ASD diagnostic tool, the definition of ASD, and the follow-up period. Moreover, the data related to the impact of each clinical risk factor on the occurrence of ASD was extracted in a specified table.

      Quality assessment

      Three reviewers, M.M., N.L., and B.Y., independently assessed the quality and risk of bias of the selected studies according to the criteria of the methodological index for non‐randomized studies (MINORS) [
      • Slim K
      • Nini E
      • Forestier D
      • Kwiatkowski F
      • Panis Y
      • Chipponi J.
      Methodological index for non-randomized studies (minors): development and validation of a new instrument.
      ]. Each criterion was given a score of 0, 1, or 2 if the item is not reported, inadequately reported, or adequately reported, respectively, with a maximum of 16 points for noncomparative studies and 24 points for comparative studies.

      The certainty of evidence assessment

      Three reviewers, M.M., N.L., and B.Y., independently evaluated the certainty of the evidence utilizing the Grading of Recommendations Assessment, Development, and Evaluation (GRADE) tool, with five domains of risk of bias, inconsistency of results, indirectness of evidence, imprecision, and publication bias [
      • Guyatt GH
      • Oxman AD
      • Vist GE
      • Kunz R
      • Falck-Ytter Y
      • Alonso-Coello P
      • et al.
      GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.
      ]. The quality of evidence was graded as high, moderate, low, or very low. Any disagreements about the quality assessment or the certainty of the evidence were settled by a discussion with the other reviewers (Z.B. and A.A.).

      Outcome measures

      The primary outcome measure was the demographic, clinical, and operative risk factors associated with increased risk of development of ASD following lumbar spine fusions. When analyzing each risk factor, a number of studies were included in the meta-analysis if they reported and compared that risk factor in patients with and without ASD.

      Statistical analysis

      The Review Manager software (RevMan V.5.2.3), the Nordic Cochrane Centre, Copenhagen, Denmark, was used for meta-analysis, which was performed when adequate data on a specific risk factor was available from at least two studies. The dichotomous data were expressed as odds ratio (OR) with corresponding 95% confidence interval (CI), and continuous data were expressed as mean difference (MD) and 95% CI. The I2 test was used to assess the statistical heterogeneity. The variables were pooled utilizing the fixed effects model when the I2 value was<50% and random effects models when the I2 value was>50%. The significance level was set at a p value of less than .05.

      Results

      Search results and study selection

      Initially, searching the whole databases resulted in obtaining a total of 6,850 unique articles. Out of them, screening by titles and abstracts resulted in 114 articles for full-text review for inclusion. Finally, 35 papers [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Lee JC
      • Kim Y
      • Soh JW
      • Shin BJ.
      Risk factors of adjacent segment disease requiring surgery after lumbar spinal fusion: comparison of posterior lumbar interbody fusion and posterolateral fusion.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Chen BL
      • Wei FX
      • Ueyama K
      • Xie DH
      • Sannohe A
      • Liu SY.
      Adjacent segment degeneration after single-segment PLIF: the risk factor for degeneration and its impact on clinical outcomes.
      ,
      • Ha KY
      • Kim YH
      • Ahn JH.
      Is it real adjacent segment pathology by stress concentration after limited fusion in degenerative lumbar scoliosis?.
      ,
      • Ha KY
      • Son JM
      • Im JH
      • Oh IS
      Risk factors for adjacent segment degeneration after surgical correction of degenerative lumbar scoliosis.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ,
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Lai PL
      • Chen LH
      • Niu CC
      • Fu TS
      • Chen WJ.
      Relation between laminectomy and development of adjacent segment instability after lumbar fusion with pedicle fixation.
      ,
      • Lee CH
      • Hyun SJ
      • Kim KJ
      • Jahng TA
      • Yoon SH
      • Kim HJ.
      The efficacy of lumbar hybrid stabilization using the DIAM to delay adjacent segment degeneration: an intervention comparison study with a minimum 2-year follow-up.
      ,
      • Lee CS
      • Hwang CJ
      • Lee SW
      • Ahn YJ
      • Kim YT
      • Lee DH
      • et al.
      Risk factors for adjacent segment disease after lumbar fusion.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Olvera AGR
      • Arroyo MV
      • Martínez LMH
      • Pérez EM
      • Hinojosa LRR.
      Adjacent segment disease in degenerative pathologies with posterior instrumentation.
      ,
      • Ramirez-Villaescusa J
      • López-Torres Hidalgo J
      • Martin-Benlloch A
      • Ruiz-Picazo D
      • Gomar-Sancho F
      Risk factors related to adjacent segment degeneration: retrospective observational cohort study and survivorship analysis of adjacent unfused segments.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Shin MH
      • Ryu KS
      • Kim IS
      • Park CK.
      Symptomatic adjacent segment degeneration following posterior lumbar arthrodesis: retrospective analysis of 26 patients experienced in 10-year of periods.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Tienboon P
      • Jaruwangsanti N.
      Rod stiffness effect on adjacent segmental degeneration: a comparative long-term study.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ,
      • Yugué I
      • Okada S
      • Masuda M
      • Ueta T
      • Maeda T
      • Shiba K.
      Risk factors for adjacent segment pathology requiring additional surgery after single-level spinal fusion: impact of pre-existing spinal stenosis demonstrated by preoperative myelography.
      ] were included in the qualitative analysis after meeting the full inclusion criteria. Out of those studies, 22 studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Chen BL
      • Wei FX
      • Ueyama K
      • Xie DH
      • Sannohe A
      • Liu SY.
      Adjacent segment degeneration after single-segment PLIF: the risk factor for degeneration and its impact on clinical outcomes.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ,
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Lee CH
      • Hyun SJ
      • Kim KJ
      • Jahng TA
      • Yoon SH
      • Kim HJ.
      The efficacy of lumbar hybrid stabilization using the DIAM to delay adjacent segment degeneration: an intervention comparison study with a minimum 2-year follow-up.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] were eligible for the quantitative analysis (Fig. 1).
      Fig 1
      Fig. 1The PRISMA flow diagram of the eligible studies.

      Risk of bias and methodological quality

      Based on the MINORS criteria, the mean score of the included studies was 12.4±1.9 (range, 8–16) points, Supplement 1. As none of the included studies were comparative, only the first 8 items of the MINORS criteria were used with the maximum score of 16 points.

      Characteristics of included studies

      Overall, 34 retrospective studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Lee JC
      • Kim Y
      • Soh JW
      • Shin BJ.
      Risk factors of adjacent segment disease requiring surgery after lumbar spinal fusion: comparison of posterior lumbar interbody fusion and posterolateral fusion.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Ghiselli G
      • Wang JC
      • Bhatia NN
      • Hsu WK
      • Dawson EG.
      Adjacent segment degeneration in the lumbar spine.
      ,
      • Lee YS
      • Kim YB
      • Park SW.
      Survival rates and risk factors for cephalad and L5-S1 adjacent segment degeneration after L5 floating lumbar fusion: a minimum 2-year follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ,
      • Ma Z
      • Huang S
      • Sun J
      • Li F
      • Sun J
      • Pi G
      Risk factors for upper adjacent segment degeneration after multi-level posterior lumbar spinal fusion surgery.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Chen BL
      • Wei FX
      • Ueyama K
      • Xie DH
      • Sannohe A
      • Liu SY.
      Adjacent segment degeneration after single-segment PLIF: the risk factor for degeneration and its impact on clinical outcomes.
      ,
      • Ha KY
      • Kim YH
      • Ahn JH.
      Is it real adjacent segment pathology by stress concentration after limited fusion in degenerative lumbar scoliosis?.
      ,
      • Ha KY
      • Son JM
      • Im JH
      • Oh IS
      Risk factors for adjacent segment degeneration after surgical correction of degenerative lumbar scoliosis.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ,
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Lai PL
      • Chen LH
      • Niu CC
      • Fu TS
      • Chen WJ.
      Relation between laminectomy and development of adjacent segment instability after lumbar fusion with pedicle fixation.
      ,
      • Lee CH
      • Hyun SJ
      • Kim KJ
      • Jahng TA
      • Yoon SH
      • Kim HJ.
      The efficacy of lumbar hybrid stabilization using the DIAM to delay adjacent segment degeneration: an intervention comparison study with a minimum 2-year follow-up.
      ,
      • Lee CS
      • Hwang CJ
      • Lee SW
      • Ahn YJ
      • Kim YT
      • Lee DH
      • et al.
      Risk factors for adjacent segment disease after lumbar fusion.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Olvera AGR
      • Arroyo MV
      • Martínez LMH
      • Pérez EM
      • Hinojosa LRR.
      Adjacent segment disease in degenerative pathologies with posterior instrumentation.
      ,
      • Ramirez-Villaescusa J
      • López-Torres Hidalgo J
      • Martin-Benlloch A
      • Ruiz-Picazo D
      • Gomar-Sancho F
      Risk factors related to adjacent segment degeneration: retrospective observational cohort study and survivorship analysis of adjacent unfused segments.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Shin MH
      • Ryu KS
      • Kim IS
      • Park CK.
      Symptomatic adjacent segment degeneration following posterior lumbar arthrodesis: retrospective analysis of 26 patients experienced in 10-year of periods.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Tienboon P
      • Jaruwangsanti N.
      Rod stiffness effect on adjacent segmental degeneration: a comparative long-term study.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ,
      • Yugué I
      • Okada S
      • Masuda M
      • Ueta T
      • Maeda T
      • Shiba K.
      Risk factors for adjacent segment pathology requiring additional surgery after single-level spinal fusion: impact of pre-existing spinal stenosis demonstrated by preoperative myelography.
      ] and one prospective study [
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ] were included in this systematic review with a total number of 7,374 patients who had undergone lumbar spine fusion.
      Two studies did not report the number of males and females [
      • Lee CS
      • Hwang CJ
      • Lee SW
      • Ahn YJ
      • Kim YT
      • Lee DH
      • et al.
      Risk factors for adjacent segment disease after lumbar fusion.
      ,
      • Olvera AGR
      • Arroyo MV
      • Martínez LMH
      • Pérez EM
      • Hinojosa LRR.
      Adjacent segment disease in degenerative pathologies with posterior instrumentation.
      ]. The remaining 33 studies included 3,714 (60.6%) females and 2,412 (39.3%) males.
      The incidence of ASD in the included studies ranged from 2.6% to 62.5%, with a total of 1,266 (17.2%) patients who developed ASD following lumbar spine fusions. The follow-up period widely varied between the included studies and ranged from at least 12 months to a mean of 165.6 months.
      Regarding the number of levels that were operated on, twenty-two studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Lee JC
      • Kim Y
      • Soh JW
      • Shin BJ.
      Risk factors of adjacent segment disease requiring surgery after lumbar spinal fusion: comparison of posterior lumbar interbody fusion and posterolateral fusion.
      ,
      • Ghiselli G
      • Wang JC
      • Bhatia NN
      • Hsu WK
      • Dawson EG.
      Adjacent segment degeneration in the lumbar spine.
      ,
      • Lee YS
      • Kim YB
      • Park SW.
      Survival rates and risk factors for cephalad and L5-S1 adjacent segment degeneration after L5 floating lumbar fusion: a minimum 2-year follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ,
      • Ma Z
      • Huang S
      • Sun J
      • Li F
      • Sun J
      • Pi G
      Risk factors for upper adjacent segment degeneration after multi-level posterior lumbar spinal fusion surgery.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Lai PL
      • Chen LH
      • Niu CC
      • Fu TS
      • Chen WJ.
      Relation between laminectomy and development of adjacent segment instability after lumbar fusion with pedicle fixation.
      ,
      • Lee CS
      • Hwang CJ
      • Lee SW
      • Ahn YJ
      • Kim YT
      • Lee DH
      • et al.
      Risk factors for adjacent segment disease after lumbar fusion.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Olvera AGR
      • Arroyo MV
      • Martínez LMH
      • Pérez EM
      • Hinojosa LRR.
      Adjacent segment disease in degenerative pathologies with posterior instrumentation.
      ,
      • Ramirez-Villaescusa J
      • López-Torres Hidalgo J
      • Martin-Benlloch A
      • Ruiz-Picazo D
      • Gomar-Sancho F
      Risk factors related to adjacent segment degeneration: retrospective observational cohort study and survivorship analysis of adjacent unfused segments.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Shin MH
      • Ryu KS
      • Kim IS
      • Park CK.
      Symptomatic adjacent segment degeneration following posterior lumbar arthrodesis: retrospective analysis of 26 patients experienced in 10-year of periods.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Tienboon P
      • Jaruwangsanti N.
      Rod stiffness effect on adjacent segmental degeneration: a comparative long-term study.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] included single and multiple-level fusions, seven studies [
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Chen BL
      • Wei FX
      • Ueyama K
      • Xie DH
      • Sannohe A
      • Liu SY.
      Adjacent segment degeneration after single-segment PLIF: the risk factor for degeneration and its impact on clinical outcomes.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Yugué I
      • Okada S
      • Masuda M
      • Ueta T
      • Maeda T
      • Shiba K.
      Risk factors for adjacent segment pathology requiring additional surgery after single-level spinal fusion: impact of pre-existing spinal stenosis demonstrated by preoperative myelography.
      ] included single-level fusion only, and three studies [
      • Ha KY
      • Kim YH
      • Ahn JH.
      Is it real adjacent segment pathology by stress concentration after limited fusion in degenerative lumbar scoliosis?.
      ,
      • Ha KY
      • Son JM
      • Im JH
      • Oh IS
      Risk factors for adjacent segment degeneration after surgical correction of degenerative lumbar scoliosis.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ] included multiple surgeries only. Three studies [
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Lee CH
      • Hyun SJ
      • Kim KJ
      • Jahng TA
      • Yoon SH
      • Kim HJ.
      The efficacy of lumbar hybrid stabilization using the DIAM to delay adjacent segment degeneration: an intervention comparison study with a minimum 2-year follow-up.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ] did not report the number of levels. The demographics, pathologies, types of surgery, number of operated levels, ASD diagnostic tools, and the ASD diagnostic criteria in each study are reported in Table 2. Analysis of clinical risk factors for ASD in each individual study is summarized in Table 3.
      Table 2Demographics, pathologies, operation, number of operated levels, ASD diagnostic tools, and ASD diagnostic criteria of the included studies
      No.Author/year,Study designRoBDemographics (mean or %)Spine pathology diagnosisOperationNo. of operated levelsASD diagnostic toolsASD diagnostic criteria
      1.Ma 2019
      • -
        Retrospective
      • -
        RoB: 13/16
      N=71

      Age: 62.2 y

      Female: 37 (52%)

      Male: 34 (48%)

      N ASD/No ASD=29 (40.9%)/42 (59.1%)

      F/U: 36 m
      Degenerative lumbar stenosisPLF/PLIF1–4 levelsRadiological (lateral X-ray)
      • >20% disc height reduction
      • >3 mm slippage distance
      • >3 mm osteophyte
      2.Olvera 2015
      • -
        Retrospective
      • -
        RoB: 9/16
      N=179

      Age: 60 y (ASD)

      Female: Not reported

      Male: Not reported

      N ASD/No ASD=20 (11.2%)/159 (88.8%)

      F/U: 39 m
      Spondylolisthesis, lumbar stenosis, degenerative scoliosisPLF/PLIFSingle or multipleClinical

      Radiological (lateral X-ray, MRI)
      Clinical:Radiculopathy, decreased functionRadiological:
      • X-ray: White and Panjabi stability criteria
      • MRI: MODIC scale of disc degeneration, canal stenosis and facet arthrosis
      3.Shin 2007
      • -
        Retrospective
      • -
        RoB: 15/16
      N=421

      Age: 56.5±11.2 y

      Female: 282 (68%)

      Male: 139 (32%)

      N ASD/No ASD=26 (6.2%)/395 (93.8%)

      F/U: Not reported
      Spinal stenosis, spondylolisthesis, segmental instability, failed back surgery syndromePLF/PLIFSingle or multipleClinical

      Radiological (lateral X-ray)
      Clinical:

      New patterns of pain

      Radiological:

      New or progressive degenerative changes
      4.Tienboon 2010
      • -
        Retrospective
      • -
        RoB: 14/16
      N=187

      Age: 61.6 y

      Female: 129 (69%)

      Male: 58 (31%)

      N ASD/No ASD=15 (8%)/172 (92%)

      F/U: 50.4 m
      Isthmic spondylolisthesis, degenerative spondylolisthesis, spinal canal stenosis, degenerative scoliosis, recurrent disc herniation, post discectomy degeneration, fracture, corrective deformityDecompression and fusion with pedicle screw instrumentationSingle or multipleRadiological (Lateral, dynamic X-rays, MRI)X-rays: adjacent level degeneration and instability

      MRI:<10 mm central canal diameter
      5.Heo 2015
      • -
        Retrospective
      • -
        RoB: 14/16
      N=378

      Age: 58.9 y

      Female: 253 (66.9%)

      Male: 125 (33.1%)

      N ASD/No ASD=33 (8.7%)/345 (91.2%)

      F/U: 71.8 m
      L4–L5 spondylolisthesisPLF/PLIFSingle (L4–L5) or multiple (L4–S1)Clinical

      Radiological (Lateral X-rays, CT)
      L3–L4 fusion extension surgery due to low back pain with radiological instability, radiculopathy, or claudication due to L3–L4 degenerative pathology
      6.Kawaguchi 2007
      • -
        Retrospective
      • -
        RoB: 13/16
      N=71

      Age: 55.7 y

      Female: 18 (25.4%)

      Male: 53 (74.6%)

      N ASD/No ASD=8 (11.3%)/63 (88.7%)

      F/U: 64.8 m
      Lumbar spinal stenosisExpansive lumbar laminoplasty and interlaminar fusion2–5 segmentsClinical

      Radiological (X-rays, CT, myelography, MRI)
      Newly developed clinical symptoms (low back pain and/or radiculopathy) with radiological lesions
      7.Kim 2016
      • -
        Retrospective
      • -
        RoB: 16/16
      N=100

      Age: 60.80 y (ASD), 60.82 y (No ASD)

      Female: 70 (70%)

      Male: 30 (30%)

      N ASD/No ASD=50 (50%)/50 (50%)

      F/U: 20.5 m
      Spinal stenosis, isthmic and degenerative spondylolisthesis, degenerative disc disease, disc herniationPLIF + open pedicle screw fixationNot reportedRadiological (lateral and dynamic X-rays, MRI)X-rays:
      • >4 mm olisthesis
      • >10° angular changes
      • >10% disc height loss
      • ≥2 grades deterioration (the UCLA disc degeneration scale)
      MRI:
      • Pfirrmann grade of IV and V
      • Spinal stenosis
      • Disc herniation
      8.Lee 2013
      • -
        Retrospective
      • -
        RoB: 15/16
      N=75

      Age: 65.7 y

      Female: 45 (60%)

      Male: 30 (40%)

      N ASD/No ASD=30 (40%)/45 (60%)

      F/U: 46.8±22.8 m
      Spinal stenosis, foraminal stenosis, radiculopathy, disk herniation, or gross instability, spondylolisthesisHybrid stabilization (PLIF + DIAM system)Not reportedRadiological (lateral, dynamic X-rays)
      • Collapsed disk space
      • ≥3 mm spondylolisthesis
      • Proximal junctional kyphosis (junction sagittal Cobb angle≥10°)
      • Compression fracture
      9.Lee 2014
      • -
        Retrospective
      • -
        RoB: 14/16
      N=490

      Age: 53 y

      Female: 307 (62.7%)

      Male: 183 (37.3%)

      N ASD/No ASD=24 (4.9%)/466 (95.1%)

      F/U: 51 m
      Spinal stenosis, degenerative or spondylolytic spondylolisthesis, herniated intervertebral disc with segmental instability and/or advanced disc degeneration, degenerative disc disease with severe back painPLF/PLIFSingle or multiple (≤ 3)Clinical

      Radiological (X-rays)
      Clinical:

      Radiculopathy

      Radiological:

      Degenerative lesions, such as spinal stenosis, segmental instability, or deformity
      10.Lee 2015
      • -
        Retrospective
      • -
        RoB: 13/16
      N=115

      Age: 58.2±10.0 y

      Female: 71 (61.7%)

      Male: 44 (38.3%)

      N ASD/No ASD=

      42 (36.5%)/73 (63.5%)

      F/U: 46.1 m
      Spinal stenosis, degenerative spondylolisthesis, isthmic spondylolisthesis, degenerative scoliosisTLIFSingle or multipleClinical

      Radiological (lateral, dynamic X-rays)
      Clinical:New back pain or radiculopathyRadiological:
      • ≥10° angular motion
      • >4 mm listhesis anterior, posterior, or lateral
      • Increase to disc degeneration grade 2 (the University of California at Los Angeles grading scale)
      11.Liang 2014
      • -
        Retrospective
      • -
        RoB: 14/16
      N=84

      Age: 61.4±12.0 y (ASD), 62.1±10.3 y (No ASD)

      Female: 55 (65.5%)

      Male: 29 (34.5%)

      N ASD/No ASD=28 (33.3%)/56 (66.7%)

      F/U:≥60 m
      Disc herniation, lumbar spondylolisthesis, or lumbar stenosisPLIFNot reportedRadiological (lateral, dynamic X-rays)
      • >3 mm anterior or posterior displacement
      • ≥20% reduction of disc height
      • >15° segmental motion instability
      12.Makino 2018
      • -
        Retrospective
      • -
        RoB: 16/16
      N=41

      Age: 66.7±9.0 y

      Female: 27 (65.9%)

      Male: 14 (34.1%)

      N ASD/No ASD=

      5 (12.2%)/36 (87.8%)

      F/U: 41.0±13.2 m
      SpondylolisthesisPLIFSingle (L4–L5)Radiological (lateral X-rays)
      • 3mm L3 antero- or retrolisthesis
      • 3 mm L3–L4 disc height reduction
      • < -5° intervertebral angle at flexion
      13.Maragkos 2020a
      • -
        Retrospective
      • -
        RoB: 13/16
      N=131

      Age: 60 y (median)

      Female: 78 (59.5%)

      Male: 53 (40.5%)

      N ASD/No ASD=33 (25.2%)/98 (74.8%)

      F/U: 21 m (median)
      Spondylolisthesis, severe canal stenosis, disc protrusion, other degenerative causesPLIFSingle (L4–L5)Clinical

      Radiological (lateral X-rays)
      Disc degeneration, stenosis, or spondylolisthesis requiring reoperation
      14.Maragkos 2020b
      • -
        Retrospective
      • -
        RoB: 13/16
      N=568

      Age: 55±14 y (ASD), 56±14 y (No ASD)

      Female: 303 (53.3%)

      Male: 265 (46.7%)

      N ASD/No ASD=167 (29.4%)/401 (70.6%)

      F/U: 33.6 m
      Spondylolisthesis, multilevel spondylosis and stenosis w/o spondylolisthesis, disc herniationALIF/LLIF/PLIF/PSF/PLIF + PSF/ALIF + PSF/LLIF + PSFSingle or multipleNot reportedSymptomatic disk degeneration, stenosis, or spondylolisthesis
      15.Anandjiwala 2011
      • -
        Prospective
      • -
        RoB: 14/16
      N=68

      Age: 63.6 y (ASD) 63.4 y (No ASD)

      Female: 55 (80.9%)

      Male: 13 (19.1%)

      N ASD/No ASD=

      14 (20.6%)/54 (79.4%)

      F/U: 67.4 m
      Stenosis, degenerative scoliosis, isthmic spondylolisthesis, degenerative spondylolisthesisPLF/PLIFSingle or multipleRadiological (lateral dynamic X-rays, MRI)
      • Complete collapse of the disc space
      • >3 mm sagittal or coronal translation
      • >5° of disc space wedging
      • >10° angular instability
      • Complete blockage of the spinal canal
      16.Bae 2010
      • -
        Retrospective
      • -
        RoB: 11/16
      N=103

      Age: 48.5±8.9 y

      Female: 64 (62.1%)

      Male: 39 (37.9%)

      N ASD/No ASD=11 (10.7%)/92 (89.3%)

      F/U: 59.2±14.6 m
      Unstable low-grade isthmic spondylolisthesis









      Mini-ALIF/mini-TLIFSingle (L4–L5 or L5–S1)Clinical

      Radiological (lateral dynamic X-rays, CT, MRI)



      • >4 mm of anterolisthesis or retrolisthesis
      • >10° of angular motion
      • spinal stenosis caused by facet joint hypertrophy
      • compression fracture
      • degenerative scoliosis
      • >10% disc height loss
      • >3 mm osteophyte formation
      17.Bagheri 2019
      • -
        Retrospective
      • -
        RoB: 12/16
      N=630

      Age: 61.37±4.12 y (ASD), 62.37±3.9 y (No ASD)

      Female: 327 (51.91%)

      Male: 303 (48.09%)

      N ASD/No ASD=76 (12.1%)/554 (87.9%)

      F/U: 51±2.2 m (ASD), 52±2.3 m (No ASD)
      Degenerative spondylolisthesis, spinal stenosis, disc herniation, degenerative scoliosisPLIF<4 levels or >4 levelsRadiological (lateral dynamic X-rays, CT, MRI)
      • >20% disc height collapse
      • >4 mm olisthesis
      • >10° angular motion
      • Spinal stenosis
      • Disc herniation
      18.Bydon 2014
      • -
        Retrospective
      • -
        RoB: 12/16
      N=511

      Age: 59.45±13.48 y

      Female: 257 (50.3%)

      Male: 254 (49.7%)

      N ASD/No ASD=80 (15.7%)/431 (84.3%)

      F/U: 39.73±46.52 m
      Spondylolisthesis, scoliosis, degenerative disc diseasePLFSingle or multipleClinical

      Radiological
      Degeneration with clinical symptoms requiring revision surgery
      19.Chen 2011
      • -
        Retrospective
      • -
        RoB: 12/16
      N=109

      Age: 53.4 y

      Female: 60 (55%)

      Male: 49 (45%)

      N ASD/No ASD=24 (22%)/85 (78%)

      F/U: 39.3 m
      L4–L5 degenerative instabilityPLIFSingle (L4–L5)Radiological (lateral dynamic X-rays)
      • >3 mm disc height
      • >5° intervertebral space angulation
      • >3 mm L3 slippage
      20.Choi 2014
      • -
        Retrospective
      • -
        RoB: 13/16
      N=49

      Age: 50.7±9.4 y (ASD), 48.9±9.4 y (No ASD)

      Female: 35 (71.4%)

      Male: 14 (28.6%)

      N ASD/No ASD=19 (38.8%)/30 (61.2%)

      F/U: 134.2 m
      Low-grade isthmic spondylolisthesisALIF with percutaneous PSFSingle (L4–L5 or L5–S1)Clinical

      Radiological (lateral dynamic X-rays, CT and MRI)
      Clinical:
      • Development of new clinical symptoms
      • VAS pain score of≥6 for back or legs
      • ODI score of more than 40%
      Radiological:
      • >3 mm olisthesis (anterolisthesis or retrolisthesis)
      • >10% disc height loss
      • >10° angular motion
      • >3 mm osteophyte formation
      • Disc herniation or spinal stenosis
      • Disc degeneration≥grade 2
      • Facet arthropathy≥grade 2
      • Scoliosis
      • Compression fracture
      21.Disch 2008
      • -
        Retrospective
      • -
        RoB: 14/16
      N=102

      Age: 54±14.7 y

      Female: 69 (67.6%)

      Male: 33 (32.4%)

      N ASD/No ASD=27 (26.5%)/75 (73.5%)

      F/U: 165.6 m
      Degenerative disease or isthmic spondylolisthesisALIF/ALIF & PLIFSingle or two (L4–S1)Radiological (AP, lateral dynamic X-rays)
      • >20% disc space narrowing
      • ≥3 mm dynamic translation
      22.Ghiselli 2004
      • -
        Retrospective
      • -
        RoB: 12/16
      N=215

      Age: 50 y

      Female: 126 (58.6%)

      Male: 89 (41.4%)

      N ASD/No ASD=59 (27.4%)/156 (72.6%)

      F/U: 80.4 m
      Progressive spondylolisthesis, degenerative or iatrogenic spondylolisthesis in patients with spinal stenosis, progressive lumbar scoliosis, iatrogenic instability from extensive decompression, two or more episodes of disc herniation at the same level, and incapacitating nonradicular back pain after failure of nonoperative treatmentPLIFSingle or multipleClinical

      Radiological (AP, lateral dynamic X-rays)
      Clinical:Symptomatic instability, radiculopathy, or spinal stenosisRadiological:
      • >4 mm translation
      • >10° angular motion
      23.Ha 2013
      • -
        Retrospective
      RoB: 12/16
      N=98

      Age: 64.4±5.1 y

      Female: 80 (81.6%)

      Male: 18 (18.4%)

      N ASD/No ASD=44 (44.9%)/54 (55.1%)

      F/U: 75.4 m
      Degenerative lumbar scoliosisScoliosis correction and lumbar/thoracolumbar fusions with pedicle screw instrumentationMultipleRadiological (lateral dynamic X-rays, MRI)
      • 4 mm translation
      • 10° angular motion
      • Severe disc space collapse
      • Herniated nucleus pulposus and stenosis
      • Vertebral compression fracture
      • Pedicle screw loosening and nonunion
      24Ha 2014
      • -
        Retrospective
      • -
        RoB: 12/16
      N=59

      Age: 67±6 y

      Female: 50 (84.7%)

      Male: 9 (15.3%)

      N ASD/No ASD=16 (27.1%)/43 (72.9%)

      F/U: 59.4±39.9 m
      Degenerative lumbar scoliosisDecompressive laminectomy and instrumented fusionMultipleRadiological (AP, lateral dynamic X-rays)
      • Disc space collapse with endplate sclerosis
      • >3 mm anterolisthesis or retrolisthesis
      • >5 ° disc space wedging
      • >10° angular motion
      • >6 mm lateral translation
      • Rotational subluxation
      25.Hyun 2007
      • -
        Retrospective
      • -
        RoB: 11/16
      N=201

      Age: 53 y

      Female: 132 (65.7%)

      Male: 69 (34.3%)

      N ASD/No ASD=61 (30%)/140 (70%)

      F/U: 73 m
      Degenerative spondylolisthesis, stenosis, instabilityPLF/PLIF/TLIFSingle or multipleClinical

      Radiological (lateral dynamic X-rays, MRI)
      Clinical:Development of new clinical symptomsRadiological:
      • Disc dehydration
      • >3 mm disc space narrowing
      • Disc space vacuum
      • Osteophyte formation
      • Degenerative retrolisthesis, antelisthesis or rotatory dislocation
      • Spinal stenosis
      • >4mm translation
      • >10° angular motion
      26.Lai 2004
      • -
        Retrospective
      • -
        RoB: 13/16
      N=101

      Age: 61 y

      Female: 83 (82.2%)

      Male: 18 (17.8%)

      N ASD/No ASD=23 (22.8%)/78 (77.2%)

      F/U:≥72 m
      Degenerative or spondylotic spondylolisthesisPLFSingle or multipleRadiological (lateral dynamic X-rays)
      • >4 mm slippage
      • >10° angular motion
      27.Lee 2009
      • -
        Retrospective
      • -
        RoB: 12/16
      N=1,069

      Age: 58.4 y (ASD), 58.2 y (No ASD)

      Female: 18 (ASD)

      Male: 10 (ASD)

      N ASD/No ASD=28 (2.6%)/1,041 (97.4%)

      F/U:≥12m
      Spinal stenosis, isthmic and degenerative spondylolisthesis, degenerative kyphosis, degenerative disc disease, disc herniationPLF/PLIFSingle or multipleClinical

      Radiological (lateral dynamic X-rays, MRI)
      Clinical:

      Newly developed symptoms and revision surgery

      Radiological:

      Degenerative lesions
      28.Min 2008
      • -
        Retrospective
      • -
        RoB: 11/16
      N=48

      Age: 53 y

      Female: 34 (70.8%)

      Male: 14 (29.2%)

      N ASD/No ASD=30 (62.5%)/18 (37.5%)

      F/U: 44.6 m
      Spondylolytic or degenerative spondylolisthesis, spinal stenosisALIF/PLIF/TLIFSingle (L4–L5)Radiological (lateral dynamic X-rays, CT, MRI)
      • >10% disc height loss
      • >4 mm listhesis (anterolisthesis, retrolisthesis)
      • >10° angular motion
      • Symptomatic disc herniation or spinal stenosis
      • Hypertrophic facet arthropathy
      • >3 mm osteophyte formation
      • Scoliosis
      • Compression fracture
      29Ou 2015
      • -
        Retrospective
      • -
        RoB: 8/16
      N=190

      Age: 65.0±12.7 y

      Female: 105 (55.3%)

      Male: 85 (44.7%)

      N ASD/No ASD=13 (6.8%)/177 (93.2%)

      F/U: 23.8±19.2 m
      Degenerative spine diseasePLIF/TLIF/PLFSingle or multipleClinical

      Radiological (MRI)
      Clinical:New symptoms of pain or neurological dysfunctionRadiological:
      • Cerebrospinal fluid-to-rootlet ratio
      • ≥1 degeneration grading change
      30.Ramirez-Villaescusa 2019
      • -
        Retrospective
      • -
        RoB: 10/16
      N=263

      Age: 59.0 y

      Female: 165 (62.7%)

      Male: 98 (37.3%)

      N ASD/No ASD=151 (57.4%)/112 (42.6%)

      F/U: 45.9±17.8 m
      Degenerative disc disease,

      degenerative spondylolisthesis, lumbar canal stenosis, degenerative lumbar scoliosis, isthmic lytic spondylolisthesis
      PLF/PLIF/TLIFSingle or multipleClinical

      Radiological (lateral dynamic X-rays, MRI)
      Clinical:
      • ≥3 points VAS score in lumbar or radicular pain
      • ≥15 points ODI
      Radiological:
      • ≥1 mm disc height loss
      • ≥3 mm anterolisthesis or retrolisthesis
      • ≥1° rotation
      • Grade 2 or 3 disc degeneration (Weiner)
      • Grades IV and V (Pfirrmann)
      31.Sakaura 2013
      • -
        Retrospective
      • -
        RoB: 11/16
      N=40

      Age: 58.6 y

      Female: 14 (35%)

      Male: 26 (65%)

      N ASD/No ASD=4 (10%)/36 (90%)

      F/U: 66.8 m
      Isthmic spondylolisthesisPLIFSingle or multipleClinical

      Radiological (lateral dynamic X-rays, CT)
      Newly developed or aggravated neurologic symptoms with radiographic degenerative changes
      32.Soh 2013
      • -
        Retrospective
      • -
        RoB: 10/16
      N=55

      Age: 50.2 y

      Female: 37 (67.3%)

      Male: 18 (32.7%)

      N ASD/No ASD=21 (38.2%)/34 (61.8%)

      F/U: 102 m
      Degenerative lumbar diseasePLF/PLIFSingle or multiple (≤ 3)

      Radiological (lateral dynamic X-rays, MRI)
      • >3 mm anterior or posterior displacement
      • ≥20% disc height loss
      • >15° angular motion
      33.Wang 2017
      • -
        Retrospective
      • -
        RoB: 10/16
      N=237

      Age: 53.2±10.8 y

      Female: 131 (55.3%)

      Male: 106 (44.7%)

      N ASD/No ASD=15 (6.3%)/222 (93.7%)

      F/U: 31.2 m
      Disc herniation, spinal stenosis, degenerative spondylolisthesisPLIF/TLIFSingle or multiple (L4–L5, L5–S1, L4–S1)Clinical

      Radiological (lateral dynamic X-rays, MRI)
      Disc degeneration with clinical symptoms of radiculopathy, stenosis, or instability
      34.Yugué 2016
      • -
        Retrospective
      • -
        RoB: 11/16
      N=161

      Age: 65.4 y

      Female: 105 (65.2%)

      Male: 56 (34.8%)

      N ASD/No ASD=22 (13.7%)/139 (86.3%)

      F/U: 77.3 m
      L4 degenerative spondylolisthesisPLF/PLIFSingle (L4–L5)Radiological (lateral dynamic X-rays, CT, MRI, myelography)
      • >4 mm spondylolisthesis
      • >10° angular motion
      35.Zhong 2017
      • -
        Retrospective
      • -
        RoB: 12/16
      N=154

      Age: 58.4±13.5 y

      Female: 110 (71.4%)

      Male: 44 (28.6%)

      N ASD/No ASD=18 (11.7%)/136 (88.3%)

      F/U: 28.6±16.8 m
      Isthmic or degenerative spondylolisthesisPLF/TLIF/ALIF/XLIFSingle or multipleClinical

      Radiological (lateral dynamic X-rays, MRI)
      New clinical symptoms with radiographic degenerative changes requiring surgery
      PLF, posterolateral fusion; PLIF, posterior lumbar interbody fusion; DIAM, Device for Interspinous Assisted Motion; TLIF, transforaminal lumbar interbody fusion; ALIF, anterior lumbar interbody fusion; LLIF, lateral lumbar interbody fusion; PSF, pedicle screw fixation; XLIF, extreme lateral interbody fusion.
      Table 3Summary of ASD incidence with various demographic, clinical, operative risk factors
      Risk factorAuthor (year)F/U (months)ASDgroupNo ASDgroupRisk ratio/Odds ratio/Hazard ratiop value
      Preoperative pathology
      Olvera 201539
      • -
        Spondylolisthesis=5
      • -
        Stenosis=14
      • -
        Degenerative scoliosis=1
      • -
        45
      • -
        102
      • -
        12
      Not reportedNot reported
      Heo 201571.8
      • -
        Isthmic spondylolisthesis=18
      • -
        Degenerative spondylolisthesis=15
      • -
        73
      • -
        272
      3.499 (1.761–6.952) (univariate cox proportional hazard ratio)

      7.07 (3.072–16.284) (multivariate cox proportional hazard ratio)
      <.001
      Kawaguchi 200764.8
      • -
        Degenerative stenosis=2
      • -
        Combined stenosis=2
      • -
        Hyperostotic stenosis=0
      • -
        Spondylolisthesis=4
      • -
        Degenerative scoliosis=1
      • -
        36
      • -
        12
      • -
        6
      • -
        9
      • -
        19
      Not reported
      • -
        .085
      • -
        .16
      • -
        .36
      • -
        .014
      • -
        .3
      Lee 201451Not reportedNot reportedNot reported.274
      Liang 2014≥60
      • -
        Disc Herniation=3
      • -
        Spondylolisthesis=3
      • -
        Stenosis=22
      • -
        12
      • -
        4
      • -
        40
      Not reported.446

      Anandjiwala 201167.4
      • -
        Stenosis=6
      • -
        Degenerative scoliosis=7
      • -
        Degenerative spondylolisthesis=1
      • -
        20
      • -
        15
      • -
        19
      Not reported.088

      Ghiselli 200480.4Not reportedNot reportedNot reported.34
      Min 200844.6- Spondylolytic Spondylolisthesis=16

      - Degenerative spondylolisthesis=14

      - Spinal stenosis=0
      - 8

      - 9

      - 1
      Not reportedNot reported
      Wang 201731.2- Disc herniation=6

      - Spinal stenosis=6

      - Spondylolisthesis=3
      - 82

      - 78

      - 62
      Not reported.606
      Zhong 201728.6±16.8- Degenerative spondylolisthesis=14

      - Isthmic Spondylolisthesis=4
      - 91

      - 45
      Not reported.429
      Hyun 200773Stenosis=3671Not reportedNot reported
      Ramirez-Villaescusa 201945.9±17.8Stenosis=Not reportedNot reportedNot reported.019
      Maragkos 2020b33.6Spondylolisthesis=37180OR: 0.5 (0.3–0.8).001 (univariate)

      .003 (multivariate logistic regression)
      Lee 201546.1Degree of spinal stenosis (none/mild vs. moderate/severe)=Not reportedNot reportedOR: 7.4 (2.0–36.3)Cephalad segment:
      • -
        CASD: 0.377
      • -
        RASD: 0.875
      Caudad (L5–S1) segment:
      • -
        CASD: 0.015
      • -
        RASD: 0.026
      OR: 0.008
      Procedure
      Maragkos 2020b33.6- Laminotomy=23

      - Laminectomy=123

      - Foraminotomy=15

      - Diskectomy=78
      - 41

      - 337

      - 53

      - 264
      Not reported- .05

      - .57

      - .43

      - .03
      Heo 201571.8- IBF + PLF=2

      - IBF alone=21

      - PLF alone=10
      - 82

      - 245

      - 18
      4.93 (2.338–10.409) (univariate cox proportional hazard ratio)

      3.85 (1.792–8.254) (multivariate cox proportional hazard ratio)
      - <.001
      Lee 201346.8±22.8- PLIF=24

      - Hybrid=6
      - 26

      - 19
      0.24 (0.09–0.88) (odds ratio).03

      Lee 201451Not reportedNot reported3.392 (1.079–10.666) (multivariate cox proportional hazards).037 (cox proportional hazard)

      .048 (univariate analysis)
      Liang 2014≥60- PLF=25

      - PLIF=3
      - 52

      - 4
      Not reported.577
      Anandjiwala 201167.4- PLF=5

      - PLIF=2

      - Both=7
      - 29

      - 14

      - 11
      Not reported.100
      Bae 201059.2±14.6- Mini-ALIF=10

      - Mini-TLIF=1
      - 65

      - 27
      Not reported.141

      Min 200844.6- ALIF=11

      - PLIF=19

      - TLIF=0
      - 14

      - 3

      - 1
      Not reported- .008

      - .003

      - .375
      Ou 201523.8±19.2- PLIF=8

      - TLIF=1

      - PLF=4
      - 111

      - 24

      - 42
      Not reported- <.99

      - <.99

      - .52
      Ramirez-Villaescusa 201945.9±17.8Not reportedNot reportedNot reported.220
      Soh 2013102- PLF=11

      - PLIF=10
      - 13

      - 21
      OR: 0.821 (0.101 - 6.680).304

      OR: 0.8535
      Wang 201731.2- TLIF=6

      - PLIF=9
      - 92

      - 130
      Not reported.913
      Yugué 201677.3Not reportedNot reportedNot reported.4737
      Zhong 201728.6±16.8- PLF=8

      - TLIF & PLF=6

      - ALIF & PLF=4

      - XLIF & PLF=0
      - 56

      - 70

      - 9

      - 1
      Not reported.121
      Zhong 201728.6±16.8- Posterior=14

      - Anterior & Posterior=4

      - Lateral & Posterior=0
      - 126

      - 9

      - 1
      Not reported.078
      Approach
      Shin 2007Not reportedNot reportedNot reportedNot reported.487
      Maragkos 2020b33.6- Anterior=8

      - Posterior=88

      - Anterior + posterior=71
      - 29

      - 203

      - 169
      Not reported.55
      Number of fused levels
      Maragkos 2020b33.61.83±1.091.76±0.83Not reported.73
      Shin 2007Not reportedNot reportedNot reportedNot reported.087
      Kim 201620.51.68±0.621.68±0.62Not reported1.00
      Lee 201451Not reportedNot reported- 2 vs 1: 1.393 (0.555–3.494)

      - 3 vs 1: 0.659 (0.80–5.432)

      (multivariate cox proportional hazards)
      .670

      - 2 vs 1: 0.480

      - 3 vs 1: 0.699

      .796 (univariate analysis)
      Lee 201546.1Not reportedNot reportedNot reportedCephalad segment:
      • -
        CASD: 0.288
      • -
        RASD: 0.430
      Caudad (L5–S1) segment:
      • -
        CASD: 0.091
      • -
        RASD: 0.493
      Liang 2014≥601.50±0.691.57±0.63Not reported.637
      Tienboon 201050.45.5mm diameter rod:
      • -
        1: 0
      • -
        2: 0
      • -
        3: 0
      • -
        4: 4
      • -
        5: 0
      • -
        6: 0
      • -
        7: 0
      • -
        8: 0
      6.0mm diameter rod:

      - 1: 1

      - 2: 2

      - 3: 4

      - 4: 2

      - 5: 2

      - 6: 0

      - 7: 0

      - 8: 0
      5.5 mm diameter rod:
      • -
        1: 23
      • -
        2: 28
      • -
        3: 27
      • -
        4: 13
      • -
        5: 5
      • -
        6: 5
      • -
        7: 1
      • -
        8: 2
      6.0mm diameter rod:

      - 1: 19

      - 2: 11

      - 3: 15

      - 4: 10

      - 5: 6

      - 6: 3

      - 7: 4

      - 8: 0
      Not reported>.05
      Anandjiwala 201167.4

      - Short (1–2 levels)=8

      - Long (>3 levels)=6
      - 42

      - 12
      Not reported.119

      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)- <4 levels=19

      - >4 levels=57
      - 329

      - 225
      Not reported<.001
      Bydon 201439.73±46.52Not reportedNot reportedNot reported.081
      Ghiselli 200480.4Not reportedNot reported3.4 (1.83–6.23) (cox proportional hazards model)<.001
      Ha 201375.4Not reportedNot reportedNot reported.7749
      Hyun 2007731.5±0.81.3±0.6Not reportedNot reported
      Ou 201523.8±19.21.7±0.81.4±0.6Not reported.13
      Ou 201523.8±19.2- Single=7

      - <1 level=6
      - 107

      - 70
      Not reported.64
      Ramirez-Villaescusa 201945.9±17.8Not reportedNot reported.009
      Soh 2013102- One level=8

      - 2 or 3 levels=13
      - 18

      - 16
      OR: 0.878 (0.109 - 7.097).284

      OR: 0.9026
      Wang 201731.2- One level=11

      - Two levels=4
      - 167

      - 55
      Not reported.539
      Zhong 201728.6±16.8- One level=12

      - Two levels=6
      - 80

      - 56
      Not reported.524
      Number of operated laminae
      Kawaguchi 200764.8- 2 levels=1

      - 3 levels=5

      - 4 levels=2

      - 5 levels=0
      - 8

      - 42

      - 10

      - 3
      Not reported.86
      Kawaguchi 200764.83.1±0.63.1±0.7Not reported1.0
      Number of decompressed levels
      Ma 201936Not reportedNot reported2.080 (1.208–3.580) (multivariate cox proportional hazards).008
      Ha 201375.4Not reportedNot reportedNot reported.7677
      Maragkos 2020b33.60.55±0.840.63±0.78Not reported.06
      Fused levels
      Olvera 201539- ISTP L4/L5=6

      - ISTEP L3/L4=1

      - ISTEP L3/L5=3

      - L4/S1=5

      - L2/S1=2

      - L3/S1=1

      - L5/S1=2
      Not reportedNot reportedNot reported
      Shin 2007Not reported- L2–L3–L4=1

      - L3–L4=9

      - L3–L4–L5=4

      - L4–L5=10

      - L5–S1=0

      - L4–L5–S1=2
      Not reportedNot reported.548
      Anandjiwala 201167.4- Floating=10

      - Lumbosacral=4
      - 33

      - 21
      Not reported.453

      Bae 201059.2±14.6

      - L4–L5=5

      - L5–S1=6
      - 46

      - 46
      Not reported.514

      Bydon 201439.73±46.52- Floating=49

      - Lumbosacral=31
      - 207

      - 224
      Not reported.030

      Choi 2014134.2- L4–L5=10

      - L5–S1=9
      - 19

      - 11
      Not reported.46
      Disch 2008165.6- L4–L5=10

      - L4–S1=7

      - L5–S1=10
      - 12

      - 22

      - 41
      Not reported<.05
      Sakaura 201366.8- Floating=20

      - Lumbosacral=4
      - 11

      - 25
      Not reportedNot reported (nonsignificant)
      Wang 201731.2- L4–L5=5

      - L5–S1=6

      - L4–S1=4
      - 75

      - 92

      - 55
      Not reported.986
      Zhong 201728.6±16.8- L3–L4=1

      - L4–L5=7

      - L5–S1=4

      - L3–L5=1

      - L4–S1=5
      - 1

      - 44

      - 35

      - 12

      - 44
      Not reported.488
      Heo 201571.8- Floating=30

      - Lumbosacral=3
      - 271

      - 74
      0.29 (0.087–0.955) (univariate cox proportional hazard ratio).042
      Ha 201459.4±39.9Below the proximal neutral vertebrae=12

      Not extending over the proximal neutral vertebrae=4
      - 17

      - 26
      Not reported.015
      Ma 201936Not reportedNot reported0.976 (0.616–1.548) (cox proportional hazard ratio).918
      Bone grafts use
      Liang 2014≥60Allograft=1931Not reported.271
      Maragkos 2020b33.6Allograft=60233Not reported.003
      Maragkos 2020b33.6BMPs=49178Not reported.18
      Zhong 201728.6±16.8BMPs=312Not reported.292
      Zhong 201728.6±16.8- Autograft=14

      - Allograft=0

      - Autograft & allograft=4
      - 98

      - 4

      - 34
      Not reported.772
      Superior facet joint violation
      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)Yes=55

      No=21
      Yes=41

      No=513
      Not reported<.001
      Choi 2014134.2Yes=8

      No=11
      Yes=16

      No=14
      Not reported.09
      Wang 201731.2Yes=12

      No=3
      Yes=36

      No=186
      OR: 2.016 (2.885–18.412)<.001
      Decompression outside fusion construct
      Lee 201451Not reportedNot reported0.867 (0.115–6.535) (multivariate cox proportional hazards).890
      Maragkos 2020a21 (median)Yes=22

      No=11
      Yes=52

      No=46
      OR: 2.68 (1.05–6.86).39
      Maragkos 2020b33.6Yes=81

      No=86
      Yes=151

      No=250
      OR: 2.6 (1.6–4.1).02

      OR:<0.001
      Zhong 2017

      28.6±16.8Yes=7

      No=11
      Yes=16

      No=120
      Not reported.002
      Instrumentation
      Hyun 200773Yes=50

      No=11
      Yes=128

      No=12
      Not reportedNot reported
      Ghiselli 200480.4Not reportedNot reportedNot reported.47
      Other operative details
      Fixed VertebraeMa 201936Not reportedNot reported0.634 (0.303–1.326).226
      Addition of interbody fusionMaragkos 2020a21 (median)Yes=6

      No=27
      Yes=27

      No=71
      OR: 0.44 (0.14–01.34).146
      Rod diameterTienboon 201050.4- 5.5 mm=4

      - 6.0 mm=11
      - 104

      - 68
      Not reported.011
      Use of interbody fusion devicesMaragkos 2020b33.6Yes=96

      No=71
      Yes=255

      No=146
      Not reported.17
      Whether floating fusion was also performedHa 201375.4Not reportedNot reportedNot reported.8936

      Facet sparing or abutting

      Anandjiwala 201167.4- Facet sparing=10

      - Facet abutting=4
      - 38

      - 16
      Not reported.946

      Rigid or dynamic instrumentationBagheri 201951±2.2 (ASD), 52±2.3 (No ASD)- Rigid=56

      - Dynamic=20
      - 375

      - 179
      Not reported<.001
      Integrity of the posterior complexLai 2004≥72- Integrity=

      - Nonintegrity=17/70
      - 29

      - 53
      Not reported.034
      Type of pedicle instrumentation (top-loading vs. side-loading screws)Ramirez-Villaescusa 201945.9±17.8Not reportedNot reportedHR: 2.983 (1.548–5.748).001
      Pedicle screw instrumentationOu 201523.8±19.2Yes=8

      No=5
      Yes=91

      No=86
      Not reported.49
      Age
      Olvera 201539- 40–49: 3

      - 50–59: 9

      - 60–69: 3

      - 70–79: 4

      - 80–89: 1

      - 90–99: 0
      Not reportedNot reportedNot reported
      Shin 2007Not reportedNot reportedNot reportedNot reported.117
      Tienboon 201050.4- 50–59: 4

      - 60–69: 8

      - 70–79: 3
      - 50–59: 62

      - 60–69: 64

      - 70–79: 46
      Not reported>.05
      Heo 201571.862.79±8.2258.66±9.891.06 (1.016–1.095) (univariate cox proportional hazard ratio)

      1.07 (1.021–1.123) (multivariate cox proportional hazard ratio)
      .005
      Kawaguchi 200764.854.5±12.655.9±12.0Not reported.76
      Lee 201346.8±22.8- Age<65=15

      - Age≥65=15
      - 18

      - 27
      OR: 0.66 (0.24–1.77).41
      Lee 201451Not reportedNot reported2.534 (1.053–6.101) (multivariate cox proportional hazards).038

      (multivariate cox proportional hazard)

      .034 (univariate analysis)
      Lee 201546.1Not reportedNot reportedNot reportedCephalad segment:
      • -
        CASD: 0.110
      • -
        RASD: 0.997
      Caudad (L5–S1) segment:
      • -
        CASD: 0.652
      • -
        RASD: 0.813
      Liang 2014≥6061.4±12.062.1±10.3Not reported.767
      Makino 201841.0±13.268.2±8.966.5±8.9Not reported.92
      Maragkos 2020a21 (median)- Rostral ASD=53 (median)

      - Bilateral ASD=56 (median)

      - Caudal ASD=60 (median)
      Not reportedOR: 0.95 (0.92–0.99).011
      Maragkos 2020b33.655±1256±14Not reported.40
      Anandjiwala 201167.4- <64 y=4

      - >64 y=10
      - 16

      - 38
      Not reported.517
      Bae 201059.2±14.6

      46.448.7Not reported.313

      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)61.37±4.1262.37±3.9Not reported.79
      Chen 201139.362.8±1049.6±9Not reported.03
      Choi 2014134.250.7±9.448.9±9.4Not reported.38
      Ghiselli 200480.4Not reportedNot reportedNot reported.13
      Ha 201375.4Not reportedNot reportedNot reported.0364
      Hyun 20077357±1251±12Not reported.002
      Lee 2009≥1258.458.2Not reported.894
      Min 200844.651.6±7.756.2±9.6Not reported.0299
      Ou 201523.8±19.263.2±15.565.2±12.5Not reported.58
      Ou 201523.8±19.2- >60=9

      - <60=4
      - 117

      - 60
      Not reported<.99
      Ramirez-Villaescusa 201945.9±17.8Not reportedNot reportedNot reported.058
      Sakaura 201366.853.5±12.659.1±15.1Not reported>.01 (nonsignificant)
      Soh 2013102- <50=7

      - ≥50=14
      - 11

      - 23
      OR: 3.284 (0.508–21.241).561

      OR: 0.2131
      Wang 201731.255.3±10.553.1±10.9.438
      Yugué 201677.3Not reportedNot reportedNot reported.3989
      Zhong 201728.6±16.859.8±14.158.2±13.4Not reportedNot reported
      Gender
      Olvera 201539Not reportedNot reportedNot reportedNot reported
      Shin 2007Not reportedNot reportedNot reportedNot reported.746
      Tienboon 201050.4Not reportedNot reportedNot reported>.05
      Heo 201571.8- Males=14

      - Females=19
      111

      234
      1.35 (0.675–2.689) (univariate cox proportional hazard ratio).398
      Kawaguchi 200764.8- Males=7

      - Females=1
      - 46

      - 17
      Not reported.38
      Lee 201346.8±22.8- Males=15

      - Females=15
      - 15

      - 30
      OR: 0.51 (0.19–1.37).18
      Lee 201451Not reportedNot reported0.540 (0.239–1.221) (multivariate cox proportional hazards).139 (multivariate) .159 (univariate)

      Lee 201546.1Not reportedNot reportedNot reportedCephalad segment:
      • -
        CASD: 0.157
      • -
        RASD: 0.539
      Caudad (L5–S1) segment:
      • -
        CASD: 0.372
      • -
        RASD: 0.064
      Liang 2014≥60- Males=11

      - Females=17
      - 18

      - 38
      Not reported.516
      Makino 201841.0±13.2- Males=2

      - Females=3
      - 12

      - 24
      Not reported>.99
      Maragkos 2020a21 (median)- Males=8

      - Females=25
      - 45

      - 53
      OR: 3.55 (1.34–9.44).011
      Maragkos 2020b33.6- Males=70

      - Females=97
      - 195

      - 206
      Not reported.14
      Anandjiwala 201167.4- Males=4

      - Females=10
      - 9

      - 45
      Not reported.244

      Bae 201059.2±14.6

      - Males=4

      - Females=7
      - 35

      - 57
      Not reported.595

      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)- Males=33

      - Females=43
      - 270

      - 284
      Not reported.395
      Choi 2014134.2- Males=6

      - Females=13
      - 8

      - 22
      Not reported.65
      Ghiselli 200480.4Not reportedNot reportedNot reported.92
      Ha 201375.4Not reportedNot reportedNot reported.3031
      Hyun 200773- Males=19

      - Females=42
      - 50

      - 90
      Not reportedNot reported
      Min 200844.6- Males=9

      - Females=21
      - 5

      - 13
      Not reported.869
      Ou 201523.8±19.2- Males=6

      - Females=7
      - 79

      - 98
      Not reported.92
      Ramirez-Villaescusa 201945.9±17.8Not reportedNot reportedNot reported.096
      Sakaura 201366.8- Males=2
      • -
        Females=2
      • -
        24
      • -
        12
      Not reported>.01 (nonsignificant)
      Soh 2013102- Males=7

      - Females=14
      - 11

      - 23
      OR: 1.026 (0.257–4.088).940

      OR: 0.9712
      Wang 201731.2- Males=6

      - Females=9
      - 100

      - 122
      Not reported.704
      Yugué 201677.3Not reportedNot reportedNot reported.3530
      Zhong 201728.6±16.8- Males=5

      - Females=13
      - 39

      - 97
      Not reported.370
      Body height
      Kim 201620.5158.34±7.87159.98±7.18Not reported.39
      Min 200844.61.57±0.11.59±0.1Not reported.5631
      Body weight
      Kim 201620.562.44±9.460.84±9.29Not reported.39
      Min 200844.662.1±9.366.1±11.7Not reported.2069
      BMI
      Kim 201620.524.86±2.7823.70±2.74OR: 1.353 (1.081–1.695).04

      .008 (multivariate regression)
      Liang 2014≥6027.9±2.325.2±3.3OR: 1.75 (1.18–2.61).000

      .006 (multivariate regression)
      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)27.8623.15Not reported.033
      Ha 201375.4Not reportedNot reportedNot reported.0543
      Hyun 20077325±324±3Not reportedNot reported
      Min 200844.625.2±3.226.2±3.7Not reported.3152
      Ou 201523.8±19.27.8±2.8

      - BMI≥25=12

      - BMI>25=1
      24.4±2.8

      - 89

      - 88
      OR: 1.68 (1.27–2.21)>.001

      .003
      Wang 201731.227.7±2.024.1±1.8OR: 1.359 (1.681–6.431).038

      OR: 0.002
      Yugué 2016

      77.3- BMI≥25 kg/m2=32.5%

      - BMI<25 kg/m2=21.1%
      Not reportedHR: 3.12 (1.18–8.49).0497

      HR: 0.0212
      BMD (T-score)
      Kim 201620.5-2.38±0.91-2.26±1.41Not reported.69
      Min 200844.6-1.0±1.3-1.7±1.5Not reported.1033
      Lee 201546.1Not reportedNot reportedNot reportedCephalad segment:
      • -
        CASD: 0.987
      • -
        RASD: 0.794
      Caudad (L5–S1) segment:
      • -
        CASD: 0.255
      • -
        RASD: 0.185
      BMD (score type not reported)
      Chen 201139.3-1.23±0.23-1.12±0.19Not reported.08
      Ha 201375.4Not reportedNot reportedNot reported.2370
      Wang 201731.2-1.0±0.2-1.2±0.3Not reported.413
      Medical comorbidities
      OsteoporosisMaragkos 2020a21 (median)Yes=2

      No=31
      Yes=2

      No=96
      Not reported.23
      Maragkos 2020b33.6Yes=5

      No=162
      Yes=9

      No=392
      Not reported.51

      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)Yes=23

      No=53
      Yes=174

      No=380
      Not reported.896
      Zhong 2017

      28.6±16.8Yes=0

      No=18
      Yes=12

      No=124
      Not reported.362
      Bydon 201439.73±46.52Not reportedNot reportedNot reported.369
      Diabetes mellitusMaragkos 2020a21 (median)Yes=6

      No=27
      Yes=21

      No=77
      Not reported.70
      Maragkos 2020b33.6Yes=17

      No=150
      Yes=53

      No=348
      Not reported.46
      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)Yes=14

      No=62
      Yes=146

      No=408
      Not reported.086
      Ou 201523.8±19.2Yes=3

      No=10
      Yes=32

      No=145
      Not reported.71
      Zhong 2017

      28.6±16.8Yes=1

      No=17
      Yes=12

      No=124
      Not reported.639
      HypertensionBagheri 201951±2.2 (ASD), 52±2.3 (No ASD)Yes=22

      No=54
      Yes=124

      No=430
      Not reported.245
      Ou 201523.8±19.2Yes=5

      No=8
      Yes=69

      No=108
      Not reported.97
      Zhong 2017

      28.6±16.8Yes=7

      No=11
      Yes=43

      No=93
      Not reported.536
      DepressionBydon 201439.73±46.52Not reportedNot reportedNot reported.490
      Zhong 2017

      28.6±16.8Yes=3

      No=15
      Yes=28

      No=108
      Not reported.697
      Coronary artery diseaseOu 201523.8±19.2Yes=0

      No=13
      No=5

      No=172
      Not reported<.99
      Medical comorbiditiesHa 201375.4Not reportedNot reportedNot reported.2766
      Zhong 2017

      28.6±16.8- Obesity=7

      - Heart diseases=1

      - Pulmonary diseases=3

      - Genitourinary diseases=3

      - Gastrointestinal disease=6

      - Anemia=1

      - Hyperlipidemia=5

      - Hypothyroidism=4

      - Osteoarthritis=4
      - 47

      - 4

      - 29

      - 17

      - 35

      - 5

      - 37

      - 23

      - 37
      Not reported- .718

      - .468

      - .767

      - .464

      - .493

      - .498

      - .959

      - .524

      - .782
      Smoking
      Liang 2014≥60Yes=8

      No=20
      Yes=10

      No=46
      Not reported.259
      Maragkos 2020a21 (median)Yes=7

      No=23
      Yes=21

      No=71
      Not reported.42
      Maragkos 2020b33.6Yes=36

      No=131
      Yes=77

      No=324
      Not reported.30

      Bagheri 201951±2.2 (ASD), 52±2.3 (No ASD)Yes=26

      No=50
      Yes=157

      No=397
      Not reported.19
      Bydon 201439.73±46.52Not reportedNot reportedNot reported.440
      Zhong 2017

      28.6±16.8Yes=6

      No=12
      Yes=34

      No=102
      Not reported.449
      JOA score
      Makino 201841.0±13.2
      • -
        Preoperative=15.0±4.1
      • -
        Best After Surgery=27.6±1.7
      • -
        Final=24.0±5.0
      • -
        14.2±4.0
      • -
        27.0±2.4
      • -
        26.4±3.4
      Not reported
      • -
        .75
      • -
        .60
      • -
        .52
      Min 200844.6- Preoperative=9.6±1.8

      - Postoperative 2–3 m=13.0±1.0

      - Postoperative 1 y=13.6±1.1

      - Final=13.4±1.0
      - 8.9±1.2

      - 13.8±0.7

      - 13.6±1.3

      - 13.7±0.8
      Not reported.1767

      .0055

      .8091

      .3530
      Sakaura 201366.8Preoperative=13.3±6.816.0±3.7Not reported>.01 (nonsignificant)
      Operative time
      Ou 201523.8±19.26.8±1.1 hours6.4±1.7Not reported.37
      Wang 201731.2165.0±10.3 minutes160.1±13.3Not reported.985
      Blood loss
      Ou 201523.8±19.2561.5±401.6550.8±384.4Not reported.92
      Wang 201731.2457.9±27.7445.5±30.8Not reported.391
      Follow-up period
      Makino 201841.0±13.248.6±15.4 m40.0±12.3 mNot reported.034
      Bae 201059.2±14.6Clinical=68.5 m

      Radiographic=66.4 m
      58.1 m

      50.1 m
      Not reported.025

      .016
      Other variables
      Length of stayOu 201523.8±19.28.6±2.38.2±2.1Not reported.51
      AlcoholZhong 201728.6±16.8Yes=8

      No=10
      No=68

      No=68
      Not reported.658
      ResidenceSoh 2013102- Urban=12

      - Rural=9
      - 23

      - 11
      OR: 0.499 (0.128–1.954).431

      OR: 0.3185
      Duration of disease (m)Wang 201731.215.1±9.712.1±7.8Not reported.140
      Mean recovery rateMin 200844.664.7±1.077.1±14.4Not reported.1787
      Success rate (%)Min 200844.686.794.4Not reported.637
      Complication rate (%)Min 200844.63.316.7Not reported.142
      Correlation between ASD and clinical symptomSoh 2013102- Satisfactory=18

      - Unsatisfactory=3
      - 26

      - 8
      Not reported.405
      Spondylolisthesis levelsZhong 201728.6±16.8- L3–L4=2

      - L4–L5=11

      - L5–S1=5

      - L4–S1=0
      - 2

      - 82

      - 47

      - 5
      Not reported.087

      Meta-analysis of risk factors

      Different risk factors for ASD were inconsistent among individual studies. Not all the risk factors were fit for meta-analysis.

      Age, gender, and BMI

      Fourteen studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Chen BL
      • Wei FX
      • Ueyama K
      • Xie DH
      • Sannohe A
      • Liu SY.
      Adjacent segment degeneration after single-segment PLIF: the risk factor for degeneration and its impact on clinical outcomes.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] with 501 ASD patients and 2,299 non-ASD patients were included in the meta-analysis for age at the time of surgery as a possible risk factor for ASD. Patients who developed ASD were slightly older than patients without ASD with no statistical significance (mean difference [MD]=0.17 years; 95% confidence interval [CI]=-0.60 to 0.94; p=.67; I2=79%).
      Regarding gender, eighteen studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kawaguchi Y
      • Ishihara H
      • Kanamori M
      • Yasuda T
      • Abe Y
      • Nogami S
      • et al.
      Adjacent segment disease following expansive lumbar laminoplasty.
      ,
      • Lee CH
      • Hyun SJ
      • Kim KJ
      • Jahng TA
      • Yoon SH
      • Kim HJ.
      The efficacy of lumbar hybrid stabilization using the DIAM to delay adjacent segment degeneration: an intervention comparison study with a minimum 2-year follow-up.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] were included in the meta-analysis. The incidence of ASD was not significantly different between males and females (Odds ratio [OR]=0.91; 95% CI=0.75–1.11; p=.36; I2=0%).
      BMI was analyzed in six studies [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Hyun SJ
      • Kim YB
      • Hong HJ
      • Kwon JT
      • Suk JS
      • Min BK.
      Predictable risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] with 197 ASD patients and 663 non-ASD patients. Patients with ASD had a statistically significant higher BMI than patients without ASD (MD=1.97 kg/m2; 95% CI=1.49–2.45; p<.001; I2=83%) (Fig. 2).
      Fig 2
      Fig. 2Forest plots of meta-analysis of age, gender, and BMI.

      Smoking, medical comorbidities, and preoperative Japanese Orthopaedic Association for low back pain (JOA) score

      Five studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ] compared the incidence of ASD in smokers and nonsmokers. Overall, the incidence of ASD was higher in smokers than nonsmokers with no statistical significance (OR=1.26; 95% CI=0.94–1.68; p=.12; I2=0%).
      Analysis of diabetes was available in five studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ] which showed a nonstatistically significant higher incidence of ASD in nondiabetic patients (OR=0.73; 95% CI=0.51–1.05; p=.09; I2=0%).
      Hypertension was included in three studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ], with a higher incidence of ASD in patients with hypertension than patients without hypertension (OR=1.33; 95% CI=0.86–2.06; p=.20; I2=0%).
      Osteoporosis was analyzed in four studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ], and the incidence of ASD was not statistically different between osteoporotic and nonosteoporotic patients (OR=1.00; 95% CI=0.64–1.57; p=.99; I2=0%).
      The T-score representing the bone mineral density (BMD) was analyzed in two studies [
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ] with 80 ASD patients and 68 non-ASD patients with no statistical significance (MD=0.21; 95% CI=-0.58–1.00; p=.60; I2=65%).
      Also, the preoperative JOA score for low back pain was assessed in three studies [
      • Makino T
      • Honda H
      • Fujiwara H
      • Yoshikawa H
      • Yonenobu K
      • Kaito T.
      Low incidence of adjacent segment disease after posterior lumbar interbody fusion with minimum disc distraction: a preliminary report.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ] with 39 ASD patients and 90 non-ASD patients with no statistically significant difference, (MD=0.65; 95% CI=-0.17–1.48; p=.12; I2=0%) (Fig. 3).
      Fig 3:
      Fig. 3Meta-analysis of smoking, medical comorbidities, and preoperative JOA score for low back pain.

      Operative risk factors

      With pooled data from different studies, three operative variables were found to be significant risk factors for ASD. Lumbar fusions excluding the sacrum (floating fusions), was associated with a statistically significant risk of developing ASD compared to distal fusions including the sacrum (OR=1.78; 95% CI=1.32–2.41; p<.001; I2=48%) as assessed in nine studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Bae JS
      • Lee SH
      • Kim JS
      • Jung B
      • Choi G.
      Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Heo Y
      • Park JH
      • Seong HY
      • Lee YS
      • Jeon SR
      • Rhim SC
      • et al.
      Symptomatic adjacent segment degeneration at the L3-4 level after fusion surgery at the L4-5 level: evaluation of the risk factors and 10-year incidence.
      ,
      • Sakaura H
      • Yamashita T
      • Miwa T
      • Ohzono K
      • Ohwada T.
      Symptomatic adjacent segment pathology after posterior lumbar interbody fusion for adult low-grade isthmic spondylolisthesis.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ]. Additionally, three studies [
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ,
      • Choi KC
      • Kim JS
      • Shim HK
      • Ahn Y
      • Lee SH.
      Changes in the adjacent segment 10 years after anterior lumbar interbody fusion for low-grade isthmic spondylolisthesis.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] found that iatrogenic superior facet joint violation during screw placement was associated with a statistically significant high incidence of ASD (OR=10.43; 95% CI=6.4–17.01; p<.001; I2=95%). Decompression outside fusion construct was also found to be a significant risk factor for ASD (OR=1.72; 95% CI=1.25–2.37; p<.001; I2=46%) as assessed in three studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Maragkos GA
      • Atesok K
      • Papavassiliou E.
      Prognostic factors for adjacent segment disease after L4-L5 lumbar fusion.
      ,
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ] (Fig. 4).
      Fig 4
      Fig. 4Meta-analysis of lumbar fusion type, superior facet joint violation, and decompression outside fusion construct.
      The pooled data from four studies [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Anandjiwala J
      • Seo JY
      • Ha KY
      • Oh IS
      • Shin DC.
      Adjacent segment degeneration after instrumented posterolateral lumbar fusion: a prospective cohort study with a minimum five-year follow-up.
      ,
      • Liang J
      • Dong Y
      • Zhao H.
      Risk factors for predicting symptomatic adjacent segment degeneration requiring surgery in patients after posterior lumbar fusion.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ] and three studies [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Min JH
      • Jang JS
      • Jung B
      • Lee HY
      • Choi WC
      • Shim CS
      • et al.
      The clinical characteristics and risk factors for the adjacent segment degeneration in instrumented lumbar fusion.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] did not find a statistically significant difference between PLF versus PLIF (OR=1.28; 95% CI=0.65–2.51; p=.48; I2=0%) and PLIF versus TLIF (OR=1.45; 95% CI=0.59–3.56; p=.42; I2=15%), respectively.
      Similarly, there was no statistically significant difference when comparing single versus multiple-level procedures (OR=0.87; 95% CI=0.50–1.51; p=.62; I2=0%) as assessed in four studies [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ,
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Soh J
      • Lee JC
      • Shin BJ.
      Analysis of risk factors for adjacent segment degeneration occurring more than 5 years after fusion with pedicle screw fixation for degenerative lumbar spine.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ], intra-operative blood loss (MD=12.39; 95% CI=-2.17–26.95; p=.10; I2=0%) as assessed in two studies [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ], or operative time (MD=5.29; 95% CI=-0.15–10.74; p=.06; I2=1%) as assessed in the same two studies [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ,
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] (Fig. 5).
      Fig 5
      Fig. 5Meta-analysis of procedure type and number of levels, intraoperative blood loss, and operative time.

      Evidence summary

      The quality of evidence for each risk factor analyzed was low to very low. Such quality precludes a definitive conclusion regarding the impact of those risk factors for increasing the incidence of ASD following lumbar fusion surgeries. Regarding the risk of bias domain, there were serious limitations for all the risk factors. Moreover, some of the risk factors had moderate or considerable unexplained heterogeneity or inconsistency of results. There were also serious limitations in the imprecision domain in some risk factors. All these factors led to low to very low-quality evidence (Table4).
      Table 4Summary of the quality of evidence
      Risk factorRisk of biasInconsistencyIndirectnessImprecisionPublicationbiasQuality ofevidence
      AgeSerious limitations,

      downgraded 1 level
      Considerable, downgraded by 2 levelsNo serious limitationsNo serious limitationsNo serious limitationsVery low
      GenderSerious limitations,

      downgraded 1 level
      LowNo serious limitationsNo serious limitationsNo serious limitationsLow
      BMISerious limitations,

      downgraded 1 level
      Considerable, downgraded by 2 levelsNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      SmokingSerious limitations,

      downgraded 1 level
      LowNo serious limitationsNo serious limitationsNo serious limitationsLow
      DiabetesSerious limitations,

      downgraded 1 level
      LowNo serious limitationsNo serious limitationsNo serious limitationsLow
      HypertensionSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      OsteoporosisSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      BMD (T-score)Serious limitations,

      downgraded 1 level
      Considerable, downgraded by 2 levelsNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      Pre-operative JOA scoreSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations, downgraded 2 levelsNo serious limitationsVery low
      Floating vs. lumbosacral fusionSerious limitations,

      downgraded 1 level
      Moderate, downgraded by 1 levelNo serious limitationsNo serious limitationsNo serious limitationsVery low
      Superior facet violationSerious limitations,

      downgraded 1 level
      Considerable, downgraded by 2 levelsNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      Decompression outside fusion constructSerious limitations,

      downgraded 1 level
      Moderate, downgraded by 1 levelNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      PLF vs. PLIFSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations, downgraded 2 levelsNo serious limitationsVery low
      PLIF vs. TLIFSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations, downgraded 1 levelNo serious limitationsVery low
      Single vs. multiple levelsSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      Intra-operative blood lossSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low
      Operative timeSerious limitations,

      downgraded 1 level
      LowNo serious limitationsSerious limitations,

      downgraded 1 level
      No serious limitationsVery low

      Discussion

      Lumbar fusion surgeries are among the most frequent surgical procedures with an increasing yearly trend with the development of new fusion procedures and better imaging modalities [
      • Rajaee SS
      • Bae HW
      • Kanim LE
      • Delamarter RB.
      Spinal fusion in the United States: analysis of trends from 1998 to 2008.
      ]. ASD is one of the long-term complications following lumbar fusion and should be carefully observed and followed to ensure patient safety [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ].
      In the current systematic review, the overall rate of ASD following lumbar fusions was 17.2%. The pooled results of the meta-analysis showed that higher BMI, floating fusion, violation of the superior facet joint, and decompression outside fusion construct were associated with a significant risk of development of ASD. Other factors including age, gender, smoking, diabetes, hypertension, osteoporosis, preoperative JOA score, approach, number of levels, intra-operative blood loss, and operative time were not associated with a significant increase in the rate of ASD.
      BMI is widely used in the preoperative assessment prior to spine surgeries, and obesity is associated with higher complication and reoperation rates following lumbar spine surgeries [
      • Goyal A
      • Elminawy M
      • Kerezoudis P
      • Lu VM
      • Yolcu Y
      • Alvi MA
      • et al.
      Impact of obesity on outcomes following lumbar spine surgery: a systematic review and meta-analysis.
      ]. The current meta-analysis found that higher BMI increases the risk of ASD development. Kim et al. [
      • Kim JY
      • Ryu DS
      • Paik HK
      • Ahn SS
      • Kang MS
      • Kim KH
      • et al.
      Paraspinal muscle, facet joint, and disc problems: risk factors for adjacent segment degeneration after lumbar fusion.
      ] reported that high BMI was a significant risk factor for developing ASD following posterior lumbar fusion after comparing 50 patients with ASD and 50 patients without ASD. Similarly, Ou et al. [
      • Ou CY
      • Lee TC
      • Lee TH
      • Huang YH.
      Impact of body mass index on adjacent segment disease after lumbar fusion for degenerative spine disease.
      ] reported a significantly higher incidence of ASD in patients with high BMI undergoing different lumbar fusions, including PLIF, TLIF, and PLF, with a 67.6% increase in ASD rate for each 1 mean value increase in BMI. With lumbar fusion, there is a significant elevation in the intradiscal pressure, motion, and mechanical stress to the adjacent levels [
      • Jiang S
      • Li W.
      Biomechanical study of proximal adjacent segment degeneration after posterior lumbar interbody fusion and fixation: a finite element analysis.
      ]. Increased body weight adds more stress and load on the intervertebral discs, leading to progressive degenerative changes and ASD development [
      • Takatalo J
      • Karppinen J
      • Taimela S
      • Niinimaki J
      • Laitinen J
      • Sequeiros RB
      • et al.
      Association of abdominal obesity with lumbar disc degeneration–a magnetic resonance imaging study.
      ]. Consequently, perioperative body weight control is crucial to improve the fusion outcomes and reduce the incidence of ASD.
      The lumbosacral segment (L5–S1), a transitional zone between the mobile lumbar spine and the fixed sacrum, is a region of increased stress and degenerative changes [
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ,
      • Tropiano P
      • Giorgi H
      • Faure A
      • Blondel B
      Surgical techniques for lumbo-sacral fusion.
      ]. Our meta-analysis found that including the sacral segment in the fusion construct is associated with a lower incidence of ASD compared to floating fusion.
      Bydon et al. [
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ] compared the incidence of ASD following floating fusions versus distal fusions ending at the sacrum in 511 patients who had undergone posterolateral instrumented fusion and found a higher rate of ASD requiring reoperation following floating lumbar fusions than fusions including the sacrum, 19.14% and 12.16%, respectively. The increased incidence of ASD with floating fusion may be due to the fact that fusing L5–S1 level eliminates the possibility of ASD development caudally, as the sacrum is developmentally fused. Bydon et al. [
      • Bydon M
      • Xu R
      • Santiago-Dieppa D
      • Macki M
      • Sciubba DM
      • Wolinsky JP
      • et al.
      Adjacent-segment disease in 511 cases of posterolateral instrumented lumbar arthrodesis: floating fusion versus distal construct including the sacrum.
      ] reported that all patients with ASD in the distal fusion cohort had ASD at the cephalad level, and 90% of patients with ASD in the floating fusion cohort had ASD at the cephalad level.
      Similarly, Disch et al. [
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ] reported a 45.5% incidence of ASD following L4/L5 fusion compared to 19.6% incidence in patients who had L5/S1 fusion after an average follow-up period of 14 years. In the L4–L5 cohort, 9 levels were cranial, and 4 were caudal out of 13 levels affected with ASD [
      • Disch AC
      • Schmoelz W
      • Matziolis G
      • Schneider SV
      • Knop C
      • Putzier M.
      Higher risk of adjacent segment degeneration after floating fusions: long-term outcome after low lumbar spine fusions.
      ].
      However, with fusions including the sacrum, the sacroiliac joint is considered an adjacent joint to the fused segment, and the same biomechanical principles of ASD could apply [
      • Ivanov AA
      • Kiapour A
      • Ebraheim NA
      • Goel V.
      Lumbar fusion leads to increases in angular motion and stress across sacroiliac joint: a finite element study.
      ]. According to Ha et al. [
      • Ha KY
      • Lee JS
      • Kim KW.
      Degeneration of sacroiliac joint after instrumented lumbar or lumbosacral fusion: a prospective cohort study over five-year follow-up.
      ], sacroiliac joint degeneration was more frequent in patients with fusion down to S1 compared to patients with fusion down to L5. Therefore, in fusions including the sacrum, the reduced risk of ASD compared to floating fusions should be weighed against the increased risk of sacroiliac joint degeneration.
      During lumbar fusion, simultaneous decompression outside the fusion construct may be performed in some circumstances, such as the presence of mild degenerative stenosis in an adjacent level as a prophylactic measure [
      • Hikata T
      • Kamata M
      • Furukawa M.
      Risk factors for adjacent segment disease after posterior lumbar interbody fusion and efficacy of simultaneous decompression surgery for symptomatic adjacent segment disease.
      ].
      Zhong et al. [
      • Zhong ZM
      • Deviren V
      • Tay B
      • Burch S
      • Berven SH.
      Adjacent segment disease after instrumented fusion for adult lumbar spondylolisthesis: incidence and risk factors.
      ] reported that decompression at an adjacent level is a significant risk factor for ASD development, following treatment of 154 patients with different interbody fusion approaches, including PLF, TLIF, ALIF, or LLIF. Similarly, Maragkos et al. [
      • Maragkos GA
      • Motiei-Langroudi R
      • Filippidis AS
      • Glazer PA
      • Papavassiliou E.
      Factors predictive of adjacent segment disease after lumbar spinal fusion.
      ] reported that decompression outside the fusion construct was associated with a significant increase in the incidence of ASD following treatment of 568 patients with different instrumented lumbar fusion approaches. Accordingly, it is advisable not to extend the decompression too far to the next level to avoid increased incidence of ASD.
      One of the underestimated consequences of pedicle screw insertion during lumbar fusion procedures is superior facet joint violation, which may alter the load-bearing capability and induce degenerative changes in the facet joint leading to the development of ASD [
      • Teles AR
      • Paci M
      • Gutman G
      • Abduljabbar FH
      • Ouellet JA
      • Weber MH
      • et al.
      Anatomical and technical factors associated with superior facet joint violation in lumbar fusion.
      ]. Moshirfar et al. [
      • Moshirfar A
      • Jenis LG
      • Spector LR
      • Burke PJ
      • Losina E
      • Katz JN
      • et al.
      Computed tomography evaluation of superior-segment facet-joint violation after pedicle instrumentation of the lumbar spine with a midline surgical approach.
      ] considered the superior facet joint violated if the pedicle screw or screw head is obviously within the facet joint, or the pedicle screw or screw head is within 1 mm or abutting the facet joint on CT scans. Percutaneous minimally-invasive screw placement is associated with a higher incidence of superior joint violation than open techniques [
      • Teles AR
      • Paci M
      • Gutman G
      • Abduljabbar FH
      • Ouellet JA
      • Weber MH
      • et al.
      Anatomical and technical factors associated with superior facet joint violation in lumbar fusion.
      ]. Bagheri et al. [
      • Bagheri SR
      • Alimohammadi E
      • Zamani Froushani A
      • Abdi A
      Adjacent segment disease after posterior lumbar instrumentation surgery for degenerative disease: incidence and risk factors.
      ] reported that intraoperative superior facet joint violation was a significant risk factor for ASD in their retrospective study of 630 patients who had PLIF. Wang et al. [
      • Wang H
      • Ma L
      • Yang D
      • Wang T
      • Liu S
      • Yang S
      • et al.
      Incidence and risk factors of adjacent segment disease following posterior decompression and instrumented fusion for degenerative lumbar disorders.
      ] reported the same finding after treating 237 patients with PLIF or TLIF.
      During fusion surgery, meticulous facet joint identification, exposure and proper pedicle screw insertion technique help prevent superior facet joint violation and consequently reduce the incidence of ASD. Chung et al. [
      • Chung KJ
      • Suh SW
      • Swapnil K
      • Yang JH
      • Song HR.
      Facet joint violation during pedicle screw insertion: a cadaveric study of the adult lumbosacral spine comparing the two pedicle screw insertion techniques.
      ], in a cadaveric study, reported a statistically significant higher incidence of superior facet joint violation during pedicle screw insertion using the mammillary process technique compared to the intersection technique.
      As the number of lumbar fusions continues to increase each year, long-term postoperative adverse consequences such as ASD must be identified and adequately managed by spine surgeons. The findings in the current meta-analysis are beneficial for the spine surgeons and patients as preoperative addressing the modifiable risk factors for ASD such as high BMI can reduce the incidence of ASD, improving the operative outcomes, and reducing medical costs associated with the second surgery.
      Despite the strength of this meta-analysis, this study has some limitations. The majority of studies included in the meta-analysis were retrospective studies. No randomized controlled trials have met the inclusion criteria and were included in the study. Additionally, there were heterogeneities in the included studies regarding the preoperative diagnosis, the number of fused levels, and the location of the fusion within the lumbar spine. Also, the definition of ASD, whether clinically or radiographically, was to some extent variable between the included studies, and some studies analyzed ASD based on the need for revision surgery. Moreover, some of the risk factors had only two or three studies for the meta-analysis. Also, there was considerable heterogeneity between the studies that were included for meta-analysis for BMI and superior facet joint violation.

      Conclusion

      The level of evidence was for all studies was low to very low. The current meta-analysis showed that higher preoperative BMI, floating fusion, concurrent decompression outside the fusion construct, and superior facet joint violation were significant risk factors for ASD after lumbar fusion surgeries. Given the lack of high level of evidence, prospective studies are needed to better understand the development of ASD after lumbar fusion surgery.

      Declaration of competing interests

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

      Acknowledgments

      The authors received no financial support for the research, authorship, and/or publication of this article. This study was organized by AO Spine through the AO Spine Knowledge Forum Degenerative, a focused group of international spine degenerative experts. AO Spine is a clinical division of the AO Foundation, which is an independent medically guided not-for-profit organization.

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