quinta-feira, 30 de abril de 2015

Eur Spine J. 2006 Jun; 15(6): 705–718.
Published online 2005 Sep 20. doi:  10.1007/s00586-005-0954-y
PMCID: PMC3489462

Review of existing grading systems for cervical or lumbar disc and facet joint degeneration

Purpose

Degeneration of the spine is a very common phenomenon. The morphological changes occurring during degeneration have often been described macroscopically [], histologically [,], and using many different imaging techniques such as plain radiography [,], discography [], computed tomography [], or magnetic resonance imaging [,]. If these techniques have to be compared with each other in their ability to depict degeneration, grading systems are needed. Degeneration also has to be graded to investigate the relationship between morphology and functional parameters such as instability or intradiscal pressure, or to assess the correlation between different morphological changes. To answer whether disc degeneration causes facet joint degeneration also requires grading systems. Thus, grading systems for disc and facet joint degeneration are useful or even needed to answer a vide variety of different questions. It is therefore not surprising that more and more grading systems are reported in the literature.
The aim of this literature review was to collect, sort and evaluate all grading systems for cervical and lumbar disc and facet joint degeneration, which are accessible from the MEDLINE database.

Materials and methods

Literature search

A MEDLINE search was conducted via PubMed using various combinations of the following key words: degeneration, ageing, classification, grade, cervical spine, lumbar spine, intervertebral disc, and facet joint. Once a new grading system was found, the “related articles” option of PubMed was used to further expand the search. All extracted articles were reviewed and those selected with own grading systems for cervical or lumbar disc or facet joint degeneration. Even though this search was carried out thoroughly, it may be not complete.
According to the grading method, the selected articles were then assigned to one of the following subgroups: macroscopic anatomy, histology, plain radiography, computed tomography, magnetic resonance imaging, or discography if disc degeneration was graded, or to macroscopic anatomy, histology, plain radiography, conventional tomography, computed tomography, or magnetic resonance imaging if facet joint degeneration was graded.

Evaluation of grading systems

The evaluation of the grading systems was divided into two steps. In the first step, they were checked for reliability tests. Focus was put on the interobserver reliability, which is generally somewhat lower than the intraobserver reliability. To assess the reliability either Kappa [] or Intraclass Correlation Coefficients (ICC) [] have to be determined. According to the criteria published by Landis and Koch [], a Kappa of <0.00 can be interpreted as poor agreement, 0.00–0.20 as slight agreement, 0.21–0.40 as fair agreement, 0.41–0.60 as moderate agreement, 0.61–0.80 as substantial agreement, and >0.81 as almost perfect agreement. Based on this classification, we defined own criteria for recommendation: a grading system for cervical or lumbar disc degeneration was recommended only if Kappa or ICC was >0.60 (at least substantial agreement). Since the assessment of facet joint degeneration was assumed to be more difficult than that of the disc, the facet joint grading systems were recommended already at Kappa or ICC>0.40 (at least moderate agreement). Articles describing linear correlation coefficients instead of Kappa or ICC did not meet our criteria for recommendation since such correlation coefficients only reflect how strong the linear relationship but not how strong the agreement between two measurements is. If, for example, observer 1 would always grade half as high as observer 2, the linear correlation would be perfect but the agreement very low.
In the second step, all statistically recommended grading systems were additionally evaluated with respect to their clinical feasibility, clinical relevance and academic value.

Results

MEDLINE search revealed 32 articles describing 42 different grading systems for cervical or lumbar disc or facet joint degeneration. Thirty of these were applied to the lumbar spine, ten to the cervical spine and two to both spinal regions (Tables 1,3,3,5,5,77).
Table 1
Publications with own grading systems for lumbar disc degeneration (see Results). Chronological order within each subchapter
Table 3
Publications with own grading systems for cervical disc degeneration (see Results). Chronological order within each subchapter
Table 5
Publications with own grading systems for lumbar facet joint degeneration (see Results). Chronological order within each subchapter
Table 7
Publications with own grading systems for cervical facet joint degeneration (see Results). Chronological order within each subchapter
The design of the grading systems varied considerably:
  • Beginning of the scale: 37 grading systems were beginning with the normal, not degenerated state [] while five grading systems were starting with the lowest degree of degeneration [].
  • Nomenclature of grades: In 35 grading systems numerical grades such as grade 0, 1, 2, ... or category I, II, III ... [,] and in seven systems terms such as “normal”, “mild”, “moderate”, or “severe” were used [,].
  • Nomenclature for the normal, not degenerated state: If the scale was beginning with the normal, not degenerated state, this state was assigned to “grade 0” (15 grading systems [,]), to “grade 1” (15 grading systems []), or to a linguistic term such as “normal” or “not degenerated” (six grading systems: []).
  • Number of grades: A 5-grade scale was used in six systems [], a 4-grade scale in 24 [], a 3-grade scale in eight [,] and a 2-grade scale in three systems []. A score instead of distinct grades was used in one grading system [].
  • Structure: In 25 grading systems a certain combination of several morphological changes was assigned to each grade [], in four others this list was divided into several subgroups such as “annulus”, “nucleus”, “endplates” for the disc or “cartilage”, “subchondral bone”, “margins” for the facet joints []. In seven grading systems each feature of degeneration was graded separately and either summed up to a summary grade [] or not [].

Grading systems for lumbar disc degeneration

Twenty-two different grading systems for lumbar disc degeneration were found (Table 1), including five for macroscopic anatomy, three for histology, six for plain radiography, five for magnetic resonance imaging, and three for discography. A grading system based on the computed tomography scans was not found probably because this imaging technique is not suitable to depict changes within the disc.
Interobserver reliability tests were found only for five grading systems (Table 2). Out of these five systems only those described by Thompson et al. [] (Table 10), Boos et al. [] (except for endplate variable “cells”) (Table 11), Lane et al. [] (except for sclerosis) (Table 13), and Pfirrmann et al. [] (Table 14) had substantial to almost perfect agreement and thus fulfilled our criteria for recommendation. Not recommended is the grading system of Madan et al. [] since the most interobserver Kappa Coefficients were below 0.60. The reliability of the grading system of Gries et al. [] and Berlemann et al. [] could not be evaluated since Spearman’s correlation coefficients were determined instead of Kappa or Intraclass Correlation Coefficients [].
Table 2
Reliability of grading systems for lumbar disc degeneration assessed in terms of Kappa or Intraclass Correlation Coefficients. Same order as in Table Table11
Table 10
Macroscopic grading of lumbar disc degeneration on sagittal sections proposed by Thompson et al. []
Table 11
Histologic grading of lumbar disc degeneration on sagittal paraffin sections stained with haematoxylin and eosin, Masson–Goldner and Alcian blue-PAS proposed by Boos et al. []
Table 13
Radiographic grading of lumbar disc degeneration on lateral views described by Lane et al. 1993 []
Table 14
Grading of lumbar disc degeneration on T2-weighted sagittal MRI-scans proposed by Pfirrmann et al. []
The clinical feasibility of the four statistically recommended grading systems of Thompson et al. [] (Table 10), Boos et al. [] (Table 11), Lane et al. [] (Table 13) and Pfirrmann et al. [] (Table 14) varies considerably: it is the highest for the grading system of Lane et al. since the only material needed are lateral radiographs and the system itself has a clear structure and can very easily be applied. The grading system of Pfirrmann et al. also has a high clinical feasibility, however, magnetic resonance images are needed and some more time is needed to arrive at the result. The clinical relevance, however, is higher for the grading system of Pfirrmann et al. than for that of Lane et al. since, on MRI images, the disc itself can directly be assessed, whereas on radiographs, only bony structures are assessable. The grading systems of Thompson et al. [] and Boos et al. [], in contrast, have more academic than clinical value since both systems can not be applied on patients. However, both of them are based on the detailed morphological studies, allow an in depth evaluation of the disc and are therefore valuable tools to grade disc degeneration in vitro.
Besides these four statistically recommended grading systems, another three are of special interest: the macroscopic grading system of Nachemson [] (Table 9), the radiographic system of Mimura et al. [] (Table 12) and the discographic system of Adams et al. [] (Table 15). Nachemson was one of the first to grade disc degeneration macroscopically. His grading system has often been used in the past. Mimura et al. were the first who tried to develop a more objective grading system. It is more based on numbers such as the percentage decrease in disc height than on subjective terms such as “mild”, “moderate”, or “severe” . Adams et al. finally need to be mentioned since they count among the first to describe the relationship between the distribution of fluid injected into the disc and disc degeneration.
Table 9
Macroscopic grading of lumbar disc degeneration on transverse sections described by Nachemson 1960 []
Table 12
Radiographic grading of lumbar disc degeneration on lateral and antero-posterior views described by Mimura et al. []
Table 15
Discographic grading of lumbar disc degeneration in the sagittal plane proposed by Adams et al. []

Grading systems for cervical disc degeneration

To grade cervical disc degeneration ten systems were found (Table 3), two based on macroscopic anatomy, four using plain radiography, two using magnetic resonance imaging and two using discography. No histological or computed tomography grading systems were found.
Interobserver reliability tests were found only for the grading system of Kellgren et al. [] (Tables 4,16).16). Since the Kappa Coefficient was 0.71, this grading system fulfilled our criteria for recommendation.
Table 4
Reliability of grading systems for cervical disc degeneration assessed in terms of Kappa or Intraclass Correlation Coefficients
Table 16
Radiographic grading of cervical disc degeneration on lateral views described by Kellgren et al. []
From a clinical point of view this system has a good feasibility since it is based on the lateral radiographs and can easily be applied. In contrast, its clinical relevance is somewhat lower since the discs can only indirectly be assessed in terms of reactive changes of the surrounding bone and a loss of disc space height.

Grading systems for lumbar facet joint degeneration

Twelve grading systems for lumbar facet joint degeneration were found via MEDLINE (Table 5). These systems were either based on the macroscopic anatomy, histology, plain radiography, conventional tomography, computed tomography, or magnetic resonance imaging.
Interobserver reliability tests were found for five of these twelve grading systems (Table 6). As expected, the Kappa or Intraclass Correlation Coefficients were generally lower for the facet joints when compared to the intervertebral discs. Thus, only three grading systems fulfilled the criteria for recommendation, even though the threshold was lower than for the discs: Pathria et al. [] (computed tomography only) (Table 17) and Weishaupt et al. [] (computed tomography and magnetic resonance imaging) (Table 18). The Kappa Coefficients of the grading systems described by Pathria et al. [] for plain radiography, and Coste et al. [] were below 0.40 and should therefore not be used. The reliability of the grading systems of Gries et al. [] and Kellgren and Lawrence [] could not be assessed since linear correlation coefficients were reported instead of Kappa or ICC.
Table 6
Reliability of grading systems for lumbar facet joint degeneration assessed in terms of Kappa or Intraclass Correlation Coefficients. Same order as in Table Table55
Table 17
Grading of lumbar facet joint degeneration on oblique conventional radiographs and CT scans described by Pathria et al. []
Table 18
Grading of lumbar facet joint degeneration using computed tomography and magnetic resonance imaging described by Weishaupt et al. []
From a clinical point of view the statistically recommended grading systems of Pathria et al. [] (Table 17) and Weishaupt et al. [] (Table 18) are both feasible and relevant since they are based CT-scans or magnetic resonance images. In contrast, from an academic point of view, systems such as those of Tanno et al. [] or Gries et al. [] could be of interest since they allow to assess facet joint degeneration in vitro either by macroscopic or histologic inspection. However, these systems have not yet been tested for reliability.

Grading systems for cervical facet joint degeneration

Cervical facet joint degeneration was only graded in four articles (Table 7). One of these four grading systems was based on the macroscopic anatomy, and three on plain radiography. No histologic grading system and no systems using conventional tomography, computed tomography or magnetic resonance imaging were found.
The interobserver reliability of the grading system of Kellgren et al. [] (Table 19) was only one fulfilling the criteria for recommendation (Table 8). The system described by Kellgren and Lawrence [] was only tested for linear correlation. Thus, its reliability still needs to be determined.
Table 8
Reliability of grading systems for cervical facet joint degeneration assessed in terms of Kappa or Intraclass Correlation Coefficients
Table 19
Radiographic grading of cervical facet joint degeneration on lateral views described by Kellgren et al. []
From a clinical point of view the recommended grading system of Kellgren et al. [] is feasible since only lateral radiographs are needed.

Discussion

Forty-two different grading systems for cervical and lumbar disc and facet joint degeneration were accessible from the MEDLINE database. This high number is not astonishing since grading systems are needed to answer a vide variety of different questions. Several grading systems were for example used to investigate the correlation between morphology and flexibility, intradiscal pressure, or pain []. Others were needed to compare different diagnostic methods with each other [,], or to investigate the relation between the disc and facet joint degeneration [].
The majority of all 42 grading systems were used for the lumbar but only few for the cervical spine. Histologic grading systems, for example, were only found for the lumbar but not for the cervical spine. This also applies to grading systems for facet joint degeneration using the conventional tomography, computed tomography or magnetic resonance imaging. Thus, despite of their high number, new grading systems may still be needed especially for the cervical spine.
Regardless of the spinal region the grading systems were belonging to, the variability of their design was very high: Some systems started with the normal, not degenerated state, others with the lowest degree of degeneration; some assigned the not degenerated state to “grade 0”, others to “grade 1”; some were using a 5-grade scale, others a 4-grade, 3-grade, or 2-grade scale; some assigned linguistic terms such as “normal”, “mild”, “severe” to each grade, some others numerical values (grade 0, grade 1, grade 2, ...). These and several other variations make comparisons difficult and may easily lead to confusion. We would therefore recommend to define certain standards. Whether to start with “grade 0” or “grade 1” or with the not degenerated or the least degenerated state and whether to use linguistic terms or numerical values to grade degeneration could easily be standardised. Our suggestion would be to begin the scale with the not degenerated state and to assign this state to “grade 0”. This is what many authors already did. For the number of grades, however, it is critical to define a standard since this number should individually be adapted to the purpose of the study and the number of discs or facet joints, which have to be graded. A small number of discs or facet joints should be divided into less degrees of degeneration than a large number since otherwise, the number of individual discs or facet joints in each group of degeneration may become too small for further evaluation. Furthermore, the method used for grading also needs to be considered since most methods have a limited resolution and only cover certain but not all structures of the discs or facet joints. Thus, if the number of discs or facet joints is small and the method does not allow a detailed inspection of all structures such as plain radiography, the use of only three or four degrees of degeneration can be recommended. If, in contrast, the number of discs or facet joints is high and methods such as histology or macroscopy are used, which allow an in depth inspection of all tissues, up to five degrees of degeneration can be recommended. However, in general less than three grades should not be used since otherwise discs or facet joints with a wide variety of different appearances would all be mixed together within one and the same degree of degeneration. Sometimes it might even be advantageous not to report an overall degree of degeneration but rather the appearance of the different structures individually, because otherwise details concerning these individual structures might get lost.
Reliability is one of the most important characteristics of a grading system. Intra- and interobserver reliability can be measured in terms of Kappa [] or ICC []. Unfortunately, only few of all reviewed grading systems were tested for reliability. Out of these, nine grading systems fulfilled our criteria for recommendation (Kappa or ICC>0.60 for discs and >0.40 for facet joints) but one for lumbar disc and two for lumbar facet joint degeneration did not (Tables 2,4,4,6,6,8)8) []. These results indicate that grading systems should always be tested for reliability before use. Thresholds for Kappa or ICC might help to decide whether to use or not to use a tested system. General thresholds such as ours are suitable, if, for example, a general comparison between several grading systems is needed. However, if a specific grading system is planned to be used, the thresholds need to be adjusted to the respective purpose of the study and to the degree of experience and training of the observers, who will use the system and who had used it to determine its reliability. The thresholds should also be modified if templates will be or were available and if the observers were involved in the development of the grading system.

Conclusions and recommendations

  • Many different systems to grade lumbar disc or facet joint degeneration were accessible from the MEDLINE database. For the cervical spine, this number was much smaller.
  • Missing standards concerning the design of the grading systems make comparisons difficult and may easily lead to confusion. We would therefore recommend to define certain standards. Our suggestion would be to use a scale of three to five grades, to begin the scale with the not degenerated state and to assign this state to “grade 0”.
  • From a statistical point of view, the following nine of all 42 reviewed grading systems can be recommended for use since their Kappa or ICC for interobserver reliability were >0.60 (discs) or >0.40 (facet joints):
    1. Thompson et al. []: lumbar disc, macroscopic anatomy (Table 10)
    2. Boos et al. []: lumbar disc, histology (except for endplate variable “cells”) (Table 11)
    3. Lane et al. []: lumbar disc, plain radiography (except for sclerosis) (Table 13)
    4. Pfirrmann et al. []: lumbar disc, magnetic resonance imaging (Table 14)
    5. Kellgren et al. 1963: cervical disc, plain radiography (Table 16)
    6. Pathria et al. []: lumbar facet joints, computed tomography (Table 17)
    7. Weishaupt et al. []: lumbar facet joints, computed tomography (Table 18)
    8. Weishaupt et al. []: lumbar facet joints, magnetic resonance imaging (Table 18)
    9. Kellgren et al. 1963: cervical facet joints, plain radiography (Table 19)
  • The interobserver reliability of the following three grading systems was ≤0.60 (discs) or ≤0.40 (facet joints). These systems are therefore not recommended for use:
    1. Madan et al. []: lumbar disc, plain radiography
    2. Pathria et al. []: lumbar facet joints, plain radiography
    3. Coste et al. []: lumbar facet joint degeneration, computed tomography
  • For all other grading systems our criteria for recommendation were not applicable since they were not tested for reliability. Since these systems could be more or less reliable than those recommended above, they should at least be tested for interobserver agreement before use.

Acknowledgements

The authors would specially like to thank the Deutsche Arthrose-Hilfe e.V. and the German Research Council (DFG, WI 1352/6-1) for financial support.

Appendix

Grading systems for lumbar disc degeneration
Macroscopic anatomy
Histology
Plain radiography
Magnetic resonance imaging
Discography
Grading systems for cervical disc degeneration
Plain radiography
Grading systems for lumbar facet joint degeneration
Computed tomography
Magnetic resonance imaging
Grading systems for cervical facet joint degeneration
Plain radiography

Footnotes

An erratum to this article can be found at http://dx.doi.org/10.1007/s00586-006-1077-9

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