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A Systematic Review of Definitions and Classification Systems of Adjacent Segment Pathology

Kraemer, Paul, MD*; Fehlings, Michael G., MD, PhD, FRCSC; Hashimoto, Robin, PhD; Lee, Michael J., MD§; Anderson, Paul A., MD; Chapman, Jens R., MD; Raich, Annie, MPH; Norvell, Daniel C., PhD

doi: 10.1097/BRS.0b013e31826d7dd6
Adjacent Segment Pathology: General Topics
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Study Design. Systematic review.

Objective. To undertake a systematic review to determine how “adjacent segment degeneration,” “adjacent segment disease,” or clinical pathological processes that serve as surrogates for adjacent segment pathology are classified and defined in the peer-reviewed literature.

Summary of Background Data. Adjacent segment degeneration and adjacent segment disease are terms referring to degenerative changes known to occur after reconstructive spine surgery, most commonly at an immediately adjacent functional spinal unit. These can include disc degeneration, instability, spinal stenosis, facet degeneration, and deformity. The true incidence and clinical impact of degenerative changes at the adjacent segment is unclear because there is lack of a universally accepted classification system that rigorously addresses clinical and radiological issues.

Methods. A systematic review of the English language literature was undertaken and articles were classified using the Grades of Recommendation Assessment, Development, and Evaluation criteria.

Results. Seven classification systems of spinal degeneration, including degeneration at the adjacent segment, were identified. None have been evaluated for reliability or validity specific to patients with degeneration at the adjacent segment. The ways in which terms related to adjacent segment “degeneration” or “disease” are defined in the peer-reviewed literature are highly variable.

Conclusion. On the basis of the systematic review presented in this article, no formal classification system for either cervical or thoracolumbar adjacent segment disorders currently exists.

Consensus Statement No recommendations regarding the use of current classification of degeneration at any segments can be made based on the available literature. A new comprehensive definition for adjacent segment pathology (ASP, the now preferred terminology) has been proposed in this Focus Issue, which reflects the diverse pathology observed at functional spinal units adjacent to previous spinal reconstruction and balances detailed stratification with clinical utility. A comprehensive classification system is being developed through expert opinion and will require validation as well as peer review.

Strength of Statement: Strong

The terms “adjacent segment disease” or “adjacent segment degeneration” refer to a common clinical entity of pathological changes adjacent to a previous spinal reconstruction. A systematic review was undertaken to determine how these terms are classified and used in the peer-reviewed literature, and to search for validated or proposed classification schemes.

*Indiana Spine Group, Department of Orthopaedic Surgery, Indiana University, Carmel, IN

Division of Neurosurgery and Spine Program, University of Toronto, Toronto, Ontario, Canada

Spectrum Research, Inc., Tacoma, WA

§Department of Orthopaedics and Sports Medicine, University of Washington, Seattle, WA

Department of Orthopaedics and Rehabilitation, University of Wisconsin, Madison, WI

Harborview Medical Center, University of Washington, Department of Orthopaedics and Sports Medicine, Seattle, WA.

Address correspondence and reprint requests to Paul Kraemer, MD, Indiana Spine Group, Department of Orthopaedic Surgery, Indiana University, 13225 N Meridian St, Carmel, IN 46032; E-mail: pkraemer@indianaspinegroup.com

Acknowledgment date: April 30, 2012. First revision date: June 28, 2012. Second revision date: August 3, 2012. Acceptance date: August 3, 2012.

The manuscript submitted does not contain information about medical device(s)/drug(s).

Supported by AOSpine North America, Inc. Analytic support for this work was provided by Spectrum Research, Inc., with funding from the AOSpine North America.

One or more of the author(s) has/have received or will receive benefits for personal or professional use from a commercial party related directly or indirectly to the subject of this manuscript: for example, honoraria, gifts, consultancies, royalties, stocks, stock options, decision-making position.

Adjacent segment degeneration,” “adjacent segment disease,” and “ASD,” are terms commonly used to describe spinal degenerative pathology, which coexists in the spine after a previous spinal reconstructive procedure. In the scientific literature, the umbrella term “ASD” may be used to refer to adjacent segment degeneration, adjacent segment disease, or a number of equally poorly defined terms such as junctional disease, junctional stenosis, or transfer lesion. “Adjacent” has a variety of interpretations, including directly above or below the index level, or elsewhere in the same spinal region, but is generally not commonly used to refer to other areas of the spine, such as coexisting lumbar and cervical pathology. “Degeneration” is also poorly defined, and may separately refer to osteophyte formation, intervertebral disc degeneration, spinal stenosis, segmental instability, facet arthrosis, or significant structural deformity including kyphosis and scoliosis. Thus, although “ASD” is a commonly used term, its definition is imprecise at best.

The rate of spinal fusion, particularly that of “complex” spinal reconstruction,14 has seen a significant increase in the decade since intervertebral cages were approved in 1996. Demographic data from Medicare registries1,4 of lumbar spine stenosis and fusion surgery support a significant increase, and the US population continues to age, with 7000 new Medicare enrollees per day in 2011,5 the year in which the first “baby boomers” reached 65 years of age. Recent retrospective series suggest that both cervical and lumbar reoperation rates at an adjacent segment are roughly 1 in 36,7 to 1 in 5 to 68 at 10 years. Multilevel fusions, or second or third revisions, are associated with greater complication rates, surgical difficulty, and costs to the system.3 Together, these trends speak to a substantial increase in adjacent level surgery in upcoming years. There seems to be an urgent clinical need for a better understanding of relevant factors contributing to this increase, both to appropriately treat current pathology and to limit the development of future pathological processes at adjacent segments.

Current published literature consists largely of retrospective single-institution series6,7,9 using revision for any reason as an endpoint, with no universally applied criteria for revision. We are unaware of any literature-supported criteria for revision, and expert opinion varies widely. In addition, spinal pathology at an adjacent segment may manifest itself as separate and distinct degenerative processes, which are themselves disparate indications for primary or revision surgical intervention.

Our goal is to identify a currently accepted and independently validated classification scheme to aid in the diagnosis of adjacent segment pathology (ASP); in the absence of this, it is to assess how the peer-reviewed literature defines terms related to adjacent segment disease and degeneration. We hope to identify or develop a robust classification system that will allow for a more concise and complete understanding of the various degenerative pathologies, which together encompass “ASP.” With an improved understanding, future treatment of these disorders can be better directed.

Adjacent segment degeneration and disease must be better understood to treat them effectively, limit their development in future patients undergoing primary surgery, and maintain access to lumbar spine surgery of all types in the face of increasing government, media, and payor scrutiny. This systematic review seeks to summarize the current scientific landscape.

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MATERIALS AND METHODS

The purpose of this systematic review was to examine the following key questions (KQs) to elucidate how the terms “adjacent segment degeneration” and “adjacent segment disease” are defined or diagnosed in the published literature:

  1. To identify and describe formal systems used to evaluate or diagnose symptomatic or asymptomatic “ASD,” including those that include or are associated with patient variables (e.g., pain, neurological dysfunction) and those that are radiological classifications:
    1. Formal classification or diagnostic systems of spinal degenerative changes adjacent to a previous fusion that were developed specifically for the purpose of evaluating or diagnosing “ASD.”
    2. Formal classification or diagnostic systems of disc degeneration that are used as a surrogate for functional spinal unit degeneration next to a fusion.
  2. To determine whether the reliability and validity of these existing systems have been evaluated in previously fused patients.
  3. To summarize the methods used in the studies included in this focus issue to diagnose “adjacent segment degeneration” or “adjacent segment disease” (including specific disease processes that serve as surrogates for pathology at an adjacent segment).
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Electronic Literature Search

Systematic searches were conducted for literature published through February 2012. Details of the PubMed searches can be found in the Web appendix (see Supplemental Tables 1–3, Supplemental Digital Content 1, available at http://links.lww.com/BRS/A697).

We first sought to identify formal diagnostic or classification systems of “ASD,” that is, those that were developed by a structured process specifically for the purpose of evaluating or diagnosing spinal degeneration at an adjacent segment (KQ 1a). To do this, we conducted a search in PubMed using key words related to adjacent segment disease or degeneration and combined them with terms related to classification or diagnostic systems. The articles identified from this search were included for full-text review if they clearly indicated in the title or abstract that a classification or grading system related to adjacent segment degeneration or disease was proposed; full-text articles were then reviewed to determine whether such a system had been developed. Finally, any classification systems identified from KQ 3 were included in KQ 1a.

We next sought to identify severity measures of disc degeneration that are used in definitions of “ASD” in the published literature (KQ 1b). This uses disc degeneration as a surrogate measure of ASP, realizing that ASP encompasses a full spectrum of disorders. To do this, we utilized the list of degenerative severity measures included in the AOSpine publication Spine Classifications and Severity Measures.10 A PubMed search was conducted that combined terms for each severity measure with terms related to adjacent segments. The articles identified from this search were included for full-text review if they clearly indicated in the title or abstract that adjacent segment degeneration or disease was evaluated; full-text articles were then reviewed to determine whether the severity measure of interest was used in the study's definition of adjacent segment degeneration. As for KQ 1a, any additional classification systems of disc degeneration identified in KQ 3 were added to the results for KQ 1b.

For KQ 2, we determined whether the severity measures that were identified as being used in published definitions of ASD had been tested for predictive validity and/or reliability in previous fusion patients. A PubMed search was conducted that combined terms related to each severity measure with those related to reliability or validity. Articles that clearly indicated in the title or abstract that validity or reliability evaluated in patients with ASD were included for full-text review; full-text articles were then reviewed to determine whether the predictive validity or reliability of the severity measure of interest was evaluated in patients with ASD. For all searches, we limited our results to humans and to articles published in the English language and included studies of adjacent segment degeneration or disease of adult patients with a history of spinal pathology (including various types of degenerative disease, trauma, deformity, fracture, axial spine pain, radiculopathy, cauda equina syndrome, or neurological dysfunction) as described in Table 1. Articles were excluded if patients were younger than 18 years of age or being treated for cancer or an infection. Other exclusions included case reports or reviews. Full texts of potential articles meeting the inclusion criteria by both methods were reviewed by 2 independent investigators (RH, AR) to obtain the final collection of included studies (Figure 1).

Figure 1

Figure 1

TABLE 1

TABLE 1

For KQ 3, we compiled the definitions of adjacent segment disease or degeneration (or related pathologies at the adjacent segment) as reported by all studies included in the other systematic reviews from this focus issue.

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RESULTS

KQ 1a: Formal Classification or Diagnostic Systems of ASD

Our PubMed search did not yield any formal comprehensive classification or diagnostic systems of either cervical or thoracolumbar or clinically symptomatic ASD. However, we did identify 2 ASD classification systems, both cervical, from the studies included in KQ 3: the radiographical grading of degenerative changes at adjacent levels severity system by Hilibrand et al,7 and Park et al's11 adjacent level ossification severity grading system.

Hilibrand et al7 created the radiographical grading system of degenerative changes at adjacent levels. This system was originally developed as part of a retrospective study that examined the progression of symptomatic ASD after anterior cervical arthrodesis for degenerative spondylosis and radiculopathy or myelopathy. The grading system allowed the authors to qualitatively grade the severity of disc degeneration at the adjacent level based on evidence from radiographs, magnetic resonance imaging, and computed tomography. Grades were based on evidence of disc space narrowing and/or osteophyte development on plain radiographs; signal changes in the disc space; and/or disc herniation with or without nerve root compression on magnetic resonance imaging, computed tomography, or myelography. Grades ranged from grade 1 (no disease) to 4 (severe disease) (Table 2).

TABLE 2

TABLE 2

Park et al's11 classification system of adjacent-level ossification was first described as part of a retrospective cohort study. Patients who had achieved solid fusion after cervical arthrodesis were evaluated for ossification at both disc spaces adjacent to the index level using the proposed grading system. Radiographical evidence of ossification was based on plain radiographs, and graded for severity on a 4-point scale that ranged from grade 0 (no ossification) to 3 (complete bridging) (Table 3).

TABLE 3

TABLE 3

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KQ 1b: Formal Classification or Diagnostic Systems of Disc Degeneration Used to Diagnose or Define ASP

Next, we sought to identify severity measures of disc degeneration that are being used in the published scientific literature to define or diagnose ASD. To this end, we conducted a PubMed search to identify studies that used any of the following 24 degenerative severity measures (as obtained from the AOSpine book Spine Classifications and Severity Measures (chapters 5.4.1 and 5.4.2)10 to define or diagnose adjacent segment disease or degeneration: Casey myelopathy disability index; Cooper Scale; Harsh Scale; Herdman European Myelopathy Score; Hukuda Japanese Orthopedic Association (JOA) scale; Muhle cervical spondylotic myelopathy classification scale; Nurick Scale; Yukawa classification of increased signal intensity; Adams Stages of disc degeneration; Carragee lumbar disc herniation classification; Ghiselli University of California Los Angeles (UCLA) grading system for intervertebral space degeneration; Kellgren and Lawrence osteoarthritis severity grade; Kettler cervical spine radiographical grading system; Kirkaldy-Willis degenerative cascade of spine disease; Lane osteoarthritis severity grade; Mirza Harborview disc disease severity score; Modic changes; Pathria facet joint disease severity grade; Pfirrmann magenetic resonance classification of lumbar intervertebral disc degeneration; Thalgott classification of lumbar degenerative disc disease; Thompson intervertebral disc severity grading system; Weiner radiographical scoring system for osteoarthritis of the lumbar spine; Weishaupt lumbar facet joint disease severity grade; and Wilke lumbar spine radiographical grading system.

From this search, we identified 4 studies that used the UCLA grading system, 3 that utilized the JOA scale, 1 that employed the Kellgren and Lawrence system, 2 that used Modic changes, and 1 that utilized Weiner radiographical scoring system. No studies were identified that used any of the other 19 degenerative severity measures listed earlier. Furthermore, we did not identify any additional severity measures of disc degeneration that were used to define ASD by the studies included in this focus issue (as described in KQ 3 (see Supplemental Table 5). All of the severity measures of disc degeneration that were identified from KQ 3 overlapped with those listed earlier: ASD was defined using the Kellgren and Lawrence osteoarthritis severity grade by 1 study, the Weiner radiographical scoring system for osteoarthritis of the lumbar spine by 4 studies, and the Ghiselli UCLA grading system for intervertebral space degeneration by 2 studies; the Park ossification grading system was used by 5 studies; and the Hilibrand criteria was employed by 4 studies. All of these severity measures from KQ 1b were lumbar, although the search was not restricted to lumbar disease. The total number of studies identified from KQs 1a and 3 that employed each of these severity measures are summarized in Figure 2.

Figure 2

Figure 2

In summary, for KQ 1, we have identified the following severity measures used to define or diagnose adjacent segment disease or degeneration in the published literature: 1 severity measure of cervical ASD (Hilibrand), 1 severity measure of cervical adjacent segment heterotopic ossification (Park), and 5 severity measures of lumbar disc degeneration (UCLA, Weiner, JOA, Kellgren/Lawrence, and Modic changes).

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KQ 2: Predictive Validity and Reliability of Classification or Severity Measures Used to Diagnose ASP

We conducted a literature search to determine whether any of the identified classification systems or severity measures used in the literature to diagnose ASD have been tested for predictive validity or reliability in previous fusion patients. No studies evaluating the predictive validity or reliability of any of the following severity measures were identified: radiographical grading system of degenerative changes at adjacent levels by Hilibrand et al7; classification system of adjacent-level ossification by Park; JOA scale; Modic changes; UCLA grading system; or Weiner radiographical scoring system.

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KQ 3: Definitions of Adjacent Segment Disease or Degeneration Used in the Studies Included in the Systematic Reviews of This Focus Issue

The purpose of this KQ was to provide a snapshot of how studies in the peer-reviewed literature define adjacent segment disease or degeneration. To do this, we included the definitions in all 94 of the primary studies included in this focus issue. Of these 94 studies, 67 reported definitions for adjacent segment disease or degeneration. The definitions are compiled in Supplemental Table 5 in the web appendix (Supplemental Digital Content 1, available at http://links.lww.com/BRS/A697), and are organized by the topics in this issue.

From these multifaceted definitions, we identified common individual components being used to define ASD, and have organized them into the 4 components considered important in severity scoring10: anatomical, biomechanical, clinical, and degree of severity components.

Criteria that fulfill the anatomical component indicate which anatomical structures are affected by the disease. We determined that of the 67 studies included in this focus issue that defined adjacent segment disease or degeneration, 67% included anatomical criteria (Figure 3). The specific criteria that were included and the frequency with which they were reported are listed in Figure 4. The most commonly utilized anatomical criteria included osteophytes (42% of studies), disc-space narrowing or loss of disc height (37% of studies), stenosis (19% of studies), “degenerative changes” (10% of studies), and disc herniation (10% of studies). The remaining criteria were reported by less than 10% of the 67 studies.

Figure 3

Figure 3

Figure 4

Figure 4

Criteria that meet the biomechanical component assess the stability of the spine or spinal segments. Of the 67 studies reporting definitions of adjacent segment disease or degeneration, 46% employed at least 1 biomechanical component in the definition (Figure 3). Details on the specific criteria and the frequency with which they were used may be found in Figure 5. The most commonly used biomechanical components included listhesis (15% of studies), instability (12% of studies), and an increase in the proximal junctional kyphosis sagittal Cobb angle (10% of studies).

Figure 5

Figure 5

The clinical component refers to criteria that indicate the patient's clinical status and includes symptoms and functional outcome measures (e.g., JOA). A total of 33% of the 67 studies included at least 1 clinical component in the definition of ASD. In this case, all definitions would pertain to symptomatic ASD, or adjacent segment disease. The individual clinical criteria are listed in Figure 6, and include new radiculopathy (15%), new back pain (10%), and new myelopathy (9% of studies) that were referable to the adjacent segment. Another commonly required clinical component of the symptomatic ASD definition was second surgery, which was reported by 9% of the studies.

Figure 6

Figure 6

Finally, the severity measure component refers to criteria that provide a distinction between levels or grades of disease severity; this component was the least commonly reported as it was included in definitions of ASP by only 25% of the studies (Figure 3). The individual severity measure and frequency of their use is documented in Figure 7. No individual severity measure was used by 10% or more of studies.

Figure 7

Figure 7

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DISCUSSION

After a thorough review of the literature, relatively little light is shed on ASP processes. Few classification systems have been proposed specifically relating to adjacent segment disease or adjacent segment degeneration. The cervical systems are unique to the cervical spine, particularly the degree of adjacent level ossification, more prevalent in anterior approaches common in the cervical spine. The lumbar systems are not unique to adjacent segment degnerative changes, but relate to disc deneration in general. Disc degneration is a common component of ASP, and sometimes serves as a surrogate for “ASD” as it is currently used, but is by no means synonomous with the full spectrum of adjacent level pathologies encountered.

We determined in KQ 1a and 1b that minimal useful “ASD” classification systems currently exist, particularly for thoracolumbar disease, where the specific component disc degeneration was used as a surrogate. In KQ 2, we determined that none of the classifications used in defining ASD had been tested for reliability or validity in this patient population.

In KQ 3, it arises from observation that no currently accepted definition of “ASD” or “adjacent segment degeneration” (or other terms mentioned earlier) exists; and therefore many definitions comprised of many anatomical, biomechanical, and clinical observations have been compiled. Similar to the redundancy and nonspecific overlapping terms of the International Classification of Diseases, ninth edition, nomenclature of many spinal diseases, this has lead to the inability to identify any given pathological process uniquely. This is most evident in Figure 4 of the appendix, where 4 of the top 5 anatomical descriptors are near-synonyms for degenerative changes of the disc. The overlapping terms “adjacent segment degeneration,” adjacent segment “disease,” “junctional stenosis,” “transfer lesion,” and others further obscure the picture. This is because multiple terms are used for the same undefined collection of nonspecific nomenclature referring to unvalidated clinical and/or radiographical findings.

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CONSENSUS STATEMENT

No recommendations regarding the use of current classification of degeneration at any segments can be made based on the basis of available literature. A new comprehensive definition for adjacent segment pathology (ASP, the now preferred terminology) has been proposed in this focus issue, which reflects the diverse pathology observed at functional spinal units adjacent to previous spinal reconstruction and balances detailed stratification with clinical utility. A comprehensive classification system is being developed through expert opinion and will require validation as well as peer review.

Strength of Statement: Strong

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Key Points

  • Currently, terms such as adjacent segment degeneration, adjacent segment disease, junctional stenosis, transfer lesion, and other similar terms refer to a common clinical entity without a precise or agreed upon definition, pathophysiological criteria, or imaging criteria.
  • No validated comprehensive classification system for pathology at the adjacent segment currently exists in the literature.
  • In the peer-reviewed literature, terms including “adjacent segment disease” or “adjacent segment degeneration” seem to consist of multiple pathological components observed in many studies, using many overlapping terms, but including intervertebral disc degeneration, segmental instability, spinal stenosis, facet arthrosis, and structural deformity including kyphosis.
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Acknowledgments

The authors thank Ms. Nancy Holmes, RN, and Chi Lam, MS, for their administrative assistance. The author P.K. contributed toward primary manuscript authorship, design and methodology, editing of Methods and Results section, managing consensus definitions, and managing deadlines and submission process; M.G.F.: design and methodology, interpretation of results, and manuscript writing and editing; R.H.: design and methodology, literature searches, assessing studies for inclusion/exclusion, analyzing data, and writing methods and results; A.R.: literature searches, assessing studies for inclusion/exclusion, analyzing data, and compiling and verifying adjacent segment definitions; D.N.: design and methodology; and M.L., P.A.A., and J.R.C.: editorial contributions and expert opinion.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.spinejournal.org).

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References

1. Deyo RA, Gray DT, Kreuter W, et al. United States trends in lumbar fusion surgery for degenerative conditions. Spine (Phila Pa 1976) 2005;30:1441–5;discussion 1446–7.
2. Deyo RA, Martin BI, Kreuter W, et al. Revision surgery following operations for lumbar stenosis. J Bone Joint Surg Am 2011;93:1979–86.
3. Deyo RA, Mirza SK. Trends and variations in the use of spine surgery. Clin Orthop Relat Res 2006;443:139–46.
4. Deyo RA, Mirza SK, Martin BI, et al. Trends, major medical complications, and charges associated with surgery for lumbar spinal stenosis in older adults. JAMA 2010;303:1259–65.
5. Medical News Today. Medicare to gain 7,000 new baby boomers per day in 2011. http://www.medicalnewstoday.com/articles/212585.php. Accessed April 27, 2012.
6. Ghiselli G, Wang JC, Bhatia NN, et al. Adjacent segment degeneration in the lumbar spine. J Bone Joint Surg Am 2004;86-A:1497–1503.
7. Hilibrand AS, Carlson GD, Palumbo MA, et al. Radiculopathy and myelopathy at segments adjacent to the site of a previous anterior cervical arthrodesis. J Bone Joint Surg Am 1999;81:519–28.
8. Sears WR, Sergides IG, Kazemi N, et al. Incidence and prevalence of surgery at segments adjacent to a previous posterior lumbar arthrodesis. Spine J 2011;11:11–20.
9. Hilibrand AS, Rand N. Degenerative lumbar stenosis: diagnosis and management. J Am Acad Orthop Surg 1999;7:239–49.
10. Chapman JR, Dettori JR, Norvell DC, et al., eds. Spine Classifications and Severity Measures. Dubendorf, Switzerland: AO Publishing; 2009.
11. Park JB, Cho YS, Riew KD. Development of adjacent-level ossification in patients with an anterior cervical plate. J Bone Joint Surg Am 2005;87:558–63.
Keywords:

adjacent segment disease; adjacent segment degeneration; adjacent segment pathology; junctional stenosis; cervical spine; lumbar spine; spine surgery; revision spine surgery; disc degeneration; spinal stenosis

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